Asthma, a chronic inflammatory disease of the respiratory

Transcription

1 original Research Improving Influenza Vaccine Coverage Among Asthmatics: A Practice-Based Research Network Study Emmanuel B. Walter, MD, MPH, Anne S. Hellkamp, MS, Kenneth C. Goldberg, MD, Debra Montgomery, RN, MSN, Beth Patterson, RN, BSN, and Rowena J. Dolor, MD, MHS Abstract Objective: To evaluate an educational postcard reminder and practice improvement interventions intended to improve influenza vaccination rates among asthmatic patients. Design: Pre post study. Patients and setting: Patients with asthma followed at 15 primary care practices located in central North Carolina. Measurements: Vaccine coverage was assessed utilizing 3 sources of immunization information: an administrative database containing immunization order and billing data, a mailed postcard survey, and an in-office handheld computer survey. Changes in vaccine coverage were compared between 8 intervention practices and 7 nonintervention practices. Results: In , the influenza vaccine coverage rates as assessed by the 3 respective methods were 23%, 78%, and 45%, and in they were 26%, 77%, and 58%. In both years, vaccine coverage did not improve with the addition of the educational message to the postcard reminder. The mean change in vaccine coverage in the practice intervention sites was +4.5%, compared with +4.0% in control practices (p = 0.55). Vaccine coverage was lower among nonwhites (p = 0.001), the uninsured (p = 0.001), and young adults (p = 0.001). Of those not receiving influenza vaccine, nearly half had concerns that the vaccine would cause the flu. Conclusions: Influenza vaccine coverage among asthmatics remains suboptimal. Neither the educational reminder nor the practice improvement strategy employed significantly influenced vaccine coverage rates in this study. Alternative strategies towards increasing influenza vaccine coverage among asthmatics should address continued misconceptions about the influenza vaccine. Asthma, a chronic inflammatory disease of the respiratory system, occurs in approximately 7% of the United States population [1]. Respiratory infections can cause significant morbidity in persons with asthma such that during times when influenza is the predominant circulating virus in the community, the rate of hospitalization for acute respiratory infections is higher among children with asthma when compared with healthy children [2,3]. The primary means for controlling influenza among adults and children is influenza vaccination, the safety of which has been demonstrated in a large randomized clinical trial of asthmatics [4,5]. In order to prevent medical complications and hospitalizations associated with influenza, annual influenza vaccination is recommended for persons with asthma [5]. Even with recommendations for use and its established safety in asthmatics, influenza vaccination remains largely underutilized in asthmatic children and young adults. In the year prior to initiating the current study, we examined computerized billing data for 15 primary care practices in the Duke University Health System and determined that 12.6% of asthmatics received an influenza vaccine. Previously reported influenza vaccine coverage rates among asthmatic children are as low as 9% and have been reported to be as high as 32% after the introduction of a computerized reminder system [6,7]. Although racial and ethnic disparities exist with respect to influenza vaccine coverage in elderly populations, similar disparities have not been described in asthmatic adults and children [8]. The Healthy People 2010 objective is 60% influenza vaccine coverage for high-risk persons aged younger than 65 years [9]. Because both our regional as well as the national experience From the Duke Children s Primary Care, Department of Pediatrics, Duke University Medical Center, Durham, NC (Dr. Walter); Duke Clinical Research Institute, Duke University Medical Center (Dr. Walter, Ms. Hellkamp, Ms. Montgomery, Ms. Patterson, and Dr. Dolor); and Durham Veterans Affairs Medical Center and Division of Internal Medicine, Department of Medicine, Duke University Medical Center (Drs. Goldberg and Dolor). Vol. 15, No. 5 May 2008 JCOM 227

2 influenza Vaccine coverage fell well short of these goals, during this 2-year study we sent all identified asthmatic patients a postcard vaccine reminder. Reminders have been shown to be an effective means of improving influenza vaccine coverage [7,10 12]. In our study, we elected to evaluate the addition of a safety message about influenza vaccine to the standard vaccine reminder as well as the implementation of a practice improvement process to enhance influenza vaccination rates among asthmatic patients cared for across a primary care network. Methods Study Design During and , asthmatic patients cared for in 15 primary care practices belonging to the Duke University Health System were individually randomized to receive either a postcard reminder or a postcard reminder with an additional educational message about the safety of influenza vaccine in asthmatics. Randomization was stratified by practice; within each practice, patients were randomly assigned to postcard type in a 1:1 ratio. Influenza vaccine coverage rates were compared between those receiving the reminder alone and those receiving the reminder with the additional educational message. In the second year, 8 practices were designated to implement a strategy to increase influenza immunization rates for their asthmatic patients. Improvement in vaccine coverage was compared between the medical offices implementing the practice improvement intervention and control offices. An office-based handheld computer survey of a convenience sample of asthmatic patients was also conducted to measure receipt of influenza vaccine and barriers to influenza vaccine use. Study Population Nine family medicine practices, 4 internal medicine practices, and 2 pediatric practices were among 15 Duke University Health System primary care practices included in this study. An administrative computerized database (IDX) for registration and billing common to the primary care practices was used to identify patients with a diagnosis of asthma (ICD-9 codes ) during the 2-year period prior to the study start. We restricted our sample to patients who were living within the state of North Carolina and who were not living in institutions (eg, prison, orphanage). Where multiple members of a household were asthmatic and went to the same practice, 1 asthmatic member was selected at random by sorting the household members alphabetically by name and selecting the first one for inclusion in the sample. In addition, demographic information, site of primary medical care, and health insurance status were obtained from IDX. Study Procedures Patient randomization. Asthmatics were randomized prior to the first influenza vaccination season to receive either a regular postcard reminder about influenza vaccination or a postcard reminder about influenza vaccination that also contained the following educational statement: A recent national study by the American Lung Association showed that influenza vaccination does not worsen symptoms associated with asthma. Patients received the same kind of postcard before each influenza vaccination season ( and ). Health care providers and practice managers were informed that their patients would receive a postcard reminder about influenza vaccination. Reminders were mailed on 27 November and 4 November during each of the respective study years. Patients who died or moved out of state between the 2 study years (n = 117) were omitted from the second year s mailing list. Practice improvement intervention. Prior to the start of the influenza vaccination season, 8 of the primary care practices (4 family medicine, 2 internal medicine, and both pediatric), were selected to participate in a practice improvement process to increase influenza immunization rates. Geographic locale, the possibility for cross-contamination of information among medical offices, and baseline immunization coverage rates were used hierarchically to determine practice assignments. Assignment to the intervention or control group was stratified by tertiles of the practices immunization coverage rate. Before the influenza immunization season, practice-specific and aggregate coverage rates for influenza vaccination were shared with the 8 intervention practices. Perceived barriers to influenza immunization were discussed at each intervention practice. At a face-to-face meeting with the study staff, intervention practices were presented with an established list of options for office-based interventions [13,14] and were requested to select at least 1 strategy for improving the practice-specific influenza immunization rate (Table 1). Measurement of influenza vaccine coverage. Immunization coverage rates during the 2 seasons were measured using the administrative (IDX) database and by a mailed survey. The IDX database identified influenza immunization by current procedural terminology (CPT) codes 90657, 90658, and in with the addition of CPT codes and in Patients whose reminder postcards were returned by the postal service as undeliverable were not included in the IDX database (n = 374, season and n = 394, season). For purposes of this study, a single dose of influenza vaccine received by an influenza vaccine naive child fulfilled the requirement for vaccine coverage. After each influenza immunization season, a postcard with a detachable postage-paid, return-addressed survey 228 JCOM May 2008 Vol. 15, No. 5

3 original Research Table 1. Office-Based Interventions for Enhancing Influenza Immunization Rates and Rate Changes in Intervention Versus Control Practices Intervention Practices Proposed Interventions Standing vaccine orders in the office Chart reminders + Patient educational materials (posters, flyers) /+ + + Personal health records Computerized record reminders Mail or telephone reminders Performance feedback Home visits Expanded access in clinical settings (evening or weekend clinics) Increase in influenza vaccine coverage to , % + Intervention practices Control practices = already in use in practice; + = implemented as part of the study. response card was mailed to a random sample of 2000 asthmatic patients who were sent a mailed vaccine reminder during the previous fall. Randomization was performed within postcard type group, with 1000 selected from each postcard type. Response cards were anonymous and coded so that only the intervention group and site of primary care were identifiable. In the second year of the study, a second random sample of 2000 asthmatic patients not including any of the first year s 2000 patients was selected and mailed the survey response cards. The survey ascertained influenza vaccination status during the previous season as well as the location where vaccine was obtained. Handheld computer survey. After each vaccination season, 2 handheld computers were placed in each of the 8 intervention practices to anonymously survey a convenience sample of asthmatics or parents of asthmatic patients. Medical office staff was trained to assist patients in completing the survey. The handheld computer survey, including an informational sheet explaining the study, was distributed to asthmatic patients or parents of asthmatic patients at the time of a health maintenance visit or an acute or chronic illness visit. If more than 1 asthmatic family member presented for a visit, the family was asked to complete the survey for the oldest member present. Patients and parents were instructed not to complete the survey if they had previously done so. The handheld computers were programmed with survey information that included information about influenza vaccine use and barriers to influenza vaccine use. Survey data from the handheld computers were downloaded on a regular basis to a central database. Human subjects. The institutional review board of Duke University Medical Center approved the protocol and the data collection instruments, including the postcard survey and the content of the handheld computer survey. All survey information was obtained anonymously and written informed consent was not obtained. Statistical analysis. Chi-square tests were used to compare influenza vaccine coverage rates among different asthmatic groups. A multivariable logistic regression model was used to relate receipt of an influenza vaccine to multiple predictor variables. All variables were entered into the model simultaneously. Candidate predictors were race (white vs. nonwhite), gender, postcard type, and insurance type (categorized as Medicaid, Medicare or private, and uninsured). The linearity of the relationship between age and probability of vaccination was assessed, and the best fit to the data (a 3-part linear spline function with knots at 26 and 73 years) was used in the model. Mean change in vaccine coverage between seasons across all sites was calculated as the average of the individual site vaccine coverage changes. Mean changes in vaccine coverage were compared between practice intervention sites and control sites using an exact stratified normal scores (Van der Waerden) test. Analyses were conducted using SAS version 8.2 (SAS Institute, Cary, NC) except for the normal scores test, which Vol. 15, No. 5 May 2008 JCOM 229

4 influenza Vaccine coverage Table 2. Influenza Vaccine Coverage by Demographic Variables and Health Insurance Status* Study Population, n (%) Influenza Vaccine Coverage Rate, % Age 6 months 2 years 296 (3) years 5761 (65) years 1784 (20) > 65 years 1071 (12) Gender Male 3263 (37) Female 5649 (63) Race/ethnicity White 4566 (51) Black 2507 (28) Hispanic 66 (1) Asian 67 (1) Native American 16 (< 1) Other 96 (1) Unknown 1594 (18) Health insurance Medicaid 885 (10) Medicare 1388 (16) Private 6327 (71) Uninsured 140 (2) Unknown 172 (2) *As determined from administrative database. was conducted with StatXact v (Cytel Software Corp., Cambridge, MA). Results Patient Demographics A total of 8912 asthmatics were sent postcard reminders during and, of these, 8355 were sent reminders during the subsequent season. Of those sent reminders, approximately half, 4440 and 4154 respectively, received a reminder with an added educational message during each influenza vaccination season. At the start of the study, the mean age of the asthmatic patients was 38 years. Nearly two thirds of the asthmatic population were female (Table 2). Influenza Vaccine Coverage For each of the study years, the influenza vaccine coverage rate as determined by IDX was 23% and 26% (Figure 1). The vaccine coverage rate did not vary by type of vaccine reminder when analyzed for both the entire vaccination season or for the period after the vaccine reminder was mailed. During both study years among asthmatics who received influenza vaccine, approximately 40% received their vaccination by the end of October and 80% received an influenza vaccine by the end of November. In , approximately 8% of the vaccinated asthmatics received their influenza shot after 31 December, while in virtually all vaccines were given before 31 December. The postcard survey response rate during both years was 26%. Of those who responded, over three quarters reported that they had received an influenza vaccine. As observed with the IDX vaccine coverage data, variation in vaccine coverage was not observed by the type of vaccine reminder. During both years, approximately 40% reported receiving their influenza vaccine at a location other than at their primary medical doctor s office. During and , locations for receipt of influenza vaccination other than the primary medical doctor s office were place of employment or work (18% both seasons), health department (6% and 4%), another doctor s office (4% and 5%), pharmacy or drug store (3% and 2%), grocery store (2% both seasons), and other (8% and 7%). Practice Intervention Interventions chosen by the 8 intervention practices incorporated patient education (n = 6), mail or phone reminders (n = 3), expanded access (n = 1), and chart reminders (n = 1) (Table 1). The mean (standard deviation) increase in the influenza vaccine coverage between seasons across all sites was 4.3% (3.8%). Practice intervention sites had a mean increase of 4.5% (3.2%) and control sites had a mean increase of 4.0% (4.6%) (p = 0.55, exact stratified normal scores test) (Table 1). There was more variation in improvement among the control sites than among practice intervention sites. Demographic Predictors of Influenza Vaccine Coverage During both seasons, influenza vaccine rates did not vary significantly according to gender (Table 2). Vaccination rates were consistently higher in whites when compared with either blacks or nonwhites (p < for both comparisons). Vaccine coverage was also uniformly higher for asthmatic patients with Medicare when compared with asthmatics with private insurance, Medicaid, or no insurance (p < for all comparisons). In both years, patients with either Medicaid or private insurance had comparable vaccination rates. Uninsured asthmatics had lower rates of vaccine coverage when compared with asthmatics with Medicaid (p < and p < 0.01, for respective seasons) or private health insurance (p < and p < 0.025, for respective seasons). Those older than 65 years had the highest rates of coverage when compared individually with each of the other age-groups (p < for all comparisons), except during the second year of the study when the coverage rate for children under 3 years of age was comparable. 230 JCOM May 2008 Vol. 15, No. 5

5 original Research Educational reminder Regular reminder All asthmatics Educational reminder Handheld survey Postcard survey Database, entire season Database, after reminder mailed Figure 1. Influenza vaccine coverage rates as measured by 3 different methods during 2 vaccination seasons Regular reminder All asthmatics Coverage rate, % Table 3. Multivariable Logistic Regression Model with Influenza Vaccination as an Outcome for Season Variable* P Odds Ratio 95% CI Age Health insurance ( ) ( ) ( ) ( ) ( ) For each 5-year increase from 1 26 years For each 5-year increase from years For each 5-year increase above 73 years For Medicare vs. Medicaid/private For Medicare vs. uninsured or unknown 1.76 ( ) For Medicaid/private vs. uninsured or unknown Race/ethnicity ( ) For white vs. all other races Gender ( ) For female vs. male Reminder ( ) For educational vs. regular CI = confidence interval. *All variables entered into model simultaneously. For the influenza season, after adjusting for site in a multivariable logistic regression model with vaccination as the outcome, significant predictor variables included white race when compared with nonwhites (odds ratio [OR], 1.28) and female gender (OR, 1.17) (Table 3). Probability of receiving a vaccine varied with age, decreasing from age 1 to 26 years (OR, 0.76 for each 5 years older), increasing from age 26 to 73 years (OR, 1.28), and decreasing thereafter (OR, 0.69) (Figure 2). Patients with Medicare were more likely to be vaccinated than those with private insurance or Medicaid (OR, 1.26). Asthmatics with Medicare and asthmatics with private insurance or Medicaid were more likely to vaccinated than those who were uninsured or where insurance was not specified (OR, 2.21 and 1.76, respectively). The type or postcard reminder remained nonsignificant as a predictor of influenza vaccination. Multivariable logistic regression results for the influenza season were essentially the same (data not shown). Handheld Computer Survey During , 118 adult asthmatics and 169 parents of asthmatic children answered the handheld computer survey, while responses were given by 57 and 50, respectively, in year 2. Vaccine coverage rates were 45% and 58% during the consecutive seasons. The location of receipt of influenza vaccine reported by adult asthmatics was the primary care provider s office (51%), place of employment (28%), or another physician s office (6%). The proportion of parents responding that their child received influenza vaccine at their primary care provider s office dropped from 93% to 81% between the study years, with up to 16% of children receiving their influenza vaccine at the health department Vol. 15, No. 5 May 2008 JCOM 231

6 influenza Vaccine coverage Vaccination rate Number of patients Age, yr Figure 2. Influenza vaccination rate by age during in year 2. The most common reason reported by asthmatics for not receiving an influenza vaccine was the belief that the influenza shot could cause the flu (Figure 3). Eight percent of patients who did not receive an influenza vaccine reported that they were allergic to eggs. Discussion Influenza vaccine coverage rates were not significantly affected by either the addition of the safety message to the postcard reminder or by the practice improvement intervention evaluated in our study. Notwithstanding the lack of effect of our study interventions, influenza vaccine coverage among the asthmatic population in this study was at least 10% higher in both years of the study than what we historically observed in the same population the year before the study started. It remains unclear if the higher coverage rates observed during the study were due to the postcard reminders sent to the entire study population or to other unmeasured factors. The present study differed significantly from a previous study that also tailored interventions to improve influenza vaccination rates to individual practice sites [15]. The previous 2-year study noted improvements in influenza vaccination rates among high-risk inner-city children followed at intervention clinic sites. In contrast to the previous study, our study included both adult and pediatric populations and limited the high-risk population to patients with asthma. Dissimilarly, we allowed the practices to manage the intervention without the direct assistance of research staff and without additional financial support. Furthermore, the previously reported study included only a single control practice site with a high baseline coverage rate, whereas our study included multiple control practice sites and controlled for baseline coverage rates. In our study, we observed several health disparities among asthmatics with respect to influenza vaccine coverage. We noted a dramatic decline in influenza vaccine coverage during adolescence, which persisted into the third decade. Because adolescents often do not seek preventive health care, they pose a particular challenge with respect to achieving high vaccine coverage rates [16]. On the other hand, universal influenza vaccination recommendations for children aged 6 to 23 months and for adults over age 50 years likely influenced the higher levels of coverage noted among asthmatics in these age-groups. Our study also documented lower influenza vaccine coverage rates among nonwhite and uninsured asthmatics. This study was conducted during the course of 2 influenza vaccination seasons, the second of which began earlier than many seasons and was moderately severe [17]. The fall 2003 influenza epidemic attracted intense media coverage, leading to an increase demand for influenza vaccine and local disruptions in the supply of vaccine due to a rapid depletion of available vaccine. The effects of high vaccine demand and regional 232 JCOM May 2008 Vol. 15, No. 5

7 original Research Causes flu Makes sick Pediatric Adult Worsens asthma Not offered Will not get flu Does not work Figure 3. Reasons given for not receiving influenza vaccine as reported by convenience sample of asthmatic patients in a handheld self-administered survey. Fear Percentage of patients vaccine shortages were demonstrated during year 2 of our study by the increased number of children receiving vaccine at the health department and by the fact that influenza vaccine was not received after December. The consequences of the intense media coverage and subsequent vaccine shortages on the vaccine coverage are unclear. Media coverage likely worked to increase vaccine coverage, while regional vaccine supply problems decreased coverage. In the handheld survey, we detected a shift in location of influenza vaccination to the public health sector, which has been described by other investigators during times of vaccine shortage [18]. During the 2004 influenza vaccine shortage, more high-risk younger adults sought vaccination at their primary care provider s office, while during the 2000 vaccine shortage, providers described that more elderly persons received their vaccine at senior citizen centers or at community clinics [19,20]. Our study demonstrates that the method by which vaccine coverage is measured yields discrepant results. The use of the administrative database likely underestimated vaccine coverage, as over 40% of those who received vaccine as reported by both the postcard and handheld computer surveys received influenza vaccine at a place other than their primary provider s office. On the other hand, the higher vaccine coverage rates ascertained by the postcard survey and to a lesser extent the handheld computer survey reflect response bias. Furthermore, our handheld computer survey assessed vaccine coverage in a convenience sample of asthmatics, omitting those who do not receive regular health care and therefore may not be representative of the asthmatic population. For those patients who did respond to the handheld computer survey, self-report of influenza vaccination is both a sensitive and specific measure for determining vaccine coverage [21]. National influenza vaccine coverage rates as determined by self-report or parental report in a recent telephone interview were 26% among adults aged 18 to 64 years with at least 1 high-risk condition and 35% among children aged 2 to 17 years with 1 or more high-risk medical conditions [22]. Among the unvaccinated who answered the handheld computer survey, the most frequent reason cited for not receiving the influenza vaccine was the perception that the vaccine causes the flu (39% pediatric, 48% adult). Similarly, concerns regarding vaccine side effects remained prevalent. Because the handheld computer survey was anonymously administered, we were unable to assess the effect of the educational message about influenza vaccine safety with respect to the worry that the vaccine would worsen asthma. Future efforts for increasing influenza vaccine acceptance need to be directed towards dispelling public misperceptions about influenza vaccine. Health care providers, public officials, and influential personalities need to deliver the message that influenza vaccine is safe and does not cause influenza. In summary, our practice-based intervention and educational safety message were not successful strategies towards increasing influenza vaccine coverage. Despite historical successes, utilization of vaccine reminders is variable and will probably not lead to the 60% coverage target established by Healthy People Furthermore, targeting high-risk groups has failed with other immunization programs, and achieving high levels of influenza vaccine coverage in high-risk groups is a challenge not yet met [23]. Anticipated increases in influenza vaccine supply in upcoming seasons will allow for a universal approach to influenza vaccination. A universal approach to influenza immunization will decrease confusion about defining at-risk populations and could potentially decrease missed opportunities for vaccination by health care providers. In addition, programs designed to enhance influenza vaccine accessibility, such as school- and work-based Vol. 15, No. 5 May 2008 JCOM 233

8 influenza Vaccine coverage immunization clinics, could help to increase overall coverage rates and potentially decrease the health disparities we observed in our study. Acknowledgments: We thank the following practices for their participation: Butner-Creedmoor Family Medicine, Duke Children s Primary Care, Duke Family Medicine, Duke General Internal Medicine, Durham Medical, Durham Pediatrics, Family Medical Associates of Durham, Harps Mill Internal Medicine, Henderson Family Medicine, Hillsborough Family Practice, Metropolitan Durham Medical, Oxford Family Physicians, Timberlyne Family Medical Center, Triangle Family Practice, and Wake Forest Family Physicians. Study staff responsible for assisting with data collection include Lisa Atkinson, RN, Kathy Chmielewski, Lynn Harrington, RN, and Leslie Walker, RN. Corresponding author: Emmanuel B. Walter, MD, MPH, Duke Children s Primary Care Clinic, 4020 N. Roxboro Rd, Durham, NC 27704, walter002@mc.duke.edu. Funding/support: Agency for Healthcare Research and Quality grant R21HS Financial disclosures: Dr. Walter is a speaker for sanofi pasteur and has conducted clinical trials funded by sanofi pasteur. Author contributions: conception and design, EBW, RJD; analysis and interpretation of data, EBW, ASH, RJD; drafting of article, EBW, ASH; critical revision of the article, EBW, KCG, RJD; provision of study materials or patients, EBW; statistical experience, ASH; obtaining of funding, EBW, RJD; administrative or technical support, EBW, KCG, DM, BP; collection and assembly of data, EBW, DM, BP. References 1. Centers for Disease Control and Prevention (CDC). Selfreported asthma prevalence among adults United States MMWR Morb Mortal Wkly Rep 2001;50: Glezen WP, Greenberg SB, Atmar RL, et al. Impact of respiratory virus infections on persons with chronic underlying conditions. JAMA 2000;283: Neuzil KM, Wright PF, Mitchell EF Jr, Griffin MR. 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All rights reserved. 234 JCOM May 2008 Vol. 15, No. 5