Skip to main content
Log in

Short-term moderate exercise provides long-lasting protective effects against metabolic dysfunction in rats fed a high-fat diet

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Introduction

A sedentary lifestyle and high-fat feeding are risk factors for cardiometabolic disorders. This study determined whether moderate exercise training prevents the cardiometabolic changes induced by a high-fat diet (HFD).

Materials and methods

Sixty-day-old rats were subjected to moderate exercise three times a week for 30 days. After that, trained rats received a HFD (EXE-HFD) or a commercial normal diet (EXE-NFD) for 30 more days. Sedentary animals also received the diets (SED-HFD and SED-NFD). Food intake and body weight were measured weekly. After 120 days of life, analyses were performed. Data were analysed with two-way ANOVA and the Tukey post-test.

Results

Body weight gain induced by HFD was attenuated in trained animals. HFD reduced food intake by approximately 30 % and increased body fat stores by approximately 75 %. Exercise attenuated 80 % of the increase in fat pads and increased 24 % of soleus muscle mass in NFD animals. HFD induced a hyper-response to glucose injection, and exercise attenuated this response by 50 %. Blood pressure was increased by HFD, and the beneficial effect of exercise in reducing blood pressure was inhibited by HFD. HFD increased vagal activity by 65 % in SED-HFD compared with SED-NFD rats, and exercise blocked this increase. HFD reduced sympathetic activity and inhibited the beneficial effect of exercise on ameliorating sympathetic activity.

Conclusion

Four weeks of moderate exercise at low frequency was able to prevent the metabolic changes induced by a HFD but not the deleterious effects of diet on the cardiovascular system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Casazza K, Dulin-Keita A, Gower BA, Fernandez JR (2009) Differential influence of diet and physical activity on components of metabolic syndrome in a multiethnic sample of children. J Am Diet Assoc 109(2):236–244

    Article  Google Scholar 

  2. Lopez-Jaramillo P, Lahera V, Lopez-Lopez J (2011) Epidemic of cardiometabolic diseases: a Latin American point of view. Ther Adv Cardiovasc Dis 5(2):119–131

    Article  Google Scholar 

  3. Ervin RB (2009) Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States, 2003–2006. Natl Health Stat Rep 5(13):1–7

    Google Scholar 

  4. Deshmukh-Taskar PR, O’Neil CE, Nicklas TA, Yang SJ, Liu Y, Gustat J et al (2009) Dietary patterns associated with metabolic syndrome, sociodemographic and lifestyle factors in young adults: the Bogalusa heart study. Public Health Nutr 12(12):2493–2503

    Article  Google Scholar 

  5. Buettner R, Scholmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity 15(4):798–808

    Article  CAS  Google Scholar 

  6. pBarnes MJ, Lapanowski K, Conley A, Rafols JA, Jen KL, Dunbar JC (2003) High fat feeding is associated with increased blood pressure, sympathetic nerve activity and hypothalamic mu opioid receptors. Brain Res Bull 61(5):511–519

    Article  Google Scholar 

  7. Gomes RM, Tofolo LP, Rinaldi W, Scomparin DX, Grassiolli S, Barella LF et al (2013) Moderate exercise restores pancreatic beta-cell function and autonomic nervous system activity in obese rats induced by high-fat diet. Cell Physiol Biochem 32(2):310–321

    Article  CAS  Google Scholar 

  8. Prior LJ, Eikelis N, Armitage JA, Davern PJ, Burke SL, Montani JP et al (2010) Exposure to a high-fat diet alters leptin sensitivity and elevates renal sympathetic nerve activity and arterial pressure in rabbits. Hypertension 55(4):862–868

    Article  CAS  Google Scholar 

  9. Wang H, Storlien LH, Huang XF (1999) Influence of dietary fats on c-Fos-like immunoreactivity in mouse hypothalamus. Brain Res 843(1–2):184–192

    CAS  Google Scholar 

  10. Chen F, Cham JL, Badoer E (2010) High-fat feeding alters the cardiovascular role of the hypothalamic paraventricular nucleus. Am J Physiol Regul Integr Comp Physiol 298(3):R799–R807

    Article  CAS  Google Scholar 

  11. Matsuo T, Iwashita S, Komuro M, Suzuki M (1999) Effects of high-fat diet intake on glucose uptake in central and peripheral tissues of non-obese rats. J Nutr Sci Vitaminol 45(5):667–673

    Article  CAS  Google Scholar 

  12. Armitage JA, Burke SL, Prior LJ, Barzel B, Eikelis N, Lim K et al (2012) Rapid onset of renal sympathetic nerve activation in rabbits fed a high-fat diet. Hypertension 60(1):163–171

    Article  CAS  Google Scholar 

  13. Schwartz JH, Young JB, Landsberg L (1983) Effect of dietary fat on sympathetic nervous system activity in the rat. J Clin Investig 72(1):361–370

    Article  CAS  Google Scholar 

  14. Barella LF, de Oliveira JC, Branco RC, Camargo RL, Gomes RM, Mendes FC et al (2012) Early exposure to a high-fat diet has more drastic consequences on metabolism compared with exposure during adulthood in rats. Horm Metab Res 44(6):458–464

    Article  CAS  Google Scholar 

  15. Afonso RA, Lautt WW, Schafer J, Legare DJ, Oliveira AG, Macedo MP (2010) High-fat diet results in postprandial insulin resistance that involves parasympathetic dysfunction. Br J Nutr 104(10):1450–1459

    Article  CAS  Google Scholar 

  16. Scomparin DX, Grassiolli S, Marcal AC, Gravena C, Andreazzi AE, Mathias PC (2006) Swim training applied at early age is critical to adrenal medulla catecholamine content and to attenuate monosodium l-glutamate-obesity onset in mice. Life Sci 79(22):2151–2156

    Article  CAS  Google Scholar 

  17. Levin BE (2005) Factors promoting and ameliorating the development of obesity. Physiol Behav 86(5):633–639

    Article  CAS  Google Scholar 

  18. Dishman RK, Berthoud HR, Booth FW, Cotman CW, Edgerton VR, Fleshner MR et al (2006) Neurobiology of exercise. Obesity 14(3):345–356

    Article  CAS  Google Scholar 

  19. Rothman SM, Griffioen KJ, Wan R, Mattson MP (2012) Brain-derived neurotrophic factor as a regulator of systemic and brain energy metabolism and cardiovascular health. Ann NY Acad Sci 1264(1):49–63

    Article  CAS  Google Scholar 

  20. Wang Q, Wang M, Whim MD (2013) Neuropeptide y gates a stress-induced, long-lasting plasticity in the sympathetic nervous system. J Neurosci 33(31):12705–12717

    Article  CAS  Google Scholar 

  21. Malta A, de Oliveira JC, Ribeiro TA, Tofolo LP, Barella LF, Prates KV, et al. (2014). Low protein diet in adult male rats has long term effects on metabolism. J Endocrinol 221(2):285–295

    Article  CAS  Google Scholar 

  22. Chao PT, Terrillion CE, Moran TH, Bi S (2011) High-fat diet offsets the long-lasting effects of running-wheel access on food intake and body weight in OLETF rats. Am J Physiol Regul Integr Comp Physiol 300(6):R1459–R1467

    Article  CAS  Google Scholar 

  23. Yasari S, Paquette A, Charbonneau A, Gauthier MS, Savard R, Lavoie JM (2006) Effects of ingesting a high-fat diet upon exercise-training cessation on fat accretion in the liver and adipose tissue of rats. Appl Physiol Nutr Metab 31(4):367–375

    Article  CAS  Google Scholar 

  24. Applegate EA, Upton DE, Stern JS (1984) Exercise and detraining: effect on food intake, adiposity and lipogenesis in Osborne–Mendel rats made obese by a high fat diet. J Nutr 114(2):447–459

    CAS  Google Scholar 

  25. Scomparin DX, Grassiolli S, Gomes RM, Torrezan R, de Oliveira JC, Gravena C et al (2011) Low-Intensity swimming training after weaning improves glucose and lipid homeostasis in MSG hypothalamic obese mice. Endocr Res 36(2):83–90

    Article  CAS  Google Scholar 

  26. Achten J, Jeukendrup AE (2004) Optimizing fat oxidation through exercise and diet. Nutrition 20(7–8):716–727

    Article  CAS  Google Scholar 

  27. Negrao CE, Moreira ED, Santos MC, Farah VM, Krieger EM (1992) Vagal function impairment after exercise training. J Appl Physiol 72(5):1749–1753

    CAS  Google Scholar 

  28. Vicente LL, de Moura EG, Lisboa PC, Monte Alto Costa A, Amadeu T, Mandarim-de-Lacerda CA et al (2004) Malnutrition during lactation in rats is associated with higher expression of leptin receptor in the pituitary of adult offspring. Nutrition 20(10):924–928

    Article  CAS  Google Scholar 

  29. Milanski M, Arruda AP, Coope A, Ignacio-Souza LM, Nunez CE, Roman EA et al (2012) Inhibition of hypothalamic inflammation reverses diet-induced insulin resistance in the liver. Diabetes 61(6):1455–1462

    Article  CAS  Google Scholar 

  30. Baudrie V, Laude D, Elghozi JL (2007) Optimal frequency ranges for extracting information on cardiovascular autonomic control from the blood pressure and pulse interval spectrograms in mice. Am J Physiol Regul Integr Comp Physiol 292(2):R904–R912

    Article  CAS  Google Scholar 

  31. Palma-Rigo K, Baudrie V, Laude D, Elghozi JL (2010) Cardiovascular rhythms and cardiac baroreflex sensitivity in AT1A receptor gain-of function mutant mice. Hypertension 55:1507–1508

    Google Scholar 

  32. Bi S, Scott KA, Hyun J, Ladenheim EE, Moran TH (2005) Running wheel activity prevents hyperphagia and obesity in Otsuka long-evans Tokushima Fatty rats: role of hypothalamic signaling. Endocrinology 146(4):1676–1685

    Article  CAS  Google Scholar 

  33. Patterson CM, Dunn-Meynell AA, Levin BE (2008) Three weeks of early-onset exercise prolongs obesity resistance in DIO rats after exercise cessation. Am J Physiol Regul Integr Comp Physiol 294(2):R290–R301

    Article  CAS  Google Scholar 

  34. Borst SE, Conover CF (2005) High-fat diet induces increased tissue expression of TNF-alpha. Life Sci 77(17):2156–2165

    Article  CAS  Google Scholar 

  35. Sclafani A (2001) Psychobiology of food preferences. Int J Obes Relat Metab Disor 25(Suppl 5):S13–S16

    Article  Google Scholar 

  36. Warwick ZS, Schiffman SS (1992) Role of dietary fat in calorie intake and weight gain. Neurosci Biobehav Rev 16(4):585–596

    Article  CAS  Google Scholar 

  37. Schutz Y, Flatt JP, Jequier E (1989) Failure of dietary fat intake to promote fat oxidation: a factor favoring the development of obesity. Am J Clin Nutr 50(2):307–314

    CAS  Google Scholar 

  38. Rinaldi B, Donniacuo M, Sodano L, Gritti G, Signoriello S, Parretta E et al (2013) Effects of sildenafil on the gastrocnemius and cardiac muscles of rats in a model of prolonged moderate exercise training. PLoS One 8(7):e69954

    Article  CAS  Google Scholar 

  39. Sasaki H, Ohtsu T, Ikeda Y, Tsubosaka M, Shibata S (2014) Combination of meal and exercise timing with a high-fat diet influences energy expenditure and obesity in mice. Chronobiol Int 9:1–17

    Google Scholar 

  40. Cruciani-Guglielmacci C, Vincent-Lamon M, Rouch C, Orosco M, Ktorza A, Magnan C (2005) Early changes in insulin secretion and action induced by high-fat diet are related to a decreased sympathetic tone. Am J Physiol Endocrinol Metab 288(1):E148–E154

    Article  CAS  Google Scholar 

  41. Wagener A, Schmitt AO, Brockmann GA (2012) Early and late onset of voluntary exercise have differential effects on the metabolic syndrome in an obese mouse model. Exp Clin Endocrinol Diabetes 120(10):591–597

    Article  CAS  Google Scholar 

  42. Shima K, Shi K, Mizuno A, Sano T, Ishida K, Noma Y (1996) Exercise training has a long-lasting effect on prevention of non-insulin-dependent diabetes mellitus in Otsuka-Long-Evans-Tokushima Fatty rats. Metabolism 45(4):475–480

    Article  CAS  Google Scholar 

  43. Laker RC, Gallo LA, Wlodek ME, Siebel AL, Wadley GD, McConell GK (2011) Short-term exercise training early in life restores deficits in pancreatic beta-cell mass associated with growth restriction in adult male rats. Am J Physiol Endocrinol Metab 301(5):E931–E940

    Article  CAS  Google Scholar 

  44. Andreazzi AE, Scomparin DX, Mesquita FP, Balbo SL, Gravena C, De Oliveira JC et al (2009) Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium l-glutamate-obesity in mice. J Endocrinol 201(3):351–359

    Article  CAS  Google Scholar 

  45. Scomparin DX, Gomes RM, Grassiolli S, Rinaldi W, Martins AG, de Oliveira JC et al (2009) Autonomic activity and glycemic homeostasis are maintained by precocious and low intensity training exercises in MSG-programmed obese mice. Endocrine 36(3):510–517

    Article  CAS  Google Scholar 

  46. Van Vliet BN, Hall JE, Mizelle HL, Montani JP, Smith MJ Jr (1995) Reduced parasympathetic control of heart rate in obese dogs. Am J Physiol 269(2 Pt 2):H629–H637

    Google Scholar 

  47. Pelat M, Verwaerde P, Lazartiques E, Cabrol P, Galitzky J, Berlan M et al (1998) Variabilite temporelle et frequentielle de la pression arterielle et de la frequence cardiaque au cours du nycthemere dans un modele experimental d’hypertension arterielle avec obesite [Twenty-four hour time and frequency domain variability of systolic blood pressure and heart rate in an experimental model of arterial hypertension plus obesity]. Arch Mal Coeur Vaiss 91(8):999–1002

    CAS  Google Scholar 

  48. Morgan DA, Thedens DR, Weiss R, Rahmouni K (2008) Mechanisms mediating renal sympathetic activation to leptin in obesity. Am J Physiol Regul Integr Comp Physiol 295(6):R1730–R1736

    Article  CAS  Google Scholar 

  49. Rahmouni K, Morgan DA, Morgan GM, Mark AL, Haynes WG (2005) Role of selective leptin resistance in diet-induced obesity hypertension. Diabetes 54(7):2012–2018

    Article  CAS  Google Scholar 

  50. Hilzendeger AM, Morgan DA, Brooks L, Dellsperger D, Liu X, Grobe JL et al (2012) A brain leptin-renin angiotensin system interaction in the regulation of sympathetic nerve activity. Am J Physiol Heart Circ Physiol 303(2):H197–H206

    Article  CAS  Google Scholar 

  51. Himeno E, Nishino K, Okazaki T, Nanri H, Ikeda M (1999) A weight reduction and weight maintenance program with long-lasting improvement in left ventricular mass and blood pressure. Am J Hypertens 12(7):682–690

    Article  CAS  Google Scholar 

  52. Moraes-Silva IC, Mostarda C, Moreira ED, Silva KA, dos Santos F, de Angelis K et al (2013) Preventive role of exercise training in autonomic, hemodynamic, and metabolic parameters in rats under high risk of metabolic syndrome development. J Appl Physiol 114(6):786–791

    Article  CAS  Google Scholar 

  53. Morvan E, Lima NE, Machi JF, Mostarda C, De Angelis K, Irigoyen MC et al (2013) Metabolic, hemodynamic and structural adjustments to low intensity exercise training in a metabolic syndrome model. Cardiovasc Diabetol 12(1):89

    Article  CAS  Google Scholar 

  54. Mostarda C, Moraes-Silva IC, Salemi VM, Machi JF, Rodrigues B, De Angelis K et al (2012) Exercise training prevents diastolic dysfunction induced by metabolic syndrome in rats. Clinics 67(7):815–820

    Article  Google Scholar 

  55. Barboza CA, Rocha LY, Mostarda CT, Figueroa D, Caperuto EC, De Angelis K et al (2013) Ventricular and autonomic benefits of exercise training persist after detraining in infarcted rats. Eur J Appl Physiol 113(5):1137–1146

    Article  Google Scholar 

  56. Mostarda C, Rogow A, Silva IC, De La Fuente RN, Jorge L, Rodrigues B et al (2009) Benefits of exercise training in diabetic rats persist after three weeks of detraining. Auton Neurosci 145(1–2):11–16

    Article  CAS  Google Scholar 

  57. Silva KA, da Silva Luiz R, Rampaso RR, de Abreu NP, Moreira ED, Mostarda CT et al (2012) Previous exercise training has a beneficial effect on renal and cardiovascular function in a model of diabetes. PLoS One 7(11):e48826

    Article  CAS  Google Scholar 

  58. Agarwal D, Dange RB, Vila J, Otamendi AJ, Francis J (2012) Detraining differentially preserved beneficial effects of exercise on hypertension: effects on blood pressure, cardiac function, brain inflammatory cytokines and oxidative stress. PLoS One 7(12):e52569

    Article  CAS  Google Scholar 

  59. Mattson MP, Wan R (2008) Neurotrophic factors in autonomic nervous system plasticity and dysfunction. Neuromolecular Med 10(3):157–168

    Article  CAS  Google Scholar 

  60. Neeper SA, Gomez-Pinilla F, Choi J, Cotman CW (1996) Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res 726(1–2):49–56

    Article  CAS  Google Scholar 

  61. Russo-Neustadt A, Beard RC, Cotman CW (1999) Exercise, antidepressant medications, and enhanced brain derived neurotrophic factor expression. Neuropsychopharmacology 21(5):679–682

    Article  CAS  Google Scholar 

  62. Hasegawa A (1991) Innervation of skeletal muscle by the lumbar sympathetic nervous system. Nihon Seikeigeka Gakkai zasshi 65(5):368–381

    CAS  Google Scholar 

  63. Cotman CW, Berchtold NC, Christie LA (2007) Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30(9):464–472

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by Grants from the Brazilian Research National Foundation: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) by receipt of the scholarship from Ciências em Fronteiras Program (Process No. 10040/13-7) and Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPQ.

Conflict of interest

The author declares no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paulo Cezar de Freitas Mathias.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tófolo, L.P., da Silva Ribeiro, T.A., Malta, A. et al. Short-term moderate exercise provides long-lasting protective effects against metabolic dysfunction in rats fed a high-fat diet. Eur J Nutr 54, 1353–1362 (2015). https://doi.org/10.1007/s00394-014-0816-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0816-7

Keywords

Navigation