Circumcision as a Strategy to Minimize HIV Transmission
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- Rosario, I.J., Kasabwala, K. & Sadeghi-Nejad, H. Curr Urol Rep (2013) 14: 285. doi:10.1007/s11934-013-0343-8
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The newest data related to the Human Immunodeficiency Virus (HIV) / Acquired Immune Disease Syndrome (AIDS) epidemic is primarily positive, but many areas of the world, especially Sub-Saharan Africa, remain disproportionately affected. Between 2005 and 2007, three large randomized trials evaluating circumcision for prevention of HIV acquisition in heterosexual African males showed a reduction in the rate of acquisition of HIV by up to 66 % over 24 months. Since the results of these studies were published, global health organizations have ramped up efforts to help target countries to provide male circumcision delivery services in sub-Saharan Africa. Male circumcision (MC) is cost-effective and efficacious, especially when used in combination with other prevention strategies. Available data shows good acceptability amongst target populations. Neonatal circumcision is well tolerated and more cost effective than adult male circumcision and should be included as part of MC initiatives in the future. Behavioral disinhibition and risk compensation are important factors that may mitigate the rate of risk reduction conferred by male circumcision and should be further investigated. As delivery of male circumcision services is expanded, the issues affecting the female sexual partners of the target population must be outlined and addressed. Whether or not the results of the African trials can be extrapolated to warrant expansion of MC programs to other populations is a critical area for further study.
KeywordsHIV/AIDSCircumcisionSexually transmitted infectionSub-Suharan AfricaEpidemic
Medical male circumcision
Joint United Nations Program on HIV/AIDS
World Health Organization
Centers for Disease Control
Human Immunodeficiency Virus
Acquired Immune Disease Syndrome
Treatment as Prevention
Sexually Transmitted Infection
Introduction - The Status of the Epidemic
In the past decade, the fight against HIV/AIDS has been characterized by a concerted, multi-national effort to work toward ending the AIDS epidemic. In 2011, as part of this global effort, the United Nations issued a formal political declaration on HIV and AIDS [1, 2, 3••]. Member states were asked to pledge their commitment to take specific steps toward to intensifying their efforts to eliminate HIV/AIDS, and were given a list of task-related goals to be met by 2015 [1, 2, 3••]. Countries were also asked to monitor and document their progress in a biennial report, which was to be analyzed by Joint United Nations Program on HIV/AIDS (UNAIDS) . Of the 193 member countries, 96 % reported in 2012, providing for a comprehensive evaluation of the state of the global HIV/ AIDS Epidemic [1, 2, 3••].
Due in large part to this tremendous international effort toward ending the epidemic, the newest data related to HIV/AIDS across the world is primarily positive. Globally, the number of new HIV infections has declined steadily in the past 15 years, and the number of people newly infected in 2011 was 20 % lower than that in 2001 [3••]. In addition, the number of people dying from AIDS and AIDS-related causes has declined steadily since the mid 2000s, due primarily to the increased availability of anti-retroviral therapy, as well as decreased incidence of infection. The number of children acquiring and dying from HIV related infection has also declined steadily [3••]. The UNAIDS global report from 2010 reported a 24 % decrease in the number of children newly infected with HIV from 2004, as well as a decrease in the total number of children being born with HIV, as access to services for preventing peri-natal transmission have increased .
Despite these trends in the positive direction, the HIV/AIDS problem remains a global epidemic, with 34 million people living with HIV worldwide. This represents 0.8 % of adults aged 15–49 years. The degree to which countries are affected by the epidemic varies significantly, with sub-Saharan Africa being the most adversely affected. As of 2011, one in 20 adults in this region was infected, representing 69 % of the total population of HIV victims worldwide [3••]. Other areas disproportionately affected include the Caribbean, Eastern Europe, and Southern Asia, where approximately 1 % of adults are affected [3••]. According to the Centers for Disease Control and Prevention (CDC), 1.1 million people in the United States age 13 and over are living with HIV . It is estimated that over 200,000 of them do not know they are infected. Incidence in the United States has remained stable for several years .
HIV/AIDS and Circumcision
For several decades after HIV was first identified and diagnosed, observational data suggested that circumcised men were less likely to be infected with HIV through heterosexual sex. There are several characteristics of the penile foreskin thought to be responsible for this phenomenon, including degree of tissue keratinization, increased density and superficial location of HIV target cells (Langerhans cells), alteration of the penile microenvironment, direct effects on HIV-transmission cofactor sexually transmitted diseases, and intercourse-related trauma .
Between 2005 and 2007, the results of three landmark randomized trials evaluating circumcision for reduction in rates of HIV acquisition in heterosexual African males were published. Studies were conducted between 2002 and 2006 in South Africa, Kenya and Uganda [8••, 9••, 10••]. All three trials were stopped early due to very compelling findings upon interim analysis. These studies provided strong evidence that circumcision reduces the acquisition of HIV by adult male heterosexuals by up to 66 % over 24 months. Importantly, adverse outcomes were uncommon in all three trials .
The irrefutable evidence provided by the trials led both the World Health Organization (WHO) and UNAIDS in 2007 to recommend voluntary adult male circumcision in areas where rates of HIV infection are high and prevalence of circumcision is low [3••]. Because sub-Saharan Africa represents the region of the world bearing most of the burden of the epidemic, this region became the area of initial focus. Since efficacy has been established and associated costs are estimated to be relatively low, adult male circumcision has become an integral component of HIV/AIDS prevention initiatives in the global arena, with special initial attention being paid to sub-Saharan Africa. Accordingly, this review will focus primarily on the role of circumcision in HIV infection in African men, with some discussion of whether or not the data can be extrapolated to other populations.
On a national level, in 2010, the American Urological Association Male Circumcision Task Force led by Dr. Ira Sharlip was formed with the goal of collaboration with the WHO and the U.S. President's Emergency Plan for AIDS Relief (PEPFAR) to help ramp-up male circumcision services in sub-Saharan Africa. One of the co-authors of this manuscript (HS) participated in this newly established task force. Volunteer board eligible/board certified urologists were recruited for training and were assigned to provide MC services in various Sub-Saharan African nations. Another co-author (IJ) participated in the program and provided circumcision services in Mhlume, Swaziland.
According to the 2012 UNAIDS global report, a rapid scale-up of voluntary male circumcision programs in Eastern and Southern Africa could potentially prevent one in five of people who would have otherwise become HIV positive from doing so through the year 2025 [3••, 12]. To date, most countries for which voluntary male circumcision is recommended have endorsed the program, adopted necessary processes and begun the training of health care workers necessary to begin implementation [3••]. In addition, each country has identified a target total number of circumcisions to be performed by 2015.
As of December 2011, the Nyanza Province of Kenya had reached 54 % of the target number, followed by Ethiopia and Swaziland, which each achieved more than 20 % of their respective goals. Ethiopia and Swaziland have also gone as far as to include male circumcision into early infant care programs [3••]. Other nations have also begun programs, but have made much slower, and often almost negligible, progress [3••].
Neonatal circumcision is generally considered to be better tolerated, more simple to perform and more cost-effective than adult male circumcision. This may be the best focus for future generations: better tolerated, easier, and more cost effective . The American Academy of Pediatrics issued a statement regarding neonatal circumcision in 2012. According to this statement, the preventative health benefits of newborn male circumcision outweigh the risks. These benefits include decreased risk of UTI in first year, decreased heterosexual acquisition after sexual debut, and decreased rates of other sexually transmitted infection (STIs) . Though there was no recommendation made for routine circumcision of all male newborns, the statement reports sufficient evidence to justify access to the procedure for families who want it, as well as third party payer coverage for circumcision . The overall risk of complications associated with newborn circumcision is low and most complications are minor. There is also a lower complication rate than when the procedure is performed later in life . Based on these advantages, it may be beneficial to include emphasis on neonatal circumcision as a standard part of MC initiatives in Africa and ultimately, worldwide.
The acceptability of newborn circumcision among parents from traditionally non-circumcising cultures will become more of an important factor as the focus shifts from adult male circumcision toward circumcision of babies . Mavhu et al. performed a qualitative analysis of willingness of parents in Zimbabwe to accept neonatal circumcision. They held group discussions involving parents, pediatricians, and traditional leaders. Discussions were recorded, transcribed, and analyzed using grounded theory principals. Overall acceptability was found to be high, though knowledge of the procedure was limited amongst participants. In addition, several cultural factors were found to influence the participants’ receptivity to the procedure. For example, elder male participants were concerned about the resultant separation of circumcision from adolescent male initiation rituals. Others expressed concern that responsibility for nursing the wound would fall to the mothers. This is traditionally considered taboo in some ethnic groups .
Future efforts toward increasing rates of newborn circumcision in populations where it would be most beneficial will require identification and management of the culture specific beliefs, practices and rituals that may discourage parents from choosing to circumcise their newborns.
Behavioral Disinhibition/Risk Compensation
The rate of risk reduction conferred by male circumcision can be mitigated by multiple factors. One of these factors is the concept of post-circumcision risk compensation, also described as behavioral disinhibition [7, 15]. This occurs when men who have been circumcised engage in more risky behavior (i.e. earlier sexual debut, increased number of partners, reduced use of condoms) due to perceived reduction in their HIV risk. In the three landmark male circumcision efficacy trials, evidence related to risk compensation was inconclusive [1, 2, 3••, 16]. Data from subsequent studies was also inconsistent . Most recently, Grund et al. conducted a small, qualitative study of MC patients in Swaziland. In contrast to previous studies, this group did show a slight increase in behavioral disinhibition following the procedure. The authors believe that their qualitative approach “allows for a more comprehensive examination of men’s behavior change after circumcision,” and may therefore be a more accurate reflection of the actual incidence of behavioral disinhibition . Because risk compensation has the possible effect of either negating, or at least mitigating, the positive effects of MC, we believe that this is an important area of further study.
Transmission to Female Partners
At the population level, there is a clear benefit of MC as related to female HIV infection [7, 17]. Reduction in HIV prevalence amongst men should result in a decrease in the number of women becoming infected via heterosexual sex . To date, the only data available has been gleaned from a meta-analysis of prospective observational studies conducted by Weiss et al. [7, 18]. This meta-analysis also included data from the only RCCT available [7, 19]. Strong evidence of a direct protective effect of MC on women was not found in this study.
Another issue related to transmission of HIV to female partners, as it pertains to MC, is the resumption of sexual intercourse prior to healing of the surgical wound. MC programs circumcise men regardless of HIV status, though testing is routinely encouraged. There is therefore a potential increased risk of transmission to a female partner if the circumcision patient is HIV positive, and conversely from female to male, in the case of early resumption of sexual activity during the postoperative healing period.
In many African countries, female sex workers have historically played a major role in HIV transmission . Early studies showed that a very significant proportion of new infections amongst men resulted from encounters with female sex workers . Though in the most recent few years this population has played a lesser role in progression of the epidemic, it still remains an important area of concern. This is especially true in countries like Zambia, where 26 % of males have had sexual encounters with sex workers .
Abbott et al. conducted a small interview based study of female sex workers in Zambia “to examine their understanding of MC and experiences with circumcised clients”. Subjects reported alarming situations, such as having sex with very recently circumcised clients and men using the fact that they are circumcised to encourage sex without condoms. The authors suggested that female sex workers, already at higher risk, may be more likely to engage in higher risk behavior as a result of MC . They believe that as MC services become increasingly available, programs should include education related to the limits of the protective effect of MC.
It is our strong belief that further efforts should also be aimed at empowering sex-workers, and all women, in ways that will promote sexual health and sexual autonomy. If incorrect ideas related to the degree of protection provided are allowed to persist, expansion of MC programs may have the untoward effect of further limiting women’s sexual negotiating power . This is especially important in African and other nations where women are disenfranchised and subjected to culturally condoned or ignored domestic and other forms of gender-based violence. The insistence on unprotected sex is a form of gender-based violence that is often not recognized as such .
The Economics of Male Circumcision
As with any global health issue, the economics associated with the recent scale-up of MC services are an area of concern and discussion. In 2011, results of The HIV Prevention Trials Network (HPTN) 052 Study were published in the New England Journal of Medicine (NEJM) [21••]. The trial enrolled 1,700 sero-discordant couples from Africa, Asia, Latin America and the United States. Only HIV positive patients with CD4 count between 350 and 550 were included, as they are not eligible for treatment of their own disease based on WHO guidelines. The results showed very strong evidence that early initiation of antiretroviral therapy (ART) reduces HIV transmission by 96 % in HIV sero-discordant couples. The strength of the evidence was of a degree to prompt early termination of the trial [21••].
This concept of “treatment as prevention” (TasP) was described by Michel Sidibé, Executive Director UNAIDS in a May 2011 UNAIDS/WHO press release as “a serious game changer” that “will drive the prevention revolution forward [22•]. It makes HIV treatment a new priority prevention option”.
At present, it remains unclear as to how TasP would be funded given the current status of funding initiatives for global HIV/AIDs programs. Barninghausen et al. sought to compare the relative costs of prevention with ART vs. MC with ART at CD4 < 350. They developed a new mathematical model to determine whether benefits comparable to TasP could be obtained through using combinations of MC and ART. This group found that TasP costs $8,375 per infection averted and $7,739 per death averted. MMC outperforms ART significantly in cost per infection averted ($1,096 vs. $6,790) and performs comparably in cost per death averted [22•]. Their data showed that high MC coverage combined with high ART coverage would provide comparable reduction in HIV incidence at a cost 5 billion dollars lower than that of TasP over the 11-year period between 2009 and 2020 [22•]. They recommend that much higher priority be given to MC scale-up in tandem with ART scale-up vs. treatment as prevention with ART.
In addition to being cost effective, MC used in combination with other prevention strategies may also provide a better risk reduction outcome. All known and currently used strategies, including MC, when used independently, only partially reduce HIV risk . HIV prevention strategies, including HIV testing, male circumcision, and ART can have a greater impact on reducing HIV incidence in African countries when combined . Allsallaq and colleagues mathematically modeled a combination prevention strategy calibrated to data from the KwaZulu-Natal province in South Africa where HIV prevalence is 23 %. This study found that compared to the current strategy of prevention using either testing, circumcision or ART, a combined strategy would reduce HIV incidence by 47 % within 4 years, and by almost 60 % after 25 years .
Attitudes Toward MC
Data regarding attitudes toward and acceptability of circumcision as a means of decreasing risk of HIV has primarily been obtained prior to the 2007 endorsement of the program by the WHO and roll-out and up-scaling of male circumcision programs. Overall acceptability was found to be generally positive. Two more recent studies evaluated attitudes and behaviors closer to the initiation and soon after the event, as initial education endeavors were being undertaken and when more definitive evidence related to efficacy was available.
Andersson and Crockroft evaluated prevalence of and attitudes toward MC in Botswana, Namibia, and Swaziland immediately before, or at the very beginning of, initial roll-out of MC programs via a survey conducted in 2008 . They interviewed 2,915 men and 4,549 women. Almost half of uncircumcised men reported planning to have MC, and almost half of young women with uncircumcised partners reported planning to request that their sexual partners be circumcised . Unfortunately, it was discovered that many of the participants held beliefs that were incorrect, and possibly even dangerous, with potential risk compensation as a consequence. Thirteen percent of young men and 10 % of young women mistakenly believed that MC provided complete protection against HIV . This was more common amongst less educated participants. Eighteen percent of respondents thought HIV positive men could not transmit the virus after circumcision, and almost 25 % believed that testing for HIV was not necessary prior to circumcision . One in five men and one in six women respondents thought it was “okay for a circumcised man to expect sex without a condom” . This was an even more common finding amongst participants from Swaziland, where one third of men and a quarter of women held this belief .
As part of the initial roll-out of MC programs, it is essential that communities be educated about the limits of protection provided by MC. Additional focus must be placed on empowering women to protect themselves and to make appropriate sexual choices related to male circumcision.
Westercamp et al. evaluated circumcision preference among women and uncircumcised men in the 2 years after release of the trial data and immediately before initial role-out of the voluntary MC programs. The study was undertaken as the first part in a series of studies designed to assess the changes over time in knowledge and beliefs related to circumcision, as well as to assess associated sexual risk behaviors and HIV prevalence . They enrolled 2,563 male and female participants between the ages of 15 and 49. Identical surveys were given to both groups and then compared between the groups. The majority of women and men (65 % and 68 %) respectively believed that a circumcised man is less likely to become infected with HIV . Statistically significant differences between men and women were noted in reporting the belief that condom usage is less necessary after MC, with women being more likely to believe they are less necessary, but equal numbers of men and women said they were likely to engage in sex without condoms now that MC is available . 99 % of study participants believed circumcision to be a safe procedure; 60 % of men reported that they would be prefer to be circumcised and 76 % of women reported a preference for circumcised partners . Barriers to acceptance of circumcision included a belief that circumcision is not part of their culture, length of recovery and “no specific reason”.
The results of the above two studies correspond with previous findings. Though the level of acceptance has remained unchanged, the reasons have differed. In earlier studies, concerns related to cost and fear of pain were more predictive of preference, with less influence from perceived protection from STI/HIV .
Extrapolation to Other Populations
Though it is abundantly clear that medical male circumcision for HIV prevention has irrefutable efficacy in the sub-Saharan African regions, the question remains as to the ability to extrapolate these results to other populations . Simply by virtue of the fact that they are different populations, other cultures and nations show significant differences in how they are affected by the HIV/AIDS epidemic. This is most simply and clearly evidenced by the fact that the prevalence of HIV/AIDS is so much higher in sub-Saharan Africa than in other parts of the world. The HIV/AIDS problem outside of sub-Saharan Africa is differentiated by alternate modes of transmission and different at risk populations, as well as varying prevalence of other contributing STDs and markedly discordant contributory socio-cultural factors . Circumcision is likely to be protective, but there will be differences in how much protection is conferred . A prime example and a population worthy of further study is the African-American population in the United States.
African Americans continue to be disproportionately affected by HIV in the United States. In 2010, they represented 12 % of the US population, but accounted for approximately 44 % of all new HIV infections [5, 6]. By CDC estimates, if current trends continue, at some point in their lifetime, one in 16 black men and one in 32 black women will be diagnosed with HIV infection . Very importantly, African Americans are noted to have lower access to neonatal circumcision services and lower overall rates of circumcision. As a population with high incidence of HIV and low rates of circumcision, the African American cohort meets the WHO/UNAIDS criteria for a potential target population of MC services. We believe it to be critical that further study related to MC and HIV be undertaken to address the specific needs and characteristics of this vulnerable population.
MC is an important tool in the global fight against the HIV/AIDS epidemic. It is efficacious, cost-effective, and should be used in conjunction with other proven preventative strategies to provide the most benefit to currently targeted populations. There are several issues related to MC and HIV/AIDS prevention that require further investigation and should be elucidated in order to enhance delivery of services to currently targeted groups, and moving forward, other significantly affected groups. Finally, there are special concerns related to the female sexual partners of high-risk males that must be addressed as part of future endeavors. As specialists in the area of male reproductive and sexual health, urologists must remain informed about all of these very important issues.
Compliance with Ethics Guidelines
Conflict of Interest
Dr. Imani Jackson Rosario reported no potential conflicts of interest relevant to this article.
Dr. Khushabu Kasabwala reported no potential conflicts of interest relevant to this article.
Dr. Hossein Sadeghi-Nejad reported no potential conflicts of interest relevant to this article.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.