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(Chest. 2003;124:653-659.)
© 2003 American College of Chest Physicians

Effect of Age on the Development of ARDS in Trauma Patients*

Craig J. Johnston, MD; Gordon D. Rubenfeld, MD, FCCP and Leonard D. Hudson, MD, FCCP

* From the Department of Medicine (Dr. Johnston), Division of Pulmonary and Critical Care Medicine (Drs. Rubenfeld and Hudson), University of Washington School of Medicine, Harborview Medical Center, Seattle, WA.

Correspondence to: Gordon D. Rubenfeld, MD, MSc, Pulmonary and Critical Care Medicine, Harborview Medical Center, Box 359762, 325 9th Ave, Seattle, WA 98104; e-mail: nodrog{at}u.washington.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: The purpose of this study was to determine the independent effect of age on the risk of developing ARDS in patients with trauma.

Design: Prospective cohort study.

Setting: Level I trauma center.

Measurements and results: A total of 4,020 consecutive trauma patients who were > 12 years of age were identified through the Harborview Medical Center Trauma Registry over a 3-year period. During this time, 484 of the trauma patients (12%) developed ARDS, as identified by the Harborview Medical Center ARDS Registry. Patients who developed ARDS were, on average, older (mean [± SD] age, 44.0 ± 18.8 vs 40.2 ± 20.0 years, respectively; p < 0.0001) and had higher injury severity scores (23.7 ± 11.3 vs 18.0 ± 10.3, respectively; p < 0.0001) than trauma patients who did not develop ARDS. The maximum unadjusted odds ratio for developing ARDS was 2.93 (95% confidence interval, 1.91 to 4.50) for the group 60 to 69 years of age compared to the group 13 to 19 years of age. Patients aged >= 80 years had an equal risk of developing ARDS compared to those age 13 to 19 years.

Conclusions: Age demonstrated a complex relationship with risk for ARDS development. Older patients showed increasingly higher risks for ARDS development up to 60 to 69 years of age, when the risk for ARDS declined. We concluded that older patients are at significantly greater risk of developing ARDS when compared to younger patients, while the oldest patients may be at less risk.

Key Words: age distribution • ARDS • epidemiology • multiple trauma


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
By the year 2030, the number of persons in the United States aged >= 65 years is projected to more than double from 34 million (13% of the current US population) to approximately 70 million (20% of the projected future US population).1 This increase in the number of older persons will be accompanied by an increase in age-related disease, which will have a profound impact on the future of health care and health-care professionals.2 3 4 5 Despite this potential public health crisis, the effect of age on the incidence of many diseases has not been fully characterized. To date, the effect of age on the incidence and risk of ARDS has not been described clearly.

Previous studies6 7 8 9 10 have identified several factors that modify or increase the risk of ARDS development in the presence of an underlying high-risk condition such as sepsis, aspiration, and trauma. One factor, severity of illness, as measured by the APACHE II (acute physiology and chronic health evaluation) score or injury severity score (ISS), in patients with a predisposing condition, has been shown to be an independent risk for the development of ARDS.7 Gender,7 chronic alcohol abuse,11 12 and cigarette smoking12 also have been proposed as factors that independently increase the risk for developing ARDS.

Despite the fact that many previous studies have illustrated a clear relationship between increased age and increased mortality13 14 15 16 17 18 19 in patients with ARDS, no studies to date have shown a clear relationship between increased age and the development of ARDS in patients with similar underlying risk conditions. In addition, few studies have prospectively studied risk factors for their association with ARDS using the current definitions most widely used by researchers and clinicians, those developed by the 1994 American-European Consensus Conference (AECC) on ARDS.20

To address these questions, we combined the data from two prospective cohorts to determine the relationship between age and the risk of ARDS in patients with trauma.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Design, Setting, and Data Collection
The design was a prospective cohort study. Data were obtained from the Harborview Medical Center Trauma Registry and ARDS Registry. The Trauma Registry is a computerized database that contains information concerning all patients evaluated for traumatic injury at Harborview Medical Center who either were admitted to the hospital or died in the emergency department. The registry is used for quality improvement and clinical research, and provides data to the Washington State Trauma Registry.21 The ARDS Registry contains clinical data from all patients identified with ARDS through the daily ICU screening of mechanically ventilated patients at Harborview Medical Center.18

Study Population
From January 1996 to January 1999, 4,020 consecutive patients who were > 12 years of age and had trauma as a principal hospital admission diagnosis were identified at Harborview Medical Center, a county teaching hospital of the University of Washington School of Medicine and a level I trauma center serving four northwestern states that is located in Seattle, WA. During the same 36-month period, 484 trauma patients were identified as having ARDS through the ARDS Registry. Patients <= 12 years of age were transferred to a children’s hospital during this time period and therefore were not followed by either registry.

Criteria for Diagnosis of ARDS
All patients were followed for their entire hospital course. Patients were considered to have developed ARDS if they met the following 1994 AECC definition20 : PaO2/fraction of inspired oxygen ratio of <= 200 mm Hg; bilateral pulmonary infiltrates consistent with pulmonary edema; pulmonary artery occlusion pressure of <= 18 mm Hg when measured; or, in the absence of a pulmonary artery catheter, no clinical evidence of left atrial hypertension.

Variables
The outcome variable for this analysis was the development of ARDS. The exposure variable was age, which was coded as a continuous variable and by decade. Possible confounding variables were those considered to be, or found to be on bivariate analysis, associated with both age and the development of ARDS. On the basis of a review of previously published analyses, we determined that severity of injury, as reflected by the ISS and abbreviated injury scale (AIS), would be included in the analysis.6 7 8 9

Statistical Analysis
Univariate comparisons between trauma patients who developed ARDS and those who did not were evaluated with the {chi}2 test or the independent samples t test, and 95% confidence intervals (CIs) were determined on all odds ratio (OR) calculations. For the confounding variables, ISS and AIS, we compared the mean differences using the independent samples t test.

We considered the following several different ways to code the age variable: as a continuous variable; by decade; and as a dichotomous variable (ie, < 65 vs >= 65 years of age). Each has advantages and disadvantages, which are presented in the analysis. To identify the crude effect of age, we used a logistic regression model with ARDS development as the dependent variable and age coded as the independent variable.

To identify the effect of age independent of injury severity, we constructed hierarchical multivariate logistic regression models, which included age in decades, and then added ISS, AIS, and the two-way interaction terms age x ISS, age squared, and ISS squared. Variables were left in the model if the p value for the coefficient was < 0.05. All statistical analysis was performed with a statistical software package (SPSS, version 9.0; SPSS, Inc; Chicago, IL).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Patient Characteristics
Table 1 shows the baseline characteristics of the patient groups stratified by trauma patients who did not develop ARDS and those who did. Of the 4,020 trauma patients who were identified for the study, 484 (12%) developed ARDS. Patients with ARDS were older than patients who did not develop ARDS (mean [± SD] age, 44.0 ± 18.7 vs 40.2 ± 20.0 years, respectively; p < 0.0001). The male gender was predominant in each group (ARDS patients, 72.3%; non-ARDS patients, 73.0%). For the study group as a whole, 3,010 patients (74.9%) were white, 296 patients (7.4%) were African-American, 237 patients (5.9%) were Hispanic, 216 patients (5.4%) were Asian, 93 patients (2.3%) were Native American, and 168 patients (4.2%) were categorized as "missing" or "other race." Patients with and without ARDS had varying incidences of mechanisms of injury, with the most common for the group as a whole being motor vehicle accidents and falls (Table 2 ). Higher incidences of motor vehicle accidents (p < 0.0001), pedestrian accidents (p = 0.016), and motorcycle accidents (p = 0.037) as presenting mechanisms of injury were seen among those patients who developed ARDS. However, patients who developed ARDS had lower incidences of fall (p = 0.047) or gunshot wound (p = 0.046) as presenting mechanisms of injury. Patients with ARDS had more severe injury than did patients who did not develop ARDS (mean ISS, 23.7 ± 11.3 vs 18.0 ± 10.3, respectively; p < 0.0001) [Table 3 ]. AIS scores for the thorax, abdomen, spine, and extremities were significantly higher in trauma patients who developed ARDS than in trauma patients who did not (all p < 0.0001). However, the AIS for the severity of head injury was significantly higher in patients who did not develop ARDS than in those who did (p < 0.0001). The mortality rate was higher in the trauma ARDS patients than in the trauma non-ARDS patients (20.0% vs 11.9%, respectively; p < 0.0001) [Table 3 ].


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  		Table 1. Baseline Characteristics of Trauma Patients Stratified by Development of ARDS

 

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  		Table 2. Mechanisms of Injury in Trauma Patients Stratified by Development of ARDS

 

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  		Table 3. Comparison of Confounding Characteristics ISS and AIS*

 
In the logistic regression analysis, the unadjusted OR for age as a continuous variable was 1.009 per year (95% CI, 1.005 to 1.014), while age as a dichotomous variable (>= 65 years or < 65 years) was not statistically significantly associated with ARDS (OR, 1.23; 95% CI, 0.96 to 1.58). However, when age was broken down into decades, with the group of patients who were 13 to 19 years of age as a reference category, patients aged 30 through 79 years all exhibited statistically significant ORs for ARDS development. Figure 1 illustrates the unadjusted ORs for the development of ARDS and the trend with increasing age by decades. ORs ranged from 1.87 (95% CI, 1.28 to 2.71) in the group 30 to 39 years of age up to 2.93 (95% CI, 1.91 to 4.50) for the group 60 to 69 years of age. Risk then declined in the group 70 to 79 years of age (OR, 2.45; 95% CI, 1.55 to 3.87), and further declined in the group >= 80 years of age (OR, 1.16 [not statistically significant]; 95% CI, 0.65 to 2.06).



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  		Figure 1. Unadjusted ORs for ARDS development in trauma patients. 95% CI bars are presented with the group of patients 13 to 19 years of age used as the referent (p < 0.05 for trend).

 
After controlling for ISS, the adjusted OR increased in all age groups (Fig 2 ). The ISS-adjusted OR of developing ARDS for patients aged 60 to 69 years (OR, 3.42; 95% CI, 2.21 to 5.29) was three times greater than that of patients aged 13 to 19 years, and the group 70 to 79 years of age had an OR of 2.88 (95% CI, 1.81 to 4.41). Despite expanding the reference group to include ages 13 to 29 years, an elevated risk of ARDS development continued to be observed in the groups of patients who were 60 to 69 years of age (OR, 2.84; 95% CI, 1.98 to 4.05) and 70 to 79 years of age (OR, 2.39; 95% CI, 1.61 to 3.55). A side-by-side comparison of adjusted and unadjusted OR trends by age in decades is presented in Figure 3 .



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  		Figure 2. Adjusted OR for ARDS development in trauma patients. Multivariate ORs are adjusted for ISS and statistically significant AIS. 95% CI bars are presented with the group of patients 13 to 19 years of age used as the referent (p < 0.05 for trend).

 


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  		Figure 3. Comparison of unadjusted vs adjusted ORs for the development of ARDS in trauma patients, with the group of patients 13 to 19 years of age used as the referent (p < 0.05 for trends).

 
To evaluate the effect of injury severity, we included ISS and AIS into the multivariate logistic regression models. In all models tested (ie, ISS, AIS, and both ISS and AIS), age remained statistically significantly associated with ARDS development. In fact, there was no evidence of confounding by injury severity (ie, the coefficient for age did not decrease), and in fact the coefficient for age increased when injury severity was included in the model. A similar increase was observed when adjusting for AIS. Results of our tests for two-way interactions revealed significant adjusted R2 values, with p < 0.05 for all models containing age squared. Therefore, the decline in risk after age 69 years is statistically significant. The variables age x ISS and age x AIS were not statistically significant when added to the complete model containing age, ISS, AIS, and age squared.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
The principal findings of this study were that age demonstrated a complex relationship with the risk of ARDS development. Older trauma patients showed an increasingly higher risk of ARDS development up to 60 to 69 years of age, after which the risk of ARDS declined with increasing age. This effect was not due to the severity of trauma, as measured by ISS or AIS. In fact, after controlling for these variables, the effect of age became more pronounced. These findings are consistent with the conclusion that age is a significant independent risk factor for the development of ARDS. However, we were surprised to find that the risk of ARDS development peaked in the range of 60 to 69 years of age and then actually declined in the oldest patients (ie, those >= 70 years of age). This peak may be explained by a couple of previously implicated ARDS risk modifiers (ie, fluid management22 and the number of blood transfusions6 ). Additional blood products is one possible mechanism whereby physicians may be less likely to tolerate low hematocrit levels and more likely to transfuse older patients. Although not evaluated in our study, it is possible that older patients are at greater risk of developing ARDS because, even after controlling for injury severity, they receive more fluids or blood products.

In contrast to the peak in risk, the apparent decline in the risk of ARDS development in the oldest patients may be due to the interplay between age as a risk factor for ARDS and age as a risk factor for death after trauma. In the oldest patient population, patients may die from their underlying trauma or age-biased care before they have a chance to develop ARDS. Alternatively, patients in the oldest patient group may actually be at a lower risk of developing ARDS due to biological differences that occur in the elderly.

Previous studies22 23 have illustrated the existence of age-biased care, in which, compared to similar younger patients, seriously ill older patients receive fewer invasive procedures and hospital care that is less resource-intensive and less costly. Therefore, the oldest trauma patients may not be admitted to the ICU where their lung injury would be diagnosed or may receive less aggressive treatment in the field or emergency department so that they died before they developed ARDS.

It is also possible that the oldest trauma patients are so frail that, regardless of the aggressiveness of their treatment, they die of other injuries before they develop ARDS. However, further analysis of our data revealed that of all the patients who died while in the hospital, those >= 80 years of age survived for an average of 7.4 days, while the average time to ARDS diagnosis in the same age group was only 4.9 days. Therefore, older patients, on average, appear to survive long enough to develop ARDS before they die from their injuries.

Furthermore, changing immunologic responses with age may add a biological explanation for the observed decline in risk. Those patients that live to be > 70 or 80 years of age prior to their trauma arguably could have genetically protective mechanisms against ARDS development such as the following: a genetic lack of coagulation abnormalities, in which microvascular thromboemboli have been described as playing a role in the injury that occurs to lung vessels in ARDS24 ; or a genetically favorable control of apoptosis pathways, in which it has been illustrated that elevated levels of FAS ligands in the alveoli of ARDS patients may help to increase apoptosis and may lead to lung injury.25 26

Study Limitations
There are several limitations to our study. It is possible that some other confounding variable accounts for the observed association between age and mortality. We were unable to address the influence of several potential confounders, including APACHE II scores and preexisting medical conditions, due to a lack of sufficiently detailed information on these variables in our data set. However, some investigators believe that anatomic injury scoring (eg, the ISS used in our study) is a superior risk adjustor to APACHE in the trauma population.27 In addition, we were unable to control for comorbid diseases, including tobacco and alcohol abuse, that have been associated with ARDS.12 Furthermore, despite utilizing the current accepted diagnostic criteria for ARDS and relying on prospective screening,20 it is possible that some older patients are at greater risk of cardiogenic edema than of noncardiogenic edema, and our observations are limited by our inability to exclude cardiogenic pulmonary edema in all older patients by invasive or noninvasive diagnostic techniques. However, neither the most recent ARDS multicenter clinical trial28 nor the most recent ARDS epidemiologic studies29 30 required specific diagnostic measures to exclude left atrial hypertension. In these studies, as in our study cohort, the assessment was left to bedside clinical discretion in accordance with the AECC ARDS definition,20 and the current diagnostic and research standards. Finally, our study took place in a single level I trauma center. Although patients were drawn from a variety of ethnic groups, socioeconomic backgrounds, and geographic regions, we cannot determine whether our results are generalizable to the community hospital setting.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
The results of our study may have several important implications. Clinically, in an ongoing effort to improve the ability to prospectively identify critically ill patients who develop ARDS, these data are valuable for appropriately designing clinical trials. Because of their increased risk of ARDS, older patients should be evaluated for (not excluded from) clinical trials that are aimed at reducing the incidence of ARDS. Considering the broad population and large sample size of our study, it also may be reasonable to generalize the hypothesis that age may be predictive of ARDS development in other high-risk patients (ie, those with sepsis, aspiration, or pneumonia). Furthermore, based on the fact that many previous studies have identified that mortality is highest in older ARDS patients,13 14 15 16 17 18 19 the overall ARDS mortality rate could rise as the population ages. Finally, as the US population ages, the possible age-biased care revealed by our study may become a very important topic for health-care professionals and the health-care system to address in the future.


   Footnotes
 
Abbreviations: AECC = American-European Consensus Conference; AIS = abbreviated injury scale; APACHE = acute physiology and chronic health evaluation; CI = confidence interval; ISS = injury severity score; OR = odds ratio

Presented in part at the American Thoracic Society 96th International Conference, May 5 to 10, 2000, Toronto, ON, Canada.

Supported in part by a National Medical Student Research Scholarship from the American Federation for Aging Research and The John A. Hartford Foundation, and by National Institutes of Health Specialized Center of Research in Acute Lung Injury grant HL30542.

Received for publication September 23, 2002. Accepted for publication January 10, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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