Transactions of the Royal Society of Tropical Medicine and Hygiene (2007) 101, 433—438

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Prevalence of urinary schistosomiasis and HIV infemales living in a rural community of Zimbabwe:does age matter?

P.D. Ndhlovua,∗, T. Mduluzab, E.F. Kjetlandc, N. Midzid, L. Nyangab,S.G. Gundersene, H. Friis f, E. Gomod

a Department of Medical Laboratory Sciences, University of Zimbabwe, Harare, Zimbabweb Department of Biochemistry, University of Zimbabwe, Harare, Zimbabwec Centre for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, Oslo, Norwayd Blair Research Laboratories, Ministry of Health, Harare, Zimbabwee Research Unit, Sorlandet Hospital/Agder University College, Kristiansand, Norwayf Department of Epidemiology, Institute of Public Health, University of Copenhagen, Copenhagen, Denmark

Received 29 June 2006; received in revised form 16 August 2006; accepted 17 August 2006Available online 24 October 2006

KEYWORDSSchistosomahaematobium;Urinaryschistosomiasis;HIV;

Summary A cross-sectional study was conducted on 544 women living in Mupfure rural areaof Zimbabwe to determine whether infection with urinary schistosomiasis is associated withHIV infection. Schistosoma haematobium infection was examined in urine samples and HIVinfection was determined in sera. The prevalence of S. haematobium infection was highest(60%) in women below 20 years of age and declined to 29% in the oldest age group (test fortrends, P < 0.001). Overall, women infected with urinary schistosomiasis had an HIV prevalence

Immune system;Age;Zimbabwe

of 33.3%, whilst women without urinary schistosomiasis had an HIV prevalence of 25.6% (�2,P = 0.053). Women above the age of 35 years and infected with urinary schistosomiasis had asignificantly higher HIV prevalence (37.5%) than those without urinary schistosomiasis (16.8%;�2, P < 0.001).© 2006 Royal Society of Tropicareserved.

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Biapproximately 60%, whilst the HIV prevalence is >27%

∗ Corresponding author. Present address: Metabolic and Clinica

Trials Unit, Department of Mental Health Sciences, Royal Free andUniversity College Medical School, Hampstead Campus, Rowland HillStreet, London NW3 2PF, UK. Tel.: +44 20 7794 0500x33951;fax: +44 20 7830 2808.

E-mail address: p.ndhlovu@medsch.ucl.ac.uk (P.D. Ndhlovu).

iWcr

0035-9203/$ — see front matter © 2006 Royal Society of Tropical Medicindoi:10.1016/j.trstmh.2006.08.008

l Medicine and Hygiene. Published by Elsevier Ltd. All rights

. Introduction

oth Schistosoma haematobium and HIV are highly endemicn Zimbabwe. The prevalence of S. haematobium is

n the general population (Ministry of Health and Childelfare, 2002). Although S. haematobium is not a major

ause of mortality, a combination of both diseases mayesult in untoward suffering, especially in developing

e and Hygiene. Published by Elsevier Ltd. All rights reserved.

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ountries that are presently feeling the strain of the HIVpidemic.

The major effector mechanism in schistosomiasis is anntibody-dependent cell-mediated cytotoxicity where CD4ells are active (Capron and Capron, 1986). The HIV virusnfects the immune system through cells bearing the CD4eceptor molecule, which then interacts with the viral enve-ope glycoprotein gp120 (Dalgleish et al., 1984). Further-ore, lesions created by the schistosome egg granuloma

n the genitals may make women susceptible to HIV trans-ission (Feldmeier et al., 1995a; Kjetland et al., 2005;

oggensee et al., 1998). Moreover, Th2 cytokine responsesredominate in schistosomiasis infection, whereas for opti-al resistance to HIV a predominantly Th1 response is

equired (Mduluza et al., 2003). It is therefore possiblehat helminth infections such as schistosomiasis may reduceesistance to HIV infection. It may be hypothesised that inopulations where helminth infections are common, viraload levels may be higher, as are the risks of transmissionand progression). Thus, people living in a schistosomiasis-ndemic area may be more prone to HIV infection than thosen non-endemic areas (Bundy et al., 2000; Kjetland et al.,006). According to Feldmeier et al. (1993), women mayave a higher schistosomiasis prevalence than men owing toraditional gender roles with regard to water contact.

Similarly, there is a well-known HIV gender quotient dis-avouring rural women in particular, with a reported ratiof 1 man to 3.2 women (Barongo et al., 1992; Denhe et al.,992; Nunn et al., 1994; UNAIDS/WHO, 2004).

Cooper et al. (2000) have reported that the helminthscaris lumbricoides polarises the immune response in youngdults, suppresses IL-2 and may thus impair immune pro-ection against HIV transmission. Furthermore, Bundy et al.2000) have suggested that helminth infections in generalight increase HIV transmission because the cellular immu-

ity needed to combat the virus may be downregulatedy predominantly T-helper 2 cell activation during chronicnfestation by helminths. Several authors have suggestedhat prevention of helminthiasis could be part of the solu-ion to the HIV/AIDS pandemic (Fincham, 2001, 2003; Hotezt al., 2006). Hence, as part of efforts to reduce HIV trans-ission, treatment of helminth infections in HIV-negativeatients has been suggested as a complementary measure.reatment of schistosomiasis in HIV-positive patients haseen hypothesised to decrease HIV viral load, to reverseenital lesions and hence indirectly to decrease the riskf HIV transmission (Feldmeier et al., 1995b; Kallestrup etl., 2005). However, a short-term assessment of viral load inenya and Uganda does not confirm these hypotheses (Brownt al., 2005; Lawn et al., 2000).

As a first step towards ascertaining whether urinary schis-osomiasis is a risk factor for HIV, our study sought to inves-igate the prevalence of HIV and urinary schistosomiasis inomen of different age groups living in an area endemic forrinary schistosomiasis.

. Materials and methods

.1. Study area and population

he study was conducted in Shamva district, Mupfureural area, situated in Mashonaland Central Province of

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imbabwe. The prevalence of S. haematobium in the areas 90% (Ndhlovu et al., 1996). Details of the study areaave been described by Kjetland et al. (2005). Briefly, thetudy area receives ample rains. A river runs through theillages during the hot dry season where abundant waterontact activities take place. No schistosomiasis controlrogramme had taken place on the adult population prioro this study. Some men and women reportedly frequentedtown growth point, 10 km from Mupfure, where activities

avouring prostitution take place.Permission to conduct the study was obtained from the

edical Research Council of Zimbabwe, which gives ethicalpproval for all studies involving human subjects. Approvalas also granted by the ethical committee of the Specialrogramme for Research and Training in Tropical DiseasesTDR), UNDP/WB/WHO. Further permission was sought andranted by the Provincial Medical Director of Mashonalandentral Province of Zimbabwe, the village administratorsnd the women.

Women aged 15—49 years who gave consent to an HIVest and gynaecological examination, who had not gonehrough the menopause and who were sexually activeere included in the study. Prior to consent, women were

nformed about HIV testing by the research nurses trainedn counselling. Post-test counselling was also given beforehe women were given the HIV results if they wished tonow them. All included and excluded women found toe positive for schistosomiasis were treated with a singleose of praziquentel at 40 mg/kg body weight. Womenith symptoms or signs of other diseases were treatedr referred in accordance with the Zimbabwean standardyndromic approach (EDLIZ, 1998).

.2. Parasitology

rom each individual, urine samples were collected on threeonsecutive days. Urine specimens were examined by theltration technique (Mott, 1983). For each woman, infection

ntensity was calculated from the mean of the three sampleser 10 ml of urine. One stool sample was examined usingato—Katz smears (Katz et al., 1972).

.3. Serology for HIV

en millilitres of blood was collected from the cubital vein.he blood was allowed to clot, spun at 300 × g to obtainerum and was stored at −20 ◦C until tested for HIV. Forhe HIV test, the Genelavia Mixt (Sanofi, Marne-la-Coquette,rance) HIV-1/2 ELISA method was used following the manu-acturer’s instructions. The second test was the RecombigenIV-1/2 enzyme immunoassay (Trinity Biotech, Dublin, Ire-

and), which uses genetically engineered solid phase antigen24, gp41 and gp120 for HIV-1 and gp41 and gp120 for HIV-2.n cases of discrepant results, a further test was done withhe Vironostica (Organon Technika, Boxtel, Holland).

.4. Demography

nurse questioned the women in Shona (the local language)or urogenital symptoms, obstetric history, and current and

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Urinary schistosomiasis and HIV in females in Zimbabwe

past sexually transmitted infections. One clinician, blindedto the HIV status of the women, examined all the womenand, if the woman wished, the husband was asked for per-mission, informed by letter or by direct communication. Theinvestigation was finalised by bimanual vaginal examination(Kjetland et al., 2005).

2.5. Data analysis

The results on dichotomous variables were presented asprevalence levels. �2 statistics were used to compare preva-lences in different age groups, whereas �2 statistics for trendwere used to look for prevalence trends over several agegroups. In the different groups, geometric mean was cal-culated by the nth root of the product of the data values,where n represents the number of cases. Statistical analysiswas performed using SPSS version 11 (SPSS Inc., Chicago, IL,USA).

3. Results

3.1. Sociodemographic characteristics of theMupfure women in the study

Of 722 women who registered for the study, 557 fulfilledthe inclusion criteria. The mean age was 33.2 years (range

Tbog

Table 1 Prevalence and intensity of urinary schistosomiasis mea

Whole group(n = 544)

Age group (years)

15—19(n = 30)

20—24(n = 95)

25(n

Schistosomahaematobium-positive (n)

216 18 46 40

Prevalence (%) 39.7 60.0 48.4 44Infection intensity

(eggs/10 ml urine)b5.3 18.1 6.4 4

a Trend.b Geometric mean.

Table 2 Prevalence of HIV infection in 544 urinary Schistosoma h

Age group (years) HIV prevalence

Total S. haematobium-positive

<35 93/277 (33.6) 39/128 (30.5)≥35 63/267 (23.6) 33/88 (37.5)15—19 6/30 (20.0) 3/18 (16.7)20—24 28/95 (29.5) 12/46 (26.1)25—29 40/90 (44.4) 18/40 (45.0)30—34 19/62 (30.6) 6/24 (25.0)35—39 30/102 (29.4) 18/39 (46.2)40—44 20/89 (22.5) 9/27 (33.3)45—49 13/76 (17.1) 6/22 (27.3)

Overall 156/544 (28.7) 72/216 (33.3)

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5—49 years) and most of the women were housewives76.2%). Of the 544 women whose infection status wasetermined, 156 (29%) had HIV infection and 216 (40%)xcreted S. haematobium eggs in the urine. The geomet-ic mean intensity of infection was 5.3 eggs/10 ml of urinerange 1—1008 eggs/10 ml urine). Stratified along tribalines, the Shona (Shona, Karanga, Manyika and Korekore,= 495) women infected with urinary schistosomiasis hadn HIV prevalence of 35%; those women who were notnfected with urinary schistosomiasis had an HIV preva-ence of 25%. The HIV prevalence ratio was 1.40 (P = 0.02).omen from the other tribes (n = 49) had stayed signif-

cantly less time in the area (P = 0.01), had an urbanhildhood (P < 0.001) and had grown up outside the Mup-ure area (P = 0.009). In this small group, the HIV preva-ence was lower in schistosomiasis-infected women (21%;/24) than in uninfected women (40%; 10/25) (prevalenceatio 0.53).

.2. Prevalence of urinary schistosomiasis and HIVn Mupfure women of different age groups

he prevalence and intensity of S. haematobium infectiony age group are given in Table 1. As shown, the prevalencef S. haematobium infection was highest in the youngest ageroup (60%) and declined to less than one-half of this value

sured by urine egg counts in different age groups

P-valuea

—29= 90)

30—34(n = 62)

35—39(n = 102)

40—44(n = 89)

45—49(n = 76)

24 39 27 22 <0.001

.4 38.7 38.2 30.3 28.9

.7 6.9 3.1 4.6 2.4 0.001

aematobium-infected and uninfected women, by age group

Prevalence ratio P-value

S. haematobium-negative

54/149 (36.2) 0.84 0.3130/179 (16.8) 2.23 <0.0013/12 (25.0) 0.67 0.5816/49 (32.7) 0.80 0.4822/50 (44.0) 1.02 0.9213/38 (34.2) 0.73 0.4512/63 (19.0) 2.43 0.00411/62 (17.7) 1.88 0.117/54 (13.0) 2.10 0.14

84/328 (25.6) 1.30 0.053

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n the oldest age group (29%; test for trends, P < 0.001).imilarly, the intensity of urinary S. haematobium infectionas highest in women less than 20 years old and lowest

n those who were older than 45 years (P = 0.001). Thereas no association between intensity of infection and HIV

erostatus, overall or in the subgroups. As shown in Table 2,he overall prevalence of HIV infection differed among thege groups surveyed. The prevalence was 20% among thoseelow 20 years of age, peaked at 44.4% in the 25—29 yearsge group and then declined to 17.1% in women above5 years of age (P = 0.003). The prevalence of HIV amongomen infected with urinary schistosomiasis was insignifi-antly higher than in women who were not infected (33.3%s. 25.6%; prevalence ratio 1.30; P = 0.053). When testedn multivariate analysis controlling for age, there was only

tendency towards a significant association in the overallopulation between urinary schistosomiasis and HIV (oddsatio 1.4, 95% CI 0.93—2.0; P = 0.11). However, women over5 years of age infected with urinary schistosomiasis had aignificantly higher HIV prevalence than those without uri-ary schistosomiasis (37.5% vs. 16.8%; prevalence ratio 2.23;< 0.001). Among women below 35 years, the HIV preva-

ence ratio was 0.84.

. Discussion

omen over 35 years of age with urinary schistosomia-is were more than twice as likely to be HIV-positive thanhose who were schistosome egg-negative in this rural Zim-abwean population. Approximately three-quarters of theomen were housewives, most had lived in rural areas all

heir lives and those infected with schistosomiasis probablyrst became infected in childhood and maintained it throughontact with infective water during their normal day-to-dayomestic activities (Kjetland et al., 2005; Ndhlovu et al.,992).

As has been reported previously from this area, thereas a significant association between urinary schistosomia-

is in all age groups and S. haematobium ova in the genitals,s well as a significant association between genital schisto-omiasis and HIV (Kjetland et al., 2005, 2006). It has beenuggested that schistosome ova lodged in the genital mucosaay offer an ideal environment for the transmission of HIV

Feldmeier et al., 1995a; Kjetland et al., 2006; Poggenseet al., 1998). Cells expressing the specific receptors for HIVinding, i.e. CD4 cells, macrophages and Langerhans cells,ound in the egg granulomas and in adjacent tissues mayavour the propagation of HIV in the female genitals (Helling-iese et al., 1996; Poggensee et al., 1999).

The prevalences of both diseases were high. Thus, theopulation was appropriate for studying the interactionetween the two diseases. The highest HIV prevalence ratesre found in urban and semi-urban areas (UNAIDS/WHO,004). Schistosoma haematobium is transmitted in fresh-ater bodies and is thus usually a rural phenomenon. The

wo diseases meet in migrating populations, newcomers to

ities, the poorest city populations, travellers, commut-ng spouses and roadside villages (Ndamba et al., 1994;erwadda et al., 1992). To our knowledge, no-one has stud-ed the childhood or adult water-body contact in urbanomen with HIV. Moreover, there are reports of rural HIV

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P.D. Ndhlovu et al.

pidemics in Africa (Gregson et al., 2001; Grosskurth et al.,995; UNAIDS/WHO, 2004). The age patterns of HIV preva-ence in this study were typical of rural sub-Saharan AfricaUNAIDS/WHO, 2004). The higher prevalence and inten-ity of infection of urinary schistosomiasis in women below0 years of age compared with older women is also typi-al of schistosomiasis infection patterns in endemic areas.he phenomenon has been ascribed to age-acquired immu-ity (Chandiwana et al., 1988; Clarke, 1966; Fisher, 1934;dhlovu et al., 1996). The intensity of infection, as deter-ined by urinary ova excretion, is usually low in adults,

lthough lesions may still be severe (Smith and Christie,986). The prevalence and severity of genital schistosomia-is have been found to be fairly constant in adult age groupss well as in this population (Kjetland et al., 2005; Leutschert al., 1997; Poggensee et al., 2000).

Karanja et al. (2002) found that HIV-positive men withow CD4+ counts in Kenya were at a higher risk of re-infectionith schistosomiasis than adults with healthy immune sys-

ems. Thus, depletion of CD4 cells may decrease resistanceo schistosomiasis (Levy, 1993). As an intact immune sys-em is necessary for schistosome eggs to be shed in uriner faeces, immunocompromised people infected with HIVay fail to shed schistosome eggs (Doenhoff et al., 1986;osseinipour et al., 2004; Kallestrup et al., 2005; Karanjat al., 1997; Lambertucci et al., 1998; Mwanakasale et al.,003). It may be argued that the lack of association betweenIV and schistosomiasis in the younger age groups may beue to immunosuppression in these age groups. Women inhe 25—29 years age group had a significantly higher HIVrevalence in our study, and most deaths in Zimbabwe occurn this age group (Ministry of Health and Child Welfare,002). This may suggest the immune system in the 25—29ears age group may be particularly impaired. However, weid not have CD4 cell count data and we did not know theime of seroconversion, so it is not possible to make assump-ions about decreased S. haematobium egg excretion in theounger groups.

We hypothesise that HIV incidence in these young peopleay be under the particular influence of other important

actors such as partner change, commuting partners, hus-and age and/or sexually transmitted diseases (Grosskurtht al., 2000; Kjetland et al., 2006).

Investigation for genital schistosomiasis is dependent onspeculum examination with a good light source and mag-

ification, which are often not available in highly-endemicreas (Kjetland et al., 2005). Further studies must be donen order to confirm whether testing older women for the twoiseases by urinary and blood specimens only may be a wayo determine whether schistosomiasis is a co-factor for HIVransmission in a particular area.

From these results, we cautiously suggest that womeniving in S. haematobium-endemic areas were infected withchistosomiasis while their immune system was intact, andhat treatment and control of schistosomiasis may be anmportant complementary method to control the HIV pan-

onflicts of interest statementhe authors have no conflicts of interest concerning the workeported in this paper.

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Urinary schistosomiasis and HIV in females in Zimbabwe

Acknowledgements

We are grateful to Blair Research Institute personnel forlogistical and technical assistance. We thank the women,village health workers and health technicians of Mupfurefor participating in the study. The Medical Research Councilin Zimbabwe and the WHO/TDR is appreciated for permis-sion to conduct the study and to publish the results. Finan-cial support was received from the WHO/TDR, NorwegianResearch Council, Danish Bilharziasis Laboratory and Ulle-vaal University Hospital. The authors are indebted to staff atMupfure Secondary School, village health workers and envi-ronmental health technicians.

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