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AIDS Patient Care and STDs
AIDS Patient Care STDS. May 2009; 23(5): 315–321.
PMCID: PMC2743100
NIHMSID: NIHMS131245

Willingness to Be Circumcised for Preventing HIV among Chinese Men Who Have Sex with Men

Yuhua Ruan, Ph.D.,1,* Han-Zhu Qian, M.D., Ph.D.,2,* Dongliang Li, M.D.,3 Wei Shi, M.D., Ph.D.,3 Qingchun Li, M.D.,1 Hongyuan Liang, M.D.,1 Ye Yang, M.D.,3 Fengji Luo, M.D.,3 Sten H. Vermund, M.D., Ph.D.,2 and Yiming Shao, M.D., Ph.D.corresponding author1

Abstract

Male circumcision can reduce the risk of HIV acquisition among heterosexual men, but its effectiveness is uncertain in men who have sex with men (MSM). Additionally, its acceptability among Chinese men is unknown given a lack of history and cultural norms endorsing neonatal and adult circumcision. This study evaluated the willingness to participate in a clinical trial of circumcision among 328 Chinese MSM. Some 11.6% respondents reported having been circumcised, most of them due to a tight foreskin. Of 284 uncircumcised MSM, 16.9% said they were absolutely willing to participate, 26.4% were probably, 28.9% were probably not, and 27.8% were absolutely not; 81% said male circumcision would help maintain genital hygiene. The major motivators for willingness to participate included contribution to AIDS scientific research and getting free medical service. Men also had concerns about ineffectiveness of circumcision in reducing HIV/sexually transmitted infection (STI) risks and side effects of the surgery. Those who did not have a Beijing resident card (adjusted odds ratio [AOR], 1.99; 95% confidence interval [CI], 1.17–3.38), did not find sexual partners through the Internet (AOR, 2.13; 95% CI, 1.21–3.75), and were not concerned about the effectiveness of circumcision (AOR, 2.37; 95% CI, 1.34–4.19) were more likely to be willing to participate in a trial. The study suggests that circumcision is uncommon among Chinese MSM. Considerable community education will be needed in circumcision advocacy among MSM in China. A clinical trial for efficacy among MSM should be considered.

Introduction

The year 2007 saw major setbacks in the development of HIV vaccines and microbicides and diaphragm intervention. The STEP and Phambili HIV vaccine trials were stopped because the vaccines were regarded unlikely to prevent HIV infection or reduce the amount of virus in those who became infected.1,2 Two microbicide trials sponsored by Family Health International and CONRAD were also stopped prematurely because of safety concerns.3,4 A randomized clinical trial in South Africa did not show added protective benefit of diaphragm against HIV infection when the diaphragm and lubricant gel were provided in addition to condoms and a comprehensive HIV prevention package.5 In contrast, significant progress was made in the evaluation of male circumcision for preventing HIV. Two randomized clinical trials were published in 20076,7 and confirmed one previously published clinical trial8 and many other observational studies9 that circumcision could lower the risk of HIV acquisition by 51% to 62% in heterosexual men.

Mechanisms have been proposed by which the presence of the foreskin may increase biologic susceptibility to HIV acquisition. There are high densities of HIV target cells in the inner mucosal surface of the human foreskin, including Langerhans' cells, CD4+ T cells, and macrophages,10 and these cells express the CCR5 and CXCR4 HIV-1 coreceptors.11 These HIV target cells lie beneath a protective layer of keratin, which is absent on the inner surface of the prepuce.12 By removing part or all of the foreskin, circumcision reduces both the number and susceptibility of target cells to HIV infection. Based on biologic, observational, and clinical evidence, the World Health Organization (WHO) and UNAIDS recommend promoting male circumcision as “an additional, important strategy for the prevention of heterosexually-acquired HIV infection in men.”13

There are sparse and equivocal data on the association of male circumcision and homosexual acquisition of HIV in men who have sex with men (MSM).14,15 The impact of male circumcision in MSM may differ from that in heterosexual men, because MSM can play versatile roles in sex with male partners (both insertive and receptive). MSM may be exposed to risk of HIV acquisition through both the penis and anal mucosa. Due to the susceptibility of anal mucosa to trauma, the risk of HIV infection through receptive anal sex is very high. Therefore, circumcision may not be protective for MSM except in those who practice exclusively insertive sex. Nevertheless, since there are only a limited number of proven HIV prevention measures, it is warranted to investigate the feasibility of a male circumcision intervention and its effects on reducing the risk of HIV acquisition in MSM.

MSM is a subgroup population heavily affected by HIV epidemic in many regions and communities around the world. In China, the risk factors of HIV are shifting from contaminated plasma collection and injection drug use to heterosexual and homosexual contacts. As of the end of 2007, some 700,000 Chinese were estimated to live with HIV/AIDS, 40.6% acquired the virus through heterosexual contacts, and 11.0% through homosexual route.16 In MSM population, HIV prevalence reached more than 3% in some cities, and syphilis prevalence was over 10% in many parts of the country.1722 For example, HIV prevalence in MSM rose from 0.4% in 2004 to 4.6% in 2005 and 5.8% in 2006 in Beijing.23 However, prevention interventions in Chinese MSM have been very limited, and the rising epidemic calls for both validated and innovative interventions.

Male circumcision is rarely practiced among Chinese male infants, and the feasibility of providing circumcision among Chinese adult men is unknown. To prepare for future male circumcision interventions and possible clinical trials among Chinese MSM, this study evaluated the prevalence of circumcision in this population and assessed their willingness to participate in a circumcision clinical trial.

Methods

Study participants and recruitment

The study participants were recruited from an ongoing MSM cohort in China's capital city, Beijing, from September to November 2007. This first Chinese prospective MSM cohort was enrolled in 2006 and 507 participants were recruited in three ways. The first method was through advertising at websites of the National Center for AIDS/STD Control and Prevention (www.Chinaids.org.cn) and a nongovernmental AIDS volunteer group (www.hivolunt.net). Second, 10 peer recruiters were hired and trained to reach out to clubs, bars, parks, and bath-houses frequented by MSM and distribute flyers with study-related information. Third, study participants were encouraged to refer their peers to participate in the study. All potential participants came to a district HIV testing and counseling clinic in downtown Beijing for eligibility assessment. Eligibility criteria included self-reported same-gender sex in the past 3 months, 18 years or older, living in Beijing with no plan to leave Beijing in next year, and willingness to provide written informed consent. The cohort was followed up every 3 months aiming to estimate the incidence of HIV and syphilis and assess the retention rate for preparation of future clinical trials. The participants for this study were recruited at the 9-month follow-up visit of the cohort. Of 394 participants successfully followed up at this time point, 328 were enrolled in this survey. Informed consent was obtained from each participant. The study protocol was approved by the Institutional Review Boards of the National Center for AIDS/STD Control and Prevention, China and Vanderbilt University, Nashville, Tennessee.

Data collection

Data were collected using a one-on-one interview questionnaire administered by trained interviewers in a private room. Prior to interview, the interviewer read an introduction about the surgery of male circumcision, its effect and mechanisms of reducing HIV risk among heterosexual men, its unknown effect among MSM, and the purpose of this study to assess their willingness to participate in a circumcision clinical trial.

Data on demographic characteristics (age, monthly income, ethnicity, education, employment, marriage, and having a Beijing resident card), risky sexual behaviors in the past 3 months (finding sexual partner through the Internet, multiple sexual partners, unprotected anal sex with regular and causal sexual partners, had sex with female partners, perceived risk of contracting HIV), and illicit drug use in the past 3 months were collected in the original cohort study. A brief questionnaire was used in this study to collect information on history of circumcision, perceptions about circumcision (its health aspects on genital hygiene, protection against HIV and other sexually transmitted diseases (STDs), impacts on sexual pleasure, and impact on finding sexual partners), and concerns about participation in a male circumcision trials (effectiveness of the intervention and side effects of circumcision surgery). We did not perform genital examination to check circumcision status due to logistical and financial reasons. A unique and confidential identification code was assigned for each questionnaire, which linked to laboratory testing results.

New infection of HIV and syphilis were tested every 3 months. The HIV infection status was determined by an enzyme immunoassay (EIA; Beijing Wantai Biological Medicine Company, China) screening and a HIV-1/2 Western blot confirmation (HIV Blot 2.2 WB™, Genelabs Diagnostics, Singapore). Syphilis infection was determined using an EIA (Beijing Wantai Biological Production Company, Beijing, China) and confirmed a Passive Particle Agglutination Test for Detection of Antibodies to Treponema pallidum (TPHA™, OMEGA, UK).

The willingness to participate in a circumcision trial was assessed on a four-point scale designed to reflect Chinese language usage are as follows:

  1. “I am absolutely willing to participant” [definitely];
  2. “I am probably willing to participate” [probably];
  3. “I am probably not willing to participate” [probably not];
  4. “I am absolutely not willing to participate” [definitely].

Data analysis

Questionnaire data were double entered and compared using EpiData software (EpiData 3.0 for Windows; The EpiData Association Odense, Denmark). After cleaning, the data were then converted and analyzed using Statistical Analysis System (SAS 9.1 for Windows; SAS Institute Inc., NC).

We created a dichotomous variable for willingness to participate. Those who were definitely or probably willing to participate were combined as willing to participate and those who were probably not or definitely not willing to participate were combined as not willing to participate.

Univariate analyses including χ2 test, Fisher's exact test, and Wilcoxon two-sample test were performed to evaluate associations of willingness to participate with demographic characteristics, drug use, sexual behaviors, and perceptions and concerns about participation in a circumcision trial. Variables significant at a level of p = 0.10 were fitted in a multivariate logistic regression model to estimate the factors associated with willingness to participate, and only the factors significant at a level of 0.05 (two-tailed) were reported.

Results

Demographic characteristics of participants

The participants were recruited from an ongoing MSM cohort who have completed 9-month follow-up. The 9-month follow up rate was 78%. HIV prevalence was 4.8% and incidence was 2.09 per 100 person-years; syphilis prevalence was 19.8% and incidence was 9.0 per 100 person-years.

Of 328 MSM who participated in the survey, 38 reported that they had been circumcised and 6 did not know their circumcision status. Therefore, 284 participants were included in the analyses of their willingness to participate in a circumcision trial. The median age was 27 years (interquartile range: 24–32); 7.4% had less or some secondary school, 21.5% had secondary school, and 71.1% had college or high education level, respectively. A total of 92.6% belonged to Han ethnic group and 0.7% were Muslims. The median monthly income was 3000 Chinese yuan (RMB, 1 dollar ≈7.7 yuans in 2006, interquartile range: 1600–4000). A total of 89.2% were employed and 7.9% were students. Eighteen percent were married or cohabited with female sex partners. A total of 34.5% had a Beijing residence card. A total of 64.8% had anal intercourse with their regular male sex partners and 28.5% had anal intercourse with their casual male sex partners in the past month, respectively. A total of 22.9% had unprotected anal intercourse with the regular male sex partners and 4.6% had unprotected anal intercourse with the casual male sex partners in the past month, respectively. A total of 54.9% had 2 or more male sex partners in the past 3 months. Twenty-two percent of participants reported completely insertive anal sex, 7.8% completely receptive sex, and the remaining reported both. In addition, 10.9% had sex with their regular female sex partners and 3.5% had sex with their casual female sex partners in the past month, respectively. No participant reported using drugs in the past 3 months.

Prevalence of circumcision

Thirty-eight men (11.6%) reported having been circumcised. Of them 31 (81.6%) were due to a tight foreskin and 5 (13.2%) for the sake of personal hygiene.

Those who were circumcised were less likely to be married than those who were not circumcised (2/38 versus 51/284; p < 0.05). There was no difference in other demographic variables between circumcised and uncircumcised.

Perceptions about male circumcision and concerns about participation in a circumcision trial

As shown in Table 1, approximately 43% of participants thought they had a great or moderate risk of HIV via sex with male partners. The majority (81%) said male circumcision would help maintain genital hygiene. Over half of participants could not judge whether circumcision might increase sexual pleasure of their own or their partners. Approximately 45% thought being uncircumcised might increase the risk of acquiring HIV or other sexually transmitted diseases (STDs); meanwhile more than one quarter believed that the risk was same for those circumcised and uncircumcised.

Table 1.
Perceptions about Male Circumcision among Two Hundred Eighty-Four Chinese Men Who Have Sex with Men

Two thirds of participants had concerns about side effects of circumcision, specifically about pains (46.5%), infections (12.7%), reduction of sexual pleasure (5.3%), and bad appearance (2.5%). Participants also expressed concerns about ineffectiveness of circumcision against HIV/STDs, and that people might think they were at high risk of HIV for participating in a clinical trial (Fig. 1).

FIG. 1.
Concerns about participation in a circumcision trial among 284 Chinese men who have sex with men (MSM).

Willingness to participate in a circumcision clinical trial

Of 284 participants who had never been circumcised, 48 (16.9%) reported that they were absolutely willing to participate; 75 (26.4%) were probably willing to participate; 82 (28.9%) were probably not; and 79 (27.8%) were absolutely not willing to participate. Those who were definitely or probably willing to participate were combined as willing to participate and those who were probably not or definitely not willing to participate were combined as nonwilling to participate. Therefore, nearly 43% were willing to participate and 57% were not willing to participate.

Among 123 subjects willing to participate, 122 responded that they wanted to “contribute to AIDS scientific research”; 2 said they wanted to get free male circumcision; and all respondents said they want to get free HIV counseling and testing.

Predictors of willingness to participate in a circumcision trial

Univariate logistic regression analyses were performed to compare the willing to participate and unwilling to participate groups in terms of the following variables: demographics (age, income, ethnicity, education, employment, marriage and having a Beijing resident card), risky sexual behaviors (finding sexual partner through the Internet, multiple sexual partners, unprotected anal sex with regular and causal sexual partners, had sex with female partners, perceived risk of contracting HIV), perceptions about circumcision (its health aspects on genital hygiene, protection against HIV and other STDs, impacts on sexual pleasure, and impact on finding sexual partners), and concerns about participation in a circumcision trials (effectiveness and side effects of circumcision). All variables that are significant at the level of p = 0.10) are presented in Table 2.

Table 2.
Predictors of Willingness to Participate in a Circumcision Trial among Two Hundred Eighty-Four Chinese Men Who Have Sex with Men

All variables in Table 2 are included in a multivariate logistic regression model, and only those significant at p < 0.05 were retained in the final model. The analysis showed that three variables are independent predictors for willingness to participate in a circumcision trial. Those who did not have a Beijing resident card (adjusted odds ratio [AOR], 1.99; 95% confidence interval [CI], 1.17–3.38), did not find sexual partners through Internet (AOR, 2.13; 95% CI, 1.21–3.75), and were not concerned about the effectiveness of circumcision (AOR, 2.37; 95% CI, 1.34–4.19) were more likely to be willing to participate in a trial (Table 2).

Discussion

Nearly 12% (38/328) of MSM participants reported having been circumcised. Of those, 81.6% (31/38) were due to a tight foreskin and 13.2% (5/38) were for the sake of personal hygiene. The prevalence is lower than among men in most African, Middle East, and Western countries.24,25 Infant circumcision is not a traditional practice in China except among Muslims, who account for less than 3% of the population. The few circumcision surgeries performed are mostly done in early childhood when parents become aware of a tight foreskin problem or they are done in young adults for consideration of genital hygiene.

Approximately 43% uncircumcised MSM in our study reported that they would like to participate in a circumcision trial for preventing homosexual transmission of HIV. A study in Peru showed that the circumcision rate among MSM was low (3.7%) but willingness to participate was higher (54.3%) than in our study sample.26 Clearly, there are widespread cultural differences in attitudes and practices regarding circumcision and these should be taken into consideration in planning circumcision trials and intervention programs.

Studies have shown that the facilitators for willingness to receive circumcision and participate in circumcision trials include maintaining penile hygiene, protection against HIV and sexually transmitted infections (STIs), being in a certain ethnic or religious group such as Muslim, increasing sexual pleasure, making use of a condom easier, and receiving free medical care and monetary incentives27,28; the barriers include fear of pain, cultural and religious restrictions, cost of the surgery and time away from work, the risk of adverse effects, and other reasons such as lack of access to health care, fear of loss of penile sensitivity, and concerns about reduction in penis size and reducing sexual pleasure. Other barriers for participation in circumcision trials also include uncertainty about trial efficacy and associated stigma and discrimination.27,28 Our study showed several similar facilitators for participation in a circumcision trial such as maintaining genital hygiene and reducing risks of acquiring HIV and sexually transmitted infections, as well as potential barriers such as worry about associated stigma of participation in a trial and concerns about ineffectiveness and side effects of circumcision.

Complications of circumcision by traditional or unqualified practitioners in informal settings could be very common,29 and men should have less concern about complications if the surgery is performed by well-trained professionals. In our study sample, those who did not have a Beijing residence card, did not find sexual partners through the Internet and were not concerned about the effectiveness of male circumcision were more likely to be willing to participate in a trial. Migrants who don't have a Beijing resident card often have low access to medical insurance and might be more motivated to join a trial that offers free medical care. On the other hand, migrants might be more difficult to be retained in a trial for follow-up assessments. Recruiting MSM participants via the Internet could potentially be effective. The number of active Chinese Internet users has been growing at a steady annual rate of 18% in the past several years and reached around 200 million in 2007. The users of the gay websites are relatively young and well educated, and highly vulnerable to HIV/AIDS.30 However, those who were recruited through non-internet routes were more willing to join a trial. Traditional routes such as outreach contact and peer referral should be prioritized in recruiting MSM study participants for longitudinal studies.

This study had several limitations. Any studies investigating attitudes and behaviors based on interviewing may be limited by social desirability bias and our study is no exception. Social desirability bias might lead to overestimation of willingness to participate in our study. In addition, our study evaluated stated willingness to participate in a hypothetical male circumcision trial among MSM. Stated willingness to participate and actual enrollment decisions may be very different. The participants in this study were recruited from an existing study cohort. Due to their experience with research and with HIV testing, their responses may be quite different from MSM with no experience as research subjects. Future studies are needed to evaluate actual enrollment. Another limitation is that circumcision status was reported by the subjects and no clinical examination was performed to verify the self-reports. In this study we did not mention if a circumcision trial is a randomized one; nether did we assess if adult circumcision might be a stigma-producing factor for men in the health care setting. Circumcision may be linked to high HIV risk by health care providers, and providing institutional regarding protection procedures may reduce discrimination by providers.31 All of the information may be important for designing a circumcision trial and should be included in future relevant studies.

Unlike in MSM in many Western countries whose risk of HIV/AIDS are largely attributable to injection drug use, available data have consistently shown that Chinese MSM in urban areas rarely inject illicit drugs and their risk of acquiring HIV is mainly due to their risky sexual behaviors.17 Therefore, Chinese MSM are an optimal target population for evaluating the impact of circumcision on reducing the risks of HIV/STIs. As adult male circumcision is rarely performed in China, feasibility studies are needed to evaluate the adverse events of the surgery and collect preliminary data to estimate the parameters for conducting larger clinical trials.

Acknowledgments

This study was supported by grants from the National Natural Science Foundation of China (10501052), the Ministry of Science and Technology of China (2004BA719A01), and by the National Institute of Health (grants #1R01AI078933-01).

Author Disclosure Statement

No competing financial interests exist.

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