BEHAVIORAL EFFECTS OF ARONIA MELANOCARPA FRUIT JUICE IN EXPERIMENTAL ANIMALS WITH DIET-INDUCED METABOLIC SYNDROME

Authors

  • M. Abtulov Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author
  • M. Eftimov Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author
  • S. Marinova Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author
  • M. Salbashian Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author
  • M. Zhelyazkova-Savova Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author
  • S. Valcheva-Kuzmanova Department of Pharmacology and Clinical Pharmacology and Therapeutics, Medical University “Prof. Dr. Paraskev Stoyanov”, Varna, Bulgaria Author

DOI:

https://doi.org/10.15547/tjs.2024.03.003

Keywords:

Aronia melanocarpa, behavior, metabolic syndrome, rats

Abstract

PURPOSE: This study evaluated the effects of polyphenol-rich Aronia melanocarpa fruit juice (AMFJ) on the behavior of rats with metabolic syndrome (MS) induced by high-fat high-fructose diet. METHODS: Fifty rats were allocated into 5 groups (10 rats per group): control, MS, MS + AMFJ2.5, MS + AMFJ5 and MS + AMFJ10. During the induction of MS in the course of 10 weeks, the last three groups were treated with AMFJ at doses 2,5 ml/kg, 5 ml/kg and 10 ml kg, respectively. The open field test was used to examine locomotion, the social interaction test was used to evaluate anxiety, the depression-like state was studied by the forced swimming test and spatial memory was evaluated by the place recognition test. RESULTS: No differences were found in the overall motor activity across the groups. Anxiety and memory impairment were established in MS rats. AMFJ counteracted the development of anxiety, and brought the memory function back to normal. CONCLUSIONS: The improvement of the MS-induced behavioral alterations might be attributed to the rich polyphenolic content of AMFJ, essential for its antioxidant, anti-inflammatory and metabolic actions, and probably underlie also the anxiolytic and memory-enhancing effects observed in the present study.

References

Christiansen, C.B., Mellbye, F.B., Hermansen, K., Jeppesen, P.B. and Gregersen, S., Effects of Aronia melanocarpa on cardiometabolic diseases: a systematic review of quasi-design studies and randomized controlled trials. Rev Diabet Stud, 18(2):76-92, 2022.

Rochlani, Y., Pothineni, N.V., Kovelamudi, S. and Mehta, J.L., Metabolic syndrome: pathophysiology, management, and modulation by natural compounds. Ther Adv Cardiovasc Dis, 11(8):215-25, 2017.

Masrouri, S., Moazzeni, S.S., Cheraghloo, N., Azizi, F. and Hadaegh, F., The clinical value of metabolic syndrome and its components with respect to sudden cardiac death using different definitions: Two decades of follow-up from the Tehran Lipid and Glucose Study. Cardiovasc Diabetol, 21(1):269, 2022.

Tang, F., Wang, G. and Lian, Y., Association between anxiety and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Psychoneuroendocrinology, 77:112-21, 2017.

Yates, K.F., Sweat, V., Yau, P.L., Turchiano, M.M. and Convit, A., Impact of metabolic syndrome on cognition and brain: a selected review of the literature. Arterioscler Thromb Vasc Biol, 32(9):2060-7, 2012.

Gancheva, S.M., Zhelyazkova-Savova, M.D., Galunska, B. and Chervenkov T., Experimental models of metabolic syndrome in rats. Scr Sci Med, 47(2):14-21, 2015.

Mukherjee, A. and Banerjee, S., Effects of metabolic syndrome on anxiety in mice. Indian J Pharm Sci, 80(3):453-9, 2018..

Mukherjee, A., Mehta, B.K., Sen, K.K. and Banerjee, S., Metabolic syndrome-associated cognitive decline in mice: role of minocycline. Indian J Pharmacol, 50:61-8, 2018.

Eftimov, M., Dobreva, C., Velkova, D. and Valcheva-Kuzmanova, S., Effect of Aronia melanocarpa fruit juice on behaviour of rats exposed to social isolation. Trakia J Sci, 12(1):123-6, 2014.

Eftimov, M., Dobreva, C., Velkova, D. and Valcheva-Kuzmanova, S., Effect of Aronia melanocarpa fruit juice on reserpine-induced hypokinesia and oxydative stress in rats. Scr Sci Pharm, 1(2):29-34, 2014.

Eftimov, M. and Valcheva-Kuzmanova, S., Antidepressant-like effect of aronia melanocarpa fruit juice applied subchronically to rats. Scri Sci Med, 45(1):7-11, 2013.

Eftimov, M. and Valcheva-Kuzmanova, S., Anxiolytic-like effect of Aronia Melanocarpa fruit juice applied subchronically to rats. Scri Sci Med, 45(Suppl.5):13-7, 2013.

Lee, H.Y., Weon, J.B., Jung, Y.S., Kim, N.Y., Kim, M.K. and Ma, C.J., Cognitive-enhancing effect of Aronia melanocarpa extract against memory impairment induced by scopolamine in mice. Evid Based Complement Alternat Med, 2016:6145926, 2016.

Tomassoni, D., Martinelli, I., Moruzzi, M., Micioni Di Bonaventura, M.V., Cifani, C., Amenta, F. and Tayebati, S. K., Obesity and age-related changes in the brain of the Zucker Leprfa/fa rats. Nutrients, 12(5):1356, 2020.

Valcheva-Kuzmanova, Sm, Eftimov, M., Belcheva, I., Belcheva, S. and Tashev, R., Anti-anxiety effect of aronia melanocarpa fruit juice administered subchronically to rats. Farmacia, 64(3):367-71, 2016.

Valcheva-Kuzmanova, S., Eftimov, M., Belcheva, I., Tashev, R. and Belcheva, S., Effect of Aronia melanocarpa fruit juice on learning and memory in the two-way active avoidance task in rats. J Biomed Clin Res, 6(1):18-23, 2013.

Valcheva-Kuzmanova, S., Eftimov, M., Tashev, R., Belcheva, I. and Belcheva, S., Memory effects of Aronia melanocarpa fruit juice in a passive avoidance test in rats. Folia med, 56(3):199-203, 2014.

Valcheva-Kuzmanova, S., Denev, P., Krachanova, M., Surleva, A. and Belcheva A., Composition and antioxidant activity of Aronia melanocarpa fruit juice. Varna Med Forum, 3(1):15-20, 2014.

Belovicova, K., Bogi, E., Csatlosova, K. and Dubovicky, M., Animal tests for anxiety-like and depression-like behavior in rats. Interdiscip Toxicol, 10(1):40-3, 2017.

File, S.E., and Hyde, J.R., Can social interaction be used to measure anxiety? Br J Pharmacol, 62(1):19-24, 1978.

Lueptow, L.M., Novel object recognition test for the investigation of learning and memory in mice. J Vis Exp, (126):55718, 2017.

Porsolt, R.D., Le Pichon, M. and Jalfre M., Depression: a new animal model sensitive to antidepressant treatments. Nature, 266(5604):730-2, 1977.

Cardoso, S. and Moreira, P.I., Diabesity and brain disturbances: a metabolic perspective. Mol Aspects Med, 66:71-9, 2019.

Gray, S.M., Meijer, R.I. and Barrett, E.J., Insulin regulates brain function, but how does it get there? Diabetes, 63(12):3992-7, 2014.

Cardoso, S., Correia, S., Santos, R.X., Carvalho, C., Santos, M.S., Oliveira, C.R., Perry, G., Smith, M. A., Zhu, X. and Moreira, P.I., Insulin is a two-edged knife on the brain. J Alzheimers Dis, 18(3):483-507, 2009.

Kellar, D. and Craft, S., Brain insulin resistance in Alzheimer's disease and related disorders: mechanisms and therapeutic approaches. Lancet Neurol, 19(9):758-66, 2020.

Taouis, M. and Torres-Aleman, I., Editorial: Insulin and the brain. Front Endocrinol (Lausanne), 10:299, 2019.

Sa-Nguanmoo, P., Tanajak, P., Kerdphoo, S., Jaiwongkam, T., Pratchayasakul, W., Chattipakorn, N. and Chattipakorn, S.C., SGLT2-inhibitor and DPP-4 inhibitor improve brain function via attenuating mitochondrial dysfunction, insulin resistance, inflammation, and apoptosis in HFD-induced obese rats. Toxicol Appl Pharmacol, 333:42-50, 2017.

Sa-Nguanmoo P, Tanajak P, Kerdphoo S, Satjaritanun P, Wang X, Liang G., Li, X., Jiang, C., Pratchayasakul, W., Chattipakorn, N. and Chattipakorn, S. C., FGF21 improves cognition by restored synaptic plasticity, dendritic spine density, brain mitochondrial function and cell apoptosis in obese-insulin resistant male rats. Horm Behav, 85:86-95, 2016.

Willmann, C., Brockmann, K., Wagner, R., Kullmann, S., Preissl, H., Schnauder, G., Maetzler, W., Gasser, T., Berg, D., Eschweiler, G. W., Metzger, F., Fallgatter, A. J., Häring, H. U., Fritsche, A. and Heni, M., Insulin sensitivity predicts cognitive decline in individuals with prediabetes. BMJ Open Diabetes Res Care, 8(2):e001741, 2020.

Mahjoub, S. and Masrour-Roudsari, J., Role of oxidative stress in pathogenesis of metabolic syndrome. Caspian J Intern Med, 3(1):386-96, 2012.

Dorszewska, J., Kozubski, W., Alzheimer's disease - the 21st century challenge. IntechOpen, 2018.

Guo, C., Sun, L., Chen, X. and Zhang, D., Oxidative stress, mitochondrial damage and neurodegenerative diseases. Neural Regen Res, 8(21):2003-14, 2013.

Asmat, U., Abad, K. and Ismail, K., Diabetes mellitus and oxidative stress-a concise review. Saudi Pharm J, 24(5):547-53, 2016.

Marseglia, L., Manti, S., D'Angelo, G., Nicotera, A., Parisi, E., Di Rosa, G., Gitto, E. and Arrigo, T., Oxidative stress in obesity: a critical component in human diseases. Int J Mol Sci, 16(1):378-400, 2014.

Kim, J.M., Park, S.K., Guo, T.J., Kang, J.Y., Ha, J.S., Lee du, S., Lee, U. and Heo, H.J., Anti-amnesic effect of Dendropanax morbifera via JNK signaling pathway on cognitive dysfunction in high-fat diet-induced diabetic mice. Behav Brain Res, 312:39-54, 2016.

Pintana, H., Sripetchwandee, J., Supakul, L., Apaijai, N., Chattipakorn, N. and Chattipakorn, S., Garlic extract attenuates brain mitochondrial dysfunction and cognitive deficit in obese-insulin resistant rats. Appl Physiol Nutr Metab, 39(12):1373-9, 2014.

Ströhle, A., Gensichen, J. and Domschke, K., The diagnosis and treatment of anxiety disorders. Dtsch Arztebl Int, 155(37):611-20, 2018.

Pan, A., Keum, N., Okereke, O.I., Sun, Q., Kivimaki, M., Rubin, R.R. and Hu, F.B., Bidirectional association between depression and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Diabetes Care, 35(5):1171-80, 2012.

Tang, F., Wang, G. and Lian, Y., Association between anxiety and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Psychoneuroendocrinology, 77:112-21, 2017.

Kahl, K.G., Schweiger, U., Correll, C., Müller, C., Busch, M.L., Bauer, M. and Schwarz, P., Depression, anxiety disorders, and metabolic syndrome in a population at risk for type 2 diabetes mellitus. Brain Behav, 5(3):e0030662, 2015.

Urwyler, S.A., Schuetz, P., Ebrahimi, F., Donath, M.Y. and Christ-Crain, M., Interleukin-1 antagonism decreases cortisol levels in obese individuals. J Clin Endocrinol Metab, 102(5):1712-8, 2017.

Grillo, C.A., Piroli, G.G., Junor, L., Wilson, S.P., Mott, D.D., Wilson, M.A. and Reagan, L. P., Obesity/hyperleptinemic phenotype impairs structural and functional plasticity in the rat hippocampus. Physiol Behav, 105(1):138-44, 2011.

Grillo, C.A., Piroli, G.G., Kaigler, K.F., Wilson, S.P., Wilson, M.A. and Reagan, L.P., Downregulation of hypothalamic insulin receptor expression elicits depressive‐like behaviors in rats. Behav Brain Res, 222(1):230–5, 2011.

Grillo CA, Tamashiro KL, Piroli GG, Melhorn S, Gass JT, Newsom RJ, Reznikov, L.R., Smith, A., Wilson, S.P., Sakai, R.R. and Reagan, L.P., Lentivirus-mediated downregulation of hypothalamic insulin receptor expression. Physiol Behav, 92(4):691-701, 2007.

Reyzov, M., Eftimov, M., Gancheva, S., Todorova, M., Zhelyazkova-Savova, M., Tzaneva, M. and Valcheva-Kuzmanova, S., Effect of Aronia melanocarpa fruit juice on glucose tolerance, lipid metabolism and obesity in a rat model of metabolic syndrome. Acta Aliment, 51(3):390-402, 2022.

Valcheva-Kuzmanova S. and Zhelyazkova-Savova M., Anxiolytic-like effect of Aronia melanocarpa fruit juice in rats. Methods Find Exp Clin Pharmacol, 31(10):651-4, 2009.

Valcheva-Kuzmanova, S., Kuzmanov, A., Kuzmanova, V. and Tzaneva, M., Aronia melanocarpa fruit juice ameliorates the symptoms of inflammatory bowel disease in TNBS-induced colitis in rats. Food Chem Toxicol, 113:33-9, 2018.

Valcheva-Kuzmanova, S., Stavreva, G., Dancheva, V., Terziev, L., Atanasova, M., Stoyanova, A., Dimitrova, A. and Shopova, V., Effect of Aronia melanocarpa fruit juice on amiodarone-induced pneumotoxicity in rats. Pharmacogn Mag, 10(38):132-40, 2014.

Banach, M., Wiloch, M., Zawada, K., Cyplik, W. and Kujawski, W., Evaluation of antioxidant and anti-inflammatory activity of anthocyanin-rich water-Soluble Aronia dry extracts. Molecules, 25(18):4055, 2020.

Zielinska‐Przyjemska, M., Olejnik, A., Dobrowolska‐Zachwieja, A. and Grajek W., Effects of Aronia melanocarpa polyphenols on oxidative metabolism and apoptosis of neutrophils from obese and non‐obese individuals. Acta Sci Pol-Technol Aliment, 6(3):75–87, 2007.

Bouayed, J., Rammal, H. and Soulimani, R., Oxidative stress and anxiety: relationship and cellular pathways. Oxid Med Cell Longev 2009;2(2):63-7.

Vogelzangs, N., Beekman, A.T., de Jonge, P. and Penninx, B.W., Anxiety disorders and inflammation in a large adult cohort. Transl Psychiatry, 3(4):e249, 2013.

McNay, E.C., Ong, C.T., McCrimmon, R.J., Cresswell, J., Bogan, J.S. and Sherwin, R.S., Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem, 93(4):546-53, 2010.

Francik, R., Krośniak, M., Sanocka, I., Bartoń, H., Hebda, T. and Francik, S., Aronia melanocarpa treatment and antioxidant status in selected tissues in Wistar rats. Biomed Res Int, 2014:457085, 2014.

Lee, H.Y., Weon, J.B., Ryu, G., Yang, W.S., Kim, N.Y., Kim, M.K. and Ma, C.J., Neuroprotective effect of Aronia melanocarpa extract against glutamate-induced oxidative stress in HT22 cells. BMC Complement Altern Med, 17(1):207, 2017.

Wen, H., Cui, H., Tian, H., Zhang, X., Ma, L., Ramassamy, C. and Li, J., Isolation of neuroprotective anthocyanins from black chokeberry (Aronia melanocarpa) against amyloid-β-Induced cognitive impairment. Foods, 10(1):63, 2020.

Wei, J., Zhang, G., Zhang, X., Xu, D., Gao, J., Fan, J. and Zhou, Z., Anthocyanins from black chokeberry (Aronia melanocarpa Elliot) delayed aging-related degenerative changes of brain. J Agric Food Chem, 65(29):5973-84, 2017.

Mu, J., Xin, G., Zhang, B., Wang, Y., Ning, C., Meng, X., Beneficial effects of Aronia melanocarpa berry extract on hepatic insulin resistance in type 2 diabetes mellitus rats. J Food Sci, 85(4):1307-18, 2020.

Kim, N.H., Jegal, J., Kim, Y.N., Heo, J.D., Rho, J.R., Yang, M.H. and Jeong, E.J., Chokeberry extract and its active polyphenols suppress adipogenesis in 3T3-L1 adipocytes and modulates fat accumulation and insulin resistance in diet-induced obese mice. Nutrients, 10(11):1734, 2018.

Downloads

Published

2024-09-17

Issue

Section

Original Contributions

How to Cite

BEHAVIORAL EFFECTS OF ARONIA MELANOCARPA FRUIT JUICE IN EXPERIMENTAL ANIMALS WITH DIET-INDUCED METABOLIC SYNDROME. (2024). TRAKIA JOURNAL OF SCIENCES, 22(3), 10. https://doi.org/10.15547/tjs.2024.03.003