To date, however, there have been few studies of the effect of food insufficiency on HIV transmission. Stillwaggon [10] found that the prevalence of HIV in 44 sub-Saharan African settings was highly correlated with declining energy and protein consumption. Similarly, Moore et al. [11] reported that weight loss in Rwanda was associated with eventual HIV seroconversion among women. Yet the mechanisms by which food insufficiency may lead to increased HIV transmission and acquisition have not been adequately characterized. One postulated mechanism is that lack of food and malnutrition weaken the immune system and can compromise gut and genital mucosal integrity, thereby increasing vulnerability to HIV once exposed [1,12]. Food insecurity is also hypothesized to increase sexual risk-taking—especially among women living in poverty who are often dependent on others for food and other resources, and whose human rights are inadequately protected [13]. Women in parts of sub-Saharan Africa such as Botswana and Swaziland often lack control over resources, including the food supply at home, while also bearing responsibility for caring for children, elder household members, and household members who are ill [1,14–16]. Previous qualitative research has shown that women may engage in sex exchange or get involved with intergenerational relationships in order to procure food for themselves and their children [1,8,17,18]. In a cross-sectional study by Oyefara et al. among 320 female sex workers in Lagos, Nigeria, 35% of respondents said that poverty and lack of other means to get food was responsible for their decision to become sex workers [19]. In addition, as a result of dependence on their partner for food and other resources, women may have little control over condom use [17]. For example, qualitative studies in Botswana and Swaziland have found that women often lack power to negotiate for safer sex in their relationships, a situation exacerbated by their poor socioeconomic circumstances [13,16,20]. While few studies have examined the specific impact of food insufficiency on sexual risk-taking, a number of studies have shown that low socioeconomic status is associated with sex exchange, coerced sex, and inconsistent condom use in African countries [1,21–25]. Conversely, greater negotiating power within sexual relationships and economic independence were found to be positively associated with condom use in a small cross-sectional study among 71 women in Gaborone, Botswana [26].

Multiple prior studies have shown strong correlations among unprotected sex, intergenerational sex, forced sex, lack of sexual control, and sex exchange in sub-Saharan Africa. For instance, African women who had experienced sexual violence and who lacked control over sexual decision-making were more likely to engage in unprotected sex, to exchange sex for money or resources, to have multiple partners, and to be HIV positive [32,35–38]. Women in intergenerational relationships were also more likely to engage in unprotected sex, sex exchange, to have multiple partners, and to have experienced forced sex [32,39]. Consequently, the impact of food insufficiency on each of these sexual behaviors is likely compounded by the interdependence of these risky behaviors on one another, risky behaviors that are in turn influenced by the social and economic inequality many African women face in a context of inadequate protection of their human rights.

Given that low socioeconomic status has been shown to be associated with inconsistent condom use, sex exchange, and forced sex in studies in sub-Saharan Africa [1,21,22], we sought to better understand whether the impact of food insufficiency on risky sex could be explained by income or other measures of socioeconomic status. We found that income and education did not significantly influence the relationship between food insufficiency and risky sexual behaviors. As has been documented elsewhere [40], this result may suggest that while food insufficiency is undoubtedly influenced by socioeconomic status, it is a distinct entity with unique causes and consequences. A possible explanation for this is that in sub-Saharan Africa there is often heterogeneity of food insecurity within socioeconomic strata; many indigent individuals are able to grow food on their own, and certain family members may be preferentially fed over others. For example, a number of studies have shown that women within households in various parts of sub-Saharan Africa may be less food secure than men as a result of unequal household food allocation, a situation exacerbated by their lack of control over decisions related to food production, consumption, and sale. Men are also often served both higher quantity as well as quality of food [40–42]. Since household income may not actually capture access to money and economic dependency within the household, another possible interpretation of these findings is that food insecurity is a better marker of poverty than income and education, and it is primarily poverty that drives increases in risky sexual behaviors. Part of the difficulty in teasing out the independent effects of food insecurity from low socioeconomic status is that these categories are complex and highly correlated. Consequently, we cannot exclude the possibility that socioeconomic status plays a more significant role in mediating the relationship between food insufficiency and risky sexual practices than our findings would suggest. Nevertheless, whether food insecurity affects HIV transmission behaviors above and beyond the effects attributable to low socioeconomic status, or whether food insecurity is simply a strong marker of socioeconomic status, these findings suggest that intervening at the level of food insecurity could potentially play an important role in curtailing the spread of HIV/AIDS.

While food insufficiency was a consistent correlate of sexual risk-taking for women, for men food insufficiency was associated with only a small increase in the odds of reporting unprotected sex (14%), and was not associated with other risky sexual outcomes. Women were also significantly more likely to report food insufficiency than men in both Botswana and Swaziland. These findings highlight the strong interplay between gender inequality, food insufficiency, and sexual risk-taking in sub-Saharan Africa. By customary law and traditional norms and practices, women often find themselves subordinated to male heads of household [43], which contributes to both food insufficiency among women and risky sexual behaviors as a means to procure food [1]. The fact that women are more likely to be malnourished further heightens their risk of acquiring HIV in view of the effects of malnutrition on the immune system [1,12]. As others have argued, there is a strong need to target gender-discrimination and gender-based violence in HIV prevention programs [18,26,36,37,43], an effort that will require social, legal, structural, and cultural changes at many levels in society. For men in sub-Saharan Africa, one possible mechanism through which food insufficiency may lead to increase sexual risk-taking is that lack of food often leads to migration for work [8,44], and migration has been found to be associated with increased sexual risk-taking and HIV prevalence in multiple studies [45–49]. Our study design was not structured to adequately capture this specific causal pathway among men, and more studies are needed that examine associations among food insufficiency, labor migration, and sexual risk-taking in men.

Most HIV prevention interventions to date focus on changing people's knowledge, attitudes, and behaviors, which are believed to be the proximate causes of high HIV transmission [50]. Few interventions actually target the underlying circumstances and fundamental causes that may foster these behaviors and attitudes, and there has been a recent call to broaden the scope of interventions to consider community- and national-level factors [51]. Blankenship et al. argue for the implementation of structural interventions for HIV prevention, in that these interventions “promote health by altering the structural context in which health is produced and reproduced” [50]. They point to evidence that micro-credit programs for women and other economic and educational interventions help improve women's household bargaining power and decrease their dependence on male partners, which in turn can provide them with a basis upon which to demand safer sexual practices. Consistent with this argument, we found that higher education was associated with lower odds of risky sexual behaviors for women but not men, suggesting that education may help improve gender power imbalances and women's ability to negotiate safer sex. Attesting to the importance of structural interventions targeted at women, the IMAGE (Intervention with Microfinance for AIDS and Gender Equity) study reported that a poverty-focused microfinance initiative combined with a gender and HIV training curriculum led to a 55% reduction in levels of intimate-partner violence [52]. In addition to income generation programs and educational initiatives, our findings suggest that interventions that use targeted food supplementation and food production strategies could help address some of the gender and economic disparities that drive unsafe sexual behaviors, and should be considered as a way to reduce HIV transmission behaviors in specific high-risk populations. Any such interventions would certainly need to address equity of food distribution within the household as well as long-term sustainability.

Consistent with previous research [32,53–55]. we found that problem drinking and heavy drinking were strongly and consistently associated with all risky sexual behaviors examined for both men and women, and that a dose–response relationship was seen between alcohol use and sexual risk-taking. We have reported that alcohol use was the strongest predictor of inconsistent condom use, sex exchange, and multiple partnerships among both men and women in Botswana [32]. This study advances those previous findings by showing that the relationship between alcohol use and risky sex also holds in Swaziland, and also by linking alcohol use to having experienced forced sex among women.

In addition to the limitations in our measures of socioeconomic status discussed above, there are several additional limitations to this study. First, the causal direction of the associations between food insufficiency and risky sexual practices cannot be inferred from the cross-sectional study design. Second, social desirability bias may have influenced reporting of risky sexual behaviors and other personal information. Of note, the WHO multi-country study on women's health and domestic violence found a higher prevalence of forced sex in three countries in sub-Saharan Africa compared to our study [56]. Under-reporting of forced sex and other risky sexual behaviors may have undermined the validity of our findings [57]. Yet, even if risky sexual practices were under-reported, this would not necessarily affect the associations we found between food insufficiency and risky sex. Third, our 12-mo interval may be vulnerable to recall bias and could not detect more precise temporal associations between short-term food insufficiency and HIV transmission risk behaviors, or seasonal variability with respect to food insufficiency. These limitations, however, would bias the study toward the null hypothesis. As such, the true associations may be stronger than our data indicate. Finally, while our single question to measure food insufficiency was previously validated, it may have underestimated the prevalence of poor access to food. Food insufficiency is only one component of the broader concept of food insecurity, which also encompasses insufficient quality and diversity of foods, feelings of deprivation or restricted choice about the amount and types of food available, and inability to procure food in a socially acceptable manner [58,59]. More detailed studies using more extensive and sensitive food security scales validated in the African context with attention to possible regional and cultural differences will be important to confirm and expand upon these preliminary relationships.