Review Article

Sexually Transmitted Infections and Male Circumcision: A Systematic Review and Meta-Analysis

Table 1

Attributes of studies meeting the inclusion criteria.

Study STI studiedLocationWhenPopulationType of studyCircumcision statusMethod of diagnosis

Agot [152];
GDS and GUD
KenyaFrom October 1999 to May 200018–49 y/o sexually active males unaware of HIV status in circumcising and noncircumcising denominations in Luo ethnic communityCross-sectionalPhysical examReport

Auvert et al. [153];
GC, CT,
and any
Kisumu, KenyaFrom June 1997 to March 1998General populationCluster design to randomly select householdsPhysical exam and self-reportSerology (HSV and syphilis). Urine DNA (GC and CT)

Auvert et al. [105];
HPV and GC
Orange Farm, South Africa2002–2006Men interested in a free circumcisionRandomized clinical trialIntention to treatUrethral swabs (HPV)

Aynaud et al. [33];
HPV
Paris, FranceFrom March 1991 to September 1992Men whose female partners had genital condylomata or intraepithelial neoplasiaCross-sectional studyPhysical examColposcopy, viral culture, and biopsy

Aynaud et al. [34];
NSU, CT, GC, HPV, and any
Paris, FranceNot documentedHeterosexual HIV-negative men whose female partner has HPV
Cross-sectional studyPhysical examChlamydia by PCR, cultures (GC), and HPV by biopsy and penoscopy

Bailey [114];
GDS, GC, and syphilis
Mbale, UgandaFrom April to May 1997General populationSingle stage cluster sampling cross sectionReportReport

Baldwin [154];
HPV
Tucson, ArizonaFrom July 2000 to January 2001High risk men attending a public STD clinicCross-sectionalPhysical examSwab of glans and sulcus (HPV)

Barile [59];
GUD
JapanNot documentedUS military personnel in Japan
Case controlPhysical examClinically

Bassett [155];
HSV
Sydney, AustraliaFrom December 1990 to May 1991STD clinicConsecutive sample of heterosexual menPhysical examHSV2 by serology

Bleeker [156];
HPV
AmsterdamFrom April 2002 to November 200218–75 years old. Group A with female partner without CIN. Group B female partner with CIN. Non-STD hospital populationConsecutive sample of male partners of
Physical examSwab of glans, sulcus, corona, and frenulum (HPV)

Burundi [72];
GDS, GUD,
and any
Burundi2010General population from 15 to 49 years oldNational representative population surveyPatient reportPatient report

Buvé [61];
syphilis and HSV
Kisumu, Kenya; Ndola, Zambia; Cotonou, Benin; Yaoundé, CameroonFrom June 1997 to March 1998General population from 15 to 49 years oldCluster design to randomly select householdsPhysical exam and self-reportSerology (HSV and Lues)

Bwayo [36];
GDS, GUD,
and syphilis
25 miles from NairobiFrom June 1989 to February 1992Truck drivers enrolled at roadside research clinicSelf-selected convenience sampleNot documentedReport (GDS and GUD) and serology (Lues)

Cameron [97];
GUD versus GDS
Nairobi, KenyaFrom March 1986 to December 1987. Followup to March 1988STD clinic and men who got STD from a prostituteProspective cohort studyPhysical examNot documented

Castellsagué [99];
HPV
Brazil, Thailand, Philippines, Spain, Columbia1985–1993Husband or stable partner of woman with cervical cancer or a control womanSeven separate case-control studiesPhysical exam in Brazil, Thailand, and Philippines. Report in Spain and ColumbiaPCR for HPV from urethra and glans swabs

Cook [30];
NSU, CT, GC, syphilis, HSV, HPV (warts), and any
Seattle, WashingtonFrom January to December 1988STD clinicChart review of heterosexual menChart review (14.3% missing)Urethral swabs, syphilis by serology, warts, and HSV clinically and warts clinically

Dave [133];
NSU, CT, GC, syphilis, HSV, HPV (warts), and any
Great Britain2000General populationLarge-scale, stratified, probability sample survey
ReportReport

Dickson et al. [157];
HSV and any
Dunedin, New Zealand1999Birth cohort from 1972 to 1973Prospective cohort repeatedly studied from birth
Not documentedSerology (HSV)

Dickson et al. [51];
any
Dunedin, New ZealandFrom 2004 to 2005Birth cohort from 1972 to 1973Prospective cohort repeatedly studied from birthLife-time medical recordsLife-time medical records

Dickson et al. [158]; HPVDunedin, New ZealandFrom 2004 to 2005Birth cohort from 1972 to 1973Prospective cohort repeatedly studied from birthLife-time medical recordsSerology for 6, 11, 16, and 18

Dinh [71];
HPV (warts)
United StatesFrom 1999 to 2004Random sample of general population aged from 18 to 59National survey NHANESPatient report using visual aidsPatient report

Diseker [159];
CT, GC, syphilis,
and any
Baltimore, Denver, Long Beach, San FranciscoFrom July 1993 to September 1996STD clinicPart of RCT, baseline analysis, and cohort analysis
Physical examGC by culture, chlamydia by urine PCR, and syphilis by serology

Donovan [160];
NSU, GC, syphilis, HSV, and HPV (warts)
Sydney, AustraliaFrom December 1990 to May 1991STD clinicConsecutive sample of heterosexual men
Physical examNGU by clinical picture and microscopy, TPHA for syphilis, HSV by cell culture or clinical criteria, and warts clinically

Fergusson [138];
CT, and any
Christchurch, New ZealandFrom 1998 and 2002Birth cohort from 1977Prospective cohort repeatedly studied from birth
Report and medical recordsPatient report

Ferris [161];
any, warts, CT, HSV, GC, and NSU
Australia200516–64 years oldRepresentative national samplePatient reportPatient report

Gebremedhin [52, 162]; anyAfrica2003–2007General population18 national demographic health surveysPatient reportPatient report

Giuliano et al. [102];
HPV
Sao Paulo,
Brazil; Morelos, Mexico, Central Florida
2005 and 200618–70 years old, no previous warts, and no STD or HIV
Prospective cohort studyPhysical examGlans, sulcus, shaft, and scrotum

Gottlieb [62];
HSV
Baltimore, Denver, Long Beach, San FranciscoFrom July 1993 to September 1996STD clinicPart of RCT cohort analysisPhysical examSerology (HSV)

Gray et al. [44, 163],
GDS, CT, GC, Lues, HSV, and GUD
Rakai, UgandaFrom November 1994 to October 1998General populationRandomized cluster of general populationReportUrine PCR (GC and CT), serology (HSV and syphilis), and clinically (GUD)

Gray et al. [53];
GUD
Rakai, UgandaCompleted December 2006Men 15–45 who wanted a free circumcisionRandomized controlled trialIntention to treatGUD on physical examination

Hand [25];
GC, syphilis, and chancroid
US Naval Hospital St. Albans, NY1945SailorsNot documentedNot documentedNot documented

Harbertson [164];
any STI
RwandaFrom October 2008 to November 2010Active duty soldiers 21 years old in Rwanda Defense Forces from 46 military sitesCross-sectionalPatient reportPatient report

Hart [69];
chancroid
Australia1970Soldiers, STD clinicCross-sectionalPhysical examClinical diagnosis

Hart [165];
CT and GC
South AustraliaFrom 1988 to 1990STD clinicConsecutive sampleNot documentedChlamydia by enzyme immunoassay and GC by smear and culture

Hernandez [35];
HPV
HawaiiFrom July 2004 to December 2006University students 18 years old
Convenience samplePhysical examHPV swabbed glans, sulcus, shaft, scrotum, and inner foreskin

Hutchinson [1];
GUD versus GDS
Metropolitan Free Hospital, London
Past year’s experienceMen with an STDNot documentedJew versus GentileClinically

Kapiga [166];
HSV
Moshi, TanzaniaFrom June to October 2000Hotel and bar workersRandomized samplePhysical examSerology (HSV)

Klavs [167];
any
Slovenia1999–2001Men 18–49 years oldNational probability sampleReportPatient report

Lajous [100];
HPV
MexicoFrom July 2000 to July 2003Healthy military menCross-sectional studyPhysical exam performed but analysis based on reportHPV DNA

Langeni [85];
any
Botswana2001Men 15–64 who had intercourseNational represented sampleReportGDS or GDS by report in the past 12 months

Laumann [89];
NSU, CT, GC, syphilis, HSV, and any
United States1992Men 18–59 years oldNational probability sampleReportReport

Lavreys [168];
GDS, syphilis, HSV, HPV (warts), GUD, and chancroid
KenyaFrom March 1993 to June 1997HIV negative-truck driversProspective cohort study and convenience samplePhysical examChlamydia by serology assay, TPHA & RPR (syphilis), HSV by serology assay, warts clinically, and chancroid by serology assay

Lloyd [57];
GC, Syphilis, and chancroid
Guy’s Hospital, LondonFrom January to June 1932STD clinicConvenience samplePhysical examClinically and soft chancre clinically

Lu [84];
HPV
Tucscon, Arizona; Tampa, FloridaFrom September 2003 to December 200518–40 year old sexually active males with no previous genital warts or penile cancer or current STDProspective cohort studyPhysical examGlans, shaft, and scrotum

Mallon [24];
HSV and HPV (warts)
Chelsea and Westminster Hospital, London1994–1997Patients referred to a dermatology specialty clinic
Retrospective case controlPhysical examNot documented

Mandal [169];
HPV
United KingdomSTD clinic and men with no evidence of clinical anogenital wartsCross-sectionalNot documentedCytology of swabs from urethra, glans, shaft, and anorectal

Mattson [170];
any
Kisumu, Kenya2002–200618–24 year olds who wanted a free circumcisionRandomized clinical trialPhysical examPCR for GC and CT and culture for T. vaginalis

Mehta et al. [171];
GC chlamydia
Kisumu, Kenya2002–2006Men interested in a free circumcisionRandomized clinical trialIntention to treatUrine for GC and chlamydia

Mehta et al. [172];
HSV, Lues, and GUD
Kisumu, Kenya2002–200618–24 year old men who wanted a free circumcisionRandomized clinical trialIntention to treatSerology (Lues and HSV) and Clinically identified (GUD)

Mor [173];
syphilis
San FranciscoFrom January 1996 to December 2005STD clinicConsecutive samplePhysical examNot documented

Mujugira [174];
HSV
Botswana, Kenya, Rwanda, South Africa, Tanzania, Uganda, ZambiaFrom November 2004 and April 2007HIV-negative partners of women who are HIV and HSV positive
Discordant couplesPhysical examSerology (HSV)

Müller [175];
HPV
Alexandra, Johannesburg, South AfricaFrom December 2006 to July 200818+ sexually active attending HIV testing clinicCross-sectionalPhysical examGlans, sulcus, and shaft

Mwandi [88];
HSV
KenyaFrom August to December 2007General population from 15 to 64 years oldRepresentative samples of householdsPatient reportSerology (HSV)

Nasio [98];
GUD versus GDS
NairobiFrom January to September 1993STD clinicConvenience samplePhysical examReport

Newell [176];
GDS, syphilis, and GUD
Mwanza Region, TanzaniaFrom 1990 to 1991General populationRandom cluster sample survey
ReportReport (GDS and GUD) and serology (syphilis)

Ng’ayo [177];
HSV
Kisumu, KenyaNot documentedFishermen along Lake Victoria 18 years of ageRandom cluster sample cross-sectional surveyNot documentedSerology (HSV)

Ng’ayo [178];
HPV
Kisumu, KenyaNot documentedFishermen along Lake Victoria 18 years of ageRandom cluster sample cross-sectional surveyPhysical examSwab of glans, corona, shaft, scrotum, and perianal

Nielson [179]; HPVTucscon, Arizona; Tampa, Florida2002–200518–40 year old sexually active males with no previous genital warts or penile cancer or current STDCross-sectionalPhysical examSwab of glans, sulcus, shaft, scrotum, perianal area, and urethra (optional)

Obasi [63];
HSV
Rural Mwanza Region, TanzaniaMay and June 1993General populationNested case-control study within an RCTNot documentedType specific ELISA for HSV2

Oglivie [180];
HPV
British Columbia, CanadaNot documentedSTD clinic never MSMCross-sectional studyPhysical examGlans, foreskin, shaft, and scrotum

Oriel [29];
HPV (warts)
St. Thomas Hospital, LondonFrom October 1967 to January 1979STD clinicConsecutive samplePhysical examNot documented

Otieno-Nyunya [181]; LuesKenya2007General populationNationally representative population-based serosurveyFind articleSerology

Parker [140];
NSU, CT, GC, syphilis, HSV, HPV (warts), and any
Perth, AustraliaFrom May to September 1981
STD clinicConsecutive sampleReport and physical examCultures and microscopy (NSU, CT, and GC), serology (syphilis) culture (HSV) and warts clinically

Partridge [182];
HPV
Seattle, WashingtonFrom June 2003 to March 2006 recruitmentUniversity of Washington students 18–20 years old history of vaginal intercourseProspective cohort studyPhysical examHPV swabs of penile shaft, glans, foreskin, scrotum, and urine.

Rakwar [70];
chancroid
Mombasa, KenyaBeginning of March 1993Long-distance truckersCross-sectionalPhysical examSerology and culture of genital ulcers

Reynolds [183];
GC, syphilis, and HSV
Pune, India1993–2000STD clinicProspective cohort studyPhysical examPositive gram stain of urethral discharge (GC), RPR, or darkfield (syphilis). Serology (HSV)

Richters [184];
GC, HSV,
NSU, and any
AustraliaFrom May 2001 to June 2002Males 16–59National probability sampleReportReport

Rodriguez-Diaz [185];
any, GC, syphilis, HSV, warts, and CT
San Juan, Puerto RicoFrom October 2009 to December 2011STD clinic and Males from 16 to 83 years oldCross-sectionalReportReport

Rombaldi [186];
HPV
Caxias do Sul, BrazilFrom February 2003 to July 2004Sexual partners of women with CINProspective, prevalence studyPhysical examPenoscopy and sampling of urethra, glans, preputial mucosa, and shaft

Schneider [187];
HSV and syphilis
Guntur district of Andhra Pradesh, India
From September 2004 to September 200515–49 year olds general populationsRandom clusters
ReportSerology

Schrek [58];
GC, syphilis
and any
Hines Veteran Hospital, Illinois1931–1944World War I veteransCross-sectional study
Age at circumcision by reportReport

Seed [188];
GDS, syphilis, GUD and any
RwandaFrom March to October 1991Steady sexual partner of women enrolled in Project San FranciscoCross-sectional studyPhysical examReport (GDS and GUD) and RPR (syphilis)

Shin [189];
HPV
Busan, South KoreaFrom August 29 to September 30, 2002University studentsCross sectionReportContinuous swab for HPV DNA from scrotum to top of glans

Simonsen [190];
GUD
NairobiFrom March to December 1986STD clinic and men with an STD from a prostituteConvenience samplePhysical examChancroid by culture

Smith [191];
NSU and GC
US military postFrom January 1983 to September 1984US Army personnelCross sectionPhysical examCDC criteria and culture

Sobngwi-Tambekou [192];
GC, CT and HSV
Orange Farm, South Africa2005Males interest in a free circumcisionRandomized clinical trialIntention to treatUrine samples for GC and CT and serology (HSV)

Suligoi [64];
HSV
Garoua, northern CameroonFrom December 1997 to January 1998General medical outpatients without complaints of STD or HIVConsecutive sampleReportHSV by ELISA

Svare [193];
HPV
Copenhagen, DenmarkFrom March to December 1993STD clinicConsecutive sampleReportPenile swab for PCR

Talukdar [194];
GC and
syphilis
Kolkata, IndiaNot documentedHomeless men 18–49 years oldCluster design among homeless menReligionUrine PCR (GC) TPHA (syphilis)

Taylor [195];
NSU, GC,
HSV, and any
Whitechapel Clinic, The London HospitalFrom June 1970 to August 1973STD clinicConsecutive sample with randomly selected controlsChart review (10.9% missing)Clinical diagnosis and HSV2 by culture

Telzak [60];
GUD
New York City1988–1991STD clinicProspective cohort studyPatient reportDark field, RPR, culture, Tzanck smear, and clinical diagnosis

Thomas [68];
any
United States MilitaryFrom February 1997 to June 2001HIV-positive cases and HIV negative controlsCase controlMedical records/patient reportPatient report

Tobian et al. [82];
HPV, HSV, syphilis, GDS, and GUD
Rakai, UgandaEnded December 2006Men 15–45 who wanted a free circumcisionRandomized clinical trialPhysical examSwab of glans and sulcus (HPV) and serology (HSV and syphilis)

Todd [145];
syphilis
Mwanza, TanzaniaFrom 1991 to 1994General populationCommunity randomized trial nested case controlNot documentedRPR and VDRL

Tseng [66];
HPV (warts)
Los Angeles, CaliforniaFrom May 1975 to October 1985Cases of penile cancer and matched controls and mean age 55.9 and 56.2, respectivelyCase controlPatient reportPatient report

Tyndall [137];
GDS and GUD
NairobiNot documentedSTD clinic and men with genital ulcersConvenience samplePhysical examReport

Uganda [73];
syphilis
UgandaFrom February to September 2011Adults from 15 to 59National representative population-based surveyPatient reportSerology

Urassa [79];
syphilis
and any
Mwanza Region, TanzaniaStudy 1: 1990-1991.
Study 2: 1994-1995.
Study 3: 1994.
Study 4: 1991–1993.
Study 5: 1992.
Study 1: GP*.
Study 2: GP.
Study 3: fishing villages.
Study 4: factory workers.
Study 5: GP*.
Study 1: stratified random cluster sample.
Study 2: community study.
Study 3: cluster sample survey.
Study 4: intake data of cohort study.
Study 5: baseline round of longitudinal cohort study to assess community level STD control measures impact on HIV.
Study 1, 2, 3, and 5: report.
Study 4: physical exam.
RPR for syphilis and patient report for any STI

Vaccarella [86];
HPV
Mexico, 27 public clinics in 14 statesFrom January 2003 to September 2004Men attending vasectomy clinicConsecutive sample
Physical exam in Mexico
Complete swab from scrotum to urethra

VanBuskirk [32];
HPV
Seattle, WashingtonFrom June 2003 to March 2006 recruitment
data through April 2010
University of Washington students 18–20 years old history of vaginal intercourseProspective cohort studyPhysical examHPV swabs of penile shaft, glans, foreskin, scrotum, and urine.

Van Den
Eeden [67];
HPV (warts)
Seattle, WashingtonFrom April 1987 to September 1991Men 18 years with condylomata acuminata and matched controls in 4 HMO clinicsCase controlPatient reportClinical exam

Van Wagoner [196];
HSV
Birmingham, AlabamaNot documentedSTD clinic and self-identified heterosexual menCross-sectionalPhysical examSerology and culture

Vardas [197];
HPV
Not reported18 countries in Africa, Asia-Pacific, Europe, Latin America, and North AmericaHeterosexual men from 16 to 24 years with 1 to 5 lifetime female partnersCross-sectionalPhysical examSerology for 6, 11, 16, and 18; swab of penis, scrotum, perineum, and perianal (HPV)

Warner [87];
GDS, GUD,
and GUD
versus GDS
Baltimore, MDFrom 1993 to 2000Heterosexual African American men undergoing HIV testing at STD clinicsChart reviewPhysical exam documented in medical recordClinical exam

Vaz [198];
syphilis
Maputo, MozambiqueFrom 1990 to 1991PrisonersConvenience samplePatient reportRPR and FTA

Weaver [31];
HPV
Seattle, WashingtonPart 1: from August 1 to October 30, 2000 and
part 2: May 3, from 2001 to July 9, 2002
Part 1: heterosexual men 18–25 years old attending STD clinic.
Part 2: sexually active undergraduate male students 18–25 years old
Consecutive samplePhysical examHPV swabs of penile shaft, glans, foreskin, scrotum, and urine.

Weiss [65];
HSV
Kisumu, Kenya; Ndola, Zambia; Cotonou, Benin; Yaondé, CameroonFrom June 1997 to March 1998General populationCluster design to randomly select householdsPhysical exam and self-reportSerology (HSV)

Wilson [23];
NSU, GC,
Lues, and HPV (warts)
CanadaNot documentedCanadian Army VD treatment centerConvenience sampleNot documentedNot documented

Wolbarst [56];
GUD versus GDS
New York CityBefore 1914 to 1926Private patients in urology practiceConvenience sampleJew versus GentileClinically

Xu [199];
HSV
United States1999–2004General populationNational health surveyPatient report using visual aidsSerology (HSV)