Compliance With Recommendations and Opportunities for Vaccination at Ages 11 to 12 Years: Evaluation of the 2009 National Immunization Survey–Teen

Objectives To determine vaccination coverage at selected ages and by birth cohort and to assess whether all indicated vaccines were administered during vaccination visits.

Design Population-based cross-sectional study.

Setting National Immunization Survey–Teen 2009 telephone interview.

Participants United States adolescents aged 13 to 17 years with provider-reported vaccination histories (N = 20 066).

Main Outcome Measures Among all adolescents and by birth cohort: coverage estimates for 3 childhood vaccines (measles-containing, hepatitis B, and varicella) and 3 adolescent vaccines (tetanus-diphtheria and/or tetanus-diphtheria-acellular pertussis, meningococcal-containing, and human papillomavirus for girls) at selected ages.

Results By age 11 years, most adolescents had obtained the childhood vaccines. Receipt of a tetanus-diphtheria and/or tetanus-diphtheria-acellular pertussis vaccine at ages 11 to 12 years increased significantly from the 1991 to 1996 birth cohort (33.8% vs 68.2%, P < .001); receipt of meningococcal-containing vaccine at ages 11 to 12 years increased significantly from the 1993 to 1996 birth cohort (8.4% vs 50.0%, P < .001). Among girls, receipt of human papillomavirus vaccine at ages 11 to 12 years increased significantly from the 1994 to 1996 birth cohort (11.1% vs 30.5%, P < .001). Overall, 54.9% of adolescents received at least 1 vaccination visit at ages 11 to 12 years. Among adolescents who made a vaccination visit at ages 11 to 12 years and were eligible for vaccination, 19.5% did not receive tetanus-diphtheria and/or tetanus-diphtheria-acellular pertussis, 60.9% did not receive meningococcal-containing, and 62.4% did not receive human papillomavirus vaccines.

Conclusions Receipt of vaccines at the recommended ages of 11 to 12 years appears to be increasing; however, providers often do not administer all indicated vaccines during a vaccination visit.

Ensuring high coverage with the increasing number of vaccines recommended for adolescents requires an ongoing assessment of adolescent vaccination practices, including whether high coverage is being achieved at the recommended ages. Beginning in 1996, tetanus-diphtheria (Td) vaccination was recommended for 11- and 12-year-old children, and the visit at which this vaccine was administered was recommended to be used as an opportunity to provide other vaccines recommended for younger children that had not previously been given (ie, hepatitis B and measles-mumps-rubella vaccines).¹ During 2005 through 2008, several vaccine recommendations targeting the adolescent population were made (Figure). Recommendations^2-4 for new vaccines included the routine administration of meningococcal conjugate vaccine (MCV4), a booster dose of tetanus and diphtheria toxoids with acellular pertussis (Tdap) vaccine, and, for females, the quadrivalent human papillomavirus (HPV) vaccine. Expanded recommendations for existing vaccines include a second dose of varicella vaccine for all adolescents who had received only 1 dose⁵ and annual influenza vaccination for all children aged 5 to 18 years.⁶

Data on vaccination coverage for adolescents aged 13 to 17 years have been collected since 2006 through the National Immunization Survey–Teen (NIS-Teen).⁷ Vaccination coverage estimates have been reported from the 2006-2009 NIS-Teen and have shown significant increases in coverage for the tetanus booster, MCV4, and HPV vaccines.^8-11 The reported estimates reflect which vaccines teens have received throughout their life until the time of the survey; however, the estimates do not reflect the specific ages at which the vaccines were received. Furthermore, because of the timing of vaccine licensure, some adolescents included in the NIS-Teen were not eligible to receive the adolescent vaccines at the recommended ages (Figure).

To better understand adolescent vaccination, we analyzed the 2009 NIS-Teen to determine the age of vaccination overall and by birth cohort, focusing on the receipt of vaccines at the recommended ages of 11 and 12 years. Our assessment includes information about the timeliness of administration of vaccines specifically recommended for 11- and 12-year-old children, the percentage of adolescents receiving needed catch-up with childhood vaccines, and whether all indicated vaccines were administered during vaccination visits.

We analyzed data from the 2009 NIS-Teen, conducted by the Centers for Disease Control and Prevention, to estimate vaccination coverage rates for US adolescents aged 13 through 17 years. The NIS-Teen uses the same sampling method as the NIS (which is conducted annually to estimate vaccination coverage rates for US children aged 19 to 35 months).⁷ The NIS-Teen uses random-digit dialing to survey households with age-eligible adolescents and, after verbal consent is obtained, to contact vaccination providers. An Immunization History Questionnaire is mailed to all of an adolescent's vaccination providers. The Immunization History Questionnaire contains a grid for providers to record the types of vaccines and the dates they were administered. If an adolescent has multiple vaccine providers, a single immunization history is constructed. The institutional review board of the National Center for Health Statistics, Centers for Disease Control and Prevention, has reviewed and approved the conduct of data collection under the NIS-Teen and subsequent immunization-related analyses of those data, including the analyses in this report.

The NIS-Teen 2009 was conducted from January 6, 2009, through February 10, 2010, and collected information on adolescents born between January 7, 1991, and February 10, 1997. This analysis is based on adolescents with a completed interview (35 004 household interviews, 82.5% of households identified with an age-eligible adolescent) and adequate vaccination history information from the vaccination providers (20 066 adolescents, 53.7% of adolescents with a completed household interview).

We assessed 3 vaccines (measles-containing, hepatitis B, and varicella) routinely recommended for infants and young children through age 6 years, with catch-up vaccination recommended anytime thereafter. We also assessed 3 vaccines specifically recommended for routine use at ages 11 to 12 years, with catch-up recommended at ages 13 to 18 years (Td and/or Tdap [Td/Tdap], meningococcal-containing, and HPV vaccines). We assessed meningococcal-containing vaccine instead of MCV4 because some adolescents may have received the tetravalent meningococcal polysaccharide vaccine in 2006 when there was a limited supply of MCV4 (Figure). Consistent with Advisory Committee on Immunization Practices recommendations,¹² we excluded measles-containing and varicella vaccines administered before the child's first birthday and any Td vaccine administered before age 7 years.

Adolescents were determined to be up-to-date for recommended vaccines if they had received 2 or more doses of measles-containing, 3 or more doses of hepatitis B (or 2 doses if 1.0 mL of Recombivax was specified by the provider¹³), 1 or more doses of Td/Tdap, 1 or more doses of meningococcal-containing, and among girls, 1 or more doses of HPV. (Because the survey was conducted approximately 2 years after the HPV recommendation was published, we focused on initiation of the 3-dose series rather than completion.) Up-to-date status for varicella vaccine was calculated among adolescents as receipt of 2 or more doses of varicella vaccine among adolescents without a reported history of varicella disease.

For each adolescent, we calculated the age in years at which each dose of vaccine was received. Outcome measures included being up-to-date with recommended vaccines at 3 ages: by 11 years (ie, birth up to the day before the 11th birthday) to assess coverage due to childhood vaccination efforts; by 13 years (ie, up to the day before the 13th birthday) to assess vaccination efforts at 11 and 12 years of age; and at the time of the interview (13 years or older) to assess catch-up vaccination.

A vaccination visit was defined as a health care encounter in which 1 or more vaccines were given. Visit dates and vaccination information were obtained from the immunization providers' records. Because the NIS-Teen does not collect information about the dates of well-child care, chronic illness care, or acute care visits at which vaccinations were not administered, these other health care visits were not included in our analysis. For each unique vaccination visit, we calculated the child's age in years. We then determined the percentage of adolescents who made at least 1 vaccination visit while aged 11 to 12 years and the percentage who made at least 1 vaccination visit while 13 years or older.

To determine whether providers were administering all indicated vaccines during vaccination visits, we assessed, among adolescents who made vaccination visits, the percentage of adolescents who were eligible to receive each vaccine at ages 11 to 12 years and at 13 years or older. Among adolescents eligible for vaccination, we further determined the percentage who received the needed vaccine.

Because of the timing of vaccine licensure and recommendation, not all adolescents surveyed were eligible for meningococcal-containing and HPV vaccines and the second dose of varicella vaccine at age 11 to 12 years. Using a conservative approach to allow providers sufficient time to implement a new vaccine recommendation, we assumed that a given vaccine would not be administered until the vaccine recommendation had been published, which is between 4 and 9 months after vaccine licensure (Figure). Therefore, unvaccinated adolescents would be considered eligible for meningococcal-containing vaccine during vaccination visits occurring on or after May 27, 2005,² and eligible for HPV vaccine during vaccination visits occurring on or after March 23, 2007.⁴ Although a single dose of varicella vaccine was licensed in 1995 and all of the adolescents in our sample were able to receive at least 1 dose of this vaccine,¹⁴ the recommendation for a second dose for all children and adolescents was not published until June 22, 2007.⁵ Therefore, we assumed that providers would administer a second dose of this vaccine on or after June 22, 2007.

Outcome measures were determined for the overall NIS-Teen sample and by annual birth cohort, which includes calendar years 1991-1996 rather than by age at the time of interview. Adolescents in the same cohort were not necessarily the same age at the time of the interview. For example, adolescents born in 1992 were either 16 or 17 years at the time of the interview. The NIS-Teen sample included 2 adolescents born in 1997, and data for these adolescents were included only in the overall estimates.

Data analysis was conducted using commercial software (SAS, version 9.2; SAS Institute, Inc, Cary, North Carolina). Estimates of percentages and 95% confidence intervals (CIs) were calculated (SUDAAN, version 10.0; Research Triangle Institute, Research Triangle Park, North Carolina). All analyses were weighted to account for the complex sampling design of the NIS-Teen.⁷

Table 1 shows estimated vaccination coverage levels by ages 11 years, 13 years, and the time of the interview by birth cohort. In general, for measles-containing, hepatitis B, and varicella vaccines, vaccination coverage by age 11 years increased with each birth cohort, with the 1996 birth cohort having the highest vaccination coverage by this age. Overall, only 3.8% and 5.6% completed the measles-containing and hepatitis B vaccine series, respectively, after age 10 years.

Overall, 6.1% of adolescents received Td/Tdap vaccine by age 11 years; coverage increased an additional 42.1 percentage points by age 13 years and an additional 28.9 percentage points by the time of interview (Table 1). Vaccination with Td/Tdap during ages 11 to 12 years increased with each cohort; significantly more adolescents born in 1996 received Td/Tdap vaccine at ages 11 to 12 years compared with the 1991 cohort (68.2% vs 33.8%, P < .001).

Overall, 18.6% of the sample had received meningococcal-containing vaccine by age 13 years, with coverage increasing 35.8 percentage points by the date of the interview (Table 1). Receipt of meningococcal-containing vaccine at ages 11 to 12 years increased by birth cohort, with a higher percentage of adolescents born in 1996 compared with 1993 (the first cohort eligible to receive the vaccine at age 12 years) receiving the vaccine at this age (50.0% vs 8.4%, P < .001). Among girls, 10.9% had received HPV vaccine by age 13 years, with coverage increasing by 33.4 percentage points by the date of the interview. Receipt of HPV vaccine at ages 11 to 12 years increased by birth cohort, with a higher percentage of girls born in 1996 compared with 1994 (the first cohort eligible to receive the vaccine at age 12 years) receiving the vaccine at this age (30.5% vs 11.1%, P < .001).

Overall, 54.9% of adolescents made at least 1 vaccination visit at ages 11 to 12 years (Table 2). Prior to the 1994 cohort, less than half the adolescents made a vaccination visit at ages 11 to 12 years. With the 1994 cohort, there was a significant increase in adolescents with a vaccination visit, and the percentage of adolescents with a visit significantly increased with each subsequent cohort.

Results of further evaluation of which vaccines were received during a vaccination visit at ages 11 to 12 years or 13 years or older are presented in Table 3. Among adolescents who made at least 1 vaccination visit at ages 11 to 12 years, Td/Tdap was the vaccine most likely to be administered when the child was eligible (80.5%). Among adolescents who made a vaccination visit at 13 years or older, vaccines routinely recommended for adolescents (ie, Td/Tdap, meningococcal-containing, and HPV) or vaccines with recent changes to administration recommendation (varicella) were more likely to be received if the child was eligible compared with vaccines routinely recommended for children (ie, hepatitis B and measles-containing). Regardless of when the vaccination visit was made, adolescents did not receive all the vaccines that they needed during the visit.

To our knowledge, this is the first time the age of vaccination among adolescents has been analyzed using provider-reported immunization data. This analysis shows encouraging progress with implementing the 3 vaccines specifically recommended for 11- and 12-year-old children. Administration of Td/Tdap vaccine to children in that age group increased with each birth cohort and, although only a few birth cohorts were eligible to receive meningococcal-containing or HPV vaccines at 11 to 12 years, administration of these vaccines at the recommended age appears to be increasing among the youngest cohorts. Most adolescents received measles-containing and hepatitis B vaccines before they became 11 years; thus, the need for catch-up vaccination at ages 11 to 12 was quite low. Despite the progress in adolescent vaccination coverage, our results revealed that providers often administer some, but not all, indicated vaccines during a vaccination visit.

Our study found that approximately 55% of all adolescents included in the 2009 NIS-Teen had a vaccination visit at ages 11 to 12. Relying solely on this measure for the overall sample could be misleading, because the meningococcal and HPV vaccine recommendations were not in place when many adolescents included in the 2009 survey were within that age range. Evaluating this measure by year of birth allows us to see that beginning with the 1994 cohort (the first cohort eligible to receive the newly recommended vaccines as early as age 11 years), vaccination visits at ages 11 to 12 years increased, reaching a high of 74% for the 1996 birth cohort. As encouraging as these results are, there remain many adolescents 13 years or older who have not yet received all the recommended vaccines. To achieve high vaccination coverage for all adolescents, vaccination programs and providers will need to continue and/or strengthen activities for adolescents 13 years or older while also promoting vaccination at the recommended ages of 11 to 12 years.

When recommendations were made to add a second dose of measles, mumps, rubella vaccine and the 3-dose hepatitis B vaccine series to the routine childhood vaccination schedule, adopting the policy to also administer these vaccines during adolescence was a necessary strategy for increasing coverage and reducing infections. Adolescent coverage objectives for these 2 vaccines were created in the form of Healthy People 2010 objectives¹⁵ and Health Plan Employer Data and Information Set measures.¹⁶ Our results indicate that most adolescents received these vaccines before age 11 years; thus, over time, fewer and fewer adolescents need these vaccines. Given the success of the infant immunization program, which by 2000 had achieved 90% coverage for hepatitis B among children aged 19 to 35 months,¹⁷ and the introduction of hepatitis B and measles vaccine requirements for school entry, it is not surprising that few adolescents need these vaccines. Perhaps because of the success of these programs, immunization providers may not be as vigilant in checking the status of their adolescent patients for these vaccines—especially after age 13 years. Among adolescents who made a vaccination visit at 13 years or older and were eligible to receive these vaccines, only 16% received measles-containing and 37% received hepatitis B.

Simultaneous administration of all vaccines for which an adolescent is eligible, as recommended by professional organizations,^18-20 is an important strategy for attaining high coverage with adolescent vaccines. Results from our analysis found that few adolescents received all the vaccines for which they were recommended during a vaccination visit: 19.5% did not receive Td/Tdap vaccine and approximately two-thirds did not receive meningococcal-containing (60.9%) or HPV (62.4%) vaccines. Recent surveys^21,22 of physicians indicate that there is reluctance among some to administer HPV and MCV4 vaccines at these ages. Nonetheless, the limited data in our analysis suggest that vaccination with meningococcal-containing and HPV vaccines at this age may be increasing.

This study is subject to several limitations. The NIS-Teen is a telephone survey and relies on identification of vaccination providers by the household respondent and on complete and accurate reporting of vaccination histories by these providers. Bias may have occurred because of household nonresponse and with households not having landline telephones. However, less than 10% of adolescents live in households that are either cellular-only or without a landline telephone. Bias may also have occurred as the result of excluding adolescents without adequate immunization data from a provider. Previous analysis⁷ has shown that consenting households without adequate provider data compared with consenting households with adequate provider data differed on key demographic characteristics, including mother's education level, mother's marital status, federal poverty level, and health insurance status. Finally, if all vaccination providers were not identified or if some providers did not report complete immunization histories, adolescents may have been misclassified as not having received all recommended vaccinations. The NIS-Teen uses a variety of weighting strategies to reduce bias and to ensure that all adolescents in the United States are represented by adolescents with adequate provider data.⁷

There are unique challenges to attaining high coverage with recommended adolescent vaccines.^23-25 Strategies to increase coverage will need to include educating parents about recommended vaccines and the diseases they prevent and the benefits of preventive health care visits as well as working with immunization providers to encourage them to take advantage of all health care encounters to administer all vaccines for which an adolescent is eligible during the same visit.²² In August 2007, the Centers for Disease Control and Prevention developed educational materials for parents promoting preventive health care visits and vaccination of their children at ages 11 to 12 years (available at http://www.cdc.gov/vaccines/who/teens/index.html).

Our analysis of the early stages of adolescent vaccine implementation show encouraging progress with implementing the new recommendations but also indicate that more can be done to increase the frequency with which adolescents receive all necessary vaccines during a visit. With the data from the NIS-Teen, we will be able to monitor vaccine uptake of new adolescent vaccine recommendations at ages 11 and 12 years and throughout adolescence.

Correspondence: Shannon Stokley, MPH, 1600 Clifton Rd, Mail Stop A-19, Atlanta, GA 30333 (sstokley@cdc.gov).

Submitted for Publication: January 7, 2011; final revision received March 11, 2011; accepted March 15, 2011.

Author Contributions: Ms Stokley had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Stokley and Cohn. Acquisition of data: Stokley and Jain. Analysis and interpretation of data: Stokley, Cohn, Jain, and McCauley. Drafting of the manuscript: Stokley. Critical revision of the manuscript for important intellectual content: Cohn, Jain, and McCauley. Statistical analysis: Stokley.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.