Male circumcision for HIV prevention: current evidence and implementation in sub-Saharan Africa

REVIEW Open Access

Male circumcision for HIV prevention currentevidence and implementation in sub-SaharanAfricaRichard G Wamai1 Brian J Morris2 Stefan A Bailis3 David Sokal4 Jeffrey D Klausner5 Ross Appleton6Nelson Sewankambo7 David A Cooper8 John Bongaarts9 Guy de Bruyn10 Alex D Wodak11 and Joya Banerjee12

Abstract

Heterosexual exposure accounts for most HIV transmission in sub-Saharan Africa and this mode as a proportion ofnew infections is escalating globally The scientific evidence accumulated over more than 20 years shows thatamong the strategies advocated during this period for HIV prevention male circumcision is one of if not the mostefficacious epidemiologically as well as cost-wise Despite this and recommendation of the procedure by globalpolicy makers national implementation has been slow Additionally some are not convinced of the protectiveeffect of male circumcision and there are also reports unsupported by evidence that non-sex-related drivers play amajor role in HIV transmission in sub-Saharan Africa Here we provide a critical evaluation of the state of thecurrent evidence for male circumcision in reducing HIV infection in light of established transmission driversprovide an update on programmes now in place in this region and explain why policies based on establishedscientific evidence should be prioritized We conclude that the evidence supports the need to accelerate theimplementation of medical male circumcision programmes for HIV prevention in generalized heterosexualepidemics as well as in countering the growing heterosexual transmission in countries where HIV prevalence ispresently low

ReviewImplementation of male circumcision (MC) for HIVprevention in sub-Saharan Africa remains disappoint-ingly slow despite its proven efficacy of greater than60 based on the results of three randomized controlledtrials (RCTs) conducted in the region [1-3] These datareceived support from a Cochrane review [4] and con-firm more than two decades of data from observationalstudies [5] An as-treated meta-analysis for the 15 obser-vational studies that adjusted for potential confoundersgave a summary risk ratio indicating a protective effectof 65 that was identical to the initial findings from thethree RCTs [67] Another meta-analysis of the RCTdata reported a relative risk reduction of 56 [8]In a meta-analysis of 13 studies 85 of which were

from sub-Saharan Africa a 58 protective effect was

noted (53 for general populations and 69 for high-risk populations) [9] In this report protection was 57for the RCTs and 61 for observational studies (cohortstudies 71 and case control 46) In addition if MCstatus was ascertained by self-report the protectiveeffect was 45 but if by direct genital examination inthe clinic it was 65 These authors pointed out thatthe current data on MC satisfy six of the nine criteria ofcausality as outlined by Sir AB Hill namely strength ofassociation consistency temporality coherence biologi-cal plausibility and experiment [10]With these definitive results key international health

bodies [1112] and numerous governments of countriesmost affected [1314] have formulated affirmative poli-cies on MC for HIV prevention There is now a consen-sus among most experts in the HIVAIDS scientificcommunity that MC although not a ldquomagic bulletrdquo is acritical component in the ldquotool boxrdquo of HIV preventionapproaches Crucial to the effectiveness of MC policy isan understanding of how effective MC will be in HIV

Correspondence rwamaineuedu1Department of African-American Studies Northeastern University BostonMA USAFull list of author information is available at the end of the article

Wamai et al Journal of the International AIDS Society 2011 1449httpwwwjiasocietyorgcontent14149

copy 2011 Wamai et al licensee BioMed Central Ltd This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (httpcreativecommonsorglicensesby20) which permits unrestricted use distribution and reproduction inany medium provided the original work is properly cited

reduction and as a corollary to this the level of impor-tance that heterosexual transmission plays in overallHIV transmission in a populationHistorically transmission of HIV has been attributed

to four main modes sexual intercourse transfusion par-enteral and perinatal acquisition [15] In light of thismultiple types of intervention strategies (behaviouralstructural and biomedical) have been advocated [16]While scientists seek to provide the evidence base pub-lic policy makers must evaluate logically where the pre-ponderance of evidence lies and make correct decisionsbased on a reasonable assessment of such evidence [17]Urgent calls have been made by experts and advocatesto accelerate HIV prevention scale up in line with theprevention principles [1819] However in someinstances skepticism about the evidence has led to hesi-tation delays and inaction leading to misery and as inSouth Africa needless death for hundreds of thousandsfrom failure to expeditiously implement programmesthat work [20]In the sub-Saharan African setting the established

convention is that heterosexual transmission is the pri-mary driver for the HIV epidemic Recently howeversome have argued that current HIV prevention interven-tions are based on ldquoinsufficient informationrdquo on modesof transmission and what works [21] We agree thatthere is a need to continually evaluate and updateknowledge on HIV transmission and what works in pre-vention so as to better inform and reinforce policy mak-ing and implementation Therefore in reinforcing thepolicy imperative for MC as a proven method for pre-vention of heterosexual HIV transmission we firstreview the state of knowledge on modes of HIV trans-mission in sub-Saharan Africa We then assess thestrength of current evidence for MC in protectingagainst HIV infection before analyzing current MCimplementation programmes in the region Finally wehighlight some of the outstanding issues and call for anacceleration in MC implementation as an evidence-based strategy to stem the HIVAIDS epidemic

What we know about the drivers of HIV infectionin sub-Saharan AfricaAccording to the latest Joint United Nations Programmeon HIVAIDS (UNAIDS) epidemic update report of the333 million people living with HIVAIDS worldwide atthe end of 2009 925 were adults [22] About halfwere women and 676 live in sub-Saharan Africawhere women comprise about 60 of cases [22] Oftotal infections globally 25 million (approximately 75of the total) were in children (aged younger than 15years) of whom 92 live in sub-Saharan Africa wherethey comprise 10 of all cases [22] Although some chil-dren younger than 15 are sexually active the prevalence

estimates show that 925 of cases globally and 90 insub-Saharan Africa are in the adult population [22]While this in itself does not necessarily show associa-

tion with sexual activity the preponderance of infectionin adults can only be explained by adult-specific factorsnot affecting children HIV distribution by sex andacross age groups are clearly consistent with sexualbehaviour as the main mode of transmission as shownby the significant and sudden increase in HIV in thoseolder than 15 years [2223]Consistent evidence for a major role of sexual inter-

course in transmission of HIV has been provided bynumerous modelling studies [24-28] and ecologicalobservations published by the World Health Organiza-tion (WHO) and UNAIDS in their annual report [22]as well as in national estimates [29] These data are col-lected according to global norms [3031] whose methodsare continually refined [32-35]The effect of sexual transmission likely lie in context-

specific factors confounding host and agent alike Theseinclude stage of the disease associated viral load otherbiological factors [2436-40] as well as the socio-eco-nomic and policy context [2041] Credible researchshows that the key initial drivers of the sexual transmis-sion were a synergistic relationship between promiscu-ous practices coupled with individual-level biologicalfactors namely sexually transmitted infections (STIs) (inparticular genital ulcer disease syphilis and HSV-2) andlack of MC [40-44] These factors also help explain thedifferences in rate of spread across the continent [4245]Among these the role of multiple and concurrent

partnerships (unstructured casual sex and polygyny) iswell documented in many sub-Saharan Africa countries[46-51] This is demonstrated for example in one ofthe most detailed studies involving 179 focus groupsand 116 in-depth interviews with diverse groups of peo-ple (malefemale youngold urbanrural) in typical day-to-day settings in 10 countries of southern Africa thathave high generalized HIV epidemics [52] Modellingand network theory reveal dynamics of exposure [5354]Nevertheless there is conflicting evidence on the extentto which multiple and concurrent partnerships drivesthe epidemic as shown in recent assessments of theexisting literature by Lurie and Rosenthal [55] andSawers and Stillwaggon [56] as well as a debate hostedon 27 October 2010 by the United States Agency forInternational Development (USAID) and the WorldBank among opposing sides [57]While heterosexual behaviour plays a leading role in

HIV transmission in sub-Saharan Africa it is fair to askwhat proportion of infections is from non-sexual driversThese include unsafe injections in medical and non-medical settings [5859] injecting drug use and bloodtransfusion [60-62] mother to child transmission


Page 2 of 17

[22616364] men who have sex with men (MSM)[6566] and cultural practices [6768] such as unsafe tra-ditional MC and female genital cutting [69-72] Whilesome argue that these play a significant role in sub-Saharan Africa [21687374] such evidence is largelycircumstantial [6275] and the level of such exposuresare altogether too low to fuel a generalized epidemic[75-77] One crucial illustration of this comes from amodelling approach in use since 2003 [61] namely theModes of Transmission (MoT) approach Developed bythe UNAIDS Reference Group to help country-level pol-icy makers respond to the epidemic and prioritize inter-ventions the MoT approach provides a robust meansfor estimating patterns of adult HIV transmissionthrough different routes [61]To date MoT analyses have been conducted in Kenya

[61] Lesotho [78] Swaziland [79] Uganda [80] andZambia [81] They show that sexual behaviour accountsfor 941 970 940 996 and 998 of new infec-tions in each respective country with the categories ofmultiple partnerships and partners of multiple partner-ships contributing more than half of all cases in Lesothoand Zambia (Table 1) On the other hand the popula-tion of MSM in sub-Saharan Africa is not known partlydue to laws prohibiting this behaviour in most countriesalthough HIV prevalence in MSM is however high [65]A systematic review estimated that the MSM routemakes an approximately 157 contribution to HIV pre-valence in sub-Saharan Africa [82] In one MSM cohortin Mombasa Kenya HIV prevalence was 43 in menreporting exclusive MSM relations compared with 12in men reporting sex with both men and women [83]In contrast in Kenyan Ugandan and Zambian studies

infections arising from blood transfusion were insignifi-cant (Table 1) Furthermore a review of Demographicand Health Surveys data from 10 countries indicated

that although having had a blood transfusion increasesrisk of HIV infection among women (but not men) inCameroon and Uganda blood transfusions are rare [62]While non-sexual routes are relatively minor they meritcontinued monitoring [217484] Nonetheless at pre-sent evidence-based means of reducing heterosexualtransmission should be prioritized [85] One of these ismale circumcision

Efficacy of male circumcision for HIV preventionan update on the evidenceAs one of the oldest surgical procedures known tohumankind and the most widely practiced surgeryworldwide male circumcision has served religioussocio-cultural and health purposes [6986-88] Since thesuggestion in the 1980s that MC might prevent HIVinfection [89-91] numerous ecological case-control andcohort studies reviews systematic reviews and meta-analyses have established that MC significantly reducesthe risk of heterosexual HIV infection [6-96992-94]The meta-analysis by Weiss et al of 27 observationalstudies to the late 1990s showed a reduced risk in 21studies [7] In 15 studies that adjusted for confoundingfactors adjusted relative risk reduction was 042 (95CI 034-054) [7] A Cochrane systematic review in 2005assessing the quality of 37 studies of MC and HIVnoted that while the different methodologies showedvarying results the protective effect of MC was sup-ported consistently [93]In 2005 and 2007 the efficacy of MC in HIV preven-

tion was verified beyond reasonable doubt by resultsfrom three large RCTs the gold standard of epidemiolo-gical research these being conducted in South AfricaKenya and Uganda [1-3] Acceptance by the interna-tional health community quickly followed [11-14] In2009 the Cochrane committee concluded that MC for

Table 1 Incident HIV infections by modes of transmission in five sub-Saharan Africa countries

share of modes of HIV transmission in five countries

Uganda (2008) Kenya (2006) Zambia (2008) Swaziland (2008) Lesotho (2008)

Injecting drug users (IDUs) 028 484 0 11 0

Partners of IDU 001 02 0 01 0

Sex workers (SW) 091 125 075 3 047

SW clients 783 1048 404 47 059

Partners of SW clients 181 11 181 26 168

Men who have sex with men (MSM) 061 449 099 36 289

Female partners of MSM 01 064 005 05 05

Multiple partnerships (MP) 2373 1831 3396 134 3104

Partnersrsquo MP (PMP) 2176 2774 3703 208 2745

Mutually monogamous heterosexual sex 4289 3014 2119 498 3515

Medical injections 006 055 017 001 004

Blood transfusions 0 024 002 002 0

Bold text indicates sexual transmission [6178-81]


Page 3 of 17

HIV prevention was supported and no further trialswere required [4] More recently a systematic review of37 late-phase RCTs of various HIV prevention interven-tions found MC to have a stronger efficacy in prevent-ing HIV infection than vaccines microbicides andtreatment of STIs [95] An important development inMC documentation has been the initiation by UNAIDSWHO and others of an online resource centre [96]Research on acceptability of MC at the population

level in sub-Saharan Africa countries in 14 studies innine countries showed varied results but was generallyhigh among men and women [9798] Continued assess-ment of impacts challenges and opportunities [99100]support the urgency of accelerating the implementationof MC for HIV prevention [101102] In 2010 the US-based Center for Global Health Policy called for ldquoaggres-sive scale uprdquo of MC based on the evidence for its abilityto prevent HIV infection [103] The quality of the evi-dence supporting MC is ldquoconclusiverdquo [7] making MC asound recommendation for public health [104] Suchevidence calls for skepticism to be dismissed [17]

Biological mechanism of male circumcision inmediating HIV infectionSeveral suggestions have been made to explain the vul-nerability of the foreskin to HIV infection The innerepithelium of the foreskin is mucosal has been found tolack protective keratin and to contain Langerhans cellsand T cells that express the HIV receptor CD4[87105-109] In an early study HIV was taken up read-ily by the inner but not the outer foreskin epithelium inexplant culture [106] Nearly a decade later Ganor andcolleagues developed two new excellent models of theforeskin epithelium an improved explant model and a3D immuno-competent in vitro model [108] Theirhuman adult ex vivo foreskin explant model showedthat Langerhans cells and dermal T cells in the less-ker-atinized inner foreskin have a significantly higher densitythan in the outer foreskin When the foreskin wasexposed to mononuclear cells highly infected with HIVbut not free HIV virions were found in the epidermis ofthe inner foreskin within one hour demonstrating thatLangerhans cells can efficiently transfer HIV to T cells[108]In another review Ganor and Bomsel suggested that

the main pathway for HIV entry was driven by molecu-lar signals such as chemokines [109] Findings of no dif-ference [110] in or greater [111] keratin thickness ofthe outer versus the inner foreskin or in susceptibility toHIV [112] have been dismissed as products of postmor-tem changes and technical artifacts [109] Foreskinaspects relevant to HIV infection include the skin sur-face area the microbiologic environment HIV-1-suscep-tible cells and tissue structure although more research

is needed to determine the relative contribution of each[113]Besides the ease of infection by inner epithelial cells to

HIV HIV is suspected of infecting the body via tears inthe fragile inner surface of the foreskin and frenulumwhich are also susceptible to infection by other STIs[4387105] STIs hamper the ability of langerin in Lan-gerhans cells to protect against HIV [107] Thus the vul-nerability of the foreskin to HIV infection lendsbiological support to the extensive epidemiological evi-dence for the protection MC confers against HIV infec-tion in men during heterosexual intercourse

The relationship between MC and HIV evidenceand issues from population-based surveysThe highly acclaimed RCTs [1-3] would not have takenplace had there not been extensive observational evi-dence in place already attesting to the ability of MC toprevent HIV transmission Nevertheless RCTs havebeen overvalued in medical studies and by themselvesthey yield insufficient evidence for policy and must besupplemented by observational evidence [5] Population-based surveys in particular the Demographic andHealth Survey (DHS) and the AIDS Indicator Surveyhave been cited frequently because of the insights theyprovide into the patterning of HIV and MC in sub-Saharan Africa [495194114115]Some have however disputed the association of HIV

prevalence and MC levels in such surveys For exampleGisselquist et al refer to DHS data showing higher pre-valence of HIV in circumcised men in seven of 13 sub-Saharan Africa countries [21] In contrast the ecologicalanalysis of 118 developing countries by Drain and col-leagues showed that high MC prevalence was stronglycorrelated with low HIV prevalence independent of reli-gion [94]Furthermore a recent cross-sectional analysis of DHS

data for 18 countries across sub-Saharan Africa from2003 to 2008 involving 70554 males aged 15 to 59 yearsconfirmed that being uncircumcised was significantlyassociated with risk of HIV infection (OR 412 95 CI385-442) and that risk increases with number of life-time partners [115] In light of the probable conflict ininterpretation Wamai et al [116] have warned that DHSdata must be used with caution because of their widelyacknowledged inherent methodological problems whichGersovitz asserts need to be overcome in order toimprove reliability [117]DHS data are moreover often bidirectional indicating

contrasting and context-specific effects In Tanzania forexample circumcision in men is higher in the upperquintiles of education and wealth and such men havemore sex partners [118] So not surprisingly HIV pre-valence in Tanzania and numerous other countries


Page 4 of 17

across sub-Saharan Africa is higher in people withhigher education and income [119120] Furthermorethis relationship is not necessarily linear and can changeover time [41] The higher risky behaviour of such mensuch as being more likely to have concurrent partnersthan uncircumcised men would explain why in certainsettings they have a high HIV prevalence despite beingcircumcised This was pointed out in a recent analysisof surveys in 21 countries in sub-Saharan Africa [49]Since DHS data involve self-reported surveys multiple

factors have to be considered when examining the rela-tionship between MC and HIV prevalence Theseinclude risky sexual behaviour time of MC whether cir-cumcision was complete partial or performed at allmarital status education wealth and patterns of resi-dence (urban vs rural) As an example a study inUganda by Gray et al of a large cohort of HIV-negativemen found that MC significantly reduced HIV acquisi-tion (unadjusted RR = 061 95 CI = 037-097) but theprotective effect was lower for post-pubertal circumci-sion (ie after 12 years of age) in Muslims it wasfurther confounded by cultural and behavioural factors[92] In another example a cross-sectional study inKenya Lesotho and Tanzania found that while the pro-tective effect of MC in adolescents was only ldquoprobablerdquoin adults the association of MC with lower HIV infec-tion was unequivocal indicating a protective effect inmales who were more likely to be sexually active [121]There is a further point to note from ecological obser-

vation Molecular clock analyses indicate that HIV hasexisted for about 70 years and may have originated in ornear Cameroon (HIV-1) Guinea-Bissau (HIV-2) and theCongo [122123] Yet none of these countries wheremost men are circumcised [69] have had adult preva-lence rates as high as those observed in eastern andsouthern Africa [2239] Hence it could be reasonablyconcluded that structural features of wealth and povertypatterning behaviour [41] reported practice of multipleand concurrent partnerships [4952] couple discordancy[124] prevalence of other STIs [404244] and geo-graphic variations in MC [6994] have synergized to pro-vide the ldquoperfect stormrdquo for the HIV epidemic in sub-Saharan African countries with low MC prevalence[4391]

Male circumcision for HIV prevention saving livesand costs - the policy imperativeUnlike other HIV prevention strategies MC is a one-time procedure conferring potentially lifelong protectivebenefits so making it a highly cost-effective life-savingintervention as revealed by several studies subsequentto the RCTs [99125-130] For example a study by theUNAIDSWHOSACEMA Expert Group on Modelingthe Impact and Cost of Male Circumcision for HIV

Prevention found that one HIV infection would beaverted for every 15 circumcisions at a cost of US$150to US$900 over a 10-year time horizon [130] The popu-lation-level impact of MC in reducing HIV incidence atsignificant cost-savings is potentially enormous asshown in an early modelling study [104]The Male Circumcision Decision Makersrsquo Program

Planning Tool (DMPPT) developed recently by USAIDrsquosHealth Policy Initiative in collaboration with UNAIDShas estimated the cost and impact of scaling up MC ser-vices [131] Using this model an analysis of 14 prioritycountries in eastern and southern Africa found thatscaling up MC services to cover 80 of all adult menand newborn boys would over the period 2009-2015avert more than 4 million new adult HIV infections at acost of US$25 billion [132] This would yield total netsaving on cost of antiretroviral therapy (ART) of US$202 billion over the same period [132]In the DMPPT model annual costs for implementa-

tion were projected to increase in the early scale-upphase due to increased demand peaking in 2012 anddeclining thereafter to level off at around $100 millionby 2015 Even countries with moderate HIV prevalencesuch as Rwanda could reap significant savings in costsrelative to lifetime HIV treatment [133] Furthermorethe cost-effectiveness of MC even in non- or low-gener-alized HIV settings increases when the procedure isperformed in newborns [134135]Despite being targeted at sexually active men MC

provides important direct and indirect benefits towomen and children For example it was estimated thatin high-prevalence areas in Kenya and Zimbabwe ldquocir-cumcision confers a 46 reduction in the rate of male-to-female HIV transmissionrdquo with the effect of theintervention ldquodoubling the number of infections avertedamong womenrdquo [136] On the other hand a RCT inUganda of sero-discordant couples in which the manwas HIV-positive was discontinued for futility after217 of women in the intervention group and 134 inthe control group became infected [137] This differencewas not however statistically significant and many mendisobeyed instructions by resuming sexual intercoursebefore healing was complete [137] More recent findingsfrom a prospective multinational study in a similar sero-discordant population showed ldquono increased risk andpotentially decreased riskrdquo of infection due to MC to thefemale partners [138]Since women in sub-Saharan Africa show high accept-

ability of MC as part of comprehensive strategies forHIV prevention they can play an important role in theadoption and implementation of MC by changing malenorms and in promoting infant MC [9798139] By low-ering infection in men and thence women MC willreduce overall infection rate and lower the number of


Page 5 of 17

children being infected by their mother Infant MC ismoreover simpler more convenient entails lower riskand provides considerable savings in cost when com-pared with circumcision at a later age including thecost of treatment over the lifetime for HIV-infected peo-ple [132-135140141] As an example one study in theUSA indicated a 16 reduction in lifetime risk of HIVinfection in all males when circumcision is done ininfancy [134]The cost savings from circumcision of boys early in

life is considerably greater than this because they enterthe sexually active period of their life with a reducedrisk of various STIs [87142-146] In the Ugandan RCTof MC and HIV MC was associated with a 25 reduc-tion in prevalence in herpes simplex virus type 2 (HSV-2) 35 lower human papillomavirus (HPV) [147] andsignificantly reduced ulceration trichomonas and bac-terial vaginosis [148] In the South African MC triallow-risk HPV prevalence was 85 in the interventionarm compared with 158 in the control arm [149] Thestrong protective mechanism by which MC preventsSTIs in men likely involves both cellular and anatomicalfactors [105147]That MC affords protection against HIV and multiple

STIs in heterosexual men and their female sexual part-ners and thereby their children is not in doubt On theother hand the effect of MC in preventing HIV inMSM is less certain In a South African study HIV inMSM was 80 lower if they were circumcised [150] Ameta-analysis of studies from countries worldwideshowed 29 protection only for MSM who adopt pri-marily the insertive role [151] This was 73 in aCochrane analysis [152] Not included was a recentstudy of MSM in the high-prevalence setting of AndhraPradesh India where 186 of MSM were HIV positive[153] Although HIV was 70 lower in circumcisedreceptive-only MSM this was probably a result ofhomophily Further research in sub-Saharan Africa thattakes into account social and sexual networks in MSMis needed [152153]With the current strong evidence that MC protects

against HIV and several common STIs questions thatare important for policy consideration have arisenThese include adverse effects acceptability risk com-pensation reduced efficacy due to early return to sexafter MC disinhibition long-term consequences andexternal validity as well as ethical issues These havebeen addressed in numerous publications[1112879798116154-156] none of which regard theseconsiderations as representing a basis for rejecting MCas part of HIV prevention strategies For example thearguments of external validity raised by Green et al[157] ignore long-standing evidence from observationalstudies [5] and have been strongly refuted as unfounded

[158] In other examples studies on disinhibition [159]and risk compensation [155160] showed no increase inrisky sexual behaviour [160] or early resumption of sex[155]Follow-up data of the Kenya RCT [2] indicated an

ongoing increase in the protective effect of MC againstHIV infections at 42 months [161] and 54 months[162] By five years the protective effect reached 73 inthe Ugandan trial [163] These results suggest that thepositive effect of MC will continue [158] Howeverimplementation of national MC programmes triggeredby the RCT findings did not begin until 2008 [7] start-ing in Kenya [164] and thus the long-term populationimpact remains to be observed in those particular areasIn light of that it is imperative to continue monitoringsexual behaviour after circumcision for continuedassessment of long-term positive impact

Current state of practice in MC interventions insub-Saharan AfricaFollowing the recommendation by global health agenciesthat MC be adopted as one of the critical tools for HIVprevention in high-prevalence generalized heterosexualepidemics [1112] WHO and UNAIDS developed opera-tional guidelines for scaling up MC services [165] Pro-grammatic development has however been slow inlarge part as a consequence of suboptimal fundingIn 2008 researchers argued that the international

community was not committing enough resources toMC commensurate with the available evidence on whatworks [166] These authors noted that the 5 allocatedfor MC from an overall budget of $32 billion thatUNAIDS had estimated was needed to achieve universalcoverage for HIV programmes by 2010 fell far short ofthe estimated need and demand for MC especiallygiven its demonstrated efficacy relative to other inter-ventions Table 2 summarizes the current state of MCintervention policy strategies projected cost savings andinfections averted as well as MC provision to date inthe 14 priority African countries It can be seen thatprogrammatic development of MC to date is ongoing inall countries but differs markedly in extent [13101167]Implementation in Kenya the first country to com-

mence was spearheaded by a national task force on MCin 2008 [14] Other countries have or are in the processof developing similar policies implementation guidelinesand strategies Some like Kenya and Lesotho havedeveloped formal MC policies while others such asBotswana and Rwanda have incorporated MC intoexisting HIV prevention policies Translating scienceinto policy is often challenging [168] and we acknowl-edge that development of documents and programmesthrough consultative and collaborative processes invol-ving stakeholders in the health ministries HIVAIDS


Page 6 of 17

Table 2 Design and implementation of MC services for HIV prevention in 14 priority countries in east and southern Africa 2011

Country HIVprevalence

()

Mencircum-cised()

Policy framework Implementationstrategy plan

status

MC delivery structure Potential infectionsaverted by scalingup MC to 80 by2015 and maintainrate through 2025

TotalNet

Savings2009-2025(US$)

Circum-cisionsto date

Estimatednumber ofMCs neededto reach

80 target

Achievementtowards 80target ()

Botswana 176 112 MC as part of existing HIVprevention policy

In place Services integrated inexisting HIV prevention

strategies

62773 248million

11197 345244 32

Phased scale-upgoal 80 of 0-49years HIV-negativemen by 2014

Ethiopia 14 -National

93 -National

MC as an additional HIVprevention strategy Regional MCTask Force is to be establisheddraft regional MC strategicdirection document under

finalization

Underdevelopment

MC to be provided in100 of medical facilitiesin Gambella (one hospitaland 25 health centres)

1479 58million

5786 100000 58

60 -Gambella

46 -Gambella

Target to provideservices in 100 ofhealthcare facilities

in GambellaRegion

Kenya 7 - National 86-National

MC policy in place lsquoNationalGuidancersquo for MC

In place Stand alone andintegrated mobile clinics

prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza

Target to reach80 of 15-49 year

old men (11million men) andnewborns by 2013

Lesotho 24 52 MC policy in place In place MC to be integrated inHIV prevention services

focused in MNCH settings

106427 618million

4000 376795 1

Launched in 2010

Malawi 11 21 In place Nationaloperational planincludes voluntary

MC

Currently offered by free-standing clinics Scale-up

structure not yetdeveloped

240685 12billion

3119 2101566 01

Mozambique 12 52 Formal policy developed MC included inoperational planfor HIV prevention

MC services available ondemand adolescent andneonatal MC are planned

215861 15billion

7733 1059104 07

Rollout in pilotsites

Wam

aietalJournalof

theInternationalA

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20111449httpw

wwjiasocietyorgcontent14149

Page7of

17

Table 2 Design and implementation of MC services for HIV prevention in 14 priority countries in east and southern Africa 2011 (Continued)

Namibia 13 21 MC policy approved In place Stand-alone mobileservices are beingconsidered Plans tointegrate into hospital

services

18373 120million

1987 330218 06


Rwanda 3 12 Formal policy in developmentDetailed operational plan in place

In place Formal scale up started inthe military Plans to

integrate into standardHIV prevention services

56840 200million

1694 1746052 01

Detailedoperational planbeing rolled out

South Africa 18 42 Draft policy in place underfinalization

In place Facility based and stand-alone centres and campsscale up from OrangeFarm to 143 sites

1083869 65billion

131117 4333134 34

Currently beingscaled upnationwide

Swaziland 26 82 Policy adopted by cabinet In place Formal scale-up ofintegrated servicesstarted dedicated

ldquocircumcision Saturdaysrsquo

56810 332million

18869 183450 133

Tanzania 57 67 Policy under way Underdevelopment

Plans to target 8regions with highHIV and low MC

prevalence

Scale-up demonstrationsites MOVE strategyrecommended in the

public sector

202900 966million

18026 1373271 14

Uganda 64 25 Policy in place In place Piloted in the military anda mobile site plans tointegrate into routine

services

339524 2 billion 9052 4145184 02

Zambia 14 128 Cabinet approved MC as part ofHIV prevention policy

In place Multi-sectored approachfocused on militarypolice prisons andneonatal services

339632 24billion

81849 1949292 42

Target of 250000MCs a year MC

sites to increase to300 by 2014

Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17


Zimbabwe 14 10 Policy in place Underdevelopment(2010-2014)

Services offered throughmobile and free-standingsites and in public health

clinics Nationwideneonatal MC planned

565751 38billion

13977 1912595 07

Notes and data sources Ethiopia MC data (personal communication Hannah Gibson Country Director Jhpiego Ethiopia) and estimated target [173] Lesotho (4000 annual circumcisions before programmeintervention) [169] for Zimbabwe 30000 circumcisions have previously been reported [170] all other data [13132167171]

The 80 target in all three columns is for uncircumcised males 14-49 years

Wam

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Page9of

17

agencies non-governmental organizations academia anddonor partners as was the case in Kenya can be timeconsumingIt is nevertheless of concern that the numbers circum-

cised across the various countries three years after pol-icy recommendations are very low relative to targets(Table 2) The latest WHOUNAIDS report indicatescumulative circumcision figures up to 2010 since scale-up started in 2008 at 555202 ie 27 of the 208 mil-lion target [167] That 74 (410904) of these occurredin 2010 alone indicates that the momentum is risingbut needs to accelerate still As the DMPPT modellingindicates to achieve the projected outcomes the 14countries will need to reach 12 million circumcisions atpeak period in 2012 [132] Accordingly five countries(Malawi South Africa Tanzania Uganda and Zim-babwe) would require at least one million circumcisionseach in 2012 [132]In most of these countries MC prevalence varies by

region and it is logical that in the scale-up phase pro-grammes for MC deliberately target low MC localitiessuch as is occurring in Ethiopia Kenya and NamibiaHowever many of the current programmes are confinedto small or pilot settings Data available for Lesotho arepre-scale up [169] for Zimbabwe they are from severalclinical sites [167170] and for South Africa they havescaled-up from Orange Farm [171] where the RCT inthat country was conducted to over 140 sites [167] InGambella Ethiopia services are currently provided inone hospital and seven health centres (personal commu-nication Hannah Gibson Country Director JhpiegoEthiopia)With a growing demand for MC services and the

potential cost and life savings it is imperative that scaleup be rapidly accelerated [103] At the current rate ofservice provision 12 million MCs by 2012 across the 14countries are highly unlikely to be met so putting injeopardy many lives and failing to achieve the desiredcost savingsIn Kenya just 232200 MCs have been completed

[167] the largest number of any country A speeded-up rapid-results initiative intervention during a 30-dayperiod in 2009 conducted by 95 teams each of fourpersons at a range of 96-228 circumcisions per teamper day achieved 36000 circumcisions (Robert Baileypersonal communication) A similar intervention con-ducted over five weeks during November-December2010 achieved 51000 circumcisions (Robert Baileypersonal communication) At these rates Kenya wouldneed several similar rapid-results initiatives to reachthe national goal of one million circumcisions by 2013[172] Nevertheless Kenyarsquos programme is a model forother African countries and if adopted could advancethe 2012 goal

Many challenges stand in the way of implementingMC programmes These include cost need for trainingof health personnel other health system barriers thepolitics surrounding policy development funding andchanging socio-cultural perceptions and beliefs aboutMC [1394101164166172173] In Gambella Ethiopiathe regional hospital reportedly cannot meet even asmall demand of 10 circumcisions per week due to staffshortages and lack of training [173]Currently the most informative assessment of MC

programmes comes from Kenya [164] This reportreveals that of 81 government health facilities surveyedin Nyanza (the target location of MC services) nonehad the capacity to implement the full package of volun-tary circumcision outlined in the national guidelines[14] Challenges included lack of a theatre MC kits andsupplies medical personnel to perform the procedureand data monitoring tools Due to this most of thereported 230000 circumcisions were done by partnerorganizations largely in high-demand settings usingmobile teams [164] The Kenya programme offers manylessons for other countriesHealth provider training and service models being

developed will need to be tailored around specific exist-ing health systems and services infrastructure HIV epi-demiological profiles and determinants as well as MCprevalence and demand Reaching the estimated 100000men that need to be circumcised in Gambella Ethiopiafor example will require a massive increase in trainedpersonnel to conduct the surgical procedure [173] SinceMC programmes are targeting healthy men high stan-dards for surgical staff training and post-operative careare essential This includes strictly following establishednational and international guidelines for sterile surgicalpractice [111214144165]To increase the number of health personnel who can

perform safe circumcisions novel service models shouldbe adopted The rapid-results initiative pursued inKenya is based on intensive mobilization of resources(human equipment and financial) in high-demand set-tings through community approaches [164] Models forOptimizing the Volume and Efficiency of MC Services(MOVErdquo) is an additional approach for meetingdemand Currently practiced in South Africa it isfocused on increasing the efficiency of staff and time byconsidering alternate surgical methods and modifyingfacilities for efficient use [174] Consideration shouldalso be given to promoting task shifting for nurses andclinical officers as per WHO guidelines [175] Already inpractice in Kenya [164] and Zambia [167] it is a com-ponent of proposals in several other countries such asNamibia Lesotho [13]In some of the scale-up countries traditional circum-

cisers already used widely [72] can play a role in


0 of 17

meeting demand [176] but only if they receive adequatecertification for acceptable standards of surgical MC Onthe other hand as exemplified by the high (90) prefer-ence among men and women for medical MC in a tra-ditionally circumcising community from northernTanzania more efforts should be made to provide thismedical service in a culturally appropriate fashion soencouraging uptake [177]Preliminary data are also becoming available on

devices that could facilitate quicker and safer adult cir-cumcision [178] These include the Shang Ring [179](which produced good results for safety and acceptabil-ity in a field test in Kenya [180]) circumcision template[181] the recently acclaimed PrePex system [182] andthe Tara KLamp [183] for which further assessment isneeded [178] after adverse effects were initially reported[184] In an important development WHO has provideda framework for clinical evaluation of devices for adultMC [185] in addition to those already recommendedfor infant MC [144]

Where do we go from hereWhile welcoming continued debate about what drivesHIV in high-prevalence populations and what works inHIV prevention programmes we echo the call made byexperts and advocates four years ago [186] and morerecently [103] including a political declaration of theUnited Nations [187] urging an acceleration in imple-mentation of proven approaches such as MC There aremultiple reasons for reiterating this call First while theincidence of HIV is now declining in many countries insub-Saharan Africa nearly 70 of new HIV infectionsglobally remain in this region [22] The rate of newinfections therefore needs to decelerate much fasterthere if the crisis is to be stemmed Towards that endpolicy makers researchers and practitioners shoulddirect energy towards viable practical and efficacioussolutions in an accelerated campaignSecond MC could stem epidemics of HIV elsewhere

than Africa Based on current UNAIDS data the mainmode of infection globally (heterosexual transmission) isgrowing as reflected in the increasing proportion ofnew HIV infections reported in women for example to35 in 2009 from 21 in 1990 in Asia [22] Although inthe USA UK Russia Canada Australia and the Asianregion major exposure categories are MSM and inject-ing drug users higher incident HIV trends in womenand heterosexual contacts [22188] should ring alarmbells [143156189] Such recent trends are likely to beexacerbated by uneven and declining MC levels espe-cially in such countries as the USA and Australia whichtraditionally until the mid-1970s and early 1980s hadMC rates of more than 90 [190191] In Australia it isheartening that infant MC is again rising [156]

In such settings as the USA MC services are particu-larly crucial especially in African-Americans [189] whocomprise a disproportionately high number of personsliving with HIV [192193] and in whom perinatal infec-tion per 100000 infants is 123 compared with just 05in white infants [194] Furthermore African-Americanshave the highest heterosexual HIV rates [195] butnational data show that they also have rates of MClower than whites [190] Therefore given the currentepidemiological trends interventions need to focus onestablished patterns of transmission for which the popu-lation-level impact in reducing HIV infections will behigh now and in the futureThird current evidence from RCTs shows that in

comparison to a protective effect of 46 for prophylaxis[196] 39 for microbicides [197] and 312 for a vac-cine [198] at the moment MC with a 60 or higherefficacy [4] is the most effective biomedical HIV pre-vention strategy in heterosexual men Furthermore MCwill help reduce HIV in women [136] and children[140141143] as well as help lower risks for STIs[146-148] that exacerbate HIV risk [199200]As part of the internationally recognized priority inter-

ventions for stemming HIV [201] and given the currentstate of implementation massive catch-up strategies foradult MC seem to be the better investment in the shortterm Importantly mainstreaming of neonatal MC aspart of a long-term strategy is both logical and clearlymore cost effective [133134140143156] and will helpsystematize MC practice and services provision in theprimary healthcare system for future generationsFurthermore the much-needed scale up in sub-SaharanAfrica will require significant additional funds reorien-tation of expenditure allocation and better morerational use of the already existing largesse[132164166]Last continued research that addresses other issues

concerning MC will be valuable in addition to thosealready underway in various countries [13] In particularcareful research is needed to1 Regularly update the impact of MC on the HIV epi-

demic in the targeted areas by monitoring behaviouralchanges following MC2 Compare different surgical approaches including

the use of different low-risk devices for adult MC tofurther improve on this procedure and the cost effec-tiveness of service models such as the rapid-resultsinitiative task shifting and ldquoMOVErdquo for acceleratingdelivery3 Explore novel hypotheses relevant to prevention

messaging for example does MC make condom useeasier andor more pleasurable4 Evaluate how to best integrate MC messages into

existing communications and prevention programmes


Page 11 of 17

5 Develop strategies to improve the safety of tradi-tional MC practices and norms so that these can beincorporated into regular scale-up programmes withoutincreasing overall risk in order to speed up MCprogrammes6 Examine the effect of MC scale up on the health

services and health system resources (human and infra-structural) as well as integration of the practice in theformal healthcare system7 Establish the definitive biologic mechanism by

which MC protects against HIV infection through thepenis8 Assess the role of MC as a potential platform for

promoting menrsquos health including participation bywomen in order to encourage couple sexual and repro-ductive health9 Evaluate the integration of routine newborn MC in

maternal-child health programmes

ConclusionsPublic health campaigns aimed at stemming the spreadof HIVAIDS should address all known transmissionroutes as specific epidemiological resources and contex-tual factors demand We support the continued promo-tion of the use of all effective methods The effect ofdoing so will be cumulative We realize that MC defini-tively disrupts the major mode of HIV transmission insub-Saharan Africa We also realize that historical cul-tural and political controversies surrounding MC [8688]may provoke passionate debates However as Collinsargues it is imperative that values underpinning scienti-fic thought form the centre of public policy interven-tions [17]Given the present body of evidence and contingent on

certain pre-conditions (eg that MC is conducted by aqualified practitioner under acceptable conditions ofhygiene in the absence of contra-indications) at thispoint in time it is clear that medical MC in infancychildhood or adulthood produces far greater good thanharm We urge policy makers to more urgently facilitateimplementation of MC as a public health measure tostem the growing heterosexual transmission of HIVworldwide and in sub-Saharan Africa to more quicklyreduce future epidemics Not only is MC highly effica-cious against HIV acquisition but it also confers multi-ple other health benefits thus making it quite rightly aldquosurgical vaccinerdquo for the 21st century [187103116154]

Author details1Department of African-American Studies Northeastern University BostonMA USA 2School of Medical Sciences University of Sydney Australia3Research amp Education Association on Circumcision Health EffectsBloomington MN USA 4Behavioral and Biomedical Research Family HealthInternational Research Triangle Park NC USA 5Department of MedicineUniversity of California San Francisco Department of Public Health USA

6College of Professional Studies Northeastern University Boston MA USA7Makerere University College of Health Sciences Kampala Uganda 8KirbyInstitute St Vincents Hospital and University of New South Wales SydneyAustralia 9Population Council One Dag Hammarskjold Plaza New York NYUSA 10Perinatal HIV Research Unit New Nurses Home Chris HaniBaragwanath Hospital Johannesburg South Africa 11Alcohol amp Drug Unit StVincentrsquos Hospital Sydney Australia 12Global Youth Coalition on HIVAIDSPretoria South Africa

Authorsrsquo contributionsRGW and BJM conceptualized the manuscript RGW drafted and developedthe manuscript BJM did extensive reviews of subsequent drafts RA wasinvolved in editing and formatting the manuscript in various stages SAB DSJDK NS DAC JB GB and ADW were involved in the early iteration of themanuscript and reviewed and made substantive contributions to the draftsDS provided crucial data on male circumcision implementation JBE readand provided insightful comments in the final revisions All authors havecontributed substantively in critically revising the content of the manuscriptAll authors have read and approved the manuscript

Competing interestsThe authors declare that they have no competing interests

Received 1 March 2011 Accepted 20 October 2011Published 20 October 2011

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Randomized controlled intervention trial of male circumcision forreduction of HIV infection risk The ANRS 1265 Trial PLoS Med 200521112-1122

2 Bailey RC Moses S Parker CB Agot K Maclean I Krieger JN Williams CFCampbell RT Ndinya-Achola JO Male circumcision for HIV prevention inyoung men in Kisumu Kenya A randomised controlled trial Lancet 2007369643-646

3 Gray RH Kigozi G Serwadda D Makumbi F Watya S Nalugoda FKiwanuka N Moulton LH Chaudhary MA Chen MZ Sewankambo NKWabwire-Mangen F Bacon MC Williams CF Opendi P Reynolds SJLaeyendecker O Quinn TC Wawer MJ Male circumcision for HIVprevention in men in Rakai Uganda A randomised trial Lancet 2007369657-666

4 Siegfried N Muller M Volmink J Deeks JJ Egger M Low N Weiss HWalker S Williamson P Male circumcision for prevention of heterosexualacquisition of HIV in men (Review) Cochrane Database of Syst Rev 2009 2CD003362

5 Lie RK Miller FG What counts as reliable evidence for public healthpolicy the case of circumcision for preventing HIV infection BMC MedRes Methodol 2011 1134

6 Weiss HA Halperin D Bailey RC Hayes RJ Schmid G Hankins CA Malecircumcision for HIV prevention from evidence to action AIDS 200822567-574

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8 Mills E Cooper C Anema A Guyatt A Male circumcision for theprevention of heterosexually acquired HIV infection a meta-analysis ofrandomized trials involving 11050 men HIV Med 2008 9332-335

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Page 12 of 17

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21 Gisselquist D Potterat JJ St Lawrence JS Hogan M Arora NK Correa MDinsmore WW Mehta G Millogo J Muth SQ Okinyi M Ounga T How tocontain generalized HIV epidemics A plea for better evidence todisplace speculation Int J STD AIDS 2009 20443-446

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27 Robinson NJ Mulder DW Auvert B Hayes RJ Modelling the impact ofalternative HIV intervention strategies in rural Uganda AIDS 199591263-1270

28 Leclerc PM Matthews AP Garenne ML Fitting the HIV epidemic inZambia a two-sex micro-simulation model PLoS One 2009 4e5439

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33 Stover J Johnson P Hallett T Marston M Becquet R Timaeus IM TheSpectrum projection package improvements in estimating incidence byage and sex mother-to-child transmission HIV progression in childrenand double orphans Sex Transm Infect 2010 86(Suppl 2)ii16e21

34 Ghys P Garnett GP The 2009 HIV and AIDS estimates and projectionsmethods tools and analyses Sex Transm Infect 2010 86ii1-ii2

35 UNAIDS Reference Group on Estimates Modeling and Projections[httpwwwepidemorg]

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42 Auvert B Buveacute A Ferry B Caraeumll M Morison L Lagarde E Robinson NJKahindo M Chege J Rutenberg N Musonda R Laourou M Akam E StudyGroup on the Heterogeneity of HIV Epidemics in African Cities Ecologicaland individual level analysis of risk factors for HIV infection in foururban populations in sub-Saharan Africa with different levels of HIVinfection AIDS 2001 15(Suppl)S15-S30

43 Buve A The HIV epidemics in sub-Saharan Africa why so severe Whyso heterogenous An epidemiological perspective In The HIVAIDSEpidemic in Sub-Saharan Africa in a Historical Perspective Edited by Denis PBecker C Senegalese Network ldquoLaw Ethics Healthrdquo 200641-55

44 Sobngwi-Tambekou J Taljaard D Lissouba P Zarca K Puren A Lagarde EAuvert B Effect of HSV-2 serostatus on acquisition of HIV by young menresults of a longitudinal study in Orange Farm South Africa J Infect Dis2009 199958-964

45 Buveacute A Caraeumll M Hayes RJ Auvert B Ferry B Robinson NJ Anagonou SKanhonou L Laourou M Abega S Akam E Zekeng L Chege J Kahindo MRutenberg N Kaona F Musonda R Sukwa T Morison L Weiss HA Laga MStudy Group on Heterogeneity of HIV Epidemics in African CitiesMulticentre study on factors determining differences in rate of spread ofHIV in sub-Saharan Africa methods and prevalence of HIV infectionAIDS 2001 15(Suppl 4)S5-S14

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47 Shelton JD Why multiple sexual partners Lancet 2009 374-36748 Morris M Barking up the wrong evidence tree Comment on Lurie amp

Rosenthal lsquorsquoConcurrent partnerships as a driver of the HIV epidemic inSub-Saharan Africa The evidence is limitedrdquo AIDS Behav 2010 1431-33

49 Mishra V Assche SBV Concurrent sexual partnerships and HIV infectionEvidence from national population based surveys 2009 [httpwwwmeasuredhscompubspdfWP62WP62pdf] DHS Working Paper 62


51 Reniers G Tfaily R Polygyny and HIV in Malawi Demographic Resh 2008191811-1830

52 One Love Multiple and concurrent sexual partnerships in Southern Africa aten country research report [httpwwwonelovesouthernafricaorgwp-contentuploads200901mcp-reportwith-cover-finalpdf]

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54 Morris M Kretzschmar M Concurrent partnerships and transmissiondynamics in networks Social Networks 1995 17299-318

55 Lurie MN Rosenthal S Concurrent partnerships as a driver of the HIVepidemic in sub-saharan Africa The evidence is limited AIDS Behav2010 1417-24

56 Sawers L Stillwaggon E Concurrent sexual partnerships do not explainthe HIV epidemics in Africa a systematic review of the evidence J IntAIDS Soc 2010 1334

57 World Bank and USAID Emerging Issues in todayrsquos HIV response[httpsiteresourcesworldbankorgINTHIVAIDSResources375798-1297872065987Debate4SUMMARYConcurrentSexualPartnershipspdf]

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60 Mathers BM Degenhardt L Phillips B Wiessing L Hickman M Strathdee SAWodak A Panda S Tyndall M Toufik A Mattick RP 2007 Reference Group


Page 13 of 17

to the UN on HIV and Injecting Drug Use Global epidemiology ofinjecting drug use and HIV among people who inject drugs asystematic review Lancet 2008 3721733-1745

61 Gouws E White PJ Stover J Brown T Short term estimates of adult HIVincidence by mode of transmission Kenya and Thailand as examplesSex Transm Infect 2006 82(Suppl 3)iii51-iii55

62 Mishra V Khan S Liu L Kottiri B Medical Injection Use and HIV in Sub-Saharan Africa DHS comparative studies no 21 Calverton MacroInternational 2008 [httpwwwmeasuredhscompubspdfCR21CR21pdf]

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65 Smith AD Tapsoba P Peshu N Sanders EJ Jaffe HW Men who have sexwith men and HIVAIDS in sub-Saharan Africa Lancet 2009 374416-422

66 Baral S Sifakis F Cleghorn F Beyrer C Elevated risk for HIV infectionamong men who have sex with men in low- and middle-incomecountries 2000-2006 A systematic review PLoS Med 2007 4e339

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68 Ounga T Okinyi M Onyuro S Correa M Gisselquist D Exploratory study ofblood exposures that are risks for HIV among Luo and Kisii ethnicgroups in Nyanza province Kenya Int J STD AIDS 2009 2019-23

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75 Hiemstra R Rabie H Schaaf HS Eley B Cameron N Mehtar S Janse vanRensburg A Cotton MF Unexplained HIV-1 infection in children ndashdocumenting cases and assessing for possible risk factors S Afr Med J2004 94188-193

76 Schmid GP Buveacute A Mugyenyi P Garnett GP Hayes RJ Williams BGCalleja JG De Cock KM Whitworth JA Kapiga SH Ghys PD Hankins CZaba B Heimer R Boerma JT Transmission of HIV-1 infection in sub-Saharan Africa and effect of elimination of unsafe injections Lancet2004 363482-488

77 de Walque D Do unsafe tetanus toxoid injections play a significant rolein the transmission of HIVAIDS Evidence from seven African countriesSex Transm Infect 2008 84122-125

78 Khobotlo M Tshehlo R Nkonyana J Ramoseme M Khobotle M Chitoshia AHildebrand M Fraser N Lesotho HIV prevention response and modes oftransmission analysis Maseru Lesotho National AIDS Commission 2009

79 Mngadi S Fraser N Mkhatshwa H Lapidos P Khumalo T Tsela SNhlabatsi N Odido H Swaziland HIV prevention response and modes oftransmission analysis Mbabane National Emergency Response Council onHIVAIDS 2009

80 Wabwire-Mangen F Odiit M Kirungi W Kisitu DK Wanyama JO UgandaHIV modes of transmission and prevention response analysis KampalaUganda National AIDS Commission 2009

81 Mulenga O Witola H Buyu C Gboun M Sunkutu MR Rodriguez-Garcia RGorgens M Fraser-Hurt N Sattin E Potter D Dzekedzeke K Banda RMichelo C Zambia HIV prevention response and modes of transmissionanalysis Lusaka Zambia National HIVAIDSSTITB Council 2009

82 Baral S Dausab F Masenior N Iipinge S Beyrer C A Systematic Review ofHIV epidemiology and risk factors among MSM in Sub-Saharan Africa

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83 Sanders EJ Graham SM Okuku HS van der Elst EM Muhaari A Davies APeshu N Price M McClelland HIV-1 infection in high risk men who havesex with men in Mombasa Kenya AIDS 2007 212513-2520

84 Brody S Potterat JJ Establishing valid AIDS monitoring and research incountries with generalized epidemics Int J STD AIDS 2004 151-6

85 Lagarde E Caraeumll M Auvert B Buve A Concurrency and sexualtransmission a response to the letter by Rothenberg et al AIDS 200216679-680

86 Kaicher DC Swan KG A Cut Above Circumcision as an ancient statussymbol Urology 2010 7618-20

87 Morris BJ Why circumcision is a biomedical imperative for the 21stcentury BioEssays 2007 291147-1158

88 Gollaher D A History of the Worldrsquos Most Controversial Surgery New York2000

89 Alcena V AIDS in third world countries New York State J Med 198686446

90 Fink AJ A possible explanation for heterosexual male infection withAIDS N Engl J Med 1986 3151167

91 Bongaarts J Reining P Way P Conant F The relationship between malecircumcision and HIV infection in African populations AIDS 19893373-377

92 Gray RH Kiwanuka N Quinn TC Sewankambo NK Serwadda DMangen FW Lutalo T Nalugoda F Kelly R Meehan M Chen MZ Li CWawer MJ Male circumcision and HIV acquisition and transmissioncohort studies in Rakai Uganda AIDS 2000 142371-2381

93 Siegfried N Muller M Deeks J Volmink J Egger M Low N Walker SWilliamson P HIV and male circumcision - a systematic review withassessment of the quality of studies Lancet Infect Dis 2005 5165-173

94 Drain PK Halperin DT Hughes JP Klausner JD Bailey RC Malecircumcision religion and infectious diseases An ecologic analysis of118 developing countries BMC Infect Dis 2006 6172

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99 Williams BG Lloyd-Smith JO Gouws E Hankins C Getz WM Hargrove J deZoysa I Dye C Auvert B The potential impact of male circumcision onHIV in sub-Saharan Africa PLoS Med 2006 3e262

100 Sawires SR Dworkin SL Fiamma A Peacock D Szekeres G Coates TJ Malecircumcision and HIVAIDS challenges and opportunities Lancet 2007369708-713

101 De Bruyn G Martinson N Gray GE Male circumcision for HIV preventiondevelopments from sub-Saharan Africa Expert Rev Anti Infect Ther 2010823-31

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106 Patterson BK Landay A Siegel JN Flener Z Pessis D Chaviano A Bailey RCSusceptibility to human immunodeficiency virus-1 infection of humanforeskin and cervical tissue grown in explant culture Am J Pathol 2002161867-873

107 de Witte L Nabatov A Pion M Fluitsma D de Jong MAWP de Gruijl TPiguet V van Kooyk Y Geijtenbeek1 TBH Langerin is a natural barrier toHIV-1 transmission by Langerhans cells Nat Med 2007 13367-371

108 Ganor Y Zhou Z Tudor D Schmitt A Vacher-Lavenu MC Gibault LThiounn N Tomasini J Wolf JP Bomsel M Within 1 h HIV-1 uses viral


Page 14 of 17

synapses to enter efficiently the inner but not outer foreskin mucosaand engages Langerhans-T cell conjugates Mucosal Immunol 20103506-522

109 Ganor Y Bomsel M HIV-1 Transmission in the male genital tract Am JReprod Immunol 2011 65284-291

110 Dinh MH McRaven MD Kelley ZL Penugonda S Hope TJ Keratinization ofthe adult male foreskin and implications for male circumcision AIDS2010 24899-906

111 Qin Q Zheng XY Wang YY Shen HF Sun F Ding W Langerhansrsquo celldensity and degree of keratinization in foreskins of Chinese preschoolboys and adults Int Urol Nephrol 2009 41747-753

112 Fischetti L Barry SM Hope TJ Shattock RJ HIV-1 infection of humanpenile explant tissue and protection by candidate microbicides AIDS2009 23319-328

113 Dinh MH Fahrbach KM Hope TJ The role of the foreskin in malecircumcision an evidence-based review Am J Reprod Immunol 201065279-283

114 Ministry of Health National AIDS and STI Control Program Kenya AIDSIndicator Survey 2007 Nairobi 2008

115 Gebremedhin S Assessment of the Protective Effect of MaleCircumcision from HIV Infection and Sexually Transmitted DiseasesEvidence from 18 Demographic and Health Surveys in Sub-SaharanAfrica Afr J Reprod Health 2010 14105-113

116 Wamai RG Weiss HA Hankins C Karim QA Shisana O Bailey RCBetukumesu B Bongaarts J Bowa K Cash R Cates W Diallo MO Dludlu SGeffen N Heywood M Jackson H Kayembe PK Kapiga S Kebaabetswe PKintaudi L Klausner JD Leclerc-Madlala S Mabuza K BenjaminMakhubele M Micheni K Morris BJ de Moya A Ncala J Ntaganira INyamucherera OF Otolorin EO Pape JW Phiri M Rees H Ruiz M Sanchez JSawires S Seloilwe ES Serwadda DM Setswe G Sewankambo NSimelane D Venter F Wilson D Woelk G Zungu N Halperin DT Malecircumcision is an efficacious lasting and cost-effective strategy forcombating HIV in high-prevalence AIDS epidemics time to movebeyond debating the science Fut HIV Ther 2008 2399-405

117 Gersovitz M The HIV epidemic in four African countries seen throughthe demographic and health surveys J Afr Econ 2005 14191-246

118 Tanzania Commission for AIDS (TACAIDS) National Bureau of Statistics(NBS) ORC Macro Tanzania HIVAIDS Indicator Survey 2003-04 CalvertonMaryland USA TACAIDS NBS and ORC Macro 2005 [httpwwwtgpshortzfileadminuploadsdocsTHIS_FINAL_2005pdf]

119 Lowndes CM Alary M Belleau M Bosu WK Kintin DF Nnorom JA Seck KVictor-Ahuchogu J Wilson D West Africa HIVAIDS epidemiology andresponse synthesis implications for prevention Washington DC World Bank2008

120 Piot P Greener R Russell S Squaring the circle AIDS poverty and humandevelopment PLoS Med 2007 4e314

121 Brewer DD Potterat JJ Roberts JM Brody S Male and female circumcisionassociated with prevalent HIV infection in virgins and adolescents inKenya Lesotho and Tanzania Ann Epidemiol 2007 17217-226

122 Keele BF Van Heuverswyn F Li Y Bailes E Takehisa J Santiago ML Bibollet-Ruche F Chen Y Wain LV Liegeois F Loul S Ngole EM Bienvenue YDelaporte E Brookfield JFY Sharp PM Shaw GM Peeters M Hahn BHChimpanzee reservoirs of pandemic and nonpandemic HIV-1 Science2006 313523-526

123 Lemey P Pybus OG Wang B Saksena NK Salemi M Vandamme AMTracing the origin and history of the HIV-2 epidemic Proc Natl Acad SciUSA 2003 1006588-6592

124 Eyawo O de Walque D Ford N Gakii G Lester RT Mills EJ HIV status indiscordant couples in sub-Saharan Africa a systematic review and meta-analysis Lancet Infect Dis 2010 10770-777

125 Kahn JG Marseille E Auvert B Cost-effectiveness of male circumcision forHIV prevention in a South African setting PLoS Med 2006 3e517

126 Gray RH Li X Kigozi G Serwadda D Nalugoda F Watya S Reynolds SJWawer M The impact of male circumcision on HIV incidence and costper infection prevented a stochastic simulation model from RakaiUganda AIDS 2007 21845-850

127 Londish GJ Murray JM Significant reduction in HIV prevalence accordingto male circumcision intervention in sub-Saharan Africa Int J Epidemiol2008 371246-1253

128 Galarraga O Colchero A Wamai RG Bertozzi SM HIV Prevention Cost-Effectiveness A Systematic Review BMC Public Health 2009 9(Suppl 1)S5

129 Uthman OA Popoola TA Uthman MMB Olatunde A Economic evaluationsof adult male circumcision for prevention of heterosexual acquisition ofHIV in men in sub-Saharan Africa a systematic review PLoS One 2010 5e9628

130 UNAIDSWHOSACEMA Expert Group on Modeling the Impact and Cost ofMale Circumcision for HIV Prevention Male circumcision for HIVprevention in high HIV prevalence settings what can mathematicalmodeling contribute to informed decision making PLoS Med 2009 6e1000109

131 Health Policy Initiative Male Circumcision Decisionmakers Tool [httpwwwhealthpolicyinitiativecomindexcfmid=softwareampget=MaleCircumcision]

132 USAID Health Policy Initiative The Potential Cost and Impact of ExpandingMale Circumcision in 14 African Countries [httpwwwmalecircumcisionorgprogramsdocuments14_country_summary11309pdf]

133 Binagwaho A Pegurri E Muita J Bertozzi S Male circumcision at differentages in Rwanda a cost-effectiveness study PLoS Med 2010 7e1000211

134 Sansom SL Prabhu VS Hutchinson AB An Q Hall HI Shrestha RK Lasry ATaylor AW Cost-effectiveness of newborn circumcision in reducinglifetime HIV risk among US males PLoS One 2010 5e8723

135 White RG Glynn JR Orroth KK Freeman EE Bakker R Weiss HAKumaranayake L Habbema JD Buveacute A Hayes RJ Male circumcision forHIV prevention in sub-Saharan Africa who what and when AIDS 2008221841-1850

136 Hallett TB Alsallaq RA Baeten JM Weiss H Celum C Gray R Abu-Raddad LWill circumcision provide even more protection from HIV to women andmen New estimates of the population impact of circumcisioninterventions Sex Transm Infect 2011 8788-93

137 Wawer MJ Makumbi F Kigozi G Serwadda D Watya S Nalugoda FBuwembo D Ssempijja V Kiwanuka N Moulton LH Sewankambo NKReynolds SJ Quinn TC Opendi P Iga B Ridzon R Laeyendecker O Gray RHCircumcision in HIV-infected men and its eff ect on HIV transmission tofemale partners in Rakai Uganda a randomised controlled trial Lancet2009 374229-237

138 Baeten JM Donnell D Kapiga SH Ronald A John-Stewart G Inambao MManongi R Vwalika B Celum C Partners in Prevention HSVHIVTransmission Study Team Male circumcision and risk of male-to-femaleHIV-1 transmission a multinational prospective study in African HIV-1-serodiscordant couples AIDS 2010 24737-744

139 Centre for HIVAIDS Prevention Studies Women and MMC interview withProf Bertran Auvert Centre for HIVAIDS Prevention Studies 2011

140 Schoen EJ Oehrli M Colby CJ Machin G The highly protective effect ofnewborn circumcision against invasive penile cancer Pediatrics 2000 105e36

141 UNAIDS Neonatal and child male circumcision a global review [httpwwwmalecircumcisionorgresearchdocumentsNeonatal_child_MC_global_reviewpdf]

142 Weiss GN Prophylactic neonatal surgery and infectious diseases PediatInfect Dis J 1997 16727-734

143 Tobian AA Gray RH Quinn TC Male circumcision for the prevention ofacquisition and transmission of sexually transmitted infections the casefor neonatal circumcision Arch Pediatr Adolesc Med 2010 16478-84

144 WHO and Jhpiego Manual for early infant male circumcision under localanaesthesia [httpwhqlibdocwhointpublications20109789241500753_engpdf]

145 MacNeily AE Afshar K Circumcision and non-HIV sexually transmittedinfections Can Urol Assoc J 2011 558-59

146 Morris BJ Gray RH Castellsague X Bosch FX Halperin DT Waskett JHHankins CA The strong protective effect of circumcision against cancerof the penis Adv Urol 2011 1-21 Article ID 812368

147 Tobian AA Serwadda D Quinn TC Kigozi G Gravitt PE Laeyendecker OCharvat B Ssempijja V Riedesel M Oliver AE Nowak RG Moulton LHChen MZ Reynolds SJ Wawer MJ Gray RH Male circumcision for theprevention of HSV-2 and HPV infections and syphilis N Engl J Med 20093601298-1309

148 Gray RH Kigozi G Serwadda D Makumbi F Nalugoda F Watya SMoulton L Chen MZ Sewankambo NK Kiwanuka N Sempijja V Lutalo TKagayii J Wabwire-Mangen F Ridzon R Bacon M Wawer MJ The effects ofmale circumcision on female partnersrsquo genital tract symptoms andvaginal infections in a randomized trial in Rakai Uganda Am J ObstetGynecol 2009 20042e1-42e7


Page 15 of 17

149 Tarnaud C Lissouba P Cutler E Puren A Taljaard D Auvert B Associationof low-risk human papillomavirus infection with male circumcision inyoung men results from a longitudinal study conducted in orange farm(South Africa) Infect Dis Obstet Gynecol 2011 2011567408

150 Lane T Raymond HF Dladla S Rasethe J Struthers H McFarland WMcIntyre J High HIV prevalence among men who have sex with men inSoweto South Africa Results from the Soweto Menrsquos Study AIDS Behav2011 15626-634

151 Millett GA Flores SA Marks G Reed JB Herbst JH Circumcision status andrisk of HIV and sexually transmitted infections among men who havesex with men a meta-analysis JAMA 2008 3001674-1684

152 Wiysonge CS Kongnyuy EJ Shey M Muula AS Navti OB Akl EA Lo YRMale circumcision for prevention of homosexual acquisition of HIV inmen Cochrane Database Syst Rev 2011 6CD007496

153 Schneider JA Michaels S Gandham SR McFadden R Liao C Yeldandi VVOruganti G A protective effect of circumcision among receptive malesex partners of Indian men who have sex with men AIDS Behav 2011

154 Rennie S Muula AS Westreich D MC and HIV prevention - ethicalmedical and public health tradeoffs in low-income countries J MedEthics 2007 33357-361

155 Mehta SD Gray RH Auvert B Moses S Kigozi G Taljaard D Puren AAgot K Serwadda D Parker CB Wawer MJ Bailey RC Does sex in the earlyperiod after circumcision increase HIV-seroconversion risk Pooledanalysis of adult male circumcision clinical trials AIDS 2009 231557-1564

156 Cooper DA Wodak AD Morris BJ The case for boosting infant malecircumcision in the face of rising heterosexual transmission of HIV Med JAust 2010 193318-319

157 Green LW Travis JW McAllister RG Peterson KW Vardanyan AN Craig AMale circumcision and HIV prevention insufficient evidence andneglected external validity Am J Prev Med 2010 39479-482

158 Banerjee J Klausner JD Halperin DT Wamai R Schoen EJ Moses SMorris BJ Bailis SA Venter F Martinson N Coates TJ Gray G Bowa KCircumcision Denialism Unfounded and Unscientific Am J Prev Med 201140e11-e12

159 Agot KE Kiarie JN Nguyen HQ Odhiambo JO Onyango TM Weiss NSMale circumcision in Siaya and Bondo districts Kenya prospectivecohort study to assess behavioral disinhibition following circumcision JAcquir Immune Defic Syndr 2007 4466-70

160 Mattson CL Campbell RT Bailey RC Agot K Ndinya-Achola JO Moses SRisk compensation is not associated with male circumcision in KisumuKenya a multi-faceted assessment of men enrolled in a randomizedcontrolled trial PLoS One 2008 3e2443

161 Bailey RC Moses S Parker CB Agot K Maclean I Krieger JN Williams CFNdinya-Achola JO The protective effect of male circumcision is sustainedfor at least 42 months results from the Kisumu Kenya Trial XVIIInternational AIDS Conference 2008 Abstract THAC05

162 Bailey RC Moses S Parker CB Agot K MacLean I Krieger JN Williams CFMNdinya-Achola JO The protective effect of adult male circumcisionagainst HIV acquisition is sustained for at least 54 months results fromthe Kisumu Kenya trial XVIII International AIDS Conference Jul 18-23 2010Vienna 2010 Abstract FRLBC1

163 Kong X Kigozi G Ssempija V Serwadda D Nalugoda F Makumbi FLutalo T Watya S Wawer M R Gray R Longer-term effects of malecircumcision on HIV incidence and risk behaviors during post-trialsurveillance in Rakai Uganda 18th Conference on Retroviruses andOpportunistic Infections Boston 2011 Abstract 36

164 Herman-Roloff A Llewellyn E Obiero W Agot K Ndinya-Achola JMuraguri N Bailey RC Implementing voluntary medical malecircumcision for HIV prevention in Nyanza Province Kenya Lessonslearned during the first year PLoS ONE 2011 6e18299

165 WHOUNAIDS Operational guidance for scaling up male circumcision servicesfor HIV prevention Geneva UNAIDS[httpwwwwhointhivpubmalecircumcisionwho_hiv_mc_opguidepdf]

166 Potts M Halperin DT Kirby D Swidler A Marseille E Klausner JD Hearst NWamai RG Kahn JG Walsh J Reassessing HIV prevention Science 2008320749-750

167 WHOUNAIDS Progress in scale-up of male circumcision for HIV prevention inEastern and Southern Africa Focus on service delivery [httpwwwmalecircumcisionorgdocumentsMC_country_12sept11apdf]

168 Gebbie KM Science and policy a perpetual dilemma AIDS Reader 200919100-101

169 Ministry of Health and Social Welfare Government of Lesotho MaleCircumcision in Lesotho Situation Analysis Report [httpwwwnasorglsdocumentsMALE_CIRCUMCISION_REPORT-FINALpdf]

170 Bugalo B Government targets circumcising 12m males by 2015 Newsday2011 [httpwwwnewsdaycozwarticle2011-06-12-government-targets-circumcising-12m-males-by-2015]

171 Dickson K Farley T Male circumcision scale-up 17th Conference onRetroviruses and Opportunistic Infections (CROI) 2010 San FranciscoAbstract oral62

172 Nyanza Provincial Task Force on Male Circumcision Nyanza UpdateQuarterly Provincial Newsletter on the voluntary medical male circumcisionprogram 2009 [httpwwwmalecircumcisionorgprogramsdocumentsNyanza_Newsletter100210pdf]

173 Patrick DM Schneiderman J Kinahan T Pollock N Marsquoayan S IntegratingMale Circumcision (MC) into HIV Prevention Efforts Our Learning in EthiopiaKenya and Rwanda Canadian Institute of Health Research 2009 [httpwwwbccdccaNRrdonlyres8A389970-CA25-4212-ACE3-6374104AC85B0Epid_research_Integrating_MC_HIV_2009_06_15pdf]

174 WHO Considerations for Implementing Models for Optimizing the Volume andEfficiency of Male Circumcision Services for HIV Prevention [httpwwwmalecircumcisionorgprogramsdocumentsmc_MOVE_2010_webpdf]

175 WHO Task Shifting Rational Redistribution of Tasks Among Health WorkforceTeams Global Recommendations and Guidelines Geneva 2008

176 Mboera LEG Massaga JJ Senkoro KP Kilima SP Mayala BK Msovela JShayo EH Challenges and Opportunities for the involvement of TraditionalPractitioners in Scaling up Safe Male Circumcision in the Context of HIVPrevention in Tanzania National Institute for Medical Research Dar esSalaam Tanzania 2009 [httpmalecircumcisionorgprogramsdocumentsTraditional_Providers_final_report1pdf]

177 Wambura M Mwanga JR Mosha JF Mshana G Mosha F Changalucha JAcceptability of medical male circumcision in the traditionallycircumcising communities in Northern Tanzania BMC Public Health 201111373

178 Morris BJ Eley C Male circumcision An appraisal of currentinstrumentation In Biomedical Engineering In Biomedical Engineering -From Theory to Applications Edited by Fazel-Rezai R 2011 InTech

179 Masson P Li PS Barone MA Goldstein M The ShangRing device forsimplified adult circumcision Nat Rev Urol 2010 7638-642

180 Barone MA Ndede F Li PS Masson P Awori Q Okech J Cherutich PMuraguri N Perchal P Lee R Kim HH Goldstein M The Shang Ring devicefor adult male circumcision a proof of concept study in Kenya J AcquirImmune Defic Syndr 2011 57e7-e12

181 Decastro B Gurski J Peterson A Adult template circumcision aprospective randomized patient-blinded comparative study evaluatingthe safety and efficacy of a novel circumcision device Urology 201076810-814

182 Bitega JP Ngeruka ML Hategekimana T Asiimwe A Binagwaho A Safetyand efficacy study of the PrePex system for male circumcision 18thConference on Retroviruses and Opportunistic Infections Boston 2011Abstract 1007

183 Peng Y-F Cheng Y Wang GY Wang SQ Jia C Yang BH Zhu R Jian SCLi QW Geng DW Clinical application of a new device for minimallyinvasive circumcision Asian J Androl 2008 10447-454

184 Lagarde E Taljaard D Puren A Auvert B High rate of adverse eventsconsecutive to circumcision of young male adults with the Tara KLamptechnique Results from a randomized trial conducted in South Africa SAfr Med J 2009 99163-169

185 WHO Framework for clinical evaluation of devices for adult male circumcision2011 [httpwwwmalecircumcisionorgprogramsdocumentsMC_device_evaluation_framework_Feb11pdf]

186 Global HIV Prevention Working Group Bringing HIV prevention to scale anurgent global priority 2007 [httpwwwmalecircumcisionorgadvocacydocumentsPWG_HIV_prevention_report_webpdf]

187 United Nations General Assembly Political Declaration on HIVAIDSIntensifying our Efforts to Eliminate HIVAIDS [httpwwwunaidsorgenmediaunaidscontentassetsdocumentsdocument20110620110610_UN_A-RES-65-277_enpdf] Resolution adopted by the GeneralAssembly on 10 June 2011

188 Kirby Institute [National Centre in HIV Epidemiology and Clinical Research]HIVAIDS Viral Hepatitis amp Sexually Transmissible Infections in Australia Annual


Page 16 of 17

Surveillance Report 2011 [httpwwwmedunsweduauNCHECRwebnsfresources2011$fileKIRBY_ASR2011pdf]

189 Smith DK Taylor A Kilmarx PH Sullivan P Warner L Kamb M Bock NKohmescher B Mastro TD Male circumcision in the United States for theprevention of HIV infection and other adverse health outcomes reportfrom a CDC consultation Public Health Rep 2010 125(Suppl 1)72-82

190 Xu F Markowitz LE Sternberg MR Aral SO Prevalence of circumcision andherpes simplex virus type 2 infection in men in the United States TheNational Health and Nutrition Examination Survey (NHANES) 1999-2004Sex Transm Dis 2007 34479-484

191 McKinney CM Klingler EJ Paneth-Pollak R Schillinger JA Gwynn RCFrieden TR Prevalence of adult male circumcision in the generalpopulation and a population at increased risk for HIVAIDS in New YorkCity Sex Transm Dis 2008 35814-817

192 Sutton MY Jones RL Wolitski RJ Cleveland JC Dean HD Fenton KA Areview of the Centers for Disease Control and Preventionrsquos response tothe HIVAIDS crisis among Blacks in the United States 1981-2009 Am JPublic Health 2009 99(Suppl 2)S351-S359

193 Hall HI Song R Rhodes P Prejean J An Q Lee LM Karon J Brookmeyer RKaplan EH McKenna MT Janssen RS HIV Incidence Surveillance GroupEstimation of HIV incidence in the United States JAMA 2008 300520-529

194 Centers for Disease Control and Prevention Racialethnic disparitiesamong children with diagnoses of perinatal HIV infection - 34 states2004-2007 MMWR 2010 5997-101

195 Centers for Disease Control and Prevention Racialethnic disparities indiagnoses of HIVAIDS ndash 33 states 2001-2005 MMWR 2007 56189-193

196 Grant RM Lama JR Anderson PL McMahan V Liu AY Vargas LGoicochea P Casapiacutea M Guanira-Carranza JV Ramirez-Cardich MEMontoya-Herrera O Fernaacutendez T Veloso VG Buchbinder SPChariyalertsak S Schechter M Bekker LG Mayer KH Kallaacutes EG Amico KRMulligan K Bushman LR Hance RJ Ganoza C Defechereux P Postle BWang F McConnell JJ Zheng JH Lee J Rooney JF Jaffe HS Martinez AIBurns DN Glidden DV iPrEx Study Team Preexposure Chemoprophylaxisfor HIV prevention in men who have sex with men N Engl J Med 20103632587-2599

197 Abdool Karim Q Abdool Karim SS Frohlich JA Grobler AC Baxter CMansoor LE Kharsany AB Sibeko S Mlisana KP Omar Z Gengiah TNMaarschalk S Arulappan N Mlotshwa M Morris L Taylor D CAPRISA 004Trial Group Effectiveness and safety of tenofovir gel an antiretroviralmicrobicide for the prevention of HIV infection in women Science 20103291168-1174

198 Rerks-Ngarm S Pitisuttithum P Nitayaphan S Kaewkungwal J Chiu JParis R Premsri N Namwat C de Souza M Adams E Benenson MGurunathan S Tartaglia J McNeil JG Francis DP Stablein D Birx DLChunsuttiwat S Khamboonruang C Thongcharoen P Robb ML Michael NLKunasol P Kim JH MOPH-TAVEG Investigators Vaccination with ALVACand AIDSVAX to Prevent HIV-1 Infection in Thailand N Engl J Med 20093612209-2220

199 Serwadda D Gray RH Sewankambo NK Wabwire-Mangen F Chen MZQuinn TC Lutalo T Kiwanuka N Kigozi G Nalugoda F Meehan MP AshleyMorrow R Wawer MJ Human immunodeficiency virus acquisitionassociated with genital ulcer disease and herpes simplex virus type 2infection a nested case-control study in Rakai Uganda J Infect Dis 20031881492-1497

200 Corey L Wald A Celum CL Quinn TC The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission a review of two overlappingepidemics J Acquir Immune Defic Syndr 2004 35435-445

201 WHO Priority interventions HIVAIDS prevention treatment and care in thehealth sector 2009 [httpwwwwhointhivpubpriority_interventions_webpdf]

doi1011861758-2652-14-49Cite this article as Wamai et al Male circumcision for HIV preventioncurrent evidence and implementation in sub-Saharan Africa Journal ofthe International AIDS Society 2011 1449

Submit your next manuscript to BioMed Centraland take full advantage of

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Page 17 of 17

reduction and as a corollary to this the level of impor-tance that heterosexual transmission plays in overallHIV transmission in a populationHistorically transmission of HIV has been attributed

to four main modes sexual intercourse transfusion par-enteral and perinatal acquisition [15] In light of thismultiple types of intervention strategies (behaviouralstructural and biomedical) have been advocated [16]While scientists seek to provide the evidence base pub-lic policy makers must evaluate logically where the pre-ponderance of evidence lies and make correct decisionsbased on a reasonable assessment of such evidence [17]Urgent calls have been made by experts and advocatesto accelerate HIV prevention scale up in line with theprevention principles [1819] However in someinstances skepticism about the evidence has led to hesi-tation delays and inaction leading to misery and as inSouth Africa needless death for hundreds of thousandsfrom failure to expeditiously implement programmesthat work [20]In the sub-Saharan African setting the established

convention is that heterosexual transmission is the pri-mary driver for the HIV epidemic Recently howeversome have argued that current HIV prevention interven-tions are based on ldquoinsufficient informationrdquo on modesof transmission and what works [21] We agree thatthere is a need to continually evaluate and updateknowledge on HIV transmission and what works in pre-vention so as to better inform and reinforce policy mak-ing and implementation Therefore in reinforcing thepolicy imperative for MC as a proven method for pre-vention of heterosexual HIV transmission we firstreview the state of knowledge on modes of HIV trans-mission in sub-Saharan Africa We then assess thestrength of current evidence for MC in protectingagainst HIV infection before analyzing current MCimplementation programmes in the region Finally wehighlight some of the outstanding issues and call for anacceleration in MC implementation as an evidence-based strategy to stem the HIVAIDS epidemic

What we know about the drivers of HIV infectionin sub-Saharan AfricaAccording to the latest Joint United Nations Programmeon HIVAIDS (UNAIDS) epidemic update report of the333 million people living with HIVAIDS worldwide atthe end of 2009 925 were adults [22] About halfwere women and 676 live in sub-Saharan Africawhere women comprise about 60 of cases [22] Oftotal infections globally 25 million (approximately 75of the total) were in children (aged younger than 15years) of whom 92 live in sub-Saharan Africa wherethey comprise 10 of all cases [22] Although some chil-dren younger than 15 are sexually active the prevalence

estimates show that 925 of cases globally and 90 insub-Saharan Africa are in the adult population [22]While this in itself does not necessarily show associa-

tion with sexual activity the preponderance of infectionin adults can only be explained by adult-specific factorsnot affecting children HIV distribution by sex andacross age groups are clearly consistent with sexualbehaviour as the main mode of transmission as shownby the significant and sudden increase in HIV in thoseolder than 15 years [2223]Consistent evidence for a major role of sexual inter-

course in transmission of HIV has been provided bynumerous modelling studies [24-28] and ecologicalobservations published by the World Health Organiza-tion (WHO) and UNAIDS in their annual report [22]as well as in national estimates [29] These data are col-lected according to global norms [3031] whose methodsare continually refined [32-35]The effect of sexual transmission likely lie in context-

specific factors confounding host and agent alike Theseinclude stage of the disease associated viral load otherbiological factors [2436-40] as well as the socio-eco-nomic and policy context [2041] Credible researchshows that the key initial drivers of the sexual transmis-sion were a synergistic relationship between promiscu-ous practices coupled with individual-level biologicalfactors namely sexually transmitted infections (STIs) (inparticular genital ulcer disease syphilis and HSV-2) andlack of MC [40-44] These factors also help explain thedifferences in rate of spread across the continent [4245]Among these the role of multiple and concurrent

partnerships (unstructured casual sex and polygyny) iswell documented in many sub-Saharan Africa countries[46-51] This is demonstrated for example in one ofthe most detailed studies involving 179 focus groupsand 116 in-depth interviews with diverse groups of peo-ple (malefemale youngold urbanrural) in typical day-to-day settings in 10 countries of southern Africa thathave high generalized HIV epidemics [52] Modellingand network theory reveal dynamics of exposure [5354]Nevertheless there is conflicting evidence on the extentto which multiple and concurrent partnerships drivesthe epidemic as shown in recent assessments of theexisting literature by Lurie and Rosenthal [55] andSawers and Stillwaggon [56] as well as a debate hostedon 27 October 2010 by the United States Agency forInternational Development (USAID) and the WorldBank among opposing sides [57]While heterosexual behaviour plays a leading role in

HIV transmission in sub-Saharan Africa it is fair to askwhat proportion of infections is from non-sexual driversThese include unsafe injections in medical and non-medical settings [5859] injecting drug use and bloodtransfusion [60-62] mother to child transmission


of 17












Sex workers (SW) 091 125 075 3 047

SW clients 783 1048 404 47 059











Page 3 of 17












Page 4 of 17











Page 5 of 17











Page 6 of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17












Sex workers (SW) 091 125 075 3 047

SW clients 783 1048 404 47 059











of 17












Page 4 of 17











Page 5 of 17











Page 6 of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17












of 17











Page 5 of 17











Page 6 of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












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of 17











Page 6 of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17











of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17



()

Mencircum-cised()


status


TotalNet




80 target




strategies

62773 248million

11197 345244 32



93 -National


finalization

Underdevelopment


1479 58million

5786 100000 58

60 -Gambella

46 -Gambella


in GambellaRegion




prison services

73420 247million

232287 860000 27

154 -Nyanza

48 -Nyanza





106427 618million

4000 376795 1

Launched in 2010


MC



240685 12billion

3119 2101566 01



215861 15billion

7733 1059104 07


Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page7of

17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17



services

18373 120million

1987 330218 06





56840 200million

1694 1746052 01




1083869 65billion

131117 4333134 34




56810 332million

18869 183450 133



prevalence


public sector

202900 966million

18026 1373271 14


services

339524 2 billion 9052 4145184 02



339632 24billion

81849 1949292 42



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page8of

17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














Page 11 of 17




























Page 12 of 17

















































Page 13 of 17




















































Page 14 of 17











































Page 15 of 17










































Page 16 of 17

























Page 17 of 17





565751 38billion

13977 1912595 07



Wam

aietalJournalof

theInternationalA

IDSSociety

20111449httpw


Page9of

17












Page 10 of 17














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Male circumcision for HIV prevention: current evidence and implementation in sub-Saharan Africa

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Transcript of Male circumcision for HIV prevention: current evidence and implementation in sub-Saharan Africa