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1 Department of Radiology, Beth Israel Deaconess Medical Center and Harvard
Medical School, 330 Brookline Ave., Boston, MA 02215.
2 Present address: Department of Radiology, New York University Medical Center
and Harvard Medical School, New York, NY.
3 Division of Pulmonary Medicine, Beth Israel Deaconess Medical Center and
Harvard Medical School, Boston, MA.
Received June 5, 2003;
accepted after revision July 23, 2003.
Address correspondence to P. M. Boiselle.
Abstract
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MATERIALS AND METHODS. The study group consisted of 20 subjects, including 10 patients with bronchoscopically proven tracheobronchomalacia and 10 control subjects of similar ages without tracheobronchomalacia. All 20 subjects underwent MDCT performed at the end of deep inspiration and during dynamic expiration. The images were analyzed at three lung levels, and the extent of air trapping was assessed visually using a 5-point scale. For each subject, a total air-trapping score was derived by summing the values for the three lung levels (possible range, 0–12). Statistical analysis was performed using the Mann-Whitney U test.
RESULTS. In the tracheobronchomalacia group, 10 (100%) of 10 patients showed air trapping, with a median score of 5 (range, 2–12). In the control group, six (60%) of 10 subjects showed air trapping, with a median score of 2 (range, 0–3). The median total air-trapping score was significantly higher (p < 0.001) for the tracheobronchomalacia group compared with the control group. Excessive central airway collapse (expiratory reduction in cross-sectional area of > 50%) was seen on CT scans in all tracheobronchomalacia patients but in none of the control subjects.
CONCLUSION. Air trapping was observed with a higher frequency and greater severity in patients with tracheobronchomalacia than in a control group of patients of similar ages without tracheobronchomalacia.
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Expiratory high-resolution CT is accepted as a reliable test for the assessment of air trapping [1–4]. Gotway et al. [5] reported that dynamic expiratory thin-section CT is a more sensitive method than end-expiratory CT for detecting air trapping.
Tracheobronchomalacia is a condition characterized by excessive central airway collapsibility due to weakness of the airway walls and supporting cartilage [6–8]. In the clinical practice of interpreting dynamic expiratory CT scans obtained for the evaluation of central airway collapse in patients with tracheobronchomalacia, we have often observed the presence of air trapping in the lungs. The purpose of this study was to compare the frequency and severity of air trapping in patients with and without tracheobronchomalacia using dynamic expiratory CT.
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Exclusion criteria were the presence of significant alveolar or interstitial pulmonary abnormalities on CT scans (including evidence of infectious pneumonia, interstitial pneumonia, or pulmonary fibrosis) or significant central airways disease other than tracheobronchomalacia, such as endobronchial neoplasms or mucoid impaction. The control subjects were selected within an age range similar to that of the tracheobronchomalacia patients to avoid the possibility of differences in air trapping due to age, because air trapping has been reported to increase in frequency with advancing age [9]. A review of each subject's computerized hospital information system records was performed to identify a history of asthma or emphysema.
Imaging Technique
All patients underwent MDCT on either a four- or eight-detector scanner
(LightSpeed, General Electric Medical Systems, Milwaukee, WI). The imaging
parameters were as follows: collimation, 2.5 mm; gantry rotation time, 0.8 sec
(four-detector scanner) or 0.5 sec (eight-detector scanner); pitch, high-speed
mode; pitch equivalent, 1.5; and 120 kVp. CT images were reconstructed with a
high-spatial-resolution algorithm (bone algorithm).
Before volumetric scanning, initial scout topographic images were obtained to determine the area of coverage, which included the trachea and central bronchi, corresponding to a length of approximately 10–12 cm. Scanning was performed in the craniocaudal dimension for both end-inspiratory and dynamic expiratory imaging. End-inspiratory scanning was performed first in all patients, and images were obtained during suspended full inspiration. After end-inspiratory scanning, patients were subsequently coached with instructions for the dynamic expiratory component of scanning. The beginning of the CT acquisition was coordinated with the onset of the patient's expiratory effort. Both inspiratory and expiratory scanning were performed with the patient in the supine position. Standard lung window settings (level, –650 H; width, 1,500 H) were used for display on a PACS (picture archiving communications system) (PathSpeed, General Electric Medical Systems).
Visual Assessment of Air Trapping
To reach consensus, two observers retrospectively reviewed the scans for
evidence of air trapping. Before assessing the study images, the two observers
reviewed a series of reference images that illustrated varying grades of air
trapping. Subsequently, the paired inspiratory–expiratory CT scans from
each of the 20 patients were reviewed randomly on a PACS monitor without
knowledge of the patients' histories.
For each subject, dynamic expiratory images were compared with end-inspiratory images at three anatomic levels: upper lung zone, defined as the level of the superior aspect of the aortic arch; middle lung zone, defined as the level of the carina; and lower lung zone, defined as the level 2 cm below the carina. The degree of air trapping was assessed by comparing end-inspiratory and dynamic expiratory images at similar anatomic levels. Air trapping was defined as the presence of radiolucent regions of the lungs on dynamic expiratory images [9, 10]. The degree of air trapping at each of the three levels was graded on a 5-point scale: 0, no air trapping; 1, 1–25% cross-sectional area affected; 2, 26–50% cross-sectional area affected; 3, 51–75% cross-sectional area affected; and 4, 76–100% cross-sectional area affected. A total air-trapping score was obtained by summing the individual grades for the three levels (maximal possible score, 12).
The pattern of air trapping was categorized as lobular, segmental, lobar, or diffuse. A lobular pattern was defined as areas of air trapping involving less than an entire segment. This pattern included small foci corresponding to the shape of secondary pulmonary lobules and larger foci, comprising several adjacent lobules with involvement of less than an entire segment. A segmental pattern was defined as involvement of an entire segment or multiple adjacent segments involving less than an entire lobe. A lobar pattern referred to involvement of an entire lobe. A diffuse pattern was defined as involvement of greater than 50% of the lungs without a characteristic distribution by lobules, segments, or lobes. It was permissible to list more than one type of pattern for a subject. When more than one pattern was present, it was considered a mixed pattern.
Statistical Analysis
The Mann-Whitney U test was used to compare the total air-trapping
score between the tracheobrancholomacia patients and the control subjects. A
p value of less than 0.05 was considered statistically
significant.
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In the tracheobronchomalacia group, 10 (100%) of 10 patients showed air trapping (Figs. 1A, 1B, 1C, 1D and 2A, 2B), with a median score of 5 (range, 2–12). In the control group, six (60%) of 10 patients showed air trapping, with a median score of 2 (range, 0–3). The total air-trapping score was significantly higher (p < 0.001) in the tracheobronchomalacia group compared with the control group.
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Because four of 10 patients in the tracheobronchomalacia group had underlying asthma or emphysema, known risk factors for air trapping, we also analyzed the data separately for the subgroups of patients with and without these underlying disorders. Of the six tracheobronchomalacia patients without asthma or emphysema, all showed evidence of air trapping, with a mean air-trapping score of 6. Similarly, the four patients with tracheobronchomalacia and history of underlying asthma or emphysema all showed evidence of air trapping, with a mean air-trapping score of 6. Among the six control subjects with underlying asthma or emphysema, two (33%) showed evidence of air trapping, including one (25%) of four control subjects with a history of asthma. The mean score among control subjects with asthma or emphysema who showed air trapping was 3. Similarly, the mean score among the four control subjects without asthma or emphysema who showed air trapping was 3.
The air-trapping patterns are listed in Table 1. The most common air-trapping pattern in the tracheobronchomalacia group was lobular, shown in five (50%) of 10 patients. Similarly, the most common air-trapping pattern for the control group was lobular, present in three (50%) of six control subjects with evidence of air trapping. All 10 patients with tracheobronchomalacia showed more than 50% reduction in the cross-sectional area of the central airways during dynamic exhalation, whereas all control subjects showed less than 50% reduction.
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In this study, air trapping was observed with a significantly higher frequency and greater severity in patients with tracheobronchomalacia compared with a control group of patients of similar ages without tracheobronchomalacia, despite a higher prevalence of disorders known to be associated with air trapping in the control group. To our knowledge, air trapping has not been previously reported in association with tracheobronchomalacia. The cause of air trapping in tracheobronchomalacia patients is uncertain, but it may reflect chronic small airways disease due to abnormal respiratory mechanics related to excessive central airway collapse. Because tracheobronchomalacia is associated with an abnormal coughing mechanism and difficulty clearing secretions, it is plausible that affected patients may experience chronic inflammation of the small airways on this basis. Future studies are necessary to clarify the precise pathophysiologic basis of small airways disease in tracheobronchomalacia patients and to determine whether it improves after therapy for tracheobronchomalacia with stent placement or tracheoplasty.
The acquired form of tracheobronchomalacia has been increasingly recognized as an important cause of chronic respiratory symptoms in recent years [6, 7]. For example, a bronchoscopic series of patients who did not smoke and were being evaluated for chronic cough found tracheobronchomalacia as the cause in 14% of cases [7]. However, tracheobronchomalacia is often overlooked because of its nonspecific clinical symptoms and its usual lack of evidence on routine imaging studies performed at end-inspiration. Clinically, the symptoms are nonspecific and include cough, wheezing, and dyspnea [6–8]. Importantly, these symptoms overlap with those of small airways disease such as asthma.
We also observed air trapping in 60% of the control subjects in our study. This finding is not surprising, considering that many of the control subjects in our study group had risk factors for air trapping such as asthma or emphysema. Additionally, air trapping has been reported in healthy subjects with normal results on pulmonary function tests. Notably, however, the severity of air trapping among the control subjects was significantly lower than that of the tracheobronchomalacia patients in our series. Because focal air trapping can be seen in healthy subjects, we emphasize that it is the extent of air trapping—and not simply its presence—that is physiologically relevant [1].
Although many of the subjects in our study had risk factors for air trapping, the degree of air trapping observed among patients with tracheobronchomalacia was similar in subgroups with and without asthma or emphysema. Similarly, the severity of air trapping among control subjects with and without asthma or emphysema was comparable to, but significantly lower than, that among patients in the tracheobronchomalacia group. Although air trapping has been reported in up to 90% of patients with severe asthma, mild to moderate asthma is associated with a lower frequency and severity of air trapping [28, 29]. Because only one of five subjects with asthma in our control group showed evidence of air trapping (and this subject had only mild air trapping), we suspect that these subjects had mild asthma. Interestingly, Park et al. [29] have shown that there is no significant difference in the prevalence of mild to moderate air trapping between patients with asthma and healthy subjects. These investigators concluded that inspiratory and expiratory thin-section CT scans were of limited value in distinguishing asthmatic patients with normal to mild airflow obstruction from healthy subjects. Thus, we do not believe that this factor influenced our finding that air trapping is of greater severity among patients with tracheobronchomalacia compared with control subjects of similar ages.
A lobular pattern was the most common form of air trapping in both the tracheobronchomalacia and control groups. Thus, the pattern of air trapping does not distinguish patients with tracheobronchomalacia from those with other causes of air trapping. However, in our experience, tracheobronchomalacia patients can readily be distinguished from those with isolated small airways disease by the presence of coexistent excessive collapse of the central airways on expiratory imaging. A reduction in cross-sectional area of more than 50% between inspiration and expiration is generally considered diagnostic of this condition [27].
Two limitations of this study should be mentioned. First, we do not have detailed smoking histories of the study participants. However, the relationship between cigarette smoking and air trapping is controversial [9, 23–26]. Second, a subjective visual assessment of the air-trapping score was performed, and pulmonary function test results were not available for analysis. However, Chen et al. [3] have reported significant correlation between the air-trapping score and inspiratory–expiratory lung attenuation changes and a significant correlation between the air-trapping score and pulmonary function test results. Other authors have also reported similar correlation between the degree of air trapping and pulmonary function test results [9, 17]. Future prospective studies are necessary to correlate air trapping and pulmonary function tests in patients with tracheobronchomalacia.
In summary, our study shows that both the frequency and severity of air trapping are increased among patients with tracheobronchomalacia compared with subjects without this disorder. Therefore, when air trapping is seen in the lung parenchyma on expiratory CT scans, one should carefully compare the caliber of the central airways on inspiratory and expiratory images to assess for tracheobronchomalacia.
Acknowledgments
We thank Alexis Potemkin for administrative assistance and Michael Larson
for assistance with photography.
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