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DOI: 10.1148/radiol.2293020827
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(Radiology 2003;229:737-742.)
© RSNA, 2003

Thoracic Imaging

Air Trapping in Heart-Lung Transplant Recipients: Variability of Anatomic Distribution and Extent at Sequential Expiratory Thin-Section CT1

Alexander A. Bankier, MD, Alain Van Muylem, PhD, Pietro Scillia, MD, Viviane De Maertelaer, PhD, Marc Estenne, MD and Pierre Alain Gevenois, MD

1 From the Department of Radiology, University of Vienna, Waehringer Guertel 18–20, A-1090 Vienna, Austria (A.A.B.); and Departments of Chest Medicine (A.V.M., M.E.) and Radiology (P.S., P.A.G.) and Statistical Unit, Institute of Interdisciplinary Research in Human and Molecular Biology (V.D.M.), University of Brussels, Belgium. Received July 10, 2002; revision requested August 29; final revision received March 18, 2003; accepted April 2. Address correspondence to A.A.B. (e-mail: alexander.bankier@univie.ac.at).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the intrapatient reproducibility of the extent and anatomic distribution of air trapping at sequential expiratory thin-section computed tomographic (CT) examinations in heart-lung transplant recipients.

MATERIALS AND METHODS: Nineteen heart-lung transplant recipients (eight with and 11 without bronchiolitis obliterans syndrome [BOS]) underwent three expiratory CT examinations within 1 hour. Residual volumes were measured at CT. Anatomic distribution and extent of air trapping were scored by two observers at two independent readings, and the reproducibility of observations was calculated for each feature. CT examination results were compared by using an analysis of variance that took into account interobserver and BOS and non-BOS effects. The Spearman rank correlation coefficient was calculated to test the association between variability of residual volumes and variability of the extent of air trapping.

RESULTS: Residual volumes did not significantly differ between the three CT examinations (P = .556). Reproducibility values for findings of anatomic distribution of air trapping ranged from 84% to 95%, with a tendency toward improved reproducibility in patients without BOS. Mean reproducibility values for the extent of air trapping ranged from 97.1% to 97.7%, and no substantial difference in these values between patients with and those without BOS was observed. The Spearman rank coefficient for the correlation between variability of residual volumes and variability of extent of air trapping ranged from 0.382 to 0.568 (P = .105–.016). No interobserver effect was detected (P = .944).

CONCLUSION: Anatomic distribution and extent are reproducible characteristics of air trapping. No substantial variability of air trapping occurs in functionally stable heart-lung transplant recipients.

© RSNA, 2003

Index terms: Bronchiolitis obliterans, 60.2191 • Heart, transplantation, 51.459 • Lung, air trapping • Lung, CT, 60.12118 • Lung, transplantation, 60.459


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
At expiratory thin-section computed tomographic (CT) examinations of heart-lung transplant recipients, air trapping is a sensitive, specific, and accurate sign for diagnosing bronchiolitis obliterans syndrome (BOS) (1–3). The BOS grading system enables physicians to functionally grade the airflow limitation caused by obliterative bronchiolitis and is the current standard of reference for the clinical assessment of chronic lung allograft rejection (4–6). As shown in previous studies, the severity of BOS is strongly associated with the extent of air trapping seen at expiratory CT (2,3). Moreover, the occurrence of air trapping can precede the airflow limitation characteristic of BOS and may, accordingly, contribute to the early detection of subclinical chronic allograft rejection (3).

The diagnosis of chronic allograft rejection in heart-lung transplant recipients relies on the intrapatient evolution of predefined test parameters observed at sequential examinations (6–13). Accurate interpretation of sequential examination results, however, requires knowledge about the variability of the test parameter being investigated (14). The variability of air trapping at sequential expiratory CT examinations is not known. It therefore remains difficult to determine whether changes in air trapping at sequential CT examinations result from an inherent variability of air trapping or from the variability of the underlying BOS. Because this problem currently weakens the clinical impact of CT examinations in patients suspected of having BOS, the aim of our study was to evaluate the intrapatient reproducibility of the extent and anatomic distribution of air trapping at sequential expiratory thin-section CT examinations in heart-lung transplant recipients.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Between March 1998 and July 2001, we prospectively and consecutively evaluated 19 heart-lung transplant recipients at the occasion of their yearly routine follow-up examination. All patients were in clinically and functionally stable condition at the time of this study, and no patient had acute infection, acute allograft rejection, or asthma. Seven of the patients were women, and 12 were men. Their mean age was 42 years ± 11 (SD) (range, 19–55 years). The mean time since heart-lung transplantation was 53 months ± 32 (range, 7–122 months). When our study was performed, the policy of the Ethics Committee at the University of Brussels was that it was the responsibility of the investigators involved in the study to determine whether or not Ethics Committee review and approval were needed. The Ethics Committee did not require submission of our study protocol, but we did obtain written informed consent from each patient after explaining the study rationale, procedures, and potential risks. Since our Ethics Committee currently does require submission of study protocols, including forms for written informed consent, both were submitted for our study. The Ethics Committee approved our study after careful consideration of the study protocol and potential benefits for the patients and in view of the information given to patients before obtaining written informed consent.

Pulmonary Function Testing
Pulmonary function testing was performed within 2 days of the CT examinations. Measurements of functional residual capacity, total lung capacity, and residual volume were obtained with the patient seated in a constant-volume body plethysmograph (Body Test; Jaeger, Wuerzburg, Germany). Measurements of forced vital capacity and forced expiratory volume in 1 second (FEV1) were obtained by using a spirometer (Sensormedics 2400; Sensormedics, Anaheim, Calif) according to the guidelines of the American Thoracic Society (15). Predicted values for static and dynamic lung volumes were derived from the literature (15,16).

The severity of BOS was graded according to the recommendations of the International Society for Heart and Lung Transplantation (4). Accordingly, a BOS score of 0 indicated an FEV1 of more than 80% of the best postoperative value (and therefore indicated that BOS was not present); a BOS score of 1, a sustained decline in FEV1 to between 80% and 66% of the best postoperative value; a BOS score of 2, a sustained decline in FEV1 to between 65% and 50% of the best postoperative value; and a BOS score of 3, a sustained decline in FEV1 of below 50% of the best postoperative value. At the time our study was performed, 11 (58%) of 19 patients had a BOS score of 0; six (32%), a BOS score of 1; and two (11%), a BOS score of 2. In three of the eight patients with BOS, transbronchial biopsy results had confirmed the presence of bronchiolitis obliterans.

CT Examinations
Before the CT examinations, breath holding at fully suspended inspiration and at fully suspended expiration was rehearsed with each patient. Then, each patient underwent three expiratory CT examinations. The first of these three expiratory CT examinations (CT1) was performed as part of yearly follow-up CT for heart-lung transplant recipients, which at our institution is routinely performed in both fully suspended inspiration and fully suspended expiration. The second expiratory CT examination (CT2) was performed 5 minutes after CT1 was completed. Between CT1 and CT2, patients remained positioned within the scanner. The third expiratory CT examination (CT3) was performed 60 minutes after CT1 was completed. Between CT2 and CT3, the patients left the scanner unit, returned, and were then repositioned, and a new scout view was obtained before data acquisition. For each of the three CT examinations, and in each patient, the first CT section was systematically positioned at the level of the lung apices shown on the scout view.

All CT images were obtained with a commercially available scanner (Somatom Plus 4C; Siemens Medical Systems, Erlangen, Germany). All patients were examined in the supine position, and none received contrast material. The acquisition time was 1 second per section, and the tube current was 140 kV at 171 mA. Section thickness was 1 mm. The intersection interval was 10 mm for 17 of the 19 patients. Two patients had difficulty holding their breath during fully suspended expiration. Therefore, the intersection interval was increased to 20 mm. 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. Images were photographed with 12 images per sheet of 35.5 x 43.0-cm film.

At all expiratory CT examinations, the residual volume was determined. This was achieved by using a software package (Pulmo CT; Siemens Medical Systems) that automatically delineates lung contours on CT images and measures the lung area. Residual volumes were then calculated by one observer (P.S.) on the basis of the values of lung areas and section intervals.

Image Analysis
Two radiologists (A.A.B., P.A.G.), each with 7 years of experience in chest imaging, analyzed the CT images. Image reading was performed in independent sessions. During each session, all images were read. The expiratory CT images were considered to reveal air trapping when lung regions did not demonstrate an increase in attenuation and/or did not show a decrease in volume with regard to their appearance on the initial inspiratory images (17,18). Because our study focused exclusively on air trapping, CT images obtained at fully suspended inspiration were used only for comparison with the corresponding CT images obtained at fully suspended expiration. Bronchial and vascular abnormalities were not recorded. However, bronchial and vascular abnormalities were used to differentiate between potentially confounding features of air trapping and mosaic attenuation caused by vascular diseases (19).

Anatomic distribution of air trapping.—The anatomic distribution of air trapping was determined on the basis of the lobular anatomy of the lung at thin-section CT (20,21). Comparisons were performed between pairs of corresponding CT sections from CT1, CT2, and CT3. According to the results of these section-by-section comparisons, corresponding pairs of CT examination results were assigned to one of the four categories illustrated in Figure 1 and defined as follows: Category 1 indicated that there was either no air trapping at both CT examinations or there was air trapping in identical secondary pulmonary lobules at both CT examinations; category 2, that there was air trapping in identical secondary pulmonary lobules at both CT examinations and additional secondary lobules showed newly appeared air trapping at the second CT examination; category 3, that previously evident air trapping was no longer visible at the second CT examination and no air trapping had newly appeared; and category 4, that previously evident air trapping was no longer visible at the second CT examination and secondary lobules other than those observed at the first CT examination showed newly appeared air trapping. Air trapping was considered newly appeared as soon as it was detected in one secondary pulmonary lobule on one pair of corresponding CT sections in a given examination.



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  		Figure 1. Scoring the anatomic distribution of air trapping. For assessing the reproducibility of the anatomic distribution of air trapping, a corresponding pair of transverse CT examination results was assigned to one of the four categories illustrated. Assignment was based on section-by-section comparison, and air trapping was considered as newly appeared as soon as it was detected in one secondary pulmonary lobule on one pair of corresponding CT sections in an examination. Dark octagons represent air trapping. H = heart, S = spine. Category 1 indicates that there is no air trapping at both CT examinations or there is air trapping in identical secondary pulmonary lobules at both CT examinations; category 2, that there is air trapping in identical secondary pulmonary lobules at both CT examinations and additional secondary lobules show newly appeared air trapping at the second CT examination; category 3, that previously evident air trapping is no longer visible at the second CT examination and no air trapping has newly appeared; and category 4, that previously evident air trapping is no longer visible at the second CT examination and secondary lobules other than those observed at the first CT examination show newly appeared air trapping.

 
Extent of air trapping.—The scoring system used to assess the extent of air trapping was adapted from previous work (2,22,23) and slightly modified 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, a score of 1 was assigned if less than 20% of the parenchyma in a CT section showed air trapping, a score of 2 was assigned if 20%–39% of the parenchyma showed air trapping, a score of 3 was assigned if 40%–59% of the parenchyma showed air trapping, a score of 4 was assigned if 60%–79% of the parenchyma showed air trapping, and a score of 5 was assigned if 80% or more of the parenchyma showed air trapping. To obtain the average air trapping score for a given CT examination, the scores for all sections from one patient were added and then divided by the number of sections acquired in this patient. The resulting score was expressed as a percentage of the maximum possible score—that is, the score that theoretically would be obtained if all sections in a patient were given a score of 5.

Statistical Analysis
All statistical analyses were performed with a personal computer by using commercially available software packages (Statistica version 5.0, StatSoft, Tulsa, Okla; and SPSS version 10.0, SPSS, Chicago, Ill). Normally distributed data were expressed as means ± 1 SD, and skewed data were expressed as medians with 25% and 75% quartiles. The normality of the distribution of the data was evaluated by using the Kolmogorov-Smirnov test (with SPSS version 10.0). Proportions were expressed as percentages with their 95% CIs. On the basis of the individual residual volumes measured at each of the three CT examinations performed in every patient, the mean residual volumes at CT1, CT2, and CT3 were calculated. Potential differences between these mean residual volumes were evaluated by using an analysis of variance for repeated measurements. For all statistical tests, P <= .05 was considered to indicate a significant difference.

For the assessment of both the anatomic distribution and the extent of air trapping, interobserver agreement was determined by using a {kappa} statistic (24). The 95% CIs for the {kappa} statistics were calculated. All {kappa} values were interpreted as recommended in the literature (24,25) as follows: A {kappa} value of 0.20 or less indicated poor agreement; a {kappa} value of 0.21–0.40, fair agreement; a {kappa} value of 0.41–0.60, moderate agreement; a {kappa} value of 0.61–0.80, good agreement; and a {kappa} value of 0.81–1.00, excellent agreement.

Anatomic distribution of air trapping.—The anatomic distribution of air trapping was considered as reproducible only if comparison between a given pair of CT examination results had resulted in an assignment to category 1 (no air trapping at both CT examinations, or air trapping in identical secondary pulmonary lobules at both CT examinations). Reproducibility of the anatomic distribution of air trapping was expressed as a percentage and was defined as the number of CT examinations assigned to category 1 divided by the total number of CT examinations whose results were assessed by both readers. The reproducibility of the anatomic distribution of air trapping was determined for the three possible comparisons among CT1, CT2, and CT3, with respect to the entire study group, and with respect to the subgroups of patients with BOS and patients without BOS.

Extent of air trapping.—To search for differences in the extent of air trapping at CT1, CT2, and CT3, we performed a global analysis taking into account (a) whether the patients did or did not have BOS, (b) results of the three sequential CT examinations CT1, CT2, and CT3, (c) the interobserver effect, and (d) all first-order interactions between these three factors. The mean extent of air trapping was subjected to an analysis of variance with one repeated factor at three levels (ie, CT1, CT2, and CT3), a between-observers (ie, the two observers) factor, and a between-groups (ie, the group of patients with BOS and the group of patients without BOS) factor.

To determine the variability of the extent of air trapping between two given CT examinations, the difference between the average air trapping scores of these two CT examinations was calculated. The absolute value of this difference was then subtracted from 100. The resulting number thus expressed the percentage of air trapping exempt from variation between the two CT examinations being compared. This percentage was defined as the reproducibility of the extent of air trapping. The reproducibility of the extent of air trapping was determined for the three possible comparisons among CT1, CT2, and CT3, with respect to the entire study group, and with respect to the subgroups of patients with BOS and patients without BOS.

To quantify the strength of the relationship between the variability of residual volume and the variability of the extent of air trapping, we calculated the Spearman rank correlation coefficient between these two variables for the comparisons of CT1 and CT2, CT1 and CT3, and CT2 and CT3.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
The 57 expiratory CT examinations (three examinations in 19 patients) performed in our study yielded a total of 921 individual CT sections (ie, three examinations times 307 sections). The mean number of CT sections acquired per patient was 15 ± 3 (range, 7–19). The mean residual volume measured at the CT examinations was 1,809 mL ± 505 at CT1, 1,815 mL ± 522 at CT2, and 1,825 mL ± 502 at CT3; no statistically significant differences were found between these values (P = .792). The extent of air trapping seen at the CT examinations of both the entire study group and the subgroups of patients with BOS and patients without BOS is shown in Table 1.


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  		TABLE 1. Extent of Air Trapping in Different Patient Groups

 
Anatomic Distribution of Air Trapping
Reproducibility of the anatomic distribution of air trapping ranged from 84% to 95% for the entire study group (Fig 2). Detailed reproducibility values for the entire study group and for the subgroups of patients with BOS and patients without BOS are listed in Table 2. The overlap between the 95% CIs for patients with BOS and the 95% CIs for patients without BOS indicates that there was no statistically significant difference in reproducibility of the anatomic distribution of air trapping between these two subgroups. Table 2 also provides the {kappa} values. They corresponded to either good or excellent interobserver agreement.



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  		Figure 2. Anatomic distribution and extent of air trapping. Transverse expiratory CT sections obtained at the level of the right lower lobe of a heart-lung transplant recipient with BOS at, A, the first CT examination, B, the second CT examination, and, C, the third CT examination show that both anatomic distribution and extent of air trapping (visible as areas of low attenuation) are reproducible between examinations.

 

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  		TABLE 2. Reproducibility of Anatomic Distribution of Air Trapping in Different Patient Groups

 
Extent of Air Trapping
The extent of air trapping was significantly greater in patients with BOS than in patients without BOS (P = .001). The mean extent of air trapping did not significantly differ among CT1, CT2, and CT3 (P = .556). Moreover, there was no statistically significant difference between the assessments of the two readers (P = .952). These three factors (whether or not a patient had BOS; extent of air trapping on CT1, CT2, and CT3; and the interobserver effect) did not interact (P = .617, P = .890, and P = .944).

Mean reproducibility of the extent of air trapping ranged from 97.1% to 97.7% for the entire study group (Fig 2). Detailed reproducibility values for the entire study group and for the subgroups of patients with BOS and patients without BOS are provided in Table 3. The overlap between the 95% CIs for patients with BOS and the 95% CIs for patients without BOS indicates that there was no statistically significant difference in reproducibility of the extent of air trapping between these two subgroups. Table 3 also provides the {kappa} values, which all show that there was excellent interobserver agreement. Reproducibility was therefore expressed as the mean of corresponding values determined by the two readers.


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  		TABLE 3. Reproducibility of Extent of Air Trapping in Different Patient Groups

 
Spearman rank correlation coefficients between variability of residual volume and variability of the extent of air trapping were 0.419 (95% CI: -0.043, 0.733; P = .076) for the comparison of CT1 and CT2, 0.382 (95% CI: -0.086, 0.712; P = .105) for the comparison of CT1 and CT3, and 0.568 (95% CI: 0.153, 0.812; P = .016) for the comparison of CT2 and CT3.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
The results of our study show that the anatomic distribution of air trapping is highly reproducible at expiratory CT examinations in heart-lung transplant recipients. When our patients remained positioned in the CT scanner between two given CT examinations, the reproducibility was 95%. When patients were repositioned, the reproducibility declined to 84% and 87%. This slight decrease could be attributed to a subtle difference in section position and, consequently, to minor anatomic misregistration. A potential effect of misregistration would have been amplified by our decision to consider air trapping as reproducible only if its anatomic distribution was strictly identical on all sections of the two CT examinations whose results were being compared. Any change in a single secondary pulmonary lobule on a single CT section would indeed have shifted the entire pair of CT examination results to a category indicating a lack of reproducibility. Despite this rigorous criterion, lack of reproducibility after repositioning occurred in only three patients. It is not surprising that two of these three patients had BOS, given that air trapping was comparatively more severe in the patients with BOS, and variability in the anatomic distribution of air trapping was therefore more likely to occur in patients with BOS than in patients without BOS. This could also account for the comparatively lower reproducibility of the anatomic distribution of air trapping in the patients with BOS.

With mean reproducibility values for the entire study group ranging from 97.1% to 97.7%, our results also show that the extent of air trapping is highly reproducible. Obviously, patient repositioning had no substantial effect on this parameter. Furthermore, reproducibility of the extent of air trapping in the patients with BOS and in those without BOS was almost identical. This indicates that the amount of air trapping does not affect the reproducibility of its extent. Mild or severe air trapping, on one hand, and the absence of air trapping, on the other hand, should be equally reproducible in functionally stable heart-lung transplant recipients. The mean differences in residual volume among the three groups of expiratory CT examinations performed in this study were not statistically significant, and the absolute differences were surprisingly small. At the same time, the weak correlation coefficients between the variability of residual volumes and the variability of the extent of air trapping revealed a loose association between these two variables. Minor variability of residual volume should thus have little effect on the individual reproducibility of the extent of air trapping at sequential CT examinations in heart-lung transplant recipients. For practical reasons, the core experiments performed in our study took 60 minutes, and potential implications of our findings have to be restricted to this time frame. There is, however, little reason to assume that air trapping could be substantially less reproducible over longer periods of time.

Air trapping in heart-lung transplant recipients is common, given the high prevalence of BOS in this patient population (13,26). We could therefore expect that the expiratory CT examinations performed in our patients would display representative arrays of both extent and anatomic distribution of air trapping. Results of our study confirm those of prior studies in showing that air trapping is more severe in patients with BOS than in patients without BOS (1–3,27). Both patients without BOS and healthy individuals, however, may also show air trapping at expiratory CT (2,28–30). Whereas air trapping in patients with BOS is presumed to result from bronchiolitis obliterans, air trapping in patients without BOS and in healthy individuals must obviously have other origins, which are still not precisely identified. Yet the results of our study showed that the potentially diverse origins of air trapping did not affect the reproducibility of the extent and anatomic distribution of air trapping. Overall, our results indicate that in functionally stable heart-lung transplant recipients, regardless of whether or not they have BOS, air trapping is an anatomically and dimensionally stable CT finding.

In summary, the results of our study show that anatomic distribution and extent are reproducible characteristics of air trapping, suggesting that no substantial variability in air trapping occurs in functionally stable heart-lung transplant recipients. This should increase diagnostic confidence when air trapping is seen at expiratory thin-section CT in these patients.


   FOOTNOTES
 
Abbreviations: BOS = bronchiolitis obliterans syndrome, FEV1 = forced expiratory volume in 1 second

Author contributions: Guarantors of integrity of entire study, all authors; study concepts, A.A.B., A.V.M., M.E., P.A.G.; study design, all authors; literature research, A.A.B., M.E.; clinical studies, A.V.M., P.S., M.E., P.A.G.; data acquisition and analysis/interpretation, all authors; statistical analysis, A.V.M., V.D.M.; manuscript preparation and editing, A.A.B.; manuscript definition of intellectual content, revision/review, and final version approval, all authors


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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Z A Aziz, J C Davies, E W Alton, A U Wells, D M Geddes, and D M Hansell
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P A de Jong, J D Dodd, H O Coxson, C Storness-Bliss, P D Pare, J R Mayo, and R D Levy
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