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Pregnancy is a Critical Period for Prevention of Obesity and Cardiometabolic Risk

  • Kristi B. Adamo
    Correspondence
    Address for correspondence: Kristi B. Adamo, PhD, Healthy Active Living and Obesity Research Group, Children’s Hospital of Eastern Ontario Research Institute, 401 Smyth Rd. Ottawa, Canada ON K1H 8L1.
    Affiliations
    Healthy Active Living and Obesity Research Group, Children’s Hospital of Eastern Ontario Research Institute, Ottawa, ON

    Faculty of Medicine, Pediatrics, University of Ottawa, Ottawa, ON

    Faculty of Health Sciences, School of Human Kinetics, University of Ottawa, Ottawa, ON
    Search for articles by this author
  • Zachary M. Ferraro
    Affiliations
    Healthy Active Living and Obesity Research Group, Children’s Hospital of Eastern Ontario Research Institute, Ottawa, ON

    Faculty of Health Sciences, School of Human Kinetics, University of Ottawa, Ottawa, ON
    Search for articles by this author
  • Kendra E. Brett
    Affiliations
    Healthy Active Living and Obesity Research Group, Children’s Hospital of Eastern Ontario Research Institute, Ottawa, ON

    Faculty of Health Sciences, School of Human Kinetics, University of Ottawa, Ottawa, ON
    Search for articles by this author

      Abstract

      Obesity is a global epidemic whose development is rooted in complex and multi-factorial interactions. Excessive weight gain throughout the lifecourse is tightly linked to, and generally precedes, the emergence of impaired glycemic control. As such, a parallel increase in the incidence of type 2 diabetes has emerged resulting in a dual epidemic. Once established, obesity is difficult to reverse and epidemiological, animal model and experimental studies have provided strong evidence implicating the intrauterine environment in downstream obesity. This review focuses on the gestational period, a crucial time of growth, development and physiological change in mother and child. It describes the interplay between maternal obesity, gestational weight gain and lifestyle behaviours, which may act independently or in combination, to perpetuate the intergenerational cycle of obesity and cardiometabolic risk. Pregnancy represents a window of opportunity for intervention via maternal nutrition and/or physical activity that may induce beneficial physiological alternations in the fetus that are mediated through favourable adaptations to in utero environmental stimuli. Many avenues of research are merging to identify the predisposing factors for positive energy balance, insulin resistance and cardiometabolic risk throughout the lifecourse and evidence in the emerging field of epigenetics suggests that chronic, sub-clinical perturbations during pregnancy may affect fetal phenotype and long-term health.

      Résumé

      L’obésité est une épidémie mondiale dont le développement prend racine dans des interactions complexes et multifactorielles. La prise de poids excessive tout au long de la vie est bien liée à l’émergence de l’altération de la régulation glycémique, et généralement la précède. À ce titre, une augmentation parallèle de l’incidence du diabète de type 2 est apparue, entraînant ainsi une double épidémie. Une fois établie, l’obésité est difficilement réversible, et le modèle animal épidémiologique et les études expérimentales ont fourni des éléments probants importants impliquant l’environnement intra-utérin de l’obésité associée. Cette revue porte sur la période gestationnelle, un moment crucial de la croissance, le développement et le changement physiologiques chez la mère et l’enfant. Il décrit le rapport entre l’obésité maternelle, la prise de poids gestationnelle et les comportements liés au style de vie, qui peuvent agir indépendamment ou de manière combinée pour perpétuer le cycle intergénérationnel de l’obésité et le risque cardiométabolique. La grossesse constitue une circonstance opportune d’intervention par la nutrition maternelle ou l’activité physique qui peuvent induire des permutations physiologiques chez le fœtus qui sont médiés par des adaptations favorables aux stimuli environnementaux in utero. Plusieurs avenues de recherche s’associent pour identifier les facteurs prédisposants à un bilan énergétique positif, à l’insulinorésistance et au risque cardiométabolique tout au long de la vie, et des données probantes dans le domaine émergent de l’épigénétique suggèrent que des perturbations sous-cliniques chroniques durant la grossesse peuvent nuire au phénotype fœtal et à la santé à long terme.

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      References

        • Power M.L.
        • Schulkin J.
        Maternal obesity, metabolic disease, and allostatic load.
        Physiol Behav. 2012; 106: 22-28
        • Guo S.S.
        • Wu W.
        • Chumlea W.C.
        • et al.
        Predicting overweight and obesity in adulthood from body mass index values in childhood and adolescence.
        Am J Clin Nutr. 2002; 76: 653-658
        • Katzmarzyk P.T.
        • Janssen I.
        The economic costs associated with physical inactivity and obesity in Canada: an update.
        Can J Appl Physiol. 2004; 29: 90-115
        • Yogev Y.
        • Catalano P.M.
        Pregnancy and obesity.
        Obstet Gynecol Clin North Am. 2009; 36: 285-300
        • Huda S.S.
        • Brodie L.E.
        • Sattar N.
        Obesity in pregnancy: prevalence and metabolic consequences.
        Semin Fetal Neonatal Med. 2010; 15: 70-76
        • Salihu H.M.
        • Weldeselasse H.E.
        • Rao K.
        • et al.
        The impact of obesity on maternal morbidity and feto-infant outcomes among macrosomic infants.
        J Matern Fetal Neonatal Med. 2011; 24: 1088-1094
        • Catalano P.M.
        • Ehrenberg H.M.
        The short- and long-term implications of maternal obesity on the mother and her offspring.
        BJOG. 2006; 113: 1126-1133
        • Kim S.Y.
        • England L.
        • Wilson H.G.
        • et al.
        Percentage of gestational diabetes mellitus attributable to overweight and obesity.
        Am J Public Health. 2010; 100: 1047-1052
        • Torloni M.R.
        • Betran A.P.
        • Horta B.L.
        • et al.
        Prepregnancy BMI and the risk of gestational diabetes: a systematic review of the literature with meta-analysis.
        Obes Rev. 2009; 10: 194-203
        • Yeung E.H.
        • Hu F.B.
        • Solomon C.G.
        • et al.
        Life-course weight characteristics and the risk of gestational diabetes.
        Diabetologia. 2010; 53: 668-678
        • Martin A.M.
        • Berger H.
        • Nisenbaum R.
        • et al.
        Abdominal visceral adiposity in the first trimester predicts glucose intolerance in later pregnancy.
        Diabetes Care. 2009; 32: 1308-1310
        • Branchtein L.
        • Schmidt M.I.
        • Mengue S.S.
        • et al.
        Waist circumference and waist-to-hip ratio are related to gestational glucose tolerance.
        Diabetes Care. 1997; 20: 509-511
        • Kim C.
        • Berger D.K.
        • Chamany S.
        Recurrence of gestational diabetes mellitus: a systematic review.
        Diabetes Care. 2007; 30: 1314-1319
        • Kim C.
        • Newton K.M.
        • Knopp R.H.
        Gestational diabetes and the incidence of type 2 diabetes: a systematic review.
        Diabetes Care. 2002; 25: 1862-1868
        • Sibai B.M.
        • Ewell M.
        • Levine R.J.
        • et al.
        Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group.
        Am J Obstet Gynecol. 1997; 177: 1003-1010
        • Mostello D.
        • Jen C.J.
        • Allen J.
        • et al.
        Recurrent preeclampsia: the effect of weight change between pregnancies.
        Obstet Gynecol. 2010; 116: 667-672
        • O'Brien T.E.
        • Ray J.G.
        • Chan W.S.
        Maternal body mass index and the risk of preeclampsia: a systematic overview.
        Epidemiology. 2003; 14: 368-374
        • Mazaki-Tovi S.
        • Romero R.
        • Vaisbuch E.
        • et al.
        Maternal serum adiponectin multimers in preeclampsia.
        J Perinat Med. 2009; 37: 349-363
        • Kaaja R.
        • Laivuori H.
        • Laakso M.
        • et al.
        Evidence of a state of increased insulin resistance in preeclampsia.
        Metabolism. 1999; 48: 892-896
        • He S.
        • Silveira A.
        • Hamsten A.
        • et al.
        Haemostatic, endothelial and lipoprotein parameters and blood pressure levels in women with a history of preeclampsia.
        Thromb Haemost. 1999; 81: 538-542
        • Smith G.C.
        • Pell J.P.
        • Walsh D.
        Pregnancy complications and maternal risk of ischaemic heart disease: a retrospective cohort study of 129,290 births.
        Lancet. 2001; 357: 2002-2006
        • Catalano P.M.
        • Nizielski S.E.
        • Shao J.
        • et al.
        Downregulated IRS-1 and PPARgamma in obese women with gestational diabetes: relationship to FFA during pregnancy.
        Am J Physiol Endocrinol Metab. 2002; 282: E522-E533
        • Sattar N.
        • Greer I.A.
        Pregnancy complications and maternal cardiovascular risk: opportunities for intervention and screening?.
        BMJ. 2002; 325: 157-160
        • Ferraro Z.M.
        • Barrowman N.
        • Prud'homme D.
        • et al.
        Excessive gestational weight gain predicts large for gestational age neonates independent of maternal body mass index.
        J Matern Fetal Neonatal Med. 2012; 25: 538-542
        • Yu Z.B.
        • Han S.P.
        • Zhu G.Z.
        • et al.
        Birth weight and subsequent risk of obesity: a systematic review and meta-analysis.
        Obes Rev. 2011; 12: 525-542
        • Catalano P.M.
        • Presley L.
        • Minium J.
        • et al.
        Fetuses of obese mothers develop insulin resistance in utero.
        Diabetes Care. 2009; 32: 1076-1080
        • Catalano P.M.
        • Farrell K.
        • Thomas A.
        • et al.
        Perinatal risk factors for childhood obesity and metabolic dysregulation.
        Am J Clin Nutr. 2009; 90: 1303-1313
        • Boney C.M.
        • Verma A.
        • Tucker R.
        • et al.
        Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus.
        Pediatrics. 2005; 115: e290-e296
        • Dabelea D.
        • Mayer-Davis E.J.
        • Lamichhane A.P.
        • et al.
        Association of intrauterine exposure to maternal diabetes and obesity with type 2 diabetes in youth: the SEARCH Case-Control Study.
        Diabetes Care. 2008; 31: 1422-1426
        • Hillier T.A.
        • Pedula K.L.
        • Schmidt M.M.
        • et al.
        Childhood obesity and metabolic imprinting: the ongoing effects of maternal hyperglycemia.
        Diabetes Care. 2007; 30: 2287-2292
      1. Mendelson M, Cloutier J, Spence L, et al. Obesity and type 2 diabetes mellitus in a birth cohort of First Nation children born to mothers with pediatric-onset type 2 diabetes. Pediatr Diabetes;12(3 Pt 2):219–28.

      2. Metzger BE, Lowe LP, Dyer AR, et al. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med;358:1991–2002.

        • Sewell M.F.
        • Huston-Presley L.
        • Super D.M.
        • et al.
        Increased neonatal fat mass, not lean body mass, is associated with maternal obesity.
        Am J Obstet Gynecol. 2006; 195: 1100-1103
        • Catalano P.M.
        • Kirwan J.P.
        Maternal factors that determine neonatal size and body fat.
        Curr Diab Rep. 2001; 1: 71-77
      3. Hyperglycemia and Adverse Pregnancy Outcome (HAPO) Study: associations with neonatal anthropometrics.
        Diabetes. 2009; 58: 453-459
        • Philipps L.H.
        • Santhakumaran S.
        • Gale C.
        • et al.
        The diabetic pregnancy and offspring BMI in childhood: a systematic review and meta-analysis.
        Diabetologia. 2011; 54: 1957-1966
        • Schaefer-Graf U.M.
        • Heuer R.
        • Kilavuz O.
        • et al.
        Maternal obesity not maternal glucose values correlates best with high rates of fetal macrosomia in pregnancies complicated by gestational diabetes.
        J Perinat Med. 2002; 30: 313-321
        • Langer O.
        • Yogev Y.
        • Xenakis E.M.
        • et al.
        Overweight and obese in gestational diabetes: the impact on pregnancy outcome.
        Am J Obstet Gynecol. 2005; 192: 1768-1776
        • Langer O.
        • Yogev Y.
        • Most O.
        • Xenakis E.M.
        Gestational diabetes: the consequences of not treating.
        Am J Obstet Gynecol. 2005; 192: 989-997
        • Catalano P.M.
        • Hauguel-de M.S.
        Is it time to revisit the Pedersen hypothesis in the face of the obesity epidemic?.
        Am J Obstet Gynecol. 2011; 204: 479-487
        • Ong K.K.
        Size at birth, postnatal growth and risk of obesity.
        Horm Res. 2006; 65: 65-69
        • Chiavaroli V.
        • Giannini C.
        • D'Adamo E.
        • et al.
        Insulin resistance and oxidative stress in children born small and large for gestational age.
        Pediatrics. 2009; 124: 695-702
        • Kitajima M.
        • Oka S.
        • Yasuhi I.
        • et al.
        Maternal serum triglyceride at 24–32 weeks' gestation and newborn weight in nondiabetic women with positive diabetic screens.
        Obstet Gynecol. 2001; 97: 776-780
        • Nolan C.J.
        • Riley S.F.
        • Sheedy M.T.
        • et al.
        Maternal serum triglyceride, glucose tolerance, and neonatal birth weight ratio in pregnancy.
        Diabetes Care. 1995; 18: 1550-1556
        • Radaelli T.
        • Varastehpour A.
        • Catalano P.
        • et al.
        Gestational diabetes induces placental genes for chronic stress and inflammatory pathways.
        Diabetes. 2003; 52: 2951-2958
        • Guelinckx I.
        • Devlieger R.
        • Beckers K.
        • Vansant G.
        Maternal obesity: pregnancy complications, gestational weight gain and nutrition.
        Obes Rev. 2008; 9: 140-150
        • Guihard-Costa A.M.
        • Papiernik E.
        • Kolb S.
        Maternal predictors of subcutaneous fat in the term newborn.
        Acta Paediatr. 2004; 93: 346-349
        • Hull H.R.
        • Thornton J.C.
        • Ji Y.
        • et al.
        Higher infant body fat with excessive gestational weight gain in overweight women.
        Am J Obstet Gynecol. 2011; 205: 211-217
        • Gillman M.W.
        Gestational weight gain: now and the future.
        Circulation. 2012; 125: 1339-1340
        • Oken E.
        • Taveras E.M.
        • Kleinman K.P.
        • et al.
        Gestational weight gain and child adiposity at age 3 years.
        Am J Obstet Gynecol. 2007; 196: 322-328
        • Wrotniak B.H.
        • Shults J.
        • Butts S.
        • et al.
        Gestational weight gain and risk of overweight in the offspring at age 7 y in a multicenter, multiethnic cohort study.
        Am J Clin Nutr. 2008; 87: 1818-1824
        • Institute of Medicine
        Weight gain during pregnancy: Reexamining the guidelines.
        The National Academies Press, Washington, DC2009
        • Kinnunen T.I.
        • Luoto R.
        • Gissler M.
        • et al.
        Pregnancy weight gain from 1960s to 2000 in Finland.
        Int J Obes Relat Metab Disord. 2003; 27: 1572-1577
        • Weisman C.S.
        • Hillemeier M.M.
        • Downs D.S.
        • et al.
        Preconception predictors of weight gain during pregnancy: prospective findings from the Central Pennsylvania Women's Health Study.
        Womens Health Issues. 2010; 20: 126-132
        • Oken E.
        • Kleinman K.P.
        • Belfort M.B.
        • et al.
        Associations of gestational weight gain with short- and longer-term maternal and child health outcomes.
        Am J Epidemiol. 2009; 170: 173-180
        • Park S.
        • Sappenfield W.M.
        • Bish C.
        • et al.
        Assessment of the Institute of Medicine recommendations for weight gain during pregnancy: Florida, 2004-2007.
        Matern Child Health J. 2011; 15: 289-301
        • Gunderson E.P.
        • Abrams B.
        • Selvin S.
        The relative importance of gestational gain and maternal characteristics associated with the risk of becoming overweight after pregnancy.
        Int J Obes Relat Metab Disord. 2000; 24: 1660-1668
        • Luke B.
        • Hediger M.L.
        • Scholl T.O.
        Point of diminishing returns: when does gestational weight gain cease benefiting birthweight and begin adding to maternal obesity?.
        J Matern Fetal Med. 1996; 5: 168-173
        • Shankar K.
        • Harrell A.
        • Liu X.
        • et al.
        Maternal obesity at conception programs obesity in the offspring.
        Am J Physiol Regul Integr Comp Physiol. 2008; 294: R528-R538
        • Villamor E.
        • Cnattingius S.
        Interpregnancy weight change and risk of adverse pregnancy outcomes: a population-based study.
        Lancet. 2006; 368: 1164-1170
        • Ehrenberg H.M.
        • Huston-Presley L.
        • Catalano P.M.
        The influence of obesity and gestational diabetes mellitus on accretion and the distribution of adipose tissue in pregnancy.
        Am J Obstet Gynecol. 2003; 189: 944-948
        • Sohlstrom A.
        • Wahlund L.O.
        • Forsum E.
        Total body fat and its distribution during human reproduction as assessed by magnetic resonance imaging.
        Basic Life Sci. 1993; 60: 181-184
        • Kinoshita T.
        • Itoh M.
        Longitudinal variance of fat mass deposition during pregnancy evaluated by ultrasonography: the ratio of visceral fat to subcutaneous fat in the abdomen.
        Gynecol Obstet Invest. 2006; 61: 115-118
        • Denison F.C.
        • Roberts K.A.
        • Barr S.M.
        • et al.
        Obesity, pregnancy, inflammation, and vascular function.
        Reproduction. 2010; 140: 373-385
        • Ludwig D.S.
        • Currie J.
        The association between pregnancy weight gain and birthweight: a within-family comparison.
        Lancet. 2010; 376: 984-990
        • Schack-Nielsen L.
        • Michaelsen K.F.
        • Gamborg M.
        • et al.
        Gestational weight gain in relation to offspring body mass index and obesity from infancy through adulthood.
        Int J Obes (Lond). 2010; 34: 67-74
        • Lawlor D.A.
        • Lichtenstein P.
        • Fraser A.
        • et al.
        Does maternal weight gain in pregnancy have long-term effects on offspring adiposity? A sibling study in a prospective cohort of 146,894 men from 136,050 families.
        Am J Clin Nutr. 2011; 94: 142-148
        • Barker D.J.
        The fetal and infant origins of adult disease.
        BMJ. 1990; 301: 1111
        • Barker D.J.
        In utero programming of cardiovascular disease.
        Theriogenology. 2000; 53: 555-574
        • Dabelea D.
        • Hanson R.L.
        • Lindsay R.S.
        • et al.
        Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships.
        Diabetes. 2000; 49: 2208-2211
        • Gluckman P.D.
        • Hanson M.A.
        • Cooper C.
        • et al.
        Effect of in utero and early-life conditions on adult health and disease.
        N Engl J Med. 2008; 359: 61-73
        • Huang R.C.
        • Burke V.
        • Newnham J.P.
        • et al.
        Perinatal and childhood origins of cardiovascular disease.
        Int J Obes (Lond). 2007; 31: 236-244
        • Jansson T.
        • Powell T.L.
        IFPA 2005 Award in Placentology Lecture. Human placental transport in altered fetal growth: does the placenta function as a nutrient sensor? – a review.
        Placenta. 2006; 27: S91-S97
        • Bayol S.A.
        • Farrington S.J.
        • Stickland N.C.
        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. 2007; 98: 843-851
        • Bayol S.A.
        • Simbi B.H.
        • Bertrand J.A.
        • et al.
        Offspring from mothers fed a 'junk food' diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females.
        J Physiol. 2008; 586: 3219-3230
        • Kral J.G.
        • Biron S.
        • Simard S.
        • et al.
        Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years.
        Pediatrics. 2006; 118: e1644-e1649
        • Smith J.
        • Cianflone K.
        • Biron S.
        • et al.
        Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity.
        J Clin Endocrinol Metab. 2009; 94: 4275-4283
        • Cawley J.
        The economics of childhood obesity.
        Health Aff (Millwood). 2010; 29: 364-371
        • Samuelsson A.M.
        • Matthews P.A.
        • Argenton M.
        • et al.
        Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming.
        Hypertension. 2008; 51: 383-392
        • Hopkins S.A.
        • Cutfield W.S.
        Exercise in pregnancy: weighing up the long-term impact on the next generation.
        Exerc Sport Sci Rev. 2011; 39: 120-127
        • Godfrey K.M.
        • Inskip H.M.
        • Hanson M.A.
        The long-term effects of prenatal development on growth and metabolism.
        Semin Reprod Med. 2011; 29: 257-265
        • Hanson M.
        • Godfrey K.M.
        • Lillycrop K.A.
        • et al.
        Developmental plasticity and developmental origins of non-communicable disease: theoretical considerations and epigenetic mechanisms.
        Prog Biophys Mol Biol. 2011; 106: 272-280
        • Gluckman P.D.
        • Hanson M.A.
        • Low F.M.
        The role of developmental plasticity and epigenetics in human health.
        Birth Defects Res C Embryo Today. 2011; 93: 12-18
        • Levin B.E.
        Epigenetic influences on food intake and physical activity level: review of animal studies.
        Obesity (Silver Spring). 2008; 16: S51-S54
        • Godfrey K.M.
        • Sheppard A.
        • Gluckman P.D.
        • et al.
        Epigenetic gene promoter methylation at birth is associated with child's later adiposity.
        Diabetes. 2011; 60: 1528-1534
        • Catalano P.M.
        Obesity and pregnancy–the propagation of a viscous cycle?.
        J Clin Endocrinol Metab. 2003; 88: 3505-3506
        • Rooney K.
        • Ozanne S.E.
        Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions.
        Int J Obes (Lond). 2011; 35: 883-890
        • Alfaradhi M.Z.
        • Ozanne S.E.
        Developmental programming in response to maternal overnutrition.
        Front Genet. 2011; 2: 27
        • Tong J.F.
        • Yan X.
        • Zhu M.J.
        • et al.
        Maternal obesity downregulates myogenesis and beta-catenin signaling in fetal skeletal muscle.
        Am J Physiol Endocrinol Metab. 2009; 296: E917-E924
        • Bauer M.K.
        • Harding J.E.
        • Bassett N.S.
        • et al.
        Fetal growth and placental function.
        Mol Cell Endocrinol. 1998; 140: 115-120
        • Clapp J.F.
        Influence of endurance exercise and diet on human placental development and fetal growth.
        Placenta. 2006; 27: 527-534
        • Olson C.M.
        Tracking of food choices across the transition to motherhood.
        J Nutr Educ Behav. 2005; 37: 129-136
        • Olson C.M.
        • Strawderman M.S.
        Modifiable behavioral factors in a biopsychosocial model predict inadequate and excessive gestational weight gain.
        J Am Diet Assoc. 2003; 103: 48-54
        • Dempsey J.C.
        • Butler C.L.
        • Williams M.A.
        No need for a pregnant pause: physical activity may reduce the occurrence of gestational diabetes mellitus and preeclampsia.
        Exerc Sport Sci Rev. 2005; 33: 141-149
        • Butte N.F.
        • Wong W.W.
        • Treuth M.S.
        Energy requirements during pregnancy based on total energy expenditure and energy deposition.
        Am J Clin Nutr. 2004; 79: 1078-1087
        • Ferraro Z.M.
        • Gaudet L.
        • Adamo K.B.
        The potential impact of physical activity during pregnancy on maternal and neonatal outcomes.
        Obstet Gynecol Surv. 2012; 67: 99-110
        • Hawley J.A.
        • Lessard S.J.
        Exercise training-induced improvements in insulin action.
        Acta Physiol (Oxf). 2008; 192: 127-135
        • Ong M.J.
        • Guelfi K.J.
        • Hunter T.
        • et al.
        Supervised home-based exercise may attenuate the decline of glucose tolerance in obese pregnant women.
        Diabetes Metab. 2009; 35: 418-421
        • Dempsey J.C.
        • Butler C.L.
        • Sorensen T.K.
        • et al.
        A case-control study of maternal recreational physical activity and risk of gestational diabetes mellitus.
        Diabetes Res Clin Pract. 2004; 66: 203-215
        • Juhl M.
        • Olsen J.
        • Anderson P.
        • et al.
        Physical exercise during pregnancy and fetal growth measures: a study within the Danish National Birth Cohort.
        Am J Obstet Gynecol. 2010; 202: 63.e1-63.e8
        • Adamo K.B.
        • Ferraro Z.M.
        • Brett K.E.
        Can we modify the intrauterine environment to halt the intergenerational cycle of obesity?.
        Int J Environ Res Public Health. 2012; 9: 1263-1307
        • Artal R.
        • O'Toole M.
        Guidelines of the American College of Obstetricians and Gynecologists for exercise during pregnancy and the postpartum period.
        Br J Sports Med. 2003; 37: 6-12
        • Davies G.A.
        • Wolfe L.A.
        • Mottola M.F.
        • et al.
        Joint SOGC/CSEP clinical practice guideline: exercise in pregnancy and the postpartum period.
        Can J Appl Physiol. 2003; 28: 330-341
        • Mottola M.F.
        Exercise prescription for overweight and obese women: pregnancy and postpartum.
        Obstet Gynecol Clin North Am. 2009; 36: 301-316
      4. Mottola MF, Ruchat SM. Exercise guidelines for women with gestational diabetes. In: InTech, editor. Gestational diabetes 2011. p. 339–62.

        • Horvath K.
        • Koch K.
        • Jeitler K.
        • et al.
        Effects of treatment in women with gestational diabetes mellitus: systematic review and meta-analysis.
        BMJ. 2010; 340: c1395
        • Oostdam N.
        • van Poppel M.N.
        • Wouters M.G.
        • et al.
        Interventions for preventing gestational diabetes mellitus: a systematic review and meta-analysis.
        J Womens Health (Larchmt). 2011; 20: 1551-1563
        • Louie J.C.
        • Markovic T.P.
        • Perera N.
        • et al.
        A randomized controlled trial investigating the effects of a low-glycemic index diet on pregnancy outcomes in gestational diabetes mellitus.
        Diabetes Care. 2011; 34: 2341-2346
        • Korpi-Hyovalti E.A.
        • Laaksonen D.E.
        • Schwab U.S.
        • et al.
        Feasibility of a lifestyle intervention in early pregnancy to prevent deterioration of glucose tolerance.
        BMC Public Health. 2011; 11: 179
        • Luoto R.
        • Kinnunen T.I.
        • Aittasalo M.
        • et al.
        Primary prevention of gestational diabetes mellitus and large-for-gestational-age newborns by lifestyle counseling: a cluster-randomized controlled trial.
        PLoS Med. 2011; 8: e1001036
        • Stafne S.N.
        • Salvesen K.A.
        • Romundstad P.R.
        • et al.
        Regular exercise during pregnancy to prevent gestational diabetes: a randomized controlled trial.
        Obstet Gynecol. 2012; 119: 29-36