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Anal Human Papillomavirus Infection Among HIV-Infected and Uninfected Men Who Have Sex With Men in Beijing, China

Hu, Yifei MD, MSc*; Qian, Han-Zhu MD, PhD†,‡; Sun, Jiangping MD, PhD*; Gao, Lei PhD§; Yin, Lu MD, PhD; Li, Xiangwei MD§; Xiao, Dong BA; Li, Dongliang MD; Sun, Xiaoyun MD#; Ruan, Yuhua PhD*; Milam, Douglas F. MD**; Pan, Stephen W.††; Shao, Yiming MD, PhD*; Vermund, Sten H. MD, PhD†,‡,‡‡

JAIDS Journal of Acquired Immune Deficiency Syndromes: September 1st, 2013 - Volume 64 - Issue 1 - p 103–114
doi: 10.1097/QAI.0b013e31829b6298
Epidemiology and Prevention

Background: In light of China’s unique ethnic and sociocultural context, and a marked rise in HIV prevalence among MSM, it is important to determine prevalence, genotypes and predictors of anal human papillomavirus (HPV) among HIV-infected and uninfected men who have sex with men (MSM) in Beijing, China.

Methods: In 2010-2011, we recruited MSM (age range 18-61; median 28 years) through peer volunteers, and collected demographic/behavioral information via interviewer-administrated questionnaires. Trained health workers collected anal swabs for HPV genotyping by PCR and blood samples for HIV/syphilis serologies.

Results: We obtained anal specimens from 212 HIV-infected and 459 HIV-uninfected participants. Among HIV-infected MSM, 82.1% were HPV-infected vs. 57.5% in HIV-uninfected (p<0.01). HIV-infected men had the greatest likelihood of multiple types: 17.9% uninfected; 36.3% with one type; 36.8% with 2-3; 9.0% with ≥4. Oncogenic HPV prevalence was higher among HIV- infected (61.3%) than uninfected participants (39.7%; p<0.01). HIV-uninfected MSM reporting always using condoms during insertive anal intercourse (past 6 months) were less likely to be HPV-infected (OR=0.49, 95%CI: 0.31-0.77). Among HIV-uninfected MSM, HPV infection was associated with unprotected receptive anal intercourse (past 6 months; OR=1.92, 95%CI: 1.19-3.11) and being forced to have sex (previous year; OR=3.32, 95%CI: 1.10-10.0). Multivariable logistic analysis among HIV infected MSM suggested that unprotected oral intercourse (past 6 months) was associated with HPV (adjusted OR=2.12, 95%CI: 1.00-4.48). Syphilis occurred in 55.8% of HIV-infected/HPV-infected, 50.0% of HIV-infected/HPV-uninfected, 19.6% of HIV-uninfected/HPV-infected, and 13.0% of HIV-uninfected/HPV-uninfected MSM.

Conclusions: HPV anal infections were more common among HIV-infected than uninfected MSM in China, including oncogenic and multiple types. Unprotected oral and receptive anal sex were was independently associated with HPV infection. Promotion of safer sex and HPV vaccination is strongly recommended among MSM.

*State Key Laboratory for Infectious Disease Prevention and Control and National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention (China CDC), Beijing, China;

Vanderbilt Institute for Global Health, Vanderbilt University School of Medicine, Nashville, TN;

Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN;

§MoH Key Laboratory of Systems Biology of Pathogens, Institute of Pathogen Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China;

Chaoyang Chinese AIDS Volunteer Group, Beijing, China;

Chaoyang Center for Disease Control and Prevention, Beijing, China;

#Xicheng District Center for Disease Prevention and Control, Beijing, China;

**Department of Pediatrics, Vanderbilt University School of Medicine, Nashville, TN;

††University of British Columbia, School of Population and Public Health, Vancouver, Canada; and

‡‡Vanderbilt University School of Medicine, Nashville, TN.

Correspondence to: Dr. Jiangping Sun, 155 Changbai Road, Changping District, Beijing 102206, China. Tel/Fax: +86-10-58900907 (e-mail: jpsun@chinaaids.cn_ or Dr. Yuhua Ruan (e-mail:

Supported by National Natural Science Foundation of China Grant 81273188, the Ministry of Science and Technology of China Grant 2012ZX10001-002, Chinese State Key Laboratory for Infectious Disease Development Grant 2012SKLID103, Vanderbilt Institute for Clinical and Translational Research Grants # UL1TR000445 and KL2TR000446, the Fogarty International Clinical Research Scholars-Fellows Support Center at Vanderbilt Grant #R24TW007988, and doctoral fellowship support from the University of British Columbia.

The authors have no funding or conflicts of interest to disclose.

Y.H. and H.-Z.Q. contributed equally to the paper. J.S., Y.S., S.H.V., and Y.R. provided guidance on study implementation, data analysis, and manuscript writing; D.F.M. trained clinicians on specimen collection; L.G. and X.L. performed laboratory testing; D.X., D.L., and X.S. conducted questionnaire interviews; L.Y. and Y.H. performed data analysis; Y.H. drafted the first version of the manuscript; H.-Z.Q., Y.R., D.F.M., S.W.P., and S.H.V. contributed to the revision of the manuscript; all authors read and approved the final version of the manuscript.

The study protocol was approved by Institutional Review Boards of Vanderbilt University and the National Center for HIV/AIDS Control and Prevention.

Received February 13, 2013

Accepted May 10, 2013

© 2013 by Lippincott Williams & Wilkins