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HPV oral and oropharynx infection dynamics in young population

  • Clinical Microbiology - Research Paper
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Abstract

The incidence of human papillomavirus (HPV)-associated cancers, especially those from the head and neck region, has increased. The relatively early age of presentation of HPV-positive head and neck cancer (HNC) indicates that viral infection might be acquired early in life. Persistent HPV infection has been recognized as the main risk factor for cancer development, but most studies have focused on evaluating HPV persistence in the genital region. Thus, in this work, we aimed to evaluate the prevalence of HPV in oral cavity and oropharynx in a young population, as well as the possible persistence of the infection after 12 months. Our results indicate that almost half (46.8%) of the analyzed population harbors an HPV infection either in the oral cavity or in the oropharynx. Furthermore, after 1 year of initial identification, half of them eliminated the infection, and only one person (5.26%) exhibited persistence. Interestingly, 50% of the individuals who successfully eliminated the infection acquired a new viral type, indicating that even when the primary infection is effectively eliminated by the immune system, there is a dynamic circulation of HR-HPV types that produce reinfection. This dynamic HPV infection among young individuals could influence the future establishment of cancer in some proportion of the cases.

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Data availability

All data regarding the present study are included in the manuscript and tables.

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References

  1. McQuillan G, Kruszon-Moran D, Markowitz LE, Unger ER, Paulose-Ram R (2017) Prevalence of HPV in adults aged 18–69: United States, 2011–2014. NCHS Data Brief 280:1–8

    Google Scholar 

  2. Brianti P, De Flammineis E, Mercuri SR (2017) Review of HPV-related diseases and cancers. New Microbiol 40(2):80–85

    CAS  PubMed  Google Scholar 

  3. Brianti P, De Flammineis E, Mercuri SR et al (2018) The intersection of HPV epidemiology, genomics and mechanistic studies of HPV-mediated carcinogenesis. Viruses 18(2):1263–1269. https://doi.org/10.1038/nrc.2018.11

    Article  CAS  Google Scholar 

  4. Torres-Poveda K, Bahena-Roman M, Madrid-Gonzalez C et al (2014) Role of IL-10 and TGF-beta1 in local immunosuppression in HPV-associated cervical neoplasia. World J Clin Oncol 5(4):753–763. https://doi.org/10.5306/wjco.v5.i4.753

    Article  PubMed  PubMed Central  Google Scholar 

  5. Candotto V, Lauritano D, Nardone M et al (2017) HPV infection in the oral cavity: epidemiology, clinical manifestations and relationship with oral cancer. Oral Implantol (Rome) 10(3):209–220. https://doi.org/10.11138/orl/2017.10.3.209

    Article  CAS  Google Scholar 

  6. Castellsagué X, Alemany L, Quer M et al (2016) HPV involvement in head and neck cancers: comprehensive assessment of biomarkers in 3680 patients. J Natl Cancer Inst 108(6):djv403. https://doi.org/10.1093/jnci/djv403

    Article  CAS  PubMed  Google Scholar 

  7. Tumban EA (2019) Current update on human papillomavirus-associated head and neck cancers. Viruses 11(10):922. https://doi.org/10.3390/v11100922

    Article  CAS  PubMed Central  Google Scholar 

  8. Wood ZC, Bain CJ, Smith DD, Whiteman DC, Antonsson A (2017) Oral human papillomavirus infection incidence and clearance: a systematic review of the literature. J Gen Virol 98(4):519–526. https://doi.org/10.1099/jgv.0.000727

    Article  CAS  PubMed  Google Scholar 

  9. de Martel C, Plummer M, Vignat J, Franceschi S (2017) Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J cancer 141(4):664–670. https://doi.org/10.1002/ijc.30716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Ndiaye C, Mena M, Alemany L et al (2014) HPV DNA, E6/E7 mRNA, and p16INK4a detection in head and neck cancers: a systematic review and meta-analysis. Lancet Oncol 15(12):1319–1331. https://doi.org/10.1016/S1470-2045(14)70471-1

    Article  CAS  PubMed  Google Scholar 

  11. Leemans CR, Snijders PJF, Brakenhoff RH (2018) The molecular landscape of head and neck cancer. Nat Rev Cancer 18(5):269–282. https://doi.org/10.1038/nrc.2018.11

    Article  CAS  PubMed  Google Scholar 

  12. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68(6):394–424. https://doi.org/10.3322/caac.21492

  13. Sturgis EM, Ang KK (2011) The epidemic of HPV-associated oropharyngeal cancer is here: is it time to change our treatment paradigms? J Natl Compr Canc Netw 6:665–673. https://doi.org/10.6004/jnccn.2011.0055

    Article  Google Scholar 

  14. D’Souza G, Agrawal Y, Halpern J, Bodison S, Gillison ML (2009) Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J Infect Dis 199(9):1263–1269. https://doi.org/10.1086/597755

    Article  PubMed  Google Scholar 

  15. Ibieta-Zarco BR, Carrillo-García A, Ponce-De-León-Rosales S, Flores-Miranda MM, Mohar A, Lizano M (2012) Frequency and genotype distribution of multiple human papillomavirus infections in cancer of the head and neck in a Mexican population. Oral Surg Oral Med Oral Pathol Oral Radiol 114(3):350–357. https://doi.org/10.1016/j.oooo.2012.05.003

    Article  PubMed  Google Scholar 

  16. Anaya-Saavedra G, Ramírez-Amador V, Irigoyen-Camacho ME et al (2008) High association of human papillomavirus infection with oral cancer: a case-control study. Arch Med Res 39(2):189–197. https://doi.org/10.1016/j.arcmed.2007.08.003

    Article  CAS  PubMed  Google Scholar 

  17. Chaturvedi AK, Engels EA, Pfeiffer RM et al (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29(32):4294–4301. https://doi.org/10.1200/JCO.2011.36.4596

    Article  PubMed  PubMed Central  Google Scholar 

  18. Louvanto K, Rintala MA, Syrjänen KJ, Grénman SE, Syrjänen SM (2010) Genotype-specific persistence of genital human papillomavirus (HPV) infections in women followed for 6 years in the Finnish Family HPV Study. J Infect Dis 202(3):436–444. https://doi.org/10.1086/653826

    Article  PubMed  Google Scholar 

  19. Bijina BR, Ahmed J, Shenoy N, Ongole R, Shenoy S, Baliga S (2016) Detection of human papilloma virus in potentially malignant and malignant lesions of the oral cavity and a study of associated risk factors. South Asian J Cancer 4:179–181. https://doi.org/10.4103/2278-330X.195337

    Article  Google Scholar 

  20. Simonidesová S, Hamšíková E, Klozar J, Tachezy R (2018) The prevalence of oral HPV infection in healthy populations: a systematic review with a focus on European populations. Epidemiol Mikrobiol Imunol Cas Spol pro Epidemiol a Mikrobiol Ces Lek Spol JE Purkyne 67(4):175–183

    Google Scholar 

  21. Chaturvedi AK, Graubard BI, Broutian T et al (2018) Effect of prophylactic human papillomavirus (HPV) vaccination on oral HPV infections among young adults in the United States. J Clin Oncol Off J Am Soc Clin Oncol 36(3):262–267. https://doi.org/10.1200/JCO.2017.75.0141

    Article  CAS  Google Scholar 

  22. Ablanedo-Terrazas Y, Romero-Mora K, Gómez-Palacio M et al (2018) Prevalence and risk factors for oral human papillomavirus infection in Mexican HIV-infected men. Salud Publica Mex 60(6):653–657. https://doi.org/10.21149/9834

    Article  PubMed  Google Scholar 

  23. Lawton G, Thomas S, Schonrock J, Monsour F, Frazer I (1992) Human papillomaviruses in normal oral mucosa: a comparison of methods for sample collection. J Oral Pathol Med Off Publ Int Assoc Oral Pathol Am Acad Oral Pathol 21(6):265–269. https://doi.org/10.1111/j.1600-0714.1992.tb01008.x

    Article  CAS  Google Scholar 

  24. Taberna M, Mena M, Pavón MA, Alemany L, Gillison ML, Mesía R (2017) Human papillomavirus-related oropharyngeal cancer. Ann Oncol 28(10):2386–2398. https://doi.org/10.1093/annonc/mdx304

    Article  CAS  PubMed  Google Scholar 

  25. Gayet C, Gutiérrez JP (2014) Calendario de inicio sexual en México. Comparación entre encuestas nacionales y tendencias en el tiempo. Salud Publica Mex 56(6):638–647

    Article  Google Scholar 

  26. Kreimer AR, Pierce Campbell CM, Lin H-Y et al (2013) Incidence and clearance of oral human papillomavirus infection in men: the HIM cohort study. Lancet (London, England) 382(9895):877–887. https://doi.org/10.1016/S0140-6736(13)60809-0

    Article  Google Scholar 

  27. Dawson DA (2011) Defining risk drinking. Alcohol Res Heal J Natl Inst Alcohol Abus Alcohol 34(2):144–156

    Google Scholar 

  28. Wilson D, Parsons J, Wakefield M (1999) The health-related quality-of-life of never smokers, ex-smokers, and light, moderate, and heavy smokers. Prev Med (Baltim) 29(3):139–144. https://doi.org/10.1006/pmed.1999.0523

    Article  CAS  Google Scholar 

  29. Acha A, Ruesga MT, Rodríguez MJ, Martínez de Pancorbo MA, Aguirre JM (2005) Applications of the oral scraped (exfoliative) cytology in oral cancer and precancer. Med Oral Patol Oral Cir Bucal 10(2):95–102

    PubMed  Google Scholar 

  30. Brunotto M, Zárate AM, Cismondi A, del Fernández M, C, Noher de Halac RI, (2005) Valuation of exfoliative cytology as prediction factor in oral mucosa lesions. Med Oral Patol Oral Cir Bucal 10(Suppl 2):E92-102

    PubMed  Google Scholar 

  31. Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F et al (2010) Exfoliative cytology for diagnosing oral cancer. Biotech Histochem Off Publ Biol Stain Comm 85(3):177–187. https://doi.org/10.3109/10520290903162730

    Article  Google Scholar 

  32. Ayala-Díaz S, Jiménez-Lima R, Ramírez-Alcántara KM et al (2019) Presence of Papillomavirus DNA sequences in the canine transmissible venereal tumor (CTVT). PeerJ 7:e7962. https://doi.org/10.7717/peerj.7962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Carrillo-García A, Ponce-de-León-Rosales S, Cantú-de-León D et al (2014) Impact of human papillomavirus coinfections on the risk of high-grade squamous intraepithelial lesion and cervical cancer. Gynecol Oncol 134(3):534–539. https://doi.org/10.1016/j.ygyno.2014.06.018

    Article  PubMed  Google Scholar 

  34. Sathish N, Wang X, Yuan Y (2014) Human papillomavirus (HPV)-associated oral cancers and treatment strategies. J Dent Res 93(7 Suppl):29S-36S. https://doi.org/10.1177/0022034514527969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kreimer AR, Bhatia RK, Messeguer AL, González P, Herrero R, Giuliano AR (2010) Oral human papillomavirus in healthy individuals: a systematic review of the literature. Sex Transm Dis 37(6):386–391. https://doi.org/10.1097/OLQ.0b013e3181c94a3b

    Article  PubMed  Google Scholar 

  36. Louvanto K, Rautava J, Willberg J et al (2013) Genotype-specific incidence and clearance of human papillomavirus in oral mucosa of women: a six-year follow-up study. PLoS ONE 8(1):e53413. https://doi.org/10.1371/journal.pone.0053413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Gonzalez-Losa MDR, Barrera ES, Herrera-Pech V, Conde-Ferráez L, Puerto-Solís M, Ayora-Talavera G (2015) Epidemiology of oral HPV in the oral mucosa in women without signs of oral disease from Yucatan. Mexico Brazilian J Microbiol 46(1):301–306. https://doi.org/10.1590/S1517-838246120130976

    Article  Google Scholar 

  38. Sinha P, Logan HL, Mendenhall WM (2012) Human papillomavirus, smoking, and head and neck cancer. Am J Otolaryngol 33(1):130–136. https://doi.org/10.1016/j.amjoto.2011.02.001

    Article  PubMed  Google Scholar 

  39. Torres-Poveda K, Piña-Sánchez P, Vallejo-Ruiz V et al (2020) Molecular markers for the diagnosis of high-risk human papillomavirus infection and triage of human papillomavirus-positive women. Rev Invest Clin 72(4):198–212. https://doi.org/10.24875/RIC.20000058

    Article  CAS  PubMed  Google Scholar 

  40. De Guglielmo Z, Rodríguez A (2010) Methods used in the identification of human papillomavirus. An Sist Sanit Navar 33(1):71–77. https://doi.org/10.4321/s1137-66272010000100008

    Article  PubMed  Google Scholar 

  41. Sasagawa T, Takagi H, Makinoda S (2012) Immune responses against human papillomavirus (HPV) infection and evasion of host defense in cervical cancer. J Infect Chemother Off J Japan Soc Chemother 18(6):807–815. https://doi.org/10.1007/s10156-012-0485-5

    Article  CAS  Google Scholar 

  42. Kalmuss D, Davidson A, Cohall A, Laraque D, Cassell C (2003) Preventing sexual risk behaviors and pregnancy among teenagers: linking research and programs. Perspect Sex Reprod Health 35(2):87–93. https://doi.org/10.1363/3508703

    Article  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Dr. Elizabeth Langley (Instituto Nacional de Cancerología, Mexico) for her valuable comments on the manuscript.

Funding

This work was partially supported by Benemérita Universidad Autónoma de Puebla Ref: VIEP-BUAP 00104, CONACyT PRONAII-7-VIRUS Y CÁNCER Ref: 303044, and Instituto Nacional de Cancerología, Mexico, Ref: (015/039/IBI) (CEI/998/15) and (017/048/IBI) (CEI/1227/17).

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Author notes

  1. Adriana Morán-Torres and Nidia G. Pazos-Salazar contributed equally to this work.

Authors and Affiliations

  1. Departamento de Microbiología, Facultad de Ciencias Químicas, Benemérita Universidad Autónoma de Puebla, Av. San Claudio, Edificio FCQ1, Ciudad Universitaria, 72570, Puebla, Mexico

    Adriana Morán-Torres, Nidia G. Pazos-Salazar & Susana Téllez-Lorenzo

  2. Instituto Nacional de Cancerología, Av. San Fernando No. 22, Col. Sección XVI, Tlalpan, 14080, Mexico City, Mexico

    Adriana Morán-Torres, Roberto Jiménez-Lima, Marcela Lizano, Diego O. Reyes-Hernández & Joaquín Manzo-Merino

  3. Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, 04510, Mexico City, Mexico

    Marcela Lizano

  4. Departamento de Patologia, Hospital General “Dr. Manuel Gea Gonzalez”, Calzada de Tlalpan 4800, Belisario Dominguez secc 1, Tlalpan, 14080, Mexico City, , Mexico

    José de J. Marin-Aquino

  5. Cátedras CONACyT-Instituto Nacional de Cancerología, San Fernando No. 22, Col. Sección XVI, Tlalpan, 14080, Mexico City, Mexico

    Joaquín Manzo-Merino

Authors
  1. Adriana Morán-Torres
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  2. Nidia G. Pazos-Salazar
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  3. Susana Téllez-Lorenzo
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  4. Roberto Jiménez-Lima
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  5. Marcela Lizano
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  7. José de J. Marin-Aquino
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  8. Joaquín Manzo-Merino
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Contributions

Conceptualization: JM-M and NGP-S.

Data collection: AM-T, NGP-S, ST-L, DOR-H, JJM-A.

Performing experiments: AM-T, NGP-S, ST-L, DOR-H, JJM-A.

Formal analysis: RJ-L, JM-M, AM-T, DOR-H, ML, NGP-S.

Funding acquisition: JM-M, ML, NGP-S.

Writing and reviewing the manuscript: JM-M, ML, AM-T, DOR-H, ST-L, NGP-S.

Figure design and elaboration: DOR-H, AM-T, JM-M.

Supervision: JM-M.

Corresponding author

Correspondence to Joaquín Manzo-Merino.

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The present study was approved by Institutional Board, Ref: VIEP-BUAP 00104.

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Participants provided written informed consent before enrolling in the present study.

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The authors declare no competing interests.

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Morán-Torres, A., Pazos-Salazar, N.G., Téllez-Lorenzo, S. et al. HPV oral and oropharynx infection dynamics in young population. Braz J Microbiol 52, 1991–2000 (2021). https://doi.org/10.1007/s42770-021-00602-3

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  • DOI: https://doi.org/10.1007/s42770-021-00602-3

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