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      The Colposcopic Atlas of Schistosomiasis in the Lower Female Genital Tract Based on Studies in Malawi, Zimbabwe, Madagascar and South Africa

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          Abstract

          Background

          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.

          Methodology/Principal findings

          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.

          Significance

          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.

          Author Summary

          Female genital schistosomiasis commonly remains undiagnosed due to its unacknowledged clinical manifestations. Millions of women in endemic areas are infected, and many suffer from abnormal vaginal discharge, contact bleeding, genital tumours, ectopic pregnancies, and an increased susceptibility to HIV. Sandy patches and rubbery papules identified by visual inspection may serve as indicators for the diagnosis of genital schistosomiasis. However, text books do not contain this information and it is not taught in medical school or to nurses serving these patients in endemic areas. The aim of this Atlas is to present the photocolposcopic manifestations of schistosomiasis in the lower female genital tract. Photocolposcopic images were captured from women between 15 and 49 years of age, between 1994 and 2012 in four different sites endemic for S. haematobium in Malawi, Zimbabwe, South Africa and Madagascar. This is the first atlas to present the clinical manifestations of schistosomiasis. Two types of sandy patches, abnormal blood vessels and rubbery papules are shown, as well as differential diagnoses. PloS NTDs makes it possible for all to access this information.

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          Most cited references60

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          Association between genital schistosomiasis and HIV in rural Zimbabwean women.

          To determine the association between female genital Schistosoma haematobium infection and HIV. A cross-sectional study with a 1-year follow-up. Gynecological and laboratory investigations were performed for S. haematobium and HIV. Sexually transmitted infections, demographic and urogenital history were analysed as confounders. The participants were 527 sexually active, non-pregnant, non-menopausal women between the ages of 20 and 49 years. The setting was a rural Zimbabwean community where S. haematobium related lesions were found in 46% of the women, HIV in 29% and herpes simplex type- 2 (HSV-2) in 65%. In permanent residents (>3 years residency), HIV was found in 41% (29/70) of women with laboratory proven genital schistosomiasis as opposed to 26% HIV positive (96/375) in the schistosomal ova negative group [odds ratio (OR), 2.1; 95% confidence interval (CI), 1.2-3.5; P = 0.008. In multivariate analysis S. haematobium infection of the genital mucosa was significantly associated with HIV seropositivity (adjusted OR, 2.9; 95% CI, 1.11-7.5; P = 0.030). All seven women who became HIV positive during the study period (seroincidence 3.1%) had signs of S. haematobium at baseline. In accordance with other studies HIV was significantly associated with HSV-2 (OR, 3.0; 95% CI, 1.7-5.3; P < 0.001), syphilis and human papillomavirus. The highest HIV prevalence (45%) was found in the 25-29 years age group. Women with genital schistosomiasis had an almost three-fold risk of having HIV in this rural Zimbabwean community. Prospective studies are needed to confirm the association.
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            Urogenital schistosomiasis in women of reproductive age in Tanzania's Lake Victoria region.

            We conducted a community-based study of 457 women aged 18-50 years living in eight rural villages in northwest Tanzania. The prevalence of female urogenital schistosomiasis (FUS) was 5% overall but ranged from 0% to 11%. FUS was associated with human immunodeficiency virus (HIV) infection (odds ratio [OR] = 4.0, 95% confidence interval [CI] = 1.2-13.5) and younger age (OR = 5.5 and 95% CI = 1.2-26.3 for ages 35 years). Overall HIV prevalence was 5.9% but was 17% among women with FUS. We observed significant geographical clustering of schistosomiasis: northern villages near Lake Victoria had more Schistosoma mansoni infections (P < 0.0001), and southern villages farther from the lake had more S. haematobium (P = 0.002). Our data support the postulate that FUS may be a risk factor for HIV infection and may contribute to the extremely high rates of HIV among young women in sub-Saharan Africa.
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              Patterns in parasite epidemiology: the peak shift.

              A characteristic relationship between infection and host age, with levels of infection reaching a peak in particular age classes, has been reported for many parasites. However, several field studies have shown that this relationship is not invariant: if age-infection data are compared across host populations, the peak level of infection is higher and occurs at a younger age when the transmission rate is high, and is lower and occurs at an older age when it is low. This pattern is called the ;peak shift'. Here, Mark Woolhouse reviews the evidence for and the implications of the peak shift. The peak shift is consistent with the predictions of mathematical models that assume gradually acquired protective immunity, and this interpretation is supported by experimental studies using animals. This agreement between theory, experimental evidence and field studies strongly suggests that acquired immunity has a major impact on epidemiological patterns not only for parasites such as malaria, where the importance of acquired immunity is not in doubt, but also for many parasitic helminths, where the role of acquired immunity is less widely accepted.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                November 2014
                20 November 2014
                : 8
                : 11
                : e3229
                Affiliations
                [1 ]Norwegian Centre for Imported and Tropical Diseases, Department of Infectious Diseases, Oslo University Hospital Ullevaal, Oslo, Norway
                [2 ]University of Oslo, Oslo, Norway
                [3 ]Imperial College London, London, United Kingdom
                [4 ]Institut Pasteur de Madagascar, Antananarivo, Madagascar
                [5 ]Center for Paediatric and Pregnancy Related Pathology, Department of Pathology, Oslo University Hospital, Oslo, Norway
                [6 ]Research Department, Sorlandet Hospital HF, Kristiansand, Norway
                [7 ]Department for Global Development and Planning, Institute for Development Studies, University of Agder, Kristiansand, Norway
                [8 ]Discipline of Obstetrics and Gynaecology, School of Clinical Medicine, Nelson R. Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa
                [9 ]Department of Gynaecology, Oslo University Hospital Ullevaal, Oslo, Norway
                [10 ]Discipline of Public Health Medicine, Nelson R. Mandela School of Medicine, College of Health Sciences, University of KwaZulu-Natal, Durban, South Africa
                Weill Cornell Medical College, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HMN EFK SDH SGG EK. Performed the experiments: HMN EFK PDN JB PMJ SDH BSR. Analyzed the data: EFK SGG HMN PDN JB BR EK BSR PMJ MO SDH. Contributed reagents/materials/analysis tools: EFK HMN BR EK BSR PMJ MO SDH. Wrote the paper: HMN EFK EK PMJ BR SGG MO BSR JB PDN SDH.

                Article
                PNTD-D-13-01899
                10.1371/journal.pntd.0003229
                4238986
                25412334
                d58b4f3a-d937-42ba-96e0-479c10b136a8
                Copyright @ 2014

                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.

                History
                : 28 November 2013
                : 29 August 2014
                Page count
                Pages: 17
                Funding
                The research leading to these results has received funding from the University of Copenhagen with the support from the Bill & Melinda Gates Foundation (Grant no. OPPGH5344), South-Eastern Norway Regional Health Authority Network project no. 2011073 and 2012032 and European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013)/ERC Grant agreement no. PIRSES-GA-2010-269245. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Diagnostic Medicine
                Infectious Diseases
                Women's Health
                Obstetrics and Gynecology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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