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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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http://dx.doi.org/10.1016/j.chest.2015.12.024


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Word count：：：：Abstract: 236；；；；Text: 2386

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.

Department of Neonatology and NICU of Bayi Children’s Hospital, Beijing Military General Hospital，Beijing

100700, China

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

Department of Neonatology & NICU of Bayi Children’s Hospital, Beijing Military General Hospital

No.5 Nanmen Cang, Dongcheng District

Beijing 100700, China

E-mail: [email protected]

Short Title: Diagnosis of TTN Using LUS

Finlacial disclosures

The authors have no financial relationships relevant to this article to disclose.

Funding source:

This work was supported by the Clinical Research Special Fund of Wu Jieping Medical

Foundation (320.6750.15072).

Conflict of Interest Statement: No

Abbreviations:

TTN＝Transient Tachypnea of the Newborn；NICU＝neonatal intensive care unit; RDS＝respiratory

distress syndrome；MAS＝meconium aspiration syndrome; AIS=alveolar-interstitial syndrome

Contributor’s Statements:

Prof. Dr.Jing Liu: contributed to the study conception, ultrasound examination, data analysis, write and

approval of the manuscript.

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.

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

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

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

results showed that white lung/compact B-line exhibited a sensitivity of 33.8% and a specificity of 91.3%

in diagnosing TTN,whereas double lung point exhibited a sensitivity of 45.6% and a specificity of 94.8%

in diagnosing severe TTN.

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.

Keywords: lung ultrasound, transient tachypnea syndrome, pulmonary edema, pulmonary interstitial

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

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,

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

characterize the ultrasound imaging features of TTN and to explore the specificity and sensitivity of lung

ultrasonography for the diagnosis of TTN.

Materials and Methods

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

infants hospitalized in the neonatal intensive care unit (NICU) of the Bayi Children’s Hospital, affiliated

with Beijing Military General Hospital, from January to December 2014 who underwent lung

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

of the neonates.

The diagnostic criteria for TTN are as follows:1,4

(1) typical clinical symptoms: rapid, labored

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

fluid in the horizontal fissure of the right lung; and (3) exclusion and vigilance other reasons forrespiratory 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 E6、E8 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 proneposition. 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

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

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

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

presence of a large amount of lung fluid (including pulmonary interstitial and alveolar fluid).6,8

(6) AIS:

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

upper and lower lung on an ultrasound due to the differences in the severity or nature of the lesions.9

Statistical Analysis

SPSS 16.0 software was used to conduct the statistical analysis. Fisher’s exact test was used to compare

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.

Results

General characteristics of the study population

At the time of hospital admission, according to the patients’ medical histories, clinical presentations,

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 occurredin 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

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

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

findings related to various lung diseases during the acute phase.

Ultrasonic Manifestations of TTN in the Convalescence Phase

As the patients recovered from the disease, the degree of pulmonary edema gradually decreased. Initially,

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

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

RDS, 10.6% (9/85) of the patients with MAS, and 12.5% (27/215) of the patients with pneumonia.

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

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-

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=

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, andaccurate 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

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

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%).

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.

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=

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;

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

disappearance can also be observed in patients with other lung diseases, they are also not specific signs of

TTN.

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

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;

this further demonstrates that lung ultrasonography is more meaningful than conventional x-rayexamination.

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

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

diagnosing severe TTN.

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

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,

among other characteristics. Therefore, it is appropriate to extensively promote the use of ultrasonography

in neonatal intensive care units.

Limitations

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

did not measure inter-observer or intra-observer variability. Any physician who would like to perform

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

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

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

Figure 2.2 Double lung point

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 patient’s

lower lung field.

Figure 3 Pleural effusion

Pleural effusion is one of the common manifestations of TTN. This patient’s ultrasound primarily reveals

AIS and pleural effusion. However, AIS and pleural effusion can also be observed in patients with other

lung diseases. Therefore, these findings are non-specific manifestations of TTN.

Figure 4 Consolidation with air bronchograms

Under ultrasound, two areas of significant lung consolidation with air bronchograms (arrow) were

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

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.

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.

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

shadows of the ribs also exist. AIS refers to the existence of lung edema.


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Table page

Table 1 The incidence of several commonly observed ultrasound signsin TTN, RDS, and MAS (n,%)

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

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)

Pleural line

abnormality 228(100) 100(100) 85(100) 215(100)

A-line disappearance

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)

Table 2 The sensitivity and specificity of white lung/compact B-line in diagnosing TTN

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%

Not present 151(c) 601(d) 752(c+d)

Total 228(a+c) 658(b+d) 886(a+b+c+d)

Note: *Includes the RDS, MAS and pneumonia.

Table 3 The sensitivity and specificity of double lung point in diagnosing TTN

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%

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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