Long-term follow-up of intrauterine growth restriction: Cardiovascular disorders

Fetal Diagnosis and Therapy

Volumn 36, Issue 2, 2014, Pages 143-153

  Demicheva, Elena ^a   Crispi, Fatima ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Cardiovascular disease; Fetal programming; Intrauterine growth restriction; Long term consequences

Indexed keywords

BLOOD CLOTTING DISORDER; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; CLINICAL EXAMINATION; COHORT ANALYSIS; DIABETES MELLITUS; DISEASE PREDISPOSITION; DYSLIPIDEMIA; EARLY DIAGNOSIS; FOLLOW UP; HUMAN; HYPERTENSION; INTRAUTERINE GROWTH RETARDATION; LOW BIRTH WEIGHT; MATERNAL NUTRITION; NONHUMAN; PLACENTA CIRCULATION; PREMATURITY; PRIORITY JOURNAL; PROSPECTIVE STUDY; REVIEW; ADOLESCENT; CHILD; DISEASE CLASSIFICATION; FEMALE; HEART ATRIUM REMODELING; ISCHEMIC HEART DISEASE; LONG TERM CARE; PLACENTA DISORDER; PLACENTA INSUFFICIENCY; PRENATAL EXPOSURE; PREVALENCE; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; PATHOPHYSIOLOGY; PREGNANCY; RISK FACTOR;

CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; FEMALE; FETAL GROWTH RETARDATION; FOLLOW-UP STUDIES; HUMANS; PREGNANCY; RISK FACTORS;

EID: 84907326055     PISSN: 10153837     EISSN: 14219964     Source Type: Journal    
DOI: 10.1159/000353633     Document Type: Review

References (129)

1. European Heart Network: European Cardiovascular Disease Statistics 2008.
2. Berenson GS: Childhood risk factors predict adult risk associated with subclinical cardiovascular disease. The Bogalusa Heart Study. Am J Cardiol 2002; 90: 3L-7L.
3. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME: Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989; 298: 564-567.
4. Barker DJ: Fetal origins of coronary heart disease. BMJ 1995; 311: 171-174.
5. Tintu A, Rouwet E, Verlohren S, Brinkmann J, Ahmad S, Crispi F, van Bilsen M, Carmeliet P, Staff AC, Tjwa M, Cetin I, Gratacos E, Hernandez-Andrade E, Hofstra L, Jacobs M, Lamers WH, Morano I, Safak E, Ahmed A, le Noble F: Hypoxia induces dilated cardiomyopathy in the chick embryo: mechanism, intervention, and long-term consequences. PLoS One 2009; 4:e5155.
6. Gluckman PD: Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res 2004; 56: 311-317.
7. Palinski W, Napoli C: Impaired fetal growth, cardiovascular disease, and the need to move on. Circulation 2008; 117: 341-343.
8. Phillips D: Insulin resistance as a programmed response to fetal undernutrition. Diabetologia 1996; 39: 1119-1122.
9. Gluckman PD, Hanson MA, Cooper C, Thornburg KL: Effect of in utero and earlylife conditions on adult health. N Engl J Med 2008; 359: 61-73.
10. Diderholm B: Perinatal energy metabolism with reference to IUGR and SGA: studies in pregnant women and newborn infants. Indian J Med Res 2009; 130: 612-617.
11. 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.
12. Alberry M, Soothill P: Management of fetal growth restriction. Arch Dis Child Fetal Neonatal Ed 2007; 92: 62-67.
13. Baschat AA: Fetal responses to placental insufficiency: an update. BJOG 2004; 111: 1031-1041.
14. Hecher K, Bilardo CM, Stigter RH, Ville Y, Hackeloer BJ, Kok HJ, Senat MV, Visser GH: Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 2001; 18: 564-570.
15. Baschat AA: Neurodevelopment following fetal growth restriction and its relationship with antepartum parameters of placental dysfunction. Ultrasound Obstet Gynecol 2011; 37: 501-514.
16. Baschat AA: Fetal growth restriction-from observation to intervention. J Perinat Med 2010; 38: 239-246.
17. Hecher K, Campbell S, Doyle P, Harrington K, Nicolaides K: Assessment of fetal compromise by Doppler ultrasound investigation of the fetal circulation: arterial, intracardiac, and venous blood flow velocity studies. Circulation 1995; 91: 129-138.
18. Crispi F, Hernandez-Andrade E, Pelsers MM, Plasencia W, Benavides-Serralde JA, Eixarch E, Le Noble F, Ahmed A, Glatz JF, Nicolaides KH, Gratacos E: Cardiac dysfunction and cell damage across clinical stages of severity in growth-restricted fetuses. Am J Obstet Gynecol 2008; 199: 254e1-e8.
19. Comas M, Crispi F, Cruz-Martinez R, Martinez JM, Figueras F, Gratacos E: Usefulness of myocardial tissue Doppler vs. conventional echocardiography in the evaluation of cardiac dysfunction in early-onset intrauterine growth restriction. J Obstet Gynecol 2010; 203: 45e1-e7.
20. Kiserud T, Kessler J, Ebbing C, Rasmussen S: Ductus venosus shunting in growth-restricted fetuses and the effect of umbilical circulatory compromise. Ultrasound Obstet Gynecol 2006; 28: 143-149.
21. Iruretagoyena JY, Torre I, Amat-Roldan I, Psilodimitrakopoulos S, Crispi F, Garcia-Canadilla P, Gonzalez-Tendero A, Nadal A, Eixarch E, Loza-Alvarez P, Artigas D, Gratacos E: Ultrastructural analysis of myocardiocyte sarcomeric changes in relation with cardiac dysfunction in human fetuses with intrauterine growth restriction. Am J Obstet Gynecol 2011; 204:S34.
22. Bijnens B, Cikes M, Butakoff C, Sitges M, Crispi F: Myocardial motion and deformation: what does it tell us and how does it relate to function? Fetal Diagn Ther 2012; 32: 5-16.
23. Huxley RR, Shiell AW, Law CM: The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens 2000; 18: 815-831.
24. Perk J, De Backer G, Gohlke H, Graham I, Reiner Z, Verschuren WM, Albus C, Benlian P, Boysen G, Cifkova R, Deaton C, Ebrahim S, Fisher M, Germano G, Hobbs R, Hoes A, Karadeniz S, Mezzani A, Prescott E, Ryden L, Scherer M, Syvanne M, et al: European guidelines on cardiovascular disease prevention in clinical practice. Eur Heart J 2012; 33: 1635-1701.
25. Skilton MR, Ayer JG, Harmer JA, Webb K, Leeder SR, Marks GB, Celermajer DS: Impaired fetal growth and arterial wall thickening. A randomized trial of omega-3 supplementation. Pediatrics 2012; 129:e698.
26. Estruch R, Ros E, Salas-Salvadó J, Covas MI, Corella D, Arós F, Gómez-Gracia E, Ruiz-Gutiérrez V, Fiol M, Lapetra J, Lamuela-Raventos RM, Serra-Majem L, Pintó X, Basora J, Muñoz MA, Sorlí JV, Martínez JA, Martínez-González MA: Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 2013; 368: 1279-1290.
27. Gennser G, Rymark P, Isberg PE: Low birth weight and risk of high blood pressure in adulthood. Bone Miner J 1988; 296: 1498-1500.
28. Leon DA, Johansson M, Rasmussen F: Gestational age and growth rate of fetal mass are inversely associated with systolic blood pressure in young adults: an epidemiologic study of 165, 136 Swedish men aged 18 years. Am J Epidemiol 2000; 152: 597-604.
29. Martyn CN, Barker DJ, Jespersen S, Greenwald S, Osmond C, Berry C: Growth in utero, adult blood pressure, and arterial compliance. Br Heart J 1995; 73: 116-121.
30. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, Winter PD: Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991; 303: 1019-1022.
31. Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ: Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 1996; 94: 3246-3250.
32. Joseph KS, Kramer MS: Review of the evidence on fetal and early childhood antecedents of adult chronic disease. Epidemiol Rev 1996; 18: 158-174.
33. Leon DA, Lithell HO, Vâgerö D, Koupilová I, Mohsen R, Berglund L, Lithell UB, McKeigue PM: Reduced fetal growth rate and increased risk of death from ischemic heart disease: cohort study of 15, 000 Swedish men and women born 1915-29. BMJ 1998; 317: 241-245.
34. Rich-Edwards JW, Stampfer MJ, Manson JE, Rosner B, Hankinson SE, Colditz GA, Willett WC, Hennekens CH: Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 1997; 315: 369-400.
35. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ: Weight in infancy and death from ischemic heart disease. Lancet 1989; 2: 577-580.
36. Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ: Early growth and death from cardiovascular disease in women. BMJ 1993; 307: 1519-1524.
37. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJ: Early growth and coronary heart disease in later life: longitudinal study. Bone Miner J 2001; 322: 949-953.
38. Eriksson JG, Forsén T, Tuomilehto J, Winter PD, Osmond C, Barker DJ: Catch-up growth in childhood and death from coronary heart disease: longitudinal study. Bone Miner J 1999; 318: 427-431.
39. Forsén T, Eriksson JG, Tuomilehto J, Teramo K, Osmond C, Barker DJ: Mother's weight in pregnancy and coronary heart disease in a cohort of Finish men: follow-up study. Bone Miner J 1997; 315: 837-840.
40. Forsén T, Eriksson JG, Tuomilehto J, Osmond C, Barker DJ: Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. Bone Miner J 1999; 319: 1403-1407.
41. Levitt NS, Lambert EV, Woods D, Hales CN, Andrew R, Seckl JR: Impaired glucose tolerance and elevated blood pressure in low birth weight, nonobese, young south African adults: early programming of cortisol axis. J Clin Endocrinol Metab 2000; 85: 4611-4618.
42. Law CM, Shiell AW: Is blood pressure inversely related to birth weight? The strength of evidence from a systematic review of the literature. J Hypertens 1996; 14: 935-941.
43. Nilsson PM, Ostergren PO, Nyberg P, Söderström M, Allebeck P: Low birth weight is associated with elevated systolic blood pressure in adolescence: a prospective study of a birth cohort of 149, 378 Swedish boys. J Hypertens 1997; 15: 1627-1631.
44. 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: 649-659.
45. 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: 57e1-e6.
46. 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, smallfor-gestational age fetuses with normal umbilical artery pulsatility index. Ultrasound Obstet Gynecol 2011; 38: 400-405.
47. Figueras F, Eixarch E, Gratacos E, Gardosi J: Predictiveness of antenatal umbilical artery Doppler for adverse pregnancy outcome in small-for- gestational-age babies according to customised birth weight centiles: population-based study. BJOG 2008; 115: 590-594.
48. Soothill PW, Bobrow CS, Holmes R: Small for gestational age is not a diagnosis. Ultrasound Obstet Gynecol 1999; 13: 225-228.
49. 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: 121e1-e9.
50. Zanardo V, Visentin S, Trevisanuto D, Bertin M, Cavallin F, Cosmi E: Fetal aortic wall thickness: a marker of hypertension in IUGR children? Hypertens Res 2013, E-pub ahead of print.
51. Villar J, Belizan JM: The timing factor in the pathophysiology of the intrauterine growth retardation syndrome. Obstet Gynecol Surv 1982; 37: 499-506.
52. Ergaz Z, Avgil M, Ornoy A: Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol 2005; 20: 301-322.
53. Ozaki T, Nishina H, Hanson MA, Poston L: Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol 2001; 530: 141-152.
54. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD: Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 2000; 279:E83-E87.
55. Barnes SK, Ozanne SE: Pathways linking the early environment to long-term health and lifespan. Prog Biophys Mol Biol 2011; 106: 323-336.
56. Tarry-Adkins JL, Ozanne SE: Mechanisms of early life programming: current knowledge and future directions. J Clin Nutr 2011; 96(suppl):1765S-1771S.
57. Garofano A, Czernichow P, Bréant B: Postnatal somatic growth and insulin contents in moderate or severe intrauterine growth retardation in the rat. Biol Neonate 1998; 73: 89-98.
58. McMillen IC, Robinson JS: Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005; 85: 571-633.
59. Langley SC, Jackson AA: Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low-protein diets. Clin Sci (Lond) 1994; 86: 217-222.
60. Snoeck A, Remacle C, Reusens B, Hoet JJ: Effect of a low-protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 1990; 57: 2107-2118.
61. Nuyt AM, Alexander BT: Developmental programming and hypertension. Curr Opin Nephrol Hypertens 2009; 18: 144-152.
62. Watkins AJ, Lucas ES, Torrens C, Cleal JK, Green L, Osmond C, Eckert JJ, Gray WP, Hanson MA, Fleming TP: Maternal low-protein diet during mouse preimplantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr 2010; 103: 1762-1770.
63. Nishina H, Green LR, McGarrigle HH, et al: Effect of nutritional restriction in early pregnancy on isolated femoral artery function in mid-gestation fetal sheep. J Physiol 2003; 553: 637-647.
64. Langley-Evans SC, Welham SJ, Sherman RC, Jackson AA: Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci 1996; 91: 607-615.
65. Huizinga CT, Engelbregt MJ, Rekers-Mombarg LT, Vaessen SF, Delemarre-van de Waal HA, Fodor M: Ligation of the uterine artery and early postnatal food restriction-animal models for growth retardation. Horm Res 2004; 62: 233-240.
66. Wigglesworth JS: Experimental growth retardation in the fetal rat. Am J Obstet Gynecol 1964; 88: 1-13.
67. Briscoe TA, Rehn AE, Dieni S, Duncan JR, Wlodek ME, Owens JA, Rees SM: Cardiovascular and renal disease in the adolescent guinea pig after chronic placental insufficiency. Am J Obstet Gynecol 2004; 191: 847-855.
68. Lafeber HN, Rolph TP, Jones CT: Studies on the growth of the fetal guinea pig. The effects of ligation of the uterine artery on organ growth and development. J Dev Physiol 1984; 6: 441-459.
69. Jones CT, Lafeber HN, Roebuck MM: Studies on the growth of the fetal guinea pig. Changes in plasma hormone concentration during normal and abnormal growth. J Dev Physiol 1984; 6: 461-472.
70. Rehn AE, Van Den Buuse M, Copolov D, Briscoe T, Lambert G, Rees S: An animal model of chronic placental insufficiency: relevance to neurodevelopmental disorders including schizophrenia. Neuroscience 2004; 129: 381-391.
71. Eixarch E, Hernandez-Andrade E, Crispi F, Illa M, Torre I, Figueras F, Gratacos E: Impact on fetal mortality and cardiovascular Doppler of selective ligature of uteroplacental vessels compared with undernutrition in rabbit model of IUGR. Placenta 2011; 32: 304-309.
72. Anthony RV, Scheaffer AN, Wright CD, Regnault TR: Ruminant models of prenatal growth restriction. Reprod Suppl 2003; 61: 183-194.
73. Morrison JL: Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol 2008; 35: 730-743.
74. Langley-Evans SC: Hypertension induced by fetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockage of maternal glucocorticoid synthesis. J Hypertens 1997; 15: 537-544.
75. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR: Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 1998; 101: 2174-2181.
76. Newnham JP: Is prenatal glucocorticoid administration another origin of adult disease? Clin Exp Pharmacol Physiol 2001; 28: 957-961.
77. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR: Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 1993; 341: 339-341.
78. Levitt NS, Lindsay RS, Holmes MC, Seckl JR: Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring. Neuroendocrinology 1996; 64: 412-418.
79. Lindsay RS, Lindsay RM, Edwards CR, Seckl JR: Inhibition of 11β-Hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in offspring. Hypertension 1996; 27: 1200-1204.
80. Langley-Evans SC, Phillips GJ, Benediktsson R, Gardner DS, Edwards CR, Jackson AA, Seckl JR: Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 1996; 173: 169-172.
81. Lesage J, Blondeau B, Grino M, Bréant B, Dupouy JP: Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary axis in the newborn rat. Endocrinology 2001; 142: 1692-1702.
82. Dwyer CM, Stickland NC: The effects of maternal undernutrition on maternal and fetal serum insulin-like growth factors, thyroid hormones and cortisol in the guinea pig. J Dev Physiol 1992; 18: 303-313.
83. Edwards CR, Benediktsson R, Lindsay RS, Seckl JR: Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet 1993; 341: 355-357.
84. Moore LG: Altitude-aggravated illness: examples from pregnancy and prenatal life. Ann Emerg Med 1987; 16: 965-973.
85. Bae S, Xiao Y, Li G, Casiano CA, Zhang L: Effect of maternal chronic hypoxic exposure during gestation in apoptosis in fetal heart. Am J Physiol Heart Circ Physiol 2003; 285:H983-H990.
86. Li G, Xiao Y, Estrella JL, Ducsay CA, Gilbert RD, Zhang L: Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult rat. J Soc Gynecol Invest 2003; 10: 265-274.
87. Bernstein IM, Mongeon JA, Badger GJ, Solomon L, Heil SH, Higgins ST: Maternal smoking and its association with birth weight. Obstet Gynecol 2005; 106: 986-991.
88. Jaddoe VW, Verburg BO, de Ridder MA, Hofman A, Mackenbach JP, Moll HA, Steegers EA, Witteman JC: Maternal smoking and fetal growth characteristics in different periods of pregnancy: the Generation R Study. Am J Epidemiol 2007; 165: 1207-1215.
89. Larsen LG, Clausen HV, Jønsson L: Stereologic examination of placentas from mothers who smoke during pregnancy. Am J Obstet Gynecol 2002; 186: 531-537.
90. Blake KV, Gurrin LC, Evans SF, Beilin LJ, Landau LI, Stanley FJ, Newnham JP: Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum Dev 2000; 57: 137-147.
91. Brion MJ, Leary SD, Lawlor DA, Smith GD, Ness AR: Modifiable maternal exposures and offspring blood pressure: a review of epidemiological studies of maternal age, diet, and smoking. Pediatr Res 2008; 63: 593-598.
92. Leichter J: Decreased birth weight and attainment of postnatal catch-up growth in offspring of rats exposed to cigarette smoke during gestation. Growth Dev Aging 1995; 59: 63-66.
93. Younoszai MK, Peloso J, Haworth JC: Fetal growth retardation in rats exposed to cigarette smoke during pregnancy. Am J Obstet Gynecol 1969; 104: 1207-1213.
94. Carter RC, Jacobson JL, Sokol RJ, Avison MJ, Jacobson SW: Fetal alcohol-related growth restriction from birth through young adulthood and moderating effects of maternal prepregnancy weight. Alcohol Clin Exp Res 2013; 37: 452-456.
95. Bateman DA, Ng SK, Hansen CA, Heagarty MC: The effects of intrauterine cocaine exposure in newborns. Am J Public Health 1993; 83: 190-193.
96. Ponnappa BC, Rubin E: Modeling alcohol's effects on organs in animal models. Alcohol Res Health 2000; 24: 93-104.
97. Sebert S, Sharkey D, Budge H, Symonds ME: The early programming of metabolic health: is epigenetic setting the missing link? Am J Clin Nutr 2011; 94: 1953S-1958S.
98. McMullen S, Langley-Evans SC, Gambling L, Lang C, Swali A, McArdle HJ: A common cause for a common phenotype: the gatekeeper hypothesis in fetal programming. Med Hypotheses 2012; 78: 88-94.
99. Rogers LK, Velten M: Maternal inflammation, growth retardation, and preterm birth: insights into adult cardiovascular disease. Life Sci 2011; 89: 417-421.
100. Canani RB, Costanzo MD, Leone L, Bedogni G, Brambilla P, Cianfarani S, Nobili V, Pietrobelli A, Agostoni C: Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev 2011; 24: 198-205.
101. Santos F, Dean W: Epigenetic reprogramming during early development in mammals. Reproduction 2004; 127: 643-651.
102. McKay JA, Mathers JC: Diet-induced epigenetic changes and their implications for health. Acta Physiol (Oxf) 2011; 202: 103-118.
103. Vaiman D, Gascoin-Lachambre G, Boubred F, Mondon F, Feuerstein JM, Ligi I, Grandvuillemin I, Barbaux S, Ghigo E, Achard V, Simeoni U, Buffat C: The intensity of IUGRinduced transcriptome deregulations is inversely correlated with the onset of organ function in a rat model. PLoS One 2011; 6:e21222.
104. Langley-Evans SC, Welham SJ, Jackson AA: Fetal exposure to a maternal low-protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci 1999; 64: 965-974.
105. Nuyt AM: Mechanisms underlying developmental programming of elevated blood pressure and vascular dysfunction: evidence from human studies and experimental animal models. Clin Sci (Lond) 2008; 114: 1-17.
106. Franco MC, Ponzio BF, Gomes GN, Gil FZ, Tostes R, Carvalho MH, Fortes ZB: Micronutrient prenatal supplementation prevents the development of hypertension and vascular endothelial damage induced by intrauterine malnutrition. Life Sci 2009; 85: 327-333.
107. Moritz KM, Singh RR, Probyn ME, Denton KM: Developmental programming of a reduced nephron endowment: more than just a baby's birth weight. Am J Physiol Renal Physiol 2009; 296:F1-F9.
108. Baum M: Role of the kidney in the prenatal and early postnatal programming of hypertension. Am J Physiol Renal Physiol 2010; 298:F235-F247.
109. Racasan S, Braam B, Koomans HA, Joles JA: Programming blood pressure in adult SHR by shifting perinatal balance of NO and reactive oxygen species toward NO: the inverted Barker phenomenon. Am J Physiol Renal Physiol 2005; 288:F626-F636.
110. Koeners MP, Braam B, Joles JA: Perinatal inhibition of NF-κB has long-term antihypertensive effects in spontaneously hypertensive rats. J Hypertens 2011; 29: 1160-1166.
111. Koeners MP, Wesseling S, Ulu A, Sepulveda RL, Morisseau C, Braam B, Hammock BD, Joles JA: Soluble epoxide hydrolase in the generation and maintenance of high blood pressure in spontaneously hypertensive rats. Am J Physiol Endocrinol Metab 2011; 300:E691-E698.
112. Jackson AA, Dunn RL, Marchand MC, Langley-Evans SC: Increased systolic blood pressure in rats induced by a maternal lowprotein diet is reversed by dietary supplementation with glycine. Clin Sci (Lond) 2002; 103: 633-639.
113. Torrens C, Brawley L, Anthony FW, Dance CS, Dunn R, Jackson AA, Poston L, Hanson MA: Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 2006; 47: 982-987.
114. Bogdarina I, Haase A, Langley-Evans S, Clark AJ: Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS One 2010; 5:e9237.
115. Cambonie G, Comte B, Yzydorczyk C, Ntimbane T, Germain N, Le NL, Pladys P, Gauthier C, Lahaie I, Abran D, Lavoie JC, Nuyt AM: 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.
116. Catta-Preta M, Oliveira DA, Mandarim-de-Lacerda CA, Aguila MB: Adult cardiorenal benefits from postnatal fish oil supplement in rat offspring of low-protein pregnancies. Life Sci 2006; 80: 219-229.
117. Bezerra DG, Lacerda Andrade LM, Pinto da Cruz FO, Mandarim-de-Lacerda CA: Atorvastatin attenuates cardiomyocyte loss in adult rats from protein-restricted dams. J Card Fail 2008; 14: 151-160.
118. Williams CL, Hayman LL, Daniels SR, Robinson TN, Steinberger J, Paridon S, Bazzarre T: Cardiovascular health in childhood: a statement for health professionals from the Committee on Atherosclerosis, Hypertension, and Obesity in the Young (AHOY) of the Council on Cardiovascular Disease in the Young, American Heart Association. Circulation 2002; 106: 143-160.
119. Skilton MR, Raitakari OT, Celermajer DS: High intake of dietary long-chain ω-3 fatty acids is associated with lower blood pressure in children born with low birth weight: NHANES 2003-2008. Hypertension 2013; 61: 972-976.
120. Skilton MR, Mikkila V, Wurtz P, Ala-Korpela M, Sim KA, Soininen P, Kangas AJ, Viikari JS, Juonala M, Laitinen T, Lehtimaki T, Taittonen L, Kahonen M, Celermajer DS, Raitakari OT: 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.
121. Skilton MR, Ayer JG, Harmer JA, Webb K, Leeder SR, Marks GB, Celermajer DS: Impaired fetal growth and arterial wall thickening: a randomized trial of ω-3 supplementation. Pediatrics 2012; 129:e698-e703.
122. Rossi P, Tauzin L, Marchand E, Boussuges A, Gaudart J, Frances Y: Respective roles of preterm birth and fetal growth restriction in blood pressure and arterial stiffness in adolescence. J Adolesc Health 2011; 48: 520-522.
123. Savchev S, Figueras F, Cruz-Martinez R, Illa M, Botet F, Gratacos E: Estimated weight centile as a predictor of perinatal outcome in small-for-gestational-age pregnancies with normal fetal and maternal Doppler indices. Ultrasound Obstet Gynecol 2012; 39: 299-303.
124. Cruz-Lemini M, Crispi F, Van Mieghem T, Pedraza D, Cruz-Martinez R: Acosta-Rojas R, Figueras F, Parra-Cordero M, Deprest J, Gratacos E. Risk of perinatal death in earlyonset intrauterine growth restriction according to gestational age and cardiovascular Doppler indices: a multicenter study. Fetal Diagn Ther 2012; 32: 116-122.
125. Figueras F, Gardosi J: Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 2011; 204: 288-300.
126. Berkley E, Chauhan SP, Abuhamad A: Doppler assessment of the fetus with intrauterine growth restriction. Am J Obstet Gynecol 2012; 206: 300-308.
127. Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E, Le Noble F, Ahmed A, Gratacos E: Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation 2010; 121: 2427-2436.
128. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, Figueras F, Gomez O, Sitges M, Bijnens B, Gratacos E: A fetal cardiovascular score to predict infant hypertension and arterial remodeling in intrauterine growth restriction (in preparation).
129. Crispi F, Gratacos E: Fetal cardiac function: technical considerations and potential research and clinical applications. Fetal Diagn Ther 2012; 32: 47-64.