Practice and Child Characteristics Associated With Influenza Vaccine Uptake in Young Children
OBJECTIVES: The objective of this study was to determine both practice and child characteristics and practice strategies associated with receipt of influenza vaccine in young children during the 2004–2005 influenza season, the first season for the universal influenza vaccination recommendation for all children who are aged 6 to 23 months.
METHODS: Clinical and demographic data from randomly selected children who were aged 6 to 23 months were obtained by chart review from a community-based cohort study in 3 US counties. The proportion of children who were vaccinated by April 5, 2005, in each practice was obtained. For assessment of practice characteristics and strategies, sampled practices received a self-administered practice survey. Practice and child characteristics that predicted complete influenza vaccination were determined by using multinomial logistic regression.
RESULTS: Forty-six (88%) of 52 sampled practices completed the survey and permitted chart reviews. Of 2384 children who were aged 6 to 23 months and were studied, 27% were completely vaccinated. The proportion of children who were completely vaccinated varied widely among practices (0%–71%). Most (87%) practices implemented ≥1 vaccination strategy. Complete influenza vaccination was associated with 3 practice characteristics: suburban location, lower patient volume, and vaccination strategies of evening/weekend vaccine clinics; with child characteristics of younger age, existing high-risk conditions, ≥6 well visits to the practice by 3 years of age, and any practice visit from October through January.
CONCLUSIONS: Modifiable factors that were associated with increased influenza vaccination coverage included October to January practice visits and evening/weekend vaccine clinics.
WHAT'S KNOWN ON THIS SUBJECT:
As pediatric influenza vaccine recommendations have expanded, coverage for young children has increased but remains suboptimal. Several practice strategies are recommended to enhance vaccination, including influenza vaccine clinics, reminder-recall systems, year-round discussions with parents, and standing orders.
WHAT THIS STUDY ADDS:
With this study the authors assessed practice and child characteristics and practice strategies that predicted complete influenza vaccination among children aged 6 to 23 months. It highlights the importance of improving access to influenza vaccine in primary care practices with several strategies.
Although influenza vaccine has been recommended for decades for children with certain high-risk conditions,1 studies have documented the substantial burden of infection in all children.2,–,6 For this reason, the Advisory Committee on Immunization Practices expanded the universal influenza vaccine recommendations to children who are aged 6 to 23 months in 2004–2005,7 to children who are aged 6 to 59 months in 2006–2007,8 and to children who are aged 6 months to 18 years in 2009–2010.9
The administration of influenza vaccine presents unique challenges to health care providers because it requires yearly administration during a relatively short period. Vaccine supply delays and shortages can occur, making it difficult for practices to predict when vaccination campaigns might begin and whether adequate supplies will be available. Because of poor immunogenicity of a single dose of vaccine in young children, 2 doses are required for children who are younger than 9 years and previously have not been completely vaccinated.9 Most studies that evaluated methods to increase vaccination rates in young children were reported before the universal influenza vaccination recommendations for young children.10,–,14 Because the majority of childhood vaccines are administered in primary care settings,15 we sought to determine both practice and child characteristics and practice strategies that were associated with influenza vaccine coverage among children who were aged 6 to 23 months in 2004–2005, the first season that influenza vaccine was universally recommended.
Institutional Review Board
This study was approved by the institutional review board of the Centers for Disease Control and Prevention (CDC) and of each participating institution in the 3 communities.
The CDC-funded New Vaccine Surveillance Network conducted in 2004–2005 a community-based cohort study of influenza vaccination coverage in 3 US counties: Hamilton County, Ohio (Cincinnati); Davidson County, Tennessee (Nashville); and Monroe County, New York (Rochester). This community-based cohort study was designed to estimate influenza vaccine effectiveness in young children during 2 study years.16 Because these data provided a practice-level assessment of influenza vaccination rates, we surveyed the practices to assess their strategies for influenza vaccination delivery. The combined practice-level chart reviews and practice surveys provided the needed information to assess how practice-level strategies were associated with influenza vaccination rates.
We used 2 sampling frameworks from a previous study of influenza vaccine effectiveness to identify the study population (Fig 1). The first involved a random sample of primary care practices in each county (n = 52 practices from the 3 counties) for practice-based assessment of influenza vaccination rates. The second sampling framework involved 9 practices that had participated in the previous study to assess vaccine effectiveness for outpatient visits.16 We used probability proportional to size sampling17 from county practices (ie, more children from larger practices) to select a random sample of the county's population.6 First, we identified the practices by randomly selecting 30 practice clusters with replacement among the pediatric and family medicine practices in each county that provided care for >30 newborns per year and agreed to participate. Then for each cluster, we randomly selected from the patient list generated by that practice 30 county children who were younger than 5 years,18 as necessitated by the original study for which this cohort was created.16 Each participating practice had between 1 and 8 clusters, depending on practice size. The end result was a sample that represented each county.
In addition, we randomly selected 249 additional children from 9 of the same practices for chart review to represent children who were enrolled in their clinic and participating in outpatient influenza surveillance (Fig 1).6 Because we wanted to assess variation among practices and account for clustering within practices in the analysis, we included all randomly selected children whose charts were reviewed from these practices.
A standardized chart review of the randomly selected children was completed by trained research assistants in the summer of 2005. Data collected included birth date, gender, date of both well and sick visits from birth through May 2005, presence of high-risk medical conditions outlined in the Advisory Committee on Immunization Practices influenza vaccine recommendations,7 and dates of documented influenza vaccinations. We determined the age of each child on October 1, 2004, and excluded children who were younger than 6 months on December 31, 2004. Race was not recorded on most charts that we reviewed and hence could not be included. To assess the level of preventive care that each child received, we measured the number of well-child visits from birth to 3 years of age.
Influenza vaccination status was determined by chart review with inclusion of vaccines that were obtained outside the practice, when available. Children who received 1 dose of influenza vaccine in 2004–2005 and had no previous documented doses were considered partially vaccinated. Children were considered completely vaccinated when they received (1) 2 doses of influenza vaccine at least 24 days apart in 2004–2005 or (2) 1 dose of influenza vaccine in 2004–2005 and at least 1 previous dose of influenza vaccine in earlier years, consistent with the 2004–2005 recommendations.7 Children who did not receive any influenza vaccine in 2004–2005 were considered unvaccinated.
A practice survey was created by specialists in pediatrics, infectious diseases, epidemiology, and vaccine delivery at the sites and CDC and on the basis of the conceptual framework proposed by the Task Force for Community Preventive Services. From this framework, we selected relevant factors from the literature and immunization strategies recommended by this task force.10,–,14,19 The survey was pilot-tested in a convenience sample of pediatric providers and their office managers. The self-administered survey included 22 items that concentrated on practice patterns for administering vaccine to children who were aged 6 to 23 months. The survey was mailed in early November 2005 to the office manager of each participating practice with an explanatory letter detailing its purpose; a maximum of 3 reminders were sent to nonresponding practices. Office managers were asked to consult with practice physicians to complete the survey; 1 survey was allotted per practice. The survey included multiple-choice responses with open text field options to characterize the practice demography, the practice's influenza vaccine supply (2004–2005 had only one-half the anticipated vaccine supply),20 the impact of vaccine shortage on vaccine delivery, characteristics of children who were routinely recommended for influenza vaccine in the practice, and strategies that were used to identify and administer influenza vaccine to young children.
The following questions ascertained strategies that were used by the practices: Did you save a second dose of influenza vaccine for previously unvaccinated children? Did your practice use a standing order system for the 2004–2005 influenza vaccine? Did your practice use flu shot clinics? For the last question, affirmative responders were to check all of the applicable times: morning, lunch, afternoon, evening, and weekends. Another question asked when providers usually discussed influenza vaccination with parents. Responses included at well visits during influenza season, at sick visits during influenza season, at visits year-round, or not discussed.
Patient-level characteristics that were obtained from the chart review included age, gender, insurance status (public or private), high-risk medical conditions, health care visits between October and January, dates of well visits from birth to 3 years, and dates of influenza vaccinations. Practice-level characteristics that were obtained from the survey included practice type, residential setting, practice volume, proportion of children who participated in the Vaccines For Children (VFC) program, and the adequacy of the practice's 2004–2005 influenza vaccine supply. Each vaccination strategy was captured. The survey asked about systems to identify vaccine-eligible children and about willingness to vaccinate at all visits; these variables were not analyzed because >90% of practices responded affirmatively to each one. The primary outcome for practice-level analysis was complete influenza vaccination.
χ2 analyses were used to compare characteristics and vaccination status of individual children. The proportion of children who were completely or partially vaccinated in each practice was calculated. For practices, we estimated the median proportion and the 95% confidence intervals of children who were completely vaccinated by practice characteristics and practice strategies. For evaluation of practice and patient characteristics, a multinomial logistic regression analysis accounting for the 3 potential outcomes—complete, partial, or no vaccination—was performed with the child as the unit of analysis, including random effects of site and practices because children within practices were clustered within 3 study sites.
A question in the practice survey stated, “Did your practice use a recall system in 2004–2005?” Responses included no, yes, or an alternative response in space provided. We discovered that some practices interpreted a recall system as personalized mailings or telephone calls for specific children who required vaccine, whereas others interpreted a recall system as generalized electronic or postal mailings about influenza vaccine at the practice (ie, a notice that the vaccine was available). Because this question was understood differently, we excluded recall/reminder systems from analysis. Statistical analyses were performed using Stata 8.1 (Stata Corp, College Station, TX), SAS (SAS Institute Inc, Cary, NC), and R 2.7.2 (R Foundation for Statistical Computing, Available at: www.r-project.org/foundation. Accessed July 28, 2010).
Forty-six (88%) of 52 practices responded to the survey and permitted chart reviews on a total of 2384 children who were aged 6 to 23 months. The number of children included per practice ranged from 18 to 275. Although influenza vaccine was administered from August 31, 2004, through April 5, 2005, in the practices surveyed, most (95%) doses were administered from October through January.
Proportion Vaccinated by Practice
Among practices, the proportion of children who were completely vaccinated ranged from 0% to 71% (median: 23%); the proportion who were partially vaccinated in 2004–2005 ranged from 6% to 62% (median: 24%; Fig 2).
Practice Characteristics and Strategies
Overall, half of the practices sampled were from Cincinnati, and one-quarter each were from Rochester and Nashville. Most practices described themselves as community-based, suburban primary care practices with a mean practice volume of 19 children per doctor per day; ≤25% of children in the practice received vaccine through VFC (Table 1). Eighteen (39%) practices reported an influenza vaccine shortage that limited their ability to vaccinate children who were aged 6 to 23 months.
Practice characteristics varied among the 3 counties: more Cincinnati and Rochester than Nashville practices were described as suburban (83%, 83%, and 36%, respectively; P = .01). Suburban practices reported having fewer children participating in VFC than urban practices (23% vs 85%; P < .001) and being less likely to save a second dose of vaccine for children who received the first of 2 recommended doses (18% vs 46%; P = .05).
Most (87%) practices reported using at least 1 strategy to facilitate influenza vaccination, with an average of 2 strategies per practice. The median complete influenza vaccine coverage increased from 12% to 32% (P = .29) for practices that reported from 0 to all 4 strategies, respectively (Fig 3).
The study children were equally divided by age groups (6 to <12 months, 12 to 17 months, and 18 to 23 months) and by gender. A total of 1735 well-child and 2910 follow-up or acute care office visits occurred from October through January. Most children had private (58%) or public (37%) health insurance; 1% had no insurance, and 4% had unknown insurance status. Overall, 9% of children had a high-risk medical condition for which influenza vaccine was specifically recommended.
More children with well visits from October through January than without such visits were completely vaccinated. Although proportions of completely vaccinated children were similar across counties, the proportions of unvaccinated children differed by location (P = .03).
Predictors of Complete Influenza Vaccine Coverage
A multinomial logistic regression analysis with random effects was performed to identify practice and child characteristics and practice strategies that predicted complete, partial, or no vaccination during 2004–2005 (Table 2). With the child as the unit of analysis, the model included random effects of sites and practices. Patient characteristics that were associated with complete influenza vaccination included (1) younger age, (2) high-risk condition for which influenza vaccine is specifically recommended, and (3) at least 6 well-child visits during the first 3 years of life. Practice characteristics that were associated with complete influenza vaccination included (1) any visit from October through January, (2) suburban practices (with a threefold higher vaccination coverage than urban practices), and (3) implementing evening/weekend influenza vaccine clinics (with a fourfold higher complete vaccination coverage).
Previous studies have examined interventions to improve influenza vaccination in children,10,–,14 but this study is the first, to our knowledge, to assess simultaneously practice and child characteristics and practice strategies that are associated with influenza vaccination coverage in geographically diverse sites. We found that 2 modifiable factors were associated with increased complete influenza vaccinations: any practice visit during October through January and evening/weekend influenza vaccine clinics. In the 2004–2005 study year, the first year when all children who were aged 6 to 23 months were recommended to receive vaccine and a year with a vaccine shortage, influenza vaccination coverage varied widely among practices : 0% to 71% for complete vaccination.
Overall, we found that 27% of children who were aged 6 to 23 months were completely vaccinated; these coverage rates were comparable to the upper range of those reported in the 2004–2005 National Immunization Survey and from sentinel vaccination sites.21,22 Our estimates were slightly higher than those reported by the Behavioral Risk Factor Surveillance System and a network of practices in New York City and slightly lower than that from Northern California Kaiser Permanente.23,–,25 Many factors likely influenced the variation in influenza vaccination estimates, including method for determining vaccination coverage.23,–,25
Confirmed by previous publications, several factors were associated with increased influenza vaccinations, including any practice visit from October through January.26 Also, children who were aged 6 to 11 months were more likely to be vaccinated than children who were aged 18 to 23 months.27 Whether this difference was attributable to providers' more frequent reviewing of vaccination status in younger than older children or more frequent visits in younger children is unknown. Children with high-risk conditions were prioritized during this vaccine shortage.28 Finally, evening/weekend vaccination clinics were associated with increased complete vaccination coverage, as was previously predicted.27,29 Discussing influenza vaccine year-round was a parental education strategy associated with a trend to increased complete vaccination. This strategy may be more effective if it were coupled with other strategies, such as year-round scheduling of influenza vaccination visits for the fall.30
One practice strategy, standing orders, is recommended by experts31,–,33 and has been associated with increased vaccine coverage in adult studies34,–,37; however, in our study, it was not associated with increased numbers of complete vaccinations. This paradoxical result likely reflects the inconsistent interpretation of the definition of standing orders,38 the ineffective coupling with other strategies, and/or inability of standing orders to overcome the uncertainty about how many doses each child needed to be completely vaccinated. For young children who need 2 vaccine doses, standing orders would need to be coupled with strategies to ensure receipt of the second dose. Additional study is needed on standing orders for children.34,–,37
This study has several limitations. Survey responses may have differed from actual practices.39,–,41 Variation in vaccination coverage among practices likely reflects a combination of differences among practices, patient populations, and parental priorities.42 All vaccinations received were based on chart review; however, children might have concurrently obtained care from multiple providers, and, thus, we may have missed some influenza vaccinations. The 6 nonparticipating practices may have systematically differed from those that participated, but with a practice response rate of 88%, this is unlikely to have affected the overall findings. Because this study was performed in urban and suburban settings, the generalizability of the results to rural counties is unknown. Race is frequently an important variable in vaccination status18,36,43; however, there is a paucity of data about racial/ethnic differences in influenza vaccination status among children. As in many practice-based studies, race was not obtainable from most charts and thus was not included in this study. In addition, we did not measure operational factors such as leadership, modification of current processes, measurement, reporting, and removal of barriers from practices, which probably influenced the effectiveness of all implemented strategies.44,–,46
Another limitation is that the 2004–2005 influenza season was the initial season when influenza vaccine was universally recommended for all children who were aged 6 to 23 months.7 The season was complicated by a limited supply of vaccine,47 making it difficult for some parents to have their child vaccinated48 and affecting 45% of pediatricians nationally with variation by region, practice type, and practice size.49 We measured the self-reported presence of a shortage within the practice; however, the dynamics of vaccine supply at the practice level, including which practices were affected and to what extent it affected public and/or private supplies and for how long, were not fully captured. In addition, some practices may have pooled their orders, and larger orders were generally filled earlier during this shortage. Thus, these results may not be representative of other influenza seasons. We studied several commonly used practice strategies for vaccine implementation but not all, such as year-around scheduling.30 Because of variations in interpretation of the reminder-recall question, we could not assess this practice strategy, although this intervention has already been shown by other studies to increase influenza vaccination coverage among children at high risk.10,14,50 The strategies that we investigated have not been well studied for children at high risk, and this is the first study to explore their effectiveness for influenza vaccination of all young children. Furthermore, we lacked the power to assess multicomponent strategies that are currently recommended.9
The expansion of influenza vaccine recommendations for children has created a challenge for pediatric providers. We found that influenza vaccine coverage for children who were aged 6 to 23 months in 2004–2005 varied widely among practices. Complete vaccination coverage was strongly associated with having a practice visit from October through January and with evening/weekend influenza vaccine clinics, suggesting that practice access is a key component. Our results suggest that high-volume practices should be cognizant of the need to implement strategies to vaccinate children better, such as scheduling evening/weekend influenza vaccine clinics at least 24 days apart or systematically scheduling second visits for those who need 2 doses. As physicians work to improve influenza vaccine coverage and as the vaccine recommendations expand to include all children who are aged 6 months to 18 years,9 continued assessment of practice-based strategies to enhance influenza immunization as well as parental preferences and priorities are needed.
This project was supported by cooperative agreement 1 U01 IP000022 from the Centers for Disease Control and Prevention and through cooperative agreements U38/CCU217969, U38/CCU417958, and U38/CCU522352.
We thank all the practices who participated and made this study possible. We also thank many others who provided invaluable support and contributions: Jim Alexander, MD, Carolyn Bridges, MD, John Copeland, SB, MS, Charmaine Coulen, MPH, Aaron Curns, MPH, Marika Iwane, MPH, PhD, Jennifer Reuer, MPH, Ben Schwartz, MD, Ranee Seither, MPH, Frances Walker, MSPH, and John Zhang, PhD, at the Centers for Disease Control and Prevention (Atlanta, GA); Nancy Back, BSN, MPH, Michol Holloway, MPH, Harrison Jackson, BS, Marilyn Rice, MS, and Meredith Tabangin, MPH, at Cincinnati Children's Hospital Medical Center (Cinicinnati, OH); Carol Ann Clay, RN, Diane Kent, RN, Erin Keckley, RN, Nayleen Whitehead, and Marie R. Griffin, MD, MPH, at Vanderbilt University Medical Center (Nashville, TN); and Christina Albertin, MPH, Geraldine Lofthus, PhD, Caroline B. Hall, MD, and Geoffrey A. Weinberg, MD, at University of Rochester School of Medicine and Dentistry (Rochester, NY).
We also thank the anonymous reviewers, whose suggestions significantly enhanced this manuscript.
- Accepted June 15, 2010.
- Address correspondence to Katherine A. Poehling, MD, MPH, Wake Forest University Medical Center, Department of Pediatrics, Winston-Salem, NC 27157. E-mail:
The views in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.
FINANCIAL DISCLOSURE: Dr Poehling has received support from Robert Wood Johnson Generalist Physician Faculty Scholar Program, National Institute of Allergy and Infectious Diseases (K23 AI065805), and Wachovia Research Fund; Dr Edwards receives research funding from the National Institutes of Health, the Centers for Disease Control and Prevention, Wyeth, Sanofi-pasteur, Novartis, and CSL Ltd; Dr Staat receives research funding from the Centers for Disease Control and Prevention, MedImmune, Merck, and GlaxoSmithKline and serves on the advisory board for MedImmune, Merck, and GlaxoSmithKline.
- CDC =
- Centers for Disease Control and Prevention •
- VFC =
- Vaccines for Children Program
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- Copyright © 2010 by the American Academy of Pediatrics