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Bias File 9. Circumcision And Case studies of bias in real life epidemiologic studies Bias File 9. Male circumcision for HIV prevention: from confounding to causality Compiled by Madhukar Pai, MD, PhD Jay S Kaufman, PhD Department of Epidemiology, Biostatistics & Occupational Health McGill University, Montreal, Canada [email protected] & [email protected] THIS CASE STUDY CAN BE FREELY USED FOR EDUCATIONAL PURPOSES WITH DUE CREDIT 1 Bias File 9. Male circumcision for HIV prevention The story of male circumcision for HIV prevention is a long and fascinating one. Ecological studies in the 1980s and early 1990s provided early evidence that in African countries where male circumcision is practised, HIV seroprevalence was considerably lower than in areas where it is not practised. For example, Moses and others published an ecological study using data from 41 countries in Africa, with results supporting this hypothesis (figure). In the 1990s and early 2000s, a large number of observational studies were done, mostly cross-sectional studies (e.g. Auvert B et al. AIDS 2001), with a few case- control (e.g. Quigley M et al. AIDS 1997) and cohort (e.g. Gray RH et al. AIDS 2000) studies. Although many of these observational studies showed a protective effect of circumcision, they were highly controversial because of concerns about bias and confounding. In 2005, a systematic review was published in the Lancet Infectious Diseases by Siegfried et al., and this review included 37 observational studies on circumcision and HIV. At that time, there were no published randomized controlled trials (RCTs) on this topic. The review concluded that "although most studies show an association between male circumcision and prevention of HIV, these results may be limited by confounding, which is unlikely to be adjusted for." The panel from the paper by Siegfried provides a list of potential confounding variables. Because of the risk of uncontrolled confounding, even in 2005, many researchers doubted whether the association between circumcision and HIV was really causal. 2 In October 2005, the first ever randomized controlled trial on male circumcision and HIV was published in PLoS Medicine (Auvert B et al.). A total of 3,274 uncircumcised men in South Africa, aged 18–24 y, were randomized to a control or an intervention (circumcision) group with follow-up visits at months 3, 12, and 21. Male circumcision was offered to the intervention group immediately after randomization and to the control group at the end of the follow-up. The trial was stopped at the interim analysis. There were 20 HIV infections (incidence = 0.85 per 100 person-years) in the intervention group and 49 (2.1 per 100 person-years) in the control group, corresponding to an RR of 0.40 (95% CI: 0.24%–0.68%). This RR corresponds to a protection of 60% (95% CI: 32%–76%). The authors concluded that "male circumcision provides a degree of protection against acquiring HIV infection, equivalent to what a vaccine of high efficacy would have achieved." This landmark first RCT on male circumcision provided powerful experimental evidence that the association between circumcision and HIV was unlikely to be due to confounding. The table below, from the PLoS Med paper, shows the distribution of various confounders in the two randomized groups. The groups were strikingly comparable, underscoring a critical advantage of randomization - known and even unknown and unmeasured confounders are likely to be evenly distributed across the intervention and control groups. Evidently, one well-conducted RCT had a bigger impact than a large number of observational studies. By 2007, two more RCTs on circumcision and HIV were fast-tracked and published in the same issue of the Lancet, one from Uganda (Gray et al. Lancet 2007) with 4996 men, and another from Kenya (Bailey et al. Lancet 2007) with 2784 men included. Both trials had to be stopped early because interim analyses showed significant efficacy. These trials confirmed the results of the first RCT from South Africa. In fact, the results of the 3 RCTs were stunningly consistent, as show in the meta-analysis by Mills et al. (HIV Med 2008). 3 The table below (from Mills et al.) summarizes the results of all 3 RCTs: The pooled random effects RR was 0.44 (95% CI 0.33–0.60). The risk difference was 0.014 (95% CI 0.07– 0.21), yielding a NNT of 72 (95% CI 50–143) [Forest plot shown below, from Mills et al.]. Because of the strong and consistent evidence from RCTs, UNAIDS and other HIV agencies now recommend that male circumcision be recognized as an additional important intervention to reduce the risk of heterosexually acquired HIV infection in men. Using the RCT evidence, subsequent mathematical modeling studies by UNAIDS & WHO (PLoS Med 2009) suggest that one HIV infection can be averted for every five to 15 male circumcisions performed, and costs to avert one HIV infection ranges from US$150 to US$900 using a 10-y time horizon. The big challenge now is to actually scale-up and implement this efficacious intervention in countries where it is urgently needed. Unfortunately, even in 2009-2010, countries such as South Africa were not routinely providing this intervention, nor educating its public about the potential benefits of circumcision (Dugger C. New York Times 2009). Clearly, translating evidence and policy into real impact and saved lives is the next big step in this evolving story. Another interesting twist in the tale is the lack of evidence that male circumcision offers the same degree of protection in homosexual men. In 2008, Millett et al. published a meta-analysis in JAMA, on whether male circumcision provides protection against HIV infection among men who have sex with men (MSM). In this meta-analysis of 15 observational studies of the association of circumcision status and HIV infection among 53 567 MSM, the odds of being HIV positive were 14% lower among MSM who were circumcised than among MSM who were uncircumcised, but the difference was not statistically significant. To date, no RCTs have looked the effect of circumcision among MSM. 4 For students of epidemiology, circumcision for HIV prevention offers a fascinating case study because this association has been studied using every possible epidemiological study design: • Ecological (e.g. Moses et al., 1990) • Cross-sectional (e.g. Auvert et al., 2001) • Case-control (e.g. Quigley et al. 1997) • Cohort (e.g. Gray et al. 2000) • Systematic review of observational studies [before RCTs were done] (Seigfried et al. 2005) • Randomized controlled trials (Auvert 2005; Gray 2007 & Bailey 2007) • Meta-analysis of RCTs (Mills et al. 2008). A complete set of these various designs is included in the appendix. Together, these papers provide real- life examples of every major epidemiologic concept, from study design, measures of disease frequency and effect, to selection bias, information bias, confounding, interaction, meta-analysis and causality. Also, this collection provides an interesting example of RCT evidence agreeing with much of the observational evidence. Not only was confounding not the reason for the association seen in the observational studies, but in fact there didn’t turn out to be very much confounding at all. The RCT effects turned out to be fairly similar in magnitude to most of the case-control and cohort estimates, suggesting that there was almost no confounding at all. Finally, this collection provides a nice example of epidemiology succeeding in uncovering a real causal effect, one that can be a useful public health intervention for an important disease for which an effective vaccine is still not available. Sources and suggested readings* 1. Moses S, et al. Geographical patterns of male circumcision practices in Africa: association with HIV seroprevalence. Int J Epidemiol 1990;19(3):693-97. 2. Auvert B, et al. Male circumcision and HIV infection in four cities in sub-Saharan Africa. AIDS 2001;15:S31-40. 3. Quigley M, et al. Sexual behavior patterns and other risk factors for HIV infection in rural Tanzania: a case- control study. AIDS 1997;11:237-48. 4. Gray RH, et al. Male circumcision and HIV acquisition and transmission: cohort studies in Rakai, Uganda. AIDS 2000;14:2371-81. 5. Siegfried N et al. HIV and male circumcision - a systematic review with assessment of the quality of studies. Lancet Infect Dis 2005;5:165-73. 6. Auvert B, et al. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 Trial. PLoS Med. 2005 Nov;2(11):e298. 7. Gray RH, et al. Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet. 2007 Feb 24;369(9562):657-66. 8. Bailey RC, et al. Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet. 2007 Feb 24;369(9562):643-56. 9. Mills E, et al. Male circumcision for the prevention of heterosexually acquired HIV infection: a meta-analysis of randomized trials involving 11,050 men. HIV Med. 2008 Jul;9(6):332-5. 10. UNAIDS/WHO/SACEMA Expert Group on Modelling the Impact and Cost of Male Circumcision for HIV Prevention (2009) Male Circumcision for HIV Prevention in High HIV Prevalence Settings: What Can Mathematical Modelling Contribute to Informed Decision Making? PLoS Med 6(9): e1000109. 11. Dugger C. South Africa Is Seen to Lag in H.I.V. Fight. New York Times, 19 July 2009. URL: http://www.nytimes.com/2009/07/20/world/africa/20circumcision.html 12. Millett GA et al. Circumcision Status and Risk of HIV and Sexually Transmitted Infections Among Men Who Have Sex With Men. JAMA. 2008;300(14):1674-1684. *From this readings list, the most relevant papers are enclosed.
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