Published online October 31, 2008
PEDIATRICS Vol. 122 No. 5 November 2008, pp. 920-928 (doi:10.1542/peds.2007-3032)
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ARTICLE

Influenza Vaccination in Adolescents With High-Risk Conditions

Mari M. Nakamura, MD, MPHa,b and Grace M. Lee, MD, MPHb,c

a Harvard Pediatric Health Services Research Fellowship Program
c Division of Infectious Diseases, Departments of Medicine and Laboratory Medicine, Children's Hospital Boston, Boston, Massachusetts
b Department of Ambulatory Care and Prevention, Harvard Medical School and Harvard Pilgrim Health Care, Boston, Massachusetts


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVES. We assessed influenza vaccination rates from 1992 to 2002, individual continuity of vaccination, and missed opportunities for vaccination in adolescents with high-risk conditions.

METHODS. We performed a retrospective observational study of 18 703 adolescents with high-risk conditions who were enrolled in a large health maintenance organization and received care at a multisite practice for ≥1 influenza season and the preceding year, between 1992 and 2002, was performed. Subjects were identified as having a high-risk condition if they had ≥1 visit with an associated International Classification of Diseases, Ninth Revision, Clinical Modification code during the season or previous year. Influenza vaccination rates were compared by season in logistic regression analyses, using generalized estimating equations for repeated measurements of subjects enrolled for multiple seasons. Vaccination continuity was measured for adolescents who were enrolled for 4 consecutive seasons (1999–2002) as the number of seasons during which vaccine was received. Missed opportunities were defined as visits during the first 4 months of influenza season at which an unvaccinated adolescent did not receive vaccine.

RESULTS. For adolescents with high-risk conditions, influenza vaccination rates varied from 8.3% to 15.4%. Rates improved significantly from 1992 to 1993, from 8.3% to 12.8%, and again in 2001, reaching 15.4%. Only 11.1% of those enrolled continuously from 1999 to 2002 received vaccine during all 4 seasons. According to season from 1992 to 2002, 45.7% to 53.6% of unvaccinated subjects had ≥1 missed opportunity.

CONCLUSIONS. Influenza vaccination rates in adolescents with high-risk conditions improved from 1992 to 2002 but were still low in recent years. Individual vaccination continuity was poor. Numerous opportunities already exist for improving coverage.

Key Words: high-risk conditions • adolescents • influenza vaccine • missed opportunities

Abbreviations: ICD-9-CM—International Classification of Diseases, Ninth Revision, Clinical Modification • CI—confidence interval • ACIP—Advisory Committee on Immunization Practices • HVMA—Harvard Vanguard Medical Associates • HPHC—Harvard Pilgrim Health Care • OR—odds ratio

Each year, influenza affects 20% to 40% of children and adolescents.1 The burden of influenza is particularly high in children with high-risk conditions; annually, influenza accounts for 2 to 19 excess hospitalizations (2–4 times higher than in healthy children), 120 to 200 outpatient visits, and 65 to 140 antibiotic courses per 1000 children at high risk.2 The Advisory Committee on Immunization Practices (ACIP) of the Centers for Disease Control and Prevention has published guidelines for pediatric influenza vaccination since before 1990.3 Annual influenza vaccination is recommended for children and adolescents 6 to 59 months of age and for those with conditions that place them at increased risk of influenza complications. Influenza vaccination is also recommended for household contacts or caretakers of persons with high-risk conditions.4

Despite the burden of influenza and long-standing vaccination recommendations, studies have demonstrated that influenza vaccination coverage among children and adolescents with high-risk conditions is low, ranging from 9% to 31%.5–8 The recent addition of meningococcal conjugate, tetanus toxoid-reduced diphtheria toxoid-acellular pertussis, and human papillomavirus vaccines to the adolescent schedule has renewed interest in understanding how to improve vaccination rates among adolescents. Furthermore, because universal influenza vaccination has now been recommended for children 6 to 59 months of age, discussion has intensified about expanding recommendations for universal vaccination to adolescents.

Although some studies have described aggregate influenza vaccination rates that include adolescents, none has focused specifically on this age group.5,7,8 To examine how well the current risk-based approach has worked for adolescents with high-risk conditions, we characterized influenza vaccination rates in this population. Our goals were (1) to assess annual influenza vaccination rates over a recent 11-year period in adolescents with high-risk conditions; (2) to evaluate individual influenza vaccination continuity, that is, the consistency with which patients receive vaccine from year to year; and (3) to examine missed opportunities for influenza vaccination among adolescents.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
The study population consisted of adolescents with conditions that placed them at increased risk of influenza complications who received care at Harvard Vanguard Medical Associates (HVMA) and were enrolled in Harvard Pilgrim Health Care (HPHC) between 1991 and 2003. HVMA is a large, multispecialty, group practice composed of 14 health centers serving ~300 000 patients in the Boston metropolitan area. HPHC is the largest nonprofit health insurance plan in New England. HPHC covers the cost of influenza vaccine administration, as well as the cost of vaccine itself if state-purchased vaccine is unavailable (Massachusetts is a universal purchase state), for patients with high-risk conditions. Influenza vaccine also is encouraged and offered at no cost for HVMA health care providers.

The inclusion criteria for our study were (1) being enrolled in HPHC and receiving care at HVMA for ≥1 influenza season, defined as October 1 through April 30, and the preceding 1-year period between 1992 and 2002; (2) age between 11 and 17 years during the influenza season; and (3) having a high-risk condition for influenza, as specified by ACIP guidelines for influenza vaccination, which remained unchanged during the study period.9,10 From 1992 to 2002, conditions for which influenza vaccination was recommended included asthma and other chronic pulmonary diseases, hemodynamically significant cardiac disease, immunosuppressive disorders or therapy (including HIV infection), sickle cell anemia and other hemoglobinopathies, diseases requiring long-term aspirin therapy, chronic renal dysfunction, and chronic metabolic diseases such as diabetes mellitus.9,10 On the basis of ACIP recommendations and previous studies on influenza in high-risk subjects,2,11–16 we compiled a set of International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) codes for high-risk conditions (Appendix). Subjects were identified as having a high-risk condition if they had ≥1 visit or hospitalization associated with 1 of those ICD-9-CM codes during the influenza season or preceding year.


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  		APPENDIX ICD-9-CM Diagnoses Associated With Increased Risk of Influenza Complications

 
Study Design
Data available from HPHC databases and HVMA electronic medical records included (1) dates of birth; (2) gender; (3) dates of enrollment; (4) dates and associated ICD-9-CM codes for outpatient visits, emergency department visits, and hospitalizations; and (5) dates and types of vaccinations received. Data on race and ethnicity, the HVMA site at which an influenza vaccine was given, the provider by whom a vaccine was administered, and egg allergy or parental refusal of vaccination were not available in existing databases.

Influenza vaccination rates for adolescents with high-risk conditions were calculated for each influenza season from 1992 to 2002. (An influenza season is referred to herein by the year in which it began; the period spanning October 1, 1992, to April 30, 1993, for example, is designated the 1992 season.) Influenza vaccination rates in high-risk adolescents over the 11-season observation period were compared, controlling for age, gender, preventive care use, and type of high-risk condition as factors that also might affect the likelihood of influenza vaccination.

Age was divided into 2 categories, that is, 11 to 13 years and 14 to 17 years. These age ranges, corresponding to the early and middle stages of adolescence, are developmentally relevant and are thought to relate to health choices and behaviors.17 Preventive care use was also treated as a dichotomous variable (0 versus ≥1 preventive care visit during the influenza season or preceding year). Outpatient visits were considered preventive if associated with code V20.2 (routine infant or child health check), V70.0 (routine general medical examination at a health care facility), or V70.3 (other medical examination for administrative purposes). Types of high-risk condition were represented as 7 categories, that is, (1) asthma or other chronic pulmonary disease, (2) chronic cardiac disease, (3) immunosuppressive disorder or therapy (including HIV infection and disorders requiring long-term aspirin therapy), (4) sickle cell anemia or other hemoglobinopathy, (5) chronic renal dysfunction, (6) chronic metabolic disease, and (7) >1 type of high-risk condition (for subjects who had visits associated with multiple types of ICD-9-CM diagnoses).

Individual vaccination continuity was assessed for subjects who were enrolled for 4 consecutive influenza seasons, from 1999 to 2002, and was measured as the number of seasons during which vaccine was received (range: 0-4 seasons). Missed opportunities were defined as outpatient visits during the first 4 months of influenza season (October through January) at which an unvaccinated high-risk subject did not receive influenza vaccine.

Data Analysis
Influenza vaccination rates were calculated for each season as the proportion of adolescents with high-risk conditions who received influenza vaccine. Changes in vaccination rates over time were assessed by using logistic regression; generalized estimating equations were employed to account for repeated measurements of subjects who were enrolled for >1 season. Age, gender, preventive care use, and type of high-risk condition were included as covariates. Because it was postulated that providers might think more often of vaccinating younger adolescents at preventive care visits, an interaction term for age and preventive care use also was included. An exchangeable correlation structure was used because the low individual vaccine continuity observed in our study suggested that receipt of influenza vaccine was not substantially more correlated between consecutive seasons than between nonconsecutive seasons.

To describe individual vaccination continuity, the proportions of subjects with high-risk conditions who were vaccinated during 0, 1, 2, 3, or 4 seasons between 1999 and 2002 were calculated. The {chi}2 test was used to assess whether an association existed between type of high-risk condition and continuity score.

To measure the frequency of missed opportunities for vaccination for each season, the proportion of adolescents with high-risk conditions who had ≥1 missed opportunity and the proportion who had ≥3 missed opportunities were determined. For all analyses, a P value of <.05 was used as the criterion for statistical significance. Analyses were performed by using Stata 9.0 (Stata, College Station, TX).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Study Population
In the 1992–2002 seasons, 18 703 adolescents with high-risk conditions were enrolled in HPHC and received care at HVMA (Table 1). Subjects were enrolled for an average of 2.1 influenza seasons (range: 1–7 seasons), resulting in 38 680 person-seasons of observation during the study period. The most common type of high-risk condition, identified in ~90% of subjects in each season, was asthma or another pulmonary condition. The frequency of types of high-risk conditions did not differ notably according to gender. According to influenza season, 73.7% to 87.6% of subjects had ≥1 preventive care visit during the season or previous year.


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  		TABLE 1 Study Population Characteristics (N = 18 703 Unique Subjects)

 
Influenza Vaccination Rates
During the 11 influenza seasons from 1992 to 2002, influenza vaccination rates in adolescents with high-risk conditions improved most strikingly from the 1992 season to the 1993 season, increasing from 8.3% (95% confidence interval [CI]: 7.3%–9.4%) to 12.8% (95% CI: 11.7%–14.0%) (Fig 1). Vaccination rates fluctuated thereafter, reaching a high of 15.4% (95% CI: 14.2%–16.7%) during the 2001 season. The vaccination rate in the final season, 2002, was 14.6% (95% CI: 13.5%–15.8%). Even in recent seasons, only ~500 of the ~3000 adolescents with high-risk conditions during each season received influenza vaccine (Fig 1).


Figure 1
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  		FIGURE 1 Influenza vaccination rates.

 
Because the greatest improvement occurred from the 1992 season to the 1993 season, the 1993 season was used as the reference season in the multivariate logistic regression analysis of vaccination rates. After adjustment for age, gender, preventive care use, and type of high-risk condition and controlling for repeated measurements of subjects, the change in vaccination rate from 1992 to 1993 was found to be significant (Table 2). The odds of receiving influenza vaccine were 0.53 times lower in 1992, compared with 1993 (P < .001). With the 1993 season as reference, the influenza vaccination rate did not change significantly again until 2001, when subjects were 1.22 times more likely to have been vaccinated than in 1993 (P = .009). In the final season, 2002, the odds of receiving influenza vaccine were 1.16 times greater than in 1993, a difference of borderline significance (P = .05).


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  		TABLE 2 Predictors of Influenza Vaccination for Adolescents With High-Risk Conditions

 
In multivariate analyses, age, gender, preventive care use, and type of high-risk condition also were significantly associated with influenza vaccination (Table 2). Adolescents 11 to 13 years of age were 1.21 times more likely to be vaccinated than those 14 to 17 years of age (P < .001), whereas female subjects were 0.90 times less likely to be vaccinated than male subjects (P = .013). Subjects who had received preventive care during the influenza season or preceding year were 1.25 times more likely to have received vaccine (P < .001). Finally, compared with subjects who had asthma or another pulmonary disease, vaccination was more likely for subjects with immunosuppressive therapy or an immunosuppressive disorder (odds ratio [OR]: 1.32; P = .027), a cardiac disease (OR: 1.44; P = .003), a metabolic disease (OR: 2.97; P < .001), or >1 type of high-risk condition (OR: 1.38; P = .002). The interaction term for age and preventive care use was not significant and was not retained in the final model.

Individual Vaccination Continuity
Among the 377 subjects who were enrolled continuously from the 1999 season to the 2002 season, only 11.1% were vaccinated against influenza in all 4 seasons; 15.6% were vaccinated in only 1 season, 7.4% in 2 seasons, and 9.3% in 3 seasons. The remaining 56.5% never received influenza vaccine during the 4 seasons. Continuity was not significantly associated with the type of high-risk condition, which suggests that, although annual vaccination rates were significantly better among subjects with certain high-risk conditions, as detailed above, individual vaccination continuity was equally low across conditions. Vaccination continuity was even worse, however, among non–high-risk adolescents; only 2.1% of adolescents without high-risk conditions received vaccine in all 4 seasons.

Missed Opportunities
According to season, ~45% to 55% of unvaccinated adolescents had ≥1 outpatient visit during the first 4 months of influenza season during which influenza vaccine was not administered (Fig 2). The proportion of unvaccinated subjects who had ≥3 missed opportunities was lower but still notable, ranging by season from ~17% to 25%. The most frequent diagnoses associated with missed-opportunity visits were preventive care; asthma, unspecified; acute pharyngitis; cough; and need for prophylactic vaccination and inoculation against unspecified disease.


Figure 2
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  		FIGURE 2 Missed opportunities.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We determined that influenza vaccination rates improved significantly for adolescents with high-risk conditions over a recent 11-year span, even though vaccination recommendations were unchanged for adolescents during that time period. This finding is eclipsed, however, by poor coverage overall; even in recent seasons, ~85% of adolescents were not vaccinated against influenza despite having a condition that predisposed them to influenza complications. In addition, we discovered that individual vaccination continuity was low regardless of the type of high-risk condition, with only 11.1% of subjects who were enrolled continuously for 4 recent seasons receiving influenza vaccine during every season. Although reaching never-vaccinated patients is the greatest priority for achieving high influenza vaccination coverage, improvement in vaccination continuity for the ever-vaccinated is also needed. Approximately one half of all unvaccinated subjects each season had ≥1 visit during the first 4 months of influenza season. Many of these encounters seem to have been true missed opportunities, because the most commonly associated diagnoses (preventive care, asthma, pharyngitis, cough, and other vaccinations) were not major febrile illnesses for which vaccination would have been contraindicated.

Our multivariate analyses revealed that, although changes in influenza vaccination rates were independently associated with time, patient characteristics (gender, age, preventive care use, and type of high-risk condition) also predicted the likelihood of vaccination. The reason for lower vaccination rates among female subjects is unclear. Some studies of health services use among school-aged patients revealed no differences according to gender,18,19 whereas another study determined that, among older adolescents, female subjects had more overall visits, largely because of visits to obstetricians/gynecologists.20 Studies of hepatitis B immunization rates in adolescents suggested that female subjects are more likely to be immunized.21 Nuances of the relationship between gender and health care utilization in this age group remain to be elucidated.

The higher vaccination coverage observed in younger subjects may result from greater influence of parents and other adults on younger adolescents regarding immunizations and other health matters.17 Providers may more readily think of vaccinating younger adolescents against influenza, consistent with physicians' reports that they were more likely to assess immunization status and to administer immunizations in younger adolescents.22 The association of preventive care use with a higher likelihood of influenza vaccination may indicate that patients (or their parents) who attend health maintenance visits tend to pursue preventive health, including vaccinations, more actively. However, the combination of low influenza vaccination rates (8.3%–15.4%) and high preventive care use (73.7%–87.6%) in our subjects suggests that preventive care use does not in itself ensure good immunization coverage.

Patients with immunosuppressive therapy or an immunosuppressive disorder, a cardiac or metabolic disease, or >1 type of high-risk condition were more likely to receive vaccine than were those with the most common type of condition, asthma or another pulmonary disease. This finding could reflect better knowledge of influenza risk factors and vaccination recommendations within these patient subpopulations or greater awareness and more successful immunization strategies on the part of their providers. It also highlights the need for increasing vaccination coverage in patients with asthma, given the prevalence of this disease. The heterogeneity of asthma severity could be one explanation for low vaccination rates; providers may not remember to vaccinate patients with milder asthma against influenza.

The high rate of missed opportunities for our subjects is consistent with a 2002 analysis of children 6 to 72 months of age with high-risk conditions, in which missed opportunities for influenza vaccination occurred at 78% of all vaccine-eligible visits for patients with asthma and 74% of visits for those with other conditions.23 The frequency of missed opportunities suggests that interventions aimed at not only patients but also providers could have a substantial impact on coverage. Both patient and provider reminders increase immunization rates,24 and reminder systems integrated with electronic health records or billing systems can facilitate identification of patients with high-risk conditions.11 During the study period, families of high-risk adolescents were mailed a reminder letter to receive influenza vaccine at the start of influenza season. An electronic reminder system for providers was incorporated into the electronic health record at HVMA after 2003, but its impact on adolescent influenza vaccination coverage has not yet been examined.

The poor influenza vaccination rates observed for our subjects support the potential merits of universal influenza vaccination for pediatric patients. Policies based on risk may be too complex, particularly for a vaccine that must be administered each year within a limited time window. Experience with other vaccines suggests that universal age-based recommendations are more effective than risk-based guidelines.25 A recent study on adolescents enrolled in HPHC and HVMA determined, for example, that 13-year-old subjects in 2004 were up to date for tetanus-diphtheria, hepatitis B, and measles-mumps-rubella vaccinations at rates of 92%, 82%, and 85%, respectively.26 Regarding influenza vaccine, vaccination rates among children 6 to 23 months of age in 2004 (the first season during which the ACIP recommended universal vaccination for this age group) were higher than rates among older children with high-risk conditions.25

A study limitation was lack of data regarding the practice site at which subjects were vaccinated and the providers who administered the vaccine; we were therefore unable to control for possible clustering according to practice site or provider in our evaluation of vaccination rates. In addition, because our subjects attended a multisite group practice in the Boston metropolitan area, some of our findings might have limited generalizability to other adolescent populations. The influenza vaccination status of study subjects was determined from HVMA automated medical records and did not reflect vaccine administration outside the practice. A previous study on influenza vaccination in HVMA pediatric patients, however, found that only a very small proportion of patients received vaccine from another source.27

Because our study was a cross-sectional analysis, we could not establish causes for improvements in vaccination coverage or, conversely, reasons why rates remained so low overall. Influenza vaccination rates increased in the early 1990s in other populations, such as adults ≥65 years of age and health care workers,28,29 but no published studies report coverage during that time among comparable subjects, such as adults with high-risk conditions. No policy changes regarding influenza vaccination occurred at HVMA that might explain the marked increase in rates in our study population from 1992 to 1993 (B. Kruskal, MD, PhD, written personal communication, January 22, 2008). Local newspaper stories during the 1993 season, however, documented sharply increased demand within Massachusetts for influenza vaccine, which was attributed to federal warnings regarding a possible early and severe influenza season.30,31 Such publicity might have contributed to the increase in coverage in 1993.

We investigated whether vaccine supply issues might have affected coverage or missed opportunities. No influenza vaccine shortages took place during the observation period, but availability was delayed for a portion of the doses in 2000 and 2001.32,33 Although ACIP recommendations during those years emphasized prioritizing vaccination of subjects with high-risk conditions32,33 and 2001 was the peak season for vaccination coverage for our subjects, delayed availability of vaccine might have caused lower vaccination rates than would have occurred otherwise. Data on HVMA's vaccine supply are not available, but to examine whether a substantial proportion of apparent missed opportunities were actually attributable to delayed vaccine availability, we reassessed missed opportunities during November through January only. Even with omission of the first month of influenza season, 35% to 45% of unvaccinated adolescents by season had ≥1 missed opportunity. We also observed that patients were vaccinated through late January or beyond during each season, which suggests that vaccine remained available even at the end of the typical influenza vaccination period.

Whatever the underlying causes, we conclude that the persistence of poor influenza vaccination rates demands a different approach to influenza vaccination for adolescents with high-risk conditions. Universal vaccination may be such a strategy, but issues must be addressed to make universal vaccination feasible. These challenges include expansion of vaccination programs to sites such as schools, to reach large numbers of patients; creation of a more-stable vaccine supply, available earlier in the year; and development of financing systems to make vaccination affordable for families and providers.25 In the meantime, adoption of measures such as reminder systems could promote the use of existing vaccination opportunities and help patients with high-risk conditions and their providers to establish yearly influenza vaccination as routine.


   ACKNOWLEDGMENTS
 
This work was supported by the Harvard Pilgrim Health Care Foundation, through an Ebert Award. Dr Lee was also supported by grant K08 HS013908-01A1 from the Agency for Healthcare Research and Quality. Dr Nakamura was supported by grant T32 HS000063-13 from the Agency for Healthcare Research and Quality.

We are grateful to Tracy A. Lieu, MD, MPH, for her valuable suggestions regarding study design. We thank Dionne Graham Manning, PhD, and Jui Haker, MD, MPH, of the Children's Hospital Clinical Research Program for their advice on statistical methods. We are grateful to the Vaccine Safety Datalink project for support of the data set that made this analysis possible.


   FOOTNOTES
 
Accepted Feb 20, 2008.

Address correspondence to Mari M. Nakamura, MD, MPH, Department of Ambulatory Care and Prevention 133 Brookline Avenue, 6th Floor Boston, MA 02115. E-mail: mari.nakamura{at}childrens.harvard.edu

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


What's Known on This Subject

Although some studies have described aggregate influenza vaccination rates that include adolescents, none has focused specifically on this age group. Studies have demonstrated that influenza vaccination coverage among children and adolescents with high-risk conditions is low.

 

What This Study Adds

We describe influenza vaccination rates in adolescents with high-risk conditions and evaluate changes in coverage over a recent 11-year period. We also assess individual year-to-year vaccination continuity and missed opportunities in this population.

 


   REFERENCES
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 METHODS
 RESULTS
 DISCUSSION
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