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Correlation of Aging and Smoking with Air Trapping at Thin-Section CT of the Lung in Asymptomatic Subjects¹

¹ From the Departments of Radiology (K.W.L., S.Y.C., I.Y., Y.L., E.Y.K.) and Internal Medicine (M.J.P.), Kangnam Sacred Heart Hospital, Hallym University College of Medicine, 948-1, Daelim-Dong, Youngdeungpo-Ku, Seoul, South Korea, 150-071. Received August 26, 1998; revision requested October 15; final revision received June 1, 1999; accepted August 19. Supported in part by a research grant of Regional University's Specialization from the Government Ministry of Education, Republic of Korea. Address reprint requests to K.W.L.

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To assess the frequency and degree of air trapping at thin-section computed tomography (CT) of the lung in relation to age and smoking history in asymptomatic subjects.

MATERIALS AND METHODS: Thin-section CT of the lung was performed prospectively at end inspiration and end expiration in 82 subjects (27 smokers, 55 nonsmokers) without any history of pulmonary diseases and without present pulmonary symptoms. The frequency and degree of air trapping were evaluated according to age and smoking status.

RESULTS: The overall frequency of air trapping was 52% (43 of 82 subjects, = 0.72). Air trapping was found in three of 13 (23%), seven of 17 (41%), nine of 18 (50%), 11 of 17 (65%), and 13 of 17 (76%) subjects aged 21–30, 31–40, 41–50, 51–60, and greater than or equal to 61 years, respectively. The frequency of air trapping increased with age (P < .05). The degree of air trapping had a significant correlation with age (r = 0.523, P < .001) and was higher in smokers with a smoking history of more than 10 pack-years (P < .05).

CONCLUSION: Air trapping was found in approximately 50% of asymptomatic subjects. The frequency of air trapping increased with age, and its severity increased with age and smoking.

Index terms: Computed tomography (CT), thin-section, 60.12118 • Emphysema, pulmonary, 60.751 • Lung, abnormalities, 60.751 • Lung, air trapping, 60.75 • Lung, CT, 60.12118 • Lung, density, 60.751, 60.90

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Air trapping on computed tomographic (CT) scans is defined as "decreased attenuation of pulmonary parenchyma, especially in attenuation during expiration" (1). From a physiologic perspective, CT scans obtained during forced exhalation show a homogeneous increase in pulmonary attenuation because the amount of air in the lung being scanned is reduced (2). With air trapping, the involved pulmonary parenchyma does not show an increase in attenuation during CT and remains more lucent than the surrounding normal pulmonary tissue (2–4).

Recently, CT scans obtained at suspended full expiration have mainly been used to show air trapping in patients with emphysema (5), asthma (6,7), bronchiectasis (8), Langerhans cell histiocytosis (9), chronic airway disease (4,10), and pediatric pulmonary disease (11,12); in asymptomatic smokers (13); and in asymptomatic subjects (2,7). To our knowledge, only a few reports exist regarding the frequency of air trapping in asymptomatic subjects, which varies from 0% to 40% (2,7,10). The predisposing factors to air trapping in asymptomatic persons have not yet been clearly defined.

The purpose of this study was to assess the frequency and degree of air trapping on thin-section CT scans of the lung in relation to age and smoking status in asymptomatic subjects.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Inspiratory and expiratory thin-section CT was performed prospectively in 88 volunteers, all urban dwellers. We recruited the volunteers from among the employees of our hospital and their relatives. They had no history of pulmonary disease and no clinically important pulmonary symptoms at the time. This study included only adults older than 20 years.

Smoking history was not taken into account during the selection of the subjects. Fifty-five nonsmokers and 27 smokers were included. Six of the 88 subjects were excluded because of the following: emphysema involving more than 1% of the cross-sectional area (n = 2), findings suggestive of active pulmonary tuberculosis (n = 1), bronchiectasis (n = 1), cardiomegaly (n = 1) on CT scans, and abnormal results of the pulmonary function test (n = 1).

Emphysema was defined as the presence of focal areas of decreased attenuation without visible walls on inspiratory CT scans. Six persons were included who had emphysema in the upper lung zone that involved less than 1% of the cross-sectional area (n = 3), minimal bronchiectasis (n = 1), and minimal parenchymal bands (n = 2) on CT scans.

This study thus included 82 subjects (39 men, 43 women) 20–80 years of age (mean age, 45 years): 13 persons aged 21–30 years, 17 aged 31–40 years, 18 aged 41–50 years, 17 aged 51–60 years, and 17 aged 61 years or older. No one age group included more than 18 participants, and no specific selection criteria were used to pick the maximum of 18 subjects for each group from the larger group of volunteers.

The study was approved by the hospital ethics committee, and informed consent was obtained from all subjects before inclusion in the study.

CT scans (Somatom Plus 4; Siemens, Erlangen, Germany) were obtained with 1-mm collimation, 120 kVp, and 200 mA by using a high-frequency reconstruction algorithm. The images were obtained at a window level of -700 HU and at a window width of 1,500 HU. In all subjects, both end-inspiratory and end-expiratory scans were obtained at five levels: at the apex, at the aortic arch, at the carina, between the carina and the diaphragm, and at the dome of the diaphragm. The subjects were coached and rehearsed in full inspiration and expiration before CT was performed. Misregistration between inspiratory and expiratory CT scans at the same level was not taken into account.

CT scans were reviewed independently by two radiologists (K.W.L., I.Y.) for the presence and degree of air trapping. We defined air trapping as failure of an area to increase in attenuation after full expiration, compared with the attenuation at full inspiration. If there was disagreement between the two radiologists, the final interpretation was obtained by consensus.

The presence and dominant site of air trapping were determined for each lung at the lobar level. The extent of air trapping and the cross-sectional lung area were assessed quantitatively for each section by superimposing a 3 x 3-mm grid on the CT image (Fig 1). The squares containing pulmonary tissue of decreased attenuation on the expiratory scan were counted manually, as were the squares overlying the parenchyma of both lungs for each section.

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Transverse, end-expiratory, thin-section CT scan with grid of 3 x 3-mm squares superimposed shows the method of quantitative assessment of air-trapping area in both lungs, which was used at five levels. The squares containing pulmonary tissue of decreased attenuation on the end-expiratory scan were counted manually, as were the squares overlying the parenchyma of both lungs for each section.

View larger version (97K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Grade I air trapping in a 37-year-old man with normal pulmonary function test results and without any history of pulmonary disease or symptoms. (a) Inspiratory, transverse, thin-section CT scan obtained through the lower lung zone shows homogeneous attenuation and no abnormal findings. (b) Expiratory, transverse, thin-section CT scan obtained at the same level as a reveals air trapping (arrows) with a mosaic pattern in the secondary pulmonary lobules. The mean of the percentages of air trapping obtained at four levels was less than 5% of the total lung area.

View larger version (106K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Grade I air trapping in a 37-year-old man with normal pulmonary function test results and without any history of pulmonary disease or symptoms. (a) Inspiratory, transverse, thin-section CT scan obtained through the lower lung zone shows homogeneous attenuation and no abnormal findings. (b) Expiratory, transverse, thin-section CT scan obtained at the same level as a reveals air trapping (arrows) with a mosaic pattern in the secondary pulmonary lobules. The mean of the percentages of air trapping obtained at four levels was less than 5% of the total lung area.

View larger version (99K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Grade II air trapping in a 51-year-old man with normal pulmonary function test results and without any history of pulmonary disease or symptoms. (a) Inspiratory, transverse, thin-section CT scan obtained through the lower lung zone shows no abnormal findings. (b) Expiratory, transverse, thin-section CT scan obtained at the same level as a reveals air trapping (arrows) with a mosaic pattern. The sum of the mean percentages of air trapping obtained at four levels was approximately 10% of the total lung area.

View larger version (108K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Grade II air trapping in a 51-year-old man with normal pulmonary function test results and without any history of pulmonary disease or symptoms. (a) Inspiratory, transverse, thin-section CT scan obtained through the lower lung zone shows no abnormal findings. (b) Expiratory, transverse, thin-section CT scan obtained at the same level as a reveals air trapping (arrows) with a mosaic pattern. The sum of the mean percentages of air trapping obtained at four levels was approximately 10% of the total lung area.

The frequency and grade of air trapping were evaluated for each age group for the correlation between air trapping and aging. The smokers were classified into three groups according to the amount of smoking as follows: less than 10 pack-years (n = 6), 11–20 pack-years (n = 7), and more than 20 pack-years (n = 14). The relationship between air trapping and the amount of smoking was also assessed. Proportions were compared with the ² test. A P value of less than .05 was considered to indicate a statistically significant difference.

Pulmonary function tests were performed in 47 of the 88 subjects immediately after obtaining the CT scans. Forced vital capacity (FVC); forced expiratory volume in 1 second (FEV₁); FEV₁/FVC; forced expiratory flow, midexpiratory phase; total lung capacity; residual volume; and diffusing capacity of carbon monoxide were obtained. Anyone with less than 70% of the predicted value of FVC, FEV₁, or FEV₁/FVC was excluded from this study. Only one of the 47 subjects was excluded.

Use of the pulmonary function test was ceased during the course of study after 47 subjects had been examined because the number already tested was thought to be sufficient for comparison of the pulmonary function test parameters between the air-trapping group and the group without air trapping. The subjects who underwent the pulmonary function test were not selected. The proportion of subjects who did not undergo pulmonary function tests was not significantly different between the air-trapping group and the non–air-trapping group.

The difference between the mean values of pulmonary function test parameters in the air-trapping group and those in the group without air trapping were tested by using the Student t test. The grade of air trapping was correlated with the results of pulmonary function test and age by using a nonparametric test (Spearman rank correlation).

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
The overall frequency of air trapping was 52% (43 of 82 subjects). Grade I air trapping was found in 26 subjects, and grade II air trapping was found in 17 subjects. No one had an area of air trapping larger than 25% of the total area of the lung. Interobserver agreement was good both for the presence of air trapping ( = 0.72) and for the grade of air trapping ( = 0.61).

Air trapping was found in three of 13 (23%) persons aged 21–30 years, seven of 17 (41%) aged 31–40 years, nine of 18 (50%) aged 41–50 years, 11 of 17 (65%) aged 51–60 years, and 13 of 17 (76%) aged 61 years or older (Table 1). The increase in the frequency of air trapping with aging was statistically significant (P < .05).

Pulmonary function test results were within normal ranges in all subjects, regardless of the presence of air trapping. A statistically significant difference was found in the mean values of FVC and FEV₁/FVC between the air-trapping group and the non–air-trapping group (Table 3). The grade of air trapping had a significant correlation with FEV₁/FVC (r = -0.438, P = .002) and with age (r = 0.523, P < .001) (Table 4).

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

However, the small number (from 10 to 14) of subjects and the relatively young ages of the subjects in these studies make the results difficult to generalize. Our study, which included 82 subjects, is to our knowledge one of the largest series of asymptomatic subjects with evaluation of air trapping. In addition, our study included an even number of subjects in each age group. In our study, the overall frequency of air trapping in asymptomatic subjects was approximately 50%, which is higher than the frequency in other reports. This result may be due to the fact that we included an older age group and smokers.

With age, the lung undergoes a predictable set of morphologic changes, which include increased alveolar duct air; decreased complexity of the alveolar surface or surface-to-volume ratio; loss of alveolar wall tissue, elastic tissue, and bronchiolar muscle; and increased frequency of emphysema (17).

Such changes in the lung with age may be due to environmental pollutants, which include smoke, rather than simply aging alone. Significant differences between current smokers, former smokers, and nonsmokers have been observed on thin-section CT scans with regard to subpleural and parenchymal micronodules, emphysema, and areas of ground-glass opacity (13). A higher frequency of air trapping has been reported in heavy smokers than in nonsmokers or light smokers (18).

In our study, air trapping increased significantly with age. The correlation between the grade of air trapping and age also was significant. In addition, we found a tendency of higher frequency of air trapping in smokers, despite the lack of statistical significance. Air trapping of grade II or higher was found more frequently in subjects with a smoking history of more than 10 pack-years (38%) than in subjects with no smoking history (15%) or a history of less than 10 pack-years (17%). The results suggest that the amount of smoking influenced the degree of air trapping. Therefore, aging and smoking could be predisposing factors to air trapping.

It was reported in a study in which 10 healthy subjects were examined that four of the subjects had air trapping. In none of these subjects did the extent of air trapping exceed 25% of the cross-sectional area of one lung at one scanning level. Three of them had air trapping in one or several secondary pulmonary lobules at various sites (2). Because occasional air trapping in isolated secondary lobules can be seen in asymptomatic subjects, it has been suggested that the extent of air trapping, not simply its presence, is important (2).

In our study, we also found no one had an air-trapping area of more than 25% of the total area of the lung. Two thirds of the subjects with air trapping had air trapping in less than 5% of the total area of the lung. This result supports the hypothesis that the extent of air trapping is important in the diagnosis of airway disease.

Air trapping appeared as a mosaic pattern in almost all of the subjects with air trapping in our study, which suggests that air trapping occurred very frequently in secondary pulmonary lobules as a unit. Air trapping is induced from occlusion or narrowing of the airway. Therefore, we suggest that occlusion or a luminal narrowing of the airway related to aging and smoking might occur at the lobular bronchiole level. Further histologic study is needed to confirm this.

Webb et al (2) reported a dominance of air trapping in the lingular segment of the left upper lobe or superior segment of both lower lobes. In our study, lower lobe dominance was present in 36 of the 43 (84%) subjects with air trapping. Even distribution of air trapping was found in seven subjects. Dominance in the lingular segment of the left upper lobe or the superior segment of both lower lobes was not found. Further studies are needed to explain the dominance of air trapping in the lower lobe.

It is well known that most parts of the lungs, especially the lower lobes, move between inspiration and expiration. This misregistration was not taken into account in our study. Exact, comparable levels for inspiratory and expiratory CT scans were not necessary for the analysis of the presence and extent of air trapping, because all of the inspiratory CT scans were normal and only expiratory CT scans showed air trapping.

Methods of quantifying pulmonary attenuation on CT scans have been addressed in numerous studies. Some authors reported using a spirometer to standardize expiratory CT (19,20). Reproducibility on the order of 5% or better could be achieved with tight spirometric control of respiration (20). However, full-inspiratory and full-expiratory CT scans were obtained without spirometric control only after rehearsal with subjects in a majority of the studies. For analysis of the presence and extent of air trapping, using a spirometer may not be necessary to standardize full-expiratory and full-inspiratory CT.

Lucidarme et al (10) suggested that expiratory CT allowed one to calculate a reduction score for a cross-sectional lung area that appeared to be better correlated with the degree of airway obstruction measured with pulmonary function tests. At a fundamental level, the small airways contribute little to normal airway resistance. Considerable small airway obstruction may be present without any change in the FEV₁. Furthermore, air trapping observed in some patients with normal pulmonary function test results suggests that expiratory CT may complement the basic evaluation for detecting small airway disease. In our study, pulmonary function test results were within normal ranges in all subjects, regardless of the presence of air trapping. However, the mean values of FVC and FEV₁/FVC showed a significant difference between the air-trapping group and the non–air-trapping group. The FEV₁/FVC also showed a significant correlation with the grade of air trapping. Our study findings suggest that air trapping on expiratory thin-section CT scans might reflect subtle changes of parameters of pulmonary function tests, especially FEV₁/FVC, without any clinical symptoms.

One limitation of our study was the lack of histologic evidence. Our criteria for choosing asymptomatic subjects may not have been strict enough, and subjects with subclinical small airway disease might have been erroneously included in our study. The fact that pulmonary function test was not performed in all subjects was another limitation.

In conclusion, air trapping occurred in approximately 50% of asymptomatic subjects on thin-section CT scans and manifested as a mosaic pattern with lower lobe predominance. Aging and smoking are possible predisposing factors to air trapping.

	Footnotes

 
Abbreviations: FEV₁ = forced expiratory volume in 1 second FVC = forced vital capacity

Author contributions: Guarantor of integrity of entire study, S.Y.C.; study concepts, K.W.L., S.Y.C.; study design, K.W.L.; definition of intellectual content, Y.L.; literature research, Y.L.; clinical studies, M.J.P.; data acquisition and analysis, K.W.L., I.Y.; statistical analysis, E.Y.K., K.W.L.; manuscript preparation, E.Y.K., K.W.L.; manuscript editing, K.W.L.; manuscript review, S.Y.C., I.Y.

	References

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This Article Abstract Figures Only Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Lee, K. W. Articles by Park, M. J. Search for Related Content PubMed PubMed Citation Articles by Lee, K. W. Articles by Park, M. J.