Human papillomavirus (HPV) causes approximately 33,000 cancers annually in the United States, more than 12,000 of which occur in men.1 HPV, a sexually transmitted virus, is the most important cause of cervical, vaginal and vulvar cancers in women, and the virus also causes anal and oropharyngeal cancers and genital warts in both sexes.1 HPV vaccination has been recommended for females since 2006, but its uptake remains low, with only 32% of adolescent women completely vaccinated according to 2010 data.2 HPV vaccination initially became available for males in 2009 based on data indicating prevention of genital warts.3 However, uptake following this permissive recommendation was low, with only 2% of males using the vaccine nationally.4 In light of evidence indicating that HPV vaccination of males can also prevent anal cancer precursors, epidemiologic data indicating a dramatic increase in HPV-related oropharyngeal cancers and national data indicating low uptake in females, in 2011 the Advisory Committee on Immunization Practices recommended universal vaccination of males between 11 and 12 years of age, with catch-up vaccination through age 21.5 These recommendations have subsequently been endorsed by the Centers for Disease Control and Prevention5 and the American Academy of Pediatrics.6 Prior experience with HPV vaccination of females indicates that parental concerns about HPV vaccination have been an important barrier to vaccine use among adolescent women.7 Hence, this study examined HPV-related knowledge, attitudes toward HPV vaccination among low-income and minority parents of sons, and actual HPV vaccination rates among their sons in the year before the introduction of universal recommendations for HPV vaccination for males.
We interviewed parents accompanying their 11- to 17-year-old sons to preventive care or problem-related visits between December 1, 2010 and December 31, 2011. Subjects were recruited from pediatric and adolescent practices in an urban academic medical center and an affiliated community health center. The adolescent population served by the academic medical center included 60% Black, 15% White and 13% Latino patients, whereas the community health center served 70% Latino, 17% White and 2% Black patients. Approximately two thirds of patients in both settings received public insurance such as Medicaid. The settings were similar in terms of number of providers and size of patient panels. Parents/guardians who spoke English, Spanish or Haitian-Creole were eligible for inclusion. Trained research assistants reviewed practice schedules to determine eligible patients and recruited parents in the waiting areas before scheduled visits. Interviews were performed in the clinic at the time of recruitment. We sought a diverse sample of parents who self-identified as Black (including African American, Afro-Caribbean, Haitian and African participants), White or Latino. Structured interviews were conducted in English, Spanish or Haitian-Creole by native speakers. Questions were translated into Spanish or Haitian-Creole and then back-translated to ensure equivalent meanings. Subjects received a $15 gift card as compensation for their participation. This study was approved by the Boston University Medical Center’s Institutional Review Board.
Interviews were designed to elicit demographic information, HPV-related knowledge, intention to vaccinate and personal experience with HPV disease. HPV-related knowledge was assessed with a previously validated quiz in true/false format8 to which 1 additional question had been added to assess participants’ knowledge of HPV-related diseases that are more common in men: oral and anal cancers. After the knowledge assessment, participants received a short educational paragraph about HPV disease (119 words; See Appendix). Intention to vaccinate was assessed by asking parents, “If the doctor recommends the HPV vaccine for your son today, how likely are to you vaccinate him?” Parents rated their likelihood of accepting vaccination for their sons on a 4-point Likert scale from very unlikely to very likely. Electronic medical records were subsequently reviewed to determine whether vaccination occurred. Documentation of HPV vaccination in the child’s immunization record, a nursing note describing vaccine injection or a pharmaceutical order for Gardasil were considered evidence of vaccination. Approximately 2 months into the study, preliminary analyses indicated the need for more detailed questions about vaccination motivations and actions parents would take if vaccination was not offered. These questions were subsequently added and asked to 86 of our 120 participants.
Separate analyses were performed to identify correlates of (1) intention to vaccinate a son against HPV and (2) receipt of vaccination. Differences in the sociodemographic and knowledge characteristics of subjects according to HPV intent and vaccination were assessed using the χ2 test. Multivariable logistic regression was used to determine correlates of vaccine intent and receipt of vaccination. All variables found to be significant in univariate analyses were included in the multivariable models. Analyses were conducted with SAS 9.2 software (SAS Institute Inc., Cary, NC).
Demographic Information and Prior Experience With HPV-related Diseases
Participants included 120 parents (68 Black, 28 Latino, 24 White; Table 1) aged 28–74 years (mean age, 44 years); their sons’ mean age was 14 years. Seventy-seven percent of those approached agreed to participate; the most common reason for declining to interview was time constraint. Most parents were mothers, married, expressed a religious affiliation and had completed at least a high school education. Consistent with the populations served by our safety-net institutions, more than half of our patients were immigrants (58%), and 38% did not speak English as their primary language. Latino parents were more likely to be immigrants, non–English-speaking and more likely to live in a nonmarriage partnership than White parents. White parents were less likely to express a religious affiliation than Black or Latino parents. Few parents knew anyone with genital warts, oral or anal cancers, but almost 20% knew someone with cervical cancer.
Preferred Sources of Health Information and Health Literacy
Most parents identified physicians as preferred sources of general health information, although friends and mass media sources were also mentioned, with 43% of Latinos identifying media sources. However, doctors were almost exclusively identified as the trusted sources of information about vaccines. Nearly all parents (97%) reported that their doctor was their most trusted source for vaccine information, and more than 90% expressed high levels of trust in their doctors overall. Similarly, 88% preferred to receive vaccine information through speaking directly with their physicians, and 86% felt that their doctors provided sufficient vaccine-related information. Whites had higher levels of satisfaction with the information provided than Blacks or Latinos (100% versus 84% versus 79%, respectively, P = 0.04). About half of the parents also preferred written information about vaccines, but nearly one quarter of the parents stated that they had difficulty understanding written materials from their physicians, in many cases due to limited English proficiency. A minority (13%) of parents had declined vaccines in the past, most commonly influenza, H1N1 and HPV.
The majority (82%) of White, 64% of Latino and 43% of Black parents had heard of HPV vaccination before participating in the interview (Table 2). Approximately half of the parents understood that HPV is a sexually transmitted infection, that it may be asymptomatic and that it can cause abnormal Pap tests and cervical cancer. Less than one third were aware of the relationships between HPV infection and genital warts, anal cancers and oral cancers. White parents were more knowledgeable about HPV than other groups.
Intention to Accept HPV Vaccination and HPV Vaccine Receipt
Eighty-six parents (75%) intended to accept HPV vaccination for their sons if recommended by their physicians; no racial differences were noted. Multivariable logistic regression indicated that those who preferred to receive vaccine information from the internet were less likely to vaccinate. Despite high levels of vaccine intent, however, only 30% of sons received vaccination. This includes almost half (48%) of the sons of parents who expressed an intention to accept vaccination if offered, suggesting missed opportunities. Multivariable logistic regression indicated that attending the community clinic (versus the academic medical center), having a son over age 15 (compared with under age 14) and intending to accept vaccination if offered were all independently associated with vaccine receipt (Tables 3 and 4).
A subset of patients (n = 86) answered additional questions about factors that might impact their decision to vaccinate and actions they would take if they desired vaccination but the vaccine was not offered. Most parents (76%, n = 65) felt that a physician’s recommendation was an important reason to vaccinate their sons, and nearly all felt that prevention of genital warts (94%; n = 81), oral and anal cancers (95%; n = 82) and cervical cancer in the son’s future sexual partners (93%; n = 80) were also important. Approximately half (53%; n = 46) said that concerns about side effects were important when considering vaccinating their sons, and a similar number (39%; n = 34) considered their son’s opinion important; a minority (22%; n = 19) felt that a son’s fear of needles was an important consideration. Despite thinking that vaccination was important, however, few parents would take action if vaccination was not offered by their physicians. Fewer than one third would ask the doctor for the vaccine (31%; n = 27), do additional research on the vaccine (31%; n = 27), discuss the vaccine with their doctor (18%; n = 16) or make an appointment to obtain the vaccine (28%; n = 24). Most patients (88%; n = 76) stated that they would take no additional action.
This survey of low-income, minority parents accompanying their sons for clinic visits indicates that most (75%) would accept HPV vaccination for their sons if offered the vaccine by their physicians. The only factor negatively associated with intention to accept vaccination was an expressed preference to receive vaccine information via the internet. A prior study of parents of sons in North Carolina also found that parents of sons who learned about HPV vaccine via the internet perceived more barriers to HPV vaccination than those who received information from other sources.9 Possible explanations for the negative association between internet sources of information and HPV vaccine use for males are currently under study. Analysis of websites related to HPV vaccination found that 57.8% of websites were from academic or government sources and were neutral in tone,10 but analysis of YouTube videos related to HPV vaccination of females indicated that up to 50% had antivaccine content.11 Parents who prefer to do their own internet research than rely exclusively on their providers are thus likely to encounter both high-quality information and misinformation that may be difficult to distinguish from one another.12 These parents may present to providers with many questions that, in a climate of increasing time constraints, can create challenges for open and nonjudgmental patient–provider dialogue about HPV vaccination. Providers should be prepared to approach concerned parents in a nonjudgmental manner and refer them to unbiased sources of information, such as the American Academy of Pediatrics or the Centers for Disease Control and Prevention.
The need for patient–provider dialogue is underscored by the robust body of literature documenting the importance of provider recommendation in HPV vaccine uptake for girls.13–17 This may be true for boys as well: our prior research with providers indicated that physicians who were recommending HPV vaccination to males found that both parents and sons were receptive.18 In addition, only 13% of patients in our study had ever declined a vaccine recommended by their physician, and more than 90% trusted their physicians and preferred to receive vaccine information from them. Further evidence of the importance of physician recommendation in this population comes from our patients’ responses to the question of what actions they would take if not offered the vaccine. Although most patients would accept vaccination if offered by their provider, more than 90% would take no further action in the absence of provider recommendation.
Our data on vaccination receipt also supports the importance of physician behavior: during the study period, the community health center had a policy that physicians should offer HPV vaccination to all eligible males whereas the hospital-based clinic did not. We found that although parents at both sites were equally likely to intend to vaccinate, 69% of patients attending the community health center received vaccination compared with 19% of those seen in the hospital-based clinic. Other factors associated with vaccine receipt included having an older son and intending to accept vaccination. It is interesting to note that the son’s age was not associated with parental intention to vaccinate. Thus, we may again be detecting a provider effect, as substantial literature has documented provider discomfort with offering HPV vaccination to younger adolescents compared with older teens.19–21
HPV-related knowledge varied by race, with White parents being more knowledgeable than minority parents. In this survey of low-income, minority and immigrant parents, only half of the participants surveyed had heard of HPV and HPV vaccines, and fewer than one third were aware of the relationship of HPV to genital warts, oral and anal cancers—the diseases that can affect men. Similar to other studies in parents of girls,8,22 HPV-related knowledge did not impact parents’ receptiveness to vaccination.
Our study has several limitations. We studied a small, convenience sample of parents attending medical visits with their sons, and the results may not generalize to other populations or settings. Parents who agreed to participate in the study may also have held more positive views toward vaccination than those who did not wish to participate or those who did not accompany their sons to appointments. As all parents were seeking medical care for their sons, results may not generalize to parents who do not access the healthcare system. However, our study was performed in a state where everyone is required to have health insurance; in addition to the variety of private and public options, our institution also provides care to the uninsured and to undocumented immigrants, which allowed us to speak with parents who would not have had healthcare access in other settings. In addition, Vaccines For Children was covering the HPV vaccine for males during the time of our study, and most patients seen at both our study sites qualify for these subsidized vaccines; therefore, financial concerns were not important barriers in this population. We did not seek to intervene with parents. However, parents were given a short informational paragraph about HPV before asking their opinion on HPV vaccination so that they could understand the questions being asked, as is often done in studies of HPV vaccine acceptance.23–25 The possibility of influencing HPV vaccine acceptability via the educational paragraph could be considered a limitation. However, our data, consistent with other literature, indicate that knowledge does not correlate well with vaccine acceptance,22 and written information, similar to that provided in our study, does not appear to influence HPV vaccine acceptance.8
This study indicates high levels of support for HPV vaccination among parents of sons that are very similar to acceptance levels among parents of daughters. Because many parents support vaccination, we have the potential to greatly increase vaccination rates if providers follow guidelines to recommend HPV vaccination for all adolescents, both boys and girls. Novel, individually tailored methods of facilitating guideline uptake by providers are warranted, such as those based on academic detailing,26–29 performance improvement, continuing medical education30 or practice facilitation.31 If improving provider adherence to HPV vaccine guidelines raises vaccination rates, we have the potential to see population-wide reductions in HPV disease.32,33
The wording of the educational paragraph was as follows: HPV is a virus. HPV is spread from one person to another by contact with the skin of the vagina or penis. People usually catch HPV from having sex, but they can catch it from touching someone else’s genitals, even if they do not have sex. Condoms can decrease the chance that a person catches HPV, but they are not 100% effective. There is a vaccine to prevent HPV. HPV can’t be cured with antibiotics because it is a virus. Sometimes after someone catches HPV, it never goes away. If this happens, it can cause problems. HPV can cause abnormal PAP smears, warts on the penis or vagina and cancer of the cervix (uterus or womb), anus and mouth.
1. Morbidity and Mortality Weekly Report.. Human papillomavirus-associated cancers—United States, 2004–2008. MMWR Morb Mortal Wkly Rep.. 2012;61:258–261
2. National Iimmunization Survey—Teen.. National and state vaccination coverage among adolescents aged 13 through 17 years—United States, 2010. MMWR Morb Mortal Wkly Rep.. 2011;60:1117–1123
3. Morbidity and Mortality Weekly Report. . FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep.. 2010;59:630–632
4. Reiter PL, McRee AL, Kadis JA, et al. HPV vaccine and adolescent males. Vaccine. 2011;29:5595–5602
5. Advisory Committee on Immunization Practices. . Recommendations on the use of quadrivalent human papillomavirus vaccine in males—Advisory Committee on Immunization Practices (ACIP), 2011. MMWR Morb Mortal Wkly Rep. 2011;60:1705–1708
6. American Academy of Pediatrics. . Recommended immunization schedule for persons aged 7 through 18 years—United States, 2012. 2012 Available at: http://aapredbook.aappublications.org/resources/IZSchedule7-18yrs.pdf
. Accessed May 02, 2012
7. Brewer NT, Fazekas KI. Predictors of HPV vaccine acceptability: a theory-informed, systematic review. Prev Med. 2007;45:107–114
8. Dempsey AF, Zimet GD, Davis RL, et al. Factors that are associated with parental acceptance of human papillomavirus vaccines: a randomized intervention study of written information about HPV. Pediatrics. 2006;117:1486–1493
9. McRee AL, Reiter PL, Brewer NT. Parents’ internet use for information about HPV vaccine. Vaccine. 2012;30:3757–3762
10. Madden K, Nan X, Briones R, et al. Sorting through search results: a content analysis of HPV vaccine information online. Vaccine. 2012;30:3741–3746
11. Keelan J, Pavri-Garcia V, Tomlinson G, et al. YouTube as a source of information on immunization: a content analysis. JAMA. 2007;298:2482–2484
12. Betsch C, Sachse K. Dr. Jekyll or Mr. Hyde? (How) the Internet influences vaccination decisions: Recent evidence and tentative guidelines for online vaccine communication. Vaccine. 2012;30:3723–3726
13. Dorell C, Yankey D, Strasser S. Parent-reported reasons for nonreceipt of recommended adolescent vaccinations, national immunization survey: teen, 2009. Clin Pediatr (Phila).. 2011;50:1116–1124
14. Bartlett JA, Peterson JA. The uptake of Human Papillomavirus (HPV) vaccine among adolescent females in the United States: a review of the literature. J Sch Nurs. 2011;27:434–446
15. Dorell CG, Yankey D, Santibanez TA, et al. Human papillomavirus vaccination series initiation and completion, 2008–2009. Pediatrics.. 2011;128:830–839
16. Litton AG, Desmond RA, Gilliland J, et al. Factors associated with intention to vaccinate a daughter against HPV: a statewide survey in Alabama. J Pediatr Adolesc Gynecol. 2011;24:166–171
17. Guerry SL, De Rosa CJ, Markowitz LE, et al. Human papillomavirus vaccine initiation among adolescent girls in high-risk communities. Vaccine. 2011;29:2235–2241
18. Perkins RB, Clark JA. Providers’ attitudes toward human papillomavirus vaccination in young men: challenges for implementation of 2011 Recommendations. Am J Mens Health.. 2012;6:320–323
19. Vadaparampil ST, Kahn JA, Salmon D, et al. Missed clinical opportunities: provider recommendations for HPV vaccination for 11-12 year old girls are limited. Vaccine. 2011;29:8634–8641
20. Kahn JA, Cooper HP, Vadaparampil ST, et al. Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians. Cancer Epidemiol Biomarkers Prev. 2009;18:2325–2332
21. McCave EL. Influential factors in HPV vaccination uptake among providers in four states. J Community Health. 2010;35:645–652
22. Christian WJ, Christian A, Hopenhayn C. Acceptance of the HPV vaccine for adolescent girls: analysis of state-added questions from the BRFSS. J Adolesc Health. 2009;44:437–445
23. Constantine NA, Jerman P. Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis. J Adolesc Health. 2007;40:108–115
24. Mays RM, Sturm LA, Zimet GD. Parental perspectives on vaccinating children against sexually transmitted infections. Soc Sci Med. 2004;58:1405–1413
25. Olshen E, Woods ER, Austin SB, et al. Parental acceptance of the human papillomavirus vaccine. J Adolesc Health. 2005;37:248–251
26. Gorin SS, Ashford AR, Lantigua R, et al. Effectiveness of academic detailing on breast cancer screening among primary care physicians in an underserved community. J Am Board Fam Med. 2006;19:110–121
27. Gorin SS, Ashford AR, Lantigua R, et al. Implementing academic detailing for breast cancer screening in underserved communities. Implement Sci. 2007;2:43
28. Litvin CB, Ornstein SM, Wessell AM, et al. Adoption of a clinical decision support system to promote judicious use of antibiotics for acute respiratory infections in primary care. Int J Med Inform. 2012;81:521–526
29. Sheffer MA, Baker TB, Fraser DL, et al. Fax referrals, academic detailing, and tobacco quitline use: a randomized trial. Am J Prev Med. 2012;42:21–28
30. Mullikin EA, Ales MW, Cho J, et al. Sharing collaborative designs of tobacco cessation performance improvement CME projects. J Contin Educ Health Prof. 2011;31(suppl 1):S37–S49
31. Nagykaldi Z, Mold JW, Robinson A, et al. Practice facilitators and practice-based research networks. J Am Board Fam Med. 2006;19:506–510
32. Brotherton JM, Fridman M, May CL, et al. Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study. Lancet. 2011;377:2085–2092
33. Read TR, Hocking JS, Chen MY, et al. The near disappearance of genital warts in young women 4 years after commencing a national human papillomavirus (HPV) vaccination programme. Sex Transm Infect. 2011;87:544–547