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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

  1. Supriya D. Mehta1,
  2. Stephen Moses3,4,,5,
  3. Kawango Agot6,
  4. Corette Parker2,
  5. Jeckoniah O. Ndinya-Achola7,
  6. Ian Maclean3 and
  7. Robert C. Bailey1
  1. 1 Department of Epidemiology and Biostatistics, University of Illinois at Chicago School of Public Health, Chicago, Illinois
  2. 2 RTI International, Research Triangle Park, North Carolina
  3. 3 Department of Medical Microbiology, Winnipeg, Canada
  4. 4 Department of Community Health Sciences, Winnipeg, Canada
  5. 5 Department of Internal Medicine University of Manitoba, Winnipeg, Canada
  6. 6 University of Nairobi, Illinois, and Manitoba Project, Kisumu
  7. 7 Department of Medical Microbiology, University of Nairobi, Nairobi, Kenya
  1. Reprints or correspondence: Dr. Mehta, 1603 W. Taylor St., M/C 923, Chicago, IL 60622 (supriyad{at}uic.edu).
 
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Abstract

Background We examined the effect of male circumcision on the acquisition of 3 nonulcerative sexually transmitted infections (STIs).

Methods We evaluated the incidence of STI among men aged 18–24 years enrolled in a randomized trial of circumcision to prevent human immunodeficiency virus (HIV) infection in Kisumu, Kenya. The outcome was first incident nonulcerative STI during 2 years of follow-up. STIs examined were laboratory-detected Neisseria gonorrhoeae, Chlamydia trachomatis, and Trichomonas vaginalis infection.

Results There were 342 incident infections among 2655 men followed up. The incidences of infection due to N. gonorrhoeae, C. trachomatis, and T. vaginalis were 3.48, 4.55, and 1.32 cases per 100 person-years, respectively. The combined incidence of N. gonorrhoeae and C. trachomatis infection was 7.26 cases per 100 person-years (95% confidence interval, 6.49–8.13 cases per 100 person-years). The incidences of these STIs, individually or combined, did not differ by circumcision status as a time-dependent variable or a fixed variable based on assignment. Risks for incident STIs in multivariate analysis included an STI at enrollment, multiple sex partners within <30 days, and sexual intercourse during menses in the previous 6 months; condom use was protective.

Conclusions Circumcision of men in this population did not reduce their risk of acquiring these nonulcerative STIs. Improved STI control will require more-effective STI management, including partner treatment and behavioral risk reduction counseling.

Three randomized clinical trials in Africa have shown that adult male circumcision reduces the risk of human immunodeficiency virus (HIV) acquisition among heterosexual men by 51%–76% [1–3]. The World Health Organization recommends male circumcision—in combination with other HIV prevention and reproductive health programs and services—as an important strategy for preventing HIV infection in areas where the prevalence of HIV infection in the general population is high and circumcision rates are low [4]. Several HIV-1 target cells, such as CD4+ T cells, macrophages, and Langerhans cells, are present in dense concentration in the unkeratinized inner mucosal surface of the foreskins of uncircumcised men [5–7], facilitating pathogen host cell attachment and entry. Other than keratinization of the penile skin, mechanisms by which circumcision may reduce the risk of acquiring HIV infection include decreased inflammation and trauma to the penis [7], increased genital hygiene of the prepuce [8], and decreased retention of secretions containing HIV. It is plausible that some of these mechanisms might also confer protection against acquisition of other sexually transmitted infections (STIs).

There is evidence from observational studies that male circumcision may reduce the risk of acquiring certain STIs. A meta-analysis of the association of male circumcision with STIs found statistically and clinically significant reductions in the risk of syphilis and chancroid [9]. However, no association has been observed between male circumcision and other bacterial STIs [10–15]. Among men enrolled in a randomized trial of adult male circumcision in Rakai, Uganda, the incidence of self-reported genital ulcer disease among circumcised men was almost half that among uncircumcised men, but there was no protective association observed for genital discharge or dysuria symptoms [2]. Although the experimental study design is strong, these results represent self-reported rather than laboratory-detected infections. We evaluated the effect of adult male circumcision and behavioral risks on the incidence of 3 non-ulcerative laboratory-diagnosed STIs among adult men participating in a randomized, controlled clinical trial of adult male circumcision to prevent HIV infection in Kisumu, Kenya.

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Methods

Study design and participants

The main trial design, circumcision technique, adverse events, and primary outcome (HIV infection) have been described elsewhere [3]. In brief, participants were recruited from sexually transmitted disease clinics, workplaces, social events, and youth organizations. Interested men were given an appointment for randomization and possible circumcision within 1 week after screening. For inclusion, men had to be uncircumcised, HIV uninfected, sexually active in the previous 12 months, and aged 18–24 years; have a hemoglobin level ⩾9.0 mmol/L; and reside in Kisumu District. Exclusion criteria included foreskin covering less than half of the glans, bleeding disorders, keloid formation, other conditions that might unduly increase the risks of elective surgery, and medical indications for circumcision. The study was approved by the institutional review boards of the University of Illinois at Chicago, Kenyatta National Hospital, RTI International, the University of Manitoba, and the University of Washington.

Clinical procedures and follow-up

After written informed consent, participants were randomized 1:1 to undergo either immediate circumcision or delayed circumcision after a 2-year follow-up period (the control group). Both groups underwent STI and HIV risk reduction counseling and were provided with unlimited supplies of free condoms. Men randomized to intervention underwent a standard forceps-guided procedure for circumcision, as described elsewhere [3].

Detailed evaluations were conducted at baseline and 1, 3, 6, 12, 18, and 24 months after randomization for both circumcision and control groups. At each visit, participants had a standardized medical history recorded and underwent physical examination; for planned visits occurring ⩾6 months after randomization, participants underwent personal interviews to obtain sociodemographic information and information on sexual behavior. Trained counselors interviewed participants in their language of choice (English, Dholuo, or Kiswahili).

Testing for STIs

At baseline and at 6-, 12-, 18-, and 24-month follow-up visits, participants were asked to provide urine specimens, which were tested for Neisseria gonorrhoeae and Chlamydia trachomatis by polymerase chain reaction (PCR) assay (Amplicor CT/NG test; Roche Diagnostics) and for Trichomonas vaginalis by culture (InPouch T. vaginalis test; BioMed Diagnostics). For men with urethral discharge, a urethral swab sample was also obtained for PCR testing (N. gonorrhoeae and C. trachomatis) and culture (N. gonorrhoeae and T. vaginalis). Men who presented between study visits with symptoms of infection were also tested, and their results are included in this analysis. Urine, urethral swab, and blood specimens were sent to the University of Nairobi Department of Medical Microbiology (Nairobi, Kenya) for testing. All tests were conducted according to manufacturers' instructions. Men who tested positive for N. gonorrhoeae, C. trachomatis, or T. vaginalis were traced and given appropriate treatment at the study clinic, in accordance with Kenyan national STI treatment guidelines. HIV testing methods have been reported in detail elsewhere [3].

Data used for analysis

Data for this analysis were collected as part of a randomized, controlled trial designed to assess the effect of male circumcision on reducing HIV seroconversion. The trial's target sample size was 2776 [3]. As a result of an interim analysis conducted in October 2006 (with 87% follow-up), the data and safety monitoring board stopped the trial in December 2006. The data presented here are the trial data, with follow-up through October 2006. Of the 1738 participants randomized at least 24 months plus 2 weeks before the October 2006 analysis, 1501 (86%) had completed their 24-month follow-up visit [3]. The percentage of men attending follow-up visits did not differ by treatment arm [3].

Statistical analysis

To be included in this analysis, participants had to be tested for all 3 infections during ⩾1 follow-up visit after randomization. The outcome measure for this analysis was the first incident infection, dichotomized as positive versus negative for each infection separately (N. gonorrhoeae, C. trachomatis, and T. vaginalis). Risks for N. gonorrhoeae and C. trachomatis infection were similar; thus, we also examined infection with N. gonorrhoeae and/or C. trachomatis as a combined outcome. For each outcome, we calculated incidence by dividing the number of persons with incident infection by the number of person-years at risk. Participants with multiple incident infections were censored at their first incident infection. Reinfections were examined for descriptive purposes and were defined as infections detected >30 days after the initial infection, provided that the initial infection was treated with appropriate antibiotic therapy. Observation times were calculated as the time from randomization to the individuals' first infection or the last visit at which they tested negative for an STI. We assumed that participants who missed interim study visits remained negative during the interim period.

Log-rank tests were used to explore the association of various risk factors individually. Variables significant at P <.05 by log-rank test were entered in a Cox proportional hazards regression model. In addition, Cox regression analysis was used to account for time-varying covariates and to compute hazard ratios (HRs) of incident STIs associated with circumcision status and sociodemographic and behavioral characteristics. Circumcision status was analyzed as a time-varying covariate, to take into account men who crossed over from the control group to the circumcision group and men who were randomized to intervention but did not undergo circumcision. In addition, treatment assignment was analyzed as a fixed variable (intention-to-treat analysis). The assumption of proportionality for Cox proportional hazards was assessed by graphical inspection of Nelson-Aalen curves and by testing for a nonzero slope in a generalized linear regression of the scaled Schoenfeld residuals on functions of time. Statistical significance for the selection of variables to be retained in each multivariate model was determined by Holm adjustment for multiple tests of significance [16]. Standard errors were estimated using a robust variance estimate (sandwich estimator). The Efron method was specified to approximate the exact conditional probability of tied events [17]. Data were analyzed using Stata/SE for Windows software (version 9.2; Stata).

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Results

Study population

There were 2784 men enrolled in the trial, 2655 (95.4%) of whom were tested for the 3 infections during follow-up. Of these men, 1318 were randomized to undergo circumcision, and 1337 were randomized to the control group. Crossovers from treatment assignment included 16 control subjects who were circumcised and 57 men who were randomized to undergo circumcision but were not circumcised. The control and treatment arms were well balanced with regard to sociodemographic details, behavioral characteristics, baseline STI prevalences, and duration of follow-up [3].

Incidence rates of infection

Of 2655 men who underwent STI testing at follow-up, 361 had 398 infections, including 148 N. gonorrhoeae, 193 C. trachomatis, and 57 T. vaginalis infections. Nearly one-fourth of infected men (85; 23.6%) had infections detected at interim visits. There were 25 men with N. gonorrhoeae and C. trachomatis coinfection, 2 with C. trachomatis and T. vaginalis coinfection, 8 with N. gonorrhoeae and T. vaginalis coinfection, and 1 with N. gonorrhoeae, C. trachomatis, and T. vaginalis coinfection. The incidences of first infection due to N. gonorrhoeae, C. trachomatis, and T. vaginalis were 3.48, 4.55, and 1.32 cases per 100 person-years (table 1). The combined incidence of N. gonorrhoeae and/or C. trachomatis infection was 7.26 cases per 100 person-years (95% confidence interval [CI], 6.49–8.13 cases per 100 person-years). One hundred sixty-eight N. gonorrhoeae infections occurred in 148 men; 20 reinfections occurred in 18 men, 6 of which occurred within the same follow-up interval as the first infection. Two hundred C. trachomatis infections occurred in 193 men; 7 reinfections occurred in 7 men during follow-up intervals after the initial infection. Sixty-one T. vaginalis infections were detected in 57 men; 1 of the 4 reinfections occurred during the same follow-up interval in which an N. gonorrhoeae infection occurred. Overall, the incidence of first infection with a nonulcerative STI in this cohort was 8.34 cases per 100 person-years (95% CI, 7.50–9.28 cases per 100 person-years); this incidence was minimally affected by inclusion of reinfections (8.77 cases per 100 person-years [95% CI, 7.93–9.69 cases per 100 person-years]).

View this table:
Table 1

Incidences of Neisseria gonorrhoeae, Chlamydia trachomatis, and Trichomonas vaginalis Infections

Effect of circumcision status on incidence of nonulcerative STI

The incidences of nonulcerative STIs, individually or combined, did not differ by circumcision status as a time-dependent variable or as a fixed variable based on assignment (table 1). Incidence rate ratios for circumcised versus uncircumcised men (time-dependent circumcision status) were 0.95 for N. gonorrhoeae infection (95% CI, 0.68–1.34; P p.781 ), 0.87 for C. trachomatis infection (95% CI, 0.65–1.16; P = .325), 0.89 for N. gonorrhoeae and/or C. trachomatis infection combined (95% CI, 0.70–1.12; P = .305), and 0.77 for T. vaginalis infection (95% CI, 0.44–1.36; P = .346).

Incidence of nonulcerative STI by sociodemographic and behavioral characteristics and baseline infection status

The incidences of N. gonorrhoeae and C. trachomatis infection were increased among men with lower educational attainment, baseline N. gonorrhoeae or C. trachomatis infection, multiple sex partners reported in the 30 days previous to the visit at which infection was detected, and a history of having sex with a woman during her menses in the 6 months before infection was detected (table 1). For both N. gonorrhoeae and C. trachomatis infection, the incidence rates were highest among men who reported having sex during a woman's menses (N. gonorrhoeae and C. trachomatis, 8.0 and 9.3 cases per 100 person-years, respectively) and among those who had baseline N. gonorrhoeae and/or C. trachomatis infection (N. gonorrhoeae and C. trachomatis, 9.8 and 9.3 cases per 100 person-years, respectively; data not shown). The incidence of T. vaginalis infection was low, and few baseline factors distinguished men with infection at follow-up from those who were not infected (table 1). Men who reported a preference for dry vaginal sex had an increased incidence of T. vaginalis infection but not of N. gonorrhoeae or C. trachomatis infection, compared with men who preferred wet vaginal sex. The incidence rate of each infection was lower by 35%–50% among men reporting condom use at their last sexual intercourse. Marital status and herpes simplex virus type 2 infection at baseline were not significantly associated with increased incidence of nonulcerative STI. Only 7 HIV seroconversions occurred among men who also had incident nonulcerative STI; HIV seroconversion was detected in the same follow-up interval as was STI for 6 of the men. Thus, HIV seroconversion was not examined as a predictor of STI.

Cox proportional hazards regression: risks for infection

In multivariate regression, risks for N. gonorrhoeae and C. trachomatis infection were similar (table 2) and included N. gonorrhoeae or C. trachomatis infection at baseline, multiple recent sex partners, and sexual intercourse with a woman during menses. Condom use at last intercourse remained significantly protective against N. gonorrhoeae infection (HR, 0.50) and T. vaginalis infection (HR, 0.52) in multivariate analysis but not against C. trachomatis infection. The only other significant risk factors for T. vaginalis infection were baseline infection with C. trachomatis or T. vaginalis. Men who reported that their penis had been abraded or felt sore during intercourse in the 6 months before infection was detected had an increased risk for N. gonorrhoeae infection (HR, 1.61). There was no statistically significant or meaningful 2-way interaction term in any model. Examination of Schoenfeld residuals identified no violation of the assumption of proportionality for each independent variable or for the global test of each model.

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Table 2

Multivariate Cox Proportional Hazards Regression Analysis: Relative Hazards of Neisseria gonorrhoeae, Chlamydia trachomatis, and Trichomonas vaginalis Infections

Cox proportional hazards regression: risks for infection with N. gonorrhoeae and/or C. trachomatis

We combined N. gonorrhoeae and C. trachomatis infection at follow-up into a single outcome, owing to similarities in stratified models and to increase our power to detect significant associations (table 3). In a multivariate Cox regression analysis, N. gonorrhoeae or C. trachomatis infection at enrollment (HR, 2.31 [95% CI, 1.64–3.26]), multiple sex partners in the previous 30 days (HR, 2.15 [95% CI, 1.42–3.27]), and sexual intercourse during a woman's menstruation (HR, 1.67 [95% CI, 1.19–2.33]) remained significant predictors of N. gonorrhoeae and/or C. trachomatis infection (table 3). Conversely, higher education (HR, 0.67 [95% CI, 0.50–0.88]) and reported condom use at last intercourse (HR, 0.64 [95% CI, 0.50–0.82]) were protective against infection. There was no statistically significant or meaningful 2-way interaction term and no violation of the assumption of proportionality for each independent variable or for the global test of the model.

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Table 3

Univariate and Multivariate Cox Regression Analysis: Relative Hazards of Incident Neisseria gonorrhoeae and Chlamydia trachomatis Infections

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Discussion

We did not find that adult male circumcision had a protective effect against any of the nonulcerative STIs examined (N. gonorrhoeae, C. trachomatis, or T. vaginalis infection) in these sexually active young men in Kisumu, Kenya. Multiple differences in organism pathogenesis and host immunogenicity may explain why circumcision may confer protection against HIV infection but not against these STIs. Specific HIV-1 target cells may be protected through increased keratinization resulting from circumcision; HIV-1 must attach to the CD4 receptor for cell entry. Bacterial STIs, such as N. gonorrhoeae, C. trachomatis, and T. vaginalis infection, however, may bind through multiple ligands and host receptors [18]. Unlike the chlamydia organism, gonococci are not obligate intracellular organisms, and T. vaginalis has complex and multiple methods of adhering to and entering host cells. The preferred host cell site is cuboidal or columnar epithelium (internal to the urethra) for both N. gonorrhoeae and C. trachomatis; thus, it is very unlikely that intact foreskin would provide protection against these infections. The suggestion of a protective effect stemmed from analysis of non-experimental study designs [19] rather than from a biological rationale. The findings of our randomized, controlled trial showing no association between circumcision status and these STIs confirm findings from several other studies with nonexperimental designs [11–14]. It is not likely that a longer observation period would have been necessary to demonstrate any potential protective effects; graphical inspection of the estimated cumulative hazard rate appears constant, and biological protective effects would be expected to appear shortly after circumcision. However, as demonstrated by statistical modeling, the effectiveness of circumcision in reducing the burden of HIV infection in the population varies by prevalence of circumcision, prevalence of HIV infection, and sexual behavior [20]; thus, adult male circumcision may have different effects on the risk of nonulcerative STIs at the population level, varying with population-level sexual practices and the prevalence of STIs and circumcision.

Despite the lack of protection against infection with N. gonorrhoeae, C. trachomatis, or T. vaginalis, adult male circumcision may have other beneficial effects on STIs, such as reduced transmission to sexual partners or decreased acuity or sequelae of infection. Among women enrolled as control subjects in a cervical cancer study in 5 countries, self-reported circumcision in male sex partners was strongly protective against C. trachomatis infection in the women [21]. Conversely, a cohort study examining hormonal contraception and the risk of HIV infection among women in 3 countries found that male sex partners' self-reported circumcision status was not associated with incident N. gonorrhoeae, C. trachomatis, or T. vaginalis infections in women [22]. However, few studies have examined this issue, and none were specifically designed to assess the association between male circumcision and the risk of STIs in female partners. Prospective studies comparing STI incidence among sexual partners and the course of infection among circumcised and uncircumcised men are necessary to determine a broader range of potential benefits of adult male circumcision.

Data on the incidence of nonulcerative STI among adolescent men in sub-Saharan Africa are limited, but the rates that we observed (combined incidence of N. gonorrhoeae and/or C. trachomatis infection, 7.26 cases per 100 person-years) seem to be relatively high. Among trucker drivers aged 16–62 years from Mombasa, Kenya, who were enrolled in a cohort study during 1993–1994, the incidence of N. gonorrhoeae infection was 12.6 cases per 100 person-years and the incidence of nongonococcal urethritis was 7.5 cases per 100 person-years [23]. As part of a 1997–1998 cross-sectional study in 4 sub-Saharan African cities, the prevalences of N. gonorrhoeae and C. trachomatis infection were 0% and 2.6%, respectively, among a representative sample of Kisumu men aged 15–49 years [24]. Beyond comparison with other populations, the incidence that we observed seems to be high contextually; the young men were enrolled in a study that provided ongoing testing and treatment for STIs, and men received risk-reduction counseling and unlimited numbers of free condoms. Men with baseline N. gonorrhoeae and C. trachomatis infection were at increased risk of reinfection. This suggests that men may become reinfected by infected partners. Infected men in the trial were given coupons for their sex partners to receive free treatment at a nearby clinic, but we do not know how many partners sought treatment. Our results suggest that more-aggressive partner tracing and treatment might be warranted.

Sexual intercourse with a woman during her menses was a risk factor for N. gonorrhoeae and C. trachomatis infection in stratified and combined analyses. In a previous analysis of our data, among men who were excluded from the trial because they were HIV infected at baseline, sexual intercourse with a woman during her menses was a risk factor for prevalent HIV infection in multivariate analysis [25]. Some studies have demonstrated increased HIV load during the menstrual phase of the menstrual cycle [26, 27]. In 1 study, sex partners of men with a diagnosis of gonorrhea were more likely to test positive for gonorrhea if they were tested during the menstrual phase rather than during other phases of the menstrual cycle [28], possibly because of increased organism shedding. There are limited published data quantifying STI organism load and transmission throughout the menstrual cycle. Individual studies suggest that mechanisms may include increased organism load or increased pathogenicity of organisms during menses as a result of altered genital flora [29]. Although further study is necessary to elucidate female-to-male transmission of STIs during the menstrual cycle, current counseling and prevention efforts could emphasize avoiding sexual intercourse during a woman's menses and using condoms.

Men who reported coital injuries (penis cut, scratched, or abraded during sexual intercourse in the 6 months before detected infection) had an increased risk of N. gonorrhoeae infection. The nature of these injuries and the mechanism by which they may increase the risk of infection are unknown. Use of condoms reduced the risk of infection by more than one-third, emphasizing the importance of promoting condom use.

The incidence (1.32 cases per 100 person-years) and baseline prevalence (2.1%) of T. vaginalis infection in our population was low, compared with prevalences detected in cross-sectional studies in other sub-Saharan countries. The prevalence of trichomoniasis was 11% among men aged 15–54 years in rural Tanzania [30] and 6.3% among male sex partners of a community-based sample of women in Moshi, Tanzania [31]. Because the epidemiological mechanism of T. vaginalis infection among African men is largely unknown, specific behaviors and sexual practices that increase risk may not have been measured in our study.

Limitations of the original trial have been reviewed elsewhere [3]; thus, our discussion of limitations is confined to the current analysis. If a large proportion of infected men sought treatment outside the study clinic, those infections would not be accounted for in this analysis, which would potentially lead to an underestimation of incidence and, thus, bias the results toward the null. Some participants did not attend all scheduled follow-up visits, but <5% of enrolled men did not have any follow-up testing for STIs. These men were significantly less likely than men with STI testing at follow-up to report coital injuries (results not shown). However, their baseline characteristics did not differ from those of men who received follow-up with regard to the number of sex partners in the previous 30 days; baseline infection with N. gonorrhoeae, C. trachomatis, or T. vaginalis; sexual intercourse during a woman's menses, condom use at last intercourse, age, educational attainment, or treatment assignment. Finally, behavioral risks were self-reported and were therefore subject to limitations of recall and socially desirable reporting.

In conclusion, we did not observe that circumcision protected against acquisition of these nonulcerative STIs. Data are lacking on whether adult male circumcision affects transmission of nonulcerative STIs to sexual partners. We measured a high incidence of STIs among a cohort of young men, despite their participation in a clinical trial that included intensive STI diagnosis and treatment, HIV risk-reduction counseling, follow-up, and a free supply of condoms. This suggests that more-effective safe sex counseling content and delivery methods must be identified, especially if circumcision is not a means of STI prevention and control. Increased STI risk among men with previous infections suggests that treatment of partners is also important.

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Footnotes

  • Potential conflicts of interest: none reported.

  • Financial support: Family Health International, supported by the US Government and the Bill and Melinda Gates Foundation (to R.C.B.); Division of AIDS, National Institute of Allergy and Infectious Diseases, National Institutes of Health (AI50440); and Canadian Institutes of Health Research (HCT 44180; investigator award to S.M.).

  • Received December 16, 2008.
  • Accepted February 27, 2009.
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  1. J Infect Dis. (2009) 200 (3): 370-378. doi: 10.1086/600074
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