Secondary Logo

Journal Logo

Original Study

Relationship Between Community-Level Alcohol Outlet Accessibility and Individual-Level Herpes Simplex Virus Type 2 Infection Among Young Women in South Africa

Rosenberg, Molly PhD*†‡; Pettifor, Audrey PhD†‡§; Lippman, Sheri A. PhD§¶; Thirumurthy, Harsha PhD‡∥; Emch, Michael PhD†‡**; Miller, William C. MD, PhD†††; Selin, Amanda MHS; Gómez-Olivé, Francesc Xavier MD, PhD§‡‡; Hughes, James P. PhD§§; Laeyendecker, Oliver PhD¶¶∥∥; Tollman, Stephen MMed, PhD§‡‡***; Kahn, Kathleen MBBCh, PhD§‡‡***

Author Information
Sexually Transmitted Diseases: May 2015 - Volume 42 - Issue 5 - p 259-265
doi: 10.1097/OLQ.0000000000000263
  • Free

Exposure to alcohol outlets (places where alcohol is sold and consumed, such as taverns, bars, and bottle shops) may influence sexual risk. At the individual level, easy access to alcohol outlets is associated with increased alcohol consumption,1–3 which increases sexual risk behaviors, such as unprotected sex,4–6 and results in poor sexual health, including HIV infection.7–9 Similarly, characteristics of alcohol outlets (e.g., music, dim lights, and unisex bathrooms)10 and the network of potential sex partners who typically frequent them11,12 may provide environments with heightened potential for risky sexual activity. At the community level, the presence of alcohol outlets may influence or reflect community norms around acceptable behaviors, yielding heightened risk for all community members, whether they patronize the establishments or not.

Community-level alcohol outlet accessibility is typically quantified with a community density measure, but can include other measures such as hours/days of alcohol sale and price. Alcohol outlet accessibility is associated with increased measures of population-level13–15 and individual-level16 sexually transmitted infections (STIs). However, the relationship between alcohol outlet accessibility and sexual risk has been underexplored in areas outside the United States and entirely unexplored in adolescent-specific populations that are at heightened risk for STI. Because adolescents may have different alcohol outlet utilization patterns and alcohol-using behaviors than adults, generalization from adult population studies to adolescents could be problematic.

South African law prohibits the sale of alcohol to minors younger than 18 years.17,18 However, this regulation is not widely enforced: approximately half of South African teens report having consumed alcohol in their lifetime, and the age of alcohol initiation is often substantially lower than 18 years, with many youth initiating alcohol consumption even before age 13 years.19–21 In practice, South African minors are also often afforded access to outlets that sell alcohol; more than 40% of young women living in rural Mpumalanga report recently visiting taverns.22 Furthermore, alcohol use and misuse are temporally connected to risky sex in this population: up to a quarter of South African teens who are sexually active report having used alcohol before sex.19,21,23

Young women in South Africa are at exceptionally high risk for STIs; nearly a third are HIV positive by the time they reach age 21 years, and up to 70% are infected with herpes simplex virus type 2 (HSV-2) in their lifetime.24,25 Thus, the need to identify potential interventions for STI reduction in this population is critical. Alcohol outlet accessibility is attractive as a potential intervention target because it is relatively modifiable through strengthening or more strictly enforcing existing government regulations.26–28 In this study, we aim to explore the association between alcohol outlet accessibility and sexual risk among adolescents in the developing world, using a population-based sample of young women in rural South Africa. We also explored the potential effect of neighborhood-level alcohol interventions using a marginal modeling approach.



To explore the relationship between alcohol outlet accessibility and sexual risk, we analyzed baseline data collected in the HPTN 068 HIV prevention trial.29 HPTN 068 is a phase III randomized controlled trial in rural Mpumalanga province, South Africa, within the Agincourt Health and Demographic Surveillance System site.30 The aim of the study is to assess whether cash transfers conditional on school attendance can prevent HIV. School-attending young women aged 13 to 21 years were enrolled in the study between March 2011 and December 2012 (n = 2533). Biological HIV and HSV-2 data were collected during routine baseline procedures completed by each young woman enrolled in the study. Data on alcohol outlets were collected as part of a community mapping exercise administered in 2010. A group of key informants from each village (average 11 key informants per village; n = 24 villages) completed a questionnaire to enumerate, by consensus, a broad number of village assets, including schools, businesses, social organizations, and government services. Taverns and bottle shops were enumerated separately. Taverns generally sell alcohol for on-premises consumption, and bottle shops generally sell alcohol for off-premises consumption; however, these are not rigid definitions. In practice, alcohol consumption can occur outside bottle shops, and conversely, taverns can sell alcohol to take home.

Ethical approval for the parent studies (HPTN 068 and community mapping study) was provided by the Office of Human Research Ethics at the University of North Carolina at Chapel Hill, the University of the Witwatersrand's Committee for Research on Human Subjects, and the Mpumalanga Province Research and Ethics Committee. The community mapping study received additional ethical approval from the Committee for Human Research at the University of California, San Francisco. Ethical approval for this secondary analysis was provided by the Office of Human Research Ethics at the University of North Carolina at Chapel Hill (No. 13-2013).

Key Measures

Alcohol outlet accessibility was quantified as the number of alcohol outlets per village, defined as the combined number of taverns and bottle shops within each village. For analysis, we considered the alcohol outlet measure in 2 ways: (1) categorically, with categories none (zero outlets), low (1–4 outlets), and high (>4 outlets), and (2) numerically, using the absolute number of alcohol outlets per village. The categorical cutpoints were chosen with a 2-stage process: (1) enumerating plausible categorizations based on visual inspection of of the histogram of number of alcohol outlets per village, then (2) choosing the categorization that minimized the quasilikelihood under the independence model criterion model fit statistic.

We used an absolute number instead of alcohol outlets per area measure because village area exhibited minimal variation (interquartile range, 1.3–3.2 km2). Furthermore, we theorize that in small areas like the villages in the study region, absolute number is more important than density because all outlets were within reasonable walking distance to all inhabitants. We used a community-level as opposed to individual-level exposure because we were interested in capturing contextual and individual effects.

From a directed acyclic graph, we identified a minimally sufficient adjustment set of 3 potential village-level confounding variables. Each variable was derived from the Agincourt Health and Demographic Surveillance System census dataset. Total population was defined by the 2011 estimated population size of each village. Proportion male was defined as the number of male residents divided by the total population of each village in 2011. Proportion employed was defined by the proportion of village residents reporting employment in the most recent labor survey in 2008. Final coding decisions were informed by comparing quasi-likelihood under the independence model criterion fit statistics for a variety of categorizations and transformations to best reflect each covariate's association with HSV-2 prevalence. Individual-level covariates predictive of the outcome (age, household socioeconomic status [SES], relationship of young woman to her primary caregiver) were also included in the adjusted model to improve their precision and predictive ability.

The outcome was individual-level prevalent HSV-2 infection at the time of enrollment in the study. Baseline testing for HSV-2 was performed at Johns Hopkins University using Kalon HSV-2 gG2 ELISA (Kalon Biological, Ltd, Surrey, United Kingdom) according to the manufacturer's protocol using standard laboratory practices.31 HIV status was not considered as an outcome because of the small number of prevalent infections at baseline and the likelihood that at least some of the cases were a result of perinatal, as opposed to sexual, transmission.

Statistical Modeling

To estimate the association between number of alcohol outlets per village and HSV-2 infection, we used generalized estimating equation (GEE) log binomial and logistic models with exchangeable working correlation matrices. The GEE models corrected the standard errors of our estimates for the clustered nature of the data. First, GEE log binomial models were used to estimate the unadjusted prevalence of HSV-2 among participants in villages with different alcohol outlet exposure categories. In all subsequent analyses, we treated the alcohol outlet number exposure numerically, as indicated by visual inspection of the categorical results. The GEE logistic regression models were used to calculate the relative difference in odds of HSV-2 infection with each 1-unit increase in number of alcohol outlets per village of residence.

Next, we used a causal inference approach to predict the population-level HSV-2 prevalence in the study population, across a range of alcohol outlet exposure levels.32 First, we imputed the probability of HSV-2 infection for each participant given their particular set of covariates, across the range of alcohol outlet exposures observed in the data (0–7 alcohol outlets per village of residence). These predicted probabilities were calculated based on the parameters estimated in the fully adjusted GEE logistic regression model. We then averaged these imputed probabilities for all participants in the study sample at each level of alcohol outlet exposure. These values estimate the HSV-2 prevalence in the study population had the alcohol outlet exposure been set to each level (from 0 to 7 outlets) for the entire population. We used a bootstrapping technique to estimate 95% confidence intervals (CIs) around each predicted prevalence. All analyses were performed in SAS statistical software, v9.1.2 (Cary, NC).


Overall, 2533 young women were enrolled in HPTN 068 and 2174 (86%) lived in 1 of the 24 villages mapped in the community survey. The overall prevalence of HSV-2 infection among young women in the sample was 5% (n = 108). The young women ranged in age from 13 to 21 years with a median age of 15 years (Table 1). Households in which the young women resided had an average of 164 Rand (US $15) in food and nonfood expenditures per capita each month. Neither age nor SES varied significantly by number of alcohol outlets per village of residence. Approximately three-fourths of the young women reported a mother or father as their primary caregiver (74%), although young women who lived in villages with high numbers of alcohol outlets (5–7) tended to be more likely to have a parent caregiver (85%).

Demographic Characteristics of Cross-Sectional Sample of 2174 Rural South African Young Women Across 24 Villages, by Number of Alcohol Outlets in Village of Residence

The population of the 24 villages ranged in size from 171 to 9836; median population size was 3544. The proportion of males per village ranged from 37% to 50%, and the proportion of employed residents per village ranged from 12% to 21% of the total population. The number of alcohol outlets per village ranged from 0 to 7. A total of 4 villages had no alcohol outlets, 16 villages had 1 to 4 outlets, and 4 villages had more than 4 outlets. Number of alcohol outlets was positively correlated with population size (r = 0.88), proportion male (r = 0.42), and proportion employed (r = 0.29).

Young women who lived in villages with more alcohol outlets were more likely to have prevalent HSV-2 infections (Table 2). The estimated prevalence of HSV-2 increased from young women living in villages with no alcohol outlets (prevalence, 1.4% [95% CI, 0.2–12.1]), to those living in villages with low numbers of alcohol outlets (prevalence, 4.5% [3.7–5.5]), and to those living in villages with high numbers of alcohol outlets (prevalence, 6.3% [5.6–7.1]). The prevalence estimate for the zero exposure level was imprecise, likely due to the small sample size and single HSV-2 infection in this category.

Treating the alcohol outlet exposure numerically, for every 1-unit increase in number of alcohol outlets per village, the odds of prevalent HSV-2 infection increased 8% (odds ratio [OR; 95% CI], 1.08 (1.01–1.15]). The point estimate changed minimally after adjustment for village- and individual-level covariates (OR [95% CI], 1.11 (0.98–1.25]); however, this adjusted estimate was less precise. Visually, the numerical model provided a reasonable representation of the pattern suggested by the categorical model (Fig. 1).

Association Between Number of Alcohol Outlets in Village of Residence and Prevalent HSV-2 Infection Among 2174 South African Young Women
Graphical representations of the association between number of alcohol outlets in home village and prevalent HSV-2 infection among 2174 South African young women. Solid line indicates ln (odds of prevalent HSV-2 infection) across varying number of alcohol outlets per village. Dashed line indicates 95% CIs around the ln(odds) estimates. (A) Number of alcohol outlets treated categorically at 0, 1 to 4, and 5 to 7 outlets per village in an unadjusted GEE model with a logit link. Note: No village had exactly 5 outlets. (B) Number of alcohol outlets treated numerically in an unadjusted GEE model with a logit link.

Using estimates from the adjusted GEE logistic regression model above, we calculated the predicted population-level HSV-2 prevalence across the observed range of alcohol outlet exposures (0–7 alcohol outlets; Fig. 2). For example, if the entire study population lived in villages with 7 alcohol outlets, the expected HSV-2 prevalence would be 6.4% (95% CI, 2.7–10.0). If the entire study population lived in villages with zero alcohol outlets, the expected HSV-2 prevalence would be 3.8% (95% CI, 0.0–7.5). However, the absolute differences should be interpreted with caution because the predicted probabilities are imprecisely measured with wide CIs and the causal relationship between alcohol outlets and HSV-2 is unconfirmed.

Predicted HSV-2 prevalence corresponding to a range of counterfactual neighborhood alcohol outlet exposure levels (0–7 alcohol outlets per village of residence). Solid line indicates the predicted probability of prevalent HSV-2 infection across varying numbers of alcohol outlets per village. Dashed line indicates 95% CIs around the predicted probability estimates.


Overall, we found that living in villages with higher numbers of alcohol outlets was associated with increased HSV-2 prevalence among young women in rural South Africa. This finding is consistent with previous studies linking alcohol outlet density to prevalent STI among adults13–16 and to risk factors for STI, like binge drinking and intimate partner violence.33,34 Furthermore, the use of individual-level HSV-2 biological data strengthens inference over prior ecological studies13–15 and studies with self-reported STI outcomes.16 We also estimated the predicted population-level HSV-2 prevalence across a range of alcohol outlet exposure levels, exploring the potential benefits of interventions to limit exposure to alcohol outlets. To our knowledge, this approach has not previously been used with regard to alcohol outlets and sexual risk.

To interpret the findings causally, we must assume that the exposure (alcohol outlets) occurs before the outcome (HSV-2 infection). However, because of the cross-sectional nature of this analysis, certainty about the temporality of the relationship between alcohol outlets and HSV-2 infection is not possible. Based on key informant reports, we believe that the absolute number of outlets likely remained constant over recent history. Conversely, although we used a prevalence measure, because this was a young cohort, those with HSV-2 infection were likely to have acquired the infection recently. Under these assumptions, the alcohol outlet exposure likely predates the HSV-2 outcome, although the findings should be interpreted with caution.

The observational nature of the data also limited our ability to assess a causal relationship between alcohol outlets and sexual risk. Self-selection of where one lives could theoretically be influenced by alcohol outlet accessibility. However, adolescents are presumably less likely to make decisions about where the family lives because they live with parents or other adult caregivers who are more likely to make that decision. Also, other unmeasured village characteristics, such as social disorganization or normative constraints against sexual activity, may vary with alcohol outlet accessibility and influence sexual risk.35 Although the association between alcohol outlets and HSV-2 remained after adjusting for measured individual- and village-level covariates, the possibility remains that confounding by other unmeasured characteristics influenced the results.

This study found that young women who live in communities with more accessible alcohol environments have higher HSV-2 prevalence than do those who do not. These findings point to potential opportunities for intervention to improve sexual health among young women. Policies limiting the number of venues distributing alcohol show promise in reducing alcohol consumption in both low- and middle-income settings, which may also result in improved sexual health.1,36 South Africa has recently enacted some alcohol policies aimed to reduce harmful alcohol consumption (e.g., reducing hours of sale and establishing a minimum legal age for consumption), although the extent of their enforcement and the extent to which they have reduced consumption is uncertain.18 At minimum, our results suggest that high-risk young women may be found in higher proportions within alcohol-accessible communities and that sexual health interventions may be appropriately targeted at communities based on their alcohol environment characteristics. Future research should focus on establishing the temporal relationship between alcohol outlet exposure and sexual risk and on identifying the pathways through which the association exists. A better understanding of how alcohol outlets are associated with sexual risk could inform recommendations about whether reducing access to outlets could reduce sexual risk, or whether the number of outlets is more likely a reflection of community norms.


1. Campbell CA, Hahn RA, Elder R, et al. The effectiveness of limiting alcohol outlet density as a means of reducing excessive alcohol consumption and alcohol-related harms. Am J Prev Med 2009; 37: 556–569.
2. Popova S, Giesbrecht N, Bekmuradov D, et al. Hours and days of sale and density of alcohol outlets: impacts on alcohol consumption and damage: A systematic review. Alcohol Alcohol 2009; 44: 500–516.
3. Bryden A, Roberts B, McKee M, et al. A systematic review of the influence on alcohol use of community level availability and marketing of alcohol. Health Place 2012; 18: 349–357.
4. Rehm J, Shield KD, Joharchi N, et al. Alcohol consumption and the intention to engage in unprotected sex: Systematic review and meta-analysis of experimental studies. Addiction 2012; 107: 51–59.
5. Kalichman SC, Simbayi LC, Kaufman M, et al. Alcohol use and sexual risks for HIV/AIDS in sub-Saharan Africa: Systematic review of empirical findings. Prev Sci 2007; 8: 141–151.
6. Sales JM, Brown JL, Vissman AT, et al. The association between alcohol use and sexual risk behaviors among African American women across three developmental periods: A review. Curr Drug Abuse Rev 2012; 5: 117–128.
7. Fisher JC, Bang H, Kapiga SH. The association between HIV infection and alcohol use: A systematic review and meta-analysis of African studies. Sex Transm Dis 2007; 34: 856–863.
8. Pithey A, Parry C. Descriptive systematic review of sub-Saharan African studies on the association between alcohol use and HIV infection. SAHARA J 2009; 6: 155–169.
9. Cook RL, Clark DB. Is there an association between alcohol consumption and sexually transmitted diseases? A systematic review. Sex Transm Dis 2005; 32: 156–164.
10. Morojele NK, Kachieng'a MA, Mokoko E, et al. Alcohol use and sexual behaviour among risky drinkers and bar and Shebeen patrons in Gauteng province, South Africa. Soc Sci Med 2006; 62: 217–227.
11. Mataure P, McFarland W, Fritz K, et al. Alcohol use and high-risk sexual behavior among adolescents and young adults in Harare, Zimbabwe. AIDS Behav 2002; 6: 211–219.
12. Watt MH, Aunon FM, Skinner D, et al. “Because he has bought for her, he wants to sleep with her”: Alcohol as a currency for sexual exchange in South African drinking venues. Soc Sci Med 2012; 74: 1005–1012.
13. Cohen DA, Ghosh-Dastidar B, Scribner R, et al. Alcohol outlets, gonorrhea, and the Los Angeles civil unrest: A longitudinal analysis. Soc Sci Med 2006; 62: 3062–3071.
14. Scribner RA, Cohen DA, Farley TA. A geographic relation between alcohol availability and gonorrhea rates. Sex Transm Dis 1998; 25: 544–548.
15. Nichols BE, Nkalamo D, Whitcomb BW. Density of drinking establishments and HIV prevalence in a migrant town in Namibia. AIDS Behav 2012; 16: 829–834.
16. Theall KP, Scribner R, Cohen D, et al. The neighborhood alcohol environment and alcohol-related morbidity. Alcohol Alcohol 2009; 44: 491–499.
17. Parliament of the Republic of South Africa. Liquor Act. Chapter 2, Section 10: Prohibition of supply of liquor or methylated spirits to minor. 2003.
18. Parry CD. Alcohol policy in South Africa: A review of policy development processes between 1994 and 2009. Addiction 2010; 105: 1340–1345.
19. Morojele N, Myers B, Townsend L, et al. Survey on Substance Use, Risk Behaviour and Mental Health among Grade 8–10 Learners in Western Cape Provincial Schools, 2011. Cape Town: South African Medical Research Council, 2013.
20. Moodley S, Matjila MJ, Moosa M. Epidemiology of substance use among secondary school learners in Atteridgeville, Gauteng. S Afr J Psychiatry 2012; 18: 2–7.
21. Reddy SP, James S, Sewpaul R, et al. Umthente Uhlaba Usamila—The South African Youth Risk Behaviour Survey 2008. South African Medical Research Council: Cape Town, 2010.
22. Rosenberg M, Pettifor A, Van Rie A, et al. The relationship between alcohol outlets, HIV risk behavior, and HSV-2 infection among South African young women: A cross-sectional study. PLOS One In press.
23. Saggurti N, Jain AK, Sebastian MP, et al. Indicators of mobility, socio-economic vulnerabilities and HIV risk behaviours among mobile female sex workers in India. AIDS Behav 2012; 16: 952–959.
24. Pettifor AE, Rees HV, Kleinschmidt I, et al. Young people's sexual health in South Africa: HIV prevalence and sexual behaviors from a nationally representative household survey. AIDS 2005; 19: 1525–1534.
25. Looker KJ, Garnett GP, Schmid GP. An estimate of the global prevalence and incidence of herpes simplex virus type 2 infection. Bull World Health Organ 2008; 86: 805–812 A.
26. Cook PJ, Moore MJ. The economics of alcohol abuse and alcohol-control policies. Health Aff (Millwood) 2002; 21: 120–133.
27. Babor TF, Aguirre-Molina M, Marlatt GA, et al. Managing alcohol problems and risky drinking. Am J Health Promot 1999; 14: 98–103.
28. Room R, Babor T, Rehm J. Alcohol and public health. Lancet 2005; 365: 519–530.
29. HIV Prevention Trials Network. Available at: Accessed January 27, 2015.
30. Kahn K, Tollman SM, Collinson MA, et al. Research into health, population and social transitions in rural South Africa: Data and methods of the Agincourt Health and Demographic Surveillance System. Scand J Public Health Suppl 2007; 69: 8–20.
31. Delany-Moretlwe S, Jentsch U, Weiss H, et al. Comparison of focus HerpesSelect and Kalon HSV-2 gG2 ELISA serological assays to detect herpes simplex virus type 2 antibodies in a South African population. Sex Transm Infect 2010; 86: 46–50.
32. Ahern J, Hubbard A, Galea S. Estimating the effects of potential public health interventions on population disease burden: A step-by-step illustration of causal inference methods. Am J Epidemiol 2009; 169: 1140–1147.
33. McKinney CM, Caetano R, Harris TR, et al. Alcohol availability and intimate partner violence among US couples. Alcohol Clin Exp Res 2009; 33: 169–176.
34. Weitzman ER, Folkman A, Kerry Lemieux Folkman M, et al. The relationship of alcohol outlet density to heavy and frequent drinking and drinking-related problems among college students at eight universities. Health Place 2003; 9: 1–6.
35. Cunradi CB. Neighborhoods, alcohol outlets and intimate partner violence: Addressing research gaps in explanatory mechanisms. Int J Environ Res Public Health 2010; 7: 799–813.
36. Cook WK, Bond J, Greenfield TK. Are alcohol policies associated with alcohol consumption in low‐and middle‐income countries? Addiction 2014; 109: 1081–1090.
© Copyright 2015 American Sexually Transmitted Diseases Association