The Diagnosis of Neonatal Pulmonary Atelectasis

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Original Research Pulmonary Procedures

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The Diagnosis of Neonatal Pulmonary Atelectasis Using Lung Ultrasonography Jing Liu, MD, PhD; Shui-Wen Chen, MD; Fang Liu, MD; Qiu-Ping Li, MD, PhD; Xiang-Yong Kong, MD, PhD; and Zhi-Chun Feng, MD

Ultrasonography has been used for the diagnosis of many kinds of lung conditions, but few studies have investigated ultrasound for the diagnosis of neonatal pulmonary atelectasis (NAP). In this study, we evaluated the usefulness of lung ultrasonography for the diagnosis of NPA.

BACKGROUND:

From May 2012 to December 2013, 80 neonates with NPA and 50 neonates without lung disease were enrolled in this study. Each lung of every infant was divided into the anterior, lateral, and posterior regions by the anterior and posterior axillary lines. Each region was scanned carefully with the probe perpendicular or parallel to the ribs. The ultrasound findings were confirmed by chest radiograph (CXR) or CT scan.

METHODS:

RESULTS: Sixty of the 80 patients with signs of NPA on lung ultrasound also had signs of NPA on CXR (termed focal-type atelectasis), and the other 20 patients had signs of NPA on chest CT scan while there were no abnormal findings on CXR (termed occult lung atelectasis). In patients with NPA, the main ultrasound findings were large areas of lung consolidation with clearly demarcated borders, air bronchograms, pleural line abnormalities, and absence of A-lines, as well as the presence of lung pulse and absence of lung sliding on real-time ultrasound. The sensitivity of lung ultrasonography for the diagnosis of NPA was 100%, whereas the sensitivity of CXR was 75%. Large areas of lung consolidation with clearly demarcated borders were only observed in patients with NPA.

Lung ultrasonography is an accurate and reliable method for diagnosing NPA; most importantly, it can find those occult lung atelectasis that could not be detected on CXR. Routine lung ultrasonography is a useful method of diagnosing or excluding NPA in neonates.

CONCLUSIONS:

CHEST 2015; 147(4):1013-1019

Manuscript received June 1, 2014; revision accepted September 29, 2014; originally published Online First October 23, 2014. ABBREVIATIONS: CXR 5 chest radiograph; FTA 5 focal type of atelectasis; NICU 5 neonatal ICU; NPA 5 neonatal pulmonary atelectasis; OLA 5 occult lung atelectasis; RDS 5 respiratory distress syndrome AFFILIATIONS: From the Department of Neonatology and NICU of Bayi Children’s Hospital (Drs J. Liu, Chen, F. Liu, Li, Kong, and Feng), Beijing Military General Hospital, Beijing; and Graduate School, Southern Medical University (Drs Chen and F. Liu), Guangzhou City, China. FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

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CORRESPONDENCE TO: Jing Liu, MD, PhD, Department of Neonatology and NICU of Bayi Children’s Hospital, Beijing Military General Hospital, 5 Nanmen Cang, Dongcheng District, Beijing 100700, China; e-mail: [email protected] © 2015 AMERICAN COLLEGE OF CHEST PHYSICIANS. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details. DOI: 10.1378/chest.14-1306

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Neonatal pulmonary atelectasis (NPA) is a common complication of a variety of lung diseases and is one of the most common reasons for difficulty in weaning from mechanical ventilation. Early and accurate diagnosis of NPA is important for enabling appropriate treatment and improving the prognosis. Previously, the diagnosis of NPA depended mainly on chest radiograph (CXR) findings, but these examinations have many disadvantages, such as difficulty in moving severely ill infants, difficulty in controlling the body position, and the risks associated with radiation exposure.1 Lung

ultrasonography has emerged as a reliable technique for the evaluation of various lung diseases2-6 and has become a first-line tool in critical and emergency care settings, with international consensus guidelines for its use.7 Lung ultrasonography has been used to diagnose neonatal respiratory distress syndrome and transient tachypnea of the newborn, monitor fluid clearance, and predict the need for respiratory support,8-12 but there has been almost no research regarding the use of lung ultrasonography for the diagnosis of NPA. This study investigated the usefulness of lung ultrasonography for the diagnosis of NPA.

Materials and Methods

no abnormal findings on CXR, it was further confirmed by chest CT scan. The diagnosis of atelectasis was excluded if there were no findings of atelectasis on chest CT scan. In the present study, those cases of NPA that could be detected on CXR were termed focal-type atelectasis (FTA), while those that could not be detected on CXR and had to be detected by chest CT scan were termed occult lung atelectasis (OLA). The diagnosis of atelectasis was primarily made according to the following criteria14,15: (1) existence of primary lung disease that could lead to atelectasis, such as pneumonia, respiratory distress syndrome (RDS), etc; (2) dyspnea that could not be explained by primary lung disease; (3) lung showing dullness on percussion, breath sounds diminished or absent on auscultation; coarse, moist rales on auscultation during deep breathing is also among the important signs of neonatal atelectasis; and (4) CXR or CT scan findings, depending on the radiologists’ findings of absence of air in the entire lung or part of a lung, as well as direct signs, including increased opacification of the airless lobe and displacement of fissures. Indirect signs included displacement of the hilar and cardiomediastinal structures, narrowing of the ipsilateral intercostal spaces, and elevation of the ipsilateral hemidiaphragm, and there could be compensatory hyperinflation of the adjacent lobes. However, CT scan was more subtle and accurate than CXR.

Patients The institutional review board of the Beijing Military General Hospital approved the study protocol (number 2011-LC- Ped-01). From May 2012 to December 2013, 80 newborn infants with NPA and 50 neonates without lung disease were enrolled in this study. All of the enrolled patients were admitted to the Department of Neonatology and NICU of Bayi Children’s Hospital (affiliated to Beijing Military General Hospital, Beijing, China). The clinical characteristics of patients with and without NPA are shown in Table 1. Lung Ultrasonography Bedside lung ultrasonography was performed using a high-frequency linear 9 to 12 MHz probe (GE Voluson E6 or E8; GE Medical Systems), with the probe positioned perpendicular or parallel to the ribs. While in a quiet state, the infants were positioned in the supine, lateral, or prone position. The findings were recorded in three areas of each lung, divided by the anterior and posterior axillary lines. The ultrasound findings recorded included pleural lines, A-lines, B-lines, comet-tail artifacts, lung consolidation with or without air or fluid bronchograms, dynamic air bronchograms, interstitial syndrome, pleural effusion, lung sliding, and lung pulse, as described previously.13 Examination Procedures

Statistical Analysis

The examination procedures of this study were as follows. The infants first received lung ultrasound examinations, and if there was suspicion of atelectasis, it was then confirmed by CXR; if there were

The data were analyzed using SPSS for Windows software, version 16.0 (IBM). The ultrasound findings were compared among the patients with and without NPA using the Fisher exact test. A value of P , .05 was considered statistically significant.

Results

Ultrasound Findings in FTA

Normal Neonatal Lung Ultrasound Findings

A total of 625 neonates with various lung diseases underwent lung ultrasonography during the study period, of whom 80 (12.8%) were diagnosed with NPA. In 60 of these 80 patients (75%), NPA was confirmed by CXR (termed FTA). The ultrasound findings of FTA were as follows: (1) large areas of lung consolidation with clearly demarcated borders (60 of 60, 100%); (2) air bronchograms (60 of 60, 100%), fluid bronchograms (nine of 60, 15%), or dynamic air bronchograms on real-time ultrasound (10 of 60, 16.7%); (3) interstitial syndrome adjacent to the area of consolidation; (4) pleural line abnormalities (60 of 60, 100%); (5) absence of A-lines (60 of 60, 100%); (6) lung pulse and absence of lung sliding in patients with severe disease (40 of 60, 66.7%);

Normal lungs appear black on ultrasound examination. On longitudinal scans, the ribs appear as curvilinear structures with posterior acoustic shadowing. The pleural line on each side appears as a smooth, clear, echogenic line with a width of , 0.5 mm. A-lines appear as a series of echogenic lines, equidistant from one another and parallel to the pleural line. Fetal lungs have a high fluid content, and B-lines and comet-tail artifacts can be observed in healthy, full-term neonates. In this study, B-lines or comettail artifacts were observed in 18 healthy neonates (Fig 1).

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147#4 CHEST APRIL 2015

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50 ...

(7) no pleural effusion; and (8) the blood flow could be observed in the area of consolidation (100%) (Figs 2-5, Table 2).

... MAS 5 meconium aspiration syndrome; NPA 5 neonatal pulmonary atelectasis; RDS 5 respiratory distress syndrome.

950 ; 3,950 50 Control subjects

24 (26)

26 1 5 d ; 40

23 (27)

28 (22)

...

...

Jaundice Pneumonia

30 22 28

MAS RDS

45 (35) 730 ; 3,950

32 (48)

Birth Weight, g Gestational Age, wk

80

42 (38)

No. Groups

NPA

Male (Female)

25 1 3 d ; 39 1 6 d

Premature (Term)

Vaginal (Cesarean Delivery)

Diagnosis on Admission

] General Clinical Information in Two Groups TABLE 1


Figure 1 – Normal neonatal lung ultrasound. The lung field is hypoechoic (black). The pleural and A-lines are smooth, clear, parallel, echogenic lines. There are no B-lines or comet-tails after the first 76 h.

Ultrasound Findings in OLA

In 20 of the 80 patients with NPA, there were no abnormal findings on CXR, and NPA was confirmed by chest CT scan (termed OLA). The ultrasound findings of OLA were as follows: (1) small area of lung consolidation with punctate bronchograms (20 of 20, 100%); (2) pleural line abnormalities and absence of A-lines in the areas of atelectasis, with normal pleural lines and A-lines in areas without atelectasis; and (3) no obvious lung pulse and lung sliding presented on real-time ultrasound (Figs 6, 7, Table 2). Sensitivity and Speciﬁcity of Lung Ultrasonography for the Diagnosis of NPA

NPA was detected on CXR in 60 of 80 cases (sensitivity 75%) and on lung ultrasound in 80 of 80 cases (sensitivity 100%). A large area of consolidation with clearly demarcated borders on lung ultrasound had specificity of 100% for diagnosing FTA.

Discussion We found that, in this study, ultrasound had important value in the diagnosis of neonatal atelectasis. The sensitivity of lung ultrasonography for the diagnosis of NPA was 100%, including cases of OLA that would normally have required chest CT scan for diagnosis, whereas CXR detected 75% of cases of NPA. Ultrasonography was, therefore, a more accurate method of diagnosing NPA than CXR, and it could rapidly 1015

Figure 2 – Infant of gestational age of 29 1 1 wk with birth weight of 890 g who was diagnosed with respiratory distress syndrome on admission. A, Lung ultrasound showed a large area of consolidation with clearly demarcated borders and air bronchograms (hyperechogenic lines in the area of consolidation) and fluid bronchograms (hypoechogenic lines in the area of consolidation) in the upper right lung. B, Chest radiograph (CXR) findings confirmed atelectasis in the area of consolidation.

determine the area of disease, as well as provide important reference information for treatment. Bedside lung ultrasonography is, therefore, performed instead of CXR as the first-line examination for lung disease in some NICUs.16

Figure 3 – Infant of gestational age of 30 1 4 wk with birth weight 1,480 g, delivered by Cesarean section. The infant had been treated with mechanical ventilation for 14 d because of respiratory distress syndrome and ventilator-associated pneumonia, with a relapse of respiratory distress soon after weaning from ventilation. A, Bedside lung ultrasound showed a large area of consolidation in the right lung with obvious air and fluid bronchograms. The echogenicity of the consolidated lung tissue was similar to that of the adjacent liver tissue. B, Real-time ultrasound showed air movement in the bronchi during breathing (Video 1). CXR confirmed a large area of atelectasis in the lower right lung. See Figure 2 legend for expansion of abbreviation.


The most important signs of NPA on lung ultrasound are a large area of consolidation with clearly demarcated borders and air bronchograms. Presence of a lung pulse and absence of lung sliding on real-time ultrasound can help to confirm the diagnosis. The ultrasound characteristics of large areas of FTA include lung consolidation with clearly demarcated borders and obvious air bronchograms or even typical parallel patterns.7 The ultrasound characteristics of OLA include small areas of lung consolidation with punctate bronchograms, pleural line abnormalities and absence of A-lines in areas of atelectasis but normal pleural lines and A-lines in areas without atelectasis, as well as absence of an obvious lung pulse and presence of lung sliding on real-time ultrasound. Because it is difficult to detect such atelectasis on CXR, we called these changes OLA. In this study, NPA was confirmed by chest CT scan in patients with signs of OLA on lung ultrasound. Dynamic air bronchograms are observed in patients with FTA but not in patients with OLA. In this study, dynamic air bronchograms were observed in 16.7% of patients with FTA. In adults, however, dynamic air bronchograms have been reported to exclude atelectasis.17 The reasons for this difference between the findings in neonates and those in adults remain unclear. Lung pulse is one of the important ultrasound signs of NPA. Lichtenstein et al18 considered a lung pulse to be an early sign of complete atelectasis, which can be detected immediately before radiologic changes with sensitivity of 93% and specificity of 100%. In this study, a lung pulse was observed in 66.7% of patients with FTA but was not observed in any patients with OLA. The occurrence of a lung pulse was related to the extent of alveolar consolidation and the strength of the

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Figure 4 – Infant of gestational age of 36 1 6 wk with birth weight of 2,850 g, delivered vaginally and diagnosed with infectious pneumonia on admission. Severe respiratory distress recurred at 12 d after treatment. A, B, Bedside lung ultrasound showed large areas of consolidation with air bronchograms in both upper lungs. C, CXR confirmed atelectasis in both upper lungs. See Figure 2 legend for expansion of abbreviation.

Figure 5 – Infant of gestational age of 25 1 3 wk with birth weight of 730 g, delivered vaginally. Lung ultrasound showed atelectasis in the lower right lung. Color Doppler ultrasound showed blood flow in the area of consolidation (A, blood flow; B, Doppler waveform).

TABLE 2

] Distribution of Ultrasound Findings in the Different Groups

Ultrasonic Signs

FTA (n 5 60)

Large area consolidation

60 (100)

Small area consolidation

0 (0)

Air bronchograms

60 (100)

Dynamic air bronchogram

10 (16.7)

Fluid bronchogram

9 (15)

Pleural line abnormalitiesa Pleural eﬀusion

60 (100) 0 (0)

Interstitial syndrome

60 (100)

Lung pulse

40 (66.7)

Disappearing lung slide

40 (66.7)

A-line disappearance

60 (100)

a

OLA (n 5 20) 0 (0) 20 (100) 20 (100)

Control Subjects (n 5 50)

P Value

0 (0)

, .001

0 (0)

, .001

0 (0)

, .001

0 (0)

0 (0)

, .001

0 (0)

0 (0)

, .001

0 (0)

, .001

20 (100) 0 (0)

0 (0)

, .001

0 (0)

, .001

0 (0)

0 (0)

, .001

0 (0)

0 (0)

, .001

0 (0)

, .001

20 (100)

20 (100)

Data are given as No. (%). FTA 5 focal-type atelectasis; OLA 5 occult lung atelectasis. Pleural line abnormalities and A-line disappearance only exists within the area of lesions in patients with OLA.

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Figure 6 – Infant of gestational age of 29 1 1 wk with birth weight of 890 g, delivered vaginally, who was diagnosed with respiratory distress syndrome on admission and was still oxygen dependent after 5 mo. A, Lung ultrasound showed consolidation in the upper right lung with punctate air bronchograms and fluid bronchograms, as well as interstitial syndrome in the lower right lung. B, CXR showed no abnormal findings, but chest CT scan showed atelectasis in the upper right lung. See Figure 2 legend for expansion of abbreviation.

heartbeat, which could explain why a lung pulse occurred less frequently than in adult patients with atelectasis and has seldom been detected in neonates with OLA. It can be difficult to detect OLA on CXR for the following reasons: (1) the area of atelectasis might be too small to detect on CXR; (2) the position of the infant and direction of the radiation beam might make it difficult to detect atelectasis in some areas, such as deep in the lungs or in the posterior lungs; (3) the radiation beam might not be sufficiently strong to detect small areas of atelectasis; and (4) the spontaneous breathing or mechanical ventilation of patients can result in CXR images obtained during inspiration. In contrast, ultrasound can detect small areas of atelectasis in any part of the lungs, regardless of the position of the patient. OLA is found mainly in two types of cases: (1) patients who are difficult to wean from ventilation or who require

repeat ventilation (8 of 20 patients with OLA in this study) and (2) premature infants with long-term oxygen dependency (12 of 20 patients with OLA in this study). We, therefore, consider it necessary to perform routine bedside lung ultrasonography in patients with suspected OLA, and ultrasonography might replace the need for chest CT scanning in the neonatal ICU (NICU) setting. Previously, the diagnosis of NPA mainly depended on CXR, CT scan, or fiber-optic bronchoscopy findings. Fiber-optic bronchoscopy is the most reliable of these investigations, but it also has the highest technical requirements, can be difficult to obtain urgently, and has been associated with a risk of trauma to the airway.19 Radiation exposure is an unavoidable disadvantage of CXR and particularly CT scanning, associated with risks of severe complications, such as DNA damage or cancer. Because cells are particularly sensitive to radiation damage during the differentiation stages, neonates can

Figure 7 – Infant of gestational age of 39 1 4 wk with birth weight of 3,890 g, delivered by Cesarean section, who was diagnosed with meconium aspiration syndrome on admission and was ventilated for 10 d. Three days after weaning from ventilation, respiratory distress recurred, and the infant was ventilated for a further 3 d. Respiratory distress recurred again after the second time the infant was weaned from ventilation. A, Bedside lung ultrasound showed consolidation and air bronchograms in the upper right lung, with absence of the pleural line and A-lines. The lower right lung had a normal appearance (black lung field with clear pleural and A-lines). CXR showed no abnormal findings. B, Chest CT scan confirmed atelectasis in the upper right lung. See Figure 2 legend for expansion of abbreviation.


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have a particularly high risk of complications because of radiation exposure, particularly if they are born prematurely.1 Sick and premature infants in the NICU are often exposed to radiation for the diagnosis or exclusion of various conditions, and they can receive relatively high cumulative doses. Definitive diagnosis of severely ill infants in the NICU can be delayed because of the difficulty of performing CXR or CT scan at the bedside, while ultrasonography is easily available at the bedside and avoids the disadvantages of CXR or CT scans. In summary, the results of this study showed that lung ultrasonography was an accurate and reliable method of

Acknowledgments Author contributions: J. L. had full access to all of the data in the study and takes responsibility for the integrity of the data, the accuracy of the data analysis, and manuscript preparation. S.-W. C., F. L., Q.-P. L., and X.-Y. K. contributed to data collection and analysis; Z.-C. F. contributed to data analysis and manuscript revision; and J. L., S.-W. C., F. L., Q.-P. L., X.-Y. K. and Z.-C. F. contributed to the approval of the final manuscript. Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article. Additional information: The Video can be found in the Multimedia section of the online article.

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