Early cardiac function and death, severe bronchopulmonary dysplasia and pulmonary hypertension in extremely preterm infants.


Journal

Pediatric research
ISSN: 1530-0447
Titre abrégé: Pediatr Res
Pays: United States
ID NLM: 0100714

Informations de publication

Date de publication:
19 Sep 2023
Historique:
received: 20 01 2023
accepted: 28 08 2023
revised: 15 07 2023
medline: 20 9 2023
pubmed: 20 9 2023
entrez: 19 9 2023
Statut: aheadofprint

Résumé

Association between early cardiac function and neonatal outcomes are scarcely reported. The aim of the current study was to describe this association with death, severe bronchopulmonary dysplasia (BPD) and BPD-related pulmonary hypertension (PH). Retrospective cohort study of infants <29 weeks born between 2015 and 2019. Infants with clinically acquired echocardiography at ≤21 days after birth were included and data were extracted by an expert masked to outcomes. A total of 176 infants were included. Echocardiogram was performed at a median of 9 days (IQR 5-13.5). Of these, 31 (18%) had death/severe BPD and 59 (33.5%) had death/BPD-related PH. Infants with death/severe BPD were of lower birth weight (745 [227] vs 852 [211] grams, p = 0.01) and more exposed to invasive ventilation, late-onset sepsis, inotropes and/or postnatal steroids. Early echocardiograms demonstrated decreased right ventricular [Tricuspid Annular Plane Systolic Excursion: 5.2 (1.4) vs 6.2 (1.5) cm, p = 0.03] and left ventricular function [Ejection fraction 53 (14) vs 58 (10) %, p = 0.03]. Infants with death/BPD-related PH had an increased Eccentricity index (1.35 [0.20] vs 1.26 [0.19], p = 0.02), and flat/bowing septum (19/54 [35%] vs 20/109 [18%], p = 0.021). In extremely premature infants, altered ventricular function and increased pulmonary pressure indices within the first 21 days after birth, were associated with the combined outcome of death/severe BPD and death/BPD-related PH. Decreased cardiac function on echocardiography performed during first three weeks of life is associated with severe bronchopulmonary dysplasia in extremely premature infants. In extreme preterm infants, echocardiographic signs of pulmonary hypertension in early life are associated with later BPD-related pulmonary hypertension close to 36 weeks post-menstrual age. Early cardiac markers should be further studied as potential intervention targets in this population. Our study is adding comprehensive analysis of echocardiographic data in infants born below 29 weeks gestational age.

Sections du résumé

BACKGROUND BACKGROUND
Association between early cardiac function and neonatal outcomes are scarcely reported. The aim of the current study was to describe this association with death, severe bronchopulmonary dysplasia (BPD) and BPD-related pulmonary hypertension (PH).
METHODS METHODS
Retrospective cohort study of infants <29 weeks born between 2015 and 2019. Infants with clinically acquired echocardiography at ≤21 days after birth were included and data were extracted by an expert masked to outcomes.
RESULTS RESULTS
A total of 176 infants were included. Echocardiogram was performed at a median of 9 days (IQR 5-13.5). Of these, 31 (18%) had death/severe BPD and 59 (33.5%) had death/BPD-related PH. Infants with death/severe BPD were of lower birth weight (745 [227] vs 852 [211] grams, p = 0.01) and more exposed to invasive ventilation, late-onset sepsis, inotropes and/or postnatal steroids. Early echocardiograms demonstrated decreased right ventricular [Tricuspid Annular Plane Systolic Excursion: 5.2 (1.4) vs 6.2 (1.5) cm, p = 0.03] and left ventricular function [Ejection fraction 53 (14) vs 58 (10) %, p = 0.03]. Infants with death/BPD-related PH had an increased Eccentricity index (1.35 [0.20] vs 1.26 [0.19], p = 0.02), and flat/bowing septum (19/54 [35%] vs 20/109 [18%], p = 0.021).
CONCLUSIONS CONCLUSIONS
In extremely premature infants, altered ventricular function and increased pulmonary pressure indices within the first 21 days after birth, were associated with the combined outcome of death/severe BPD and death/BPD-related PH.
IMPACT CONCLUSIONS
Decreased cardiac function on echocardiography performed during first three weeks of life is associated with severe bronchopulmonary dysplasia in extremely premature infants. In extreme preterm infants, echocardiographic signs of pulmonary hypertension in early life are associated with later BPD-related pulmonary hypertension close to 36 weeks post-menstrual age. Early cardiac markers should be further studied as potential intervention targets in this population. Our study is adding comprehensive analysis of echocardiographic data in infants born below 29 weeks gestational age.

Identifiants

pubmed: 37726544
doi: 10.1038/s41390-023-02817-6
pii: 10.1038/s41390-023-02817-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive licence to the International Pediatric Research Foundation, Inc.

Références

Mourani, P. M. et al. Early pulmonary vascular disease in preterm infants at risk for bronchopulmonary dysplasia. Am. J. Respir. Crit. Care Med. 191, 87–95 (2015).
pubmed: 25389562 pmcid: 4299632 doi: 10.1164/rccm.201409-1594OC
Morty, R. E. Recent advances in the pathogenesis of Bpd. Semin Perinatol. 42, 404–412 (2018).
pubmed: 30384986 doi: 10.1053/j.semperi.2018.09.001
Stoll, B. J. et al. Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993–2012. JAMA 314, 1039–1051 (2015).
pubmed: 26348753 pmcid: 4787615 doi: 10.1001/jama.2015.10244
Alvarez-Fuente, M. et al. Exploring clinical, echocardiographic and molecular biomarkers to predict bronchopulmonary dysplasia. PLoS One 14, e0213210 (2019).
pubmed: 30840669 pmcid: 6402695 doi: 10.1371/journal.pone.0213210
Bancalari, E. & Claure, N. Definitions and diagnostic criteria for bronchopulmonary dysplasia. Semin Perinatol. 30, 164–170 (2006).
pubmed: 16860155 doi: 10.1053/j.semperi.2006.05.002
Pérez-Tarazona, S. et al. Respiratory outcomes of “New” bronchopulmonary dysplasia in adolescents: A multicenter study. Pediatr. Pulmonol. 56, 1205–1214 (2021).
pubmed: 33314679 doi: 10.1002/ppul.25226
Rite, S. et al. The consensus definition of bronchopulmonary dysplasia is an adequate predictor of lung function at preschool age. Front Pediatr. 10, 830035 (2022).
pubmed: 35186811 pmcid: 8854776 doi: 10.3389/fped.2022.830035
Doyle, L. W. & Anderson, P. J. Long-term outcomes of bronchopulmonary dysplasia. Semin Fetal Neonatal Med. 14, 391–395 (2009).
pubmed: 19766550 doi: 10.1016/j.siny.2009.08.004
Dartora, D. R. et al. Association of bronchopulmonary dysplasia and right ventricular systolic function in young adults born preterm. Chest 160, 287–296 (2021).
pubmed: 33549599 doi: 10.1016/j.chest.2021.01.079
Flahault, A. et al. Left ventricle structure and function in young adults born very preterm and association with neonatal characteristics. J. Clin. Med. 10, 1760 (2021).
pubmed: 33919540 pmcid: 8072582 doi: 10.3390/jcm10081760
Lasry, A. et al. Cardiopulmonary function abnormalities in cohort of adults following bronchopulmonary dysplasia as preterm infants. Am. J. Perinatol 39, 1410–1417 (2021).
pubmed: 33454944
Arjaans, S. et al. Fate of pulmonary hypertension associated with bronchopulmonary dysplasia beyond 36 weeks postmenstrual age. Arch. Dis. Child Fetal Neonatal Ed. 106, 45–50 (2021).
pubmed: 32571832 doi: 10.1136/archdischild-2019-318531
Doyle, L. W. Postnatal corticosteroids to prevent or treat bronchopulmonary dysplasia. Neonatology 118, 244–251 (2021).
pubmed: 33975319 doi: 10.1159/000515950
Abman, S. H. Pulmonary hypertension: The hidden danger for newborns. Neonatology 118, 211–217 (2021).
pubmed: 33951650 doi: 10.1159/000516107
Mourani, P. M. et al. Early pulmonary vascular disease in preterm infants is associated with late respiratory outcomes in childhood. Am. J. Respir. Crit. Care Med. 199, 1020–1027 (2019).
pubmed: 30303395 pmcid: 6467308 doi: 10.1164/rccm.201803-0428OC
Mirza, H. et al. Natural history of postnatal cardiopulmonary adaptation in infants born extremely preterm and risk for death or bronchopulmonary dysplasia. J. Pediatr. 198, 187–193.e181 (2018).
pubmed: 29625730 doi: 10.1016/j.jpeds.2018.02.034
Kim, H. H. et al. Early pulmonary hypertension is a risk factor for bronchopulmonary dysplasia-associated late pulmonary hypertension in extremely preterm infants. Sci. Rep. 11, 11206 (2021).
pubmed: 34045608 pmcid: 8160152 doi: 10.1038/s41598-021-90769-4
Kim, Y. J., Shin, S. H., Park, H. W., Kim, E. K. & Kim, H. S. Risk factors of early pulmonary hypertension and its clinical outcomes in preterm infants: A systematic review and meta-analysis. Sci. Rep. 12, 14186 (2022).
pubmed: 35986155 pmcid: 9391329 doi: 10.1038/s41598-022-18345-y
Sheth, S., Goto, L., Bhandari, V., Abraham, B. & Mowes, A. Factors associated with development of early and late pulmonary hypertension in preterm infants with bronchopulmonary dysplasia. J. Perinatol. 40, 138–148 (2020).
pubmed: 31723236 doi: 10.1038/s41372-019-0549-9
Abman, S. H. et al. Pediatric pulmonary hypertension: Guidelines from the American Heart Association and American Thoracic Society. Circulation 132, 2037–2099 (2015).
pubmed: 26534956 doi: 10.1161/CIR.0000000000000329
Lakshminrusimha, S. & Steinhorn, R. H. Pulmonary vascular biology during neonatal transition. Clin. Perinatol. 26, 601–619 (1999).
pubmed: 10494467 doi: 10.1016/S0095-5108(18)30039-3
Jobe, A. H. & Bancalari, E. Bronchopulmonary dysplasia. Am. J. Respir. Crit. Care Med 163, 1723–1729 (2001).
pubmed: 11401896 doi: 10.1164/ajrccm.163.7.2011060
Higgins, R. D. et al. Bronchopulmonary dysplasia: Executive summary of a workshop. J. Pediatr. 197, 300–308 (2018).
pubmed: 29551318 pmcid: 5970962 doi: 10.1016/j.jpeds.2018.01.043
Richardson, D. K., Corcoran, J. D., Escobar, G. J. & Lee, S. K. Snap-Ii and Snappe-Ii: Simplified newborn illness severity and mortality risk scores. J. Pediatr. 138, 92–100 (2001).
pubmed: 11148519 doi: 10.1067/mpd.2001.109608
Chou, J. H., Roumiantsev, S. & Singh, R. Peditools electronic growth chart calculators: Applications in clinical care, research, and quality improvement. J. Med. Internet Res. 22, e16204 (2020).
pubmed: 32012066 pmcid: 7058170 doi: 10.2196/16204
Lai, W. W. 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. 19, 1413–1430 (2006).
pubmed: 17138024 doi: 10.1016/j.echo.2006.09.001
Altit, G., Bhombal, S., Feinstein, J., Hopper, R. K. & Tacy, T. A. Diminished right ventricular function at diagnosis of pulmonary hypertension is associated with mortality in bronchopulmonary dysplasia. Pulm. Circ. 9, 2045894019878598 (2019).
pubmed: 31662848 pmcid: 6792284 doi: 10.1177/2045894019878598
Mertens, L. L., Ganame, J. & Eyskens, B. Echocardiographic evaluation of systolic function. In Echocardiography in pediatric and congenital heart disease: from fetus to adult (eds Lai, W. W., Mertens, L. L., Cohen, M. S. & Geva T.) 76-94 (John Wiley & Sons, Ltd, 2009).
Sehgal, A., Malikiwi, A., Paul, E., Tan, K. & Menahem, S. Right ventricular function in infants with bronchopulmonary dysplasia: association with respiratory sequelae. Neonatology 109, 289–296 (2016).
pubmed: 26886137 doi: 10.1159/000442967
Altit, G. et al. Pathophysiology, screening and diagnosis of pulmonary hypertension in infants with bronchopulmonary dysplasia—a review of the literature. Paediatr. Respir. Rev. 23, 16–26 (2017).
pubmed: 27986502
Koestenberger, M., Friedberg, M. K., Nestaas, E., Michel-Behnke, I. & Hansmann, G. Transthoracic echocardiography in the evaluation of pediatric pulmonary hypertension and ventricular dysfunction. Pulm. Circ. 6, 15–29 (2016).
pubmed: 27162612 pmcid: 4860554 doi: 10.1086/685051
Jone, P. N., Hinzman, J., Wagner, B. D., Ivy, D. D. & Younoszai, A. Right ventricular to left ventricular diameter ratio at end-systole in evaluating outcomes in children with pulmonary hypertension. J. Am. Soc. Echocardiogr. 27, 172–178 (2014).
pubmed: 24325962 doi: 10.1016/j.echo.2013.10.014
Jone, P. N. et al. Right atrial deformation in predicting outcomes in pediatric pulmonary hypertension. Circ. Cardiovasc Imaging 10, e006250 (2017).
pubmed: 29233835 pmcid: 5730878 doi: 10.1161/CIRCIMAGING.117.006250
Jone, P. N. & Ivy, D. D. Echocardiography in pediatric pulmonary hypertension. Front Pediatr. 2, 124 (2014).
pubmed: 25429362 pmcid: 4228850 doi: 10.3389/fped.2014.00124
Abraham, S. & Weismann, C. G. Left ventricular end-systolic eccentricity index for assessment of pulmonary hypertension in infants. Echocardiography 33, 910–915 (2016).
pubmed: 26773570 doi: 10.1111/echo.13171
Haque, U. et al. Right ventricular performance using myocardial deformation imaging in infants with bronchopulmonary dysplasia. J. Perinatol. 37, 81–87 (2017).
pubmed: 27711043 doi: 10.1038/jp.2016.173
Murase, M., Morisawa, T. & Ishida, A. Serial assessment of left-ventricular function using tissue doppler imaging in premature infants within 7 days of life. Pediatr. Cardiol. 34, 1491–1498 (2013).
pubmed: 23475256 doi: 10.1007/s00246-013-0675-7
James, A. T. et al. Longitudinal assessment of left and right myocardial function in preterm infants using strain and strain rate imaging. Neonatology 109, 69–75 (2016).
pubmed: 26583602 doi: 10.1159/000440940
Czernik, C. et al. Development of left ventricular longitudinal speckle tracking echocardiography in very low birth weight infants with and without bronchopulmonary dysplasia during the neonatal period. PLoS One 9, e106504 (2014).
pubmed: 25184634 pmcid: 4153617 doi: 10.1371/journal.pone.0106504
Helfer, S., Schmitz, L., Bührer, C. & Czernik, C. Tissue doppler-derived strain and strain rate during the first 28 days of life in very low birth weight infants. Echocardiography 31, 765–772 (2014).
pubmed: 24372717 doi: 10.1111/echo.12463
Bokiniec, R., Własienko, P., Borszewska-Kornacka, M. & Szymkiewicz-Dangel, J. Evaluation of left ventricular function in preterm infants with bronchopulmonary dysplasia using various echocardiographic techniques. Echocardiography 34, 567–576 (2017).
pubmed: 28370301 doi: 10.1111/echo.13488
Torres, E. et al. Left ventricle phenotyping utilizing tissue doppler imaging in premature infants with varying severity of bronchopulmonary dysplasia. J. Clin. Med 10, 2211 (2021).
pubmed: 34065264 pmcid: 8160781 doi: 10.3390/jcm10102211
Seth, S. A., Soraisham, A. S. & Harabor, A. Risk factors and outcomes of early pulmonary hypertension in preterm infants. J. Matern Fetal Neonatal Med 31, 3147–3152 (2018).
pubmed: 28783986 doi: 10.1080/14767058.2017.1365129
Bhat, R., Salas, A. A., Foster, C., Carlo, W. A. & Ambalavanan, N. Prospective analysis of pulmonary hypertension in extremely low birth weight infants. Pediatrics 129, e682–e689 (2012).
pubmed: 22311993 pmcid: 3289526 doi: 10.1542/peds.2011-1827
Mehler, K. et al. An echocardiographic screening program helps to identify pulmonary hypertension in extremely low birthweight infants with and without bronchopulmonary dysplasia: A single-center experience. Neonatology 113, 81–88 (2018).
pubmed: 29131022 doi: 10.1159/000480694
Altit, G. et al. Outcomes of extremely premature infants comparing patent ductus arteriosus management approaches. J. Pediatr. 235, 49–57 (2021).
pubmed: 33864797 doi: 10.1016/j.jpeds.2021.04.014
de Carvalho Nunes, G. et al. Natural evolution of the patent ductus arteriosus in the extremely premature newborn and respiratory outcomes. J. Perinatol. 42, 642–648 (2022).
pubmed: 34815521 doi: 10.1038/s41372-021-01277-2
Hundscheid, T. et al. Expectant management or early ibuprofen for patent ductus arteriosus. N. Engl. J. Med. 388, 980–990 (2023).
pubmed: 36477458 doi: 10.1056/NEJMoa2207418
Benitz, W. E. Treatment of persistent patent ductus arteriosus in preterm infants: Time to accept the null hypothesis? J. Perinatol 30, 241–252 (2010).
pubmed: 20182439 doi: 10.1038/jp.2010.3
Benitz, W. E. Patent ductus arteriosus: To treat or not to treat? Arch. Dis. Child. Fetal Neonatal Ed. 97, F80–F82 (2012).
pubmed: 22174019 doi: 10.1136/archdischild-2011-300381
Benitz, W. E. & Committee on Fetus and Newborn, American Academy of Pediatrics. Patent ductus arteriosus in preterm infants. Pediatrics 137 (2016).
El-Khuffash, A. et al. A patent ductus arteriosus severity score predicts chronic lung disease or death before discharge. J. Pediatr. 167, 1354–1361.e1352 (2015).
pubmed: 26474706 doi: 10.1016/j.jpeds.2015.09.028
El-Khuffash, A., Weisz, D. E. & McNamara, P. J. Reflections of the changes in patent ductus arteriosus management during the last 10 years. Arch. Dis. Child Fetal Neonatal Ed. 101, F474–F478 (2016).
pubmed: 27118761 doi: 10.1136/archdischild-2014-306214

Auteurs

Shiran S Moore (SS)

Neonatology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.
Neonatology-Dana Dwek Children's Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.

Gabriela De Carvalho Nunes (G)

Neonatology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.

Adrian Dancea (A)

Pediatric Cardiology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.

Punnanee Wutthigate (P)

Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand.

Jessica Simoneau (J)

Pediatric Cardiology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.

Marc Beltempo (M)

Neonatology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.

Guilherme Sant'Anna (G)

Neonatology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada.

Gabriel Altit (G)

Neonatology-McGill University Health Centre-Montreal Children's Hospital; Department of Pediatrics-McGill University, Montreal, QC, Canada. gabriel.altit@mcgill.ca.

Classifications MeSH