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Acute Respiratory Distress Syndrome: CT Abnormalities at Long-term Follow-up

¹ Departments of Radiology (S.R.D., M.B.R., D.M.H.)
² Thoracic Medicine (A.U.W.)
³ Intensive Care Medicine (T.W.E.), Royal Brompton Hospital, Sydney St, London SW3 6NP, England.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To document abnormalities at computed tomography (CT) in adult survivors of acute respiratory distress syndrome (ARDS), to determine the relationships between CT patterns during the acute phase and at follow-up, and to assess the effects of mechanical ventilation on the development of CT abnormalities.

MATERIALS AND METHODS: Thin-section CT scans were obtained during the acute illness and at follow-up in 27 patients with ARDS. The extent and distribution of individual CT patterns were independently analyzed.

RESULTS: At follow-up CT, a reticular pattern was the most prevalent (23 patients [85%]) and extensive CT abnormality, with a striking anterior distribution (more anterior distribution than posterior distribution, P < .001). A reticular pattern at follow-up was inversely correlated with the extent of intense parenchymal opacification on scans obtained during the acute illness (Spearman r = -0.26; P < .001). The extent of a reticular pattern at follow-up CT was independently related to the total duration of mechanical ventilation (P = .02) but was most strongly related to the duration of pressure-controlled inverse-ratio ventilation (P < .001).

CONCLUSION: A reticular pattern, with a striking anterior distribution, is a frequent finding of follow-up CT in ARDS survivors and is most strongly related to the duration of pressure-controlled inverse-ratio ventilation.

Index terms: Computed tomography (CT), electron beam, 60.12118 • Lung, assisted ventilation, 60.4132 • Lung, CT, 60.12118 • Lung, fibrosis, 60.4132, 60.6113 • Respiratory distress syndrome, adult (ARDS), 60.4132

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The acute respiratory distress syndrome (ARDS) in adults is a nonspecific and catastrophic response of the lung to injury. "ARDS," when first defined in 1967, included the following constellation of clinicoradiologic features: sudden onset of dyspnea, refractory hypoxemia, decreased lung compliance, and widespread infiltration at chest radiography (1).

In ARDS, computed tomography (CT) is of value in the acute stages; in addition to its role in the detection of complications (2,3), use of CT has increased understanding of the pathophysiology (4–6). To our knowledge, the long-term morphologic sequelae of ARDS have previously been reported in only a limited number of patients (7). Moreover, the pathophysiologic importance of CT changes in survivors has not been fully evaluated. The present study was undertaken to (a) document the spectrum of CT abnormalities of the lung parenchyma in patients who have survived ARDS, (b) evaluate the relationship between CT patterns in ARDS survivors with those seen during the acute illness and the influence of mechanical ventilation on CT appearances seen at follow-up, and (c) determine the functional importance, if any, of the CT changes in ARDS survivors.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Sixty-three patients fulfilling American-European Consensus Conference diagnostic criteria for the diagnosis of ARDS (8) were admitted to the intensive care unit of our institution during a 3-year 1-month period. During the acute phase, when clinically stable, all patients underwent thoracic CT (initial CT) as part of the initial management protocol. The mean duration ± SD between intubation and the initial CT was 7.7 days ± 6.2 (range, 0–24 days). Twenty-seven of the survivors (Table 1) returned for follow-up evaluation and underwent formal lung function tests and repeat chest CT (follow-up CT); the mean duration between the initial and follow-up CT studies was 196.2 days ± 41.3 (range, 110–267 days). All CT studies and pulmonary function tests were undertaken for clinical reasons at the request of referring physicians. The demographic records, cause of ARDS, smoking history, and modes and duration of mechanical ventilation (recorded in all but one patient) were extracted from case records and are summarized in Table 1.

All CT examinations were performed with an electron-beam scanner (Imatron, San Francisco, Calif). Initial CT was performed with 3.0-mm collimation (10-mm intervals) to allow the shortest scan acquisition time of 100 msec; follow-up CT was performed with 1.5-mm collimation (10-mm interval; acquisition time, 200 msec). All patients underwent CT in the supine position; only those of our cohort were turned prone for a short period during their time in the intensive care unit. Initial CT was performed during assisted mechanical ventilation, and follow-up CT was performed with the patient in full inspiration. Images were reconstructed with a high-spatial-frequency reconstruction algorithm and were photographed at window settings appropriate for viewing the lung parenchyma (window level, -550 HU; window width, 1,500 HU).

All CT scans were scored independently by two observers (D.M.H., M.B.R.) for the extent of four CT patterns. A disparity in the extent of an individual CT pattern of greater than 15% was resolved by consensus; a mean figure was used in cases with less than 15% disparity. The initial and follow-up CT scans were scored on separate occasions, and the observers were blinded to the clinical and lung function data. Three anatomically comparable levels on initial and follow-up studies were preselected by one of the authors (S.R.D.) not involved in the scoring: level 1, which was the aortic arch; level 2, which was between the carina and pulmonary venous confluence; and level 3, which was 1 cm above the right hemidiaphragm. Each level was divided into four quadrants: right anterior, right posterior, left anterior, and left posterior.

For each quadrant, observers determined the extent of the following CT abnormalities, in accordance with standard morphologic descriptors based on the recent Fleischner Society Nomenclature Committee recommendations (9).

1. "Ground-glass opacification" was defined as a hazy increase in lung attenuation, with preservation of bronchial and vascular margins. The ground-glass opacification was taken to represent edematous or inflammatory lung on initial scans and fine fibrosis, beyond the limits of CT resolution (10), on follow-up scans.

2. "Intense parenchymal opacification" was defined as a homogeneous increase in lung attenuation that obscured bronchovascular margins in which an air-bronchogram may have been present and was taken to represent consolidation, compression atelectasis, or both on initial scans.

3. "Reticular pattern" was defined as innumerable interlacing line shadows that may be fine, intermediate, or coarse, with associated distortion of the lung architecture; it was taken to represent fibrosis.

4. For "decreased attenuation," observers were asked to distinguish between decreased attenuation due to emphysema (defined as centrilobular decreased attenuation, usually without visible walls and of nonuniform distribution and located predominantly in the upper lung levels [9]) and that attributable to small-airways disease (defined as regions of decreased attenuation associated with a reduction in the number and caliber of pulmonary vessels [11]).

To assess the determinants of CT changes at follow-up, the individual CT patterns on the initial and follow-up scans were quantified visually to the nearest 5% in each quadrant. Observers also recorded the presence and extent of a number of pleural abnormalities (pneumothorax, pleural effusion, and pleural thickening) on the initial and follow-up scans; for this assessment, all CT sections were reviewed.

Pulmonary function tests were performed within 4 weeks of the follow-up CT examination (mean duration between follow-up CT and pulmonary function tests, 2.7 days ± 5.6; duration range, 0–22 days), and results were expressed as a percentage of values predicted from the patient's age, sex, and height (12). The following were recorded: forced expiratory volume in 1 second, forced vital capacity, and the ratio of forced expiratory volume in 1 second to forced vital capacity; total lung capacity, residual volume, and the ratio of residual volume to total lung capacity; and the maximum expiratory flow rates at 25% and at 50% above residual volume. Indexes of gas transfer (corrected for hemoglobin concentration) were obtained by means of the carbon monoxide single-breath technique (single-breath carbon monoxide diffusing capacity) and were adjusted for alveolar volume. Measurements of lung volumes were obtained with a rolling seal spirometer (Spiroflow; Morgan, Rainham, Kent, United Kingdom); those of diffusing capacity, with transfer factor equipment (Morgan).

Data are given as mean figures ± SD or as median figures with ranges, depending on the normality of distribution. A P value of less than .05 was taken to indicate a significant difference. Differences between subgroups were examined nonparametrically by using the Wilcoxon rank sum test or the Kruskal-Wallis test, as appropriate. Univariate correlations were examined by using the Spearman rank correlation test. Individual relationships (a) between ventilatory factors during the acute episode and CT findings at follow-up and (b) CT findings at follow-up and functional impairment at follow-up were evaluated by using stepwise forward regression; abnormally distributed variables were transformed before analysis (categoric or zero-skewness transformations, as appropriate). The assumptions of multiple linear regression were met in all analyses, as judged by testing for heteroscedasticity and omitted variables.

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
CT Patterns on Initial and Follow-up Scans in 27 Patients
On the initial scans, areas of ground-glass opacification and intense parenchymal opacification were documented in all patients and were the most extensive CT abnormalities (Table 2); ground-glass opacification was more frequently seen in the anterior quadrants (P < .001), whereas areas of intense parenchymal opacification were more common in the posterior quadrants (P < .001). Other patterns were seen less frequently on initial scans and are given in Table 2. There was no significant difference in the distribution of total decreased attenuation between the anterior and posterior quadrants (P = .99). The extents of ground-glass opacification, intense parenchymal opacification, or total decreased attenuation did not differ significantly between the three levels (P = .98, P = .16, and P = .83, respectively).

Pneumothorax was documented in seven patients (unilateral, four patients; bilateral, three patients), and pleural effusion was documented in nine patients (unilateral, two patients; bilateral, seven patients).

On follow-up CT scans, a coarse reticular pattern was the single most frequent pattern, (23 patients [85%]) and was strikingly more extensive anteriorly (P < .001) (Fig 1). The extent of a reticular pattern did not differ between levels 1, 2, and 3 (P = .13). Other patterns were seen less frequently on the follow-up CT scans and are summarized in Table 2. Ground-glass opacification (Fig 2) and areas of decreased attenuation were more extensive anteriorly (P = .01 and P = .05, respectively) but did not differ in extent between levels 1, 2, and 3. On follow-up CT scans, there was evidence of pleural thickening in seven patients (unilateral, two patients; bilateral, five patients), judged minimal in all cases by both observers. There were no residual pneumothoraces or pleural effusions at follow-up CT.

View larger version (120K): [in this window] [in a new window]   Figure 1a. (a) CT scan obtained in an 18-year-old woman who survived ARDS shows a limited extent of a reticular pattern, with associated distortion (arrows) of the lung parenchyma anteriorly. (b) CT scan obtained in an 26-year-old woman who survived ARDS shows more extensive parenchymal destruction and distortion (black arrows) anteriorly and a few irregular bands (white arrows) posteriorly. Both a and b illustrate the distribution of CT abnormalities in the anterior quadrants.

View larger version (126K): [in this window] [in a new window]   Figure 1b. (a) CT scan obtained in an 18-year-old woman who survived ARDS shows a limited extent of a reticular pattern, with associated distortion (arrows) of the lung parenchyma anteriorly. (b) CT scan obtained in an 26-year-old woman who survived ARDS shows more extensive parenchymal destruction and distortion (black arrows) anteriorly and a few irregular bands (white arrows) posteriorly. Both a and b illustrate the distribution of CT abnormalities in the anterior quadrants.

View larger version (130K): [in this window] [in a new window]   Figure 2a. Thin-section CT scans obtained at the 7-month follow-up examination in a 55-year-old man who survived ARDS. (a) CT scan shows predominant ground-glass opacification with a nonanterior distribution. There is sparing of some secondary pulmonary lobules (arrows). (b) CT scan shows an anterior distribution of reticular patterns and ground-glass opacification. There is dilatation (arrows) of some subsegmental bronchi within areas of ground-glass opacification.

View larger version (103K): [in this window] [in a new window]   Figure 2b. Thin-section CT scans obtained at the 7-month follow-up examination in a 55-year-old man who survived ARDS. (a) CT scan shows predominant ground-glass opacification with a nonanterior distribution. There is sparing of some secondary pulmonary lobules (arrows). (b) CT scan shows an anterior distribution of reticular patterns and ground-glass opacification. There is dilatation (arrows) of some subsegmental bronchi within areas of ground-glass opacification.

Relationships between CT Changes on Initial and Follow-up Scans in 25 Patients
A reticular pattern on follow-up CT scans correlated inversely with the extent of intense parenchymal opacification (Spearman r = -0.26, P < .001) and directly with the extent of ground-glass opacification (Spearman r = 0.25, P < .001) on initial scans (Fig 3). However, at multivariate analysis, CT patterns on initial scans had no independent effects on the extent of a reticular pattern on follow-up scans. No correlation was demonstrated between ground-glass opacification seen on initial scans and that seen on follow-up scans (Spearman r = 0.06, P = .29).

View larger version (114K): [in this window] [in a new window]   Figure 3a. CT scans obtained in a 25-year-old man who survived ARDS. (a) Initial scan obtained during the acute illness shows typical areas of intense parenchymal opacification in the dependent lung and nondependent ground-glass opacification. (b) Follow-up scan obtained 8 months after a demonstrates relatively normal lung parenchyma in the posterior quadrants and a reticular pattern anteriorly (arrows). There are two secondary pulmonary lobules (arrowheads) with inconspicuous decreased attenuation.

View larger version (86K): [in this window] [in a new window]   Figure 3b. CT scans obtained in a 25-year-old man who survived ARDS. (a) Initial scan obtained during the acute illness shows typical areas of intense parenchymal opacification in the dependent lung and nondependent ground-glass opacification. (b) Follow-up scan obtained 8 months after a demonstrates relatively normal lung parenchyma in the posterior quadrants and a reticular pattern anteriorly (arrows). There are two secondary pulmonary lobules (arrowheads) with inconspicuous decreased attenuation.

View larger version (11K): [in this window] [in a new window]   Figure 4. Graph shows the relationship between the duration of pressure-controlled inverse-ratio ventilation (PCIRV) and the CT extent of a reticular pattern (Spearman r = 0.82, P < .001).

Relationships between CT Appearances on Follow-up Scans and Pulmonary Function Test Results in 25 Patients
The results of pulmonary function tests are given in Table 4. There were no significant correlations between the extent of a reticular pattern, ground-glass opacification, or areas of decreased attenuation and pulmonary function indexes. However, the extents of a reticular pattern and of ground-glass opacification combined showed a significant negative correlation with the forced vital capacity (Spearman r = -0.41, P = .04) and a positive correlation with the residual volume (Spearman r = 0.47, P = .02) and the ratio of residual volume to total lung capacity (Spearman r = 0.50, P = .01).

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

In the present study, a coarse reticular pattern with distortion of lung parenchyma was the most prevalent CT abnormality in ARDS survivors. Ground-glass opacification was also a frequent pattern, and, although a nonspecific sign, it seems probable that ground-glass opacification represents fine intralobular fibrosis below the resolution limits of CT (9,10). There is indirect evidence to justify this assumption: First, in the present study, there is a significant positive correlation between the extents of a reticular pattern and ground-glass opacification. Second, both patterns have a similar distribution at follow-up. Finally, in a recent CT study of ARDS survivors (16), the authors reported that ground-glass opacification was almost invariably associated with bronchial dilatation; bronchial dilatation without ancillary CT signs of fibrosis was recorded in only six (10%) of 60 lobes in that study.

The anterior distribution of the reticular pattern at follow-up seems to be a distinctive feature and, to our knowledge, has been commented on in only one previous report (17) on three patients with severe ARDS in whom follow-up CT scans revealed an anteriorly distributed coarse reticular pattern with associated traction bronchiectasis. The authors (17) suggested that the anterior reticular pattern resulted from alveolar overdistention in "unprotected" nonconsolidated lung. During the acute phase of ARDS, hyperattenuating areas of unaerated or collapsed parenchyma are typically seen in dependent parts of the lung (4,18). There is some evidence in our study to support the view that collapsed or consolidated lung is protected from the effects of alveolar overdistention: A negative correlation was noted between the extent of a reticular pattern on follow-up CT scans and the extent of intense parenchymal opacification on initial CT scans.

The relationships between the development of lung fibrosis after ARDS and causal factors are complex. In an early study of ARDS, there were significant and stronger correlations between pathologic scores of interstitial fibrosis and duration of treatment than with the total duration of respiratory failure (14). The authors (14) speculated that the deposition of pulmonary fibrosis was largely iatrogenic rather than due to the disease itself. These findings were borne out in a later study (19) in which a group of ARDS survivors was compared with a group of nonsurvivors. The subgroup of nonsurviving patients with an increased lung collagen level had required a substantially greater number of days of high inspired oxygen fraction than survivors and nonsurvivors without an increased collagen level. Furthermore, although there were no statistically significant differences in the number of days of positive end-expiratory pressure ventilation between the three groups, a higher mean positive end-expiratory pressure level had been delivered to the increased collagen group as compared to nonsurvivors without an increased collagen level. One possible inference from these results is that the more intense therapy was merely a reflection of greater primary lung injury and that the more pronounced ARDS was primarily responsible for lung fibrosis. However, the difference in severity of ARDS between the two nonsurviving groups was thought to be not substantial (19).

Although other data have generally supported the view that lung damage may be ventilator-induced, there are some conflicting results. In animal studies, ventilator-induced permeability edema in rats treated with intermittent positive-pressure breathing at conventional or high pressures may be prevented by means of the coapplication of positive end-expiratory pressure (20,21). The independent and positive relationship between the extent of a reticular pattern and the duration of pressure-controlled inverse-ratio ventilation in our study favors mechanical ventilation as an important etiologic factor. However, whether the known harmful effect of a high inspired oxygen fraction (22) has a synergistic or independent role in this context is unclear; in any event, there is no reliable method for the noninvasive measurement of regional lung oxygen concentration.

The converse view that treatment factors are less important to the development of pulmonary fibrosis than the lung injury itself has also been expressed (23). In an autopsy study (23) of patients with and patients without ARDS who received ventilation, only patients with ARDS had abnormally increased lung collagen levels, which suggests that mechanical ventilation and oxygen administration play an adjunctive rather than a primary role in the development of fibrosis. It has also been suggested that the histopathologic features of pulmonary fibrosis in the acute stage have no bearing on subsequent lung function abnormalities (24). Nevertheless, it is likely that the detrimental effects of high oxygen concentrations (22) and mechanical ventilation (25,26) together with normal repair mechanisms after acute lung injury all contribute to residual functional impairment (27).

Although comparisons between results of the present and previous studies of post-ARDS pulmonary fibrosis are difficult, there are intriguing parallels between the entity of bronchopulmonary dysplasia in adults and the CT features described in our patients. Histopathologic features similar to those in childhood bronchopulmonary dysplasia have been described in three adult patients with ARDS (28); at postmortem examination, interstitial fibrosis and cysts of variable size were noted in both lungs. The macroscopic image of excised lung in one patient revealed a profusion of cysts in an anterior distribution, similar to those seen in bronchopulmonary dysplasia of infancy (28).

A wide variation of lung functional impairment has been documented in ARDS survivors, but the patterns of dysfunction are usually mild (29,30). A tendency to return to normal function is typical, with stabilization of all routine test results at 4-6 months in two of every three patients (31). An obstructive defect was noted in two of 10 patients, with elevation of the ratio of residual volume to total lung capacity in three; marked lung restriction was a feature in two patients (31). Depression of carbon monoxide gas transfer is the most consistent pulmonary function defect in ARDS survivors (32,33). In one study (34), there was initial improvement in carbon monoxide gas transfer during the 1st year in 11 of 13 survivors. However, in seven cases, at 6 months or later follow-up, carbon monoxide gas transfer remained markedly below predicted values. The depression of carbon monoxide gas transfer was not attributable to coexistent emphysema, because the carbon monoxide gas transfer corrected for alveolar volume was increased. In this context, it is notable that emphysema was an uncommon feature in our patients; although mean carbon monoxide gas transfer was below that predicted in our patients, the mean carbon monoxide gas transfer corrected for alveolar volume was normal. Furthermore, the median extent of emphysema visible at CT in the present study was trivial.

Given the limited extent of all CT patterns at follow-up, it is not surprising that the functional importance of CT changes was minimal. The tendency for lung function to drift toward normality after acute lung injury and the limited extents of all CT changes at follow-up are the most likely explanations for the lack of correlation. The correlation of the combined extents of a reticular pattern and ground-glass opacification with indexes of airflow obstruction is difficult to explain. Whether obstruction occurs at the level of the large or smaller airways in ARDS survivors is not clear, but it is known that small-airway obstruction may accompany lung fibrosis (35). In a meticulous study (36) in 18 patients with idiopathic pulmonary fibrosis, in most patients the small airways were narrowed in association with peribronchiolar fibrosis. Fibrosis around bronchioles was the most frequent abnormality associated with narrowed airways. Whether the residual fine fibrosis in our patients is centered on small airways is not known. Moreover, to our knowledge, histologic evidence is lacking and, in the context of ARDS survivors, is unlikely to be forthcoming.

In conclusion, we have shown that a reticular pattern at follow-up is the most common CT pattern in ARDS survivors. The duration of ventilation—in particular, pressure-controlled inverse ratio ventilation—is independently related to the extent of the reticular pattern at follow-up CT. The relationship between CT signs of pulmonary fibrosis and indexes of airflow obstruction is not clear but may be related to the obstruction of small airways.

	Footnotes

 
Address reprint requests to D.M.H.

Abbreviation: ARDS = acute respiratory distress syndrome

Author contributions: Guarantor of integrity of entire study, D.M.H.; study concepts, S.R.D., A.U.W., D.M.H.; study design, A.U.W., D.M.H.; definition of intellectual content, S.R.D., A.U.W., T.W.E., D.M.H.; literature research, S.R.D.; clinical studies, T.W.E., S.R.D., M.B.R., D.M.H.; data acquisition, S.R.D.; data analysis, D.M.H., M.B.R., A.U.W.; statistical analysis, A.U.W.; manuscript preparation, S.R.D.; manuscript editing, D.M.H., A.U.W.; manuscript review, T.W.E., D.M.H.

Received February 4, 1998; revision requested April 15, 1998; revision received May 26, 1998; accepted July 20, 1998.

	References

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

1. Ashbaugh DG, Bigelow DB, Petty TL, Levine BE. Acute respiratory distress in adults. Lancet 1967; 2:319-323.[Medline]
2. Mirvis SE, Tobin KD, Kostrubiak I, Belzberg H. Thoracic CT in detecting occult disease in critically ill patients. AJR 1987; 148:685-689.[Abstract/Free Full Text]
3. Snow N, Bergin KT, Horrigan TP. Thoracic CT scanning in critically ill patients: information obtained frequently alters management. Chest 1990; 97:1467-1470.[Abstract/Free Full Text]
4. Gattinoni L, Mascheroni D, Torresin A, et al. Morphological response to positive end expiratory pressure in acute respiratory failure: computerized tomography study. Intensive Care Med 1986; 12:137-142.[Medline]
5. Gattinoni L, Pelosi P, Vitale G, Pesenti A, D'Andrea L, Mascheroni D. Body position changes redistribute lung computed-tomographic density in patients with acute respiratory failure. Anesthesiology 1991; 74:15-23.[Medline]
6. Gattinoni L, Bombino M, Pelosi P, et al. Lung structure and function in different stages of severe adult respiratory distress syndrome. JAMA 1994; 271:1772-1779.[Abstract]
7. Owens CM, Evans TW, Keogh BF, Hansell DM. Computed tomography in established adult respiratory distress syndrome: correlation with lung injury score. Chest 1994; 106:1815-1821.[Abstract/Free Full Text]
8. Bernard GR, Artigas A, Brigham KL, et al. The American-European consensus conference on ARDS: definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 1994; 149:818-824.[Abstract]
9. Austin JHM, Müller NL, Friedman PJ, et al. Glossary of terms for computed tomography of the lungs: recommendations of the Nomenclature Committee of the Fleischner Society. Radiology 1996; 200:327-331.[Free Full Text]
10. Rémy-Jardin M, Rémy J, Giraud F, Wattinne L, Gosselin B. Computed tomography assessment of ground-glass opacity: semiology and significance. J Thorac Imaging 1993; 8:249-264.[Medline]
11. Stern EJ, Swensen SJ, Hartman TE, Frank MS. CT mosaic pattern of lung attenuation: distinguishing different causes. AJR 1995; 165:813-816.[Abstract/Free Full Text]
12. Quanjer PH. Standardized lung function testing. Eur Respir J 1993; 6(suppl):1-100.
13. Wright JL. Adult respiratory distress syndrome. In: Thurlbeck WM, Churg AM, eds. Pathology of the lung. 2nd ed. New York, NY: Thieme Medical, 1995; 385-399.
14. Pratt PC, Vollmer RT, Shelburne JD, Crapo JD. Pulmonary morphology in a multihospital collaborative extracorporeal membrane oxygenation project. I. Light microscopy. Am J Pathol 1979; 95:191-214.[Abstract]
15. Zapol WM, Trelstad RL, Coffey JW, Tsai I, Salvador RA. Pulmonary fibrosis in severe acute respiratory failure. Am Rev Respir Dis 1979; 119:547-554.[Medline]
16. Howling SJ, Evans TW, Hansell DM. The significance of bronchial dilatation on CT in patients with adult respiratory distress syndrome. Clin Radiol 1998; 53:105-109.[Medline]
17. Finfer S, Rocker G. Alveolar overdistension is an important mechanism of persistent lung damage following severe protracted ARDS. Anaesth Intensive Care 1996; 24:569-573.[Medline]
18. Gattinoni L, Pelosi P, Pesenti A, et al. CT scan in ARDS: clinical and physiopathological insights. Acta Anaesthesiol Scand 1991; 35:87-96.
19. Collins JF, Smith JD, Coalson JJ, Johanson WG, Jr. Variability in lung collagen amounts after prolonged support of acute respiratory failure. Chest 1984; 85:641-646.[Abstract/Free Full Text]
20. Webb HH, Tierney DF. Experimental pulmonary edema due to intermittent positive pressure ventilation with high inflation pressures: protection by positive end-expiratory pressure. Am Rev Respir Dis 1974; 110:556-565.[Medline]
21. Dreyfuss D, Soler P, Basset G, Saumon G. High inflation pressure pulmonary edema: respective effects of high airway pressure, high tidal volume, and positive end-expiratory pressure. Am Rev Respir Dis 1988; 137:1159-1164.[Medline]
22. Deneke SM, Fanburg BL. Normobaric oxygen toxicity of the lung. N Engl J Med 1980; 303:76-86.[Medline]
23. Last JA, Siefkin AD, Reiser KM. Type I collagen content is increased in lungs of patients with adult respiratory distress syndrome. Thorax 1983; 38:364-368.[Abstract]
24. Suchyta MR, Elliott CG, Colby T, Rasmusson BY, Morris AH, Jensen RL. Open lung biopsy does not correlate with pulmonary function after the adult respiratory distress syndrome. Chest 1991; 99:1232-1237.[Abstract/Free Full Text]
25. Zwillich CW, Pierson DJ, Creagh CE, Sutton FD, Schatz E, Petty TL. Complications of assisted ventilation: a prospective study of 354 consecutive episodes. Am J Med 1974; 57:161-170.[Medline]
26. Albelda SM, Gefter WB, Kelley MA, Epstein DM, Miller WT. Ventilator-induced subpleural air cysts: clinical, radiographic, and pathologic significance. Am Rev Respir Dis 1983; 127:360-365.[Medline]
27. Parker JC, Hernandez LA, Peevy KJ. Mechanisms of ventilator-induced lung injury. Crit Care Med 1993; 21:131-143.[Medline]
28. Churg A, Golden J, Fligiel S, Hogg JC. Bronchopulmonary dysplasia in the adult. Am Rev Respir Dis 1983; 127:117-120.[Medline]
29. Rotman HH, Lavelle TF, Jr, Dimcheff DG, VandenBelt RJ, Weg JG. Long-term physiologic consequences of the adult respiratory distress syndrome. Chest 1977; 72:190-192.[Abstract/Free Full Text]
30. Douglas MME, Downs JB. Pulmonary function following severe acute respiratory failure and high levels of positive end-expiratory pressure. Chest 1977; 71:18-23.
31. Lakshminarayan S, Stanford RE, Petty TL. Prognosis after recovery from adult respiratory distress syndrome. Am Rev Respir Dis 1976; 13:7-16.
32. Peters JI, Bell RC, Prihoda TJ, Harris G, Andrews C, Johanson WG, Jr. Clinical determinants of abnormalities in pulmonary functions in survivors of the adult respiratory distress syndrome. Am Rev Respir Dis 1989; 139:1163-1168.[Medline]
33. Ghio AJ, Elliott CG, Crapo RO, Berlin SL, Jensen RL. Impairment after adult respiratory distress syndrome: an evaluation based on American Thoracic Society recommendations. Am Rev Respir Dis 1989; 139:1158-1162.[Medline]
34. Elliott CG, Morris AH, Cengiz M. Pulmonary function and exercise gas exchange in survivors of adult respiratory distress syndrome. Am Rev Respir Dis 1981; 123:492-495.[Medline]
35. Ostrow D, Cherniack RM. Resistance to airflow in patients with diffuse interstitial lung disease. Am Rev Respir Dis 1973; 108:205-209.[Medline]
36. Fulmer JD, Roberts WC, von Gal ER, Crystal RG. Small airways in idiopathic pulmonary fibrosis: comparison of morphologic and physiologic observations. J Clin Invest 1977; 60:595-610.

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				Y.-C. Chang, C.-J. Yu, S.-C. Chang, J. R. Galvin, H.-M. Liu, C.-H. Hsiao, P.-H. Kuo, K.-Y. Chen, T. J. Franks, K.-M. Huang, et al. Pulmonary Sequelae in Convalescent Patients after Severe Acute Respiratory Syndrome: Evaluation with Thin-Section CT Radiology, September 1, 2005; 236(3): 1067 - 1075. [Abstract] [Full Text] [PDF]

				D. A. Lynch, W. D. Travis, N. L. Muller, J. R. Galvin, D. M. Hansell, P. A. Grenier, and T. E. King Jr Idiopathic Interstitial Pneumonias: CT Features Radiology, July 1, 2005; 236(1): 10 - 21. [Abstract] [Full Text] [PDF]

				T Fischer, J H Reynolds, and S E Trotter The idiopathic interstitial pneumonias: a beginner's guide Imaging, October 1, 2004; 16(1): 37 - 49. [Abstract] [Full Text] [PDF]

				H.-H. Hsu, C. Tzao, C.-P. Wu, W.-C. Chang, C.-L. Tsai, H.-J. Tung, and C.-Y. Chen Correlation of High-Resolution CT, Symptoms, and Pulmonary Function in Patients During Recovery From Severe Acute Respiratory Syndrome Chest, July 1, 2004; 126(1): 149 - 158. [Abstract] [Full Text] [PDF]

				E. D. Moloney and M. J. D. Griffiths Protective ventilation of patients with acute respiratory distress syndrome Br. J. Anaesth., February 1, 2004; 92(2): 261 - 270. [Abstract] [Full Text] [PDF]

				G. M. Joynt, G. E. Antonio, P. Lam, K. T. Wong, T. Li, C. D. Gomersall, and A. T. Ahuja Late-Stage Adult Respiratory Distress Syndrome Caused by Severe Acute Respiratory Syndrome: Abnormal Findings at Thin-Section CT Radiology, February 1, 2004; 230(2): 339 - 346. [Abstract] [Full Text] [PDF]

				B. Trotman-Dickenson Radiology in the Intensive Care Unit (Part 2) J Intensive Care Med, September 1, 2003; 18(5): 239 - 252. [Abstract] [PDF]

				D. M. Hansell Small-Vessel Diseases of the Lung: CT-Pathologic Correlates Radiology, December 1, 2002; 225(3): 639 - 653. [Abstract] [Full Text] [PDF]

				T Whitehead and A S Slutsky The pulmonary physician in critical care * 7: Ventilator induced lung injury Thorax, July 1, 2002; 57(7): 635 - 642. [Abstract] [Full Text] [PDF]

				American Thoracic Society/European Respiratory Society International Multidisciplinary Consensus Classification of the Idiopathic Interstitial Pneumonias . This Joint Statement of the American Thoracic Society (ATS), and the European Respiratory Society (ERS) was adopted by the ATS Board of Directors, June 2001 and by The ERS Executive Committee, June 2001 Am. J. Respir. Crit. Care Med., January 15, 2002; 165(2): 277 - 304. [Full Text] [PDF]

				L. GATTINONI, P. CAIRONI, P. PELOSI, and L. R. GOODMAN What Has Computed Tomography Taught Us about the Acute Respiratory Distress Syndrome? Am. J. Respir. Crit. Care Med., November 1, 2001; 164(9): 1701 - 1711. [Full Text] [PDF]

				P. Scillia, S. A. Kafi, C. Melot, C. Keyzer, R. Naeije, and P. A. Gevenois Oleic Acid-induced Lung Injury: Thin-Section CT Evaluation in Dogs Radiology, June 1, 2001; 219(3): 724 - 731. [Abstract] [Full Text] [PDF]

				I. GOLDSTEIN, M.-T. BUGHALO, C.-H. MARQUETTE, G. LENAOUR, Q. LU, J.-J. ROUBY, and the Experimental ICU Study Group Mechanical Ventilation-induced Air-Space Enlargement during Experimental Pneumonia in Piglets Am. J. Respir. Crit. Care Med., March 15, 2001; 163(4): 958 - 964. [Abstract] [Full Text]

				S. R. Desai, A. U. Wells, G. Suntharalingam, M. B. Rubens, T. W. Evans, and D. M. Hansell Acute Respiratory Distress Syndrome Caused by Pulmonary and Extrapulmonary Injury: A Comparative CT Study Radiology, March 1, 2001; 218(3): 689 - 693. [Abstract] [Full Text]

				Michigan abstracts Perfusion, May 1, 2000; 15(3): 263 - 270. [PDF]

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