Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-16T01:20:20.807Z Has data issue: false hasContentIssue false

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
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])

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.

Type
Original Article
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2013 

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

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, 136140.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, 804814.Google Scholar
5.Anderson, JW, Patterson, K. Snack foods: comparing nutrition values of excellent choices and ‘junk foods’. J Am Coll Nutr. 2005; 24, 155156.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, 11091117.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, 21672179.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, 843851.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, R768R778.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, 924932.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, 785793.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, 964978.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, 1210712119.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, R1464R1472.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, 12751284.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, 221230.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, 513520.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, R528R538.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, R20R28.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, 11331142.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, 47564764.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, 53485356.CrossRefGoogle ScholarPubMed
24.Simerly, RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci. 2002; 25, 507536.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, 383392.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, E792E799.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, R675R681.CrossRefGoogle ScholarPubMed