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Cardiovascular adaptation to extrauterine life after intrauterine growth restriction

  • Luciana Rodriguez-Guerineau (a1) (a2), Miriam Perez-Cruz (a3), María D. Gomez Roig (a3), Francisco J. Cambra (a2), Juan Carretero (a1), Fredy Prada (a1), Olga Gómez (a3), Fátima Crispi (a3) and Joaquim Bartrons (a1)...



The adaptive changes of the foetal heart in intrauterine growth restriction can persist postnatally. Data regarding its consequences for early circulatory adaptation to extrauterine life are scarce. The aim of this study was to assess cardiac morphometry and function in newborns with late-onset intrauterine growth restriction to test the hypothesis that intrauterine growth restriction causes cardiac shape and functional changes at birth.


A comprehensive echocardiographic study was performed in 25 neonates with intrauterine growth restriction and 25 adequate-for-gestational-age neonates.


Compared with controls, neonates with intrauterine growth restriction had more globular ventricles, lower longitudinal tricuspid annular motion, and higher left stroke volume without differences in the heart rate. Neonates with intrauterine growth restriction also showed subclinical signs of diastolic dysfunction in the tissue Doppler imaging with lower values of early (e′) diastolic annular peak velocities in the septal annulus. Finally, the Tei index in the tricuspid annulus was higher in the intrauterine growth restriction group.


Neonates with history of intrauterine growth restriction showed cardiac remodelling and signs of systolic and diastolic dysfunction. Overall, there was a significant tendency to worse cardiac function results in the right heart. The adaptation to extrauterine life occurred with more globular hearts, higher stroke volumes but a similar heart rate compared to adequate-for-gestational-age neonates.


Corresponding author

Correspondence to: L. Rodriguez-Guerineau, MD, Pediatric Cardiology Department, Hospital Sant Joan de Déu, Universitat de Barcelona, Passeig Sant Joan de Déu 2, 08950 Esplugues de Llobregat, Barcelona, Spain. Tel: +34 932 53 21 00; Fax: +34 932 03 39 59; E-mail:


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1. Wang, Y, Fu, W, Liu, J. Neurodevelopment in children with intrauterine growth restriction: adverse effects and interventions. J Matern Fetal Neonatal Med 2016; 29: 660668.
2. Bozynski, ME, Hanafy, FH, Hernandez, RJ. Association of increased cardiothoracic ratio and intrauterine growth retardation. Am J Perinatol 1991; 8: 2830.
3. Makikallio, K, Vuolteenaho, O, Jouppila, P, Rasanen, J. Ultrasonographic and biochemical markers of human fetal cardiac dysfunction in placental insufficiency. Circulation 2002; 105: 20582063.
4. Crispi, F, Hernandez-Andrade, E, Pelsers, MM, et al. Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses. Am J Obstet Gynecol 2008; 199: 254.e1-8.
5. Comas, M, Crispi, F, Cruz-Martinez, R, Figueras, F, Gratacos, E. Tissue Doppler echocardiographic markers of cardiac dysfunction in small-for-gestational age fetuses. Am J Obstet Gynecol 2011; 205: 57.e1-6.
6. Crispi, F, Figueras, F, Cruz-Lemini, M, Bartrons, J, Bijnens, B, Gratacos, E. Cardiovascular programming in children born small for gestational age and relationship with prenatal signs of severity. Am J Obstet Gynecol 2012; 207: 121.e1-9.
7. Crispi, F, Bijnens, B, Figueras, F, et al. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 2010; 121: 24272436.
8. Barker, DJ, Osmond, C, Golding, J, Kuh, D, Wadsworth, M. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989; 298: 564567.
9. Kaijser, M, Bonamy, AK, Akre, O, et al. Perinatal risk factors for ischemic heart disease: disentangling the roles of birth weight and preterm birth. Circulation 2008; 117: 405410.
10. Leipälä, JA, Boldt, T, Turpeinen, U, Vuolteenaho, O, Fellman, V. Cardiac hypertrophy and altered hemodynamic adaptation in growth-restricted preterm infants. Pediatr Res 2003; 53: 989993.
11. Fouzas, S, Karatza, AA, Davlouros, PA, et al. Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res 2014; 75: 651657.
12. Sehgal, A, Doctor, T, Menahem, S. Cardiac function and arterial biophysical properties in small for gestational age infants: postnatal manifestations of fetal programming. J Pediatr 2013; 163: 12961300.
13. Robinson, HP, Sweet, EM, Adam, AH. The accuracy of radiological estimates of gestational age using fetal crown-rump length measurements by ultrasound as a basis for comparison. Br J Obstet Gynaecol 1979; 86: 525528.
14. Baschat, AA, Gembruch, U. The cerebroplacental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003; 21: 124127.
15. Lopez, L, Colan, SD, Frommelt, PC, et al. Recommendations for quantification methods during the performance of a pediatric echocardiogram: a report from the Pediatric Measurements Writing Group of the American Society of Echocardiography Pediatric and Congenital Heart Disease Council. J Am Soc Echocardiogr 2010; 23: 465495.
16. Lowes, BD, Gill, EA, Abraham, WT, et al. Effects of carvedilol on left ventricular mass, chamber geometry, and mitral regurgitation in chronic heart failure. Am J Cardiol 1999; 83: 12011205.
17. Connolly, HM, Oh, JK. Echocardiography. In: Braunwald E, (ed.). Braunwald’s Heart Disease: A Textbook of Cardiovascular Medicine. Elsevier Saunders, Philadelphia, PA, 2012: 200269.
18. Cui, W, Roberson, DA, Chen, Z, Madronero, LF, Cuneo, BF. Systolic and diastolic time intervals measured from Doppler tissue imaging: normal values and Z-score tables, and effects of age, heart rate, and body surface area. J Am Soc Echocardiogr 2008; 21: 361370.
19. Turan, OM, Turan, S, Gungor, S, et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008; 32: 160167.
20. Veille, JC, Hanson, R, Sivakoff, M, Hoen, H, Ben-Ami, M. Fetal cardiac size in normal, intrauterine growth retarded, and diabetic pregnancies. Am J Perinatol 1993; 10: 275279.
21. Martinussen, M, Brubakk, AM, Vik, T, Yao, AC. Relationship between intrauterine growth retardation and early postnatal superior mesenteric artery blood flow velocity. Biol Neonate 1997; 71: 2230.
22. Marciniak, A, Claus, P, Sutherland, GR, et al. Changes in systolic left ventricular function in isolated mitral regurgitation. A strain rate imaging study. Eur Heart J 2007; 28: 26272636.
23. Grangl, G, Pansy, J, Burmas, A, Koestenberger, M. Tricuspid annular plane systolic excursion is reduced in infants with pulmonary hypertension: value of tricuspid annular plane systolic excursion (TAPSE) to determine right ventricular function in various conditions of pediatric pulmonary hypertension. Echocardiography 2015; 32: 883884.
24. Cruz-Lemini, M, Crispi, F, Valenzuela-Alcaraz, B, et al. Value of annular M-mode displacement vs tissue Doppler velocities to assess cardiac function in intrauterine growth restriction. Ultrasound Obstet Gynecol 2013; 42: 175181.
25. Tei, C, Ling, LH, Hodge, DO, et al. New index of combined systolic and diastolic myocardial performance: a simple and reproducible measure of cardiac function – a study in normals and dilated cardiomyopathy. J Cardiol 1995; 26: 357366.
26. Tei, C, Nishimura, RA, Seward, JB, Tajik, AJ. Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements. J Am Soc Echocardiogr 1997; 10: 169178.
27. Eidem, BW, O’Leary, PW, Tei, C, Seward, JB. Usefulness of the myocardial performance index for assessing right ventricular function in congenital heart disease. Am J Cardiol 2000; 86: 654658.


Cardiovascular adaptation to extrauterine life after intrauterine growth restriction

  • Luciana Rodriguez-Guerineau (a1) (a2), Miriam Perez-Cruz (a3), María D. Gomez Roig (a3), Francisco J. Cambra (a2), Juan Carretero (a1), Fredy Prada (a1), Olga Gómez (a3), Fátima Crispi (a3) and Joaquim Bartrons (a1)...


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