Korean J Pediatr Search

CLOSE


Korean J Pediatr > Volume 59(1); 2016 > Article
Cho and Suh: Catch-up growth and catch-up fat in children born small for gestational age

Abstract

Infants born small for gestational age (SGA) are at increased risk of perinatal morbidity, persistent short stature, and metabolic alterations in later life. Recent studies have focused on the association between birth weight (BW) and later body composition. Some reports suggest that fetal nutrition, as reflected by BW, may have an inverse programing effect on abdominal adiposity later in life. This inverse association between BW and abdominal adiposity in adults may contribute to insulin resistance. Rapid weight gain during infancy in SGA children seemed to be associated with increased fat mass rather than lean mass. Early catch-up growth after SGA birth rather than SGA itself has been noted as a cardiovascular risk factor in later life. Children who are born SGA also have a predisposition to accumulation of fat mass, particularly intra-abdominal fat. It is not yet clear whether this predisposition is due to low BW itself, rapid postnatal catch-up growth, or a combination of both. In this report, we review the published literature on central fat accumulation and metabolic consequences of being SGA, as well as the currently popular research area of SGA, including growth aspects.

Introduction

Infants born small for gestational age (SGA) are at increased risk of perinatal morbidity, persistent short stature and metabolic alterations in later life1). Although approximately 70%–90% of SGA infants show catch-up growth during the first years of life, individuals born SGA may continue to have a short stature in adulthood2,3). The fetal origins hypothesis states that SGA children have a higher risk of developing metabolic syndrome (MetS) later in adult life4). There have been many recent reports of metabolic alterations in SGA children in later life, even in adolescence. In this report, we reviewed the published literature and the currently popular research area of SGA.

Definition and causes of SGA

The definition of SGA has been variably set at the 3rd or 10th percentile, or at less than –2 standard deviations (SDs) from the mean. Weight below the 10th percentile is used by neonatologists because it captures those at risk of perinatal morbidity and mortality5). The incidence of SGA births in each country is not exactly known, because birth anthropometric data and gestational age are rarely recorded in most national databases6). The prevalence of SGA (11.4%) in the 5th Korean National Health and Nutrition Examination Survey 2010–20117), conducted on Korean adolescents, is similar to that of other countries, including Japan, Norway, and the United States, using weight below the 10th percentile to define SGA8,9,10).
Fetal growth depends on oxygen supply and blood vessel formation in the placenta as well as endocrine regulation of cellular expansion. The etiology of most SGA births remains unknown; however, several factors involving the fetus and placenta have been evaluated6,11,12,13). Maternal factors include poor nutrition, chronic disease and infections6,13,14), as well as potential environmental toxins (e.g., smoking and alcohol consumption). Paternal factors including diabetes may also contribute to being born SGA15). Among these causes, lack of nutritional supply to the fetus is believed to be the primary cause of reduced fetal growth16).

Postnatal growth of SGA

Between 3% and 10% of all live neonates worldwide are born SGA. The majority of infants born SGA experience catch-up growth in the first few months, followed by a normal pattern of development. Catch-up growth of infants born SGA mainly occurs from 6 months to 2 years and approximately 85% of SGA children will have caught up by age 2 years2,17,18,19). SGA children are at high-risk of developing permanent short stature, and 10% continue to fall below the 3rd percentile of height into adulthood20). We reported significant positive relationships between birth weight (BW) for gestational age and the current height-standard deviation score (SDS) and weight-SDS in adolescents aged 10–18 years in Korea7). The growth hormone/insulin-like growth factor (GH/IGF) axis has a major role in promoting human fetal growth, as well as growth during infancy and childhood. Classic GH deficiency is rare in the SGA population6). Abnormalities in the GH/IGF axis have been reported in SGA children. Mean serum levels of IGF1 and IGF-binding protein-3 of SGA children at birth are known to be around 1 SD lower than for appropriate for gestational age (AGA) births. However, the serum levels of IGF1 of SGA children at later ages are contradictory. Some reports showed that SGA children have a higher IGF1 level than AGA children after catch-up growth21,22). However, another report suggests a persistent lower IGF1 level in SGA children23). Recently, IGF1 gene deletions, point mutations, and polymorphisms have been described in populations born SGA24,25). These long-term abnormalities of IGF1 in SGA may be implicated in the association with metabolic disease in later life22,23,26).
General postnatal growth pattern can be divided into three phases: infancy, childhood, and puberty. Failure of growth in any of these phases can reduce growth potential and eventually cause adult short stature27,28). SGA children who fail to catch up do not reach their target height range, and remain short throughout childhood and into adulthood2,17,29,30). The mechanisms of catch-up growth remain unclear. The finding of higher basal GH levels suggested hypersecretion as a factor in early catch-up growth31). On the other hand, BW, birth length, gestational age, and midparental height have also been identified as factors influencing catch-up growth17,18,29).
Puberty in SGA tends to have a normal or slightly early onset30,32), although age at menarche seems to be within the normal range32). Small variations from the normal pubertal growth pattern have been reported33,34), but overall the final height prognosis in short children born SGA does not seem to be altered by the time of onset and/or progress of puberty29,33,34). Being born SGA without adequate postnatal catch-up growth is a condition responsible for short stature in childhood and reduced adult height35); for adults with short stature, 22% were reported to be born SGA, if based on birth length2).

Insulin resistance and metabolic consequences of SGA

MetS is often referred to as the combination of central obesity, impaired glucose tolerance or overt type 2 diabetes mellitus, dyslipidemia, and hypertension36). For children, there are slight differences in the definition and basic criteria for MetS (Table 1)5). Excess visceral fat is strongly associated with free fatty acid (FFA) release and high FFA concentration can induce insulin resistance in muscle and the liver. Visceral adipose tissue is also prone to inflammation and inflammatory cytokine production, which contributes impairment in insulin signaling.
The "thrifty phenotype" hypothesis suggests that the fetus adapts to an adverse intrauterine environment giving rise to changes in insulin sensitivity and a predisposition to type 2 diabetes in later life4). The "fetal salvage" hypothesis also indicates the association between abnormal insulin sensitivity and a characteristic of subjects with intrauterine growth retardation37). In 1962, Neel38) suggested that genes promote survival and growth of the fetus in poor prenatal environments and induce the development of insulin resistance, given sufficient nutritional support after birth. Recently, several candidate genes have been regarded as contributing factors for developing insulin resistance39). Vu-Hong et al.40) showed the interaction between severe fetal growth restriction and the insulin gene variable number of tandem repeats locus, which were associated with insulin resistance in young adults born SGA.
Recent studies have also focused on the association between BW and later body composition (Table 2). Some reports suggest that fetal nutrition, as reflected by BW, may have an inverse programing effect on abdominal adiposity later in life. This inverse association between BW and abdominal adiposity in adults may contribute to insulin resistance. Byberg et al.41) reported that BW has a negative association with hypertension, insulin resistance and trunk fat in later life. Laitinen et al.42) suggest SGA itself is a risk factor for central obesity in female adults. Vaag et al.43) indicate that being born SGA and with low BW is associated with type 2 diabetes in a nongenetic manner, and programming of muscle insulin action and signaling represents an early mechanism responsible for this association. Rasmussen et al.44) report that low BW subjects had a significantly higher total abdominal fat mass and a higher proportion of trunk and abdominal fat mass but less leg fat relative to total fat mass. In spite of similar body mass index (BMI) and body composition, girls born SGA had a higher leptin level and insulinogenic index than AGA girls. These data suggest that low BW affects insulin resistance even in puberty45). Szalapska et al.46) observed a high frequency of MetS in Polish SGA children aged 5 to 9 years. The association of low BW was found to be significantly associated with such components of MetS as systolic blood pressure, diastolic blood pressure, triglycerides, insulin level, and insulin resistance, even in healthy Japanese high school girls47).
Children born large for gestational age (LGA) seem to have a larger body size but harmonic body composition and adequate body fat distribution. Children born SGA had higher central adiposity regardless of their body size48). Being SGA at birth could program excess abdominal fat deposition in children, which is a major component in the clustering of cardiovascular disease risk factors defining MetS.
Labayen et al.49) reported that impaired fetal growth, measured by BW, may be related to central fat distribution in Spanish boys. Labayen et al.36) also reported that adjusted BW z-score was inversely associated with central adiposity in male and female Spanish adolescents. Adjusted BW z-score was inversely associated with central adiposity, negatively associated with abdominal regional fat mass index independent of total fat mass, and inversely associated with the subscapular to triceps skinfolds ratio in boys50,51). In 2014, American children with intrauterine growth restriction were reported to have higher waist circumference, higher insulin, higher homeostasis model assessment for insulin resistance (HOMA-IR), and lower adiponectin levels in adolescence, independent of other childhood and maternal factors52).
However many previous reports showed an inconsistent relationship between fat mass and BW. Choi et al.53) suggest that the association between low BW and insulin resistance is not mediated by abdominal obesity. Low BW was not associated with MetS in early adulthood8). Size at birth was positively associated with adult height and weight, but shows only weak association with BMI, and is not associated with waist/hip ratio when adjusted for socio-economic and lifestyle factors54). In data we previously reported, the prevalence of MetS was 1.2% and there were no differences in MetS components between SGA and AGA or LGA groups in 792 Korean adolescents7). Therefore, further studies are needed on the relationship between being born with low BW and metabolic risk.

Catch-up growth after SGA and central fat distribution in later life

Rapid weight gain during SGA infancy seemed to be associated with increased fat mass rather than lean mass55,56,57,58,59) (Table 3). Early catch-up growth after SGA birth rather than SGA itself has been noted as a cardiovascular risk factor in later life60).
Stevens et al.61) reported that catch-up SGA children are at high risk of cardiometabolic disease. Deng et al.62) report that HOMA-IR of term catch-up SGA children is higher than term AGA children. In a study on mice, forced catch-up growth after fetal protein restriction was reported to influence the adipose gene expression program63).
During recovery from wasting diseases and protein-energy malnutrition in children and adults, fat mass is accumulated much faster than muscle mass. These phenomena also occurred during SGA catch-up growth. Dulloo et al.64) noted that the insulin resistance seen in SGA catch-up growth is related to aforementioned phenomenon. This thrifty "catch-up fat phenotype" may be caused by complex interactions between earlier reprograming and a modern lifestyle characterized by nutritional abundance and low physical activity. The development of this catch-up fat phenotype is a central event that predisposes SGA children with catch-up growth to abdominal obesity, type 2 diabetes, and cardiovascular disease65).
Ong et al.66) showed that SGA children who showed catch-up growth between 0 and 2 years of age were fatter and had more central fat distribution at 5 years than other children. In SGA children, total and abdominal fat mass at 4 years was more closely related to the rate of weight gain between 0 and 2 years than between 2 and 4 years67). Leunissen et al.68) also report that weight gain during childhood is an important determinant of body composition in young adulthood, whereas birth size is less important. Kerkhof et al.69) demonstrates that a higher gain in weight for length in the first 3 months of life is associated with a higher prevalence of MetS at 21 years, whereas low BW is not. Wells et al.70) reported associations between rapid weight gain and fat mass in Brazilian adolescents.

Conclusions

SGA children have a tendency to accumulate intra-abdominal fat mass. It is not clear whether this is due to low BW itself, rapid postnatal catch-up growth, or a combination of both56). Catch-up growth has certain advantages in improved neurodevelopment, enhanced immune function, and final adult height. However, there are also certain disadvantages such as MetS, type 2 diabetes mellitus, cardiovascular disease, increased fat mass, and obesity. Therefore, early feeding of SGA children requires particular caution. In clinical practice, excess weight gain in SGA children should be prevented. Growth of SGA children should be measured every 3 months in the first year, and regular assessment of catch-up fat is necessary. Further studies are needed to prevent the complications of SGA as well as to develop and promote feeding guidelines for SGA children.

Conflicts of interest

Conflicts of interest:
No potential conflict of interest relevant to this article was reported.

References

1. Clayton PE, Cianfarani S, Czernichow P, Johannsson G, Rapaport R, Rogol A. Management of the child born small for gestational age through to adulthood: a consensus statement of the International Societies of Pediatric Endocrinology and the Growth Hormone Research Society. J Clin Endocrinol Metab 2007;92:804–810.
crossref pmid
2. Karlberg J, Albertsson-Wikland K. Growth in full-term small-for-gestational-age infants: from birth to final height. Pediatr Res 1995;38:733–739.
crossref pmid
3. Westwood M, Kramer MS, Munz D, Lovett JM, Watters GV. Growth and development of full-term nonasphyxiated small-for-gestational-age newborns: follow-up through adolescence. Pediatrics 1983;71:376–382.
pmid
4. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 1992;35:595–601.
crossref pmid
5. Hernandez MI, Mericq V. Metabolic syndrome in children born small-for-gestational age. Arq Bras Endocrinol Metabol 2011;55:583–589.
crossref pmid
6. Saenger P, Czernichow P, Hughes I, Reiter EO. Small for gestational age: short stature and beyond. Endocr Rev 2007;28:219–251.
crossref pmid
7. Cho WK, Jung IA, Suh BK. Crrent growth status and metabolic parameters of Korean adolescents born small for gestational age: results from the Korea National Health and Nutrition Examination Surveys (KNHANES) 2010-2011. Pediatr Int 2014;56:344–348.
crossref pmid
8. Euser AM, Dekker FW, Hallan SI. Intrauterine growth restriction: no unifying risk factor for the metabolic syndrome in young adults. Eur J Cardiovasc Prev Rehabil 2010;17:314–320.
pmid
9. Kaneshi T, Yoshida T, Ohshiro T, Nagasaki H, Asato Y, Ohta T. Birthweight and risk factors for cardiovascular diseases in Japanese schoolchildren. Pediatr Int 2007;49:138–143.
crossref pmid
10. Hediger ML, Overpeck MD, Maurer KR, Kuczmarski RJ, McGlynn A, Davis WW. Growth of infants and young children born small or large for gestational age: findings from the Third National Health and Nutrition Examination Survey. Arch Pediatr Adolesc Med 1998;152:1225–1231.
pmid
11. Pollack RN, Divon MY. Intrauterine growth retardation: definition, classification, and etiology. Clin Obstet Gynecol 1992;35:99–107.
crossref pmid
12. Chernausek SD. Mendelian genetic causes of the short child born small for gestational age. J Endocrinol Invest 2006;29(1 Suppl): 16–20.
crossref pmid
13. Clausson B, Cnattingius S, Axelsson O. Preterm and term births of small for gestational age infants: a population-based study of risk factors among nulliparous women. Br J Obstet Gynaecol 1998;105:1011–1017.
crossref pmid
14. Lee PA, Chernausek SD, Hokken-Koelega AC, Czernichow P. International Small for Gestational Age Advisory Board. International Small for Gestational Age Advisory Board consensus development conference statement: management of short children born small for gestational age, April 24-October 1, 2001. Pediatrics 2003;111(6 Pt 1): 1253–1261.
crossref pmid
15. Lindsay RS, Dabelea D, Roumain J, Hanson RL, Bennett PH, Knowler WC. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes 2000;49:445–449.
crossref pmid
16. Gluckman PD, Harding JE. The physiology and pathophysiology of intrauterine growth retardation. Horm Res 1997;48(Suppl 1): 11–16.

17. Hokken-Koelega AC, De Ridder MA, Lemmen RJ, Den Hartog H, De Muinck Keizer-Schrama SM, Drop SL. Children born small for gestational age: do they catch up? Pediatr Res 1995;38:267–271.
crossref pmid
18. Karlberg J, Albertsson-Wikland K, Kwan CW, Chan FY. Early spontaneous catch-up growth. J Pediatr Endocrinol Metab 2002;15(Suppl 5): 1243–1255.
pmid
19. Leger 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;315:341–347.
crossref pmid pmc
20. Argente J, Mehls O, Barrios V. Growth and body composition in very young SGA children. Pediatr Nephrol 2010;25:679–685.
crossref pmid
21. Iñiguez G, Ong K, Bazaes R, Avila A, Salazar T, Dunger D, et al. Longitudinal changes in insulin-like growth factor-I, insulin sensitivity, and secretion from birth to age three years in small-for-gestational-age children. J Clin Endocrinol Metab 2006;91:4645–4649.
crossref pmid
22. Tenhola S, Halonen P, Jaaskelainen J, Voutilainen R. Serum markers of GH and insulin action in 12-year-old children born small for gestational age. Eur J Endocrinol 2005;152:335–340.
crossref pmid
23. Albertsson-Wikland K, Boguszewski M, Karlberg J. Children born small-for-gestational age: postnatal growth and hormonal status. Horm Res 1998;49(Suppl 2): 7–13.
crossref
24. Johnston LB, Dahlgren J, Leger 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;88:4805–4810.
crossref pmid
25. Arends N, Johnston L, Hokken-Koelega A, van Duijn C, de Ridder M, Savage M, et al. Polymorphism in the IGF-I gene: clinical relevance for short children born small for gestational age (SGA). J Clin Endocrinol Metab 2002;87:2720
crossref pmid
26. 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;88:2699–2705.
crossref pmid
27. Botero D, Lifshitz F. Intrauterine growth retardation and long-term effects on growth. Curr Opin Pediatr 1999;11:340–347.
crossref pmid
28. Brook CG, Hindmarsh PC, Stanhope R. Growth and growth hormone secretion. J Endocrinol 1988;119:179–184.
crossref pmid
29. Leger 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;43:808–812.
crossref pmid
30. Albertsson-Wikland K, Karlberg J. Postnatal growth of children born small for gestational age. Acta Paediatr Suppl 1997;423:193–195.
pmid
31. Leger 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;40:101–107.
crossref pmid
32. Hokken-Koelega AC. Timing of puberty and fetal growth. Best Pract Res Clin Endocrinol Metab 2002;16:65–71.
crossref pmid
33. Lazar L, Pollak U, Kalter-Leibovici O, Pertzelan A, Phillip M. Pubertal course of persistently short children born small for gestational age (SGA) compared with idiopathic short children born appropriate for gestational age (AGA). Eur J Endocrinol 2003;149:425–432.
crossref pmid
34. Vicens-Calvet E, Espadero RM, Carrascosa A. Spanish SGA Collaborative Group. Small for gestational age. longitudinal study of the pubertal growth spurt in children born small for gestational age without postnatal catch-up growth. J Pediatr Endocrinol Metab 2002;15:381–388.
pmid
35. Jaquet D, Collin D, Levy-Marchal C, Czernichow P. Adult height distribution in subjects born small for gestational age. Horm Res 2004;62:92–96.
pmid
36. Labayen I, Moreno LA, Ruiz JR, Gonzalez-Gross M, Warnberg J, Breidenassel C, et al. Small birth weight and later body composition and fat distribution in adolescents: the Avena study. Obesity (Silver Spring) 2008;16:1680–1686.
crossref pmid
37. Hofman PL, Cutfield WS, Robinson EM, Bergman RN, Menon RK, Sperling MA, et al. Insulin resistance in short children with intrauterine growth retardation. J Clin Endocrinol Metab 1997;82:402–406.
pmid
38. NEEL JV. Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"? Am J Hum Genet 1962;14:353–362.
pmid pmc
39. Dunger DB, Ong KK, Huxtable SJ, Sherriff A, Woods KA, Ahmed ML, et al. Association of the INS VNTR with size at birth. ALSPAC Study Team. Avon Longitudinal Study of Pregnancy and Childhood. Nat Genet 1998;19:98–100.
crossref pmid
40. Vu-Hong TA, Durand E, Deghmoun S, Boutin P, Meyre D, Chevenne D, et al. The INS VNTR locus does not associate with smallness for gestational age (SGA) but interacts with SGA to increase insulin resistance in young adults. J Clin Endocrinol Metab 2006;91:2437–2440.
crossref pmid
41. Byberg L, McKeigue PM, Zethelius B, Lithell HO. Birth weight and the insulin resistance syndrome: association of low birth weight with truncal obesity and raised plasminogen activator inhibitor-1 but not with abdominal obesity or plasma lipid disturbances. Diabetologia 2000;43:54–60.
crossref pmid
42. Laitinen J, Pietilainen K, Wadsworth M, Sovio U, Jarvelin MR. Predictors of abdominal obesity among 31-y-old men and women born in Northern Finland in 1966. Eur J Clin Nutr 2004;58:180–190.
crossref pmid
43. Vaag A, Jensen CB, Poulsen P, Brons C, Pilgaard K, Grunnet L, et al. Metabolic aspects of insulin resistance in individuals born small for gestational age. Horm Res 2006;65(Suppl 3): 137–143.
pmid
44. Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H, Poulsen P, et al. Altered fat tissue distribution in young adult men who had low birth weight. Diabetes Care 2005;28:151–153.
crossref pmid
45. Martínez-Aguayo A, Capurro T, Pena V, Iniguez G, Hernandez MI, Avila A, et al. Comparison of leptin levels, body composition and insulin sensitivity and secretion by OGTT in healthy, early pubertal girls born at either appropriate- or small-for-gestational age. Clin Endocrinol (Oxf) 2007;67:526–532.
pmid
46. Szalapska M, Stawerska R, Borowiec M, Mlynarski W, Lewinski A, Hilczer M. Metabolic syndrome components among children born small for gestational age: analysis of the first decade of life. Pediatr Endocrinol Diabetes Metab 2010;16:270–276.
pmid
47. Mori M, Mori H, Yamori Y, Tsuda K. Low birth weight as cardiometabolic risk in Japanese high school girls. J Am Coll Nutr 2012;31:39–44.
crossref pmid
48. Dolan MS, Sorkin JD, Hoffman DJ. Birth weight is inversely associated with central adipose tissue in healthy children and adolescents. Obesity (Silver Spring) 2007;15:1600–1608.
crossref pmid
49. Labayen I, Moreno LA, Blay MG, Blay VA, Mesana MI, Gonzalez-Gross M, et al. Early programming of body composition and fat distribution in adolescents. J Nutr 2006;136:147–152.
crossref pmid
50. Labayen I, Ruiz JR, Vicente-Rodriguez G, Turck D, Rodriguez G, Meirhaeghe A, et al. Early life programming of abdominal adiposity in adolescents: The HELENA Study. Diabetes Care 2009;32:2120–2122.
crossref pmid pmc
51. Labayen I, Ortega FB, Ruiz JR, Sjostrom M. Birth weight and subsequent adiposity gain in Swedish children and adolescents: a 6-year follow-up study. Obesity (Silver Spring) 2012;20:376–381.
crossref pmid
52. Crume TL, Scherzinger A, Stamm E, McDuffie R, Bischoff KJ, Hamman RF, et al. The long-term impact of intrauterine growth restriction in a diverse U.S. cohort of children: the EPOCH study. Obesity (Silver Spring) 2014;22:608–615.
crossref pmid
53. Choi CS, Kim C, Lee WJ, Park JY, Hong SK, Lee MG, et al. Association between birth weight and insulin sensitivity in healthy young men in Korea: role of visceral adiposity. Diabetes Res Clin Pract 2000;49:53–59.
crossref pmid
54. Pilgaard K, Færch K, Poulsen P, Larsen C, Andersson EA, Pisinger C, et al. Impact of size at birth and prematurity on adult anthropometry in 4744 middle-aged Danes: The Inter99 study. J Dev Orig Health Dis 2010;1:319–328.
crossref pmid
55. Howe LD, Chaturvedi N, Lawlor DA, Ferreira DL, Fraser A, Davey Smith G, et al. Rapid increases in infant adiposity and overweight/obesity in childhood are associated with higher central and brachial blood pressure in early adulthood. J Hypertens 2014;32:1789–1796.
crossref pmid pmc
56. Druet C, Ong KK. Early childhood predictors of adult body composition. Best Pract Res Clin Endocrinol Metab 2008;22:489–502.
crossref pmid
57. Chomtho S, Wells JC, Williams JE, Davies PS, Lucas A, Fewtrell MS. Infant growth and later body composition: evidence from the 4-component model. Am J Clin Nutr 2008;87:1776–1784.
crossref pmid
58. Okada T, Takahashi S, Nagano N, Yoshikawa K, Usukura Y, Hosono S. Early postnatal alteration of body composition in preterm and small-for-gestational-age infants: implications of catch-up fat. Pediatr Res 2015;77:136–142.
crossref pmid
59. Tinnion R, Gillone J, Cheetham T, Embleton N. Preterm birth and subsequent insulin sensitivity: a systematic review. Arch Dis Child 2014;99:362–368.
crossref pmid
60. Kelishadi R, Haghdoost AA, Jamshidi F, Aliramezany M, Moosazadeh M. Low birthweight or rapid catch-up growth: which is more associated with cardiovascular disease and its risk factors in later life? A systematic review and cryptanalysis. Paediatr Int Child Health 2015;35:110–123.
crossref pmid
61. Stevens A, Bonshek C, Whatmore A, Butcher I, Hanson D, De Leonibus C, et al. Insights into the pathophysiology of catch-up compared with non-catch-up growth in children born small for gestational age: an integrated analysis of metabolic and transcriptomic data. Pharmacogenomics J 2014;14:376–384.
crossref pmid
62. Deng HZ, Li YH, Su Z, Ma HM, Huang YF, Chen HS, et al. Association between height and weight catch-up growth with insulin resistance in pre-pubertal Chinese children born small for gestational age at two different ages. Eur J Pediatr 2011;170:75–80.
crossref pmid
63. Bol VV, Delattre AI, Reusens B, Raes M, Remacle C. Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 2009;297:R291–R299.
crossref pmid
64. Dulloo AG, Jacquet J, Seydoux J, Montani JP. The thrifty 'catch-up fat' phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome. Int J Obes (Lond) 2006;30(Suppl 4): S23–S35.
crossref pmid
65. Dulloo AG. Regulation of fat storage via suppressed thermogenesis: a thrifty phenotype that predisposes individuals with catch-up growth to insulin resistance and obesity. Horm Res 2006;65(Suppl 3): 90–97.
pmid
66. Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ 2000;320:967–971.
crossref pmid pmc
67. Ibanez L, Ong K, Dunger DB, de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab 2006;91:2153–2158.
crossref pmid
68. Leunissen RW, Stijnen T, Hokken-Koelega AC. Influence of birth size on body composition in early adulthood: the programming factors for growth and metabolism (PROGRAM)-study. Clin Endocrinol (Oxf) 2009;70:245–251.
crossref pmid
69. Kerkhof GF, Leunissen RW, Hokken-Koelega AC. Early origins of the metabolic syndrome: role of small size at birth, early postnatal weight gain, and adult IGF-I. J Clin Endocrinol Metab 2012;97:2637–2643.
crossref pmid pmc
70. Wells JC, Dumith SC, Ekelund U, Reichert FF, Menezes AM, Victora CG, et al. Associations of intrauterine and postnatal weight and length gains with adolescent body composition: prospective birth cohort study from Brazil. J Adolesc Health 2012;51(6 Suppl): S58–S64.
crossref pmid pmc
71. Zimmet P, Alberti KG, Kaufman F, Tajima N, Silink M, Arslanian S, et al. The metabolic syndrome in children and adolescents: an IDF consensus report. Pediatr Diabetes 2007;8:299–306.
crossref pmid
72. Steinberger J, Daniels SR, Eckel RH, Hayman L, Lustig RH, McCrindle B, et al. Progress and challenges in metabolic syndrome in children and adolescents: a scientific statement from the American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee of the Council on Cardiovascular Disease in the Young; Council on Cardiovascular Nursing; and Council on Nutrition, Physical Activity, and Metabolism. Circulation 2009;119:628–647.
crossref pmid
Table 1

Diagnostic criteria for childhood metabolic syndrome

kjped-59-1-i001
IDF criteria71)
(3 or more criteria must be present for the diagnosis of metabolic syndrome)
AHA criteria72)
(central obesity and 2 or more criteria)
Age (yr) 6-9 10-15 12-19
Waist circumference ≥90th Percentile for age ≥90th Percentile for age ≥90th Percentile for age, sex, and height
Blood pressure Systolic>130 or diastolic>85 mmHg ≥90th Percentile for age, sex, and height
Triglycerides ≥150 mg/dL ≥110 mg/dL
HDL-C ≤40 mg/dL ≤10th Percentile for race and sex
Fasting glucose ≥100 mg/dL ≥100 mg/dL

IDF, international diabetes federation; AHA, American Heart Association; HDL-C, high density lipoprotein cholesterol.

Table 2

Published data from clinical trials about inslin resistance and metabolic consequences in SGA

kjped-59-1-i002
Source Study population (n) Outcome measure Results
Hofman et al.37) (1997) 27 Case control study SGA have a specific impairment in insulin sensitivity compared to normal BW children (P=0.0048)
Byberg et al.41) (2000) 1,268 Population study Low BW predicts high blood pressure, insulin resistance, truncal obesity (P=0.03).
Choi et al.53) (2000) 22 Association study BW is not associated with any of the abdominal obesity measurements.
Laitinen et al.42) (2004) 5,771 Cohort study Abdominal obesity was independently associated with small size for GA
Rasmussen et al.44) (2005) 74 Case control study BW within the lowest 10th percentile is associated with changes in body fat content in early adulthood
Labayen et al.49) (2005) 234 Association study BW was inversely associated with the subscapular to triceps skinfolds ratio (P=0.05) in boys
Martinez-Aguayo et al.45) (2007) 65 Case control study Higher leptin level (P=0.01) and insulinogenic index (P=0.02) in girls born SGA.
Dolan et al.48) (2007) 101 Association study Low BW is associated with truncal fat mass, adjusted for total fat mass (P=0.03).
Labayen et al.36) (2008) 1,223 Cross sectional study Adjusted BW z-score was inversely associated with central obesity in both sexes (P=0.026)
Labayen et al.50) (2009) 284 Association study BW was negatively associated with abdominal regional fat mass indexes (all P=0.05)
Szalapska et al.46) (2010) 91 Association study In SGA children, a high frequency of particular diagnostic criteria for MetS was observed.
Pilgaard et al.54) (2010) 4,744 Association study Size at birth was not associated with waist/hip ratio when adjusted for socio-economic and lifestyle factors
Mori et al.47) (2012) 243 Association study BW was inversely related to SBP (P=0.007), DBP (P=0.033), TG (P=0.009), insulin level (P=0.047), insulin resistance (P=0.050), and number of metabolic risk factors (P=0.022).
Labayen et al.51) (2012) 409 Association study BW was inversely associated with changes in BMI (P=0.002) and the sum of five skinfolds (P=0.009) in girls.
Crume et al.52) (2014) 42 SGA had higher waist circumference (P=0.03), higher insulin (P=0.0002), higher HOMA-IR (P=0.03), and lower adiponectin levels (P=0.003) in adolescence.
Cho et al.7) (2014) 1,750 Cross sectional study BWGA is not related to individual components of MetS.

SGA, small for gestational age; BW, birth weight; GA, gestational age; MetS, metabolic syndrome; SBP, systolic blood pressure; DBP, diastolic blood pressure; TG, triglyceride; BMI, body mass index; HOMA-IR, homeostasis model assessment for insulin resistance; BWGA, birth weight at gestational age.

Table 3

Early catch-up growth and catch-up fat in SGA

kjped-59-1-i003
Source Study population Outcome measure Results
Ong et al.66) (2000) 848 Cohort study CUG children between 0 and 2 years were fatter and had more central fat distribution at five years
Ibanez et al.67) (2006) In SGA children, total and abdominal FM at 4 yr was more closely related to rate of weight gain between 0 and 2 yr (P=0.002) than between 2 and 4 yr (P=0.04)
Chomtho et al.57) (2008) 234 Association study Relative weight gain from 0 to 3 mo and from 3 to 6 mo showed a positive relationship with childhood FM, WC, and trunk FM
Leunissen et al.68) (2009) 312 Association study Weight gain during childhood is an important determinant of body composition in young adulthood.
Deng et al.62) (2011) 109 Case control study HOMA-IR in CUG SGA were higher than in NCUG SGA (P=0.002) and AGA children (P=0.036).
Kerkhof et al.69) (2012) 280 Association study Higher gain in weight for length in the first 3 months of life is associated with a higher prevalence of MetS at 21 yr.
Wells et al.70) (2012) 425 Rapid infant weight and length gains were primarily associated with larger size in adolescence rather than increased adiposity.
Howe et al.55) (2014) 3,154 Cohort study Rapid adiposity gain in infancy and continued overweight/obesity are associated with greater higher BP in young adulthood.
Stevens et al.61) (2014) 33 CU SGA children showed changes that may relate to cardiometabolic risk.

SGA, small for gestational age; FM, fat mass; WC, waist circumference; HOMA-IR, homeostasis model assessment for insulin resistance; CUG, catch-up growth; NCUG, non catch-up growth; AGA, appropriate for gestational age; MetS, metabolic syndrome; BP, blood pressure; CU, catch-up.



ABOUT
ARTICLE CATEGORY

Browse all articles >

BROWSE ARTICLES
AUTHOR INFORMATION
Editorial Office
#1606 Seocho World Officetel, 19 Seoun-ro, Seocho-ku, Seoul 06732, Korea
Tel: +82-2-3473-7305    Fax: +82-2-3473-7307    E-mail: kjpped@gmail.com                

Copyright © 2018 by Korean Pediatric Society. All rights reserved.

Developed in M2community

Close layer
prev next