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Original article
Lung ultrasound immediately after birth to describe normal neonatal transition: an observational study
  1. Douglas A Blank1,2,
  2. C Omar Farouk Kamlin1,
  3. Sheryle R Rogerson1,
  4. Lisa M Fox1,
  5. Laila Lorenz1,3,
  6. Stefan Charles Kane4,5,
  7. Graeme R Polglase2,
  8. Stuart B Hooper2,
  9. Peter G Davis1
  1. 1 Newborn Research Centre, The Royal Women’s Hospital, Melbourne, Victoria, Australia
  2. 2 The Ritchie Centre, Hudson Institute of Medical Research, Monash University, Melbourne, Victoria, Australia
  3. 3 Department of Neonatology, University Children’s Hospital of Tübingen, Tübingen, Germany
  4. 4 Department of Obstetrics and Gynaecology, The University of Melbourne, Melbourne, Victoria, Australia
  5. 5 Pregnancy Research Centre, The Royal Women’s Hospital, Melbourne, Victoria, Australia
  1. Correspondence to Dr Douglas A Blank, Newborn Research Centre, 7th Floor, The Royal Women’s Hospital Cnr Grattan Street & Flemington Road, Parkville, VIC, Australia 3052; douglas.blank{at}thewomens.org.au

Abstract

Objective Lung ultrasound (LUS) has shown promise as a diagnostic tool for the evaluation of the newborn with respiratory distress. No study has described LUS during ‘normal’ transition. Our goal was to characterise the appearance of serial LUS in healthy newborns from the first minutes after birth until airway liquid clearance is achieved.

Study design Prospective observational study.

Setting Single-centre tertiary perinatal centre in Australia.

Patients Of 115 infants born at ≥35 weeks gestational age, mean (SD) gestational age of 386/7 weeks±11 days, mean birth weight of 3380±555 g, 51 were delivered vaginally, 14 via caesarean section (CS) after labour and 50 infants via elective CS.

Interventions We obtained serial LUS videos via the right and left axillae at 1–10 min, 11–20 min and 1, 2, 4 and 24 hours after birth.

Main outcome measures LUS videos were graded for aeration and liquid clearance according to a previously validated system.

Results We analysed 1168 LUS video recordings. As assessed by LUS, lung aeration and airway liquid clearance occurred quickly. All infants had an established pleural line at the first examination (median=2 (1–4) min). Only 14% of infants had substantial liquid retention at 10 min after birth. 49%, 78% and 100% of infants had completed airway liquid clearance at 2, 4 and 24 hours, respectively.

Conclusions In healthy transitioning newborn infants, lung aeration and partial liquid clearance are achieved on the first minutes after birth with complete liquid clearance typically achieved within the first 4 hours of birth.

Trial registration number ANZCT 12615000380594.

  • Neonatology
  • lung liquid
  • lung aeration
  • lung ultrasound
  • newborn

http://dx.doi.org/10.1136/archdischild-2017-312818

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    What is known on this subject?

    • Ultrasound beams passing through an aerated lung produces characteristic artefacts that can be interpreted for diagnostic purposes.

    • Lung ultrasound has been able to distinguish between respiratory distress syndrome, pneumothorax and transient tachypnoea of the newborn in infants with respiratory distress.

    • To date, no studies describe the healthy transitioning newborn lung using ultrasound from the first minutes after birth through complete lung liquid clearance.

    What this study adds?

    • In a population of healthy newborns, all infants achieved lung aeration and partial airway liquid clearance within the first 20 min after birth.

    • Serial lung ultrasound can be used to monitor changes in lung aeration and airway liquid clearance after birth.

    • Complete airway liquid clearance is typically achieved within the first 4 hours after birth.

    Background

    Lung ultrasound (LUS) has shown promise as a diagnostic tool for evaluation of the newborn with respiratory distress. Specifically, LUS has been able to distinguish between respiratory distress syndrome, pneumothorax and transient tachypnoea of the newborn.1–15 During birth, the infant must transition from dependency on the placenta for gas exchange to lungs that successfully perform this function.16 This process involves inflation and liquid clearance of a gasless lung resulting in fully aerated lung with an established functional residual capacity. LUS may be able to characterise this transition. LUS can be performed by the bedside clinician in real time with minimal delay, may be easily repeated during clinical changes and treatments and does not expose the infant to radiation.17 18

    Ultrasound beams passing through an aerated lung produce characteristic artefacts.1 8 19 20 Traditionally, the interference of sound waves caused by air in the lungs has discouraged the use of LUS as a diagnostic tool. However, these characteristic artefacts are now recognised as having diagnostic importance.1 6 8 9 12 13

    No studies describe the appearance of the normally transitioning newborn lung using ultrasound on a healthy population of infants from the first minute after birth until full lung aeration and liquid clearance are achieved. We hypothesise that we can use LUS to describe lung aeration and liquid clearance starting in the delivery room through the first hours after birth in healthy term and near term infants.

    Methods

    This was a single centre, prospective, observational study of term and late preterm conducted at the Royal Women’s Hospital, in Melbourne, Australia, a regional referral hospital with a high-risk perinatal service averaging >7000 deliveries per year.

    Participants were eligible for the study if they were ≥35 weeks gestation at delivery and did not have an antenatal diagnosis of significant pulmonary pathology (ie, diaphragmatic hernia). Written, informed, antenatal consent was obtained from expecting mothers prior to delivery. We also obtained oral permission from the delivering obstetrician or midwife to be present at deliveries and conduct the study. Patients were recruited as a convenience sample, with a target enrollment of 100 infants, 50 born via elective caesarean section (CS) (without labour) and 50 born via vaginal delivery. In addition, we studied a third group of infants, not included in our goal sample size of 100, who were born via unplanned CS after a period of labour (minimum cervical dilation of at least 5 cm and more than 2 hours of uterine contractions). The study was approved by the Royal Women’s Hospital ethics committee and registered with the Australian and New Zealand Clinical Trials Registry: 12615000380594.

    Data collection

    We obtained serial LUS video recordings, using a GE Venue 50 ultrasound machine (GE Healthcare, Chicago, Illinois, USA) and a ‘hockey-stick,’ L8-18i linear transducer with a depth of 2.5 cm and a gain of 60. Images were interpreted and graded during or immediately after each LUS examination by the researcher. We obtained 3 s video recordings of the right and left side of the chest using B-mode and M-mode. Images were collected at 1–10 min, 11–20 min, 1 hour, 2 hours and 4 hours after birth. Vital signs (heart rate, respiratory rate and SpO2) were also assessed at each time point. At the 4-hour examination, if the infant had achieved a LUS grade consistent with full liquid clearance and complete aeration and the postductal SpO2 was >97%, no further ultrasounds were performed. If not, a repeat examination was performed at 24 hours after birth. We collected clinical and demographic information until hospital discharge.

    LUS examination

    Infants were examined while being held by their mother or on a warming bed. Healthy infants born vaginally were placed on the mother’s chest immediately after birth. During each examination, the LUS probe was placed in the infant’s axillae with the notch pointed superiorly. The probe was then adjusted until a ‘bat sign’ was achieved and the lungs appeared as aerated and dry as possible.8 19 21 The probe was 3.5 cm long and a typical image included the lung parenchyma from two to three rib spaces. We choose to place the LUS probe in the infant’s axillae because we could obtain consistent images regardless if the infant was prone or supine, while minimising handling. We used a previously validated LUS grading system described by Raimondi and colleagues,1–3 assigning a grade of type 1, 2 or 3 to each video (figure 1). In addition, we evaluated for the presence of lung sliding on B-mode video loops and the ‘seashore sign’ on M-mode to rule out pneumothorax.21–26

    Figure 1
    Figure 1

    Grading system for lung ultrasound from Raimondi et al.1–3 Left: type 1 or ‘white-out’ lung, significant liquid retention associated with respiratory distress syndrome (type 1) is seen between the acoustic shadow cast by the ribs (R). White-out is produced by the coalescence of B-lines (CBL) and the pleural line is blunt. Centre: type 2, retention of lung liquid after birth is characterised by the presence of hyperechoic vertical projections called ‘B-lines’ (B) that arise from the sharp pleural line (SPL), extend through the ultrasound image and obscure the ‘A-lines’ (A).3 5 15 20 33 This represents an intermediate step in the progression of liquid-filled to air-filled lungs of the transitioning newborn. Right: type 3 or aerated neonatal lung with horizontal A-lines, which are hyperechoic reverberation artefact produced by the ultrasound beam encountering air.1 6 8 19 20 Other ultrasound signs indicating a healthy lung include characteristic movement of the pleural line with respiration, seen as ‘lung sliding’ on B-mode video recordings and the ‘seashore sign’ on M-mode. A-lines, with no B-lines, a lack of lung sliding (abnormal movement) and the ‘stratosphere’ sign on M-mode, is indicative of pneumothorax.21 23–26

    Analysis and statistics

    The LUS grade from each side of the chest at a single time point was combined for analysis. Infants could have a grade of type 3/3 (type 3 on both sides of the chest), type 2/3 (type 2 on one side and type 3 on the other side of the chest), type 2/2 (type 2 on both sides of the chest), type 1/2 (type 1 on one side and type 2 on the other side of the chest), type 1/1 (type 1 on both sides of the chest) and so on. The Friedman test was used to compare LUS grades between time points for the whole cohort. The Kruskal-Wallis H Test using Dunn’s procedure with Bonferroni adjustment was used to compare results based on mode of delivery. Mean and SD are reported for normally distributed continuous variables and medians and 25%–75% IQR for skewed variables. Four blinded observers independently evaluated 30 video recordings and repeated the evaluation with a 3-month gap between the first and second evaluation. An intraclass correlation coefficient with a two-way random model and a one-way model was used to calculate inter-rater and intrarater reliability, respectively. Statistical significance was defined as p<0.05. Descriptive statistics were performed using IBM SPSS Statistics V.21.0.

    Results

    Between March 2015 and February 2016, we studied 115 patients and analysed 1168 videos. Mean gestational age was 386/7 weeks±11 days, and mean birth weight was 3380±555 g (table 1). Fifty-one infants were delivered vaginally, 50 via elective CS and 14 via CS after labour (table 1). Infants delivered vaginally had a significantly higher gestational age than infants born via elective CS and more time prior to umbilical cord clamping than infants delivered via CS. Infants born via elective CS had more exposure to antenatal steroids than infants born after labour. All other parameters were non-significant.

    View this table:
    Table 1

    Demographic information

    Vital signs and APGAR scores are shown in table 1. Infants who delivered vaginally had higher HRs initially, which may reflect the stress of labour; no subsequent difference was seen. We found no evidence of pneumothorax in any infants enrolled in the study. Only one infant was admitted to the nursery with tachypnoea, which started at 17 hours after birth and was thought to be due to suspected sepsis. The infant was placed on antibiotics and the tachypnoea resolved without respiratory support.

    LUS grades

    The timing of the LUS examinations is shown in table 1. The median (IQR) time of the 2-hour, 4-hour and 24-hour ultrasound examinations was 131 (120–150) min, 259 (233–300) min and 28 (24–48) hours after birth, respectively, with no differences between groups.

    At the 1–10 min examination, only 3% had type 1/1 and 13% had type 1/2. By 11–20 min examination, no infants had type 1/1 or type 1/2. By 4 hours and 24 hours after birth, 69% and 85% of infants had a type 3/3 grade, respectively. In the first 2 hours after birth, LUS grades at the different examination time points did not differ significantly. However, the LUS grades at 4 hours and 24 hours were significantly higher than at 1–10 min, 11–20 min, 1 hour and 2 hours (comparing 2 hours with 4 hours, p=0.009, p<0.001 for all other significant comparisons) (figure 2). Although a type 1/3 was possible, we did not observe a type 1/3 at any LUS examination.

    Figure 2
    Figure 2

    Lung ultrasound (LUS) grading over 24 hours for all subjects. Three-second B-mode and M-mode video loops were acquired at the midaxillary line of the right and left chest. By 10 min after birth, all infants had type 2/2 or higher. The LUS grade at 4 and 24 hours was significantly higher than at 10 min, 20 min, 1 hour and 2 hours (comparing 2 hours with 4 hours, p=0.009, p<0.001 for all other significant comparisons).

    We compared LUS grades for infants delivered vaginally, via elective CS and via CS after labour. Infants delivered via elective CS had significantly lower LUS grades than infants born vaginally and infants born via CS after labour at 1–10 min (elective CS vs vaginal delivery, p=0.001 and elective CS vs CS after labour, p=0.01) and 11–20 min (elective CS vs vaginal delivery, p<0.001 and elective CS vs CS after labour, p=0.03). At 1 hour, infant born via elective CS had non-significantly lower LUS scores (elective CS vs vaginal delivery, p=0.09 and elective CS vs CS with labour, p=0.06; figure 3). There were no differences in LUS grades between vaginally delivered infants and infants delivered via CS after labour (p=1 at 1–10 and 11–20 min).

    Figure 3
    Figure 3

    Lung ultrasound (LUS) grading over 24 hours based on mode of delivery. Infants born vaginally and infants born via caesarean section (CS) after a trial of labour had significantly higher LUS grades than infants born via elective CS (ie, CS without labour) at 1–10 min and 11–20 min. No differences were seen between vaginally delivered infants and infants born via CS after a trial of labour.

    We also compared infants delivered via elective CS and infants delivered after labour (combining vaginal birth with CS after a period of labour); infants delivered after labour had higher LUS grades at 1–10 min, 11–20 min and at 1 hour after birth (p<0.001, p<0.001, p=0.009, respectively). After the 1-hour examination, no statistical difference was seen between these two groups (p=0.09 at 2 hours, p=0.6 at 4 hours and p=0.46 at 24 hours).

    ‘Backsliding’

    Several infants had achieved a type 3 grade on one side of the chest, but then had a type 2 grade on that side in subsequent examinations. We called this ‘backsliding’, which refers to the LUS grade worsening from one time point to the next. Overall, backsliding occurred at least once in 47% of the infants, with 10% backsliding twice. Backsliding occurred less frequently at each subsequent time point (table 2). Backsliding was seen in 51%, 38% and 57% of infants delivered vaginally, via elective CS and via CS after labour, respectively, and did not differ based on mode of delivery (p=0.14). No infant regressed to a type 1/1 and we only observed one example of an infant regressing to type 2/1 grade. This occurred between the 20 min and 1-hour examination. The infant then was graded as type 2/2 on the 2-hour examination. Between the 4-hour and 24-hour examinations, no backsliding was observed.

    View this table:
    Table 2

    ‘Backsliding,’ the percentage of infants at each time point that had a ‘lower’ lung ultrasound (LUS) grade at the subsequent examination

    Inter-rater and intrarater reliability

    Intraclass correlation coefficient confirmed that there was a strong positive correlation for inter-rater reliability (k=0.96, 95% CI 0.93 to 0.98) and intrarater reliability (rater 1: k=0.96, 95% CI 0.91 to 0.98, rater 2: k=0.9, 95% CI 0.8 to 0.95, rater 3: k=0.85, 95% CI 0.72 to 0.93, rater 4: k=0.79, 95% CI 0.61 to 0.9).

    Discussion

    This is the earliest study, starting within 10 min after birth, to use ultrasound to describe the temporal change in airway liquid clearance in healthy term and near term infants until neonatal adaption to birth is complete. LUS has been used previously to predict which infants will need admission to the neonatal intensive care unit (NICU), which preterm infants will receive surfactant, and to describe transient tachypnoea of the newborn, meconium aspiration syndrome, pneumothorax and the appearance of the lungs after surfactant administration.2–7 11 24 The present study might be used as a reference for identifying airway liquid retention and monitoring the progress of lung aeration after birth.

    Animal studies indicate that the primary mechanism of airway liquid clearance is likely due to the negative pressure generated during inspiration, which drives the liquid out of the airways.27–30 Infants born after a period of labour likely had some liquid clearance before birth, which may explain why they had higher LUS grades in the first hour after birth compared with infants born via elective CS. Although our numbers are small, infants in this study who were exposed to labour had similar LUS grades at all time points, regardless if they were delivered vaginally or via CS. Of note, 38% of the infants delivered by elective CS in this study had received antenatal steroids to reduce the risk of respiratory distress after delivery. The mechanism may be due to enhancing lung liquid clearance, potentially explaining why we only saw a difference in LUS grades between different modes of delivery initially, but no difference by 2 hours after birth.11 31 32

    We observed partial or complete liquid clearance occur within the first minutes after birth in this cohort of healthy infants. After establishment of lung inflation, residual lung liquid may take several hours to clear. In addition to intrapleural pressure differences, secondary mechanisms of lung liquid absorption likely contribute to this process. Most of the infants in this study were crying vigorously during the 1–10 and 11–20 min examinations, then transitioned to quiet breathing by the 1-hour and 2-hour examinations. ‘Backsliding’ from type 3 and type 2 was seen in 47% of the infants, likely due to liquid re-entry into the airways. Fluctuation in LUS grades may be dependent on the infant transitioning from vigorous crying immediately after birth to quiet, regular breathing observed several minutes after birth. Quiet breathing may not generate the same intrathoracic pressure to drive the lung liquid into the interstitial space. In the current study, only one infant showed backsliding from type 2/2 transiently to a type 1/2. No infants had a type 1/1 after 10 min after birth. Only three infants had a type 1/1 grade at the first examination. All were born via elective CS and all had the first LUS examination at 1 min after birth.

    A limitation of this study was the lack of infants with tachypnoea or respiratory distress. We can only speculate on the utility of LUS in the delivery room to detect and manage common neonatal pathologies. Raimondi and colleagues2 3 reported that a type 1/1 grade at 120 min after birth correlates with respiratory distress syndrome and the need for support. In addition, 4 out of 46 infants with a type 2 grade in that study were subsequently admitted to the NICU for continuous positive airway pressure and oxygen. No infant in the current study was admitted for respiratory distress and very few had tachypnoea after birth, despite the prevalence of infants with a type 2/2 grade (38% at 2 hours). The difference in clinical outcomes between studies may be due to a more mature patient population, differences in interpretation, chance variation or error in the ability of LUS to detect respiratory distress. Other studies support that there may be no clinical difference between infants with type 2/2 and better LUS grades in the first hours after birth.5 6 13 15 We only observed type 1/1 or 1/2 transiently in 14% of infants; it is possible that these images are subtly different than images due to respiratory distress syndrome. However, the strong agreement in LUS grades (inter-rater and intrarater reliability) was reassuring.

    Conclusion

    In a population of healthy newborns, all infants achieved lung aeration and partial airway liquid clearance within the first 20 min after birth. Serial LUS can be used to monitor changes in lung aeration and airway liquid clearance after birth. Complete airway liquid clearance is typically achieved within the first 4 hours after birth. Further studies using LUS in the delivery room for diagnosis and management pathological conditions of the newborn are warranted.

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    Footnotes

    • Contributors All authors have made significant contributions to the conception and design of the study, acquisition of data, data analysis and interpretation, drafting and revising the manuscript and final approval. All research was conducted at the Royal Women’s Hospital, Melbourne, Victoria, Australia. DAB wrote the first draft of the manuscript. No author received payment to produce the manuscript. All authors have reviewed and approve of the submitted version of the manuscript and they take full responsibility for the content.

    • Competing interests None declared.

    • Patient consent Guardian consent obtained.

    • Ethics approval The Royal Women’s Hospital.

    • Provenance and peer review Not commissioned; externally peer reviewed.