Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Current Pediatrics Reports
Published in: Current Pediatrics Reports 2/2020

01-06-2020 | Neonatology (C Juliano and K Gluck, Section Editors)

Long-Term Metabolic Consequences of Intrauterine Growth Restriction

Authors: Kyoung Eun Joung, Jieun Lee, Jae Hyun Kim

Published in: Current Pediatrics Reports | Issue 2/2020

Login to get access

Abstract

Purpose of Review

To summarize recent findings on the associations of intrauterine growth restriction (IUGR) and long-term metabolic consequences such as obesity, type 2 diabetes (T2D), and cardiovascular diseases and the underlying mechanisms.

Recent Findings

Recent evidence suggests that metabolic diseases such as obesity, T2D, hypertension, and coronary artery disease are related to developmental programming in fetal period and early childhood. Rapid postnatal catch-up growth is also an important factor that contributes to the development of these long-term metabolic complications. The underlying mechanisms include oxidative stress, changes in hormonal milieu, vascular endothelial dysfunction, epigenetic regulation, and the potential alteration of microbiome.

Summary

Fetal and early life environment is an important determinant of long-term cardiometabolic risks. Children with IUGR need close follow-up for early detection of these complications.
Literature
1.
Hales CM CM, Fryar CD, Ogden CL. Prevalence of obesity among adults and youth: United States, 2015–2016. In: NCHS Data Brief 2017, National Center for Health Statistics (No. 288):Nati.
2.
Ogden CL, Carroll MD, Curtin LR, Lamb MM, Flegal KM. Prevalence of high body mass index in US children and adolescents, 2007-2008. JAMA. 2010;303(3):242–9.PubMedCrossRef
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(6673):564–7.PubMedPubMedCentralCrossRef
4.
Linner A, Almgren M. Epigenetic programming—the important first 1000 days. Acta Paediatr. 2019;109(3):443–52.
5.
American College of Obstetrics and Gynecologists. ACOG Practice bulletin No. 134: fetal growth restriction. Obstet Gynecol. 2013;121(5):1122–33.CrossRef
6.
Martin RJ, Fanaroff AA, Walsh MC. Fanaroff and Martin’s neonatal-perinatal medicine: diseases of the fetus and infant, vol. 1. 10th ed. Philadelphia: Saunders/Elsevier; 2015.
7.
Suhag A, Berghella V. Intrauterine growth restriction (IUGR): etiology and diagnosis. Curr Obstet Gynecol Rep. 2013;2:102–11.CrossRef
8.
Sharma D, Shastri S, Farahbakhsh N, Sharma P. Intrauterine growth restriction—part 1. J Matern Fetal Neonatal Med. 2016;29(24):3977–87.PubMedCrossRef
9.
Sharma D, Farahbakhsh N, Shastri S, Sharma P. Intrauterine growth restriction—part 2. J Matern Fetal Neonatal Med. 2016;29(24):4037–48.PubMedCrossRef
10.
• Kesavan K, Devaskar SU. Intrauterine growth restriction: postnatal monitoring and outcomes. Pediatr Clin N Am. 2019;66(2):403–23 This is the most recent summary of IUGR and its short term and long term endocrinologic complications such as short stature and polycystic ovarian disease.CrossRef
11.
Wang X, Zhu J, Guo C, Shi H, Wu D, Sun F, et al. Growth of infants and young children born small for gestational age: growth restriction accompanied by overweight. J Int Med Res. 2018;46(9):3765–77.PubMedPubMedCentralCrossRef
12.
Li P, Yang F, Xiong F, Huo T, Tong Y, Yang S, et al. Nutritional status and risk factors of overweight and obesity for children aged 9-15 years in Chengdu, Southwest China. BMC Public Health. 2012;12:636.PubMedPubMedCentralCrossRef
13.
Jornayvaz FR, Vollenweider P, Bochud M, Mooser V, Waeber G, Marques-Vidal P. Low birth weight leads to obesity, diabetes and increased leptin levels in adults: the CoLaus study. Cardiovasc Diabetol. 2016;15:73.PubMedPubMedCentralCrossRef
14.
Meas T, Deghmoun S, Armoogum P, Alberti C, Levy-Marchal C. Consequences of being born small for gestational age on body composition: an 8-year follow-up study. J Clin Endocrinol Metab. 2008;93(10):3804–9.PubMedPubMedCentralCrossRef
15.
Kensara OA, Wootton SA, Phillips DI, Patel M, Jackson AA, Elia M, et al. Fetal programming of body composition: relation between birth weight and body composition measured with dual-energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr. 2005;82(5):980–7.PubMedCrossRef
16.
Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Insulin resistance early in adulthood in subjects born with intrauterine growth retardation. J Clin Endocrinol Metab. 2000;85(4):1401–6.PubMed
17.
Valdez R, Athens MA, Thompson GH, Bradshaw BS, Stern MP. Birthweight and adult health outcomes in a biethnic population in the USA. Diabetologia. 1994;37(6):624–31.PubMedCrossRef
18.
Jaquet D, Gaboriau A, Czernichow P, Levy-Marchal C. Relatively low serum leptin levels in adults born with intra-uterine growth retardation. Int J Obes Relat Metab Disord. 2001;25(4):491–5.PubMedCrossRef
19.
Thurber KA, Dobbins T, Kirk M, Dance P, Banwell C. Early life predictors of increased body mass index among indigenous Australian children. PLoS One. 2015;10(6):e0130039.PubMedPubMedCentralCrossRef
20.
Boscaini C, Pellanda LC. Birth weight, current anthropometric markers, and high sensitivity C-reactive protein in Brazilian school children. J Obes. 2015;2015:846376.PubMedPubMedCentralCrossRef
21.
Rillamas-Sun E, Sowers MR, Harlow SD, Randolph JF Jr. The relationship of birth weight with longitudinal changes in body composition in adult women. Obesity (Silver Spring). 2012;20(2):463–5.CrossRef
22.
Zhao Y, Wang SF, Mu M, Sheng J. Birth weight and overweight/obesity in adults: a meta-analysis. Eur J Pediatr. 2012;171(12):1737–46.PubMedCrossRef
23.
Schellong K, Schulz S, Harder T, Plagemann A. Birth weight and long-term overweight risk: systematic review and a meta-analysis including 643,902 persons from 66 studies and 26 countries globally. PLoS One. 2012;7(10):e47776.PubMedPubMedCentralCrossRef
24.
Evensen E, Emaus N, Kokkvoll A, Wilsgaard T, Furberg AS, Skeie G. The relation between birthweight, childhood body mass index, and overweight and obesity in late adolescence: a longitudinal cohort study from Norway, the Tromso Study, fit futures. BMJ Open. 2017;7(6):e015576.PubMedPubMedCentralCrossRef
25.
Qiao Y, Ma J, Wang Y, Li W, Katzmarzyk PT, Chaput JP, et al. Birth weight and childhood obesity: a 12-country study. Int J Obes Suppl. 2015;5(Suppl 2):S74–9.PubMedPubMedCentralCrossRef
26.
Stansfield BK, Fain ME, Bhatia J, Gutin B, Nguyen JT, Pollock NK. Nonlinear relationship between birth weight and visceral fat in adolescents. J Pediatr. 2016;174:185–92.PubMedPubMedCentralCrossRef
27.
Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999;70(5):811–6.PubMedCrossRef
28.
Sachdev HP, Osmond C, Fall CH, Lakshmy R, Ramji S, Dey Biswas SK, et al. Predicting adult metabolic syndrome from childhood body mass index: follow-up of the New Delhi birth cohort. Arch Dis Child. 2009;94(10):768–74.PubMedCrossRef
29.
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(7240):967–71.PubMedPubMedCentralCrossRef
30.
Belfort MB, Gillman MW, Buka SL, Casey PH, McCormick MC. Preterm infant linear growth and adiposity gain: trade-offs for later weight status and intelligence quotient. J Pediatr. 2013;163(6):1564–1569e1562.PubMedCrossRef
31.
Tzoulaki I, Sovio U, Pillas D, Hartikainen AL, Pouta A, Laitinen J, et al. Relation of immediate postnatal growth with obesity and related metabolic risk factors in adulthood: the northern Finland birth cohort 1966 study. Am J Epidemiol. 2010;171(9):989–98.PubMedCrossRef
32.
Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med. 1995;1(12):1311–4.PubMedCrossRef
33.
Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372(6505):425–32.PubMedCrossRef
34.
Attig L, Djiane J, Gertler A, Rampin O, Larcher T, Boukthir S, et al. Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development. Am J Physiol Endocrinol Metab. 2008;295(5):E1117–25.PubMedCrossRef
35.
Teller IC, Hoyer-Kuhn H, Bronneke H, Nosthoff-Horstmann P, Oosting A, Lippach G, et al. Complex lipid globules in early-life nutrition improve long-term metabolic phenotype in intra-uterine growth-restricted rats. Br J Nutr. 2018;120(7):763–76.PubMedCrossRef
36.
Vickers MH, Gluckman PD, Coveny AH, Hofman PL, Cutfield WS, Gertler A, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005;146(10):4211–6.PubMedCrossRef
37.
Martinez-Cordero C, Amador-Licona N, Guizar-Mendoza JM, Hernandez-Mendez J, Ruelas-Orozco G. Body fat at birth and cord blood levels of insulin, adiponectin, leptin, and insulin-like growth factor-I in small-for-gestational-age infants. Arch Med Res. 2006;37(4):490–4.PubMedCrossRef
38.
Milenkovic S, Jankovic B, Mirkovic L, Jovandaric MZ, Milenkovic D, Otasevic B. Lipids and adipokines in cord blood and at 72 h in discordant dichorionic twins. Fetal Pediatr Pathol. 2017;36(2):106–22.PubMedCrossRef
39.
Mendez-Ramirez F, Barbosa-Sabanero G, Romero-Gutierrez G, Malacara JM. Ghrelin in small-for-gestational age (SGA) newborn babies: a cross-sectional study. Clin Endocrinol. 2009;70(1):41–6.CrossRef
40.
Mantzoros CS, Rifas-Shiman SL, Williams CJ, Fargnoli JL, Kelesidis T, Gillman MW. Cord blood leptin and adiponectin as predictors of adiposity in children at 3 years of age: a prospective cohort study. Pediatrics. 2009;123(2):682–9.PubMedCrossRef
41.
Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999;402(6762):656–60.PubMedCrossRef
42.
Farquhar J, Heiman M, Wong AC, Wach R, Chessex P, Chanoine JP. Elevated umbilical cord ghrelin concentrations in small for gestational age neonates. J Clin Endocrinol Metab. 2003;88(9):4324–7.PubMedCrossRef
43.
Onal EE, Cinaz P, Atalay Y, Turkyilmaz C, Bideci A, Akturk A, et al. Umbilical cord ghrelin concentrations in small- and appropriate-for-gestational age newborn infants: relationship to anthropometric markers. J Endocrinol. 2004;180(2):267–71.PubMedCrossRef
44.
Cortelazzi D, Cappiello V, Morpurgo PS, Ronzoni S, Nobile De Santis MS, Cetin I, et al. Circulating levels of ghrelin in human fetuses. Eur J Endocrinol. 2003;149(2):111–6.PubMedCrossRef
45.
Kitamura S, Yokota I, Hosoda H, Kotani Y, Matsuda J, Naito E, et al. Ghrelin concentration in cord and neonatal blood: relation to fetal growth and energy balance. J Clin Endocrinol Metab. 2003;88(11):5473–7.PubMedCrossRef
46.
Ng PC, Lee CH, Lam CW, Chan IH, Wong E, Fok TF. Ghrelin in preterm and term newborns: relation to anthropometry, leptin and insulin. Clin Endocrinol. 2005;63(2):217–22.CrossRef
47.
Briana DD, Malamitsi-Puchner A. Intrauterine growth restriction: the controversial role of perinatal adipocytokines in the prediction of metabolic adult disease. J Matern Fetal Neonatal Med. 2019:1–6.
48.
Alves MB, Laureano DP, Dalle Molle R, Machado TD, Salvador APA, Miguel PM, et al. Intrauterine growth restriction increases impulsive behavior and is associated with altered dopamine transmission in both medial prefrontal and orbitofrontal cortex in female rats. Physiol Behav. 2019;204:336–46.PubMedCrossRef
49.
Laureano DP, Alves MB, Miguel PM, Machado TD, Reis AR, Mucellini AB, et al. Intrauterine growth restriction modifies the accumbal dopaminergic response to palatable food intake. Neuroscience. 2019;400:184–95.PubMedCrossRef
50.
Volkow ND, Wang GJ, Fowler JS, Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond Ser B Biol Sci. 2008;363(1507):3191–200.CrossRef
51.
Wang GJ, Volkow ND, Logan J, Pappas NR, Wong CT, Zhu W, et al. Brain dopamine and obesity. Lancet. 2001;357(9253):354–7.PubMedCrossRef
52.
Xiong F, Zhang L. Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Front Neuroendocrinol. 2013;34(1):27–46.PubMedCrossRef
53.
Lucassen EA, Cizza G. The hypothalamic-pituitary-adrenal axis, obesity, and chronic stress exposure: sleep and the HPA axis in obesity. Curr Obes Rep. 2012;1(4):208–15.PubMedPubMedCentralCrossRef
54.
Vieau D, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007;32(Suppl 1):S16–20.PubMedCrossRef
55.
Zhang L, Xu D, Zhang B, Liu Y, Chu F, Guo Y, et al. Prenatal food restriction induces a hypothalamic-pituitary-adrenocortical axis-associated neuroendocrine metabolic programmed alteration in adult offspring rats. Arch Med Res. 2013;44(5):335–45.PubMedCrossRef
56.
Mierzynski R, Dluski D, Darmochwal-Kolarz D, Poniedzialek-Czajkowska E, Leszczynska-Gorzelak B, Kimber-Trojnar Z, et al. Intra-uterine growth retardation as a risk factor of postnatal metabolic disorders. Curr Pharm Biotechnol. 2016;17(7):587–96.PubMedCrossRef
57.
Jansson T, Powell TL. Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin Sci (Lond). 2007;113(1):1–13.CrossRef
58.
Gomez-Roig MD, Mazarico E, Cardenas D, Fernandez MT, Diaz M, Ruiz de Gauna B, et al. Placental 11B-hydroxysteroid dehydrogenase type 2 mRNA levels in intrauterine growth restriction versus small-for-gestational-age fetuses. Fetal Diagn Ther. 2016;39(2):147–51.PubMedCrossRef
59.
Kajantie E, Dunkel L, Turpeinen U, Stenman UH, Wood PJ, Nuutila M, et al. Placental 11 beta-hydroxysteroid dehydrogenase-2 and fetal cortisol/cortisone shuttle in small preterm infants. J Clin Endocrinol Metab. 2003;88(1):493–500.PubMedCrossRef
60.
Krochik AG, Chaler EA, Maceiras M, Aspres N, Mazza CS. Presence of early risk markers of metabolic syndrome in prepubertal children with a history of intrauterine growth restriction. Arch Argent Pediatr. 2010;108(1):10–6.PubMed
61.
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(12):4611–8.PubMed
62.
Phillips DI, Walker BR, Reynolds RM, Flanagan DE, Wood PJ, Osmond C, et al. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension. 2000;35(6):1301–6.PubMedCrossRef
63.
Jousse C, Parry L, Lambert-Langlais S, Maurin AC, Averous J, Bruhat A, et al. Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. FASEB J. 2011;25(9):3271–8.PubMedCrossRef
64.
65.
Williams L, Seki Y, Delahaye F, Cheng A, Fuloria M, Hughes Einstein F, et al. DNA hypermethylation of CD3(+) T cells from cord blood of infants exposed to intrauterine growth restriction. Diabetologia. 2016;59(8):1714–23.PubMedCrossRef
66.
•• Vaiserman A, Lushchak O. Developmental origins of type 2 diabetes: focus on epigenetics. Ageing Res Rev. 2019;55:100957 This review is the most up-to-date summary of researches on epigenetic modifications in type 2 diabetes.PubMedCrossRef
67.
Oses M, Margareto Sanchez J, Portillo MP, Aguilera CM, Labayen I. Circulating miRNAs as biomarkers of obesity and obesity-associated comorbidities in children and adolescents: a systematic review. Nutrients. 2019;11(12):E2890
68.
Chambers KF, Day PE, Aboufarrag HT, Kroon PA. Polyphenol effects on cholesterol metabolism via bile acid biosynthesis, CYP7A1: a review. Nutrients. 2019;11(11):E2588
69.
70.
71.
72.
Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31.PubMedCrossRef
73.
Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022–3.PubMedCrossRef
74.
Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480–4.PubMedCrossRef
75.
Zhang W, Ma C, Xie P, Zhu Q, Wang X, Yin Y, et al. Gut microbiota of newborn piglets with intrauterine growth restriction have lower diversity and different taxonomic abundances. J Appl Microbiol. 2019;127(2):354–69.PubMedPubMedCentralCrossRef
76.
Jiang L, Feng C, Tao S, Li N, Zuo B, Han D, et al. Maternal imprinting of the neonatal microbiota colonization in intrauterine growth restricted piglets: a review. J Anim Sci Biotechnol. 2019;10:88.PubMedPubMedCentralCrossRef
77.
Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991;303(6809):1019–22.PubMedPubMedCentralCrossRef
78.
de Lauzon-Guillain B, Balkau B, Charles MA, Romieu I, Boutron-Ruault MC, Clavel-Chapelon F. Birth weight, body silhouette over the life course, and incident diabetes in 91,453 middle-aged women from the French Etude Epidemiologique de Femmes de la Mutuelle Generale de l’Education Nationale (E3N) cohort. Diabetes Care. 2010;33(2):298–303.PubMedCrossRef
79.
Kaijser M, Bonamy AK, Akre O, Cnattingius S, Granath F, Norman M, et al. Perinatal risk factors for diabetes in later life. Diabetes. 2009;58(3):523–6.PubMedPubMedCentralCrossRef
80.
81.
Rich-Edwards JW, Colditz GA, Stampfer MJ, Willett WC, Gillman MW, Hennekens CH, et al. Birthweight and the risk for type 2 diabetes mellitus in adult women. Ann Intern Med. 1999;130(4 Pt 1):278–84.PubMedCrossRef
82.
Feng C, Osgood ND, Dyck RF. Low birth weight, cumulative obesity dose, and the risk of incident type 2 diabetes. J Diabetes Res. 2018;2018:8435762.PubMedPubMedCentral
83.
Whincup PH, Kaye SJ, Owen CG, Huxley R, Cook DG, Anazawa S, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008;300(24):2886–97.PubMedCrossRef
84.
Dyck RF, Klomp H, Tan L. From “thrifty genotype” to “hefty fetal phenotype”: the relationship between high birthweight and diabetes in Saskatchewan registered Indians. Can J Public Health. 2001;92(5):340–4.PubMedPubMedCentralCrossRef
85.
Fall CH, Stein CE, Kumaran K, Cox V, Osmond C, Barker DJ, et al. Size at birth, maternal weight, and type 2 diabetes in South India. Diabet Med. 1998;15(3):220–7.PubMedCrossRef
86.
Harder T, Rodekamp E, Schellong K, Dudenhausen JW, Plagemann A. Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. Am J Epidemiol. 2007;165(8):849–57.PubMedCrossRef
87.
Zanetti D, Tikkanen E, Gustafsson S, Priest JR, Burgess S, Ingelsson E. Birthweight, type 2 diabetes mellitus, and cardiovascular disease: addressing the Barker hypothesis with Mendelian randomization. Circ Genom Precis Med. 2018;11(6):e002054.PubMedPubMedCentralCrossRef
88.
• Wang T, Huang T, Li Y, Zheng Y, Manson JE, Hu FB, et al. Low birthweight and risk of type 2 diabetes: a Mendelian randomisation study. Diabetologia. 2016;59(9):1920–7 This is an important Mendelian randomization study investigating the potential causal relationship of low birth weight and the risk of type 2 diabetes.PubMedPubMedCentralCrossRef
89.
Giapros V, Vavva E, Siomou E, Kolios G, Tsabouri S, Cholevas V, et al. Low-birth-weight, but not catch-up growth, correlates with insulin resistance and resistin level in SGA infants at 12 months. J Matern Fetal Neonatal Med. 2017;30(15):1771–6.PubMedCrossRef
90.
Brufani C, Grossi A, Fintini D, Tozzi A, Nocerino V, Patera PI, et al. Obese children with low birth weight demonstrate impaired beta-cell function during oral glucose tolerance test. J Clin Endocrinol Metab. 2009;94(11):4448–52.PubMedCrossRef
91.
Veening MA, van Weissenbruch MM, Heine RJ, Delemarre-van de Waal HA. Beta-cell capacity and insulin sensitivity in prepubertal children born small for gestational age: influence of body size during childhood. Diabetes. 2003;52(7):1756–60.PubMedCrossRef
92.
Akhaphong B, Lockridge A, Jo S, Mohan R, Wilcox JA, Wing CR, et al. Reduced uterine perfusion pressure causes loss of pancreatic beta-cell area but normal function in fetal rat offspring. Am J Physiol Regul Integr Comp Physiol. 2018;315(6):R1220–31.PubMedPubMedCentralCrossRef
93.
Abuzgaia AM, Hardy DB, Arany E. Regulation of postnatal pancreatic Pdx1 and downstream target genes after gestational exposure to protein restriction in rats. Reproduction. 2015;149(3):293–303.PubMedCrossRef
94.
Limesand SW, Rozance PJ, Macko AR, Anderson MJ, Kelly AC, Hay WW Jr. Reductions in insulin concentrations and beta-cell mass precede growth restriction in sheep fetuses with placental insufficiency. Am J Physiol Endocrinol Metab. 2013;304(5):E516–23.PubMedCrossRef
95.
Limesand SW, Jensen J, Hutton JC, Hay WW Jr. Diminished beta-cell replication contributes to reduced beta-cell mass in fetal sheep with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2005;288(5):R1297–305.PubMedCrossRef
96.
Van Assche FA, De Prins F, Aerts L, Verjans M. The endocrine pancreas in small-for-dates infants. Br J Obstet Gynaecol. 1977;84(10):751–3.PubMedCrossRef
97.
Wang T, Liu C, Feng C, Wang X, Lin G, Zhu Y, et al. IUGR alters muscle fiber development and proteome in fetal pigs. Front Biosci (Landmark Ed). 2013;18:598–607.CrossRef
98.
Yates DT, Clarke DS, Macko AR, Anderson MJ, Shelton LA, Nearing M, et al. Myoblasts from intrauterine growth-restricted sheep fetuses exhibit intrinsic deficiencies in proliferation that contribute to smaller semitendinosus myofibres. J Physiol. 2014;592(14):3113–25.PubMedPubMedCentralCrossRef
99.
Brown LD, Rozance PJ, Thorn SR, Friedman JE, Hay WW Jr. Acute supplementation of amino acids increases net protein accretion in IUGR fetal sheep. Am J Physiol Endocrinol Metab. 2012;303(3):E352–64.PubMedPubMedCentralCrossRef
100.
Mavalli MD, DiGirolamo DJ, Fan Y, Riddle RC, Campbell KS, van Groen T, et al. Distinct growth hormone receptor signaling modes regulate skeletal muscle development and insulin sensitivity in mice. J Clin Invest. 2010;120(11):4007–20.PubMedPubMedCentralCrossRef
101.
Padoan A, Rigano S, Ferrazzi E, Beaty BL, Battaglia FC, Galan HL. Differences in fat and lean mass proportions in normal and growth-restricted fetuses. Am J Obstet Gynecol. 2004;191(4):1459–64.PubMedCrossRef
102.
Beltrand J, Nicolescu R, Kaguelidou F, Verkauskiene R, Sibony O, Chevenne D, et al. Catch-up growth following fetal growth restriction promotes rapid restoration of fat mass but without metabolic consequences at one year of age. PLoS One. 2009;4(4):e5343.PubMedPubMedCentralCrossRef
103.
Yliharsila H, Kajantie E, Osmond C, Forsen T, Barker DJ, Eriksson JG. Birth size, adult body composition and muscle strength in later life. Int J Obes. 2007;31(9):1392–9.CrossRef
104.
Rashid CS, Bansal A, Simmons RA. Oxidative stress, intrauterine growth restriction, and developmental programming of type 2 diabetes. Physiology (Bethesda). 2018;33(5):348–59.
105.
Tarry-Adkins JL, Fernandez-Twinn DS, Chen JH, Hargreaves IP, Neergheen V, Aiken CE, et al. Poor maternal nutrition and accelerated postnatal growth induces an accelerated aging phenotype and oxidative stress in skeletal muscle of male rats. Dis Model Mech. 2016;9(10):1221–9.PubMedPubMedCentral
106.
Kelly AC, Bidwell CA, McCarthy FM, Taska DJ, Anderson MJ, Camacho LE, et al. RNA sequencing exposes adaptive and immune responses to intrauterine growth restriction in fetal sheep islets. Endocrinology. 2017;158(4):743–55.PubMedPubMedCentralCrossRef
107.
Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008;118(6):2316–24.PubMedPubMedCentral
108.
Thompson RF, Fazzari MJ, Niu H, Barzilai N, Simmons RA, Greally JM. Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats. J Biol Chem. 2010;285(20):15111–8.PubMedPubMedCentralCrossRef
109.
Zhang L, Chen W, Dai Y, Zhu Z, Liu Q. Detection of expressional changes induced by intrauterine growth restriction in the developing rat pancreas. Exp Biol Med (Maywood). 2016;241(13):1446–56.CrossRef
110.
Chu A, Casero D, Thamotharan S, Wadehra M, Cosi A, Devaskar SU. The placental Transcriptome in late gestational hypoxia resulting in murine intrauterine growth restriction parallels increased risk of adult Cardiometabolic disease. Sci Rep. 2019;9(1):1243.PubMedPubMedCentralCrossRef
111.
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(Pt 1):141–52.PubMedPubMedCentralCrossRef
112.
Tare M, Parkington HC, Bubb KJ, Wlodek ME. Uteroplacental insufficiency and lactational environment separately influence arterial stiffness and vascular function in adult male rats. Hypertension. 2012;60(2):378–86.PubMedCrossRef
113.
Gennser G, Rymark P, Isberg PE. Low birth weight and risk of high blood pressure in adulthood. Br Med J (Clin Res Ed). 1988;296(6635):1498–500.CrossRef
114.
Nilsson PM, Ostergren PO, Nyberg P, Soderstrom M, Allebeck P. Low birth weight is associated with elevated systolic blood pressure in adolescence: a prospective study of a birth cohort of 149378 Swedish boys. J Hypertens. 1997;15(12 Pt 2):1627–31.PubMedCrossRef
115.
116.
Tan M, Cai L, Ma J, Jing J, Ma Y, Chen Y. The association of gestational age and birth weight with blood pressure among children: a Chinese national study. J Hum Hypertens. 2018;32(10):651–9.PubMedCrossRef
117.
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(7):815–31.PubMedCrossRef
118.
Fattal-Valevski A, Bernheim J, Leitner Y, Redianu B, Bassan H, Harel S. Blood pressure values in children with intrauterine growth retardation. Isr Med Assoc J. 2001;3(11):805–8.PubMed
119.
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(8):935–41.PubMedCrossRef
120.
Roseboom TJ, van der Meulen JH, Ravelli AC, van Montfrans GA, Osmond C, Barker DJ, et al. Blood pressure in adults after prenatal exposure to famine. J Hypertens. 1999;17(3):325–30.PubMedCrossRef
121.
de Jong F, Monuteaux MC, van Elburg RM, Gillman MW, Belfort MB. Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension. 2012;59(2):226–34.PubMedCrossRef
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(5):520–2.PubMedCrossRef
123.
Parkinson JR, Hyde MJ, Gale C, Santhakumaran S, Modi N. Preterm birth and the metabolic syndrome in adult life: a systematic review and meta-analysis. Pediatrics. 2013;131(4):e1240–63.PubMedCrossRef
124.
Fattal-Valevski A, Bassan H, Bernheim J, Redianu B, Leitner Y, Harel S. Blood pressure values in 8-12 year old children with a history of intrauterine growth retardation. Isr Med Assoc J. 2011;13(8):480–4.PubMed
125.
Strambi M, Messa G, Berni S, Capitani S, Pammolli A, Iacoponi F, et al. Basal and post-ischemic vascular compliance in children/adolescents born small for gestational age. Pediatr Nephrol. 2012;27(9):1541–6.PubMedPubMedCentralCrossRef
126.
Lindstrom L, Skjaerven R, Bergman E, Lundgren M, Klungsoyr K, Cnattingius S, et al. Chronic hypertension in women after perinatal exposure to preeclampsia, being born small for gestational age or preterm. Paediatr Perinat Epidemiol. 2017;31(2):89–98.PubMedCrossRef
127.
Juonala M, Cheung MM, Sabin MA, Burgner D, Skilton MR, Kahonen M, et al. Effect of birth weight on life-course blood pressure levels among children born premature: the cardiovascular risk in young Finns Study. J Hypertens. 2015;33(8):1542–8.PubMedCrossRef
128.
Belfort MB, Rifas-Shiman SL, Rich-Edwards J, Kleinman KP, Gillman MW. Size at birth, infant growth, and blood pressure at three years of age. J Pediatr. 2007;151(6):670–4.PubMedPubMedCentralCrossRef
129.
Singhal A, Cole TJ, Fewtrell M, Kennedy K, Stephenson T, Elias-Jones A, et al. Promotion of faster weight gain in infants born small for gestational age: is there an adverse effect on later blood pressure? Circulation. 2007;115(2):213–20.PubMedCrossRef
130.
Garcia-Canadilla P, de Vries T, Gonzalez-Tendero A, Bonnin A, Gratacos E, Crispi F, et al. Structural coronary artery remodelling in the rabbit fetus as a result of intrauterine growth restriction. PLoS One. 2019;14(6):e0218192.PubMedPubMedCentralCrossRef
131.
Bubb KJ, Cock ML, Black MJ, Dodic M, Boon WM, Parkington HC, et al. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol. 2007;578(Pt 3):871–81.PubMedCrossRef
132.
Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80.PubMedCrossRef
133.
Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45. Heart. 2000;84(6):595–8.PubMedPubMedCentralCrossRef
134.
Izquierdo AG, Crujeiras AB, Casanueva FF, Carreira MC. Leptin, Obesity, and Leptin Resistance: Where Are We 25 Years Later? Nutrients. 2019;11(11):E2704.
135.
Grandvuillemin I, Buffat C, Boubred F, Lamy E, Fromonot J, Charpiot P, et al. Arginase upregulation and eNOS uncoupling contribute to impaired endothelium-dependent vasodilation in a rat model of intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2018;315(3):R509–20.PubMedCrossRef
136.
Schneider D, Hernandez C, Farias M, Uauy R, Krause BJ, Casanello P. Oxidative stress as common trait of endothelial dysfunction in chorionic arteries from fetuses with IUGR and LGA. Placenta. 2015;36(5):552–8.PubMedCrossRef
137.
Krause BJ, Carrasco-Wong I, Caniuguir A, Carvajal J, Farias M, Casanello P. Endothelial eNOS/arginase imbalance contributes to vascular dysfunction in IUGR umbilical and placental vessels. Placenta. 2013;34(1):20–8.PubMedCrossRef
138.
Franco MC, Kawamoto EM, Gorjao R, Rastelli VM, Curi R, Scavone C, et al. Biomarkers of oxidative stress and antioxidant status in children born small for gestational age: evidence of lipid peroxidation. Pediatr Res. 2007;62(2):204–8.PubMedCrossRef
139.
Barnea M, Chapnik N, Genzer Y, Froy O. The circadian clock machinery controls adiponectin expression. Mol Cell Endocrinol. 2015;399:284–7.PubMedCrossRef
140.
Dodson RB, Rozance PJ, Fleenor BS, Petrash CC, Shoemaker LG, Hunter KS, et al. Increased arterial stiffness and extracellular matrix reorganization in intrauterine growth-restricted fetal sheep. Pediatr Res. 2013;73(2):147–54.PubMedCrossRef
141.
Burkhardt T, Matter CM, Lohmann C, Cai H, Luscher TF, Zisch AH, et al. Decreased umbilical artery compliance and igf-I plasma levels in infants with intrauterine growth restriction - implications for fetal programming of hypertension. Placenta. 2009;30(2):136–41.PubMedCrossRef
142.
Stergiotou I, Crispi F, Valenzuela-Alcaraz B, Cruz-Lemini M, Bijnens B, Gratacos E. Aortic and carotid intima-media thickness in term small-for-gestational-age newborns and relationship with prenatal signs of severity. Ultrasound Obstet Gynecol. 2014;43(6):625–31.PubMedCrossRef
143.
Sebastiani G, Diaz M, Bassols J, Aragones G, Lopez-Bermejo A, de Zegher F, et al. The sequence of prenatal growth restraint and post-natal catch-up growth leads to a thicker intima-media and more pre-peritoneal and hepatic fat by age 3-6 years. Pediatr Obes. 2016;11(4):251–7.PubMedCrossRef
144.
Tzschoppe A, von Kries R, Struwe E, Rascher W, Dorr HG, Jungert J, et al. Intrauterine growth restriction (IUGR) induces signs of subclinical atherosclerosis in 6-year-old infants despite absence of excessive growth. Klin Padiatr. 2017;229(4):209–15.PubMedCrossRef
145.
Jiang B, Godfrey KM, Martyn CN, Gale CR. Birth weight and cardiac structure in children. Pediatrics. 2006;117(2):e257–61.PubMedCrossRef
146.
Mitchell P, Liew G, Rochtchina E, Wang JJ, Robaei D, Cheung N, et al. Evidence of arteriolar narrowing in low-birth-weight children. Circulation. 2008;118(5):518–24.PubMedCrossRef
147.
Gopinath B, Baur LA, Wang JJ, Teber E, Liew G, Cheung N, et al. Smaller birth size is associated with narrower retinal arterioles in early adolescence. Microcirculation. 2010;17(8):660–8.PubMedCrossRef
148.
Liew G, Wang JJ, Duncan BB, Klein R, Sharrett AR, Brancati F, et al. Atherosclerosis risk in communities S: low birthweight is associated with narrower arterioles in adults. Hypertension. 2008;51(4):933–8.PubMedCrossRef
149.
Crispi F, Bijnens B, Figueras F, Bartrons J, Eixarch E, Le Noble F, et al. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation. 2010;121(22):2427–36.PubMedCrossRef
150.
Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135(6):1382–6.PubMedCrossRef
151.
Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr. 2008;100(2):278–82.PubMedPubMedCentralCrossRef
152.
Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, et al. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res. 2005;33(21):6823–36.PubMedPubMedCentralCrossRef
153.
Burris HH, Braun JM, Byun HM, Tarantini L, Mercado A, Wright RJ, et al. Association between birth weight and DNA methylation of IGF2, glucocorticoid receptor and repetitive elements LINE-1 and Alu. Epigenomics. 2013;5(3):271–81.PubMedCrossRef
154.
Lopes LL, Bressan J, Peluzio M, Hermsdorff HHM. LINE-1 in obesity and Cardiometabolic diseases: a systematic review. J Am Coll Nutr. 2019;38(5):478–84.PubMedCrossRef
155.
Muka T, Koromani F, Portilla E, O'Connor A, Bramer WM, Troup J, et al. The role of epigenetic modifications in cardiovascular disease: a systematic review. Int J Cardiol. 2016;212:174–83.PubMedCrossRef
156.
Wei L, Liu S, Su Z, Cheng R, Bai X, Li X. LINE-1 hypomethylation is associated with the risk of coronary heart disease in Chinese population. Arq Bras Cardiol. 2014;102(5):481–8.PubMedPubMedCentral
157.
Lin RT, Hsi E, Lin HF, Liao YC, Wang YS, Juo SH. LINE-1 methylation is associated with an increased risk of ischemic stroke in men. Curr Neurovasc Res. 2014;11(1):4–9.PubMedCrossRef
158.
Baccarelli A, Tarantini L, Wright RO, Bollati V, Litonjua AA, Zanobetti A, et al. Repetitive element DNA methylation and circulating endothelial and inflammation markers in the VA normative aging study. Epigenetics. 2010;5(3):222–8.PubMedCrossRef
159.
Kong DH, Kim YK, Kim MR, Jang JH, Lee S. Emerging Roles of Vascular Cell Adhesion Molecule-1 (VCAM-1) in Immunological Disorders and Cancer. Int J Mol Sci. 2018;19(4):E1057.
160.
Wilhelm-Benartzi CS, Houseman EA, Maccani MA, Poage GM, Koestler DC, Langevin SM, et al. In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect. 2012;120(2):296–302.PubMedCrossRef
161.
Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS One. 2011;6(9):e25254.PubMedPubMedCentralCrossRef
162.
Hromadnikova I, Kotlabova K, Ivankova K, Vedmetskaya Y, Krofta L. Profiling of cardiovascular and cerebrovascular disease associated microRNA expression in umbilical cord blood in gestational hypertension, preeclampsia and fetal growth restriction. Int J Cardiol. 2017;249:402–9.PubMedCrossRef
163.
De Rosa S, Arcidiacono B, Chiefari E, Brunetti A, Indolfi C, Foti DP. Type 2 diabetes mellitus and cardiovascular disease: genetic and epigenetic links. Front Endocrinol (Lausanne). 2018;9:2.CrossRef
164.
Hromadnikova I, Kotlabova K, Hympanova L, Krofta L. Cardiovascular and cerebrovascular disease associated microRNAs are Dysregulated in placental tissues affected with gestational hypertension, preeclampsia and intrauterine growth restriction. PLoS One. 2015;10(9):e0138383.PubMedPubMedCentralCrossRef
Metadata
Title
Long-Term Metabolic Consequences of Intrauterine Growth Restriction
Authors
Kyoung Eun Joung
Jieun Lee
Jae Hyun Kim
Publication date
01-06-2020
Publisher
Springer US
Published in
Current Pediatrics Reports / Issue 2/2020
Electronic ISSN: 2167-4841
DOI
https://doi.org/10.1007/s40124-020-00212-x