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Circumcision for HIV Prevention: Failure to Fully Account for Behavioral Risk Compensation EDITORIAL
 
 
  Seth Kalichman, Lisa Eaton, Steven Pinkerton
 
Seth Kalichman (seth.kalichman@uconn.edu)
Lisa Eaton, University of Connecticut, Storrs, Connecticut, United States of America
Steven Pinkerton, Center for AIDS Intervention Research, Milwaukee, Wisconsin, United States of America
 
Funding: Preparation of this article was supported by the National Institute of Mental Health grant R01 MH71164.
 
Competing Interests: The authors have declared that no competing interests exist.
 
Citation: Kalichman S, Eaton L, Pinkerton S (2007) Circumcision for HIV Prevention: Failure to Fully Account for Behavioral Risk Compensation. PLoS Med 4(3): e138 doi:10.1371/journal.pmed.0040138
 
Published: March 27, 2007
 
Three randomized controlled trials (RCTs) of male circumcision (MC) have been halted when interim analyses showed significant reductions in HIV infection among men who received this intervention [1-3]. Modeling suggests that increased MC coverage in southern Africa could prevent as many as 2 million HIV infections over ten years [4]. Moreover, the cost-effectiveness analysis by Kahn et al. recently published in PLoS Medicine indicates that MC could be cost-saving [5]. However, the protection of MC may be partially offset by increased HIV risk behavior, or "risk compensation," especially reduction in condom use or increases in numbers of sex partners. Risk compensation occurs when individuals adjust their behavior in response to perceived changes in their vulnerability to a disease [6]. Risk compensation may be especially important for MC because avoiding the sexual dissatisfactions of condom use and the desire to have more sex partners are likely to be significant motivations for men to seek circumcision [7]. In South Africa, 73% of men between the ages of 15 and 24 report using condoms during the last time they had sex [8]. It is difficult to imagine a convincing public health message that effectively influences men to undergo circumcision and continue to consistently use condoms.
 
Circumcised men in the ANRS 1265 trial reported 18% more sexual contacts at follow-up than did uncircumcised men, but no other sexual behavior differences were obtained [1]. However, for ethical reasons all men in MC RCTs receive ongoing risk-reduction counseling and free condoms, which reduces the utility of these trials for estimating the potential behavioral impact of MC when implemented in a natural setting. One model of the potential impact of MC did not take into account risk compensation [4], but noted that "increases in risk-taking behaviour among circumcised men could reduce the benefit of MC." Based on the 18% difference in sexual contacts for circumcised and uncircumcised men in the ANRS 1265 trial and the assumption that "risk compensation might be higher in a nonresearch program scale-up," Kahn et al. [5] adjusted the 60% effectiveness estimate obtained in this RCT downward to 50% to reflect a 25% increase in sexual risk behaviors among circumcised men. Although Kahn et al.'s model explicitly incorporated the increased risk of HIV acquisition associated with risk compensation, it did not consider the impact of risk compensation on the HIV transmission risk of HIV-infected circumcised men, or on circumcised men's risk for non-HIV sexually transmitted infections (STIs).
 
There is no evidence that circumcision increases or decreases the risk of HIV transmission by HIV-infected men. However, risk compensation by HIV-infected circumcised men will substantially increase the risk of transmission to their sex partners. This suggests that, in the short term at least, circumcision would reduce the incidence of HIV among men, but increase the incidence among women, translating to increased prevalence among women, which in turn translates to greater risk to men. Epidemiological models of MC should take this dynamic into account.
 
Countless studies have shown that ulcerative and non-ulcerative STIs account for at least some of the rapid increases in HIV transmission in southern Africa [9]. Non-HIV STIs are associated with a 2- to 5-fold increase in HIV transmission risk in countries with low and high rates of MC [9]. In areas with prevalent STIs, the relative increase in men's STI-associated HIV risk can be as high as 60% to 340% [10]. Circumcision likely reduces the risk of acquiring a non-HIV STI and may be partially responsible for the decreased HIV risk observed in circumcision RCTs [1]. Nevertheless, the failure of models to account for increased STI risk due to risk compensation likely inflates estimates of averted HIV infections. Estimates of HIV risks resulting from increased exposure to STIs that coincide with reductions in condom use have been included in previous models of the cost-effectiveness of HIV prevention interventions [11] and should be included in MC models.
 
References
 
1. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, et al. (2005) Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: The ANRS 1265 Trial. PLoS Med 2: e298-doi:10.1371/journal.pmed.0020298 doi:10.1371/journal.pmed.0020298. Find this article online
 
2. Bailey RC, Moses S, Parker C, Agot K, Maclean I, et al. (2007) Male circumcision for HIV prevention in young men in Kisumu, Kenya: A randomized controlled trial. Lancet 369: 643-656. Find this article online
 
3. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, et al. (2007) Male circumcision for HIV prevention in Rakai, Uganda: A randomized trial. Lancet 369: 657-666. Find this article online
 
4. Williams BG, Lloyd-Smith JO, Gouws E, Hankins C, Getz WM, et al. (2006) The potential impact of male circumcision on HIV in Sub-Saharan Africa. PLoS Med 3: e262-doi:10.1371/journal.pmed.0030262 doi:10.1371/journal.pmed.0030262. Find this article online
 
5. Kahn JG, Marseille E, Auvert B (2006) Cost-effectiveness of male circumcision for HIV prevention in a South African setting. PLoS Med 3: e517-doi:10.1371/journal.pmed.0030517 doi:10.1371/journal.pmed.0030517. Find this article online
 
6. Pinkerton SD (2001) Sexual risk compensation and HIV/STD transmission: Empirical evidence and theoretical considerations. Risk Analysis 21: 727-736. Find this article online
 
7. Westercamp N, Bailey RC (2006) Acceptability of male circumcision for prevention of HIV/AIDS in sub-Saharan Africa: A review. AIDS Behav. E-pub 20 October 2006. doi: 10.1007/s10461-006-9169-4.
 
8. Shisana O, Rehle T, Simbayi L, Parker W, Bhana A, et al. (2005) South African national HIV prevalence, incidence, behaviour and communication survey 2005. Cape Town: Human Sciences Research Council Press.
 
9. Fleming DT, Wasserheit JN (1999) From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Trans Infect 75: 3-17. Find this article online
 
10. Royce R, Sena A, Cates W Jr, Cohen MS (1997) Sexual transmission of HIV. New Eng J Med 336: 1072-1078. Find this article online
 
11. Chesson HW, Pinkerton SD (2000) Sexually transmitted diseases and the increased risk for HIV transmission: Implications for cost-effectiveness analyses of sexually transmitted disease prevention interventions. J Acquir Immune Defic Syndr 24: 48-55.
 
Circumcision for HIV Prevention: Authors' Reply
 
James G. Kahn, Elliot Marseille, Bertran Auvert
 
Funding: The authors received no specific funding for this article.
 
Competing Interests: The authors have declared that no competing interests exist.
 
Citation: Kahn JG, Marseille E, Auvert B (2007) Circumcision for HIV Prevention: Authors' Reply. PLoS Med 4(3): e146 doi:10.1371/journal.pmed.0040146
 
Published: March 27, 2007
 
James G. Kahn (jgkahn@ucsf.edu)
Elliot Marseille, University of California San Francisco, San Francisco,
California, United States of America
Bertran Auvert, Institut National de la Sante et de la Recherche Medicale (INSERM), U687 Saint-Maurice, France
 
The issues regarding risk compensation raised by Kalichman et al. [1] are cogent for refining modeled estimates of the impact of male circumcision (MC). Even more important is to empirically monitor risk compensation during the scale-up of male circumcision.
 
As Kalichman et al. note, we included in our modeling of MC impact a risk compensation level for men susceptible to HIV above that observed in the Orange Farm trial.
 
However, we did not incorporate risk compensation among the HIV infected, an adjustment which would have lessened the estimated benefits of male circumcision. These two biases are offsetting. Another conservative bias in our analysis is that we used the per-randomization protective effect of 0.60, rather than the per-clinical protocol protective effect of 0.70. Arguably, effectiveness in practice is better captured by the latter, and this would increase the estimated benefits of male circumcision.
 
The inclusion of the effects of non-HIV sexually transmitted infections (STIs) as risk co-factors would add a useful dimension to our analysis. The net effect could be to decrease or increase MC impact. As Kalichman et al. note, increased STIs associated with risk compensation in newly circumcised HIV-infected men would likely lessen MC impact. However, in a concentrated epidemic setting where STIs play a greater role in HIV transmission than in South Africa, the STI-reducing effects of MC in HIV-susceptible men could further increase the benefits of MC in preventing HIV.
 
Regarding the magnitude of risk compensation, we are encouraged by recent data suggesting that MC does not increase risky behavior, and may lead to a transient decrease [2]. However, we, like Kalichman et al. and others, are eager to see the favorable experience in clinical trials carried over to routine and widely operating programs. Thus, the current efforts to plan MC scale-up emphasize the need for an MC procedure that incorporates effective risk reduction counseling. In the context of a medicalized adult male circumcision model, and a clear public health message, risk compensation can be minimized. Thus, a great value of MC scale-up is the opportunity to directly deliver a strong behavioral prevention message. A similar risk reduction message has worked well with antiretroviral therapy in Africa [3].
 
The ultimate and critical test is monitoring risk behaviors in communities where MC is scaled up. If risk compensation is higher than expected, redoubled risk reduction methods will be imperative.
 
References
 
1. Kalichman S, Eaton L, Pinkerton S (2007) Circumcision for HIV prevention: Failure to fully account for behavioral risk compensation. PLoS Med 4: e138-doi:10.1371/journal.pmed.0040138 doi:10.1371/journal.pmed.0040138. Find this article online
 
2. Agot KE, Kiarie JN, Nguyen HQ, Odhiambo JO, Onyango TM, et al. (2007) Male circumcision in Siaya and Bondo Districts, Kenya: Prospective cohort study to assess behavioral disinhibition following circumcision. J Acquir Immune Defic Syndr 44: 66-70. Find this article online
 
3. Bunnell R, Ekwaru JP, Solberg P, Wamai N, Bikaako-Kajura W, et al. (2006) Changes in sexual behavior and risk of HIV transmission after antiretroviral therapy and prevention interventions in rural Uganda. AIDS 20: 85-92.
 
 
 
 
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