Background

Infecting nearly 80 million people in the United States (U.S.), the human papillomavirus (HPV) is currently the most common sexually transmitted infection [1]. HPV infection can cause genital warts, anal cancer, and cervical cancer as well as many other sequelae [1]. In 2006, the Food and Drug Administration (FDA) approved Gardasil vaccination to protect against HPV infections [2]. The U.S. Center for Disease Control and Prevention (CDC) currently recommends that all boys and girls aged 11 and 12 should be vaccinated, and persons who were not vaccinated in adolescence should be vaccinated anytime to age 26 [2]. In 2018, the FDA approved an extension to the acceptable age for the catch-up vaccination to adults through the age of 45 [3]. Despite CDC recommendations, less than 50% of females and 38% of males in the U.S. have completed the HPV vaccination [4].

Racial/ethnic minority adult populations, specifically Black/African Americans and Latino/as, disproportionally carry the burden of poor HPV-related outcomes. Though studies have shown that racial/ethnic minority populations tend to have higher vaccine initiation than their White counterparts, there may be lower completion rates for additional vaccine doses [5, 6]. Further, the barriers faced by racial/ethnic minority groups may differ significantly from White individuals. While health disparities regarding vaccine initiation and completion have been observed among Black/African Americans and Hispanics, specific barriers to explain these disparities have not been reviewed in racial/ethnic minority groups. Thus, this paper synthesizes available data collected over the past 10 years to assess barriers faced by racial/ethnic minority populations on HPV vaccination. This information is critical because understanding these barriers will enable public health officials to target racial/ethnic minority populations with resources to increase HPV vaccination coverage, which would in turn decrease the burden of poor HPV-related outcomes in these vulnerable populations.

Methods

The PubMed database, which includes Ovid Medline, was used to identify peer-reviewed articles and abstracts that reported on health disparities related to HPV vaccination in racial/ethnic minority populations. The keyword search comprised a combination of terms “human papillomavirus (HPV) vaccine barriers” (Appendix 2). The search was conducted on July 30, 2020. Studies conducted in the U.S. and published in the English language over the past 10 years from 2010 to July 2020, and primarily focused on HPV and HPV vaccination were included. However, studies that were not conducted in the U.S. or focused solely on cervical cancer screening were excluded. Further, studies that did not examine racial/ethnic disparities were also excluded. To preserve the congruency of this review, systematic review articles and intervention studies were not included, but are referenced where applicable. Studies with qualitative outcome measures were included.

The study screening process was conducted independently and is presented in Fig. 1. Initially, 532 articles were retrieved from the database and 14 articles were retrieved from keyword suggestions in PubMed. All studies were then transferred to Excel. Three duplicates and 496 other studies were eliminated due to the exclusion criteria, leaving 47 studies used in this systematic literature review. The selected articles utilized cross-sectional surveys and interviews, as well as focus groups; thus, each individual study may be at risk of inherent temporal bias. The populations covered in these articles were mostly female and consisted of racial/ethnic minority groups such as Hispanics/Latinos/as, Blacks/African Americans, Asians, and non-U.S.-born individuals, as well as Whites.

Fig. 1
figure 1

Preferred reporting items for systematic reviews and meta-analyses (PRISMA) flow diagram

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Table 1 presents a summary of the studies included in this review. Forty-six articles utilized a cross-sectional study design and collected data with questionnaires and interviews measuring outcomes with quantitative and qualitative methods, and one article utilized a longitudinal study design. Twenty-five studies gathered data from parents of adolescents, while nine studies gathered information from college-aged young adults and fourteen were focused on adults. Overall, thirty-three studies had a relatively large sample size (N > 100), and fourteen of the studies had smaller sample sizes (N < 100). Specified data collection dates for these studies ranged from 2006 to 2017.

Table 1 Summary of included studies evaluating barriers to HPV vaccine uptake among racial/ethnic minorities (N = 47)
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Results

The data reviewed demonstrated various barriers to HPV vaccination among racial/ethnic minorities compared with the White counterparts. The major findings are presented in three major themes: (1) gaps in knowledge and provider recommendations, (2) medical mistrust and safety concerns, and (3) religious and cultural beliefs (Appendix 1 Table 4). These barriers are discussed in detail below.

Gaps in Knowledge and Provider Recommendations

Differences in knowledge and awareness were demonstrated in various ways. Gender differences were shown to be a predictor of disparate knowledge and awareness of HPV and the HPV vaccine. In general, women and mothers of adolescent girls were more aware of HPV and the HPV vaccine as well as the association between cervical cancer and HPV infection, while men and parents of adolescent boys were typically less aware of both HPV and HPV vaccine, and had little-to-no intention of vaccinating their sons [7,8,9,10].

In some studies, racial/ethnic minority groups had significantly lower knowledge of HPV, the HPV vaccine, and the association between HPV and other cancers when compared with Whites (i.e. oral, anal, and penile cancers) [11,12,13,14,15,16,17,18,19,20,21]. Not only were the parents of adolescents lacking knowledge, but adult individuals who were still in the catch-up age range lacked knowledge of HPV and the HPV vaccine [8, 22, 23, 24]. However, in other studies, women reported higher levels of awareness (i.e., having heard of HPV and the HPV vaccine), but exhibited low levels of specific knowledge about HPV and the HPV vaccine, specifically in regard to the number of doses required for vaccination completion and the potential severity of HPV infection [11, 25,26,27].

Table 2 summarizes the main quantitative findings on relative measures of association (i.e., odds ratios) regarding knowledge of HPV and the HPV vaccine, as well as vaccination willingness and intentions. When quantified, Hispanic adult individuals tended to have lower odds of having heard of the HPV vaccine when compared with non-Hispanics [23, 28, 29]. Black and Asian adult individuals tended to have lower odds of having heard of HPV when compared with Whites. Also, Asian adult individuals had lower odds of having heard of the HPV vaccine compared with Whites [23, 28,29,30].

Table 2 Summary of Main Quantitative Findings For Studies That Reported Relative Measures of Association
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Despite these disparities, racial/ethnic minority parents tended to be more likely to initiate the HPV vaccination in their children when compared with their White counterparts [31,32,33,34,35,36]. Notably, an inverse association between knowledge of HPV and willingness to vaccinate may exist among Black parents [37]. This may imply that having any knowledge of HPV may decrease willingness of Black parents to vaccinate their children when compared with having no knowledge of HPV. Conversely, in other individual adult racial/ethnic minorities, willingness to vaccinate was associated with higher levels of HPV knowledge [37, 38].

In addition to these findings, foreign-born Black and Latino/a individuals were less likely to know where they could obtain an HPV vaccine compared with their U.S.-born counterparts (Table 3) [14, 39]. Studies were conflicting in their findings about the role that language preference may have in Hispanics with regard to willingness to vaccinate. Some studies suggest that Spanish-speaking parents were more willing to vaccinate their children when compared with English-speaking parents, while other findings suggest the opposite [40, 41].

Table 3 Summary of main quantitative findings for studies that reported frequency measures
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The literature suggests that low knowledge may be tied to a lack of recommendations for HPV vaccination from healthcare providers. Receipt of a provider recommendation was found to be the strongest predictor of HPV vaccination and intent/willingness of racial/ethnic minority parents to vaccinate their children [13, 16, 18, 26, 35, 41,42,43,44]. In parents who had initiated vaccination in their children, provider recommendation was found to be the main reason [13, 18, 33, 34, 40, 42, 44]. Similarly, racial/ethnic minority adult individuals reported that having discussed the vaccine with their healthcare provider was associated with increased likelihood of vaccination [20, 38].

Further, a lack of a strong recommendation from healthcare providers was also associated with decreased vaccine initiation and completion in racial/ethnic minority populations [10, 17, 31, 40, 42, 43, 45, 46]. Results showed that some providers offered the vaccine as optional or of low importance [31, 47]. Lower perceived risk for HPV infection was also reported among these populations [15, 18]. Furthermore, some parents of racial/ethnic minority adolescents who had initiated vaccination but did not complete the vaccine series reported receiving no information from their healthcare providers about follow-up to receive subsequent, necessary doses of the vaccine at a later date [18, 25, 47].

Medical Mistrust and Safety Concerns

The level of importance of medical mistrust and safety concerns regarding HPV vaccination among racial/ethnic minorities varies. In general, racial/ethnic minorities who had not initiated vaccination in their children were more likely to exhibit some level of mistrust with healthcare professionals and pharmaceuticals [15, 25, 26, 32, 33, 46, 48, 49]. In adult individuals who reported medical mistrust as a barrier to vaccination, it was suggested that Hispanics and Blacks preferred a healthcare provider of the same-sex, and/or same race/ethnicity [50, 51]. Further, Black and Asian women who had not been vaccinated demonstrated higher medical mistrust when compared with those who had been vaccinated, which was associated with preference to receive the HPV vaccine recommendation from a healthcare provider of the same race/ethnicity [50, 51].

In addition, racial/ethnic minority parents who were knowledgeable about HPV and the HPV vaccine tended to have concerns with the vaccine’s safety and side effects. Those who reported safety and efficacy concerns noted that this was a very important factor in deciding whether or not to vaccinate their children against HPV [25, 26, 32, 48]. Some parents believed vaccination may cause infertility in their daughters and were unsure of other potential side effects that might be associated with the vaccine [25, 26, 32, 48, 52]. They were also concerned that other long-term health problems may be associated with vaccinating their children [25, 26, 32, 48].

In studies examining racial/ethnic minority adult individuals in the catch-up age range, some reported that they would be willing to vaccinate if they could be sure that side effects were not severe [7, 8, 53]. Conversely, it was suggested that non-Hispanic White men may be more wary of potential side effects than their Black and Hispanic counterparts, leading to no intention of vaccination [53].

Religious and Cultural Beliefs

Religious and cultural beliefs were mostly assessed in qualitative studies and non-U.S.-born populations. Asian-American parents and foreign-born Hispanic parents were found to demonstrate a belief that the HPV vaccine was unacceptable for their children, especially their daughters, due to fear of promoting promiscuous behavior [26]. With fathers acting as the ultimate decision-makers in these familial paradigms, most children are not vaccinated [19]. Further, cultural perceptions were reported to serve as the main source of knowledge in some non-U.S.-born parents’ decisions about HPV and willingness to vaccinate their children [19, 33].

Conclusions

Our findings suggest a considerable lack of accurate knowledge and awareness of HPV and the HPV vaccine within racial/ethnic minority communities. However, educational interventions have not been shown to be an effective strategy in increasing vaccine uptake. Further, with Black parents possibly showing an inverse correlation between knowledge and intent to vaccinate, targeting education towards increasing HPV knowledge may not have the intended effects across racial/ethnic minority communities. Thus, increasing strong provider recommendations may be the most effective strategy in combatting low vaccine coverage among these populations. Specifically, an approach used by the American Academy of Pediatrics called “same day, same way” approach may be useful in heightening healthcare providers’ ability to introduce the HPV vaccine and to address the concerns of parents who have hesitance about the HPV vaccine [54]. This may be especially important in curtailing misinformation about HPV vaccination and easing concerns of safety and adverse vaccine reactions. Being that provider recommendations were shown to be the most important factor in parents’ willingness to vaccinate their children, this area should be targeted effectively.

Further, because some racial/ethnic minority adult individuals reported being more trusting of educators and healthcare providers who look like them, diversity among health educators and healthcare providers, and presenting information in a way that is tailored to each community may be beneficial in the effort to increase HPV vaccination rates. Though the role of patient-physician racial/ethnic concordance has not been thoroughly studied in HPV vaccination, it is an idea to be considered.

Moreover, an increase in awareness and vaccination recommendations for boys is needed and parents of both girls and boys must equally be educated. Also, awareness and recommendations must increase for adult individuals in the age range for catch-up vaccination. Gender differences should be addressed if vaccine uptake is to increase.

Over half of the literature covered in this review involved parents of adolescent children. There is low representation of adults who are in the catch-up age range for vaccination as well as males. Though the priority population for HPV vaccination remains 11–12-year-olds, there may be benefit in understanding the disparities faced by persons in the catch-up age range. This is due to the fact that even if someone has already been exposed to HPV, catch-up vaccination through age 45 has been shown to be efficacious in protecting against persistent infection and other strains of HPV [55, 56]. Both children and adults in the vaccine-appropriate age range should be vaccinated, since recommendations for HPV vaccination have now been expanded through age of 45.

It is critical to identify and address barriers to vaccination, in order to increase vaccine initiation and completion and decrease the disparate burden of poor HPV-related health outcomes experienced by racial/ethnic minority groups. Low provider recommendations as well as lack of accurate knowledge and awareness among racial/ethnic minority populations is associated with a decrease in HPV vaccine initiation and completion. The most common barriers to HPV vaccination were lack of healthcare provider recommendations, low knowledge, and awareness of HPV and the HPV vaccine, as well as safety concerns. To effectively target these communities, multi-level interventions need to be established. An increase in provider recommendations along with distribution of accurate information to these communities is necessary to combat the lack of HPV vaccination initiation and completion. As the recommended interventions are completed, prospective studies will be needed to assess the effectiveness of such intervention programs on HPV vaccination.

Limitations

There is limited literature available that specifically examines barriers in racial/ethnic health disparities related to HPV vaccination, thus, this review was limited to the few available literature. The decision to use PubMed was because it is believed that this database provides good coverage of the available English-language literature; however, it is possible that additional relevant articles not represented in PubMed were missed. Further, the data included in this review were cross-sectional in nature and so there is a risk of temporal ambiguity. The survey data collection used by most of the studies leaves room for self-report bias. Specifically, self-reported vaccination has been shown to be racially biased thus linking barriers to self-reported vaccination may be inherently biased [5, 57]. Additionally, the classifications of race in these studies may be a limitation as not all studies used the same classifications, thus making it difficult to compare across studies.