Use of Neonatal Chest Ultrasound to PredictNoninvasive Ventilation Failure

WHAT’S KNOWN ON THIS SUBJECT: Lung ultrasound outperformsconventional radiology in the emergency diagnosis ofpneumothorax and pleural effusions. In the pediatric age, lungultrasound has been also successfully applied to the fluid-to-airtransition after birth and to rapid pneumonia diagnosis.

WHAT THIS STUDY ADDS: Nasal ventilation has dramaticallydecreased the need for invasive mechanical respiratory support.This study demonstrates that, after a short trial on nasalcontinuous positive airway pressure, lung ultrasonographyreliably predicts the failure of noninvasive ventilation unlike theconventional chest radiogram.

abstractBACKGROUND: Noninvasive ventilation is the treatment of choice forneonatal moderate respiratory distress (RD). Predictors of nasal ven-tilation failure are helpful in preventing clinical deterioration. Work onneonatal lung ultrasound has shown that the persistence of a hyper-echogenic, “white lung” image correlates with severe distress in thepreterm infant. We investigate the persistent white lung ultrasoundimage as a marker of noninvasive ventilation failure.

METHODS: Newborns admitted to the NICU with moderate RD and sta-bilized on nasal continuous positive airway pressure for 120 minuteswere enrolled. Lung ultrasound was performed and blindly classifiedas type 1 (white lung), type 2 (prevalence of B-lines), or type 3(prevalence of A-lines). Chest radiograph also was examined andgraded by an experienced radiologist blind to the infant’s clinicalcondition. Outcome of the study was the accuracy of bilateral type1 to predict intubation within 24 hours from scanning. Secondaryoutcome was the performance of the highest radiographic gradewithin the same time interval.

RESULTS: We enrolled 54 infants (gestational age 32.5 6 2.6 weeks;birth weight 1703 6 583 g). Type 1 lung profile showed sensitivity88.9%, specificity 100%, positive predictive value 100%, and negativepredictive value 94.7%. Chest radiograph had sensitivity 38.9%, spec-ificity 77.8%, positive predictive value 46.7%, and negative predictivevalue 71.8%.

CONCLUSIONS: After a 2-hour nasal ventilation trial, neonatal lung ul-trasound is a useful predictor of the need for intubation, largely out-performing conventional radiology. Future studies should addresswhether including ultrasonography in the management of neonatal mod-erate RD confers clinical advantages. Pediatrics 2014;134:e1089–e1094

AUTHORS: Francesco Raimondi, MD, PhD,a FiorellaMigliaro, MD,a Angela Sodano, MD,a Teresa Ferrara, MD,a

Silvia Lama, MD,a Gianfranco Vallone, MD,b and LetiziaCapasso, MDa

aDivision of Neonatology, Section of Pediatrics, Department ofTranslational Medical Sciences, and bDivision of PediatricDiagnostics, Department of Biomorphological and FunctionalSciences, Università “Federico II,” Naples, Italy

KEY WORDSultrasonography, lung, neonate, distress

ABBREVIATIONSCI—confidence intervalFN—false-negativeFP—false-positivenCPAP—nasal continuous positive airway pressureNIV—noninvasive ventilationNPV—negative predictive valuePPV—positive predictive valueRD—respiratory distressTN—true-negativeTP—true-positive

Dr Raimondi conceived and designed the study, drafted theinitial manuscript, and approved the final manuscript assubmitted; Drs Migliaro and Sodano carried out the initialanalyses, performed the ultrasound scans, and reviewed andrevised the manuscript; Dr Vallone reviewed the ultrasoundscans and the chest radiographs as a third, masked observer;Drs Ferrara and Lama designed the data collection instruments,coordinated and supervised data collection, and providedstatistical support; and Dr Capasso critically reviewed themanuscript and approved the final manuscript as submitted.

www.pediatrics.org/cgi/doi/10.1542/peds.2013-3924

doi:10.1542/peds.2013-3924

Accepted for publication Jul 24, 2014

Address correspondence to Francesco Raimondi, MD, PhD,Division of Neonatology, Section of Pediatrics, Department ofTranslational Medical Sciences, Università “Federico II”, viaPansini 5, 80131 Napoli, Italy. E-mail: raimondi@unina.it

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2014 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they haveno financial relationships relevant to this article to disclose.

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have indicatedthey have no potential conflicts of interest to disclose.

PEDIATRICS Volume 134, Number 4, October 2014 e1089

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Chest ultrasound has recently beenapplied with success in different set-tings of adult medicine, ranging fromcardiopulmonary emergencies andtrauma surgery to the care of pre-eclampticwomenorpatientswith renalfailure.1–4

A systematic ultrasound semeiologyhas been validated across a wide spanof ages using both chest anatomicstructures (ie, the ribs or the pleuralline)andartifactual images, suchas theB-lines, that are discrete, laserlikevertical hyperechoic reverberationsarising from the pleural line. Multiplediffuse bilateral B-lines are suggestiveof interstitial syndrome (eg, pulmonaryedema, interstitial pneumonia, diffuseparenchymal lung disease)5 (Fig 1A). Inthe neonate, one can accurately dif-ferentiate the aerated dry lung,appearing as uniform hypoechogenicpattern, sliding with respiration andoften showing horizontal reverber-ations of the pleural image (the A-lines)(Fig 1B) from the hyperechogenic“white” pattern of the markedly “wet”or inflamed organ (Fig 1C)6–8

Noninvasive ventilation (NIV) is widelyused for the treatment of moderate re-spiratory disease of the newborn tostabilize spontaneous breathing whileavoiding the complications of invasiveventilation.9,10 NIV-assisted infants aremore easily accessed by parents andhealth care givers, allowing an optimi-

zation also of nonventilatory strategies.However, clinical monitoring of theseinfants is needed, as some will pro-gressively show increased respiratoryeffort and/or deterioration of bloodgas exchange requiring endotrachealintubation, surfactant administration,and mechanical ventilation. At present,there is a need for reliable predictors ofNIV failure that would spare the infantbecoming exhausted from ineffectivebreathing. As clinics and chest radio-graphs are often discordant in gradingthe severity of neonatal respiratorydistress syndrome, conventional radi-ology is often of little help. On the otherhand, the persistence of a “white-lung”ultrasound image has been shown tocorrelate with clinical respiratory dis-tress (RD) in preterm infants.11 In thepresent study, we hypothesized that thismarker may predict the failure of nasalcontinuous positive airway pressure(nCPAP) in aerating the premature lung,heralding the need for a more invasiveapproach.

METHODS

The study was conducted from December2012 to July 2013 in a level 3 hospitalwith 2400 total births per year. The in-vestigation received permission from thelocal institutional review board and for-mal consent was obtained from theparents. Newborns were enrolled if ad-mitted to the NICU for moderate RD and

treated with nCPAP. These criteria in-cluded infants of any degree of pre-maturity who had mild symptoms(tachypnea, shallow breathing, grunting,nasal flaring, sub- and intercostal re-tractions) before stabilization on nCPAP(+4–5 cm H2O and FiO2 ,0.4 to keep ox-ygen saturation in the 92%–96% range,with a respiratory rate ,60/min andpH .7.28, PaO2 .50 mmHg, PaCO2,60 mmHg).12 Infants with major con-genital malformations and those intu-bated in the delivery room or within20 minutes after admission to the NICUwere excluded from the study.

Failure of NIV was defined as endotra-cheal intubation and surfactant ad-ministration (Curosurf, Parma, Italy;200 mg/kg) without attempting furtherNIV strategies. This procedure waseventually performed by the attendingneonatologist, who was blind to thestudy, in case chest dynamics weredeteriorating (evidence of severeupper/lower chest or xyphoid retrac-tions, marked nares dilatation, or ex-piratory grunting) and/or if the infantfailed to maintain adequate blood gasvalues as reported previously.

At admission, infants were placed onnCPAP in an incubator and vascularaccess was established. After 120minutes from nCPAP application, lungultrasound images were acquiredscanning each lung in the anterior andlateral projectionswith the infant in the

FIGURE 1A, The prevalence of B-lines (arrows) has been linked to the interstitial syndrome in the adult and to a progressive aeration of the neonatal lung after birth. B,Reverberations of thepleural image (also knownas A-lines) in the normally aerated lung. C,White-lung image soonafter birth; its persistencehasbeen linked tothe inflamed lung with hyaline membrane disease.

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supine position. This time point waschosen because it is the conventionaltime limit for early versus late surfac-tant rescue13 and because of experi-mental animal evidence that lung fluidclearance is accomplished in 2 hours.14

A broadband linear transducer (modL12–5; Philips, Eindhoven, Netherlands)that encompasses the superior andinferior lung fields in the same imagewas used. Images were classified astype 1 (white lung), type 2 (prevalenceof B-lines), and type 3 (prevalence ofA-lines), as previously described.15

Chest radiographs were acquired in thesame time frame with a portable device(Practix 33 plus; Philips, Eindhoven,Netherlands) at the infant’s incubator.Images were classified as grade 1 (finehomogeneous ground glass shadow-ing), grade 2 (addition ofwidespread airbronchograms), grade 3 (developmentof confluent alveolar shadowing), andgrade 4 (complete white-out of the lungfields with obscuring of the cardiacborder in the most severe cases).16

To ensure proper blinding, lung ultra-sound scans and chest radiographswere coded when acquired in the NICUand classified as previously describedby an experienced pediatric radiologistwho was blind to the infants’ clinicalcondition. Blind evaluation of codedlung scans was also performed by anexperienced neonatologist to assessinterobserver variability. The mainoutcome of the study was the accuracyof the sonographic profile with maxi-mal echodensity (type 1 or white lung)to predict intubation within 24 hoursfrom scanning. The secondary outcomewas the accuracy of the highest radio-graphic grade to predict intubationwithin the same time interval.

Statistics

In a nursery setting,15 a type 1 lung ul-trasound profile had a 77.7% sensitivityin predicting the need of ventilatorysupport shortly after birth. We calcu-

lated that a population of 54 pretermneonates was required to estimate the99% confidence intervals (CIs) fora sensitivity of type 1 lung ultrasoundprofile of 85.0% 6 12.5%. We definedtrue-positive (TP) as type 1 and intu-bated; true-negative (TN) as type 2 or 3and not intubated; false-positive (FP) astype 1 and not intubated; false-negative(FN) as type 2 or 3 and intubated. Thespecificity of the test was defined asTN/(TN+FP); sensitivity was TP/(TP+FN);positive predictive value (PPV) wasTP/(TP+FP); negative predictive value(NPV) was TN/(TN+FN). Ninety-five per-cent CIs around measures of test char-acteristics were calculated by using thenormal distribution mode, according tothe following formula:

sample  value6 1:96 3 standard   error:

The k coefficient was also provided toassess the interobserver variability.Our cohort was divided by gestationalage (.29 weeks vs ,29 weeks); Pvalues to show differences betweenthese groups were calculated by usingStudent t test for continuous variablesand exact x2 test for categorical vari-ables. A level of P, .05 was chosen asstatistically significant.

RESULTS

A total of 72 neonates presented with RDand were initially treated with nCPAP; 18were excluded because of endotrachealintubation before entering the NICU (15infants) or within 20 minutes from ad-

mission. Fifty-four infants were thenenrolled in the study; their demographiccharacteristics are shown in Table 1.There was no significant difference be-tween infants who succeeded or failednCPAP (data not shown). Based on lungultrasound scan after 120 minutes onnCPAP, 24 neonates were assigned totype 3, 12 to type 2, and 16 to type 1. Theremaining 2 neonates showed a type 1on one side and type 2 on the other. Allnewborns with either unilateral or bi-lateral type 1 were intubated after anaverage interval of 6 hours. No infantwith type 2 or type 3 profile was in-tubated. In predicting failure of NIV,bilateral type 1 had the following ac-curacy: sensitivity 88.9% (CI 67.2–96.8),specificity 100% (CI 94.9–100), PPV 100%(CI 80.6–100), NPV 94.7% (CI 82.7–98.5).On the basis of the chest radiograph, noinfant was assigned to grade 4 or 3,whereas 15 neonates were assigned tograde 2 and 39 to grade 1. The accuracyof grade 2 to predict intubation was asfollows: sensitivity 38.9% (CI 20–61.1),specificity 77.8% (CI 61.7–88.5), PPV46.7% (CI 24.8–69.9), NPV 71.8% (CI 56.2–83.4). Concordance of ultrasound andradiographic results is shown in Table 2.There was full interobserver agreementin the images’ interpretation (k = 1).The average duration of a complete ul-trasound scan was 2.5 minutes andthe examination was well tolerated byenrolled patients. All scans showeda normal pleural line and sliding sign;no air-leak syndromes were docu-mented throughout the study.

TABLE 1 Demographic Characteristics of the Study Cohort

Characteristics GA ,29 wk n = 10 GA .29 wk n = 44 P

Mean birth weight, g (SD) 1080 (94) 1810 (253) 0.10Cesarean delivery 7 26 0.41Apgar ,7 @ 1 min 3 9 0.43Apgar ,7 @ 5 min 0 0 N/AROM .12 h 2 6 0.26Prenatal steroids, 2 doses 0 28 0.35Failed nCPAP 4 14 0.25PaO2 at intubation (SD) 41.1 (1.8) 46.3 (2.1) 0.08PaCO2 at intubation (SD) 70.3 (3.1) 68.0 (3.2) 0.12

GA, gestational age; N/A, not applicable; ROM, rupture of membranes.

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DISCUSSION

Our data show that, unlike the con-ventional radiograph, lung ultrasoundcan accurately predict those newbornswith RD who will fail NIV (Fig 2). In theNICU setting, our work marks a novelapproach to both neonatal respiratorymanagement and lung ultrasonogra-phy. Previous authors had describedultrasound signs for hyaline mem-brane disease,11 transient tachypnea ofthe newborn,17 pneumonia,18 pneumo-thorax,19 and pleural effusion.20 Weprovide evidence to a functional appli-

cation of lung ultrasound. This in-formation is rapidly obtained at thebedside without any radiation expo-sure and can be acquired with a fairlysteep learning curve.5 In the study byShah et al,21 only 60 minutes of trainingwas needed to accurately diagnosepneumonia in children, outperformingconventional chest radiographs. Usinglung ultrasonography as an NIV failurepredictor can be particularly useful forlevel 1 and 2 nurseries where limitedrespiratory support may be occasion-ally available but transferring a neo-

nate to a level 3 NICU has to be carefullyplanned in advance.

There is a paucity of data on techniquesor parameters that monitor RD reliablyenough to predict intubation. A clinical-radiologic correlation was attemptedby Kero and Mäkinen22 in 55 preterminfants (mean gestational age: 33weeks) with mild, moderate, and se-vere RDS. It is not clear whether theinvestigation was properly masked,but they report a 38% general dis-agreement between clinical and ra-diologic criteria and only a 50%agreement rate on moderate RDS. Thesame radiologic criteria were used inassociation with clinical intubationpredictors in a large retrospective co-hort by Ammari et al.23 None of the 3variables associated with CPAP failure(positive pressure ventilation at birth,an alveolar-arterial oxygen tension

TABLE 2 Concordance of Ultrasound and Radiographic Results

Ultrasound Result Radiographic Result

Grade 4 Grade 3 Grade 2 Grade 1

Type 1 0 0 7 9Type 2 0 0 6 6Type 3 0 0 2 22Type 1/2 0 0 0 2

FIGURE 2Comparedchest ultrasound and radiographof 31-week twins onCPAPbecause ofmoderate RDafter birth. Twin 1was intubated and received a surfactant dose;twin 2 transitioned to room air. Lung ultrasound showed uniform hyperechogenicity for twin 1 (B) and A-lines for twin 2 (D). Both radiographs showed groundglass opacity and bronchograms (A–C).

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gradient.180 mm Hg and severe RDSon the initial chest radiograph) hada positive predictive value .55%. Adifferent clinical predictor, such as themaximal oxygen requirement in thefirst 72 hours of life, was studied byMorosini and Davies24 in a retrospec-tive cohort of 592 infants with a gesta-tional age.32 weeks and any cause ofRD. They found that a maximal FiO2$0.5 gave a PPV of 60% and NPV of100% (sensitivity = 0.93, specificity =0.91) for need for intubation and in-termittent positive pressure ventila-tion. From their data, however, it isunclear exactly when this maximal ox-ygen requirement was reached beforeintubation. The lack of this piece of in-formation and of prospective valida-tion are important limits to thepractical application of this interestingarticle. Boo et al25 prospectively in-vestigated 97 consecutive preterminfants (,37 weeks) with an un-specified level of nCPAP: pneumothoraxand sepsis during treatment weresignificant CPAP failure predictors. Inthe adult, lung ultrasonography alsohas been proven a useful predictor of

extubation failure but data in the pe-diatric or neonatal settings are cur-rently lacking.26

We acknowledge that our protocol hassome limitations that restrict the im-mediate generalization of our results.First, by applying a narrow interval ofCPAP (4–5 cm H2O), we might have in-cluded in the NIV failure group someinfants who would have achieveda better lung recruitment with higherpressures. However, multiple CPAPadjustments would have required re-peated ultrasound scans, which, in turn,represent a conspicuous intrusion intothe routine clinical care and a threat tothe study masking. We believe that in-vestigating lung ultrasound changes inresponse to CPAP optimization is a clin-ically relevant topic for a separate study,as already attempted in the adult.27 Inaddition, a fixed CPAP level was used insome of the largest international, mul-ticenter trials on continuous distendingpressure. Although the Neocosur28 trialused 5 cm H2O, the COIN trial with 8 cmH2O29 documented a significant higherrate of air-leak syndromes, restrictingthe window of clinically useful pres-

sures. Second, our series encompassesa wide range of birth weights. We feel,however, that the CPAP failure rate inour series (33%) is in keeping withcurrent practices. Recent data from theVermont Oxford Network regarding 20200 very low birth weight infants reportan early CPAP failure rate of 34.3%, withan upper quartile set at 46.2%.

CONCLUSIONS

Although NIV is an effective and gentleway of respiratory support in the pre-term infant, it is not without limits orrisks. At the bedside, lung ultrasonog-raphy is an accurate method for pre-dicting the failure of NIV and it isadvantageous over chest radiography.

ACKNOWLEDGMENTSTheauthors thankDrEduardoBancalari,University of Miami, Dr Alistair Philip,Stanford University, and Dr FabrizioSandri, Ospedale Maggiore di Bolognafor their helpful suggestions. The au-thors also are grateful to RobertoPaludetto, MD, for his NICU clinical su-pervision while the study was ongoing.

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DOI: 10.1542/peds.2013-3924 originally published online September 1, 2014; 2014;134;e1089Pediatrics 

Gianfranco Vallone and Letizia CapassoFrancesco Raimondi, Fiorella Migliaro, Angela Sodano, Teresa Ferrara, Silvia Lama,

Use of Neonatal Chest Ultrasound to Predict Noninvasive Ventilation Failure

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DOI: 10.1542/peds.2013-3924 originally published online September 1, 2014; 2014;134;e1089Pediatrics 

Gianfranco Vallone and Letizia CapassoFrancesco Raimondi, Fiorella Migliaro, Angela Sodano, Teresa Ferrara, Silvia Lama,

Use of Neonatal Chest Ultrasound to Predict Noninvasive Ventilation Failure

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