Human Papillomavirus Genital Infections among Men, China, 2007–2009

Zhonghu He¹, Ying Liu¹, Yuan Sun¹, Long Fu Xi, Ke Chen, Yiqiang Zhao, Lei Gao, Fangfang Liu, Yaqi Pan, Tao Ning, Lixin Zhang, Hong Cai, and Yang Ke

Author affiliations: Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Laboratory of Genetics, Peking University Cancer Hospital and Institute, Beijing, People’s Republic of China (Z. He, Y. Liu, Y. Sun, K. Chen, Y. Zhao, L. Gao, F. Liu, Y. Pan, T. Ning, H. Cai, Y. Ke); University of Washington, Seattle, Washington, USA (L.F. Xi); Anyang Cancer Hospital, Anyang, People’s Republic of China (L. Zhang)

Abstract

To determine prevalence of genital human papillomavirus (HPV) infection among men in rural China, we analyzed genital swab specimens. Among 2,236 male residents of rural Henan Province, HPV infection prevalence was 17.5%. The most common oncogenic and nononcogenic types were HPV-16 and HPV-3, respectively. Infection was associated with younger age and multiple sex partners.

Human papillomavirus (HPV) is an etiologic agent of cervical cancer. Among men, genital HPV infection plays a role in the development of anogenital cancer (1). Estimates of HPV infection prevalence among heterosexual men, mostly from North America and Europe, vary substantially (3.5%–45%) (1,2). In the People’s Republic of China, estimated HPV prevalence among women varies by geographic location (3), but no such estimate is available for men. Therefore, we conducted this cross-sectional study to determine the prevalence of genital HPV infection in a large population of men in a rural province of China and to evaluate relevant factors.

The Study

In 2007–2009, a population-based esophageal cancer cohort study was initiated in 9 villages in rural Anyang, Henan Province, China (4). This HPV investigation was added to the original cohort study in 6 of the 9 villages. Eligibility criteria were as follows: 1) male sex; 2) permanent residency in the target villages; 3) age 25–65 years; and 4) no history of cancer, cardiovascular disease, or mental disorder. Of 3,571 eligible men, 3,172 (89%) were enrolled. The main reason why the other 399, who were substantially younger, did not participate was loss of contact because they were employed outside Anyang.
Participants were interviewed, and exfoliated cells were collected from the penile shaft, glans penis, coronal sulcus, and scrotum by using saline-soaked swabs (5). The sampling procedure was identical for circumcised and uncircumcised men. To assess the adequacy of the specimens, we tested each specimen by PCR for the β-globin gene. Positive specimens were subsequently tested for 13 oncogenic and 37 nononcogenic types of HPV by using PCR-based direct sequencing with a pair of SPF1/GP6+ primers (6). Samples with ambiguous HPV typing signals were subjected to further cloning and sequencing.
To evaluate the associations between exposure variables and the presence of HPV DNA, we used logistic regression analysis with stepwise backward elimination at p>0.1. To examine the association across the ordered categorical variables, we used a trend test.
Of 3,172 specimens tested, 2,236 were positive for β-globin and were included in the analysis (median participant age 42 years; interquartile range 35–52 years). We excluded from the study men who were older and reported less risky sexual behavior than those who were included (Technical Appendix

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Of the 40 HPV types we tested for, we detected 36, including 13 oncogenic types. Overall prevalence of HPV infection was 17.5% (95% CI 16%–19%). Oncogenic HPV was detected in 140 (6.3%; 95% CI 5.3%–7.3%) specimens, and nononcogenic HPV was detected in 251 (11%; 95% CI 9.9%–13%) specimens. Among 15 HPV-positive specimens that had ambiguous direct sequencing signals and were further cloned and resequenced for genotyping, 3 had a second type and minor types were ignored. Among these infections (Table 1), the most common oncogenic type detected was HPV-16 (17.4%), followed by HPV-18 (7.2%). The most common nononcogenic type was HPV-3 (16.4%), followed by HPV-57 (7.9%).
Prevalence of infection of any or nononcogenic HPV types decreased significantly with participant’s increasing age (Table 2). Risk for infection with any HPV type was associated with being unmarried, having had multiple sex partners, and having had oral and anal sex. When the outcome was stratified by oncogenicity of HPV type, the association remained statistically significant for having had multiple sex partners.