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Race, Ethnicity, and Income Factors Impacting Human Papillomavirus Vaccination rates

      Abstract

      Background

      Human papillomavirus (HPV) infection and cervical cancer disproportionately affect low-income and minority women. HPV vaccines have the potential to either reduce or exacerbate racial disparities in HPV-related diseases and cervical cancers, depending on the equitability of vaccine uptake.

      Objectives

      This review aims to identify barriers and facilitators of equitable uptake of HPV vaccination among low-income and minority girls. This review discusses factors related to race, ethnicity, and income that are associated with initiation and completion rates of the 3-dose HPV vaccine series and presents targets for intervention.

      Methods

      We reviewed relevant English-language literature to identify current vaccination rates and factors associated with vaccine uptake. Study findings related to race (black, Latino, Asian), and incomes were summarized.

      Results

      Current trends in the United States indicate low uptake among all adolescents, and that rates stagnated between 2011 and 2012. Low-income and minority adolescents are equally or more likely to start the HPV vaccination series than are white and higher-income adolescents, but are less likely to complete all 3 shots. Provider recommendation is a key factor in HPV vaccination, and minorities are less likely to report receiving recommendations for HPV vaccination.

      Conclusions

      As black, Hispanic, and Asian populations continue to grow in the United States over the next several decades, it is imperative that we not only improve HPV vaccination rates overall, but also focus on high-risk populations to prevent an increase in cervical cancer disparities.

      Key words

      Racial/ethnic and income disparities in cervical cancer and human papillomavirus vaccination

      Human papillomavirus (HPV) is ubiquitous,
      • Clifford G.
      • Franceschi S.
      • Diaz M.
      • et al.
      Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases.
      but cervical cancer disproportionately affects poor and minority women. An estimated 12,000 women are diagnosed with cervical cancer annually in the United States,

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Stat Fact Sheets: Cervix uteri cancer. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed November 4, 2013.

      and >500,000 women worldwide develop cervical cancer each year.
      • Denny L.
      The prevention of cervical cancer in developing countries.
      In the United States, cervical cancer incidence is nearly twice as high in counties with poverty levels >20% compared with those with poverty levels <10%,

      Centers for Disease Control and Prevention. HPV-associated cancers and poverty levels. http://wwwcdcgov/cancer/hpv/statistics/povertyhtm. Accessed February 27, 2012.

      and cervical cancer incidence and mortality are 25% and 95% higher, respectively, among blacks and 53% and 41% higher for Latinas compared with whites.

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Incidence-mortality. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed October 7, 2011.

      Rates of cervical cancer are inversely proportional to screening and treatment access, and poor and minority women face more barriers to health care access; therefore, higher rates of cervical cancer are found in US regions with large minority and impoverished populations.

      US Cancer Statistics: 1999–2009 incidence and mortality Web-based report. http://www.cdc.gov/uscs. Accessed September 1, 2013.

      HPV causes nearly all cervical cancer,
      • Clifford G.
      • Franceschi S.
      • Diaz M.
      • et al.
      Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases.
      with genotypes 16 and 18 accounting for ~70% of cervical cancer worldwide.
      • Kahn J.A.
      • Cooper H.P.
      • Vadaparampil S.T.
      • et al.
      Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians.
      Low-risk HPV, genotypes 6 and 11, account for 90% of benign disease, such as genital warts.
      • Kahn J.A.
      • Cooper H.P.
      • Vadaparampil S.T.
      • et al.
      Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians.
      Two vaccines are currently recommended in the United States: the quadrivalent vaccine (HPV4)
      Trademark: Gardasil® (Merck Sharp & Dohme Corp., Ambler, Pennsylvania).
      and the bivalent vaccine (HPV2).
      Trademark: Cervarix® (GlaxoSmithKline, Research Triangle Park, North Carolina).
      Advisory Committee on Immunization Practices
      Quadrivalent human papillomavirus vaccine: recommendations of the advisory comitte on immunization practices.
      Advisory Committee on Immunization Practices
      FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP).
      Both vaccines prevent up to 98% of HPV 16/18–related cervical dysplasia, the precursor to cervical cancer. The quadrivalent vaccine also prevents vaginal, vulvar, and anal dysplasia as well as genital warts, and is also indicated for males.
      Advisory Committee on Immunization Practices
      Quadrivalent human papillomavirus vaccine: recommendations of the advisory comitte on immunization practices.
      Advisory Committee on Immunization Practices
      FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP).
      Since the licensures of these vaccines, vaccine-type HPV prevalence (HPV 6, 11, 16, and 18) decreased from 11.5% in 2003–2006 to 5.1% in 2007–2010 among teenagers aged 14 to 19 years, a decline of 56%; the prevalence of high-risk HPV decreased by 50%.
      • Markowitz L.E.
      • Hariri S.
      • Lin C.
      • et al.
      Reduction in human papillomavirus (HPV) prevalence among young women following HPV vaccine introduction in the United States, National Health and Nutrition Examination Surveys, 2003–2010.
      Routine vaccination is recommended at age 11 or 12 years, with catch-up vaccination through age 26 years.
      Advisory Committee on Immunization Practices
      Quadrivalent human papillomavirus vaccine: recommendations of the advisory comitte on immunization practices.
      Advisory Committee on Immunization Practices
      FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP).
      The recommended vaccination age of 11 or 12 years was chosen to minimize the likelihood of HPV exposure before vaccination; 6.2% of adolescents in the United States initiate sexual activity before age 13 years.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      Despite these recommendations, however, the overall rates of initiating and completing the HPV vaccination series among US adolescents are only 54% and 33% respectively,

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      which are statistically unchanged from 2011 to 2012.
      Black and Latina, low-income, urban, and publicly insured adolescents initiate HPV vaccination at equivalent or higher rates than do their white, higher-income counterparts.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      However, these groups are consistently less likely to complete the series than are white, suburban, privately insured, or affluent adolescents,
      • Chou B.
      • Krill L.S.
      • Horton B.B.
      • et al.
      Disparities in human papillomavirus vaccine completion among vaccine initiators.
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • Markowitz L.E.
      Human papillomavirus vaccination series initiation and completion, 2008–2009.
      • Niccolai L.M.
      • Mehta N.R.
      • Hadler J.L.
      Racial/ethnic and poverty disparities in human papillomavirus vaccination completion.
      • Gold R.
      • Naleway A.L.
      • Jenkins L.L.
      • et al.
      Completion and timing of the three-dose human papillomavirus vaccine series among adolescents attending school-based health centers in Oregon.
      • Tan W.
      • Viera A.J.
      • Rowe-West B.
      • et al.
      The HPV vaccine: are dosing recommendations being followed?.
      • Dempsey A.
      • Cohn L.
      • Dalton V.
      • Ruffin M.
      Patient and clinic factors associated with adolescent human papillomavirus vaccine utilization within a university-based health system.
      so their rates of complete vaccination are similar (Figure).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      Universally high rates of HPV vaccination could substantially reduce disparities in cervical cancer, but lower rates of complete vaccination in vulnerable populations could widen racial/ethnic and socioeconomic disparities in cervical cancer in the future. This article reviews factors associated with HPV vaccine acceptability, initiation, and series completion among adolescents of different racial, ethnic, and socioeconomic groups in the United States.
      Figure thumbnail gr1
      FigureRates of human papillomavirus (HPV) vaccine series initiation and completion in black, Latina, and white girls and girls below and above the poverty level.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      *P < 0.05 versus non-Hispanic white and above/below poverty.

      Materials and Methods

      We reviewed relevant English-language literature to identify current vaccination rates and factors associated with vaccine uptake. Study findings related to race (black, Latino, Asian) and incomes were summarized.

      Results

       Factors affecting HPV vaccination among young black women

      Approximately 14% of US women

      Vaccines for Children Program. http://www.cdc.gov/vaccines/programs/vfc/index.html. Accessed August 31, 2013.

      self-identify as black or African American. Black women have higher rates of HPV infections than do women of other racial/ethnic groups, which increases the importance of early HPV vaccination for black girls.
      • Hariri S.
      • Unger E.R.
      • Sternberg M.
      • et al.
      Prevalence of genital human papillomavirus among females in the United States, the National Health And Nutrition Examination Survey, 2003–2006.
      • Dunne E.F.
      • Unger E.R.
      • Sternberg M.
      • et al.
      Prevalence of HPV infection among females in the United States.
      The 2011, the Youth Risk Behavior report found that more black teens (60%) reported having sexual intercourse than did Latina (48.6%) and white (44.3%) teens.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      One possible explanation is that black girls complete puberty earlier than do girls of other races,
      • Sun S.S.
      • Schubert C.M.
      • Chumlea W.C.
      • et al.
      National estimates of the timing of sexual maturation and racial differences among US children.
      which in turn may influence the age of sexual debut. Nearly 14% of blacks initiate sexual intercourse prior to age 13 years, compared with 7.1% of Latinas and 3.9% of whites.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      Nearly one fourth of black teens reported 4 or more lifetime partners, compared with <15% of Latinas and whites.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      At the time of college entry, 87% of black students were sexually experienced, with an average of 6 lifetime partners,
      • Bynum S.A.
      • Brandt H.M.
      • Annang L.
      • et al.
      Do health beliefs, health care system distrust, and racial pride influence HPV vaccine acceptability among African American college females?.
      underscoring the importance of early vaccination to maximize vaccine efficacy.
      Because parental permission is required for vaccination of girls under age 18 years, parental attitudes and behavior play a central role in vaccine uptake. Table I summarizes barriers faced by girls of different races/ethnicities. Over 70% of black mothers support HPV vaccination, and studies examining parents’ intention to vaccinate their daughters found no racial differences in levels of parental support for vaccination.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      • Olshen E.
      • Woods E.R.
      • Austin S.B.
      • et al.
      Parental acceptance of the human papillomavirus vaccine.
      • Brawner B.M.
      • Baker J.L.
      • Voytek C.D.
      • et al.
      The development of a culturally relevant, theoretically driven HPV prevention intervention for urban adolescent females and their parents/guardians.
      • Gainforth H.L.
      • Cao W.
      • Latimer-Cheung A.E.
      Message framing and parents’ intentions to have their children vaccinated against HPV.
      • Roche K.C.
      • Wiechens N.
      • Owen-Hughes T.
      • Perkins N.D.
      The FHA domain protein SNIP1 is a regulator of the cell cycle and cyclin D1 expression.
      Black parents’ concerns related to a lack of information with respect to vaccine efficacy and safety, fear that the vaccine was experimentation on their daughters, cost, long-term side effects, and a belief that vaccination may increase early or unsafe sexual behavior have been implicated in the lack of vaccination acceptance in this population.
      • Scarinci I.C.
      • Garces-Palacio I.C.
      • Partridge E.E.
      An examination of acceptability of HPV vaccination among African American women and Latina immigrants.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      Perceptions that facilitated vaccination included the belief that vaccination was beneficial, provider recommendation, knowing peers who were vaccinated, and having had a personal experience with HPV-related disease.
      • Scarinci I.C.
      • Garces-Palacio I.C.
      • Partridge E.E.
      An examination of acceptability of HPV vaccination among African American women and Latina immigrants.
      • Hamlish T.
      • Clarke L.
      • Alexander K.A.
      Barriers to HPV immunization for African American adolescent females.
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      Table IBarriers and facilitators of HPV vaccination among racial/ethnic groups.
      BlackLatinoAsianWhite
      Barriers
      • 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 United States;
      • lower rates of provider recommendation compared with whites;
      • language barriers and inaccurate information in internationally born subgroups
      • Language;
      • safety concerns;
      • not knowing where to obtain vaccine;
      • lack of health insurance, especially among poor and undocumented immigrants;
      • lower rates of provider recommendation compared with whites;
      • logistical challenges to completion of three dose series
      • Language;
      • limited knowledge;
      • concerns related to sexual activity;
      • lack of health insurance, especially among poor
      • Lack of information;
      • lack of trust in vaccine safety and benefits among college-educated, high-income families;
      • more likely to feel vaccine is “not necessary” for their daughters due to low perceptions of sexual risk-taking
      Facilitators
      • Desire to prevent cancer;
      • desire to protect against a sexually transmitted infection;
      • experience with vaccine-preventable diseases in internationally born subgroups
      • Provider recommendation;
      • desire to prevent cancer;
      • trust in providers;
      • favorable attitude toward vaccines;
      • experience with vaccine preventable diseases and cervical cancer in home countries
      • Provider recommendation;
      • desire to prevent cancer
      • Provider recommendation;
      • desire to prevent cancer
      Modified with permission from Jeudin P, Liveright E, del Carmen MG, Perkins RB. Race, ethnicity and income as factors for HPV vaccine acceptance and use. Human Vaccines & Immunotherapeutics 2013; 9:1413–1420; PMID: 23571170; http://dx.doi.org/10.4161/hv.24422
      Despite high reported levels of HPV vaccine acceptability among blacks, actual HPV vaccination rates have been modest. In the initial years following HPV vaccine availability, studies of Medicaid and privately insured patients, as well as the National Survey of Family Growth, showed lower rates among black girls compared with white and Latina girls.
      • Cook R.L.
      • Zhang J.
      • Mullins J.
      • et al.
      Factors associated with initiation and completion of human papillomavirus vaccine series among young women enrolled in Medicaid.
      • Chao C.
      • Velicer C.
      • Slezak J.M.
      • Jacobsen S.J.
      Correlates for human papillomavirus vaccination of adolescent girls and young women in a managed care organization.
      • Gelman A.
      • Miller E.
      • Schwarz E.B.
      • et al.
      Racial disparities in human papillomavirus vaccination: does access matter?.
      More recent national data indicate similar rates of series initiation among black and white girls,
      • Kester L.M.
      • Zimet G.D.
      • Fortenberry J.D.
      • et al.
      A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for non-vaccination.
      but disparities may be re-emerging. The National Immunization Survey–Teen (NIS-Teen)
      • Opel D.J.
      • Robinson J.D.
      • Heritage J.
      • et al.
      Characterizing providers’ immunization communication practices during health supervision visits with vaccine-hesitant parents: a pilot study.
      reported a 6% decrease between 2011 and 2012 in the percentage of non-Latina black girls initiating vaccination (from 56% to 50%) compared with a 3% increase among non-Latina white girls (from 48% to 51%) (Table II

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Incidence-mortality. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed October 7, 2011.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      • Clegg L.X.
      • Reichman M.E.
      • Miller B.A.
      • et al.
      Impact of socioeconomic status on cancer incidence and stage at diagnosis: selected findings from the surveillance, epidemiology, and end results: National Longitudinal Mortality Study.
      • Chu K.C.
      • Miller B.A.
      • Springfield S.A.
      Measures of racial/ethnic health disparities in cancer mortality rates and the influence of socioeconomic status.
      ).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      Table IIRelationship of race, ethnicity, and poverty to cervical cancer incidence and mortality, and HPV vaccine initiation and completion
      All data reflect females, with the exception of the last column, as specified.
      ParameterRace/EthnicityPoverty Level
      White, Non-LatinoBlack, Non-LatinoLatinoAsian>100%<100%
      Current US female population, %63.613.717.26.18515
      Projected US female population 2050, %50.715.626.99.3N/AN/A
      Cervical cancer incidence per 100,000

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Incidence-mortality. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed October 7, 2011.

      • Clegg L.X.
      • Reichman M.E.
      • Miller B.A.
      • et al.
      Impact of socioeconomic status on cancer incidence and stage at diagnosis: selected findings from the surveillance, epidemiology, and end results: National Longitudinal Mortality Study.
      7.19.110.46.72.013.66
      Cervical cancer mortality per 100,000

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Incidence-mortality. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed October 7, 2011.

      • Chu K.C.
      • Miller B.A.
      • Springfield S.A.
      Measures of racial/ethnic health disparities in cancer mortality rates and the influence of socioeconomic status.
      1.94.12.81.72.2
      <10% of county below poverty level.
      3.5
      >20% of county below poverty level.
      HPV vaccine initiation in girls, %

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      51.150.162.955.950.4624.9
      HPV vaccine completion in girls, %

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      33.729.035.533.832.536.2
      HPV vaccine completion among girls who start series, %

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      71.863.759.361.869.959.3
      HPV vaccine completion in males, %

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      4.65.412.9NA5.510.7
      low asterisk All data reflect females, with the exception of the last column, as specified.
      <10% of county below poverty level.
      >20% of county below poverty level.
      Three doses are recommended for complete immunization because the long-term efficacy of incomplete vaccination is undetermined.
      • Paavonen J.
      • Naud P.
      • Salmeron J.
      • et al.
      Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women.
      Group FIS
      Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions.
      • Pomfret T.C.
      • Gagnon Jr, J.M.
      • Gilchrist A.T.
      Quadrivalent human papillomavirus (HPV) vaccine: a review of safety, efficacy, and pharmacoeconomics.
      Between 2006 and 2012, the rate of vaccination completion improved across most races. Earlier studies found lower adherence to the recommended vaccination schedule among black girls than other races, with black girls being half as likely to complete vaccination as their white counterparts in 2 studies of publically insured patients.
      • Cook R.L.
      • Zhang J.
      • Mullins J.
      • et al.
      Factors associated with initiation and completion of human papillomavirus vaccine series among young women enrolled in Medicaid.
      • Widdice L.E.
      • Bernstein D.I.
      • Leonard A.C.
      • et al.
      Adherence to the HPV vaccine dosing intervals and factors associated with completion of 3 doses.
      From 2006 to 2009, complete vaccination rates among black girls ranged from 11.1% to 24.6% compared with 19.5% to 65.3% among whites.
      • Niccolai L.M.
      • Mehta N.R.
      • Hadler J.L.
      Racial/ethnic and poverty disparities in human papillomavirus vaccination completion.
      • Chao C.
      • Velicer C.
      • Slezak J.M.
      • Jacobsen S.J.
      Correlates for human papillomavirus vaccination of adolescent girls and young women in a managed care organization.
      • Opel D.J.
      • Robinson J.D.
      • Heritage J.
      • et al.
      Characterizing providers’ immunization communication practices during health supervision visits with vaccine-hesitant parents: a pilot study.
      • Widdice L.E.
      • Bernstein D.I.
      • Leonard A.C.
      • et al.
      Adherence to the HPV vaccine dosing intervals and factors associated with completion of 3 doses.
      NIS-Teen 2011–2012 reported a dramatic increase in completion rates in comparison to previous years; however, and blacks who began the HPV vaccine series had a completion rate similar to that of whites in 2012: 63.7% (95% CI, 56.6–70.8) for black girls and 71.8% (95% CI, 69.1–74.5) for white girls
      • Opel D.J.
      • Robinson J.D.
      • Heritage J.
      • et al.
      Characterizing providers’ immunization communication practices during health supervision visits with vaccine-hesitant parents: a pilot study.
      (Table II).

       Factors Affecting HPV Vaccination among Subpopulations of Black Women

      The Caribbean has one of the highest incidences of cervical cancer, with rates in Haiti (87/100,000)
      • Villa L.L.
      Cervical cancer in Latin America and the Caribbean: the problem and the way to solutions.
      >10-fold higher than in the United States. In 2009, it was estimated that Caribbean immigrants numbered 3.5 million people and composed 9% of US immigrants.

      Caribbean immigrants in the United States. Migration Information Source April 2011. http://www.migrationinformation.org/USfocus/display.cfm?ID=834. Accessed October 1, 2013.

      Women from these areas tend to be heterogeneous in language, beliefs, and attitudes, and differences can also be observed in behaviors and vaccine acceptance. One survey showed higher rates of both sexual activity and vaccine acceptance in Caribbean-American than in US-born African-American teens (56% vs 46% sexually active by age 16 years; 54% vs 35% acceptance of HPV vaccine).
      • Read D.S.
      • Joseph M.A.
      • Polishchuk V.
      • Suss A.L.
      Attitudes and perceptions of the HPV vaccine in Caribbean and African-American adolescent girls and their parents.
      Parents from different Caribbean countries may have differing attitudes toward vaccination, and reported support ranges from 30% to 70%.
      • Poole J.C.
      • Thain A.
      • Perkins N.D.
      • Roninson I.B.
      Induction of transcription by p21Waf1/Cip1/Sdi1: role of NFkappaB and effect of non-steroidal anti-inflammatory drugs.
      • Kobetz E.
      • Menard J.
      • Hazan G.
      • et al.
      Perceptions of HPV and cervical cancer among Haitian immigrant women: implications for vaccine acceptability.
      • Gust D.A.
      • Darling N.
      • Kennedy A.
      • Schwartz B.
      Parents with doubts about vaccines: which vaccines and reasons why.
      Haitian parents may be especially reluctant to vaccinate their daughters. Many Haitian women have limited knowledge and hold various misconceptions about HPV, including beliefs that transmission may depend on sexual position, that physical symptoms occur with initial infection, and that HPV causes AIDS. Haitian parents are also concerned that HPV vaccination was intended for Haitians as an experiment or would be used as a tool for discrimination against the Haitian community.
      • Kobetz E.
      • Menard J.
      • Hazan G.
      • et al.
      Perceptions of HPV and cervical cancer among Haitian immigrant women: implications for vaccine acceptability.
      • Gust D.A.
      • Darling N.
      • Kennedy A.
      • Schwartz B.
      Parents with doubts about vaccines: which vaccines and reasons why.
      Other barriers relate to strong taboos against premarital sexual relations in the Haitian community. Some parents did not believe that HPV vaccination fell within their parental role because their children should not become sexually active before adulthood,
      • Poole J.C.
      • Thain A.
      • Perkins N.D.
      • Roninson I.B.
      Induction of transcription by p21Waf1/Cip1/Sdi1: role of NFkappaB and effect of non-steroidal anti-inflammatory drugs.
      • Joseph N.P.
      • Clark J.A.
      • Bauchner H.
      • et al.
      Knowledge, attitudes, and beliefs regarding HPV vaccination: ethnic and cultural differences between African-American and Haitian immigrant women.
      while others 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 vaccination may be misinterpreted as permission to engage in sexual activity, that vaccination was necessary only for women with multiple partners, or that vaccination was not necessary for people who practiced abstinence.
      • Opel D.J.
      • Taylor J.A.
      • Mangione-Smith R.
      • et al.
      Validity and reliability of a survey to identify vaccine-hesitant parents.
      Because studies using race-based data often group women by appearance and color but fail to account for differences based on culture and country of origin, more research is needed to understand factors affecting HPV vaccination initiation and completion among black subgroups.

       HPV Vaccination in the Hispanic/Latina Community

      Latina females currently represent 17% of US women,

      Vaccines for Children Program. http://www.cdc.gov/vaccines/programs/vfc/index.html. Accessed August 31, 2013.

      and numbers are rising rapidly. Latinas have the second highest prevalence of HPV infection (44.2%),
      • Hariri S.
      • Unger E.R.
      • Sternberg M.
      • et al.
      Prevalence of genital human papillomavirus among females in the United States, the National Health And Nutrition Examination Survey, 2003–2006.
      and many are first- or second-generation immigrants from countries with high rates of cervical cancer.
      • Denny L.
      The prevention of cervical cancer in developing countries.
      Thus most (58%–90%) Latina women surveyed stated that they would accept HPV vaccination.
      • Scarinci I.C.
      • Garces-Palacio I.C.
      • Partridge E.E.
      An examination of acceptability of HPV vaccination among African American women and Latina immigrants.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      • Podolsky R.
      • Cremer M.
      • Atrio J.
      • et al.
      HPV vaccine acceptability by Latino parents: a comparison of U.S. and Salvadoran populations.
      • Sanderson M.
      • Coker A.L.
      • Eggleston K.S.
      • et al.
      HPV vaccine acceptance among Latina mothers by HPV status.
      • Yeganeh N.
      • Curtis D.
      • Kuo A.
      Factors influencing HPV vaccination status in a Latino population; and parental attitudes towards vaccine mandates.
      Beliefs facilitating vaccination included general trust in vaccine safety, believing that the HPV vaccine could help to prevent cervical cancer, and a prior personal experience with HPV-related disease.
      • Sanderson M.
      • Coker A.L.
      • Eggleston K.S.
      • et al.
      HPV vaccine acceptance among Latina mothers by HPV status.
      • Yeganeh N.
      • Curtis D.
      • Kuo A.
      Factors influencing HPV vaccination status in a Latino population; and parental attitudes towards vaccine mandates.
      Practical issues also affected vaccine support: those who knew where to obtain vaccination for their children were more likely support vaccination,
      • Sanderson M.
      • Coker A.L.
      • Eggleston K.S.
      • et al.
      HPV vaccine acceptance among Latina mothers by HPV status.
      and those with higher levels of American acculturation were more likely to report provider recommendation, which is associated with increased reports of vaccination.
      • Gerend M.A.
      • Zapata C.
      • Reyes E.
      Predictors of human papillomavirus vaccination among daughters of low-income Latina mothers: the role of acculturation.
      Most Latina 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.
      • Scarinci I.C.
      • Garces-Palacio I.C.
      • Partridge E.E.
      An examination of acceptability of HPV vaccination among African American women and Latina immigrants.
      • Yeganeh N.
      • Curtis D.
      • Kuo A.
      Factors influencing HPV vaccination status in a Latino population; and parental attitudes towards vaccine mandates.
      • Bastani R.
      • Glenn B.A.
      • Tsui J.
      • et al.
      Understanding suboptimal human papillomavirus vaccine uptake among ethnic minority girls.
      Few parents believed that vaccination would be misinterpreted as permission to engage in intercourse at a young age.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      • Yeganeh N.
      • Curtis D.
      • Kuo A.
      Factors influencing HPV vaccination status in a Latino population; and parental attitudes towards vaccine mandates.
      Even among parents who expressed concerns, many believed that the overall benefits of vaccination outweighed potential risks.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      The NIS-Teen surveys in 2008, 2009, 2011, and 2012, as well as National Health Interview Survey 2010 all found higher HPV vaccination initiation rates among Latina than white girls.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      • Kester L.M.
      • Zimet G.D.
      • Fortenberry J.D.
      • et al.
      A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for non-vaccination.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2008. http://wwwcdcgov/vaccines/stats-surv/nisteen/tables/08/tab14_HPV1_racexls 2010. Accessed January 12, 2010.

      NIS-Teen
      National and state vaccination coverage among adolescents aged 13 through 17 years—United States, 2010.
      • Davis T.C.
      • Williams M.V.
      • Marin E.
      • et al.
      Health literacy and cancer communication.
      • Perkins R.B.
      • Langrish S.M.
      • Stern L.J.
      • et al.
      Comparison of visual inspection and Papanicolau (PAP) smears for cervical cancer screening in Honduras: should PAP smears be abandoned?.
      In 2012, 63% of Latina girls received ≥1 doses of the vaccine compared with 51% of white and 50% of black girls

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      (Table II). Similar to in black girls, however, rates of HPV vaccination among Latina girls decreased slightly from 2011 to 2012 (from 65% to 63%). Despite the higher rates of initiation, NIS-Teen 2012 most recently reported that Latina girls who begin the series are significantly less likely to complete vaccination series than are their white and black counterparts (Latina, 59.3 [95% CI, 52.5–66.1] vs. white, 71.8 [95% CI, 69.1–74.5] and black, 63.7 [95% CI, 56.6–70.8]).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      Although black and Latina girls have similar or better HPV vaccination initiation rates compared with white girls, it is concerning that overall completion rates are similar, indicating lower rates of follow-through among minority compared with white girls. Failure to complete the vaccine series seems to relate to logistical issues such as a lack of parental knowledge about vaccine dosing or schedules, lack of flexibility of parents’ and children’s schedules, finding the times and locations of the clinics inconvenient,
      • Kouyoumdjian F.G.
      • Bailowitz A.
      Completion of the human papillomavirus vaccine series in females attending an urban immunization clinic.
      and a lack of clinic reminder/recall systems.
      • Brawner B.M.
      • Baker J.L.
      • Voytek C.D.
      • et al.
      The development of a culturally relevant, theoretically driven HPV prevention intervention for urban adolescent females and their parents/guardians.
      • Gainforth H.L.
      • Cao W.
      • Latimer-Cheung A.E.
      Message framing and parents’ intentions to have their children vaccinated against HPV.
      • Suh C.A.
      • Saville A.
      • Daley M.F.
      • et al.
      Effectiveness and net cost of reminder/recall for adolescent immunizations.
      • Kempe A.
      • Barrow J.
      • Stokley S.
      • et al.
      Effectiveness and cost of immunization recall at school-based health centers.

       Racial Disparities in Provider Recommendation of HPV Vaccination

      HPV vaccination recommendation by a health care provider has been shown to increase the likelihood of vaccination up to 18-fold (95% CI, 1–23),

      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. Vaccine. 2012;30:3112–3118.

      and up to 90% of females who report vaccination also report provider recommendation.
      • Kester L.M.
      • Zimet G.D.
      • Fortenberry J.D.
      • et al.
      A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for non-vaccination.
      However, parents of black and Latina girls report lower rates of provider recommendation of HPV vaccination than do parents of white girls,

      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. Vaccine. 2012;30:3112–3118.

      • Polonijo A.N.
      • Carpiano R.M.
      Social inequalities in adolescent human papillomavirus (HPV) vaccination: a test of fundamental cause theory.
      an issue that may be further exacerbated by differences in primary language and acculturation status.
      • Gerend M.A.
      • Zapata C.
      • Reyes E.
      Predictors of human papillomavirus vaccination among daughters of low-income Latina mothers: the role of acculturation.
      Therefore, effective communication, along with an understanding of cultural health beliefs, is central to increasing adherence.

       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; these women represent ~5% of the US population.

      Vaccines for Children Program. http://www.cdc.gov/vaccines/programs/vfc/index.html. Accessed August 31, 2013.

      This racial group is highly diverse, and much of the data available examining cervical cancer screening and HPV vaccination are specific to certain subgroups. Overall cervical cancer incidence for Asians is low (7.3 per 100,000 for Asians compared with 9.6 per 100,000 for blacks, 10.9 per 100,000 for Latinas, and 7.5 per 100,000 for non-Latina whites),

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Stat Fact Sheets: Cervix uteri cancer. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed November 4, 2013.

      with certain subgroups having much higher rates, specifically Vietnamese-American women (14 per 100,000 women) and Korean-American women (11 per 100,000).
      • McCracken M.
      • Olsen M.
      • Chen Jr, M.S.
      • et al.
      Cancer incidence, mortality, and associated risk factors among Asian Americans of Chinese, Filipino, Vietnamese, Korean, and Japanese ethnicities.
      Low rates of Papanicolaou screening may contribute to these disparities: only 55% of Vietnamese and 48% of Korean women report Pap screening compared with 80% for white women.
      • Schegloff E.
      A Primer of Conversation Analysis: Sequence Organization.
      Low rates of Pap screening in many ethnic groups relate to poverty and limited access; however, this may not be true for Asians: the 2001 California Health Interview Study
      • Heritage J.
      • Maynard D.
      Communication in Medical Care: Interaction Between Primary Care Physicians and Patients.
      found that Asians had higher rates of income and education but lower rates of Pap screening than did any other ethnicity. Surveys examining parents’ intention to vaccinate have shown lower rates among Asians than other ethnic groups,
      • Bastani R.
      • Glenn B.A.
      • Tsui J.
      • et al.
      Understanding suboptimal human papillomavirus vaccine uptake among ethnic minority girls.
      • Constantine N.A.
      • Jerman P.
      Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis.
      • Jaen C.R.
      • Stange K.C.
      • Nutting P.A.
      Competing demands of primary care: a model for the delivery of clinical preventive services.
      which may result in part from language barriers and limited knowledge.
      • Bastani R.
      • Glenn B.A.
      • Tsui J.
      • et al.
      Understanding suboptimal human papillomavirus vaccine uptake among ethnic minority girls.
      • Jaen C.R.
      • Stange K.C.
      • Nutting P.A.
      Competing demands of primary care: a model for the delivery of clinical preventive services.
      • Miller W.R.
      Motivational Interviewing: Helping People Change.

      The Dartmouth Atlas of Healthcare. http://www.dartmouthatlas.org/keyissues/issue.aspx?con=2939. Accessed January 17, 2013.

      • Eppes C.
      • Wu A.
      • Cameron K.A.
      • et al.
      Does obstetrician knowledge regarding influenza increase HINI vaccine acceptance among their pregnant patients?.
      Recent data from a study in 2013 of Vietnamese-American women showed that English proficiency and length of stay in the United States were associated with an increase of up to 4-fold in series initiation.
      • Yi J.K.
      • Anderson K.O.
      • Le Y.C.
      • et al.
      English proficiency, knowledge, and receipt of HPV vaccine in Vietnamese-American women.
      • Yi J.K.
      • Lackey S.C.
      • Zahn M.P.
      • et al.
      Human papillomavirus knowledge and awareness among Vietnamese mothers.
      Despite these findings, NIS-Teen 2012 data indicate similar rates of series initiation and completion among Asian and white girls (initiation: Asians, 55.9% [95% CI, 45.0–66.8] vs whites, 51.1% [95% CI, 49.0–53.2]; completion among those who start: Asians, 61.8% [95% CI, 46.0–77.6] vs whites, 71.8% [95% CI, 69.1–74.5]).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      In an effort to increase vaccination further, the data suggest practicing sensitivity to cultural and language barriers in the Asian-American community.

       Poverty Status and HPV Vaccination

      Nearly 15% of Americans live below the poverty level, with poverty concentrated among blacks (27.6% [95% CI, 25.6–28.6]) and Latinos (25.3% [95% CI, 24.5–26.1]), compared with Asians (12.3% [95% CI, 11.1–13.5]) and whites (9.8% [95% CI, 9.5–10.1]).
      • Leddy M.A.
      • Anderson B.L.
      • Power M.L.
      • et al.
      Changes in and current status of obstetrician-gynecologists’ knowledge, attitudes, and practice regarding immunization.
      Women living below the poverty level have a higher prevalence of HPV infections (56.5%) than do those living above poverty (39.7%),
      • Hariri S.
      • Unger E.R.
      • Sternberg M.
      • et al.
      Prevalence of genital human papillomavirus among females in the United States, the National Health And Nutrition Examination Survey, 2003–2006.
      are more likely to be diagnosed with advanced cervical cancer, and are 30% less likely to survive after a diagnosis of metastatic disease.
      • Perkins R.B.
      • Hall J.E.
      • Martin K.A.
      Neuroendocrine abnormalities in hypothalamic amenorrhea: spectrum, stability, and response to neurotransmitter modulation.
      Perhaps due to more personal experiences with cervical cancer, low-income mothers view HPV vaccination positively.
      • Gainforth H.L.
      • Cao W.
      • Latimer-Cheung A.E.
      Message framing and parents’ intentions to have their children vaccinated against HPV.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      Education and income are highly correlated, and mothers with a high school education or less were also more willing to vaccinate their daughters than were those with college degrees.
      • Constantine N.A.
      • Jerman P.
      Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis.
      • Rosenthal S.L.
      • Rupp R.
      • Zimet G.D.
      • et al.
      Uptake of HPV vaccine: demographics, sexual history and values, parenting style, and vaccine attitudes.
      • Zimet G.D.
      • Mays R.M.
      • Sturm L.A.
      • et al.
      Parental attitudes about sexually transmitted infection vaccination for their adolescent children.
      Differences may be more pronounced for girls aged 13 years 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),
      • Constantine N.A.
      • Jerman P.
      Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis.
      although another showed that parental education level had no effect.
      • Gust D.A.
      • Darling N.
      • Kennedy A.
      • Schwartz B.
      Parents with doubts about vaccines: which vaccines and reasons why.
      Reasons for supporting vaccination included concerns for health, safety, and to avoid future feelings of regret in the event of an adverse outcome.
      • Perkins R.B.
      • Pierre-Joseph N.
      • Marquez C.
      • et al.
      Why do low-income minority parents choose human papillomavirus vaccination for their daughters?.
      • Constantine N.A.
      • Jerman P.
      Acceptance of human papillomavirus vaccination among Californian parents of daughters: a representative statewide analysis.
      In 2012, the national rate of series initiation among girls below the poverty line was higher (64.9% [95% CI, 60.7–69.1]) than that of those living above the poverty line (50.4% [95% CI, 48.4–52.4]).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      However, rates of series completion among those who start were lower among impoverished girls (59.3% [95% CI, 53.5–65.1]) than among those living above poverty (69.9% [95% CI, 67.2–72.6]).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

       HPV Vaccination in Boys

      The HPV vaccine was approved by the US Food and Drug Administration in 2009 to be given to males aged 9 to 26 years
      Advisory Committee on Immunization Practices
      FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP).
      but was not routinely recommended and universally covered by insurance until 2011.
      Advisory Committee on Immunization Practices
      Recommendations on the use of quadrivalent human papillomavirus vaccine in males—Advisory Committee on Immunization Practices (ACIP), 2011.
      Data on racial and ethnic disparities in male vaccination are limited, but NIS-Teen 2012 indicated marked racial and income differences. Both black (25.9% [95% CI, 21.3–30.5]) and Latino (31.7% [95% CI, 27.0–36.4]) male teens are more likely to initiate vaccination than are white male teens (20.8% [95% CI, 19.3–22.3]). Those below poverty initiate vaccination more often (29.9% [95% CI, 26.0–33.8]) than do those above poverty (17.3% [95% CI, 15.8–18.8]).

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      These data are consistent with parent surveys indicating high receptivity for male vaccination among low-income and minority parents of sons.
      • Perkins R.
      • Tipton H.
      • Shu E.
      • et al.
      Attitudes toward HPV vaccination among low-income and minority parents of sons: a qualitative analysis.
      • Perkins R.B.
      • Apte G.
      • Marquez C.
      • et al.
      Factors affecting human papillomavirus vaccine use among white, black and latino parents of sons.
      Although males stand to benefit directly from HPV vaccination due to the prevention of genital warts and anal and oropharyngeal cancers,
      Advisory Committee on Immunization Practices
      Recommendations on the use of quadrivalent human papillomavirus vaccine in males—Advisory Committee on Immunization Practices (ACIP), 2011.
      vaccinating males also protects women. Several studies have shown that vaccinating boys is cost-effective and provides substantial public health benefits to women as well as men.
      • Elbasha E.H.
      • Dasbach E.J.
      Impact of vaccinating boys and men against HPV in the United States.
      • Kim J.J.
      • Goldie S.J.
      Cost effectiveness analysis of including boys in a human papillomavirus vaccination programme in the United States.
      Vaccinating low-income and minority boys can also help to protect vulnerable girls because most young adults tend to have sexual partners from within their communities.
      • Grieb S.M.
      • Davey-Rothwell M.
      • Latkin C.A.
      Social and sexual network characteristics and concurrent sexual partnerships among urban African American high-risk women with main sex partners.
      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.

      Discussion

      Race/ethnicity and low socioeconomic status are known predictors of late-stage diagnosis of cervical cancer and are important predictors of mortality.

      McCarthy AM, Dumanovsky T, Visvanathan K, et al. Racial/ethnic and socioeconomic disparities in mortality among women diagnosed with cervical cancer in New York City, 1995–2006. Cancer Causes Control. 2010;21:1645–1655.

      In the United States, ~12,000 women develop cervical cancer and >4000 die of the disease each year, with higher incidence and mortality rates reported in low-income minority populations.

      Surveillance, Epidemiology, and End Results Program, National Cancer Institute. Stat Fact Sheets: Cervix uteri cancer. http://seer.cancer.gov/statfacts/html/cervix.html. Accessed November 4, 2013.

      Some of these observed differences are due to the differences in the burden of HPV infection, which are culturally and socially mediated and relate to both the age of sexual debut and the number of lifetime partners.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      • Akers A.Y.
      • Newmann S.J.
      • Smith J.S.
      Factors underlying disparities in cervical cancer incidence, screening, and treatment in the United States.
      Other factors relate to health care access and utilization and reflect both linguistic and cultural barriers, including low health literacy and fatalistic beliefs,
      • Lee M.C.
      Knowledge, barriers, and motivators related to cervical cancer screening among Korean-American women. A focus group approach.
      • Powe B.D.
      • Finnie R.
      Cancer fatalism: the state of the science.
      • Vanslyke J.G.
      • Baum J.
      • Plaza V.
      • et al.
      HPV and cervical cancer testing and prevention: knowledge, beliefs, and attitudes among Hispanic women.
      as well as systems-related inequities, including differential access to screening, follow-up, and treatment for abnormal Pap tests, cervical dysplasia, and cancer.
      • Davis T.C.
      • Williams M.V.
      • Marin E.
      • et al.
      Health literacy and cancer communication.
      • Garbers S.
      • Chiasson M.A.
      Inadequate functional health literacy in Spanish as a barrier to cervical cancer screening among immigrant Latinas in New York City.
      • Downs L.S.
      • Smith J.S.
      • Scarinci I.
      • et al.
      The disparity of cervical cancer in diverse populations.
      • Brooks S.E.
      • Chen T.T.
      • Ghosh A.
      • et al.
      Cervical cancer outcomes analysis: impact of age, race, and comorbid illness on hospitalizations for invasive carcinoma of the cervix.
      HPV vaccination has been shown to reduce the prevalence of high-risk HPV infection among teens
      Advisory Committee on Immunization Practices
      Quadrivalent human papillomavirus vaccine: recommendations of the advisory comitte on immunization practices.
      and thus has the potential to decrease the risks of cervical dysplasia and cancer among vaccinated women even in the absence of screening. In fact, sentinel surveillance studies indicate a decline in the annual rate of high-grade cervical dysplasia, from 834 per 100,000 in 2008 to 688 per 100,000 in 2011, among women aged 21 to 24 years (P < 0.001), which may reflect the impact of vaccination.
      • Niccolai L.M.
      • Julian P.J.
      • Meek J.I.
      • et al.
      Declining rates of high-grade cervical lesions in young women in Connecticut, 2008–2011.
      However, declines were not significant in areas with high proportions of blacks, Latinos and/or people living below the federal poverty level, which may indicate lower access to vaccination, failure to achieve vaccination before HPV exposure, or a higher proportion of severe dysplasia caused by HPV types not covered by the vaccine among minority and low-income women.
      • Niccolai L.M.
      • Russ C.
      • Julian P.J.
      • et al.
      Individual and geographic disparities in human papillomavirus types 16/18 in high-grade cervical lesions: associations with race, ethnicity, and poverty.
      Despite efforts from grassroots and public health organizations, the medical community, and researchers, the rates of vaccination initiation and completion across all racial, ethnic, and income groups have remained relatively stagnant over the past several years.
      • Eaton D.K.
      • Kann L.
      • Kinchen S.
      • et al.
      Youth risk behavior surveillance—United States, 2011.
      Successful reduction of cervical cancer mortality will require an integrative effort, including increased access to care, such as that included in the Affordable Care Act, improvements in provider recommendation and patient and provider education, and system-based changes to facilitate series completion. Because access to health care is expanded for low-income Americans, providers serving these communities should receive support and education regarding successful tools for integrating HPV vaccination into their practices.
      • Hamlish T.
      • Clarke L.
      • Alexander K.A.
      Barriers to HPV immunization for African American adolescent females.
      Patient-targeted interventions should focus on the importance of series completion among low-income and minority teens.
      Current trends indicate that low-income and minority male and female adolescents initiate HPV vaccination at higher rates than do their more affluent white counterparts, but have lower rates of completing the vaccine series once they start, resulting in similar rates of complete vaccination among racial/ethnic and income groups.

      NIS-Teen. Vaccination coverage among adolescents aged 13–17 years—United States, 2012. http://www.cdc.gov/vaccines/stats-surv/nisteen/data/tables_2012.htm. Accessed September 12, 2013.

      • Davis T.C.
      • Williams M.V.
      • Marin E.
      • et al.
      Health literacy and cancer communication.
      And although vaccine efficacy is excellent following 3 doses, little is known about the effects of incomplete vaccination,
      • Paavonen J.
      • Naud P.
      • Salmeron J.
      • et al.
      Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women.
      Group FIS
      Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions.
      • Pomfret T.C.
      • Gagnon Jr, J.M.
      • Gilchrist A.T.
      Quadrivalent human papillomavirus (HPV) vaccine: a review of safety, efficacy, and pharmacoeconomics.
      indicating that substantial numbers of men and women at high risk of HPV-related cancers may be inadequately protected. Known facilitators of HPV vaccination include access to primary care, a strong provider recommendation, and parental knowledge and interest in receiving vaccination. Yet vaccine support does not always lead to series completion among minorities. Since the advent of the HPV vaccine, black and Latina girls who initiate vaccination have lower rates of vaccine completion than do whites. Common reasons for failing to complete the vaccine series include being unaware of the need for subsequent doses, side effects, being too busy, and/or finding the times and locations of the clinics inconvenient.
      • Kouyoumdjian F.G.
      • Bailowitz A.
      Completion of the human papillomavirus vaccine series in females attending an urban immunization clinic.
      These issues are often more common among low-income and minority women who may have limited English proficiency or low health literacy, hold unskilled jobs with inflexible work hours, or have limited child care options. Additional research is needed, however, to explore and identify barriers to HPV vaccine completion among high-risk adolescents, and to develop education initiatives that will target these issues.
      Because parental decisions about vaccination are strongly influenced by provider recommendation, it is important for practitioners to improve their recommendations of HPV vaccine to parents. Providers appear to be more important than race or socioeconomic status in determining vaccine receipt.
      • Dorell C.G.
      • Yankey D.
      • Santibanez T.A.
      • Markowitz L.E.
      Human papillomavirus vaccination series initiation and completion, 2008–2009.
      • Bartlett J.A.
      • Peterson J.A.
      The uptake of human papillomavirus (HPV) vaccine among adolescent females in the United States: a review of the literature.
      • Litton A.G.
      • Desmond RA
      • Gilliland J
      • et al.
      Factors associated with intention to vaccinate a daughter against HPV: a statewide survey in Alabama.
      • Guerry S.L.
      • De Rosa C.J.
      • Markowitz L.E.
      • et al.
      Human papillomavirus vaccine initiation among adolescent girls in high-risk communities.
      One report showed that 90% of teens who received ≥1 dose of the HPV vaccine received strong recommendation from a provider.
      • Kester L.M.
      • Zimet G.D.
      • Fortenberry J.D.
      • et al.
      A national study of HPV vaccination of adolescent girls: rates, predictors, and reasons for non-vaccination.
      In another study, lack of provider recommendation was the most frequently reported reason for not receiving HPV vaccination among women found to have precancerous cervical lesions.
      • Mehta N.R.
      • Julian P.J.
      • Meek J.I.
      • et al.
      Human papillomavirus vaccination history among women with precancerous cervical lesions: disparities and barriers.
      However, only half of providers strongly recommend HPV vaccination to girls aged 11 or 12 years,

      Strength of HPV vaccine recommendation for female patients. https://cdc.confex.com/cdc/nic2011/webprogram/Paper25652.html. Accessed October 1, 2013.

      and providers are reluctant to vaccinate girls aged 11 or 12 years compared with older teens.
      • Kahn J.A.
      • Cooper H.P.
      • Vadaparampil S.T.
      • et al.
      Human papillomavirus vaccine recommendations and agreement with mandated human papillomavirus vaccination for 11-to-12-year-old girls: a statewide survey of Texas physicians.
      • Vadaparampil S.T.
      • Kahn J.A.
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      the percentage of unvaccinated girls with at least 1 missed opportunity (ie, a health care encounter in which a patient did not receive the HPV vaccine after age 11 years) increased from ~21% to 84% from 2007 to 2012. If all missed opportunities were eliminated, vaccination coverage with at least 1 dose of the HPV vaccine would reach almost 93%. The CDC also estimates that if vaccination coverage were to improve to 80%, 53,000 cases of cervical cancer could potentially be prevented over the lifetime of girls aged 12 years and over.
      Centers for Disease Control and Prevention
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      may be effective ways to improve vaccination rates. Because minorities are less likely to receive provider recommendations,

      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. Vaccine. 2012;30:3112–3118.

      • Polonijo A.N.
      • Carpiano R.M.
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      such interventions may be especially important for providers of care to these populations.
      Minority, immigrant, and non–English-speaking parents consistently demonstrate lower rates of HPV-related knowledge than do white and English-speaking parents.
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      parents with little knowledge of the benefits of vaccination may be less likely to advocate for themselves. Low knowledge may also contribute to lower rates of completion among minority adolescents. This is significant because the US Census Bureau projects that by 2050, Latinas will compose 26.9% of the female population, non-Latinas blacks will compose 15.6%, and Asians, 9.3%. With the increasing proportions of blacks, Latinas, and Asians in the US population, achieving equitable and adequate rates of vaccination among underserved adolescents is imperative. It is important for health care professionals and other public health officials to recognize these gaps in knowledge and to provide appropriate counseling to dispel all misconceptions surrounding HPV vaccination. Patient-oriented solutions, such as patient navigation systems, have demonstrated efficacy for improving follow-up after abnormal Pap test or mammogram results among minority and low-income populations,
      • Gorin S.S.
      • Ashford A.R.
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      and might also be applied to improve completion among those who have started the series.

      Conclusions

      There is a need for increasing HPV vaccination among all adolescents and ensuring that rates are high among girls and boys from all racial, ethnic, and income groups. Failure to achieve equitable vaccination may exacerbate disparities in cervical cancer incidence and mortality in the future. Research indicates that low-income and minority parents are just as willing to vaccinate their children as are white, affluent parents; however, successful strategies to aid in vaccine completion may not be the same across all races and subpopulations. Therefore, an integrated initiative focused on HPV awareness, widespread vaccination, and culturally sensitive educational programs may be necessary to achieve high rates of complete vaccination across all racial, ethnic, and income groups. Understanding current vaccination trends and the barriers to series initiation and completion will facilitate the development of effective strategies to improve vaccine completion and to reduce disparities in cervical cancer in years to come.

      Conflicts of Interest

      Funding for this research was provided by an American Cancer Society Mentored Research Scholar grant (no. MRSG-09-151-01). The study funders had no role in any part of the study. The authors have indicated that they have no conflicts of interest with regard to the content of this article.

      Acknowledgments

      Dr. Perkins led the design of the review, oversaw literature review, and participated in drafting and revising the article. Drs. Jeudin and Liveright conducted the primary literature reiview and participated in drafting and revising the article. Dr. del Carmen participated in design of the review, and revised the article for important intellectual content.
      Funding for the research was provided by an American Cancer Society Mentored Research Scholar Grant (MRSG-09-151-01).

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