National Human Papillomavirus Vaccination Coverage Among Adolescents Aged 13–17 Years — National Immunization Survey – Teen, United States, 2011

C. Robinette Curtis, MD1

Christina Dorell, MD1

David Yankey, MS1

Jenny Jeyarajah, MS1

Harrell Chesson, PhD2

Mona Saraiya, MD3

Rebecca Gold, JD4

Eileen F. Dunne, MD2

Shannon Stokley, MPH1

1Immunization Services Division, National Center for Immunization and Respiratory Diseases, CDC

2Division of STD Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD and TB Prevention, CDC

3Division of Cancer Prevention and Control, National Center for Chronic Disease Prevention and Health Promotion, CDC

4Office of Policy, Planning and Evaluation, National Center for Immunization and Respiratory Diseases, CDC

Corresponding author: C. Robinette Curtis, Immunization Services Division, National Center for Immunization and Respiratory Diseases, CDC. Telephone: 404-639-8389; E-mail: rcurtis@cdc.gov.

Introduction

Genital human papillomavirus (HPV) is the most common sexually transmitted infection in the United States. An estimated 14 million persons are newly infected with HPV each year; approximately half of new HPV infections occur among persons aged 15–24 years (1). Although the majority of HPV infections are asymptomatic and resolve, persistent infections can cause disease, including cancers. No cure exists for HPV infection; treatments can be directed only at HPV-associated lesions (e.g., warts, precancerous lesions, and cancers) (2). Annual costs of cervical cancer screening and treatment of HPV-associated health outcomes have been estimated at $8 billion (in 2010 U.S. dollars) (3). Almost all cervical cancers and many vaginal, vulvar, anal, penile, and oropharyngeal cancers are attributable to persistent, oncogenic HPV infections (4). In 2009, approximately 35,000 HPV-associated cancers were reported in the United States. Of these, 39% occurred in males (4).

Approximately 100 HPV types have been described; HPV types 16 and 18 cause approximately 70% of cervical cancers globally (2). Among types associated with other HPV-related cancers, HPV 16 is most prevalent (5). Nononcogenic types can result in clinically significant disease; HPV types 6 and 11 can cause recurrent respiratory papillomatosis (a rare condition in which warts develop in the respiratory tract) and cause nearly all genital warts (6). Approximately 355,000 (range: 250,000–1 million) new cases of genital warts are estimated to occur annually (3,7,8).

Two HPV vaccines are licensed in the United States for prevention of specific HPV types and HPV-associated outcomes. In June 2006, a quadrivalent HPV vaccine (HPV4; Gardasil; Merck and Co., Inc.) was licensed by the Food and Drug Administration (FDA) for use in females aged 9–26 years for prevention of cervical cancer, cervical cancer precursors, vulvar and vaginal cancer precursors,* and anogenital warts caused by HPV types 6,11,16, and 18 (2). In 2009, HPV4 was licensed for use in males aged 9–26 years for genital warts prevention (10). Also in 2009, FDA licensed bivalent HPV vaccine (HPV2; Cervarix; GlaxoSmithKline) for use in females aged 9–25 years for prevention of cervical cancer and cervical cancer precursors caused by HPV types 16 and 18 (11,12). In December 2010, HPV4's indications were expanded to include prevention of anal cancer in females and males (10). Both vaccines are administered as a 3-dose series over 6 months (12).

During 2006–2011, as data on parameters including safety, efficacy, and cost-effectiveness of HPV4 and HPV2 became available for females and, later, for use of HPV4 among males, CDC's Advisory Committee on Immunization Practices (ACIP) provided national vaccination recommendations. In 2006, ACIP recommended routine use of HPV4 among females (2). In 2009, ACIP issued guidance that HPV4 could be administered to males and, in October 2011, recommended routine HPV4 vaccination for males (10). ACIP recommends routine HPV vaccination for all adolescents aged 11–12 years. For females, ACIP recommends either HPV4 or HPV2; for males, ACIP recommends HPV4.† For persons who have not initiated or completed the series, ACIP recommends vaccination for females through age 26 years and males through age 21 years (10,13).§

In addition to annual seasonal influenza vaccination and routine HPV vaccination, ACIP recommends routine vaccination with tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis (Tdap) and quadrivalent meningococcal conjugate (MenACWY) vaccines for adolescents aged 11–12 years (13). Since 2005, ACIP has recommended routine Tdap and MenACWY vaccination for preteens (14–16). For persons aged ≤18 years who are not fully immunized consistent with routine recommendations, a catch-up immunization schedule is available (13).

In 2010, national Healthy People 2020 vaccination coverage targets of 80% were specified for adolescents aged 13–15 years for ≥1 dose Tdap, ≥1 dose MenACWY, and (among females) ≥3 doses of HPV vaccine (objectives IID-11.1, 11.3, and 11.4) (17). To increase rates of pediatric patients up-to-date with Level I preventive services, the National Quality Forum (NQF) has defined measures for Tdap, MenACWY, HPV, and influenza vaccines. The HPV vaccination measure is defined as the percentage of female adolescents aged 13 years who had 3 doses of HPV vaccine by their 13th birthday (NQF #1959) (18).

The reports in this supplement provide the public and stakeholders responsible for infant, child, and adolescent health (including public health practitioners, parents or guardians and their employers, health plans, health professionals, schools, child care facilities, community groups, and voluntary associations) with easily understood and transparent information about the use of selected clinical preventive services that can improve the health of infants, children, and adolescents. The topic in this report is one of 11 topics selected on the basis of existing evidence-based clinical practice recommendations or guidelines for the preventive services and availability of data system(s) for monitoring (19). Through primary prevention, increased HPV vaccine use among adolescents (measured by vaccine coverage) has the potential to diminish the substantial health and economic burdens caused by HPV-associated diseases, including cancers. This report analyzes 2011 data from the National Immunization Survey–Teen (NIS-Teen) to estimate the proportion, by sex, of adolescents aged 13–17 years who received HPV vaccination as recommended by ACIP. Public health authorities and clinicians can use these data to promote evidence-based strategies to increase HPV vaccination coverage among adolescents consistent with national recommendations and to protect adolescents against vaccine-preventable HPV-associated diseases, including cancers.

Methods

To attain national estimates of the proportions, by sex, of adolescents who had received ≥1 dose and ≥3 doses of HPV vaccine consistent with evolving ACIP recommendations, CDC analyzed 2011 data from NIS-Teen. For this report, 2011 data were chosen as a baseline because information collection occurred after the December 2010 FDA licensure of HPV4 for an anal cancer prevention indication that included both sexes (and thus which theoretically might have influenced HPV4 coverage). Because most 2011 NIS-Teen data were collected before ACIP recommended routine male HPV4 vaccination in October 2011 (10), findings represent baseline data for monitoring that recommendation's implementation.

The 2011 NIS-Teen employed a random-digit–dialed sample of landline and cellular telephone numbers (20) to collect immunization information for adolescents aged 13–17 years residing in the 50 states, the District of Columbia, and other selected areas (21). Respondents who were parents or guardians of adolescents aged 13–17 years provided information regarding their adolescents' immunization histories, health-care use, health insurance coverage, and sociodemographics. After respondents had given their consents, questionnaires were mailed to all identified health-care providers to obtain vaccination history data from medical records, so that composite validated immunization histories could be analyzed (21). Details regarding NIS-Teen methodology, including immunization history development and weighting methods, have been described previously (22,23).

A total of 23,564 adolescents with provider-verified vaccination records were included in this report, of whom 11,236 (47.7%) were female. Of this total, data were obtained for 20,848 adolescents from completed interviews from landline sampling and for 2,716 adolescents from cellular-telephone sampling (21). The Council of American Survey Research Organizations (CASRO) landline and cellular-telephone response rates were 57.2% and 22.4%, respectively.¶ Results are stratified by age, sex, and sociodemographic variables. Reported household incomes and numbers of persons living/staying in surveyed households were employed with 2010 Census poverty thresholds to determine income-to-poverty ratios (21,22). Vaccine financing categories included 1) entitled to the federal Vaccines for Children (VFC) program on the basis of being age <19 years and meeting at least one of the three following criteria: Medicaid eligible, American Indian/Alaska Native (AI/AN) descent, or underinsured and vaccinated at a federally qualified health center (FQHC) or rural health center (RHC);** 2) VFC-entitled because of being aged <19 years and uninsured; 3) privately insured (either fully insured or underinsured, but not vaccinated at either an FQHC or RHC); 4) Children's Health Insurance Program (CHIP); 5) military health care or insurance; and 6) other.

Among all adolescents with provider-reported vaccination records, CDC assessed ≥1 and ≥3 dose coverage by including vaccinations received by household interview date. To assess 3-dose series completion rates among those who received ≥1 dose and had sufficient time to complete the series, CDC identified the percentage of females and males who had received ≥3 doses among those who had received ≥1 HPV dose and had at least 24 weeks between first dose receipt and interview date. Among males, sample sizes limited analyses regarding receipt of ≥3 doses and completion status.

To account for the survey's complex sampling design, CDC analyzed data using SAS-callable SUDAAN 9.2 (Research Triangle Institute, Research Triangle Park, North Carolina). CDC employed t-tests to assess vaccination coverage differences and a weighted linear regression to assess coverage trends among females. Estimates with confidence interval (CI) widths exceeding 20 percentage points might not be reliable. Estimates were not reported if an unweighted sample size for a denominator was <30 or if the 95% CI half-width divided by the estimate was >0.6. Results were considered statistically significant at p<0.05.

Results

Sociodemographic and other characteristics of sampled adolescents are provided (Table 1). Overall, among males aged 13–17 years, 8.3% had received ≥1 dose, and 1.3% had received ≥3 doses (Table 2). Among females aged 13–17 years, 53.0% had received ≥1 HPV vaccine dose, and 34.8% had received ≥3 doses (Table 2). Coverage among females increased by an average of 5 to 6 percentage points per year of age for both ≥1 dose and ≥3 doses (p<0.01). Among females aged 13–15 years, for whom Healthy People 2020 coverage targets are specified, 30.0% (95% CI = 28.0–32.1) received ≥3 doses. HPV series completion among those who had ≥1 HPV dose and at least 24 weeks between first dose receipt and interview date was documented among 70.7% of females (Table 3) and 28.1% (95% CI = 22.0–35.0) of males.

Vaccination coverage patterns varied by racial/ethnic group, poverty status, and other sociodemographic variables depending on whether receipt of ≥1 dose, ≥3 doses, or series completion was assessed (Table 3). For both sexes, receipt of ≥1 dose was significantly higher among Hispanics and non-Hispanic blacks compared with non-Hispanic whites. Among females, receipt of ≥3 doses was higher among Hispanics compared with non-Hispanic whites (Table 3). Series completion was lower among black females compared with white females. For both sexes, coverage for ≥1 dose was higher among persons living in households in the lowest income-to-poverty ratio group compared with those living in households in the highest income-to-poverty ratio group. Series completion rates among females increased as income-to-poverty ratios increased. Compared with adolescents living in central city areas, ≥1 dose coverage for both sexes was lower among adolescents living in other areas. Although lower coverage for ≥3 doses was observed among females living outside a Metropolitan Statistical Area, completion rates did not differ by area. Compared with adolescents having mothers who did not complete high school, lower coverage for ≥1 dose was observed for males and females having mothers with a high school or college education. In contrast, series completion among females having mothers with college educations was approximately 15 percentage points higher compared with females having mothers who did not complete high school. For both sexes, coverage for ≥1 dose was higher among those with mothers aged ≤34 years compared with adolescents having mothers aged ≥45 years; however, ≥3-dose coverage among females was lower among those with younger mothers. Series completion rates among females increased as mother's age increased (Table 3).

Among males and females, VFC entitlement because of Medicaid eligibility, AI/AN descent, or being underinsured (and vaccinated at either an FQHC or RHC) was associated with higher coverage for ≥1 dose compared with privately insured, non-VFC–entitled adolescents (Table 3). Among females, the magnitude of the difference between these groups dropped from a 15 percentage point difference for ≥1 dose to a 4.6 percentage point difference for ≥3 doses. Series completion rates were higher among privately insured females. Similar patterns were evident when CHIP and private insurance estimates were compared. For ≥1 dose coverage among females, there was no statistically significant difference between those who were privately insured and those who were VFC entitled and uninsured; however, for ≥3 dose coverage among females, 34.1% of privately insured adolescent females were vaccinated compared with only 20.3% (p<0.05) of VFC-entitled uninsured.

More than 70% of males and females with history of having had ≥1 dose received their initial HPV doses in pediatric settings (Table 1). Among female adolescents for whom HPV4 was licensed and available when they were aged 11–12 years, coverage for ≥1 dose and ≥3 doses as well as series completion were higher for those who had a provider-reported 11–12 year preventive visit (Table 3). For receipt of ≥1 dose among both sexes and ≥3 doses among females, higher coverage rates were observed among adolescents whose parents reported having received providers' vaccination recommendations (Table 3).

Discussion

The results of this survey, which was conducted approximately 5 years after HPV4 was licensed in 2006 for use in females, demonstrate that approximately half of females aged 13–17 years sampled in 2011 had not yet received the recommended first HPV vaccine dose, and nearly two thirds had not received the ≥3 doses required for series completion. Among females who initiated the series, approximately 30% still needed to complete it. Among males, 2011 coverage estimates primarily reflect 2009 licensure and policy (i.e., HPV4's initial licensure for males and ACIP's guidance that HPV4 could be administered to males aged 9–26 years); these 2011 data provide a baseline for monitoring implementation of the October 2011 routine HPV4 vaccination recommendation for males.

At only 30.0%, coverage among females aged 13–15 years is substantially below the Healthy People 2020 target of 80% coverage for ≥3 HPV vaccine doses. In contrast, in 2011, coverage estimates among all adolescents aged 13–15 years for ≥1 dose Tdap and ≥1 dose MenACWY were 80.5% and 71.5%, respectively (21), demonstrating achievement of the Healthy People 2020 target for Tdap coverage and highlighting that 80% vaccination coverage is attainable among adolescents. These findings also indicate that opportunities are being missed to deliver HPV vaccine with other routinely recommended vaccines.

With some fluctuation, analyses of 2008–2010 NIS-Teen data (24–27) have shown higher HPV vaccination series initiation rates among adolescent females who were black, Hispanic, or living below poverty, yet lower rates for series completion among these groups. In 2011, although receipt of ≥1 dose was significantly higher among black and Hispanic adolescents compared with whites, series completion among females was significantly lower among blacks than whites. In addition, receipt of ≥1 dose was significantly higher among adolescents with household incomes <133% of the federal poverty level (FPL) compared with those having household incomes ≥503% of FPL, while series completion among females was significantly lower among those with household incomes <133% of FPL compared with those having household incomes ≥503% of FPL. The observation of higher vaccination coverage for ≥1 HPV vaccine dose among adolescents living in poverty might be related to the effectiveness of the VFC program in facilitating vaccination of these adolescents consistent with ACIP recommendations. However, the availability of vaccines at no cost to families for vaccines through the VFC program might not be sufficient to transcend other barriers to vaccination. This might account for findings related to series completion. Higher series completion among females in those having household incomes ≥503% of FPL might suggest that these adolescents' families have resources to transcend barriers to completing the 3-dose series that persons with household incomes <133% of FPL might not. For example, adolescents belonging to higher income households might have better access to transportation compared with adolescents with household incomes <133% of FPL. Understanding these barriers is important to achieving the increased HPV vaccination series completion rates that are needed, especially among groups with higher cervical cancer rates (28).

To increase use of universally recommended vaccinations, CDC's Community Guide to Preventive Services includes a systematic review of evidence available to support implementation of specific interventions (29). As examples, the Guide suggests that improved vaccination rates can be achieved by decreasing client out-of-pocket costs (e.g., through providing insurance coverage) (30). Immunization providers also can reduce clients' out-of-pocket costs by participating in the VFC program, which is administered by CDC in partnership with federal immunization awardees and enrolled VFC immunization providers. By supplying vaccines at no purchase cost through enrolled VFC immunization providers, the VFC program helps families of children who might not have other means of accessing vaccines (31). Whereas some Guide recommendations, including reducing out-of-pocket costs, have strong evidence of effectiveness among children, adolescents, and adults, evidence bases available for development of some Guide recommendations have not included adolescent vaccination studies consistently. However, more data pertaining directly to adolescent vaccination are accruing. Examples include recently published findings demonstrating reminder/recall effectiveness among adolescents in Denver private practices and school-based health centers (SBHCs) (32,33).

Published studies consistently indicate that HPV vaccination of girls aged 12 years in the United States is cost-effective (34,35). However, existing literature reveals less agreement regarding the cost-effectiveness of HPV vaccination of boys. Most models suggest that male HPV vaccination might be cost-effective, particularly if coverage among females is low and if analyses include all potential vaccination health benefits (34,35). Evidence substantiating HPV vaccination's effectiveness is becoming available in other countries (36,37) and domestically, especially for early outcomes (e.g., HPV type prevalence and genital warts).

Ongoing changes in the U.S. health-care system offer opportunities to improve the use of clinical preventive services among infants, children, and adolescents. The Patient Protection and Affordable Care Act of 2010 (as amended by the Health Care and Education Reconciliation Act of 2010 and referred to collectively as the Affordable Care Act [ACA]) expands insurance coverage, consumer protections, and access to care, and places a greater emphasis on prevention (38). As of September 23, 2010, ACA § 1001 requires nongrandfathered private health plans to cover, with no cost-sharing, a collection of four types of clinical preventive services, including 1) recommended services of the U.S. Preventive Services Task Force graded A (strongly recommended) or B (recommended) (39); 2) vaccinations recommended by ACIP (40); 3) services adopted for infants, children, and adolescents under the Bright Futures guidelines supported by the Health Resources and Services Administration (HRSA) and the American Academy of Pediatrics (41) and those developed by the Discretionary Advisory Committee on Heritable Disorders in Newborns and Children (42); and 4) women's preventive services as provided in comprehensive guidelines supported by HRSA (43). ACIP recommends routine HPV vaccination for all children aged 11–12 years; recommendations for persons who have not initiated or completed the vaccine series vary by sex but can extend through age 26 years (10,13). Per ACIP recommendations and ACIP-approved VFC resolutions, state Medicaid programs cover HPV vaccination as part of the Early and Periodic Screening, Diagnostic and Treatment benefit (44).

The Health Insurance Marketplace (or Health Insurance Exchange) began providing access to private health insurance for small employers and to persons and families interested in exploring their options for coverage, with policies taking effect as early as January 2014.†† Federal tax credits are available on a sliding scale to assist those living at 100%–400% of FPL who purchase health insurance through the Marketplace (ACA § 1401). Insurance plans sold on the Marketplace must cover the four types of recommended clinical preventive services without cost-sharing, including HPV vaccination for ACIP-recommended groups.

ACA contains additional provisions that might promote administration and acceptance of HPV vaccine and other vaccines recommended for adolescents. ACA § 10503 expands access to primary care by establishing a new mandatory fund for community health centers (CHCs), which provide health-care services to uninsured and underserved populations. This funding might help increase access to vaccination at CHCs by underinsured children who are eligible to receive VFC-purchased vaccines in those settings. Also, in 2011, through ACA § 4101, approximately $95 million in federal grants to establish 278 SBHCs became available (45). Although this funding expands SBHCs from a baseline of only approximately 2,000 nationally, this increase might be important for vulnerable populations, including low-income and uninsured adolescents (46), who might not have "medical homes."

Although ACA promises to expand access to vaccination services for many persons, including the uninsured, immunization stakeholders will need to collaborate to promote public and provider awareness of new and existing policies and programs that promote immunization consistent with ACIP recommendations. Furthermore, it is important for immunization providers to understand the importance of strongly recommending HPV vaccination and of providing vaccines, including HPV vaccine, at every opportunity in the absence of a clinical contraindication (47,48).

Limitations

The findings in this report are subject to at least three limitations. First, response rates were low. The cellular telephone household response rate was only 22.4%, and the landline household response rate was 57.2%. Only 54.6% (cellular telephones) and 61.5% (landline) of those with completed household interviews also had adequate provider data. Analyses included only adolescents whose providers submitted sufficient vaccination information for vaccination status determination. After weighting adjustments, nonresponse and noncoverage bias might have remained. Increases in coverage estimates of approximately 3 percentage points for Tdap, 2 percentage points for MenACWY, and 6 percentage points among females for HPV vaccination initiation might have resulted, on the basis of a total survey error model with comparison to provider-reported data obtained from a sample of National Health Interview Survey participants. Estimates of bias do not include vaccination status errors (e.g., underascertainment from incomplete vaccination provider identification and unknown medical record completeness) and do not address potential differential noncoverage or nonresponse bias over time (49). Second, weighted linear regression analyses did not account for methodologic changes in sampling frames. Although vaccination estimates from landline only (2006–2010) and dual sampling frames (2011–2012) might not be comparable, prior methodologic assessment suggests that the addition of cellular telephone numbers beginning in 2011 should have had limited effects on annual national coverage estimates (20). Finally, estimates for racial/ethnic populations with sample sizes <1,000 might be unreliable. For HPV coverage analyses by sex, small sample sizes decrease the power to detect differences (50).

Conclusion

HPV vaccination has the potential to decrease substantial health and economic burdens caused by HPV-associated diseases, including cancers. At only 30.0% in 2011, coverage among females aged 13–15 years is far short of the Healthy People 2020 target of 80% coverage for ≥3 HPV vaccine doses. If health-care reform implementation expands adolescents' access to primary care and vaccination services, it could facilitate achievement of national vaccination coverage goals and, ultimately, reduce the substantial burden of HPV-associated diseases and cancers in the U.S. population.

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