S. haematobium as a Common Cause of Genital Morbidity in Girls: A Cross-sectional Study of Children in South Africa.
ABSTRACT Schistosoma (S.) haematobium infection is a common cause of genital morbidity in adult women. Ova in the genital mucosal lining may cause lesions, bleeding, pain, discharge, and the damaged surfaces may pose a risk for HIV. In a heterogeneous schistosomiasis endemic area in South Africa, we sought to investigate if young girls had genital symptoms and if this was associated with urinary S. haematobium.
In a cross-sectional study of 18 randomly chosen primary schools, we included 1057 schoolgirls between the age of 10 and 12 years. We interviewed assenting girls, whose parents had consented to their participation and examined three urines from each of them for schistosome ova.
One third of the girls reported to have a history of genital symptoms. Prior schistosomal infection was reported by 22% (226/1020), this was associated with current genital symptoms (p<0.001). In regression analysis the genital symptoms were significantly associated both with urinary schistosomiasis (p<0.001) and water contact (p<0.001).
Even before sexually active age, a relatively large proportion of the participating girls had similar genital symptoms to those reported for adult genital schistosomiasis previously. Anti-schistosomal treatment should be considered at a young age in order to prevent chronic genital damage and secondary infections such as HIV, sexually transmitted diseases and other super-infections.
- [Show abstract] [Hide abstract]
ABSTRACT: Urogenital schistosomiasis is one of the greatest single infectious sources of human morbidity and mortality known. Through a complex cycle of infection, migration and eventual maturation and mating, S. haematobium (the aetiological agent of urogenital schistosomiasis) deposits highly immunogenic eggs within the bladder and other pelvic organs, activating a wide range of immune programs that determine both infection outcome as well as downstream immunopathology. In this review, we discuss the experimental and observational bases for our current understanding of these immune programs, focusing specifically on how the balance of type 1 and type 2 responses governs subsequent immunopathology and clinical outcome.Parasite Immunology 09/2014; 36(9). · 1.85 Impact Factor
- [Show abstract] [Hide abstract]
ABSTRACT: Schistosoma (S.) haematobium is a neglected tropical disease which may affect any part of the genital tract in women. Female genital schistosomiasis (FGS) may cause abnormal vaginal discharge, contact bleeding, genital tumours, ectopic pregnancies and increased susceptibility to HIV. Symptoms may mimic those typical of sexually transmitted infections (STIs) and women with genital schistosomiasis may be incorrectly diagnosed. An expert consensus meeting suggested that the following findings by visual inspection should serve as proxy indicators for the diagnosis of schistosomiasis of the lower genital tract in women from S. haematobium endemic areas: sandy patches appearing as (1) single or clustered grains or (2) sandy patches appearing as homogenous, yellow areas, or (3) rubbery papules. In this atlas we aim to provide an overview of the genital mucosal manifestations of schistosomiasis in women. Photocolposcopic images were captured from women, between 1994 and 2012 in four different study sites endemic for S. haematobium in Malawi, Zimbabwe, South Africa and Madagascar. Images and specimens were sampled from sexually active women between 15 and 49 years of age. Colposcopic images of other diseases are included for differential diagnostic purposes. This is the first atlas to present the clinical manifestations of schistosomiasis in the lower female genital tract. It will be freely available for online use, downloadable as a presentation and for print. It could be used for training purposes, further research, and in clinical practice.PLoS Neglected Tropical Diseases 11/2014; 8(11):e3229. · 4.49 Impact Factor
- [Show abstract] [Hide abstract]
ABSTRACT: Background. The incidence of tubal ectopic gestation caused by schistosomiasis induced tubal pathology is undocumented in this environment, which may be due to rarity of this pathology. Bilateral tubal gestation is common in patients that have undergone in vitro fertilization. We report a hitherto undocumented case of spontaneous bilateral ectopic gestation following tubal schistosomiasis. Case Report. Mrs. OB was a 32-year-old G4P3(+0) (3 alive) woman who complained of abdominal pain and bleeding per vaginam of 4 and 2 days' duration respectively following 8 weeks of amenorrhea. A clinical impression of ruptured ectopic gestation was confirmed by ultrasound scanning. She had bilateral salpingectomy with histology of specimens showing bilateral ectopic gestation with Schistosoma haematobium induced salpingitis (findings of Schistosoma haematobium ova noted on slide). Conclusion. Schistosoma induced salpingitis is a rare but possible cause of bilateral tubal gestation.Case reports in obstetrics and gynecology. 01/2014; 2014:674514.
S. haematobium as a Common Cause of Genital
Morbidity in Girls: A Cross-sectional Study of Children in
Ingrid Elise Amlie Hegertun1,2., Kristin Marie Sulheim Gundersen1,2.*, Elisabeth Kleppa1,2,
Siphosenkosi Gift Zulu3, Svein Gunnar Gundersen4,5, Myra Taylor3, Jane D. Kvalsvig3, Eyrun
1Centre for Imported and Tropical Diseases, Department of Infectious Diseases Ullevaal, Oslo University Hospital, Oslo, Norway, 2University of Oslo, Oslo, Norway,
3School of Public Health Medicine, Nelson R Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa, 4Research Department, Sorlandet Hospital
HF, Kristiansand, Norway, 5Institute for Development Studies, University of Agder, Kristiansand, Norway, 6School of Biological and Conservation Sciences, University of
KwaZulu-Natal, Durban, South Africa
Background: Schistosoma (S.) haematobium infection is a common cause of genital morbidity in adult women. Ova in the
genital mucosal lining may cause lesions, bleeding, pain, discharge, and the damaged surfaces may pose a risk for HIV. In a
heterogeneous schistosomiasis endemic area in South Africa, we sought to investigate if young girls had genital symptoms
and if this was associated with urinary S. haematobium.
Methodology: In a cross-sectional study of 18 randomly chosen primary schools, we included 1057 schoolgirls between the
age of 10 and 12 years. We interviewed assenting girls, whose parents had consented to their participation and examined
three urines from each of them for schistosome ova.
Principal findings: One third of the girls reported to have a history of genital symptoms. Prior schistosomal infection was
reported by 22% (226/1020), this was associated with current genital symptoms (p,0.001). In regression analysis the genital
symptoms were significantly associated both with urinary schistosomiasis (p,0.001) and water contact (p,0.001).
Conclusions: Even before sexually active age, a relatively large proportion of the participating girls had similar genital
symptoms to those reported for adult genital schistosomiasis previously. Anti-schistosomal treatment should be considered
at a young age in order to prevent chronic genital damage and secondary infections such as HIV, sexually transmitted
diseases and other super-infections.
Citation: Hegertun IEA, Sulheim Gundersen KM, Kleppa E, Zulu SG, Gundersen SG, et al. (2013) S. haematobium as a Common Cause of Genital Morbidity in Girls:
A Cross-sectional Study of Children in South Africa. PLoS Negl Trop Dis 7(3): e2104. doi:10.1371/journal.pntd.0002104
Editor: Jennifer A. Downs, Weill Cornell Medical College, United States of America
Received June 21, 2012; Accepted January 28, 2013; Published March 21, 2013
Copyright: ? 2013 Hegertun et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The study was funded by Centre for Imported and Tropical Diseases, Oslo University Hospital, Oslo University Hospital Ullevaal (VIRUUS), Ship owner
Tom Wilhelmsen Foundation (http://legatsiden.no), S.G. Sønneland Foundation (http://legatsiden.no) and General Travel Scholarships (http://legatsiden.no). The
funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: firstname.lastname@example.org
. These authors contributed equally to this work.
Urogenital schistosomiasis causes gynecological morbidity in
adult women [1,2]. Schistosoma (S.) haematobium is primarily known
for its effect on the urinary tract, but in endemic areas
schistosomiasis may be the most common cause of genital
morbidity and mucosal lesions . An estimated 390 million
females are at risk of schistosomiasis infection [4,5]. It is second
only to malaria in terms of public health impact of the parasitic
diseases, with more than 100 million females infected, 85% of
them live in rural parts of Africa.
Previous studies on urogenital schistosomiasis have been
conducted in adult women of childbearing age. S. haematobium
ova when deposited in the female reproductive tract seem to be
equally distributed in the different genital parts, but are most
commonly identified in the cervix and the vagina [6,7,8,9]. Both
viable and dead ova may cause tissue reactions, morbidity and
symptoms long after contact with infested waters [10,11]. The
disease may manifest itself in both the genital and urinary tract
and may be found exclusively in the genitals [6,12]. In young girls
there have only been a few case reports, hypothesizing that the
pre-pubertal predilection site is in the vulva [7,8,9,13,14]. This
may partly be because gynecological inspections are not prioritized
in rural areas, controversial in virgins, but also because the causal
relationship between schistosomiasis and genital lesions in young
females has not been explored on a large scale [14,15].
It has been hypothesized that female genital schistosomiasis
poses an increased risk to secondary infections such as human
PLOS Neglected Tropical Diseases | www.plosntds.org1 March 2013 | Volume 7 | Issue 3 | e2104
papillomavirus and other STDs. Most importantly, these women
have been found to have significantly more HIV [16,17,18,19]. In
the wake of the HIV epidemic and a realistic prospect of successful
anti-schistosomal mass-treatment programs this study sought to
explore if girls before sexual debut had signs of genital disease .
In Ugu District, South Africa the study aimed to explore the
association between gynecologic symptoms and urinary S.
haematobium in young girls.
Study design and participants
We carried out a cross-sectional study in 18 primary schools,
which were randomized for inclusion from 309 primary schools in
the area. We invited all girls aged 10–12 years in the included
schools. Girls who were absent on the days of the invitations were
excluded, as were girls with serious illnesses, or if their guardians
or they refused.
The schools were visited between September 2009 and
November 2010 in the predominantly rural Ugu District,
KwaZulu Natal, South Africa, an S. haematobium endemic area,
which covers 5866 km2(Figure 1). It has an estimated population
of 700 000 almost exclusively isiZulu speaking people, 84% reside
in the rural areas, 51% are below the age of 20 years and 55% are
The study was approved by The Biomedical Research Ethics
Administration, UKZN 2009, Ref BF029/07; by the Department
of Health, Pietermaritzburg, 2009, Ref HRKM010 - 08; by the
Norwegian ethics committee, Ref 469 - 07066a1.2007.535, 2007,
and the Departments of Health (2008) and Education (2009) in
Ugu District. The Helsinki Declaration was followed. All members
of the group, including students and research assistants had passed
exams in Good Clinical Practice and signed Declarations of
Confidentiality. The interviewers did not know the study subjects
beforehand. Prior to the study there were information meetings for
the parents, principals, school governing bodies and/or teachers of
each school. Informed consent was given by each girl, and the
parents/guardians signed consent forms. Identifying information
was stored separate from the interview information (in separate
towns). All were informed about their right to withdraw and to
abstain from answering questions without negative consequences.
In order to protect girls from stigmatization the disease was
discussed in general terms as urinary schistosomiasis. Treatment
for schistosomiasis was offered to all, and all were informed about
possible side effects. A private psychologist was hired by the project
to take care of referred cases as felt necessary; for psychological,
practical and legal issues. When other medical help was required,
the girls were referred to a government clinical facility, or offered
private care if government services were unavailable. For ethical
and community liaison reasons the project staff was not involved in
any physical or psychological examinations after referral.
The interviews (30 minutes duration) were conducted face to
face in isiZulu (the local language) by trained female fieldworkers.
Questions were asked about recent (the last week) or previous
urogenital symptoms of itch, burn, ulcers or tumors (swelling,
lumps) in the genitals, malodorous discharge, color of discharge
and feeling of a burning sensation in the genitals, as well as red
urine, dysuria, urge and stress incontinence [1,2]. They were also
asked questions about confounders for bloody discharge (men-
struation and red urine), malodorous discharge (sexual intercourse
and sexual abuse) and for burning sensations in the genitals (sexual
intercourse and dysuria). The girls in a pilot study (same age) had
no concept of the local anatomy and we therefore decided to not
include questions on exact localization of e.g. tumors. In case the
child did not seem to understand, terms were explained and if she
seemed too shy/uncomfortable to answer the interviewers were
instructed to move to the next question. The discharge color was
defined using a custom-made color chart. The study population
was not familiar with the details of the questionnaire on
beforehand. A water body was defined as a river, dam, lake,
Urogenital schistosomiasis (Bilharzia) is a common cause of
gynecological disease in adult women. Reports to date
indicate that genital lesions in adults become chronic and
that the damages make women susceptible to HIV. This is
the first study on urogenital schistosomiasis in pre-
pubertal girls. We interviewed girls aged 10 to 12 years
of age for urinary and gynecological symptoms. The
research assistants did not know the schistosomiasis
infection status in the school or the individuals. We
collected three urines that were examined for schistosome
eggs. We found that a significantly increased number of
girls with urinary schistosomiasis have stinking, bloody
discharge, ulcers, tumors and a burning sensation in their
genitals. This indicates that gynecological damages due to
schistosomiasis start before sexual activity, and before
menstruation. By preventing urogenital schistosomiasis in
girls we may have an innovative opportunity to reduce
teenage HIV transmission and gynecological disease. This
study presents a new aspect of a neglected disease
affecting more than 100 million females, long overdue for
Figure 1. Map of Ugu district in South Africa. The coastal areas are
inhabited by the more affluent and the schools here were excluded.
Genital Morbidity in Girls - Schistosomiasis
PLOS Neglected Tropical Diseases | www.plosntds.org2 March 2013 | Volume 7 | Issue 3 | e2104
stream or pond. Each child was asked if she carried out any of
seven specific water-related activities known in the study area
(playing/swimming, washing/bathing, laundry, washing blankets,
collecting water, fishing and crossing) . Furthermore, there
were validated demographic, social and psychological components
in the questionnaire that will not be analyzed here.
The researchers aimed to visit each school at least three times.
We obtained urine samples from each girl on three consecutive
days between 10 am and 2 pm. After gentle tilting we deposited
10 ml of urine into a container with 1 ml methylate-formalin
solution and the same week we investigated the specimens by
microscopy . After centrifuging, we transferred all of the
precipitate onto microscopy slides; the last amount was washed
with water before transferred. If the mean number of eggs of the
three specimens was higher than 50 per 10 ml urine the infection
was classified as high-intensity . One stool sample per child
was collected for Kato Katz and analyzed for Ascaris lumbricoides,
Ancylostoma duodenale, Taenia solium, Trichuris trichiura and S. mansoni.
If there was at least one ovum in a specimen it was defined as
Data management and statistical analyses
Based on data from studies in adults we estimated the
prevalence of genital schistosomiasis to be 30% and urinary
schistosomiasis 40% . We hypothesized that the expected
prevalence of genital ulcers in the schistosomiasis exposed to be
9% and in the unexposed 4%. To detect a difference with a
significance level of 5% and a power of 80%, the sample size
would have to be 511 unexposed and 341 schistosomiasis exposed
young women, in all 852 subjects. The information was recorded
on paper; the personal information sheet was separated from the
other information as soon as the record number had been secured.
Data was entered into EpiData (interview) or Excel (urine) and
subsequently exported into IBM SPSS version 19 (Chicago,
Illinois, USA). Chi-square and odds ratios (OR) with 95%
confidence interval (CI) were used to compare impacts of water
contact or current urinary schistosomiasis infection on genital
symptoms. In order to study the impact of other variables (for
example menstruation or red urine), logistic regression analysis
was applied with a 5% significance level; variables were included if
the P-value in the crude association was less than 0.2 and if the
Spearman rank correlation coefficient was below 0.7. When there
were less than 10 cases, the variable was not included in regression
analysis. The statistical analysis was computed using SPSS.
Characteristics of the study group
Schools that were randomized for inclusion were visited in no
particular order. We invited all pupils aged 10 to 12 years. All
schools were visited several times in order to collect guardian
consent forms and to find as many students as possible. The
parents of 1241/1948 (64%) pupils in 18 schools provided consent.
On the days we were in the schools we were able to include 1057
assenting girls. In the first 13 schools, where there was adequate
time before exams, the consent forms were returned and signed by
92% (1109/1201) of the parents. The pupils were recruited from
grades 1 to 7, median grade 5.
Menstruation, HIV testing and sexual history
Answers were recorded as missing if the child chose not to
answer or did not understand the topics. Seven percent of the girls
(71/1019) had started menstruating. Only 5% (51/981) said they
had been tested for HIV. Three out of 980 (0.3%) knew they had
HIV, as many as 495 said they did not know and 77 girls did not
reply to this question. Less than one percent (7/1017) reported to
have had intra-vaginal sex. However, two percent (22/953)
reported to have been sexually abused. They were referred to
psychosocial follow-up. All in all 24 of 1019 young girls had
experienced voluntary or involuntary vaginal sex.
Out of the 1057 girls who were interviewed, 970 submitted at
least one urine for examination, and out of these 791 submitted
three urine samples. S. haematobium eggs were found in 32% (312/
970) of the girls. High-intensity urinary infection was found in
28% (88/312) of these. In those who had ova in the urine, the
mean intensity of infection was 52 eggs/10 ml urine (range 1–
624/10 ml). Among the 658 girls with negative urine specimens,
79% (522) submitted three negative urine samples. There was
neither any difference in urinary schistosomiasis infection intensity
nor presence of symptoms between those who had submitted three
urine samples versus one sample.
Thirty five percent reported to have had genital symptoms
(356/1018), and as many as 17% (172/1008) reported genital
symptoms the last week. Eighteen girls reported having a genital
tumor or an ulcer this last week. Table 1 shows the association
between urinary schistosomiasis and symptoms in girls. Controlled
for confounders in multivariate analyses the table shows that
urinary schistosomiasis remained associated with bloody dis-
charge, a burning sensation in the genitals, genital ulcers, tumors
and incontinence. Having had vaginal sex was not significantly
associated with any of the symptoms; however the variable
‘vaginal sex’ was forced into the multivariate analyses. It did not
influence the association between the symptoms and urinary
schistosomiasis or water contact. Likewise, having soil-transmitted
helminths did not influence the associations (data not shown) and
only one person had S. mansoni. The discharge color was white in
51% (84/164) of the cases; cream color in 35% (58/164) and
yellow in 9% (14/164). The discharge had streaks/traces of red in
13% (11/87) of the cases, light red in 66% (57/87) of the cases and
an even lighter shade of red (light pink) in 9% (8/87). Patients with
symptoms were referred but not investigated by the project.
Nuances in urinary schistosomiasis negative and positive
In order to explore the urinary negative girls in more detail they
were first divided into two groups (Figure 2), those in high-endemic
school versus those in low endemic. The pupils from the low-
endemic schools were further split into two, those who admitted
water body contact and those who did not. Figure 2 shows that
symptoms are significantly more common in those that have a
high intensity of infection. The figure also highlights that low-
endemic schools (the ‘most negative’ in the district) have a low
prevalence of genital symptoms. Amongst the girls with high-
intensity schistosomiasis almost 50% had genital symptoms,
compared to less than 5% in the negative girls who lived in
non-endemic areas and had no water contact. These girls denied
having genital tumors, ulcers, bloody or smelly discharge. Bloody
discharge was found in the high-endemic schools only, notably also
in those individuals of these schools who were negative for
schistosomiasis in three urines (Figure 1, category III). Urge
incontinence and genital itch were both relatively constant in the
Genital Morbidity in Girls - Schistosomiasis
PLOS Neglected Tropical Diseases | www.plosntds.org3 March 2013 | Volume 7 | Issue 3 | e2104
Table 1. Association between the urogenital symptoms in rural 10–12 year old girls and urinary schistosomiasis.
In 298 urinary
In 628 urinary
negative (%)OR (95% CI)b
PAdj. OR (95%CI)c
Never247 (83)608 (97)1.01.0
Sometimes32 (11) 13 (2)6.1(3.1–11.7)
Always 19 (6) 7 (1) 6.7 (2.8–16.1)
,0.001 3.3 (1.3–8.5)0.01
Never207 (69) 568 (90)1.01
Sometimes37 (12) 34 (5)2.9 (1.8–4.9)
,0.001 2.4 (1.5–4.1) 0.001
This week 54 (18)26 (4) 5.7 (3.5–9.3)
Never254 (85)565 (90) 1.01.0
Sometimes 20 (7)39 (6)1.1 (0.7–2.0)0.641.1 (0.6–2.0)0.69**
Always 24 (8)24 (4) 2.2 (1.2–4.0)0.0072.2 (1.2–4.0)0.008
Never237 (80)524 (83)1.01.0
Sometimes39 (13)62 (10)1.4 (0.9–2.1)0.131.4 (0.9–2.2)0.12**
This week22 (7)42 (7)1.2 (0.7–2.0)0.591.2 (0.7–2.0)0.57**
Burning sensation in the
Never243 (82)561 (89) 1.01.0
Sometimes 34 (11)43 (7)1.8 (1.1–2.9)0.011.6 (1.0–2.6)0.05
This week 21 (7) 24 (4)2.0 (1.1–3.7)0.021.9 (1.0–3.5) 0.05
Never220 (74)516 (82) 1.01.0
Sometimes 55 (18) 75 (12)1.7 (1.2–2.5)0.0051.6 (1.1–2.3)0.02
This week23 (8) 37 (6) 1.5 (0.9–2.5)0.171.3 (0.7–2.2) 0.42**
Never 266 (89)598 (95) 1.01.0
Sometimes 27 (9)25 (4)2.4 (1.4–4.3)0.0022.4 (1.4–4.3)0.002
This week5 (2)5 (1)2.2 (0.6–7.8)0.202.2 (0.6–7.7)0.21**
Never283 (95)613 (98) 1.01.0
Sometimes12 (4) 13 (2)2.0 (0.9–4.4)0.092.0 (0.9–4.4)0.09
This week3 (1)2 (0)3.2 (0.5–19.6)0.19 3.3 (0.5–19.6)0.19**
Never184 (62)443 (71) 1.0 1.0
Sometimes 77 (26)109 (17)1.7 (1.2–2.4)0.0021.7 (1.2–2.4)0.002
This week 37 (12)76 (12)1.2 (0.8–1.8)0.471.2 (0.8–1.8)0.44**
Never212 (71)530 (84) 1.01.0
Sometimes 44 (15) 66 (11)1.7 (1.1–2.5)0.021.7 (1.1–2.5) 0.02
This week42 (14)32 (5)3.3 (2.0–5.3)
Eight separate multivariate analyses.
Age was forced into each model and did not influence the results (data not shown).
aThe presence of at least one schistosome ova in any of the urine examined specimens.
bOdds ratio (OR) with 95% confidence interval (CI).
cAdjusted odds ratio, different confounding variables were included in each multivariate analysis for the specific genital symptom.
dRed urine as seen by the child.
**If recalculated as ‘ever had the symptom’ it is significantly associated with urinary schistosomiasis.
Genital Morbidity in Girls - Schistosomiasis
PLOS Neglected Tropical Diseases | www.plosntds.org4March 2013 | Volume 7 | Issue 3 | e2104
Figure 2. Genital and urinary symptoms in girls of two S. haematobium positive groups and three negative risk groups.aLikelihood
ratio.bThree urines investigated for S. haematobium ova, all were negative.cMore than 50 S. haematobium ova per 10 ml urine.d1–49 ova per 10 ml
urine.eThese girls have water body contact (e.g. river, dam or lake).fThese girls deny water body contact.
Genital Morbidity in Girls - Schistosomiasis
PLOS Neglected Tropical Diseases | www.plosntds.org5March 2013 | Volume 7 | Issue 3 | e2104