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Pediatrics

Associations of prenatal exposure to impaired glucose tolerance with eating in the absence of hunger in early adolescence

Abstract

Objective

Exposure to impaired gestational glucose tolerance has been shown to have sex-specific associations with offspring obesity risk, perhaps by affecting the development of appetite regulation. We examined the extent to which prenatal exposure to impaired glucose tolerance was associated with eating in the absence of hunger (EAH) in early adolescent offspring, and in turn, whether EAH was cross-sectionally associated with body composition.

Methods

We included data from 1097 adolescents participating in Project Viva, a pre-birth longitudinal cohort. We obtained the results of two-stage prenatal glycemic screening (50 g glucose challenge test, followed if abnormal by 100 g oral glucose tolerance test) at 26–28 weeks of gestation, and categorized mothers as having normal glucose tolerance, isolated hyperglycemia (IH, n = 92, 8.4%), impaired glucose tolerance (IGT, n = 36, 3.3%), or gestational diabetes mellitus (GDM, n = 52, 4.7%). At a median age of 13 years, offspring reported on two modified items of the Eating in the Absence of Hunger in Children and Adolescents questionnaire, we measured height and weight, and performed dual X-ray absorptiometry scans to assess fat and fat-free mass. We used multivariable linear regression analyses adjusted for sociodemographic and prenatal covariates, including maternal pre-pregnancy BMI.

Results

On a ten-point scale, the mean (SD) EAH score was 4.4 points (SD = 1.5) in boys and 4.4 (SD = 1.4) in girls. In girls, prenatal exposure to both IH and IGT was associated with more EAH compared with normal glucose tolerance (e.g., for IH: 0.56 points, 95% CI: 0.17, 0.96), whereas in boys, prenatal exposure to IGT was associated with less EAH (–0.81 points, 95% CI: −1.41, −0.21). We did not observe an association between exposure to GDM and EAH, nor did we observe associations between EAH and body composition in early adolescence.

Conclusions

These findings suggest sex-specific associations of exposure to impaired gestational glucose tolerance with offspring EAH in early adolescence.

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References

  1. 1.

    Ferrara A. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care. 2007;30(Suppl 2):S141–6.

    Article  Google Scholar 

  2. 2.

    DeSisto CL, Kim SY, Sharma AJ. Prevalence estimates of gestational diabetes mellitus in the United States, Pregnancy Risk Assessment Monitoring System (PRAMS), 2007-2010. Prev Chronic Dis. 2014;11:E104.

    Article  Google Scholar 

  3. 3.

    Lavery JA, Friedman AM, Keyes KM, Wright JD, Ananth CV. Gestational diabetes in the United States: temporal changes in prevalence rates between 1979 and 2010. BJOG. 2017;124:804–13.

    CAS  Article  Google Scholar 

  4. 4.

    Page KA, Romero A, Buchanan TA, Xiang AH. Gestational diabetes mellitus, maternal obesity, and adiposity in offspring. J Pediatr. 2014;164:807–10.

    Article  Google Scholar 

  5. 5.

    Gillman MW, Rifas-Shiman S, Berkey CS, Field AE, Colditz GA. Maternal gestational diabetes, birth weight, and adolescent obesity. Pediatrics. 2003;111:e221–6.

    Article  Google Scholar 

  6. 6.

    Zhao YL, Ma RM, Lao TT, Chen Z, Du MY, Liang K, et al. Maternal gestational diabetes mellitus and overweight and obesity in offspring: a study in Chinese children. J Dev Orig Health Dis. 2015;6:479–84.

    CAS  Article  Google Scholar 

  7. 7.

    Kim SY, England JL, Sharma JA, Njoroge T. Gestational diabetes mellitus and risk of childhood overweight and obesity in offspring: a systematic review. Exp Diabetes Res. 2011;2011:541308.

    Article  Google Scholar 

  8. 8.

    Regnault N, Gillman MW, Rifas-Shiman SL, Eggleston E, Oken E. Sex-specific associations of gestational glucose tolerance with childhood body composition. Diabetes Care. 2013;36:3045–53.

    CAS  Article  Google Scholar 

  9. 9.

    Franks PW, Looker HC, Kobes S, Touger L, Tataranni PA, Hanson RL, et al. Gestational glucose tolerance and risk of type 2 diabetes in young Pima Indian offspring. Diabetes. 2006;55:460–5.

    CAS  Article  Google Scholar 

  10. 10.

    Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP. Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001;185:73–9.

    CAS  Article  Google Scholar 

  11. 11.

    Neary NM, Goldstone AP, Bloom SR. Appetite regulation: from the gut to the hypothalamus. Clin Endocrinol (Oxf). 2004;60:153–60.

    Article  Google Scholar 

  12. 12.

    Langley-Evans SC, Bellinger L, McMullen S. Animal models of programming: early life influences on appetite and feeding behaviour. Matern Child Nutr. 2005;1:142–8.

    Article  Google Scholar 

  13. 13.

    Steculorum SM, Bouret SG. Maternal diabetes compromises the organization of hypothalamic feeding circuits and impairs leptin sensitivity in offspring. Endocrinology. 2011;152:4171–9.

    CAS  Article  Google Scholar 

  14. 14.

    Muhlhausler BS, Duffield JA, McMillen IC. Increased maternal nutrition increases leptin expression in perirenal and subcutaneous adipose tissue in the postnatal lamb. Endocrinology. 2007;148:6157–63.

    CAS  Article  Google Scholar 

  15. 15.

    Ornellas F, Souza-Mello V, Mandarim-de-Lacerda CA, Aguila MB. Combined parental obesity augments single-parent obesity effects on hypothalamus inflammation, leptin signaling (JAK/STAT), hyperphagia, and obesity in the adult mice offspring. Physiol Behav. 2016;153:47–55.

    CAS  Article  Google Scholar 

  16. 16.

    Morris MJ, Chen H. Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int J Obes (Lond). 2009;33:115–22.

    CAS  Article  Google Scholar 

  17. 17.

    Fisher JO, Birch LL. Restricting access to foods and children’s eating. Appetite. 1999;32:405–19.

    CAS  Article  Google Scholar 

  18. 18.

    Lansigan RK, Emond JA, Gilbert-Diamond D. Understanding eating in the absence of hunger among young children: a systematic review of existing studies. Appetite. 2015;85:36–47.

    Article  Google Scholar 

  19. 19.

    Francis LA, Ventura AK, Marini M, Birch LL. Parent overweight predicts daughters’ increase in BMI and disinhibited overeating from 5 to 13 years. Obes (Silver Spring). 2007;15:1544–53.

    Article  Google Scholar 

  20. 20.

    Faith MS, Berkowitz RI, Stallings VA, Kerns J, Storey M, Stunkard AJ. Eating in the absence of hunger: a genetic marker for childhood obesity in prepubertal boys? Obes (Silver Spring). 2006;14:131–8.

    Article  Google Scholar 

  21. 21.

    Wardle J, Guthrie C, Sanderson S, Birch L, Plomin R. Food and activity preferences in children of lean and obese parents. Int J Obes Relat Metab Disord. 2001;25:971–7.

    CAS  Article  Google Scholar 

  22. 22.

    Shapiro ALB, Sauder KA, Tregellas JR, Legget KT, Gravitz SL, Ringham BM, et al. Exposure to maternal diabetes in utero and offspring eating behavior: The EPOCH study. Appetite. 2017;116:610–5.

    Article  Google Scholar 

  23. 23.

    Fisher JO, Cai G, Jaramillo SJ, Cole SA, Comuzzie AG, Butte NF. Heritability of hyperphagic eating behavior and appetite-related hormones among Hispanic children. Obesity. 2007;15:1484–95.

    Article  Google Scholar 

  24. 24.

    Oken E, Baccarelli AA, Gold DR, Kleinman KP, Litonjua AA, De Meo D, et al. Cohort profile: project viva. Int J Epidemiol. 2015;44:37–48.

    Article  Google Scholar 

  25. 25.

    Wright CS, Rifas-Shiman SL, Rich-Edwards JW, Taveras EM, Gillman MW, Oken E. Intrauterine exposure to gestational diabetes, child adiposity, and blood pressure. Am J Hypertens. 2009;22:215–20.

    Article  Google Scholar 

  26. 26.

    Tanofsky-Kraff M, Ranzenhofer LM, Yanovski SZ, Schvey NA, Faith M, Gustafson J, et al. Psychometric properties of a new questionnaire to assess eating in the absence of hunger in children and adolescents. Appetite. 2008;51:148–55.

    Article  Google Scholar 

  27. 27.

    Rifas-Shiman SL, Willett WC, Lobb R, Kotch J, Dart C, Gillman MW. PrimeScreen, a brief dietary screening tool: reproducibility and comparability with both a longer food frequency questionnaire and biomarkers. Public Health Nutr. 2001;4:249–54.

    CAS  Article  Google Scholar 

  28. 28.

    Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat. Series 11, 2002;246:1–190.

  29. 29.

    Willett W. Nutritional Epidemiology. 2. New York, NY: Oxford University Press; 1998.

    Book  Google Scholar 

  30. 30.

    Lange NE, Rifas-Shiman SL, Camargo CA Jr., Gold DR, Gillman MW, Litonjua AA. Maternal dietary pattern during pregnancy is not associated with recurrent wheeze in children. J Allergy Clin Immunol. 2010;126:250–5. 5 e1-4

    Article  Google Scholar 

  31. 31.

    Fawzi WW, Rifas-Shiman SL, Rich-Edwards JW, Willett WC, Gillman MW. Calibration of a semi-quantitative food frequency questionnaire in early pregnancy. Ann Epidemiol. 2004;14:754–62.

    Article  Google Scholar 

  32. 32.

    Oken E, Kleinman KP, Rich-Edwards J, Gillman MW. A nearly continuous measure of birth weight for gestational age using a United States national reference. BMC Pediatr. 2003;3:6.

    Article  Google Scholar 

  33. 33.

    VanderWeele TJ, Mumford SL, Schisterman EF. Conditioning on intermediates in perinatal epidemiology. Epidemiology. 2012;23:1–9.

    Article  Google Scholar 

  34. 34.

    Gingras V, Rifas-Shiman SL, Derks IPM, Aris IM, Oken E, Hivert MF. Associations of Gestational Glucose Tolerance with Offspring Body Composition and Estimated Insulin Resistance in Early Adolescence. Diabetes Care. 2018. https://doi.org/10.2337/dc18-1490 [e-pub ahead of print].

  35. 35.

    Regnault N, Botton J, Heude B, Forhan A, Hankard R, Foliguet B, et al. Higher cord C-peptide concentrations are associated with slower growth rate in the 1st year of life in girls but not in boys. Diabetes. 2011;60:2152–9.

    CAS  Article  Google Scholar 

  36. 36.

    O’Tierney-Ginn P, Presley L, Minium J, Hauguel deMouzon S, Catalano PM. Sex-specific effects of maternal anthropometrics on body composition at birth. Am J Obstet Gynecol. 2014;211:292 e1–9.

    Article  Google Scholar 

  37. 37.

    Landon MB, Rice MM, Varner MW, Casey BM, Reddy UM, Wapner RJ, et al. Mild gestational diabetes mellitus and long-term child health. Diabetes Care. 2015;38:445–52.

    Article  Google Scholar 

  38. 38.

    Okereke NC, Uvena-Celebrezze J, Hutson-Presley L, Amini SB, Catalano PM. The effect of gender and gestational diabetes mellitus on cord leptin concentration. Am J Obstet Gynecol. 2002;187:798–803.

    CAS  Article  Google Scholar 

  39. 39.

    Kostalova L, Leskova L, Kapellerova A, Strbak V. Body mass, plasma leptin, glucose, insulin and C-peptide in offspring of diabetic and non-diabetic mothers. Eur J Endocrinol. 2001;145:53–8.

    CAS  Article  Google Scholar 

  40. 40.

    Oken E, Morton-Eggleston E, Rifas-Shiman SL, Switkowski KM, Hivert MF, Fleisch AF, et al. Sex-Specific Associations of Maternal Gestational Glycemia with Hormones in Umbilical Cord Blood at Delivery. Am J Perinatol. 2016;33:1273–81.

    Article  Google Scholar 

  41. 41.

    Allard C, Desgagne V, Patenaude J, Lacroix M, Guillemette L, Battista MC, et al. Mendelian randomization supports causality between maternal hyperglycemia and epigenetic regulation of leptin gene in newborns. Epigenetics. 2015;10:342–51.

    CAS  Article  Google Scholar 

  42. 42.

    De Silva A, Salem V, Matthews PM, Dhillo WS. The Use of Functional MRI to Study Appetite Control in the CNS. Experimental Diabetes Res 2012;2012:1–13.

  43. 43.

    Birch LL, Fisher JO, Davison KK. Learning to overeat: maternal use of restrictive feeding practices promotes girls’ eating in the absence of hunger. Am J Clin Nutr. 2003;78:215–20.

    CAS  Article  Google Scholar 

  44. 44.

    Fisher JO, Birch LL. Eating in the absence of hunger and overweight in girls from 5 to 7 y of age. Am J Clin Nutr. 2002;76:226–31.

    CAS  Article  Google Scholar 

  45. 45.

    Shunk JA, Birch LL. Girls at risk for overweight at age 5 are at risk for dietary restraint, disinhibited overeating, weight concerns, and greater weight gain from 5 to 9 years. J Am Diet Assoc. 2004;104:1120–6.

    Article  Google Scholar 

  46. 46.

    Francis LA, Birch LL. Maternal weight status modulates the effects of restriction on daughters’ eating and weight. Int J Obes (Lond). 2005;29:942–9.

    CAS  Article  Google Scholar 

  47. 47.

    Moens E, Braet C. Predictors of disinhibited eating in children with and without overweight. Behav Res Ther. 2007;45:1357–68.

    Article  Google Scholar 

  48. 48.

    Hill C, Llewellyn CH, Saxton J, Webber L, Semmler C, Carnell S, et al. Adiposity and ‘eating in the absence of hunger’ in children. Int J Obes (Lond). 2008;32:1499–505.

    CAS  Article  Google Scholar 

  49. 49.

    Butte NF, Cai G, Cole SA, Wilson TA, Fisher JO, Zakeri IF, et al. Metabolic and behavioral predictors of weight gain in Hispanic children: the Viva la Familia Study. Am J Clin Nutr. 2007;85:1478–85.

    CAS  Article  Google Scholar 

  50. 50.

    Kelly NR, Shomaker LB, Pickworth CK, Brady SM, Courville AB, Bernstein S, et al. A prospective study of adolescent eating in the absence of hunger and body mass and fat mass outcomes. Obes (Silver Spring). 2015;23:1472–8.

    Article  Google Scholar 

  51. 51.

    Madowitz J, Liang J, Peterson CB, Rydell S, Zucker NL, Tanofsky-Kraff M, et al. Concurrent and convergent validity of the eating in the absence of hunger questionnaire and behavioral paradigm in overweight children. Int J Eat Disord. 2014;47:287–95.

    Article  Google Scholar 

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Acknowledgements

Project Viva is supported by the National Institutes of Health (R01 HD034568, UG3OD023286). We appreciate the dedication of Project Viva participants and staff. This study was supported by the Dutch KNAW Ter Meulen Foundation. PWJ is supported by the Dutch Diabetes Foundation (grant number: 2013.81.1664).

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Correspondence to Ivonne P. M. Derks.

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Derks, I.P.M., Hivert, MF., Rifas-Shiman, S.L. et al. Associations of prenatal exposure to impaired glucose tolerance with eating in the absence of hunger in early adolescence. Int J Obes 43, 1903–1913 (2019). https://doi.org/10.1038/s41366-018-0296-6

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