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87, 2014
Fig. 1. A 28-year-old woman with clinical signs of pneumonia. on both sides. c LUS of the left side on day 16 is normal, where-
a LUS of the left side reveals an echopoor lesion with typical as chest X-ray on day 16 still shows residual disease on both
positive air bronchogram. b Corresponding chest X-ray per- sides (d).
formed on the day of her hospital admission shows infiltration
Area of echopoor echogenicity and an Pleural line attenuation corresponding Color Doppler sonography: enhanced,
inhomogeneous echotexture with blurred to the affected area tree-like vascularity
margins
Positive air bronchogram: reflects residua of Localized pleural effusion Spectral curve analysis: pulmonary and
air within consolidated areas bronchial artery
Positive fluid bronchogram: reflects Basal pleural effusion Contrast-enhanced sonography: short
fluid-filled airways time to enhancement and marked extent
of enhancement
Necrotic areas within pneumonic lesions
possible
Superficial fluid alveologram: subpleural
echopoor region without bronchogram
and fluid bronchogram
bronchogram. Malignancies are polycyclic, not well de- Doppler sonography. Pleurisy and pleural lesions of un-
marcated and sometimes infiltration into the thorax wall known causes may be further differentiated by contrast-
may be discovered that avoids breath-dependent motion enhanced sonography [21]. For further reading on this
of the lesion. In spectral curve analysis, various vessels are topic, we like to refer to the review by Kreuter et al. [22]
detectable, particularly new blood vessels in tumor tissue in this Thematic Review Series.
(neoangiogenesis). Atelectasis, compressive atelectasis as well as resorp-
Pulmonary embolism may also cause pneumonia due tive atelectasis have to be differentiated from pneumo-
to embolic occlusion, which might be suspected if pneu- nia. Compressive atelectasis is normally induced by a
monia is triangular. Characteristic sonographic signs of large pleural effusion and moves within the effusion like
peripheral pulmonary embolism are multiple (mean a ‘waving hand’. It is moderately echoic, sharp demar-
2–3), mostly triangular, hypoechoic, subpleural lesions cated and concave. Occasionally, it is possible to notice
with breath-dependent motion, which prefered the dorsal breath-dependent ventilation within the atelectasis. Af-
and basal regions of the lung [19, 20]. Peripheral pulmo- ter thoracocentesis or diuretic therapy, compressive at-
nary embolism typically reveals no flow signals in color electasis becomes smaller or even disappears. Resorptive
Feature Gehmacher et al. Reissig and Parlamento et al. Sperandeo et al. Reissig et al. Cortellaro et al.
[12], 1995 Kroegel [15], 2009 [14], 2011 [9], 2012 [18], 2012
(n = 143) [13], 2007 (n = 49) (n = 342) (n = 362) (n = 120)
(n = 30)
Study design Patient with Patient with Patient with Inclusion of Patient with Patient with suspected
X-ray-established suspected CAP; suspected CAP X-ray-established suspected CAP; CAP in ED; CT if
pneumonia LUS follow-up admitted to ED CAP; LUS LUS follow-up clinically indicated
was required follow-up (n = 30); most X-rays in
supine position; final
diagnosis as surrogate
Established 143 (100%) LUS and X-ray 32/49 (65.3%) 342 (100%) 229/362 (63.3%) 81/120 (67.5%)
diagnosis of follow-up
pneumonia
LUS positive 127/143 (88.8%) Not reported 31/32 (96.9%) 314/342 (92%) 211/229 (92.1%) 80/81 (98%)
X-ray positive Reference test Reference test 24/32 (75%) Reference test 199/229 (86.9%) 54/81 (67%)
Interstitial Not reported Not reported 22/32 (68.8%) Not reported Not reported 7/80 (8.8%)
pattern alveolar IS
Positive air 112/127 (88.1%) 32/32 (97%) 16/32 (50%) 220/314 (70%) 183/211 (87.7%) 71/80 (88.8%)
bronchogram (dynamic)
Fluid Not reported 0/33 (0%) Not reported 100/314 (31%)* 17/211 (8.1%) 28/80 (35%)
bronchogram
Basal pleural 78/143 (54.5%) 20/33 (61%) 11/32 (34.4%) 120/34 (35.1%) 105/193 (54.4%) 31/80 (38.8%)
effusion in
LUS
Size (LUS), cm Not reported 3.37×0.94 and Not reported 6.63×3.11 3.2×3.7 Not reported
9.12×4.53
Sensitivity for Not applicable Not reported Not reported Not applicable 93.4%; 98%;
LUS CI: 89.2–96.3% CI: 93.3–99.9%
Specificity for Not applicable Not reported Not reported Not applicable 97.7%; 95%;
LUS CI: 93.4–99.6% CI: 82.7–99.4%
Likelihood Not applicable Not reported Not reported Not applicable 40.5 19.3
ratio for CI: 13.2–123.9% CI: 4.99–74.2%
positive LUS
Likelihood Not applicable Not reported Not reported Not applicable 0.07 0.01
ratio for CI: 0.04–0.11% CI: 0.002–0.09%
negative LUS
atelectasis is a consequence of airway obstruction, most- may be detected. In contrast to pneumonia and compres-
ly caused by cancer, exudate or aspiration. The accom- sive atelectasis, resorptive atelectasis does not reveal a
panying effusion is small in comparison with the atelec- dynamic air bronchogram [23]. Using contrast-en-
tasis, and thoracocentesis does not influence the size of hanced sonography, resorptive atelectasis may be de-
resorptive atelectasis. Its echogenicity is comparable to marcated from the inducing cancer or metastasis [24],
that of the liver and the shape is very variable. Sometimes which is very helpful to determine the optimal site for
a fluid bronchogram reflecting exudate-filled airways tumor biopsy.
Feature Copetti and Cattarossi Iuri et al. [25] Caiulo et al. [26] Shah et al. [27]
[8], 2008 2009 2013 2013
(n = 79) (n = 28) (n = 102) (n = 200)
Study design Patient with suspected Patient with suspected Patient with suspected CAP in Patient with suspected
CAP; comparison to CAP; comparison to X-ray hospitalized children; CAP; comparison to
X-ray in 1 plane (2 planes over 4 years) comparison to X-ray in 1 plane X-ray in 2 planes
Established diagnosis 60/70 (75%) 28/28 (100%) 89/102 (87%) 54/200 (27%)
of pneumonia
LUS positive 60/60 (100%) 22/28 (78%) 88/89 (98.8%) 49/54 (90.7%)
X-ray positive 53/60 (83.3%) 28/28 (100%) 81/89 (92%) 36/54 (66.6%)
Sensitivity for LUS Not reported 91.7% Not reported 86%
Specificity for LUS Not reported 100% Not reported 97%
LUS Compared With X-Ray, CT and Auscultation ments in LUS techniques, it has the potential to establish
The sensitivity of LUS in detecting CAP varies between as a very important diagnostic imaging option for pneu-
93.4 and 98%, and the specificity between 97.7 and 95%; monia, especially in children [28].
the positive likelihood ratio ranges from 19.3 to 40.5, and
the negative likelihood ratio from 0.01 to 0.07 [9, 18]. In Sonomorphology
several studies, LUS was at least as good as X-ray evaluation The ultrasonographic appearance of pneumonia does
in detecting CAP [8, 9, 15]. Nevertheless, the gold standard not differ between children and adults [11]. Pneumonia
CT was never used in all patients due to the hazards of ra- appears as a hypoechogenic area with poorly defined bor-
diation exposure [8, 9, 15]. Sonography detects peripheral ders and with the presence of B-lines at the far-field mar-
pneumonic lesions, even small ones, whereas X-ray covers gin. The pleural line is less echogenic in the area affected
also central localized processes, but small ones may escape by lung consolidation and lung sliding is reduced or ab-
radiological detection. During the follow-up, LUS may al- sent. In the case of consolidations, branching echogenic
ready appear normal because the lesion no longer reaches structures – representing air bronchograms – are seen in
the peripheral pleura. However, both techniques have ad- the infected area (fig. 2 and fig. 3). Air bronchograms may
vantages and disadvantages. They are comparable as well show intrinsic dynamic centrifugal movements due to
as complementary. It has been demonstrated that a com- breathing. This finding is called dynamic air broncho-
bination of LUS and auscultation findings resulted in a gram: it attests bronchial patency and rules out obstruc-
higher positive (42.9, 95% confidence interval, CI, 10.8– tive atelectasis. Multiple lenticular echoes, representing
17.0) as well as in a lower negative likelihood ratio (0.04, air trapped in the smaller airways, are also frequently ob-
CI 0.02–0.09) [9]. LUS enables the early detection of com- served. Fluid bronchograms, described in postobstructive
plications such as empyema and lung abscesses. pneumonia, are identified as anechoic tubular structures
with hyperechoic walls but without color Doppler signals.
Fluid bronchograms are frequently observed in pneumo-
LUS Compared with Other Methods in the Diagnosis nia in children (fig. 4, 5). Pleural effusion is easily detect-
and Follow-Up of CAP in Children ed on LUS and appears as an anechoic area in the pleural
space. A honeycomb organization of fibrin is observed in
At present, only a few papers have been published on pleural empyema (fig. 6).
this topic [8, 25–27], but all studies have demonstrated that
LUS is able to diagnose pneumonia in children and young Differential Diagnosis
adults with high accuracy (table 3). It will not completely Like in adults, pulmonary atelectasis may simulate
replace chest radiography, but with increasing use and ex- pneumonia. The dynamic ultrasound signs are often very
perience by ultrasonographers combined with improve- useful for the differential diagnosis and may be monitored
Fig. 4. Fluid bronchograms, which are frequently observed in post- Fig. 5. Lobar pneumonia in a 10-year-old child admitted to the
obstructive pneumonia, appear as anechoic tubular structures emergency department for fever and cough. LUS reveals air and
with hyperechoic walls without any color Doppler signal. fluid bronchograms within the affected area.
To date, the following issues remain open to discus- Table 4. Characteristic sonomorphologic features of DPLD (mod-
sion: ified after [11])
– counting of B-lines (8-zone technique vs. 28 rib inter-
Multiple, diffusely distributed, bilateral, nonhomogeneous
spaces) [11, 34]; B-lines (mostly in the lower lobes and dorsally)
– the effect of the ultrasound equipment, the scanner
(convex or linear) and penetration depth used on the B-line localization/distribution correlates with CT signs of fibrosis
number of B-lines and pleural line abnormalities; Pleural line abnormalities (irregular/fragmented) are detectable
– differences in scoring systems between various studies Subpleural abnormalities (small echopoor lesions) may occur
(>6 B-lines per scan; ≥3 B-lines in a longitudinal plane
Minor pleural effusion is possible
between 2 ribs; ≥3 B-lines in ≥2 adjacent scanning sites
or >5 B-lines) [11, 33, 37].
In general, it has to be taken in account that counting
of B-lines is best performed in real-time mode as they
may disappear on a frozen image. of IS [11, 42]. In ARDS, the damage of the alveolar capil-
lary membrane causes an early, diffuse, heterogeneous
Increase in Extravascular Lung Water: Acute Heart alveolar flooding ranging from a ‘ground glass’ appear-
Failure and ARDS ance to lung consolidation. The heterogeneous involve-
In acute cardiopulmonary clinical conditions, bilateral ment of the lungs in ARDS explains the presence of
and diffuse B-lines are more frequently an ultrasono- ‘spared areas’. Pleural line abnormalities are very com-
graphic sign of increased extravascular lung water. The mon in patients with ARDS and may be well visualized
sensitivity of B-lines in detecting the increase in extravas- with a linear probe. It is possible to observe areas with a
cular lung water is very high, ranging from 96.9 to 100% reduction or absence of ‘lung sliding’ and often areas in
in different studies, and their absence in a dyspneic pa- which B-lines are coalescent (‘white lung’) are observed.
tient virtually rules out pulmonary edema [42, 43]. In addition, the ‘lung pulse’ sign could be observed. The
In critically ill patients, the differential diagnosis be- pleural line appears irregular, thickened and coarse be-
tween acute cardiogenic pulmonary edema (APE) and cause of the presence of multiple small subpleural con-
ARDS may be very difficult [44]. Differential diagnosis solidations. Involvement of the pleural line is not homo-
using CT has been well described, although the accuracy geneous and corresponds to the distribution and degree
of chest X-ray is unclear. Chest X-ray is a poor at detect- of IS (fig. 8; table 5).
ing the cause or location of excess extravascular lung wa- In contrast, APE is a hydrostatic edema and IS shows
ter [45]. a homogeneous distribution involving both anterior and
The pathophysiology of ARDS is completely different posterior lung fields. Superior lung fields might be less
from that of APE and this generates different pleuropul- affected but ‘spared areas’ cannot be observed, which re-
monary ultrasound patterns with a different distribution flects the pathophysiology. B-lines initially prefer the lung
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