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Original article| Volume 53, ISSUE 6, P756-762, December 2013

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Racial Disparities in Human Papillomavirus Vaccination: Does Access Matter?

      Abstract

      Purpose

      To examine the association between race/ethnicity and human papillomavirus (HPV) vaccine initiation and to determine how access to health care influences this relationship.

      Methods

      We used nationally representative data from the National Survey of Family Growth to assess HPV vaccine initiation in 2,168 females aged 15–24 years. A series of regression analyses were performed to determine the independent effect of race/ethnicity on HPV vaccine initiation after controlling for sociodemographic variables and health care access measures. Age-stratified regression analyses were also performed to assess whether the relationship between race/ethnicity and HPV vaccine initiation differed among females aged 15–18 and 19–24 years.

      Results

      There were significant racial/ethnic disparities in HPV vaccination; United States (US)-born Hispanics, foreign-born Hispanics, and African-Americans were less likely to have initiated vaccination than were whites (p < .001). Adjusting for sociodemographic characteristics attenuated the disparity for both US-born and foreign-born Hispanics (adjusted odds ratio [AOR], .76; 95% confidence interval [CI], .50–1.16; and AOR, .67; 95% CI, .37–1.19) but not for African-Americans (AOR, .47, 95% CI, .33–.66). Adding health care access measures further attenuated the disparity for US-born and foreign-born Hispanics (AOR, .85, 95% CI, .54–1.34; and AOR, .84, 95% CI, .45–1.55). However, African-Americans remained less likely than whites to have initiated vaccination (AOR, .49, 95% CI, .36–.68). These racial/ethnic trends were similar for females aged 15–18 and 19–24 years.

      Conclusions

      Lower rates of HPV vaccination among African-American females do not appear to be explained by differential access to health care. More research is necessary to elucidate factors contributing to HPV vaccination in this population.

      Keywords

      Implications and Contribution
      African-American females are less likely to have initiated HPV vaccination compared with whites; this cannot simply be explained by differential access to health care.
      Squamous cell cervical cancer risk begins with human papillomavirus (HPV) infection. Two strains (HPV 16 and 18) are responsible for 70% of all cervical cancer [
      • Grulich A.E.
      • Jin F.
      • Conway E.L.
      • et al.
      Cancers attributable to human papillomavirus infection.
      ]. In the United States (US), the availability of two HPV vaccines active against these HPV subtypes (Gardasil, approved in 2006 and Cervarix, approved in 2009) provides an opportunity for primary prevention of HPV infection. Given the important role of HPV vaccination in preventing cervical cancer, as well as other cancers and genital warts, the Centers for Disease Control and Prevention recommends that all girls and boys aged 11–12 years receive the three-dose vaccination series, with catch-up recommended through age 26 for girls and age 21 for boys [

      Centers for Disease Control and Prevention. HPV vaccine information for young women—fact sheet. http://www.cdc.gov/std/hpv/stdfact-hpv-vaccine-young-women.htm [accessed 01.01.13].

      ]. Because even one dose may provide significant HPV protection [
      • Kreimer A.R.
      • Rodriguez A.C.
      • Hildesheim A.
      • et al.
      Proof-of-principle evaluation of the efficacy of fewer than three doses of a bivalent HPV16/18 vaccine.
      ], initiation of the HPV vaccine series is a highly important public health goal.
      Despite the safety and efficacy of HPV vaccination [
      • Pomfret T.C.
      • Gagnon Jr., J.M.
      • Gilchrist A.T.
      Quadrivalent human papillomavirus (HPV) vaccine: A review of safety, efficacy, and pharmacoeconomics.
      ], national rates of vaccination remain suboptimal, with only 53% of adolescent girls (aged 13–17 years) [
      • Centers for Disease Control and Prevention
      National and state vaccination coverage among adolescents aged 13-17 years—United States, 2011.
      ] and 21% of young adult females (aged 19–26 years) [
      • Centers for Disease Control and Prevention
      Adult vaccination coverage—United States, 2010.
      ] reporting vaccine initiation. Given that cervical cancer is more common and is associated with higher mortality in African-American and Hispanic women than in white women [
      • Downs L.S.
      • Smith J.S.
      • Scarinci I.
      • et al.
      The disparity of cervical cancer in diverse populations.
      ,
      ], it is especially important to understand barriers to HPV vaccination for these populations. Previous multivariable analyses have had mixed conclusions regarding racial and ethnic differences in HPV vaccination among females. For adolescents (below the age of 18 or 19 years), nationally representative studies have shown lower, equivalent, and higher rates of HPV vaccine initiation among females in minority racial/ethnic groups compared with white females [
      • Wong C.A.
      • Berkowitz Z.
      • Dorell C.G.
      • et al.
      Human papillomavirus vaccine uptake among 9- to 17-year-old girls: National Health Interview Survey, 2008.
      ,
      • Lau M.
      • Lin H.
      • Flores G.
      Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children's Health.
      ,
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • et al.
      Human papillomavirus vaccination series initiation and completion, 2008-2009.
      ,
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      An update on human papillomavirus vaccine uptake among 11-17 year old girls in the United States: National Health Interview Survey, 2010.
      ,
      • Sadigh G.
      • Dempsey A.F.
      • Ruffin IV, M.
      • et al.
      National patterns in human papillomavirus vaccination: An analysis of the National Survey of Family Growth.
      ]. A recent meta-analysis including 14 local and nationally representative studies between 2007 and 2010 showed that black adolescent females were, on average, less likely to have initiated HPV vaccination compared with their white counterparts, whereas data for Hispanic females were too heterogeneous to pool [
      • Fisher H.
      • Trotter C.L.
      • Audrey S.
      • et al.
      Inequalities in the uptake of human papillomavirus vaccination: A systematic review and meta-analysis.
      ]. Studies using national data to assess vaccine initiation in young adults (over the age of 17 or 18 years) have mostly found equivalent vaccination rates for African-American, Hispanic, and white females in multivariable analyses [
      • Williams W.W.
      • Lu P.J.
      • Saraiya M.
      Factors associated with human papillomavirus vaccination among young adult women in the United States.
      ,
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      Human papillomavirus vaccine uptake among 18- to 26-year-old women in the United States: National Health Interview Survey, 2010.
      ,
      • Jain N.
      • Euler G.L.
      • Shefer A.
      • et al.
      Human papillomavirus (HPV) awareness and vaccination initiation among women in the United States, National Immunization Survey—Adult 2007.
      ,
      • Ford J.L.
      Racial and ethnic disparities in human papillomavirus awareness and vaccination among young adult women.
      ,
      • Anhang Price R.
      • Tiro J.A.
      • Saraiya M.
      • et al.
      Use of human papillomavirus vaccines among young adult women in the United States: An analysis of the 2008 National Health Interview Survey.
      ]. To our knowledge, there have been no multivariable studies using national data after 2008 to assess the relationship between race/ethnicity and HPV vaccine initiation in both adolescents and young adults.
      Racial variation in HPV vaccination, like many health disparities, is likely multifactorial. Decreased access to health care and poorer quality of care have been documented for many racial/ethnic minorities [

      Agency for Healthcare Research and Quality. Chapter 10: Priority populations, in national healthcare disparities report; 2011. http://www.ahrq.gov/qual/nhdr11/chap10.htm#racial [accessed 01.01.13].

      ]. Among adolescents and young adults, African-Americans and Hispanics are less likely to have continuous insurance coverage or to have had a doctor visit in the past year compared with age-matched whites [
      • Mulye T.P.
      • Park M.J.
      • Nelson C.D.
      • et al.
      Trends in adolescent and young adult health in the United States.
      ]. Hispanic adolescents and young adults are also less likely to have a usual place to go to when they are sick than are their white or African-American counterparts [
      • Mulye T.P.
      • Park M.J.
      • Nelson C.D.
      • et al.
      Trends in adolescent and young adult health in the United States.
      ]. Given that the HPV vaccine must be administered by a health care professional, decreased access to health services may contribute to the under-vaccination of minority females. In addition, vaccination is estimated to cost $390 without insurance [

      Centers for Disease Control and Prevention. HPV vaccine information for young women—fact sheet. http://www.cdc.gov/std/hpv/stdfact-hpv-vaccine-young-women.htm [accessed 01.01.13].

      ], although these costs may be mitigated by Vaccines for Children, a federal program that offers vaccination to uninsured or underinsured children under the age of 19 years, and pharmaceutical company–sponsored assistance programs. Many studies have identified an association between use of health care resources and HPV vaccination [
      • Wong C.A.
      • Berkowitz Z.
      • Dorell C.G.
      • et al.
      Human papillomavirus vaccine uptake among 9- to 17-year-old girls: National Health Interview Survey, 2008.
      ,
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • et al.
      Human papillomavirus vaccination series initiation and completion, 2008-2009.
      ,
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      An update on human papillomavirus vaccine uptake among 11-17 year old girls in the United States: National Health Interview Survey, 2010.
      ,
      • Williams W.W.
      • Lu P.J.
      • Saraiya M.
      Factors associated with human papillomavirus vaccination among young adult women in the United States.
      ,
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      Human papillomavirus vaccine uptake among 18- to 26-year-old women in the United States: National Health Interview Survey, 2010.
      ,
      • Ford J.L.
      Racial and ethnic disparities in human papillomavirus awareness and vaccination among young adult women.
      ,
      • Moss J.L.
      • Gilkey M.B.
      • Reiter P.L.
      • et al.
      Trends in HPV vaccine initiation among adolescent females in North Carolina, 2008-2010.
      ,
      • Perkins R.B.
      • Brogly S.B.
      • Adams W.G.
      • et al.
      Correlates of human papillomavirus vaccination rates in low-income, minority adolescents: A multicenter study.
      ,
      • Tiro J.A.
      • Pruitt S.L.
      • Bruce C.M.
      • et al.
      Multilevel correlates for human papillomavirus vaccination of adolescent girls attending safety net clinics.
      ], but whether limited access to health care explains racial/ethnic disparities in HPV vaccination has not been thoroughly explored.
      Because HPV vaccination has been shown to decrease the prevalence of oncogenic HPV strains and cervical neoplasia [
      • Pomfret T.C.
      • Gagnon Jr., J.M.
      • Gilchrist A.T.
      Quadrivalent human papillomavirus (HPV) vaccine: A review of safety, efficacy, and pharmacoeconomics.
      ], it is important to identify disparities in vaccination. Moreover, an analysis of the role of health care access in explaining disparities in HPV vaccination may clarify whether making the vaccine more accessible is likely to increase vaccine uptake in vulnerable populations. Therefore, the authors used nationally representative data to examine the independent effect of race/ethnicity on HPV vaccine initiation in adolescent girls and young women and to determine whether access to health care influences this relationship.

      Methods

      Data source

      This study used data from the 2006–2010 National Survey of Family Growth (NSFG) [

      National Center for Health Statistics. National survey of Family Growth 2006—2010. http://www.cdc.gov/nchs/nsfg.htm [accessed 01.01.13].

      ], a national cross-sectional survey. The NSFG is designed and administered by the National Center for Health Statistics, an agency of the US Department of Health and Human Services, to provide national estimates of factors affecting reproductive health. Interviewing for the 2006–2010 NSFG occurred between June 2006 and June 2010, and the full data set was released to the public in October 2011. One of the key independent variables used for these analyses (whether the respondent has a usual source of health care) was added to the survey in July 2008; thus, the authors used only data collected between July 2008 and June 2010 for this study. Each year of interviewing in the NSFG can be considered a nationally representative sample, and results from multiple years can be combined for more reliable population estimates.

      Study sample

      The NSFG uses a national probability sample designed to represent men and women aged 15–44 years, living in households in all 50 states and the District of Columbia. Teenage, African-American, Hispanic, and female participants were oversampled, and the NSFG provides sampling weights to adjust for the different sampling and response rates within the survey sample. Self-reported HPV vaccination status was assessed only for female participants under the age of 25 years; thus, this cohort comprised the study population.

      Study outcome

      The primary outcome of interest was whether the participant had ever received the HPV vaccine. Participants were first asked whether they had heard of “the cervical cancer vaccine, HPV shot, or Gardasil.” Because this question was added to the NSFG survey in 2007, soon after the national release of Gardasil but before the release of Cervarix, only Gardasil is listed by name. If a participant said that she had heard of the HPV vaccine, she was subsequently asked about her HPV vaccination status. If a participant had received at least one of the three HPV vaccine shots, she was considered to have received the vaccine. The NSFG does not assess how many doses of the HPV vaccine respondents have received. If a participant indicated that she had received no HPV vaccination, or if she had not heard of the HPV vaccine, she was considered not to have been vaccinated in this study.

      Independent variables

      The primary independent variable of interest was self-reported race/ethnicity. Participants were asked whether they were Hispanic, Latino, or of Spanish origin. Those who answered affirmatively were classified as Hispanic. Participants were subsequently categorized as non-Hispanic white, non-Hispanic black, or non-Hispanic other, based on a follow-up question about their racial background. Participants categorized as non-Hispanic other (n = 135) were removed from the analysis because this group was too small and too heterogeneous to generate meaningful conclusions. Participants were also asked whether they were born in the US. Given the large number of Hispanic females born outside the US, Hispanics were divided into US-born and foreign-born.
      Sociodemographic factors including age, religion, parent education level, household income, place of residence (urban, suburban, or rural), and number of lifetime male sexual partners were examined as potential confounders. Participant education was initially considered as a covariate but was ultimately excluded because of its high correlation with age in this young sample. Two health care access variables that could influence vaccination status were also examined: insurance status and whether the participant had a usual place for receiving health care.

      Statistical analysis

      Sociodemographic and access variables were compared by race/ethnicity using chi-square tests for all categorical variables. Bivariate associations between each covariate and the primary outcome, HPV vaccine initiation, were then assessed, and unadjusted odds ratios (ORs) were calculated for each pair.
      To understand the role of health care access as a confounder for the association between race/ethnicity and HPV vaccine initiation, a series of regression analyses was conducted. The unadjusted relationship between race/ethnicity and HPV vaccination was first examined (Model 1). Model 2 adjusted for sociodemographic variables that were associated with HPV vaccination at p < .10 in bivariate analyses, with the exception that the authors decided a priori to force household income into the model. Model 3 adjusted for all of the sociodemographic variables included in Model 2 as well as the two health care access variables. A change of at least 10% between Models 2 and 3 was considered a confounding effect by health care access [
      • Bliss R.
      • Weinberg J.
      • Webster T.
      • et al.
      Determining the probability distribution and evaluating sensitivity and false positive rate of a confounder detection method applied to logistic regression.
      ].
      Given that existing national studies have restricted their analyses to either adolescents or young adults, age-stratified analyses were conducted to enable comparison with existing published data. The same series of regression analyses described above was performed for each age group (15–18 and 19–24 years), using the same covariates as in the main analyses.
      Statistics for this analysis were performed using Stata 11 SE software (StataCorp, College Station, TX), using appropriate adjustment for the NSFG's complex sample design. All percentages shown have been weighted to reflect national estimates; however, actual sample sizes are also provided to give the reader an indication of the reliability of the estimates. The University of Pittsburgh Institutional Review Board approved this study.

      Results

      Our study sample included 2,168 females aged 15–24 years. Table 1 shows the sociodemographic characteristics of the study sample by race/ethnicity. Briefly, 63.6% were white, 13.8% were US-born Hispanic, 5.3% were foreign-born Hispanic, and 17.2% were African-American. The four groups differed significantly in all sociodemographic and health care access variables. For example, US-born and foreign-born Hispanics were more likely to be uninsured than were whites (25.9%, 41.1%, and 16.3%, respectively). African-Americans were more likely to have public insurance than were whites (44.4% and 17.2%, respectively). Both US-born and foreign-born Hispanics and African-Americans were less likely than whites to have a usual source of health care (76.1%, 71.1%, 79.6%, and 84.7%, respectively).
      Table 1Sociodemographic and health care access characteristics, by race/ethnicity
      VariableWhite, % (n = 1,110)Hispanic (United States–born), % (n = 405)Hispanic (foreign-born), % (n = 149)African-American, % (n = 504)p Value
      Total population63.613.85.317.2
      Age, years.001
       15–1835.246.826.940.3
       19–2464.853.273.159.7
      Religion<.001
       Protestant47.321.714.878.1
       Catholic20.158.875.15.4
       Other7.73.92.03.3
       None24.915.68.113.2
      Parent education level
      Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
      <.001
       Less than high school2.425.754.37.4
       High school diploma20.927.521.229.9
       At least some college76.746.824.562.7
      Household income, % poverty level
      Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
      <.001
       <10022.738.249.243.8
       100–19924.429.329.224.5
       ≥20052.932.521.631.7
      Place of residence
      In the NSFG, place of residence is divided into three groups consistent with US Office of Management and Budget definitions: Metropolitan Statistical Area (MSA)–central city, MSA–other, and non-MSA. These roughly correspond to urban, suburban, and rural settings.
      <.001
       Urban24.037.241.358.3
       Suburban53.956.449.037.6
       Rural22.16.49.74.1
      Lifetime male sexual partners<.001
       034.136.430.331.7
       1–334.047.151.027.4
       >331.916.518.740.9
      Insurance status<.001
       No insurance
      Participants with only single service plans were considered to have no insurance.
      16.325.941.117.5
       Public insurance17.237.235.444.4
       Private insurance66.536.923.538.1
      Has a usual source of health care84.776.171.179.6.002
      n = 2,168; weighted to reflect US female household population.
      a Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
      b Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
      c In the NSFG, place of residence is divided into three groups consistent with US Office of Management and Budget definitions: Metropolitan Statistical Area (MSA)–central city, MSA–other, and non-MSA. These roughly correspond to urban, suburban, and rural settings.
      d Participants with only single service plans were considered to have no insurance.
      Table 2 shows results from the bivariate and unadjusted analyses. Overall, only 28.4% of participants had received at least one dose of an HPV vaccine. United States–born and foreign-born Hispanics and African-Americans were significantly less likely than whites to have been vaccinated (unadjusted OR, .65, 95% confidence interval [CI], .44–.95; OR, .39, 95% CI, .23–.68; and OR, .45, 95% CI, .33–.62, respectively). Females who were aged 15–18 years, had at least one parent with a high school diploma or some college education, had public or private insurance, or had a usual source of health care had higher rates of vaccine initiation in unadjusted analyses.
      Table 2Unadjusted odds of human papillomavirus vaccine initiation
      Human papillomavirus vaccine initiation, %Unadjusted odds ratiop Value
      Total sample28.4
      Race/ethnicity<.001
       White33.1Reference
       Hispanic, United States–born24.2.65 (.44–.95).028
       Hispanic, foreign- born16.2.39 (.23–.68).001
       African-American18.2.45 (.33–.62)<.001
      Age, years.001
       15–1834.7Reference
       19–2424.6.62 (.46–.82).001
      Religion.200
       Protestant27.0Reference
       Catholic31.01.22 (.90–1.65).197
       Other21.1.72 (.45–1.17).181
       None30.41.18 (.85–1.65).319
      Parent education level
      Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
      <.001
       Less than high school12.0Reference
       High school diploma24.32.35 (1.40–3.94).002
       At least some college32.03.45 (1.98–6.00)<.001
      Household income, % poverty level
      Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
      .150
       <10024.8Reference
       100–19929.01.24 (.92–1.67).152
       ≥20030.51.33 (.98–1.81).070
      Place of residence
      In the NSFG, place of residence is divided into three groups consistent with US Office of Management and Budget definitions: Metropolitan Statistical Area (MSA)–central city, MSA–other, and non-MSA. These roughly correspond to urban, suburban, and rural settings.
      .426
       Urban26.4Reference
       Suburban28.01.08 (.82–1.43).569
       Rural33.51.40 (.75–2.65).286
      Lifetime male sexual partners.532
       028.2Reference
       1–330.41.11 (.82–1.50).491
       >326.3.91 (.61–1.36).633
      Insurance status<.001
       No insurance
      Participants with only single service plans were considered to have no insurance.
      10.2Reference
       Public insurance26.13.12 (1.98–4.90)<.001
       Private insurance35.74.91 (3.03–7.95)<.001
      Has a usual source of health care<.001
       No12.1Reference
       Yes32.03.43 (2.08–5.65)<.001
      n = 2,168; weighted to reflect the US female household population.
      a Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
      b Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
      c In the NSFG, place of residence is divided into three groups consistent with US Office of Management and Budget definitions: Metropolitan Statistical Area (MSA)–central city, MSA–other, and non-MSA. These roughly correspond to urban, suburban, and rural settings.
      d Participants with only single service plans were considered to have no insurance.
      Table 3 shows results from the multivariable regression analyses. After adjusting for sociodemographic variables (age, parent education level, and household income) in Model 2, the odds of HPV vaccine initiation among both US-born and foreign-born Hispanics increased and became not significantly different from the odds of HPV vaccine initiation among whites (adjusted OR (AOR), .76, 95% CI, .50–1.16; and AOR, .67, 95% CI, .37–1.19, respectively). Adding the two health care access variables (insurance and has a usual source of health care) in Model 3 further increased the odds of vaccination for US-born and foreign-born Hispanics (AOR, .85, 95% CI, .54–1.34; and AOR, .84, 95% CI, .45–1.55, respectively). However, African-Americans remained significantly less likely to have reported vaccination than whites after adjusting for sociodemographic factors in Model 2 (AOR, .47; 95% CI, .33–.66). The addition of health care access variables in Model 3 did not substantially alter this disparity (AOR, .49, 95% CI, .36–.68). In the final adjusted analysis (Model 3), females who were aged 15–18 years, had at least one parent with some college education, had public or private insurance, and had a usual source of health care had a higher likelihood of HPV vaccine initiation.
      Table 3Adjusted odds of human papillomavirus vaccine initiation
      Model 1
      Unadjusted odds ratios by race/ethnicity, replicated from Table 2.
      Model 2
      Model includes race/ethnicity, age, parent education level, and household income.
      Model 3
      Model includes race/ethnicity, age, parent education level, household income, insurance status, and usual source of health care.
      ORp ValueORp ValueORp Value
      Race/ethnicity
       WhiteReferenceReferenceReference
       Hispanic, US-born.65 (.44–.95).028.76 (.50–1.16).195.85 (.54–1.34).484
       Hispanic, foreign-born.39 (.23–.68).001.67 (.37–1.19).166.84 (.45–1.55).569
       African-American.45 (.33–.62)<.001.47 (.33–.66)<.001.49 (.36–.68)<.001
      Age, years
       15–18ReferenceReference
       19–24.59 (.44–.79).001.71 (.53–.95).023
      Parent education level
      Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
       Less than high schoolReferenceReference
       High school diploma2.05 (1.11–3.77).0221.83 (.98–3.41).056
       At least some college2.85 (1.43–5.70).0042.34 (1.16–4.70).018
      Household income, % poverty level
      Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
       <100ReferenceReference
       100–1991.11 (.82–1.51).4771.09 (.80–1.49).575
       ≥2001.06 (.75–1.50).719.89 (.62–1.28).519
      Insurance status
       No insurance
      Participants with only single service plans were considered to have no insurance.
      Reference
       Public insurance2.71 (1.70–4.33)<.001
       Private insurance3.36 (2.10–5.36)<.001
      Has usual source of health care
       NoReference
       Yes2.45 (1.49–4.02).001
      n = 2,168; weighted to reflect the US female household population.
      OR = odds ratio.
      a Unadjusted odds ratios by race/ethnicity, replicated from Table 2.
      b Model includes race/ethnicity, age, parent education level, and household income.
      c Model includes race/ethnicity, age, parent education level, household income, insurance status, and usual source of health care.
      d Participants who had no mother or father were considered to have a mother or father with less than high school education, respectively. Participants who did not know their mother's or father's education were considered to have a mother or father with at least some college education, respectively.
      e Poverty threshold based on 2008–2010 level defined by the US Census Bureau, which takes into account total household income and number.
      f Participants with only single service plans were considered to have no insurance.
      Table 4 shows the results from the age-stratified analyses. Because of comparable trends among US-born and foreign-born Hispanics in the full sample, we combined these groups in the stratified analyses to improve the reliability of our estimates. Among the 872 adolescent girls aged 15–18 years, Hispanics and African-Americans were significantly less likely to have initiated HPV vaccination in unadjusted analysis compared with whites (OR, .48, 95% CI, .31–.72; and OR, .41, 95% CI, .27–.62, respectively). Adjusting for sociodemographic variables (parent education level and household income) substantially increased the odds of vaccination for Hispanics, which became not significantly different from the odds of vaccination among white adolescents (AOR, .64; 95% CI, .38–1.09). Adding the two health care access variables into the model further increased the odds of vaccination for Hispanics (AOR, .73; 95% CI, .42–1.27). Conversely, African-Americans remained less likely to have initiated vaccination after adjusting for sociodemographic covariates (AOR, .44; 95% CI, .28–.68). The addition of health care access variables also did not substantially affect the odds of vaccine initiation for African-American adolescents (AOR, .47; 95% CI, .29–.75).
      Table 4Adjusted odds of human papillomavirus vaccine initiation, stratified by age
      Model 1
      Unadjusted odds ratios by race/ethnicity.
      Model 2
      Model includes race/ethnicity, parent education level, and household income.
      Model 3
      Model includes race/ethnicity, parent education level, household income, insurance status, and usual source of health care.
      ORp ValueORp ValueORp Value
      Ages 15–18 years (n = 872)
       WhiteReferenceReferenceReference
       Hispanic.48 (.31–.72).001.64 (.38–1.09).100.73 (.42–1.27).262
       African-American.41 (.27–.62)<.001.44 (.28–.68).001.47 (.29–.75).002
      Ages 19–24 years (n = 1,296)
       WhiteReferenceReferenceReference
       Hispanic.62 (.35–1.08).088.88 (.48–1.63).6781.03 (.54–2.00).920
       African-American.46 (.27–.78).005.47 (.27–.82).009.51 (.29–.88).016
      n = 2,168; weighted to reflect the US female household population.
      OR = odds ratio.
      a Unadjusted odds ratios by race/ethnicity.
      b Model includes race/ethnicity, parent education level, and household income.
      c Model includes race/ethnicity, parent education level, household income, insurance status, and usual source of health care.
      For the 1,296 young women aged 19–24 years, Hispanics were less likely to have initiated vaccination, but this did not reach statistical significance (OR, .62; 95% CI, .35–1.08). Adjusting for sociodemographic variables increased the odds of vaccination for Hispanics (AOR, .88; 95% CI, .48–1.63); the odds were further increased with the addition of health care access variables into the model (AOR, 1.03; 95% CI, .54–2.00). Conversely, African-Americans were significantly less likely to have reported HPV vaccination compared with whites across all three models, with no attenuation in the disparity even after adjusting for sociodemographic variables and health care access variables (OR, .46, 95% CI, .27–.78 in Model 1; AOR, .47, 95% CI, .27–.82 in Model 2; and AOR, .51, 95% CI, .29–.88 in Model 3).

      Discussion

      In this nationally representative sample of adolescent girls and young women interviewed between 2008 and 2010, African-Americans were significantly less likely than whites to have initiated HPV vaccination, even after taking into account sociodemographic and health care access covariates. This disparity persisted among both younger (aged 15–18 years) and older (aged 19–24 years) African-Americans. Disparities in HPV vaccination for Hispanics, on the other hand, were fully attenuated after adjusting for sociodemographic and health care access variables.
      Our results among adolescents aged 15–18 years are consistent with a recent meta-analysis showing that black female adolescents are less likely to have initiated HPV vaccination compared with their white counterparts [
      • Fisher H.
      • Trotter C.L.
      • Audrey S.
      • et al.
      Inequalities in the uptake of human papillomavirus vaccination: A systematic review and meta-analysis.
      ]. However, several studies have shown equal or higher vaccine initiation among adolescents from racial/ethnic minority groups [
      • Centers for Disease Control and Prevention
      National and state vaccination coverage among adolescents aged 13-17 years—United States, 2011.
      ,
      • Wong C.A.
      • Berkowitz Z.
      • Dorell C.G.
      • et al.
      Human papillomavirus vaccine uptake among 9- to 17-year-old girls: National Health Interview Survey, 2008.
      ,
      • Lau M.
      • Lin H.
      • Flores G.
      Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children's Health.
      ,
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • et al.
      Human papillomavirus vaccination series initiation and completion, 2008-2009.
      ,
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      An update on human papillomavirus vaccine uptake among 11-17 year old girls in the United States: National Health Interview Survey, 2010.
      ,
      • Moss J.L.
      • Gilkey M.B.
      • Reiter P.L.
      • et al.
      Trends in HPV vaccine initiation among adolescent females in North Carolina, 2008-2010.
      ,
      • Centers for Disease Control and Prevention
      National and state vaccination coverage among adolescents aged 13 through 17 years—United States, 2010.
      ]. One explanation for the inconsistency with other studies is that patterns of HPV vaccination may be changing over time. Of note, the 2010 National Immunization Study (NIS)-Teen demonstrated increased HPV vaccine initiation in Hispanic girls and comparable rates of vaccine initiation among African-American and white girls ages 13–17 years (56.2%, 48.9%, and 45.8%, respectively) [
      • Centers for Disease Control and Prevention
      National and state vaccination coverage among adolescents aged 13 through 17 years—United States, 2010.
      ]. Then, the 2011 NIS-Teen showed increased HPV vaccine initiation in both Hispanic and African-American girls compared with white girls (65%, 56%, and 47.5%, respectively) [
      • Centers for Disease Control and Prevention
      National and state vaccination coverage among adolescents aged 13-17 years—United States, 2011.
      ]. These findings suggest that patterns of HPV vaccination are rapidly changing in adolescent girls, with greater increases in vaccine initiation among Hispanics and African-Americans compared with whites. These changes may reflect increasing provider and patient familiarity with the HPV vaccine, as well as federal vaccine programs offering vaccine assistance and outreach to children over time. The NIS-Teen's different racial/ethnic patterns of HPV vaccine initiation, as well as the higher rates of HPV vaccine initiation overall compared with our findings, may also reflect different methods of obtaining vaccination status in the NIS-Teen compared with the NSFG. In particular, whereas the NSFG relies solely on self-report, the NIS-Teen confirms parental report of vaccination status with provider immunization records. A recent study demonstrated that parents of Hispanic and African-American adolescents were less likely than parents of white adolescents to correctly identify that their daughters had received HPV vaccination [
      • Ojha R.P.
      • Tota J.E.
      • Offutt-Powell T.N.
      • et al.
      The accuracy of human papillomavirus vaccination status based on adult proxy recall or household immunization records for adolescent females in the United States: Results from the National Immunization Survey-Teen.
      ]; likewise, it is possible that the Hispanic and African-American adolescents in our study were underreporting HPV vaccination. Whereas the NIS-Teen's vaccination data are slightly more recent and perhaps less subject to recall error, using the NSFG for our analyses allowed us to capture and examine personal participant information such as sexual activity and usual source of health care.
      For young women aged 19–24 years, our results are consistent with several local studies showing significantly lower HPV vaccine initiation in African-American young adults compared with their white counterparts [
      • Bednarczyk R.A.
      • Birkhead G.S.
      • Morse D.L.
      • et al.
      Human papillomavirus vaccine uptake and barriers: Association with perceived risk, actual risk and race/ethnicity among female students at a New York State university, 2010.
      ,
      • Schluterman N.H.
      • Terplan M.
      • Lydecker A.D.
      • et al.
      Human papillomavirus (HPV) vaccine uptake and completion at an urban hospital.
      ]. However, a recent analysis of the 2010 National Health Interview Survey (NHIS) found that lower rates of vaccine initiation among Hispanic and African-American females compared with whites aged 19–26 years (18.1%, 18.8%, and 24.9%, respectively) were not statistically significant [
      • Laz T.H.
      • Rahman M.
      • Berenson A.B.
      Human papillomavirus vaccine uptake among 18- to 26-year-old women in the United States: National Health Interview Survey, 2010.
      ]. Our different results may reflect methodological differences between the NHIS and NSFG, including the slightly smaller sample size (n = 1,892) and wider age range (ages 18–26 years) in the NHIS.
      Interestingly, we found that disparities in HPV vaccine initiation among Hispanics, but not African-Americans, were attenuated after adjusting for health care access variables. Given that Hispanics were the least likely racial/ethnic group to have insurance or a usual source of health care, our findings suggest that improving these health care access parameters could lead to increased vaccination rates in this population. On the other hand, our findings in African-Americans suggest that other unmeasured patient- or provider-level factors contribute to under-vaccination and that alternate strategies will need to be identified to increase HPV vaccination. Although the data are limited, negative attitudes toward the HPV vaccine appear to be barriers to HPV vaccination among African-American females [
      • Lechuga J.
      • Swain G.R.
      • Weinhardt L.S.
      The cross-cultural variation of predictors of human papillomavirus vaccination intentions.
      ,
      • Wilson R.
      • Brown D.R.
      • Boothe M.A.
      • et al.
      Knowledge and acceptability of the HPV vaccine among ethnically diverse black women.
      ]. Conversely, provider recommendation for HPV vaccination has emerged as an important enabling factor for increasing HPV vaccination among African-American females [
      • Hamlish T.
      • Clarke L.
      • Alexander K.A.
      Barriers to HPV immunization for African American adolescent females.
      ,
      • Sanders Thompson V.L.
      • Arnold L.D.
      • Notaro S.R.
      African American parents' HPV vaccination intent and concerns.
      ]. Whereas there is a positive association between receiving a recommendation and HPV vaccine receipt among white, Hispanic, and African-American females, the relationship is strongest for African-Americans [
      • Ylitalo K.R.
      • Lee H.
      • Mehta N.K.
      Health care provider recommendation, human papillomavirus vaccination, and race/ethnicity in the US National Immunization Survey.
      ]. Unfortunately, African-Americans are less likely to receive an HPV vaccine recommendation from a provider compared with whites [
      • Lau M.
      • Lin H.
      • Flores G.
      Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children's Health.
      ,
      • Ylitalo K.R.
      • Lee H.
      • Mehta N.K.
      Health care provider recommendation, human papillomavirus vaccination, and race/ethnicity in the US National Immunization Survey.
      ]. These findings indicate that improving access to health care may be insufficient in increasing HPV vaccination among African-Americans; perhaps, addressing negative attitudes and beliefs and increasing provider recommendation for HPV vaccination will be fruitful in increasing HPV vaccination rates in this population.
      Our study had several important limitations. First, sociodemographic characteristics and health care access variables were assessed at the time of interview, rather than at the time of vaccination, and may have changed over time. Similarly, date of vaccination is not documented by the NSFG, so the authors cannot discern whether this study's findings reflect current or previous vaccine uptake patterns. Because the NSFG does not mention Cervarix when assessing HPV vaccination status, it is possible that some participants who received this vaccine were not aware of its indication or were not familiar that it is a product similar to Gardasil. The NSFG also does not confirm vaccination status with immunization records, which could lead to misclassification bias. Finally, the NSFG assesses only vaccine initiation, rather than completion of the three dose series, which appears to differ by race [
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • et al.
      Human papillomavirus vaccination series initiation and completion, 2008-2009.
      ]. However, given that even one HPV vaccine dose effectively reduces HPV acquisition [
      • Kreimer A.R.
      • Rodriguez A.C.
      • Hildesheim A.
      • et al.
      Proof-of-principle evaluation of the efficacy of fewer than three doses of a bivalent HPV16/18 vaccine.
      ], racial/ethnic disparities in HPV vaccine initiation are a significant public health problem.
      In summary, after controlling for sociodemographic factors and markers of access to health care, African-American females aged 15–24 years were significantly less likely to have initiated HPV vaccination compared with white females. Observed disparities in HPV vaccine initiation among both US-born and foreign-born Hispanics, on the other hand, were largely explained by sociodemographic and health care access variables. Research is needed to further elucidate the reasons for under-vaccination among African-American adolescents and young women, and to identify ways in which providers and health care systems may improve HPV vaccine uptake in this vulnerable population.

      Acknowledgments

      The project described was supported by the University of Pittsburgh's Clinical and Translational Sciences Institute (National Institutes of Health through Grants UL1 RR024153 and UL1TR000005). An abstract of this work was submitted to the 2013 Society of General Internal Medicine Meeting.

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