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* From the Center for Airway Imaging, Department of Radiology, and Division of Thoracic Surgery and Interventional Pulmonary, Beth Israel Deaconess Medical Center, Boston, MA.
Correspondence to: Armin Ernst, MD, FCCP, Division of Thoracic Surgery and Interventional Pulmonary, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215; e-mail: aernst{at}bidmc.harvard.edu
Abstract
Objective: To assess the accuracy of dynamic expiratory CT for detecting airway malacia using bronchoscopy as the diagnostic "gold standard."
Materials and methods: A computerized hospital information system was used to retrospectively identify all patients with bronchoscopically proven airway malacia referred for CT airway imaging at our institution during a 19-month period. CT was performed within 1 week of bronchoscopy. All patients were scanned with a standard protocol, including end-inspiratory and dynamic expiratory volumetric imaging, using an eight-detector multislice helical CT scanner. For both CT and bronchoscopy, malacia was defined as 
50% expiratory reduction of the airway lumen. CT and bronchoscopic findings were subsequently jointly reviewed by the radiologist and bronchoscopist for concordance.
Results: Twenty-nine patients (12 men and 17 women; mean age, 60 years; range, 36 to 79 years) comprised the study cohort. CT correctly diagnosed malacia in 28 of 29 patients (97%). The most common presenting symptoms were dyspnea in 20 patients (69%), severe or persistent cough in 16 patients (55%), and recurrent infection in 7 patients (24%). The estimated radiation dose (expressed as dose-length product) for the dual-phase study is 508 mGy-cm, which is comparable to a routine chest CT.
Conclusion: Dynamic expiratory CT is a highly sensitive method for detecting airway malacia and has the potential to serve as an effective, noninvasive test for diagnosing this condition.
Key Words: airway • bronchomalacia • CT • malacia • tracheobronchomalacia • tracheomalacia
Acquired tracheomalacia, a condition defined by excessive expiratory collapse of the trachea due to weakness of the airway walls and/or supporting cartilage,12 is a relatively common but frequently overlooked cause of chronic cough and other respiratory symptoms.3 It has been associated with a variety of risk factors and comorbidities, most notably COPD.3456
Because tracheomalacia cannot be detected with routine end-inspiratory imaging studies such as chest radiography and standard CT, it is widely considered an underdiagnosed condition.78 Importantly, if left untreated, tracheomalacia can cause significant respiratory morbidity, and it can rarely be fatal.3 Although bronchoscopy with functional maneuvers can reliably detect tracheomalacia, it may not be clinically feasible or desirable to perform this test in all patients who present with chronic cough and other nonspecific respiratory symptoms. Thus, there is a need for an effective, noninvasive test to improve the detection of tracheomalacia.
Recent advances in CT imaging afford the opportunity to noninvasively diagnose tracheomalacia using dynamic expiratory imaging (imaging during a forced exhalation). To date, however, only small case series910 have been published. Thus, the purpose of this study is to compare the results of dynamic expiratory CT with the reference "gold standard" of bronchoscopy in a large series of patients with airway malacia in order to determine whether CT has the potential to serve as an effective, noninvasive method for diagnosing this condition.
Materials and Methods
Subjects
Our hospital institutional review board approved the review of radiologic and clinical data for this study. Informed consent was not required for this retrospective analysis, but patient confidentiality was protected. This study was compliant with the requirements of the Health Insurance Portability and Accountability Act.
We used our computerized hospital information system to retrospectively identify all patients with bronchoscopically proven airway malacia referred for CT airway imaging at our institution during a 19-month period (October 2002 to April 2004). At our institution, many patients referred for bronchoscopy routinely undergo a CT airway study prior to the procedure. We initially identified 31 patients with bronchoscopically confirmed airway malacia who underwent both CT and bronchoscopy. Because the diagnosis of airway malacia requires assessment of the airway in the expiratory phase of respiration, patients referred for CT who were unable to cooperate with the dynamic expiratory breathing protocol (described in the section below) were excluded (n = 2). Thus, the final study population was comprised of 29 patients.
For each subject, computerized medical records were retrospectively reviewed. Presenting clinical symptoms and risk factors for airway malacia were recorded.
Imaging Technique
CT imaging for each subject was performed prior to flexible bronchoscopy. All patients underwent imaging on an eight-channel, multidetector, helical CT scanner (LightSpeed; General Electric Medical Systems; Milwaukee, WI) with gantry rotation time of 0.5 s. Patients were imaged with our standard CT central airway protocol, which includes imaging during two different phases of respiration: end-inspiratory (imaging during suspended end-inspiration) and continuous dynamic expiratory (imaging during forceful exhalation). Prior to helical 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 to 12 cm. Helical scanning was performed in the craniocaudal dimension for both end-inspiratory and dynamic expiratory scans. The end-inspiratory scan was performed first in all cases (170 mA; 120 kilovolt peak; 2.5-mm collimation; high-speed mode; with pitch equivalent of 1.5). Following the end-inspiratory scan, patients were subsequently coached with instructions for the dynamic expiratory component of the scan (40 mA; 120 kilovolt peak; 2.5-mm collimation; high-speed mode; with pitch equivalent of 1.5). For this sequence, patients were instructed to take a deep breath in and to blow it out during the CT acquisition, which was coordinated to begin with the onset of the forced expiratory effort.
In order to minimize radiation exposure, a low-dose technique (40 mA) was employed for the dynamic expiratory sequence. The use of a low-dose technique for expiratory imaging of the central airways has been validated by Zhang et al.10
Image Analysis
As part of an ongoing multidisciplinary protocol, an experienced thoracic radiologist prospectively reviewed the CT images on a picture archiving and communication system (PACS) [PathSpeed, General Electric Medical Systems] prior to bronchoscopy. Standard lung (level, – 650 Hounsfield units [HU]; width, 1,500 HU) and soft tissue (level, 50 HU; width, 350 HU) window settings were used for display on a PACS workstation. For each study, both end-inspiratory and dynamic expiratory images were assessed for evidence of malacia. The dynamic expiratory images were first visually inspected for the airway site of maximal collapse. Using a computerized tracing tool that is available as part of our PACS system, the inner wall of the airway was hand traced at the level of maximal collapse in order to calculate the cross-sectional area of the airway in millimeters squared (Fig 1
). The cross-sectional area of the airway lumen at the same level on end-inspiration was then determined by using the same tracing method. To calculate the percentage of luminal collapse, the dynamic expiratory cross-sectional area was subtracted from the end-inspiratory cross-sectional area and then divided by the end-inspiratory cross-sectional area and multiplied by 100. Malacia was determined to be present if the percentage of luminal collapse on dynamic expiration was 50%.11 The distribution of malacia involving the trachea, bronchi, or both was also recorded.
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Following the completion of both CT and bronchoscopy, findings for each subject were subsequently jointly reviewed by the radiologist and bronchoscopist for any discrepancies. The sensitivity of CT was calculated using bronchoscopy as the diagnostic "gold standard."
Results
The final study cohort was comprised of 29 patients (17 women and 12 men; mean age, 60 years; range, 36 to 79 years). CT findings were concordant with bronchoscopic findings for the presence and distribution of airway malacia in 28 of 29 patients (97%) [Figs 234 ]. CT was concordant with bronchoscopy regarding the distribution of malacia in these 28 cases: diffuse tracheobronchomalacia in 23 cases (82%), bronchomalacia in 3 cases (11%), and tracheomalacia in 2 cases (7%) [Table 1 ].
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50% dynamic expiratory collapse) for the diagnosis of tracheomalacia (Fig 5
). At bronchoscopy, this subject was noted to have a moderate degree of tracheomalacia involving the middle and distal trachea.
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The estimated dose-length product (as recorded from the CT display monitor for a 70-kg patient) for this dual-phase, modified-dose protocol is 508 mGy-cm. This compares to a reference standard of 650 mGy-cm for a standard chest CT.8
Discussion
Acquired tracheomalacia has been increasingly recognized as a relatively common but underdiagnosed cause of chronic respiratory symptoms.1341115 Bronchoscopic visualization of dynamic airway collapse is the current "gold standard" for diagnosis, but it is an invasive technique with small but inherent risks. Pulmonary function testing may provide supportive evidence of this condition, but it is not diagnostic.3 Because it is a functional abnormality that cannot be diagnosed on routine end-inspiratory imaging, malacia usually goes undetected on standard chest CT examinations. Thus, there is a need for an effective noninvasive test to improve its detection.
Dynamic expiratory CT imaging has emerged as a potentially promising noninvasive method to assess for airway malacia.11 To date, however, there are only limited data in the literature regarding its accuracy in direct comparison with the reference standard of bronchoscopy. A study by Gilkeson et al9 included six patients with suspected airway malacia who were evaluated both with paired inspiratory and dynamic expiratory CT imaging and flexible bronchoscopy. These authors found that CT findings agreed with bronchoscopic results in five of six patients; however, CT underestimated the degree of collapse in one patient.
In our study, we compared the results of dynamic expiratory CT with bronchoscopy for diagnosing airway malacia in a larger series comprised of patients with a broad range of ages. Notably, we found that the sensitivity (97%) of this technique approaches that of bronchoscopy. Although our study design did not allow for an assessment of specificity, one would anticipate a high specificity for CT because of its reliance on precise calculations of the change in caliber of the airway for diagnosis.
As is typical for patients with this condition, our study cohort presented with nonspecific chronic respiratory complaints, including dyspnea, cough, and recurrent infections. Thus, it is not possible to make the diagnosis of malacia on the basis of clinical symptoms alone. Although bronchoscopy can reliably diagnose this condition, it may not be clinically feasible to perform this procedure in all patients with chronic respiratory symptoms.
Our results suggest a potential role for CT as a noninvasive, safe, and highly sensitive test to screen for the presence of malacia among patients with otherwise unexplained chronic respiratory symptoms who are at risk for this potentially treatable condition. Importantly, by using a previously validated, reduced-dose technique, our protocol has a similar radiation dose as a routine chest CT.16 Although this study focused on the sensitivity of CT for diagnosing malacia, it should be noted that this same CT examination can simultaneously assess for other causes of chronic respiratory symptoms, including emphysema and bronchiectasis. Thus, in patients without evidence of malacia, CT offers the possibility of identifying another cause of respiratory symptoms.
Although a large majority of our study patients completed the dual-phase CT protocol, there were two patients referred for CT who were unable to follow the breathing protocol. These patients comprised 6% of all patients referred for this test during the study period. In our experience, very elderly patients and those with hearing impairment are most likely to have difficulty with this protocol. Radiologic imaging alternatives for such patients include imaging with CT during other functional maneuvers such as coughing. Regarding the single false-negative finding in our cohort (Fig 5), we anticipate that the discrepancy between CT and bronchoscopy is due to either suboptimal timing of the scan with respect to the patient’s exhalation or due to a submaximal expiratory effort. Thus, bronchoscopy should be performed if clinical suspicion for malacia is high, despite a negative CT result.
This study is limited by its retrospective design. As such, the interventional pulmonologists performing bronchoscopy were not blinded to the initial CT findings. We recognize that knowledge of the presence of malacia on CT could have introduced bias among the pulmonologists. A future double-blinded study would be helpful to avoid this potential bias. Moreover, a prospective, multicenter trial comparing dynamic expiratory CT and bronchoscopy among patients with nonspecific chronic respiratory symptoms would be helpful to assess the reproducibility of our findings across multiple centers. Such a study would also help to determine the prevalence of malacia among patients with chronic nonspecific respiratory symptoms and to assess the specificity of CT for diagnosing tracheobronchomalacia.
Finally, we emphasize that this protocol was performed using existing multidetector row CT scanners, which are increasingly available in a variety of practice settings. Additionally, the technique requires only minimal training of CT technologists to familiarize them with the breathing instructions and scanning parameters.
In summary, our study shows that dynamic expiratory CT is a highly sensitive method for diagnosing airway malacia when compared with bronchoscopy, the current "gold standard." Thus, dynamic expiratory CT has the potential to play an important role in improving the detection of airway malacia, an underdiagnosed and potentially treatable cause of chronic respiratory symptoms.
Footnotes
Abbreviations: HU = Hounsfield unit; PACS = picture archiving and communication system
The authors do not report any conflicts of interest related to the topic discussed in this article.
Received for publication August 31, 2006. Accepted for publication October 12, 2006.
References
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