Effects of black Berberis vulgaris L combined with aerobic and resistance exercise on blood metabolic parameters and liver enzymes in obese rats

  1. SARA TORKAMANEH 1
  2. JAVIER GENE-MORALES 1
  3. ALVARO JUESAS 1
  4. JORGE FLÁNDEZ 2
  5. RAOUF HAMMAMI 3
  6. MOHMOUD RAFIEIAN-KOPAEI 4
  7. JUAN CARLOS COLADO 1
  1. 1 Universitat de València
    info

    Universitat de València

    Valencia, España

    ROR https://ror.org/043nxc105

  2. 2 Universidad Austral de Chile
    info

    Universidad Austral de Chile

    Valdivia, Chile

    ROR https://ror.org/029ycp228

  3. 3 Manouba University
    info

    Manouba University

    Manouba, Túnez

    ROR https://ror.org/0503ejf32

  4. 4 Shahrekord University of Medical Sciences
    info

    Shahrekord University of Medical Sciences

    Shahr-e Kord, Irán

    ROR https://ror.org/0506tgm76

Revista:
Journal of Human Sport and Exercise: JHSE

ISSN: 1988-5202

Ano de publicación: 2021

Título do exemplar: Autumn Conferences of Sports Science

Volume: 16

Número: 2

Páxinas: 619-629

Tipo: Artigo

DOI: 10.14198/JHSE.2021.16.PROC2.47 DIALNET GOOGLE SCHOLAR lock_openRUA editor

Outras publicacións en: Journal of Human Sport and Exercise: JHSE

Obxectivos de Desenvolvemento Sustentable

Resumo

Purpose: The aim of this study was to investigate the effects of a six-week intake of Berberis vulgaris L in combination with resistance and aerobic exercise on the lipid profile, metabolic parameters, and liver enzymes of obese male rats. Methods: 56 male Wistar rats were divided into seven groups: 1) healthy control (n = 8); 2) hypercaloric fatty-food-based diet (n = 8); 3) aerobic exercise (AE, n = 8); 4) resistance exercise (RE, n = 8); 5) black Berberis vulgaris L extract intake (n = 8); 6) Berberis intake combined with aerobic exercise (BAE, n = 8); and 7) Berberis intake combined with resistance exercise (BRE, n = 8). All the rats (except the controls) were induced fatty liver by six weeks of a hypercaloric diet before the intervention. After six weeks of intervention, blood samples were taken to obtain cholesterol, triglycerides, high-density lipoprotein cholesterol (HDL), low-density lipoprotein cholesterol (LDL), glucose of c-reactive protein (CRP), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and urea. Differences between groups were evaluated using the Kruskal Wallis test with post-hoc pairwise comparisons. Results: All the intervention groups significantly (p < .05) improved the parameters compared to the hypercaloric group in almost all the assessed parameters, reaching in many cases significantly better values than the healthy group (control). Similar results were obtained between the experimental groups; however, the outcomes were slightly better (non-significant differences) for the combination of the Berberis extract and both exercise methodologies. Conclusion: The use of herbal medicines such as Berberis vulgaris L in combination with aerobic or resistance exercises may be useful in the prevention of cardiovascular disease by improving risk factors such as blood lipid levels.

Referencias bibliográficas

  • Aslani, N., Entezari, M. H., Askari, G., Maghsoudi, Z., & Maracy, M. R. (2016). Effect of garlic and lemon juice mixture on lipid profile and some cardiovascular risk factors in people 30-60 years old with moderate hyperlipidaemia: a randomized clinical trial. International Journal of Preventive Medicine, 7(1), 95. https://doi.org/10.4103/2008-7802.187248
  • Atkins, J. L., Whincup, P. H., Morris, R. W., Lennon, L. T., Papacosta, O., & Wannamethee, S. G. (2014). Sarcopenic obesity and risk of cardiovascular disease and mortality: a population-based cohort study of older men. Journal of the American Geriatrics Society, 62(2), 253-260. https://doi.org/10.1111/jgs.12652
  • Bernhardt, V., Stickford, J. L., Bhammar, D. M., & Babb, T. G. (2016). Aerobic exercise training without weight loss reduces dyspnea on exertion in obese women. Respiratory Physiology & Neurobiology, 221, 64-70. https://doi.org/10.1016/j.resp.2015.11.004
  • Calabresi, L., & Franceschini, G. (2010). Lecithin: cholesterol acyltransferase, high-density lipoproteins, and atheroprotection in humans. Trends in Cardiovascular Medicine, 20(2), 50-53. https://doi.org/10.1016/j.tcm.2010.03.007
  • Cao, H., Li, C., Lei, L., Wang, X., Liu, S., Liu, Q., Huan, Y., Sun, S., & Shen, Z. (2020). Stachyose improves the effects of berberine on glucose metabolism by regulating intestinal microbiota and short-chain fatty acids in spontaneous type 2 diabetic KKAy Mice. Frontiers in Pharmacology, 11, 1641. https://doi.org/10.3389/fphar.2020.578943
  • Changizi Ashtiyani, S., Zarei, A., Taheri, S., Rezaei, A., Golshan, M., & Ghafarzadegan, R. (2013). A comparative study of hypolipidemic activities of the extracts of Melissa officinalis and Berberis vulgaris in rats. Journal of Medicinal Plants, 12(47), 38-47.
  • Dulić, M., Ciganović, P., Vujić, L., & Zovko Končić, M. (2019). Antidiabetic and cosmeceutical potential of common barbery (Berberis vulgaris L) root bark extracts obtained by optimization of 'Green' ultrasound-assisted extraction. Molecules, 24(19), 3613. https://doi.org/10.3390/molecules24193613
  • Earnest, C. P., Artero, E. G., Sui, X., et al. (2013). Maximal estimated cardiorespiratory fitness, cardiometabolic risk factors, and metabolic syndrome in the aerobics center longitudinal study. In Mayo Clinic Proceedings, 88(3), 259-270). https://doi.org/10.1016/j.mayocp.2012.11.006
  • Emamat, H., Zahedmehr, A., Asadian, S., Tangestani, H., & Nasrollahzadeh, J. (2020). Effect of barberry (Berberis vulgaris) consumption on blood pressure, plasma lipids, and inflammation in patients with hypertension and other cardiovascular risk factors: study protocol for a randomized clinical trial. Trials, 21(1), 1-9. https://doi.org/10.1186/s13063-020-04918-7
  • Fatehi-Hassanabad, Z., Jafarzadeh, M., Tarhini, A., & Fatehi, M. (2005). The antihypertensive and vasodilator effects of aqueous extract from Berberis vulgaris fruit on hypertensive rats. Phytother Research: An International Journal Devoted to Pharmacological and Toxicological Evaluation of Natural Product Derivatives, 19(3), 222-225. https://doi.org/10.1002/ptr.1661
  • Firouzi, S., Malekahmadi, M., Ghayour-Mobarhan, M., Ferns, G., & Rahimi, H. R. (2018). Barberry in the treatment of obesity and metabolic syndrome: possible mechanisms of action. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 11, 699-705. https://doi.org/10.2147/DMSO.S181572
  • Ghanbari-Niaki, A., Khabazian, B. M., Hossaini-Kakhak, S. A., et al. (2007). Treadmill exercise enhances ABCA1 expression in rat liver. Biochemical and Biophysical Research Communications, 361(4), 841- 846. https://doi.org/10.1016/j.bbrc.2007.07.100
  • Haselgrübler, R., Lanzerstorfer, P., Röhrl, C., et al. (2019). Hypolipidemic effects of herbal extracts by reduction of adipocyte differentiation, intracellular neutral lipid content, lipolysis, fatty acid exchange and lipid droplet motility. Scientific Reports, 9(1), 1-18. https://doi.org/10.1038/s41598-019-47060-4
  • Iloon Kashkooli, R., Najafi, S. S., Sharif, F., Hamedi, A., Hoseini Asl, M. K., Najafi Kalyani, M., & Birjandi M. (2015). The effect of Berberis vulgaris extract on transaminase activities in non-alcoholic fatty liver disease. Hepatitis Monthly, 15(2), https://doi.org/10.5812/hepatmon.25067
  • Imenshahidi, M. & Hosseinzadeh, H. (2019). Berberine and barberry (Berberis vulgaris): a clinical review. Phytotherapy Research, 33(3), 504-523. https://doi.org/10.1002/ptr.6252
  • Kamada, M., Shiroma, E. J., Buring, J. E., Miyachi, M., & Lee, I. M. (2017). Strength training and allcause, cardiovascular disease, and cancer mortality in older women: a cohort study. Journal of the American Heart Association, 6(11), e007677. https://doi.org/10.1161/JAHA.117.007677
  • Kang, J. G. & Park., C.-Y. (2012). Anti-obesity drugs: a review about their effects and safety. Diabetes & Metabolism Journal, 36(1), 13-25. https://doi.org/10.4093/dmj.2012.36.1.13
  • Kazeminasab, F., Marandi, M., Ghaedi K., Esfarjani, F., & Moshtaghian, J. (2013). Endurance training enhances LXRα gene expression in Wistar male rats. European Journal of Applied Physiology, 113(9), 2285-2290. https://doi.org/10.1007/s00421-013-2658-z
  • Kobayashi, J., Nohara, A., Kawashiri, M., Inazuc, A., Koizumid, J., Nakajimae, K., & Mabuchia, H. (2007). Serum lipoprotein lipase mass: clinical significance of its measurement. Clinica Chimica Acta, 378(1- 2), 7-12. https://doi.org/10.1016/j.cca.2006.12.003
  • Kraus, W., Houmard, J., Duscha B., et al. (2002). Effects of the amount and intensity of exercise on plasma lipoproteins. New England Journal of Medicine, 347(19), 1483-1492. https://doi.org/10.1056/NEJMoa020194
  • Lazavi, F., Mirmiran, P., Sohrab, G., Nikpayam, O., Angoorani, P., & Hedayati, M. (2018). The barberry juice effects on metabolic factors and oxidative stress in patients with type 2 diabetes: a randomized clinical trial. Complementary Therapies in Clinal Practice, 31, 170-174. https://doi.org/10.1016/j.ctcp.2018.01.009
  • LeMura, L., von Duvillard, S., Andreacci, J., Klebez, J. M., Chelland. S. A., & Russo J. (2000). Lipid and lipoprotein profiles, cadiovascular fitness, body composition, and diet during and after resistance, aerobic and combination training in young women. European Journal of Applied Physiology, 82(5- 6), 451-458. https://doi.org/10.1007/s004210000234
  • Liu, Y., Lee, D. C., Li, Y., et al. (2019). Associations of resistance exercise with cardiovascular disease morbidity and mortality. Medicine and science in sports and exercise, 51(3), 499. https://doi.org/10.1249/MSS.0000000000001822
  • MacDonald, H. V., Johnson, B. T., Huedo‐Medina, T. B., et al. (2016). Dynamic resistance training as stand‐alone antihypertensive lifestyle therapy: a meta‐analysis. Journal of the American Heart Association, 5(10), e003231. https://doi.org/10.1161/JAHA.116.003231
  • Maliakkal, B. J. (2020). Pathogenesis of non-alcoholic fatty liver disease and implications on cardiovascular outcomes in liver transplantation. Translational Gastroenterology and Hepatology, 5, 36. https://doi.org/10.21037/tgh.2019.12.02
  • Matsuura, H. (2001). Saponins in garlic as modifiers of the risk of cardiovascular disease. The Journal of Nutrition, 131(3), 1000S-1005S. https://doi.org/10.1093/jn/131.3.1000S
  • Mazidi, M. & Speakman, J. R. (2018). Impact of obesity and ozone on the association between particulate air pollution and cardiovascular disease and stroke mortality among US adults. Journal of the American Heart Association, 7(11), e008006. https://doi.org/10.1161/JAHA.117.008006
  • Miyachi, M. (2013). Effects of resistance training on arterial stiffness: a meta-analysis. British Journal of Sports Medicine, 47(6), 393-396. https://doi.org/10.1136/bjsports-2012-090488
  • Miyashita, M., Eto, M., Sasai, H., Tsujimoto, T., Nomata, Y., & Tanaka, K. (2010). Twelve-week jogging training increases pre-heparin serum lipoprotein lipase concentrations in overweight/obese middleaged men. Journal of Atherosclerosis and Thrombosis, 17(1), 21-29. https://doi.org/10.5551/jat.2337
  • Mohammadi, A., Sahebkar, A., Kermani, T., Zhilaee, M., Tavallaie, S., & Ghayour Mobarhan, M. (2014). Barberry administration and pro-oxidant-antioxidant balance in patients with metabolic syndrome. Iranian Red Crescent Medical Journal, 16(12), e16786. https://doi.org/10.5812/ircmj.16786
  • Mohammadi, M., Bagheri, A., Marashi, H., Moshtaghi, N., & Balandari, A. (2011). Investigation into seasonal effect and browning inhibitor on callus regeneration of seedless barberry (Berberis vulgaris var. asperma). Plant Tissue Culture and Biotechnology, 21(2), 161‐168. https://doi.org/10.3329/ptcb.v21i2.10239
  • Schroeder, E. C., Franke, W. D., Sharp, R. L., & Lee, D. (2019). Comparative effectiveness of aerobic, resistance, and combined training on cardiovascular disease risk factors: a randomized controlled trial. PloS One, 14(1), e0210292. https://doi.org/10.1371/journal.pone.0210292
  • Shamsoddini, A., Sobhani, V., Ghamar Chehreh, M. E., Alavian, S. M., & Zaree, A. (2015). Effect of aerobic and resistance exercise training on liver enzymes and hepatic fat in Iranian men with nonalcoholic fatty liver disease. Hepatitis Monthly, 15(10), e31434. https://doi.org/10.5812/hepatmon.31434
  • Shidfar, F., Ebrahimi, SS., Hosseini, S., Heydari, I., Shidfar, S., & Hajhassani, G. (2012). The effects of Berberis vulgaris fruit extract on serum lipoproteins, apoB, apoA-I, homocysteine, glycemic control and total antioxidant capacity in type 2 diabetic patients. Iranian Journal of Pharmaceutical Research, 11(2), 643-652.
  • Tabeshpour, J., Imenshahidi, M., & Hosseinzadeh, H. (2017). A review of the effects of Berberis vulgaris and its major component, berberine, in metabolic syndrome. Iranian Journal of Basic Medical Sciences, 20(5), 557-568.
  • Taheri, S., Zarei, A., Ashtiyani, S. C., Rezaei, A., & Zaheiri, S. (2012). Evaluation of the effects of hydroalcoholic extract of berberis vulgaris root on the activity of liver enzymes in male hypercholesterolemic rats. Avicenna Journal of Phytomedicine, 2(3), 153.
  • Torkamaneh, S., Sharifi, GH., & Rafieian, M. (2016). The comparison between the effects of Berberis vulgaris Extract and aerobic exercise on none-alcoholic fatty liver in male rats. Der Pharma Chemica, 8(1), 244-247.
  • Vrzal, R., Zdařilová, A., Ulrichová, J., Bláha, L., Giesy, J. P., & Dvořák, Z. (2005). Activation of the aryl hydrocarbon receptor by berberine in HepG2 and H4IIE cells: biphasic effect on CYP1A1. Biochemical Pharmacology, 70(6), 925-936. https://doi.org/10.1016/j.bcp.2005.06.016
  • Wang, Y., & Xu, D. (2017). Effects of aerobic exercise on lipids and lipoproteins. Lipids in Health and Disease, 16(1), 1-8. https://doi.org/10.1186/s12944-017-0515-5
  • Wood, P. D., Stefanick, M. L., Williams, P. T., & Haskell, W. L. (1991). The effects on plasma lipoproteins of a prudent weight-reducing diet, with or without exercise, in overweight men and women. New England Journal of Medicine, 325(7), 461-466. https://doi.org/10.1056/NEJM199108153250703
  • World Health Organization (2017). Global recommendations on physical activity for health. ISBN: 9789241599979. Retrieved from: https://www.who.int/publications/i/item/9789241599979
  • Yang, Y., Chan, S. W., Hu, M., Walden, R., & Tomlinson, B. (2011). Effects of some common food constituents on cardiovascular disease. ISRN Cardiology, 2011, 397136. https://doi.org/10.5402/2011/397136
  • Yang, Z., Scott, C. A., Mao, C., Tang, J., & Farmer, A. J. (2014). Resistance exercise versus aerobic exercise for type 2 diabetes: a systematic review and meta-analysis. Sports Medicine, 44(4), 487-499. https://doi.org/10.1007/s40279-013-0128-8
  • Zarei, A., Changizi-Ashtiyani, S., Taheri, S., & Ramezani, M. (2015). A quick overview on some aspects of endocrinological and therapeutic effects of Berberis vulgaris L. Avicenna Journal of Phytomedicine, 5 (6), 485-497.
  • Zhan, J., Liu, Y. J., Cai, L. B., Xu, F. R., Xie, T., & He, Q. Q. (2017). Fruit and vegetable consumption and risk of cardiovascular disease: a meta-analysis of prospective cohort studies. Critical Reviews in Food Science and Nutrition, 57(8), 1650-1663. https://doi.org/10.1080/10408398.2015.1008980