A Contemporary Systematic Review on Repartition of HPV-Positivity in Oropharyngeal Cancer Worldwide

Amanda F Carlander, Kathrine K Jakobsen, Simone K Bendtsen, Martin Garset-Zamani, Charlotte D Lynggaard, Jakob Schmidt Jensen, Christian Grønhøj, Christian von Buchwald, Amanda F Carlander, Kathrine K Jakobsen, Simone K Bendtsen, Martin Garset-Zamani, Charlotte D Lynggaard, Jakob Schmidt Jensen, Christian Grønhøj, Christian von Buchwald

Abstract

Significant variation in human papillomavirus (HPV) prevalence in oropharyngeal squamous cell carcinoma (OPSCC) across countries ranging from 11% in Brazil to 74% in New Zealand has been reported earlier. The aim of this study was to systematically review the most recently published studies on the occurrence of HPV in OPSCC globally. PubMed and Embase were systematically searched for articles assessing the occurrence of HPV+ OPSCC published between January 2016 and May 2021. Studies with a study period including 2015 and the following years were included. Both HPV DNA and/or p16 were accepted as indicators of HPV+ OPSCC. 31 studies were enrolled comprising 49,564 patients with OPSCC (range 12-42,024 patients per study) from 26 different countries covering all continents. The lowest occurrences of HPV+ OPSCC were observed in India (0%) and Spain (10%) and the highest occurrences were observed in Lebanon (85%) and Sweden (70%). We observed great variation in HPV prevalence in OPSCC worldwide varying from 0% to 85%. The highest occurrences of HPV+ OPSCC were found in general in Northern European countries, USA, Lebanon, China, and South Korea. We observed a trend of increase in HPV-positivity, indicating a mounting burden of HPV+ OPSCC.

Keywords: HPV genotype; global; head and neck cancer; human papillomavirus; oropharyngeal cancer; oropharyngeal squamous cell carcinoma; prevalence; worldwide.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
PRISMA flow diagram of article selection.
Figure 2
Figure 2
Proportion meta-analysis of HPV+ OPSCC in enrolled studies. Occurrence of HPV+ OPSCC worldwide among patients with OPSCC. OPSCC: oropharyngeal squamous cell carcinoma. HPV +: human papillomavirus-positive.
Figure 3
Figure 3
HPV-positivity in patients with OPSCC over time worldwide. OPSCC: oropharyngeal squamous cell carcinoma. HPV: human papillomavirus.

References

    1. Ferlay J., Colombet M., Soerjomataram I., Mathers C., Parkin D.M., Piñeros M., Znaor A., Bray F. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int. J. Cancer. 2019;144:1941–1953. doi: 10.1002/ijc.31937.
    1. Chaturvedi A.K., Anderson W.F., Lortet-Tieulent J., Curado M.P., Ferlay J., Franceschi S., Rosenberg P.S., Bray F., Gillison M.L. Worldwide Trends in Incidence Rates for Oral Cavity and Oropharyngeal Cancers. J. Clin. Oncol. 2013;31:4550–4559. doi: 10.1200/JCO.2013.50.3870.
    1. Dalianis T. Human papillomavirus and oropharyngeal cancer, the epidemics, and significance of additional clinical biomarkers for prediction of response to therapy (review) Int. J. Oncol. 2014;45:1799–1805. doi: 10.3892/ijo.2014.2355.
    1. Zamani M., Grønhøj C., Jensen D.H., Carlander A.F., Agander T., Kiss K., Olsen C., Baandrup L., Nielsen F.C., Andersen E., et al. The current epidemic of HPV-associated oropharyngeal cancer: An 18-year Danish population-based study with 2,169 patients. Eur. J. Cancer. 2020;134:52–59. doi: 10.1016/j.ejca.2020.04.027.
    1. Bouvard V., Baan R., Straif K., Grosse Y., Secretan B., El Ghissassi F., Benbrahim-Tallaa L., Guha N., Freeman C., Galichet L., et al. A review of human carcinogens--Part B: Biological agents. Lancet Oncol. 2009;10:321–322. doi: 10.1016/S1470-2045(09)70096-8.
    1. Hayes D.N., Van Waes C., Seiwert T.Y. Genetic Landscape of Human Papillomavirus-Associated Head and Neck Cancer and Comparison to Tobacco-Related Tumors. J. Clin. Oncol. 2015;33:3227–3234. doi: 10.1200/JCO.2015.62.1086.
    1. Lewis J.S., Khan R.A., Masand R.P., Chernock R.D., Zhang Q., Al-Naief N.S., Muller S., McHugh J.B., Prasad M.L., Brandwein-Gensler M., et al. Recognition of nonkeratinizing morphology in oropharyngeal squamous cell carcinoma—A prospective cohort and interobserver variability study. Histopathology. 2012;60:427–436. doi: 10.1111/j.1365-2559.2011.04092.x.
    1. Grønhøj C., Jensen D.H., Dehlendorff C., Marklund L., Wagner S., Mehanna H., Munck-Wikland E., Ramqvist T., Näsman A., Wittekindt C., et al. Development and external validation of nomograms in oropharyngeal cancer patients with known HPV-DNA status: A European Multicentre Study (OroGrams) Br. J. Cancer. 2018 doi: 10.1038/s41416-018-0107-9.
    1. Mirghani H., Casiraghi O., Guerlain J., Amen F., He M.X., Ma X.J., Luo Y., Mourareau C., Drusch F., Lakdhar A.B., et al. Diagnosis of HPV driven oropharyngeal cancers: Comparing p16 based algorithms with the RNAscope HPV-test. Oral. Oncol. 2016;62:101–108. doi: 10.1016/j.oraloncology.2016.10.009.
    1. Mariz B.A.L.A., Kowalski L.P., William W.N., de Castro G., Chaves A.L.F., Santos M., de Oliveira T.B., Araújo A.L.D., Normando A.G.C., Ribeiro A.C.P., et al. Global prevalence of human papillomavirus-driven oropharyngeal squamous cell carcinoma following the ASCO guidelines: A systematic review and meta-analysis. Crit. Rev. Oncol. Hematol. 2020;156 doi: 10.1016/j.critrevonc.2020.103116.
    1. Stjernstrøm K.D., Jensen J.S., Jakobsen K.K., Grønhøj C., von Buchwald C. Current status of human papillomavirus positivity in oropharyngeal squamous cell carcinoma in Europe: A systematic review. Acta Otolaryngol. 2019;139:1112–1116. doi: 10.1080/00016489.2019.1669820.
    1. Aboagye E., Agyemang-Yeboah F., Duduyemi B.M., Obirikorang C. Human papillomavirus detection in head and neck squamous cell carcinomas at a tertiary hospital in Sub-Saharan Africa. Sci. World J. 2019;2019 doi: 10.1155/2019/2561530.
    1. Faraji F., Rettig E.M., Tsai H.L., El Asmar M., Fung N., Eisele D.W., Fakhry C. The prevalence of human papillomavirus in oropharyngeal cancer is increasing regardless of sex or race, and the influence of sex and race on survival is modified by human papillomavirus tumor status. Cancer. 2019;125:761–769. doi: 10.1002/cncr.31841.
    1. Bandhary S.K., Shetty V., Saldanha M., Gatti P., Devegowda D., Pushkal S.R., Shetty A.K. Detection of human papilloma virus and risk factors among patients with head and neck squamous cell carcinoma attending a tertiary referral centre in South India. Asian Pacific J. Cancer Prev. 2018;19:1325–1330. doi: 10.22034/APJCP.2018.19.5.1325.
    1. Maroun C.A., Al Feghali K., Traboulsi H., Dabbous H., Abbas F., Dunya G., Ziade G., Mahfouz R., Youssef B., Tamim H., et al. HPV-related oropharyngeal cancer prevalence in a middle eastern population using E6/E7 PCR. Infect. Agent. Cancer. 2020;15:1–7. doi: 10.1186/s13027-019-0268-z.
    1. Tealab S.H., Sedhom N.F.H., Hassouna A., Gouda I., Ismail H. Prevalence of human papilloma virus in oropharyngeal, tongue and lip squamous cell carcinoma: An experience from the Egyptian National Cancer Institute. J. Investig. Med. 2019;67:1061–1066. doi: 10.1136/jim-2018-000968.
    1. Kabagenyi F., Otiti J., Namwagala J., Kamulegeya A., Kalungi S. A descriptive study of human papilloma virus in upper aero-digestive squamous cell carcinoma at Uganda cancer institute assessed by P16 immunohistochemistry. Cancers Head Neck. 2020;5 doi: 10.1186/s41199-020-00057-3.
    1. Sekee T.R., Burt F.J., Goedhals D., Goedhals J., Munsamy Y., Seedat R.Y. Human papillomavirus in head and neck squamous cell carcinomas in a South African cohort. Papillomavirus Res. 2018;6:58–62. doi: 10.1016/j.pvr.2018.10.006.
    1. Argirion I., Zarins K.R., McHugh J., Cantley R.L., Teeramatwanich W., Laohasiriwong S., Kasemsiri P., Naruikon J., Srimanta P., Chinn S.B., et al. Increasing prevalence of HPV in oropharyngeal carcinoma suggests adaptation of p16 screening in Southeast Asia. J. Clin. Virol. 2020;132:104637. doi: 10.1016/j.jcv.2020.104637.
    1. Kim Y., Joo Y.H., Kim M.S., Lee Y.S. Prevalence of high-risk human papillomavirus and its genotype distribution in head and neck squamous cell carcinomas. J. Pathol. Transl. Med. 2020;54:411–418. doi: 10.4132/jptm.2020.06.22.
    1. Xu T., Shen C., Wei Y., Hu C., Wang Y., Xiang J., Sun G.H., Su F., Wang Q., Lu X. Human papillomavirus (HPV) in Chinese oropharyngeal squamous cell carcinoma (OPSCC): A strong predilection for the tonsil. Cancer Med. 2020;9:6556–6564. doi: 10.1002/cam4.3339.
    1. Ni G., Huang K., Luan Y., Cao Z., Chen S., Ma B., Yuan J., Wu X., Chen G., Wang T., et al. Human papillomavirus infection among head and neck squamous cell carcinomas in southern China. PLoS ONE. 2019;14:1–13. doi: 10.1371/journal.pone.0221045.
    1. Nopmaneepaisarn T., Tangjaturonrasme N., Rawangban W., Vinayanuwattikun C., Keelawat S., Bychkov A. Low prevalence of p16-positive HPV-related head-neck cancers in Thailand: Tertiary referral center experience. BMC Cancer. 2019;19:1–9. doi: 10.1186/s12885-019-6266-0.
    1. Chotipanich A., Siriarechakul S., Mungkung O. Role of high-risk human papillomavirus in the etiology of oral and oropharyngeal cancers in Thailand: A case–control study. SAGE Open Med. 2018;6:205031211876560. doi: 10.1177/2050312118765604.
    1. Shaikh M.H., Khan A.I., Sadat A., Chowdhury A.H., Jinnah S.A., Gopalan V., Lam A.K., Clarke D.T.W., McMillan N.A.J., Johnson N.W. Prevalence and types of high-risk human papillomaviruses in head and neck cancers from Bangladesh. BMC Cancer. 2017;17:1–11. doi: 10.1186/s12885-017-3789-0.
    1. Toman J., Von Larson S., Umeno H., Kurita T., Furusaka T., Hasegawa H., Prasad M.L., Sasaki C.T. HPV-Positive Oropharyngeal Cancer Via p16 Immunohistochemistry in Japan. Ann. Otol. Rhinol. Laryngol. 2017;126:152–158. doi: 10.1177/0003489416681582.
    1. Yap L.F., Lai S.L., Rhodes A., Sathasivam H.P., Abdullah M.A., Pua K.C., Rajadurai P., Cheah P.L., Thavaraj S., Robinson M., et al. Clinico-pathological features of oropharyngeal squamous cell carcinomas in Malaysia with reference to HPV infection. Infect. Agent. Cancer. 2018;13:1–6. doi: 10.1186/s13027-018-0193-6.
    1. Alsbeih G., Al-Harbi N., Bin Judia S., Al-Qahtani W., Khoja H., El-Sebaie M., Tulbah A. Prevalence of human papillomavirus (HPV) infection and the association with survival in saudi patients with head and neck squamous cell carcinoma. Cancers. 2019;11:820. doi: 10.3390/cancers11060820.
    1. Khasawneh A.I., Himsawi N., Abu-Raideh J., Salameh M., Abdullah N., Khasawneh R., Saleh T. Prevalence of Human Papillomavirus Associated with Head and Neck Squamous Cell Carcinoma in Jordanian Patients. Open Microbiol. J. 2020;14:57–64. doi: 10.2174/1874285802014010057.
    1. Mhawej R., Ghorra C., Naderi S., Khoueir N., Abou Hamad W., Melkane A.E. Human papillomavirus prevalence and clinicopathological associations in oropharyngeal squamous cell carcinoma in the Lebanese population. J. Laryngol. Otol. 2018;132:636–641. doi: 10.1017/S0022215118001019.
    1. Girardi F.M., Wagner V.P., Martins M.D., Abentroth A.L., Hauth L.A. Prevalence of p16 expression in oropharyngeal squamous cell carcinoma in southern Brazil. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2020;130:681–691. doi: 10.1016/j.oooo.2020.08.021.
    1. Donà M.G., Rollo F., Pichi B., Spriano G., Moretto S., Covello R., Pellini R., Benevolo M. Evolving profile of hpv-driven oropharyngeal squamous cell carcinoma in a national cancer institute in italy: A 10-year retrospective study. Microorganisms. 2020;8:1498. doi: 10.3390/microorganisms8101498.
    1. Haeggblom L., Attoff T., Jingru Y., Holzhauser S., Vlastos A., Mirzae L., Ährlund-Richter A., Munck-wikland E., Marklund L., Lalle H.-N., et al. Changes in incidence and prevalence of human papillomavirus in tonsillar and base of tongue cancer during 2000-2016 in the Stockholm region and Sweden. Head Neck. 2018:1–8. doi: 10.1002/hed.25585.
    1. Mena M., Frias-Gomez J., Taberna M., Quirós B., Marquez S., Clavero O., Baena A., Lloveras B., Alejo M., León X., et al. Epidemiology of human papillomavirus-related oropharyngeal cancer in a classically low-burden region of southern Europe. Sci. Rep. 2020;10:1–11. doi: 10.1038/s41598-020-70118-7.
    1. Rietbergen M.M., van Bokhoven A.A.J.D., Lissenberg-Witte B.I., Heideman D.A.M., Leemans C.R., Brakenhoff R.H., Bloemena E. Epidemiologic associations of HPV-positive oropharyngeal cancer and (pre)cancerous cervical lesions. Int. J. Cancer. 2018;143:283–288. doi: 10.1002/ijc.31315.
    1. Tsimplaki E., Argyri E., Sakellaridis A., Kyrodimos E., Xesfyngi D., Panotopoulou E. Oropharyngeal and laryngeal but not oral cancers are strongly associated with high-risk human papillomavirus in 172 Greek patients. J. Med. Virol. 2017;89:170–176. doi: 10.1002/jmv.24614.
    1. Božinović K., Sabol I., Rakušić Z., Jakovčević A., Šekerija M., Lukinović J., Prgomet D., Grce M. HPV-driven oropharyngeal squamous cell cancer in Croatia—Demography and survival. PLoS ONE. 2019;14:1–17. doi: 10.1371/journal.pone.0211577.
    1. Del Mistro A., Frayle H., Menegaldo A., Favaretto N., Gori S., Nicolai P., Spinato G., Romeo S., Tirelli G., da Mosto M.C., et al. Age-independent increasing prevalence of Human Papillomavirus-driven oropharyngeal carcinomas in North-East Italy. Sci. Rep. 2020;10:1–10. doi: 10.1038/s41598-020-66323-z.
    1. Wittekindt C., Wagner S., Bushnak A., Prigge E.S., Von Knebel Doeberitz M., Wurdemann N., Bernhardt K., Pons-Kuhnemann J., Maulbecker-Armstrong C., Klussmann J.P. Increasing incidence rates of oropharyngeal squamous cell carcinoma in Germany and significance of disease burden attributed to human papillomavirus. Cancer Prev. Res. 2019;12:375–382. doi: 10.1158/1940-6207.CAPR-19-0098.
    1. Adilbay D., Adilbayev G., Kidirbayeva G., Shipilova V., Sadyk Z., Koyanbekova G., Sokolenko E., Klozar J. HPV infection and P16 expression in oral and oropharyngeal cancer in Kazakhstan. Infect. Agent. Cancer. 2018;13:2–5. doi: 10.1186/s13027-018-0175-8.
    1. Wakeham K., Pan J., Pollock K.G., Millan D., Bell S., McLellan D., McPhaden A., Conway D.I., Graham S.V., Kavanagh K., et al. A Prospective Cohort Study of Human Papillomavirus-Driven Oropharyngeal Cancers: Implications for Prognosis and Immunisation. Clin. Oncol. 2019;31:e132–e142. doi: 10.1016/j.clon.2019.05.010.
    1. Lewis J.S., Beadle B., Bishop J.A., Chernock R.D., Colasacco C., Lacchetti C., Moncur J.T., Rocco J.W., Schwartz M.R., Seethala R.R., et al. Human papillomavirus testing in head and neck carcinomas guideline from the college of American pathologists. Arch. Pathol. Lab. Med. 2018;142:559–597. doi: 10.5858/arpa.2017-0286-CP.
    1. Castellsagué X., Alemany L., Quer M., Halec G., Quirós B., Tous S., Clavero O., Alòs L., Biegner T., Szafarowski T., et al. HPV Involvement in Head and Neck Cancers: Comprehensive Assessment of Biomarkers in 3680 Patients. J. Natl. Cancer Inst. 2016;108:1–12. doi: 10.1093/jnci/djv403.
    1. Näsman A., Du J., Dalianis T. A global epidemic increase of an HPV-induced tonsil and tongue base cancer—potential benefit from a pan-gender use of HPV vaccine. J. Intern. Med. 2020;287:134–152. doi: 10.1111/joim.13010.
    1. Lehtinen M., Luostarinen T., Vänskä S., Söderlund-Strand A., Eriksson T., Natunen K., Apter D., Baussano I., Harjula K., Hokkanen M., et al. Gender-neutral vaccination provides improved control of human papillomavirus types 18/31/33/35 through herd immunity: Results of a community randomized trial (III) Int. J. Cancer. 2018;143:2299–2310. doi: 10.1002/ijc.31618.
    1. Mehanna H., Bryant T.S., Babrah J., Louie K., Bryant J.L., Spruce R.J., Batis N., Olaleye O., Jones J., Struijk L., et al. Human Papillomavirus (HPV) Vaccine Effectiveness and Potential Herd Immunity for Reducing Oncogenic Oropharyngeal HPV-16 Prevalence in the United Kingdom: A Cross-sectional Study. Clin. Infect. Dis. 2019;69:1296–1302. doi: 10.1093/cid/ciy1081.
    1. Wolff E., Elfström K.M., Haugen Cange H., Larsson S., Englund H., Sparén P., Roth A. Cost-effectiveness of sex-neutral HPV-vaccination in Sweden, accounting for herd-immunity and sexual behaviour. Vaccine. 2018;36:5160–5165. doi: 10.1016/j.vaccine.2018.07.018.
    1. Schache A.G., Liloglou T., Risk J.M., Filia A., Jones T.M., Sheard J., Woolgar J.A., Helliwell T.R., Triantafyllou A., Robinson M., et al. Evaluation of human papilloma virus diagnostic testing in oropharyngeal squamous cell carcinoma: Sensitivity, specificity, and prognostic discrimination. Clin. Cancer Res. 2011;17:6262–6271. doi: 10.1158/1078-0432.CCR-11-0388.

Source: PubMed

Sponsor e collaboratori

Condizioni mediche

Interventi farmacologici

3
Sottoscrivi