Generation of Maternal Obesity Models in Studies of Developmental Programming in Rodents

  • Paul D. TaylorEmail author
  • Phillippa A. Matthews
  • Imran Y. Khan
  • Douglas Rees
  • Nozomi Itani
  • Lucilla Poston
Part of the Methods in Molecular Biology book series (MIMB, volume 1735)


Mother-child cohort studies have established that both pre-pregnancy body mass index (BMI) and gestational weight gain (GWG) are independently associated with cardio-metabolic risk factors in juvenile and adult offspring, including systolic and diastolic blood pressure. In rodent studies maternal obesity confers many facets of the metabolic syndrome including a persistent sympathy-excitatory hyperresponsiveness and hypertension acquired in the early stages of development. Insight from these animal models raises the possibility that early life exposure to the nutritional and hormonal environment of obesity in pregnancy in humans may lead to early onset of metabolic syndrome and/or essential hypertension. This chapter will address the development of rodent models of maternal overnutrition and obesity, which have proved invaluable in generating testable hypotheses for clinical translation and the development of intervention strategies to stem the swelling tide of obesity and its comorbidities predicted for future generations.

Key words

Maternal obesity Developmental programming Rodents Diet Metabolic syndrome 



This work was funded by the British Heart Foundation and the EU Framework 6 Project, EARNEST.


  1. 1.
    Reynolds RM, Allan KM, Raja EA, Bhattacharya S, McNeill G, Hannaford PC et al (2013) Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ 347:f4539. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Poston L (2012) Maternal obesity, gestational weight gain and diet as determinants of offspring long term health. Best Pract Res Clin Endocrinol Metab 26(5):627–639CrossRefPubMedGoogle Scholar
  3. 3.
    O’Reilly JR, Reynolds RM (2013) The risk of maternal obesity to the long-term health of the offspring. Clin Endocrinol 78(1):9–16CrossRefGoogle Scholar
  4. 4.
    Drake AJ, Reynolds RM (2010) Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 140(3):387–598CrossRefPubMedGoogle Scholar
  5. 5.
    Heslehurst N, Rankin J, Wilkinson JR, Summerbell CD (2010) A nationally representative study of maternal obesity in England, UK: trends in incidence and demographic inequalities in 619 323 births, 1989–2007. Int J Obes 34(3):420–428CrossRefGoogle Scholar
  6. 6.
    Heslehurst N, Simpson H, Ells LJ, Rankin J, Wilkinson J, Lang R et al (2008) The impact of maternal BMI status on pregnancy outcomes with immediate short-term obstetric resource implications: a meta-analysis. Obes Rev 9(6):635–683CrossRefPubMedGoogle Scholar
  7. 7.
    Castillo-Laura H, Santos IS, Quadros LC, Matijasevich A (2015) Maternal obesity and offspring body composition by indirect methods: a systematic review and meta-analysis. Cad Saude Publica 31(10):2073–2092. CrossRefPubMedGoogle Scholar
  8. 8.
    Catalano P, deMouzon SH (2015) Maternal obesity and metabolic risk to the offspring: why lifestyle interventions may have not achieved the desired outcomes. Int J Obes 39(4):642–649CrossRefGoogle Scholar
  9. 9.
    Zhao YL, Ma RM, Lao TT, Chen Z, Du MY, Liang K et al (2015) Maternal gestational diabetes mellitus and overweight and obesity in offspring: a study in Chinese children. J Dev Orig Health Dis 6(6):479–484CrossRefPubMedGoogle Scholar
  10. 10.
    Yu Z, Han S, Zhu J, Sun X, Ji C, Guo X (2013) Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: a systematic review and meta-analysis. PLoS One 8(4):e61627. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gaillard R, Steegers EA, Duijts L, Felix JF, Hofman A, Franco OH et al (2014) Childhood cardiometabolic outcomes of maternal obesity during pregnancy: the generation R study. Hypertension 63(4):683–691CrossRefPubMedGoogle Scholar
  12. 12.
    Gaillard R, Steegers EA, Franco OH, Hofman A, Jaddoe VW (2015) Maternal weight gain in different periods of pregnancy and childhood cardio-metabolic outcomes. The generation R study. Int J Obes 39(4):677–685CrossRefGoogle Scholar
  13. 13.
    Fraser A, Tilling K, Macdonald-Wallis C, Sattar N, Brion MJ, Benfield L et al (2010) Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood. Circulation 121(23):2557–2564CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Oostvogels AJ, Stronks K, Roseboom TJ, van der Post JA, van Eijsden M, Vrijkotte TG (2014) Maternal prepregnancy BMI, offspring’s early postnatal growth, and metabolic profile at age 5-6 years: the ABCD study. J Clin Endocrinol Metab 99(10):3845–3854CrossRefPubMedGoogle Scholar
  15. 15.
    Hochner H, Friedlander Y, Calderon-Margalit R, Meiner V, Sagy Y, Avgil-Tsadok M et al (2012) Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem perinatal family follow-up study. Circulation 125(11):1381–1389CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Gademan MG, van Eijsden M, Roseboom TJ, van der Post JA, Stronks K, Vrijkotte TG (2013) Maternal prepregnancy body mass index and their children’s blood pressure and resting cardiac autonomic balance at age 5 to 6 years. Hypertension 62(3):641–647CrossRefPubMedGoogle Scholar
  17. 17.
    Filler G, Yasin A, Kesarwani P, Garg AX, Lindsay R, Sharma AP (2011) Big mother or small baby: which predicts hypertension? J Clin Hypertens (Greenwich) 13(1):35–41CrossRefGoogle Scholar
  18. 18.
    Wen X, Triche EW, Hogan JW, Shenassa ED, Buka SL (2011) Prenatal factors for childhood blood pressure mediated by intrauterine and/or childhood growth? Pediatrics 127(3):e713–e721CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Taylor PD, Samuelsson AM, Poston L (2014) Maternal obesity and the developmental programming of hypertension: a role for leptin. Acta Physiol (Oxf) 210(3):508–523CrossRefGoogle Scholar
  20. 20.
    Karachaliou M, Georgiou V, Roumeliotaki T, Chalkiadaki G, Daraki V, Koinaki S et al (2015) Association of trimester-specific gestational weight gain with fetal growth, offspring obesity, and cardiometabolic traits in early childhood. Am J Obstet Gynecol 212(4):502 e1–502 14CrossRefGoogle Scholar
  21. 21.
    Basak S, Duttaroy AK (2012) Leptin induces tube formation in first-trimester extravillous trophoblast cells. Eur J Obstet Gynecol Reprod Biol 164(1):24–29CrossRefPubMedGoogle Scholar
  22. 22.
    Samolis S, Papastefanou I, Panagopoulos P, Galazios G, Kouskoukis A, Maroulis G (2010) Relation between first trimester maternal serum leptin levels and body mass index in normotensive and pre-eclamptic pregnancies—role of leptin as a marker of pre-eclampsia: a prospective case-control study. Gynecol Endocrinol 26(5):338–343CrossRefPubMedGoogle Scholar
  23. 23.
    Kral JG, Biron S, Simard S, Hould FS, Lebel S, Marceau S et al (2006) Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 118(6):e1644–e1649CrossRefPubMedGoogle Scholar
  24. 24.
    Smith J, Cianflone K, Biron S, Hould FS, Lebel S, Marceau S et al (2009) Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab 94(11):4275–4283CrossRefPubMedGoogle Scholar
  25. 25.
    Guenard F, Deshaies Y, Cianflone K, Kral JG, Marceau P, Vohl MC (2013) Differential methylation in glucoregulatory genes of offspring born before vs. after maternal gastrointestinal bypass surgery. Proc Natl Acad Sci U S A 110(28):11439–11444CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Guenard F, Lamontagne M, Bosse Y, Deshaies Y, Cianflone K, Kral JG et al (2015) Influences of gestational obesity on associations between genotypes and gene expression levels in offspring following maternal gastrointestinal bypass surgery for obesity. PLoS One 10(1):e0117011. CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Guenard F, Tchernof A, Deshaies Y, Cianflone K, Kral JG, Marceau P et al (2013) Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients. J Obes 2013:492170. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Patel N, Godfrey KM, Pasupathy D, Levin J, Flynn AC, Hayes L et al (2017) Infant adiposity following a randomised controlled trial of a behavioural intervention in obese pregnancy. Int J Obes 41(7):1018–1026CrossRefGoogle Scholar
  29. 29.
    Palinski W, D’Armiento FP, Witztum JL, de Nigris F, Casanada F, Condorelli M et al (2001) Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res 89(11):991–996CrossRefPubMedGoogle Scholar
  30. 30.
    Napoli C, Witztum JL, Calara F, de Nigris F, Palinski W (2000) Maternal hypercholesterolemia enhances atherogenesis in normocholesterolemic rabbits, which is inhibited by antioxidant or lipid-lowering intervention during pregnancy: an experimental model of atherogenic mechanisms in human fetuses. Circ Res 87(10):946–952CrossRefPubMedGoogle Scholar
  31. 31.
    Khan IY, Taylor PD, Dekou V, Seed PT, Lakasing L, Graham D et al (2003) Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41(1):168–175CrossRefPubMedGoogle Scholar
  32. 32.
    Khan IY, Dekou V, Hanson M, Poston L, Taylor PD (2004) Predictive adaptive responses to maternal high fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation 110(9):1097–1102CrossRefPubMedGoogle Scholar
  33. 33.
    Ghosh P, Bitsanis D, Ghebremeskel K, Crawford MA, Poston L (2001) Abnormal aortic fatty acid composition and small artery function in offspring of rats fed a high fat diet in pregnancy. J Physiol 533(Pt 3):815–822CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Robb JL, Messa I, Lui E, Yeung D, Thacker J, Satvat E et al (2017) A maternal diet high in saturated fat impairs offspring hippocampal function in a sex-specific manner. Behav Brain Res 326:187–199CrossRefPubMedGoogle Scholar
  35. 35.
    Tamashiro KL, Terrillion CE, Hyun J, Koenig JI, Moran TH (2009) Prenatal stress or high-fat diet increases susceptibility to diet-induced obesity in rat offspring. Diabetes 58(5):1116–1125CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Chen H, Simar D, Lambert K, Mercier J, Morris MJ (2008) Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology 149(11):5348–5356CrossRefPubMedGoogle Scholar
  37. 37.
    Srinivasan M, Katewa SD, Palaniyappan A, Pandya JD, Patel MS (2006) Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 291(4):E792–E799CrossRefPubMedGoogle Scholar
  38. 38.
    Koukkou E, Ghosh P, Lowy C, Poston L (1998) Offspring of normal and diabetic rats fed saturated fat in pregnancy demonstrate vascular dysfunction. Circulation 98(25):2899–2904CrossRefPubMedGoogle Scholar
  39. 39.
    Howie GJ, Sloboda DM, Kamal T, Vickers MH (2009) Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol 587(Pt 4):905–915CrossRefPubMedGoogle Scholar
  40. 40.
    Ferezou-Viala J, Roy AF, Serougne C, Gripois D, Parquet M, Bailleux V et al (2007) Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 293(3):R1056–R1062CrossRefPubMedGoogle Scholar
  41. 41.
    Cerf ME, Muller CJ, Du Toit DF, Louw J, Wolfe-Coote SA (2006) Hyperglycaemia and reduced glucokinase expression in weanling offspring from dams maintained on a high-fat diet. Br J Nutr 95(2):391–396CrossRefPubMedGoogle Scholar
  42. 42.
    Buckley AJ, Keseru B, Briody J, Thompson M, Ozanne SE, Thompson CH (2005) Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism 54(4):500–507CrossRefPubMedGoogle Scholar
  43. 43.
    Cerf ME, Williams K, Nkomo XI, Muller CJ, Du Toit DF, Louw J et al (2005) Islet cell response in the neonatal rat after exposure to a high-fat diet during pregnancy. Am J Physiol Regul Integr Comp Physiol 288(5):R1122–R1128CrossRefPubMedGoogle Scholar
  44. 44.
    Gregersen S, Dyrskog SE, Storlien LH, Hermansen K (2005) Comparison of a high saturated fat diet with a high carbohydrate diet during pregnancy and lactation: effects on insulin sensitivity in offspring of rats. Metabolism 54(10):1316–1322CrossRefPubMedGoogle Scholar
  45. 45.
    Guo F, Jen KL (1995) High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol Behav 57(4):681–686CrossRefPubMedGoogle Scholar
  46. 46.
    MacDonald KD, Moran AR, Scherman AJ, McEvoy CT, Platteau AS (2017) Maternal high-fat diet in mice leads to innate airway hyperresponsiveness in the adult offspring. Physiol Rep 5(5). pii: e13082. doi:
  47. 47.
    Ito J, Nakagawa K, Kato S, Miyazawa T, Kimura F, Miyazawa T (2016) The combination of maternal and offspring high-fat diets causes marked oxidative stress and development of metabolic syndrome in mouse offspring. Life Sci 151:70–75CrossRefPubMedGoogle Scholar
  48. 48.
    Taylor PD, Khan IY, Lakasing L, Dekou V, O’Brien-Coker I, Mallet AI et al (2003) Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp Physiol 88(3):389–398CrossRefPubMedGoogle Scholar
  49. 49.
    Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L (2004) Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol 561(Pt 2):355–377CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Taylor PD, Khan IY, Hanson MA, Poston L (2004) Impaired EDHF-mediated vasodilatation in adult offspring of rats exposed to a fat-rich diet in pregnancy. J Physiol 558(Pt 3):943–951CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Taylor PD, McConnell J, Khan IY, Holemans K, Lawrence KM, Asare-Anane H et al (2005) Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol 288(1):R134–R139CrossRefPubMedGoogle Scholar
  52. 52.
    Sanchez J, Priego T, Garcia AP, Llopis M, Palou M, Pico C et al (2012) Maternal supplementation with an excess of different fat sources during pregnancy and lactation differentially affects feeding behavior in offspring: putative role of the leptin system. Mol Nutr Food Res 56:1715–1728Google Scholar
  53. 53.
    Sun B, Purcell RH, Terrillion CE, Yan J, Moran TH, Tamashiro KL (2012) Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes 61:2833–2841CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Bayol SA, Farrington SJ, Stickland NC (2007) A maternal ‘junk food’ diet in pregnancy and lactation promotes an exacerbated taste for ‘junk food’ and a greater propensity for obesity in rat offspring. Br J Nutr 98(4):843–851CrossRefPubMedGoogle Scholar
  55. 55.
    Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT et al (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring) 19:1109–1117Google Scholar
  56. 56.
    Akyol A, Langley-Evans SC, McMullen S (2009) Obesity induced by cafeteria feeding and pregnancy outcome in the rat. Br J Nutr 102(11):1601–1610CrossRefPubMedGoogle Scholar
  57. 57.
    Morris MJ, Chen H, Watts R, Shulkes A, Cameron-Smith D (2008) Brain neuropeptide Y and CCK and peripheral adipokine receptors: temporal response in obesity induced by palatable diet. Int J Obes (Lond) 32:249–258CrossRefGoogle Scholar
  58. 58.
    Pomar CA, van Nes R, Sanchez J, Pico C, Keijer J, Palou A (2017) Maternal consumption of a cafeteria diet during lactation in rats leads the offspring to a thin-outside-fat-inside phenotype. Int J Obes 41:1279. CrossRefGoogle Scholar
  59. 59.
    Jacobs S, Teixeira DS, Guilherme C, da Rocha CF, Aranda BC, Reis AR et al (2014) The impact of maternal consumption of cafeteria diet on reproductive function in the offspring. Physiol Behav 129:280–286CrossRefPubMedGoogle Scholar
  60. 60.
    Chen H, Morris MJ (2009) Differential responses of orexigenic neuropeptides to fasting in offspring of obese mothers. Obesity (Silver Spring) 17:1356–1362Google Scholar
  61. 61.
    Castro H, Pomar CA, Palou A, Pico C, Sanchez J (2017) Offspring predisposition to obesity due to maternal-diet-induced obesity in rats is preventable by dietary normalization before mating. Mol Nutr Food Res 61(3).
  62. 62.
    Akyol A, McMullen S, Langley-Evans SC (2012) Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr 107(7):964–978CrossRefPubMedGoogle Scholar
  63. 63.
    Mucellini AB, Goularte JF, de Araujo d, Cunha AC, Caceres RC, Noschang C et al (2014) Effects of exposure to a cafeteria diet during gestation and after weaning on the metabolism and body weight of adult male offspring in rats. Br J Nutr 111(8):1499–1506Google Scholar
  64. 64.
    Ong ZY, Muhlhausler BS (2014) Consuming a low-fat diet from weaning to adulthood reverses the programming of food preferences in male, but not in female, offspring of ‘junk food’-fed rat dams. Acta Physiol 210(1):127–141CrossRefGoogle Scholar
  65. 65.
    Bouanane S, Benkalfat NB, Baba Ahmed FZ, Merzouk H, Mokhtari NS, Merzouk SA et al (2009) Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring. Clin Sci (Lond) 116(8):669–680CrossRefGoogle Scholar
  66. 66.
    Sanchez-Blanco C, Amusquivar E, Bispo K, Herrera E (2016) Influence of cafeteria diet and fish oil in pregnancy and lactation on pups’ body weight and fatty acid profiles in rats. Eur J Nutr 55(4):1741–1753CrossRefPubMedGoogle Scholar
  67. 67.
    Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M et al (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9(10):577–589CrossRefPubMedGoogle Scholar
  69. 69.
    Lepage P, Leclerc MC, Joossens M, Mondot S, Blottiere HM, Raes J et al (2013) A metagenomic insight into our gut’s microbiome. Gut 62(1):146–158CrossRefPubMedGoogle Scholar
  70. 70.
    Bajzer M, Seeley RJ (2006) Physiology: obesity and gut flora. Nature 444(7122):1009–1010CrossRefPubMedGoogle Scholar
  71. 71.
    Dahlen HG, Downe S, Kennedy HP, Foureur M (2014) Is society being reshaped on a microbiological and epigenetic level by the way women give birth? Midwifery 30(12):1149–1151CrossRefPubMedGoogle Scholar
  72. 72.
    Dahlen HG, Kennedy HP, Anderson CM, Bell AF, Clark A, Foureur M et al (2013) The EPIIC hypothesis: intrapartum effects on the neonatal epigenome and consequent health outcomes. Med Hypotheses 80(5):656–662CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Hyde MJ, Mostyn A, Modi N, Kemp PR (2012) The health implications of birth by caesarean section. Biol Rev Camb Philos Soc 87(1):229–243CrossRefPubMedGoogle Scholar
  74. 74.
    Mueller NT, Whyatt R, Hoepner L, Oberfield S, Dominguez-Bello MG, Widen EM et al (2015) Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int J Obes 39(4):665–670CrossRefGoogle Scholar
  75. 75.
    Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S et al (2010) Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328(5975):228–231CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA et al (2011) Linking long-term dietary patterns with gut microbial enterotypes. Science 334(6052):105–108CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X et al (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5(2):220–230CrossRefPubMedGoogle Scholar
  78. 78.
    David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE et al (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505(7484):559–563CrossRefPubMedGoogle Scholar
  79. 79.
    Armitage JA, Taylor PD, Poston L (2005) Experimental models of developmental programming; consequences of exposure to an energy rich diet during development. J Physiol 565(Pt 1):3–8CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Erlanson-Albertsson C (2005) Appetite regulation and energy balance. Acta Paediatr Suppl 94(448):40–41CrossRefPubMedGoogle Scholar
  81. 81.
    Zhang M, Balmadrid C, Kelley AE (2003) Nucleus accumbens opioid, GABaergic, and dopaminergic modulation of palatable food motivation: contrasting effects revealed by a progressive ratio study in the rat. Behav Neurosci 117(2):202–211CrossRefPubMedGoogle Scholar
  82. 82.
    Ramsay JE, Greer I, Sattar N (2006) ABC of obesity. Obesity and reproduction. BMJ 333(7579):1159–1162CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Brand-Miller JC, Holt SH, Pawlak DB, Mcmillan J (2002) Glycemic index and obesity. Am J Clin Nutr 76:281S–285SCrossRefPubMedGoogle Scholar
  84. 84.
    Schulze MB, Liu S, Rimm EB, Manson JE, Willett WC, Hu FB (2004) Glycemic index, glycemic load, and dietary fiber intake and incidence of type 2 diabetes in younger and middle-aged women. Am J Clin Nutr 80:348–356PubMedGoogle Scholar
  85. 85.
    Wang Jensen B, Nichols M, Allender S, de Silva-Sanigorski A, Millar L, Kremer P et al (2012) Consumption patterns of sweet drinks in a population of Australian children and adolescents (2003–2008). BMC Public Health 12:771Google Scholar
  86. 86.
    Nikpartow N, Danyliw AD, Whiting SJ, Lim H, Vatanparast H (2012) Fruit drink consumption is associated with overweight and obesity in Canadian women. Can J Public Health 103:178–182PubMedGoogle Scholar
  87. 87.
    Zhang C, Liu S, Solomon CG, Hu FB (2006) Dietary fiber intake, dietary glycemic load, and the risk for gestational diabetes mellitus. Diabetes Care 29:2223–2230CrossRefPubMedGoogle Scholar
  88. 88.
    Walsh JM, McGowan CA, Mahony R, Foley ME, McAuliffe FM (2012) Low glycaemic index diet in pregnancy to prevent macrosomia (ROLO study): randomised control trial. BMJ 345:e5605CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2018

Authors and Affiliations

  • Paul D. Taylor
    • 1
    Email author
  • Phillippa A. Matthews
    • 1
  • Imran Y. Khan
    • 1
  • Douglas Rees
    • 1
  • Nozomi Itani
    • 1
  • Lucilla Poston
    • 1
  1. 1.Division of Women’s Health, Women’s Health Academic CentreKing’s College London and King’s Health PartnersLondonUK

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