ARTICLE IN PRESS

Ultrasound in Med. & Biol., Vol. ■■, No. ■■, pp. ■■–■■, 2018
Copyright © 2018 World Federation for Ultrasound in Medicine & Biology. All rights reserved.
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https://doi.org/10.1016/j.ultrasmedbio.2018.04.007

● Original Contribution

LUNG ULTRASOUND FINDINGS UNDETECTABLE BY CHEST RADIOGRAPHY IN

CHILDREN WITH COMMUNITY-ACQUIRED PNEUMONIA
Giulio Iorio,* Maria Capasso,† Salvatore Prisco,* Giuseppe De Luca,* Carlo Mancusi,*
Bruno Laganà,* Maria Antonietta Piscopo,* and Vincenzo Comune*
* Department of Pediatrics, “San Giovanni di Dio” Hospital, Azienda Sanitaria Locale Napoli 2 Nord, Frattamaggiore, Naples, Italy;
and † District 18, Azienda Sanitaria Locale di Caserta, Sant’Arpino, Caserta, Italy
(Received 5 January 2018; revised 15 March 2018; in final form 9 April 2018)

Abstract—The purpose of our study was to evaluate any differences between lung ultrasonography and chest ra-
diography (CR) images in children with a diagnosis of community-acquired pneumonia (CAP) and, if there are
any, to analyze the reasons and possible clinical implications. We reviewed the medical records of patients ad-
mitted to the pediatric ward from January 2014 to December 2016 and selected only cases discharged with a diagnosis
of CAP who had undergone performed lung ultrasound (LUS) and CR within 24 h of each other. All radiologic
and sonographic images of the selected cases were examined blindly by a senior radiologist and a skilled sonographer,
respectively, with respect to number, position and size of lung injuries. Of the 47 cases of pneumonia, 28 lung
lesions spotted by LUS were undetected by CR. Compared with CR, LUS detects more cases of pneumonia, a
greater number of cases of double pneumonia and minimal pleural effusions. LUS should be considered the first-
line imaging tool for CAP. (E-mail: [email protected]) © 2018 World Federation for Ultrasound in Medicine
& Biology. All rights reserved.
Key Words: Double-pneumonia, Pleural effusion, Pulmonary ultrasonography, Sub-pleural consolidations, Lung
ultrasound, Chest X-rays, Pneumonia.

INTRODUCTION of 93% for diagnosing pneumonia, and other studies

promote lung ultrasound as the first choice (Iorio et al.
Community-acquired pneumonia (CAP) is one of the
2015) or as a valid alternative tool to replace chest radi-
leading causes of death at pediatric age worldwide. The
ography (CR) (Jones et al. 2016).
World Health Organization (WHO) estimated the median
The LUS and CR examinations may produce differ-
global incidence of pneumonia to be 0.28 episodes per
ent results ranging from the technical mode as ultrasound
child-year (Rudan et al. 2004), and 95% of all episodes
or radiation, to a different resolution capability, to vari-
of pneumonia in young children occur in developing
ability of interpretation. The aim of this study was to
countries.
determine if there are any differences in number, posi-
In developed countries the diagnosis is usually based
tion and size of lung lesions between sonographic images
on clinical history, respiratory rate, fever, respiratory signs
and the corresponding radiographic images in cases of
and symptoms and, possibly, radiography especially in
pneumonia, to analyze the reasons in the event of differ-
severe or complicated cases (Bradley et al. 2011; Harris
ences and to assess whether these differences have clinical
et al. 2011).
implications.
The use of lung ultrasound (LUS) for the diagnosis
of CAP has been growing in multiple settings, and nu-
METHODS
merous studies have reported its reliability and accuracy
in diagnosing this pathology in children and young adults. A retrospective analysis of all medical records of chil-
The meta-analysis of Pereda et al. (2015) confirmed that dren with a final diagnosis of pneumonia who were
LUS has an overall sensitivity of 96% and a specificity admitted to the Pediatric Department of San Giovanni di
Dio Hospital between January 2014 and December 2016
was conducted. We included patients admitted to the
Address correspondence to: Giulio Iorio, Department of Pediatrics,
San Giovanni di Dio Hospital Via Pirozzi 37, 80028 Frattamaggiore, NA, Emergency Department and subsequently admitted to the
Italy. E-mail: [email protected] Pediatric Department on whom CR and LUS were

1
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2 Ultrasound in Medicine & Biology Volume ■■, Number ■■, 2018

Fig. 1. Flowchart of selection of medical records. CR = chest radiography; LUS = lung ultrasound.

performed within 24 h of each other. We excluded all pa- further sub-divided into upper and lower sub-areas by a
tients with congenital anomalies, bronchitis, bronchiolitis, horizontal line.
asthma, hemodynamic instability, other co-morbidities and All sonographic and radiologic images collected were
external CR. de-identified, assigned a research study number and placed
A total of 124 medical records with diagnosis of CAP into a designated picture archive, eliminating any possi-
were discharged during the period of study, of which 47 bility of linking the clinical patient data.
were enrolled in this study (Fig. 1). The radiologic film was divided into two zones (upper
Posterior–anterior chest radiographs were obtained and lower) by drawing one horizontal line. Each of these
in accordance with the British Thoracic Society guide- zones occupies approximately half the height of the lungs.
lines (Harris et al. 2011) using a Villa Moviplan800 X-ray The injuries in correspondence with the separation line were
machine (Villa Sistemi Medicali, Buccinasco, Milan, Italy), classified in the upper or lower district based on the greater
and the pneumonia was diagnosed in accordance with area of occupancy. The radiologic images were reviewed
WHO criteria for the standardized interpretation of pedi- by a senior radiologist, and the sonographic pictures were
atric chest radiographs (WHO 2001). The LUS was examined by a skilled sonographer; each was unaware of
performed by a skilled sonographer within 24 h of CR using the other’s findings.
Sonosite MicroMaxx Systems ecographic equipment The main findings of the CR and LUS were catego-
(Fujifilm SonoSite, Bothell, WA, USA) with a 5- to 10- rized as negative, consolidation and pleural effusion, and
MHz linear probe (L38 e). The probe was placed the number, position and size of any image abnormali-
perpendicular, oblique and parallel to the ribs in the an- ties were evaluated. Sonographic results were defined as
terior, lateral and posterior thorax, as described by Copetti follows: presence of A-lines without B-lines and regular
and Cattarossi (2008), with the patient in the supine po- pleural line as “negative”; hypo-echogenic area of varying
sition and sitting position to scan the posterior thorax. size and shape with poorly defined borders with air
Each hemithorax during lung ultrasound examina- bronchograms as “consolidation”; and presence of fluid
tion was divided into three major areas (anterior, lateral >3 mm in width within the pleural space as “pleural ef-
and posterior) delineated by the parasternal, anterior ax- fusion” (Mong et al. 2012; Reissig and Kroegel 2007;
illary and posterior axillary lines (Cattarossi 2013) and Volpicelli et al. 2012). Consolidations were divided into
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Lung US findings undetectable by chest X-ray ● G. Iorio et al. 3

two size groups, ≤1 cm and >1 cm (in depth from the Table 2. Chest radiography and lung ultrasound
pleural line), on the basis of threshold visibility of the CR findings
(Raoof et al. 2012; Shah et al. 2013). We did not consid- Finding Chest radiography Lung ultrasound
er the exclusive confluent B-line ultrasound patterns. For
radiologic results, consolidation was defined as dense, often Right upper region
Consolidations >1 cm 6 6
homogeneous, confluent alveolar infiltrate or fluffy, mass- Consolidations ≤1 cm 0 0
like or cloud-like, density that erases heart and diaphragm Pleural effusion 0 0
borders (silhouette sign) with or without air bronchograms Right lower region
Consolidations >1 cm 26 32
and pleural effusion as a fluid collecting in the pleural space Consolidations ≤1 cm 0 6
(WHO 2001). Pleural effusion* 3 0
The results are expressed as the mean ± standard de- Left upper
Consolidation >1 cm 3 5
viation (SD) for quantitative variables and as the frequency Consolidations ≤1 cm 0 0
(percentage) for categorical variables. The differences Pleural effusion 0 0
between LUS and CR findings were assessed using the Left lower region
Consolidations >1 cm 6 13
McNemar χ2-test for paired data. p Values < 0.05 were con- Consolidations ≤1 cm 0 9
sidered to indicate significance. All tests were two- Pleural effusion 0 1
tailed, and statistical analysis was performed using SPSS Total 44 72
software (Version 20.0, IBM, Armonk, NY, USA) and * The three pleural effusions found by chest radiography are instead lung
MedCalc software (Version 13.3, MedCalc Software bvba, consolidations by lung ultrasound.
Ostend, Belgium).
The study protocol was approved by the ethics com- Table 3. Comparison of chest radiography and lung
mittee of San Giovanni di Dio Hospital with Approval No. ultrasonography results for pneumonia and double
355/CE. All patient records and clinical information were pneumonia
anonymized and de-identified before analysis; the insti- Lung ultrasound
tutional review board considered the informed consent to
Chest radiography Positive Negative Total
be unnecessary.
Pneumonia (McNemar p = 0.004)
RESULTS Positive 38 0 38
Negative 9 0 9
The children ranged in age from 1 mo to 12 y (mean Total 47 0 47
Double pneumonia (McNemar p = 0.03)
age: 4 y, SD: ± 2.5 y, median: 3.6 y, interquartile range: Positive 1 0 1
3 y); there were 27 males (57.4%) and 20 females (42.6%). Negative 6 40 46
The average hospital stay was 5.4 ± 2.1 d, and the most Total 7 40 47
common symptoms were fever and cough. General patient
characteristics are listed in Table 1.
Among the 47 cases of pneumonia, a total of 44 12 consolidations >1 cm, 3 were detected in the right lung
lesions were detected on CR, whereas LUS identified 72 with both CR and LUS, and 9 were negative by CR
injuries; 28 lesions detected by LUS were not detected by (p = 0.004). In one case, CR detected consolidations >1 cm
CR. Of these, LUS spotted 15 consolidations ≤1 cm, 12 bilaterally, while LUS identified consolidations >1 cm in
consolidations >1 cm and 1 minimal pleural effusion. The both lungs in 7 cases (p = 0.03).
3 pleural effusions identified by CR were in fact lung con- Of the 15 consolidations ≤1 cm, all were associated
solidations spotted by LUS; one minimal pleural effusion with the presence of a consolidation >1 cm; 7 were present
spotted on LUS was not found by CR (Table 2). Of the in the same lung of the main consolidation, and 8 were
located in the contralateral lung.
Finally, the position of all lesions detected by LUS
Table 1. Baseline characteristics of the study and visible on CR corresponded to the same area of pro-
participants, n = 47 jection on radiographic films. Table 3 compares CR and
Characteristic Mean ± SD/No. (%) LUS results for pneumonia and double pneumonia.

Age, y 4.0 ± 2.5

Male sex 27 (57.4%)
DISCUSSION
Tachypnea for age (%) 36 (76.6%)
Cough 45 (95.7%)
According to current guidelines, the diagnosis of CAP
Fever, d 4.2 ± 1.1 is clinical and CR is considered in children in poor or com-
Body temperature on admission, °C 38.5 ± 0.6 plicated condition (Bradley et al. 2011; Harris et al. 2011).
Length of stay, d 5.4 ± 2.1
Unfortunately, despite these indications, CR is still
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4 Ultrasound in Medicine & Biology Volume ■■, Number ■■, 2018

Fig. 2. Negative chest X-ray (a) of patient with localized crackles and rales in basal posterior left lung. In this case, lung ul-
trasound detected consolidation and minimal pleural effusion (b).

performed in children with mild and/or uncomplicated cluded that non-lobar types of infiltrates could be
pneumonia (Bowen and Thomson 2013). underdiagnosed in 15% of patients using the frontal view
One of the limitations of radiography is the risk of alone (Rigsby et al. 2004). In addition, we need to con-
damage from ionizing radiation, which is greater for chil- sider the interpretive variability (Johnson and Kline 2010;
dren than for adults because children have a higher Williams et al. 2013) and the difficulty involved in de-
sensitivity to ionizing radiation exposure (Ait-Ali et al. tecting infiltrates or consolidations in the juxta-
2010; Frush and Slovis 2013). Numerous studies have re- diaphragmatic region.
ported the high diagnostic accuracy of ultrasonography Among the radiologic false-negative cases, LUS iden-
imaging and indicated that LUS is an excellent tool for tified one case of bilateral pneumonia with consolidations
detecting pneumonia in children (Copetti and Cattarossi located in the retro-cardiac left region and anterior para-
2008; Pereda et al. 2015; Volpicelli et al. 2012). For these sternal right region. In yet another case, the consolidation
reasons, LUS should be the main alternative to CR or, at was visible on CR only in the left region, whereas LUS
the least, the first-line examination. identified the same consolidation on the left with minimal
The findings of this study indicate that LUS can iden- pleural effusion and another consolidation in the anterior
tify lung consolidations undetectable by CR. In 9 cases, parasternal right region. In one case of double pneumo-
CR findings were negative for consolidations, and the dis- nia, there was correspondence between CR and LUS, and
charge diagnosis was based on clinical history, respiratory in the other 4 cases, CR did not identify the consolida-
signs and symptoms, crackles in the thoracic region, lab- tion in the left posterior basal region.
oratory findings and clinical course compatible with It is apparent that negative radiologic findings could
pneumonia (Harris et al. 2011). Of these 9 cases all de- mislead the physician both on diagnosis and on therapeu-
tected by LUS, 7 consolidations >1 cm were localized in tic management because of their failure to recognize
the posterior basal region (retro-cardiac) of the left lung pneumonia and double pneumonia.
undetectable by CR because of the cardiac shadow, and Another interesting result of our study is the detec-
2 were in the anterior basal parasternal region of the right tion of small consolidations (≤1 cm) entirely invisible to
lung (juxta-diaphragmatic), corresponding to the same areas CR. Among the 15 cases, 7 small consolidations were lo-
of auscultation for localized rales (Fig. 2). However, in calized on the same lung as the main consolidation, and
3 of the 9 cases, CR was performed within 48 h of the onset the remaining 8 (about 15% of all pneumonias) were
of fever, which could lead to misleading results (Hagaman on the contralateral side. In particular, we noted that when
et al. 2009). the main consolidation was localized in the lower or, less
Chest radiographs have been obtained only in the an- frequently, upper anterior district of the right lung in an-
teroposterior projection in accordance with current terior scans, a small sub-pleural consolidation was observed
guidelines of the British Thoracic Society. For this reason, in the posterior basal segments of the left lung (7 cases)
it is possible for retro-cardiac consolidations to escape de- and vice versa (1 case). This type of contralateral injury,
tection in radiologic examinations. A retrospective study which we called a “satellite lesion” (SL) to distinguish it
reviewed the frontal radiographs alone and the frontal and from the main lesion, is visible only on LUS because the
lateral radiographs separately for 1268 children and con- sub-centimeter size is undetectable by CR (Fig. 3).
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Lung US findings undetectable by chest X-ray ● G. Iorio et al. 5

Fig. 3. Lung consolidation (b) confirmed on chest X-ray (a) in inferior right region. In the same patient, lung ultrasound de-
tected a “satellite lesion” in the inferior posterior region of the left lung (c).

Although it is difficult to differentiate whether SLs are true Finally, the ability of ultrasound to detect even small
areas of consolidation or focal atelectases, because of bron- pleural effusions measuring 3–5 mL is widely acknowl-
chial inflammation and obstruction, we noted that the edged (Coley 2011). Pleural fluid volumes less than 200
disappearance of this lesion was closely linked to reduc- or 50 mL might not be visible on a frontal or lateral chest
tion of the main injury. This event, detected during an radiograph, respectively, and it can be difficult to identi-
ultrasonographic follow-up performed routinely in all cases fy an opacification of pleural fluid from a consolidation
of pneumonia, may well not be an incidental finding. The (Mong et al. 2012). For the diagnosis of pleural effu-
clinical relevance of sub-centimeter consolidations is not sion, chest radiography is reported to have a sensitivity
yet fully clarified. In our study, the small consolidations of 65% and specificity of 81%, whereas thoracic ultra-
were never isolated. Those on the same side of the lung sound is reported to have a sensitivity of 100% and
may be part of the same main consolidation; it is more specificity of 100% (Xirouchaki et al. 2011). In our study,
difficult to explain SLs situated on the contralateral lung. 3 lesions identified by CR as pleural effusions were con-
A possible explanation of SL could be linked to the eti- solidations by LUS, and one case of minimal pleural
ology of pneumonia and to the lymphatic network. Indeed, effusion spotted by LUS was not identified by the CR. In
the left inferior lobe drains mostly to right superior tra- such cases, the radiologic results could mislead physi-
cheobronchial nodes, and lymph nodes that drain from right cians in diagnosis and therapy.
anterior segments anastomose with lymph nodes of left The limitations of this study are clear. First, it is a
lower segments (Behera 2010; Netter 2003). Therefore, retrospective study, and the sample is small. Second, the
in these cases, a possible etiology could be limited to bac- CR was performed only in anterior-posterior projection,
teria able to follow these pathways such as intracellular as suggested by British Thoracic Society guidelines, al-
Mycoplasma pneumoniae and Chlamydia pneumoniae though the lateral view would not have added anything to
(Kicinski et al. 2011). Several studies have found that M. the identification of lesions ≤1 cm. Third, the cultures and
pneumoniae is identified in children with CAP admitted serologic tests were unavailable, and we were not able to
to the hospital in 4% to 39% of cases (Juvén et al. 2000; assume the secure etiology of pneumonia in the pres-
Michelow et al. 2004; Principi et al. 2001). ence of the SL ultrasonographic pattern. Finally, a
Although LUS, like CR (Korppi et al. 1993), is unable comparison with the computed tomography (CT) would
to determine the exact etiology of pneumonia, the pres- be necessary to confirm these differences, even though this
ence of SLs, if confirmed by further prospective studies could raise ethical issues.
with serologic tests, along with the age epidemiologic cri- Although the guidelines state that there is no need to
terion could justify the use of macrolides as the first choice perform CR in children without severe CAP, as already
in the treatment of pneumonia. mentioned at the beginning of the Discussion, approximately
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6 Ultrasound in Medicine & Biology Volume ■■, Number ■■, 2018

90% of inappropriate radiographs are performed in clin- Coley BD. Chest sonography in children: Current indications, tech-
niques, and imaging findings. Radiol Clin North Am 2011;49:825–
ical practice (Bowen and Thomson 2013). The unreliability 846.
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tendency. A recent meta-analysis suggests that clinical fea- dren. Radiol Med 2008;113:190–198.
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the medical literature, including the results of this study, p. 3–11.
Hagaman JT, Rouan GW, Shipley RT, Panos RJ. Admission chest ra-
it would be desirable to modify the workup for the diag- diograph lacks sensitivity in the diagnosis of community-acquired
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reduction and the possibility of obtaining similar results Harris M, Clark J, Coote N, Fletcher P, Harnden A, McKean M, Thomson
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sized that LUS detects more radiologically negative Iorio G, Capasso M, De Luca G, Prisco S, Mancusi C, Laganà B, Comune
V. Lung ultrasound in the diagnosis of pneumonia in children: Pro-
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supposed etiologic sign, could even have important clin- interpretation of pediatric chest radiographs. Emerg Radiol 2010;
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ical meanings (Jones et al. 2016). Based on the principle Jones BP, Tay ET, Elikashvili I, Sanders JE, Paul AZ, Nelson BP, Spina
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CONCLUSIONS Eskola J, Saikku P, Ruuskanen O. Etiology of community-acquired
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Korppi M, Kiekara O, Heiskanen-Kosma T, Soimakallio S. Compari-
limitations, our study also highlights another novelty: the son of radiological findings and microbial aetiology of childhood
ability to detect lesions invisible on CR. Therefore, its use pneumonia. Acta Paediatr 1993;82:360–363.
should be encouraged also considering the possible clin- Michelow IC, Olsen K, Lozano J, Rollins NK, Duffy LB, Ziegler T,
Kauppila J, Leinonen M, McCracken GH, Jr. Epidemiology and clin-
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the detection of CR’s false-negative pneumonia, the rec- children. Pediatrics 2004;113:701–707.
ognition of a greater number of double pneumonias and Mong A, Epelman M, Darge K. Ultrasound of the pediatric chest. Pediatr
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