Abstract
Introduction
Special needs population have barriers accessing healthcare, higher incidence of sexual assaults and lower sexual education. Due to the above this study was conducted- 1) To assess the current prevalence of oral HPV infection among individuals with SHCN (special health care needs) as compared to the general population and 2) To compare the prevalence of HPV vaccination in SHCN individuals (within the recommended age groups) to general population.
Methods
This data was obtained from NHANES 2013-14 and included 665 individuals with special needs. Weighted prevalence estimates and prevalence ratios (PR) were calculated for oral HPV infection by gender, age (18–59 years), race, smoking history, economic status, and sexual behavior. Prevalence rates were calculated for HPV vaccination.
Results
Oral HPV was detected in 9% (7.1–11.5; p = 0.05) of special needs adults. High-risk HPV genotypes prevalence was also higher among adults with special needs [5.56% (3.9–7.9) vs 3.87% (2.7–5.4)]. The HPV vaccination rates among 9–26 years special needs females (33.5% vs 37%) and males aged 9–21 years (16.7% vs 21.2%) with special needs was lower than non-special needs individuals.
Conclusion
There is higher burden of oral HPV infection among adults with special needs compared to general population. Contrastingly, lower vaccination rates were observed among them within the recommended age groups. Further studies are required to determine the barriers to HPV vaccination among individuals with special needs.
Keywords: Humanpapilloma virus, Vaccination, Special needs, Oral HPV
Highlights
-
•
The prevalence of Oral HPV infection is higher among the adults with special health care needs.
-
•
Individuals with Special health care needs have lower uptake of HPV vaccination with in the recommended age groups, compared to the general population.
-
•
Males are more likely to have high-risk Oral HPV infection and lower vaccination rates compared to females.
1. Introduction
Human Papillomavirus (HPV) has been well established as the most common cause for cervical, Oropharyngeal cancers (OPC), and a subset of anogenital cancers [[1], [2], [3]]. Studies have established a causal relation between OPC and the presence of HPV [[4], [5], [6]]. The HPV- 16 strain is detectable in almost 90% of HPV related OPC cases [[7], [8], [9]]. The incidence of HPV related cancers has increased worldwide in the last decade.
Developing HPV related OPC has predictably shown a strong association to sexual activity [10]. Lifetime number of sexual partners and oral sex activities were strongly associated with HPV cancers [6,11]. Among those who have one to five sexual partners, the odds of HPV-OPC increase by two times, and five times among those who have six or more partners [5]. The incidence of HPV related OPC among younger age groups, men, and non-Hispanic whites have increased due to changes in sexual practices [10,12].
The American Academy of Pediatric Dentistry (AAPD) defines special health care needs (SHCN) as “any physical, developmental, mental, sensory, behavioral, cognitive, or emotional impairment or limiting condition that requires medical management, health care intervention, and/or use of specialized services or programs. The condition may be congenital, developmental, or acquired through disease, trauma, or environmental cause and may impose limitations in performing daily self-maintenance activities or substantial limitations in a major life activity” [13]. Studies have indicated higher level of sexual abuse and victimization among individuals with SHCN [[14], [15], [16], [17], [18], [19]]. Individuals with SHCN have low sexual esteem, acceptance, and knowledge of sex compared to non-special needs individuals [20,21]. The combination of lower sexual knowledge, higher frequency of sexual assaults, and a difficulty to access health care facilities [22,23] places the individuals with SHCN at a higher risk of acquiring sexually transmitted diseases.
Recent studies have shown a decrease in HPV prevalence among general population and the increasing utilization of HPV vaccinations among adolescents and younger adults [24,25]. These studies have shown the efficacy of HPV vaccination in preventing HPV transmission. There is a higher risk of sexual assaults and lower sexual knowledge, but there are no nationally representative studies in the US that indicate the current prevalence of oral HPV and uptake of HPV vaccine among individual with SHCN. We undertook this study to 1) estimate the prevalence of Oral HPV infection among adults with SHCN and 2) to compare the HPV vaccine (within the recommended age groups) uptake among the individuals with SHCN to the general population.
2. Materials and methods
2.1. Study design and HPV genotyping
In this study, we used the publicly available National Health and Nutrition Examination Survey (NHANES) 2013-14 dataset for the analysis. NHANES is conducted among a nationally representative non-institutionalized civilian US population. The demographics, vaccination history, and sexual behavior questionnaires were recorded. Oral HPV rinse samples were collected at the examination site by NHANES examiners. Purified DNA samples were analyzed for 37 types of HPV via Roche Linear Array HPV Genotyping Test and the Roche Linear Array Detection Kit. This test helps to determine the presence of 14 high-risk HPV genotypes and 23 low-risk HPV genotypes.
2.2. Statistical analysis
The population prevalence values were reported as weighted counts and percentages for the presence of estimated oral HPV infection among a subsample of individuals aged 18–59 years who have SHCN. Sample weights were used to account for the complex survey design. A chi-square test was used to measure the association of selected demographic and presence of oral HPV infection. The presence of oral HPV infection was defined by the variable ORXHPV that was based on the results from the Roche Linear Array HPV Genotyping Test. The disability survey recorded whether the individual had serious hearing, vision (even with corrective lens), walking, dressing, and/or bathing difficulties. A positive response for any of the above variables was coded as having a physical disability. A positive response for having serious difficulty in concentrating, remembering, or making decisions because of a physical, mental, or emotional condition was coded as having a intellectual disability. Positive answers to both questions were coded as having both (physical & intellectual) disabilities. Multivariable logistic regression was used to determine the prevalence ratios of oral HPV infection. All analyses were conducted using STATA 13.0 version. Differences with P values of <0.05 were considered statistically significant.
3. Results
Table 1 describes the demographic features of the population with SCHN and without SCHN based on the presence of Oral HPV infection, aged 18–59 years. About 9% of the people, aged 18–59 years, have oral HPV infection. This is significantly different (p = 0.04) from the population who do not have any special needs (6.7%). The prevalence of HPV was significantly higher among males compared to women in both the categories (p = 0.008 & <0.0001). The prevalence was significantly higher among African Americans compared to all the other races among SCHN (p = 0.009). HPV prevalence was higher among current smokers compared to those who never smoked and individuals who had smoked in the past (p = 0.017). Socio-economic status did not show any association to oral HPV infection. As oral HPV is associated with sexual behavior, it showed higher prevalence among those who have had any form of sexual intercourse compared to those who have never partaken (p = 0.01).
Table 1.
Prevalence of Oral Human Papillomavirus (HPV) Infection Among Men and Women with special health care needs (SHCN) and non-SHCN, aged 18–59 years, National Health and Nutrition Examination Survey, 2013–14.
| Among SHCN |
Non-SCHN |
|||||
|---|---|---|---|---|---|---|
| Weighted Percentage | (95% CI) | P-value | Weighted Percentage | (95% CI) | P-value | |
| Total | 9.07 | (7.1–11.5) | 6.7 | (5.1–8.8) | 0.04 | |
| Age | ||||||
| 18–27 | 7.71 | (4.3–13.3) | 0.44 | 5.26 | (3.2–8.4) | 0.06 |
| 28–39 | 7.27 | (4.2–12.1) | 6.28 | (4.5–8.6) | ||
| 40–49 | 12.78 | (6.5–23.5) | 6.42 | (4.4–9.2) | ||
| 50–59 | 8.36 | (4.7–14.2) | 9.67 | (6.2–14.6) | ||
| Gender | ||||||
| male | 13.45 | (9.4–18.9) | 0.008 | 10.76 | (8.1–14.2) | <0.0001 |
| female | 5.08 | (3.0–8.8) | 2.75 | (1.8–4.1) | ||
| Type of disability | ||||||
| Physical | 9.21 | (5.4–15.2) | 0.88 | – | – | |
| Intellectual | 8.07 | (4.6–13.6) | – | – | ||
| Both | 9.93 | (5.5–17) | – | – | ||
| Race | ||||||
| Non-Hispanic white | 8.11 | (5.7–12) | .009 | 7.44 | [5.2–10.5) | 0.08 |
| Non-Hispanic black | 17.46 | (10.2–28.5) | 7.52 | (5.8–9.6) | ||
| Hispanic | 7.84 | (5.5–11) | 5.02 | (3.2–7.5) | ||
| Other | 2.77 | (0.8–8.8) | 4.44 | (2.7–7.1) | ||
| smoking | ||||||
| Never smoker | 6.06 | (3.6–10.3) | 0.017 | 4.59 | (3.2–4.4) | <0.0001 |
| Past smoker | 6.70 | (3.7–12) | 8.35 | (5.9–11.7) | ||
| Current smoker | 13.88 | (9.7–20.4) | 12.18 | (8.2–17.8) | ||
| Ever had oral, vaginal or anal sex | ||||||
| Yes | 8.56 | (6.3–11.8) | 0.012 | 6.91 | (5.1–9.2) | 0.09 |
| No | 0.92 | (.0.1–7.4) | 2.24 | (0.5–8.8) | ||
| Income poverty ratio | ||||||
| <=1 | 9.61 | (5.7–16.6) | 0.89 | 7.81 | (5.9–10.2) | 0.80 |
| >=1 to <=2 | 9.52 | (4.6–20) | 6.32 | (3.5–10.9) | ||
| >=2 to <=3 | 9.85 | (3.2–26.8) | 6.36 | (3.7–10.7) | ||
| >=3 | 7.10 | (3.3–14.6) | 6.65 | (4.5–9.5) | ||
Table 2 shows the unadjusted and the adjusted prevalence ratios of oral HPV presence and associated factors among SCHN individuals. The prevalence of oral HPV infection was significantly higher among men (adjusted PR = 2.74, p = 0.02) compared to women. African Americans had higher odds of oral HPV compared to non-Hispanic Whites (APR = 2.7, p = 0.05). Hispanics had higher adjusted prevalence ratio (APR = 1.4) and other races had a lower prevalence ratio (0.44), but were not significant. Smoking behavior had a significant association to oral HPV. Subjects who had sexual encounters with one to four partners (APR = 4.4, p = 0.22) had higher prevalence ratios compared to those who have never had sexual encounters. Subjects who had more than five lifetime partners had adjusted prevalence ratios of 11.01 (p = 0.02). Those who ever performed oral sex had higher prevalence ratio (PR = 1.42) compared to those who never performed oral sex, but was not significant (P = 0.6).
Table 2.
Prevalence ratios of HPV prevalence among special needs population in the US- 2013-14.
| Unadjusted prevalence ratio of Oral HPV infection | p- value | Adjusted Prevalence ratios | p-value | |
|---|---|---|---|---|
| Sex | ||||
| Female | 1.00 | 1.00 | ||
| Male | 2.90 | 0.01 | 2.74 | 0.021 |
| Race | ||||
| Non-Hispanic White | 1.00 | 1.00 | ||
| African American Descent | 2.39 | 0.02 | 2.72 | 0.05 |
| Hispanic | 0.96 | 0.89 | 1.39 | 0.30 |
| Others | 0.32 | 0.07 | 0.44 | 0.26 |
| Smoking status | ||||
| Never Smoker | 1.00 | 1.00 | ||
| Former Smoker | 1.11 | 0.76 | 0.87 | 0.751 |
| Current smoker | 2.49 | 0.02 | 2.48 | 0.023 |
| Sexual activity | ||||
| No. of lifetime sex partners | ||||
| Never had sex | 1.00 | 1.00 | ||
| 1 to 2 partner | 3.40 | 0.30 | 4.35 | 0.23 |
| 3–4 partners | 3.66 | 0.311 | 4.47 | 0.22 |
| 5 or more partners | 13.60 | 0.021 | 11.01 | 0.019 |
| Ever performed oral sex | ||||
| No | 1.00 | Omitted | ||
| Yes | 1.42 | 0.608 | ||
Table 3 describes the prevalence of high-risk HPV presence among the special needs population. High-risk oral HPV genotypes were found in 5.5% of the subjects compared to 3.8% of the non-special needs population (p = 0.15). Males and females with special needs had a higher prevalence of high-risk HPV. Males with SHCN had a 7.7% prevalence of high-risk oral HPV compared to the 6.6% prevalence of the general population, but was not significant. There was a significantly higher prevalence of high-risk HPV among special needs women (3.6%) compared to the 1.5% prevalence among the general population (p = 0.004).
Table 3.
High risk HPV oral infection prevalence.
| Special needs status |
|||
|---|---|---|---|
| Yes- % (CI) | No (CI) | P-value | |
| Females | 3.69% (1.8–7.1) | 1.15% (0.8–1.6) | 0.004 |
| Males | 7.74% (4.1–14.1) | 6.62% (4.5–9.5) | 0.68 |
| Total | 5.56% (3.9–7.9) | 3.87% (2.7–5.4) | 0.16 |
Table 4 represents the HPV vaccination rates among the nine to 26 year old population. The analysis was completed among this age group that was recommended by the Advisory Committee on Immunization Practices (ACIP) and the CDC for HPV vaccinations. Among females with SHCN, 32% were vaccinations compared to 37% of the general population. Among males with SHCN, 16% had been vaccinated compared to 21% in the general population. The vaccination rates are slightly lesser among the special needs population but the findings are not statistically significant.
Table 4.
HPV vaccination rates among special needs population. Females between 9 years and 26 years and males 9–21 Years.
| Gender | Special needs status |
||
|---|---|---|---|
| Yes (CI) | No (CI) | P-value | |
| Females | 33.55% (22.9–46) | 37.18% (31.7–42.9) | 0.50 |
| Males | 16.7% (10.1–26.3) | 21.25% (18.6–24) | 0.32 |
4. Discussion
The overall prevalence of oral HPV infection among adults with SHCN is about 9% (7.1–11.5), which is significantly greater than the general population (6.7%; p = 0.05). This approximates to 2.5 million Americans with SHCN. We found a higher prevalence in men than in women. The gender difference is consistent with the prevalence of oral HPV among people without SHCN [26]. Prevalence of high-risk HPV genotypes was also higher among adults with SHCN.
People with SHCN may have lower sexual self-esteem, partners, knowledge, and acceptance19−20. Although sexual encounters may be less among people with disabilities, previous studies have highlighted their vulnerability to physical and sexual assaults 13−18. This increased vulnerability supports the need for more proactive vaccination among people with SHCN. Previous studies have established the role of oral sex and oral HPV. Our study results show that those who performed oral sex on a partner had higher prevalence of oral HPV (8.7%) compared to those who did not (6.2%, p = 0.6).
Smoking and intensity of smoking are associated with HPV infection. Smokers have higher HPV viral load compared to non-smokers. Smoking also increases the risk of viral persistence, which is a key factor for malignancy development [27,28]. Smoking can cause immunosuppression by decreasing the number of Langerhans cells and helper T lymphocytes, which suggests the independent role of smoking towards HPV related neoplasia [[29], [30], [31]]. Consistent with other previous studies [10,12], our study results show that current and past smokers have higher chances of contracting oral HPV. Previous studies conducted that among the general population, the use of marijuana and alcohol as predictors for oral HPV infection was inconsistent [11,12,32]. Our study also did not show any significance for the above among the population with SHCN (results not shown).
HPV vaccination, under optimistic conditions, has shown to be highly cost effective. Inclusion of males up to 21 years, women and gay men up to 26 years in vaccination programs have showed better QALY gain [[33], [34], [35], [36]]. The Advisory Committee on Immunization Practices (ACIP) recommends routine HPV vaccination for 11 and 12 year old children. HPV vaccination can be started as early as nine years of age. As a catch-up vaccination recommendation, males up to 21 years and females up to 26 years of age should be vaccinated. Immunocompromised individuals and children with sexual abuse history can be vaccinated up to the age of 26 years according to this recommendation [37]. In our analysis, we have determined that HPV vaccination rate among the individuals with SHCN is lower than in the general population. Females aged 9–26 years and males aged 9–21 years with special needs had a vaccination rate of 32% (vs 37%) in females and 16% (vs 21%) in males. Previous studies have also indicated the lower vaccination rates; however, these studies were limited to small sample size and geography [[38], [39], [40], [41]].
There are a few limitations in our study. The study did not include the individuals with SHCN living in institutional settings. Sexual behaviors and sexuality are difficult to capture and biased due to selective misreporting. Special needs/disability and vaccination history are self-reported and may result in bias. The self-reporting bias may be less due to the randomization of the sample in NHANES. The cross-sectional nature of this study cannot establish causal relation.
To our knowledge, this is the first study of oral HPV prevalence and vaccination among individuals with SHCN. Given that incidents of sexual assault and violence are higher among people with SHCN, the vaccination rates need to be increased among them. Through this study, we have determined that vaccination rates, although not significant, are lower among individuals with special needs. This tips the balance towards more HPV incidence among individuals with SHCN. The vaccination rates are far off from the healthy people 2020 target of 80% among 13–15 year old individuals. Our study bridges the gap between the low vaccination rates and higher prevalence of Oral HPV among SHCN adults. There is a need for development of programs aimed to provide recommended HPV vaccination to individuals with SHCN.
5. Conclusion
Our study provides the first national estimate of prevalence of oral HPV infection among adults with SHCN. Compared to the general population, individuals with SHCN have higher prevalence of oral HPV (6.7% vs 9%; p = 0.05). Vaccination rates among the ACIP recommended age groups are also lower among the individuals with SHCN. Overall, our analysis implicates a need to provide higher access to and to further study the barriers of HPV vaccination among individuals with SHCN.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.pvr.2019.100182.
Appendix A. Supplementary data
The following is the Supplementary data to this article:
References
- 1.Walboomers J.M.M., Jacobs M.V., Manos M.M. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 1999;189:12–19. doi: 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F. [DOI] [PubMed] [Google Scholar]
- 2.zur Hausen H. Human papillomaviruses in the pathogenesis of anogenital cancer. Virology. 1991;184:9–13. doi: 10.1016/0042-6822(91)90816-t. [DOI] [PubMed] [Google Scholar]
- 3.Chaturvedi A.K., Anderson W.F., Lortet-Tieulent J. 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. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Gillison M.L., Koch W.M., Capone R.B. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J. Natl. Cancer Inst. 2000;92:709–720. doi: 10.1093/jnci/92.9.709. [DOI] [PubMed] [Google Scholar]
- 5.Marur S., D'Souza G., Westra W.H. HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol. 2010;11:781–789. doi: 10.1016/S1470-2045(10)70017-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.D'Souza G., Kreimer A.R., Viscidi R. Case–control study of human papillomavirus and oropharyngeal cancer. N. Engl. J. Med. 2007;356:1944–1956. doi: 10.1056/NEJMoa065497. [DOI] [PubMed] [Google Scholar]
- 7.Gillison M.L. Human papillomavirus-related diseases: oropharynx cancers and potential implications for adolescent HPV vaccination. J. Adolesc. Health. 2008;43:S52–S60. doi: 10.1016/j.jadohealth.2008.07.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ramqvist T., Dalianis T. Oropharyngeal cancer epidemic and human papillomavirus. Emerg. Infect. Dis. 2010;16:1671–1677. doi: 10.3201/eid1611.100452. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Marklund L., Hammarstedt L. Impact of HPV in oropharyngeal cancer. J. Oncol. 2011;2011:509036. doi: 10.1155/2011/509036. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Smith E.M., Ritchie J.M., Summersgill K.F. Age, sexual behavior and human papillomavirus infection in oral cavity and oropharyngeal cancers. Int. J. Cancer. 2004;108:766–772. doi: 10.1002/ijc.11633. [DOI] [PubMed] [Google Scholar]
- 11.D'Souza G., Agrawal Y., Halpern J. Oral sexual behaviors associated with prevalent oral human papillomavirus infection. J. Infect. Dis. 2009;199:1263–1269. doi: 10.1086/597755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Gillison M.L., Broutian T., Pickard R.K.L. Prevalence of oral HPV infection in the United States, 2009-2010. JAMA. 2012;307:693. doi: 10.1001/jama.2012.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.American Academy of Pediatric Dentistry Definition of special health care needs. Pediatr. Dent. 2016;38:16. [PubMed] [Google Scholar]
- 14.Martin S.L., Ray N., Sotres-Alvarez D. Physical and sexual assault of women with disabilities. Violence Against Women. 2006;12:823–837. doi: 10.1177/1077801206292672. [DOI] [PubMed] [Google Scholar]
- 15.Casteel C., Martin S.L., Smith J.B. National study of physical and sexual assault among women with disabilities. Inj. Prev. 2008;14:87–90. doi: 10.1136/ip.2007.016451. [DOI] [PubMed] [Google Scholar]
- 16.Krnjacki L., Emerson E., Llewellyn G. Prevalence and risk of violence against people with and without disabilities: findings from an Australian population-based study. Aust. N. Z. J. Public Health. 2016;40:16–21. doi: 10.1111/1753-6405.12498. [DOI] [PubMed] [Google Scholar]
- 17.Rand M.R., Harrell E., Statisticians B. 2007. Bureau of Justice Statistics Special Report Crime against People with Disabilities. 2009. [Google Scholar]
- 18.Jones L., Bellis M.A., Wood S. Prevalence and risk of violence against children with disabilities: a systematic review and meta-analysis of observational studies. Lancet. 2012;380:899–907. doi: 10.1016/S0140-6736(12)60692-8. [DOI] [PubMed] [Google Scholar]
- 19.Hughes K., Bellis M.A., Jones L. Prevalence and risk of violence against adults with disabilities: a systematic review and meta-analysis of observational studies. Lancet. 2012;379:1621–1629. doi: 10.1016/S0140-6736(11)61851-5. [DOI] [PubMed] [Google Scholar]
- 20.Vansteenwegen A., Jans I., Revell A.T. Sexual experience of women with a physical disability: a comparative study. Sex. Disabil. 2003;21:283–290. [Google Scholar]
- 21.Cheng M.M., Udry J.R. Sexual experiences of adolescents with low cognitive abilities in the U.S. J. Dev. Phys. Disabil. 2005;17:155–172. [Google Scholar]
- 22.Khalid I., Chandrupatla S.G., Kaye E. Dental sealant prevalence among children with special health care needs: national health and nutrition examination survey (NHANES) 2013 to 2014. Pediatr. Dent. 2019;41:186–190. [PubMed] [Google Scholar]
- 23.Iezzoni L.I. Eliminating health and health care disparities among the growing population of people with disabilities. Health Aff. 2011;30:1947–1954. doi: 10.1377/hlthaff.2011.0613. [DOI] [PubMed] [Google Scholar]
- 24.Bauer H.M., Wright G., Chow J. Evidence of human papillomavirus vaccine effectiveness in reducing genital warts: an analysis of California public family planning administrative claims data, 2007-2010. Am. J. Public Health. 2012;102:833–835. doi: 10.2105/AJPH.2011.300465. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Markowitz L.E., Hariri S., Lin C. 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. 2013;208:385–393. doi: 10.1093/infdis/jit192. [DOI] [PubMed] [Google Scholar]
- 26.Sonawane K., Suk R., Chiao E.Y. Oral human papillomavirus infection: differences in prevalence between sexes and concordance with genital human papillomavirus infection, NHANES 2011 to 2014. Ann. Intern. Med. 2017;167:714. doi: 10.7326/M17-1363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Kero K, Rautava J, Syrjänen K, et al. Smoking Increases Oral HPV Persistence Among Men: 7-year Follow-Up Study. [DOI] [PubMed]
- 28.Giuliano A.R., Sedjo R.L., Roe D.J. Clearance of oncogenic human papillomavirus (HPV) infection: effect of smoking (United States) Cancer Causes Control. 2002;13:839–846. doi: 10.1023/a:1020668232219. [DOI] [PubMed] [Google Scholar]
- 29.Syrjänen K., Shabalova I., Petrovichev N. Smoking is an independent risk factor for oncogenic human papillomavirus (HPV) infections but not for high-grade CIN. Eur. J. Epidemiol. 2007;22:723–735. doi: 10.1007/s10654-007-9180-8. [DOI] [PubMed] [Google Scholar]
- 30.Campo M. In: Papillomavirus Research: from Natural History to Vaccines and beyond. Saveria, editor. Horizon Scientific Press; 2006. [Google Scholar]
- 31.Trottier H., Franco E.L. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24 doi: 10.1016/j.vaccine.2005.09.054. S4–S15. [DOI] [PubMed] [Google Scholar]
- 32.Ortiz A.P., González D., Ramos J. Association of marijuana use with oral HPV infection and periodontitis among Hispanic adults: implications for oral cancer prevention. J. Periodontol. 2018;89:540–548. doi: 10.1002/JPER.17-0372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Kim J.J., Goldie S.J. Cost effectiveness analysis of including boys in a human papillomavirus vaccination programme in the United States. BMJ. 2009;339:b3884. doi: 10.1136/bmj.b3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Kim J.J. Targeted human papillomavirus vaccination of men who have sex with men in the USA: a cost-effectiveness modelling analysis. Lancet Infect. Dis. 2010;10:845–852. doi: 10.1016/S1473-3099(10)70219-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Graham D.M., Isaranuwatchai W., Habbous S. A cost-effectiveness analysis of human papillomavirus vaccination of boys for the prevention of oropharyngeal cancer. Cancer. 2015;121:1785–1792. doi: 10.1002/cncr.29111. [DOI] [PubMed] [Google Scholar]
- 36.Elbasha E.H., Dasbach E.J. Impact of vaccinating boys and men against HPV in the United States. Vaccine. 2010;28:6858–6867. doi: 10.1016/j.vaccine.2010.08.030. [DOI] [PubMed] [Google Scholar]
- 37.Meites E., Kempe A., Markowitz L.E. Use of a 2-dose schedule for human papillomavirus vaccination — updated recommendations of the advisory committee on immunization practices. MMWR Morb. Mortal. Wkly. Rep. 2016;65:1405–1408. doi: 10.15585/mmwr.mm6549a5. [DOI] [PubMed] [Google Scholar]
- 38.Rowe M., Pritt A.L., Stratton A.J. HPV vaccination among females with mental and physical limitation. Marshall J. Med. 2017;3 [Google Scholar]
- 39.McRee A.L., Maslow G.R., Reiter P.L. Receipt of recommended adolescent vaccines among youth with special health care needs. Clin. Pediatr. (Phila). 2017;56:451–460. doi: 10.1177/0009922816661330. [DOI] [PubMed] [Google Scholar]
- 40.O'Neill J., Newall F., Antolovich G. The uptake of adolescent vaccinations through the School Immunisation Program in specialist schools in Victoria, Australia. Vaccine. 2019;37:272–279. doi: 10.1016/j.vaccine.2018.11.034. [DOI] [PubMed] [Google Scholar]
- 41.O'Neill J., Elia S., Perrett K.P. Human papillomavirus vaccine uptake in adolescents with developmental disabilities. J. Intellect. Dev. Disabil. 2019:98–102. [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.