Large birth size, infancy growth pattern, insulin resistance and β-cell function

in European Journal of Endocrinology
View More View Less
  • 1 Department of Obstetrics and Gynecology, Prosserman Centre for Population Health Research, Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, and Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Canada
  • 2 Sainte-Justine Hospital Research Center, University of Montreal, Montreal, Canada
  • 3 Ministry of Education-Shanghai Key Laboratory of Children’s Environmental Health, Department of Pediatrics, Xinhua Hospital, Shanghai Jiao-Tong University School of Medicine, Shanghai, China
  • 4 CHU de Quebec-Laval University Research Center, Laval University, Quebec City, Canada
  • 5 Department of Obstetrics and Gynecology, Centre de recherche du Centre Hospitalier Universitaire de Sherbrooke, University of Sherbrooke, Sherbrooke, Canada

Correspondence should be addressed to Z-C Luo Email zcluo@lunenfeld.ca
Restricted access

Objective

Large birth size programs an elevated risk of type 2 diabetes in adulthood, but data are absent concerning glucose metabolic health impact in infancy. We sought to determine whether the large birth size is associated with insulin resistance and β-cell function in infancy and evaluate the determinants.

Design and participants

In the Canadian 3D birth cohort, we conducted a nested matched (1:2) study of 70 large-for-gestational-age (LGA, birth weight >90th percentile) and 140 optimal-for-gestational-age (OGA, 25th–75th percentiles) control infants. The primary outcomes were homeostasis model assessment of insulin resistance (HOMA-IR) and beta-cell function (HOMA-β) at age 2-years.

Results

HOMA-IR and HOMA-β were similar in LGA and OGA infants. Adjusting for maternal and infant characteristics, decelerated growth in length during early infancy (0–3 months) was associated with a 25.8% decrease (95% confidence intervals 6.7–41.0%) in HOMA-β. During mid-infancy (3–12 months), accelerated growth in weight was associated with a 25.5% (0.35–56.9%) increase in HOMA-IR, in length with a 69.3% increase (31.4–118.0%) in HOMA-IR and a 24.5% (0.52–54.3%) increase in HOMA-β. Decelerated growth in length during late infancy (1–2 years) was associated with a 28.4% (9.5–43.4%) decrease in HOMA-IR and a 21.2% (3.9–35.4%) decrease in HOMA-β. Female sex was associated with higher HOMA-β, Caucasian ethnicity with lower HOMA-IR, and maternal smoking with lower HOMA-β.

Conclusions

This study is the first to demonstrate that large birth size is not associated with insulin resistance and β-cell function in infancy but infancy growth pattern matters. Decelerated infancy growth may be detrimental to beta-cell function.

Supplementary Materials

    • Table S1 (online only). Crude associations of infancy growth (weight or length) patterns in early (0-3 months), mid (3-12 months) and late (12-24 months) infancy with HOMA indices at age 2 years
    • Figure 1. Flowchart in the selection of study subjects in a nested matched (1:2) study of LGA and OGA (control) infants in the 3D birth cohort. LGA: large-for-gestational-age (birth weight >90th percentile); OGA: optimal-for-gestational-age (birth weight 25th-75th percentiles).

 

     European Society of Endocrinology

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 142 142 142
Full Text Views 13 13 13
PDF Downloads 18 18 18
  • 1

    Harder T, Rodekamp E, Schellong K, Dudenhausen JW & Plagemann A Birth weight and subsequent risk of type 2 diabetes: a meta-analysis. American Journal of Epidemiology 2007 165 849857. (https://doi.org/10.1093/aje/kwk071)

    • Search Google Scholar
    • Export Citation
  • 2

    Zethelius B, Byberg L, Hales CN, Lithell H & Berne C Proinsulin and acute insulin response independently predict type 2 diabetes mellitus in men – report from 27 years of follow-up study. Diabetologia 2003 46 2026. (https://doi.org/10.1007/s00125-002-0995-2)

    • Search Google Scholar
    • Export Citation
  • 3

    Dong Y, Luo ZC, Nuyt AM, Audibert F, Wei SQ, Abenhaim HA, Bujoid E, Julien P, Huang H & Levy E et al. Large-for-gestational-age may be associated with lower fetal insulin sensitivity and β-cell function linked to leptin. Journal of Clinical Endocrinology and Metabolism 2018 103 38373844. (https://doi.org/10.1210/jc.2018-00917)

    • Search Google Scholar
    • Export Citation
  • 4

    Simental-Mendía LE, Castañeda-Chacón A, Rodríguez-Morán M & Guerrero-Romero F Birth-weight, insulin levels, and HOMA-IR in newborns at term. BMC Pediatrics 2012 12 94. (https://doi.org/10.1186/1471-2431-12-94)

    • Search Google Scholar
    • Export Citation
  • 5

    Dyer JS, Rosenfeld CR, Rice J, Rice M & Hardin DS Insulin resistance in hispanic large-for-gestational-age neonates at birth. Journal of Clinical Endocrinology and Metabolism 2007 92 38363843. (https://doi.org/10.1210/jc.2007-0079)

    • Search Google Scholar
    • Export Citation
  • 6

    Boney CM, Verma A, Tucker R & Vohr BR Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005 115 e290e296. (https://doi.org/10.1542/peds.2004-1808)

    • Search Google Scholar
    • Export Citation
  • 7

    Giapros V, Evagelidou E, Challat A, Kiortsis D, Drougia A & Andronikou S Serum adiponectin and leptin levels and insulin resistance in children born large for gestational age are affected by the degree of overweight. Clinical Endocrinology 2007 66 353359. (https://doi.org/10.1111/j.1365-2265.2006.02736.x)

    • Search Google Scholar
    • Export Citation
  • 8

    Chiavaroli V, Marcovecchio ML, de Giorgis T, Diesse L, Chiarelli F & Mohn A Progression of cardio-metabolic risk factors in subjects born small and large for gestational age. PLoS ONE 2014 9 e104278. (https://doi.org/10.1371/journal.pone.0104278)

    • Search Google Scholar
    • Export Citation
  • 9

    Gluckman PD & Hanson MA Living with the past: evolution, development, and patterns of disease. Science 2004 305 17331736. (https://doi.org/10.1126/science.1095292)

    • Search Google Scholar
    • Export Citation
  • 10

    Singhal A, Cole TJ, Fewtrell M, Deanfield J & Lucas A Is slower early growth beneficial for long-term cardiovascular health? Circulation 2004 109 11081113. (https://doi.org/10.1161/01.CIR.0000118500.23649.DF)

    • Search Google Scholar
    • Export Citation
  • 11

    Ekelund U, Ong KK, Linné Y, Neovius M, Brage S, Dunger DB, Wareham NJ & Rossner S Association of weight gain in infancy and early childhood with metabolic risk in young adults. Journal of Clinical Endocrinology and Metabolism 2007 92 98103. (https://doi.org/10.1210/jc.2006-1071)

    • Search Google Scholar
    • Export Citation
  • 12

    Leunissen RW, Kerkhof GF, Stijnen T & Hokken-Koelega A Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthood. JAMA 2009 301 22342242. (https://doi.org/10.1001/jama.2009.761)

    • Search Google Scholar
    • Export Citation
  • 13

    Zhang DL, Du QW, Djemli A, Julien P, Fraser WD & Luo ZC Early and late postnatal accelerated growth have distinct effects on metabolic health in normal birth weight infants. Frontiers in Endocrinology 2017 8 340. (https://doi.org/10.3389/fendo.2017.00340)

    • Search Google Scholar
    • Export Citation
  • 14

    Liu C, Wu B, Lin N & Fang X Insulin resistance and its association with catch-up growth in Chinese children born small for gestational age. Obesity 2017 25 172177. (https://doi.org/10.1002/oby.21683)

    • Search Google Scholar
    • Export Citation
  • 15

    Soto N, Bazaes RA, Peña V, Salazar T, Avila A, Iniguez G, Ong KK, Bunger DB & Mericq MV Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. Journal of Clinical Endocrinology and Metabolism 2003 88 36453650. (https://doi.org/10.1210/jc.2002-030031)

    • Search Google Scholar
    • Export Citation
  • 16

    Fraser WD, Shapiro GD, Audibert F, Dubois L, Pasquier JC, Julien P, Berard A, Muckle G, Trasler J & Tremblay RE 3D cohort study: the integrated research network in perinatology of Quebec and Eastern Ontario. Paediatric and Perinatal Epidemiology 2016 30 623632. (https://doi.org/10.1111/ppe.12320)

    • Search Google Scholar
    • Export Citation
  • 17

    Kramer MS, Platt RW, Wen SW, Joseph KS, Allen A, Abrahamowicz M, Blondel B, Breart GFetal/Infant Health Study Group of the Canadian Perinatal Surveillance System. A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 2001 108 E35. (https://doi.org/10.1542/peds.108.2.e35)

    • Search Google Scholar
    • Export Citation
  • 18

    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF & Turner RC Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985 28 412419. (https://doi.org/10.1007/BF00280883)

    • Search Google Scholar
    • Export Citation
  • 19

    Veena SR, Krishnaveni GV, Wills AK, Hill JC, Karat SC & Fall CH Glucose tolerance and insulin resistance in Indian children: relationship to infant feeding pattern. Diabetologia 2011 54 2533–2537. (https://doi.org/10.1007/s00125-011-2254-x)

    • Search Google Scholar
    • Export Citation
  • 20

    Ripa P, Robertson I, Cowley D, Harris M, Masters IB & Cotterill AM The relationship between insulin secretion, the insulin-like growth factor axis and growth in children with cystic fibrosis. Clinical Endocrinology 2002 56 383389. (https://doi.org/10.1046/j.1365-2265.2002.01484.x)

    • Search Google Scholar
    • Export Citation
  • 21

    Sakata N, Chan NK, Chrisler J, Obenaus A & Hathout E Bone marrow cell co-transplantation with islets improves their vascularization and function. Transplantation 2010 89 686693. (https://doi.org/10.1097/TP.0b013e3181cb3e8d)

    • Search Google Scholar
    • Export Citation
  • 22

    Tang S, Xin Y, Yang M, Zhang D & Xu C Osteoprotegerin promotes islet β cell proliferation in intrauterine growth retardation rats through the PI3K/AKT/FoxO1 pathway. International Journal of Clinical and Experimental Pathology 2019 12 23242338.

    • Search Google Scholar
    • Export Citation
  • 23

    Schrader J, Rennekamp W, Niebergall U, Schoppet M, Jahr H, Brendel MD, Horsch D & Hofbauer LC Cytokine-induced osteoprotegerin expression protects pancreatic beta cells through p38 mitogen-activated protein kinase signalling against cell death. Diabetologia 2007 50 12431247. (https://doi.org/10.1007/s00125-007-0672-6)

    • Search Google Scholar
    • Export Citation
  • 24

    Ong KK & Dunge DB Birth weight, infant growth and insulin resistance. European Journal of Endocrinology 2004 151 (Supplement 3) U131U13 9. (https://doi.org/10.1530/eje.0.151u131)

    • Search Google Scholar
    • Export Citation
  • 25

    Young-Hyman D, Schlundt DG, Herman L, De Luca F & Counts D Evaluation of the insulin resistance syndrome in 5-to 10-year-old overweight/obese African-American children. Diabetes Care 2001 24 13591364. (https://doi.org/10.2337/diacare.24.8.1359)

    • Search Google Scholar
    • Export Citation
  • 26

    Hall E, Volkov P, Dayeh T, Esguerra JLS, Salo S, Eliasson L, Ronn T, Bacos K & Ling C Sex differences in the genome-wide DNA methylation pattern and impact on gene expression, microRNA levels and insulin secretion in human pancreatic islets. Genome Biology 2014 15 522. (https://doi.org/10.1186/s13059-014-0522-z)

    • Search Google Scholar
    • Export Citation
  • 27

    Kodama K, Tojjar D, Yamada S, Toda K, Patel CJ & Butte AJ Ethnic differences in the relationship between insulin sensitivity and insulin response: a systematic review and meta-analysis. Diabetes Care 2013 36 17891796. (https://doi.org/10.2337/dc12-1235)

    • Search Google Scholar
    • Export Citation
  • 28

    Behl M, Rao D, Aagaard K, Davidson TL, Levin ED, Slotkin TA, Srinivasan S, Wallinga D, White MF & Walker VR Evaluation of the association between maternal smoking, childhood obesity, and metabolic disorders: a national toxicology program workshop review. Environmental Health Perspectives 2013 121 170180. (https://doi.org/10.1289/ehp.1205404)

    • Search Google Scholar
    • Export Citation
  • 29

    Rogers JM Smoking and pregnancy: epigenetics and developmental origins of the metabolic syndrome. Birth Defects Research 2019 111 12591269. (https://doi.org/10.1002/bdr2.1550)

    • Search Google Scholar
    • Export Citation
  • 30

    Fang F, Luo ZC, Dejemli A, Delvin E & Zhang J Maternal smoking and metabolic health biomarkers in newborns. PLoS ONE 2015 10 e0143660. (https://doi.org/10.1371/journal.pone.0143660)

    • Search Google Scholar
    • Export Citation
  • 31

    Owen CG, Martin RM, Whincup PH, Smith GD & Cook DG Does breastfeeding influence risk of type 2 diabetes in later life? A quantitative analysis of published evidence. American Journal of Clinical Nutrition 2006 84 104310 54. (https://doi.org/10.1093/ajcn/84.5.1043)

    • Search Google Scholar
    • Export Citation
  • 32

    Brown RJ & Yanovski JA Estimation of insulin sensitivity in children: methods, measures and controversies. Pediatric Diabetes 2014 15 151161. (https://doi.org/10.1111/pedi.12146)

    • Search Google Scholar
    • Export Citation
  • 33

    Gungor N, Saad R, Janosky J & Arslanian S Validation of surrogate estimates of insulin sensitivity and insulin secretion in children and adolescents. Journal of Pediatrics 2004 144 4755. (https://doi.org/10.1016/j.jpeds.2003.09.045)

    • Search Google Scholar
    • Export Citation