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Obstetrics & Gynecology 2005;106:66-72
© 2005 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Racial Differences in Asthma Morbidity During Pregnancy

Kecia N. Carroll, MD MPH, Marie R. Griffin, MD MPH, Tebeb Gebretsadik, MPH, Ayumi Shintani, PhD MPH, Ed Mitchel, MS and Tina V. Hartert, MD MPH

From Vanderbilt University School of Medicine, Departments of Pediatrics, Medicine, and Preventive Medicine, and the Division of General Pediatrics, Division of General Internal Medicine, Division of Allergy, Pulmonary and Critical Care Medicine, Center for Education and Research on Therapeutics, Center for Health Services Research; Department of Biostatistics, Mid-South Geriatric Research Education and Clinical Center; Quality Scholars Program, VA TN Valley Health Care System; General Clinical Research Center; and Meharry/Vanderbilt Center for Reducing Asthma Disparities, Nashville, Tennessee.


    ABSTRACT
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective: Little is known about racial differences in asthma outcomes during pregnancy. We performed a cohort study to estimate racial differences in maternal asthma outcomes in a low-income population of pregnant women in which blacks and whites have similar medical care access and benefits.

Methods: We conducted a population-based cohort study of asthma-related morbidity in black and white pregnant women enrolled in Tennessee’s Medicaid Program, TennCare. Pregnant women were identified through TennCare enrollment files linked to birth certificates, 1995–2001. Prepregnancy, women with asthma were identified using International Classification of Diseases, 9th Revision, codes for health care visits and pharmacy files for asthma medication. Adjusted relative rates (RR) of rescue corticosteroid prescriptions, emergency department (ED) visits, and hospitalizations during pregnancy were compared by race using Poisson regression.

Results: We identified 4,315 women with asthma (4%) from a population of 112,171 pregnant women of black or white race with at least 180 days of continuous enrollment in TennCare before pregnancy. Blacks were more likely to receive a course of rescue corticosteroids than whites (14.6% versus 11.9%, adjusted RR 1.35, 95% confidence interval [CI] 1.14–1.61), have an emergency department visit (16.7% versus 8.7%, adjusted RR 1.89, 95% CI 1.57–2.27), or be hospitalized for asthma (9.0% versus 5.2%, adjusted RR 1.73, 95% CI 1.34–2.24).

Conclusion: Pregnant women with asthma had high asthma-related morbidity. Black women had clinically significantly more morbidity than whites. There is a need to improve the medical care of low-income women with asthma, particularly black women.

Level of Evidence: II-2


In the United States, asthma is one of the most common chronic diseases, affecting approximately 9% of the population.1 Asthma may complicate up to 8.4% of pregnancies and has the potential to adversely affect the health of both the mother and fetus. Previous studies have examined the course of asthma during pregnancy, with results from a recent prospective cohort study determining that one third of pregnant women with mild asthma moved into a more severe asthma category, whereas approximately 20% of patients with moderate-severe disease were reclassified into the mild category.5,6 The aim of asthma management in pregnant patients is to establish well-controlled asthma, treat exacerbations appropriately, and maintain the good health of the mother and fetus.4 Although the course of asthma in pregnancy has been addressed in multiple studies, little is known about racial disparities in asthma morbidity during pregnancy.7

Racial disparities in asthma morbidity and mortality have been documented in different patient populations, with blacks exhibiting increased asthma morbidity and attributable mortality compared with whites. Blacks at higher risk for asthma morbidity and mortality are disproportionately low income, and the impact of race and poverty on increased asthma morbidity is difficult to separate. The Tennessee Medicaid Program (TennCare) provides health care access and benefits to low-income, Medicaid-eligible, and uninsured state residents. Using a large population-based administrative database linked with vital records, we examined racial disparities in asthma-specific outcomes during pregnancy among women with asthma enrolled in TennCare.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We conducted a population-based cohort study of 4,315 pregnant women with asthma who were enrolled in TennCare from 1995–2001, the most recent years for which data were available at the start of the study. In 1994, TennCare replaced the federal Medicaid program as a state-based managed health care program that covers Medicaid-eligible individuals and the uninsured.11 Subjects were identified from a population of 112,171 black and white pregnant women, aged 15–44 years, with singleton births and at least 180 days of continuous enrollment in TennCare before the subject’s last menstrual period. Continuous enrollment was defined as no gap in coverage of more than 7 days total during the 180 days before the last menstrual period. Approximately 50% of infants born in Tennessee are born to women enrolled in TennCare, and 48% of deliveries to mothers in TennCare met the continuous enrollment criteria. Childbearing women outside of the 15–44-year age range and women of nonblack or nonwhite race were too few to study. The primary study outcomes were measures of asthma morbidity during pregnancy (from the first day of their pregnancy [last menstrual period] to the date of delivery), including asthma-related emergency department visits, hospitalizations, or rescue corticosteroid therapy. The primary predictor variable was maternal race.

Data were obtained from linked TennCare administrative data files and Tennessee state vital records files by using previously described methods for linkage at the study institution.12,13 After linkage, the necessary information was extracted from primary files, an analysis file was created, and all personal identifiers were removed. Analysis files contain no personal identifiers and study results are reported in aggregate and cannot be linked to individuals.13 We determined medication use through drug prescription billing claims to the TennCare program. Demographic variables were obtained from Tennessee birth certificate data and TennCare enrollment files. Date of last menstrual period was obtained from birth certificate data and used to determine week of pregnancy.

Linked Tennessee birth certificate files and TennCare data were used to identify eligible pregnant women. The first day of pregnancy was defined as the date of the last menstrual period as listed on the birth certificate for 92.6% of the women. When last menstrual period information from the birth certificate was not available, it was calculated from the median gestational period in weeks for the infant’s race, birth weight, and birth year (7.35%), or last menstrual period was assigned as 270 days before birth (0.05%). Women with spontaneous or induced abortions (< 20 weeks gestation and/or < 500 g) were not included in the study.

Maternal asthma was determined by using inpatient, outpatient, and/or pharmacy file claims during the 180 days before the last menstrual period date. This baseline period allowed us to identify women with asthma before the onset of pregnancy by using a previously validated method of identifying patients with asthma.14 Women with an International Classification of Diseases, Ninth Revision (ICD-9-CM) diagnosis code of 493 (asthma) in any of the 9 diagnostic fields for inpatient, other hospital care (23-hour observation), or outpatient physician visit claims were considered to have asthma. In addition, women with 2 prescriptions for any short-acting ß-agonist or a single prescription for any other asthma medication (inhaled anti-inflammatory, long-acting ß-agonist, leukotriene-modifying drug) during the 180 days before pregnancy were considered to have asthma. Rescue corticosteroid use was defined as a single prescription of at least 3 days or more for corticosteroids, with each course defined by the end of a prescription to the start of the next prescription, separated by at least 7 days.

Maternal asthma-specific outcomes assessed during pregnancy included prescriptions filled for inhaled anti-inflammatory agents (any versus none), emergency department visits (any versus none), hospitalizations for asthma (any versus none), and courses of rescue corticosteroids (any versus none). Dexamethasone, betamethasone, and hydrocortisone were not included as asthma-related corticosteroid therapy because these medications may be used in pregnant women at risk for preterm labor to prevent infant respiratory distress syndrome. Asthma-related emergency department visits and hospitalizations were identified by using ICD-9 code 493. Asthma-specific medication use was determined through pharmacy files as has been previously described.14,15

Maternal race (black, white) and region of residence (urban included metropolitan areas with populations of at least 100,000, suburban included areas not urban, but in standard metropolitan statistical areas, and rural included all other areas) were identified from the TennCare enrollment files. Demographic variables determined from infant birth certificate data included maternal age at delivery, maternal education level, marital status, previous pregnancy, smoking status, and adequacy of prenatal care. Adequacy of prenatal care was defined by using the Kotelchuck index, which classifies prenatal care, based on the timing of the initiation of care and service use, in the following categories: none, inadequate, intermediate, adequate, and adequate plus.16 Comorbidities were defined by using medical diagnoses in diagnostic fields from inpatient or outpatient visits or through prescriptions filled during the 180 days before pregnancy, as indicators of chronic diseases, as previously described.12 Using comorbid diseases, patients were classified as having a high-risk pregnancy if, during the 180 days before their pregnancy, we identified an ICD-9 diagnosis or a pharmacy file indicating chronic heart disease, chronic lung disease other than asthma, renal disease, immunosuppressive disorders including human immunodeficiency virus (HIV) infection, diabetes mellitus, and cancer. We defined high-risk asthma as the presence of any of the following during the 180 days before pregnancy: an asthma-related hospitalization (including 23-hour observation) or emergency department visit, chronic corticosteroid use (≥ 90-day supply of oral corticosteroids), a course of rescue corticosteroids (3 days or more of oral corticosteroids), or 3 or more short-acting ß-agonist prescriptions. By definition, women in the non–high-risk subgroup did not meet the above criteria.

The protocol was approved by the institutional review boards of Vanderbilt University and the Tennessee Department of Health.

Women’s baseline characteristics were presented by race for the total cohort of women with asthma by using proportions. Chi-squared tests were used to compare categorical variables by race. We performed analyses using Poisson regression to estimate the unadjusted and adjusted rate ratios of an asthma-related emergency department visit, hospitalization, or course of rescue corticosteroids for black women compared with whites.17 All women were followed during their pregnancy, with follow-up ending at delivery. Covariates in the model included age, as a nonlinear restricted cubic spline function,18 education level, prior pregnancy, smoking status, high-risk pregnancy, region of residence, and year of delivery. Analyses were performed with SAS 8.02 (SAS Institute, Cary, NC) and R 1.9.1 statistical software version. We graphically depicted the cumulative incidence of first emergency department visit and hospitalization during pregnancy in black and white women.

Finally, to study access to care, we identified a comparison cohort of women who met our study definition of asthma during pregnancy, but not during the prepregnancy baseline period. However, all asthma-specific outcome analyses were restricted to women identified as having asthma during the baseline period, before the ascertainment of study outcomes.


    RESULTS
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A total of 112,171 eligible mother-infant dyads were identified; 43% of the mothers were black. Approximately 4% of all women met the criteria for asthma during the prepregnancy baseline period, with black women making up 29% of the women with asthma. The majority of the women with asthma were aged 15–24 years at the time of delivery (63%), had a high school degree or less (87%), and were not married (59%). Eleven percent of the pregnancies in this cohort were classified as high-risk pregnancy. The women were from urban (40%), suburban (24%), and rural regions (36%) of the state. Thirty-nine percent of the women reported smoking, and 28% received less than adequate prenatal care during their pregnancy (combined inadequate and intermediate categories).

There were distinct differences in several characteristics between races (Table 1). Compared with whites, black women were more likely to be single (86% versus 47%, P < .001), live in urban areas (76% versus 25%, P < .001), and be nonsmokers (86% versus 50%, P < .001). More blacks received less than adequate prenatal care than whites (combined inadequate and intermediate categories, 35% versus 25%, P < .001). The prevalence of asthma in the cohort was 2.7% (1,285/47,856) in the black population and 4.7% (3,030/64,315) in the white population. The asthma cohort was further classified as non–high-risk asthma (1,871/4,315, 43.4%) or high-risk asthma (2,444/4,315, 56.6%). In the group of black women, 60.9% were classified as having high-risk asthma, compared with 54.9% of white women, P < .001 (Table 1). During pregnancy 3,834 women (2,503 whites and 1,331 blacks), categorized as not having asthma during the baseline period, met the criteria for asthma based on health care or medication use during pregnancy. This comparison cohort represented 3.9% of white women and 2.8% of black women.


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Table 1. Baseline Characteristics of Study Cohort of Pregnant Women With Asthma Enrolled in TennCare, 1995–2001 (N = 4,315)

 

A minority of patients with asthma used inhaled anti-inflammatory agents during their pregnancy (685/4,315, 15.9%). In the group of black women, 19.8% filled a prescription for inhaled anti-inflammatory agents, compared with 14.2% of white women, P < .001.

During pregnancy 12.7% (547/4,315) of women with asthma received one or more courses of rescue corticosteroids. Black women were more likely to receive a course of steroids than whites (14.6% of black women versus 11.9% of white women), with unadjusted rate ratio (RR) of 1.57 (95% confidence interval [CI] 1.37–1.81). The increased rate at which black women received a course of steroids remained significant after controlling for age, education level, previous pregnancy, smoking status, high-risk pregnancy, region of residence in state, and delivery year (adjusted RR 1.35, 95% CI 1.14–1.61) (Table 2).


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Table 2. Univariate and Multivariable Analyses of Asthma-Related Health Care Use by Racial Group Among Pregnant Women with Asthma Enrolled in TennCare, 1995–2001

 

Overall, 11.1% of women with asthma had an asthma-related emergency department visit during pregnancy. Black women were more likely to have an asthma-related emergency department visit than whites (16.7% of black women versus 8.7% of whites, adjusted RR 1.89, 95% CI 1.57–2.27) (Table 2). The increased cumulative rate of emergency department visits during pregnancy for black women compared with whites is illustrated in Figure 1A.



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Fig. 1. Cumulative rate of asthma-related emergency department (ED) visits (A) and hospitalizations (B) among black and white pregnant women enrolled in TennCare 1995–2001.

Carroll. Racial Differences in Asthma Morbidity. Obstet Gynecol 2005.

 

Overall 6.3% of the women were hospitalized for asthma. Black women had an increased rate of hospitalization compared with whites (9% of blacks versus 5.2% of whites, adjusted RR 1.73, 95% CI 1.34–2.24). The increased rate of hospitalization during pregnancy for black women compared with whites is illustrated in Figure 1B.


    DISCUSSION
 TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pregnant women with asthma in this low-income population had significant asthma-related morbidity during pregnancy, as measured by requirements for rescue corticosteroids (12.7%), emergency department visits (11.1%), and hospitalizations (6.3%) for asthma. In a recent prospective study of women with asthma, hospitalization rates ranged from 2.3% in women with mild asthma to 6.8% and 26.9% for women with moderate and severe asthma, respectively.6 Although we were unable to categorize asthma severity in this administrative data set, rates of asthma hospitalization among women with high-risk asthma were 8.6% overall, 12.1% for blacks, and 6.9% for whites. Potentially contributing to the morbidity found, a large percentage of women in the cohort smoked during pregnancy (39%), and only a minority filled a prescription for an inhaled anti-inflammatory agent (16%).

The main objective of the current investigation was to examine asthma morbidity during pregnancy by race. Racial disparities in asthma morbidity and mortality have been documented in nonpregnant patient populations, and blacks have increased rates of asthma-associated emergency department visits, hospitalizations, and mortality compared with whites.8–10,19–24 Emergency department visits and hospitalizations have been used as standard measures of asthma morbidity in studies that use administrative data. In addition, major public health initiatives, such as Healthy People 2010,25 include emergency department visits and hospitalizations as measures of asthma morbidity and have set national objectives to decrease both as indicators of improvement in the nation’s health. A recent retrospective study that captured asthma diagnoses at the delivery hospitalization found that adjustment for insurance status diminished, but did not totally eliminate, racial differences in asthma diagnosis.7 Because racial disparities in asthma morbidity may be confounded by factors such as differential access to medical care or socioeconomic factors, we examined pregnant women in TennCare, a state health plan for low-income individuals where blacks and whites have similar medical care access and benefits. After controlling for factors such as rural or urban residence, level of education, and smoking status, black women disproportionately required at least one emergency department visit (adjusted RR 1.89, 95% CI 1.57–2.27), hospitalization (adjusted RR 1.73, 95% CI 1.34–2.24), or rescue corticosteroid prescription (adjusted RR 1.35, 95% CI 1.14–1.61), compared with whites. Studies looking at nonpregnant adults in managed care settings have similarly found differences in rates of emergency department visits and hospitalization by race.26,27

Reasons for the disparities in health and health care between black and white patients are not well delineated, but are likely multifactored. Increased asthma morbidity and mortality has been found in residents of inner city areas where blacks disproportionately live, potentially caused, in part, by increased exposure to indoor or outdoor triggers that exacerbate asthma.31,32 In addition, differences in asthma management may contribute to racial disparities in asthma morbidity, with studies finding that, within the same health care network, white adults were more likely to report receiving education regarding asthma self-management and specialist referral than blacks.26,33 Variation in the use of beneficial preventive medications, such as inhaled corticosteroids, by race has been noted in a number of studies.26,27,34 In the TennCare cohort, rates of inhaled corticosteroid prescription–filling were low, although more blacks than whites filled a prescription (20% versus 14%). Although blacks and whites in TennCare have similar access, blacks may disproportionately receive fewer services. In this study cohort, black women were less likely to receive adequate prenatal care than whites, as determined by the Kotelchuck index, a standard measure of the adequacy of prenatal care.16 If black patients receive inadequate treatment or a lower quality of care in one aspect of their health care, it is possible that other medical conditions, such as asthma, are inadequately treated as well. In addition, medical management involves a patient-physician partnership, and societal factors that contribute to a lack of cultural understanding or racial discrimination may negatively impact the relationships black patients develop with their doctors and thus serve as barriers to good health practices and outcomes.28,35–37

There are several potential limitations of this study that are important to consider. This investigation was conducted using an administrative database in which health care utilization was the sole measure of asthma morbidity and not clinical symptoms or objective tests of asthma severity. However, using such an administrative data set allowed us to study a large number of women over a 7-year period with objective assessments of morbidity. We defined asthma by using ICD-9 diagnoses and medication use and would not have detected asymptomatic women or women with mild symptoms who did not visit a medical provider or fill a prescription during the baseline period. In addition, we would not have identified symptomatic persons who were not receiving care or treatment. Although not sensitive for mild or untreated asthma, our definition of asthma was specific, with previous work showing that similarly defined women had definite asthma (62%) or probable asthma (38%) by chart review.14 We determined whether prescriptions were filled for a medication, but we could not determine whether the medications were actually taken or if medications were obtained from other sources. However, filling a prescription is the first step in medication use, and it is likely that differences in filling practices reflect differences in use of medication. Although we controlled for a measure of socioeconomic status by conducting our study in a low-income population, it is possible that variations in income or other socioeconomic factors remained that could affect health behaviors and practices and medical care use. However, the percentage of black women identified as having asthma in the baseline period was similar to the percentage of black women identified during pregnancy, a period when women were likely getting routine follow-up. This suggests that lack of access during the baseline period may not have been a large barrier, although similar access to care does not mean that the quality or quantity of the care received was the same. Finally, the racial distribution of women with asthma in our study, which consisted of 2.7% of blacks and 4.7% of whites, was lower than expected, suggesting that black women may be less likely to be identified and appropriately treated for their asthma. Another explanation involves the effect of smoking on asthma. Almost 50% of white women in this cohort were smokers, compared with less than 15% of blacks; it is possible that smoking contributed to exacerbations that prompted asthma visits or prescription filling. Higher smoking rates in whites than blacks could lead to increased identification of disease among whites.

Using uniform criteria, we identified black and white low-income women with asthma before pregnancy, followed their asthma-related outcomes throughout pregnancy, and found that a substantial number of pregnant women required emergency department visits or hospitalizations for asthma. Despite similar medical access and benefits, asthma-specific morbidity during pregnancy was significantly higher for blacks. Asthma programs that target low-income black women and/or system-wide programs aimed at improving asthma outcomes through improved asthma management and smoking cessation efforts may decrease asthma-related morbidity overall and racial disparities during pregnancy. Improvements in asthma care may lead to better maternal-fetal outcomes for all women with asthma, particularly black woman, who have higher rates of morbidity.


    Footnotes
 
This study was supported in part by research grants UO1 HL 72471, MO1 RR00095, and KO8 AI01582 from the Agency for Healthcare Research and Quality, Centers for Education and Research, grant U18-HS10384 from the Geriatric Research Education and Clinical Centers (GRECC), Department of Veterans Affairs, and grant K12 RR17697 from the National Center for Research Resources.

The authors thank the Tennessee Bureau of TennCare of the Department of Finance and Administration, and the Tennessee Department of Health, Office of Policy, Planning and Assessment, for providing the data.

Address reprint requests to: Tina V. Hartert, MD, MPH, Division of Allergy, Pulmonary and Critical Care Medicine, Center for Health Services Research, 6107 MCE, Vanderbilt University School of Medicine, Nashville, TN 37232-8300; e-mail: tina.hartert{at}vanderbilt.edu.

doi:10.1097/01.AOG.0000164471.87157.4c


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Right arrow Epidemiology/public health
Right arrow Medical complications of pregnancy


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