Epidimiology & Social
HIV infection among youth in a South African mining town is associated with herpes simplex virus-2 seropositivity and sexual behaviour
Auvert, Bertrana,b; Ballard, Ronc; Campbell, Catherined; Caraël, Michele; Carton, Matthieua; Fehler, Glendac; Gouws, Eleanorf; MacPhail, Catherineg; Taljaard, Dirkg; Van Dam, Johannesh; Williams, Briang
From aINSERM U88, Saint-Maurice, the bHôpital Ambroise Paré, Boulogne-Billancourt, France, the cReference Centre for Sexually Transmitted Diseases, School of Pathology, University of the Witwatersrand and South African Institute for Medical Research, Johannesburg, South Africa, the dLondon Schools of Economics and Political Science, London, UK, the eUNAIDS, Geneva, Switzerland, the fMedical Research Council, Durban, the gCouncil for Scientific and Industrial Research, Johannesburg, South Africa and the hPopulation Council, Washington DC, USA.
Correspondence to Bertran Auvert, INSERM U88, 14, rue du Val d'Osne, 94415 Saint-Maurice Cedex, France. E-mail: firstname.lastname@example.org
Received: 30 June 2000;
revised: 10 November 2000; accepted: 20 December 2000.
Sponsorship: The original project was funded by the Department for International Development from the beginning of 1998 and by the US Agency for International Development through the Population Council's Horizons Project since the beginning of 1999 under Cooperative agreement HRN-A-00-97-00012-00. Funding was received from Agence Nationale de Recherche contre le SIDA (2000-129), Ensemble Contre le SIDA, Institut National de la Santé et de la Recherche Médicale, Glaxo Wellcome Research and Development UK and UNAIDS. The Gauteng Department of Health contributed to the costs of the survey. Support was provided by the Council for Scientific and Industrial Research, the South African Institute for Medical Research, the London School of Economics and Progressus.
Note: The authors of this paper are listed alphabetically. Their respective contributions were as follows: Bertran Auvert conceptualized the HSV-2 part of the study, arranged for the laboratory testing to be done, supervized the analysis of the data, and wrote the first draft of the paper. Brian Williams, who is the principal investigator for the Carletonville–Mothusimpilo Project, and Catherine Campbell conceptualized the original project and they have been responsible for running the project since its inception in January 1998. Catherine Campbell was responsible for co-ordinating all the social science aspects of the project. Catherine MacPhail worked extensively with Catherine Campbell and Michel Caraël on the social and behavioural aspects of the work and carried out the validation study. Dirk Taljaard was responsible for carrying out the biomedical and social surveys and gave inputs for the data analysis. Ron Ballard and Glenda Fehler co-ordinated and supervised all of the laboratory testing and provided valuable input concerning HSV-2 in particular. Eleanor Gouws contributed to the statistical analysis of the data. Johannes Van Dam was involved in the conceptualization and design of the project and has worked closely with Brian Williams on the epidemiological aspects and with Catherine Campbell on the social aspects of the study. Matthieu Carton carried out statistical analysis and contributed to writing the first draft of the paper. Michel Caraël was responsible for the design of the social and behavioural questionnaire and has provided important technical advice regarding the social aspects of the project.
Objectives: To determine the seroprevalence of HIV and herpes simplex virus-2 (HSV-2) by age and gender among young people aged 14-24 years in a South African town and to identify risk factors for HIV infection.
Design: A community-based, cross-sectional study was conducted on a random sample of men (n = 723) and women (n = 784) living in a township in the Carletonville district of South Africa.
Methods: Potential demographic and behavioural risk factors associated with HIV were recorded by questionnaire and biological tests were performed on serum and urine. Data analysis was performed using multivariate logistic regression.
Results: Among men and women the prevalence of HIV infection was 9.4 and 34.4%, respectively, and of positive HSV-2 serology was 17.0 and 53.3%, respectively. Among 24-year-old women the prevalence of HIV was 66.7% [95% confidence interval (CI), 54.6–77.3%]. HSV-2 seropositivity was a strong independent risk factor for HIV infection with odds ratios of 5.3 (95% CI, 2.7–10.3) for men and 8.4 (95% CI, 4.9–14.2) for women. There was no independent effect of age at first sex or serological markers of other sexually transmitted infections on HIV infection.
Conclusions: HIV infection among young women increases rapidly after the onset of sexual activity and reaches extremely high levels by 24 years of age. These findings suggest that rates of HIV transmission from men to women are high and that HSV-2 plays a major role in the spread of HIV in this population.
South Africa is experiencing one of the most rapidly growing HIV epidemics in the world. In 1990 the prevalence of HIV infection among women attending antenatal clinics was less than 1%. At the end of 1999 national antenatal prevalence had reached 23% with provincial prevalences ranging from a low of 7% in the Western Cape to a high of 33% in KwaZulu/Natal . There is some evidence that the rates of infection in KwaZulu/Natal are levelling off .
Many studies have investigated risks factors for HIV infection among adults in sub-Saharan countries and the most important risk factors that have been identified include risky sexual behaviour, the presence of sexually transmitted infections (STI) and lack of male circumcision [2–8]. In the past, particular attention has been paid to sexually transmitted infections that can lead to genital ulcer disease (GUD) such as those caused by Treponema pallidum, Haemophilus ducreyi and herpes simplex virus type 2 (HSV-2), because these infections are known to increase both the susceptibility of uninfected people to HIV and the infectivity of people who are themselves infected with HIV [2,5,9–13]. A recent study undertaken in South Africa among men attending sexually transmitted diseases (STD) clinics found that HSV-2 was the most common cause of GUD with an overall seroprevalence of antibodies to HSV-2 of around 50% .
Most studies of the prevalence of HSV-2 and its role as a risk factor for HIV have been carried out in particular groups that are not representative of the overall population, such as STD or antenatal clinic attendees, blood donors, or men who have sex with men [9,15–19]. Only three population-based surveys have been reported from Africa [20–22]. None of these focused on the association between HIV and HSV-2 infection among youth specifically even though young people, and especially young women, are at particularly high risk of HIV infection in many developing countries .
The purpose of the present study was: (1) to measure the prevalence of HIV and HSV-2 seropositivity by gender and age among 14- to 24-year-olds living in a South African township; and (2) to assess risk factors for HIV infection in these young people, with particular regard to the role of HSV-2 seropositivity. The results are discussed in terms of prevention efforts that are needed to protect young people from becoming infected with HIV.
In August 1999 a population-based, cross-sectional study was conducted in a township northwest of Carletonville, in Gauteng Province, South Africa. The Carletonville district, with a population of 150 000 people, contains the largest gold-mining complex in the world, which houses approximately 70 000 migrant mineworkers  in twelve single-sex hostel complexes around the mineshafts to the south of Carletonville town. The survey was designed to collect data on 800 men and 800 women aged 14 to 24 years living in a nearby township. Households were selected by a two-stage random sampling technique. Index houses were randomly selected from a map obtained from the local municipal offices. Using each index house as a starting point, a systematic sample of households was taken. The sampling scheme was designed to be self-weighting. All men and women aged 14 to 24 years, who slept in the selected households the night before the study team visit were eligible for inclusion in the study. The field workers were able to find the occupants of 89.0% of the sample households and 11.3% of potential participants declined to participate. Eligible participants were transported to a local facility for the interviews and the collection of blood and urine samples. If eligible participants were not at home, the study team made up to three repeated visits before abandoning that household.
The questionnaire used in this study was based on a UNAIDS questionnaire  adapted to the local situation and to the age of subjects enrolled in the sample. The consent form was presented in the language of the respondent, who was invited to take part in the study, and those who agreed were asked to sign the consent form. The interviewers completed the questionnaire during a private interview in the preferred language of the interviewee. Data were collected on background and behavioural characteristics as well as a medical and sexual history. Sexual partnerships were divided into casual partnerships and other partnerships, that are composed of those who were married or living as married. A section of the questionnaire was reserved for information concerning the respondent's last five casual partnerships.
Following the interview, blood and first-catch urine specimens were collected. A single Capillus HIV-1/HIV-2 latex aggregation test (Cambridge Biotech Corporation, Galway, Ireland), which has a sensitivity and specificity of greater than 99.9 and 99.6%, respectively, was subsequently used to screen the sera for HIV infection. A non-treponemal carbon antigen test (Immutrep RPR test; Omega Diagnostics, Alloa, Scotland, UK) and a specific treponemal test (FTA test, Cellognost Syphilis H; Dade Behring, Marburg, Germany) were used for syphilis serology. A qualitative enzyme-linked immunosorbent assay (ELISA) test was used to detect HSV-2 type specific IgG antibodies (MRL Diagnostics, Los Angeles, California, USA). Neisseria gonorrhoeae- and Chlamydia trachomatis-specific DNA sequences were detected in the urine samples by using ligase chain reaction (LCR) test (Abbott Laboratories, North Chicago, Illinois, USA). Treatment of symptomatic and asymptotic STI's were subsequently offered to all participants prior to destruction of all identifiers and performance of HIV testing. Any participants who wished to know their HIV status were offered a separate ELISA test with pre- and post-test counselling to be arranged through the normal clinic channels.
Laboratory results and data generated from questionnaires were entered twice into a database (Microsoft Access, Redmond, Washington, USA) by different people. The two entries were compared and discrepancies were corrected. The data were then extensively checked for inconsistencies. The files were then imported into the Statistical Package for Social Sciences (SPSS 8.0 for Windows, Chicago, Illinois, USA) and prepared for statistical analysis.
Five months after completion of the survey, a validation study was conducted among a random sample of young people who participated in the main study. This sample was stratified by gender and by whether or not they had ever had sexual intercourse. The aim was to verify the age at first sex and the number of lifetime partners at the time of the survey interview. Of the 120 selected participants, 106 (88.3%) were traced and interviewed using an in-depth, semi-structured topic guide.
A total of 723 men and 784 women agreed to participate in the survey. In order to assess risk factors for HIV infection, the analysis was restricted to men and women who reported ever having had penetrative vaginal intercourse. These individuals are referred to below as ‘sexually active'.
The following risk factors for HIV infection were explored in the univariate analysis. Background characteristics: current age, marital status, whether respondent had living children, living in a squatter settlement, was born in the Carletonville area, had consumed alcohol in the last month, or was currently in secondary school. Sexual practices: age at first sexual intercourse, number of lifetime sexual partners, age difference between respondent and partners, number of current relationships, condom use, having had forced sex, having had sex with married people, having exchanged money for sex (men), and, for women, having had sex with mineworkers. Health issues and STI's: symptoms of STI's in the last year, circumcision status and penile hygiene (men), dry sex (women), serology status for HSV-2 and syphilis (RPR and FTA), and detection of specific DNA sequence of N. gonorrhoeae and of C. trachomatis in urine.
Computations were carried out ignoring clustering. Means and proportions were calculated with 95% confidence intervals (CI). For non-normally distributed parameters, medians were calculated with the inter-quartile range (IQR) and significance testing was carried out using the Kruskall–Wallis test. Medians were compared using the median test. Median and IQR of age at first sexual intercourse and of duration of partnership were computed using survival analysis. Duration of partnerships among men and women were compared using the log rank test.
We used 95% CI of the odds ratio (OR) and χ2 tests to investigate the statistical significance of the association between HIV infection and potential risk factors. Continuous variables were categorized. All risk factors associated with HIV infection at a significance level of 0.25 or less were entered into a forward stepwise selection, multiple logistic regression model. Two models are presented. Model 1 was constructed without HSV-2 serology and model 2 with HSV-2 serology. All potential interactions involving age, HSV-2 serostatus and number of lifetime partners were tested in models 1 and 2.
We compared HIV prevalence among women aged 16–18 years with the HIV prevalence among their casual partners. For this purpose we first estimated the prevalence of HIV among the casual partners of these women by taking the age distribution of their most recent casual partner as reported by the women, and then combining this with the age-specific HIV prevalence of men in the sample. In this estimate, we assumed that the 4.9% (eight of 162) of casual partners above the age of 24 years [with a mean (median) age of 28.7 years (27.5 years)] have the same HIV prevalence (40.0%) as the 24-year-old men in the sample. The male-to-female transmissibility of HIV per-partnership is defined as the probability per-partnership of transmission from an infected man to his female partner. Based on the HIV status of women aged 16–18 years, their number of lifetime partners and the estimate of prevalence among their casual partners, the male-to-female transmissibility of HIV per-partnership was estimated using a Bernoulli model [26,27] and the maximum likelihood method. The IQR was estimated using the non-parametric resampling bootstrap technique  applied to the sample of women aged 16–18 years and to their partners (see Appendix).
Ethical approval for the project was obtained from the committee for Research on Human Subjects of the University of Witwatersrand, Johannesburg, on 10 March 1997 (Protocol number M 970235).
The male-to-female sex ratio was 0.92 (723 of 784) (Table 1). The median age was 18 years for men (IQR, 16–21 years) and 19 years for women (IQR, 16–21 years). Approximately half (53.0%) of the sample was born in the Carletonville district, 26.6% in another urban area in South Africa, 16.1% in a rural area in South Africa and 4.4% in another country. The majority of the participants were either students or scholars (59.7%), or unemployed (31.4%) and three men were mineworkers. Among those aged 14 to 16 years, 94.1% of the men and 85.2% of the women were students or scholars at the time of the survey. Among those aged 17 to 18 years, the corresponding figures were 84.0 and 76.5%, respectively. Background characteristics of sexually active men and women are reported in Table 1.
The median age at first sex was 16.6 years for men (IQR, 15.2–18.2 years) and 17.2 years for women (IQR, 16.0–18.5 years). The first decile for age at first sex was 13.7 years for men and 15.0 for women. At the time of the interview, 77.6% (560 of 722) of the men and 79.4% (622 of 783) of the women reported having had sex. The majority of men (96.5%) and women (86.5%) had never been married. Of the men, 5.8% said that they had had more than 11 lifetime sexual partners whereas among the women, 7.8% said that they had had more than four partners. The proportion of men and women who lived in the Carletonville area at the time of first sex was 85.5 and 75.7%, respectively. From the age of the participants and the reported age at first sex, we estimated that the proportion of young women aged 15 to 19 years who were sexually active increased significantly between 1994 and 1999 (56.9 versus 67.5%, P = 0.0032). This increase was not significant among men in the same age group (65.9 versus 68.4%, P = 0.51).
Sexual behaviour characteristics of sexually active men and women are reported in Table 2. The mean (median) number of lifetime partners was 4.7 (3) and 2.6 (2), respectively. Of the women, 9.0% reported having had sexual partners who were at least 10 years older than themselves. The median number of sexual acts in the last month was one for both men and women. Of those who had at least one current casual relationship, 28.3% of men and 13.7% of women had more than one current relationship. Forty one percent of men and 42.5% of women reported never having used condoms. Of the women, 15.8% reported ever having had sex against their will.
We considered the last five casual relationships, 1578 for men and 1345 for women, as reported by the respondents. Of sexually active men and women, 80.5 and 95.6%, respectively had five or fewer casual relationships. Women generally had casual partners who were older than themselves (median age difference of 2 years; IQR, 0–5 years) whereas men generally had casual partners who were younger than themselves (median age difference of 3 years; IQR, 1–5 years). The median duration of relationships reported by women (12 months; IQR, 4–48 months) was longer than the duration of relationships reported by men (8 months; IQR, 2–37 months) (P < 0.0001). The median number of times that sexual intercourse occurred per relationship for women (6; IQR, 3 to > 20) was significantly higher than that for men (3; IQR, 1–7) (P < 0.0001). The casual partners of women were more likely to be married than were the casual partners of men (10.8 versus 2.4%, respectively, P < 0.0001). Of the relationships reported by women, 7.8% involved mineworkers. The casual partners of women living in squatter settlements were more likely to be mineworkers than were the casual partners of other women (12.4 versus 3.9%, respectively, P < 0.0001). Condoms were never or rarely used in 68.8% of the relationships reported by men and in 75.6% of relationships reported by women. However, the situation is improving: whereas condoms were never or rarely used in 80.2% of relationships that started between 1993 and 1995, this had fallen to 69.3% in relationships that started between 1996 and 1998 (P < 0.0001).
Prevalence of HIV and HSV-2 seropositivity
The overall prevalence of HIV was 22.4% (338 of 1507) and of HSV-2 seropositivity was 35.4% (533 of 1489) with higher rates among women than among men. The prevalence of HIV infection was 9.4% (68 of 723) among men and 34.4% (270 of 784) among women and of HSV-2 was 17.0% (122 of 718) among men and 53.3% (411 of 771) among women. The comparison of HIV prevalence and HSV-2 seroprevalence by age among men and women shows that in both genders and in all age groups HSV-2 seroprevalence exceeded HIV prevalence (Figs 1a, b). The prevalence of HIV and HSV-2 seropositivity increased rapidly with age, especially among women. The prevalence of HIV increased from 6.1% (95% CI, 1.2–11.0) among women aged 14 to 15 years to 66.7% (95% CI, 56.0–77.4) among women aged 24 years, and the prevalence of HSV-2 seropositivity rose from 18.6% (95% CI, 11.4–25.8) to 94.3% (95% CI, 87.6–100). Among HIV-seropositive individuals, 64.7% of men and 90.7% of women were also HSV-2 positive.
Among those who said that they had never had sex, 13 of 323 (4.0%) were HIV-positive and 26 of 319 (8.2%) were HSV-2 positive representing 3.8% (13 of 338) and 4.9% (26 of 533) of all HIV and HSV-2 positive individuals, respectively.
The increase in prevalence of HIV and of HSV-2 seropositivity by number of lifetime partners was more marked among women than among men (Fig. 2a, b). The HIV prevalence among men who said that they had never had sex was 1.2% (95% CI, 0.0–3.8%) and reached 18.8% (95% CI, 4.7–32.8%) among men who reported having had eight to 10 lifetime partners. Among women who reported having had zero, one, two and three or more lifetime partners, the prevalence of HIV was 6.8, 19.9, 42.7 and 56.1%, respectively.
Among sexually active men and women the prevalence of HIV was 11.8 and 41.6%, respectively, and the median (IQR) number of lifetime partners was 3 (2–4) and 2 (1–3), respectively. If we consider only sexually active women aged 16 to 18 years, the prevalence of HIV was 21.1% (95% CI, 15.9–26.2%), the median (IQR) number of sexual partners was 1 (1–2) and the mean 1.7 (95% CI, 1.6–1.9). Among these sexually active women, 3.0% (95% CI, 0.0–6.2%) declared ever having had a casual partnership with a mineworker. HIV prevalence among those who declared casual partnerships only with men living in the township did not differ from other women of the same age group who declared no casual partnerships with miners (20.0 versus 20.4%, P = 1.0). Using the method described above, we estimated that the prevalence of HIV among the 162 most recent casual partners of these women is 13.4%. It appears, therefore, that the prevalence of HIV among the partners of women aged 16 to 18 years is lower than among the women themselves. The male-to-female per-partnership transmissibility (IQR) from men to women aged 16 to 18 years is estimated to be 0.92 (0.77–1) per partnership. If women under-report their number of lifetime partners by a factor of 2, say, then this transmissibility is estimated to be 0.49 (0.39–0.56) (see Appendix).
Risk factors for HIV status of sexually active men and women
The HIV prevalence amongst married men was found to be more than four times greater (44.0%/10.0%) than the prevalence amongst men who had never been married (OR, 7.1; 95% CI, 3.0–16.3) (Table 1). Being married was also a risk factor for women but the OR was smaller (OR, 2.9; 95% CI, 1.8–4.4). About four out of every ten women had at least one living child and the prevalence of HIV among these women was higher than among those without children (54.8 and 32.9%, respectively; P < 0.0001). The prevalence of HIV was higher among men and women born outside the Carletonville area than it was among those born in the Carletonville area. It was also higher among those not attending secondary school. Almost half of the men, but only 16.2% of the women, drank alcohol at least once a month, and those who consumed alcohol were more likely to be HIV infected than those who did not.
HIV prevalence was lower amongst those who had sex for the first time at or before 15 years of age for men and for women (Table 2). However, this is probably due to the relationship between age and age at first sex in our sample, which is composed of sexually active people. When adjusted for age, the OR related to age at first sex became non significant (men: adjusted OR, 1.5; 95% CI, 0.8–2.7; women: adjusted OR, 0.8; 95% CI, 0.5–1.3).
The likelihood of being infected with HIV increased with the number of sexual partners. Compared to those who had one casual partner, the odds ratio for HIV infection for those who had two partners was 1.1 for men (95% CI, 0.4–2.7) and 3.0 for women (95% I, 1.9–4.7). For those who had three or more partners the odds ratio was 2.1 for men (95% CI, 1.0–4.3) and 6.0 for women (95% CI, 3.9–9.2). For men the prevalence of HIV was not significantly associated with the number of current relationships or whether or not they had at least one casual partner who had other sexual partners. Both men and women who used condoms during their first sexual encounter were less likely to be infected with HIV than those who did not. Women who reported having had sex with mineworkers were more likely to be infected with HIV than those who said that they had not.
Health issues and STI's
Self-reported symptoms of STI's in the last year were common in both sexes (18.0% of men and 31.9% of women reported having had a discharge or genital pain in the last year) and HIV prevalence was higher amongst those who reported such symptoms (Table 3). Circumcision was not common (only 10.1% of men were circumcised) and median (IQR) age at circumcision was 16 years (12–19 years). No protective effect of circumcision on HIV prevalence was shown. The prevalence of HIV was lower among the 21 sexually active men who were circumcised before their first sexual encounter than among the 535 other sexually active men (4.8 versus 12.1%) but the difference was not significant (P = 0.50). The few men (12.7%) who washed their penis with soap less than once a day had a higher prevalence of HIV than among those who did wash it at least once a day. The highest odds ratios for men were related to HSV-2 serology and syphilis serology. Men who were HSV-2 seropositive were seven times (prevalence ratio, 38.7%/5.2%) more likely to be HIV positive than men who were HSV-2 seronegative. The association between positive urine tests for N. gonorrhoeae or C. trachomatis and HIV status was not significant.
For women the association between syphilis and HIV was not significant whereas the association between N. gonorrhoeae and HIV was significant. For women, being infected with HSV-2 was strongly associated with HIV infection. No significant effect of dry sex or of time between menarche and first sex was found on HIV status.
Multivariate analysis of risk factors
In the multivariate analysis, only a few factors were significantly associated with HIV (Table 4). For men, in model 2, six factors were significantly associated with HIV namely HSV-2 serostatus, age, history of discharge, genital pain or sores in the last year, ever having had sex against his will, not attending secondary school and washing the penis with soap less than once a day. The most significant factor associated with HIV status was HSV-2 serostatus. With the exception of HSV-2 serostatus, model 1 and model 2 are composed with the same risk factors. For women, in model 2, four factors were significantly associated with HIV namely HSV-2 serostatus, age, number of sexual partners and type of housing. As for men, the most significant factor was HSV-2 serostatus. In comparison with model 2, model 1 included two additional factors namely reporting sexual partnership with a mineworker and reporting at least one casual partnership involving 20 or more sexual acts. Interactions tested did not reach statistically significant levels. When adjusted for factors composing model 1, the OR related to syphilis status was non-significant (men: adjusted OR, 3.0; 95% CI, 0.7–12.6; women: adjusted OR, 1.0; 95% CI, 0.4–2.4) and the OR related to HSV-2 status was close to values in model 2 (men: adjusted OR, 5.3; 95% CI, 2.7–10.3; women: adjusted OR ,8.3; 95% CI, 4.8–14.3).
The prevalence of HIV infection detected among people aged 14 to 24 years recorded in this study was extremely high. In South Africa, the prevalence of HIV infection has increased rapidly over the last few years. In Gauteng, the province within which Carletonville falls, the prevalence of HIV infection among women aged 15 to 49 years attending antenatal clinics in the public sector, increased from 0.7% in 1990, to 2.5% in 1992 and 15.5% in 1996 . Although surveillance studies have been conducted at several sentinel sites in South Africa, Carletonville is one of only a few sites at which a large-scale, population-based study has been conducted. Further research is urgently needed to assess the situation in other urban and rural centres in South Africa, to determine the likelihood that equally high infection rates have been reached, and to plan interventions.
The results presented here are from a large, population-based, cross-sectional study conducted in August 1999 in which the refusal rate was low. The quality of the data on reported sexual behaviour was reasonably good as assessed by a validation study among 106 randomly selected respondents. Of those people who indicated in the survey that they had not had sex, 11 of 54 (20.4%) subsequently said in the validation study that they had experienced sex at the time of the survey. Among those who reported having had at least one lifetime partner at the time of the survey, the median of the paired differences in the number of lifetime partners reported in the survey and the validation study was 0 (IQR, -1 to 1). Among these people, seven of 27 women (25.9%) and six of 21 men (28.9%) reported a higher number of lifetime partners in the subsequent validation study. These results indicate that there was some inconsistent reporting of lifetime partners by both sexes.
The main risk factors for HIV were related to STI's, sexual behaviour and age. Multivariate risk factor analysis showed that reporting symptoms of STI's in the last year was an independent risk factor for HIV amongst men. Syphilis serological status did not appear to be independently associated with HIV but the power of the analysis of this association was small because of the low syphilis prevalence in the studied population. Among women, the age at first sex and having been forced to have sex, which appeared to be relatively common in this population, were not independent risk factors for HIV infection. By contrast, the number of lifetime partners was a strong and independent predictor of HIV status among women. The significant increase in HIV prevalence as a function of the number of lifetime partners indicates the high vulnerability of young women to HIV infection.
We found that women being married or living as married, and women and men reporting casual partnerships with 20 or more sexual acts are more at risk of HIV infection. A likely interpretation is that the per-partnership transmission of HIV from males-to-females and from females-to-males depends on the number of sexual acts in the relationship. Having had a sexual relationship with a mineworker was a significant independent risk factor only when not taking account of HSV-2. It is likely that sexual relationship with mineworkers, the vast majority of whom live in single-sex hostels without their wives or families, who are relatively well paid, and whose HIV prevalence is 28.5% , could have played a role in the introduction of HIV in this township. But the low proportion of young township women reporting ever having had a sexual relationship with a mineworker indicates that the current high HIV prevalence in the township is unlikely to be sustained solely by sexual mixing with mineworkers.
In this study a strong, independent association between HIV and HSV-2 serological status was detected. The high seroprevalence of HSV-2, the association between HIV infection and HSV-2 seroprevalence, and the fact that HSV-2 infection is a cause of genital lesions indicate that HSV-2 infection could play a major role in the spread of HIV in the population of this study. A recent study conducted in South Africa drew attention to the likely impact of genital herpes on HIV infection . Our study supports those previous findings. Although HSV-2 has been used as a marker of sexual risk behaviour , the relationship between HIV and HSV-2 infection is complex and poorly understood. Whereas it is highly likely that HSV-2 facilitates infection with HIV, being infected with HIV may also facilitate the spread of HSV-2 [4,9,14,18–20,22,31–36]. Further studies, in particular longitudinal studies involving available treatments for HSV-2, are needed to elucidate the nature of the relationship between infection with HSV-2 and HIV, especially among youth, in order to understand the spread of HIV in sub-Saharan Africa and the role played by HSV-2 infection.
The finding that poor penile hygiene was associated with HIV infection is important and should help in the design of interventions, even though most of the men in this study already washed their penis at least once a day. The effect of post-coital cleansing on HIV transmission should be investigated.
The prevalence of HIV infection among sexually active women between the ages of 16 and 18 years was high (21.1%) even though they only reported a median of one lifetime partner (upper quartile 2) and the best estimate of HIV prevalence among their casual partners was 13.4%. It is clear from our data that the high prevalence of HIV infection among young women is not simply due either to very high rates of infection amongst their partners or to very high levels of sexual activity. Even if there is under-reporting of sexual activity, as is likely to be the case among women in particular, the validation study indicates that it is unlikely that such under-reporting would be sufficient to substantially change these arguments.
Rather, the high rates of HIV infection among these young women are suggestive of high male-to-female transmissibility. A recent review of European and American studies found estimates of heterosexual, male-to-female transmissibility ranging from 0.1 to 0.3 per partnership . Our estimates of transmissibility are substantially higher than those reported in developed countries and several factors could explain this difference. A recent study has shown that viral load is an important predictor of the risk of heterosexual transmission of HIV-1 in Uganda  and viral loads in South Africa may be higher than in Europe and America. Alternatively, the high prevalence of genital herpes  in our sample might contribute to the high transmissibility of HIV. Further studies are needed to explore infection rates in young women and these should ideally include measurements of the viral load in the HIV-positive partners of these women, including mineworkers. Finally, this high male-to-female transmissibility could be explained by under-reporting of lifetime partners by women but even if we assume that women under-report by a factor of two, the estimate of per partnership male-to-female transmissibility is still substantially higher than that reported in developed countries.
Reducing HIV transmission in this population is a major challenge. The survey data reported here were collected as part of an intervention to control STI's and ultimately HIV–AIDS in a major mining centre. At the present time there is insufficient evidence concerning the extent to which HSV-2 increases the transmission of HIV to recommend mass treatment of genital herpes. Moreover, genital herpes, a viral STI, can only be treated symptomatically or suppressed by using specific antiviral drugs at considerable cost, and no HSV-2 vaccine is currently commercially available. Therefore, the best options for reducing transmission includes prompt treatment of curable STI's, communication campaigns aimed at alerting the population to the relatively mild manifestations of genital herpes and the need to abstain from sexual contact while lesions persist. In addition it is important to find ways to persuade young people to reduce their number of lifetime partners and to substantially increase condom use. Our evidence for an increase in reported condom use among young people between 1992–1995 and 1996–1999 is encouraging but rates of condom use are still disappointingly low. We believe that condom use should be promoted as strongly as possible, and that only a high rate of consistent condom use will have an effect on the spread of HIV and other STI's in this population. As most young people in this study were still at school when they had their first sexual experience, attempts to limit the future spread of HIV should involve not only prevention in the community but also the development, evaluation and implementation of effective school-based interventions as an essential part of the school curriculum.
We thank all those who supported this work and in particular the Carletonville community and the Mothusimpilo intervention team: Solly Moema, Zodwa Mzaidume and Bareng Rasego. Very special thanks go to Reathe Taljaard and Gaph Pathedi who helped to make the survey possible. Mrs. Venessa Tshabalala-Maseko, Mr. F. Radebe, Mr. D. Mabaso and Mr S. Khumalo provided excellent technical assistance in regard to the laboratory testing. We thank Lewis Ndhlovu, Population Council, South Africa and Jamie Robinson, Wellcome Research and Development, UK for their invaluable assistance and support.
1. Anon. Report, 1999: National HIV Sero-prevalence Survey of Women Attending Public Antenatal Clinics in South Africa.
Pretoria, South Africa: Department of Health; 2000:1–13.
2. Behets FM, Liomba G, Lule G. et al
. Sexually transmitted diseases and human immunodeficiency virus control in Malawi: a field study of genital ulcer disease. J Infect Dis 1995, 171: 451 –455.
3. Simonsen JN, Cameron DW, Gakinya MN. et al
. Human immunodeficiency virus infection among men with sexually transmitted diseases. Experience from a center in Africa.
N Engl J Med 1988, 319: 274 –278.
4. Langeland N, Haarr L, Mhalu F. Prevalence of HSV-2 antibodies among STD clinic patients in Tanzania. Int J STD AIDS 1998, 9: 104 –107.
5. Plourde PJ, Pepin J, Agoki E. et al
. Human immunodeficiency virus type 1 seroconversion in women with genital ulcers. J Infect Dis 1994, 170: 313 –317.
6. Halperin DT, Bailey RC. Male circumcision and HIV infection: 10 years and counting. Lancet 1999, 354: 1813 –1815.
7. Cameron DW, Simonsen JN, D'Costa LJ. et al
. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet 1989, 2: 403 –407.
8. Bassett MT, McFarland WC, Ray S. et al
. Risk factors for HIV infection at enrollment in an urban male factory cohort in Harare, Zimbabwe. J Acquir Immune Defic Syndr Hum Retrovirol 1996, 13: 287 –293.
9. Holmberg SD, Stewart JA, Gerber AR. et al
. Prior herpes simplex virus type 2 infection as a risk factor for HIV infection. JAMA 1988, 259: 1048 –1050.
10. Perez G, Skurnick JH, Denny TN. et al
. Herpes simplex type II and Mycoplasma genitalium
as risk factors for heterosexual HIV transmission: report from the heterosexual HIV transmission study. Int J Infect Dis 1998, 3: 5 –11.
11. Gray RH, Wawer MJ, Sewankambo NK. et al
. Relative risks and population attributable fraction of incident HIV associated with symptoms of sexually transmitted diseases and treatable symptomatic sexually transmitted diseases in Rakai District, Uganda. Rakai Project Team.
AIDS 1999, 13: 2113 –2123.
12. Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases.
Sex Transm Dis 1992, 19: 61 –77.
13. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999, 75: 3 –17.
14. Chen CY, Ballard RC, Beck-Sague CM. et al
. Human immunodeficiency virus infection and genital ulcer disease in South Africa: the herpetic connection. Sex Transm Dis 2000, 27: 21 –29.
15. Cowan FM, Johnson AM, Ashley R, Corey L, Mindel A. Antibody to herpes simplex virus type 2 as serological marker of sexual lifestyle in populations. BMJ 1994, 309: 1325 –1329.
16. Cunningham AL, Lee FK, Ho DW. et al
. Herpes simplex virus type 2 antibody in patients attending antenatal or STD clinics. Med J Aust 1993, 158: 525 –528.
17. Ades AE, Peckham CS, Dale GE, Best JM, Jeansson S. Prevalence of antibodies to herpes simplex virus types 1 and 2 in pregnant women, and estimated rates of infection. J Epidemiol Community Health 1989, 43: 53 –60.
18. Krone MR, Wald A, Tabet SR, Paradise M, Corey L, Celum CL. Herpes simplex virus type 2 shedding in human immunodeficiency virus-negative men who have sex with men: frequency, patterns, and risk factors. Clin Infect Dis 2000, 30: 261 –267.
19. Schacker T, Zeh J, Hu HL, Hill E, Corey L. Frequency of symptomatic and asymptomatic herpes simplex virus type 2 reactivations among human immunodeficiency virus-infected men. J Infect Dis 1998, 178: 1616 –1622.
20. Wagner HU, Van Dyck E, Roggen E. et al
. Seroprevalence and incidence of sexually transmitted diseases in a rural Ugandan population. Int J STD AIDS 1994, 5: 332 –337.
21. Obasi A, Mosha F, Quigley M. et al
. Antibody to herpes simplex virus type 2 as a marker of sexual risk behavior in rural Tanzania. J Infect Dis 1999, 179: 16 –24.
22. McFarland W, Gwanzura L, Bassett MT. et al
. Prevalence and incidence of herpes simplex virus type 2 infection among male Zimbabwean factory workers. J Infect Dis 1999, 180: 1459 –1465.
23. UNAIDS. AIDS epidemic update: December 1999.
In: Report on the Global HIV/AIDS Epidemic
Geneva: UNAIDS; 2000: 46– 49
24. Williams B, Campbell C. Response to HIV/AIDS in the Mining Industry: Past Experiences and Future Challenges. Managing HIV/AID in South Africa. Lessons from Industrial Settings.
Johannesburg, South Africa: Council for Industrial and Scientific Research; 1999: 13– 29.
25. UNAIDS. Looking deeper into the HIV epidemic: a questionnaire for tracing sexual networks.
In: Best Practice Collection, Key Material 98/27.
Geneva: UNAIDS; 1998: 1– 24.
26. Vittinghoff E, Douglas J, Judson F, McKirnan D, MacQueen K, Buchbinder SP. Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol 1999, 150: 306 –311.
27. Grant RM, Wiley JA, Winkelstein W. Infectivity of the human immunodeficiency virus: estimates from a prospective study of homosexual men. J Infect Dis 1987, 156: 189 –193.
28. Carpenter J, Bithell J. Bootstrap confidence intervals: when, which, what? A practical guide for medical statisticians. Stat Med 2000, 19: 1141 –1164.
29. Swanevelder JP, Kustner HG, van Middelkoop A. The South African HIV epidemic, reflected by nine provincial epidemics, 1990
S Afr Med J 1998, 88: 1320 –1325.
30. Gilgen D, Campbell C, Williams B, Taljaard D, MacPhail C. The Natural History of HIV/AIDS in South Africa: a Biomedical and Social Survey in Carletonville.
Johannesburg, South Africa: Council for Scientific and Industrial Reasearch; 2000: 41 41.
31. Augenbraun M, Feldman J, Chirgwin K. et al
. Increased genital shedding of herpes simplex virus type 2 in HIV-seropositive women. Ann Intern Med 1995, 123: 845 –847.
32. Gwanzura L, McFarland W, Alexander D, Burke RL, Katzenstein D. Association between human immunodeficiency virus and herpes simplex virus type 2 seropositivity among male factory workers in Zimbabwe. J Infect Dis 1998, 177: 481 –484.
33. Hook EWD, Cannon RO, Nahmias AJ. et al
. Herpes simplex virus infection as a risk factor for human immunodeficiency virus infection in heterosexuals. J Infect Dis 1992, 165: 251 –255.
34. Kamali A, Nunn AJ, Mulder DW, Van Dyck E, Dobbins JG, Whitworth JA. Seroprevalence and incidence of genital ulcer infections in a rural Ugandan population. Sex Transm Infect 1999, 75: 98 –102.
35. Wald A, Zeh J, Selke S. et al
. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N Engl J Med 2000, 342: 844 –850.
36. Mbopi-Keou FX, Gresenguet G, Mayaud P. et al
. Interactions between herpes simplex virus type 2 and human immunodeficiency virus type 1 infection in African women: opportunities for intervention. J Infect Dis 2000, 182: 1090 –1096.
37. Mastro TD, Kitayaporn D. HIV type 1 transmission probabilities: estimates from epidemiological studies. AIDS Res Hum Retroviruses 1998, 14 (Suppl 3): S223 –S227.
38. Quinn TC, Wawer MJ, Sewankambo N. et al
. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group.
N Engl J Med 2000, 342: 921 –929.
In a Bernoulli model, the probability of remaining uninfected is (1− T)n, where n is the number of partners and T is the per-partnership transmission so that the probability of infection is 1−(1− T)n.
Let τ be the male-to-female transmissibility of HIV per-partnership, and Pm be the prevalence of HIV among the pool of men who are the casual partners of the women. Under the hypothesis that women choose their casual partners randomly, the probability of HIV infection (Pw) for a woman who has had n non-spousal partners is EQUATION Applying equation (1) to women aged 16 to 18 years; the maximum likelihood estimate of τ Pm is 0.124. With Pm = 13.4% we obtain a value for the transmissibility of τ = 0.92, and for the IQR by the bootstrap technique of 0.77–1. If we assume that women under-report their number of lifetime partners by a factor of 2, the estimate of τ Pm is 0.0658. With Pm = 13.4% we obtain a value for the transmissibility of τ = 0.49, and a IQR of 0.39–0.56. Cited Here...
This article has been cited 98 time(s).
International Journal of Std & AIDSPartner-concurrency associated with herpes simplex virus 2 infection in young South AfricansInternational Journal of Std & AIDS
International Journal of Std & AIDSBirds of a feather: homophily and sexual network structure in sub-Saharan AfricaInternational Journal of Std & AIDS
British Medical Journal
The impact of HIV and AIDS on Africa's economic development
British Medical Journal, 324():
Journal of Infectious Diseases
How does herpes simplex virus type 2 influence human immunodeficiency virus infection and pathogenesis?
Journal of Infectious Diseases, 187():
Scandinavian Journal of Infectious DiseasesSexually transmitted herpes simplex virusesScandinavian Journal of Infectious Diseases
International Journal of Gynecology & ObstetricsHIV infection among pregnant women in NigeriaInternational Journal of Gynecology & Obstetrics
Journal of the South African Institute of Mining and Metallurgy
Measuring the impact of HIV and STIs in a community in a coal mining town, Mpumalanga, South Africa
Journal of the South African Institute of Mining and Metallurgy, 105(6):
Drug use patterns and infection with sexually transmissible agents among young adults in a high-risk neighbourhood in New York City
International Journal of Std & AIDS
Heavy episodic drinking among Kenyan female sex workers is associated with unsafe sex, sexual violence and sexually transmitted infections
International Journal of Std & AIDS, 18():
Journal of Infectious Diseases
Herpes simplex virus type 2 infection as a risk factor for human immunodeficiency virus acquisition in men who have sex with men
Journal of Infectious Diseases, 187(1):
Studies in Family Planning
Female genital cutting and HIV/AIDS among Kenyan women
Studies in Family Planning, 38(2):
Philosophical Transactions of the Royal Society of London Series B-Biological Sciences
The epidemiology of human immunodeficiency virus in South Africa
Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 356():
Journal of Infectious Diseases
Changes in plasma human immunodeficiency virus type 1 RNA associated with herpes simplex virus reactivation and suppression
Journal of Infectious Diseases, 186():
AIDSChanging patterns of knowledge, reported behaviour and sexually transmitted infections in a South African gold mining communityAIDS
Lancet Infectious Diseases
HIV and male circumcision - a systematic review with assessment of the quality of studies
Lancet Infectious Diseases, 5(3):
ContraceptionPredictors of dual method use for pregnancy and HIV prevention among adolescent South African womenContraception
Journal of Biosocial ScienceAdolescent sexuality and the HIV epidemic in Yaounde, CameroonJournal of Biosocial Science
Emerging Infectious Diseases
Health consequences of child marriage in Africa
Emerging Infectious Diseases, 12():
American Journal of Public HealthPredictors of condom use among young adults in South Africa: The Reproductive Health and HIV Research Unit National Youth SurveyAmerican Journal of Public Health
The multicentre study on factors determining the differential spread of HIV in four African cities: summary and conclusions
Jaids-Journal of Acquired Immune Deficiency Syndromes
Opportunity for prevention of HIV and sexually transmitted infections in Kenyan youth: Results of a population-based survey
Jaids-Journal of Acquired Immune Deficiency Syndromes, 31(5):
International Journal of Std & AIDS
Heterosexual transmission of HIV in Africa: an empiric estimate
International Journal of Std & AIDS, 14(3):
Bmc Infectious DiseasesSeroepidemiology of Herpes Simplex virus type 1 and 2 in Western and Southern Switzerland in adults aged 25-74 in 1992-93: a population-based studyBmc Infectious Diseases
Male circumcision and risk of HIV-1 infection
Factors affecting HIV concordancy in married couples in four African cities
Journal of VirologySusceptibility of CCR5-deficient mice to genital herpes simplex virus type 2 is linked to NK cell mobilizationJournal of Virology
Response to Brown et al., 'incident and prevalent herpes simplex virus type 2 infection increases risk of HIV acquisition among women in Uganda and Zimbabwe'
Sexually Transmitted Infections
Prevalence of herpes simplex type 2 and syphilis serology among young adults in a rural Gambian community
Sexually Transmitted Infections, 77(5):
Bmc Public HealthAssociations between sexual behaviour change in young people and decline in HIV prevalence in ZambiaBmc Public Health
International Journal of Std & AIDS
Does selected ecological evidence give a true picture of HIV transmission in Africa?
International Journal of Std & AIDS, 15(7):
International Journal of Std & AIDS
Running on empty: sexual co-factors are insufficient to fuel Africa's turbocharged HIV epidemic
International Journal of Std & AIDS, 15(7):
Journal of Biosocial ScienceSocioeconomic status as a risk factor for HIV infection in women in East, Central and southern Africa: A systematic reviewJournal of Biosocial Science
Demographic ResearchSexual behaviour patterns in South Africa and their association with the spread of HIV: Insights from a mathematical modelDemographic Research
Young people's sexual health in South Africa: HIV prevalence and sexual behaviors from a nationally representative household survey
Scandinavian Journal of Infectious DiseasesMinimal change in HSV-2 seroreactivity: A cross-sectional Swedish population studyScandinavian Journal of Infectious Diseases
Bmc Public HealthEffects of neighbourhood-level educational attainment on HIV prevalence among young women in ZambiaBmc Public Health
International Journal of Std & AIDS
Relative risk of HIV infection among young men and women in a South African township
International Journal of Std & AIDS, 13(5):
The spread and effect of HIV-1 infection in sub-Saharan Africa
Journal of Infectious Diseases
Progress in meeting today's demands in genital herpes: An overview of current management
Journal of Infectious Diseases, 186():
Sexually Transmitted InfectionsSentinel surveillance of sexually transmitted infections in South Africa: a reviewSexually Transmitted Infections
Bmc Infectious DiseasesHIV-1, HSV-2 and syphilis among pregnant women in a rural area of Tanzania: Prevalence and risk factorsBmc Infectious Diseases
Sexually Transmitted InfectionsComparison of focus HerpesSelect and Kalon HSV-2 gG2 ELISA serological assays to detect herpes simplex virus type 2 antibodies in a South African populationSexually Transmitted Infections
Sexually Transmitted Infections
Variations of HIV and STI prevalences within communities neighbouring new goldmines in Tanzania: importance for intervention design
Sexually Transmitted Infections, 79(4):
International Journal of Std & AIDS
The case against sexual transmission of HIV
International Journal of Std & AIDS, 14():
Plos OneSexual Risk Factors for HIV Infection in Early and Advanced HIV Epidemics in Sub-Saharan Africa: Systematic Overview of 68 Epidemiological StudiesPlos One
Journal of Child Psychology and PsychiatryPromoting child and adolescent mental health in the context of the HIV/AIDS pandemic with a focus on sub-Saharan AfricaJournal of Child Psychology and Psychiatry
Plos OneRelatively Low HIV Infection Rates in Rural Uganda, but with High Potential for a Rise: A Cohort Study in Kayunga District, UgandaPlos One
Journal of Health Care for the Poor and Underserved
Transient Populations: Linking HIV, Migrant Workers, and South African Male Inmates
Journal of Health Care for the Poor and Underserved, 20(2):
Ima Journal of Applied MathematicsQualitative dynamics of a vaccination model for HSV-2Ima Journal of Applied Mathematics
The socioeconomic determinants of HIV incidence: Evidence from a longitudinal, population-based study in rural South Africa
Journal of Clinical MicrobiologyPerformance of commercially available enzyme Immunoassays for detection of antibodies against herpes simplex virus type 2 in African populationsJournal of Clinical Microbiology
Tropical Medicine & International HealthA community-based study to examine the effect of a youth HIV prevention intervention on young people aged 15-24 in South Africa: results of the baseline surveyTropical Medicine & International Health
Revista De Saude Publica
HIV infection and AIDS in a small municipality in Southeast Brazil
Revista De Saude Publica, 39(6):
Sexually Transmitted InfectionsThe sexual health of pupils in years 4 to 6 of primary schools in rural TanzaniaSexually Transmitted Infections
International Journal of Std & AIDS
Epidemiology of HIV infection in urban Burkina Faso
International Journal of Std & AIDS, 15(6):
Bmc Infectious DiseasesPatterns of sexually transmitted infections in adolescents and youth in Dar es Salaam, TanzaniaBmc Infectious Diseases
Annals of EpidemiologyMale and female circumcision associated with prevalent HIV infection in virgins and adolescents in Kenya, Lesotho, and TanzaniaAnnals of Epidemiology
Archives of Medical ResearchHerpes simplex virus type 2 among Mexican high school adolescents: Prevalence and association with community characteristicsArchives of Medical Research
Environmental Impact Assessment ReviewAssessing health impacts in complex eco-epidemiological settings in the humid tropics: Advancing tools and methodsEnvironmental Impact Assessment Review
Bulletin of the World Health Organization
Genital herpes and human immunodeficiency virus: double trouble
Bulletin of the World Health Organization, 82(6):
Samj South African Medical Journal
The burden of disease attributable to sexually transmitted infections in South Africa in 2000
Samj South African Medical Journal, 97(8):
Plos OneHIV Prevalence and Associated Risk Factors among Individuals Aged 13-34 Years in Rural Western KenyaPlos One
Transmission of HIV-1 infection in sub-Saharan Africa and effect of elimination of unsafe injections
Scandinavian Journal of Infectious DiseasesThe burden of infection with herpes simplex virus type 1 and type 2: Seroprevalence study in EstoniaScandinavian Journal of Infectious Diseases
Sexually Transmitted InfectionsA critique of international indicators of sexual risk behaviourSexually Transmitted Infections
Quarterly Journal of Economics
Sexually transmitted infections, sexual behavior, and the HIV/AIDS epidemic
Quarterly Journal of Economics, 120(2):
International Journal of Std & AIDS
Association between the intact foreskin and inferior standards of male genital hygiene behaviour: a cross-sectional study
International Journal of Std & AIDS, 16(8):
Sexually Transmitted InfectionsMale circumcision and risk of syphilis, chancroid, and genital herpes: a systematic review and meta-analysisSexually Transmitted Infections
Acta Dermato-VenereologicaDemographic and behavioural factors in Tanzanian and Norwegian patients with sexually transmitted infectionsActa Dermato-Venereologica
International Journal of Std & AIDS
HIV infections in sub-Saharan Africa not explained by sexual or vertical transmission
International Journal of Std & AIDS, 13():
Journal of Infectious Diseases
Age-specific prevalence of infection with herpes simplex virus types 2 and 1: A global review
Journal of Infectious Diseases, 186():
AIDS Care-Psychological and Socio-Medical Aspects of AIDS/HivPotential for an intervention based on male circumcision in a South African town with high levels of HIV infectionAIDS Care-Psychological and Socio-Medical Aspects of AIDS/Hiv
International Journal of Std & AIDS
Review of evidence from risk factor analyses associating HIV infection in African adults with medical injections and multiple sexual partners
International Journal of Std & AIDS, 15(4):
Bmc Public HealthRisk behaviors of 15-21 year olds in Mexico lead to a high prevalence of sexually transmitted infections: results of a survey in disadvantaged urban areasBmc Public Health
Clinical Microbiology and Infection
Herpes simplex virus type 2 and heterosexual spread of human immunodeficiency virus infection in developing countries: hypotheses and research priorities
Clinical Microbiology and Infection, 9(3):
Clinical Infectious Diseases
Management of herpes simplex virus type 2 infection in HIV type 1-infected persons
Clinical Infectious Diseases, 43(3):
HIV incidence among post-partum women in Zimbabwe: risk factors and the effect of vitamin A supplementation
AIDS and BehaviorBeyond Monogamy: Opportunities to Further Reduce Risk for HIV Infection Among Married Zimbabwean Women with only One Lifetime PartnerAIDS and Behavior
Epidemiology and InfectionPrevalence of, and risk factors, for, HSV-2 antibodies in sexually transmitted disease patients, healthy pregnant females, blood donors and medical students in Tanzania and NorwayEpidemiology and Infection
Studies in Family PlanningYoung People's Sexual Partnerships in KwaZulu-Natal, South Africa: Patterns, Contextual Influences, and HIV RiskStudies in Family Planning
Annales De Dermatologie Et De Venereologie
Genital herpes: epidemiology, transmission, clinic, asymptomatic viral excretion, impact on other sexually transmitted diseases, prevention, and treatment
Annales De Dermatologie Et De Venereologie, 129(4):
Plos OneHSV-2 Infection as a Cause of Female/Male and Racial/Ethnic Disparities in HIV InfectionPlos One
Antiviral ResearchPoly (4-styrenesulfonic acid-co-maleic acid) is an entry inhibitor against both HIV-1 and HSV infections - Potential as a dual functional microbicideAntiviral Research
International Journal of Std & AIDSHerpes simplex virus type 2 infection as a biomarker for sexual debut among young people in sub-Saharan Africa: a literature reviewInternational Journal of Std & AIDS
American Journal of Reproductive ImmunologyIs Early Sexual Debut a Risk Factor for HIV Infection Among Women in Sub-Saharan Africa? A Systematic ReviewAmerican Journal of Reproductive Immunology
International Journal of Std & AIDSDeterminants of generalized herpes simplex virus-2 epidemics: the role of sexual partner concurrencyInternational Journal of Std & AIDS
Ajar-African Journal of AIDS ResearchPoverty, sexual behaviour, gender and HIV infection among young black men and women in Cape Town, South AfricaAjar-African Journal of AIDS Research
JAIDS Journal of Acquired Immune Deficiency SyndromesThe Effects of Herpes Simplex Virus-2 on HIV-1 Acquisition and Transmission: A Review of Two Overlapping EpidemicsJAIDS Journal of Acquired Immune Deficiency Syndromes
JAIDS Journal of Acquired Immune Deficiency SyndromesAssociation Between HIV and Subpreputial Penile Wetness in Uncircumcised Men in South AfricaJAIDS Journal of Acquired Immune Deficiency Syndromes
© 2001 Lippincott Williams & Wilkins, Inc.