Vaccines | Free Full-Text | Understanding Barriers to Human Papillomavirus Vaccination among Parents of 9–10-Year-Old Adolescents: A Qualitative Analysis

The human papillomavirus (HPV) is the most common sexually transmitted infection. About 13 million women and men in the United States (US) acquire HPV each year. HPV is a risk factor for genital warts as well as oropharyngeal, anal, penile, cervical, vulvar, and vaginal cancers [1,2]. Out of the 100 known HPV types, 13 are known to cause cancer. Genotypes for HPV 16 and 18 cause 70% of cervical cancers, while genotypes 6 and 11 cause genital warts [3,4,5].

High-risk HPV is responsible for approximately 2% of all cancers in men and 3% of all cancers in women in the US. HPV has been shown to cause about 90% of cervical and anal cancers, 70% of vulvar and vaginal cancers, and 60% of penile cancers [1]. Despite effective screening and the introduction of the HPV vaccine, over 13,000 women were diagnosed with cervical cancer in 2020 in the US, and nearly 4000 women died from this disease [5,6]. HPV-related cancers also have a significant economic burden; diagnosis and treatment of cervical changes and anogenital warts cost up to $2.9 billion a year [7].

It is estimated that HPV will infect 80% of men and women within their lifetime, usually as a result of sexual activity [1]. Thus, understanding the age at onset of sexual intercourse among US children and adolescents is essential to inform HPV vaccination recommendations. A 2011 NIH report found that about half of the US teenagers are sexually experienced, and a large group of teenagers report at least three lifetime sexual partners in the past year. Within 14-year-olds, the youngest cohort surveyed, 12.5% of females and 13.1% of males reported ever having sex [8]. However, various social and environmental factors correlate with the earlier onset of sexual intercourse. A meta-analysis in 2007 found that adolescents who have problems in school drink alcohol and face psychological complications: aggression for boys and depressive symptoms for girls were more likely to have sexual intercourse before the age of 15. Race, ethnicity, and gender play a role in the age of first intercourse. Black males are 2.5 to 3.5 more likely to have earlier initiation of first sexual intercourse compared to their adolescent peers; however, this pattern did not covary with school attitudes and educational aspirations. Sexual intercourse is more closely linked to religious attitudes and behavior among nonwhite girls and education level among white girls [9]. For this reason, it has been suggested that adolescents should complete all required doses of the HPV vaccine by age 13.

The Advisory Committee on Immunization Practices (ACIP) recommends starting HPV vaccination at 11–12 years of age, but it can be started as early as age nine. If not previously vaccinated, catch-up vaccination is recommended between 13 and 26 years of age [10]. Only two doses (6 to 12 months apart) are required if the individual is less than 15 years old when the first dose is administered. If the patient is older, three doses are recommended [10]. According to the Centers for Disease Control and Prevention, 53,000 cervical cancer cases could be prevented within the lifespan of girls younger than age 12 if HPV vaccination rates increased to 80% in eligible patients [11]. However, HPV vaccination rates continue to be suboptimal in the US even though the vaccine has been available for over 15 years. In 2019, 71.5% of adolescents 13–17 years old had received ≥1 dose of HPV vaccine, but only 54.2% had completed all required doses [11]. HPV vaccination up-to-date rates were even lower among males than females (52% versus 57%) in 2019. Asian and Hispanic adolescents, as well as adolescents with Medicare coverage, were more likely to be up to date in their HPV vaccination schedule than white adolescents, adolescents with private insurance, or those who were uninsured. Adolescent HPV vaccination rates also differ by state, from 31% of adolescents being HPV up to date in Mississippi to 79% in Rhode Island [12].

Factors associated with low vaccination rates include race/ethnicity, parental education, marital status, provider recommendation, income, and age [13]. Since the HPV vaccine may be initiated as young as age 9, parental beliefs significantly determine the age at which a child receives it. Parental HPV-vaccine decision-making is often influenced by concerns about vaccine safety, perceived low susceptibility to HPV infection, and lack of knowledge about HPV and the vaccine series [14]. A systematic review of studies from 1995 to 2007 of HPV-related beliefs and HPV vaccine acceptability studies showed that vaccine acceptability was higher when people believed the vaccine was effective, the vaccine was recommended by a physician, and when they perceived that HPV infection was likely to occur. Additionally, vaccine acceptability was higher in parents with lower educational levels. However, 6% to 12% of parents reported concerns that vaccination would promote adolescent sexual behavior [15]. A more recent study conducted in 2016 demonstrated that secondary acceptance of the HPV vaccine after an initial rejection was strongly associated with receiving follow-up counseling about HPV vaccination from healthcare providers, receiving a higher quality HPV vaccine recommendation during the initial discussion, and greater satisfaction with provider communication [16].

Vaccinating at earlier ages is medically beneficial in multiple ways. HPV vaccines had more than 99% efficacy when administered to women without prior exposure to HPV [17]. The HPV vaccine elicits a higher immune response when administered at ages 11 to 12 compared to later in adolescence [12]. When HPV vaccination is initiated at 9 to 10 years of age, there is a significant increase in up-to-date (UTD) status by age 13 [18]. Additional benefits include the consequential spacing of recommended vaccines and an increased emphasis on cancer prevention messaging [19].

In 2014, Dr. Abbey B. Berenson initiated a program in the pediatric clinics at the University of Texas Medical Branch to increase HPV vaccine uptake among children 9–17 years of age. Funding is provided by the Cancer Prevention and Research Institute of Texas to hire patient navigators (PNs) who educate families in person and offer the vaccine at no cost to those with an adolescent child receiving care at a participating clinic. This program has been highly successful in increasing both initiation and completion rates. However, we observed that parents of children 9–10 were less likely to initiate the vaccination series than those with 11–12-year-old children [20]. This study aimed to further examine parental attitudes towards earlier vaccine initiation by interviewing parents of 9–10-year-old children who received vaccination counseling through this program. Our secondary aim is to understand parental perspectives on general childhood vaccination and school-based vaccination initiatives to inform potential interventions and improve HPV vaccination rates in Texas.

Our study found that caretakers’ opinions on the timing of HPV vaccination differed from the ACIP guidelines. Many participants preferred starting the HPV series during their child’s teenage years (>10 years). The rationale for this preference varied widely between individuals and was not necessarily scientifically supported. Many of the justifications given for delayed vaccination had to do with the misguided association between the HPV vaccine and sexual maturity. Much work has been carried out to deconstruct this narrative, including the rebranding of the HPV vaccine by the CDC-Hager Sharp campaign in 2015 [21]. Providers’ support and counseling continue to be key aspects in educating parents on this subject. When parents believe that a child’s vaccination could initiate sexual behavior, rather than disproving their argument, providers should attempt to desexualize the HPV vaccine by highlighting its use against cervical cancer and emphasizing its novelty [22]. When questioned on the necessity of its early administration, providers can emphasize the need to vaccinate before the onset of potential HPV infection. Another strategy is to inform caretakers that HPV vaccination provides a more robust immune response when administered at a young age. Additional assistance for physicians in navigating difficult discussions with parents can be found in the CDC HPV vaccination recommendations [23]. It should also be noted that most participants in our study agreed with starting early HPV vaccination. However, the interviews reported parents’ opinions after PN education had already occurred. It is, therefore, difficult to assess whether participants felt this way before the PN HPV vaccination educational session.

Overall, interviews of parents with 9- to 10-year-old children revealed considerable concern about vaccination side effects. This may have led parents to avoid certain vaccines, such as those to prevent influenza and COVID-19. Despite concern about vaccine safety, in general, most of the parents interviewed believed that the HPV vaccine was beneficial to their child’s health by protecting them against future diseases. These results conflict with the findings in the literature, which mention an overall increase in HPV vaccine hesitancy. For example, a questionnaire administered to 5249 women in Greece found a decline in intention to vaccinate when the HPV vaccine became available, coinciding with a rise in the proportion of women concerned about its potential side effects, specifically those promoted by the media [24]. It should be noted that while the participants in our study voiced a strong distrust in news/social media when obtaining vaccination information, side-effect hesitancy continues to be a strong influence against HPV vaccination. Since parents were interviewed after their child’s clinic visit, their responses likely reflect the education on HPV and the vaccine they received from a PN. In fact, 18 out of the 21 parents agreed to have their child receive the HPV vaccine the day of the visit. Therefore, our study suggests that educating parents on HPV and the HPV vaccine is an effective strategy to help overcome barriers to vaccination.

Throughout interviews, multiple caregivers demonstrated inadequate medical information or a lack of understanding of the medical process and vaccine functionality. School-based health education has consistently improved student health knowledge surrounding the scientific and philosophical principles of individual and societal health [25]. However, as of 2018, only 38 states and the District of Columbia mandate sex education and HIV education, and when these are provided, only 17 states require the content to be medically accurate. In Texas, where this study occurred, sex or HIV information is not mandated. If provided, it does not need to be medically accurate, only age-appropriate, and can allow for the promotion of religion [26]. None of the states consider vaccine literacy as an objective in their health education curriculum. Thirty-two states have no formal vaccine education, and few require it in their school health curriculum. Only Colorado and Maryland require health classes to discuss vaccination during middle and high school. Texas requires vaccine education during high school and not in middle school. Furthermore, none of the states provide vaccine guidance to teachers, which explains why only 37% discuss herd immunity in their classrooms [27]. These circumstances provide the platform for vaccine misinformation and vaccine illiteracy. Therefore, states need to change school health education content requirements before it could be another avenue to educate individuals on HPV and the vaccine.

Knowledge is critical in the beginning stages of behavior change, especially in adopting healthy behavior [28]. Key stakeholders (such as parents, school staff, and providers) should possess adequate knowledge about HPV and the vaccine to make correct decisions regarding their children’s or students’ health. Even though all participants had received education from a PN, they still reported a lack of HPV vaccine information and a lack of exposure to positive or negative sources of information. These results indicate that participants had not likely received HPV education before counseling by the PN. Apart from the physician’s office, a large portion of education is expected to be completed in schools. However, in 2017, the US Department of Health and Human Services released a report stating that only 1.2% of secondary schools in Texas provide the HPV vaccine, with a national range of 0–29%. Regarding general sexual health services, only 0.3% of Texas schools would provide STD treatment (0–19% range), and only 0.3% would provide condoms (0–20% range). Seventy-eight percent of Texas secondary schools did not provide sexual or reproductive health, and only 29% provided parents and families with information on how to communicate with their children about sex [29]. Vaccination education should be a multidisciplinary approach, as vaccination initiatives would likely suffer if public schools were not used as a communication channel.

Interview responses indicate that many participants mistrust medical advances, approaches, and vaccine testing. Some mistrust is rooted in the history of the medical profession, specifically regarding research and the use of people as subjects of experimentation. The infamous Tuskegee Syphilis Study between 1932 and 1972 left racial and ethnic minorities with generational trauma, continuously propagated by a health system that creates, sustains, and reinforces racism, classism, homophobia, transphobia, and stigma [30]. Half of the participants identified as black, and approximately one-fourth identified as Hispanic; data, however, was not stratified by race or ethnicity, making it difficult to know whether medical mistrust is related to minority status within this study. However, it should be noted that participants’ mistrust revolved around the theme of medical experimentation. A few participants believed that the longer it takes to produce a vaccine, the safer the vaccine. The rapid development of the COVID-19 vaccine fueled such misconceptions [31]. Other participants felt that medical processes and procedures were dangerous. Lastly, caretakers also felt that the medical industry uses people as a means to understand treatments. When interviewing a caretaker, he stated that his niece convinced him to take the COVID-19 vaccine by focusing on the overall public benefit and coming to terms with being considered a guinea pig. The participant’s feelings appeared to arise from the belief that the healthcare system in place does not prioritize an individual’s well-being or health. Individuals are, therefore, forced to see for their well-being and protect themselves from medical management. Medical mistrust can have serious consequences, such as lower healthcare utilization and poorer management of health conditions. It is the responsibility of the healthcare community to amend these wrongdoings by acknowledging past and ongoing trauma and collaborating among communities that have experienced historical and social exclusion [32].

Provider endorsement is an important determinant factor in HPV vaccine acceptance [33]. Physicians’ recommendations can increase HPV vaccination and completion by three and nine times [34]. These findings are consistent with our data, as caretakers thought doctors were a trustworthy source of medical information and vaccine administration. Moreover, caretakers preferred that their child’s physician supervise vaccination. These results indicate that parents prefer that their child be vaccinated in a clinical setting. Despite public trust in healthcare professionals, many providers lack general HPV and vaccine knowledge and are hesitant to make recommendations not stated in professional organizations’ guidelines. HPV vaccination initiatives should encourage doctors to internalize HPV vaccination guidelines from their colleagues and profession. Additionally, many providers believe they will not convince parents and patients of the vaccine’s effectiveness and value. An initiative focused on self-efficacy might address this issue by improving physician confidence in addressing parental concerns [34]. How vaccination is discussed can also significantly influence a parent’s decision to vaccinate their children. In a 2013 study, the American Academy of Pediatrics found that parental odds with vaccination increased when providers discussed vaccines with parents compared to when providers treated vaccines as routine [35]. Many participants reported feeling more comfortable when medical professionals incorporate patients into decisions regarding their care. However, a collaborative discussion, as well as shared decision-making, surrounding vaccinations is not typically executed by providers since doing so would present vaccine avoidance as a valid option. Yet, disregarding parental emotions in the matter could hinder the physician–patient relationship and, thus, future scheduled vaccinations. Therefore, a physician should tread carefully in this matter as a choice should be given to the patient or the patient’s parents while concurrently voicing a strong recommendation for the HPV vaccine.

Patient navigators can assist in creating a discussion with the patient or family in situations when providers cannot do so. PNs can take advantage of regular clinic visits to inform unvaccinated or partially vaccinated patients about HPV and the availability of a vaccine that protects against infection and disease. Such a program was initiated in 2014 at the University of Texas Medical Branch. The PNs hired by the vaccination program screened the electronic medical records of 9–17-year-old patients with upcoming appointments at a UTMB clinic and approached parents whose children were unvaccinated or incompletely vaccinated against HPV. If the parents consented, the children received the vaccine that day. The vaccine is administered at no cost to the family. The program’s high initiation and completion rates show that taking advantage of a routine clinic visit to educate patients on HPV and offer the vaccine is an effective strategy to increase vaccination rates [20].

Moreover, school-based vaccination is considered one of the most effective and efficient means of ensuring high HPV vaccination rates among adolescents [36,37]. Under this initiative, schools would routinely deliver recommended vaccine doses to students, making these prime locations for vaccine initiatives. HPV vaccination has historically been offered exclusively in clinics, which may create a barrier for caregivers. Offering vaccines in school settings at no cost has increased adolescent immunization rates in some areas of the US. However, only Rhode Island, the District of Columbia, and Virginia schools require individuals to receive the HPV vaccine. “Vaccinate before you Graduate” is a Rhode Island program where the Department of Health offers free vaccines to all middle and high school students. Rhode Island is now known to have the highest HPV vaccination rate in the country [36]. Replicating such a program elsewhere may be feasible as the Affordable Care Act requires insurance companies to cover vaccines recommended by the ACIP without copays. Furthermore, Vaccines for Children (VFC) is another federally funded program that can provide free vaccination to uninsured children or those not covered by Medicaid [38]. Despite greater accessibility, caretakers were reluctant to vaccinate their children at a school. The school’s cleanliness was questioned, as well as the qualifications of the school nurse and concerns surrounding the safety of the children. This is consistent with previous findings from a school influenza study [39]. For similar reasons, many caretakers were unwilling to vaccinate their children at pharmacies.

Some caretakers would consider school vaccination if this became a common practice, indicating that culture and social norms are potential barriers. These findings are like those seen in a study of parents of 11- to 14-year-old children attending seven middle schools in a large urban school district. Parents who had previously used a school vaccination program were 2.5 to 4 times more likely to report willingness to receive each specific vaccine at school than those whose children received immunizations at another site [40]. Therefore, various trials of school vaccination programs will need to occur before seeing a rise in caretaker willingness to change to this venue for vaccinations. The government plays a crucial role in implementing school vaccination programs. School vaccination programs in Canada, Australia, and some parts of the UK are funded by the government and have seen a significant increase in adolescent vaccination rates. However, the US does not currently have a culture supporting this agenda [41].

When considering governmental policy surrounding school vaccination, compulsory vaccination should be mentioned. Most participants believed that the government should not enforce HPV vaccination as a prerequisite for public benefits. Regardless of increased vaccine accessibility for adolescents and children, caretakers continue to have the right to refuse any vaccination that is not mandatory under state law. However, exemptions are made for individuals with medical conditions or based on religious freedom [41]. A 2019 systematic review of public opinions surrounding compulsory vaccination found that parents were more likely to refuse the HPV vaccine than any other adolescent vaccine. It was also found that support towards mandatory vaccination increased after their implementation, indicating a possible cultural shift that needs to be addressed [42].