Ground glass opacity on CT scanning of the chest: What does it mean?

G round
<strong>Ground</strong> <strong>glass</strong> <strong>opacity</strong> on
CT scanning of the chest:
What does it mean?
<strong>glass</strong> <strong>opacity</strong> (GGO) is
described as a “hazy increased
attenuation of lung, with preservation
of bronchial and vascular margins;
it is caused by partial filling of air
spaces, interstitial thickening, partial
collapse of alveoli, normal expiration, or
increased capillary blood volume.” 1
GGO is a nonspecific finding, and the
differential diagnosis of the many
causes of GGO can be lengthy. An
“ABCs” approach and a “pattern”
approach to the interpretation of GGO
on HRCT scanning of the lungs have
previously been described. 2,3 This paper
provides an abbreviated review of the
physiologic correlates of the HRCT scan
findings of GGO, focusing on infiltrative
processes and their different GGO
patterns of presentation.
GGO can be patchy, resulting in a
mosaic pattern of lung attenuation.
Such a pattern can be seen in infiltrative
lung disease, airway abnormalities
(e.g., asthma, bronchiolitis obliterans),
and chronic pulmonary vascular disease
(e.g., chronic thromboembolic disease).
4 The distinction between these
three entities can be made by observing
the size of the pulmonary vessels in the
area of increased lung attenuation
(increased in both airway disease and
vascular disease, but not in infiltrative
disease), and by examining air trapping
on expiratory scans (indicating airway
disease) (figure 1).
Dr. Collins is in the Department of Radiology
at the University of Wisconsin Hospital
and Clinics, in Madison, WI. Dr.
Stern is in the Department of Radiology
at Harborview Medical Center, University
of Washington in Seattle, WA.
APPLIED RADIOLOGY, December 1998
Jannette Collins, MD and Eric J. Stern, MD
Pitfalls in the interpretation of GGO on
CT scanning
As recognition of GGO is based on a
subjective assessment of lung attenuation,
it is important to understand the
parameters that can interfere with lung
density and make attenuation measurements
unreliable. 5,6 Window widths and
levels that are too narrow can erroneously
create the appearance of GGO
by artificially “blooming” small structures.
In evaluating for GGO, collimation
ideally should be 1.0 to 1.5 mm.
True GGO can not always be visualized
with a thicker collimation because of
volume averaging, and a thicker collimation
sometimes results in a pseudo-GGO
pattern. GGO is therefore best imaged
with high-resolution CT (HRCT).
Lung attenuation normally increases
homogeneously with expiration. This
increased attenuation can obscure
underlying pathologic GGO. Furthermore,
if the expiratory nature of the
A B
examination is not recognized, an erroneous
interpretation of pathologic GGO
can be made.
Cardiac and respiratory motion also
can create pseudo-GGO, which can be
distinguished from pathologic GGO by
recognizing the blurring and double
images of vessels and fissures. GGO in
the gravity dependent portions of the
lungs is often seen as a result of microatelectasis,
which can be differentiated
from pathologic GGO by re-scanning
the area of question with the patient in
the prone position.
Infiltrative processes resulting in GGO
Many patterns of distribution of
ground <strong>glass</strong> <strong>opacity</strong> can be seen on
HRCT of the lungs. It is important to
emphasize that most such disease
processes can and do result in more than
one pattern, often simultaneously; the
patterns change depending upon the
acuity or chronicity of the disease
FIGURE 1. Asthma. Image shows a 20-year-old woman with wheezing and shortness of breath
responsive to bronchodilator treatment. (A) Inspiratory HRCT (1.0 mm collimation) was normal. (B)
Expiratory HRCT (1.0 mm collimation) shows a mosaic pattern of lung attenuation. The areas of
increased attenuation represent normal lung during expiration, while the adjacent abnormal lucent
areas of lung represent air trapping. This pattern of air trapping on expiratory scanning, without
associated abnormalities, is seen most often with obliterative bronchiolitis and asthma (small airways
diseases), and should be differentiated from infiltrative processes where areas of GGO are
seen on the inspiratory images and mosaic attenuation is not accentuated on expiratory imaging.
17

Causes of a diffuse pattern of
GGO on CT scanning
• Acute rejection of lung
transplantation
• Adult respiratory distress syndrome
• Edema
• Extrinsic allergic alveolitis
• Hemorrhage
• Infectious pneumonia
Table 1 FIGURE 2. Acute rejection of lung transplantation.
A 38-year-old man presents with increasing
shortness of breath 3 weeks after
process. We have categorized the etiologies
of GGO according to the most commonly
seen patterns of distribution:
Diffuse pattern of GGO—Disease
processes commonly resulting in a diffuse
pattern of GGO on CT scanning
are listed in table 1. Acute rejection is
common after lung transplantation.
However, differentiating between
reperfusion edema, infection, and rejection
can be difficult both clinically and
radiographically. HRCT is reported to
be 65% sensitive and 85% specific in
making the diagnosis of acute rejection
in the lung transplant population. 7 The
only significant HRCT finding in acute
rejection (seen in 65% of these patients)
is GGO, which is patchy and localized
in mild rejection and widespread in
severe rejection (figure 2). The main
differential diagnosis in this group of
patients is cytomegalovirus pneumonia,
which can have an identical radiographic
appearance.
Adult respiratory distress syndrome
(ARDS) is a form of nonhydrostatic pulmonary
edema, characterized by leaky
capillary membranes. These leaks lead
to extravasation of protein-rich fluid into
the interstitial and alveolar spaces of the
lung. Among the common causes of
ARDS are aspiration, contusion, smoke
inhalation, and sepsis. CT scan findings
of ARDS include bilateral and gravitydependent
lung opacities. 8 Early in the
course of ARDS, all patients demonstrate
GGO on CT, which persists on follow-up
CT in 50% of patients (figure 3). 9
Both cardiogenic and non-cardiogenic
edema occurs when the capacity
of the lung lymphatics to drain capillary
transudate is exceeded. Etiologies
include venous and lymphatic obstruction,
increased capillary permeability,
and hypoproteinemia. 5 HRCT scan find-
bilateral lung transplantation. HRCT (1.0 mm
collimation) shows diffuse bilateral GGO, correlating
with a pathologic diagnosis of severe
acute rejection.
FiGURE 3. Early adult respiratory distress
syndrome (ARDS). A 12-year-old boy with
acute shortness of breath and hypoxemia,
requiring intubation and mechanical ventilation
after receiving chemotherapy for lymphoma.
HRCT (1.0 mm collimation) shows
diffuse bilateral GGO. Pulmonary artery
wedge pressure was normal, and transbronchial
lung biopsy and bronchoalveolar
lavage showed no evidence of infection.
The patient went on to develop severe
ARDS with complications of barotrauma.
ings in patients with hydrostatic pulmonary
edema include areas of GGO,
interlobular septal thickening, peribronchovascular
interstitial thickening,
increased vascular caliber, pleural effusion,
and thickening of fissures. 10
Extrinsic allergic alveolitis, also
called hypersensitivity pneumonitis, is
a complex immunologic reaction by
the lung, primarily to inhaled organic
antigens. The clinical presentation may
be acute, subacute, or chronic. HRCT
scan findings will vary with the stage
of disease. In the acute and subacute
phases, findings include GGO (in
82%), small nodules (55%), a reticular
pattern (36%), and air trapping. 11 GGO
FIGURE 4. Extrinsic allergic alveolitis.
Imaging of a 50-year-old farmer with an
acute onset of increasing shortness of
breath. HRCT (1.0 mm collimation) shows
diffuse bilateral GGO, correlating with the
clinical diagnosis of acute farmer’s lung.
FIGURE 5. Diffuse alveolar hemorrhage. A
45-year-old man presents with increasing
shortness of breath 2 months after bone marrow
transplantation. Helical CT scan (10 mm
collimation) shows diffuse bilateral GGO.
correlates histologically with mononuclear
cell infiltration of the alveolar
walls. 11 The distribution of GGO can be
diffuse, patchy, or centrilobular (figure
4) in this condition.
Pulmonary hemorrhage can be diffuse,
patchy, or focal, depending on the underlying
cause, of which there are many. 12 In
the acute phase, CT scans show consolidation
or GGO (figure 5). In the subacute
phase, CT shows 1- to 3-mm nodules that
are distributed in a uniform fashion, commonly
accompanied by GGO and interlobular
septal thickening. 13
Infectious pneumonia of any cause
(e.g., bacterial, viral, mycobacterial, fungal,
and parasitic) can cause GGO to
appear on HRCT scans. A diffuse pattern
of GGO in the absence of associated CT
scan findings is a characteristic presentation
for cytomegalovirus pneumonia
(CMV) and Pneumocystis carinii pneumonia
(PCP). CMV is the most common
viral pathogen to cause substantial mor-
18 APPLIED RADIOLOGY, December 1998

Causes of a patchy pattern of
GGO on CT scanning
• Acute rejection of lung
transplantation
• Adult respiratory distress syndrome
• Bronchiolitis obliterans organizing
pneumonia (BOOP)
• Bronchioloalveolar cell carcinoma
• Extrinsic allergic alveolitis
• Hemorrhage
• Infectious pneumonia
• Pulmonary alveolar proteinosis
Table 2
bidity and mortality in patients with
AIDS, 14 and is a relatively common complication
in organ transplant recipients. In
patients with AIDS and CMV pneumonia,
CT scanning will show GGO, dense
consolidation, bronchial wall thickening
or bronchiectasis, and interstitial reticulation
without air-space disease (although
GGO may occur in isolation). 15 In organ
transplant recipients with CMV pneumonia,
CT scanning shows small nodules,
consolidation, GGO, and irregular lines
(figure 6). The presence of an isolated
ground <strong>glass</strong> infiltrate without additional
findings in patients with AIDS is highly
suggestive of PCP(figure 7). 16
Patchy GGO patterns—Many of the
causes of a patchy distribution of GGO
on HRCT scanning, listed in table 2,
may also result in a diffuse pattern of
GGO. Pulmonary alveolar proteinosis is
a disease of the lung that results in filling
in of the alveoli by a periodic acid-
Schiff-positive proteinaceous material
that is rich in lipid. 17,18 HRCT scanning
of this disorder shows GGO, with an
overlying branching pattern of white
linear structures forming geometric
shapes and outlining polygonal, triangular,
and square forms. 19,20 This pattern is
often referred to as “crazy paving,” and
is characteristic, but not pathognomonic,
of the diagnosis of alveolar proteinosis
(figure 8). 21 Other processes that
can show a crazy paving pattern at
HRCT scanning include ARDS, lipoid
pneumonia, and PCP.
Focal GGO patterns—There is overlap
between causes of diffuse, patchy,
and focal distributions of GGO (table 3)
with chest CT scanning. When pulmonary
hemorrhage is due to focal neo-
APPLIED RADIOLOGY, December 1998
FIGURE 6. Cytomegalovirus pneumonia.
Imaging of a 42-year-old man with acute
respiratory symptoms 3 months after bone
marrow transplantation. Helical CT scan
(10 mm collimation) shows diffuse bilateral
GGO, areas of septal thickening (straight
arrows), and ill-defined small nodular opacities
(curved arrows). Small bilateral pleural
effusions are present.
FIGURE 7. Pneumocystis carinii pneumonia
in a 39-year-old man with AIDS. HRCT
(1.5 mm collimation) shows patchy bilateral
areas of GGO and a small cystic lesion in
the left upper lobe (arrows).
plasm, trauma, or pulmonary infarction,
a focal pattern of <strong>opacity</strong> results. Certain
infections, such as lobar pneumonia, also
may result in a focal pattern of GGO.
Bronchoalveolar lavage is a procedure
used to diagnose pulmonary diseases and
to identify predictors of prognosis. The
technique involves injection of normal
saline through a bronchoscope that is
generally wedged into the lingular or
middle lobe bronchus. Most, but not all
of the fluid is aspirated back into the
scope and examined for inflammatory
and immune mediator cells and specific
proteins. 22 The residual fluid demonstrates
a segmental or lobar distribution
of GGO on CT scanning, which should
suggest the possibility of recent bronchoalveolar
lavage, especially if the
GGO is observed in the right middle lobe
or lingula. 5
The “halo” pattern of GGO—A
“halo” of GGO occasionally can be seen
around a nodule or focal area of lung
FIGURE 8. Lipoid pneumonia. Image is of a
46-year-old man with a 6-month history of
mild dyspnea and chronic rhinitis, treated
with oily nose drops. HRCT (1.0 mm collimation)
shows bilateral patchy areas of
GGO with a background of intralobular and
interlobular septal thickening, producing the
“crazy paving” pattern first described with
alveolar proteinosis. (Figure courtesy of
Tomas Franquet, MD, Barcelona, Spain.)
FIGURE 9. Invasive aspergillosis. Image is of a
49-year-old man with acute myelogenous
leukemia and fever. Helical CT scan (7.0 mm
collimation) shows a triangular area of consolidation
abutting the peripheral right lung and
involving both the right middle and lower lobes.
This distribution and shape is characteristic of
hemorrhagic infarction caused by the angioinvasive
fungal agent aspergillosis. The surrounding
GGO, creating the “halo sign”,
represents hemorrhage and is highly specific for
early invasive aspergillosis in leukemic patients.
consolidation. Table 4 lists the processes
known to produce the halo sign. It was
first reported as a sign of early invasive
pulmonary aspergillosis in patients with
leukemia. 23 The GGO represents a
Causes of a focal pattern of GGO
on CT scanning
• Bronchiolitis obliterans organizing
pneumonia (BOOP)
• Bronchoalveolar lavage
• Bronchioloalveolar cell carcinoma
• Hemorrhage
• Pulmonary infection
Table 3
19

FIGURE 10. Bronchiolitis obliterans organizing
pneumonia. Image is of a 50-year-old
man with increasing shortness of breath after
bilateral lung transplantation. HRCT (1.0 mm
collimation) shows bilateral patchy areas of
GGO in both a bronchovascular and peripheral
distribution.
FIGURE 11. Contusions. Image is of a 22year-old
man involved in a motor vehicle accident.
Helical CT scan (10 mm collimation)
shows bilateral areas of GGO and consolidation
in a typical peripheral non-segmental distribution.
There are both posterior and anterior
rib fractures adjacent to the sites of contusion.
peripheral ring of hemorrhage or hemorrhagic
infarction surrounding target
lesions of pulmonary aspergillosis (figure
9). Several infectious and noninfectious
causes of the CT halo sign have
since been reported. 24 In most patients,
hemorrhagic nodules can be distinguished
from nonhemorrhagic nodules
by the presence of a halo of GGO.
Another cause of focal GGO, or a
nodule with a surrounding halo of GGO,
is the post-biopsy pseudo nodule. These
pseudo nodules have been described in
Causes of a “halo” pattern of
GGO on CT scanning
• Invasive pulmonary aspergillosis
• Neoplasm, hemorrhagic
• Post-biopsy pseudo nodule
Table 4
FIGURE 12. Desquamative interstitial pneumonitis.
Image is of a 77-year-old man with a
3-month history of increasing shortness of
breath. HRCT (1.5 mm collimation) shows
bilateral areas of GGO and consolidation in a
peripheral distribution without evidence of
honeycombing or traction bronchiectasis.
patients who have undergone lung transplantation
and transbronchial lung
biopsy, 25 but they may be seen in any
patient after lung biopsy.
A peripheral pattern of GGO—
Processes that are known to result in a
peripheral lung distribution of GGO
with HRCT scanning are listed in table
5. This particular distribution pattern
can be very helpful in narrowing the differential
diagnosis, especially when
combined with other clinical data and
associated CT scan findings.
Bronchiolitis obliterans organizing
pneumonia (BOOP) is a disease characterized
histologically by the presence of
granulation tissue plugs within respiratory
bronchioles and alveolar ducts, and
organizing pneumonia extending into
the surrounding alveoli. 26 CT scans
show patchy GGO (in 8 to 75% of
patients), nodules, or areas of consolidation
with a predominantly peripheral
(50% of patients), bilateral, and nonsegmental
distribution (figure 10). 27-29
Collagen vascular diseases are multisystem
disorders characterized by
vascular changes, fibrosis, and inflammation
of connective tissue. Specific
diseases include progressive systemic
sclerosis (scleroderma), systemic lupus
erythematosus, polymyositis/dermatomyositis,
rheumatoid arthritis, and Sjogren’s
syndrome. GGO is seen on CT
scanning in 63 to 100% of these
patients, 30 and is a sign of active inflammation
in the absence of significant honeycombing,
bronchiectasis, or other
signs of lung fibrosis. 31
Pulmonary contusion results from
trauma to the chest wall and lung, with
Causes of a peripheral pattern of
GGO on CT scanning
• Bronchiolitis obliterans organizing
pneumonia (BOOP)
• Collagen vascular disease
• Contusion
• Desquamative interstitial
pneumonitis
• Drug toxicity
• Eosinophilic pneumonia
• Fibrosis
• Sarcoidosis
Table 5
bleeding into the air spaces and lung
interstitium. Generally, the cause is a
compression injury with significant
kinetic energy absorption adjacent to the
site of chest wall injury. The CT scan
appearance of lung contusion is that of
ill-defined areas of GGO, consolidation,
or both, usually with a peripheral, nonanatomic
distribution (figure 11). 32,33
Desquamative interstitial pneumonitis
is characterized by alveolar filling with
macrophages. The HRCT scan findings
consist of GGO with a lower lung zone
(73%) and a peripheral (59%) predominant
distribution (figure 12). Usual interstitial
pneumonitis, or idiopathic
pulmonary fibrosis, results in a similar
distribution of GGO on CT scanning but
typically with more areas of honeycombing
and traction bronchiectasis
(figure 13).
Pulmonary toxicity has been associated
with numerous drugs and a variety
of radiographic and CT patterns. CT
scanning shows nodular areas of GGO
and consolidation, often with a peripheral
distribution. 35,36
Pulmonary eosinophilia occurs with a
variety of conditions or diseases, or can
be idiopathic. Chronic idiopathic
eosinophilic pneumonia is characterized
by multiple dense areas of <strong>opacity</strong> on
chest radiographs and CT scans. In one
study of patients with chronic
eosinophilic pneumonia, the most common
HRCT finding was GGO, usually
adjacent to areas of consolidation, with
a peripheral distribution. 37 Acute idiopathic
eosinophilic pneumonia is characterized
by diffuse GGO and
micronodules on chest radiographs and
CT scans, often in a bronchovascular
distribution. 38
20 APPLIED RADIOLOGY, December 1998

FIGURE 13. Usual interstitial pneumonitis.
Image is of a 78-year-old man with chronic
progressive shortness of breath. HRCT (1.5
mm collimation) shows GGO associated with
honeycombing and traction bronchiectasis in
a peripheral and bibasilar distribution. In this
case, the GGO likely reflects microfibrosis.
Sarcoidosis is a multisystemic disorder
of unknown cause characterized by
the presence of noncaseating granulomatous
inflammation affecting various
sites of the body, with a propensity to
involve the respiratory tract. The most
common HRCT scan findings of pulmonary
sarcoidosis are irregularly thickened
bronchovascular bundles (88%)
and small nodules along vessels (50%). 39
GGO is present in 75% of patients with
sarcoidosis, which corresponds histologically
with many granulomatous lesions,
with or without perigranulomatous
fibrosis, in the interstitium and alveolar
septa around small vessels. Sarcoidosis
can result in a predominantly peripheral
distribution of GGO and/or consolidation,
or a diffuse or patchy pattern of
only GGO (figures 14 and 15).
Bronchovascular and centrilobular
patterns of GGO—Processes that can
result in GGO in a predominantly bronchovascular
distribution include eosinophilic
pneumonia and sarcoidosis. A
predominantly centrilobular distribution
of GGO has been described with both
extrinsic allergic alveolitis and respiratory
bronchiolitis. All reported cases of
respiratory bronchiolitis have occurred in
cigarette smokers. 40-42 In the majority of
these patients, HRCT shows GGO,
which is often extensive, as the predominant
finding. 43 Pigmented macrophages
within respiratory bronchioles and adjacent
alveolar ducts and alveoli lead to the
bronchovascular distribution of GGO.
Conclusion
GGO from infiltrative lung disease is
a nonspecific finding on HRCT scans
APPLIED RADIOLOGY, December 1998
FIGURE 14. Sarcoidosis. Image is of a 33year-old
asymptomatic woman. HRCT (1.0
mm collimation) shows bilateral patchy areas
of GGO. There were no enlarged lymph
nodes or parenchymal nodules.
FIGURE 15. Sarcoidosis. Image is of a 25year-old
asymptomatic man. HRCT (1.0 mm
collimation) shows bilateral patchy areas of
GGO in a bronchovascular distribution, some
showing air bronchograms (arrows).
of the chest, correlating histologically
with partial filling of air spaces,
inflammatory or fibrotic interstitial
thickening, or increased capillary
blood volume. GGO also can represent
mosaic perfusion secondary to chronic
vascular disease, or air trapping from
small airways disease. It is important to
correlate the HRCT pattern of GGO
with clinical history and associated
HRCT scan findings in developing a
differential diagnosis. AR
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