Pediatric Infectious Disease Journal:
Factors Associated With Receipt of Two Doses of Varicella Vaccine Among Adolescents in the United States
Kawai, Kosuke ScD*; O’Brien, Megan A. PhD, MPH†; Conway, James H. MD, FAAP‡; Marshall, Gary S. MD§; Kuter, Barbara J. PhD, MPH†
From the *School of Pharmacy, Temple University, Philadelphia; †Merck, West Point, PA; ‡Department of Pediatrics, Division of Pediatric Infectious Disease, School of Medicine and Public Health, University of Wisconsin, Madison, WI; and §Division of Pediatric Infectious Diseases, University of Louisville School of Medicine, Louisville, KY.
Accepted for publication November 27, 2012.
K.K., M.A.O., J.H.C., G.S.M. and B.J.K. are responsible for the work described in this article. All authors were involved in at least one of the following: conception; design; acquisition; analysis; statistical analysis; interpretation of data and drafting the article or revising the article for important intellectual content. All authors provided final approval of the version to be published. M.A.O. and B.J.K. are employees of Merck Sharp & Dohme, a subsidiary of Merck, and own stock in the Company. K.K. is a postdoctoral fellow funded by Merck. G.S.M. has been a principal investigator on research contracts from GlaxoSmithKline, Merck, Novartis and Sanofi-Pasteur, and has received honoraria from those companies as well as Pfizer for service as a consultant. J.H.C. has been a principal investigator on research contracts from Sanofi-Pasteur, has received program support from the Merck Foundation and has received honoraria for scientific advising from Merck and Novartis. The findings and conclusions in this article are those of the authors and not necessarily of the National Center for Health Statistics. The authors have no other funding or conflicts of interest to disclose.
Address for correspondence: Kosuke Kawai, ScD, Temple University, School of Pharmacy, 3307 N. Broad Street, Philadelphia, PA 19140. E-mail: firstname.lastname@example.org.
Background: In 2006, routine two-dose varicella vaccination for all children was recommended, including a second dose catch-up program for older children and adolescents. Recent studies have shown that a second dose of the vaccine provides incremental protection against varicella disease.
Methods: This study is a cross-sectional analysis of data collected in the National Immunization Survey–Teen 2010 combined with publicly available data related to state immunization requirements. Bivariate and multivariable logistic regression analyses were performed to examine individual-level and state-level factors associated with receipt of two doses of varicella vaccine among 10,542 adolescents 13 to 17 years of age with no history of varicella.
Results: Overall, 58.1% of adolescents without any history of varicella had received two doses of varicella vaccine. Coverage varied widely among states, ranging from 19.7% in South Dakota to 85.3% in Rhode Island. In the multivariable model, receipt of two doses of varicella vaccine was significantly associated with younger age, higher maternal education level, private health insurance, more frequent health care visits, receipt of both quadrivalent meningococcal conjugate and tetanus, diphtheria, and acellular pertussis vaccinations, and residing in a state with two-dose policies for middle school entry. Vaccines for Children program–eligible adolescents were less likely to have received two doses.
Conclusion: Two-dose varicella vaccination coverage remained low among adolescents in 2010, despite the universal recommendation. Programs that are aimed specifically at Vaccines for Children program–eligible adolescents, state policies requiring two doses for middle school entry, and broad education and implementation of the adolescent vaccination platform may help to improve varicella vaccination coverage.
In the prevaccine era, varicella was universal in childhood and frequently was complicated by secondary bacterial infection, pneumonia, encephalitis, and even death.1 In 1996, 1 year after the varicella vaccine was licensed, the Advisory Committee on Immunization Practices recommended one dose for all children 12 months to 12 years of age.1 Subsequently, varicella morbidity decreased by 80% to 85% and mortality attributable to varicella declined by 88%.2,3 However, outbreaks in daycare centers and schools continued to occur.2,4,5 In 2006, the recommendation was updated to include administration of two doses of the vaccine to all children 4 to 6 years of age and catch-up vaccination for older children and adolescents.6,7 Recent studies have shown that two doses of the vaccine provide incremental protection against varicella disease.8–10
Many challenges remain in achieving high completion rates for two doses of varicella vaccine, especially among adolescents. Two-dose vaccination coverage among adolescents in 2010 was relatively low (58%).11 Numerous studies have found that receipt of the first dose of varicella vaccine, as well as receipt of routine adolescent vaccines (quadrivalent meningococcal conjugate [MCV4]; tetanus, diphtheria, and acellular pertussis [Tdap]; and hepatitis B vaccines), may be influenced by socioeconomic factors, vaccine financing systems, and state school entry requirements.12–18 However, no study has examined factors associated with receipt of two doses of varicella vaccine at a national level. The objective of this study was to examine individual-level and state-level factors associated with receipt of two doses of varicella vaccine among adolescents 13 to 17 years of age.
National Immunization Survey (NIS)–Teen is an annual survey conducted by the Centers for Disease Control and Prevention to estimate routine vaccine coverage among adolescents 13 to 17 years of age residing in each of the 50 states and the District of Columbia.11,19 The survey is conducted by telephone through random digit dialing of households; parents or guardians of adolescents 13 to 17 years of age who are knowledgeable about the immunization status of their teens are asked to participate, appropriately consented, and interviewed. The NIS-Teen 2010 survey was approved by the Institutional Review Board of the Centers for Disease Control and Prevention. With the consent of the parent or guardian, surveys are mailed to all vaccination providers to obtain immunization records. The vaccination coverage estimates in the NIS-Teen are based on provider-verified responses. The household response rate for the 2010 NIS-Teen was 58.0%. Among those who completed the household survey, 59.2% had provider-verified vaccination records. A total of 19,257 adolescents were included in the national estimates for the 2010 NIS-Teen report. Of these, 10,452 (54.8%) did not have a personal history of varicella and were included in this analysis.
The outcome of interest in this study was the provider-verified receipt of two doses of varicella vaccine (reported in the NIS-Teen 2010 as having received two or more doses) among adolescents without any history of varicella. The following individual-level factors were considered as potential correlates of receipt of two doses of varicella vaccine: age at time of survey; gender; race/ethnicity; maternal marital status; maternal education level; household income; insurance status; eligibility for the Vaccines for Children (VFC) program (a federal entitlement that provides vaccine at no cost for eligible children); health care provider facility type; number of health care visits in the previous year; health care provider reporting to an immunization registry; and receipt of both one dose or more of MCV4 and one dose or more of Tdap. The household income and family size also were assessed to define poverty level. Poverty status was based on the reported household income and the federal poverty threshold, which is defined according to the family size and the number of children younger than 18 years of age.
State-level factors considered in this analysis included the number of pediatricians per 100,000 children in the respondent’s state of residence20 and state policies requiring two doses of varicella vaccine for middle school entry (Table 1).21 State-level school entry requirements for MCV4 and Tdap also were examined because these policies may provide opportunities for physicians to recommend and administer other vaccinations. Data regarding middle school vaccine requirements were obtained from the Immunization Action Coalition.21
Two-dose varicella vaccine coverage rates were analyzed by individual-level and state-level characteristics. For all analyses, sampling weights (using the proc survey means procedure) were incorporated to account for nonresolution of a telephone number, nonresponse or refusal by interviewees, inability to obtain provider-reported vaccination data, and households without landline telephones.19,22 Logistic regression models (using the proc survey logistic procedure) were used to examine factors associated with receipt of two doses of varicella vaccine in bivariate and multivariable analyses. The backward elimination procedure was used to build the multivariable model. All independent variables significant at P<0.20 in the bivariate analysis were initially included in the multivariable model. The variables with the highest P value and nonsignificance (>0.05) were subsequently removed one-by-one from the multivariable model. Variables with P<0.05 as well as gender and race were forced into the final model. For variables with missing responses, we used a missing indicator method to build multivariable model.23 All analyses were conducted using SAS version 9.2 (SAS Institute, Cary, NC).
Among the 10,542 adolescents, 90.5% received at least one dose and 58.1% received two doses of varicella vaccine. Two-dose vaccination coverage varied widely among states, ranging from 19.7% in South Dakota to 85.3% in Rhode Island. The coverage rate for two doses of varicella vaccine differed by age, household income status, maternal education level, insurance status, health care provider facility type, and frequency of health care visits, but the coverage did not differ by gender and race (Table 2). Coverage among VFC-eligible adolescents (54.2% for Medicaid, underinsured, or others; 45.4% for uninsured) was lower compared with non-VFC-eligible adolescents with private insurance (62.5%) or public insurance (58.4%). Vaccination coverage was significantly higher among adolescents who received both MCV4 and Tdap vaccines compared with adolescents who received neither of those or only one of them (76.0% versus 34.6%). Coverage also differed significantly based on the timing of the implementation of two-dose policies for middle school entry (76.1% for states with policies implemented in 2007 or 2008, 64.1% for states with policies implemented in 2009 or 2010, and 54.5% for states without any policy).
In the multivariable regression model, receipt of two doses of varicella vaccine was significantly associated with younger age at time of survey, higher maternal education, insured adolescents not eligible for the VFC program, more frequent health care visits, receipt of both MCV4 and Tdap vaccinations, and residing in a state with legislation requiring two doses of varicella vaccine for middle school entry (Table 2). Of these variables, receipt of both MCV4 and Tdap vaccines and middle school vaccine requirements were most strongly associated with receipt of two doses of varicella vaccine. Adolescents who had received both MCV4 and Tdap vaccines were more likely to have received two doses of varicella vaccine compared with those who had not (adjusted odds ratio [OR], 5.84; 95% confidence interval [CI], 5.01–6.82). Adolescents who resided in states that had two-dose policies in place for ≥2 years were more likely to receive their second dose compared with those residing in states that had no such policies (adjusted OR, 3.32; 95% CI, 2.45–4.49 for states implemented in 2007 or 2008).
Household income level, vaccine provider facility type, or residing in a state with legislation requiring meningococcal vaccination for school entry were associated with receipt of two doses of varicella vaccine in the bivariate analysis. However, none of these factors remained statistically significant in the multivariable model, and thus they were not included in the final model. Vaccination coverage did not differ by other state-level factors, such as number of pediatricians per 100,000 children in state of residence, in the bivariate analysis.
Although the Advisory Committee on Immunization Practices recommended a routine two-dose varicella vaccine schedule in 2006, two-dose vaccination coverage was still relatively low (58%) among adolescents without a personal history of varicella. Recent studies have shown that two doses of the vaccine provide incremental protection against varicella disease.8–10 Importantly, this analysis shows that the receipt of two doses of varicella vaccine was strongly associated with more frequent health care visits, receipt of both MCV4 and Tdap vaccines, and state policies requiring varicella immunization before middle school entry.
Two-dose varicella vaccination coverage rates in the survey steadily increased over time (19% in 2007, 34% in 2008, 49% in 2009, and 58% in 2010).11,24,25 However, coverage rates remained far below the Healthy People 2020 target of 90%, a national goal for health promotion and disease prevention, and was less than coverage rates for the adolescent vaccines recommended in 2005 (69% for Tdap and 63% for MCV4 in 2010).11,26 A recent study in California also showed gradual increase in the uptake of a second dose of the varicella vaccine, but coverage rates remained relatively low among adolescents.27
When compared with older teenagers (16 or 17 years of age), younger adolescents (13 or 14 years of age) had higher two-dose vaccine coverage. The rates for older adolescents may have been lower than the rates for younger adolescents for a number of reasons, such as less access to preventive services or fewer opportunities to receive a second dose because of their age at the time the second dose recommendation was initiated. The Centers for Disease Control and Prevention as well as other professional societies have recommended a comprehensive health services visit at 11 or 12 years of age, which should include administration of all recommended and catch-up vaccinations. The older adolescents (16 and 17 years of age) would have been 12 and 13 in 2006 when the two-dose recommendation was made, so they may have missed the most significant opportunity to receive a second dose of varicella vaccine. Another potential reason for the difference in coverage may be that both parents and providers may have different perceptions of varicella infection risk in younger and older adolescents. Whereas health care professionals recognize that varicella is more serious with increasing age, parents of older children may view varicella as a childhood disease and may believe that older children are no longer at risk; therefore, parents may believe the older children do not need the additional benefit of a second dose of vaccine.
Previous research has shown that major barriers to adolescent immunization include factors related to health care access, such as infrequent preventive visits to physicians, vaccine financing, and limitations in delivery systems.13,14,28 Consistent with these previous findings, this study found that frequency of health care visits was positively associated with receipt of two doses of varicella vaccine. It is not possible to determine in this analysis why certain adolescents have more frequent health care visits and how this may impact vaccination, because some adolescents with chronic health conditions may require frequent health care visits. The most straightforward interpretation of this finding would be to assume that more frequent health care visits provide more opportunities for vaccination. Alternate explanations for this association are that frequent health care visits may be associated with either more health-seeking behaviors or more positive relationships with health care providers, either of which may result in a greater likelihood to request immunizations or accept immunizations when offered.
VFC-eligible adolescents were less likely to have received two doses of varicella vaccine compared with non-VFC-eligible adolescents who were covered by private health insurance. Similarly, in a previous study, coverage with Tdap and MCV4 among VFC-eligible adolescents was lower compared with non-VFC-eligible adolescents.29 Lower coverage among VFC-eligible adolescents may be attributable to lack of awareness of their eligibility, lack of access to primary care in general, or differences in the quality of health care received. Adolescents with no health insurance may have particularly lower frequency of health care visits compared with adolescents with insurance of any type. These findings indicate that there are still significant barriers to accessing vaccines among VFC-eligible adolescents, even when financial barriers to vaccination are reduced, as through VFC funding.
The third access-related variable that was found to be strongly associated with receipt of two doses of varicella was receipt of Tdap and MCV4. This finding may suggest that certain health care providers may make stronger recommendations for all adolescent vaccines than other providers, including, in this case, catch-up varicella immunization. Although the NIS-Teen survey does not include data related to why adolescents did or did not receive two doses of varicella, the survey does ask parents to provide reasons why their child had not received Tdap or MCV4. Almost 90% of parents of adolescents who did not receive Tdap or MCV4 reported not receiving recommendations for either of these vaccines from their health care provider.30 A previous study also reported lack of provider recommendation as the most common reason for not receiving Tdap and MCV4.30 It is possible, given the strong association between receipt of two doses of varicella vaccine and receipt of Tdap and MCV4, that the reasons for not receiving all of these vaccines are similar.
In addition to increasing health care visits and strong health care provider recommendations, communication between providers, adolescents, and their parents about the benefits and potential risks associated with vaccines may be essential to improve vaccine coverage rates.31,32 Moreover, to address concerns about vaccination, a health care provider may need to focus on developing trusting relationships with adolescents and their parents and on providing reliable, scientific information about vaccines.32
The only state-level variable found to be associated with two-dose varicella vaccination coverage was the existence of middle school varicella vaccine requirements. States that had two-dose policies in place for at least 2 years had substantially higher vaccine coverage compared with states that had no such policies (76.1% versus 54.5% in unadjusted analysis). As of 2010, only 17 of the 50 states and the District of Columbia required two doses of varicella vaccine for entry into middle school.21 Although the cross-sectional nature of this study precludes us from knowing whether adolescents may have been vaccinated before state policy implementation, the findings are consistent with previous studies showing the importance of school requirements for receipt of a first dose of varicella vaccine and other vaccines in improving coverage rates.15–18,33 It is also important to note that middle school vaccination requirements typically apply to adolescents 11 to 14 years of age. Because the NIS-Teen survey also includes older adolescents, the results may underestimate the overall impact of state policies.
This study has several limitations. Although we adjusted for most factors that may influence vaccine uptake, unmeasured factors, such as variations in vaccine financing systems across states, may confound the observed associations. Also, factors found to be associated with two-dose coverage in the NIS-Teen survey may serve as proxies for unmeasured underlying factors. States with middle school entry requirements also may have stronger public health systems, financing mechanisms, and provider recognition of the importance of immunization. Another issue that may underestimate the true impact of two-dose recommendations in this analysis is the fact that there may be a lag between the time that a state law is enacted and when it is enforced. Some states may allow for longer implementation periods than others, which may affect the impact of the requirements on coverage rates. To address this issue, two time periods were defined in this analysis to capture the impact of requirements that have been in place for longer periods of time compared with more recent requirements. The cross-sectional analysis of the survey precluded our ability to determine the temporality of the associations. Although we incorporated sampling weights to adjust for nonresponse and noncoverage, bias still may have occurred from nonresponse.22 Vaccination coverage may have been underestimated because of incomplete vaccination records of providers. Finally, because the NIS-Teen is a random digit sampling survey of landline households, results may not be representative of the general United States population.
In conclusion, two-dose varicella vaccine coverage remained relatively low among adolescents in the United States. Programs aiming at VFC-eligible adolescents, strong provider recommendations, state policies requiring two doses for middle school entry, and broad education and implementation of the adolescent immunization platform may improve varicella vaccine coverage.
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varicella vaccination; National Immunization Survey–Teen; adolescents
© 2013 Lippincott Williams & Wilkins, Inc.
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