Negative effect of high-calorie high-salt diet on spleen oxidant/antioxidants and structure: preventive effects of sprint interval training

Document Type : Research Paper

Authors

Department of Physical Education and Sport, Shahed University, Tehran, Iran

10.22070/jbcp.2022.17049.1163

Abstract

Objective: We investigated the effect of a high-calorie high-salt diet and sprint interval training on oxidant/antioxidant status and structural changes in the spleen of male Wistar rats.
Materials and Methods: Eighteen male Wistar rats were randomized into three groups: normal diet (ND), high-calorie high-salt diet (HCSD), and HCSD + sprint interval training (HCSD+SIT). Rats in HCSD and HCSD+SIT groups were under a high-calorie high-salt diet. The SIT (4-9 reps of 10 s duration sprints) performed 3 sessions/week for 8 weeks. Forty-eight hours after the last training session, spleen was removed and used for the assessment of oxidant/antioxidant status and histomorphometric parameters.
Results: Results revealed that compared to the ND group, superoxide dismutase (SOD) activity, glutathione peroxidase (GPx) level, and total antioxidant capacity (TAC) were significantly lower (P<0.001) and malondialdehyde (MDA) level was significantly higher in the spleen tissue of the HCSD group (P<0.001) and there was no significant difference between the HCSD+SIT and ND groups in none of the assessed variables (P>0.05). Moreover, there was a significant increase in the red to white pulp ratio and a significant decrease in the number of lymph cells and splenic trabecular volume in the HCSD group (P<0.001). Nonetheless, in none of the assessed morphometric parameters, a significant difference was observed between the HCSD+SIT and ND groups (P>0.05).
Conclusion: It seems that SIT training may avert HCSD-induced unfavourable changes in the spleen oxidant/antioxidant status and counteract the deleterious effects of the HCSD on the spleen structure.

Keywords


  1. Fuente M, Miquel J. An Update of the Oxidation-Inflammation Theory of Aging: The Involvement of the Immune System in Oxi-Inflamm-Aging. Current Pharmaceutical Design 2009.;15(26):3003–26. doi:10.2174/138161209789058110.
  2. Chiu CJ, Liu S, Willett WC, Wolever TM, Brand-Miller JC, Barclay AWi. Informing food choices and health outcomes by use of the dietary glycemic index. Nutrition Reviews 2011.;69(4):231–42. doi: 10.1111/j.1753-4887.2011.00382.x.
  3. Mayyas F, Alzoubi KH, Al-Taleb Z. Impact of high fat/high salt diet on myocardial oxidative stress. Clinical and Experimental Hypertension 2017.;39(2):126–32. doi: 10.1080/10641963.2016.1226894.
  4. Hunsche C, Hernandez O, De la Fuente M. Impaired Immune Response in Old Mice Suffering from Obesity and Premature Immunosenescence in Adulthood. The Journals of Gerontology 2016.;71(8):983–91. doi: 10.1093/gerona/glv082.
  5. Aleksandrova K, Koelman L, Rodrigues CE. Dietary patterns and biomarkers of oxidative stress and inflammation: A systematic review of observational and intervention studies. Redox Biology 2021.;42:101869. doi: 10.1016/j.redox.2021.101869.
  6. Buchan L, St Aubin CR, Fisher AL, Hellings A, Castro M, Al-Nakkash L. High-fat, high-sugar diet induces splenomegaly that is ameliorated with exercise and genistein treatment. BMC Research Notes 2018.;11(1):1–6. doi: 10.1186/S13104-018-3862-Z/FIGURES/3. 10.
  7. Steffany E, Santana S, Alves De Oliveira C, Iranni F, Lima A. Effect of Resistance Training and Diet Intake on Spleen Structure of Ovariectomized Wistar Rats. Journal of Health and Allied Sciences 2022.;12(01):47–52. doi: 10.1055/S-0041-1732812.
  8. Gheorghe A, Pérez de Heredia F, Hunsche C, Redondo N, Díaz LE, Hernández O. Oxidative stress and immunosenescence in spleen of obese mice can be reversed by 2-hydroxyoleic acid. Experimental Physiology 2017.;102(5):533–44. doi: 10.1113/EP086157/FULL.
  9. Unruh D, Srinivasan R, Benson T, Haigh S, Coyle D, Batra N. Red blood cell dysfunction induced by high-fat diet: Potential implications for obesity-related atherosclerosis. Circulation 2015.;132(20):1898–908. doi: 0.1161/CIRCULATIONAHA.115.017313.
  10. Bronte V, Pittet MJ. The Spleen in Local and Systemic Regulation of Immunity. Immunity 2013.;39(5):806–18. doi: 10.1016/J.IMMUNI.2013.10.010.
  11. Gotoh K, Inoue M, Masaki T, Chiba S, Shiraishi K, Shimasaki T. Obesity-related chronic kidney disease is associated with spleen-derived IL-10. Nephrology Dialysis Transplantation 2013.;28(5):1120–30. doi: 10.1093/NDT/GFS440.
  12. Fibbins H, Ward PB, Watkins A, Curtis J, Rosenbaum S. Improving the health of mental health staff through exercise interventions: a systematic review. Journal of Mental Health 2018.;27(2):184–91. doi: 10.1080/09638237.2018.1437614.
  13. Vollaard NBJ, Metcalfe RS, Williams S. Effect of number of sprints in an SIT session on change in v O2max: A meta-analysis. Sv. 49, Medicine and Science in Sports and Exercise. Lippincott Williams and Wilkins 2017; 1147–56. doi: 10.1249/MSS.0000000000001204.
  14. Asadi M, Rahmani M, Samadi A, Kalantari Hesari A. Acetylsalicylic acidā€induced alterations in male reproductive parameters in Wistar rats and the effect of sprint interval training. Andrologia 2022.;54(3):e14339. doi: 10.1111/and.14339.
  15. Burgomaster KA, Hughes SC, Heigenhauser GJF, Bradwell SN, Gibala MJ. Six sessions of sprint interval training increases muscle oxidative potential and cycle endurance capacity in humans. Journal of Applied Physiology 2005.;98(6):1985–90. doi: 10.1152/japplphysiol.01095.2004.
  16. Gillen JB, Percival ME, Skelly LE, Martin BJ, Tan RB, Tarnopolsky MA. Three Minutes of All-Out Intermittent Exercise per Week Increases Skeletal Muscle Oxidative Capacity and Improves Cardiometabolic Health. Hayashi N, urednik. PLoS One 2014.;9(11):e111489. doi: 10.1371/journal.pone.0111489.
  17. Townsend LK, Islam H, Dunn E, Eys M, Robertson-Wilson J, Hazell TJ. Modified sprint interval training protocols. Part II. Psychological responses. Applied Physiology, Nutrition, and Metabolism 2017.;42(4):347–53. doi: 10.1139/apnm-2016-0479.
  18. Abbasi B, Samadi A, Bazgir B. The combined effect of high-intensity interval training and intermittent fasting on lipid profile and peroxidation in Wistar rats under high-fat diet. Sport Sci Health 2020.;16(4):645–52. doi: 10.1007/s11332-020-00637-3.
  19. Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V. Method for the measurement of antioxidant activity in human fluids. Journal of Clinical Pathology 2001.;54(5):356–61. doi: 10.1136/JCP.54.5.356.
  20. McCord JM, Fridovich I. Superoxide Dismutase. Journal of Biological Chemistry 1969.;244(22):6049–55. doi: 10.1016/S0021-9258(18)63504-5.
  21. Ahmadvand H, Dehnoo MG, Cheraghi R, Rasoulian B, Ezatpour B, Azadpour M. Amelioration of altered serum, liver, and kidney antioxidant enzymes activities by sodium selenite in alloxan-induced diabetic rats. Reports of Biochemistry & Molecular Biology 2014.;3(1):14.
  22. Lowry O, Rosebrough N, Farr AL, Randall R. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 1951.;193(1):265–75. doi: 10.1016/S0021-9258(19)52451-6.
  23. Van de Vlekkert D, Machado E, D’Azzo A. Analysis of Generalized Fibrosis in Mouse Tissue Sections with Masson’s Trichrome Staining. Bio-protocol 2020.;10(10):e3629. doi: 10.21769/BioProtoc.3629.
  24. Odermatt A. The Western-style diet: a major risk factor for impaired kidney function and chronic kidney disease. American Journal of Physiology 2011.;301(5):F919–31. doi: 10.1152/ajprenal.00068.2011.
  25. Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, Morio B. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. Journal of Clinical Investigation 2008.;118(2):789–800. doi: 10.1172/JCI32601.
  26. Noeman SA, Hamooda HE, Baalash AA. Biochemical Study of Oxidative Stress Markers in the Liver, Kidney and Heart of High Fat Diet Induced Obesity in Rats. Diabetology & Metabolic Syndrome 2011.;3(1):17. doi: 10.1186/1758-5996-3-17.
  27. Uetake Y, Ikeda H, Irie R, Tejima K, Matsui H, Ogura S, et al. High-salt in addition to high-fat diet may enhance inflammation and fibrosis in liver steatosis induced by oxidative stress and dyslipidemia in mice. Lipids in Health and Disease 2015.;14(1):6. doi: 10.1186/s12944-015-0002-9.
  28. Sanchez-Valle V, C. Chavez-Tapia N, Uribe M, Mendez-Sanchez N. Role of Oxidative Stress and Molecular Changes in Liver Fibrosis: A Review. Current Medicinal Chemistry 2012.;19(28):4850–4860. doi: 10.2174/092986712803341520.
  29. Pereira B, Costa Rosa LFB, Safi DA, Medeiros MHG, Curi R, Bechara EJH. Superoxide dismutase, catalase, and glutathione peroxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiology & Behavior 1994.;56(5):1095–1099. doi: 10.1016/0031-9384(94)90349-2.
  30. Feriani DJ, Sousa AS, Delbin MA, Ruberti OM, Crestani CC, Rodrigues B. Spleen tissue changes after restraint stress: effects of aerobic exercise training. Stress 2021.;24(5):572–583. doi: :10.1080/10253890.2021.1895112.
  31. Senna SM, Torres MK, Lopes DAP, Alheiros-Lira MC, de Moura DB, Pereira VRA. Moderate physical training attenuates perinatal low-protein-induced spleen lymphocyte apoptosis in endotoxemic adult offspring rats. European Journal of Nutrition 2016.;55(3):1113–1122. doi: 10.1007/S00394-015-0925-Y.
  1. Biswas SK. Does the Interdependence between Oxidative Stress and Inflammation Explain the Antioxidant Paradox? Oxidative Medicine and Cellular Longevity 2016; 1–9. doi: 10.1155/2016/5698931.
  2. Kvernmo H, Olsen JO, Østerud B. Changes in blood cell response following strenuous physical exercise. European Journal of Applied Physiology and Occupational Physiology 1992.;64(4):318–22. doi: 10.1136/bjsm.34.4.246.
  3. El-Tahawy N, Ali AH. Swimming Exercise Ameliorates the Chronic Immobilization Stress-Induced Alterations in Spleen and Splenic T-cell Population in Adult Male Albino Rats: Histological and Immunohistochemical Study. Egyptian Journal of Histology 2021.;44(1):83–95. doi: 10.21608/EJH.2020.24673.1253.
  4. Stewart IB, Warburton DER, Hodges ANH, Lyster DM, McKenzie DC. Cardiovascular and splenic responses to exercise in humans. Journal of Applied Physiology ;94(4):1619–26. doi: 10.1152/japplphysiol.00040.2002.
  5. Vargas-Mendoza N, Morales-González Á, Madrigal-Santillán EO, Madrigal-Bujaidar E, Álvarez-González I, García-Melo LF. Antioxidant and adaptative response mediated by Nrf2 during physical exercise. Antioxidants 2019.;8(6):196. doi: 10.3390/antiox8060196.
  6. Carratelli C. The effect of dietary lipid manipulation on murine splenic lymphocytes apoptosis and heat shock protein over expression. FEMS Immunology and Medical Microbiology 1999.;24(1):19–25. doi: 10.1016/S0928-8244(99)00002-4.
  7. Zeng X, Li Y, Lv W, Dong X, Zeng Ch, Zeng L, et al. A High-Salt Diet Disturbs the Development and Function of Natural Killer Cells in Mice. Journal of Immunology Research 2020.;6687143. doi: 10.1155/2020/6687143.
  8. Cui J, Xiao Y, Shi YH, Wang B, Le GW. Lipoic acid attenuates high-fat-diet–induced oxidative stress and B-cell–related immune depression. Nutrition 2012.;28(3):275–80. doi: 10.1016/j.nut.2011.10.016.