Sex differences in the incidence and clearance of anal human papillomavirus infection among heterosexual men and women in Liuzhou, China: An observational cohort 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, Fujian, 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, Fujian, China
Search for more papers by this authorXingmei Yao
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, Fujian, China
Search for more papers by this authorXuelian Cui
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorLihong Bian
Department of Gynecology, The 307th Hospital of Chinese People's Liberation Army, Beijing, China
Search for more papers by this authorKai Yin
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorXiaojuan Yu
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, Fujian, China
Search for more papers by this authorChunlan Zhuang
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, Fujian, China
Search for more papers by this authorZhaofeng Bi
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, 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, Fujian, China
Search for more papers by this authorMingqiang Li
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorTing 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, 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, Fujian, China
Search for more papers by this authorCorresponding Author
Jun 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, Fujian, China
Correspondence to: Jun Zhang, School of Public Health, Xiamen University, Xiamen 361102, Fujian, China, Tel.: +86-592-2184110, Fax: +86-592-2181258, E-mail: [email protected]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, Fujian, 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, Fujian, China
Search for more papers by this authorXingmei Yao
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, Fujian, China
Search for more papers by this authorXuelian Cui
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorLihong Bian
Department of Gynecology, The 307th Hospital of Chinese People's Liberation Army, Beijing, China
Search for more papers by this authorKai Yin
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorXiaojuan Yu
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, Fujian, China
Search for more papers by this authorChunlan Zhuang
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, Fujian, China
Search for more papers by this authorZhaofeng Bi
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, 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, Fujian, China
Search for more papers by this authorMingqiang Li
Liuzhou Center for Disease Control and Prevention, Liuzhou, Guangxi, China
Search for more papers by this authorTing 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, 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, Fujian, China
Search for more papers by this authorCorresponding Author
Jun 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, Fujian, China
Correspondence to: Jun Zhang, School of Public Health, Xiamen University, Xiamen 361102, Fujian, China, Tel.: +86-592-2184110, Fax: +86-592-2181258, E-mail: [email protected]Search for more papers by this authorAbstract
Anal cancer is primarily caused by human papillomavirus (HPV) infection in both men and women. However, little is known about the sex differences in the natural history of anal HPV infection in a heterosexual population. From May 2014 to March 2016, perianal/anal canal (PA) swab samples were collected semiannually from 2,302 heterosexual men and 2,371 heterosexual women aged 18–55 years old in Liuzhou, China. The specimens were genotyped for HPV DNA by polymerase chain reaction. The incidence rate ratio (IRR) and clearance rate ratio (CRR) were used to analyze the sex differences of incidence and clearance by Poisson regression, respectively. The incidences of PA oncogenic HPV in men and women were 3.4 per 1,000 person-months and 8.6 per 1,000 person-months, respectively, with an IRR of 0.39 (95% confidence interval (CI), 0.29–0.54 for men versus women) (p < 0.0001). The CRR of PA oncogenic HPV infection for men versus women was 1.54 (95% CI, 1.17–2.03) (p = 0.0022). At 12 months, 44% (20/45) of HPV 16/18 infections among women remained positive, whereas no (0/7) infections persisted among men (p = 0.0350). Both the higher incidence and slower clearance of anal carcinogenic HPV infection among women may lead to a higher burden of anal cancer among women than among men in a heterosexual population.
Abstract
What's new?
While human papillomavirus (HPV) infection is a major cause of anal cancer in men and women, anal cancer incidence differs between the sexes. The dynamics of anal HPV infection in the general heterosexual population, however, are not well understood. Here, women were found to have a higher risk of acquiring anal carcinogenic HPV infection than men based on follow-up and analysis of perianal/anal canal specimens for approximately 4,000 heterosexual Chinese men and women. Women were also found to have a lower likelihood of clearing anal HPV infection. These differences potentially contribute to increased anal cancer burden in women.
References
- 1Bruni L, Albero G, Serrano B, et al. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human papillomavirus and related diseases in the world. Summary Report 22 January 2019. (accessed 18 March 2019)
- 2de 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.
- 3Chiao EY, Krown SE, Stier EA, et al. A population-based analysis of temporal trends in the incidence of squamous anal canal cancer in relation to the HIV epidemic. J Acquired Immune Defic Syndr 2005; 40: 451–5.
- 4Parkin DM, Bray F. Chapter 2: the burden of HPV-related cancers. Vaccine 2006; 24: S11–25.
- 5Brewster DH, Bhatti LA. Increasing incidence of squamous cell carcinoma of the anus in Scotland, 1975-2002. Br J Cancer 2006; 95: 87–90.
- 6de Pokomandy A, Rouleau D, Ghattas G, et al. Prevalence, clearance, and incidence of anal human papillomavirus infection in HIV-infected men: the HIPVIRG cohort study. J Infect Dis 2009; 199: 965–73.
- 7Darwich L, Canadas MP, Videla S, et al. Prevalence, clearance, and incidence of human papillomavirus type-specific infection at the anal and penile site of HIV-infected men. Sex Transm Dis 2013; 40: 611–8.
- 8Videla S, Darwich L, Canadas MP, et al. Natural history of human papillomavirus infections involving anal, penile, and oral sites among HIV-positive men. Sex Transm Dis 2013; 40: 3–10.
- 9Machalek DA, Grulich AE, Jin F, et al. The epidemiology and natural history of anal human papillomavirus infection in men who have sex with men. Sex Health 2012; 9: 527–37.
- 10Phanuphak N, Teeratakulpisarn N, Pankam T, et al. Anal human papillomavirus infection among Thai men who have sex with men with and without HIV infection: prevalence, incidence, and persistence. J Acquired Immune Defic Syndr 2013; 63: 472–9.
- 11Hernandez AL, Efird JT, Holly EA, et al. Incidence of and risk factors for type-specific anal human papillomavirus infection among HIV-positive MSM. AIDS 2014; 28: 1341–9.
- 12Goodman MT, Shvetsov YB, McDuffie K, et al. Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV cohort study. J Infect Dis 2008; 197: 957–66.
- 13Beachler DC, D'Souza G, Sugar EA, et al. Natural history of anal vs oral HPV infection in HIV-infected men and women. J Infect Dis 2013; 208: 330–9.
- 14Moscicki AB, Ma Y, Farhat S, et al. Natural history of anal human papillomavirus infection in heterosexual women and risks associated with persistence. Clin Infect Dis 2014; 58: 804–11.
- 15Wei F, Yin K, Wu X, et al. Human papillomavirus prevalence and associated factors in women and men in south China: a population-based study. Emerging Microbes Infect 2016; 5: e119.
- 16Wei F, Sheng W, Wu X, et al. Incidence of anogenital warts in Liuzhou, south China: a comparison of data from a prospective study and from the national surveillance system. Emerging Microbes Infect 2017; 6: e113.
- 17Wei F, Li M, Wu X, et al. The prevalence and concordance of human papillomavirus infection in different anogenital sites among men and women in Liuzhou, China: a population-based study. Int J Cancer 2018; 142: 1244–51.
- 18Bouvard V, Baan R, Straif K, et al. A review of human carcinogens--part B: biological agents. Lancet Oncol 2009; 10: 321–2.
- 19Giuliano AR, Lee JH, Fulp W, et al. Incidence and clearance of genital human papillomavirus infection in men (HIM): a cohort study. Lancet 2011; 377: 932–40.
- 20Wei LJ, Lin DY, Weissfeld L. Regression analysis of multivariate incomplete failure time data by modeling marginal distributions. J Am Stat Assoc 1989; 84: 1065–73.
- 21Schiffman M, Doorbar J, Wentzensen N, et al. Carcinogenic human papillomavirus infection. Nat Rev Dis Primers 2016; 2: 16086.
- 22Lin C, Franceschi S, Clifford GM. Human papillomavirus types from infection to cancer in the anus, according to sex and HIV status: a systematic review and meta-analysis. Lancet Infect Dis 2018; 18: 198–206.
- 23Zhang YJ, Feng XX, Fan YG, et al. HIV transmission and related risk factors among serodiscordant couples in Liuzhou, China. J Med Virol 2015; 87: 553–6.
- 24 Centers of Diseases Control and Prevention. HPV-associated anal cancer rates by race and ethnicity. Available at https://www.cdc.gov/cancer/hpv/statistics/anal.htm (accessed 18 March 2019).
- 25 Cancer Reaserch UK. Anal cancer incidence by sex and UK country. Available at https://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/anal-cancer/incidence#heading-Zero (accessed 18 March 2019).
- 26Daling JR, Weiss NS, Hislop TG, et al. Sexual practices, sexually transmitted diseases, and the incidence of anal cancer. N Engl J Med 1987; 317: 973–7.
- 27Daling JR, Weiss NS, Klopfenstein LL, et al. Correlates of homosexual behavior and the incidence of anal cancer. JAMA 1982; 247: 1988–90.
- 28Bower M, Powles T, Newsom-Davis T, et al. HIV-associated anal cancer: has highly active antiretroviral therapy reduced the incidence or improved the outcome? J Acquired Immune Defic Syndr 2004; 37: 1563–5.
- 29Nyitray AG, Carvalho da Silva RJ, Baggio ML, et al. Six-month incidence, persistence, and factors associated with persistence of anal human papillomavirus in men: the HPV in men study. J Infect Dis 2011; 204: 1711–22.
- 30Glick SN, Feng Q, Popov V, et al. High rates of incident and prevalent anal human papillomavirus infection among young men who have sex with men. J Infect Dis 2014; 209: 369–76.
- 31Dona MG, Vescio MF, Latini A, et al. Anal human papillomavirus in HIV-uninfected men who have sex with men: incidence and clearance rates, duration of infection, and risk factors. Clin Microbiol Infect 2016; 22: e1–7.
- 32Mullins TL, Wilson CM, Rudy BJ, et al. Incident anal human papillomavirus and human papillomavirus-related sequelae in HIV-infected versus HIV-uninfected adolescents in the United States. Sex Transm Dis 2013; 40: 715–20.
- 33Kojic EM, Conley L, Bush T, et al. Prevalence and incidence of anal and cervical high-risk human papillomavirus (HPV) types covered by current HPV vaccines among HIV-infected women in the SUN study. J Infect Dis 2018; 217: 1544–52.
Citing Literature
