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      The Potential Impact of Male Circumcision on HIV in Sub-Saharan Africa

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          Abstract

          Background

          A randomized controlled trial (RCT) has shown that male circumcision (MC) reduces sexual transmission of HIV from women to men by 60% (32%−76%; 95% CI) offering an intervention of proven efficacy for reducing the sexual spread of HIV. We explore the implications of this finding for the promotion of MC as a public health intervention to control HIV in sub-Saharan Africa.

          Methods and Findings

          Using dynamical simulation models we consider the impact of MC on the relative prevalence of HIV in men and women and in circumcised and uncircumcised men. Using country level data on HIV prevalence and MC, we estimate the impact of increasing MC coverage on HIV incidence, HIV prevalence, and HIV-related deaths over the next ten, twenty, and thirty years in sub-Saharan Africa. Assuming that full coverage of MC is achieved over the next ten years, we consider three scenarios in which the reduction in transmission is given by the best estimate and the upper and lower 95% confidence limits of the reduction in transmission observed in the RCT.

          MC could avert 2.0 (1.1−3.8) million new HIV infections and 0.3 (0.1−0.5) million deaths over the next ten years in sub-Saharan Africa. In the ten years after that, it could avert a further 3.7 (1.9−7.5) million new HIV infections and 2.7 (1.5−5.3) million deaths, with about one quarter of all the incident cases prevented and the deaths averted occurring in South Africa. We show that a) MC will increase the proportion of infected people who are women from about 52% to 58%; b) where there is homogenous mixing but not all men are circumcised, the prevalence of infection in circumcised men is likely to be about 80% of that in uncircumcised men; c) MC is equivalent to an intervention, such as a vaccine or increased condom use, that reduces transmission in both directions by 37%.

          Conclusions

          This analysis is based on the result of just one RCT, but if the results of that trial are confirmed we suggest that MC could substantially reduce the burden of HIV in Africa, especially in southern Africa where the prevalence of MC is low and the prevalence of HIV is high. While the protective benefit to HIV-negative men will be immediate, the full impact of MC on HIV-related illness and death will only be apparent in ten to twenty years.

          Editors' Summary

          Background.

          Africa is the continent most affected by HIV/AIDS, and it is important to consider all possible means of reducing the spread of HIV infection. Male circumcision has been a tradition in many parts of Africa for hundreds of years. Boys who are circumcised usually have it done in late childhood or their early teenage years. It was noticed some years ago that those African groups in which circumcision is routinely done on all boys have fewer cases of HIV/AIDS than are found in groups where circumcision is not a tradition. This finding gave rise to the idea that circumcision might give a degree of protection against HIV, though it was recognised that some other, unknown difference between these groups of people might actually be the important factor. In 2005 a trial was reported from the Orange Farm area of South Africa, in which uncircumcised men were offered the chance to be circumcised. The men who agreed were divided at random into those who had the operation straightaway and those who were to have it two years later. During the next 18 months, the number of new cases of HIV infection was much higher amongst the men who had not been circumcised. Circumcision did therefore seem to offer a measure of protection against infection. This protective effect was estimated at being about 60%. Similar trials are under way in other parts of Africa but there are no results available from them at this stage.

          Why Was This Study Done?

          If the level of effectiveness of circumcision suggested by the South African trial is correct, then, as one part of a range of measures to reduce the spread of HIV, it would seem logical to encourage the practice of male circumcision. It would be useful to have an estimate of just how many new cases could be prevented and how many lives would be saved by the promotion of male circumcision. Calculations would have to allow for various factors, such as the present level of HIV infection, which varies from one country to another, and the fact that many men are already circumcised.

          What Did the Researchers Do and Find?

          This research did not involve collecting any new data. The researchers used mathematical modelling to make calculations. They based their model on data from the Orange Farm trial and on information from various sub-Saharan African countries on the proportion of men who are circumcised and the proportion who are HIV-positive. They made the assumption that if circumcision is intensively promoted, all men in those countries will be circumcised in 10 years time. They calculated the number of new cases that would be prevented and the lives that would be saved in ten years, 20 years, and 30 years time. Their best estimate is that with the promotion of male circumcision, two million cases and 0.3 million deaths will be avoided in ten years time. Over the following ten years, according to the researchers' model, a further 3.7 million cases and 2.7 million deaths would be prevented. Most of the initial impact would be in men, but the reduction in the number of HIV-positive men would in time also lower the risk of women becoming infected. Overall, on the basis of these calculations, male circumcision would reduce the rate of infections by about 37%—both female-to-male and male-to-female transmission. The size of the impact would vary from one country to another; it would be greatest in southern Africa where HIV infection rates are high and circumcision rates relatively low compared with the rest of sub-Saharan Africa.

          What Do These Findings Mean?

          Male circumcision alone cannot bring the HIV/AIDS epidemic in Africa under control. Even circumcised men can become infected, though their risk of doing so is much lower. However, the researchers call for the promotion of male circumcision to become a major part of AIDS control programmes. Their results are based on the findings of just one study (the Orange Farm trial), and it will be important to repeat the calculations when further studies have been completed.

          Additional Information.

          Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0030262:

          • The Orange Farm trial was published in PLoS Medicine. Several articles discussing the trial were also published in the same issue of the journal

          • The Joint United Nations Programme on HIV/AIDS (UNAIDS) has information about the state of the HIV/AIDS epidemic and prevention strategies worldwide. It produces an annual report and has documents on a wide range of topics

          •  AEGIS is the world's largest searchable database on HIV and AIDS.

          • Many organizations provide information on AIDS prevention—for example, the Terrence Higgins Trust

          • The World Bank's Global HIV/AIDS Program has a report about male circumcision and HIV infection

          Abstract

          A modelling study, based on one trial plus national figures for current prevalence of HIV and of male circumcision (MC), found increasing MC in Africa could produce major fall in HIV prevalence in 10-12 years.

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          Most cited references40

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          Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

          From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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            Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda.

            The probability of HIV-1 transmission per coital act in representative African populations is unknown. We aimed to calculate this probability overall, and to estimate how it is affected by various factors thought to influence infectivity. 174 monogamous couples, in which one partner was HIV-1 positive, were retrospectively identified from a population cohort in Rakai, Uganda. Frequency of intercourse and reliability of reporting within couples was assessed prospectively. HIV-1 seroconversion was determined in the uninfected partners, and HIV-1 viral load was measured in the infected partners. Adjusted rate ratios of transmission per coital act were estimated by Poisson regression. Probabilities of transmission per act were estimated by log-log binomial regression for quartiles of age and HIV-1 viral load, and for symptoms or diagnoses of sexually transmitted diseases (STDs) in the HIV-1-infected partners. The mean frequency of intercourse was 8.9 per month, which declined with age and HIV-1 viral load. Members of couples reported similar frequencies of intercourse. The overall unadjusted probability of HIV-1 transmission per coital act was 0.0011 (95% CI 0.0008-0.0015). Transmission probabilities increased from 0.0001 per act at viral loads of less than 1700 copies/mL to 0.0023 per act at 38 500 copies/mL or more (p=0.002), and were 0.0041 with genital ulceration versus 0.0011 without (p=0.02). Transmission probabilities per act did not differ significantly by HIV-1 subtypes A and D, sex, STDs, or symptoms of discharge or dysuria in the HIV-1-positive partner. Higher viral load and genital ulceration are the main determinants of HIV-1 transmission per coital act in this Ugandan population.
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              • Record: found
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              Male circumcision and risk of HIV infection in sub-Saharan Africa: a systematic review and meta-analysis.

              To systematically review studies of male circumcision and the risk of HIV-1 infection in men in sub-Saharan Africa, and to summarize the findings in a meta-analysis. A meta-analysis of observational studies. A systematic literature review was carried out of studies published up to April 1999 that included circumcision as a risk factor for HIV-1 infection among men in sub-Saharan Africa. A random effects meta-analysis was used to calculate a pooled relative risk (RR) and 95% confidence interval (CI) for all studies combined, and stratified by type of study population. Further analyses were conducted among those studies that adjusted for potential confounding factors. Twenty-seven studies were included. Of these, 21 showed a reduced risk of HIV among circumcised men, being approximately half that in uncircumcised men (crude RR = 0.52, CI 0.40-0.68). In 15 studies that adjusted for potential confounding factors, the association was even stronger (adjusted RR = 0.42, CI 0.34-0.54). The association was stronger among men at high risk of HIV (crude RR = 0.27; adjusted RR = 0.29, CI 0.20-0.41) than among men in general populations (crude RR = 0.93; adjusted RR = 0.56, CI 0.44-0.70). Male circumcision is associated with a significantly reduced risk of HIV infection among men in sub-Saharan Africa, particularly those at high risk of HIV. These results suggest that consideration should be given to the acceptability and feasibility of providing safe services for male circumcision as an additional HIV prevention strategy in areas of Africa where men are not traditionally circumcised.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Med
                pmed
                PLoS Medicine
                Public Library of Science (San Francisco, USA )
                1549-1277
                1549-1676
                July 2006
                11 July 2006
                : 3
                : 7
                : e262
                Affiliations
                [1] 1World Health Organization, Stop TB Department, Geneva, Switzerland
                [2] 2Department of Environmental Science, Policy, and Management, University of California Berkeley, Berkeley, California, United States of America
                [3] 3Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, Pennsylvania, United States of America
                [4] 4Joint United Nations Programme on HIV/AIDS (UNAIDS), Policy, Evidence, and Partnerships Department, Geneva, Switzerland
                [5] 5South African Centre for Epidemiological Modelling and Analysis, Stellenbosch, South Africa
                [6] 6World Health Organization, Family and Community Health, Geneva, Switzerland
                [7] 7INSERM, Saint Maurice, France
                [8] 8University of Versailles-Saint Quentin, Faculté de Médecine Paris-Ile-de-France-Ouest, Saint Maurice, France
                [9] 9Assistance Publique-Hôpitaux de Paris, Hôpital Ambroise Pare, Boulogne, France
                San Francisco General Hospital United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: williamsbg@ 123456who.int

                Competing Interests: The authors have declared that no competing interests exist.

                Article
                10.1371/journal.pmed.0030262
                1489185
                16822094
                e3cf79d5-5dd8-42a9-938d-27004d47eef9
                Copyright: © 2006 Williams et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 7 December 2005
                : 28 March 2006
                Categories
                Research Article
                Infectious Diseases
                Epidemiology/Public Health
                Health Policy
                HIV/AIDS
                Statistics
                HIV Infection/AIDS
                Sexual Health
                Public Health
                Epidemiology
                Medicine in Developing Countries

                Medicine
                Medicine

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