The Kindest Cut: Proof that Male Circumcision Is Cost-Effective Against Transmission of HIV Brings New Hope for Sub-Saharan Africa

by Beryl Lieff Benderly

Beryl Lieff Benderly is a prize-winning Washington journalist and author specializing in health, behavior, and science policy. Her articles appear in major magazines and on the Internet, and she is a regular contributor to the Science magazine website. Her eight books include In Her Own Right: The IOM Guide to Women's Health Issues.

Riots and near-riots are commonplaces of news coverage, with causes ranging from disputed elections and food shortages to disappointing sports scores.  But the stampede of angry residents on Mbabane, Swaziland, in February 2006, sprang from an unusual grievance.  The men who came close to violence outside a clinic in the African nation’s capital city were outraged because they couldn’t get appointments to be circumcised.

An angry crowd of citizens demanding a painful surgical operation that has long had important religious and cultural overtones may seem an unlikely reason for civil unrest.   But the men, who live in a country where one-third of  adults are HIV positive,¹ were responding to an even more remarkable news event—the first scientific results conclusively demonstrating that “male circumcision [MC] provides a degree of protection against acquiring HIV infection,” in the words of a team of French and South African researchers sponsored by the French National Agency for Research on AIDS.²  A clinical trial they had done in South Africa found that circumcised men have a 60% lower chance of becoming infected with the virus through heterosexual intercourse than uncircumcised counterparts.  The media quickly spread the word and the demand for the surgery, which until then was not widely practiced in Swaziland, overwhelmed health care facilities.

The disgruntled men of Mbabane are not the only ones excited about the possibility of obtaining a significant level of permanent HIV protection through a one-time, relatively inexpensive outpatient procedure. Scientists and public health experts have hailed the result as a major and very timely breakthrough in AIDS protection, especially since efforts to create an effective vaccine have not succeeded.  They see MC as a potentially powerful new tool in the struggle against HIV in Africa, the continent hardest hit by the epidemic.  But, many experts warn, turning the finding into programs that benefit the people of poor countries heavily affected by HIV presents significant technical, administrative, ethical, and cultural challenges.

Compelling Evidence

“The research evidence that male circumcision is efficacious in reducing sexual transmission of HIV from women to men is compelling,” announced a World Health Organization/UNAIDS Technical Consultation in March 2007.³  MC is “at least as effective, for heterosexual transmission, as the-long-hoped for AIDS vaccine,” according to Jeffrey Klausner of the Harvard School of Public Health and colleagues.⁴  Some experts even call it a “surgical vaccine” because of the level of protection it offers.⁵  A cost-benefit analysis based on the South African clinical trial data found MC “amongst the most economically efficient HIV prevention strategies in Sub-Saharan Africa,” stated James Kahn of University of California-San Francisco and colleagues.⁶ 

Since publication of the South African trial in October 2005, two other trials, one done in Kenya and the other in Uganda, have resoundingly confirmed its conclusion.  Results in both trials were so convincing that the United States National Institutes of Health stopped them early. 

Even before these studies established MC’s efficacy beyond dispute, “evidence suggesting that male circumcision decreases the risk of acquiring…HIV [was] strong,” according to Disease Control Priorities in Developing Countries, 2nd edition, one of the three 2006 publications of the Disease Control Priorities Project.  Muslim countries, for example, where nearly all men are circumcised in childhood, have low HIV rates.  Observers have also long noted that circumcised men are less likely to acquire genital herpes, syphilis, gonorrhea, and several other sexually transmitted diseases, some of which are known to facilitate infection by HIV.⁷

Low-Risk Surgery

Circumcision, from the Latin for “cutting around,” is a surgical operation that in males removes the foreskin, a sleeve of tissue that covers the tip of the flaccid penis and retracts during erection.  In the hands of an experienced operator, the procedure can be performed quickly on an outpatient basis using local anesthesia.  Properly done in sanitary conditions, it carries a low risk of complications, which can include infection, swelling, excessive bleeding, and pain. In the South African trial, for example, the 1,568 adult men who underwent MC by general practitioner physicians in their offices experienced a total of 60 surgery-related adverse events—nearly all of them minor--within a month of the operation.  One additional doctor visit resolved all but two of these cases.⁸  When done in infancy, MC carries even lower risk.  Complete healing takes about six weeks, during which time the patient must avoid sexual activity, which would greatly raise the risk of infection, including with HIV.  A trial performed in Uganda and published in January 2008 found that, after the wound had healed, MC had no effect on sexual function or desire.⁹

Researchers believe that MC lowers risk of HIV infection by closing off a route the virus can use to enter the body.   The foreskin’s inner surface consists of tissue that contains large numbers of cells, especially of a type known as Langerhans’ cells, that are particularly susceptible to HIV.  In addition, that inner surface lacks the protective layer of tissue containing a substance known as keratin that shields the tip and shaft of the penis from entry of the virus.  Langerhans’ cells form part of the immune system’s early warning system.  Their role is presenting to the T cells in the lymph nodes the antigens (foreign bodies including viruses) that they encounter. Attacking a particular type of T cell, the T-4, is a crucial step in HIV’s invasion of the body.

The Langerhans’ cells on the foreskin’s inner surface  “will be the first to come in contact with HIV…from the man’s infected partner,” according to Scott McCoombe and Roger Short of the University of Melbourne, who studied the location of HIV-susceptible cells and the levels of keratin in the penis.¹⁰  “This primary infection is most likely to occur when [as on the inner surface of the foreskin,] there is little or no protective layer” of keratin, they state.  In addition, after intercourse, the space between the foreskin and the shaft of the penis may also provide an environment favorable to the viruses’ survival “and thus increase transmission in uncircumcised men,” they add. After circumcision removes the susceptible foreskin tissue, however, the “thickly keratinized” layer of tissue on the remaining shaft and tip of the penis interferes with the entry of HIV.

High Cost-Effectiveness

MC is not only effective in protecting against HIV infection, but is also very cost-effective, according to an analysis of the South African trial data by James Kahn and Elliot Marseille of the University of California-San Francisco and Bertran Auvert of the French National Institute of Health and Medical Research based on data from the South African trial. MC, they found, can produce large savings in both dollars and DALYs, or disability-adjusted life years.¹¹  (The DALY is a metric of illness or health used in comparisons of the cost effectiveness of interventions; see box). MC is not an expensive operation to perform in the South African context--an estimated US$560 per person as part of a hypothetical program providing a package of services that includes clinic-based surgeries, counseling, community publicity, and follow-up care for the small number of complications.  The savings in both suffering and expense that each procedure could produce are enormous.  

In a region with an HIV infection rate of about 25 percent and a program that would circumcise all eligible men, the authors estimate that each 1,000 circumcisions would prevent 308 adult infections over 20 years (a total of 427 infections averted, discounted to the present at 3 percent), with a cost of $181 per infection averted and overall savings of more than US$2.4 million in medical expenses and 4,600 DALYs averted.  Where infection rates are lower, the cost per infection and DALY averted would rise, but the procedure still remains a very good buy.  Cost effectiveness rises when boys are circumcised before they become sexually active.

MC thus compares quite favorably in cost effectiveness to other accepted HIV prevention strategies, the researchers note.  Condom distribution costs $10 to $2,188 per infection averted, depending on the circumstances; voluntary counseling and testing cost $398 to $482; and anti-retroviral drugs to prevent transmission from mother to infant cost $20 to $2,198.

MC provides no direct protection from HIV to men’s female sexual partners.  A portion of the averted infections in the cost-effectiveness analysis nonetheless represent women who were not exposed to HIV during sex with circumcised men who had escaped infection because of MC.  These women would also not transmit the virus to their infants. A high level of MC in a country, the researchers note, thus protects the population at large, not just the men who undergo the operation.  In the next 20 years, MC could prevent 5.7 million people of both sexes in Africa from contracting HIV and 3 million from dying, according to a mathematical model developed by Brian Williams of the World Health Organization and co-authors. “MC is equivalent to an intervention, such as a vaccine or increased condom use, that reduces transmission in both directions by 37%,” they write.¹²

Significant Challenges

The high though incomplete level of protection that MC offers opens up a new and dangerous risk, however,—and one that may explain “the long circumcision lines in front of the health centres,” according to David Gusongoirye, editor of the New Times newspaper in Kigali, the capital of Rwanda.¹³  In a front-page article he reported a conversation with a young man recovering from a recent circumcision. “These AIDS people have spoken for long about fighting the disease, but they had never come up with a practical solution as good as this one,” the young man said.  “Don’t have sex, don’t do this, don’t do that. Eh, man, how can a young man such as I forfeit sex, eh? And the condoms – where is the sense in putting on a condom when you are having sex? Sex is about feeling, and so no young person likes them!”

Despite having a “good education,” Gusongoirye noted, this young man seemed not to have grasped the crucial facts that circumcision only reduces, but does not remove, the threat of contracting HIV and that other measures, such as condoms and sexual fidelity, remain necessary. If circumcision programs do not correct this “appalling” misapprehension, “whatever sensitisation that had been done about ways of protecting oneself against HIV infection were going to be thrown to the wind, because circumcision would now provide full coverage!” Gusongoirye warned.

The danger that circumcision will bestow a false sense of safety to risky sexual practices, experts note, is only one of the significant challenges that health authorities must overcome as they roll out programs that use MC to help staunch the spread of HIV in Africa.  Another important one is fitting the procedure into the social and cultural context of each country.   MC is rare in some areas of Africa but widely practiced in others, where it forms part of the traditional practices of numerous ethnic and tribal groups, generally as an element of ceremonies associated with initiation into manhood or adult status in the community.  MC is also a basic element of Islam, which has many adherents in Africa, as well as of Judaism, which is practiced by small numbers in Africa. 

The specific rituals, customs, beliefs, and symbolism surrounding MC in different groups vary considerably, but in traditional tribal and religious contexts it nearly always carries significant symbolic, spiritual, and social implications for the individuals who undergo it. Ritual circumcisions are often performed by traditional circumcisers who lack formal medical training and the techniques and sanitary conditions during surgery and wound healing can vary widely.  Public health programs that seek to incorporate traditional circumcisers and circumcision practices into HIV prevention campaigns therefore face issues of evaluating and certifying the fitness of traditional practitioners and practices. 

Introducing MC into HIV prevention programs also raises complex ethical and legal issues involving accessibility, confidentiality, informed consent, and other considerations, according to the UNAIDS Secretariat.¹⁴  Especially crucial, it states in a report, is clearly differentiating MC from the practice of ritual female genital mutilation, which is sometimes called female circumcision, but has “drastically different” health consequences. The exact procedures used vary, and can include removing part or all of the female external genitalia and “complete removal of the clitoris as well as additional cutting and stitching of the labia resulting in a constricted vaginal opening,” the report states.  “There are no known health benefits associated with female genital cutting or mutilation,” and the procedures can “put the woman at risk in the short and long term, pose risks to the mother and infant during childhood [including] increased deaths rates among infants during and shortly after birth and increased rates of obstetrical complications.”¹⁵

Other issues that must be determined include the type of facility that will offer MC,  the programs of public education and individual counseling that will precede it and prepare both the public and the patients to understand both the benefits and the risks, and the place of circumcision in overall HIV-reduction policies.  Given these complex considerations, introducing MC into HIV prevention programming always requires careful study of local conditions, warns Nancy Padian, executive director of the Women’s Global Health Initiative, a program of the Research Triangle Institute International.  “Any new intervention [involving MC] requires operations research to find the best way to roll it out at a population level,” she says.

“Anything that will give a person a chance to escape HIV infection is gladly welcome,” observes Gusongoirye.   But even so, his dangerously misinformed young friend and the others like him who “are rushing to get circumcised in order to ‘enjoy’ their sex unhindered” convince Gusongoirye that MC can only yield benefit as an element of a carefully designed, overall HIV prevention program and never the “entire and only shield.”¹⁶   But if properly used in such a program, experts believe, MC will dramatically reduce HIV transmission in Africa, allowing millions of men, women, and children to escape the disease.

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¹Unicef Information by Country, Swaziland Statistics.
²Auvert B., D. Taljaard, E. Lagarde, J. Sobngwi-Tambekou, R. Sitta, and A. Puren. “Randomized, Controlled Intervention Trial of Male Circumcision for Reduction of HIV Infection Risk: the ANRS 1265 Trial. PLoS Medicine. 2005; 2(11): e298.
³New Data on Male Circumcision and HIV Prevention: Policy and Programme Implications. WHO/UNAIDS Technical Consultation, Montreux, March 6-8, 2007.
⁴Klausner, J., R. Wamai, K. Bowa, K. Agot, J. Kagimba, and D. Halperin. “Is Male Circumcision as Good as the HIV Vaccine We’ve Been Waiting For? Future HIV Therapy. 2008; 2(1). 
⁵Potts, M., D. Halperin, D. Kirby, A. Swidler, M. Marseille, J. Klausner, N. Hearst, R. Wamai, J. Kahn, J. Walsh. “Reassessing HIV Prevention.” Science. 2008; 320: 749-50.  
⁶Kahn, J., E. Marselle, and B. Auvert. “Cost-effectivenes of Male Circucision for HIV in a South African Setting.” PLoS Medicine. 2006; 3(12): e517.
⁷McCoombe, S. and R. Short. “Potential HIV-1 Target Cells in the Human Penis.” AIDS. 2006; 20: 1491-95.
⁸Kahn et al.
⁹Kigozi G., S. Watya, C.B. Polis, C. Buwembo, V. Kiggundu, M.J. Wawer, D. Serwadda, F. Nalugoda, N. Kiwanuka, M.C. Bacon, V. Ssempijja, F. Makumbi, and R.H. Gray. “The Effect of Male Circumcision on Sexual Satisfaction and Function, Results From a Randomized Trial of Male Circumcision for Human Immunodeficiency Virus Prevention, Rakai, Uganda.” BJU International. 2008; 101(1): 65-70.
¹⁰McCoombe and Short.
¹¹Kahn et al.
¹² Williams, B., J. Lloyd-Smith, E. Gouws, C. Hankins, W. Getz, J. Hargrove, I. de Zoysa, C. Dye, and B. Auvert. “The Potential Impact of Male Circumcision on HIV in Sub-Saharan Africa.” PLoS Medicine. 2006; 3(7): e262.

¹³Gusongoirye, D. “Nothing Can Fight HIV/Aids Better Than Discipline.” New Times. May 8, 2008.
¹⁴Safe, Voluntary, Informed Male Circumcision and Comprehensive HIV Prevention Programming: Guidance for Decision-makers on Human Rights, Ethical and Legal Considerations. 2008. New York: UNAIDS.
¹⁵Ibid.
¹⁶Gusongoirye.