Accepted Manuscript

Lung Ultrasonography to Diagnose Transient Tachypnea of the Newborn

Jing Liu, M.D., PhD, Xin-Xin Chen, M.D., Xiang-Wen Li, M.D., Shui-Wen Chen, M.D.,
PhD, Yan Wang, M.D., PhD., Zhi-Chun Feng, M.D

PII: S0012-3692(16)00441-4
DOI: 10.1016/j.chest.2015.12.024
Reference: CHEST 226

To appear in: CHEST

Received Date: 15 September 2015

Revised Date: 15 November 2015
Accepted Date: 18 December 2015

Please cite this article as: Liu J, Chen XX, Li XW, Chen SW, Wang Y, Feng ZC, Lung Ultrasonography
to Diagnose Transient Tachypnea of the Newborn, CHEST (2016), doi: 10.1016/j.chest.2015.12.024.

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 ACCEPTED MANUSCRIPT
Word count
Abstract: 236
Text: 2386

Lung Ultrasonography to Diagnose Transient Tachypnea of the Newborn

Jing Liu, M.D., PhDXin-Xin Chen, M.D.,Xiang-Wen Li, M.D.,Shui-Wen Chen, M.D., PhDYan Wang, M.D.,
PhD., Zhi-Chun Feng,M.D.

Department of Neonatology and NICU of Bayi Childrens Hospital, Beijing Military General HospitalBeijing

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100700, China

Corresponding Author: Pro.Dr. Jing Liu, MD, PhD.

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Department of Neonatology & NICU of Bayi Childrens Hospital, Beijing Military General Hospital
No.5 Nanmen Cang, Dongcheng District

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Beijing 100700, China
E-mail: liujingbj@live.cn

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Short Title: Diagnosis of TTN Using LUS
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Finlacial disclosures
The authors have no financial relationships relevant to this article to disclose.
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Funding source:
This work was supported by the Clinical Research Special Fund of Wu Jieping Medical
Foundation (320.6750.15072).
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Conflict of Interest Statement: No

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Abbreviations:
TTNTransient Tachypnea of the NewbornNICUneonatal intensive care unit; RDSrespiratory
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distress syndromeMASmeconium aspiration syndrome; AIS=alveolar-interstitial syndrome

Contributors Statements:
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Prof. Dr.Jing Liu: contributed to the study conception, ultrasound examination, data analysis, write and
approval of the manuscript.
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Dr Xin-Xin Chen:contributed to clinical data analysis, manuscript preparation, and approval of the final
manuscript.
Dr Xiang-Wen Li: contributed to clinical data analysis, manuscript preparation, and approval of the final
manuscript.
Dr Yan Wang: contributed to clinical data collection, manuscript revision, and approval of the final
manuscript.
Dr Shui-Wen Chen:contributed to data collection, manuscript revision, and approval of the final
manuscript.
Prof. Zhi-Chun Feng: contributed to data collection, manuscript revision, and approval of the final
manuscript.
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Abstract
BACKGROUND This study aimed to explore the sensitivity and specificity of ultrasound for the
diagnosis of transient tachypnea of the newborn (TTN).

Methods The ultrasound was done by one export.The patients were placed in a supine,lateral recumbent,
or prone position.The probe was placed perpendicular or parallel to the ribs, and each region of the lung
was scanned.The scan results were compared to conventional chest X-ray results.

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Results A total of 1,358 infants were included in this study, we identified 412 cases without pulmonary
diseases,228 TTN cases, 358 respiratory distress syndrome (RDS) cases,85 meconium aspiration

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syndrome (MAS) cases, 215 infectious pneumonia cases,and 60 other cases.The primary ultrasonic
characteristic of TTN was pulmonary edema.White lung or compact B-line were only observed in

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severe cases,whereas mild TTN primarily presented as pulmonary interstitial syndrome or double lung
point.Furthermore,Double lung point could appear during the recovery period of severe TTN or RDS,
MAS, and pneumonia.Lung consolidation with air bronchograms were not observed in TTN patients.The

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results showed that white lung/compact B-line exhibited a sensitivity of 33.8% and a specificity of 91.3%
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in diagnosing TTN,whereas double lung point exhibited a sensitivity of 45.6% and a specificity of 94.8%
in diagnosing severe TTN.
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Conclusion Pulmonary edema,AIS,double lung point,white lung and compact B-line are the primary
ultrasound characteristics of TTN.Ultrasonic diagnosis of TTN bases on these findings is accurate and
reliable.TTN can be ruled out in the presence of lung consolidation with air bronchograms.
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Keywords: lung ultrasound, transient tachypnea syndrome, pulmonary edema, pulmonary interstitial
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syndrome, double lung point, white lung, compact B-line, infant, newborn
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Introduction
Transient tachypnea of the newborn (TTN), also known as wet lung, is one of the most common causes of
dyspnea in newborns. Some epidemiological studies indicate that the incidence of TTN is 4-5.7% in full-
term newborns and 10% in preterm infants.1 Although TTN rarely leads to neonatal death, it must be
accurately differentiated from other causes of dyspnea, such as respiratory distress syndrome (RDS),
meconium aspiration syndrome (MAS), pneumonia, and congenital heart disease, among others, to aid in
the correct management of TTN. Generally, TTN is primarily diagnosed based on medical history, typical

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clinical presentation, arterial blood gas analysis, and chest X-ray examination, among other factors, and
lung ultrasound is typically not included in the diagnostic work-up of TTN. Recently, chest ultrasound has
been used in the diagnosis of many types of neonatal and children's lung diseases, including RDS, MAS,

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pneumonia and atelectasis.2,3 However, there exists limited literature concerning the diagnosis of TTN
using lung ultrasound. This study aimed to use a large series of lung ultrasonography findings to

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characterize the ultrasound imaging features of TTN and to explore the specificity and sensitivity of lung
ultrasonography for the diagnosis of TTN.

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Materials and Methods
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Study Subjects
The institutional review board of the Beijing Military General Hospital approved the study protocol
(number 2011-LC-Ped-01). This was a retrospective series study that included a total of 1,358 newborn
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infants hospitalized in the neonatal intensive care unit (NICU) of the Bayi Childrens Hospital, affiliated
with Beijing Military General Hospital, from January to December 2014 who underwent lung
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ultrasonography. All of the lung ultrasonography examinations were performed by one doctor, the clinical
data were collected by different doctors, and the ultrasound operator was blinded to the clinical condition
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of the neonates.
The diagnostic criteria for TTN are as follows:1,4 (1) typical clinical symptoms: rapid, labored
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breathing of more than 60 breaths a minute within the first several hours after birth, grunting or moaning
sounds when the baby exhales, flaring nostrils, retractions and cyanosis around the mouth and nose; (2)
chest x-ray findings: prominent perihilar pulmonary vascular markings, flattening of the diaphragm, and
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fluid in the horizontal fissure of the right lung; and (3) exclusion and vigilance other reasons for
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respiratory distress. Patients who required mechanical ventilation support (including invasive or
noninvasive) were defined as having severe TTN, whereas those who needed supplemental oxygen but not
mechanical ventilation were defined as having mild TTN.

Lung Ultrasound Examination Methods

Instruments: GE Voluson E6E8 and Logiq C9 ultrasound equipment was used. The frequency of the
linear array probe was 10-14 MHz.

Examination Method: In a resting state, each patient was placed in a supine, lateral recumbent, or prone
position. Using the anterior and posterior axillary lines as boundaries, each side of the lung was divided
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into three regions: anterior, lateral, and posterior. The probe was perpendicular or parallel to the ribs, and
each region of both sides of the lung was scanned.

Observation Indices: (1) Pleural line: On an ultrasound, the organ and the parietal pleura present as
smooth, regular, linear hyperechoic echoes, namely the pleural line.5 (2) A-line: Due to the horizontal
artifacts formed by the multiple reflections generated by the differences in acoustic impedance of the
pleura-lung interface, the ultrasound reveals a series of linear hyperechoic echoes that are parallel to and
below the pleural line and are equidistant from each other.6 (3) B-line: Line-like artifacts originating from

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and perpendicular to the pleural line that present as radial divergence to the deep parts of the lung field.7 (4)
Lung consolidation: On the ultrasound, this presents as hepatization and may be accompanied by air

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bronchograms or fluid bronchograms of the lung tissues.5 (5) White lung: Characterized by compact
B-line or A-line disappearance in all six regions of the lung. Compact B-line refers to a type of

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ultrasonography in which the dense existing B-line makes the acoustic shadows of the ribs in the entire
scan area disappear when the probe scans in a direction that is perpendicular to the ribs. White lung and
compact B-line are manifestations of severe alveolar-interstitial syndrome (AIS) and are caused by the

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presence of a large amount of lung fluid (including pulmonary interstitial and alveolar fluid).6,8 (6) AIS:
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Characterized by the presence of more than three B-lines with the disappearance of A-lines in the lung
field; however, the acoustic shadows of the ribs may also be present. Severe AIS can manifest as white
lung or compact B-line. 6,8 (7) Double lung point: the stark demarcation point that is formed between the
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upper and lower lung on an ultrasound due to the differences in the severity or nature of the lesions.9

Statistical Analysis
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SPSS 16.0 software was used to conduct the statistical analysis. Fishers exact test was used to compare
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the rate of positive neonatal ultrasound findings between the two groups. The specificity and sensitivity of
the primary examination results for diagnosing TTN were calculated based on this test, and p < 0.05 was
considered statistically significant.
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Results
General characteristics of the study population
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At the time of hospital admission, according to the patients medical histories, clinical presentations,
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arterial blood gas analyses, chest x-ray examinations, and lung ultrasound findings, there were 412
patients without lung diseases (gestational age 27+2-40+3 weeks; 228 male cases, 184 female cases; 255
delivered via vaginal delivery and 157 delivered via cesarean section; birth weight 1,280-4,220 g) and 946
cases of patients with various lung diseases (with gestational age 25+4-41+3 weeks; 491 male cases, 455
female cases; 546 delivered via vaginal delivery and 400 delivered via cesarean section; birth weight
710-5,120 g). Among the patients with lung disease, there were 228 cases of TTN, 358 RDS cases, 85
MAS cases, 215 cases of infectious pneumonia, and 60 other cases.

Ultrasonic Manifestations of TTN in the Acute Phase

(1) During the acute phase, the primary manifestation of TTN on the patients lung ultrasounds was
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pulmonary edema. The patients with severe TTN (77 cases) exhibited either white lung or compact B-line
on both sides (Figures 1.1 and 1.2), and the patients with mild TTN (151 cases) exhibited either lung AIS
(47 cases) or double lung point (104 cases) (Figures 2.1 and 2.2). (2) Pleural line abnormality was one of
the commonly observed but non-specific manifestations of TTN and presented as a thickened, blurry, or
missing line that was observed in all of the patients (100%) (Figures 1 to 2). (3) Pleural effusion occurred
in 22 of the severe cases (22/77=28.6%) and 12 of the mild cases (12/151=7.9%); among these cases,
pleural effusion occurred on either one side or both sides (Figure 3). (4) A-line disappearance was

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commonly observed in the lung fields of patients with more severe pulmonary lesions, whereas A-line
reduction was observed in the lung fields of patients with milder pulmonary lesions; these were observed
in all of the patients (Figures 1 to 3). (5) Lung consolidation with air bronchograms were not observed in

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any of the TTN patients; if they had been observed, the patients may have been diagnosed with RDS or
other lung diseases (Figure 4). See Table 1 for the incidence of several commonly observed ultrasound

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findings related to various lung diseases during the acute phase.

Ultrasonic Manifestations of TTN in the Convalescence Phase

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As the patients recovered from the disease, the degree of pulmonary edema gradually decreased. Initially,
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the ultrasound revealed the presence of white lung/compact B-line, but this finding gradually became
milder and revealed signs of AIS. During the convalescence phase, a double lung point was observed in 25
patients with severe TTN. In these cases, the pleural line gradually emerged on the A-line, pleural effusion
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disappeared, and the patients observation indices ultimately returned to normal (Figure 5). In addition, a
double lung point was observed during the convalescence phase in 7.5% (27/358) of the patients with
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RDS, 10.6% (9/85) of the patients with MAS, and 12.5% (27/215) of the patients with pneumonia.
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Sensitivity and Specificity of White Lung/Compact B-line and Double Lung Point in Diagnosing TTN
Based on the aforementioned results, the white lung/compact B-lines and double lung point were the
relative common and specific LUS findings of TTH; therefore, this study used the presence of white
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lung/compact B-line double lung point as a parameter for calculating the sensitivity (a/a+c) and specificity
(d/b+d) of ultrasonography for diagnosing severe TTN. The results indicate that white lung/compact B-
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line exhibited a sensitivity of 33.8% (95%CI=22.7%~40.3%) and a specificity of 91.3% (95%CI=88.9%~

93.4%) in diagnosing TTN (Table 2), whereas double lung point exhibited a sensitivity of 45.6% (95%CI=
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39.0% ~52.3%) and a specificity of 94.8% (95%CI=92.3%~96.7%) in diagnosing severe TTN (Table 3).

Discussion
Breathing difficulty is a common early neonatal critical illness that requires timely and appropriate
treatment. Several of the common neonatal lung diseases can cause severe neonatal breathing difficulty,
including TTN, RDS, pneumonia, pneumothorax, MAS, pulmonary hemorrhage, and congenital
diaphragmatic hernia, among others. Among these conditions, TTN is the most common cause of neonatal
dyspnea and accounts for approximately 33-50% of neonatal breathing difficulty cases.10 Early, rapid, and
accurate diagnosis is the key to correctly treating and improving the prognosis of patients with these kind
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of lung diseases.
This large sample study confirms that lung ultrasonography can be used to accurately diagnose TTN
and to differentiate it from other lung diseases. Moreover, lung ultrasonography has several advantages in
that it is simple, intuitive, reliable, and convenient for dynamic observation and bedside use. The primary
pathological characteristic of TTN is pulmonary edema, which manifests as white lung, compact B-line,
AIS, pleural line abnormality, A-line disappearance, and pleural effusion, among other signs, on
ultrasound. In the past, the presence of a double lung point was believed to be a specific and sensitive sign

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of TTN, and both its sensitivity and specificity for diagnosing TTN were reported to be 100%.9,11 However,
the present large sample case study found that the presence of a double lung point is not specific to TTN
because it can also appear in patients with diseases such as RDS, pneumonia, and MAS. Additionally, the

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sensitivity of a double lung point for TTN was not found to be 100%; it only appeared in 45.6% (95%CI=
39.0%~52.3%) of the patients who had TTN with a specificity of 94.8%(95%CI=92.3%~96.7%).

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Furthermore, we found that severe TTN manifested as white lung or compact B-line during the acute
phase and that a double lung point only occurred in some of the patients during the convalescence phase.

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This is the first study to report that white lung compact B-lines only appear during the acute phase of
severe TTN and of a small number of other lung diseases and that it has a sensitivity of 33.8% (95%CI=
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22.7%~40.3%) with a specificity of 91.3% (95%CI=88.9%~ 93.4%) in diagnosing TTN.
Pleural line abnormality and A-line disappearance were two of the most common ultrasound findings;
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these findings were observed in all of the patients. Pleural line abnormalities manifest as the thickening,
blurring, or disappearance of the pleural line. However, because pleural line abnormalities and A-line
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disappearance can also be observed in patients with other lung diseases, they are also not specific signs of
TTN.
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The results of this study indicate that pleural effusion is a common complication of pathological
changes in various types of lung diseases that is very easy to identify through ultrasonography. The present
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study found that 17.5% of patients with TTN, 15.4% of patients with RDS, 12.6% of patients with
pneumonia, and 9.4% of patients with MAS exhibited varying degrees of pleural effusion. Prior to the use
of lung ultrasonography, the identification of pleural effusion through x-ray examination was very difficult;
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this further demonstrates that lung ultrasonography is more meaningful than conventional x-ray
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examination.12-15
The present study also found that the ultrasound signs of TTN may clearly differ according to the
various lung fields. Not only did the ultrasonic manifestations of TTN differ between the two sides of the
lung, but the ultrasound signs of TTN also varied between the different lung fields on the same side of the
lung; this implies that the lung tissue water content (i.e., the degree of pulmonary edema) varies across the
different lung regions. Therefore, lung ultrasonography furthers our understanding of lung diseases such as
TTN and RDS.14,16
Additionally, the present study confirmed that lung ultrasonography in patients with TTN does not
identify changes in lung consolidation with air bronchograms, even though these changes are seen in
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patients with lung diseases such as RDS, MAS, pneumonia, and atelectasis, among others.12-20 Therefore,
if lung consolidation with air bronchograms are observed under ultrasound, TTN can be excluded.16

In conclusion, the present study involved a more in-depth investigation of the ultrasonic
characteristics of TTN and clarified the various ultrasonic manifestations of different degrees of TTN.
Severe TTN primarily manifests as white lung or a compact B-line, whereas mild TTN primarily
manifests as AIS or a double lung point. These findings contradict past findings that both the sensitivity
and specificity of identifying a double lung point in diagnosing TTN are 100%; instead, our findings

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indicate that white lung/compact B-line had a sensitivity of 33.8% and a specificity of 91.3% for
diagnosing TTN, whereas double lung point had a sensitivity of 45.6% and a specificity of 94.8% for

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diagnosing severe TTN.
Lung ultrasonography is an accurate and reliable tool for diagnosing TTN and is valuable for the

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early and differential diagnosis of TTN. In addition, ultrasound examination has numerous advantages in
that it is a simple and non-invasive procedure, does not expose patients and medical staff to radiation, can
be used at the bedside, and is appropriate for dynamic observation and therapeutic efficacy evaluation,

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among other characteristics. Therefore, it is appropriate to extensively promote the use of ultrasonography
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in neonatal intensive care units.

Limitations
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This study also had some limitations due to the inclusion of a non-consecutive sample that may not be
fully representative of all TTN patients. All of the lung ultrasound examinations were performed by one
single doctor; thus, the results may not apply in the hands of a less experienced examiner. Furthermore, we
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did not measure inter-observer or intra-observer variability. Any physician who would like to perform
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lung ultrasonography should be properly trained. As a follow-up, we aim to design a prospective study
that compares lung ultrasonography in the neonate to the final diagnosis reached by a blinded panel. This
study would provide definitive validation for the lung imaging modality.
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FIGURE LEGENDS

Figure 1 Compact B-line

The probe is perpendicular to the ribs during scanning. The dense existing B-line makes the acoustic
shadows of the ribs disappear from the entire scanned area. The pleural line thickens and blurs, and the
A-line disappears. Observed in severe TTN.

Figure 2.1. AIS

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Lung AIS was identified by the presence of three or more B-lines within the lung field. The pleural line
was abnormal, and the A-line disappeared; however, the acoustic shadows of the ribs may be present. This

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is one of the common non-specific manifestations of TTN.

Figure 2.2 Double lung point

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During ultrasonography, the lung field echoes clearly differ between the upper and lower lung. This
demarcation point is called the double lung point. Less pleural effusion was observed in this patients

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lower lung field. AN
Figure 3 Pleural effusion
Pleural effusion is one of the common manifestations of TTN. This patients ultrasound primarily reveals
AIS and pleural effusion. However, AIS and pleural effusion can also be observed in patients with other
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lung diseases. Therefore, these findings are non-specific manifestations of TTN.

Figure 4 Consolidation with air bronchograms

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Under ultrasound, two areas of significant lung consolidation with air bronchograms (arrow) were
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observed in the left lung field of this patient. Thus, the TTN could be ruled out.

Figure 5 Normal lung image

Lung tissues appear hypoechoic. The pleural line and the A-line present as smooth, clear, regular
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hyperechoic echoes with an equidistant distribution. The A-line echoes gradually weaken from the shallow
to the deep parts of the lung field until they disappear.
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VIDEO LEGENDS

VIDEO 1. Normal lung ultrasound manifestation

The clear, smooth and regular pleural line and A-lines can be easily found under ultrasound in a healthy
infant. The pleura move in a to-and-fro pattern with respiration, which is termed lung sliding.

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VIDEO 2. B-lines
The hyperechoic B line vertical to the pleural line moves with respiration, as in video 1, and the lung
sliding is much more clear here.

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VIDEO 3. Alveolar-interstitial syndrome (AIS)
There are more than three B-lines with the disappearance of A-lines in the lung field, and the acoustic

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shadows of the ribs also exist. AIS refers to the existence of lung edema.
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tool for early diagnosis. Neonatology 2008;94(1): 52-59.
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Chest, 2014;146 (2): 483-488

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[14] Liu J, Cao HY, Wang HW, et al. The role of lung ultrasound in diagnosis of respiratory distress
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[17] Stefanidis K, Dimopoulos S, Tripodaki ES, et al. Lung sonography and recruitment in patients with
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Table page

Table 1 The incidence of several commonly observed ultrasound signs

in TTN, RDS, and MAS (n,%)

Ultrasound Signs TTN(228,%) RDS(358,%) MAS(85,%) Pneumonia(215,)

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White lung/compact
B-line 77(33.8) 35(9.8) 5(5.9) 17(7.9)
Double lung point 104(45.6) 19(5.3) 6(7.1) 9(4.2)

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Pleural line
abnormality 228(100) 100(100) 85(100) 215(100)
A-line disappearance

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or reduction 228 (100) 358(100%) 85(100) 215(0)
Pleural effusion 40(17.5) 55(15.4%) 8(9.4) 27(12.6)
Lung consolidation 0(0) 358(100%) 85(100%) 215(100)

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Table 2 The sensitivity and specificity of white lung/compact B-line in diagnosing TTN
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White lung/compact B-line TTN Others* Total Sensitivity (a/a+c) Specificity (d/b+d)
Present 77(a) 57(b) 134(a+b) 33.8% 91.3%
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Not present 151(c) 601(d) 752(c+d)

Total 228(a+c) 658(b+d) 886(a+b+c+d)
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Note: *Includes the RDS, MAS and pneumonia.

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Table 3 The sensitivity and specificity of double lung point in diagnosing TTN
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Double lung point TTN Others* Total Sensitivity (a/a+c) Specificity (d/b+d)
Present 104(a) 34(b) 138(a+b) 45.6% 94.8%
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Not present 124(c) 624(d) 748(c+d)

Total 228(a+c) 658(b+d) 886(a+b+c+d)
Note: *Includes the RDS, MAS and pneumonia.
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