An estimated 90% of all HIV infections occur in low-income settings where heterosexual intercourse is the predominant mode of transmission. Prevention is still the main tool for controlling HIV epidemics. Programmes aiming to change sexual behaviours have formed the backbone of prevention efforts and have been heavily utilized since the start of the HIV epidemic. In general, these encourage abstinence, fidelity, limited numbers of sexual partners and condom use, and they mainly address transmission outside marriage. Interventions are often evaluated through surveys of knowledge, attitudes and practice; however, there are serious concerns about how well changes in knowledge and attitudes correspond to the adoption of new behaviour and about the validity and accuracy of self-reported sexual behaviour in such surveys [1,2].
Ideally, evaluation of behaviour-change interventions directed at HIV transmission would be based on HIV incidence . However, its use may be problematic because of ethical considerations surrounding testing and the large sample sizes that are needed. The problem of large samples is particularly acute where HIV incidence is still relatively low but where there is also the greatest potential to prevent large-scale epidemics. An alternative outcome for evaluation is the incidence of other sexually transmitted infections, which, sharing a common mode of transmission with HIV, may provide an indication of patterns of HIV risk behaviour . The need for appropriate biological markers to capture HIV risk based on incidence of other sexually transmitted infections has been highlighted [4,5]. In studies in both developed and developing countries, biological markers have been used to triangulate with other indicators, such as those that might be collected in surveys of knowledge, attitudes and practice, to allow an improved evaluation of HIV risk [5–7]. The usefulness of any such biological markers depends on the availability of accurate diagnostic tests, the incidence and prevalence of infection, and the pattern of sexual networking in the target population.
Herpes simplex virus 2 (HSV2) has been suggested as a suitable biological marker to capture patterns of HIV risk behaviour [6,8–13]. HSV2 infection is responsible for considerable morbidity in populations of reproductive age and shares a common route of transmission with HIV [8,14]. In several sub-Saharan populations, HSV2 infection has been linked to specific behaviours targeted in behaviour-change programmes [6,7]. There is convincing evidence that HSV2 and HIV form mutually enhancing epidemics [3,7,8,15,16]. HSV2 has been shown to be associated with both increased HIV infectiousness and increased susceptibility to HIV infection [17,18]. Even in the absence of genital ulcers, HSV2 shedding has been found to be more common in women co-infected with HIV-1 .
Much of the work on the association between HSV2 epidemiology and sexual behaviour has been done in predominantly monogamous settings [9,10]. The dynamics of HSV2 transmission in polygynous settings deserve particular attention. Polygyny is based on concurrent multiple partners, a man and his wives. Compared with monogamous marriages, each polygynous marriage set includes more people who might introduce HSV2 and, once introduced, more people who are exposed. The institution of polygyny supports high rates of previous multiple partners because polygynous societies tend to have high rates of marital disruption, through death or divorce . The dynamics of polygyny in many sub-Saharan populations is characterized by large age differences between partners and later age at first marriage for men to overcome nearly equal sex ratios at the population level. Simulation models suggest that patterns of sexual mixing that involve concurrent partners and large age differences between partners may lead to an accelerated rate of HIV spread relative to settings where the same number of partners are involved through serial relationships and where smaller age differences exist between partners [21,22].
This study examines risk factors for the prevalence of HSV2 seropositivity among women in a polygynous setting in rural Gambia. Associations between women's HSV2 status and the specific marriage experiences of these women and their husbands are considered to identify if marriage patterns confer risk. Implications for behaviour-change programmes aiming to reduce HIV risk in polygynous settings are considered with respect to the usefulness of HSV2 as an evaluation marker. Patterns of HSV2 risk are considered for their implication for the spread of HIV in polygynous West Africa.
The UK Medical Research Council operates a demographic surveillance system in 40 villages between 32 km east and 22 km west of Farafenni town in The Gambia. There are three main ethnic groups in the area; in 1999, the population included 43% Mandinka, 36% Wollof and 21% Fula and was almost entirely Muslim. Most people live by subsistence farming. Male circumcision is universally practiced, whereas female genital cutting varies between ethnic groups . In 1998, 40% of the married men and 54% of the married women were in polygynous unions, and married men had an average of 1.5 wives . Islamic polygyny allows men to marry up to four wives at any one time. The potential for polygyny is present in any marriage.
The data used here came from two studies. In the first half of 1999, the Reproductive Morbidity Survey (RMS) measured reproductive health and fertility outcomes for all consenting women between the ages of 15 and 54 years in 20 villages randomly selected from the population . Of 1871 eligible women, 1348 (72%) were interviewed and 1157 had a gynaecological examination. HSV2 serology was assessed using a peptide-55 enzyme-linked immunosorbent assay (ELISA), as described by Marsden et al. . Serological reactivity with peptide-55 corresponds to an immunodominant epitope spanning residues 561–578 of glycoprotein G of HSV2 (gG2). Positive and negative African sera controls were used. Samples were considered positive if the absorbance reading was greater than the mean plus 5SD of three negative controls. Samples were recorded as positive or negative only. The Male Fertility Survey (MFS) interviewed adult men (18 years and over) and women (15–54 years) in 21 of the surveillance villages during the period February to June 1998 : 1315 men (79% of those eligible) and 1621 women (87% of those eligible) were interviewed about their detailed marriage and fertility histories. Men were also asked about their interests in future marriages and fertility and about fertility events outside of marriage. All marriages were Islamic and marriage dates were taken as the day of the tying ceremony at the mosque. Fourteen villages participated in both surveys.
Two datasets were created for this analysis. The first dataset included all women who had never married (never-married women) taken from the RMS dataset (150). Eighty-four of these women had consented to a vulval examination by the gynaecologist. This dataset was used to look at risk factors for HSV2 infection among this group. Potential risk factors included sociodemographic variables and reported sexual activity.
The second dataset included 525 women who had been or were married (ever-married women), who participated in both the RMS and MFS and whose current or most recent husbands had participated in the MFS. Women's sociodemographic, marriage and reproductive/sexual health data, from the RMS and MFS, were matched to their interviewed husband's sociodemographic, marriage and fertility data, from the MFS. Data on husbands were matched to each of their interviewed wives; 404 husbands were included in the dataset with an average of 1.3 wives. This dataset was used to look at associations between the women's HSV2 status and their own and their husbands’ sociodemographic and marriage history characteristics.
This second dataset was also collapsed to look at patterns of HSV2 infection between co-wives in a marriage set. Many of the 404 marriage sets did not include all co-wives because the surveys were not able to include every woman in the study area and wives may have been resident outside the area. Of the marriage sets, 225 were monogamous and 72 were polygynous with data for only one wife available. A subset of 107 marriage sets in which information on more than one wife was available was used in the analysis of patterns of HSV2 concordance between co-wives.
All data analysis was conducted in Stata 6.0 . For ever-married women, each potential risk factor was evaluated for associations with HSV2 status in logistic regression models with age, using Huber/White standard errors and allowing for clustering by husbands. Multivariate models were built using variables that were significant in the age-adjusted models at the 0.05 level. As variables were introduced in the model hierarchy, each was assessed for significance and for colinearity with other variables. Variables that did not contribute significantly to the multivariate model were subsequently excluded to achieve a parsimonious model of independent risk factors. A kappa statistic was calculated to estimate the concordance of HSV2 serostatus among co-wives for all marriage sets, with between two and four co-wives, despite the fact that a test of significance is not available for concordance among sets of varying numbers of wives . The kappa statistic was also calculated for the set of marriages that includes only two wives and where both of those wives were interviewed.
Specificity of the peptide-55 serology for herpes simplex virus 2
The HSV2 test used here, assessing serological reactivity with peptide-55, has been found to have a higher specificity than other gG2-based tests and does not cross-react with HSV1; it is, therefore, considered to have favourable properties for type-specific serodiagnosis [26,29]. Using samples from elsewhere in The Gambia , the peptide-55 test was compared with the UK Central Public Health Laboratory monoclonal antibody-blocking ELISA (CPHL) HSV1- and HSV2-specific tests . The CPHL test has been reported to have a specificity of 91% and a sensitivity of 93–96% compared with Western blot in African sera . Anti-HSV1 reactivity was 100% in a sample of 100 15–17-year-old Gambian rural adolescents; reactivity to HSV2 was 2% using the peptide-55 ELISA and 5% using the CPHL test (R. Gopal, personal communication). For a similar sample of 98 30–35 year olds, HSV2 reactivity was 31% by the peptide-55 ELISA and 44% by the CPHL test. Therefore, the peptide-55 ELISA test can be expected to generate lower prevalence rates relative to the CPHL test but cross-reactivity with HSV1 does not seem to be a problem in this setting.
The mean age of the never-married women at interview was 17 years (range 15–32) and 93% of these women reported no sexual activity ever. Overall, HSV2 prevalence for the never-married women was 16% (compared with the 32% prevalence shown amongst all women who participated in the full RMS). HSV2 seropositivity was higher among the sexually active women (36%) compared with those who reported never having had sex (15%). Of 84 women who consented to a vulval examination, 73 were considered to have an intact hymen and among these women, 16% were HSV2 seropositive. There were no women with an intact hymen who reported to be sexually active. Genital cutting was very common among the HSV2- positive women with intact hymens; 10 out of 12 were cut.
Women who matched to husbands were 33 years of age on average (Table 1). Slightly less than half of the women had experienced genital cutting. Cutting was significantly associated with ethnic group: 98% of Mandinka, 33% of Fula and 4% of Wollof women were cut. Women married for the first time at an average age of 17 years; 57% of the women surveyed were currently in polygynous unions and 19% had experienced a terminated marriage (44 had divorced and 46 had been widowed). Around 20% of the women reported not having had sex in the last 3 months. Slightly more than half of the women were their husband's first wife and approximately a third were their husband's only wife ever. First wives were less likely than higher order wives to have been married before, controlling for age [odds ratio (OR) 0.16, 95% confidence interval (CI) 0.10–0.26)]. First wives were also closer in age to their husbands, on average (9.1 years younger), compared with wives of higher marriage order (19.2 years younger). Marriage patterns were associated with ethnicity: Fula women were younger at first marriage, more likely to be in monogamous marriages and more likely to be related to their husband than women of the other two ethnic groups.
Husbands were, on average, 46 years old at interview, had married for the first time at age 24 and had been married 2.1 times (Table 1). Polygyny had been experienced in the marriage history by 53%, and 45% were polygynous at interview, with an average of 2.3 current wives. A terminated marriage was reported by 34% (94 had divorced and 60 had been widowed). Thirty-nine per cent of the husbands had only been married once in their lifetime. The average of these husbands at interview was 38 years and they tended to be younger than the husbands who had had other marriages. Thirty-eight per cent of the husbands said they were interested in marrying another wife in the coming year.
HSV2 prevalence in ever-married women was 36%. The prevalence increased with age, with the sharpest increase in the age groups 15–19 (10%) and 24–29 (34%) years. In a multivariate logistic regression model, women's age, ethnicity and genital cutting status were significantly associated with HSV2 prevalence (Table 2). Uncut Fula (OR 0.27, 95% CI 0.14–0.52) and Wollof (OR 0.12, 95% CI 0.07–0.22) women were both at significantly lower risk compared with Mandinka women. Women whose husbands married for the first time after age 35 were nearly three times as likely to be HSV2 positive compared with women whose husbands married by age 24 (OR 2.72, 95% CI 1.20–6.10). Both women whose husbands were currently monogamous but had had other marriages (OR 2.76, 95% CI 1.30–5.88) and women who were in currently polygynous marriages (OR 2.88, 95% CI 1.66–5.01) were nearly three times as likely to be HSV2 positive as women who were their husband's only wife ever. Those women whose husband reported interest in a new marriage were nearly twice as likely to be HSV2 positive (OR 1.91, 95% CI 1.18–3.09).
Among 101 marriage sets where data were available for more than one wife, none of the recorded co-wives was HSV2 positive in 53 sets (52%) and all of the recorded co-wives were HSV2 positive in 27 sets (27%). Overall, there was 80% concordance of HSV2 serostatus among recorded co-wives (kappa coefficient of concordance was 0.57, categorized as ‘good’ agreement ). Restricting the analysis to marriage sets with two wives where both wives were included (n = 75) gave similar results [kappa coefficient of concordance 0.57 (P < 0.001) that the observed concordance would occur owing to chance, ‘good’ agreement].
The overall seroprevalence of HSV2 among women in this sample is consistent with the 28% HSV2 seroprevalence in women aged 15–34 years found elsewhere in The Gambia where the same test was used . Several serological tests for HSV2 are in use and there is at present no agreed gold standard, so caution is necessary when making comparisons between studies. The HSV2 test used here, assessing serological reactivity with peptide-55, has been found to have a higher specificity than other gG2-based tests and does not cross-react with HSV1; it is, therefore, considered to have favourable properties for type-specific serodiagnosis [26,29].
Although the use of different serological tests means that studies are not directly comparable, overall seroprevalence of HSV2 among women in this sample does not differ greatly from results for other West African populations. In Cotonou, Benin, an overall HSV prevalence of 30% was found among all women: rising from 9% in the 15–19 year age group to 56% among those aged 45–49 years . In that sample, HSV2 prevalence among women in monogamous marriages was 32% compared with 53% for women in polygynous marriages. Higher HSV2 prevalences have been reported for female populations in East, Central and Southern Africa [6,7,12,33].
The 16% prevalence of HSV2 seropositivity among never-married women is higher than that reported in other studies. Shaw et al.  reported a prevalence of 5.4% for never-married women in a different rural population in The Gambia, where the Jola ethnic group is dominant, Weiss et al.  reported 13% prevalence among urban, never-married women in Cotonou. Comparisons of never-married women across studies should be undertaken with caution: given that HSV2 and age are tightly linked, especially in the younger age groups, the age distribution of samples will affect prevalence. Additionally, several events mark West African marriages and so variations in the definitions of marriage may affect who is included in this category. In the present study, 8% of the never-married women reported sexual intercourse and HSV2 prevalence was higher for these women. Twelve women who had an intact hymen on examination tested positive for HSV2, a finding that is difficult to explain except by some false-positive results or, as has been suggested elsewhere, that HSV2 transmission is associated with non-penetrative sexual activity  or other non-sexual routes of infection. Ten out of these twelve women with intact hymens had undergone genital cutting, and whether this facilitates transmission by non-penetrative sexual activity deserves further study.
Women's personal characteristics and husband's marriage history were both important determinants of risk for ever-married women matched to their husbands. HSV2 prevalence increased with woman's age, which is most likely to be a proxy for exposure time. Differences were found in HSV2 prevalence between ethnic groups and genital cutting status. Ethnicity was closely associated with genital cutting and, therefore, it is difficult to separate out the independent effects of the two factors. Genital cutting was identified as a risk factor for HSV2 from the full RMS, controlling for fewer confounders . Ethnic variation in HSV2 risk is likely a result of biological and/or social differences, including patterns of sexual behaviour. Husband's age at first marriage affected HSV2 risk for their wives. HSV2 risk was highest for women whose husbands had married after age 35, 10 years later than the average age at first marriage for men in this population . Men who postpone marriage may have engaged in higher levels of premarital sexual activity, but this could not be considered with the data available here. Women whose husbands had expressed interest in a new marriage in the coming year were at higher risk for HSV2. Such an interest may correspond to a general interest in other relationships that these husbands had acted on in the past.
Current marital status alone was not significantly associated with HSV2 risk in multivariate models. The variable that was included in the model encompassed both current marital status and the husband's marriage history. Women in polygynous marriages and women in monogamous marriages where the man had been married before had a similar risk of HSV2; the protective effect for women came from being the only wife ever for a husband. Ideally, the epidemiology of sexually transmitted infections should be based on numbers of sexual partners and sexual behaviours specifically. In many settings, this is not possible and marriage information is more suitable. Contrary to other studies , this analysis indicates that classifying individuals according to current marriage status is not enough to capture exposure risk in polygynous populations, and some information from marriage histories may be needed.
Interestingly, after controlling for other factors in the multivariate models, increased risk for HSV2 was not associated with a women's past marriages, with her age at first marriage or with her age difference from her spouse. Clearly, a woman's own experiences will be associated with risk; the 16% HSV2 prevalence among never-married women provides evidence for this risk outside of marriage. In the model of HSV2 risk in ever-married women however, exposure was accounted for by variables that came from the husband's marriage history rather than the woman's marriage history. Some of the men's marriage history variables that are included in the model, age at first marriage and interest in a new marriage, do not describe his experience with marriage per se but rather the amount of time spent as a young unmarried man and possibly his experience with other women outside of marriage. This indicates that a large proportion of exposure for ever-married women is likely to come within marriage through their husband's cumulative experience. The high degree of concordancy in HSV2 serostatus among recorded co-wives supports this.
Transmission within marriage deserves particular attention for further research because of its implications for patterns of spread of sexually transmitted infections and for the design and evaluation of behaviour-change programmes. The relative importance of transmission within marriage, as opposed to outside marriage, will depend on patterns of marriage and sexual behaviour in each setting. A study designed to look at marital transmission in this polygynous setting might include husbands and all co-wives to look at risk factors of HSV2 within and between partner sets.
The common transmission route with HIV means that, regardless of whether HSV2 is a good marker for specific behaviours, any individual infected with HSV2 has also been at increased risk of exposure to HIV. A high proportion of transmission occurring within marriage may compromise the usefulness of HSV2 as a marker to evaluate behaviour-change programmes targeting personal risk behaviours at the population level. Even if behaviour change programmes are successful in promoting abstinence, fidelity, limited numbers of sexual partners and condom use, people will still be exposed and expose others based on their behaviour within marriage. Promoting personal protection between partners within a marriage will be difficult in rural West African populations such as this one, given high fertility desires, limited communication between partners and greater sexual freedom for men [34–36]. Individual behaviour should still be targeted to prevent HSV2 and HIV from entering marriage sets, though it is necessary to recognize that marriage sets that are already infected with HSV2 will act as a reservoir of infection that spreads as partners take on new marriages. Transmission in marriage will sustain the epidemic and dilute the effect of behaviour change over time compared with other populations.
In conclusion, so far HSV2 and HIV-1 prevalence has been low in Islamic West Africa relative to other African regions. In this setting, our data suggest that much transmission of HSV2 occurs within marriage, where opportunity for personal protection is limited. Programmes that set out to curb transmission through sexual behaviour risk reduction are still of great importance; however, their impact on HSV2 and HIV incidence may be undermined by transmission within marriage.
We thank Hilton Whittle and Maarten Schim van der Loeff for their comments on a previous draft of the paper.
Sponsorship: The RMS was funded by the Medical Research Council (UK), while the MFS was jointly funded by the Rockefeller Foundation and the Medical Research Council.
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