Regulation of fetal growth is multifactorial and complex. Diverse factors, including intrinsic fetal conditions as well as maternal and environmental factors, can lead to intrauterine growth restriction (IUGR). The interaction of these factors governs the partitioning of nutrients and rate of fetal cellular proliferation and maturation. Although IUGR is probably a physiologic adaptive response to various stimuli, it is associated with distinct short- and long-term morbidities. Immediate morbidities include those associated with prematurity and inadequate nutrient reserve, while childhood morbidities relate to impaired maturation and disrupted organ development. Potential long-term effects of IUGR are debated and explained by the fetal programming hypothesis. In formulating a comprehensive approach to the management and follow-up of the growth-restricted fetus and infant, physicians should take into consideration the etiology, timing, and severity of IUGR. In addition, they should be cognizant of the immediate perinatal response of the growth-restricted infant as well as the childhood and long-term associated morbidities. A multi disciplinary approach is imperative, including early recognition and obstetrical management of IUGR, assessment of the growth-restricted newborn in the delivery room, possible monitoring in the neonatal intensive care unit, and appropriate pediatric follow-up. Future research is necessary to establish effective preventive, diagnostic, and therapeutic strategies for IUGR, perhaps affecting the health of future generations.
1. Hooken-Koelega ACS. Intrauterine growth retardation. Int Growth Monitor. 2001;11:2-8.
2.
2. Lin CC, Su SJ, River LP. Comparison of associated high-risk factors and perinatal outcome between symmetric and asymmetric fetal intrauterine growth retardation. Am J Obstet Gynecol. 1991;164:1535-1541.
3.
3. Menendez C, Ordi J, Ismail MR, et al. The impact of placental malaria on gestational age and birth weight. J Infect Dis. 2000;181:1740-1745.
4.
4. Crosby WM. Studies in fetal malnutrition. Am J Dis Child. 1991;145:871-876.
6. Snijders RJM, Sherrod C, Gosden CM, Nicolaides KH. Fetal growth retardation: associated malformations and chromosomal abnormalities. Am J Obstet Gynecol. 1993;168:547-555.
7.
7. Khoury MJ, Erickson D, Cordero JE, McCarthy BJ. Congenital malformations and intrauterine growth retardation: a population study. Pediatrics. 1988;82:83-90.
8.
8. Lin C-C, Santolaya-Forgas J.Current concepts of fetal growth restriction: part I. Causes, classification, and pathophysiology. Obstet Gynecol. 1998;92:1044-1055.
9.
9. Martinelli P, Grandone E, Colaizzo D, et al. Familial thrombophilia and the occurrence of fetal growth restriction. Haematologica. 2001;86:428-431.
10.
10. Heilmann L, von Tempelhoff GF, Pollow K.Antiphospholipid syndrome in obstetrics. Clin Appl Thromb Hemost. 2003;9:143-150.
11.
11. Barker DJP. Mothers, Babies and Disease in Later Life. London, UK: B.M.J. Publishing; 1994.
12.
12. Roseboom TJ, van der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJB, Bleker O.Effects of prenatal exposure to the Dutch famine on adult disease later in life: an overview. Mol Cell Endocrinol. 2001;185:93-98.
13.
13. Prentice AM, Cole TJ. Seasonal changes in growth and energy status in the Third World. Proc Nutr Soc. 1994;53:509-519.
14.
14. Schwartz ID. Failure to thrive: an old nemesis in the new millennium. Pediatr Rev. 2000;21:257-264.
15.
15. Haworth JC, Ellestad-Sayed JJ, King J, Dilling LA. Fetal growth retardation in cigarette-smoking mothers is not due to decreased maternal food intake. Am J Obstet Gynecol. 1980;137:719-723.
16.
16. Meyer MB. How does maternal smoking affect birth weight and maternal weight gain? Evidence from the Ontario Perinatal Mortality Study. Am J Obstet Gynecol. 1978;131:888-893.
17.
17. Cliver SP, Goldenberg RL, Cutter GR, Hoffman HJ, Davis RO, Nelson KG. The effect of cigarette smoking on neonatal anthropometric measurements. Obstet Gynecol. 1995;85:625-630.
18.
18. Andres RL, Day MC. Perinatal complications associated with maternal tobacco use. Semin Neonatol. 2000;5:231-241.
19.
19. Lee PA, Chernausek SD, Hokken-Koelega ACS, Czernichow P.International Small for Gestational Age Advisory Board Consensus Development Conference statement: management of short children born small for gestational age. Pediatr. 2003;111:1253-1261.
20.
20. Lim KH, Zhou Y, Janatopour M, et al. Human cytotrophoblast differentiation/invasion is abnormal in preeclampsia. Am J Pathol. 1991;151:1809-1818.
21.
21. Khong TY, De Wolf F, Robertson WB, Brosens I.Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational-age infants. Br J Obstet Gynaecol. 1986;93:1049-1059.
22.
22. Kingdom J, Huppertz B, Seaward G, Kaufmann P.Development of the placental villous tree and its consequences for fetal growth. Obstet Gynecol. 2000;92:35-43.
23.
23. Smith SC, Baker PN, Symonds EM. Increased placental apoptosis in intrauterine growth restriction. Am J Obstet Gynecol. 1997;177:1395-1401.
24.
24. Axt R, Kordina AC, Meyberg R, Reitnauer K, Mink D, Schmidt W.Immunohisto chemical evaluation of apoptosis in placentae from normal and intrauterine growth-restricted pregnancies. Clin Exp Obstet Gynecol. 1999;26:195-198.
25.
25. Baker J, Liu JP, Robertson EJ, Efstratiadis A.Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 1993;75:73-82.
26.
26. Fowden AL. The insulin-like growth factors and feto-placental growth. Placenta. 2003;24:803-812.
27.
27. Wang HS, Lim J, English J, Irvine L, Chard T.The concentration of insulin-like growth factor-I and insulin-like growth factor binding protein-1 in human umbilical cord serum at delivery: relation to fetal weight. J Endocrinol. 1991;129:459-464.
28.
28. Giudice LC, de Zegher F, Gargosky SE, Dsupin BA, de las Fuentes L, Crystal RA. Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth. J Clin Endocrinol Metab. 1995;80:1549-1555.
29.
29. Giudice LC, Martina NA, Crystal RA, Taguke S, Druzin M.Insulin-like growth factor binding protein-1 at the maternal-fetal interface and insulin-like growth factor-I, insulin-like growth factor II, and insulin-like growth factor binding protein-1 in the circulation of women in severe preeclampsia. Am J Obstet Gynecol. 1997;176:751-758.
30.
30. Woods KA, Camacho-Hubner C, Savage MO, Adrian JL. Brief report: intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med. 1996;335:1363-1367.
31.
31. Abuzzahab MJ, Schneider A, Goddard A, et al. IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med. 2003;349:2211-2222.
32.
32. Crossey PA, Pillai CC, Miell JP. Altered placental development and intrauterine growth restriction in IGF binding protein-1 transgenic mice. J Clin Invest. 2002;110:411-418.
33.
33. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A.Mice carrying null mutations of the genes encoding insulinlike growth factor I (IGF-1) and type I IGF receptor. Cell. 1993;75:59-72.
34.
34. Gluckman PD. The endocrine regulation of fetal growth in late gestation-the role of insulin like growth factors. J Clin Endocrinol Metab. 1995;80:1047-1050.
35.
35. Hay WW Jr, Catz CS, Grave GD, Yaffe SJ. Workshop summary: fetal growth—its regulation and disorders. Pediatrics. 1997;99:585-591.
36.
36. Evain-Brion D.Maternal endocrine adaptations to placental hormones in humans. Acta Paediatr Suppl. 1999;88:12-16.
37.
37. Robinson JS, Moore VM, Owens JA, McMillen IC. Origins of fetal growth restriction. Eur J Obstet Gynecol. 2000;92:13-19.
38.
38. Janatpour MJ, Utset MF, Cross JC, et al. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev Genet. 1999;25:146-157.
39.
39. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet. 2000;25:311-314.
40.
40. Schreiber J, Riethmacher-Sonnenberg E, Riethmacher D, et al. Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol Cell Biol. 2000;20:2466-2474.
41.
41. Christou H, Serdy S, Mantzoros CS. Leptin in relation to growth and developmental processes in the fetus. Semin Reprod Med. 2002;20:123-130.
42.
42. Jansson T, Powell TL. Placental nutrient transfer and fetal growth. Nutrition. 2000;16:500-502.
43.
43. Malandro MS, Beveridge MJ, Kihlberg MS, Novak DA.Effect of low-protein diet-induced intrauterine growth retardation on rat placental amino acid transport. Am J Phsyiol. 1996;271:C295-C303.
44.
44. Gilbert WM, Danielsen B.Pregnancy outcomes associated with intrauterine growth restriction. Am J Obstet Gynecol. 2003;188:1596-1601.
45.
45. Gulmezoglu M, de Onis M, Villar J.Effectiveness of interventions to prevent or treat impaired fetal growth. Obstet Gynecol Surv. 1997;52:139-148.
46.
46. Hay WW, Thureen PJ, Anderson MS. Intrauterine growth restriction. NeoReviews. 2001;2:e129-e137.
47.
47. Group EC. Randomized trial of low-dose aspirin for the prevention of maternal and fetal complications in high-risk pregnant women. Br J Obstet Gynaecol. 1996;103:39-47.
49. Bekedam DJ, Mulder EJ, Snijders RJ, Visser GH.The effects of maternal hyperoxia on fetal breathing movements, body movements and heart rate variation in growth retarded fetuses. Early Hum Dev. 1991;27:223-232.
50.
50. Arduini D, Rizzo G, Mancuso S, Romanini C.Short-term effects of maternal oxygen administration on blood flow velocity waveforms in health and growth-retarded fetuses. Am J Obstet Gynecol. 1988;159:1077-1080.
51.
51. Say L, Gulmezoglu AM, Hofmeyr GJ.Maternal oxygen administration for suspected impaired fetal growth. Cochrane Database Syst Rev. 2003;1:CD000137-CD000137.
52.
52. Ribbert LSM, van Lingen RA, Visser GHA. Continuous maternal hyperoxygenation in the treatment of early fetal growth retardation. Ultrasound Obstet Gynecol. 1991;1:331-335.
53.
53. Gulmezoglu AM, Hofmeyr GJ. Bed rest in hospital for suspected impaired fetal growth. Cochrane Database Syst Rev. 2000;2:CD000034-CD000034.
54.
54. Seeds JW, Peng T.Impaired growth and risk of fetal death: is the tenth percentile the appropriate standard?Am J Obstet Gynecol. 1998;178:658-669.
55.
55. Elimian A, Verma U, Canterino J, Shah J, Visintainer P, Tejani N.Effectiveness of antental steroids in obstetrics subgroups. Obstet Gynecol. 1999;93:174-179.
56.
56. Schaap AH, Wolf H, Bruinse HW, Smolders-De Haas H, Van Ertbruggen I, Treffers EE. Effects of antenatal corticosteroid administration on mortality and long-term morbidity in early preterm growth restricted infants. Obstet Gynecol. 2001;97:954-960.
57.
57. Dubinsky T, Lau M, Powell F, et al. Predicting poor neonatal outcome: a comparative study of noninvasive antenatal testing methods. Am J Roentgenol. 1997;168:827-831.
58.
58. Devoe LD, Jones CR. Nonstress test: evidence-based use in high-risk pregnancy. Clin Obstet Gynecol. 2002;45:986-992.
59.
59. Manning FA, Harman CR, Morrison I, Menticoglou SM, Lange IR, Johnson JM. Fetal assessment based on fetal biophysical profile scoring. IV: an analysis of perinatal morbidity and mortality. Am J Obstet Gynecol. 1990;162:703-709.
60.
60. Soothill PW, Ajayi RA, Campbell S, Nicolaides KH. Prediction of morbidity in small and normally grown fetuses by fetal heart rate variability, biophysical profile score and umbilical artery Doppler studies. Br J Obstet Gynaecol. 1993;100:742-745.
61.
61. Ferrazzi E, Vegni C, Bellotti M, Borboni A, Della Peruta S, Barbera A.Role of umbilical Doppler velocimetry in the biophysical assessment of the growth-retarded fetus: answers from neonatal morbidity and mortality. J Ultrasound Med. 1991;10:309-315.
62.
62. Karsdorp VH, van Vugt JM, van Geijn HP, et al. Clinical significance of absent or reversed end diastolic velocity waveforms in umbilical artery. Lancet. 1994;344:1664-1668.
63.
63. Neilson JP, Alfirevic Z.Doppler ultrasound for fetal assessment in high risk pregnancies. Cochrane Database Syst Rev. 2000;2:CD000073-CD000073.
64.
64. Divon MY, Ferber A.Doppler evaluation of the fetus. Clin Obstet Gynecol. 2002;45:1015-1025.
66. Ferrazzo E, Bulfamante G, Mezzopane R, Barbera A, Ghidini A, Pardi G.Uterine Doppler velocimetry and placental hypoxic-ischemic lesion in pregnancies with fetal intrauterine growth restriction. Placenta. 1999;20:389-394.
67.
67. Berg AT. Childhood neurological morbidity and its association with gestational age, intrauterine growth retardation and perinatal stress. Paediatr Perinat Epidemiol. 1988;2:229-238.
68.
68. Ley D, Laurin J, Bjerre I, Marsal K.Abnormal fetal aortic velocity waveform and minor neurological dysfunction at 7 years of age. Ultrasound Obstet Gynecol. 1996;8:152-159.
69.
69. Bekedam DJ, Visser GH, van der Zee AG, Snijders RJ, Poelmann-Weesjes G.Abnormal velocity waveforms of the umbilical artery in growth retarded fetuses: relationship to antepartum late heart rate decelerations and outcome. Early Hum Dev. 1990;24:79-89.
70.
70. Montenegro N, Santos F, Tavares E, Matias A, Barros H, Leite LP. Outcome of 88 pregnancies with absent or reversed end-diastolic blood flow in the umbilical arteries. Eur J Obstet Gynecol Reprod Biol. 1998;79:43-46.
71.
71. McParland P, Steel S, Pearce JM. The clinical implications of absent or reduced end-diastolic frequencies in umbilical artery flow velocity waveforms. Eur J Obstet Gynecol Reprod Biol. 1990;37:15-23.
72.
72. Ott WJ. Diagnosis of intrauterine growth restriction: comparison of ultrasound parameters. Am J Perinatol. 2000;19:133-137.
73.
73. Boito S, Struijk PC, Ursem NT, Stijnen T, Wladimiroff JW. Umbilical venous volume flow in the normally developing and growth-restricted human fetus. Ultrasound Obstet Gynecol. 2002;19:344-349.
74.
74. 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.
75.
75. Pardi G, Cetin I, Marconi AM, et al. Diagnostic value of blood sampling in fetuses with growth retardation. N Engl J Med. 1993;328:728-729.
76.
76. Chan FY, Pun TC, Lam P, Lam C, Lee CP, Lam YH. Fetal cerebral Doppler studies as a predictor of perinatal outcome and subsequent neurologic handicap. Obstet Gynecol. 1996;87:981-988.
77.
77. Scherjon SA, Oosting H, Smolders-DeHaas H, Zondervan HA, Kok JH. Neuro developmental outcome at three years of age after fetal “brain-sparing.” Early Hum Dev. 1998;52:67-79.
78.
78. Bahado-Singh RO, Kovanci E, Jeffres A, et al. The Doppler cerebroplacental ratio and perinatal outcome in intrauterine growth restriction. Am J Obstet Gynecol. 1999;180:750-756.
79.
79. Einspieler C, Prechtl HF, Ferrari F, Cioni G, Bos AF. The qualitative assessment of general movements in preterm, term, and young infants: review of the methodology. Early Hum Dev. 1997;50:47-60.
80.
80. Prechtl HFR. Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum Dev. 1990;23:151-158.
81.
81. Bos AF, Einspieler C, Prechtl HFR. Intrauterine growth retardation, general movements, and neuro developmental outcome: a review. Dev Med Child Neurol. 2001;43:61-68.
82.
82. Bos AF, van Loon AJ, Martjin A, van Asperen RM, Okken A, Prechtl HFR. Spontaneous motility in preterm, small for gestational age infants. II: qualitative aspects. Early Hum Dev. 1997;50:131-147.
83.
83. Harman CR, Baschat AA. Comprehensive assessment of fetal wellbeing: which Doppler tests should be performed?Curr Opin Obstet Gynecol. 2003;15:147-157.
84.
84. Williams KP, Farquaharson DF, Bebbington M, et al. Screening for fetal well-being in a high-risk pregnant population comparing the nonstress test with umbilical artery Doppler velocimetry: a randomized controlled clinical trial. Am J Obstet Gynecol. 2003;188:1366-1371.
85.
85. Owen P, Harrold AJ, Farrell T.Fetal size and growth velocity in the prediction of intrapartum caesarean section for fetal distress. Br J Obstet Gynaecol. 1997;104:445-449.
86.
86. Ounsted M, Moar V, Scott WA. Perinatal morbidity and mortality in small-for-date babies: the relative importance of some maternal factors. Early Hum Dev. 1981;5:367-375.
88. Piper JM, Xenakis EM, McFarland M, Elliott BD, Berkus MD, Langer O.Do growth-retarded premature infants have different rates of perinatal morbidity and mortality than appropriately grown premature infants?Obstet Gynecol. 1996;87:169-174.
89.
89. Shankar M, Navti O, Amu O, Konje JC. Assessment of stillbirth risk and associated risk factors in a tertiary hospital. J Obstet Gynecol. 2002;22:34-38.
90.
90. Bernstein IM, Horber JD, Badger GJ, Ohlsson A, Golan A.Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol. 2000;182:198-206.
91.
91. Kramer MS, Olivier M, McLean FH, Willis DM, Usher RH. Impact of intrauterine growth retardation and body proportionality on fetal and neonatal outcome. Pediatrics. 1990;86:707-713.
92.
92. Low JA, Austin RW, Pancham SR. Fetal asphyxia during the antepartum period in intrauterine growth retarded infants. Am J Obstet Gynecol. 1972;113:351-357.
93.
93. Dijxhoorn MJ, Visser GH, Touwen BC, Huisjes HJ. Apgar score, meconium and acidaemia at birth in small-for-gestational age infants born at term, and their relation to neonatal neurological morbidity. Br J Obstet Gynaecol. 1987;94:873-879.
94.
94. Doctor BA, O’Riordan MA, Kirchner HL, Shah D, Hack M.Perinatal correlates and neonatal outcomes of small for gestational age infants born at term gestation. Am J Obstet Gynecol. 2001;185:652-659.
95.
95. Beiner ME, Simchen MJ, Sivan E, Chetrit A, Kuint J, Schiff E.Risk factors for neonatal thrombocytopenia in preterm infants. Am J Perinatol. 2003;20:49-54.
96.
96. Ott WJ. Intrauterine growth retardation and preterm delivery. Am J Obstet Gynecol. 1993;168:1710-1715.
97.
97. Bardin C, Zelkowitz P, Papageorgiou A.Outcome of small-for-gestational age and appropriate-for-gestational age infants born before 27 weeks of gestation. Pediatrics. 1997;100:E4-E4.
98.
98. Gortner L, Wauer RR, Stock GJ, et al. Neonatal outcome in small for gestational age infants: do they really do better?J Perinat Med. 1999;27:484-489.
99.
99. Simchen MJ, Beiner ME, Strauss-Liviathan N, et al. Neonatal outcome in growth-restricted versus appropriately grown preterm infants. Am J Perinatol. 2000;17:187-192.
100.
100. Lal MK, Manktelow BN, Draper ES, Field DJ. Chronic lung disease of prematurity and intrauterine growth retardation: a population-based study. Pediatrics. 2003;111:483-487.
101.
101. Zaw W, Gagnon R, da Sliva O.The risks of adverse neonatal outcome among preterm small for gestational age infants according to neonatal versus fetal growth standards. Pediatrics. 2003;111:1273-1277.
102.
102. Tyson JE, Kennedy K, Broyles S, Rosenfeld CR. The small for gestational age infant: assessment or delayed pulmonary maturation? Increased or decreased survival?Pediatrics. 1995;95:534-538.
103.
103. Friedman SA, Schiff E, Kao I, Sibai BM. Neonatal outcome after preterm delivery for preeclampsia. Am J Obstet Gynecol. 1995;172:1785-1788.
104.
104. Bhatt AB, Tank PD, Barmade KB, Damania KR. Abnormal Doppler flow velocimetry in the growth restricted foetus as a predictor for necrotising enterocolitis. J Postgrad Med. 2002;48:182-185.
105.
105. Soregaroli M, Bonera R, Danti L, et al. Prognostic role of umbilical artery Doppler velocimetry in growth-restricted fetuses. J Matern Fetal Neonatal Med. 2002;11:199-203.
106.
106. Thorpe-Beeston JG, Nicolaides KH, Snijders RJ, Felton CV, McGregor AM. Thyroid function in small for gestational age fetuses. Obstet Gynecol. 1991;77:701-706.
107.
107. Nieto-Diaz A, Villar J, Matorras-Weinig R, Valenzuela-Ruiz P.Intrauterine growth retardation at term: association between anthropometric and endocrine parameters. Acta Obstet Gynecol Scand. 1996;75:127-131.
108.
108. Hay WWJ, Lucas A, Heird WC, et al. Workshop summary: nutrition of the extremely low birth weight infant. Pediatrics. 1999;104:1360-1368.
109.
109. Martin CR, Van Marter LJ, Allred EN, Leviton A.Growth-restricted premature infants are at increased risk for low thyroxine. Early Hum Dev. 2001;64:119-128.
110.
110. Dashe JS, McIntire DD, Lucas MJ, Leveno KJ. Effects of symmetric and asymmetric fetal growth on pregnancy outcomes. Obstet Gynecol. 2000;96:321-327.
111.
111. Williams MC, Wyble LE, O’Brien WF, Nelson RM, Schwenke JR, Casanova C.Persistent pulmonary hypertension of the neonate and asymmetric growth restriction. Obstet Gynecol. 1998;91:336-341.
112.
112. Merlet-Benichou C, Gilbert T, Muffat-Joly M, Lelievre-Pegorier M, Leroy B.Intrauterine growth retardation leads to a permanent nephron deficit in the rat. Pediatr Nephrol. 1994;8:175-180.
113.
113. Konje JC, Bell SC, Morton JJ, de Chazal R, Taylor DJ. Human fetal kidney morphometry during gestation and the relationship between weight, kidney morphometry and plasma renin concentration at birth. Clin Sci (Lond). 1996;91:169-175.
114.
114. Bassan H, Trejo LL, Kariv N, et al. Experimental intrauterine growth retardation alters renal development. Pediatr Nephrol. 2000;15:192-195.
115.
115. Bauer R, Walter B, Ihring W, Kluge H, Lampe V, Zwiener U.Altered renal function in growth-restricted newborn piglets. Pediatr Nephrol. 2000;14:735-739.
116.
116. Mackenzie HS, Lawler EV, Brenner BM. Congenital oligonephropathy: the fetal flaw in essential hypertension?Kidney Int Suppl. 1996;55:S30-S34.
117.
117. Langely-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.
118.
118. Vehaskari VM, Aviles DH, Manning J.Prenatal programming of adult hypertension in the rat. Kidney Int. 2001;59:238-245.
119.
119. Karlberg J, Jalil F, Lam B, Low L, Yeung CY. Linear growth retardation in relation to the three phases of growth. Eur J Clin Nutr. 1994;48:S25-S44.
120.
120. Leger J, Limoni C, Czernichow P.Prediction of the outcome of growth at 2 years of age in neonates with intra-uterine growth retardation. Early Hum Dev. 1997;48:211-223.
121.
121. Steward DK. Biological vulnerability in infants with failure to thrive: the association with birthweight. Child Care Health Dev. 2001;27:555-567.
122.
122. Strauss RS, Dietz WH. Effects of intrauterine growth retardation in premature infants on early childhood growth. J Pediatr. 1997;130:95-102.
123.
123. Boguszewski M, Albertsson-Wikland K, Aronsson S, et al. Growth hormone treatment of short children born small-for-gestational age: the Nordic Multicenter Trial. Acta Paediatr. 1998;87:257-263.
124.
124. Lee PA, Chernausek SD, Hooken-Koelega ACS, Czernichow P.International SGA Advisory Board Consensus Development Conference statement: management of short children born small for gestational age. Pediatrics. 2003;111:1253-1261.
125.
125. Bozzola E, Lauriola S, Messina MF, Bona G, Tinelli C, Tato L.Effect of different growth hormone dosages on the growth velocity in children born small for gestational age. Horm Res. 2004;61:98-102.
126.
126. Van Pareren Y, Mulder P, Houdijk M, Jansen M, Reeser M, Hokken-Koelega A.Adult height after long-term, continuous growth hormone treatment in short children born small for gestational age: results of a randomized, double-blind, dose response GH trial. J Clin Endocrinol Metab. 2003;88:3584-3590.
127.
127. Carel JC, Chatelain P, Rochiccioli P, Chaussain JL. Improvement in adult height after growth hormone treatment in adolescents with short stature born small for gestational age: results of a randomized controlled study. J Clin Endocrinol Metab. 2003;88:1587-1593.
128.
128. Ranke MB, Lindberg A, Cowell CT, et al. Prediction of response to growth hormone treatment in short children born small for gestational age: analysis of data from KIGS. J Clin Endocrinol Metab. 2003;88:125-131.
129.
129. de Zengher F, Albertsson-Wikland K, Wollmann HA, et al. Growth hormone treatment of short children born small for gestational age: growth responses with continuous and discontinuous regimens over 6 years. J Clin Endocrinol Metab. 2000;85:2816-2821.
130.
130. Sas T, de Waal W, Mulder P, et al. Growth hormone treatment in children with short stature born small for gestational age: 5-year results of a randomized, double-blind, dose response trial. J Clin Endocrinol Metab. 1999;84:3064-3070.
131.
131. Proceedings of the 13th Novo Nordisk Symposium on Growth Hormone and Endocrinology of the SGA/IUGR Satellite Symposium. Horm Res. 2003;59:1-143.
132.
132. Sommerfelt K, Andersson HW, Sonnander K, et al. Cognitive development of term small for gestational age children at five years of age. Arch Dis Child. 2000;83:25-30.
133.
133. Sommerfelt K, Sonnander K, Skranes J, et al. Neuropsychologic and motor function in small-for-gestation preschoolers. Pediatr Neurol. 2002;26:186-191.
134.
134. Hawdon JM, Hey E, Kolvin I, Fundudis T.Born too small: is outcome still affected?Dev Med Child Neurol. 1990;32:943-953.
135.
135. Pryor J, Silva PA, Brooke M.Growth, development and behaviour in adolescents born small-for-gestational-age. J Paediatr Child Health. 1995;31:403-407.
136.
136. Martyn CN, Gale CR, Sayer AA, Fall C.Growth in utero and cognitive function in adult life: follow up study of people born between 1920 and 1943. BMJ. 1996;312:1393-1396.
137.
137. Paz I, Laor A, Gale R, Harlap S, Stevenson DK, Seidman DS. Term infants with fetal growth restriction are not at increased risk for low intelligence scores at age 17 years. J Pediatr. 2001;138:87-91.
138.
138. O’Keefe MJ, O’Callaghan M, Williams GM, Najman JK, Bor W.Learning, cognitive, and attentional problems in adolescents born small for gestational age. Pediatrics. 2003;112:301-307.
139.
139. Blair E, Stanley F.Intrauterine growth and spastic cerebral palsy. Am J Obstet Gynecol. 1990;162:229-237.
140.
140. Uvebrant P, Hagberg G.Intrauterine growth in children with cerebral palsy. Acta Paediatr. 1992;81:407-412.
141.
141. Topp M, Langhoff-Roos J, Uldall P, Kristensen J.Intrauterine growth and gestational age in preterm infants with cerebral palsy. Early Hum Dev. 1996;44:27-36.
142.
142. Harvey D, Prince J, Burton J, Parkinson C, Campbell S.Abilities of children who were small-for-gestational-age babies. Pediatrics. 1982;69:296-300.
143.
143. Parkinson CE, Wallis S, Harvey D.School achievement and behavior of children who were small-for-dates at birth. Dev Med Child Neurol. 1981;23:41-50.
144.
144. Sung IK, Vohr B, Oh W.Growth and neuro developmental outcome of very low birth weight infants with intrauterine growth retardation: comparison with control subjects matched by birth weight and gestational age. J Pediatr. 1993;123:618-624.
145.
145. Wienerroither H, Steinder H, Tomaselli J, Lobendanz M, Thun-Hohenstein L.Intrauterine blood flow and long-term intellectual, neurologic, and social development. Obstet Gynecol. 2001;97:449-453.
146.
146. Vossbeck S, de Camargo OK, Grab D, Bode H, Pohlandt F.Neonatal and neuro developmental outcome in infants born before 30 weeks of gestation with absent or reversed end-diastolic flow velocities in the umbilical artery. Eur J Pediatr. 2001;160:128-134.
147.
147. Berg AT. Indices of fetal growth retardation, perinatal hypoxia-related factors and childhood neurological morbidity. Early Hum Dev. 1989;19:271-283.
148.
148. Low JA, Handley-Derry MH, Burke SO, et al. Association of intrauterine fetal growth retardation and learning deficits at age 9 and 11 years. Am J Obstet Gynecol. 1992;167:1499-1505.
149.
149. Sommerfelt K, Troland K, Ellertsen B, Markestad T.Behavioral problems in low-birthweight preschoolers. Dev Med Child Neurol. 1996;38:927-940.
150.
150. Halsey CL, Collin MF, Anderson CL. Extremely low-birth-weight children and their peers: a comparison of school-age outcomes. Arch Pediatr Adolesc Med. 1996;150:790-794.
151.
151. Goldenberg R, Hack M, Grantham-McGregor SM, Schurch B.Report of the IDECG/IUNS Working Group on IUGR effects on neurological, sensory, cognitive, and behavioral function. Eur J Clin Nutr. 1998;52:S100-S101.
152.
152. Buck GM, Cookfair DL, Michalek AM, et al. Intrauterine growth retardation and risk of sudden infant death syndrome (SIDS). Am J Epidemiol. 1989;129:874-884.
153.
153. Wierenga H, Brand R, Geudeke T, van Geijn HP, van der Harten H, Verloove-Vanhorick SP. Prenatal risk factors for cot death in very preterm and small for gestational age infants. Early Hum Dev. 1990;23:15-26.
154.
154. Filiano JJ, Kinney HC. A perspective on neuropathologic findings in victims of the sudden infant death syndrome: the triple-risk model. Biol Neonate. 1994;65:194-197.
155.
155. Harding R, Tester ML, Moss TJ, et al. Effects of intrauterine growth restriction on the control of breathing and lung development after birth. Clin Exp Pharm Phys. 2000;27:114-119.
156.
156. Rona RJ, Gulliford MC, Chinn S.Effects of prematurity and intrauterine growth on respiratory health and lung function in childhood. BMJ. 1993;306:817-820.
157.
157. Barker DJP, Osmond C.Infant mortality, childhood nutrition, and ischeamic heart disease in England and Wales. Lancet. 1986;1:1077-1081.
158.
158. Barker DJP. The developmental origins of adult disease. Eur J Epidemiol. 2003;18:733-736.
159.
159. 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;360:659-665.
160.
160. 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.
161.
161. Hinchliffe SA, Lynch MR, Sargent PH, Howard CV, Van Velzen D.The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynaecol. 1992;99:296-301.
162.
162. Manalich R, Reyes L, Herrera M, Melendi C, Fundora I.Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int. 2000;58:770-773.
163.
163. Brenner BM, Chertow GM. Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kid Dis. 1994;23:171-175.
164.
164. Hales CN, Ozanne SE. For debate: fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure. Diabetologia. 2003;46:1013-1019.
165.
165. Hales CN, Ozanne SE. The dangerous road to catch-up growth. J Physiol. 2003;547:5-10.
166.
166. Ozanne SE, Olsen GS, Hansen LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003;177:235-241.
167.
167. Sparre T, Reusens B, Cherif H, et al. Intrauterine programming of fetal islet gene expression in rats: effects of maternal protein restriction during gestation revealed by proteome analysis. Diabetologia. 2003;46:1497-1511.
168.
168. Eriksson JG, Forsen T, Tuomilehto J, Osmond C, Barker DJ. Early adiposity rebound in childhood and risk of type 2 diabetes in adult life. Diabetologia. 2003;46:190-194.
169.
169. Singhal A, Fewtrell M, Cole TJ, Lucas A.Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet. 2003;361:1089-1097.
170.
170. Eriksson JG, Lindi V, Uusitupa M, et al. The effects of the Pro12Ala polymorphism of the peroxisome proliferator activated receptor-g2 gene on insulin sensitivity and insulin metabolism interact with size at birth. Diabetes. 2002;51:2321-2324.
171.
171. Davis L, Roullet JB, Thornburg KL, Shokry M, Hohimer AR, Giraud GD. Augmentation of coronary conductance in adult sheep made anaemic during fetal life. J Physiol. 2003;547:53-59.
172.
172. Broberg CS, Giraud GD, Schultz JM, Thornburg KL, Hohimer AR, Davis LE. Fetal anemia leads to augmented contractile response to hypoxic stress in adulthood. Am J Physiol. 2003;285:R649-R655.
173.
173. Philip AGS. Classification by birthweight and gestational age. NeoReviews. 2003;4:e91-e93.
174.
174. Cetin I, Marconi AM, Baggiani AM, et al. In vivo placental transport of glycine and leucine in human pregnancies. Pediatr Res. 1995;37:571-575.
175.
175. Lok F, Owens JA, Mundy L, Robinson JS, Owens PC. Insulin-like growth factor I promotes growth selectively in fetal sheep in late gestation. Am J Physiol. 1996;270:R1148-R1155.
