Differences in Oral Sexual Behaviors by Gender, Age, and Race Explain Observed Differences in Prevalence of Oral Human Papillomavirus Infection

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Abstract

Purpose

This study explores whether gender, age and race differences in oral sexual behavior account for the demographic distribution of oral human papillomavirus infection (HPV) and HPV-positive oropharyngeal cancer (HPV-OSCC)

Methods

This analysis included 2,116 men and 2,140 women from NHANES (2009–10) who answered a behavioral questionnaire and provided an oral-rinse sample for HPV detection. Weighted prevalence estimates and prevalence ratios (PR) were calculated for sexual behaviors and oral HPV infection by gender, age-cohort (20–29, 30–44, 45–59, 60–69), and race, and contrasted with incidence rate ratios (IRR) of OSCC from SEER 2009. Multivariate logistic regression was used to evaluate predictors of oral sexual behavior and oral HPV16 infection.

Results

Differences in oral sexual behavior were observed by gender, age-cohort and race. Most men (85.4%) and women (83.2%) had ever performed oral sex, but men had more lifetime oral and vaginal sexual partners and higher oral HPV16 prevalence than women (each p<0.001). 60–69 year olds (yo) were less likely than 45–59 or 30–44 (yo) to have performed oral sex (72.7%, 84.8%, and 90.3%, p<0.001), although oral HPV16 prevalence was similar. Prevalence ratios (PR) of ever oral sex in men vs. women (PR = 1.03), and 45–59 vs. 30–44 year-old men (PR = 0.96) were modest relative to ratios for oral HPV16 infection (PRs = 1.3–6.8) and OSCC (IRR = 4.7–8.1). In multivariate analysis, gender, age-cohort, and race were significant predictors of oral sexual behavior. Oral sexual behavior was the primary predictor of oral HPV16 infection; once this behavior was adjusted for, age-cohort and race were no longer associated with oral HPV16.

Conclusion

There are differences in oral sexual behaviors when considering gender, age-cohort and race which explain observed epidemiologic differences in oral HPV16 infection across these groups.

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Most cited references 15

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Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States.

Anil Chaturvedi, Eric Engels, William F Anderson … (2008)

To investigate the impact of human papillomavirus (HPV) on the epidemiology of oral squamous cell carcinomas (OSCCs) in the United States, we assessed differences in patient characteristics, incidence, and survival between potentially HPV-related and HPV-unrelated OSCC sites. Data from nine Surveillance, Epidemiology, and End Results program registries (1973 to 2004) were used to classify OSCCs by anatomic site as potentially HPV-related (n = 17,625) or HPV-unrelated (n = 28,144). Joinpoint regression and age-period-cohort models were used to assess incidence trends. Life-table analyses were used to compare 2-year overall survival for HPV-related and HPV-unrelated OSCCs. HPV-related OSCCs were diagnosed at younger ages than HPV-unrelated OSCCs (mean ages at diagnosis, 61.0 and 63.8 years, respectively; P < .001). Incidence increased significantly for HPV-related OSCC from 1973 to 2004 (annual percentage change [APC] = 0.80; P < .001), particularly among white men and at younger ages. By contrast, incidence for HPV-unrelated OSCC was stable through 1982 (APC = 0.82; P = .186) and declined significantly during 1983 to 2004 (APC = -1.85; P < .001). When treated with radiation, improvements in 2-year survival across calendar periods were more pronounced for HPV-related OSCCs (absolute increase in survival from 1973 through 1982 to 1993 through 2004 for localized, regional, and distant stages = 9.9%, 23.1%, and 18.6%, respectively) than HPV-unrelated OSCCs (5.6%, 3.1%, and 9.9%, respectively). During 1993 to 2004, for all stages treated with radiation, patients with HPV-related OSCCs had significantly higher survival rates than those with HPV-unrelated OSCCs. The proportion of OSCCs that are potentially HPV-related increased in the United States from 1973 to 2004, perhaps as a result of changing sexual behaviors. Recent improvements in survival with radiotherapy may be due in part to a shift in the etiology of OSCCs.

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Annual Report to the Nation on the Status of Cancer, 1975–2005, Featuring Trends in Lung Cancer, Tobacco Use, and Tobacco Control

Ahmedin Jemal, Michael Thun, Lynn A. G. Ries … (2008)

Background The American Cancer Society, the Centers for Disease Control and Prevention (CDC), the National Cancer Institute (NCI), and the North American Association of Central Cancer Registries (NAACCR) collaborate annually to provide updated information on cancer occurrence and trends in the United States. This year’s report includes trends in lung cancer incidence and death rates, tobacco use, and tobacco control by state of residence. Methods Information on invasive cancers was obtained from the NCI, CDC, and NAACCR and information on mortality from the CDC's National Center for Health Statistics. Annual percentage changes in the age-standardized incidence and death rates (2000 US population standard) for all cancers combined and for the top 15 cancers were estimated by joinpoint analysis of long-term (1975–2005) trends and by least squares linear regression of short-term (1996–2005) trends. All statistical tests were two-sided. Results Both incidence and death rates from all cancers combined decreased statistically significantly (P < .05) in men and women overall and in most racial and ethnic populations. These decreases were driven largely by declines in both incidence and death rates for the three most common cancers in men (lung, colorectum, and prostate) and for two of the three leading cancers in women (breast and colorectum), combined with a leveling off of lung cancer death rates in women. Although the national trend in female lung cancer death rates has stabilized since 2003, after increasing for several decades, there is prominent state and regional variation. Lung cancer incidence and/or death rates among women increased in 18 states, 16 of them in the South or Midwest, where, on average, the prevalence of smoking was higher and the annual percentage decrease in current smoking among adult women was lower than in the West and Northeast. California was the only state with decreasing lung cancer incidence and death rates in women. Conclusions Although the decrease in overall cancer incidence and death rates is encouraging, large state and regional differences in lung cancer trends among women underscore the need to maintain and strengthen many state tobacco control programs.

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Reduced Prevalence of Oral Human Papillomavirus (HPV) 4 Years after Bivalent HPV Vaccination in a Randomized Clinical Trial in Costa Rica

Rolando Herrero, Wim Quint, Allan Hildesheim … (2013)

Background Human papillomavirus (HPV) infection, particularly with type 16, causes a growing fraction of oropharyngeal cancers, whose incidence is increasing, mainly in developed countries. In a double-blind controlled trial conducted to investigate vaccine efficacy (VE) of the bivalent HPV 16/18 vaccine against cervical infections and lesions, we estimated VE against prevalent oral HPV infections 4 years after vaccination. Methods and Findings A total of 7,466 women 18–25 years old were randomized (1∶1) to receive the HPV16/18 vaccine or hepatitis A vaccine as control. At the final blinded 4-year study visit, 5,840 participants provided oral specimens (91·9% of eligible women) to evaluate VE against oral infections. Our primary analysis evaluated prevalent oral HPV infection among all vaccinated women with oral and cervical HPV results. Corresponding VE against prevalent cervical HPV16/18 infection was calculated for comparison. Oral prevalence of identifiable mucosal HPV was relatively low (1·7%). Approximately four years after vaccination, there were 15 prevalent HPV16/18 infections in the control group and one in the vaccine group, for an estimated VE of 93·3% (95% CI = 63% to 100%). Corresponding efficacy against prevalent cervical HPV16/18 infection for the same cohort at the same visit was 72·0% (95% CI = 63% to 79%) (p versus oral VE = 0·04). There was no statistically significant protection against other oral HPV infections, though power was limited for these analyses. Conclusions HPV prevalence four years after vaccination with the ASO4-adjuvanted HPV16/18 vaccine was much lower among women in the vaccine arm compared to the control arm, suggesting that the vaccine affords strong protection against oral HPV16/18 infection, with potentially important implications for prevention of increasingly common HPV-associated oropharyngeal cancer. ClinicalTrials.gov, Registry number NCT00128661

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Author and article information

Contributors

Xuefeng Liu: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2014

Publication date (Electronic): 24 January 2014

Volume: 9

Issue: 1

Electronic Location Identifier: e86023

Affiliations

[1 ]Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America

[2 ]Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins Hospital, Baltimore, Maryland, United States of America

[3 ]Greenebaum Cancer Center, University of Maryland, Baltimore, Maryland, United States of America

[4 ]Department of Health, Behavior and Society, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America

[5 ]Department of Health Policy and Management, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America

[6 ]Hopkins Center for Health Disparities Solutions, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United States of America

[7 ]Milton J. Dance Jr. Head and Neck Cancer Center, Greater Baltimore Medical Center, Baltimore, Maryland, United States of America

Georgetown University, United States of America

Author notes

* E-mail: gdsouza@ 123456jhsph.edu (GD); cfakhry@ 123456jhmi.edu (CF)

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: GD KC CF. Analyzed the data: GD. Wrote the paper: GD KC JB RT CF.

Article

Publisher ID: PONE-D-13-40133

DOI: 10.1371/journal.pone.0086023

PMC ID: 3901667

PubMed ID: 24475067

SO-VID: 8903aefc-a11b-407a-8f6d-9bf61b211913

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 26 September 2013

Date accepted : 4 December 2013

Page count

Pages: 12

Funding

The authors have no support or funding to report.

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Differences in Oral Sexual Behaviors by Gender, Age, and Race Explain Observed Differences in Prevalence of Oral Human Papillomavirus Infection

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Abstract

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Conclusion

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PLOS Climate

Most cited references 15

Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States.

Annual Report to the Nation on the Status of Cancer, 1975–2005, Featuring Trends in Lung Cancer, Tobacco Use, and Tobacco Control

Reduced Prevalence of Oral Human Papillomavirus (HPV) 4 Years after Bivalent HPV Vaccination in a Randomized Clinical Trial in Costa Rica

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