Effect of Upper Respiratory Tract Infection in Patients with Neuromuscular Disease
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1 Effect of Upper Respiratory Tract Infection in Patients with Neuromuscular Disease JANET M. POPONICK, I. JACOBS, GERALD SUPINSKI, and ANTHONY F. DIMARCO Pulmonary Division, Department of Medicine, Case Western Reserve University, MetroHealth Medical Center, Cleveland, Ohio Respiratory muscle strength during acute upper respiratory tract infection (URI) was assessed in patients with various forms of neuromuscular disease. Vital capacity (VC), oxygen saturation, end-tidal PCO 2, maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP) were determined in 25 stable patients with various forms of neuromuscular disease. Thirteen episodes of URI developed in 10 patients. Respiratory parameters were reassessed within h following the onset of symptoms in each patient. In patients with URI, mean baseline VC, MIP, and MEP were 1.16 L 0.14, 49.2 cm H 2 O 6.8, and 35.5 cm H 2 O 3.8 and fell to 1.01 L 0.15, 37.1 cm H 2 O 6.2, and 25.5 cm H 2 O 3.0 during URI (p 0.05 for each), respectively. Mean baseline PCO 2 and oxygen saturation were 39.1 mm Hg 1.1 and 95.1% 1.0, and during URI, 43.9 mm Hg 2.1 (p 0.05) and 95.0% 1.0 (NS), respectively. Five episodes of significant hypercapnia were observed in 4 patients. All parameters returned to near baseline values following recovery. We conclude that patients with various forms of neuromuscular disease develop reductions in respiratory muscle strength in association with URI. Unlike normal subjects, however, these decrements in respiratory muscle function may result in symptoms of shortness of breath, reductions in vital capacity, and acute hypercapnia in this patient population. Poponick JM, Jacobs I, Supinski G, DiMarco AF. Effect of upper respiratory tract infection in patients with neuromuscular disease. AM J RESPIR CRIT CARE MED 1997;156: The development of acute infectious illness is associated with reduction in muscle function and physical performance (1 4). Previous investigations have described decrements in both cardiac and skeletal muscle force production consequent to a variety of infections in normal subjects (1, 3). Interestingly, even viral upper respiratory tract infections (URI) are associated with impairment of skeletal muscle function (1), including the respiratory muscles (5). While reductions in peripheral skeletal muscle function are not likely to result in significant clinical sequelae, respiratory muscle impairment could have more ominous consequences. In normal subjects, previous reports have described reductions in respiratory muscle strength in the range of cm H 2 O in association with naturally occurring viral URI (5). Since this magnitude of reduction in respiratory muscle strength is small relative to maximum pressure-generating capacity (10 15%), it is unlikely that this degree of respiratory muscle weakness would result in any significant pulmonary symptoms or adverse clinical sequelae in normal individuals. In patients with neuromuscular disease and consequent reductions in baseline respiratory muscle strength, however, the development of (Received in original form November 8, 1996 and in revised form February 13, 1997) Correspondence and requests for reprints should be addressed to: Anthony F. Di- Marco, M.D., MetroHealth Medical Center, 2500 MetroHealth Drive, H-323, Cleveland, OH Am J Respir Crit Care Med Vol pp , 1997 URI and even modest reductions in respiratory muscle strength could have much greater clinical consequences (5 7). The purpose of the present investigation, therefore, was to assess the effects of URI in a group of patients with known severe neuromuscular disease. METHODS Young adults and children with various neuromuscular diseases were recruited consecutively from the Muscular Dystrophy Clinic at Metro- Health Medical Center. These diseases included Werdnig-Hoffman disease, limb-girdle muscular dystrophy, Duchenne s disease, Friedreich s ataxia, myotonic dystrophy, spinal muscle atrophy, and Charcot-Marie-Tooth atrophy. This investigation was approved by the Institutional Review Board at MetroHealth Medical Center. Informed consent was obtained from each patient and, in those subjects less than 18 yr of age, from a parent or guardian. We followed 25 patients who were in stable condition and free of respiratory symptoms for at least 15 wk prior to enrollment in the study. This group consisted of 19 men and 6 women with an age range of 7 40 yr (mean 20 yr 2 SE). There was a wide range of functional limitations among patients; the least affected were ambulatory with braces, while the most severe were bedridden. However 14 of the 25 patients had severe disease and were either confined to a wheelchair or bedridden. All were nonsmokers. Baseline pulmonary function studies, including vital capacity (VC), oxygen saturation, end-tidal PCO 2, and maximal inspiratory pressure (MIP), and maximial expiratory pressure (MEP), were performed while patients were in stable condition. All tests were performed while the patients were seated. Vital capacity was measured using a Respiradyne
2 660 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL TABLE 1 CLINICAL FEATURES OF MUSCULAR DYSTROPHY PATIENTS WITH URI Case Disease Type Age Sex Functional Status* 1 Werdnig-Hoffman disease 36 F Wheelchair 2 Werdnig-Hoffman disease 13 M Wheelchair 3 Duchenne s disease 14 M Wheelchair 4 Duchenne s disease 9 M Wheelchair 5 Duchenne s disease 8 M Wheelchair 6 Duchenne s disease 11 M Wheelchair 7 Myotonic dystrophy 11 F Walks 8 Myotonic dystrophy 8 M Walks 9 Duchenne s disease 13 M Wheelchair 10 Werdnig-Hoffman disease 29 M Bed-bound * Wheelchair indicates patients were confined to a wheelchair; Walks indicates patients were able to walk independently. hand-held spirometer (Sherwood Medical, St. Louis, MO). Oxygen saturation and end-tidal PCO 2 were measured using a Nellcor Multi-functional Monitor (Nellcor, Inc.). Respiratory muscle strength was assessed from measurements of MIP and MEP at residual volume and total lung capacity, respectively. The greatest pressures maintained for 1 s, measured with a mouthpiece connected to a Magnehelic Pressure Manometer (Model No 2150C; Dwyer Institute, Michigan City, IN), were recorded; the best of 3 5 efforts was used. If pressure measurements varied by more than 10 cm H 2 O, additional studies were performed until reproducible efforts were obtained. Baseline studies were performed on at least two separate days to ensure an accurate assessment of baseline function. If reproducible results were not obtained, studies were repeated on an additional day, if necessary. Family members and patients were instructed to notify one of the study investigators at the onset of symptoms indicative of an upper respiratory tract infection. URI was defined clinically by the onset of symptoms of cough, fever, rhinorrhea, and sore throat. Thirteen episodes of URI occurred in 10 patients. The characteristics in terms of muscle disease type, age, and sex of the 10 patients who developed URI and those who did not develop infection are presented in Tables 1 and 2, respectively. Most patients in the infection group had severe muscle weakness and were either wheelchair- or bed-bound. Each of the 10 patients experienced cough, fever, and myalgias with the onset of infection; 70% of patients also had either rhinorrhea, sore throat, or both. Four patients complained of dyspnea with onset of URI, which gradually resolved. Symptom duration ranged between 5 and 13 d TABLE 2 CLINICAL FEATURES OF NEUROMUSCULAR PATIENTS WITHOUT URI Case Disease Type Age Sex Functional Status* 1 Spinal muscular atrophy 38 M Wheelchair 2 Limb-girdle dystrophy 22 M Walks 3 Charcot-Marie-Tooth atrophy 38 M Walks 4 Duchenne s disease 16 M Wheelchair 5 Friederich s ataxia 35 F Wheelchair 6 Spinal muscle atrophy 38 F Wheelchair 7 Duchenne s disease 22 M Wheelchair 8 Duchenne s disease 13 M Wheelchair 9 Werdnig-Hoffman disease 7 M Wheelchair 10 Duchenne s disease 9 M Wheelchair 11 Limb-girdle dystrophy 11 F Walks 12 Myotonic dystrophy 14 F Walks 13 Limb-girdle dystrophy 39 M Walks 14 Myotonic dystrophy 37 M Walks 15 Duchenne s disease 10 M Walks * Wheelchair indicates patients were confined to a wheelchair; Walks indicates patients were able to walk independently. (mean, 7 SE). None of these patients developed acute chest radiographic abnormalities during URI. Respiratory parameters were reassessed within h following the onset of symptoms in each patient. Measurements were made every other day thereafter until symptoms resolved. If parameters did not return to baseline with resolution of symptoms, measurements were made biweekly for an additional 4 wk. Control, postinfection, and postrecovery data were analyzed using repeated measures ANOVA and post-hoc Neuman-Keuls test and reported as mean standard error (SE). Statistical significance was defined as a p value RESULTS The pattern of respiratory muscle function in one patient with Duchenne s disease who developed URI is shown in Figure 1. Within 24 h of the onset of symptoms of URI, there were reductions in both inspiratory and expiratory muscle strength, and vital capacity. In this patient, there was also an increase in end-tidal PCO 2 from 45 to 56 mm Hg. Of interest, the maximal change in these parameters occurred within 24 h of the onset of URI. Over subsequent days, there was gradual improvement in these parameters with the gradual return to near baseline values. Oxygen saturation remained greater than 90% throughout the study period. Mean VC and respiratory muscle strength of the patients who developed infections are presented in Table 3. Mean baseline VC, MIP, and MEP were markedly reduced compared with predicted values (8, 9) (mean: 50.1%, 51.5%, and 26.8% predicted, respectively). In two patients, reductions in respiratory muscle strength were particularly pronounced with MIP values of 25% and 32% predicted and MEP values of 19% and 13% predicted, respectively. Baseline MEP for the group was significantly less than baseline MIP (p 0.05). With the onset of URI, there were significant reductions in VC, MIP, and MEP (p 0.05 for each). Oxygen saturation was not significantly affected. Mean values of MIP, MEP, and VC following resolution of URI were not significantly different compared with baseline values. However, respiratory parameters did not return to baseline values in 2 patients, neither of whom had the worst baseline function. Mean baseline PCO 2 was within the normal range at 39.1 mm Hg. The highest level of baseline PCO 2 (45 mm Hg) was present in a patient with severe reductions in respiratory muscle strength. Mean PCO 2 increased significantly to 43.9 mm Hg with the development of URI and fell to baseline values during the recovery period. Five episodes of significant hypercapnia (PCO 2 43 mm Hg and 5 mm Hg increase in PCO 2 post infection) were observed in 4 patients. In these patients, mean PCO 2 at baseline was 40.2 mm Hg 1.8 SE, and during acute URI, 48.2 mm Hg 3.0 SE. Three of the 4 patients complained of dyspnea at rest with the onset of URI, whereas only 1 of the remaining 7 patients complained of dyspnea. The level of dyspnea was moderately severe in two of the patients, and both required hospitalization. Neither required mechanical ventilatory support, and both recovered with consecutive therapy. In the hypercapnic patients, baseline MIP and MEP were 31.6% 7.4 and 16.5% 3.5 SE predicted and fell to 19.3% 6.3 SE and 11.3% 2.9 SE, respectively. In comparison, baseline MIP and MEP were 74.3% 7.0 SE (p 0.05) and 33.7% 4.1 SE in the remaining patients (p 0.05). In this latter group, MIP and MEP fell to 52% 7.1 SE and 25.3% 2.3 SE, respectively, during infection (p 0.05 for each when compared with the hypercapnic patients). For the group as a whole, the magnitude of MIP during URI correlated significantly with the change in PCO 2 (r: 0.61; p
3 Brief Communication 661 Figure 1. Effects of acute URI on vital capacity, maximal inspiratory and expiratory pressures, transcutaneous oxygen saturation, and end-tidal PCO 2 in one subject with neuromuscular disease. See text for further explanation. 0.05) (Figure 2). As shown in the figure, patients with large increases in PCO 2 with onset of URI generally had MIP values during infection that were less than 30% predicted. Control MIP values did not correlate significantly with changes in PCO 2 (p 0.1). Similarly, the magnitude of VC during infection also correlated significantly with the change in PCO 2 (r: 0.86; p 0.01) (Figure 3). As shown, patients with large increases in PCO 2 had VC values during infection that were also less than 30% predicted. DISCUSSION Consistent with previous investigations in normal subjects (5), this study demonstrates that patients with various forms of neuromuscular disease also develop reductions in respiratory muscle strength in association with upper respiratory tract infection. Unlike normal individuals, however, these decrements in respiratory muscle function may result in symptoms of shortness of breath, reductions in vital capacity, and acute hypercapnia in this patient population. Respiratory Strength Measurements One of the significant and obvious limitations of the use of maximal respiratory pressures to assess respiratory muscle strength relates to the fact that the adequacy of these tests are highly dependent upon the level of patient effort. Moreover, respiratory tract infections are often associated with malaise and the sensation of generalized weakness, further complicating the performance of these studies. Consequently, motivational and volitional factors may have contributed to the observed changes, particularly following the onset of illness. While this factor cannot be discounted entirely, the measurement of end-tidal PCO 2 did not have this limitation, and this parameter increased in 4 of the 10 patients. Moreover, changes in PCO 2 during respiratory infections correlated significantly with the level of reductions in inspiratory muscle strength, supporting the validity of these measurements. Comparison to Previous Studies Other studies have previously demonstrated that viral infection is associated with alterations in muscle strength. Friman (1), for example, also showed that viral infection was associated with significant reductions in isometric muscle strength when compared with a control group of healthy men confined to bed for similar time periods. In experimentally induced sand fly fever in humans, a recognized model of viral illness causing fever, malaise, and myalgias, isometric muscle strength and exercise per-
4 662 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL TABLE 3 MEAN VC, MIP, MEP, SO 2 AND END-TIDAL PCO 2 AT BASELINE, AT ONSET OF URI AND FOLLOWING RECOVERY VC (L) MIP (cm H 2 O) MEP (cm H 2 O) PCO 2 (mm Hg) SO 2 (mm Hg) Baseline (50.1% 6.6) URI * (43.4% 6.5) Recovery (48.5% 6.5) (51.5% 8.2) * (38.9% 7.1) (47.9% 8.4) (26.8% 3.9) * (19.7% 2.8) (25.8% 3.3) * Significantly less than baseline values (p 0.05). Significantly greater than baseline values (p 0.05). Mean absolute and percent predicted values are provided. formance were reduced during the period of fever (3). Muscle strength decreased between 2% and 23% during the fever; similar decreases have been reported by other investigators (2). Mier-Jedrzejowicz and coworkers (5) demonstrated that acute viral illness was also associated with reductions in respiratory muscle strength (10 15% of baseline values) in normal subjects. While similar decrements in respiratory muscle function were observed in the present study, baseline values were markedly reduced in our study population. Consequently, these changes represented a much higher percentage of baseline function. In contrast to the present study, Mier-Jedrzejowicz and coworkers (5) found that viral infection was not associated with reductions in MIP and MEP in approximately 30% of their subjects. Despite obvious differences in the study population, differences in the character of viral illness may also have been different. In their study, only 37% of acute infections were associated with fever and myalgias, whereas each of the patients in the present study had these symptoms. Since reductions in muscle strength were observed in 6 of the 7 patients who developed fever in the study of Mier-Jedrzejowicz and coworkers (5), it is possible that the reductions in muscle strength may relate, in part, to the presence of fever (see below). Effects of Infection on PCO 2 An important observation in the present study was the associated development of hypercapnia during URI in some individuals. There are a number of potential factors that may have contributed to the observed increases in PCO 2 during infection, including reduction in ventilatory drive, alteration in respiratory mechanics, or reduction in respiratory muscle strength. Reductions in ventilatory drive and associated chronic CO 2 retention have been reported previously in patients with myopathic disease. With the exception of one patient with borderline PCO 2 elevation (45 mm Hg), however, the patients in our study had normal baseline PCO 2 values. While it is conceivable that URI may have induced temporary reductions in ventilatory drive, we know of no evidence to support this contention. Consequently, it is unlikely that alterations in respiratory drive could account for the observed elevations in PCO 2. A second possibility is that URI may have placed sufficient resistive and/or elastic loads on the respiratory system and thereby led to the development of hypercapnia. It is well known that mechanical abnormalities in lung function are a common accompaniment to acute viral illness even in normal individuals, both children (10) and adults (11 13). In general, most of these studies have demonstrated transient peripheral Figure 2. Relationship between maximal inspiratory pressure (MIP) (expressed as a percent predicted) and change in end-tidal PCO 2. See text for further explanation. Figure 3. Relationship between vital capacity during infection (expressed as a percent predicted) and change in end-tidal PCO 2.
5 Brief Communication 663 airway obstruction with preserved spirometric indices. One study (10) in children, however, did find small reductions in FVC 5%), FEV ( 3%), and peak flow rates ( 6%) with no change in total lung capacity. These changes were attributed to peripheral airway closure. Reductions in lung compliance have also been identified in patients with respiratory muscle weakness (14). The mechanism by which this occurs is not entirely clear but has been attributed to microatelectasis (14, 15). With the onset of URI, respiratory system compliance may have fallen further due to other complicating factors. Expiratory muscle weakness and consequent reduced cough effectiveness, for example, may lead to retention of secretions and secondary atelectasis. The fact that significant reductions in oxygen saturation did not occur during URI in our study population argues against the development of a significant increase in the A-a gradient, which is expected with significant atelectasis. A third, and perhaps the most important, factor potentially contributing to hypercapnia was the development of respiratory muscle weakness. Relevant to this issue, Braun and colleagues (15) evaluated respiratory muscle function in a large group of patients with a variety of differrent myopathies to determine the level of muscle weakness at which hypercapnic respiratory failure was likely to occur. They found that hypercapnia did not occur until respiratory muscle strength (average of percent predicted MIP and MEP) was less than 40% of normal and was not severe unless this parameter had fallen to 30% of normal values. Given the degree of baseline respiratory muscle impairment in our patients, it is not surprising that some individuals developed hypercapnia with the further reductions in muscle function associated with URI. Consistent with this previous report of Braun and colleagues (15), we also observed significant increases in PCO 2 when values of MIP and VC fell below 30% predicted. Based upon this previous data, it is reasonable to postulate that the observed degree of muscle weakness alone is sufficient to account for the observed elevations in PCO 2. Our results suggest that the major factor contributing to the development of respiratory failure in association with URI patients with muscular dystrophy relates to the development of respiratory muscle dysfunction in association with URI rather than mechanical abnormalities affecting lung function. It should also be mentioned that fever and associated increases in CO 2 production could potentially contribute to hypercapnia, independent of further reductions in muscle strength, given the degree of baseline muscle weakness in this patient population. MIP values during infection, however, correlated significantly with the change in PCO 2, whereas control MIP values did not. This suggests that reductions in muscle function were the major factor responsible for increases in PCO 2. Effects of Infection on Muscle Strength No attempt was made to determine the specific types of viral infection that occurred in our study population. However, due to the wide age range in our study group, it is likely that the responsible organisms varied among patients. Respiratory syncytial virus predominates in young children, whereas rhinovirus and the influenza and parainfluenza viruses are more common in adults (16). While it is possible that respiratory muscle dysfunction is more common with certain viruses, the fact that respiratory muscle dysfunction occurred both in the very young and older individuals suggests that the mechanism of virus-induced dysfunction is not virus-specific. While the precise mechanism by which infection results in a reduction in muscle strength is not clear, several potential mechanisms exist. The results of a number of animal studies (4, 17) suggest that acute viral infection can be associated with direct muscle injury and that sepsis-induced inspiratory muscle dysfunction may be mediated by oxygen-derived free radicals (18, 19). Other studies have suggested abnormalities in neuromuscular transmission during the acute phase of viral illness (20). Alternatively, the effects of viral illness on respiratory muscle function may be indirect. Acute illness is often associated with anorexia, resulting in reduced fat intake and potential changes in the supply of magnesium (21) and phosphate (22) to exercising muscle. Such alterations could also have an adverse effect on respiratory muscle function. Finally, antibiotic administration can also adversely affect respiratory muscle function (23). The patients in the present study received only penicillin-type drugs. Since these agents are only rarely associated with the development of a myopathy, it is unlikely that these drugs significantly affected muscle function in the present study. Respiratory decompensation associated with the development of respiratory infection is generally attributed to the concurrent development of mechanical abnormalities in lung function. The results of this study suggest that clinically significant alterations in respiratory muscle function in association with acute infectious illnesses may also play a major role in this regard. Moreover, while this study was limited to the study of URI, it is likely that other types of infections such as bacterial disease and sepsis may also affect respiratory muscle function and could conceivably have even greater adverse effects on muscle function. Based upon the results of this study, we recommend that patients with neuromuscular disease and baseline MIP or VC values that are 50% predicted or less should be closely monitored and identified as high risk for the development of respiratory failure. References 1. Friman, G Effect of acute infectious disease on isometric muscle strength. Scand. J. Clin. Lab. Invest. 37: Daniels, W. L., D. S. Sharp, J. E. Wright, J. A. Vogel, G. Friman, W. R. Beisel, and J. J. Knapik Effects of virus infection on physical performance in man. Mil. Med. 150: Friman, G., J. E. Wright, N. G. Ilback, W. R. Beitel, J. D. White, D. S. Sharp, E. L. Stephen, W. L. Daniels, and J. A. Vogel Does fever or myalgia indicate reduced physical performance capacity in viral infections? Acta Med. Scand. 217: McCarter, R., J. McGee, S. Witherspoon, C. J. Gauntt, and A. Vardiman Effects of viral infection on contraction of the diaphragm in mice. Proc. Soc. Exp. Biol. Med. 182: Mier-Jedrzejowicz, M., C. Brophy, and M. Green Respiratory muscle weakness during upper respiratory tract infections. Am. Rev. Respir. Dis. 138: Lynn, D. J., R. P. Woda, and J. R. Mendell Respiratory dysfunction in muscular dystrophies and other myopathies. Clin. Chest Med. 15: Altose, M. D Viral infections and respiratory muscle contractility. Am. Rev. Respir. Dis. 138: Gaultier, L., and R. Zinman Maximal static pressures in healthy children. Respir. Physiol. 51: Black, L. F., and R. E. Hyatt Maximal respiratory pressures: normal values and relationship to age and sex. Am. Rev. Respir. Dis. 99: Collier, A. M., R. L. Pimmel, V. Hasselblad, W. A. Clyde, J. H. Knelson, and J. G. Brooks Spirometric changes in normal children with upper respiratory infections. Am. Rev. Respir. Dis. 117: Hall, W. J., R. G. Douglas, R. W. Hyde, F. K. Roth, A. S. Cross, and D. M. Speers Pulmonary mechanics after uncomplicated influenza A infection. Am. Rev. Respir. Dis. 113: O Connor, S. A., D. P. Jones, J. V. Collins, R. B. Heath, M. J. Campbell, and M. H. Leightar Changes in pulmonary function after naturally acquired respiratory infection in normal persons. Am. Rev. Respir. Dis. 120: Blair, H. T., S. B. Greenberg, P. M. Stevens, P. A. Bilunos, and R. B. Couch Effects of rhinovirus infection on pulmonary function of
6 664 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL healthy human volunteers. Am. Rev. Respir. Dis. 114: Gibson, G. J., N. B. Pride, J. N. Davis, and L. C. Loh Pulmonary mechanics in patients with respiratory muscle weakness. Am. Rev. Respir. Dis. 115: Braun, N. M. T., N. S. Aurora and D. F. Rochester Respiratory muscle and pulmonary function in polymyositis and other myopathies. Thorax 38: Busse, W. W The contribution of viral respiratory infections to the pathogenesis of airway hyperreactivity. Chest 93: Åström, E., G. Friman, and L. Pilström Effects of viral and mycoplasma infections on ultrastructure and enzyme activities in human skeletal muscle. Acta Paediatr. Scand. 84: Supinski, G., D. Nethery, and A. DiMarco Effect of free radical scavengers on endotoxin-induced respiratory muscle dysfunction. Am. Rev. Respir. Dis. 148: Shindoh, C., A. DiMarco, D. Nethery, and G. Supinski Effect of PEG-superoxide dismutase on the diaphragmatic response to endotoxin. Am. Rev. Respir. Dis. 145: Friman, G., H. H. Schiller, and M. S. Schwartz Disturbed neuromuscular transmission in viral infections. Scand. J. Infect. Dis. 9: Molloy, D. W., S. Dhingra, F. Solven, A. Wilson, and D. D. McCarthy Hypomagnesemia and respiratory muscle power. Am. Rev. Respir. Dis. 129: Newman, J. H., T. A. Neff, and P. Ziporin Acute respiratory failure associated with hypophosphatemia. N. Engl. J. Med. 296: Aldrich, T. K., and D. J. Prezant Adverse effects of drugs on the respiratory muscles. Clin. Chest Med. 11:
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