Sport Biosciences

The Effect of Eight Weeks of Aerobic Training and Royal Jelly on Oxidative Stress and Liver Tissue Enzymes in Obese Rats

Document Type : Research Paper

Authors

Ali Asghar Magholi 1
Ahmad Abdi 2
Asieh Abbasi daloii 1

1 Department of Exercise Physiology, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran.

2 Corresponding Author, Department of Exercise Physiology, Ayatollah Amoli Branch, Islamic Azad University, Amol, Iran.

https://doi.org/10.22059/jsb.2022.332096.1491
Abstract
Introduction: Oxidative stress is associated with a variety of inflammatory and metabolic diseases, including obesity. This study aimed to investigate the effect of eight weeks of aerobic training and Royal Jelly on oxidative stress and liver tissue enzymes of obese rats.
Methods: In this experimental study, 45 male Wistar rats (mean weight= 187.5±9.37 grams) were divided into 5 groups: Normal Diet (ND), High-Fat Diet (HFD), High-Fat Diet + Training (HFDT), High-Fat Diet + Royal Jelly (HFDRJ) and High-Fat Diet + Training + Royal Jelly (HFDTRJ). The supplement groups orally received 100 mg of royal jelly (per kg of body weight) diluted in distilled water during the intervention period. An aerobic training program including running on a treadmill with an intensity of 50-60% of oxygen consumption (VO2max), was performed Five days a week for eight weeks. Data were analyzed using a one-way analysis of variance and Tukey’s post hoc test at a significance level of α=0.05. Results: There was a significant increase in malondialdehyde (MDA) and a significant decrease in Superoxide Dismutase (SOD), Glutathione Peroxidase (GPX), and Catalase (CAT) in HFD group compared with ND group (P=0.001). Also, a significant decrease in MDA values and a significant increase in amounts of SOD, GPX, and CAT was observed in HFDT, HFDRJ, and HFDTRJ groups compared with the HFD group; and in the HFDTRJ group compared with HFDT and HFDRJ groups (P=0.001).  
Conclusion: It seems that the intervention of aerobic training and royal jelly can help to reduce oxidative stress and improve liver enzymes during obesity.

Highlights


    1. Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15(5):288-98. https://doi.org/10.1038/s41574-019-0176-8.
    2. Garg S, Maurer H, Reed K, Selagamsetty R. Diabetes and cancer: two diseases with obesity as a common risk factor. Diabetes Obes Metab. 2014;16(2):97-110. https://doi.org/10.1111/dom.12124.
    3. Sonta T, Inoguchi T, Tsubouchi H, Sekiguchi N, Kobayashi K, Matsumoto S, et al. Evidence for contribution of vascular NAD (P) H oxidase to increased oxidative stress in animal models of diabetes and obesity. Free Radic Biol Med. 2004;37(1):115-23. https://doi.org/10.1016/j.freeradbiomed.2004.04.001.
    4. Vincent HK, Taylor AG. Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes. 2006;30(3):400-18. https://doi.org/10.1038/sj.ijo.0803177.
    5. Pi‐Sunyer FX. The obesity epidemic: pathophysiology and consequences of obesity. Obes Res. 2002;10(S12):97S-104S. https://doi.org/10.1038/oby.2002.202.
    6. Valdecantos P, Matute P, Martínez A: Obesity and oxidative: role of antioxidants supplementation. Rev Invest Clin. 2009, 61(2): 127-127.
    7. Mishra KP. Cell membrane oxidative damage induced by gamma-radiation and apoptotic sensitivity. J Environ Pathol Toxicol Oncol. 2004;23(1) 23: 61-66. https://doi.org/10.1615/jenvpathtoxoncol.v23.i1.60.
    8. Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. 2003;91(2):179-94. https://doi.org/10.1093/aob/mcf118.
    9. Uzun H, Konukoglu D, Gelisgen R, Zengin K, Taskin M. Plasma protein carbonyl and thiol stress before and after laparoscopic gastric banding in morbidly obese patients. Obes Surg. 2007;17(10):1367-73. https://doi.org/10.1007/s11695-007-9242-8.
    10. Taubes G. The science of obesity: what do we really know about what makes us fat? An essay by Gary Taubes. BMJ. 2013;346. https://doi.org/10.1136/bmj.f1050.
    11. Soliman N, Asalah A, Moursi S, Gamal S, Eldeen M. Effect of Exercise Training on Metabolic Homeostasis and Some Hemodynamics (Some Hepatic and Cardiovascular Functions) in Experimentally Induced Obesity. J Obes Weight Loss Ther. 2018;8:2-13. https://doi.org/10.4172/2165-7904.1000368.
    12. Heydarnia E, Taghian F, Dehkodi KJ, Moghadasi M. Effects of Eight Weeks of Combined Training with Antioxidant Vitamins E and C on Glutathione, Glutathione Peroxidase, and Superoxide Dismutase in the Heart Tissue of Streptozotocin-induced Diabetic Rats. Gene, Cell Tissue. 2021;8(3) e111277. https://doi.org/10.5812/gct.111277.
    13. Shahin jahromy S, abbassi daloii A, barari A, Saeidi A. The effect of aerobic training with two types of normal and high cholesterol diet on antioxidant and cardiac oxidative stress in male rats. J Jiroft Univ Med Sci. 2020;7(1):285-91. http://journal.jmu.ac.ir/article-1-347-en.html.
    14. Zacarias AC, Barbosa MA, Guerra-Sá R, De Castro UGM, Bezerra FS, de Lima WG, et al. Swimming training induces liver adaptations to oxidative stress and insulin sensitivity in rats submitted to high-fat diet. Redox Rep. 2017;22(6):515-23. https://doi.org/10.1080/13510002.2017.1315513.
    15. Cao J, Xiao G, Chen X. Effects of Exercises of Different Intensity on Oxidative Stress and Adiponectin/Adiponectin Receptors of Livers in Obese Rats. Chinese J Sports Med. 2017:779-87. https://pesquisa.bvsalud.org/portal/resource/pt/wpr-666680.
    16. Oh S, Tanaka K, Warabi E, Shoda J. Exercise reduces inflammation and oxidative stress in obesity-related liver diseases. Med Sci Sports Exerc. 2013;45(12):2214-22. https://doi.org/10.1249/MSS.0b013e31829afc33.
    17. Groussard C, Maillard F, Vazeille E, Barnich N, Sirvent P, Otero YF, et al. Tissue-specific oxidative stress modulation by exercise: A comparison between MICT and HIIT in an obese rat model. Oxid Med Cell Longev. 2019; 2019:1965364. https://doi.org/10.1155/2019/1965364.
    18. Azimpour M, Fathi M, Dezfoulian O. Effect of eight weeks of forced physical activity with royal jelly consumption on depression and anxiety levels and antioxidant capacity in trimethyltin-induced Alzheimer's rats. J Appl Exe Phy. 2021;17(33):1-2. (In Persian). https://doi.org/10.22080/JAEP.2020.19373.1962.
    19. Anbara H, Shahrooz R, Malekinejad H, Saadati S. Investigating the Antioxidant Properties of Royal Jelly and Vitamin C on Enzymes, Histomorphometric and Liver Cells Apoptosis in Mice Suffering Hemolytic Anemia. J Fasa Uni Med Sci. 2016;6(2):178-87. (In Persian). https://journal.fums.ac.ir/article-1-929-en.html.
    20. Najafi G, Nejati V, Shalizar Jalali A, Zahmatkesh E. Protective role of royal jelly in oxymetholone-induced oxidative injury in mouse testis. Iran J Toxic. 2014;8(25):1073-80.( In Persian). http://ijt.arakmu.ac.ir/article-1-326-en.html.
    21. Zamani Z, Reisi P, Alaei H, Pilehvarian AA. Effect of Royal Jelly on spatial learning and memory in rat model of streptozotocin-induced sporadic Alzheimer's disease. Adv Biomed ReS. 2012; 1(26):1-6. https://doi.org/10.4103/2277-9175.98150.
    22. Mesri Alamdari N, Irandoost P, Roshanravan N, Vafa M, Asghari Jafarabadi M, Alipour S, et al. Effects of Royal Jelly and Tocotrienol Rich Fraction in obesity treatment of calorie-restricted obese rats: a focus on white fat browning properties and thermogenic capacity. Nutr Metab (Lond). 2020;17(1):1-13. https://doi.org/10.1186/s12986-020-00458-8.
    23. Rocha-Rodrigues S, Rodríguez A, Gouveia AM, Gonçalves IO, Becerril S, Ramírez B, et al. Effects of physical exercise on myokines expression and brown adipose-like phenotype modulation in rats fed a high-fat diet. Life sci. 2016;165(15):100-8. https://doi.org/10.1016/j.lfs.2016.09.023.
    24. Huang T-W, Chang C-L, Kao E-S, Lin J-H. Effect of Hibiscus sabdariffa extract on high fat diet–induced obesity and liver damage in hamsters. Food Nutr Res. 2015;59(1):29018. https://doi.org/ 10.3402/fnr.v59.29018.
    25. Brea A, Puzo J. Non-alcoholic fatty liver disease and cardiovascular risk. Int J Cardiol. 2013;167(4):1109-17. https://doi.org/10.1016/j.ijcard.2012.09.085.
    26. Ebrahimi-Mamghani M, Arefhosseini S. Comparison of low-calorie diet with and without sibutramine on body weight and liver function of patients with non-alcoholic fatty liver disease. Armaghane danesh. 2011;16(2):101-10. (In Persian). http://armaghanj.yums.ac.ir/article-1-378-en.html.
    27. Radák Z, Sasvári M, Nyakas C, Taylor AW, Ohno H, Nakamoto H, et al. Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys. 2000;383(1):114-8. https://doi.org/10.1006/abbi.2000.2042.
    28. Hoffman-Goetz L, Spagnuolo P. Effect of repeated exercise stress on caspase 3, Bcl-2, HSP 70 and CuZn-SOD protein expression in mouse intestinal lymphocytes. J 2007;187(1-2):94-101. https://doi.org/10.1016/j.jneuroim.2007.04.012.
    29. Yavari A, Javadi M, Mirmiran P, Bahadoran Z. Exercise-induced oxidative stress and dietary antioxidants. Asian J Sports Med. 2015;6(1):e24898. https://doi.org/10.5812/asjsm.24898.
    30. Muthusamy VR, Kannan S, Sadhaasivam K, Gounder SS, Davidson CJ, Boeheme C, et al. Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium. Free Radic Biol Med. 2012;52(2):366-76. https://doi.org/10.1016/j.freeradbiomed.2011.10.440.
    31. Derbre F, Ferrando B, Gomez-Cabrera MC, Sanchis-Gomar F, Martinez-Bello VE, Olaso-Gonzalez G, et al. Inhibition of xanthine oxidase by allopurinol prevents skeletal muscle atrophy: role of p38 MAPKinase and E3 ubiquitin ligases. PLoS One, 2012;7(10):e46668. https://doi.org/10.1371/journal.pone.0046668.
    32. El-Nekeety AA, El-Kholy W, Abbas NF, Ebaid A, Amra HA, Abdel-Wahhab MA. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon. 2007;50(2):256-69. https://doi.org/10.1016/j.toxicon.2007.03.017.
    33. Taghizadeh S, Nejati V, Najafi G. Protective effect of oral administration of royal jelly on liver damage induced by chronic immobilization stress in adult male mice. J Mazandaran Uni Med Sci. 2014;24(119):122-31. (in Persian). http://jmums.mazums.ac.ir/article-1-4694-en.html.
    34. Kanbur M, Eraslan G, Beyaz L, Silici S, Liman BC, Altınordulu Ş, et al. The effects of royal jelly on liver damage induced by paracetamol in mice. Exp Toxicol Pathol. 2009;61(2):123-32. https://doi.org/10.1016/j.etp.2008.06.003.
    35. Karadeniz A, Simsek N, Karakus E, Yildirim S, Kara A, Can I, et al. Royal jelly modulates oxidative stress and apoptosis in liver and kidneys of rats treated with cisplatin. Oxid Med Cell Longev. 2011;2011:981793. https://doi.org/10.1155/2011/981793.
    36. Kamakura M. Signal transduction mechanism leading to enhanced proliferation of primary cultured adult rat hepatocytes treated with royal jelly 57-kDa protein. j biochem. 2002;132(6):911-9. https://doi.org/ 10.1093/oxfordjournals.jbchem.a003304.
    37. Nagai T, Inoue R. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food chemi. 2004;84(2):181-6. https://doi.org/10.1016/S0308-8146(03)00198-5.
    38. Silici S, Ekmekcioglu O, Kanbur M, Deniz K. The protective effect of royal jelly against cisplatin-induced renal oxidative stress in rats. World J Urol. 2011;29(1):127-32. https://doi.org/10.1007/s00345-010-0543-5.
    39. Viuda‐Martos M, Ruiz‐Navajas Y, Fernández‐López J, Pérez‐Álvarez J. Functional properties of honey, propolis, and royal jelly. J food sci. 2008;73(9):R117-R24. https://doi.org/10.1111/j.1750-3841.2008.00966.x.
    40. Testa R, Bonfigli AR, Genovese S, De Nigris V, Ceriello A. The possible role of flavonoids in the prevention of diabetic complications. Nutrients. 2016;8(5):310. https://doi.org/10.3390/nu8050310.
    41. Guo H, Kouzuma Y, Yonekura M. Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chemi. 2009;113(1):238-45. https://doi.org/10.1016/j.foodchem.2008.06.081.

    42.Soleimani P, Shemshaki A, Hedayati M, Astinchap A. Effect of two-week exercise and supplementation of royal jelly on total antioxidant capacity of plasma and superoxide dismutase in obese male rats. J applied heal stu sport phy. 2018;5(1):77-82.( in Persian). https://doi.org/10.22049/JASSP.2019.26365.1188.

Keywords

Aerobic exercise
Oxidant and antioxidant
Liver tissue
Obesity
Subjects
  1. Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019;15(5):288-98. https://doi.org/10.1038/s41574-019-0176-8.
  2. Garg S, Maurer H, Reed K, Selagamsetty R. Diabetes and cancer: two diseases with obesity as a common risk factor. Diabetes Obes Metab. 2014;16(2):97-110. https://doi.org/10.1111/dom.12124.
  3. Sonta T, Inoguchi T, Tsubouchi H, Sekiguchi N, Kobayashi K, Matsumoto S, et al. Evidence for contribution of vascular NAD (P) H oxidase to increased oxidative stress in animal models of diabetes and obesity. Free Radic Biol Med. 2004;37(1):115-23. https://doi.org/10.1016/j.freeradbiomed.2004.04.001.
  4. Vincent HK, Taylor AG. Biomarkers and potential mechanisms of obesity-induced oxidant stress in humans. Int J Obes. 2006;30(3):400-18. https://doi.org/10.1038/sj.ijo.0803177.
  5. Pi‐Sunyer FX. The obesity epidemic: pathophysiology and consequences of obesity. Obes Res. 2002;10(S12):97S-104S. https://doi.org/10.1038/oby.2002.202.
  6. Valdecantos P, Matute P, Martínez A: Obesity and oxidative: role of antioxidants supplementation. Rev Invest Clin. 2009, 61(2): 127-127.
  7. Mishra KP. Cell membrane oxidative damage induced by gamma-radiation and apoptotic sensitivity. J Environ Pathol Toxicol Oncol. 2004;23(1) 23: 61-66. https://doi.org/10.1615/jenvpathtoxoncol.v23.i1.60.
  8. Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot. 2003;91(2):179-94. https://doi.org/10.1093/aob/mcf118.
  9. Uzun H, Konukoglu D, Gelisgen R, Zengin K, Taskin M. Plasma protein carbonyl and thiol stress before and after laparoscopic gastric banding in morbidly obese patients. Obes Surg. 2007;17(10):1367-73. https://doi.org/10.1007/s11695-007-9242-8.
  10. Taubes G. The science of obesity: what do we really know about what makes us fat? An essay by Gary Taubes. BMJ. 2013;346. https://doi.org/10.1136/bmj.f1050.
  11. Soliman N, Asalah A, Moursi S, Gamal S, Eldeen M. Effect of Exercise Training on Metabolic Homeostasis and Some Hemodynamics (Some Hepatic and Cardiovascular Functions) in Experimentally Induced Obesity. J Obes Weight Loss Ther. 2018;8:2-13. https://doi.org/10.4172/2165-7904.1000368.
  12. Heydarnia E, Taghian F, Dehkodi KJ, Moghadasi M. Effects of Eight Weeks of Combined Training with Antioxidant Vitamins E and C on Glutathione, Glutathione Peroxidase, and Superoxide Dismutase in the Heart Tissue of Streptozotocin-induced Diabetic Rats. Gene, Cell Tissue. 2021;8(3) e111277. https://doi.org/10.5812/gct.111277.
  13. Shahin jahromy S, abbassi daloii A, barari A, Saeidi A. The effect of aerobic training with two types of normal and high cholesterol diet on antioxidant and cardiac oxidative stress in male rats. J Jiroft Univ Med Sci. 2020;7(1):285-91. http://journal.jmu.ac.ir/article-1-347-en.html.
  14. Zacarias AC, Barbosa MA, Guerra-Sá R, De Castro UGM, Bezerra FS, de Lima WG, et al. Swimming training induces liver adaptations to oxidative stress and insulin sensitivity in rats submitted to high-fat diet. Redox Rep. 2017;22(6):515-23. https://doi.org/10.1080/13510002.2017.1315513.
  15. Cao J, Xiao G, Chen X. Effects of Exercises of Different Intensity on Oxidative Stress and Adiponectin/Adiponectin Receptors of Livers in Obese Rats. Chinese J Sports Med. 2017:779-87. https://pesquisa.bvsalud.org/portal/resource/pt/wpr-666680.
  16. Oh S, Tanaka K, Warabi E, Shoda J. Exercise reduces inflammation and oxidative stress in obesity-related liver diseases. Med Sci Sports Exerc. 2013;45(12):2214-22. https://doi.org/10.1249/MSS.0b013e31829afc33.
  17. Groussard C, Maillard F, Vazeille E, Barnich N, Sirvent P, Otero YF, et al. Tissue-specific oxidative stress modulation by exercise: A comparison between MICT and HIIT in an obese rat model. Oxid Med Cell Longev. 2019; 2019:1965364. https://doi.org/10.1155/2019/1965364.
  18. Azimpour M, Fathi M, Dezfoulian O. Effect of eight weeks of forced physical activity with royal jelly consumption on depression and anxiety levels and antioxidant capacity in trimethyltin-induced Alzheimer's rats. J Appl Exe Phy. 2021;17(33):1-2. (In Persian). https://doi.org/10.22080/JAEP.2020.19373.1962.
  19. Anbara H, Shahrooz R, Malekinejad H, Saadati S. Investigating the Antioxidant Properties of Royal Jelly and Vitamin C on Enzymes, Histomorphometric and Liver Cells Apoptosis in Mice Suffering Hemolytic Anemia. J Fasa Uni Med Sci. 2016;6(2):178-87. (In Persian). https://journal.fums.ac.ir/article-1-929-en.html.
  20. Najafi G, Nejati V, Shalizar Jalali A, Zahmatkesh E. Protective role of royal jelly in oxymetholone-induced oxidative injury in mouse testis. Iran J Toxic. 2014;8(25):1073-80.( In Persian). http://ijt.arakmu.ac.ir/article-1-326-en.html.
  21. Zamani Z, Reisi P, Alaei H, Pilehvarian AA. Effect of Royal Jelly on spatial learning and memory in rat model of streptozotocin-induced sporadic Alzheimer's disease. Adv Biomed ReS. 2012; 1(26):1-6. https://doi.org/10.4103/2277-9175.98150.
  22. Mesri Alamdari N, Irandoost P, Roshanravan N, Vafa M, Asghari Jafarabadi M, Alipour S, et al. Effects of Royal Jelly and Tocotrienol Rich Fraction in obesity treatment of calorie-restricted obese rats: a focus on white fat browning properties and thermogenic capacity. Nutr Metab (Lond). 2020;17(1):1-13. https://doi.org/10.1186/s12986-020-00458-8.
  23. Rocha-Rodrigues S, Rodríguez A, Gouveia AM, Gonçalves IO, Becerril S, Ramírez B, et al. Effects of physical exercise on myokines expression and brown adipose-like phenotype modulation in rats fed a high-fat diet. Life sci. 2016;165(15):100-8. https://doi.org/10.1016/j.lfs.2016.09.023.
  24. Huang T-W, Chang C-L, Kao E-S, Lin J-H. Effect of Hibiscus sabdariffa extract on high fat diet–induced obesity and liver damage in hamsters. Food Nutr Res. 2015;59(1):29018. https://doi.org/ 10.3402/fnr.v59.29018.
  25. Brea A, Puzo J. Non-alcoholic fatty liver disease and cardiovascular risk. Int J Cardiol. 2013;167(4):1109-17. https://doi.org/10.1016/j.ijcard.2012.09.085.
  26. Ebrahimi-Mamghani M, Arefhosseini S. Comparison of low-calorie diet with and without sibutramine on body weight and liver function of patients with non-alcoholic fatty liver disease. Armaghane danesh. 2011;16(2):101-10. (In Persian). http://armaghanj.yums.ac.ir/article-1-378-en.html.
  27. Radák Z, Sasvári M, Nyakas C, Taylor AW, Ohno H, Nakamoto H, et al. Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle. Arch Biochem Biophys. 2000;383(1):114-8. https://doi.org/10.1006/abbi.2000.2042.
  28. Hoffman-Goetz L, Spagnuolo P. Effect of repeated exercise stress on caspase 3, Bcl-2, HSP 70 and CuZn-SOD protein expression in mouse intestinal lymphocytes. J 2007;187(1-2):94-101. https://doi.org/10.1016/j.jneuroim.2007.04.012.
  29. Yavari A, Javadi M, Mirmiran P, Bahadoran Z. Exercise-induced oxidative stress and dietary antioxidants. Asian J Sports Med. 2015;6(1):e24898. https://doi.org/10.5812/asjsm.24898.
  30. Muthusamy VR, Kannan S, Sadhaasivam K, Gounder SS, Davidson CJ, Boeheme C, et al. Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium. Free Radic Biol Med. 2012;52(2):366-76. https://doi.org/10.1016/j.freeradbiomed.2011.10.440.
  31. Derbre F, Ferrando B, Gomez-Cabrera MC, Sanchis-Gomar F, Martinez-Bello VE, Olaso-Gonzalez G, et al. Inhibition of xanthine oxidase by allopurinol prevents skeletal muscle atrophy: role of p38 MAPKinase and E3 ubiquitin ligases. PLoS One, 2012;7(10):e46668. https://doi.org/10.1371/journal.pone.0046668.
  32. El-Nekeety AA, El-Kholy W, Abbas NF, Ebaid A, Amra HA, Abdel-Wahhab MA. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon. 2007;50(2):256-69. https://doi.org/10.1016/j.toxicon.2007.03.017.
  33. Taghizadeh S, Nejati V, Najafi G. Protective effect of oral administration of royal jelly on liver damage induced by chronic immobilization stress in adult male mice. J Mazandaran Uni Med Sci. 2014;24(119):122-31. (in Persian). http://jmums.mazums.ac.ir/article-1-4694-en.html.
  34. Kanbur M, Eraslan G, Beyaz L, Silici S, Liman BC, Altınordulu Ş, et al. The effects of royal jelly on liver damage induced by paracetamol in mice. Exp Toxicol Pathol. 2009;61(2):123-32. https://doi.org/10.1016/j.etp.2008.06.003.
  35. Karadeniz A, Simsek N, Karakus E, Yildirim S, Kara A, Can I, et al. Royal jelly modulates oxidative stress and apoptosis in liver and kidneys of rats treated with cisplatin. Oxid Med Cell Longev. 2011;2011:981793. https://doi.org/10.1155/2011/981793.
  36. Kamakura M. Signal transduction mechanism leading to enhanced proliferation of primary cultured adult rat hepatocytes treated with royal jelly 57-kDa protein. j biochem. 2002;132(6):911-9. https://doi.org/ 10.1093/oxfordjournals.jbchem.a003304.
  37. Nagai T, Inoue R. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food chemi. 2004;84(2):181-6. https://doi.org/10.1016/S0308-8146(03)00198-5.
  38. Silici S, Ekmekcioglu O, Kanbur M, Deniz K. The protective effect of royal jelly against cisplatin-induced renal oxidative stress in rats. World J Urol. 2011;29(1):127-32. https://doi.org/10.1007/s00345-010-0543-5.
  39. Viuda‐Martos M, Ruiz‐Navajas Y, Fernández‐López J, Pérez‐Álvarez J. Functional properties of honey, propolis, and royal jelly. J food sci. 2008;73(9):R117-R24. https://doi.org/10.1111/j.1750-3841.2008.00966.x.
  40. Testa R, Bonfigli AR, Genovese S, De Nigris V, Ceriello A. The possible role of flavonoids in the prevention of diabetic complications. Nutrients. 2016;8(5):310. https://doi.org/10.3390/nu8050310.
  41. Guo H, Kouzuma Y, Yonekura M. Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chemi. 2009;113(1):238-45. https://doi.org/10.1016/j.foodchem.2008.06.081.

42.Soleimani P, Shemshaki A, Hedayati M, Astinchap A. Effect of two-week exercise and supplementation of royal jelly on total antioxidant capacity of plasma and superoxide dismutase in obese male rats. J applied heal stu sport phy. 2018;5(1):77-82.( in Persian). https://doi.org/10.22049/JASSP.2019.26365.1188.

Sport Biosciences
Volume 14, Issue 2
Summer 2022
Pages 29-42

  • Receive Date 10 October 2021
  • Revise Date 07 April 2022
  • Accept Date 09 April 2022

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