- Email: [email protected]
Asthma and Influenza Vaccination
clinical investigations Asthma and Influenza Vaccination* Findings From the 1999 –2001 National Health Interview Surveys Earl S. Ford, MD, MPH; David M. Mannino, MD, FCCP; and Seymour G. Williams, MD
Study objectives: People with asthma are at high risk for complications from influenza; therefore, the Centers for Disease Control and Prevention recommends an annual influenza vaccination for people with asthma. Because little is known about such vaccination rates among adults, especially those aged 18 to 49 years and 50 to 64 years, we sought to estimate influenza vaccination rates among US adults. Design: Cross-sectional analyses of the 1999 to 2001 National Health Interview Surveys. Setting: US population. Participants: Representative samples of US adults aged > 18 years. Measurements and results: Asthma status and receipt of influenza vaccination during the past 12 months were self-reported. We found that 35.1% (95% confidence interval [CI], 33.0 to 37.0%), 36.7% (95% CI, 34.7 to 38.6%), and 33.3% (95% CI, 31.6 to 35.0%) of participants with asthma reported having had an influenza vaccination in 1999 (n ⴝ 2,620), 2000 (n ⴝ 3,007), and 2001 (n ⴝ 3,582), respectively. Among participants aged 18 to 49 years, the vaccination rates were 20.9% (SE 1.2%), 22.7% (SE 1.2%), and 21.1% (SE 1.0%), respectively. Among participants aged 50 to 64 years, the vaccination rates were 46.2% (SE 2.6%), 47.8% (SE 2.3%), and 42.3% (SE 2.1%), respectively. Vaccination rates increased strongly with age and with education in each year. Associations with sex or with race or ethnicity were inconsistent during the 3 years. Conclusions: The suboptimal vaccination rates among people with asthma aged 18 to 64 years suggest the need to increase influenza vaccination rates in this age group. (CHEST 2003; 124:783–789) Key words: asthma; health surveys; influenza; vaccination Abbreviations: CI ⫽ confidence interval; NHIS ⫽ National Health Interview Surveys; SE ⫽ standard error
health burden attributable to asthma in T hethepublic United States is considerable and is growing.1 In 2000, data from the Behavioral Risk Factor Surveillance System suggested that 14.6 million US
adults had current asthma.2 In 1998, the estimated cost of asthma was $12.7 billion.3 The public health burden of influenza is also enormous, and this For editorial comment see page 775
*From the Division of Environmental Hazards and Health Effects, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA. Manuscript received November 26, 2002; revision accepted March 21, 2003. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (e-mail: [email protected]). Correspondence to: Earl Ford, MD, MPH, Centers for Disease Control and Prevention, 4770 Buford Highway NE, Mailstop K66, Atlanta, GA 30341; e-mail: [email protected] www.chestjournal.org
disease accounts for an average of 20,000 deaths each year.4,5 In 2000, influenza and pneumonia were the seventh-leading cause of mortality in the United States.6 Upper respiratory tract infections are an important trigger of asthma and an important source of morbidity and mortality among persons with asthma.7,8 Influenza is a major cause of these upper respiratory CHEST / 124 / 3 / SEPTEMBER, 2003
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tract infections9; however, significant reductions in the morbidity and mortality associated with influenza can be achieved through vaccination.10,11 In 1997, the National Asthma Education and Prevention Program guidelines recommended that only people with persistent asthma receive annual vaccinations.12 For some time, the Centers for Disease Control and Prevention has recommended that persons with asthma receive annual influenza vaccinations.13 Despite these recommendations, influenza vaccine rates among children with asthma are low (9 to 25%).14 –19 Little is known, however, about the vaccination rates of adults with asthma, who are considered a high-risk group. Results from the Behavioral Risk Factor Surveillance System showed that vaccination rates for all adults aged ⱖ 65 years, an age group in which all adults should be vaccinated, were 65.6% in 1997 and 66.9% in 1999, but rates for participants with asthma of the 1999 survey were not provided.20,21 To examine the prevalence of influenza vaccinations among people with asthma, we examined data from the 1999-2001 National Health Interview Surveys (NHIS). Materials and Methods Since the early 1960s, a sample of the US population has participated in the NHIS. One adult per family was selected and asked to complete the sample adult questionnaire. AfricanAmerican and Hispanic populations were oversampled. Census interviewers conducted interviews with respondents in person. Participants were asked to complete a core set of questions, which has remained relatively constant from year to year, and to complete special supplements, which vary considerably each year. The numbers of adults aged 18 to ⬎ 85 years who were selected using a multistage sampling design and participated in the survey were 30,801 in 1999, 32,374 in 2000, and 33,326 in 2001. The final response rates for the sample adult questionnaires were 69.6% in 1999, 72.1% in 2000, and 73.8% in 2001. Details of the methods from 1999 to 2001 NHIS may be found elsewhere.22–24 Participants were asked, “Have you ever been told by a doctor or other health professional that you had asthma?” and “During the past 12 months, have you had an episode of asthma or asthma attack”? In addition, participants were asked, “During the past 12 months, have you had a flu shot?” Self-reported asthma status has
acceptable sensitivity and specificity when compared with more rigorous methods of defining asthma.25–27 We examined by age, sex, race or ethnicity, and educational attainment the percentages of participants with asthma who reported having an influenza vaccination. Direct age adjustment was performed using the age structure of the year 2000 US population aged ⱖ 18 years. We used logistic regression analysis to examine the independent associations of sociodemographic variables with vaccination status. Analyses were conducted with Software for the Statistical Analysis of Correlated Data (SUDAAN; Research Triangle Institute; Research Triangle Park, NC) to produce valid estimates of the variance.28 Estimates were calculated using sampling weights.
Results After excluding participants with missing values for the study variables, 29,981 participants (2,620 with asthma) were included in the analysis in 1999, 31,635 participants (3,007 with asthma) in 2001, and 32,572 participants (3,582 with asthma) in 2001. In all 3 years, participants with asthma were younger and more likely to be women than participants without asthma (Table 1). In 2000 and 2001, participants with asthma were also more likely to be white than those without asthma. Educational attainment was similar for the two groups. Overall, the percentage of participants with asthma who reported having received an influenza vaccination was 35.1% (95% confidence interval [CI], 33.0 to 37.0%) in 1999, 36.7% (95% CI, 34.7 to 38.6%) in 2000, and 33.3% (95% CI, 31.6 to 35.0%) in 2001 (Table 2). These percentages were significantly higher than those among participants without asthma in all 3 years (p ⬍ 0.001 in each year). Among participants with asthma, the percentages who reported having been vaccinated were 20.9% (standard error [SE] 1.2%) among participants aged 18 to 49 years, 46.2% (SE 2.6%) among participants aged 50 to 64 years, and 72.8% (SE 2.4%) among participants aged ⱖ 65 years in 1999. In comparison, these percentages among participants without asthma were 16.0% (SE 0.4%), 33.1% (SE 0.7%), and 65.2% (SE 0.8%), respectively. In 2000, these percentages were 22.7% (SE 1.2%), 47.8% (SE
Table 1—Unadjusted Means or Percentages of Selected Sociodemographic Variables Among Participants Aged > 18 Years, by Self-Reported Asthma Status, NHIS 1999 –2001* 1999
2000
2001
Variables
Asthma (n ⫽ 2,620)
No Asthma (n ⫽ 27,361)
p Value
Asthma (n ⫽ 3,007)
No Asthma (n ⫽ 28,628)
p Value
Asthma (n ⫽ 3,582)
No Asthma (n ⫽ 28,990)
p Value
Mean age, yr Male gender White race Less than high school
42.0 (0.4) 39.9 (1.2) 82.9 (0.9) 17.9 (0.9)
45.1 (0.2) 48.6 (0.4) 82.6 (0.4) 17.9 (0.3)
⬍ 0.001 ⬍ 0.001 0.761 0.941
43.1 (0.4) 41.4 (1.1) 76.9 (0.9) 18.8 (0.9)
45.1 (0.2) 48.5 (0.3) 73.9 (0.4) 17.9 (0.3)
⬍ 0.001 ⬍ 0.001 0.001 0.325
42.4 (0.3) 41.2 (1.0) 76.6 (0.8) 17.1 (0.8)
45.3 (0.1) 48.8 (0.3) 73.4 (0.4) 17.6 (0.3)
⬍ 0.001 ⬍ 0.001 ⬍ 0.001 0.557
*Data are presented as % (SE). 784
Clinical Investigations
Table 2—Age-Specific and Age-Adjusted Percentage of Participants Aged > 18 Years Who Reported Receiving an Influenza Vaccination During the Previous Year, by Self-Reported Asthma and Selected Sociodemographic Variables, NHIS 1999 –2001* 1999 Variables Total Age, yr 18–29 30–39 40–49 50–59 60–69 ⱖ 70 Sex Men Women Race or ethnicity Hispanic White African American Other Education Less than high school High school graduate or GED Some college or bachelor’s degree Graduate degree
2000
2001
Asthma (n ⫽ 2,620)
No Asthma (n ⫽ 27,361)
Asthma (n ⫽ 3,007)
No Asthma (n ⫽ 28,628)
Asthma (n ⫽ 3,582)
No Asthma (n ⫽ 28,990)
35.1 (1.0)
27.9 (0.3)
36.7 (1.0)
28.0 (0.3)
33.3 (0.9)
25.9 (0.3)
17.7 (1.9) 18.0 (2.0) 28.3 (2.4) 41.7 (2.9) 61.2 (3.3) 75.7 (2.7)
13.6 (0.6) 14.6 (0.5) 19.8 (0.7) 30.1 (0.8) 48.8 (1.0) 68.6 (0.9)
15.7 (1.6) 24.8 (2.1) 31.0 (2.3) 46.3 (2.5) 55.9 (3.7) 75.1 (2.3)
13.1 (0.6) 15.2 (0.5) 21.6 (0.7) 30.3 (0.9) 48.3 (1.0) 66.8 (0.8)
17.0 (1.5) 17.9 (1.6) 30.2 (2.0) 41.0 (2.5) 51.7 (3.3) 68.4 (2.7)
11.3 (0.5) 13.9 (0.5) 17.8 (0.6) 27.7 (0.8) 48.4 (1.0) 65.0 (0.8)
35.1 (1.7) 34.8 (1.2)
27.3 (0.4) 28.4 (0.4)
34.1 (1.5) 38.3 (1.2)
27.5 (0.4) 28.5 (0.4)
34.3 (1.4) 32.6 (1.0)
25.6 (0.4) 26.3 (0.4)
37.0 (2.9) 34.7 (1.2) 31.3 (3.0) 43.7 (5.5)
22.4 (0.9) 29.0 (0.4) 23.0 (0.8) 29.3 (1.7)
34.4 (2.6) 37.9 (1.2) 27.2 (2.4) 44.4 (4.5)
21.9 (0.8) 29.3 (0.4) 21.1 (0.6) 29.6 (1.8)
25.2 (2.4) 34.2 (1.0) 26.2 (2.0) 50.7 (5.1)
20.9 (0.8) 27.0 (0.3) 21.8 (0.8) 23.9 (1.4)
30.6 (2.2) 35.1 (1.8) 34.7 (1.7) 41.6 (3.2)
23.6 (0.6) 25.7 (0.5) 30.1 (0.4) 33.8 (1.1)
30.0 (2.2) 34.8 (1.8) 39.5 (1.5) 42.3 (3.1)
21.9 (0.6) 26.3 (0.5) 29.8 (0.5) 38.1 (1.2)
27.6 (2.1) 30.2 (1.5) 36.5 (1.2) 43.5 (4.0)
20.8 (0.6) 24.5 (0.5) 27.7 (0.4) 33.1 (1.2)
*Data are presented as % (SE). GED ⫽ general equivalency diploma.
2.3%), and 71.2% (SE 2.3%) among participants with asthma, and 16.6% (SE 0.4%), 33.3% (SE 0.8%), and 63.8% (SE 0.8%) among participants without asthma. In 2001, these percentages were 21.1% (SE 1.0%), 42.3% (SE 2.1%), and 64.8% (SE 2.4%) among participants with asthma, and 14.3% (SE 0.4%), 31.0% (SE 0.7%), and 62.8% (SE 0.7%) among participants without asthma. In each year, the percentage of participants with asthma who reported receiving an influenza vaccination increased strongly with age (Table 2). Vaccination rates were similar for men and women in 1999 and 2001. Participants with race or ethnicity designated as “other” showed the highest rate of vaccination. The vaccination rate progressively increased with higher educational attainment. To examine the associations between age, sex, race or ethnicity, and education and vaccination status among participants with asthma, we used multiple logistic regression analysis (Table 3). Age and education were significantly, independently, and positively associated with vaccination status in each year. In 2000, men were less likely to report having been vaccinated than women, and African-American participants were less likely to report having been vaccinated than white participants. In 2001, Hispanic participants were significantly less likely and participants with a race or ethnicity designated as other www.chestjournal.org
were significantly more likely to report having been vaccinated than white participants.
Discussion The results from this study indicate that only about one in three people with asthma are receiving influenza vaccinations. This vaccination rate has changed little from 1999 through 2001. These results suggest that recommendations to vaccinate adults with asthma are not being met. In particular, younger people with asthma are not being vaccinated against influenza. Only approximately one in five people with asthma aged 18 to 49 years reported having received such a vaccination. Respiratory infections, including influenza, can cause serious morbidity in people with asthma.29,30 Some evidence suggests that people with asthma may be more likely to experience influenza-associated morbidity than people who do not have asthma. For example, during periods when influenza virus was the predominant circulating upper respiratory virus, hospitalization rates for acute respiratory infections among children with asthma were much higher than those among children without a high-risk condition.31 These considerations taken together with the fact that inactivated influenza vaccine has CHEST / 124 / 3 / SEPTEMBER, 2003
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Table 3—Associations Between Selected Sociodemographic Variables and Influenza Vaccination Status From Multiple Logistic Regression Analysis Among Adults With Asthma Aged > 18 Years, NHIS 1999 –2001* Variables Age, yr 18–29 (reference) 30–39 40–49 50–59 60–69 ⱖ 70 Sex Men Women (reference) Race or ethnicity Hispanic White (reference) African American Other Education, yr Less than high school (reference) High school graduate or GED Some college or bachelor’s degree Graduate degree
1999 (n ⫽ 2,620)
2000 (n ⫽ 3,007)
2001 (n ⫽ 3,582)
1.00 1.00 (0.70–1.45) 1.75 (1.22–2.50) 3.27 (2.32–4.60) 7.85 (5.36–11.50) 15.50 (10.21–23.52)
1.00 1.68 (1.21–2.33) 2.32 (1.70–3.16) 4.59 (3.34–6.31) 7.24 (4.94–10.60) 18.52 (12.98–26.43)
1.00 1.02 (0.76–1.39) 2.11 (1.60–2.79) 3.41 (2.58–4.51) 5.74 (4.07–8.10) 12.27 (8.68–17.35)
0.99 (0.79–1.24) 1.00
0.82 (0.67–0.99) 1.00
1.05 (0.88–1.25) 1.00
1.16 (0.84–1.58) 1.00 1.02 (0.70–1.50) 1.63 (0.86–3.08)
0.97 (0.71–1.33) 1.00 0.67 (0.50–0.88) 1.39 (0.81–2.39)
0.75 (0.56–0.99) 1.00 0.77 (0.59–1.01) 2.18 (1.28–3.70)
1.00 1.29 (0.93–1.78) 1.33 (0.97–1.80) 2.22 (1.50–3.28)
1.00 1.31 (0.95–1.79) 1.64 (1.21–2.21) 2.05 (1.39–3.02)
1.00 1.17 (0.89–1.53) 1.63 (1.23–2.16) 2.18 (1.43–3.33)
*Data are presented as odds ratio (95% CI). See Table 2 for expansion of abbreviation.
been shown to be both clinically effective and costeffective32—albeit not necessarily based on studies of participants with asthma—suggest that people with asthma could benefit considerably from receiving an influenza vaccine. Yet, a review of nine randomized trials noted that the benefits and risks of vaccination for patients with asthma were inconclusive.33 All but three trials had sample sizes ⬍ 100 participants. In these trials, both early and late outcomes (mortality, hospital admission, pneumonia, asthma symptom scores, lung function measurements, medical visits, number of rescue courses of corticosteroids) were examined. The authors called for additional trials of sufficient size to study the question of the benefits and adverse effects of influenza vaccination in people with asthma. Questions about the short-term safety of the vaccine among people with asthma may have been answered by a large, randomized trial34 of children and adults with asthma that was published after the review. In this trial,34 the administration of inactivated influenza vaccine did not affect the frequency of exacerbations of asthma during the 2 weeks following the vaccination. The cost-effectiveness of annually vaccinating all eligible people with asthma is unknown. The Healthy People 2010 objectives call for 90% of noninstitutionalized adults aged ⱖ 65 years and 60% of noninstitutionalized high-risk adults aged 18 to 64 years to receive an annual influenza vaccination.35 People with asthma are included in the high-risk designation. The NHIS data show that 20.9 to 22.7% of asthmatic participants aged 18 to 49 786
years, 42.3 to 47.8% of asthmatic participants aged 50 to 64 years, and 64.8 to 72.8% of asthmatic participants aged ⱖ 65 years received a vaccination from 1999 to 2001. Previous studies of people aged ⱖ 65 years who participated in the Behavioral Risk Factor Surveillance System showed that 65.5% in 1997 and 66.9% in 1999 reported receiving an influenza vaccination during the 12 months prior to their interview.20,21 No estimates were reported for asthma status in these reports, however. Although a number of studies have reported low influenza vaccination rates among children, the vaccination rates among adults have apparently received little study. In one study,36 however, the influenza vaccination rate for a small cohort of asthmatic patients with a mean age of 38 years ranged from 64 to 78% during three consecutive influenza seasons. Age was a strong predictor of vaccination status among participants with and without asthma. As people age and become more likely to acquire a health condition, they are probably more likely to be vaccinated against influenza because of these conditions. In addition, influenza vaccine recommendations were initially focused on people aged ⱖ 65 years. Consequently, many of the campaigns to remind people and clinicians of the importance of influenza vaccination were targeted at people in this age group. In more recent years, the recommended age of vaccination has been lowered. The fact that people with asthma were more likely to report being vaccinated than those without asthma in each age Clinical Investigations
group suggests that having asthma probably increased the likelihood of being vaccinated. Reasons for the low vaccination rates among people with asthma are multifactorial and pertain to both health-care providers and patients. Patients may be reluctant to be vaccinated because they believe they will contract influenza from the vaccination, or they do not perceive any value in it.37 Barriers for health-care providers may include reimbursement issues and lack of methods to help them readily identify the patients who require vaccination and who need to be contacted.37 For persons aged ⱖ 65 years, influenza vaccination is reimbursed by Medicare, but for persons aged 18 to 64 years, reimbursement may be less available. Furthermore, the extent to which health-care providers are aware of the recommendations to vaccinate all patients with asthma, barring contraindications, is unclear. For example, physician awareness of the Centers for Disease Control and Prevention recommendations was associated with higher vaccination rates of pregnant patients.38 Furthermore, differing vaccine recommendations may also be a source of confusion to health-care providers. Asthmatic patients may be reluctant to be vaccinated against influenza for several reasons. In addition to the usual barriers to vaccination (such as availability of vaccine, scheduling of appointments, convenience, and cost), people with asthma, especially younger ones, may not perceive a need or may not be aware of the need for such vaccinations. Others may be concerned about possible adverse effects of vaccinations on their asthma. Yet, influenza vaccination has been shown to be safe in children and adults.18,19,34 Patients with asthma are recommended to have regular follow-up visits for asthma (1- to 6-month intervals) to ensure that control of asthma is maintained.12 These visits provide important opportunities to administer influenza vaccine to patients with asthma or to remind them of the need to receive such vaccinations. Improving vaccination rates for many vaccines among adults has proved to be a challenge. Because of the many reasons for suboptimal vaccination rates, a variety of possible approaches to improving these rates have been reviewed.39 Although vaccine characteristics differ, the strategies and interventions that have been recommended to improve vaccine rates for other vaccines may be useful to improve vaccine rates among people with asthma. For example, sending computerized reminder letters has been shown to significantly improve influenza vaccination rates among children with asthma.16,40 A review of patient reminder/recall systems found them to be effective in increasing vaccination rates for a variety of diseases among both children and adults.41 Another www.chestjournal.org
review showed that audit and feedback were also effective in improving immunization rates.42 Although these recommendations are likely to improve vaccine rates among people with asthma, it is unclear whether strategies specifically targeted at people with asthma may be helpful. The most obvious limitation of this study is that all information, including asthma status and vaccination status, are based on self-reports. Self-reported vaccination status has been shown to have high sensitivity and moderate specificity.43 Furthermore, the NHIS does not include institutionalized people in its surveys. Thus, NHIS results are applicable to the noninstitutionalized US population. In conclusion, only a fraction of people with asthma reported receiving influenza vaccine 12 months prior to their interview. Vaccination rates were especially low for participants ⬍ 50 years old. These results suggest several needs. First, the benefits and risks of administering influenza vaccine to people with asthma should be clarified. Second, reasons for the low vaccination rates among people with asthma should be determined.44 Focus group testing and surveys among people with asthma may help to define reasons why people choose not to be vaccinated. In addition to the usual reasons people may have for not getting vaccinated, asthma-specific issues, such as the fear of triggering acute asthma exacerbations, deserve study. Third, the knowledge, attitudes, and beliefs among health-care providers concerning administering influenza vaccination to people with asthma deserve additional investigation.38,45 Finally, determining whether there is a need for asthma-specific interventions may be needed.
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Forthcoming Articles in CHEST Home Diagnosis of Sleep Apnea: A Systematic Review of the Literature; An Evidence Review Cosponsored by the American Academy of Sleep Medicine, the American College of Chest Physisians, and the American Thoracic Society Flemons and coworkers Clinical Ventilator Adjustments That Improve Speech Holt and coworkers A Comparison of Smoking Habits Among Medical and Nursing Students Patkar and coauthors Radiologic Findings Are Strongly Associated With a Pathologic Diagnosis of Usual Interstitial Pneumonia Hunninghake and colleagues The Relationship Between Congestive Heart Failure, Sleep Apnea, and Mortality in Older Men Ancoli-Israel and coauthors Hetastarch and Bleeding Complications After Coronary Artery Surgery Avorn and colleagues Editorial comment by John Alexander, Jr.
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Study objectives: People with asthma are at high risk for complications from influenza; therefore, the Centers for Disease Control and Prevention recommends an annual influenza vaccination for people with asthma. Because little is known about such vaccination rates among adults, especially those aged 18 to 49 years and 50 to 64 years, we sought to estimate influenza vaccination rates among US adults. Design: Cross-sectional analyses of the 1999 to 2001 National Health Interview Surveys. Setting: US population. Participants: Representative samples of US adults aged > 18 years. Measurements and results: Asthma status and receipt of influenza vaccination during the past 12 months were self-reported. We found that 35.1% (95% confidence interval [CI], 33.0 to 37.0%), 36.7% (95% CI, 34.7 to 38.6%), and 33.3% (95% CI, 31.6 to 35.0%) of participants with asthma reported having had an influenza vaccination in 1999 (n ⴝ 2,620), 2000 (n ⴝ 3,007), and 2001 (n ⴝ 3,582), respectively. Among participants aged 18 to 49 years, the vaccination rates were 20.9% (SE 1.2%), 22.7% (SE 1.2%), and 21.1% (SE 1.0%), respectively. Among participants aged 50 to 64 years, the vaccination rates were 46.2% (SE 2.6%), 47.8% (SE 2.3%), and 42.3% (SE 2.1%), respectively. Vaccination rates increased strongly with age and with education in each year. Associations with sex or with race or ethnicity were inconsistent during the 3 years. Conclusions: The suboptimal vaccination rates among people with asthma aged 18 to 64 years suggest the need to increase influenza vaccination rates in this age group. (CHEST 2003; 124:783–789) Key words: asthma; health surveys; influenza; vaccination Abbreviations: CI ⫽ confidence interval; NHIS ⫽ National Health Interview Surveys; SE ⫽ standard error
health burden attributable to asthma in T hethepublic United States is considerable and is growing.1 In 2000, data from the Behavioral Risk Factor Surveillance System suggested that 14.6 million US
adults had current asthma.2 In 1998, the estimated cost of asthma was $12.7 billion.3 The public health burden of influenza is also enormous, and this For editorial comment see page 775
*From the Division of Environmental Hazards and Health Effects, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA. Manuscript received November 26, 2002; revision accepted March 21, 2003. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (e-mail: [email protected]). Correspondence to: Earl Ford, MD, MPH, Centers for Disease Control and Prevention, 4770 Buford Highway NE, Mailstop K66, Atlanta, GA 30341; e-mail: [email protected] www.chestjournal.org
disease accounts for an average of 20,000 deaths each year.4,5 In 2000, influenza and pneumonia were the seventh-leading cause of mortality in the United States.6 Upper respiratory tract infections are an important trigger of asthma and an important source of morbidity and mortality among persons with asthma.7,8 Influenza is a major cause of these upper respiratory CHEST / 124 / 3 / SEPTEMBER, 2003
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tract infections9; however, significant reductions in the morbidity and mortality associated with influenza can be achieved through vaccination.10,11 In 1997, the National Asthma Education and Prevention Program guidelines recommended that only people with persistent asthma receive annual vaccinations.12 For some time, the Centers for Disease Control and Prevention has recommended that persons with asthma receive annual influenza vaccinations.13 Despite these recommendations, influenza vaccine rates among children with asthma are low (9 to 25%).14 –19 Little is known, however, about the vaccination rates of adults with asthma, who are considered a high-risk group. Results from the Behavioral Risk Factor Surveillance System showed that vaccination rates for all adults aged ⱖ 65 years, an age group in which all adults should be vaccinated, were 65.6% in 1997 and 66.9% in 1999, but rates for participants with asthma of the 1999 survey were not provided.20,21 To examine the prevalence of influenza vaccinations among people with asthma, we examined data from the 1999-2001 National Health Interview Surveys (NHIS). Materials and Methods Since the early 1960s, a sample of the US population has participated in the NHIS. One adult per family was selected and asked to complete the sample adult questionnaire. AfricanAmerican and Hispanic populations were oversampled. Census interviewers conducted interviews with respondents in person. Participants were asked to complete a core set of questions, which has remained relatively constant from year to year, and to complete special supplements, which vary considerably each year. The numbers of adults aged 18 to ⬎ 85 years who were selected using a multistage sampling design and participated in the survey were 30,801 in 1999, 32,374 in 2000, and 33,326 in 2001. The final response rates for the sample adult questionnaires were 69.6% in 1999, 72.1% in 2000, and 73.8% in 2001. Details of the methods from 1999 to 2001 NHIS may be found elsewhere.22–24 Participants were asked, “Have you ever been told by a doctor or other health professional that you had asthma?” and “During the past 12 months, have you had an episode of asthma or asthma attack”? In addition, participants were asked, “During the past 12 months, have you had a flu shot?” Self-reported asthma status has
acceptable sensitivity and specificity when compared with more rigorous methods of defining asthma.25–27 We examined by age, sex, race or ethnicity, and educational attainment the percentages of participants with asthma who reported having an influenza vaccination. Direct age adjustment was performed using the age structure of the year 2000 US population aged ⱖ 18 years. We used logistic regression analysis to examine the independent associations of sociodemographic variables with vaccination status. Analyses were conducted with Software for the Statistical Analysis of Correlated Data (SUDAAN; Research Triangle Institute; Research Triangle Park, NC) to produce valid estimates of the variance.28 Estimates were calculated using sampling weights.
Results After excluding participants with missing values for the study variables, 29,981 participants (2,620 with asthma) were included in the analysis in 1999, 31,635 participants (3,007 with asthma) in 2001, and 32,572 participants (3,582 with asthma) in 2001. In all 3 years, participants with asthma were younger and more likely to be women than participants without asthma (Table 1). In 2000 and 2001, participants with asthma were also more likely to be white than those without asthma. Educational attainment was similar for the two groups. Overall, the percentage of participants with asthma who reported having received an influenza vaccination was 35.1% (95% confidence interval [CI], 33.0 to 37.0%) in 1999, 36.7% (95% CI, 34.7 to 38.6%) in 2000, and 33.3% (95% CI, 31.6 to 35.0%) in 2001 (Table 2). These percentages were significantly higher than those among participants without asthma in all 3 years (p ⬍ 0.001 in each year). Among participants with asthma, the percentages who reported having been vaccinated were 20.9% (standard error [SE] 1.2%) among participants aged 18 to 49 years, 46.2% (SE 2.6%) among participants aged 50 to 64 years, and 72.8% (SE 2.4%) among participants aged ⱖ 65 years in 1999. In comparison, these percentages among participants without asthma were 16.0% (SE 0.4%), 33.1% (SE 0.7%), and 65.2% (SE 0.8%), respectively. In 2000, these percentages were 22.7% (SE 1.2%), 47.8% (SE
Table 1—Unadjusted Means or Percentages of Selected Sociodemographic Variables Among Participants Aged > 18 Years, by Self-Reported Asthma Status, NHIS 1999 –2001* 1999
2000
2001
Variables
Asthma (n ⫽ 2,620)
No Asthma (n ⫽ 27,361)
p Value
Asthma (n ⫽ 3,007)
No Asthma (n ⫽ 28,628)
p Value
Asthma (n ⫽ 3,582)
No Asthma (n ⫽ 28,990)
p Value
Mean age, yr Male gender White race Less than high school
42.0 (0.4) 39.9 (1.2) 82.9 (0.9) 17.9 (0.9)
45.1 (0.2) 48.6 (0.4) 82.6 (0.4) 17.9 (0.3)
⬍ 0.001 ⬍ 0.001 0.761 0.941
43.1 (0.4) 41.4 (1.1) 76.9 (0.9) 18.8 (0.9)
45.1 (0.2) 48.5 (0.3) 73.9 (0.4) 17.9 (0.3)
⬍ 0.001 ⬍ 0.001 0.001 0.325
42.4 (0.3) 41.2 (1.0) 76.6 (0.8) 17.1 (0.8)
45.3 (0.1) 48.8 (0.3) 73.4 (0.4) 17.6 (0.3)
⬍ 0.001 ⬍ 0.001 ⬍ 0.001 0.557
*Data are presented as % (SE). 784
Clinical Investigations
Table 2—Age-Specific and Age-Adjusted Percentage of Participants Aged > 18 Years Who Reported Receiving an Influenza Vaccination During the Previous Year, by Self-Reported Asthma and Selected Sociodemographic Variables, NHIS 1999 –2001* 1999 Variables Total Age, yr 18–29 30–39 40–49 50–59 60–69 ⱖ 70 Sex Men Women Race or ethnicity Hispanic White African American Other Education Less than high school High school graduate or GED Some college or bachelor’s degree Graduate degree
2000
2001
Asthma (n ⫽ 2,620)
No Asthma (n ⫽ 27,361)
Asthma (n ⫽ 3,007)
No Asthma (n ⫽ 28,628)
Asthma (n ⫽ 3,582)
No Asthma (n ⫽ 28,990)
35.1 (1.0)
27.9 (0.3)
36.7 (1.0)
28.0 (0.3)
33.3 (0.9)
25.9 (0.3)
17.7 (1.9) 18.0 (2.0) 28.3 (2.4) 41.7 (2.9) 61.2 (3.3) 75.7 (2.7)
13.6 (0.6) 14.6 (0.5) 19.8 (0.7) 30.1 (0.8) 48.8 (1.0) 68.6 (0.9)
15.7 (1.6) 24.8 (2.1) 31.0 (2.3) 46.3 (2.5) 55.9 (3.7) 75.1 (2.3)
13.1 (0.6) 15.2 (0.5) 21.6 (0.7) 30.3 (0.9) 48.3 (1.0) 66.8 (0.8)
17.0 (1.5) 17.9 (1.6) 30.2 (2.0) 41.0 (2.5) 51.7 (3.3) 68.4 (2.7)
11.3 (0.5) 13.9 (0.5) 17.8 (0.6) 27.7 (0.8) 48.4 (1.0) 65.0 (0.8)
35.1 (1.7) 34.8 (1.2)
27.3 (0.4) 28.4 (0.4)
34.1 (1.5) 38.3 (1.2)
27.5 (0.4) 28.5 (0.4)
34.3 (1.4) 32.6 (1.0)
25.6 (0.4) 26.3 (0.4)
37.0 (2.9) 34.7 (1.2) 31.3 (3.0) 43.7 (5.5)
22.4 (0.9) 29.0 (0.4) 23.0 (0.8) 29.3 (1.7)
34.4 (2.6) 37.9 (1.2) 27.2 (2.4) 44.4 (4.5)
21.9 (0.8) 29.3 (0.4) 21.1 (0.6) 29.6 (1.8)
25.2 (2.4) 34.2 (1.0) 26.2 (2.0) 50.7 (5.1)
20.9 (0.8) 27.0 (0.3) 21.8 (0.8) 23.9 (1.4)
30.6 (2.2) 35.1 (1.8) 34.7 (1.7) 41.6 (3.2)
23.6 (0.6) 25.7 (0.5) 30.1 (0.4) 33.8 (1.1)
30.0 (2.2) 34.8 (1.8) 39.5 (1.5) 42.3 (3.1)
21.9 (0.6) 26.3 (0.5) 29.8 (0.5) 38.1 (1.2)
27.6 (2.1) 30.2 (1.5) 36.5 (1.2) 43.5 (4.0)
20.8 (0.6) 24.5 (0.5) 27.7 (0.4) 33.1 (1.2)
*Data are presented as % (SE). GED ⫽ general equivalency diploma.
2.3%), and 71.2% (SE 2.3%) among participants with asthma, and 16.6% (SE 0.4%), 33.3% (SE 0.8%), and 63.8% (SE 0.8%) among participants without asthma. In 2001, these percentages were 21.1% (SE 1.0%), 42.3% (SE 2.1%), and 64.8% (SE 2.4%) among participants with asthma, and 14.3% (SE 0.4%), 31.0% (SE 0.7%), and 62.8% (SE 0.7%) among participants without asthma. In each year, the percentage of participants with asthma who reported receiving an influenza vaccination increased strongly with age (Table 2). Vaccination rates were similar for men and women in 1999 and 2001. Participants with race or ethnicity designated as “other” showed the highest rate of vaccination. The vaccination rate progressively increased with higher educational attainment. To examine the associations between age, sex, race or ethnicity, and education and vaccination status among participants with asthma, we used multiple logistic regression analysis (Table 3). Age and education were significantly, independently, and positively associated with vaccination status in each year. In 2000, men were less likely to report having been vaccinated than women, and African-American participants were less likely to report having been vaccinated than white participants. In 2001, Hispanic participants were significantly less likely and participants with a race or ethnicity designated as other www.chestjournal.org
were significantly more likely to report having been vaccinated than white participants.
Discussion The results from this study indicate that only about one in three people with asthma are receiving influenza vaccinations. This vaccination rate has changed little from 1999 through 2001. These results suggest that recommendations to vaccinate adults with asthma are not being met. In particular, younger people with asthma are not being vaccinated against influenza. Only approximately one in five people with asthma aged 18 to 49 years reported having received such a vaccination. Respiratory infections, including influenza, can cause serious morbidity in people with asthma.29,30 Some evidence suggests that people with asthma may be more likely to experience influenza-associated morbidity than people who do not have asthma. For example, during periods when influenza virus was the predominant circulating upper respiratory virus, hospitalization rates for acute respiratory infections among children with asthma were much higher than those among children without a high-risk condition.31 These considerations taken together with the fact that inactivated influenza vaccine has CHEST / 124 / 3 / SEPTEMBER, 2003
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Table 3—Associations Between Selected Sociodemographic Variables and Influenza Vaccination Status From Multiple Logistic Regression Analysis Among Adults With Asthma Aged > 18 Years, NHIS 1999 –2001* Variables Age, yr 18–29 (reference) 30–39 40–49 50–59 60–69 ⱖ 70 Sex Men Women (reference) Race or ethnicity Hispanic White (reference) African American Other Education, yr Less than high school (reference) High school graduate or GED Some college or bachelor’s degree Graduate degree
1999 (n ⫽ 2,620)
2000 (n ⫽ 3,007)
2001 (n ⫽ 3,582)
1.00 1.00 (0.70–1.45) 1.75 (1.22–2.50) 3.27 (2.32–4.60) 7.85 (5.36–11.50) 15.50 (10.21–23.52)
1.00 1.68 (1.21–2.33) 2.32 (1.70–3.16) 4.59 (3.34–6.31) 7.24 (4.94–10.60) 18.52 (12.98–26.43)
1.00 1.02 (0.76–1.39) 2.11 (1.60–2.79) 3.41 (2.58–4.51) 5.74 (4.07–8.10) 12.27 (8.68–17.35)
0.99 (0.79–1.24) 1.00
0.82 (0.67–0.99) 1.00
1.05 (0.88–1.25) 1.00
1.16 (0.84–1.58) 1.00 1.02 (0.70–1.50) 1.63 (0.86–3.08)
0.97 (0.71–1.33) 1.00 0.67 (0.50–0.88) 1.39 (0.81–2.39)
0.75 (0.56–0.99) 1.00 0.77 (0.59–1.01) 2.18 (1.28–3.70)
1.00 1.29 (0.93–1.78) 1.33 (0.97–1.80) 2.22 (1.50–3.28)
1.00 1.31 (0.95–1.79) 1.64 (1.21–2.21) 2.05 (1.39–3.02)
1.00 1.17 (0.89–1.53) 1.63 (1.23–2.16) 2.18 (1.43–3.33)
*Data are presented as odds ratio (95% CI). See Table 2 for expansion of abbreviation.
been shown to be both clinically effective and costeffective32—albeit not necessarily based on studies of participants with asthma—suggest that people with asthma could benefit considerably from receiving an influenza vaccine. Yet, a review of nine randomized trials noted that the benefits and risks of vaccination for patients with asthma were inconclusive.33 All but three trials had sample sizes ⬍ 100 participants. In these trials, both early and late outcomes (mortality, hospital admission, pneumonia, asthma symptom scores, lung function measurements, medical visits, number of rescue courses of corticosteroids) were examined. The authors called for additional trials of sufficient size to study the question of the benefits and adverse effects of influenza vaccination in people with asthma. Questions about the short-term safety of the vaccine among people with asthma may have been answered by a large, randomized trial34 of children and adults with asthma that was published after the review. In this trial,34 the administration of inactivated influenza vaccine did not affect the frequency of exacerbations of asthma during the 2 weeks following the vaccination. The cost-effectiveness of annually vaccinating all eligible people with asthma is unknown. The Healthy People 2010 objectives call for 90% of noninstitutionalized adults aged ⱖ 65 years and 60% of noninstitutionalized high-risk adults aged 18 to 64 years to receive an annual influenza vaccination.35 People with asthma are included in the high-risk designation. The NHIS data show that 20.9 to 22.7% of asthmatic participants aged 18 to 49 786
years, 42.3 to 47.8% of asthmatic participants aged 50 to 64 years, and 64.8 to 72.8% of asthmatic participants aged ⱖ 65 years received a vaccination from 1999 to 2001. Previous studies of people aged ⱖ 65 years who participated in the Behavioral Risk Factor Surveillance System showed that 65.5% in 1997 and 66.9% in 1999 reported receiving an influenza vaccination during the 12 months prior to their interview.20,21 No estimates were reported for asthma status in these reports, however. Although a number of studies have reported low influenza vaccination rates among children, the vaccination rates among adults have apparently received little study. In one study,36 however, the influenza vaccination rate for a small cohort of asthmatic patients with a mean age of 38 years ranged from 64 to 78% during three consecutive influenza seasons. Age was a strong predictor of vaccination status among participants with and without asthma. As people age and become more likely to acquire a health condition, they are probably more likely to be vaccinated against influenza because of these conditions. In addition, influenza vaccine recommendations were initially focused on people aged ⱖ 65 years. Consequently, many of the campaigns to remind people and clinicians of the importance of influenza vaccination were targeted at people in this age group. In more recent years, the recommended age of vaccination has been lowered. The fact that people with asthma were more likely to report being vaccinated than those without asthma in each age Clinical Investigations
group suggests that having asthma probably increased the likelihood of being vaccinated. Reasons for the low vaccination rates among people with asthma are multifactorial and pertain to both health-care providers and patients. Patients may be reluctant to be vaccinated because they believe they will contract influenza from the vaccination, or they do not perceive any value in it.37 Barriers for health-care providers may include reimbursement issues and lack of methods to help them readily identify the patients who require vaccination and who need to be contacted.37 For persons aged ⱖ 65 years, influenza vaccination is reimbursed by Medicare, but for persons aged 18 to 64 years, reimbursement may be less available. Furthermore, the extent to which health-care providers are aware of the recommendations to vaccinate all patients with asthma, barring contraindications, is unclear. For example, physician awareness of the Centers for Disease Control and Prevention recommendations was associated with higher vaccination rates of pregnant patients.38 Furthermore, differing vaccine recommendations may also be a source of confusion to health-care providers. Asthmatic patients may be reluctant to be vaccinated against influenza for several reasons. In addition to the usual barriers to vaccination (such as availability of vaccine, scheduling of appointments, convenience, and cost), people with asthma, especially younger ones, may not perceive a need or may not be aware of the need for such vaccinations. Others may be concerned about possible adverse effects of vaccinations on their asthma. Yet, influenza vaccination has been shown to be safe in children and adults.18,19,34 Patients with asthma are recommended to have regular follow-up visits for asthma (1- to 6-month intervals) to ensure that control of asthma is maintained.12 These visits provide important opportunities to administer influenza vaccine to patients with asthma or to remind them of the need to receive such vaccinations. Improving vaccination rates for many vaccines among adults has proved to be a challenge. Because of the many reasons for suboptimal vaccination rates, a variety of possible approaches to improving these rates have been reviewed.39 Although vaccine characteristics differ, the strategies and interventions that have been recommended to improve vaccine rates for other vaccines may be useful to improve vaccine rates among people with asthma. For example, sending computerized reminder letters has been shown to significantly improve influenza vaccination rates among children with asthma.16,40 A review of patient reminder/recall systems found them to be effective in increasing vaccination rates for a variety of diseases among both children and adults.41 Another www.chestjournal.org
review showed that audit and feedback were also effective in improving immunization rates.42 Although these recommendations are likely to improve vaccine rates among people with asthma, it is unclear whether strategies specifically targeted at people with asthma may be helpful. The most obvious limitation of this study is that all information, including asthma status and vaccination status, are based on self-reports. Self-reported vaccination status has been shown to have high sensitivity and moderate specificity.43 Furthermore, the NHIS does not include institutionalized people in its surveys. Thus, NHIS results are applicable to the noninstitutionalized US population. In conclusion, only a fraction of people with asthma reported receiving influenza vaccine 12 months prior to their interview. Vaccination rates were especially low for participants ⬍ 50 years old. These results suggest several needs. First, the benefits and risks of administering influenza vaccine to people with asthma should be clarified. Second, reasons for the low vaccination rates among people with asthma should be determined.44 Focus group testing and surveys among people with asthma may help to define reasons why people choose not to be vaccinated. In addition to the usual reasons people may have for not getting vaccinated, asthma-specific issues, such as the fear of triggering acute asthma exacerbations, deserve study. Third, the knowledge, attitudes, and beliefs among health-care providers concerning administering influenza vaccination to people with asthma deserve additional investigation.38,45 Finally, determining whether there is a need for asthma-specific interventions may be needed.
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Forthcoming Articles in CHEST Home Diagnosis of Sleep Apnea: A Systematic Review of the Literature; An Evidence Review Cosponsored by the American Academy of Sleep Medicine, the American College of Chest Physisians, and the American Thoracic Society Flemons and coworkers Clinical Ventilator Adjustments That Improve Speech Holt and coworkers A Comparison of Smoking Habits Among Medical and Nursing Students Patkar and coauthors Radiologic Findings Are Strongly Associated With a Pathologic Diagnosis of Usual Interstitial Pneumonia Hunninghake and colleagues The Relationship Between Congestive Heart Failure, Sleep Apnea, and Mortality in Older Men Ancoli-Israel and coauthors Hetastarch and Bleeding Complications After Coronary Artery Surgery Avorn and colleagues Editorial comment by John Alexander, Jr.
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