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Adult offspring of high-fat diet-fed dams can have normal glucose tolerance and body composition

  • K. M. Platt (a1), R. J. Charnigo (a2) and K. J. Pearson (a1)
Abstract

Maternal high-fat diet consumption and obesity have been shown to program long-term obesity and lead to impaired glucose tolerance in offspring. Many rodent studies, however, use non-purified, cereal-based diets as the control for purified high-fat diets. In this study, primiparous ICR mice were fed purified control diet (10–11 kcal% from fat of lard or butter origin) and lard (45 or 60 kcal% fat) or butter (32 or 60 kcal% fat)-based high-fat diets for 4 weeks before mating, throughout pregnancy, and for 2 weeks of nursing. Before mating, female mice fed the 32 and 60% butter-based high-fat diets exhibited impaired glucose tolerance but those females fed the lard-based diets showed normal glucose disposal following a glucose challenge. High-fat diet consumption by female mice of all groups decreased lean to fat mass ratios during the 4th week of diet treatment compared with those mice consuming the 10–11% fat diets. All females were bred to male mice and pregnancy and offspring outcomes were monitored. The body weight of pups born to 45% lard-fed dams was significantly increased before weaning, but only female offspring born to 32% butter-fed dams exhibited long-term body weight increases. Offspring glucose tolerance and body composition were measured for at least 1 year. Minimal, if any, differences were observed in the offspring parameters. These results suggest that many variables should be considered when designing future high-fat diet feeding and maternal obesity studies in mice.

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Copyright
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution licence http://creativecommons.org/licenses/by/3.0/
Corresponding author
*Address for correspondence: K. J. Pearson, Graduate Center for Nutritional Sciences, College of Medicine, University of Kentucky, 900 South Limestone, Lexington, KY 40536-0200, USA. (Email kevin.pearson@uky.edu)
References
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1. Ogden, CL, Carroll, MD, Kit, BK, Flegal, KM. Prevalence of obesity in the United States, 2009–2010. NCHS Data Brief. 2012; 82, 18.
2. Cawley, J, Meyerhoefer, C. The medical care costs of obesity: an instrumental variables approach. J Health Econ. 2012; 31, 219230.
3. Wang, Y, Beydoun, MA, Liang, L, Caballero, B, Kumanyika, SK. Will all Americans become overweight or obese? Estimating the progression and cost of the US obesity epidemic. Obesity. 2008; 16, 23232330.
4. Kissebah, AH, Peiris, AN. Biology of regional body fat distribution: relationship to non-insulin-dependent diabetes mellitus. Diabetes Metab Rev. 1989; 5, 83109.
5. Balkau, B, Deanfield, JE, Despres, JP, et al. International Day for the Evaluation of Abdominal Obesity (IDEA): a study of waist circumference, cardiovascular disease, and diabetes mellitus in 168,000 primary care patients in 63 countries. Circulation. 2007; 116, 19421951.
6. Vahratian, A. Prevalence of overweight and obesity among women of childbearing age: results from the 2002 National Survey of Family Growth. Matern Child Health J. 2009; 13, 268273.
7. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595601.
8. Barker, DJ, Gluckman, PD, Godfrey, KM, et al. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993; 341, 938941.
9. Roseboom, T, de Rooij, S, Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006; 82, 485491.
10. Tenenbaum-Gavish, K, Hod, M. Impact of maternal obesity on fetal health. Fetal Diagn Ther. 2013; 34, 17.
11. Whitaker, RC, Wright, JA, Pepe, MS, Seidel, KD, Dietz, WH. Predicting obesity in young adulthood from childhood and parental obesity. N Engl J Med. 1997; 337, 869873.
12. Gregorio, BM, Souza-Mello, V, Carvalho, JJ, Mandarim-de-Lacerda, CA, Aguila, MB. Maternal high-fat intake predisposes nonalcoholic fatty liver disease in C57BL/6 offspring. Am J Obstet Gynecol. 2010; 203, e491e498.
13. Lanham, SA, Roberts, C, Hollingworth, T, et al. Maternal high-fat diet: effects on offspring bone structure. Osteoporos Int. 2010; 21, 17031714.
14. Gniuli, D, Calcagno, A, Caristo, ME, et al. Effects of high-fat diet exposure during fetal life on type 2 diabetes development in the progeny. J Lipid Res. 2008; 49, 19361945.
15. Rother, E, Kuschewski, R, Alcazar, MA, et al. Hypothalamic JNK1 and IKKbeta activation and impaired early postnatal glucose metabolism after maternal perinatal high-fat feeding. Endocrinology. 2012; 153, 770781.
16. 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. Br J Nutr. 2007; 98, 843851.
17. White, CL, Purpera, MN, Morrison, CD. Maternal obesity is necessary for programming effect of high-fat diet on offspring. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R1464R1472.
18. Buckley, AJ, Keseru, B, Briody, J, et al. Altered body composition and metabolism in the male offspring of high fat-fed rats. Metabolism. 2005; 54, 500507.
19. Khan, I, Dekou, V, Hanson, M, Poston, L, Taylor, P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004; 110, 10971102.
20. Ornellas, F, Mello, VS, Mandarim-de-Lacerda, CA, Aguila, MB. Sexual dimorphism in fat distribution and metabolic profile in mice offspring from diet-induced obese mothers. Life Sci. 2013; 93, 454463.
21. Samuelsson, AM, Matthews, PA, Argenton, M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51, 383392.
22. Elahi, MM, Cagampang, FR, Mukhtar, D, et al. Long-term maternal high-fat feeding from weaning through pregnancy and lactation predisposes offspring to hypertension, raised plasma lipids and fatty liver in mice. Br J Nutr. 2009; 102, 514519.
23. Taylor, PD, McConnell, J, Khan, IY, et al. Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R134R139.
24. Ainge, H, Thompson, C, Ozanne, SE, Rooney, KB. A systematic review on animal models of maternal high fat feeding and offspring glycaemic control. Int J Obes (Lond). 2011; 35, 325335.
25. Nivoit, P, Morens, C, Van Assche, FA, et al. Established diet-induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009; 52, 11331142.
26. Masuyama, H, Hiramatsu, Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression. Endocrinology. 2012; 153, 28232830.
27. Dunn, GA, Bale, TL. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology. 2009; 150, 49995009.
28. Chechi, K, Herzberg, GR, Cheema, SK. Maternal dietary fat intake during gestation and lactation alters tissue fatty acid composition in the adult offspring of C57Bl/6 mice. Prostaglandins Leukot Essent Fatty Acids. 2010; 83, 97104.
29. Giraudo, SQ, Della-Fera, MA, Proctor, L, et al. Maternal high fat feeding and gestational dietary restriction: effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice. Pharmacol Biochem Behav. 2010; 97, 121129.
30. Gout, J, Sarafian, D, Mutel, E, et al. Metabolic and melanocortin gene expression alterations in male offspring of obese mice. Mol Cell Endocrinol. 2010; 319, 99108.
31. Hartil, K, Vuguin, PM, Kruse, M, et al. Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero. Pediatr Res. 2009; 66, 368373.
32. Liang, C, Oest, ME, Prater, MR. Intrauterine exposure to high saturated fat diet elevates risk of adult-onset chronic diseases in C57BL/6 mice. Birth Defects Res B Dev Reprod Toxicol. 2009; 86, 377384.
33. Howie, GJ, Sloboda, DM, Kamal, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905915.
34. Srinivasan, M, Katewa, SD, Palaniyappan, A, Pandya, JD, Patel, MS. 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.
35. Sun, B, Purcell, RH, Terrillion, CE, et al. Maternal high-fat diet during gestation or suckling differentially affects offspring leptin sensitivity and obesity. Diabetes. 2012; 61, 28332841.
36. Bieri, JG, Stoewsand, GS, Briggs, GM, Phillips, RW, Woodard, JC, Knapka, JJ. Report of the American Institute of Nutrition ad hoc Committee on standards for nutritional studies. J Nutr. 1977; 107, 13401348.
37. Reeves, PG. Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr. 1997; 127, 838S841S.
38. Heindel, JJ, vom Saal, FS. Meeting report: batch-to-batch variability in estrogenic activity in commercial animal diets – importance and approaches for laboratory animal research. Environ Health Perspect. 2008; 116, 389393.
39. Jensen, MN, Ritskes-Hoitinga, M. How isoflavone levels in common rodent diets can interfere with the value of animal models and with experimental results. Lab Anim. 2007; 41, 118.
40. Mead, MN. The feed factor: estrogenic variability in lab animal diets. Environ Health Perspect. 2006; 114, A640A642.
41. Samuelsson, AM, Matthews, PA, Jansen, E, Taylor, PD, Poston, L. Sucrose feeding in mouse pregnancy leads to hypertension, and sex-linked obesity and insulin resistance in female offspring. Front Physiol. 2013; 4, 14.
42. Douglas, G, Armitage, JA, Taylor, PD, et al. Cardiovascular consequences of life-long exposure to dietary isoflavones in the rat. J Physiol. 2006; 571, 477487.
43. Burton, JL, Wells, M. The effect of phytoestrogens on the female genital tract. J Clin Pathol. 2002; 55, 401407.
44. Chiang, SS, Pan, TM. Beneficial effects of phytoestrogens and their metabolites produced by intestinal microflora on bone health. Appl Microbiol Biotechnol. 2013; 97, 14891500.
45. Masilamani, M, Wei, J, Sampson, HA. Regulation of the immune response by soybean isoflavones. Immunol Res. 2012; 54, 95110.
46. Orgaard, A, Jensen, L. The effects of soy isoflavones on obesity. Exp Biol Med (Maywood). 2008; 233, 10661080.
47. Souzeau, E, Belanger, S, Picard, S, Deschepper, CF. Dietary isoflavones during pregnancy and lactation provide cardioprotection to offspring rats in adulthood. Am J Physiol Heart Circ Physiol. 2005; 289, H715H721.
48. Klein, SL, Wisniewski, AB, Marson, AL, Glass, GE, Gearhart, JP. Early exposure to genistein exerts long-lasting effects on the endocrine and immune systems in rats. Mol Med. 2002; 8, 742749.
49. Hilakivi-Clarke, L, Cho, E, Clarke, R. Maternal genistein exposure mimics the effects of estrogen on mammary gland development in female mouse offspring. Oncol Rep. 1998; 5, 609616.
50. Jefferson, WN, Padilla-Banks, E, Newbold, RR. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol Reprod. 2005; 73, 798806.
51. Sedova, L, Seda, O, Kazdova, L, et al. Sucrose feeding during pregnancy and lactation elicits distinct metabolic response in offspring of an inbred genetic model of metabolic syndrome. Am J Physiol Endocrinol Metab. 2007; 292, E1318E1324.
52. Platt, KM, Charnigo, RJ, Kincer, JF, Dickens, BJ, Pearson, KJ. Controlled exercise is a safe pregnancy intervention in mice. J Am Assoc Lab Anim Sci. 2013; 52, 524530.
53. Shimizu, R, Sakazaki, F, Okuno, T, Nakamuro, K, Ueno, H. Difference in glucose intolerance between C57BL/6J and ICR strain mice with streptozotocin/nicotinamide-induced diabetes. Biomed Res. 2012; 33, 6366.
54. Schlenker, E, Shi, Y, Johnson, C, Wipf, J. Acetazolamide affects breathing differently in ICR and C57 mice. Respir Physiol Neurobiol. 2006; 152, 119127.
55. Weizman, R, Paz, L, Backer, MM, et al. Mouse strains differ in their sensitivity to alprazolam effect in the staircase test. Brain Res. 1999; 839, 5865.
56. Miller, RA, Harrison, DE, Astle, CM, et al. An aging interventions testing program: study design and interim report. Aging Cell. 2007; 6, 565575.
57. Rebholz, SL, Jones, T, Burke, KT, et al. Multiparity leads to obesity and inflammation in mothers and obesity in male offspring. Am J Physiol Endocrinol Metab. 2012; 302, E449E457.
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