IJE Advance Access originally published online on October 9, 2006
International Journal of Epidemiology 2006 35(6):1455-1460; doi:10.1093/ije/dyl217
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Article |
Factors associated with HIV sero-positivity in young, rural South African men
1 Gender & Health Research Unit, Medical Research Council, Private Bag X385, Pretoria 0001, South Africa.
2 Behavioral Sciences and Health Education, Emory University, Atlanta, GA, USA.
3 Department of Psychology, University of the Witwatersrand, PO Box 104, Wits 2050, South Africa.
4 Biostatistics Unit, Medical Research Council, Private Bag X385, Pretoria 0001, South Africa.
5 College of Public Health, University of Arizona, Tucson, Arizona, USA.
6 National Institute for Communicable Disease, Private Bag X4, Sandringham 2131 South Africa.
7 International Council for Research on Women, Washington DC, USA.
* Corresponding author. Gender & Health Research Unit, Medical Research Council, Private Bag X385, Pretoria 0001, South Africa. E-mail: rjewkes{at}mrc.ac.za.
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Abstract |
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Objective To describe factors associated with HIV infection in men aged 15–26 years.
Setting Rural Eastern Cape Province, South Africa.
Sample A total of 1277 sexually experienced Xhosa male volunteers from 70 villages participating in a cluster randomized controlled trial of an HIV behavioural intervention. Xhosas circumcise during manhood initiation rituals.
Design Cross-sectional, analysis of the study's baseline interviews.
Main measure HIV sero-status, sexual practices measured with an interviewer-administered questionnaire.
Results About 2% of the men were HIV positive. A logistic regression model showed HIV positivity to be associated with age (OR 1.55; 95%CI 1.22–1.95), having made a woman pregnant (OR 2.93; 95% CI 1.28–6.68), having been circumcised (OR 0.40; 95% CI 0.16–0.98), and having had sex with a man (OR 3.61; 95% CI 1.0–13.0).
Conclusions Our findings provide further evidence to suggest that circumcision is protective. There was much heterosexual risk taking among men but only pregnancy (with its association with sexual frequency) predicted HIV sero-positivity. Although relatively rare, same-sex sexual experiences were a risk factor. Male–male sexual contact is rarely assessed in HIV research in Africa and almost never addressed in general HIV prevention programming. Our findings suggest that it should be given more attention.
Keywords HIV, MSM, circumcision, heterosexual men, South Africa, rural
Accepted 31 August 2006
Young people in Sub-Saharan Africa are a particularly important HIV risk group. In South Africa, the age-specific prevalence amongst men in their teens and early 20s (4.8%) is substantially lower than that for women (15.5%)1 but still much higher than the prevalence of HIV in all age groups in many countries.2 Understanding the factors driving the epidemic in this young age group and developing appropriately targeted interventions are of great importance in overall efforts to combat HIV and improve adolescent sexual health.
The Stepping Stones Study offers a unique opportunity to examine risk factors for HIV positivity in a large group of young men from rural South Africa. The men were volunteers participating in an HIV behavioural prevention trial that collected detailed information on their sexual practices and HIV sero-status at baseline. Behavioural information included culturally appropriate assessments of all standard risk behaviours as well as male–male sexual contact. Male–male intercourse is a well-established risk factor for HIV transmission in the developed world, but rarely examined in developing countries,3 and often considered a taboo topic in research in Africa.4,5 Beginning to address this issue may break an important silence about transmission risk in sub-Saharan Africa.
The study participants came from an infrequently researched part of South Africa and one that is ethnically homogeneous. Compared with the country as a whole, participants were also socially homogeneous; they were mostly in school (although not necessarily in the age-appropriate year) and came from homes that ranged between poor and very poor (Table 1). All men in the study belonged to the Xhosa ethnic group, which has the cultural practice of circumcising all boys in the course of initiation into manhood. They, therefore, provide an interesting group in which to examine the association between circumcision and HIV prevalence.
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The analysis presented here describes a comprehensive examination of potential risk factors associated with HIV infection in rural South Africa men aged 15–26 years participating in the Stepping Stones evaluation.
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Methods |
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Between 2002 and 2003, we recruited 1396 men into a randomized controlled trial undertaken to evaluate the HIV prevention behavioural intervention Stepping Stones.6 A detailed description of the trial methods is presented elsewhere.7 The participants were volunteers from 70 study villages in the rural Eastern Cape province of South Africa near the town of Mthatha. Most were recruited from schools after a meeting at which the study was explained. They were told they would be asked to complete questionnaires in face-to-face interviews and give blood for HIV testing at intervals over 2 years, and to attend the HIV prevention intervention. They were also told they would receive R20 (
£1.50) after each round of data collection. Between 15 and 25 men per village completed the baseline questionnaire and gave blood for HIV testing.
Data collection
Interviews were undertaken using a structured questionnaire, administered in Xhosa by young male interviewers. Following the World Health Organization's rapid testing protocol,8 a venous blood was tested for HIV using two rapid tests. Determine (Abbott Diagnostics, Johannesburg) was used as a screening test, with confirmation of positive samples using Uni-goldTM (Trinity Biotech, Dublin, Ireland). An ELISA was performed to clarify any indeterminate results and taken as the definitive result. Participants in the study were offered their HIV results by the study nurses who made return visits to the schools. A total of 60 men (4.4%) had been tested for HIV before the study and 40 had taken their results. Of the latter, one had tested HIV positive.
The questionnaire asked about social and demographic factors (age, education, current schooling, earnings in last year or ever, and socioeconomic status), and perceptions of the community. Socioeconomic status was measured on a scale that captured household goods ownership (TV, radio, and car), frequency of hunger, frequency of having meat, and perceived difficulty accessing a modest sum for a medical emergency (R100 or £9) (Cronbach's alpha 0.60). Adverse childhood experiences were measured on a modified version of the short form of the Childhood Trauma Questionnaire.9 It covered emotional neglect, emotional abuse, physical neglect/hardship, physical abuse, and sexual abuse (Cronbach's alpha 0.72). We used scales to measure knowledge of sexual and reproductive health, and HIV. We measured perceived susceptibility to peer pressure to have sex on a 3-item scale (Cronbach's alpha 0.72).
It asked about men's health including whether they had ever been told by a woman that they had made her pregnant (and whether they agreed), circumcision (when it occurred, the method, and complications), and sexual experiences including first sex and sex with men and women. Men were asked about sex with men in two parts of the questionnaire. One question asked ‘Have you ever had sex with another man?’. The other question asked the respondent whether a man had ever ‘forced or persuaded you to have sex against your will’.
We measured attitudes to gender relations and controlling practices directed at the current or most recent main girlfriend using a set of questions that included a modified (13-item) form of the Sexual Relationship Power Scale10 and items on attitudes towards gender relations in women (Cronbach's alpha 0.69). We collected detailed information on the current or most recent main girlfriend. This included when the relationship started (or ended), and social and demographic characteristics of the partner (age, education, schooling, employment, earnings). We asked when last sex had been and whether condoms had been used. We assessed consistency of condom use in the past year for main partners and casual partners separately. We asked about numbers of main and casual female partners and history of transactional sex with women, which was defined as sex primarily motivated by material gain (for either the man or woman), where material gain was defined as provision of food, cosmetics, clothes, transportation, items for children or family, school fees, somewhere to sleep, or cash.11 We measured alcohol use using the AUDIT scale,12 which has been extensively validated in developing countries. It has 12 items and asks about the frequency, quantity, and consequences of drinking. We used a cut-point of 8 for ‘problem drinking’. Rape of non-intimate partners was assessed by four questions asking about making women have sex when they did not want to, were too drunk to consent, and participation in gang rape.13 We also measured physical and sexual (female) intimate partner violence (IPV) using questions from the World Health Organization's instrument.14 IPV questions contained specific, objective descriptions of men's behaviour and asked about frequency. Six items covered physical violence: pushed, shoved, slapped, hit with fist, kicked, beaten up, strangled, burnt, hurt/threatened with a weapon, threw something that could hurt her. Four items asked about being physically forced to have sex, having sex when frightened of the consequences, being forced to do oral or anal sex. Further information on the questionnaire is presented in Jewkes et al.7 Written informed consent was given. Ethical approval for the study was given by the University of Pretoria.
Statistical analysis
All data analyses used procedures that took into account the study design, i.e. the fact that participants were clustered within villages. First a descriptive analysis was carried out, with means of continuous variables and percentages for binary variables, given by HIV status, together with 95% confidence intervals. These were calculated using standard methods for the analysis of data from multistage surveys.15
In order to find risk factors associated with being HIV positive at baseline, the following procedure was followed: first stepwise logistic regression models were fitted using both forward selection and backward elimination, ignoring the clustering of subjects in the study design and using a liberal P-value of 0.15 for inclusion/exclusion, in order to identify a maximal set of potential explanatory variables. Generalized linear mixed models were then fitted using the identified maximal set of explanatory factors, with the cluster as a random effect, adjusted for using numerical quadrature. Any factors found to be no longer significant at the 10% level after adjusting for the effect of cluster were removed from the model. The models were confirmed by fitting ‘survey’ logistic regression models (in which the parameter estimates are unchanged from ordinary logistic regression, but the standard errors are inflated to allow for clustering). All analyses were carried out using Stata release 8.0.16
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Results |
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A total of 1396 men were enrolled in the study. At the time of enrolment, 1277 men completed interviews and had ever had sex (94.0% of those with sexual history available), and were included in this analysis. The paper presents all results only for these men. The men ranged in age from 15 to 26 years [mean 19.2 years, 95% CI (19.0–19.4); median age 19 years; IQR 17–20 years). Around 2.04% (26) of men were HIV positive at the time of interview. Table 1 shows selected background characteristics of the study subjects broken down by HIV status.
The median age of first sex was 14.7 (IQR 12.9–16.2). The men were all unmarried and the majority (88.8%) currently had a sexual partner. Only one man said he had never had a girlfriend (but had had sex). The mean number of lifetime partners was 6.9. Around 80.4% reported having a current main girlfriend who was younger than them; 13.5% had a main girlfriend of the same age; and 6.1% had an older main girlfriend. Around 59.3% reported a casual female partner during the past 12 months, with 23.2% reporting a one-night stand, and 55.2% reported having one or more khwapheni. The latter are concurrent partners who are kept secret from a main partner and usually they are women who themselves have another main partner. Around 17.8% reported having ever had transactional sex with a casual partner (where men gave something in return for sex). Around 65.1% had ever used condoms and 26.1% reported consistent use with a main girlfriend. In the past year 40.0% of those with casual partners reported consistent use in those relationships. The mean duration of the current main relationship for men was 2.1 years (95% CI 2.0–2.2) and median 1.5 years (IQR 0.7–3.2 years). The median number of days since last intercourse was 21 (IQR 5–60).
Around 46 (3.6%) of the men reported sexual contact with a man. The vast majority (42) said they had been ‘persuaded or forced to when they did not want to’. Four men reported consensual male–male sex, but three of these also reported an experience of being forced. Most of the group reporting coerced sex said there was one event (34 or 75.6%). Men were asked what their relationship was to the other man, the most common was a man from the neighbourhood (22 or 48.9%), a stranger or unknown person (13 or 28.9%), a boy from the neighbourhood (5 or 11.1%), and a teacher (2 or 4.4%). The median age of first coerced sex with a man was 16.9 years (IQR 14.9–18.5 years; range 5.2–21.8).
Around 54.1% of men had been circumcised. The mean age of circumcision was 16.9 years (95%CI 16.7–17.2) range 10.6–22.9 years. The proportion circumcised increased consistently across the age range of the sample (Table 2). Around 0.72% (1) of men circumcised before first sex had HIV, compared with 2.2% (25) of men circumcised afterwards (P = 0.249).
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Around 16.3% of men had made a woman pregnant. The mean number of women impregnated by these men was 1.12 and range 1–4. Men who had made a girlfriend pregnant had more frequent sex (data not shown).
Table 3 shows the results of the logistic regression analysis of factors associated with prevalent HIV infections. After adjusting for age, increased risk of HIV was associated with having ever had sex with a man and having impregnated a woman; risk was reduced for men who had been circumcised. The Population Attributable Fraction for non-circumcision was 27.6% and for having sex with a man it was 2.6%.
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Discussion |
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The HIV prevalence in these men was lower than that found in women in the same study (12.4%)17 but comparable with that of the country as a whole (4.8%).1 There have been many studies on factors associated with HIV sero-positivity in Africa, with notable exceptions,1 these have usually been conducted in samples of men from the general population rather than focused on youth, and the key risk factors described have been sexual behaviour, male non-circumcision, and sexually transmitted infections.1,18–21 Our findings add to the discussion in several ways. First we found that although our young men reported a great deal of risky heterosexual behaviour, for the most part it did not predict HIV infection. The only marker of heterosexual behaviour that was associated with HIV positivity was having impregnated a woman, which was in turn associated with more frequent intercourse.
Circumcision is increasingly often found associated with a lower likelihood of having HIV,1,22–24 and, recently, this has been demonstrated in a randomized controlled trial of circumcision in South Africa.25 The relatively large PAF for circumcision suggests that it is a particularly important protective factor in this age group. Our population was of interest because all men in the study would be expected to eventually circumcise, the fact that they had not all already done so reflected their age. Therefore, we would not expect the relationship between circumcision and HIV positivity to be confounded by unmeasured cultural differences between circumcised and non-circumcised groups. Xhosas circumcise men in their late teens or early 20s, although our study found many men had been circumcised early. According to the criminal law in the Eastern Cape Province,26 traditional circumcision is only supposed to be practiced after the age of 17 years. The mounting evidence of the protective effect of circumcision against HIV suggests that earlier circumcision, performed under safe conditions, may be desirable.
Men having sex with men is an established sexual risk factor in European, and North and South American research on HIV, yet it is very rarely examined in research on sexual practices in Africa. A recent report found that Kenyan men who have sex with men self-report more STI symptoms than men in the general population, but this study lacked both a comparison group and biological data.27 Our study finding that young men who have had sexual contact with men may be more likely to be HIV positive suggests that it is a risk factor for HIV in young men in South Africa that deserves more attention. Although the prevalence of men reporting having had sex with a man is not very high, and the overall number of men with HIV is small, our findings suggest that it is a mistake to overlook this risk factor.
We found that most of the same sex activity was revealed in response to a question framed in terms of coercion, rather than a direct question. This participant group also reported a high rate of male–female rape (see Jewkes et al.13), which indicates that sexual coercion was generally common in the area. It is also possible that this partially reflects a stigmatization of homosexuality and, therefore, a bias against reporting same-sex behaviour as consensual. Approximately two-thirds of African countries still criminalize same-sex behaviour,27 and many men who have sex with men experience high levels of violence, especially sexual violence,25,27,28 whether or not they self-identify. Preliminary findings from Kenya also suggest that self-identified MSM who had recently experienced violence were more likely to have unprotected sex.28 Qualitative research undertaken with study participants suggests that many of the experiences were male rape, but there were also circumstances where men were persuaded to undertake acts that they had not previously thought of doing and where they felt coerced (Sikweyiya Y, personal communication). Only one of the participants in the study openly identified himself to project staff as gay. Further research is needed on the types of male–male sexual encounters, the circumstances under which they occur, the extent to which they are and are not consensual, and their associations with young men's HIV risk.
Limitations of this research included the use of a volunteer sample. Volunteer bias may have altered the relationships between variables in ways that are impossible to determine, but it does not seem likely that this would have had a substantial effect on the study's findings. In other respects, because it was a study with a small geographical base and had tightly controlled fieldwork (see Jewkes et al.7) we may have been more successful than some other researchers in reducing misclassification arising as a result of under-reporting of the sensitive sexual behaviour variables. An indication of this is that our reporting of partner numbers are much higher than those previously reported by Pettifor et al.1(mean number of partners ever 6.9 vs 4.9). Despite the large numbers of partners reported, men's general heterosexual risk-taking behaviour was not associated with HIV risk, and we would suggest that this may be explained by their age and their tendency to have sex with women younger than them, who still generally have a low age-specific HIV prevalence.1
We did not have data on sexually transmitted diseases (STDs) to use in our model. A measure of STDs (whether self-reported or biological) is commonly included in models of factors associated with HIV positivity, but this is not epidemiologically unproblematic. STDs may be (at least partially) pathway variables since they may result from risky sexual practices, as well as increasing risk of HIV in their own right. Many epidemiologists recognize the problem of pathway variables in regression models, as they mask the role of other independent variables. It is usually argued that they should be omitted, or that alternative models with and without them should be presented. A further problem arises with biologically measured STDs is they are subject to much lower levels of measurement error than self-reported sexual practices. There is a substantial risk that models of factors associated with HIV that include biologically measured STDs are masking associations between sexual behaviour and HIV, given the tendency for the under-reporting of stigmatized behaviour to result in the masking of true effects. Although our findings represent an important insight into one model of factors associated with HIV in young men from the rural Eastern Cape province of South Africa, we acknowledge that with other variables there could be other models.
Our findings support arguments made previously that circumcision is an important protective factor against HIV in Africa and that substantial risk is associated with experiences of having impregnated a woman, which may be partly because it is related to intercourse frequency. They also point to the potential importance of male–male sex in young men's HIV risk in Africa. This is a risk factor that has been given scant attention in research and in general HIV prevention interventions in South Africa. The men in our study were young and the prevalence of HIV was low, but the question of what drives the sexual epidemic in the youngest age groups is an important one. Our findings suggest that having sex with men should be included as a measure in sexual behaviour questionnaires for men in Africa and, further, that issues of violence and consent need specific exploration. Deepening understanding of the role of male–male sex in the Southern African HIV epidemic and developing an appropriate programmatic response is potentially important for both young men and their female partners.
KEY MESSAGES
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Acknowledgments |
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This study was funded by the National Institute of Mental Health grant number MH 64882-01 and the South African Medical Research Council. Dr Dunkle's participation was supported by funding from the Harry F. Guggenheim Foundation. We would like to acknowledge the contributions of the following: the National Institute for Communicable Diseases for quality control, testing and storage of specimens; Field nurses & field workers: Leslie Setheni, Veliswa Gobinduku, Yandisa Sikweyiya, Mthokozisi Madiya, Bongwekazi Rapiya, Sanele Mdlungu, Ayanda Mxekezo, Lungelo Mdekazi, Nocawe Mxinwa, Andiswa Njengele, Mvuyo Mayisela; Nobapostile Malu, Lizo Tshona, and Philiswa Bango. Data management, data entry, and secretarial support: Bomkazi Mnombeli, Engela Gerber, Dikeledi Moti, Alta Hansen, and Martie Swart; Prof Daniel Kayongo; Chief Sindile Mtirara; and all the Members of the Community Advisory Board.
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