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    Women in rural Zimbabwe treated at an early age had less genital mucosal contact bleeding upon gentle insertion of a speculum. *Significantly lower prevalence contact bleeding than women who were treated after the age of 20 years. **Significantly less childhood waterbody contact and more urban childhoods, but current waterbody contact was the same as that of the treated population.

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    Year and age at prior treatment for schistosomiasis, as recalled by women in a rural Zimbabwean area. The type of treatment was according to official Zimbabwean/Rhodesian records.1824

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Prevention of Gynecologic Contact Bleeding and Genital Sandy Patches by Childhood Anti-schistosomal Treatment

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  • 1 Centre for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, Oslo, Norway; University of Oslo, Oslo, Norway; College of Health Sciences, University of Zimbabwe; Blair Research Institute (now National Institute for Health Research), Harare, Zimbabwe; Department of International Nutrition and Health, University of Copenhagen, Copenhagen, Denmark; Research Unit, Sorlandet Hospital HF, Kristiansand, Norway; University of Agder, Kristiansand, Norway

Schistosoma haematobium infection may cause genital mucosal pathology in women with and without urinary schistosomiasis. This report seeks to explore the long-term effect of anti-schistosomal treatment on the clinical manifestations of S. haematobium infection in the lower genital tract. Prior treatment was reported by 248 (47%) of 527 women. Treatment received before the age of 20 years was significantly associated with the absence of sandy patches and contact bleeding, and this association was independent of current waterbody contact. Treatment in the past five years did not influence the prevalence of gynecologic schistosoma-induced lesions. The study indicates that early treatment may be more efficient for gynecologic morbidity control. Findings warrant an exploration into several chemotherapeutic agents administered at an early age, as well as in adults.

INTRODUCTION

Seven hundred million people are at risk of acquiring schistosomiasis and 85% are in Africa.1 Genital schistosomiasis may affect up to 50% of the women in areas endemic for Schistosoma haematobium.26 Even in the absence of urinary ova excretion, 23–41% of women have been found to have genital schistosomiasis.68 The disease is associated with considerable morbidity. Moreover, there is increasing evidence that female genital schistosomiasis makes women susceptible to the human immunodeficiency virus (HIV).4,5,9

Although mass chemotherapy with praziquantel for treatment of urinary schistosomiasis is feasible and has been adopted as a World Health Organization health policy for women and children, the effect of treatment on genital mucosal pathology has barely been explored.1,1012 Regular treatment may result in resolution of urinary tract pathology and reduction in morbidity.1316 This report presents data on the long-term effect of self-reported anti-schistosomal treatment on the clinical manifestations of S. haematobium infection in the lower genital tract in rural Zimbabwean women.

MATERIALS AND METHODS

A cross-sectional study was conducted in northern Zimbabwe in 1998. All women 20–49 years of age were invited to take part in the study. Virgins and pregnant, postmenopausal, or menstruating women were excluded. Inclusion in the study took place after individual informed oral consent was provided. Permission to conduct the study was granted by the Provincial and District Medical Directors, the village head-man, and at village meetings. Ethical approval was provided by the Medical Research Council of Zimbabwe and by the ethical committee of the Special Program for Research and Training in Tropical Diseases Research/World Bank/World Health Organization. Patients and partners were treated in accordance with the standard Zimbabwean syndromic approach and referred when necessary.17

Treatment history and clinical examination.

Individual treatment records were not available. In Zimbabwe, anti-schistosomal treatment before 1973 was lucanthonen hydrochloride, followed by metrifonate.1820 From 1981 through 1995, there was an overlapping period with praziquantel.2124 Since 1995, praziquantel has been used in nearly all cases.

A nurse who knew local events questioned the women in Shona (the local language) for waterbody contact and time of former treatment (year, season/month). Questions about timing were open-ended and allowed the necessary time to remember. Clinical investigations were conducted by one clinician (E.F.K) as described.6 At the time, the clinician did not know the HIV or S. haematobium test results. Genital surfaces were examined with a photocolposcope. Homogenous yellow sandy patches were sandy-looking areas with no distinct grains at 15× magnification.6,25 Grainy sandy patches comprised oblong (approximately 0.05 mm × 0.2 mm) grains situated in the mucosa. Neo-vascularization was defined as pathological convoluted (corkscrew), reticular, circular and/ or branched, uneven-caliber blood vessels visible (15× magnification) on the mucosal surface. Contact bleeding was defined as fresh blood originating from the mucosal surface. Women were tested for a median of seven (range = 1–8) sexually transmitted diseases in order to investigate for differential diagnosis.6

Parasitology.

Three consecutive mid-day urine samples were examined for S. haematobium ova.26 One terminal-spined ovum gave a positive diagnosis in Pap smears, wet mounts, or biopsies of genital tissue.27 Wet mounts were taken from consenting women who showed debris or friable, loose, and bleeding tissue. Biopsies were performed only in consenting women with suspected cancer. Stool was processed by the Kato-Katz technique.28

Statistical methods.

Chi-square test, Fisher’s exact test (for numbers < 5) and odds ratios (ORs) with 95% confidence intervals (95% CIs) were used when comparing prevalence in two groups of persons. 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 < 0.2 and if the Spearman rank correlation coefficient was < 0.7. Statistical analysis was conducted using SPSS version 14 (SPSS Inc., Chicago, IL).

RESULTS

Of the 527 included women 248 (47%) reported to have been treated for schistosomiasis before the study commenced. Patients could not remember the names of the drugs they had been given. Median age at reported treatment was 16 years (range = 3–46). Of those who had received treatment before the study, 79% had been treated before the age of 20 and 52% before the age of 13.

Morbidity and age at treatment.

Figure 1 shows that contact bleeding was found most often in women who had been treated after the age of 20 years. Table 1 shows in more detail the prevalence of the current clinical phenomena by age at reported first treatment. The lowest prevalence of sandy patches was found in the women who reported to have been treated before the age of 13. Grainy sandy patch prevalences were lower in women who had been treated up to the age of 20. Current waterbody contact did not influence the association between morbidity and the age at treatment. Because of the heterogeneity of the teenage years29 the age group 13–19 years was split into two and three subgroups for further analyses. The subgroups showed the same trends as the whole group. Furthermore, analyses were conducted for other lesions that have been hypothesized to be associated with genital S. haematobium infection (ulcers, leukoplakia, papillomatous tumors, and polyps). Timing of prior treatment did not influence any lesions other than those listed in Table 1. Further analyses were done for treatment received at 20–24 years of age and 25–29 years of age (using the older women as the indicator variable). Such late treatment did not influence the prevalence of lesions. The time interval between the treatment and investigation did not influence the associations. HIV seropositivity and S. mansoni in stool did not influence the findings.

Although genital schistosomiasis was the most important predictor for morbidity listed in Table 1, other reproductive tract diseases were also associated with some of the phenomena.6 Homogenous yellow sandy patches were associated with schistosomiasis and herpes simplex type 2 (HSV-2), neovascularization was associated with cervical intra-epithelial neo-plasia, pre-contact bleeding was associated with HSV-2, and contact bleeding was associated with high-risk human papillomavirus and HSV-2. The association between current morbidity (Table 1) and age at treatment was not influenced by the other current reproductive tract diseases.

Type of treatment and duration since treatment.

The mean ± SD age of those who had been treated was 34 ± 8.9 years, and they had been treated a mean ± SD of 18.6 ± 10.8 years ago. The length of time between observation and prior treatment was grouped into five-year intervals. Women who had been treated more than 20 years ago had significantly less sandy patches (Adjusted [for age and current waterbody contact] OR = 0.27, 95% CI = 0.1–0.8, P = 0.006). This finding coincides with the period of treatment with metrifonate and lucanthonen hydrochloride, before praziquantel became available (Figure 2). However, after controlling for the age at treatment, the type of treatment was not associated with the presence of lesions. Recent treatment one, two, three, four, and five years ago together or separately did not have any influence on any of the sandy patch types, contact bleeding, neovascularization. However, the latter subgroups were small (n = 4–35).

Untreated women.

Figure 1 shows the prevalence of contact bleeding in the different groups. Untreated women had lived more often in an urban area in childhood (P < 0.001). The mean ± SD age of untreated women was the same as that for treated women (34 ± 8.3 years). Untreated women had significantly less childhood waterbody contact (P = 0.001). Untreated women had insignificantly less grainy sandy patches than women who had been treated (adjusted for age, current and childhood waterbody contact, OR = 0.7 95% CI = 0.5–1.1, P = 0.166). The prevalence of current water-body contact was the same in the treated (88.7%) and untreated groups (87.3%; P = 0.7). There was no significant difference in urinary schistosomiasis prevalence between untreated and previously treated women (adjusted OR = 1.3, 95% CI = 0.86–1.8, P = 0.21; the unadjusted figures are identical. HIV seropositivity and S. mansoni in stool did not influence the findings.

DISCUSSION

In this S. haematobium-endemic area of rural Zimbabwe, mucosal sandy patches and contact bleeding in the genital tract were significantly lower in women who had received treatment before the age of 20 years. Having received treatment before the age of 13 years seemed to offer the best overall protection against S. haematobium-induced pathology in the genital tract. After adjusting for age, the different types of historic anti-schistosomal treatment seemed to have an equal effect on current findings. However, we cannot conclude that a one-time anti-schistosomal treatment will prevent all gynecologic morbidity, even if given at an early age.

Schistosomiasis transmission was ongoing in the study area, with a current school child prevalence of more than 85% (Mduluza T, unpublished data). The women had regular water contact and reinfection was highly probable. It is likely that women who had high-risk water contact in their youth would continue this contact later in life.30 However, in our population, the current waterbody contact was independent of former risk contact. Moreover, we have controlled for current exposure in our calculations and the age at treatment remained a predictor for the current lesion status.

The study is based on recall because women did not have written records of treatment. This poses some problems for the interpretation. First, the age at treatment cannot be verified. Women would reason with the interviewer to remember the year of treatment, e.g., “the year I stopped school,” “the year Mugabe became president,” “the year of the last drought”. It is possible that women who had genital morbidity may have believed that their treatment was a long time ago. However, symptoms of genital schistosomiasis were not known to these women and were likely not attributed to schistosomiasis (Kjetland EF and others, unpublished data). Second, we do not know which treatment women had received. Thus, we are not certain that the reported treatment was actually for schistosomiasis. However, schistosomiasis was the only disease for which mass treatment was given in those years, and the community was well informed about urinary symptoms and remembered side effects vividly (others’ or their own).31 Furthermore, many patients and their families had participated in water contact or prevalence studies. Several regimens were available in Zimbabwe in the transition phases and because we were not able to ascertain the type of treatment we have chosen not to perform extensive analyses of the assumptions. Furthermore, we did not record whether the women had received treatment as part of mass-treatment projects or as a consequence of approaching the health services with symptoms. The available treatment two decades prior to the study was not praziquantel. However, the possible advantageous effects of lucanthonen hydrochloride and metrifonate were no longer significant after we had corrected for age at treatment.20,24,32

Ova of S. haematobium may be deposited in genital tissue and cause inflammation, fibrous tissue, and calcification.3335 These areas (sandy patches) are granulomatous lesions that may occur both in the urinary bladder and the genital mucosa. Lesions in the urinary tract are usually assessed by ultrasonography, which is clinically relevant for diagnosing morbidity in the urinary tract. However, in the genital tract, morbidity such as spot bleeding or risk of contracting HIV may be related to destruction of thin layers of the epithelium.36 Such details cannot be detected by ultrasound and this level of detail has not been assessed in the urinary tract, possibly because repeated cystoscopies in large groups of asymptomatic patients may be considered ethically and clinically unfeasible.12,3740 The long-term course of genital sandy patches has not been explored and there is also sparse information of the course of sandy patches in the bladder.11,40 If the clinical phenomena were acute, one could speculate that there would be a better effect of recent treatment, whereas if the clinical phenomena were established a long time ago one would expect a better effect of treatment a long time ago. Although urinary excretion ceased after treatment with praziquantel in this population, there was no significant decrease in lower genital tract morbidity assessed at 3, 9, and 12 months.11 Although early treatment seemed to have a relative protective effect, there was still ample sandy patches even in these groups. Furthermore, genital lesions have also been found in exposed travelers from areas not endemic for schistosomiasis.4148 Thus, childhood contact is not necessary for the development of genital schistosomal morbidity. We hypothesize that genital grainy sandy patches are created as eggs become deposited in genital mucosa and that neovascularization and the ensuing mucosal bleeding are reactions to the intact or disintegrating egg.33,34,49 When many ova have disintegrated, we assume that homogenous yellow sandy patches without distinct grains may be seen. The long-term presence of ova and continuous disintegration of new ova may develop into a chronic reaction that may last for years or even for life. In some women, these areas probably transform into fibrous scar tissue as ova are no longer fed into the region.33

The evidence from this study in Zimbabwe may indicate that treatment before and during the teenage years may have some protective effect against genital schistosomal morbidity in adulthood. Further studies are needed to assess the impact of the different anti-schistosomal drugs on genital mucosa.20,40 The findings warrant an exploration into chemo-therapeutic agents given repeatedly at an early age. Furthermore, as a measure against the spread of HIV, other regimens should be explored for effect in women with lesions.

Table 1

Age at anti-schistosomal treatment as a predictor for current mucosal clinical findings and urinary schistosomiasis in 248 rural Zimbabwean women*

Age (years) at treatment as reported by rural women†
Characteristic≥ 20 ‡13–1912< 12Current age in years, mean (SD)§Current¶ waterbody contact N = 220/248
* Data were corrected for age and current waterbody contact in seven separate multivariate analyses. Anti-schistosomal treatment was self-reported. OR = odds ratio; CI = confidence interval; Adj. = adjusted.
† Some women may have been treated with metrifonate or lucanthone hydrochloride. In Zimbabwe, praziquantel has been recommended as a treatment for infection with Schistosoma haematobium since 1995; however, both metrifonate and praziquantel were used for several years (Figure 2).
‡ Indicator variable for other age groups.
§ For each type of morbidity.
¶ Currently exposed to schistosomiasis; 28 women were not in current contact with a waterbody and their results are not presented.
# Superficial or deep grains.
** Adjusted for age and current waterbody contact.
†† All P values are for the multivariate analysis.
‡‡ Sandy-looking areas with no distinct grains observed by 15× magnification.
§§ Convoluted (corkscrew), reticular, circular and/or branched, uneven-caliber blood vessels.
¶¶ Fresh red intravaginal blood originating from mucosal surface after careful insertion of speculum.
## Darkened intravaginal blood not caused by recent menstruation.
*** Urine results are missing for 15 people.
Current morbidity, no.52675970
Grainy sandy patches,# no. (%)27 (52)19 (28)19 (32)20 (29)34 (8.7)78/220 (36)
OR (95% CI)10.4 (0.2–0.8)0.4 (0.2–1.0)0.4 (0.2–0.8)1.0 (1.0–1.0)1.8 (0.9–3.4)
Adj. OR (95% CI)**10.3 (0.2–0.7)0.4 (0.2–0.9)0.3 (0.2–0.7)1.0 (0.9–1.0)1.7 (0.7–4.3)
P††0.0060.0300.0060.220.25
Homogenous yellow sandy patches,‡‡ no. (%)21 (40)23 (34)11 (19)15 (21)34 (9.5)61/220 (28)
OR (95% CI)10.8 (0.4–1.6)0.3 (0.1–0.8)0.4 (0.2–0.9)1.0 (1.0–1.0)1.5 (0.8–2.9)
Adj. OR (95% CI)10.8 (0.4–1.6)0.3 (0.1–0.8)0.4 (0.2–0.9)1.0 (1.0–1.0)0.8 (0.3–1.9)
P0.490.0140.0260.930.63
Both sandy patch types together, no. (%)35 (67)31 (46)24 (41)29 (41)34 (8.9)112/220 (60)
OR (95% CI)10.4 (0.2–0.9)0.3 (0.2–0.7)0.3 (0.2–0.7)1.0 (1.0–1.0)2.2 (1.2–3.9)
Adj. OR (95% CI)10.4 (0.2–0.9)0.3 (0.1–0.7)0.3 (0.2–0.7)1.0 (1.0–1.0)1.6 (0.7–3.6)
P0.0180.0050.0040.410.29
Neovascularization,§§ no. (%)31 (60)28 (42)28 (48)30 (43)35 (9.1)106/220 (48)
OR (95% CI)10.5 (0.2–1.0)0.6 (0.3–1.3)0.5 (0.2–1.1)1.0 (1.0–1.0)1.7 (1.0–2.9)
Adj. OR (95% CI)10.5 (0.2–1.0)0.6 (0.3–1.3)0.5 (0.3–1.1)1.0 (1.0–1.0)1.4 (0.6–3.2)
P0.0610.190.090.760.39
Contact bleeding,¶¶ no. (%)22 (42)13 (19)10 (17)15 (21)35 (8.9)54/220 (25)
OR (95% CI)10.3 (0.1–0.7)0.3 (0.1–0.7)0.4 (0.2–0.8)1.0 (1.0–1.0)1.5 (0.8–3.0)
Adj. OR (95% CI)10.3 (0.1–0.8)0.3 (0.1–0.7)0.4 (0.2–0.9)1.0 (1.0–1.0)1.2 (0.5–3.3)
P0.010.0040.0240.540.67
Pre-contact bleeding,## no. (%)10 (19)9 (13)4 (7)8 (11)37 (8.5)28/220 (13)
OR (95% CI)10.7 (0.2–1.7)0.3 (0.1–1.0)0.5 (0.2–1.5)1.0 (1.0–1.1)1.3 (0.6–3.0)
Adj. OR (95% CI)10.7 (0.3–2.0)0.3 (0.1–1.0)0.6 (0.2–1.8)1.0 (1.0–1.1)1.3 (0.3–4.6)
P0.530.0550.390.110.72
Urinary schistosomiasis,*** no. (%)26 (53)23 (37)22 (40)26 (39)33 (9.1)88/205 (43)
OR (95% CI)10.5 (0.2–1.1)0.6 (0.3–1.3)0.6 (0.3–1.2)1.0 (0.9–1.0)1.8 (1.0–3.3)
Adj. OR (95% CI)10.4 (0.2–1.0)0.6 (0.3–1.3)0.5 (0.2–1.0)1.0 (0.9–1.0)1.8 (0.7–4.2)
P0.0420.180.0650.0060.19
Figure 1.
Figure 1.

Women in rural Zimbabwe treated at an early age had less genital mucosal contact bleeding upon gentle insertion of a speculum. *Significantly lower prevalence contact bleeding than women who were treated after the age of 20 years. **Significantly less childhood waterbody contact and more urban childhoods, but current waterbody contact was the same as that of the treated population.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 79, 1; 10.4269/ajtmh.2008.79.79

Figure 2.
Figure 2.

Year and age at prior treatment for schistosomiasis, as recalled by women in a rural Zimbabwean area. The type of treatment was according to official Zimbabwean/Rhodesian records.1824

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 79, 1; 10.4269/ajtmh.2008.79.79

*

Address correspondence to Eyrun Floerecke Kjetland, Center for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, 0407 Oslo, Norway. E-mail: e.f.kjetland@medisin.uio.no

Authors’ addresses: Eyrun Floerecke Kjetland, Center for Imported and Tropical Diseases, Department of Infectious Diseases, Ullevaal University Hospital, 0407 Oslo, Norway, E-mail: e.f.kjetland@medisin.uio.no. Patricia Ndhlovu, Metabolic and Clinical Trials Unit, Camden Mews Day Hospital, 5 Camden Mews, London NW1 9DB, United Kingdom, E-mail: patricia.ndhlovu@candi.nhs.uk. Edith Nyaradzai Kurewa and Exnevia Gomo, College of Health Sciences, University of Zimbabwe, Avondale, Harare, Zimbabwe, E-mails: enkurewa@hotmail.com and egomo@rsc.medcol.mw. Nicholas Midzi, National Institute for Health Research (formerly Blair Research Institute), Harare, Zimbabwe, E-mail: nicholas.midzi@yahoo.com. Takafira Mduluza, Biochemistry Department, University of Zimbabwe, Mount Pleasant, Harare, Zimbabwe, E-mails: mduluza@medic.uz.ac.zw and tmduluza@yahoo.com. Henrik Friis, International Nutrition and Health Department, University of Copenhagen, Copenhagen, Denmark, E-mail: hfr@life.ku.dk. Svein Gunnar Gundersen, Research Unit, Sorlandet Hospital HF, Kristiansand, Norway and University of Agder, Kristiansand, Norway, E-mails: s.g.gundersen@sshf.no and s.g.g.gundersen@hia.no.

Acknowledgments: We thank Dr. S. Charimari (Provincial Medical Director and Supervisor); the Mupfure community, the staff at Madziwa, Harare Central, and Mount Darwin Hospitals; the personnel at Blair Research Laboratory; the library at the Ministry of Health; and Drs. T. Magwali, B. Mhlanga, and I. Lyngstad-Vik; and Professors F. Jerve, B. Myrvang and L. Sandvik for technical, medical, and cultural assistance. We also thank the Medical Research Council of Zimbabwe, the staff at Mupfure Secondary School, V. Mugabe (Headmistress), Sister J. Chikoore, the late Sister P. Dungare, C. Chadzimura (Councillor), the village health workers, environmental health technicians, N. Taremeredzwa, C. Mukahiwa, R. Manyaira, and T. Mushipe for prolonged hard work under very difficult circumstances.

Financial support: This study was supported by a director’s initiative grant from the United Nations Development Program/The World Bank/World Health Organization Special Program for Research and Training in Tropical Diseases, The Norwegian Research Council NO-RAD, the Department for Infectious Diseases, Centre for Imported and Tropical Diseases and Research Forum, Ullevaal University Hospital, Oslo, Norway, and the Danish Bilharziosis Laboratory.

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