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Trends in Preventive Asthma Medication Use Among Children and Adolescents, 1988–2008

Brian K. Kit, Alan E. Simon, Cynthia L. Ogden and Lara J. Akinbami
Pediatrics January 2012, 129 (1) 62-69; DOI: https://doi.org/10.1542/peds.2011-1513
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Abstract

Objectives: To examine trends in preventive asthma medication (PAM) use among children with current asthma in the United States from 1988 to 2008.

Methods: We performed a cross-sectional analysis of PAM use among 2499 children aged 1 to 19 years with current asthma using nationally representative data from the National Health and Nutrition Examination Survey (NHANES) during 3 time periods: 1988–1994, 1999–2002, and 2005–2008. PAMs included inhaled corticosteroids, leukotriene receptor antagonists, long-acting β-agonists, mast-cell stabilizers, and methylxanthines.

Results: Among children with current asthma, there was an increase in the use of PAMs from 17.8% (SE: 3.3) in 1988–1994 to 34.9% (SE: 3.3) in 2005–2008 (P < .001 for trend). Adjusting for age, gender, race/ethnicity, and health insurance status, the odds of PAM use were higher in 2005–2008 compared with 1988–1994 (adjusted odds ratio [aOR] = 2.6; 95% confidence interval [CI]: 1.5–4.5). A multivariate analysis, combining all 3 time periods, showed lower use of PAMs among non-Hispanic black (aOR = 0.5 [95% CI: 0.4–0.7]) and Mexican American (aOR = 0.6 [95% CI: 0.4–0.9]) children compared to non-Hispanic white children. PAM use was also lower in 12 to 19 year olds compared with 1 to 5 year olds and also in children who did not have health insurance compared with those who did.

Conclusions: Between 1988 and 2008, the use of PAM increased among children with current asthma. Non-Hispanic black and Mexican American children, adolescents aged 12 to 19 years, and uninsured children with current asthma had lower use of PAM.

KEY WORDS
  • Abbreviations:
    aOR —
    adjusted odds ratio
    CI —
    confidence interval
    NAEPP —
    National Asthma Education and Prevention Program
    NHANES —
    National Health and Nutrition Examination Survey
    PAM —
    preventive asthma medication

    • What’s Known on This Subject:

    Preventive asthma medications (PAMs) are a primary management strategy to control asthma morbidity. Little is known about changes over time in prevalence of PAM use among children and adolescents in the United States.

    What This Study Adds:

    Our analysis demonstrates an increase in use of PAMs among children and adolescents with current asthma in the United States from 1988–1994 to 2005–2008, but racial and ethnic disparities in use of PAMs persist.

    In 2009, the prevalence of current asthma was 9.6% among children and adolescents in the United States, the highest prevalence measured.1,2 Childhood asthma is associated with significant disease burden, including limitations in physical activity, missed school, emergency department visits, hospitalizations, and death.1,2 Despite declines since the early- to mid-1990s in some measures of asthma disease burden, including mortality and hospitalizations, children and adolescents continue to experience significant asthma morbidity.2 For example, in 2005–2007, children and adolescents aged 0 to 17 years experienced 640 000 emergency department visits and 10.5 million missed school days as a result of asthma.1

    The burden of asthma among specific racial and ethnic communities is even more substantial. Compared with white children, American Indian, Alaska Natives, and black children have significantly higher asthma prevalence.1,2 Furthermore, high asthma prevalence among some Latino groups, particularly Puerto Rican children, has been described.1,2 Higher asthma-related emergency department visits, hospitalizations, and mortality among black children, compared with white children, further define the disparities in asthma disease burden that exist among children and adolescents in the United States.1,2

    Control of asthma symptoms and prevention of adverse asthma outcomes are goals of asthma management as outlined in the National Asthma Education and Prevention Program’s (NAEPP) asthma treatment guidelines, which were first released in 1991.3 Preventive asthma medications (PAMs) are the primary management strategy recommended by these guidelines to control asthma symptoms among children with persistent asthma. In addition to PAMs, other evidence-based strategies for asthma control include asthma trigger avoidance4,5 and asthma management education.6,7

    Despite known benefits,8–13 PAMs remain underutilized.14–22 A previous report with a national sample estimated between 28.5% and 32.8% of children and adolescents with current asthma used PAMs in 2003 to 2005.23 Furthermore, minority children have been less likely to receive adequate preventive therapy.15,19,22,24–27 What is unknown, however, is whether the use of PAM has increased or decreased over time or if efforts to address racial and ethnic disparities have reduced the differences in use between groups.28 The authors of this study examine trends in the use of PAMs among children and adolescents with current asthma in the United States from 1988 to 2008. The authors also examine disparities in PAM use.

    Methods

    Study Design

    The National Health and Nutrition Examination Survey (NHANES) is a nationally representative, multistage probability sample of the US civilian, noninstitutionalized population conducted by the National Center for Health Statistics of the Centers for Disease Control and Prevention. NHANES initially was conducted as a periodic survey (including NHANES III from 1988–1994). Since 1999, however, NHANES has been in the field continuously, and data are released in 2-year increments. Participants in NHANES receive a detailed in-person home interview followed by a physical examination at a mobile examination center, as described elsewhere.29,30

    Written informed consent for data collection was obtained from all participants aged 16 years and older. A proxy, typically a parent or guardian, provided informed consent for children younger than 16 years. The survey was approved by the National Center for Health Statistics ethics review board.

    Survey Years

    Data from NHANES III, collected from 1988–1994 and 4 additional NHANES data releases, were included in this analysis: 1999–2000, 2001–2002, 2005–2006, and 2007–2008. To increase sample size and statistical reliability of estimates, multiple data releases were combined. The final categorization of survey years for this analysis was 1988–1994, 1999–2002, and 2005–2008. The data years 2003–2004 were excluded to create 3 roughly comparable survey periods. The unweighted interview response rate ranged from 78% to 84% for the data releases; additional details are available elsewhere.31

    Current Asthma

    During the in-home interview, participants or their proxy for children younger than 16 years of age were asked, “Has a doctor or health professional ever told you that you have asthma?” and “Do you still have asthma?” Consistent with previous epidemiologic studies, a participant was considered to have current asthma if an affirmative response to both questions was provided.2,32

    PAMs

    Data on prescription medication use were collected during the in-home interview. Participants were asked, “Have you taken or used any prescription medicines in the past month?” Participants with an affirmative response were asked to provide the medication containers for the interviewer to review. If the container was not available, use of the medication was self- or proxy-reported.

    A medication was categorized as a PAM if it was listed as a long-term controller medication in the NAEPP asthma treatment guidelines.3 Specifically, PAMs included the following medication classes: inhaled corticosteroids, leukotriene receptor antagonists, long-acting β-agonists, mast-cell stabilizers, and methylxanthines. Medications manufactured with more than 1 class of PAM contributed to each class of PAM contained within the medication. Because the NAEPP treatment guidelines delineate indications for use of multiple PAMs, the authors examined use of multiple asthma medications by categorizing the number of PAMs as 1 or more (any PAM) and 2 or more (≥2 PAM).

    Demographic and Health Insurance Variables

    Age was categorized as 1 to 5 years, 6 to 11 years, and 12 to 19 years. Race/ethnicity was categorized as non-Hispanic white, non-Hispanic black, Mexican American, and “other” based on self-reported race and ethnicity. In all survey years included in the analysis, non-Hispanic black participants were oversampled, and in all years except 2007–2008, Mexican American participants were oversampled. Beginning in 2007–2008, Latino participants overall, rather than solely Mexican American participants, were oversampled; however, sufficient numbers of Mexican American participants were retained to follow trends in health outcomes.33 Children for whom race/ethnicity was categorized as “other” are included in overall estimates, but results for this group are not reported separately. Status of health insurance coverage was asked of all participants at the time of the interview. PAM use did not differ between privately and publically insured youth. To increase statistical power, health insurance coverage status was examined dichotomously as insured (public or private insurance) versus uninsured. Less than 1% of children and adolescents were missing health insurance data; these individuals were excluded from health insurance analyses. Family income also was considered for inclusion in this study but was found to be highly correlated with health insurance status (polychoric correlation > 0.6). Model fit, using Hosmer-Lemeshow Goodness-of-Fit Test, was better when health insurance was used, so health insurance rather than income was included in the final analyses.

    Statistical Analysis

    Prevalence estimates and SEs were calculated for use of any PAM, ≥2 PAMs, and each PAM class overall and by age, gender, race/ethnicity, and health insurance status. Trends by time period in the use of PAMs were tested using logistic regression models. In instances in which sufficient data were available for only 2 time periods, differences between time periods were tested with a Student’s t test. To describe disparities in use of PAM during the most recent time period, 2005–2008, prevalence estimates are reported, and differences between non-Hispanic white participants and both non-Hispanic black and Mexican American participants were tested with a Student’s t test.

    Multivariate logistic regression analyses were performed to test the trends in use of PAMs over survey periods while adjusting for the confounding effects of age, gender, race/ethnicity, and health insurance status. All variables in the multivariate logistic regression analysis were analyzed as categorical variables. aORs and 95% CIs are reported. Because the prevalence of the outcome (use of PAM) was >10%, the OR yielded by logistic regression overestimates relative risk.

    Statistical analyses were performed using SAS software version 9.2 (SAS Institute Inc, Cary, NC), and SUDAAN software version 10.0 (RTI, Research Triangle Park, NC) was used to account for the complex design of the survey. Sample weights, which account for differential probabilities of selection, nonresponse, and noncoverage, were used to obtain estimates representative of the noninstitutionalized US population. A P value of <.05 is considered significant for all analyses. No adjustment for multiple comparisons was made.

    Analytic Sample

    In 1988–1994, a total of 13 062 boys and girls aged 1 to 19 years were interviewed. In 1999–2002, a total of 9672 participants were interviewed, and in 2005–2008, 8574 participants were interviewed. Participants with missing or incomplete data for current asthma status or prescription medication use were excluded (n = 95). Of the remaining 34 057 children and adolescents, there were 2499 with reported current asthma (767 in 1988–1994, 870 in 1999–2002, and 862 in 2005–2008), which comprised our analytic sample. Demographics of the sample are described in Table 1.

    View this table:
    TABLE 1

    Sample Sizes and Descriptive Information for the Analytic Sample, 1988–1994, 1999–2002, and 2005–2008

    Results

    Overall, among children and adolescents aged 1 to 19 years with current asthma, there was an increasing trend in the use of PAM (1988–1994: 17.8%; 1999–2002: 21.1%; and 2005–2008: 34.9%; P < .001 for trend) (Table 2). In stratified analyses, children 1 to 5 years and 6 to 11 years of age, boys and girls, non-Hispanic white children, non-Hispanic black children, Mexican American children, and insured youth each had an increase in use of PAM from 1988–1994 to 2005–2008 (P < .05 for each trend). In contrast, the estimated increases between 1988–1994 and 2005–2008 for use of PAM among adolescents 12 to 19 years of age and uninsured youth were not statistically significant.

    View this table:
    TABLE 2

    Percent of Children and Adolescents With Current Asthma Using PAMs Over Time by Age, Gender, Race/Ethnicity, and Health Insurance Status

    Trends over time in use of specific PAM classes also were examined. In 1988–1994, inhaled corticosteroids, methylxanthines, and mast-cell stabilizers were used by 4.7% (SE: 1.3), 10.4% (SE: 1.8), and 4.9% (SE: 1.8), respectively, of children and adolescents with current asthma (Table 3). In 2005–2008, compared with 1988–1994, reported use of inhaled corticosteroids increased (4.7% vs 23%, P < .001 for trend). In 2005–2008, compared with 1999–2002, reported use of leukotriene receptor antagonists (7.2% vs 21%, P < .001) and long-acting β-agonists (3% vs 11.4%, P < .001) increased. Use of ≥2 PAMs increased from 1999–2002 to 2005–2008 (5.6% vs 16.5%, P < .001). Reported use of inhaled corticosteroids among non-Hispanic black and Mexican American children and adolescents did not differ significantly from non-Hispanic white children and adolescents for the 2005–2008 survey years (Table 4).

    View this table:
    TABLE 3

    Percent of Children Aged 1 to 19 Years With Current Asthma Using Specific PAMs Over Time

    View this table:
    TABLE 4

    Percent of Children Aged 1 to 19 Years With Current Asthma Using Specific PAMs by Race/Ethnicity, 2005–2008

    In multivariate logistic regression analysis, controlling for potential shifts in the age, gender, race/ethnicity, and health insurance status of children with current asthma, there was still an increased odds of PAM use in 2005–2008 as compared with 1988–1994 (aOR = 2.6; 95% CI: 1.5–4.5) (Table 5). In 1999–2002, compared with 1988–1994, the odds of PAM use did not statistically differ. The odds of PAM use were lower among non-Hispanic black children (aOR = 0.5; 95% CI: 0.4–0.7) and Mexican American children (aOR: 0.6; 95% CI: 0.4–0.9) compared with non-Hispanic white children. Adolescents, compared with children 1 to 5 years of age (aOR: 0.5; 95% CI: 0.4–0.8), and uninsured children compared with insured children (aOR: 0.6; 95% CI: 0.4–0.9), had a lower odds of PAM use. There were no statistically significant differences by gender in the odds of PAM use. All possible 2-way interactions were tested in our final models; there were no significant interactions.

    View this table:
    TABLE 5

    Logistic Regression Analysis of PAM Use Among Children and Adolescents With Current Asthma

    Discussion

    Overall, among children and adolescents with current asthma, use of PAM increased from 1988–1994 to 2005–2008. Use of anti-inflammatory medication classes (eg, inhaled corticosteroids and leukotriene receptor antagonists) also increased between 1988–1994 and 2005–2008. Additional changes in use of PAM during our study period include an increase in long-acting β-agonists and use of 2 or more classes of PAM.

    Our estimates for use of PAM are generally consistent with those reported by the Agency for Healthcare Quality and Research using data from the Medical Expenditures Panel Survey. For example, in 2003, 2004, and 2005, the Agency for Healthcare Quality and Research reported that 28.5%, 32.8%, and 30.6%, respectively, of children and adolescents aged 0 to 17 years with current asthma used PAM.23 To our knowledge, there are no other nationally representative studies that describe the use of PAM among children and adolescents with current asthma before 2003 or after 2005.

    Over the past 30 years, there have been advances in asthma research, including greater knowledge of the role of inflammation in symptom development and chronic airway remodeling.34,35 Additionally, clinical research also has demonstrated the benefits of PAMs, particularly anti-inflammatory medications, in reducing asthma morbidity8–13 and achieving asthma control.36,37 To this end, our findings of an increase over time in the proportion of children with asthma using PAMs, and anti-inflammatory medications specifically, parallel advances in asthma research.

    Use of long-acting β-agonists alone, without concurrent use of another PAM, is associated with adverse health outcomes, including death,38,39 and is not recommended by the NAEPP. In our analysis, we sought to examine trends in the prevalence of long-acting β-agonist use alone, but these estimates were not statistically reliable. However, by 2005–2008, ∼96% of children and adolescents with current asthma who used long-acting β-agonists also used inhaled corticosteroids. Further, an exclusion of children and adolescents who used long-acting β-agonists alone did not significantly change the estimates presented in our analysis. The risks of long-acting β-agonist use are not inconsequential, however, and to further examine the role of long-acting β-agonists in asthma management, plans for clinical trials have been reported recently.40

    Similar to other studies,15,19,22,24–27 we report racial and ethnic disparities in the use of PAMs among children with asthma. Given that underutilization of PAMs may contribute to racial disparities in asthma outcomes, we were interested in trends in PAM use among racial/ethnic groups.3,24 Our results demonstrate there were increases in the use of PAMs among each examined racial and ethnic group. We further examined whether the relationship between race and ethnicity and PAM use changed over time by assessing effect modification between race/ethnicity and survey time periods. Because there was no evidence of effect modification in our analysis, our results demonstrate persistence of disparities in PAM use between non-Hispanic white children and both non-Hispanic black and Mexican American children during our study period.

    Another group with relatively low use of PAMs is adolescents 12 to 19 years of age. National data show that asthma morbidity in the adolescent age group is similar to that among younger ages, and although a rare event among children, the asthma death rate is similar between adolescents and young children.2 Adolescence is a period of increasing responsibility for asthma medication administration41 and also is associated with decreased adherence to medications,42 despite the remaining need for preventive medications. Although adherence to asthma medications is a recognized problem for children of all ages,15,43–47 lower adherence among adolescents as compared with younger children may have contributed to the differences by age in use of PAMs. Other factors, however, including low utilization of primary care services during adolescence,48 also may have contributed to our findings of low use of PAMs among adolescents.

    In our analysis, children and adolescents without health insurance coverage had lower use of PAM than those who were insured, which is consistent with other literature that has explored associations between health insurance coverage and prescription medication use among children and adolescents.49,50 A study in New York State revealed that after previously uninsured children with asthma acquired health insurance through the State Children’s Health Insurance Program, their parents reported substantially fewer problems obtaining asthma medication.51 Lower financial barriers52,53 and greater access to a usual source of care54–56 may partly explain higher use of PAM among insured children compared with uninsured children and adolescents.

    There are several factors that may have contributed to the increase in use of PAMs over time. The NAEPP asthma treatment guidelines were first released in 1991 and subsequently updated in 1997 and 2007, with an interim update in 2002.3 The concerted efforts to educate health care professionals, patients and their families, and the public about the importance of inflammation in the pathology of asthma and the value of preventive medications in averting adverse outcomes may have contributed to increases in the use of PAM. Entirely new classes of PAMs, including leukotriene receptor antagonists, became available during our study period.57 Similarly, the growth of direct-to-consumer advertising of pharmaceuticals during this period has been documented,58 and such advertisements may increase medication use.59 Although still other factors may have contributed to our findings, our study suggests that any changes in the population composition by age, gender, race/ethnicity, and health insurance status of children and adolescents with current asthma did not fully explain the increase in PAM usage over time.

    A sensitivity analysis was conducted to assess if patterns of PAM use during the most current survey years, 2005–2008, were similar to those observed in our full analytic sample. In a model with all covariates shown in Table 5 except for survey time period, we observed similar associations with PAM for the remaining covariates, that is, lower odds of PAM use in non-Hispanic white children, Mexican American children, older children, and uninsured children. Because of decreased sample size, however, not all associations were statistically significant.

    Our study has several strengths. Prescription medication data were obtained during an in-home interview by trained interviewers who verified most of the reported medications based on review of the medication containers. Additionally, the sample was nationally representative. There are also limitations to our study. We are unable to classify asthma severity using the NAEPP criteria, although underutilization of PAMs among children and adolescents with persistent asthma has been well documented.14–21 Additional studies are needed to accurately define and describe the proportion of children and adolescents untreated for persistent asthma using NAEPP criteria. In 2005–2008, we were able to examine PAM use among individuals with potentially more severe disease, defined as either use of PAM or limitations in physical activity because all children and adolescents in this survey period were asked about limitations in physical activity due to respiratory difficulties. Among youth with potentially more severe disease, lower use of PAM among non-Hispanic black participants, Mexican American participants, and adolescents was observed, and aORs were similar to those reported for our main analysis; however, the sample sizes for uninsured children were too small in this restricted sample to produce a reliable estimate (results not shown). Finally, residual confounding from factors not assessed, including provider practice type60 and continuity of health insurance coverage,32 also may be a limitation of this study.

    Conclusions

    Between 1988 and 2008, more children with asthma were treated with PAMs. Further, there were changes in the classes of PAMs used and an increase in the simultaneous use of multiple asthma medications. Improved asthma management, including increased use of PAMs, may have contributed to the declines in childhood asthma morbidity.61 Future research may focus on identifying interventions effective in improving delivery of asthma care consistent with NAEPP’s asthma treatment guidelines, including PAM use, and reducing disparities in PAM use.

    Footnotes

      • Accepted September 9, 2011.
    • Address correspondence to Brian K. Kit, MD, MPH, 3311 Toledo Rd, Room 4419, Hyattsville, MD 20782. E-mail: igd0{at}cdc.gov

    • Dr Kit contributed to conception and design, acquisition of data, analysis and interpretation of the data, and drafting the article; Dr Simon contributed to conception and design, analysis and interpretation of the data, and revising the article; Dr Ogden contributed to conception and design, acquisition of data, analysis and interpretation of the data, and revising the article; and Dr Akinbami contributed to conception and design, analysis and interpretation of the data, and revising the article. All authors provided final approval for submission of the article to Pediatrics.

    • The findings and conclusions in this report are those of the authors and not necessarily of the National Center for Health Statistics, Centers for Disease Control and Prevention.

    • FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

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    PRESIDENTIAL PARDON: I did not buy a live turkey this year for Thanksgiving, so when I purchased my bird from the store, it did not so much resemble a bird but a large round package wrapped in plastic. The anonymity of the package may be one reason why I did not feel any remorse planning my holiday meal. However, I wonder what would have happened if I had gone to a farm and selected one to be slaughtered from a gaggle of live turkeys. Would I have felt differently? Would I have bought the turkey and then released it? After all, the President of the United States pardons a turkey each Thanksgiving. As reported on CNN.com (Holidays: November 22, 2011), the tradition of a Presidential turkey pardon dates back to when Abraham Lincoln was in office. Minutes before the scheduled demise of a pet turkey raised by his son Tad for the holiday meal, Tad burst into a cabinet meeting and pleaded with his father not to kill the bird. President Lincoln wrote the order for a reprieve on a card and the turkey was granted its freedom. The tradition of annual Presidential turkey pardons, however, is a much more recent phenomenon. President Eisenhower was presented a turkey each Thanksgiving holiday by the National Turkey Federation. President Eisenhower, parsimonious in all his pardons, simply ate the birds. President George H.W. Bush began the modern tradition of pardons in 1989. When presented with a live gobbler for the holiday meal he decreed that the turkey would not be eaten by anyone and granted an official presidential pardon. This year two birds will be selected for pardon. After a Rose garden ceremony, the birds will be taken to Mount Vernon Estates and Gardens where they will be on display until January. A protected environment for the pardoned turkeys seems like a good idea. I am pretty sure that pardoned domesticated turkeys released into the wild in our neck of the woods would not survive too long. As for me, having raised and then eaten the sheep I raised, I think that “I like Ike.”

    Noted by WVR, MD

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    Pediatrics
    Vol. 129, Issue 1
    1 Jan 2012
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    Trends in Preventive Asthma Medication Use Among Children and Adolescents, 1988–2008
    Brian K. Kit, Alan E. Simon, Cynthia L. Ogden, Lara J. Akinbami
    Pediatrics Jan 2012, 129 (1) 62-69; DOI: 10.1542/peds.2011-1513
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