According to various estimates, there are close to five and a half million HIV-infected individuals living in South Africa, more than in any other country in the world [1–3]. The exceptional severity of the epidemic in the countries of Southern Africa necessitates a detailed understanding of the epidemiology of HIV/AIDS in these countries. In South Africa, national surveys of HIV prevalence in pregnant women attending public antenatal clinics have been conducted annually since 1990, and published reports have presented HIV prevalence levels by age, by province and most recently by health district [3–9]. These surveys have shown a rise in HIV prevalence from 1% in 1990 to 29% in 2006 . There is substantial heterogeneity between provinces, with provincial HIV prevalence in the 2006 survey varying between 15 and 39% , and significant heterogeneity in HIV prevalence has also been found within provinces . However, there has to date been no published multivariate analysis of the relationship between HIV infection and the various demographic variables recorded in the surveys.
Factors that are often thought to increase women's risk of HIV include low socioeconomic position relative to men and having substantially older male partners [11–15]. However, studies conducted in Africa have found that the relationship between these factors and the risk of HIV is complex. Higher educational attainment, which is often used as a proxy for higher socioeconomic status, has generally been found to be associated with increased risk of HIV in the early stages of the HIV/AIDS epidemic, both in men and women . However, in more mature epidemics in which HIV/AIDS education programmes have been introduced, higher educational attainment appears to become protective against HIV [17–23]. Studies [24,25] have also suggested that the effect of having an older partner on a woman's risk of HIV infection may differ in relation to the woman's age, with young women tending to have their risk increased to a greater extent than older women.
This study aims to examine whether the relationship between HIV risk, educational attainment and partner age in South African women differs from that observed in other African studies. Two hypotheses are tested, using antenatal clinic survey data collected between 2000 and 2005. On the basis of observed age variation in the effect of educational attainment on HIV risk [18,19,26] and the effect of partner age difference on HIV risk [24,25], the first hypothesis tested is that the effects of these variables differ by age. The second hypothesis tested is that trends in HIV risk differ by educational attainment, as suggested by evidence from other African settings [16,17]. An ancillary objective of this study is to assess whether the observed interprovincial heterogeneity in HIV prevalence can be explained by differences in the demographic variables recorded in the antenatal surveys.
Sampling procedures and laboratory methods are described in detail in the survey protocol  and in the published survey reports [4–9]. Briefly, the survey was conducted during October of each year, by the South African Department of Health, amongst women attending public sector antenatal clinics for the first time in their current pregnancy. Clinics were sampled on a probability proportional to size (PPS) basis within each province, the measure of size being the average monthly number of antenatal visits to the clinic. The survey followed an unlinked, anonymous, cross-sectional design. The purpose of the survey was explained to all eligible women, and those who consented to participate in the survey provided demographic information that was recorded on a data collection form, which was linked to the HIV sample by a unique barcode. In addition to the blood sample that was routinely collected from all pregnant women for the purpose of syphilis screening at their first antenatal visit, women participating in the survey provided a second Vacutainer (Becton Dickinson and Company; Franklin Lakes, New Jersey, USA) of blood. Participants who wished to know their HIV status were referred for voluntary counselling and testing (VCT) within the clinic or at the nearest VCT site.
Blood samples were stored at 4°C before being transported to participating laboratories. In line with WHO recommendations for populations with a prevalence of more than 10% , a single enzyme-linked immunosorbent assay test (Abbott Axsym System for HIV-1/HIV-2, Abbott Park, Illinois, USA) was applied to each blood sample, and in the Western Cape province, where HIV prevalence is relatively low, confirmatory testing was also conducted. Testing for syphilis was conducted using a rapid plasma reagin (RPR) test. Quality assurance of HIV testing and RPR testing was conducted by the National Institute for Communicable Diseases and the Medical University of Southern Africa, respectively. Data were initially entered by participating laboratories and then reentered and checked by provincial coordinators.
Statistical analysis of the data was conducted using STATA 9.2 (StataCorp, College Station, Texas, USA), with survey commands that reflected the stratification by province, clustering by clinic and sample weights. The analysis was limited to the data collected from 2000 to 2005, as clinic identifiers could not be obtained prior to 2000, and clinic identifiers changed after 2005, following a substantial change in the clinics that were sampled. Three different statistical models were applied to the data. First, multivariate logistic regression analyses  were run separately for data collected in each year, not allowing for any interactions (Model 1). To test the hypothesis of age variation in the effect of educational attainment and partner age difference on HIV risk, the same multivariate regression was also applied separately to the 15–24 and 25–49 years age groups (Model 2). The second hypothesis, of differences in HIV prevalence trends by educational attainment, was tested by combining data from 2000 to 2005 (Model 3). As with Model 2, this multivariate analysis was conducted separately for the 15–24 and 25–49 years age groups. Tests for trend were conducted by including year as a continuous explanatory variable in the model, and allowing for interactions between year and educational attainment.
A total of 99 153 women were tested for HIV from 2000 to 2005, with between 16 000 and 17 000 tested in each year. Sample sizes and levels of HIV prevalence in each year are shown in the online table. Over the 2000–2005 period, HIV prevalence rose from 24.5% [95% confidence interval (CI) 23.4–25.6] to 30.2% (95% CI 29.1–31.2), although HIV prevalence in women aged 15–24 years remained relatively stable. HIV prevalence levels increased at all levels of educational attainment. However, in women aged 15–24 years, HIV prevalence increased only in those women with no secondary education (Fig. 1).
In the first multivariate analysis (Table 1), it was found that women who had incomplete secondary education had a higher risk of HIV infection than women who had only primary education, although this was only significant at the 5% level in 3 years (2000, 2003 and 2004). Women who had completed their secondary education, however, were at a significantly reduced risk of HIV infection when compared with women who had only primary education, in all years except 2000. Women whose partners were 5 or more years older had a significantly increased risk of HIV infection in all years. Race was the most significant factor affecting HIV risk, with HIV risk in African women being substantially higher than that in women of other race groups. The risk of HIV infection varied significantly between the provinces, being consistently highest in KwaZulu-Natal and lowest in Limpopo. In the four provinces that were consistently associated with the highest HIV risk during the 2000–2002 period (Free State, Gauteng, KwaZulu-Natal and Mpumalanga), there appeared to be reductions in HIV risk relative to the Western Cape (baseline) over the 2000–2005 period. HIV risk also varied significantly in relation to age, with HIV risk being consistently highest in the 25–29 years age group. Other factors that were found to be significantly associated with the risk of HIV were second pregnancy and syphilis infection.
When the multivariate analysis was performed separately for the 15–24 and 25–49 years age groups (Model 2), the effect of educational attainment and partner age was found to differ considerably in the two age groups (Table 2). Amongst women aged 15–24 years, incomplete secondary education did not significantly affect the risk of HIV infection, but completed secondary education was associated with a significantly reduced risk of HIV infection in all years except 2000. Amongst women aged 25–49 years, however, incomplete secondary education was associated with a significantly increased risk of HIV infection in all years except 2001 and 2002, and the risk of infection in women with completed secondary education did not differ significantly from that amongst women with only primary education, except in 2001. Amongst young women, having a partner 5 or more years older significantly increased the risk of HIV infection, but amongst women aged 25 and older, having an older partner tended to reduce the risk of HIV, with this reduction reaching statistical significance in 2004 and 2005 [OR 0.90 (95% CI 0.80–1.00) and OR 0.88 (95% CI 0.78–0.98), respectively]. Other variables had similar effects to those estimated in Model 1 (results not shown).
When the data from all years were combined to test for trends (Model 3), trends in HIV risk were found to differ significantly in relation to age and educational attainment (Table 3). In the 15–24 years age group, there was no significant change in HIV risk over time amongst women with incomplete or completed secondary education, but amongst women who had no secondary education the risk of HIV infection increased by 8% per annum (OR 1.08 per annum, 95% CI 1.04–1.12). In the 25–49 years age group, the risk of HIV infection increased significantly over time, and the extent of this increase was not significantly affected by women's educational attainment.
This analysis suggests that in recent years, higher educational attainment has become protective against HIV in young South African women, and there have been significant differences in trends in HIV risk amongst young women with different levels of education. This could be due to recent social marketing and school-based HIV/AIDS lifeskills programmes having more impact in educated women. Consistent with studies in Uganda [19,22] and Zambia , the protective effect of higher educational attainment appears to be limited largely to young women. The absence of a clear association between educational attainment and HIV risk at older ages, in our analysis, may be an indication that HIV prevention strategies have been more successful in young women than in older women. Alternatively, it may reflect the longer average duration of HIV infection in older women, most of whom would have been infected prior to the introduction of significant social marketing programmes.
Earlier data confirm the general lack of association between educational attainment and HIV risk in the early stages of the South African epidemic. Multivariate analysis of antenatal clinic data collected in 1998 and 1999 confirmed the patterns observed in 2000 (i.e. no protective effect of completed secondary education, either at young ages or at older ages), although these data were not included in the present analysis due to sample weights and clinic identifiers not being available. More recent South African studies [30,31] have found that higher educational attainment is associated with significantly reduced HIV incidence, suggesting that the relationship between educational attainment and HIV risk may have changed over time.
This analysis suggests that the effect of having an older partner also varies in relation to women's age. In young women with a partner 5 or more years older, the odds of HIV infection is 40 to 70% greater than that in young women with a partner less than 5 years older. However, in women aged 25 years and older, having an older partner does not increase HIV risk. This could be because in men aged 35 years and older, older age is associated with reduced HIV risk, and having an older male partner is therefore associated with reduced risk of HIV exposure.
Substantial interprovincial differences in HIV prevalence have been noted in previous reports, and this analysis demonstrates that these differences persist even after controlling for differences in demographic profiles between provinces. To some extent, these are due to differences in epidemic timing, as shown in the reductions in the odds of HIV in the four worst affected provinces, relative to the Western Cape, over the 2000–2005 period. Interprovincial differences in HIV prevalence could also be explained by differences in the prevalence of male circumcision  and differences in levels of urbanization , factors not controlled for in this analysis.
A key strength of this analysis is that it is based on what is probably the largest HIV prevalence data set in the world. The large sample size makes it possible to test for associations and interactions that would normally not be statistically significant with smaller samples. However, a major limitation of the study is that no information was captured in respect of women who refused to participate in the survey, except in the Western Cape. In the Western Cape, participation rates were close to 98% , suggesting that nonresponse bias is unlikely to distort the results substantially. An additional limitation is that the sample is drawn only from public health facilities, and hence there remains some uncertainty regarding the relationship between educational attainment and HIV risk in the general population, as highly educated women are more likely to attend private health facilities. Reductions in fertility due to HIV and differences in sexual behaviour between pregnant and nonpregnant women also limit the extent to which the findings can be generalized to the rest of the population.
The explanation for the growing gap between educated and less educated women, in terms of HIV risk, is not completely clear, but there are several possible policy implications. First, there is a need to reduce rates of school dropout and to strengthen existing school HIV/AIDS lifeskills programmes. Second, social marketing programmes may need to develop materials more appropriate for less educated individuals with low literacy, and it may be appropriate to introduce special campaigns in communities with low levels of education. Last, measures to improve the socioeconomic status of women may be appropriate in empowering women to reduce their exposure to HIV risk [34,35].
The South African Department of Health is thanked for providing the antenatal survey data.
L.M. was responsible for the survey design and organization. H.dP. and R.D. assisted in the processing and coding of the data. L.J. conducted the statistical analysis of the data and D.B. and R.D. assisted in the analysis. L.J. drafted the paper and all other authors participated in the writing of the paper.
There are no conflicts of interest.
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