The Effect of Royal Jelly and Endurance Exercise on Cognitive Function and Pathological Changes of Hippocampus Tissue in Rats with Experimental Autoimmune Encephalomyelitis

Document Type : Research Paper

Authors

Department of Exercise Physiology, Central Tehran Branch, Islamic Azad University, Tehran, Iran.

Abstract

Introduction: Although the positive effects of physical trainings as well as nutrition on cognitive function are reported. But there is limited information regarding their combined effect. Present study aimed to review the effect of royal jelly (RJ) and endurance exercise (EE) on cognitive function and pathological changes of hippocampus tissue in rats with experimental autoimmune encephalomyelitis (EAE). Methods: Forty- nine Sprague- Dawley female EAE rats selected as sample and assigned in 1) EE+RJ100, 2) EE+RJ50, 3) EE, 4) RJ100, 5) RJ50, 6) Sham (Sh), and 7) EAE groups also 7 healthy rats assigned in healthy control group (HC). Rats in EE groups trained 4 sessions per week (30 minutes with speed of 11-15 m/min) for five weeks and RJ was injected intra- peritoneal. One-way ANOVA along with Tukey's post hoc was used for data analysis (P≤0.05). Results: The percentage of healthy cells in the C1 region (PHC), avoidance (AM) and spatial memory (SM) levels in the EE group were more favorable than the EAE group (P≤0.05). Also, the PHC in the C3 and C1 regions, the AM and SM values in the RJ50 and RJ100 groups were higher than the EAE group (P≤0.05). As well as the PHC in C1 and C3 regions, AM and SM levels in the EE+RJ50 and EE+RJ100 groups were significantly more favorable than the EAE group (P≤0.05). The effects of EE+RJ50 and EE+RJ100 on improving SM and some subsections of AM were more favorable than the effects of RJ100 (P≤0.05). Conclusion: Although EE and RJ (50 and 100mg/kg) alone and their interactive effects have favorable effects on improving memory and neurogenesis.

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  1. Tacchino A, Podda J, Bergamaschi V, Pedullà L, Brichetto G. Cognitive rehabilitation in multiple sclerosis: Three digital ingredients to address current and future priorities. Front Hum Neurosci. 2023;17:1130231.
  2. Hafedh M, Parnow A. Exercise training improves memory and produces changes in the adrenal gland morphology in the experimental autoimmune encephalomyelitis. Endocr Regul. 2022;56(1):31–7.
  3. Jamoussi H, Ali N Ben, Missaoui Y, Cherif A, Oudia N, Anane N, et al. Cognitive impairment in multiple sclerosis: Utility of electroencephalography. Mult Scler Relat Disord. 2023;70:104502.
  4. Theodosis-Nobelos P, Rekka EA. The Multiple Sclerosis Modulatory Potential of Natural Multi-Targeting Antioxidants. Molecules. 2022;27(23):8402.
  5. Charabati M, Wheeler MA, Weiner HL, Quintana FJ. Multiple sclerosis: Neuroimmune crosstalk and therapeutic targeting. Cell. 2023;186(7):1309–27.
  6. Yazdanfar SK, Edalatmanesh MA, Hosseini SE. The Effect of Gallic Acid on Passive Avoidance Memory, Working Memory, and Dark Neuron Cell Density in CA1/CA3 Areas in Rats Hippocampal Degeneration Model. J Anim Biol. 2022;14(4):263–74.
  7. Sheikholeslami-Vatani D, Salehi OR, Hosseini SA. Psycho-physiological effects of high intensity interval training and vitamin E consumption in elderly trimethyltin-treated Alzheimer’s rats. Metab Exerc. 2021;11(2):57–76.
  8. Sandroff BM, Wylie GR, Baird JF, Jones CD, Diggs MD, Genova H, et al. Effects of walking exercise training on learning and memory and hippocampal neuroimaging outcomes in MS: A targeted, pilot randomized controlled trial. Contemp Clin Trials. 2021;110:106563.
  9. Parnow A, Hafedh M, Tsunoda I, Patel DI, Baker JS, Saeidi A, et al. Effectiveness of exercise interventions in animal models of multiple sclerosis. Front Med. 2023;10.
  10. Riemenschneider M, Hvid LG, Petersen T, Stenager E, Dalgas U. Exercise Therapy in Early Multiple Sclerosis Improves Physical Function But Not Cognition: Secondary Analyses From a Randomized Controlled Trial. Neurorehabil Neural Repair. 2023;15459683231159660.
  11. Hosseini SA, Salehi OR, Farzanegi P, Farkhaie F, Darvishpour AR, Roozegar S. Interactive Effects of Endurance Training and Royal Jelly Consumption on Motor Balance and Pain Threshold in Animal Model of the Alzheimer Disease. Arch Neurosci. 7(2).
  12. Zamani Z, Reisi P, Alaei H, Pilehvarian AA, Zamani Z. Effect of Royal Jelly (RJ) on Learning and Memory in Rats after Intracerebroventricular Injection of Streptozotocin (icv-STZ). J Isfahan Med Sch. 2011;28(123).
  13. Kheirdeh M, Jahromi MK, Hemmatinafar M, Nemati J. Additive beneficial effects of aerobic training and royal jelly on hippocampal inflammation and function in experimental autoimmune encephalomyelitis rats. Mult Scler Relat Disord. 2023;70:104527.
  14. Molaei R, Vahidian-Rezazadeh M, Moghtaderi A. Effect of 6 weeks aerobic exercise and oral Royal Jelly consumption on inflammatory factors’ multiple sclerosis patients. Med J mashhad Univ Med Sci. 2019;62(3):1524–35.
  15. Kheirdeh M, Koushkie Jahromi M, Brühl AB, Brand S. The effect of exercise training and royal jelly on hippocampal cannabinoid-1-receptors and pain threshold in experimental autoimmune encephalomyelitis in rats as animal model of multiple sclerosis. Nutrients. 2022;14(19):4119.
  16. Lohrasbi M, Taghian F, Jalali Dehkordi K, Hosseini SA. The functional mechanisms of synchronizing royal jelly consumption and physical activity on rat with multiple sclerosis-like behaviors hallmarks based on bioinformatics analysis, and experimental survey. BMC Neurosci. 2022;23(1):1–18.
  17. Jalali Dehkordi K, Hosseini SA. The Effect of Aerobic Training with Royal Jelly Consumption on Health Related Anthropometric Markers in an Experimental Autoimmune Encephalomyelitis Model. Jorjani Biomed J. 2021;9(4):1–12.
  18. Sellitto C, Corbi G, Stefanelli B, Manzo V, Trucillo M, Charlier B, et al. Antioxidant Supplementation Hinders the Role of Exercise Training as a Natural Activator of SIRT1. Nutrients. 2022;14(10):2092.
  19. Weissert R. Actively induced experimental autoimmune encephalomyelitis in rats. Mult Scler Methods Protoc. 2016;161–9.
  20. Kalkowski L, Golubczyk D, Kwiatkowska J, Domzalska M, Walczak P, Malysz-Cymborska I. Local autoimmune encephalomyelitis model in a rat brain with precise control over lesion placement. PLoS One. 2022;17(1):e0262677.
  21. Malekinejad H, Ahsan S, Delkhosh-Kasmaie F, Cheraghi H, Rezaei-Golmisheh A, Janbaz-Acyabar H. Cardioprotective effect of royal jelly on paclitaxel-induced cardio-toxicity in rats. Iran J Basic Med Sci. 2016;19(2):221.
  22. Tajiri N, Yasuhara T, Shingo T, Kondo A, Yuan W, Kadota T, et al. Exercise exerts neuroprotective effects on Parkinson’s disease model of rats. Brain Res. 2010;1310:200–7.
  23. Bernardes D, Oliveira ALR de. Regular exercise modifies histopathological outcomes of pharmacological treatment in experimental autoimmune encephalomyelitis. Front Neurol. 2018;9:950.
  24. Bozorgi A, AliHosseini S, Rasoli MH. Effect of Voluntary and Forced Training with Royal Jelly Consumption on Learning and Spatial Memory of Rat Model of Alzheimer’s Disease. Jundishapur J Chronic Dis Care. 9(1).
  25. Hosseini SA, Salehi O, Keikhosravi F, Hassanpour G, Ardakani HD, Farkhaie F, et al. Mental health benefits of exercise and genistein in elderly rats. Exp Aging Res. 2022;48(1):42–57.
  26. Schiffmann D, Lampkemeyer V, Lindner M, Fleck A-K, Koch K, Eschborn M, et al. Endurance Exercise Attenuates Established Progressive Experimental Autoimmune Encephalomyelitis and Is Associated with an Amelioration of Innate Immune Responses in NOD Mice. Int J Mol Sci. 2023;24(21):15798.
  27. Seydyousefi M, Fallahmohammadi Z, Moazzami M, Yaghoubi A, Faghfoori Z. Impact of early endurance training on improvement of brain damage in CA1 region of Hippocampus and expression of A2A protein following ischemic stroke in rats. J Isfahan Med Sch. 2019;37(526):485–92.
  28. Shamsaei N, Abdi H, Shamsi M. The Effect of a continuous training on necrosis and apoptosis changes in the hippocampus of diabetic rats. J Ilam Univ Med Sci. 2017;25(1):1–11.
  29. Yaghoubi M, Kordi M, Gaeini A. The Effect of Forced and Voluntary Exercise before Induction of Experimental Autoimmune Encephalomyelitis on the Integrity of the Blood-Brain Barrier and Gene Expression of Some of Tight Junction Proteins. J Appl Exerc Physiol. 2020;16(32):87–101.
  30. Ibrahim DS, Shahen EMS. Effect of royal jelly on acrylamide-induced neurotoxicity in rats. J Chem Neuroanat. 2023;134:102358.
  31. e Silva TG de S, da Silva JRM, da Silva Alves A, Britto LRG, Xavier GF, Sandoval MRL. Oral treatment with royal jelly improves memory and presents neuroprotective effects on icv-STZ rat model of sporadic Alzheimer’s disease. Heliyon. 2020;6(2).
  32. Hashemi P, Moloudi MR, Vahabzadeh Z, Izadpanah E. Anticonvulsant Effects of Royal Jelly in Kainic Acid-Induced Animal Model of Temporal Lobe Epilepsy Through Antioxidant Activity. Neurochem Res. 2023;48(7):2187–95.
  33. Raoufi S, Salavati Z, Komaki A, Shahidi S, Zarei M. Royal jelly improves learning and memory deficits in an amyloid β-induced model of Alzheimer’s disease in male rats: Involvement of oxidative stress. Metab Brain Dis. 2023;38(4):1239–48.