Textbook of Clinical Parasitology in Dogs and Cats (VetBooks - Ir)
Textbook of Clinical Parasitology in Dogs and Cats (VetBooks - Ir)
Textbook of Clinical Parasitology in Dogs and Cats (VetBooks - Ir)
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Clinical Parasitology
in dogs and cats
Frédéric Beugnet
Lénaïg Halos
Jacques Guillot
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English edition:
Textbook of clinical parasitology in dogs and cats
Copyright © 2018 Frédéric Beugnet, Lénaïg Halos and Jacques Guillot
Illustrator:
Jacob Gragera Artal
ISBN: 978-2-9550805-2-8
EAN: 9782955080528
Disclaimer:
Veterinary science is constantly evolving, as are pharmacology and the other sciences.
It is therefore the responsibility of the veterinarian to determine and verify the dosage, the
method of administration, the duration of treatment and any possible contraindications to
the treatments given to each individual patient, based on his or her professional experi-
ence. Neither the publisher nor the authors can be held liable for any damage or harm
caused to people, animals or property resulting from the correct or incorrect application of
the information contained in this book.
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Textbook of
Clinical Parasitology
in dogs and cats
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ACKNOWLEDGEMENTS
The authors would like to thank:
- Danielle Craig and Chef du Monde agency for their assistance with English writing and
corrections.
- The Parasitology Departments of the French Veterinary Schools and Merial R&D for pro-
viding numerous parasite pictures.
- Oleg Mediannikov who provided the picture of Amblyomma tick infesting dog used for the
cover.
- Óscar Deza and the team from Grupo Asís, for all the artwork and design on the book, as
well as his patience while waiting for us to send material over the last 3 years.
- Boehringer Ingelheim Animal Health Management for their interest in parasitology and
science, and for supporting our ambition of producing educational materials, such as this
textbook.
- The co-authors who contributed to the first editions of this textbook: Gilles Bourdoiseau and
Hoan Dang.
Finally, we would like to thank all the veterinary parasitologists who shared their knowledge of
specific parasites and helped us to complete this book: thanks to Jody Gookin (trichomonosis),
Adam Birkenheuer (cytauxzoonosis), Banie Penzhorn (babesiosis), and Donato Traversa (feline
lungworm).
VIII
TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS
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AUTHORS
Prof. Frédéric Beugnet
DVM, PhD, Agrégé en Parasitologie et Maladies Parasitaires, Dip. EVPC
Frédéric Beugnet graduated as a Doctor of Veterinary Medicine from the National Veterinary
School of Lyon (France) in 1991. He holds a PhD in Parasitology, is a Diplomate of the Euro-
pean Veterinary Parasitology College (EVPC), and is also Agrégé en Parasitologie et Maladies
Parasitaires and holds an HDR (Habilitation à Diriger les Recherches). He spent more than 10
years teaching and researching at university before joining Merial and still gives university lec-
tures. He specialises in veterinary parasitology for dogs, cats and horses, as well as antiparasitic
drugs, mathematical modelling of flea and tick dynamics, and epidemiology of vector-borne
diseases in pets and horses. Frédéric is Head of the Global Technical Services for Parasitology
and Parasiticides at Merial (now Boehringer Ingelheim Animal Health).
PREFACE
This book is the second edition of a group of two volumes edited in 2005, and addresses clin-
ical aspects of canine and feline parasitoses.
This book concentrates on the most important general information and does not discuss tax-
onomy, morphology or biology in any great detail.
The pictures in this book have been sourced from the French Veterinary Schools, other Europe-
an veterinary faculties, and the authors. Not all photos are of the same size or proportions due
to the variation in microscopy equipment used, processing techniques, magnification, zoom, etc.
The life cycles are adapted and inspired from an original version published by Doug Carithers
and Guadalupe Miró in Pet Owner Educational Atlas. Parasites, Ed. Servet, 2012.
The authors focused on Parasitology sensu stricto (helminthology, protozoology and ento-
mo-acarology), so fungal infections are not included in this book.
This book has been developed specifically for veterinarians and veterinary students so that they
may rapidly access information about infestation, clinical studies, diagnosis, therapy, preven-
tion and zoonotic risks.
The authors
Preface / Specific note from the authors XI
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In line with the World Association for the Advancement of Veterinary Parasitology (WAAVP),
we decided to follow the international recommendations for the Standardised Nomenclature
of Animal Parasitic Diseases. Consistency in the use of terminology is an important require-
ment for clear communication in any field of science. In contrast to the basically homogene-
ous terminology of bacterial and fungal diseases, different names are being used with variable
frequency in the nomenclature of parasitic diseases to denote the same disease entity, such as
leishmaniasis and leishmaniosis, dirofilariasis and dirofilariosis, toxocariasis and toxocarosis,
etc. To address this issue, the Standardised Nomenclature of Parasitic Diseases (SNOPAD)
guidelines were published in 1988. Their proposal was endorsed in 1990 by the World Federa-
tion of Parasitologists for all parasitic diseases, including human parasitoses.
• When disease names are formed from the taxonomic name of the parasite, the suffixes
“-asis” and “-iasis” used to describe a disease or infestation should be discontinued,
and only the suffix “-osis” (“-oses” in the plural) should be used.
• Another major source of confusion in the nomenclature originates from variations
in the stems of words which are formed either from the nominative genus (e.g., tryp-
anosomosis, hypodermosis) or from the family name (e.g., trypanosomatosis, hypo-
dermatosis). SNOPAD offers a simple solution for uniform usage by proposing that
the suffix “-osis” be added to the stem of the parasite taxon, which is usually formed
from the nominative case of the taxon with the last one or two letters removed (e.g.,
Toxocara/toxocarosis; Dirofilaria/dirofilariosis; Aelurostrongylus/aelurostrongylosis;
Isospora/isosporosis; Leishmania/leishmaniosis, etc.).
• When taxa end with -x in the nominative, the stem is formed from the genitive and the
disease name is derived from this stem (e.g., Pulex/pulicosis).
• In some cases, the disease name is formed by adding the suffix “-osis” to the full name
of the parasite taxon (e.g., Hepatozoon/hepatozoonosis).
As a rule, all parasitic diseases are denominated using the suffix “-osis” or “-iosis” in this book.
Finally, there is some debate between the words “infection” and “infestation”: we decided to fol-
low the zoological definition and to split based on the taxonomy; “infection” applies to viruses,
bacteria, protozoa and fungi, while “infestation” applies to multicellular organisms, i.e., Metazoa.
TABLE OF CONTENTS
GASTROINTESTINAL PARASITOSES 1
Cestodoses .......................... 35
Dipylidiosis ........................................ 35
Mesocestoidosis ............................... 41
Taenioses sensu stricto ..................... 43
Echinococcoses ................................ 49
Diphyllobothriosis
and spirometrosis ............................. 56
Table of contents XIII
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Entomoses ................................................. 209
Flea infestation ........................................................................ 210
Lice infestation ......................................................................... 221
Myiasis ..................................................................................... 226
Flying insect bites .................................................................... 230
Acarioses ................................................... 235
Tick infestation ......................................................................... 236
Otodectic mange ..................................................................... 254
Sarcoptic mange ..................................................................... 258
Notoedric mange ..................................................................... 263
Cheyletiellosis .......................................................................... 265
Canine demodicosis ................................................................ 268
Feline demodicosis ................................................................. 275
Trombiculosis ......................................................................... 278
Straelensiosis ........................................................................... 281
Lynxacarosis ............................................................................ 284
Dermanyssus infestation ......................................................... 286
Table of contents XV
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General principles ...................................... 290
Coproscopy ............................................... 291
General comments .................................................................. 291
Macroscopic examination ........................................................ 292
Microscopic techniques .......................................................... 292
Discussion ............................................................................... 309
Identification of parasite eggs, cysts and larvae in dogs ......... 310
Identification of parasite eggs, cysts and larvae in cats .......... 326
Anthelmintics ............................................. 349
Antiprotozoals ............................................ 361
Ectoparasiticides ....................................... 367
APPENDICES 381
GASTROINTESTINAL
PARASITOSES
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Oesophageal and
gastric parasitoses
TABLE OF
4 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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Ollulanosis
General comments
Ollulanus tricuspis is a nematode belonging to the order
Strongylida (superfamily Trichostrongyloidea). It is very
small in size (approximately 1 mm in length), very slender
and coiled like a watch spring at the anterior end (Fig. 1).
This parasite is found in the stomachs of wild cats and
foxes, and can occasionally be found in domestic cats.
Biology
Ollulanus is an unusual type of strongylid nematode because
0.1 mm
the female is viviparous and releases the infective third-stage
larvae (L3) into the stomach lumen. The L3 can continue Figure 1. Female Ollulanus observed in the vomit from a cat.
to develop into the immature L4, and then the adult stage, Courtesy of Michael Dryden.
GASTROINTESTINAL PARASITOSES
Spirocercosis
Figure 2. Spirocerca nodules in the aortic wall. Figure 3. Aortic Spirocerca lesions.
TABLE OF
6 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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Dogs become infested by consuming these intermediate The life cycle takes approximately 4 months. The adults
or paratenic hosts. Intermediate hosts are digested in the are located inside granulomas that measure 4–10 cm in di-
dog's stomach and release L3 larvae which burrow into the ameter, and have an opening where the females lay their
stomach wall, towards the gastroepiploic artery and the aor- eggs. This location makes it difficult for anthelmintic agents
ta. Once they reach the aorta, they travel along the aortic to reach them because such agents do not penetrate granu-
wall and then migrate to the oesophagus where they form lomatous tissue well.
granulomatous nodules in the oesophageal wall (Figs. 4–8).
D.H.
Dog, fox, wolf, jackal, coyote and wild felids
(bobcats, snow leopards and lynxes)
in in
Infective L3 larvae
rI e
.H
re-encyst in
.
viscera of P.H.
Prepatent period:
4–5 months
granulomas
2
mo
.
P.H
nth
by
sted
Egg will not hatch
s
Embryonated egg
I.H. ingests eggs
Faeces
Develops into
infective L3 larvae
and encysts in the D.H. = definitive host
I.H.
I.H. (dung beetle) I.H. = intermediate host
P.H. = paratenic host
TABLE OF
CONTENTS Oesophageal and gastric parasitoses 7
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GASTROINTESTINAL PARASITOSES
S. lupi can cause significant damage to the arteries. This Beetles or Dictyoptera insects can be intermediate hosts
parasite may cause thickening of arterial walls and fibrosis and paratenic hosts are also possible, especially rodents (e.g.,
which increases the risk of verminous aneurysm, rupture and mice, voles). Excreted eggs measure 55–60 × 36–38 µm.
internal haemorrhaging.
Figure 4. Oesophageal Spirocerca nodules. Figure 5. Spirocerca nodule inside the oesophagus.
Epidemiology Complications
Canine spirocercosis and feline spirurosis are sporadic in • Possible aortic rupture, followed by fatal internal bleeding.
temperate climates and enzootic in warm climates. Spiru- • Moderate bleeding from the aorta, causing chronic
roids which affect carnivores are mainly seen in rural envi- anaemia.
ronments because they must be ingested by an intermediate • Rupture of the oesophagus (rare).
host, usually a beetle, or a paratenic host (e.g., lizard, bird, • Development of oesophageal neoplasia: although rare in
small mammal, etc.). dogs, oesophageal neoplasms seem to be closely linked to
S. lupi infestation. These are most commonly fibrosarco-
Parasite sources mas, which often metastasise to the lungs, and the progno-
• Intermediate hosts: dung beetles (Geotrupes, Scarabeus), sis in such cases is poor.
Dictyoptera (cockroaches). • Development of hypertrophic pulmonary osteoarthropa-
• Paratenic hosts: amphibians, reptiles, birds or small thy with characteristic signs of marked hypertrophy of the
mammals. long bones, oedema in the legs and considerable locomo-
tion difficulty (Fig. 9). This syndrome, called the Cadiot
Mechanism of infestation syndrome, is characteristic of canine spirocercosis in re-
Ingestion of intermediate or paratenic hosts. gions where the parasitosis is enzootic.
Host susceptibility
Carnivores living in rural environments are more likely to
hunt paratenic hosts.
GASTROINTESTINAL PARASITOSES
• Development of nodules, 2–7 mm in diameter, contain- Control measures
ing larvae and growing to 1 to 2 cm in size. Treatment
• Widely dispersed thickening of the tunica intima and Their location makes it difficult for anthelmintic products to
tunica media, which may weaken the arterial wall and reach the nodules containing Spirocera because these prod-
result in aneurysm and potential rupture. ucts do not circulate well in this kind of tissue.
Subcutaneous injection of 10 mg/kg nitroxynil is effective.
Diagnosis It binds to plasma proteins and is active against the majority
In regions where the parasite is enzootic, clinical suspicion of haematophagous nematodes.
must arise when dogs present with chronic gastric disorders Topical administration of 2.5 mg/kg moxidectin is also ef-
and and their general condition has changed. Endoscopic ex- fective. 0.5 mg/kg milbemycin oxime administered orally at
amination and visualization of the pathognomonic fibrous weekly intervals for one month has also proven to be active.
nodules will confirm diagnosis. Endoscopic examination
can also be used to follow the progress of lesions following Prevention
treatment: nodules should regress and become whitish in col- A monthly topical administration of 2.5 mg/kg moxidectin
our (they are usually pinkish-red to start with). This demon- prevents infestation effectively.
strates a reduction in parasite viability. Faecal examination Oral milbemycin oxime, administered monthly at
is possible, but at this stage, the eggs are often only found 0.5 mg/kg, has been shown to prevent infestations in some
in small quantities and are laid irregularly (Fig. 10). Faecal studies.
flotation in a saturated sugar solution seems to be the most
sensitive test.
20 μm
Other gastrointestinal
spiruroses *
General comments
Dogs and cats can become infested with several species of Physaloptera praeputialis, which is 15–45 mm long, is
spiruroid, mostly exotic. Only Spirocerca lupi is found in found in the stomachs of domestic and wild felids. Physalop-
dogs in many countries (see Spirocercosis, page 5). Cats can tera canis infests dogs (Fig. 1).
be infested by Spirura rytipleurites. Gnathostoma spinigerum is mainly found in cats, but
Species found in hot climates belong to the genera Physa- sometimes in dogs and wild carnivores too.
loptera and Gnathostoma. Rictularia, a fox spiruroid, can
also infest other canids, including dogs. Importance
Intestinal spirurosis is usually asymptomatic in carnivores,
Geographical distribution but some species may be transmitted to humans, such as
Cases of spirurosis occur sporadically in temperate to cold G. spinigerum in the Far East, India, America and Australia.
climates around the world but they are widespread in tropi- This spiruroid causes severe visceral or cutaneous (especially
cal regions (America, the Caribbean, Asia, India, China, In- facial) larva migrans in humans.
donesia, Malaysia, Pacific Islands, Africa, Madagascar and
the island of Reunion). Feline spirurosis is frequent in North Morphology
Africa. Gnathostomosis is mainly found in Asia, while Spirura rytipleurites is 20–30 mm long and has a diameter
physalopterosis is reported in Asia and Africa, and also in of 0.6–0.8 mm.
America. Physaloptera praeputialis is 15–45 mm long. Physa-
lopteridae have a characteristic ring around their anterior
Hosts extremity.
S. rytipleurites is found in the oesophagus and stomach of Gnathostoma spinigerum is 10–30 mm long. Gnathosto-
cats. midae have a characteristic spiny dome in the cephalic region.
50 μm
*Gnathostoma spinigerum
TABLE OF
CONTENTS Oesophageal and gastric parasitoses 11
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GASTROINTESTINAL PARASITOSES
Biology Clinical signs
Adult forms of S. rytipleurites live in the wall of oesopha- • Feline spirurosis: Spirura rytipleurites is less pathogenic
gus and stomach. Adult forms of the parasites Gnathostoma than Spirocerca lupi, but gastritis can still lead to chronic
(G. spinigerum) and Physaloptera (P. praeputialis), are found vomiting, sometimes tinged with blood, and weight loss.
in the stomach or small intestine, depending on the species. Infested cats are often asymptomatic.
Their life cycles involve tissue migration, but this does not af- • Physalopterosis: often asymptomatic, but can cause chron-
fect the arteries, which means that the medical consequences ic granulomatous gastritis with vomiting in infested cats
are less serious than those of canine spirocercosis. or dogs.
Gnathostoma spinigerum lives in bloody pockets in the • Gnathostomosis: causes nodular gastritis, generally well
stomach wall, and comes into contact with the gastric con- tolerated by the final host. Necrotic hepatic lesions con-
tents via an orifice in the pocket. nected with larval migration are possible.
Intestinal
parasitoses
TABLE OF
14 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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NEMATODOSES
Ancylostomoses *
Hosts
• Dogs and other canids (A. caninum, A. braziliense, A. cey-
General comments lanicum, U. stenocephala).
Ancylostomosis is a helminth infestation caused by the pen- • Cats (A. tubaeforme, A. braziliense, A. ceylanicum).
etration or ingestion and migration to the small intestine of
Ancylostomatidae nematodes (hookworms). The clinical Geographical distribution
signs are a general loss of condition (weight loss, anaemia), Although ancylostomosis occurs worldwide, parasites of the
intestinal disorders (diarrhoea) and more rarely, skin or res- genus Ancylostoma are mainly found in warmer regions.
piratory conditions. In temperate countries, dogs are infest- Uncinaria seems to be more adapted to temperate and cold
ed by Ancylostoma caninum and Uncinaria stenocephala, regions and is thought to have originally been a parasite of
while cats are infested by Ancylostoma tubaeforme and rare- the fox.
ly, U. stenocephala. In Asia, the most important species in-
festing both dogs and cats is A. ceylanicum. These are nema- Importance
todes of the order Strongylida, suborder Ancylostomatoidea. Ancylostoma are of great medical significance because of the
Ancylostoma are small, round, slender and white in col- their pathogenic nature.
our, measuring approximately 10 mm in length. At the ante- They are of economic significance when they affect com-
rior extremity they have a buccal capsule with either hooks munities of dogs (breeding kennels, rescue shelters, hunting
(Ancylostoma) or cutting plates (Uncinaria) around its edge kennels).
(Fig. 1). Hookworms are of zoonotic significance because humans
may become infested by A. caninum, A. ceylanicum and A.
Synonyms braziliense, which can cause larva migrans. A. ceylanicum
• Hookworm infestation. (Fig. 2) is unique in that it not only causes larva migrans,
• Ancylostomosis (when caused by Ancylostoma). but can also develop into an adult worm in the intestine of
• Uncinariosis (when caused by Uncinaria). humans.
0.1 mm 0.05 mm
GASTROINTESTINAL PARASITOSES
Biology
Hookworms are parasites of the small intestine and are par- In female dogs and cats, a few larvae will continue their
tially haematophagous (especially Ancyclostoma). The fe- migration through the blood stream after leaving the lungs
males lay strongyle-type eggs which are then shed in faecal and become disseminated in various tissues and organs, as
matter and develop in the environment. Adults have a life it occurs with Toxocara. They will then encyst and remain
span of approximately 6 months. quiescent for several months or years but, if a bitch or queen
The strongyle-type eggs are oval with a thin, smooth shell is pregnant, the larvae may mobilise at birth and infest the
and they enclose one morula containing only 8 to 16 cells young through the mother’s milk. In utero infestations seem
when they are shed. They are approximately 30–40 × 55– to be rare.
75 µm in size (Figs. 3 and 4).
The eggs hatch in the environment and release a stage 1
(rhabditiform, L1) larva which, after two moults, will be-
come the stage 3 (filariform, L3) infective larva. Larval de-
velopment requires moist, warm soil at least 16 °C, and can
occur in as little as 7 days at optimum temperatures (22 °C).
Larval formation generally occurs in the environment, on
grassy soils, as it does in the parasitic strongylids of rumi-
nants and horses. It cannot occur on concrete or hard mud/
clay surfaces. Infective larvae can survive for a number of
weeks in a favourable environment.
Dogs and cats will either ingest the larvae (which fre-
quently occurs with Uncinaria), or the larvae will penetrate
the skin and migrate subcutaneously (especially Ancylos-
toma). The stage 3 larvae will then rapidly find their way
into the lymph vessels or the blood stream and migrate to
the heart and pulmonary arterioles. They then penetrate the
pulmonary alveoli, ascend the bronchial tree and are then
swallowed into the gastro-intestinal tract, where they reside
and develop into adults. The migratory cycle is similar to that
20 μm
of ascarids and the life cycle takes approximately 6 weeks to
complete. Figure 3. Ancylostoma tubaeforme egg.
50 μm
Adult worm
feeding on
intestinal
mucosa
Adult buccal
capsule hooklet
~ 2 wee
~4
we ks p
eks os
Transmammary transmission
po t ski
to puppies is the most
st i n p
ng
common route of infestation.
est enet
Transplacental transmission is
ion rati
very rare and only described Ancylostoma Uncinaria
Intestinal for A. caninum (hooks) (cutting plates)
cells
on
Faeces
ion
m n
Some larvae
ns sio
iss
on temperature
eo ran
intestines and
an l t
Epidemiology
Ancylostomosis can be contracted by all types of carnivores, encysted in their tissues and remain infective. These paraten-
but generally affects stray animals, or animals living in com- ic hosts will then infest any carnivores that eat them. L3 lar-
munities. It is often found in hunting dogs and in dogs kept vae need damp, grassy areas to survive as they do not resist
in kennels, and it is commonly seen in rural areas. dry conditions well. They are also sensitive to ordinary dis-
The source of the parasites are dog and cat carriers, and soils infectants. As with the majority of parasitic diseases, young
contaminated by stage 3 larvae. When the filariform larvae carnivores are the most susceptible and other factors, such as
are ingested by small mammals (e.g., rats, mice) they become malnutrition or fatigue (hounds), will increase susceptibility.
TABLE OF
CONTENTS Intestinal parasitoses 17
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GASTROINTESTINAL PARASITOSES
Clinical signs and lesions Control measures
• Cutaneous signs: penetration of the skin by the L3 larvae Treatment
can result in papular lesions covered with scales on the Ancylostoma are relatively sensitive to nematodicides, such
legs and ventral areas. These inflamed areas become itchy as pyrantel, benzimidazoles, emodepside, eprinomectin,
and the lesions can become infected and develop into pyo- milbemycin, moxidectin, and selamectin. In some commu-
derma. Superficial adenitis is often seen (popliteal lymph nities, populations of Uncinaria may be chemoresistant to
node, in particular). benzimidazoles. However, this phenomenon seems to be lim-
• Respiratory signs: migration of the larvae causes cough- ited, and is not comparable to the levels of resistance found in
ing and signs of pneumonia, as it does in toxocarosis in horse or ruminant strongyles.
puppies and kittens. Other signs of ancylostomosis in dogs
include loss of sense of smell (often occurring in hunting Prevention
dogs), change to the bark (to a higher pitch) and epistaxis. Regular deworming of carnivores with anthelmintics that
• Intestinal disorders: adult parasites will cause congestive have a larvicidal effect is essential to prevent ancylostomo-
haemorrhagic enteritis and sometimes, diarrhoea, which is sis. Gestating females should also be treated 15 days prior to
often abundant and haemorrhagic. giving birth.
• General disorders: the continued parasitic burden in some Environmental control may include covering mud/dirt ar-
dogs will lead to chronic weight loss, muscular atrophy eas with gravel, regularly removing faeces and cleaning con-
and development of a wasting syndrome. crete areas, and rodent control. Boiling water or disinfectants
may be used to clean at weekly intervals.
Lesions A vaccine, involving inoculation with irradiated stage 3
Congestive haemorrhagic enteritis, with worms found in the larvae was developed, providing protection for 1.5 years, but
mucosa (Fig. 5). it was abandoned for economic reasons such as cost of pro-
duction, supply challenges, and stability issues.
Diagnosis
Ancylostomosis should be considered in dogs with epistaxis, Risk to humans
associated gastrointestinal disorders and weight loss. Dif- Hookworms from dogs and cats may infest humans with a
ferential diagnosis may include other parasitic or wasting complete life cycle (A. ceylanicum) or cutaneous larva mi-
diseases, such as leishmaniosis or other helminthoses (e.g., grans after penetration through the skin (A. braziliense, A.
trichuriosis). caninum, and rarely U. stenocephala).
However, diagnosis based on clinical signs is not possi-
ble, and intestinal disorders and weight loss will only suggest
possible parasite infestation. A definitive diagnosis can only
be made by examination of faeces and identification of eggs.
Toxocaroses *
General comments
Toxocarosis is a parasitic disease caused by the presence and Roundworms are the primary parasites that can cause
development of large nematodes of the order Ascaridida, ge- growth retardation in young carnivores. Roundworm con-
nus Toxocara, in the small intestine. Dogs and cats may also trol requires hygienic measures and regular treatment of
be infested by Toxascaris leonina. breeding stock and young animals.
Roundworms (or ascarids) are the most common hel- Toxocarosis is a significant public health issue because it
minths in dogs and cats: 10–20 % of dogs and cats in ur- can infest humans when embryonated eggs of T. canis and
ban and rural areas are infested, and infestation levels are T. cati are ingested.
approximately 60 % in kennels. 20–40 % of dogs and cats
with parasitic worm burdens have Toxocara canis or Toxo- Synonyms
cara cati, 5–20 % of dogs have hookworms (Ancylostoma The infestation should be called ascarididosis after the
and Uncinaria) and 10–30 % of dogs are infested with whip- parasitic order Ascaridida.
worms (Trichuris vulpis). Due to the nature of their life cycle, The accepted terms could then be ascaridosis (for all infes-
roundworms are mainly found in young carnivores and are tations by roundworms) or toxocarosis (only for infestation
responsible for a variety of clinical signs, such as coughing, due to Toxocara).
diarrhoea, vomiting, pot-belly and abdominal pain. Subclin- The term ascaridiosis is sometimes found in the legal doc-
ical signs, such as growth retardation and fragile bones, may uments for certain dewormers (e.g., summary of product
also occur. Nevertheless, roundworms can be diagnosed in characteristics) which is totally incorrect as Ascaridia are
adults and are not restricted to young puppies or kittens. bird parasites.
5 mm 5 mm
Figure 1. Anterior end of Toxocara. Electron microscopy. Figure 2. Anterior end of Toxocara cati. Light microscopy.
GASTROINTESTINAL PARASITOSES
Morphology
Three species of roundworms infest dogs and cats: T. canis Ascarid eggs are easily identified in the faeces. Females
(dog only), T. cati (cat only) and Toxascaris leonina (dog are considered prolific, and lay spherical to subspherical eggs
and cat). measuring approximately 75–85 µm in diameter. These eggs
Infestations caused by T. canis and T. cati (Figs. 1–3) are contain a single, brown cell which does not fill the whole
by far the most significant, because of their prevalence, zo- egg. The brown shell is thick and the wall features concentric
onotic potential and serious consequences in puppies and striations (Figs. 6 and 7). The external layer of the shell is
kittens. irregular and pitted in the Toxocara genus, with a “thimble
Toxascaris leonina can infest both dogs and cats, and is like” surface, whereas the external layer of Toxascaris eggs is
usually seen in rural environments, in carnivores that hunt completely smooth (Figs. 8 and 9). The distinction is impor-
mice. The importance of the paratenic host is such that some tant since only Toxocara can infest humans.
authors suggest that it acts more like an intermediate host Eggs are seen in large numbers shortly after the adult
with a dixenous life cycle (Fig. 4). worms appear in the small intestine because the females are
Adult roundworms are found during autopsies of young highly prolific, laying approximately 200,000 eggs per day.
carnivores, or when they are shed in the faeces or vomitus
of the infected animal. The adults are 5–15 cm long and
2–3 mm in diameter, and they are large, white worms which
are easily recognisable (Fig. 5).
100 μm
Figure 3. Toxocara buccal lips. Electron microscopy. Figure 5. Toxocara canis adults.
5 mm
Biology
Ascarids are not haematophagous, but do consume large arrested by drought or wet conditions, so they can thus re-
amounts of glucose, amino-acids, vitamins, trace elements main infective to dogs and cats for 2–5 days.
and minerals, such as calcium and phosphorous. The loss of When the eggs containing the Toxocara larvae are ingest-
these nutrients may explain the bone disorders observed in ed by a young puppy or kitten (under 6 months old) they
heavily infested puppies and kittens, and the risk of convul- migrate through the intestine and eventually develop into
sive hypoglycaemic seizures. adults. The larvae can also pass through the wall of the intes-
The worms can form balls in the small intestine of young tine and travel through the lymph vessels or the bloodstream
carnivores, which leads to signs of obstruction and diarrhoea to the liver and heart. They also move through the pulmo-
or constipation. In rare cases, the gastro-intestinal tract may nary arteries to the lungs, where they leave the vessels to en-
be perforated, leading to fatal peritonitis. ter the pulmonary alveoli. Next, they travel up the bronchi to
Ascarids have a monoxenous cycle (i.e., they parasitise a the trachea, where they are swallowed and return to the in-
single host). The eggs laid in carnivores by the female worms testine where they finally become adults and mate. This ente-
are shed in the faeces and develop in the external environ- ro-pneumo-tracheo-enteral migration takes 5 weeks. Passage
ment for 3 to 4 weeks, before becoming infective (Fig. 10). through the lungs explains the respiratory signs (coughing,
They are particularly resistant and can survive at tempera- with no hyperthermia) which precede or accompany the in-
tures between -10 °C and +45 °C, and development is not testinal disorders.
40 μm 200 μm
Figure 6. Toxocara (dark) and Toxascaris eggs in dog faeces. Figure 7. Ancylostoma, Toxocara and Toxascaris eggs in dog faeces.
Coproscopy. Coproscopy.
40 μm 40 μm
Figure 8. Toxocara egg in dog faeces. Coproscopy. Figure 9. Toxascaris egg in dog faeces. Coproscopy.
TABLE OF
CONTENTS Intestinal parasitoses 21
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GASTROINTESTINAL PARASITOSES
This cycle only takes place in Toxocara, while T. le-
onina develops directly in the small intestine, without any
migration.
When embryonated eggs of Toxocara are ingest-
ed by dogs or cats, 6 months or older, the larvae migrate
to the lungs but may not penetrate the alveoli. They head
for the heart through the pulmonary veins, are distribut-
ed throughout the body in the bloodstream and will be-
come encysted in various organs while still alive. In male
50 μm
dogs, larvae die out, usually after about a year. In female
dogs, the encysted larvae remain infective for several years. Figure 10. Embryonated Toxocara egg. Flotation from sand.
D.H.
Dog
Adults
(detail of the
anterior end)
Th gs o
eg
ed rt
og he
ing P.H
es .
ts
inf
ec
Prepatent period:
tiv
ingestion, ~5 weeks
after egg ingestion
P.H. (rodents)
in
e
or
ef
sb
s
egg
4
~
P.H. ingested by a
ts i
ges
This phenomenon is progressive and depends on a number of cycle so adult worms will be present in the intestine after
factors including age, immune status and, possibly, the breed 5 weeks. Larvae that are reactivated between 15 days before
of animal. birth and 15 days after birth will either develop into adult
Toxocara canis larvae can reactivate in bitches when they worms and infest the puppies through the uterus, or via the
are on heat or before giving birth. This parasitic activity de- colostrum and milk. The larvae that infest puppies prior to
pends on the hormone cycle of the bitch and involves dormant birth will develop into adults when the puppies are 10 days
larvae which are encysted in the mammary glands, uterus or old. Larvae ingested from the colostrum or milk will migrate
muscle tissue. The larvae that are reactivated around oestrus through the puppies’ bloodstream and lungs, before develop-
will travel to the lungs and undergo the classic migratory ing into adults in the intestine.
D.H.
Cat
Th inf
e ect
or
Adult
ca iv
t in e e
(detail of the
ge gg
anterior end)
sts s
P.
H.
21 1 m
~
in the tissues
wi wi
ng ng
in ing
ge e
st sti
io on
n
of of
P. eg
H gs
.
P.H. (rodents)
s
est
. ing s
.H egg
eP
Th ctive 2–4 weeks
Non-infective egg
e
inf
Faeces
Infective egg
D.H. = definitive host
Non-infective egg P.H. = paratenic host
TABLE OF
CONTENTS Intestinal parasitoses 23
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GASTROINTESTINAL PARASITOSES
There is no in utero passage in queens, but T. cati larvae Infestation with roundworms triggers an immune re-
will infest kittens through their mother’s milk from the sec- sponse which reduces the risk of infestation in adult carni-
ond day after birth and for about 10 days thereafter. vores. However, this response is incomplete and can be lost.
If a rodent ingests an egg containing L3 larvae, it will har- Moreover, carnivores which were not infested at a young age
bour quiescent larvae in its tissues and will then act as a pa- will remain naive and fully receptive to the parasite.
ratenic host. This role is very important in ascaridosis caused
by T. leonina, but also for T. cati infestation.
D.H.
Dog and cat
D.H
or i . inge
nfe s
ste ts inf
d I. e
H. ctive
egg
s
Dir
Ind ect in
ire
ct festa
I.H. inf tion
est
(rodents) atio (egg
n ( s) ~
I.H
.) ~ 74 d
63 ays
da
ys
7–11 days in rodents
Adults
gs
e eg ues
t iv iss
infec the t
sts yst in
ge
nt in e enc
de a
Ro d larv
n s Faeces
a day
3–6
GASTROINTESTINAL PARASITOSES
Diagnosis the purchase of a breeding animal), so faecal matter must
Clinical diagnosis is easy in young animals which have just be examined and, if results are positive, the animal must be
been purchased, but it must be confirmed with tests. At the given the appropriate treatment.
end of the prepatent period, eggs are shed in large quantities Biosecurity: people who enter the dog or cat kennels or
so examination of the faeces under a microscope will usually breeding facility may bring infective elements with them
reveal roundworm eggs and enable the genus (Toxocara or from outside, or carry them from one enclosure to another
Toxascaris) to be identified. (for example, on muddy shoes or boots). For this reason, one
or more footbaths should be installed between enclosures
Control measures and at the entrance to the kennels. Not many disinfectants
Toxocarosis must be controlled because of its prevalence, its are active against ascarid eggs: 3 % formalin, 2 % creosote
veterinary and economic impact on breeding facilities and mixtures, or a mixture of 3 % formalin and copper sulphate
kennels, and the risk of zoonotic transmission. Measures are at 2 %. Bleach, phenol derivatives, iodophors and amphoter-
taken in a healthy environment to avoid introducing a par- ic amino acids are not sufficiently active.
asite carrier, whereas measures in a contaminated environ-
ment aim to reduce infestation rates. Measures to be taken in a contaminated
environment
Prevention in breeding facilities General hygiene in the kennel. Parasite eggs are very resistant
and kennels in the external environment (Toxocara eggs can survive for
Measures to be taken in a healthy environment several years).
(e.g., a kennel)
The introduction of parasite carriers should be avoided when The following three measures must be put in place:
a new animal is introduced to the kennel (for instance, after • Limit contamination of the kennel environment and,
therefore, infection of the animals. Avoid overcrowding,
isolate young bitches as soon as possible post-partum and
bring them back for feeding purposes only.
• Keep the kennel environment clean:
• Surfaces made of bare earth, clay or sand should be cov-
ered in gravel. Large-particle gravel will let the eggs drop
through and develop but they will not be able to contam-
inate the dogs. Earth can be dug over to bury the eggs,
but they will not be destroyed.
• Hard surfaces (concrete, cement), kennels and cages:
these must be hosed down once or twice daily to elim-
Figure 11. Toxocarosis in a puppy. inate faecal matter and most of the parasitic elements.
A high-pressure jet is more efficient than an ordinary
hose. Scrubbing floor surfaces, including cracks and
crevices, regularly is an excellent idea (once a week or
every 10 days). This mechanical action is essential to
keep the environment clean and to prevent parasites.
• Disinfect the kennel environment: disinfection must be
preceded by cleaning and should be carried out regularly,
at least once every 2 months, depending on the degree of
parasitic infestation or other infectious problems.
GASTROINTESTINAL PARASITOSES
Strongyloidosis * (L1) when they are laid (Fig. 2). This L1 will be shed and
found in the faeces. It has a rhabditiform oesophagus and is
approximately 300 µm long.
General comments
Strongyloidosis is an enteric disease caused by nematodes of Biology
the genus Strongyloides (threadworms) penetrating the skin Threadworms are parasites of the small intestine. The ovo-
and migrating in the body of the host. The disease can cause viviparous females shed eggs containing larvae, which will
severe enteritis. The species which infests dogs, cats and hu- hatch in the soil and develop if the environment is sufficient-
mans is Strongyloides stercoralis. It causes a true zoonosis, ly damp, muddy and warm. These rhabditiform larvae will
since humans can be a major source of infestation for dogs.
Strongyloidosis can be diagnosed in cats even if it is less com-
mon than in dogs. Strongyloides species (other than S. ster-
coralis) have been described in cats. Other free-living Rhab-
ditidae (Pelodera, Rhabditis) may cause skin lesions.
Synonyms
Threadworm infestation.
Geographical distribution
Found throughout the world but with a higher prevalence in
countries with hot, humid climates. Canine strongyloidosis
50 μm
is sometimes seen in Europe, particularly in breeding facili-
ties and kennels with low levels of hygiene. The disease has Figure 1. Adult nematode of the genus Strongyloides (threadworm).
also been seen in areas where soils are damp and marshy, or
where there is unauthorised camping and unsanitary condi-
tions prevail.
Hosts
Horses are infected by S. westeri, pigs by S. ransomi, and
ruminants by S. papillosus. Carnivores and humans are
infested by S. stercoralis. Although cats can be infested,
strongyloidosis caused by S. stercoralis is mainly a parasitic
disease of dogs.
20 μm
Importance
S. stercoralis is important as it is a zoonosis. It is possible
to genetically distinguish between the parasite populations
adapted to each host.
Morphology
Threadworms are small, slender nematodes measuring
2–9 mm in length (Fig. 1). Only the parthenogenetic females
are parasitic and they produce eggs without males being
10 μm
present. These eggs are small, oval and clear and they meas-
ure approximately 30 × 40 µm and contain one stage 1 larva Figure 2. Strongyloides eggs.
*Strongyloides stercoralis
TABLE OF
28 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
VetBooks.ir
develop through rhabditiform stages 2, 3, 4 and pre-adult and the lungs via the right ventricle of the heart. From the trachea,
finally become free-living adult male and female worms. This they are coughed up and swallowed down into the small in-
happens very rapidly, in a single week if environmental condi- testine where they become mature adults.
tions are favourable. After mating, the non-parasitic females In immunocompromised hosts, the eggs laid by the para-
lay eggs which hatch and develop into L1, L2 and finally L3 sitic females may hatch and develop inside the host, produc-
infective filariform larvae. This second generation stage 3 lar- ing stage 3 larvae and new generations. These then invade
va is the parasitic stage, and it consists solely of females which other organs and the peritoneum, causing hyperinfective
can penetrate the host by ingestion, but they more commonly (sometimes called disseminated) stongyloidosis in humans,
enter via the skin. They reach the bloodstream and pass into but not described in dogs.
Parasitic generation
Infective
in
filariform
larva
Larvae infest Infective
puppies via milk filariform
larva
The LACTOGENIC
rhabditiform TRANSMISSION
An
larva becomes
ima
INDIRECT CYCLE
Env
an infective
l/H
filariform larva
iron
um
me
Adult
an
INTERNAL AUTOINFECTION
nta
Egg
Embryonated egg
Free-living generation
Faeces
Rhabditiform larva
Adults develop,
mate and lay eggs Rhabditiform larva
D.H. = definitive host
TABLE OF
CONTENTS Intestinal parasitoses 29
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GASTROINTESTINAL PARASITOSES
The normal life cycle takes 4 to 6 weeks to complete. Clinical signs and lesions
Stage 3 larvae continue their migration into the pulmonary Invasive phase: appearance of papules on the ventral parts
arterioles and disseminate throughout the host’s tissue. of the animal. These skin infestations can also be caused by
They then become encysted and remain dormant for several other types of nematodes or rhabditoids (of the genus Pelod-
months but they can recommence migration during periods era or Rhabditis, for example).
of stress, for example parturition, when they can then infest Migration phase: coughing may occur when larvae migrate
puppies through the mother’s milk. into the lung parenchyma.
Intestinal phase: severe enteritis accompanied by colic, diar-
Epidemiology rhoea and anaemia. Threadworms lead to profuse diarrhoea
Strongyloidosis is seen all year round in warm countries, and and often cause a febrile syndrome (pyrexia, tremors and
through the summer in temperate countries. It is a helminth lethargy). Strongyloidosis can easily be mistaken for bacteri-
infestation which can affect animals housed indoors as well al enteritis, such as colibacillosis or salmonellosis.
as those which have access to the outdoors, and it affects
young animals in particular. The free-living adults can devel- Lesions
op in badly kept breeding facilities and kennels, with damp Development of acute catarrhal enteritis, sometimes with ul-
soils and surfaces. cers and haemorrhaging.
Trichuriosis
General comments
Definition Synonyms
Trichuriosis (whipworm infestation) is a disease of the pos- Trichocephalosis. The name Trichocephalus refers to the
terior part of the gastro-intestinal tract in mammals caused very fine (hair-like) anterior extremity of this parasite, while
by the presence and development of nematodes of the genus the posterior third is thicker in diameter. In fact, this name
Trichuris. Whipworms are host-specific: in canids, infesta- is actually more exact than Trichuris, which means the op-
tion is caused by Trichuris vulpis (Fig. 1). In pigs, infesta- posite. But international nomenclature has retained the first
tion is caused by Trichuris suis and in humans by Trichuris description, even though erroneous.
trichiura.
Although cats in Europe do not harbour specific Tri- Geographical distribution
churis, some species of Trichuris do infest certain wild feline Worldwide.
species in South and Central America, and infestation of pet
cats by these species has been described. Importance
This parasite causes colitis, and even significant anaemia
when associated with Ancylostoma nematodes.
Morphology
Trichuris nematodes are clearly divided into two parts: a
fine, thin, long anterior portion (measuring 2/3 of the total
length), and a thicker, shorter posterior portion. Trichuris
vulpis measures 3–5 cm in length (Figs. 2 and 3).
5 mm
5 mm
5 mm
Figure 2. Trichuris vulpis. Figure 3. Trichuris vulpis male (at the top) and female (at the bottom).
TABLE OF
CONTENTS Intestinal parasitoses 31
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GASTROINTESTINAL PARASITOSES
Biology
Trichuris are parasites of the caecum and colon and they at- yellow-brown coloured eggs with a thick, smooth shell with
tach themselves to the mucosa with the anterior end, by em- bipolar plugs at each end and measuring 60–70 × 25–40 µm.
bedding it in the tissue. After the eggs, containing larvae, are When the eggs are shed, they contain only a single cell but
ingested and the larvae are released, complete development they develop into embryonated eggs in 1 month in the ex-
takes 10–12 weeks. This development occurs with no sys- ternal environment and survive in the soil for several years,
temic migration, the larvae remaining in the wall of the intes- where they are not particularly sensitive to extreme weather
tine. The females are relatively prolific and lay barrel-shaped, conditions (cold, drought) or to ordinary disinfectants.
D.H.
Dog
Embryonated egg
eg
gs
containing a first
stage larva (L1) Prepatent period: 8–12 weeks
Adults
Epidemiology
Infestation is possible at any age by ingesting embryonated Infested dogs are the only parasite reservoir, which ex-
eggs; however, adult dogs are more commonly infested than plains why trichuriosis is often found in communal environ-
young animals. ments (rescue shelters, breeding kennels).
These eggs are formed 3 to 4 weeks after being shed and
are very resistant, surviving in the soil for several years, Clinical signs
which is why the risk of contamination can be long-lasting. Infestation causes congestive and haemorrhagic colitis, re-
This explains the incidence of trichuriosis in breeding facili- sulting in diarrhoea which is sometimes haemorrhagic. This
ties and kennels. may be the only clinical sign in mild infestations.
Certain types of floor surfaces, such as clay or mud, pro- Anaemia may also be connected with whipworm, par-
mote survival of the eggs. ticularly in chronic infestations or due to a combination with
another helminth, especially A. caninum.
Chronic infestation will cause considerable weight loss in
dogs.
Lesions
This parasitic infestation causes catarrhal and haemorrhagic
typhlitis, with inflammation of the colon and rectum (Figs. 4
and 5).
GASTROINTESTINAL PARASITOSES
Diagnosis
Clinical signs are non-specific, so any faecal examination Emodepside is also active against Trichuris in an oral dose
which will reveal the eggs is the best method of diagnosis of 1 mg/kg.
(Fig. 6). Macrocyclic lactones can be active, depending the mole-
cule and the formulation. Milbemycin oxime is active in an
Control measures oral dose of 0.5 mg/kg. Moxidectin, administered topically,
Treatment is also effective at 2.5 mg/kg.
Trichuris are usually less sensitive to anthelmintics than oth-
er common nematodes (roundworms, hookworms). Prevention
In dogs, benzimidazoles are effective as long as they are Eggs can be eliminated by cleaning hard surfaces with high
administered for several consecutive days. pressure jet hoses. Loose soil can eventually be dug over, thus
Oxantel is a tetrahydropyrimidine anthelmintic (related burying the eggs out of reach. Covering loose soil surfaces
to pyrantel) which is specifically effective against Trichuris with gravel or pebbles is also a solution, to limit contact be-
at a dose of 20 mg/kg (it is often combined with pyrantel and tween eggs and dogs.
praziquantel).
25 μm 40 μm
100 μm 40 μm
Capillariosis
The Capillariidae are thread-like nematodes, usually meas- Capillaria (syn. Calodium) hepaticum is a very particu-
uring 10–80 mm in length and with a diameter in the region lar member of the Capillariidae family, which can also be
of 50–100 µm. found in carnivore faeces. This nematode is a parasite of wild
Most Capillariidae have a monoxenous life cycle. rodents that settles in the liver parenchyma. The eggs, con-
Capillaria (syn. Aonchotheca) putorii is a parasite of tained in the uterus of the female, are not shed and remain
the small intestine in wild carnivores, especially Mustelidae within the final host. They are only disseminated if the host
(polecats, skunk, martens, minks, weasels, stoats and ferrets) is ingested by a predator, such as a fox, but sometimes a cat
which can occasionally infest cats. It is not pathogenic and or dog.
infections are generally asymptomatic. The eggs can be seen
on faecal examination (Fig. 1).
GASTROINTESTINAL PARASITOSES
CESTODOSES
Dipylidiosis
General comments
Teniosis, intestinal cestodosis, or tapeworm infestation, is a
1 cm
common intestinal disorder in dogs and cats. The presence of
tapeworm segments in the perianal region and signs of per- Figure 1. Segments of Dipylidium caninum.
ianal itching are common causes for consultation. Intestinal
cestodoses are parasitic diseases caused by infestation with Domestic carnivores, such as cats and dogs, often excrete
adult cestodes: flat, segmented tapeworms belonging mainly whitish elements about half a centimetre in length around
to the order Cyclophyllidea, or to the order Pseudophyllidea. the anal area. These are usually the ovigerous segments of
Clinial signs are subtle or even absent. D. caninum. The posterior gravid segments, which are elon-
Most cestode parasites of dogs and cats are host-specific, gated and called proglottids (Fig. 1), contain capsules full of
however some are common to both species, such as various eggs (oviferous capsules).
Dilepididae, in particular Dipylidium caninum. Wild car- Dipylidium caninum is a long, white, tape-like worm,
nivores (Mustelidae, Felidae and Canidae) can also harbour 15–70 cm long and 2–3 mm wide (Figs. 2 and 3). Other,
dog and cat cestodes, as well as those that are specific to their much rarer Dilepididae can infest dogs and cats; these are
own species. Two genetically distinct populations of Dipylid- Diplopylidium spp. or Joyeuxiella spp., very similar in mor-
ium caninum have recently been described: one is frequently phology but smaller in size (Figs. 4–8). The intermediate
found in dogs, the other one in cats. hosts of the last two cestodes are reptiles (snakes and lizards)
Dipylidium caninum can infest humans, who become con- rather than arthropods. The oviferous capsules contain a
taminated through ingestion of the intermediate host, the flea. single egg, as opposed to the dozens in D. caninum (Fig. 9).
1 mm
100 μm 0.5 mm
100 μm 20 mm
15 μm 20 mm
GASTROINTESTINAL PARASITOSES
Biology
The life cycle of D. caninum is dixenous, i.e., it has two host
species. The most common intermediate host is the flea, and
the other one is the louse. Flea larvae actively ingest sever-
al types debris in their environment, including hairs, skin
debris, and also faeces or Dipylidium proglottids, so the
flea larvae can ingest the oviferous capsules in the gravid
terminal segments. D. caninum eggs survive for between
1 and 3.5 months in the dried segments or in the capsules.
30 μm
D.H.
Dog and cat
Adult (small
D.
H.
intestine)
in
ge
Develops to infective
sts
D.H.
Pre wee
g
4–6
lou
pat ks
se
ent
per
1–2 days
Metacestode
iod
:
Faeces
Proglottid
g (containing
feedin
nd begins oviferous
ges a
emer capsule)
Flea
~10 days and up to ~1 year
(depending on I.H.)
Oviferous
Adult flea capsule
Epidemiology
Dipylidium caninum has a worldwide distribution. Geo-
100 μm
graphical distribution of Joyeuxiella and Diplopylidium is
limited (Mediterranean region to Central Africa). D.H. are Figure 10. Dipylidium caninum non-infective larval stage.
domestic or wild dogs and cats. Copepods and fish are inter-
mediate hosts, as they are for Diphyllobothrium.
The sources of parasites are fleas or lice. Dogs and cats are
infested by ingesting intermediate hosts which have them-
selves been parasitised.
Age does not affect susceptibility and a final host will
never acquire immunity. Reinfestation is therefore possible
throughout the life of the dog or cat, however, certain life-
styles can promote infestation: suburban or rural cats and
dogs are often infested with fleas and therefore risk infesta-
tion with D. caninum.
200 μm
GASTROINTESTINAL PARASITOSES
Both general and localised clinical signs can be seen: Itching:
• Itching of the perianal region is common and characterised
General signs by licking and nibbling at the base of the tail. One of the
Adult cestodes can cause moderate loss of vitamins, mineral most characteristic signs is rubbing or dragging the rear
trace elements and carbohydrates, so emaciation can be seen end on the ground. The itching is connected with mechan-
in underfed or severely infested animals, or in growing young ical irritation and congestion of the anal glands. Licking of
carnivores. the perianal region also causes eggs to be deposited on the
Neurological signs due to B group vitamin deficiency (B1, animal’s fur.
B6 and B12) and hypoglycaemia are both possible, but very • Congestion of the anal glands accentuates itching. This is
rare. This manifests itself by epileptiform convulsions and evidenced by the expulsion of a foul smelling, brownish
seizures and, very rarely, blindness. These signs may also be liquid containing the disintegrated oviferous segments.
linked to significant irritation of the autonomic plexuses of Anal abscesses are a possible complication.
the neurovisceral system, or to a lack of glucose, as has been • General itching can be seen. Cestodosis reduces the skin
observed with toxocarosis in puppies and kittens. sensitivity threshold in dogs, and abdominal or general
pruritis can be associated with parasites of the gastro-in-
Localised signs testinal system.
These are generally the only ones seen.
Intestinal signs are irregular and diversely associated: Lesions
• Variable appetite, sometimes even increased. Dipylidiosis in both cats and dogs is evidenced by chronic
• Loose or diarrhoeic faeces (due to congestive enteritis). enteritis of the small intestine (Fig. 14) as the parasites are
• Elimination of gravid segments (Fig. 13). These are gen- found in the duodenum and jejunum.
erally easily visible and measure 10–12 × 5–8 mm. Di- A proinflammatory, irritative effect is responsible for re-
pylidium segments can move around the perianal region actions in the gastro-intestinal system. Fixation of the scolex,
by themselves. They desiccate and shrivel up, resembling the chain of segments rubbing against the mucosa of the
whitish, uncooked rice grains, 3–5 mm long. The segments gastro-intestinal system and the fragments of membrane re-
can be found either in the perianal region or in the faeces. moved by the parasite cause this enteritis. Mechanical action
Owners sometimes mistake these grains for the oxyurids obstructs the anal gland orifices; and, very rarely, intestinal
(pinworms) seen in children, but it should be noted that obstruction similar to that caused by ascarid pellets can
dogs and cats are never infested with pinworms. occur.
Figure 13. Dipylidium caninum segments. Figure 14. Adult Dipylidium caninum in cat intestine.
TABLE OF
40 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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Diagnosis
Clinical diagnosis is impossible except when proglottids are Praziquantel in a single dose of 5 mg/kg, in oral or inject-
visible. The reason for veterinary consultation is generally the able form, or at 10 mg/kg in transcutaneous formulations.
presence of moderate intestinal disorders (variable appetite, This will have an effect on all cestodes present, including
diarrhoea, signs of perianal itching). Diagnosis of dipylidiosis Echinococcus.
is based on finding oviferous segments by macroscopic ex- Treatment for D. caninum is advisable in dogs and cats
amination of faecal samples. Eggs can be found in the faeces with flea infestations and the insecticides used to treat fleas
if a segment is destroyed before it is expelled. These eggs can will limit the risk of infestation with D. caninum. Effective
be isolated or grouped together inside the oviferous capsules. and ongoing prevention of the former prevents infestation by
the latter.
Control measures
Various cestodicides can be used to treat D. caninum: ben- Risk to humans
zimidazoles, niclosamide and praziquantel. The accidental ingestion of a flea by a child, which is unusu-
Oxfendazole in a drinkable suspension is used in dogs, at al, can result in a case of dipylidiosis. The symptoms are the
a dose of 11.3 mg/kg/day for 3 days. It is also active against same as those for dogs and cats: reduced appetite, abdominal
cestodes of the genus Taenia at this dose. discomfort, anal pruritus.
Niclosamide can be used in a single dose of 80 mg/kg.
Video 2.1
Dipylidium caninum (tapeworm) eggs
in an oviferous capsule (microscopic view).
Video 2.2
Moving Dipylidium caninum (tapeworm)
proglottids on the anal area of a cat.
TABLE OF
CONTENTS Intestinal parasitoses 41
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GASTROINTESTINAL PARASITOSES
Mesocestoidosis
General comments
Mesocestoides are cestodes of the order Cyclophyllidea Morphologically these tapeworms are of average size,
which use two intermediate hosts, whereas all other Cyclo- measuring 20–50 cm in length, and their segments are as
phillidea have only one. The first is an arthropod, which wide as they are long and have rounded edges (Fig. 1).
harbours the cysticercoid larvae. The second is an insectiv- Mesocestoides lineatus and Mesocestoides litteratus
orous vertebrate, which harbours an elongated larva called cause cestodosis in both dogs and cats.
a tetrathyridium.
D.H.
Dog, cat and other carnivores
Faeces
Prepatent period:
3–5 weeks
Proglottid
Horizontal division
or binary fission
Embryonated
eggs
Biology
Carnivores become infested by ingesting the second inter- pleural cavities of cats and dogs (see Peritonitis due to Meso-
mediate hosts which harbour the second larval stage, the cestoides larvae, page 194). After accidental ingestion of the
tetrathyridium. These hosts are amphibians, reptiles or birds. first intermediate host (arthropod), or sometimes the second
In the case of M. lineatus, second intermediate hosts are intermediate host, the larvae migrate through the wall of the
amphibians and, in M. litteratus, they are birds. intestine into the peritoneum, where they will transform and
Another species, Mesocestoides corti (syn. Mesocestoides multiply after repeated budding (asexual reproduction). The
vogae) is a parasite of carnivores in North America. larvae appear to be deformed, due to this multiple budding
Normal larvae, found in the second intermediate hosts, and they proliferate in a disorganised fashion, usually in the
are 5–7 cm long and a few millimetres wide. They are rib- peritoneum of infested carnivores, and cause parasitic peri-
bon-like, with a depression enclosing the future scolex of the tonitis and ascites. This proliferation produces numerous
adult at one extremity. white, semolina-like grains, in an inflammatory exudate.
The tapeworm will appear approximately 4–6 weeks af- Clinically, the infestation can be asymptomatic, or give rise
ter ingestion of the larvae. Carnivores excrete the oviferous to signs of peritonitis, and diagnosis is often made by acci-
segments containing the eggs, which are spherical in shape dent, during surgery. This larval cestodosis seems to be more
with a smooth, thin outer shell (Fig. 2). The hexacanth em- common in cats than in dogs.
bryo is protected by a second inner shell, separated from the In dogs, parasitic peritonitis with ascites can be caused by
first by a vitelline layer. multiplication other cestodes, including the larva of Taenia
crassiceps, a fox parasite.
Epidemiology
Mesocestoidosis is a relatively rare type of tapeworm infesta- Diagnosis
tion, which is sporadically seen in dogs and cats which hunt, Clinical diagnosis is difficult. Ascites may be diagnosed by
and it is mainly a rural parasitosis. X-ray or ultrasound scan, and then confirmed on abdomino-
centesis, when the numerous white grains will be seen. This
Clinical signs parasite infestation can often be diagnosed by laparotomy
Mesocestoidosis is often well tolerated, only rarely caus- (for example, during ovariohysterectomy).
ing intestinal disorders, as is the case with other cestodes.
Changes to appetite, from anorexia to polyphagia, have been Control measures
described. Mesocestoides parasites are unusual in that the Treatment for adult forms consists of standard cestodicides
larval stage (tetrathyridium) can develop in the peritoneal or (such as praziquantel).
1 mm 25 mm 15 mm
GASTROINTESTINAL PARASITOSES
Taenioses sensu stricto
Scolex
Proglottids
or segments nt
The infective larva is ingested and the
excreted in faeces pate ths
ain n
tapeworm scolex attaches itself to the Rem –30 mo
intestinal wall for 7
Small intestine
GASTROINTESTINAL PARASITOSES
Eggs/proglottids ingested by I.H.
Faeces
Embryo
Viable for
Proglottid with eggs months
6 months
30 days to
Intestinal cells
Infective larval
sted
form in I.H.
tissu
D.H.
e
200 μm 0.5 cm
Figure 1. Taenia sp. scolex viewed from the top. Figure 2. Taenia sp. proglottids.
GASTROINTESTINAL PARASITOSES
Muscular cysticercosis in sheep, Epidemiology
caused by Taenia ovis Hepato-peritoneal cysticercosis in rabbits
Muscular cysticerci measure 2.5–4 × 4–9 mm in length, and This parasitic disease is found in the wild and in rural areas.
are similar to those of Taenia solium, one of the three tape- In the latter, it occurs where rabbits are reared in hutches and
worms infesting humans (the others being Taenia saginata have been fed with grasses soiled by dog faeces.
and Taenia asiatica). They develop fully in approximately
83 days, but are infective from the 46th day. They degenerate Hepato-peritoneal cysticercosis
rapidly after death of the ruminant, those found in the cardi- in ruminants
ac region taking approximately 3 months. This parasitic disease is found in rural areas where dogs have
access to the viscera of sheep which have been slaughtered or
Nervous coenurosis in sheep died from various causes.
The Taenia multiceps larva develops in the intermediate
host's central nervous system, mainly in sheep's brains. It is Coenurosis in sheep
infective after about 2 months but continues to grow. The Nervous coenurosis is enzootic to sheep-producing regions,
larva looks like a small balloon containing water, with a di- and is contracted by animals under 2 years old. It is currently
ameter of 10–20 cm, and it contains several white dots which very rare in Europe and mainly affects sheep , but cattle and
are the cephalic invaginations of future Taenia multiceps goats can also be infested. Horses or humans can occasion-
scoleces. It compresses the nervous tissue, causing specific ally be infested. Once again, dogs must ingest raw sheep’s
neurological signs in infested ruminants. brains, and therefore need access to dead sheep, for animals
to become infested and for the life cycle to be continued.
Subcutaneous coenurosis of rabbits
The Taenia serialis larva develops in the subcutaneous tissue Muscular cysticercosis in sheep
of the intermediate hosts, domestic and wild lagomorphs. It The final hosts of T. ovis are dogs or other canids. The adult
is infective after about 2 months but continues to grow. The tapeworm is 45–110 cm long, and the oviferous segments
larva looks like a subcutaneous tumour, with a diameter of measure 15 × 3.5 mm. The prepatent period lasts 7–9 weeks.
approximately 10 cm. On opening, the larva is a soft, large The segments are usually excreted by dogs and the eggs then
cyst containing several white dots which are the cephalic ingested by sheep. Cysticerci are formed in approximately
invaginations of Taenia serialis scoleces. It can induce par- 5 weeks and dogs are infested by eating infected meat or of-
ticular clinical signs in rabbits by compressing muscles or fal. The cysticerci mainly attach in their host' heart and liver,
articulations. but also in the muscles.
0.2 mm
GASTROINTESTINAL PARASITOSES
Echinococcoses E. multilocularis, which sheds some oviferous segments, al-
though this is rare.
Hydatidosis is usually asymptomatic in animals and is
General comments characterised by the formation of a cyst, called a hydatid
Hydatid echinococcosis, or hydatid disease, is an infectious cyst, consisting of the larvae surrounded by inflammatory
but non-contagious disease caused by the larvae of a cestode, tissue caused by the host's reaction.
common in humans and a number of other animal species. It Dogs are infested by the adult cestodes. Echinococcus
is caused by development of the cestode, Echinococcus gran- granulosus is a small cestode, 3–6 mm long, and consists
ulosus sensu lato, in tissues and organs, mainly the liver and of 4 to 5 segments, only the final segment being oviferous
lungs. This cestode is an intestinal parasite in the dog. (Fig. 1). This final segment represents about half of the total
Another species that can also be observed in dogs is Echi- length of the worm and contains an elongated, non-sack-like
nococcus multilocularis, which mainly affects foxes, but it uterus. These two characteristics enable it to be distinguished
is the agent of multilocular or alveolar echinococcosis in ro- from E. multilocularis, in which the oviferous segment con-
dents and humans. tains a sack-like uterus (Fig. 2) and is less than half of the
Echinococcus granulosus cannot develop into the adult whole worm.
stage in the cat, which therefore plays no role in the epidemi- The eggs contained in the uterus are identical to all Taenii-
ology of hydatid disease. Cats can, however, be infested with dae embryophores and cannot be distinguished from Taenia
eggs. They are spherical, measuring 30–45 µm in diameter,
with a single, thick shell with concentric striation. Each egg
contains a hexacanth embryo with six hooks, a number of
which are visible (Fig. 3).
Synonyms
Infestation with Echinococcus larvae
(in intermediate hosts)
Hydatid echinococcosis caused by the larva of E. granulosus
and multilocular or alveolar echinococcosis caused by the
larva of E. multilocularis.
0.5 mm
Infestation with adult Taeniidae
Figure 1. Echinococcus granulosus. Taeniosis (in dogs or other canids).
0.5 mm 12 μm
GASTROINTESTINAL PARASITOSES
Life cycle of Echinococcus granulosus sensu lato
D.H.
Dog and other canids
D.
H.
inf
es
Protoscolices
ted
(evaginated-above,
by
protoscolices
on
tam
ina
ted
vis
Pr –6 w
ce
ep e
4
ra
at ek
en s
tp
er
io
d:
depends on the I.H.
Maturation rate
Unilocular
hydatid cysts
Adult
Immediately infective,
persist for months in the
external environment
gs
ed eg
yonat
disseminates through
the blood vessels
I.H. in
Embryonated egg
D.H.
Fox, dog (and cat)
D.
H.
inf
es
ted
Protoscolex
by
(multilocular proliferative)
es
tin
I.H.
I.H
.
3–
4
we
ek
s
depends on the I.H.
Maturation rate
Adult
Multilocular
larva
ely
ediat ts
Imm e, persis
e c t iv
inf t h s
on
for m
bryonated eggs
I.H.
Voles, lemmings, field
mice, shrews (rarely: other
mammals, including humans)
Embryonated D.H. = definitive host
egg I.H. = intermediate host
Epidemiology
Hydatid echinococcosis Different cycles can be seen in different countries. For in-
It is possible to distinguish epidemiological cycles in wild an- stance, a sheep/dog cycle exists alongside a dingo/kangaroo
imals from those in domestic rural animals where infestation cycle in Australia. Cycles involving zebus in Africa, or buffa-
of urban human populations is possible. In Southern Europe, lo in Asia, have been described. Sometimes pigs also play an
the sheep/dog cycle is predominant. This does not mean that important role. These cycles generally involve different host
dogs in an urban environment cannot be infested; they only animals and genetically different parasite genotypes (and
need to access infested viscera, for example, in a dustbin after maybe even species). Ten genotypes of E. granulosus have
sheep have been illegally slaughtered. been identified, but are still a subject of controversy.
TABLE OF
CONTENTS Intestinal parasitoses 53
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GASTROINTESTINAL PARASITOSES
Echinococcus granulosus: different genotypes or species Multilocular echinococcosis
This parasitic disease has a woodland element involving wild
• G1 and G2: sheep genotypes, distributed worldwide,
zoonotic; marsupial genotypes in Australia, zoonotic.
animal hosts in its epidemiological cycle. Occasional infesta-
• G3: cattle and buffalo genotypes (first identified in India),
tion of domestic dogs or cats as final hosts is still a possibility.
zoonotic.
• G4: horse genotypes in Europe, either less zoonotic or not Sources of parasites
zoonotic. Proposed name Echinococcus equinus. • Direct: foxes, and sometimes dogs.
• G5: cattle genotypes, distributed worldwide, zoonotic. The • Indirect: rodents (Microtidae).
name Echinococcus ortleppi proposed by some authors.
• G6: camel genotypes in Africa, and Near and Middle East,
Mechanisms of infection
zoonotic. Proposed name Echinococcus intermedius.
• G7 and G9: pig genotypes, distributed worldwide, zoonotic.
• Of the final host: by consuming rodents.
• G8 and G10: northern genotypes, infesting Cervidae in • Of the intermediate host: by ingesting plants or fruits con-
particular, zoonotic, considered by some authors to be taminated by Echinococcus eggs (blackberries, blueber-
ancestral genotypes. Proposed as Echinococcus canadensis ries, wild strawberries).
(G10) and Echinococcus borealis (G8).
Susceptibility
Where human echinococcosis (alveolar or hydatid) is con-
cerned, the parasite is destroyed in some individuals and
Sources of parasites allowed to develop in others, although there are more sero-
• Intermediate hosts carrying cysts, mainly sheep, and espe- positive patients than there are individuals infested with a
cially those over a year old (the time required for infective viable parasite.
larvae to form; 6 months in pigs, 10 months in sheep).
• Dogs or other canids that excrete oviferous segments (a Predisposing factors
long-lasting source: 6-month life span for the adult ces- • Behavioural habits of foxes which defecate near vole holes.
tode. A dog can harbour several thousand echinococcal • Behavioural changes in infested rodents which become less
cestodes; the lack of acquired immunity means that rein- reactive, and are therefore caught more easily.
festation is possible). • Some intermediate hosts die rapidly, but the life span of
others is doubled and they become parasite reservoirs,
Mechanisms of infestation in intermediate hosts hence the distinction between species of receptive voles
Ingestion of food or water contaminated with oviferous seg- which are called “permissive”, and which play a determin-
ments or embryophores. Possible contamination of humans ing role, and species which are susceptible but which do
if embryophores are present on the dog’s coat. not play an important part in the epidemiology.
• Risk of increased cases of humans infection during periods
Predisposing factors of rodent proliferation, or because of increasing fox popu-
Dog/sheep association in mountain pastures or on farms. Ille- lations. The impact of rabies vaccination should therefore
gal slaughter of sheep and distribution of offal to carnivores. be measured.
TABLE OF
54 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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GASTROINTESTINAL PARASITOSES
0.2 mm 0.2 mm
Figure 4. Echinococcus protoscolex in Figure 5. Free Echinococcus protoscolex. Figure 6. Hydatid larva in liver.
hydatid cyst.
Figure 7. Hydatid larva in the lung of a cow. Figure 8. Echinococcus multilocularis larva Figure 9. Echinococcus multilocularis larva
in the liver of a microtid rodent. in the liver of a microtid rodent.
The final hosts for the genus Spirometra are wild or domestic Biology
carnivores which are likely to ingest the second intermediate Bothriocephalic cestodes are found in the small intestine and
hosts (amphibians or fish). The second stage, pleroceroid lar- take approximately 6 weeks to form after an infested inter-
vae may cause larva migrans in humans because amphibian mediate fish host is ingested. The tapeworm sheds the eggs
skin is sometimes used in traditional medicine for its healing which are found in the faeces and, if the eggs fall into water,
properties. Subcutaneous larvae can also penetrate through they hatch and liberate spherical, ciliated and mobile coracid-
cuts and sores and cause serious tissue inflammation contain- ium larvae. These are ingested by freshwater copepods (Cy-
ing living larvae. This larval cestodosis is called sparganosis. clops), and develop into procercoid larvae inside them. The
first intermediate host copepods are themselves ingested by
Importance second intermediate host fish, in which the plerocercoid lar-
Diphyllobothriosis is zoonotic and medically significant, be- vae develop. The plerocercoid larva resembles an adult and
cause of the size of the adults (which can reach 12 metres in measures 2–3 cm. It is located in the abdominal cavity of the
length), and the loss of vitamin B12 it can cause. This can fish. If that particular fish is hunted by another fish, the larva
lead to a state of pernicious anaemia. will reencyst and accumulate in the predator fish.
TABLE OF
CONTENTS Intestinal parasitoses 57
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GASTROINTESTINAL PARASITOSES
Life cycle of Diphyllobothrium latum
D.H.
Dog, cat, other carnivores
and human
Plerocercoids develop
D.
Adult
r2
nd
Pre
I.H
~3 pate
.
–5 n
we t per
eks iod
:
te
ula
acc d,
so g-live
um
Microscopic
Lon
eggs excreted
P.H.
in faeces
(rarely
Plerocercoid proglottids)
The second I.H. is ingested
Eg Egg
in gs ha
Lo ac
fre
ng cu
so
Procercoid sh tch a
-liv mu
s wa nd
ek
ed lat
ter de
we
,
3 vel
1– op
e
Cop h devel
(wh
2–3 weeks
s
epo
od
ic
ep
ds in op into
2nd I.H.
cop
Procercoids
gest
d
ste
invade tissues
nfe
cora ocercoi
pr
pleurocercoids Coracidium
cidia
.ea
I.H
2 nd
D.H.
Bobcat, raccoon, cat and dog
Adult
I.H
. is
ing
es
ted
by
Plerocercoids develop
D.
in the muscles or
H.
15–30 days
subcutaneous tissues of
the I.H.
Microscopic eggs
excreted in faeces
(rarely proglottids)
Plerocercoid
so accumulate
Long-lived,
Egg
Egg
s
hatc develop
h in
fres and
s
eek
h wa
ter
3w
1–
10–14 days
ds
Co
po
pe
pe
2nd I.H.
po
Coracidium
co
Procercoid
di
sts
(amphibians, reptiles,
ng
ge
es
.
ts
I.H
co
2 nd
rac
idi
a
GASTROINTESTINAL PARASITOSES
The plerocercoid larvae can be found in many fish, such Control measures
as the Esocidae or pike family, (the northern pike, Esox lu- Treatment
cius), Percidae or perch family (the European perch, Perca Diphyllobothriidae are less sensitive than other cestodes
fluviatilis) and Salmonidae (trout, Salmo trutta and Oncho- to the active ingredients in many anthelmintic products so
rhynchus mykiss; and the char or brook trout, arctic salmon praziquantel is the only effective treatment, but it must be
and trout, Salvelinus). used at 8 times the regular dose, i.e., 40 mg/kg instead of
5 mg/kg. It should be given orally.
Epidemiology
Final hosts always become infested by ingesting the second Prevention
intermediate hosts harbouring the plerocercoid larvae (fresh- Preventing infestation in dogs and cats includes not feeding
water fish for D. latum and amphibians for Spirometra). them fish or the viscera of fish caught in lakes, particularly
The final hosts shed the eggs (cestodes with tocostoma) mountain lakes.
which develop in an aquatic environment.
These are essentially wild cycle cestodes that are limited to
regions where there are lakes and ponds.
Domestic mammals become part of the cycle by chance:
for example, a dog that goes fishing with its owner, or walk-
ing around a lake.
Clinical signs
D. latum is probably the most pathogenic of the tapeworms.
It causes intestinal disorders, abdominal discomfort and di-
arrhoea, but also vitamin B12 deficiency by inhibiting ab-
100 μm
sorption of this vitamin, so infested animals or humans will
present with pernicious anaemia that will only be eradicated
with the death of the parasite. Intestinal infestations of cats
and dogs with Spirometra spp. rarely cause disturbance.
Diagnosis
Diagnosis is made by examining the faeces for eggs, which
are usually numerous (Fig. 1).
100 μm
TREMATODOSES
Heterophyidae
Very small trematodes (less than 2 mm long) with a broad-
ened posterior end. Most have a sucker enclosing the genital
pore (gonotyl) (Fig. 2). Aquatic molluscs and fish play a part
50 μm
in the life cycle, the latter being host to the metacercaria, or
encysted stage. Heterophyids are parasites of the small intes- Figure 1. Mesostephanus egg.
tine in mammals and birds.
GASTROINTESTINAL PARASITOSES
Echinostomatidae Diplostomatidae
Trematodes whose anterior suckers enclose a necklace of 1 or Trematodes with an oblate anterior end:
2 rows of spines. The second intermediate hosts are molluscs • Alaria alata, Alaria marcianae, Alaria americana:
or fish. The eggs are large, similar to those of the fasciolid 3–6 mm long. The eggs are large: 100–125 × 60–80 µm.
ruminant parasite: 90–150 × 60–80 μm: Parasites of the small intestine in cats, dogs and wild carni-
• Euparyphium melis: 3.5–12 × 1.5 mm. A parasite of the vores. The second intermediate host is an amphibian or a
small intestine of aquatic carnivores, such as otters, and reptile. Paratenic hosts are possible (such as rodents or pigs).
also cats and hedgehogs. It has been found in Europe.
• Echinochasmus perfoliatus: 2–4 × 0.5–1 mm. A parasite Clinical signs and treatment
of aquatic carnivores, and sometimes cats, dogs, pigs and These parasites do not usually cause any intestinal disor-
humans. Found in Central Europe and Asia (Fig. 4). ders and they are discovered accidentally through faecal
examination.
Order of holostomes Intestinal disorders and pancreatic failure have been de-
Trematodes whose bodies are divided into two parts, the scribed very rarely, in massive infestations.
proximal part having two suckers (oral sucker and tribocytic Various anthelmintic treatments have been tested, includ-
organ), the sac-like extremity containing the sexual organs. ing the standard flukicides used in ruminants (nitroxynil,
triclabendazole, albendazole) and praziquantel (used in hu-
mans against schistosomes). Praziquantel at 75 mg/kg, taken
for 2–3 days seems to offer the best results.
A B
Figure 3. Metagonimus yokogawai. Courtesy of Guangxi University. Figure 4. (A) Echinochasmus liliputanus and (B) Echinochasmus
perfoliatus. Courtesy of Guangxi University.
TABLE OF
62 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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Heterophyidae
+
Apophallinae Apophallus (Rossicotrema) donicus, muehlingi, venustus
Acanthotrema felis
+
Diorchitrema formosanus, pseudocirratum
GASTROINTESTINAL PARASITOSES
Table 1. Overview of trematodes infesting domestic carnivores (continuation).
Opisthorchis (Fig. 5)
Biliary and/or
pancreatic Opisthorchiidae Parametorchis complexus
ducts
Paropisthorchis caninus
Pseudamphistomum truncatum +
PROTOZOOSES
GASTROINTESTINAL PARASITOSES
Life cycle of Cryptosporidium spp.
D.H.
Dog and cat
Ing
est
ion
of o Infective form
ocy
st (sporozoites)
2–1
Oocyst
0 da
ys
Da
ys
to
m
on
th
s
Faeces
Oocyst containing
Faecal-oral four sporozoites
Diagnosis
Diagnosis based on clinical signs is impossible. Intermittent Two drugs have also shown some success in other animal
or persistent diarrhoea in animals in poor condition can be species and are worth trying in the most serious cases: these
the only guide to diagnosis and confirmation is based on the are paromomycin at a dose of 100 mg/kg/day per os for 7
detection of oocysts in faecal matter. This cannot be done days and halofuginone lactate at a dose of 100 mg/kg/day
using the standard coproscopic techniques used in carnivores per os for 3 days. Nitazoxanide is currently used in the treat-
because of the size of the oocytes. Screening requires either ment of human cryptosporidiosis in children in the United
specific colouration, such as a modified Ziehl-Neelsen stain, States and a regimen has also been approved to treat animals
or flotation in a sucrose solution (Figs. 1 and 2). (see Antiprotozoals, page 359).
10 μm 10 μm
Figure 1. Cryptosporidium oocysts (in red) Figure 2. Two Cryptosporidium oocysts (white)
(Ziehl-Neelsen staining). (Gomori staining).
TABLE OF
CONTENTS Intestinal parasitoses 67
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GASTROINTESTINAL PARASITOSES
Coccidioses Morphology
These protozoa appear in different forms: intracellular forms
called schizonts (meronts) and gamonts (gametocytes) can be
General comments seen in intestinal cells.
Canine and feline coccidioses are infectious diseases caused Free forms also exist in the intestinal lumen. Some have
by intestinal Apicomplexan protozoa of the class Coccidea. a very short life, and are therefore rarely observed: these
Coccidioses are characterised by the development of gener- are the sporozoites, merozoites and microgametes. Others
ally severe enteritis with diarrhoea which can sometimes be are more resistant and are found in the faeces: these are the
haemorrhagic. Coccidioses are caused by coccidia which are oocysts, with the exception of Sarcocystis spp., which shed
specific to dogs - Isospora canis, Isospora ohioensis, Sar- sporocysts. Diagnosis of the type of coccidiosis is based on
cocystis spp. specific to dogs, Hammondia heydorni and finding one or the other on faecal examination.
Neospora caninum, or to cats - Isospora felis and Isospora
rivolta, Sarcocystis spp specific to cats, Hammondia ham- Biology
mondi and Toxoplasma gondii. Coccidia, which cause coccidiosis in dogs and cats, multiply
Coccidiosis is a protozoan disease with worldwide distri- in the intestinal tract and invade the mucous membranes.
bution. Coccidiosis caused by Isospora spp. is seen in young They may even migrate to extraintestinal locations, as is the
animals, where it is common and frequently underestimated. case with genus Isospora. Multiplication of the parasites gen-
Coccidiosis caused by Sarcocystis spp. is linked to the in- erally takes place in the small intestine, with the exception of
gestion of raw or undercooked meat. I. ohioensis where it generally takes place in the large intes-
tine (caecum and colon).
Taxonomy The pathogenesis of coccidiosis is not well understood,
Coccidia are Apicomplexan protozoa of the subphylum but it seems to be connected with the destruction of the intes-
Sporozoa, belonging to the class Coccidea (Coccidia sensu tinal epithelium by the parasite and the host’s inflammatory
lato) and to the suborder Eimeriorina. Dog and cat coccidia reaction, which causes oedema and thickening of the mucous
belong to three different families: membranes. These lesions then reduce the absorption by the
• The Isosporidae family, subfamily Isosporinae; I. canis, intestine. There is also a generally toxic effect, which would
I. ohioensis, I. felis and I. rivolta, characterised by a ho- explain cases of neurological dysfunction.
moxenous life cycle.
• The Isosporidae family, subfamily Toxoplasmatinae; Epidemiology
H. heydorni and H. hammondi, T. gondii, N. caninum and The epidemiology of coccidiosis depends on the species of
Besnoitia spp., with a heteroxenous life cycle. An asexually coccidia involved because their life cycles are different.
reproductive phase is followed by a sexual reproduction
phase in the definitive host dog or cat. There is a variety of Coccidiosis caused by Isospora spp.
intermediate hosts, including birds and rodents for Ham- Coccidiosis caused by Isospora is both widespread and com-
mondia reptiles and mammals for Besnoitia; many birds mon. It generally affects young animals living in a communal
and mammals (including humans) for T. gondii and many environment (breeding facilities, kennels, pet shops), or those
mammals (but not humans) for N. caninum. that have just been acquired from one of these sources.
• The Isosporidae family, subfamily Sarcocystinae; Sarco- The initial symptoms appear at around 3 weeks of age
cystis spp. which have a heteroxenous cycle and only the and are often observed after stress (weaning, sale, transport).
sexual reproduction phase takes place in the definitive host Clinical signs are more severe in animals with impaired im-
dog or cat. munity. Protective immunity is triggered by a primary infec-
tion, so clinical coccidiosis is less common in adult animals.
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15 μm 10 μm
Figure 1. Oocysts of Isospora felis. Coproscopy. Figure 2. Isospora oocysts (Isospora canis [large] - Isospora
ohioensis [small]). Coproscopy.
Life cycle of heteroxenous coccidia (Besnoitia, Hammondia, Toxoplasma and Neospora spp.)
D.H.
Dog and cat
Non-infective
Small and large intestine cells oocyst
5–6 days
s
ue
d tiss Infective
te
fec oocyst
est in
Ing
Months to years
In
ge
sti
on
Toxoplasma Toxoplasma
gondii gondii
GASTROINTESTINAL PARASITOSES
Carrier dogs and cats are sources of parasites and they Oocysts shed into the external environment must undergo
shed oocysts in their faeces for a limited period of time sporulation in order to become infective. Sporulation takes
(Figs. 1 and 2). The parasitic forms may survive for a long at least 24 hours, but is sometimes longer, depending on the
time in various organs, enabling persistent infection, so humidity and temperature. Sporulated oocysts consist of a
breeding animals are a potential source of infection. A car- smooth wall enclosing two sporocysts, each containing four
nivore developing a concurrent disease may also re-excrete sporozoites. They are very resistant and can survive in the
oocysts and many mammals, such as mice, can become pa- environment for 1 to 2 years, but they are sensitive to des-
ratenic hosts after ingesting sporulated oocysts. These hosts iccation, heat (destroyed in 30 minutes at 60 °C), ultraviolet
retain a latent form. Infection of new carnivore hosts occurs light, and cold (destroyed in 3 months at 0 °C and in 7 days
after they ingest the viscera of these paratenic hosts. at 25 °C). Many disinfectants have little or no effect: only
ammonia, and to a lesser degree, Cresyl, is effective.
Bradyzoites
Gametocytes
Infective
ys
sporocysts
Faeces
Ingestion
s
s onth
ue om
tiss st
ted ek
infec We
est
Ing
20 μm 20 μm
50 μm 100 μm
GASTROINTESTINAL PARASITOSES
Table 1. Sarcocystis and Hammondia species with cats or
dogs as definitive hosts.
Definitive
Species Intermediate host
host
Sarcocystis cruzi Dog Cattle
Sarcocystis gigantea
Cat Sheep
(syn. S. tenella)
Each of these coccidia has a specific intermediate host. Figure 7. Besnoitia cyst. Subcutaneous location. Biopsy.
Sarcocystis sporocysts that are shed into the external en- Haematoxylin-eosin stain.
Coccidiosis caused by Neospora caninum
A whole chapter is devoted to this coccidial disease, because
of its specificity to dogs (see Neosporosis, page 182).
Coccidiosis caused by Toxoplasma gondii
A whole chapter is devoted to this coccidial disease, because
of its specificity to cats (see Toxoplasmosis, page 175).
Clinical signs
Coccidiosis caused by Isospora spp.
10 μm
This coccidiosis presents in a variety of forms, from asymp-
tomatic coccidiosis to a subacute, or severe, type of coccidal Figure 9. Toxoplasma oocyst. Coproscopy.
disorder.
The asymptomatic form is more common in well-kept
breeding facilities and it corresponds to a primary infection
with a low parasite burden for the first weeks of life, during
which time immunity is acquired.
The subclinical form reduces growth rate. The acute form
is characterised by foul-smelling, mucoid-to-haemorrhagic
diarrhoea, sometimes with abdominal pain, accompanied
by a change in the general condition of the animal. Other
signs include anaemia, dehydration, anorexia and weight
loss. A febrile syndrome and encephalitic disorders may also
20 μm
be seen. Death may occur in a few days in extreme cases, but
improvement is usually seen in 7 to 10 days. Figure 10. Sporulated oocysts of Toxoplasma. Confocal microscopy.
The chronic form is characterised by pasty, foul-smelling
diarrhoea. The general condition of the animal gradually
changes and there is significant weight loss which may result
in stunting.
GASTROINTESTINAL PARASITOSES
Diagnosis
Clinical diagnosis is impossible: only the presence of frank
or gelatinous blood in the faeces of a young animal will sug-
gest coccidiosis. Differential diagnosis must include canine
parvovirus infection in young dogs, and panleukopenia (fe-
line distemper) in kittens.
Confirmation is based on the detection of oocysts or
sporocysts in the faeces (Fig. 12), which is relatively simple
using coproscopy after enrichment with a dense liquid.
The presence of oocysts in the faeces is not always associ-
ated with clinical coccidiosis, so faecal examination always
10 μm
needs to accompany careful consideration of the clinical
signs. Figure 12. Isospora oocysts. Coproscopy.
Table 2. Characteristics of oocysts and sporocysts that can be found in dog and cat faeces. It should be noted that Hammondia,
Neospora and Toxoplasma oocycts cannot be differentiated.
Species Parasitic elements shed in faeces Average size Infective forms (after sporulation)
Isospora canis Oocyst with one rounded end (basal) Oocyst with two sporocysts,
38 × 30 µm
(dog) and one pointed end (conical) each containing four sporozoites
Isospora ohioensis Oocyst with one rounded end (basal) Oocyst with two sporocysts,
23 × 19 µm
(dog) and one pointed end (conical) each containing four sporozoites
Isospora felis Oocyst with one rounded end (basal) Oocyst with two sporocysts,
38–51 × 27–39 µm
(cat) and one pointed end (conical) each containing four sporozoites
Isospora rivolta Oocyst with one rounded end (basal) Oocyst with two sporocysts,
21–28 × 18–23 µm
(cat) and one pointed end (conical) each containing four sporozoites
12 × 8 µm to 20 × 16 µm
Sarcocystis spp. Sporocyst containing four sporozoites Directly infective sporocyst
depending on the species
Control measures
Treatment Prevention
Outcome is normally favourable after administration of a Prevention is limited in carnivores. The housing in breeding
symptomatic treatment. The specific treatment traditionally facilities and kennels should be kept clean and dry (through
consists of sulphonamides, and the most active is considered daily removal of faecal matter), and surfaces, such as floors
to be sulfadimethoxine. It is used at a dose of 30 mg/kg/day and walls should be disinfected regularly. Sporulated oocysts
per os for 10 to 14 days, and is sometimes combined with are highly resistant but they can be destroyed by high-pres-
baquiloprim. A combination of trimethoprim and sulfadi- sure water vapour (130 bars) and ammonia-based disinfect-
azine at a dose of 15 mg (of sulfadiazine)/kg/day per os for 6 ants. Other measures may also be adopted, such as concret-
days can also be used. ing surfaces in communal areas to allow better disinfection.
Toltrazuril and diclazuril, newer drugs that were original-
ly used in poultry and ruminant farming, are often used by
dog breeders.
Toltrazuril is labelled for use at a dosage of 9 mg/kg, in
combination with emodepside (0.45 mg/kg) orally, to treat
Isospora infection as well as gastrointestinal nematodes in
dogs.
Diclazuril can be used at a dosage of 2.5 mg/kg per os.
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GASTROINTESTINAL PARASITOSES
Giardiosis
General comments
Giardiosis is a protozoan infection of the small intestine,
characterised by the development of enteritis with chronic
diarrhoea, often appearing steatorrhoeic. Protozoa of the ge-
nus Giardia (formerly Lamblia) infect amphibians (G. agi-
lis), reptiles (G. muris), birds (G. muris), and mammals
10 μm
(G. muris in rodents, G. duodenalis (syn. G. intestinalis) in
numerous mammals, including humans).
Giardiosis is a protozoan infection which occurs world-
wide because the parasitic reservoir consists of a great num-
ber of healthy carriers.
It is an infection shared by animals and humans, although
the genotype adapted to each species is quite distinct. This
intestinal parasite is common in cats and dogs but underesti-
mated in veterinary medicine, because of its difficult diagno-
sis, which is still based on faecal examination. 15 μm
Taxonomy
Giardia duodenalis is a flagellated protozoan (phylum Sar-
comastigophora, subphylum Mastigophora), belonging to
the order Diplomonadida (bilaterally symmetrical due to the
incomplete longitudinal division of the parasite) and to the
family Hexamitidae (having eight flagella).
Morphology
This protozoan has two active stages: trophozoites, measur-
5 μm
ing 6–8 × 12–15 µm and equipped with a sucking disk which
enables them to adhere to the surface of intestinal epithelial Figure 1. Giardia cysts (no staining, except Lugol’s iodine in the
cells; and the quiescent, cyst stage, which is shed in faecal bottom image). Coproscopy.
Giardia feed by a process of pinocytosis, engulfing nu- Infection occurs when the cysts are digested by gastric or du-
tritional elements mostly through the dorsal membrane. odenal enzymes, then the two trophozoites contained in the
They multiply by binary division of the trophozoites in the cyst mature and the cyst will then liberate them into the du-
small intestine, where they carpet the surface of the intestinal odenum. Experimentally, this stage takes only 10 to 30 min-
epithelium. utes. The trophozoites then actively multiply by simple lon-
gitudinal binary fission in 5 to 40 hours. In humans, it has
Life cycle been shown that the speed of trophozoite growth depends on
The life cycle of Giardia duodenalis is simple, with alternat- the Giardia strain and on the immune and nutritional status
ing phases of trophozoite multiplication and cyst formation. of the host. No sexually reproductive stage is known.
D.H.
Dog and cat
Animals eliminate
An either trophozoites
im
als or cysts via faeces
ing
es
t cy
sts
Mature cyst
~ 7 days
Cy sev
for
sts era
ca l m
n r on
em th
ain s
inf
ec
tiv
e
Trophozoite
Faeces
Humans ingest
cysts shed by Faecal-oral
pets or, more transmission
likely, other (contamination
humans of food/water)
Mature cyst
GASTROINTESTINAL PARASITOSES
Cysts form gradually during passage from the small to the Epidemiology
large intestine, by a mechanism which is not yet well under- Healthy human or animal carriers are sources of the parasite
stood. pH, concentration of bile salts, and certain fatty acids and infection takes place when cysts are ingested. They are
all play a part. The cyst contains two incompletely formed relatively fragile in the external environment and are sensitive
trophozoites (two to four scarcely visible nuclei, fragments of to desiccation and to ordinary disinfectants. Cysts tend to ac-
crescent-shaped ventral disks). cumulate in moist environments (such as vegetable gardens)
and are conveyed by contaminated water or foodstuffs (raw
Various characteristics of the host and the parasite are in- vegetables, for instance). They can resist for several weeks in
volved and the main host factors seem to be: pre-existing ma- a moist environment (2 months at 8 °C, 1 month at 21 °C,
labsorption, deficient nutritional status and various physical only 4 days at 37 °C).
and chemical changes which alter conditions for the para- It is likely that any period of weakened immunity will fa-
site’s development in the gastro-intestinal tract. Atrophy of cilitate clinical expression of the disease following infection,
the villi is partly caused by the host’s inflammatory and im- or cause a latent infected state to turn into a full-blown dis-
mune responses. The virulence varies according to the strain. ease, as it does in humans.
• Giardia carpet the brush border and mechanically inter- Giardiosis is common in dogs and cats in Europe and in
fere with absorption by the intestine (lactase and sucrase the United States, affecting animals of all ages, with a higher
activity is disrupted in humans). prevalence in young animals from weaning to 2 years old.
• They also cause mucus hypersecretion which disrupts ex- According to a number of epidemiological studies, it can
change at the enterocyte level and shortening of the villi be found in approximately 10 % of faecal examinations in
reduces the surface area for exchange. carnivores that have diarrhoea and are taken to the vet for
• Enterocyte renewal is accelerated, which may cause defec- examination. Epidemiological studies in breeding kennels
tive glucose and amino acid transport (immature cells have indicate that the parasite is present in nearly 100 % of cases,
inadequate enzyme systems). Giardia also interfere with and that the prevalence of infection in dogs is up to 50 %.
fat absorption by inhibiting pancreatic lipase. These figures are identical or slightly higher than in helminth
• The parasites may release toxic substances which can infections, which makes G. duodenalis one of the most com-
affect the metabolism of the brush border and inhibit a mon intestinal parasites in domestic carnivores.
number of enzyme systems. A direct cytopathic effect of
reduced sucrase and alkaline phosphatase activity in en- Clinical signs
terocytes has been demonstrated. Cytopathic effects have Carnivores that have ingested cysts will usually present clin-
been observed in some cell lines (Vero and Hela) in vitro. ical signs one week later, but the incubation period varies
• Giardia may disrupt bile secretion and promote bacterial greatly from one animal to another, and some show no signs
proliferation, though the diarrhoea observed in Giardia of infection and become carriers. There are two forms of the
infection is caused by an absorption disorder rather than disease: a rare, acute form, and a common chronic form.
increased secretion. The acute form is characterised by watery diarrhoea which
is resistant to treatment, colic and bloating, and a change in
Young animals are usually more sensitive than adults, which the overall condition of the animal. There is usually no fever.
can spontaneously limit the infection and this disease is more The chronic form is characterised by pasty, foul-smelling
common in individuals in a state of altered immunity. diarrhoea and steatorrhoea which causes faeces to be yellow-
Immunity is based on both humoral and cell mechanisms, ish and fatty. Frequency of emission is often increased, from
and antibodies and effector cells may cooperate to eliminate one to five or six times a day. Abdominal pain is perceptible
the parasite. Specific antibodies have been found in humans on palpation. The overall condition of the animal will gradu-
and mice, IgA and IgG in particular. They are transmitted ally deteriorate and weight loss will occur as the animal gen-
through the mother’s milk and determine the resistance of erally retains its appetite but will be polydipsic.
unweaned mice from mothers which have been infected. The
local lymphocyte reaction also seems to play a role in eliminat-
ing the parasites, and causes epithelial lesions (atrophied villi).
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Lesions
Giardiosis lesions vary greatly in severity and location. The elements which are sometimes difficult to see, corresponding
intestinal villi are the site of massive lymphocyte infiltration to two to four nuclei and fragments of flagella. Stains which
and a mixed inflammatory reaction involving macrophages, are fixed by the cyst walls can be used so that internal struc-
granulocytes and lymphocytes can also be seen. Parasites are tures can be seen more easily. It is then possible to distinguish
sometimes found in the lamina propria and necrosis at the the cysts on first observation of the slide at a low magnifica-
apex of the villi has been described in dogs. tion (×100 = obj. 10). Lugol’s iodine solution is useful and
and is made up of 10 g sublimated iodine, 50 g potassium
Diagnosis iodide and water qs 100 mL. A drop of iodine on the edge
Clinical diagnosis is difficult, as only the steatorrhoea and of the slide is all that is required and this will make Giardia
chronic diarrhoea which develops over a number of days cysts take on a very clear orange hue (Fig. 2). Merthiolate-io-
or weeks, punctuated by phases of remission, will indicate dine-formaldehyde (MIF) is another iodine-based stain
giardiosis. which is used in human medicine and can also be used to
Diagnosis must differentiate between giardiosis and bac- detect parasites. Iodine does not colour coccidial oocysts or
terial enteritis, which is usually accompanied by fever, and sporocysts, and facilitates differential diagnosis of Giardia
exocrine pancreatic insufficiency, which presents a very sim- cysts.
ilar clinical picture in young dogs. These cysts can also be seen on duodenal smears during
Confirmation is based on identification of Giardia cysts in endoscopy, but this method requires more equipment and is
the faeces. Elimination of the cysts may be variable, which is more difficult than faecal examination. It also does not nec-
why a second test should be carried out about a week after a essarily provide more accurate results.
negative faecal examination. Elimination of cysts is generally
massive in clinical giardiosis, and they are easily identified
using coproscopy after enrichment, but the number of cysts
is much lower in asymptomatic carriers.
Giardia cysts are more or less rounded, approximately
8 × 12 µm in size, therefore not easily visible with the ×10
objective lens used for helminth eggs. They are quite light in
colour, with a thin, smooth shell, and enclose a number of
GASTROINTESTINAL PARASITOSES
Immunological diagnosis is possible: disinfecting floors. Cysts are very sensitive to quaternary am-
• By direct immunofluorescence assay: monoclonal anti- monium (the majority of common commercial disinfectants),
bodies which allow Giardia cysts to be detected by im- but appear to be fairly resistant to chlorine (bleach). During
munofluorescence assay are available. This technique is as epidemics in communal housing, the carriers must be treated
effective as the flotation method of faecal examination for as well as the sick animals, so they must all be screened.
detection of Giardia cysts in humans but a fluorescence Giardiosis is probably the most common intestinal proto-
microscope is required, which limits this test to specialised zoan disease in carnivores but its prevalence is underestimat-
laboratories. ed due to the limited number of faecal examinations carried
• Using an ELISA kit to detect the coproantigens present in out in veterinary clinics. The technique is actually easy, and
faecal matter from infected individuals. does not necessarily require expensive equipment, such as a
centrifuge. Finding evidence of Giardia cysts is facilitated by
Control measures staining with iodised solutions.
Treatment An inactivated vaccine has been marketed in some Amer-
The outcome is favourable after a course of symptomatic ican countries over the past few years but there have been
treatment (mucosal protective agents, antispasmodics) and contradictory reports on its efficacy.
specific therapy. The latter will almost certainly consist of
either metronidazole, or certain benzimidazoles. Risk to humans
Metronidazole may be administered at a dose of 20 mg/ Many arguments insist on the zoonotic nature of some
kg per os twice a day for 10 days. According to the studies strains/genotypes of G. duodenalis but not all:
published, efficacy varies from 100 % down to 67 % and • Giardia from humans can be transmitted to various ani-
adverse reactions, such as nausea, vomiting and ataxia, have mal species in the laboratory.
been described. • There is a strong antigenic similarity between isolates from
A number of benzimidazoles have been shown to be animals (cats, beavers, sheep, muskrats, dogs) and those
90 to 100 % effective and use of these drugs could be advan- from human patients.
tageous because of their excellent safety, even at high dos- • Morphometry is identical.
es. Fenbendazole (50 mg/kg), oxfendazole (11.3 mg/kg) and • There are significant genetic similarities between isolates
febantel (15 mg/kg) administered for 5 consecutive days all of animal and human origins, as restriction fragment
demonstrated their efficacy. length polymorphism (RFLP) studies using DNA imprints
Treatment failure, or the persistence of cysts in faeces is or sequencing have shown.
mainly attributable to almost immediate reinfection. Indeed, • Electrophoretic profiles were very close to identical in most
dogs undergoing treatment continue to ingest cysts which of the enzyme groups studied, but there were variations
develop very rapidly (in 2 to 3 days), so when the dogs are between geographical isolates.
placed in clean kennels (washed and disinfected), treatment • Various epidemiological studies have shown that animals,
is much more effective. Recontamination in dogs belonging especially carnivores, have acted as parasite sources for
to private owners is much less common, so treatment results humans.
are good and relapses are rarer.
However, genetic studies tend to show that different popula-
Prevention tions of the parasite G. duodenalis are more or less adapted
Prevention is limited in carnivores but possible with human to each type of host. Studies of Giardia DNA and isoenzymes
giardiosis, through measures to ensure that drinking water is from humans and dogs discovered different characteristics.
clean. In cat or dog kennels, treatment is based on keeping It should be accepted that Giardia of animal origin may
cages clean and dry (by frequent removal of faecal matter) and infect humans.
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5 μm
Figure 1. Cytological preparation of cultured feline Tritrichomonas foetus. Stained with Wright-Giemsa and photographed at
×100 magnification. (a) Anterior flagella, (b) undulating membrane, (c) posterior flagellum, (d) axostyle, (e) nucleus.
* From chapter originally written by Jody Gookin for the book Parasitoses and Vector Borne Diseases of Cats. Ed. Merial, 2015. Pictures from Jody Gookin.
TABLE OF
CONTENTS Intestinal parasitoses 81
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GASTROINTESTINAL PARASITOSES
little evidence for venereal transmission of T. foetus in cats. isolates revealed a single-nucleotide polymorphism that dis-
Studies conducted on the reproductive organs of purebred tinguishes feline isolates from those of cattle and pigs. Mo-
cats where a high prevalence of intestinal T. foetus infection lecular sequencing also revealed 10 distinct genotypic poly-
was identified, found no light microscopic, immunohisto- morphisms between the T. suis/T. foetus “cattle genotype”
chemical or molecular evidence of T. foetus colonisation. In- and the T. foetus “feline genotype” for a total of 1.03 %
fection of the uterus with T. foetus was reported in one cat, difference between genotypes from these hosts, with the
although it was unclear whether T. foetus was a primary or greatest difference recorded for the cysteine protease (CP)
opportunistic pathogen. From these data, it is unlikely that genes. From this and other data, it has been concluded that
reproductive tract infection with T. foetus plays a significant the feline and cattle isolates may be divided into two distinct
role in transmission of the disease or is a frequent cause of genotypes so it has been proposed that the feline trichomon-
reproductive tract pathology in breeding catteries. ad be renamed T. blagburni based on molecular analyses,
host specificity and pathology.
Relationship between feline and bovine Unlike in the cross-transmission studies between pig and
Tritrichomonas foetus and porcine cattle trichomonads, experimental infection of cattle with a
Tritrichomonas suis feline T. foetus isolate resulted in a similar, but not identical,
There has been considerable debate regarding the relation- course of colonization of the vagina, cervix and uterus but
ship between feline and bovine isolates of T. foetus and less endometrial pathology than caused by bovine T. foetus.
porcine T. suis. T. foetus is a well-recognised cattle path- When cats were infected with a bovine T. foetus isolate, the
ogen and is sexually transmitted from bull to cow. In the researchers reported that the bovine isolate was less patho-
cow, T. foetus infects the vagina, cervix and uterus and may genic for cats than the feline isolate.
cause mild infection or more severe sequela including vag-
initis, early abortion, and occasional pyometra, resulting Pathogenesis
in permanent infertility. The porcine trichomonad T. suis Great progress has been made in the past 15 years in deter-
colonises hollow organs, including the nasal cavity, stom- mining the molecular identity and genetics of feline T. foe-
ach, small and large intestines and caecum in pigs. It had tus and in developing diagnostic tests and, to some extent,
previously been described as a pathogen possibly associated effective treatment for this infection. However, very little is
with rhinitis in pigs but additional research has now shown known about how these organisms actually cause diarrhoea.
it to be a harmless commensal in that host. The trichomon- Based on what is known about the pathogenic mechanisms
osis first described in cats in the late 1990s was identified of bovine T. foetus in the reproductive tract and what can be
as T. foetus from a limited molecular comparison between observed in cats infected with feline T. foetus, multiple path-
bovine and feline isolates. ogenic factors are likely. Pathogenic factors associated with
Based on a plethora of comparisons, including cross-infec- Trichomonas infection include interaction with endogenous
tivity studies, virulence assays, molecular analysis, geograph- bacterial flora, adherence to host epithelium, and production
ical distribution, morphological characteristics and immuno- of cytotoxins and enzymes. Infecting specific-pathogen-free
logical analysis, there appears to be no significant difference cats with cultures of feline T. foetus results in chronic colo-
between the bovine T. foetus “genotype” and porcine T. suis. nisation of the terminal ileum, caecum, and colon, and large
Infecting cattle with T. suis resulted in similar pathology to bowel diarrhoea similar to that observed in naturally infect-
infection with the bovine parasite, and pigs have been found ed cats. In cats infected naturally, T. foetus is found in the
to be easily infected with the cattle trichomonad. The conclu- superficial mucus and in contact with the surface epithelium
sion is that these “sister species” are synonymous. of the caecum and colon. Uptake of T. foetus antigens by
Recent studies have demonstrated significant genetic the colonic surface epithelial cells can also be demonstrat-
differences between the T. suis/T. foetus “cattle genotype” ed. Histologically, this is associated with the infiltration of
and the T. foetus “feline genotype”. Sequencing the ITS- lymphocytes, plasma cells, and neutrophils into the colonic
1 - 5.8 DNA gene through ITS-2 of both cattle and feline lamina propria.
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Clinical signs
Feline T. foetus infection is characterised by waxing and
waning diarrhoea that often contains fresh blood or mu-
cus. Diarrhoea is semi-formed to a “cow pat” consistency
is and malodorous. In most cases, infected cats maintain
good health and body condition which presumably reflects
confinement of the infection to the colon. However, some
kittens develop faecal incontinence and overt swelling and
inflammation of the anal region from faecal scalding (Fig. 2).
Cats with diarrhoea and concurrent T. foetus infection are
generally young but can range widely in age. Older infect-
ed cats may be clinically healthy or may have a long history
of diarrhoea since they were a kitten. Cats originating from Figure 2. Faecal incontinence and anusitis in a kitten with Tritricho-
catteries (i.e., pedigrees) or shelters appear to be at increased monas foetus colitis and chronic diarrhoea.
GASTROINTESTINAL PARASITOSES
Direct faecal smear
For a direct faecal smear examination, commonly known
as a “wet mount”, a small amount of faeces is diluted with
saline solution and examined under a coverslip using a light
microscope equipped with a 20× or 40× objective. Lowering
the microscope condenser will increase contrast and enhance
visualization of any trichomonads (Fig. 3). Trichomonad tro-
phozoites are almost identical in size to Giardia and must be
carefully distinguished. Giardia trophozoites have a concave
shape similar to a rose petal and sluggish motility reminis-
cent of a “falling leaf” but Trichomonads are shaped like a
teardrop and possess an undulating membrane that courses
the entire length of the body. They are also vigorously motile. Figure 3. Faecal wet mount taken through the ocular lens of a
Where there is difficulty distinguishing trichomonads from light microscope. Copious tear-drop shaped trichomonads can be
observed at various depths in the saline solution.
Giardia spp. trophozoites, a Giardia antigen test can be per- Courtesy of Bronya Redden.
formed on the faeces. The presence of trichomonads will not
cause a positive Giardia antigen test result. However, it is
important to recognise that co-infection of cats with Giardia
spp. and T. foetus is common, so a positive Giardia antigen
test result does not rule out the possibility of a co-infection
with T. foetus.
A direct smear examination is the easiest way to diagnose
trichomonosis; however it is also the least sensitive. T. foe-
tus can also be difficult to distinguish from non-pathogenic
intestinal trichomonads, such as Pentatrichomonas hom-
inis based on light microscopic examination of live organ-
isms only. Feline trichomonads are generally presumed to be
T. foetus in cats. P. hominis can be distinguished from T. foe-
tus by species-specific PCR testing if necessary.
Faecal culture
If repeated direct microscopic examination is negative for
trichomonads, faeces may be cultured using commercially
available pouches (such as the In Pouch TF-Feline system
from Biomed Diagnostics) (Fig. 4). Faecal culture using In
Pouch TF is more sensitive than direct faecal smear exam-
ination for T. foetus diagnosis. The pouches are made of
clear plastic and contain a proprietary culture medium
and antibiotics that suppress unwanted bacterial growth.
For diagnosis of feline T. foetus, the pouches should be Figure 4. Pouch system for the culture of Tritrichomonas foetus.
inoculated with 0.05 g (approximately the size of a rice
grain) of faeces and incubated in an upright position at ei-
ther 37 °C / 98.6 °F or room temperature (25 °C / 77 °F).
Trichomonads multiply quickly at 37 °C and many organ-
isms can be observed by light microscopy within 72 hours.
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GASTROINTESTINAL PARASITOSES
Other therapies for the treatment of T. foetus in cats are If left untreated, it is estimated that diarrhoea in most cats
limited. Many approaches to diarrhoea control have been (88 %) with T. foetus infection will resolve spontaneously
tried without success, including changes to the diet, use of within 2 years (median 9 months; range 5 months to 2 years).
different antimicrobials, and supplementation with nutra- However, most of these cats will still be infected, based on
ceuticals and probiotics. However, there have been no con- positive PCR test results for T. foetus and may therefore be
trolled studies of any of these therapies. It has been suggested sources of infection for other cats. The role of these “asymp-
that frequent changes in diet and indiscriminate use of an- tomatic carriers” in disease transmission is unclear, but these
timicrobials prolong the time it takes for cats to resolve the cats can suffer a full recurrence of diarrhoea that is teeming
diarrhoea on their own. Vets should be careful of embracing with trichomonads as much as 6 years after onset of their
any particularly successful antimicrobial drug as treatment clinical “remission”. Any cat carrying T. foetus should be
for T. foetus infection because many drugs merely suppress therefore be considered a potential source of infection, and
detection of the organism rather than eradicating it. screening for these cats appears to be warranted for the sake
of preventing disease transmission. No studies have been car-
ried out, and there is currently no evidence to suggest any
long-term adverse health effects of asymptomatic T. foetus
infection in cats.
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Opisthorchidoses
General comments
Carnivores can be infested by trematode flukes, which are The first intermediate hosts are aquatic snails, mainly
parasites of the liver and bile duct, particularly in Asia. These of the genus Bythinia (B. leachi), and many fish (cyprinids:
flukes belong to the family Opisthorchiidae, hence the name tench, carp, pike, etc.) are second intermediate hosts for the
of the disease, opisthorchidosis. Infestation is usually asymp- infective metacercariae.
tomatic and the significance of these diseases is mainly due Clonorchis sinensis: this small fluke, called the Chinese
to their prevalence in certain areas (where more than 80 % fluke or the Oriental liver fluke, measures 5–12 × 1–2 mm
of dogs and cats are infested) and to the subsequent public and is commonly found in carnivore bile ducts in the Far
health risk, as most species are zoonotic. Carnivores ensure East. The fluke lays small eggs with opercula measuring
the survival of these Asian flukes and are the main reservoir 25 × 15 µm. As is the case with Opisthorchis, the first inter-
of the parasites. mediate hosts are aquatic snails, mainly of the genus Bythin-
Opisthorchis felineus and Opisthorchis viverrini meas- ia, and many fish, especially cyprinids, are second interme-
ure 10–18 × 2 mm, and are reddish when fresh, with a diate hosts.
non-branching caecum and lobed testes located at one end Metorchis albidus and Metorchis bilis: these small par-
(Fig. 1). They shed eggs measuring 26–30 × 10–15 µm that asitic flukes measure 5.5–4 × 1–2 mm (Fig. 3) are found in
have a characteristic operculum (Fig. 2). Central Europe, where they live in the gall bladder of wild
They are parasites of the bile ducts in domesticated and carnivores (foxes, wildcats), and sometimes in domesticated
wild carnivores (such as raccoon dogs), as well as humans. cats. They lay eggs measuring 30 × 15 µm. As in the two
They are mainly found in Southeast and Central Asia, but previous flukes, the first intermediate host is an aquatic snail,
cases have been reported in Eastern Europe, as far west as and the second intermediate host, which harbours the meta-
Germany. cercariae, is a cyprinid fish.
100 μm 200 μm 1 mm
GASTROINTESTINAL PARASITOSES
Epidemiology Clinical signs and diagnosis
Opisthorchiidae are parasites of ichthyophagous mammals The disease is usually asymptomatic in infested carnivores
and are not very host-specific, so they infest not only domes- but, liver failure and gastro-intestinal disorders can be seen
ticated and wild carnivores, but also pigs and humans. in heavy infestations, and the disease can develop into cirrho-
They are very common in Asia, where several million hu- sis and jaundice.
mans and carnivores are infested each year, and several out- After several years, chronic infestation can lead to liver
breaks have also been reported in Europe. cancer, which has a poor prognosis.
More than 7 million humans in Central Asia (mainly in Diagnosis is made by faecal examination, revealing the
China and Russia) are infested by C. sinensis. 113 species of characteristic eggs (Fig. 4).
fish have been listed as hosting the metacercariae and nine
species of snails as the first intermediate hosts. Control measures
In Southeast Asia, more than 7 million Thai people and Treatment is with praziquantel, at 75 mg/kg per os in 3 indi-
2 million Laotians are infested by O. viverrini. vidual doses on the same day, which is 25 times the normal
In Russia, more than 2 million people are infested by cestodicide dose (5 mg/kg).
O. felineus. Indigenous outbreaks were reported in East Ger- Prevention in domesticated carnivores entails simply pre-
many in 1996 and confirmed in 1999, with 32.5 % of foxes venting the consumption of raw or undercooked fresh-water
infested (6.7 % by O. felineus and 28.1 % by M. bilis). fish.
A B
50 μm 2 mm
D.H.
Dog, cat, fox, pig, human
and some wild mammals
D.
un H. i
de ng
rc est
oo s
ke raw
d
fis or
h
Prep s
4 we
small intestine and migrate to the
atent
ek
bile duct and gall bladder, where
Encyst and persist for
pe
the life of the fish
riod:
Faeces
6–8 weeks s
onth
to m
ct
I.H. (fresh infe
ively
Days
ct
water fish) ae a in fish
cari
Da Sporocyst
Cer encyst ys
to
d Miracidium Sn Embryonated
an we ail
e ks Rediae ea egg
ts
eg
g,
be
co
m
ing
inf
ec
Cercariae ted
il
sna
Cercaria
exit
iae
INTERNAL
NON‑GASTROINTESTINAL
PARASITOSES
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Table 1. Geographical distribution and vectors of the various Babesia and Theileria species infecting dogs worldwide.
Mainly Asia,
Haemaphysalis longicornis in Asia
Babesia gibsoni Small USA, South America,
elsewhere?
Australia, Europe
Babesia conradae Small Rhipicephalus sanguineus? USA (California)
Figure 1. Babesia canis. Round intraerythrocytic forms. Figure 2. Babesia canis. Intraerythrocytic bigeminated forms.
Blood smear, Stevenel’s blue stain. Blood smear, MGG stain.
10 μm 5 μm
Figure 3. Babesia canis. Intraerythrocytic bigeminated forms, Figure 4. Blood smear, MGG stain, showing small round
showing four elements resulting from binary divisions. intraerythrocytic element (diameter smaller than the radius of the
Blood smear, MGG stain. erythrocyte), indicating a small Babesia, type Babesia gibsoni.
I.H.
Vertebrate
Kinete migrates to the
salivary glands, developing
into infective sporozoites
Infe
ctio
Transstadial transmission:
nd
larvae, nymphs, adults
urin
g tic
k fe
edin
g
transmission
Transovarial
Sporozoite
penetrates
the host’s red
blood cells
ays
4d
7–1
Kinete
Tick
Gamont Zygote
inges
Multiply, rupture
and infect other red
ts inf
Epidemiology
Geographical distribution and epidemiological characteris- the activity of the ticks that cause it. However, this may
tics are linked to the biology of each tick vector (Fig. 6). change drastically with the appearance of the endophilic
Babesiosis due to B. canis is widespread in France, tick R. sanguineus, which is found in kennels and can be
Northern Italy, Spain, Belgium, Germany, Austria, Swit- active all year round.
zerland and Eastern Europe (Hungary, the Czech Republic, Babesia and Theileria are fairly specific parasites: B. canis
Slovenia), but distribution follows a heterogeneous mosaic is a parasite of canids. Frequently observed in young dogs,
pattern. Babesiosis is a seasonal disease (peak in spring and babesiosis particularly affects “outdoor dogs” (hunting/farm
autumn); the cold of winter and drought in summer reduce dogs, etc.) that are exposed to tick bites.
Transstadial
tio
n
transmission
du
rin
gt
Asexual multiplication
ick
Lymphocyte
g
with schizont
Schizonts
rupture releasing
merozoites, which
invade red blood
cells
Weeks to months
Days to weeks
Merozoite
The parasite
colonizes the tick
gut cells where it Merozoites reproduce
reproduces sexually asexually, then invade
new red blood cells
Tick ingests infected
D.H.
Hard tick
blood
Other forms, which vary greatly in their clinical expression, Clinical signs of small piroplasm infection
are described below: After an incubation period of a few days, the clinical pres-
• Locomotor forms: unsteady gait, lower back and joint entation is similar to the typical form of babesiosis due to
pain, paresis, paralysis, ataxia. B. canis, but more intense.
• Cerebral and ocular forms: convulsions, nystagmus, an- The animal presents with hyperthermia (generally over
isocoria, behavioural changes and coma. This form is 40 °C) lasting for at least a week and associated with an-
sometimes followed by complete recovery without relapse. orexia and depression. Bilirubinuria is present, sometimes
• Intestinal and respiratory forms. accompanied by haemoglobinuria. Anaemia is confirmed by
• Renal forms; oliguria, anuria, haemoglobinuria, accompa- a marked paleness of the mucosae. Intestinal problems, such
nied by renal insufficiency syndrome. as vomiting and diarrhoea, may be seen. Death may occur
• Vascular, cutaneous and mucosal forms: oedema, diffuse within a few days (acute renal insufficiency, shock, hypovol-
haemorrhaging, purpura, stomatitis, haematoma (attribut- aemia, haemorrhaging).
able to severe thrombopaenia), cutaneous ulcers and ne- Significant changes in blood and urine values indicate
crosis of the extremities. renal insufficiency: hyperazotaemia, hypercreatininaemia,
proteinuria and haematuria. Clinical reports on dogs in-
Development of these diverse forms is very variable: fected by B. vulpes (T. annae) reveal abnormally high serum
• Recovery without relapse is possible, even without treat- concentrations of urea and creatinine, with elevated concen-
ment, either because the animal has an effective natural trations of inorganic phosphorus, hypoalbuminaemia, hy-
resistance or because it is infected by a strain that is not percholesterolaemia, proteinuria, a high protein/creatinine
very pathogenic. ratio. The presence of hyaline and granular casts on micro-
• Death from shock or acute renal insufficiency following scopic examination of urine sediment suggest a glomerular
the onset of jaundice. component to the disease.
• All situations between these two extremes are possible: Severe hyperchromic and regenerative anaemia (raised
rapid or slow recovery after treatment, more or less fre- reticulocytes, Howell-Jolly bodies counts), moderate leuko-
quent relapses, apparent recovery followed by a new bout cytosis and thrombocytopaenia are almost constant charac-
due to immunosuppression after surgical intervention teristics of infection with small piroplasms in dogs. Azotae-
(such as hysterectomy) or some other infection, etc. mia is also seen in many cases. Anaemia is attributable to
erythrophagocytosis (extravascular haemolysis, an autoim-
Lesions mune process confirmed by the presence of anti-erythrocyte
• Splenomegaly: congested, hypertrophied spleen, dark membrane antibodies).
red in colour due to the process of extravascular
erythrophagocytosis. Diagnosis
• Bilateral nephritis: congestion, necrosis and subcap- Diagnosis is based on epidemiological elements (seasons and
sular haemorrhages, glomerulonephritis and tubular areas of tick activity, age of the animal, etc.) and clinical signs
degeneration. (combination of pyretic and haemolytic syndromes, etc.).
• Hepatic centrilobular degeneration. However, piroplasmosis must sometimes be differentiated:
• Vasculitis, haemorrhaging, pulmonary and subcutaneous • From other causes of anaemia, such as poisoning by roden-
oedema, ascites, and capillary embolism causing ischae- ticides, canine monocytic ehrlichiosis, immune-mediated
mia and necrosis. These can affect various tissues and or- haemolytic anaemia, etc.
gans, such as the skin, lungs, kidneys, liver, brain, spinal • From other causes of fever, depression, anorexia, etc.
cord, etc. • From other piroplasmosis: it is important to differentiate
piroplasmosis caused by a small form from piroplasmosis
caused by a large form because this will affect the choice
of treatment.
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the likelihood of recovery is significantly different when treat- Treatment of small piroplasm infection
ment is carried out following the same protocol as would be It is more difficult to treat babesiosis caused by small forms
used for immunocompetent or immunosuppressed animals. than large forms. The piroplasmicides available appear to be
The inability of certain dogs to acquire cellular mediated im- less effective against these small forms.
munity to seems to explain this phenomenon. Various combined strategies for treating small piroplasms,
It is essential to combine symptomatic treatment of sus- especially B. gibsoni have been described in dogs. However,
ceptible individuals (old animals, or those with a history of relapses after administration of some combinations of an-
piroplasmosis, or suffering from another pathology, etc.) with ti-babesia drugs are common and pose significant challenges
specific treatment: blood transfusion diuretics, isotonic sodi- to veterinary surgeons. In Asia, atovaquone (ATV)-resistant
um chloride solutions administration of corticoids to control strains of B. gibsoni are an additional challenge. Combina-
glomerulonephritis due to deposition of immune complexes tions of drugs appear to be a better choice for treating in-
(for example, prednisolone 1–2 mg/kg/day for 1 week). fection by small piroplasms. Different protocols for specific
All treatment (specific and symptomatic) must be accom- treatment are shown in Table 2.
panied by a biological and clinical follow-up appropriate to
the state of the animal (blood count, blood urea and creati-
nine levels, proteinuria, etc.).
Table 2. Protocols for the control of large and small piroplasms in dogs.
IM or SC
Transstadial transmission:
nd
Sporozoite
penetrates
the host’s red
blood cells
ays
4d
7–1
Kinete
Tick
Gamont Zygote
inges
Multiply, rupture
and infect other red
ts inf
* Chapter inspired by the original chapters written by Prof. Adam Birkenheuer (chap. 3–02), Gad Baneth (chap. 3–03), Luis Cardoso and Banie Penzhorn
(chap. 5–03) in Guide to Parasitoses and Vector Borne Diseases of Pets. Ed. Merial, Lyon, 2013.
TABLE OF
CONTENTS Blood parasitoses 107
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I.H.
Vertebrate
Tick salivary
du
glands
rin
Sporozoite
gt
ick
fee
din
g
Macrophage
(with schizont)
The parasite
colonizes the
cells of the
intestine and
undergoes
sexual
reproduction
d
oo
bl
ed
ct
fe
in
Merozoites
sts
ge
in
k
Tic
D.H.
Hard ticks:
} Dermacentor variabilis
} Amblyomma americanum
Piroplasms in
red blood cells D.H. = definitive host
I.H. = intermediate host
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Table 1. Geographical distribution and vectors of the (Fig. 1). In some regions where cytauxzoonosis is enzootic,
various piroplasm species infecting cats worldwide. the prevalence in domestic cats may be as high as 30 %. An
endemic focus of Cytauxzoon spp. infection in domestic cats
Geographical
Species Vectors has been described recently in the Northwest region and
distribution
Babesia felis ? South Africa
infection in feral cats was 30 %. However, no associations
between breed, gender, age, presence of ticks and/or fleas,
Babesia cati ? India
clinical status, laboratory findings such as anaemia, FIV and/
Babesia lengau ? Africa or FeLV status and mortality rate were found.
Babesia herpailuri ?
South Most cats affected by babesiosis due to B. felis seem to be
America
young adults under 3 years old. No breed or sex predispo-
Babesia canis
Rhipicephalus sanguineus? Israel
sition is evident, but Siamese cats may be over-represented
presentii
among purebred cats.
North and
Amblyomma americanum,
Cytauxzoon felis South
Amblyomma cajennense?
America
Clinical signs
Cytauxzoonosis
Acute cytauxzoonosis is characterised by disseminated par-
October, which corresponds well with peak tick activity. It asitic thrombosis, a severe systemic inflammatory response
has been speculated that cytauxzoonosis in the Americas and multi-organ dysfunction or failure. It is assumed that
represents a “species jump” from bobcats to domestic cats. sporozoites infect a cell of myeloid origin, although the spe-
The prevalence of C. felis in bobcats ranges from 0 to 79 %, cific myeloid lineage of this cell (CD34+ blast, monocyte,
depending on their geographical location. Bobcats are not macrophage, dendritic cell or Langerhans cell) remains un-
believed to develop severe disease symptoms, but this is based known. Although it is known how merozoites develop from
on an extremely small number of experimental infections. schizonts in infected cells, the specific mechanisms by which
The specific cause of mortality in bobcats, particularly kit- sporozoites target cells, and whether or not schizont-infect-
tens, is poorly defined. The reason for the “species jump” ed cells replicate, remain a mystery. The ability to transmit
and subsequent emergence of C. felis in domestic cats re- disease by serial passage of small volumes of infected tissue
mains unknown. Changes in distribution of the tick vector suggests that there is either a subset of schizont-infected cells
(A. americanum) and host-parasite adaptation, making that replicate, similar to Theileria spp., or there is “lateral
domestic cats a viable reservoir host for C. felis appear to transmission” of schizonts from one myeloid cell to another.
be plausible causes. Domestic cats should no longer be con- Serial passage of sporozoites or continued sporogony in the
sidered dead-end hosts, and may in fact be the most impor- vertebrate host seems least likely. Understanding the mecha-
tant reservoir host for new infections in other domestic cats nisms behind the infection of myeloid cells, and the source of
15 μm 15 μm
Figure 1. Babesia felis in a blood smear from a cat in George, South Africa. MGG stain. Courtesy of Tanya Schoeman.
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50 μm
Infected cats present raised concentrations of pro-inflamma-
tory cytokines, including tumour-necrosis factor α and inter- Figure 2. Schizont of Cytauxzoon felis shown in a cross section
leukin-1 β8. The course of the disease is short and, without of infected tissue stained with H&E. Courtesy of Adam Birken-
heuer.
treatment, many cats succumb within 5 days of the onset of
clinical signs.
Acute cytauxzoonosis is characterised by acute fe- constipation and pica. Parasitaemia is variable and can
brile illness. The results of physical examination are often be very low or extremely high. The strong correlation be-
non-specific. Cats usually have a high fever, but hypother- tween central and peripheral parasitaemia indicates that
mia may be observed in moribund animals. Cats are usu- sequestration is not a feature of the disease. Macrocytic,
ally depressed, and vocalization (a so-called death yowl) is hypochromic, regenerative anaemia is the most consistent
common in advanced cases. Dyspnoea is a prominent clin- haematological finding, although not present in many in-
ical feature or the main symptom in some cats. Lymphad- fected cats. When present, anaemia can become severe in
enopathy and splenomegaly are common but not universal advanced cases, is haemolytic, presumably resulting from
findings, and some cats will be jaundiced. On presentation, both intravascular and extravascular erythrolysis. Other
laboratory test abnormalities may include non-regenerative changes in the cell blood count are inconsistent and may
anaemia, leukopaenia, thrombocytopaenia, hyperbilirubi- indicate concurrent illness or infection.
naemia and bilirubinuria, raised liver enzyme levels (often The most significant clinicopathological changes are
not as severe as would be expected considering the degree raised hepatic cytosolic enzyme activity and increased total
of hyperbilirubinaemia), hyperglycaemia and hypoalbumi- bilirubin concentration. Serum alanine transaminase is sig-
naemia. Thrombocytopaenia and neutropaenia are the most nificantly elevated in most cases, but alkaline phosphatase
common complete blood count findings. Coagulation test and gamma-glutamyl transferase are generally within nor-
results are consistent with disseminated intravascular co- mal limits. This provides evidence of primary hepatocellular
agulation secondary to consumption of platelets and coag- damage or inflammation in feline babesiosis. The hyperbil-
ulation factors. Despite significantly increased prothrombin irubinaemia is probably due to haemolysis, but secondary
and activated partial thromboplastic times, and very reduced hepatocellular damage is probably an additional contribut-
platelet counts, clinical bleeding is rare. Many of the typical ing factor. Renal damage is not a consistent feature of the
laboratory abnormalities become more pronounced as the disease.
disease progresses (Fig. 2).
Diagnosis
Babesiosis due to Babesia felis Diagnosis of piroplasmosis in cats is based on epidemiology
Unlike babesiosis in dogs, feline babesiosis is generally not (region and season of tick activity) and clinical presentation
associated with pyrexia. Anorexia, lethargy and weight (combination of haemolytic and pyretic syndromes), as it is
loss are often the first signs observed by owners. The most in dogs. Confirmation relies on blood smears, stained with
common clinical signs are anorexia, listlessness and anae- MGG to reveal parasitic elements. The presence of parasites
mia, followed by icterus. Less common signs are weakness, in the blood is synchronous with hyperthermia phases.
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Serology with indirect immunofluorescence is not diag- Two doses of imidocarb diproprionate 2–4 mg/kg IM
nostically useful since antibodies are only detectable after at an interval of 15 days has not proven to be as effective.
approximately a week, and their presence only confirms con- Side-effects include pain at the injection site and cholin-
tact between host and parasite. The possibility of cross-reac- ergic reactions. The use of diminazene aceturate has been
tion with B. canis cannot be ruled out. proposed.
Diagnostic techniques involving PCR from a blood sample Supportive care is the basis of all therapy for cytaux-
now allow the various species of Babesia to be distinguished zoonosis. This includes maintaining hydration and blood
and even studied. However, this is more for epidemiological volume, supplementing oxygen in patients with respiratory
interest, and to screen parasite carriers, than to carry out an compromise, administering anti-coagulant/platelet drugs
urgent diagnosis. and providing nutritional support. Clinical recovery is slow,
Rapid diagnosis is critical for cytauxzoonosis. Microscopic and most patients deteriorate during the first 24–48 hours,
identification of C. felis remains the diagnostic test of choice. gradually improving over the next few days. Minimising
An initial search for organisms can be performed by exam- handling and stress is recommended. Cats with severe res-
ining thin, stained smears of peripheral blood and in-house piratory compromise should be checked for pleural effusion
“quick stains” are usually adequate. The feathered edge by ultrasound, and therapeutic thoracocentesis should be
should be examined with low power (×100) first, to identify performed if necessary.
schizont-infected myeloid cells. These cells are easily confused With recent advances in treatment, the prognosis for acute
with clumps of platelets. High power (×500–×1000) inspec- cytauxzoonosis should be considered fair.
tion will reveal a very large single cell (50–250 μm diameter)
with an eccentric nucleus containing a single prominent nucle- Babesiosis
olus. The cytoplasm contains a parasite syncytium with a vari- Primaquine phosphate at 0.5 mg/kg is highly effec-
able number (tens to thousands) of basophilic particles stained tive, but often causes vomiting when administered oral-
magenta. These are the developing merozoites. Organisms in ly, and has proven lethal at doses exceeding 1 mg/kg.
red blood cells are most easily identified on a ×1000 magni- Despite its drawbacks, primaquine remains the drug of
fication. If organisms are not identified on peripheral blood choice. Repeated or long-term therapy may be required.
smears, fine needle aspiration and cytology of liver, spleen and Doxycycline may potentially improve treatment of this dis-
lymph nodes can facilitate a rapid diagnosis in suspected cases. ease (10 mg/kg PO, in 1 or 2 doses, for at least 10 consec-
Identification of schizont-infected myeloid cells confirms acute utive days). Concurrent symptomatic treatment is essential.
cytauxzoonosis and merozoite-infected red blood cells are a Although response to therapy is usually good, and premunity
supportive, but sometimes incidental, finding. PCR testing can is assumed to develop over time, mortality from feline babe-
be sensitive and specific but should not be considered as a re- siosis is estimated to be approximately 15 %.
placement for in-house microscopic diagnosis.
Prevention
Treatment There is no vaccine against cytauxzoonosis or other feline
Cytauxzoonosis babesiosis, so any method of reducing the risk of tick expo-
Treatment should be initiated within hours of admission and sure has to be considered and appropriate use of acaricides is
should be started empirically in suspected cases in enzootic essential if cats are allowed outside.
areas, even if a definitive diagnosis is not available.
A combination of atovaquone (15 mg/kg per os t.i.d. with
a fatty meal to facilitate drug absorption) and azithromycin
(10 mg/kg per os q.24.h.) is the current treatment of choice
for cytauxzoonosis. This combination should be adminis-
tered as a matter of urgency. A nasoesophageal feeding tube
should be inserted on admission, to facilitate medication and
nutrition.
TABLE OF
CONTENTS Blood parasitoses 111
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* Chapter inspired by the original chapters written by Prof. Gad Baneth in the books Guide to Vector Borne Diseases of Pets. Ed. Merial, Lyon, 2013;
and Parasitoses and Vector Borne Diseases of Cats. Ed. Merial, Lyon, 2015.
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5 μm
Figure 1. Heavy infection of polynuclear cells by Hepatozoon canis gamonts. MGG stain. Courtesy of Gad Baneth.
Epidemiology
Hepatozoon canis was first reported in India in 1905 and
has since been found in Southern Europe, Africa, the Middle
East, the Far East and South America. H. americanum was
initially considered a strain of H. canis, until it was described
as a different species in 1997. H. americanum is an emerging
10 μm
infectious agent in the USA. It seems that it spread from the
North and East of Texas, where it was reported for the first Figure 2. Infection of two polynuclear cells by Hepatozoon canis
time in 1978, to Louisiana, Alabama, Oklahoma, Georgia, gamonts. MGG stain.
I.H.
Dog, cat, other carnivores
Do
gi
nfe
Oocyst
cte
db
ye
Sporozoites
ati
migrate through
ng
intestine wall
tic
ks
~ 45 days in tick
s
ek
we
10
4–
od
blo
ted
D.H.
fec
Macroschizont with
ts in
macromerozoite
ges
Microschizont with
Tick
micromerozoites
(infect white blood cells)
5 μm
20 μm
Control measures
Imidocarb dipropionate at a dose of 5–6 mg/kg every 14 days
until gamonts are no longer present in blood smears has long
been considered the drug of choice to treat canine hepato-
zoonosis, along with toltrazuril, an anticoccidial drug (5 to
10 mg/kg/day per os for at least 10 consecutive days). Oral-
ly-administered doxycycline (10 mg/kg/day for 21 days) is
also used in combination with imidocarb. Elimination of H.
canis gamonts from the surrounding blood is a long process,
taking up to 8 weeks, and treatment failure is often reported.
H. americanum infection is treated with a combination of
oral trimethoprim-sulfadiazine (15 mg/kg every 12 hours),
20 μm
pyrimethamine (0.25 mg/kg every 24 hours), and clindamy-
cin (10 mg/kg every 8 hours) and treatment must be followed Figure 5. Hepatozoon americanum schizonts. H&E staining of a
muscle biopsy.
for several weeks. After remission of clinical signs, this treat-
ment can be prolonged by oral administration of decoquin-
ate (an anticoccidial) at 10–20 mg/kg mixed in food, every
12 hours for 2 years. Relapse is common, whether or not the
treatment period is respected. Symptomatic treatment of in-
fected dogs with anti-inflammatories relieves pain and fever
effectively.
Prevention is by reducing dogs’ exposure to ticks and us-
ing acaricides.
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occurs after a few years; the exact length of this period is The megaoesophagus and megaviscera reported in humans
not known. The acute, less common form is mainly found are not reported in the dog.
in the young dog and is rapidly fatal due to cardiac insuffi- African trypanosomosis induces either an acute, rapidly
ciency: collapse is sometimes preceded by breathlessness and fatal form, seen especially with T. congolense in non-native
fatigue, anorexia and diarrhoea. The chronic form is more dogs, or a rarer chronic form. Dogs are considered to be very
common and affects mainly adult or older dogs. It is charac- susceptible to infection with T. congolense and they develop
terised by adenomegaly, ascites combined with hepatomeg- more severe disease symptoms than other animals.
aly and splenomegaly due to right-sided heart failure, and The following signs have been reported in acute cases of
by various nervous manifestations (meningoencephalitis and 2 to 3 weeks’ duration: anaemia and jaundice, adenomegaly,
ataxia, suggesting distemper). It is linked to the development intestinal disorders (acute ulcerative stomatitis), ocular dis-
of dilated cardiomyopathy with ventricular arrhythmia. orders (photophobia, keratitis, uveitis and corneal oedema),
*
I.H.
Dogs and small mammals
1. B
ite from infected vector
ec
2. F
aecal contamination
tio
n
of wound or mucous
membrane by insect
3. E
ating vectors or infected
dead animal
2–
Trypomastigote
3
da
ys
Infective
Trypomastigote Epimastigote
trypomastigote
For T. cruzi, the
14–21 days resulting amastigotes
multiply in the host
cells, destroy the cells
and trypomastigotes
ays invade new cells
21d
7–
al
me
od
D.H. (biological
Blo
vector)
For the trypanosomes
(other than T. cruzi)
D.H. = definitive host only extracellular stages
I.H. = intermediate host are present
* Zoonotic trypanosomes: T. cruzi (from different mammals including dogs), T. brucei rhodesiense (from ruminants)
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100 μm 100 μm
Figure 2. Trypanosoma (trypomastigote form) in the blood of an Figure 3. Trypanosoma brucei in a blood smear. Courtesy of
infected animal. MGG-stained blood smear. Department of Veterinary Tropical Diseases, Faculty of Veterinary
Science, Pretoria.
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Respiratory
and circulatory
parasitoses
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122 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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Geographical distribution
Dirofilariosis is widely distributed worldwide though prev-
alence differs from one country to another, and even from
one region to another, depending on the density of mosquito
vectors and their seasonality.
Dirofilariosis is particularly common in tropical areas
(Africa, Asia, Australia, Central and South America, Pacif-
ic islands) where between 20 % and 60 % of dogs can be
infested, but it is also found in Canada, Japan, and most
other US states (although particularly in the south: Florida,
Louisiana).
It is also found in Southern Europe, particularly in the
Highly enzootic areas rea with no cases/imported
A
Mediterranean area (Spain, Italy and Greece) and in the far
Moderately enzootic areas cases
South of France (Provence), but it is sporadic here. It is enzo-
Derived from Morchón, 2012.
otic in Corsica, Sardinia and some Eastern European coun- Courtesy of Luís Cardoso, Robert Farkas, Domenico Otranto,
tries (Romania), although it is less common than the sub- Kurt Pfister, Xavier Roura, Smaragda Sotiraki, Donato Traversa,
Richard Wall.
cutaneous filarial nematode, D. repens in Northern Europe.
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D.H.
Dog
Microfilariae
develop into
L1, then moult
into L2, then
moult again into L3 develop into L4 larvae in 3 days.
10–14 days
47–67 days.
m
9
producing microfilariae
tp
en
at
ep
e od
Pr
I.H. mosquito
ria blo
ge fila ts
(Aedes, Culex,
sta icro ges
Anopheles)
n
rv g m o i
-la in uit
)
re in q
(p ta os
co e m
al
Th
n
Figure 2. Female mosquito of the genus Aedes, a vector of Figure 3. Mosquito of the genus Culex, a vector of Dirofilaria immitis
Dirofilaria immitis. in Europe.
D.H.
Cat
The larvae (L3) migrate
Th larv e in
L3 rfac
e m ae a d
os are rop
Infective L3 larva
the on olym
Larvae
(migrate to
ca the ph
ta
mosquito
nd skin
mouthparts)
10–14 days
Microfilariae
develop into L3 develop into L4 larvae in
L1, then moult a few days then the L4 larvae
into L2, then migrate through the tissues,
ion
into infective
ma
develop.
fe re g
do val
on
in (p stin
8m
ed ar
g
an iae ge
ct -l
6–
m lar y in
fro ofi b
ly icr ted
ike m c
t l g fe
os nin in
m ai is
), nt ito
Adults in heart
ge co qu
sta d os
and lungs
bl e m
Th
oo
Diagnosis
In enzootic areas, clinical suspicion is easy: the dog is tired,
and can present with shortage of breath and coughing, and
clinical signs get worse with effort (after going for a walk,
for example).
Examination of the blood shows regenerative anaemia.
Hypereosinophilia is possible but not symptomatic. Auscul-
tation and electrocardiograms (ECG) do not identify par-
ticularly characteristic elements but confirm the diagnosis of
right-sided cardiac insufficiency.
50 μm 100 μm
Figure 10. Microfilariae observed after concentrated MGG staining by the Knott method.
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CONTENTS Respiratory and circulatory parasitoses 129
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Figure 11. Histochemical staining of Dirofilaria immitis microfilaria. Phosphatasic acid activity (red stain) concentrated in the excretory pore
(anterior 1/3) and anal pore (posterior).
Direct examination between µF moving little in the field µF moving little in the field
µF moving very quickly in the field of view
slide and slip cover of view of view
One (red) spot at each end, For A. reconditum microfilariae: Diffuse activity;
After histochemical staining Area of posterior activity
corresponding to the anterior for A. dracunculoides: two zones of activity
and evaluation of acid corresponding to the anal
excretory pore and posterior similar to those observed with D. immitis but
phosphatase activity pore
anal pore smaller in size
Video 3
Live worms in the autopsy
of a dog that died of
heartworm disease.
50 μm
Figure 1. Binocular lens view of adult Angiostrongylus vasorum Figure 2. L1 larva of Angiostrongylus vasorum.
from a necropsy sample. Microscopic coproscopy.
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D.H.
Fox and dog
L1 larvae infest
molluscs, and Prepatent period: 8 weeks
develop into the
infective L3 stage
ys
da
Larva (L1)
6
–3
33
L4 larvae in the mesenteric lymph nodes on the 4th day. The source of parasites is wild or domestic canids, which
They then migrate through the lymphatic system towards the expel the larvae in their excrement.
right heart, into the arteries and pulmonary arterioles, where The mechanism of infestation is the ingestion of an in-
they evolve into pre-adults and adults. Ovigerous females termediate host, or perhaps a paratenic host (rodents,
appear from the 33rd day and excretion of L1 larvae in the batrachians).
faeces starts around 44 days after infestation (the prepatent The predisposing factors are those which promote con-
period in dogs is approximately 8–10 weeks). Prepatent peri- tact with intermediate hosts: hunting dogs appear to be es-
od in cats: 6–8 weeks. Parasite lifespan: up to 2 years. pecially at risk.
Like other metastrongylids, the life cycle of A. vasorum in- Clinical signs and lesions
cludes many species of slugs and snails as intermediate hosts: Clinical signs
• Slugs: Arion rufus, Arion ater, Arion lusitanicus, Dero- Angiostrongylosis usually causes a chronic illness.
ceras spp. • In the early stages, exercise intolerance, increasing breath-
• Snails: Helix aspersa, Helix pomatia and the Cepaea, Eu- lessness at rest, fatigability, and tachycardia are common-
parypha, Sucuinea, Lymnacea, Physa, Planorbis species, ly seen and the animal often presents with a bad hacking
etc. cough, accompanied by expectoration. Blood counts usu-
ally indicate hypereosinophilia (with 10–30 % eosino-
Paratenic hosts may be involved, as is the case with feline phils) and this initial phase may last several months.
aelurostrongylosis and a Danish study has demonstrated that • The late stage corresponds to the development of right-sided
the green frog, Rana temporaria, could be a paratenic host. cardiac insufficiency, associated with pulmonary disorders:
• Emaciated, prostrate, anaemic dogs.
Epidemiology • Dyspnoea and cough.
The prevalence of this parasitosis is little understood. It de- • Abnormal pulmonary and cardiac auscultation (pulmo-
velops sporadically but is not rare. Foxes could play a role as nary emphysema, respiratory frequency).
reservoirs: an epidemiological survey conducted in Hungary • Modified electrocardiogram.
found that 5 % of foxes were infested by A. vasorum and • Pulmonary and cardiac disruption visible by radiology
a similar survey in Italy found a prevalence of 34 % in this (Fig. 3).
species. • Eosinophilia.
A serological survey to evaluate the prevalence of antibod- • In the final stage, the dog may present with dependent
ies and antigens in the blood of a random sample of dogs oedema, ascites and cyanotic mucosae.
(4,030 animals) in the south of the UK showed that 1.32 %
of the dogs were antigen-positive, and 3.2 % were positive
for specific antibodies. The number of cases described in the
UK and Ireland has been increasing over the last 5 years,
which could be related to the increasing population of foxes
and their changing habits, as they become suburban or even
urban. Existing clusters of infection have been described in
South East England and South Wales. A survey of more than
1,400 vet practices across the country found that practioners
reported more than 20 cases of angiostrongylosis per year
in those areas. Vet practices in the affected areas are 15 to
16 times more likely to see clinical angiostrongylosis cases
than anywhere else in the UK.
Elsewhere, the disease is commonly described in hunting Figure 3. Radiographic examination: lateral view of the thorax of a
dogs which have been left to roam in forests and have prob- dog with clinical signs of angiostrongylosis. Right cardiac hypertro-
phy, and bronchi significantly more visible than normal.
ably eaten slugs.
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Figure 4. In situ localisation of adult Angiostrongylus vasorum in the Figure 5. Necroscopic heart and lung sample from a dog severely
lung of a dog. infested by Angiostrongylus vasorum.
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10 μm 50 μm
Figure 6. Angiostrongylus vasorum L1 larva. Microscopic coproscopy. Figure 7. Numerous Angiostrongylus vasorum L1 larvae and one
Trichuris vulpis egg. Microscopic coproscopy.
Video 4.1
Binocular lens observation of the moving L1 larvae
of lungworms (Angiostrongylus vasorum) collected
from the faeces of an infested dog after Baermann
sedimentation.
Video 4.2
Binocular lens observation of the moving adults of
lungworms (Angiostrongylus vasorum) collected from
the pulmonary circulatory system of an infested dog.
Females have a typical “barber’s pole” appearance.
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D.H.
Dog and wild canid
on
within 6 hours
-
of
L1
in
:
Larvae are
immediately
infective
Life cycle of Oslerus osleri and of Filaroides, embryonated eggs are laid in the pulmonary
Filaroides hirthi alveoli, where the adults are found.
F. hirthi and O. osleri have a characteristic direct monoxenous The L1 survive only briefly in the soil and are ingested
cycle, since the L1 larvae excreted in the faeces are directly by another definitive host. Once ingested, they cross the in-
infective. Infestation occurs through ingestion of these L1 lar- testinal wall, moult quickly into L2, L3 then L4 larvae in
vae, which cross the digestive wall, then migrate to the lungs. the mesenteric lymph nodes, before migrating through the
In Oslerus infestation, larval eggs are expelled from the lymphatic system towards the right heart, pulmonary arter-
definitive host in nasal discharge, saliva or faeces. These ies and arterioles. They enter the alveoli, where they devel-
eggs hatch immediately in the respiratory tract. In the case op into pre-adults then adults, which will either stay in the
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CONTENTS Respiratory and circulatory parasitoses 139
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Figure 1. Necroscopic sample: respiratory Figure 2. Microscopic coproscopy: Figure 3. Microscopic coproscopy:
tract of a dog infested by Oslerus osleri. Oslerus osleri L1 larva. Size 250–350 µm, Crenosoma vulpis L1 larva.
Numerous brownish nodules containing oesophagus is not visible, curved tail. Size 260–330 µm.
adult worms. Oesophagus is visible, tail is tapered.
D.
H.
ing
es
ts
I.H
.o
rP
.H
.
Eggs deposited
in alveolar ducts
and alveoli
s
2–
ek
5
we
we
6
ek
5–
s
Larva (L1)
Epidemiology
Aelurostrongylosis seems to be enzootic in populations of wild Troglostrongylus spp. in cat populations. However, one ep-
or stray cats, particularly in rural or forest areas. Cases are idemiological survey carried out on the island of Sardinia
sporadic in domestic cats and they are infested by chance con- (Italy) reported a T. brevior prevalence of 6.5 % in domestic
sumption of intermediate or paratenic hosts. There are two cats and catteries. Co-infestations by T. brevior and A. ab-
seasonal peaks, in spring and autumn, and these seem to be strusus have also been described in cats, suggesting that both
linked to the resurgence of intermediate hosts at these times. species may exist in sympatry.
Information on troglostrongylosis in domestic cats is
mainly based on case reports, so there are no reliable epi- Source of parasites
demiological data on the distribution and incidence of Wild or stray felids expelling larvae in their excrement.
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20 μm
100 μm
Figure 1. Different stages of Aelurostrongylus abstrusus collected after necroscopic examination and
lung digestion of an infested cat. (A) L1 larvae; (B) adult worms.
Clinical signs and lesions larvae (Fig. 3). Functional alveoli disappear from lysed ar-
Aelurostrongylosis eas and the arterial system is also lysed: endarteritis and
Clinical signs are affected by worm burden, health status, possible thrombosis can obliterate blood vessels.
age and the immune response of the infested animal. Indeed, The pathogenic effect of the parasites is linked to the
A. abstrusus causes a wide spectrum of clinical pictures, immuno-inflammatory response of the pulmonary paren-
ranging from asymptomatic, subclinical or mild disease up chyma and endarterium of the infested capillaries (tissue
to severe, potentially fatal pneumonia, although this is rare. infiltration by polynuclears, monocytes then fibro-con-
In the mild form of the disease, which is more common in junctive reaction) on one hand, and the formation of em-
adult cats and in cases of low worm burdens, the infesta- boli consisting of eggs and first stage larvae in pulmonary
tion may be self-limiting and respiratory signs gradually and capillaries, resulting in type III and IV hypersensitivities
spontaneously disappear within weeks. and thrombosis, on the other.
• Respiratory signs: aelurostrongylosis is characterised by
mild to intense chronic coughing, sneezing, wheezing, mu-
copurulent nasal discharge, dyspnoea, tachypnoea, tach-
ycardia, and open-mouthed abdominal breathing. Severe
respiratory signs and death are more common in young,
debilitated or immunosuppressed cats. Clinical cases may
be complicated by pyothorax and pneumothorax when
migrating larvae carry intestinal bacteria with them. Infes-
tation with A. abstrusus has been implicated in anesthet-
ic-associated deaths.
• General signs: development is chronic. Hyperthermia is in-
consistent and, when it does occur, it can be linked to sec-
ondary bacterial infections (such as pneumonia). General
signs, like lethargy, depression and weight loss may occur
and blood counts frequently indicate hypereosinophilia. Figure 2. Necroscopic sample: subpleural, greyish-white, coalesc-
Diarrhoea has also been reported in some cats. Develop- ing parasitic granulomatous nodules involving the parenchyma
of both lungs of a cat presenting respiratory failure due to severe
ment is slow and the animal usually recovers spontaneous- aelurostrongylosis.
ly after a few months; more rarely, its condition deterio-
rates, with cachexia and bacterial pneumonia.
• Lesions of aelurostrongylosis
The lungs are congested and the parenchyma is covered
in many small, greyish granulomatous nodules measuring
1–10 mm in diameter There are many of these nodules on
the surface of the pulmonary lobes and greyish and fibrous
plates may also appear on the lobes (Fig. 2).
The general appearance is similar to the lesions caused
by verminous pneumonia in small ruminants.
The nodules are granulomas centred on eggs and L1
larvae and, when cut, a fluid rich in parasitic elements may
200 μm
flow out. Adult worms are still very difficult to observe.
Histological lung sections show significant fibro-con- Figure 3. Section of a cat lung stained with haematoxylin and eosin.
junctive infiltration of the parenchyma cells, surrounding Alveolar lumina filled with several Aelurostrongylus abstrusus adults
and larvae. The surrounding parenchyma shows a mixed inflamma-
alveoli containing Aelurostrongylus eggs and first stage tory infiltrate.
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Diagnosis A B
Epidemiology
Respiratory strongylosis in cats are not easily interpreted in
current veterinary practice, because other overlapping con-
ditions should be considered in any differential diagnoses,
e.g., mycoses, viral and bacterial infections, nasopharynge-
al polyps, allergic bronchitis, foreign bodies and respiratory
neoplasms. C
Cats which go outside often and present suddenly with
a cough, dyspnoea, tachypnoea, weight loss and fatigabili-
ty may be clinically suspected. No sign is pathognomonic,
so epidemiological conditions will point to complementary
testing.
20 μm
Vets usually misdiagnose aelurostrongylosis and treat the
condition as an allergic respiratory disease or cat bronchial Figure 5. First stage larva of Troglostrongylus brevior. (A) View of
disease/asthma. As treatment is symptomatic, the infested the entire larva; (B) magnification of the anterior end of the larva,
showing a pointed extremity and a sub-terminal oral opening;
cat may show clinical improvement after administration of (C) magnification of the tail of the larva, showing a deep dorsal
corticosteroids and bronchodilators, so clinicians have no incisure and a shallower ventral one. Courtesy of Donato Traversa,
Angela Di Cesare and Emanuele Brianti.
reason to suspect that they have made a misdiagnosis.
Medical imaging
Radiography does not allow a definitive diagnosis, but con-
firms the pulmonary disorder: pulmonary densification,
nodular images (fibrous tissue), and dilation of the pulmo-
nary arteries, and the images can also indicate tumours,
pneumonia, etc.
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Parasitological examination
The technique of choice is microscopic coproscopy and the A differential diagnosis must be made from other larvae
identification of L1 larvae (Figs. 5 and 6). Aelurostrongylus which can be found in the faeces: L1 of Crenosoma vulpis
is fairly prolific, so the sensitivity of coproscopy is good, al- (rarer), L3 of Ollulanus tricuspis (rarer and L3 present in
though it can be useful to carry out several tests (3 at 48 hour vomit), hookworm larvae which may be present in samples
intervals). that have been allowed to incubate, and larvae from free
The Baermann migration method is the gold standard to nematodes if the faeces are not collected fresh and have sat in
diagnose cat aelurostrongylosis with a sensitivity of ≈90 %, the soil, even for a few hours.
although it requires 24–36 hours before larvae can be found,
and specific skill in detecting L1.
Diameter 15 µm 18–19 µm
Anterior extremity Rounded with terminal oral opening Pointed anterior extremity
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Paragonimoses
General comments
Paragonimoses are found in many mammals, particularly
carnivores and humans, and are caused by the presence and
development of Troglotrematidae trematodes of the genus
100 μm
Paragonimus in the pulmonary parenchyma. The diseases
are characterised by afebrile respiratory signs linked to par- Figure 1. Adult Paragonimus kellicotti, red carmine staining. Trema-
asitic pneumonia: dyspnoea, breathlessness, and coughing, tode approximately 10 mm long, with a fleshy body with a flattened
side and domed side, making it looks like a fresh coffee grain.
but the parasites may be carried by many healthy animals.
There are more than 50 species in the genus Paragonimus,
but many species are not officially fully recognised as such. Biology
Three species are important in domestic carnivores and hu- Trematodes of the genus Paragonimus have a trixenous life
mans: P. kellicotti (Fig. 1), found in North America and Cen- cycle. The adults live in intrapulmonary cysts in the respirato-
tral Asia; P. westermani, found in Asia; and P. africanus in ry tract, bronchi and pulmonary bronchioles in the definitive
tropical Africa. host and are usually found in pairs in these cysts. The adults
No autochthonous case has been described in Europe, but release eggs into the lungs, where they are coughed up the
imported cases are possible as a result of animal movements. pharynx and swallowed, then expelled either in expectora-
A case of sudden death in an autochthonous dog was de- tion or with the faeces.
scribed in Israel in 1997, suggesting that the parasite exists in If the eggs fall into an aquatic environment (fresh water),
this region of the Mediterranean area. they mature in 2–3 weeks and hatch into miracidia. This sur-
The main species affected are wild carnivores, which vives very briefly and must actively penetrate a freshwater
are likely to consume second intermediate hosts (crayfish amphibious gastropod, the first intermediate host (Pomati-
and fresh water crabs) and otters, racoons, foxes, mink, opsis, Melania, Ampullaria and many other genera).
black-footed ferrets, wild cats, dogs and domestic cats. The miracidia develop into sporocysts, rediae and then
into cercariae, which are formed in 75 to 100 days, before
Morphology being released.
Paragonimus, or lung flukes, are trematodes with two dis- Swimming cercariae will actively infest the second in-
tinct suckers. The genital pore is situated behind the ventral termediate hosts: fresh water crustaceans, especially crabs
sucker, which is located nearby, and the two testicles are pos- (Eriocher spp., Patomon spp., Sesarma spp., Pseudotelphus
terior and situated next to each other. spp., etc.) and crayfishes (Astacus spp., Cambarus spp., etc.).
The adults are fleshy parasites measuring approximately Cercariae develop into encysted metacercariae in these hosts.
10–15 by 5–7 by 5 mm. The definitive hosts are infested by ingesting freshwater
Each egg contains a miracidium larva and is ovoid, crustaceans. Immature adults (also called adolescariae) are
capped, brownish-orange, and measures approximately released in the stomach where they cross the digestive mucosa
90 × 60 µm. and migrate directly, for approximately 14 days, to the peri-
toneal cavity via the diaphragm, then to the pulmonary pa-
renchyma where they encyst, usually in pairs. Some parasites
may occasionally migrate to, and encyst in, erratic locations:
hepatic parenchyma, kidneys, myocardium, diaphragm.
The prepatent period is around 1 month (30–36 days).
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10 μm
Figure 1. Capillaria aerophila egg. Coproscopy (×40): the egg is barrel-shaped, and presents
asymmetry of bipolar plugs, no ring thickening, and a net-like outer shell with depressions and
irregular anastomosing ridges and bridges. The long and short axes of these eggs are 65 × 30–40 μm,
respectively.
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Linguatulosis
Morphology
General comments Adult pentastoma are whitish crustaceans with elongated,
Linguatulosis is a parasitic rhinosinusitis caused by the pres- worm-shaped bodies which are sometimes striated (pseu-
ence and development of a crustacean parasite, Linguatula do-segmentation) and more or less flat. Females are generally
serrata (syn. Linguatula rhinaria) in the nasal cavity and si- larger than males. They have a complete digestive tract.
nuses of carnivores. At the anterior end, the mouth is surrounded by two pairs
Linguatula organisms belong to a homogenous group of of small rudimentary legs, with articulated hooks (made up
parasites previously known as pararthropods, in the class of two segments) and localised to the fossa. The name pen-
Pentastomida (Heymons, 1926). Some recent molecular tastoma comes from these four appendices, plus the mouth.
studies have compared them to parasitic crustaceans, the Adult male L. serrata measure 18–20 × 3–4 mm and
Copepod subclass in particular so Pentastomida is now an females, 18–130 × 8–10 mm. They are elongated, flat and
order of this subclass. tongue-shaped, with a tapered posterior end (Figs. 1 and 2).
In their adult state, many species are parasites of reptiles The brownish eggs measure 90 × 70 µm and they have a
(Porocephalidae family Heymans, 1922). L. serrata (Fröh- thick, smooth shell and contain an embryo with two pairs
lich, 1978) is the only representative of the Linguatulidae of hooks.
(Shipley, 1898). The first egg-derived larval stage measures 500 µm. This
This parasite is distributed worldwide but it seems to be stage is not striated and has no buccal orifice, and it devel-
more common in tropical countries (North Africa, Central ops in nine successive moults to the nymph stage, which is
Asia, and the Middle East). It has only been reported sporad- 4–6 mm long. The nymph is morphologically similar to the
ically in Europe. adult and is only differentiated by its small size and absence
As the life cycle requires ingestion of the raw viscera of of reproductive organs.
mammalian intermediate hosts (ruminants, rabbits or ro-
dents), it mainly involves wild carnivores, particularly can- Biology
ids: foxes, wolves, although dogs and, occasionally, cats may The parasitic cycle is a dixenous cycle. The adult Linguatu-
also ingest the parasitised viscera and become infested. la live in the nasal cavities or, more rarely, in the sinuses or
Rare human cases have also been described. pharynx of the definitive hosts, which are carnivores, held
there by their hooks.
Figure 1. Macroscopic view of an adult Linguatula serrata Figure 2. Adult Linguatula serrata (approximately 7 cm long)
(approximately 7 cm long) extracted with tweezers from a nasal extracted with tweezers from a nasal cavity. Observation after
cavity. Courtesy of Parasitology Unit, Alfort Veterinary School. lactophenol clarification. The striated appearance of the whole body
and presence of four hooks at the anterior extremity can be seen.
Courtesy of Parasitology Unit, Alfort Veterinary School.
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Figure 3. Histological section of the rumen mucosa of a cow, Figure 4. Linguatula sp. egg, excreted with nasal mucus.
showing a larva of a Linguatula sp. curved around itself. Obj. ×10. Microscopic examination.
Courtesy of Parasitology Unit, Alfort Veterinary School.
The males die quickly after fertilisation (4 months after were infested and carrying 1–29 Linguatula. Dogs over
infestation), whereas the female lifespan is approximately 15 5 years old were significantly more infested than dogs up
months. The females lay eggs which are either expectorated to 4 years old.
with nasal discharge or, more rarely, expelled with the faeces.
Eggs are directly infective and can survive for a few days Clinical signs and diagnosis
in the soil. If they are ingested by herbivores (ruminants, Linguatula’s size and mechanism of fixation are responsible
horses, rabbits, rodents), they release stage 1 larvae (L1) for sinus and nasal inflammation which causes clinical signs.
which resemble small mites. The larvae encyst in the intes- Infestation may be asymptomatic or manifests itself
tinal mucosa or migrate in the lymphatic vessels towards the through only mild clinical signs: animals sniff and sneeze,
mesenteric lymph nodes, liver or other organs. They may and epistaxis is common. Dogs present with abundant nasal
spread through the whole organism. After developing for discharge, serous where there areno complications, but often
several months (going through successive moults), the nymph haemorrhagic. Expulsion of parasites during sneezing attacks
which resembles an adult is formed. It resembles an adult, is possible.
and is usually localised within a small cystic gall bladder. Af- Differential diagnosis must be made between all causes
ter developing for 7 months, the nymph comes out of its cyst of rhinitis in dogs and cats: the clinical signs of linguatulosis
and enters the thoracic or abdominal cavity. are resistant to antibiotic treatment, but may improve with
If a carnivore consumes raw viscera from an infested her- anti-inflammatory treatment.
bivore, the cycle continues and the nymph travels up from the Definitive diagnosis depends on visualisation of adult
stomach towards the buccal cavity, then enters the pharynx Linguatula (by rhinoscopy) or eggs in discharge or faeces
and nasal cavity, where it remains and becomes an adult. The (Figs. 3 and 4).
period of development is approximately 6 months in dogs.
Control measures
Epidemiology It is sometimes possible to remove Linguatula from a tran-
Linguatulosis is sporadic in domestic carnivores, particularly quilised dog with forceps.
dogs, in Western Europe. The natural cycle takes place in the Active antiparasitic drugs are effective against haemato-
wild, and involves carnivores, herbivores, lagomorphs and phagous parasites, notably nitroxinil, administered subcu-
rodents. taneously at a dose of 10 mg/kg. Closantel could be tested.
Linguatulosis can be enzootic in other areas, such as Cen- Avermectins/milbemycins can be used at an insecticidal/
tral Asia and Africa. acaridicidal dose.
Prevalence may be particularly high in stray dogs and Prophylaxis relies on preventing carnivores from access-
a survey in Iran in 2003 reported that 62.2 % of dogs ing ruminant or lagomorph offal.
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Figure 1. Adults Pneumonyssoides caninum observed between Figure 2. Adults Pneumonyssoides caninum observed fresh under
slide and coverslip in Amann’s lactophenol. Size approximately a binocular magnifier. Size approximately 700 µm. Courtesy of
700 µm. Courtesy of Parasitology Unit, Oniris. Patrick Bourdeau, Parasitology Unit, Oniris.
TABLE OF
CONTENTS Respiratory and circulatory parasitoses 155
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A B
Figure 3. Pneumonyssoides caninum in situ by (A) intra-nasal endoscopy and Figure 4. Presence of adults
(B) necroscopy. Courtesy of Patrick Bourdeau, Parasitology Unit, Oniris. Pneumonyssoides on the nose of a dog.
From the thesis of Lotta Gunarsson. Courtesy of Patrick Bourdeau, Parasitology
Unit, Oniris. From the thesis of Lotta
Gunarsson.
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Urinary parasitoses
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20 μm
20 μm
D.H.
Dog, cat and fox
Ing
es
tP
.H Eggs and
.
larvae
Small
intestine
s
ts egg 5–
inges be 7 w
P.H. co ee
m ks
e i to
nf
ec
tiv
e
Urine
10 μm 5 μm
10 μm
Dioctophymosis
General comments
Dioctophymosis is a helminthosis of the kidney caused by
parasitism by Dioctophyme renale (or Dioctophyma renale).
This parasite is a nematode belonging to the Dioctophy- Figure 1. Adult Dioctophyme renale,
matoidea order, which does not contain any other nematode isolated after extraction.
Morphology
D. renale is large roundworm, 20–80 cm long (Fig. 1). Both
sexes are bright red in colour and taper at both the anteri-
or and posterior ends. The posterior end is bell-shaped. Figure 2. Observation of a male’s bell-shaped caudal bursa.
Male D. renale worms have a bursa, which is used for at-
tachment during mating, but it is not supported by chitinous
ribs as are the copulatory bursa of Strongylida males (Fig. 2). Epidemiology
D. renale is found in all cold temperate regions of the North-
Biology ern hemisphere where freshwater is available, as its cycle re-
The adults are localised to the renal pelvis, mostly in the right quires an aquatic environment.
kidney, and sometimes even in the ureters, and they cause The adults, measuring 20–80 cm in length, mainly para-
atrophy of the renal parenchyma and an associated reduc- sitise piscivorous mammals, in particular mustelids (otters,
tion in renal filtration, with the onset of lower back pain and minks) and sometimes canids, or humans. Dioctophymosis
haematuria. is principally a parasitosis of wild fauna and is found sporad-
The life cycle is aquatic and dixenous. The females lay eggs ically in domestic carnivores.
which are expelled in the urine, and develop in an aquatic The consumption of contaminated fish, which act as pa-
environment into embryonated eggs containing L1 larvae in ratenic hosts, is the main source of infestation in mammals.
1–3 months. If these eggs are ingested by the intermediate
host, an oligochaete annelid (such as Lumbriculus sp., Cam- Clinical signs and lesions
barincola sp.), they develop into L3 larvae (after 100 days) Clinical signs
but may re-encyst in numerous paratenic hosts: batrachian Dioctophymosis is characterised by slow development of re-
or freshwater fishes, including catfish (Ichtalurus melas). nal insufficiency and the animal presents with acute lower
The intermediate host or paratenic host is then eaten by a back pain on palpation of the kidneys (particularly the right
definitive host, where the L3 larvae penetrate the intestinal lin- kidney, which is infested in more than 90 % of cases).
ing and migrate to the liver. After maturing for approximately A change in general condition is also seen. Nervous signs
50 days, they migrate to the kidneys and moult into adults. The are possible: paresis, paraplegia, and rabies-like clinical signs.
prepatent period is of 4–5 months. Upon maturation, D. re- Blood count shows high levels of urea and creatinine and
nale can survive for approximately 5 years in its host. constant or intermittent haematuria may be seen.
TABLE OF
CONTENTS Urinary parasitoses 163
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Figure 5. Extraction of an
adult Dioctophyme renale after
nephrectomy (right kidney).
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Disseminated
parasitoses
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Leishmaniosis Importance
Veterinary importance for the dog is linked to the severity
of the disease. It usually advances gradually until the animal
General comments dies and treatment provides only temporary clinical recovery.
General canine leishmaniosis is an infectious protozoan It does not eliminate the parasites and relapse is common.
disease, transmitted by phlebotomine sandfly bites (Fig. 1). There is a threat to public health because dogs act as a para-
It is caused by the presence and multiplication of flagellate site reservoir for humans but it is very rarely contagious from
protozoa belonging to the Leishmania (donovani) infantum dogs to humans.
species in cells from the mononuclear phagocyte line. It is
characterised by visceral and mucocutaneous damage, hence Geographical distribution
the name “general leishmaniosis”, and by damage to all or- The distribution of Leishmania reflects that of its vectors.
gans and tissues containing macrophage cells. L. infantum is found in the Mediterranean Basin, the Near
Leishmania infantum is a zoonotic parasite, the agent for and Middle East, Central Asia and China, as well as Sub-Sa-
human visceral leishmaniosis, otherwise known as Mediter- haran West Africa. It was imported to South and Central
ranean kala-azar (as opposed to Indian kala-azar, which is America by European colonists and there, the parasite is
caused by L. donovani donovani). known as L. chagasi, but it is the same as L. infantum.
Leishmania infantum was previously called L. canis as it In Europe, leishmaniosis is enzootic in Italy (except in
infects domestic and wild canids (foxes in France), but lago- alpine areas), Sardinia, Sicily, Spain, Portugal, the southern
morphs and rodents, including black rats, mice and hamsters, third of France, Corsica and Greece.
can also be infected with some strains.
Some cases of leishmaniosis have been reported in cats
and horses but they are still rare. Figure 2. Distribution of canine leishmaniosis due to
In humans, this infection has historically affected mainly Phlebotomus spp. in Europe.
children, hence the name infantum. Currently, the most cases
are seen in immunosuppressed individuals, especially those
infected by HIV.
I.H.
Dog, sometimes cats
Sa
nd
fly
bit
e in
fec
ts h
~1 week
ost
Promastigote
Amastigote Promastigote
2–3 days
~ 7 days
The macrophages
phagocytose the
promastigotes
g
D.H. din
Sandfly e fee Promastigotes become
hil amastigotes, and
tedw Weeks to months
ec multiply in macrophages
inf
dfly
n
Sa
10 μm
10 μm
Figure 3. Leishmania infantum amastigotes inside macrophages. MGG-stained lymph node puncture.
(A) Courtesy of the Parasitology Unit, Alfort Veterinary School.
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CONTENTS Disseminated parasitoses 169
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Clinical signs
These appear after a very variable incubation period, how-
ever this is usually between 3 months and a year after in-
Figure 4. Dog with leishmani- Figure 5. Amyotrophy in a fection, so Leishmania can be seen in dogs which returned
osis: view of the head. Wasting dog with leishmaniosis (right). from enzootic areas several months, and sometimes several
of the masseter and frontal Courtesy of Blaise Hubert.
muscles, making the dog look years, earlier. As the incubation period is long, serology is
old. Diffuse alopecia, significant often already positive when signs start to appear.
squamosis. Courtesy of Blaise
Leishmaniosis is clinically very polymorphic, causing a
Hubert.
variety of clinical signs, both general and cutaneous. The
presence of a single sign must arouse suspicion of the disease,
Leishmania survive inside macrophages by inhibiting their especially in enzootic areas.
activity and adjusting the host’s immune response so that the Clinical signs may be more or less pronounced and vary in
macrophage phagocyte system is not activated: stimulation the length of time they take to develop.
of a type Th2 (humoral) response to the detriment of a type
Th1 (cellular) response. General clinical signs
L. infantum is dermotropic and viscerotropic in the dog. • Character change: a relatively consistent sign and one of-
Pathogenicity is linked to the infection of cells which are ten reported by owners. The dog becomes apathetic, less
part of the immune system, causing an immunopathological playful, depressed. This state can progress as far as torpor.
disorder. Appetite is also reduced.
Leishmania, like all parasites, have a complex antigenic • Amyotrophy: dogs show signs of muscle wasting, which
structure, including surface antigens (lipophosphoglycan, affects the head first, especially the temporal and jaw mus-
surface glycoprotein and somatic antigens). The antigenic cles. The temporal fossae deepen, giving the animal a rath-
coating differs between infective promastigotes and amastig- er typical “old dog’s head” (Fig. 4). Later, even the limbs
otes, which is a mechanism for escaping immune recognition. get thinner, as well as the hips, which become prominent
An immune response follows infection of the dog and it is (Fig. 5).
cellular and humoral. The non-protective humoral response is • Weight loss: this accompanies the muscle wasting. The dog
early and intense and manifests itself by the appearance of an- starts to look like a sad, old dog.
tibodies, mainly of the IgG type. These can facilitate phagocy- • Inconstant hyperthermia: this is particularly seen in young
tosis by macrophages, so they seem not to play any protective dogs, less than 2 years old.
role; quite the opposite. Their abundance and the formation of • Blood and biochemical changes: anaemia, leukopaenia
complexes with antigens are responsible for immunopatholog- and thrombocytopaenia are usually noted. Leukopaenia
ical signs: glomerulonephritis, arthritis. Specific serum IgGs is accompanied by monocytosis and hyperproteinaemia is
are found by various techniques: ELISA, agglutination or indi- soon seen. Globulins increase, resulting in a reversal of the
rect immunofluorescence, which is still the reference. albumin/globulin ratio from 1 to 0.3–0.1.
TABLE OF
CONTENTS Disseminated parasitoses 171
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General comments
Toxoplasmosis is an infectious disease caused by the mul-
tiplication and pathogenic activity of the protozoan species
Toxoplasma gondii, which infects cells in the mononuclear
phagocyte system (MPS). However, the parasite’s location
and the pathogenic stage lead to the definition of two differ-
ent entities, according to clinical and epidemiological criteria
10 μm
and public health criteria:
• Toxoplasmic coccidiosis, only affecting cats and other Figure 1. Toxoplasma gondii tachyzoites. MGG staining. Sporozoites
felids, which are the parasite’s definitive hosts. Similar to collected in ascites of an infected mouse.
50 μm 20 μm
Figure 2. Cyst with bradyzoites. H&E staining. Brain histology. Figure 3. Toxoplasma gondii pseudocysts. Intense tissular multipli-
cation. Acute toxoplasmosis in a kangaroo imported into the Forest
Park in Noumea, New Caledonia. Tissue smear. MGG staining.
ENTERIC-EPITHELIAL CYCLE
in definitive host (cat only)
Unsporulated oocyst
(non-infective form)
Microgamete
1–5 days
Zygote Non-infective
Merozoites
oocysts are
excreted in
Macrogamete
faeces
Gamonts Small intestine cells
Cat ingests tissue cysts with bradyzoites - new oocysts in 3–10 days
Cat ingests oocysts - oocysts in 19–48 days
D.H.
Cat
Unsporulated
oocysts in faeces
I.H.
All warm-blooded
animals susceptible Sporozoites
Sporulated oocyst
(infective form)
Faeces
~ 3 weeks
Neosporosis
~ 5 days
Non-sporulated
oocyst
Oocysts shed
D.H. for 5–17 days
Dog and coyote
Faeces
tissue
t infected
Inges ~3 days in faeces
for oocyst to become
infective
Sporulated oocyst
Months (infective form)
to years
Inge
I.H.
Tachyzoites
st oo
and bradyzoites
cyst
20 μm
Figure 1. Neospora cyst containing bradyzoites in the brain tissue of a puppy with clinical
signs of neosporosis. Courtesy of Laboratoire Territorial de Diagnostic Vétérinaire de
Nouvelle-Calédonie.
The role of dogs as definitive hosts has been demonstrated Mechanisms of infection
experimentally by examining the faecal excretion of oocysts Neosporosis is transmitted horizontally, by ingestion of
after ingestion of tissue from infected mice. sporulated oocysts, and vertically, from the mother to the foe-
tus, in the majority of species, especially cattle. This congeni-
Epidemiology tal transmission can occur during any gestation and not only
Source of parasites at primary infection, as occurs in toxoplasmosis. This mode
• The definitive host contaminating the environment of of transmission seems to be the main explanation for the sur-
the intermediate hosts (cattle or other mammals), nota- vival of Neospora in cattle herds for several generations.
bly grasslands, with infective oocysts. Dogs are definitive
hosts, but shed few oocysts expelled in the experimental Predisposing factors
infections carried out. Other carnivores are certainly in- Many animals are healthy carriers, as with Toxoplasma, as
volved: foxes (and perhaps mustelids). Neospora can be transmitted without causing neosporosis.
Epidemiological surveys do not always confirm the dog as It seems that the immune status of the host plays an impor-
having a major role in cases of neosporosis in cattle. Some tant role in explaining the presence or absence of 1) verti-
authors consider that they do not have a greater presence in cal transmission, 2) abortion, and 3) post-natal congenital
cases where seroprevalence and abortions due to Neospora neosporosis.
are frequent or pose problems.
• Intermediate hosts, which are consumed by carnivores, Geographical distribution and prevalence
therefore continuing the dixenous cycle. Distribution is thought to be worldwide. The serological
• Pregnant females, whose bradyzoite cysts are likely to be and/or parasitological prevalence in cattle is significant in the
activated during gestation, releasing tachyzoites, which USA, Canada, New Zealand, and Australia, but also in Eu-
can vertically infect the foetus. rope (France, Germany, UK), where this parasite is respon-
sible for up to 20 % of abortions (the second most common
cause of abortion in cattle).
TABLE OF
CONTENTS Disseminated parasitoses 185
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Encephalitozoonosis
Control measures
There is no specific treatment. Trials using fenbendazole have
produced very good results in rabbits, with a daily adminis-
tration of 20 mg/kg for 21 days. Albendazole is used with
good result in humans, although it is relatively toxic for dogs,
for whom fenbendazole is preferred.
For ocular disorders, the antibiotic fumagillin has been
10 μm
applied topically each day until keratitis regressed.
Figure 1. Section of liver from a patient with AIDS and infected There are no particular preventative measures, since
by Encephalitozoon hellem. Encephalitozoon spores stained by
spores are resistant in the external environment. Rabbits and
immunofluorescence. Anti-E. cuniculi polyclonal antibody serum.
Fixed by conjugated FITC goat anti-rabbit IgG (Antonella Tosoni et rabbit farming are factors contributing to the presence and
al. 2002. Modern Pathology. 15(5): 577–583). concentration of spores.
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Miscellaneous
parasitoses
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20 μm
Figure 1. Parasitic peritonitis due to Taenia crassiceps in an Figure 2. Cysticercus presenting the characteristic budding process
experimental mouse model showing invasion of the peritoneal cavity of Taenia crassiceps. Courtesy of Parasitology Unit, Alfort Veterinary
by thousands of cysticerci (semolina-like appearance). Courtesy of School.
Parasitology Unit, Alfort Veterinary School.
TABLE OF
CONTENTS Miscellaneous parasitoses 193
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20 μm 50 μm
Figure 3. Cysticercus presenting the characteristic budding process Figure 4. Numerous cysticerci obtained by puncturing the
of Taenia crassiceps. The start of invagination and strobila formation deformed subcutaneous mass in the dog in Figure 5. Courtesy of
can also be seen. Courtesy of Parasitology Unit, Alfort Veterinary Parasitology Unit, Alfort Veterinary School.
School.
A B
Figure 1. Ascitic fluid caused by parasites and Mesocestoides larvae in the abdomen of a dog.
Courtesty of Jean-Paul Lemonnier.
TABLE OF
CONTENTS Miscellaneous parasitoses 195
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*
Peritoneal and
subcutaneous filarioses
General comments
Dogs and cats may be infested by filarial species other than
Dirofilaria immitis. These are less pathogenic but must be
included in any differential diagnosis when blood microfilar-
iae are observed.
• Dirofilaria immitis.
• Dirofilaria repens, located in subcutaneous tissue and
muscle fasciae (Figs. 1–3).
• Cercopithifilaria (formerly Dipetalonema) grassii, locat-
ed in perirenal, peritoneal and subcutaneous tissues.
• Acanthocheilonema (formerly Dipetalonema) dracuncu-
loides, located in the peritoneal cavity.
• Acanthocheilonema (formerly Dipetalonema) reconditum,
located in the peritoneal cavity and subcutaneous tissue.
Geographical distribution
The subcutaneous filarial species D. repens is found world-
wide, but seems to be absent from North America. The en-
zootic areas of D. repens and D. immitis overlap in many
regions of Europe. Transmission frequency and the spread
of D. repens depend on environmental factors, such as tem-
perature, the density of vector populations and the presence
of microfilaraemic dogs and wild canids, which are the main 15 μm
reservoirs of infestation.
Figure 3. Dirofilaria repens microfilaria stained with acid
phosphatase. There is only one red spot (2 spots for
Dirofilaria immitis).
*Dirofilaria repens
TABLE OF
CONTENTS Miscellaneous parasitoses 197
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D.H.
Dog, cat and human
The mosquito bites the D.H. and the
L3 larva penetrates the wound and
reaches the subcutaneous tissue
Microfilariae
develop into L1
larvae, moult into
L2s, then moult
again into infective
L3 larvae
days
The L3 larvae
10–16
ts
es ae
d ing filari
n ro
s a ic
bite g m L4 and L5 larvae
ito ini n
qu ta
m os con
e od
Th blo
th e The adults form nodules
which can be located in
Microfilaria (L1) subcutaneous tissue, among
the tendons of the limbs and
Adults produce microfilariae (L1) in the lymph nodes
that remain in the blood and lymph
spaces in the skin. Similar in size Adults in subcutaneous tissue
and appearance to D. immitis D.H. = definitive host
microfilariae I.H. = intermediate host
TABLE OF
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D.H.
Dog
I.H fect
. b ive
in
ite L3
L2 and L3 larvae
ul
at
es
days
7–14
m
loo
Adult
3
iae b
2–
lar the
ofi ts
icr es
m ing
Adults produce
I.H. (haematophagous
ng d
ini an
microfilariae which
arthropods)
nta tes
circulate in blood
co . bi
I.H
Control measures
Moxidectin is labelled for the prevention of D. repens infes-
tation in dogs, and the treatment of circulating microfilariae.
A microfilaricidal treatment based on ivermectin (50 µg/kg)
can be administered when clinical signs suggest microfilariae
(off-label use).
There is no known effective adulticide for D. repens and
30 μm
there are no prophylactic measures other than vector control.
Figure 4. Microfilaria of Achantocheilonema reconditum detected
by Knott technique.
Table 1. Morphological features of filarial species in dogs and cats (adapted from ESCCAP Guideline 5).
Thelaziosis
Figure 1. Adult Thelazia callipaeda. Direct examination after Figure 2. Phortica variegata. Courtesy of Domenico Otranto.
extraction.
TABLE OF
CONTENTS Miscellaneous parasitoses 201
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A B
Figure 3. Clinical infestation with Thelazia callipaeda in a cat (A) and a dog (B). Courtesy of Domenico Otranto.
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D.H.
Dog and cat, sometimes humans
th
on
Infective L3 larva 15
–3 1
m
0d
ay
s
infective L3 larvae
Control measures
Treatment is based on the direct removal of nematodes the
eyes of affected animals (after local or general anaesthesia)
and the use of an antiparasitic drug. Moxidectin applied in a
spot-on, oral milbemycin oxime and subcutaneous ivermec-
tin have all proven to be effective treatments for thelaziosis in
dogs. Antibiotic ointments or ocular drops s are recommend-
Video 6
ed in cases of bacterial infection.
Adult Thelazia callipaeda on the surface
Prophylactic measures include the use of macrocyclic
of the nictitating membrane of a dog.
lactones in a spot-on form administered monthly or in a
Courtesy of Olivier Pennant.
slow-release form during the vector’s active period.
TABLE OF
CONTENTS Miscellaneous parasitoses 203
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Control measures
Treatment
There is no treatment for livestock but high doses of benzim-
idazoles could be considered for use in domestic carnivores
and humans.
Anthelmintic treatment is more effective when adminis-
tered early, killing the intestinal females and larvae which
have not yet encysted. No treatment is active after larvae have
encysted. Corticotherapy limits allergic reactions in humans.
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EXTERNAL
PARASITOSES
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Entomoses
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Flea infestation C. felis felis is not host-specific and can take its blood meal
from various mammals (domestic and wild carnivores, opos-
sums, rodents, rabbits, ruminants, humans, etc.) (Fig. 3).
Introduction More than 50 hosts have been identified, even though this
The cat flea, Ctenocephalides felis, is the predominant flea sub-species is called the cat flea. The owners of flea-infested
species found on cats and dogs, with a prevalence of over cats and dogs are often bitten and frequently develop pruritic
90 % cited in almost all publications (Fig. 1). However, other papules on their legs and ankles.
flea species can occasionally be seen on carnivores: Cteno-
cephalides canis (dog flea) (Fig. 2), Spilopsyllus cuniculi (rab-
bit flea), Ceratophyllus spp. (bird fleas), Xenopsylla cheopis
(rat flea), Archeopsylla erinacei (hedgehog flea), Leptopsylla
segnis (rodent flea) and Pulex irritans (human or fox flea).
These fleas represent less than 1 % of the fleas found on cats,
and are usually found on outdoor cats which hunt.
C. canis is the predominant flea species found on dogs in
some parts of the world, such as Central Europe. P. irritans,
the fox and human flea, is also common on dogs in some areas.
C. felis can be divided into four sub-species, three of which
infest felids. C. felis felis (Bouché, 1935) is the predominant
sub-species in Europe and North America, whereas C. felis
strongylus is more common in Africa and the Middle East.
C. felis orientis (Jordan, 1925) is found in Asia. These last
two sub-species are morphologically very similar to C. can-
is (Curtis, 1826). C. felis damarensis (Jordan, 1936) infests
small carnivores and is found in North America. Figure 2. Adult Ctenocephalides canis.
Figure 1. Adults Ctenocephalides felis. Figure 3. Sheep heavily infested by Ctenocephalides felis.
TABLE OF
CONTENTS Entomoses 211
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Fleas are the most common ectoparasites infesting pets in The third pair of legs is bigger than the others, and adapt-
both rural and urban habitats. Cat fleas are adapted to their ed to jumping to facilitate infestation of the host. The average
environment (outdoor and indoor) and persist throughout jumping distance of C. felis felis is 20 cm (2–48 cm), and of
the seasons, even surviving through the winter in temperate C. canis is 30 cm (3–50 cm). Jump height is about 15 cm,
countries. Nevertheless, infestation and clinical manifesta- with a maximum height of 25 cm attained by C. felis.
tion usually peaks between spring and autumn. Flea eggs are small (0.2–0.5 mm), ovoid and white to
Cats usually tolerate fleas quite well but flea infestation yellow-white.
can sometimes provoke intense pruritus and some animals
will develop flea allergy dermatitis (FAD) with more pro-
nounced skin lesions.
C. felis is usually recovered from 5 % to over 50 % of the
cats studied in epidemiological surveys, and the variation is
linked to methodology, country, season, treatment history,
etc. C. felis probably originated in Africa and is better adapt-
ed to warm climates than cold. It is found in both rural and
urban areas and on pets living indoors or outdoors.
Morphology
Fleas are wingless insects, 2–4 mm long and a yellow-
EXTERNAL PARASITOSES
ish-brown colour, belonging to the order Siphonaptera.
There are approximately 2,500 flea species, divided into
15 families and 200 genera. Most fleas of medical and veter-
inary importance belong to the family Pulicidae.
Many species bear one or more “combs” or ctenidia,
which are groups of sclerotinised spines. Flea classification
is mainly based on the morphology of the head and the adult
genitalia, and the number of ctenidia and their positions.
Ctenocephalides fleas have two pronounced ctenidia: the ge-
nal ctenidia on the ventral margin of the head, and the pro-
notal ctenidia on the posterior margin of the head (Fig. 4).
Fleas usually have well-developed eyes, and antennae
which are composed of three segments and located in an-
tennal fossae on each side of the head. The mouthparts are
well adapted to blood sucking: the two labial palps locate
the feeding site, then the other mouthparts (the “stylets”) are
used to pierce the skin through to a capillary. They then form
a feeding canal and a salivary canal.
C. felis felis belongs to the family Pulicidae. It is 2–4 mm
long and orange to dark brown in colour. The front of its
head is rounded and has two perpendicular combs lined with
dark brown teeth. The body is laterally compressed to facili-
tate movement between hairs and the third pair of legs is very
well developed and adapted to jumping. C. canis is smaller
than C. felis, the head is shorter and the first spine of the
genal ctenidia measures half of the second in C. canis and
almost the same length in C. felis. Figure 4. Head of Ctenocephalides felis showing the two ctenidiae.
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Figure 7. Female flea laying an egg on its host. Figure 8. Flea eggs on the ground.
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A B
200 μm 200 μm
EXTERNAL PARASITOSES
Figure 9. Electronic
microscopy showing a flea
egg (A and B) and a recently
hatched stage 1 larva of 100 μm
C. felis.
1 mm
Figure 10. Stage 3 Ctenocephalides felis larva. Figure 11. Flea cocoons and stage 3 larvae on a sofa.
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Biology of Ctenocephalides fleas animals. However, the epidemiological role of these few ma-
Over the last 20 years, studies on the biology of fleas on ture fleas which transfer from one host to another can be
pets have improved our understanding of the flea life cycle, significant due to the prolificacy of each female.
providing us with essential information to construct an ef- Adult fleas take their first blood meal 30 minutes to
fective flea control programme. Some ideas about cat fleas 1 hour after arrival on the animal and then breed within the
have been found to be wrong, for example, the adult flea is following 48 hours (Figs. 5 and 6). Each female can lay up
no longer considered a transitory parasite, found on the cat to 50 eggs per day at her peak, starting to lay a few eggs
or dog only when feeding, but a permanent parasite which 36 hours after infesting the host and averaging 20–30 eggs
tends to stay on the same animal. It only survives for 3 to per day (Fig. 7). Females lay eggs throughout their whole life,
5 days in the external environment if it falls off. Adult fleas which is usually short (15 to 30 days). They probably take
on pet animals exceptionally change host and infest other 4 to 10 blood meals per day, each lasting several minutes.
D.H.
Adult fleas typically stay Dog and cat
on the host until they die,
Each female flea can lay an average
rarely moving from animal to
of 25 eggs per day (up to 2,000 in a
animal
reproductive lifetime). Eggs drop off
the animal to infest the environment
(bedding, home, garden)
s
Adult ce
d fae
n
s a st
egg ho
a om
Fle p fr
dro Flea faeces
and eggs
vibration or
movement,
Stimulated by y emerges
g adult rapidl
CO2, the youn Stage 1
s the host
and acquire Entire life cycle: 14 to 325 days larvae hatch
(depending on conditions)
8–
32
ys
5
da
da
Stage 1 larva
11
ys
5–
The eggs are not fixed to the host and fall to the ground When humidity is favourable, the life cycle of C. felis
as the animal moves around (Figs. 8 and 9). It has been esti- takes 14 days at 29 oC. On average, a complete life cycle can
mated that the eggs remain on the animal’s skin for around be considered to take 3 to 4 weeks.
2 hours before falling off. This enables contact with any The emergence of fleas from their cocoons is influenced by
insecticides or insect growth regulators (IGRs) that may be various factors: shadows, footsteps, vibrations (for example,
present on the animal’s skin. When temperature and humid- from a vacuum cleaner) can all trigger emergence. Cats typi-
ity are optimal, eggs hatch in 3–7 days on the ground. The cally catch fleas by passing through an infested environment,
maximum number of eggs will usually be found where pets either outdoors in the right season, or indoors (e.g., when visit-
are resting. ing someone else’s house), and they often bring fleas into their
The larvae are a few millimetres in length and are non-par- own house, where they then breed and become a source of in-
asitic, feeding on organic debris, mainly skin debris and adult festation for other cats or dogs sharing the same environment.
flea faeces (desiccated blood). They prefer dark and humid
conditions and can move horizontally for about 20 cm in se- Ecology
cluded places (for example, under sofas, carpets and rugs, or Most flea species infesting wild animals are nidicolous, so
in pet bedding) L1 and L2 are very sensitive to UV light and they live in nests or burrows and infest their hosts just to
desiccation. take their blood meal. Their reproductive cycle may run
Having passed through three larval stages over a period of in parallel to their hosts’, which is the case for the rab-
a week to a month, each L3 spins a cocoon in which it met- bit flea, S. cuniculi, whose population increases when
amorphoses into a pre-emerged flea within about 10 days. their rabbit or hare hosts give birth to their progeny.
EXTERNAL PARASITOSES
The cocoon is sticky and is surrounded by debris which pro- These nidicolous fleas mainly infest small mammals (ro-
tects it (Figs. 10 and 11). dents, lagomorphs, bats) and birds.
Adult fleas quickly emerge from the pupae if hosts are The situation is different for fleas which infest carnivores
nearby but, if no hosts are available, the non-emerged adult as adult stages of these fleas are more permanent parasites,
fleas can survive for 6 to 12 months, protected by their co- remaining in the host’s fur. The environment is then contami
coons. Pre-emerged fleas are an important reservoir of new nated by the immature stages (eggs, larvae, and pre-emerged
fleas which are relatively resistant to insecticides while pro- fleas in their cocoons) which represent the source of infes-
tected by their cocoon They are easily transported from one tation. It is this distribution between adults and pre-adults
place to another by animals and humans as they are sticky which makes controlling fleas on pets so difficult, as well as
and attach to shoes, socks, trousers, etc. the low host specificity.
Newly emerged fleas actively seek out a host (preferably Most pet owners just wait until they see their pet scratch-
a cat or dog) and can survive for about a week without a ing, then want to kill the fleas which are actually on the ani-
blood meal. mal, but the most difficult aspect of flea control is that most
Environmental conditions affect the development and pet owners do not realise the importance of the pre-existing
timing of flea life cycles. Each stage in the life cycle is suscep- environmental infestation or understand its relationship to
tible to desiccation and relative humidity of 85 % is optimal. flea biology.
Temperature can accelerate or slow down development. The This is why the concept of integrated flea control is so
minimum temperature for C. felis seems to be 22 oC, with important. By the time a pet owner notices fleas on his/her
the optimum being 25–26 oC. Temperatures above 30 oC re- pet, there is already a large biomass of flea life stages pre
duce adult lifespans. In winter, an outside temperature below sent in the pet’s environment. Flea biology dictates that it will
0 oC is fatal to larvae and pupae. The life cycle slows down take approximately 1–2 months for these life stages to com-
considerably at 17–19 oC, but pre-emerged adults survive, plete their development: for the eggs to develop into larvae,
waiting for more favourable conditions. This means that then into pupae and finally into pre-emerged adults ready to
fleas can survive all year round, with a sudden population emerge from the pupal cocoon and jump onto a passing ani-
explosion in spring. mal. It is therefore biologically impossible to eradicate a flea
infestation overnight, regardless of which product is chosen
to treat the animal.
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It is important to understand that the length of time it will of reinfestation and the reason that fleas can still be seen on
take to resolve any individual flea problem is governed by a pets which are consistently treated with a long-lasting anti-flea
number of factors that are unknown at the beginning of the product. Seeing a few fleas on a treated pet does not equate to
treatment. product failure and expecting pets with access to the outdoors
to be “flea free” in humid, tropical conditions is unrealistic.
The most important ecological questions in flea control is:
• Where are the fleas coming from: indoors/outdoors or a Clinical signs
combination of the two? The source of fleas can be neigh- Fleas are responsible for numerous clinical signs, and allergic
bouring cats and dogs, but also stray cats and wild ani- animals should be differentiated from non-allergic animals.
mals, such as opossums, raccoons, etc. The reservoir of The vast majority of animals suffer from irritation and pruri-
pupae could be located outside the house, in the basement, tus (Fig. 12): they continuously scratch, groom, lick or nibble
in the garden or even outside the garden, in a place where at themselves, more or less vigorously, in an attempt to catch
dogs and cats often visit. the fleas, swallowing them in the process. Cats are very suc-
• How many immature stages are already present in the en- cessful, and this largely explains the infestation by Dipylidi-
vironment? The life cycle never stops in tropical and Med- um caninum cestodes, with fleas as intermediate hosts. Toler-
iterranean climates, but it stops outdoors, and slows down ance of this infestation varies drastically from one animal to
indoors, during cold periods (and also during hot and dry another: some cats are able to withstand infestation by hun-
periods), and increases in spring, in temperate and conti- dreds of parasites and only express mild pruritus, whereas
nental climates. others present with allergic dermatitis with only a few fleas.
• How long will it take for the immature stages to complete
their development? This can vary according to fluctuations
at a microclimate level.
• Is there an ongoing source of new flea eggs in the
environment?
Flea allergy dermatitis (FAD) is triggered by individual Beside intense pruritus with scratching wounds, other le-
factors and the antigens that provoke this immuno-inflam- sions in cats and dogs include diffuse hair loss, primarily but
matory response come from flea saliva. Cats and dogs with not exclusively on the lumbosacral area. Chronic inflamma-
FAD overreact and show some typical, and some less typical, tion can alter the skin’s appearance, which thickens (ortho-
clinical signs (Fig. 13–15). These clinical signs correspond keratotic hyperkeratosis) and acquires a greyish colouration
to a mast cell-mediated cutaneous hypersensitivity reaction, (melanosis). Secondary infection by yeasts (Malassezia pach-
with tissue infiltration by polynuclear cells (including baso- ydermatis) or Staphylococcus intermedius is common.
phils and eosinophils) and increased IgE production. De-
granulation follows, and inflammatory mediators (especially
histamine, serotonin and various leukotrienes) are released,
provoking a skin hypersensitivity reaction.
EXTERNAL PARASITOSES
Figure 14. Typical appearance of flea allergy dermatitis in dogs with dorsal alopecia and squamosis.
Pictures from Canine Dermatology Guide, E. Guaguère and P. Prélaud, Ed. Merial, 2008.
Figure 16. Skin of a cat with flea allergy dermatitis which has Figure 17. Hypersensitivity to flea bites in a human.
licked itself repeatedly.
Figure 18. Flea faeces on a cat’s chin, with scratching injury. Figure 19. Flea faeces visible in the fur.
Other clinical signs are more specific to cats, such as mil- Diagnosis
iary dermatitis, which is defined by numerous papules and The diagnosis of flea infestation relies on finding fleas in
scabs on the back and around the neck, which feels as if it is the coat, but it sometimes presents great difficulties due to
covered with sand. The animal scratches itself continuously the mobility of the fleas. The tail, ventral face and neck are-
and can even harm itself with its claws. Continuous licking as must be examined for fleas and finding the insects in the
and self-inflicted injury are also possible and hair loss can be fur can be very difficult. It has been demonstrated that only
seen on the abdominal area, legs, flanks or tail (Figs. 15 and 5–15 % of fleas carried on an animal are discovered. Finding
16) as a result. Flea saliva allergens may also result in feline just one flea, or flea droppings, therefore justifies treatment.
eosinophilic complex with various clinical manifestations: The level of infestation is described as average (<5 fleas), high
granuloma or cutaneous eosinophilic plaques, labial ulcera- (5–10 fleas) or very high (>10).
tion, lymphadenopathy. Flea faeces are easier to find than the fleas themselves, ap-
Besides this directly pathogenic involvement of fleas, they pearing as a small “comma-shaped” grain of up to 1 mm in
play an indirect role in pathogenesis by spreading Dipylidi- length when intact and, when dampened on white paper, the
um caninum, Taenia and Bartonella henselae, the agent of “flea dirt” appear as a reddish colouration due to the flea’s
“cat scratch disease” in humans (Fig. 17). blood diet (Figs. 18 and 19).
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EXTERNAL PARASITOSES
There is literature worldwide concerning the infection of cats by
“Haemobartonella”, now called Mycoplasma haemominutum or
Putative transmission of other
Mycoplasma haemofelis. The prevalence of infection is usually
pathogens
high (20 % to 40 %), but pathogenicity is still considered to
Some authors have suggested the possible role of fleas as vec-
be low, except where there is co-infection, for example, with
tors for many pathogens. FIV and FeLV viruses have been stu-
FIV-FeLV in cats.
died, but no proof of a vector role has yet been published. It
is important to remember that finding pathogen DNA in fleas
Flea-borne spotted fever due to collected from cats, dogs or other animals through PCR only
Rickettsia felis means that the flea has ingested the pathogen (dead or alive,
Rickettsia felis emerged recently as a new pathogen in humans, whole or fragmented) in the blood of its host, and nothing
responsible for flea-borne spotted fever, also called cat-flea more. There has recently been some controversy regarding the
typhus. role of fleas in the transmission of Leishmania infantum to
dogs, but the distribution of canine leishmaniosis would likely
This bacterium was first detected in the cat flea, C. felis, in
be very different if fleas could act as vectors. Experimental de-
1990, using molecular biology. DNA fragments of this organism
signs using natural transmission are necessary to demonstrate
were then detected in blood samples taken from the first human
a vector role: from host to vector, and from vector to host. In the
patient, in Texas. It is thought to be distributed worldwide, like
case of fleas, transovarial transmission should also be demons-
its main vector, C. felis.
trated, bearing in mind that adult fleas do not usually move
The prevalence of R. felis can be very high, and it varies with from one host to another.
environment and season. Although C. felis is the main biologi-
cal vector for R. felis, this bacterium has also been detected in
C. canis, P. irritans (the human flea), and A. erinacei. R. felis
has also recently been found in X. cheopis, the Oriental rat flea.
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Control measures
Fleas both on the animal and in its environment must be con- furniture) to be defined, which can be difficult. The environ-
sidered to prevent infestation. Preventive agents must have ment should be considered in its larger context, not only the
two properties: an immediate effect and a long-lasting effect habitat, or places where the animal travels to, but also other
(sustained action) (Fig. 20). To interrupt the insect cycle, fleas animals (other cats, dogs) which may come into contact with
must be eliminated before they can reproduce and lay eggs, the animal. Where possible, all animals encountered should
therefore before the end of the first 36 hours, as indicated be included in the prevention programme and regularly
on most insecticides. Some products have a rapid effect (less treated for flea infestation. Environmental (household) for-
than 24 hours) combined with sustained efficacy and these mulations usually contain both an insecticide and a growth
interrupt the cycle completely. The combination of IGR and regulator (juvenile hormone analogue) which interfere with
insecticides to treat dogs and cats has been proven to be use- the normal development of immature stages. Diffusers are
ful to accelerate flea eradication in the environment, especial- a volumetric treatment which enables widespread distribu-
ly when owners do not treat for fleas regularly. tion of insecticide molecules. Sprays are particularly useful
Controlling fleas in the environment requires all of the for inaccessible zones but, as these products cannot reach all
potentially infested areas (sleeping areas, carpets, cars, environmental life stages, efficacy remains partial.
Video 7.1
The flea risk.
Video 7.2
Adult fleas
in a dog’s fur.
Figure 20. Anti-flea treatment applied topically (A)
or given orally (B) to a dog.
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Lice infestation
General comments found on pets which lead an outdoor life, bringing them into
Lice infestation in dogs is most commonly caused by the direct contact with other animals. Louse species are very
chewing (or biting) louse Trichodectes canis (family Tricho- host-specific, and there is no risk of transmission between
dectidae; Fig. 1) than by the sucking louse Linognathus se- pet species, or to humans.
tosus (family Haematopinidae; Fig. 2), characterised by an Lice are small, grey-brown insects, dorsoventrally flat-
elongated head, like other sucking lice, such as the human tened and wingless. All louse species spend their entire life
louse Pediculus humanus. Mixed infestations can also occur. on the host and are very host-specific. Adult female lice lay
The only cat louse is the chewing louse Felicola subro- individual eggs and attach them to individual hairs. Imma-
stratus (Fig. 3). ture lice (nymphs), resembling small adults, hatch from the
Lice infestation is a rare ectoparasitosis in domestic pets egg after approximately 1 to 2 weeks and then develop into
but a common one in both stray cats and dogs. It can be mature adults over the next 3 weeks.
EXTERNAL PARASITOSES
1 mm 1 mm
1 mm 1 mm
D.H.
Dog (T. canis) or cat (F. subrostratus)
Lice have stout mandibles on the
ventral side of their head. They feed
on epidermal scales and sebaceous
Nymphs moult and gradually secretions, and, occasionally also
grow until they reach the adult on blood
stage (simple metamorphosis)
Adults
50 µm
Figure 5. Louse egg (nit).
D.H.
Dog and fox
Adults and nymphs can move
to new hosts or remain on the
same host to complete their
EXTERNAL PARASITOSES
life cycle. Most transfer occurs
during direct contact between
Nymphs moult hosts
and gradually grow
until they reach the
adult stage (simple
metamorphosis)
Adult
Nymphs
Clinical signs
Small numbers of lice may go unnoticed but heavy infesta- Figure 8. Lice infestation in a dog.
tions, particularly of chewing/biting lice, may cause alopecia
and dermatitis. Depending on coat colour, louse eggs cement-
ed to hairs may be easily visible (particularly against dark
hairs) or the lice themselves may be visible against pale skin. No treatments are indicated for sucking lice in dogs, but
A heavy L. setosus infestation may cause anaemia. treatments indicated for chewing lice should be effective.
A single treatment may be all that is required if the prod-
Diagnosis uct’s residual activity ensures that immature lice hatching
EXTERNAL PARASITOSES
Lice are visible to the naked eye and are characteristically from eggs after application will also be killed (egg shells are
flattened dorsoventrally. Eggs can be seen as pale structures not very permeable to insecticides). However, it is worth
attached to hairs (Fig. 8). checking that there are no remaining signs of lice after ap-
proximately a month, particularly where infestation has been
Control measures heavy, to evaluate whether further treatment is necessary.
A range of insecticides are recommended for treatment of Although it has not been studied, the insect growth regula-
chewing lice on cats and dogs, and all animals of the same tors (IGRs) used to control fleas (i.e., pyriproxyfen, (S)-meth-
species in the household should also be checked and/or treat- oprene, lufenuron) may have an effect on louse reproduction
ed at the same time as the animal with the louse infestation. and development of the nymphal stages.
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Figure 1.
Lucilia
sericata. Figure 4. Cordylobia sp. stage 3 larva.
Figure 5.
Figure 2. Sarcophaga
Musca sp. fly. sp. fly.
TABLE OF
CONTENTS Entomoses 227
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Lucilia sericata are attracted by moist areas of the body, Powerful hooks and proteolytic enzyme secretion give lar-
skin lesions, urine and diarrhoea, where they lay several vae a great capacity for tissue destruction which then attracts
thousand eggs in clumps of 50–100. more flies.
Cutaneous myiasis mostly occurs in the summer. Predis- D. hominis and C. anthropophaga larvae may also para-
posing factors include unprotected wounds, constant mois- sitise humans.
ture on the body (caused by urine and faecal staining in
recumbent, debilitated dogs, for example) and close contact
with sheep (especially W. magnifica and L. sericata).
EXTERNAL PARASITOSES
from the eggs
Stage 3 larva
on exudates
ole
loc
ate
d
Adult
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Figure 6. Maggot.
Figure 7. Myiasis in a dog. Figure 8. Myiasis lesions in (A) a dog and (B) a cat.
Courtesy of Blaise Hubert.
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CONTENTS Entomoses 229
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EXTERNAL PARASITOSES
Calliphoridae (L1 to L3). Anterior end thin, final segments larger. Stigmatic plates, very pronounced in
L3, composed of three very straight clefts converging on the terminal button.
Diptera, Brachycera, • Adult: large (12 mm). Dark blue mouth with orange eyes.
Cyclorrhapha, • Larva: first stage (3 mm) subcylindrical. Spines on each segment. Very characteristic
Dermatobia hominis
Cuterebridae second stage (5–6 mm) divided into anterior globular part (11 segments) and posterior
(South America)
(related to part extending to the tail. Last stage (10 mm) cylindrical, with small spines on
Oestridae) intermediate segments and two distinct clumps of spines on the anterior surface.
• Adult: hairy, greyish fly with no metallic sheen. 8–14 mm. Round spots on abdomen.
Diptera, Brachycera,
• Larva: yellowish maggot, blackish buccal sclerites clearly visible. 1–6 mm according to
Wohlfahrtia magnifica Cyclorrhapha,
stage (L1 to L3). Anterior end thin, final segments larger. Posterior stigmatic plates very
Sarcophagidae
pronounced in final segment of L3, and composed of three very straight clefts.
• Adult: hairy, greyish fly with glossy sheen. 8–12 mm. Black lines on abdomen.
Diptera, Brachycera,
• Larva: yellowish maggot, blackish buccal sclerites clearly visible. 1–6 mm according to
Sarcophaga spp. Cyclorrhapha,
stage (L1 to L3). Anterior end thin, final segments larger. Posterior stigmatic plates very
Sarcophagidae
pronounced in final segment of L3, and composed of three very straight clefts.
Precise identification of dipteran larvae is very difficult and can only be carried out by a specialist. Identifying adults is easier although there are
many dipteran species.
General description of dipteran larvae: usually three stages, L1, L2 and L3.
Larvae (sometimes called maggots, especially those of the fly family Muscidae) usually conical, pointed in front and truncated behind.
Larvae have 13 segments but the first two are fused (so only 12 are visible). Acephalic, eyeless, no antennae. Mouth with cephalopharyngeal
chitinous exoskeleton; two anterior hooks (labial sclerites) and two posterior, pharyngeal sclerites used in classification.
Caudally, larvae have two respiratory stigmatic plates, each consisting of a chitinous, often circular, plate or peritreme, with a false orifice
(button) and respiratory orifices, grouped together in three sinuous or straight stigmatic clefts.
Video 8
Cutaneous myiasis
on a dog.
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Diptera, Brachycera
Flying insect bites Biting flies include stable flies (Stomoxys calcitrans [Fig. 1]),
horn flies (Haematobia irritans), horse flies (Tabanus spp.)
and deer flies (Chrysops). They can induce severe pruritic le-
sions, such as crusts, erythema and oedema, often localised
A number of flying insects can cause problems in animals, on the nose, face and ears (Fig. 2). Reactions are caused by
such as the Diptera and Hymenoptera. hypersensitivity to the biting insects” antigenic saliva.
EXTERNAL PARASITOSES
Figure 3. Mosquito feeding. Figure 4. Sandfly feeding.
Adults emerge
through a T-shaped
hole in the back of
the pupa
Adult female
Adult
Males live ~ 7 days (feed on plants)
Females live 4–5 months (capable of hibernation)
The adults
lay eggs in
water, then
The pupal seek a new
stage lasts blood meal
2–
3
from 2 days
ar
da
ye
ys
to 1 week Pupa
to
ys
7 days
Da
Eggs
Larvae
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CONTENTS Entomoses 233
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Adult
Pupa } Phlebotomus
(Africa, Eurasia)
} Lutzomyia
EXTERNAL PARASITOSES
(America)
Acarioses
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Tick infestation
Introduction
Ixodidae, known as hard ticks, are giant mites. They have
adapted to live in all habitats and to feed on any kind of host,
from reptiles to mammals. In industrialised countries, they
are also known for their major impact on animal health,
including pets or sport animals (dogs, horses) and livestock
(cattle). They are vectors for many pathogenic agents: virus-
es, bacteria, protozoa or helminths, some of which are com-
mon in humans and animals (Colwell et al., 2011). The most
important tick genera infesting pets worldwide are Ixodes,
Rhipicephalus, Dermacentor, Amblyomma and Haemaph-
ysalis (Fig. 1).
EXTERNAL PARASITOSES
are characterised by three life stages: larva, nymph and adult, (carnivores, humans) when their usual host is unavailable.
each requiring only one blood meal before developing into Otobius megnini is distributed in the Americas. It usually
the next stage. The main genera are Hyalomma (27 species), locates in the ears of mammals, including dogs and cattle (see
Amblyomma (143 species), Rhipicephalus (79 species, in- life cycle, page 253).
cluding Boophilus species), Dermacentor (38 species), Hae- The next paragraphs will only focus on hard ticks, given
maphysalis (166 species) and Ixodes (249 species). their medical and veterinary importance .
Argasidae are mainly bird and reptile parasites, charac-
terised morphologically by a downward-curving rostrum Geographical distribution
(on the underside of the head) and by the lack of a scutum, and host preference
which together define their status as soft ticks. They are char- Hard ticks are distributed worldwide but each species is re-
acterised by the succession of one larval stage, four to six stricted to a particular biotope and climate (Fig. 3). Popu-
nymphal stages, and one adult stage, and by having several lations in each habitat may be subject to marked seasonal
blood meals in the nymphal and adult stages (only one in changes.
Morphology of hard ticks
Stages Anatomy
• Larvae: 0.5–1 mm, hexapods (Fig. 5). • Anterior extremity: mouthparts or gnathosoma
• Nymphs: 3–5 mm before blood meal, octopods (Fig. 6). The gnathosoma is found in the capitulum comprising the
• Adults: 5–10 mm before blood meal, up to 30 mm for en- rostrum or hypostome (single piece, toothed), two cheli-
gorged females (Fig. 7), octopods, sexually dimorphic. cerae and two pedipalps. Pedipalps are tactile organs that
help the tick choose biting sites. Chelicerae, which end in
harpoon-like structures, pierce the skin, anchor the tick
to the skin after muscle contraction and help the hypos-
tome penetrate the skin. Backward-pointing barbs on the
hypostome secure the attachment. Ticks are either brevi-
rostris (Rhipicephalus, Haemaphysalis, Dermacentor) or
longirostris (Ixodes, Amblyomma, Hyalomma), according
to the length of the rostrum. The tick always anchors its
rostrum sideways because its gnathosoma cannot be bent
(Fig. 8).
EXTERNAL PARASITOSES
Figure 5. Tick larva - Ixodes.
Figure 7.
Engorged female
- Rhipicephalus. Figure 8. Tick rostrum.
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Figure 9. Haller’s organ. Figure 10. Tick claw and sticky pad to infest host.
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EXTERNAL PARASITOSES
northern and eastern Australia (mainly Queensland).
Different stages of the same species may be either endophilic • D. reticulatus: larvae and nymphs usually feed on micro-
or exophilic. mammals, whereas adults will await a passing dog or horse.
• H. longicornis: larvae and nymphs usually feed on micro-
Climate variations mammals, but adults target ungulates (domestic and wild
In addition to the biotope, temperature and humidity play key ruminants). All stages can also bite any mammal that they
roles in determining the presence of one species or another. encounter (human, dog, cat, etc.), which is why this tick is
• Hygrophilic ticks: require humidity and do not tolerate ex- the vector for canine babesiosis in Japan.
cessive heat and desiccation. • R. sanguineus: all stages prefer to parasitise canids, but
This is the case for many Ixodes such as I. ricinus in Eu- cats may also be infested.
rope, I. scapularis in the USA, I. persulcatus and I. ovatus
in Asia and Japan, and Dermacentor ticks like D. reticula- Attachment to the host
tus in Europe and D. variabilis in America. Ticks find their hosts by detecting heat, vibration, shadows,
• Xerophilic ticks: live in warm areas and may tolerate des- breath (CO2) and odour. They use the Haller’s organs locat-
iccation, but not frost. ed on the tarsus of first leg, which help them locate a host
This is the case for R. sanguineus. Other may prefer warm, and gauge their distance from it. In order to locate their host,
humid conditions and be susceptible to desiccation, like H. ticks rely on features such as heat, smell, sight and touch.
longicornis in Asia.
Figure 11. Questing female Dermacentor. These two habits are quite similar to those seen in spiders,
which belong to the order Araneae and the same Arachnida
class as the Acari. Some spiders spin a web and wait for their
prey to get caught while others hide and attack their prey.
Ticks infest theirs hosts rather quickly, in a matter of sec-
onds. They usually do not jump down onto the host since
they do not live in trees, but close to the ground and on
stretches of grass. They grab onto the host with the sticky
pad on their tarsus and then use their legs and claws to crawl
through the fur and over the skin, to find a suitable place to
attach and feed (Figs. 2 and 14).
Figure 13. Questing female Ixodes on grass. Courtesy of Phil Ward. Figure 14. Haemaphysalis longicornis attached to a dog.
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Attachment
• The process of tick attachement involves many specific
organs of the tick, such as the chelicerae and hypostome.
First, the tick uses its tactile pedipalps to locate the at-
tachment site, then it attaches with its chelicerae, which
Figure 15. Attached ticks in a dog’s ear. look like harpoons with two terminal hooks. These pen-
etrate the skin and are retracted by the tick through mus-
cular contraction which allows the skin to be penetrated
obliquely by the hypostome.
• Upon attachment, the tick secretes cement for 10–30 min-
EXTERNAL PARASITOSES
utes (primary and secondary cement produced by types II
and III salivary gland acini). This cement is made up of
glycoproteins that polymerise on exposure to air and skin.
• As soon as attachment occurs, some pathogens may be
transmitted and the first pathogenic agents to be inoculat-
ed must be present in the saliva and immediately infective.
This is the case for viruses, which may be inoculated with-
in 15 minutes after the start of attachment.
The meal is not strictly a blood meal, as it is for mosquitoes, • The second phase is the rapid ingestion phase: the tick in-
as it contains not only blood but digested tissue and many gests the fluids and cells and the volume of the female in-
leucocytes. Food intake occurs in two phases: creases dramatically (from 30 to 250 mg) (Figs. 18 and 19).
• The first, which can be called a preparatory phase, involves The female concentrates the ingested meal and excretes the
intense secretory activity during which the tick produces excess fluid in order to prevent osmotic shock.
enzymes and peptides, inducing immunomodulatory, an- • Each phase involves the activity of different salivary
ticoagulant and proteolytic effects. This phase creates an gland acini. Besides enzymes, the saliva contains peptides
area of haemorrhagic necrotising liquid through the diges- which act as cytokines with an immunomodulatory role.
tion of subcutaneous tissue which attracts many leucocytes This prevents a protective immune response by the host,
(monocytes, phagocytes, granulocytes). This preparatory which is uncommon in mammals except guinea pigs,
phase lasts at least 3 days, during which the tick exchanges which develop basophilic hypersensitivity to tick bites.
fluids with the host. The volume of the female tick does not This immunomodulation attracts many white blood cells ,
increase much during this phase (from 2 to 30 mg). and these will form part of the meal and “help” the process
of localised necrosis to occur. This also favours pathogen
transmission, as occurs in other vectors, such as mosqui-
toes (Plasmodium) or sandflies (Leishmania).
• Pathogenic agents can be transmitted throughout the whole
blood meal. The directly infective bacteria in the saliva are
inoculated quite quickly, an average of 3 to 24 hours after
attachment. This applies to Ehrlichia, Anaplasma, Rick-
ettsia, etc. Other pathogens, such as Borrelia burgdorferi
sensu lato, must undergo multiplication and antigenic var-
iation to become infective, so transmission occurs later,
usually after 36 to 48 hours. Babesia sporozoites have to
become infective and migrate to the saliva so they are usu-
ally transmitted 48 to 96 hours after attachment.
• Females will actively detach at the end of the blood meal,
and fall off the host onto the ground.
Figure 19. Engorging Rhipicephalus in kennelled dog. Figure 20. Engorged Rhipicephalus ready to lay eggs.
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Figure 21. Ticks mating. Figure 22. Rhipicephalus female laying eggs.
Courtesy of Emanuele Brianti.
EXTERNAL PARASITOSES
different tick-borne pathogens, often more humans
than one at a time.
und,
n the gro
ys eggs o
lts
ale la
Adu
fem ission)
The adult rial transm
(transova
and dies
Ny
La
mp
hs
Larvae
The larv p into nymphs
and dev
ae drop
elo
Reproduction and egg-laying ground, they will search for a crevice to hide in, and lay
Females and males mate on the host and mating occurs be- their eggs within 48 to 72 hours. The females bend their
fore or during the female’s meal (Fig. 20). Ticks of some gen- anterior extremity which splits dorsally on the capitulum
era secrete pheromones to attract ticks of the opposite sex. (camerostomal fold). The egg-laying phase will last 48 to
Pathogens can be exchanged between one tick and another 72 hours and the female will die at the end. The eggs are
during co-feeding at the same location. protected and clustered together by a yellow lipid wax and
In utero egg formation starts during the female’s blood an average of 3,000 to 10,000 eggs is laid at once (Figs. 21
meal and, after the females fall off their host onto the and 22).
Mo
ult Females engorge
6–21 days
nd dies
ggs a
d lays e
d fee Dro Fem
ale
ttach an po
A ff
Engorged nymph
Engorged larva
EXTERNAL PARASITOSES
Cycle duration varies widely and depends on both climatic ing paralysis in their hosts: ascending tick paralysis in Aus-
conditions and host behaviour. The life cycle may be inter- tralia (I. holocyclus), Africa (I. gibbosus), and America (D.
rupted: egg diapause (exceptional); behavioural diapause in andersoni). The Australian paralysis tick is the best-known,
larvae, nymphs or adults, awaiting favourable conditions; due to its potentially fatal effects and the thousands of cases
diapause in fasting stages for up to a year, waiting for a host. diagnosed in dogs each year. This tick is a tropical Ixodes
There may be just one stage per year in ticks like I. ricinus whose natural hosts are marsupials, but pet and human infes-
or D. marginatus i.e., a complete cycle and one generation tation is easy due to the presence of possums or other marsu-
in 3 years. There may be more generations per year if the pials in backyards. An antitoxin is available in Australia due
climate is favourable and there are many hosts: 7 days per to this incidence of human cases, especially children.
meal, moulting within 3–4 days in the environment, the
same for egg-laying, waiting for new hosts, so a minimum of Indirect pathogenic role
2 months for one generation, at best. Ticks are the most important vectors in veterinary medicine
If we link this to the vertical transmission of pathogenic because of the range of diseases transmitted, their economic
agents from the female to the eggs, demonstrated over three importance in production animals and their zoonotic im-
or four tick generations in some pathogens like Babesia can- pact. This is not the case in human medicine, where mosqui-
is, the ticks in a “tick area” transform it into a “babesiosis toes are the predominant vectors.
area” for many years, without an infected dog having to en- Transstadial transmission is one of the conditions required
ter that area. In this case, ticks are not only the vector, but for ticks to be vectors and the infected stage is never a vector.
also the reservoir of the disease. Ticks alone can maintain
babesiosis levels and they do not need carnivores to survive, The agents transmitted can be categorised in many groups:
as they can feed on small mammals. • Viruses (>99 %): responsible for tick-borne encephali-
tis (classic tick-borne encephalitis virus, Powassan fever,
Kyasanur forest disease, Omsk haemorrhagic fever and
Langat virus, ovine encephalomyelitis or louping ill, Colo-
rado tick fever, etc.).
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• Rickettsiae: responsible for ehrlichiosis, anaplasmosis, The requirements for a good anti-tick product are:
coxiellosis (Q fever), cowdriosis, Rocky Mountain spotted • To be curative and preventive:
fever, Mediterranean spotted fever, African spotted fever, • Curative = kills and detaches existing ticks;
Australian spotted fever, Queensland tick typhus, Siberian • Preventive = quickly kills any ticks infesting the animal,
tick typhus, etc. if possible before pathogen transmission;
• Other bacteria: responsible for tularaemia, dermatophilo- • Sustained: effect persisting for a certain period of time
sis, Lyme disease, etc. (from one month to several months).
• Protozoa: • To be waterproof (swimming, rainy season, etc.) as dogs
• Babesia: inevitable and exclusive biological vector, the are usually infested during outdoor activities.
tick is the definitive host. • To have a good distribution over the body (for products
• Theileria: inevitable and exclusive biological vector, the which act on contact).
tick is the definitive host.
• Hepatozoon canis (transmission by ingestion of the The objective of anti-tick treatments is not only to kill ticks,
tick). but to reduce the risk of tick-borne pathogen transmission
• Helminths: filarial parasites (Acanthocheilonema and where possible. Prevention of Babesia canis, Borrelia burg-
Cercopithifilaria). dorferi, and Ehrlichia canis by several anti-tick products has
been demonstrated and published.
Diagnosis
Diagnosis is based on inspection of preferred attachment Environmental control methods can be added in particular
sites and observing ticks attached to the skin. circumstances, especially against the kennel tick Rhipiceph-
During tick seasons and in tick areas, owners must always alus sanguineus:
be advised to search for ticks after walking their animal, even • Clean up and reduce wild/feral animal habitats (destroy
if their antiparasitic treatment is up-to-date. refuge areas for animals that serve as alternative hosts for
Tick species, stages and level of engorgement should be ticks).
identified to assess the risk of pathogen transmission. • Eliminate undergrowth (grass, weeds and brush), especial-
ly if they are close to buildings or animal housing.
Control measures (treatment of the • Prevent access to crawl spaces under homes, decks, or
animal during parasitic phases) outbuildings.
The tick control is still based on regular treatment of the • Pesticides can be used to treat the environment, especial-
animal with acaricides. These kill existing ticks and prevent ly kennel walls and cages, in cases of massive infestation.
new tick infestation. Protection can be short to long term, The risk of environmental pollution by spraying acaricides
depending on the formulation and the molecule used. should be taken into account.
When ticks are diagnosed, they must be immediately and • Some zoological measures are available, such as the use
carefully removed, then an anti-tick treatment should be ap- of various tick-eating bird species (“tick birds” in tropical
plied to the animal. areas, e.g., Buphagus in Africa; Moluccan bluebird, Acri-
dotheres tristis in Asia and the Pacific; and also chicken or
Treatment should limit infestation, providing “general Guinea fowl in gardens).
repellency”: • The use of entomopathogenic fungi, including Beauveria
• Disrupt tactile or olfactory chemoreception (direct repel- bassiana and Metarhizium anisopliae conidiospores, has
lency + irritant repellency); not been adopted in the field but should be considered as a
• And/or disrupt attachment (repellency in general); promising strategy.
• And/or inhibit feeding (repellency in general);
Risk to humans
Treatment should also kill quickly = acaricidal action Ticks will infest humans directly from the environment but
specifically there is no risk of transfer from an animal to a human.
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Diagnose of the main tick genera infesting dogs, cats and humans
• Phylum Arthropoda
• Absence of antenna, presence of chelicera: subphylum Chelicerata
• Aerial respiratory system: class Arachnida
• Body formed by the prosoma and the opisthosoma which are not clearly separated; 8 legs in
the adult stage: order Acari
• Respiratory stigma behind the 4th leg; large acarines: Ixodida = ticks
• Terminal capitulum + dorsal scutum: Ixodoidea = hard ticks
• Anal groove anterior to the anus: Prostriata
• Long capitulum
• Genus Ixodes
• Ixodes ricinus (Europe)
• Ixodes scapularis (North America)
• Anal groove posterior to the anus or absent: Metastriata
• Brevirostris = short hypostome and palps
• Rectangular basis capituli
• Male has large coxa IV
-- Dermacentor
EXTERNAL PARASITOSES
-- Dermacentor reticulatus (Europe)
-- Dermacentor variabilis (North America)
• Male has normal coxa IV
-- Haemaphysalis
-- Haemaphysalis longicornis (Asia - Pacific)
• Hexagonal basis capituli
• Festoons present
-- Rhipicephalus
-- Rhipicephalus sanguineus (worldwide)
• Longirostris = long hypostome and palps
• Dorsal scutum colorized
• Male has no ventral plates
• Amblyomma
• Amblyomma americanum (North America)
TABLE OF CONTENTS
IXODES
AMBLYOMMA
3.5 mm
6.5 mm
Female dorsal
Female dorsal
Female ventral
4 mm
3 mm 4 mm
Male dorsal
Male dorsal Male dorsal
1. Ixodes
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Female dorsal
2. Ixodes
Male dorsal
1 2
3. Rhipicephalus
Female dorsal
4. Rhipicephalus
Male dorsal
3 4
5. Dermacentor
Female dorsal
6. Dermacentor
Male dorsal
5 6
7. Amblyomma
Female dorsal
8. Amblyomma
Male dorsal
7 8
9. Haemaphysalis
Female dorsal
9
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The larvae parasitise the external Nymphs feed and develop through
auditory canal of the host, feed for several phases or stages, but all
several days, and moult to become occur in the ear of the same host
nymphs
Nymph I
Larva
EXTERNAL PARASITOSES
Larvae can
survive several
months without
feeding Adults in the environment
Adult ticks do not
feed, they breed in the
environment and the
females produce eggs
Video 9
The tick risk.
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D.H.
Dog, cat and other carnivores Mites feed on epidermal
debris in the ear canal and
All stages of this mite live deep the secretions produced
down in the external ear canal. by inflammation
EXTERNAL PARASITOSES
The adults also parasitise the
skin near the ear
Nymph
3–5 days
Adults
5–11 days
3– ys
8
da da
4
ys 3–
Larva
Eggs
D.H. = definitive host
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Pathogenesis
O. cynotis causes irritation (mechanical and chemical) and
type I and III hypersensitivity reactions in its host. The pres-
ence of immunoglobulins E and G, and circulating immune
complexes has been demonstrated by passive cutaneous an-
aphylaxis tests. Antigenic cross-reactions shown by positive
intradermal reactions to Dermatophagoides farinae and
Dermatophagoides pteronyssinus are also extremely impor-
tant, because they raise the possibility of false positive reac-
tions to house dust mites in intradermal testing.
There are several primary causes of otitis externa, includ-
ing O. cynotis and other parasites such as Demodex spp.,
atopy and foreign bodies. A number of predisposing factors
are associated with otitis externa, such as moisture in the
ears due to regular swimming or bathing, for example, and
systemic disease, but none of these are pertinent to the es-
tablishment of O. cynotis infestation. Infestations are usu-
ally bilateral, affecting both ears and, in addition to being a
source of discomfort and irritation in the ear, they can occa-
sionally cause dermatitis elsewhere on the host. O. cynotis
can induce hypersensitivity reactions, the host becoming ex-
posed to mite antigens when the mite bites the host to ingest
body fluids. Secondary bacterial or yeast (M. pachydermatis)
infections, associated with the pruritus and consequent ear
Figure 5. Ceruminous otitis.
scratching and rubbing, are common, especially in dogs.
Clinical signs
The incubation period lasts for about 2 to 3 weeks following
infestation. Otitis, usually bilateral and erythemato-cerumi-
nous, ensues with dry (flaky or powdery), brownish-black
cerumen (Fig. 5). Aural pruritus is associated with a pin-
nal-pedal reflex, variable in intensity but apparently less in-
Figure 6. Pruritic
tense in the dog than in the cat (Figs. 6 and 7). Self-induced auricular reflex in
erosive, crusting lesions are often seen behind the ears and an infested cat.
secondary bacterial and fungal infections are common.
Skin involvement is rare but may occur when mites mi-
grate from the ear canal to neighbouring areas of skin, such
as the face (eyelids and interocular region in brachycephalic
breeds), pinnae, neck and cranial carpi. Skin lesions involve
hair loss, erosions, crusts and constant pruritus.
Systemic signs including aggression, fits and vestibular
syndrome (following rupture of the tympanic membrane)
may be seen.
Figure 7. Audito
pedal reflex in a
cat infested by
Otodectes cynotis.
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Figure 8. Otodectes cynotis female and eggs. Figure 9. Otodectes cynotis eggs.
EXTERNAL PARASITOSES
Microscopic examination of a sample from the external treatment by the owner. However, as most products do not
ear canal, mounted in liquid paraffin, chloral lactophenol have ovicidal effects unless they are effective for longer than
or 10 % potassium hydroxide may reveal otodectic mites; 3–4 weeks, a second administration may still be required to
adults and immature stages (eggs, larvae and nymphs) break the parasite life cycle, even if this is not actually stated
(Figs. 8 and 9). However, detecting the parasite is not always on the product label. Cleaning the ear to remove the ceru-
straightforward. minous exudate is often omitted from product labels but is
Cytology of an ear canal swab often reveals cocci and good practice and is thought to improve acaricidal efficacy.
yeasts (M. pachydermatis). It is usually recommended that all dogs and cats in a house-
When the skin is involved, skin scrapings reveal far fewer hold are treated simultaneously to prevent reinfestation from
O. cynotis (both adult and immature forms). asymptomatic carriers.
Differential diagnosis includes other causes of erythema-
to-ceruminous otitis, sarcoptic mange, cheyletiellosis, and
trombiculosis.
Prognosis
Prognosis is usually good, especially in young animals. It is
more guarded in dogs which are continuously reinfested and
also in older dogs with concurrent diseases, such as leish-
maniosis, diabetes and lymphoma.
Video 10
Moving ear mites in ear wax (Otodectes cynotis)
observed under the microscope.
Courtesy of Stéphane Girodon.
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Figure 1. Adult Sarcoptes scabiei. Figure 2. Sarcoptes scabiei nymph and eggs.
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D.H.
Adult mites mate on
Dog and fox
the surface of the skin
Nymphs and adults are
the main contagious
stages of S. scabiei
The mature female digs
EXTERNAL PARASITOSES
tunnels in the epidermis and
feeds on the basal layers
Nymph
~ ive
5 for
L
da a
ys bo
ays
fo ut
re 1
d
gg mo
7–9
pr nth
od
uc
tio
Adults
3–
4
da
ys
s
ay
–5d
g s3
Eg
Larva
A B C
D E F
Figure 3. Clinical signs of sarcoptic mange. A, B, C and D (typical distribution of the early lesion of sarcoptic mange): diffuse alopecia
of the legs, lower abdomen and face. E and F: diffuse erythema and crusted papules on the pinnal margins. Courtesy of Parasitology
Unit, Alfort Veterinary School.
Clinical signs
Classic form
The incubation period lasts about 3 weeks after contact with papules, crusted papules where mites penetrate the epider-
contaminated material. The classical form is characterised mis, and patchy hair loss) are seen only at the onset. Urti-
by intense pruritus and a positive pinnal-pedal scratch reflex carial lesions (papules and oedematous plaques) are seen in
(note that this reflex is present in only 75–90 % of sarcop- about 30 % of cases. Secondary lesions (excoriations, ero-
tic mange cases and can also be seen in other pruritic skin sions, crusts, lichenification and hyperpigmentation) soon
conditions). Initial distribution of lesions on the face (pin- follow in the case of intense pruritus. Superficial pyoderma
nal margins), lateral elbows and sternum is very indicative (folliculitis), bacterial proliferation syndrome and Malassezia
of sarcoptic mange. Primary skin lesions (diffuse erythema, dermatitis are commonly seen in cases of chronic mange.
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EXTERNAL PARASITOSES
sites, making them easier to find on the slide. Microscopic
examination is carried out at an initial magnification of ×40,
then ×100 and ×250, under low to moderate lighting. Only a
few parasites (1–2 adult sarcoptids) are usually found. Scrap-
ings should also be examined for eggs and mite faeces. In
Norwegian scabies, scrapings from thick crusts reveal huge
numbers of mites in different stages of development (adult,
larva and egg).
Serology
ELISA testing using a purified extract of S. scabiei is avail-
able and this test seems to be sensitive and specific, with no
cross-reactivity in dogs with house dust mite sensitivity. It is
particularly useful to distinguish sarcoptic mange from atop-
ic dermatitis, however, dogs with sarcoptic mange show posi-
tive intradermal reactions and may have allergen-specific IgE
and IgG to Dermatophagoides farinae and D. pteronyssinus.
Skin biopsies
Histopathology is of little use in diagnosis as sarcoptic mites
are rarely detected, but it does alert the clinician to the pres-
ence of an inflammatory skin condition: superficial perivas-
cular dermatitis mainly with eosinophils and mast cells, or
an eosinophilic pustular dermatitis also seen in allergic der-
matitis. It is not uncommon to see cases of sarcoptic mange
treated for atopic dermatitis, purely on the basis of this type
Figure 5. Skin scraping showing Sarcoptes mites and eggs. of histopathology report.
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Video 11
The pinnal-pedal reflex is usually
positive in case of sarcoptic mange.
Courtesy of Parasitology Unit,
Alfort Veterinary School.
EXTERNAL PARASITOSES
nerve endings in the host’s skin. Disease lesions usually be-
gin as erythematous papules on the head, specifically around
the leading edge of the ears, with rapid spread to the entire
upper surface of the ears, face, eyelids and thereafter to other
parts of the body such as the neck, feet and perineum (Fig. 4).
Figure 3.
Notoedric
mange in a
stray cat.
Figure 4.
Notoedric
mange
lesions on a
Figure 2. Notoedres cati female and larva. cat’s face.
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The skin becomes thickened, wrinkled and alopecic, and Control measures
excoriation caused by the intense pruritus usually leads to Products which are licensed for the treatment of sarcoptic
secondary bacterial infection and peripheral lymphadenopa- mange and also indicated as safe for use in cats are likely to be
thy. Untreated disease has occasionally resulted in toxaemia, effective against notoedric mange at the recommended dose
anorexia, cachexia, and death (Figs. 5 and 6). for cats. One spot-on combination containing eprinomectin
is licensed for the treatment of notoedric mange. Before treat-
Clinical signs ment, infested cats should be washed with an anti-sebor-
Notoedric mange in cats is characterised by severe pruri- rhoeic shampoo to soften and remove skin crusts. The key to
tus, initially with localised alopecia, erythema, scaling and treating this disease is simultaneous treatment of all affected
crusting leading to lichenification. Common sites include and contact animals, and regular cleaning/disinfection of the
the head, specifically the proximal edge of the pinnae and environment by vacuuming and washing bedding through-
neck. Excoriation leading to secondary bacterial infection out the treatment period. It is advisable to skin scrape all
is very common. The disease can become more generalised, treated animals regularly and to continue treatment until
with lesions spreading over the body as it does in Sarcoptes scrapes are negative and lesions resolve.
infestations.
Risk to humans
Diagnosis Notoedres cati is a zoonotic parasite. The lesions associated
Definitive diagnosis is by skin scraping, using the same tech- with human infestations are intensely pruritic but the mite
nique as for S. scabiei, and although the mites are smaller, does not reproduce on human skin and the disease will re-
they are more readily identified in skin scrapings, occurring solve spontaneously within 2–6 weeks.
more superficially and in greater numbers. N. cati is mor-
phologically similar to S. scabiei with similar short legs, but
the dorsal surface of the mite is covered with concentric rings
rather than the spines and triangular scales seen on S. sca-
biei, and the anus is located dorsally.
Figure 5. Hyperkeratotic lesions of notoedric mange in a cat. Figure 6. Cachexia in a cat suffering from notoedric mange.
Courtesy of Emanuele Brianti. Courtesy of Emanuele Brianti.
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EXTERNAL PARASITOSES
also been reported to parasitise fleas, lice and flies, which
Biology provide another mode of transmission for mammalian infes-
All stages of the life cycle can be found at the skin surface as tations. Cheyletiella may survive for several weeks in kennels
the mites are surface feeders and do not burrow into the skin and they are thought to be predators of acarian dust mites.
surface, and they prefer to infest the dorsal skin of their host. This explains how difficult it is to control cheyletiellosis in
Females lay eggs which attach to the hair by fibrillar strands groups of animals.
(Fig. 2). White, elongated eggs hatch into six-legged larvae
which develop into protonymphs, deutonymphs and finally Pathogenesis
new adults. The life cycle takes about 3 weeks. Mites can Squamosis can be severe in affected animals and mites are
survive about 5–6 weeks off the host, feeding on small mites usually present in large numbers, but occasionally the inten-
but they cannot breed off host. sity of the pruritus is disproportionate to the parasite burden,
perhaps due to hypersensitivity. An asymptomatic carrier
state is also common, particularly in adults.
Clinical signs
The primary clinical signs of cheyletiellosis are mild to mod-
erate pruritus and skin scaling (Fig. 3). Erythema and crusted
lesions may be seen in affected areas and the disease may
appear as miliary dermatitis in cats. The degree of pruritus is
very variable and does not appear to be proportional to the
mite burden, so some hosts carrying large numbers of mites
will only exhibit scaling with little or no pruritus, usually
along the dorsal aspect of the trunk (Fig. 4), whilst others
will be intensely pruritic. If the infestation is not treated in
time, scaling may become severe and widespread, leading to
hair loss.
Figure 3. Scales caused by cheyletiellosis.
Diagnosis
Diagnosis is made by mite identification. The easiest way to
collect material for examination is to sit the patient on a dark
surface and groom some of the scale from the skin surface.
If the animal has cheyletiellosis, the dislodged material may
appear to move (“walking dandruff”). This movement is vis-
ible as the pearly white, mobile, adult mites drag skin scales
along, trapped in the long dorsal hairs on their body surfac-
es. The material dislodged can be collected in a petri dish or
on a slide for microscopic examination at 40× magnification.
Mites and eggs can also be harvested using sticky tape strips
applied to the affected area and then stuck to a microscope
slide. Superficial skin scrapings can also be performed and
the material collected placed on a microscope slide with a Figure 4. Dorsal scaling caused by cheyletiellosis in a puppy.
drop of water under a cover slip. Individual mites can be ex-
amined by adding a drop of water to groomed debris on a mi-
croscope slide and covering it with a cover slip (Fig. 5): adults
have four pairs of legs that protrude beyond the body mar-
gin and palps with powerful curved terminal claws (Fig. 6).
The slightly hexagonal body has a “waist” just in front of
the two pairs of hind legs and all of the legs have combs on
the ends. Mite eggs may also be detected via coproscopy, be-
cause of the excessive grooming habits of some infested cats
and dogs.
Control measures
No treatments are specifically licensed for the treatment of
cheyletiellosis but the mites have proven susceptible to many
of the current topical acaricides licensed for use in dogs and
cats. The presence of asymptomatic carriers, the highly con-
tagious nature of the disease, with mites readily transferred
between hosts, and the ability of the female mite to survive
off-host make treatment of affected and contact animals a
wise precaution.
Risk to humans
Humans in contact with pets having cheyletiellosis can ac-
quire transient infestations which are seen as pruritic, pap-
ular lesions, often arranged linearly. Lesions are generally
seen in areas that come into contact with the pet, such as
Figure 6. Anterior part of an adult Cheyletiella mite. the torso, arms and anterior surface of the thighs and they
can occur even where clothing might been expected to pro-
vide protection (Fig. 7). Direct treatment seems unnecessary,
provided that the primary hosts are effectively treated, as the
EXTERNAL PARASITOSES
mites do not reproduce on humans.
Canine demodicosis
General comments
Canine demodicosis is a parasitic skin condition caused by
the characteristically cigar-shaped mite Demodex canis
(family Demodicidae) in dogs (Fig. 1). The disease is caused
by excessive multiplication of these host-specific, commen-
sal mite, in hair follicules and sebaceous glands. The mite is
a skin commensal believed to be transmitted from the dam
10 μm
when the young suckle. Signs of infestation are only seen
when mite numbers increase significantly. Mites complete Figure 1. Adult Demodex canis.
their entire life cycle on a single host.
Other species have been suggested (e.g., Demodex injai,
and Demodex cornei), but some authors consider that they
are only morphological variants of D. canis. Immunodefi-
ciency is a predisposing factor which is probably hereditary
in young dogs (under 2 years old) and acquired in adult dogs,
following development of an underlying cause (e.g., excessive
glucocorticoid therapy, Cushing’s syndrome, diabetes melli-
tus and neoplasia). It is common but also under-diagnosed
and can be very serious medically. Canine demodicosis can Figure 2. Demodex canis egg. Courtesy of Parasitology Unit,
also have dramatic consequences in breeding units: bitches Alfort Veterinary School.
that have given birth to puppies with demodicosis must be
removed from breeding, along with all their descendants.
D. canis has short legs, arranged in the shape sometimes
described as resembling the Brandenburg cross. The male
measures 150 μm in length and the female 200–300 μm.
Demodex mites mainly feed on scale and sebum, the produc-
tion of which they help increase. They never feed on blood
and are incapable of living off their host.
Epidemiology
Demodex sp. mites are highly host-specific but ubiquitous
throughout the canine population. The infestation and dis-
ease is not transmissible between adult dogs and is not ac-
quired from the environment.
About 50 % of adult dogs are asymptomatic carriers of
Demodex. The only time that dog-dog transmission can oc-
cur is during the first 72 hours of life when the newborn pup-
10 μm
py can acquire mites from the suckling bitch during washing
and feeding. At no other time can mites be transmitted be-
Figure 5. Adult Demodex canis. tween dogs.
D.H.
All stages of Demodex mites Dog
reside in the lumen of the hair
follicle and the duct of the
Dogs may act as
sebaceous gland
asymptomatic carriers.
EXTERNAL PARASITOSES
Clinical infestation develops
when the animal is
immunocompromised
Nymph
Puppies become infested by direct
skin contact while nursing
Adult
Larva
Eggs
D.H. = definitive host
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Although demodicosis can occur in any breed of dog, The absence of cytotoxic T lymphocytes in localised de-
there are clear breed predispositions which include the Staf- modicosis may allow spontaneous resolution. In generalised
fordshire Bull Terrier, Old English Sheepdog, Boston Terrier, demodicosis, the immune defect involves both cytotoxic T
French Bulldog, Bernese Mountain Dog, German Pointer, lymphocytes and helper T lymphocytes and enables parasitic
Boxer, English Bulldog, English Bull Terrier, Pug, Cavalier proliferation. In pyoderma associated with demodicosis, the
King Charles Spaniel, Dobermann, Great Dane, Argentin- immune defect involves cytotoxic T lymphocytes, helper T
ian Mastiff, Dogue de Bordeaux, Jack Russell Terrier, Af- lymphocytes and B lymphocytes. Both type 1 and type 2 help-
ghan Hound, Neapolitan Mastiff, Scottish Terrier, Shar Pei, er T lymphocytes seem to be involved in generalised demodi-
Shih Tzu, Rottweiler, Newfoundland, West Highland White cosis. A defect in interleukin 2 caused by dysfunction or inhi-
Terrier, Whippet and Yorkshire Terrier. This list is not ex- bition of type 1 helper T lymphocytes has been reported and
haustive. Interestingly, breeds like the Poodle that almost may be responsible for the condition becoming generalised.
never suffer from Generalised Juvenile-Onset Demodicosis In AOD, an underlying cause (e.g., long-term glucocor-
(GJOD) seem to be predisposed to Adult-Onset Demod- ticoids, chemotherapy and other iatrogenic factors; spon-
icosis (AOD) probably because of a breed susceptibility to taneous hyperadrenocorticism, lymphoma and other types
hyperadrenocorticism, a common predisposing factor in the of neoplasia; diabetes mellitus) has been identified in about
development of AOD. 75 % of cases. Any form of immunosuppression is likely to
promote the development of clinical demodicosis.
Pathogenesis
Pathogenesis is complex and not fully understood. In addition Clinical signs
to the mechanical and irritant effects of D. canis, antigenic ef- Skin lesions are highly pleomorphic and vary according to
fects and immunosuppression both contribute to pathogenic- breed and underlying factors. Two types of disease are rec-
ity. Substances released during moulting, metabolic products ognised: localised and generalised. Localised demodicosis,
and products from the degradation of epithelial cells can act whilst aesthetically undesirable, is normally benign and of-
as antigens. Immunosuppression may arise through the pro- ten self-resolving. Generalised demodicosis is defined as juve-
duction of immunosuppressive substances produced by the nile- or adult-onset and remains difficult to cure.
parasite itself. GJOD may be the result of a specific hereditary
defect in cellular (T lymphocytic) immunity to D. canis and Localised demodicosis
this host defect may allow Demodex to breed and produce • Nummular (coin-shaped) demodicosis involves a small
immunosuppressive substances that can be detected in the se- number of areas (<5) of variably circumscribed erythema,
rum of dogs with demodicosis. This leads to a vicious circle scaling and hair loss (Fig. 6). The face (eyelids and lips),
which enables the parasite to proliferate. Humoral immunity, limbs and occasionally the trunk are most likely to be in-
on the other hand, seems to be stimulated. Plasma cell num- volved (Figs. 7–10). Pruritus is usually absent. Lesions re-
bers increase in the spleen, lymph nodes and skin. IgG levels gress spontaneously within a few weeks in 90 % of cases.
increase 2.5-fold and the number of circulating immune com- Nummular demodicosis is common in short-coated breeds
plexes also increases significantly. such as the Staffordshire Bull Terrier, Boston Terrier,
Figure 6. Nummular alopecia due to Figure 7. Facial hyperkeratosis due to Figure 8. Localised facial demodicosis
demodicosis. demodicosis. lesion in a puppy.
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EXTERNAL PARASITOSES
to-ceruminous otitis with profuse brownish discharge. It seen in the Shar Pei, and this must be distinguished from
is usually found in association with demodicosis of other bacterial folliculitis, a common condition in this breed.
parts of the body. The authors have seen several cases in
Neapolitan Mastiffs.
Figure 9. Erythema due to demodicosis. Figure 12. Generalised alopecia due to Figure 13. Generalised demodicosis
Courtesy of Parasitology Unit, demodicosis. in a pug. Courtesy of Parasitology Unit,
Alfort Veterinary School. Alfort Veterinary School.
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Systemic signs
Systemic signs are inconsistent. In generalised demodicosis
with secondary bacterial infection, severe systemic signs may
arise, including anorexia, pyrexia (40–41 oC), lethargy, de- Figure 16. Comedones in a dog with demodicosis. Courtesy of
hydration and electrolyte disturbances. Septicaemia is not Parasitology Unit, Alfort Veterinary School.
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Diagnosis
Diagnosis is based on medical history, clinical signs and de-
tection of the parasite at different stages of its life cycle.
50 μm
• Deep skin scrapings (deep enough to see capillary
“ooze”) should be examined in chloral lactophenol, on Figure 17. Demodex canis adults from a skin scraping.
a microscope slide under a cover slip (Fig. 17). Micro-
scopic examination, at an initial magnification of ×40,
then at ×100, reveals large numbers of Demodex mites:
D. canis (eggs, larvae and adults). One Demodex mite is
not enough to diagnose demodicosis since about 50 %
of normal dogs with no clinical signs have Demodex
mites. An appropriate history, indicative clinical signs
EXTERNAL PARASITOSES
and the presence of Demodex mites in skin scrapings
are required to make the diagnosis (Fig. 18). Dogs with
pododemodicosis sometimes need to be anaesthetised to
obtain good skin scrapings. In cases of ulceration, crust-
ing and haemorrhagic bullae, skin scrapings taken from
ulcers and bullae respectively do not always reveal De-
modex mites. In fact, there are no Demodex in ulcers
since the mites live in pilosebaceous follicles; equally,
50 μm
mites in bullae are often lysed. In these cases, skin scrap-
ings should be taken from the edge of the ulcer or bulla Figure 18. Demodex canis adults.
or from other types of lesions.
• Hair plucks from affected areas, mounted in chloral lac-
tophenol, also reveal numerous mites in various stages of Pei demodicosis, perifollicular macrophagic granulomas,
the life cycle, arranged around the hair shaft. Taking hair made up of histiocytes and giant cells, and pyogranulomas
plucks is a very straightforward procedure and particular- arranged around fragments of Demodex are commonly
ly useful when dealing with cases with follicular casts but found. In subclinical demodicosis, early histopathologi-
it is not very sensitive. cal lesions include degeneration of the wall of the isthmus
• Histopathological examination of skin biopsies is useful around the sebaceous glands, associated with histiocytes
but not the principal means of diagnosing demodicosis. and giant cells. Lymphocytic mural folliculitis and per-
Demodex mites will often be clearly seen in hair follicles ifollicular granulomas are seen later in the absence of
and sebaceous glands, along with lymphocytic mural fol- Demodex.
liculitis and folliculitis lesions, furunculosis and cellulitis.
The main indications for biopsy are pododemodicosis, de- Prognosis
modicosis in the Shar Pei (the skin is thick in this breed Prognosis has improved considerably in recent years, thanks
because of dermal depots of mucin; hair follicles also to the development of systemically-acting products (macro-
penetrate further into the skin than in other breeds) and cyclic lactones and isoxazolines) effective against Demodex,
subclinical demodicosis. In pododemodicosis and Shar some of which are licenced for use in dogs.
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Control measures of larvae, eggs and ghost forms (clear, dead mites) allows
Excellent communication between vet and owner is essen- treatment efficacy to be assessed. Clinical resolution (Fig. 19)
tial, as treatment can be long and expensive. normally comes before parasitological cure and cases should
be reviewed every 2 months for a year after the parasitologi-
Indications cal cure. Relapse occurs in an average of 15 % of cases in the
Treatment for generalised demodicosis, with or without year following cessation of treatment.
secondary bacterial infection, pododemodicosis and aural
demodicosis, is essential. Localised forms of demodicosis re- Treatment of the underlying cause
solve spontaneously in 90 % of cases but they must be mon- In cases of AOD, it is important to treat the underlying cause
itored carefully to determine which cases may subsequently when identified. This may involve stopping glucocorticoid
need to be treated. therapy or treating hyperadrenocorticism.
Monitoring B
Monitoring is essential. A dog with demodicosis needs to be
cared for by its vet and its owner and it is to the vet’s respon-
sibility to motivate owners and give them good advice.
Treatment duration is often long, sometimes several
months.
Each case should be reviewed clinically and parasitolog-
ically every month. The number of Demodex mites can be
assessed semi-quantitatively at selected sites and the average
number of different life stages can be recorded, along with Figure 19. Demodicosis in a dog before treatment (A) and
counts of live and dead mites. The reduction in the number after (B). Courtesy of Parasitology Unit, Alfort Veterinary School.
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Feline demodicosis
General comments
Demodicosis is a rare skin condition in the cat and only one
species, Demodex cati (Hirst, 1919), had been described
in this host species until recently. However, another species
(Demodex gatoi) has been suggested in the last two decades.
This new species is clearly morphologically, biologically,
epidemiologically and molecularly different from D. cati.
The existence of a third morphologically distinct species
30 μm
has recently been proposed, following further observation.
However, this is still under debate and additional data are Figure 1. Adult Demodex sp. in a cat. Courtesy of Parasitology
required to confirm its existence. Unit, Alfort Veterinary School.
EXTERNAL PARASITOSES
total length and is finely tapered. The adult female is 220 µm
long and about 30 µm wide, and the adult male is small-
er (182 µm × 20 µm) (Fig. 2). The egg is lemon-shaped and
measures approximately 70 × 20 µm. D. cati mites live in the
hair follicles, especially in the eyelids, face, chin and neck.
There has been no specific work on the life cycle of D. cati
but it is assumed to be similar to D. canis in the dog or D.
brevis in humans. The eggs are laid in the follicular cavity,
hatch to produce larvae then protonymphs, and finally male
20 μm
and female adults.
Demodex gatoi was first observed in a cat in Louisiana, Figure 2. Adult Demodex cati. Skin scraping.
USA (Fig. 3). Since then, its presence has been reported in
other regions of the USA, and Europe. D. gatoi is smaller
than D. cati, mainly due to the fact that the mite’s opistho-
soma is much shorter (half the full length of the mite) and
blunt. The female and the male are about 100 and 90 µm
long, respectively. D. gatoi inhabits the superficial skin layer
(stratum corneum). Its life cycle has not been fully described
and this mite species has biological and epidemiological fea-
tures which are clearly different from D. cati. Molecular
techniques have also confirmed that D. cati and D. gatoi are
distinct species.
30 μm
Pathogenesis
There is a known relationship between mite proliferation
and the existence of potentially immunosuppressive systemic
diseases in D. cati-infested cats, but very little information is
available on the underlying immune mechanisms in the cat.
Some studies suggest that humoral immunity does not play a
major role. In humans, innate cutaneous immunity (Toll-like Figure 4. Feline demodicosis due to Demodex cati.
receptors, antimicrobial peptides, proteases) may play a key
role, but this has not been investigated in the cat.
The proliferation of D. gatoi causes a pruritic and poten-
tially contagious skin condition which does not seem to be
associated with a primary immunosuppressive disease. In-
terestingly, some infected cats do not exhibit clinical signs.
It has been suggested that affected cats may develop a hy-
persensitivity reaction to different mite allergens. Affected
cats over-groom and this behaviour eliminates many mites,
which may cause a diagnostic challenge. In contrast, infect-
ed asymptomatic cats may harbour very large numbers of
parasites.
Diagnosis
In addition to medical history and clinical examination,
D. cati infestations rely on detection of the mite in deep skin
scrapings. A trichogram may be useful in areas that are diffi-
cult to scrape, as the mite inhabits hair follicles. Detection of Figure 6. Feline demodicosis due to Demodex gatoi.
mite eggs is also diagnostic. Biopsies are rarely used but can
reveal mites in the hair follicles.
The mite population in cats infested with D. gatoi may be Control measures
reduced, and the aetiological diagnosis made challenging, by Relatively little information on evidence-based medicine
over-grooming. Several superficial skin scrapings should be is available as far as the treatment of feline demodicosis is
EXTERNAL PARASITOSES
taken from different body areas, especially those which are concerned. Classically, lime sulphur dips and amitraz were
difficult to groom. Cellophane tape may also be used and successfully used but lime sulphur is not widely available, es-
faecal flotation may reveal the ingested parasites. Identifica- pecially in Europe, and amitraz must be used with caution
tion is usually based on the typical morphology and superfi- in cats.
cial localisation of this mite.
Risk to humans
Demodex species are host specific and there is no zoonotic
risk associated with feline demodicosis.
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Trombiculosis
General comments
Trombiculosis is a non-infectious, non-contagious ectopar-
asitosis caused by various species of mites belonging to the
family Trombiculidae. It is common in cats, although many
other species of mammals (including dogs, horses, cattle,
sheep and humans), birds, reptiles and amphibians may be
infested by these mites. Trombiculids are unique in that only
the larval stage is parasitic because the nymphs and adults are
free-living (Fig. 1). Depending on the geographical location, Figure 1. Adult Trombicula.
the larvae are known as harvest mites, chiggers, red bugs
and scrub itch mites. They have also received very specific
names in other languages. These names are either related to
the mite’s colour, its seasonal activity or the clinical signs of
the condition it induces.
The most important species in veterinary medicine be-
long to the genus Trombicula which is subdivided into the
sub-genera Neotrombicula and Eutrombicula. The main
species are Neotrombicula (syn. Trombicula) autumnalis
in Europe, Eutrombicula alfreddugesi and Eutrombicu-
la splendens in the Americas, and Eutrombicula sarcina
50 μm
in Australasia. However, other species have also been de-
scribed and can be important locally. Consequently, trom- Figure 2. Neotrombicula autumnalis larva.
biculosis can be considered to be a condition of mammals
worldwide. Free-roaming cats are particularly exposed to
the mites as the larval stages are found outdoors in specific Biology
biotopes (meadows, lawns, heathlands, corn field, wood- The life cycle of N. autumnalis takes 2 to 12 months. The
ed and marshy areas, etc.) depending on the mite species. larvae, which are the only parasitic stage, can essentially
Mite distribution in the environment is known to be quite be seen in summer and autumn so trombiculosis mainly
patchy, so noticeable differences in prevalence can be seen, occurs during those periods in temperate regions of north
even within fairly limited areas. The factors responsible for hemisphere. After the larval stage hatches in the environ-
this irregular distribution are largely unknown. ment, it climbs onto different plants, questing for a suita-
Only the larval stage has been described, as the nymphs ble host. After attachment to the skin, the larvae feed on
and adults are never found on the animal. The six-legged tissues (Figs. 3–5). They pierce the skin with their mouth
N. autumnalis larva is very hairy, orange in colour and is parts and inject histolytic saliva, so a mixture of blood and
250–750 µm long, depending on the stage of repletion digested dermal tissues is ingested. This ingestion takes
(Fig. 2). The dorsal shield or scutum is roughly pentangular place through a canal known as stylostome, formed follow-
and the chelicerae are flanked by stout, five-segmented palps. ing the hardening of a specific salivary secretion; feeding
The larvae of E. alfreddugesi are very similar to those of behaviour reminiscent of ticks. Larvae are often attached in
N. autumnalis and they measure 150–600 µm in length and clusters which make their detection easier, as they appear as
have a rectangular scutum. E. splendens is very similar to an “orange powder” in preferred sites (Fig. 6). Engorgement
E. alfreddugesi, and is often sympatric. usually takes 24– 72 hours but may take up to 10 days. The
larvae drop off into the environment after completing their
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CONTENTS Acarioses 279
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100 μm
Figure 3. Trombicula mites attached to the skin. Courtesy of Figure 4. Attached Trombicula mites.
Parasitology Unit, Alfort Veterinary School.
EXTERNAL PARASITOSES
Figure 5. Trombiculosis in a dog. Figure 6. Several Trombicula mites attached.
meal. Life cycles of the other trombiculid species are very Epidemiology
similar, but may differ in length according to local climatic The larval stage is parasitic on a wide range of mammals
conditions. such as cats, dogs, rodents, rabbits, humans and birds and
In Europe, several generations of trombiculids are pro- larvae will infest almost any animal entering their habitat,
duced between March and October and the risk of infesta- for example, horses being exercised, which they often attack
tion persists until autumn. The larvae feed for 3–4 days be- on the legs. This mite is typically active in late summer and
fore leaving the host to moult into nymphs, a process which early autumn. Larval mites climb onto plants or other van-
takes 2–3 days. The immobile stage 1 nymph develops into tage points so that they can swarm onto a host when it comes
stage 2 over 4– 5 days. The mobile second nymph stage feeds close. Adult and nymphal mites have a free-living, predatory
on small soil mites before moulting into a stage 3 nymph over life cycle, feeding on other arthropods.
3– 4 days, and then into the adult in a further 3–4 days. Infestation is exclusively from the external environment
Adult trombiculids mate and the females lay eggs after 8–10 (gardens, undergrowth, hedges and copses) in summer and
days. They live for several weeks in the environment in the autumn, although it is not uncommon to see infestations in
summer, before entering a resting stage at the end of autumn. the spring, or even in winter, when weather conditions are
They then become active again the following spring. Eggs favourable. There is no direct transmission. Trombiculosis is
hatch rapidly into hungry young larvae, the only parasitic not a true zoonosis, as people are infested directly from the
stage, which actively seek out hosts on which to feed. They environment. Severe, often persistent pruritus, erythema and
can fast for several months if necessary. papules are seen on the limbs and trunk of infested people.
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EXTERNAL PARASITOSES
(Fig. 1). Nymphs and eggs can also be found in the environ- dorsal lumbosacral region, tail), medial and lateral limbs and
ment. Only the larvae are pathogenic and their preferred occasionally over the whole body (Fig. 2). They are pruritic
hosts are foxes, and possibly small mammals. The dog is an and often very painful, causing extreme skin hyperaesthesia
accidental host which, when bitten, displays a severe cystic and aggressive behaviour. Excoriations and thick crusts may
reaction at the point of attachment. be seen in chronic cases and systemic signs (e.g., lethargy and
Infestation mainly occurs in areas where these para- anorexia) are sometimes seen in severe, painful cases.
sites abound, for example near fox earths or badger setts.
Straelensiosis is consequently seen more commonly in hunt- Diagnosis
ing dogs, notably terriers (e.g., Fox Terriers, Dachshunds and Diagnosis is based on medical history, clinical signs and de-
Jack Russell Terriers). Seasonal variation is not well under- tection of parasitic larvae.
stood and no age or sex predisposition has been reported. Superficial skin scrapings are often unrewarding.
The affected area should first be clipped under general
anaesthesia. Very deep skin scrapings and papular incisions
should then reveal the larvae. Selected papules should be raised
and effectively scalped from underneath. Scrapings should be
examined microscopically in chloral lactophenol, initially
under ×40 magnification and subsequently under ×100 and
×250, with low to moderate lighting. U‑shaped parasitic cysts
with thick translucent walls can be seen (Figs. 3–5). The par-
asite is the rostrum located towards the base of the U.
The parasite can be identified by fine dissection of pap-
ules, preserved in 70 % alcohol, under a binocular dissecting
microscope.
Histopathology of skin biopsies is indicative (Fig. 6). Af-
fected hair follicles have a very dilated infundibulum con-
Figure 1. Fox earth or badge sett, source of Straelensia mites for taining a parasitic cyst made up of the shell of the thick
hunting dogs. basophilic cyst and the parasite. The parasite has a variably
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calcified, striated external cuticle, a rostrum, a histosiphon Differential diagnosis includes sarcoptic mange, demodi-
(which pierces the end of the U-shaped cocoon) and fine silky cosis, trombiculosis, calcinosis cutis, deep mycoses and cer-
strands. A neutrophil-rich liquid can be seen in the dermis at tain multicentric tumours.
the end of the histosiphon. The thick, double-layered cyst is
made up of vestiges of the external root sheath which exhib- Prognosis and control measures
its severe trichilemmal keratinisation associated with severe The prognosis is very guarded. There is no licensed treatment
pseudo-epitheliomatous hyperplasia. The adjacent dermis is for this condition and therapeutic response is uncertain. Long-
rich in blood vessels and often mucinous. A severe inflamma- term application of amitraz has been proposed but results seem
tory reaction, dominated by a variable number of eosinophils disappointing. Isoxazolines may be alternative treatments.
and plasma cells may be present, depending on the chronicity Prevention seems to be difficult and involves limiting con-
of the lesions. Evidence of eliminated cysts or pyogranuloma- tact between dogs and the parasite’s usual hosts (e.g., foxes)
tous reactions may also be seen. in high risk areas during the hunting season.
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100 μm
Figure 3. Straelensia nodule extracted from the skin. Figure 5. Straelensia mite in a cyst.
EXTERNAL PARASITOSES
100 μm 100 μm
Lynxacarosis parasite typically exhibits the same life cycle as other listro-
phorids. The large and elongated eggs (about 200 μm long) are
glued to the hairs distally (Fig. 2). They hatch into a six-legged
General comments larva then an eight-legged nymph, which moults into the adult
Lynxacarosis is caused by the development of the fur mite stage. Details of the life cycle have not been studied.
Lynxacarus radovskyi on the skin surface and coat in the Mite transmission is thought to occur mainly by direct
cat. The parasite was first described in Hawaii (1974) and contact, and the condition appears to be contagious. How-
Puerto Rico (1977) and it seems to be quite common in trop- ever, indirect contamination through fomites also seems
ical or warm regions. It has been observed in southern parts possible.
of the USA (Texas, Florida), Australia, New Zealand, New Human contamination is unlikely, although there is one
Caledonia, French Guyana, Caribbean Fiji, Malaysia, the report of a papular rash on the arms of the owner of a highly
Philippines and South America (several regions in Brazil). infested cat that cleared when the cat was treated.
Distribution is probably much wider. Five species of Lynx-
acarus are already present in temperate countries, infesting Clinical signs
wild carnivores (e.g., L. mustelae on mustelids). Many cases remain asymptomatic. Lynxacarus mites are
Lynxacarus radovskyi (Tenorio, 1974) is a Listrophorida most commonly found on the tail and head, and in the per-
mite. Adult Lynxacarus sp. measure about 500 μm long, are ineal/perianal area. Mites can be found over entire body in
elongated and laterally compressed, and the first third of the heavy infestations. Distribution on the body is variable, and
body is sclerotised (Fig. 1). The legs are relatively short and ter- often generalised in long-haired cats.
minate in suckers, adapted to cling to the hairs. The different The most common and indicative presentation is a dan-
species of Lynxacarus are morphologically very close and the druff-like condition, with a dull and dry coat associated with
the mites. This gives a “peppered” appearance due to the The pruritus induced by the parasite is variable; usually
whitish colour of the mites, eggs and thin scales on the hairs. mild in animals with light infestation, but possibly very in-
Evidence of pruritus, alopecia and excoriations can be tense in heavily infested individuals. Severe cases can be as-
seen in some cats. Diffuse alopecia or “mangy” patches can sociated with feline miliary dermatitis
also be seen. Alopecia is occasionally visible on the dorsal Other signs are probably caused by the excessive groom-
and lateral parts of the hind limbs, with evidence of self-in- ing induced by the parasite: gingivitis, gastrointestinal distur-
duced injury. bances, rectal irritation or prolapses, and hairballs. Infested
cats may also present with weight loss, anorexia, restlessness,
and fever.
Diagnosis
The parasites can be detected by microscopic observation of
samples obtained by combing, trichoscopy or the adhesive
tape test. Different stages of mites and/or their eggs attached
to the hair shafts can be seen. Diagnosis of heavy infestations
is easy, but subclinical infestation is likely to be difficult to
detect.
EXTERNAL PARASITOSES
Control measures
A number of treatments have been shown to be effective and
the parasite seems to be sensitive to all acaricides tested.
Figure 2. Lynxacarus eggs.
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Dermanyssus
infestation
General comments
Dermanyssus gallinae (De Geer, 1778) (Dermanyssoidea) is The mite’s life cycle has been extensively studied because
distributed worldwide and mainly affects birds. Infestation of its significant economic impact on the poultry industry.
with D. gallinae is quite common in mammals and occurs The mites live in the poultry housing, especially in egg-laying
when animals or humans associate with infested poultry or hen houses, close to the avian hosts. The adult mites feed on
pigeons. blood at night and most of them return to the cracks and
crevices after leaving their hosts. Up to seven eggs are laid
Biology at a time and these eggs hatch after 2 to 3 days, releasing
D. gallinae is known as the poultry red mite because it the six-legged larvae, which do not feed. The larvae moult
turns red after feeding on blood. Unfed mites are whitish into the protonymph stage which feeds on blood (Fig. 1). The
or greyish. The fully engorged female mite is oval, around 1 final moult takes place after another 2– 3 days, producing
mm long and is easily seen with the naked eye. All other de- the adults (Fig. 2). The entire life cycle can be completed in
velopmental stages are smaller. Besides its colour, other dis- 7 days under optimum conditions and the mites can survive
tinctive morphological characters are obvious after clearing for 5 months without feeding.
and microscopic examination: very prominent dorsal shield Only mammals which live close to poultry, ornamental
with a truncated posterior end, prominent anal plate on the birds and pigeons are affected. Humans can be bitten from
posterior ventral surface, anus located on the posterior as- the same sources, and present with pruritic papular dermati-
pect of this plate and a pair of long, whip-like chelicerae. tis on the hands, forearms and legs.
100 μm
EXTERNAL PARASITOSES
tiellosis, trombiculosis, louse infestation, flea allergy derma-
titis and atopic dermatitis.
Prognosis is usually favourable.
50 μm
PARASITOLOGICAL
DIAGNOSIS
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General principles
Parasites, especially intestinal worms and ectoparasites, are Trichuris antigens can also be detected in faecal matter
often thought to be “easy” to treat, without any diagnosis by (coproantigens). Not only is the infestation diagnosed, but
a vet. This common view probably explains why infestation the presence of antigens indicates the viable and infectious
rate is underestimated and treatment often fails. nature of the parasite. Developments in molecular biolo-
gy over the past few years have raised the possibility that
The diagnosis of parasitic diseases is based primarily on PCR tests could be developed to identify parasite DNA,
an epidemiological and clinical suspicion. The climate, the whether it be circulating, in tissues, or excreted in faeces.
period during which clinical signs appear, the animal’s age • Indirect tests seek evidence of a host response to parasitic
and lifestyle, along with the expression of indicative clinical infection or infestation and can be specific (antibody de-
signs, can all raise the suspicion of a parasitic infection. Ex- tection) or non-specific (modification of blood chemistry,
perimental confirmation is, however, necessary to identify complete blood count [CBC] with noticeable eosinophilia
the pathogenic agent(s). The laboratory diagnosis of parasitic during parasite migrations).
diseases employs both direct and indirect techniques:
• Direct tests seek evidence of the parasite, or a fragment/ In this chapter, we will focus on parasitological diagnosis
element of the parasite (e.g., the whole parasite itself, eggs, based on direct detection of the parasite (or fragment of the
DNA, etc.). New immunological tests have been devel- parasite) in a range of samples, for which some techniques
oped that look for circulating or eliminated parasite an- have been developed, which are specific to parasitology.
tigens rather than antibodies. The most well-known test These are the most common methods because they are easy
is undoubtedly the ELISA test for circulating Dirofilaria to perform, inexpensive and offer a rapid definitive diagno-
immitis (heartworm) antigens in dogs. Excreted Giardia, sis. However, they do require experienced users and may
Echinococcus and recently Toxocara, Ancylostoma and have a low sensitivity.
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Coproscopy*
PARASITOLOGICAL DIAGNOSIS
method of choice. Even ectoparasite eggs (e.g., mites and lice) Particular care should be taken in handling FM as it can
may be licked from the skin, swallowed and found in fae- contain zoonotic agents, so good laboratory hygiene (e.g., the
cal samples. Pseudoparasites (pollens, free-living nematodes, use of disposable gloves) is imperative.
maggots, etc.) can also be observed in the faecal preparation, Veterinary diagnosticians do not usually have the oppor-
which may confuse the untrained observer. An accurate tunity to collect faecal samples and must rely on samples
diagnosis of parasitism is based primarily on the diagnos- brought in by clients. Regardless of who obtains them, it is
tician’s awareness of the parasites prevalent in a particular important to have fresh faeces to work with. Faeces collect-
region. However, with globalization and the movement of ed from litter boxes, gardens, kennel floors, etc. may be old
animals and humans, “exotic” and “unusual” parasites may and dry, so parasite eggs may have embryonated or larvat-
be brought to the attention of veterinary practitioners. There- ed, oocysts may have sporulated, or pseudoparasites may be
fore, when parasite-like material (pseudoparasite) is found in present. If fresh faeces cannot be submitted promptly, clients
a faecal sample, correct identification is required by qualified should be advised to refrigerate the sample for 1–3 days. Fae-
and accredited parasitologists. ces should be submitted in a sealed glass or plastic container,
Before performing any of the coproscopic procedures de- clearly marked with the time and date of collection, species
scribed in the following sections, some important rules for of animal, animal’s name, owner’s name, and any other in-
technician safety and the accurate diagnosis of internal para- formation relevant to the case.
sites should be considered. These rules can be summarised as Coprological analysis can be performed on fresh fae-
follows: I) handle faecal samples carefully; II) clean up imme- cal samples or samples stored at 4° C for 1–3 days, and/or
diately after a coproscopic test is performed; III) keep good preserved (fixed) faecal samples. The sample should not be
records of any observations on the appearance of the faecal frozen because freezing and other preservation methods will
sample and the presence of parasites. alter the results, but fresh FM should be submitted to the
*This chapter is inspired from Chapter 1–10 Coproscopy diagnosis. Laura Rinaldi et al., published in Parasitoses and Vector Borne Diseases of Cats, Ed. Merial, 2015.
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laboratory packed with cold packs. Buffered formalin (5 % and double pores for Dipylidium). Larval stages of arthro-
or 10 %) or sodium acetate-acetic acid-formalin (SAF) may pods (e.g., flies) may also be found. Parasites should be iden-
be used to preserve samples if required. The use of preserva- tified morphometrically (using keys in the literature) or by
tives/fixatives may incur additional shipping costs as many of using appropriate molecular techniques.
these fluids are considered to be hazardous materials in some After gross examination is completed, the faeces should
countries, and require very specific packaging and shipping be examined by copromicroscopy, which can either be
conditions. However, fixatives have the added benefit of in- qualitative; only demonstrating the presence/absence of a
activating any other infectious organisms that may be pres- particular PE (eggs, larvae, cysts, oocysts), or quantitative;
ent. Special fixatives, such as polyvinyl alcohol (PVA), are providing quantification by faecal egg count (FEC). The FEC
required to preserve protozoan trophozoites. The sample is is expressed as eggs/larvae/oocysts/cysts per gram of faeces
best preserved by mixing faeces and fixative in a 1:4 ratio; (EPG/LPG/OPG/CPG).
that is, 1 part faeces with 3 parts fixative (formalin 5 % or
10 %, or SAF). The faeces must be completely homogenised Microscopic techniques
with the fixative (Table 1) as soon as they are mixed. Many copromicroscopic techniques have been developed
In carnivores/omnivores, the type of diet can produce since copromicroscopy was first used by C.J. Davaine in
undesirable residues in the faeces which may influence the 1857, each with its own advantages and limitations. Al-
clarity of the resulting preparation, due to the flotation of though these techniques can be quantitative (FEC), di-
small and/or large particles of debris. It is important to avoid agnosis in dogs and cats is often only made qualitatively
feeding fatty foods to dogs and cats before a sample is col- (presence or absence of a parasitic element). Coccidia are
lected for coproscopy, where possible. Either ether or ethyl an exception and are often expressed in a semi-quantitative
acetate can be used as a fat-remover, but the former is tox- manner (e.g., 1+, 2+ and so on, correlating with the num-
ic to humans and dangerous for the environment, and the bers seen per 10× field).
latter is flammable and irritant to humans. Hemo-De is an Techniques for the examination of faeces for helminth
alternative to ethyl acetate and is generally regarded as a safe eggs/larvae and protozoan cysts/oocysts may vary from
compound to remove fats from faeces. a simple direct smear to more complex methods involving
concentration of PEs by either flotation or sedimentation.
Macroscopic examination Flotation in centrifuge can also be performed, and novel
Coprological diagnosis must start with a macroscopic ex- multivalent devices, such as FLOTAC and its derivatives Mi-
amination of the faeces. Gross faecal characteristics, such ni-FLOTAC and Fill-FLOTAC, have been recently designed.
as consistency (watery, soft, hard), age of sample (parasito- Although the direct smear was used for many parasites
logical analysis may be wrong in old samples), colour and for many years, it has one great disadvantage and that is
presence of blood or mucus in the sample should be noted. the small amount of faeces used, which often gives rise to
Alongside these observations, the faeces sample should be false-negative results. To overcome this problem, some meth-
grossly examined for entire or part parasites, such as intact ods have been developed to concentrate parasitic material
roundworms (Toxocara, Toxascaris) and/or of tapeworms from a larger faecal sample into a smaller volume, which may
proglottids (e.g., Dipylidium caninum and Taenia spp.). Pro- then be examined microscopically. Concentration methods,
glottids can be motile and are identified by the number of which have greater analytical sensitivity than smears, include
genital pores on each segment (e.g., single pore for Taenia flotation and sedimentation, and the modified Baermann
Fixative Composition
SAF C2H3NaO2 1.5 g, C2H4O2 2 mL, CH2O (40 %) 4 mL, H2O 92 mL
technique. These methods are designed to separate the vari- The main techniques used for copromicroscopic examina-
ous parasitic stages from FM. Faecal sedimentation concen- tion in cats are described below.
trates both faeces and eggs at the bottom of a liquid medium,
usually tap water. In contrast, the principle of faecal flotation Direct smear
is based on the ability of a flotation solution (FS) to allow less The simplest method of microscopic faecal examination
dense material (including PEs) to rise to the surface. Finally, for parasites is the direct smear (Fig. 1), which consists of
the modified Baermann technique is used to recover nema- placing a small amount of faeces directly on a microscope
tode larvae, many of which are unable to swim against grav- slide. Some practitioners make direct smears using only the
ity. There are many refinements and modifications of these amount of faeces that clings to a rectal thermometer after
techniques, but the same simple principle underlies them all. taking the cat’s temperature.
Copromicroscopic examination for parasite eggs/larvae/ Several drops of saline solution or water are placed on the
oocysts/cysts is a fundamental part of the daily routine for slide with an equal amount of faeces. The solution and fae-
most veterinary practices. Despite their limitations, direct ces are then mixed together with a wooden applicator (or a
smears are useful to detect motile protozoa (e.g., Tritrich- pipette) until the solution is homogenous, and the solution
omonas or Giardia trophozoites), and sedimentation tech- is smeared over the slide in a thin film which should be thin
niques are useful for recovering heavy eggs (e.g., from Physa- enough to read print through. Finally, any large pieces of
loptera spp.) or operculated eggs (e.g., fluke eggs) that do not faeces are removed and a coverslip is placed over the smear
float consistently or are distorted by the effect of FSs. Flota- which is examined under low microscopic power (×100).
tion techniques are most frequently used to recover parasite Faecal smears can also be air-dried and stained for iden-
eggs, oocysts and cysts (see following sections). tification of intestinal protozoa (e.g., trichrome stain for
Manuals of veterinary parasitology diagnostic are avail- Giardia and carbol-fuchsin, Giemsa or Ziehl-Neelsen for
able and cover multiple animal species and techniques. Cryptosporidium).
PARASITOLOGICAL DIAGNOSIS
1 Homogenise the faecal sample
2 Transfer a drop of tap water or saline solution onto
the slide with an equal amount of faeces
3 Mix the solution and faeces together with a wooden
applicator until the solution is homogenous
4 Cover with the coverslip
5 Read
1 2 3 4 5
Flotation
Flotation techniques are the most common methods used to
recover PEs. These procedures are based on differences in
the specific gravity (s.g.) of parasite eggs, larvae, oocysts and
cysts, faecal debris and FS (Fig. 2).
The average s.g. of many nematode eggs, including dog
and cat ascarids, is between 1.05 and 1.24. The s.g. of the FS
must be greater than that of the eggs to allow parasite eggs
to float. Most of the FSs used in coproscopy (Table 2) are
saturated and made by adding a measured amount of salt
or sugar to a specific amount of water to produce a solution
with the desired s.g. The salt or sugar (or a combination of
both, depending on the FS) should be dissolved in the water Figure 2. Flotation technique.
Specific gravity
Flotation solution Composition
at saturation
Sucrose and formaldehyde C12H22O11 454 g, CH2O solution (40 %) 6 mL, H2O 355 mL 1.200
Sodium nitrate NaNO3 250 g, Na2O3S2 ∙ 5 H2O 300 g, made up to 1,000 mL 1.300
Sodium chloride and zinc chloride NaCl 210 g, ZnCl2 220 g, H2O made up to 1,000 mL 1.350
Sucrose and sodium nitrate C12H22O11 540 g, NaNO3 360 g, H2O made up to to 1,000 mL 1.350
The FSs normally used for nematode and cestode eggs are It is also important to note that the type of diet can produce
mainly based on sodium chloride, whereas saturated solu- undesirable residues and fats in the faeces which may influ-
tions of zinc chloride or zinc sulphate are widely used for ence the clarity of reading, due to the flotation of small and/
trematode eggs. Ideally, all PEs would float and still main- or large particles of debris.
tain their morphological integrity, and faecal debris would
sink, in the chosen FS. The choice of FS is important and, in Simple (gravitational) faecal flotation
the authors’ opinion, it is not given enough attention by the One method is as follows: a small quantity of the faecal sam-
scientific community, despite the substantial effect that the ple (about 3 g) is placed in a 90 to 150 ml waxed paper cup
FS can have on the diagnostic performance of any flotation then about 20 ml of FS are added. An emulsion is made by
technique. Only the s.g. or density of the FS is usually report- thoroughly mixing the solution with the faeces using a tongue
ed in manuals of diagnostic or in peer-reviewed literature. depressor, until a faecal slurry is formed. This mixture of fae-
The efficiency of a FS in terms of the capacity to bring PEs to ces and FS is filtered through a double layer of cheesecloth
flotation is commonly believed to increase as the s.g. of the or gauze, or a tea strainer could also be used. The mixture
FS increases, but PEs should not be considered to be merely is poured into a shell vial which is then filled to the top and
“inert elements”. Instead, interactions between the elements slightly overfilled, so that a slight convex meniscus forms at
within a floating faecal suspension (e.g., FS components, PE, the lip of the vial. If there is not enough fluid in the cup to
fixative, ether and residues of the host’s diet) might be com- fill the shell vial, a small amount of fresh flotation medium
plex. As a rule of thumb: may be added. Finally, a glass coverslip is placed gently on top
• Different FSs with the same s.g. do not produce the same of the fluid and allowed to sit, undisturbed, for 10–20 min-
results with respect to the same PE, even when the same utes. The coverslip is then removed carefully and immediately
technique is used. placed on the microscope slide for examination (Fig. 3).
• An FS which might be highly effective with respect to a A plethora of flotation techniques, of varying degrees
particular PE and a particular technique, produces differ- of difficulty (simple to complex), are described in the text-
ent results if the technique is changed. books, diagnostic manuals and scientific literature, and there
PARASITOLOGICAL DIAGNOSIS
• An FS which is effective with respect to a particular PE and are several kits, complete with specific instructions, available
a particular technique, using a fresh faecal sample, pro- commercially. These kits consist of prepared FS, disposable
duces different results if the method of faecal preservation plastic vials, and strainers.
changes (e.g., frozen, preserved in formalin or SAF, or in
other fixatives; see discussion above). Advantages
• An FS which is effective with respect to a particular PE Inexpensive and easy to perform.
and a particular technique, produces different results if the
host’s diet changes. Disadvantages
• It follows that each PE must be considered independent- The slide must be examined promptly, otherwise, osmotic
ly with respect to the FS, the technique and the method distortion may render the PEs difficult to identify, or crys-
of faecal preservation used when copromicroscopic flota- tallisation of the medium may obscure the microscopic field.
tion is employed. What is known for a specific PE can- Trematode eggs may be distorted because of the hypertonic
not be readily translated to a “similar” PE, or to the same effect exerted by the FS, as FSs have a very high s.g.
PE when the technique or the faecal preservation method
changes.
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1 2 3 4
5 6 7
8 9 10
1 Homogenise the faecal sample 6 Transfer the faecal suspension into the tube; fill to the top and
2 Take a small quantity of faeces (about 3 g) slightly overfill it so that a meniscus forms above the lip of the tube
5 Filter through a wire mesh (aperture = 250 µm) 9 Transfer the coverslip onto the glass slide
10 Read
PARASITOLOGICAL DIAGNOSIS
1 2 3 4
1 2 3 4
5 6 7 8
PARASITOLOGICAL DIAGNOSIS
9 10 11 12 13
14 15
1 Homogenise the faecal sample 9 Fill the tube approximately half full with FS
2 Weigh 3–5 g of fresh faeces 10 Resuspend the pellet using a wooden stick
3 Add tap water to 25 mL 11 Top the tube up with FS until a meniscus is formed
4 Homogenise thoroughly with a stick 12 Place a 22 × 22 mm coverslip over the top of the tube
5 Filter through a wire mesh (aperture = 250 µm) 13 Centrifuge at 150 × g for 10 min
6 Transfer the faecal suspension into the tube 14 Transfer the coverslip onto the slide
7 Centrifuge at 150 × g for 10 min 15 Read
8 Discard the supernatant
FLOTAC techniques
These techniques use a FLOTAC apparatus and are based The tubes are centrifuged for 3 min at 170 × g at room tem-
on the centrifugal flotation of a faecal suspension and subse- perature, then each supernatant is discarded, leaving only
quent translation (cutting) of the apical portion of the float- the sediment (pellets) in the tubes. Each tube is then filled
ing suspension. with the chosen FS to the previous 6 mL level. The suspen-
Three methods can be used with the FLOTAC device (ba- sions are homogenised thoroughly (before and between the
sic, dual and double), and these are variants of a single tech- fillings) and the two flotation chambers of the FLOTAC ap-
nique, but with different applications (Fig. 7). paratus are filled. The FLOTAC apparatus is then closed and
The FLOTAC basic technique uses a single FS. This tech- centrifuged for 5 min at 120 × g at room temperature. After
nique is recommended for use with faecal samples containing centrifugation, simultaneous 45° rotation of the apparatus’s
a low or very low number of PEs from a single parasite spe- translation disc and reading disc cuts (removal) the top por-
cies (natural or experimental mono-infection), or with fae- tion of the suspension in both chambers (= translation) and
cal samples containing a low or very low number of various the reading disc is examined under a microscope (Fig. 8).
types of PEs, which all have the same behaviour with respect
to the FS used. With the FLOTAC basic technique, the ref- Advantages
erence units are the two flotation chambers (total volume 10 The large amount of faecal suspension examined gives few-
mL; corresponding to 1 g of faeces). The analytic sensitivity er false-negative results, so it is particularly suitable for sit-
of the FLOTAC basic technique is 1 PE per gram. uations of low parasite elements. Results obtained with the
The FLOTAC dual technique is based on the use of two FLOTAC apparatus are easy to read.
different FSs that have complementary s.g. and are used in
parallel on the same faecal sample. This technique is indi- Disadvantages
cated for epidemiological surveys and routine diagnosis, to A certain level of laboratory infrastructure (e.g., large vol-
screen for a wide range of PEs with different characteristics ume centrifuge or benchtop centrifuge with rotor for micro-
in relation to the FS. With the FLOTAC dual technique, the titre plates) is required for FLOTAC techniques, which is of-
reference unit is the single flotation chamber (volume 5 mL; ten not available in resource-constrained settings. It is more
corresponding to 0.5 g of faeces) and the analytical sensitivi- time-consuming than some other flotation techniques.
ty of this technique is 2 PEs per gram.
The FLOTAC double technique is based on the simulta-
neous examination of two different faecal samples from two
different hosts using a single FLOTAC apparatus. With this
technique, the two faecal samples are assigned to their own
single flotation chamber, using the same FS, and the refer-
ence unit for this technique is the single flotation chamber
(volume 5 mL; corresponding to 0.5 g of faeces). The ana-
lytic sensitivity of the FLOTAC double technique is 2 PEs
per gram.
The procedure is as follow: each faecal sample is diluted in
tap water (dilution ratio 1:10). After homogenisation (the use
of a hand blender is recommended), the resulting suspension
is filtered through a wire mesh (aperture = 250 μm), then Figure 7. Devices in the “FLOTAC family”: Mini-FLOTAC,
6 mL from the filtered suspensionis placed into conical tubes. FLOTAC and Fill-FLOTAC.
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CONTENTS Coproscopy 301
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1 2 3 4
5 6 7 8
PARASITOLOGICAL DIAGNOSIS
9 10 11 12
13 14
4 Homogenise the suspension thoroughly 10 Resuspend the pellet using a wooden stick
5 Filter through a wire mesh (aperture = 250 µm) 11 Fill the two FLOTAC flotation chambers
6 Transfer two 6 mL aliquots of the filtered suspension into 12 Centrifuge at 120 × g for 5 min
two conical tubes 13 Translate
7 Centrifuge at 170 × g for 3 min 14 Read
Mini-FLOTAC technique
Mini-FLOTAC was developed to overcome the issue of Advantages
limited facilities by eliminating the centrifugation step. Mi- It operates in a closed system and can be performed on fixed
ni-FLOTAC is recommended for use in combination with faecal samples. It can be used in place of the FLOTAC tech-
Fill-FLOTAC, a disposable sampling kit, which consists of niques in laboratories where the centrifugation step cannot
a container, a collector and a filter. Fill-FLOTAC facilitates be performed.
the first four steps of the Mini-FLOTAC technique, i.e., sam- Mini-FLOTAC has been already validated in veterinary
ple collection and weighing, homogenisation, filtration and parasitology for the diagnosis of helminths (e.g., ascarids,
filling. hookworms, trichurids, gastrointestinal nematodes) in pets
Briefly, 2 g of fresh faeces are weighed in a container and and livestock.
FS to 20 mL are then added (dilution ratio = 1:10). The sus-
pension is homogenised thoroughly then filtered through a Disadvantages
wire mesh (aperture = 250 µm). The suspension is mixed Minimum detection limit of 5 EPG may not be appropriate
thoroughly and the two chambers of the Mini-FLOTAC in all situations.
filled (these four steps can be performed in the Fill-FLO-
TAC). The Mini-FLOTAC is left to stand for 10 minutes,
then the top parts of the Mini-FLOTAC’s flotation chambers
are translated and read under the microscope (Fig. 9). The
analytic sensitivity of the Mini-FLOTAC basic technique is
5 PEs per gram.
1 2 3 4
5 6 7 8
PARASITOLOGICAL DIAGNOSIS
1 Homogenise the faecal sample 5 Fill the Mini-FLOTAC using the filling holes until the flotation chambers
2 Weigh 2 g of fresh faeces are filled with the faecal suspension and a slight meniscus is formed
Faecal sedimentation
A sedimentation procedure is used to isolate eggs or cysts Advantages
whose s.g. is too high to float readily in common FSs or The benefit of the sedimentation procedure is to detect eggs
which would be severely distorted by FS (Fig. 10). One com- that do not easily float if they are too heavy or too delicate
mon method is as follows: to be concentrated by flotation, for example, so this proce-
100 mL of water are mixed with 10 g of faeces and placed dure is mainly used for trematodes and some nematode (e.g.,
in a beaker or other container. The mixture of faeces and Physaloptera spp.) eggs. Large volumes of faeces can also be
water is strained through a double layer of cheesecloth or evaluated.
gauze, or a tea strainer into a container. It is advisable to use
a 250 mL conical container (height = 18 cm) or a 500 mL Disadvantages
beaker (height = 12 cm). The mixture is allowed to sit for It is more time-consuming to perform.
20–30 minutes to 1 hour and then the supernatant is decant-
ed. Water is then added to the previous level, the sediment
is resuspended, and the sample allowed to rest again from
20–30 minutes to 1 hour. The supernatant is decanted again,
and the sediment is removed and placed into a Petri dish for
evaluation. Alternatively, a few drops of the remaining mix-
ture can be placed on a microscope slide, a coverslip added
and the preparation examined (Fig. 11).
1 Homogenise the faecal sample Repeat steps 6–7–8 until the suspension is clear
2 Weigh 3 g of fresh faeces
9 Remove 90 % of the supernatant
3 Add 100 mL of water
10 Stir the remaining mixture
4 Homogenise thoroughly with a stick
11 Place the entire amount in the Petri dish or place a few drops
5 Filter through a wire mesh (aperture = 250 µm)
on the glass slide
6 Allow the mixture to rest for 1 hour
12 Read
7 Remove 70 % of the supernatant
8 Refill the beaker with fresh water
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CONTENTS Coproscopy 305
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1 2 3 4
5 6 7
PARASITOLOGICAL DIAGNOSIS
8 9 10
11 12
Telemann technique
The Telemann technique concentrates eggs, cysts and lar- so that the larvae can migrate out and be collected. One
vae in samples with high fat concentrations. Briefly, about method is as follows:
1 gram of faeces is put in a beaker with 5 mL hydrochloric Place warm water (at approximately 25 °C) into a glass
acid (15 %) and homogenised. The faecal suspension is fil- funnel with a stopcock or a clamp on a rubber hose over the
tered through a double layer of gauze and transferred into a end of the funnel. 5 or more grams of faeces are wrapped in
15 mL centrifuge tube. An equal amount of ether is added two layers of gauze and placed in the water in the funnel. A
and the tube is plugged then shaken vigorously and cen- support, such as a screen, tea strainer or sieve, is placed in
trifuged at 170 × g for 1 minute. Four layers are formed the funnel, and the gauze-wrapped faeces are placed on it.
by the centrifugation: 1) ether; 2) plug of faecal debris; 3) The sample is allowed to rest for at least 8 hours, or pref-
acid; 4) sediment containing the PEs. The tube is placed erably overnight. The clamp is then released and the first
in a horizontal position and the upper layers are removed, 10 mL of fluid collected in a centrifuge tube. This is spun
leaving only the sediment in the tube. The walls of the tube for a minimum of 3 minutes at 170 × g, the supernatant
are cleaned with a cotton swab and, finally, a few drops is discarded, and the sediment examined (Fig. 13). Identi-
of sediment are placed on a microscope slide, a coverslip fication of the larvae often requires that they be killed in
is placed on top and the preparation is examined (Fig. 12). an extended position. This is easily achieved by judiciously
warming the droplet of water before applying the coverslip.
Advantages As an alternative to heating, a drop of Lugol’s solution may
This technique is useful for samples with high fat be added at the edge of the coverslip. This both relaxes and
concentrations. stains the larvae.
The sluggishness of some larvae is a problem with this
Disadvantages method, so fresh samples are absolutely essential. Another
It is time-consuming to perform, and uses hazardous and issue may be the sloped sides of the funnels, so modified
toxic materials. funnels with vertical sides have been produced to try to over-
come this.
Baermann test This technique is considered to be the gold standard for
The Baermann test is used to isolate larvae from faecal sam- lungworm detection.
ples. It depends on the ability of the larvae to migrate away
from the faeces and into the surrounding water. The lar- Advantages
vae settle out and are found at the bottom of the container. The larvae recovered are not distorted and easier to identify
It requires equipment to hold the faecal sample in the water because no flotation medium is used.
1 2 3 4
5 6 7 8
PARASITOLOGICAL DIAGNOSIS
Ether
Plug of debris
Acid
Sediment
9 10 11 12
13 14
1 2 3 4
5 6 7 8
9 10
PARASITOLOGICAL DIAGNOSIS
In human medicine, it is widely accepted that diagnostic fections requires in-depth training for the specimen prepara-
methods must be accurate, simple and affordable to be use- tion, and expertise and experience for the subsequent micro-
ful. They must also provide a result quickly enough to imple- scopic examination.
ment effective control measures, especially treatment. The method of copromicroscopy to be chosen also de-
Although a faecal examination is considered a routine pends on what the information is going to be used for.
procedure in many veterinary clinics, little thought is often
given to performing the procedure correctly.
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Microscopic coproscopy
Trematodes
Spirometra spp.
Dipylidium caninum
Hexacanth embryo
Joyeuxiella spp.
Taeniidae
Toxocara canis
Thick-shelled,
1 cell
Toxascaris leonina
Thin-shelled,
No larva Ancylostoma or Uncinaria
1 morula
Trichuris vulpis
With polar
plugs
No embryo
Capillariidae
Larva
Egg-shaped with
Sarcocystis spp.
two sporozoites, 12 μm
PARASITOLOGICAL DIAGNOSIS
Major helminth larvae in dogs
Macroscopic coproscopy
Toxocara canis
Roundworms: Ascaridida
Toxascaris leonina
Dipylidium caninum
Segment size
>0.5 cm Taenia spp.
Tapeworms:
Mesocestoides spp.
cestoda
Segment size
Echinococcus spp.
<0.5 cm
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Opisthorchiidae
Trematode egg
Description: small ovoid egg; thick
shell with an operculum at one pole
and a spine at the other (Fig. 14).
Contents: an embryo.
Size: 30 × 20 μm.
Diphyllobothrium latum
Cestode egg
Description: medium-sized, spherical
to ovoid egg; thin shell with an
operculum at one pole (Fig. 15).
Contents: a light brown syncytium
that fills the entire egg.
Size: 60 × 45 μm.
PARASITOLOGICAL DIAGNOSIS
Spirometra
Cestode egg
Description: medium-sized, ovoid to
almost spherical egg; smooth, thin
shell with an operculum at one pole
(Fig. 15).
Contents: a light brown syncytium
that fills the entire egg.
Size: 70 × 60 μm.
Figure 15. Diphyllobothrium or Spirometra eggs.
Dipylidium caninum
Cestode egg
Description: small egg; smooth, thin
shell (Fig. 16).
Contents: a hexacanth embryo.
Size: 50 × 40 μm.
Comment: Dipylidium spp. eggs are
grouped in clusters of 20 inside a
Figure 16. Dipylidium eggs. Figure 17. Dipylidium oviferous thin shell: the egg packet or oviferous
capsule. capsule (Fig. 17).
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Joyeuxiella
Cestode egg
Description: small egg; smooth, thin
shell; cannot be differentiated from
Dipylidium caninum using only a
microscope (Fig. 18).
Contents: a hexacanth embryo.
Size: 50 × 40 μm.
Comment: oviferous capsule
containing only one egg.
Taeniidae
Cestode egg
Description: small, globular egg with
a unique, thick envelope; radially
striated (Fig. 19).
Contents: a hexacanth embryo.
Size: 30–40 × 20–30 μm.
Comment: eggs are excreted in an
oviferous segment; no morphological
differences between Taenia and
Echinococcus. Figure 19. Taeniidae eggs.
Mesocestoides
Cestode egg
Description: small, globular egg;
smooth, thin shell (Fig. 20).
Contents: a hexacanth embryo.
Size: 50 × 40 μm.
Toxocara canis
Nematode egg
Description: medium-sized, globular
egg; thick-shelled with an alveolar
external layer (thimble-like) and
smooth internal layer (Fig. 21).
Contents: a single, dark-brown cell
that almost fills the entire egg.
Size: 70–90 × 65–75 μm.
Toxascaris leonina
Nematode egg
Description: medium-sized,
subglobular egg; thick, smooth outer
shell with concentric layers (Fig. 22).
Contents: a single, light-brown cell
that does not fill the entire egg.
Size: 75–85 × 65–75 μm.
PARASITOLOGICAL DIAGNOSIS
Figure 22. Toxascaris leonina egg.
Capillaria
Nematode egg
Description: medium-sized, quite
narrow beige to brown egg; smooth
shell of medium thickness; elongated
lemon shape with a flattened polar
plug at each pole (Fig. 23).
Contents: one cell.
Size: 55–70 × 30 μm.
Comment: differentiation from
Trichuris eggs is based on the
protruding appearance of the polar
plugs, and globular shape, of
Trichuris compared to Capillaria.
Spirocerca lupi
Nematode egg
Description: small, elongated egg;
smooth shell with parallel sidewalls
(Fig. 25).
Contents: a clearly visible first stage
larva, often folded twice.
Size: 35 × 10–15 μm.
Strongyloides
Nematode egg
Description: small, rectangular small
egg with parallel sidewalls; thin-
shelled; light coloured (Fig. 26).
Content: a larva, not always clearly
visible.
Size: 35–50 × 25–30 μm.
Comment: stage 1 larvae are expelled
in carnivores, whereas eggs are
excreted in herbivores and Suidae.
Trichuris vulpis
Nematode egg
Description: medium-sized, orange-
brown egg; smooth, thick shell;
PARASITOLOGICAL DIAGNOSIS
elongated lemon shape with a
protruding polar plug at each pole
(Fig. 27).
Contents: a single cell.
Size: 60–85 × 40–45 μm.
Giardia
Protozoan cyst
Description: egg-shaped to oval cyst;
smooth, thin shell (Fig. 28).
Contents: two to four flagella, the
cellular nucleus and drumstick-like
residual bodies of which are visible
and feature a central S shape (similar
to the Ying/Yang symbol).
Size: small (7–10 × 8–12 μm).
Sarcocystis
Protozoan cyst
Description: sporocyst with four
sporozoites; very thin shell element;
smooth, elongated shape with
rounded poles (Fig. 29).
Contents: four infective, banana-
shaped cells: the sporozoites.
Size: 12 × 8 μm to 20 × 16 μm
according to the species.
Comment: excreted as oocysts similar
to Isospora, but directly sporulated
and often producing sporocysts in the
digestive tract, therefore possible to
detect by coproscopy.
Figure 29. Sarcocystis cyst.
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Isospora
Protozoan cyst
Description: ovoid oocyst; thin-
shelled; slightly more pointed at one
end and more rounded at the other
(Fig. 30).
Contents: a rounded cell with granular
content when hatched; two sporocysts
that contain four sporozoites each
after sporulation in the external
environment.
Size: medium-sized
(20–40 × 15–35 μm);
Isospora canis: 38 × 30 μm;
Isospora ohioensis: 23 × 19 μm.
PARASITOLOGICAL DIAGNOSIS
Figure 30. Isospora oocysts.
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Cryptosporidium parvum
Protozoan cyst
Description: spherical to egg-shaped
oocyst, with a relatively thick shell
compared to other coccidia (Fig. 31).
Contents: clearly visible oocyst
residual body, and four vermiform
sporozoites hardly visible with light
microscopy.
Size: small (5 × 4 μm).
Strongyloides stercoralis
Nematode larva
Description: thin, rhabditiform stage
1 larva; club-shaped anterior end;
short buccal cavity; sharp, pointed
tail. Large genital primordium clearly
visible (Fig. 33).
Size: 280–380 × 15–18 μm.
Oslerus osleri
Nematode larva
Description: strongyle-like stage
PARASITOLOGICAL DIAGNOSIS
1 larva; undulating, pointed tail with
two curls;. oesophagus hardly visible
(Fig. 34).
Size: 250–350 μm long.
Angiostrongylus vasorum
Nematode larva
Description: thin, strongyle-like
stage 1 larva; button on the head;
undulating, pointed tail with a dorsal
notch (Fig. 35).
Size: 330–360 μm long.
Crenosoma vulpis
Nematode larva
Description: strongyle-like stage
1 larva; elongated caudal end with
no dorsal notch; no button on the
head; oesophagus clearly visible
and strongyle-like, measuring up to
1/3 of the entire length of the larva
(Fig. 36).
Size: 265–330 μm long.
Dipylidium caninum
Cestode
Description: strobila made up of
whitish segments longer than they
are wide; relatively narrow and barrel-
shaped.
Expelled one at a time
(2–4 × 6–10 mm) or in clusters
PARASITOLOGICAL DIAGNOSIS
of segments (Figs. 38 and 39).
Elements attach to fur and look like a
Figure 38. Dipylidium proglottids on dog faeces. rice or semolina grains when drying.
Can be found in the animal’s direct
environment: bed, chairs, etc.
Taenia spp.
Cestode
Description: strobila made up of
rectangular, whitish segments, longer
than they are wide. Expelled as single
element or in clusters (Fig. 40).
Size: 8–15 × 5–6 mm for each
oviferous segment.
Mesocestoides (segment)
Cestode
Description: small whitish segments
with rounded sidewalls; central spot
representing the parauterine organ
(Fig. 41).
Size: 5–6 × 3–4 mm.
Echinococcus granulosus
Cestode
Description: one rectangular oviferous
segment per cestode; 4–6 mm long
and 1 wide; difficult to identify
macroscopically. Oviferous segment
represents more than half of the
total body length and contains a
longitudinally elongated uterus
(Fig. 42).
Echinococcus multilocularis
Cestode
PARASITOLOGICAL DIAGNOSIS
Description: one rectangular oviferous
segment per cestode; 2-3 mm long
and 1 wide; difficult to identify
macroscopically. Oviferous segment
represents less than half of the
total body length and contains a
sacculated uterus (Fig. 43).
Microscopic coproscopy
Trematodes
Spirometra spp.
Taeniidae
Toxocara cati
Thick-shelled,
1 cell
Toxascaris leonina
Thin-shelled,
No larva Ancylostoma or Uncinaria
1 morula
With polar
Capillariidae
plugs
No embryo
Larva
Cryptosporidium parvum
Spherical, 4–5 μm
Cryptosporidium felis
Egg-shaped with
Sarcocystis spp.
two sporozoites, 12 μm
PARASITOLOGICAL DIAGNOSIS
Major helminth larvae in cats
Rhabditoid apparatus absent or difficult Third stage larvae in sheath, and tail
Ollulanus tricuspis
to distinguish (no anterior spot) with three sharp points
Macroscopic coproscopy
Toxocara cati
Roundworms: Ascaridida
Toxascaris leonina
Dipylidium caninum
Segment size
>0.5 cm Taenia taeniaeformis
Tapeworms:
Mesocestoides spp.
cestoda
Segment size
Echinococcus spp.
<0.5 cm
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Opisthorchiidae:
Clonorchis and Metorchis
Trematode egg
Description: small ovoid egg; thick
shell with an operculum at one end
and a polar spine at the opposite end
(Fig. 44).
Contents: an embryo.
Size: 30 × 20 μm.
Diphyllobothrium or
PARASITOLOGICAL DIAGNOSIS
Spirometra
Cestode egg
Description: medium-sized ovoid
egg; smooth shell with an operculum
(Fig. 45).
Contents: light golden-yellow
syncytium which fills the entire shell.
Size: 60 μm long × 45 μm wide.
Dipylidium caninum
Cestode egg
Description: small egg; thin, smooth
shell (Fig. 46).
Contents: a hexacanth embryo.
Size: 40 × 50 μm.
Comment: Dypilidum spp. eggs are
grouped in clusters of about 20 in
egg capsules, encased by a thin shell:
the oviferous or egg-bearing capsule.
Size: 200 × 400 μm.
Taeniidae
Cestode egg
Description: small globular egg;
unique, thick envelop; radially
striated (Fig. 47).
Contents: a hexacanth embryo.
Size: 30–40 × 20–30 μm.
Comment: eggs are eliminated in
an ovigerous segment. Genus and
species diagnosis is not possible
(Taenia or Echinococcus).
Mesocestoides
Cestode egg
Description: small, globular egg; thin,
smooth shell (Fig. 48).
Contents: a hexacanth embryo.
Size: 40 × 50 μm.
Toxocara cati
Nematode egg
Description: medium-sized, globular
egg; thick-shelled with an alveolar
external layer (thimble-like) and
smooth internal layer (Fig. 49).
Contents: a single, brownish-black
cell filling almost all the shell.
Size: 70–90 × 65–75 μm.
Toxascaris leonina
Nematode egg
Description: medium-sized,
subglobular egg; smooth, thick shell
with concentric layers (Fig. 50).
Contents: a single, yellowish-brown
cell filling only part of the shell.
PARASITOLOGICAL DIAGNOSIS
Size: 75–85 × 65–75 μm.
Ancylostoma or Uncinaria
Nematode egg
Description: ovoid, medium-sized
strongyle-like egg; thin, smooth shell
(Fig. 51).
Contents: a morula with four to eight
large blastomeres.
Size: 55–65 × 40–45 μm.
Comment: Ancylostoma eggs are
smaller (55–65 × 40 μm) than
Uncinaria eggs (65–80 × 45–50 μm),
but it is difficult to distinguish
between them in practice.
Figure 51. Ancylostoma egg.
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Capillaridae
Nematode egg
Description: medium-sized light-
coloured egg; relatively straight,
smooth and semi-thick shell;
elongated (lemon-shaped) with a
flattened polar plug at each end
(Figs. 52 and 53).
Contents: a single cell. Figure 52. Capillaria plica (urine) egg. Figure 53. Capillaria aerophila egg.
Size: 55–70 × 30 μm.
Comment: the identification of Trichuris
eggs is not relevant to domestic cats
in Europe. The only known Trichuris
in Felidae were found in wild animal
species, especially in South America.
Spirura rytipleurites
Nematode egg
Description: elongated egg; thick,
smooth shell (Fig. 54).
Contents: a well-developed larva.
Size: 45–55 × 25–35 μm.
Strongyloides
Nematode egg
Description: small, rectangular small
egg with parallel sidewalls; thin-
shelled; light coloured (Fig. 55).
Content: a larva, not always clearly
visible.
Size: 35–50 × 25–30 μm.
Comment: stage 1 larvae are expelled
early in carnivores, whereas eggs are
excreted in herbivores and Suidae.
Giardia
Protozoan cyst
Description: egg-shaped to oval cyst;
smooth, thin shell (Fig. 56).
Contents: two to four flagella, the
cellular nucleus and drumstick-like
residual bodies of which are visible
and feature a central S shape (similar
to the Ying/Yang symbol).
Size: small (7–10 × 8–12 μm).
Comment: lugol staining.
Cryptosporidium
Protozoan cyst
Description: spherical to egg-shaped
oocyst; relatively thick shell compared
to other coccidia (Fig. 57).
Contents: clearly visible oocyst
residual body, and four sporozoites
PARASITOLOGICAL DIAGNOSIS
hardly visible with light microscopy.
Size: small (5 × 4 μm).
Comment: Ziehl-Nielsen staining.
Toxoplasma, Hammondia
and Besnoitia
Protozoan cyst
Description: egg-shaped oocyst;
smooth, thin shell with rounded ends
(Fig. 59).
Contents: a single granular, spherical
cell before sporulation, then
two sporocysts that contain four
sporozoites each at sporulation in the
external environment.
Size: 12–15 × 10–13 μm.
Isospora
Protozoan cyst
Description: thin-shelled, ovoid oocyst
with one end being more pointed than
the other (Fig. 60).
Contents: a single rounded cell with
granular contents when hatching;
two sporocysts that contain four
sporozoites each after sporulation in
the external environment.
Size: Isospora felis: 40 × 30 μm;
Isospora rivolta: 25 × 20 μm.
Strongyloides
Nematode larva
Description: thin, rhabditiform stage
1 larva; club-shaped anterior end;
short buccal cavity; sharp, pointed
tail. Large genital primordium clearly
visible (Fig. 61).
Size: 280–380 × 15–18 μm.
PARASITOLOGICAL DIAGNOSIS
Figure 61. Strongyloides L1.
Crenosoma vulpis
Nematode larva
Description: strongyle-like larva 1;
elongated posterior end; no dorsal
spine or cephalic plug. Strongyle-
like oesophagus clearly visible and
measuring a third of the total length
(Fig. 62).
Size: 265–330 μm.
Aelurostrongylus abstrusus
Nematode larva
Description: thin-walled, strongyle-
like larva 1 with undulating, pointed
tail at the posterior end and a dorsal
spine (Fig. 63).
Size: 360–400 μm.
Toxocara cati –
Toxascaris leonina
Nematode
When adults are numerous in a kitten
intestine, they can be expelled in
faeces or vomit.
Description: large, white, rounded
worms measuring up to 10 cm long,
with a diameter of 2–3 mm; often
intertwined with one another and
forming ascarid clusters (Fig. 64).
Dipylidium caninum
(strobila)
Cestode
Description: strobila made up of
whitish segments, longer than they
PARASITOLOGICAL DIAGNOSIS
are wide; relatively narrow and barrel-
shaped. Expelled one at a time
(2–4 × 6–10 mm) or in clusters of
segments (Fig. 65). Elements attach
to fur and look like a rice or semolina
grains when drying. Can be found in
the animal’s direct environment: bed,
chairs, etc.
Taenia taeniaeformis
Cestode
Description: strobila made up of
rectangular, whitish segments, longer
than they are wide. Expelled as single
element or in clusters (Fig. 66).
Size: 8–15 × 5–6 mm for each
oviferous segment.
Mesocestoides
Cestode
Description: small whitish segments
with rounded sidewalls; central spot
representing the parauterine organ
(Fig. 67).
Size: 5–6 × 3–4 mm.
Echinococcus multilocularis
Cestode
Description: rectangular oviferous
segment; 2–3 mm long and 1 mm
wide; one per cestode; difficult to
identify macroscopically (Fig. 68).
PARASITOLOGICAL DIAGNOSIS
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1 2
Contact between the two slides
3 4
Gently push slide 2 to spread the
blood over slide 1
PARASITOLOGICAL DIAGNOSIS
TABLE OF
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Dermatological
examination
External examination of the animal’s skin and fur enables Superficial skin scrapings are taken from large body areas.
several ectoparasites to be detected and identified. These in- Deep skin scrapings are usually performed in an area of hair
cludes fleas, lice, mites and ticks which can cause parasitic loss or skin lesions. The skin is squeezed before or during
diseases, but also transmit vector-borne pathogens. Some the scraping to promote extrusion of mites from hair follicles
ectoparasites are visible to the naked eye, and others require (Demodex) or burrows (Sarcoptes).
microscopic identification (see Ectoparasites of dogs and
cats under the microscope, page 345). Trichogram (microscopic
examination of plucked hair)
Skin scrapings A trichogram consists of plucking several hairs using clamp
A skin scraping may be superficial or deep. In the first case, it scissors (Fig. 2). It enables whole hair follicles to be collected,
consists of sampling the first layers of the epidermis to collect which is useful for the observation of Demodex mites, espe-
ectoparasites that remain on the surface of the skin (Cheyletiel- cially in areas where skin scraping is difficult or especially
la mites). Deep skin scrapings are recommended for Demodex painful (from sites close to the eyes, for example).
mites which live deep in the hair follicle, and for Sarcoptes sca-
biei females that burrow into the deeper layer of the epidermis. Scotch tape test
Scraping is carried out with a blunt scalpel blade (Fig. 1). The use of a clear sticky tape enables debris to be collected from
Lactophenol (or paraffin oil, which does not kill Demodex) the surface of the skin. The sticky side of the tape is pressed
may be applied to the blade to make sure debris and para- down onto the skin several times and then pressed onto a slide
sites adhere, and is also placed on the slide and mixed with where it serves as a coverslip. This technique is especially use-
the collected material before being covered with a coverslip. ful for the detection of Cheyletiella and Lynxacarus mites.
Figure 1. Skin scraping being taken from a skin lesion in a dog with suspected Figure 2. Hairs being plucked
demodicosis. from a skin lesion in a dog with
suspected demodicosis.
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Tick extraction
Ticks are the biggest arthropods found on animals and they
are visible to the naked eye. Methodical examination of the
dog/cat fur by thumb palpation is still required to locate
them and unengorged immature stages may be difficult to
see and identify. When extracting the tick, it is important to
avoid leaving the tick rostrum in the skin. Tweezers should
therefore be used to carefully twist the tick until the whole
rostrum is detached, or a specific tick remover can be used
(Fig. 3). Once removed, the tick can be identified using a di-
agnostic key (see Diagnose of the main tick genera infesting
dogs, cats and humans, page 249).
Figure 3. A tick being extracted from a dog using a tick
Flea combing remover.
It may be difficult to see fleas on an infested animal, especial-
ly animals with a long, dark coat. All debris can be collected Collection of ear wax
from the coat with a specific comb with very fine teeth, called Ear wax collection is the examination of choice to diagnose
PARASITOLOGICAL DIAGNOSIS
a flea comb. Flea faeces may be collected in the absence of Otodectes cynotis, which causes ear mange. Ear mites can
fleas and these may be differentiated from other debris by often be seen during otoscopic examination. The typical
placing them onto damp white paper or tissue where dilution dark brown smelly debris can be collected, mounted in lac-
of the faeces shows as red traces of digested blood. tophenol and examined under the microscope.
TABLE OF CONTENTS
NEMATODES EGGS
ROUNDWORMS (ASCARIDS) HOOKWORMS WHIPWORMS
70–90 × 65–75 µm 75–85 × 65–75 µm 55–65 × 40–45 µm 60–85 × 40–45 µm
PROTOZOAN CYSTS
Magnesium sulphate: 35 % saturated solution of
magnesium sulphate (D = 1.28).
Zoonosis
TABLE OF CONTENTS
INSECTS
FLEAS LICE
2–3 mm long 2–3 mm long 1–2 mm long 1–2 mm long 1–1.5 mm long
Ctenocephalides felis Ctenocephalides canis Linognathus setosus Trichodectes canis Felicola subrostratus
◗ Most common flea on dogs and cats ◗ Seen on dogs, less common than Sucking louse Chewing louse Chewing louse
◗ Orange to dark brown, wingless C. felis ◗ Small pointed head with terminal ◗ Head is wider than it is long ◗ Wide body
◗ Laterally compressed body ◗ Similar to C. felis in size and appearance mouthparts ◗ Wide yellowish body ◗ Triangular head, pointed anterior end
◗ Long head, 6 notches bearing setae ◗ Short head, 8 notches bearing setae on ◗ Bluish-black colour ◗ Antennae in 3 segments
on dorsal border of hind tibia dorsal border of hind tibia
◗ Possible pathogen transmission:
• Bartonella henselae ◗ Possible pathogen transmission
(cat scratch disease)
• Dipylidium caninum (tapeworm)
0.5 mm 0.5 mm
Eggs Eggs Eggs: 1 mm Eggs: 1 mm Eggs: 1 mm
ACARIDS
MITES
0.2–0.4 mm long 0.5 mm long 0.2–0.4 mm long 0.5 mm long 0.25–0.3 mm long
Sarcoptes scabiei
Dog sarcoptic mange mite C. yasguri C. blakei D. canis D. cati
◗ Seen in deep skin scrapings, difficult Otodectes cynotis
to find Cheyletiella spp. Neotrombicula autumnalis Ear mite Demodex spp.
◗ Best results from non-excoriated sites Fur mite, Walking dandruff Harvest mite, Chigger ◗ Visible in situ with otoscope (poor ◗ Seen in deep skin scrapings from areas
e.g., edges of the ears, elbows, hocks ◗ Saddle-shaped with a “waist” ◗ 3 pairs of legs (larva is the only parasitic sensitivity) of comedomes
◗ White oval body stage)
◗ 4 pairs of legs ◗ Adults and eggs seen microscopically in ◗ Squeeze skin to extrude mites from
◗ 4 pairs of short legs: anterior legs have
◗ Found by direct examination of coat ◗ Bright red, pin-head dots, typically found ear cerumen follicles
suckers, posterior legs do not extend
brushings with magnifying glass between paws, on ears, or on eyelids ◗ Large white oval body ◗ Take hair plucks from affected areas
beyond body
◗ Many transverse ridges and triangular ◗ Confirmed microscopically by ◗ Seasonal; seen in autumn ◗ 4 pairs of projecting legs (4th pair reduced ◗ Long cigar-shaped body
scales on dorsum superficial skin scrapings or ◗ Confirmed microscopically by superficial in females) ◗ 4 pairs of atrophied legs
adhesive band test skin scrapings ◗ Whip-like setae attach terminally to 3rd and
Notoedres cati
Cat mange mite 4th pairs of legs
◗ Smaller than S. scabiei ◗ Adult mites occasionally seen in skin
◗ Many concentric striations on dorsum scrapings from other body areas
TREATMENT AND
PROPHYLAXIS
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Anthelmintics
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Anthelmintics suitable for dogs and cats belong to various Dog and cat anthelmintics have no persistent effect, which
chemical groups and they have traditionally been admin- means that a single administration will kill the parasites pres-
istered orally, although spot-on formulations have recently ent in the host at the time of treatment, but will not protect
been introduced (especially for use in cats). Consideration the host against reinfestation.
must also to be given to the development of parasiticidal
drugs with both internal and external antiparasitic effects
which meet the demand for prevention of both endo- and
ectoparasitoses in carnivores.
Cholinergic agonist
N Roundworms,
H that selectively
hookworms, and
S causes depolarisation
Imidazothiazoles Levamisole nematodes of the No
N and spastic paralysis
respiratory and urinary
of nematode muscle
systems
cells
N
Roundworms,
Pyrantel No
N Cholinergic agonist hookworms
that selectively
S
causes depolarisation
Pyrimidines
and spastic paralysis
of nematode muscle
N
cells
Oxantel OH Whipworms No
N
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CONTENTS Anthelmintics 351
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O
S CH3
HN O Roundworms,
Febantel (pro-
N NH hookworms, whipworms No
fenbendazole)
H3C NH CH3 (single administration)
O O O
O
Roundworms,
O hookworms, whipworms,
N O
Fenbendazole Taenia spp. No
NH
S N (repeated administration
H required)
Roundworms,
O
hookworms, whipworms,
N O
NH Taenia spp.,
Oxfendazole Inhibit tubulin No
S N Dipylidium caninum
H polymerisation
Benzimidazoles O (repeated administration
by binding to
and required)
the a-tubulin in
probenzimidazoles
nematodes and
O
some cestodes
CH3 Roundworms,
O C N
H Roundworms,
O N
NH hookworms, whipworms,
Oxibendazole No
N O Taenia spp. (repeated
O administration required)
O H3CO Roundworms,
N O hookworms, whipworms,
Flubendazole NH No
Taenia spp. (repeated
F N
H administration required)
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HO H O
OH O
N O Roundworms
O
H OH (Toxocara canis,
O O
Selamectin T. cati), hookworms Yes
H OH
O (Ancylostoma caninum,
A. tubaeforme)
Roundworms (Toxocara
Open chloride
HO cati, Toxascaris leonina),
O O H channels in the
H O hookworms
Macrocyclic O
H
neuronal synapses by
(Ancylostoma
O H
lactones Eprinomectin O OCH3
OH O binding to glutamate Yes
H tubaeforme,
(avermectins and OCH3 receptors. Cause
A. braziliense,
HN O
milbemycins) H OH hyperpolarisation and
A. ceylanicum),
O
block muscle cell
Capillaria plica
stimulation
H
O
Roundworms,
O R
hookworms
Milbemycin O O (Ancylostoma),
OH R: CH3 (30 %) Yes
oxime R: CH2CH3 (70 %)
whipworms, Thelazia
callipaeda, Spirocerca
O
H
N lupi
HO
O
N
CH3
H3C
CH3 Roundworms,
H
O H
CH3
hookworms, whipworms,
O Angiostrongylus
H CH3 CH3
Moxidectin H3C
H O O Yes
OH
vasorum, Spirocerca
H
lupi, Crenosoma vulpis,
O H CH3 Thelazia callipaeda
OH
O Bind to a group of
N G protein-coupled
O
receptors called Roundworms,
O
N
O
N latrophilins in hookworms (including
Octadepsipeptides Emodepside O O O OO No
neuromuscular migrating larvae) and
N N O
O junctions in whipworms
O
O N nematode muscle
O cells
▲
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CONTENTS Anthelmintics 353
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N O
Taenia spp.,
Epsiprantel N Echinococcus spp., No
Dipylidium caninum
O
Causes muscular
contraction in
Isoquinolines
cestodes and some
trematodes
O
Taenia spp.,
Praziquantel N Echinococcus spp., No
Dipylidium caninum
N O
O Inhibits oxidative
N+ phosphorylation
O O Taenia spp. (at 80 to
Niclosamide Cl and blocks glucose No
N 150 mg/kg)
H absorption by
Cl
OH cestodes
Inhibits the
O Roundworms,
respiratory chain (ATP
Nitroscanate S hookworms, Taenia spp., No
O2N C synthesis) in parasite
N Dipylidium caninum
cells
Blocks the
H acetylcholine and
N
Effects on heartworms
have not been
completely defined
NH2 but include alterations
in glucose uptake
NH2 S
As NH2 and metabolism, Dirofilaria immitis
Melarsomine N N S No
glutathione reductase (adults)
H2N N N
inhibition, and
H
alterations in the
structure and function
of the parasite’s
intestinal epithelium
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354 TEXTBOOK OF CLINICAL PARASITOLOGY IN DOGS AND CATS CONTENTS
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have been published and the protocol usually recommended treatment of intestinal nematodes in dogs and topical treat-
for breeding bitches is the daily administration of 50 mg/kg ment of otoacariosis in cats. Various scientific publications
fenbendazole during the last third of gestation and the first have reported the activity of ivermectin, at a subcutaneous
15 days of lactation. Infestation of the puppies in utero and dose of 200 µg/kg, against most nematode parasites: round-
through the milk is therefore avoided. Such measures are only worms, hookworms (Ancylostoma and Uncinaria, whip-
possible under certain conditions in special breeding facilities. worms, spiruroids, Oslerus osleri, and Angiostrongylus
In addition to their anthelmintic activity, some benzimi- vasorum). Signs of intoxication have been observed in some
dazoles are effective against some flagellate protozoa, espe- dogs, especially Collies and similar breeds (Australian Shep-
cially Giardia duodenalis. Fenbendazole and oxfendazole, herds, Old English Sheepdogs, Shetland Sheepdogs, etc.) at
administered at the anthelmintic dose for 3 days, can there- doses as low as 50 µg/kg. These dogs have a mutation in the
fore be used to treat giardiosis in dogs and cats. MDR1 gene that affects the blood-brain barrier and makes
it more permeable to ivermectin.
Nitroscanate Milbemycin oxime licenced for the prevention of cardio-
Nitroscanate is a phenyl isothiocyanate that inhibits the res- pulmonary canine dirofilariosis (in a single dose of 500 µg/
piratory chain of parasite cells (inhibition of ATP synthesis). kg every month) and for the treatment of intestinal nema-
Administered at 50 mg/kg, nitroscanate is very effective todes in dogs and cats (in combination with praziquantel).
against roundworms and hookworms but not totally effec- Milbemycin oxime is effective against roundworms, hook-
tive against whipworms. It is tolerated well by dogs, in spite worms (Ancylostoma spp.) and whipworms.
of possible vomiting due to gastric irritation which can be Selamectin is an avermectin administered as a spot-on ap-
avoided by administering the drug in the morning with one plication at 6 mg/kg bodyweight. The product is absorbed
third of the dog’s daily ration. Nitroscanate is not tolerated through the skin into the bloodstream and it has both a resid-
well by cats, so it is not licenced for use in cats. ual action on some external parasites (fleas, Sarcoptes spp.,
Otodectes) and an anthelmintic effect. It is effective against:
Macrocyclic lactones T. canis, T. cati, Ancylostoma caninum and A. tubaeforme,
Macrocyclic lactones of the avermectin/milbemycin group but it is not effective against Uncinaria stenocephala, Toxas-
are effective against most nematodes found in carnivores. caris leonina or Trichuris vulpis.
These molecules are considered endectocides as they are also Moxidectin is now used as a spot-on, like selamectin, for
active against external arthropod parasites, such as lice, Dip- dogs, cats and ferrets. The dosage is 1 mg/kg for cats and fer-
tera, mange mites, Demodex spp., and some fleas. Macrocy- rets, and 2.5 mg/kg for dogs. Moxidectin is effective against
Puppies should be treated with appropriate anthelmintics 2 weeks before the end of gestation, immediately after birth
when they are 2 weeks of age, continuing at fortnightly in- of the puppies, and then every 2 weeks until the puppies are
tervals until 2 weeks after weaning, and then monthly until weaned. An anthelmintic with a larvicidal effect against
6 months of age. As prenatal infestation does not occur in roundworms should be used (benzimidazoles, emodepside or
kittens, fortnightly treatment can begin at 3 weeks of age avermectin/milbemycin). Special protocols might be required
and be repeated fortnightly until 2 weeks after weaning, in breeding facilities.
then monthly for 6 months. An anthelmintic which is active Breeding cats (queens) should be dewormed when their
against migrating larvae is recommended until puppies and kittens are born, then every 15 days until the kittens are
kittens are weaned. Thereafter, any anthelmintics are suita- weaned, with an anthelmintic which is active against larvae.
ble, including those that do not cross the intestinal barrier, Queens can be dewormed 1 month after each oestrus since
such as pyrantel. The choice will also depend on what other encysted roundworm larvae can be reactivated at this time.
parasites are present if coproscopy indicates that the animal
is infested with whipworms, tapeworms (Dipylidium) or Gi- Environment and lifestyle
ardia, for example. Urban and rural cats and dogs may host different parasites,
There is less risk of reinfestation when weaned puppies and animals living in urban areas, with no access to
and kittens go to live with their new owners. Systematic de- gardens, peri-urban parks or woodland, may host less
worming is recommended when animals are purchased and various parasites. These urban animals should be dewormed
1 month later. This can easily be done when the young ani- following faecal examination and treated with products
mals are presented in consultation for their vaccinations. which are active against these parasites (and fleas).
Toxocara spp. infestation can occur in older dogs and In rural areas, domestic carnivores spend more time out-
cats, and is extremely unlikely to be associated with clin- doors, especially hunting dogs and farm cats, and many
ical signs; therefore it is difficult to detect whether a dog parasites can be found in these animals so polyparasitism is
is infested unless regular faecal examinations are conduct- common. For example, dogs might be infested with Ancy-
ed. These parasites are prolific egg-layers and just a few lostoma (Uncinaria)/Trichuris and/or Taenia species (if they
worms can produce a large number of eggs. Continued, have access to ruminant or rabbit viscera). Cats are often in-
regular treatment of dogs and cats using a suitable anthel- fested by Taenia taeniaeformis or Mesocestoides spp. tape-
mintic is therefore recommended by ESCCAP (European worms by eating rodents (rats and mice).
Scientific Counsel Companion Animal Parasites: www. E. granulosus infestation in dogs is mainly associated with
esccap.org) if regular diagnostic testing is not undertak- lifestyle: sheepdogs and dogs who have access to viscera from
Spectrum of activity
Clinical suspicion and faecal examination should be used Water-dispersible liquids, and tablets that can be mixed
more when deciding whether to use anthelmintics to treat with feed, make it easier to administer a drug but they are
carnivores. Faecal examination is inexpensive and easy to only effective if they do not reduce the palatability of the food
perform at the veterinary practice, and can prevent healthy and are correctly and completely consumed. They are not
animals being treated, and enable treatment to be adapted to suitable for group treatment because it is difficult to know
each situation. how much each animal has received. Transdermal drug de-
A good example of this is D. caninum. This cestode is livery systems, such as systemic spot-on formulations, have
not a major pathogen and infestation is tolerated well by the the advantage of being easy for pet owners to administer.
animal. The segments are numerous and clearly visible. They Regardless of the drug delivery system, most pet owners
are 4–6 mm long and either mobile and whitish, or dry and prefer one-step administration protocols to repeated treat-
white. They can be seen in the perianal region or on the ani- ments. The choice depends on the commercial products
mal’s hind legs, or in its immediate surroundings. Diagnosis available and the internal parasites targeted. Certain diseas-
is simple and treatment can be restricted to animals known es, such as giardiosis, still require repeated administrations.
to be infested.
Finally, one of the most prevalent parasites is the flagellate Conclusion
G. duodenalis. The presence of cysts should be actively in- Deworming dogs and cats is now very common and it is often
vestigated and, when they are identified, this parasite should done systematically, without prior diagnosis. In this context,
be included in any treatment for internal parasites. the anthelmintic is selected based on epidemiological factors,
such as the age and the lifestyle of the animal. Product choice
Ease of administration also depends on the size of the animal and owner compliance
Pet owners demand products that are not only effective, but with the treatment regime.
easy to use. Considerable progress has been made in the de- Systematic deworming has the advantage of limiting new
velopment of veterinary products to control both external infestations but it is still possible for animals to be infested
and internal parasite infestations. outside the classic deworming periods, and treatment can fail
Injectable forms are useful in breeding facilities and oral due to the presence of parasites (e.g., protozoa, cestodes or
pastes are easy to administer, especially to young or small less common nematodes) that are not covered by the chosen
animals. Tablets are also easy to administer to medium-sized anthelmintic.
and large dogs, but small dogs and cats, which may be less Breeding facilities must remember that regular worming
obliging, are generally resistant to this form of product and is necessary, but not the only precaution required, as effective
pill size is a determining factor. Chewable worming tablets cleaning and disinfection are essential.
are now available and these formulations are easily adminis-
tered to dogs and cats.
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Antiprotozoals
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Ectoparasiticides
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Companion animals are commonly treated with ectoparasit- Chemical groups and molecules
icides, which represent 75 % of all antiparasitic drugs used in Ectoparasiticides used in cats and dogs have evolved in terms
dogs and cats. This is due to the prevalence of ectoparasites of active ingredients, dosage forms and pharmacokinetics,
which cause the most common diseases in carnivores. and they mainly act on the arthropod nerve synapses and
Ectoparasiticides applied directly onto the animal are vet- axons. Traditional chemical groups, especially organophos-
erinary drugs. They must be registered as veterinary medi- phates and carbamates, have been supplanted by new com-
cines by the health agencies in each country in order to be pounds. In addition to insecticides-acaricides, insect growth
granted with marketing authorisation. On the other side, in- inhibitors have also emerged, and these can be separated into
secticides or acaricides which are not applied to the animal two categories: juvenile hormone analogues and chitin syn-
but used in their environment are not considered to be veter- thesis inhibitors.
inary drugs but pesticides in the broader sense, even if they
sometimes involve the same molecules. Their formulations Cyclodiene organochlorines
(especially the excipients) are different and they are not reg- The cyclodiene organochlorine most commonly used in an-
ulated by the same legislation, nor do they require marketing imals used to be lindane, which was isolated in 1912 and
authorisation as veterinary medicines. started to be used in animals in 1943, but it has now been
In addition to the molecules used and their mode of action, banned in most countries. These molecules had a broad
it is important to chose formulations that will either facilitate spectrum of activity against arthropods but were not free
product application, which is the case for spot-ons, palatable from toxicity; they are highly persistent in the environment,
tablets and collars, or modify the pharmacokinetics to in- in milk and in meat, and may be retained in vertebrate fat.
crease the duration of the product’s activity. Development of Organochlorines inhibit gamma aminobutyric acid (GABA)
parasiticidal drugs with both external and internal antipar- and/or stimulate the sodium channels located in the nerve
asitic spectra is required to meet the demand for prevention cell membrane to open.
of both ecto- and endo-parasitosis in domestic carnivores.
TABLE OF
CONTENTS Ectoparasiticides 369
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CI
CI CI CI Binding sodium channel.
Cyclodiene Stimulation of sodium entry
Lindane * CI Insects + ticks + mites
organochlorines into nerve cells. Arthropod
hyperexcitation
CI
CH3
CH3 CH S O CH2 CH3
Diazinon (= N P
O
Insects + ticks + mites
dympilate) N O CH2 CH3
O
C CH3 Acetylcholinesterase binding.
Carbamates Carbaryl O N Acetylcholine hyperactivity, nerve Fleas
H
O
H C O CH2 O
Insects + ticks + mites
Permethrin
H CH3 (repellent)
CI
C C CH3
CI H Sodium channel binding.
Pyrethroids Sodium entry, nerve cell
O hyperexcitation
CI
CI C Sodium channel binding.
N
Pyrethroids Flumethrin CH O Sodium entry, nerve cell Ticks
C O
C
H3C O CH F hyperexcitation
CH3
F
F F
C
O S CN
CI CI
Pyriprole H N Insects + ticks
N N
N
S
F N
F
N N
Imidacloprid Insects
CI N N NO2
NO2
Chloronicotinyl N Nicotinic acetylcholine receptor
nitroguanidines, Dinotefuran agonist, postsynaptic neuron Insects
C
neonicotinoids H3C N N CH2 O stimulation
H H
CI N
H2C O H
H3C O H H
F
O F
O O F
CI O Voltage-dependent sodium
Oxadiazines Indoxacarb Insects
N N channel blocker
N
O
O
O
OCF3
O
F3C N
HN
H
N Sodium channel antagonist,
Semicarbazones Metaflumizone Insects
resulting in paralysis and death
C
N
O
H3C N
CH3 H CH3
O
OH
H
O
O Insects + mites +
Selamectin H
H O nematodes
O
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H
O
O R
Avermectins/ Glutamate receptor binding,
milbemycins O O R: CH3 (30%)
chloride ion channel stimulation. Demodex + Sarcoptes
Milbemycin oxime R: CH2CH3 (70%)
OH
(macrocyclic Entry of chloride ions. Inihibition scabiei
lactones) of nerve cell activity
O
H
N
HO
F F
F O N
CI O
H
F
Afoxolaner N
N
Fleas + ticks + mites
F F F
O H F
F
D10361
F F
F O N
CI
Sarolaner O O Fleas + ticks + mites
F N S O
CI CH3
O
F
CI H H Chitin synthetase inhibitor
Organofluorines- N N
Lufenuron FFF F Inhibits egg hatching, induces Fleas
benzoylureas F O O F
O CI mortality during moulting
F
TABLE OF
CONTENTS Ectoparasiticides 373
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Organophosphates Amitraz
Organophosphates exert an anti-cholinesterase effect which Amitraz is a formamidine that is selective towards arthro-
results in acetylcholine accumulation in the synapses. This pods and has been used since the late 1960s to control ticks.
neurotransmitter has a postsynaptic stimulating action and Amitraz does not act directly on nerve conduction but alters
arthropods become hyperactive prior to death. arthropod behaviour, which has been studied in ticks. It in-
Their spectrum of activity is broad, and includes insects terferes with the arthropods’ octopaminergic system, which
and acari. Organophosphates have been used for many years is similar to the adrenergic system in mammals, by binding
(since the 1950s) so cases of chemoresistance are not uncom- to the octopamine receptors, stimulating monoamine ox-
mon and have been reported all over the world. These cases idases (adenylate cyclase activity) and G proteins. This in-
involve flies, crawling insects, ticks and fleas. duces the synthesis of cAMP and cGMP which have various
Organophosphates have short residual activity (only a intracellular activities. At a sublethal dose, attached ticks will
few days) apart from in certain formulations, such as collars. fall off their host, and those that infest the host do not attach
They are hydrolysed quite rapidly in the environment and or feed. Reproduction is impaired, prolificacy is reduced and
are persistent for a few weeks on inert surfaces but far less on most of the eggs do not hatch.
organic surfaces. They can be toxic (parasympathomimet- Amitraz is used on dogs to control ticks of the main gen-
ic) in mammals and any overdose or accidental ingestion, of era infesting dogs (Rhipicephalus, Dermacentor, Ixodes,
a collar for instance, must be avoided. Cats are much more Haemaphysalis and Amblyomma) or to treat mite infes-
sensitive than dogs. tations, such as demodicosis (Demodex canis), sarcoptic
The molecules belonging to this group, and their formu- mange (Sarcoptes scabiei var. canis) or cheyletiellosis (Chey-
lations, are numerous, as solutions, sprays, powders, spot- letiella yasguri).
ons and collars are available on the veterinary health market. Amitraz may interact with the adrenergic system in car-
The molecules most widely used in pets are: coumaphos, nivores. Intoxication can be caused by ingesting, chewing or
cythioate, diazinon (also called dimpylate), dichlorvos, feni- sucking amitraz-impregnated collars, or by licking spot-ons
trothion, and fenthion. or solutions. Intoxication has an a2-agonist effect which
induces hyperglycaemia, causes a neurosedative effect (leth-
Carbamates argy and ataxia) and, more rarely, leads to cardiovascular
Carbamates, esters of carbamic acid and classified as methyl disorders (bradycardia, hypotension). Specific treatment for
or dimethyl carbamates, also inhibit acetylcholinesterase. poisoning is possible with atipamezole, an a2-antagonist
They are not long-acting (2 to 4 days), except in collars, and and/or yohimbine. Cats are sensitive to amitraz, probably
Fipronil Spinosyns
Fipronil belongs to the phenylpyrazole group and it was Spinosyns are isolated from the bacterial culture of actino-
introduced to veterinary medicine in the mid-1990s in the mycete species, such as Saccharopolyspora spinosa. The two
form of an alcohol spray for use on dogs and cats. It binds main molecules are spinosyns A and D, but many other com-
to GABA and glutamate receptors, which inhibits chloride pounds are derived from this fermentation, and semi-syn-
ion channel opening and consequently leads to neuronal hy- thetic modifications may change insecticidal and pharma-
peractivity. GABA and glutamate are neurotransmitters that cokinetic properties.
inhibit muscle activity in insects and mites. Their attach- Spinosyns have a unique mode of action as they bind to
ment to specific receptors opens neuronal chloride channels and stimulate nicotinic acetylcholine receptors, which stimu-
(in motoneurons or cerebral ganglion neurons in insects), lates postsynaptic neurons. Spinosyns are most active as insec-
inhibiting depolarisation. Glutamate receptors are specific ticides and have little effect on acarian. They can affect insects
to arthropods, resulting in a wide safety margin. Fipronil’s on contact or after ingestion so they may be used in topical
spectrum of activity includes insects (fleas and lice) as well formulations which have combined systemic activity (after ab-
as acari (ticks, Sarcoptes and Cheyletiella) and it is lipophilic sorption) and contact effects, or directly, in oral formulations
and photostable. Whether in a spot-on formulation or a such as tablets. In mammals, they are stored in fat tissues that
spray, the effect on cats or dogs lasts from 15 days (ticks in act as reservoirs, which explains their possible persistence. As
cats) up to 2 months (fleas in dogs). The molecule remains for any systemic drug, the rate of absorption, followed by stor-
active on animals which may get wet in the rain or be washed age and elimination, may vary between animals.
in shampoo, due to its lipophilicity. Spinosad, a mixture of spinosyns A and D, is used in the
It acts on contact with fleas, which die within approximate- form of palatable tablets in dogs and cats. It has anti-flea ef-
ly 24 hours, and ticks which die within 48 hours. Fipronil may fects, which begin 30 minutes after the tablet is ingested, and
be combined with S-methoprene to be active against immature the curative effect against existing flea infestations reaches
flea stages. Synergistic combination with permethrin adds re- maximum efficacy within 4 hours. Anti-flea effects then per-
pellent effect to ticks and flying insects and sustained speed of sist for approximately 1 month against new infestations, and
kill against fleas and ticks. are effective within 48 hours. Combination with milbemycin
Pyriprole, which is similar to fipronil, is lipophilic, so oxime extends the spectrum of activity to include nematodes
treatment and prevention of flea and tick infestations on dogs in dogs.
is by a spot-on solution. Spinetoram is the result of semi-synthetic modifications
of spinosyn J and it has a longer half-life than spinosad. It
affected, leading to cessation of feeding and death. Avermec- New antiparasitic drugs in this chemical class are likely to
tins/milbemycins have a sublethal effect on female nematodes appear in the future. They may be combined with other mol-
and arthropods, stopping egg-laying. Avermectins/milbemy- ecules like milbemycin or selamectin to add nematodicidal
cins are absorbed transcutaneously after spot-on application, activity. Other formulations than oral are possible.
then they circulate in the plasma and are stored in fat tissues.
They are gradually eliminated, mainly in the faeces. Other insecticides
Ivermectin was widely used off-label to treat sarcop- Use of insecticides that do not act on nerve conduction is very
tic mange and ear mange in carnivores, as well as canine limited. Some oxidative phosphorylation inhibitors used as
demodicosis. anthelmintics, especially flukicides, may be effective against
haematophagous arthropods. This is the case for closantel
Nowadays, several avermectins/milbemycins are marketed and nitroxinil which can be used in carnivores to treat para-
for use in domestic carnivores: sitoses such as linguatulosis or some myiases, such as Cordy-
• Milbemycin oxime is used mainly as a broad-spectrum an- lobia anthropophaga.
thelmintic, but may be indicated in dogs with demodicosis. Piperonyl butoxide, an oxidase inhibitor, is a synergist for
It is administered orally. the pyrethroids found in some environmental insecticidal/aca-
• In addition to its nematicidal action, selamectin is used as ricidal formulations but is rarely used in veterinary medicine.
a spot-on in dogs and cats to treat and/or prevent certain Organic silicones or polysiloxanes, especially dime-
ectoparasitoses (pulicosis, canine sarcoptic mange and ear thicone, are used for lice in human medicine. They asphyxi-
mange). ate the arthropod, blocking its respiratory openings and cov-
• Moxidectin is available as a spot-on treatment in combi- ering its entire cuticle.
nation with imidacloprid and is indicated for very simi-
lar uses: nematicidal spectrum plus insecticidal/acaricidal Insect growth regulators
spectrum. Insect growth regulators (IGRs) are molecules that interfere
with hormones or enzymes. They inhibit reproduction in
Isoxazolines adult insects and block organogenesis in immature stages.
Isoxazolines belong to a new chemical class discovered in Their use in veterinary medicine began 20 years ago, to con-
the 2000s. They have very recently been introduced as vet- trol fleas in livestock and domestic carnivores. IGRs used in
erinary products against fleas and ticks in dogs, but they are dogs and cats may be classified into two groups: juvenile hor-
also effective against numerous other arthropods. Isoxazo- mone analogues and chitin synthesis inhibitors.
lines are all isoxazole derivatives and they are non-competi- • Juvenile hormone, or neotenin, analogues act on contact
tive GABA and glutamate receptor antagonists, much more or on ingestion. They enter flea eggs via adult fleas that
selective for GABA receptors in insects or ticks than for those come into contact with the active ingredients, or directly
in mammals, including humans. They bind to a unique site through the cuticle of the eggs. The first mechanism in-
on GABA-gated chloride channels in nerve and muscle cells, hibits egg hatching and these neotenin analogs can also
blocking pre- and postsynaptic transfer of chloride ions prevent the last stage 3 larvae from moulting into pupae.
across cell membranes. This induces hyperexcitation due to These analogs are either used in the environment, in the
uncontrolled activity in the central nervous system of the ar- form of sprays or diffusers and often combined with an
thropod and causes its death. insecticide, or applied directly to the animal.
Afoxolaner, fluralaner, sarolaner, and lotilaner are only Juvenile hormone analogues include methoprene and
used in veterinary medicine. They are characterised by high S-methoprene (active isomer), pyriproxyfen and fenoxy-
permeability and low aqueous solubility. Following oral ad- carb. Fenoxycarb is only used in the environment. In most
ministration, they are quickly absorbed and are highly bio- cases, these analogues are used in animals in combination
available. They are highly bound to plasma proteins and me- with an insecticide/acaricide, such as fipronil, permethrin,
tabolised slowly by P450 enzymes in the hepatocytes. dinotefuran or imidacloprid.
These molecules are lipophilic and persist for several
weeks, which allows residual IGR effects to last for 1 to
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3 months, depending on the formulation and the study time points but, more interestingly, the dogs were clinically
concerned. Fleas that do not die are less prolific, and the followed-up as well as serologically tested, biopsied, PCRed
hatching and development rates are reduced, and there and blood sampled for culture for several weeks. Untreated
will eventually be no further new flea generations. dogs served as controls to confirm pathogen infection.
• Chitin synthesis inhibitors affect female insect fecundity Another way to demonstrate the reduction in pathogen
and prolificacy and inhibit egg hatching and larval moult- transmission is by field surveys where the rate of infection
ing. In veterinary medicine, these molecules are used in in control dogs and regularly treated dogs living in enzootic
the environment (flufenoxuron) or directly on the animal areas are compared. This has been used to assess the reduced
(lufenuron). Lufenuron acts systemically. It is either admin- risk of canine monocytic ehrlichiosis, canine leishmaniosis,
istered by subcutaneous injection or orally and is stored in or several pathogens at the same time.
fat tissues or fixed to plasma proteins.
Reasons for treatment failure
Use of insecticides/acaricides to No cases of confirmed resistance to recent external antipar-
treat and prevent both ectoparasite asitic drugs against ectoparasites in carnivores have been
infestation and arthropod-borne described. All follow-ups performed when failures were sus-
pathogen transmission pected highlighted many other reasons for the failure.
The ectoparasites of pets can be divided into two groups: Failures in tick or flea control must first be attributed to
ones that induce disease, are diagnosed and should be treat- ecological and biological factors. The high level of environ-
ed; and ones that represent a continuous nuisance and a mental tick infestation can often explain why infestations
threat as pathogen vectors. keep recurring in carnivores. Apart from Rhipicephalus san-
Many mites, such as Demodex, Otodectes, Notoedres, guineus, which usually infests dogs, ticks are fairly non-spe-
Sarcoptes and Cheyletiella species are found in the first cific and feed on many hosts: birds, rodents, insectivores,
group. There are no preventive measures available against deer, wild boar, etc. The reservoir host is very important, and
these mites and dogs and cats are treated after a veterinary ticks are not subject to antiparasitic pressure. Acaricides used
diagnosis. There is no need for long-lasting protection against in carnivores have a certain speed of kill so it is still possible
these parasites, so molecules/formulations that include them to see attached and engorging ticks on regularly treated dogs.
in their spectrum of activity are used. Active ingredient release may have been irregular on the
Fleas, sandflies, mosquitoes and ticks are in the second dog’s body, or the concentration may have been reduced by
group. They may induce clinical signs like itching, hair loss frequent shampooing. The dog’s weight might have been un-
It is easier to question the efficacy of antiparasitic treat- • Development of combination drugs to either cover a broad-
ments than to seek the true cause and explain control meas- er spectrum or improve properties such as speed of action,
ures in relation to flea and tick biology to pet owners. inhibition of attachment or repellency.
• Research into new insecticidal families with different
Conclusion modes of action and likely to be used in new formulations,
External antiparasitic drugs have evolved in recent years such as oral insecticide formulations.
with the development of new active ingredients and formu- • Increased protection to reduce the risk of arthropod-borne
lations. Older molecules are still being used, mainly due to pathogen transmission.
their low cost. The number of external antiparasitic drugs
available on the market has increased in the past 10 years, Vaccines against ectoparasitosis still do not exist and exter-
with some clear tendencies: nal antiparasitic drugs will probably remain the main thera-
• Introduction of many generic products. peutic and preventive solution for many years to come.
Improvements in external and internal antiparasitic drugs are compare the product with its competitors. The repellent effect,
not only achieved through research into new active ingredients prevention of attachment, and inhibition of blood feeding in
but the dosage form and innovative pharmacokinetic properties haematophagous arthropods are also assessed.
are also undoubtedly part of the success of these drugs. There Powders, aerosols, shampoos and lotions are generally short-
are several objectives: acting (less than a week) but spot-ons are designed for long-
• Ease of administration to pets with minimal handling. lasting effects, at least for fleas and ticks. They represent a large
• Long-term efficacy to avoid repeat treatments and to evolve part of the external antiparasitic drugs available for domestic
from the concept of cure to that of prevention. carnivores. They are based on the pharmacological properties
of active ingredients and excipients which enables transdermal
• A broad spectrum of activity.
delivery followed by plasma distribution for some, and diffusion
• A high level of safety for both animal and owner. across the entire skin due to the lipophilic properties of others.
Active ingredients remain in the sebum and the sebaceous
The parasiticidal properties of all formulations must be assessed glands for several weeks. Studies involving radiolabelling of active
by controlled experimental and field trials. Some guidelines are ingredients using hair clippings and skin samples (biopsies) help
defined by drug agencies: the European Medicines Agency in to demonstrate the cutaneous pharmacokinetics of these spot-ons.
Europe, and the Environmental and Pesticide Agency, or Food They must be applied to dry skin for optimal effectiveness, and it
and Drug Administration in the United States, and occasionally is therefore best not to wash the animal just before application,
by scientific associations, such as the World Association for the which enables the skin’s lipid film to rebuild. Regular shampooing
Advancement of Veterinary Parasitology. will remove the active ingredients and reduce their persistence.
Studies help to define the spectrum of activity, the speed of action Some active ingredients used in spot-on formulations act on
against existing infestation (curative effect), or against reinfestation contact with the arthropod; others are systemic and/or mixed
(preventive effect) and the duration (sustained effect). They are in their mode of action, with transcutaneous penetration and
also useful to assess effects on immature stages (eggs, larvae), plasma circulation. The molecules formulated as tablets act
prolificacy in females or inhibition of reproduction. These studies, systemically and may have a short-term effect or a persistent
which have many different designs, are first conducted to licence efficacy. Oral palatable formulations have recently taken
the product, but many are carried out after the product launch, to a large part of dog ectoparasiticides. Collars are made of
refine some points, such as the speed of kill for existing infestation, plastic polymers, the matrix of which is impregnated with the
the sustained speed of kill for new infestation, inhibition of egg insecticide/acaricide. Rubbing of the collar against the skin
production and new generation emergence and, of course, to releases the active ingredients continuously and gradually.
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CONTENTS Ectoparasiticides 379
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The effect of any insecticidal/acaricidal product is assessed in usually by a minimum number of arthropods: 50 ticks (25 males
relation to the time post infestation. Performance is evaluated and 25 females) or 100 fleas, and it may be repeated (usually
either in the crate/cage or on the animal itself, according to the weekly).
study design. Treatments may be applied before (usually 24–48 hours)
A control group is always required to be sure that the infestation infestation (to assess any preventive effect) or after (to assess
process is normal and the comparisons and calculations are any curative effect). The arthropods are counted on the animal
always made between treated and control groups. by thumb counting (they remain on their host, which allows
Arthropod infestation may be achieved by directly placing the successive counts on the same host) or removal counts.
arthropods on the animal (the classic method for fleas and When dealing with fleas, flea eggs can be collected on the
ticks) or by placing them in a crate/cage/box/under a net where ground 12–36 hours after infestation in order to assess the
a sedated animal will be placed later (the classic method for impact of the treatment on female prolificacy, egg viability and
mosquitoes, phlebotomes, flies and some ticks). Infestation is the rate of development into new fleas.
Anti-attachment
Alive free on the animal Not repelled/expelled Killing effect not demonstrated
Arthropod effect considered
status Killing effect demonstrated.
Anti-attachment Depending on the timing of the
Dead free on the animal Not repelled/expelled
On the dog effect considered counts, speed of kill can be
or cat determined
Dead attached to the dog No anti-
Killing effect demonstrated
(applicable to ticks only) attachment effect
APPENDICES
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General definitions
Parasites, predators, commensals and symbionts
• Parasites are living organisms (animal or plant) that develop at the expense of another living organism (the
host), sometimes causing its death.
Parasite • A parasite is therefore defined by its relationship with other living beings, and must be distinguished from
animals or plants with different relationships, such as predators, commensals, saprophytes, saprobes,
symbionts and parasitoids.
Predator • Predators are living beings that develop by destroying other living beings, their prey.
• A commensal is an organism that depends on another organism for its development, but the relationship
is not harmful to the host as it is in parasitism: it is mutually beneficial.
• For example, certain protozoa (unicellular organisms) live commensally in the digestive tracts of
herbivores, where conditions are suitable for their nutrition and reproduction (food supply, temperature,
Commensal
pH, etc.).
In return, they allow cellulose to be digested and ensure that water-soluble vitamins, especially vitamin B,
can be produced. Some other organisms also perform this function.
• Commensal Trichomonas can be observed in the digestive and genital tracts of carnivores.
• When the positive relationship between the commensal and host becomes essential for development
of the host and survival of the parasite this is known as symbiosis, and the two organisms are called
symbionts.
Symbiont
• For example, some ciliate protozoa in termite digestive tracts are symbionts. These protozoa themselves
harbour symbiotic bacteria, and allow the termites to digest wood.
• Some fungi associate with algae to create lichens.
• When an organism lives off another without negative (parasitic) or positive (symbiotic) effects, it is called
a saprophyte.
Saprophyte/Saprobe • Some authors restrict the term “saprophyte” to plants, using the word “saprozoite” for animals.
• The single term “saprobe” has been proposed and is particularly suitable for fungi, which are currently
considered to belong to a kingdom between animals and plants.
• There is one other relationship, hyperparasitism, which is linked to parasitoid organisms.
These feed at the expense of their host and inevitably cause its death. Numerous arthropod larvae exhibit
this parasitoid behaviour.
Hyperparasite
• For example, Hymenoptera larvae of the Ichneumonidae family (adults of which resemble wasps) develop
on or in certain arthropods (caterpillars, ticks) and cause the death of the host during transformation of
the larvae into adults by pupation.
Major parasitoses
of dogs and cats
Dogs Cats
• Ascaridoses
• Ascaridoses (Toxocara cati, Toxascaris leonina)
(Toxocara canis, Toxascaris leonina)
• Hookworms (Uncinaria stenocephala,
• Hookworm infestation (Uncinaria stenocephala,
Ancylostoma tubaeforme)
Ancylostoma caninum)
• Ollulanosis (Ollulanus tricuspis)
Intestinal helminthoses • Trichuriosis (Trichuris vulpis)
• Teniosis (Taenia taeniaeformis, Dipylidium
• Strongyloidosis (Strongyloides stercoralis)
caninum, Mesocestoides, Diphyllobothrium
• Teniosis (Taenia spp., Dipylidium caninum,
and Spirometra species, Echinococcus
Mesocestoides, Diphyllobothrium, Spirometra,
multilocularis)
Echinococcus spp.)
• Giardiosis (Giardia duodenalis)
• Giardiosis (Giardia duodenalis)
Intestinal protozooses • Coccidiosis (Isospora, Toxoplasma, Hammondia,
• Coccidiosis (Isospora, Neospora species)
Besnoitia species)
• Respiratory strongyloses • Respiratory strongyloses
Respiratory parasitoses (Oslerus osleri, Crenosoma vulpis) (Aelurostrongylus abstrusus, Troglostrongylus)
• Capillariosis • Capillariosis
• Babesiosis (Babesia canis)
Blood parasitoses • Babesiosis and cytauxzoonosis (Cytauxzoon felis)
• Hepatozoonosis
• Dirofilariosis (Dirofilaria immitis) • Dirofilariosis (Dirofilaria immitis)
Cardiovascular parasitoses
• Angiostrongylosis (Angiostrongylus vasorum) • Aelurostrongylosis (Aelurostrongylus abstrusus)
General parasitosis • Leishmaniosis (Leishmania infantum)
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Appendices 385
CONTENTS
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Arthropods and
vector-borne diseases
Arthropods and the pathogens they transmit in humans or animals
Parasites listed in purple are the main helminths found in dogs and cats.
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Parasites listed in purple are the main cestodes and trematodes found in dogs and cats.
TABLE OF
Appendices 395
CONTENTS
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Parasites listed in purple are the main protozoa found in dogs and cats.
TABLE OF
Appendices 397
CONTENTS
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Phylum Arthropoda
Parasites listed in purple are the main arthropods found in dogs and cats.
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Suborder Anoplura
Head thinner than thorax. Antennae in five segments.
• Family Pediculidae: Pediculus humanus (var. capiti and
var. corporis), Phtirius pubis.
• Family Haematopinidae: Haematopinus, Linognathus,
Solenopotes.
Suborder Mallophaga
Head wider than thorax.
• Family Trichodectidae: Trichodectes canis, Felicola
subrostratus, Bovicola.
• Family Gyropidae: Gyropus, Gliricolla.
• Family Boopidae:
Heterodoxus spiniger.
• Family Menoponidae: Menopon.
• Family Philopteridae: Goniodes, Lipeurus,
Columbicola.
MAIN PARASITES
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Eyeworms
OF THE DOG
Subcutaneous worms Coccidia
Giardia
Walking dandruff
Ticks Mange mites
Whipworms
Fleas Oesophageal worms
Demodex mites
Stable flies
Lungworms
Sandflies
Bladder worms
Mosquitoes Heartworms
Roundworms
Hookworms
Liver flukes
DOG ENDOPARASITES
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Trypanosoma
Mesocestoides Liver flukes Trypanosoma spp.
Oesophageal worms Threadworms Eyeworms Bladder worms tapeworms Opisthorchis spp., Giardia Macrophages
Spirocerca lupi Strongyloides stercoralis Thelazia callipaeda Capillaria plica Mesocestoides spp. Clonorchis sinensis Giardia duodenalis and muscle cells
Oesophagus Small intestine Eyes Urinary tract Small intestine Liver Small intestine
The sizes of the illustrations are not representative of actual parasite size.
DOG ECTOPARASITES
Insects Acarids
Ticks
Demodex mites
Ixodes spp., Haemaphysalis spp., Ear mites
Demodex canis
Rhipicephalus sanguineus, Otodectes cynotis
Dermacentor spp. Entire body, especially
Ears
face and legs
Entire body
Mosquitoes
Flesh flies Stable flies Sandflies Aedes spp.,
Calliphora spp. Stomoxys calcitrans Phlebotomus spp. Culex spp.
Hair and wounds Blood sucking Blood sucking Blood sucking
MAIN PARASITES
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OF THE CAT
Ear mites Demodex mites
Roundworms
Mosquitoes
Hookworms
Tritrichomonas
Coccidia
Eyeworms
Chiggers
Babesia
Dipylidium tapeworms
Echinococcus tapeworms
Broad tapeworms
Mesocestoides tapeworms
CAT ENDOPARASITES
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The sizes of the illustrations are not representative of actual parasite size.
CAT ECTOPARASITES
Insects Acarids
Ticks
Ixodes spp., Ear mites Demodex mites
Haemaphysalis spp., Otodectes cynotis Demodex cati
Rhipicephalus spp. Ears Head, neck
Head, neck, ears
Walking Chiggers
Mange mites
Fleas Chewing lice dandruff Trombicula autumnalis
Notoedres cati
Ctenocephalides felis Felicola subrostratus Cheyletiella blakei
Entire body Head, neck, feet
Entire body Face, ears, back Back and upper body
Sandflies Mosquitoes
Phlebotomus spp. Aedes spp.
Exposed skin Exposed skin
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ALPHABETICAL
INDEX
TABLE OF
Alphabetical index 405
CONTENTS
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Dirofilariosis 112, 119, 122, 125, 126, 127, 131, 132, Hepatozoon 111, 112, 113, 114, 115, 116, 248, 365,
341, 350, 355, 384 389, 390, 396, 400, 401
Distomes 60, 394, 395 Hepatozoonosis 111, 112, 114, 116, 365, 384
Heterodoxus 221, 222, 399
Heterophyidae 60, 62, 395
E Heterophyidosis 63
Echinochasmus 61, 62, 63, 395 Holostomes 61, 394, 395
Echinococcosis XVIII, 49, 50, 52, 53, 54, 55, 383, 406 Hookworms 14, 15, 18, 33, 291, 302, 323, 344, 350,
Echinococcus 40, 43, 48, 49, 51, 52, 53, 54, 55, 192, 351, 352, 353, 354, 355, 356, 383, 384, 400, 401,
290, 312, 314, 325, 328, 330, 339, 344, 353, 356, 402, 403
384, 386, 387, 394, 400, 401, 402, 403 Hydatidosis 49, 54, 55
Echinostomatidae 61, 62, 395
Echinostomatidosis 63
I
Encephalitozoon 188, 189
Encephalitozoonosis 188 Isospora 67, 68, 71, 72, 73, 74, 175, 176, 177, 182,
Eucoleus 34, 150, 393 311, 318, 319, 327, 333, 334, 344, 384, 387, 396
Euparyphium 61, 395 Ixodes 96, 236, 237, 238, 239, 240, 241, 242, 243, 245,
Eurytrema 60, 62, 395 247, 249, 250, 252, 345, 373, 377, 385, 389, 390,
Eutrombicula 278 398, 401, 403
F J
Felicola 221, 222, 224, 277, 345, 385, 399, 403 Joyeuxiella 35, 36, 38, 310, 314, 394
Filaroides 137, 138, 139, 392
Flea infestation 210, 211, 215, 218, 220, 373
Fleas 38, 40, 108, 125, 196, 198, 210, 211, 212, 214, L
215, 216, 218, 219, 220, 225, 265, 342, 343, 345, Leishmania 114, 166, 167, 168, 169, 170, 171, 173,
355, 357, 369, 372, 373, 374, 375, 376, 377, 378, 174, 219, 244, 341, 362, 363, 384, 389, 396, 400,
379, 383, 385, 386, 387, 389, 398, 400, 401, 402, 401, 402, 403
403 Leishmaniosis 17, 111, 112, 119, 166, 169, 170, 171,
Flying insect bites 230 172, 174, 201, 219, 257, 363, 364, 377, 384
French heartworm 132 Leptopsylla 210
Lice 38, 125, 221, 222, 223, 224, 225, 241, 265, 291,
342, 345, 355, 374, 375, 376, 383, 385, 386, 387,
G 389, 399, 400, 401, 402, 403
Giardia 75, 76, 77, 78, 79, 80, 82, 83, 84, 290, 293, Lice infestation 221, 225, 385
311, 318, 327, 333, 344, 355, 357, 362, 363, 384, Linguatula 152, 153
387, 396, 400, 401, 402, 403 Linguatulosis 152, 153, 376
Giardiosis 75, 77, 78, 79, 355, 358, 363, 384, 387, 388 Linognathus 221, 345, 385, 399, 401
Glossina 117, 119, 398 Lucilia 226, 227, 229, 398
Gnathostoma 5, 7, 10, 11, 392 Lutzomyia 231, 233, 389, 398
Lynxacarosis 284
Lynxacarus 284, 285, 342
H
Haemaphysalis 96, 98, 236, 237, 239, 242, 245, 249,
M
251, 252, 373, 385, 389, 390, 398, 401, 403
Haematobia 230, 374, 398 Mesocestoides 41, 42, 194, 195, 310, 312, 314, 324,
Hammondia 67, 68, 70, 71, 72, 73, 175, 182, 311, 320, 326, 328, 330, 338, 357, 384, 386, 394, 400, 401,
327, 334, 344, 384, 396, 401, 403 402, 403
Heartworms 128, 353, 400, 401, 402, 403 Mesocestoididae 43, 394
Mesocestoidosis 41, 42
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P T
Paragonimoses 148 Tabanus 230, 398
Paragonimosis 63 Taenia 40, 42, 43, 44, 45, 46, 47, 48, 49, 54, 55, 56,
Paragonimus 60, 63, 148, 149, 395 192, 193, 194, 218, 292, 312, 314, 324, 328, 330,
Phlebotomus 166, 169, 231, 233, 374, 389, 398, 401, 338, 344, 351, 353, 356, 357, 383, 384, 386, 387,
403 394, 400, 401, 402, 403
Phortica 200, 202 Taeniidae 43, 49, 192, 310, 314, 326, 330, 344, 383, 394
Physaloptera 5, 10, 11, 293, 304, 392 Taeniosis 35, 43, 46, 49, 219, 383, 384, 387
Piroplasmosis 98, 101, 102, 103, 104, 106, 109, 365 Theileria 96, 97, 98, 100, 104, 106, 108, 111, 248, 365,
Platynosomum 60, 62, 395 389, 396, 401
Pneumonyssoides 154, 155, 397 Theileriosis 96
Pneumonyssoidosis 154 Thelazia 200, 201, 202, 352, 393, 401, 403
Pulex 210, 385, 389, 398 Thelaziosis 200, 201, 202
408 TABLE OF
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Ticks 96, 98, 100, 107, 108, 111, 112, 113, 116, 125,
196, 198, 236, 237, 238, 239, 240, 241, 242, 243,
245, 246, 247, 248, 249, 253, 278, 342, 343, 345,
369, 370, 372, 373, 374, 375, 376, 377, 378, 379,
382, 383, 385, 389, 397, 398, 400, 401, 402, 403
Toxascaris 18, 19, 20, 23, 24, 25, 26, 292, 310, 312,
315, 323, 326, 328, 331, 337, 344, 352, 354, 355,
384, 386, 391, 401, 403
Toxocara 15, 18, 19, 20, 21, 22, 25, 26, 290, 292, 310,
312, 315, 323, 326, 328, 331, 337, 344, 352, 354,
357, 384, 386, 391, 401, 403
Toxocarosis 17, 18, 24, 25, 29, 39, 337, 387, 388
Toxoplasma 67, 68, 71, 72, 73, 114, 175, 176, 177,
178, 180, 181, 182, 183, 184, 327, 334, 344, 363,
384, 396, 403
Toxoplasmosis 72, 175, 176, 177, 180, 181, 182, 183,
184, 363
Trematodes 60, 61, 62, 63, 148, 149, 304, 310, 326,
353, 355, 356, 394, 401, 403
Triatoma 117
Trichinella 203, 204, 205, 393
Trichinellosis 203, 204, 205
Trichodectes 221, 222, 224, 345, 385, 399, 401
Trichomonosis 80, 81, 83, 363, 388
Trichuriosis 17, 30, 32, 384, 387, 388
Trichuris 18, 30, 31, 33, 136, 158, 290, 310, 315, 317,
332, 344, 354, 355, 357, 384, 386, 393, 401
Tritrichomonas 80, 81, 82, 83, 293, 396, 402, 403
Troglostrongylosis 141, 142, 145
Troglostrongylus 141, 142, 145, 146, 147, 384, 392
Troglotrematidae 60, 63, 148, 395
Trombicula 278, 279, 280, 385, 397, 401, 403
Trombiculosis 257, 262, 277, 278, 279, 280, 282, 287,
385
Trypanosoma 117, 118, 119, 340, 364, 389, 396, 400,
401
Trypanosomosis 117, 118, 119, 364
U
Uncinaria 14, 15, 16, 17, 18, 310, 316, 326, 331, 344,
354, 355, 357, 384, 386, 388, 391, 401
W
Whipworms 18, 30, 151, 323, 350, 351, 352, 354, 355,
356, 357, 400, 401
Wohlfahrtia 226, 229, 398
X
Xenopsylla 210, 398
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CONTENTS
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K
Keratitis 118, 172, 189, 200, 201
TABLE OF
Alphabetical index 411
CONTENTS
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SELECTED
BIBLIOGRAPHY
The objective of this book is educational, and it is aimed at students and veterinarians.
It is impossible to propose an exhaustive list of references: selecting particular articles would
lead to many omissions, and listing pages of references would not be helpful.
These days, it is easy to find papers published on precise scientific veterinary topics, and it
seems that searching the internet is finally more common than looking at listings on paper.
We therefore decided to provide a restricted list of references, including published scientific
books that themselves contain bibliographies, and only a few reviews.
Acha, P.N. and Szyfres, B. Zoonoses et maladies transmissibles communes à l'homme et aux
animaux. 3rd edition, OIE, 2005, Volume I 382 p., Volume II 405 p., Volume III 399 pp.
Ackermann, L. Atlas of Small Animal Dermatology. Ed. Intermedica, Argentina, 2008, 510 pp.
Beaucournu, J.C. and Launay, H. Les puces de France et du Bassin méditerranéen occidental.
Faune de France 76. Ed. Fédération Française des Sociétés de Sciences Naturelles, 1990, 550 pp.
Beugnet, F. and Franc, M. Insecticide and acaricide molecules and/or combinations to prevent
pet infestation by ectoparasites. Trends in Parasitology, 2012, 28(7): 267–279.
Beugnet, F. et al. Guide to Vector Borne Diseases of Pets. Ed. Ferreol, Lyon, France, 2013, 425 pp.
Beugnet, F. Helminthoses digestives des Carnivores domestiques. Encyclopédie Médico-Chiru-
rgicale Vétérinaire, Elsevier SAS, 2010, 0300, 31 pp.
Beugnet, F., Dang, H. and Bourdoiseau, G. Abrégé de Parasitologie Clinique des Carnivores
Domestiques - Volume 1 - Parasitoses Digestives. Ed Kalianxis, Paris, 2004, 266 pp.
Beugnet, F., Dang, H. and Bourdoiseau, G. Abrégé de Parasitologie Clinique des Carnivores
Domestiques - Volume 2 - Parasitoses Internes Non Digestives. Ed. Kalianxis, Paris, France,
2006, 233 pp.
Beugnet, F., Halos, L. et al. Parasitoses and Vector Borne Diseases of Cats. Ed. Ferreol, Lyon,
France, 2015, 381 pp.
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