Voluntary medical male circumcision (VMMC) is highly efficacious in preventing HIV acquisition in men.[1–4] In South Africa, where HIV incidence has been extremely high over the past three decades, national guidelines recommend that all men who test HIV-negative be offered a comprehensive prevention package that includes information on and referral to VMMC services, and that “the success of testing programs should be measured by the number of individuals successfully linked to…medical male circumcision services for HIV-negative males.”[5]

However, little is known about the current differences in HIV prevalence by circumcision status in real-world, non-clinical trial settings. The evidence justifying VMMC trials came from a body of observational studies demonstrating lower HIV prevalence among traditionally circumcised men.[6] It is unknown if this association differs after years of expanding VMMC access when the decision to undergo the procedure may relate to current HIV status or factors associated with future HIV status, and specifically whether these kinds of selection effects could be strong enough to outweigh the protective biological effect of VMMC. One message transmitted by current VMMC policy and the proven protective effect of VMMC is that circumcised men are less likely to be HIV-positive. There is emerging potential for female partners, who report preference for circumcision in part due to perceptions about HIV status,[7,8] to change their sexual behaviors in response to this assumption.[9,10] The implications for HIV risk rest on whether or not this assumption is founded.

There is also little known about male circumcision acceptability and uptake among older men in South Africa. In younger and general population South African and sub-Saharan African men, circumcision is generally perceived positively, with the link between circumcision and HIV/STI prevention cited as an important reason to become circumcised.[11–13] Older men, who are often overlooked as targets for HIV prevention interventions due to incorrect assumptions about their lack of sexual risk-taking,[14,15] and who came of age prior to VMMC recommendations for HIV prevention, may have different circumcision attitudes and patterns of circumcision uptake. Further, circumcision associated with traditional initiation ceremonies marking the rite of passage from childhood to adulthood is relatively common among Black South Africans and is more prevalent among older men than younger men.[16]

In this paper, we aim to fill persistent knowledge gaps related to male circumcision in older men in sub-Saharan Africa. First, we describe the prevalence of male circumcision in the population and identify socio-demographic predictors of being circumcised in a sample of men 40 years and older from a rural South African community. Then, we model the association between circumcision status and prevalent HIV infection to provide insight into how HIV prevalence differs by circumcision status in a non-experimental setting in a time of expanding VMMC access.

Of the 2345 men enrolled in the study, 68% were currently married, 41% reported no formal education, 11% reported African/traditional religious affiliation, and 29% were of Mozambican descent (Table 1). Median age was 61 years with interquartile range between 52 and 71 years.

One quarter of the men reported circumcision; of them, over half (56%) were circumcised in traditional initiation-based circumcision ceremonies while 44% were circumcised in hospital-based procedures. Those who reported hospital-based circumcision were younger, less likely to be widowed, more likely to have higher educational attainment, more likely to identify with Christian or Islamic religion, less likely to be of Mozambican descent, and more likely to live in a household in the highest wealth quintile, compared to those who were uncircumcised. Those who reported initiation-based circumcision were older, less likely to be married, more likely to have higher educational attainment, and less likely to be of Mozambican descent, compared to those who were uncircumcised.

Nearly a quarter of circumcised men (23%) were circumcised in childhood or early adolescence (before age 14), 36% were circumcised during adolescence (age 14–18), and 41% were circumcised in adulthood (age 19 or older). As expected, those who reported hospital-based circumcisions were more likely to report circumcision in adulthood compared to those who reported initiation-based circumcision.

Overall, laboratory-confirmed HIV prevalence among HAALSI men was 23% (95% CI: 21, 25), with no evidence for differences between uncircumcised men [24% (95% CI: 22, 26)] and circumcised men [23% (95% CI: 19, 27)] (Table 2 and Fig 1). HIV prevalence was lowest among those who reported an initiation-based circumcision [16% (95% CI: 12, 21)], higher among those who did not report circumcision [24% (95% CI: 22, 26)], and highest among those who reported a hospital-based circumcision [31% (95% CI: 25, 37)]. After adjustment, a protective association between traditional circumcision and HIV prevalence remained [PR (95% CI): 0.73 (0.54, 0.98)], and the association between hospital-based circumcision and heightened HIV prevalence was smaller in magnitude [PR (95% CI): 1.11 (0.88, 1.40)] with confidence interval spanning the null. No clear pattern emerged in HIV prevalence by age at circumcision in adjusted or unadjusted analyses; however, those who were circumcised between the ages of 14 to 18 years were the least likely to test HIV-positive [18% (95% CI: 13, 25)], compared to those who were circumcised at age 13 years or younger [23% (95% CI: 17, 33)], and those who were circumcised after age 18 [27% (95% CI: 21, 34)]. HIV prevalence did not vary significantly by age at circumcision when stratified by circumcision type.

In this analysis of population-based data on older men in rural South Africa, we examined circumcision history and the association between circumcision and HIV status in the current circumcision landscape. We found that one quarter of older men reported being circumcised, with slightly more than half of circumcisions reported as traditional initiation-based procedures as opposed to medical procedures. This circumcision prevalence is lower than the 2012 national estimate of 46% in men age 15 and older, but in line with findings indicating traditional circumcisions are more common than medical circumcision.[20] We also found that the demographic profile of those who were uncircumcised differed substantially from those with hospital-based circumcisions and those with initiation-based circumcisions. We found no differences in HIV prevalence by circumcision status overall, and that men with hospital-based circumcisions were more likely to test HIV-positive compared to both uncircumcised men and men with traditional initiation-based circumcision.

That hospital-based circumcision was not associated with lower HIV prevalence differs from the findings we expected based on (i) the national policy on selection of HIV-negative men for VMMC, (ii) the protective effect of VMMC on HIV acquisition, and (iii) the protective association we observed between traditional initiation-based circumcision and HIV. A large body of observational studies from the pre-VMMC era established that traditionally circumcised men were less likely to be HIV-positive. A systematic review of 27 studies[6] reported a protective effect in nearly all of the unadjusted analyses, with strengthened associations after covariate adjustment. In population-based, cross-sectional studies like ours, the overall protective effect was 0.55 (95% CI: 0.34, 0.54), slightly stronger than our estimate for traditionally circumcised men, but in contrast to our estimate for medically circumcised men.

Of course, our findings are plausible despite the high biological efficacy of medical circumcision in preventing HIV acquisition in men. The most likely explanation is that HIV-positive older men are circumcised in clinical settings in larger numbers than HIV-negative men, counter to the South African policy to target HIV-negative men with circumcision information and referral. One plausible pathway for this explanation is that HIV-positive men are more engaged in care than their HIV-negative counterparts, and circumcision services could be one of the clinical services to which they have more access.

Another possible explanation is that men who engage in riskier sexual behavior self-select into VMMC, resulting in heightened risk for subsequent HIV infection. Although no significant differences were observed by age at circumcision, HIV prevalence was highest among men who were circumcised in the oldest age category (after age 18). One possible explanation for this finding is that in adulthood men with higher than average risk of HIV acquisition chose to be circumcised but that no such selection effect existed in childhood. However, this explanation requires the perhaps improbable assumption that the risk behaviors among the circumcised confer risk at a magnitude able to overcome the otherwise protective circumcision effect.

Similarly, it is possible that older men engage in riskier sexual behavior after circumcision because they know that they are now at substantially reduced risk for HIV acquisition. However, this explanation is unlikely as there has been no evidence for this kind of risk compensation in prior circumcision studies in Africa,[21–26] and the magnitude of risk compensation that would have had to occur in our study population to bias the otherwise protective effect to become a significant association on the other side of the null is likely implausibly large. The possibility also exists for risk compensation in men with traditional initiation-based circumcision if they had been informed of the protective effects of circumcision. While risk compensation is unlikely to be the only explanation of the observed association between circumcision and HIV status in this study, it could have contributed to some extent to our findings, warranting further research on quantifying the level of risk compensation in communities similar to the study community.

Several features of the data structure and quality call for our findings be interpreted with caution. First, we used self-reported circumcision status with no objective examination to confirm true circumcision status, which could lead to biased results if men were unwilling or unable to accurately report their true circumcision status. Second, the data were cross-sectional in design so we were unable to disentangle the temporal relationship between circumcision and HIV status. Plausible bidirectional mechanisms exist and we were not able to assess their relative contributions given the rough categorization of age at circumcision and unknown date of HIV seroconversion. Finally, these data were collected in a sample of older men in a rural South African community. Generalizability of these results to younger men or men in more urban settings may not be possible.

Our findings are important for HIV prevention policy in South Africa for several reasons. First, among older men in rural South Africa, there remain many HIV-negative uncircumcised men who could receive HIV prevention benefits from VMMC as part of a comprehensive HIV prevention package promoting safer sexual practices tailored to the particular needs of older adults. Expansion of VMMC services to target older men with referrals could help address this unmet need. Second, the policy to target HIV-negative men with VMMC is likely not complied with in real-world settings as HIV prevalence was higher among medically circumcised men than among uncircumcised men. It is plausible that this policy, coupled with the widely-known protective effect of VMMC, gives the false impression that circumcised men are safer sex partners. If HIV-positive men actually take up the procedure at high rates, the promotion of VMMC as a procedure for HIV-negative men to prevent HIV may have the unintended consequence of increasing HIV transmission at the population-level. To reduce this risk, modifications of the existing VMMC policies and associated public engagement campaigns should be considered.

Medically circumcised older men in rural South Africa had higher HIV prevalence than uncircumcised men, despite the biological efficacy of VMMC and the South African policy explicitly targeting HIV-negative men for circumcision. This finding suggests that the association between circumcision and HIV status may be more strongly driven by selection into circumcision than the biological efficacy of circumcision in preventing HIV acquisition. The impression given from circumcision policy and dissemination of prior trial findings that those who are circumcised are safer sex partners may be incorrect in this age group.