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Unlimited access to low-energy diet causes acute malnutrition in dams and alters biometric and biochemical parameters in offspring

Published online by Cambridge University Press:  14 November 2013

E. do Nascimento ,
G. de Santana Muniz ,
M. das Graças de Santana Muniz ,
L. de Souza Alexandre ,
L. S. da Rocha ,
C. G. Leandro ,
R. M. de Castro  and
F. Bolaños-Jimenez
E. do Nascimento*
Affiliation:
Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil
G. de Santana Muniz
Affiliation:
Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil
M. das Graças de Santana Muniz
Affiliation:
Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil
L. de Souza Alexandre
Affiliation:
Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil
L. S. da Rocha
Affiliation:
Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil
C. G. Leandro
Affiliation:
Department of Physical Education and Sports Science, CAV -Federal University of Pernambuco, Brazil
R. M. de Castro
Affiliation:
Department of Nutrition, Federal University of Pernambuco, Brazil
F. Bolaños-Jimenez
Affiliation:
INRA, UMR 1280, Physiologie des Adaptations, Nutritionnelles, Université de Nantes, Nantes Atlantique Université, Nantes, France
*
*Address for correspondence: E. do Nascimento, Department of Nutrition, Laboratory of Experimental Nutrition and Dietetic, Federal University of Pernambuco, Brazil. (Email: [email protected])
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Abstract

Here we analyze the outcomes of unlimited access to a low-energy (LE) diet in dams and their offspring. At 3 weeks’ gestation, pregnant Wistar rats were divided into two groups: (1) the control group received a normoenergetic diet; and (2) the experimental group received the LE diet. In dams, lactation outcomes, food intake, body weight, plasma IGF-1, prealbumin, transferrin and retinol-binding protein levels were evaluated; in offspring, biometric and biochemical parameters and food intake were evaluated. No differences were observed during pregnancy. However, after lactation, dams that received the LE diet demonstrated significant reductions in body weight (P<0.05), plasma IGF-1 (P=0.01), prealbumin and visceral fat (P<0.001). Pups born to dams that received the LE diet demonstrated reduced body length and weight at weaning (P<0.001) and were lighter than the control animals at the end of the experimental period. Pups also demonstrated reduced plasma, low-density lipoprotein (P=0.04), triglycerides (P=0.002) and glucose levels (P<0.05), and differences were noted in visceral fat. These results indicate that feeding dams with LE diet during the reproductive period induces acute malnutrition and impairs the growth and development of offspring, as well as certain metabolic parameters.

Keywords

biochemistrybiometrylow-energy dietrats
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 1 , February 2014 , pp. 45 - 55
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2013 

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References

1. Kirchengast, S, Hartmann, B. Maternal prepregnancy weight status and pregnancy weight gain as major determinants for newborn weight and size. Ann Hum Biol. 1998; 25, 17–28.Google Scholar
2. Gopalakrishnan, GS, Gardner, DS, Dandrea, J, et al. Influence of maternal pre pregnancy body composition and diet during early-mid pregnancy on cardiovascular function and nephron number in juvenile sheep. Br J Nutr. 2005; 94, 938–947.Google Scholar
3. Symonds, ME, Pearce, S, Bispham, J, et al. Timing of nutrient restriction and programming of fetal adipose tissue development. Proc Nutr Soc. 2004; 63, 397–403.Google Scholar
4. Ayala, MR, Racotta, R, Hernández-Montes, H, Quevedo, L. Some metabolic effects on lactating rats of a low-energy diet restricted in good-quality protein. Br J Nutr. 2006; 96, 667–673.Google Scholar
5. Friggens, NC, Hay, DEF, Oldham, JD. Interactions between major nutrients in the diet and the lactational performance of rats. Br J Nutr. 1993; 69 59–71.Google Scholar
6. Fowden, AL, Ward, JW, Wooding, FP, et al. Programming placental nutrient transport capacity. J Physiol. 2006; 572 5–15.Google Scholar
7. Herrera, E, Gomez-Coronado, D, Lasuncion, MA. Lipid metabolism in pregnancy. Biol Neonate. 1987; 51, 70–77.CrossRefGoogle ScholarPubMed
8. Álvarez-Ordás, I, Gutiérrez, JM, Casado, C, et al. Effects of maternal food restriction on the evolution of pregnancy in the rat. Rev Esp Fisiol. 1992; 48 277–284.Google Scholar
9. Cañas, R, Romero, JJ, Baldwin, RL. Maintenance energy requirements during lactation in rats. J Nutr. 1982; 112 1876–1890.CrossRefGoogle ScholarPubMed
10. Dewey, KG. Energy and protein requirements during lactation. 462. Annu Rev Nutr. 1997; 17, 19–36.CrossRefGoogle Scholar
11. Desai, M, Gayle, D, Babu, J, Ross, MG. The timing of nutrient restriction during rat 465 pregnancy/lactation alters metabolic syndrome phenotype. Am J Obstet Gynecol. 2007; 196, 555e1–555e7.Google Scholar
12. Passos, MCF, Ramos, CF, Moura, EG. Short and long term effect of malnutrition in rats during lactation on the body weight of offspring. Nutrition Research. 2000; 20 1603–1612.Google Scholar
13. Byrne, CD. Programming other hormones that affect insulin. Br Med Bull. 2001; 60, 153–171.Google Scholar
14. Bertin, E, Gangnerau, MNL, Bellon, G, et al. Development of β-cell mass in fetuses of rats deprived of protein and/or energy in last trimester of pregnancy. Am J Physiol Regul Integr Comp Physiol. 2002; 283, R623–R630.Google Scholar
15. Fernandez-Twinn, DS, Ozanne, SE. Mechanisms by wich poor early growth programs type-2 diabetes, obesity and metabolic syndrome. Physiol Behav. 2006; 88, 234–243.Google Scholar
16. Armitage, JA, Khan, IY, Taylor, PD, et al. Developmental 484 programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals. J Physiol. 2004; 561, 355–377.CrossRefGoogle Scholar
17. Cherala, G, Shapiro, BH, D’Mello, AP. Two low protein diets differentially affect food consumption and reproductive performance in pregnant and lactating rats and long-term growth in their offspring. J Nutr. 2006; 136, 2827–2833.CrossRefGoogle ScholarPubMed
18. Josephine, FW. Effects of pregnancy, sucrose, and various low-protein diets on the eating behavior of rats. Physiol Behav. 1997; 62, 779–782.Google Scholar
19. Xu, RY, Wan, YP, Tang, QY, et al. Carbohydrate-to-fat ratio affects food intake and body weight in Wistar rats. Exp Biol Med. 2010; 235, 833–838.Google Scholar
20. Dutriez-Casteloot, I, Breton, C, Coupé, B, et al. Tissue-specific programming expression of glucocorticoid receptors and 11 beta-HSDs by maternal perinatal undernutrition in the HPA axis of adult male rats. Horm Metab Res. 2008; 40, 257–261.Google Scholar
21. Léonhardt, M, Lesage, J, Dufourny, L, et al. Perinatal maternal food restriction induces alterations in hypothalamo-pituitary-adrenal axis activity and in plasma corticosterone-binding globulin capacity of weaning rat pups. Neuroendocrinology. 2002; 75, 45–54.Google Scholar
22. Mendoza, J, Pévet, P, Challet, E. High-fat feeding alters the clock synchronization to light. J Physiol. 2008; 586, 5901–5910.CrossRefGoogle ScholarPubMed
23. Reeves, PG. Components of the AIN-93 diets as improvements in 509 the AIN-76 diet. J Nutr. 1997; 127, 838s–841s.Google Scholar
24. Muniz, GS, Silva, AM, Cavalcante, TC, et al. Early physical activity minimizes the adverse effects of a low-energy diet on growth and development parameters. Nutr Neurosci. 2013; 16, 113–124.Google Scholar
25. Lopes de Souza, S, Orozco-Solis, R, Grit, I, et al. Perinatal protein restriction reduces the inhibitory action of serotonin on food intake. Eur J Neurosci. 2008; 27, 1400–1408.Google Scholar
26. Novelli, ELB, Diniz, YS, Galhardi, CM, et al. Anthropometrical parameters and markers of obesity in rats. Lab Anim. 2007; 41, 111–119.Google Scholar
27. Bernardis, LL. Prediction of carcass fat, water and lean body mass from Lee’s nutritive ratio in rats with hypothalamic obesity. Experientia. 1970; 26, 789–790.Google Scholar
28. Lui, JC, Forcinito, P, Chang, M, et al. Coordinated postnatal down-regulation of multiple growth-promoting genes: evidence for a genetic program limiting organ growth. FASEB J. 2010; 24, 3083–3092.Google Scholar
29. 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. Br J Nutr. 2004; 92, 513–520.Google Scholar
30. Zhang, Y, Li, N, Yang, J, et al. Effects of maternal food restriction on physical growth and neurobehavior in newborn Wistar rats. Brain Res Bull. 2010; 83, 1–8.Google Scholar
31. De Moura, EG, Lisboa, PC, Custódio, CM, et al. Malnutrition 533 during lactation changes growth hormone mRNA expression in offspring at weaning and in adulthood. J Nutr Biochem. 2007; 18, 134–139.Google Scholar
32. Palou, M, Priego, T, Sánchez, J, et al. Moderate caloric restriction in lactating rats protects offspring against obesity and insulin resistance in later life. Endrocrinology. 2010; 151, 1030–1041.Google Scholar
33. Nascimento, E, Omar, G, Delacourt, N, et al. Long-Lasting effect of perinatal exposure to l-tryptophan on circadian clock of primary cell lines established from male offspring born from mothersfed on dietary protein restriction. PLoS One. 2013; 8, e5631.Google Scholar
34. Denis, RGP, Bing, C, Brocklehurst, S, et al. Diurnal changes in hypothalamic neuropeptide and SOCS-3 expression: effects of lactation and relationship with serum leptin and food intake. J Endocrinol. 2004; 183, 173–181.Google Scholar
35. Moretto, VL, Ballen, MO, Gonçalves, TSS, et al. Low-protein diet during lactation and maternal metabolism in rats. ISRN Obstet Gynecol. 2011; 2011, 1–7.CrossRefGoogle ScholarPubMed
36. Sampson, DA, Jansen, GR. Measurement of milk yield in the lactating rat from pup weight and weight gain. J Pediatr Gastroenterol Nutr. 1984; 3, 613–617.Google Scholar
37. Marchini, JS, Moriguti, JC, Padovan, GJ, et al. Métodos atuais de investigação do metabolismo proteico: aspectos básicos e estudos experimentais e clínicos. Medicina. 1998; 31, 22–30.Google Scholar
38. Flint, DJ, Vernon, RG. Effects of food restriction on the responses of the mammary gland and adipose tissue to prolactin and growth hormone in the lactting rat. J Endocrinol. 1998; 156, 299–305.Google Scholar
39. Picarel-Blanchot, F, Alvarez, C, Bailbe, D, et al. Changes in insulin action and insulin secretion in the rat after dietary restriction early in life: infuence of food restriction versus low-protein food restriction. Metabolism. 1995; 44, 1519–1526.Google Scholar
40. Stellwagen, D, Shatz, CJ. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron. 2002; 33, 357–367.Google Scholar
41. Sutton, GM, Centanni, AV, Butler, AA. Protein malnutrition pregnancy in C57BL/6J mice results in offspring with altered circadian physiology before obesity. Endocrinology. 2010; 151, 1570–1580.Google Scholar
42. Kwon, DH, Kang, W, Nam, YS, et al. Dietary protein restriction induces steatohepatitis and alters leptin/signal transducers and activators of transcription 3 signaling in lactating rats. J Nutr Biochem. 2012; 23, 791–799.Google Scholar
43. Poore, KR, Cleal, JK, Newman, JP, et al. Nutritional challenges during development induce sex-specific changes in glucose homeostasis in the adult sheep. Am J Physiol Endocrinol Metab. 2007; 292, E32–E39.CrossRefGoogle ScholarPubMed
44. Fernandes, FS, Carmo, MGT, Herrera, E. Influence of maternal diet during early pregnancy on the fatty acid profile in the fetus at late pregnancy in rats. Lipids. 2012; 47, 505–517.Google Scholar
45. Fernandes, RMP, Abrue, AV, Schanaider, A, et al. Effects of protein and energy restricted diet during lactation leads to persistent morphological changes on tibia growth in the weaned pups. Int J Morphol. 2007; 25, 565–571.Google Scholar
46. Reichling, TD, German, RZ. Bones muscles and organs of protein malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. J Nutr. 2000; 130, 2326–2332.CrossRefGoogle ScholarPubMed
47. Bayne, K. Revised Guide for the Care and Use of Laboratory Animals available. American Physiological Society. The Physiologist. 1996; 39, 199–208.Google Scholar