Summary
Objective
Asthma is one of the most common medical conditions complicating pregnancy. Despite the presence of published guidelines outlining the care of the pregnant patient with asthma, disparities in the treatment of acute asthma exacerbations in the emergency department related to pregnancy status are known to exist. We sought to determine if pregnancy status affected the treatment of women presenting to a tertiary emergency department for care of acute asthma exacerbations.
Methods
We retrospectively compared the emergency department treatment of acute asthma exacerbations in 123 pregnant women to 123 non-pregnant controls. Asthma exacerbations were classified by severity according to pre-determined criteria.
Results
In the emergency department (ED), pregnant women were significantly less likely to be treated with systemic corticosteroids than non-pregnant controls (50.8% versus 72.4%, p = 0.001). Similarly, 41% of pregnant women received prescriptions for prednisone at the time of discharge from the ED compared to 69.2% of non-pregnant women (p < 0.001).
Conclusions
In this population of asthmatics presenting to a tertiary emergency department with acute asthma exacerbations, pregnant women were less likely to receive appropriate therapy with systemic corticosteroids.
Keywords
Abbreviations:
ED (emergency department), ICS (inhaled corticosteroids), NAEPP (National Asthma Education and Prevention Program), PEF (peak expiratory flow)Introduction
Background
There is disparity in asthma care resulting in higher rates of morbidity for minority groups, lower socioeconomic classes and urban populations.
1
Women are disproportionately affected, as asthma rates are higher for women than for men and women are more likely to live at or below poverty level.2
Pregnancy may further increase vulnerability for high risk groups.National Health Interview Survey. Hyattsville, MD 2008 [12-08-10]; Available from: http://www.cdc.gov/nchs/fastats/asthma.htm.
3
, 4
Asthma is one of the most common serious medical conditions to complicate pregnancy, with approximately 8% of pregnancies affected.
5
Asthma exacerbations during pregnancy are common, with 12.6–51.9% of women likely to experience an asthma exacerbation during pregnancy depending on the underlying severity of their disease.6
However, the effects of pregnancy on overall asthma control are often quite variable with reports of 23% of women experiencing improvement in asthma control and 30% noting worsening during pregnancy, with pre-pregnancy asthma severity seeming to be most predictive of asthma course during pregn-ancy provided that appropriate asthma therapy is continued.6
, 7
Importance
Recent studies have highlighted under-utilization of controller medications in pregnant women with asthma during pregnancy but have not been designed to explore the reasons underlying these potential treatment disparities.
8
, 9
In 1999 Cydulka and colleagues found that pregnant women who presented to an emergency department (ED) for treatment for an acute asthma exacerbation were less likely to receive appropriate treatment with systemic corticosteroids than non-pregnant women, highlighting suboptimal care of the pregnant asthmatic during an acute exacerbation.4
These findings are surprising considering the National Asthma Education and Prevention Program (NAEPP) published the first guidelines outlining asthma care during pregnancy in 1993, providing evidenced based principles for maintenance therapy and treatment of exacerbations which are nearly equivalent to those of the non-pregnant patient.10
Interestingly, the literature is relatively void of similar studies since 1999, and it is not known if practice patterns have changed particularly since the NAEPP published updated guidelines for managing asthma in pregnancy in 2004.5
Goals of this investigation
The purpose of this study was to compare the clinical presentation and treatment of acute asthma in the emergency department between pregnant and non-pregnant women and to assess the adequacy of therapy for acute exacerbations when compared to currently published guidelines.
Methods
Study design and selection of participants
We retrospectively compared the emergency department treatment of acute asthma exacerbations in pregnant women to non-pregnant controls. Potential subjects were identified through the assistance of an electronic database which identified women who presented to the emergency department at a single tertiary care center with the diagnoses of asthma and pregnancy between January 1996 and September 2009. Non-pregnant women presenting to the emergency department with acute asthma exacerbations were selected as controls and were matched according to age, race, and year of visit. The institutional review board at the participating institution deemed the study exempt from formal review.
Inclusion criteria included age 18–45 and clinical history consistent with an acute asthma exacerbation as determined by the treating clinician. Repeat visits by individual subjects were excluded. 809 potential pregnant women with asthma exacerbations were identified, with 686 records excluded as a result of repeat visits for individual subjects or ED encounters for non-asthma related complaints. The medical records of 123 pregnant women and 123 controls were reviewed.
Data collection
The medical records of all subjects were retrospectively reviewed. Data was collected on a standardized data collection form to assess patient demographic characteristics, current asthma medications, details of current asthma exacerbation, ED management and disposition, and perinatal outcomes (when available). Return visits to the ED for persistent or worsening asthma symptoms were recorded if they occurred during the two weeks following the observed period. Asthma exacerbations were classified according to severity based on the following criteria (Table 1): 1). “Mild” exacerbations: dyspnea with activity, peak expiratory flow (PEF) ≥ 70% predicted, or sympt-oms relieved by ≤ 1 short-acting bronchodilator in the ED 2). “Moderate” exacerbations: dyspnea interferes with usual activity, PEF 40–69% predicted, or symptoms relieved with 2–3 short-acting bronchodilators in the ED 3). “Severe” exacerbations: dyspnea with conversation or at rest, PEF < 40% predicted, or symptoms requiring > 3 short-acting bronchodilators in the ED 4). “Life threatening” exacerbations: distress or too dyspneic to speak, PEF < 25% predicted, and symptoms requiring > 3 short-acting bronchodilators in the ED.
Table 1Classification of severity of asthma exacerbation at presentation to the emergency department.
| Symptoms & signs | Initial peak expiratory flow rate (PEF) | Short-acting bronchodilator treatments required for symptom relief in the ED | |
|---|---|---|---|
| Mild | Dyspnea with activity | PEF ≥ 70% predicted | ≤1 |
| Moderate | Dyspnea interferes with usual activity | PEF 40–69% predicted | 2–3 |
| Severe | Conversational dyspnea or at rest | PEF < 40% predicted | >3 |
| Life threatening | Distress, too dyspneic to speak | PEF < 25% predicted | >3 |
ED = emergency department; PEF = peak expiratory flow. Adapted from National Asthma Education and Prevention Program (NAEPP). Expert Panel Report 3: guidelines for the diagnosis and management of asthma: full report 2007.
Primary data analysis
We compared demographic and clinical characteristics between pregnant and non-pregnant subjects using the two-sample t-test for continuous variables and Fisher’s exact test for categorical variables. Continuous variables were assessed for normality and equal variance across the two groups in order to run the two-sample t-test. Categorical variables are presented as counts and percents while continuous variables are presented as means and standard deviations. All analyses were run using Stata 10.1, Stata Corporation, College Station, TX.
Results
The study included 123 pregnant women and 123 non-pregnant controls. Demographic data and baseline asthma medications are summarized in Table 2. The subjects were matched by age, race, and year of visit. Pregnant women were more likely to have health insurance coverage provided by Medicaid, and were less likely to be taking oral leukotriene modifiers at the time of presentation. Otherwise, the groups were similar.
Table 2Demographic characteristics of participants.
| Non-pregnant | Pregnant | p-value | |
|---|---|---|---|
| n | 123 | 123 | |
| Age, mean (sd) | 24.7 (5.6) | 24.9 (5.4) | – |
| Race, % | |||
| White | 24.4 | 25.2 | – |
| Black | 74.0 | 73.2 | – |
| Other | 1.6 | 1.6 | – |
| Insurance, % | |||
| Private | 32.5 | 22.2 | <0.001 |
| Medicaid | 39.8 | 67.5 | |
| None | 27.6 | 10.3 | |
| Current smoker, % | |||
| No | 56.1 | 54.5 | 0.939 |
| Yes | 25.2 | 27.6 | |
| Unknown | 18.7 | 17.9 | |
| Hospital at presentation | |||
| Main University, % | 62.6 | 56.6 | 0.364 |
| University Affiliate, % | 37.4 | 43.4 | |
| Current Medication Use, % | |||
| Short-acting β-agonist | 68.9 | 73.0 | 0.573 |
| Inhaled anti-cholinergic | 2.5 | 1.7 | 0.999 |
| Long-acting β-agonist (LABA) | 5.7 | 4.1 | 0.769 |
| Inhaled corticosteroids (ICS) | 15.6 | 12.4 | 0.580 |
| Combination ICS/LABA | 13.1 | 11.6 | 0.846 |
| Oral leukotriene modifier | 13.9 | 4.1 | 0.012 |
| Theophylline | 3.3 | 1.6 | 0.446 |
| Prednisone | 4.9 | 2.5 | 0.500 |
sd = standard deviation; LABA = long-acting β-agonist; ICS = inhaled corticosteroids.
Asthma related symptoms on presentation for pregnant and non-pregnant women are shown in Table 3. The groups were similar in terms of duration of preceding symptoms, self-reported antecedent viral respiratory illnesses, and reported non-adherence to use of inhaled corticosteroids prior to ED presentation (10.8% in controls vs. 16.1% in pregnant women, p = 0.167). In those women who reported non-adherence to use of inhaled corticosteroids, all non-pregnant controls (n = 4) reported running out of their medications while 40% (n = 2) of pregnant women reported running out of their medication and 60% (n = 3) reported discontinuing the medications specifically due to pregnancy. Use of the classification for severity of exacerbation did not reveal any statistically significant differences by pregnancy status; a similar proportion of non-pregnant versus pregnant women presented with mild exacerbations (18.7% versus 31.1% respectively), moderate exacerbations (61.0% versus 52.1%) and severe/life threatening exacerbations (20.3% versus 16.8%); overall p = 0.090. Peak expiratory flow rates and arterial blood gas values were recorded when available, but due to the extremely small sample size, no analysis was performed (data not shown).
Table 3Clinical characteristics of participants.
| Non-pregnant | Pregnant | p-value | |
|---|---|---|---|
| n = 123 | n = 123 | ||
| Duration of symptoms, % | |||
| ≤ 3 h | 8.6 | 4.2 | 0.397 |
| 4–23 h | 35.6 | 31.1 | |
| 1–7 days | 51.3 | 53.8 | |
| > 7 days | 14.5 | 10.8 | |
| Exacerbation severity, % | |||
| Mild | 18.7 | 31.1 | 0.090 |
| Moderate | 61.0 | 52.1 | |
| Severe/life threatening | 20.3 | 16.8 | |
| Respiratory rate, mean | 21.3 | 20.9 | 0.473 |
| Oxygen saturation [SpO2%], mean | 96.1 | 97.6 | 0.148 |
| Associated viral symptoms, % | 56.9 | 56.2 | 0.999 |
| Stopped inhaled corticosteroids preceding ED visit, % | 10.8 | 16.1 | 0.167 |
| ED visit for asthma in preceding six months, % | 10.6 | 16.3 | 0.261 |
ED = emergency department.
Pregnant and non-pregnant women received comparable numbers of aerosolized short-acting bronchodilators while in the ED as one would expect for similar levels of severity, yet pregnant women were significantly less likely to be treated with systemic corticosteroids in the ED (50.8% versus 72.4%, p = 0.001) (Table 4). It does not appear that the decreased use of systemic steroids in the pregnant patients was related to treatment biases related to trimester of pregnancy. Forty-five percent of patients presenting during the first trimester (n = 40) received systemic corticosteroids compared to 56.1% (n = 57) of those presenting in the second trimester, and 55.6% (n = 18) of those presenting in the third trimester (p = 0.549). Similar disparities in prescribing patterns were noted in patients discharged from the ED, where pregnant women were significantly less likely to be prescribed corticosteroids compared to non-pregnant controls. Forty-one percent of pregnant women received prescriptions for prednisone at the time of discharge from the ED compared to 69.2% of non-pregnant women, while inhaled corticosteroids (ICS) were prescribed infrequently in both groups (3.7% versus 2.5% respectively for ICS alone and 3.7% versus 7.5% for ICS in combination with prednisone, overall p < 0.001).
Table 4Emergency department treatment and disposition.
| Non-pregnant (n = 123) | Pregnant (n = 123) | p-value | ||
|---|---|---|---|---|
| Bronchodilator given in ED, % | Albuterol | 41.7 | 49.1 | 0.290 |
| Albuterol/ipratroprium | 58.3 | 50.9 | ||
| Number of nebulized short-acting bronchodilators received in ED, mean (sd) | 2.6 (1.4) | 2.3 (1.5) | 0.097 | |
| Systemic corticosteroids given in ED, % | 72.4 | 50.8 | 0.001 | |
| Corticosteroids given at discharge from ED, % | None | 20.8 | 51.4 | <0.001 |
| Prednisone | 69.2 | 41.3 | ||
| Inhaled corticosteroids | 2.5 | 3.7 | ||
| Both | 7.5 | 3.7 | ||
| Disposition, % | Discharge | 95.1 | 87.7 | 0.066 |
| Admission or observation in labor & delivery | 4.9 | 12.3 | ||
| Representation to ED within two weeks, % | 2.5 | 9.7 | 0.026 |
ED = emergency department; sd = standard deviation.
Severity of asthma exacerbation did seem to influence the use of systemic corticosteroids (Table 5). During treatment in the ED, pregnant women with moderate exacerbations were significantly less likely to receive systemic corticosteroids (56.5% versus 77.3% respectively, p = 0.011) but there was no difference noted for mild (18.9% versus 34.8%, p = 0.223) or severe/life threatening exacerbations (95% versus 88%, p = 0.617). At the time of discharge from the ED, pregnant women with both mild and moderate exacerbations were significantly less likely to receive prescriptions for prednisone (13.5% versus 47.8%, p = 0.007, and 50.9% versus 75.7%, p = 0.011 respectively) but there was no difference noted for severe/life threatening exacerbations (78.6% versus 72.7%, p = 0.628).
Table 5Corticosteroids administered in the emergency department by severity of asthma exacerbation and pregnancy status.
| Asthma severity | Mild | Moderate | Severe/life threatening | |||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Pregnant | No | Yes | p-value | No | Yes | p-value | No | Yes | p-value | |
| Systemic corticosteroids given in ED, % | 34.8 (n = 23) | 18.9 (n = 37) | 0.223 | 77.3 (n = 75) | 56.5 (n = 62) | 0.011 | 88 (n = 25) | 95 (n = 20) | 0.617 | |
| Corticosteroids given at discharge from ED, % | n = 23 | n = 37 | n = 75 | n = 59 | n = 22 | n = 14 | ||||
| None | 47.8 | 81.1 | 0.007 | 17.3 | 40.7 | 0.011 | 4.6 | 14.3 | 0.628 | |
| Prednisone | 47.8 | 13.5 | 75.7 | 50.9 | 72.7 | 78.6 | ||||
| Inhaled corticosteroids | 0 | 2.7 | 2.8 | 5.1 | 12.4 | 0.0 | ||||
| Both | 4.4 | 2.7 | 5.3 | 3.4 | 18.2 | 7.1 | ||||
ED = emergency department.
Year of treatment did not influence the decision to use systemic corticosteroids in either patient group, with similar results noted when subjects were divided into two groups: 1996–2004 and 2005–2009 to account for the possible influence of the updated asthma in pregnancy guidelines (data not shown).
5
Pregnant women exhibited a trend toward more frequent hospitalizations for their asthma exacerbations with 12.3% being admitted or observed for at least 24 h versus only 4.9% of non-pregnant women (p 0.066). More notable is the observation that pregnant women were nearly four times more likely than non-pregnant women to represent to this same institution’s ED for recurrent or persistent asthma symptoms within two weeks (9.7% versus 2.5%, p = 0.026). However, the small sample size precludes detailed analysis. In the small subset of women in whom pregnancy outcome data was available, there were no significant associations with use of systemic corticosteroids (Table 6).
Table 6Pregnancy related outcomes.
| Corticosteroids administered in ED | p-value | |||
|---|---|---|---|---|
| No | Yes | |||
| Occurrence of spontaneous abortion, % (n) | 8.1 (3/37) | 2.6 (1/38) | 0.358 | |
| Preterm labor, % (n) | 24.2 (8/33) | 11.4 (4/35) | 0.211 | |
| APGAR 1 min < 7, % (n) | 3.0 (1/33) | 19.4 (7/36) | 0.057 | |
| APGAR 5 min < 7, % (n) | 3.0 (1/33) | 2.9 (1/35) | 0.999 | |
| Trimester of pregnancy at time of ED presentation, % | First | 40.0 (22/55) | 30.0 (18/60) | 0.549 |
| Second | 45.5 (25/55) | 53.3 (32/60) | ||
| Third | 14.5 (8/55) | 16.7 (10/60) | ||
| Gestational age in weeks at time of delivery, mean [sd] (n) | 37.8 [2.1] 27 | 36.6 [5.9] 29 | 0.329 | |
| Birth weight in grams, mean [sd] (n) | 2947 [605] 32 | 3.192 [631] 32 | 0.119 | |
APGAR = Apgar score; ED = emergency department; sd = standard deviation; n = number.
Discussion
In this retrospective case-control analysis of acute asthma exacerbations, we found that pregnant and non-pregnant women presented to the ED with similar clinical characteristics and asthma severity. However, pregnant women were under-treated with systemic corticosteroids both in the ED and at the time of discharge when compared to their non-pregnant counterparts. Moreover, pregnant women were nearly four times more likely than non-pregnant women to return to the same ED within two weeks for recurrent or on-going asthma symptoms.
Our findings are similar to those noted by Cydulka et al
4
in a prospective study of pregnant women presenting to the ED with acute asthma exacerbations, where they noted that pregnant women were significantly less likely to be treated with systemic corticosteroids in the ED or at discharge when compared to non-pregnant women (44% versus 66%, p = 0.002 and 38% versus 64%, p = 0.002 respectively). These authors also noted that pregnant women were three times more likely to report on-going asthma symptoms at two week follow-up.Treatment differences according to pregnancy status may be based on concerns about potential harmful effects of medications on the fetus or lack of familiarity with current national guidelines. While the risks and benefits of any medication used during pregnancy must always be considered, little debate exists regarding the safety of inhaled corticosteroids (ICS) during pregnancy.
5
Investigators have shown that ICS improve asthma control during pregnancy11
, 12
and reduce hospitalizations.13
However, the use of these controller medications often decreases during pregnancy8
, 14
, 15
leading to an increase in ED visits.15
Although our study did not specifically address changes in medication adherence related to pregnancy, we do note with some concern that only 24% of the pregnant women in our study reported use of ICS at the time of their ED visit despite the evident severity of their disease (Table 2).The most notable difference between the treatment of pregnant and non-pregnant women in this study involved the use of systemic corticosteroids. Currently available guidelines and expert statements
5
, 16
recommend the use of systemic corticosteroids for acute asthma exacerbations during pregnancy similar to the management in non-pregnant patients, as uncontrolled maternal asthma may increase the risk of adverse perinatal outcomes.17
, 18
, 19
, 20
, 21
, 22
, 23
However, women with well-controlled asthma in pregnancy generally have good pregnancy outcomes.12
, 24
, 25
The use of oral corticosteroids in pregnant women is associated with some risk. Oral corticosteroid use during the first trimester of pregnancy has been associated with a 3-fold increased risk for cleft lip with or without cleft palate in women taking it for many reasons.
26
Schatz and colleagues reported an increased risk of pre-eclampsia,27
preterm labor,28
and low birth weights28
in the offspring of asthmatic women who received systemic corticosteroids even after adjusting for potential confounding variables. Bracken and colleagues found similar results in a prospective cohort of women.29
Perlow and coworkers described an increased incidence of diabetes mellitus, preterm labor and delivery, low birth weight infants, and premature rupture of membranes in 31 steroid-dependant pregnant asthmatics.30
Unfortunately, it remains difficult to clearly separate the potential effects of the medications from the potential effects of poorly controlled maternal asthma in many cases.There was a trend towards more frequent need for hospitalization in the pregnant women in our study, but this did not reach statistical significance, perhaps due to the small sample size. Despite this, the pregnant women were nearly four times more likely to return to the same ED with persistent or recurrent asthma symptoms within two weeks. This is similar to the findings noted by Cydulka and colleagues,
4
where the pregnant women were three times more likely to report on-going asthma symptoms at two week follow-up. Although lack of corticosteroid treatment in the ED or at discharge may have contributed to these findings, the small sample size prohibited detailed analysis. Additional contributing factors such as the impact of asthma-specific quality of life must be considered. Schatz and coworkers found that asthma-specific quality of life predicts subsequent exacerbations in pregnancy.31
Limitations
This study has several potential limitations. First, the retrospective study design limited our ability to more objectively characterize the subjects at the time of presentation. We attempted to account for this by including the exacerbation severity classification descriptions noted above. Similarly, we were unable to evaluate on-going asthma symptoms after discharge from the emergency department, and were limited by the fact that some subjects with persistent or recurrent asthma exacerbations may have chosen to seek further care at other facilities. Accordingly, we may have underestimated the possible effects of not treating pregnant women with asthma exacerbations with systemic corticosteroids in this study. Our statistical power is limited by the relatively small number of pregnant women (n = 123) presenting to the ED for acute asthma exacerbations. This may reflect the policy that all pregnant patients after a certain point in pregnancy be triaged to “labor and delivery” for any medical evaluation, or it may reflect an inability of the computerized database to identify all potential subjects. Since our patients were enrolled from a single academic ED and its community affiliated hospital, they may not be representative of the medical community as a whole. However, because emergency physicians in academic centers are more likely to have been exposed to national asthma guidelines than those practicing in other settings,
32
our findings may actually be an underestimation rather than an overestimation. Finally, the potential influence of the pregnant patients’ own desire (or lack thereof) to receive treatment with systemic corticosteroids could not be assessed in this retrospective study, and could have potentially accounted for some of the treatment differences we observed.Regardless of these limitations, we have identified an area of significant potential concern. Despite two nationally published guidelines specifically addressing the care of the pregnant patient with asthma,
5
, 10
there does not appear to have been a significant impact on the clinical care of these patients with an acute exacerbation in the emergency department setting when comparing our data to those published by Cydulka and colleagues over a decade ago.4
In summary, we found that in this population of asthmatics presenting to a tertiary emergency department with acute asthma exacerbations, significant treatment disparities existed between pregnant and non-pregnant women. Failure of the pregnant women to receive adequate treatment for their exacerbations may have contributed to prolonged or recurrent symptoms and more frequent healthcare utilization. Poorly controlled asthma in pregnancy increases the risk of adverse perinatal outcomes and potential harm to the fetus is more likely to result from severe uncontrolled asthma than from the medications used to treat it.5 Pregnancy should be considered an indication for maximizing therapy during an exacerbation, rather than withholding it. All members of the healthcare team should work together to ensure optimal care of the pregnant asthmatic.
Author contributions
Dr. McCallister: contributed to the overall study design and development; data collection and management; oversight of the data analysis; and the writing, review, and approval of the manuscript.
Ms. Benninger: contributed to the overall study design and development; data collection; and the writing, review, and approval of the manuscript.
Dr. Frey: contributed to the data collection; and the review and approval of the manuscript.
Mr. Phillips: contributed to the data analysis; and the writing, review, and approval of the manuscript.
Dr. Mastronarde: contributed to the overall study design and development; oversight of the data analysis; and the writing, review, and approval of the manuscript.
Conflict of interest statement
None.
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Article info
Publication history
Published online: June 23, 2011
Accepted:
May 25,
2011
Received:
February 16,
2011
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