Electronic Supplementary Material
Lung Ultrasound in Critically Ill Patients –
Comparison with Bedside Chest Radiography
Nektaria Xirouchaki*, Eleftherios Magkanas+, Katerina Vaporidi*, Eumorfia
Kondili*, Maria Plataki*, Alexandros Patrianakos++, Evaggelia Akoumianaki*,
and Dimitrios Georgopoulos*
*Department of Intensive Care Medicine, +Department of Radiology and
++
Department o Cardiology, University Hospital, Heraklion,
University of Crete, Greece
Address for correspondence: D. Georgopoulos,
Professor of Medicine,
Director, Department of Intensive Care Medicine,
University Hospital of Heraklion,
University of Crete,
Heraklion, Crete,
Greece
Fax: +30-2810-392636
E-mail: georgop@med.uoc.gr
METHODS
Chest radiography
Anterior chest x-ray was performed with the patients in supine position using
portable X-Ray equipment (Siemens polymobile, Erlangen, Germany). The evaluation
of chest x-ray was performed by an expert radiologist, unaware of the ultrasound and
thoracic computed (CT) findings.
Consolidation, interstitial syndrome (including
alveolar edema), pneumothorax and pleural effusion were defined using the
terminology of the Nomenclature Committee of the Fleishner Society [1]. For regions
location the anatomic landmarks used were lung apex, mid-axillary line, hilar line,
external limit of the rib cage, mediastinal border and diaphragm, as previously
described [2]. The “silhouette sign” was also used to facilitate regions locations.
Multiple Detector Computed Tomography (MDCT)
MDCT was performed with a Siemens Somatom Sensation (16 slices,
Erlangen, Germany). Scans were obtained in the supine position from the apex of the
thorax to the lung bases. Iodine contrast material was administered to differentiate
pleural effusion from alveolar consolidation and atelectasis. The decision to use
iodine contrast material was made by the patient’s attending physician. Assessment
included thin MDCT high Resolution Computed Tomography (MDCT-HRCT) and
spiral MDCT scans. Thin MDCT-HRCT scans consisted of 1mm section thickness at
10 mm intervals, were used to reveal diffuse lung parenchymal involvement as ground
glass opacities, septal or non-septal lines and fibrotic changes (architectural
distortion). MDCT consisted of contiguous axial 7mm thickness slices reconstructed
from the volumetric data of the MDCT software. MDCT scans were evaluated for
mediastinal and pleural pathology (pleural effusion, pneumothorax) and lung lesions
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(consolidation, atelectasis, parenchymal bands), as described by the Nomenclature
Committee of the Fleischner Society [1]. To facilitate comparison between methods
interstitial syndrome was defined as the presence of ground glass opacities, septal or
non-septal lines or fibrotic changes. Similarly consolidation was defined as the
presence of atelectasis, consolidation or parenchymal bands.
Lung regions were
located using the same anatomical landmarks with x-ray. Two individual radiologists,
unaware of lung-ultrasound and CXR findings studied the MDCT-HRCT and MDCT
images and decisions were reached by consensus.
Lung-ultrasound Visualization of the lungs was performed using a
microconvex 5-9 MHz transducer appropriate for transthoracic examination,
(HITACHI EUB 8500). Lung-ultrasound was performed by a single operator (N.X.)
who was unaware of CT and chest radiography information. The operator had more
than 4 years of extensive experience in lung-ultrasound. The main preset parameters
were custom made by the same operator (N.X.). Filters suppressing lung sliding were
by-passed. Access to standardized images (seashore sign, stratosphere sign) was
possible. Lungs were divided in 12 regions as previously described [2]. The anterior
surface of each lung was defined by clavicle, parasternal, anterior axillary line, and
diaphragm and was divided in two areas, upper and lower. The lateral surface was
defined by the anterior and posterior axillary lines and divided in an upper and lower
area. Finally, the posterior lung surface was defined by the posterior axillary and the
paravertebral lines and divided in an upper and lower area. The apex was scanned
from supraclavicular space. Patients were studied in the supine position. The lateral
position was used for posterior lung surface examination.
2
In lung-ultrasound the normal lung displays the “lung sliding” and A lines.
Lung sliding indicates sliding of the visceral pleura against the parietal pleura and A
lines are repetitive horizontal artifacts parallel to the pleural line generated by subpleural air [3, 4]. Consolidation was defined as an iso-echoic tissue-like structure
which is caused by the loss of lung aeration [5, 6]. Power Doppler was used in order
to differentiate tissue like structures (e.g. echoic pleural effusion) from consolidation
[7]. (Video 1). The shred sign, specific for consolidation, was not used. [3] Interstitial
syndrome was defined as presence of multiple B-lines in a specific lung area. B-lines
are well defined hyperechoic comet–tail artifacts, arising from pleural line and
spreading up indefinitely, erasing A lines and moving with the lung sliding when lung
sliding is present [3]. The B-lines 7+1 mm apart indicate thickening of the interlobular
septa (B7-lines) and 3+1mm apart indicate ground glass areas (B3-lines), as
previously described [4, 8, 9]. Pneumothorax was diagnosed when the A-line sign
(only A-lines visible), was associated with the stratosphere sign (complete abolition of
lung sliding). Local lung sliding or B-lines exclude the diagnosis of pneumothorax
[10]. The lung point, (defined as inspiratory synchronized changes from lung patterns
to pneumothorax patterns), was additionally used for diagnosis of pneumothorax [11].
(Fig. S1). Pleural effusion was determined as a hypo echoic or echoic structure,
containing iso-echoic particles or septations in inflammatory pleural diseases. In
addition to power Doppler the quad and sinusoid signs which indicate pleural effusion
regardless of its echogenicity, were also used. [9, 12]. Power Doppler may not be
mandatory for proper lung ultrasound examination, providing that shred sign [3], quad
sign and sinusoid sign [9, 12] are used.
Data analysis
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Each lung region was evaluated and characterized as positive or negative for
each abnormality. A hemithorax was characterized as positive for an abnormality if it
presented at least one positive region, and negative if all regions were negative. The
results of CXR and lung-ultrasound were compared with the corresponding CT scan
results. Sensitivity, specificity, positive and negative predictive values and diagnostic
accuracy were calculated using standard formulas.
RESULTS
Regional analysis
A total of 504 lung regions (12 in each patient) were evaluated by the three
imaging techniques. Sensitivity, specificity, positive and negative predictive values,
and diagnostic accuracy of lung-ultrasound and chest x-ray for each region and for
each pathologic entity are shown in table S1. It is of interest to note that in 23 cases
CT identified in the same region both consolidation and interstitial syndrome, while
lung-ultrasound recognized only one pathology (either consolidation or interstitial
syndrome).
Interstitial syndrome
Interstitial syndrome was identified in 228 regions with CT scan, in 67 regions
with x-ray and in 233 regions with lung-ultrasound. Lung-ultrasound correctly
identified this entity in 204 regions, and x-ray in 49 regions. (Fig. S2, Fig. S3). Lungultrasound had 29 false positive regions and 22 of them (76%) were adjunct to regions
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positive for this abnormality both in lung-ultrasound and CT. It follows that is
discrepancy between lung-ultrasound and CT findings was mainly due to overlap. The
difference in time between the two imaging techniques (up to 4 hours) might be an
additional cause of some false positive cases, (Fig. S4). Lung-ultrasound had 24 false
negative regions. The presence of pneumothorax in some cases (2 patients) interfered
with the ability of lung-ultrasound to evaluate the affected lung regions.
Consolidation
Consolidation was identified in 120 regions with CT scan, in 47 regions with
x-ray and in 149 regions with lung-ultrasound. Lung-ultrasound correctly identified
this entity in 101 regions, and x-ray in 27 regions. (Fig. S5). Lung-ultrasound had 48
false positive regions (Fig. S6) and 38 of them (79%) were adjunct to regions positive
for this abnormality both in lung-ultrasound and CT. (Fig. S7, Fig S8).These results
indicate that overlapping between acoustic windows of adjuncts regions is the main
reason of false positive results with lung-ultrasound. Lung-ultrasound was negative
for consolidation while CT was positive in 19 regions (false negative). The reasons of
this discrepancy was due to 1) the presence of pneumothorax, (Fig S9) 2) the
peripheral location of consolidation (consolidation which did not reach lung surface),
and 3) difficulties to delineate the consolidation borders.
Pleural effusion
Pleural effusion was identified in 116 regions with CT scan, in 64 regions with
x-ray and in 150 regions with lung-ultrasound. Lung-ultrasound correctly identified
this entity in 106 regions, and x-ray in 46 regions. Lung-ultrasound had 10 false
negative regions. All of them were located in upper posterior field. We believe that
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the lateral position of the patient (due to lung-ultrasound protocol we followed) and
the scapula were the main reasons of this discrepancy. Lung-ultrasound was positive
for pleural effusion where CT was negative in 44 regions, mostly in the lower lateral
field, but in 91% of the cases a pleural effusion was identified by both techniques in
the lower posterior region. (Fig. S7, Fig. S8).
Pneumothorax
Pneumothorax was identified in 13 regions with CT, in 2 regions with x-ray
and in 13 regions with lung ultrasonography. Lung-ultrasound correctly identified this
entity in 8 regions. Chest x-ray did not recognize any regions which was positive for
this abnormality with CT (zero true positive). Lung-ultrasound had 5 false negative
and 5 false positive regions for pneumothorax. The 5 false positive regions occurred
in three patients with subcutaneous emphysema due to chest trauma and in two
patients with acute exacerbation of COPD and hyperinflation, (Fig. S10).
The
pneumothoraces missed by lung-ultrasound were small, located in the apex and did
not require any intervention.
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Table S1: Regional analysis
Sensitivity, specificity, positive and negative predictive values and diagnostic
accuracy of chest x-ray (CXR) and lung-ultrasound (LU) compared to thoracic
computed tomography (CT) scan for each abnormality and for each lung region.
PPV; positive predictive value, NPV; negative predictive value, DA; Diagnostic
accuracy. +; positive for the abnormality. -; negative for the abnormality.
Pathology
Consolidation
Pneumothorax
Pleural Effusion
Interstitial
Syndrome
LU/CXR
LU +
LU CXR +
CXR LU +
LU CXR +
CXR –
LU +
LU CXR +
CXR LU +
LU CXR +
CXR -
CT +
CT -
101
19
27
93
8
5
0
13
106
10
46
70
204
24
49
179
48
336
20
363
5
486
2
489
44
344
18
370
29
247
18
258
Sensitivity Specificity
(%)
(%)
PPV
(%)
NPV
(%)
DA
(%)
84
88
68
95
87
23
95
57
80
78
62
99
62
99
98
0
100
0
97
97
91
89
71
97
89
40
95
72
84
83
89
89
88
91
89
21
93
73
59
61
Sensitivity = (TP /TP+FN) ×100.
Specificity = (TN/TN+FP) ×100.
Positive Predictive Value = (TP/TP+FP)×100.
Negative Predictive Value = (TN/TN+FN) ×100.
Diagnostic accuracy= (TP+TN/ TP+TN+FP+FN) ×100
TP; True Positive. TN; True Negative. FP; False Positive. FN; False Negatives
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Legends of Video
Video 1. Power Doppler application in one of the studied patients in order to
differentiate echoic pleural effusion from lower lobe consolidation.
Legends of Figures
Figure S1. Top: The lung point. Lung point was used as guide for pneumothorax
location. Bottom: Stratosphere sign. This is the intercostal space where chest tube was
placed.
Figure S2. Left: MDCT at the upper lung fields revealed ground glass opacities.
Right: Lung-ultrasound examination revealed B3 lines at the upper anterior regions in
a patient suffered from cardiogenic pulmonary oedema.
Figure S3. Top: MDCT at the left middle lung revealed ground glass opacities.
Bottom-right: Lung-ultrasound examination revealed lung rockets at the same region.
Bottom-Left: Multiple B-lines in the left anterior upper region. Images were received
from supraclavicular space.
Figure S4. Lung-ultrasound examination of left lower lateral region revealed B-lines
in a polytrauma patient with chest trauma. CT was negative for the same pathology at
the same region. False positive result.
Figure S5. Left: MDCT after iv contrast material revealed bilateral consolidations
with air bronchogram associated with pleural effusions. Right: Lung-ultrasound
longitudinal scan at the lower lateral regions. The main ultrasound features included
bilateral consolidations with air bronchogram and pleural effusions.
Figure S6. False positive case of lower lobe segmental consolidation. MDCT didn’t
identify the same pathology.
Figure S7. Top: MDCT revealed pleural effusion at the left costophrenic angle and a
small consolidation with air bronchogram. Bottom: Lung-ultrasound longitudinal
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scan at the left base corresponding at the left lower lateral region. The main
ultrasound features included consolidation with air bronchogram and pleural effusion.
Figure S8. Top: MDCT after iv contrast material displayed pleural effusion at the left
posterior region and a small consolidation. Right: Lung-ultrasound longitudinal scan
at the left lower lateral region revealed consolidation and pleural effusion.
Radiological and ultrasound findings were identical at the contrary hemithorax.
Figure S9: Top: MDCT shows pneumothorax and nodular consolidation. Bottom:
Stratosphere sign and lung point. In the lung-ultrasound examination the consolidation
was not observed due to the presence of pneumothorax.
Figure S10: False positive test for pneumothorax in a COPD patient with over
inflation.
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