Skip to main content Accessibility help
×
Home

Western diet in the perinatal period promotes dysautonomia in the offspring of adult rats

  • R. Vidal-Santos (a1), F. N. Macedo (a1), M. N. S. Santana (a1), V. U. De Melo (a1), J. L. de Brito Alves (a2), M. R. V. Santos (a1), L. C. Brito (a3), E. Nascimento (a4), J. H. Costa-Silva (a2) and V. J. Santana-Filho (a1)...

Abstract

The present study investigated the impact of a western diet during gestation and lactation on the anthropometry, serum biochemical, blood pressure and cardiovascular autonomic control on the offspring. Male Wistar rats were divided into two groups according to their mother’s diet received: control group (C: 18% calories of lipids) and westernized group (W: 32% calories of lipids). After weaning both groups received standard diet. On the 60th day of life, blood samples were collected for the analysis of fasting glucose and lipidogram. Cardiovascular parameters were measured on the same period. Autonomic nervous system modulation was evaluated by spectrum analysis of heart rate (HR) and systolic arterial pressure (SAP). The W increased glycemia (123±2 v. 155±2 mg/dl), low-density lipoprotein (15±1 v. 31±2 mg/dl), triglycerides (49±1 v. 85±2 mg/dl), total cholesterol (75±2 v. 86±2 mg/dl), and decreased high-density lipoprotein (50±4 v. 38±3 mg/dl), as well as increased body mass (209±4 v. 229±6 g) than C. Furthermore, the W showed higher SAP (130±4 v. 157±2 mmHg), HR (357±10 v. 428±14 bpm), sympathetic modulation to vessels (2.3±0.56 v. 6±0.84 mmHg2) and LF/HF ratio (0.15±0.01 v. 0.7±0.2) than C. These findings suggest that a western diet during pregnancy and lactation leads to overweight associated with autonomic misbalance and hypertension in adulthood.

Copyright

Corresponding author

*Address for correspondence: R. V. dos Santos, Department of Physiology, Federal University of Sergipe, Frei Paulo St. 445, apt 303, Building Pegasus, Aracaju/SE 49052-270, Brazil. (Email robervanvidal@hotmail.com)

References

Hide All
1. Popkin, BM, Gordon-Larsen, P. The nutrition transition: worldwide obesity dynamics and their determinants. Int J Obes Relat Meta. Disord. 2004; 28, S2S9.
2. Popkin, BM, Adair, LS, Ng, SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012; 70, 321.
3. Feoli, AM, Roehrig, C, Rotta, LN, et al. Serum and liver lipids in rats and chicks fed with diets containing different oils. Nutrition. 2003; 19, 789793.
4. Batista Filho, M, Rissin, A. Nutritional transition in Brazil: geographic and temporal trends. Cad Saude Publica. 2003; 19(Suppl. 1), S181S191.
5. Buettner, R, Scholmerich, J, Bollheimer, LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring). 2007; 15, 798808.
6. Langley-Evans, SC, Welham, SJ, Sherman, RC, et al. Weanling rats exposed to maternal low-protein diets during discrete periods of gestation exhibit differing severity of hypertension. Clin Sci. 1996; 91, 607615.
7. Bayol, SA, Simbi, BH, Bertrand, JA, et al. Offspring from mothers fed a ‘junk food’ diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol. 2008; 586, 32193230.
8. Costa-Silva, JH, Silva, PA, Pedi, N, et al. Chronic undernutrition alters renal active Na+ transport in young rats: potential hidden basis for pathophysiological alterations in adulthood? Eur J Nutr. 2009; 48, 437445.
9. de Brito Alves, JL, Nogueira, VO, de Oliveira, GB, et al. Short- and long-term effects of a maternal low-protein diet on ventilation, O2/CO2 chemoreception and arterial blood pressure in male rat offspring. Br J Nutr. 2014; 111, 606615.
10. Tennant, IA, Barnett, AT, Thompson, DS, et al. Impaired cardiovascular structure and function in adult survivors of severe acute malnutrition. Hypertension. 2014; 64, 664671.
11. Barros, MA, De Brito Alves, JL, Nogueira, VO, et al. Maternal low-protein diet induces changes in the cardiovascular autonomic modulation in male rat offspring. Nutr Metab Cardiovasc Dis. 2015; 25, 123130.
12. Mehta, SH. Nutrition and pregnancy. Clin Obstet Gynecol. 2008; 51, 409418.
13. Ferro Cavalcante, TC, Lima da Silva, JM, da Marcelino da Silva, AA, et al. Effects of a westernized diet on the reflexes and physical maturation of male rat offspring during the perinatal period. Lipids. 2013; 48, 11571168.
14. Karlen-Amarante, M, da Cunha, NV, de Andrade, O, et al. Altered baroreflex and autonomic modulation in monosodium glutamate-induced hyperadipose rats. Metabolism. 2012; 61, 14351442.
15. Grassi, G, Seravalle, G, Dell’Oro, R, et al. Adrenergic and reflex abnormalities in obesity-related hypertension. Hypertension. 2000; 36, 538542.
16. Carlson, SH, Shelton, J, White, CR, et al. Elevated sympathetic activity contributes to hypertension and salt sensitivity in diabetic obese Zucker rats. Hypertension. 2000; 35, 403408.
17. Overton, JM, Williams, TD, Chambers, JB, et al. Cardiovascular and metabolic responses to fasting and thermoneutrality are conserved in obese Zucker rats. Am J Physiol Regul Integr Comp Physiol. 2001; 280, R10071015.
18. Schreihofer, AM, Mandel, DA, Mobley, SC, et al. Impairment of sympathetic baroreceptor reflexes in obese Zucker rats. Am J Physiol Heart Circ Physiol. 2007; 293, H2543.
19. Sandovici, I, Hoelle, K, Angiolini, E, et al. Placental adaptations to the maternal-fetal environment: implications for fetal growth and developmental programming. Reprod Biomed Online. 2012; 25, 6889.
20. Kohsaka, A, Laposky, AD, Ramsey, KM, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 2007; 6, 414421.
21. Reeves, PG, Nielsen, FH, Fahey, GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123, 19391951.
22. Carvalho, MF, Evangelista da Costa, MKM, Muniz, GS, et al. Experimental diet based on the foods listed in the Family Budget Survey is more detrimental to growth than to the reflex development of rats. Rev. Nutr. 2013; 26, 177196.
23. Novelli, EL, Diniz, YS, Galhardi, CM, et al. Anthropometrical parameters and markers of obesity in rats. Lab Anim. 2007; 41, 111119.
24. Bertinieri, G, di Rienzo, M, Cavallazzi, A, et al. A new approach to analysis of the arterial baroreflex. J Hypertens Suppl Off J Int Soc Hypertens. 1985; 3, S7981.
25. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996; 93, 10431065.
26. Friedewald, WT, Levy, RI, Fredrickson, DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972; 18, 499502.
27. Yuan, Q, Chen, L, Liu, C, et al. Postnatal pancreatic islet beta cell function and insulin sensitivity at different stages of lifetime in rats born with intrauterine growth retardation. PLoS One. 2011; 6, e25167.
28. Gutin, B, Barbeau, P, Litaker, MS, et al. Heart rate variability in obese children: relations to total body and visceral adiposity, and changes with physical training and detraining. Obes Res. 2000; 8, 1219.
29. Martini, G, Riva, P, Rabbia, F, et al. Heart rate variability in childhood obesity. Clin Auton Res. 2001; 11, 8791.
30. Soares-Miranda, L, Alves, AJ, Vale, S, et al. Central fat influences cardiac autonomic function in obese and overweight girls. Pediatr Cardiol. 2011; 32, 924928.
31. Taylor, AE, Sandeep, MN, Janipalli, CS, et al. Associations of FTO and MC4R variants with obesity traits in Indians and the role of rural/urban environment as a possible effect modifier. J Obes. 2011; 2011, 307542.
32. Willett, WC. Is dietary fat a major determinant of body fat? Am J Clin Nutr. 1998; 67, 556S562S.
33. Ascherio, A, Katan, MB, Zock, PL, et al. Trans fatty acids and coronary heart disease. N Engl J Med. 1999; 340, 19941998.
34. Barker, DJ. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171174.
35. Gluckman, PD. Editorial: nutrition, glucocorticoids, birth size, and adult disease. Endocrinology. 2001; 142, 16891691.
36. Armitage, JA, Taylor, PD, Poston, L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005; 565, 38.
37. 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, 938947.
38. 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.
39. 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.
40. Wang, X, Liu, X, Zhan, Y, et al. Pharmacogenomic, physiological, and biochemical investigations on safety and efficacy biomarkers associated with the peroxisome proliferator-activated receptor-gamma activator rosiglitazone in rodents: a translational medicine investigation. J Pharmacol Exp Ther. 2010; 334, 820829.
41. Bayol, SA, Simbi, BH, Stickland, NC. A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol. 2005; 567, 951961.
42. 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.
43. Laraia, BA, Bodnar, LM, Siega-Riz, AM. Pregravid body mass index is negatively associated with diet quality during pregnancy. Public Health Nutr. 2007; 10, 920926.
44. 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.
45. Brandorff, NP. The effect of dietary fat on the fatty acid composition of lipids secreted in rats’ milk. Lipids. 1980; 15, 276278.
46. Del Prado, M, Delgado, G, Villalpando, S. Maternal lipid intake during pregnancy and lactation alters milk composition and production and litter growth in rats. J Nutr. 1997; 127, 458462.
47. Chang, GQ, 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.
48. Lee, EB, Ahima, RS. Alteration of hypothalamic cellular dynamics in obesity. J Clin Invest. 2012; 122, 2225.
49. Vickers, MH, Clayton, ZE, Yap, C, et al. Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology. 2011; 152, 13781387.
50. Erlanson-Albertsson, C. How palatable food disrupts appetite regulation. Basic Clin Pharmacol Toxicol. 2005; 97, 6173.
51. Howie, GJ, Sloboda, DM, Kamal, T, et al. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905915.
52. Ferro Cavalvante, TCF, Silva, AAM, Lira, MCA, et al. Early exposure of dams to a westernized diet has long-term consequences on food intake and physiometabolic homeostasis of the rat offspring. Int J Food Sci Nutr. 2014; 8, 15.
53. Dandona, P, Aljada, A, Chaudhuri, A, et al. Endothelial dysfunction, inflammation and diabetes. Rev Endocr Metab Dis. 2004; 5, 189197.
54. Delzenne, N, Ferre, P, Beylot, M, et al. Study of the regulation by nutrients of the expression of genes involved in lipogenesis and obesity in humans and animals. Nutr Metab Cardiovasc Dis. 2001; 11(Suppl.), 118121.
55. Uyeda, KL, Yamashita, H, Kawaguchi, T. Carbohydrate responsive element-binding protein (ChREBP): a key regulator of glucose metabolism and fat storage. Biochem Pharmacol. 2002; 63, 20752080.
56. Després, JP, Lemieux, I, Tchernof, A, et al. Distribution et métabolisme des masses grasses. Diabetes Metab. 2001; 27, 209214.
57. Valenzuela, AB, Nieto, SK. Ácidos grasos omega-6 y omega-3 en la nutrición perinatal: su importância em el desarrolo del sistema nervioso y visual. Rev Chil Pediatr. 2003; 74, 149157.
58. Paige, SL, Plonowska, K, Xu, A, et al. Molecular regulation of cardiomyocyte differentiation. Circ Res. 2015; 116, 341353.
59. Danfeng, W, Siyu, C, Mei, L, et al. Maternal obesity disrupts circadian rhythms of clock and metabolic genes in the offspring heart and liver. Inform Healthcare J. 2015; 32, 615626.
60. Wu, KL, Chun-Ying, H, Julie, YHC, et al. An increase in adenosine-5’-triphosphate (ATP) content in rostral ventrolateral medulla is engaged in the high fructose diet-induced hypertension. J Biomed Sci. 2014; 21, 8.
61. Bardgett, ME, Amanda, LS, Glenn, MT. Activation of corticotropin-releasing factor receptors in the rostral ventrolateral medulla is required for glucose-induced sympathoexcitation. Am J Physiol Endocrinol Metab. 2014; 307, E944E953.
62. Werther, GA, Hogg, A, Oldfield, BJ, et al. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology. 1987; 121, 15621570.
63. Unger, J, McNeill, TH, Moxley, RT III, et al. Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience. 1989; 31, 143157.
64. Marks, JL, Porte, D Jr, Stahl, WL, et al. Localization of insulin receptor mRNA in rat brain by in situ hybridization. Endocrinology. 1990; 127, 32343236.
65. Sim, LJ, Joseph, SA. Arcuate nucleus projections to brainstem regions which modulate nociception. J Chem Neuroanat. 1991; 4, 97109.
66. Geerling, JC, Shin, JW, Chimenti, PC, et al. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol. 2010; 518, 14601499.
67. Adachi, A, Kobashi, M, Funahashi, M. Glucose-responsive neurons in the brainstem. Obes Res. 1995; 3(Suppl. 5), 735S740S.
68. Dallaporta, M, Himmi, T, Perrin, J, et al. Solitary tract nucleus sensitivity to moderate changes in glucose level. Neuroreport. 1999; 10, 26572660.
69. Mizuno, Y, Oomura, Y. Glucose responding neurons in the nucleus tractus solitarius of the rat: in vitro study. Brain Res. 1984; 307, 109116.
70. Wan, S, Browning, KN. Glucose increases synaptic transmission from vagal afferent central nerve terminals via modulation of 5-HT3 receptors. Am J Physiol Gastrointest Liver Physiol. 2008; 295, G1050G1057.
71. Yettefti, K, Orsini, JC, el Ouazzani, T, et al. Sensitivity of nucleus tractus solitarius neurons to induced moderate hyperglycemia, with special reference to catecholaminergic regions. J Auton Nerv Syst. 1995; 51, 191197.
72. Camargo, RL, Torrezan, R, de Oliveira, JC, et al. An increase in glucose concentration in the lateral ventricles of the brain induces changes in autonomic nervous system activity. Neurol Res. 2013; 35, 1521.
73. Inoguchi, T, Li, P, Umeda, F, et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes. 2000; 49, 19391945.
74. Cassuto, J, Dou, H, Czikora, I, et al. Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients. Diabetes. 2014; 63, 13811393.
75. Zhu, M, Wen, M, Sun, X, et al. Propofol protects against high glucose-induced endothelial apoptosis and dysfunction in human umbilical vein endothelial cells. Anesth Analg. 2015; 120, 781789.
76. Park, JY, Takahara, N, Gabriele, A, et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes. 2000; 49, 12391248.
77. Schneider, JG, Tilly, N, Hierl, T, et al. Elevated plasma endothelin-1 levels in diabetes mellitus. Am J Hypertens. 2002; 15, 967972.
78. Maloyan, A, Muralimanoharan, S, Huffman, S, et al. Identification and comparative analyses of myocardial miRNAs involved in the fetal response to maternal obesity. Physiol Genomics. 2013; 45, 889900.
79. Aagaard-Tillery, KM, Grove, K, Bishop, J, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol. 2008; 41, 91102.
80. Suter, M, Bocock, P, Showalter, L, et al. Epigenomics: maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J. 2011; 25, 714726.
81. 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.
82. Vinson, C, Chatterjee, R. CG methylation. Epigenomics. 2012; 4, 655663.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed