JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Prevention
Who Gets Tested for HIV in a South African Urban Township? Implications for Test and Treat and Gender-Based Prevention Interventions
Venkatesh, Kartik K PhD*; Madiba, Precious MSW†; De Bruyn, Guy MBBCH, MPH†; Lurie, Mark N PhD*; Coates, Thomas J PhD‡; Gray, Glenda E MBBCH, FCPaeds (SA)†
From the *Department of Community Health, Alpert Medical School, Brown University, Providence, RI; Perinatal HIV Research Unit (PHRU), University of the Witwatersrand, Chris Hani Baragwanath Hospital, Johannesburg, South Africa; and University of California Los Angeles, Los Angeles, CA.
Received for publication August 28, 2010; accepted October 20, 2010.
This research was sponsored by the US National Institute of Mental Health as a cooperative agreement, through contracts U01MH066687 (Johns Hopkins University-David Celentano, PI); U01MH066688 (Medical University of South Carolina-Michael Sweat, PI); U01MH066701 (University of California, Los Angeles-Thomas J. Coates, PI); and U01MH066702 (University of California, San Francisco-Stephen F. Morin, PI). In addition, this work was supported as HPTN Protocol 043 through contracts U01AI068613 (HPTN Network Laboratory-Susan Eshleman, PI); U01AI068617 (SCHARP-Deborah Donnell, PI); and U01AI068619 (HIV Prevention Trials Network-Sten Vermund, PI) of the Division of AIDS of the US National Institute of Allergy and Infectious Diseases; and by the Office of AIDS Research of the US National Institutes of Health.
Views expressed are those of the authors and not necessarily those of sponsoring agencies.
The authors have no conflicts of interest to declare.
K.K.V. and G.E.G. designed the study and wrote the article. K.K.V. with assistance from G.D.B. and M.N.L. did the analyses. G.E.G. and P.M. oversaw data collection. T.J.C., and G.D.B. provided oversight on analysis and article writing.
The Appendix Tables 1 and 2 are listed in Appendix section.
Correspondence to: Glenda E. Gray, MBBCH, FCPaeds (SA), Perinatal HIV Research Unit (PHRU), Chris Hani Baragwanath Hospital, University of the Witwatersand, P.O. Box 114, Diepkloof, Johannesburg 1864.
Background: With increasing calls for linking HIV-infected individuals to treatment and care via expanded testing, we examined sociodemographic and behavioral characteristics associated with HIV testing among men and women in Soweto, South Africa.
Methods: We conducted a cross-sectional household survey involving 1539 men and 1877 women as part of the community-randomized prevention trial Project ACCEPT/HPTN043 between July 2007 to October 2007. Multivariable logistic regression models, stratified by sex, assessed factors associated with HIV testing and then repeated testing.
Results: Most women (64.8%) and 28.9% of men reported ever having been tested for HIV, among whom 57.9% reported repeated HIV testing. In multivariable analyses, youth and students had a lower odds of HIV testing. Men and women who had conversations about HIV/AIDS with increasing frequency and who had heard about antiretroviral therapy were more likely to report HIV testing, and repeated testing. Men who had ≥12 years of education and who were of high socioeconomic status, and women who were married, who were of low socioeconomic status, and who had children under their care had a higher odds of HIV testing. Women, older individuals, those with higher levels of education, married individuals, and those with children under their care had a higher odds of reporting repeated HIV testing. Uptake of HIV testing was not associated with condom use, having multiple sex partners, and HIV-related stigma.
Conclusions: Given the low uptake of HIV testing among men and youth, further targeted interventions could facilitate a test and treat strategy among urban South Africans.
There have been increasing calls to expand access to HIV testing and then promptly link those found to be HIV infected to care and treatment in settings with high HIV prevalence.1,2 HIV voluntary counseling and testing (VCT) can be an important strategy for primary prevention and an entry point to care, treatment, and support for those found to be HIV infected.3,4 Studies have demonstrated the efficacy of VCT in decreasing risky sexual behaviors in generally healthy populations.5-7 However, individuals who report repeated VCT uptake may be more likely to engage in high-risk sexual behaviors8 and may also have higher rates of HIV acquisition,9,10 and hence may represent a potential group for targeted prevention interventions.11 Most studies to date that have provided a clearer understanding of risk behaviors and sociodemographic characteristics associated with HIV testing have been conducted in the developed world among high-risk groups.9,11,12 As VCT becomes an integrated part of a comprehensive HIV prevention and care strategy in resource-limited settings, further regional data assessing individual-level characteristics associated with HIV testing from the general population are warranted.4,13,14
Examining access to HIV testing in South Africa is timely as the government recently launched a national effort to test 15 million individuals for HIV and to start an estimated 0.5 million new HIV-infected individuals on antiretroviral therapy (ART) by 2011.15 South Africa is home to the largest HIV epidemic in the world, with 5.7 million infected individuals, prevalence among adults aged 15-49 years of nearly 20%,16 and an estimated incidence in young women of 5.5 per 100 woman-years.17 HIV prevalence among South African youth is among the highest in the world, which is likely driven by a range of sexual behaviors, including low levels of condom use, multiple sex partners, and densely connected sexual networks in which few HIV individuals are aware of their infection.18-23 In light of increases in population testing and ART initiation in South Africa,24 the current study utilizing a large representative sample of the general population can inform programs aimed at expanded testing and linkage of HIV-infected individuals to care and treatment.
We conducted a household survey in Soweto, South Africa, to determine sociodemographic and behavioral characteristics associated with HIV testing among men and women as part of the baseline assessment for the community randomized trial Project ACCEPT/HPTN 043. We also examined differences between individuals who reported first-time HIV testing compared with those who reported repeated testing.
Setting and Participants
A baseline household survey was conducted in communities in Soweto between July 2007 to October 2007. Soweto, an urban African township in Gauteng Province, is located outside Johannesburg, with a population of approximately 1 million people living in an area of nearly 63 km2.25 Ten communities, each having a population size ranging from 15,000 to 20,000, were assessed. Further details about the study design, sampling procedures, including household enumeration and sampling procedures, and methods of this trial can be found elsewhere.26 Briefly, a multistage sampling strategy was used to enumerate all households in each community. Households were randomly ordered and selected in batches of a prespecified size, and all households within a batch were visited by interview teams until the target sample sizes were reached and all households in the batch were visited. One eligible household member, who met the residency criteria and was aged 18-32 years, was randomly selected to be interviewed in each household.
All assessments were performed via face-to-face interview, but no individual identifying information was collected, so participants remained anonymous. The study received ethical approval by the University of Witwatersrand.
Interviews took place in a private place in the participant's household. The interviews were conducted in the language of the participants' choice, including Sotho, Zulu, Tsonga, and English. Themes addressed in the baseline survey included issues such as alcohol and substance use; sexual risk behaviors; conversations about HIV/AIDS; HIV testing history and disclosure of HIV status; social norms on HIV testing; HIV/AIDS stigma; and knowledge and uptake of ART. Further information about instrument development and validation can be found elsewhere.27
The outcome variable of HIV testing was defined as “Have you ever been tested for HIV?” followed by the number of times a person has been tested and the reasons for testing. Responses were coded as never tested, nonvoluntary (including pregnancy), tested once, and repeated testing (ie, 2 or more occasions). HIV status was assessed by asking a respondent “What were the results of your last HIV test?” Answer choices included HIV negative, HIV positive, don't know, and refused to answer. If participants had not been tested, they were asked questions about barriers to testing.
The following socioeconomic variables were assessed: age, education, primary occupation, income, marital status, currently has a sex partner, source of medical care, and plans to migrate. Socioeconomic status was assessed as “high” if the participant owned a car, “medium” if did not own a car but did own at least 2 of the following items, namely drinking water in house, refrigerator, or cell phone, and “low” if otherwise.
The following behavioral variables were assessed: ever used alcohol, ever used drugs, ever had vaginal sex, and ever had anal sex. Sexual behavior over the past 6 months was assessed by inquiring about sexual frequency (regardless of the number of sex partners) and frequency of condom use. Condom use with spouse and other sex partners, number of sex partners, and forced sex were analyzed only among the subset of participants who reported being sexually active in the last 6 months. Participants were classified as “consistent” condom users if they reported using condoms for 100% of reported sex acts with all sex partners in the last month and otherwise were classified as “inconsistent”. Participants were also asked whether they had experienced physical abuse by a sex partner, had an unwanted sexual experience before the age of 12, and had experienced physical violence before the age of 12.
Participants were asked about talking about HIV/AIDS, social norms around HIV testing, and HIV-associated stigma, and further information about how these items were operationally defined and measured can be found elsewhere.28 Briefly, conversations about HIV/AIDS were assessed by asking participants if they had talked to anyone about HIV/AIDS in the last 6 months. Next, participants were asked to whom they had talked to in the last 6 months. Responses were coded into 3 ordinal factors: “never,” “some,” and “common” conservations about HIV/AIDS. Participants were also asked if they had heard of ART. Social norms around HIV testing were assessed with 6 questions, each with response choices on a Likert scale.28 After calculating an overall social norms index, scores were divided into 3 categories-“unfavorable,” “intermediate,” and “favorable” based on the underlying distribution. HIV-related stigma was assessed with a 19-item scale, each with responses on a 5-point Likert scale, specifically developed for measuring HIV stigma in developing countries.29 The overall stigma score was split into 3 categories: “low,” “intermediate,” and “high” based on the underlying distribution.
The primary outcome was first dichotomized as “HIV testing” and “no HIV testing” as never tested. To better elucidate sex-specific characteristics associated with HIV testing (effect modification), we present analyses stratified by participant sex (men vs. women). We then examined participants who reported “first-time HIV testing” relative to those who reported “repeated HIV testing.” Multivariable logistic regression models were used to calculate adjusted odds ratios of factors associated with HIV testing. To elucidate the impact of more distal sociodemographic factors on more proximate behavioral factors,30,31 we constructed 2 multivariable logistic models, in which we first examined sociodemographic factors associated with HIV testing and then examined behavioral factors after controlling for sociodemographic factors. A stepwise approach was used to identify independent risk factors in which variables whose association reached significance (P < 0.20) were first examined, and those variables independently associated with HIV testing (P < 0.10) were retained in the core model. Confounding was assessed based on either a change of >0.10 of the nonlog-transformed beta coefficient of independent risk factors, or a priori confounders indentified from the literature. Colinearity of included variables was examined. All data analyses were conducted using STATA (STATACORP, version 10.0, College Station, TX) software.
HIV Testing Among South African Men and Women
Among the 3416 enrolled participants, over half (54.9%) were women. A little under half (48.6%) of the participants reported ever having tested for HIV, with more women (64.8%) reporting past testing than men (28.9%) (P < 0.0001). Among those who had ever been tested, 57.9% reported repeated HIV testing, which was also more common among women than men (60.9% vs. 49.5%; P < 0.0001). Within the past 12 months, 16.8% of men and 43.8% of women reported having tested for HIV. Figure 1 presents the distribution of HIV testing by sex, number of times (first vs. repeated testing), and type (voluntary vs. nonvoluntary testing). For men and women who reported never having undergone HIV testing (51.4%), the main reasons included: not thinking they were at risk (37.0%), being nervous about getting test results (17.0%), and not thinking of getting tested (14.2%).
Sociodemographic Characteristics Associated With Having Tested for HIV by Sex
Tables 1 and 2 present univariate and multivariable analyses for sociodemographic factors associated with having tested for HIV for men and women, respectively. In multivariable analyses, men who were older (>23 years), who had ≥12 years of education, and who were of moderate and high socioeconomic status had a higher odds of having tested for HIV. Men who were students, who were unemployed, who received care from the traditional medical sector, and who did not have a sex partner had a lower odds of having tested for HIV. Women who were older (>23 years), who were married, and who had ≥1 child under their care had a higher odds of having tested for HIV. Women who were students, who were of high socioeconomic status, and who did not have a sex partner had a lower odds of having tested for HIV.
Behavioral Characteristics Associated With Having Tested for HIV by Sex
Tables 3 and 4 present univariate and multivariable analyses of behavioral factors associated with having tested for HIV for men and women, respectively. Men who ever had vaginal sex, ever had anal sex, and who had sex in the last 6 months had a higher odds of having tested for HIV. Women who ever had vaginal sex, who had ≥ 1 lifetime sex partners, and who had sex in the last 6 months had a higher odds of having tested for HIV. Both men and women who had ever talked about HIV/AIDS, who had conversations about HIV/AIDS with increasing frequency, and who had heard of ART had a higher odds of having tested for HIV. Men and women who had experienced physical violence before the age of 12 had a higher odds of having tested for HIV, and also women who had ever been physically abused by a sex partner. Condom use, number of sex partners in the last 6 months, HIV-related stigma, and substance use were not significantly associated with having tested for HIV for both men and women.
Multivariable Analysis of Characteristics Associated With First and Repeated HIV Testing
Tables 5 and 6 present multivariable analyses of sociodemographic and behavioral factors, respectively, associated with first-time and repeated HIV testing compared with those who reported no HIV testing. In general, these associations were stronger for those who reported repeated HIV testing compared with those who reported first-time HIV testing. Women, those who were older, and those who had children under their care had a higher odds of reporting both first-time and repeat HIV testing. Students and those who did not currently have a sex partner had a lower odds of first-time and repeat HIV testing. Those who had undergone repeat HIV testing were more likely to have higher levels of education (≥8 years) and be married. Both first-time and repeat HIV testing were associated with neither income nor socioeconomic status.
In regard to sexual behavior, those who had undergone both first-time and repeat HIV testing had a higher odds of ever having had vaginal sex, having ≥1 lifetime sex partners, and having a sex partner in the last 6 months compared with those who reported no HIV testing. Both first-time and repeat acceptors of HIV testing were more likely to have ever talked about HIV/AIDS, to have had conversations about HIV/AIDS with increasing frequency, and to have heard of ART. Both first-time and repeat acceptors were more likely to report having been ever physically abused by a sex partner, and repeat acceptors were also more likely to report having experienced physical violence before the age of 12. Both first-time and repeat HIV testing were associated with neither substance use nor condom use.
To elucidate differences by gender in uptake of repeated HIV testing, we also conducted analyses stratified by participant sex (men vs. women) (Appendix Tables 1 and 2). In multivariable analyses, though correlates of repeated HIV testing were broadly similar across gender, we noted differences for the following sociodemographic variables, namely education, occupation, socioeconomic status, having children under care; and the following behavioral variables, alcohol use, having had vaginal and anal sex, lifetime number of sex partners, and physical abuse.
HIV Testing and Disclosure History
Among those who had been tested, most (>80%) reported receiving information about the meaning of a positive or negative HIV test result before they underwent HIV testing and over 90% reported getting their last HIV test result. A high proportion (>85%) reported ever disclosing their HIV test results. On their last HIV test, 6.3% of participants reported a positive HIV test result. Men were more likely to report decreased risk behaviors after HIV testing compared with women, including using condoms more often (40.0% vs. 29.3%; P < 0.0001) and reducing number of sex partners (44.1% vs. 24.9%; P < 0.0001).
The current study conducted among a representative sample of urban South African men and women identified several sociodemographic and behavioral characteristics associated with HIV testing that could assist in the development of future test and treat strategies. It is of great concern that about half of the participants (51%) remained unaware of their HIV status in a hyperendemic setting following expanded public-sector access to HIV care and ART through both the South African government and US President's Emergency Plan for AIDS Relief.32 Among those who had not been tested, over a third reported not thinking they were at risk for HIV. HIV testing in the urban population of Soweto was not higher than recent national South African survey data in which about half of the respondents reported past HIV testing.16 Younger individuals and students, who are at particularly high risk of HIV acquisition, were less likely to report having tested for HIV.16 HIV infections among youth aged 15-24 years represent more than 40% of all infections globally, and 63% reside in sub-Saharan Africa.33 Further studies in Africa are needed to examine acceptable youth-specific HIV prevention programs, including school-based interventions and routine testing of youth attending healthcare facilities,34,35 and testing in nonclinical settings.36
Men and women who had talked about HIV with increasing frequency were more likely to report having tested for HIV, which also held for repeated HIV testing. An earlier analysis from all regional sites of the current study found that the only variable that was significantly and consistently associated with past HIV testing was frequent conversations about HIV.28 Increased communication about HIV may lead to greater acceptance and uptake of testing; in addition, those who are tested for HIV may be more likely to speak openly about HIV.14 Further studies are needed to elucidate with whom these conversations occur, the context of these conversations and the impact on HIV testing. Men and women who had heard of ART were also more likely to report having tested for HIV and repeated HIV testing. This is an interesting finding as the current study was conducted in 2007, which was after the roll out of the government ART program. HIV testing has since accelerated with the increasing availability of ART.37 Although there has been great concern about stigma's role in impeding testing in South Africa,38-40 HIV stigma was not associated with having tested for HIV. It is possible that national prevention campaigns, such as loveLife (www.lofeLife.com) for South African youth, may be linked to wider awareness about HIV and consequent HIV testing.14
Men who were older, employed, and of higher educational and socioeconomic status were more likely to report having tested for HIV, which is consistent with earlier data from Zimbabwe and South Africa.14,41 Given what is known about risk behavior among young people, it is of concern that young and unmarried men were less likely to get tested.40,42,43Community-based HIV prevention programs in South Africa have been developed to involve men, such as Sonke Gender Justice Network (www.genderjustice.org.za) and Engender Health (www.engenderhealth.org). Further interventions are needed to target young men who may be left out of current public VCT programs, including routine opt-in or opt-out testing of all individuals and the expansion of community-based barrier-free VCT.40,44-46
In sub-Saharan Africa, it has been estimated that nearly 80% of HIV-infected adults are unaware of their status.47 This study documents a relatively high level of HIV testing (ie, close to 50%), which is similar to recent data from Botswana but much higher than rural Zimbabwe.40,41 Also, among those who had been tested, most (>90%) reported receiving their test result, which is higher than some earlier data from South Africa.14,38 However, these data suggest that there is still a great need for scaling-up HIV testing in this hyperendemic urban setting. Women were much more likely to report both first-time and repeat HIV testing compared with men, which is different from Ugandan data,48 but in accordance with recent South African surveys.16 Prevalence studies from South Africa suggest that younger women are 4 times more likely to be infected with HIV in comparison to men of the same age.22,23 In the current study, women who were married, who had an increasing number of children under their care, and who were of lower socioeconomic status had a higher likelihood of HIV testing, which is consistent with previous data.43 Pregnancy among young South African women is high with close to a third of 15-19 years olds and nearly two-thirds of 20-24 year olds reporting a past pregnancy.23 For many women in this population, HIV testing was likely offered at the time of pregnancy through routine antenatal testing.
Despite high levels of reported sexual risk behavior in this study population,27 after controlling for sociodemographic characteristics, our results do not indicate that condom use and number of sex partners are associated with HIV testing. Additionally, these data do not suggest that those who reported repeated HIV testing were more likely to report safer sex. For men and repeat testers, the current study suggests that those who were most risk-averse with the least number of sex partners in the last 6 months were taking up HIV testing, which is in accordance with some African studies.41,49 Other data from this region have suggested that individuals who accept repeat VCT may be more likely to engage in high-risk sexual behaviors, despite the potential prevention benefits associated with repeat VCT.8,11,13,50 Unless the respondent receives a positive test result, VCT may not impact subsequent risk taking.12 The current baseline analysis included participants who had already undergone HIV testing as an individual-level behavioral intervention, which may not be adequate to address prevalent high-risk behaviors in the community.4 The prevalence of sexual risk behaviors, measured as inconsistent condom use and multiple sex partners, was higher in this urban population than South African national survey data.16 In light of the high frequency of sexual risk behaviors, particularly among men, and the lack of an association between HIV testing and sexual risk behaviors, these findings suggest that there is a need for more effective risk reduction counseling as part of HIV testing.
A limitation of this study is we were not able to investigate particular reasons for HIV testing (ie, separating out whether nonvoluntary testing was due to pregnancy versus requested by a health care provider for other diagnostic purposes). Due to the cross-sectional design of the current study, causal or temporal inferences cannot be drawn from the associations. The lack of an association between HIV testing and current sexual risk behaviors may be due to the cross-sectional assessment. Questions regarding substance use and sexual behavior have the potential for misreporting due to recall and social desirability bias, especially in face-to-face interviews. However, surveys were confidential, and no identifiable personal information was collected. This baseline dataset did not involve actual HIV testing, but rather used retrospective self-report. A strength of the current study was a large representative population-based sample with high survey completion rates and very little missing data,27 which allowed for greater generalizability and representativeness of these findings. Earlier studies have often relied on clinic-based populations where HIV testers may represent a self-selecting group. The large sample size allowed for assessing relatively rare exposures.
The current study highlights individual-level characteristics that influence the utilization of HIV testing and found that a number of population subgroups could be targeted for VCT uptake, particularly youth, students, and men. To date patterns and predictors of HIV testing use have not been fully characterized in resource-limited settings.4 As VCT continues to be rapidly scaled-up in South Africa, repeat testers will represent a larger proportion of individuals undergoing VCT, and further research will be needed to examine whether sexual risk behaviors change among repeat testers. Given the continued high prevalence of HIV and plans to expand VCT in South Africa, the current study is timely in emphasizing the need for further targeted efforts to expand HIV testing.
We thank the communities that partnered with us in conducting this research and all study participants for their contributions. We also thank study staff and volunteers at all participating institutions for their work and dedication.
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