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Bovine retained placenta: Aetiology, pathogenesis and economic loss

Article  in  The Veterinary record · December 1996


DOI: 10.1136/vr.139.19.465 · Source: PubMed

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The Veterinary Record, November 9, 1996 465

neonatal period. The absence of any significant independent asso- DEAN, A. D., DEAN, J. A., BURTON, A. H. & DICKER, R. C. (1990) Epi Info,
ciation between the lambs' immunoglobulin status and faecal soil- Version 5: a word processing, database, and statistics program for epidemiology
on micro-computers. USD
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immunity were negligible in the two- to six-month-old lambs, or, Record 131, 337
alternatively, because the high mortality among the neonates with FRENCH, N. P., WALL, R. & MORGAN, K. L. (1994) Veterinary Record 134,463
low immunoglobulin levels removed many of this potentially high FRENCH, N. P., WALL, R. & MORGAN, K. L. (1995) Medical and Veterinary
Entomology 9, 1
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This study has identified a number of associations between Veterinary Research 50, 792
neonatal and maternal risk factors and the rate of the development GRAHAM, N. P. H., JOHNSTONE, I. L. & RICHES, J. H. (1947) Australian
of faecal soiling in lambs. Further studies are needed before any Veterinary Journal 23, 31
GRAY, G. D. (1991) Breeding for Resistance in Farm Animals. Eds J. B. Owen, R.
firm recommendations for preventing faecal soiling can be made. F. E. Axford. Wallingford, CAB International
Reducing the level of faecal soiling in sheep flocks could not only GREEN, L. E. & MORGAN, K. L. (1994) Preventive Veterinary Medicine 21, 19
benefit the meat and wool industry, but also have major implica- MITCHELL, G. & LINKLATER, K. (1983) Veterinary Record Supplement In
tions in the control of flystrike and reduce the need to dag, crutch Practice 5, 4
NEWTON, K. G., HARRISON, J. C. L. & WAUTERS, A. M. (1978) Journal of
and dock lambs' tails. Applied Bacteriology 45, 75
PARE, J., THURMOND, M. C., GARDNER, I. A. & PICANSO, J. P. (1993)
Canadian Journal of Veterinary Research 57, 241
Acknowledgements. - Many thanks are due to the eight farmers RAADSMA, H. W. (1993) Australian Journal ofAgricultural Research 44, 915
involved in the study, Geoff Werret, the veterinary investigation SCOTT, W. N. (1978) The Care and Management of Farm Animals. 2nd edn.
centre at Langford, David Harbour, Hidayet Erdogan, Laura London, Bailliere Tindall. p 96
SUSSER, M. (1981) American Journal of Clinical Nutrition 34, 784,
Green, Dilip Patel, Tim Parkin and Galip Kaya. The project was VICTORIA, C. G., BARROS, F. C., VAUGHAN, J. P. & TEIXEIRA, A. M. B.
funded by the Wellcome Trust. (1987) International Journal of Epidemiology 16, 239
WARDHAUGH, K. G., VOGT, W. G., DALLWITZ, R. & WOODBURN, T. L.
(1989) General and Applied Entomology 21, 11
WATTS, J. E. & MARCHANT, R. S. (1977) Australian Veterinary Journal 53, 118
References WATTS, J. E. & PERRY, D. A. (1975) Australian Veterinary Journal 51, 586
BISSETT, S. A., VLASSOFF, A., MORRIS, C. A., SOUTHEY, B. R., BAKER, R. L. YAPI, C. V., BOYLAN, W. J. & ROBINSON, R. A. (1990) Preventive Veterinary
& PARKER, A. G. H. (1992) New Zealand Journal ofAgricultural Research 35, 51 Medicine 10, 145

Review Article
Bovine retained placenta: aetiology, pathogenesis
and economic loss
R. A. Laven, A. R. Peters
Veterinary Record (1996) 139, 465-471 tion is the presence of fetal membranes 24 hours or more post par-
tum (Esslemont and Peeler 1993), but retention for more than six
The literature on the effects and causes of retained placenta in hours is probably a better definition, particularly in older cows
the cow is reviewed. On a herd basis the condition can (van Werven and others 1992).
adversely affect milk yield and fertility, but on an individual The cow and the water buffalo (Bubalus bubalis) are the only
cow basis the effects are unpredictable. The aetiology of domestic ruminants in which retained placenta is a routine abnor-
retained placenta has been extensively studied and many mality. It affects other ruminants less frequently with little evi-
causal factors have been implicated, but little is known of how dence of associated problems. Estimates of the incidence of
many of them cause the condition. As a result its prevention retained fetal membranes in the cattle population vary widely,
and prediction is uncertain, primarily because of the lack of partly depending upon the definition used, but also on the country
knowledge of the normal process of placental release. of origin of the report, with tropical pastoral systems apparently
Vascular changes and uterine contractions play a role in pla- having higher rates (Table 1). The incidence in the United
cental release, but current opinion suggests that the primary Kingdom after normal calving is usually quoted at around 4 to 8
cause of retained placenta is the retention of the feto-maternal per cent (Esslemont and Peeler 1993, Arthur and others 1995), but
union. Release only occurs after a process of maturation, in many herds the incidence is much higher.
which involves hormonal and structural changes. The factors
which are thought to influence these changes, and thus cause
the condition, are discussed. The effects of retained placenta

LOSS of the placenta in the cow occurs during the third stage of Reduction in milk sold
parturition, the process of separation usually taking less than six
hours (Roberts 1986). Thus the placenta is normally retained until This is thought to occur in two ways: first, in some countries,
after the birth of the calf and a pathologically retained placenta is including the UK, milk from cows with retained placenta cannot be
difficult to define. The time scales used range from six to 71 hours sold for human consumption. Thus retention for more than 96
(van Werven and others 1992). The most commonly used defini- hours leads to a monetary loss even if milk production is appar-
ently normal. Secondly, 55 to 65 per cent of cows with retained
placenta have a reduced appetite (Arthur and others 1995). Loss in
yield is said to be more pronounced in the 20 to 25 per cent of
R. A. Laven, BVetMed, MRCVS, A. R. Peters, DVetMed, PhD, BA, FRCVS, cases that exhibit moderate to severe symptoms of metritis
Department of Farm Animal and Equine Medicine and Surgery, Royal (Roberts 1986), though this extra loss is probably less than that
Veterinary College, Boltons Park Farm, Hawkshead Road, Potters Bar due to the retained placenta alone (Simerl and others 1992).
EN6 1NB Despite these effects, several studies have shown that the condi-
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466 The Veterinary Record, November 9, 1996

TABLE 1: Published estimates of the incidence of retained placenta in ty of subsequent metritis and thus the apparent effect of retained
different countries placenta on fertility; and reduced fertility expectations can mask
Definition by deleterious effects, for example Palmer (1932) found no effect of
retention Incidence the condition on the calving interval, but the cows were not served
Country time (hours) (%) Reference until 90 days post partum. Individual variations in the effect of the
UK >24 3.8 Esslemont and Peeler (1993)
condition are pronounced. Erb and others (1958) found that the
USA >24 7.7 Muller and Owens (1974) fertility of 60 per cent of cows with retained placenta was similar
Israel >24 8.4 Ben-David (1968) to that of the rest of the herd, but that the remaining 40 per cent
India NS 8-86 Pandit and others (1981) had considerably lower fertility.
Sweden >24 7.7 Bendixen and others (1987)
Bangladesh >12 39 Samad and others (1989)
Iraq NS 12.8 Majeed and others (1991)
Tunisia >24 15 Zaiem and others (1994) Other losses
Ireland >12 4.06 Mee (1991)
Saudi Arabia NS 6-3 Arthur and Abdul-Rahim (1984) Veterinary treatment, including subsequent milk withdrawal, is
New Zealand >12 2.0 Moller and others (1967)
Indonesia >12 30 Putro (1989) a further cause of economic loss. Despite veterinary treatment, the
mortality (usually due to severe toxic metritis) can approach 4 per
NS Not stated cent (Arthur and others 1995) adding further to the losses.
Esslemont and Peeler (1993) calculated that, on average, each
tion has no effect on milk production (Kay 1978, Martin and oth- case costs £239.79. Applying this figure to an incidence of 4 per
ers 1986) and one study claimed that it can be associated with an cent the condition costs the UK dairy industry more than £25 mil-
increase in milk yield (Muller and Owens 1974). Such results are lion per year. It is an important reproductive disease which causes
probably due to looking at the total milk yields achieved, rather considerable economic loss at the herd level.
than comparing lactation curves (Lucey and others 1986), but not
all cows with the condition will have a significantly reduced milk
yield. Aetiology of retained placenta
Many factors have been implicated in the production of retained
Reduction infertility placenta; some are shown in Table 2. Many of them are interrelat-
ed; for example, high environmental temperatures, twin pregnan-
The consequences of retained placenta are an increase in calv- cies and hydrops amnion may all lead to the condition by causing
ing to first service interval, a reduction in pregnancy rate to first premature birth, but others are seemingly contradictory; for exam-
service, an increase in the number of services per conception and ple, Trinder and others (1969) reduced the incidence of retained
consequently a longer calving interval (Fung 1983, Halpern and placenta by selenium supplementation whereas Yde Blom and oth-
others 1985, Heinonen and Heinonen 1989). ers (1984) increased it. Factors responsible for the condition on
The condition is thought to reduce fertility in two ways: first, one farm will not always cause an increase in its incidence on
by a direct effect through an unknown mechanism and secondly, another. In many cases despite extensive study no cause can be
by an indirect effect as a major component in the pathogenesis of found for increases in the incidence of retained placenta.
metritis which is usually associated with a deleterious effect on The significance of each factor on a herd basis is difficult to
fertility (Mellado and Reys 1994). assess; as a result preventive techniques are limited to broad mea-
sures such as providing adequate nutrition and the reduction of
The direct effect. The magnitude of this effect varies widely
- peripartum stress. Pre-partum blood sampling, for example for
from study to study. Borsberry and Dobson (1989) and Erb and selenium or beta-carotene, may be useful in some herds, but in
others (1981) have found that uncomplicated retained placenta can many cases will be of no benefit. The lack of ability to prevent or
lead to an increase in calving interval. However, other studies predict the condition is primarily due to the paucity of knowledge
have shown no direct effect of the condition on fertility (Sandals of the normal placental separation process. Gunnink (1984) could
and others 1979, Nakao and others 1992). find no reports of basic research on the process of placental sepa-
ration and little has changed since then.
The indirect effect. There is a very close association between
-

retained placenta and the development of metritis, which may be


up to 19 times more likely than after a normal calving (Curtis and The bovine placenta
others 1985). This increase in metritis is thought to be the major
route by which the condition affects fertility. However, not all The bovine placenta is synepitheliochorial (Wooding 1992)
studies of metritis do show a deleterious effect on fertility; with three identifying characteristics. First, a large number of bi-
Etherington and others (1985) found improved fertility (a reduc- nucleate cells in the fetal trophectoderm; these cells have an ultra-
tion in days to first service and days open) after post partum structure different from the surrounding uninucleate cells.
metritis associated with systemic signs, and Dohoo and Martin Secondly, the formation, at the beginning of implantation, on the
(1984) found no effect on breeding performance of reproductive maternal side of the placentome, of a syncytium; this is produced
tract infections diagnosed less than 22 days post partum (the type by the fusion between binucleate cells, which migrate across the
usually linked to retained placenta). feto-matemal junction, and the maternal endometrium. However,
in the cow, unlike the sheep and goat, this syncytium is only tem-
The overall effect. Although retained placenta is said to have
-
porary because once the binucleate cells release their granules
direct and indirect effects on fertility, many studies, using both they are resorbed and the syncytium is overgrown by the rapid
induced and natural retentions, show a lack of effect on fertility. division of the maternal epithelium (King and others 1979).
O'Farrell and Langley (1975), Bolinder and others (1988) and Binucleate cells continue to migrate throughout pregnancy but
Garcia and others (1988) all found that retained placenta produced form only transient trinucleate cells in the maternal epithelium
by early induction of parturition had no effect on subsequent fer- (Wooding and Wathes 1980). Thirdly, the bovine placenta has a
tility. Studies by Muller and Owens (1974), Shanks and others cotyledonary chorio-allantoic organisation with villus develop-
(1977) and Gwazduaskas and others (1979) all found similar ment restricted to discrete regions of non-glandular uterine epithe-
results after spontaneous retained placenta. Such apparent contra- lium.
dictions occur because conception is a complex process and many
factors can interact to increase or reduce fertility. For example, The anatomy of separation. - The delivery of the placenta post
differences in herd management can have profound effects on fer- partum is a physiological process, involving the loss of feto-
tility; unhygenic conditions can increase the incidence and severi- maternal adherence, together with uterine muscular contractions
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The Veterinary Record, November 9, 1996 467

TABLE 2: Some of the factors associated with retained placenta in other histological studies of separation (Gross and others 1987);
Factor Effect
their source is unclear and their function and significance are
unknown.
Breed Ayrshires more susceptible (Erb and Martin 1978) Further suggested changes include the obliteration of blood ves-
Year Herd incidence varies from year to year (Larson and others sel lumina by the hyalinisation of their walls and the proliferation
1985) of connective tissue (Grunert 1984). However, there is no evi-
Season Summer temperatures increase rate (Dubois and Williams dence for increased hyalinisation (Sharpe and others 1989).
(1980). Highest incidence in spring (Wetherill 1965) Maturation also involves the swelling of the maternal connective
Herd Great inter-herd variability (Roberts 1986) tissue by the absorption of water by the connective tissue cells.
Length of Prolonged and shortened gestation increase incidence
These changes were thought to be dependent on increasing con-
gestation (Muller and Owens 1974) centrations of oestrogen (Grunert and others 1989), but the pre-
Induction High incidence after use of corticosteroids or PGs (Zerobin partum placentome is not sensitive to oestrogens (Sauerwein and
and others 1973, Peters and Poole 1992) others 1989).
Dystocia Incidence up to 55 per cent (Vandeplassche and Martens
After maturation the constantly changing uterine pressure fur-
1961) ther impairs the feto-matemal junction. The rupture of the umbili-
Hypocalcaemia Both linked to linolenic acid-rich diets (Barnouin and
cal cord leads to anaemia of the fetal villi, and uterine contractions
Chassagne 1991) invert the fetal sac and expel the placenta (Arthur and others
Twins Forty per cent of cases due to twins (Erb and others 1958)
1995).
This description does not explain the loss of adhesion between
Age Rates increase with age (Erb and others 1958) the fetal and maternal epithelia. Little is known of how the fetal
Abortion Incidence greater if after 120 days (Roberts 1986) and maternal epithelia are maintained in apposition. It is now
Heredity Low but not insignificant (Distl and others 1991) thought that the acellular layer (or glueline) between the two
Fatty liver Predisposes to uterine atony and retained placenta (Morrow epithelia contains adhesive proteins and that it is a change in its
and others 1979) composition that allows placental separation. There is some evi-
Selenium/ Good response to supplementation (Julien and others 1976). dence for a chemical change in the glueline before release.
Vitamin E Over supplementation increases rate (Yde Blom and others Sections of placentome taken post partum, but before release,
1984) show that the glueline becomes more intensely stained (Bjorkman
Vitamin A Deficiency of vitamin or precursor (P-carotene) increases and Sollen 1960). Furthermore, during normal parturition small
rate (Ronning and others 1953) areas of chorionic villi remain attached to the maternal tissue, per-
Iodine Deficiency predisposes to stillbirth and retained placenta haps owing to the maintenance of adhesion, and in such sections
(Moberg 1961) there is no increase in the staining intensity (Bjorkman and Sollen
General Many factors linked to the condition from increased by- 1960). However, until the pre-partum chemical composition is
nutrition product use (Grunert 1986) to low magnesium, copper, zinc known, the changes taking place during placental release cannot
and iron (Zhang and others 1992) be elucidated.

which physically expel the placenta. Uterine motility is thus The induction of retained placenta
important but the determining factor appears to be the disengage-
ment of the fetal and maternal villi (Bjorkman and Sollen 1960). In many cases the predisposing cause of retained placenta is
Post partum collapse of the fetal-placental circulation and uncertain, as are the events inducing it; even in those cases where
reduction of the blood supply to the maternal caruncles leads to the cause is known, mechanism linking the cause and the condi-
shrinking of the villi. However, as the process occurs over a peri- tion is unclear. There have been few studies linking the histology
od of one to three hours, separation cannot be a purely vascular of the condition with the predisposing cause; most studies have
phenomenon (Roberts 1986). In sheep, the process of detachment been limited to looking at gross appearance and the ease of
is completed by the explosive degeneration of the fetal uninucle- removal, with little linking back to cause. Most commonly they
ate cells, but in the cow the majority of the chorionic villus layer divide retained placentas into two types (Hindson 1976,
is expelled intact (Steven 1975). This lack of damage to the fetal Matthijsen 1995): thin and difficult to remove, and thick and easy
membranes during their expulsion rules out the possibility of to remove. Wetherill (1965) included two further categories: a
detachment being a purely physical process; placental separation semi-liquid jelly-like mass, and tough membranes with little
therefore requires a reduction in feto-maternal adherence. putrefaction. However, except for a link between this last group
This loss of adherence is thought to occur only after the placen- and retained placenta due to abortion (also found by Bjorkman
tome has undergone a process of maturation, with maturity usual- and Sollen 1961), no link to predisposing cause has been found.
ly being reached three to five days before parturition (Grunert There are three ways in which a retained placenta can be
1984). Grunert suggested that this process involves the flattening induced: myometrial dysfunction, retention of the feto-maternal
of the maternal epithelium and collagenisation of the placentome. union and mechanical obstruction. The relative importance of the
The flattening was observed in peripartum placentomes by three is unclear. However, mechanical obstruction is apparently
Bjorkman and Sollen (1960) and leads to an apparent four-fold rare with estimates ranging from 2 per cent (Hindson 1976) to less
decrease in the number of maternal epithelial cells, partly due to than 0 5 per cent (Grunert 1984).
stretching but also to a resyncitialisation of the endometrium The estimates for myometrial dysfunction are very variable:
(Grunert 1984). However, there is no increase in total placentomal Grunert (1984) suggested that less than 1 per cent of cases were
collagen after day 270 of pregnancy (Sharpe and others 1989), caused primarily by myometrial dysfunction, but gave no data to
although there is a changeover from type I to type III collagen back up the figure. Hindson (1976), in a survey of cows 96 hours
which may be involved in a reduction of the strength of attach- post partum, estimated that at least 10 per cent of retained placen-
ment (Sharpe and others 199Q). tas were due to myometrial inertia. As it is impossible to predict
Other changes in cell type and number are thought to be when the condition will occur, most studies of post partum motili-
involved in maturation. An increase in the number and activity of ty and retained placenta have used cows prematurely induced with
leucocytes appears to be an important part of the detachment pro- corticosteroids, a procedure which produces up to 100 per cent of
cess (Gunnink 1984). There is also a decrease in the number of cases. Martin and others (1986) and Burton and others (1987)
binucleate cells in the trophectoderm from 20 per cent to 5 per found no evidence that the condition was due to a decrease in, or
cent in the last week of pregnancy, owing to a decrease in their disruption of, uterine activity during the immediate post partum
production combined with a continuation of the migration (Gross period. However, Jordan (1952), in a study of three naturally
and others 1985). Grunert (1984) also described the appearance of occurring cases, found that all three had reduced uterine motility.
phagocytic, polynuclear giant cells. These cells are not mentioned There is no known reason for this discrepancy.
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468 The Veterinary Record, November 9, 1996

Arthur and others (1995) suggested that retained placenta was parturition. This infection may lead to uterine inertia, retained pla-
analogous to uterine exhaustion in polytocous species. This sug- centa, and secondary placentitis. The evidence is anecdotal and
gestion is supported by evidence that the injection at parturition of lacks histological confirmation and some small studies have found
oxytocin (Shaw 1938) or PGF2a (Majeed and others 1991), both of no link between farm hygiene and the incidence of the condition
which can have potent ecbolic effects, reduces the incidence of (D. E. Noakes, personal communication). Metritis is usually a
the condition. Also, Vinattieri and others (1945) showed that consequence of retained placenta rather than a cause of it.
suckling post partum, which stimulates the release of oxytocin, (viii) Immature placentomes. There is a very close link between
reduced the incidence of retained placenta in buffaloes. However, short gestation periods and retained placenta. Bjorkman and
such effects may not be mediated by increasing motility; for Sollen (1961) found immature placentomes in association with
instance, Horta (1986), after inducing retained placenta with abortion and twin births, and Woicke and others (1986) found
prostaglandin inhibitors, found that PGE2 increased uterine motili- them after parturition induced by corticosteroids. Grunert (1986)
ty but did not stimulate placental release, whereas PGF2a did the believes that immature placentomes were one of the most impor-
opposite. tant causes of the condition. However, Bjorkman and Sollen
As the changes leading to placental separation begin signifi- (1961), Manasayan and others (1986) and Dzuvic and others
cantly before the onset of parturition (Grunert 1986), it is likely (1976) found the necrotic type to predominate in cases with no
that retained placenta induced by changes around parturition is obvious predisposing cause. Kathiresan and others (1990) found
due to an effect on myometrial function. Examples would include that placentomes from buffaloes that had aborted had significant
transport during birth (Heuweiser and Grunert 1987) and the anec- histological differences from those retained after a normal birth.
dotal evidence concerning acute metritis post partum (Roberts Thus, although the link between premature birth and retained pla-
1986). Although the relative incidence of atony and retention is centa is clear, the overall significance of an immature placenta is
still unknown, owing to the lack of published field surveys, the uncertain.
balance of opinion appears to be against primary myometrial dys- In immature placentomes, the number of maternal epithelial
function as an important cause of retained placenta (Grunert 1984, cells is similar to the number present around day 270 of gestation
Paisley and others 1986). A better understanding of the process of in the normal cow (Grunert 1986) and the thin maternal epitheli-
placental separation, particularly the timescale over which it um is dominated by the fetal component. Large mesenchymal
occurs, may allow a better assessment of the role of motility in cores are found in the chorionic villi. The glueline is still present
inducing the condition. although it is less densely stained than in the normal pre-release
Paisley and others (1986) listed eight factors that may interfere placentome (Bjorkman and Sollen 1961).
with the release of the placenta.
(i) Uterine atony.
(ii) Necrosis. This was the commonest histological finding in the Hormones and retained placenta
study of Bjorkman and Sollen (1961). It was characteristic of
firmly attached placentomes and was preceded by bleeding Placental maturation is probably controlled hormonally
between the chorionic and maternal villi. Cell necrosis was espe- (Grunert and others 1989). Many studies have examined the dif-
cially prominent at the villous tips and also in close relation to the ferences in hormonal concentrations (both pre- and post partum)
maternal epithelium. Autolysis was slow in comparison with more between cows calving normally and those that develop retained
loosely attached placentae. This necrosis, in combination with placenta. The induction of calving with corticosteroids and/or
hyperaemia and oedema, was the predominant finding in the stud- prostaglandins has been commonly used in order to induce the
ies of Manasayan and others (1986) and Dzuvic and others condition reliably and as a result the hormone profiles for induced
(1976). Paisley and others (1986) suggested that such changes parturition are fairly well understood. However, their relevance to
may be due to allergic reactions and that they may be due to pre- the spontaneous condition is still unclear. The results from studies
partum changes induced by generalised disease. There is little evi- of spontaneous retained placenta are contradictory and inconclu-
dence for either of these theories. Necrotic areas are present in sive, particularly when samples are taken post partum and espe-
normal non-retained fetal membranes (Margolis and others 1988) cially after a diagnosis of retained placenta. The placenta is an
and they increase greatly in the first six hours post partum in both endocrine organ and could release prostaglandins and oestrogens
retained and subsequently released membranes. Necrosis was not for several days post partum. The cow's own response to the pres-
significantly less in released placentas compared to retained pla- ence of foreign material in the uterus, for example, producing
centas. Thus it is likely that many of the studies which have inflammatory prostaglandins, adds further complications.
observed a high level of necrosis associated with retained placen- Sampling at parturition is not sufficient because the placenta
tas took samples too late, allowing time for more pathological matures over a period of several days (Grunert 1984, Gunnink
changes to occur, and that the necrosis of fetal membranes does 1984).
not always lead to the condition.
(iii) Oedema of the chorionic villi. This is usually associated with Progesterone. - The induction of calving with corticosteroids or
uterine torsion or caesarean section and perhaps other forms of PGF2a (and its analogues) leads to a decrease in the concentration
dystocia (Grunert 1986). of progesterone (Chew and others 1979a, Johnson and Jackson
(iv) Advanced involution of the placentomes. This is associated 1982). At parturition the progesterone concentration in these cows
with prolonged gestation. Proliferative changes in the maternal is not significantly different from those in cows calving naturally
caruncular epithelium mechanically inhibit the loosening of the (Henricks and others 1977, Prakash and Madan 1985). However,
placenta (Holm and others 1964). in one study, progesterone concentrations were found to be signif-
(v) Hyperaemia. This is usually thought to be due to blood vessel icantly higher four to six days pre-partum in induced cows (Chew
proliferation on one side of the feto-maternal junction. Grunert and others 1979a), although this effect is not always present
(1986) considered it to be a rare cause of retained placenta, but (Henricks and others 1977).
Hindson (1976) found that 54 per cent of cases showed evidence For spontaneous retained placenta the situation is less clear.
of hyperaemia, though it is not clear when he took his samples. Chew and others (1979b) and Bosu and others (1984) both found
(vi) Placentitis and cotyledonitis. These conditions lead to the high concentrations of progesterone pre-partum followed by nor-
mechanical inhibition of placentome loosening. They have proba- mal concentrations at calving in cows with retained placentas.
bly become much less important as a cause of retained placenta in However, von Furstenberg and others (1990) found a low concen-
Europe since the decrease in the incidence of brucellosis. tration of progesterone seven days pre-partum, and Inaba and oth-
(vii) Acute post partum metritis. Sudden increases in the incidence ers (1986), Musah and others (1987) and Peter and Bosu (1987)
of retained placenta occur in cattle calving indoors. Roberts found no correlation between retained placenta and pre-partum
(1986) suggested that such cases are usually associated with an progesterone concentrations.
acute post partum metritis, due to pathogenic organisms, for Chronically low progesterone concentrations (post ovari-
example Actinomyces pyogenes, entering the genital tract during ectomy) are also associated with the condition (Chew and others
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The Veterinary Record, November 9, 1996 469

1978), so it is unlikely that progesterone concentrations are the although the concentrations at parturition were not different from
sole cause of retained placenta. normal. Peter and Bosu (1987) found that cows which developed
the condition had significantly higher levels of cortisol throughout
Oestrogens. - For oestrogens the situation is complex, because of the peri-partum period as did cows bearing twins in the study by
the variety of oestrogens present in maternal serum. Some surveys Matton and others (1979). It is unlikely that cortisol has a direct
measure all three main oestrogens (Chew and others 1979a), while role in the induction of retained placenta.
others measure two (Henricks and others 1977) or one (von
Furstenberg and others 1990). Other surveys differentiate between Prostaglandins. - Prostaglandins play an important role in the loss
unconjugated and conjugated forms (Mostl and others 1985). of the placenta (Horta 1986). Many studies have investigated
Direct comparison of the studies is often difficult. peripheral prostaglandin metabolites (most commonly PGFM) in
The induction of calving with PGF2a (or its analogues) does not natural (Matton and others 1979, Peter and Bosu 1987) and
stimulate oestrogen synthesis (Mostl and others 1987). Thus, induced (Henricks and others 1977, Lindell and others 1977)
Henricks and others (1977) found that mean plasma oestradiol- retained placenta. However, Heuweiser and others (1992) showed
173 concentration was significantly lower in heifers induced with that there is no correlation between the utero-ovarian vein concen-
PGF2o than in those calving normally, from 13 days pre-partum tration of prostaglandins and the concentrations of their metabo-
until, and including, the day of calving. However, oestrone con- lites in peripheral veins. As prostaglandins act locally, it is their
centrations, although lower initially, increased sufficiently for local concentration that is important. Owing to the combined diffi-
there to be no significant difference at calving. Mostl and others culties of cannulating the utero-ovarian vein and predicting
(1987) observed similar levels, with unconjugated oestrogens retained placenta there have been few studies of the local changes
remaining low throughout and conjugated oestrogens being nor- in prostaglandins and the condition. Heuweiser and others (1993),
mal at parturition. in a study of cows with dystocia requiring caesarean section,
Exogenous corticosteroids can stimulate the synthesis of oestro- found higher concentrations of PGF2a, PGFM, PGE2 (and its metabo-
gens in vivo (Arbeiter and others 1984). However, the plasma lite PGEM) in the uterine and/or umbilical circulation of cows that
concentrations of oestrogens found at parturition after induction did not develop retained placenta than in those that did. The ratio
are variable. Chew and others (1978) found high oestrogen-17,B of PGF2c to PGE2 in the uterine vein was thus higher in the cows
concentrations at all induced calvings, with cows that developed that developed retained placenta.
retained placentas also having high oestrone and oestradiol-170X The results obtained in this study are only partly in agreement
concentrations; Kesler and others (1976) also found an increase in with the results from studies of in vitro production of
oestradiol at calving. However, Kaker and others (1984) found no prostaglandins by placentomes from cows within six hours post
difference in the concentrations of oestradiol at calving. Also partum. Leidi and others (1980), Gross and others (1987) and
Evans and Wagner (1976), Chew and others (1979a) and Prakash Slama and others (1993) all found that placentomes from cows
and Madan (1985) all found that at calving induced cows had that subsequently developed retained placentas produced much
lower plasma concentrations of one or more of the oestrogens. less PGF2x; however, Slama and others (1993) and Gross and oth-
The pre-partum oestrogen concentrations are clearer, induced ers (1987) also found that these placentomes produced more PGE2.
cows begin the calving process with much lower plasma concen- Gross and others (1987) suggested that this increased PGE2 pro-
trations than normal cows (Chew and others 1979b). duction was due to the retention of the binucleated cells in cows
For spontaneous retained placenta, several studies have which developed retained placenta; these cells were able to con-
observed no significant difference in oestrogen concentrations tinue to convert any PGF2,, produced by the allantochorion, to
from normally calving cows (Matton and others 1979, Elecko and PGE2. This suggestion is supported by the study of Kankofer and
others 1982, Inaba and others 1986). Agthe and Kolm (1975), others (1994) who found no evidence that the low concentrations
however, found that cows with retained placenta had a marked of PGF2Q in cows with retained placenta were due to increased
increase in oestrogen concentration within 12 hours post partum, catabolism by 15-PGDH. The discrepancy between these placen-
whereas there was little change in its mean concentration in nor- tome studies and the study of Heuweiser and others (1993) may
mal cows. Von Furstenberg and others (1990) found mean oestro- be due to differences between in vivo and in vitro metabolism.
gen-17P concentrations decreased in both normal cows and cows Heuweiser and others (1993) suggested that the low concentra-
which developed the condition in the 24 hours before calving but tions of PGE2 in cows with retained placenta may be due to the
also that they were lower in cows with retained placenta from increased metabolism of PGE2, which may not occur when the pla-
seven days before calving. Chew and others (1977) also found centomes have separated.
that the oestrogen-173 concentrations were lower during this peri- Slama and others (1993) also found differences in other prod-
od, but the oestrone concentrations were not significantly different ucts of arachidonic acid metabolism. In particular, there were dif-
and the oestrogen-1 70 concentrations were both higher and lower. ferences in the production of thromboxane B2 (TXB2) and PGIM.
A subsequent study by Chew and others (I 979a) using more cows The production of TXs2 was highest in cows with normal placental
(82 as opposed to 22) gave a different picture; no difference in the release, whereas PGIM was highest in cows that developed retained
concentrations of oestrone or oestrogen- 17f but higher concentra- placenta. In both groups these two compounds are the major prod-
tions of oestrogen- I 7a. ucts of arachidonic acid metabolism, and it was suggested that
Thus the data on oestrogen concentration and retained placenta may play a major role in the placental separation.
are inconclusive; Musah and others (1987) claimed that the condi-
tion was unrelated to oestrogen levels. Chew and others (1978)
suggested that rising oestrogen concentrations in the immediate The immune system and retained placenta
pre-partum period were linked with the condition, a suggestion
which correlates well with the results obtained by Agthe and Immunological processes appear to be closely involved in pla-
Kolm (1975). Chew and others (1979a) suggested that it is the cental release. Heuweiser and Grunert (1987) found a reduction in
ratio of progesterone to oestrogens (in particular oestrogen-173) the chemotactic activity of leucocytes in cows that went on to
that is important in the development of retained placenta. They develop retained placenta. Gunnink (1984) measured leucocyte
suggested that the ratio six days pre-partum could be used to pre- chemotactic activity and also estimated the number of leucocytes
dict retained placenta, but the results are not conclusive, and in the cotyledon. An absence of leucocytes and activity was
Chew and others (1979a) suggested a role for oestrogen-171 in always associated with retained placenta, and negative chemotaxis
uterine maturation. However, the fetal placentome has no oestro- had an incidence of 36 per cent. Dilution experiments suggested
gen receptors (Sauerwein and others 1989). that the placentomes of cows with no chemotaxis or leucocytes
produced an inhibitory factor. Thus the condition could be
Cortisol. - In a study by Matton and others (1979) cortisol con- induced by a failure to switch off the immunoprotective mecha-
centrations in cows that calved single calves and developed nisms of pregnancy.
retained placenta were significantly lower seven days pre-partum, This suggestion agrees with Joosten and Hensen (1992) who
Downloaded from veterinaryrecord.bmj.com on July 16, 2011 - Published by group.bmj.com

470 The Veterinary Record, November 9, 1996

found a link between retained placenta and the major histocom- ETHERINGTON, W. G., MARTIN, S. W., DOHOO, 1. R. & BOSU, W. T. K.
patibility complex (MHC) class I compatibility of the calf and dam. (1985) Canadian Journal of Comparative Medicine 49, 254
EVANS, L. E. & WAGNER, W. C. (I1976) Acta Endocrinologica 81, 385
MHC class I antigens combine with endogenous antigens, such as FUNG, H. P. (1983) Journial of the Chinese Society for Veterinary Science 9, 75
viruses, to allow cytotoxic T cells to destroy infected cells (Tizard GARCIA, A., BARTH, A. D. & MAPLETOFT, R. J. (1988) Proceedings of the
1992). Thus retained placenta may be due to a failure of alloreac- Annual Meeting of the Society for Theriogenology, Orlando, Florida. p 135
tivity. However, the way in which this alloreactivity is triggered is GROSS, T. S., WILLIAMS, W. F. & MANSPEAKER, J. E. (1985) Biology of
Reproduction 32 (Supplement 1), 154
unclear; fetal MHC class I is expressed only in the interplacentomal GROSS, T. S., WILLIAMS, W. F., MANSPEAKER, J. E., LEWIS, G. S. &
area (Low and others 1990) and its function there is uncertain. RUSSEK-COHEN, E. (I1987) Prostaglandins 34, 903
The role of MHC class I in normal placental separation is unclear; GRUNERT, E. (1984) Proceedings of the 10th International Congress on Animal
Joosten and Hensen (1992) suggest the MHC compatibility may Reproduction and Artificial Insemination, Urbana Champaign. p XI 17
GRUNERT, E. (1986) Current Therapy in Theriogenology. Ed D. A. Morrow.
have an effect on maturation. However, they based their study on Philadelphia, W. B. Saunders. p 237
retained placenta that occurred after normal, single calvings; in GRUNERT, E., AHLERS, D. & HEUWEISER, W. (1989) Theriogenology 31, 1081
such calvings the commonest pathological finding is 'necrosis' GUNNINK, J. W. (I1984) Veterinary Quarterly 6, 49
(Bjorkman and Sollen 1961) rather than an immature placenta. GWAZDUASKAS, F. C., BIBB, T. L., McGILLIARD, M. L. & LINEWEAVER,
J. A. (I1979) Journal of Dairy Science 62, 978
Further elucidation is necessary. HALPERN, N. E., ERB, H. N. & SMITH, R. D. (1985) Theriogenology 23, 807
HEINONEN, M. & HEINONEN, K. (I1989) Acta Veterinaria Scandinavica 30, 425
HENRICKS, D. M., RAWLINGS, N. C. & ELLICOTT, A. R. (1977)
Conclusion Theriogenology 7, 17
HEUWEISER, W. & GRUNERT, E. (1987) Theriogenology 27, 907
HEUWEISER, W., GRUNERT, E. & HOPPEN, H. 0. (1992) Journal of Veterinary
The seemingly simple diagnosis of 'retained placenta' hides a Medicine 39, 509
condition of great complexity. A large number of causal factors HEUWEISER, W., GRUNERT, E. & HOPPEN, H. 0. (1993) Prostaglandins 45, 35
has been related to an increased incidence of the condition, but lit- HINDSON, J. C. (1976) Veterinary Record 99, 49
HOLM, L. W., SALVATORE, C. & ZEEK-MINNING, P. (1964) Amnerican Journal
tle is known of how the majority of these factors induce placental of Obstetrics and Gynaecology 8, 479
retention. The normal process of placental separation is poorly HORTA, A. E. M. (1986) Zootechnia 33, 39
understood, particularly the relationship between hormonal and INABA, T., INOUE, A., SHIMIZU, R., NAKANO, Y. & MORI, J. (1986) Japanese
Journal of Veterinary Science 48, 505
structural changes, and the exact nature of most of those changes.
JOHNSON, C. T. & JACKSON, P. S. (1982) British Veterinar) Journal 138, 212
The methods for preventing the condition are at the moment limit- JOOSTEN, I. & HENSEN, E. J. (I1992) Animal Reproduction Science 28, 451
ed to reducing the prevalence of some of the predisposing factors, JORDAN, W. J. (I1952) Journal of Comparative Pathology 62, 54
for example by providing balanced nutrition and clean calving JULIEN, W. E., CONRAD, H. R., JONES, J. E. & MOXON, L. E. (1976) Journal oa
Dairy Science 59, 1955
areas, because of the lack of knowledge of its aetiology. Further
KAKER, M. L., MURRAY, R. D. & DOBSON, H. (1984) Veterinary Record 115, 378
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KATHIRESAN, D., RAJASUNDARAM, R. C. & PATTABIRAMAN, S. R. (1990)
Indian Veterinary Journal 67, 939
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Short Communications
Pyelonephritis following inadvertent TABLE 1: Significant haematological and biochemical abnormalities at
presentation
excision of the ureter during Test Result Expected range Unit
ovariohysterectomy in a bitch White cell count 32 6 5-0-18.0 103/pl
Segmented neutrophils 28.362 3.000-11-500 103/pl
Bands 1.956 0-000-0 300 103/pl
A. E. Kyles, J. P. Douglass, J. B. Rottman Albumin 27 28-44 g/litre
Alkaline phosphatase 224 10-150 iu/litre
Creatine 1.0 0.0-1 8 mg/dl
Veterinary Record (1996) 139, 471-472 Urea 17 8-24 mg/dl

OVARIOHYSTERECTOMY is commonly performed as an elec-


tive surgical procedure in the bitch. A number of complications of 16 days after elective ovariohysterectomy. The referring veterinar-
surgery have been recognised (Joshua 1965, Pearson 1973), ian reported that a spay hook had been used to locate both horns
including haemorrhage, recurrent oestrus, stump pyometra, suture of the uterus. The tubular structure identified as the right uterine
granulomas, abdominal adhesions and failure of wound healing. horn appeared to terminate close to the right kidney and the right
latrogenic damage to the urinary tract during ovariohysterectomy ovary could not be identified. This structure was ligated proximal-
has been described. Hydronephrosis has been reported following ly and distally and excised. A two week course of antibiotics was
inadvertent inclusion of one or both ureters in the ovarian or cer- prescribed (Amoxicillin; Novopharm, 22 mg/kg by mouth). Two
vical stump and may result in post renal azotaemia (Thun and oth- days after completion of antibiotic therapy, the dog became
ers 1975, Okkens and others 1981, McEvoy 1994). Accidental depressed, inappetent, pyrexic and started vomiting.
incorporation of the ureter in the cervical stump can also result in On presentation the dog was markedly depressed and unwilling
the formation of a uretero-vaginal fistula (Pearson and Gibbs to stand. Its heart rate was 100 beats per minute, respiratory rate
1980, MacCoy and others 1988). Ewers and Holt (1992) reported 48 breaths per minute and rectal temperature 40-2°C. Abdominal
accidental ligation of the bladder neck during ovariohysterectomy palpation was resented. Haematological examination revealed a
that resulted in urethral obstruction and a vesiculovaginal fistula. marked neutrophilia with a regenerative left shift; biochemical
A six-month-old Bouvier de Flandres was presented to the examination showed mild hypoalbuminaemia, an elevated alka-
College of Veterinary Medicine, North Carolina State University, line phosphatase concentration and no azotaemia (Table 1).
Urinalysis was unremarkable.
An ultrasonographic examination revealed marked enlargement
of the right kidney (Fig 1). The renal pelvis was markedly dilated.
A. E. Kyles, Department of Companion Animal and Special Species The cortex was thin and normal medullary tissue was not identi-
Medicine, J. P. Douglass, Department of Sciences and Radiology, J. B. fied. There was hyperechoic sediment in the pelvis which moved
Rottman, Department of Microbiology, Pathology and Parasitology, depending on the position of the dog. The proximal ureter was
College of Veterinary Medicine, North Carolina State University, 4700 markedly dilated and terminated abruptly. There were parallel
Hillsborough Street, Raleigh, NC 27606, USA lines of hyperechogenicity at the level of the ureteral termination,
Dr Rottman's present address is Leukosite Inc, 215 First Street, suggestive of suture material.
Cambridge, MA 02142, USA Mannitol (Mannitol; Abbott, 0 5 g/lkg intravenously) and
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Bovine retained placenta: aetiology,


pathogenesis and economic loss
R. A. Laven and A. R. Peters

Veterinary Record 1996 139: 465-471


doi: 10.1136/vr.139.19.465

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