Epidemiology and Social
Association between genital schistosomiasis and HIV in rural Zimbabwean women
Kjetland, Eyrun Fa; Ndhlovu, Patricia Db; Gomo, Exeneviab,c; Mduluza, Takafirab; Midzi, Nicholasc; Gwanzura, Lovemoreb; Mason, Peter Rb,d; Sandvik, Leive; Friis, Henrikf; Gundersen, Svein Gunnarg
From the aCentre for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, Oslo, Norway
bCollege of Health Sciences, University of Zimbabwe
cBlair Research Institute
dBiomedical Research and Training Institute, Harare, Zimbabwe
eCentre for Clinical Research, Ullevaal University Hospital and Medical Faculty, Oslo, Norway
fDepartment of Epidemiology, Institute of Public Health, University of Copenhagen, Denmark
gResearch Unit, Sorlandet Hospital HF/ Agder University College, Kristiansand, Norway.
Received 13 June, 2005
Revised 21 October, 2005
Accepted 1 December, 2005
Correspondence to Eyrun F. Kjetland, Centre for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, 0407 Oslo, Norway. E-mail: firstname.lastname@example.org
Objective: To determine the association between female genital Schistosoma haematobium infection and HIV.
Design and methods: 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%.
Results: 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.
Conclusion: 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.
Two hundred million people in 76 countries have schistosomiasis and 85% of these are on the African continent . Women with urinary Schistosoma haematobium may have lesions on the uterine cervix, in the vagina and on the vulva [2–6]. Furthermore women may have genital schistosomiasis, even without urinary schistosomiasis [7–9]. Genital sandy patches, often accompanied by concomitant blood vessel friability and inflammation, are reportedly pathognomonic for S. haematobium infection, and have been found in up to 46% of the women in high-endemic areas [6,7,9–11].
Women comprise 57% of the HIV-infected population in Africa . Several studies on HIV prevalence have shown an unexplained gender quotient disfavouring rural women [12,13], with 1.3–6.4 HIV-positive women to every man. Furthermore, in rural women the HIV prevalences peak at younger ages, suggesting that risk factors in rural and urban populations may be different [13–15].
Sexually transmitted genital ulcers may provide points of entry for viral transmission [14,16–19]. In epidemiological studies sexually transmitted diseases (STDs) have been associated with increased risk of HIV transmission. No study has scrutinized the possible association between genital schistosomiasis and HIV.
In Africa the highest HIV prevalence rates are found in urban and semi-urban areas . Schistosoma haematobium is transmitted in freshwater bodies and is thus usually a rural phenomenon. The two diseases meet in migrating populations, travellers, commuting spouses and roadside villages , moreover there are now reports of rural HIV epidemics in Africa [12,15,21]. This study sought to assess if there is an association between genital S. haematobium infection and HIV in women in rural Zimbabwe.
MATERIALS AND METHODS
Inclusion and exclusion criteria
A cross-sectional study was conducted in north-western Zimbabwe. All women aged 20–49 years were invited to take part in the study [7,22]. From the area directly around the clinic and at three pick-up points 83% (294/353) attended, but only 33% (233/706) attended from the surrounding areas. As has been described previously women from the pick-up points did not differ from women from the surrounding areas with respect to symptoms or diseases. Virgins, pregnant, postmenopausal and menstruating women were excluded. No schistosomiasis control programme had been done on the adult population.
Inclusion in the study took place after individual informed oral consent. Permission was granted by the provincial and district medical directors, the village headman and at village meetings. Ethical approval was given by the Medical Research Council of Zimbabwe and by the ethical committee of the Special Programme for Research and Training in Tropical Diseases Research, UNDP/WB/WHO. Patients and partners were treated in accordance with the standard Zimbabwean syndromic approach and referred when necessary .
A nurse questioned the women in Shona (the local language) for current and past urogenital symptoms and obstetric history. Clinical investigations were done by one clinician (E.F.K.) as has been described previously . Briefly, at the time the clinician knew neither the HIV result nor the result of S. haematobium examination in urine. Genital surfaces were examined using a photocolposcope after which papanicolaou (Pap) smears were done in all consenting women. Upon suspicion and if the patient agreed, specimens for STD or cancer diagnosis were taken .
Homogenous yellow sandy patches were sandy looking areas with no distinct grains using 15-times magnification [5,7]. Grainy sandy patches portrayed oblong (approximately 0.05 mm by 0.2 mm) grains situated in the mucosa. Neo-vascularization was defined as pathological convoluted (cork-screw), reticular, circular and/or branched, uneven-calibre blood vessels visible (15-times magnification) on the mucosal surface. Contact bleeding was defined as fresh blood originating from the mucosal surface. Body mass index (BMI), used as a surrogate marker for CD4 cell count, was calculated by dividing weight (kg) by height (m)2 [24,25].
Urine samples were examined for S. haematobium ova [7,26]. A single terminal-spined ovum gave a positive diagnosis in Pap smears, wet mounts or biopsies of genital tissue . Wet mounts were taken from consenting women who showed debris or friable, loose and bleeding tissue. As lesions may offer an entry port for HIV, and many women in the area may not be able to decide whether to have intercourse , biopsies were only done in consenting women on clinical indication. Stool was processed by the Kato Katz technique .
Other specimens and laboratory tests
As described in detail previously, examinations for STDs and HIV were carried out last, and only when there was sample material remaining after other examinations [7,22,30]. Women were tested for a median of seven STDs (range, 1–8, selected results below): Serologic tests were run for HIV (29%, 153/523), trichomonas and herpes simplex virus type 2 (HSV-2). HSV-2 was found in 65% (307/476). Current syphilis was determined by the presence of an ulcer and seroconversion. Past syphilis (6%, 30/481) was determined by two serological tests. Cultures were run for Haemophilus ducreyi. Polymerase chain reactions (PCR) were run for H. ducreyi and human papillomavirus (HPV, 33%, 81/236). Trichomoniasis was also tested by microscopic examination, as was candidiasis and Neisseriae gonorrhoeae. Bacterial vaginosis was diagnosed using Nugent's criteria. PCR was run for N. gonorrhoeae and Chlamydia trachomatis (Chlamydia). Pap smears were investigated for cell atypia. Herpes simplex virus type 1 and donovaniasis were not tested due to high and negligible prevalence, respectively.
Chi-squared, Fisher's exact test (for numbers below 5) and odds ratio (OR) with 95% confidence interval (95% CI) were used when comparing prevalence in two groups of subjects. Mann–Whitney U-test was used to compare BMI or age in two groups. In order to study simultaneously the impact of several variables, logistic regression analysis was applied with a 5% significance level; variables were included if the P-value from crude association was less than 0.2 and if the Spearman rank correlation coefficient was below 0.7. Where there were less than 10 cases, the variable was not included in regression analysis. Pap smear was the only laboratory test for S. haematobium ova taken irrespective of findings and was therefore chosen for analysis against other variables . The statistical analysis was computed using Statistical Package for the Social Sciences (SPSS), version 11 (SPSS Inc., Chicago, Illinois, USA).
Baseline schistosomal data have been reported in detail previously [7,22,30]. Briefly 46% (243/527) were found to have genital sandy patches, 44% (231/527) had neo-vascularization, and 23% (122/527) had contact bleeding. Median age was 30 years for HIV-positive, and 36 years for HIV-negative women (P = 0.003). Women between the ages of 25 and 29 years had the highest HIV prevalence (45%). BMI was significantly associated with HIV seropositivity (age adjusted OR, 0.89; 95% CI, 0.8–0.9; P = 0.002).
Genital S. haematobium was the strongest predictor for neo-vascularization, the two types of genital sandy patches, and contact bleeding in multivariate analysis, adjusted for sexually transmitted diseases . Only later did we realize that we should have adjusted for HIV status and age as well. Table 1 shows that adjustment for HIV, age, and length of stay in the area did not have a modifying effect on the association between the lesions and S. haematobium ova. Moreover, in HIV-positive women, BMI did not have modifying effect on the association between these findings and S. haematobium ova; and did not influence the size of the lesions (data not shown).
Length of stay in the area and HIV results was known in 520 women. Further results represent the 479 women who had stayed more than 3 years in the area. HIV was found in 41% (29/70) of women with laboratory-proven genital schistosomiasis as opposed to 26% HIV-positive women (96/375) in the schistosomal ova negative group (OR, 2.1; 95% CI, 1.2–3.5; P = 0.008). Table 2 shows that HIV was significantly associated with homogenous yellow, but not with grainy sandy patches. In the HIV-positive women there was no association between BMI and the listed findings in Table 2 (data not shown, small subgroups). Adjustment for age did not have a modifying effect on the association between the HIV and S. haematobium-related findings in Table 2.
Genital schistosomiasis as a possible cause of infertility will be discussed in detail later (manuscript in preparation). Infertility was significantly associated with S. haematobium in Pap smears, and also when adjusted for age (adjusted OR, 4.2; 95% CI, 1.3–13.9; P = 0.020) and is included in the analysis below. There was no association between S. haematobium and divorce or number of sexual partners (data not shown).
Multivariate analysis of genital schistosomiasis and other predictors for HIV
Table 3 shows that S. haematobium ova in Pap smears were found more frequently in women with HIV. Less than half (42%, 200/479) were tested for HPV, there were less than 10 cases of unskilled paid labour, and there was only one case who had both S. haematobium and past syphilis; thus these variables were excluded from the multivariate model. HIV seropositivity was not significantly with Chlamydia, atypical cells, bacterial vaginosis, candidiasis, or trichomoniasis.
Homogenous yellow sandy patches and urinary schistosomiasis were not included in the multivariate analysis as risk factors for HIV because they were in the same causal pathway as S. haematobium ova found in Pap smears (Table 1). However, when tested in the same multivariate analysis (instead of Pap smears), homogenous yellow sandy patches remained a significant predictor for HIV (adjusted OR, 1.7; 95% CI, 1.04–2.8; P = 0.044). Urinary S. haematobium ova excretion however, was not significantly associated with HIV (adjusted OR, 1.4; 95% CI, 0.8–2.2; P = 0.23). Schistosoma mansoni infection, other STDs, divorce, religion, and tribe did not influence the associations.
Genital schistosomiasis and HIV seroconversion
Twelve months after baseline seven of the 224 re-investigated HIV-negative women had become HIV positive (incidence 3.1%); six of them had been treated with praziquantel at baseline. The median age was 28 years for seroconverters, and 38 for HIV-negative women (P = 0.056), six were married and one was divorced. All seven women had S. haematobium-related findings before seroconversion as opposed to 65% (142/217) of women who remained HIV negative (P = 0.098). Sandy patches were found in five of the seven women before seroconversion. The two women who did not have any genital schistosomal findings, had urinary schistosomiasis. All seroconverted women had a rural childhood and current regular water body contact. There were no significant differences for the STDs between the seroconverters and the 217 women who did not become HIV positive. Two women were found to be seropositive for HSV-2. However at baseline or at 3 months, none of the seroconverted women had vesicles, ulcers, erosions, fissures, vaginal discharge, leukoplakia or tumours. Baseline laboratory analyses of the seroconverted showed no current or past syphilis, HPV, atypical cells, gonorrhoea, bacterial vaginosis, candidiasis, or trichomoniasis in smears.
Newcomers to the area
Forty-one women had stayed 3 years, or less in the area. They were more often single (P = 0.068) and infertile (P = 0.073), and the median age was 23 years as opposed to 36 years in the rest (P < 0.001). They were more often farm labourers (P = 0.013), had more Chlamydia (P < 0.006), trichomoniasis (P = 0.015) and current syphilis (P = 0.10) than the rest of the women. Moreover newcomers were more often from an urban area (P = 0.003) and had less childhood water body contact (P = 0.003) than the women who had stayed for a longer time in the study area. Homogenous yellow sandy patches and S. haematobium ova were found in 12 and one cases, respectively; none were associated with HIV seropositivity (P = 0.17 and P = 1.0, respectively, numbers were small).
Death, HIV and genital schistosomiasis
Twelve of 527 people had passed away 12 months after the baseline investigation. Although the cause of death was not known, 11 of these had been HIV positive at baseline (OR for HIV seropositivity in the dead, 26; 95% CI, 3.3–203; P = 0.002). Seven of the deceased had an S. haematobium-related finding at baseline (P = 0.67). The median age was 33 years for deceased and 35 years for live women. Of the women who had passed away five had urinary S. haematobium ova excretion at baseline and five had homogenous yellow sandy patches. Only one had grainy sandy patches, and only one of the deceased had S. haematobium ova (by biopsy); four of them had been biopsied.
Women with S. haematobium ova in Pap smears had a three-fold risk of having HIV in this rural Zimbabwean population. The association remained highly significant after controlling for established risk factors [15,18,21]. All seven women in this rural area, who became HIV positive had signs of S. haematobium infection at baseline. Homogenous yellow sandy patches were also significantly associated with HIV in multivariate analysis. As has been reported previously women in the age group 25–29 years had the highest HIV infection prevalence . Furthermore the study confirmed HSV-2, past syphilis and HPV were also significantly associated with HIV [15,18,30,31]. The study confirms that excretion or presence of S. haematobium ova in urine is not exacerbated in HIV-positive women [32–34]. Although the associations are significant, some confidence intervals are wide and there has been multiple statistical testing; results must therefore be interpreted with caution.
Does HIV have an effect on the presence of ova in Pap smears?
The Pap smear test method is an insensitive test method for S. haematobium ova, reflected in the wide confidence interval in its correlation with HIV [7,35]. Low CD4 cell count has been suggested to increase susceptibility to schistosomal re-infection after treatment . It is not known if low CD4 cell count exacerbates genital schistosomiasis or increases susceptibility to primary acquisition of schistosomiasis. However, newcomers did not have more S. haematobium-related findings than permanent residents. Furthermore HIV neither influenced the association between S. haematobium ova and the sandy patches, neo-vascularization or contact bleeding, nor was there an association, in the HIV-positive women, between BMI (as a surrogate marker for CD4 cell count [24,25]) and clinical or laboratory-proven genital schistosomiasis. CD4 cell counts were regrettably unknown in this study. Most women had to walk a distance to the clinic or to a vehicle, we therefore cannot preclude that women with AIDS are under-represented although a number of women reported having had recurrent herpes zoster and oral thrush, and although geographical subgroups of women were similar with respect to reproductive tract diseases . Eleven women with HIV passed away during the study period and it is likely that this group had lower CD4 cell counts than the HIV-negative women. However, the deceased neither had more positive Pap smears, nor more homogenous yellow sandy patches than the HIV-negative women. Treatment for urinary schistosomiasis has been found equally effective in HIV-positive and HIV-negative individuals . Moreover, other studies have shown that schistosomal ova excretion rates are lower, not higher in HIV-positive patients, or comparable in HIV-positive and HIV-negative individuals [32–34,38,39]. Schistosomal disease such as liver fibrosis is reportedly not exacerbated in HIV-positive individuals . We therefore find it likely that the significantly higher prevalence of genital schistosomiasis, in HIV-positive individuals, is caused by persistent schistosomal disease from before HIV infection , rather than HIV catalysis of genital ova excretion to the mucosal surface.
It is not possible to determine cause and effect of HIV in a cross-sectional study . HIV infection has occurred, at an unknown point in time, possibly in a different phase and hypothetically in the absence of schistosomal disease. In adult women, however, there is no difference in genital schistosomiasis in the different age groups [7,9]. It is therefore likely that most local rural women already had schistosomiasis at the time of HIV transmission [7,9,41].
Genital schistosomiasis as a cause of promiscuous behaviour
Previous papers have suggested that genital schistosomiasis is the cause of infertility [8,10]. In addition it has been suggested that women may be less attractive sexual partners due to events such as dyspareunia or post-coital bleeding . Schistosoma-positive and negative groups showed comparable divorce rates and numbers of sexual partners. The partner HIV status was not known and a woman's schistosomal disease may have been severe, but she would not have been at risk of HIV if her partner were HIV negative. Women in this area claimed that infertility led husbands to have out-of-wedlock sexual relationships. However, the effect of infertility on HIV transmission has been controlled for in this paper and the comparable divorce and partner rates in women with and without genital schistosomiasis make it unlikely that husband HIV status would have a confounding effect in our study population although we cannot completely preclude it.
Transmission of HIV to women
There is a considerable degree of mucosal change such as sandy patches, contact bleeding and proliferated blood vessels associated with S. haematobium ova deposition in the female reproductive organs [7,11,42,43]. Surrounding each ovum or cluster of ova there may be Langerhans cells, eosinophils, neutrophils, plasma cells, fibroblasts, macrophages and T cells with schistosoma-induced higher density of CCR5 and CXCR4 HIV-receptors on the cells [41,42,44–46]. Feldmeier et al. have hypothesized that HIV in semen may attain easy access through the friable and eroded epithelium or through broken vessels, during coitus, creating direct points of contact between the HIV virus and the receptive cells of the woman .
Transmission of HIV to men
Furthermore, HIV has been demonstrated in genital ulcer exudates [40,48,49] and this may hold true for schistosomal lesion exudates as well. Women with genital schistosomiasis may pose an additional risk of HIV transmission to their male sexual partners. Genital HIV-RNA excretion has been shown to decrease after treatment of other reproductive tract diseases [19,50,51]. However no study has investigated the effect of vaginal HIV viral load after treatment of female genital schistosomiasis, and no study has investigated the transmission of HIV from ‘schistosomal women’ to men.
Genital sandy patches, was the commonest current genital lesion in this population and was found in almost half of the women, 29% had homogenous yellow sandy patches [7,22]. Hence S. haematobium may be hypothesized to predominate as a cause of mucosal susceptibility in certain geographic areas. In S. haematobium endemic areas HIV may have spread with genital schistosomiasis, rather than STDs, as an essential risk factor for heterosexual transmission [7,38,47].
The economic burden of the HIV/ AIDS epidemic has made it difficult for many countries to invest in schistosomiasis control . This study indicates that schistosomiasis control – possibly starting in the young girls  – may perhaps be an important auxiliary in the current prevention programmes for HIV. The possibility of reduced HIV transmission in schistosomiasis endemic areas adds new intervention points in the battle against HIV on the behavioural aspects and on the development of sanitary infrastructures. Prospective studies however, are needed to confirm whether genital S. haematobium infection indeed poses a risk factor for HIV transmission to women. In addition, the effect of female genital schistosomiasis, as a risk factor for HIV transmission to men, needs to be explored.
The authors are grateful for the financial support received. Technical, medical, statistical or cultural assistance were provided by the Provincial Medical Director and Supervisor, Dr L. Charimari, Mupfure community and the councillor and staff at Madziwa, Harare Central and Mt. Darwin Hospitals, personnel from Blair Research Laboratory, Dr T. Magwali and Professor B. Myrvang. We are indebted to the Medical Research Council of Zimbabwe, staff and headmistress of Mupfure Secondary School, and the following indispensable people: sisters J. Chikoore, E. N. Kurewa and late sister P. Dungare, village health workers, environmental health technicians, and in particular N. Taremeredzwa, C. Mukahiwa, W. Mashange, R. Manyaira, and T. Mushipe for prolonged hard work under very difficult circumstances.
Sponsorship: Financial support was granted by UNDP/ World Bank/ WHO Special Programme for Research and Training in Tropical Diseases, Danish Bilharziosis Laboratory, Norwegian Research Council, NORAD and Ullevaal University Hospital: Research Forum, Department of Infectious Diseases and Centre for Imported and Tropical Diseases.
2. Renaud G, Devidas A, Develoux M, Lamothe F, Bianchi G. Prevalence of vaginal schistosomiasis caused by Schistosoma haematobium
in an endemic village in Niger. Trans R Soc Trop Med Hyg 1989; 83:797–797.
3. Leutscher P, Ravaoalimalala VE, Raharisolo C, Romarokoto CE, Rasendramino M, Roabelison A, et al
. Clinical findings in female genital schistosomiasis in Madagascar. Trop Med Int Health 1998; 3:327–332.
4. Kjetland EF, Poggensee G, Helling-Giese G, Richter L, Sjastad A, Chitsulo L, et al
. Female genital schistosomiasis due to Schistosoma haematobium
. Clinical and parasitological findings in women in rural Malawi. Acta Trop 1996; 62:239–255.
5. Badawy A. Schistosomiasis of the cervix. BMJ 1962; 5275:369–372.
6. Gibson RWB. Bilharziasis of the female genital tract. Med J SA 1925; 21:44–45.
7. Kjetland EF, Ndhlovu PD, Mduluza T, Gomo E, Gwanzura L, Mason PR, et al
. Simple clinical manifestations of genital Schistosoma haematobium
infection in rural Zimbabwean women. Am J Trop Med Hyg 2005; 72:311–319.
8. Bland KG, Gelfand M. The effects of schistosomiasis on the fallopian tubes in the African female. J Obs Gyn Br Com 1970; 77:1024–1027.
9. Poggensee G, Kiwelu I, Weger V, Goppner D, Diedrich T, Krantz I, Feldmeier H. Female genital schistosomiasis of the lower genital tract: prevalence and disease-associated morbidity in Northern Tanzania. J Infect Dis 2000; 181:1210–1213.
10. Friedberg D, Berry A, Schneider J. Schistosomiasis of the female genital tract. Med J SA 1991; 8:S1–S16.
11. Freedman D, Ottesen E. Eggs of Schistosoma mansoni
stimulate endothelial cell proliferation in vitro. J Infect Dis 1988; 158:556–562.
12. WHO, UNAIDS. AIDS epidemic update
. Geneva: WHO/UNAIDS; 2004. p. 87.
13. Barongo L, Borgdorff MW, Mosha FF, Nicoll A, Grosskurth H, Senkoro KP, et al
. The epidemiology of HIV -1 infection in urban areas roadside settlements and rural villages in Mwanza Region, Tanzania. AIDS 1992; 6:1521–1528.
14. Nunn AJ, Kengeya-Kayondo JF, Malamba SS, Seeley JA, Mulder DW. Risk factors for HIV-1 infection in adults in a rural Ugandan community: a population study. AIDS 1994; 8:81–86.
15. Grosskurth H, Mosha F, Todd J, Senkoro K, Newell J, Klokke A, et al
. A community trial of the impact of improved sexually transmitted disease treatment on the HIV epidemic in rural Tanzania: 2. Baseline survey results. AIDS 1995; 9:927–934.
16. Cohen MS. Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet 1998; 351:5–7.
17. Wald A, Link K. Risk of human immunodeficiency virus in herpes simplex virus type 2-serpositive persons: a meta-analysis. J Infect Dis 2002; 185:45–52.
18. Corey L, Wald A, Celum C, Quinn TC. The effects of herpes simplex virus-2 on HIV-1 acquistion and transmission: a review of two overlapping epidemics. J Acquir Immune Defic Syndr 2004; 35:435–445.
19. Orroth KK, Gavyole A, Todd J, Mosha F, Ross D, Mwijarubi E, et al
. Syndromic treatment of sexually transmitted diseases reduces the proportion of incident HIV infections attributable to these diseases in rural Tanzania. AIDS 2000; 14:1429–1437.
20. Serwadda D, Wawer MJ, Musgrave SD, Sewankambo NK, Kaplan JE, Gray RH. HIV risk factors in three geographic strata of rural Rakai District, Uganda. AIDS 1992; 6:983–989.
21. Gregson S, Mason PR, Garnett GP, Zhuwau T, Nyamukapa CA, Anderson RM, Chandiwana SN. A rural HIV epidemic in Zimbabwe? Findings from a population-based survey. Int J STD AIDS 2001; 12:189–196.
22. Kjetland EF, Gwanzura L, Ndhlovu PD, Mduluza T, Gomo E, Mason PR, et al
. Herpes simplex virus type 2 prevalence of epidemic proportions in rural Zimbabwean women: association with other sexually transmitted infections. Arch Gynecol Obstet 2005; 272:67–73.
23. EDLIZ. Essential drugs list and standard treatment guidelines for Zimbabwe
. 1998. 3 ed. Harare, Zimbabwe: NDTPAC.
24. van der Sande MA, Schim van der Loeff MFS, Aveika AA, Sabally S, Togun T, Sarge-Nije R, et al
. BMI predicts survival as well as <200 CD4s body mass index at time of HIV diagnosis: A strong and independent predictor of survival, as strong as <200 CD4 count. J Acquir Immune Defic Syndr 2004; 37:1288–1294.
25. Jones CY, Hogan JW, Snyder B, Klein RS, Rompalo A, Schuman P, et al
. Overweight and human immunodeficiency virus (HIV) progression in women: associations HIV disease progression and changes in body mass index in women in the HIV epidemiology research study cohort. Clin Infect Dis 2003; 37:S69–S80.
26. Doehring E, Feldmeier H, Dafalla AA. Day-to day variation and circadian rhythm of egg excretion in urinary schistosomiasis in the Sudan. Ann Trop Med Parasitol 1983; 77:587–594.
27. Peters PA, El Alamy MA, Warren KS, Mahmod AA. Quick Kato for field quantification of S.mansoni
eggs. Am J Trop Med Hyg 1980; 29:217–219.
28. Swart PJ, van der Merwe JV. Wet-smear diagnosis of genital schistosomiasis. Med J SA 1987; 72:631–632.
29. Hindin MJ. Understanding women's attitudes towards wife beating in Zimbabwe. Bull WHO 2003; 81:501–508.
30. Baay MFD, Kjetland EF, Ndhlovu PD, Deschoolmeester V, Mduluza K, Gomo E, et al
. Human papillomavirus in a rural community in Zimbabwe: the impact of HIV co-infection on HPV genotype distribution. J Med Virol 2004; 73:481–485.
31. Brinkman JA, Jones WE, Gaffga AM, Sanders JA, Chaturvedi AK, Slavinsky J III, et al
. Detection of human papillomavirus DNA in urine specimens from human immunodeficiency virus-positive women. J Clin Microbiol 2002; 40:3155–3161.
32. Kallestrup P, Zinyama R, Gomo E, Butterworth AE, van Dam GJ, Erikstrup C, Ullum H. Schistosomiasis and HIV-1 infection in rural Zimbabwe: implications of coinfection for excretion of eggs. J Infect Dis 2005; 191:1311–1320.
33. Mwanakasale V, Vounatsou P, Sukwa TY, Ziba M, Ernest A, Tanner M. Interactions between Schistosoma haematobium
and human immunodeficiency virus type 1: the effects of coinfection on treatment outcomes in rural Zambia. Am J Trop Med Hyg 2003; 69:420–428.
34. N'Zoukoudi-N'Doundou MY, Dirat I, Akouala JJ, Penchenier L, Makuwa M, Rey JL. [Bilharziasis and human immunodeficiency virus infection in Congo]. Med Trop 1995; 55:249–251.
35. Poggensee G, Sahebali S, Van Marck E, Swai B, Krantz I, Feldmeier H. Diagnosis of genital cervical schistosomiasis: comparison of cytological, histopathological and parasitological examination. Am J Trop Med Hyg 2001; 65:233–236.
36. Karanja DM, Hightower AW, Colley DG, Mwinzi PN, Galil K, Andove J, Secor WE. Resistance to reinfection with Schistosoma mansoni
in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 2002; 360:592–596.
37. Karanja DM, Boyer AE, Strand M, Colley DG, Nahlen BL, Ouma JH, Secor WE. Studies on schistosomiasis in western Kenya: II. Efficacy of praziquantel for treatment of schistosomiasis in persons coinfected with human immunodeficiency virus-1. Am J Trop Med Hyg 1998; 59:307–311.
38. Secor WE, Karanja DM, Colley DG. Interactions between schistosomiasis and human immunodeficiency virus in Western Kenya. Mem Inst Oswaldo Cruz 2004; 99:93–95.
39. Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE. Studies on schistosomiasis in western Kenya: I. Evidence for immune- facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 1997; 56:515–521.
40. Grosskurth H, Gray R, Hayes R, Mabey D, Wawer M. Control of sexually transmitted diseases for HIV-1 prevention: understanding the implications of the Mwanza and Rakai trials. Lancet 2000; 355:1981–1987.
41. Secor WE, Shah A, Mwinzi PM, Ndenga BA, Watta CO, Karanja DM. Increased density of human immunodeficiency virus type 1 coreceptors CCR5 and CXCR4 on the surfaces of CD4(+) T cells and monocytes of patients with Schistosoma mansoni
infection. Infect Immun 2003; 71:6668–6671.
42. Berry A. Evidence of gynecologic bilharziasis in cytologic material. A morphologic study for cytologists in particular. Acta Cytol 1971; 15:482–498.
43. El-Zeneiny AH, Badawy SZ, Iskander SG. Bilharziasis of the female genital tract. J Egypt Med Assoc 1968; 51:543–553.
44. Helling-Giese G, Sjaastad A, Poggensee G, Kjetland EF, Richter J, Chitsulo L, et al
. Female genital schistosomiasis (FGS): relationship between gynecological and histopathological findings. Acta Trop 1996; 62:257–267.
45. Wright ED, Chipangwi J, Hutt MSR. Schistosomiasis of the female genital tract. A histopathological study of 176 cases from Malawi. Trans R Soc Trop Med Hyg 1982; 76:822–829.
46. El- Shoura SM. Human Bilharzial ureters III. Fine structure of egg granuloma. Appl Parasitol 1993; 34:265–273.
47. Feldmeier H, Krantz I, Poggensee G. Female genital schistosomiasis as a risk-factor for the transmission of HIV. AIDS 1994; 8:368–372.
48. Ghys PD, Fransen K, Diallo MO, Ettiegne-Traore V, Coulibaly IM, Yeboue KM, et al
. The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Cote d'Ivoire. AIDS 1997; 11:F85–F93.
49. Lawn SD, Subbarao S, Wright TC Jr, Evans-Strickfaden T, Ellerbrock TV, Lennox JL, et al
. Correlation between human immunodeficiency virus type 1 RNA levels in the female genital tract and immune activation associated with ulceration of the cervix. J Infect Dis 2000; 181:1950–1956.
50. Wang CC, McClelland RS, Reilly M, Overbaugh J, Emery SR, Mandaliya K, et al
. The effect of treatment of vaginal infections on shedding of human immunodeficiency virus type 1. J Infect Dis 2001; 183:1017–1022.
51. Mayaud P, McCormick D. Interventions against sexually transmitted infections (STI) to prevent HIV infection. Br Med Bull 2001; 58:129–153.
52. WHO. Report of the WHO informal consultation on schistosomiasis control
. Geneva: WHO; 1998. pp. 1–45.
53. Kjetland EF, Mduluza T, Ndhlovu PD, Gomo E, Gwanzura L, Midzi N, et al
. Genital schistosomiasis in women - a clinical in vivo 12-months' study following treatment with praziquantel. Trans R Soc Trop Med Hyg
2005; in press.
This article has been cited 49 time(s).
Journal of the International AIDS SocietyMeasuring and modelling concurrencyJournal of the International AIDS Society
Plos Neglected Tropical DiseasesPotential Cost-Effectiveness of Schistosomiasis Treatment for Reducing HIV Transmission in Africa - The Case of Zimbabwean WomenPlos Neglected Tropical Diseases
Plos Neglected Tropical DiseasesS-haematobium as a Common Cause of Genital Morbidity in Girls: A Cross-sectional Study of Children in South AfricaPlos Neglected Tropical Diseases
Tropical Medicine & International HealthHIV and Schistosoma haematobium prevalences correlate in sub-Saharan AfricaTropical Medicine & International Health
Clinical Infectious DiseasesEfficacy of Mefloquine Intermittent Preventive Treatment in Pregnancy Against Schistosoma haematobium Infection in Gabon: A Nested Randomized Controlled Assessor-Blinded Clinical TrialClinical Infectious Diseases
Proceedings of the National Academy of Sciences of the United States of AmericaCost-effectiveness of a community-based intervention for reducing the transmission of Schistosoma haematobium and HIV in AfricaProceedings of the National Academy of Sciences of the United States of America
Infectious Disease Clinics of North AmericaFever of unknown origin due to zoonosesInfectious Disease Clinics of North America
Plos Neglected Tropical DiseasesHelminth-HIV Coinfection: Should We Deworm?Plos Neglected Tropical Diseases
Neglected Tropical Diseases 2 Integration of control of neglected tropical diseases into health-care systems: challenges and opportunities
Revista Da Sociedade Brasileira De Medicina Tropical
Schistosomiasis mansoni in the seminal vesicle
Revista Da Sociedade Brasileira De Medicina Tropical, 40(3):
World Journal of GastroenterologyHelminth infections and intestinal inflammationWorld Journal of Gastroenterology
NatureNeglected disease boostNature
Journal of Clinical InvestigationHelminth infections: the great neglected tropical diseasesJournal of Clinical Investigation
American Journal of Tropical Medicine and HygieneSchistosomiasis PCR in Vaginal Lavage as an Indicator of Genital Schistosoma haematobium Infection in Rural Zimbabwean WomenAmerican Journal of Tropical Medicine and Hygiene
Archives of Gynecology and ObstetricsExploring the feasibility and possible efficacy of mass treatment and education of young females as schistosomiasis influences the HIV epidemicArchives of Gynecology and Obstetrics
Journal of Biological SystemsModeling the Effects of Schistosomiasis on the Transmission Dynamics of Hiv/AIDSJournal of Biological Systems
Trends in ParasitologyRecent progress in integrated neglected tropical disease controlTrends in Parasitology
International Journal of Std & AIDSPolitical determinants of variable aetiology resonance: explaining the African AIDS epidemicsInternational Journal of Std & AIDS
New England Journal of Medicine
Current concepts - Control of neglected tropical diseases
New England Journal of Medicine, 357():
Bulletin of the World Health OrganizationGlobal trends in schistosomiasis controlBulletin of the World Health Organization
Journal of Infectious DiseasesHIV and parasitic infection and the effect of treatment among adult outpatients in MalawiJournal of Infectious Diseases
Clinical Infectious DiseasesCoinfection with HIV and tropical infectious diseases. II. Helminthic, fungal, bacterial, and viral pathogensClinical Infectious Diseases
Plos Neglected Tropical DiseasesNeglected Tropical Diseases in Sub-Saharan Africa: Review of Their Prevalence, Distribution, and Disease BurdenPlos Neglected Tropical Diseases
Development and Change
Understanding the Southern African 'Anomaly': Poverty, Endemic Disease and HIV
Development and Change, 41(2):
Clinical Infectious DiseasesCoexistence of urogenital schistosomiasis and sexually transmitted infection in women and men living in an area where Schistosoma haematobium is endemicClinical Infectious Diseases
Tropical Medicine & International HealthFemale genital schistosomiasis - a differential diagnosis to sexually transmitted disease: genital itch and vaginal discharge as indicators of genital Schistosoma haematobium morbidity in a cross-sectional study in endemic rural ZimbabweTropical Medicine & International Health
Mucosal ImmunologyAn African perspective on mucosal immunity and HIV-1Mucosal Immunology
Neglected tropical diseases and HIV/AIDS
Plos Neglected Tropical DiseasesAfrica's 32 Cents Solution for HIV/AIDSPlos Neglected Tropical Diseases
Transactions of the Royal Society of Tropical Medicine and HygieneAscaris, co-infection and allergy: the importance of analysis based on immunological variables rather than egg excretionTransactions of the Royal Society of Tropical Medicine and Hygiene
Nature Clinical Practice UrologyUrologic complications of HIV and AIDSNature Clinical Practice Urology
Bmc Infectious DiseasesDownregulation of MIP-1 alpha/CCL3 with praziquantel treatment in Schistosoma haematobium and HIV-1 co-infected individuals in a rural community in ZimbabweBmc Infectious Diseases
The helminth HIV connection: time to act
Feminist EconomicsRace, Sex, and the Neglected Risks for Women and Girls in Sub-Saharan AfricaFeminist Economics
Indian Journal of Experimental Biology
Malaria vaccine: Latest update and challenges ahead
Indian Journal of Experimental Biology, 47(7):
HIV Incidence in Sub-Saharan Africa: A Review of Available Data with Implications for Surveillance and Prevention Planning
AIDS Reviews, 11(3):
Plos Neglected Tropical DiseasesEmpowering Women and Improving Female Reproductive Health through Control of Neglected Tropical DiseasesPlos Neglected Tropical Diseases
ParasitologySchistosomiasis control in Africa: 8 years after World Health Assembly Resolution 54.19Parasitology
Parasite ImmunologyHelminths and HIV infection: epidemiological observations on immunological hypothesesParasite Immunology
Microbes and InfectionImmune interactions in malaria co-infections with other endemic infectious diseases: implications for the development of improved disease interventionsMicrobes and Infection
ParasitologyA wake up call for urinary schistosomiasis: reconciling research effort with public health importanceParasitology
Plos Neglected Tropical DiseasesSchistosomiasis in Africa: An Emerging Tragedy in Our New Global Health DecadePlos Neglected Tropical Diseases
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivCofactor infections and HIV epidemics in developing countries: implications for treatmentAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
Clinical Microbiology ReviewsCurrent status of vaccines for schistosomiasisClinical Microbiology Reviews
Transactions of the Royal Society of Tropical Medicine and HygienePrevalence of urinary schistosomiasis and HIV in females living in a rural community of Zimbabwe: does age. matter?Transactions of the Royal Society of Tropical Medicine and Hygiene
American Journal of Tropical Medicine and Hygiene
Prevention of gynecologic contact bleeding and genital sandy patches by childhood anti-schistosomal treatment
American Journal of Tropical Medicine and Hygiene, 79(1):
Tropical Medicine & International HealthDetectable urogenital schistosome DNA and cervical abnormalities 6 months after single-dose praziquantel in women with Schistosoma haematobium infectionTropical Medicine & International Health
AIDS Research and TherapySeroprevalence of Schistosomiasis and Strongyloides infection in HIV-infected patients from endemic areas attending a European infectious diseases clinicAIDS Research and Therapy
Current Opinion in Infectious DiseasesSchistosomiasis: challenges for control, treatment and drug resistanceCurrent Opinion in Infectious Diseases
Schistosoma haematobium; genital schistosomiasis; HIV; women; sexually transmitted diseases; sandy patch; Africa
© 2006 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.