Ultrasonografía pulmonar para diagnosticar hemorragia pulmonar del

recién nacido.

Xiao-Ling Ren, Wei Fu, Jing Liu, Ying Liu & Rong-Ming Xia.

Bayi Children’s Hospital, the Army General Hospital of the Chinese PLA, Beijing, China

J. Matern Fetal Neonatal Med, 2017; 30(21): 2601–2606

OBJETIVOS: El objetivo de este estudio fue investigar la aplicación de la ecografía

pulmonar para el diagnóstico de hemorragia pulmonar del recién nacido (HPN).

MÉTODOS: De julio de 2013 a junio de 2016, 157 neonatos fueron incluidos en el

estudio. Se dividieron en dos grupos: un grupo de estudio de 57 recién nacidos, a

quienes se les diagnosticó hemorragia pulmonar neonatal (HPN) de acuerdo con su

historia clínica, manifestaciones clínicas y radiografías de tórax, y un grupo control de

100 neonatos sin enfermedad pulmonar. Todos los sujetos se sometieron a ultrasonido

de pulmón en estado de reposo, posición supina, lateral o prona, realizado por un único

médico experto. Los hallazgos ecográficos se compararon entre los dos grupos.

RESULTADOS: Los hallazgos principales de la ecografía pulmonar asociados a la HPN

incluyeron consolidación pulmonar con broncograbado aéreo con una incidencia de

82,5%, signo de desgarramiento con incidencia de 91,2%, derrame pleural con incidencia

de 84,2% (pleurocentesis confirmó que el líquido sangraba) , atelectasia con incidencia

de 33,3%, anomalías de la línea pleural, así como líneas A desaparecidas con una

incidencia del 100%, y 11,9% de estos pacientes presentaron las principales

manifestaciones del síndrome alveolar intersticial (AIS). El signo de destello mostró una

sensibilidad del 91,2% y una especificidad del 100% en el diagnóstico de HPN.

CONCLUSIONES: La ecografía pulmonar es útil y confiable para el diagnóstico de HPH,

que es adecuada para la aplicación de rutina en la unidad de cuidados intensivos

neonatales.

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The Journal of Maternal-Fetal & Neonatal Medicine

ISSN: 1476-7058 (Print) 1476-4954 (Online) Journal homepage: http://www.tandfonline.com/loi/ijmf20

Lung ultrasonography to diagnose pulmonaryhemorrhage of the newborn

Xiao-Ling Ren, Wei Fu, Jing Liu, Ying Liu & Rong-Ming Xia

To cite this article: Xiao-Ling Ren, Wei Fu, Jing Liu, Ying Liu & Rong-Ming Xia (2017) Lungultrasonography to diagnose pulmonary hemorrhage of the newborn, The Journal of Maternal-Fetal& Neonatal Medicine, 30:21, 2601-2606, DOI: 10.1080/14767058.2016.1256997

To link to this article: http://dx.doi.org/10.1080/14767058.2016.1256997

Accepted author version posted online: 03Nov 2016.Published online: 22 Nov 2016.

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J Matern Fetal Neonatal Med, 2017; 30(21): 2601–2606! 2016 Informa UK Limited, trading as Taylor & Francis Group. DOI: 10.1080/14767058.2016.1256997

ORIGINAL ARTICLE

Lung ultrasonography to diagnose pulmonary hemorrhage of thenewborn

Xiao-Ling Ren1,2*, Wei Fu2*, Jing Liu1,2*, Ying Liu1*, and Rong-Ming Xia1*

1Department of Neonatology and NICU, Beijing Chaoyang District Maternal and Child Health Care Hospital, Beijing, China and 2Department of

Neonatology and NICU of Bayi Children’s Hospital, the Army General Hospital of the Chinese PLA, Beijing, China

Abstract

Objectives: This study was aimed to investigate the application of lung ultrasound for thediagnosis of pulmonary hemorrhage of the newborn (PHN).Methods: From July 2013 to June 2016, 157 neonates were enrolled in the study. They weredivided into two groups: a study group of 57 neonates, who were diagnosed with PHNaccording to their medical history, clinical manifestations and chest X-ray findings, and acontrol group of 100 neonates with no lung disease. All subjects underwent bedside lungultrasound in a quiet state in a supine, lateral or prone position, performed by a single expertphysician. The ultrasound findings were compared between the two groups.Results: The lung ultrasound main findings associated with PHN included lung consolidationwith air bronchograms with an incidence of 82.5%, a shred sign with an incidence of 91.2%,pleural effusion with an incidence of 84.2% (pleurocentesis confirmed the fluid was reallybleeding), atelectasis with a incidence of 33.3%, pleural line abnormalities, as well asdisappearing A-lines with an incidence of 100%, and 11.9% of these patients had the mainmanifestations of alveolar-interstitial syndrome (AIS). The shred sign exhibited a sensitivity of91.2% and a specificity of 100% in diagnosing PHN.Conclusions: Lung ultrasonography is useful and reliable for diagnosing PHN, which is suitablefor routine application in the neonatal intensive care unit.

Keywords

Lung ultrasound, pulmonary hemorrhage,infants, newborn

History

Received 17 October 2016Accepted 1 November 2016

Introduction

Pulmonary hemorrhage of the newborn (PHN) is a common

severe and critical disease in newborn infants, and it has

complicated etiologies, rapid progression and a high mortality

rate [1,2]. Recently, great progress has been made in the

treatment of PHN, but the mortality rate remains high. Rapid

and accurate diagnosis is of great significance in guiding

treatment and improving the prognosis of PHN patients. Until

now, a diagnosis of PHN has been mainly based on the case

history, typical clinical manifestations, arterial blood gas

analysis and chest X-rays findings, while lung ultrasound has

not been applied in the diagnostic protocol. Recently,

ultrasounds have been used extensively and successfully in

the diagnosis of many types of neonatal lung diseases, such as

respiratory distress syndrome (RDS), pneumonia, atelactisis,

meconium aspiration syndrome (MAS), transient tachypnea

of the newborn (TTN) and pneumothorax, among others

[3–9]. However, no studies have addressed PHN. Therefore,

this study aimed to investigate the diagnostic value of lung

ultrasonography for PHN.

Patients and methods

Patients

The institutional review board of the Army General Hospital

of the Chinese PLA approved the study (protocol number

2011-LC- Ped-01). There was no consent needed from the

patients because the ultrasound procedure is harmless to

patients. From July 2013 to June 2016, 57 newborn infants

with PHN and 100 neonates with no lung disease were

enrolled in this study. All the enrolled patients were admitted

to the Department of Neonatology and NICU of Bayi

Children’s Hospital, which is affiliated to the Army General

Hospital of the Chinese PLA (Beijing, China).

Instruments and examination method

A high-frequency linear 10–14 MHz probe (GE Voluson i or

Logiq e; GE Medical Systems, Kretz, Austria) was used for

ultrasound examinations. While in a quiet state, infants were

positioned in a supine, lateral or prone position. The probe

was perpendicular (the most frequently used) or parallel to the

ribs, and each side of the lung was divided into three regions

*Every author contributed equally to this work.

Address for correspondence: Prof. Dr Jing Liu, MD, PhD, Department ofNeonatology and NICU, Beijing Chaoyang District Maternal and ChildHealth Care Hospital, Beijing 100101, China. Tel: +86-10-66721804.E-mail: liujingbj@live.cn

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(anterior, lateral and posterior) by the anterior and posterior

axillary lines. Each region of both sides of the lung was

scanned, and the ultrasonic findings were recorded. 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.

Observation indices

The observation indices included pleural lines, A-lines, B-

lines, interstitial syndrome, white lung, lung consolidation

with an air bronchogram or fluid bronchogram, double lung

point, and pleural effusion, which were defined as the

following [10–18]: (1) Pleural line: the regular echogenic

line under the superficial layers of the thorax moving

continuously during respiration, while abnormal pleural lines

were pleural lines that disappeared or had a thickened,

irregular or coarse and indistinct appearance; (2) A-line: a

series of echogenic, horizontal, parallel lines equidistant from

one another below the pleural line; (3) B-lines: also known as

ultrasound lung comets, are hyperechoic narrow-based arti-

facts spreading like laser rays from the pleural line to the edge

of the screen; (4) Alveolar-interstitial syndrome (AIS): defined

as the presence of more than three B-lines in every examined

area; (5)White lung: defined as the presence of compact B-

lines in the six areas without horizontal reverberation; (6)

Lung consolidation: defined as areas of hepatization with the

presence of air bronchograms and/or fluid bronchograms; an

air or fluid bronchogram is caused by reflection of ultrasound

beams in the air-filled or fluid-filled bronchi surrounded by

consolidated tissue; (7) Shred sign: a shred sign appears when

the border of an aerated lung and consolidated lung is not

sharp; (8) Double point: Due to a difference in severity or the

nature of pathological changes in different areas of the lung, a

longitudinal scan shows a clear difference between the upper

and lower lung fields; this sharp cut-off point between the

upper and lower lung field is known as a double point; and (9)

Pleural effusion: defined as anechoic-dependent collections

limited by the diaphragm and the pleura.

Statistical analysis

The Statistical Package for the Social Sciences (SPSS) 19.0

software (Wuxi, China) was used to statistically analyze the

data. Fisher’s exact test was used to compare the positive rates

of the ultrasound test results of the newborns of each group,

and the specificity and sensitivity of the main test results for

the diagnosis of PHN were calculated. A value of p50.05

indicated statistically significant differences. The information

reported was evaluated by an expert.

Results

General information for the two groups

The perinatal clinical characteristics of the two groups are

shown in Table 1.

The etiology and onset time of PHN

According to the case history, clinical manifestations and

laboratory findings, it was hypothesized that the possible

reasons for PHN were the following: severe intrauterine

infection (pneumonis and/or sepsis)19 cases (33.3%); severe

fetal distress and/or birth asphyxia, 12 cases (21.1%); RDS, 12

cases (21.1%); MAS, 8 cases (14.0%); and postnatal sepsis

and or disseminated intravascular coagulation (DIC), 6 cases

(10.5%). The onset time was within 6 h after birth in 46

patients (80.7%), within 24 h after birth in 48 patients

(84.2%), within 1 week after birth in 52 cases (91.2%),

while only less than 10% of the cases (5 cases, 8.8%) occurred

after 1 week of birth.

Normal lung ultrasound appearance

The ultrasound appearance of a normal lung is black. The

pleural line appears as a smooth echogenic line that exhibits

respirophasic movement. A-lines are present as a series of

echogenic parallel lines, equidistant from one another, below

the pleural line. B lines, which can be seen in healthy term

newborns, are echogenic vertically orientated lines that start

at the pleural line and reach the lower edge of the image;

however, there is no pleural effusion and lung consolidation

(Figure 1).

Figure-1. Normal neonatal lung ultrasound. The lung field ishypoechoic (black). The pleural and A-lines are smooth, clear, parallel,echogenic lines. They are arranged in parallel with each other. TheA-line echo gradually weakened and finally disappeared from the surfaceto the depth of the lung field.

Table 1. General clinical information in two groups.

Groups nMale/

FemaleGA

(Weeks)Birth

weight (g)Premature/

TermVD/

CD/FD

PHN 57 32/25 30+5�41+6 1585�4600 10/47 30/23/4Controls 100 56/44 31+3�40+5 1650�4120 18/8 54/37/9

PHN: pulmonary hemorrhage of the newborn; GA: gestational age; VD:veginal delivery; CD: cesarean delivery; FD: forceps delivery.

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The ultrasound manifestations of PHN

The main ultrasound manifestations of PHN were the

following: (1) Shred sign: every baby who had lung consoli-

dation had a shred sign at the edge of the consolidation area

and the shred sign was the major ultrasound findings in the

other five infants; the total incidence rate of this sign was

91.2% (Figures 2–6). (2) Lung consolidation with an air

bronchogram or fluid bronchogram: 47 babies had lung

consolidation with an air bronchogram (82.5%)and eight of

these babies also had a fluid bronchogram (8/47, 17.0%;

Figures 3–6); (3) Atelectasis: 19 of these patients had

atelectasis (33.3%; Figures 4 and 5); (4) Abnormal pleural

lines and A-line disappearance: this was found in all of the

patients (100%); (5) Pleural effusion: this was seen in 48 cases

(84.2%; Figures 3–7). The fluid was confirmed as bleeding by

thoracocentesis. In severe cases with destruction of red blood

cells, fibrous protein deposition in the formation of a fibrous

cord similar to floating objects were seen with fluid

movement under real-time ultrasound (Figure 6, avi-1); and

(6) AIS: 7 of the infants had AIS (12.2%) with lung edema

(Figure 7).

The sensitivity and specificity of the shred sign indiagnosing PHN

Based on the results of this study, the shred sign was the

most common and specific ultrasonic findings of PHN.

Therefore, this study used the presence of a shred sign as a

parameter for calculating the sensitivity (a/a + c) and speci-

ficity (d/b + d) of ultrasonography for diagnosing severe

PHN. The results indicated that the shred sign exhibited a

sensitivity of 91.2% and a specificity of 100% in diagnosing

PHN (Table 2).

Discussion

It was reported that the incidence rate of PHN was 1 � 12%of live births, and it increased to 50% in infants with high risk

factors [19]. The common risk factors included premature

birth, intrauterine growth restriction (IUGR), patent ductus

arteriosus (PDA), severe birth asphyxia, hypoxia or oxygen

toxicity, disseminated intravascular coagulation (DIC), RDS,

MAS, hypotension, severe infection or sepsis, polycythemia,

mechanical ventilation, multiple births, male gender as well

as surfactant therapy [1]. In this study, the main causes of

PHN were severe intrauterine infection (33.3%), severe birth

asphyxia (21.1%) and RDS (21.1%), which accounted for

more than 75% of the patients. MAS and severe postnatal

infection accounted for 25% of these patients. PHN often

occurred within the first several days after birth. In this study,

40 (71.4%) cases developed PHN within several hours to 24 h

after birth, 45 cases (80.4%) developed PHN within three days

of life, 50 infants (89.5%) developed PHN within seven days

of life, while only six cases (10.5%) developed PHN between

1 to 2 weeks after birth, which means nearly 90% of the NPH

cases occurred within the first week of life.

During the early years, the mortality of PHN may be as

high as 50%. The survival of infants was affected by several

factors contributing to a long-term poor prognosis. For

example, the incidence of nerve sensory disturbance doubled

in severe PHN patients, the incidence of bronchopulmonary

dysplasia, cerebral palsy and cognitive delay increased 2.5

times in premature infants with NPH, and the incidence of

seizure periventricular leukomalacia also increased signifi-

cantly [1]. Recently, mortality decreased significantly with

the development of new treatment methods [20–22]. There

were only two PHN patients who died in this study, so the

mortality rate was 3.51%.

Figure 3. The ultrasonic findings in a mildNPH case. The baby was G2P1 with agestational age of 38+ weeks and had avaginal delivery with a birth weight of3070 g. The baby was admitted to the NICUbecause of NPH caused by severe asphyxia.The ultrasound showed small consolidationwith an air bronchogram under the pleur lineand a shred sign at the edge of consolidation,as well as an abnormality of the pleur line, adisappeared A-line and a small amount ofpleural effusion.

Figure 2. Shred sign is a most common ultrasonic sign of NPH. A babywas that was G1P1 with a gestational age of 41 weeks was admitted to theNICU because of lung bleeding. The chest X-ray had high density cloudyshadows in the right lung field. The lung ultrasound manifestated withAIS and a thickened and fuzzy pleural in the left lung, while the rightlung showed consolidation with an air bronchogram and shred sign.

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Figure 5. The ultrasonic findings in a severeNPH case. The baby was G1P1 with agestational age of 38+6 weeks and had aCesarean delivery with a birth weight of3345 g. The baby was admitted to the NICUbecause of NPH caused by severe birthasphyxia. The lung ultrasound showed a largearea of lung consolidation with an airbronchogram, a shred sign at the edge ofconsolidation, a disappeared pleural line,A-lines in both sides of the lungs, and pleuraleffusion in the right lung (which was con-firmed as bleeding by thoracocentesis).

Figure 4. The ultrasonic findings in a severeNPH case. The baby was G1P1 with agestational age of 39+6 weeks and had avaginal delivery with a birth weight of3180 g. The baby was admitted to the NICUbecause of NPH caused by severe intrauterineinfection. The lung ultrasound showed a largearea of lung consolidation with an airbronchogram, a shred sign at the edge ofconsolidation, pleural effusion in both sidesof the lungs (which was confirmed asbleeding by thoracocentesis), a disappearedpleural line and A-lines.

Figure 6. The ultrasonic findings in a severeNPH case. The baby was G3P1 with agestational age of 37+1 weeks and had aCesarean delivery with a birth weight of4600 g. The baby was admitted to the NICUbecause of NPH caused by MAS. The lungultrasound showed a large area of lungconsolidation with an air bronchogram, ashred sign, disappeared pleural line and A-lines in both sides of the lungs, as well aspleural effusion in the right lung. It was foundthat there was fibrous protein deposition inthe formation of fibrous cord-like floatingobjects with fluid movement under real-timeultrasound.

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The key protocol for decreasing PHN mortality is based on

early, quick and accurate diagnosis. For a long time, the diagnosis

of PHN has been mainly based on medical history, typical

clinical presentation and chest X-ray examination. Although

chest X-ray is non-specific, it is usually necessary in the

diagnosis of PHN, which often manifests with fluffy opacities,

focal ground-glass opacities, or even ‘‘white out’’ in severe

patients. Lung ultrasound is not usually performed in cases of

suspected PHN. In the present study, we therefore investigated

the diagnostic value of lung ultrasound for PHN. Through the

systemic observation of lung ultrasonic characteristics of 57 PHN

patients, we found lung ultrasound can accurately diagnose PHN,

which is also useful for dynamic observation, timely understand-

ing of the changes of pulmonary lesions and, thus, helping to

guide treatment and improve the prognosis.

According to the results of this study, we found that the

major ultrasonic characteristics of PHN are the following: (1)

Shred sign: when the border of the aerated lung and

consolidated lung is not sharp, a shred sign appears [12].

The shred sign is the most common ultrasonic sign of PHN,

and it occurred in more than 90% of the patients. The shred

sign is the main ultrasonic finding in mild PHN patients or

within the lung on the side with mild bleeding. In addition,

the shred sign is often found at the edge of large areas of

consolidation. (2) Lung consolidation with an air broncho-

gram: this is one of the most common ultrasonic signs of PHN

and was seen in more than 80% of the patients. We think that

the reasons for consolidation were mainly related to the

original lung diseases, the lung bleeding itself or the

secretions blocking the trachea and bronchus. (3) Pleural

effusion: this is another common sign of PHN and it occurred

in more than 85% of the PHN cases. Pleural effusion can be

found in one or both side of the thorax, but is often seen on

the side with more severe bleeding in the lung. The fluid

amount was associated with the original diseases and/or the

degree of bleeding. The fluid was confirmed as bleeding by

thoracocentesis. Severe cases are due to the destruction of red

blood cells, and fibrous protein depositions result in the

formation of fibrous cord like floating objects. These fiber

strip floating objects could be observed with fluid movement

under real-time ultrasound (avi-1). (4) Pulmonary atelectasis:

this was seen in one-third of the patients. In addition to lung

consolidation, atelectasis is mainly related to the original lung

diseases, such as pneumonia, RDS or MAS, while lung

bleeding itself or the secretions blocking the trachea and

bronchus are also associated with these pathogenic findings.

(5) Abnormal pleural lines and A-line disappearance: both of

these signs were the most common and non-specific ultra-

sonic findings of PHN. (6) AIS: In some cases with mild

bleeding, or in the acute stages of some cases with severe

bleeding, AIS is the main manifestation.

Lung ultrasound for the diagnosis of PHN has high

sensitivity and specificity. According to the results of this

study, the shred sign, which had a sensitivity of 91.2% and a

specificity of 100%, is especially helpful for diagnosing PHN.

Conclusions

In conclusion, the value and characteristics of ultrasound

imaging of PHN were determined in this study. We found that

ultrasound had a definitive diagnostic value for NPH. The

advantage of ultrasound is it allows observation of changes in

the condition of the disease easily, and it is of great

significance in guiding treatment and adjusting the treatment

plan over time. In addition, it is non-invasive, harmless and

can avoid being inspected. Other newborns within the same

endemic area and the staff may suffer from radiation damage

with other types of imaging techniques. Ultrasound is

therefore worth being widely used in neonatal wards and

may eventually be able to replace chest X-rays and CT

[23,24].

Declaration of interest

Ethical approval and consent to participate: The institutional

review board of the Army General Hospital of the Chinese

PLA approved the study protocol (number 2011-LC- Ped-01).

Consent for publication: All the coauthors approve the

publication of this manuscript.

Availability of supporting data: All the data are available for

the editors and reviewers of Critical Care, and will be

submitted if required.

This work was supported by the Clinical Research Special

Fund of Wu Jieping Medical Foundation (320.6750.15072).

Contributorship statement

Prof. Dr Jing Liu: contributed to the study conception, lung

ultrasound examination, data analysis, manuscript prepar-

ation, and write and approval of the manuscript.

Figure 7. The ultrasonic findings in the acute stages of NPH. The babywas G1P1 with a gestational age of 39+5 weeks and had a vaginaldelivery with a birth weight of 3180 g. The baby was admitted to theNICU with a diagnosis of RDS. The NPH was diagnosed after 10 h fromadmission to the hospital when the lung ultrasound showed AIS, a fuzzypleural line and disappeared A-lines, as well as a small pleural effusionin the right side of the thorax.

Table 2. The sensitivity and specificity of shred sign for the diagnosis ofdiagnosing PHN.

Co-existsigns* PHNs Controls Total

Sensitivity(a/a + c)

Specificity(d/b + d)

Present 52 (a) 0 (b) 52 (a + b) 91.2% 100%Not present 5 (c) 100 (d) 105 (c + d)Total 7 (a + c) 100 (b + d) 157 (a + b+c + d)

*Includes the shred sign, lung consolidation and pleural effusion.

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Dr Xiao-Ling Ren: contributed to lung ultrasound exam-

ination, data analysis, manuscript preparation, the baby care,

and approval of the final manuscript.

Dr Wei Fu: contributed to data analysis, manuscript

preparation, and approval of the final manuscript.

Dr Ying Liu and Rong-Ming Xia: contributed to data

analysis, manuscript preparation, and approval of the final

manuscript.

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