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Thoracic Imaging |
1 From the Department of Radiology, Yamaguchi University School of Medicine, 1-1-1 Minamikogushi, Ube, Yamaguchi 755-8505, Japan (N.T., T.M., G.M., T.E., N.M., K.U.); and Department of Radiology, University of Colorado Health Science Center, Denver (D.A.L.). From the 2001 RSNA scientific assembly. Received March 25, 2002; revision requested June 10; revision received August 28; accepted October 24. Address correspondence to N.T. (e-mail: ntanaka@yamaguchi-u.ac.jp).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: The study group consisted of 50 subjects with normal pulmonary function, including 26 nonsmokers and 24 smokers (14 current and 10 ex-smokers; 11 mild and 13 heavy smokers). All 50 subjects underwent thin-section CT at which images were obtained during deep inspiration and expiration at three lung levels. The mean expiratory increase in lung attenuation was measured at each level. Air trapping was visually classified into four degrees (none, lobular, mosaic, or extensive), and the extent of air trapping was also semiquantitatively calculated. The visual grade and semiquantitative ratio of air trapping were compared among nonsmokers, current smokers, and ex-smokers and among nonsmokers, mild smokers, and heavy smokers by using the Kruskal-Wallis rank test and the Fisher protected least significant difference test, respectively.
RESULTS: The mean increase in lung attenuation in the three levels at expiration was 111.9 HU ± 46.3 (SD). The overall frequency of air trapping was 64%. Lobular, mosaic, and extensive air trapping were seen in 10 (20%), 14 (28%) and eight (16%) patients, respectively. There was no significant difference in the visual grade of air trapping among the nonsmokers, current smokers, and ex-smokers (P = .387) or among the nonsmokers, mild smokers, and heavy smokers (P = .231). There was also no significant difference in the semiquantitative ratio of air trapping among nonsmokers, current smokers, and ex-smokers (P = .859) or among nonsmokers, mild smokers, and heavy smokers (P = .897).
CONCLUSION: Various degrees of air trapping, including the mosaic or extensive types, can be observed in subjects with normal pulmonary function and have no correlation with the subject’s current smoking status or cigarette consumption.
© RSNA, 2003
Index terms: Emphysema, pulmonary, 60.751 • Lung, air trapping, 60.751 • Lung, CT, 60.12118 • Lung, function
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The purpose of this study was to determine the degree and extent of air trapping at CT in patients with normal pulmonary function test (PFT) results.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All patients had normal values (>70%) for the ratio of forced expiratory volume in 1 second to forced vital capacity (FEV1/FVC) and normal values (>80%) for percent predicted vital capacity according to age and sex. The value of 70% as the limit of FEV1/FVC for normal lung function was based on the guidelines for the diagnosis of chronic obstructive pulmonary disease published by the Japanese Respiratory Society (21). Furthermore, to exclude patients with small-airway disorders, we selected only those with normal percent predicted maximum expiratory flow at 50% of vital capacity (MEF50%) values for their age and sex. We used 60% as the normal lowest level of percent predicted MEF50% because Mastora et al (16) have reported that a percent predicted MEF50% value of less than 60% is one of the indexes of small-airway disorder.
Patients were excluded from this study because of (a) a history of chest surgery; (b) previous pleural or respiratory illness, especially asthma, bronchiolitis, or pneumonia of any origin; (c) obvious exposure to environmental and/or occupational pollutants; (d) respiratory symptoms including chronic cough, sputum, and dyspnea; and/or (e) abnormal findings on inspiratory thin-section CT scans, including evidence of pneumonia, interstitial pneumonia, or pulmonary fibrosis, bronchial wall changes (thickening of the bronchial wall and bronchiectasis), or bronchiolar changes (centrilobular opacities). We also excluded patients who were older than 60 years to avoid the possible inclusion of patients with "aging lung."
Subjects were placed into one of three groups: current smokers (who had smoked regularly for more than 5 years) (n = 14), ex-smokers (who had not smoked for more than 2 years) (n = 10), and nonsmokers (n = 26). Cigarette consumption (in pack-years) was evaluated in current smokers and ex-smokers. Each current smoker or ex-smoker was also placed into one of two groups: mild smokers (less than 20 pack-years) (n = 11) and heavy smokers (more than 20 pack-years) (n = 13). The cohort consisted of 28 men and 22 women with a mean age of 48.0 years (age range, 30–59 years).
CT Scanning
All 50 patients were examined with a Somatom Plus 4 CT scanner (Siemens, Erlangen, Germany). The scanning parameters were as follows: 2-mm collimation, 120 kVp, 180 or 200 mA, and a scanning time of 1.00 or 0.75 second. CT scans were reconstructed with a high-spatial-resolution algorithm (bone-detail algorithm). In each subject, three sequential inspiratory scanning sequences were performed at 5-mm intervals at three levels through the upper lung (at the aortic arch), lower lung (2 cm above the diaphragm), and middle portion of the lung (midpoint between upper and lower lung). After inspiratory scans were obtained during suspended full inspiration at each of the three levels, three sequential scans during suspended full expiration were obtained at 5-mm intervals with 2-mm collimation. The upper level was 15 mm above the inspiratory level, the middle level was 20 mm above the inspiratory level, and the lower level was 30 mm above the inspiratory level. This method was used to obtain comparable images of the lung parenchyma at inspiratory and expiratory scanning (9).
Before expiratory scanning, the following breathing instructions were given to all subjects: "Take a deep breath, blow out hard, and do not breathe in again for 10 seconds." Each patient practiced this protocol several times before scanning was begun. Both inspiratory and expiratory scanning were performed with the patient in the supine position; no contrast medium was used. Among the expiratory scans obtained at each level, one scan on which the depicted anatomy was comparable to that on an inspiratory scan was chosen for interpretation. A total of six scans from each patient—three inspiratory and three corresponding expiratory scans—were evaluated to calculate the increase in lung attenuation during expiration and to visually and quantitatively assess the extent and characteristics of air trapping. Standard lung window settings (level, -700 HU; width, 1,500 HU) were routinely used for this display.
Assessment of Lung Attenuation
On each image, mean lung attenuation was measured in Hounsfield units within two regions of interest (ROIs), which were drawn freehand at a workstation (SIENET MagicView 1000; Siemens) for each lung by one radiologist (N.T.), thus generating two measurements of mean lung attenuation for each image. The mean lung attenuation within each ROI was measured in all six images of each of the subjects, meaning that 12 ROIs were measured for each subject. The ROIs excluded the chest wall and large hilar vessels. Results of our preliminary experiments indicated that mean lung attenuation values were not markedly affected by small variations in the ROI if the chest wall and major hilar vessels were carefully excluded from the ROI. Three CT measurements were performed at each CT examination: (a) mean lung attenuation of each lung at each lung level during inspiration (lung attenuation during inspiration), (b) mean lung attenuation of each lung at each lung level during expiration (lung attenuation during expiration), and (c) mean increase in lung attenuation from inspiration to expiration at each lung level (increase in attenuation). The last measurement was calculated by subtracting the mean lung attenuation value during inspiration from that during expiration at each level.
Visual Assessment of Air Trapping
For the visual assessment of air trapping, two chest radiologists (N.T. and G.M.) who were blinded to patient information independently reviewed the six pairs of inspiratory-expiratory CT images from each of the 50 patients in random order and assessed the degree and characteristics of air trapping. Air trapping was classified into one of the following categories: no air trapping, lobular air trapping, mosaic air trapping, and extensive air trapping. Air trapping on expiratory CT images was defined as the presence of lung regions that were more lucent than adjacent lung regions (17). Air trapping was classified as lobular when composed of small areas of hypoattenuation that corresponded to one or two adjacent secondary pulmonary lobules in one or two regions per lung level; as mosaic when three or more areas of lobular air trapping were observed to alternate with areas of normally attenuating lung, usually in a multilobular distribution; and as extensive when a contiguous area of air trapping was larger than three adjacent pulmonary lobules and was subsegmental, segmental, or lobar in distribution. Before assessing the study images, the two radiologists reviewed several actual examples of lobular, mosaic, and extensive air trapping as reference images.
In cases of discordant analysis, the two radiologists reviewed the images together with a third chest radiologist (T.M.), and a final decision was reached by the three radiologists in consensus. The distribution of the areas of air trapping was also assessed. The presence or absence of air trapping was recorded in the nondependent and dependent lung areas in each upper, middle, and lower lung level—six areas in total. Nondependent and dependent areas of lung were demarcated by drawing a horizontal line at the workstation across both lungs halfway between the anterior and posterior margins of the thorax.
Semiquantitative Assessment of Air Trapping
The extent of air trapping and the cross-sectional lung area were assessed semiquantitatively by one chest radiologist (N.T.) for each section by superimposing a 3 x 3-mm grid on the CT images (Fig 1). The squares containing pulmonary lung parenchyma of decreased attenuation on expiratory scans were counted manually, as were the squares overlying the parenchyma of both lungs on each scan. The semiquantitative ratio of air trapping, which represents the extent of air trapping, was obtained by determining the ratio of the total number of squares containing air trapping to the total number of squares overlying lung parenchyma. Then, an overall ratio of air trapping was calculated as the mean of the ratios obtained at the three lung levels. The degree of air trapping was classified according to the following grading system: grade 1, area of air trapping between 0%–5% of total lung parenchyma; grade 2, area of air trapping between 6%–15% of total; and grade 3, area of air trapping more than 16% of total.
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value was calculated ( < 0.20 was considered to indicate 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, very good agreement). All other statistical analysis was performed with commercially available software (StatView version 4.5; Abacus Concepts, Berkeley, Calif) and with commercially available free software (G-Power version 2.1.2; Axel Buchner et al. Available at: www.psycho.uni-duesseldorf.de/aap/projects/gpower/index.html).
For multiple comparisons involving patient characteristics (age, FEV1/FVC value, percent predicted MEF50% value), lung attenuation measurements (CT parameters), and the semiquantitative ratio of air trapping among the three groups, the Fisher protected least significant difference (PLSD) test was used. For comparisons of cigarette consumption between the group of current smokers and the group of ex-smokers and between the group of mild smokers and the group of heavy smokers and for comparisons of the semiquantitative ratio of air trapping between the group of smokers and the group of nonsmokers, the Student t test was used. The Kruskal-Wallis rank test was used for comparisons involving the visual assessment (visual grade) of air trapping among the three groups; the Mann-Whitney U test was used for such comparison between the group of smokers and the group of nonsmokers. A P value of less than .05 was considered to indicate a statistically significant difference.
For correlation of PFT results with CT measurements and with the semiquantitative ratio of air trapping, and for correlation of smoking habit (in pack-years) with the semiquantitative ratio of air trapping, a parametric test (Pearson correlation coefficient) was used. For correlation of PFT results with the visual grade of air trapping and for correlation of the semiquantitative ratio of air trapping with the visual grade of air trapping, a nonparametric test (Spearman correlation coefficient by rank) was used. A correlation was considered to be present when a P value was less than .05.
The power analysis for the comparison of three CT attenuation measurements (lung attenuation during inspiration, lung attenuation during expiration, and expiratory increase in lung attenuation) and for the comparison of visual grades or semiquantitative ratio of air trapping between nonsmokers and smokers was performed with the G-Power software. The 
error value (the probability of a type 1 error) was set at .05, and the ß error value (the probability of falsely accepting the null hypothesis) and the power (ie, 1 - ß) were calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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= 0.730). There was no significant correlation between the visual grade of air trapping and PFT results. There was no significant correlation between FEV1/FVC or percent predicted MEF50% and the visual grade of air trapping (P = .07 and .657, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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There are several possible reasons for this difference: (a) All healthy volunteers in the study of Webb et al (17) were considerably younger (age range, 24–31 years) than the patients in our study, and all were nonsmokers; (b) CT attenuation in the previously mentioned studies was measured within relatively small ROIs (approximately 2 x 2 cm in both studies)—this was markedly different from our method of measurement of the mean attenuation of both lungs, and CT attenuation in small ROIs does not fully represent the mean lung attenuation of the lungs; and (c) it is possible that full inspiration or full expiration was not achieved in some cases in our study because we did not use spirometrically gated inspiratory and expiratory CT.
In the present study, no significant difference in increase in lung attenuation during expiration was observed among the ex-smokers, current smokers, and nonsmokers. The change in lung attenuation from inspiration to expiration probably reflects global pulmonary function rather than a local function such as local air trapping. Smokers and nonsmokers with abnormal pulmonary function were excluded from our study, and there were no significant differences in PFT results among nonsmokers, ex-smokers, and current smokers. Therefore, it is not surprising that no significant difference in increase in lung attenuation during expiration was observed among these three groups.
Air trapping is a pathophysiologic term for the retention of excess gas in all or part of the lung at any stage of expiration, according to the definition proposed by the Nomenclature Committee of the Fleischner Society (1). Several authors have described the frequency of air trapping in subjects with normal pulmonary function. Table 7 summarizes the results of previous studies and our study in terms of the frequency of air trapping in normal subjects. Webb et al (17) mentioned, in their report of 10 young, healthy volunteers with normal pulmonary function, that four subjects (40%) had local air trapping. Chen et al (18) reported that air trapping was seen in eight (61.5%) of 13 healthy participants. Lee et al (19) reported a frequency of air trapping of 52% in 82 asymptomatic patients with normal PFT results. Mastora et al (16) recently reported air trapping in 155 (62.0%) of 250 volunteers. Although 214 of the 250 volunteers in that study had normal pulmonary function, air trapping was seen in a considerable number of the volunteers with normal pulmonary function (the precise number was not mentioned) (16).
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Potential reasons for the high prevalence of air trapping in patients with normal pulmonary function are as follows: (a) extensive difference in local lung compliance or muscle tone of small airways without small-airway disorder, or (b) presence of a small-airway disorder that is too mild to be detected by percent predicted MEF50% testing because such testing does not have adequate sensitivity for the detection of small-airway disorder. This suggests that expiratory CT may be more sensitive in detecting local air trapping than pulmonary function testing. However, other sensitive tests for small-airway disorders, such as the nitrogen washout test or the closing volume test, were not performed in this study.
Lobular air trapping was observed in 10 patients (20%) in this study. Air trapping in isolated secondary pulmonary lobules is sometimes seen in healthy subjects (10). Webb et al (17) reported that three (30%) of 10 healthy volunteers in their study had lobular air trapping. Lee et al (19) reported that air trapping appeared entirely in secondary pulmonary lobules in all 43 subjects (52%) who had air trapping in their study. Park et al (7) reported a frequency of lobular air trapping of 54% among 14 healthy nonsmokers with normal pulmonary function. Mastora et al (16) reported lobular air trapping in 117 (47%) of 250 volunteers. Lee et al (19), Park et al (7), and Mastora et al (16) did not use the concept of mosaic air trapping. Lobular air trapping as defined in their studies might encompass mosaic air trapping as defined in our present study. Webb et al (17) suggested that lobular air trapping was caused by regional differences in lung compliance and the phenomenon of interdependence of adjacent lung units: Because of interdependence, a lung region that is less compliant than the lung parenchyma that surrounds it will show relative air retention during expiration, with less of an increase in lung attenuation than that of the surrounding lung. Mastora et al (16) believed that lobular air trapping was never caused by smallairway diseases because the frequency of lobular air trapping in their study was not significantly different among smokers, ex-smokers, and nonsmokers.
Although lobular air trapping has been regarded as a normal or physiologic phenomenon, extensive air trapping has been regarded as an abnormal feature that is not seen in healthy subjects. Mastora et al (16) found that extensive air trapping was more frequently observed among smokers and believed that it suggested the presence of small-airway disease. However, according to the results of the evaluation of 14 healthy nonsmokers with normal pulmonary function by Park et al (7), the frequencies of moderate air trapping (involvement of between three adjacent lobules and a segment) and severe air trapping (involvement of more than a segment), both of which seem to correspond to extensive air trapping in the present study, were 39% and 14%, respectively. Furthermore, Lee et al (19) reported a frequency of subsegmental or segmental air trapping of 8.5% among 82 healthy subjects with normal pulmonary function.
Extensive air trapping may be seen even in subjects with normal pulmonary function—even in nonsmokers. It remains unclear whether the mosaic pattern of air trapping represents a normal or abnormal phenomenon. Stern et al (23) characterized mosaic air trapping as "extensive lobular air trapping" and regarded it as a morbid phenomenon. However, Chen et al (18) found multifocal air trapping in seven (53.8%) of 13 healthy volunteers. Although it is questionable whether the "multifocal air trapping" in the report of Chen et al (18) is identical to mosaic air trapping, Chen et al regarded multifocal air trapping as a more extensive finding than focal, lobular air trapping. The results of that study indicated that mosaic air trapping can be seen in healthy subjects. In our study, extensive air trapping, as well as mosaic air trapping, was fairly frequently observed (in 16% and 28%, respectively, of patients with normal PFT results). Therefore, we cannot conclude that extensive or mosaic air trapping is an abnormal phenomenon.
In our study, both visual and semiquantitative assessment of air trapping revealed no correlation between smoking habits and the extent of air trapping. In particular, the frequencies of extensive air trapping in current smokers, ex-smokers, and nonsmokers were 21%, 10%, and 15%, respectively, with no significant difference among the three groups. It is also surprising that semiquantitative grade 3 air trapping was seen in three nonsmokers. On the other hand, in the study of Mastora et al (16), segmental and lobar air trapping, which seemed to correspond to "extensive air trapping" in our study, was statistically more frequently observed in current (26%) or ex-smokers (27%) than in nonsmokers (16%). Because the frequency in nonsmokers was almost the same, the difference between the study of Mastora et al (16) and the present study seems to result from the difference in the frequency of air trapping in current or ex-smokers.
In the study of Mastora et al (16), some smokers had abnormal PFT results and inspiratory CT findings, including micronodules, bronchial wall changes, and emphysema. In our study, because all patients had normal PFT results and normal inspiratory CT findings, smokers seemed to have less small-airway impairment than those in the study of Mastora et al (16). This may be a major reason for the lack of a correlation between extent of air trapping and smoking habits in our study. Another reason may be the possibility that diffuse air trapping was not visually identified in the smokers. Unlike focal air trapping, diffuse air trapping is sometimes difficult to detect by means of visual inspection of expiratory images. Results of power analysis for the comparison of visual grade and semiquantitative ratio of air trapping between nonsmokers and smokers indicated a relatively low power for detection of significant differences between the groups, suggesting that the lack of significant differences between nonsmokers and smokers could have been due to the small number of patients. The important point, however, is that both the study by Mastora et al (16) and our study revealed a relatively high prevalence of air trapping in nonsmokers.
There have been several reports of studies that evaluated the correlation between cigarette consumption and the CT finding of air trapping. Lee et al (19) found a significant difference in the grade of moderate air trapping between mild smokers (<10 pack-years) and heavy smokers (>10 pack-years). Verschakelen et al (20) found a significant correlation between cigarette consumption in pack-years and air trapping score. On the other hand, in the current study, we could not find a significant difference either in visual grade or in semiquantitative ratio of air trapping between mild smokers and heavy smokers. There was also no correlation between cigarette consumption and semiquantitative ratio of air trapping. As discussed above, this may have been due to the relatively small number of patients in the smoking groups.
The results of the current study seem to show that mosaic or extensive air trapping can exist in subjects with normal PFT results, irrespective of current smoking status and cigarette consumption. Semiquantitative ratio of air trapping showed a significant correlation with FEV1/FVC. This seems to mean that semiquantitative ratio is a significant index of pulmonary function. The visual grade of air trapping showed a strong correlation with semiquantitative ratio. However, the visual grade of air trapping showed no significant correlation with PFT results.
In terms of the distribution of air trapping, we found a tendency toward lower lung and dependent lung predominance. This result is identical to the results reported by Lee at al (19) and Verschakelen et al (20). The reason for lower lung predominance of air trapping in normal subjects is unclear. However, with regard to dependent lung predominance, Verschakelen et al (20) speculated that air trapping can be depicted more easily because the increase in lung attenuation during expiration is higher in dependent lung. In the study of Verschakelen et al (20), no air trapping was seen in the nondependent lung in nonsmokers, while in the current study, air trapping was observed in the nondependent lung in two nonsmokers. The reason for this discrepancy is unclear. It is possible that small-airway disease was present in these subjects, although careful exclusion of patients with previous respiratory diseases was performed.
There were several limitations in this study. First, we did not use spirometrically gated inspiratory and expiratory CT. This may in part explain our finding of a lower increase in lung attenuation during expiration. Sufficient expiration to the level of residual volume could not be reached by some subjects. Second, CT evaluation was performed only at three levels of the lung. This may not be sufficient because the three levels may not be representative of the whole lung. Third, selection of patients might not have been strict enough. Patients with extrathoracic tumor may have some respiratory problems and may be different from a group of healthy volunteers. Furthermore, because detailed physiologic evaluation for small-airway disease was not performed, it is possible that some subjects with subclinical small-airway disorder might have been included in the study. Finally, the number of patients was relatively small. The reason that there were no significant differences between smokers and nonsmokers at visual or semiquantitative assessment of air trapping might be related to the small number of patients included in this study.
Our study results showed a considerable prevalence of mosaic and extensive air trapping, even in nonsmokers with normal PFT results. Local air trapping on expiratory images should not be regarded as a morbid phenomenon. It may be important to look for other CT signs, including the presence of bronchial wall changes or centrilobular nodules, to support a diagnosis of airway disease. Alternatively, it may be useful to confirm that the results are reproducible by repeating CT after some interval. Furthermore, the prevalence of extensive air trapping in patients with normal PFT may lead us to the speculation that low-attenuating lung areas on expiratory CT images do not necessarily represent real air trapping but may be related to other factors, including pulmonary blood flow. We stress that various degrees of air trapping can be observed in subjects with normal pulmonary function, irrespective of current smoking status and cigarette consumption.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, N.T., T.M., N.M.; study concepts and design, N.T., N.M.; literature research, T.E., G.M.; clinical studies, N.T., T.E.; data acquisition, K.U.; data analysis/interpretation, N.T.; statistical analysis, N.T.; manuscript preparation, N.T., T.M.; manuscript definition of intellectual content, N.T., G.M.; manuscript editing, D.A.L.; manuscript revision/review and final version approval, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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