Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T08:06:55.500Z Has data issue: false hasContentIssue false
  • English
  • Français

Cardiovascular risk factors in offspring exposed to gestational diabetes mellitus in utero: systematic review and meta-analysis

Published online by Cambridge University Press:  06 January 2020

Maleesa M. Pathirana ,
Zohra S. Lassi ,
Claire T. Roberts  and
Prabha H. Andraweera Open the ORCID record for Prabha H. Andraweera [Opens in a new window]
Maleesa M. Pathirana
Affiliation:
Adelaide Medical School, The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Zohra S. Lassi
Affiliation:
Adelaide Medical School, The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Claire T. Roberts
Affiliation:
Adelaide Medical School, The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Prabha H. Andraweera*
Affiliation:
Adelaide Medical School, The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
*
Address for correspondence: Prabha Andraweera, Adelaide Medical School, Robinson Research Institute, The University of Adelaide, Adelaide, SA 5005, Australia. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Gestational diabetes mellitus (GDM) is a pregnancy complication that affects one in seven pregnancies. Emerging evidence demonstrates that children born of pregnancies complicated by GDM may be at increased risk of cardiovascular disease (CVD) in adulthood. Therefore, the aim of this study was to determine cardiovascular risk factors in offspring exposed to GDM in utero. PubMed, CINAHL, SCOPUS, and EMBASE databases were searched. Information was extracted on established CVD risk factors including blood pressure, lipids, blood glucose, fasting insulin, body mass index (BMI), and endothelial/microvascular function. The review protocol is registered in PROSPERO (CRD42018094983). Prospective and retrospective studies comparing offspring exposed to GDM compared to controls (non-GDM pregnancies) were considered. We included studies that defined GDM based on the International Association of Diabetes and Pregnancy Study Groups (IADPSG) definition, or prior definitions. The PRISMA guidelines were followed in conducting this systematic review. Methodological quality was assessed using the Newcastle–Ottawa Quality Assessment Scale. Study selection, data extraction, and quality assessment were done by two independent reviewers. The data were pooled using a random-effects model. Of 59 eligible studies, 24 were included in the meta-analysis. Offspring exposed to GDM had higher systolic blood pressure (mean difference (MD): 1.75 mmHg, 95% CI 0.57–2.94; eight studies, 7264 participants), BMI z-score (MD 0.11, 95% CI 0.02–0.20; nine studies, 8759 participants), and glucose (standard MD 0.43, 95% CI 0.08–0.77; 11 studies, 6423 participants) than control participants. In conclusion, offspring exposed to GDM have elevated systolic blood pressure, BMI, and glucose. Those exposed to GDM in utero may benefit from early childhood blood pressure measurements.

Keywords

pregnancygestational diabetes mellituscardiovascular diseasechild health
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 6 , December 2020 , pp. 599 - 616
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andraweera, PH, Dekker, GA, Arstall, M, Bianco-Miotto, T, Roberts, CT. Complications of pregnancy and future cardiovascular risk. Encycl Cardiovasc Res Med. 2018; 1, 643–650.CrossRefGoogle Scholar
Bellamy, L, Casas, JP, Hingorani, AD, Williams, D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 2009; 373, 1773–1779.CrossRefGoogle ScholarPubMed
Federation ID. IDF Diabetes Atlas, 2017. International Diabetes Federation, Brussels, Belgium.Google Scholar
Metzger, BE, Lowe, LP, Dyer, AR, et al. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med. 2008; 358: 1991–2002.Google ScholarPubMed
Tam, WH, Ma, RCW, Ozaki, R, et al. In utero exposure to maternal hyperglycemia increases childhood cardiometabolic risk in offspring. Diabetes Care 2017; 40, 679–686.CrossRefGoogle ScholarPubMed
Aceti, A, Santhakumaran, S, Logan, KM, et al. The diabetic pregnancy and offspring blood pressure in childhood: a systematic review and meta-analysis. Diabetologia 2012; 55, 3114–3127.CrossRefGoogle ScholarPubMed
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009; 6, e1000097.CrossRefGoogle ScholarPubMed
Drahota, ABE. RevMan Calculator. Cochrane Handbook, Part 2. The Cochrane Collaboration.Google Scholar
Wells, GA, Shea, B, O’Connell, D, Peterson, J, Welch, V, Losos, M. Newcastle-Ottawa Quality Assessment Scale, 2013. Ottawa Hospital Research Institute, Canada.Google Scholar
Buzinaro, EF, Berchieri, CB, Haddad, AL, Padovani, CR, Pimenta Wde, P. Overweight in adolescent offspring of women with hyperglycemia during pregnancy. Arq Bras Endocrinol Metabol. 2008; 52, 85–92.Google ScholarPubMed
Catalano, PM, Farrell, K, Thomas, A, et al. Perinatal risk factors for childhood obesity and metabolic dysregulation. Am J Clin Nutr. 2009; 90, 1303–1313.CrossRefGoogle ScholarPubMed
Chang, Y, Chen, X, Zhang, ZK. Intrauterine exposure to maternal diabetes is associated with adiposity in children at 6 years of age in China. Biomed Environ Sci. 2015; 28, 140–142.Google ScholarPubMed
Krishnaveni, GV, Veena, SR, Jones, A, et al. Exposure to maternal gestational diabetes is associated with higher cardiovascular responses to stress in adolescent Indians. J Clin Endocrinol Metab. 2015; 100, 986–993.CrossRefGoogle ScholarPubMed
Patel, S, Fraser, A, Smith, GD, et al. Associations of gestational diabetes, existing diabetes, and glycosuria with offspring obesity and cardiometabolic outcomes. Diabetes Care 2012; 35, 63–71.CrossRefGoogle ScholarPubMed
Tam, WH, Ma, RCW, Yang, X, et al. Glucose intolerance and cardiometabolic risk in adolescents exposed to maternal gestational diabetes: a 15-year follow-up study. Diabetes Care 2010; 33, 1382–1384.CrossRefGoogle ScholarPubMed
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, 215–220.CrossRefGoogle ScholarPubMed
Pirkola, J, Vaarasmaki, M, Leinonen, E, et al. Maternal type 1 and gestational diabetes: postnatal differences in insulin secretion in offspring at preschool age. Pediatr Diabetes 2008; 9, 583–589.CrossRefGoogle ScholarPubMed
Krishnaveni, GV, Veena, SR, Hill, JC, Kehoe, S, Karat, SC, Fall, CH. Intrauterine exposure to maternal diabetes is associated with higher adiposity and insulin resistance and clustering of cardiovascular risk markers in Indian children. Diabetes Care 2010; 33, 402–404.CrossRefGoogle ScholarPubMed
Lee, H, Jang, HC, Park, HK, Cho, NH. Early manifestation of cardiovascular disease risk factors in offspring of mothers with previous history of gestational diabetes mellitus. Diabetes Res Clin Pract. 2007; 78, 238–245.CrossRefGoogle ScholarPubMed
Page, KA, Romero, A, Enriquez, F, Xiang, AH, Buchanan, TA. Increased fasting glucose levels in children exposed to gestational diabetes in utero . Diabetes 2013; 62, A364.Google Scholar
Tam, WH, Ma, RCW, Yang, X, et al. Glucose intolerance and cardiometabolic risk in children exposed to maternal gestational diabetes mellitus in utero . Pediatrics 2008; 122, 1229–1234.CrossRefGoogle ScholarPubMed
Tsadok, MA, Friedlander, Y, Paltiel, O, et al. Obesity and blood pressure in 17-year-old offspring of mothers with gestational diabetes: insights from the Jerusalem Perinatal Study. Exp Diabetes Res. 2011; 2011, 906154.Google ScholarPubMed
Vääräsmäki, M, Pouta, A, Elliot, P, et al. Adolescent manifestations of metabolic syndrome among children born to women with gestational diabetes in a general-population birth cohort. Am J Epidemiol. 2009; 169, 1209–1215.CrossRefGoogle Scholar
Davis, JN, Gunderson, EP, Gyllenhammer, LE, Goran, MI. Impact of gestational diabetes mellitus on pubertal changes in adiposity and metabolic profiles in Latino offspring. J Pediatr. 2013; 162, 741–745.CrossRefGoogle ScholarPubMed
Holder, T, Giannini, C, Santoro, N, et al. A low disposition index in adolescent offspring of mothers with gestational diabetes: a risk marker for the development of impaired glucose tolerance in youth. Diabetologia 2014; 57, 2413–2420.CrossRefGoogle ScholarPubMed
Kearney, M, Perron, J, Marc, I, Weisnagel, JS, Tchernof, A, Robitaille, J. Association of prenatal exposure to gestational diabetes with offspring body composition and regional body-fat distribution. Diabetes 2017; 66, A368.Google Scholar
Page, KA, Romero, A, Buchanan, TA, Xiang, AH. Gestational diabetes mellitus, maternal obesity, and adiposity in offspring. J Pediatr. 2014; 164, 807–810.CrossRefGoogle ScholarPubMed
Whitaker, RC, Pepe, MS, Seidel, KD, Wright, JA, Knopp, RH. Gestational diabetes and the risk of offspring obesity. Pediatrics 1998; 101, E9.Google ScholarPubMed
Baptiste-Roberts, K, Nicholson, W, Wang, N-Y, Brancati, F. Gestational diabetes and subsequent growth patterns of offspring: The National Collaborative Perinatal Project…[corrected] [published erratum appears in MATERN CHILD HEALTH J 2012; 16(1):266]. Matern Child Health J. 2012; 16, 125–132.Google ScholarPubMed
Lawlor, DA, Fraser, A, Lindsay, RS, et al. Association of existing diabetes, gestational diabetes and glycosuria in pregnancy with macrosomia and offspring body mass index, waist and fat mass in later childhood: findings from a prospective pregnancy cohort. Diabetologia 2010; 53, 89–97.CrossRefGoogle ScholarPubMed
Page, KA, Romero, A, Enriquez, I, Chirikian, V, Buchanan, TA, Xiang, A. Increased central adiposity in hispanic children exposed to gestational diabetes in utero . Diabetes 2012; 61, A517.Google Scholar
Retnakaran, R, Ye, C, Hanley, A, et al. Effect of maternal gestational diabetes on the cardiovascular risk factor profile of infants at 1 year of age. Nutr Metab Cardiovasc Dis. 2013; 23, 1175–1181.CrossRefGoogle ScholarPubMed
Eslamian, L, Akbari, S, Marsoosi, V, Jamal, A. Association between fetal overgrowth and metabolic parameters in cord blood of newborns of women with GDM. Minerva Med. 2013; 104, 317–324.Google ScholarPubMed
Jaber, SM. Metabolic hormones profile in 2 weeks old healthy infants of diabetic mothers. Saudi Med J. 2006; 27, 1338–1345.Google ScholarPubMed
König, AB, Junginger, S, Reusch, J, Louwen, F, Badenhoop, K. Gestational diabetes outcome in a single center study: higher BMI in children after six months. Horm Metab Res. 2014; 46, 804–809.Google Scholar
Zhao, P, Liu, E, Qiao, Y, et al. Maternal gestational diabetes and childhood obesity at age 9–11: results of a multinational study. Diabetologia 2016; 59, 2339–2348.CrossRefGoogle ScholarPubMed
Li, S, Zhu, Y, Yeung, E, et al. Offspring risk of obesity in childhood, adolescence and adulthood in relation to gestational diabetes mellitus: a sex-specific association. Int J Epidemiol. 2017; 46, 1533–1541.CrossRefGoogle ScholarPubMed
Krishnaveni, GV, Hill, JC, Leary, SD, et al. Anthropometry, glucose tolerance, and insulin concentrations in Indian children: relationships to maternal glucose and insulin concentrations during pregnancy. Diabetes Care 2005; 28, 2919–2925.CrossRefGoogle ScholarPubMed
Nehring, I, Chmitorz, A, Reulen, H, von Kries, R, Ensenauer, R. Gestational diabetes predicts the risk of childhood overweight and abdominal circumference independent of maternal obesity. Diabet Med. 2013; 30, 1449–1456.CrossRefGoogle ScholarPubMed
Nielsen, GL, Dethlefsen, C, Lundbye-Christensen, S, Pedersen, JF, Molsted-Pedersen, L, Gillman, MW. Adiposity in 277 young adult male offspring of women with diabetes compared with controls: a Danish population-based cohort study. Acta Obstet Gynecol Scand. 2012; 91, 838–843.CrossRefGoogle ScholarPubMed
Pirkola, J, Pouta, A, Bloigu, A, et al. Risks of overweight and abdominal obesity at age 16 years associated with prenatal exposures to maternal prepregnancy overweight and gestational diabetes mellitus. Diabetes Care 2010; 33, 1115–1121.CrossRefGoogle ScholarPubMed
Silverman, BL, Rizzo, TA, Cho, NH, Metzger, BE. Long-term effects of the intrauterine environment. The Northwestern University Diabetes in Pregnancy Center. Diabetes Care 1998; 21 (Suppl 2) B142–B149.Google Scholar
Vohr, BR, McGarvey, ST, Garcia Coll, C. Effects of maternal gestational diabetes and adiposity on neonatal adiposity and blood pressure. Diabetes Care 1995; 18, 467–475.CrossRefGoogle ScholarPubMed
Vohr, BR, McGarvey, ST, Tucker, R. Effects of maternal gestational diabetes on offspring adiposity at 4–7 years of age. Diabetes Care 1999; 22: 1284–1291.CrossRefGoogle ScholarPubMed
Farfel, A, Rabinovitz, R, Kampino, G, et al. Children of mothers with pre-gestational and gestational diabetes tend to be overweight at age 17. Horm Res Paediatr. 2013; 80, 414.Google Scholar
Rutkowska, J, Bandurska-Stankiewicz, E, Wiatr-Bykowska, D, Myszka-Podgórska, K, Kuglarz, E, Matuszewski, W. The growth patterns in children born to mothers with gestational diabetes mellitus. Diabetologia 2015; 58, S488.Google Scholar
Le Moullec, N, Fianu, A, Maillard, O, et al. Sexual dimorphism in the association between gestational diabetes mellitus and overweight in offspring at 5–7 years: the OBEGEST cohort study. PLoS One 2018; 13, e0195531.CrossRefGoogle ScholarPubMed
Teng, ZJ, Xia, MJ, Qu, CH, Yu, HX. Long-term risk of metabolic disorders in gestational diabetes mellitus mothers and offspring. Biomed Res (India) 2017; 28, 4466–4470.Google Scholar
López Morales, CM, Brito Zurita, OR, González Heredia, R, Cruz López, M, Méndez Padrón, A, Matute Briseño, JA. Placental atherosclerosis and markers of endothelial dysfunction in infants born to mothers with gestational diabetes. Medicina Clinica. 2016; 147, 95–100.CrossRefGoogle ScholarPubMed
Miettinen, HE, Rono, K, Koivusalo, SB, Eriksson, JG, Gylling, H. Effect of gestational diabetes mellitus on newborn cholesterol metabolism. Atherosclerosis 2018; 275, 346–351.CrossRefGoogle ScholarPubMed
Chandler-Laney, PC, Bush, NC, Granger, WM, Rouse, DJ, Mancuso, MS, Gower, BA. Overweight status and intrauterine exposure to gestational diabetes are associated with children’s metabolic health. Pediatr Obes. 2012; 7, 44–52.CrossRefGoogle ScholarPubMed
Borgoño, CA, Hamilton, JK, Ye, C, et al. Determinants of insulin resistance in infants at age 1 year: impact of gestational diabetes mellitus. Diabetes Care 2012; 35, 1795–1797.CrossRefGoogle ScholarPubMed
Bozkurt, L, Göbl, CS, Rami-Merhar, B, et al. The cross-link between adipokines, insulin resistance and obesity in offspring of diabetic pregnancies. Horm Res Paediatr. 2016; 86, 300–308.CrossRefGoogle ScholarPubMed
Plagemann, A, Harder, T, Kohlhoff, R, Rohde, W, Dorner, G. Overweight and obesity in infants of mothers with long-term insulin-dependent diabetes or gestational diabetes. Int J Obes Relat Metab Disord. 1997; 21, 451–456.CrossRefGoogle ScholarPubMed
Plagemann, A, Harder, T, Kohlhoff, R, Rohde, W, Dorner, G. Glucose tolerance and insulin secretion in children of mothers with pregestational IDDM or gestational diabetes. Diabetologia 1997; 40, 1094–1100.CrossRefGoogle ScholarPubMed
Clausen, TD, Mathiesen, ER, Hansen, T, et al. High prevalence of type 2 diabetes and pre-diabetes in adult offspring of women with gestational diabetes mellitus or type 1 diabetes: the role of intrauterine hyperglycemia. Diabetes Care 2008; 31, 340–346.CrossRefGoogle ScholarPubMed
Wilk, M, Horodnicka-Jozwa, A, Moleda, P, et al. Assessment of selected carbohydrate parameters in children exposed to gestational diabetes in utero . Neuro Endocrinol Lett. 2015; 36, 504–510.Google ScholarPubMed
Visentin, S, Londero, AP, Bellamio, B, et al. Fetal endothelial remodeling in late-onset gestational hypertension. Am J Hypertens. 2016; 29, 273–279.CrossRefGoogle ScholarPubMed
Visentin, S, Lapolla, A, Londero, AP, et al. Adiponectin levels are reduced while markers of systemic inflammation and aortic remodelling are increased in intrauterine growth restricted mother-child couple. Biomed Res Int. 2014; 2014, 401595.CrossRefGoogle ScholarPubMed
Chen, X, Wang, Y. Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis. Circulation 2008; 117, 3171–3180.CrossRefGoogle ScholarPubMed
Raitakari, OT, Juonala, M, Kähönen, M, et al. Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: the cardiovascular risk in Young Finns Study. JAMA 2003; 290, 2277–2283.CrossRefGoogle ScholarPubMed
Oikonen, M, Nuotio, J, Magnussen, CG, et al. Repeated blood pressure measurements in childhood in prediction of hypertension in adulthood. Hypertension 2016; 67, 41–47.CrossRefGoogle ScholarPubMed
Lewington, S, Clarke, R, Qizilbash, N, Peto, R, Collins, R. Age-specific relevance of usual blood pressure to vascular mortality: a meta-analysis of individual data for one million adults in 61 prospective studies. Lancet 2002; 360, 1903–1913.Google ScholarPubMed
Kizirian, NV, Kong, Y, Muirhead, R, et al. Effects of a low-glycemic index diet during pregnancy on offspring growth, body composition, and vascular health: a pilot randomized controlled trial. Am J Clin Nutr. 2016; 103, 1073–1082.CrossRefGoogle ScholarPubMed
Freedman, DS, Sherry, B. The validity of BMI as an indicator of body fatness and risk among children. Pediatrics 2009; 124, Suppl 1, S23–34.CrossRefGoogle ScholarPubMed
Kawasaki, M, Arata, N, Miyazaki, C, et al. Obesity and abnormal glucose tolerance in offspring of diabetic mothers: a systematic review and meta-analysis. PLoS One 2018; 13, e0190676.CrossRefGoogle ScholarPubMed
Jago, R, Mendoza, JA, Chen, T, Baranowski, T. Longitudinal associations between BMI, waist circumference, and cardiometabolic risk in US youth: monitoring implications. Obesity (Silver Spring, Md) 2013; 21, E271–E279.CrossRefGoogle ScholarPubMed
Dissanayake, HU, Anderson, L, McMullan, RL, et al. Influence of maternal and placental factors on newborn body composition. J Paediatr Child Health 2019. doi: 10.1111/jpc.14565. [Epub ahead of print].CrossRefGoogle Scholar
Enzi, G, Inelmen, EM, Caretta, F, Villani, F, Zanardo, V, DeBiasi, F. Development of adipose tissue in newborns of gestational-diabetic and insulin-dependent diabetic mothers. Diabetes 1980; 29, 100–104.CrossRefGoogle ScholarPubMed
Skilton, MR, Siitonen, N, Wurtz, P, et al. High birth weight is associated with obesity and increased carotid wall thickness in young adults: the cardiovascular risk in young Finns study. Arterioscler Thromb Vasc Biol. 2014; 34, 1064–1068.CrossRefGoogle ScholarPubMed
D’Adamo, E, Caprio, S. Type 2 diabetes in youth: epidemiology and pathophysiology. Diabetes Care 2011; 34, Suppl 2, S161–S165.Google ScholarPubMed
Rhodes, ET, Prosser, LA, Hoerger, TJ, Lieu, T, Ludwig, DS, Laffel, LM. Estimated morbidity and mortality in adolescents and young adults diagnosed with type 2 diabetes mellitus. (Report) (clinical report). Diabetic Med. 2012; 29, 453.CrossRefGoogle Scholar
Li, L, Peters, H, Gama, A, et al. Maternal smoking in pregnancy association with childhood adiposity and blood pressure. Pediatr Obes. 2016; 11, 202–209.CrossRefGoogle ScholarPubMed
Riedel, C, Fenske, N, Muller, MJ, et al. Differences in BMI z-scores between offspring of smoking and nonsmoking mothers: a longitudinal study of German children from birth through 14 years of age. Environ Health Perspect. 2014; 122, 761–767.CrossRefGoogle ScholarPubMed
Gademan, MG, van Eijsden, M, Roseboom, TJ, van der Post, JA, Stronks, K, Vrijkotte, TG. Maternal prepregnancy body mass index and their children’s blood pressure and resting cardiac autonomic balance at age 5 to 6 years. Hypertension 2013; 62, 641–647.CrossRefGoogle ScholarPubMed
Shaat, N, Groop, L. Genetics of gestational diabetes mellitus. Curr Med Chem. 2007; 14, 569–83.CrossRefGoogle ScholarPubMed
West, NA, Crume, TL, Maligie, MA, Dabelea, D. Cardiovascular risk factors in children exposed to maternal diabetes in utero . Diabetologia 2011; 54, 504–547.CrossRefGoogle ScholarPubMed
Wang, J, Pan, L, Liu, E, et al. Gestational diabetes and offspring’s growth from birth to 6 years old. Int J Obes. 2019; 43, 663–672.CrossRefGoogle ScholarPubMed
Kaseva, N, Vaarasmaki, M, Matinolli, HM, et al. Pre-pregnancy overweight or obesity and gestational diabetes as predictors of body composition in offspring twenty years later: evidence from two birth cohort studies. Int J Obes (Lond). 2018; 42, 872–879.CrossRefGoogle ScholarPubMed
Hammoud, NM, De Valk, HW, Biesma, DH, Visser, GHA. Intrauterine adiposity and BMI in 4- to 5-year-old offspring from diabetic pregnancies. Neonatology. 2017; 111, 177–181.CrossRefGoogle ScholarPubMed
Hakanen, T, Saha, MT, Salo, MK, et al. Mothers with gestational diabetes are more likely to give birth to children who experience early weight problems. Acta Paediatr Int J Paediatr. 2016; 105, 1166–1172.CrossRefGoogle ScholarPubMed
Page, KA, Wang, X, Romero, A, Buchanan, TA, Xiang, AH. Insulin sensitivity and β-cell function are reduced in children exposed to gestational diabetes in utero. Diabetes. 2015; 64, A94.Google Scholar
Zhao, YL, Ma, RM, Lao, TT, et al. Maternal gestational diabetes mellitus and overweight and obesity in offspring: a study in Chinese children. J Dev Orig Health Dis. 2015; 6, 479–484.CrossRefGoogle ScholarPubMed
Pham, MT, Brubaker, K, Pruett, K, Caughey, AB. Risk of childhood obesity in the toddler offspring of mothers with gestational diabetes. Obstet Gynecol. 2013; 121, 976–982.CrossRefGoogle ScholarPubMed
Jahan, S, Ahmed, CM, Zinnat, R, et al. Influence of maternal diabetes on serum leptinemic and insulinemic status of the offspring: a case study of selected patients in a tertiary care hospital in Bangladesh. Diabetes Metab Syndr. 2011; 5, 33–37.CrossRefGoogle Scholar
Boerschmann, H, Pfluger, M, Henneberger, L, Ziegler, AG, Hummel, S. Prevalence and predictors of overweight and insulin resistance in offspring of mothers with gestational diabetes mellitus. Diabetes Care. 2010; 33, 1845–1849.Google ScholarPubMed
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, e290–e296.Google ScholarPubMed
Gillman, MW, Rifas-Shiman, S, Berkey, CS, Field, AE, Colditz, GA. Maternal gestational diabetes, birth weight, and adolescent obesity. Pediatrics. 2003; 111, e221–e226.CrossRefGoogle ScholarPubMed
Silverman, BL, Metzger, BE, Cho, NH, Loeb, CA. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care. 1995; 18, 611–617.CrossRefGoogle ScholarPubMed
Supplementary material: File

Pathirana et al. supplementary material

Tables S1-S6 and Figures S1-S9

Download Pathirana et al. supplementary material(File)
File 199.7 KB