Browse > Article
http://dx.doi.org/10.3345/kjp.2009.52.2.142

Growth and sex differentiation of children born small for gestational age  

Kim, Se Young (Department of Pediatrics, Bundang Jesaeng General Hospital)
Publication Information
Clinical and Experimental Pediatrics / v.52, no.2, 2009 , pp. 142-151 More about this Journal
Abstract
The incidence of small for gestational age (SGA) births is frequent, accounting for 2.3% to 8% of all live births. Several childhood and adult diseases are related to early postnatal growth and birth size, and 10% of children born SGA may have a short stature throughout postnatal life. Additionally, they may have abnormal growth hormone (GH)-insulin like growth factor axis, HPA axis, and gonadal function. Permanent changes are detrimental in an environment of nutritional abundance, and predispose SGA children to an array of diseases in adolescence and adulthood. Such changes may also cause premature pubarche, adrenarche, and precocious puberty. The varying results from clinical studies necessitate more prospective case control studies. Reproductive tract abnormalities and reproductive dysfunction are related to SGA births. GH treatment is required for SGA infants who do not experience catch-up growth.
Keywords
Small for gestational age; Growth; Growth hormone; Premature pubarche; Precocious puberty; Adrenarche; Reproductive function;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Grunt JA, Howard CP, Daughaday WH. Comparison of growth and somatomedin C responses following growth hormone treatment in children with small-for-date short stature, significant idiopathic short stature and hypopituitarism. Acta Endocrinol (Copenh) 1984;106:168-74
2 Johnston LB, Dahlgren J, Lger J, Gelander L, Savage MO, Czernichow P, et al. Association between insulin-like growth factor I (IGF-I) polymorphisms, circulating IGF-I, and pre- and postnatal growth in two European small for gestational age populations. J Clin Endocrinol Metab 2003; 88:4805-10   DOI   ScienceOn
3 Cianfarani S, Geremia C, Scott CD, Germani D. Growth, IGF system, and cortisol in children with intrauterine growth retardation: is catch-up growth affected by reprogramming of the hypothalamic-pituitary-adrenal axis? Pediatr Res 2002;51:94-9   DOI   ScienceOn
4 Juul A, Scheike T, Davidsen M, Gyllenborg J, Jorgensen T. Low serum insulin-like growth factor I is associated with increased risk of ischemic heart disease: a population-based case-control study. Circulation 2002;106:939-44   DOI   ScienceOn
5 Villar J, de Onis M, Kestler E, Bolanos F, Cerezo R, Bernedes H. The differential neonatal morbidity of the intrauterine growth retardation syndrome. Am J Obstet Gynecol 1990;163:151-7   ScienceOn
6 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Ferrer A, Rodriguez-Hierro F, Marcos MV, de Zegher F. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocrinol Metab 2002;87:3391-93   DOI   ScienceOn
7 Engelbregt MJT, Houdijk MEC, Popp-Snijders C, Delemarre-van de Waal HA. The effects of intrauterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res 2000;48:803-7   DOI   ScienceOn
8 Veening MA, van Weissenbruch MM, Roord JJ, de Delemarre-van Waal HA. Pubertal development in children born small for gestational age. J Pediatr Endocrinol Metab 2004; 17:1497-505
9 Francois I, de Zegher F. Adrenarche and fetal growth. Pediatr Res 1997;41:440-2   DOI   ScienceOn
10 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Marcos MV, de Zegher F. Exaggerated adrenarche and hyperinsulinism in adolescent girls born small for gestational age. J Clin Endocrinol Metab 1999;84: 4739-41   DOI   ScienceOn
11 Ib$\acute{a}{\tilde{n}}$ez L, Valls C, Potau N, Marcos MV, de Zegher F. Polycystic ovary syndrome after precocious pubarche: ontogeny of the low-birthweight effect. Clin Endocrinol (Oxf) 2001;55:667-72   DOI   ScienceOn
12 Ib$\acute{a}{\tilde{n}}$ez L, Valls C, Cols M, Ferrer A, Marcos MV, De Zegher F. Hypersecretion of FSH in infant boys and girls born small for gestational age. J Clin Endocrinol Metab 2002;87:1986-8   DOI   ScienceOn
13 Skakkebaek NE. Testicular dysgenesis syndrome: new epidemiological evidence. Int J Androl 2004;27:189-91   DOI   ScienceOn
14 Cools M, Drop SL, Wolffenbuttel KP, Oosterhuis JW, Looijenga LH. Germ cell tumors in the intersex gonad: old paths, new directions, moving frontiers. Endocr Rev 2006; 27:468-84   DOI   ScienceOn
15 Ong KK, Ahmed ML, Emmett MA, Preece MA, Dunger DB. Associations between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 2000; 320:967-71   DOI   ScienceOn
16 Albanese A, Stanhope R. GH treatment induces sustained catch-up growth in children with intrauterine growth retardation: 7-year results. Horm Res 1997;48:173   DOI   ScienceOn
17 Ranke MB, Lindberg A. Growth hormone treatment of short children born small for gestational age or with Silver- Russell syndrome: results from KIGS (Kabi International Growth Study), including the first report on final height. Acta Paediatr 1996;Suppl 417:18-26
18 Van Pareren Y, Mulder P, Houdijk M, Jansen M, Reeser M, Hokken-Koelega A. Adult height after long-term, continuous growth hormone (GH) treatment in short children born small for gestational age: results of a randomized, double- blind, dose-response GH trial. J Clin Endocrinol Metab 2003;88:3584-90   DOI   ScienceOn
19 Stettler N, Stallings VA, Troxel AB, Zhao J, Schinnar R, Nelson SE, et al. Weight gain in the first week of life and overweight in adulthood: a cohort study of European American subjects fed infant formula. Circulation 2005;111:1897- 903   DOI   ScienceOn
20 Albertson-Wikland K, Karlberg J. Natural growth in children born small for gestational age with and without catch- up growth. Acta Paediatr Scand 1994;399(suppl):64-70   DOI
21 Bay K, Asklund C, Skakkebaek NE, Andersson AM. Testicular dysgenesis syndrome: possible role of endocrine disrupters. Best Pract Res Clin Endocrinol Metab 2006;20:77-90   DOI   ScienceOn
22 Chellakooty M, Schmidt IM, Haavisto AM, Boisen KA, Damgaard IN, Mau C, et al. Inhibin A, inhibin B, follicle- stimulating hormone, luteinizing hormone, estradiol, and sex hormone-binding globulin levels in 473 healthy infant girls. J Clin Endocrinol Metab 2003;88:3515-20   DOI   ScienceOn
23 Hernandez MI, Martinez A, Capurro T, Pena V, Trejo L, Avila A, Salazar T, Asenjo S, Iniguez G, Mericq V. Comparison of clinical, ultrasonographic, and biochemical differences at the beginning of puberty in healthy girls born either small for gestational age or appropriate for gestational age: preliminary results. J Clin Endocrinol Metab 2006;91: 3377-81   DOI   ScienceOn
24 Ib$\acute{a}{\tilde{n}}$ez L, Ong K, De Zegher F, Marcos MV, Del Rio L, Dunger DB. Fat distribution in non-obese girls with and without precocious pubarche: central adiposity related to insulinaemia and androgenemia from prepuberty to postmenarche. Clin Endocrinol 2003;58:372-9   DOI   ScienceOn
25 Ib$\acute{a}{\tilde{n}}$ez L, Jaramillo A, Enriquez G, Miro E, Lopez-Bermejo A, Dinger D, De Zegher F. Polycystic ovaries after precocious pubarche: relation to prenatal growth. Hum Reprod 2007;22:395-400   DOI   ScienceOn
26 Ib$\acute{a}{\tilde{n}}$ez L, Valls C, Ong K, Dunger DB, de Zegher F. Metformin therapy during puberty delays menarche, prolongs pubertal growth, and augments adult height: a randomized study in low-birth-weight girls with early-normal onset of puberty. J Clin Endocrinol Metab 2006;91:2068-73   DOI   ScienceOn
27 Dahlgren J, Wikland KA. Final height in short children born small for gestational age treated with growth hormone. Pediatr Res 2005;57:216-22   DOI   ScienceOn
28 Abuzzahab MJ, Schneider A, Goddard A, Grigorescu F, Lautier C, Keller E, et al. Intrauterine Growth Retardation (IUGR) Study Group. IGF-I receptor mutations resulting in intrauterine and postnatal growth retardation. N Engl J Med 2003;349:2211-22   DOI   ScienceOn
29 Cianfarani S, Ladaki C, Geremia C. Hormonal regulation of postnatal growth in children born small for gestational age. Horm Res 2006;65(Suppl 3):70-4   ScienceOn
30 Albertsson-Wikland K, Karlberg J. Postnatal growth of children born small for gestational age. Acta Paediatr Suppl 1997;423:193-5   ScienceOn
31 Boonstra VH, Mulder PG, de Jong FH, Hokken-Koelega AC. Serum dehydroepiandrosterone sulfate levels and pubarche in short children born small for gestational age before and during growth hormone treatment. J Clin Endocrinol Metab 2004;89:712-7   DOI   ScienceOn
32 De Zegher F, Francois I, Boehmer AL, Saggese G, Muller J, Hiort O, et al. Androgens and fetal growth. Horm Res 1998; 50:243-4   DOI   ScienceOn
33 Toumba M, Stanhope R. Growth and metabolic parameters in children with Russell-Silver syndrome treated with growth hormone for more than 7 years. Horm Res 2006; Suppl 4:150
34 Ranke MB, Lindberg A, Cowell CT, Wikland KA, Reiter EO, Wilton P, Price DA. KIGS International Board. Prediction of response to growth hormone treatment in short children born small for gestational age: analysis of data from KIGS (Pharmacia International Growth Database). J Clin Endocrinol Metab 2003;88:125-31   DOI   ScienceOn
35 L${\acute{e}}$ger J, Oury JF, Noel M, Baron S, Benali K, Blot P, Czernichow P. Growth factors and intrauterine growth retardation. Serum growth hormone, insulin-like growth factor (IGF)-I, IGF-II, and IGF binding protein 3 levels in normally grown and growth-retarded human fetuses during the second half of gestation. Pediatr Res 1996;40:94-100   DOI   ScienceOn
36 Chellakooty M, Juul A, Boisen KA, Damgaard IN, Kai CM, Schmidt IM, et al. A prospective study of serum insulin- like growth factor I (IGF-I) and IGF-binding protein-3 in 942 healthy infants: associations with birth weight, gender, growth velocity, and breastfeeding. J Clin Endocrinol Metab 2006;91:820-6   DOI   ScienceOn
37 Ong KK, Potau N, Petry CJ, Jones R, Ness AR, Honour JW. Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J Clin Endocrinol Metab 2004;89:2647-51   DOI   ScienceOn
38 Gunnell D, Miller LL, Rogers I, Holly JM. Association of insulin-like growth factor I and insulin-like growth factor- binding protein-3 with intelligence quotient among 8- to 9- year-old children in the Avon Longitudinal Study of Parents and Children. Pediatrics 2005;116:e681-6   DOI   PUBMED   ScienceOn
39 Hokken-Koelega A, de Ridder M, van Lemmen R, den Hartog H, de Muinck Keizer-Schrama S, et al. Children born small for gestational age: do they catch up? Pediatr Res 1995;38:262-71   DOI   PUBMED   ScienceOn
40 Baron J, Klein KO, Colli MJ, Yanovski JA, Novosad JA, Bacher JD, et al. Catch-up growth after glucocorticoid excess: a mechanism intrinsic to the growth plate. Endocrinology 1994;135:1367-71   DOI   ScienceOn
41 De Zegher F, Albertsson-Wikland K, Wollmann HA, Chatelain P, Chaussain JL, Lofstrom A, Jonsson B, Rosenfeld RG. 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;85:2816-21   DOI   ScienceOn
42 Hamilton BE, Martin JA, Ventura SJ, Sutton PD, Menacker F. Births: preliminary data for 2004. Natl Vital Stat Rep 2005;54:1-17
43 Widdowson EM, McCance RA. The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proc R Soc Lond B Biol Sci 1963;158:329-42   DOI   ScienceOn
44 Mul D, Fredriks AM, van Buuren S, Oostdijk W, Verloove- Vanhorick SP, Wit JM. Pubertal development in The Netherlands 1965-1997. Pediatr Res 2001;50:479-86   DOI   ScienceOn
45 Sas T, Mulder P, Hokken-Koelega A. Body composition, blood pressure, and lipid metabolism before and during long-term growth hormone (GH) treatment in children with short stature born small for gestational age either with or without GH deficiency. J Clin Endocrinol Metab 2000;85: 3786-92   DOI   ScienceOn
46 De Zegher F, Hokken-Koelega A. Growth hormone therapy for children born small for gestational age: height gain is less dose dependent over the long term than over the short term. Pediatrics 2005;115:e458-e462   DOI   PUBMED   ScienceOn
47 Low JA, Handley-Derry MH, Burke SO, Peters RD, Pater EA, Killen HL, et al. Association of intrauterine fetal growth retardation and learning deficits at age 9 to 11 years. Am J Obstet Gynecol 1992;167:1499-505   ScienceOn
48 Moller H, Weidner IS. Epidemiology of cryptorchidism and hypospadias. Epidemiology 1999;10:352-4   DOI   PUBMED
49 Richiardi L, Askling J, Granath F, Akre O. Body size at birth and adulthood and the risk for germ-cell testicular cancer. Cancer Epidemiol Biomarkers Prev 2003;12:669-73
50 Sas T, de Waal W, Mulder P, Houdijk M, Jansen M, Reeser M, Hokken-Koelega A. 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;84:3064-70   DOI
51 Persson I, Ahlsson F, Ewald U, Tuvemo T, Qingyuan M, von Rosen D, et al. Influence of perinatal factors on the onset of puberty in boys and girls: implications for interpretation of link with risk of long term diseases. Am J Epidemiol 1999;150:747-55   PUBMED   ScienceOn
52 de Waal WJ, Hokken-Koelega AC, Stijnen T, de Muinck Keizer-Schrama SM, Drop SL. Endogenous and stimulated GH secretion, urinary GH excretion, and plasma IGF-I and IGF-II levels in prepubertal children with short stature after intrauterine growth retardation. The Dutch Working Group on Growth Hormone. Clin Endocrinol (Oxf) 1994;41:621-30   DOI   ScienceOn
53 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Francois I, de Zegher F. Precocious pubarche, hyperinsulinism, and ovarian hyperandrogenism in girls: relation to reduced fetal growth. J Clin Endocrinol Metab 1998;83:3558-62   DOI   ScienceOn
54 Wit JM, Finken MJ, Rijken M, de Zegher F. Preterm growth restraint: a paradigm that unifies intrauterine growth retardation and preterm extrauterine growth retardation and has implications for the small-for-gestational- age indication in growth hormone therapy. Pediatrics 2006;117:e793-5   DOI   PUBMED   ScienceOn
55 Ib$\acute{a}$${\tilde{n}}$ez L, Ferrer A, Ong K, Amin R, Dunger D, de Zegher F. Insulin sensitization early after menarche prevents progression from precocious pubarche to polycystic ovary syndrome. J Pediatr 2004;144:23-9   DOI   ScienceOn
56 L${\acute{e}}$ger J, Noel M, Limal JM, Czernichow P. Growth factors and intrauterine growth retardation. II. Serum growth hormone, insulin-like growth factor (IGF) I, and IGF-binding protein 3 levels in children with intrauterine growth retardation compared with normal control subjects: prospective study from birth to two years of age. Study Group of IUGR. Pediatr Res 1996;40:101-7   DOI   ScienceOn
57 Ib$\acute{a}{\tilde{n}}$ez L, Jimenez R, de Zegher F. Early puberty-menarche after precocious pubarche: relation to prenatal growth. Pediatrics 2006;117:117-21   DOI   ScienceOn
58 Francois I, de Zegher F, Spiessens C, D'Hooghe T, Vanderschueren D. Low birth weight and subsequent male subfertility. Pediatr Res 1997;42:899-901   DOI   ScienceOn
59 Verkauskiene R, Jaquet D, Deghmoun S, Chevenne D, Czernichow P, Levy-Marchal C. Smallness for gestational age is associated with persistent change in insulin-like growth factor I (IGF-I) and the ratio of IGF-I/IGF-binding protein-3 in adulthood. J Clin Endocrinol Metab 2005;90: 5672-6   DOI   ScienceOn
60 L${\acute{e}}$ger J, Levy-Marchal C, Bloch J, Pinet A, Chevenne D, Porquet D, et al. Reduced final height and indications for insulin resistance in 20 year olds born small for gestational age: regional cohort study. BMJ 1997;315:341-7   DOI   PUBMED   ScienceOn
61 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Ferrer A, Rodriguez-Hierro F, Marcos MV, de Zegher F. Anovulation in eumenorrheic, nonobese adolescent girls born small for gestational age: insulin sensitization induces ovulation, increases lean body mass, and reduces abdominal fat excess, dyslipidemia, and subclinical hyperandrogenism. J Clin Endocrinol Metab 2002;87: 5702-5   DOI   ScienceOn
62 Levine S. Maternal and environmental influences on the adrenocortical response to stress in weanling rats. Science 1967;156:258-60   DOI   PUBMED   ScienceOn
63 Woods KA, Camacho-Hubner C, Savage MO, Clark AJ. Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N Engl J Med 1996;335:1363-7   DOI   ScienceOn
64 Engelbregt MJ, van Weissenbruch MM, Popp-Snijders C, Lips P, Delemarre-van de Waal HA. Body mass index, body composition, and leptin at onset of puberty in male and female rats after intrauterine growth retardation and after early postnatal food restriction. Pediatr Res 2001;50: 474-8   DOI   ScienceOn
65 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Zampolli M, Prat N, Gussinye M, Saenger P, et al. Source localization of androgen excess in adolescent girls. J Clin Endocrinol Metab 1994;79:1778-84   DOI   ScienceOn
66 Binder G, Baur F, Schweizer R, Ranke MB. The d3-growth hormone (GH) receptor polymorphism is associated with increased responsiveness to GH in Turner syndrome and short small-for-gestational-age children. J Clin Endocrinol Metab 2006;91:659-64   DOI   ScienceOn
67 Ib$\acute{a}{\tilde{n}}$ez L, Ferrer A, Marcos MV, Hierro FR, de Zegher F. Early puberty: rapid progression and reduced final height in girls with low birth weight. Pediatrics 2000;106:1-3   DOI   PUBMED   ScienceOn
68 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Ferrer A, Rodriguez-Hierro F, Marcos MV, de Zegher F. Reduced ovulation rate in adolescent girls born small for gestational age. J Clin Endocrinol Metab 2002;87:3391-3   DOI   ScienceOn
69 Fjellestad-Paulsen A, Czernichow P, Brauner R, Bost M, Colle M, Lebouc JY, Lecornu M, Leheup B, Limal JM, Raux MC, Toublanc JE, Rappaport R. Three-year data from a comparative study with recombinant human growth hormone in the treatment of short stature in young children with intrauterine growth retardation. Acta Paediatr 1998;87: 511-7   DOI   ScienceOn
70 Giudice LC, de Zegher F, Gargosky SE, Dsupin BA, de las Fuentes L, Crystal RA, et al. Insulin-like growth factors and their binding proteins in the term and preterm human fetus and neonate with normal and extremes of intrauterine growth. J Clin Endocrinol Metab 1995;80:1548-55   DOI   ScienceOn
71 Baskin LS, Ebbers MB. Hypospadias: anatomy, etiology, and technique. J Pediatr Surg 2006;41:463-72   DOI   ScienceOn
72 Jaquet D, Gaboriau A, Czenichow P, Ley-Marchal C. Insulin resistance early in adulthood in subjects with intrauterine growth retardation. J Clin Endocrinol Metab 2000;85:1401-6   DOI   ScienceOn
73 Cicognani A, Alessandroni R, Pasini A, Pirazzoli P, Cassio A, Barbieri E, et al. Low birth weight for gestational age and subsequent male gonadal function. J Pediatr 2002;141: 376-9   DOI   ScienceOn
74 Ib$\acute{a}{\tilde{n}}$ez L, Potau N, Enriquez G, Marcos MV, de Zegher F. Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age. Hum Reprod 2003;18:1565-9   DOI   ScienceOn
75 World Health Organization 2005 World Health Statistics 2005. Geneva: World Health Organization
76 van Pareren YK, Duivenvoorden HJ, Slijper FS, Koot HM, Hokken-Koelega AC. Intelligence and psychosocial functioning during long-term growth hormone therapy in children born small for gestational age. J Clin Endocrinol Metab 2004;89:5295-302   DOI   ScienceOn
77 Barker DJ, Osmond C, Forsn TJ, Kajantie E, Eriksson JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med 2005;353:1802-9   DOI   ScienceOn
78 Cianfarani S, Maiorana A, Geremia C, Scire G, Spadoni GL, Germani D. Blood glucose concentrations are reduced in children born small for gestational age (SGA), and thyroid- stimulating hormone levels are increased in SGA with blunted postnatal catch-up growth. J Clin Endocrinol Metab 2003;88:2699-705   DOI   ScienceOn
79 Loos RJ, Beunen G, Fagard R, Derom C, Vlietinck R. Birth weight and body composition in young adult women: a prospective twin study. Int J Obes Relat Metab Disord 2002;75:676-82
80 Lger J, Limoni C, Collin D, Czernichow P. Prediction factors in the determination of final height in subjects born small for gestational age. Pediatr Res 1998;43:808-12   DOI   ScienceOn
81 English PB, Goldberg DE, Wolff C, Smith D. Parental and birth characteristics in relation to testicular cancer risk among males born between 1960 and 1995 in California (United States). Cancer Causes Control 2003;14:815-25   DOI   ScienceOn
82 Boonstra VH, Arends NJ, Stijnen T, Blum WF, Akkerman O, Hokken-Koelega AC. Food intake of children with short stature born small for gestational age before and during a randomized GH trial. Horm Res 2006;65:23-30   DOI   ScienceOn
83 Albertsson-Wikland K, Karlberg J. Natural growth in children born small for gestational age with and without catch-up growth. Acta Paediatr Suppl 1994;399:64-70; discussion, 71
84 Moller H, Skakkebaek NE. Testicular cancer and cryptorchidism in relation to prenatal factors: case-control studies in Denmark. Cancer Causes Control 1997;8:904-12   DOI   ScienceOn