Dietary Glycemic Index during Pregnancy Is Associated with Biomarkers of the Metabolic Syndrome in Offspring at Age 20 Years

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Abstract

Objective

Growing evidence indicates that metabolic syndrome is rooted in fetal life with a potential key role of nutrition during pregnancy. The objective of the study was to assess the possible associations between the dietary glycemic index (GI) and glycemic load (GL) during pregnancy and biomarkers of the metabolic syndrome in young adult offspring.

Methods

Dietary GI and GL were assessed by questionnaires and interviews in gestation week 30 and offspring were clinically examined at the age of 20 years. Analyses based on 428 mother-offspring dyads were adjusted for maternal smoking during pregnancy, height, pre-pregnancy body mass index (BMI), education, energy intake, and the offspring’s ambient level of physical activity. In addition, possible confounding by gestational diabetes mellitus was taken into account.

Outcome Measures

Waist circumference, blood pressure, HOMA insulin resistance (HOMA-IR) and plasma levels of fasting glucose, triglycerides, HDL cholesterol, LDL cholesterol, total cholesterol, insulin, and leptin were measured in the offspring.

Results

Significant associations were found between dietary GI in pregnancy and HOMA-IR (the relative increase in HOMA-IR per 10 units’ GI increase was 1.09 [95% CI: 1.01, 1.16], p = 0.02), insulin (1.09 [95% CI: 1.02, 1.16], p = 0.01) and leptin (1.21 [95% CI: 1.06, 1.38], p = 0.01) in the offspring; whereas no associations were detected for GL.

Conclusions

Our data suggests that high dietary GI in pregnancy may affect levels of markers for the metabolic syndrome in young adult offspring in a potentially harmful direction.

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Most cited references 32

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The thrifty phenotype hypothesis.

C N Hales, D. J. Barker (2001)

The thrifty phenotype hypothesis proposes that the epidemiological associations between poor fetal and infant growth and the subsequent development of type 2 diabetes and the metabolic syndrome result from the effects of poor nutrition in early life, which produces permanent changes in glucose-insulin metabolism. These changes include reduced capacity for insulin secretion and insulin resistance which, combined with effects of obesity, ageing and physical inactivity, are the most important factors in determining type 2 diabetes. Since the hypothesis was proposed, many studies world-wide have confirmed the initial epidemiological evidence, although the strength of the relationships has varied from one study to another. The relationship with insulin resistance is clear at all ages studied. Less clear is the relationship with insulin secretion. The relative contribution of genes and environment to these relationships remains a matter of debate. The contributions of maternal hyperglycaemia and the trajectory of postnatal growth need to be clarified.

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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.

Tine D. Clausen, Elisabeth Mathiesen, Torben Hansen … (2008)

The role of intrauterine hyperglycemia and future risk of type 2 diabetes in human offspring is debated. We studied glucose tolerance in adult offspring of women with either gestational diabetes mellitus (GDM) or type 1 diabetes, taking the impact of both intrauterine hyperglycemia and genetic predisposition to type 2 diabetes into account. The glucose tolerance status following a 2-h 75-g oral glucose tolerance test (OGTT) was evaluated in 597 subjects, primarily Caucasians, aged 18-27 years. They were subdivided into four groups according to maternal glucose metabolism during pregnancy and genetic predisposition to type 2 diabetes: 1) offspring of women with diet-treated GDM (O-GDM), 2) offspring of genetically predisposed women with a normal OGTT (O-NoGDM), 3) offspring of women with type 1 diabetes (O-type 1), and 4) offspring of women from the background population (O-BP). The prevalence of type 2 diabetes and pre-diabetes (impaired glucose tolerance or impaired fasting glucose) in the four groups was 21, 12, 11, and 4%, respectively. In multiple logistic regression analysis, the adjusted odds ratios (ORs) for type 2 diabetes/pre-diabetes were 7.76 (95% CI 2.58-23.39) in O-GDM and 4.02 (1.31-12.33) in O-type 1 compared with O-BP. In O-type 1, the risk of type 2 diabetes/pre-diabetes was significantly associated with elevated maternal blood glucose in late pregnancy: OR 1.41 (1.04-1.91) per mmol/l. A hyperglycemic intrauterine environment appears to be involved in the pathogenesis of type 2 diabetes/pre-diabetes in adult offspring of primarily Caucasian women with either diet-treated GDM or type 1 diabetes during pregnancy.

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Obesity at the age of 50 y in men and women exposed to famine prenatally.

A C J Ravelli, J van der Meulen, C Osmond … (1999)

It was shown that men who were conceived during the Dutch famine of 1944-1945 had higher rates of obesity at age 19 y than those conceived before or after it. Our objective was to study the effects of prenatal exposure to the Dutch famine on obesity in women and men at age 50 y. We measured the body size of 741 people born at term between November 1943 and February 1947 in Amsterdam. We compared people exposed to famine in late, mid, or early gestation (exposed participants) with those born before or conceived after the famine period (nonexposed participants). The body mass index (BMI; in kg/m(2)) of 50-y-old women exposed to famine in early gestation was significantly higher by 7. 4% (95% CI: 0.7%, 14.5%) than that of nonexposed women. BMI did not differ significantly in women exposed in mid gestation (-2.1%; -7.0%, 3.1%) or in late gestation (-1.3%; -6.3%, 3.9%). In 50-y-old men, BMI was not significantly affected by exposure to famine during any stage of gestation: BMI differed by 0.4% (-3.5%, 4.5%) in men exposed to famine in late gestation, by -1.2% (-5.5%, 3.3%) in those exposed in mid gestation, and by 0.5% (-4.6%, 6.0%) in those exposed in early gestation compared with nonexposed men. Maternal malnutrition during early gestation was associated with higher BMI and waist circumference in 50-y-old women but not in men. These findings suggest that pertubations of central endocrine regulatory systems established in early gestation may contribute to the development of abdominal obesity in later life.

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Author and article information

Contributors

Kartik Shankar: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Electronic): 1932-6203

Publication date Collection: 2013

Publication date (Electronic): 31 May 2013

Volume: 8

Issue: 5

Electronic Location Identifier: e64887

Affiliations

[1 ]Centre for Fetal Programming, Department of Epidemiology Research, Statens Serum Institute, Copenhagen, Denmark

[2 ]The Unit for Nutrition Research, Faculty of Food Science and Nutrition, School of Health Sciences, University of Iceland, Reykjavik, Iceland

[3 ]Centre for Fetal Programming, Department of Public Health, Section for Epidemiology, Aarhus University, Aarhus, Denmark

[4 ]Department of Paediatrics, Aarhus University Hospital, Skejby, Denmark

[5 ]Department of Endocrinology, Rigshospitalet, Copenhagen, Denmark

[6 ]Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

University of Arkansas for Medical Sciences, United States of America

Author notes

* E-mail: ind@ 123456ssi.dk

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: SFO. Performed the experiments: DR BHB TBH. Analyzed the data: ID CG. Contributed reagents/materials/analysis tools: DR CGS TH. Wrote the paper: ID. Editing of the manuscript: AV SFO TBH BHB DR TH. Contribution to the discussion: AV SFO.

Article

Publisher ID: PONE-D-13-03758

DOI: 10.1371/journal.pone.0064887

PMC ID: 3669023

PubMed ID: 23741411

SO-VID: 98dd8458-a60d-41fe-8bf6-612b4a96b9bf

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 24 January 2013

Date accepted : 19 April 2013

Page count

Pages: 8

Funding

The study was supported by the Danish Council for Strategic Research (09-067124; 09-063072; 2101-06-0005). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Dietary Glycemic Index during Pregnancy Is Associated with Biomarkers of the Metabolic Syndrome in Offspring at Age 20 Years

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Abstract

Objective

Methods

Outcome Measures

Results

Conclusions

Related collections

PLOS Climate

Most cited references 32

The thrifty phenotype hypothesis.

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.

Obesity at the age of 50 y in men and women exposed to famine prenatally.

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