Intrauterine growth restriction: Impact on cardiovascular development and function throughout infancy

Pediatric Research

Volumn 79, Issue 6, 2016, Pages 821-830

  Cohen, Emily ^a,b   Wong, Flora Y ^a,c   Horne, Rosemary S C ^a   Yiallourou, Stephanie R ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c MONASH CHILDREN S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ARTERIAL STIFFNESS; BIOCHEMICAL ANALYSIS; CARDIOVASCULAR FUNCTION; CHRONIC DISEASE; DIASTOLIC DYSFUNCTION; FETUS; FETUS HYPOXIA; HEART DEVELOPMENT; HEART VENTRICLE REMODELING; HUMAN; INFANT; INTRAUTERINE GROWTH RETARDATION; MORBIDITY; NUTRIENT SUPPLY; NUTRITIONAL DEFICIENCY; OXYGEN SUPPLY; PLACENTA INSUFFICIENCY; POSTNATAL GROWTH; PRIORITY JOURNAL; REVIEW; SYSTOLE; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; BRAIN; CARDIOVASCULAR SYSTEM; DIASTOLE; FEMALE; GROWTH, DEVELOPMENT AND AGING; HEART; NEWBORN; PATHOPHYSIOLOGY;

OXYGEN;

ADAPTATION, PHYSIOLOGICAL; AUTONOMIC NERVOUS SYSTEM; BLOOD PRESSURE; BRAIN; CARDIOVASCULAR SYSTEM; DIASTOLE; FEMALE; FETAL GROWTH RETARDATION; FETUS; HEART; HUMANS; INFANT, NEWBORN; OXYGEN; SYSTOLE; VASCULAR STIFFNESS;

EID: 84976448913     PISSN: 00313998     EISSN: 15300447     Source Type: Journal    
DOI: 10.1038/pr.2016.24     Document Type: Review

References (86)

1. Cox P, Marton T. Pathological assessment of intrauterine growth restriction. Best Pract Res Clin Obstet Gynaecol 2009;23:751-64.
2. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet 1989;2:577-80.
3. World Health Organization. Global Status Report on Noncommunicable Diseases, 2010. http://whqlibdoc.who.int/publications/2011/ 9789240686458-eng.pdf
4. Vayssière C, Sentilhes L, Ego A, et al. Fetal growth restriction and intrauterine growth restriction: guidelines for clinical practice from the French College of Gynaecologists and Obstetricians. Eur J Obstet Gynecol Reprod Biol 2015;193:10-8.
5. Gardosi J. Intrauterine growth restriction: new standards for assessing adverse outcome. Best Pract Res Clin Obstet Gynaecol 2009;23:741-9.
6. Vijlbrief DC, van Bel F, Molenschot MC, et al. Early detection of prenatal cardiocirculatory compromise in small for gestational age infants. Neonatology 2014;105:256-62.
7. 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.
8. Pérez-Cruz M, Cruz-Lemini M, Fernández MT, et al. Fetal cardiac function in late-onset intrauterine growth restriction vs small-for-gestational age, as defined by estimated fetal weight, cerebroplacental ratio and uterine artery Doppler. Ultrasound Obstet Gynecol 2015;46:465-71.
9. Parra-Saavedra M, Crovetto F, Triunfo S, et al. Placental findings in lateonset SGA births without Doppler signs of placental insufficiency. Placenta 2013;34:1136-41.
10. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, et al. Fetal cardiovascular remodelling persists at 6 months of life in infants with intrauterine growth restriction. Ultrasound Obstet Gynecol 2015. Epub ahead of print DOI 10.1002/uog.15767.
11. Baschat AA, Harman CR. Antenatal assessment of the growth restricted fetus. Curr Opin Obstet Gynecol 2001;13:161-8.
12. Turan OM, Turan S, Gungor S, et al. Progression of Doppler abnormalities in intrauterine growth restriction. Ultrasound Obstet Gynecol 2008;32:160-7.
13. Spinillo A, Gardella B, Bariselli S, Alfei A, Silini EM, Bello BD. Cerebroplacental Doppler ratio and placental histopathological features in pregnancies complicated by fetal growth restriction. J Perinat Med 2014;42:321-8.
14. Mari G, Hanif F, Kruger M, Cosmi E, Santolaya-Forgas J, Treadwell MC. Middle cerebral artery peak systolic velocity: a new Doppler parameter in the assessment of growth-restricted fetuses. Ultrasound Obstet Gynecol 2007;29:310-6.
15. Brantberg A, Sonesson SE. Central arterial hemodynamics in small-forgestational-Age fetuses before and during maternal hyperoxygenation: a Doppler velocimetric study with particular attention to the aortic isthmus. Ultrasound Obstet Gynecol 1999;14:237-43.
16. Oros D, Figueras F, Cruz-Martinez R, Meler E, Munmany M, Gratacos E. Longitudinal changes in uterine, umbilical and fetal cerebral Doppler indices in late-onset small-for-gestational age fetuses. Ultrasound Obstet Gynecol 2011;37:191-5.
17. Iruretagoyena JI, Gonzalez-Tendero A, Garcia-Canadilla P, et al. Cardiac dysfunction is associated with altered sarcomere ultrastructure in intrauterine growth restriction. Am J Obstet Gynecol 2014;210:550.e1-7.
18. Norman M. Low birth weight and the developing vascular tree: a systematic review. Acta Paediatr 2008;97:1165-72.
19. Humphrey JD. Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress. Hypertension 2008;52: 195-200.
20. Thompson JA, Richardson BS, Gagnon R, Regnault TR. Chronic intrauterine hypoxia interferes with aortic development in the late gestation ovine fetus. J Physiol 2011;589(Pt 13):3319-32.
21. Cosmi E, Visentin S, Fanelli T, Mautone AJ, Zanardo V. Aortic intima media thickness in fetuses and children with intrauterine growth restriction. Obstet Gynecol 2009;114:1109-14.
22. Skilton MR, Evans N, Griffiths KA, Harmer JA, Celermajer DS. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet 2005;365:1484-6.
23. Lo Vasco VR, Salmaso R, Zanardo V, et al. Fetal aorta wall inflammation in ultrasound-detected aortic intima/media thickness and growth retardation. J Reprod Immunol 2011;91:103-7.
24. Koklu E, Kurtoglu S, Akcakus M, et al. Increased aortic intima-media thickness is related to lipid profile in newborns with intrauterine growth restriction. Horm Res 2006;65:269-75.
25. Koklu E, Ozturk MA, Kurtoglu S, Akcakus M, Yikilmaz A, Gunes T. Aortic intima-media thickness, serum IGF-I, IGFBP-3, and leptin levels in intrauterine growth-restricted newborns of healthy mothers. Pediatr Res 2007;62:704-9.
26. 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;163:1296-300.
27. Iwashima S, Ishikawa T, Akira O, Itou H. Association of abdominal aortic wall thickness in the newborn with maternal factors. Am J Perinatol 2012;29:441-8.
28. Stergiotou I, Crispi F, Valenzuela-Alcaraz B, Cruz-Lemini M, Bijnens B, Gratacos E. Aortic and carotid intima-media thickness in term small-forgestational-Age newborns and relationship with prenatal signs of severity. Ultrasound Obstet Gynecol 2014;43:625-31.
29. 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.
30. 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;80:119-23.
31. Akira M, Yoshiyuki S. Placental circulation, fetal growth, and stiffness of the abdominal aorta in newborn infants. J Pediatr 2006;148:49-53.
32. 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:e49-54.
33. Bubb KJ, Cock ML, Black MJ, et al. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 2007;578(Pt 3):871-81.
34. 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.
35. Takahashi N, Nishida H, Arai T, Kaneda Y. Abnormal cardiac histology in severe intrauterine growth retardation infants. Acta Paediatr Jpn 1995;37:341-6.
36. Czernik C, Rhode S, Metze B, Bührer C, Schmitz L. Comparison of left ventricular cardiac dimensions between small and appropriate for gestational age preterm infants below 30 weeks of gestation. J Perinat Med 2013;41:219-26.
37. Fouzas S, Karatza AA, Davlouros PA, et al. Neonatal cardiac dysfunction in intrauterine growth restriction. Pediatr Res 2014;75:651-7.
38. Leipälä JA, Boldt T, Turpeinen U, Vuolteenaho O, Fellman V. Cardiac hypertrophy and altered hemodynamic adaptation in growth-restricted preterm infants. Pediatr Res 2003;53:989-93.
39. Cinar B, Sert A, Gokmen Z, Aypar E, Aslan E, Odabas D. Left ventricular dimensions, systolic functions, and mass in term neonates with symmetric and asymmetric intrauterine growth restriction. Cardiol Young 2013:1-7.
40. Altin H, Karaarslan S, Karatas Z, Alp H, Sap F, Baysal T. 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;88:757-64.
41. Gürses D, Seyhan B. Evaluation of cardiac systolic and diastolic functions in small for gestational age babies during the first months of life: a prospective follow-up study. Cardiol Young 2013;23:597-605.
42. Crispi F, Bijnens B, Figueras F, et al. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 2010;121: 2427-36.
43. Fouzas S, Karatza AA, Davlouros PA, et al. Heterogeneity of ventricular repolarization in newborns with intrauterine growth restriction. Early Hum Dev 2014;90:857-62.
44. Benavides-Serralde A, Scheier M, Cruz-Martinez R, et al. Changes in central and peripheral circulation in intrauterine growth-restricted fetuses at different stages of umbilical artery flow deterioration: new fetal cardiac and brain parameters. Gynecol Obstet Invest 2011;71:274-80.
45. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, Oros D, Gratacos E. 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;38:400-5.
46. Nassr AA, Youssef AA, Zakherah MS, Ismail AM, Brost BC. Clinical application of fetal left modified myocardial performance index in the evaluation of fetal growth restriction. J Perinat Med 2015;43:749-54.
47. Rizzo G, Arduini D. Fetal cardiac function in intrauterine growth retardation. Am J Obstet Gynecol 1991;165(4 Pt 1):876-82.
48. Verburg BO, Jaddoe VW, Wladimiroff JW, Hofman A, Witteman JC, Steegers EA. Fetal hemodynamic adaptive changes related to intrauterine growth: the Generation R Study. Circulation 2008;117:649-59.
49. Rizzo G, Capponi A, Rinaldo D, Arduini D, Romanini C. Ventricular ejection force in growth-retarded fetuses. Ultrasound Obstet Gynecol 1995;5:247-55.
50. Girsen A, Ala-Kopsala M, Mäkikallio K, Vuolteenaho O, Räsänen J. Cardiovascular hemodynamics and umbilical artery N-Terminal peptide of proB-Type natriuretic peptide in human fetuses with growth restriction. Ultrasound Obstet Gynecol 2007;29:296-303.
51. Robel-Tillig E, Knüpfer M, Vogtmann C. Cardiac adaptation in small for gestational age neonates after prenatal hemodynamic disturbances. Early Hum Dev 2003;72:123-9.
52. Guajardo CD, Mandelbaum V, Linderkamp O. Cardiac output and cerebral blood flow velocity in small for gestational age infants during the first 5 days after birth. Early Hum Dev 1994;37:187-93.
53. Vitarelli A, Gheorghiade M. Diastolic heart failure: standard Doppler approach and beyond. Am J Cardiol 1998;81(12A):115G-21G.
54. Harada K, Suzuki T, Takahashi Y, et al. Abnormal left ventricular diastolic filling patterns in small-for-gestational-Age infants. Early Hum Dev 1998;51:197-204.
55. Bahlmann F, Krummenauer F, Spahn S, Gallinat R, Kampmann C. Natriuretic peptide levels in intrauterine growth-restricted fetuses with absent and reversed end-diastolic flow of the umbilical artery in relation to ductus venosus flow velocities. J Perinat Med 2011;39:529-37.
56. Mäkikallio K, Vuolteenaho O, Jouppila P, Räsänen J. Association of severe placental insufficiency and systemic venous pressure rise in the fetus with increased neonatal cardiac troponin T levels. Am J Obstet Gynecol 2000;183:726-31.
57. Chaiworapongsa T, Espinoza J, Yoshimatsu J, et al. Subclinical myocardial injury in small-for-gestational-Age neonates. J Matern Fetal Neonatal Med 2002;11:385-90.
58. Yiallourou SR, Wallace EM, Miller SL, Horne RS. Effects of intrauterine growth restriction on sleep and the cardiovascular system: The use of melatonin as a potential therapy?. Sleep Med Rev 2016;26:64-73.
59. Nijhuis IJ, ten Hof J, Mulder EJ, et al. Fetal heart rate in relation to its variation in normal and growth retarded fetuses. Eur J Obstet Gynecol Reprod Biol 2000;89:27-33.
60. Vinkesteijn AS, Struijk PC, Ursem NT, Hop WC, Wladimiroff JW. Fetal heart rate and umbilical artery flow velocity variability in intrauterine growth restriction: a matched controlled study. Ultrasound Obstet Gynecol 2004;23:461-5.
61. Graatsma EM, Mulder EJ, Vasak B, et al. Average acceleration and deceleration capacity of fetal heart rate in normal pregnancy and in pregnancies complicated by fetal growth restriction. J Matern Fetal Neonatal Med 2012;25:2517-22.
62. Sriram B, Mencer MA, McKelvey S, et al. Differences in the sleep states of IUGR and low-risk fetuses: An MCG study. Early Hum Dev 2013;89: 815-9.
63. Ribbert LS, Snijders RJ, Nicolaides KH, Visser GH. Relation of fetal blood gases and data from computer-Assisted analysis of fetal heart rate patterns in small for gestation fetuses. Br J Obstet Gynaecol 1991;98:820-3.
64. Spassov L, Curzi-Dascalova L, Clairambault J, et al. Heart rate and heart rate variability during sleep in small-for-gestational age newborns. Pediatr Res 1994;35(4 Pt 1):500-5.
65. Galland BC, Taylor BJ, Bolton DP, Sayers RM. Heart rate variability and cardiac reflexes in small for gestational age infants. J Appl Physiol (1985) 2006;100:933-9.
66. Gonçalves H, Bernardes J, Ayres-de-Campos D. Gender-specific heart rate dynamics in severe intrauterine growth-restricted fetuses. Early Hum Dev 2013;89:431-7.
67. Pagani G, D'Antonio F, Khalil A, et al. Association between reduced fetal movements at term and abnormal uterine artery Doppler indices. Ultrasound Obstet Gynecol 2014;43:548-52.
68. Gazzolo D, Visser GH, Santi F, et al. Behavioural development and Doppler velocimetry in relation to perinatal outcome in small for dates fetuses. Early Hum Dev 1995;43:185-95.
69. van Laar JO, Peters CH, Vullings R, Houterman S, Oei SG. Power spectrum analysis of fetal heart rate variability at near term and post term gestation during active sleep and quiet sleep. Early Hum Dev 2009;85:795-8.
70. Cohen G, Vella S, Jeffery H, Lagercrantz H, Katz-Salamon M. Cardiovascular stress hyperreactivity in babies of smokers and in babies born preterm. Circulation 2008;118:1848-53.
71. Van Reempts PJ, Wouters A, De Cock W, Van Acker KJ. Stress responses to tilting and odor stimulus in preterm neonates after intrauterine conditions associated with chronic stress. Physiol Behav 1997;61:419-24.
72. Pal GK, Pal P, Nanda N, Amudharaj D, Adithan C. Cardiovascular dysfunctions and sympathovagal imbalance in hypertension and prehypertension: physiological perspectives. Future Cardiol 2013;9:53-69.
73. Schäffer L, Burkhardt T, Müller-Vizentini D, et al. Cardiac autonomic balance in small-for-gestational-Age neonates. Am J Physiol Heart Circ Physiol 2008;294:H884-90.
74. Spence D, Stewart MC, Alderdice FA, Patterson CC, Halliday HL. Intrauterine growth restriction and increased risk of hypertension in adult life: a follow-up study of 50-year-olds. Public Health 2012;126:561-5.
75. Huxley R, Neil A, Collins R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure?. Lancet 2002;360:659-65.
76. Singhal A, Cole TJ, Fewtrell M, et al. Promotion of faster weight gain in infants born small for gestational age: is there an adverse effect on later blood pressure?. Circulation 2007;115:213-20.
77. Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ. Early growth and death from cardiovascular disease in women. BMJ 1993;307:1519-24.
78. Hindmarsh PC, Bryan S, Geary MP, Cole TJ. Effects of current size, postnatal growth, and birth size on blood pressure in early childhood. Pediatrics 2010;126:e1507-13.
79. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull 2001;60:5-20.
80. Lim K, Lombardo P, Schneider-Kolsky M, Black MJ. Intrauterine growth restriction coupled with hyperglycemia: effects on cardiac structure in adult rats. Pediatr Res 2012;72:344-51.
81. Robertson MC, Murila F, Tong S, Baker LS, Yu VY, Wallace EM. Predicting perinatal outcome through changes in umbilical artery Doppler studies after antenatal corticosteroids in the growth-restricted fetus. Obstet Gynecol 2009;113:636-40.
82. Giussani DA, Niu Y, Herrera EA, et al. Heart disease link to fetal hypoxia and oxidative stress. Adv Exp Med Biol 2014;814:77-87.
83. Satterfield MC, Bazer FW, Spencer TE, Wu G. Sildenafil citrate treatment enhances amino acid availability in the conceptus and fetal growth in an ovine model of intrauterine growth restriction. J Nutr 2010;140:251-8.
84. Miller SL, Wallace EM, Walker DW. Antioxidant therapies: a potential role in perinatal medicine. Neuroendocrinology 2012;96:13-23.
85. Skilton MR, Ayer JG, Harmer JA, et al. Impaired fetal growth and arterial wall thickening: a randomized trial of ?-3 supplementation. Pediatrics 2012;129:e698-703.
86. Skilton MR, Raitakari OT, Celermajer DS. High intake of dietary longchain ?-3 fatty acids is associated with lower blood pressure in children born with low birth weight: NHANES 2003-2008. Hypertension 2013;61:972-6.