We developed a model to estimate the potential impact of male circumcision programs for men and women in sub-Saharan Africa and examined the dynamic interaction between reduced susceptibility to HIV infection and subsequent behavioral disinhibition in the use of condoms by circumcised males. Overall, we found that circumcision programs could prevent a substantial number of new HIV infections in the African setting, and that moderate changes in condom use behavior do not significantly influence this outcome. The magnitude of the benefits from circumcision programs was sensitive to changes in sexual risk behavior, which for this study we approximated with changes in condom use to examine potential gender discrepancies: increased condom use would naturally lead to augmented program benefits but decreases in condom use would lead to decreased program benefits. All circumcision programs in which circumcision efficacy was approximately 60% or greater provided net benefits to the overall population in terms of infections prevented regardless of moderate changes in condom use behavior; only very large changes in condom use behavior (e.g., 50% or greater decrease in condom use) could significantly offset these benefits. In addition, we found that even relatively small circumcision programs would be beneficial and would continue to produce reductions in HIV transmission during the following decades. We estimated that conservative 5-year expanded circumcision programs targeting only 10–20% of uncircumcised men each year could produce substantial benefits over a wide range of values for circumcision protective effect, while tolerating moderate decreases in condom use.
We also found that a substantial number of infections would be prevented in women indirectly due to the decrease in male infections afforded by the circumcision programs and their associated potential for risk-reduction counseling to increase condom use—although the benefits to females were quantitatively less than the benefits to males. After twenty years, one-third of all infections prevented by these 5-year programs with 10 and 20% coverage goals would occur in the female population, but these gender differences in program benefits would gradually diminish over time. Additionally, transmission of HIV to females was still decreased for a wide variety of program simulations involving potential changes in risk behavior.
However, our model showed substantial gender disparities in program outcomes for some scenarios in which condom use decreased, which addresses concerns that an increase in risky sexual behavior by circumcised HIV-positive men might cause an increase in HIV prevalence in women, which could then increase the risk to men in a cyclical fashion [45
]. Although the majority of potential program scenarios we estimated resulted in a positive net value for the number of infections prevented, women might experience a greater number of HIV infections over the 20-year period in certain simulations if condom use decreased following program implementation. This could occur despite a positive net value for the overall number of infections prevented because of the difference in magnitude between the outcomes of the program for men and women. And even if women did not experience a greater number of HIV infections over the 20-year period (e.g., a positive net value for the total infections prevented in women), some scenarios with decreased condom use still resulted in periods of increased HIV infections for women over several years of the program.
Due to gender disparities in the protective effect of this intervention, circumcised males receive a direct benefit due to the protective effect of circumcision, while females receive only an indirect benefit from reduced population HIV prevalence. Further, because we modeled condom use in sexual partnerships to be determined by males, changes in sexual risk behavior for men receiving the intervention of circumcision directly correlated with changes in sexual risk behavior that place women at risk for HIV infection. In addition to highlighting the differences between potential benefits for men and women, our analyses demonstrate that risk behavior changes in the form of increases or decreases in condom use may be more or less influential in programs where an intervention can provide a direct benefit to only a fraction of the population (such as the case with male circumcision) versus the entire population (such as the case with HIV vaccines [26
Our results have confirmed the findings of previous model-based studies on the impact of male circumcision programs [16
], but have allowed for the examination of modest program coverage goals, post-circumcision changes in condom use behaviors, and gender interactions in heterosexual HIV transmission and program outcomes in greater detail—demonstrating the benefits of circumcision programs even when taking into account potentially offsetting factors such as minimal program coverage and moderate condom use behavior change in settings where the negotiation of condom use is gender-based. Although a recent expert panel on mathematical modeling of male circumcision programs concluded that increases in risk behavior would decrease the benefits of male circumcision programs overall [25
], whether these programs could cause potential harm—rather than just a decrease in benefit—to women at the population level has not been examined. Our analyses show the potential for circumcision programs to place women at greater overall risk for HIV infection in certain settings, and further exploration of gender-specific outcomes of male circumcision interventions is needed.
While the inclusion of gender-specific condom use negotiation and risk compensation is a strength of our model, our assumption of exclusive male negotiation of condom use for these analyses is one of its limitations. Although there is an imbalance of power in the negotiation of safe sex in Southern Africa, it is not absolute, and the impact of variations in male and female negotiating power warrants further investigation. In addition, the focus of the present analysis was to explore the impact of gender differences in power to negotiate safe sex, which is primarily manifested in the ability to specify condom use during sexual partnerships, on circumcision program outcomes. Other behavioral manifestations of gender differences in power to negotiate safe sex, such as polygamy, should be explored in the future.
The reduction in FTM HIV transmission of 61% (95%CI: 34,77%) used in our base case analyses for Soweto was based on the randomized controlled trial of adult male circumcision in South Africa, which was a single site study conducted nearby in Orange Farm [3
]. The other two trials in Kenya and Uganda reported efficacy results of 53% (95%CI: 22,72%) [2
] and 51% (95%CI: 16,72%) [1
], respectively, and preliminary long term follow-up data in Kenya indicates that circumcision efficacy is sustained and possibly strengthened to 64% (95%CI: 43,77%) at 42 months [46
]. Additional long-term follow-up data on circumcision efficacy is not yet available and the effectiveness of circumcision in preventing HIV transmission might vary in other populations and non-trial conditions. For these reasons, we explored values for the reduction in FTM HIV transmission from 20 to 80%, which encompass the trial confidence intervals, in sensitivity analyses, although a number of ecological and cohort studies indicate that the protective effect is indeed likely to be very high [47
]. We found that the model predictions were consistent over a wide variety of values and thus our results can likely be generalized to other populations with similar epidemic profiles and predominantly heterosexual spread of HIV, despite the initialization of the model with parameters specific to the African setting. However, the results cannot be extended to populations with major differences in route of HIV transmission or stage of the epidemic.
We examined only the impact of circumcising adult males, but modeling studies examining the impact of increased pediatric circumcision are certainly merited. Despite the immediate epidemiological benefits and reduced ethical issues surrounding the circumcision of sexually active adults able to provide informed consent, circumcision of infants and boys would eventually be more practical and provide greater public health benefits [57
]. We also did not simulate the impact of circumcision on other sexually transmitted infections (STIs) or their effect on HIV transmission. While circumcision may reduce other STIs, which in turn contributes to a reduction in HIV transmission, this effect is likely to be minimal compared with the effect of circumcision on HIV transmission itself [58
Additionally, our results do not take into account the fact that circumcision programs would involve a one-time intervention while programs to increase condom use require an intervention that must be practiced with every sex act over the life of the individual; therefore the best manner in which to allocate resources between different programs cannot be determined by our analyses. Our model also does not consider the impact of multiple, simultaneous prevention programs such as education on delaying intercourse, partner reduction, promotion of condom use, access to HIV counseling and testing, syringe exchange programs, STI treatment, treatment of HIV-positive individuals to reduce viral load, and eventually, chemoprophylaxis regimens, microbicides, and prophylactic or therapeutic vaccines [59
]. Further work on assessing the impact of multiple partially effective prevention programs is merited to allow for relative comparisons between different intervention package combinations.
Male circumcision has been shown to be effective, safe, affordable, acceptable, and will likely confer lifelong benefits. However, implementation of even the modest circumcision programs described in our study will depend on the ability to scale up operations: many clinics in Africa are already struggling to cope with the increased demand for circumcision following coverage in the media [30
] and a study in Soweto has shown limited capacity in public sector hospitals [62
]. Further, programs must ensure that all male circumcision procedures are both safe and voluntary and must remain sensitive to the cultural practices of different populations—although even cultures and ethnic groups which do not currently encourage circumcision may find it acceptable, as was shown in the South African Zulu and Tswana populations [63
]. Circumcision programs will need to provide risk-reduction counseling, both to individuals as well as the community. This is particularly important in the South African context, where studies have revealed beliefs that circumcised men can increase their sexual risk behavior [29
] and where risk behavior was already shown to increase slightly during the large circumcision trial conducted near Soweto [3
]. Further, in an HIV vaccine trial in Soweto, men who elected to undergo male circumcision reported higher levels of risky sexual behavior at baseline [65
]. Additionally, this risk-reduction counseling may need to be targeted in particular to men, given the reduced ability of women to negotiate condom use in the African setting and the fact that men will be receiving the intervention. Finally, programs should be evaluated on their effectiveness, with particular emphasis on whether changes in sexual risk behavior have occurred and the individual benefits to men and women.