by ALBERT S. MAKONE | HIV/AIDS|Zimbabwe Charity, INC. (HAZ)
In sub-Saharan Africa, heterosexual transmission of HIV is the primary driver for the epidemic. At the end of 2009, 33.3 million people were living with HIV/AIDS worldwide and of these, 67.6% lived in sub-Saharan Africa. Male circumcision is one of the strategies being advocated for HIV prevention. Debates are ongoing on the protective effect of male circumcision. The current article critically evaluates the evidence for circumcision against the backdrop of arguments presented by opponents of male circumcision. The review involved the use of published texts and documents. Arguments presented by Boyle and Hill (2011) on methodological concerns, ethical and legal concerns on the male circumcision randomised controlled trials done in Kenya, Uganda and South Africa, are evaluated. Current evidence shows that medical male circumcision is efficacious in preventing HIV infection and reduced morbidity and mortality from multiple sexually transmitted infections and genital cancers in men and their female sexual partners. Male circumcision has been shown to be cost effective. The current review concludes that current evidence supports the need to accelerate the implementation of medical male circumcision programmes for HIV prevention in high HIV burden countries.
In sub-Saharan Africa, heterosexual transmission of HIV is the primary driver for the epidemic (Alistar & Brandeau, 2012). At the end of 2009, 33.3 million people were living with HIV/AIDS worldwide and of these, 67.6% lived in sub-Saharan Africa (UNAIDS & UNICEF, 2009). HIV/AIDS funding has been substantially affected by the global economic crisis with HIV prevention funds leveling off in the last decade and future funding commitments unclear. Funding constraints have created pressure on prevention programmes to be more accountable, by providing clearer evidence of cost effectiveness and delivering better value for money (Padian et al., 2011; Padian, McCoy, Balkus, & Wasserheit, 2010). Medical male circumcision is one of the prevention methods being rolled out in Africa. Male circumcision is the removal of the foreskin of the penis and it is one of the oldest, simple procedures that have been undertaken for religious, cultural, social and medical reasons (Westercamp & Bailey, 2007).
The World Health Organization (WHO) and the Joint United Nations Programme on HIV/AIDS (UNAIDS), in March 2007, recommended male circumcision as an efficacious intervention for the prevention of heterosexually acquired HIV infection in men (WHO & UNAIDS, 2007). In 2005 and 2006 randomized controlled trials in three African countries demonstrated that voluntary medical male circumcision (VMMC) reduced the risk of female–to–male sexual transmission by roughly 60% (Auvert et al., 2005; R. C. Bailey et al., 2007; R.H. Gray et al., 2007). Since 2007, both the WHO and UNAIDS have recommended that countries with generalized HIV epidemics and a low prevalence of male circumcision progressively expand access to safe voluntary medical male circumcision services (WHO & UNAIDS, 2011a). It is with this evidence that the WHO and UNAIDS identified 13 priority countries for the scale-up of VMMC: Botswana, Kenya, Lesotho, Malawi, Mozambique, Namibia, Rwanda, South Africa, Swaziland, Uganda, the United Republic of Tanzania, Zambia and Zimbabwe.
The current article critically evaluates the evidence for circumcision against the backdrop of arguments presented by opponents of male circumcision (Boyle & Hill, 2011; Chin, 2011; Conroy, 2011; Darby, 2011; Darby & Van Howe, 2011; Forbes, 2011; Green et al., 2010; Paix, 2011). The review thus tries to address a question that many a contemporary African man must be asking themselves; “To circumcise or not to circumcise?”
In conducting research for the current article, the author adopted a tertiary documentary review approach, using quantitative and qualitative approaches for the analysis of information on male circumcision. Documentary review refers to the analysis of documents that contain information about the phenomenon under study (K. Bailey, 1994). In the current case, documentary review involved the use of published texts covering the time frame addressed in the debates on male circumcision as the practice relates to HIV/AIDS (i.e. 1986 to 2012). Source materials included publications from international organizations (e.g. UNAIDS, World Bank, World Health Organization) as well as government publications, journal papers, public access databases, and other written sources in hard copy or electronic form.
Boolean search queries were conducted, which were comprised of: (HIV “OR” prevention) “AND” (HIV prevention methods) “AND” (HIV incidence) “AND” (male circumcision “OR” voluntary medical male circumcision) “AND” (circumcision “OR” effectiveness “OR” management) “AND” (sexual risk behaviour) “AND” (HIV testing “OR” operations research) “AND” (circumcision critics “OR” circumcision opposition).
The following databases were searched:
- Scientific publications such as: (AJOL, BMJ, Cochrane, EBSCO, Merck Index, MedlinePlus, PubMed, and Science Direct)
- Electronic conference proceedings of recent HIV/AIDS-related conferences up to the end of May, 2012
- Reports and publications from advocacy groups involved in HIV prevention
- Public-access search engines such as Google Scholar and Google Web (Scientific publications, UNAIDS, and WHO publications)
The articles reviewed were restricted to those published in the English language. A list of materials retrieved by the search was created and materials retrieved were reviewed, and documents were marked which included relevant information. Marked materials were then reviewed in-depth to determine and or confirm initial identified relevance. Unmarked items were then reviewed to determine their relevance and finally a list of marked materials was created in the American Psychological Association (APA) format using EndNote.
I. Methodological Concerns of the randomised controlled trials
Boyle and Hill (2011) highlighted some methodological concerns on the three randomised controlled trials (RCT) carried out in Kenya, Uganda and South Africa. They highlighted issues to do with researcher expectation bias, participant bias, inadequate double blinding, selection and sampling bias, lead-time bias and early termination. Randomized controlled trials are studies designed in such a way that the study participants are randomly (by chance alone) allocated to the different groups of a study or intervention, so as to eliminate any bias by the researchers (Jadad, 1998). Bias in research is anything that produces a systematic error, where a particular finding deviates from a ‘true’ finding. Double blinding is an experimental technique in clinical research in which neither the researcher nor the patient knows whether the intervention administered is considered inactive or active (Sibbald, 1998). The purpose of a double-blind study is to eliminate the risk of prejudgment by the participants, which could distort the results (Sibbald, 1998). RCTs constitute a working model where researchers can exercise maximum control. However, the reality in the real world is that things may be very different. The use of RCTs is limited by ethical and practical concerns.
Three RCTs in Kenya, Uganda and South Africa with comparable designs showed that male circumcision was effective against HIV acquisition. The first RCT was carried out between 2002 and 2005 in a peri-urban setting near Johannesburg, Orange Farm, in South Africa (Auvert, et al., 2005). 3,274 HIV‐negative men, aged 18-24 years, were randomized, 1,617 to immediate and 1,656 to later circumcision. After circumcision, men were advised to wait for complete healing before resuming sexual activity. During the trial, the subjects received repeated information on HIV prevention and other sexually transmitted diseases, as well as free condoms. This RCT was stopped early at 18 months after a planned interim analysis showed a significant 61% reduction in HIV risk. These results were confirmed in two trials with a similar design carried out in Kenya (R. C. Bailey, et al., 2007) and in Uganda (R.H. Gray, et al., 2007), also stopped early as evidence emerged that male circumcision provided significant benefits.
The argument that the trials of male circumcision lack external validity because of ideal counseling conditions and condom promotion is illogical because both study arms were equally exposed to those non-circumcision interventions (Lissouba et al., 2010). The concern that the effect is not durable is not supported by evidence from the Kenya trial showing that the protective effect of medical male circumcision was sustained and actually strengthened at 54 months of follow-up (Banerjee et al., 2011). The researchers of the three trials did the best they could to make the trial scientifically acceptable to other researchers since human beings are not illogical subjects without free will. In research involving humans, all studies are subject to confounding and bias. Data from the three RCTs satisfy six of the nine criteria of causality as outlined by Sir AB Hill; namely strength of association, consistency, temporality, coherence, biological plausibility and experiment.
It is worth pointing out that observational studies had already been conducted on male circumcision for up to two decades, prior to the three RCTs. A meta-analysis by Weiss and colleagues of 27 observational studies from the late 1990s showed a reduced risk in 21 studies (Weiss, Quigley, & Hayes, 2000). Evidence from observational studies have been useful to confirm the results from RCTs (Lie & Miller, 2011).
A Cochrane systematic review in 2005 assessing the quality of 37 studies of HIV and male circumcision noted that while the different methodologies showed varying results, the protective effect of male circumcision was supported consistently in all the studies (Siegfried et al., 2005). Drain and colleagues did an ecological analysis of 118 developing countries that showed that high male circumcision prevalence was strongly correlated with low HIV prevalence, independent of religion (Drain, Halperin, Hughes, Klausner, & Bailey, 2006). Gebremedhin in 2010 did a cross-sectional analysis of Demographic Health Survey (DHS) data for 18 countries across sub-Saharan Africa from 2003 to 2008 involving 70,554 males aged 15 to 59 years and the study confirmed that being uncircumcised was significantly associated with higher risk of HIV infection and the risk increases with the number of partners (Gebremedhin, 2010). Evidence from the regions where male circumcision was almost universally practiced showed no country with an adult HIV prevalence greater than 6% (Klausner et al., 2008).
Thus, the arguments from Boyle and Hill on methodological concerns do not hold much power considering the vast evidence from various studies pointing to the same direction.
II. Circumcision as a cause of HIV infection
Boyle and Hill (2011) stated that male circumcision was a possible cause of HIV transmission as it was associated with 61% increased transmission of HIV to female sex partners of circumcised HIV-infected men, as suggested by a study by Wawer and colleagues in Uganda. However, Boyle and Hill selectively quote this study, where HIV-positive men resumed sexual activities before complete wound healing (Wawer et al., 2009). Nonetheless, from a scientific point of view, the increase in transmission was not statistically significant. Indeed resuming sex too soon before wounds heal does pose a potential risk for increased HIV transmission. Hankins in 2007 showed that male circumcision conferred long-term indirect and potential direct positive impacts on women (Hankins, 2007). The indirect impact comes from lowering of HIV prevalence in men (Gwandure, 2011; UNAIDS/WHO/SACEMA Expert Group on Modelling the Impact and Cost of Male Circumcision for HIV Prevention, 2009). Weiss and colleagues carried out a meta-analysis study where they found 20% lower HIV in the female partners of HIV-positive circumcised men (Weiss, Hankins, & Dickson, 2009). Studies done in Zimbabwe and Kenya using mathematical modeling in the general population settings predicted that male circumcision would lower male-to-female HIV transmission by 46% (Hallett et al., 2011; Halperin et al., 2011).
III. Non-sexual transmission of HIV
Boyle and Hill stated that the three trials in Kenya, Uganda and South Africa did not report on non-sexual transmission of HIV, such as exposure through blood transfusions or infected needles. They thus argue that circumcision may not be as effective at decreasing HIV transmission and they quoted an article by Vines (Vines, 2006). UNAIDS has shown that HIV distribution by sex, and across age groups, is clearly consistent with sexual behavior as the main mode of transmission (UNAIDS & UNICEF, 2009; UNAIDS & WHO, 2008; WHO & UNAIDS, 2011b). The WHO and UNAIDS using modeling studies and ecological observations have shown consistent evidence for the major role of sexual intercourse in the transmission of HIV (WHO & UNAIDS, 2007, 2011b). In many sub-Saharan African countries, the role of multiple and concurrent partnerships is well documented (Halperin, et al., 2011; Klausner, et al., 2008; Masuku, Kurewa, Sisimayi, Chandiwana, & Babill-Stray, 2012; Shelton, 2009).
A UNAIDS Reference Group in 2003 developed a Modes of Transmission (MoT) approach to help country-level policy makers respond to the epidemic and prioritize interventions. The MoT approach provides a robust means for estimating patterns of adult HIV transmission through different routes (Gouws, White, Stover, & Brown, 2006). MoT analyses conducted in Kenya, Lesotho, Swaziland, Uganda and Zambia show that sexual behavior accounts for over 94% of new infections in each country (Gala´rraga, Colchero, Wamai, & Bertozzi, 2009; Wamai et al., 2011). Literature shows that non-sexual routes of HIV transmission are minor and it is important to prioritize evidence-based means of reducing heterosexual transmission, of which male circumcision is one.
IV. Contradictory Evidence
Boyle and Hill (2011) highlighted that the 60% relative reduction in HIV infections in the trials was not true. They calculated their own absolute decrease in HIV infection to be only 1.31% and quoted a study by Green and colleagues on 17 observational studies which found no relationship between male circumcision and HIV transmission (Green, et al., 2010). In 2005 and 2007, the efficacy and evidence of male circumcision was verified beyond any doubt by results from three large RCTs in Kenya, South Africa and Uganda (Auvert, et al., 2005; R. C. Bailey, et al., 2007; R.H. Gray, et al., 2007). UNAIDS and WHO accepted the results and the Cochrane committee concluded that male circumcision for HIV prevention was supported and there were no further trials needed (Siegfried et al., 2009; UNAIDS & UNICEF, 2009; UNAIDS & WHO, 2008; WHO & UNAIDS, 2007, 2011a). In 2010, Padian and colleagues conducted a systematic review of 37 late-phase RCTs of various HIV prevention interventions and found that male circumcision had a stronger efficacy in preventing HIV infection than microbicides and treatment of STIs (Padian, et al., 2010).
Male circumcision has been shown to be protective against other sexually transmitted infections (STIs), such as herpes simplex virus-2 (HSV-2) (A. A. Tobian et al., 2009; A. A. R. Tobian, Gray, & Quinn, 2010), human papillomavirus (HPV) (R. Gray et al., 2012; R. H. Gray et al., 2010; Wawer et al., 2011), and genital ulcer disease (R.H. Gray et al., 2009), and is associated with a reduction in the risk of genital cancers among both men and women (Mosconi, Roila, Gatta, & Theodore, 2005).
Several studies have been done on the biological mechanism of male circumcision in mitigating HIV infection. The foreskin contains a high density of Langerhans / dendritic cells and CD4/CD8 T lymphocytes, all target cells for HIV (Ganor & Bomsel, 2011; Morris, 2007; Szabo & Short, 2000). By reducing the surface of the foreskin, male circumcision reduces the number of these target cells.
V. Ethical and Legal Arguments
Lack of fully informed consent and participant inducement are the ethical issues raised by Boyle and Hill (2011) in their paper criticizing male circumcision. The example quoted by Boyle and Hill, of Ugandan men who thought that by getting circumcised they would not catch HIV, is not strong enough to denounce three clinical trials. Boyle and Hill also argue that participants of the trials were paid and this might have induced them to participate. It should be noted that the participants were not paid but they received compensation for their participation.
As is often the case with many new medical interventions, male circumcision faces a number of criticisms in its implementation in sub-Saharan Africa, some of which have been highlighted above. Incidence of HIV is now declining in many sub-Saharan African countries. However, nearly 70% of new HIV infections globally, are still within this region (WHO & UNAIDS, 2011b). Current evidence from RCTs shows that in comparison to a protective effect of 31.2% for a vaccine, 39% for microbicides, and 46% for prophylaxis, male circumcision has a 60% efficacy (Auvert, et al., 2005; R. C. Bailey, et al., 2007; Brooks et al., 2010; R.H. Gray, et al., 2007; Sawires et al., 2007; Williams et al., 2006). Male circumcision has been shown to reduce urinary tract infections in infants and children, ulcerative sexually transmitted infections (STIs), human papilloma virus, which causes cervical cancer in women, and bacterial vaginosis and trichomonas in the female partners of circumcised men (R.H. Gray, et al., 2009; Wawer, et al., 2011).
UNAIDS in 2011 determined that scale-up of voluntary medical male circumcision in appropriate settings constitutes a high-impact intervention with excellent value for money (Njeuhmeli et al., 2011). Male circumcision has been shown to be cost effective as male circumcision scale up to 80% coverage will avert 3.4 million, or 22%, of new HIV infections through 2025 and will result in net savings amounting to US$16.5 billion due to treatment and care costs averted (Kahn, Marseille, & Auvert, 2006; WHO, March 2012).
So why not invest in this cost effective method of HIV prevention? Male circumcision opponents misrepresent credible research, and cite questionable websites, outlier studies, and non-peer-reviewed book chapters (Conroy, 2011; Garenne, 2006; Morris et al., 2006; Schoen, Oehrli, Colby, & Machin, 2000). The current review of the evidence for VMMC in the backdrop of the arguments presented by opponents of VMMC leaves this author with no choice but to recommend male circumcision as a way of reducing the transmission of HIV. The demonstrated benefits far outweigh the arguments presented by the critics of male circumcision.
The Political Declaration on HIV/AIDS, adopted at the June 2011 High Level Meeting on HIV/AIDS at the United Nations General Assembly, reiterates the insistence of Member States that “prevention must constitute the cornerstone of the global HIV and AIDS response” and specifically pledges to “promote medical MC where HIV prevalence is high and male circumcision rates are low” (WHO & UNAIDS, 2011a). To date, the evidence presented shows that if male circumcision is performed by a qualified practitioner under acceptable conditions of hygiene in the absence of contra-indications, far greater good results than harm.
Opponents of male circumcision question the intervention’s efficacy, and following the recent release of the 2010-2011 Zimbabwe Health Demographic Survey, their opposition to the intervention is likely to be bolstered. Data from the recent survey indicates that 14 percent of circumcised men in the country between the ages of 15 and 49 contracted HIV, when compared to uncircumcised men. There are various explanations that can explain why the HIV infection percentage was high amongst circumcised men.
One possibility is that the circumcised men resumed sex before their surgical wounds had completely healed. As previously explained in the current review, resuming sexual activities too prior to complete healing of the surgical wounds poses a potential risk as was seen in the study in Rakai, Uganda, by Wawer and colleagues in 2009 (Wawer, et al., 2009). The role of multiple and concurrent partnerships is well documented in many sub-Saharan Africa countries and this is also a key driver in the spread of HIV infection (Halperin, et al., 2011; Shelton, 2009; Wamai, et al., 2011).
It should be pointed out that the Demographic Health Survey (DHS) data has previously been called into question due to inherent methodological designs that impact on the interpretation of the data (Gala´rraga, et al., 2009; Gersovitz, 2005; Wamai, et al., 2011). DHS data are often bidirectional, indicating contrasting and context-specific effects (Wamai, et al., 2011). There is need to better understand the context of the subjects who took part in the survey, in view of similar findings which were once reported in Tanzania in 2005 (TACAIDS, 2005). In the Tanzania survey, HIV infections were also high among circumcised men, who also happened to be highly educated and had high incomes (TACAIDS, 2005). The men in this context were found to engage in higher risk behaviour of, such as having multiple concurrent sex partners, than were circumcised men of lower educational background and income (Klausner, et al., 2008; Shelton, 2009).
Multiple factors thus need to be examined when evaluating the relationship between male circumcision and HIV prevalence, particularly in a case such as in this with, DHS surveys that involve self-reported data. Such factors may include risky sexual behaviour, time of male circumcision, marital status, education, wealth and patterns of residence (i.e. urban vs rural) (Wamai, et al., 2011). As has been pointed out previously, evidence from regions where male circumcision is almost universal show no country with an adult HIV prevalence greater than 6% (Klausner, et al., 2008).
Although male circumcision is efficacious in reducing the risk of HIV infection for men, care must be taken to ensure that men and women understand that the procedure does not provide 100% protection against HIV infection. Male circumcision must be considered as just one element of a comprehensive HIV prevention package that includes delaying the onset of sexual relations (after surgery), correct and consistent use of condoms, reductions in the number of sexual partners, and testing and counselling to know one’s HIV serostatus (UNAIDS & WHO, 2008; WHO & UNAIDS, 2007).
The author recommends policy makers to urgently facilitate implementation of male circumcision as a public health measure to stop the growing heterosexual transmission of HIV in sub-Saharan Africa and globally. Male circumcision is highly efficacious against STIs and HIV acquisition and it also confers other multiple health benefits (Wamai, et al., 2011). It is time to mobilize sufficient resources to provide safe and widespread medical male circumcision in high HIV burden countries.
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- To circumcise or not to circumcise: That is the question. - July 20, 2012