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AJR 2001; 176:205-210
© American Roentgen Ray Society


Original Report

Tracheobronchomalacia

Dynamic Airway Evaluation with Multidetector CT

R. C. Gilkeson1, Leslie M. Ciancibello1, Rana B. Hejal2, Hugo D. Montenegro2 and Paul Lange2

1 Department of Radiology, University Hospitals of Cleveland, Case Western Reserve University School of Medicine, 11100 Euclid Ave., Cleveland, OH 44106.
2 Division of Pulmonary and Critical Care Medicine, University Hospitals of Cleveland, Cleveland, OH 44106.

Received March 14, 2000; accepted after revision June 20, 2000.

 
Address correspondence to R. C. Gilkeson.


Abstract
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. The objective of our study was to evaluate the role of dynamic inspiratory-expiratory imaging with multidetector CT in patients with suspected tracheobronchomalacia.

CONCLUSION. Multidetector CT with inspiratory-expiratory imaging is a promising method in the evaluation of patients with dynamic airway collapse. In our study, the degree of dynamic collapse correlated well with bronchoscopic results. Dynamic expiratory multidetector CT may offer a feasible alternative to bronchoscopy in patients with suspected tracheobronchomalacia.


Introduction
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Although tracheobronchomalacia is traditionally viewed as a disease of infants and neonates, recent literature suggests that there is greater recognition of this airway disorder by physicians treating adult patients with respiratory symptoms. Several large studies suggest that the incidence of tracheobronchomalacia is 5-10% in patients presenting with pulmonary complaints and that the incidence increases with advanced age [1, 2]. Equally impressive are recent data that dynamic airway collapse is seen in 10-15% of patients referred to a pulmonologist for evaluation of chronic cough [3]. Although historically diagnosed with cine fluoroscopy [4] and more recently with bronchoscopy, several articles have documented the value of dynamic expiratory CT, and particularly of electron beam CT [5], in the diagnosis of tracheobronchomalacia. Early reports suggest that multidetector CT provides greater anatomic accuracy than conventional single-slice CT [6]. In devising this study, we postulated that the decreased imaging time enabled by multidetector CT would allow volumetric evaluation of the central airways during dynamic expiration, a technique shown to be more sensitive in airway obstruction than conventional end expiratory techniques [7]. This report presents our early experience with the use of multidetector CT in the evaluation of patients with suspected tracheobronchomalacia.


Subjects and Methods
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Thirteen patients with suspected tracheobronchomalacia were evaluated by multidetector CT. Clinical histories were reviewed in all patients. The patients included seven males and six females who ranged in age from 14 to 88 years (mean age, 49 years). Three patients had a clinical history of asthma, and one patient was a smoker. Six patients were referred with a history of chronic cough, whereas seven patients presented with unexplained dyspnea. Of the 13 patients, 12 underwent pulmonary function testing including flow-volume loops, and six patients underwent correlative fiberoptic bronchoscopy. Chest radiographs were available for 12 of the 13 patients.

All patients were imaged on a multidetector CT scanner (Picker MX 8000; Marconi Medical Systems, Cleveland, OH). Initial topographic images were obtained first to determine the coverage of the trachea and central bronchi, which generally corresponded to an imaging range of 10-12 cm. CT parameters included a slice thickness of 2.5 mm with a reconstruction interval of 1.25 mm. A single-slice pitch equivalent of 1.5-1.75 was chosen to ensure both thin collimation and adequate coverage of the trachea and central bronchi. With multidetector CT technology, four contiguous 2.5-mm slices are obtained simultaneously. With a gantry rotation speed of 500 msec, the effective z-axis coverage is 3 cm/sec at 2.5-mm collimation, for a single-slice pitch equivalent of 12. Given these parameters, 10-12 cm of the central tracheobronchial tree can be imaged in 4-6 sec, with all slices having an effective thickness of 2.5 mm. Because of an effective 50% reconstruction interval, multiplanar and virtual endoscopic imaging were performed in all patients.

With the use of these imaging parameters, an initial CT scan was obtained during full inspiration; the scan time was 4-6 sec. All patients were scanned in the craniocaudal direction. After the patient was coached for a short period, the onset of the patient's expiratory effort was synchronized with the onset of the expiratory phase of the CT examination. These scans were also obtained in 4-6 sec and were successfully obtained during the expiratory phase in all patients. In patients with suspected laryngomalacia, a second imaging volume was appropriately chosen to cover the upper airways. Images were reviewed at both mediastinal windows (level, 40 H; width, 340 H) and lung parenchymal windows (level, -500 H; width, 1500 H). Inspiratory and dynamic expiratory images were visually inspected for evidence of airway collapse. In the regions of maximal expiratory collapse, cross-sectional area measurements of the tracheobronchial tree were performed using standard software available on the Voxel Q workstation (Marconi Medical Systems). Airway collapse was then classified as 50-75% collapse, 75-100%, and 100% collapse. Axial images were volumetrically reconstructed on a workstation (Voxel Q or OmniPro; Marconi Medical Systems), and virtual bronchoscopic images were acquired using software (Voyager; Marconi Medical Systems). All studies were reviewed with the patient's pulmonologist and were correlated with the bronchoscopic results if bronchoscopy had been performed.


Results
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Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Seven patients presented with unexplained dyspnea, whereas six patients presented with chronic cough. In the group of six patients with chronic cough, sinus disease was excluded on the basis of CT findings and results of a barium swallow, which showed no evidence of gastroesophageal reflux. Asthma was excluded because of negative findings on a methacholine challenge test in five of six patients, whereas one patient who had a history of asthma had a persistent cough despite therapy. Chest radiographs were interpreted as showing normal findings in 10 of the 13 patients, whereas two patients exhibited diffuse intrathoracic tracheal narrowing without evidence of focal parenchymal disease.

Pulmonary function testing with determinations of flow volume was performed before inspiratory-expiratory multidetector CT in 12 of 13 patients. Data are summarized in Table 1. Nine of the 13 patients showed evidence of an obstructive impairment, with values for forced expiratory volume in 1 sec (FEV1) ranging from 23% to 76% of predicted values, whereas three patients had a normal FEV1 value. There was little correlation between the degree of tracheobronchomalacia and the degree of obstruction indicated by the by FEV1 value. Flattening of the expiratory limb of the flow volume curve is a finding highly suggestive of tracheobronchomalacia and was seen in six of 12 patients who underwent pulmonary function tests. Although the three patients with significant tracheobronchomalacia seen on dynamic expiratory CT had a normal FEV1 value, flattening of the expiratory limb of the flow-volume loop was seen in all three patients.


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TABLE 1 Patient Characteristics, Pulmonary Function Test Results, and Imaging Findings

 

All patients showed evidence of airway collapse on inspiratory-dynamic expiratory CT. These data are summarized in Table 1. Of the 13 patients, dynamic expiratory CT showed complete collapse (100%) in three patients, collapse of greater than 75% in seven patients, and 50-75% collapse in three patients. The appearance and extent of tracheobronchomalacia varied significantly. In eight of the 13 patients, involvement of the central tracheobronchial tree was diffuse. In six of these patients, the crescentic form of tracheobronchomalacia (Figs. 1A,1B,2A,2B,3A,3B) was seen, whereas two patients exhibited the "saber sheath" form. Of the four patients exhibiting focal forms of airway collapse, CT showed focal tracheobronchomalacia in two patients and localized bronchomalacia in two patients (Fig. 4A,4B,4C). One patient underwent inspiratory-expiratory CT before and after tracheobronchial stenting, which depicted persistent bronchomalacia and air-trapping distal to the endobronchial stents (Fig. 5A,5B,5C).



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Fig. 1A. 35-year-old woman with history of sarcoidosis and asthma who presented with persistent dyspnea. Pulmonary function tests showed flattening of expiratory limb of flow-volume loop, suggestive of upper airway collapse. Axial CT scan of trachea obtained during inspiration shows normal-caliber trachea.

 


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Fig. 1B. 35-year-old woman with history of sarcoidosis and asthma who presented with persistent dyspnea. Pulmonary function tests showed flattening of expiratory limb of flow-volume loop, suggestive of upper airway collapse. Axial CT scan of trachea obtained during dynamic expiration shows crescentic bowing of posterior membranous trachea consistent with tracheobronchomalacia (arrows).

 


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Fig. 2A. 12-year-old boy with history of recurrent childhood infections and persistent barking cough. Pulmonary function tests showed expiratory flattening of flow-volume loop, suggestive of upper airway collapse. Axial CT scan obtained at level of carina during inspiration shows normal caliber of mainstem bronchi.

 


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Fig. 2B. 12-year-old boy with history of recurrent childhood infections and persistent barking cough. Pulmonary function tests showed expiratory flattening of flow-volume loop, suggestive of upper airway collapse. Axial CT scan obtained at level of carina during dynamic expiration shows marked narrowing (arrows) of trachea and mainstem bronchi.

 


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Fig. 3A. 19-year-old man with Hunter's syndrome, cough, and recurrent dyspnea in whom indirect laryngoscopy (not shown) suggested laryngomalacia with soft-tissue infiltration of upper airways. Because of patient's clinical status, family refused bronchoscopy. Axial CT scan of trachea obtained during expiration shows marked crescentic narrowing of tracheal lumen. Note soft-tissue infiltration of mediastinum and trachea (arrows), consistent with mucopolysaccharide deposition.

 


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Fig. 3B. 19-year-old man with Hunter's syndrome, cough, and recurrent dyspnea in whom indirect laryngoscopy (not shown) suggested laryngomalacia with soft-tissue infiltration of upper airways. Because of patient's clinical status, family refused bronchoscopy. Shaded-surface display image of central airways in posterolateral projection shows diffuse narrowing of trachea and bronchi (arrows).

 


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Fig. 4A. 57-year-old woman with suspected congenital lobar emphysema of right lung. Axial CT scan obtained during dynamic expiration at level of bronchus shows extensive emphysematous change within right lung, with extensive air-trapping and mediastinal shift due to hyperinflated right lung.

 


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Fig. 4B. 57-year-old woman with suspected congenital lobar emphysema of right lung. Virtual bronchoscopic image obtained at level of bronchus intermedius during full inspiration shows mildly narrowed but patent right middle (M) and lower (L) lobe bronchi.

 


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Fig. 4C. 57-year-old woman with suspected congenital lobar emphysema of right lung. Virtual bronchoscopic image obtained during dynamic expiration shows marked narrowing of right middle lobe bronchus (straight arrow) with complete collapse of lower lobe orifice (curved arrow). These findings were not clearly appreciated on axial CT images (not shown) but were confirmed on bronchoscopy.

 


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Fig. 5A. 52-year-old man with idiopathic tracheobronchomalacia and persistent cough after undergoing stenting of mainstem bronchi. Fiberoptic bronchoscopic image obtained before stenting shows marked expiratory collapse of central airways (arrows), which is consistent with tracheobronchomalacia.

 


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Fig. 5B. 52-year-old man with idiopathic tracheobronchomalacia and persistent cough after undergoing stenting of mainstem bronchi. Axial CT scan obtained at level of upper lobe bronchus during inspiration shows persistent narrowing of proximal portion of upper lobe bronchus (arrow) distal to endobronchial stent. Note position of bronchial stents. Position of bronchial stents are identified by arrowheads.

 


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Fig. 5C. 52-year-old man with idiopathic tracheobronchomalacia and persistent cough after undergoing stenting of mainstem bronchi. Axial CT scan obtained during dynamic expiration shows focal collapse of proximal right upper lobe bronchus (straight arrow). Note hyperlucency of right upper lobe, consistent with air-trapping of affected lung (curved arrows). Arrowheads = bronchial stents.

 

Fiberoptic bronchoscopy was performed in six of the 13 patients, with two patients undergoing fiberoptic bronchoscopy before CT, and four patients undergoing bronchoscopy after inspiratory-expiratory CT. Bronchoscopy correlated well with the pattern and distribution of airway collapse seen on CT (Table 1), although dynamic expiratory CT underestimated the degree of collapse in one patient.


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Tracheobronchomalacia is characterized by weakness of the tracheal walls and supporting cartilage. Pathologically, tracheobronchomalacia is thought to result from a weakening of the cartilage and hypotonia of the posterior membranous trachea, with degeneration and atrophy of the longitudinal elastic fibers. Primary tracheobronchomalacia is a congenital weakness that presents at birth, whereas secondary or acquired tracheobronchomalacia is associated with prior intubation or radiation and a history of tumors and chronic obstructive pulmonary disease. Previous surgery and a history of tracheoesophageal fistula are also recognized risk factors for the development of tracheobronchomalacia [8].

The incidence of tracheobronchomalacia has been studied in several bronchoscopic series. In a series of more than 2000 bronchoscopies described by Jokinen et al. [1], 4.5% of the patients were found to have tracheobronchomalacia. Other large series using videobronchoscopy have cited an incidence of 15%, with incidence increasing with advancing patient age [2]. Recent clinical data suggest that in patients presenting with chronic cough, tracheobronchomalacia is the third most common cause after asthma and gastroesophageal reflux [3].

The diagnosis of tracheobronchomalacia is often delayed, particularly in adults. Symptoms are nonspecific; include cough, wheezing, and dyspnea; and are often misinterpreted as asthma [9]. Unfortunately, as witnessed in our patient population, there is poor correlation between the degree of tracheobronchomalacia and the severity of obstruction indicated by results of pulmonary function tests. Although most of our patients showed evidence of obstructive lung disease, two of the most pronounced cases of tracheobronchomalacia had normal FEV1 values, which were measured spirometrically. Although flattening of the flow-volume loop is highly suggestive of upper airway collapse, this finding may be difficult to isolate in the setting of severe obstruction. Indeed, although this finding was helpful in our study population, it was present in only 50% of the cases.

The body of literature defining the criteria for tracheobronchomalacia is significant. In one of the original articles about tracheobronchomalacia, Johnson et al. [4] used fluoroscopy and cine evaluation to define the increasing severity of tracheomalacia. In their study, Johnson et al. found that patients often had associated chronic obstructive pulmonary disease and that the degree of tracheomalacia correlated with the severity of chronic obstructive pulmonary disease [4]. Videobronchoscopic studies of healthy children showed that the ratio of the expiratory-inspiratory cross-sectional area was 0.82. Children with tracheobronchomalacia had a expiratory-inspiratory ratio of 0.35 [10].

Recent literature has focused on the use of dynamic CT to evaluate tracheomalacia. Stern et al. [5] used electron beam CT to evaluate the dynamic range of normal tracheal diameters during inspiration and expiration. Similar to the findings in the bronchoscopy literature, Stern et al. reported that healthy volunteers showed a mean decrease of 35% in the cross-sectional area and that one patient with tracheomalacia showed a decrease of 82%. Ultrafast CT has been successfully used in infants with tracheomalacia associated with tracheoesophageal fistulas [11]. In these studies, dynamic axial images were obtained during inspiration and expiration at preselected levels in the trachea, and the maximal decrease in tracheal caliber was seen late but it was seen before end expiration. Other researchers have studied airway dynamics using electron beam CT and have been particularly successful in the evaluation of patients with obstructive sleep apnea. Reports have described the use of cine MR imaging as a particularly sensitive method in the evaluation of tracheomalacia [12]. The 50- to 100-msec imaging time, which was allowed by cine evaluation, of tracheal collapse during coughing is thought to be the most physiologically sensitive indicator of tracheomalacia.

Although multidetector CT is an exciting new application and was successfully used in our patient population, several limitations in our study design should be recognized. Our cohort was a highly selected patient population without healthy control subjects, and the images were interpreted with the knowledge of the clinical history and pulmonary function tests. Airway physiology studies have shown that during expiration, the small airways generally collapse before the larger airways. Our scanning protocol means that we imaged the upper airway early during expiration, whereas the distal airways were imaged near or at end expiration. These factors suggest that our craniocaudal scanning technique may have underestimated the degree of tracheobronchial collapse in the proximal airway. Although the close correlation of findings in our small population undergoing multidetector CT and bronchoscopy is encouraging, further research to determine the role of multidetector CT in the evaluation of airway dynamics is clearly needed.

Despite these limitations, our preliminary results suggest that the information provided by our technique was important to our referring clinicians. Because of the volumetric nature of scan acquisition, we were able to visualize focal malacic segments that would have potentially been missed if interpreting scans obtained at selected axial levels. Although studies have shown that the addition of virtual bronchoscopic images does not significantly alter diagnosis, these images were preferred by many of our clinicians, and in several cases obviated further bronchoscopic evaluation in patients who refused bronchoscopy or whose clinical status precluded fiberoptic bronchoscopy. Although further studies need to be performed, we suspect future research will establish an important role for multidetector CT in the evaluation of patients with airway disease.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

  1. Jokinen K, Palva T, Sutinen S, Nuutinen J. Acquired tracheobronchomalacia. Ann Clin Res 1997;9:52 -57
  2. Ikeda S, Hanawa T, Konishi T, et al. Diagnosis, incidence, clinicopathology and surgical treatment of acquired tracheobronchomalacia [in Japanese]. Nihon Kyobu Shikkan Gakkai Zasshi 1992;30:1028 -1035[Medline]
  3. Palombini BC, Villanova CA, Araujo E, et al. A pathologenic triad in chronic cough: asthma, post nasal drip, and gastroesophageal reflux disease. Chest 1999;116:279 -284[Abstract/Free Full Text]
  4. Johnson TH, Mikita JJ, Wilson RJ, Feist JH. Acquired tracheomalacia. Radiology 1973;109:577 -580
  5. Stern EJ, Graham CM, Webb WR, Gamsu G. Normal trachea during forced expiration: dynamic CT measurements. Radiology 1993;187:27 -31[Abstract/Free Full Text]
  6. Min J, Shiau M, Leung AN, Rubin G. Quantitation of improved pulmonary arterial visualization with multidetector-row CT. (abstr) Society of Thoracic Radiology Annual Meeting, San Diego, California, March 12-16, 2000: 123
  7. Gotway MB, Golden JA, Lee ES, Reddy GP, Webb WR. Low-dose dynamic expiratory HRCT of the lungs using a spiral CT scanner. (abstr) AJR 2000;174[American Roentgen Ray Society 100th Annual Meeting Program Book suppl]:38 -39
  8. Demajumdar R, Rajesh PB. Have we got the full picture? J Laryngol Otol 1998;112:788 -789[Medline]
  9. Imaizumi H, Kaneko M, Mori K, Yamada K, Asakura K, Tamagawa M. Reversible acquired tracheobronchomalacia of a combined crescent type and saber-sheath type. J Emerg Med 1995;13:43 -49[Medline]
  10. Rozycki HJ, Van Houten ML, Elliott GR. Quantitative assessment of intrathoracic airway collapse in infants and children with tracheobronchomalacia. Ped Pulmonol 1996;21:241 -245
  11. Kao SC, Smith WL, Sato Y, Franken EA Jr, Kimura K, Soper RT. Ultrafast CT of laryngeal and tracheobronchial obstruction in symptomatic postoperative infants with esophageal atresia and tracheoesophageal fistula. AJR 1990;154:345 -350[Abstract/Free Full Text]
  12. Suto Y, Tanabe Y. Evaluation of tracheal collapsibility in patients with tracheomalacia using dynamic MR imaging during coughing. AJR 1998;171:393 -394[Free Full Text]

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