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(Radiology. 2000;216:768-772.)
© RSNA, 2000


Thoracic Imaging

Evaluation of Air Trapping at CT: Comparison of Continuous- versus Suspended-Expiration CT Techniques1

Olivier Lucidarme, MD, Philippe A. Grenier, MD, Medhi Cadi, MD, Isabelle Mourey-Gerosa, MD, Karim Benali, MD and Philippe Cluzel, MD

1 From the Department of Radiology, Université Pierre-et-Marie-Curie, Hôpital de la Pitié-Salpêtrière, 47 boulevard de l’Hôpital, 75651 Paris cedex 13, France (O.L., P.A.G., M.C., I.M.G., P.C.); Institut National de la Santé et de la Recherche Médicale, Paris, France (P.A.G.); and Cyclotron Biomedical de Caen, Caen, France (K.B.). From the 1997 RSNA scientific assembly. Received March 29, 1999; revision requested May 10; final revision received January 7, 2000; accepted January 12. Address correspondence to O.L. (e-mail: olivier.lucidarme@psl.ap_hop_paris.fr).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To compare thin-section computed tomographic (CT) scans obtained during suspended end expiration with helical CT scans obtained during continuous expiration for the assessment of air trapping.

MATERIALS AND METHODS: Forty-nine patients with an airway disease were examined with suspended-end-expiration CT after a 6–8-second expiratory maneuver, which was followed with continuous-expiration CT during a 10-second expiratory maneuver. The extent of expiratory air-trapping areas was calculated by two observers by using a semiquantitative grid score. The relative decrease in attenuation in the areas of air trapping was evaluated with a visual continuous-scale score.

RESULTS: Air trapping was noted in 36 and 35 patients with continuous-expiration CT and with suspended-end-inspiration CT, respectively. The extents of and relative attenuation decreases in air-trapping areas in patients with air-trapping areas on at least one expiratory CT scan increased significantly in scans obtained with continuous-expiration CT compared with those obtained with suspended-end-expiration CT, respectively, with mean extent scores of 0.24 ± 0.20 (SD) and 0.18 ± 0.20 (paired t test, P = .001) respectively, and with mean relative contrast decrease scores of 0.35 ± 0.23 and 0.27 ± 0.23 (paired t test, P = .007), respectively.

CONCLUSION: When suspended-end-expiration CT images are ambiguous, complementary continuous-expiration CT can be used to improve the conspicuity and apparent extent of air trapping.

Index terms: Lung, abnormalities, 60.26, 60.751, 60.754, 60.755 • Lung, CT, 60.12111, 60.12115, 60.12118 • Lung, function • Lung, ventilation


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Expiratory computed tomographic (CT) techniques as an adjunct to inspiratory imaging techniques are particularly useful for the assessment of obstructive lung disease and for providing physiologic information concerning regional lung function. It is normal for lung attenuation to increase during expiration, while the cross-sectional lung area decreases (1). In contrast, when air trapping is present, lung attenuation fails to increase, while cross-sectional lung area fails to decrease (2,3).

Thin-section CT during suspended end expiration is the most widely used technique to visualize expiratory air trapping. This technique has been used to demonstrate air trapping in patients with emphysema (4), asthma (5,6), bronchiectasis (7), hypersensitivity pneumonitis (8,9), sarcoidosis (10), or Langerhans cell histiocytosis (11) and in asymptomatic patients who smoke (12). Furthermore, in a recent study, Arakawa et al (13) showed that the use of suspended-end-expiration scanning significantly improved diagnostic accuracy in patients with inhomogeneous areas of attenuation on inspiratory scans. CT during continuous expiration (1,2), which can be used to collect data at a fixed level during expiration, is the second technique available. Electron-beam CT initially was performed, with a scanning time of 100 msec per image, to assess the dynamic changes in lung attenuation and in architecture during expiration, with minimal motion artifacts. This technique has been used to demonstrate air trapping in patients with constrictive bronchiolitis (2) and in healthy men (1).

More recently, a dynamic expiratory maneuver performed during helical CT was described in a small number of patients, with good results in spite of a longer scanning time per image (14,15). To the best of our knowledge, no comparison between continuous-expiration CT and suspended-end-expiration CT to assess air trapping has been reported in the literature. The purpose of this study was to evaluate the reliability of continuous-expiration CT performed with a helical scanner and to compare it with that of suspended-end-expiration CT for the assessment of air trapping.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
We retrospectively studied the chest CT scans of 49 patients (27 men, 22 women; mean age, 51 years; age range, 18–78 years) who had an airway disease (clinical history of asthma [n = 6], who had a clinical history of chronic bronchitis with recurrent or persistent sputum production on most days for at least 3 months of the year for at least 2 successive years [n = 31], or who were clinically suspected to have bronchiectasis [n = 12]) who were referred to the Department of Radiology of the Pitié Salpêtrière Hospital between November 1994 and November 1996. Thirty-five patients were included in a previous study (3) in which suspended-end-expiration CT data were correlated with pulmonary function test results. The means and ranges of pulmonary function test results, expressed as percentages of values predicted from the patient’s age, sex, and height, were residual volume, 103% (58%–153%); forced expiratory volume in 1 second, 70% (28%–118%); vital capacity, 83% (50%–131%); their ratio (forced expiration volume in 1 second to vital capacity), 80% (45%–107%); and forced midexpiratory flow rate (25%–75%), 43% (4%–88%). The remaining 14 patients included in the present study did not undergo pulmonary function testing.

CT Scanning
All CT scans were obtained with a Tomoscan SR 7000 scanner (Philips, Eindhoven, the Netherlands), with a scanning time of 1 second. First, full-inspiration thin-section CT was performed by using 1.5-mm collimation every 10 mm from the lung apex to the diaphragm. Then, during the same session, two expiratory thin-section CT examinations were performed successively. The first included five, six, or seven sections of 1.5-mm collimation obtained every 30 or 40 mm at the end of expiration, from the lung apex to the diaphragm (suspended-end-expiration CT).

The second examination was based on a volumetric acquisition during expiration. It was a standard examination at the Pitié Salpêtrière Hospital between November 1994 and November 1996 for evaluation of the change in the total cross-sectional lung area by using a cine loop. It consisted of a 15-mm-thick lung volume obtained above the bronchus intermedius that was acquired with 1.5-mm collimation and with a pitch of 1 in a caudocranial direction. A 180° linear interpolation reconstruction algorithm was used. Ten sections were obtained during a 10-second period as the patient performed an expiratory maneuver (continuous-expiration CT).

The breath-hold technique at full expiration and during the expiratory maneuver was rehearsed with each patient before the CT examination. For the first examination, the patients were instructed to exhale for 6–8 seconds to reach the residual volume and then to stop breathing. For the second examination, the patients were instructed to exhale completely for 6–8 seconds to reach the residual volume and then to continue their expiratory efforts until the end of the acquisition. The operator controlled these maneuvers visually during the procedure. All lung images were reconstructed and were laser printed with a high-frequency reconstruction algorithm. Window settings appropriate for the assessment of the bronchi and the lung parenchyma (level, -600 HU; width, 1,600 HU) and of the mediastinum (level, 30–50 HU; width, 300–450 HU) were used. No contrast medium was used.

Interpretation of CT Scans
For each patient, the 10 images obtained during the expiratory maneuver and the one image obtained at a comparable level with suspended-end-expiration CT were interpreted independently and in a random order by two radiologists (O.L., I.M.G.) who were not blinded to the type of expiratory scan (the 49 patients in the study were selected from among 59 patients because the two expiratory scans were obtained at the same level). They compared them with the corresponding full-inspiration image. The observers interpreted the images twice. The first reading was performed independently by the two observers to evaluate the presence, extent, and relative contrast of areas of air trapping compared with the surrounding lung parenchyma, whereas the second reading was performed with consensus for motion artifacts and for the presence of air trapping. We defined air trapping as all areas that failed to increase in attenuation after full expiration compared with full inspiration. This definition included areas of decreased attenuation that involved only a few secondary pulmonary lobules, which usually are considered to be physiologic, per lung (1). The spurious appearances of areas of decreased attenuation (rarefied zones in the vicinity of the minor fissure or the relatively low-attenuating apical segments of the lower lobes [1]) that were caused by beam hardening due to the effect of adjacent ribs all were disregarded.

The relative contrast, which represents the attenuation difference between the areas of air trapping and the surrounding lung parenchyma, was assessed semiquantitatively with a visual score by using a continuous 50-mm scale. The zero point represented the absence of areas of decreased attenuation; the 50-mm point corresponded to a theoretic maximum contrast between the area of decreased attenuation, which would produce no attenuation (black on the image), and the surrounding lung parenchyma, which would produce complete attenuation (white on the image). The sequence of 10 images obtained with continuous-expiration CT was accorded an overall score. When different scores coexisted on the same or successive images, only the highest value was retained. A relative contrast score was calculated by measuring the distance between the zero point and the point reported by each observer, which then was divided by the length of the scale. A mean relative contrast score was calculated by averaging the two observers’ scores.

The cross-sectional areas of air trapping were assessed semiquantitatively on the expiratory scans by superimposing a grid of 2 x 2-mm squares that corresponded to 0.3–0.7 cm2 on the CT image (according to the field of view used for image reconstruction) (3,16). The number of squares that contained an area of air trapping was counted, as was the number of squares that overlaid the parenchyma of both lungs. Furthermore, an air-trapping extent score was calculated by determining the ratio of the total number of squares that contained an area of decreased attenuation to the total number of squares that overlaid the lung parenchyma. Only the image in the series of 10 sequential continuous-expiration CT images for which the relative contrast score was considered to be at a maximum was retained to establish the continuous-expiration CT score. A mean air-trapping extent score was calculated by averaging the results from the two observers.

The change in the total cross-sectional lung area between the inspiration section and each corresponding expiration section (degree of expiration) also was calculated independently by each radiologist by using DE = 1 - (Ne/Ni), where DE represents degree of expiration, Ne represents the number of squares that overlaid the lung parenchyma on the expiration image (as above, only the continued-expiration CT image for which the relative contrast score was considered to be at a maximum was counted), and Ni represents the number of squares that overlaid the lung parenchyma during full inspiration. A mean degree of expiration was calculated by averaging the two observers’ results.

Statistical Analyses
Results were expressed as means (± SD) or as percentages. To assess the interobserver variability of the nominal CT findings (the presence or absence of air trapping), the {kappa} coefficient of agreement was computed (17,18). Its significance was interpreted according to its z score value. Furthermore, {kappa} values were interpreted subjectively, as recommended by Altman (19) ({kappa} < 0.20, poor; {kappa} = 0.21–0.40, fair; {kappa} = 0.41–0.60, moderate; {kappa} = 0.61–0.80, good; {kappa} = 0.81–1, very good).

Interobserver agreements on the quantitative parameters (air-trapping extent score, relative contrast score, degree of expiration) were assessed for the patients considered by both observers to have decreased-attenuation areas to minimize the underestimation that resulted from interobserver disagreement for the presence or absence of air trapping. This was done by using the intraclass correlation coefficient of agreement (ri) (16,20). Values obtained were interpreted as follows: 0.30 as poor; 0.31–0.50, low; 0.51–0.70, moderate; 0.71–0.90, good; and 0.91–1, very good interobserver agreement (20).

A paired t test was performed to compare the intersubject quantitative CT parameters of both CT scans. When the difference between the CT parameters had a very skewed distribution and the intergroup differences in variability were significant, the nonparametric paired Wilcoxon test was performed to compare continuous-expiration and suspended-end-expiration CT scores. The {chi}2 test with continuity correction or the Fisher exact test was used, as appropriate, to compare percentages. All P values were two-tailed and, when less than .05, were considered to indicate a significant difference.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Areas of air trapping were noted at the consensual reading in 36 patients by using continuous-expiration CT and in 35 patients by using suspended-end-expiration CT. Four patients’ findings were positive on only continuous-expiration CT images, and three patients’ findings were positive on only suspended-end-expiration CT images. The first observer noted air trapping in 34 patients with continuous-expiration CT and in 30 patients with suspended-end-expiration CT, while the second observer noted air trapping in 36 patients with continuous-expiration CT and in 31 with suspended-end-expiration CT. The interobserver agreements for continuous-expiration CT and suspended-end-expiration CT were 91% ({kappa} = 0.81, P < .001) and 85% ({kappa} = 0.71, P < .001), respectively.

The 10th continuous-expiration CT image always was selected by each observer to quantify the air-trapping score and the degree of expiration. Good interobserver agreements were obtained for the degrees of expiration, with ri values of 0.82 for both techniques. The interobserver agreements were moderate for the extent of air trapping (continuous-expiration CT and suspended-end-expiration CT ri values of 0.61 and 0.69, respectively) and for the assessment of the relative contrast of air-trapping areas (continuous-expiration and suspended-end-expiration CT ri values of 0.64 and 0.62, respectively).

For the 39 (80%) of 49 patients with areas of air trapping on at least one expiratory CT scan at the consensual reading, the air-trapping extent and the relative contrast scores obtained with continuous-expiration CT were significantly higher than those obtained with suspended-end-expiration CT. The mean extent scores were 0.24 ± 0.20 and 0.18 ± 0.20 (paired t test, P = .001), and mean relative contrast scores were 0.35 ± 0.23 and 0.27 ± 0.23 (paired t test, P = .007) for continuous-expiration CT and suspended-end-expiration CT, respectively. The degrees of expiration obtained with continuous-expiration CT did not differ significantly from those obtained with suspended-end-expiration CT (paired t test, P = .07), with respective mean values of 0.25 ± 0.09 and 0.21 ± 0.10.

For the subgroup (25 [64%] of 39) of patients with higher mean air trapping extent scores obtained with continuous-expiration CT, the degree of expiration was increased significantly by, on average, 0.07 ± 0.05 with continuous-expiration CT compared with suspended-end-expiration CT (paired t test, P = .01) (Figure). Likewise, for the 28 (72%) patients with higher mean relative contrast scores obtained with continuous-expiration CT, the degree of expiration was increased significantly by, on average, 0.07 ± 0.06 (paired t test, P = .02) (Figure). For the 14 (36%) patients with lower mean air-trapping extents and for the 11 (28%) patients with lower mean relative contrast scores obtained with continuous-expiration CT, the degrees of expiration did not differ significantly between continuous-expiration CT and suspended-end-expiration CT (paired t test, P = .13).



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Figure a. (a) Full-inspiration thin-section transverse CT scan in the lower lobes of the lungs in a 37-year-old man suspected to have bronchiectasis shows atelectasia (star) in the right middle lobe. (b) Suspended-end-expiration thin-section transverse CT scan obtained at the same level as a. The mean degree of expiration was 0.19 ± 0.02. Air trapping (stars) was considered to be present by both observers, with a mean air-trapping-extent score of 0.15 ± 0.04 and with a mean relative contrast score of 0.34 ± 0.05. (c) The last transverse thin section, obtained at the same level as a during the active expiratory maneuver, shows a higher degree of expiration (0.25 ± 0.03). The extent and the relative contrast of air trapping (stars) also were higher (0.55 ± 0.07 and 0.62 ± 0.09, respectively).

 


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Figure b. (a) Full-inspiration thin-section transverse CT scan in the lower lobes of the lungs in a 37-year-old man suspected to have bronchiectasis shows atelectasia (star) in the right middle lobe. (b) Suspended-end-expiration thin-section transverse CT scan obtained at the same level as a. The mean degree of expiration was 0.19 ± 0.02. Air trapping (stars) was considered to be present by both observers, with a mean air-trapping-extent score of 0.15 ± 0.04 and with a mean relative contrast score of 0.34 ± 0.05. (c) The last transverse thin section, obtained at the same level as a during the active expiratory maneuver, shows a higher degree of expiration (0.25 ± 0.03). The extent and the relative contrast of air trapping (stars) also were higher (0.55 ± 0.07 and 0.62 ± 0.09, respectively).

 


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Figure c. (a) Full-inspiration thin-section transverse CT scan in the lower lobes of the lungs in a 37-year-old man suspected to have bronchiectasis shows atelectasia (star) in the right middle lobe. (b) Suspended-end-expiration thin-section transverse CT scan obtained at the same level as a. The mean degree of expiration was 0.19 ± 0.02. Air trapping (stars) was considered to be present by both observers, with a mean air-trapping-extent score of 0.15 ± 0.04 and with a mean relative contrast score of 0.34 ± 0.05. (c) The last transverse thin section, obtained at the same level as a during the active expiratory maneuver, shows a higher degree of expiration (0.25 ± 0.03). The extent and the relative contrast of air trapping (stars) also were higher (0.55 ± 0.07 and 0.62 ± 0.09, respectively).

 
For the remaining 10 (20%) patients, no areas of air trapping were visualized with either CT technique. In these patients, the mean degrees of expiration obtained with continuous-expiration CT did not differ significantly from those obtained with suspended-end-expiration CT, with respective mean values of 0.22 ± 0.15 and 0.21 ± 0.14 (paired t test, P = .39).

Motion-related artifacts were considered to be present on the continuous-expiration and suspended-end-expiration CT scans of 12 (24%) and seven (14%) patients (not significant, P = .31), respectively, but without spoiled scan interpretation.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To the best of our knowledge, continuous-expiration CT with a helical scanner rarely has been described in the literature (14,15), and no comparison between continuous-expiration and suspended-end-expiration CT for the assessment of air trapping has been published. In our study, significant differences for the assessment of air trapping were found between continuous-expiration and suspended-end-expiration CT. The improvement provided by continuous-expiration CT could be explained by a small increase in the degree of expiration, which leads to a better detection of air trapping. Although this increase was not significant when all patients were considered, the degree of expiration was significantly higher with continuous-expiration CT when only patients who manifested more marked air trapping at continuous-expiration CT were considered. Patients could have greater difficulty maintaining the residual volume after an exhalation than during an active exhalation when they have to continue the expiratory effort until the end of the acquisition. Furthermore, since no attempt was made to mechanically control the volume and rate of the exhalation during expiratory CT and because the continued-expiration CT images selected by the two observers always were obtained approximately 2 seconds after the suspended-end-expiration CT images, patients could have reached full residual volume on only continued-expiration CT images. In addition, the analysis of the complete set of continued-expiration CT images allows the selection of the section in which air trapping is at a maximum. Since, in our study, the 10th image always was selected as showing the best air trapping, we consider that the number of images could be reduced to decrease radiation exposure. Nevertheless, we think that 4 or 5 seconds of scanning around the late phase of expiration remains necessary to obtain a 180° linear interpolation reconstruction that reduces artifacts due to movement. Furthermore, having more than one or two images could ensure the selection of the best image of air trapping if the patient were unable to continue expiration and started inspiration before the end of the acquisition.

Motion artifacts, which increase as temporal resolution decreases, represent the major limitation of continued-expiration CT. In our study, minor motion-related degradation of images acquired during active expiration but without spoiled scan interpretation was visible for 12 (24%) of the 49 cases, which was not significantly different from that acquired during suspended-end-expiration CT. This result could be explained by the use of a 180° linear interpolation algorithm with a 1-second rotation time, which represents a scanning period of about 500 msec, to reconstruct individual active expiratory scans. Furthermore, since the acquisition was made in a caudocranial direction during expiration to compensate for the rising diaphragm and the cephalad movement of the lungs, motion artifacts were minimized. Finally, motion artifacts were at a maximum during the early phase of expiration and were at a minimum during its late phase, which thereby allowed good visualization of lobular air trapping with helical CT.

Three potential limitations of our study were the subjective quantification of the intensity of air trapping by using the relative contrast score, the order of implementation of each expiratory technique, and the lack of blinding of the observers to the type of expiratory scan being read. Because it was a retrospective study, we could not use regions of interest to quantify the relative contrast between the areas of air trapping and the surrounding lung parenchyma. However, in standard clinical examinations, only subjective analysis is performed routinely (13). Since suspended-end-expiration CT always was performed before continued-expiration CT, a training bias might explain the higher degree of expiration with continued-expiration CT. On the other hand, since the residual volume was maintained passively at suspended-end-expiration CT and actively at continued-expiration CT, the two expiratory techniques were sufficiently different at the late phase of expiration that performance of the first technique did not really ensure the greater success of the second. Finally, since the two observers were not blinded to the type of expiratory scan, they might have been biased subconsciously toward the more experimental continued-expiration CT technique. However, this bias should have been marginal, as scans obtained with both expiratory techniques were interpreted independently.

In conclusion, when suspended-end-expiration CT images are ambiguous or when patients have difficulty performing the suspended-end-expiration maneuver adequately, complementary continued-expiration CT can be performed with a helical scanner to improve the conspicuity and the apparent extent of air trapping at a given anatomic level.


    FOOTNOTES
 
Author contributions: Guarantors of integrity of entire study, O.L., P.A.G.; study concepts, O.L., P.A.G., P.C.; study design, O.L., P.A.G.; definition of intellectual content, O.L., P.A.G.; literature research, O.L.; clinical studies, O.L., M.C.; data acquisition, M.C., I.M.G.; data analysis, O.L.; statistical analysis, K.B.; manuscript preparation and editing, O.L.; manuscript review, P.A.G., P.C.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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