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Figure.
Prevalence Estimates and Ratios for Vaccine-Type and Nonvaccine-Type Oral HPV Infections Among Unvaccinated Men and Women Aged 18-59 Years, NHANES, 2009-2016
Prevalence Estimates and Ratios for Vaccine-Type and Nonvaccine-Type Oral HPV Infections Among Unvaccinated Men and Women Aged 18-59 Years, NHANES, 2009-2016

Human papillomavirus (HPV) prevalence data shown across 4 National Health and Nutrition Examination Survey (NHANES) cycles (2009-2010, 2011-2012, 2013-2014, and 2015-2016). HPV-16/-18/-6/-11 were considered vaccine types. Prevalence ratios were adjusted for age, race/ethnicity, education-level, marital status, smoking, and lifetime number of same- and opposite-sex oral sex partners. Prevalence trends across cycles were assessed using integer scores and quantified through odds ratios and 95% confidence intervals (CIs). Individuals with missing covariate values for education (n = 8), marital status (n = 5), or smoking (n = 895) were imputed the modal value. Individuals with missing lifetime (n = 1606) number of oral sex partners were imputed the sex-specific mean. All analyses accounted for the complex sample design, including the use of sample weights adjusted for unit nonresponse and the combination of 4 cycles. Weights were further poststratified to the age × sex × race distribution of the cycle-specific US population to account for nonparticipation in the sexual behavioral questionnaire or oral HPV components. Error bars indicate 95% CIs.

Table.  
Characteristics of the US Population Aged 18-59 Years, NHANES, 2009-2016a
Characteristics of the US Population Aged 18-59 Years, NHANES, 2009-2016a
1.
Petrosky  E, Bocchini  JA  Jr, Hariri  S,  et al; Centers for Disease Control and Prevention.  Use of 9-valent human papillomavirus (HPV) vaccine: updated HPV vaccination recommendations of the advisory committee on immunization practices.  MMWR Morb Mortal Wkly Rep. 2015;64(11):300-304.PubMedGoogle Scholar
2.
Chaturvedi  AK, Graubard  BI, Broutian  T,  et al.  Effect of prophylactic human papillomavirus (HPV) vaccination on oral HPV infections among young adults in the United States.  J Clin Oncol. 2017;36(3):262-267. doi:10.1200/JCO.2017.75.0141PubMedGoogle ScholarCrossref
3.
Malagón  T, Laurie  C, Franco  EL.  Human papillomavirus vaccination and the role of herd effects in future cancer control planning: a review.  Expert Rev Vaccines. 2018;17(5):395-409. doi:10.1080/14760584.2018.1471986PubMedGoogle ScholarCrossref
4.
Gillison  ML, Broutian  T, Pickard  RK,  et al.  Prevalence of oral HPV infection in the United States, 2009-2010.  JAMA. 2012;307(7):693-703. doi:10.1001/jama.2012.101PubMedGoogle ScholarCrossref
5.
Drolet  M, Bénard  É, Boily  MC,  et al.  Population-level impact and herd effects following human papillomavirus vaccination programmes.  Lancet Infect Dis. 2015;15(5):565-580. doi:10.1016/S1473-3099(14)71073-4PubMedGoogle ScholarCrossref
6.
Oliver  SE, Unger  ER, Lewis  R,  et al.  Prevalence of human papillomavirus among females after vaccine introduction—National Health and Nutrition Examination Survey, United States, 2003-2014.  J Infect Dis. 2017;216(5):594-603. doi:10.1093/infdis/jix244PubMedGoogle ScholarCrossref
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Research Letter
September 10, 2019

Prevalence of Oral HPV Infection in Unvaccinated Men and Women in the United States, 2009-2016

Author Affiliations
  • 1Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, Maryland
  • 2The Ohio State University, Columbus
  • 3MD Anderson Cancer Center, Houston, Texas
  • 4Information Management Services Inc, Calverton, Maryland
JAMA. 2019;322(10):977-979. doi:10.1001/jama.2019.10508

Prophylactic human papillomavirus (HPV) vaccination has been recommended for routine use in US females since 2006 and males since 2011 for the prevention of anogenital HPV infections.1 Although studies have demonstrated high vaccine efficacy in reducing prevalence of oral HPV infection,2 prevention of oral HPV infections and oropharyngeal cancers is not a vaccine indication because of lack of randomized trials. Also lacking are surveillance studies for herd protection against oral HPV infections.3

We investigated evidence for herd protection against oral HPV infections in unvaccinated US men and women aged 18 to 59 years via temporal (2009-2016) comparisons of oral HPV prevalence for 4 vaccine types (HPV-16/-18/-6/-11) and 33 nonvaccine types.

Methods

This study was conducted across 4 cycles of the National Health and Nutrition Examination Survey (NHANES), a cross-sectional, stratified, multistage probability sample of the civilian US population. Response rates for the examination component were in 68.5% in 2009-2010, 69.5% in 2011-2012, 68.5% in 2013-2014, and 58.7% in 2015-2016. Procedures for data collection and HPV testing have been described.4 DNA from oral rinses was evaluated for presence of HPV using PGMY09/11 polymerase chain reaction and linear array genotyping for 37 types.4

Sex-stratified analyses were conducted in unvaccinated individuals. All analyses accounted for the complex sample design, including the use of NHANES sample weights adjusted for unit nonresponse and the combination of 4 NHANES cycles. Weights were further poststratified to the age × sex × race distribution of the cycle-specific US population to account for nonparticipation in the sexual behavioral questionnaire or oral HPV components. Prevalence comparisons across cycles were conducted through multivariable logistic regression, with adjustment for age, self-reported race/ethnicity, education level, marital status, smoking, and lifetime number of same- and opposite-sex oral sex partners. Heterogeneity across age subgroups was evaluated through cycle × age interaction.

Analyses were conducted in SAS-callable SUDAAN version 11.0.1 (RTI International). A 2-sided P < .05 was considered statistically significant. Participants provided written informed consent. The study was approved by ethics committees of NHANES and The Ohio State University.

Results

During 2009-2016 (n = 13 676, representing 174 333 402 individuals in the US population aged 18-59 years), HPV vaccination rates increased from 0% to 5.8% in men and from 7.3% to 15.1% in women. Demographic and behavioral characteristics were unchanged in men and women (Table).

Vaccine-type oral HPV prevalence declined from 2.7% during 2009-2010 to 1.6% during 2015-2016 in unvaccinated men aged 18 to 59 years (Figure) (adjusted prevalence ratio [PR], 0.63 [95% CI, 0.44-0.90]; P= .009 for trend). This decline was not heterogeneous by age (P = .41 for interaction). Prevalence of nonvaccine-type oral HPV infections remained unchanged in unvaccinated men aged 18 to 59 years (8.6% in 2009-2010 vs 8.4% in 2015-2016; adjusted PR, 1.02 [95% CI, 0.79-1.33]; P = .66 for trend).

In unvaccinated women aged 18 to 59 years, oral HPV prevalence remained unchanged for vaccine types (0.6% in 2009-2010 vs 0.5% in 2015-2016; adjusted PR, 0.96 [95% CI, 0.23-3.98]; P = .79 for trend) and for nonvaccine types (2.6% in 2009-2010 vs 3.3% in 2015-2016; adjusted PR, 1.29 [95% CI, 0.71-2.35]; P = .58 for trend) (Figure).

Discussion

Vaccine-type oral HPV prevalence declined by 37% between 2009-2010 and 2015-2016 in a sample of unvaccinated US men aged 18 to 59 years, suggesting herd protection against oral HPV infections. Nonvaccine-type oral HPV prevalence remained unchanged. Herd protection likely arises from increased levels of female HPV vaccination in the US population. These results are consistent with modeling and surveillance studies of herd protection against genital HPV infections in unvaccinated US females during 2004-2014.5,6 The lack of herd protection toward oral HPV infections in unvaccinated women could reflect low statistical power due to low prevalence in women.

A limitation of this study is the use of self-reported HPV vaccination status. Also, there was low statistical power to investigate herd protection stratified by age subgroups.

The estimated herd protection should be incorporated into evaluations of the cost-effectiveness of HPV vaccination of men older than 26 years. Vaccine trials of oral HPV incidence and persistence in men should inflate sample sizes to account for herd protection.

Section Editor: Jody W. Zylke, MD, Deputy Editor.
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Article Information

Accepted for Publication: June 27, 2019.

Corresponding Author: Maura L. Gillison, MD, PhD, Division of Cancer Medicine, Department of Thoracic Head and Neck Medical Oncology, MD Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030 (mgillison@mdanderson.org).

Author Contributions: Dr Chaturvedi had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Gillison, Chaturvedi.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Gillison, Chaturvedi, Graubard, Xiao.

Critical revision of the manuscript for important intellectual content: Gillison, Chaturvedi, Graubard, Broutian, Pickard, Kahle.

Statistical analysis: Gillison, Chaturvedi, Graubard, Kahle.

Obtained funding: Gillison, Chaturvedi.

Administrative, technical, or material support: Gillison, Broutian, Xiao, Pickard.

Supervision: Gillison.

Conflict of Interest Disclosures: Dr Gillison reported consulting for Amgen, Aspyrian, AstraZeneca, Bayer, Bristol-Myers Squibb, Celgene, EMD Serono, Genocea, GlaxoSmithKline, Lilly, NewLink, Merck, Roche, and TRN Oncology; receiving grants from the National Institute of Dental and Craniofacial Research (NIDCR); and receiving personal fees from Roche Diagnostics. No other disclosures were reported.

Funding/Support: This study was supported in part by NIDCR grant R01DE023175 and the Intramural Research Program of the National Cancer Institute. Dr Gillison is a Cancer Prevention and Research Institute of Texas (CPRIT) Scholar.

Role of the Funder/Sponsor: The study funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

References
1.
Petrosky  E, Bocchini  JA  Jr, Hariri  S,  et al; Centers for Disease Control and Prevention.  Use of 9-valent human papillomavirus (HPV) vaccine: updated HPV vaccination recommendations of the advisory committee on immunization practices.  MMWR Morb Mortal Wkly Rep. 2015;64(11):300-304.PubMedGoogle Scholar
2.
Chaturvedi  AK, Graubard  BI, Broutian  T,  et al.  Effect of prophylactic human papillomavirus (HPV) vaccination on oral HPV infections among young adults in the United States.  J Clin Oncol. 2017;36(3):262-267. doi:10.1200/JCO.2017.75.0141PubMedGoogle ScholarCrossref
3.
Malagón  T, Laurie  C, Franco  EL.  Human papillomavirus vaccination and the role of herd effects in future cancer control planning: a review.  Expert Rev Vaccines. 2018;17(5):395-409. doi:10.1080/14760584.2018.1471986PubMedGoogle ScholarCrossref
4.
Gillison  ML, Broutian  T, Pickard  RK,  et al.  Prevalence of oral HPV infection in the United States, 2009-2010.  JAMA. 2012;307(7):693-703. doi:10.1001/jama.2012.101PubMedGoogle ScholarCrossref
5.
Drolet  M, Bénard  É, Boily  MC,  et al.  Population-level impact and herd effects following human papillomavirus vaccination programmes.  Lancet Infect Dis. 2015;15(5):565-580. doi:10.1016/S1473-3099(14)71073-4PubMedGoogle ScholarCrossref
6.
Oliver  SE, Unger  ER, Lewis  R,  et al.  Prevalence of human papillomavirus among females after vaccine introduction—National Health and Nutrition Examination Survey, United States, 2003-2014.  J Infect Dis. 2017;216(5):594-603. doi:10.1093/infdis/jix244PubMedGoogle ScholarCrossref
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