ARTICLE

Use of Neonatal Chest Ultrasound to Predict

Noninvasive Ventilation Failure
AUTHORS: Francesco Raimondi, MD, PhD,a Fiorella WHAT’S KNOWN ON THIS SUBJECT: Lung ultrasound outperforms
Migliaro, MD,a Angela Sodano, MD,a Teresa Ferrara, MD,a conventional radiology in the emergency diagnosis of
Silvia Lama, MD,a Gianfranco Vallone, MD,b and Letizia pneumothorax and pleural effusions. In the pediatric age, lung
Capasso, MDa ultrasound has been also successfully applied to the fluid-to-air
aDivision of Neonatology, Section of Pediatrics, Department of
transition after birth and to rapid pneumonia diagnosis.
Translational Medical Sciences, and bDivision of Pediatric
Diagnostics, Department of Biomorphological and Functional
WHAT THIS STUDY ADDS: Nasal ventilation has dramatically
Sciences, Università “Federico II,” Naples, Italy
decreased the need for invasive mechanical respiratory support.
KEY WORDS
This study demonstrates that, after a short trial on nasal
ultrasonography, lung, neonate, distress
continuous positive airway pressure, lung ultrasonography
ABBREVIATIONS
reliably predicts the failure of noninvasive ventilation unlike the
CI—confidence interval
FN—false-negative conventional chest radiogram.
FP—false-positive
nCPAP—nasal continuous positive airway pressure
NIV—noninvasive ventilation
NPV—negative predictive value
PPV—positive predictive value
RD—respiratory distress abstract
TN—true-negative
TP—true-positive
BACKGROUND: Noninvasive ventilation is the treatment of choice for
neonatal moderate respiratory distress (RD). Predictors of nasal ven-
Dr Raimondi conceived and designed the study, drafted the
initial manuscript, and approved the final manuscript as tilation failure are helpful in preventing clinical deterioration. Work on
submitted; Drs Migliaro and Sodano carried out the initial neonatal lung ultrasound has shown that the persistence of a hyper-
analyses, performed the ultrasound scans, and reviewed and echogenic, “white lung” image correlates with severe distress in the
revised the manuscript; Dr Vallone reviewed the ultrasound
scans and the chest radiographs as a third, masked observer; preterm infant. We investigate the persistent white lung ultrasound
Drs Ferrara and Lama designed the data collection instruments, image as a marker of noninvasive ventilation failure.
coordinated and supervised data collection, and provided
statistical support; and Dr Capasso critically reviewed the
METHODS: Newborns admitted to the NICU with moderate RD and sta-
manuscript and approved the final manuscript as submitted. bilized on nasal continuous positive airway pressure for 120 minutes
www.pediatrics.org/cgi/doi/10.1542/peds.2013-3924 were enrolled. Lung ultrasound was performed and blindly classified
doi:10.1542/peds.2013-3924 as type 1 (white lung), type 2 (prevalence of B-lines), or type 3
Accepted for publication Jul 24, 2014
(prevalence of A-lines). Chest radiograph also was examined and
graded by an experienced radiologist blind to the infant’s clinical
Address correspondence to Francesco Raimondi, MD, PhD,
Division of Neonatology, Section of Pediatrics, Department of condition. Outcome of the study was the accuracy of bilateral type
Translational Medical Sciences, Università “Federico II”, via 1 to predict intubation within 24 hours from scanning. Secondary
Pansini 5, 80131 Napoli, Italy. E-mail: raimondi@unina.it outcome was the performance of the highest radiographic grade
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). within the same time interval.
Copyright © 2014 by the American Academy of Pediatrics
RESULTS: We enrolled 54 infants (gestational age 32.5 6 2.6 weeks;
FINANCIAL DISCLOSURE: The authors have indicated they have birth weight 1703 6 583 g). Type 1 lung profile showed sensitivity
no financial relationships relevant to this article to disclose.
88.9%, specificity 100%, positive predictive value 100%, and negative
FUNDING: No external funding.
predictive value 94.7%. Chest radiograph had sensitivity 38.9%, spec-
POTENTIAL CONFLICT OF INTEREST: The authors have indicated
ificity 77.8%, positive predictive value 46.7%, and negative predictive
they have no potential conflicts of interest to disclose.
value 71.8%.
CONCLUSIONS: After a 2-hour nasal ventilation trial, neonatal lung ul-
trasound is a useful predictor of the need for intubation, largely out-
performing conventional radiology. Future studies should address
whether including ultrasonography in the management of neonatal
moderate RD confers clinical advantages. Pediatrics 2014;134:1–6

PEDIATRICS Volume 134, Number 4, October 2014 1

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Chest ultrasound has recently been
applied with success in different set-
tings of adult medicine, ranging from
cardiopulmonary emergencies and
trauma surgery to the care of pre-
eclamptic women or patients with renal
failure.1–4
A systematic ultrasound semeiology
has been validated across a wide span
of ages using both chest anatomic
structures (ie, the ribs or the pleural
line) and artifactual images, such as the
B-lines, that are discrete, laserlike
vertical hyperechoic reverberations
arising from the pleural line. Multiple
diffuse bilateral B-lines are suggestive
of interstitial syndrome (eg, pulmonary
edema, interstitial pneumonia, diffuse
parenchymal lung disease)5 (Fig 1A). In
the neonate, one can accurately dif-
ferentiate the aerated dry lung,
appearing as uniform hypoechogenic
pattern, sliding with respiration and
often showing horizontal reverber-
ations of the pleural image (the A-lines)
(Fig 1B) from the hyperechogenic
“white” pattern of the markedly “wet”
or inflamed organ (Fig 1C)6–8
Noninvasive ventilation (NIV) is widely
used for the treatment of moderate re-
spiratory disease of the newborn to
stabilize spontaneous breathing while
avoiding the complications of invasive
ventilation.9,10 NIV-assisted infants are
more easily accessed by parents and
health care givers, allowing an optimi-
FIGURE 1
A, The prevalence of B-lines (arrows) has been linked to the interstitial syndrome in the adult and to a progressive aeration of the neonatal lung after birth. B,
Reverberations of the pleural image (also known as A-lines) in the normally aerated lung. C, White-lung image soon after birth; its persistence has been linked to
the inflamed lung with hyaline membrane disease.
2 RAIMONDI et al
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zation also of nonventilatory strategies.
However, clinical monitoring of these
infants is needed, as some will pro-
gressively show increased respiratory
effort and/or deterioration of blood
gas exchange requiring endotracheal
intubation, surfactant administration,
and mechanical ventilation. At present,
there is a need for reliable predictors of
NIV failure that would spare the infant
becoming exhausted from ineffective
breathing. As clinics and chest radio-
graphs are often discordant in grading
the severity of neonatal respiratory
distress syndrome, conventional radi-
ology is often of little help. On the other
hand, the persistence of a “white-lung”
ultrasound image has been shown to
correlate with clinical respiratory dis-
tress (RD) in preterm infants.11 In the
present study, we hypothesized that this
marker may predict the failure of nasal
continuous positive airway pressure
(nCPAP) in aerating the premature lung,
heralding the need for a more invasive
approach.
METHODS
The study was conducted from December
2012 to July 2013 in a level 3 hospital
with 2400 total births per year. The in-
vestigation received permission from the
local institutional review board and for-
mal consent was obtained from the
parents. Newborns were enrolled if ad-
mitted to the NICU for moderate RD and
treated with nCPAP. These criteria in-
cluded infants of any degree of pre-
maturity who had mild symptoms
(tachypnea, shallow breathing, grunting,
nasal flaring, sub- and intercostal re-
tractions) before stabilization on nCPAP
(+4–5 cm H2O and FiO2 ,0.4 to keep ox-
ygen saturation in the 92%–96% range,
with a respiratory rate ,60/min and
pH .7.28, PaO2 .50 mm Hg, PaCO2
,60 mm Hg).12 Infants with major con-
genital malformations and those intu-
bated in the delivery room or within
20 minutes after admission to the NICU
were excluded from the study.
Failure of NIV was defined as endotra-
cheal intubation and surfactant ad-
ministration (Curosurf, Parma, Italy;
200 mg/kg) without attempting further
NIV strategies. This procedure was
eventually performed by the attending
neonatologist, who was blind to the
study, in case chest dynamics were
deteriorating (evidence of severe
upper/lower chest or xyphoid retrac-
tions, marked nares dilatation, or ex-
piratory grunting) and/or if the infant
failed to maintain adequate blood gas
values as reported previously.
At admission, infants were placed on
nCPAP in an incubator and vascular
access was established. After 120
minutes from nCPAP application, lung
ultrasound images were acquired
scanning each lung in the anterior and
lateral projections with the infant in the

supine position. This time point was
chosen because it is the conventional
time limit for early versus late surfac-
tant rescue13 and because of experi-
mental animal evidence that lung fluid
clearance is accomplished in 2 hours.14
A broadband linear transducer (mod
L12–5; Philips, Eindhoven, Netherlands)
that encompasses the superior and
inferior lung fields in the same image
was used. Images were classified as
type 1 (white lung), type 2 (prevalence
of B-lines), and type 3 (prevalence of
A-lines), as previously described.15
Chest radiographs were acquired in the
same time frame with a portable device
(Practix 33 plus; Philips, Eindhoven,
Netherlands) at the infant’s incubator.
Images were classified as grade 1 (fine
homogeneous ground glass shadow-
ing), grade 2 (addition of widespread air
bronchograms), grade 3 (development
of confluent alveolar shadowing), and
grade 4 (complete white-out of the lung
fields with obscuring of the cardiac
border in the most severe cases).16
To ensure proper blinding, lung ultra-
sound scans and chest radiographs
were coded when acquired in the NICU
and classified as previously described
by an experienced pediatric radiologist
who was blind to the infants’ clinical
condition. Blind evaluation of coded
lung scans was also performed by an
experienced neonatologist to assess
interobserver variability. The main
outcome of the study was the accuracy
of the sonographic profile with maxi-
mal echodensity (type 1 or white lung)
to predict intubation within 24 hours
from scanning. The secondary outcome
was the accuracy of the highest radio-
graphic grade to predict intubation
within the same time interval.
Statistics
In a nursery setting,15 a type 1 lung ul-
trasound profile had a 77.7% sensitivity
in predicting the need of ventilatory
support shortly after birth. We calcu-
PEDIATRICS Volume 134, Number 4, October 2014
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lated that a population of 54 preterm
neonates was required to estimate the
99% confidence intervals (CIs) for
a sensitivity of type 1 lung ultrasound
profile of 85.0% 6 12.5%. We defined
true-positive (TP) as type 1 and intu-
bated; true-negative (TN) as type 2 or 3
and not intubated; false-positive (FP) as
type 1 and not intubated; false-negative
(FN) as type 2 or 3 and intubated. The
specificity of the test was defined as
TN/(TN+FP); sensitivity was TP/(TP+FN);
positive predictive value (PPV) was
TP/(TP+FP); negative predictive value
(NPV) was TN/(TN+FN). Ninety-five per-
cent CIs around measures of test char-
acteristics were calculated by using the
normal distribution mode, according to
the following formula:
sample  value 6 1:96 3 standard  error:
The k coefficient was also provided to
assess the interobserver variability.
Our cohort was divided by gestational
age (.29 weeks vs ,29 weeks); P
values to show differences between
these groups were calculated by using
Student t test for continuous variables
and exact x2 test for categorical vari-
ables. A level of P , .05 was chosen as
statistically significant.
RESULTS
A total of 72 neonates presented with RD
and were initially treated with nCPAP; 18
were excluded because of endotracheal
intubation before entering the NICU (15
infants) or within 20 minutes from ad-
TABLE 1 Demographic Characteristics of the Study Cohort
Characteristics
Mean birth weight, g (SD)
Cesarean delivery
Apgar ,7 @ 1 min
Apgar ,7 @ 5 min
ROM .12 h
Prenatal steroids, 2 doses
Failed nCPAP
PaO2 at intubation (SD)
PaCO2 at intubation (SD)
GA, gestational age; N/A, not applicable; ROM, rupture of membranes.
ARTICLE
mission. Fifty-four infants were then
enrolled in the study; their demographic
characteristics are shown in Table 1.
There was no significant difference be-
tween infants who succeeded or failed
nCPAP (data not shown). Based on lung
ultrasound scan after 120 minutes on
nCPAP, 24 neonates were assigned to
type 3, 12 to type 2, and 16 to type 1. The
remaining 2 neonates showed a type 1
on one side and type 2 on the other. All
newborns with either unilateral or bi-
lateral type 1 were intubated after an
average interval of 6 hours. No infant
with type 2 or type 3 profile was in-
tubated. In predicting failure of NIV,
bilateral type 1 had the following ac-
curacy: sensitivity 88.9% (CI 67.2–96.8),
specificity 100% (CI 94.9–100), PPV 100%
(CI 80.6–100), NPV 94.7% (CI 82.7–98.5).
On the basis of the chest radiograph, no
infant was assigned to grade 4 or 3,
whereas 15 neonates were assigned to
grade 2 and 39 to grade 1. The accuracy
of grade 2 to predict intubation was as
follows: sensitivity 38.9% (CI 20–61.1),
specificity 77.8% (CI 61.7–88.5), PPV
46.7% (CI 24.8–69.9), NPV 71.8% (CI 56.2–
83.4). Concordance of ultrasound and
radiographic results is shown in Table 2.
There was full interobserver agreement
in the images’ interpretation (k = 1).
The average duration of a complete ul-
trasound scan was 2.5 minutes and
the examination was well tolerated by
enrolled patients. All scans showed
a normal pleural line and sliding sign;
no air-leak syndromes were docu-
mented throughout the study.
GA ,29 wk n = 10 GA .29 wk n = 44 P
1080 (94) 1810 (253) 0.10
7 26 0.41
3 9 0.43
0 0 N/A
2 6 0.26
0 28 0.35
4 14 0.25
41.1 (1.8) 46.3 (2.1) 0.08
70.3 (3.1) 68.0 (3.2) 0.12
3
TABLE 2 Concordance of Ultrasound and Radiographic Results nate to a level 3 NICU has to be carefully
Ultrasound Result Radiographic Result planned in advance.
Grade 4 Grade 3 Grade 2 Grade 1 There is a paucity of data on techniques
Type 1 0 0 7 9 or parameters that monitor RD reliably
Type 2 0 0 6 6 enough to predict intubation. A clinical-
Type 3 0 0 2 22
Type 1/2 0 0 0 2
radiologic correlation was attempted
by Kero and Mäkinen22 in 55 preterm
infants (mean gestational age: 33
DISCUSSION cation of lung ultrasound. This in- weeks) with mild, moderate, and se-
Our data show that, unlike the con- formation is rapidly obtained at the vere RDS. It is not clear whether the
ventional radiograph, lung ultrasound bedside without any radiation expo- investigation was properly masked,
can accurately predict those newborns sure and can be acquired with a fairly but they report a 38% general dis-
with RD who will fail NIV (Fig 2). In the steep learning curve.5 In the study by agreement between clinical and ra-
NICU setting, our work marks a novel Shah et al,21 only 60 minutes of training diologic criteria and only a 50%
approach to both neonatal respiratory was needed to accurately diagnose agreement rate on moderate RDS. The
management and lung ultrasonogra- pneumonia in children, outperforming same radiologic criteria were used in
phy. Previous authors had described conventional chest radiographs. Using association with clinical intubation
ultrasound signs for hyaline mem- lung ultrasonography as an NIV failure predictors in a large retrospective co-
brane disease,11 transient tachypnea of predictor can be particularly useful for hort by Ammari et al.23 None of the 3
the newborn,17 pneumonia,18 pneumo- level 1 and 2 nurseries where limited variables associated with CPAP failure
thorax,19 and pleural effusion.20 We respiratory support may be occasion- (positive pressure ventilation at birth,
provide evidence to a functional appli- ally available but transferring a neo- an alveolar-arterial oxygen tension

FIGURE 2
Compared chest ultrasound and radiograph of 31-week twins on CPAP because of moderate RD after birth. Twin 1 was intubated and received a surfactant dose;
twin 2 transitioned to room air. Lung ultrasound showed uniform hyperechogenicity for twin 1 (B) and A-lines for twin 2 (D). Both radiographs showed ground
glass opacity and bronchograms (A–C).

4 RAIMONDI et al
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gradient .180 mm Hg and severe RDS
on the initial chest radiograph) had
a positive predictive value .55%. A
different clinical predictor, such as the
maximal oxygen requirement in the
first 72 hours of life, was studied by
Morosini and Davies24 in a retrospec-
tive cohort of 592 infants with a gesta-
tional age .32 weeks and any cause of
RD. They found that a maximal FiO2
$0.5 gave a PPV of 60% and NPV of
100% (sensitivity = 0.93, specificity =
0.91) for need for intubation and in-
termittent positive pressure ventila-
tion. From their data, however, it is
unclear exactly when this maximal ox-
ygen requirement was reached before
intubation. The lack of this piece of in-
formation and of prospective valida-
tion are important limits to the
practical application of this interesting
article. Boo et al25 prospectively in-
vestigated 97 consecutive preterm
infants (,37 weeks) with an un-
specified level of nCPAP: pneumothorax
and sepsis during treatment were
significant CPAP failure predictors. In
the adult, lung ultrasonography also
has been proven a useful predictor of
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 Use of Neonatal Chest Ultrasound to Predict Noninvasive Ventilation Failure
Francesco Raimondi, Fiorella Migliaro, Angela Sodano, Teresa Ferrara, Silvia Lama,
Gianfranco Vallone and Letizia Capasso
Pediatrics originally published online September 1, 2014;

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 Use of Neonatal Chest Ultrasound to Predict Noninvasive Ventilation Failure
Francesco Raimondi, Fiorella Migliaro, Angela Sodano, Teresa Ferrara, Silvia Lama,
Gianfranco Vallone and Letizia Capasso
Pediatrics originally published online September 1, 2014;

The online version of this article, along with updated information and services, is
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http://pediatrics.aappublications.org/content/early/2014/08/26/peds.2013-3924

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