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Tracheomalacia Incidentally Detected on CT Pulmonary Angiography of Patients with Suspected Pulmonary Embolism

¹ Department of Radiology, Beth Israel Deaconess Medical Center and Harvard Medical School, 330 Brookline Ave., Boston, MA 02215.
² Present address: Department of Diagnostic Radiology, School of Medicine, Keio University, Tokyo, Japan.

Received February 12, 2003; accepted after revision July 1, 2003.

 
Supported by GE-YMS Educational Fund.

Address correspondence to I. Hasegawa (ihasegaw{at}caregroup.harvard.edu).

Abstract

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OBJECTIVE. The aim of this study was to determine the frequency of tracheomalacia incidentally detected on CT pulmonary angiography in patients with suspected pulmonary embolism.

MATERIALS AND METHODS. CT records of 163 consecutive patients imaged with CT pulmonary angiography for suspected pulmonary embolism were retrospectively reviewed at our institution. The patients underwent CT pulmonary angiography with three different types of CT scanners. All images were visually assessed by two thoracic radiologists for excessive collapse of the trachea and the main bronchi. The cross-sectional area of the lumen at the site of maximal collapse of the airway was measured, and the percentage of luminal narrowing was calculated by comparing it with the cross-sectional area of the airway lumen at an adjacent area without collapse. We defined tracheomalacia as a 50% or greater decrease in tracheal lumen.

RESULTS. Sixteen (10%) of 163 patients showed evidence of tracheomalacia (seven men, nine women; age range, 41–95 years; mean age, 72 years). The most common presenting symptom was shortness of breath, which was observed in 13 (81%) of 16 patients. Known causes of tracheomalacia were found in 15 (94%) of 16 patients, prior intubation was confirmed in 12 patients, and history of asthma or chronic obstructive pulmonary disease was observed in five patients.

CONCLUSION. Tracheomalacia is a relatively common incidental finding on CT pulmonary angiography studies. The central airways, as well as pulmonary vasculature, should be reviewed carefully for clinical interpretation in patients with suspected pulmonary embolism. Paired expiratory–inspiratory CT is recommended if patients present with known causes of tracheomalacia such as prior intubation, chronic obstructive pulmonary disease, or asthma.

Introduction

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Tracheobronchomalacia has been recognized as an important cause of nonspecific pulmonary symptoms [1–3], but it is likely an underdiagnosed condition. Previous studies in the general population reported that tracheobronchomalacia is identified in 1–10% of bronchoscopies and in up to 20% of autopsies [4, 5]. Jokinen et al. [6] showed a 23% incidence rate in 214 patients examined bronchoscopically for a history of chronic bronchitis. Although the diagnosis of tracheobronchomalacia has historically required cine fluoroscopy or bronchoscopy [1, 7], recent advances in CT technology, including electron beam CT and MDCT, have made it possible to diagnose this process [1, 8]. For example, Gilkeson et al. [1] reported that MDCT with dynamic inspiratory–expiratory imaging is a promising method in the evaluation of patients with tracheomalacia. The most common CT finding during dynamic expiration was tracheal collapse with crescentic bowing of the posterior membranous trachea [1].

Tracheobronchomalacia is characterized by increased compliance and excessive collapsibility of trachea or bronchi. Increase in compliance is due to loss of structural integrity of components in the tracheal wall and may be congenital or acquired [9]. The causes of congenital tracheomalacia include cartilage deficiency, generalized tracheomalacia, and congenital tracheoesophageal fistula [9]. Acquired tracheomalacia is associated with endotracheal tubes and tracheostomy, closed chest trauma, lung resection, radical neck dissection, radiation therapy, chronic obstructive pulmonary disease, relapsing polychondritis, paratracheal vascular abnormality, and chronic or recurrent infection [9].

CT pulmonary angiography is an established diagnostic tool to evaluate pulmonary embolism [10–12]. Patients with pulmonary embolism typically have dyspnea or pleuritic chest pain [13]. However, the symptoms are often nonspecific and overlap with a variety of other thoracic conditions. Considering the relatively high incidence of tracheobronchomalacia in patients with dyspnea and other nonspecific respiratory symptoms, we hypothesized that significant numbers of patients with tracheobronchomalacia could be shown by CT pulmonary angiography in a population with clinical suspicion for pulmonary embolism. The purpose of this study was to determine the frequency of tracheomalacia incidentally detected on CT pulmonary angiography in patients with suspected pulmonary embolism.

Materials and Methods

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One hundred sixty-three consecutive patients (73 men and 90 women; mean age, 60 years) with suspected pulmonary embolism underwent CT pulmonary angiography from November 1999 to May 2002. These patients were retrospectively identified using CT records at our institution. All patients were imaged on either single-detector CT (Somatom Plus 4, Siemens Medical Solutions, Erlangen, Germany) or MDCT scanners (LightSpeed, General Electric Medical Systems, Milwaukee, WI) with four or eight detector rows. Gantry rotation times of single detector CT, MDCT with four and eight detector rows are 0.75, 0.8, and 0.5 sec, respectively. The imaging parameters used for each type of scanner are as follows: for single-detector CT, collimation of 3.0 mm with a pitch of 1.5 or 2.0; for MDCT, collimation of 2.5 mm with a pitch of 6.0 in fast mode for four-channel MDCT and collimation of 1.25 mm with a pitch of 13.5 in fast mode for eight-channel MDCT. With these protocols, the chest can be scanned in 28 sec for single-detector CT, 9 sec for four-channel MDCT, and 12 sec for eight-channel MDCT (the longer scanning time for eight-channel MDCT compared with four-channel MDCT reflects the use of the narrower collimation with eight-channel MDCT). All patients were scanned from lung base to apex. During the study, 75–100 mL of ioversol 68% (Optiray 320, 320 mg I/mL, Mallinckrodt Medical, St. Louis, MO) was administered IV with an automated injector (Medrad, Pittsburgh, PA) at a rate of 3.5 mL/sec. Scanning delay was 20–25 sec.

Axial images were reconstructed with intervals as follows: 1.5 mm for single-detector CT, 1.25 mm for four-detector rows, and 0.6 mm for eight-detector rows. The studies were interpreted on a PACS (picture archiving and communication system) (PathSpeed, General Electric Medical Systems). Images were reviewed using combined cine stack with static one-on-one viewing. All images were displayed in both mediastinal (window level, 40 H; window width, 350 H) and lung (window level, –500 H; window width, 1500 H) window settings.

Although patients were instructed to hold their breath during the CT study, many patients were unable to maintain prolonged breath-holds. If patients could not hold their breath during the study, they were instructed to resume quiet breathing. Because our scanning protocol is caudal–cranial, such breathing is usually maximal in the upper and mid chest. Thus, in some patients, the trachea and main bronchi were incidentally scanned during both inspiration and expiration.

For each patient, all images were visually assessed for collapse of the trachea through bronchi by two thoracic radiologists who each had more than 5 years' clinical experience. They assessed the images by consensus. Patients with collapsed trachea on visual analysis of images were recorded as having suspected tracheomalacia. Subsequently, after the initial review of all cases, those patients with suspected tracheomalacia were further analyzed quantitatively by performing cross-sectional area measurement of the tracheal lumen on lung window settings. For quantitative analysis of the degree of collapse, the cross-sectional areas were measured at the site of maximal collapse of the airway and at the closest adjacent region of the trachea without collapse between the levels of thoracic inlet to carina. From these two values, the percentage of luminal narrowing was calculated. We defined tracheomalacia as a 50% or greater decrease in tracheal lumen [1, 14]. Exclusion criteria included extrinsic mass compressing the trachea or bronchi.

Clinical histories were also reviewed retrospectively to identify chief complaints for undergoing CT pulmonary angiography, medical history, and hospital course. Our institutional review board approved our study of the retrospective review of medical records and images but did not require patient informed consent for this retrospective study.

Results

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Thirty-one patients were classified as having suspected tracheomalacia on the basis of visual analysis of the images of all 163 patients. Of these patients, 16 (seven men and nine women; age range 41–95 years; mean age, 72 years) met quantitative criteria for tracheomalacia, defined as 50% or greater decrease in the tracheal lumen (Figs. 1A, 1B, 2A, 2B, 3A, 3B). The percentage of luminal narrowing ranged from 50% to 79% (mean, 60%). Chief complaints for undergoing CT pulmonary angiography were as follows: acute shortness of breath in 13 (81%) of 16, chest pain in three (19%) of 16, lower leg swelling in two (13%) of 16, acute desaturation on monitor in two (13%) of 16, and suspected pulmonary embolism or dissection on echocardiogram in one (6%) of 16. Chest pain and lower leg swelling (in three and two patients, respectively) were accompanied by shortness of breath in all cases. Known causes of tracheomalacia were found in 15 (94%) of 16 patients; prior intubation was confirmed in 12 (75%) patients; and a history of asthma or chronic obstructive pulmonary disease was present in five patients (31%). Smoking or remote smoking history was revealed in 10 patients (63%) and sleep apnea, in two patients (13%). One patient (6%) had a known malignancy involving the chest because of breast cancer. Pulmonary embolism was detected in one patient (6%) with tracheomalacia. The reasons given by clinicians for these clinical symptoms are as follows: congestive heart failure in five patients, chronic obstructive pulmonary disease exacerbation in two patients, pulmonary embolism in one patient, coronary artery disease in one patient, acute respiratory distress syndrome in one patient, oxycodone overdose in one patient, pneumonia in one patient, and unknown in four patients. Because the possible presence of tracheomalacia was not mentioned at the time of primary interpretation of CT pulmonary angiography in all cases, bronchoscopy was not recommended to the referring clinicians.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Tracheomalacia in 88-year-old woman with shortness of breath. Axial CT scan shows normal trachea.

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Tracheomalacia in 88-year-old woman with shortness of breath. Axial CT scan obtained at higher level shows excessive reduction in tracheal lumen, consistent with tracheomalacia.

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Tracheomalacia in 68-year-old man with suspected pulomonary embolism or dissection on sonography. Axial CT scan shows trachea with minimal bowing of posterior wall.

View larger version (112K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Tracheomalacia in 68-year-old man with suspected pulomonary embolism or dissection on sonography. Axial CT scan obtained at level of aortic arch shows excessive reduction in tracheal lumen, consistent with tracheomalacia.

View larger version (128K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —Tracheomalacia in 95-year-old woman with dyspnea. Axial CT scan shows normal trachea.

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —Tracheomalacia in 95-year-old woman with dyspnea. Axial CT scan obtained at higher level than A shows excessive reduction in tracheal lumen, consistent with tracheomalacia.

Fifteen of the 16 patients with tracheomalacia showed no significant tracheal wall thickening. However, one patient exhibited diffuse airway collapse with associated wall thickening that measured greater than 3 mm [15]. The combination of malacia and wall thickening may be associated with relapsing polychondritis, but we are not aware of a known diagnosis of this patient's condition. However, the crescentic form of tracheal collapse was shown in this patient; therefore, tracheomalacia was diagnosed (Fig. 4A, 4B, 4C).

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —Tracheomalacia in 41-year-old man with desaturation seen on monitor after knee surgery. Axial CT scan shows excessive reduction in tracheal lumen, consistent with tracheomalacia.

View larger version (146K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —Tracheomalacia in 41-year-old man with desaturation seen on monitor after knee surgery. Axial CT image obtained at level below carina shows collapsed bronchi bilaterally, consistent with bronchomalacia.

View larger version (123K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —Tracheomalacia in 41-year-old man with desaturation seen on monitor after knee surgery. Axial CT image obtained at level of carina shows thickening of bilateral main bronchi on mediastinal window setting.

Two patients with collapsed bronchi were observed. Because of the technical difficulty in determining the sites of maximal collapse and the airway with maximal cross-sectional area, these patients were not included in the 16 positive cases because there was no evidence of associated collapse of the trachea.

There were no patients in whom an extrinsic mass compressing the trachea was identified. Thus, no patients were excluded on this basis.

Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
The incidence of tracheomalacia on CT studies has not been reported previously and is of significance because this is an important condition that is frequently underdiagnosed. Although CT pulmonary angiography studies are performed at end inspiration, severely dyspneic patients often breathe during the study, providing a dynamic assessment of the airway that provides an opportunity to diagnose this condition. Our study showed the incidence of tracheomalacia to be 10%, which is in the high range of the previous reports. These results confirmed our hypothesis that this condition would be identified in a significant number of patients imaged with CT pulmonary angiography for suspected pulmonary embolism. In terms of clinical symptoms, 13 patients (81%) presented with shortness of breath, whereas chest pain was seen in only three patients (19%) and was always accompanied by shortness of breath. Chest pain and dyspnea are the most frequent symptoms of pulmonary embolism [13]. The possibility of tracheomalacia should be considered as well as pulmonary embolism when patients present with shortness of breath without chest pain.

For clinical interpretation on CT pulmonary angiography, radiologists necessarily place emphasis on pulmonary vasculature rather than on the airways. However, our results emphasize the importance of also carefully inspecting the central airways on CT pulmonary angiography studies. In our study, known causes of tracheomalacia were found in 15 of 16 patients; prior intubation was confirmed in 12 patients; and history of asthma or chronic obstructive pulmonary disease was observed in five patients. Both radiologists and referring physicians should become familiar with the various causes of tracheomalacia and should consider this possibility when evaluating patients with nonspecific symptoms such as shortness of breath. Indeed, the central airways should be reviewed carefully in patients with suspected pulmonary embolism who have known potential causes of tracheomalacia because unrecognized tracheomalacia can cause life-threatening airway obstruction [16].

Our results show that a significant number of tracheomalacia cases might be over-looked in patients with suspected pulmonary embolism. The incidental detection of tracheomalacia on CT pulmonary angiography warrants a dedicated CT airway study to confirm the extent of this disorder. Clinical correlation with patient history, including history of cough, wheezing, shortness of breath, and stridor, is also important; correlative pulmonary function tests may also be helpful because they often show characteristic findings in patients with tracheomalacia [1]. For patients with documented tracheomalacia on a CT airway study, significant clinical symptoms, and characteristic pulmonary function test findings, interventional therapy may be beneficial [17].

The retrospective nature of our study limited our ability to verify the presence of tracheomalacia and to determine its clinical impact. However, on the basis of our experience in imaging patients with tracheomalacia, the degree of airway narrowing that we observed in this series of patients is usually considered clinically significant. Future prospective studies are necessary in this regard.

Although our study showed the incidence of tracheomalacia to be nearly 10% in patients with suspected pulmonary embolism, there were additional limitations. We compared the tracheal lumen at different levels, but because the trachea has a relatively fixed size throughout its intrathoracic course [18], our quantitative definition of tracheomalacia should still be reasonably accurate. Because we did not have any patients with bronchoscopically proven disease, we cannot confirm the accuracy of our findings with a gold standard. For the diagnosis of tracheomalacia on imaging studies, paired inspiratory–expiratory CT or cine evaluation is generally necessary to definitively diagnose tracheomalacia. The most physiologically sensitive indicator of tracheomalacia is thought to be tracheal collapse during coughing on cine evaluation [1]. Alternatively, the rare focal stenosis or diffuse fixed tracheal stenosis could be included in our positive cases. However, tracheal stenosis from intubation is usually a focal coronal narrowing without bowing of the posterior membranous wall. The characteristic morphology of tracheomalacia with the pronounced crescentic anterior bowing of the posterior wall is helpful for confirming the diagnosis [1]. Therefore, it is unlikely that we misdiagnosed tracheal stenosis as tracheomalacia.

Despite these limitations, it is likely that more patients with tracheomalacia could have been detected with supplemental expiratory CT because we had 15 patients with collapsed trachea whose cross-sectional area showed less than 50% luminal narrowing, which did not meet our strict criteria for malacia. Kao et al. [8] reported that the maximal decrease in tracheal caliber was seen before end expiration. Therefore, we believe that patients with tracheomalacia in this study are true-positive cases.

In conclusion, the prevalence of tracheomalacia in patients undergoing CT pulmonary angiography was 10% in this study. The central airways as well as pulmonary vasculature should be reviewed carefully in patients with suspected pulmonary embolism. Paired inspiratory–expiratory CT is recommended if patients present with dyspnea without chest pain and known cause of tracheomalacia, such as prior intubation, chronic obstructive pulmonary disease, or asthma. Future prospective studies of such patients using paired inspiratory–expiratory CT or cine evaluation for tracheomalacia would be helpful for more accurately characterizing the prevalence of this disorder.

Acknowledgments
 
We thank Donna Wolfe for editorial assistance and Ronald J. Kukla for assistance with photography.

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