Published online June 22, 2007
PEDIATRICS Vol. 119 No. 3 March 2007, pp. e580-e586 (doi:10.1542/peds.2006-1580)
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ARTICLE

Influenza Vaccine Coverage and Missed Opportunities Among Inner-city Children Aged 6 to 23 Months: 2000-2005

Jennifer R. Verani, MD, MPH, Matilde Irigoyen, MD, Shaofu Chen, MD, PhD and Frank Chimkin, MBA, MSW

Department of Pediatrics, Columbia University, New York, New York


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. In 2002, the Advisory Committee on Immunization Practices recommended universal influenza vaccination of 6- to 23-month-olds. Little is known about coverage and missed opportunities for influenza vaccination at inner-city practices. The objective of this study was to assess the 2000–2001 to 2004–2005 coverage and the prevalence of missed opportunities for influenza vaccination among inner-city children.

METHODS. We conducted a retrospective review for the 2000–2001 to 2004–2005 influenza seasons at a practice network in New York City. The study population included 5 annual cohorts of 6- to 29-month olds as of March 31 of each year with ≥1 visit to the network in the previous 12 months (n = 7063). Immunization data were obtained from the network registry and the New York Citywide Immunization Registry. Coverage levels were estimated for 1 dose (partial) and 2 doses (full). Missed opportunities were assessed for visits within each influenza season.

RESULTS. Coverage rose steadily throughout the 5 years (full: 1.6% to 23.7%; partial: 1.5% to 18.1%). The relationship between year and coverage was linear. Missed opportunities occurred in 82% of visits and were more common for first (89%) than for repeat doses (38%). Missed opportunities per child per season decreased from 2.9 to 2.0 during the study period.

CONCLUSIONS. Influenza vaccine coverage among 6- to 23-month-olds at inner-city practices increased steadily from 2000–2001 through 2004–2005, and the prevalence of missed opportunities per child decreased. However, coverage remained suboptimal, with most of children not vaccinated or undervaccinated. Missed opportunities were major contributors to low coverage.

Key Words: childhood immunizations • influenza vaccine • inner-city children • missed opportunities

Abbreviations: ACIP—Advisory Committee on Immunization Practices • CIR—Citywide Immunization Registry • CI—confidence interval

Influenza is a significant cause of morbidity for young children and infants.1–5 Hospitalization rates for influenza-attributable disease among children who are younger than 2 years are comparable to those of elderly and older children with chronic illnesses.6–8 In 2002, the Advisory Committee on Immunization Practices (ACIP) encouraged the immunization of healthy children aged 6 to 23 months,1,9 and in 2004, ACIP recommended universal vaccination of this age group.10 Given concerns about the viability of incorporating additional shots to an already crowded childhood immunization schedule,11,12 as well as the low coverage levels that are seen among other groups of at-risk children with long-standing recommendations for annual influenza vaccine,13–16 it is important to evaluate the uptake of this recommendation.

A small number of publications have described increases in influenza vaccine coverage levels after the changes in recommendation. Among inner-city children who were seen at a resident clinic in Nashville, Tennessee, coverage for at least 1 influenza vaccine dose increased from 1% in 2002 to 17% in 2003. In 2002–2003, on the basis of telephone surveys that were conducted nationwide, 7% of children aged 6 to 23 months had received at least 1 influenza dose17; in 2004–2005, coverage had increased to 48%.18 Among patients who were enrolled in a large health maintenance organization in California, coverage increased from 47% in 2003–2004 to 57% in 2004–2005, based on registry data and population estimates.19

Although influenza vaccine coverage is increasing, questions remain regarding the nature and the extent of the coverage and the challenges that remain. Studies have compared coverage for 1 or 2 seasons for the same population, yet descriptions of coverage that encompass the years before and after the ACIP recommendations may help understanding of patterns of uptake. Few studies have focused on inner-city populations, where immunization coverage levels are known to be low.20–22 Much of the research has relied on parental surveys, which are subject to recall bias. In addition, provider immunization delivery practices are a key determinant of vaccination levels, and additional research is needed on the contribution of provider practices to influenza vaccine coverage. For example, missed opportunities are known to contribute to low influenza vaccine coverage among children with asthma,23 as well as in children with chronic medical conditions,24 yet their impact on influenza vaccination among healthy young children is unknown. The 2 objectives of this study were (1) to assess influenza vaccine coverage levels among children aged 6 to 23 months in an inner-city population during 2000–2005, a 5-year time period that spanned the change in ACIP recommendation, and (2) to assess the impact of provider missed opportunities on influenza coverage levels in this age group.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Setting
The study was conducted at a network of 5 community-based pediatric practices that are affiliated with an academic health center at an inner-city community in New York City. The network is the major pediatric health care provider in the community (>63000 pediatric visits in 2005, ranging from 8000 to 20000 per practice). The patient population predominantly is Latino and black. Most children are covered by Medicaid, and of these, half are enrolled on managed care plans. The Vaccine for Children Program provides the majority of vaccines (>90%) that are given at the practices.

Study Design and Population
We conducted a retrospective cohort study of influenza vaccine coverage among children who were aged 6 to 23 months for 5 consecutive influenza seasons. The eligibility criteria included (1) age 6 to 29 months as of March 31 (2001–2005) of each year and (2) at least 1 visit to the network in the previous 12 months. We included children who were aged up to 29 months because they would have been ≤23 months at the start of the season and therefore eligible for vaccination. The children then were grouped into 5 annual cohorts of children, 2000–2001 through 2004–2005, with a cohort sample size ranging from 1396 to 1428. Each child could have been included in up to 2 cohorts.

Data Sources
Children were identified through the network's billing/registration system, which was the source for demographic and visit data. Children were classified as Medicaid participants when they were currently or at any time in the past insured by Medicaid.

Vaccine data were collected from both the network immunization registry, EzVAC, and the New York Citywide Immunization Registry (CIR). EzVAC is a point-of-service registry that is linked to the hospital billing system and includes all children who receive care at the hospital or affiliated network. CIR is New York City's population-based registry. EzVAC has a capture proportion of 95% of vaccines administered at network sites (M. Irigoyen, MD, verbal communication, 2006). New York City providers are mandated to report to CIR: >90% of providers report to CIR, and, of these, 80% do so regularly (A. Metroka, MSW, written communication, 2003).

Outcome Measures
For each cohort, we determined influenza vaccine coverage levels. We defined "full coverage" as 2 doses of influenza vaccine, either 2 doses in 1 season or 1 dose during the season of interest and at least 1 dose during the previous season. We defined "partial coverage" as only 1 dose among children who did not receive a dose during the previous season. "Any coverage" included all children with either full or partial coverage.

Missed opportunities were defined as clinic visits during the vaccination period during which the child was eligible for vaccination but no influenza vaccine was given. To control for availability of the vaccine, we started the vaccination period with the date of administration of the first dose of influenza vaccine per season for each clinic site and continued through March 31. We examined missed opportunities for the first and second doses. Missed opportunity visits included (1) for children who received no influenza vaccine during the season, any visit during the vaccination period; (2) for children who needed 2 doses but received only 1, any visit before the date of the first dose and any visit >1 month after the date of the first dose; (3) for children who needed only 1 dose and received 1 dose, any visit before the visit in which the dose was given; and (4) for children who needed 2 doses and received 2 doses, any visit before the visit in which the first dose was given and any visit >1 month after the date of the first dose and before the date of the second dose. Visits that occurred when a child was aged <6 months or >23 months were not considered missed opportunities.

Analysis
We calculated 95% confidence intervals (CI) for all 3 types (full, partial, and any) of influenza vaccine coverage. We also conducted Pearson's correlation analysis to test the trend over the 5-year period in coverage levels. All analyses were conducted with SPSS 13.0 (SPSS Inc, Chicago, IL). The study was approved by the institutional review board of Columbia University Medical Center.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Study Population
As shown in Table 1, half of the children were male, and there was an even distribution across age groups. Most children were insured by Medicaid. There were no significant differences across the 5 cohorts with regard to age, gender, or insurance type. The annual cohorts ranged in size from 1396 to 1428 with a mean of 1413 and a total N = 7063 for the 5-year period (Table 2). A total of 88.4% of vaccines were recorded in both registries; 5.2% of vaccines were recorded in EzVAC only, and 6.5% were recorded in CIR only. Each season, >90% of vaccines were administered between October and January (Fig 1).


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  		TABLE 1 Study Population Characteristics

 

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  		TABLE 2 Influenza Vaccine Coverage Levels: Children Aged 6 to 23 Months, 2000–2005

 

Figure 1
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  		FIGURE 1 Percentage of cumulative distribution of influenza vaccine doses over time by season.

 
Coverage Levels
Coverage levels increased throughout the 5-year period (Table 2). From 2000 though 2005, coverage for any dose rose from 3.2% (95% CI: 2.2%–4.1%) to 41.8% (95% CI: 39.2%–44.3%). The proportion of children who were fully immunized increased from 1.6% (95% CI: 1.0%–2.3%) to 23.7% (95% CI: 21.5%–25.9%) during the 5-year period, and the proportion who were partially vaccinated (required 2 doses but received only 1) increased from 1.5% (95% CI: 0.9%–2.2%) to 18.1% (95% CI: 16%–20.1%). The relationship between year and coverage was linear for both fully and partially immunized (R2 = 0.9139 and R2 = 0.9322, respectively; Fig 2).


Figure 2
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  		FIGURE 2 Trends in influenza vaccine coverage levels, children 6 to 23 months of age, 2000–2005.

 
Coverage initially was higher among the children aged 25 to 29 months at the end of the season. However, in the years after the change in recommendation, coverage increased most dramatically among 13- to 24-month-olds. In 2004–2005, coverage was highest among those aged 13 to 18 months (31.5% [95% CI: 26.7%–36.4%] were fully vaccinated) and lowest among those aged 6 to 12 months (16.9% [95% CI: 13.0%–20.7%]; Fig 3).


Figure 3
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  		FIGURE 3 Influenza vaccine full coverage by age, 2000–2005.

 
Missed Opportunities
Missed opportunities occurred in 82.2% (95% CI: 81.5%–83.0%) of all vaccine-eligible visits. Of the visits during which a first dose of vaccine could have been administered, 89.2% (95% CI: 88.6%–89.8%) resulted in missed opportunities. Among visits that were eligible for a second dose, the proportion of missed opportunities was lower (38.4% [95% CI: 35.9%–40.8%]). The months with the greatest proportion of missed opportunities varied from year to year, with no clear trend over the 5-year study period.

When looking at missed opportunities that were experienced by each child, we found that the proportion of children in each cohort with at least 1 missed opportunity ranged from a high of 61% (95% CI: 58.8%–63.9%) in 2001–2002 to a low of 40% (95% CI: 37.5%–42.7%) in 2004–2005 (Fig 4). The average number of missed opportunities per child decreased from 2.9 in 2000–2001 to 2.0 in 2004–2005 (Fig 5). The proportion of all visits with missed opportunities decreased steadily during the 5-year period—from 97% in 2000–2001 to 55% in 2004–2005—and was inversely proportional to coverage level (Fig 6).


Figure 4
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  		FIGURE 4 Percentage of children with missed opportunities for influenza vaccination by season, 2000–2005.

 

Figure 5
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  		FIGURE 5 Average number of missed opportunities for influenza vaccination per child per season, 2000- 2005.

 

Figure 6
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  		FIGURE 6 Influenza vaccination in children aged 6 to 23 months: visits with missed opportunities and coverage levels by season, 2000–2005.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
In response to a growing body of evidence that young children are at high risk for significant influenza-related morbidity, in 2002, ACIP expanded its recommendations to include vaccination of children aged 6 to 23 months. This study found that in the 5-year period that spanned the change in recommendation, coverage levels for 6- to 23-month-olds at an inner city practice network increased steadily. Nonetheless, even in 2004–2005, more than three quarters of children were either nonvaccinated or undervaccinated. Each year, nearly half of children who received 1 dose of vaccine failed to receive a required second dose. These low coverage levels are striking when compared with the high levels of coverage that were seen for other childhood vaccines in the United States.21,22

The range of full and partial influenza vaccine coverage levels in this population falls within those reported by previous studies.17–19,25–28 The increase in coverage after the change in recommendation also is consistent with previously published data. The perspective of a 5-year window provides additional insight into the adaptation of the new policy. One might expect a marked increase in coverage level in the season immediately after the change in recommendation. However, our data showed a more gradual, linear increase in coverage from 2000–2005, with suboptimal coverage even at the end of the 5-year period.

Our study found extremely high numbers of missed opportunities for influenza vaccination: >80% of all possible occasions to vaccinate were missed. The proportion of visits with missed opportunities per season decreased markedly during the 5-year study period, and the inverse relation with coverage levels highlights the crucial role that missed opportunities play in determining influenza immunization coverage. Missed opportunities have been shown to contribute to low levels of influenza vaccination among children with asthma23 and other high-risk conditions.24 Notably, a much larger proportion of first dose–eligible visits resulted in missed opportunities as compared with second dose–eligible visits, suggesting fewer barriers to receiving a second dose once a first dose of vaccine has been administered. Our data do not provide insight into the reasons behind missed opportunities (eg, oversight, physician noncompliance, parental opposition). More research in this area is required, and future efforts to improve vaccination coverage should focus on reducing missed opportunities, particularly for the first dose.

Low coverage and missed opportunities may reflect a lack of physician compliance with the new recommendation. According to the awareness-to-adherence model, physicians progress through 4 phases in the process of changing clinical behaviors in response to clinical guidelines: awareness, agreement, adoption, and adherence.29 Awareness of influenza vaccine guidelines may have been affected by the changing nature of the recommendation. In 2002 and 2003, ACIP urged physicians to "encourage when feasible" the vaccination of healthy children aged 6 to 23 months,9 but in 2004, ACIP "recommended" universal vaccination in this age group.10 A survey that was conducted in 2001 reported that only 50% of pediatricians and 40% of family practitioners believed that universal influenza vaccination of children aged 6 to 23 months would be feasible.30 The perception that one is not capable of implementing a new guideline is an important barrier to physician compliance.31

Parental beliefs and attitudes also can serve as a barrier to immunization. Parents frequently have concerns about the safety of the influenza vaccine,32,33 particularly inner-city parents.34 Parents often do not perceive their child to be at risk.33,35 Parental attitudes may have changed after the 2003–2004 season, which received substantial media attention regarding severe influenza cases among children.36 Surveys of parents consistently find that the recollection of a physician recommendation for influenza vaccine is associated with higher reported vaccination levels.35–37

Studies have demonstrated the effectiveness of interventions that aim to increase influenza vaccine coverage among 6- to 23-month-olds. A multifaceted strategy that comprises education, reminders, standing orders, and express immunization service had a strong positive impact at 10 inner-city clinics in Pittsburgh, Pennsylvania, during the 2002–2003 season.27 Likewise, a registry reminder intervention proved effective at increasing coverage during the 2003–2004 season in Denver, Colorado.28 There is significant evidence to support the use of provider reminder recall and provider assessment and feedback to reduce missed opportunities for vaccination among children.13,38–41 Given the low levels of vaccination among children aged 6 to 23 months found in this and other studies, such interventions will be needed to achieve adequate immunization coverage.

This study had several limitations. The coverage levels may have been underestimated as a result of underreporting to 1 or both registries. This problem may be compounded by use of multiple providers and record scatter.42 The study population was limited to patients of 1 practice network that serves inner-city children, and the findings may not be generalizable to other types of practices or patient populations. We assumed a steady supply of vaccine starting from the first date of administration of an influenza vaccine at each site; however, shortages may have affected delivery of vaccine and coverage. Although shortages theoretically should not have affected coverage in this prioritized at-risk group, there were reports in 2004–2005 of difficulties in obtaining vaccine for children aged 6 to 23 months,43 and it is unclear how shortages may have affected coverage during the 5-year period. Last, we may have overestimated missed opportunities; some of these may be attributable to parent refusals.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Influenza vaccine coverage among a population of inner-city children aged 6 to 23 months increased steadily from 2000 through 2005. However, even in the final year of analysis, coverage was suboptimal, with more than three quarters of children in this age group remaining nonvaccinated or undervaccinated. Throughout the study period, >80% of all opportunities to vaccinate were missed. The proportion of visits with missed opportunities by season decreased during the 5-year period and was inversely proportional to coverage levels. In the future, continuous monitoring of coverage among this age group is required. It is important to investigate factors that contribute to missed opportunities, particularly for the first dose. The role of vaccine supply and shortages on coverage in this age group is another area for future research. Interventions that are known to be effective at increasing influenza vaccine coverage among other high-risk groups should be expanded to include this age group.


   FOOTNOTES
 
Accepted Sep 15, 2006.

Address correspondence to Shaofu Chen, MD, PhD, Department of Pediatrics, Columbia University, 622 W 168th St, VC-412, New York, NY 10032. E-mail: sc57{at}columbia.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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