Skip Navigation

Circumcision and Risk of Sexually Transmissible Infections in a Community-Based Cohort of HIV-Negative Homosexual Men in Sydney, Australia

  1. David J. Templeton1,3,
  2. Fengyi Jin1,
  3. Garrett P. Prestage1,
  4. Basil Donovan1,4,
  5. John C. Imrie2,
  6. Susan C. Kippax2,
  7. Phillip H. Cunningham5,
  8. John M. Kaldor1,
  9. Adrian Mindel6,
  10. Anthony L. Cunningham7 and
  11. Andrew E. Grulich1
  1. 1National Centre in HIV Epidemiology and Clinical Research and
  2. 2National Centre in HIV Social Research, University of New South Wales,
  3. 3RPA Sexual Health Clinic, Royal Prince Alfred Hospital, and
  4. 4Sydney Sexual Health Centre, Sydney Hospital, Sydney,
  5. 5Centre for Immunology, St Vincent’s Hospital, Darlinghurst,
  6. 6Sexually Transmitted Infections Research Centre, Westmead Hospital and University of Sydney, and
  7. 7Westmead Millennium Institute, Centre for Virus Research, Westmead Hospital, Westmead, Australia
  1. Reprints or correspondence: Dr Templeton, National Centre in HIV Epidemiology and Clinical Research, University of New South Wales, Level 2, 376 Victoria St, Sydney NSW 2010, Australia (dtempleton{at}nchecr.unsw.edu.au)
 
Next Section

Abstract

BackgroundCircumcision status was examined as an independent risk factor for sexually transmissible infections (STIs) in the Health in Men cohort of homosexual men in Sydney

MethodsFrom 2001 through 2004, 1427 initially human immunodeficiency virus (HIV)–negative men were enrolled and followed up until mid-2007. All participants were offered annual STI testing. The history of STIs was collected at baseline, and information on sexual risk behaviors was collected every 6 months. At annual face-to-face visits, participants reported STI diagnoses received during the previous year

ResultsCircumcision was not associated with prevalent or incident herpes simplex virus 1, herpes simplex virus 2, or self-reported genital warts. There was also no independent association of circumcision with incident urethral gonorrhea or chlamydia. Being circumcised was associated with a significantly reduced risk of incident (hazard ratio, 0.35 [95% confidence interval, 0.15–0.84]) but not prevalent (odds ratio, 0.71 [95% confidence interval, 0.35–1.44]) syphilis. The association was somewhat stronger among men who reported predominantly insertive unprotected anal intercourse (hazard ratio, 0.10 [95% confidence interval, 0.01–0.82])

ConclusionsThese are the first prospective data obtained from homosexual men to assess circumcision status as a risk factor for STIs. Circumcised men were at reduced risk of incident syphilis but no other prevalent or incident STIs. Circumcision is unlikely to have a substantial public health impact in reducing acquisition of most STIs in homosexual men

Men who have sex with men (MSM) bear a disproportionate burden of sexually transmissible infections (STIs) in resource-rich countries. A substantial decrease in rates of many STIs occurred in MSM soon after human immunodeficiency virus (HIV)/AIDS was recognized, but many countries have witnessed a resurgence of STIs among this population [1]. Conventional methods of STI control are clearly failing to control the STI epidemic among MSM, and novel strategies to reduce STI transmission require investigation

Observational evidence among heterosexual men suggests that circumcision may reduce the risk of syphilis, chancroid, and possibly herpes simplex virus (HSV) type 2 [2]. Recently published data from randomized trials in Africa have demonstrated that circumcised heterosexual men are at reduced risk of HSV-2 acquisition [3, 4] but not syphilis infection [3]. Compared with uncircumcised men, circumcision also resulted in a lower prevalence of high-risk penile human papilloma virus (HPV) [3, 5] but had no impact on the incidence [6] or prevalence [7] of urethral gonorrhea or chlamydia. Because the range of sexual behaviors of homosexual men is substantially different from those of heterosexual men, it is likely that these results cannot be generalized to homosexual men

The small number of studies performed among MSM, none of which was prospective, have demonstrated little impact of circumcision on selected STIs [8–10] or STIs overall [11]. The association of circumcision status and STIs was assessed in the community-based Health in Men (HIM) cohort of HIV-negative homosexual men in Sydney, in which the incidence and other risk factors for a wide range of anogenital STIs had already been well characterized [12–15]

Previous SectionNext Section

Methods

Participants

Study participants were men who were recruited from a range of community-based sources from June 2001 through December 2004 and followed up through June 2007. Details of recruitment sources and methods of the HIM study have been described elsewhere [15]. Briefly, men eligible for participation in the HIM study met the following criteria: (1) they reported having sex with men in the 5 years before enrollment, (2) they lived in Sydney and/or participated in its gay community, and (3) they tested negative for HIV infection at baseline. Signed, informed consent was obtained from all participants. Ethics approval was granted by the University of New South Wales

Data Collection

All participants underwent annual face-to-face interviews, with 6-monthly telephone interviews between these visits. Detailed behavioral data were collected every 6 months, including number and position (insertive or receptive) of unprotected anal intercourse (UAI) acts. In addition, each year participants reported their preference for anal intercourse position (preference for insertive or receptive role or no preference). At the annual face-to-face interviews, participants were asked to report whether they had received diagnoses of anogenital gonorrhea, chlamydia, or warts in the past 12 months. They were also asked at the baseline interview whether they had ever received a diagnosis of anogenital warts. As part of the study design, participants were offered annual testing for STIs at the time of the face-to-face interview. Circumcision status was reported by participants at baseline. Self-report was validated by clinical examination in a subgroup of 237 participants and correlated with examination findings in 98% of cases [16]

Laboratory Studies

Detailed information on specimen collection and laboratory diagnostic methods have been published elsewhere [12–15, 17] and are briefly summarized below

Neisseria gonorrhoeaeand Chlamydia trachomatis. Nucleic acid amplification tests (NAATs) for N. gonorrhoeae and C. trachomatis were introduced to the HIM study in January 2003. Consenting participants collected first-void urine and self-obtained anal swab samples annually for NAATs by the BD ProbeTec assay (BD Diagnostics). For anal N. gonorrhoeae diagnosis, all positive ProbeTec results underwent supplementary porA testing. The full methods of this supplementary testing have been described in detail elsewhere [17]. Only porA-positive samples were included as true anal N. gonorrhoeae infections in the analyses

SyphilisConsenting participants were screened annually for syphilis by enzyme immunoassay (ICE Syphilis; Murex Biotech). Positive assay results were confirmed with the Treponema pallidum particle agglutination assay and fluorescent treponemal antibody absorption test. The rapid plasma reagin test was used to assist clinical staging and to detect reinfection

HSVBaseline serum samples and sequential specimens were tested for antibody to HSV, with use of an algorithm involving the Enzygnost anti-HSV IgG enzyme-linked immunosorbent assay (ELISA) (Behring), and type-specific ELISAs (HerpeSelect 1 and 2 ELISA IgG; Focus Technologies) [15]. Equivocal results were resolved by Western blot analysis

Anogenital wartsNo HPV tests or routine anogenital examinations for warts were performed in the HIM study. Participants self-reported a lifetime history of genital or anal warts at baseline and reported annually whether anogenital warts had been diagnosed since the last face-to-face interview [12]

Incidence Definition

For each STI, incidence was expressed as the number of incident cases per 100 person-years

N. gonorrhoeaeand C. trachomatis. To be able to estimate the incidence of urethral and anal N. gonorrhoeae more comprehensively, participants who reported a diagnosis of urethral or anal N. gonorrhoeae or C. trachomatis or tested positive for such infection at their HIM study visit were treated as having incident cases. Because the NAATs were added to the study in January 2003, this calculation was applicable only from 2003 forward [14]

SyphilisIncident syphilis was defined as syphilis seroconversion or reinfection during the study period. Reinfection was defined as a 4-fold increase in rapid plasma reagin titer on sequential serum specimens collected at annual visits

HSVIncident HSV-1 and HSV-2 infections were defined as HSV-1 and/or HSV-2 seroconversion during the study

Anogenital wartsFor genital and anal warts, prevalent infection was defined as a self-reported lifetime diagnosis of warts at the baseline interview. Incident warts were defined as self-reported diagnoses of anogenital warts during the previous 12-month period

Statistical Analysis

Statistical analyses were performed using Stata software (version 10.0; StataCorp). Participants’ preference for anal intercourse position was correlated with reported UAI behavior (Table 1). Because the data for number of UAI acts were highly skewed, the median was used as the measure of central tendency. The exact binomial method was used to calculate 95% confidence intervals (CIs) for prevalence and incidence values. Crude and adjusted analyses were performed to identify the association of circumcision status with prevalent and incident urethral N. gonorrhoeae urethral C. trachomatis syphilis, HSV-1, HSV-2, and anogenital warts. Odds ratios (for prevalent infection) and hazard ratios (HRs) (for incident infection) and their corresponding 95% CIs were calculated for these associations

Table 1
View larger version:
Table 1

Correlation of Reported Preference of Anal Intercourse Position with Anal Intercourse Behavior among Participants Reporting Any Unprotected Anal Intercourse (UAI) in the Health in Men Study

For analyses of the entire cohort, multivariate logistic regression (for prevalent infections) (Table 2) and Cox regression (for incident infections) (Table 3) models included sexual behavioral variables found to be associated with prevalent and incident infections in other HIM study analyses of anogenital N. gonorrhoeae and C. trachomatis [14], syphilis [13], HSV [15], and anogenital warts [12]. Covariates were entered in the multivariate model if they were found to be independent predictors of each STI in these other analyses and are outlined in the footnotes of Tables 2 and 3

Table 2
View larger version:
Table 2

Circumcision Status and Prevalent (Baseline) Sexually Transmissible Infections (STIs) in the Health in Men Cohort

Table 3
View larger version:
Table 3

Circumcision Status and Incident Sexually Transmissible Infections (STIs) in the Health in Men Cohort

For analyses of participants predominantly practicing the insertive role in anal intercourse, the multivariate Cox regression model (Table 4) included the total number of insertive UAI acts in the past 6 months. Circumcision status and age were a priori covariates in each multivariate model. To avoid the possibility of residual confounding, age was analyzed as a continuous variable because of the strong independent association of age with circumcision status in the HIM study [18] and the association of age with urethral N gonorrhoeae and C. trachomatis infections [14], genital warts [12], and HSV-1 infection [15]. Of other demographic variables associated with circumcision status in the HIM cohort [18], neither country of birth nor ethnicity was associated with any prevalent or incident STI, so these variables were not included as covariates in the multivariate models

Table 4
View larger version:
Table 4

Circumcision Status and Incident Sexually Transmissible Infections (STIs) in the Health in Men Cohort among Participants Who Predominantly Practiced the Insertive Role in Unprotected Anal Intercourse

Multiple failures in the subsequent interview(s) were allowed only for incidence calculations involving gonorrhea, chlamydia, and syphilis. For incidence risk factor analyses of these STIs, mixed models were used that allowed for repeated measures in the same individuals. These models, which allow for within- and between-subject variability, provide robust variance estimates and, therefore, appropriate P values and CIs [19]

Participants’ own circumcision status would have had no plausible effect on their STI acquisition via receptive anal sex. We examined circumcision as a risk factor for anal gonorrhea, chlamydia, and warts, only to contrast these findings with the same infections at genital sites

Previous SectionNext Section

Results

From June 2001 through December 2004, a total of 1427 participants were enrolled. The median age at enrollment was 35 years (range, 18–75 years); 68% of participants were Australian born, 74% were of Anglo ethnicity, and 95% of participants self-identified as gay or homosexual. One participant who reported a surgically reconstructed foreskin was excluded, so analyses of circumcision status and risk of STIs were based on 1426 participants

By the end of the HIM study in June 2007, the total follow-up time was 5160.7 person-years, and the median follow-up time for participants was 3.9 years. The follow-up time from commencement of gonorrhea and chlamydia NAATs in January 2003 to the end of the HIM study in June 2007 was 3781.5 person-years. The uptake of N. gonorrhoeae and C. trachomatis anal and urine testing was high; a total of 4090 NAATs (90.2% of eligible visits) were performed during this period. All participants consented to HSV and syphilis serological testing. The proportion of circumcised participants among those unavailable for follow-up was very similar to the proportion of circumcised participants in the entire cohort at baseline (65.4% vs 65.8%; P=.879)

Circumcision status and prevalent STIsResults of analyses of the association of circumcision status and prevalent (baseline) STIs are shown in Table 2. There was no univariate or multivariate association of circumcision status with syphilis, HSV-1, or HSV-2 seropositivity at baseline, nor any univariate or multivariate association of circumcision status with a lifetime history of genital or anal warts

Circumcision status and incident STIs The association of circumcision status with incident STIs in the HIM cohort is shown in Table 3. Circumcised participants were at reduced risk of acquiring syphilis during the study period after results were controlled for age, number of male sexual partners, and number of receptive UAI acts with HIV-positive partners or partners of unknown HIV status (HR, 0.35; 95% CI, 0.15–0.84, P=.019). Circumcision status was not associated with any other incident STI in univariate or multivariate analyses. Comparison of analyses of genital and anal STIs revealed little difference in HRs for incident warts, gonorrhea, and chlamydia

Only 10.1% of total person-years of follow-up were among men who exclusively practiced insertive, but not receptive, UAI. However, 33.1% of total person-years of follow-up were among participants who reported a preference for the insertive role in anal intercourse and whose sexual behavior closely reflected this preference (Table 1). Among these 404 participants, the protective effect of circumcision on incident syphilis infection remained despite only 6 incident infections in this subgroup (HR, 0.10; 95% CI, 0.01–0.82; P=.033) (Table 4). There was no association of circumcision status with any other STI in men who predominantly practiced the insertive role in UAI

Previous SectionNext Section

Discussion

Circumcised participants in the HIM cohort were at significantly reduced risk of incident syphilis infection, although there was no association of circumcision with baseline syphilis seropositivity. Circumcision was not associated with prevalent or incident urethral gonorrhea or chlamydia, HSV, or genital warts

Only 3 other published studies, all cross-sectional, have examined the relationship between circumcision and specific STIs in homosexual men [8–10]. The first was a study of almost 900 MSM attending an STI clinic in the United States [9], which found no univariate association of being circumcised with prevalent urethral gonorrhea or chlamydia. The second was a small study of mostly uncircumcised Peruvian MSM, quoted in a subsequent meta-analysis [2, 10], in which there was no independent association of circumcision with prevalent syphilis. Most recently, among >20,000 San Francisco STI clinic attendees, there was no univariate association between being circumcised and syphilis infection among either HIV-positive or HIV-negative MSM [8]. A recent meta-analysis that included some unpublished data also found no overall association of circumcision status with STIs among MSM [11]. Although other published studies of circumcision and STI risk have included MSM, results were not presented separately for this subgroup [20–24]

Of the STIs considered in the HIM study, the published evidence for a protective association with circumcision is strongest for syphilis. However, the majority of other observational studies have been cross-sectional studies of heterosexual men in developing countries. Most have found circumcised men to have lower odds of syphilis infection [2]. Recent data from a randomized trial among heterosexual men in Rakai, Uganda, found no effect of circumcision on incident syphilis [3]. However, this finding may have resulted from lack of power attributable to the small number of syphilis infections identified at follow-up testing [25]. Although the adjusted odds ratio for prevalent syphilis in the HIM cohort was 0.71, lower than that of the other prevalent STIs examined (Table 1), it was not statistically significant. Syphilis was very common among Australian homosexual men in the 1970s, but was virtually eliminated during the late 1980s and 1990s [26]. One possible explanation for an association with incident but not prevalent syphilis is that participants who initiated MSM sexual activity during the late 1980s and 1990s would have been at very low risk of acquiring syphilis irrespective of their sexual behavior or circumcision status. Only recently, since 2001, has syphilis reemerged among Australian MSM [13]

Recent publications have described a reduction in HSV-2 risk among circumcised heterosexual men in 2 of the African circumcision trials [3, 4]. We observed no such association of circumcision with incident HSV-2 infection in the HIM cohort, and ours is the first study to assess the association among homosexual men

In the HIM study, as in most longitudinal studies, HSV and syphilis were diagnosed serologically, and the anatomical site of acquisition was not known [27, 28]. The initial site of infection may have been oral or anal, for which, a man’s own circumcision status could have no plausible protective effect. Should circumcised homosexual men be at reduced risk of genital acquisition of both of these infections, the lack of data on site-specific diagnosis could, in part, explain the lack of association with circumcision in homosexual men

No reduction in incidence of urethral gonorrhea or chlamydia was observed among circumcised participants in the HIM study. Circumcision had no influence on prevalent or incident urethral gonorrhea or chlamydia in 2 of the African heterosexual circumcision trials [6, 7]. Likewise, the only published study involving MSM [9] found no association of circumcision status with urethral gonorrhea or chlamydia among STI clinic attendees. These findings suggest that circumcision has little impact on acquisition of these urethral bacterial infections

Data on the association of circumcision status and clinically apparent genital warts among heterosexual men are conflicting [9, 21, 23, 29–33]. Although a lower prevalence of polymerase chain reaction–based diagnoses of high-risk HPV was recently reported among circumcised heterosexual men in 2 circumcision trials [3, 5], observational data are inconsistent regarding the effect of circumcision on penile HPV infection [34]. There was no overall association of circumcision with self-reported genital warts in the HIM study, and this is the first time such a relationship has been examined in MSM

Several strengths of this study should be noted. First, the prospective nature of the HIM study avoided prevalence-incidence bias which may have been an issue in most other studies that assessed circumcision status and STI risk, employing a cross-sectional design. This may be an important bias; there is some evidence that the presence of a foreskin could lead to an altered clinical expression of infection with sexually transmitted pathogens [3, 29–31, 33]

Second, potential confounding demographic factors were assessed [18] and, where appropriate, included in the multivariate model. Third, the community-based nature of the HIM study avoided selection bias, which may be problematic in clinic-based studies if men of a particular circumcision status more commonly have, or notice, abnormal genital lesions. Fourth, self-reported circumcision status was validated by clinical examination in a subgroup of HIM study participants, and self-report was found to be a valid measure of circumcision status in this group [16]. Fifth, nondifferential misclassification was minimized by the use of highly sensitive and specific diagnostic testing algorithms for gonorrhea, chlamydia, syphilis, and HSV

In addition, the overall uptake of STI testing offered to HIM study participants was high; >90% of men agreed to STI testing during the study. Importantly, we sought to differentiate genital STIs for which the presence of a foreskin could plausibly affect the risk of acquisition during insertive sexual practices, with use of (1) analyses of site-specific anal gonorrhea and chlamydia infections and anal warts, which allowed direct comparison between anal infections, for which circumcision should afford no protection, and the same infections at genital sites; and (2) analyses of the subgroup of men who predominantly practiced the insertive role in UAI

A number of limitations of the study also need to be addressed. First, it is possible that some STIs may be associated with circumcision status but that the power of the study was insufficient to detect a significant effect during the study period. Nonetheless, a significant reduced risk of syphilis was observed in the HIM cohort despite the low incidence of infection (Tables 3 and 4). Second, for men with prevalent infections such as HSV and syphilis, especially those in whom life-long seropositivity persists [27, 28], imprecise or inadequate control for past sexual behavioral confounding factors may have influenced the outcome of this analysis. However, no prevalent infection examined in the HIM study was associated with circumcision status at either univariate or adjusted analysis (Table 2). Third, as already mentioned, the results of HSV and syphilis serological tests do not reveal the site of infection, and the lack of association with HSV-2 observed in the HIM study could be a result of infections being acquired at nonpenile sites, for which circumcision would have no plausible benefit. Finally, anogenital warts were self-reported in the HIM study. This may have resulted in some misclassification, as has been described elsewhere for anogenital warts among participants in the United States Multicenter AIDS Cohort Study [35]

Circumcision was associated with a reduced risk of incident syphilis in this cohort. It had little, if any, effect on most other prevalent and incident STIs. To confirm our findings, further prospective studies are warranted among MSM with higher STI incidence. Alternative biological or behavioral public health interventions are needed to combat increasing STI rates among homosexual men

Previous SectionNext Section

Footnotes

  • Potential conflicts of interest: none reported

  • Presented in part: 17th International Society for Sexually Transmitted Diseases Research Meeting/10th International Union against Sexually Transmitted Infections World Congress, 29 July to 1 August 2007, Seattle, Washington (late-breaker abstract 4)

  • Financial support: National Health and Medical Research Council (public health scholarship 351044 to D.J.T., 2005–2007) and Royal Australasian College of Physicians (GSK scholarship for virological research to D.J.T., 2008). The National Centre in HIV Epidemiology and Clinical Research and the National Centre in HIV Social Research are funded by the Australian Government Department of Health and Ageing. The Health in Men cohort study was funded by the National Institutes of Health, US Department of Health and Human Services (HIV Vaccine Design and Development Teams award N01-AI-05395 from the Division of Acquired Immunodeficiency Syndrome, National Institute of Allergy and Infectious Diseases), Australian Government Department of Health and Ageing (Canberra), New South Wales Health Department (Sydney), and National Health and Medical Research Council (project grant 400944)

  • Received March 27, 2009.
  • Accepted July 13, 2009.
Previous Section
 

References

  1. ↵
    1. Fenton KA,
    2. Imrie J
    . Increasing rates of sexually transmitted diseases in homosexual men in Western Europe and the United States: why. Infect Dis Clin North Am 2005;19:311-31.
    CrossRefMedlineWeb of Science
  2. ↵
    1. Weiss HA,
    2. Thomas SL,
    3. Munabi SK,
    4. Hayes RJ
    . Male circumcision and risk of syphilis, chancroid, and genital herpes: a systematic review and meta-analysis. Sex Transm Infect 2006;82:101-9.
    Abstract/FREE Full Text
  3. ↵
    1. Tobian AA,
    2. Serwadda D,
    3. Quinn TC,
    4. et al
    . Male circumcision for the prevention of HSV-2 and HPV infections and syphilis. N Engl J Med 2009;360:1298-309.
    CrossRefMedline
  4. ↵
    1. Sobngwi-Tambekou J,
    2. Taljaard D,
    3. Lissouba P,
    4. et al
    . Effect of HSV-2 serostatus on acquisition of HIV by young en: results of a longitudinal study in Orange Farm, South Africa. J Infect Dis 2009;199:958-64.
    Abstract/FREE Full Text
  5. ↵
    1. Auvert B,
    2. Sobngwi-Tambekou J,
    3. Cutler E,
    4. et al
    . Effect of male circumcision on the prevalence of high-risk human papillomavirus in young men: results of a randomized controlled trial conducted in Orange Farm, South Africa. J Infect Dis 2009;199:14-9.
    Abstract/FREE Full Text
  6. ↵
    1. Mehta SD,
    2. Moses S,
    3. Agot K,
    4. et al
    . Adult male circumcision does not reduce the risk of incident Neisseria gonorrhoeae, Chlamydia trachomatis or Trichomonas vaginalis infection: results from a randomized, controlled trial in Kenya. J Infect Dis 2009;200:370-8.
    Abstract/FREE Full Text
  7. ↵
    1. Sobngwi-Tambekou J,
    2. Taljaard D,
    3. Nieuwoudt M,
    4. Lissouba P,
    5. Puren A
    . Male circumcision and Neisseria gonorrhoeae, Chlamydia trachomatis, and Trichomonas vaginalis: observations in the aftermath of a randomised controlled trial for HIV prevention. Sex Transm Infect 2009;85:116-20.
    Abstract/FREE Full Text
  8. ↵
    1. Mor Z,
    2. Kent CK,
    3. Kohn RP,
    4. Klausner JD
    . Declining rates in male circumcision amidst increasing evidence of its public health benefit. PLoS One 2007;2:e861-e861.
    Medline
  9. ↵
    1. Lafferty WE,
    2. Hughes JP,
    3. Handsfield HH
    . Sexually transmitted diseases in men who have sex with men: acquisition of gonorrhea and nongonococcal urethritis by fellatio and implications for STD/HIV prevention. Sex Transm Dis 1997;24:272-8.
    MedlineWeb of Science
  10. ↵
    1. Tabet S,
    2. Sanchez J,
    3. Lama J,
    4. et al
    . HIV, syphilis and heterosexual bridging among Peruvian men who have sex with men. AIDS 2002;16:1271-7.
    CrossRefMedlineWeb of Science
  11. ↵
    1. Millett GA,
    2. Flores SA,
    3. Marks G,
    4. Reed JB,
    5. Herbst JH
    . Circumcision status and risk of HIV and sexually transmitted infections among men who have sex with men: a meta-analysis. JAMA 2008;300:1674-84. (erratum: JAMA 2009; 301:1126–9).
    Abstract/FREE Full Text
  12. ↵
    1. Jin F,
    2. Prestage GP,
    3. Kippax SC,
    4. et al
    . Risk factors for genital and anal warts in a prospective cohort of HIV-negative homosexual men: the HIM study. Sex Transm Dis 2007;34:488-93.
    MedlineWeb of Science
  13. ↵
    1. Jin F,
    2. Prestage GP,
    3. Kippax SC,
    4. et al
    . Epidemic syphilis among homosexually active men in Sydney. Med J Aust 2005;183:179-83.
    MedlineWeb of Science
  14. ↵
    1. Jin F,
    2. Prestage GP,
    3. Mao L,
    4. et al
    . Incidence and risk factors for urethral and anal gonorrhoea and chlamydia in a cohort of HIV-negative homosexual men: the Health in Men Study. Sex Transm Infect 2007;83:113-9.
    Abstract/FREE Full Text
  15. ↵
    1. Jin F,
    2. Prestage GP,
    3. Mao L,
    4. et al
    . Transmission of herpes simplex virus types 1 and 2 in a prospective cohort of HIV-negative gay men: the health in men study. J Infect Dis 2006;194:561-70.
    Abstract/FREE Full Text
  16. ↵
    1. Templeton DJ,
    2. Mao L,
    3. Prestage GP,
    4. Jin F,
    5. Kaldor JM
    . Self-report is a valid measure of circumcision status in homosexual men. Sex Transm Infect 2008;84:187-8.
    Abstract/FREE Full Text
  17. ↵
    1. McNally LP,
    2. Templeton DJ,
    3. Jin F,
    4. et al
    . Low positive predictive value of a nucleic-acid amplification test for non-genital Neisseria gonorrhoeae infections in homosexual men. Clin Infect Dis 2008;47:e25-7.
    Abstract/FREE Full Text
  18. ↵
    1. Templeton DJ,
    2. Mao L,
    3. Prestage G,
    4. Kaldor JM,
    5. Kippax S
    . Demographic predictors of circumcision status in a community-based sample of homosexual men in Sydney, Australia. Sex Health 2006;3:191-3.
    CrossRefMedline
  19. ↵
    1. Rogers WH
    . Regression standard errors in clustered samples. Stata Tech Bull 1993;13:19-23.
  20. ↵
    1. Talukdar A,
    2. Khandokar MR,
    3. Bandopadhyay SK,
    4. Detels R
    . Risk of HIV infection but not other sexually transmitted diseases is lower among homeless Muslim men in Kolkata. AIDS 2007;21:2231-5.
    CrossRefMedlineWeb of Science
  21. ↵
    1. Dave SS,
    2. Fenton KA,
    3. Mercer CH,
    4. Erens B,
    5. Wellings K
    . Male circumcision in Britain: findings from a national probability sample survey. Sex Transm Infect 2003;79:499-500. (erratum: Sex Transm Infect 2004; 80:78).
    FREE Full Text
  22. ↵
    1. Hart G
    . Factors associated with genital chlamydial and gonococcal infection in males. Genitourin Med 1993;69:393-6.
    MedlineWeb of Science
  23. ↵
    1. Richters J,
    2. Smith AM,
    3. de Visser RO,
    4. Grulich AE,
    5. Rissel CE
    . Circumcision in Australia: prevalence and effects on sexual health. Int J STD AIDS 2006;17:547-54.
    Abstract/FREE Full Text
  24. ↵
    1. Xu F,
    2. Markowitz LE,
    3. Sternberg MR,
    4. Aral SO
    . Prevalence of circumcision and herpes simplex virus type 2 infection in men in the United States: the National Health and Nutrition Examination Survey (NHANES), 1999–2004. Sex Transm Dis 2007;34:479-84.
    MedlineWeb of Science
  25. ↵
    1. Golden MR,
    2. Wasserheit JN
    . Prevention of viral sexually transmitted infections: foreskin at the forefront. N Engl J Med 2009;360:1349-51.
    CrossRefMedlineWeb of Science
  26. ↵
    1. Mulhall BP,
    2. Hart G,
    3. Harcourt C
    . Sexually transmitted diseases in Australia: a decade of change. Epidemiology and surveillance. Ann Acad Med Singapore 1995;24:569-78.
    Medline
  27. ↵
    1. Fatahzadeh M,
    2. Schwartz RA
    . Human herpes simplex virus infections: epidemiology, pathogenesis, symptomatology, diagnosis, and management. J Am Acad Dermatol 2007;57:737-63.
    CrossRefMedlineWeb of Science
  28. ↵
    1. Domantay-Apostol GP,
    2. Handog EB,
    3. Gabriel MT
    . Syphilis: the international challenge of the great imitator. Dermatol Clin 2008;26:191-202.
    CrossRefMedlineWeb of Science
  29. ↵
    1. Hernandez BY,
    2. Wilkens LR,
    3. Zhu X,
    4. et al
    . Circumcision and human papillomavirus infection in men: a site-specific comparison. J Infect Dis 2008;197:787-94.
    Abstract/FREE Full Text
  30. ↵
    1. Parker SW,
    2. Stewart AJ,
    3. Wren MN,
    4. Gollow MM,
    5. Straton JA
    . Circumcision and sexually transmissible disease. Med J Aust 1983;2:288-90.
    MedlineWeb of Science
  31. ↵
    1. Cook LS,
    2. Koutsky LA,
    3. Holmes KK
    . Clinical presentation of genital warts among circumcised and uncircumcised heterosexual men attending an urban STD clinic. Genitourin Med 1993;69:262-4.
    MedlineWeb of Science
  32. ↵
    1. Donovan B,
    2. Bassett I,
    3. Bodsworth NJ
    . Male circumcision and common sexually transmissible diseases in a developed nation setting. Genitourin Med 1994;70:317-20.
    MedlineWeb of Science
  33. ↵
    1. Aynaud O,
    2. Piron D,
    3. Bijaoui G,
    4. Casanova JM
    . Developmental factors of urethral human papillomavirus lesions: correlation with circumcision. BJU Int 1999;84:57-60.
    CrossRefMedlineWeb of Science
  34. ↵
    1. Gray RH,
    2. Wawer MJ,
    3. Serwadda D,
    4. Kigozi G
    . The role of male circumcision in the prevention of human papillomavirus and HIV infection. J Infect Dis 2009;199:1-3.
    FREE Full Text
  35. ↵
    1. Wiley DJ,
    2. Grosser S,
    3. Qi K,
    4. et al
    . Validity of self-reporting of episodes of external genital warts. Clin Infect Dis 2002;35:39-45.
    Abstract/FREE Full Text
| Table of Contents

This Article

  1. J Infect Dis. (2009) 200 (12): 1813-1819. doi: 10.1086/648376
  1. AbstractFree
  2. » Full Text (HTML)Free
  3. Full Text (PDF)Free

Classifications

Share

  1. Email this article

Navigate This Article

Current Issue

  1. March 1, 2012 205 (5)
  1. Journal of Infectious Diseases
  1. Alert me to new issues

Most