Imaging, 22 (2013), 20100062

CHEST IMAGING

Imaging of large and small airway disease

J H REYNOLDS,

MMed Sci, FRCR

and R KOLAWOLE,

MRCP, FRCR

Department of Radiology, Birmingham Heartlands Hospital, Birmingham, UK

Summary
Tracheal abnormalities may present late as symptoms are put down to more

common problems such as asthma.

High-resolution CT is the method of choice for diagnosing bronchiectasis.
Clinical tests are relatively insensitive for the detection of small airway disease and

this has led to a key role for high-resolution CT.

The term mosaic attenuation pattern refers to lung parenchyma that has varying

density on CT. This may be due to technical factors or may be due to airway,
vascular or infiltrative lung disease.

doi: 10.1259/imaging.
20100062
2013 The British Institute of
Radiology

Cite this article as: Reynolds JH, Kolawole R. Imaging of large and small airway disease. Imaging 2013;22:20100062.

Abstract. Imaging plays a key role in the diagnosis of

diseases of the trachea, bronchi and small airways. The
technical advances relating to CT, and in particular the ability
to rapidly acquire a volume of data with multidetector CT, has
revolutionised the investigation of patients with suspected
airway disease. Tracheal abnormalities can be due to intrinsic
or extrinsic causes and may be focal, multifocal or diffuse. CT
is now the investigation of choice for suspected bronchiectasis.
Asthma remains a clinical diagnosis, but advances in CT
technology now allow quantitative assessment of the bronchial
wall and this is providing insights into the nature of airway
remodelling that occurs in asthma. Small airways (for practical
purposes the bronchioles) are numerous and thus clinical tests
are insensitive in detecting disease. This has increased the role
and importance of CT in identifying either of the two main
categories of small airway diseaseconstrictive bronchiolitis
and exudative bronchiolitis.
The airways can be conveniently divided into large
and small, with the large airways comprising the trachea
and bronchi, and the small airways comprising the
bronchioles. For this review that distinction will be used,
although it should be borne in mind that the airways
represent a continuum from the larynx to the bronchioles
and disease processes that affect one section will commonly extend in a proximal or distal manner to involve
another part of the airway.
The development of first high-resolution CT (HRCT)
and subsequently helical and multidetector helical CT
(MDCT) has revolutionised the ability to detect airway
disease.
Address correspondence to: Dr John Reynolds, Department of
Radiology, Birmingham Heartlands Hospital, Bordesley Green East,
Birmingham B9 5SS, UK. E-mail: john.reynolds@heartofengland.
nhs.uk

imaging.birjournals.org

The trachea
Anatomy
The trachea is a midline, cylindrical structure of about
12 cm length in adulthood that commences immediately
below the cricoid cartilage at the level of the C6 vertebral
body and terminates at the carina, at the level of the fifth
thoracic vertebra, where it divides into the right and left
main bronchi. It has an extrathoracic or cervical component that measures approximately 24 cm in length and
a longer intrathoracic component [1, 2].
The trachea is formed from between 16 and 22 cartilaginous C-shaped rings that form the anterior and
lateral walls. These rings are separated and held together by fibroelastic connective tissue and smooth
muscle, which enables slight lengthening and shortening during the changes in respiration and positioning
of the neck. The posterior wall is formed by the posterior tracheal membrane, which also comprises muscle
(the trachealis muscle) and connective tissue [2]. In
cross-section the trachea is more or less circular in
shape, although there may be flattening of the posterior
membrane [3]. In expiration the posterior membrane
tends to bow forwardsthis sign can help establish the
state of inspiration when assessing a CT study of the
thorax [4] (Figure 1).
Ciliated pseudo-stratified columnar epithelium forms
the tracheal mucosa. This produces mucus, which traps
inspired pathogens and particulate matter; the beating
cilia expel the mucous in a cephalad direction. This socalled mucociliary escalator takes inspired particles to
the oropharynx where they may be swallowed or expectorated. This process can be disrupted by pathological
processes within the airway or by iatrogenic intervention
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J H Reynolds and R Kolawole

(a)

(b)

Figure 1. Axial images of the upper trachea at end-inspiration (a) and end-expiration (b). Note the forward bowing of the
posterior membrane at end-expiration. This finding can be helpful in assessing a CT examination for compliance with breathing
instructions.

such as surgery or stent insertion with consequent retention of mucus and risk of lower airway infection [5].
Variations of normal anatomy will sometimes be encountered. For example, the right-sided tracheal bronchus, a right upper lobe bronchus arising directly from
the trachea, has been reported in 0.12.0% of cases [6].

Clinical presentation
The central airways may be affected by a variety of
diseases, producing symptoms such as cough, stridor,
dyspnoea or wheeze [7]. Owing to the relative infrequency
of significant tracheal pathology and the often non-specific
manner of presentation, patients with tracheal disease are
often assumed to have more common abnormalities such
as asthma or chronic obstructive pulmonary disease
(COPD), with consequent delay in diagnosis and appropriate medical or surgical management.

Imaging techniques
The plain chest radiograph remains a convenient firstline investigation for any patient presenting with respiratory symptoms and signs. The air within the trachea gives
good inherent radiographic contrast. Well-penetrated films
(130150 kVp with a grid) may demonstrate focal intrinsic
tracheal narrowing [8]. Extrinsic masses causing airway
compression may also be visualised. Large airway obstructive lesions may be inferred from a lobar collapse.
CT is the most common method of tracheal imaging
after radiography and has been shown to be superior to
conventional radiography in detecting abnormalities of
the major airways [9].
With helical CT, which is now regarded as the key investigative technique for assessing the large airways after
the chest radiograph, a continuous volumetric data set of
the thorax during a single breath-hold is acquired, thus
avoiding problems of slice misregistration and respiratory
movement artefact. Modern workstations allow the production of two-dimensional (2D) or three-dimensional
(3D) reformatted images. Multiplanar reformation (MPR)
allows the data to be displayed in 2D along any axis.
Surface rendering or shaded surface display (SSD), volume
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rendering (VR) and maximum intensity projection (MIP)

or minimum intensity projection (mIP) are common techniques employed in 3D reconstruction [10, 11].
Virtual bronchoscopy (VB) or CT bronchography is
a non-invasive technique whereby the data obtained from
helical (volumetric) scanning are reformulated to provide
an internal rendering of the tracheobronchial walls and
lumen similar to the endoscopic view of the inside of the
airways [12].
End-expiratory acquisitions may aid the detection of
air trapping associated with small airway diseases and
allow assessment of the tracheal wall in suspected tracheomalacia [13].
Although it is still the axial images that are primarily
used for diagnostic purposes, the 2D and 3D reformatted
images offer a number of advantages. These include [14]

better assessment of the craniocaudal extent of disease

the ability to detect subtle airway stenosis
clarification of complex, congenital airway abnormalities
improved planning of surgical or international radiological procedures
better communication between radiologists, clinicians
and patients.

Diseases of the trachea

Disorders of the trachea can result from abnormalities
of the airway wall or from compression from adjacent
structures. Extrinsic compression is commonly caused by
retrosternal thyroid goitres and masses, lymph nodes,
and vascular lesions in the superior mediastinum.

Focal abnormalities of the trachea

Tracheal tumours are rare, accounting for less than 1% of
all tumours [15]. Most are malignant and the majority are
squamous or adenoid cystic carcinomas [16] (Figure 2).
Benign tracheal lesions are usually derived from mesenchymal tissue with hamartoma, leiomyoma, schwannoma
and lipoma being the most frequent [17].
Tuberculosis is rarely a cause of tracheal pathology in the
developed world, but in areas of high prevalence focal
tracheal strictures may occur by extension of an involved
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Imaging of large and small airways disease

Figure 2. An example of an adenoid

cystic carcinoma of the trachea (arrow)
on an axial CT image.

paratracheal lymph node into the adjacent airway wall. A

subsequent inflammatory response may be followed by
fibrosis [17]. Among the commoner forms of tracheal stenosis encountered in clinical practice are those that follow
intubation or tracheostomy (Figure 3). They can occur many
years after the initial insult [18]. With intubation, endotracheal cuff inflation of greater than 30 mmHg will exceed
the mucosal capillary pressure and lead to ischaemia followed by fibrosis [19].
Causes of focal tracheal disease are summarised in
Table 1.

Diffuse abnormalities of the trachea

Wegeners granulomatosis (WG) is a multisytem disorder
particularly affecting respiratory and renal tracts. It most
frequently affects the renal tract and usually manifests
with airway involvement at a later stage. CT can demonstrate tracheal and bronchial stenoses in WG, which may
vary in length from several millimetres to several centimetres (Figure 4). There is mural thickening of the airway, which may be concentric or eccentric [20].
Relapsing polychondritis is a condition causing intermittent cartilage inflammation followed by necrosis and
fibrosis. The upper trachea is the most common site affected, but any site within the cartilaginous airway may
be affected [21] (Figure 5).
Amyloidosis is a multisystem disorder characterised by
extracellular protein deposition. Respiratory tract amyloidosis can occur alone or as part of the systemic form of
the disease. Pulmonary parenchymal involvement is the
most frequent respiratory manifestation of the disease,
but airway involvement can occur, often in combination.
Tracheobronchial involvement with amyloid can be localised or extensive, but may be found incidentally at
bronchoscopy in elderly people [22]. CT demonstrates tracheal or bronchial wall thickening with luminal narrowing,
and linear calcification of the airway walls (Figure 6).
Localised forms of amyloid affecting the airway may appear plaque-like or as tumour-like nodules or masses [23].
Sabre-sheath trachea is a descriptive term for tracheal
deformity whereby there is coronal narrowing of the intrathoracic trachea, with widening of its sagittal diameter;
this can be symmetric or asymmetric in shape. At least
imaging.birjournals.org

95% of patients with sabre-sheath trachea have evidence

of COPD. Sabre-sheath deformity of the trachea can be
identified on chest radiographs and its characteristic
shape and dimensions can be readily appreciated on CT
[24].
Tracheobronchopathia osteochondroplastica (TO) is a rare
benign disorder of the laryngotracheobronchial tree
characterised by the formation of multiple submucosal
mineralised cartilaginous or bony nodules that protrude
into the lumen of the airway. The nodules usually have a
diameter of between 1 and 3 mm but can be much larger,
and are located mainly in the lower third of the trachea
and upper part of the main bronchi. Characteristically the
posterior membranous part of the trachea is spared. The
aetiology is not known. Typically the disorder is asymptomatic, discovered incidentally at post-mortem, bronchoscopy or CT (Figure 7) [25, 26].
Tracheobronchomegaly (MounierKuhn syndrome) is a rare
disorder characterised by marked dilatation of the trachea and main bronchi, and bronchiectasis. Most patients
are men, diagnosed in the third to fifth decades of life.
Imaging reveals a tracheal diameter typically in excess of
3 cm and dilated mainstem bronchi usually larger than
2 cm (Figure 8) [27]. Tracheocoeles (focal dilatation) may be
associated with tracheobronchomegaly or be an isolated
finding. They tend to arise from the right posterior tracheal wall and can contain fluid [21].
Tracheobronchomalacia (TBM) literally means softening
of the trachea and bronchi. The tracheal or bronchial wall
is insufficiently rigid to maintain adequate luminal patency
during the respiratory cycle and collapses with changes in
pressure or lung volume, or when impinged upon by external structures. In primary TBM the cartilaginous support
of the trachea or bronchi is deficient, resulting in abnormal
airway compliance. Secondary TBM is an acquired malacia
resulting from effects upon a potentially or previously
normal airway. These include the effects of prolonged intubation and ventilation or external compression by an
adjacent mass or vessel [28]. TBM is primarily a bronchoscopic diagnosis since the dynamic changes of the
airways during respiration and coughing can be observed directly during endoscopy. Imaging with spiral
CT can support or suggest the diagnosis. Gilkeson and
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J H Reynolds and R Kolawole

and colleagues [30] found dynamic CT elicited a greater

degree of respiratory collapse than end-expiratory CT
in patients with TBM. A more recent study has evaluated the degree of respiratory collapse of the airway in
healthy volunteers and a wide range of forced expiratory
collapse. 37 of 51 patients (73%) exceeded the traditional
diagnostic threshold for TBM of a 50% reduction in crosssectional area, suggesting that this traditional threshold
may need to be revised [31].
The causes of diffuse tracheal abnormalities are summarised in Table 2.

The bronchi
(a)

The trachea bifurcates into right and left main bronchi

at the carina. These large airways retain a similar structure to the trachea, formed by incomplete cartilaginous
rings. The right main bronchus is shorter, wider and
more vertical than the left. The main bronchi divide
into lobar then segmental bronchi. Peripheral airways
without cartilage in their walls are referred to as
bronchioles.

Diseases of the bronchi

(b)
Figure 3. (a) Axial and (b) three-dimensional shaded surface
display images demonstrating a post-intubation stenosis of
the upper trachea (arrow).

colleagues [29] evaluated 13 patients with suspected

tracheobronchomalacia using dynamic multislice CT.
This involved an acquisition at end-inspiration and
another during expiration. They found good correlation
between the bronchoscopic findings and the degree of
dynamic collapse seen on CT. CT during expiration
revealed airway collapse of 50100% in terms of reduction in cross-sectional area [29] (Figure 9). Baroni
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Bronchiectasis
Bronchiectasis is defined as chronic irreversible dilatation of the bronchi [17]. These dilated airways are
a reservoir for infection, leading to the symptoms of purulent sputum and haemoptysis [7].
Common causes of bronchiectasis are summarised in
Table 3. From a morphological aspect, bronchiectasis has
traditionally been subdivided into three categories
cylindrical, varicose and cysticeach reflecting increasing
severity of disease.
Bronchiectasis may manifest on the chest radiograph
as thickened bronchial walls visible as parallel lines or
tram-lines. Bronchiectatic airways seen end-on appear as poorly defined ring shadows. Dilated bronchi
filled with mucus and pus result in tubular opacities.
Cystic bronchiectasis leads to multiple thin-walled ring
shadows, often containing air fluid levels [17]. Mucous
plugging and mucocoele formation can manifest as the
finger-in-glove sign on the plain chest radiograph
(Figure 10).
The HRCT signs of bronchiectasis were first described
by Naidich et al [32] in 1982 and, with minor qualifications, these have stood the test of time [33]. The convenient yardstick for assessing bronchial dilatation when
bronchi are running perpendicular to the plain of scanning is the diameter of the accompanying pulmonary
artery. A bronchus is regarded as being dilated when its
internal diameter is greater than the overall diameter of
the artery [33]. When the bronchial dilatation is marked
the appearance is referred to as the signet ring sign
resembling a ring with a stone attached (Figure 11). When
airways lie parallel to the plane of the scan, dilated airways are recognised by a lack of normal tapering producing a tram-line or flared appearance [33]. A bronchial
lumen being visible in the peripheral 12 cm of the lung is
also an indication of bronchial dilatation [34]. Indirect
signs of bronchial dilatation include bronchial wall
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Imaging of large and small airways disease

Table 1. Causes of focal abnormalities of the trachea
Condition

Key radiological features

Tumours (most are malignant; the commonest types are

squamous cell carcinoma and adenoid cystic carcinoma)
Tuberculosis

Focal masses arising from the tracheal wall with luminal

narrowing
Focal fibrosis leading to bronchial wall distortion and
luminal narrowing
Tracheal wall fibrosis at the site of either a tracheostomy
stoma or the balloon of an endotracheal tube; mucosal
ulceration and inflammation leads to fibrosis and
luminal narrowing
Rare (less than 3% of cases of sarcoidosis), but
granulomata formation leads to nodular thickening of
the tracheal wall, usually in the upper trachea, which
may progress to luminal narrowing
Rare; multifocal tracheal wall inflammation (with
ulceration) leading to radiological wall thickening
Rare; multifocal tracheal wall inflammation and
thickening; typically affects the upper trachea or larynx

Post-intubation or post-tracheostomy

Sarcoidosis

Behets disease
Crohns disease

Figure 4. Coronal multiplanar reformatted image demonstrating bronchial wall thickening and luminal narrowing
caused by Wegeners granulomatosis.

thickening, crowding of bronchi, loss of volume of the

affected lobe and focal air trapping.
The advent of multidetector CT has led to a reevaluation of the technique of examining the airways,

Figure 6. Axial CT image demonstrating thickening of the

walls of the bronchi close to the carina due to amyloidosis.

with the ability to obtain a block of imaging data

covering the entire lungs now easily achieved compared
with the original HRCT technique of obtaining thin
section slices at 10 mm intervals. This technique is less
reliant on patient compliance, with just one breath-hold

Figure 5. Axial CT image demonstrating marked narrowing

of the bronchial lumen at each main bronchus in a case of
relapsing polychondritis.

imaging.birjournals.org

Figure 7. Axial CT image demonstrating submucosal tracheal

nodules in a case of tracheopathia osteochondroplastica.
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J H Reynolds and R Kolawole

(a)

(b)

Figure 8. Axial CT images demonstrating (a) a widened trachea and (b) main bronchi in a case of tracheobronchomegaly.

(a)

(b)

Figure 9. Axial CT images at (a) end-inspiration and (b) end-expiration illustrating collapse of the trachea on expiration in a case
of tracheobronchomalacia secondary to the presence of a vascular ring.

Table 2. Causes of diffuse abnormalities of the trachea

Condition

Key radiological features

Wegeners granulomatosis

Single or multiple stenoses associated with airway wall

thickening, which may be concentric or eccentric;
commonly involves the larynx and subglottic trachea
Destruction of cartilage rings follows inflammation and
necrosis; this leads to luminal narrowing, which is most
common in the upper trachea but can occur anywhere
within the cartilaginous airway
Tracheal or bronchial wall thickening with luminal narrowing
which may be localised or extensive; localised disease may
appear as plaque-like or tumour-like nodules
Tracheal deformity associated with chronic obstructive
pulmonary disease with pronounced narrowing of the
coronal diameter of the trachea
Multiple submucosal mineralised cartilaginous or bony
nodules, typically 13 mm in diameter, in the lower third of
the trachea and bronchi, and usually with sparing of the
posterior membrane of the trachea.
Dilatation of the trachea and main bronchi-tracheal diameter
usually exceeds 3 cm; proximal bronchiectasis
Softening of tracheal and bronchial cartilage leads to luminal
collapse on expiration

Relapsing polychondritis

Amyloidosis

Sabre-sheath trachea

Tracheopathia osteochondroplastica

Tracheobronchomegaly
Tracheobronchomalacia

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Table 3. Causes of bronchiectasis
Cause of bronchiectasis

Examples

Post-infective

Bacterial: including recurrent aspiration

Mycobacteria
Viral: measles, pertussis
Fungi: allergic bronchopulmonary aspergillosis
a-1 antitrypsin
Cystic fibrosis
Kartageners syndrome
Foreign body
Tumour
Stricture
Hypogammaglobulinaemia
Human immunodeficiency virus
In chronic rejection
Graft versus host disease
Rheumatoid disease
Sjorgens syndrome
Ankylosing spondylitis
Relapsing polychondritis
Inflammatory bowel disease
MounierKuhn syndrome
Bronchopulmonary sequestration
Yellow nail syndrome
Sarcoidosis

Inherited cellular defects and mucociliary impairment

Post-obstructive

Immune deficiency
Post-transplant
Autoimmune disease

Miscellaneous

being used as opposed to multiple breath-holds in noncontiguous scanning. The disadvantage is of a higher
ionising radiation dose (helical contiguous CT effective
dose 5.8 mSv vs non-contiguous HRCT effective dose 1.2
mSv) [35]. Chooi et al [36] examined 23 patients and found
that agreement between observers in the diagnosis of
bronchiectasis and emphysema was improved when

Figure 10. Chest radiograph demonstrating the finger in

glove sign on the right side secondary to bronchial mucus
plugging related to allergic bronchopulmonary aspergillosis.

imaging.birjournals.org

multiplanar reformatted (MPR) images were used in conjunction with the axial images. Hill and colleagues [37]
found a 32% increased confidence with contiguous 1 mm
scans compared with conventional HRCT in the diagnosis
of bronchiectasis (p,0.001). Dodd and colleagues [38] also
found contiguous helical multidetector CT superior to
conventional HRCT in terms of showing the presence and
extent of bronchiectasis.
There are a number of potential pitfalls regarding the
HRCT assessment of bronchial dilatation. The division
of a bronchus may not lie in the same scan plane as the
corresponding artery division, and this may make the
bronchus appear larger than either of the two accompanying pulmonary artery branches. Pulmonary artery
calibre does vary due to either physiological or pathological causes, such as hypoxic vasoconstriction, which
can create a false impression of a dilated bronchus [33].
The pattern and distribution of bronchiectasis may in
some cases lead to the suggestion of a specific underlying
cause. However, in many cases, the cause of the bronchiectasis will remain unknown: there is significant overlap in
the appearance of bronchiectasis from known and unknown causes [34]. In a study by Lee et al [39], experienced
observers looked at HRCT examinations from 108 patients
with bronchiectasis of various causes but only established
a correct first choice diagnosis in 45% of cases. In another
study, Reiff and colleagues [40] concluded that CT did
identify features that occurred more frequently with
certain groups of patients with an identifiable cause of
bronchiectasis, but these were not regarded as sufficiently diagnostic.
The patterns of bronchiectasis in a number of conditions are summarised in Table 4.

Asthma and bronchitis

The diagnoses of asthma and bronchitis are based on
clinical and physiological parameters, rather than on
imaging findings. However, the presence of bronchial
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(a)

(b)

Figure 11. Axial (a) and sagittal multiplanar reformatted (b) CT images demonstrating bronchiectasis (arrows). Note the signet
ring sign on the axial image, where the bronchus is wider than its accompanying pulmonary artery.

wall thickening and hyperinflated lungs on plain radiography may suggest either condition [41]. In cases of
clinical deterioration, the plain radiograph plays an important role in identifying causes such as infection or
pneumothorax [42], and HRCT may show features such
as mucus plugging, previously undetected bronchiectasis and air trapping [34]. Advances in scanner and
image-processing technology have led to an interest in

the measurement of the bronchi, including wall thickness and cross-sectional area. In one study, axial reconstructions with orthogonal measurements along the
airways enabled by 3D segmentation methods demonstrated significant changes in bronchial morphometry,
predicting airflow limitation in asthma, and may have
a role in the non-invasive measurement of airway
remodelling [43].

Table 4. Patterns of bronchiectasis in specific conditions

Disease process

Pattern of bronchiectasis

Associated HRCT findings

Non-tuberculous mycobacterial
infection (non-classical variety
without pre-existing lung disease)
Allergic bronchopulmonary
aspergillosis (ABPA)

Bronchiectasis preferentially
involving right middle lobe and
lingula segments
Central, proximal bronchiectasis,
often varicose or cystic with
bronchial wall thickening

Cystic fibrosis

Central, proximal peri-hilar

bronchietcasis with bronchial wall
thickening
Accelerated, aggressive form of
bronchiectasis usually following
pneumonia; bilateral, symmetrical
lower lobe bronchiectasis most
common
Bilateral lower lobe, right middle
lobe and lingula cylindrical
bronchiectasis

Parenchymal nodules clustered

around peripheral airways along
with the tree-in-bud sign
Mucus plugging, mosaic
attenuation, signs of mucus
impaction in bronchioles with the
tree-in-bud sign
Branching or nodular opacities due
to mucus plugging of bronchi and
bronchoioles, mosaic attenuation
Signs of bronchiolitis such as the
tree-in-bud sign

Acquired immune deficiency

syndrome (AIDS)

Hypogammaglobulinaemia

Bronchial wall thickening is

commonly present

HRCT, high-resolution CT.

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Bronchial tumours
The majority of carcinoid tumours (8090%) arise in
lobar, segmental or proximal subsegmental bronchi, where
they appear as polypoidal masses that protrude into the
airway lumen. Carcinoid tumours are low-grade malignant tumours of neuroendocrine origin. The endobronchial location is usually easier to appreciate on CT than
plain radiographs and there is often associated atelectasis
or obstructive pneumonitis [44] (Figure 12).

resulting in the narrowing or complete obliteration of

bronchiolar lumen [13]. In exudative bronchiolitis, the
predominant pathological process is of inflammatory or
cellular infiltrates involving the bronchiolar lumen
and/or wall with minimal or absent fibrosis [46]. A wide
variety of conditions have been described that are associated with an inflammatory or exudative bronchiolitis, such
as infectious bronchiolitis, follicular bronchiolitis, diffuse
panbronchilitis and respiratory bronchiolitis [47].

The small airways

Imaging of small airway disease

The small airways refer to airways that are less than

3 mm in diameter. These largely comprise the bronchioles. Bronchioles contain no cartilage in their walls
and are divided into membranous bronchioles, which are
purely conductive in their function, and respiratory bronchioles, which contain alveoli in their walls and are involved in respiration [45].
Patients with small airway disease will normally suffer
from breathlessness, but the disease is often difficult to
diagnose by traditional pulmonary diagnostic tests. The
branching pattern of the bronchi means that there is
a very large number of small airways or bronchioles, and
thus widespread small airway involvement needs to be
present before patients become symptomatic and pulmonary function tests become abnormal [46].
Bronchiolar disease (bronchiolitis) may originate from
the bronchioles or may be the result of extension of diseases affecting mainly the bronchi (chronic bronchiectasis
and bronchitis) or the lung parenchyma (bronchopneumonia, cryptogenic organising pneumonia) [45]. Various
forms of bronchiolitis may lead to alterations in bronchiolar and surrounding parenchymal structure, which
produce characteristic radiological findings that are
detectable on HRCT [45].

There are two main subgroups of small airway disease,

namely constrictive (or obliterative) bronchiolitis and
exudative (or cellular) bronchiolitis [45].
Constrictive or obliterative bronchiolitis is typified by
submucosal and peribronchiolar irreversible fibrosis,

Chest radiography is relatively insensitive in the diagnosis of small airway disease. Chest radiographs of
patients with constrictive bronchiolitis are usually normal
or may reveal hyperinflated areas with peripheral pruning of pulmonary vessels. Inflammatory bronchiolitis may
occasionally reveal a reticulonodular pattern [48, 49].
HRCT is the principal imaging modality in the assessment of small airway disease.
Normal lobular bronchioles are not visible on HRCT as
they are below the limit of its resolution [45]. The normal
bronchiolar wall is not visible on HRCT, but diseased
bronchioles may become visible [48].
HRCT findings in small airway disease can be subdivided into direct and indirect [48, 50].
Direct signs refer to direct visualisation of diseased
bronchioles. Diseased bronchiolar walls become thickened, the lumina dilated and impacted by mucus, pus or
other cellular material, and there may be surrounding
inflammation. These pathological changes can manifest
on HRCT as 24 mm nodular, branching or linear centrilobular opacities [51] (Figure 13). Branching V and
Y shapes with adjacent nodularity is referred to as the
tree-in-bud sign [52] (Figure 14). This pattern was first
described by Im et al [52] in relation to the endobronchial spread of Mycobacterium tuberculosis. However, it
has subsequently been shown to be a non-specific sign
seen in a variety of bronchiolar diseases such as infectious bronchiolitis, diffuse panbronchiolitis, follicular
bronchiolitis and bronchial disease extending to involve
the bronchioles, such as in cystic fibrosis [51, 53].
Indirect signs of small airway disease include air trapping with overinflation of the lungs, lack of decrease in

(a)

(b)

Pathological classification of small airway disease

Figure 12. (a) Axial and (b) virtual bronchoscopic CT images demonstrating an endobronchial carcinoid tumour.
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Figure 13. Axial CT image demonstrating nodules with

a centrilobular distribution in the right lung in a case of
infectious bronchiolitis.

cross-sectional area of the lung on expiration and a reduction in size and number of pulmonary vessels [13, 54].
Air trapping is a common finding in patients with
bronchiolar disease. The lung parenchyma distal to

Figure 14. Axial CT image demonstrating the tree-in-bud

sign in a case of inflammatory bronchiolitis secondary to
allergic bronchopulmonary aspergillosis (arrow).
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diseased, stenotic airways remain aerated as a result of

collateral air drift or hyperaerated because of a ballvalve effect when the lumen of the involved airway is
not entirely occluded [48]. In parts of the lung where
normal pulmonary architecture is preserved, this is
seen as areas of reduced lung density or attenuation.
The Pendulluft phenomenon has been proposed as a
mechanism for air trapping. Partially obstructed lung
empties more slowly than normal lung during rapid expiration, emphasising attenuation differences [46]. These
areas of air trapping caused by bronchiolar disease are
seen as regional hypoattenuation (areas of lung that remain black/lucent) interspersed with normal areas of
higher density lung [46]. This HRCT pattern is referred to
as mosaic attenuation [5557]. As the attenuation of the
normal lung increases on expiration but lung affected by
air-trapping does not, these lobular or larger areas of air
trapping tend to be accentuated and are more visible on
end-expiratory CT scans [46]. End-expiratory scans will
also confirm that affected parts of the lungs do not
change in cross-sectional area [13, 58] (Figure 15).
In everyday clinical practice, identifying air trapping
on an HRCT study can be challenging. Some patients
have difficulty complying with breath-holding instructions and may not have taken a full inspiration. In this
situation even a normal individual may demonstrate
mosaic attenuation. Mastora et al [59] found in their
study that 31 (53%) out of 59 non-smoking healthy subjects demonstrated isolated lobules of air trapping with
larger (segmental or lobar) areas being found in 5 (8%)
subjects. However, these areas of air trapping are not
usually present on inspiratory scans of normal individuals
and normally do not exceed 25% of the cross-sectional area
on expiratory scan [60]. Hansell [58], in his recent review
of CT findings that lie within the normal range, suggests
that the greater the volume of lung demonstrating apparently decreased attenuation, the greater the likelihood
that it is outside the normal range, and hence likely to be
a manifestation of disease.
Frequency of identification and extent of air trapping
increases with age and smoking. In smokers, the extent of
air trapping is related to the smoking history, independent of present smoking habits [61, 62].
Air trapping is relatively easy to detect when focal
or lobular in distribution. However, in diffuse small
airway disease, the lungs can appear of generally reduced attenuation so that the mosaic pattern is lost; also,
end-expiratory scans may appear virtually identical to
inspiratory sections [58] (Figure 16).
Determination of the inspiratory or expiratory state of
the scan may be aided by assessing the posterior membrane of the trachea, which normally bows forwards on
an expiratory scan [58] (Figure 1).
Mosaic attenuation can be seen in two other pathological processes, namely pulmonary vascular disease
and infiltrative lung diseases. With pulmonary vascular
occlusive disease (such as chronic thromboembolism),
ancillary signs of pulmonary arterial hypertension such
as enlarged pulmonary arteries may be seen. A mosaic
attenuation pattern can be produced by infiltrative lung
disease such as alveolar proteinosis, for example, with
characteristic ground-glass opacity, which may be patchy
in distribution. With infiltrative lung diseases the airway
and pulmonary arteries are likely to be normal. With both
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Imaging of large and small airways disease

(a)

(b)

Figure 15. CT images at (a) end-inspiration and (b) end-expiration showing a mosaic attenuation pattern related to an infective
exacerbation of chronic bronchitis. Note that the low-density portion of lung becomes more prominent on the end-expiration image.

vascular and infiltrative causes of mosaic attenuation

there will not be any accentuation of the low-density
areas on end-expiratory imagesthe low-density areas
will become greyer with both of these causes of
mosaic attenuation [46].

Constrictive (obliterative) bronchiolitis

This is defined pathologically as the concentric, luminal
narrowing of the membranous and respiratory bronchioles due to irreversible submucosal and peribronchiolar
fibrosis.
Numerous causes and predisposing conditions have
been described; the commonest are post-infectious (childhood viral infection with adenovirus, respiratory syncytial
virus, Mycoplasma pneumoniae), connective tissue disorders, transplant recipients (bone marrow, heartlung
transplant), toxic fume inhalation (isocyanates, sulphur
dioxide) and drugs (for instance, patients with connective tissue disease treated with penicillamine) [63].

Figure 16. CT image demonstrating a global reduction in

lung parenchymal density along with a reduced number of
vessels in a case of post-transplant obliterative bronchiolitis.

imaging.birjournals.org

Indirect signs predominate on HRCT since fibrosis of

the bronchiolar wall is the primary abnormality, rather
than peribronchiolar inflammation. Direct signs of small
airway disease tend to be few and are seen in only 10% of
cases [5557]. HRCT features include areas of reduced
lung attenuation, which usually have poorly defined
margins but may sometimes have a sharp geographical
outline (a collection of secondary pulmonary lobules),
giving rise to the mosaic attenuation pattern of lobular air
trapping seen in 66% of cases of obliterative bronchiolitis
[5557]. Other findings on HRCT include reduced number and size of pulmonary vessels due to reactive hypoxic
vasoconstriction of vessels in areas of reduced lung density
and bronchial wall abnormalitiesthe majority of patients
with obliterative bronchiolitis demonstrate peripheral and
central bronchiectasis [64]. There will be a lack of change
of cross-sectional area and density of affected lung on endexpiratory scans [13]. Air-trapping at expiratory HRCT is
the most sensitive sign for detecting obliterative bronchiolitis [53], and its extent provides the best correlation
with indices of physiological impairment [65].
Reduced attenuation can, however, be so severe in
constrictive bronchiolitis as to render it indistinguishable from early-stage panlobular emphysema (due to
a-1 antitrypsin deficiency). The presence of permeative
parenchymal destruction, pulmonary vascular distortion
and basal septal thickening would favour panlobular
emphysema [46, 58].
Very rarely, HRCT findings in patients with obliterative
bronchiolitis can be normal. However, a normal scan should
not preclude diagnosis of this disorder. Routine use of expiratory scans when obliterative bronchiolitis is suspected
clinically should increase sensitivity for diagnosis since airtrapping may not be apparent on inspiratory images.

Exudative bronchiolitis
This is a form of bronchiolitis in which inflammatory
cellular infiltrates characteristically involve the lumen
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J H Reynolds and R Kolawole

Figure 17. Axial CT image demonstrating centrilobular

nodules and the tree-in-bud sign along with cylindrical

bronchiectasis in a case of diffuse panbronchiolitis.

and/or wall of the bronchioles and the surrounding

peribronchiolar tissues. Direct findings predominate on
HRCT with thickened, dilated and impacted bronchioles
visualised as centrilobular, branching, linear opacities
and the tree-in-bud sign [49].
It is a feature of infectious bronchiolitis such as may
be seen with viral and mycoplasma infections. Airway

infection with other organisms such as tuberculosis or

non-tuberculous mycobacteria may also demonstrate a
cellular bronchiolitis pattern on CT, commonly indicating
endobronchial spread of disease.
Diffuse pan-bronchiolitis is an exudative bronchiolitis
that is seen predominantly in the Asian population and in
particular Japanese males [64]. It is characterised by
chronic inflammation of the paranasal sinuses and respiratory bronchioles. HRCT demonstrates small centrilobular nodules, branching linear opacities (tree-in-bud
pattern), bronchiectasis and bronchiolectasis [53]
(Figure 17).
Follicular bronchiolitis is primarily a histopathological
diagnosis defined as lymphoid hyperplasia of bronchusassociated lymphoid tissue. Most cases are associated
with collagen vascular disorders, particularly rheumatoid
arthritis and Sjogrens syndrome, and immunodeficiency
and hypersensitivity reactions. The main findings on
HRCT include small centrilobular nodules, areas of
ground-glass opacification and mild bronchial dilatation
with wall thickening [66].
Respiratory bronchiolitis is a common incidental finding at a histopathological level in most cigarette smokers.
It is characterised by mild chronic inflammation and accumulation of pigmented alveolar macrophages in the
lumina of respiratory bronchioles and adjacent alveoli.

Table 5. Summary of the main radiological and pathological findings in the more common types of bronchiolitis
Classification

Radiological pattern Pathological features

Exudative

Cellular
bronchiolitis

Exudative

Panbronchiolitis

Exudative

Follicular
bronchiolitis

Exudative

Respiratory
bronchiolitis

Constrictive Constrictive/
obliterative
bronchiolitis

Accumulation
of inflammatory
cells (neutrophils),
mucus, exudates
in and adjacent
to the
bronchioles
Severe transmural
infiltrate of
lymphocytes,
plasma cells and
lymphocytes
Hyperplastic
lymphoid
follicles with
reactive germinal
centres adjacent
to bronchioles

HRCT findings

Direct signs: thickened,

dilated impacted
bronchioles visible
as centrilobular,
nodular, branching,
linear opacities,
tree-in-bud pattern
Small centrilobular
nodules, tree-in-bud
pattern,
bronchiectasis,
bronchiolectasis
Centrilobular
and peribronchial
nodules, ground
glass opacification,
mild bronchial
dilatation with
wall thickening
Accumulation of
Poorly defined
pigmented
centrilobular
alveolar
nodules,
macrophages in
tree-in-bud
respiratory
pattern, mild
bronchioles and
fibrosis, centrilobular
adjacent alveoli
emphysema and
air trapping
Circumferential
Geographic or diffuse
thickening of
air trapping, pruning
bronchiolar wall
of pulmonary
with narrowing or
vessels, central and
obliteration
peripheral
of the lumen
bronchiectasis
(indirect signs of
small airway disease

Typical condition

Differential diagnosis

Acute infection:
Hyper-sensitivity
bacterial, viral,
pneumonitis
mycoplasmafungal;
chronic infection:
mycobacterial

Diffuse
panbronchiolitis

Cystic fibrosis,
Immunodeficiency

Rheumatoid
arthritis

Respiratory
bronchiolitis
interstitial lung
disease

Other smoking
related lung
diseases

Cryptogenic
bronchiolitis
obliterans

Pan-lobular
emphysema

HRCT, high-resolution CT.

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Imaging of large and small airways disease

The majority of patients with respiratory bronchiolitis are

asymptomatic. However, in a small proportion, more
extensive changes occur with the development of symptoms of cough, dyspnoea and the full clinicopathological
syndrome of respiratory bronchiolitis-associated interstitial lung disease (RB-ILD). HRCT features in RB-ILD
include ground glass opacification, poorly defined centrilobular nodules and, rarely, tree-in-bud pattern, mild
fibrosis with thickening of the interlobular septa, centrilobular emphysema and areas of reduced lung attenuation due to air trapping [67, 68].
In cryptogenic organising pneumonia the histological
hallmark is the presence of loosely textured myxoid fibroblastic tissue that occludes or partially obstructs the
bronchioles with extension of the process into the alveolar ducts and air spaces. The most frequent finding on
HRCT is unilateral or bilateral air space consolidation,
which has a subpleural or peripheral distribution in over
half of cases [69]. Other findings include ground-glass
attenuation and centrilobular nodular opacities.
The various types of small airway disease together
with the key radiological findings are summarised in
Table 5.

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