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Authors Robert S Van Howe, MD, MS, Abstract FAAP, Clinical Assistant The objective of this study was to determine whether the justifications given for promoting mass Professor, Marquette, Michigan circumcision as a preventive measure for HIV infection are reasonable and whether mass circumcision 49855, USA Tel: +1 906 228 7454 is a feasible preventive measure for HIV infection in developing countries. Email: [email protected] The medical literature concerning the practice of circumcision in the absence of medical indication J Steven Svoboda, JD (Harv), was reviewed regarding its impact on HIV infection and related issues. The literature was analysed with MA (Berkeley), Executive careful attention to historical perspective. Director, Attorneys for the Rights of the Child, Berkeley, Our results show that the medical literature supporting mass circumcision for the prevention of HIV California, USA infection is inconsistent and based on observation studies. Even if the two ongoing randomised Frederick M Hodges, DPhil controlled trials in Africa show a protective benefit of circumcision, factors such as the unknown (Oxon), PO Box 5815, Berkeley, complication rate of the procedure, the permanent injury to the , human rights violations and the California 94705, USA potential for veiled colonialism need to be taken into account. Based on the best estimates, mass Corresponding author: circumcision would not be as cost-effective as other interventions that have been demonstrated to be Robert S Van Howe, 1414 W effective. Fair Avenue, Suite 226, Marquette, Michigan 49855, Even if effective, mass circumcision as a preventive measure for HIV in developed countries is USA difficult to justify. Tel: +1 906 225 3925 Email: [email protected] Received 20 July 2004, revised and accepted 9 February 2005 INTRODUCTION theory of disease developed and the understanding Portions of this manuscript The explosion of publicity accorded to the of disease processes improved, the true aetiologies of were presented at the HIV/AIDS pandemic can in part be attributed to the the illnesses for which circumcision was believed to Fourteenth Meeting of the lack of clear understanding of the disease mecha- hold the cure were elucidated. During the Cold War, International Society for Sexually Transmitted Diseases nism and the apparently inescapable mortality mass involuntary circumcision of the newborn was Research, Berlin, Germany, July attributed to the acquisition of HIV. The public’s implemented in the USA, giving the practice a 2001 awareness and fear of HIV have resulted in changes cultural foothold.6 New medical-sounding justifica- Key words in sexual behaviours such as increased condom use, tions, however, were sought to justify its continued which has been less comprehensive and long-lasting use as a routine neonatal surgery since the tradition- Circumcision; HIV infection; 1 informed consent; medical than originally expected. Regrettably, some have al justifications for preventing masturbation and history; prophylaxis capitalised on the fear generated by the HIV/AIDS ‘nervous diseases’ were no longer as persuasive to the pandemic to promote personal or political public or the medical profession. The prevention of agendas.2-5 In the medical establishment, this has cancer, sexually transmitted diseases (STDs) and been manifested in the scientifically dubious promo- urinary tract infections were each in turn invoked to tion of male circumcision as a preventive measure justify infant male circumcision, although the for HIV infection.2 medical evidence supporting such claims ranged from paltry to imaginary. HISTORY OF CIRCUMCISION A clear pattern has emerged: any incurable disease PROMOTION that happens to be the focus of national attention at This is not the first time that circumcision has been any given time will be used by US circumcision promoted as a panacea for an incurable disease. As a advocates as an excuse for the continued imposition medical procedure, circumcision was first intro- of mass circumcision. In the 1870s, epilepsy was the duced in the nineteenth century in English-speaking focus of national attention, so circumcision advo- countries as a means of preventing and ‘curing’ cates claimed that circumcision could cure and masturbation, which was then believed to cause prevent epilepsy.6 In the 1940s, STDs were the focus everything from epilepsy, insanity, tuberculosis, of national attention, so circumcision advocates spinal paralysis, to hip dysplasia.6 As the germ claimed that circumcision could cure and prevent

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the spread of STDs.6 Likewise in the 1950s, support an association.19, 20 Likewise, tific inquiry might be a randomised cancer was the focus of national attention, general population surveys have, as a controlled trial, problems exist with such a and again circumcision advocates claimed whole, failed to demonstrate a strong asso- project. A trial involving permanent ampu- that circumcision could cure and prevent a ciation.19, 20 It is only when limiting the tation of a body part, the benefit of which variety of cancers including penile cancer, analysis to African studies and using values is largely unproven, is fraught with ethical cancer of the tongue, prostate cancer, rectal obtained following multivariate analysis pitfalls and would not be likely to be cancer and cervical cancer.6 Since the late that an association can be extracted from approved in a developed nation. The 1980s, HIV and AIDS have become the these studies.21 One of the challenges in subject would certainly need to be fully focus of national attention, and circumci- interpreting these various observational informed, and the potential for manipula- sion advocates have, predictably, claimed studies is determining whether circumci- tion of the information provided would that circumcision can prevent HIV infec- sion status may be a risk factor or a marker need to be prevented. Studies have already tion.6 for other risk factors. The fundamental demonstrated that pro-circumcision prop- flaw in multivariate analysis is that to be aganda can effectively influence attitudes LINKING CIRCUMCISION AND accurate it is assumed that the variables regarding circumcision.25-30 Despite the HIV/AIDS controlled for are independent of one clear ethical contraindications, two Against this historical backdrop, the another. Many of these variables, including randomised controlled trials to determine HIV/AIDS pandemic is merely the latest sexual, religious and hygienic practices, as if a relationship exists between HIV status incarnation of a 130-year-old pattern of well as economic status, appear to be and circumcision to be undertaken in circumcision promotion by a small, but linked to tribal affiliation, which in turn is Africa have received funding from the US very influential, portion of the medical strongly correlated with circumcision National Institutes of Health. Both studies community in circumcising first world status.22 These multiple, highly-correlated, are markedly overpowered so as to find a countries.7-12 The idea that circumcision confounding factors influencing sexual statistically significant difference where a can prevent AIDS was developed by Fink, a behaviours and HIV susceptibility create a significant clinical difference may not long-time advocate of mass circumcision. co-linearity problem that can make these exist.31-33 A report in the lay literature Fink introduced the hypothesis in a letter regression models unstable and yield unre- suggests that compliance following to the New England Journal of Medicine,13 liable results. Consequently, without more randomisation may pose a serious threat to which he later admitted was based purely reliable data it is irresponsible to place the study’s completion.34 Therefore, the on speculation rather than hard data.14 blame for HIV’s spread on normal penile subsequent analysis must employ an Seeking to capitalise on public anxiety over anatomy. intent-to-treat approach, as otherwise the spread of HIV, other advocates of mass Many of the studies suggesting an associ- serious bias would be introduced into the circumcision sought to develop Fink’s ation between circumcision status and HIV results. hypothesis by producing geographical infection tested a wide assortment of analyses of Africa, which studied maps factors, fishing for significant risk factors FACTORS TO CONSIDER BEFORE rather than men, which they argued could without making the proper adjustments RECOMMENDING A be used to legitimise mass circumcision in for multiple comparisons. As a result, CIRCUMCISION PROGRAMME the US. Using decades-old anthropological many of the positive associations asserted In the unlikely event that a randomised data and extrapolating HIV incidence could be due merely to oversampling. controlled trial demonstrates a benefit, the rates, an association between the Meta-analysis has demonstrated signifi- decision to recommend universal circum- and HIV was suggested.15 Next came a cant between-study variability independ- cision in Africa would need to take several number of observational studies suggesting ent of the vagaries of geography, study additional factors into consideration. an association between the foreskin and an design and circumcision’s prevalence 1) How does universal circumcision increased risk of HIV infection in men, within a community,19 and has suggested compare in efficacy, cost and complica- mostly in Kenya, who exhibited high-risk the possibility of publication bias, whereby tions to other interventions aimed at behaviours.16, 17 These studies compared studies failing to find a correlation between reducing HIV infection? disparate populations that were distin- circumcision status and HIV infection are The aggressive diagnosis and treatment guishable on other relevant independent either never submitted for publication or of STDs and various treatment modalities variables, such as religion, social class, are passed over by editors.20 Observational in the African context have been shown to tribal affiliation, sexual practices and pres- studies, when compared to randomised be clinically effective and reasonably cost- ence of genital ulcer disease. Subsequently, controlled trials, have been shown to effective.35-37 Our preliminary calculations the degree of association of the initial consistently overestimate odds ratios by indicate that to be competitive with these studies and the infectivity attributed to the 30%.23 In light of this unexplained hetero- proven interventions, even granting for the foreskin could not be replicated in the geneity and possible publication bias, any sake of argument the proponents’ claims same population by the same team of conclusion based on these observational for the effectiveness of circumcision, a investigators.18 studies should be viewed with scepticism.24 circumcision would need to cost less than Partner studies in which associations On the basis of weak scientific evidence, $1.52 (unpublished data). Estimates of the were suggested between the HIV status of a many circumcision proponents have called costs of a sterile circumcision in Africa, woman and the circumcision status of her for universal circumcision in Africa.2-4 excluding the cost of treating any compli- sexual partner have overall failed to Although the next logical step in this scien- cations from the surgery are $15.38 Surgery

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thus does not seem an economically or a amputation of the foreskin appear univer- of those targeted. Therefore, cultures that medically logical intervention for this sally unaware or unwilling to acknowledge currently do not circumcise should not be infection. Since the spread of HIV infec- its immunological, protective and eroge- induced to adopt the practice.55 tion is primarily caused by behaviour, nous functions. This is to be explained by 7) The removal of the majority of the many AIDS researchers believe that behav- the fact that circumcision advocates are male genital mucosa would diminish the ioural interventions hold the most hope in almost always circumcised men from effectiveness of the mucosal vaccines being the long term.39 circumcising cultures.51 developed. 2) The surgical complications of the 4) Careful scrutiny must be given to 8) The demand for male circumcision procedure, which are believed to be higher legal, ethical and human rights considera- may translate into an increased demand for in developing nations, need to be consid- tions surrounding the removal of healthy female circumcision, since the justifica- ered. Although no study has been complet- tissue from non-consenting minors to tions for both practices are strikingly ed to address this issue comprehensively, allegedly protect them from a behaviour- similar.56 circumcision in developing nations entails based disease that may not exist or for additional risks of tuberculosis,40 which they may not be at risk when they LACK OF BIOLOGICAL PLAUSABILITY tetanus,41, 42 and severe complications.43, 44 reach sexual maturity.52 In order for the scientific community and Immediate complications following neona- 5) The potential for bias in the informa- the public to accept circumcision as a tal circumcision in North America occur in tion transmitted during the informed preventive measure for HIV, a biological 2% to 6% of infants,45, 46 while delayed consent process in older males has been basis for the intervention is needed. complications, such as meatal stenosis established.26 Using a selective bibliogra- Circumcision proponents have responded requiring meatotomy, occur in 5% to 10% phy, a convincing argument can be made by propagating speculations as if they were of circumcised boys.47 in favour of circumcision.53 Such an fact in the apparent hope that, if repeated The US pro-circumcision information approach may be attractive to a healthcare often enough, they will be regarded as fact. campaigns targeted at Africa are beginning provider or investigator wishing to Such assertions include: to increase the number of requests for the promote the practice. Clearly, such coer- a) The claim that the preputial mucosa is procedure from African men who have cion - with amputation taking the place of more prone to abrasion than the exter- been understandably misled into believing education - is not in the best interests of nalised mucosa of the glans of the circum- that it will make them immune to HIV the patient. The public may be left, cised penis.57 In fact, a study by a infection.25-31 If this pattern continues, the whether intended or not, with the impres- prominent circumcision proponent found demand for circumcision may outstrip the sion that circumcision provides complete a trend in the opposite direction.58 In a capacity to provide the procedure in a protection from HIV infection. An increase similar vein, women reported more prob- controlled setting. Non-sterile procedures in high-risk behaviours might ensue. lems with adequate coital lubrication with performed by untrained individuals, who Following circumcision, a male still needs their circumcised partners than with their would undercut the price of sterile proce- to engage in safe sexual practices to avoid genitally intact partners.50 Regrettably, the dures, would result in a higher rate of acquisition of HIV. This needs to be impact of ‘dry sex’ on the risk of HIV in complications and perhaps a higher rate of emphasised, and statements that circumci- the male partner has been largely unex- HIV infection. Ironically, a higher number sion provides a ‘natural condom’54 are plored.59 of boys in Africa could then die at the counter-productive. b) The suggestion that the subpreputial hands of their circumciser than the total 6) It is likely that a recommendation for space is more likely to harbour sexually that ostensibly might have been protected universal circumcision in Africa would be transmitted viruses and to promote their from HIV infection. Without better infor- interpreted as thinly-veiled colonialism. In propagation.57 Recent studies have shown mation regarding complications, a recom- addition to raising human rights issues, that genital warts are more common in the mendation for universal circumcision is such a call for circumcision would come circumcised male.60 When the studies unfounded. into conflict with the role of circumcision exploring the association between circum- 3) The permanent untoward effects of status as a sign of tribal affiliation. cision status and human papilloma virus the amputation have been largely ignored. Assimilation is probably the greatest threat infections are combined in a meta-analysis, Circumcision removes the vast majority of to tribal/cultural identity. Imposition of the summary effect indicates no associa- fine-touch neuroreceptors found on the circumcision on cultures where it has not tion (random effects model OR=1.24, penis. Studies of the foreskin have revealed been previously practised thus poses a 95%=0.91-1.69) (unpublished data). it to contain highly complex, specialised serious threat to tribal/cultural identity. Likewise, a large American study found tissue.48 By contrast, the glans has primari- Should healthy body parts be amputated to circumcised men to be at higher risk for ly free nerve endings, which can only sense conform to the cultural and religious prac- genital herpes,22 while meta-analysis fails deep pressure and pain.49 The anatomical tices of scientists from outside cultures to support an association (random effects changes caused by circumcision may be whose only rationale is they believe that it model OR=1.15, 95%=0.92-1.45) (unpub- responsible for the differing sexual prac- may confer some benefit? Attempts to lished data). tices seen in circumcised men,22 as well as change cultural practices are often unwel- c) The assertion that the preputial for coital techniques that make the experi- come and strenuously resisted. Every mucosa is rich in Langerhans cells, which ence less satisfactory for their female part- attempt should be made to counter the are believed to be the port of entry for ners.50 Those touting the benefits of the AIDS epidemic within the cultural context HIV. This assertion is based primarily on

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an opinion piece published by vocal advo- ed with higher rates of HIV infection.19 published in a journal read primarily by cates of mass circumcision.4 What is This result is driven by the US where the North American paediatricians, three needed to decide this to date undocument- incidence of heterosexually-acquired HIV leading circumcision advocates were ed assertion, is data on the density of infection is double to triple that docu- allowed to publish a long opinion piece Langerhans cells in the prepuce of sexually mented in western Europe.67 Other differ- recounting the many supposed medical active men with and without STDs. Such ences between North America and Africa benefits of neonatal circumcision.5 Despite information, which would facilitate a include the predominant HIV strain and one author’s previous admission that determination of the importance of this the principal sexual mixing patterns. studies of HIV in Africa did not pertain to factor, has not been published.61 Moreover, Another example is the attention paid to North America,63 the authors provided a inflammatory T-cells may be needed for a randomised controlled trial that was selective recounting of the studies from HIV to enter a , suggesting rejected by The Lancet. The reports of the Africa to suggest an association between that a predisposing infection may be a results of this study have appeared in the foreskin and HIV infection in the US.5 necessary condition for HIV infection.62 Science68 and The Wall Street Journal,69 but The authors’ assertions were publicly Clearly, further study is needed. has yet to be published in a peer-reviewed dismissed by the chairman of the AAP Task journal. At the Third International AIDS Force, prompting an additional letter to IMPACT ON NORTH AMERICA Society Conference on HIV Pathogenesis the editor by this trio, who cited new Circumcision advocates appear unduly and Treatment in Rio de Janeiro in July publications to support their position.84 hasty in their desire to implement univer- 2005, a study indicating that female Two of these publications were, in fact, sal circumcision in Africa, despite weak circumcision was associated with a lower opinion pieces.2, 85 The two genuine studies support for their endorsement and the risk of HIV infection was presented,70 yet referenced had serious methodological significant number of unanswered issues. this finding has received little or no atten- flaws and were written by a member of this We contend that the rush to intervene has tion. If the true aim is to reduce the inci- trio,86, 87 calling their objectivity into ques- little to do with preventing HIV infection dence of HIV infection, one would expect tion. Several years later, the lead author in Africa and may have more to do with a physicians advocating a surgical preventive had yet another letter published in the conscious and/or unconscious impulse to for males would also expend the same same journal pushing the same message, help perpetuate and promote the practice energy advocating a surgical preventive for i.e., that mass circumcision was necessary in North America. There is ample indirect females. in the US to fight AIDS.88 evidence to support this contention. 3) Several opinion pieces published in 1) The call for universal circumcision in the medical literature have been portrayed CONCLUSION Africa did not emanate from Africa, but as ‘studies’ in both lay and medical publi- Why are circumcision proponents expend- rather from North American physicians cations.2-4 The authors have made no ing so much time and energy promoting and researchers, most of whom had a long noticeable attempts to correct this mass circumcision to North Americans history of vocal advocacy of mass circum- mischaracterisation. This suggests that when their supposed aim is to prevent HIV cision in the US.2, 3, 57 these authors are playing to the general in Africa? The circumcision rate is declin- 2) A large amount of coverage in the public, especially in North America, in the ing in the US, especially on the west North American lay press has been devoted manner most advantageous to their coast;89 the two North American national to the studies suggesting an association agenda, and dispensing with their obliga- paediatric organisations have elected not to between the foreskin and HIV infection tion to avoid misrepresenting the impor- endorse the practice, and the practice’s among males in Africa, despite clear tance and validity of their opinions. legality has been questioned in both the concessions that the African experience 4) The neonatal circumcision juggernaut medical and legal literature.50, 90-94 ‘Playing differs in a number of significant ways in the US is beginning to lose steam. the HIV card’ misdirects the fear under- from the American experience.63 The Despite efforts to halt and reverse the standably generated in North Americans American experience, as far as can be decline,71-77 neonatal circumcision rates by the HIV/AIDS pandemic into a concrete determined, in certain respects has been continue to fall in the US. In 1996, the action: the perpetuation of the outdated the opposite of that in Africa, with homo- Canadian Paediatric Society issued a policy practice of neonatal circumcision. sexual men, rather than heterosexual statement that recommended against Amputation of highly erogenous genital women, as the focus of the early pandemic. neonatal circumcision.78 More recently, the tissue is viewed as barbaric by cultures that None of the published studies in the US Royal Australasian College of Physicians, as do not subscribe to the practice.95 From a has been able to demonstrate a clear asso- well as provincial paediatric organisations psychological standpoint, it can be inferred ciation among heterosexuals between HIV in British Columbia and Saskatchewan, that, in cultures where circumcision is and presence of the foreskin.22, 64, 65 One have issued policy statements strongly common, circumcisers desire to be study found a marginally significant asso- condemning neonatal circumcision.79-82 In empowered by their actions. Similarly, ciation in homosexual men.66 These results 1999, the American Academy of Pediatrics circumcised males are conditioned to are suspect in that the investigators relied (AAP) Task Force on Circumcision believe that their incomplete penis is supe- on history, which is known to be unreli- concluded that the medical evidence rior to the intact penis. Medical justifica- able, to determine circumcision status. favouring circumcision was ‘not sufficient tions, even though repeatedly proposed Geographic analysis of developed nations to recommend routine neonatal circumci- and disproven,6 are a means by which these demonstrates that circumcision is associat- sion’.83 In response to this policy statement psychological objectives can be accom-

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plished. Beliefs and fears alone, no matter how rationally rather than use AIDS as yet In the quest to conquer AIDS, as with understandable, deeply held or traditional, another excuse to promote an old blood any disease, medicine and science ought to cannot justify the amputation of healthy rite. be purged of all vestiges of superstition, tissue. Scientific efforts to understand, personal agendas and wishful thinking. contain and prevent HIV infection are Medicine must ally itself with scientifically more likely to be successful when the proven practices within the dictates of scientists involved in this endeavor can medical ethics, human rights and the law. gather and analyse data objectively and

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dren?: the practice of circumcision in the Comparative Analysis of Legal and Extralegal Multidisciplinary Approach to a United States. J Gender Soc Pol Law Methods to Control Child Body Mutilation Multidimensional Problem. New York: Kluwer 1998;7(1):87-123 Practices. In: Denniston GC, Milos MF, Hodges Academic/Plenum Publishers, 2001. pp. 297- 95 Svoboda JS. The Limits of the Law: FM, editors. Understanding Circumcision: A 365

Contributions invited for JRSH Members and readers are encouraged to send in contributions to JRSH in the form of original research and articles. Forthcoming issues in 2006 will feature the following themes:

Arts and health - May 2006 Injuries - September 2006

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November 2005 Vol 125 No 6 The Journal of The Royal Society for the Promotion of Health JRSH