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Health care providers may find it help- ful to gauge the response to bronchodilator therapy by asking patients with acute asthma about the different qualities of.
Language of Dyspnea in Assessment of Patients with Acute Asthma Treated with Nebulized Albuterol MARILYN L. MOY, MARY L. LANTIN, ANDREW HARVER, and RICHARD M. SCHWARTZSTEIN Divisions of Pulmonary and Critical Care Medicine and Emergency Medicine, Department of Medicine, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts; and Department of Psychology, University of North Carolina–Charlotte, Charlotte, North Carolina

To investigate whether the language of dyspnea provides relevant clinical information in addition to that provided by ratings of overall dyspnea intensity when assessing subjective response to therapy, we conducted a prospective study in a cohort of 25 patients with acute asthma presenting to the emergency department of a tertiary care hospital. Patients received nebulized albuterol treatments every 20 min with a maximum of three doses. At presentation and after each treatment, patients completed spirometry, rated overall dyspnea intensity on a modified Borg scale, and selected phrases that described qualities of breathlessness from a 15-item questionnaire. Paired Student’s t tests revealed significant improvements in FEV1 (from 1.39 6 0.66 L to 1.80 6 0.76 L, p , 0.001) and reductions in dyspnea intensity (from 5.12 6 2.08 to 2.82 6 1.59, p , 0.001) after the first albuterol treatment. Dyspnea intensity continued to decrease significantly in response to the second treatment, modified Borg rating 2.26 6 1.52, although there was no positive bronchodilator response. The results from Cochran Q tests revealed that the frequency of the experience of “chest tightness” decreased significantly across the phases of treatment. However, the sensations of “work” or “breathing effort” persisted at the same time that the FEV1 revealed ongoing airways obstruction. We conclude that attention to the language of dyspnea would alert health care providers to residual air flow obstruction despite decreases in overall dyspnea intensity. Moy ML, Lantin ML, Harver A, Schwartzstein RM. Language of dyspnea in assessment of patients with acute asthma treated AM J RESPIR CRIT CARE MED 1998;158:749–753. with nebulized albuterol.

Dyspnea is a general term used to characterize a range of qualitatively distinct sensations (1, 2). Investigators have studied the language of these distinct sensations with the use of descriptive phrases that have been shown to be valid and reliable. Simon and coworkers compiled a list of 19 representative phrases by asking patients with a variety of lung and cardiac diseases, who complained of shortness of breath, to describe the sensations associated with their uncomfortable awareness of breathing (3). Examples of the descriptors included “My breath does not go out all the way,” “My breathing requires effort,” and “My chest feels tight.” Similarly, Elliott and coworkers developed a questionnaire of 45 descriptors by circulating the list of descriptors used by Simon’s group to their clinical and research staff who were asked to add descriptors of their own respiratory sensations and those that had been used by their patients (4). Two physicians and five senior

(Received in original form July 18, 1997 and in revised form April 28, 1998) Supported in part by NIH/NHLBI Grant HL07633. Correspondence and requests for reprints should be addressed to Richard M. Schwartzstein, M.D., Division of Pulmonary and Critical Care Medicine, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215. E-mail: [email protected] Am J Respir Crit Care Med Vol 158. pp 749–753, 1998 Internet address: www.atsjournals.org

nurses modified the final 45 descriptors so that they would be the most easily understood by patients and were not redundant. Further support for the construct validity of the descriptors was demonstrated by Mahler and colleagues who administered the 15-item questionnaire of Simon’s group to 15 patients (5). Patient comments resulted in modifications that addressed the clarity, comprehensiveness, and redundancy of the items. Satisfactory test–retest reliability of the 15-item instrument was demonstrated by Mahler and colleagues in a cohort of patients with chronic obstructive pulmonary disease (5). The percent agreement for all descriptors selected at visits 1 and 2 was 79% (r 5 0.82; p 5 0.001). Similarly, using their questionnaire of 45 items, Elliott and coworkers (4) demonstrated good test-retest reliability by administering the questionnaire on two occasions. Eighty-two percent of their patients (169 of 207) had less than one-third changed responses between questionnaires. Using the descriptors of dyspnea, Simon and coworkers (3) demonstrated that normal volunteers could distinguish among the kinds of breathlessness induced by different stimuli such as breathholding, CO2 inhalation, exercise, resistive and elastic loads, and constrained tidal volume. In that study, distinct clusters of phrases emerged to characterize variations in the subjective experiences induced by the different stimuli. Subsequently, several investigators have shown that qualitatively distinct sensations of breathlessness are reported by patients

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with different cardiopulmonary diseases (4–6). In particular, patients with asthma most frequently chose descriptors that clustered into sensations of “work/effort,” “tightness,” and difficulty with “exhalation.” That virtually identical findings were obtained in three separate studies of patients with asthma serves as further validation of the instrument’s ability to systematically measure the qualitatively distinct aspects of dyspnea. The descriptors of dyspnea have not been examined either in patients with acute exacerbations of asthma or following therapy with bronchodilators. Some patients with acute or stable asthma experience resolution of their dyspnea despite minimal improvements in lung function and the persistence of significant air flow obstruction. These patients have been described as “poor perceivers.” McFadden and associates (7) found that the FEV1 was only 40 to 50% of predicted normal values when patients who presented with acute asthma became asymptomatic after treatment with bronchodilators. Similarly, substantial airway dysfunction, despite disappearance of dyspnea, was demonstrated in patients with acute asthma who were treated and discharged from the emergency room (8). Wolkove and coworkers (9) demonstrated that 26% of their patients with obstructive lung disease had a significant improvement in dyspnea without a positive bronchodilator response as reflected by the FEV1. Rubinfeld and Pain (10) showed that 10% of their patients with asthma had a FEV1 less than 50% of predicted when they had no symptoms at baseline, and 5% were still asymptomatic with marked airways obstruction at the height of an attack of methacholine-induced asthma. These studies suggest that patients’ perception of their dyspnea in response to changes in lung function is nonspecific and that assessments directed toward the intensity of breathlessness alone may not accurately reflect the level of persistent airways obstruction. We hypothesized that during resolution of acute asthma, changes in the descriptors of dyspnea are more specifically associated with changes in lung function than overall intensity of shortness of breath. We predicted that despite relatively small changes in lung function and persistent airways obstruction, patients would exhibit improvements in overall breathing discomfort and that the language, rather than the intensity, of dyspnea would more accurately detect the ongoing air flow obstruction. In the present study, we examined FEV1, the intensity of dyspnea, and the pattern of language descriptors used to describe dyspnea in patients with asthma and acute airways obstruction on presentation to the emergency department (ED) and during therapy with nebulized albuterol.

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Protocol A history and physical exam were performed. Historical data included time since diagnosis of asthma, duration of current symptoms, and markers of severity of obstructive airways disease such as use of systemic corticosteroids and history of intubation. Subjects were instructed to grade the intensity of their “breathing discomfort,” if any, by assigning a numerical value using a modified Borg scale (12). Following this, the 15-item questionnaire of descriptors of dyspnea (Table 1) was given to the subject by the investigator who administered it by reading the 15 descriptors. Subjects were instructed to listen to the entire list of 15 phrases before making their choices. Patients were asked to choose up to three of the phrases that best described their “breathing discomfort” at that time. Each subject was aware of the option of choosing none of the phrases. All patients were instructed to describe “breathing discomfort” and not associated symptoms such as tremulousness, cough, or palpitations. One of five versions of the questionnaire, differing in the order in which the phrases were presented, was randomly used for each subject. The same version was used for a particular subject throughout the course of treatment. Baseline pulmonary function tests were obtained with a pulmonary function spirometer (Warren E. Collins Inc., Braintree, MA). The patient was in sitting position, and the best of two forced expiratory maneuvers (highest FVC) was recorded. The patient then received 2.5 mg nebulized albuterol (0.5 ml in 2.5 ml normal saline) via a Marquest Whisper Jet micronebulizer (Marquest, Englewood, CO). Twenty patients received three nebulized treatments 20 min apart; five others received only two treatments. Spirometry, modified Borg ratings, and phrases that characterized “breathing discomfort” were obtained after each treatment. Decisions regarding the number of albuterol treatments given, the use of corticosteroids, and the need for hospital admission were made by the ED physicians. A debriefing period occurred at the conclusion of each study. Patients were asked whether they were able to adequately quantitate and describe their “breathing discomfort” using the modified Borg scale and the descriptors of dyspnea. Spontaneous comments regarding the menu of descriptors and interpretation of the phrases were elicited.

Statistical Analysis The correlation between FEV1 and modified Borg rating of dyspnea intensity was calculated using Pearson’s correlation coefficient. Paired Student’s t tests were used to compare mean values after each treatment. Statistical significance was defined as p , 0.05, and results are presented as mean 6 standard deviation. A positive bronchodilator response was defined according to American Thoracic Society criteria as a 12% increase and an absolute increase of 200 ml in FEV1 (13). The Cochran Q test was used to assess changes in the selection of specific descriptors by patients in each phase of the study. Cochran’s Q statistic is appropriate for determining changes in dichotomous ratings (in this case, the presence or absence of a specific descriptor) obtained repeatedly in the same individuals, and is approximated by the chi-square distribution.

METHODS Subjects Twenty-five patients who presented to the ED with the chief complaint of shortness of breath were enrolled in the study. These subjects had a history of asthma as defined by the criteria of the American Thoracic Society (11) or based on clinical history of wheezing without a significant smoking history (less than 10 pack-years). English was the primary language for all participants in the study. Patients with pulmonary vascular disease, lung cancer, congestive heart failure, infiltrate on chest X-ray, or neuromuscular disease were excluded from the study. Pregnant women were not studied. Patients who had received a nebulized bronchodilator treatment in the hour prior to presentation were excluded. Patients who were in extremis or who could not perform forced expiratory maneuvers did not participate in the study. All subjects had an oxygen saturation greater than 90% while breathing air or supplemental oxygen as measured by a Nellcor pulse oximeter. Informed consent was obtained in accordance with the guidelines of the Committee on Clinical Investigations, Beth Israel Deaconess Medical Center.

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TABLE 1 DESCRIPTORS OF DYSPNEA I feel that my breathing is rapid. My breath does not go out all the way. My breath does not go in all the way. My breathing is shallow. My breathing requires effort. My breathing requires more work. I feel that I am smothering. I feel that I am suffocating. I feel a hunger for more air. I feel out of breath. I cannot get enough air. My chest feels tight. My chest is constricted. My breathing is heavy. I feel that I am breathing more.

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Moy, Lantin, Harver, et al.: Language of Dyspnea in Acute Asthma TABLE 2 PATIENT CHARACTERISTICS Characteristic Number of patients Gender: males/females Age, yr Race: Caucasian/Black Years diagnosed with asthma 0–5 6–10 . 10 Inhaled anti-inflammatory drugs Current systemic corticosteroids History of intubation Smoking history Current antibiotics Current theophylline Duration of current flare, d Admitted to hospital Baseline FEV1, L Baseline % predicted FEV1 Baseline modified Borg

Number of Patients (%) 25 6 (24)/19 (76) 33.6 6 9.23* 15 (60)/10 (40) 14 (56) 3 (12) 8 (32) 15 (60) 3 (12) 0 (0) 6 (24) 6 (24) 4 (16) 3.78 6 3.03* 6 (24) 1.39 6 0.66* 46.4 6 22.3* 5.12 6 2.08*

* Values are expressed as mean 6 SD.

RESULTS Twenty-five patients, 19 women and 6 men with a mean age (6 SD) of 33.6 6 9.23 yr, participated in the study. None of the patients had required assisted mechanical ventilation in the past, three patients were taking oral corticosteroids at the time of study, and six patients required admission to the hospital (Table 2). Patients presented with moderate airways obstruction with a mean FEV1 of 1.39 6 0.66 L (46.4 6 22.3% predicted) and a modified Borg rating of 5.12 6 2.08 which corresponded to a dyspnea intensity of “severe.” Figure 1 shows the relationship between FEV1 and intensity of dyspnea for the entire cohort at baseline and during treatments with nebulized albuterol. The correlation coefficient was low, r 5 20.38, but statistically significant, p 5 0.0001. The strength of the correlation between FEV1 and Borg rating was similar when analyzed separately at baseline and after each treatment; r values ranged from 20.18 to 20.38. At any given level of FEV1, there was a wide range of dyspnea intensity experienced by all the patients. After the first albuterol treatment, patients exhibited significant increases in FEV1 (from 1.39 6 0.66 L to 1.80 6 0.76 L, p , 0.001) and decreases in dyspnea intensity (from 5.12 6

Figure 2. Response of FEV1 (open circles) and dyspnea intensity (closed squares) to nebulized albuterol therapy in 25 patients with acute asthma. There were significant increases in FEV 1 and decreases in dyspnea intensity after the first and second treatments; *p , 0.001, †p 5 0.007.

2.08 to 2.82 6 1.59, p , 0.001, Figure 2). Although there was a statistically significant increase in the FEV1 after the second treatment (from 1.80 6 0.76 L to 1.90 6 0.72 L, p 5 0.007), this change did not represent a positive clinical bronchodilator response. The mean FEV1 of 1.90 6 0.72 L (64.7 6 25.2% predicted) after the second albuterol treatment revealed ongoing airways obstruction. However, dyspnea intensity continued to decline; the change in mean Borg rating from 2.82 6 1.59 to 2.26 6 1.52 was statistically significant, p , 0.001. There was no significant change in either FEV1 or modified Borg rating in response to the third treatment. The five descriptors selected most often by patients are displayed in Table 3, along with the frequency with which patients selected each descriptor at each phase of the study. These phrases were the same as those in the unique clusters chosen by patients with asthma in previous studies (4–6). Therefore, cluster analysis was not performed and only these five phrases were submitted for statistical analysis. The presence of “chest tightness” decreased over the course of treatment, x2(3) 5 20.86, p , 0.05, and sensations of “breathing more” increased, x2(3) 5 17.11, p , 0.05. In both cases, the maximal change in subjective experience occurred after the first albuterol treatment. Importantly, no significant changes in the distribution of scores were observed for either “work,” “effort,” or “breath does not go out all the way.” These sensations persisted at the same time that the FEV1 revealed ongoing airways obstruction and the overall dyspnea intensity was decreasing. During the debriefing period, all patients reported that they were able to adequately quantitate and describe their

TABLE 3 NUMBER OF PATIENTS SELECTING EACH DESCRIPTOR OF DYSPNEA AT BASELINE AND AFTER EACH ALBUTEROL TREATMENT

Figure 1. Relationship between FEV1 and intensity of dyspnea at baseline and during treatment with nebulized albuterol in 25 patients with acute asthma; r 5 20.38, p 5 0.0001.

Descriptor

Pre

Post 1

Post 2

Post 3

Tight Breathing more Work Effort Breath does not go out

16 1 7 6 7

8 11 3 5 5

5 12 5 4 4

6 6 4 3 4

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“breathing discomfort” using the modified Borg scale and the descriptors of dyspnea. With the first several patients who chose the phrase “I feel that I am breathing more,” we observed that they used the phrase to describe the sensation of “breathing better” or “breathing with less discomfort.” As these were not the expected meanings of this phrase, all subsequent patients who chose this descriptor were asked why they had chosen the phrase. All patients selected the phrase to describe improvements in their breathing. Patients were also able to characterize improvements in subjective levels of breathing discomfort by choosing “zero” on the modified Borg scale and by selecting none of the descriptors as applicable.

DISCUSSION In this study, the language of dyspnea provided relevant clinical information to supplement that provided by ratings of overall dyspnea intensity in patients with acute asthma during treatment with bronchodilator therapy. Although further studies are needed to determine the full role of these descriptors in this and other treatment settings in which dyspnea is being assessed, the persistence in the frequency of reported sensations of the “work” or “effort” of breathing at the same time that the FEV1 revealed ongoing air flow obstruction supports the hypothesis that the language of dyspnea reflected the continued airways obstruction more clearly than the decreasing overall intensity ratings. Attention to the language of dyspnea would alert health care providers to significant remaining airways obstruction despite improvements or resolution of overall dyspnea intensity. The most frequently chosen descriptors in this cohort of 25 patients with asthma were similar to those most commonly selected in previous studies. For example, in one study, seven patients with moderate asthma, mean FEV1 1.69 L (54% predicted), chose descriptors that clustered into sensations of difficulty with “exhalation,” “work/effort,” and “tightness” (6). Similarly, using the 15-item questionnaire, Mahler and colleagues studied 56 patients with asthma (mean FEV1 2.13 L, 72% predicted) who most frequently chose descriptors that described “work/effort” and “tightness” (5). Thirty-one patients with asthma in London, England also chose descriptors of “work/effort” and “tightness” to describe their dyspnea when presented with a questionnaire of 45 items (4). The current study not only provides further evidence of the validity of the descriptors to assess dyspnea, but also offers preliminary data that the instrument is responsive to changes in the subjective experience of breathlessness during therapy. In this context, it is interesting that the phrases most frequently chosen to describe dyspnea by patients with asthma included “tightness,” “work,” and “effort.” These descriptors may reflect two pathophysiologic mechanisms of airways obstruction leading to dyspnea in patients with asthma. Chest “tightness” may reflect the breathing discomfort resulting from acute bronchoconstriction; the “work” or “effort” of breathing may be due to the more persistent airways obstruction related to the inflammatory component of asthma and the associated mechanical load on the ventilatory muscles. Clinically, increases in airway caliber by albuterol would result in improvements in FEV1 and decreases in the experience of “tightness” as evidenced most prominently after the first albuterol treatment. Remaining airways obstruction from inflammation would correspond to continued reductions in FEV1 and the persistence of the sensations of “work” or “effort” of breathing as experienced by these patients after the second and third albuterol treatments. The descriptors of dyspnea, in conjunction with intensity

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ratings of respiratory discomfort, may reflect clinically significant changes in FEV1 more clearly than ratings of overall intensity of dyspnea alone. Because patients have varied perceptions of the quality of their breathlessness, an overall rating of the intensity of “dyspnea” may not adequately characterize the patient’s respiratory discomfort. They may have breathing discomfort from remaining airways obstruction that they do not perceive as “shortness of breath.” Descriptors such as “chest tightness,” “effort,” or “work” of breathing may better relate to their dyspnea. Health care providers may find it helpful to gauge the response to bronchodilator therapy by asking patients with acute asthma about the different qualities of their sensation of breathlessness in addition to assessing overall dyspnea intensity. There are similar examples in other disease states of how the choice of descriptive words to characterize general terms, such as dyspnea or pain, is important when taking a clinical history. Patients with myocardial ischemia may deny chest pain, but admit to having chest pressure described as “an elephant sitting on their chest.” Because patients experience large variations in dyspnea intensity at a given level of airways obstruction and because of the potential placebo effect of nebulizer treatments, attention to the language of dyspnea would help alert health care providers to significant residual airways obstruction during treatment in the ED despite resolution of overall dyspnea. Possibly, patients experienced a reduction in dyspnea intensity despite the absence of a clinically significant improvement in FEV1 following the second albuterol treatment because of a generalized effect of becoming comfortable in the ED under the careful monitoring of health care providers. Yet the sensations of “work/effort” persisted. Attention to both objective measurements of air flow obstruction and the language of dyspnea may help detect persistent bronchospasm at times when patients report decreases in or resolution of their overall dyspnea. While measurement of indices of airways obstruction is recommended when treating patients with asthma, McFadden and associates (14) showed that physicians in the ED do not always incorporate objective data into their management decisions. They found that 48% of patients who required further treatment after intensive nebulizer therapy were discharged when the peak expiratory flow rate was less than 60% of predicted. In the present study, eight patients were discharged with a FEV1 less than 60% of predicted. Of these eight patients, all but one had an overall dyspnea intensity rating less than 1.5. While all eight patients may be considered “poor perceivers,” it is remarkable that half of them continued to select phrases that described breathing as “tight” or requiring “work” or “effort.” Thus, use of the language of dyspnea to supplement global ratings of dyspnea intensity may help identify these patients. Follow-up information obtained from hospital records showed that none of these patients returned to the ED or required admission shortly after being discharged. However, two patients presented to the ED with an asthma exacerbation 1 mo after the study visit. The possibility that care was sought at other hospitals cannot be excluded. It is not clear how well the intensity of dyspnea relates to airways obstruction as measured by FEV1 in patients with acute and stable asthma. Although the correlation between FEV1 and dyspnea intensity in the present study was statistically significant, the r value of 20.38 was low. Kunitoh and coworkers (15) showed that in patients with acute asthma there was no correlation between FEV1 and dyspnea intensity before or after treatment. On the other hand, Janson and Herala (16) obtained a low but significant correlation between change in dyspnea score and FEV1 in patients presenting to an emer-

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gency room with acute asthma. In a separate investigation, patients demonstrated a close linear relationship between FEV1 and dyspnea rating (17) in response to histamine-induced bronchoconstriction, but Janson-Bjerklie and coworkers (18) showed that dyspnea was not related to changes in airway caliber induced by methacholine. Not only is the relationship between FEV1 and dyspnea mixed, but considerable variation in the severity of breathlessness exists among patients for any particular degree of air flow obstruction. These findings lend further support to the idea that the concomitant use of the language of dyspnea may allow more accurate detection of airways obstruction. We acknowledge that this group of patients with asthma was heterogenous with respect to past and present anti-inflammatory medications and therefore levels of acute and chronic inflammation. There was also variability in the number of patients who were receiving antibiotics or theophylline at the time of presentation. All these factors may contribute to the sensation of dyspnea in different ways. We also recognize that cultural and educational backgrounds may influence the results of this study which is so dependent on the use of language and the interpretation of subtleties in language. All subjects spoke English and appeared to understand the questionnaires and the differences of the descriptor phrases. Although it has been observed that subjects in a study may respond in a way that they believe will “please” the investigator, it seems unlikely that this behavior was a significant confounder in the present study. If patients were randomly selecting descriptors from the questionnaire, one would have expected responses that were evenly distributed among the available options rather than the consistent choosing of phrases within the clusters encompassing “chest tightness” and “work and effort of breathing,” clusters that have been shown to be associated with asthma. Furthermore, it is not evident why some phrases would disappear, e.g., “tightness,” whereas others would persist, e.g., “effort,” if subjects were merely trying to appear cooperative and consistent. In addition, only one term increased in frequency as the study progressed. Although we did not anticipate that “breathing more” would be used as an indicator that patients experienced less respiratory distress, the fact that they selected this phrase suggests that they were thoughtful in their responses and not selecting descriptors at random. Use of an open-ended format rather than the questionnaire to elicit information about the patients’ sensory experiences potentially carries more significant problems. Most people have never been asked to describe the quality of their breathing sensations. Our clinical experience demonstrates that confronted with such a task during an acute illness without the structure of a questionnaire, patients are generally unprepared to provide specific details about their symptoms. The use of a questionnaire allows quantitative assessment of patient experiences. We believe the use of the combination of a structured response along with an open-ended debriefing provides the most information. The information obtained during the debriefing revealed that subjects were using the descriptor “I feel that I am breathing more” to indicate improvement in their breathing rather than a new sense of dyspnea. We acknowledge the potential double meaning of this phrase (which has been used in previous studies to indicate breathing discomfort), but we do not feel that its selection was counterintuitive on the part of the subjects who were clearly trying to be accurate, nor do we believe this unexpected use of the descriptor invalidates the other aspects of the study. The list of descriptors used in the

present study was developed to assess the “language of dyspnea” and not “improvements in dyspnea.” The ways in which patients experience improvement in their respiratory distress may warrant further study. In summary, these data demonstrate that the language of dyspnea is a useful supplement to overall ratings of dyspnea intensity while monitoring response to bronchodilator therapy in patients with acute asthma. Attention to the language of dyspnea would alert health care providers to significant remaining airways obstruction despite improvements in or resolution of overall dyspnea when assessed by general ratings of the intensity of breathing discomfort. Further studies are needed to examine whether patterns of language descriptors differ among patients who are “nonresponders” to bronchodilator therapy as well as patients who are “poor perceivers” of overall dyspnea. Acknowledgment : The authors thank Glen Kimball and the Respiratory Therapy staff for their technical assistance.

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