Race, ethnicity and income as factors for HPV vaccine acceptance and use

Abstract

If distributed equitably, Human Papillomavirus (HPV) vaccines have the potential to reduce racial disparities in HPV-related diseases and cervical cancers. However, current trends in the US indicate low uptake among all adolescents, with persistent disparities among minority and low-income adolescents despite largely positive views of vaccination among their parents. As Black, Hispanic, and Asian populations continue to grow in the US over the next 40 y, it is imperative that we not only improve HPV vaccination rates overall, but focus on high-risk populations to prevent an increase in cervical cancer disparities. This review discusses initiation and completion rates of the three-dose HPV vaccine series among adolescents in high-risk groups and describes cultural similarities and differences in motivation and barriers to vaccination. The goal of this review is to highlight factors leading to vaccination in different adolescent racial groups and to help guide the development of strategies to increase rates of vaccine initiation and completion among groups at the highest risk for developing cervical cancer.

Keywords: :

• HPV vaccine
• vaccine uptake
• racial disparities
• vaccine acceptance
• review
• income
• pediatrics
• policy
• vaccinology

Introduction

Racial disparities in cervical cancer and human papillomavirus (HPV) vaccination

In the United States, cervical cancer remains the third most common gynecological cancer, with an estimated incidence of approximately 12,000 new cases of invasive disease and 4,000 deaths annually.¹ Cervical cancer incidence and mortality are 25% and 95% higher respectively among Blacks and 53% and 41% higher respectively for Latinas compared with Whites.¹ Cervical cancer incidence is nearly twice as high in counties with the poverty levels above 20% compared with less than 10%.² Because minorities in the US are more likely to be poor than Whites, have less access to healthcare, and may receive differential treatment based on insurance status, race, or both, disentangling the effects of race, socioeconomic status, and healthcare access on cervical cancer disparities is challenging.

Chronic HPV infection causes 99.7% of invasive cervical cancers,³ and HPV is the most common sexually transmitted infection, with a prevalence of 42.5% in women ages 14–59.⁴ Low risk HPV, genotypes 6 and 11, account for 90% of benign disease such as genital warts, and genotypes 16 and18 account for approximately 70% of cervical cancers worldwide.⁵ Since 2006, a quadrivalent vaccine (Gardasil^® or HPV4) and a bivalent vaccine (Cervarix^® or HPV2) have been recommended to protect against HPV infection in women.^6,7 Both vaccines can prevent up to 98% of HPV 16- and 18-related cervical intraepithelial neoplasia, a precursor to cervical cancer, and the quadrivalent vaccine also prevents vaginal, vulvar and anal dysplasia as well as genital warts.^6,7 Routine vaccination is recommended for girls at age 11–12, with catch-up vaccination through age 26. The recommended vaccination age of 11–12 was chosen to minimize the likelihood of HPV exposure prior to vaccination; 6.2% of adolescents nationwide initiate sexual activity prior to age 13.⁸

Despite these recommendations, however, the overall rate of initiating and completing the HPV vaccine series among US female adolescents are only 53% and 35% respectively,⁹ even though studies indicate that approximately 70% of parents of all races and income levels intend to vaccinate their daughters.^10,11 Unlike the patterns seen for invasive cervical cancer, however, HPV vaccine initiation rates are highest in Black and Hispanic girls and those living below poverty, although disparities remain related to vaccine completion among those who start the series, with the highest rates for White girls living above poverty. This article reviews factors associated with HPV vaccine acceptability, uptake, and completion among adolescents of different racial, ethnic, and income groups in the United States.

HPV vaccination in the Black community

Black women, who represent approximately 14% of US women,¹² have the highest rates of HPV infections, making HPV vaccination prior to sexual debut especially important among this group.^4,13 The 2011 Youth Risk Behavior report found that more Black teens (60%) reported having sexual intercourse than Hispanic (48.6%) and White (44.3%) teens. Nearly 14% of African-Americans had their first sexual experience prior to age 13, compared with 7.1% for Hispanics and 3.9% for Whites.⁸ In addition, 24.8% of Black teens reported four or more lifetime partners, compared with 14.8% of Hispanics and 13.1% of Whites.⁸

Black mothers have been shown to have an overall positive view on vaccination after education about HPV, citing a desire to prevent cancer and protect their children against a sexually transmitted infection.^8,14,15 Concerns described by African-American parents include a lack of information on vaccine efficacy and safety, cost, long-term side effects, the belief that vaccination may increase early or unsafe sexual behavior, and concern that the new vaccines are experimental (Table 1).^16,17 Studies of vaccination rates shortly after the vaccine was released indicated lower rates among Black compared with White girls. Among 9–20 y-old female Medicaid patients surveyed in 2008, Black girls had the lowest rates of vaccination among (5.1%), compared with 7.2% of Whites and 9.5% of Hispanics.¹⁸ While the effects of race are often difficult to distinguish from those of income and insurance status, a larger study involving middle class adolescents enrolled in a managed care organization also found a lower rate of HPV vaccine uptake among Black compared with Whites teens in the 18 mo following vaccine approval.¹⁹ The most recent national data, however, indicates that disparities in vaccine initiation may be improving. The National Health Interview Survey (NHIS) found no difference in vaccine initiation between 11–17 y-old Black and White teens,²⁰ and the National Immunization Survey- Teen (NIS-teen)⁹ reported that 56% of non-Hispanic Black teens initiated in 2011 compared with 47.5% for non-Hispanic White teens (Table 2).

Table 1. Barriers and facilitators of HPV vaccination among minority groups

	Barrier	Facilitator
Black	Lack of information Concern about long-term side effects Concern that vaccine is experimental Logistical challenges to completion of three dose series Lack of health insurance, especially among poor in Southern US Foreign-born subgroups: Language barriers and inaccurate information	Provider recommendation Desire to prevent cancer Desire to protect against a sexually transmitted infection Federally funded Vaccines for Children program Foreign-born subgroups: Experience with vaccine-preventable diseases
Hispanic	Language Safety concerns Not knowing where to obtain vaccine Lack of health insurance, especially among poor and undocumented immigrants	Provider recommendation Desire to prevent cancer Trust in providers Favorable attitude toward vaccines Experience with vaccine preventable diseases and cervical cancer in home countries Federally funded Vaccines for Children program
Asian	Language Limited knowledge Concerns related to sexual activity Lack of health insurance, especially among poor	Provider recommendation Desire to prevent cancer Federally funded Vaccines for Children program

¹ The percentage of girls without insurance includes those who did not have coverage at least some of the time during the year, and those covered by public insurance are children that did have health insurance at least some time during the year.

Table 2. Relationship of race, ethnicity, and poverty to cervical cancer incidence and mortality, and HPV vaccine initiation and completion

Race and poverty level	Current(%) US female population^64	Projected (%) US female population 2050^64	Cervical cancer incidence per 100,000^1^,^115	Cervical cancer mortality per 100,000^1^,^116	HPV vaccine initiation (%)^117	HPV vaccine completion           (%)^117	HPV vaccine completion among those who start series           (%)^117
White, non-Hispanic	63.6	50.7	7.1	1.9	47.5	33.0	74.8
Black, non-Hispanic	13.7	15.6	9.1	4.1	56.0	31.7	60.8
Hispanic	17.2	26.9	10.4	2.8	65.0	41.6	69.4
Asian, non-Hispanic	6.1	9.3	6.7	1.7	55.8	35.0	70.5
> 100% poverty level	85	N/A	2.01	2.2*	50.1	33.4	72.6
< 100% poverty level	15	N/A	3.66	3.5 **	62.1	39.0	66.4

* < 10% of county below poverty level; ** > 20% of county below poverty level

While initiation is important, completion of all three doses of the HPV vaccine is recommended given the lack of data showing efficacy of incomplete vaccination.^21-23 Many studies have found lower adherence to the recommended vaccination schedule among Black females than other races, with Blacks being half as likely to complete vaccination as their White counterparts in two studies of publically insured patients.^18,24 From 2006–2009, complete vaccination rates among Black teens ranged from 11.1–24.6% compared with 19.5–65.3% among Whites.^9,19,24,25 NIS-Teen 2011 reported a dramatic increase in completion rates across most races compared with prior years, however Blacks who begin the HPV vaccine series continue to have a lower completion rate than Whites: 60.8% (95% CI 54.1–67.5) vs. 74.8% (95% CI 72.3–77.3).⁹

HPV vaccination among sub-populations of Black women

Much research on Black women fails to account for the heterogeneity of beliefs and attitudes among subgroups of this population, particularly with respect to immigrants from the Caribbean. One survey showed a slightly higher rate of sexual activity in Caribbean-American than African-Americans teens (56% vs. 46% by age 16), and also more interest in vaccination (54% for Caribbean-American vs. 35% for African-American, p = 0.016).²⁶ Research with parents of Caribbean American teens indicates mixed views about vaccination, however, with reported support for vaccination ranging from 30–70%.^27-29 Barriers to HPV vaccination may be especially prevalent in the Haitian community (Table 1). Many Haitian women have very little knowledge and hold various misconceptions about HPV including beliefs that transmission may depend on sexual position, that physical sequelae are often manifested with initial infection, and beliefs related to confusion between HPV and HIV, such as HPV causing AIDS, and concerns that the vaccine was intended for Haitians as an experiment, or would be used as a tool for discrimination against the Haitian community.^28,29 Another study of Haitian parents indicated that some did not feel that HPV vaccination fell within their parental role as their children should not become sexually active before adulthood.²⁷ Other parents believed that their daughters were too young for vaccination, that their children were not sexually active (and that sex at a young age is an “American” trait), that the vaccine may be misinterpreted as permission to engage in sexual activity, that the vaccine was only necessary for women with multiple partners, and that vaccination was not necessary for people who practiced abstinence.³⁰ Studies looking at the initiation and completion rates among other Black subgroups, especially among immigrants from African countries, are lacking.

HPV vaccination in the Hispanic/Latino community

Hispanic females, who represent approximately 17% of US women,¹² have the second highest prevalence of HPV infection (44.2%).⁴ Similar to Black women, most (58–90%) Hispanic women surveyed stated that they would accept HPV vaccination.^16,17,31-33 Women with HPV infections were more likely to accept vaccination, to favor a law recommending vaccination for girls prior to entry in the sixth grade, and to know where to bring their children to be vaccinated.³² Those who believed vaccines in general were safe, who trusted their providers, and who also believed that the HPV vaccine could help prevent cervical cancer were also more likely to vaccinate their daughters.^16,33 Most Hispanic parents who expressed reservations or declined vaccination for their daughters stated that they needed more information, were concerned about vaccine safety, or did not know where to obtain vaccination.^17,33,34 Few parents believed that the vaccine would be misinterpreted as permission to engaged in intercourse at a young age (Table 1).^16,33

The NIS-Teen surveys in 2008, 2009, and 2011 and the NHIS 2010 all found higher HPV vaccine initiation rates among Hispanic girls than White teens.^20,35-38 In 2011, 65% of Hispanic adolescents received one or more doses of the vaccine compared with 47.5% of White and 56% of Black adolescents⁹ (Table 2). Among Hispanic adolescents who begin the series, 69.4% (95% CI 63.9–74.9) complete three shots compared with 74.8% (95% CI 72.3–77.3) for Whites.⁹ High acceptance of HPV vaccination among Hispanics may be due, in part, to favorable views toward vaccines in general, due to personal experience with vaccine-preventable diseases in their home countries.¹⁶ In addition, cervical cancer is the leading cause of death for women in many parts of Latin America,³⁹ and up to 30% of Hispanic women know someone who has suffered with this disease.^16,40 Differences based on country of origin have been documented for other cancer prevention measures,⁴¹ and research comparing HPV knowledge in the Southeastern US found that fewer immigrants from Mexico and Honduras had heard of HPV and HPV vaccination than immigrants from Puerto Rico, though all were equally likely to favor HPV vaccination.⁴² Similarly, Mexican-Americans in Los Angeles were equally likely to vaccinate their daughters compared with Hispanics from other countries.³³

HPV and vaccination in Asian/Pacific Islander communities

The term Asian/Pacific Islander refers to people from East Asia, Southeast Asia, the Indian subcontinent, or the Pacific Islands, and represents approximately 5% of the US population.¹² Although cervical cancer incidence for Asians overall is lower than other ethnic groups (6.7 per 100,000 for Asians compared with 9 per 100,000 for Blacks, 10 per 100,000 for Hispanics, and 7 per 100,000 for non-Hispanic Whites),¹ certain subgroups have extremely high rates, specifically Vietnamese-American women (14 per 100,000 women) and Korean-American women (11 per 100,000).⁴³ Asian/Pacific Islander is a highly diverse group and limited data are available examining HPV vaccination.

Surveys examining parents’ intention to vaccinate have shown lower rates among Asians than other ethnic groups,^34,44,45 perhaps due to language barriers, limited knowledge, and concerns related to promoting sexual activity.^34,45-48 Different perceptions of the effect of HPV vaccination on sexual activity were noted between Mandarin- and Cantonese-speaking Chinese immigrants,⁴⁵ and Cambodian American parents suggested that traditional values related to sexuality contribute to hesitation in vaccinating their children (Table 1).⁴⁹ Nationwide data are conflicting regarding education rates for Asians. NIS-teen 2011 data indicate similar rates of vaccine initiation and completion among Asian and White teens (initiation: 55.8, 95% CI 45.0–66.6 for Asians vs. 47.5 95% CI 45.6–49.4 for Whites; completion among those who start: 70.5 95% CI 55.3–85.7 for Asians vs. 74.8 95% CI 72.3–77.3).⁹ NHIS 2010 data, however, shows that Asians overall are less likely than all other minority groups sampled to initiate vaccination series (OR 0.65 vs. 0.68 for Hispanic and 0.75 for Black).⁵⁰

Poverty status, education and HPV vaccination

Approximately 15% of the American population lives below poverty, with higher proportion of Blacks (27.6%, 90% CI 25.6–28.6%) and Hispanics (25.3%, 90% CI 24.5–26.1) living below poverty than Asians (12.3%, 90% CI 11.1–13.5) and Whites (9.8%, 90% CI 9.5–10.1).⁵¹ In comparison to women at or above poverty level, those below poverty level have a higher prevalence of HPV infections at 56.5% vs. 39.7%,⁴ are more likely to be diagnosed with advanced cervical cancer, and are 30% less likely to survive after a diagnosis of distant-stage disease.⁵² Some studies suggest that a large percentage of low income mothers have overall positive views if HPV vaccinations^10,16 and are very likely to accept vaccinations for their daughters. In fact, several studies have shown that parents with a high school education or less were more willing to vaccinate their daughters than those with college degrees.^44,53,54 Differences may be more pronounced for girls age 13 or younger: one study found that 87% of parents with a high school education or less would vaccinate compared with 66% of college-educated parents (p = 0.005),⁴⁴ though another showed that parental education level had no effect.⁴⁶ Reasons for supporting vaccination included concerns for health, safety, and to avoid future feelings of regret in the event of an adverse outcome.^16,44 Consistent with high levels of support for HPV vaccination among low-income parents, the NIS-teen 2011⁹ reported higher levels of vaccine initiation among females below than those above the poverty level (62.1% 95% CI 58.4–65.8% vs. 50.1% 95% CI 48.1–51.9) (Table 2). Among those who start the series, however, a trend toward lower completion rates is noted among poor teens compared with those above the poverty level (66.4% 95% CI 61.2–70.8 vs. 72.6 95% CI 70.0–75.2). Reported barriers to vaccination include lack of information and lack of urgency to vaccinate,⁵³ moral concerns for their daughter’s sexuality, and concern for safety.⁴⁴

Discussion

In the United States approximately 12,000 cases of cervical cancer occur each year. As with many other types of cancer,⁵⁵ higher incidence and mortality rates are seen in low-income minority populations.¹ Some of these observed differences are due to higher rates of HPV exposure, which are culturally and socially mediated and relate to both the age of sexual debut and the number of lifetime partners.^8,56 Other factors relate to healthcare access and utilization, and reflect both linguistic and cultural barriers including low health literacy and fatalistic beliefs,^57-59 as well as systems-related inequities, with limited access to health care for those who are uninsured or underinsured, leading to differential access to screening, follow-up and treatment for abnormal pap smears, cervical dysplasia, and cancer^37,60-62. HPV vaccination has the potential to reduce the impact of a number of these factors by limiting exposure to the virus among sexually active young adults, thus decreasing the risk of cervical dysplasia and cancer among vaccinated women, even if access to screening and treatment remains inequitable. Achieving equivalent or higher rates of HPV vaccination among low-income and minority adolescents compared with affluent and White adolescents is important for two reasons. First, most young adults tend to have sexual partners from within their communities,⁶³ thus the achievement of herd immunity for a sexual network may depend on achieving high vaccination rates along racial, ethnic, and income groups, as well as by geographic area. Second, the proportions of the US population that are Black, Hispanic, and Asian are increasing rapidly. The U.S Census Bureau projects that by 2050, Hispanics will comprise 26.9% of the female population, Black non-Hispanics will comprise 15.6%, and Asians 9.3%, increases which could substantially increase the national burden cervical cancer unless steps are taken to reduce disparities.⁶⁴

The United States has much lower HPV vaccination rates than other high-income countries. England, Australia, Portugal, Spain, and Scotland, which have national healthcare systems and vaccinate girls in school,⁶⁵ have all achieved as high as 80% three-dose coverage.⁶⁶ Canada, which also has a national healthcare system, has vaccinated 58–85% of teen girls, with the highest coverage in provinces using school-based systems, and lowest rates in provinces relying on clinic visits for vaccination.⁶⁶ The United States healthcare system is insurance-based, with 59% of insurance for children coming from employer-based, private insurance companies, and 36% from public sources.^67-69 The remaining 9%¹ of children are uninsured, but have access to vaccines, including HPV vaccines, through the federal Vaccines for Children program,^12,70 a federal program created in 1993 to cover all vaccines recommended by the Advisory Committee on Immunization Practices for uninsured children and adolescents as well as those enrolled in Medicare, Native American, Alaskan Native and those who receive care at rural health centers.^12,70 While this program covers vaccines, however, it does not provide coverage for routine medical care that would allow patients to establish a relationship with a primary care provider. The Affordable Care Act⁷¹ was designed to help make prevention affordable and accessible for all Americans by requiring both public and private health insurance plans to cover preventive services and by eliminating cost sharing, which includes immunizations, and will also expand Medicaid in most states, effectively increasing the number of low-income children with a regular source of care.

HPV vaccination rates for all girls in the United States are well below the rates needed to achieve herd immunity, and though current trends indicate that low-income and minority adolescents in the US have higher rates of initiating HPV vaccination than White and affluent adolescents,⁹ minority and low-income girls who start the series are not as likely to complete all three doses as White and affluent girls, and little is known about the effects of incomplete vaccination.^21-23 Unlike the United States, other high-income countries with high rates of HPV vaccination indicate lower uptake of HPV vaccination among ethnic minority groups and poor students,^72-74 as well as lower rates among some racial and religious groups, specifically Asians (OR = 0.38, CI: 0.15–0.95), Muslims (OR = 0.19, CI: 0.06–0.59) or practicing Sikhs/Hindus (OR = 0.12, CI: 0.03–0.45) in the UK and lower uptake in areas of the Netherlands with higher proportions of voters for Religious Political Parties in the Netherlands.^74,75

Because neither school mandates nor school-based vaccination programs are in place on a national scale in the US, vaccination is largely dependent on individual communication between parents of adolescents and their providers, and thus is based on human interactions between parents, adolescents, and providers, which may be influenced by factors related to race, insurance status, and healthcare access. Over 84% of parents of all races and ethnicities use their doctor as their main source of vaccine information,⁶⁵ most parents (55–90%) say they would accept HPV vaccination if offered by their provider,^16,44,76-79 and recommendations of a health care provider are often more important than race or socioeconomic status in determining vaccine receipt^78,80-85 Ninety percent of teens that received one or more doses of the HPV vaccine received strong recommendation from a provider,²⁰ a telephone survey of primarily low-income Black and Hispanic families in Los Angeles found that provider recommendation increased the odds of vaccination 48-fold,⁷⁸ and lack of recommendation from a health care professional was the most frequently reported reasoning for not receiving the HPV vaccination among women found to have precancerous cervical lesions.⁸⁶

Provider factors associated with offering HPV vaccination include prevention of cervical cancer and HPV-related disease,⁸⁷ knowledge about⁸⁸ or experience with these diseases,⁸⁹ and recommendations of professional societies.^90,91 Provider-described barriers include reimbursement concerns,^87,89,92 parental concerns which result in delayed or missed vaccinations,^87,93 concerns that patients would not return for follow-up injections,⁹² the complex and time-consuming nature of discussing vaccination against sexually transmitted infections,⁹⁴ and poor public understanding of HPV.⁹⁵ Physicians as well and other health care providers also have poor understanding of the multiple diseases caused by HPV: while nearly all know that HPV causes cervical cancer, few are aware of the relationship with vulvar, vaginal, anal, and oropharyngeal cancers.^96,97 Several surveys demonstrate providers’ reluctance to vaccinate 11–12 y olds compared with older teens.^5,98,99 Similarly, studies indicate that providers who defer vaccination for their own children are less likely to recommend it to their patients.^100,101 As practitioner recommendation is crucial to vaccine uptake, and each provider interacts with hundreds to thousands of patients, interventions targeting providers such as academic detailing^102,103 or performance improvement continuing medical education¹⁰⁴ may be an effective way to improve vaccination rates.

Given that only 35% of teens nationwide have completed HPV vaccination, increasing parents’ awareness of HPV may also help improve vaccination rates since parental permission is required for vaccination of girls under age 18. Minority, immigrant, and non-English-speaking parents consistently demonstrate lower rates of HPV-related knowledge than White and English-speaking parents.^105-107 While poor knowledge is not necessarily associated with declining vaccination,¹⁰⁸ parents with little knowledge of the benefits of vaccination may be less likely to advocate for themselves. Inadequate knowledge may also contribute to lower rates of completion among minority adolescents. The most common reason given by parents for non-completion was being unaware of the need for subsequent doses; other reasons included side effects, being too busy, and finding the times and locations of the clinics inconvenient.¹⁰⁹ These issues may be more common among low-income and minority women who may have limited English proficiency, low health literacy, hold unskilled jobs with inflexible work hours, or have limited childcare options. Factors that would facilitate minority parents’ decisions to vaccinate their children: improved education, affordability, and knowing others who were vaccinated.¹⁷ Other predictors of HPV vaccine acceptability include perceived benefits of vaccination, provider recommendation, personal experience with HPV infection or cervical disease, and perceived susceptibility to HPV disease.^110,111 Patient-oriented solutions such as patient navigation systems have demonstrated efficacy for improving follow-up after abnormal Pap tests and mammograms among minority and low-income populations,^112,113 and could perhaps also be applied to improve completion among those who have started the series.

Strengths and limitations

This review aims to describe HPV vaccine uptake among girls of different racial, ethnic, and income groups in the United States. Because the HPV vaccination rates among different groups change annually, and vary by geographic region, we have used the 2011 National Immunization Survey data to represent the most recent and accurate vaccination data. To explore factors unique to different racial and ethnic groups, we have included both surveys and qualitative studies. All studies will reflect the geographic area and time period when data were collected, which may limit their generalizability. Garinci and colleagues review of studies assessing HPV vaccine uptake found both selection and information biases in available surveys.¹¹⁴ In addition, this review focuses on HPV vaccination in females in the United States; vaccination of males, detailed comparison of vaccination systems (provider-based, school based, compulsory) in high-income countries, and introduction of the HPV vaccine in low-income countries are not addressed.

Conclusions

Overall rates of HPV vaccination in the US are low for all racial, ethnic and socioeconomic groups in the United States. Improvement of HPV vaccination rates will require an integrative effort that may include increased access to care, improved efficacy of provider recommendation, patient education, and system-based changes to facilitate series completion. As access to healthcare is expanded for low-income Americans, health care providers serving these communities should receive support and education regarding successful tools for integrating HPV vaccination into their practices.¹¹⁰ Patient-targeted interventions should focus on the importance of series completion among low-income and minority teens. With an integrated initiative focused on HPV awareness, widespread vaccination should be achievable across all races and demographics. Understanding the current trends as well as the barriers to vaccination will allow for the development of effective strategies to increase rates of vaccination and completion which can alter the future disparities in cervical cancer.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Funding

American Cancer Society Mentored Research Scholar Grant (MRSG-09–151–01).