PEDIATRICS Vol. 110 No. 5 November 2002, pp. 929-934
Hepatitis B Vaccination Among Adolescents in 3 Large Health Maintenance Organizations
* Epidemiology Program Office, assigned to the National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia
National Immunization Program, Centers for Disease Control and Prevention, Atlanta, Georgia
Center for Health Research, Kaiser Permanente Northwest, Portland, Oregon
|| Center for Health Studies, Group Health Cooperative of Puget Sound, Seattle, Washington
¶ Division of Research, Kaiser Permanente of Northern California, Oakland, California
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ABSTRACT |
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Objective. In 1995, the Advisory Committee on Immunization Practices (ACIP) recommended routine hepatitis B (HB) vaccination of all unvaccinated 11- to 12-year-old adolescents. Little is known about the implementation of these recommendations in a managed care setting. The objective of this study was to determine the impact of ACIP recommendations on HB vaccination among adolescents in 3 managed care settings.
Methods. We assessed HB vaccination coverage among adolescents who were enrolled in 3 large health maintenance organizations (HMOs) and who turned 13 years old after the 1995 ACIP recommendations. Children who were 8 to 10 years of age during May 1993 and were continuously enrolled through December 1998 were eligible. We used the HMOs’ computerized immunization tracking system to collect HB vaccination dates. The percentage of adolescents who received 3 doses of HB vaccine was determined.
Results. In HMOs A, B, and C, coverage levels for 3 doses of HB vaccine were 43.4%, 65.5%, and 25.7%, respectively, among 13-year-olds in 1998 compared with 26.1%, 50.4%, and 5.5% among 13-year-olds in 1996. Between the ages of 11 and 13 years, coverage rates among adolescents aged 13 in 1998 rose more than the coverage among adolescents aged 13 in 1996. The proportion of 13-year-olds in 1998 who received the first dose of HB vaccine by December 1998 was much higher at 89.6%, 65.2%, and 56.6% in HMOs A, B, and C, respectively, compared with the proportion who completed the 3-dose series (43.4%, 65.5%, and 25.7%, respectively).
Conclusions. After the 1995 ACIP recommendations, HB vaccination coverage levels among 13-year-olds increased in each of the HMOs, suggesting adherence with national recommendations. Differences among the 3 HMOs may reflect differences in internal policies. More effective strategies may be needed to achieve the Healthy People 2010 goal of 90% vaccination coverage rates among adolescents.
Key Words: hepatitis B vaccine • adolescence • health maintenance organizations • managed care • vaccination • immunization
Abbreviations: HBV, hepatitis B virus • ACIP, Advisory Committee on Immunization Practices • HB, hepatitis B • AAP, American Academy of Pediatrics • VFC, Vaccines for Children • HMO, health maintenance organization • VSD, Vaccine Safety Datalink • CDC, Centers for Disease Control and Prevention
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONRECOMMENDATIONSREFERENCES |
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Prevention of hepatitis B virus (HBV) infection through vaccination of adolescents before they enter adulthood is crucial because young adults have the highest incidence of HBV infection in the United States.1 Once infected, 2% to 6% of older children, adolescents, and adults will develop chronic HBV infections, putting them at increased risk for developing chronic liver disease or, later in life, primary hepatocellular carcinoma.2 In 1982, the Advisory Committee on Immunization Practices (ACIP) recommended hepatitis B (HB) vaccination of individuals who are at high risk for HBV infection.3 This strategy proved unsuccessful in part because such individuals were difficult to reach with vaccine before they became infected and approximately 30% to 40% of adolescents and adults with acute HBV infection have no identifiable risk factors.4 In 1991, the ACIP recommended universal vaccination of infants with the HB vaccine, a strategy to eliminate HBV transmission, and universal vaccination of adolescents who live in communities where injecting drug use, teenage pregnancy, and/or sexually transmitted diseases is common.5 In 1992, the American Academy of Pediatrics (AAP) recommended the implementation of universal vaccination of adolescents where resources permit.6 In 1995, the ACIP expanded its recommendations to include routine HB vaccination of all previously unvaccinated 11- to 12-year-old adolescents7 and in 1997 to all unvaccinated children and adolescents 0 to 18 years of age.8
In the past decade, substantial success has been achieved in universal childhood HB vaccination with coverage rates approaching 90% among children aged 19 to 35 months.9 Available information about adolescent HB vaccination coverage suggests that coverage is substantially lower (<50%)9; however, the data are limited. There may be potential barriers for vaccinating adolescents, including insufficient health care visits; the failure of providers to assess adolescent vaccination status at illness-related visits, resulting in missed opportunities10; financial barriers, such as lack of insurance coverage for adolescent vaccinations10; or adolescents who do not use the health care system. To reduce cost-related barriers, the ACIP in October 1997 made HB vaccine available through the Vaccines for Children (VFC) program for individuals who are 0 to 18 years and eligible for VFC.8 The VFC program is a federal-state partnership that provides public-purchased vaccine to public and private health care providers for children who are 0 to 18 years old and enrolled in Medicaid, American Indians or Alaska Natives, uninsured, or underinsured with respect to vaccinations (more information is available at www.cdc.gov/nip/vfc). In 1999, 30% of the US population was enrolled in managed care organizations, ranging from 23% to 24% in the Midwest and the South to 37% in the Northeast and 41% in the West.11 To understand better adolescent vaccination among this population and the possible impact of the ACIP recommendations, we examined HB vaccination coverage rates among adolescents who were enrolled in 3 large health maintenance organizations (HMOs) on the West Coast, which provided HB vaccine as a covered benefit.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONRECOMMENDATIONSREFERENCES |
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Study Design, Population, and Collection of Data
We used data from 3 HMOs that participate in the Vaccine Safety Datalink (VSD) Project. The VSD project is a collaboration between the Centers for Disease Control and Prevention (CDC) and several large HMOs in the United States. The VSD methodology has been described in detail elsewhere.12 The VSD project began in 1990 with the main purpose of evaluating the safety of vaccines.13 Computerized data on vaccinations, medical outcomes (eg, outpatient visits, emergency department visits, hospitalizations, deaths), and demographic characteristics are collected prospectively and linked under joint protocol at these HMOs for analysis.13 At the time of our study, 3 HMOs that were participating in the VSD project provided data on adolescents.
The study population consisted of adolescents who were 8, 9, and 10 years of age as of December 31, 1993, and who were continuously enrolled in 1 of the 3 HMOs from May 1, 1993 (when adolescent data became available for all 3 HMOs), through December 31, 1998. At the end of our follow-up period, these adolescents were 13, 14, and 15 years of age, respectively. Across the 3 HMOs, the proportion of adolescents who were continuously enrolled during the time of our study ranged from 22.9% to 38.4%. The 3 HMOs varied in size; HMO A had the largest number of continuously enrolled adolescents in each of the 3 age groups as of 1998 (13-year-olds, 20 268; 14-year-olds, 20 754; 15-year-olds, 21 391), followed by HMO B (13-year-olds, 3059; 14-year-olds, 3299; 15-year-olds, 3392) and HMO C (13-year-olds, 2348; 14-year-olds, 2305; 15-year-olds, 2541). Overall, 79 357 adolescents were included in our study.
Outcomes of Interest and Statistical Analysis
We assessed receipt of HB vaccine from May 1993 through December 1998. The principal outcome of interest was the percentage of adolescents who received at least 3 doses of HB vaccine during that time period. We collected information on dates of vaccine administration, date of birth, and gender. Only vaccinations entered into the HMOs’ computerized immunization tracking system were counted. We examined whether there was a change in HB vaccine 3-dose coverage among each cohort of adolescents within each HMO between 1994 (just before implementation of the ACIP recommendations to vaccinate 11- to 12-year-old adolescents) and 1998. We also evaluated whether coverage differed by gender.
We examined the coverage for doses 1, 2, and 3 of HB vaccine to assess the drop-off rates from the first to the third doses. To evaluate the quality of vaccine administration and adherence to ACIP recommendations, we calculated the time intervals between receipt of HB vaccine doses 1, 2, and 3. Dose 2 was administered too early when the interval between doses 1 and 2 was <28 days. Dose 3 was administered too early when the interval between doses 2 and 3 was <61 days and/or when the interval between doses 1 and 3 was <122 days. All frequencies were derived using SAS 6.12 (SAS, Inc, Cary, NC).
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RESULTS |
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An increase in HB vaccine 3-dose coverage was observed for each of the age groups of adolescents in each of the 3 HMOs from 1994 through 1998 (Fig 1). However, there were marked differences among the 3 HMOs in the coverage levels attained. By 1998, HB vaccine 3-dose coverage was highest among adolescents in HMO B: 65.5% among 13-year-olds, 68.6% among 14-year-olds, and 68.1% among 15-year-olds. In HMO A, coverage was 43.4%, 45.8%, and 50.9% among 13-, 14-, and 15-year-olds, respectively. Coverage was lowest in HMO C: 25.7%, 25.2%, and 27.6% among 13-, 14-, and 15-year-olds, respectively. In all 3 HMOs, HB vaccine 3-dose coverage was similar among male and female adolescents (data not presented).
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As Table 1 indicates, the net increase in coverage between age 11 and 13 years increased over time across all 3 HMOs. For example, in HMO A, adolescents who were 11 in 1994 had an increase in coverage of 17.2% between 11 and 13 years of age, whereas those who were 11 in 1995 had an increase in coverage of 20.0%, and those who were 11 in 1996 had an increase in coverage of 24.7%. Despite having the lowest HB vaccine 3-dose coverage rates, HMO C showed the greatest acceleration in vaccination rates. Among adolescents in HMO C who were 11 years old in 1994, HB vaccine 3-dose coverage increased from 0.5% in 1994 to 5.5% in 1996, which is a 5.0% net increase. However, among adolescents in HMO C who were 11 years old in 1996, HB vaccine 3-dose coverage increased from 2.9% in 1996 to 25.7% in 1998, which is a 22.8% net increase in coverage.
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We next looked at the first to third dose completion rates. We noticed a considerable difference between the proportion of 13-year-olds in 1998 who received the first dose of HB vaccine (89.6%, 65.2%, and 56.6% in HMOs A, B, and C, respectively) and the proportion who completed the 3-dose series (65.5%, 43.4%, and 25.7%, respectively) by 1998 (Fig 2). This same trend was also observed for 14- and 15-year-old adolescents in 1998 (data not shown). The difference between the proportion of adolescents who received the first dose and the proportion who completed the 3-dose series was greatest among 15-year-old adolescents in 1998 in HMO C (33.0% difference) and lowest among 14-year-old adolescents in 1998 in HMO B (19.5% difference).
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More than 96% of all doses of HB vaccine were administered in accordance with the recommended minimum time intervals as set by the ACIP.14 Among 13-year-old adolescents in 1998 in HMOs A, B, and C who received 2 doses of HB vaccine, 2% or fewer received their second dose too early, and 3.8% or fewer of those who received 3 doses received their third dose too early (Table 2). Similar results were observed for 14- and 15-year-old adolescents in 1998 in HMOs A, B, and C (Table 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONRECOMMENDATIONSREFERENCES |
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Our findings suggest that adolescent immunization practices in the 3 HMOs in our study improved after the ACIP recommendations in 1995. However, only limited success with HB vaccination was evident as the highest coverage among any of the HMOs assessed was still below 70%, despite that routine vaccinations were a completely covered benefit for the adolescent populations studied. To our knowledge, this is the first published study to examine adolescent HB vaccination among HMO enrollees over a period of several years. As an increasingly larger proportion of the population receives health care from HMOs, the potential role of HMOs in adolescent vaccination is substantial.
Our findings also indicate that there were marked differences in the coverage levels attained by each of the HMOs. These differences may be attributable in part to different policies and strategies used by the 3 HMOs. HMO B, which achieved the highest coverage, implemented the most proactive strategy. At the end of 1994, it implemented an electronic immunization registry, reminding providers on a monthly basis which patients were overdue for immunizations. In 1996, the immunization registry was expanded to allow providers to print a patient-specific immunization letter that indicated which immunizations were due, thus acting as both a provider and a client reminder/recall system. In addition, HMO B sent annual letters to all clients who were turning 11 years of age to remind them to schedule an appointment for vaccinations and a physical examination. In contrast, HMO A implemented a 1-time provider and client reminder/recall notice at the end of 1997. This preventive health prompt printed 2 copies of the patient’s immunization history and needed vaccines at the time of patient check-in. One copy was given to the provider, and the other copy was given to the patient. The preventive health prompt targeted adolescents 11 to 15 years of age. HMO A also sent annual letters to all clients who were turning 11 years of age to remind them of adolescent vaccinations and the need for a physical examination. HMO C did not have similar strategies in place during the time of our study. However, in April 2000, HMO C implemented an electronic weekly immunization list that was sent to providers. This weekly immunization list identifies 12-year-old clients who are overdue for immunizations.
Among all cohorts of adolescents in each of the 3 HMOs, we found that there was a marked drop-off from receipt of the first dose of HB vaccine to completion of the 3-dose series. Our findings are consistent with previous reports. For example, a study of the effectiveness of a seventh-grade school entry HB vaccination requirement in Florida during the 1997/1998 school year showed that 44% fewer third doses of HB vaccine than first doses were administered during 3 school vaccination sessions.15 Another study that assessed compliance of HB vaccination in patients who presented to a teenage medicine practice in California that was part of a prepaid HMO found that although 90% of patients completed the first dose, only 38% and 10% completed the second and third doses, respectively.16 A third study at a hospital-based and school-based adolescent clinic in Boston found that 72% of 896 eligible participants had completed the vaccination series after 26 months despite receiving HB written and oral education, reminder postcards or telephone calls, monetary or movie pass incentives after vaccination, and vaccines provided free of charge.17 In addition, a study conducted in a large hospital-based adolescent clinic in Cincinnati where there was a provider reminder system, participants and parents received HB written and oral education, attempts were made to reschedule missed appointments, and vaccines were offered at a reduced cost reported that 445 (85%) of participants were up-to-date on the vaccine series after 1 year.18
Antibody response to HB vaccination can vary depending on the time interval between vaccinations, with an early third dose resulting in a lower-than-anticipated response.19 Our results showed that the vast majority of vaccinations were administered according to the minimum ACIP recommended vaccination time intervals.
One of the strengths of our study is that we followed adolescents who were continuously enrolled in the HMOs for >5 years, with the HMOs serving as their medical home during that period. The AAP defines the "medical home" as a place where the medical care of infants, children, and adolescents is accessible, continuous, comprehensive, family centered, coordinated, and compassionate.20 It is likely that having a medical home will lead to higher vaccination coverage rates among adolescents by enhancing continuity of care and by reducing record scattering. Another strength of our study is the large size of the adolescent populations that were followed. Furthermore, this study provides us with a unique opportunity to assess and compare HB vaccination coverage rates before and after the implementation of the 1995 ACIP adolescent vaccination recommendations. However, other recommendations made by the ACIP5 and the AAP6 before 1995 may have played a role, too.
A few potential limitations may influence the interpretation of our findings. First, we do not have data on HB vaccinations administered before May 1993. However, because universal HB vaccination of children and adolescents was not a routine practice before the ACIP recommendations, it is unlikely that many of these adolescents received HB vaccine in their childhood. Another limitation is that we may miss vaccinations administered outside the HMO. Because these adolescents were continuously enrolled in these HMOs for >5 years and vaccinations were offered as a covered benefit, the likelihood of vaccinations received outside this setting is low. In addition, we used only administrative data to estimate coverage, which does not take into account vaccines documented in the medical chart but not entered into the computerized system and thus may underestimate coverage. A previous study conducted in these HMOs to assess the quality of the administrative databases between 1991 and 1995 found that the percentage of abstracted paper-based medical records of common childhood vaccinations that were present in the automated source ranged from 82% to 98%.21 A final limitation of our study is that our findings may not be generalizable to other HMOs or other managed care settings because these HMOs collaborate with the CDC in the VSD project and may, therefore, be more likely to adhere to ACIP recommendations and to implement strategies for increasing coverage rates.
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RECOMMENDATIONS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONRECOMMENDATIONSREFERENCES |
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Given our findings of a marked drop-off rate between the first and third doses of HB vaccine, 1 strategy likely to result in more complete protection of adolescents in this setting is the use of the 2-dose HB vaccination schedule approved in 1999 for adolescents 11 to 15 years of age.22 A recent study suggested that this 2-dose HB vaccination schedule for adolescents 11 to 15 years of age was as immunogenic as the 3-dose series.23 In our study, if adolescents had needed only 2 doses to complete their HB vaccine series, then coverage would have been much higher. For example, for the 13-year-old adolescents in 1998 in HMO A, 2-dose coverage was 55.8% compared with 3-dose coverage of 43.4%, 81.5% instead of 65.5% for HMO B, and 42.1% instead of 25.7% for HMO C. However, in our study, the time interval between doses 1 and 2 is shorter (minimum of 1 month after dose 1), compared with the 2-dose HB vaccination scheduled for 11 to 15 years of age (minimum of 4 months after dose 1). Because adolescents average only 1 visit to a health care provider per year, it is crucial to simplify the HB vaccination schedule.24 The National Vaccine Advisory Committee is revising its 1993 Standards for Pediatric Immunization Practices,25 with an increased focus on adolescent immunizations. Furthermore, voluntary school-based vaccination programs have been shown to be highly successful in achieving high HB vaccination coverage rates among adolescents,26–32 and a 2-dose schedule may prove to be easier to implement during the academic school year. However, providers should not be discouraged to start the HB vaccination series even if there is likelihood that the adolescent might not return to complete the series, because high seroconversion rates have been reported after 1 dose.19,33
Another strategy to improve coverage rates among adolescents in these settings may actually involve allowing for longer intervals between doses. The American Medical Association and the AAP recommend a routine preventive annual visit for adolescents through 21 years of age.34,35 The immunogenicity of HB vaccine administered at yearly intervals compared with the 0-, 1-, and 6-month schedule among children and adolescents 5 through 16 years of age has been studied and found to be highly immunogenic.19,36,37 Assessment of vaccination status at each annual preventive health visit in conjunction with a 2-dose schedule would allow for complete protection to be achieved in a 12-month period.
Third, middle school-entry vaccination mandates have proved to be an effective intervention at improving routine adolescent vaccinations.15,38,39 During the time of our study, there were no middle school-entry HB vaccination mandates in states covering these HMOs. The HB vaccination practices were probably more likely to be affected by the ACIP recommendations than by a state mandate. Two of the 3 HMOs were in states that enacted middle school-entry HB vaccination requirements in 1999 and 2000. However, it is difficult to assess how these subsequent requirements might have influenced vaccination coverage by 1998. As more and more states implement and enforce these laws, it is likely that school requirements will contribute substantially toward the attainment of the Healthy People 2010 goal of 90% HB vaccination coverage among adolescents.9
Last, it is important to note that this study describes HB vaccination coverage before 1999; thus, the impact of the recently revised Health Employer Data and Information Set assessments on managed care plans’ performance may not be captured in our study. Because many HMOs have made major efforts to improve further the adolescent HB vaccination coverage rates in the past few years, future evaluations are warranted.
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ACKNOWLEDGMENTS |
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We greatly appreciate Dr Susan Chu for assistance in preparing this report, Dr Edward Brink for helpful comments on the manuscript, and the Vaccine Safety Datalink Team (October 2000): Frank DeStefano MD, MPH; Robert T. Chen, MD, MA; John Glasser, PhD, MPH; Philip H. Rhodes, PhD; Piotr Kramarz, MD; Thomas Verstraeten, MD; David Walker, MPH; and Catherine Okoro (National Immunization Program, Centers for Disease Control and Prevention, Atlanta, GA); Robert S. Thompson, MD; Lisa A. Jackson, MD, MPH; Robert L. Davis, MD, MPH; William E. Barlow, PhD; Kari Bohlke, ScD; Patti Benson, MPH; Barbara Carste, MPH; Jo Ann Habakangas, BA; Christi Hanson, BA; Minqi Jiang, MS; Paula Lee Poy, BA; Darren Malais, BS; Viviana Rebolledo, BS; Wendy Rogers, BA; David Rubanowice, BS; Dennis Sheeran, MS; Onchee Yu, MS; and Ann Zavitkovsky, MPH, MPA (Group Health Cooperative, Seattle, WA); John P. Mullooly, PhD; Julie E. Maher, PhD, MS; Sheila Weinman, PhD; Lois Drew, BA; Jill Mesa; Kim Olson; Heather Houston, RN; Colleen Chun, MD; Steven Gancher, MD; John A. Pearson, MD; Jerry Slepak, MD; Alan Bauck, BS; Teresa Kimes, MS; Joseph Murphy, BA; Nadia Redmond, MSPH; Karen Riedlinger, BS; Roberleigh Schuler, MS; Carol Sullivan; and Gayle Thomas-Monk (Kaiser Permanente Northwest Region, Portland, OR); Steve B. Black, MD; Henry R. Shinefield, MD; Paula Ray, MPH; Edwin Lewis, MPH; Bruce H. Fireman, MA; Joan Schwalbe; Ajit De Silva; and Patti Hallam (Kaiser Permanente of Northern California, Oakland, CA); Joel I. Ward, MD; Connie M. Vadheim, PhD; Hang Lee, PhD; Ken Zangwill, MD; Eileen Eriksen, MPH; Tracy Zhang, MS; Lennifer Lee, MS; Jennie Jing, MA; Nancy Goff; and Jeffrey Perlman, MD (Center for Vaccine Research Harbor-UCLA Medical Center, Torrance, CA); S. Michael Marcy, MD; and Marlene Lugg, DrPH (Southern California Kaiser Permanente, Los Angeles, CA); M. Miles Braun, MD, MPH; Robert P. Wise, MD, MPH; and Robert Ball, MD, MPH (Center for Biologics Evaluation and Research, Food and Drug Administration, Rockville, MD); and Vito Caserta, MD, MPH; and Geoffrey Evans, MD (Division of Vaccine Injury Compensation, Health Resources and Services Administration, Rockville, MD).
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FOOTNOTES |
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Received for publication Feb 12, 2002; Accepted Jun 13, 2002.
Reprint requests to (M.S.M.) National Immunization Program, Centers for Disease Control and Prevention, 1600 Clifton Rd, Mail Stop E-52, Atlanta, GA 30333. E-mail: mmassoudi{at}cdc.gov
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PEDIATRICS (ISSN 1098-4275). ©2002 by the American Academy of Pediatrics
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 P. G. Szilagyi, S. Schaffer, R. Barth, L. P. Shone, S. G. Humiston, S. Ambrose, and F. Averhoff Effect of Telephone Reminder/Recall on Adolescent Immunization and Preventive Visits: Results From a Randomized Clinical Trial Arch Pediatr Adolesc Med, February 1, 2006; 160(2): 157 - 163. [Abstract] [Full Text] [PDF]
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