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

Document Type : Research Paper

Authors

1 Department of Physical Education and Sport Sciences, Faculty of Literature and Human Sciences, Lorestan University, Khoramabad, Iran

2 Department of Pathobiology, School of Veterinary Medicine, University of Khoramabad, Lorestan, Iran

10.22080/jaep.2020.19373.1962

Abstract

Background and Purpose: The aim of this study was to investigate the protective role of Royal Jelly as an antioxidant on behavioral disorders of depression and anxiety caused by trimethyltytin toxin and the level of superoxide dismutase and glutathione peroxidase enzymes in Alzheimer's rats treated with trimethyltin after eight weeks of forced swimming exercise.
Methodology: The present study was performed experimentally with 48 male rats; 40 of them were induced by Alzheimer's TMT. The rats were randomly divided into six groups: Healthy control, Alzheimer's control, Alzheimer- forced exercise, Alzheimer- sham, Alzheimer- forced exercise- royal jelly and Alzheimer's-Royal Jelly were divided. Forced Swimming Test (FST) for depression assessment and Elevated Plus-Maze (EPM) for anxiety assessment were used. The expression of SOD and GPX genes were evaluated by Real Time PCR technique. The 2-ΔΔCT formula was used to quantify the expression values of the target genes. Due to the abnormal distribution of some data, the non-parametric statistical method of Kruskal–Wallis was used by SPSS version 20.
Results: Significant differences in groups with dependent variables (p <0.05) showed that swimming training with Royal Jelly reduced depression and anxiety, and swimming training did not have a significant effect on SOD and GPX. But taking Royal Jelly alone increased the SOD and GPX index.
Conclusion: Trimethylthine administration induced depressive and anxiety-like behaviors in rats. This volume of forced swimming training protocol for Alzheimer's rats does not seem to have a positive effect on antioxidant parameters. However, the positive effect of royal jelly consumption on increasing SOD, GPX was observed, and the use of royal jelly with antioxidant properties and the combination of forced exercise with the use of royal jelly supplement has the ability to modulate mood in the current model, and can be used as a useful method.

Keywords


##Bhatti GK, Reddy AP, Reddy PH, Bhatti JS. Lifestyle modifications and nutritional interventions in aging-associated cognitive decline and Alzheimer’s disease. Frontiers in aging neuroscience. 2019;11.## Lopez C, Sanchez JL, Martin J. [Exploratory analysis of the influence of cognitive reserve on the benefits of cognitive stimulation therapy in patients with sporadic late-onset Alzheimer's disease]. Revista de neurologia. 2020;70(8):271-81.## Rao U, Chen L-A, Bidesi AS, Shad MU, Thomas MA, Hammen CL. Hippocampal changes associated with early-life adversity and vulnerability to depression. Biological psychiatry. 2010;67(4):357-64.## Petit-Demouliere B, Chenu F, Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology. 2005;177(3):245-55.## Franzoni F, Federighi G, Fusi J, Cerri E, Banducci R, Petrocchi A, et al. Physical exercise improves total antioxidant capacity and gene expression in rat hippocampal tissue. Archives Italiennes de Biologie. 2017;155(1/2):1-10.## Zhong H, Rong J, Zhu C, Liang M, Li Y, Zhou R. Epigenetic modifications of GABAergic interneurons contributes to the deficits in adult hippocampus neurogenesis and depression-like behavior in prenatally stressed mice. The international journal of neuropsychopharmacology. 2020.## Miki T, Eguchi M, Kochi T, Akter S, Hu H, Kashino I, et al. Prospective study on the association between dietary non-enzymatic antioxidant capacity and depressive symptoms. Clinical nutrition ESPEN. 2020;36:91-8.## Agar A, Kucukatay V, Yargicoglu P, Bilmen S, Gumuslu S, Yucel G. Effect of sulfur dioxide inhalation on erythrocyte antioxidant status and lipid peroxidation in experimental diabetes. Diabetes and Metabolism. 2000;26(2):140-4.## Guardia de Souza EST, do Val de Paulo MEF, da Silva JRM, da Silva Alves A, Britto LRG, Xavier GF, et al. 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):e03281.## Rahmani A, Gorzi A, Ghanbari M. The effects of high intensity interval training and strenuous resistance training on hippocampal antioxidant capacity and serum levels of malondialdehyde and total antioxidant capacity in male rats. 2018.## Zolfaghari F, Peeri M, Hosseini M-J. The effect of adolescent treadmill mandatory exercise on symptoms of depression and brain inflammatory responses following maternal separation stress in mature male rats. EBNESINA. 2018;19(4):4-12.##Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Archives of neurology. 2001;58(3):498-504.## e Silva TGdS, 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):e03281.## Verghese J, Lipton RB, Katz MJ, Hall CB, Derby CA, Kuslansky G, et al. Leisure activities and the risk of dementia in the elderly. New England Journal of Medicine. 2003;348(25):2508-16.##   Madden DJ, Blumenthal JA, Allen PA, Emery CF. Improving aerobic capacity in healthy older adults does not necessarily lead to improved cognitive performance. Psychology and aging. 1989;4(3):307.## Broe G, Creasey H, Jorm A, Bennett H, Casey B, Waite L, et al. Health habits and risk of cognitive impairment and dementia in old age: a prospective study on the effects of exercise, smoking and alcohol consumption. Australian and New Zealand journal of public health. 1998;22(5):621-3.## Cesur G, Atay E, Ogut S, Polat M, Ongel K. Effect of indoor climbing exercise on plasma oxidative stress, hematologic parameters and heart rate responses in sedentary individuals. 2012.## Nonato L, Rocha-Vieira E, Tossige-Gomes R, Soares A, Soares B, Freitas D, et al. Swimming training attenuates oxidative damage and increases enzymatic but not non-enzymatic antioxidant defenses in the rat brain. Brazilian Journal of Medical and Biological Research. 2016;49(10).## Nakhostin-Roohi B, Babaei P, Rahmani-Nia F, Bohlooli S. Effect of vitamin C supplementation on lipid peroxidation, muscle damage and inflammation after 30-min exercise at 75% VO^ sub 2max. Journal of sports medicine and physical fitness. 2008;48(2):217.##  Ogonovszky H, Sasvári M, Dosek A, Berkes I, Kaneko T, Tahara S, et al. The effects of moderate, strenuous, and overtraining on oxidative stress markers and DNA repair in rat liver. Canadian journal of applied physiology. 2005;30(2):186-95.## Yavari A, Javadi M, Mirmiran P, Bahadoran Z. Exercise-induced oxidative stress and dietary antioxidants. Asian journal of sports medicine. 2015;6(1).##  Tanzi R, Parson A. Decoding Darkness: The genetic causes of Alzheimer's disease. PERSEUS (NY) Publishing. 2014:69-73.## Ceccariglia S, Alvino A, Del Fa A, Parolini O, Michetti F, Gangitano C. Autophagy is Activated In Vivo during Trimethyltin-Induced Apoptotic Neurodegeneration: A Study in the Rat Hippocampus. International journal of molecular sciences. 2019;21(1).## Malekzadeh S, Edalatmanesh MA, Mehrabani D, Shariati M. Effect of the Xenograft Transplantation of Human Dental Pulp Stem Cells on Anxiety and Memory in Trimethyltin Induced-Alzheimer Disease Model. Qom University of Medical Sciences Journal. 2019;13(7):10-21.## Bazyar Y, Rafiei S, Hosseini A, Edalatmanesh MA. Effect of endurance exercise training and gallic acid on tumor necrosis factor-? in an animal model of alzheimer’s disease. 2015.## Malekzadeh S, Edalatmanesh MA, Mehrabani D, Shariati M. Drugs induced Alzheimer’s disease in animal model. Galen Medical Journal. 2017;6(3):185-96.## Zare M, Zar A, Edalatmanesh M. The implementation of eight weeks of endurance training and lithium chloride administration on brain-derived neurotrophic factor (BDNF) serum levels in rats with alzheimer's disease. J Adv Med Biomed Res. 2016;24(103):62-70.##  Arzi A, Houshmand G, Goudarzi M, Khadem Haghighian H, Rashidi Nooshabadi M. Comparison of the analgesic effects of royal jelly with morphine and aspirin in rats using the formalin. Journal of Babol University of Medical Sciences. 2015;17(2):50-6.## Webster I, Du Toit EF, Huisamen B. The effect of long term swim training on physiological stress levels in the rat: peer reviewed short communication. Medical technology SA. 2010;24(2):37-40.## Sadock BJ, Sadock VA, Ruiz P. Comprehensive textbook of psychiatry: lippincott Williams & wilkins Philadelphia, PA; 2000.## Marco EM, Llorente R, López-Gallardo M, Mela V, Llorente-Berzal Á, Prada C, et al. The maternal deprivation animal model revisited. Neuroscience & Biobehavioral Reviews. 2015;51:151-63.## Nemoda Z, Massart R, Suderman M, Hallett M, Li T, Coote M, et al. Maternal depression is associated with DNA methylation changes in cord blood T lymphocytes and adult hippocampi. Translational psychiatry. 2015;5(4):e545-e.## Pan Y, Xu J, Jin P, Yang Q, Zhu K, You M, et al. Royal Jelly Ameliorates Behavioral Deficits, Cholinergic System Deficiency, and Autonomic Nervous Dysfunction in Ovariectomized Cholesterol-Fed Rabbits. Molecules (Basel, Switzerland). 2019;24(6):1149.## Patki G, Li L, Allam F, Solanki N, Dao AT, Alkadhi K, et al. Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder. Physiology & behavior. 2014;130:47-53.## Sadeghi M, Peeri M, Hosseini M-J. Adolescent voluntary exercise attenuated hippocampal innate immunity responses and depressive-like behaviors following maternal separation stress in male rats. Physiology & behavior. 2016;163:177-83.## Greenwood BN, Foley TE, Day HE, Burhans D, Brooks L, Campeau S, et al. Wheel running alters serotonin (5-HT) transporter, 5-HT1A, 5-HT1B, and alpha1b-adrenergic receptor mRNA in the rat raphe nuclei. Biological psychiatry. 2005;57(5):559-68.## Jafarzadeh Baghan A, Azarbayjani MA. The effect of four weeks of voluntary and compulsory training on anxiety-like behavior induced by childhood stress and cerebellar inflammatory factors in rats. Yafteh. 2019;21(3).## Vimalanathan A, Gidyk DC, Diwan M, Gouveia FV, Lipsman N, Giacobbe P, et al. Endocannabinoid modulating drugs improve anxiety but not the expression of conditioned fear in a rodent model of post-traumatic stress disorder. Neuropharmacology. 2020:107965.##  Evans GW, Kim P. Childhood poverty, chronic stress, self‐regulation, and coping. Child development perspectives. 2013;7(1):43-8.## Goto C, Higashi Y, Kimura M, Noma K, Hara K, Nakagawa K, et al. Effect of different intensities of exercise on endothelium-dependent vasodilation in humans: role of endothelium-dependent nitric oxide and oxidative stress. Circulation. 2003;108(5):530-5.## da Cunha MJ, da Cunha AA, Ferreira AG, Machado FR, Schmitz F, Lima DD, et al. Physical exercise reverses glutamate uptake and oxidative stress effects of chronic homocysteine administration in the rat. International Journal of Developmental Neuroscience. 2012;30(2):69-74.## Camiletti-Moirón D, Aparicio VA, Nebot E, Medina G, Martínez R, Kapravelou G, et al. High-protein diet induces oxidative stress in rat brain: protective action of high-intensity exercise against lipid peroxidation. Nutricion hospitalaria. 2015;31(2):866-74.## Schneider CD, Barp J, Ribeiro JL, Belló-Klein A, Oliveira AR. Oxidative stress after three different intensities of running. Canadian journal of applied physiology. 2005;30(6):723-34.## Calabrese EJ, Baldwin LA. Defining hormesis. Human & experimental toxicology. 2002;21(2):91-7.## Hill Y, Kiefer AW, Silva PL, Van Yperen NW, Meijer RR, Fischer N, et al. Antifragility in Climbing: Determining Optimal Stress Loads for Athletic Performance Training. Front Psychol. 2020;11:272.##  Selye H. Stress and distress. Comprehensive therapy. 1975;1(8):9-13.##  Notkola I-L, Sulkava R, Pekkanen J, Erkinjuntti T, Ehnholm C, Kivinen P, et al. Serum total cholesterol, apolipoprotein E {FC12} e4 allele, and Alzheimer’s disease. Neuroepidemiology. 1998;17(1):14-20##