Bedside Lung Ultrasound in The Assessment of Alveolar-Interstitial Syndrome

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American Journal of Emergency Medicine (2006) 24, 689 – 696

www.elsevier.com/locate/ajem

Original Contribution

Bedside lung ultrasound in the assessment of


alveolar-interstitial syndrome
Giovanni Volpicellia,*, Alessandro Mussaa, Giorgio Garofalob, Luciano Cardinaleb,
Giovanna Casolia, Fabio Perottob, Cesare Favab, Mauro Frasciscoa
a
Department of Emergency Medicine, S. Luigi Hospital, Orbassano (TO) 10043, Italy
b
Institute of Radiology, S. Luigi Hospital, Orbassano (TO) 10043, Italy

Received 23 December 2005; revised 2 February 2006; accepted 17 February 2006

Abstract
Objectives: To assess the potential of bedside lung ultrasound to diagnose the radiologic alveolar-
interstitial syndrome (AIS) in patients admitted to an emergency medicine unit and to estimate
the occurrence of ultrasound pattern of diffuse and multiple comet tail artifacts in diseases involving
lung interstitium.
Methods: The ultrasonic feature of multiple and diffuse comet tail artifacts B line was investigated in
each of 300 consecutive patients within 48 hours after admission to our emergency medicine unit.
Sonographic examination was performed at bedside in a supine position. Eight anterolateral ultrasound
chest intercostal scans were obtained for each patient.
Results: The artifact showed a sensitivity of 85.7% and a specificity of 97.7% in recognition of
radiologic AIS. Corresponding figures in the identification of a disease involving lung interstitium were
85.3% and 96.8%.
Conclusion: Comet tail artifact B line is a lung ultrasound sign reasonably accurate for diagnosing AIS
at bedside.
D 2006 Elsevier Inc. All rights reserved.

1. Introduction edema, interstitial pneumonia). Lung ultrasound is a


noninvasive technique potentially useful in detecting AIS
The alveolar-interstitial syndrome (AIS) of the lung at bedside. Sonographic diagnosis of AIS relies on the
includes several heterogeneous conditions with diffuse detection of multiple and diffuse comet tail B lines at lung
involvement of the interstitium and impairment of the scans [1-3]. These are vertical artifacts fanning out from the
alveolocapillary exchange capacity, which leads to more or lung-wall interface and spreading up to the edge of the
less severe respiratory failure. Such conditions are either screen (Fig. 1). They are due to thickened interlobular septa
chronic (eg, pulmonary fibrosis) or acute (eg, acute and extravascular lung water and have been found to be
respiratory distress syndrome (ARDS), acute pulmonary associated with bedside diagnosis of diffuse infiltrative lung
diseases, pulmonary edema, and ARDS in critically ill
* Corresponding author. S.C.D.O. Medicina d’Urgenza, Ospedale San
patients [2]. Other authors found diffuse comet tail artifacts
Luigi da Orbassano, Torino, Italy. Tel.: +39 11 9026603 9026827. in patients with diffuse parenchymal lung disease [4,5].
E-mail address: [email protected] (G. Volpicelli). Jambrik et al [6] showed the usefulness of the artifacts as a

0735-6757/$ – see front matter D 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.ajem.2006.02.013
690 G. Volpicelli et al.

Fig. 1 (Left panel) Normal ultrasound lung scan with horizontal hyperechogenic lines regularly spaced due to reverberation of the lung
wall. Absence of vertical artifacts. (Right panel) Comet tail vertical artifacts fanning out from the lung-wall interface and spreading up to the
edge of the screen (B line) from a patient with acute pulmonary edema.

nonradiologic sign of extravascular lung water. More before admission, and a lung ultrasound was performed
recently, Agricola et al [7] showed that, in cardiac surgery within 48 hours during hospital stay. Five patients (1 with
patients without lung diseases, the number of comet tail mesothelioma, 2 with fibrothorax, and 2 with lung cancer
images provides an estimate of extravascular lung water. who had undergone extended pneumonectomy) were
Detecting lung AIS is of great importance in the excluded because of noninterpretable ultrasound and/or
evaluation of dyspneic patients in the ED. Normally, chest radiograph because of lack of lung-wall interface or
diagnosis of AIS depends on pulmonary high resolution bad quality plain film. Among the remaining 295 patients,
computerized scanning, but in the ED, we are usually 135 were with diagnosed conditions irrelevant to cardio-
dependent upon plain radiography. When chest x-ray is pulmonary changes and 160 had a cardiac and/or pulmonary
performed at bedside, it may be technically deficient. involvement. Out of the latter, for 75, the final clinical
Nevertheless, it remains the only basis for taking therapeutic diagnosis was AIS. Clinical features observed in these AIS
decisions. In the evaluation of dyspneic patients presented to patients were congestive heart failure in 59 patients,
the ED, plain film showed high specificity with low pulmonary fibrosis in 6, interstitial pneumonia in 3, pulmo-
sensitivity in diagnosing congestive heart failure [8]. Lung nary tubercolosis miliaris in 3, multiple bilateral pneumonia
ultrasound is easy to be implemented and potentially useful in 3, and ARDS in 1. Among patients with cardiopulmonary
in detecting AIS at bedside. When performed by the diseases, 84 had a diagnosis other than diffuse AIS. They
attending emergency physicians, it is not time consuming were 32 instances of isolated pneumonia, 12 of pulmonary
and permits real-time assessment of dyspneic patients. cancer, 26 of exacerbation of chronic obstructive pulmonary
The present study aims at assessing the potential of disease (COPD), 6 of pulmonary thromboembolic disease,
bedside lung ultrasound to diagnose AIS in internal 3 of pleurisy, 2 of exacerbation of asthma, 5 of decom-
medicine inpatients and aims at estimating feasibility and pensated cor pulmonale in obstructive or restrictive lung
interobserver agreement in the detection of B line artifacts. disease, and 1 of idiopathic pulmonary hypertension. Three
had more than one diagnosis. In all cases, confirmation of
the diagnosis was based on medical history recorded at
2. Methods presentation, x-ray images, results of tests such as echocar-
diography or left ventriculography, pulmonary function
The study was conducted at San Luigi community examination, response to therapy during the hospital course,
Hospital, Orbassano. It is a university hospital in the west and follow-up at 1 month.
side of Turin. The ED serves a primarily adult population
with a volume of approximately 40,000 visits per year. The 2.2. Chest radiograph
same emergency physician group attending the ED cover Each patient underwent posterior-anterior chest radio-
the 9 beds of the adult emergency medicine unit. graph using a commercially available radiograph machine
2.1. Patients population and a standard technique. Critically ill patients were
submitted to bedside x-ray with a portable unit. The film
During a 10-month period (from June 2004 to March was read by an independent radiologist who was unaware of
2005), 300 consecutive patients admitted to our emergency ultrasound and clinical findings. Diagnoses were grouped
medicine unit were studied (186 men, 114 women, mean into 2 series, with and without radiological evidence of
age 68.4 F 15.2 years [FSD]). Patients gave informed diffuse AIS (presence of diffuse and bilateral alveolar and/or
consent before entering the study. All underwent chest x-ray interstitial opacities, either as confluent, septal, linear or
Lung ultrasound in the assessment of AIS 691

pattern which was considered abnormal had all of the


following 3 features: (1) multiple artifacts per scan (at least
3 artifacts), (2) diffuse positivity in more than one scan per
side, and (3) bilateral positivity. Thus, a positive ultrasound
test for AIS was defined as the presence of multiple, diffuse,
and bilateral artifacts. Patients with positive and negative
ultrasound were, respectively, 71 and 224. Lung ultrasound
examinations were never longer than 3 minutes.

2.4. Thoracic computed tomography


In 18 cases, a thoracic computed tomography (CT) scan
was recorded within 2 days on admission for clinical
reasons not linked to our study protocol. They were 1 basal
CT, 4 high-resolution CT, and 13 contrast-enhanced CT
scans. CT examinations were performed from the apex to
the diaphragm. Images were analyzed by an independent
Fig. 2 The areas of thoracic ultrasonography considered in the radiologist, who was unaware of results of other tests and
study. Areas 1 and 2: upper anterior and lower anterior; areas 3 clinical data. Attention was focused on the presence of
and 4: upper lateral and basal lateral. Each area was the same on
diffuse signs of thickened interlobular septa, ground-glass
right and left side. AAL, anterior axillary line; PAL, posterior
axillary line.
areas, and multiple and diffuse parenchymal thickening.

nodular, distension of pulmonary veins, redistribution to the


apices, and interstitial edema). Seventy-seven patients had a 3. Results
radiologic evidence of AIS. Among the 218 patients without
Among 300 cases studied, ultrasound and chest radio-
radiologic evidence of diffuse AIS, 63 had a radiologic
graph findings could be compared in 295. In only 5 patients
diagnosis of localized and unique lung parenchymal or
could a scan not be compared with plain film. They had
interstitial thickening.
noninterpretable ultrasound (2 patients with pneumonectomy
2.3. Lung ultrasound in lung cancer and 2 patients with fibrothorax, because of
lack of lung-wall interface) or noninterpretable radiograph (1
A GS 50 portable unit (Siemens, Germany), equipped patient with mesothelioma, because of technically deficient
with a convex 3.5-MHz transducer, was used. The image). In the 24 randomly selected patients who performed
investigator was unaware of the result of the chest double ultrasound examination, we obtained 183 concordant
radiogram and clinical data of the patient. Five specifically and 9 discordant scan diagnoses, with an interobserver
trained investigators (3 emergency physicians and 2 radiol- variability on interpretation of the single scan of 4.9%.
ogists) performed the bedside lung ultrasound examinations.
These consist bilateral scanning of the anterior and lateral 3.1. Ultrasound versus chest x-ray
chest wall and were performed with patients in supine or
The association between the presence of the artifacts and
near-to-supine position. The correct scan was intercostal
radiologic findings was investigated (Table 1). When
with the maximum extension of the visible pleural line. The
considering all ultrasounds with multiple and diffuse B
chest wall was divided into 8 areas, and 1 scan for each area
lines (at least 2 positive scans on each side) as positive for
was obtained. The areas were 2 anterior and 2 lateral per
side (Fig. 2). The anterior chest wall was delineated from the
sternum to the anterior axillary line and was subdivided into Table 1 Agreement between sonographic pattern of AIS and
upper and lower halves (approximately from clavicle to the radiologic findings
second-third intercostal spaces and from the third space to Findings at x-ray Sonographic findings Total
diaphragm). The lateral zone was delineated from the
N1 Positive scan Negative
anterior to the posterior axillary line and was subdivided
per side ultrasound
into upper and basal halves. Each image was recorded on a
CD-ROM. A random set of 24 examinations were Diffuse AIS 66 11 77
Localized lung 3 60 63
performed twice by 2 independent observers among the
lesion and
5 mentioned above to assess interobserver variability. Thus,
negative AIS
the 295 patients produced a total of 2552 scans. The Negative 2 153 155
elementary image analyzed was the comet tail artifact chest x-ray
fanning out from the lung-wall interface and spreading up Total 71 224 295
to the edge of the screen, previously named B line [3]. The
692 G. Volpicelli et al.

AIS, this sign had a sensitivity of 85.7% and a specificity of


97.7% for diagnosing radiologic AIS, with a positive
predictive value of 93.0% and a negative predictive value
of 95.1%. Among the 59 patients with congestive heart
failure, 49 had a positive ultrasound, 55 had a positive
radiograph, and 48 had a concordant positive chest x-ray
and ultrasound (Fig. 3). Sixteen discordant cases were noted
(11 false negative and 5 false positive). False-negative cases
include 8 acute left heart failure, 2 exacerbation of COPD,
and 1 pneumonia. False-positive cases include 1 rheumatoid
arthritis, 2 right-sided pneumonia, 1 congestive heart failure,
and 1 fever in aplastic anemia.

3.2. Ultrasound versus clinical outcome


Using the same criteria, the agreement between the
presence of the artifacts and the clinical diagnosis at
discharge was also estimated (Table 2). Lung ultrasound
with diffuse B lines had a sensitivity of 85.3% and a
specificity of 96.8% for diagnosing a disease with alveolar-
interstitial involvement, with a positive predictive value of
90.1% and a negative predictive value of 95.1%. Eighteen
discordant cases were noted. Eleven cases were false
negative and 7 were false positive. False-negative cases
include 10 acute left cardiac failure (7 with positive and
3 with negative chest x-ray) and 1 multiple and diffuse
bilateral pneumonia. False positives include 4 right pneu-
monia (3 basal, 1 apical), 1 lung cancer, 1 rheumatoid
arthritis, and 1 fever in aplastic anemia.

3.3. Ultrasound versus computed tomography


All the 18 CT scans corresponded to ultrasound. Five
patients had AIS on CT, and all of them exhibited diffuse
anterolateral artifacts. They were acute pulmonary edema
(n = 3) and interstitial pneumonia (n = 2). In these cases, the
CT showed diffuse thickened interlobular septa and/or
diffuse and bilateral ground-glass areas all over the anterior
and lateral surface of the lung (Figs. 4 and 5). The other
13 CT scans did not show diffuse AIS, and all these patients
had negative ultrasound. Diagnosis of these were isolated
pneumonia (n = 3), acute pericarditis (n = 1), lung cancer
(n = 4), renal hematoma (n = 1), exacerbation of COPD
(n = 2), and traumatic pleural effusion (n = 1).

Table 2 Comparison between sonographic diagnoses of AIS


and clinical outcomes
Positive clinical Negative clinical Total
diagnosis of AIS diagnosis of AIS
Positive 64 7 71
sonographic
AIS
Fig. 3 Acute pulmonary edema. (Upper panel) Ultrasound Negative 11 213 224
pattern positive for AIS: comet tail artifacts are multiple (at least sonographic
3) in each scan and diffuse in all the 8 anterior and lateral scans AIS
(4 per side). (Lower panel) Corresponding chest x-ray showing Total 75 220 295
signs of pulmonary hypertension and pleural effusion.
Lung ultrasound in the assessment of AIS 693

Fig. 4 Diffuse interstitial pneumonia. (Left panel) Lung ultrasound pattern of diffuse AIS. (Right panel) Corresponding high-resolution
CT showing multiple interstitial reticular thickening, some ground-glass areas, and bilateral pleural effusion.

In 17 cases, CT scan and ultrasound correlated also with 4. Discussion


the chest radiograph and clinical outcome. In one case, the
CT did not agree with the chest x-ray. It was a case of Some authors previously showed that comet tail
idiopathic pulmonary hypertension without signs of respi- artifacts type B at lung sonography generate through
ratory failure at admission. In this case, the CT scan and resonance due to multiple reflection of the beam from
ultrasound were normal, whereas at plain film, the thickened interlobular septa to lung surface [2-7,9]. In a
radiologist described diffuse interstitial involvement. series of critically ill patients admitted to an intensive
694 G. Volpicelli et al.

Fig. 5 Idiopathic pulmonary fibrosis. (Left panel) Diffuse presence of B lines at lung ultrasound, together with thickened and irregular
pleural line. (Right panel) Corresponding high-resolution CT showing bilateral thickened interlobular septa reaching the whole surface of the
lung, with some right-sided and peripheral honeycomb patterns.

care unit, Lichtenstein et al [2] showed that the artifact ARDS. They found an association between the presence
and pulmonary subpleural thickened interlobular septa of the artifact and radiologic AIS. Both sensitivity and
and/or ground-glass areas at CT were largely associated. specificity increased when the presence of an artifact
The same authors observed that in healthy persons, the limited laterally to the last intercostal space was consid-
artifact can be limited to the last intercostal spaces, ered as a feature of the normal lung. They concluded that
whereas it was diffused all over the lung surface in the detection of the comet tail artifact is reasonably
patients with pulmonary edema, pulmonary fibrosis, and accurate to allow diagnosis of AIS, but they did not
Lung ultrasound in the assessment of AIS 695

Table 3 Positivity (percent) at each of the 8 chest areas


this could be a matter of a future study trial. We cannot
studied in 64 patients with clinical diagnosis of AIS and explain the other 3 cases with positive ultrasound but
ultrasound lung pattern of diffuse B lines negative plain film and clinical outcome. In all 3 cases, the
ultrasound showed 2 positive scans per side.
Right chest (%) Left chest (%)
Another objective of our study was to define the criteria
Anterior upper 67.2 65.6 needed to diagnose diffuse alveolar syndrome at lung
Anterior lower 73.4 71.9
ultrasound in noncritically ill patients. Lichtenstein et al
Lateral upper 78.1 85.9
Lateral basal 93.8 93.8
defined adequately the features of a normal ultrasound, that
is, B lines either absent or limited to the last intercostal
space above the diaphragm. They also defined an abnormal
define exactly the feature of a pathologic lung ultra- sonographic scan, with at lest 3 B lines. A general definition
sound [2]. of a lung ultrasound diagnostic of AIS is still lacking.
The first objective of our study was to determine the According to our experience, diagnosing diffuse AIS
accuracy of the artifact in diagnosing AIS in patients requires at least 2 positive scans per side. Our series of
admitted to an emergency medicine ward. Such patients cases was analyzed according to such a criterion. We
are less severely ill and with a wider variety of diagnosis observed 63 patients with isolated alveolar consolidation
than patients admitted to an intensive care unit. Never- (pneumonia, cancer, or other) without diffuse AIS, and most
theless, in our series, sensitivity and specificity of the of them exhibited comet tail artifacts just in the area
artifact in diagnosing AIS using the x-ray picture as gold surrounding the lung consolidation. In 60 of these, the lung
standard were satisfactory. Moreover, when comparing the ultrasound did not meet our criteria for diagnosing diffuse
ultrasound diagnosis with the clinical outcome, the AIS (see Table 1). On the contrary, all 9 cases of interstitial
accuracy of the test in diagnosing clinical AIS was pneumonia or multiple and bilateral pneumonia studied
similarly high. Interstitial lung involvement, either acute exhibited positive ultrasound patterns.
or chronic, mild or severe, led to the presence of the The skill to recognize a pathologic pattern at lung
artifact in our series. Particularly, acute pulmonary edema, ultrasound was easily acquired by radiologists and emer-
interstitial pneumonia, and chronic interstitial diseases gency physicians. Feasibility and reproducibility of the
mostly showed diffuse B lines at bedside lung ultrasound. exam were good, and all the physicians involved judged it
Positivities at ultrasound for each of the 8 chest windows as an easy-to-use diagnostic tool. As for the clinical
are shown on Table 3. significance of sonographic AIS, the bedside diagnosis
Eleven patients exhibited negative ultrasounds but of AIS in dyspneic patients is useful particularly in the
positive radiographs. They were 8 cases of acute left heart emergency setting [10]. Chest radiograph is not always
failure, 2 cases of exacerbation of COPD, and 1 case of decisive [11,12]. The rapid recognition of B lines allows to
pneumonia. Ultrasound was performed within 48 hours, distinguish between different sources of respiratory failure.
whereas chest radiograph was obtained always at presenta- According to the literature, sonographic comet tail artifacts
tion in the ED. This delay may explain the discordant may be useful for ruling out pneumothorax [13] and
findings of the 2 tests in the 8 cases of congestive heart differentiating cardiogenic pulmonary edema from decom-
failure, as a result of resolution of interstitial lung pensated COPD [14]. This is particularly valuable when
involvement due to treatment. Although in all these 8 cases a high-quality chest radiograph cannot be quickly obtained,
artifacts were present in at least 3 scans, criteria for and diagnosis is not clinically straightforward. Moreover,
diagnosing diffuse sonographic AIS were not met. In the many EDs lack a radiologist at night and during week-
other 3 discordant cases, the absence of diffuse artifacts ends, whereas the interpretation of a bedside-performed
at ultrasound was consistent with the clinical outcome chest x-ray, often of bad quality, is not always easy for the
because exacerbation of COPD and isolated pneumonia are attending emergency physician.
not included in AIS. It must be said that the radiologic
detection of interstitial syndrome is often questionable and 4.1. Limitations
subjective, particularly when the radiologist read chest films Whereas our study shows the advantages of ultrasound
of bad quality. detection of AIS compared to chest radiograph, it must be
Five patients exhibited a positive ultrasound with a acknowledged that the latter is not the best gold standard for
negative chest x-ray. One of them had a final diagnosis the study of lung interstitium. The accuracy of ultrasound in
positive for AIS (congestive heart failure during acute detecting AIS should be assessed in comparison with high-
bronchitis). The other 4 had a clinical outcome negative for resolution CT. However, in the everyday practice in EDs,
AIS. They were 2 cases of unilateral pneumonia, 1 patient clinical decisions must be taken in the absence of findings
with fever of unknown origin and 1 patient with rheumatoid obtained with the latter technique. The purpose of the
arthritis. In the latter case, we could hypothesize that the present study was to compare ultrasound with the test
artifact is detectable at a very early stage of pulmonary ordinarily used to evaluate lung interstitium in the emer-
interstitial involvement in a collagen vascular disease, and gency setting.
696 G. Volpicelli et al.

4.2. Conclusion ultrasound in the critically ill. 1st ed. Heidelberg7 Springer-Verlag;
2005. p. 105 - 15.
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