AJR 2000; 175:1537-1543
© American Roentgen Ray Society
Expiratory High-Resolution CT
Diagnostic Value in Diffuse Lung Diseases
Hiroaki Arakawa1,
Hiroshi Niimi1,
Yasuyuki Kurihara1,
Yasuo Nakajima1 and
W. Richard Webb2
1
Department of Radiology, St. Marianna University School of Medicine, 2-16-1
Sugao, Miyamae-Ku, Kawasaki City, 214-0015 Japan.
2
Department of Radiology, M396, University of California, 505 Parnassus Ave.,
San Francisco, CA 94143-0628.
Received March 27, 2000;
accepted after revision May 26, 2000.
Presented at the annual meeting of the Radiological Society of North
America, Chicago, November 1999.
Address correspondence to H. Arakawa.
Introduction
Expiratory high-resolution CT is a powerful adjunct to inspiratory
high-resolution CT in the diagnosis of diffuse lung disease. This technique
reveals dynamic changes in lung attenuation related to the interplay among the
amount of air in the alveoli, the pulmonary interstitium, and the pulmonary
blood volume. It is particularly sensitive for the detection of small airways
obstruction. Combining both inspiratory and expiratory high-resolution CT, we
can better understand the mechanisms of inhomogeneous lung attenuation and
more accurately diagnose diffuse lung diseases.
Technique
Inspiratory high-resolution CT is typically obtained at the end of full
inspiration using 1- to 2-mm collimation and 10-mm scan spacing. Expiratory
high-resolution CT scans are obtained with thin collimation at the end of
forced expiration. Usually, scans are obtained at two to six preselected
levels or in a region of interest, depending on the reason for the study.
Reconstruction with a high-frequency algorithm is mandatory. Because the lung
may show unexpected air-trapping during exhalation, we recommend the routine
use of expiratory scans at preselected levels even in patients with
normal-appearing inspiratory scans.
Expiratory High-Resolution CT
Inhomogeneous lung attenuation is frequently encountered in patients with
diffuse lung disease [1]. It
may represent ground-glass attenuation, mosaic perfusion due to airway
abnormality, or mosaic perfusion due to vascular abnormality. Expiratory scans
may be valuable in distinguishing these causes.
Inspiratory scanning sometimes allows differentiation among the three
common causes of inhomogeneous lung attenuation. For example, smaller vessels
in the lower attenuation areas are seen in mosaic perfusion, regardless of
cause (i.e., air-trapping or vascular obstruction), and the vessels are of
comparable size in both high- and low-attenuation areas in ground-glass
opacity (Figs.
1A,1B
and
2A,2B).
Small vessels in low-attenuation areas are present in 68-94% of cases of
mosaic perfusion [1,
2]. The presence of
bronchiectasis in low-attenuation areas favors mosaic perfusion due to
air-trapping. However, "abnormalities" seen on inspiratory
scanning do not always indicate a disorder and, in our experience, cannot be
relied on for diagnosis [1]
(Fig.
3A,3B).

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Fig. 1A. 43-year-old woman with bronchiolitis obliterans after
bilateral lung transplantation. Inspiratory CT scan shows inhomogeneous lung
attenuation. Vessels in low-attenuation areas appear smaller than those in
high-attenuation areas, suggesting mosaic perfusion as cause of inhomogeneous
lung attenuation.
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Fig. 1B. 43-year-old woman with bronchiolitis obliterans after
bilateral lung transplantation. Expiratory CT scan obtained at slightly lower
level than in A shows contrast between high- and low-attenuation areas
as more conspicuous than in A, confirming air-trapping in
low-attenuation areas. Area of normal lung shows decrease in volume as lung
attenuation increased. Note postoperative metal artifact.
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Fig. 2A. 51-year-old woman with chronic pulmonary thromboembolism and
pulmonary hypertension. On inspiratory CT scan, mosaic perfusion is identified
with disparity in vessel size. Left lung shows higher attenuation and larger
vessels than right lung. Localized area of high attenuation is noted in left
upper lobe (arrows), which may be chronically hyperperfused area.
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Fig. 2B. 51-year-old woman with chronic pulmonary thromboembolism and
pulmonary hypertension. Expiratory CT scan shows normal increase of lung
attenuation and decrease of lung volume in both high- and low-attenuation
areas, with exception of some small areas in left lung (arrows). This
normal increase in attenuation suggests vascular obstruction as cause of
mosaic perfusion. Note that superior segment of lower lobes remains relatively
radiolucent compared with upper lobes, which is normal finding.
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Fig. 3A. 60-year-old man with idiopathic bronchiolitis obliterans.
Inspiratory CT scan shows inhomogeneous opacity with mixed high- and
low-attenuation areas. Vessels in high- and low-attenuation areas appear
similar in size; it is difficult to determine with confidence which areas are
abnormal.
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Fig. 3B. 60-year-old man with idiopathic bronchiolitis obliterans.
Expiratory CT scan shows normal increase in lung attenuation in
high-attenuation areas. Little or no increase in attenuation is noted in
low-attenuation areas, which confirms air-trapping as cause of mosaic
perfusion.
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When expiratory scans are available, mosaic perfusion due to air-trapping
is often confidently discriminated from other causes of inhomogeneous opacity.
The diagnostic value of expiratory scanning is further enhanced by the fact
that normal-appearing lung parenchyma in patients with ground-glass
attenuation or consolidation may in fact prove to represent areas of
air-trapping. This may be seen in cases of bronchopneumonia, hypersensitivity
pneumonitis, sarcoidosis, and concomitant airway obstructive and infiltrative
lung diseases (Fig.
4A,4B).

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Fig. 4A. 56-year-old man with chronic hypersensitivity pneumonitis.
Inspiratory CT scan shows reticular and ground-glass opacities in bilateral
lower lobes. Multiple lower attenuation areas are seen surrounded by areas of
ground-glass opacity (arrows). Vessels appear equal in both high- and
low-attenuation areas.
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Fig. 4B. 56-year-old man with chronic hypersensitivity pneumonitis.
Expiratory CT scan shows areas of air-trapping in low-attenuation areas of
right lung. However, normal increase of lung attenuation is noted in those
areas of left lung. Note honeycombing in right lung.
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Air-Trapping in an Otherwise Normal Lung
Air-trapping may be seen in patients with normal inspiratory scans; it is
reported in about 20% of patients clinically suspected of having chronic
airways disease [3]. The
differential diagnosis of this occurrence includes bronchitis (acute or
chronic) (Fig.
5A,5B),
bronchial asthma, bronchiolitis obliterans (Fig.
6A,6B),
sarcoidosis (Fig.
7A,7B),
hypersensitivity pneumonitis, and smoker's lung
[4]. In patients with these
diseases, pulmonary function test results are intermediate, falling between
those of normal controls and those showing air-trapping and abnormalities on
inspiratory scanning [4]. In
selected cases, the expiratory scans reveal obstructive lung disease in an
early stage, even when the pulmonary function test has normal findings.

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Fig. 5B. 57-year-old woman with chronic bronchitis. However,
expiratory CT scan shows multifocal areas of air-trapping. Pulmonary function
test results showed mild impairment with reduced forced expiratory flow at 50%
and 25% of vital capacity, suggesting small airways obstruction. Forced
expiratory volume in 1 sec was normal.
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Fig. 6A. Bronchiolitis obliterans in 60-year-old woman after right
lung transplantation for idiopathic pulmonary fibrosis. Inspiratory CT scan
shows right lung that appears almost normal. Note postoperative lung
herniation (arrows) through right chest wall.
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Fig. 6B. Bronchiolitis obliterans in 60-year-old woman after right
lung transplantation for idiopathic pulmonary fibrosis. Expiratory CT scan
shows areas of air-trapping suggesting airway obstruction that was not
observed on previous postoperative CT examination.
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Fig. 7B. Biopsy-proven sarcoidosis in 62-year-old woman. Expiratory CT
scan shows extensive air-trapping. Pulmonary function test in this patient
showed mild obstruction with reduced forced expiratory flow at 50% and 25% of
vital capacity.
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Air-Trapping in Diffuse Lung Diseases
Expiratory scanning is sensitive for the detection of air-trapping, which
is a definitive sign of airway obstruction. Air-trapping is a frequent finding
in bronchiectasis and often precedes the development of overt bronchiectasis
(Figs.
8A,8B
and
9A,9B).
These areas of air-trapping correlate well with obstructive functional
deficit. Air-trapping is seen more frequently in areas of mucoid impaction
than in areas without.

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Fig. 8A. Bronchiectasis in 64-year-old man. Inspiratory CT scan shows
area of slightly lower attenuation, associated with fewer vessels and
bronchiectasis, in right upper lobe. Left lung appears normal.
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Fig. 9A. Recently diagnosed diffuse panbronchiolitis in 57-year-old
woman. Inspiratory CT scan shows diffuse small centrilobular nodules with
tree-in-bud appearance. Minimal bronchial dilatation is identified in left
lower lobe.
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Fig. 9B. Recently diagnosed diffuse panbronchiolitis in 57-year-old
woman. Expiratory CT scan shows air-trapping in left and right lower lobes
(arrows). Note that bronchi collapsed after exhalation.
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In bronchiolitis obliterans, expiratory scanning enables early detection of
air-trapping before any other noticeable abnormalities develop on inspiratory
scans and is particularly useful in the early detection of this disease after
lung transplantation. The extent of air-trapping is a good predictor of
obstructive functional deficit.
Air-trapping and airway obstruction are seen not only in airway diseases
but also in interstitial lung diseases, including hypersensitivity pneumonitis
and sarcoidosis [5].
In hypersensitivity pneumonitis, chronic inflammatory infiltrates along
small airways (cellular bronchiolitis) cause bronchiolar narrowing, and
air-trapping is a common finding in many cases
[6] (Fig.
10A,10B).

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Fig. 10A. Summer-type hypersensitivity pneumonitis in 51-year-old man.
Inspiratory CT scan shows inhomogeneous attenuation. Minimal reticulation is
seen in high-attenuation areas suggesting that these areas represent
ground-glass attenuation. Lower attenuation areas appear relatively
normal.
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Fig. 10B. Summer-type hypersensitivity pneumonitis in 51-year-old man.
Expiratory CT scan confirms presence of air-trapping in low-attenuation areas,
even though centrilobular ground-glass nodules representing bronchiolitis are
not obvious on inspiratory scan.
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Sarcoidosis is a disease of the interstitium and usually shows a
restrictive functional deficit. However, small airways obstruction is now
considered an important feature
[7]. Compression of airways by
enlarged lymph nodes, the presence of endobronchial lesions, fibrotic scarring
of endobronchial lesions, and bronchial distortion by peribronchial fibrosis
and small airways abnormalities are considered to cause airway narrowing (Fig.
11A,11B).

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Fig. 11B. 58-year-old woman with sarcoidosis. Expiratory CT scan shows
multifocal areas of air-trapping. Pulmonary function test in this patient
showed moderate obstruction with forced expiratory flow in 1 sec and forced
expiratory vital capacity of 63.7%.
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Limitations of Expiratory High-Resolution CT
The effectiveness of this technique depends on patient cooperation.
Inadequate exhalation results in little increase in lung attenuation; this may
be mistaken for diffuse air-trapping.
Expiratory scanning is considered more sensitive in detecting an
obstructive deficit than the pulmonary function test, but this is not always
true. Many patients who show obstructive functional deficit do not show
air-trapping. This is partly because the pulmonary function test reflects
overall lung function. On the contrary, air-trapping on the CT scan may
reflect a more localized abnormality.
Mosaic perfusion due to vascular obstruction cannot always be discriminated
from that due to air-trapping, even with expiratory scans. Some cases of
pulmonary thromboembolism show evidence of air-trapping in the absence of an
obvious airway abnormality (Fig.
12A,12B,12C).
The mechanism of air-trapping in pulmonary thromboembolism is considered to be
that recent embolus causes release of humoral mediators such as histamine and
serotonin from circulating platelets, which in turn cause generalized and
transient bronchoconstriction and asthmatic wheezing
[8].

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Fig. 12A. Acute pulmonary embolism in 68-year-old woman with previous
history of pulmonary embolism. Helical CT angiogram at mediastinal window
setting shows pulmonary embolism in basal segmental arteries in both
lungs.
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Fig. 12B. Acute pulmonary embolism in 68-year-old woman with previous
history of pulmonary embolism. Inspiratory CT scan shows inhomogeneous lung
attenuation with patchy ground-glass attenuation. Note lobular areas of low
attenuation (arrows).
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Fig. 12C. Acute pulmonary embolism in 68-year-old woman with previous
history of pulmonary embolism. Expiratory high-resolution CT scan shows
multifocal areas of air-trapping both in low-attenuation areas and in regions
appearing normal on inspiratory scan (arrows).
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Conclusion
Expiratory high-resolution CT is useful in the differentiation of causes of
inhomogeneous lung attenuation. Air-trapping in a patient with a
normal-appearing inspiratory scan is a frequent finding. These patients
generally show a mild obstructive functional deficit. Expiratory scans,
revealing not only generalized but also localized air-trapping, may be more
sensitive than the pulmonary function test in the diagnosis of obstructive
lung disease. We recommend routine use of paired inspiratory and expiratory
high-resolution CT in the diagnosis of diffuse lung diseases.
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