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Thoracic Imaging |
1 From the Departments of Anaesthesia and Intensive Care (G.M.J., P.L., T.L., C.D.G.) and Radiology and Organ Imaging (G.E.A., K.T.W., A.T.A.), Chinese University of Hong Kong, Shatin NT, Hong Kong. Received June 13, 2003; revision requested July 22; final revision received September 4; accepted September 16. Address correspondence to G.E.A. (e-mail: gregantonio@cuhk.edu.hk).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Eight patients in the late stage of ARDS (ie, more than 2 weeks after onset) were imaged with thin-section CT. Images were evaluated for ground-glass opacification, consolidation, interstitial thickening, evidence of fibrosis, and any other abnormalities. Patient records were reviewed, and relevant respiratory and ventilatory parameters, total steroid dose, and outcome were recorded.
RESULTS: All patients received high-dose pulse methylprednisolone (minimum, 2.5 g total), and all patients who received ventilation received low-pressure, low-volume ventilation. Five patients received prolonged mechanical ventilation (for more than 14 days), one received ventilation for 72 hours, and two patients did not receive ventilation. Three patients died, four were discharged from the hospital, and one continued to require ventilation. Ground-glass opacification and interstitial thickening were present at CT in all eight patients. Consolidation was present in six patients. Three patients had evidence of fibrosis. Patients who received long-term ventilation, those who received short-term ventilation, and those who did not receive ventilation had similar pulmonary changes at CT. Pulmonary cysts, most of which were small (<1 cm), were present in five patients. Cysts were present in one patient who received only short-term low-pressure and low-volume ventilation and in one patient who received no mechanical ventilation.
CONCLUSION: The CT features of late-stage ARDS caused by SARS are similar to those seen in late-stage ARDS of other causes, with no apparent differences between patients who do and patients who do not receive prolonged mechanical ventilation. The presence of cysts in one patient who received short-term and one patient who received no mechanical ventilation suggests that severe SARS-induced ARDS may independently result in cyst formation.
© RSNA, 2004
Index terms: Lung, CT, 60.12118 • Lung, fibrosis, 60.792 • Lung, ground-glass opacification, 60.2069 • Respiratory distress syndrome, adult (ARDS), 60.4132, 60.4134 • Severe acute respiratory syndrome (SARS), 60.2069
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The respiratory failure seen in SARS is accompanied by the appearance of progressive opacification on chest radiographs (5); however, chest radiographs provide only limited information regarding the nature and extent of pathologic changes in lung tissue. The use of computed tomography (CT) aided the understanding of ARDS in the mid-1980s. On the basis of radiographic findings, ARDS was initially thought to be a homogeneous, diffuse disease affecting parenchymal lung tissue.
However, CT scans obtained in critically ill patients demonstrated unexpected heterogeneous patterns (6). These findings fundamentally changed the understanding of the pathophysiologic mechanisms of ARDS and eventually resulted in changes in clinical care (7). It has also been suggested that the pathogenesis of acute lung injury and ARDS results in specific morphologic changes seen at CT, and typical changes have been described for acute lung injury and ARDS of different causes (8). It is also known that there are changes in the CT findings over time—changes that are particularly related to the duration of mechanical ventilation and the natural evolution of ARDS (9).
The purpose of this study was to evaluate abnormal thin-section CT findings in patients in the ICU during the late stage of ARDS caused by SARS.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Between March 17 and April 21, 2003, a total of 44 patients were admitted to the ICU at our institution. Of these patients, 20 met the criteria for late-stage SARS. The number of patients with SARS admitted to the hospital during the relevant period was 275. Imaging was not performed for all patients with chronic SARS. CT imaging was not considered appropriate if death was imminent or unavoidable, if patients were not considered clinically stable enough to transport to the radiology suite, if patients or relatives declined to give consent, or if patients were already showing signs of steady improvement in their condition.
A total of eight patients with SARS who were admitted to the ICU in the late stage of ARDS (ie, more than 2 weeks after the onset of ARDS [9]) were imaged. They constituted 2.9% of the total number of patients with SARS in our institution (ie, 275 patients) and 18% of the total number of patients with SARS in the ICU (ie, 44 patients) during the relevant time period. The mean age of the patients was 49.1 years (age range, 33–73 years), and there were six men and two women. The baseline characteristics of the patients included in the series are shown in Table 1. All patients had SARS as defined by existing U.S. Centers for Disease Control and Prevention criteria (10). ARDS was defined according to the criteria of the American-European Consensus Conference on ARDS (11).
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Oxygen Therapy and Mechanical Ventilation
Patients who developed hypoxemia were given oxygen through nasal cannulae and/or high-flow reservoir masks. Intubation was performed and patients received ventilation when there was persistent failure to achieve arterial oxygen saturation of 90% while they were receiving 100% oxygen through a high-flow reservoir mask and/or at onset of respiratory muscle fatigue as evidenced by sweating, tachycardia, an increase in partial pressure of arterial carbon dioxide, and/or a subjective feeling of exhaustion.
Pressure-control mechanical ventilation was used. Positive end-expiratory pressure (PEEP) and inspired oxygen concentration were titrated to achieve an arterial saturation of 90%–95%. Tidal volume was maintained at 6–8 mL/kg of estimated lean body weight, and peak pressure was maintained at 30 cm H2O or lower. The partial pressure of arterial carbon dioxide was allowed to rise, provided the pH was greater than 7.15 (12). Patients who did not meet the above parameters received ventilation in the prone position. Fluid intake was strictly controlled to equalize intake and output. Patients were otherwise cared for according to standard ICU protocols.
Data Collection
All physiologic and treatment data were collected as part of routine clinical care and documentation. The following data were extracted and recorded by P.L. and G.M.J. at a review of patient records: duration of mechanical ventilation and daily (0800) absolute values for tidal volume, peak airway pressure, PEEP, and the ratio of partial pressure of arterial oxygen to the fraction of inspired oxygen. The daily absolute values were then used to calculate the mean and median values presented in the Results section. The total dose of pulse methylprednisolone and the outcome of the patient’s stay in the ICU were also recorded.
CT Scanning Protocol
All examinations were performed with the same CT scanner (HighSpeed Advantage; GE Medical Systems, Milwaukee, Wis) in nonhelical mode with the patient in a supine position. The scanning protocol included the following parameters: 1-mm section thickness with 6-mm gap, 1-second scanning time, 120 kV, and 140 mA. Spontaneously breathing patients were scanned during voluntary inspiration, and patients who were receiving mechanical ventilation were scanned when respiration was mechanically suspended during expiratory pause at zero PEEP. The CT examinations were performed an average of 37 days (range, 22–54 days) after the onset of ARDS. Thin-section CT rather than conventional CT (ie, CT with a 7- or 10-mm section thickness) was performed in view of a previous report that described thin-section CT findings in SARS (13). Each patient underwent CT only once during his or her ICU stay.
Viewing and Assessment of CT Images
The CT images were retrospectively reviewed by two radiologists (A.T.A. and G.E.A., with 13 and 8 years of experience in thoracic CT image interpretation, respectively) by using a viewing console (HighSpeed Advantage Workstation 3.1; GE Medical Systems) and were interpreted by using the descriptors proposed by the Fleischner Society Nomenclature Committee (14). Findings and interpretations were based on consensus opinion. The window width used was 1,500 HU, and the window length was -700 HU. These were altered if further analysis of a particular lesion (ie, area of abnormality) was required. Similarly, lesions were magnified by using a built-in zoom function.
Ground-glass opacification was defined as increased lung parenchymal attenuation that did not obscure the underlying vascular architecture (14). Consolidation was defined as opacification that obscured the underlying vasculature (14). Each segment of the lung was reviewed for lesions, and the extent of involvement of each segment was described as small (ie, 1 to less than 3 cm of segment involved), subsegmental (ie, 3 cm to less than 50% of segment involved), or segmental (ie, 50%–100% of segment involved). By using this grading scheme, the distribution of ground-glass opacification was further defined as either confluent (ie, involving 50%–100% of a segment) or patchy (ie, consisting of multiple small [1–3-cm] discrete areas, with lung parenchyma of normal attenuation existing between such areas).
Each lesion was magnified and examined for intralobular interstitial, interlobular septal, or peribronchovascular interstitial thickening. Attention was also paid to the presence of nodules or masses, lymphadenopathy, cavitation or calcification, bronchiolar and/or bronchial dilatation, overinflated secondary pulmonary lobules, pulmonary interstitial emphysema, pneumothorax, and pneumomediastinum. The presence of parenchymal bands; irregular bronchovascular, pleural, or mediastinal interfaces; and traction bronchiectasis was considered evidence of probable fibrosis (15–18). Thickened interstitium was not used as evidence of probable fibrosis because it may also be present during the early stage of SARS (13). Any other abnormalities were noted.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Ground-Glass Opacification
CT findings are summarized in Table 3. All eight patients had areas of ground-glass opacification that involved most segments of the lung (all 18 lung segments in five patients and 15 segments in three patients). Bilateral involvement was seen in all patients. The opacification was confluent and segmental in five patients and patchy and segmental in three. In two patients (patients 6 and 7), the most peripheral 5 mm of lung were spared (Fig 1). In one patient (patient 5), there was a patchy pattern of attenuation, with secondary lobules of ground-glass opacification and apparently hyperinflated secondary lobules (Fig 2). The secondary lobules that were of low attenuation were overinflated but still showed thickened interlobular septae. The lobules with higher attenuation were of relatively smaller caliber.
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Evidence of Fibrosis
Three patients had evidence of fibrosis—that is, irregular interfaces (bronchovascular, pleural, or mediastinal), parenchymal bands, and traction bronchiectasis (Fig 4). These were the same patients (patients 4, 6, and 7) who had irregular septal thickening.
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Other Findings
There was no evidence of lymphadenopathy, calcification, discrete nodules, or mass in any of the patients. Bronchiolar and/or bronchial dilatation was not present outside the areas of traction bronchiectasis in any patient.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The natural progression of ARDS has been well described. The early or exudative stage is characterized by pulmonary edema with early hyaline membrane formation. The intermediate stage begins in the 2nd week and is a transition period during which edematous fluid is reabsorbed and proliferative processes begin. Fibrous processes begin to appear from the 2nd week onward and are visible at CT in this stage of ARDS (9). These processes are manifested radiologically by the appearance of architectural distortions (ie, irregular interfaces and traction bronchiectasis), a reticular pattern (with septal thickening and parenchymal bands), and subpleural cysts (7,20). In a study by Desai et al (20) of the appearance of ARDS at follow-up CT, CT findings of fibrosis (described as a reticular pattern) were present in six (22.2%) of 27 patients 7.7 days after intubation and in 85.2% of patients 196.2 days after intubation. In the present study, three (38%) of eight patients had CT signs of fibrosis 37 days after the onset of ARDS. More signs of probable fibrosis may become apparent at CT in our patients as the consolidation resolves with time, in accordance with a relationship observed by Desai et al (20).
The cystic changes seen at thin-section CT in our patients were similar to those observed in the late stage of ARDS (9). The cysts seen in the present study were not a feature in a previous study involving treated patients with SARS who underwent early follow-up (18). Therefore, these cysts may be a result of ARDS or a consequence of mechanical ventilation. Subpleural cysts of similar size and distribution have been considered by others (7,21) to represent the organization and fibrotic phase of ARDS (ie, the 2nd week of ARDS and beyond). These cysts may be an indicator of a fibrosing process and may themselves not be permanent.
Pulmonary cysts have also sometimes been attributed to overdistention of the lung during positive pressure ventilation (7,22). It has always been assumed that the changes seen in patients receiving positive pressure ventilation represent a combination of the effects of the primary disease that is causing inflammatory changes in the lung parenchyma and the damage caused by prolonged positive pressure ventilation itself (9). The cystic changes or bullae, in particular, have been attributed to "volutrauma/barotrauma" (7).
To our knowledge, CT findings in patients with chronic ARDS who are not receiving ventilation have not been reported. Mechanical ventilation was avoided in our patients with SARS because early on we observed a high incidence of barotrauma in these patients. The presence of single-organ respiratory failure in this group also allowed spontaneous breathing to be comfortably tolerated longer than would normally be the case. As a consequence, a number of our patients did not receive mechanical ventilation, despite the fact that they met the criteria for ARDS. In the present study, cysts were observed in one patient (patient 6) who received only short-term low-pressure and low-volume ventilation and in one patient (patient 7) who received no mechanical ventilation at all. This suggests that severe SARS-induced ARDS may independently result in cyst formation.
It is too early to be certain that the lung abnormalities that suggest fibrosis will become permanent fibrotic tissue in these patients, but some of the gross architectural distortion is unlikely to resolve. The appearance of this probable fibrosis was similar to that described in another report of thin-section CT findings in the early follow-up of patients with SARS (18).
Four of the patients in the present study developed pneumothorax on at least one side. In view of the relative success achieved in our study in meeting the requirements of low-volume and low-pressure ventilation, this was a surprising finding. The lack of evidence of overinflation on the CT images in these four patients also suggests that the patients were receiving appropriate ventilation; this, and the relatively unusual occurrence of pneumothorax in a spontaneously breathing patient, would tend to support the view that the disease process itself might predispose a patient to develop pneumothorax.
Images in one patient (patient 5) demonstrated an interesting patchy pattern of attenuation with secondary lobules of ground-glass opacification and apparently hyperinflated secondary lobules. This patient did not have pneumothorax or pneumomediastinum. The patchy pattern may represent the appearance resulting from differential ventilation— an appearance in which overinflated secondary lobules are mixed with ventilated lobules with interstitial thickening. When patients with ARDS receive mechanical ventilation with positive pressure and PEEP, poorly aerated lobules may be recruited and previously normally aerated regions may become overinflated.
The widespread distribution of ground-glass opacification in our patients is consistent with the distribution seen in CT images in patients with ARDS (7,23). Similarly, the finding of consolidation in the dependent segments of the lung is also common in ARDS. Ground-glass opacification is a nonspecific CT sign and may represent interstitial edema, inflammation, or fibrosis, depending on the stage of the disease process (24). The sparing of the most peripheral 5 mm of the lung from ground-glass opacification observed in our study was similar to that seen in cases of pulmonary edema, suggesting that a component of interstitial edema was present in some of our patients. The posterior or dependent segments of the lung were preferentially involved in patients who had consolidation. This, again, is in keeping with the distribution of consolidation observed in other studies of CT findings in ARDS (7,23). The size of the areas of consolidation in the present study varied (four patients had 1–3-cm lesions only, and two patients had segmental lesions in addition to 1–3-cm lesions).
We found evidence of pulmonary fibrosis in three patients. These were also the patients who had the least amount of consolidation (two patients had no consolidation, and one patient had only two segments affected by consolidation). These three patients were probably in the late fibrotic phase of ARDS. The findings of probable pulmonary fibrosis are similar to those described in a report of a larger study of the thin-section CT findings in treated patients with SARS (18). Although steroid therapy has been suggested as a means of shortening the fibrotic phase of ARDS (25), all of the three patients with evidence of fibrosis in our study had received moderately high doses of methylprednisolone.
In conclusion, the thin-section CT features of late-stage ARDS caused by SARS are similar to those seen in late-stage ARDS with other causes, and similar features were noted in patients who received prolonged mechanical ventilation (ie, for more than 14 days) and in those who did not. Features of late-stage ARDS may be present even in patients with SARS who do not receive mechanical ventilation.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, G.M.J., A.T.A.; study concepts, G.M.J., G.E.A., A.T.A., T.L.; study design, G.M.J., G.E.A.; literature research, G.M.J., G.E.A.; clinical studies, G.M.J., P.L., T.L., C.D.G.; data acquisition, P.L., G.E.A., K.T.W., T.L.; data analysis/interpretation, G.M.J., G.E.A.; statistical analysis, G.M.J., G.E.A.; manuscript preparation and definition of intellectual content, G.M.J., G.E.A., P.L.; manuscript editing and revision/review, G.M.J., A.T.A.; manuscript final version approval, G.M.J., G.E.A., A.T.A.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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