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The biventricular contribution to chronic pulmonary hypertension of the extremely premature infant

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Abstract

Objective

Evaluate factors associated with significant pulmonary hypertension [PH] (≥2/3 systemic) and its impact on ventricular function at 36 weeks postmenstrual age (PMA).

Study design

Retrospective cohort of infants born at <29 weeks who survived to their echocardiography screening for PH at 36 weeks PMA. Masked experts extracted conventional and speckle-tracking echocardiography [STE] data.

Results

Of 387 infants, 222 were included and 24 (11%) categorized as significant PH. Significant PH was associated with a decrease in tricuspid annular plane systolic excursion (0.79 vs 0.87 cm, p = 0.03), right peak longitudinal strain [pLS] by STE (−19.6 vs −23.1%, p = 0.003) and left pLS (−25.0 vs −22.7%, p = 0.02). The association between biventricular altered function by STE and significant PH persisted after adjustment for potential confounders – LV-pLS (p = 0.007) and RV-pLS (p = 0.01).

Conclusion

Our findings are suggestive that premature newborns with significant PH at 36 weeks PMA have a biventricular cardiac involvement to their pathophysiology.

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Fig. 1: Flowchart for patient inclusion.

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References

  1. Morty RE. Recent advances in the pathogenesis of BPD. Semin Perinatol. 2018;42:404–12.

    Article  Google Scholar 

  2. Beltempo M, Shah P, Yoon EW, Chan P, Balachandran N. Canadian Neonatal Network Annual Report 2019. Canadian Neonatal Network; 2019.

  3. Stoll BJ, Hansen NI, Bell EF, Walsh MC, Carlo WA, Shankaran S, et al. Trends in care practices, morbidity, and mortality of extremely preterm neonates, 1993–2012. Jama. 2015;314:1039–51.

    Article  CAS  Google Scholar 

  4. Bhattacharya S, Sen S, Levy PT, Rios DR. Comprehensive evaluation of right heart performance and pulmonary hemodynamics in neonatal pulmonary hypertension. Curr Treat Options Cardiovasc Med. 2019;21:1–15.

    Article  Google Scholar 

  5. Altit G, Bhombal S, Feinstein J, Hopper RK, Tacy TA. Diminished right ventricular function at diagnosis of pulmonary hypertension is associated with mortality in bronchopulmonary dysplasia. Pulm Circulation. 2019;9:1–11.

    Article  Google Scholar 

  6. Mourani PM, Sontag MK, Younoszai A, Miller JI, Kinsella JP, Baker CD, et al. Early pulmonary vascular disease in preterm infants at risk for bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2015;191:87–95.

    Article  Google Scholar 

  7. Berkelhamer SK, Mestan KK, Steinhorn RH. Pulmonary hypertension in bronchopulmonary dysplasia. Semin Perinatol. 2013;37:124–31.

    Article  Google Scholar 

  8. Altit G, Bhombal S, Hopper RK, Tacy TA, Feinstein J. Death or resolution: the “natural history” of pulmonary hypertension in bronchopulmonary dysplasia. J Perinatol Off J Calif Perinat Assoc. 2019;39:415–25.

    Google Scholar 

  9. Altit G, Bhombal S, Van Meurs K, Tacy TA. Diminished cardiac performance and left ventricular dimensions in neonates with congenital diaphragmatic hernia. Pediatr Cardiol. 2018;39:993–1000.

    Article  Google Scholar 

  10. Altit G, Dancea A, Renaud C, Perreault T, Lands LC, Sant’Anna G. Pathophysiology, screening and diagnosis of pulmonary hypertension in infants with bronchopulmonary dysplasia - A review of the literature. Paediatr Respir Rev. 2017;23:16–26.

    Google Scholar 

  11. Abman SH, Hansmann G, Archer SL, Ivy DD, Adatia I, Chung WK, et al. Pediatric pulmonary hypertension: guidelines from the American heart association and American thoracic society. Circulation. 2015;132:2037–99.

    Article  Google Scholar 

  12. Hansmann G, Koestenberger M, Alastalo TP, Apitz C, Austin ED, Bonnet D, et al. 2019 updated consensus statement on the diagnosis and treatment of pediatric pulmonary hypertension: The European Pediatric Pulmonary Vascular Disease Network (EPPVDN), endorsed by AEPC, ESPR and ISHLT. J Heart Lung Transplant. 2019;38:879–901.

    Article  Google Scholar 

  13. Lau EMT, Manes A, Celermajer DS, Galie N. Early detection of pulmonary vascular disease in pulmonary arterial hypertension: time to move forward. Eur Heart J. 2011;32:2489–98.

    Article  Google Scholar 

  14. Parasuraman S, Walker S, Loudon BL, Gollop ND, Wilson AM, Lowery C, et al. Assessment of pulmonary artery pressure by echocardiography—A comprehensive review. IJC Heart Vasculature. 2016;12:45–51.

    Article  Google Scholar 

  15. Carlton EF, Sontag MK, Younoszai A, DiMaria MV, Miller JI, Poindexter BB, et al. Reliability of echocardiographic indicators of pulmonary vascular disease in preterm infants at risk for bronchopulmonary dysplasia. J Pediatrics. 2017;186:29–33.

    Article  Google Scholar 

  16. Krishnan U, Feinstein JA, Adatia I, Austin ED, Mullen MP, Hopper RK, et al. Evaluation and management of pulmonary hypertension in children with bronchopulmonary dysplasia. J Pediatr. 2017;188:24–34.e1.

    Article  Google Scholar 

  17. El-Khuffash A, Schubert U, Levy PT, Nestaas E, De, Boode WP. Deformation imaging and rotational mechanics in neonates: a guide to image acquisition, measurement, interpretation, and reference values. Pediatr Res. 2018;84:30–45.

    Article  Google Scholar 

  18. Lai WW, Geva T, Shirali GS, Frommelt PC, Humes RA, Brook MM, 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;19:1413–30.

    Article  Google Scholar 

  19. Abraham S, Weismann CG. Left ventricular end-systolic eccentricity index for assessment of pulmonary hypertension in infants. Echocardiography 2016;33:910–5.

    Article  Google Scholar 

  20. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med. 2001;163:1723–9.

    Article  CAS  Google Scholar 

  21. Mirza H, Ziegler J, Ford S, Padbury J, Tucker R, Laptook A. Pulmonary hypertension in preterm infants: prevalence and association with bronchopulmonary dysplasia. J Pediatr. 2014;165:909–14.e1.

    Article  Google Scholar 

  22. Burns AT, La Gerche A, D’Hooge J, Macisaac AI, Prior DL. Left ventricular strain and strain rate: characterization of the effect of load in human subjects. Eur J Echocardiogr. 2010;11:283–9.

    Article  Google Scholar 

  23. Kumar KR, Clark DA, Kim EM, Perry JD, Wright K, Thomas SA, et al. Association of atrial septal defects and bronchopulmonary dysplasia in premature infants. J Pediatr. 2018;202:56–62.e2.

    Article  Google Scholar 

  24. Choi EK, Jung YH, Kim HS, Shin SH, Choi CW, Kim EK, et al. The impact of atrial left-to-right shunt on pulmonary hypertension in preterm infants with moderate or severe bronchopulmonary dysplasia. Pediatr Neonatol. 2015;56:317–23.

    Article  Google Scholar 

  25. Mahgoub L, Kaddoura T, Kameny AR, Lopez Ortego P, Vanderlaan RD, Kakadekar A, et al. Pulmonary vein stenosis of ex-premature infants with pulmonary hypertension and bronchopulmonary dysplasia, epidemiology, and survival from a multicenter cohort. Pediatr Pulmonol. 2017;52:1063–70.

    Article  Google Scholar 

  26. Koestenberger M, Friedberg MK, Nestaas E, Michel-Behnke I, Hansmann G. Transthoracic echocardiography in the evaluation of pediatric pulmonary hypertension and ventricular dysfunction. Pulm Circ. 2016;6:15–29.

    Article  CAS  Google Scholar 

  27. Amà R, Leather HA, Segers P, Vandermeersch E, Wouters PF. Acute pulmonary hypertension causes depression of left ventricular contractility and relaxation. Eur J Anaesthesiol. 2006;23:824–31.

    Article  Google Scholar 

  28. Mechelinck M, Hein M, Bellen S, Rossaint R, Roehl AB. Adaptation to acute pulmonary hypertension in pigs. Physiol Rep. 2018;6:e13605.

    Article  Google Scholar 

  29. Telles F, McNamara N, Nanayakkara S, Doyle MP, Williams M, Yaeger L, et al. Changes in the preterm heart from birth to young adulthood: a meta-analysis. Pediatrics. 2020;146:e20200146.

    Article  Google Scholar 

  30. Lewandowski AJ, Augustine D, Lamata P, Davis EF, Lazdam M, Francis J, et al. Preterm heart in adult life: cardiovascular magnetic resonance reveals distinct differences in left ventricular mass, geometry, and function. Circulation. 2013;127:197–206.

    Article  Google Scholar 

  31. Rosenkranz S, Gibbs JSR, Wachter R, De Marco T, Vonk-Noordegraaf A, Vachiéry J-L. Left ventricular heart failure and pulmonary hypertension. Eur Heart J. 2016;37:942–54.

    Article  Google Scholar 

  32. Khemani E, McElhinney DB, Rhein L, Andrade O, Lacro RV, Thomas KC, et al. Pulmonary artery hypertension in formerly premature infants with bronchopulmonary dysplasia: clinical features and outcomes in the surfactant era. Pediatrics. 2007;120:1260–9.

    Article  Google Scholar 

  33. Slaughter JL, Pakrashi T, Jones DE, South AP, Shah TA. Echocardiographic detection of pulmonary hypertension in extremely low birth weight infants with bronchopulmonary dysplasia requiring prolonged positive pressure ventilation. J Perinatol Off J Calif Perinat Assoc. 2011;31:635–40.

    CAS  Google Scholar 

  34. An HS, Bae EJ, Kim GB, Kwon BS, Beak JS, Kim EK, et al. Pulmonary hypertension in preterm infants with bronchopulmonary dysplasia. Korean Circ J. 2010;40:131–6.

    Article  Google Scholar 

  35. Kwon HW, Kim HS, An HS, Kwon BS, Kim GB, Shin SH. et al. Long-term outcomes of pulmonary hypertension in preterm infants with bronchopulmonary dysplasia. Neonatology. 2016;110:181–9.

    Article  Google Scholar 

  36. Altit G, Saeed S, Beltempo M, Claveau M, Lapointe A, Basso O. Outcomes of extremely premature infants comparing patent ductus arteriosus management approaches. J Pediatr. 2021;235:49–57.e2.

    Article  Google Scholar 

  37. Gournay V. The ductus arteriosus: physiology, regulation, and functional and congenital anomalies. Arch Cardiovasc Dis. 2011;104:578–85.

    Article  Google Scholar 

  38. Philip R, Lamba V, Talati A, Sathanandam S. Pulmonary hypertension with prolonged patency of the ductus arteriosus in preterm infants. Children (Basel). 2020;7:139.

    Google Scholar 

  39. Flahault A, Altit G, Sonea A, Gervais AS, Mian MOR, Wu R, et al. Left ventricle structure and function in young adults born very preterm and association with neonatal characteristics. J Clin Med. 2021;10:1760.

    Article  Google Scholar 

  40. Gandhi C, Uhal BD. Roles of the angiotensin system in neonatal lung injury and disease. JSM Atheroscler. 2016;1:1014.

    Google Scholar 

  41. Sehgal A, Krishnamurthy MB, Clark M, Menahem S. ACE inhibition for severe bronchopulmonary dysplasia - an approach based on physiology. Physiol Rep. 2018;6:e13821.

    Article  Google Scholar 

  42. Altit G, Bhombal S, Chock VY, Tacy TA. Immediate postnatal ventricular performance is associated with mortality in hypoplastic left heart syndrome. Pediatr Cardiol. 2019;40:168–76.

    Article  Google Scholar 

  43. Dartora DR, Flahault A, Luu TM, Cloutier A, Simoneau J, White M, et al. Association of bronchopulmonary dysplasia and right ventricular systolic function in young adults born preterm. Chest. 2021;160:287–96.

    Article  Google Scholar 

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Acknowledgements

We acknowledge the support of the Canadian Neonatal Network who provided some of data for our center.

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Authors

Contributions

GCN conceptualized and designed the study, collected the data, analyzed the data, drafted the manuscript, and adjusted the manuscript according to the comments of co-authors; PW collected the data and revised the manuscript; JS collected the data and revised the manuscript; CR and AD reviewed and revised the manuscript; MB conceptualized and designed the study, collected the data, critically appraised the analysis of the data and reviewed and revised the manuscript; GA conceptualized and designed the study, supervised data collection, critically appraised the analysis of the data, wrote and critically reviewed the manuscript for important intellectual content.

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Correspondence to Gabriel Altit.

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de Carvalho Nunes, G., Wutthigate, P., Simoneau, J. et al. The biventricular contribution to chronic pulmonary hypertension of the extremely premature infant. J Perinatol 43, 174–180 (2023). https://doi.org/10.1038/s41372-022-01497-0

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