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Thoracic Imaging |
1 From the Department of Radiology, Harvard Medical School, Boston, Mass (A.A.B.); and the Departments of Pulmonology (A.V.M., C.K., M.E.) and Radiology (P.A.G.), Erasme Hospital, Free University of Brussels, Belgium. Received March 9, 2000; revision requested April 11; revision received June 26; accepted July 25. A.A.B. supported by a research grant from the Max Kade Foundation. Address correspondence to A.A.B., Department of Radiology, University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria (e-mail: alexander.bankier@univie.ac.at).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Over 7 years, 111 combined inspiratory and expiratory computed tomographic examinations were performed in eight healthy control subjects and 38 heart-lung transplant recipients. Functional impairment was assessed with the BOS classification. Receiver operating characteristic (ROC) analysis was performed to determine the optimal threshold of air trapping to distinguish between patients with and those without BOS and to compute sensitivity and specificity for diagnosing BOS.
RESULTS: The extent of air trapping increased with BOS severity (P = .001). A threshold of 32% of air trapping is optimal for distinguishing between patients with and those without BOS and provides a sensitivity of 83%, a specificity of 89%, and an accuracy of 88%. The prevalence of BOS and positive predictive value of air trapping increased with postoperative time, but the negative predictive value of air trapping remained high throughout the study. Patients without BOS who had air trapping exceeding 32% of the parenchyma were at significantly increased risk of developing BOS (P = .004).
CONCLUSION: At the threshold of 32%, air trapping is sensitive, specific, and accurate for diagnosing BOS. Patients with air trapping below 32% are unlikely to have BOS. Air trapping exceeding 32% may be an early indicator of future BOS.
Index terms: Bronchiolitis obliterans, 60.2191, 671.755 • Computed tomography, comparative studies, 60.12111, 60.12118, 60.12119 • Computed tomography (CT), thin-section, 60.12118 • Lung, CT, 60.12111, 60.12118 • Lung, transplantation, 60.459
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The findings of two prior studies (4,5) have provided evidence that air trapping on expiratory computed tomographic (CT) scans is an accurate indicator of the bronchiolar obliterations that underlie BOS. This evidence, however, was based on small numbers of patients (4,5). Also, a control group was not used (4) and air trapping was not compared with the decline of FEV1 (5). Moreover, no information about the evolution of air trapping over time was obtained. Thus, both the potential of air trapping in the diagnosis of BOS and the role of expiratory CT in the follow-up of lung transplant recipients remain unclear. The purpose of our study, therefore, was twofold: to determine the test performance of air trapping for the diagnosis of BOS in a representative population of lung transplant recipients and to analyze the longitudinal evolution of air trapping, with emphasis on its potential contribution to the early detection of chronic allograft dysfunction.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Indications for transplantation were cystic fibrosis (n = 17), primary pulmonary hypertension (n = 11), Eisenmenger syndrome (n = 3), bronchiectasis (n = 3), idiopathic pulmonary fibrosis (n = 1), Langerhans cell histiocytosis (n = 1), coal worker’s pneumoconiosis (n = 1), or pulmonary emphysema resulting from 
-1-antitrypsin deficiency (n = 1). The hearts and lungs transplanted into these patients had been donated by 38 individuals (16 female patients, 22 male patients) with a mean age of 29 years ± 11 (age range, 10–50 years).
Throughout the current study, expiratory CT examinations were performed whenever the inspiratory CT examination did not disclose parenchymal abnormalities other than bronchiectasis or bronchial wall thickening. This criterion was chosen because the presence of parenchymal abnormalities might have potentially acted as a confounding factor in the interpretation of expiratory CT images and thereby made the assessment of air trapping less accurate. A total of 115 expiratory CT examinations were performed in the patients. These had been performed either for yearly routine follow-up (n = 81) or for clinical indications (n = 34). Clinical indications were suspected pulmonary infection (n = 14), decreased FEV1 (n = 13), suspected lymphoma (n = 1), and follow-up after treatment for bacterial pneumonia (n = 4), cytomegalovirus infection (n = 1), or pulmonary lymphoma (n = 1). At four of the latter CT examinations, infectious bronchitis (n = 2) or acute allograft rejection (n = 2) was diagnosed. Because both conditions may affect the small airways in lung transplant recipients, the corresponding CT scans were discarded (6,7). Our analysis was thus based on the results of a total of 111 combined inspiratory and expiratory CT examinations. The time frames in which these CT examinations were performed are detailed in Table 1.
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Pulmonary Function Tests
Pulmonary function tests were performed in patients and healthy control subjects within 24 hours before or after the CT examinations. Functional residual capacity, total lung capacity, and residual volume were measured with the patient seated in a constant volume body plethysmograph (Body Test; Jaeger, Wuerzburg, Germany). Measurements of forced vital capacity, FEV1, and mid-expiratory flow rates (FEF25–75) were made by using a model 2400 unit (Sensormedics, Anaheim, Calif) and following the guidelines of the American Thoracic Society (8). Predicted values for static and dynamic lung volumes were derived from the literature (8,9).
The severity of BOS was graded by following the recommendations of the International Society for Heart and Lung Transplantation (3). In accordance with these recommendations, a grade of 0 indicated a FEV1 of more than 80% of the best postoperative value; 1, a sustained decline in FEV1 between 80% and 66% of the best postoperative value; 2, a sustained decline between 65% and 50% of the best postoperative value; and 3, a sustained decline of less than 50% of the best postoperative value.
CT Examinations
Thin-section CT images were obtained by using commercially available scanners (Somatom Plus 4, Plus 4A, Plus 4C; Siemens Medical Systems, Erlangen, Germany). Patients were examined while in a supine position, and none received contrast material. Examinations were performed during breath holding at full suspended inspiration and full suspended expiration. Breath holding at both volumes was rehearsed with each patient prior to the CT examination. The acquisition time was 1 second per section, and the tube current was 140 kV at 171 mA. The section thickness was 1 mm, with a 10-mm intersection interval. All examinations were performed from the apex to the base of the lungs. Images were reconstructed by using a high-spatial-resolution (bone) algorithm at a display window width of 1,600 HU and a window center of -600 HU. Twelve images were obtained per sheet of 35.5 x 43.0-cm film.
Image Analysis
Image analysis was performed by two board-certified chest radiologists (A.A.B., P.A.G.) who were experienced in interpreting thoracic CT scans. Each radiologist analyzed all 111 CT scans. Analyses were performed in two separate and independent sessions. CT scans obtained in the healthy control subjects were analyzed in a single session. Both radiologists were unaware of clinical and functional information. For all CT examinations, all sections obtained above the level of the diaphragm were analyzed. Each section was assessed individually, but left and right lungs were not graded separately.
CT at full suspended inspiration.—Because our study was focused exclusively on air trapping, CT images obtained at full suspended inspiration were used only for comparison with the corresponding CT images obtained at full suspended expiration. Bronchial and vascular abnormalities were not recorded. However, bronchial and vascular abnormalities were used to overcome potentially confounding features of airway and vascular diseases (10).
CT at full suspended expiration.—Air trapping was considered to be present on the expiratory CT images when lung regions failed to increase in attenuation and/or failed to decrease in volume, as compared with the corresponding inspiratory images (11). The diagnosis of air trapping was based on visual assessment, and quantitative measurements were not obtained. The scoring system used to assess the extent of air trapping was adapted from prior studies (4,12,13) and modified slightly, in that the number of possible scores was increased from five to six to allow for a more subtle grading of air trapping. A score of 0 was assigned if there was no abnormality; 1, if less than 20% of the parenchyma in the section showed air trapping; 2, if 20%–39% showed air trapping; 3, if 40%–59% showed air trapping; 4, if 60%–79% showed air trapping; or 5, if more than 80% showed air trapping. This yielded a maximum possible score of 5 per CT scan. The air trapping scores of each scan were added and expressed as a percentage of the maximum possible (ie, if each scan had been assigned a score of 5).
Statistical Analysis
Our analysis of air trapping and comparison of air trapping with functional data followed a stepwise approach. First, we studied the association between air trapping scores and severity of functional impairment, as determined by using the BOS grades. For this purpose, a Kruskall-Wallis analysis of variance was applied to our overall patient population, with the BOS grades as a potential cause of variation. Then pairwise comparisons were made between the subgroup with a BOS grade of 0 and the normal controls and between the subgroup with a BOS grade of 0 and the other three subgroups. For these pairwise comparisons, we performed the Mann-Whitney test, and Bonferroni correction was applied, given the repetitive character of the original measurements.
Second, we studied the test performance of air trapping in the diagnosis of BOS. We therefore performed receiver operating characteristic (ROC) analysis and determined the optimal threshold of air trapping that was required to distinguish between patients who did and those who did not have BOS. This threshold was defined as the intersection of the ROC curve with the second bisectrix, at which sensitivity equaled specificity (14). Detailed sensitivity, specificity, and diagnostic accuracy of air trapping in the diagnosis of BOS were calculated. The test performance of air trapping was also analyzed by using a sustained 12% decline of the FEV1 and a sustained 25% decline of FEF25–75 as an alternative standard of reference (15,16). Furthermore, we calculated the prevalence of BOS in the patient population at given times after transplantation. On the basis of these prevalences, positive and negative predictive values for air trapping were determined by using the Bayes theorem (17,18).
Third, we studied the longitudinal course of all patients who received a BOS grade of 0 at their first expiratory CT examination and underwent subsequent CT examinations. CT examination results were classified as either false positive (air trapping score exceeding the threshold determined with ROC analysis) or true negative (air trapping score below the threshold determined with ROC analysis). The course of the CT scores and FEV1 was followed over time, and a potential onset of BOS was noted. The subgroups resulting from this analysis were compared by performing the two-tailed Fisher exact test.
Interobserver agreement in the assessment of air trapping was analyzed by using a weighted 
statistic (19). The 95% CIs for the statistics were calculated. The null hypothesis of no agreement between the two observers was tested, and the associated P values were calculated (20). The weighted values were compared by performing a test based on a standard normal statistic; this statistic uses the estimation of the asymptotic standard error on a weighted statistic, as presented by Cohen (21). All values were interpreted on the basis of data in the literature (19,22): A value of less than 0.20 indicated poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, good agreement; and 0.81–1.00, excellent agreement.
All statistical analyses were performed on a personal computer by using commercially available software (Statistica version 5.0; StatSoft, Tulsa, Okla and StatXact version 3; Cytel, Cambridge, Mass). Data with a normal distribution were expressed as means plus or minus 1 SD, and data with a skewed distribution were expressed as medians with their 25% and 75% quartiles. Significance for all tests was set at the P 
.05 level.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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In the subgroup with a BOS grade of 0, 10 CT examinations performed in six patients who underwent more than one CT examination were false-positive (air trapping score >32%). Of these six patients, five subsequently developed BOS; all five had air trapping exceeding 32% at follow-up CT. The remaining patient was returned to the true-negative category. In the other 24 patients with a BOS grade of 0 who underwent more than one CT examination, 69 CT examinations were true-negative (air trapping score <32%). Of these 24 patients, four were excluded because they underwent at least one false-positive CT examination at subsequent follow-up. Of the remaining 20 patients, three eventually developed BOS, and all three had air trapping exceeding 32% at follow-up CT. In contrast, all 17 patients who did not develop BOS had air trapping of less than 32% at follow-up CT. The fraction of patients with false-positive CT examinations (five of six) who developed BOS was significantly greater (P = .004) than the fraction of patients with true-negative CT examinations (three of 20) who developed BOS.
Data on interobserver agreement in the assessment of air trapping, as determined by using the weighted statistics, showed that interobserver agreement was excellent for the subgroups with a BOS grade of 0, 1, or 2 and good for the subgroup with a BOS grade of 3. The lack of overlap between the 95% CIs of the values in the subgroups with BOS grades of 0 or 1 with those in the subgroup with a BOS grade of 3 indicated that the difference between those values (excellent and good, respectively) was significant (P = .001). The null hypothesis of no agreement between the two observers was rejected. Details of interobserver agreement analysis are summarized in Table 4.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The potential of expiratory CT in depicting BOS was highlighted by the shape of the ROC curve. Both the arch of the curve and the large area under the curve identified expiratory CT as accurate for the diagnosis of BOS (14). By using the 32% threshold, we found air trapping to have a sensitivity and specificity of 88% and an accuracy of 87%. The prevalence of BOS steadily increases with postoperative time (2). The positive predictive value of CT, therefore, gradually improved. On the other hand, the negative predictive value of CT barely changed over time and remained high throughout the study. This indicates that patients with air trapping below 32% have a high probability of not having BOS, even at a time point distant from transplantation.
No significant difference was found between air trapping scores of patients assigned to the subgroups with BOS scores of 1, 2, or 3. This might have been due to the relatively small number of individuals included in each subgroup. It might also suggest that once BOS is established, the extent of air trapping does not necessarily reflect the degree of functional impairment.
Investigators in at least two previous investigations have performed expiratory CT in lung transplant recipients with biopsy-proved BOS. Leung et al (4) performed 21 CT examinations in 21 patients, 11 of whom had BOS. Air trapping was considered abnormal if it exceeded 25%, but no healthy control subjects were examined to validate this threshold. Worthy et al (5) examined 15 patients with BOS, and air trapping was considered abnormal when it exceeded one pulmonary segment. Given the varying size of anatomic lung segments, this approach does not permit quantification of the extent of air trapping. In addition, investigators in both studies restricted expiratory CT to the acquisition of five images per patient. This might not provide representative samples because BOS is heterogeneously distributed throughout the lungs (1). We therefore believe that the use of a validated threshold of air trapping and CT examinations covering the entire lungs strengthened our results.
Despite these differences in study design, our results are congruent with those reported previously. Leung et al (4) and Worthy et al (5) found air trapping to have 80%–91% sensitivity, 80%–94% specificity, and 86% accuracy for the detection of biopsy-proved BOS. Other than that in the current study, however, no correlation was found between the extent of air trapping scores and the degree of functional impairment, as assessed by using the BOS grades (4). This lack of correlation was attributed to inter- and intrapatient variation in the volumes at which CT data were obtained and to motion artifacts on the CT images (4). In the current study, we attempted to acquire CT data as close as possible to residual volume by training our patients prior to the CT examinations. We did not assess motion artifacts on the resultant CT images, but, according to the two radiologists in charge of image review, motion artifacts were minor and constituted no obstacle to image interpretation.
This was indirectly supported by the good to excellent interobserver agreement for the assessment of air trapping in the current study. Investigators in prior studies (24,25) have shown that expiratory CT is accurate in the detection of air trapping that is unrelated to lung transplantation and that a semiquantitative scoring system, like the one used in the current study, is suitable for assessing the extent of air trapping. Although CT scans were reviewed by two radiologists in the studies by Leung et al (4) and Worthy et al (5), no formal assessment of interobserver agreement was reported.
From a clinical perspective, stabilization or resolution of bronchiolitis obliterans in response to treatment is more likely to occur if treatment is initiated while patients still have a BOS grade of 0 (1). We find it interesting that five of the six patients whose CT examinations were initially classified as false-positive (patients with a BOS grade of 0 and an air trapping score exceeding 32%) subsequently developed BOS. This observation indicates that CT might be used to provide evidence of abnormal air trapping before the FEV1 declines below 80% of the best postoperative value. Although this FEV1 decline has been used to define the onset of BOS in the international classification, investigators in two studies (15,16) have suggested that using a 12% decline of FEV1 or a 25% decline in FEF25–75 would be more appropriate for detection of chronic allograft dysfunction. We therefore performed a complementary analysis of our data by using these parameters as alternative standards of reference. As expected, the resultant ROC curves were slightly displaced toward lower values of sensitivity and specificity. The shapes of the ROC curves and the areas under the curves, however, were comparable with those of the curve obtained when a 20% decline of FEV1 was used as a reference.
Although the diagnosis of chronic allograft rejection in lung transplant recipients is primarily based on spirometric and histologic findings, investigators in several recent studies have proposed complementary diagnostic tools that could contribute to the early detection of this complication. These tools include increased specific airway resistance (26), bronchodilator response at low lung volumes (27), bronchial hyperreactivity (28), increased levels of neutrophils and interleukin-8 in bronchoalveolar lavage fluid (29,30), increased levels of exhaled nitric oxide (31), and alterations in ventilation distribution in the lung periphery (32). Our findings suggest that, alone or in combination with complementary diagnostic parameters, air trapping in excess of 32% of the parenchyma should be considered as suggestive of bronchiolitis obliterans, even if the spirometric criteria for the diagnosis of BOS are not met. If this can be substantiated by the results of larger prospective studies, expiratory CT could become a powerful screening modality for BOS.
In conclusion, our study findings enhance the role of expiratory CT in the evaluation and follow-up of lung transplant recipients. The extent of air trapping is strongly associated with the degree of decline of FEV1, as determined by using the BOS grades. The threshold of 32% of air trapping will help to distinguish between patients who do and those who do not have BOS. When this threshold is used, air trapping analysis is a sensitive, specific, and accurate method for diagnosing BOS.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, A.A.B., M.E., P.A.G.; study concepts, A.A.B., M.E., P.A.G.; study design, all authors; definition of intellectual content, all authors; literature research, all authors; clinical studies, A.V.M., C.K., P.A.G.; data acquisition, A.V.M., C.K., P.A.G.; data analysis, all authors; statistical analysis, A.V.M.; manuscript preparation, A.A.B.; manuscript editing and review, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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= individual air trapping scores obtained at 111 expiratory CT examinations. Vertical bars = median scores with their 25% and 75% quartiles, dashed line = 32% threshold of air trapping, as determined by performing ROC analysis to distinguish between patients who did and those who did not have BOS.
= sustained 25% decline of FEF25-75, 
= sustained 12% decline of FEV1. The intersection of the curve with the second bisectrix, at which sensitivity equals specificity, was used to determine the optimal threshold to distinguish between patients who did and those who did not have BOS.
