ARTICLE IN PRESS

The Egyptian Journal of Radiology and Nuclear Medicine (2015) xxx, xxxxxx

Egyptian Society of Radiology and Nuclear Medicine

The Egyptian Journal of Radiology and Nuclear Medicine

www.elsevier.com/locate/ejrnm
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ORIGINAL ARTICLE

Lung ultrasonography in evaluation of neonatal

respiratory distress syndrome
Hosam El-Deen Galal M. El-Malah a,*, Seif Hany a,
Mohammad Koriem Mahmoud a, Ahmed M. Ali b

a
Department of Diagnostic Radiology, Faculty of Medicine, Assiut University, Egypt
b
Department of Pediatric, Faculty of Medicine, Assiut University, Egypt

Received 24 November 2014; accepted 19 January 2015

Available online xxxx

KEYWORDS Abstract Objectives: To evaluate diagnostic ability of lung ultrasonography (LUS) in detection of
Respiratory distress pulmonary manifestations of neonatal respiratory distress syndrome as well as follow up the
syndrome (RDS); response to treatments.
Neonate; Patients and methods: One hundred neonates with clinical and radiographic signs of respiratory
Lung ultrasonography distress (RDS) were included in this prospective study. LUS was done using both a transthoracic
(LUS) and a transabdominal approach within the rst 24 h of life and after that for detection of pulmon-
ary manifestations and follow up the response to treatment. LUS ndings were compared with chest
radiography ndings.
Results: In comparison with chest X-ray the LUS had sensitivity 98% and specicity 92% in detec-
tion of pulmonary manifestations of RDS. In follow up to response of treatment the LUS had
100% sensitivity and 94% specicity.
Conclusion: The LUS can be an alternative diagnostic imaging modality for chest X-ray in follow
up neonates with RDS and subsequent reduction dose of radiation.
2015 The Authors. The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by
Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).

1. Introduction units (NICU) (1). Of the many complications of prematurity,

lung diseases such as RDS and its complications (pulmonary
Respiratory distress syndrome (RDS), also known as hyaline hemorrhage, pneumonia, atelectasis, pneumothorax, air leak
membrane disease is the most common clinical syndrome syndrome, and bronchopulmonary dysplasia (BPD)), remain
encountered among neonates treated in neonatal intensive care the most common cause of neonatal morbidity (2). RDS is a
disease of hypoventilation and a manifestation of pulmonary
* Corresponding author. Tel.: +20 1014269335; fax: +20 882343420. immaturity and surfactant deciency. Surfactant usually coats
E-mail addresses: h.elmalah@yahoo.com (Hosam El-Deen Galal M. the alveoli and prevents atelectasis by lowering surface tension.
El-Malah), hanyseifrad@yahoo.com (S. Hany), koriemomar@yahoo. In respiratory distress syndrome, the lungs are poorly compli-
com (M.K. Mahmoud), dr_ahmed_neo@yahoo.com (A.M. Ali). ant with acinar atelectasis, and there is a gradual development
Peer review under responsibility of Egyptian Society of Radiology and of thickening of the interstitium and dilatation of the terminal
Nuclear Medicine. airways (3).
http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
0378-603X 2015 The Authors. The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: El-Malah H-EDGM et al., Lung ultrasonography in evaluation of neonatal respiratory distress syndrome, Egypt J Radiol Nucl Med
(2015), http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
 ARTICLE IN PRESS
2 H.E.-D.G.M. El-Malah et al.

Neonatal respiratory disease is currently diagnosed on the 1.1. Image assessment

basis of clinical signs and plain chest X-ray (CXR) (4). RDS
is typically presented with tachypnea, expiratory grunting,
nasal aring, cyanosis, substernal and intercostal retractions
(5). On plain X-ray chest radiography there is reticulogranular
or ground glass opacication, progressive hypo-aeration and
air bronchograms (Fig.1). Radiological abnormalities correlate
well with the clinical severity. Symptoms and radiological signs
progress during the rst 6 h of life, and in mild to moderate
disease, the granular densities persist for 35 days, clearing
from peripheral to central and upper to lower lungs (3). The
risk of the effects of ionizing radiation (IR) is higher the youn-
ger the child is; with the same dose of ionizing radiation (IR), a
1-year-old child is 1015 times more at risk of developing car-
cinoma than an adult (68). Clinical staging of the RDS using
the Clinical Risk Index for Babies (CRIB) score (9) correlated
with the 4-stage radiographic scale (10) (Table 1). Reduction of
the dose of (IR) is one of the main goals of pediatric radiology.
Thus, the continuous search for the balance between the
potential benets and the potential delayed adverse effects,
which may arise from the use of diagnostic procedures based
on IR, is inevitable when working with children. Ultrasound
imaging is increasingly being used as a non-invasive routine
procedure at NICUs for the diagnosis of the central nervous
system, abdominal cavity, heart, and hip joints. It has the
advantage over X-rays that it does not expose the infant to
ionizing radiation. Recently few studies evaluated the use of
lung ultrasound in the evaluation of neonatal RDS.
Normal transthoracic LUS: the pleura is visualized as a
smooth, echogenic periodically horizontal moving line (lung
sliding sign), synchronous with respiratory cycle below super-
cial planes and between the rib images, which represents the
sliding of the visceral pleura over the parietal pleura (11).
Beneath the pleura the lungs are lled with air, which disables
visualization of the lung parenchyma. However, the high
acoustic impedance between the visceral pleura and the lung
parenchyma results in horizontal artifacts, which are the paral-
lel echogenic lines below the pleural line, equally distanced
from one another, and are called A-lines (Fig. 2) (12,13).
Normal trans-abdominal LUS is based on the artifact phe-
nomenon, which occurs within the phrenopulmonic border. In
a neonate with normally aerated lungs, a transmitted sound
beam is completely reected by the phrenopulmonic border.
After another reverberation against the liver or spleen
parenchyma, sound waves are transmitted back toward the
phrenopulmonic border and then return to a transducer with
subsequent reection of liver or splenic shadow supra-
diaphragmatic that so called acoustic mirror image phenom-
enon, was rst described by Cosgrove et al. (14) (Fig. 3).

Fig. 2 The normal transthoracic LUS. Transverse scan revealing

the ribs and their acoustic shadowing, the pleural line and A-lines.

Fig. 1 Plain radiography antro-posterior view on supine

position for neonate presented with severs RDS, shows diffuse
ground glass opacity of both lungs.

Table 1 Plain radiography staging of RDS (10).

Radiographic stage of RDS Chest X-ray ndings
Stage I Fine homogenous ground glass
shadowing
Stage II Bilateral widespread air bronchogram
Stage III Conuent alveolar shadowing
Stage IV Alveolar shadowing obscuring Fig. 3 Normal transabdominal LUS image, no echogenicity in
cardiac border the retrophrenic area can be seen with mirror image in both side of
echogenic phrenopulmonic border (arrow).

Please cite this article in press as: El-Malah H-EDGM et al., Lung ultrasonography in evaluation of neonatal respiratory distress syndrome, Egypt J Radiol Nucl Med
(2015), http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
 ARTICLE IN PRESS
Lung ultrasonography in evaluation of neonatal respiratory distress syndrome
LUS ndings of RDS: when the lung parenchymal disease
propagates to the pleura, an acoustic window is formed using
either a transthoracic or a transabdominal approach. This
enables transmission of an ultrasound beam and evaluation
of lung tissue. Pathological nding is presented with vertically
oriented comet-tail artifacts in the lungs, which extend from
the pleural line to the bottom of the screen. They are hypere-
chogenic, clearly dened, erase the A lines, move with lung
sliding, and are called the B lines (Figs. 4 and 5). They are a
result of the accumulation of uid in the subpleural interlobu-
lar septa surrounded by air (15,16). B-lines can be seen as indi-
vidual or multiple artifacts with a trend to coalesce into a white
lung image (ill-dened homogenous echogenic shadow) of
sicker patients (Fig. 6). RDS was diagnosed by Copetti et al.
(17) with the simultaneous presence of three ultrasound nd-
ings: abnormalities of the pleural line, white lung image, and
absence of spared areas in all lung elds. In the neonate, spo-
radic B-lines are often present after birth, especially after cesar-
ean delivery (probably because of retained lung uid), but a
white lung image is never regarded as normal. Lung consolida-
tion on ultrasonography is visualized as a subpleural echopoor
or tissue like region with blurred margins or wedge-shaped
borders (18). Therefore, signicant atelectasis or pneumonia
is the only circumstance where a real image of the lung paren-
chyma is generated by ultrasounds. Sonographic air broncho-
grams are hyperechoic linear elements representing air in
bronchioles that appear within the hypoechoic consolidated
lung (19). A vertical motion of pleural line, synchronous with
cardiac activity (the lung pulse sign) is observed in the nonven-
tilated lung or in lung atelectasis. In a neonate with RDS,
because of decreased lung aeration (atelectasis), a sound beam
of transabdominal LUS can be transmitted further beyond the
phrenopulmonic border into the lung parenchyma, where it is
Fig. 4 RDS in its 1st ultrasonographically stage is characterized by retrophrenic hyperechogenicity (B lines) diverging radially (arrow),
observed only on expiration. (A) inspiration, (B) expiration.
Fig. 5 RDS in its 2nd stage is characterized ultrasonographically by retrophrenic (B lines), seen on inspiration, which merge together
into areas of homogenous echo enhancement (white lung) on expiration (arrow). (A) inspiration, (B) expiration.
Please cite this article in press as: El-Malah H-EDGM et al., Lung ultrasonography in evaluation of neonatal respiratory distress syndrome, Egypt J Radiol Nucl Med
(2015), http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
3
then completely reverberated. Lung parenchymal echogenicity
varies the phase of the respiration cycle. Transabdominal LUS
ndings severities were classied into 3-stage scale (20,21)
(Table 2, Figs. 46).
2. Aim of the work
This study aimed to evaluate diagnostic ability of lung ultraso-
nography (LUS) in detection of pulmonary manifestations of
neonatal respiratory distress syndrome as well as follow up
the response to treatments.
3. Patients and methods
This prospective study was carried out at Pediatric Asyut Uni-
versity Hospital from January 2013 till August 2014. LUS
examination was done for one hundred neonates (66 male
and 44 female). The age of neonates ranged from 36 weeks
of gestation to full term (mean value 37.86; birth weight ranged
from 2100 g to 3000 g mean value: 2400 g. LUS examinations
were performed by radiologists, using a7.5 MHz linear probe
and 5 MHz convex probe (Sonoline Adara, Siemens, Erlangen,
Germany) for both transthoracic and transabdominal
approaches respectively. Clinical evaluation of the included
newborns was performed using the Clinical Risk Index for
Babies score (CRIB). Scores are given for birth-weight, gesta-
tional age, maximum and minimum fraction of inspired oxy-
gen and maximum base excess during the rst 12 h, and the
presence of congenital malformations. All LUS ndings of
RDS were recorded. Follow-up LUS examinations were per-
formed till completely normal neonatal lung scans were
obtained and discharged from the hospital, or the eventual
 ARTICLE IN PRESS
4 H.E.-D.G.M. El-Malah et al.
Fig. 6 RDS in its 3rd stage is characterized ultrasonographically by retrophrenic white lung (arrow) observed irrespective of respiratory
phase. (A) inspiration, (B) expiration.
Table 2 Transabdominal LUS stages of RDS severity (20,21).
Stage LUS ndings
Stage I Retrophrenic striped patterns of hyperechogenicity
(B lines) diverging radially, observed only on expiration
Stage II Retrophrenic striped patterns of hyperechogenicity
diverging radially, observed only on inspiration,
also merging together into areas of homogenous
echo enhancement on expiration
Stage III Retrophrenic homogenous hyperechogenicity (white lung)
observed irrespective of respiratory phase
fatal outcome. Persistent of abnormal LUS ndings after ten
days of follow up was diagnosed as complicated cases. The fol-
low up duration ranged from 48 h till 14 days. The average
time of LUS examinations was 34 min. Ultrasound gel was
kept warm before the examinations for avoiding neonate ther-
mal loss. The diagnosis of RDS was established and its stage of
severity was determined on the basis of the 4-stage radio-
graphic scale. The evaluation of chest radiograms carried out
by another radiologist not aware by ultrasonographic ndings.
3.1. Inclusion and exclusion criteria
3.1.1. Inclusion criteria
Neonates with clinical and radiographic signs of neonatal
respiratory distress within rst 24 h of life were included in this
study.
3.1.2. Exclusion criteria
Neonates with multiple congenital anomalies and or sever
gross retardation were excluded from this study.
3.2. Patient preparation
No special preparation, sedation, food or uid restrictions
were needed.
3.3. Ethics approved
The study protocol was approved from the ethics committee of
Faculty of Medicine Asyut University. Written informed con-
sent was not necessary as LUS is non-invasive procedure and
requested as routine examination.
Please cite this article in press as: El-Malah H-EDGM et al., Lung ultrasonography in evaluation of neonatal respiratory distress syndrome, Egypt J Radiol Nucl Med
(2015), http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
3.4. Technique
3.4.1. Imaging protocol
The transthoracic LUS approach was done by a 7.5 MHz
linear probe included examination in supine and both lateral
decubitus positions of the anterior lung area (between the ster-
num and the anterior axillary line), lateral lung area (between
the anterior and posterior axillary lines), and posterior lung
area (between the posterior axillary line and the spine) in cau-
do-cranial direction. The transabdominal LUS by a 5 MHz
convex probe included the transhepatic and transsplenic
approach in supine position to examine both lung bases.
Longitudinal, transverse and oblique scans were included. A
routine plain chest X-ray obtained to each neonate just before
performing initial ultrasound. LUS was done immediately
after every chest X-ray was requested for follow up the
response of administrative therapy.
3.4.2. Statistical analysis
LUS ndings were compared with chest plain radiographic
ndings as standard radiological examination. Statistics was
performed using true positive, true negative, false positive,
false negative, sensitivity and specicity values.
4. Results
Trans-thorax LUS was done for 600 lung areas (100 right ante-
rior RA, 100 right lateral RL, 100 right posterior RP, 100 left
anterior LA, 100 left lateral LL and 100 left posterior LP). RA
lung areas had positive LUS ndings in 10 neonates, LA areas
affected in 8 neonates, RL areas in 18 neonates, LL lung areas
in 17, RP lung areas in 48 neonates and LP lung areas in 52
neonates. Trans-abdominal LUS was done for 200 lung bases
(100 in each side). Right lung bases had positive LUS ndings
in 83 neonates, left lung bases on 79 neonates and bilateral
lung bases affected on 58 neonates. Stage I LUS ndings with
B-lines during only expiration and normal LUS during expira-
tion were found in 32 neonates, stage II with B-line during
inspiration and white lung during expiration in 44 neonates
while stage III with white lung during inspiration and expira-
tion in 22 neonates. In comparison with chest X-ray the
LUS had sensitivity 98% and specicity 92% in detection of
pulmonary manifestations of RDS. Out of 8 neonates were
diagnosed by LUS as RDS, 4 were congenital pneumonia
and 4 neonates had normal chest X-ray ndings. Two neonates
had normal LUS while on plain radiography had stage I plain
 ARTICLE IN PRESS
Lung ultrasonography in evaluation of neonatal respiratory distress syndrome
Table 3 Comparison of results obtained by ultrasonography
and plain radiography.
RDS severity stage RDS severity stage
assessed on LUS assessed on CXR (N = 98)
(N = 98)
I (n = 32) I n = 28 (87.5%)
False positive result on US n = 4 (12.5%)
II (n = 44) I n = 6 (13.6%)
II n = 35 (79.5%)
III n = 1 (2.3%)
False positive result on US n = 2 (4.6%)
III (n = 22) II n = 2 (9%)
III n = 13 (59%)
IV n = 5 (23%)
False positive result on US n = 2 (9%)
radiography ndings. LUS stages I, II correlated with plain
radiography stage I, II respectively, while stage III LUS corre-
lated with stage III and IV plain radiography (Table 3). Signif-
icant correlation between the stages of RDS assessed by the
ultrasound method and by chest radiography was observed
within the all stages. No statistically signicant differences
between right and left lungs were noted on LUS ndings.
Complete lung aeration with complete disappearance of
white lung, B-lines and returned normal pleural lung sliding
sign and A-lines were seen in the rst 48 h follow up in 58 neo-
nates, after 72 h follow up in 20 neonates and after one week
follow up in 11 neonates. Persistent positive LUS of RDS after
ten days suggesting complicated RDS was found in 5 neonates.
In comparison with CXR LUS had 100% sensitivity and 94%
specicity in follow up the response of treatment. Neonatal
death occurred in 4 patients within rst 72 h from sever
neonatal sepsis and complications of RDS.
5. Discussion
Chest radiography has been considered to be the standard
radiological diagnostic tool for RDS, and the four-stage scale
of RDS severity based on radiographic ndings correlates clo-
sely with the actual disease severity (6,8,17). In some clinical
practice there is a need for exposing a neonate to ionizing
radiation in order to evaluate effectiveness of administered
therapy, and this carries the risk for long-term adverse effects
(22). In recent years, LUS has strengthened its role in the eval-
uation of many neonatal diseases including RDS (23,24, 25).
This is supported by the fact that neonates have a thinner tho-
racic wall, and smaller width of the thorax and lung volume,
which enables a better image quality and visualization of
almost the entire surface of the lungs when compared to the
adult population. Lack of contraindications for ultrasound
examination, its low costs and patient safety have contributed
a lot to the clinical and diagnostic utility of the method (26). In
our study the LUS had high sensitivity value (98%) in
detection of lung manifestations of RDS; however LUS had
relatively low specicity (92%) so showed tendency of over
diagnosis of RDS. In this study LUS had the ability to suggest
a complete re-expansion of the lungs, based on the presence of
the lung sliding sign, as well as A-lines that consistent with
Please cite this article in press as: El-Malah H-EDGM et al., Lung ultrasonography in evaluation of neonatal respiratory distress syndrome, Egypt J Radiol Nucl Med
(2015), http://dx.doi.org/10.1016/j.ejrnm.2015.01.005
5
other studies (23,27). In follow up RDS, lung ultrasonography
had high sensitivity in comparison with CXR for evaluation of
full lung aeration responding to administrated therapy and
also had prognostic value as persistent of retrophrenic echog-
enicity enhancement by trans-abdominal LUS or sub-pleural
abnormality by trans-thoracic approach beyond 10 days
follow up correlated with chronic complications and bron-
cho-pulmonary dysplasis that consistent with other studies
(26,28).
LUS is a dynamic diagnostic procedure which enables one
to perform and observe real time images of the organ
movements, synchronized with the respiratory cycle. Thus
the ultrasound method may demonstrate areas of decreased
lung aeration more reliably owing to its dynamic nature. The
ultrasound method for dynamic assessment of the degree of
lung aeration may perhaps become a technique that not only
complements, but even conrm information obtained by
means of CXR in cases of RDS with inconclusive radiographic
ndings. Many studies evaluated intra-uterine LUS in predica-
tion of RDS depending upon evaluation of many parameters
as fetal lung volume with pulmonary artery resistance index
(29), or abdomen to thoracic ratio (30). Performing an initial
chest X-ray is essential for the differential diagnosis of
respiratory disorders in neonates, but it may be replaced by
ultrasound examination in monitoring the effects of adminis-
tered therapy. This may signicantly reduce the number of
chest X-rays being performed and ultimately result in lower
exposure of a neonate to ionizing radiation.
6. Conclusion
The LUS can be an alternative diagnostic imaging modality
for chest X-ray in follow up neonates with RDS and
subsequent reduction dose of radiation.
Conflict of interest
None declared.
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