Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T20:45:27.791Z Has data issue: false hasContentIssue false
  • English
  • Français

Human fetal growth restriction: a cardiovascular journey through to adolescence

Published online by Cambridge University Press:  07 July 2016

A. Sehgal ,
M. R. Skilton Open the ORCID record for M. R. Skilton [Opens in a new window]  and
F. Crispi
A. Sehgal*
Affiliation:
Monash Children’s Hospital, Block E Monash Medical Centre, Clayton VIC 3186, Australia Department of Paediatrics, Monash University, Melbourne, Australia
M. R. Skilton
Affiliation:
The Boden Institute of Obesity, Nutrition, Exercise & Eating Disorders, The University of Sydney, New South Wales, Australia
F. Crispi
Affiliation:
BCNatal-Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), IDIBAPS, University of Barcelona, Centre for Biomedical Research on Rare Diseases (CIBER-ER), Barcelona, Spain
*
*Address for correspondence: A. Sehgal, Neonatologist, Monash Newborn, Monash Children’s Hospital, Monash University, 246, Clayton Road, Clayton, Melbourne, VIC 3168, Australia. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Intrauterine growth restriction has been noted to adversely impact morbidity and mortality in the neonatal period as well as cardiovascular well-being in adolescence and adulthood. Recent data based on a wide range of ultrasound parameters during fetal and neonatal life has noted early and persistent involvement of the cardiovascular system. Some of these measures are predictive of long-term morbidities. Assessment of vascular mechanics is a new and novel concept in this population, and opens up avenues for diagnosis, monitoring and evaluation of the likely effectiveness of interventions. Prevention of these adverse vascular and cardiac outcomes secondary to fetal growth restriction may be feasible and of clinical relevance. This review focuses on growth restriction in humans with respect to cardiovascular remodeling and dysfunction during fetal life, persistence of functional cardiac impairment during early childhood and adolescence, and possible preventive strategies.

Keywords

cardiovascular functiondietary interventionsfetal ultrasoundintrauterine growth restrictionomega-3 supplementation
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 6: Themed Issue: Developmental Origins of Adult Mental Health and Illness , December 2016 , pp. 626 - 635
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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.)

Footnotes

†

Arvind Sehgal wrote the first draft but all authors are equal first authors.

References

1. Figueras, F, Gratacós, E. Update on the diagnosis and classification of fetal growth restriction and proposal of a stage-based management protocol. Fetal Diagn Ther. 2014; 36, 86–98.Google Scholar
2. Alberry, M, Soothill, P. Management of fetal growth restriction. Arch Dis Child Fetal Neonatal Ed. 2007; 92, 62–67.Google Scholar
3. Byrne, CD, Phillips, DI. Fetal origins of adult disease: epidemiology and mechanisms. J Clin Pathol. 2005; 3, 822–828.Google Scholar
4. Gluckman, PD, Hanson, MA. Living the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.Google Scholar
5. Cater, J, Gill, M. The follow-up study: medical aspects. In Low Birth Weight, a Medical Psychological and Social Study (eds. Illsley R, Mitchell RG), 1984; pp. 191–205. John Wiley: Chichester.Google Scholar
6. Simpson, A, Mortimer, JG, Silva, PA, et al. Correlates of blood pressure in a cohort of Dunedin seven year old children. In Hypertension in the Young and Old (eds. Onesti G, Kim KE), 1981; pp. 153–156. Grune and Stratton: New York, NY.Google Scholar
7. Barker, DJP, Osmond, C. Infant mortality, childhood nutrition and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 1077–1081.Google Scholar
8. Barker, DJP, Osmond, C. Death rates from stroke in England and Wales predicted from past maternal mortality. Br Med J. 1987; 295, 83–86.Google Scholar
9. Cruz-Lemini, M, Crispi, F, Valenzuela-Alcaraz, B, et al. A fetal cardiovascular score to predict infant hypertension and arterial remodeling in intrauterine growth restriction. Am J Obstet Gynecol. 2014; 210, 552.e1–552.e22.Google Scholar
10. 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, 1296–1300.CrossRefGoogle ScholarPubMed
11. Altin, H, Karaarslan, S, Karataş, Z, et al. Evaluation of cardiac functions in term small for gestational age newborns with mild growth retardation: a serial conventional and tissue Doppler imaging echocardiographic study. Early Hum Dev. 2012; 88, 757–764.CrossRefGoogle ScholarPubMed
12. Fouzas, S, Karatza, AA, Davlouros, PA, et al. Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res. 2014; 75, 651–657.CrossRefGoogle ScholarPubMed
13. Crispi, F, Figueras, F, Cruz-Lemini, M, et al. Cardiovascular programming in children born small for gestational age and relationship with prenatal signs of severity. Am J Obstet Gynecol. 2012; 207, 121e1–121e9.CrossRefGoogle ScholarPubMed
14. Bradley, TJ, Potts, JE, Lee, SK, et al. Early changes in the biophysical properties of the aorta in pre-adolescent children born small for gestational age. J Pediatr. 2010; 156, 388–392.Google Scholar
15. Committee on Practice Bulletins Gynecology, American College of Obstetricians and Gynecologists. Intrauterine growth restriction. Clinical management guidelines for obstetrician-gynecologists. Int J Gynecol Obstet. 2001; 72, 85–96.Google Scholar
16. Baschat, AA, Cosmi, E, Bilardo, CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol. 2007; 109, 253–261.Google Scholar
17. Baschat, AA. Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol. 2011; 37, 501–514.Google Scholar
18. Parra-Saavedra, M, Crovetto, F, Triunfo, S, et al. Placental findings in late-onset SGA births without Doppler signs of placental insufficiency. Placenta. 2013; 34, 1136–1141.Google Scholar
19. 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 e1–254 e8.Google Scholar
20. Cruz-Lemini, M, Crispi, F, Valenzuela-Alcaraz, B, et al. Value of annular M-mode displacement versus tissue Doppler velocities to assess cardiac function in intrauterine growth restriction. Ultrasound Obstet Gynecol. 2013; 42, 175–181.Google Scholar
21. Comas, M, Crispi, F, Cruz-Martinez, R, et al. Tissue Doppler echocardiographic markers of cardiac dysfunction in small-for-gestational age foetuses. Am J Obstet Gynecol. 2011; 205, 57e1–57e6.Google Scholar
22. Crispi, F, Bijnens, B, Figueras, F, et al. Fetal growth restriction results in remodelled and less efficient hearts in children. Circulation. 2010; 121, 2427–2436.Google Scholar
23. Cruz-Lemini, M, Bijnens, B, Valenzuela-Alcaraz, B, et al. Cardiac remodelling in utero in early- and late-onset intrauterine growth restriction. Ultrasound Obstet Gynecol. 2012; 40, 14.Google Scholar
24. Comas, M, Crispi, F, Cruz-Martinez, R, et al. Usefulness of myocardial tissue Doppler vs conventional echocardiography in the evaluation of cardiac dysfunction in early-onset intrauterine growth restriction. Am J Obstet Gynecol. 2010; 203, 45e1–45e7.CrossRefGoogle ScholarPubMed
25. Bilardo, CM, Wolf, H, Stigter, RH, et al. Relationship between monitoring parameters and perinatal outcome in severe, early intrauterine growth restriction. Ultrasound Obstet Gynecol. 2004; 23, 119–125.Google Scholar
26. Makikallio, K, Vuolteenaho, O, Jouppila, P, et al. Ultrasonographic and biochemical markers of human fetal cardiac dysfunction in placental insufficiency. Circulation. 2002; 105, 2058–2063.Google Scholar
27. Niewiadomska-Jarosik, K, Lipecka-Kidawska, E, Kowalska-Koprek, U, et al. Assessment of cardiac function in fetuses with intrauterine growth retardation using the Tei index. Med Wieku Rozwoj. 2005; 9, 153–160.Google Scholar
28. Larsen, LU, Petersen, OB, Sloth, E, et al. Color Doppler myocardial imaging demonstrates reduced diastolic tissue velocity in growth retarded fetuses with flow redistribution. Eur J Obstet Gynecol Reprod Biol. 2011; 155, 140–145.Google Scholar
29. Crispi, F, Bijnens, B, Sepulveda-Swatson, E, et al. Post-systolic shortening by myocardial deformation imaging as a sign of cardiac adaptation to pressure overload in fetal growth restriction. Circ Cardiovasc Imaging. 2014; 7, 781–787.Google Scholar
30. Pérez-Cruz, M, Cruz-Lemini, M, Fernández, MT, et al. Fetal cardiac function in late-onset ‘intrauterine growth restriction’ versus ‘small-for-gestational age’ as defined by estimated fetal weight, cerebro-placental ratio and uterine artery Doppler. Ultrasound Obstet Gynecol. 2015; 46, 465–471.Google Scholar
31. Cruz-Martinez, R, Figueras, F, Hernandez-Andrade, E, et al. Changes in myocardial performance index and aortic isthmus and ductus venosus Doppler in term, small-for-gestational age fetuses with normal umbilical artery pulsatility index. Ultrasound Obstet Gynecol. 2011; 38, 400–405.Google Scholar
32. Chaiworapongsa, T, Espinoza, J, Yoshimatsu, J, et al. Subclinical myocardial injury in small-for-gestational-age neonates. J Matern Fetal Neonatal Med. 2002; 11, 385–390.Google Scholar
33. Skilton, MK, Evans, N, Griffiths, KA, et al. Aortic wall thickness in newborns with intrauterine restriction. Lancet. 2005; 23, 1484–1486.CrossRefGoogle Scholar
34. Rizzo, G, Capponi, A, Pietrolucci, ME, et al. The significance of visualising coronary blood flow in early onset severe growth restricted fetuses with reverse flow in the ductus venosus. J Matern Fetal Neonatal Med. 2009; 22, 547–551.Google Scholar
35. Aburawi, EH, Malcus, P, Thuring, A, et al. Coronary flow in neonates with impaired intrauterine growth. J Am Soc Echocardiogr. 2012; 25, 313–318.Google Scholar
36. Reller, MD, Morton, MJ, Giraud, GD, et al. Maximal myocardial blood flow is enhanced by chronic hypoxemia in late gestation fetal sheep. Am J Physiol. 1992; 263, H1327–H1329.Google Scholar
37. Thornburg, KL, Reller, MD. Coronary flow regulation in the fetal sheep. Am J Physiol. 1999; 277, R1249–R1260.Google Scholar
38. Sehgal, A, Doctor, T, Menahem, S. Cardiac function and arterial indices in infants born small for gestational age: analysis by speckle tracking. Acta Paediatr. 2014; 103, e49–e54.Google Scholar
39. Koklu, E, Ozturk, MA, Kurtoglu, S, et al. Aortic intima-media thickness, serum IGF-I, IGFBP-3, and leptin levels in intrauterine growth-restricted newborns of healthy mothers. Pediatr Res. 2007; 62, 704–709.CrossRefGoogle ScholarPubMed
40. Zanardo, V, Fanelli, T, Weiner, G, et al. Intrauterine growth restriction is associated with persistent aortic wall thickening and glomerular proteinuria during infancy. Kidney Int. 2011; 80, 119–123.Google Scholar
41. McGill, HC Jr, McMahan, CA, Herderick, EE, et al. Patho-biological determinants of atherosclerosis in youth research group. effect of coronary heart disease risk factors on atherosclerosis of selected regions of the aorta and right coronary artery. Arterioscler Thromb Vasc Biol. 2000; 20, 836–845.Google Scholar
42. Litwin, M, Niemirska, A. Intima-media thickness measurements in children with cardiovascular risk factors. Pediatr Nephrol. 2008; 24, 707–719.Google Scholar
43. Blacher, J, Safar, ME. Large artery stiffness, hypertension and cardiovascular risk in older patients. Cardiovasc Med. 2005; 2, 450–455.Google Scholar
44. Tauzin, L, Rossi, P, Giusano, B, et al. Characteristics of arterial stiffness in very low birth weight premature infants. Pediatr Res. 2006; 60, 592–596.Google Scholar
45. Norman, M, Martin, H. Preterm birth attenuates association between low birth weight and endothelial dysfunction. Circulation. 2003; 108, 996–1001.Google Scholar
46. Martin, H, Gazelius, B, Norman, M. Impaired acetylcholine-induced vascular relaxation in low birth weight infants: implications for adult hypertension? Pediatr Res. 2000; 47, 457–462.Google Scholar
47. Verburg, BO, Jaddoe, VW, Wladimiroff, JW, et al. Fetal hemodynamic adaptive changes related to intrauterine growth: the Generation R study. Circulation. 2008; 117, 649–659.Google Scholar
48. Gardiner, H, Brodszki, J, Marsal, K. Ventriculo-vascular physiology of the growth restricted fetus. Ultrasound Obstet Gynecol. 2001; 18, 47–53.Google Scholar
49. Tintu, A, Rouwet, E, Verlohren, S, et al. Hypoxia induces dilated cardiomyopathy in the chick embryo: mechanism, intervention, and long-term consequences. PLoS One. 2009; 4, e5155.Google Scholar
50. Tintu, AN, Noble, FA, Rouwet, EV. Hypoxia disturbs fetal hemodynamics and growth. Endothelium. 2007; 14, 353–360.Google Scholar
51. Rouwet, EV, Tintu, AN, Schellings, MW, et al. Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyper-innervation of peripheral arteries in the chick embryo. Circulation. 2002; 105, 2791–2796.Google Scholar
52. Miles, KA, McDonnell, BJ, Maki-Petaja, KM, et al. The impact of birth weight on blood pressure and arterial stiffness in later life: the Enigma study. J Hypertens. 2011; 29, 2324–2331.Google Scholar
53. Dratva, J, Breton, CV, Hodis, HN, et al. Birth weight and carotid artery intima-media thickness. J Pediatr. 2013; 162, 906–911.e2.Google Scholar
54. Skilton, MR, Pahkala, K, Viikari, JS, et al. The association of dietary alpha-linolenic acid with blood pressure and subclinical atherosclerosis in people born small for gestational age: the special turku coronary risk factor intervention project study. J Pediatr. 2015; 166, 1252–1257.Google Scholar
55. Skilton, MR, Ayer, JG, Harmer, JA, et al. Impaired fetal growth and arterial wall thickening. A randomized trial of omega-3 supplementation. Pediatrics. 2012; 129, e698.Google Scholar
56. Norman, M. Low birth weight and the developing vascular tree: a systematic review. Acta Paediatr. 2008; 97, 1165–1172.Google Scholar
57. Skilton, MR, Viikari, JS, Juonala, M, et al. Fetal growth and preterm birth influence cardiovascular risk factors and arterial health in young adults: the cardiovascular risk in young Finns study. Arterioscler Thromb Vasc Biol. 2011; 31, 2975–2981.Google Scholar
58. Napoli, C, Glass, CK, Witztum, JL, et al. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet. 1999; 354, 1234–1241.Google Scholar
59. Hietalampi, H, Pahkala, K, Jokinen, E, et al. Left ventricular mass and geometry in adolescence: early childhood determinants. Hypertension. 2012; 60, 1266–1272.Google Scholar
60. Kuh, D, Ben-Shlomo, Y. Should we intervene to improve fetal and infant growth?. In A Life Course Approach to Chronic Disease Epidemiology (eds. Kuh D, Ben Shlomo Y, Ezra S), 2004; pp. 399–414. Oxford University Press: New York.Google Scholar
61. Godfrey, KM, Gluckman, PD, Hanson, MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010; 21, 199–205.Google Scholar
62. Yu, ZB, Han, SP, Zhu, GZ, et al. Birth weight and subsequent risk of obesity: a systematic review and meta-analysis. Obes Rev. 2011; 12, 525–542.Google Scholar
63. Rodriguez-Lopez, M, Osorio, L, Acosta, R, et al. Influence of breastfeeding and postnatal nutrition on cardiovascular remodelling induced by fetal growth restriction. Pediatric Res. 2016; 79, 100–106.Google Scholar
64. Stocks, T, Renders, CM, Bulk-Bunschoten, AM, et al. Body size and growth in 0-to 4-year-old children and the relation to body size in primary school age. Obes Rev. 2011; 12, 637–652.Google Scholar
65. Skilton, MR, Marks, GB, Ayer, JG, et al. Weight gain in infancy and vascular risk factors in later childhood. Pediatrics. 2013; 131, e1821–e1828.Google Scholar
66. Wen, LM, Baur, LA, Simpson, JM, et al. Effectiveness of home based early intervention on children’s BMI at age 2: randomised controlled trial. BMJ. 2012; 344, e3732.Google Scholar
67. Kramer, MS, Chalmers, B, Hodnett, ED, et al. Promotion of Breastfeeding Intervention Trial (PROBIT): a randomized trial in the Republic of Belarus. JAMA. 2001; 285, 413–420.Google Scholar
68. Skilton, MR, Raitakari, OT, Celermajer, DS. High intake of dietary long chain omega-3 fatty acids is associated with lower blood pressure in children born with low birth weight: NHANES 2003–2008. Hypertension. 2013; 61, 972–976.Google Scholar
69. Mori, TA, Beilin, LJ. Omega-3 fatty acids and inflammation. Curr Atheroscler Rep. 2004; 6, 461–467.Google Scholar
70. Labayen, I, Moreno, LA, Ruiz, JR, et al. Associations of birth weight with serum long chain polyunsaturated fatty acids in adolescents; the HELENA study. Atherosclerosis. 2011; 217, 286–291.Google Scholar
71. Ozanne, SE, Martensz, ND, Petry, CJ, et al. Maternal low protein diet in rats programmes fatty acid desaturase activities in the offspring. Diabetologia. 1998; 41, 1337–1342.CrossRefGoogle ScholarPubMed
72. Ornish, D, Brown, SE, Scherwitz, LW, et al. Can lifestyle changes reverse coronary heart disease? The lifestyle heart trial. Lancet. 1990; 336, 129–133.Google Scholar
73. Estruch, R, Ros, E, Salas-Salvadó, J, et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med. 2013; 368, 1279–1290.Google Scholar
74. Giussani, DA, Camm, EJ, Niu, Y, et al. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One. 2012; 7, e31017.Google Scholar
75. Kane, AD, Herrera, EA, Camm, EJ, et al. Vitamin C prevents intrauterine programming of in vivo cardiovascular dysfunction in the rat. Circ J. 2013; 77, 2604–2611.Google Scholar
76. Richter, HG, Camm, EJ, Modi, BN, et al. Ascorbate prevents placental oxidative stress and enhances birth weight in hypoxic pregnancy in rats. J Physiol. 2012; 15, 590, 1377–1387.Google Scholar
77. Cambonie, G, Comte, B, Yzydorczyk, C, et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1236–R1245.CrossRefGoogle ScholarPubMed
78. Tare, M, Parkington, HC, Wallace, EM, et al. Maternal melatonin administration mitigates coronary stiffness and endothelial dysfunction, and improves heart resilience to insult in growth restricted lambs. J Physiol. 2014; 592, 2695–2709.Google Scholar
79. Itani, N, Skeffington, KL, Beck, C, et al. Melatonin rescues cardiovascular dysfunction during hypoxic development in the chick embryo. J Pineal Res. 2016; 60, 16–26.Google Scholar
80. Skilton, MR, Mikkilä, V, Würtz, P, et al. Fetal growth, omega-3 (ω-3) fatty acids, and progression of subclinical atherosclerosis: preventing fetal origins of disease? The cardiovascular risk in young finns study. Am J Clin Nutr. 2013; 97, 58–65.Google Scholar