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Evolving disparities in the epidemiology of oral cavity and oropharyngeal cancers

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Abstract

Incidence rates of head and neck cancers (HNC) associated with human papillomavirus (HPVa) infection are increasing while non-HPV-associated (non-HPVa) HNC cancer rates are decreasing. As nearly all sexually active individuals will acquire an HPV infection, it is important to understand epidemiologic trends of HNCs associated with this sexually transmitted disease. We analyzed SEER 9 (1973–2012) and 18 data (2000–2012) for HPVa HNCs (oropharynx area; OP) and non-HPVa (oral cavity area; OC). Incidence rates were examined by gender, race, rurality, geographic location, and time. Joinpoint regression analyses assessed temporal variations. From 1973 to 2012, OC incidence decreased while OP increased, with changes largely driven by males (whose OP rate increased 106.2% vs female decrease of 10.3%). Males consistently had higher rates of both cancer groups across each registry except Alaska, OP rates among blacks changed from significantly above whites to below, and trend analysis indicated significant differences in rates over time by gender, race, and geography. Analysis of SEER 18 found that rates discordantly varied by group and gender across the 18 registries, as did the male/female rate ratio with overall means of 4.7 for OP versus 1.7 for OC (only Alaska and Georgia having overlapping ranges). Our findings indicate that much of the HPVa rate increases were driven by rate increases among males and that there were changing differences in risk between genders, race, and geographic location. The epidemiology of HNCs is complex, with locally relevant factors requiring further research for elucidation of demographic disparities in incidence.

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References

  1. 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. doi:10.1200/JCO.2011.36.4596

    Article  PubMed  PubMed Central  Google Scholar 

  2. National Institutes of Health, National Cancer Institute (2016) HPV and Cancer. Available at: http://www.cancer.gov/about-cancer/causes-prevention/risk/infectious-agents/hpv-fact-sheet#q7. Accessed 4 Jan 2016

  3. Cole L, Polfus L, Peters ES (2012) Examining the incidence of human papillomavirus-associated head and neck cancers by race and ethnicity in the U.S., 1995–2005. PLoS ONE 7(3):e32657. doi:10.1371/journal.pone.0032657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Simard EP, Ward EM, Seigel R, Jemal A (2012) Cancers with increasing trends in the United States: 1999 through 2008. CA Cancer J Clin 62(2):118–128

    Article  PubMed  Google Scholar 

  5. Gillison ML, Broutian T, Pickard RK et al (2012) Prevalence of oral HPV infection in the United States, 2009–2010. JAMA 307(7):693–703. doi:10.1001/jama.2012.101.

    Article  CAS  PubMed  Google Scholar 

  6. Zhang H, Dziegielewski PT, Jean Nguyen TT et al (2015) The effects of geography on survival in patients with oral cavity squamous cell carcinoma. Oral Oncol 51(6):578–585. doi:10.1016/j.oraloncology.2015.03.012

    Article  PubMed  Google Scholar 

  7. Chesson HW, Dunne EF, Hariri S, Markowitz LE (2014) The estimated lifetime probability of acquiring human papillomavirus in the United States. Sex Transm Dis 41:660–664

    Article  PubMed  Google Scholar 

  8. Deschler DG, Richmon JD, Khariwala SS, Ferris RL, Wang MB (2014) The “new” head and neck cancer patient-young, nonsmoker, nondrinker, and HPV positive: evaluation. Otolaryngol Head Neck Surg 151(3):375–380. doi:10.1177/0194599814538605

    Article  PubMed  PubMed Central  Google Scholar 

  9. Jayaprakash V, Reid M, Hatton E et al (2011) Human papillomavirus types 16 and 18 in epithelial dysplasia of oral cavity and oropharynx: a meta-analysis, 1985–2010. Oral Oncol 47:1048–1054

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zaravinos A (2014) An updated overview of HPV-associated head and neck carcinomas. Oncotarget 5:3956–3969

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kreimer AR, Clifford GM, Boyle P, Franceschi S (2005) Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol Biomarkers Prev 14(2):467–475

    Article  CAS  PubMed  Google Scholar 

  12. Ernster JA, Sciotto CG, O’Brien MM et al (2007) Rising incidence of oropharyngeal cancer and the role of oncogenic human papilloma virus. Laryngoscope 117:2115–2128

    Article  PubMed  Google Scholar 

  13. Shin A, Jung YS, Jung KW, Kim K, Ryu J, Won YJ (2013) Trends of human papillomavirus-related head and neck cancers in Korea: National cancer registry data. Laryngoscope 123:E30–E37

    Article  PubMed  Google Scholar 

  14. Chaturvedi AK, Engels EA, Anderson WF, Gillison ML (2008) Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol 26(4):612–619. doi:10.1200/JCO.2007.14.1713

    Article  PubMed  Google Scholar 

  15. Jemal A, Simard EP, Dorell C et al (2013) Annual Report to the Nation on the Status of Cancer, 1975–2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 105(3):175–201. doi:10.1093/jnci/djs491

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chaturvedi AK, Anderson WF et al (2013) Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin Onco 31:4550–4559

    Article  Google Scholar 

  17. Jamal A, Homa DM, O’Connor E, Babb SD, Caraballo RS, Singh T, Hu SS, King BA (2015) Current cigarette smoking among adults—United States, 2005–2014. MMWR Morb Mortal Wkly Rep 64(44):1233–1240. doi:10.15585/mmwr.mm6444a2

    Article  PubMed  Google Scholar 

  18. Dawson DA, Goldstein RB, Saha TD, Grant BF (2015) Changes in alcohol consumption: United States, 2001–2002 to 2012–2013. Drug Alcohol Depend 148:56–61. doi:10.1016/j.drugalcdep.2014.12.016

    Article  PubMed  Google Scholar 

  19. Nguyen NP, Nguyen LM, Thomas S, Hong-Ly B, Chi A, Vos P, Karlsson U, Vinh-Hung V; International Geriatric Radiation Oncology Group (2016) Oral sex and oropharyngeal cancer: the role of the primary care physicians. Medicine 95(28):e4228. doi:10.1097/MD.0000000000004228

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fakery C, Westra WH, Li S et al (2008) Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 100:261–269

    Article  Google Scholar 

  22. Ang KK, Harris J, Wheeler R et al (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363:24–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Benard VB, Johnson CJ, Thompson TD, Roland KB, Lin SM, Cokkinides V, Tangka F, Hawkins NA, Lawson H, Weir HK (2008) Examining the association between socioeconomic status and potential human papilloma virus-associated cancers. Cancer 113(10 Suppl):2910–2918

    Article  PubMed  Google Scholar 

  24. Surveillance, Epidemiology, End Results (SEER) Program (http://www.seer.cancer.gov) SEER*Stat Database: Incidence - SEER 9 Regs Research Data, Nov 2014 Sub (1973–2012) < Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969–2013 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2015, based on the November 2014 submission

  25. Surveillance, Epidemiology, End Results (SEER) Program (http://www.seer.cancer.gov) SEER*Stat Database: Incidence - SEER 18 Regs Research Data, Nov 2014 Sub (1973–2012) < Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969–2013 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2015, based on the November 2014 submission

  26. United States Department of Agriculture (2016) Rural-urban continuum codes. Available at http://www.ers.usda.gov/data-products/rural-urban-continuum-codes.aspx. Accessed 11 Jan 2016

  27. National Cancer Institute (2016) County attributes. Available at http://seer.cancer.gov/seerstat/variables/countyattribs/ Accessed 11 Jan 2016

  28. Markowitz LE, Hariri S, Lin C, Dunne EF, Steinau M, McQuillan G, Unger ER (2013) Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003–2010. J Infect Dis 208(3):385–393. doi:10.1093/infdis/jit192

    Article  CAS  PubMed  Google Scholar 

  29. Thompson EL, Vamos CA, Vázquez-Otero C, Logan R, Griner S, Daley EM (2016) Trends and predictors of HPV vaccination among U.S. College women and men. Prev Med 86:92–98. doi:10.1016/j.ypmed.2016.02.003

    Article  CAS  PubMed  Google Scholar 

  30. Weatherspoon DJ, Chattopadhyay A, Boroumand S, Garcia I (2015) Oral cavity and oropharyngeal cancer incidence trends and disparities in the United States: 2000–2010. Cancer Epidemiol 39(4):497–504

    Article  PubMed  PubMed Central  Google Scholar 

  31. National Cancer Institute Number of Persons by Race and Hispanic Ethnicity for SEER Participants (2010 Census Data) Available at http://seer.cancer.gov/registries/data.html. Accessed 8 Mar 2016

  32. National Cancer Institute (2016) Oral Cavity and Oropharyngeal Cancer Screening (PDQ®)–Patient Version. Available at: http://www.cancer.gov/types/head-and-neck/patient/oral-screening-pdq#section/_24. Accessed 3 Aug 2016

  33. Steinau M, Saraiya M, Goodman MT et al (2014) Human papillomavirus prevalence in oropharyngeal cancer before vaccine introduction, United States. Emerg Infect Dis 20(5):822–828. doi:10.3201/eid2005.131311

    Article  PubMed  PubMed Central  Google Scholar 

  34. Curtis CR, Dorell C, Yankey D et al (2014) National human papillomavirus vaccination coverage among adolescents aged 13–17 years-National Immunization Survey--teen, United States, 2011. MMWR Suppl 63(2):61–70

    PubMed  Google Scholar 

  35. Beavis AL, Levinson KL (2016) Preventing cervical cancer in the United States: barriers and resolutions for hpv vaccination. Front Oncol 6:19. doi:10.3389/fonc.2016.00019

    Article  PubMed  PubMed Central  Google Scholar 

  36. Henry KA, Stroup AM, Warner EL, Kepka D (2016) Geographic factors and human papillomavirus (hpv) vaccination initiation among adolescent girls in the United States. Cancer Epidemiol Biomarkers Prev 25(2):309–317. doi:10.1158/1055-9965.EPI-15-0658

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ortiz M, Torres M, Muñoz L et al (2006) Oncogenic human papillomavirus (HPV) type distribution and HPV type 16 E6 variants in two Spanish population groups with different levels of HPV infection risk. J Clin Microbiol 44(4):1428–1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Muñoz N, Bosch FX, de Sanjosé S et al (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348(6):518–527

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Georgia Mueller-Luckey, MS, PhDc, for her review of the statistical methodologies utilized in this study.

Funding

Wiley D. Jenkins is supported in part by a grant from the National Cancer Institute (1P20CA192987-01A1).

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Correspondence to Wiley D. Jenkins.

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Javadi, P., Sharma, A., Zahnd, W.E. et al. Evolving disparities in the epidemiology of oral cavity and oropharyngeal cancers. Cancer Causes Control 28, 635–645 (2017). https://doi.org/10.1007/s10552-017-0889-8

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  • DOI: https://doi.org/10.1007/s10552-017-0889-8

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