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  Early Human Development 90S2 (2014) S41  –  S43   Contents lists available at ScienceDirect   Early Human Development    j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / e a r l h u m d e v   Research article   Lung ultrasound findings in meconium aspiration syndrome   Marco Piastra a , Nadya Yousef  b,c,  *, Roselyne Brat c , Paolo Manzoni d , Mostafa Mokhtari  b , Daniele De Luca a,c   a    Pediatric Intensive Care Unit, Institute of Anesthesiology and Critical Care, University Hospital “A.   Gemelli”, Catholic University of the Sacred Heart, Rome, Italy    b    Neonatal and Pediatric Intensive Care Unit, FAME Department, South Paris University Hospitals, “Kremlin -  Bicˆetre” Medical Center, Paris, France   c    Division of Pediatrics and Neonatal Critical Ca re, FAME Department, South Paris University Hospitals, “A. Becl`ere” Medical Center, Paris, France d   Neonatal Intensive Care Unit, OISRM S. Anna, Turin, Italy   a r t i c l e i n f o   s u m m a r y    Keywords:   Meconium aspiration syndrome (MAS) is a rare and life-threatening neonatal lung injury induced   Meconium aspiration   y meconium in the lung and airways. Lung ultrasound (LUS) is a quick, easy and cheap imaging    Neonate   technique that is increasingly being used in critical care settings, also for newborns. In this paper    Lung ultrasound   e describe ultrasound findings in MAS.   Six patients with MAS of variable severity were examined by LUS during the first hours of life.   Chest X-rays were used as reference.   The following dynamic LUS signs were seen in all patients: (1) B-pattern (interstitial) coalescent   or sparse; (2) consolidations; (3) atelectasis; (4) bronchograms. No pattern was observed for    the distribution of signs in lung areas, although the signs varied with time, probably due to   the changing localisation of meconium in the lungs. LUS images corresponded well with X-ray   findings.   In conclusion, we provide the first formal description of LUS findings in neonates with MAS. LUS   is a useful and promising tool in the diagnosis and management of MAS, providing real-time   edside imaging, with the additional potential benefit of limiting radiation exposure in sick    neonates.   © 2014 Elsevier Ireland Ltd. All rights reserved.   1. Introduction   Meconium aspiration syndrome (MAS) is a rare and life-threatening neonatal lung injury caused by several patho-physiological mechanisms induced by meconium in lung tissue and airways [1]. Lung ultrasound (LUS) is a quick, easy and relatively inexpensive imaging technique that is slowly gaining popularity as a tool to diagnose and monitor lung diseases. LUS is increasingly being used in critical care settings and specific recommendations for bedside use have recently been elaborated [2]. LUS provides accurate diagnostic information when compared with conventional lung imaging methods, such as CT scans and chest radiographs [3], and has the additional advantage of being non-irradiating, adapted to bedside use and easily repeatable with no side effects for the patient. LUS is easy to learn, does not require sophisticated ultrasound machines or settings, and shows low intra- and interobserver variability when a standardized approach is used [4].   *   Corresponding author. Dr. Nadya Yousef, MD, Service de P ediatrie´ et Reanimation´ Neonatale,´ Groupe Hospitalo-Universitaire Paris Sud, CHU “A. Becl´ere”,` 157 rue de la Porte de Trivaux, 92140 Clamart (Paris), France. Tel.: +33145374837.  E-mail address: nadya.yousef@bct.aphp.fr (N. Yousef). LUS can also be used to diagnose neonatal lung disease [4  –  6]. The same LUS signs are found in the lung of a newborn baby as in that of an adult [7]. Specific LUS findings have been described for some types of neonatal lung injury, such as neonatal respiratory distress syndrome [8,9], transient tachypnea of the neonate [9,10] and neonatal pneumonia [11]. No formal data exist on ultrasound imaging of MAS, although some of its pathophysiological characteristics produce visible signs on LUS [4].   Here we provide a first comprehensive description of MAS semiology using LUS.   2. Methods   Six term neonates presenting with MAS, and recruited from three tertiary neonatal intensive care units in Italy and France (A. Gemelli Hospital in Rome, Italy, and the South Paris University Hospitals of Antoine Becl´ere` and Bicˆetre in Paris, France), underwent lung examination with ultrasound in the first 24 hours after admission. Standard chest radiographs were performed according to local protocol.   The operators were not blinded; LUS was performed by a  pediatrician/neonatologist skilled in lung and heart sonography who knew the patient’s condition and history. The choice of    0378-3782/$  –   see front matter © 2014 Elsevier Ireland Ltd. All rights reserved.    S42    M. Piastra et al. / Early Human Development 90S2 (2014) S41  –  S43   Table 1   Basic data of the study population   Patient 1   Patient 2   Patient 3   Patient 4   Patient 5   Patient 6   Gestational age (weeks)   40   39   40   40   41   40   Body weight (g)   3990   4020   3020   2945   3200   3500   Gender    M   F   M   F   F   F   Apgar score   1   2   3   1   3   1   1   5   4   4   8   5   1   6   SNAPPE-II   41   26   30   23   25   39   Respiratory support during lung US   HFOV, iNO   HFOV   CMV   O 2  therapy   CMV   CMV   CMV, conventional mechanical ventilation; HFOV, High-frequency oscillatory ventilation; iNO, inhaled nitric oxide; SNAPPE-II, Score for Neonatal Acute Physiology  –   Perinatal Extension.   ultrasound device and probe depended on local availability; for patients 1 and 2, an 8  –  4 MHz phase array probe was used (Sonosite M-Turbo, Fujifilm Sonosite Inc.) to obtain transversal and longitudinal scans of the anterior chest wall; for patients 3 and 4, an 8 MHz curved array probe (GE Loqiq 7, GE Healthcare, General Electric Company) was used; and for patients 5 and 6, a high-resolution 12  –  18 MHz linear probe (GE Logiq E9; GE Healthcare, General Electric Company) was used to scan the anterior, lateral and posterior chest walls.   Fig. 1. Comparison between chest X-rays and LUS for (A) patient 1 and (B)    patient 2. LUS was  performed with an 8  –  4 MHz phased array probe. Transversal and longitudinal scans of the anterior chest wall (3 rd  intercostal space) were obtained in the supine position. Confluent B-lines and bronchograms (panel A) and irregular consolidation (panel B) are visible. These correspond with irregular “snow - like” opacities on the chest -X rays.   3. Study cases   We observed six cases of MAS of variable severity (Table 1). The following LUS signs were found in all patients: (1) B-pattern (interstitial) coalescent or sparse; (2) consolidations; (3) at-electasis; (4)  bronchograms (often with irregular borders) and airway inflammation. We did not find any specific pattern for the distribution of these signs in the different lung areas.   The signs seen on LUS in the six neonates with MAS using the different ultrasound probes are shown in Fig. 1 (neonates 1 and 2), Fig. 2 (neonates 3 and 4), Fig. 3 (neonate 5) and Fig. 4 (neonate 6). Chest radiographs, which are the current imaging gold standard for MAS, are  provided for comparison. The observed LUS images corresponded well with X-ray findings. LUS signs were dynamic and varied throughout the clinical course; different signs appeared in the same lung area over time, reflecting the changing auscultation patterns. We believe this varying  pattern to be due to the changing distribution of meconium and to the displacement and/or dissolution of meconium plugs.   The concurrent and irregular presence of the above-described signs has never been formally described in other neonatal respiratory conditions.   Fig. 2. Comparison between chest X-rays and LUS for (A) patient 3 and (B) patient 4.   Transversal and longitudinal scans of the anterior chest wall were made using an 8 MHz curved array probe with the patient in the supine position. Confluent B-lines and irregular consolidations are visible in panel A. Panel B shows a patient in a less severe phase (well-spaced B-lines and A-lines visible). The corresponding chest X-rays were clearly different for the two cases (snow-like appearance with alveolar opacities for panel A, mild opacities and aerated lung for panel B).   Fig. 3. Comparison between chest X-rays and LUS for patient 5. LUS was performed   on admission with a 12  –  18 MHz linear probe. Longitudinal and horizontal scans of the anterior and  postero-lateral chest wall were performed in the supine position. LUS showed an irregular and thickened pleural line (panel A), multiple B-lines (panels A  –  D), with areas of B-line confluence (panels D, E), as well as multiple consolidations (panels B, C, F) with numerous bronchograms (panels B, C, E, F) and pleural effusion (panel F). These findings were more severe for the right lung. The corresponding chest radiograph shows multiple bilateral ill-defined opacities.    . Piastra et al. / Early Human Development 90S2 (2014) S41  –  S43   S43   Fig. 4. Comparison between chest X-ray and LUS for patient 6. LUS was performed   in the supine position, with a 12  –  18 MHz linear probe, 24 hours after birth when the patient was already showing clinical improvement. Compared to patient 5, LUS showed a more aerated lung with fewer and more widely spaced B-lines, a few sub-pleural consolidations, and some visible A-lines. A horizontal scan of the postero-lateral chest wall is presented here with the corresponding chest radiograph, which shows well-aerated lungs and mild opacities.   4. Discussion   LUS is based on the analysis of artifacts that arise from the interaction of air and interstitial fluid in the lung [3  –  5]. In a normal lung the pleura is seen as a regular hyperechoic line that moves with respiration. The  presence of air in the lungs gives rise to horizontal artifacts called A-lines, which are seen as a series of echoic parallel lines. An abnormality of the interstitial or alveolar compartment gives rise to vertical artifacts defined as B- lines. Lung consolidation has a ‘tissue - like’ aspect, often with irregular borders with movement of air in the bronchioles represented by bronchograms. The normal lung of a newborn has a ‘black appearance’, although  B-lines may be seen in the first day of life [4,5]. Although LUS is slowly gaining ground in neonatal intensive care units, and despite all its advantages, with few exceptions, LUS is still not included in the systematic diagnostic workup of neonatal respiratory distress.   In the six patients with MAS, we observed a range of unevenly distributed dynamic signs. The lungs showed a changing and irregular  presence of a variety of signs in the different lung areas during the clinical course, which were easily detected by portable ultrasound devices. The choice of ultrasound probe did not influence the result of LUS, although a precise evaluation of the pleural line was not possible using the phased array and the curved array probes. Both standard chest radiographs and LUS show typical and easily interpreted findings in MAS, but LUS has the added advantage of allowing for a three-dimensional and serial/real time evaluation of the lungs at both the  parenchyma and the airway level, thereby describing more closely the clinical situation.   Even though this is not shown in our cases, severe MAS with extensive surfactant dysfunction could progress to a fully condensed (white) lung [4], which is clearly a form of meconium-induced acute respiratory distress syndrome through increased inflammation and surfactant catabolism [12].   LUS in neonates and infants is usually performed using linear, high-resolution probes [3  –  5]. Our imaging has been provided with different  probes, according to the availability in the different centres; despite this limitation, consistent and reasonable findings were found. Our cases were collected from several tertiary referral centers due to the fact that MAS has become a rare disease [12] and hence one single center would not be able to see enough cases.   LUS should not be a substitute for standard chest radio-graphs [4], which easily provide the diagnosis of MAS. However, LUS can reduce the use of X-rays in clinical practice, with clear benefits in terms of irradiation [13], especially if multiple serial imaging needs to be  performed. LUS allows for a three-dimensional study of different lung areas, whilst chest X-rays describe them only in a single projection. Finally, LUS allows for real time bedside follow-up of patients since the observed signs change with the improving clinical picture.   Conversely, it is important to note that LUS might express all its  potential only if used by clinicians who know the patient’s clinical history and, therefore, if imaging and clinical findings are correlated [3,4,7]. A future step would be to study the potential of LUS to estimate lung aeration and to guide mechanical ventilation at the bedside: this will require specific clinical studies and technical improvements.   In conclusion, we provide the first formal data about US imaging of MAS. This may be useful in clinical practice and as a future research tool.   Conflict of interest statement   The authors have no conflicts of interest to declare.   References   1.   van Yerland Y, de Beaufort AJ. Why does meconium cause meconium aspiration syndrome? Current concepts of MAS pathophysiology. Early Hum Dev 2009;85: 617  –  20. 2.   Volpicelli G, Elbarbary M, Blaivas M, Lichtenstein DA, Mathis G, Kirkpatrick AW, et al.; International Liaison Committee on Lung Ultrasound (ILC-LUS) for International Consensus Conference on Lung Ultrasound (ICC-LUS). International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012;38:577  –  91. 3.   Lichtenstein D, Mauriat P. Lung ultrasound in the critically ill neonate. Curr Pediatr Rev 2012;8(3):217  –  23. 4.   Cattarossi L. Lung ultrasound: its role in neonatology and pediatrics. Early Hum Dev 2013;89(Suppl 1):S17  –  9. 5.   Liu J. Lung ultrasonography for the diagnosis of neonatal lung disease. J Matern Fetal  Neonatal Med 2014;27(8):856  –  61. 6.   Raimondi F, Migliaro F, Sodano A, Vallone G, Ferrara T, Maddaluno S, et al. Point-of-care chest ultrasound in the Neonatal Intensive Care Unit. J Pediatr Neonat Individual Med 2013;2(2):e020214. 7.   Lichtenstein D. Ultrasound examination of the lungs in the intensive care unit. Pediatr Crit Care Med 2009;10(6):693  –  8. 8.   Copetti R, Cattarossi L, Macagno F, Violino M, Furlan R. Lung ultrasound in respiratory distress syndrome: a useful tool for early diagnosis. Neonatology 2008;94:52  –  9.   9. Vergine   M, Copetti R, Brusa G, Cattarossi L. Lung ultrasound accuracy in respiratory distress syndrome and transient tachypnea of the newborn. Neonatology 2014;106(2):87  –  93.   10.   Copetti R, Cattarossi L. The ‘double lung point’: an ultrasound sign diagnostic of transi ent tachypnea of the newborn. Neonatology 2007;91:203  –  9. 11.   Liu J, Liu F, Liu Y, Wang HW, Feng ZC. Lung ultrasound for the diagnosis of severe neonatal pneumonia. Chest 2014 May 15 [Epub ahead of print]. doi: 10.1378/ chest.13-2852. 12.   De Luca D, Minucci A, Tripodi D, Piastra M, Pietrini D, Zuppi C, et al. Role of distinct  phospholipases A2 and their modulators in meconium aspiration syndrome in human neonates. Intensive Care Med 2011;37:1158  –  65. 13.   Cattarossi L, Copetti R, Poskurica B. Radiation exposure early in life can be reduced by lung ultrasound. Chest 2011;139:730  –  1.
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