High burden of human papillomavirus infection among men in Guangzhou, South China: Implications for HPV vaccination strategies

References

• Dykens JA, Peterson CE, Holt HK, Harper DM. Gender neutral HPV vaccination programs: reconsidering policies to expand cancer prevention globally. Front Public Health. 2023;11:1067299. doi:10.3389/fpubh.2023.1067299.
   PubMed Web of Science ®Google Scholar
• Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–9. doi:10.3322/caac.21660.
   PubMed Web of Science ®Google Scholar
• Crosbie EJ, Einstein MH, Franceschi S, Kitchener HC. Human papillomavirus and cervical cancer. Lancet. 2013;382(9895):889–899. doi:10.1016/S0140-6736(13)60022-7.
   PubMed Web of Science ®Google Scholar
• Rahangdale L, Mungo C, O’Connor S, Chibwesha CJ, Brewer NT. Human papillomavirus vaccination and cervical cancer risk. BMJ. 2022;379:e070115. doi:10.1136/bmj-2022-070115.
   PubMedGoogle Scholar
• Partridge JM, Koutsky LA. Genital human papillomavirus infection in men. Lancet Infect Dis. 2006;6(1):21–31. doi:10.1016/S1473-3099(05)70323-6.
   PubMed Web of Science ®Google Scholar
• Bruni L, Albero G, Rowley J, Alemany L, Arbyn M, Giuliano AR, Markowitz LE, Broutet N, Taylor M. Global and regional estimates of genital human papillomavirus prevalence among men: a systematic review and meta-analysis. Lancet Glob Health. 2023;11:1345–1362. doi:10.1016/S2214-109X(23)00305-4.
   Web of Science ®Google Scholar
• Chaturvedi AK, Graubard BI, Pickard RK, Xiao W, Gillison ML. High-risk oral human papillomavirus load in the US population, national health and nutrition examination survey 2009–2010. J Infect Dis. 2014;210:441–447. doi:10.1093/infdis/jiu116.
   PubMed Web of Science ®Google Scholar
• Buttmann N, Nielsen A, Munk C, Liaw KL, Kjaer SK. Sexual risk taking behaviour: prevalence and associated factors. A population-based study of 22,000 Danish men. BMC Public Health. 2011;11:764. doi:10.1186/1471-2458-11-764.
   PubMed Web of Science ®Google Scholar
• Centers for Disease Control and Prevention (CDC). FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the advisory committee on immunization practices (ACIP). Morb Mortal Wkly Rep. 2010;59:630–632.
   PubMedGoogle Scholar
• Bruni L, Saura-Lazaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, Afsar OZ, LaMontagne DS, Mosina L, Contreras M, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019. Prev Med. 2021;144:106399. doi:10.1016/j.ypmed.2020.106399.
   PubMed Web of Science ®Google Scholar
• Wei LH, Su YY, Hu YM, Li RC, Chen W, Pan QJ, Zhang X, Zhao F-H, Zhao Y-Q, Li Q, et al. Age distribution of human papillomavirus infection and neutralizing antibodies in healthy Chinese women aged 18–45 years enrolled in a clinical trial. Clin Microbiol Infect. 2020;26:1069–1075. doi:10.1016/j.cmi.2019.12.010.
   PubMed Web of Science ®Google Scholar
• Zhu J, Ge Z, Xia J, Liu Q, Ran Q, Yang Y. Status quo and problem analysis of cervical cancer screening program in China: based on RE-AIM framework. Front Public Health. 2022;10:987787. doi:10.3389/fpubh.2022.987787.
   PubMed Web of Science ®Google Scholar
• Wang S, Han B, Wan Y, Liu J, Zhao T, Liu H, Cui F. Do male university students know enough about human papillomavirus (HPV) to make informed decisions about vaccination? Med Sci Monit. 2020;26:e924840. doi:10.12659/MSM.924840.
   PubMed Web of Science ®Google Scholar
• Dai Z, Si M, Su X, Wang W, Zhang X, Gu X, Ma L, Li J, Zhang S, Ren Z, et al. Willingness to human papillomavirus (HPV) vaccination and influencing factors among male and female university students in China. J Med Virol. 2022;94(6):2776–2786. doi:10.1002/jmv.27478.
   PubMed Web of Science ®Google Scholar
• Yang X, Li Y, Tang Y, Li Z, Wang S, Luo X, He T, Yin A, Luo M. Cervical HPV infection in Guangzhou, China: an epidemiological study of 198,111 women from 2015 to 2021. Emerg Microbes Infect. 2023;12:12. doi:10.1080/22221751.2023.2176009.
   Web of Science ®Google Scholar
• Zou Z, Fairley CK, Ong JJ, Hocking J, Canfell K, Ma X, Chow EPF, Xu X, Zhang L, Zhuang G, et al. Domestic HPV vaccine price and economic returns for cervical cancer prevention in China: a cost-effectiveness analysis. Lancet Glob Health. 2020;8:1335–1344. doi:10.1016/S2214-109X(20)30277-1.
   Web of Science ®Google Scholar
• Giuliano AR, Palefsky JM, Goldstone S, Moreira ED Jr., Penny ME, Aranda C, Vardas E, Moi H, Jessen H, Hillman R, et al. Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. N Engl J Med. 2011;364(5):401–411. doi:10.1056/NEJMoa0909537.
   PubMed Web of Science ®Google Scholar
• Ma DM, Sun MX, Li XY, Li S, Nie XJ, Jin DH, Chen L-M. Distribution of high-risk human papillomavirus genotypes in male attendees at a clinic for sexually transmitted infections in Northern China. Eur Rev Med Pharmacol Sci. 2019;23:9714–9720. doi:10.26355/eurrev_201911_19533.
   PubMed Web of Science ®Google Scholar
• Yin WG, Yang M, Peng L, Liu YM, Cheng B, Xuan SX, Chen C, Tan F-J. Male papillomavirus infection and genotyping in the Qingyuan area. Virol J. 2020;17:155. doi:10.1186/s12985-020-01423-w.
   PubMed Web of Science ®Google Scholar
• Zhang C, Zhang C, Huang J, Shi W. The genotype of human papillomavirus and associated factors among high risk males in Shanghai, China: a molecular epidemiology study. Med Sci Monit. 2018;24:912–918. doi:10.12659/MSM.905789.
   PubMed Web of Science ®Google Scholar
• He Z, Liu Y, Sun Y, Xi LF, Chen K, Zhao Y, Gao L, Liu F, Pan Y, Ning T, et al. Human papillomavirus genital infections among men, China, 2007–2009. Emerg Infect Dis. 2013;19:992–995. doi:10.3201/eid1906.111597.
   PubMed Web of Science ®Google Scholar
• Wei F, Yin K, Wu X, Lan J, Huang S, Sheng W, Zhao J, Su Y, Wang Y, Li Y, et al. Human papillomavirus prevalence and associated factors in women and men in South China: a population-based study. Emerg Microbes Infect. 2016;5:1–8. doi:10.1038/emi.2016.118.
   PubMed Web of Science ®Google Scholar
• Smith JS, Gilbert PA, Melendy A, Rana RK, Pimenta JM. Age-specific prevalence of human papillomavirus infection in males: a global review. J Adolesc Health. 2011;48(6):540–552. doi:10.1016/j.jadohealth.2011.03.010.
   PubMed Web of Science ®Google Scholar
• Shi JF, Qiao YL, Smith JS, Dondog B, Bao YP, Dai M, Clifford GM, Franceschi S. Epidemiology and prevention of human papillomavirus and cervical cancer in China and Mongolia. Vaccine. 2008;26(Suppl 12):M53–M59. doi:10.1016/j.vaccine.2008.05.009.
   PubMedGoogle Scholar
• Pamnani SJ, Sudenga SL, Viscidi R, Rollison DE, Torres BN, Ingles DJ, Abrahamsen M, Villa LL, Lazcano-Ponce E, Salmeron J, et al. Impact of serum antibodies to HPV serotypes 6, 11, 16, and 18 to risks of subsequent genital HPV infections in men: the HIM study. Cancer Res. 7616;76(20):6066–6075. doi:10.1158/0008-5472.CAN-16-0224.
   PubMed Web of Science ®Google Scholar
• Goldstone S, Palefsky JM, Giuliano AR, Moreira ED Jr., Aranda C, Jessen H, Hillman RJ, Ferris DG, Coutlee F, Liaw K-L, et al. Prevalence of and risk factors for human papillomavirus (HPV) infection among HIV-seronegative men who have sex with men. J Infect Dis. 2011;203(1):66–74. doi:10.1093/infdis/jiq016.
   PubMed Web of Science ®Google Scholar
• Vardas E, Giuliano AR, Goldstone S, Palefsky JM, Moreira ED Jr., Penny ME, Aranda C, Jessen H, Moi H, Ferris DG, et al. External genital human papillomavirus prevalence and associated factors among heterosexual men on 5 continents. J Infect Dis. 2011;203(1):58–65. doi:10.1093/infdis/jiq015.
   PubMed Web of Science ®Google Scholar
• Vyas NS, Pierce Campbell CM, Mathew R, Abrahamsen M, Van der Kooi K, Jukic DM, Stoler MH, Villa LL, da Silva RC, Lazcano-Ponce E, et al. Role of histological findings and pathologic diagnosis for detection of human papillomavirus infection in men. J Med Virol. 2015;87(10):1777–1787. doi:10.1002/jmv.24238.
   PubMed Web of Science ®Google Scholar
• Liu X, Lin H, Chen X, Shen W, Ye X, Lin Y, Lin Z, Zhou S, Gao M, Ding Y, et al. Prevalence and genotypes of anal human papillomavirus infection among HIV-positive vs. HIV-negative men in Taizhou, China. Epidemiol Infect. 2019;147:e117. doi:10.1017/S0950268818003205.
   PubMed Web of Science ®Google Scholar
• Lorenzon L, Terrenato I, Dona MG, Ronchetti L, Rollo F, Marandino F, Carosi M, Diodoro MG, Sentinelli S, Visca P, et al. Prevalence of HPV infection among clinically healthy Italian males and genotype concordance between stable sexual partners. J Clin Virol. 2014;60(3):264–269. doi:10.1016/j.jcv.2014.04.003.
   PubMed Web of Science ®Google Scholar
• Wendland EM, Villa LL, Unger ER, Domingues CM, Benzaken AS, Group PO-BS. Prevalence of HPV infection among sexually active adolescents and young adults in Brazil: the POP-Brazil study. Sci Rep. 2020;10:4920. doi:10.1038/s41598-020-61582-2.
   PubMed Web of Science ®Google Scholar
• Han JJ, Beltran TH, Song JW, Klaric J, Choi YS. Prevalence of genital human papillomavirus infection and human papillomavirus vaccination rates among US adult men: national health and nutrition examination survey (NHANES) 2013–2014. JAMA Oncol. 2017;3(6):810–816. doi:10.1001/jamaoncol.2016.6192.
   PubMed Web of Science ®Google Scholar
• Chan PK, Cheung TH, Tam AO, Lo KW, Yim SF, Yu MM, To K-F, Wong Y-F, Cheung JLK, Chan DPC, et al. Biases in human papillomavirus genotype prevalence assessment associated with commonly used consensus primers. Int J Cancer. 2006;118(1):243–245. doi:10.1002/ijc.21299.
   PubMed Web of Science ®Google Scholar
• Clifford GM, Vaccarella S, Franceschi S, Tenet V, Umulisa MC, Tshomo U, Dondog B, Vorsters A, Tommasino M, Heideman DAM, et al. Comparison of two widely used human papillomavirus detection and genotyping methods, GP5+/6±Based PCR followed by reverse line blot hybridization and multiplex type-specific E7-based PCR. J Clin Microbiol. 2016;54:2031–2038. doi:10.1128/JCM.00618-16.
   PubMed Web of Science ®Google Scholar
• Clifford GM, Rana RK, Franceschi S, Smith JS, Gough G, Pimenta JM. Human papillomavirus genotype distribution in low-grade cervical lesions: comparison by geographic region and with cervical cancer. Cancer Epidemiol Biomarkers Prev. 2005;14(5):1157–1164. doi:10.1158/1055-9965.EPI-04-0812.
   PubMed Web of Science ®Google Scholar
• de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, Bosch FX. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007;7:453–459. doi:10.1016/S1473-3099(07)70158-5.
   PubMed Web of Science ®Google Scholar
• Ingles DJ, Lin HY, Fulp WJ, Sudenga SL, Lu B, Schabath MB, Papenfuss MR, Abrahamsen ME, Salmeron J, Villa LL, et al. An analysis of HPV infection incidence and clearance by genotype and age in men: the HPV infection in men (HIM) study. Papillomavirus Res. 2015;1:126–135. doi:10.1016/j.pvr.2015.09.001.
   PubMedGoogle Scholar
• Cao X, Wei R, Zhang X, Zhou J, Lou J, Cui Y. Impact of human papillomavirus infection in semen on sperm progressive motility in infertile men: a systematic review and meta-analysis. Reprod Biol Endocrinol. 2020;18(1):38. doi:10.1186/s12958-020-00604-0.
   PubMed Web of Science ®Google Scholar
• Foresta C, Garolla A, Zuccarello D, Pizzol D, Moretti A, Barzon L, Palù G. Human papillomavirus found in sperm head of young adult males affects the progressive motility. Fertil Steril. 2010;93:802–806. doi:10.1016/j.fertnstert.2008.10.050.
   PubMed Web of Science ®Google Scholar
• Korhonen S, Hokynar K, Eriksson T, Natunen K, Paavonen J, Lehtinen M, Puolakkainen M. The prevalence of HSV, HHV-6, HPV and Mycoplasma genitalium in Chlamydia trachomatis positive and Chlamydia trachomatis negative urogenital samples among young women in Finland. Pathogens. 2019;8:276. doi:10.3390/pathogens8040276.
   PubMed Web of Science ®Google Scholar
• Seraceni S, Campisciano G, Contini C, Comar M. HPV genotypes distribution in Chlamydia trachomatis co-infection in a large cohort of women from north-east Italy. J Med Microbiol. 2016;65(5):406–413. doi:10.1099/jmm.0.000245.
   PubMedGoogle Scholar
• Luna AJ, Sterk RT, Griego-Fisher AM, Chung JY, Berggren KL, Bondu V, Barraza-Flores P, Cowan AT, Gan GN, Yilmaz E, et al. MEK/ERK signaling is a critical regulator of high-risk human papillomavirus oncogene expression revealing therapeutic targets for HPV-induced tumors. PLoS Pathog. 2021;17(1):e1009216. doi:10.1371/journal.ppat.1009216.
   PubMed Web of Science ®Google Scholar
• Challagundla N, Chrisophe-Bourdon J, Agrawal-Rajput R. Chlamydia trachomatis infection co-operatively enhances HPV E6-E7 oncogenes mediated tumorigenesis and immunosuppression. Microb Pathog. 2023;175:105929. doi:10.1016/j.micpath.2022.105929.
   PubMed Web of Science ®Google Scholar