The Epidemiological surveillance of Human Papillomavirus (HPV) genotypes in oral and genital tracts and the impact of HPV vaccination on male university students from Rio de Janeiro state, Brazil

Authors

  • Kátia Cristina da Silva Universidade Federal Fluminense, Biomedical Institute, Department of Microbiology and Parasitology, Virology Research Center – Niterói (RJ), Brazil. https://orcid.org/0000-0002-6404-2360
  • Willker Menezes da Rocha Universidade Federal Fluminense, Biomedical Institute, Department of Microbiology and Parasitology, Virology Research Center – Niterói (RJ), Brazil. https://orcid.org/0000-0002-3890-2902
  • Milena Siqueira Pereira Universidade Federal Fluminense, Biomedical Institute, Department of Microbiology and Parasitology, Virology Research Center – Niterói (RJ), Brazil. https://orcid.org/0000-0001-5940-9642
  • Hugo Boechat Andrade Universidade Federal Fluminense, Biomedical Institute, Microbiology and Parasitology Department, Sexually Transmitted Diseases Sector – Niterói (RJ), Brazil. https://orcid.org/0000-0001-6781-6125
  • Tegnus Depes de Gouvea Universidade Federal Fluminense, Biomedical Institute, Microbiology and Parasitology Department, Sexually Transmitted Diseases Sector – Niterói (RJ), Brazil. https://orcid.org/0000-0003-4978-0450
  • Charbell Miguel Haddad Kury Secretaria de Saúde do Município de Campos dos Goytacazes – Campos dos Goytacazes (RJ), Brazil. https://orcid.org/0000-0002-7568-7367
  • Mauro Romero Leal Passos Universidade Federal Fluminense, Biomedical Institute, Microbiology and Parasitology Department, Sexually Transmitted Diseases Sector – Niterói (RJ), Brazil. https://orcid.org/0000-0002-6183-7985
  • Silvia Maria Baeta Cavalcanti Universidade Federal Fluminense, Biomedical Institute, Department of Microbiology and Parasitology, Virology Research Center – Niterói (RJ), Brazil. https://orcid.org/0000-0002-2994-7172

DOI:

https://doi.org/10.5327/DST-2177-8264-2023351392

Keywords:

HPV, Vaccination, Genital tract, Genotype

Abstract

Introduction: Human Papillomavirus (HPV) infections are of significant concern in men, given its potential impact on their health and the risk of transmission to partners. Understanding and addressing this infection in men is crucial to evaluate the effectiveness of vaccination in reducing HPV-related diseases. Objective: To assess the impact of HPV vaccination, potential genotype shifts, and adverse effects, through a prospective study conducted with male university students. Methods: The study involved 286 volunteers who were examined at Sexually Transmitted Disease Clinics at the Universidade Federal Fluminense in Niterói, Rio de Janeiro, Brazil. The HPV prevalence was evaluated using generic PCR, genotyped by DNA microarray and monitored adverse effects. Results: The findings of this study revealed the absence of moderate or severe adverse effects. Genetic shifts were observed, including the disappearance of oncogenic HPV types 16 and 18. Surprisingly, even after completing the full vaccine regimen, students still harbored HPV11 in the oral tract. Furthermore, persistent HPV 6 and 11 infections were identified in three students, who had pre-existing infections prior to vaccination, at the follow-up visit. Multivariate analysis uncovered independent associations, notably an increased risk of HPV infection in the oral tract among men who have sex with men. HPV prevalence rates remained low both before and after the vaccination scheme (T0: 14.7%, T1: 8.7%). Even after the full vaccination scheme, the prevalence remained similar at T2 (14.6%), with no statistically significant differences recorded. HPV11 emerged as the most prevalent type throughout the study, followed by HPV6. Vaccine genotypes were detected in a significant proportion of samples at T0 (85.4%), T1 (89.5%), and T2 (100%). Conclusion: Overall, this study suggests that vaccination may represent a promising approach to reducing HPV-related health risks. These findings shed light on the potential benefits and challenges of HPV vaccination, emphasizing the need for continued monitoring and vaccination efforts.

Downloads

Download data is not yet available.

References

Bruni L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, Bosch FX, de Sanjosé S. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in the World. Summary Report [Internet]. 2023 [cited on 2019 June 17]. Available at: https://www.hpvcentre.net/statistics/reports/XWX.pdf

Afonso LA, Carestiato FN, Ornellas AA, Ornellas P, Rocha WM, Cordeiro TI, et al. Human Papillomavirus, Epstein-Barr virus, and methylation status of p16ink4a in penile cancer. J Med Virol. 2017;89(10):1837-43. https://doi.org/10.1002/jmv.24833

Lieblong BJ, Montgomery BEE, Su LJ, Nakagawa M. Natural history of human papillomavirus and vaccinations in men: a literature review. Health Sci Rep. 2019;2(5):e118. https://doi.org/10.1002/hsr2.118

Wierzbicka M, Klussmann JP, San Giorgi MR, Wuerdemann N, Dikkers FG. Oral and laryngeal HPV infection: incidence, prevalence and risk factors, with special regard to concurrent infection in head, neck and genitals. Vaccine. 2021;39(17):2344-50. https://doi.org/10.1016/j.vaccine.2021.03.047

World Health Organization. Guide to introducing HPV vaccine into national immunization programmes [Internet]. [cited on 2023 Aug 07]. Available from: https://www.who.int/publications/i/item/9789241549769

Brasil. Ministério da Saúde. SIPNI – Sistema de Informações do Programa Nacional de Imunizações [Internet]. 2014 [cited on 2023 July 22]. Available from: http://sipni.datasus.gov.br/si-pni-web/faces/inicio.jsf

Muñoz N, Manalastas Jr R, Pitisuttithum P, Tresukosol D, Monsonego J, Ault K, et al. Safety, immunogenicity, and efficacy of quadrivalent human papillomavirus (types 6, 11, 16, 18) recombinant vaccine in women aged 24-45 years: a randomized, double-blind trial. Lancet. 2009;373(9679):1949-57. https://doi.org/10.1016/S0140-6736(09)60691-7

Hernández-Ávila M, Torres-Ibarra L, Stanley M, Salmerón J, Cruz-Valdez A, Muñoz N, et al. Evaluation of the immunogenicity of the quadrivalent HPV vaccine using 2 versus 3 doses at month 21: an epidemiological surveillance mechanism for alternate vaccination schemes. Hum Vaccin Immunother. 2016;12(1):30-8. https://doi.org/10.1080/21645515.2015.1058458

Bauer HM, Greer CE, Manos MM. Determination of genital HPV infection using consensus PCR. In: Herrington CS, McGee JOD, eds. Diagnostic molecular pathology: a practical approach. Oxford: Oxford University Press; 1992. p. 131-52.

Kury CMH, Guimaraes GR, Leandro CG, Fernandes LA, Silva PRT, Petraglia TC, et al. Associations of human papillomavirus (HPV) genotypes and related risk factors in a cohort of women living with HIV in a Brazilian countryside city. J Med Virol. 2022;94(6):2802-10. https://doi.org/10.1002/jmv.27582

ICO/IARC Information Centre on HPV and Cancer. Brazil: human papillomavirus and related cancers, fact sheet 2023 [Internet]. 2023 [cited on 2023 Nov 17]. Available from: https://hpvcentre.net/statistics/reports/BRA_FS.pdf

Ribeiro DV, Fedrizzi EN, Steffens SM. The impact of the HPV vaccine on the world: initial outcomes and challenges. DST J Bras Doenças Sex Transm. 2020;32:e203204:1-7. https://doi.org/10.5327/DST-2177-8264-2003204

Drolet M, Bénard É, Boily MC, Ali H, Baandrup L, Bauer H, et al. Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect Dis. 2015;15(5):565-80. https://doi.org/10.1016/S1473-3099(14)71073-4

Dilley S, Miller KM, Huh WK. Human papillomavirus vaccination: ongoing challenges and future directions. Gynecol Oncol. 2020;156(2):498-502. https://doi.org/10.1016/j.ygyno.2019.10.018

Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância de Doenças Transmissíveis. Coordenação-Geral do Programa Nacional de Imunizações. Informe técnico da vacina papillomavirus humano 6, 11, 16 e 18 (recombinante) 2015. Segunda dose [Internet]. Brasília: Ministério da Saúde; 2015. [cited on 2023 Sept 29]. Available from: https://saude.es.gov.br/Media/sesa/PEI/Informe_Tecnico_vacina_papilomavirus_humano_6_11_16_18_recombinante_agosto_2015.pdf

Moura LL, Codeço CT, Luz PM. Human papillomavirus (HPV) vaccination coverage in Brazil: spatial and age cohort heterogeneity. Rev Bras Epidemiol. 2020;18:24:e210001. https://doi.org/10.1590/1980-549720210001

Burd EM. Human papillomavirus laboratory testing: the changing paradigm. Clin Microbiol Rev. 2016;29(2):291-319. https://doi.org/10.1128/CMR.00013-15

Gillison ML, Chaturvedi AK, Anderson WF, Fakhry C. Epidemiology of human papillomavirus-positive head and neck squamous cell carcinoma. J Clin Oncol. 2015;33(29):3235-42. https://doi.org/10.1200/JCO.2015.61.6995

Pim D, Banks L. Interaction of viral oncoproteins with cellular target molecules: infection with high-risk vs low-risk human papillomaviruses. APMIS. 2010;118(6-7):471-93. https://doi.org/10.1111/j.1600-0463.2010.02618.

Hartwig S, Syrjänen S, Dominiak-Felden G, Brotons M, Castellsagué X. Estimation of the Epidemiological Burden of Human Papillomavirus-related Cancers and Non-malignant diseases in Men in Europe: a review. BMC Cancer. 2012;12:30. https://doi.org/10.1186/1471-2407-12-30

Pogoda CS, Roden RB, Garcea RL. Immunizing against anogenital cancer: HPV vaccines. PLoS Pathog. 2016;12(5):e1005587. https://doi.org/10.1371/journal.ppat.1005587

Morán-Torres A, Pazos-Salazar NG, Téllez-Lorenzo S, Jiménez-Lima R, Lizano M, Reyes-Hernández DO, et al. HPV oral and oropharynx infection dynamics in young population. Braz J Microbiol. 2021;52(4):1991-2000. https://doi.org/10.1007/s42770-021-00602-3

D’Souza, G., Cullen K., Bowie J., Thorpe R., Fakhry C. Differences in oral sexual behaviors by gender, age, and race explain observed differences in prevalence of oral human papillomavirus infection. PLoS One. 2014;9(1):e86023. https://doi.org/10.1371/journal.pone.0086023

Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol. 2011;29(32):4294-301. https://doi.org/10.1200/JCO.2011.36.4596

Chaturvedi AK, Anderson WF, Lortet-Tieulent J, Curado MP, Ferlay J, Franceschi S, et al. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Oncol. 2013;31(36):4550-9. https://doi.org/10.1200/JCO.2013.50.3870

Bui TC. Markham CM, Ross MW, Mullen PD. Examining the association between oral health and oral HPV infection. Cancer Prev Res (Phila). 2013;6(9):917-24. https://doi.org/10.1158/1940-6207.CAPR-13-0081

Vardas E, Giuliano AR, Goldstone S, Palefsky JM, Moreira Jr ED, Penny ME, et al. External genital human papillomavirus prevalence and associated factors among heterosexual men on 5 continents. J Infect Dis. 2011;203(1):58-65. https://doi.org/10.1093/infdis/jiq015

Rocha WM, Afonso LA, Dobao E, Gouvea TD, Carestiato FN, Cavalcanti SMB. Evaluation of anogenital human papillomavirus infection in asymptomatic men from Rio de Janeiro, Brazil, Rev Patol Trop. 2015;44(4):375-85. https://doi.org/10.5216/rpt.v44i4.39241

Baptista AD, Simão CX, Santos VCG, Melgaço JG, Cavalcanti SMB, Fonseca SC, et al. Knowledge of human papillomavirus and Pap test among Brazilian university students. Rev Assoc Med Bras (1992). 2019;65(5):625-32. https://doi.org/10.1590/1806-9282.65.5.625

Thuler LCS, Bergmann A, Casado L. Perfil das pacientes com câncer do colo do útero no Brasil, 2000-2009: estudo de base secundária. Rev Bras Cancerol. 2012;58(3):351-7.

Teixeira LA. From gynecology offices to screening campaigns: the trajectory of cervical cancer prevention in Brazil. Hist Ciênc Saúde-Manguinhos. 2015;22(1):221-40. https://doi.org/10.1590/S0104-59702015000100013

Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S. Human papillomavirus and cervical cancer. Lancet. 2007;370(9590):890-907. https://doi.org/10.1016/S0140-6736(07)61416-0

Franceschi S, Castellsagué X, Dal Maso L, Smith JS, Plummer M, Ngelangel C, et al. Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer. 2002;86(5):705-11. https://doi.org/10.1038/sj.bjc.6600194

Kury CMH, Guimaraes GR, Leandro CG, Fernandes LA, Silva PRT, Petraglia TCMB, et al. Associations of human papillomavirus (HPV) genotypes and related risk factors in a cohort of women living with HIV in a Brazilian countryside city. J Med Virol. 2022;94(6):2802-10. https://doi.org/10.1002/jmv.27582

Drolet M, Bénard E, Pérez N, Brisson M; HPV Vaccination Impact Study Group. Population-level impact and herd effects the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis. Lancet. 2019;394(10197):497-509. https://doi.org/10.1016/S0140-6736(19)30298-3

Merck. Gardasil®9 (Human Papillomavirus 9-valent vaccine, recombinant) Instructions for preparing suspension for intramuscular injection [Internet]. 2014 [cited on 2023 Aug 14]. Available from: https://www.merck.com/product/usa/pi_circulars/g/gardasil_9/gardasil_9_pi.pdf

Downloads

Published

2023-12-20

How to Cite

1.
Silva KC da, Rocha WM da, Pereira MS, Andrade HB, Gouvea TD de, Kury CMH, et al. The Epidemiological surveillance of Human Papillomavirus (HPV) genotypes in oral and genital tracts and the impact of HPV vaccination on male university students from Rio de Janeiro state, Brazil. DST [Internet]. 2023 Dec. 20 [cited 2024 May 2];35. Available from: https://www.bjstd.org/revista/article/view/1392

Issue

Vol. 35 (2023)

Section

Original Article

License

Copyright (c) 2023 Brazilian Journal of Sexually Transmitted Diseases

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.