Barriers to Human Papillomavirus Vaccination Among US Adolescents

Abstract

IMPORTANCE

Since licensure of the human papillomavirus (HPV) vaccine in 2006, HPV vaccine coverage among US adolescents has increased but remains low compared with other recommended vaccines.

OBJECTIVE

To systematically review the literature on barriers to HPV vaccination among US adolescents to inform future efforts to increase HPV vaccine coverage.

EVIDENCE REVIEW

We searched PubMed and previous review articles to identify original research articles describing barriers to HPV vaccine initiation and completion among US adolescents. Only articles reporting data collected in 2009 or later were included. Findings from 55 relevant articles were summarized by target populations: health care professionals, parents, underserved and disadvantaged populations, and males.

FINDINGS

Health care professionals cited financial concerns and parental attitudes and concerns as barriers to providing the HPV vaccine to patients. Parents often reported needing more information before vaccinating their children. Concerns about the vaccine’s effect on sexual behavior, low perceived risk of HPV infection, social influences, irregular preventive care, and vaccine cost were also identified as potential barriers among parents. Some parents of sons reported not vaccinating their sons because of the perceived lack of direct benefit. Parents consistently cited health care professional recommendations as one of the most important factors in their decision to vaccinate their children.

CONCLUSIONS AND RELEVANCE

Continued efforts are needed to ensure that health care professionals and parents understand the importance of vaccinating adolescents before they become sexually active. Health care professionals may benefit from guidance on communicating HPV recommendations to patients and parents. Further efforts are also needed to reduce missed opportunities for HPV vaccination when adolescents interface with the health care system. Efforts to increase uptake should take into account the specific needs of subgroups within the population. Efforts that address system-level barriers to vaccination may help to increase overall HPV vaccine uptake.

Human papillomavirus (HPV) infection is common, with prevalence peaking among young adults.^1,2 Most HPV infections clear within 1 to 2 years, but persistent infections can progress to precancers or cancer. Nearly all cervical cancers and many vulvar, vaginal, penile, anal, and oropharyngeal cancers are caused by persistent infection with oncogenic or high-risk HPV types.^3,4 HPV-16 and HPV-18 are responsible for 70% of cervical cancers and most noncervical HPV-associated cancers.⁵ A recent study⁶ found that more than 40% of females aged 14 to 59 years were HPV positive, and nearly 30% of infections were with high-risk types. Approximately 26 200 cancers per year are attributable to HPV (17 400 among females and 8800 among males), many of which could be preventable with appropriate use of current or future vaccines.³

Two vaccines, a bivalent (HPV2) and a quadrivalent (HPV4) vaccine, are available to protect against HPV-16 and HPV-18.⁷ In addition, HPV4 protects against HPV-6 and HPV-11, which are responsible for 90% of genital warts.⁷ Both vaccines are administered as a 3-dose series. The Advisory Committee on Immunization Practices (ACIP) recommends routine vaccination of girls aged 11 to 12 years with either HPV2 or HPV4.⁸ The series can begin at age 9 years and is also recommended for females aged 13 to 26 years who have not initiated or completed the series. For boys aged 11 to 12 years, the ACIP recommends routine vaccination with HPV4.⁹ Vaccination with HPV4 for males can begin at age 9 years and is recommended for all males through age 21 years who have not initiated or completed the series.HPV4 vaccination is also recommended for men who have sex with men or who are immunocompromised through age 26 years. Ideally, the vaccine should be administered before potential exposure to HPV through sexual contact.^8,9

Healthy People 2020 objectives include increasing HPV vaccine series completion for females aged 13 to 15 years to 80% by the year 2020.¹⁰ Since vaccine licensure in 2006, HPV vaccine coverage among US females has increased but remains low compared with other recommended adolescent vaccines. Data from the 2011 National Immunization Survey (NIS)–Teen indicated that 53.0% of US girls aged 13 to 17 years had received at least 1 dose of the HPV vaccine and 34.8% had completed the 3-dose series.¹¹ Healthy People 2020 objectives do not address HPV vaccination among males, but vaccination of males is recommended to protect both males and their future sexual partners from HPV-related diseases.⁹ In 2011, 8.3% of US males aged 13 to 17 years had initiated the HPV vaccine series.¹¹ This article systematically reviews the literature on barriers to HPV vaccination among US adolescents, both males and females, to inform future efforts to increase HPV vaccine coverage.

Methods

We searched PubMed using the following search string: human papillomavirus OR HPV OR human papillomavirus AND (vaccine OR vaccination OR vaccinate). We limited the search to original research articles published in English from January 1, 2009, through December 31, 2012. One coauthor (D.M.H.) reviewed the titles and abstracts of all articles returned in the search and retrieved the full texts of potentially relevant articles to make a final determination of their relevance. The bibliographies of selected articles were scanned for additional relevant studies. Only articles that reported data collected in 2009 or later and addressed barriers to HPV vaccination among US adolescents aged 11 to 17 years were included. Articles that solely reported data collected before 2009 were excluded in an effort to focus on current barriers. Articles that focused on barriers to adult HPV vaccination or vaccination outside the United States were also excluded. One coauthor (D.M.H.) coded each article based on the target populations (eg, health care professionals, parents, and underserved populations) and topics (eg, completion and system-level barriers) addressed in the article. The coauthors (V.B., K.B.R., M.W., N.L., S.S.) then each abstracted and synthesized all findings related to a specific target population or topic. A second coauthor (D.M.H.) reviewed each section independently for accuracy. Disagreements were resolved by discussions among all the authors.

Results

The search in PubMed returned 2460 articles, of which 55 met the inclusion criteria. Findings are summarized in the Box and in the sections below by target populations: health care professionals, parents, underserved and disadvantaged populations, and males. The last section of the Results describes barriers to HPV vaccine series completion. Many articles reported quantitative data, but findings based solely on qualitative data are indicated as such within each section.

Box. Summary of Key Barriers to HPV Vaccination Among US Adolescentsa.

Health Care Professionals

Parents’ attitudes and concerns regarding HPV vaccination^12,16–18

Financial concerns^13,15,18

Knowledge gaps^17,19

Inadequate insurance coverage and reimbursement^14,18

Preference for vaccinating older vs younger adolescents⁵⁰

Preference for vaccinating girls vs boys¹⁷

Parents

Not receiving a health care professional’s recommendation for the HPV vaccineb

Need more information about the HPV vaccinec

Belief that one’s child is too young to get vaccinated for HPVd

Concerns about vaccine adverse effects, safety, and newnesse

Cost of the HPV vaccinef

Concerns about finding a clinic that offers the HPV vaccine²⁰

Underserved and Disadvantaged Populations

Limited knowledge about HPV and the HPV vaccine^40,52

Lack of insurance coverage^22,39

Not Receiving a Health Care Professional’s Recommendation for the HPV Vaccine⁴¹

Distrust of the health care system¹³

Cultural factors¹³

Immigration status¹³

Males

Lack of perceived benefit or need to vaccinate males^17,26,35,40

Lack of awareness that vaccine can be given to males^35,44,45

Not receiving a health care professional’s recommendation for the HPV vaccine^17,28

Cost of the vaccine⁴⁴

Barriers Specific to Completion of the 3-Dose HPV Vaccine Series

Lack of insurance coverage^47–49

Lack of a regular medical home⁴⁷

Lack of a health care professional recommendation³³

Little contact with the medical system³⁷

Being unaware of or forgetting about the need for additional doses⁴⁶

Abbreviation: HPV, human papillomavirus.

^a Review limited to original research studies reporting data collected in 2009 or later.

^b References 13,21–25,27–31,33,34,36,38,41,43

^c References 13,20–22,24,28,31,32,34,35,40,43

^d References 22,26,28,34,35,38,40,50,51

^e References 13,20,26,35,38,40,42

^f References 13,26,31,35,38

Health Care Professionals

Ten articles^{12–19,50,51} (18.2%) addressed barriers among health care professional to vaccinating their patients. Two studies^17,19 identified continuing knowledge gaps. For example, some studies^17,19 indicated low knowledge among health care professionals about the relationship between HPV infection and genital warts or the relationship between HPV and noncervical cancers. Two qualitative studies (N = 60 and 184 respondents) indicated that, when offering the vaccine to patients, health care professionals either offered little information about the vaccine, treating it like other recommended adolescent vaccines, or provided detailed information about the risks and benefits of the vaccine, highlighting it as optional.^50,51 In 3 qualitative studies (N = 31–184 respondents), health care professionals reported using a risk-based approach according to the perceived level of the patient’s sexual activity or household characteristics⁵¹ and expressed a preference for vaccinating older vs younger adolescents⁵⁰ and girls vs boys.¹⁷

Three other qualitative studies^13,15,18 (N = 8–112 respondents) found that the most common barriers for health care professionals related to financial concerns. These concerns included cost to parents,¹³ cost to health care professionals,¹³ and inadequate insurance coverage and reimbursement.¹⁸ A study¹⁴ of Florida Medicaid providers (N = 428) found that those participating in the Vaccines For Children (VFC) program were less likely to cite cost of stocking the vaccine and lack of adequate or timely reimbursement as barriers compared with non-VFC providers.

Several qualitative studies^12,16–18 (N = 21–112 respondents) found that health care professionals thought the decision to vaccinate was beyond their control and cited parental attitudes and concerns as a barrier. Concerns about safety and efficacy were rarely identified as barriers.^16,18 One qualitative study¹⁶ (N = 34) found that some health care professionals did not view HPV as an important health threat, whereas others cited time constraints and forgetting to offer the vaccine as additional barriers.

Parents and Caregivers

Most studies^{11,13,20–43,50,51,53–59} (63.6%) addressed the barriers experienced by parents and caregivers. Studies indicated that most parents were aware of the vaccine,^31,39,54 but parents reported needing more information before vaccinating their children and cited lack of knowledge as a barrier.^* In one qualitative study (N = 32),²⁹ parents reported that exposure to media and advertisement increased their knowledge and awareness of the vaccine. Some parents reported concerns about adverse effects, safety, and newness of the vaccine, but results were mixed as to whether such concerns hindered vaccine uptake.^†

Across studies, few parents (1%–18%)expressed concern about the effect of vaccination on their child’s sexual behavior.^{13,20,26,35,38,40,42} In a qualitative study³¹ among African Americans (n = 19) and Haitian immigrants (n = 51), parents reported concern about vaccination being interpreted as condoning sexual activity but also appreciation for the protection that the vaccine could provide. In another qualitative study (N = 44),⁴⁰ parents reported concern about discussing the vaccine’s purpose with their children, which might necessitate discussion about sexual activity. In 2 other qualitative studies (N = 32–38),^29,43 parents indicated an interest in protecting their children before they became sexually active, and in many studies,^{21–24,29,34,50,55} perceived risk of HPV-related disease was a predictor of vaccine acceptance and series initiation.

Young age of the child was a common reason for refusing or delaying HPV vaccination,^‡ and older girls were more likely to be vaccinated than younger girls.^{11,20,22,23,28,30,34,56} Alternatively, in 2 studies (N = 403 and 700), age did not predict intention to vaccinate.^54,58 Vaccine acceptance was also associated with the belief that vaccinating one’s child was in accordance with social norms in 2 studies (N = 78 and 325).^23,32 Furthermore, parents’ history of seeking preventive care for themselves or their children was positively associated with HPV vaccine uptake.^{26,28,34,56,58} Results were mixed as to whether parents’ previous HPV-related experiences (eg, prior abnormal Papanicolaou test, colposcopy, or cervical cancer) was correlated with acceptance of the HPV vaccine for one’s child. One quantitative study⁵⁴ (N = 421) found that mothers with a history of HPV-related experiences were more likely to intend to vaccinate their daughters. Another study⁵⁹ (N = 150) found similar results among non-Hispanic white and black mothers but not Hispanic mothers. Alternatively, 3 other quantitative studies (N = 200–501) found no association between parents’ HPV-related experiences and HPV vaccine acceptance or uptake.^25,26,33 Two studies (N = 70 and 400) indicated certain religious affiliations were associated with opposition to or nonreceipt of the HPV vaccine.^31,57 However, in 2 other studies (N = 200 and 403), religiosity did not predict vaccine acceptance.^25,54

Receiving a physician’s recommendation or discussing the HPV vaccine with a physician was associated with vaccine acceptance and initiation in numerous studies,^§ and parents frequently cited not having a physician’s recommendation as the reason for not vaccinating their child.^{22,28,33,34,43} Furthermore, preventive care visits,^22,56 increased contact with the medical system,³⁷ and receipt of other recommended vaccines^28,37 were associated with vaccine initiation in several studies. In contrast, only one study²⁶ (N = 322) found that a physician’s consultation or recommendation did not influence vaccine uptake.

Findings were mixed regarding the cost of the HPV vaccine, with some identifying cost as a barrier^{13,26,33,35,38} and only one study (N = 403) indicating cost was not a barrier.⁵⁴ A study²⁰ among low-income, uninsured, ethnic minority, and immigrant women (N = 490) found that concerns about finding a clinic that offered the vaccine created additional barriers.

Underserved and Disadvantaged Populations

More than one-fourth (27.3%) of the studies ^‖ addressed barriers among historically underserved populations (eg, minorities, those with a lower household income, and those without health insurance). Differences in HPV vaccine acceptance, initiation, and series completion have been noted across racial/ethnic groups.^{11,22,28,34,52} Recent data from NIS-Teen indicate that black and Hispanic girls are less likely to complete the HPV vaccine series compared with whites^11,22,52 and may be less likely to receive a recommendation for the vaccine from a health care professional.⁴¹

Most reported barriers to vaccination are similar across racial/ethnic groups but may affect some groups more than others. For example, one study⁴⁴ (N = 309) that compared HPV vaccination among non-Hispanic white vs Hispanic girls found that the effects of age at first intercourse, mother-daughter communication about values related to sex, and social norms on vaccination status differed by ethnicity. In addition, a qualitative study⁴⁰ among ethnically diverse black women (N = 44) found limited knowledge and confusion about HPV and the vaccine. Cultural differences can create unique barriers for specific subpopulations. For example, a qualitative study¹³ of 12 Hispanic immigrants identified immigration status, cultural factors, and distrust of health care facilities as barriers, and a study³¹ of 70 African American and Haitian immigrant mothers found distinct barriers between the 2 groups.

Studies^11,52 also indicate a possible association between HPV vaccination and both household income and health insurance coverage. Data from NIS-Teen indicate that the highest rates of HPV vaccine initiation are among adolescents from households below the federal poverty level. Another study²⁸ (N = 751) found that household income predicted vaccination initiation in boys only, with boys from homes with an annual household income of $50 000 or more being less likely to be vaccinated than those with a lower income. With regard to insurance status, data from NIS-Teen and one other study (N = 479)^22,39 indicated that girls with public health insurance were more likely to initiate HPV vaccination compared with girls with private or no insurance coverage. In contrast, 2 studies found no association between vaccination (N = 700)⁵⁸ or intent to vaccinate⁵⁹ (N = 150) and insurance status.

One study⁶⁰ (N = 50) described the unique barriers to vaccinating adolescents detained in juvenile justice facilities. Barriers included short length of stay, general lack of education regarding HPV vaccination, parental consent requirements, lack of adequate staff to administer the vaccine, staff reluctance to administer vaccine, lack of refrigerator storage space, patient fears, and cost.

Males

Eleven studies^# (20.0%) examined barriers to male HPV vaccination. The NIS-Teen data indicate that uptake of the HPV vaccine is much lower among male adolescents than female adolescents.¹¹ Similar to females, rates of vaccine series initiation are higher among black and Hispanic males compared with white males and higher among males below the poverty level compared with males living at or above the poverty level.¹¹ Unlike females, HPV vaccine initiation does not vary with age among male adolescents,¹¹ and one qualitative study⁴⁰ among black women (N = 44) found mothers were more accepting of vaccinating sons at a young age than daughters. As mentioned previously, health care professionals may be more likely to recommend the vaccine to females than males.^17,28 Furthermore, one qualitative study¹⁷ (N = 31) found that some health care professionals did not think vaccinating males was worth the cost or effort, were unaware of serious HPV-related disease in males, or thought that parents would not be interested in vaccinating their sons. Results from other studies indicated that parents were unclear about the need to vaccinate males,^26,40 perceived the consequences of HPV infection as less severe for males,³⁵ or were unaware that the vaccine could be given to males.^35,61,62 One mixed-methods study⁴⁶ among adolescent males (N = 86) found that participants did not think they were sufficiently informed to make a decision about vaccination on their own. Parents and sons were more accepting of the vaccine if they perceived greater benefits for their sons or their sons’ future female partners,^45,61,62 if their family or friends had positive views about the vaccine,^46,62 or if the vaccine was recommended by a physician.^36,46 Cost was also cited as a potential barrier to vaccinating males in one study (N = 406).⁶¹

Vaccine Series Completion

Ten studies^{11,22,33,37,47–49,63–65} (18.2%) addressed barriers to completion of the 3-dose HPV vaccine series. Studies indicated that rates of HPV vaccine series completion tended to be lower among black^{11,22,33,37,47,48,64} and Hispanic^22,33 girls and lower among those who lacked insurance coverage,^48,64,66 a regular medical home,⁴⁸ or a health care professional recommendation.³³

One small study⁶³ (N = 22) found some participants were unaware of or forgot the need for additional vaccine doses or were too busy for a return clinic visit. Another study³⁷ (N = 7702) found that increased contact with the medical system was associated with completion of the HPV vaccine series. Two retrospective cohort studies (N = 4117 and 271 976) found that younger adolescents were more likely to complete the series than older adolescents^49,65 and that completion rates varied by physician specialty, with higher rates of completion rates in pediatric departments⁴⁹ and obstetrics-gynecology departments.⁶⁵

Discussion

Since vaccine licensure, HPV vaccine coverage among US adolescents has increased but remains low compared with coverage for other vaccines recommended for adolescents (eg, 70.5% coverage for meningococcal conjugate and 78.2% coverage for tetanus, diphtheria, and acellular pertussis in 2011).¹¹ This systematic review summarizes the literature on barriers to HPV vaccination among this age group and will inform future efforts to increase vaccine uptake. The literature emphasizes the importance of receiving a recommendation for HPV vaccination from a health care professional. Most health care professionals offer the HPV vaccine and support adolescent HPV vaccination. However, health care professionals tend to be less likely to recommend the vaccine to younger patients and often recommend the vaccine based on perceived risk. Continued efforts are needed to ensure that health care professionals understand the importance of vaccinating adolescents before they become sexually active. Health care professionals may benefit from guidance on communicating HPV vaccine recommendations to patients and parents. In addition, although health care professionals may be finding ways to overcome financial challenges, the barriers related to vaccine cost should not be ignored. Some have suggested expanding or increasing health care professional participation in the VFC programas potential strategies for reducing financial barriers.^14,67

Parents are also critical to successful provision of the HPV vaccine. Parents want to protect their children from the harmful effects of HPV infection and are generally accepting of the vaccine. However, many report needing more information before vaccinating their children. Providing adequate, clear, and accessible information to parents about HPV infection, vaccine safety, adverse effects, and the appropriate age for vaccination may be one way health care professionals can reduce concerns and misconceptions about the vaccine. Communication efforts should also address logistical concerns (eg, vaccine financing).

Beliefs that only sexually active adolescents need the vaccine may lead parents to decline or delay HPV vaccination. Parents may underestimate their adolescents’ sexual experience and potentially miss an opportunity for prevention.⁶⁸ Vaccinating at ages 11 or 12 years targets adolescents at an age when most are not yet sexually active and also when the immune response to vaccination is greater than it is at older ages.⁶⁹

Communication efforts are also needed to highlight the benefits and importance of male vaccination. Studying the barriers to vaccinating high-risk male adolescents may pose challenges because of the sensitive nature of some of the risk factors for HPV infection in male adolescents.

Targeted efforts are also needed to increase vaccine uptake and completion among traditionally underserved populations. For example, HPV vaccine initiation is higher among blacks than whites, but rates of series completion are lower for blacks than whites.¹¹ This disparity is concerning given that cervical cancer incidence and mortality are higher among black women than white women.⁷⁰ Series completion is lower among females living below the poverty level compared with females living at or above poverty level.¹¹ Information about the HPV vaccine should be distributed strategically to best reach underserved populations and provided in ways that are culturally sensitive, tailored to the target audience, and written at an appropriate reading level. School-based vaccination programs and health policy initiatives may further help to increase vaccine uptake and reduce disparities.⁴⁸

The need for 3 doses of the HPV vaccine creates additional challenges for parents.⁷¹ Adolescents generally encounter the health care system less frequently than any other age group⁷² and often seek only acute care or physical examinations for athletics.⁷³ Providing opportunities for HPV vaccination in less traditional health care settings (eg, pharmacies and retail health clinics) and using reminder and recall systems may facilitate vaccine series completion.⁷⁴ Innovative, communications-based interventions, including text message reminders and electronic medical records, may also increase series completion. However, such programs should take into account the specific populations they serve and consider that certain methods may not be effective for reaching underserved groups.^63,75

Although studies typically identify barriers to HPV vaccination via reports from individual parents and health care professionals, many of the barriers identified stem from system- or organizational-level factors. For example, health care professionals consistently cite poor insurance coverage or reimbursement and cost to purchase and store the vaccine as barriers. Among parents, vaccine cost and lack of insurance coverage are commonly noted. Most studies do not directly examine variation in HPV vaccination initiation or series completion at the system or organizational level. Several commentaries in the literature discuss the system-level barriers that likely influence overall uptake, including consent and confidentiality issues for adolescents,^76–79 cultural stigma associated with a vaccine for a sexually transmitted disease,^80,81 no usual source of care and decreased preventive services for adolescents,^76–79 and confusing societal norms that are unclear about adolescent autonomy and responsibility for sex and health care decisions.⁷⁷ All of these factors plausibly influence HPV vaccine uptake and should be considered when developing strategies to increase vaccine uptake and series completion. Multilevel analyses would be helpful for further understanding the role of system-level barriers on HPV vaccine uptake.

The literature search for this review yielded a large number of relevant studies, indicating that adolescent HPV vaccination is a high priority within public health and clinical communities. Despite the high volume of studies, study protocols and questionnaires varied widely. Use of standardized tools for collecting information about reasons for accepting or declining the HPV vaccine could facilitate more consistent data collection and enable researchers to more accurately compare barriers across groups and identify factors that facilitate HPV vaccination. One such tool is already available: the Carolina HPV Immunization Attitudes and Beliefs Scale provides standardized measures of parents’ attitudes and beliefs about the HPV vaccine.⁸² A similar tool is needed for collecting data on the barriers faced by health care professionals.

This review provides a systematic and comprehensive summary of the barriers to HPV vaccination that have been identified in the literature. A limitation of this review was that several commentaries that described system-level barriers were initially captured in the literature search but were ultimately excluded because they did not include analyses of original data. The system-level barriers described in those commentaries were examined briefly in the Discussion section.

In conclusion, this review describes the barriers to US adolescent HPV vaccination that have been identified in the literature. Barriers faced by health care professionals and parents should be carefully considered when developing strategies to improve HPV vaccine uptake and completion. Efforts should also address the needs of traditionally underserved groups, with particular sensitivity to social and cultural differences and the financial and logistical challenges that may have a greater effect on uptake among certain groups. Ultimately, efforts to better understand and address system-level barriers and social determinants of vaccination could potentially increase HPV vaccine uptake and completion among all US adolescents.⁸³