The prevalence and concordance of human papillomavirus infection in different anogenital sites among men and women in Liuzhou, China: A population-based study
Feixue Wei
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorMingqiang Li
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorXin Wu
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorKai Yin
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorJian Lan
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorWei Sheng
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorMeng Guo
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorShoujie Huang
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorYing Wang
China National Center for Biotechnology Development, Beijing, 100039 China
Search for more papers by this authorYanping Li
Guangxi Center for Disease Control and Prevention, Nanning, 530028 Guangxi, China
Search for more papers by this authorRongcheng Li
Guangxi Center for Disease Control and Prevention, Nanning, 530028 Guangxi, China
Search for more papers by this authorYingying Su
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorCorresponding Author
Ting Wu
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Correspondence to: Ting Wu, Xiamen University, Xiamen 361102, Fujian, China, E-mail: [email protected]; Tel: +86 5922880621Search for more papers by this authorJun Zhang
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorNingshao Xia
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorFeixue Wei
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorMingqiang Li
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorXin Wu
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorKai Yin
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorJian Lan
Liuzhou Center for Disease Control and Prevention, Liuzhou, 545007 Guangxi, China
Search for more papers by this authorWei Sheng
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorMeng Guo
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorShoujie Huang
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorYing Wang
China National Center for Biotechnology Development, Beijing, 100039 China
Search for more papers by this authorYanping Li
Guangxi Center for Disease Control and Prevention, Nanning, 530028 Guangxi, China
Search for more papers by this authorRongcheng Li
Guangxi Center for Disease Control and Prevention, Nanning, 530028 Guangxi, China
Search for more papers by this authorYingying Su
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorCorresponding Author
Ting Wu
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Correspondence to: Ting Wu, Xiamen University, Xiamen 361102, Fujian, China, E-mail: [email protected]; Tel: +86 5922880621Search for more papers by this authorJun Zhang
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorNingshao Xia
State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, Strait Collaborative Innovation Center of Biomedicine and Pharmaceutics, School of Public Health, Xiamen University, Xiamen, 361102 Fujian, China
Search for more papers by this authorAbstract
Human papillomavirus (HPV) infection is the pathogenesis of anogenital cancers and genital warts in both men and women, whereas there is a scarcity of large studies focused on HPV prevalence in different anogenital sites of both sexes in the same population. From May to July 2014, 2,309 men and 2,378 women aged 18–55 were enrolled from communities in Liuzhou, China. Penis/glans penis/coronary sulcus (PGC) and perianal/anal canal (PA) specimens of men, and vaginal (VA), vulvar (VU) and PA specimens of women, were collected and genotyped for HPV. The prevalence of any HPV tested in PGC and PA samples from men and VA, VU and PA samples from women was 10.8%, 3.8%, 14.2%, 13.3% and 8.4%, respectively. The concordance of VA and VU was highest (kappa = 0.74), followed by VU and PA (0.44), VA and PA (0.38) and PGC and PA (0.14). Besides sex behavior, ever having used a towel supplied by a hotel was a risk factor for both external genital and PA HPV infection. Our data indicated that women were more of a major reservoir for oncogenic HPV infection of both genital sites and PA sites than was men. In both sexes, the genital sites were more likely than PA sites to harbor HPV infection. The concordance rates of HPV infection between genital sites and PA infection were poor.
Abstract
What's new?
Comparing the prevalence of human papilloma virus (HPV) infection in different anogenital sites is difficult because of inconsistencies in the methods used in different studies. Here, the authors systematically analyzed HPV retrieved from different sites in more than 4,000 men and women in communities in South-Western China with a high incidence of sexually transmitted diseases. In both sexes, genital sites were more likely to harbor HPV than was the perianal site, and the HPV type concordance was poor between genital and perianal sites. Interestingly, usage of hotel towels was a risk factor for external genital and perianal, but not vaginal HPV infection, underscoring the importance of personal hygiene and direct contact in acquiring the infection.
References
- 1 Bruni L, Barrionuevo-Rosas L, Albero G, et al. ICO Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in the World. Summary Report 15 December, 2016.
- 2 Zhao FH, Lewkowitz AK, Hu SY, et al. Prevalence of human papillomavirus and cervical intraepithelial neoplasia in China: a pooled analysis of 17 population-based studies. Int J Cancer 2012; 131: 2929–38.
- 3 De Vuyst H, Clifford G, Li N, et al. HPV infection in Europe. Eur J Cancer 2009; 45: 2632–9.
- 4 de Sanjose S, Diaz M, Castellsague X, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis 2007; 7: 453–9.
- 5 Smith JS, Melendy A, Rana RK, et al. Age-specific prevalence of infection with human papillomavirus in females: a global review. J Adolesc Health 2008; 43:S5-S25, S25.e1-41.
- 6 Herrero R, Gonzalez P, Markowitz LE. Present status of human papillomavirus vaccine development and implementation. Lancet Oncol 2015; 16: e206–e16.
- 7 Weaver BA, Feng Q, Holmes KK, et al. Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis 2004; 189: 677–85.
- 8 Nielson CM, Flores R, Harris RB, et al. Human papillomavirus prevalence and type distribution in male anogenital sites and semen. Cancer Epidemiol Biomarkers Prev 2007; 16: 1107–14.
- 9 Vardas E, Giuliano AR, Goldstone S, et al. External genital human papillomavirus prevalence and associated factors among heterosexual men on 5 continents. J Infect Dis 2011; 203: 58–65.
- 10 Hernandez BY, McDuffie K, Zhu X, et al. Anal human papillomavirus infection in women and its relationship with cervical infection. Cancer Epidemiol Biomarkers Prev 2005; 14: 2550–6.
- 11 Crawford R, Grignon AL, Kitson S, et al. High prevalence of HPV in non-cervical sites of women with abnormal cervical cytology. BMC Cancer 2011; 11: 473.
- 12 Twu NF, Yen MS, Lau HY, et al. Type-specific human papillomavirus DNA testing with the genotyping array: a comparison of cervical and vaginal sampling. Eur J Obstet Gynecol Reprod Biol 2011; 156: 96–100.
- 13 Goncalves MA, Randi G, Arslan A, et al. HPV type infection in different anogenital sites among HIV-positive Brazilian women. Infect Agents Cancer 2008; 3: 5.
- 14 Nyitray AG, Smith D, Villa L, et al. Prevalence of and risk factors for anal human papillomavirus infection in men who have sex with women: a cross-national study. J Infect Dis 2010; 201: 1498–508.
- 15 Ferreccio C, Corvalan A, Margozzini P, et al. Baseline assessment of prevalence and geographical distribution of HPV types in Chile using self-collected vaginal samples. BMC Public Health 2008; 8: 78.
- 16 Lazcano-Ponce E, Lorincz AT, Cruz-Valdez A, et al. Self-collection of vaginal specimens for human papillomavirus testing in cervical cancer prevention (MARCH): a community-based randomised controlled trial. Lancet 2011; 378: 1868–73.
- 17 Patel H, Wagner M, Singhal P, et al. Systematic review of the incidence and prevalence of genital warts. BMC Infect Dis 2013; 13: 39.
- 18 He Z, Liu Y, Sun Y, et al. Human papillomavirus genital infections among men, China, 2007–2009. Emerging Infect Dis 2013; 19: 992–5.
- 19 Wei F, Yin K, Wu X, et al. Human papillomavirus prevalence and associated factors in women and men in south China: a population-based study. Emerg Microbes Infect 2016; 5:e119.
- 20 IARC Working Group. Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 2012; 100: 255–313. http://monographs.iarc.fr/ENG/Monographs/vol100B/mono100B-11.pdf>
- 21 Giuliano AR, Nyitray AG, Kreimer AR, et al. EUROGIN 2014 roadmap: differences in human papillomavirus infection natural history, transmission and human papillomavirus-related cancer incidence by gender and anatomic site of infection. Int J Cancer 2015; 136: 2752–60.
- 22 de Martel C, Plummer M, Vignat J, et al. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer 2017; 141: 664–70.
- 23 Zhao FH, Zhu FC, Chen W, et al. Baseline prevalence and type distribution of human papillomavirus in healthy Chinese women aged 18–25 years enrolled in a clinical trial. Int J Cancer 2014; 135: 2604–11.
- 24 The FUTURE I/II Study Group,
Dillner J,
Kjaer SK, et al. Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial. BMJ 2010; 341:c3493.
10.1136/bmj.c3493 Google Scholar
- 25 Bruni L, Barrionuevo-Rosas L, Albero G, et al. ICO Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in China. Summary Report 15 December, 2016.
- 26 Confortini M, Carozzi F, Zappa M, et al. Human papillomavirus infection and risk factors in a cohort of Tuscan women aged 18–24: results at recruitment. BMC Infect Dis 2010; 10: 157.
- 27 Shi R, Devarakonda S, Liu L, et al. Factors associated with genital human papillomavirus infection among adult females in the United States, NHANES 2007–2010. BMC Res Notes 2014; 7: 544.
- 28 Smith JS, Backes DM, Hudgens MG, et al. Prevalence and risk factors of human papillomavirus infection by penile site in uncircumcised Kenyan men. Int J Cancer 2010; 126: 572–7.