International Journal For Parasitology

International Journal for Parasitology 46 (2016) 395–404
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International Journal for Parasitology

journal homepage: www.elsevier.com/locate/ijpara
Invited Review
Female genital schistosomiasis (FGS): from case reports to a call for

concerted action against this neglected gynaecological disease
Vanessa Christinet a, Janis K. Lazdins-Helds b, J. Russell Stothard c, Jutta Reinhard-Rupp d,⇑
a
Centre International de Recherches, d’Enseignements et de Soins en Milieu Tropical (CIRES), Akonolinga, Cameroon
b
Geneva, Switzerland
c
Department of Parasitology, Liverpool School of Tropical Medicine, Liverpool L3 5QA, UK
d
Merck, Coinsins, Switzerland
a r t i c l e i n f o a b s t r a c t
Article history: In recent years, control of neglected tropical diseases has been increasingly gaining momentum and
Received 30 December 2015 interventions against schistosomiasis are being progressively scaled-up through expansion of donated
Received in revised form 22 February 2016 praziquantel and preventive chemotherapy campaigns. However, the public health importance of female
Accepted 23 February 2016
genital schistosomiasis is not fully recognised nor its control is adequately addressed. Taking a clinical
Available online 8 April 2016
and anatomopathological perspective, we evaluated the available literature to highlight the importance
of female genital schistosomiasis and its connections with two sexually transmitted infections of global
Keywords:
importance, Human Immunodeficiency Virus (HIV) and Human Papilloma Virus. Outside the long list of
Urogenital schistosomiasis
Gynaecology
clinical descriptive reports beginning in 1899, there is presently a shocking gap in epidemiological assess-
FGS ment and a significant underestimation of the burden of FGS remains. The scarcity of integrated
HIV/AIDS approaches to address female genital schistosomiasis calls for more concerted action in its detection,
Praziquantel treatment and prevention alongside other concomitant women’s health issues, otherwise female genital
Female genital schistosomiasis schistosomiasis will remain a neglected gynaecological disease.
Ó 2016 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an
open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
1. Introduction individuals rarely harbour schistosomiasis alone, prior infection

with Schistosoma can increase the severity of other bacterial,
Schistosomiasis is a water-borne parasitic disease caused by protozoal or helminth infections acquired later (Abruzzi and
infection with trematode worms of the genus Schistosoma. The dis- Fried, 2011).
ease was originally described in Egypt by Theodor Bilharz in 1851 Schistosomiasis can be broadly classified as either acute or
and today can be found throughout Africa, South America and Asia chronic presentations (Colley et al., 2014). Upon initial percuta-
(Colley et al., 2014). Infection may affect humans of all ages and neous infection by cercariae, acute symptoms may include der-
genders, and globally it has the highest burden of disease among matitis, then later non-specific symptoms of fever, headache and
the 17 recognised neglected tropical diseases (World Health cough. Acute symptoms normally resolve in a few weeks but in
Organization (WHO), 2016b). Owing to a variety of factors exceptional cases, death by hyper-infection may occur. As adult
underlying an individual’s exposure and infection, there can be schistosomes mature within the body and commence egg deposi-
substantial differences in prevalence and intensity of infection tion, chronic manifestations ensue, typically related to immuno-
across communities, as well as an associated spectrum in the pathological lesions and the formation of granulomata in various
severity of disease. These manifestations are determined by a organs around eggs (Colley et al., 2014). The involvement of the
number of causal factors such as the species of schistosome, intestinal tract with hepato-splenic disease and the urinary tract
the duration of infection, host-specific factors that influence with its associated organs is well-known (Centers for Disease Con-
immuno-pathological lesions to the worm eggs and access trol and Prevention (CDC), 2012 http://www.cdc.gov/parasites/
to praziquantel treatment (Hirayama, 2006). Furthermore, as schistosomiasis/disease.html; WHO, 2016, http://www.who.int/
mediacentre/factsheets/fs115/en/). Since eggs can be found
throughout the body in variable amounts, other clinical and patho-
⇑ Corresponding author at: Translational Innovation Platform Global Health, Ares
Trading SA, route de la Verrerie 6, 1267 Coinsins, Switzerland. Tel.: +41 21 900
logical diseases can be found in the heart, lungs, brain and spinal
3170. cord as well as in the genital organs of both genders (Barsoum
E-mail address: [email protected] (J. Reinhard-Rupp). et al., 2013).
http://dx.doi.org/10.1016/j.ijpara.2016.02.006
0020-7519/Ó 2016 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
396 V. Christinet et al. / International Journal for Parasitology 46 (2016) 395–404
The pathological alterations due to the presence of schistosome 3. An overview of the FGS literature
eggs in the genitalia of women have been defined as a particular
entity called female genital schistosomiasis (FGS). In 1997, the A total of 193 publications featuring reports on the clinical and
Gender Task Force of the Tropical Disease Research Programme pathological presentation of FGS were identified while preparing
(TDR) of the WHO included FGS in a list of scientific areas that this review. A considerable proportion describe African cases pub-
deserve higher research priority (Poggensee et al., 1999). Since lished during the colonial era (Fig. 1). Some 44 publications were
then, however, the extent of morbidity ascribed to FGS, which from Europe, USA and Oceania, describing FGS in migrants or trav-
can be found in both the lower and upper genital tract, has contin- ellers coming from schistosomiasis-endemic countries (Table 1).
ued to be insufficiently addressed. Moreover, FGS has failed to be The large majority of the reviewed publications were case reports
reported at national levels which has hampered an international or case series; the oldest published FGS case was reported in the
appraisal. As an unfortunate outcome, prevention and control of Lancet in 1899 (Madden, 1899). The analysis of case reports and
FGS is largely disconnected from global efforts to improve the case series shows that every female genital organ (vulva, vagina,
reproductive and sexual health of women. To address this, we uterine cervix, uterine body, Fallopian tubes and ovaries) can be
attempted to draw together the available literature to give a conti- affected by schistosomiasis. We note that uterine body involve-
nental perspective and highlight how FGS should be integrated ment is greatly under-reported in such reports, being clearly
into a broader vision of improving women’s health. revealed upon comparison with findings from post-mortem stud-
ies. These latter studies demonstrate that the most frequently
2. Methodology affected gynaecological organs are the uterine cervix and the
uterine body, followed by the adnexa and the vulvo-vagina
PubMed was used as the search tool. The key words used to (Charlewood et al., 1949; Gelfand and Ross, 1953; Youssef et al.,
gather information on FGS in general were ‘female’, ‘genital’ and ‘ 1970; Gelfand et al., 1971; Edington et al., 1975). Of the three
schistosomiasis’. Only publications treating the clinical and anato- schistosomes of most medical significance, the majority of FGS is
mopathological aspects of FGS were selected and mapped or caused by S. haematobium but in Brazil, for example, FGS has been
displayed in the table. Articles published between 1899 and shown to be caused by Schistosoma mansoni (Chaves and Palitot,
September 2015 were included. Articles in English, French, German 1964; Coelho et al., 1979; Poggensee et al., 2001; Downs et al.,
and Spanish were considered. Articles in Portuguese, Japanese or 2011; Goncalves Amorim et al., 2014). In Asia, cases of FGS have
Chinese were included only as cited in Table 1 or Fig. 1. A specific also been described as resultant from Schistosoma japonicum. Less
review was performed on FGS attributed to Schistosoma haemato- important schistosome species such as Schistosoma intercalatum
bium and its association with HIV infection. The following have also been shown to cause FGS (Koller, 1975; Berry, 1976;
keywords were used: ‘HIV’ OR ‘acquired immunodeficiency Yang, 1984; Picaud et al., 1990; Qunhua et al., 2000; WHO, 2016,
syndrome’ AND ‘schistosomiasis’ OR ‘bilharzia’ or ‘haematobium’. http://www.who.int/schistosomiasis/genital_schistosomiasis/en/).
Owing to their wider implications, publications that addressed Most of the FGS cases reported before 1990 probably underrep-
schistosomiasis during pregnancy and HPV/cervical cancer, when resented the real burden of FGS for, in our opinion, they were based
encountered during the initial literature review, were also on reports from African urban centres or in northern countries
inspected but the topic was formalised in the initial search where more advanced screening tools were available. Several
algorithm. more recent studies attempted to address this systemic bias by
Table 1
Forty-six publications out of the 193 reviewed papers are from Europe, USA and Oceania describing Female Genital Schistosomiasis in migrants or travellers coming from
schistosomiasis endemic countries. The table provides an overview of countries of diagnosis, countries of infection, patient number and age, clinical condition and Schistosoma
spp.
Country of Schistosomiasis infestation Age (years) Schistosomiasis-associated clinical condition Schistosoma spp. Publication
diagnosis origin reference
number
UK Malawi Lake, Zimbabwe (t), 34, 43, 51, 26, Vulvar granuloma (3 cases), adnexal mass, infertility, tubal S. haematobium 14, 17, 37,
Zambia, Nigeria, Zimbabwe 39, 37, 27, 31, carcinoma, ectopic pregnancy, teratoma, HPV/HIV infection, 107, 147, 148,
(m) 28, 29, 28, 29 cervicitis, cervical carcinoma in situ 156, 168, 183
USA Senegal, East Africa, Liberia, 27, 20, 28, 41, Cervical dysplasia with HPV, cervical dysplasia with HPV/ S. haematobium, S. 2, 13, 45, 54,
Guinea, South Africa (m) 22, 20, 63, 32, HIV, sandy patches, ectopic pregnancy, salpingitis, mansoni (1 case) 93, 131, 154
37 infertility, perianal fistula, cervical cancer without HPV
France DRC (m), Mauritania (m), 28, 34, 22, 29, Infertility, cervical dysplasia, tubal obstruction, S. haematobium, S. 51, 58, 60,
Senegal (ms), Tunisia (m), 32, 35, 29, 21, hydrosalpinx, adnexal mass, secondary amenorrhea, mansoni (DRC, 1 108, 123, 124,
Mali (m), Mali (t), Senegal (m) 33, 27 endometritis, ectopic pregnancy case from Senegal) 165
Germany Angola, Sierra Leone, Togo (m) 24, 30, 21 Ectopic pregnancy, leiomyoma, infertility, adnexal tumour S. haematobium 86, 118, 161
Netherlands Malawi Lake, Mali (t) 37, 33 Leiomyoma, infertility S. mansoni, S. 29, 79
haematobium
Spain Nigeria (m) Mali (t) 26 Infertility, vulvitis S. haematobium 15, 50
Switzerland Egypt, Malawi Lake (t) 54, 26 Vulvar granuloma, asymptomatic ovarian and tubal S. haematobium 28, 76, 105
schistosomiasis, vulvar lesion and cervical lesions
Portugal Ovarian schistosomiasis, external genital mass 104, 179
Australia 91
Belgium Mali, Senegal (t) 20 Vulvar mass S. haematobium 39
Czech Rep. Brazil Hydrosalpynx, tubal schistosomiasis S. mansoni 136
Israel Ethiopia (m) 19 Recto-vaginal fistula 102
Ireland Nigeria (m) 31 Ectopic pregnancy, tubal schistosomiasis 67
Italy South Tunisia (t) Vaginal mass S. haematobium 23
New Malawi Lake 30, 28 Adnexal mass, vulvar lesion S. haematobium 52, 111
Zealand
m, migrants; t, travellers; HPV, human papilloma virus; HIV, human immunodeficiency virus.
V. Christinet et al. / International Journal for Parasitology 46 (2016) 395–404 397
Fig. 1. Map indicating all publications reviewed with a considerable proportion of papers describing African cases published during the colonial era, followed by Brazil. Each
hexagon represents one publication with its respective reference number. The years of publication are classified into three groups of colour shades: light colours show
publications before 1986; medium colours show those between 1986 and 2000 and dark colours those from 2001 to 2015. In particular, the two last groups highlight a time
period before and after the World Health Assembly (WHA) resolution 54.19 in 2001, which promotes regular chemotherapy for school-age children and women to reduce
morbidity. Map modified from Gryseels et al. (2006).
measuring the prevalence of cervical schistosomiasis in several et al., 1996; Leutscher et al., 1997; Poggensee et al., 1998), whereas
rural communities known to be endemic for schistosomiasis. These in other studies, up to one-fourth of cervical lesions were present
studies assessed the cervical form of FGS (diagnosed by biopsy without eggs being detected in urine (Nouhou et al., 1998;
except in the Talaat study (Talaat et al., 2004) in the frame of schis- Poggensee et al., 1998; Kjetland et al., 2005, 2008; Shennan and
tosomiasis screening studies targeting the general population in Gelfand, 1971). The imprecise relationship between FGS and egg-
regions known to be endemic for schistosomiasis in Madagascar, patent urogenital schistosomiasis confounds attempts to estimate
Tanzania, Malawi, Niger and Egypt. In these studies, cervicovaginal the number of women with, or at risk of FGS with current esti-
schistosomiasis prevalence ranged from 33% (95% confidence mates for those with urogenital schistosomiasis. By examining
interval (CI): 19–51) in Madagascar to 75% (95% CI 65–87) in Niger, the literature relative to the clinical presentation and the reported
with Tanzania and Egypt in between (Renaud et al., 1989; consequences of FGS, as well as the potential relationship
Leutscher et al., 1998; Poggensee et al., 2000; Talaat et al., 2004; with other sexually transmitted diseases, we seek to reposition
Kjetland et al., 2005). schistosomiasis in the broader context of gynaecological diseases.
Another systematic bias apparent in the literature is that most
FGS cases were reported in women less than 30 years of age, how-
4. Schistosomiasis and female genital pathologies
ever, this probably reflects the age of the studied population and
not the true age distribution of FGS. Symptoms attributable to
The clinical symptoms of FGS are in general non-specific and
FGS have been reported in young children (Hegertun et al., 2013)
can be similar to those resulting from other causes. Clinical diagno-
particularly the vulvo-vaginal forms (Berry, 1966; Al-Adnani and
sis requires trained health care professionals and/or histopatholog-
Saleh, 1982; Gouzouv et al., 1984), as well as in post-menopausal
ical visualisation of the eggs in the lesions. FGS cases have been
women (Berry, 1966; McKee et al., 1983; Arora et al., 1986;
reported in African women, African migrants or European or
Billy-Brissac et al., 1994; Nouhou et al., 1998; North et al., 2003).
American travellers, and in some instances they had a similar
With the above considerations, the examined literature report-
clinical presentation. In the following section we highlight the
ing FGS cases from Africa and Brazil were mapped to show their
pathological conditions affecting the female genital tract, however
geographical distribution with the underlying prevalence of
the recurrent challenge is to assess whether schistosomiasis is
S. haematobium and S. mansoni (Fig. 1). The years of publication
directly implicated in the pathological process or if it is just an
are classified into three groups: before 1986; between 1986 and
incidental finding in the biopsies or in the anatomopathological
2000 and from 2001 to 2015. In particular, the two last groups
tissue samples. In most of the case reports the causal relationship
highlight a similar time period (15 years) before and after the
is well based, however in some of the cases reported in anato-
WHO World Health Assembly (WHA) resolution number 54.19
mopathological series the causal relationship is sometimes less
endorsed in 2001 which promotes regular chemotherapy for
obvious and the conclusions cannot be clearly supported.
school-age children and women to reduce morbidity due to schis-
tosomiasis and soil transmitted helminths (STH). Publications
reporting FGS cases in other parts of the world are also listed 4.1. Schistosomiasis and ectopic pregnancy (EP)
(Fig. 1). It should also be noted that FGS can be associated with
active egg-patent excretion but can also be present without eggs Ectopic pregnancy (EP) is a pregnancy that occurs outside the
detected in urine or stools. For example, several studies showed uterine cavity. Tubal pregnancy is the implantation of the embryo
a prevalence of cervico-vaginal schistosomiasis of 55–75% in in the Fallopian tube and is the most frequent type of EP.
women with S. haematobium eggs detected in urine (Kjetland It is potentially a deadly condition as it can occasion severe
intra-abdominal bleeding due to tubal rupture and requires emer- (Scheller, 1971). In Niger a prevalence of 38.5% of urinary schisto-
gency surgical intervention (Bugalho et al., 1991b). EPs attributed somiasis was found in 109 women with infertility. Women with
to schistosomiasis have been repeatedly reported in many geo- schistosomiasis presented more lesions of the female genital tract
graphical areas between 1943 and 2013 and by several authors, (cervicitis, adnexal mass) than those who were not infected
i.e.: in Mozambique in a series of 103 cases of EPs, 4 out of 103 (Nayama et al., 2007). In the analysis of 111 patients with female
were attributed to a genital foci of schistosomiasis (Bugalho genital schistosomiasis in Tanzania, Swai et al. (2006) reported
et al., 1991a,b). In Ivory Coast 12 out of 331 cases of EPs were asso- 7% infertility.
ciated with tubal schistosomiasis. In Loubière’s anatomopatholog- Infertility was often the only reason leading to the histopatholog-
ical series (Loubière et al., 1977), 15 Fallopian tubes out of 32 cases ical diagnosis of schistosomiasis involvement of the upper genital
of tubal schistosomiasis were removed due to tubal pregnancy. tract. In many cases there were no other symptoms (Adeniji, 2001).
Schistosoma granuloma was always present but sometimes not Occasionally the schistosomiasis finding was reported as incidental
prominent enough to be considered as the causal factor except in (DeMille et al., 1995; Goverde et al., 1996), however, in most cases
one case of a bilateral tubal schistosomiasis due to S. mansoni infertility was attributed to Schistosoma lesions found in the Fallop-
which was responsible for bilateral EPs (Loubière et al., 1977). ian tubes. As for EPs attributed to schistosomiasis, the surgical
Two cases of tubal pregnancies in a series of 17 utero-adnexal procedures often described important peritoneal, peri-ovarian and
schistosomiasis cases were described by Diouf et al. (1973). peri-tubal adherences (Gilbert, 1943; Seneze et al., 1963; Mouktar,
Although two studies from the 1970s comparing cases and con- 1966; Diouf et al., 1973; Bailey et al., 2011; Cornier et al., 1981;
trols failed to demonstrate any association between schistosomia- El-Mahgoub, 1982; El-maraghy et al., 1982; Harouny and Pedersen,
sis and EPs (Bland and Gelfand, 1970a; Frost, 1975), tubal 1988; Letterie and Sakas, 1991; Morice et al., 1993, 1996; Ogunniyi
pregnancy was considered as the consequence of tubal alteration et al., 1994; Balasch et al., 1995; Schroers et al., 1995; Nouhou
due to schistosomiasis granulomata and/or salpingitis in the anato- et al., 1998; Swai et al., 2006; Schanz et al., 2010). Two cases of infer-
mopathological analysis of a salpingectomy specimen in the tility associated with endometrium pathology have been reported
following cases: Gilbert (1943), El-Bedri, (1958), Hassim, (1966), (Le Guyader et al., 1965; Krolikowski et al., 1995). Tuberculosis has
Rosen and Kim, (1974), Vass and Lucey, (1982), Yang, (1984), been reported concomitantly to peritoneo-tubal schistosomiasis in
Okonofua et al. (1990), Ekoukou et al. (1995), Nouhou et al. an infertile woman (Ekoukou et al., 1995). Tuberculosis granuloma
(1998), Schneider and Steyn (2000), Woto-Gaye et al. (2000), in the genitals is the main differential diagnosis of schistosoma
Eogan et al. (2002), Hoffmann and Bauerfeind (2003), Garba et al. granuloma in the genital tract.
(2004), Mohammed et al. (2004), Bahrami et al. (2006), Laxman In two studies of female infertility where male causes were
et al. (2008), Owusu-Bempah et al. (2013), Sahu et al. (2013), excluded, El-Mahgoub (1972) evoked several mechanisms of female
Aminu et al. (2014). Most of the previous cases were reported in infertility induced by schistosomiasis: tubal obstruction, defective
African residents or migrants, one in a traveller, one in a Chinese luteal phase, anovulation or antispermatozoal antibodies. He also
resident, one in an Indian and one in an Iraqui woman. Two cases reported the presence of antispermatozoal antibodies in 63% of
were attributed to S. mansoni and one to S. japonicum. The possible the 41 women with cervicovaginal schistosomiasis compared with
physiopathological mechanism as to how schistosomiasis can 10% in a control group of women with urinary or gastrointestinal
increase the risk of EP could be due to tubal submucosa alteration. schistosomiasis without FGS. (El-Mahgoub, 1972, 1982).
Mucosal alteration have also been described (Mohammed et al.,
2004), which rarely results in an obstruction but could induce a 4.3. Schistosomiasis and adnexal mass
loss of tubal elasticity. This would affect the peristalsis of the tube
and the ovum carriage. Fertilisation may occur and the conceptus Ovarian or tubal adnexal masses associated with S. haemato-
implants in the tubal mucosa instead of uterine cavity (Bland bium, S. mansoni or S. japonicum infections have been reported
and Gelfand, 1970a; Ville et al., 1991; Hoffmann and Bauerfeind, independently from infertility or EP cases. Lower abdominal pain
2003). Several descriptions of surgical procedures report peri- was sometimes the only clinical symptom (Gilbert, 1943; Ali
toneal, peri-ovarian and/or peri-tubal adherences, reflecting a et al., 1956; Seif-Eldin, 1958; Carpenter et al., 1964; Diouf et al.,
chronic inflammatory process associated with chronic schistoso- 1973; Gloor et al., 1979; Bac et al., 1987; Crump et al., 2000; Lee
miasis infection (Mensah et al., 1972; Schneider and Steyn, 2000; et al., 2000; Shekhar et al., 2000; Lambertucci et al., 2009; Batista
Bahrami et al., 2006). et al., 2010; Bailey et al., 2011; Sedlis, 1961). Schistosomiasis
fibrous tumours involving the adnexa has been described in very
4.2. Schistosomiasis and sub-fertility and infertility young girls (Symmers, cited in Camain et al. (1951)). Various types
of adnexal tumours associated with schistosomiasis have been
It is estimated that female causes of infertility account for described such as arrhenoblastoma (Lemos et al., 1960; Foda
between 25% and 37% of infertility worldwide, with the largest et al., 1961), cystadenoma (El-Maraghy et al., 1982), teratoma
proportions in sub-Saharan Africa and south-eastern Asia, which (Paradinas, 1972; Sunder-Raj, 1976; Gigase and Vanderputte,
are the regions with the highest worldwide prevalence of schisto- 1980; Kahn et al., 1978), ovarian carcinoma (Goncalves Amorim
somiasis and FGS (Nguyen and Kols, 1997). Two case-control stud- et al., 2014) ovarian Brenner cell tumour (Iskander and Kamel,
ies have shown a significant association between S. haematobium 1968), ovarian thecoma (Onuigbo and Twomey, 1978) and one
and infertility. One study was conducted in 483 Zimbabwean carcinoma of the Fallopian tube (Beadles et al., 2007). An important
women whose husbands’ infertility had been excluded. The pres- proportion of schistosomiasis adnexal involvement due to
ence of Schistosoma eggs in the cervical smear was significantly S. haematobium or S. mansoni has been demonstrated in several
associated with infertility (Odd ratio (OR): 3.6 (95%CI: 1.05–12; histopathological series (Arean, 1956; Badawy, 1962; Ricosse
P = 0.041) (Kjetland et al., 2010a,b). The second study which was et al., 1980; Al-Adnani and Saleh, 1982; Gouzouv et al., 1984;
done in Malawi showed a significantly higher proportion of infec- Gwavava et al., 1984; Mohammed et al., 2007).
tion with S. haematobium in a group of primary and secondary
infertile women than in fertile controls (41.3% versus 21.4%; 4.4. Schistosomiasis and vulvo-vaginal pathology
P < 0.02) (Bullough, 1976).
In a study in Pemba Island, Zanibar, tubal schistosomiasis was The first FGS report was published in 1899. It was a case of a
found in 40% of the cases of primary or secondary infertility warty prominent mass in the vagina of an Egyptian woman
(Madden, 1899). Many other cases of vulvo-vaginal lesions 4.6. Schistosomiasis and cervical alterations
associated with schistosomiasis have been described since then.
Schistosomiasis on the vulva or in the vagina, histopathologically In anatomopathological case series and post-mortem studies,
typically consists of a granuloma or a polypous/papillomatous the uterine cervix is the female genital organ most frequently
tumour (Scheller, 1971; Al-Adnani and Saleh, 1982; Helling-Giese affected by schistosomiasis. Cervical schistosomiasis has been the
et al., 1996; Mohammed et al., 2007). Clinically it appears as a most studied aspect of FGS with many studies conducted during
swelling, wart, sore, plaque, bleeding pseudotumoural mass the last 20 years by Feldmeier, Kjetland and associates. FGS clinical
(Ricosse et al., 1980; Wright et al., 1982). Vulvar schistosomiasis presentation can be similar to other gynaecological pathologies
lesions can be easily confounded with condyloma acuminata (sexually transmitted infection, endometriosis, etc). Several clinical
(genital warts due to Human Papilloma Virus (HPV)) (Boulle and signs and symptoms have been significantly associated with
Noreloviu, 1964; McKee et al., 1983; Samuel and Taylor, 2015) or cervical schistosomiasis such as low abdominal pain, irregular
syphilis. Helling-Giese and colleagues have demonstrated that menstruation, cervical contact bleeding, abnormal vaginal dis-
polypoid/papillomatous tumours, in the vagina and vulva, can be charge, dysparunia, vaginal or cervical polyps, contact bleeding,
considered to be pathognomonic for FGS only in the absence of vulval itching and chronic cervicitis (Leutscher et al., 1998;
HPV infection or syphilis (Helling-Giese et al., 1996). Prominent Anosike et al., 2003; Talaat et al., 2004; Swai et al., 2006). Rubbery
lesions of the vulva were described in a series in Zambia in which papules, sandy patches and neovascularization are cervical lesions
the mean age was 18 years (S.D. = 5) (Attili et al., 1983). Descrip- that have been statistically strongly associated with S. haemato-
tions of similar prominent lesions can also be found in earlier bium, (Kjetland et al., 2005; Randrianasolo et al., 2015) and with
publications (Kingsley, 1969; Gras et al., 1980). In post-mortem S. mansoni (Poggensee et al., 2001); grainy and yellow sandy
studies (Gelfand et al., 1971; Edington et al., 1975), as in patches and rubbery papules being considered pathognomonic of
histopathological series (van Raalte et al., 1981; Al-Adnani and cervical schistosomiasis (Kjetland et al., 2012, 2014; Norseth
Saleh, 1982; Swai et al., 2006) vulvo-vaginal schistosomiasis et al., 2014). In Europe and in the USA several cases of schistosomi-
infections are predominantly found in young girls or teenagers. asis have been diagnosed through cervical smears of women with
Cases of vulvo-vaginal schistosomiasis have been also associated dysplasia (Adeniran et al., 2003; Chenault and Hoang, 2006;
with S. mansoni (Arean, 1956). Several cases of schistosomiasis Dzeing-Ella et al., 2009; Chen et al., 2012). Endocervical forms of
lesions of the vulva have been described in Europe and the USA schistosomiasis such as polyps have been described as well (Eladl
in migrants (Mawad et al., 1992) or travellers (Bianchi and De et al., 2012; Delmondes et al., 2014). Three cases of schistostomia-
Carneri, 1970; Leslie et al., 1993; Corachan et al., 1997; Blum sis have been reported in HIV patients with cervical dysplasia or
et al., 1998; Laven et al., 1998; Carey et al., 2001; Catteau et al., carcinoma with HPV (Chenault and Hoang, 2006; Rachaneni
2011; Samuel and Taylor, 2015). Landry et al. (1996) described in et al., 2007; Toller et al., 2015). In an observational study con-
a female traveller a case of a vulvar schistosomiasis lesion 1 year ducted in the Limpopo province in South Africa, van Bogaert
after a retrospective diagnosis of Katayama syndrome (fever due (2011) found an HIV prevalence of 14% in 234 women with
to primary schistosomiasis infection in non-immune persons). biopsy-confirmed FGS, which is the expected HIV prevalence in
Vesico-vaginal fistulas (Servais, 1965; Ricosse et al., 1980; Kunin this region; schistosomiasis cervical involvement was observed in
et al., 1996) and perianal fistulas (DeMille et al., 1995), associated the large majority of HIV-positive women and more frequently
with schistosomiasis, have been reported. In contrast, Bland did than in the whole study group of (HIV+ and HIV ) women with
not find any association between schistosomiasis and vesico- FGS (94% versus 54%). Intraepithelial neoplasia was observed more
vaginal fistula but patients with vesico-vaginal fistulas and frequently in HIV-positive women than in the whole studied group
schistosomiasis were less likely to heal after surgical procedures (50% versus 17.5%). HIV-infected women were significantly older
than those who did not have schistosomiasis (Bland and Gelfand, than women with FGS who were not infected with HIV (42 versus
1970b). 35 years; P = 0.003) (van Bogaert, 2011).
4.5. Schistosomiasis and uterine body-associated pathology

5. Schistosoma haematobium and HIV
As previously noted clinical cases of schistosomiasis with
uterine body involvement are underreported compared with the In 1995, the first article suggesting FGS as a risk factor for HIV
frequently described uterine body involvement in post-mortem was published, establishing a plausibility and prevalence correla-
studies. This contradiction was already noted by Attia in his tion between HIV and urinary schistosomiasis (Feldmeier et al.,
review (Attia, 1962). In some recent publications, S. mansoni and 1995a,b). Since then, several studies documented that schistosomi-
S. haematobium infections have been associated with leiomyoma asis of the uterine cervix is associated with disrupted epithelia,
of the uterus, a pathology which is known to frequently affect neovascularisation, contact bleeding or spontaneous bleeding
sub-Saharan African women (Boers et al., 2003; Mayr et al., (Wright et al., 1982; Poggensee et al., 2000; Kjetland et al., 2005,
2005; Cavalcanti et al., 2011; Hillers and Wiersema, 1961). A case 2006a,b, 2009; Swai et al., 2006; Jourdan et al., 2011b, 2013), and
of endometritis due to the presence of the parasite in the intramu- a higher density of HIV target cells; factors that predispose to
ral uterine vein in a 42 year old Chinese woman (Ching-ch’ien, HIV infection (Jourdan et al., 2011a; Kleppa et al., 2014). While
1951) and a Japanese case with endometrial schistosomiasis were the association between S. haematobium and HIV has been
reported (Sugiyama et al., 1963). Cases of schistosomiasis documented in several observational studies, the association
associated with pregnancy have been associated with stillbirths between S. mansoni and HIV is less clear. Two case control studies
(Narabayashi, 1914 cited in Carpenter et al., 1964; Youssef performed in comparable groups and adjusted for the main con-
and Abdine, 1958; Sutherland et al., 1965; Berry, 1966; founding factors showed two- to four-fold increased odds of HIV
Bittencourt et al., 1980). One case control study examined the in women with FGS due to S. haematobium (Kjetland et al.,
impact of schistosomiasis on birth weight. While not showing 2006b) or urogenital schistosomiasis (Downs et al., 2011). In an
any differences in the delivery term, it did show that schistosomi- ecological study including 43 sub-Saharan African countries
asis in pregnant women was significantly associated with low Ndeffo Mbah et al. (2013b) demonstrated that each infection with
birth weight in preterm deliveries (Siegrist and Siegrist-Obimpeh, S. haematobium per 100 individuals was associated with a 2.9%
1992). relative increase in HIV infection (95% CI: 0.2–5.8%; P = 0.038).
Three mathematical modelling studies have shown a correlation studies were mostly performed in S. haematobium endemic
between HIV and schistosomiasis epidemics and an impact of areas. Despite the relatively similar methodology, these studies
schistosomiasis treatment on the HIV epidemic (Gibson et al., revealed significantly different results, which most likely
2010; Mushayabasa and Bhunu, 2011; Ndeffo Mbah et al., reflected the prevalence and intensity of schistosomiasis in the
2013a). Furthermore, one of these studies showed the cost studied areas. However, other reasons cannot be excluded and
effectiveness of a schistosomiasis intervention on HIV infection deserve further research. Equally relevant is the lack of popula-
prevention (Ndeffo Mbah et al., 2014). The main limitation of tion studies in areas endemic to S. mansoni (and eventually
the above cited observational studies is that they cannot prove S. japonicum), given the abundance of case reports of FGS associ-
causality and some relevant confounding factors may have been ated with this species, particularly in Brazil (Fig. 1). Traditionally,
missed. the interface between parasitology and gynaecology has been
The interpretation of the results could be wrong if HIV infection weak and largely focused on diseases caused by protists e.g.
would occur before FGS and if it would induce more severe FGS Trichomonas vaginalis. It has been only recently appreciated that
lesions (as it is the case for cervical dysplasia). Schistosomiasis helminths, and particularly schistosomiasis, cause significant
age prevalence curves and its genital manifestation before the damage to the female genitalia, as highlighted in a relevant
onset of sexual activity tend to make more it probable that schis- WHO document (WHO, 2016a).
tosomiasis infection and its related genital lesions occur before Today, we appreciate many of the possible consequences of FGS
HIV infection (Poggensee et al., 2000; Kjetland et al., 2005; such as EP, infertility, spontaneous abortion, low premature infant
Hegertun et al., 2013). Moreover FGS clinical presentation does birth weight, possibly cervical cancers, cervical lesions and
not differ in HIV-infected women versus HIV non-infected women especially its probable role in increasing susceptibility to other
(Kleppa et al., 2015). Egg excretion in urine might be increased in infections such as HIV/AIDS, however we lack reliable up-to-date
HIV-positive women which would overestimate the association epidemiological information on prevalence, incidence and geo-
but several studies have shown that egg excretion tends to be sim- graphical distribution of FGS. We can only make conservative
ilar or even lower in HIV-infected individuals with urinary schisto- estimates of the overall prevalence of the disease and of the 250
somiasis (N’Zoukoudi-N’Doundou et al., 1995; Mwanakasale et al., million people infected with schistosomiasis, approximately two-
2003; Kallestrup et al., 2005; Kleppa et al., 2015). thirds of whom (ca. 170 million) are infected by the urogenital
form caused by S. haematobium (the form with the highest correla-
6. Cervical schistosomiasis, HPV and cervical carcinoma tion with cases of FGS). Among those 170 million, half of them are
women (ca. 85 million) and at least one-third of those women may
It is well established that cervical carcinoma is mainly due to suffer from FGS. Of them, probably 20 million are girls or young
HPV infection. While the association between schistosomiasis women, most of them lacking suitable medical attention (Hotez
and cervical carcinoma remains unclear, several cases of cervical and Whitham, 2014). We consider that this lack of validated
carcinoma associated with schistosomiasis have been reported epidemiological information is the major impediment towards
many years ago (Chaves, 1966; Pimentafilho, 1964). In two bringing FGS to the forefront of strategic discussions not only in
histopathological series, cervical carcinoma was found in 9–10% the context of schistosomiasis disease control interventions, but
of the studied cervical schistosomiasis cases (Badawy, 1962; perhaps even more importantly, in the context of addressing
Gwavava et al., 1984). Payet and Camain (cited in Gwavava et al. women’s health in the broadest sense including mental health,
(1984)) found four cases of cervical cancer associated with schisto- sexually transmissible diseases, cancer and reproductive/maternal
somiasis in a series of 38 cervical carcinoma cases. Youssef health. This is especially important when considered in the context
reported 15 cases of invasive cervical carcinoma in which Schisto- of achieving the 2030 Sustainable Development Goals (SDGs) and
soma eggs were visualised microscopically out of 121 cases of particularly SDG 3: ‘‘Ensure healthy lives and promote well-being
cervical schistosomiasis (Youssef et al., 1970). On the other hand, for all at all ages”. FGS falls within the targets set for SDG3 on at
other studies found no association between cervical carcinoma least two accounts: ‘‘By 2030, ensure universal access to sexual
and schistosomiasis (Williams, 1967; Coelho et al., 1979; Wright and reproductive health-care services, including for family
et al., 1982; Szela et al., 1993). However, in one study when no planning, information and education, and the integration of repro-
association between cervical cancer and cervical schistosomiasis ductive health into national strategies and programmes” and ‘‘By
was found, it was observed that women affected with both schisto- 2030, end the epidemics of AIDS, tuberculosis, malaria and
somiasis and cervical cancer were significantly younger than those neglected tropical diseases and combat hepatitis, water-borne
affected by cervical cancer only (Moubayed et al., 1994, 1995). This diseases and other communicable diseases”. (SDG 3 www.un.org/
could reflect the fact that young girls are more at risk of having FGS sustainabledevelopment/sustainable-development-goals).
but it could also be compatible with the hypothesis that schistoso- When examining the case reports, the vast majority of those
miasis could increase the carcinogenic effect of HPV infection on were in the context of medical care reports from women living in
the uterine cervix by predisposing to HPV infection or favouring schistosomiasis endemic countries or from individual cases of
its persistence as several authors have hypothesised. Indeed tourists who acquired FGS in sub-Saharan countries and were
Petry and colleagues (2003) found a higher proportion of high risk diagnosed in the well-equipped health care facilities of western
HPV in the genitals of women from a schistosomiasis endemic area countries. In those reports it was often difficult to be affirmative
compared with controls (Poggensee et al., 1999; Poggensee and regarding the causal relationship between schistosomiasis and
Feldmeier, 2001; Petry et al., 2003). More recently a longitudinal the described pathology. The high number of FGS descriptions to
study showed that the development of high-grade squamous date has had little impact on performing large scale population
intraepithelial neoplasia was significantly associated with FGS of based studies to estimate more precisely the FGS burden and to
a minimum of 5 years duration, while no association was found address its public health implications, particularly in relation to
between FGS and persistent high-risk HPV (Kjetland, 2010). gynaecological health or to highly prevalent infections such as
HIV or HPV. Therefore, well designed prospective studies address-
7. Discussion ing the full spectrum of potential target organs, particularly the
upper genital tract (Richter et al., 1995), should be conducted in
The majority of the publications examined in this review were various schistosomiasis endemic areas (including S. mansoni and
case reports or case series. The few general population based S. japonicum).
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International Journal for Parasitology 46 (2016) 395–404

Contents lists available at ScienceDirect

International Journal for Parasitology

Female genital schistosomiasis (FGS): from case reports to a call for

1. Introduction individuals rarely harbour schistosomiasis alone, prior infection

4.5. Schistosomiasis and uterine body-associated pathology

The main challenge when planning or conducting the above References

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