Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-23T08:11:14.428Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered biventricular function in neonatal hypoxic-ischaemic encephalopathy: a case–control echocardiographic study

Published online by Cambridge University Press:  06 September 2022

Gabriel Altit Open the ORCID record for Gabriel Altit [Opens in a new window] ,
Sonia Lomeli Bonifacio ,
Carolina V. Guimaraes ,
Ganesh Sivakumar ,
Beth Yan ,
Valerie Chock ,
Krisa Van Meurs  and
Shazia Bhombal
Gabriel Altit*
Affiliation:
Department of Pediatrics, Division of Neonatology, Montreal Children’s Hospital, McGill University Health Center, Montreal, Quebec, Canada
Sonia Lomeli Bonifacio
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University School of Medicine and Lucile Packard Children’s Hospital Stanford, Palo Alto, CA, USA
Carolina V. Guimaraes
Affiliation:
Clinical Professor of Radiology Division Chief of Pediatric Radiology Pediatric Neuroradiology University of North Carolina, School of Medicine, Department of Radiology, Chapel Hill, North Carolina 2006 Old Clinic Building, CB# 7510, Chapel Hill, NC, 27599-7510, USA
Ganesh Sivakumar
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University – Lucile Packard Children’s Hospital, Palo Alto, CA, USA
Beth Yan
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University School of Medicine and Lucile Packard Children’s Hospital Stanford, Palo Alto, CA, USA
Valerie Chock
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University School of Medicine and Lucile Packard Children’s Hospital Stanford, Palo Alto, CA, USA
Krisa Van Meurs
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University School of Medicine and Lucile Packard Children’s Hospital Stanford, Palo Alto, CA, USA
Shazia Bhombal
Affiliation:
Division of Neonatal and Developmental Medicine, Stanford University School of Medicine and Lucile Packard Children’s Hospital Stanford, Palo Alto, CA, USA
*
Author for correspondence: Dr. Gabriel Altit, MDCM, Department of Pediatrics, Division of Neonatology, McGill University, Montreal Children’s Hospital, McGill University Health Centre, 1001 Décarie, B05.2513, Division of Neonatology, Montreal, Quebec, Canada. Tel: 1-514-412-4452. E-mail: Gabriel.altit@mcgill.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Background:

In newborns with hypoxic-ischaemic encephalopathy, more profound altered right and left ventricular function has been associated with mortality or brain injury. Mechanisms underlying cardiac dysfunction in this population are thought to be related to the persistence of increased pulmonary vascular resistance and myocardial ischaemia. We sought to compare cardiac function in newborns with hypoxic-ischaemic encephalopathy to controls using echocardiography.

Methods:

We did a retrospective case–control study with moderate or severe hypoxic-ischaemic encephalopathy between 2008 and 2017. Conventional and speckle-tracking echocardiography measures were extracted to quantify right and left ventricular systolic and diastolic function. Fifty-five newborns with hypoxic-ischaemic encephalopathy were compared to 28 controls.

Results:

Hypoxic-ischaemic encephalopathy newborns had higher estimated systolic pulmonary pressure (62.5 ± 15.0 versus 43.8 ± 17.3 mmHg, p < 0.0001) and higher systolic pulmonary artery pressure/systolic blood pressure ratio [101 ± 16 (iso-systemic) versus 71 ± 27 (2/3 systemic range) %, p < 0.0001]. Tricuspid annular plane systolic excursion was decreased (7.5 ± 2.2 versus 9.0 ± 1.4 mm, p = 0.002), E/e’ increased (7.9 ± 3.3 versus 5.8 ± 2.0, p = 0.01), and right ventricle-myocardial performance index increased (68.1 ± 21.5 versus 47.8 ± 9.5, p = 0.0001) in hypoxic-ischaemic encephalopathy. Conventional markers of left ventricle systolic function were similar, but e’ velocity (0.059 ± 0.019 versus 0.070 ± 0.01, p = 0.03) and left ventricle-myocardial performance index were statistically different (77.9 ± 26.2 versus 57.9 ± 11.2, p = 0.001). The hypoxic-ischaemic encephalopathy group had significantly altered right and left ventricular deformation parameters by speckle-tracking echocardiography. Those with decreased right ventricle-peak longitudinal strain were more likely to have depressed left ventricle-peak longitudinal strain.

Conclusion:

Newborns with hypoxic-ischaemic encephalopathy have signs of increased pulmonary pressures and altered biventricular systolic and diastolic function.

Keywords

Brain injurycardiac dysfunctionhypoxic-ischaemic encephalopathyspeckle-tracking echocardiographytherapeutic hypothermia
Type
Original Article
Information
Cardiology in the Young , Volume 33 , Issue 9 , September 2023 , pp. 1587 - 1596
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Jacobs, SE, Berg, M, Hunt, R, Tarnow-Mordi, WO, Inder, TE, Davis, PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev 2013; 2013: Cd003311.Google ScholarPubMed
Shankaran, S, Laptook, AR, Ehrenkranz, RA et al. Whole-body hypothermia for neonates with hypoxic–ischemic encephalopathy. N Engl J Med 2005; 353: 1574–1584.10.1056/NEJMcps050929CrossRefGoogle ScholarPubMed
Lakshminrusimha, S, Shankaran, S, Laptook, A et al. Pulmonary hypertension associated with hypoxic-ischemic encephalopathy-antecedent characteristics and comorbidities. J Pediatr 2018; 196: 45–51.e43.10.1016/j.jpeds.2017.12.055CrossRefGoogle ScholarPubMed
Giesinger, RE, Bailey, LJ, Deshpande, P and Mcnamara, PJ. Hypoxic-ischemic encephalopathy and therapeutic hypothermia: The hemodynamic perspective. 2017; 180: 22–30.e2.10.1016/j.jpeds.2016.09.009CrossRefGoogle Scholar
Giesinger, RE, El Shahed, AI, Castaldo, MP et al. Impaired right ventricular performance is associated with adverse outcome after hypoxic ischemic encephalopathy. Am J Respir Crit Care Med 2019; 200: 1294–1305.10.1164/rccm.201903-0583OCCrossRefGoogle ScholarPubMed
Altit, G, Bonifacio, SL, Guimaraes, CV et al. Cardiac dysfunction in neonatal HIE is associated with increased mortality and brain injury by MRI. Am J Perinatol 2021. [Epub ahead of print].Google ScholarPubMed
Breatnach, CR, Forman, E, Foran, A et al. Left ventricular rotational mechanics in infants with hypoxic ischemic encephalopathy and preterm infants at 36 weeks postmenstrual age: A comparison with healthy term controls. Echocardiography (Mount Kisco, NY) 2017; 34: 232–239.10.1111/echo.13421CrossRefGoogle ScholarPubMed
Altit, G, Bhombal, S, Chock, VY and Tacy, TA. Immediate postnatal ventricular performance is associated with mortality in hypoplastic left heart syndrome. Pediatr Cardiol 2019; 40: 168–176.10.1007/s00246-018-1974-9CrossRefGoogle ScholarPubMed
Altit, G, Bhombal, S, Van Meurs, K and Tacy, TA. Diminished cardiac performance and left ventricular dimensions in neonates with congenital diaphragmatic hernia. Pediatr Cardiol 2018; 39: 993–1000.10.1007/s00246-018-1850-7CrossRefGoogle ScholarPubMed
Sarnat, HB and Sarnat, MS. Neonatal encephalopathy following fetal distress: a clinical and electroencephalographic study. Arch Neurol 1976; 33: 696–705.10.1001/archneur.1976.00500100030012CrossRefGoogle ScholarPubMed
Altit, G, Bhombal, S, Feinstein, J, Hopper, RK and Tacy, TA. Diminished right ventricular function at diagnosis of pulmonary hypertension is associated with mortality in bronchopulmonary dysplasia. Pulm Circ 2019; 9: 2045894019878598.10.1177/2045894019878598CrossRefGoogle ScholarPubMed
Altit, G, Bhombal, S, Van Meurs, K, Tacy, TA. Ventricular performance is associated with need for extracorporeal membrane oxygenation in newborns with congenital diaphragmatic hernia. J Pediatr 2017; 191: 28–34.e21.10.1016/j.jpeds.2017.08.060CrossRefGoogle ScholarPubMed
Lai, WW, Geva, T, Shirali, GS et al. Guidelines and standards for performance of a pediatric echocardiogram: a report from the Task Force of the Pediatric Council of the American Society of Echocardiography. J Am Soc Echocardiogr 2006; 19: 1413–1430.10.1016/j.echo.2006.09.001CrossRefGoogle ScholarPubMed
Erickson, CT, Levy, PT, Craft, M, Li, L, Danford, DA, Kutty, S. Maturational patterns in right ventricular strain mechanics from the fetus to the young infant. Early Hum Dev 2019; 129: 23–32.10.1016/j.earlhumdev.2018.12.015CrossRefGoogle Scholar
Jain, A, Mohamed, A, El-Khuffash, A et al. A comprehensive echocardiographic protocol for assessing neonatal right ventricular dimensions and function in the transitional period: normative data and z scores. J Am Soc Echocardiogr 2014; 27: 1293–1304.10.1016/j.echo.2014.08.018CrossRefGoogle ScholarPubMed
Khan, U, Omdal, TR, Matre, K, Greve, G. What is left ventricular strain in healthy neonates? A systematic review and meta-analysis. Pediatr Cardiol 2020; 41: 1–11.10.1007/s00246-019-02219-8CrossRefGoogle ScholarPubMed
Levy, PT, Machefsky, A, Sanchez, AA et al. Reference ranges of left ventricular strain measures by two-dimensional speckle-tracking echocardiography in children: A systematic review and meta-analysis. J Am Soc Echocardiogr 2016; 29: 209–225 e206.10.1016/j.echo.2015.11.016CrossRefGoogle ScholarPubMed
Barrington, KJ, Finer, N, Pennaforte, T and Altit, G. Nitric oxide for respiratory failure in infants born at or near term. Cochrane Database Syst Rev 2017; 1: Cd000399.Google ScholarPubMed
Shah, PS. Hypothermia: a systematic review and meta-analysis of clinical trials. Semin Fetal Neonatal Med 2010; 15: 238–246.10.1016/j.siny.2010.02.003CrossRefGoogle ScholarPubMed
Yoon, JH, Lee, EJ, Yum, SK et al. Impacts of therapeutic hypothermia on cardiovascular hemodynamics in newborns with hypoxic-ischemic encephalopathy: a case control study using echocardiography. J Matern Fetal Neonatal Med 2018; 31: 2175–2182.10.1080/14767058.2017.1338256CrossRefGoogle ScholarPubMed
Hochwald, O, Jabr, M, Osiovich, H, Miller, SP, McNamara, PJ, Lavoie, PM. Preferential cephalic redistribution of left ventricular cardiac output during therapeutic hypothermia for perinatal hypoxic-ischemic encephalopathy. J Pediatr 2014; 164: 999–1004.e1001.10.1016/j.jpeds.2014.01.028CrossRefGoogle ScholarPubMed
Bhasin, H and Kohli, C. Myocardial dysfunction as a predictor of the severity and mortality of hypoxic ischaemic encephalopathy in severe perinatal asphyxia: a case-control study. Paediatr Int Child Health 2019; 39: 259–264.10.1080/20469047.2019.1581462CrossRefGoogle ScholarPubMed
Sehgal, A, Wong, F, Mehta, S. Reduced cardiac output and its correlation with coronary blood flow and troponin in asphyxiated infants treated with therapeutic hypothermia. Eur J Pediatr 2012; 171: 1511–1517.10.1007/s00431-012-1764-yCrossRefGoogle ScholarPubMed
Aggarwal, S and Natarajan, G. Biventricular function on early echocardiograms in neonatal hypoxic-ischaemic encephalopathy. Acta Paediatr 2017; 106: 1085–1090.10.1111/apa.13866CrossRefGoogle ScholarPubMed
Sobeih, AA, El-Baz, MS, El-Shemy, DM, Abu El-Hamed, WA. Tissue Doppler imaging versus conventional echocardiography in assessment of cardiac diastolic function in full term neonates with perinatal asphyxia. J Matern Fetal Neonatal Med 2020: 1–6.Google ScholarPubMed
Chaiyakulsil, C, Chantra, M, Katanyuwong, P, Khositseth, A, Anantasit, N. Comparison of three non-invasive hemodynamic monitoring methods in critically ill children. PLoS One 2018; 13: e0199203.10.1371/journal.pone.0199203CrossRefGoogle ScholarPubMed
Villavicencio, C, Leache, J, Marin, J et al. Basic critical care echocardiography training of intensivists allows reproducible and reliable measurements of cardiac output. Ultrasound J 2019; 11: 5.10.1186/s13089-019-0120-0CrossRefGoogle ScholarPubMed
Pees, C, Glagau, E, Hauser, J, Michel-Behnke, I. Reference values of aortic flow velocity integral in 1193 healthy infants, children, and adolescents to quickly estimate cardiac stroke volume. Pediatr Cardiol 2013; 34: 1194–1200.10.1007/s00246-012-0628-6CrossRefGoogle ScholarPubMed
Mukherjee, M, Chung, SE, Ton, VK et al. Unique abnormalities in right ventricular longitudinal strain in systemic sclerosis patients. Circ Cardiovasc Imaging 2016; 9.10.1161/CIRCIMAGING.115.003792CrossRefGoogle ScholarPubMed
Mercer-Rosa, L, Parnell, A, Forfia, PR, Yang, W, Goldmuntz, E, Kawut, SM. Tricuspid annular plane systolic excursion in the assessment of right ventricular function in children and adolescents after repair of tetralogy of Fallot. J Am Soc Echocardiogr 2013; 26: 1322–1329.10.1016/j.echo.2013.06.022CrossRefGoogle ScholarPubMed
Costa, SP, Beaver, TA, Rollor, JL, Vanichakarn, P, Magnus, PC and Palac, RT. Quantification of the variability associated with repeat measurements of left ventricular two-dimensional global longitudinal strain in a real-world setting. J Am Soc Echocardiogr 2014; 27: 50–54.10.1016/j.echo.2013.08.021CrossRefGoogle ScholarPubMed
Risum, N, Ali, S, Olsen, NT et al. Variability of global left ventricular deformation analysis using vendor dependent and independent two-dimensional speckle-tracking software in adults. J Am Soc Echocardiogr 2012; 25: 1195–1203.10.1016/j.echo.2012.08.007CrossRefGoogle ScholarPubMed
Liu, MY, Tacy, T, Chin, C, Obayashi, DY and Punn, R. Assessment of speckle-tracking echocardiography-derived global deformation parameters during supine exercise in children. Pediatr Cardiol 2016; 37: 519–527.10.1007/s00246-015-1309-zCrossRefGoogle ScholarPubMed
Supplementary material: PDF

Altit et al. supplementary material

Altit et al. supplementary material

Download Altit et al. supplementary material(PDF)
PDF 383.5 KB