Human fetal growth restriction: A cardiovascular journey through to adolescence

Journal of Developmental Origins of Health and Disease

Volumn 7, Issue 6, 2016, Pages 626-635

  Sehgal, A ^a   Skilton, M R ^b   Crispi, F ^c  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

cardiovascular function; dietary interventions; fetal ultrasound; intrauterine growth restriction; omega 3 supplementation

Indexed keywords

ADOLESCENT; CARDIOVASCULAR DISEASE; FEMALE; HUMAN; INTRAUTERINE GROWTH RETARDATION; PATHOPHYSIOLOGY;

ADOLESCENT; CARDIOVASCULAR DISEASES; FEMALE; FETAL GROWTH RETARDATION; HUMANS;

EID: 84978116066     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174416000337     Document Type: Review

References (80)

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
2. Alberry M, Soothill P. Management of fetal growth restriction. Arch Dis Child Fetal Neonatal Ed. 2007; 92, 62-67
3. Byrne CD, Phillips DI. Fetal origins of adult disease: epidemiology and mechanisms. J Clin Pathol. 2005; 3, 822-828
4. Gluckman PD, Hanson MA. Living the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733-1736
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
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
7. Barker DJP, Osmond C. Infant mortality, childhood nutrition and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 1077-1081
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
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
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
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
12. Fouzas S, Karatza AA, Davlouros PA, et al. Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res. 2014; 75, 651-657
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, 121 e1-121 e9
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
15. Committee on Practice Bulletins Gynecology, American College of Obstetricians and Gynecologists. Intrauterine growth restriction. Clinical management guidelines for obstetriciangynecologists. Int J Gynecol Obstet. 2001; 72, 85-96
16. Baschat AA, Cosmi E, Bilardo CM, et al. Predictors of neonatal outcome in early-onset placental dysfunction. Obstet Gynecol. 2007; 109, 253-261
17. Baschat AA. Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol. 2011; 37, 501-514
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
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
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
21. Comas M, Crispi F, Cruz-Martinez R, et al. Tissue Doppler echocardiographic markers of cardiac dysfunction in small-forgestational age foetuses. Am J Obstet Gynecol. 2011; 205, 57 e1-57 e6
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
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
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, 45 e1-45 e7
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
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
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
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
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
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
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
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
33. Skilton MK, Evans N, Griffiths KA, et al. Aortic wall thickness in newborns with intrauterine restriction. Lancet. 2005; 23, 1484-1486
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
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
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
37. Thornburg KL, Reller MD. Coronary flow regulation in the fetal sheep. Am J Physiol. 1999; 277, R1249-R1260
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
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
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
41. McGill HC Jr, McMahan CA, Herderick EE, et al. Pathobiological 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
42. Litwin M, Niemirska A. Intima-media thickness measurements in children with cardiovascular risk factors. Pediatr Nephrol. 2008; 24, 707-719
43. Blacher J, Safar ME. Large artery stiffness, hypertension and cardiovascular risk in older patients. Cardiovasc Med. 2005; 2, 450-455
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
45. Norman M, Martin H. Preterm birth attenuates association between low birth weight and endothelial dysfunction. Circulation. 2003; 108, 996-1001
46. Martin H, Gazelius B, Norman M. Impaired acetylcholineinduced vascular relaxation in low birth weight infants: implications for adult hypertension? Pediatr Res. 2000; 47, 457-462
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
48. Gardiner H, Brodszki J, Marsal K. Ventriculo-vascular physiology of the growth restricted fetus. Ultrasound Obstet Gynecol. 2001; 18, 47-53
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
50. Tintu AN, Noble FA, Rouwet EV. Hypoxia disturbs fetal hemodynamics and growth. Endothelium. 2007; 14, 353-360
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
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
53. Dratva J, Breton CV, Hodis HN, et al. Birth weight and carotid artery intima-media thickness. J Pediatr. 2013; 162, 906-911.e2
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
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
56. Norman M. Low birth weight and the developing vascular tree: a systematic review. Acta Paediatr. 2008; 97, 1165-1172
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
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
59. Hietalampi H, Pahkala K, Jokinen E, et al. Left ventricular mass and geometry in adolescence: early childhood determinants. Hypertension. 2012; 60, 1266-1272
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
61. Godfrey KM, Gluckman PD, Hanson MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010; 21, 199-205
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
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
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
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
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
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
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
69. Mori TA, Beilin LJ. Omega-3 fatty acids and inflammation. Curr Atheroscler Rep. 2004; 6, 461-467
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
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
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
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
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
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
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
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
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
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
80. Skilton MR, Mikkilä V, Würtz P, et al. Fetal growth, omega-3 (?-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