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Advanced Technologies f or

I m a g i n g an d V i s u a l i z a t i o n
o f t h e Tr a c h e o b ro n c h i a l Tree
From Computed Tomography and MRI to
Virtual Endoscopy
Micheal C. McInnis, MDa,b, Gordon Weisbrod, MDb,c,
Heidi Schmidt, MDb,d,*

KEYWORDS
 Trachea  Computed tomography  MRI  Virtual endoscopy  Dynamic CT  Tracheal stenosis

KEY POINTS
 Virtual endoscopy plays a complementary role to flexible bronchoscopy and has a role to play in
overcoming some inherent limitations of flexible bronchoscopy.
 Because of the significant advances in imaging, computed tomography can now provide accurate
3-dimensional reconstructions of the trachea.
 Imaging of the trachea assists in planning for bronchoscopy and surgical intervention.
 Dynamic expiratory imaging of the trachea is accurate in the diagnosis of tracheomalacia and su-
perior to end-expiratory imaging.
 MRI is useful for imaging of vascular rings and may see increasing use in the pediatric patient pop-
ulation.

HISTORY steeple sign.1,2 Given the early limitations of imag-


ing, bronchoscopy has been long considered the
Imaging of the trachea has undergone a revolution gold standard for evaluation of the airway and is
over the course of Dr Pearson’s career. Before clearly superior to plain radiographic techniques.
computed tomography (CT), imaging of the tra- Other advances followed, such as bronchography,
chea involved assessment by plain radiograph providing further insight into the radiographic
and tomography. Used over decades, these appearance of the airways but remained of limited
limited techniques did identify a few classic signs use until the advent of CT. Since then, there has
of disease, such as the saber-sheath trachea or been a continuous evolution with advances in

Disclosure: The authors have nothing to disclose.


a
Joint Department of Medical Imaging, University Health Network, Mount Sinai Hospital, Women’s College
Hospital, 76 Grenville Street, Room 2248, Toronto, Ontario M5S 1B2, Canada; b Department of Medical Imag-
ing, University of Toronto, 263 McCaul Street, Toronto, ON M5T 1W, Canada; c Joint Department of Medical
thoracic.theclinics.com

Imaging, University Health Network, Mount Sinai Hospital, Women’s College Hospital, Toronto General Hospi-
tal, 200 Elizabeth Street, Toronto, Ontario M5G 2C4, Canada; d Joint Department of Medical Imaging, Univer-
sity Health Network, Mount Sinai Hospital, Women’s College Hospital, 76 Grenville Street, Room 2231,
Toronto, Ontario M5S 1B2, Canada
* Corresponding author. Joint Department of Medical Imaging, Women’s College Hospital, 76 Grenville Street,
Room 2231, Toronto, Ontario M5S 1B2.
E-mail address: Heidi.Schmidt@uhn.ca

Thorac Surg Clin 28 (2018) 127–137


https://doi.org/10.1016/j.thorsurg.2018.01.005
1547-4127/18/Ó 2018 Elsevier Inc. All rights reserved.
128 McInnis et al

computing power facilitating virtual endoscopy performed without contrast. Indications for intra-
(VE) and entirely new methods, such as MRI of venous contrast commonly include evaluation of
the airways. Although bronchoscopy is still tumors or vascular anatomy adjacent the trachea.
regarded as the gold standard, advanced technol- The authors routinely reconstruct their images in
ogies for imaging of the airways have an important 3-mm-thick axial (transverse plane) slices with
role to play where bronchoscopy meets limitations 1-mm or thinner slices available for review when
and in this way plays a complementary role. Some needed. Images are reconstructed in a soft tissue
limitations of bronchoscopy overcome by imaging kernel and an edge-enhanced (lung) kernel. Im-
include the risks related to the invasiveness of ages are interpreted in lung windows to evaluate
the procedure, its inability to visualize structures the lumen (window level, 600 Hounsfield units
external to the airway, as in the case with extrinsic [HU]; window width, 1500 HU). Soft tissue win-
compression, adjacent vasculature, or invasive tu- dows (window level, 40 HU; window width,
mors, as well as the inability to visualize distal to an 350 HU) may be helpful for evaluating the tracheal
obstruction. wall and adjacent fat and identifying calcification.

Multi-planar Reformats
COMPUTED TOMOGRAPHY
Technical Factors and Protocol With the advent of helical CT and isotropic imag-
ing, it is possible to reconstruct images in any
Multi-detector CT (MDCT) imaging of the trachea desired plane, in 2 dimensions. Standard recon-
is preferably performed with 64 slices or greater. structions for the trachea include axial, sagittal,
State-of-the-art CT tracheal imaging optimally and coronal planes; these are routinely performed
uses up to 320 slices that span over a length of on all scans. However, multi-planar reformats
16 cm. Generally, this would cover the length of (MPRs) in oblique planes may be obtained partic-
the trachea and the scan could be completed in ularly to display findings to the best advantage in
the time it takes for the CT gantry to make one a single image along the course of the entire tra-
complete rotation. This rapid rotation time reduces chea. Interpretation is routinely performed using
motion artifact inherent in imaging of the airways. the axial images, correlating with MPRs when
Detector collimation is narrow (1 mm or less) for necessary.
high resolution and facilitating reformat recon-
struction. The authors’ standard protocol uses a Three-Dimensional Volume-Rendered Images
tube current of 50 mA and tube voltage of
120 kV. The gantry rotation time is 0.5 seconds. Volume rendering provides bronchogramlike
Because a 320-slice CT can cover the length of images of the tracheobronchial tree using postpro-
the trachea in one rotation, the scan time will be cessing techniques.3 The use of volume-rendered
equal to the gantry rotation time, thus, achieving images, even on 16-slice CT scanners, has been
very short scan times. Because the scan time is shown to improve interpreter confidence, provide
so short, the technique can be applied to patients additional diagnostic information, and improve
with limited ability to breath-hold, including chil- confidence in the interpretation of congenital
dren and infants. The total radiation dose depends airway abnormalities when compared with axial
on patient factors and technical parameters but is slices alone.4 Volume rendering includes shaded
less than a full chest CT. Low-dose techniques can surface display (SSD) as well as minimum intensity
be applied to adults when warranted and when im- projection (MinIP) and maximum intensity projec-
aging children. tion (MIP) reconstructions. MinIP accentuates the
Patients are instructed to cough before the pro- air spaces and may be useful for demonstrating
cedure to clear secretions and positioned supine the tracheal air column. MIP has limited value in
on the gantry table. Adequate patient instruction routine imaging of the trachea but does accen-
is critical for high-quality imaging with breathing in- tuate nodularity and filling defects.
structions provided in the patients’ preferred lan- SSD requires more operator manipulation but
guage. The scan is performed under breath-hold ultimately provides visually pleasing 3-dimensional
at full inspiration. Imaging of the trachea alone in- (3D) reconstructions of the trachea that are of
cludes a narrow field of view of around 10 cm for particular interest to the consulting physicians,
optimal spatial resolution beginning from above as the presentation more closely mimics surgical
the vocal cords to below the carina. This view anatomy than axial images alone.
excludes most of the lung. The entire chest
Normal Computed Tomography Appearance
may be scanned separately following the tracheal
CT with a wide field of view to visualize the Although the detailed tracheal anatomy is familiar
lungs and small airways. Studies are generally to the thoracic surgeon, there are key points to
From CT and MRI to Virtual Endoscopy 129

review as it pertains to the appearance on cross- in diseases, such as tracheobronchopathia osteo-


sectional imaging. The normal trachea extends chondroplastica (TPO), tracheobronchial amyloid-
over a length of 10 to 12 cm and is demonstrated osis (Fig. 1), and relapsing polychondritis.9,10
over its entire length on coronal or sagittal refor- Calcification can also be seen in masses, such
mats. The width of the adult trachea is generally as hamartomas, chondromas, and carcinoid
2.0 to 2.5 cm with maximal cross-sectional areas tumors.
reported in the literature.5 The normal shape of
the trachea on axial images of an inspiratory CT
Tracheal stenosis
has been described most commonly as round,
MDCT allows for accurate measurement of steno-
oval, or horseshoe-shaped with a flat posterior
sis grade, length, length from vocal cord, and
membrane.5,6 The trachea may have a different
preoperative resection planning. Findings corre-
shape at different levels.6 The shape is attributed
late well with the gold standard of preoperative
to cartilaginous anterior C-shaped rings,
bronchoscopy and intraoperative findings.11,12
numbering 16 to 20 in total, with a flexible thin
Although MDCT is highly accurate in identifying
membranous posterior wall that moves with respi-
airway stenosis, there is a tendency to overesti-
ration. The tracheal wall is normally smooth aside
mate the true grade of stenosis.13 Coronal or obli-
from the undulations of cartilaginous rings. Thick-
que coronal planes may display the entire length of
ening or nodularity may be a sign of disease but
the trachea, including the stenosis, in one image
most commonly relates to retained secretions, a
and is a helpful reference for referring physicians.
common imaging pitfall in evaluating the trachea.7
MinIP reconstructions further accentuate the
contrast between the stenosed airway lumen and
Computed Tomography Applications
the adjacent tracheal wall (Fig. 2).
Calcification The most common cause of tracheal narrowing
CT is useful for identifying airway calcifications. is a saber-sheath trachea as seen in patients
Diffuse calcification is not uncommon in elderly with chronic obstructive pulmonary disease
patients, referred to as senescent calcification, (COPD) characterized by a narrowing of coronal
and more prevalent in women than in men. Diffuse diameter.1 The most common cause of true steno-
calcification sparing the posterior membrane may sis relates to intubation; however, tracheal steno-
also be seen in patients on long-term warfarin sis can also be seen as the sequela of a host
therapy.8 of infectious and inflammatory processes. Apart
Calcification is an important indicator of disease from demonstrating the stenosis, CT may provide
when focal or nodular. Calcifications are seen a clue as to the cause by revealing associated

Fig. 1. (A) Axial CT in a 67-year-old woman with amyloidosis demonstrates a small calcified nodule (arrow) along
the posterior wall of the trachea. (B) MIP image in the same patient accentuates tracheal irregularity seen cranial
to the nodule in (A).
130 McInnis et al

Fig. 2. (A) Axial CT image of a 44-year-old woman demonstrates a postintubation tracheal stenosis. (B) Coronal
MinIP demonstrates the location of the stenosis in relation to the rest of the trachea (arrow). MinIP underesti-
mates the degree of this stenosis.

disease findings. A classic inflammatory example


is Wegener granulomatosis whereby in a small
MDCT series of 10 patients all were found to
have stenosis, 90% of the lesions being subglottic
(Fig. 3).14 Other inflammatory causes of stenosis
demonstrated by CT are not common, such as in-
flammatory bowel disease, Behçet syndrome, and
relapsing polychondritis.15 Infection is reviewed
more completely later, but a classic example of
infection causing stenosis is Mycobacterium
tuberculosis. Other causes of stenosis include
TPO, amyloidosis, external compression from
vascular rings, and neoplasms, as reviewed later.

Airway stents
MDCT is useful in the preoperative evaluation for
airway stenting. In addition to characterizing the
lesions to be stented, MPR assists in planning for
the type of stent to be used.16 MDCT can be
used to determine the location of obstruction,
diameter of the required stent, stent length, and to-
tal number of stents needed.17 Following stent
placement, MDCT can be used in monitoring the
stent for complications. Three-dimensional ren-
derings have been found to be highly accurate in
the identification of stent complications, including
narrowing due to granulation tissue or secretions,
stent migration, fracture, perforation, and invasion
of stent by tumor.18

Benign and malignant airway tumors Fig. 3. Surface shade display in a 25-year-old man
MDCT is complementary to bronchoscopy in the with granulomatosis with polyangiitis demonstrates
evaluation of tumors and is commonly performed a severe stenosis of the left main bronchus (arrow).
From CT and MRI to Virtual Endoscopy 131

as a noninvasive first step. MDCT may be helpful in volume-rendered images in patients with actively
planning for biopsy of the tumor or suspicious caseating disease, disease manifested as circum-
lymph nodes. MDCT not only identifies a tumor ferential wall thickening, irregular luminal narrow-
within the airway but also details the extent of a tu- ing, and findings of mediastinitis.21 When chronic
mor outside the airway within the mediastinum. and fibrotic, the infection manifests as fibrosis
There are limitations in that MDCT is insensitive causing smooth, irregular, or occlusive airway
in the detection of small mucosal-based lesions disease.21
and retained airway secretions can be mistaken Fungal infection can involve the trachea, but
for pathology.7,19 Malignant tumors of the trachea there is limited literature on its appearance. In
include squamous cell carcinoma, adenoid cystic one series of patients with airway-invasive asper-
carcinoma, mucoepidermoid carcinoma, carci- gillosis, disease in the trachea or main stem
noid tumor, metastases (including direct invasion), bronchi had no apparent imaging manifestations
and rare entities, such as primary sarcomas of the on MDCT in their 2 patients.22 Immunosuppressed
trachea and lymphoma (Fig. 4). Benign tumors patients who have undergone a lung transplant
include harmatoma, tracheobronchial papilloma- are a cohort susceptible to aspergillus infection
tosis, lipoma, leiomyoma, neurogenic tumors, an airway at the bronchial anastomosis where
and other rare entities.20 tissue is relatively devascularized. Aspergillus
can manifest as narrowing or stricture causing
Infection clinically relevant obstruction.23
The trachea may be involved by acute or chronic Chronic tracheal infection can be seen in tracheo-
viral, bacterial, and fungal infections. Infections bronchial papillomatosis caused by human papillo-
of the trachea are most commonly viral, such as mavirus. This infection is usually acquired at
parainfluenza or respiratory syncytial virus, mani- birth and manifests as endobronchial papillomas
festing as focal or diffuse thickening (Fig. 5). On causing small endobronchial nodules or diffuse
a frontal plain radiograph, infection of the large air- nodular thickening.20 Rhinoscleroma, a chronic
ways manifests as a steeple sign characterized by granulomatous infection extending from the naso-
narrowing of the subglottic upper airway in pediat- pharynx to occasionally involve the trachea, causes
ric patients with croup producing an inverted V tracheal stenosis; but imaging reports are sparse.15
shape.2
M tuberculosis of the tracheobronchial tree Airway dilation and diverticula
is less common in the era of modern medicine. In CT readily demonstrates congenital tracheobron-
one study using CT with multi-planar and 3D chomegaly (Mounier-Kuhn syndrome), which

Fig. 4. (A) Axial CT in a 77-year-old man with rectal carcinoma demonstrates a new tiny nodule along the poste-
rior wall of the trachea (arrow). (B) Follow-up CT 6 months later demonstrates significant growth (arrow). Bron-
choscopic resection revealed metastatic colon cancer.
132 McInnis et al

Fig. 5. (A) Axial CT in an immunosuppressed 44-year-old man with cough after a bone marrow transplant dem-
onstrates subtle diffuse thickening of the tracheal wall (arrow). (B) Follow-up CT after resolution of symptoms
demonstrates complete resolution of the tracheal thickening. The membranous posterior wall is now barely
perceptible (arrow).

manifests as a dilated trachea greater than 3 cm caution must be used in reconstruction, as the
measured 2 cm above the aortic arch.24 MPRs size of the structures depends on the reconstruc-
are helpful in demonstrating the scalloping and tion settings.27 A trained technologist can perform
outpouchings that may be seen with Mounier- the postprocessing in around 10 minutes.
Kuhn syndrome. Using VE involves no additional radiation. Low-
Paratracheal air cysts are common and usually dose techniques have been used in pediatric pa-
present on the right posterior lateral wall of the tra- tients with foreign body aspiration with excellent
chea at the level of the thoracic inlet as an air-filled or good quality in 91% of the children studied.28
cyst that may or may not have a visible connection VE is usually performed during inspiration; there-
to the tracheal lumen. They are associated with fore, it has a low negative predictive value for
COPD and may be seen in glassblowers.25 tracheomalacia, which is best demonstrated on
MDCT also readily demonstrates congenital dynamic imaging.11
abnormalities of the airways, such as tracheal
bronchus, as well as the relationship of the air- Applications
ways to congenital abnormalities of the central
vasculature.26 Tracheal stenosis
VE is highly sensitive in evaluating airway
VIRTUAL ENDOSCOPY obstruction when compared with the gold
standard of bronchoscopy and intraoperative
In clinical practice, the radiologist is adept at findings.11 Correlation between VE and conven-
reading scans using the axial images. However, tional bronchoscopy of stenosis contour and
as with MPRs, VE provides an opportunity for shape was excellent with stenosis-to-lumen ratio
added information and improved display of the measures found to be within 10%.29 One distinct
findings. With VE, the airway lumen is recon- advantage of VE is the ability to view beyond a
structed taking advantage of the high air-to-soft high-grade obstruction that may not be passed
tissue contrast ratio. The 3D reconstruction that by bronchoscopy (Fig. 6). In fact, some investi-
results provides an endoluminal view of the tra- gators suggest the combination of MDCT with
chea and is navigated using a fly-through to simu- MPR and VE could be considered as a substitute
late conventional bronchoscopy. The tissue color to direct visualization in select scenarios.12
is preset by the software package but can be The use of VE reduces the overestimation of ste-
modified. A threshold value of 500 HU is used nosis compared with axial and MPRs and corre-
to delineate between air and tracheal wall. Some lates more closely in grading stenosis with
From CT and MRI to Virtual Endoscopy 133

Fig. 6. Anterograde (A) and retrograde (B) VE of the postintubation stenosis seen in Fig. 2.

conventional bronchoscopy.13 Compared with Congenital airway abnormalities


conventional axial MDCT, VE was slightly more Low-dose MDCT in the pediatric population can
accurate in evaluating significant stenosis in achieve a 79% to 86% dose reduction while
lung transplant. It does not replace conventional correctly depicting 11 of 12 airway stenoses using
bronchoscopy but is complementary in this pa- VE in combination with axial CT, MPRs, and
tient group.30 SSD.32

Airway tumors
Dynamic Expiratory Imaging
Although VE is excellent in depiction of airway tu-
mors, it suffers from poor sensitivity in detecting Dynamic imaging is useful for evaluating the tra-
mucosal lesions.19 VE is limited compared with vi- chea for narrowing during expiration. The dynamic
sual examination in that it cannot distinguish be- CT protocol involves scanning the trachea at end
tween the color and texture of the tracheal inspiration followed by several acquisitions during
mucosa. Of course, VE cannot sample tissue or dynamic expiration. The authors acquire images
treat lesions but has found a potential role in plan- of the trachea typically at 8 time points during
ning transbronchial needle aspiration of medias- expiration (Fig. 7). The use of dynamic imaging is
tinal and hilar lymph nodes.31 important because the trachea may be narrowest

Fig. 7. Normal dynamic expiratory imaging of the trachea in a 77-year-old man demonstrates the tracheal lumen
at inspiration (top left panel) through to expiration (bottom right panel).
134 McInnis et al

during the process of expiration and not neces- of 54.34% 18.6. Because a tracheal narrowing
sarily at end expiration.33 Dynamic imaging could of more than 50% is commonly seen in normal pa-
be challenging in those with hearing impairment tients during expiration, the study authors suggest
when following breathing instructions is critical.34 caution when using a cutoff of 50% for the diag-
A low-dose technique may be used to limit radia- nosis of tracheomalacia because of the risk of
tion exposure from multiple acquisitions, and overdiagnosis.5 That being the case, dynamic
low-dose techniques have been validated in the expiratory CT is highly sensitive for the diagnosis
literature.35 of tracheomalacia, approaching that of the gold
The inspiratory shape of the trachea will nearly standard of bronchoscopy with only one false
always be normal in tracheomalacia.36 Tracheo- negative in one reported cohort (Fig. 8).34
malacia is, therefore, likely underdiagnosed on
routine end-inspiratory imaging. On expiratory im-
MRI
aging, the trachea shows a wide range of collaps-
Technical Factors and Protocol
ibility, even in the healthy population, because of
the mobile membranous posterior wall.5 The There are many pros and cons to using MRI in im-
tracheal shape on expiratory imaging is variable, aging of the trachea. CT remains superior based
but the frown configuration was seen in only 1 of on its speed and widespread availability. CT is
51 healthy patients and has been more commonly superior in scan time, spatial resolution, and
associated with tracheomalacia.5,36 The degree generally fewer artifacts compared with magnetic
of deformity or bowing has been classified in resonance (MR) examinations. MR also suffers
4 groups as expiratory (1) through expiratory (4 ) from challenges with claustrophobia.
depending on the degree of anterior bowing MRI provides superior soft tissue contrast
of the posterior tracheal membrane, this ter- particularly for delineating planes between the tra-
minology may be applied to patients with chea and adjacent structures. In addition, MRI can
tracheomalacia.36,37 visualize vasculature in the absence of intravenous
The decrease in the anteroposterior and trans- contrast, which is useful when there is renal failure
verse diameter of the trachea on CT correlate or an iodinated contrast allergy. MR is superior to
well with the decrease in cross-sectional area.5,37 CT in that there is no ionizing radiation.
The maximal cross-sectional area of the trachea There are limited reports of normal MR anatomy
in a set of normal patients measured in the upper of the trachea in the literature.38 Overall, there is
trachea was 255.8  61.81 mm2. The minimal limited experience in MR of the trachea, which
cross-sectional area of the upper trachea during relates to the widespread use of CT because
expiration was 112.57  49.32 mm2, a reduction of its speed and availability. There are select

Fig. 8. (A) Inspiratory and (B) expiratory CT in a 59-year-old woman with recurrent barking cough demonstrates
marked tracheal collapse consistent with tracheomalacia.
From CT and MRI to Virtual Endoscopy 135

Fig. 9. (A) T1-weighted image in an 18-year-old man demonstrates a right-sided aortic arch (arrow) with aberrant
left subclavian artery and diverticulum of Kommerell (asterisk). (B) Inspiratory and (C) expiratory axial CT demon-
strates mild narrowing of the trachea during expiration.

applications whereby MR may be helpful and One potential application of MRI is imaging of
serve as a problem-solving tool. the airways in infants using ultrashort echo times
without respiratory gating when breath-hold
Magnetic Resonance Applications cannot be achieved.42
Tumors
Likely the most common indication for evaluating SUMMARY
the trachea by MRI in adults is for assessing the There are evolving imaging modalities available for
extent of a mediastinal or lung tumor. The superior evaluating the trachea. Each imaging modality,
soft tissue contrast allows delineation of fat planes from MDCT, VE, dynamic expiratory imaging,
that may not be visible by CT. This delineation is and MR, provides a diverse array of applications
important in determining the management of to answer important clinical questions. Technol-
tracheal masses. One example of this is with endo- ogy has advanced far beyond the plain radiog-
luminal tumors whereby MR may be able to distin- raphy at the early stages of tracheal imaging in
guish between lesions with a stalk and those with Dr Pearson’s career to see advanced imaging
a broad base as reported in one case of a rare play an increasingly important and complementary
tracheal leiomyoma.39 role to bronchoscopy in evaluating a myriad of
Stenosis diseases.
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