Abstract
Background/Objectives
Maternal obesity and excessive gestational weight gain are associated with an increased risk of obesity in offspring. It remains unclear whether maternal adiposity also affects organ fat, which has important adverse cardiometabolic health consequences and whether the associations reflect intrauterine causal mechanisms. We examined the associations of parental pre-pregnancy body mass index (BMI) and gestational weight gain with general, abdominal, pericardial, and liver fat in 10-year-old children.
Subjects/Methods
In a population-based prospective cohort study among 2354 parents and their children, we obtained pre-pregnancy maternal and paternal BMI and gestational weight gain and offspring BMI, fat mass index (total fat/height4) by dual-energy X-ray absorptiometry, and subcutaneous fat index (subcutaneous fat/height4), visceral fat index (visceral fat/height3), pericardial fat index (pericardial fat/height3), and liver fat fraction by magnetic resonance imaging (MRI) at 10 years.
Results
A 1-standard deviation score (SDS) higher maternal pre-pregnancy BMI was associated with higher childhood BMI (difference 0.32 (95% confidence interval (CI) 0.28, 0.36) SDS), fat mass index (difference 0.28 (95% CI 0.24, 0.31) SDS), subcutaneous fat index (difference 0.26 (95% CI 0.22, 0.30) SDS), visceral fat index (difference 0.24 (95% CI 0.20, 0.28) SDS), pericardial fat index (difference 0.12 (95% CI 0.08, 0.16) SDS), and liver fat fraction (difference 0.15 (95% CI 0.11, 0.19) SDS). After conditioning each MRI adiposity measure on BMI at 10 years, higher maternal pre-pregnancy BMI remained associated with higher childhood subcutaneous and visceral fat indices. Smaller but not statistically different effect estimates were observed for paternal BMI. Gestational weight gain was not consistently associated with organ fat.
Conclusions
Higher maternal pre-pregnancy BMI, but not gestational weight gain, was associated with higher general and organ fat. Similar associations of pre-pregnancy maternal and paternal BMI with offspring adiposity suggest a role of family shared lifestyle factors and genetics.
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References
Yu Z, Han S, Zhu J, Sun X, Ji C, Guo X. Pre-pregnancy body mass index in relation to infant birth weight and offspring overweight/obesity: a systematic review and meta-analysis. PLoS ONE. 2013;8:e61627.
Marchi J, Berg M, Dencker A, Olander EK, Begley C. Risks associated with obesity in pregnancy, for the mother and baby: a systematic review of reviews. Obes Rev. 2015;16:621–38.
Fall CH. Evidence for the intra-uterine programming of adiposity in later life. Ann Hum Biol. 2011;38:410–28.
Lawlor DA, Timpson NJ, Harbord RM, Leary S, Ness A, McCarthy MI, et al. Exploring the developmental overnutrition hypothesis using parental–offspring associations and FTO as an instrumental variable. PLoS Med. 2008;5:e33.
Patro B, Liber A, Zalewski B, Poston L, Szajewska H, Koletzko B. Maternal and paternal body mass index and offspring obesity: a systematic review. Ann Nutr Metab. 2013;63:32–41.
Gaillard R, Steegers EA, Duijts L, Felix JF, Hofman A, Franco OH, et al. Childhood cardiometabolic outcomes of maternal obesity during pregnancy: the Generation R Study. Hypertension. 2014;63:683–91.
Liu J, Fox CS, Hickson D, Sarpong D, Ekunwe L, May WD, et al. Pericardial adipose tissue, atherosclerosis, and cardiovascular disease risk factors: the Jackson Heart Study. Diabetes Care. 2010;33:1635–9.
Preis SR, Massaro JM, Robins SJ, Hoffmann U, Vasan RS, Irlbeck T, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham Heart Study. Obesity (Silver Spring, MD). 2010;18:2191–8.
Tadros TM, Massaro JM, Rosito GA, Hoffmann U, Vasan RS, Larson MG, et al. Pericardial fat volume correlates with inflammatory markers: the Framingham Heart Study. Obesity (Silver Spring, MD). 2010;18:1039–45.
Liu J, Fox CS, Hickson D, Bidulescu A, Carr JJ, Taylor HA. Fatty liver, abdominal visceral fat, and cardiometabolic risk factors: the Jackson Heart Study. Arterioscler Thromb Vasc Biol. 2011;31:2715–22.
Modi N, Murgasova D, Ruager-Martin R, Thomas EL, Hyde MJ, Gale C, et al. The influence of maternal body mass index on infant adiposity and hepatic lipid content. Pediatr Res. 2011;70:287–91.
Brumbaugh DE, Tearse P, Cree-Green M, Fenton LZ, Brown M, Scherzinger A, et al. Intrahepatic fat is increased in the neonatal offspring of obese women with gestational diabetes. J Pediatr. 2013;162:930–6. e931
Moschonis G, Kaliora AC, Karatzi K, Michaletos A, Lambrinou CP, Karachaliou AK, et al. Perinatal, sociodemographic and lifestyle correlates of increased total and visceral fat mass levels in schoolchildren in Greece: the Healthy Growth Study. Public Health Nutr. 2016;20:660–70.
Ensenauer R, Chmitorz A, Riedel C, Fenske N, Hauner H, Nennstiel-Ratzel U, et al. Effects of suboptimal or excessive gestational weight gain on childhood overweight and abdominal adiposity: results from a retrospective cohort study. Int J Obes (Lond). 2013;37:505–12.
Kaar JL, Crume T, Brinton JT, Bischoff KJ, McDuffie R, Dabelea D. Maternal obesity, gestational weight gain, and offspring adiposity: the exploring perinatal outcomes among children study. J Pediatr. 2014;165:509–15.
Gaillard R, Steegers EA, Franco OH, Hofman A, Jaddoe VW. Maternal weight gain in different periods of pregnancy and childhood cardio-metabolic outcomes. The Generation R Study. Int J Obes (Lond). 2015;39:677–85.
Santos S, Severo M, Gaillard R, Santos AC, Barros H, Oliveira A. The role of prenatal exposures on body fat patterns at 7 years: intrauterine programming or birthweight effects? Nutr Metab Cardiovasc Dis. 2016;26:1004–10.
Kooijman MN, Kruithof CJ, van Duijn CM, Duijts L, Franco OH, van IMH, et al. The Generation R Study: design and cohort update 2017. Eur J Epidemiol. 2016;31:1243–64.
Institute of Medicine and National Research Council Committee to Reexamine IOM Pregnancy Weight Guidelines. Weight Gain During Pregnancy: Reexamining the Guidelines. Washington, DC: National Academy Press; 2009.
Fredriks AM, van Buuren S, Wit JM, Verloove-Vanhorick SP. Body index measurements in 1996–7 compared with 1980. Arch Dis Child. 2000;82:107–12.
Gishti O, Gaillard R, Manniesing R, Abrahamse-Berkeveld M, van der Beek EM, Heppe DH, et al. Fetal and infant growth patterns associated with total and abdominal fat distribution in school-age children. J Clin Endocrinol Metab. 2014;99:2557–66.
Kaul S, Rothney MP, Peters DM, Wacker WK, Davis CE, Shapiro MD, et al. Dual-energy X-ray absorptiometry for quantification of visceral fat. Obesity (Silver Spring, MD). 2012;20:1313–8.
Hu HH, Nayak KS, Goran MI. Assessment of abdominal adipose tissue and organ fat content by magnetic resonance imaging. Obes Rev. 2011;12:e504–515.
Langeslag SJ, Schmidt M, Ghassabian A, Jaddoe VW, Hofman A, van der Lugt A, et al. Functional connectivity between parietal and frontal brain regions and intelligence in young children: the Generation R Study. Hum Brain Mapp. 2013;34:3299–307.
Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging. 2011;34:spcone.
VanItallie TB, Yang MU, Heymsfield SB, Funk RC, Boileau RA. Height-normalized indices of the body’s fat-free mass and fat mass: potentially useful indicators of nutritional status. Am J Clin Nutr. 1990;52:953–9.
Wells JC, Cole TJ, steam As. Adjustment of fat-free mass and fat mass for height in children aged 8 y. Int J Obes Relat Metab Disord. 2002;26:947–52.
Keijzer-Veen MG, Euser AM, van Montfoort N, Dekker FW, Vandenbroucke JP, Van Houwelingen HC. A regression model with unexplained residuals was preferred in the analysis of the fetal origins of adult diseases hypothesis. J Clin Epidemiol. 2005;58:1320–4.
Poston L, Caleyachetty R, Cnattingius S, Corvalan C, Uauy R, Herring S, et al. Preconceptional and maternal obesity: epidemiology and health consequences. Lancet Diabetes Endocrinol. 2016;4:1025–36.
Gaillard R, Durmus B, Hofman A, Mackenbach JP, Steegers EA, Jaddoe VW. Risk factors and outcomes of maternal obesity and excessive weight gain during pregnancy. Obesity (Silver Spring, MD). 2013;21:1046–55.
Liu J, Fox CS, Hickson DA, May WD, Hairston KG, Carr JJ, et al. Impact of abdominal visceral and subcutaneous adipose tissue on cardiometabolic risk factors: the Jackson Heart Study. J Clin Endocrinol Metab. 2010;95:5419–26.
Richmond RC, Timpson NJ, Felix JF, Palmer T, Gaillard R, McMahon G, et al. Using genetic variation to explore the causal effect of maternal pregnancy adiposity on future offspring adiposity: a Mendelian randomisation study. PLoS Med. 2017;14:e1002221.
Gaillard R, Santos S, Duijts L, Felix JF. Childhood health consequences of maternal obesity during pregnancy: a narrative review. Ann Nutr Metab. 2016;69:171–80.
Mamun AA, Mannan M, Doi SA. Gestational weight gain in relation to offspring obesity over the life course: a systematic review and bias-adjusted meta-analysis. Obes Rev. 2014;15:338–47.
Ugalde-Nicalo PA, Schwimmer JB. On the origin of pediatric nonalcoholic fatty liver disease. J Pediatr Gastroenterol Nutr. 2015;60:147–8.
Russell A, Gillespie S, Satya S, Gaudet LM. Assessing the accuracy of pregnant women in recalling pre-pregnancy weight and gestational weight gain. J Obstet Gynaecol Can. 2013;35:802–9.
Acknowledgements
We gratefully acknowledge the contribution of general practitioners, hospitals, midwives, and pharmacies in Rotterdam. The article is also available online as part of a thesis (https://www.generationr.nl/wp-content/uploads/2017/11/dissertation_Susana-Santos.pdf).
Author contributions
SS and VWVJ: conceived the study; SS, CM, and VWVJ: participated in the collection and statistical analysis of the data; SS and VWVJ: participated in the interpretation of the results; SS and VWVJ: drafted the manuscript; CM, JFF, LD, and RG: critically reviewed the manuscript; VWVJ: had primary responsibility for final content; and all authors: read and approved the final manuscript.
Funding
The general design of the Generation R Study is made possible by financial support from the Erasmus MC, University Medical Center, Rotterdam, Erasmus University Rotterdam, Netherlands Organization for Health Research and Development (ZonMw), Netherlands Organization for Scientific Research (NWO), Ministry of Health, Welfare and Sport and Ministry of Youth and Families. Research leading to these results has received funding from the European Union’s Seventh Framework Programme (FP7/2007-2013), project EarlyNutrition under grant agreement no. 289346, and the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 633595 (DynaHEALTH), and the European Union’s Horizon 2020 research and innovation programme under grant agreement 733206 (LifeCycle Project). LD received a grant from ERA-Net on Biomarkers for Nutrition and Health (696295, Horizon 2020; 529051014, ZonMW, The Netherlands, ALPHABET). RG received funding from the Dutch Heart Foundation (grant number 2017T013) and the Dutch Diabetes Foundation (grant number 2017.81.002). VWVJ received grants from the Netherlands Organization for Health Research and Development (VIDI 016.136.361) and the European Research Council (Consolidator Grant, ERC-2014-CoG-648916).
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Santos, S., Monnereau, C., Felix, J.F. et al. Maternal body mass index, gestational weight gain, and childhood abdominal, pericardial, and liver fat assessed by magnetic resonance imaging. Int J Obes 43, 581–593 (2019). https://doi.org/10.1038/s41366-018-0186-y
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DOI: https://doi.org/10.1038/s41366-018-0186-y
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