Consequences of being overweight or obese during pregnancy on diabetes in the offspring: a record linkage study in Aberdeen, Scotland

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Abstract

Aims/hypothesis

Maternal obesity in pregnancy is associated with cardiovascular disease and mortality rate in the offspring. We aimed to determine whether maternal obesity is also associated with increased incidence of type 2 and type 1 diabetes in the offspring, independently of maternal diabetes as a candidate mechanistic pathway.

Methods

Birth records of 118,201 children from 1950 to 2011 in the Aberdeen Maternity and Neonatal Databank were linked to Scottish Care Information–Diabetes, the national register for diagnosed diabetes in Scotland, to identify incident and prevalent type 1 and type 2 diabetes up to 1 January 2012. Maternal BMI was calculated from height and weight measured at the first antenatal visit. The effect of maternal obesity on offspring outcomes was tested using time-to-event analysis with Cox proportional hazards regression to compare outcomes in offspring of mothers in underweight, overweight or obese categories of BMI, compared with offspring of women with normal BMI.

Results

Offspring of obese (BMI ≥30 kg/m ²) and overweight (BMI 25–29.9 kg/m ²) mothers had an increased hazard of type 2 diabetes compared with mothers with normal BMI, after adjustment for gestation when weight was measured, maternal history of diabetes before pregnancy, maternal history of hypertension, age at delivery, parity, socioeconomic status, and sex of the offspring: HR 3.48 (95% CI 2.33, 5.06) and HR 1.39 (1.06, 1.83), respectively.

Conclusions/interpretation

Maternal obesity is associated with increased incidence of type 2 diabetes in the offspring. Evidence-based strategies that reduce obesity among women of reproductive age and that might reduce the incidence of diabetes in their offspring are urgently required.

Electronic supplementary material

The online version of this article (10.1007/s00125-019-4891-4) contains peer-reviewed but unedited supplementary material, which is available to authorised users.

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Most cited references 19

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Hyperglycaemia and Adverse Pregnancy Outcome (HAPO) Study: associations with maternal body mass index.

(2010)

To determine whether higher maternal body mass index (BMI), independent of maternal glycaemia, is associated with adverse pregnancy outcomes. Observational cohort study. Fifteen centres in nine countries. Eligible pregnant women. A 75-g 2-hour oral glucose tolerance test (OGTT) was performed between 24 and 32 weeks of gestation in all participants. Maternal BMI was calculated from height and weight measured at the OGTT. Fetal adiposity was assessed using skinfold measurements and percentage of body fat was calculated. Associations between maternal BMI and pregnancy outcomes were assessed using multiple logistic regression analyses, with adjustment for potential confounders. Predefined primary outcomes were birthweight >90th percentile, primary caesarean section, clinical neonatal hypoglycaemia and cord serum C-peptide >90th percentile. Secondary outcomes included pre-eclampsia, preterm delivery (before 37 weeks) and percentage of body fat >90th percentile. Among 23 316 blinded participants, with control for maternal glycaemia and other potential confounders, higher maternal BMI was associated (odds ratio [95% confidence interval] for highest {> or =42.0 kg/m(2)} versus lowest { 90th percentile (3.52 [2.48-5.00]) and percentage of body fat >90th percentile (3.28 [2.28-4.71]), caesarean section (2.23 [1.66-2.99]), cord C-peptide >90th percentile (2.33 [1.58-3.43]) and pre-eclampsia (14.14 [9.44-21.17]). Preterm delivery was less frequent with higher BMI (0.48 [0.31-0.74]). Associations with fetal size tended to plateau in the highest maternal BMI categories. Higher maternal BMI, independent of maternal glycaemia, is strongly associated with increased frequency of pregnancy complications, in particular those related to excess fetal growth and adiposity and to pre-eclampsia.

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Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem Perinatal Family Follow-up Study.

Hagit Hochner, Yechiel Friedlander, Ronit Calderon-Margalit … (2012)

Accumulating evidence demonstrates that both maternal prepregnancy body mass index (mppBMI) and gestational weight gain (GWG) are associated with adult offspring adiposity. However, whether these maternal attributes are related to other cardiometabolic risk factors in adulthood has not been comprehensively studied. We used a birth cohort of 1400 young adults born in Jerusalem who had extensive archival data and clinical information at 32 years of age to prospectively examine the associations of mppBMI and GWG with adiposity and related cardiometabolic outcomes. Greater mppBMI, independently of GWG and confounders, was significantly associated with higher offspring BMI, waist circumference, systolic and diastolic blood pressures, insulin, and triglycerides and with lower high-density lipoprotein cholesterol. For example, the effect sizes were translated to nearly 5 kg/m(2) higher mean BMI, 8.4 cm higher waist circumference, 0.13 mmol/L (11.4 mg/dL) higher triglycerides, and 0.10 mmol/L (3.8 mg/dL) lower high-density lipoprotein cholesterol among offspring of mothers within the upper mppBMI quartile (mppBMI >26.4 kg/m(2)) compared with the lower quartile (mppBMI 14 kg) and lower (GWG <9 kg) quartiles of GWG were compared. Further adjustment for offspring adiposity attenuated the observed associations to the null. Maternal size both before and during pregnancy is associated with cardiometabolic risk factors in young adult offspring. The associations appear to be driven mainly by offspring adiposity. Future studies that explore mechanisms underlying the intergenerational cycle of obesity are warranted to identify potentially novel targets for cardiometabolic risk-reduction interventions.

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Developmental programming of obesity in mammals.

P D Taylor, L. Poston (2007)

Converging lines of evidence from epidemiological studies and animal models now indicate that the origins of obesity and related metabolic disorders lie not only in the interaction between genes and traditional adult risk factors, such as unbalanced diet and physical inactivity, but also in the interplay between genes and the embryonic, fetal and early postnatal environment. Whilst studies in man initially focused on the relationship between low birth weight and risk of adult obesity and metabolic syndrome, evidence is also growing to suggest that increased birth weight and/or adiposity at birth can also lead to increased risk for childhood and adult obesity. Hence, there appears to be increased risk of obesity at both ends of the birth weight spectrum. Animal models, including both under- and overnutrition in pregnancy and lactation lend increasing support to the developmental origins of obesity. This review focuses upon the influence of the maternal nutritional and hormonal environment in pregnancy in permanently programming appetite and energy expenditure and the hormonal, neuronal and autocrine mechanisms that contribute to the maintenance of energy balance in the offspring. We discuss the potential maternal programming 'vectors' and the molecular mechanisms that may lead to persistent pathophysiological changes resulting in subsequent disease. The perinatal environment, which appears to programme subsequent obesity, provides a potential therapeutic target, and work in this field will readily translate into improved interventional strategies to stem the growing epidemic of obesity, a disease which, once manifest, has proven particularly resistant to treatment.

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Author and article information

Contributors

Rebecca M. Reynolds: R.Reynolds@ed.ac.uk

Journal

Journal ID (nlm-ta): Diabetologia

Journal ID (iso-abbrev): Diabetologia

Title: Diabetologia

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0012-186X

ISSN (Electronic): 1432-0428

Publication date (Electronic): 19 June 2019

Publication date PMC-release: 19 June 2019

Publication date (Print): 2019

Volume: 62

Issue: 8

Pages: 1412-1419

Affiliations

[1 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, British Heart Foundation Centre for Cardiovascular Science, Queen’s Medical Research Institute, , University of Edinburgh, ; 47 Little France Crescent, Edinburgh, EH14 6TJ UK

[2 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, Tommy’s Centre for Maternal and Fetal Health, Medical Research Council Centre for Reproductive Health, Queen’s Medical Research Institute, , University of Edinburgh, ; Edinburgh, UK

[3 ]ISNI 0000 0004 0410 2071, GRID grid.7737.4, Department of Psychology and Logopedics, Faculty of Medicine, , University of Helsinki, ; Helsinki, Finland

[4 ]ISNI 0000 0004 1936 7291, GRID grid.7107.1, Institute of Applied Health Sciences, , University of Aberdeen, ; Aberdeen, UK

[5 ]ISNI 0000 0004 1936 7988, GRID grid.4305.2, Usher Institute of Population Health Sciences and Informatics, , University of Edinburgh, ; Edinburgh, UK

[6 ]ISNI 0000 0001 2193 314X, GRID grid.8756.c, Institute of Cardiovascular and Medical Sciences, , University of Glasgow, ; Glasgow, UK

Article

Publisher ID: 4891

DOI: 10.1007/s00125-019-4891-4

PMC ID: 6647186

PubMed ID: 31214738

SO-VID: f1561853-d194-4441-93bf-55420f0ef199

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 20 September 2018

Date accepted : 20 March 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;

Award ID: MR/N022556/1

Custom metadata

ScienceOpen disciplines: Endocrinology & Diabetes

Keywords: diabetes,obesity,offspring,pregnancy

Data availability:

ScienceOpen disciplines: Endocrinology & Diabetes

Keywords: diabetes, obesity, offspring, pregnancy

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Consequences of being overweight or obese during pregnancy on diabetes in the offspring: a record linkage study in Aberdeen, Scotland

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Abstract

Aims/hypothesis

Methods

Results

Conclusions/interpretation

Electronic supplementary material

Related collections

Bioscientifica Open Endocrinology

Most cited references 19

Hyperglycaemia and Adverse Pregnancy Outcome (HAPO) Study: associations with maternal body mass index.

Associations of maternal prepregnancy body mass index and gestational weight gain with adult offspring cardiometabolic risk factors: the Jerusalem Perinatal Family Follow-up Study.

Developmental programming of obesity in mammals.

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Cited by 29

Most referenced authors 485