Pediatric Pulmonology 48:280287

(2013)

Lung Ultrasound Characteristics of CommunityAcquired Pneumonia in Hospitalized Children

Vito Antonio Caiulo, MD,1* Luna Gargani, MD,2 Silvana Caiulo, MD,3 Andrea Fisicaro,
Fulvio Moramarco, MD,1 Giuseppe Latini, MD,4 Eugenio Picano, MD, PhD,2
and Giuseppe Mele, MD5

Summary. Background: The diagnosis of communityacquired pneumonia (CAP) is based mainly on the patients
medical history and physical examination. However, in
severe cases a further evaluation including chest X-ray
(CXR) may be necessary. At present, lung ultrasound (LUS)
is not included in the diagnostic work-up of pneumonia.
Aim: To describe the ultrasongraphic appearance of CAP at
presentation and during the follow-up. Methods: A total of
102 patients with clinical signs and symptoms suggesting
pneumonia, who underwent a clinically driven CXR, were
evaluated by LUS on the same day. LUS signs of
pneumonia included subpleural lung consolidation, Blines, pleural line abnormalities, and pleural effusion. The
diagnostic gold standard was the expost diagnosis of
pneumonia made by two independent experienced
pediatricians on the basis of clinical presentation, CXR and
clinical course following British Thoracic Guidelines
recommendations. Results: A nal diagnosis of pneumonia
was conrmed in 89/102 patients. LUS was positive for the
diagnosis of pneumonia in 88/89 patients, whereas CXR
was positive in 81/89. Only one patient with normal LUS
examination had an abnormal CXR, whereas 8 patients with
normal CXR had an abnormal LUS. LUS was able to detect
pleural effusion resulting from complicated pneumonia in
16 cases, whereas CXR detected pleural effusion in 3
cases. Conclusions: LUS is a simple and reliable imaging
tool, not inferior to CXR in identifying pleuropulmonary
alterations in children with suspected pneumonia. During
the course of the disease, LUS allows a radiation-free
follow-up of these abnormalities.
Key words: lung ultrasound; pneumonia; B-lines; chest
X-ray.

MD,

INTRODUCTION
In accordance with the British Thoracic
Society
guidelines,
community-acquired
pneumonia (CAP) can be clinically dened as
the presence of signs and symptoms of
pneumonia (such as fever of >38.58C, cough
and respiratory distress) in a previously
healthy child, due to an infection which has
been acquired outside the hospital.1 Chest
X-ray (CXR) is not recommended to
be
performed routinely in uncomplicated cases.
However, in selected cases, the diagnosis of
pneumonia needs to be conrmed with a
CXR.
The use of ultrasound for the evaluation of
the lung is relatively recent. Until a few years
ago, the lung was considered off-limits for
ultrasound.2 This concept, only partially true,
derives from the fact that in the normal lung,
which consists mostly of air, ultrasound
waves are almost completely reected,
without being translated into an image. In a
normal subject the pleura is the only visible
structure, since the high acoustic impedance
of the air below prevents visualization of the
lung parenchyma. In a normal lung,
reverberation artifacts, repetitive and parallel
to the pleura, called A-lines, are

1Department of Pediatrics, Perrino Hospital,

Brindisi, Italy.
2Institute of Clinical Physiology, National
Research Council of Pisa, Italy.
3School of Medicine, San Raffaele
University, Milan, Italy. 4Department
of Neonatology, Perrino Hospital,
Brindisi, Italy. 5Italian Federation of
Pediatricians, Lecce, Italy.
*Correspondence to: Vito Antonio Caiulo,
Department of Pediatrics, Perrino Hospital,
Piazza Angeli, 3 - 72100 Brindisi, Italy.
E-mail: antoniocaiulo@inwind.it
Received 12 October 2011; Revised 19
March 2012; Accepted 20 March
2012.
DOI 10.1002/ppul.22585
Published online 2 May 2012 in Wiley Online
Library (wileyonlinelibrary.com).

Fig. 1. Normal lung. Note the echogenic

line representing the normal pleura, and
the horizontal artifacts, called A-lines.

Fig. 2. Abnormal, discrete

laser-like
vertical
hyperechoic
reverberation
artifacts that arise from the pleural line (Blines).

generated (Fig. 1). In the presence of

pathological processes that lead to thickening
of peripheral interlobular septa, A-lines are
replaced by other artifacts, perpendicular to
the pleural line, called B-lines (Fig. 2).3 Their

versatile application of echography: It is rapid,

portable, repeatable, and non-ionizing. This
last issue is especially important in infants,
who carry a higher risk of cancer from
exposure to radiation than people of other
ages.7 Therefore, alternative diagnostic

physical genesis seems to be linked to the

thickening of the interlobular interstitium of
subpleural secondary lobules, allowing the
reverberation of the ultrasound beam,4
therefore

B-lines

are

considered

the
sonographic sign of interstitial syndrome.5
When an infectious process replaces the
alveolar air content with exudate, the lung
parenchyma becomes accessible to the
ultrasound beam because air content is highly
reduced or dissolved, and its sonographic
appearance becomes similar to that of a
parenchymal organ. If the consolidation
reaches the pleura, it is possible to visualize
the lesion, which has a random conformation
with
irregular, blurred and sometimes
indistinct edges. Multiple lenticular echoes,
representing air trapped in the smaller
airways, are also frequently observed (Fig.
3).6
Lung ultrasound (LUS) is a very easy and

methods that do not involve the use of

ionizing radiation should
be considered
when evaluating young individuals, in order to
minimize cancer risk.8
LUS has been shown to be useful also in
bronchiolitis9
and
in
pneumonia,10
performing even better than CXR, when
compared to chest CT.6
The aim of this study was to dene the
ultrasonographic appearance of pneumonia
in children, and to evaluate the correlation
between clinical and ultrasound ndings
during the course of the disease.
ABBREVIAT IONS:
LUS
P
CXR

Lung ultrasound
Pneumonia
Chest X-ray

Fig. 3. Lung consolidation: Multiple

hyperechoic lenticular elements,
representing air bronchogram s.
METHODS
Study Population
From December 2009 to April 2011, 102
inpatients (53 males) admitted to the
Department of Pediatrics of the Antonio
Perrino Hospital in Brindisi were enrolled.
Inclusion criteria were: (1) Clinical signs and
symptoms suggesting pneumonia (cough,
tachypnea, crackles and/ or decreased breath
sounds, fever with or without chills, chest
pain); (2) age >1 and <16 year-old (which is
the maximum age allowed in our pediatric
department);
(3) presence of a clinically-

driven CXR; (4) availability of

a pediatric
sonographer expert in LUS. Age ranged from
1 to 16 years (mean 5 T 3, median 5.1,
interquartile range 2.38.5 years). In all
patients rst LUS examination was performed
on the day of the admission, dened as day 1,
then between days 3 and 6 (n 88), 7 and
10 (n 67), and 11 and 15 (n 23). LUS
follow-up was stopped when the sonographic
appearance of the lung appeared normal. All
patients underwent a clinically-driven posteroanterior CXR on the day of the admission.
Informed consent was obtained from all
parents, and the investigation followed the
guidelines of the local ethics committee.
The diagnostic gold standard was the expost diagnosis of pneumonia made by two
independent experienced pediatricians on the
basis of clinical presentation, CXR and clinical
course, following British Thoracic Guidelines
recommendations.1 The pediatricians were
blinded to LUS data. LUS examinations were
performed by an expert pediatric sonographer.
The sonographer was informed about the
clinical indication but he was blinded to
radiographic ndings. CXR were performed by
a radiologist informed about the clinical
indication. The radiologist was blinded to LUS
ndings.

CXR Examination

1.

Posterioranterior CXR were acquired with

2.
patients in supine position and recorded by
commercially available X-ray machines. In
accordance with the British Thoracic Society 3.
guidelines, lateral radiographs were not
4.
obtained.1
LUS Examination

Normal pattern, dened as normal lung

sliding with or without A-lines.
Presence of focal multiple or conuent Blines.
Pleural line abnormalities, dened as
irregular appearance of the pleural line.
Presence
of
subpleural
lung
consolidations, dened as subpleural
echo-poor or tissue like region, with
blurred margins, with or without airbronchogram
(internal
hyperechoic
punctiform or linear elements).
Pleural effusion, dened as anechoic or
hypoechoic uid, with or without oating
debris.

Transthoracic LUS examinations were

performed with commercially available
ultrasound machines (Kontron Agile, Toshiba 5.
Nemio), equipped with a high resolution linear
probe with frequencies ranging from 6 to 12
MHz. The LUS examination was performed
following a pre-dened scanning scheme, as Statistical Analysis
previously described.9 The sonographer
Continuous variables are expressed as
always performed a complete scanning of the
mean standard deviation or as median
chest in all children. LUS examination (25th, 75th percentiles) as appropriate.
consisted of both longitudinal and transversal Categorical variables are presented as
sections. On the anterior chest, transversal counts and percentages. All statistical
sections were obtained by positioning the analyses were performed using the SPSS/PC
probe transversally to the chest, from the
software package version 13 (SPSS Inc,
second to the fth intercostal space, whereas Chicago, IL).
longitudinal sections were obtained by positioning the probe longitudinally to the chest, RESULTS
along the parasternal, mid-clavicular, anterior
A nal diagnosis of pneumonia was
axillary and mid-axillary lines. On the
posterior chest, transversal sections were conrmed in 89/ 102 patients. All patients had
obtained positioning the probe on the acute pneumonia without coexisting chronic
intercostal spaces below the scapular spine, lung disease or predisposing congenital
whereas longitudinal sections were obtained abnormalities. None of these children were
along the paraverte- bral, scapular and admitted to the intensive care unit. There
posterior-axillary lines. This method- ology is were no deaths.
LUS results were available soon after the
similar to the one previously described by
examination, since interpretation was always
Copetti et al.6 The selected setting for the
performed real time during the scan. Of the
ultrasound probe was the same as that used
89 children with a conrmed diagnosis of
for soft tissue analysis, with a maximum depth
pneumonia, LUS
showed nd- ings
of 8 cm. This setting allows scanning around
consistent with pneumonia in 88 children,
the entire lung area. LUS has a very good
whereas CXR was positive for pneumonia in
intra- and inter-observer variability, as
81 children. Only one child with normal
previously described.1113
LUS examination had an abnormal CXR
LUS ndings were classied according the
showing a lung consolidation, whereas eight
following patterns:

patients with normal CXR had abnormal

LUS. In these nine patients with discordant
results, the clinical course was always
consistent with pneumonia. In 13/ 102
patientswith normal LUS and CXRupper
respiratory tract infection was diagnose.

any abnormalities at LUS examination. A

sonographic
pattern with A-lines was
predominant. Only one patient showed a few
isolated B-lines (considered as a nonpathological pattern).

LUS Findings
On day 1, LUS ndings in children and
adolescents with pneumonia were as follows:
In 83/89 patients we found subpleural lung

consolidations; mean size was 18 mm

(range 648 mm) (Fig. 4). These lesions
were multiple in 26 patients. Air
bronchograms were observed in 65/83
(78%)
patients. In 59/89 patients we found the
presence of numerous conuent B-lines
(Fig. 5). B-lines were often seen in the
areas adjacent to the consolidation,
probably as an expression of inammatory
perilesional edema.
In 18/89 patients we found pleural line
abnormali- ties (Fig. 6).
In 16/89 patients we found pleural
effusion (Fig. 7).
LUS appeared to be normal in 1/89
children with pneumonia. In this patient,
CXR identied a lung consolidation.
Pleural line abnormalities and pleural
effusion were always associated with areas
of
conuent
B-lines
and/or
lung
consolidations.
In
13
cases,
lung
consolidations were the only ultrasound sign.
In 55 cases, lung consolidations were
associated with the presence of areas of
conuent B-lines. In three cases, areas of
conuent B-lines were the only LUS sign. In
two cases pleural abnormalities were the
only LUS sign. Mean
lung consolidations
was 18 T 14 mm (median 14, interquartile
range: 1120 mm). Children and adolescents
without pneumonia, but with a diagnosis of
upper respiratory tract infection did not show

Fig.
4.
Lung
consolidation:
Internal
hyperechoic linear elements, representing
air bronchogram s.
Fig. 5. Conuent B-lines, dened as areas
of white lung, an expression of perilesional
inammatory edema.

Dynamic LUS Changes During

the Course of Disease
Patients were followed-up for more than 14
days, in order to obtain more information on
the sonomorphology
of
the
pleuro
pulmonary abnormalities during the course

follow-up was not ameliorating, initial therapy

(amoxicillin in four cases, clarithromycin in
three cases) was modied switching to
clarithromycin and ceftriaxone. In 59 of 59
areas of conuent B-lines, a disappearance of
the B-lines or a change in the pattern of
multiple, isolated B-lines, as a sign of lung reaeration, was observed.14 Pleural line
abnormalities were observed in 18 children:
In two cases pleural abnormalities were the
only LUS sign on day 1. In these patients a
pulmonary consolidation appeared near the
pleural lesion at the rst follow-up (Fig. 8),
and a decrease in size was observed later. In
all cases, pleural line
abnormalities
disappeared during the follow-up. Local
pleural effusion corresponding to the area of

Fig. 6. Pleural line abnormalities.

of the disease. In 76/83 patients with lung
consolidations, a decrease in size or
disappearance of the subpleural hypoechoic
areas was observed, always associated with
clinical improvement (no fever, cough, or
dyspnea and a drop in inammatory
laboratory indexes such as C-reactive
protein). However, in seven cases, lung
consolidations initially increased in size at
the time of the rst follow-up examination,
and a reduction in size was observed
thereafter. In these seven patients, since the
clinical courseconsistently with LUS

Fig. 7. Pleural effusion.

lung consolidations was observed in 16 cases,

but disappeared in all cases during the followup.
CXR Findings
The CXR ndings were the following:
Lung consolidations were found in 73/89

patients. These lesions were multiple in

six cases.
Peribronchial thickening was found in
8/89 patients.
Pleural effusion was found in 3/89
patients.
CXR appeared to be normal in 8/89

patients with pneumonia.

In the eight patients with a negative CXR
and positive LUS, the clinical course was
consistent with pneumonia. In these patients,
LUS identied lung abnormalities that were
not revealed by CXR. LUS and CXR ndings
are summarized in Figure 9.
DISCUSSION
This study conrms that LUS is a simple
and reliable imaging tool, not inferior to CXR
in identifying pleuropulmonary abnormalities
in children with suspected pneumonia.
Moreover, this is the rst study addressing

Fig. 8. In this patient, pleural abnormalities were the only LUS sign on day 1 (A);
pulmonary consolidation appeared near the pleural lesion at the rst follow -up (B).

Fig. 9. LUS and CXR overall ndings.

the sonographic follow-up of LUS ndings,

showing the dynamic changes of pleuropulmonary abnormalities over time.
At present, LUS is not included in the
management
of pneumonia, although
previous articles have demonstrated that LUS
is a reliable tool in this condition, both in
children and in adults.6,1517 Parlamento et
al.15 demonstrated that LUS is more
sensitive than CXR (97% vs 75%) in adult
patients admitted to the Emergency Department with suspected pneumonia. Copetti
et al.6 also showed that LUS is more sensitive

Prevention,20 and the National Institute of

Environmental Health Sciences.21
The
radiological risk is cumulative in nature: Every
exam adds dose to dose and risk to risk.22
Children are at least four times more sensitive
than adults to the induction of cancer, as they
have more rapidly dividing cells than adults
and have longer life expectancy.2325
Unfortunately, pediatricians are often unaware
of these risks.26 The long-term risk associated

with radiation exposure should be considered

in the risk-benet assessment behind
appropriate
prescription
of
diagnostic
than CXR in the diagnosis of pneumonia in
8,27
children. Accordingly, LUS is indicated as a testing.
Some other interesting information may be
clinically useful diagnostic tool in pediatric
patients with suspected pneumonia in the derived from this study. A single pneumonic
recent
International
evidence-based lesion was observed in 57/89 cases, but
recommendations for point-of-care lung more than one lung consolidation was found
in 26/89 patients. This is quite surprising,
ultrasound.18
since multiple pneumonic inltrates are only
The clinical implication of these ndings
rarely detected on conventional CXR (6/89
could be important. If these will be further
cases in our series). However, a possible
conrmed in larger populations in multicenter
reason to explain this
studies, LUS could be routinely proposed in
children with suspected pneumonia:
A
clinical picture consistent with pneumonia,
associated with positive LUS ndings would
exclude the need to perform a CXR. In our
series, LUS was also superior to CXR in
detecting pleural effusion resulting from
complicated pneumonia. These data show
that LUS is a potential additional imaging
technique to CXR
and chest computed
tomography (CT), with the advantages of a
shorter time of execution and interpretation,
and lack of ionizing radiation. Ionizing
radiation has long been known to increase the
risk of cancer. X-rays have been ofcially
classied as carcinogen by the World Health
Organizations International Agency for
Research on Cancer,19 the Agency for Toxic
Substances and Disease Registry of the
Centers
for
Disease
Control
and

Fig. 10. CXR shows a mass-like area of increased opacity in

the right lower lobe. LUS shows consolidations near the
posterior-axillary line (A), mid-axillary line (B), mid-clavicular
line (D) and anterior axillary line (F). Furthermore LUS shows
areas of white lungs (conuent B-lines) in the subscapular
region (C) and between the anterior-axillary line and midclavicular line (E).
nding is the following: In CXR standard
projection gives a summation image resulting
from superimposed normal and abnormal or
partially affected lobules, whereas LUS
allows examination along the circumference
of the lung, which may differentiate between
single affected parenchymal sections (Fig.
10). However, LUS cannot identify whether
consolidations converge
in more distal
parenchymal areas (1/89 cases in our series). The described LUS ndings are not
specic for pneumonia. Lung consolidations
may have a variety of causes including
infection, pulmonary embolism, lung cancer
and metastasis, compression atelectasis,
obstructive atelectasis, and lung contusion.18
Additional sonographic signs, such as the
presence of air bronchogram may help to
determine the etiology. In presence of large
consolidations,
branching
echogenic
structure representing air bronchograms are

seen in the consolidated area. Multiple

lenticular
echoes,
representing
air
bronchograms in the smaller airways, are
frequently
observed
also
in
small
consolidations, proving bronchial patency and
helping in ruling out atelectasis.
In our study population, air bronchogram
was present in about 78% of the population,
consistently with previous data.6
We acknowledge some limitations of this
study. LUS can miss consolidations that do not
reach the pleura.18 The sample size is small,
and therefore conrmatory data on a larger
sample size are needed. The sonographer
was not blinded to clinical data, moreover
being not continually present, this could have
led to some selection bias. Presence of LUS
abnormalities not revealed by CXR were not
conrmed by a gold standard such as chest
CT, which cannot be routinely performed for
obvious ethical reasons, although they were
always consistent with the clinical course. Fur-

thermore, the percentage of false-negative to other ultrasound applications.1213

CXR of this study concerning diagnosis of
pneumonia is consistent with literature CONCLUSION
data.28 Syrjala et al.28 comparing chest CT
Our data show that LUS is not inferior to CXR
with CXR ability in the diagnosis of
in identifying pleuropulmonary abnormalities in
pneumonia, found 8 (30.8%) negative CXR
children with suspected pneumonia. LUS can
cases out of 26 conrmed pneumonias.
help to better char- acterize and stratify the
Another limitation of our study is that only one
patients, and for the follow-up
of lung
experienced operator performed all LUS, and
abnormalities. If these results will be conrmed
it is reasonable to hypothesize that similar
by further studies on larger populations, the
results cannot be immediately achieved by
routine use of LUS for pediatric patients with
less
experienced
operators.
As
suspected pneumonia could reduce the number
recommended by the American College of
of CXR performed, reducing the potentially
Emergency Physicians, at least 150 US
harmful radiation burden, as now recomexaminations must be performed and
mended by the Food and Drug Administration
interpreted under supervision by an expert
30 the International Atomic Energy
instructor
to
achieve
sufcient (FDA),
31 and the Presidents Cancer
competency.29 However, the LUS learning Agency (IAEA),
curve is relatively fast and simple compared Panel 2010.32

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