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The effects of prenatal exposure to a ‘junk food’ diet on offspring food preferences and fat deposition can be mitigated by improved nutrition during lactation

Published online by Cambridge University Press:  06 August 2013

J. R. Gugusheff ,
M. Vithayathil ,
Z. Y. Ong  and
B. S. Muhlhausler
J. R. Gugusheff
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, South Australia, Australia
M. Vithayathil
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, South Australia, Australia
Z. Y. Ong
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, South Australia, Australia
B. S. Muhlhausler*
Affiliation:
FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, South Australia, Australia
*
*Address for correspondence: Dr B. Muhlhausler, FOODplus Research Centre, School of Agriculture Food and Wine, The University of Adelaide, Adelaide 5064, Australia. (Email [email protected])
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Abstract

Exposure to a maternal junk food (JF) diet in utero and during the suckling period has been demonstrated to increase the preference for palatable food and increase the susceptibility to diet-induced obesity in adult offspring. We aimed to determine whether the effects of prenatal exposure to JF could be ameliorated by cross-fostering offspring onto dams consuming a standard rodent chow during the suckling period. We report here that when all offspring were given free access to the JF diet for 7 weeks from 10 weeks of age, male offspring of control (C) or JF dams that were cross-fostered at birth onto JF dams (C-JF, JF-JF), exhibited higher fat (C-C: 12.3 ± 0.34 g/kg/day; C-JF: 14.7 ± 1.04 g/kg/day; JF-C: 11.5 ± 0.41 g/kg/day; JF-JF: 14.0 ± 0.44 g/kg/day; P < 0.05) and overall energy intake (C-C: 930.1 ± 18.56 kJ/kg/day; C-JF: 1029.0 ± 82.9 kJ/kg/day; JF-C: 878.3 ± 19.5 kJ/kg/day; JF-JF: 1003.4 ± 25.97 kJ/kg/day; P < 0.05) than offspring exposed to the JF diet only before birth (JF-C) or not at all (C-C). Female offspring suckled by JF dams, despite no differences in food intake, had increased fat mass as percentage of body weight (C-C: 19.9 ± 1.33%; C-JF: 22.8 ± 1.57%; JF-C: 17.4 ± 1.03%; JF-JF: 22.0 ± 1.0%; P < 0.05) after 3 weeks on the JF diet. No difference in fat mass was observed in male offspring. These findings suggest that the effects of prenatal exposure to a JF diet on food preferences in females and susceptibility to diet-induced obesity in males can be prevented by improved nutrition during the suckling period.

Keywords

cross-fosteringfood preferencesnutritional programming
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 4 , Issue 5 , October 2013 , pp. 348 - 357
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2013 

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References

1. WHO. World Health Organisation Fact Sheet: obesity and overweight, 2011. Retrieved 15 January 2013 from http://www.who.int/mediacentre/factsheets/fs311/en/index.htmlGoogle Scholar
2.Dodd, JM, Grivell, RM, Nguyen, AM, et al. Maternal and perinatal health outcomes by body mass index category. Aust N Z J Obstet Gynaecol. 2011; 51, 136–140.Google Scholar
3.Athukorala, C, Rumbold, AR, Willson, KJ, et al. The risk of adverse pregnancy outcomes in women who are overweight or obese. BMC Pregnancy Childbirth. 2010; 10, 56.Google Scholar
4.Swinburn, BA, Sacks, G, Hall, KD, et al. The global obesity pandemic: shaped by global drivers and local environments. The Lancet. 2011; 378, 804–814.Google Scholar
5.Anderson, JW, Patterson, K. Snack foods: comparing nutrition values of excellent choices and ‘junk foods’. J Am Coll Nutr. 2005; 24, 155–156.Google Scholar
6.Sampey, BP, Vanhoose, AM, Winfield, HM, et al. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity. 2011; 19, 1109–1117.Google Scholar
7.Ong, Z, Muhlhausler, B. Maternal ‘junk-food’ feeding of rat dams alters food choices and development of the mesolimbic reward pathway in the offspring. FASEB J. 2011; 25, 2167–2179.Google Scholar
8.Bayol, SA, Farrington, SJ, Stickland, NC. 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. Brit J Nut. 2007; 98, 843–851.CrossRefGoogle Scholar
9.Gorski, JN, Dunn-Meynell, AA, Hartman, TG, et al. Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance. Am J Physiol Regul Intergr Comp Physiol. 2006; 291, R768–R778.Google Scholar
10.Teegarden, SL, Scott, AN, Bale, TL. Early life exposure to a high fat diet promotes long-term changes in dietary preferences and central reward signaling. Neuroscience. 2009; 162, 924–932.Google Scholar
11.Wright, TM, Fone, KCF, Langley-Evans, SC, et al. Exposure to maternal consumption of cafeteria diet during the lactation period programmes feeding behaviour in the rat. Int J Dev Neurosci. 2011; 29, 785–793.Google Scholar
12.Akyol, A, McMullen, S, Langley-Evans, SC. Glucose intolerance associated with early-life exposure to maternal cafeteria feeding is dependent upon post-weaning diet. Br J Nutr. 2011; 1, 964–978.Google Scholar
13.Chang, G-Q, Gaysinskaya, V, Karatayev, O, et al. Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci. 2008; 28, 12107–12119.Google Scholar
14.Chen, H, Simar, D, Morris, MJ. Hypothalamic neuroendocrine circuitry is programmed by maternal obesity: interaction with postnatal nutritional environment. PLoS ONE. 2009; 4, e6259.Google Scholar
15.White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Intergr Comp Physiol. 2009; 296, R1464–R1472.CrossRefGoogle ScholarPubMed
16.Gugusheff, JR, Ong, ZY, Muhlhausler, BS. A maternal ‘junk-food’ diet reduces sensitivity to the opioid antagonist naloxone in offspring postweaning. FASEB J. 2012; 27, 1275–1284.Google Scholar
17.Zambrano, E, Bautista, C, Deas, M, et al. A low maternal protein diet during pregnancy and lactation has sex and window of exposure specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571, 221–230.CrossRefGoogle ScholarPubMed
18.Bellinger, L, Lilley, C, Langley-Evans, SC. Prenatal exposure to a maternal low-protein diet programmes a preference for high-fat foods in the young adult rat. Brit J Nut. 2004; 92, 513–520.Google Scholar
19.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.CrossRefGoogle ScholarPubMed
20.Mitra, A, Alvers, KM, Crump, EM, et al. Effect of high-fat diet during gestation, lactation, or postweaning on physiological and behavioral indexes in borderline hypertensive rats. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R20–R28.CrossRefGoogle ScholarPubMed
21.Nivoit, P, Morens, C, Van Assche, F, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009; 52, 1133–1142.Google Scholar
22.Vucetic, Z, Kimmel, J, Totoki, K, et al. Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology. 2010; 151, 4756–4764.Google Scholar
23.Chen, H, Simar, D, Lambert, K, et al. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology. 2008; 149, 5348–5356.CrossRefGoogle ScholarPubMed
24.Simerly, RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci. 2002; 25, 507–536.Google Scholar
25.Samuelsson, A-M, Matthews, PA, Argenton, M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance. Hypertension. 2008; 51, 383–392.Google Scholar
26.Srinivasan, M, Katewa, SD, Palaniyappan, A, et al. Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab. 2006; 291, E792–E799.Google Scholar
27.Shelley, P, Martin-Gronert, MS, Rowlerson, A, et al. Altered skeletal muscle insulin signaling and mitochondrial complex II-III linked activity in adult offspring of obese mice. Am J Physiol Regul Intergr Comp Physiol. 2009; 297, R675–R681.CrossRefGoogle ScholarPubMed