Human papillomavirus (HPV) is one of the most common sexually transmitted infections and a causal factor for cervical cancer among women.^1–3 Since 2006, vaccines to prevent infection from some types of HPV have been available and recommended for adolescents. Currently, there are 3 HPV vaccines available in the United States: a bivalent vaccine (2vHPV), licensed in 2009 for use in females, protects against HPV types 16 and 18; a quadrivalent vaccine (4vHPV), licensed in 2006 for use in females and 2009 for use in males, protects against HPV types 6, 11, 16, and 18; and a 9-valent vaccine (9vHPV), licensed in 2014 for use in males and females, protects against the 4 types included in 4vHPV plus types 31, 33, 45, 52, and 58.^1,4–6 HPV vaccination is recommended at 11 or 12 years and through 26 years for females who had not been previously vaccinated. This recommendation was based on several considerations, including vaccination safety and immunogenicity at this age, the need to vaccinate prior to HPV exposure, the practicality of administering HPV vaccine with other vaccines that are recommended at this age, and many adolescents have preventive health care visits at this age.^1,7

While ≥1-dose HPV vaccination coverage among 13-year-old girls has increased each year since 2007, coverage remains low, with only 50.6% initiating the 3-dose HPV vaccine series in 2013 by the Advisory Committee on Immunization Practices (ACIP) recommended age guidelines.^8,9 Additionally, national coverage for HPV vaccination among 13-year-old girls is much lower than the coverage for other adolescent vaccines such as the tetanus toxoid, reduced diphtheria toxoid and acellular pertussis (Tdap), and the meningococcal conjugate (MenACWY) vaccines.

The purpose of this study was to examine HPV vaccination coverage before 13 years (“on-time”) and from 13 to 17 years (“catch-up”) among girls born in 1995–2000. We identify socio-demographic factors associated with receipt of ≥1 dose of HPV vaccination before 13 years and trends across birth cohorts in receipt of ≥1 dose of HPV vaccination before 13 years overall and stratified by sociodemographic characteristics. For the most recent cohorts (the girls who were born in 1999 or 2000), we examined the percentage of girls who had missed opportunities for HPV vaccination before 13 years and the potentially achievable coverage before 13 years if these opportunities had not been missed. We also examine the association of sociodemographic factors with missed vaccination opportunity and achievable coverage. We also examine the cumulative proportion of girls receiving ≥1 dose of HPV vaccination by age, stratified by annual birth cohort.

A total of 33 707 girls between 13 and 17 years old with adequate provider data from the 2008–2013 NIS–Teen were included in the study. Table 1 shows the demographic characteristics of the 2008–2013 sample.

Figure 1 shows estimated HPV vaccination coverage before 13 years by minimum number of doses received and birth cohort. In general, vaccination coverage significantly increased (test for trend, P < .05) from the older cohort (1995) to the younger cohort (2000). For those who received ≥1 dose, the increase was from 28.4% to 46.8%; ≥2 doses, the increase was from 20.0% to 36.2%; and ≥3 doses, the increase was from 11.3% to 26.6%. Coverage for ≥1 dose of HPV and ≥2 doses of HPV vaccination increased with each subsequent cohort, though not all increases were statistically significant. Coverage for ≥3 doses of HPV vaccine increased from 1995 to 2000, although there was a plateau in coverage for the 1996–1999 birth year cohorts.

Table 2 shows coverage for ≥1 dose of HPV vaccine before 13 years by birth year cohorts and the average birth year percentage increase (ABYPI), by selected sociodemographic characteristics. For the most recent cohorts (1999–2000), the characteristics that were significantly associated with a higher level of HPV vaccination series initiation coverage compared with the referent group included Hispanic (54.6% had ≥1 dose of HPV vaccine), those with income <133% (51.7%), whose mothers were ≤34 (50.5%) or 35–44 years old (44.5%), those whose mothers had less than high school (54.9%) or high school education (50.6%), those whose mothers were divorced/widowed/separated/deceased (47.3%) or never married (51.0%), those who had an 11- to 12-year preventive care visit (51.6%), those who received provider recommendation (51.6%), those who had Medicaid insurance (47.6%), those who had other insurance (73.8%), and those living in the West census region (52.6%) (P < .05). Those living in suburban areas (39.1%) and those who had military insurance (23.9%) had lower HPV vaccination coverage (P < .05). The national ABYPI in HPV vaccination coverage among girls before 13 years was 3.1 percentage points. HPV vaccination series initiation coverage and the ABYPI were consistently highest among Hispanic girls across all cohorts. Subgroups with the highest coverage across the cohorts also tended to have higher ABYPI, including girls in households with income <133%, those whose mother’s age was ≤34 years, those whose mothers had less than high school education, and those living in the West census region.

Table 3 shows results of analysis of missed opportunities, potentially achievable coverage with ≥1 dose of HPV vaccination and the gap between potential coverage and actual coverage among the subset of girls born in 1999–2000, overall and by socio-demographic characteristics. For the most recent cohorts (1999–2000), 57.2% of girls were not vaccinated with ≥1 HPV before 13 years. Among the girls who were not vaccinated before age 13, 80.1% had a missed opportunity for the first dose of HPV vaccine before 13 years. That is, 80.1% of unvaccinated girls had a health care encounter where another vaccine was administered but the HPV vaccine was not given. If missed opportunities had been eliminated by administering the first dose of HPV vaccine during a visit when other vaccines were administered for the recent cohorts, HPV vaccination initiation before 13 years among girls would have reached 88.6%, a 45.8–percentage point difference between actual and potential coverage (Table 3, fifth column). There were only 5 subgroups among those examined with point estimates of potentially achievable coverage below 80%, including girls without a preventive care visit at 11 to 12 years, those who had not received a provider recommendation for HPV vaccination, those who had no health insurance, those who had military insurance, and those who received all vaccinations at public facilities.

Figure 2 shows the cumulative coverage for ≥1 dose of HPV vaccine by age for each birth year cohort. As expected, HPV vaccination coverage increased with age for each cohort. HPV vaccination coverage reached 59% to 62% before 18 years for the oldest cohorts for which information was available, and 60% before 16 years for girls born in 1998. HPV vaccination coverage before 14 years significantly increased from 1995 to 2000 birth year cohort (test for trend, P < .05).

We found that HPV vaccination coverage before 13 years significantly increased from girls born in 1995 through girls born in 2000. Among girls born in 2000, who reached their 13th birthday in 2013, 47% had received ≥1 HPV vaccine dose, and 27% had received all 3 recommended HPV vaccination doses before 13 years. With “catch-up” vaccination of older girls, ≥1 dose HPV vaccination coverage reached 60% before 18 years for the oldest cohorts and 54% before 14 years for girls born in 2000. Thus, a substantial amount of HPV vaccination initiation is occurring after the 13th birthday, even in the most recent birth cohorts examined (born 2000 who turned 13 in 2013). This may reflect reluctance of providers to make strong HPV vaccination recommendations for younger girls and parent’s hesitancy to consider HPV vaccination until their daughters are older.¹⁴ Delaying vaccination might lower chances of later vaccination, given less frequent preventive visits for older girls¹⁵ and less frequent opportunities for HPV vaccination when other vaccinations (e.g., Tdap, MenACWY) are administered and could increase the likelihood of infection. Vaccination coverage before 13 years increased over time for most socio-demographic subgroups, although increases were larger (>5% ABYPI) for some segments (Hispanic, household income <133% of the federal poverty level, mothers with less than high school education). Racial and ethnic differences in coverage were noted, and the ABYPI for Hispanic girls was 2.7 times that of non-Hispanic White adolescent girls (5.4% vs 2.0%, P < .05).

For the 1999–2000 birth year cohort, we identified several subgroups where >50% of the girls had initiated HPV vaccination before 13 years. These subgroups were Hispanic girls, those with household income <133% of the federal poverty level, those whose mothers were ≤34 years old, those whose mothers have less than high school education or high school education, those whose mothers never married, those who had 11- to 12-year preventive care visit, those who received provider recommendation for HPV vaccination, and those living in the West census region. Furthermore, a higher proportion of missed opportunity and lower HPV vaccination coverage were identified among the girls who were White, whose households had higher income, whose mothers were ≥45 years old, whose mothers were college educated, whose mothers were married, and who received all vaccine at private facilities. Previous research showed that a higher proportion of delay and refusal of HPV vaccine was observed for the above groups.^16,17 A similar pattern was found among 19- to 35-month-old children.¹⁸ Thus, the lower vaccination coverage and the higher missed opportunity among these groups may be related to findings of greater active delay and refusal of HPV vaccine.

Missed vaccination opportunities before 13 years were common in all sociodemographic groups examined. However, several subgroups still were less likely to have vaccination visits and had lower potentially achievable coverage (<80%), including girls who had no health insurance, did not have a preventive care visit at 11–12 years, did not receive provider recommendation, and received all their vaccinations at public facilities. This suggests that for a segment of the population, barriers to health care (lack of health insurance, lack of a medical home, financial and access issues) may be an important contributing factor for lack of HPV vaccination. Although access to vaccine is provided for uninsured girls through the Vaccines for Children (VFC) program, parents of uninsured children may lack a medical home and not be aware of opportunities to receive VFC vaccine from health departments or VFC-qualified providers.¹⁹

Our study suggests, that 93.3% of those who had an 11- to 12-year preventive care visit and 87.1% of those who received a provider recommendation had a missed opportunity identified. These findings may be related to fewer providers making a strong recommendation to 11- to 12-year-old girls. Since preventive care visits are the visit type most associated with vaccination,²⁰ and these visits are more common among younger adolescents,²¹ vaccination opportunities during preventive visits at 11 to 12 years should not be missed.^22,23 In previous studies, the factors associated with not recommending HPV vaccine strongly to 11- to 12-year-old groups included, uneasiness in communicating to parents the importance of HPV vaccination prior to daughters becoming sexually active, the time it takes to discuss HPV vaccination, and reports of more refusal of HPV vaccine among the parents of younger adolescents than older adolescents.²⁴

There are 2 major limitations in this study. First, the NIS–Teen excludes households without any telephone service and response rates were low. Some bias may remain after weighting adjustment designed to minimize nonresponse bias and incomplete representation of the target population by the sampling frame. Second, the potentially achievable coverage that could be obtained if missed opportunities were eliminated assumes that all parents would accept uptake of the missing HPV vaccine for their daughters. Since some parents may not be willing to accept the vaccine even if the provider recommended the vaccine, we may be overestimating potential vaccination coverage.

Despite these limitations, the birth cohort analysis can be used to characterize “on-time” HPV vaccination (vaccination by 13 years) and target socio-demographic groups with lagging “on-time” HPV vaccination. Analysis by birth cohort introduces a new approach to presenting NIS–Teen data that facilitates interpretation of trends in vaccination coverage and timing of vaccination by age, which are difficult to sort out in the usual analysis of the prevalence of HPV vaccination among adolescents in a given age range (eg, 13–15 or 13–17 years).

In light of recent studies that show providers giving weaker recommendations for HPV vaccination, especially to younger adolescents and their parents,^24,25 it is important that health care providers communicate with parents to understand their personal beliefs and overcome barriers regarding HPV vaccination.²⁶ Also, providers should modify their counseling practices to provide strong recommendations for HPV vaccination²⁵ and administration of all vaccines recommended for adolescents at the same visit. Strategies to decrease missed opportunities for HPV vaccination should be implemented in vaccination settings, particularly at 11 to 12 years when these opportunities are most likely to occur. These strategies include use of client reminder and recall systems with educational messages, provider reminders, standing orders, and provider vaccination coverage assessment and feedback to help ensure every provider visit is used to ensure adolescents are fully protected from vaccine-preventable infections and cancers.^27–29