asthma exacerbations and environme”>American Journal of Emergency Medicine (2011) 29, 1074-1082

Original Contribution

Adult asthma exacerbations and environmental triggers: a retrospective review of ED visits using an electronic medical record

Larissa May MD ^a,?, Marianne Carim MD ^b, Kabir Yadav MD ^a

^aDepartment of Emergency Medicine, The George Washington University, Washington, DC 20037, USA

^bDepartment of Internal Medicine, The George Washington University, Washington, DC 20037, USA

Received 27 January 2010; revised 2 June 2010; accepted 22 June 2010

Abstract

Background: Despite familiarity with triggers for asthma, there is little recent study on the association of triggers with the emergency department (ED) presentation of adult asthma exacerbation.

Methods: Retrospective electronic chart review of adult patients treated in an urban teaching hospital ED with chief complaint and Diagnostic coding related to asthma and upper respiratory tract infection (URI) was conducted. Monthly aeroallergen data and environmental conditions were obtained from a local allergen extract laboratory and local government sources. Data analysis was performed using Newey-West Time series regression modeling with adjustment for autocorrelation or ordinary least squares linear Regression modeling using outcome variables of asthma visits and admissions.

Results: There were 56 747 visits, with 554 asthma visits and 1 514 URI visits. Asthma visits (R² = 0.631) were positively correlated with tree pollen counts (correlation coefficient = 0.458 [0.152-0.765]) and average humidity (correlation coefficient = 1.528 [0.296-2.760]). Asthma admissions (R² = 0.480) were negatively correlated with average temperature (correlation coefficient = -0.557 [-1.052 to

-0.061]) when adjusting for confounding by fine particulate matter.

Conclusions: The ED acute asthma exacerbation presentation is positively correlated with tree pollen and humidity, whereas need for admission is associated with dropping temperatures. These results reinforce the need for vigilance during periods of increased risk and perhaps focused preventative strategies.

(C) 2011

Background

Asthma is a chronic lung disease responsible for tremendous morbidity and mortality, which has increased in prevalence in the United States over the past few decades [1]. In 2004, there were 1.8 million visits to emergency departments (EDs) for asthma (64 per 10 000 people). Death

* Corresponding author. Tel.: +1 202 741 2920.

E-mail address: [email protected] (L. May).

rates in 2003 were 1.4/100 000 population for adults, significantly higher than that for children (0.3/100 000) [2]. Hospital admission is an important risk factor for asthma mortality [3]. Strategies to prevent morbidity and mortality for acute asthma exacerbations (AAE) thus focus on early recognition and intervention. To address the recent increase in asthma prevalence as well as the Severity of asthma exacerbations, research and clinical management have focused on better characterization and understanding of asthma triggers and their pathophysiology. Pollen counts and

0735-6757/$ - see front matter (C) 2011 doi:10.1016/j.ajem.2010.06.034

air particulate matter (PM) have been shown to be important triggers to AAE alongside weather changes and viral respiratory tract infections.

Particulate matter is the most serious component affecting AAE and is composed of all types of solid and liquid particulates including pollen grains. The World Health Organization estimated that inhalation of PM is responsible for 500 000 excess deaths each year worldwide [4].

One large study demonstrated an association between pollen and small particulates with AAE in children [5]. Other studies have demonstrated a lag time effect between pollen counts and AAE [6-8]. Other pollutants such as carbon dioxide, sulfur dioxide, and ozone are believed to contribute to AAE by priming the lung for reactivity to pollen exposures [9].

Ozone and humidity have been identified as environmen- tal factors associated with asthma exacerbations. Recently published studies have shown a positive correlation between ozone exposure and AAE in children in urban populations [10]. One prevailing theory is that an increase in ozone exposure diminishes lung function; which in turn may lead to increased biomarkers of respiratory and systemic inflamma- tion [11]. Ozone may be the primary pollutant related to hospital admissions in pediatric patients; however, this association appears less evident for adults [12].

Prior studies have suggested a link between adult AAE and Viral illness [13-16]. Nonetheless, there are limited recent data on the effect of these triggers on adult asthma presentation to EDs. Better understanding of the triggers associated with AAE ED visits could help focus ED and primary care strategies on early diagnosis, prevention, and upper respiratory tract infections“>control of asthma symptoms.

Objective

The first objective of our study was to analyze the association of adult asthma exacerbations with the following factors: pollen counts, upper respiratory tract infection (URI) chief complaints, temperature, humidity, PM, and ozone levels in the Washington, DC, area using retrospective electronic medical record (EMR) data from an urban ED and local environmental data.

The second objective was to characterize the severity of asthma exacerbations, as identified by asthma admissions, and correlate them with individual asthma triggers.

Methods

We conducted a retrospective chart review of our urban academic university ED system EMR (Picis, Inc, Wakefield, MA) for the period of June 1, 2005, through May 30, 2006. All adults older than 18 years who were assigned a disposition diagnosis of “asthma” or “asthma exacerbation” by International Classification of Diseases, Ninth Revision

codes in our EMR were included in this study. The study was approved by our Institutional Review Board.

The EMR in use at our institution (Picis, Inc.) allows free text of the chief complaint as well as entry from a pull-down menu by the triage nurse. Final diagnosis is entered from a predetermined set of International Classification of Dis- eases, Ninth Revision codes used for billing purposes, and is entered at the time of patient disposition. Thus, in some cases, the chief complaint and final diagnosis are the same if the clinician did not have additional information on the diagnosis at the time of disposition. All diagnoses are assigned at time of patient disposition from the ED: discharge from the ED, admission to the Inpatient unit, or transfer to another facility. We collectED asthma admission rates to use as a surrogate outcome for Asthma severity.

We chose to include patients with diagnoses of asthma only to avoid including patients presenting with wheezing who were diagnosed with bronchitis or other respiratory conditions.

Pollen counts

We obtained aeroallergen data from the Walter Reed Army Medical Center’s US Army Centralized Allergen Extract Laboratory for the months of June 2005 through May 2006. The aeroallergen data were reported as total counts per day of ragweed and tree pollen in units of grains per cubic meter. Monthly averages of tree and ragweed pollen, for which we had the most complete data, were calculated by dividing the monthly total counts by the number of days with measured tree or ragweed pollen count for that month.

Upper respiratory tract infections

Patients with possible viral respiratory illnesses were identified from retrospective chart review of presenting chief complaint as determined by the triage nurse. Elements that were considered consistent with URI included URI and sinusitis.

Particulate matter

We obtained fine PM data (PM 2.5 um) collected by the Metropolitan Washington Council of Governments (MWCOG, http://air.mwcog.org). The monthly average for PM 2.5 was used in our analysis. Data were averaged from 3 collection sites for the Washington, DC, area for all days where data were available. We chose to include all metropolitan sites in our averages because of patients working and living in multiple zip codes in the Washington, DC, area.

Ozone

We obtained ozone averages from air quality data collection by the MWCOG (http://air.mwcog.org). The monthly average for maximum ozone was used in our analysis. Data were averaged from 18 collection sites for the

Fig. 1 Tree pollen, ragweed, and asthma exacerbation averages.

Washington, DC, area for all days where data were available. We chose to include all metropolitan sites in our averages because of patients working and living in multiple zip codes in the Washington, DC, area.

Temperature and humidity

Average monthly temperatures for the area were obtained from the DC National Weather Web site for the Eastern Region Headquarters. Humidity data were obtained from The Johns Hopkins University Applied Physics Laboratory located in Laurel, MD, for the Washington, DC, metropolitan area. The data were available as minimum and maximum relative humidity (RH). For the purposes of our analysis, we computed a monthly average RH.

Data analysis

Data were analyzed for trends by both visualization and Time series analysis. Alongside monthly AAE ED visits and AAE admissions, we graphed pollen averages, URI chief complaints, air pollution indices, temperature, and humidity. Time series analysis was performed using multivariate Newey-West time series regression modeling with adjust- ment for autocorrelation or ordinary least squares linear regression modeling in Stata 10.1 (StataCorp, College Station, TX) using outcome variables of asthma visits and asthma admissions. Backward stepwise model building was

performed with appropriate regression diagnostics.

Results

There were 56 747 total ED visits during the study period, with 554 asthma visits and 1514 URI visits.

Approximately 92% of patients presenting with the chief complaint of asthma or wheezing were assigned an ED diagnosis of asthma; the majority of the remaining 8% of patients with asthma or wheezing complaints were assigned a diagnosis of Acute bronchitis.

Pollen trends

For our data, there were 2 dominant peaks for ED adult asthma exacerbations: one in autumn (September) and one in

Fig. 2 Hospital admission rates for AAE vs tree and ragweed pollen counts.

Fig. 3 Acute asthma exacerbations vs URI chief complaints.

the spring (March). The autumn peak of asthma exacerba- tions follows the peak for ragweed by approximately 1 month, suggesting a lag period. The spring peak shows similar trends when compared with the tree pollen curve. In our regression analysis, we found an association between tree pollen counts and AAE in the spring (Fig. 1).

We evaluated the graphical relationship between Severe asthma exacerbations (using the surrogate of asthma admissions) and pollen counts. Fig. 2 represents pollen counts plotted against hospital admission rates for AAE as a percentage of total AAE. The admission rates for AAE peaked during the month of February, which does not fall during increased periods of pollen; furthermore, there is no consistent trend for AAE admissions and pollen counts.

Upper respiratory tract infections

To analyze for trends, monthly counts of AAE were plotted against URI chief complaints (Fig. 3); and asthma admission counts were plotted against URI complaints (Fig. 4). We found no association between URI chief complaints and AAE.

Particulate matter and ozone levels

The monthly counts of AAE were analyzed for trends compared with average maximum air quality (PM 2.5 and ozone) and are graphically represented in Fig. 5. There is no discernable graphical relationship between PM or ozone and AAE; however, asthma admissions were negatively corre- lated with temperature when adjusting for confounding by fine PM.

Temperature and humidity

Temperature and RH were plotted against AAE and admissions trends. There seems to be a direct correlation between both temperature and humidity in relation to both AAE and admissions (Fig. 6). In multivariate analysis,

average RH and asthma visits were found to be positively correlated, whereas temperature was negatively correlated, with asthma admissions.

Summary of environmental triggers and AAE

As seen in Fig. 7, the only environmental trigger that bears a strong graphical relationship to AAE in our data is that for tree pollen, with no relationship for fine PM or ozone.

Time series analysis

Asthma visits (R² = 0.631) were positively correlated with tree pollen counts (correlation coefficient = 0.458 [0.152- 0.765]) and average humidity (correlation coefficient = 1.528 [0.296-2.760]). Asthma admissions (R² = 0.480) were negatively correlated with average temperature (correlation coefficient = -0.557 [-1.052 to -0.061]) when adjusting for confounding by fine PM.

Discussion

In this study, AAE visit trends most closely follow the rise in tree pollen counts and rising humidity, with little

Fig. 4 Acute asthma exacerbations admissions vs URI chief complaints.

Fig. 5 Acute asthma exacerbations vs fine PM (2.5 um) and ozone.

relationship to ozone or PM. Asthma severity as marked by asthma admission rates appears to peak in February, possibly corresponding to a drop in temperature. Thus, whereas AAE presented to the ED after a rise in tree pollen counts, severe asthma exacerbations peaked during periods of colder temperatures. It is possible, however, that this peak may be instead related to the peak of influenza during the 2005-2006 season. We did not specifically evaluate visits for influenza- like illness in this analysis, and URI visits may not be a good indicator for influenza-like illness [17]

Pollen

Our results are consistent with prior studies of ED asthma exacerbations and pollen counts. A study of the impact of pollen on more than 5000 asthma visits in New York City EDs for 3 years showed that ED asthma visits graphically mirrored pollen counts in New York City [18]. A second study of acute asthma in Oregon showed that ED and urgent care admissions peaked with very high grass pollen counts [19]. Other studies have shown a lag time effect between pollen counts and AAE [6-8] air pollutants such as CO₂, SO₂, and ozone may also cause an increased production of pollen as well as contribute to the priming of lung reactivity to pollen exposures [9].

There is pathophysiologic basis supporting the relation- ship of pollen and exacerbations of allergic diseases. Pollen spores contain significant amounts of antigenic material and, given their small size, are easily disseminated in the air and readily inhaled to reach the peripheral airways, causing an AAE in already sensitized individuals [20-23]. Other investigators have hypothesized that fine PM in urban areas may cause alveolar inflammation resulting in the release of acute Inflammatory mediators that favor acute episodes of respiratory diseases [24]. One large study in children suggests strong synergistic associations between pollen and small particulates with AAE [5]. The relationship in older studies, however, is not as clearly defined [25-27].

URI complaints

We found no association in this study between URI complaints and AAE counts in this analysis. Rather, AAE admission rates peak the month preceding the peak in URI complaints. Because we analyzed monthly rather than daily data, it is plausible that a subtle relationship for the severity of AAE early in the rise of URI activity may not have been detected using our methods.

A longitudinal study in England suggested that respira- tory viral infections are commonly associated with asthma

Fig. 6 Acute asthma exacerbations vs temperature and average RH.

Fig. 7 Summary of AAE vs environmental triggers.

exacerbations in adults [10]. A study among 49 persons, ages 3 to 60 years, found that 55% of symptomatic respiratory tract infections including rhinovirus, respiratory syncitial virus (RSV), and influenza type A occurred with asthma [11]. In another study, 89% of colds were associated with asthma symptoms; and 24% of laboratory-confirmed non- bacterial infections were associated with reductions in main peak expiratory flow rate [10]. However, viral pathogens in patients with asthma exacerbations might not be as prevalent in adults as expected [28]. Further study in the adult population is recommended to determine the true relation- ship and whether asthma complaints may serve as a surrogate for an increase in viral respiratory pathogen activity.

The severity of asthma is indicated by admission to the hospital. A study aiming to document the incidence of respiratory tract infection (RTI) in adults hospitalized for acute asthma found that, over 12 months, 37% of adult patients with acute asthma admitted to a hospital had evidence of recent RTI, including rhinovirus, influenza, RSV, and adenovirus. Seventy-nine percent of RTIs found in the patient group were viral [29]. However, in our data, we found no association between asthma admissions and URI complaints. It is possible that URI may precede the AAE in some cases; however, it may not be the presenting complaint.

Particulate matter and ozone

Our study found no correlation between increased AAE and ozone or PM counts, contrary to prior studies showing an association between daily concentrations of ozone and ED visits in other cities with a chief complaint of asthma [30-34], at least for pediatric patients. It is possible that PM may be a confounder for asthma admissions and thus may be synergistic with other triggers or that ozone is not a trigger

for adult AAE. Nonetheless, other studies have not shown a significant association, perhaps because of relatively low ozone concentrations [35-37]. Ozone levels are not low in this region, although ozone reporting was incomplete; thus, it is possible that this study was not able to show an association between AAE and ozone.

A study showing an association between particle air pollution and ED visits looked at respirable PM (PM 10), whereas our study evaluated fine PM [32]. PM 2.5 has also been implicated in indoor pollution in neighborhoods with high asthma rates [38].

We cannot imply cause and effect for our data because there may be other coexisting factors and confounders that were not accounted for in this study, such as other air pollutants.

Temperature and humidity

We found a positive association between asthma visits and average humidity and an association of asthma admissions with decreasing temperatures.

Temperature (either very cold or very hot) has been shown to affect AAE. At high temperatures and with more sunlight, emissions are more likely to be converted to ozone at ground level, another known factor that plays a role in asthma exacerbations [39]. At Low Temperature, air tends to hold less moisture; and the dry air acts as an irritant, possibly causing these AAE [40-42]. Future studies evaluating weather patterns and including photochemical smog and haze might provide additional insight into AAE.

In certain cases of AAE, the severity of illness necessitates management in an intensive care setting. To predict an increase in AAE cases requiring management in an intensive care unit, knowledge of the triggers leading to this severity would be clinically useful. Based on our data, admissions for asthma peaked during the winter season

(February), whereas AAE overall peaked in the spring and fall seasons (September and March). Thus, the peak of hospital admissions for asthma does not seem to correspond to increased AAE or pollen counts and may be related to trends in influenza or pneumonia, which could account for more severe exacerbations requiring hospitalization. Further study into this relationship is warranted, as focused Preventative measures to prevent severe AAE may empha- size influenza And pneumonia vaccination over the control of allergic rhinitis.

The results from this study are consistent with previous studies showing an association between pollen counts and AAE, and PM and AAE, although many of the studies done were on children and not adults.

Limitations

Our data are based on a retrospective review of a single institution’s EMR system. This analysis should be replicated in other institutions in our geographic location to confirm the potential benefit of monitoring pollen counts. The pollen count data were limited in that these were not reported on a daily basis, but according to available manpower at the facility, a limiting factor for determining specific daily trends. In fact, many of the studies on air pollutants cited compare daily pollutant levels rather than monthly averages; because we did not look at daily counts of asthma compared with Environmental factors, we may not have detected an association on the daily level.

Furthermore, although this study provides compelling evidence of trends for pollen counts and asthma for our region, we cannot conclude a causal relationship between ozone, PM, pollen, or URI and AAE, only a correlation. In addition, potential confounders such as other pollutants were not considered. We were limited to the analysis of ozone and PM because these are the pollutants reported by the MWCOG, and we did not have data available on other environmental pollutants that may play a role in AAE.

We did not include pediatric patients in our study, as our institution primarily sees adult patients and little recent research has focused on triggers for ED visits for asthma in adults, who tend to have a higher mortality from asthma. Further study in children should be undertaken because AAE in children have been found to correlate with URI, particularly RSV and influenza [43]. Many studies in children have shown an association of RTI with asthma symptoms [39,44-48]. Although the older literature for children clearly suggests a link between viral illness and asthma exacerbation, recent literature for children is conflicting [39,49]. Furthermore, many of the studies cited looking at air pollutants and asthma have been undertaken in children. It is possible that the pattern of AAE differ for adults from children.

The patterns of AAE relationship to air pollution may exhibit variability from year to year and by geographic

location; thus, this study should be expanded to include different geographic locations and over a longer period. Of particular concern with time series analysis is the issue of seasonality, which requires far more than a year’s worth of data to analyze.

Our URI data are limited by the lack of laboratory confirmation of viral respiratory pathogen activity. It is possible that URI complaints may have been a reflection of seasonal allergies rather than infectious etiology.

It is also possible that the severity of asthma in our adult ED population may be greater than for that presenting to outpatient clinics; thus, the results may not be generalizable to all asthma exacerbations.

Although our temperature and RH data were obtained from sources located near Washington, DC, there may have been some minor variations in the values for our location that could have had a small albeit real effect on the results.

Conclusions

Acute asthma exacerbations in the adult population during the spring peak show similar trends to tree pollen counts in the Washington, DC, area. In addition, peaks in asthma admissions are not associated with pollen counts but are associated with colder weather and perhaps the influenza season. Research into asthma triggers in adults and ED asthma visits should be continued to facilitate primary prevention of asthma exacerbations and decreased ED visits. In addition, ED physicians should consider more aggressive management of asthma exacerbations during times of rising pollen counts and during the influenza season. The increasing use of EMRs in EDs should facilitate further research into trends for asthma and its triggers, including URI, air pollution, and climate factors. Further understand- ing of which factors are involved in AAE may provide valuable information that may allow both primary care and emergency physicians to institute focused preventative and Therapeutic measures, including vaccination for pneumonia and influenza, treatment of seasonal allergies, and recogni- tion of factors that may increase the severity of AAE and thus the need for admission.

Acknowledgments

The authors would like to express their sincere appreci- ation to Susan Kosisky and her staff at the United States Army Centralized Allergen Extract Laboratory, Department of Allergy-Immunology, Walter Reed Medical Center, for providing aeroallergen data; to Jennifer Desimone and the staff at the Metropolitan Washington Council of Govern- ments for providing air quality data for this study; and to Erin Jones, MSPH, for assisting with data collection.

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