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(Chest. 2004;126:369-374.)
© 2004 American College of Chest Physicians

Physician Asthma Education Program Improves Outcomes for Children of Low-Income Families*

Randall Brown, MD, MPH; Susan L. Bratton, MD, MPH; Michael D. Cabana, MD, MPH; Niko Kaciroti, PhD and Noreen M. Clark, PhD

* From the Department of Pediatrics (Drs. Brown, Bratton, Cabana, and Kaciroti), University of Michigan Health Sciences, and the Department of Health Behavior and Health Education (Dr. Clark), University of Michigan, Ann Arbor, MI.

Correspondence to: Susan L. Bratton, MD, F6884 Mott/0243, 1500 East Medical Center Dr, Ann Arbor, MI 48109-0243; e-mail: Brattons{at}med.umich.edu


    Abstract
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To determine whether an interactive physician seminar that has been shown to improve patient/parent satisfaction and to decrease emergency department visits for children with asthma was also effective for those children from low-income families.

Design: Seventy-four pediatricians and 637 of their patients were randomized to receive two asthma seminars or no educational programs and were observed for 2 years.

Setting: Physicians in the New York, NY, and Ann Arbor, MI, areas were enrolled, and, on average, 10 patients with asthma per provider were surveyed and observed for 2 years.

Patients or participants: A total of 637 subjects were enrolled, and 369 subjects remained in the study after 2 years. Of these, 279 had complete medical and survey information.

Interventions: Physicians were randomized, and then a random sample of their patients was enrolled and surveyed regarding the physician’s communication style, the child’s asthma symptoms, medical needs, and asthma care. Low income was defined as annual income of < $20,000.

Measurements and results: The families of 36 children (13%) had an income of < $20,000, and they were treated by 23 physicians. Low-income children in the treatment group tended to have higher levels of use of controller medications, to receive a written asthma action plan, and to miss fewer days of school, although these differences were not statistically significant compared to low-income children in the control group. However, low-income treatment group children were significantly less likely to be admitted to an emergency department (annual rate, 0.208 vs 1.441, respectively) or to a hospital (annual rate, 0 vs 0.029, respectively) for asthma care compared to children in the control group.

Conclusions: The educational program for physicians improved asthma outcomes for their low-income patients. Provider interventions targeted to these high-risk patients may diminish hospital and emergency department asthma care.

Key Words: asthma • communication • controller medications • emergency department • hospitalization • pediatric • physician education


    Introduction
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Asthma, the most common chronic disease of childhood, has major public health and financial consequences.1 Although children of low-income families and minority children, particularly those using Medicaid insurance, are more likely to have asthma, they are less likely to receive optimal medical care. These children have been shown to receive fewer preventive asthma medications23456 and to use more emergency department and inpatient services for the treatment of acute exacerbations.78910 A low level of use of controller medications and more frequent need for emergency services increases the total health-care costs.

Barriers to quality asthma care for low-income children include discontinuous health insurance coverage, poor physician continuity of care, family stress, patient/family health beliefs, concerns about medication side effects, and communication barriers between providers and patients.5111213 One method to improve patient outcomes would be to focus on the teaching health-care professionals regarding asthma care.

We previously reported on a physician education program, an interactive seminar based on self-regulation theory that emphasized not only asthma treatment practices but also physician communication and patient education skills.14 This program was associated with improved patient/parent satisfaction, increased prescription of antiinflammatory therapy, increased use of written asthma action plans, decreased number of nonemergent physician visits, and less use of urgent health-care services for asthma compared to asthma patients whose physician did not attend the interactive seminar.1415 We now report on the effects of this education program, specifically on a high-risk group (ie, low-income patients) to see whether they benefited equally.


    Materials and Methods
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study Sample
Physician enrollment included a convenience sample of 74 pediatricians in the New York, NY, and Ann Arbor, MI, areas, as previously reported.14 Primary care pediatricians were randomized to the interactive seminars or to a control group. A random sample of patients from each of the participating physicians was selected to assess the effectiveness of the program. Children enrolled in the study were 1 to 12 years of age, had a diagnosis of asthma made by a physician, had no other chronic conditions, and had received emergency care at least once for asthma in the prior year. On average, 10 patients per physician provided study information. A total of 637 patients and parent pairs were enrolled. Parents and children were unaware of whether their physician had participated in the interactive seminars or had not.

Intervention
The interactive seminar was based on the theory of the self-regulation14151617 of guiding physicians to enhance their therapeutic skills in treating childhood asthma, and to develop their ability to educate and counsel families about asthma self-management. There were two main components to the program, as follows: optimal clinical practice based on the National Asthma Education and Prevention Program Guidelines1; and patient teaching and communication.18 Several activities and materials were used, including brief lectures from a local asthma expert, a video showing effective clinician teaching and communication behavior,1419 case studies that presented clinical problems, a protocol by which physicians could assess their own communication behavior, and a review of messages to communicate and materials to distribute to patients/families. The seminars were delivered in two sessions of 2 to 3 h each, which were held over a period of 2 to 3 weeks.

Data Collection and Study Period
Physicians who did not attend the intervention were assigned a time corresponding to the training sessions for the purposes of scheduling data collection. The first visit that the patient made to the physician within 22 months after the intervention was followed by an interview with the parent. The patient then was tracked and evaluated at 12 months and 24 months after the initial visit. A total of 472 parents were initially interviewed, and 399 had complete data for prior and current medication intake, parent’s income and education, as well as prior and current health-care use. The parent interview consisted of questions related to the children’s asthma symptoms, prescribed medications, use of health-care services, and parental observations regarding the physician’s teaching and communication behaviors. At the time of final evaluation, 369 patients remained in the study, and 279 had complete data for prior and current medication intake, parent’s income and education, as well as prior and current health-care use.15

Statistical Analysis
The data were analyzed to assess changes related to the following outcomes of interest: change in the parent’s view of physician performance; and change in the child’s health status and health-care utilization. Children with a family income of <$20,000 per year were defined as low income and were compared to children of higher income families (ie, those with incomes of ≥ $20,000 per year). Race was recorded as white, African American, Latino/Hispanic, or other. Medicaid insurance was defined as children insured by Medicaid or self-insured. All analyses of postintervention information were controlled for baseline scores. Persistent asthma was defined as more than eight episodes of asthma symptoms per month, limitations of the child’s activities by asthma more than eight times per month, or awakening of the child from sleep more than twice a month during any season (ie, summer, fall, winter, or spring). Children with moderate or severe persistent asthma had symptoms or limited play during the day or awoke from sleep > 28 times a month during at least one season of the year.

Simple statistics included the {chi}2 test and the {chi}2 test for trend. Models were derived from the Poisson regression with generalized estimating equations to control for the clustering of patients around the same physician, and yearly health-care contact rates were calculated. The models controlled for severity of illness, which was defined as persistent asthma, moderate-to-severe persistent symptoms, prior and current use of antiinflammatory medications, income level, an interaction term of income level with intervention indicator, and "low" education, which was defined as high school or fewer years of parental education. Statistical significance was defined as p < 0.05.


    Results
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Among the 279 children with compete information there were 36 children (12.9%) from low-income families and 243 children (87.1%) from families with annual incomes of > $20,000 per year. Twenty-three physicians (intervention group, 12 physicians; control group, 11 physicians) treated the 36 low-income children. Their demographic characteristics are presented in Table 1 . A total of 112 children (40.1%) had Medicaid insurance with similar proportions in the two study groups (treatment group, 41.4%; control group, 47.1%). There were no significant differences between groups for patient age or household income. More patients whose physicians had undergone the educational program were nonwhite (28.0%) compared to the control group (25.4%). However, this difference was not statistically significant. Significantly fewer parents (19.1%) whose physicians had undergone the educational program had a high school or lower level of education compared to 35.3% of parents in the control group (p = 0.002). Children in the study had frequent asthma symptoms. Parents reported that 96.1% of all children had persistent symptoms and that 88.2% had moderate-to-severe persistent asthma during at least one season of the year.


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Table 1. Selected Characteristics of Children Treated by Study Physicians*

 
The parental views concerning physician demeanor and communication for the provider groups are presented in Table 2 and compare children from low-income families to others in the respective treatment groups. These views were reported at the 2-year follow-up assessment. Parents of children in the treatment and control groups with low income consistently reported less favorable impressions of their physician’s communication skills and demeanor compared to higher income families, however these differences were not statistically significant.


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Table 2. Parents’ View of Pediatrician Performance in the Physician Groups*

 
At the 2-year assessment, parents of children with moderate-to-severe persistent symptoms tended to be more likely to report that their child had received a prescription for inhaled antiinflammatory therapy from the physician who had attended the educational seminar compared to those parents in the control group (relative risk [RR],1.15; 95% confidence interval [CI], 0.93 to 1.43). Low-income treatment group parents also tended to be more likely to report that their child had received a prescription for inhaled antiinflammatory therapy from physicians who had attended the educational seminar compared to those parents in the control group (RR, 1.60; 95% CI, 0.78 to 3.25). Low-income parents reported that the physicians in the treatment group tended to be more likely to give a written asthma action plan to adjust the dose of medicine at home when symptoms change compared to physicians in the control group (RR, 1.40; 95% CI, 0.58 to 3.36). Finally, the average number of school days missed was 8.65 for the low-income children in the treatment group compared to 12.61 days for the low-income control patients, however, this difference was not significant (p = 0.48).

Changes in the adjusted use of urgent health-care services are presented in Table 3 . We compared the treatment and control groups by low-income status and Medicaid insurance status. Models that also adjusted for race were evaluated, but because of the sample size the models were unstable, and race was not included in the final analysis. Low-income children in the treatment group were significantly less likely to have used emergency department care and to have been admitted to a hospital during the 2-year assessment period compared to low-income children in the control group. Children with Medicaid insurance in the treatment group tended to have lower levels of use of an emergency department and had significantly lower rates of hospital admission compared to children in the control group. Because asthma is a chronic condition, we evaluated whether the intervention was associated with more scheduled follow-up visits but did not find a significant difference. Differences in the use of physician office visits were not significantly different but tended to be fewer in the low-income intervention group compared to low-income control patients.


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Table 3. Adjusted Yearly Rates of Emergency Department Visits and Hospitalization for Asthmatic Children by Income Levels and Medicaid Insurance Coverage*

 

    Discussion
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
It was previously reported that 2 years after physicians had attended an interactive seminar to enhance their ability to treat asthma and counsel patients, hospitalizations and emergency department visits had significantly decreased for children with higher levels of utilization at baseline.15 In this analysis, we have reported that the effect of the intervention was not limited to children from high-income or medium-income families, but that children from low-income families also benefited. Low-income families reported a trend for greater use of inhaled antiinflammatory medications and more common receipt of a written action asthma plan, and their children tended to miss fewer days of school compared to low-income families treated by physicians who had not received the educational intervention. The children from low-income families in the treatment group used significantly less emergency department and hospital care.

Current national and international guidelines120 recommend the daily use of maintenance medications for children with moderate-to-severe asthma. Antiinflammatory medications have been shown to prevent asthma exacerbations and to decrease hospital and emergency department use.2122 Inadequate controller therapy for asthma has been well-documented,5 however, children from low-income families are significantly less likely to receive a prescription for antiinflammatory therapy than are those from higher income families.23 We had a relatively small sample size of low-income patients and only showed a trend for improved prescription of inhaled corticosteroids in low-income patients treated by providers who attended the seminars.

For optimum asthma outcomes, providers must appropriately prescribe the medicine and explain its use clearly to educate patients and parents so that they can carry out a range of management activities needed to keep the disease in control. Both low parental education status and racial minority status have been identified as risk factors for the underuse of controller medications.1324 Our analysis suggests that the physician educational seminar may have helped providers to better identify and assist patients in this high-risk group (ie, low family income) who needed inhaled antiinflammatory medication therapy, and to give the parents an asthma action plan. Although the parental rating of physician communication did not differ significantly between groups, the ratings suggested that general communications between providers and low-income, high-risk patients needs improvement.

Improved asthma care for children may yield significant cost savings. Children with asthma incur almost 90% more health costs than children without asthma who receive care in a health maintenance organization and use twice as many inpatient hospital days.25 Lozano et al25 estimated that urgent care and hospitalizations consume a third of childhood asthma expenditures for a health maintenance organization. Hospital charges for inpatient asthma care vary by severity of illness, however, in 1995 the median hospital charges for pediatric asthma were $3,168 for a mild asthma exacerbation and $19,689 for a severe one.26 The median length of stay was 2 days for a mild case and 5 days for a severe case. Children who live in poverty or those insured by Medicaid are more likely to have severe exacerbations with prolonged lengths of stay and costs.2627

A rudimentary assessment of costs suggests that a wider use of the intervention for physicians could generate savings. Although Medicaid insures approximately 21% of American children,28 it insures about 52% of children hospitalized for asthma.26 We estimated the payments to the University of Michigan Health System for a Michigan Medicaid-insured pediatric asthma emergency department admission at $400 per visit. In 2000, Michigan Medicaid paid for 12,000 pediatric asthma emergency department visits (S. Clark, MPH, and K. Domkowski, PhD; personal communication; July 23, 2002). Based on the study treatment effect for low-income families, we estimated a 85.6% decrease in emergency department use, which would save Medicaid approximately $4.1 million on a statewide annual basis. Using the lower estimate of the 95% CI, which was a 53.3% reduction in visits, the annual savings would be $2.56 million. Using the lower estimate of the 99% CI, the reduction would be 32.7%, or an annual saving $1.57 million. There are approximately 3,600 family practice physicians and 1,700 pediatricians in Michigan.29 The direct cost of providing the interactive seminar to physicians is approximately $150 per physician or approximately $795,000 if given to all the pediatric primary care providers in the state.

Our research has several limitations. Although the study sample comprised a large group of pediatric asthma patients, the number of nonwhite children was relatively small. We did not include race in the final model because of small sample size, however, both African Americans and Hispanic Americans have been shown to receive less preventive asthma care, even after adjustment for insurance status.2342430 Likewise, the number of low-income children was also small, and the physician teaching intervention needs further testing with providers who care for this high-risk population. The study included children with more severe disease. To be eligible for the study, all children had to have been treated in an emergency department at least once in the prior year. We had complete data on a subset of the initial study participants, which may overrepresent patients with more severe disease as less ill patients could be less motivated to participate for the entire 2 years of study.

The study groups were not well-matched regarding parent education level, with significantly greater numbers of parents having a high school education or less in the control group compared to those in the treatment group. However, we found that the relationship between low income and improved asthma care remained even after adjustment for parent education level. The physician education intervention gives examples of ways for providers to effectively teach parents core asthma concepts and skills, to enable them to feel more confident and less worried, and to develop for families a picture of how the regimen can help the child reach health and personal goals. This method of educating patients appears to have reached and assisted parents with lower levels of formal education.


    Conclusion
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
The physician’s interactive seminar1415 has been shown to enhance asthma care and outcomes. The impact of the program is not reserved merely for those patients with more resources. The greatest decline in emergency department use was in children from low-income families. We believe that providers who care for high-risk asthma populations could benefit from this educational program and can provide better care at lower costs to children with asthma.


    Acknowledgements
 
The original data collection was conducted by a collaboration of investigators from the University of Michigan and Columbia University.1415 We are grateful to Dr. Molly Gong and to the providers, patients, and parents who were involved in the study.


    Footnotes
 
Abbreviations: CI = confidence interval; RR = relative risk

This work was supported in part by a grant from the Michigan Department of Health and Community Services, and by grant number HL-44976 from the Lung Division of the National Heart, Lung, and Blood Institute.

Received for publication December 16, 2003. Accepted for publication March 5, 2004.


    References
 TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

  1. National Heart Lung Blood Institute. National asthma education and prevention program: practical guide for the diagnosis and management of asthma. Bethesda, MD; National Institutes of Health, US Department of Health and Human Services, 1997; Publication No. 97–4063
  2. Finkelstein, JA, Barton, MB, Donahue, JG, et al Comparing asthma care for Medicaid and non-Medicaid children in a health maintenance organization. Arch Pediatr Adolesc Med 2000;154,563-568[Abstract/Free Full Text]
  3. Lieu, TA, Lozano, P, Finkelstein, JA, et al Racial/ethnic variation in asthma status and management practices among children in managed Medicaid. Pediatrics 2002;109,857-865[Abstract/Free Full Text]
  4. Ortega, AN, Gergen, PJ, Paltiel, AD, et al Impact of site of care, race and Hispanic ethnicity on medication use for childhood asthma. Pediatrics 2002;109,E1[CrossRef][Medline]
  5. Halterman, JS, Yoos, L, Kaczorowski, JM, et al Providers underestimate symptom severity among urban children with asthma. Arch Pediatr Adolesc Med 2002;156,141-146[Abstract/Free Full Text]
  6. Clark, NM, Brown, R, Joseph, CL, et al Issues in identifying asthma and estimating prevalence in an urban school population. J Clin Epidemiol 2002;55,870-881[CrossRef][ISI][Medline]
  7. Goodman, DC, Stukel, TA, Chang, C Trends in pediatric asthma hospitalization rates: regional and socioeconomic differences. Pediatrics 1998;101,208-213[Abstract/Free Full Text]
  8. Parker, JD, Schoendorf, KC Variation in hospital discharges for ambulatory care-sensitive conditions among children. Pediatrics 2000;106,942-948[Abstract/Free Full Text]
  9. Lozano, P, Sullivan, SD, Smith, DH, et al The economic burden of asthma in US children: estimates from the national medical expenditure survey. J Allergy Clin Immunol 1999;104,957-963[CrossRef][ISI][Medline]
  10. Mak, H, Johnston, P, Abbey, H, et al Prevalence of asthma and health service utilization of asthmatic children in an inner city. J Allergy Clin Immunol 1982;70,367-372[CrossRef][ISI][Medline]
  11. Aligne, CA, Auinger, P, Byrd, RS, et al Risk factors for pediatric asthma contributions of poverty, race, and urban residence. Am J Respir Crit Care Med 2000;162,873-877[Abstract/Free Full Text]
  12. Lara, M, Rosenbaum, S, Rachelefsky, G, et al Improving childhood asthma outcomes in the United States a blueprint for policy action. Pediatrics 2002;109,919-930[Abstract/Free Full Text]
  13. Mansour, ME, Lanphear, BP, DeWitt, TG Barriers to asthma care in urban children; parent perspective. Pediatrics 2000;106,512-519[Abstract/Free Full Text]
  14. Clark, NM, Gong, M, Schork, A, et al Impact of education for physicians on patient outcomes. Pediatrics 1998;101,831-836[Abstract/Free Full Text]
  15. Clark, NM, Gong, M, Schork, MA, et al Long-term effects of asthma education for physicians on patient satisfaction and use of health services. Eur Respir J 2000;16,15-21[Abstract]
  16. Bandura, A Social foundations of thought and action. 1986 Prentice-Hall. Englewood Cliffs, NJ:
  17. Clark, N, Zimmerman, BJ A social cognitive view of self-regulated learning about health. Health Educ Res 1990;5,371-379[Abstract/Free Full Text]
  18. Clark, NM, Nothwehr, F, Gong, M, et al Physician-patient partnership in managing chronic illness. Acad Med 1995;70,957-959[ISI][Medline]
  19. Clark, N, Gong, M, Schork, MA, et al A scale for assessing health care providers’ teaching and communication behavior regarding asthma. Health Educ Behav 1997;24,245-256[Abstract/Free Full Text]
  20. Global Initiative for Asthma (GINA). National Heart, Lung and Blood Institute (NHLBI). World Health Organization (WHO). Global initiative for asthma. 2002 Global Initiative for Asthma (GINA), National Heart, Lung and Blood Institute (NHLBI). Bethesda, MD:
  21. The Childhood Asthma Management Program Research Group. Long-term effects of budesonide or nedocromil in children with asthma. N Engl J Med 2000;343,1054-1063[Abstract/Free Full Text]
  22. Adams, RJ, Fuhlbrigge, A, Finkelstein, JA, et al Impact of inhaled antiinflammatory therapy on hospitalization and emergency department visits for children with asthma. Pediatric 2001;107,706-711
  23. Kozyrkyj, A, Mustard, CA, Simons, ER Socioeconomic status, drug insurance benefits, and new prescriptions for inhaled corticosteroids in schoolchildren with asthma. Arch Pediatr Adolesc Med 2001;155,1219-1224[Abstract/Free Full Text]
  24. Finkelstein, JA, Lozano, P, Farber, HT, et al Underuse of controller medications among Medicaid insured children with asthma. Arch Pediatr Adolesc Med 2002;156,562-567[Abstract/Free Full Text]
  25. Lozano, P, Fishman, P, VonKorff, M, et al Health care utilization and costs among children with asthma who were enrolled in a health maintenance organization. Pediatrics 1997;99,757-764[Abstract/Free Full Text]
  26. Meurer, J, Varghese, G, Subichin, S, et al Asthma severity among children hospitalized in 1990 and 1995. Arch Pediatr Adolesc Med 2000;154,143-149[Abstract/Free Full Text]
  27. Bratton, SL, Roberts, JS, Watson, RS, et al Acute severe asthma: outcome and Medicaid insurance. Pediatr Crit Care Med 2002;3,234-238[CrossRef][Medline]
  28. Medical expenditure panel survey (MEPS) 1996. Available at: http://www.meps.ahrq.gov/papers/99–0042/99–0042.htm# table4. Accessed August 2000
  29. American Medical Association. Master file. Available at: http://www.mmslists.com/main/asp. Accessed November 2003
  30. Akinbami, LJ, Schoendorf, KC Trends in childhood asthma: prevalence, health care utilization, and mortality. Pediatrics 2002;110,315-322[Abstract/Free Full Text]



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