Advertisement

National and State-Level Composite Completion of Recommended Vaccines Among Adolescents in the United States, 2015–2018

Open AccessPublished:September 10, 2021DOI:https://doi.org/10.1016/j.jadohealth.2021.07.020

      Abstract

      Background

      Routine adolescent vaccination recommendations in the United States include tetanus, diphtheria, and acellular pertussis, quadrivalent meningococcal conjugate vaccine, and human papillomavirus vaccines. Although coverage for these individual vaccines is known, limited data are available on composite completion for all three vaccines.

      Methods

      This cross-sectional analysis of pooled 2015–2018 National Immunization Survey–Teen data used logistic regression to estimate model-adjusted composite vaccination completion nationally and by state among United States adolescents aged 17 years. National Immunization Survey–Teen data were combined with state-level data to estimate a multilevel model identifying factors associated with composite vaccination completion.

      Results

      The pooled model-adjusted composite vaccination completion was 30.6% (95% confidence interval [CI], 30.13%–31.04%) nationally, varying from 11.3% in Idaho (6.91%–17.95%) to 56.4% (49.81%–62.82%) in Rhode Island. Individual-level factors with the greatest impact on composite completion were having a provider's recommendation for human papillomavirus vaccination (odds ratio, 3.24; 95% CI, 2.76–3.80) and a check-up visit at age 16–17 years (odds ratio, 2.35; 95% CI, 1.80–3.07), with other individual-level factors associated with completion including being Medicaid insured, female, Hispanic, or non-Hispanic black. State-level quadrivalent meningococcal conjugate vaccination mandates were also associated with an increased likelihood of composite vaccination completion (odds ratio, 1.64; 95% CI, 1.16–2.33).

      Conclusions

      Fewer than one-third of 17-year-old individuals have completed all three recommended vaccines, with rates varying by state. Although this study identified implementable strategies to improve composite completion, additional research is needed to further understand factors associated with adolescent vaccination completion.

      Keywords

      Implications and Contribution
      Assessing vaccination completion for recommended vaccines will help identify and target quality improvement initiatives for adolescents who are inadequately vaccinated. Provider visits at 16–17 years of age, vaccine recommendations from providers, insurance coverage expansion, Medicaid, and state mandates for meningococcal vaccination are strategies to increase adolescents' vaccination coverage.
      The United States (US) Advisory Committee on Immunization Practices (ACIP) recommends for all adolescents [
      • Robinson C.L.
      • Bernstein H.
      • Poehling K.
      • et al.
      Advisory committee on immunization practices recommended immunization schedule for children and adolescents aged 18 years or younger - United States, 2020.
      ] the administration of (1) influenza vaccine annually, (2) tetanus, diphtheria, and acellular pertussis (Tdap) vaccine, preferably at age 11–12 years, [
      Centers for Disease Control and Prevention (CDC)
      Diphtheria, tetanus, and pertussis vaccine recommendations.
      ] (3) quadrivalent meningococcal conjugate (MenACWY) vaccine at age 11–12 years with a booster dose at age 16 years [
      Centers for Disease Control and Prevention (CDC)
      Meningococcal vaccine recommendations.
      ], and (4) human papillomavirus (HPV) vaccine in a two or three dose series, depending on the age at initial vaccination [
      Centers for Disease Control and Prevention (CDC)
      HPV vaccine recommendations.
      ].
      The immunization schedule for adolescents in the US includes two immunization platform visits: one at 11–12 years of age and another at 16 years of age [
      • Curran D.
      • Van Oorschot D.
      • Varghese L.
      • et al.
      Assessment of the potential public health impact of Herpes Zoster vaccination in Germany.
      ]. Both visits integrate administration of vaccinations with other essential preventive care services for adolescents [
      Immunization of adolescents
      Recommendations of the Advisory Committee on Immunization Practices, the American Academy of Pediatrics, the American Academy of Family Physicians, and the American Medical Association.
      ]. The presence of these immunization platforms emphasizes the importance of on-time vaccination, serving as reminders to health care professionals (HCPs) and parents or guardians that the adolescents are due for a set of age-appropriate vaccinations [
      Immunization of adolescents
      Recommendations of the Advisory Committee on Immunization Practices, the American Academy of Pediatrics, the American Academy of Family Physicians, and the American Medical Association.
      ,
      Society for Adolescent Health and Medicine
      Establishing an immunization platform for 16-year-olds in the United States.
      ]. The visit at 11–12 years of age marks an opportunity to document the immunization needs for individuals transitioning from childhood to adolescence [
      Immunization of adolescents
      Recommendations of the Advisory Committee on Immunization Practices, the American Academy of Pediatrics, the American Academy of Family Physicians, and the American Medical Association.
      ]. The older adolescent visit at 16 years of age ensures completion of all age-appropriate vaccinations before graduating from high school and transitioning into young adulthood [
      Society for Adolescent Health and Medicine
      Establishing an immunization platform for 16-year-olds in the United States.
      ].
      While progress in vaccination coverage has been made [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ], many adolescents continue to be vulnerable to vaccine-preventable diseases, as indicated by suboptimal vaccination coverage in 2019 based on the National Immunization Survey–Teen (NIS-Teen) data [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ]. For example, only 53.7% (95% confidence interval [CI], 49.9%–57.4%) of adolescents aged 17 years had completed the two-dose series of MenACWY vaccine, and only 54.2% (95% CI, 52.7%–55.8%) of adolescents were up to date with HPV vaccine series [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ]. Tdap vaccine coverage is the exception to these suboptimal rates, with a 2019 coverage estimate of 90.2% (95%CI, 89.2%–91.1%) among adolescents aged 13–17 years [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ].
      While existing literature estimates coverage for each of these individual vaccines, NIS-Teen data have not yet been used to evaluate vaccination completion of all recommended adolescent vaccines both nationally and by state. This measure of vaccine completion across all recommended vaccines is important to better understand the extent to which adolescents are fully protected against vaccine-preventable diseases and to be able to tailor interventions aimed at improving vaccination rates as needed. In addition, while previous research has shown disparities in vaccination coverage by state and socioeconomic status [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ,
      • Walker T.Y.
      • Elam-Evans L.D.
      • Williams C.L.
      • et al.
      Trends in human papillomavirus (HPV) vaccination initiation among adolescents aged 13-17 by metropolitan statistical area (MSA) status, National Immunization Survey - teen, 2013 - 2017.
      ], an understanding of the potential factors contributing to the observed disparities is lacking. This study aimed to evaluate composite measures of completion of ACIP-recommended HPV, MenACWY, and Tdap vaccines at the age of 17 years and to identify individual- and state-level factors associated with the composite vaccination completion measure.

      Methods

      This cross-sectional study retrospectively analyzed data from 2015 to 2018 NIS-Teen integrated with publicly available state-level data. The 4 years of NIS-Teen data were pooled to increase the sample size for the analysis and thus improve the precision of state-level estimates. Included in the analysis were data from adolescents 17 years of age at the time of the survey, who were living in one of the 50 US states or the District of Columbia, and whose provider-reported vaccination data were adequate to establish whether they were up to date with the recommended vaccination schedule. The study only included 17-year-old individuals (and not younger ages) to be able to capture all recommended adolescent vaccines, including the MenACWY booster at the age of 16 years.
      The NIS-Teen survey is sponsored and conducted every year by the Centers for Disease Control and Prevention (CDC) and records provider-reported vaccination coverage data for adolescents aged 13–17 years. Sociodemographic characteristics are collected during a telephone interview with the adolescent's parent or guardian, and after their consent, immunization data are obtained through the adolescent's vaccination provider(s).

       Study endpoints

      The primary end point was a derived composite measure of vaccination completion. This was estimated as the percentage of adolescents aged 17 years who received all recommended doses of (1) HPV series (i.e., receipt of two doses for individuals aged 9–14 years at first vaccination or receipt of three doses for individuals aged 15 years or older at first vaccination) [
      Centers for Disease Control and Prevention (CDC)
      HPV vaccine recommendations.
      ], (2) MenACWY series (i.e., receipt of two doses) [
      Centers for Disease Control and Prevention (CDC)
      Meningococcal vaccine recommendations.
      ], and (3) Tdap vaccine (i.e., receipt of one dose) [
      Centers for Disease Control and Prevention (CDC)
      Diphtheria, tetanus, and pertussis vaccine recommendations.
      ].
      We assumed that all individuals were eligible for the recommended vaccinations in their age group because the NIS-Teen data do not provide information on ineligibility due to contraindications or other reasons. Because the NIS-Teen data were pooled, all completion estimates represent a pooled average over the 2015–2018 time frame.

       Covariates

      Individual-level variables included in the analysis involved sociodemographic and health insurance characteristics, most of which have previously been shown to be associated with vaccine uptake [
      • Takayama M.
      • Wetmore C.M.
      • Mokdad A.H.
      Characteristics associated with the uptake of influenza vaccination among adults in the United States.
      ,
      • Lau J.S.
      • Adams S.H.
      • Irwin Jr., C.E.
      • et al.
      Receipt of preventive health services in young adults.
      ,
      • Yoo B.K.
      • Hasebe T.
      • Szilagyi P.G.
      Decomposing racial/ethnic disparities in influenza vaccination among the elderly.
      ,
      • Forshaw J.
      • Gerver S.M.
      • Gill M.
      • et al.
      The global effect of maternal education on complete childhood vaccination: A systematic review and meta-analysis.
      ,
      • Feemster K.A.
      • Spain C.V.
      • Eberhart M.
      • et al.
      Identifying infants at increased risk for late initiation of immunizations: Maternal and provider characteristics.
      ]. These variables included sex, race/ethnicity, maternal education, health insurance status, continuity of health insurance coverage since the age of 11 years, whether the adolescent was 16 or 17 years of age at the last checkup, number of physician or other health care professional visits during the past 12 months, whether a doctor or other health care professional ever recommended that the adolescent should receive the HPV vaccine, and the state of residence.
      Furthermore, state-level variables that could be considered “actionable,” that is, that could be influenced by local initiatives and policies, were obtained from external data sources (Table A1) and linked to the NIS-Teen data by state. Variables that were duplicates of individual-level or other state-level variables were excluded. Variables with limited variation across states were also excluded. As a result of this initial selection phase, more than 25 variable categories were considered for inclusion in the multilevel model analysis, details of which are summarized in Table A1. Because some of the state-level variables were available only for a single year, we generally used the most recent year of available data that best aligned with the available years of data from NIS-Teen. Those variables with data available for 2015–2018 were averaged across that period. The five state-level variables that were retained in the final multilevel model (with year of data availability) included the following:

       Statistical methods

      The unadjusted composite vaccination completion was calculated at the national level and by state. Results included point estimates and 95% CIs, accounting for NIS-Teen sampling weights [
      Centers for Disease Control and Prevention (CDC)
      About the National Immunization Surveys (NIS). National immunization survey-teen (NIS-teen) A. Purpose and scope and B. A user’s guide for the 2018 public-use data file.
      ]. As the NIS-Teen has a complex survey design, the analysis weights provided by NIS-Teen using their weighting methodology [
      Centers for Disease Control and Prevention (CDC)
      About the National Immunization Surveys (NIS). National immunization survey-teen (NIS-teen) A. Purpose and scope and B. A user’s guide for the 2018 public-use data file.
      ] were used in all analyses to produce estimates representative of the overall US adolescent population. Missing data owing to differential willingness to participate in the NIS-Teen survey were accounted for in the NIS-Teen weighting methodology [
      Centers for Disease Control and Prevention (CDC)
      About the National Immunization Surveys (NIS). National immunization survey-teen (NIS-teen) A. Purpose and scope and B. A user’s guide for the 2018 public-use data file.
      ].
      Model-adjusted composite vaccination completion at national- and state-level was calculated after controlling for the individual-level variables using multivariable logistic regression (Appendix, Supplementary methods a). Individual-level covariates were selected for inclusion using a systematic variable selection process [
      • Hosmer D.W.
      • Lemeshow S.
      • Sturdivant R.X.
      Applied logistic regression.
      ] (Supplementary methods a). Results were summarized through weighted odds ratios (ORs) with associated 95% CIs and p values. Weighted ORs were displayed graphically in a forest plot. Model-adjusted vaccination completion estimates and 95% CIs were generated using predicted marginal proportions [
      • Bieler G.S.
      • Brown G.G.
      • Williams R.L.
      • et al.
      Estimating model-adjusted risks, risk differences, and risk ratios from complex survey data.
      ]; a corresponding heat map was created displaying the average state-level estimates for the pooled data.
      Multilevel modeling was used to evaluate the association between individual- and state-level characteristics and vaccination completion (Appendix, Supplementary methods b). Individuals were treated as nested within their states of residence. At the first level, the log odds of vaccination completion were modeled using fixed effects for individual-level along with a random intercept term; the same individual-level covariates with those in the previous regression model were used. At the second level, the state-level intercepts were modeled as a function of state-level covariates (also selected using a systematic variable selection process [Appendix, Supplementary methods b]) and a state-specific random effect to account for within-state correlation. Survey weights were rescaled so that the new weights summed to the cluster sample size [
      • Carle A.C.
      Fitting multilevel models in complex survey data with design weights: Recommendations.
      ]. Weighted ORs and 95% CIs for each individual- and state-level factor were generated.
      As part of the multilevel modeling, the variance partition coefficient (VPC) and median OR (MOR) were calculated to quantify the interstate heterogeneity in likelihood of vaccination completion [
      • Merlo J.
      • Wagner P.
      • Ghith N.
      • et al.
      An original stepwise multilevel logistic regression analysis of discriminatory accuracy: The case of neighbourhoods and health.
      ] (Appendix, Supplementary methods c). Of the total observed individual variation in vaccination completion, the VPC indicates the proportion that can be attributed to between-state variation; the MOR reflects how much the likelihood of vaccination completion (in median) would increase for a randomly selected individual moving to a state with higher vaccination completion.
      SAS statistical software (version 9.4; SAS Institute; Cary, North Carolina) with SUDAAN 11 (RTI International; Research Triangle Park, North Carolina; 2012) was used for the analyses.

      Results

       Vaccination completion

      After controlling for individual-level sociodemographic and health care use characteristics, the pooled 2015–2018 average adjusted composite vaccination completion rate was 30.6% (95% CI, 30.1%–31.0%) nationally, varying across states from 11.3 % in Idaho (95% CI, 6.9%–18.0%) to 56.4% (95% CI, 49.8%–62.8%) in Rhode Island (Figure 1, Table A2). Compared with the reference state, Alabama (selected alphabetically), 27 states had higher likelihoods of vaccination completion, with only Idaho having a lower likelihood of completion (Figure A1). As an example, the likelihood of vaccination completion is nearly six times higher in Rhode Island than in Alabama (OR, 5.92; 95% CI, 3.63–9.65).
      Figure thumbnail gr1
      Figure 1Model-adjusted composite completion of ACIP-recommended HPV, MenACWY, and Tdap vaccines among 17-year-old individuals in the United States, 2015–2018. (A) Composite vaccination completion was based on completion of the HPV vaccine series (i.e., receipt of two doses for individuals aged 9–14 years at first vaccination or receipt of three doses for individuals aged 15 years or older at first vaccination), completion of the MenACWY vaccine series (i.e., receipt of two doses), and receipt of the Tdap vaccine. (B) Model-adjusted composite vaccination completion was adjusted for sex, race/ethnicity, maternal education, health insurance status, continuity of health insurance coverage since the age of 11 years, whether the adolescent was 16 or 17 years of age at their last checkup, the number of physician or other health care professional visits in past 12 months, whether a doctor or other health care professional ever recommended that the adolescent receive the HPV vaccine, and the resident state. ACIP, Advisory Committee on Immunization Practices; HPV, human papillomavirus; MenACWY, quadrivalent meningococcal conjugate; Tdap, tetanus, diphtheria, and acellular pertussis.
      The unadjusted 2015–2018 average NIS-Teen weighted composite vaccination completion rates can be found in the Table A3.

       Individual- and state-level characteristics associated with vaccination completion

      Figure 2 summarizes the multilevel model results on individual- and state-level variables associated with vaccination completion. As per these results, 17-year-old individuals who were female (OR, 1.35; 95% CI, 1.22–1.49), Hispanic (OR, 1.55; 95% CI, 1.30–1.84), or non-Hispanic black (OR, 1.63; 95% CI, 1.25–2.13) were more likely to have received all three vaccines (Figure 2). Adolescents whose mothers had more than 12 years of education but were not college graduates (OR, .71; 95% CI, .60–.86) were less likely to have received all vaccinations as compared with adolescents whose mothers had less than 12 years of education (Figure 2).
      Figure thumbnail gr2
      Figure 2Individual- and state-level variables associated with an individual's composite completion of ACIP-recommended HPV, MenACWY, and Tdap vaccines among 17-year-old individuals in the United States, 2015–2018. (A) Composite vaccination completion is based on completion of the HPV series (i.e., receipt of two doses for individuals aged 9–14 years at first vaccination or receipt of three doses for individuals aged 15 years or older at first vaccination), completion of the MenACWY series (i.e., receipt of two doses), and receipt of the Tdap vaccine. (B) The continuous state-level variables are in SD units. ACIP, Advisory Committee on Immunization Practices; CI, confidence interval; HCP, health care provider; HPV, human papillomavirus; MenACWY, quadrivalent meningococcal conjugate; PCP, primary care physician; Tdap, tetanus, diphtheria, and acellular pertussis. ∗Data for 2014; †data for 2019; ‡data for 2017; ∗∗pooled data 2015–2018.
      Furthermore, being insured through Medicaid was associated with increased likelihood of being vaccinated compared to private/other insurance (OR, 1.25; 95% CI, 1.02–1.53), whereas adolescents who were uninsured (OR, .65; 95 % CI, .45–.93) at the time of the survey or who had been uninsured at some point since the age of 11 years (OR, .73; 95% CI, .54–.98) were less likely to have received all three vaccinations.
      Likelihood of vaccination completion was higher for individuals with recent checkups (i.e., adolescents who were aged 16 or 17 years at the last checkup [OR, 2.35; 95% CI, 1.80–3.07]) and for individuals who had received a doctor's or other HCP's recommendation for HPV vaccination (OR, 3.24; 95% CI, 2.76–3.80) (Figure 2). Adolescents who had a record of more frequent HCP visits in the past 12 months also were more likely to have completed all vaccinations (Figure 2). Of the state-level variables, adolescents in states with MenACWY school mandates had higher likelihood of vaccination completion (OR, 1.64; 95% CI, 1.16–2.33).
      The calculated VPC value was .035, indicating that 3.5 % of the total observed individual variation in composite vaccination completion could be attributed to between-state variation. The calculated MOR value was 1.39, indicating that if individuals move to another state with a higher likelihood of vaccination completion, the individual's likelihood of receiving all three vaccinations would (in median) increase by 39%.

      Discussion

      The present study found that in the period 2015–2018, only three of 10 US adolescents aged 17 years had received the full complement of the ACIP-recommended HPV, MenACWY, and Tdap vaccines. Moreover, the vaccination completion rates for the full complement were substantially lower than the vaccination coverage for each vaccine separately, as shown by the latest NIS-Teen data analysis [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ].
      Previous published data on composite vaccination completion rates are scarce. An analysis of 2009–2014 MarketScan insurance claims data found that among adolescents aged 11 years, only 26.5% received one dose of each of the three vaccines HPV, MenACWY, and Tdap during the study's median follow-up of 16 months (interquartile range 7.1–31.2) [
      • Vielot N.A.
      • Butler A.M.
      • Brookhart M.A.
      • et al.
      Patterns of use of human papillomavirus and other adolescent vaccines in the United States.
      ]. This analysis also found that only 56.1% of adolescents received at least one of the adolescent vaccines [
      • Vielot N.A.
      • Butler A.M.
      • Brookhart M.A.
      • et al.
      Patterns of use of human papillomavirus and other adolescent vaccines in the United States.
      ]. Therefore, although many adolescents are receiving at least some of the recommended vaccines, as indicated by the higher coverage rates for the individual vaccines [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ], few are receiving all of them. These findings indicate the importance of evaluating a composite measure of vaccination, in order to identify and target quality improvement initiatives for adolescents who have not received all age-appropriate recommended vaccines (e.g., to educate on the value of the remaining vaccines that have not yet been completed).
      The present study also found that vaccination completion rates varied substantially across states. This is consistent with previous analyses reporting differences in adolescents' vaccination rates by place of residence [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ,
      • Vielot N.A.
      • Butler A.M.
      • Brookhart M.A.
      • et al.
      Patterns of use of human papillomavirus and other adolescent vaccines in the United States.
      ,
      • Fuller K.M.
      • Hinyard L.
      Factors associated with HPV vaccination in young males.
      ,
      • Nelson N.P.
      • Yankey D.
      • Singleton J.A.
      • et al.
      Hepatitis A vaccination coverage among adolescents (13-17 years) in the United States, 2008-2016.
      ,
      • Cheng W.Y.
      • Chang R.
      • Novy P.
      • et al.
      Determinants of meningococcal ACWY vaccination in adolescents in the US: Completion and compliance with the CDC recommendations.
      ]. For example, in an analysis of NIS-Teen 2011–2016 data, MenACWY vaccination completion rates among adolescents aged 17 years varied from 8.7% in Idaho to 39.7% in Michigan [
      • Cheng W.Y.
      • Chang R.
      • Novy P.
      • et al.
      Determinants of meningococcal ACWY vaccination in adolescents in the US: Completion and compliance with the CDC recommendations.
      ]. These results are consistent with our findings, where Idaho had the lowest vaccination completion rate and only a handful of other states had completion rates that were higher than Michigan. In 2019, state-specific vaccination rates among adolescents aged 13–17 years ranged from 81.7% in Alaska to 96.7% in North Dakota for ≥1 dose of Tdap vaccine, from 60.3 % in Mississippi to 98.2% in Rhode Island for ≥1 dose of MenACWY vaccine, and from 49.5% in Mississippi to 91.9% in Rhode Island for ≥1 dose of HPV vaccine [
      • Elam-Evans L.D.
      • Yankey D.
      • Singleton J.A.
      • et al.
      National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
      ]. Consistent with these results, we found the highest completion rate in Rhode Island, followed by North Dakota. Of note, Rhode Island was the first state to include the booster dose in their MenACWY mandate and was also the only state with an active HPV mandate covering both males and females during our study period, factors that might have contributed to a “vaccination culture” in this state.
      Furthermore, the present study evaluated individual- and state-level variables associated with vaccination completion rates, in order to identify “actionable” factors for which provider and/or policy decisions can be leveraged to improve vaccination coverage across states). As an example, adolescents in states with school MenACWY vaccination mandates (including mandates requiring just the first dose or first dose and booster) were more likely to receive all three HPV, MenACWY, and Tdap vaccines, providing state-level decision makers with an actionable strategy to increase vaccination completion. In a post hoc analysis of model-adjusted vaccination completion rates by MenACWY mandate status, median completion rates were generally lower for states that had no MenACWY mandate at the start of our study period in 2015 (29.2%; range: 13.2%–47.1 %) as compared with states that had a 1-dose MenACWY mandate (35.0%; range: 11.3%–40.3%) or also required a booster dose as part of the mandate (35.2%; range: 29.0%–56.4%).
      Our findings are consistent with previously documented higher rates of vaccination among states with mandates [
      • Nelson N.P.
      • Yankey D.
      • Singleton J.A.
      • et al.
      Hepatitis A vaccination coverage among adolescents (13-17 years) in the United States, 2008-2016.
      ,
      • Cheng W.Y.
      • Chang R.
      • Novy P.
      • et al.
      Determinants of meningococcal ACWY vaccination in adolescents in the US: Completion and compliance with the CDC recommendations.
      ]. A recent study showed that strengthening school vaccination policies for those entering the 12th grade significantly increased MenACWY, HPV, and MenB vaccination rates among 17–18 year-old individuals [
      • Srivastava T.
      • Emmer K.
      • Feemster K.A.
      Impact of school-entry vaccination requirement changes on clinical practice implementation and adolescent vaccination rates in metropolitan Philadelphia.
      ]. However, states have been slow to adopt and mandate policies [
      • Rodriguez S.A.
      • Mullen P.D.
      • Lopez D.M.
      • et al.
      Factors associated with adolescent HPV vaccination in the U.S.: A systematic review of reviews and multilevel framework to inform intervention development.
      ]. For example, although the first MenACWY vaccination mandate was implemented in August 2005 [
      Immunization Action Coalition
      State information. MenACWY vaccine mandates for elementary and secondary schools.
      ], approximately 16 years later, there are still 17 states without MenACWY school mandates (Figure A2) and only 18 states include the booster dose as part of the mandate.
      With only four states with active HPV mandates as of 2020 [
      Immunization Action Coalition
      State information. MenACWY vaccine mandates for elementary and secondary schools.
      ], the implementation of HPV vaccination mandates has been particularly slow in the US as parents often are reluctant to support them [
      • Rodriguez S.A.
      • Mullen P.D.
      • Lopez D.M.
      • et al.
      Factors associated with adolescent HPV vaccination in the U.S.: A systematic review of reviews and multilevel framework to inform intervention development.
      ,
      • Barraza L.
      • Weidenaar K.
      • Campos-Outcalt D.
      • et al.
      Human Papillomavirus and Mandatory Immunization Laws: What can we learn from early mandates?.
      ,
      • Brandt H.M.
      • Pierce J.Y.
      • Crary A.
      Increasing HPV vaccination through policy for public health benefit.
      ]. In addition to Rhode Island, the District of Columbia and Virginia also had HPV mandates in place during our study period, although they only covered female individuals; Hawaii implemented an HPV mandate more recently in 2020. In states that lack adolescent HPV mandates or comprehensive mandates that cover both male and female individuals, providers may play a particularly important role in consistently recommending these vaccines to patients and addressing any potential disparities. A post hoc analysis found that female individuals had a higher model-adjusted vaccination completion rate as compared with male individuals (34.0%; 95% CI, 31.9%–36.1% vs. 27.2%; 95% CI, 25.3%–29.1%, respectively), which speaks to the need to consider increased emphasis of vaccine recommendations for both sexes.
      Insurance coverage was another policy-relevant variable associated with vaccination completion. Because the ACIP-recommended vaccines are included in the Vaccines for Children (VFC) program, the CDC is able to purchase these vaccines at a discount price and distribute them to VFC grantees (e.g., state health departments), who then provide them to registered VFC providers at no charge [
      Centers for Disease Control and prevention (CDC)
      Vaccines for children program (VFC).
      ]. In this study, uninsured or occasionally insured adolescents were less likely to have received all ACIP-recommended vaccines compared with insured counterparts. Moreover, those with Medicaid insurance were more likely to have received all vaccines than those with private insurance. This is possibly because Medicaid-insured adolescents are eligible to receive the vaccines at no cost through the VFC program. Uninsured and underinsured individuals are also eligible for the VFC program, but this might not have successfully been communicated to these adolescents [
      • Hill H.A.
      • Singleton J.A.
      • Yankey D.
      • et al.
      Vaccination coverage by age 24 months among children born in 2015 and 2016 - National Immunization Survey-Child, United States, 2016-2018.
      ], who, with other cost–related concerns, may be less likely to visit their providers in general and thus might not take advantage of no-cost vaccines.
      The current and previous research findings [
      • Vielot N.A.
      • Butler A.M.
      • Brookhart M.A.
      • et al.
      Patterns of use of human papillomavirus and other adolescent vaccines in the United States.
      ,
      • Nelson N.P.
      • Yankey D.
      • Singleton J.A.
      • et al.
      Hepatitis A vaccination coverage among adolescents (13-17 years) in the United States, 2008-2016.
      ,
      • Cheng W.Y.
      • Chang R.
      • Novy P.
      • et al.
      Determinants of meningococcal ACWY vaccination in adolescents in the US: Completion and compliance with the CDC recommendations.
      ,
      • Lu P.J.
      • Yankey D.
      • Jeyarajah J.
      • et al.
      Hepatitis B vaccination among adolescents 13-17 years, United States, 2006-2012.
      ,
      • Landis K.
      • Bednarczyk R.A.
      • Gaydos L.M.
      Correlates of HPV vaccine initiation and provider recommendation among male adolescents, 2014 NIS-teen.
      ] showed that (1) checkups at the ages of 16–17 years, (2) frequency of health care visits in the past 12 months, and (3) provider recommendations for HPV vaccines are health care–related variables that can be leveraged by providers and policy decision makers to increase completion of all recommended adolescent vaccines. In 2017, the CDC established the immunization platform visit at the age of 16 years [
      Centers for Disease Control and Prevention (CDC)
      Recommended immunization schedule for children and adolescents aged 18 years or younger, United States, 2017.
      ], providing an opportunity for HCPs to explicitly recommend age-appropriate vaccinations, which has been shown here and in previous studies to be associated with increased adolescent vaccination rates [
      • Rodriguez S.A.
      • Mullen P.D.
      • Lopez D.M.
      • et al.
      Factors associated with adolescent HPV vaccination in the U.S.: A systematic review of reviews and multilevel framework to inform intervention development.
      ,
      • Lu P.J.
      • Yankey D.
      • Jeyarajah J.
      • et al.
      Impact of provider recommendation on Tdap vaccination of adolescents aged 13-17 years.
      ,
      • Lu P.J.
      • Yankey D.
      • Fredua B.
      • et al.
      Association of provider recommendation and human papillomavirus vaccination initiation among male adolescents aged 13-17 years-United States.
      ]. The addition of this clearly defined visit in the adolescent immunization schedule was championed by several professional societies that saw it not only as an opportunity to administer a second MenACWY vaccine dose but also as an opportunity to catch up on other childhood vaccinations that may have been missed [
      Society for Adolescent Health and Medicine
      Establishing an immunization platform for 16-year-olds in the United States.
      ,
      • Munger M.
      • Yasuda K.
      • Hollier L.M.
      • et al.
      16-year-old patients: make sure they receive their annual well visit and vaccinations.
      ].
      This study found that after adjusting for individual- and state-level characteristics, substantial variation in completion rates across states remained, as indicated by the relatively low VPC and MOR values (representing the proportion of variance that can be attributed to between-state variation and how much the likelihood of completion would increase in median for a randomly selected individual moving to a state with higher completion, respectively). Therefore, additional factors may be impacting the observed completion rates, such as attitudes and beliefs related to vaccines or access and reimbursement barriers. Additional research is needed to determine other factors that may help to further explain state-level differences in adolescent vaccination completion rates.

       Limitations

      Several study limitations should be noted. Given the lack of universal and interconnected patient-level immunization records in the United States, it was necessary to use NIS-Teen, a survey which includes both parent and provider-reported data on immunization status. Although the NIS-Teen data include statistical adjustments to account for telephone survey nonresponse and households without cell phones, some bias may persist. The present analysis did not consider whether the vaccines had been received on time or within the recommended age span of vaccination. In addition, provider-reported vaccination histories may be incomplete, potentially resulting in underestimated vaccination coverage. Another factor that may contribute to the underestimation of completion rates is that the NIS-Teen survey does not include individuals aged 18 years and older. Three states did not meet the CDC standards for precision of subgroup estimates [
      Centers for Disease Control and Prevention (CDC)
      About the National Immunization Surveys (NIS). National immunization survey-teen (NIS-teen) A. Purpose and scope and B. A user’s guide for the 2018 public-use data file.
      ]. As a result, vaccination completion was further analyzed by 4-category census region and 9-category census divisions. The individual- and state-level variables included in the present study were limited to those available in the NIS-Teen data and publicly available external data sources, respectively. Furthermore, because the analysis focused on state-level variables that were deemed actionable, the study may have excluded other state-level factors affecting vaccination coverage (e.g., demographic composition). The included state-level variables also may not capture factors impacting likelihood of vaccination at a more local level (e.g., vaccination initiatives in local communities or neighborhoods, attitudes and beliefs toward vaccinations within social groups).
      The COVID-19 pandemic severely impacted vaccination coverage rates for other vaccine-preventable diseases across all age groups [
      The COVID-19 pandemic: Impact on US adolescent and adult vaccine utilization across markets. Avalere health white paper.
      ,
      • Santoli J.M.
      • Lindley M.C.
      • DeSilva M.B.
      • et al.
      Effects of the COVID-19 pandemic on routine pediatric vaccine ordering and administration - United States, 2020.
      ,
      • Hong K.
      • Zhou F.
      • Tsai Y.
      • et al.
      Decline in receipt of vaccines by medicare beneficiaries during the COVID-19 pandemic - United States, 2020.
      ,
      • Bramer C.A.
      • Kimmins L.M.
      • Swanson R.
      • et al.
      Decline in child vaccination coverage during the COVID-19 pandemic - Michigan Care Improvement Registry, May 2016-May 2020.
      ]. In the US, declines in childhood vaccination rates were reported in multiple studies as early as May 2020 [
      • Santoli J.M.
      • Lindley M.C.
      • DeSilva M.B.
      • et al.
      Effects of the COVID-19 pandemic on routine pediatric vaccine ordering and administration - United States, 2020.
      ,
      • Bramer C.A.
      • Kimmins L.M.
      • Swanson R.
      • et al.
      Decline in child vaccination coverage during the COVID-19 pandemic - Michigan Care Improvement Registry, May 2016-May 2020.
      ]. More recently, an analysis of adult and adolescent vaccine claims found a 41%–53% decrease in aggregate claims between March to August 2020 as compared with the same months in 2019 [
      The COVID-19 pandemic: Impact on US adolescent and adult vaccine utilization across markets. Avalere health white paper.
      ]. Therefore, efforts are needed to address the urgent challenges [
      • Immunization, Vaccines and Biologicals
      Special feature: Immunization and COVID-19 - second pulse poll offers a more detailed understanding of disruptions to vaccination caused by COVID-19 and how to respond.
      ] of regaining losses in vaccine uptake, resuming routine immunization services, and further improving vaccination coverage.

      Conclusions

      Among US adolescents aged 17 years during 2015–2018, composite HPV, MenACWY, and Tdap vaccination completion rates were suboptimal and highly variable across states. In addition, the study evaluated several factors associated with vaccination completion to identify strategies that may be implemented by providers and policy decision makers to increase adolescent vaccination completion. These potential strategies include health care visits at 16–17 years of age, recommendation from providers for the HPV vaccine, expansion of insurance coverage, including Medicaid, and state mandates for MenACWY vaccination completion of recommended adolescent vaccines.

      CRediT Authorship Contribution Statement

      EL, DG, SH, SP, PN, and PG contributed to the conception and design of the study and manuscript. SH, EL and SP contributed to the acquisition of data. EL, DG, and SP performed the analysis and all authors participated in the interpretation of data. All authors revised the article critically for important intellectual content and provided final approval of the submitted version.

      Acknowledgments

      The authors thank the Business & Decision Life Sciences platform for editorial assistance and manuscript coordination, on behalf of GSK. Amandine Radziejwoski coordinated the manuscript development and editorial support. Athanasia Benekou provided medical writing support. EL, SP, and PG are employed by the GSK group of companies and hold shares in the GSK group of companies. PN was an employee of the GSK group of companies at the time of the study. DG and SH are employees of RTI Health Solutions, which was contracted by the GSK group of companies to design and implement the present study.

      Funding Sources

      GlaxoSmithKline Biologicals SA funded this study (GSK Study Identifier: HO-19-19991) and was involved in all stages of study conduct, including analysis of the data. GlaxoSmithKline Biologicals SA also covered all costs associated with the development and publication of this manuscript.

      Supplementary Data

      References

        • Robinson C.L.
        • Bernstein H.
        • Poehling K.
        • et al.
        Advisory committee on immunization practices recommended immunization schedule for children and adolescents aged 18 years or younger - United States, 2020.
        MMWR Morb Mortal Wkly Rep. 2020; 69: 130-132
        • Centers for Disease Control and Prevention (CDC)
        Diphtheria, tetanus, and pertussis vaccine recommendations.
        (Available at:)
        • Centers for Disease Control and Prevention (CDC)
        Meningococcal vaccine recommendations.
        (Available at:)
        • Centers for Disease Control and Prevention (CDC)
        HPV vaccine recommendations.
        (Available at:)
        • Curran D.
        • Van Oorschot D.
        • Varghese L.
        • et al.
        Assessment of the potential public health impact of Herpes Zoster vaccination in Germany.
        Hum Vaccin Immunother. 2017; 13: 2213-2221
        • Immunization of adolescents
        Recommendations of the Advisory Committee on Immunization Practices, the American Academy of Pediatrics, the American Academy of Family Physicians, and the American Medical Association.
        MMWR Recomm Rep. 1996; 45: 1-16
        • Society for Adolescent Health and Medicine
        Establishing an immunization platform for 16-year-olds in the United States.
        J Adolesc Health. 2017; 60: 475-476
        • Elam-Evans L.D.
        • Yankey D.
        • Singleton J.A.
        • et al.
        National, regional, state, and selected local area vaccination coverage among adolescents aged 13-17 years - United States, 2019.
        MMWR Morb Mortal Wkly Rep. 2020; 69: 1109-1116
        • Walker T.Y.
        • Elam-Evans L.D.
        • Williams C.L.
        • et al.
        Trends in human papillomavirus (HPV) vaccination initiation among adolescents aged 13-17 by metropolitan statistical area (MSA) status, National Immunization Survey - teen, 2013 - 2017.
        Hum Vaccin Immunother. 2020; 16: 554-561
        • Takayama M.
        • Wetmore C.M.
        • Mokdad A.H.
        Characteristics associated with the uptake of influenza vaccination among adults in the United States.
        Prev Med. 2012; 54: 358-362
        • Lau J.S.
        • Adams S.H.
        • Irwin Jr., C.E.
        • et al.
        Receipt of preventive health services in young adults.
        J Adolesc Health. 2013; 52: 42-49
        • Yoo B.K.
        • Hasebe T.
        • Szilagyi P.G.
        Decomposing racial/ethnic disparities in influenza vaccination among the elderly.
        Vaccine. 2015; 33: 2997-3002
        • Forshaw J.
        • Gerver S.M.
        • Gill M.
        • et al.
        The global effect of maternal education on complete childhood vaccination: A systematic review and meta-analysis.
        BMC Infect Dis. 2017; 17: 801
        • Feemster K.A.
        • Spain C.V.
        • Eberhart M.
        • et al.
        Identifying infants at increased risk for late initiation of immunizations: Maternal and provider characteristics.
        Public Health Rep. 2009; 124: 42-53
        • Kaiser Family Foundation (KFF) State Health Facts
        About state health facts. 2020.
        (Available at:)2020
        • Immunization Action Coalition
        State information. MenACWY vaccine mandates for elementary and secondary schools.
        (Available at:)
        https://www.immunize.org/laws/menin_sec.asp
        Date accessed: September 22, 2020
        • Centers for Disease Control and Prevention (CDC)
        About the National Immunization Surveys (NIS). National immunization survey-teen (NIS-teen) A. Purpose and scope and B. A user’s guide for the 2018 public-use data file.
        (Available at:) (Accessed July 21, 2020)
        • Hosmer D.W.
        • Lemeshow S.
        • Sturdivant R.X.
        Applied logistic regression.
        3rd edition. John Wiley and Sons, Inc., Hoboken, NJ2013
        • Bieler G.S.
        • Brown G.G.
        • Williams R.L.
        • et al.
        Estimating model-adjusted risks, risk differences, and risk ratios from complex survey data.
        Am J Epidemiol. 2010; 171: 618-623
        • Carle A.C.
        Fitting multilevel models in complex survey data with design weights: Recommendations.
        BMC Med Res Methodol. 2009; 9: 49
        • Merlo J.
        • Wagner P.
        • Ghith N.
        • et al.
        An original stepwise multilevel logistic regression analysis of discriminatory accuracy: The case of neighbourhoods and health.
        PLoS One. 2016; 11: e0153778
        • Vielot N.A.
        • Butler A.M.
        • Brookhart M.A.
        • et al.
        Patterns of use of human papillomavirus and other adolescent vaccines in the United States.
        J Adolesc Health. 2017; 61: 281-287
        • Fuller K.M.
        • Hinyard L.
        Factors associated with HPV vaccination in young males.
        J Community Health. 2017; 42: 1127-1132
        • Nelson N.P.
        • Yankey D.
        • Singleton J.A.
        • et al.
        Hepatitis A vaccination coverage among adolescents (13-17 years) in the United States, 2008-2016.
        Vaccine. 2018; 36: 1650-1659
        • Cheng W.Y.
        • Chang R.
        • Novy P.
        • et al.
        Determinants of meningococcal ACWY vaccination in adolescents in the US: Completion and compliance with the CDC recommendations.
        Hum Vaccin Immunother. 2020; 16: 176-188
        • Srivastava T.
        • Emmer K.
        • Feemster K.A.
        Impact of school-entry vaccination requirement changes on clinical practice implementation and adolescent vaccination rates in metropolitan Philadelphia.
        Hum Vaccin Immunother. 2020; 16: 1155-1165
        • Rodriguez S.A.
        • Mullen P.D.
        • Lopez D.M.
        • et al.
        Factors associated with adolescent HPV vaccination in the U.S.: A systematic review of reviews and multilevel framework to inform intervention development.
        Prev Med. 2020; 131: 105968
        • Barraza L.
        • Weidenaar K.
        • Campos-Outcalt D.
        • et al.
        Human Papillomavirus and Mandatory Immunization Laws: What can we learn from early mandates?.
        Public Health Rep. 2016; 131: 728-731
        • Brandt H.M.
        • Pierce J.Y.
        • Crary A.
        Increasing HPV vaccination through policy for public health benefit.
        Hum Vaccin Immunother. 2016; 12: 1623-1625
        • Centers for Disease Control and prevention (CDC)
        Vaccines for children program (VFC).
        (Available at:)
        • Hill H.A.
        • Singleton J.A.
        • Yankey D.
        • et al.
        Vaccination coverage by age 24 months among children born in 2015 and 2016 - National Immunization Survey-Child, United States, 2016-2018.
        MMWR Morb Mortal Wkly Rep. 2019; 68: 913-918
        • Lu P.J.
        • Yankey D.
        • Jeyarajah J.
        • et al.
        Hepatitis B vaccination among adolescents 13-17 years, United States, 2006-2012.
        Vaccine. 2015; 33: 1855-1864
        • Landis K.
        • Bednarczyk R.A.
        • Gaydos L.M.
        Correlates of HPV vaccine initiation and provider recommendation among male adolescents, 2014 NIS-teen.
        Vaccine. 2018; 36: 3498-3504
        • Centers for Disease Control and Prevention (CDC)
        Recommended immunization schedule for children and adolescents aged 18 years or younger, United States, 2017.
        (Available at:)
        • Lu P.J.
        • Yankey D.
        • Jeyarajah J.
        • et al.
        Impact of provider recommendation on Tdap vaccination of adolescents aged 13-17 years.
        Am J Prev Med. 2017; 53: 373-384
        • Lu P.J.
        • Yankey D.
        • Fredua B.
        • et al.
        Association of provider recommendation and human papillomavirus vaccination initiation among male adolescents aged 13-17 years-United States.
        J Pediatr. 2019; 206: 33-41 e31
        • Munger M.
        • Yasuda K.
        • Hollier L.M.
        • et al.
        16-year-old patients: make sure they receive their annual well visit and vaccinations.
        (Available at:)
      1. The COVID-19 pandemic: Impact on US adolescent and adult vaccine utilization across markets. Avalere health white paper.
        (Available at:)
        • Santoli J.M.
        • Lindley M.C.
        • DeSilva M.B.
        • et al.
        Effects of the COVID-19 pandemic on routine pediatric vaccine ordering and administration - United States, 2020.
        MMWR Morb Mortal Wkly Rep. 2020; 69: 591-593
        • Hong K.
        • Zhou F.
        • Tsai Y.
        • et al.
        Decline in receipt of vaccines by medicare beneficiaries during the COVID-19 pandemic - United States, 2020.
        MMWR Morb Mortal Wkly Rep. 2021; 70: 245-249
        • Bramer C.A.
        • Kimmins L.M.
        • Swanson R.
        • et al.
        Decline in child vaccination coverage during the COVID-19 pandemic - Michigan Care Improvement Registry, May 2016-May 2020.
        MMWR Morb Mortal Wkly Rep. 2020; 69: 630-631
        • Immunization, Vaccines and Biologicals
        Special feature: Immunization and COVID-19 - second pulse poll offers a more detailed understanding of disruptions to vaccination caused by COVID-19 and how to respond.
        (Available at:)