Thursday April 12 2012

Male circumcision for HIV prevention: What does the scientific evidence say?


By Joseph KB Matovu, Rhoda K. Wanyenze & David Serwadda

Of recent, the media has published a number of articles related to male circumcision, including two articles in the Daily Monitor. The first article entitled ‘Circumcision does not reduce HIV spread’ (Daily Monitor, March 6, 2012) was written by Flavia Lanyero. Flavia’s article is based on a paper published by Gregory J Boyle and George Hill in the Journal of Law and Medicine in 2011. This paper is one among many articles authored by self-proclaimed anti-circumcision crusaders. Indeed, George describes himself as the Vice President for Bioethics and Medical Science under a programme known as ‘Doctors Opposing Circumcision’ based in Seattle, Washington, D.C. As B.J. Morris and his colleagues have concluded, these anti-male circumcision crusaders “misrepresent good scientific studies, selectively cite references, some containing fallacious information; and draw erroneous conclusions” in order to reframe the male circumcision debate in their favor. The second article entitled, “Circumcision and HIV: are we being fed on half-truths?” (Daily Monitor, March 22, 2012) was written by Agnes Namaganda. Agnes questions the truth in the statement, “male circumcision reduces the risk of contracting HIV”, and presents contrasting views about male circumcision without necessarily helping the reader to reach a definite conclusion about the effect of male circumcision in HIV prevention. While she did not explicitly state which side of the debate she falls, we believe that the taste of her article hinged more on the side of those who are opposed to male circumcision, considering the nature of evidence cited. In writing this article, we intended to not only respond to these issues but also provide a more elaborate view of male circumcision and its role in HIV prevention based on scientific evidence at hand.

How the male circumcision debate begun
Male circumcision has been practiced for generations. It is one of the oldest surgical procedures known to mankind. Over time, the scientific community observed that the risk of acquiring sexually transmitted infections (STIs), including HIV, was lower in men who were circumcised than in those who were not. While nobody could clearly explain the science behind these observations, there was a general perception that male circumcision could be the reason for the observed differences.

However, since there was evidence of high HIV prevalence in some circumcising communities, it was not possible to come to a conclusion about the protective effect of male circumcision, before subjecting it to rigorous scientific scrutiny. Whereas proponents argue for increased scale-up of male circumcision programs, opponents have initiated campaigns to discredit male circumcision. But what does science tell us about male circumcision?

Some studies indicated lower HIV prevalence in circumcised men vis-à-vis uncircumcised men, but these studies had methodical challenges. For example, in many parts of Africa where circumcision was shown to be associated with low HIV prevalence in men, these areas also happened to have a high number of Muslim men. It was, therefore, not clear whether it was circumcision per se that was protective or whether it was because of other attributes already known to be associated with Muslim men (e.g. Muslim men do not drink alcohol) that reduced their risk for HIV infection. On the other hand, there are studies that have shown that circumcised men have high HIV prevalence, which, on close examination, found that most of these men were circumcised as result of having STIs. All these observations made it difficult to conclude whether male circumcision per se reduced chances of acquiring HIV among adult men.

To respond to this question, scientists designed further research studies known as randomized clinical trials. These types of studies are taken as the “gold standard” of research evidence. In these studies men who were not circumcised and who were free from HIV infection were divided into two groups with one group circumcised immediately while the other group was asked to wait for some time to receive circumcision and thus acted as the comparison group. Scientists followed both groups for a defined period of time, and tested them for HIV at regular intervals. They also provided free counseling services to all men as well as free condoms to those who were interested in using them. These trials, conducted in three countries (South Africa, Kenya and Uganda) between 2000 and 2006, involving a total of 5,411 men in the circumcised arm and 5,497 in the comparison group indicated that circumcised men were less likely to acquire HIV than those who were not circumcised. The level of protection of male circumcision from the risk of HIV infection ranged between 50 per cent to 60 per cent across the three countries. These findings, from studies conducted in different countries and communities, were so convincing that in 2007 the World Health Organisation (WHO) together with the Joint UN Programme on HIV/AIDS (Unaids) recommended male circumcision as part of a comprehensive HIV prevention strategy (alongside condom use, being faithful to one’s HIV-free sexual partner, treatment of sexually transmitted infections, among others) in ‘countries with heterosexual epidemics, high HIV and low male circumcision prevalence’, such as those found in sub-Saharan Africa.
It is important to note that the WHO guidelines refer to ‘medical’ or ‘safe’ male circumcision as opposed to the culturally performed circumcision which may be associated with other risks such as serial use of unsterilized instruments that could potentially transmit HIV. This and other cultural practices around circumcision may partly explain the high HIV prevalence among communities that perform circumcision for cultural reasons, as has been cited in some communities in Botswana and elsewhere.

Recent evidence on the impact of male circumcision at the community level
Studies done after the end of the clinical trials in Kenya and Uganda have found that male circumcision’s protective effect against HIV is sustained and may even become stronger over time. The risk of HIV infection among circumcised men was reduced by 67 per cent after 4.5 years in Kenya and by 73 per cent after 4.8 years in Uganda.
Equally exciting are recent results confirming that this level of protection can be achieved outside the relatively controlled setting of a clinical trial.

Last year, a community-based study indicated that providing male circumcision in a South African township reduced the rate of new HIV infections among circumcised men by 76 per cent in three years. In a recent paper entitled Population-level impact of male circumcision on HIV incidence: Rakai, Uganda, Ronald H. Gray and colleagues found that the number of new HIV infections among non-Muslim men decreased with greater uptake of male circumcision. Dr. Gray and his colleagues conducted an observational study among 14,000 individuals in 50 communities in Rakai District between 2000 and 2009.
Male circumcision among non-Muslim men in Rakai increased from 5.6 per cent in 2000 to 25.3 per cent in 2009. The number of new HIV infections decreased by 37 per cent during the same period among non-Muslim men. No effect on new HIV infections was seen among females in this study. This study focused on non-Muslim men because it is the practice in the Muslim community to circumcise young boys.

There are concerns expressed that male circumcision will lead to an increase in risky sexual behaviors, such as less frequent use of condoms or increased numbers of sexual partners. However, recent evidence suggests that male circumcision does not lead to increased risky behaviors.

For instance, a study done among 2,500 circumcised men who were followed up for up to five years in Rakai did not find increased risk behaviour among these men compared to uncircumcised men with respect to number of sexual partners or condom use. Other studies in Kenya and South Africa have found out that male circumcision does not result in increased risky sexual behaviors such as having sex with multiple sexual partners or abandonment of condom use.

On the contrary, circumcised men report increased safer sexual practices following risk-reduction counselling, suggesting that male circumcision programmes should incorporate risk-reduction messages into the promotional campaigns. It is interesting to note that such concerns were also voiced with the introduction of antiretroviral drugs (ARVs), but this did not stop rolling out ARVs.

Does male circumcision protect uninfected women against acquiring HIV?
Although male circumcision reduces the risk of HIV acquisition in HIV-negative men, evidence of protection for HIV-negative female partners of HIV-positive men is not conclusive. Studies carried out earlier in Uganda, particularly among HIV discordant couples (with one partner HIV-negative and the other positive), had indicated that if the HIV positive partner was circumcised, there was a reduced risk of transmission of HIV to the HIV-negative women; these studies were conducted among men who were circumcised at birth.

However, no studies had demonstrated whether the same protective effect could be seen among men circumcised as adults. A randomised clinical trial by Maria J. Wawer and her colleagues shows that female partners of HIV-positive men, circumcised as adults, may be at an increased risk of acquiring HIV if the couple resumes sex before the wound of the HIV-positive partner has healed.

It is important to note that the trend towards increased risk was seen only among women in couples who resumed sex too soon after circumcision, i.e. before proper wound healing. Gregory and George’s article, and indeed other articles from anti-male circumcision crusaders don’t mention this fact. It is crucial for couples to follow the recommendation to abstain from sex for six weeks post-circumcision (after wound heals). One can argue that logically, when fewer men are infected, transmission to women at population level would also reduce over time. Indeed, there are several studies that indicate some protective effect for women, but until such evidence is available consistently across different studies, male circumcision will continue to me promoted as a strategy for the prevention of ‘heterosexually acquired HIV infection in men’, as per the WHO recommendations. Other benefits of male circumcision beyond HIV prevention

There is overwhelming evidence to prove that male circumcision provides other benefits beyond HIV prevention. Male circumcision improves male hygiene, reduces risk of genital ulcer disease and cancer of the penis, and lowers the risk of cervical cancer among women with circumcised male partners by reducing the prevalence of the virus that is associated with this cancer (Human Papilloma Virus).

The role of male circumcision in relation to other HIV prevention approaches
We should point out that a circumcised man can still acquire or transmit HIV (if HIV-positive), except that male circumcision reduces the risk of HIV infection among initially HIV-negative, circumcised men. We should also point out that the risk of acquiring as well as transmitting HIV among circumcised men increases when sexual intercourse is resumed too early (before complete healing) or when circumcised men increase their risky behaviors due to the belief that they are protected.

This is the reason why the campaigns for male circumcision still encourage other risk reduction interventions such as abstinence, faithfulness and condom use, and advise men not to resume sex until six weeks post-circumcision (when proper wound healing has occurred). The interventions around male circumcision also include HIV testing with associated risk reduction counseling as part of the package. This is important because whereas the protective effect of acquisition of HIV by a negative man has been proven, a HIV infected man who is circumcised can still transmit infection to their uninfected partner.

Opponents of male circumcision argue that if other interventions are required in addition to circumcision then it is not beneficial. To argue that any intervention that is not 100 per cnt effective is not useful would invalidate many interventions in health (including for example several vaccines and car seat belts) and probably interventions in many other fields outside health. The realisation that no single intervention is 100 per cent effective in HIV prevention has led to the current efforts towards what is now called ‘combination prevention’ an approach that encourages the use of a comprehensive package of scientifically proven medical interventions as well as social and cultural factors that predispose women and men to HIV infection.

Policy implications
The Uganda Male Circumcision Policy (2010) recommends that “counselors should stress that male circumcision provides only partial protection against HIV, and that maintenance of other risk reduction strategies is necessary.” In addition, the National HIV Prevention Strategy indicates that “there is no single HIV prevention intervention or “magic bullet”. Thus, male circumcision is currently promoted as part of a comprehensive HIV prevention package rather than as a single magic bullet, as anti-male circumcision crusaders would like to make us believe.

The writers are lecturers at Makerere University School of Public Health, Kampala, Uganda