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

Published online by Cambridge University Press:  09 December 2016

R. Vidal-Santos ,
F. N. Macedo ,
M. N. S. Santana ,
V. U. De Melo ,
J. L. de Brito Alves ,
M. R. V. Santos ,
L. C. Brito ,
E. Nascimento ,
J. H. Costa-Silva  and
V. J. Santana-Filho
R. Vidal-Santos*
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
F. N. Macedo
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
M. N. S. Santana
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
V. U. De Melo
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
J. L. de Brito Alves
Affiliation:
Department of Physical Education and Sport Sciences, Academic Center of Vitória (CAV), Federal University of Pernambuco, Vitória do Santo Antão, Brazil
M. R. V. Santos
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
L. C. Brito
Affiliation:
Department of Nutrition, Federal University of Sergipe, São Cristovão, Brazil
E. Nascimento
Affiliation:
Department of Nutrition, Federal University of Pernambuco, Recife, Brazil
J. H. Costa-Silva
Affiliation:
Department of Physical Education and Sport Sciences, Academic Center of Vitória (CAV), Federal University of Pernambuco, Vitória do Santo Antão, Brazil
V. J. Santana-Filho
Affiliation:
Department of Physiology, Federal University of Sergipe, São Cristovão, Brazil
*
*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 [email protected])
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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.

Keywords

autonomic controlhypertensionoffspringwesternized diet
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 2 , April 2017 , pp. 216 - 225
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Copyright
© Cambridge University Press 2016. This is a work of the U.S. Government and is not subject to copyright protection in the United States. 

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References

1. Popkin, BM, Gordon-Larsen, P. The nutrition transition: worldwide obesity dynamics and their determinants. Int J Obes Relat Meta. Disord. 2004; 28, S2–S9.CrossRefGoogle ScholarPubMed
2. Popkin, BM, Adair, LS, Ng, SW. Global nutrition transition and the pandemic of obesity in developing countries. Nutr Rev. 2012; 70, 3–21.CrossRefGoogle ScholarPubMed
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, 789–793.CrossRefGoogle ScholarPubMed
4. Batista Filho, M, Rissin, A. Nutritional transition in Brazil: geographic and temporal trends. Cad Saude Publica. 2003; 19(Suppl. 1), S181–S191.CrossRefGoogle ScholarPubMed
5. Buettner, R, Scholmerich, J, Bollheimer, LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring). 2007; 15, 798–808.CrossRefGoogle ScholarPubMed
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, 607–615.CrossRefGoogle ScholarPubMed
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, 3219–3230.CrossRefGoogle ScholarPubMed
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, 437–445.CrossRefGoogle ScholarPubMed
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, 606–615.CrossRefGoogle Scholar
10. Tennant, IA, Barnett, AT, Thompson, DS, et al. Impaired cardiovascular structure and function in adult survivors of severe acute malnutrition. Hypertension. 2014; 64, 664–671.CrossRefGoogle ScholarPubMed
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, 123–130.CrossRefGoogle ScholarPubMed
12. Mehta, SH. Nutrition and pregnancy. Clin Obstet Gynecol. 2008; 51, 409–418.CrossRefGoogle ScholarPubMed
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, 1157–1168.CrossRefGoogle ScholarPubMed
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, 1435–1442.CrossRefGoogle ScholarPubMed
15. Grassi, G, Seravalle, G, Dell’Oro, R, et al. Adrenergic and reflex abnormalities in obesity-related hypertension. Hypertension. 2000; 36, 538–542.CrossRefGoogle ScholarPubMed
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, 403–408.CrossRefGoogle ScholarPubMed
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, R1007–1015.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 68–89.CrossRefGoogle Scholar
20. Kohsaka, A, Laposky, AD, Ramsey, KM, et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 2007; 6, 414–421.CrossRefGoogle ScholarPubMed
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, 1939–1951.CrossRefGoogle Scholar
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, 177–196.CrossRefGoogle Scholar
23. Novelli, EL, Diniz, YS, Galhardi, CM, et al. Anthropometrical parameters and markers of obesity in rats. Lab Anim. 2007; 41, 111–119.CrossRefGoogle ScholarPubMed
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, S79–81.Google ScholarPubMed
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, 1043–1065.CrossRefGoogle Scholar
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, 499–502.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 12–19.CrossRefGoogle ScholarPubMed
29. Martini, G, Riva, P, Rabbia, F, et al. Heart rate variability in childhood obesity. Clin Auton Res. 2001; 11, 87–91.CrossRefGoogle ScholarPubMed
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, 924–928.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
32. Willett, WC. Is dietary fat a major determinant of body fat? Am J Clin Nutr. 1998; 67, 556S–562S.CrossRefGoogle Scholar
33. Ascherio, A, Katan, MB, Zock, PL, et al. Trans fatty acids and coronary heart disease. N Engl J Med. 1999; 340, 1994–1998.CrossRefGoogle ScholarPubMed
34. Barker, DJ. Fetal origins of coronary heart disease. BMJ. 1995; 311, 171–174.CrossRefGoogle ScholarPubMed
35. Gluckman, PD. Editorial: nutrition, glucocorticoids, birth size, and adult disease. Endocrinology. 2001; 142, 1689–1691.CrossRefGoogle ScholarPubMed
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, 3–8.CrossRefGoogle Scholar
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, 938–947.CrossRefGoogle ScholarPubMed
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, R134–R139.CrossRefGoogle ScholarPubMed
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, 383–392.CrossRefGoogle ScholarPubMed
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, 820–829.CrossRefGoogle ScholarPubMed
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, 951–961.CrossRefGoogle ScholarPubMed
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, 843–851.CrossRefGoogle Scholar
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, 920–926.CrossRefGoogle ScholarPubMed
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, 2833–2841.CrossRefGoogle ScholarPubMed
45. Brandorff, NP. The effect of dietary fat on the fatty acid composition of lipids secreted in rats’ milk. Lipids. 1980; 15, 276–278.CrossRefGoogle ScholarPubMed
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, 458–462.CrossRefGoogle ScholarPubMed
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, 12107–12119.CrossRefGoogle ScholarPubMed
48. Lee, EB, Ahima, RS. Alteration of hypothalamic cellular dynamics in obesity. J Clin Invest. 2012; 122, 22–25.CrossRefGoogle ScholarPubMed
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, 1378–1387.CrossRefGoogle ScholarPubMed
50. Erlanson-Albertsson, C. How palatable food disrupts appetite regulation. Basic Clin Pharmacol Toxicol. 2005; 97, 61–73.CrossRefGoogle ScholarPubMed
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, 905–915.CrossRefGoogle ScholarPubMed
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, 1–5.Google Scholar
53. Dandona, P, Aljada, A, Chaudhuri, A, et al. Endothelial dysfunction, inflammation and diabetes. Rev Endocr Metab Dis. 2004; 5, 189–197.CrossRefGoogle ScholarPubMed
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.), 118–121.Google ScholarPubMed
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, 2075–2080.CrossRefGoogle ScholarPubMed
56. Després, JP, Lemieux, I, Tchernof, A, et al. Distribution et métabolisme des masses grasses. Diabetes Metab. 2001; 27, 209–214.Google Scholar
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, 149–157.CrossRefGoogle Scholar
58. Paige, SL, Plonowska, K, Xu, A, et al. Molecular regulation of cardiomyocyte differentiation. Circ Res. 2015; 116, 341–353.CrossRefGoogle ScholarPubMed
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, 615–626.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, E944–E953.CrossRefGoogle ScholarPubMed
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, 1562–1570.CrossRefGoogle ScholarPubMed
63. Unger, J, McNeill, TH, Moxley, RT III, et al. Distribution of insulin receptor-like immunoreactivity in the rat forebrain. Neuroscience. 1989; 31, 143–157.CrossRefGoogle ScholarPubMed
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, 3234–3236.CrossRefGoogle ScholarPubMed
65. Sim, LJ, Joseph, SA. Arcuate nucleus projections to brainstem regions which modulate nociception. J Chem Neuroanat. 1991; 4, 97–109.CrossRefGoogle ScholarPubMed
66. Geerling, JC, Shin, JW, Chimenti, PC, et al. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J Comp Neurol. 2010; 518, 1460–1499.CrossRefGoogle Scholar
67. Adachi, A, Kobashi, M, Funahashi, M. Glucose-responsive neurons in the brainstem. Obes Res. 1995; 3(Suppl. 5), 735S–740S.CrossRefGoogle ScholarPubMed
68. Dallaporta, M, Himmi, T, Perrin, J, et al. Solitary tract nucleus sensitivity to moderate changes in glucose level. Neuroreport. 1999; 10, 2657–2660.CrossRefGoogle ScholarPubMed
69. Mizuno, Y, Oomura, Y. Glucose responding neurons in the nucleus tractus solitarius of the rat: in vitro study. Brain Res. 1984; 307, 109–116.CrossRefGoogle ScholarPubMed
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, G1050–G1057.CrossRefGoogle Scholar
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, 191–197.CrossRefGoogle ScholarPubMed
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, 15–21.CrossRefGoogle ScholarPubMed
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, 1939–1945.CrossRefGoogle ScholarPubMed
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, 1381–1393.CrossRefGoogle ScholarPubMed
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, 781–789.CrossRefGoogle ScholarPubMed
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, 1239–1248.CrossRefGoogle ScholarPubMed
77. Schneider, JG, Tilly, N, Hierl, T, et al. Elevated plasma endothelin-1 levels in diabetes mellitus. Am J Hypertens. 2002; 15, 967–972.CrossRefGoogle ScholarPubMed
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, 889–900.CrossRefGoogle ScholarPubMed
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, 91–102.CrossRefGoogle ScholarPubMed
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, 714–726.CrossRefGoogle ScholarPubMed
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, 2823–2830.CrossRefGoogle ScholarPubMed
82. Vinson, C, Chatterjee, R. CG methylation. Epigenomics. 2012; 4, 655–663.CrossRefGoogle ScholarPubMed