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Review

Quercetin supplementation and muscular atrophy in animal models: A systematic review and meta-analysis

ORCID Icon, ORCID Icon, , & ORCID Icon
Pages 2166-2183 | Received 13 Jul 2022, Accepted 16 Sep 2022, Published online: 26 Sep 2022

References

  • Cohen, S.; Nathan, J. A.; Goldberg, A. L.; Muscle Wasting in Disease: Molecular Mechanisms and Promising Therapies. Nat. Rev. Drug Discov. 2015, 14(1), 58–74. DOI:10.1038/nrd4467.
  • Yin, L.; Li, N.; Jia, W.; Wang, N.; Liang, M.; Yang, X.; Du, G. Skeletal Muscle Atrophy: From Mechanisms to Treatments. Pharmacol. Res. 2021, 172, 105807. DOI: 10.1016/j.phrs.2021.105807.
  • Cruz-Jentoft, A. J.; Sayer, A. A. Sarcopenia. Lancet. 2019, 393(10191), 2636–2646. DOI: 10.1016/S0140-6736(19)31138-9.
  • Brill, K. T.; Weltman, A. L.; Gentili, A.; Patrie, J. T.; Fryburg, D. A.; Hanks, J. B.; Urban, R. J.; Veldhuis, J. D. Single and Combined Effects of Growth Hormone and Testosterone Administration on Measures of Body Composition, Physical Performance, Mood, Sexual Function, Bone Turnover, and Muscle Gene Expression in Healthy Older Men. J. Clin. Endocrinol. Metab. 2002, 87(12), 5649–5657. DOI: 10.1210/jc.2002-020098.
  • Zhang, L.; Pan, J.; Dong, Y.; Tweardy, D. J.; Dong, Y.; Garibotto, G.; Mitch, W. E. Stat3 Activation Links a C/EBPδ to Myostatin Pathway to Stimulate Loss of Muscle Mass. Cell Metab. 2013, 18(3), 368–379. DOI: 10.1016/j.cmet.2013.07.012.
  • Carter, G. T.; Wineinger, M. A.; Walsh, S. A.; Horasek, S. J.; Abresch, R. T.; Fowler, W. M.; Effect of Voluntary Wheel-Running Exercise on Muscles of the Mdx Mouse. Neuromuscul. Disord. 1995, 5(4), 323–332. DOI:10.1016/0960-8966(94)00063-f.
  • Kim, T. N.; Choi, K. M.; Sarcopenia: Definition, Epidemiology, and Pathophysiology. J. Bone Metab. 2013, 20(1), 1–10. DOI:10.11005/jbm.2013.20.1.1.
  • Sartori, R.; Romanello, V.; Sandri, M. Mechanisms of Muscle Atrophy and Hypertrophy: Implications in Health and Disease. Nat. Commun. 2021, 12(1), 330. DOI: 10.1038/s41467-020-20123-1.
  • Spaulding, H. R.; Ballmann, C. G.; Quindry, J. C.; Selsby, J. T.; Kumar, A. Long-Term Quercetin Dietary Enrichment Partially Protects Dystrophic Skeletal Muscle. PLOS ONE. 2016, 11(12), e0168293. DOI: 10.1371/journal.pone.0168293.
  • Ebrahimpour, S.; Zakeri, M.; Esmaeili, A. Crosstalk between Obesity, Diabetes, and Alzheimer’s Disease: Introducing Quercetin as an Effective Triple Herbal Medicine. Ageing Res. Rev. 2020, 62, 101095. DOI: 10.1016/j.arr.2020.101095.
  • Tang, S. M.; Deng, X. T.; Zhou, J.; Li, Q. P.; Ge, X. X.; Miao, L. Pharmacological Basis and New Insights of Quercetin Action in Respect to Its Anti-cancer Effects. Biomed. Pharmacother. 2020, 121, 109604. DOI: 10.1016/j.biopha.2019.109604.
  • Davis, J. M.; Murphy, E. A.; Carmichael, M. D.; Davis, B.; Quercetin Increases Brain and Muscle Mitochondrial Biogenesis and Exercise Tolerance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296(4), R1071–R1077. DOI:10.1152/ajpregu.90925.2008.
  • Koshinaka, K.; Honda, A.; Masuda, H.; Sato, A. Effect of Quercetin Treatment on Mitochondrial Biogenesis and Exercise-Induced AMP-Activated Protein Kinase Activation in Rat Skeletal Muscle. Nutrients. 2020, 12(3), 3. DOI: 10.3390/nu12030729.
  • Hajieva, P.;. The Effect of Polyphenols on Protein Degradation Pathways: Implications for Neuroprotection. Molecules. 2017, 22(1), 159. DOI: 10.3390/molecules22010159.
  • MacRae, H. S.; Mefferd, K. M.; Dietary Antioxidant Supplementation Combined with Quercetin Improves Cycling Time Trial Performance. Int. J. Sport Nutr. Exerc. Metab. 2006, 16(4), 405–419. DOI:10.1123/ijsnem.16.4.405.
  • Cheuvront, S. N.; Ely, B. R.; Kenefick, R. W.; Michniak-Kohn, B. B.; Rood, J. C.; Sawka, M. N.; No Effect of Nutritional Adenosine Receptor Antagonists on Exercise Performance in the Heat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296(2), R394–401. DOI:10.1152/ajpregu.90812.2008.
  • Kressler, J.; Millard-Stafford, M.; Warren, G. L. Quercetin and Endurance Exercise Capacity: A Systematic Review and Meta-analysis. Med. Sci. Sports Exerc. 2011, 43(12), 2396–2404. DOI: 10.1249/MSS.0b013e31822495a7.
  • Qu, Z.; Zhou, S.; Li, P.; Liu, C.; Yuan, B.; Zhang, S.; Liu, A. Natural Products and Skeletal Muscle Health. J. Nutr. Biochem. 2021, 93, 108619. DOI: 10.1016/j.jnutbio.2021.108619.
  • Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L. A.; PRISMA-P Group. Preferred Reporting Items for Systematic Review and Meta-analysis Protocols (PRISMA-P) 2015 Statement. Syst. Rev 2015, 4(1), 1. DOI:10.1186/2046-4053-4-1.
  • Fedorov, S.; GetData Graph Digitizer Version 2.26. Available from: Get data-graph-digitizer-com. Russia. (accessed on March 13 2022).
  • Salekzamani, S.; Ebrahimi-Mameghani, M.; Rezazadeh, K. The Antioxidant Activity of Artichoke (Cynara Scolymus): A Systematic Review and Meta-analysis of Animal Studies. Phytother. Res. 2019, 33(1), 55–71. DOI: 10.1002/ptr.6213.
  • Higgins, J. P.; Altman, D. G.; Gøtzsche, P. C.; Jüni, P.; Moher, D.; Oxman, A. D.; Savovic, J.; Schulz, K. F.; Weeks, L.; Sterne, J. A.; Cochrane Bias Methods Group; Cochrane Statistical Methods Group. The Cochrane Collaboration’s Tool for Assessing Risk of Bias in Randomised Trials. BMJ 2011, 343(oct18 2), d5928. DOI:10.1136/bmj.d5928.
  • Percie du Sert, N.; Hurst, V.; Ahluwalia, A.; Alam, S.; Avey, M. T.; Baker, M.; Browne, W. J.; Clark, A.; Cuthill, I. C.; Dirnagl, U., et al. the ARRIVE Guidelines 2.0. The ARRIVE Guidelines 2.0. The ARRIVE Guidelines 2.0: Updated Guidelines for Reporting Animal Research. Br. J. Pharmacol. 2020, 177(16), 3617–3624. DOI: 10.1111/bph.15193.
  • Percie du Sert, N.; Ahluwalia, A.; Alam, S.; Avey, M. T.; Baker, M.; Browne, W. J.; Clark, A.; Cuthill, I. C.; Dirnagl, U.; Emerson, M., et al. Reporting Animal Research: Explanation and Elaboration for the ARRIVE Guidelines 2.0. PLoS Biol. 2020, 18(7), e3000411. DOI: 10.1371/journal.pbio.3000411.
  • Thanigaimani, S.; Phie, J.; Golledge, J. Animal Models of Ischemic Limb Ulcers: A Systematic Review and Meta-analysis. B.M.J. Open Diabetes Res. Care. 2020, 8(1). 10.1136/bmjdrc-2020-001676
  • Cochrane Handbook for Systematic Reviews of Interventions Version 6.3. https://training.cochrane.org/handbook (accessed March 13 2022)
  • Patsopoulos, N. A.; Evangelou, E.; Ioannidis, J. P. Sensitivity of between-Study Heterogeneity in Meta-analysis: Proposed Metrics and Empirical Evaluation. Int. J. Epidemiol. 2008, 37(5), 1148–1157. DOI: 10.1093/ije/dyn065.
  • Arias, N.; Macarulla, M. T.; Aguirre, L.; Martínez-Castaño, M. G.; Portillo, M. P. Quercetin Can Reduce Insulin Resistance without Decreasing Adipose Tissue and Skeletal Muscle Fat Accumulation. Genes Nutr. 2014, 9(1), 361. DOI: 10.1007/s12263-013-0361-7.
  • Le, N. H.; Kim, C. S.; Park, T.; Park, J. H.; Sung, M. K.; Lee, D. G.; Hong, S. M.; Choe, S. Y.; Goto, T.; Kawada, T., et al. Quercetin Protects against Obesity-Induced Skeletal Muscle Inflammation and Atrophy. Mediators Inflamm. 2014, 2014, 834294. DOI: 10.1155/2014/834294.
  • Velázquez, K. T.; Enos, R. T.; Narsale, A. A.; Puppa, M. J.; Davis, J. M.; Murphy, E. A.; Carson, J. A. Quercetin Supplementation Attenuates the Progression of Cancer Cachexia in ApcMin/+ Mice. J. Nutr. 2014, 144(6), 868–875. DOI: 10.3945/jn.113.188367.
  • Assi, M.; Derbré, F.; Lefeuvre-Orfila, L.; Rébillard, A. Antioxidant Supplementation Accelerates Cachexia Development by Promoting Tumor Growth in C26 Tumor-Bearing Mice. Free Radic. Biol. Med. 2016, 91, 204–214. DOI: 10.1016/j.freeradbiomed.2015.12.019.
  • Selsby, J. T.; Ballmann, C. G.; Spaulding, H. R.; Ross, J. W.; Quindry, J. C. Oral Quercetin Administration Transiently Protects Respiratory Function in Dystrophin-Deficient Mice. J. Physiol. 2016, 594(20), 6037–6053. DOI: 10.1113/JP272057.
  • Mukai, R.; Matsui, N.; Fujikura, Y.; Matsumoto, N.; Hou, D. X.; Kanzaki, N.; Shibata, H.; Horikawa, M.; Iwasa, K.; Hirasaka, K., et al. Preventive Effect of Dietary Quercetin on Disuse Muscle Atrophy by Targeting Mitochondria in Denervated Mice. J. Nutr. Biochem. 2016, 31, 67–76. DOI: 10.1016/j.jnutbio.2016.02.001.
  • Kohara, A.; Machida, M.; Setoguchi, Y.; Ito, R.; Sugitani, M.; Maruki-Uchida, H.; Inagaki, H.; Ito, T.; Omi, N.; Takemasa, T. Enzymatically Modified Isoquercitrin Supplementation Intensifies Plantaris Muscle Fiber Hypertrophy in Functionally Overloaded Mice. J. Int. Soc. Sports Nutr. 2017, 14(1), 32. DOI: 10.1186/s12970-017-0190-y.
  • Spaulding, H. R.; Quindry, T.; Hammer, K.; Quindry, J. C.; Selsby, J. T. Nutraceutical and Pharmaceutical Cocktails Did Not Improve Muscle Function or Reduce Histological Damage in D2-mdx Mice. J. Appl. Physiol. (1985). 2019, 127(4), 1058–1066. DOI: 10.1152/japplphysiol.00162.2019.
  • Spaulding, H. R.; Quindry, T.; Quindry, J. C.; Selsby, J. T.; Nutraceutical and Pharmaceutical Cocktails Did Not Preserve Diaphragm Muscle Function or Reduce Muscle Damage in D2-mdx Mice. Exp. Physiol. 2020, 105(6), 989–999. DOI:10.1113/EP087887.
  • Tsukamoto-Sen, S.; Kawakami, S.; Maruki-Uchida, H.; Ito, R.; Matsui, N.; Komiya, Y.; Mita, Y.; Morisasa, M.; Goto-Inoue, N.; Furuichi, Y., et al. Effect of Antioxidant Supplementation on Skeletal Muscle and Metabolic Profile in Aging Mice. Food Funct. 2021, 12(2), 825–833. DOI: 10.1039/d0fo02051f.
  • Cao, R. Y.; Li, J.; Dai, Q.; Li, Q.; Yang, J. Muscle Atrophy: Present and Future. Adv. Exp. Med. Biol. 2018, 1088, 605–624. DOI: 10.1007/978-981-13-1435-3_29.
  • Cruz-Jentoft, A. J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A. A., et al. Sarcopenia: Revised European Consensus on Definition and Diagnosis. Age Ageing. 2019, 48(1), 16–31. DOI: 10.1093/ageing/afy169.
  • Wu, J.; Gao, W.; Wei, J.; Yang, J.; Pu, L.; Guo, C.; Quercetin Alters Energy Metabolism in Swimming Mice. Appl. Physiol. Nutr. Metab. 2012, 37(5), 912–922. DOI:10.1139/h2012-064.
  • Nieoczym, D.; Socała, K.; Raszewski, G.; Wlaź, P. Effect of Quercetin and Rutin in Some Acute Seizure Models in Mice. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2014, 54, 50–58. DOI: 10.1016/j.pnpbp.2014.05.007.
  • Doherty, T. J.;. Invited Review: Aging and Sarcopenia. J. Appl. Physiol. (1985). 2003, 95(4), 1717–1727. DOI: 10.1152/japplphysiol.00347.2003.
  • Young, A.; Stokes, M.; Crowe, M.; Size and Strength of the Quadriceps Muscles of Old and Young Women. Eur. J. Clin. Investig. 1984, 14(4), 282–287. DOI:10.1111/j.1365-2362.1984.tb01182.x.
  • Hughes, V. A.; Frontera, W. R.; Roubenoff, R.; Evans, W. J.; Singh, M. A. Longitudinal Changes in Body Composition in Older Men and Women: Role of Body Weight Change and Physical Activity. Am. J. Clin. Nutr. 2002, 76(2), 473–481. DOI: 10.1093/ajcn/76.2.473.
  • Goodpaster, B. H.; Park, S. W.; Harris, T. B.; Kritchevsky, S. B.; Nevitt, M.; Schwartz, A. V.; Simonsick, E. M.; Tylavsky, F. A.; Visser, M.; Newman, A. B.; The Loss of Skeletal Muscle Strength, Mass, and Quality in Older Adults: The Health, Aging and Body Composition Study. J. Gerontol. A Biol. Sci. Med. Sci. 2006, 61(10), 1059–1064. DOI:10.1093/gerona/61.10.1059.
  • Frontera, W. R.; Meredith, C. N.; O’Reilly, K. P.; Knuttgen, H. G.; Evans, W. J. Strength Conditioning in Older Men: Skeletal Muscle Hypertrophy and Improved Function. J. Appl. Physiol. (1985). 1988, 64(3), 1038–1044. DOI: 10.1152/jappl.1988.64.3.1038.
  • Ciciliot, S.; Rossi, A. C.; Dyar, K. A.; Blaauw, B.; Schiaffino, S. Muscle Type and Fiber Type Specificity in Muscle Wasting. Int. J. Biochem. Cell Biol. 2013, 45(10), 2191–2199. DOI: 10.1016/j.biocel.2013.05.016.
  • Chen, X.; Liang, D.; Huang, Z.; Jia, G.; Zhao, H.; Liu, G. Quercetin Regulates Skeletal Muscle Fiber Type Switching via Adiponectin Signaling. Food Funct. 2021, 12(6), 2693–2702. DOI: 10.1039/d1fo00031d.
  • D’Andrea, G.;. Quercetin: A Flavonol with Multifaceted Therapeutic Applications? Fitoterapia. 2015, 106, 256–271. DOI: 10.1016/j.fitote.2015.09.018.
  • Boots, A. W.; Haenen, G. R.; Bast, A. Health Effects of Quercetin: From Antioxidant to Nutraceutical. Eur. J. Pharmacol. 2008, 585(2–3), 325–337. DOI: 10.1016/j.ejphar.2008.03.008.
  • Harwood, M.; Danielewska-Nikiel, B.; Borzelleca, J. F.; Flamm, G. W.; Williams, G. M.; Lines, T. C. A Critical Review of the Data Related to the Safety of Quercetin and Lack of Evidence of in Vivo Toxicity, Including Lack of Genotoxic/Carcinogenic Properties. Food Chem. Toxicol. 2007, 45(11), 2179–2205. DOI: 10.1016/j.fct.2007.05.015.
  • Chan, S. T.; Chuang, C. H.; Lin, Y. C.; Liao, J. W.; Lii, C. K.; Yeh, S. L. Quercetin Enhances the Antitumor Effect of Trichostatin A and Suppresses Muscle Wasting in Tumor-Bearing Mice. Food Funct. 2018, 9(2), 871–879. DOI: 10.1039/c7fo01444a.
  • Dunnick, J. K.; Hailey, J. R.; Toxicity and Carcinogenicity Studies of Quercetin, a Natural Component of Foods. Fundam. Appl. Toxicol. 1992, 19(3), 423–431. DOI:10.1016/0272-0590(92)90181-g.
  • Singh, B.; Mense, S. M.; Bhat, N. K.; Putty, S.; Guthiel, W. A.; Remotti, F.; Bhat, H. K. Dietary Quercetin Exacerbates the Development of Estrogen-Induced Breast Tumors in Female ACI Rats. Toxicol. Appl. Pharmacol. 2010, 247(2), 83–90. DOI: 10.1016/j.taap.2010.06.011.
  • Wang, L.; Xu, Z.; Ling, D.; Li, J.; Wang, Y.; Shan, T. The Regulatory Role of Dietary Factors in Skeletal Muscle Development, Regeneration and Function. Crit. Rev. Food Sci. Nutr. 2022, 62(3), 764–782. DOI: 10.1080/10408398.2020.1828812.
  • Mansouri, A.; Reiner, Ž.; Ruscica, M.; Tedeschi-Reiner, E.; Radbakhsh, S.; Bagheri Ekta, M.; Sahebkar, A. Antioxidant Effects of Statins by Modulating Nrf2 and Nrf2/HO-1 Signaling in Different Diseases. J. Clin. Med. 2022, 11(5), 1313. DOI: 10.3390/jcm11051313.
  • Huang, D. D.; Fan, S. D.; Chen, X. Y.; Yan, X. L.; Zhang, X. Z.; Ma, B. W.; Yu, D. Y.; Xiao, W. Y.; Zhuang, C. L.; Yu, Z. Nrf2 Deficiency Exacerbates Frailty and Sarcopenia by Impairing Skeletal Muscle Mitochondrial Biogenesis and Dynamics in an Age-Dependent Manner. Exp. Gerontol. 2019, 119, 61–73. DOI: 10.1016/j.exger.2019.01.022.
  • Habtemariam, S.;. The Nrf2/HO-1 Axis as Targets for Flavanones: Neuroprotection by Pinocembrin, Naringenin, and Eriodictyol. Oxid. Med. Cell. Longev. 2019, 2019, 4724920. DOI: 10.1155/2019/4724920.
  • Kim, Y.; Kim, C. S.; Joe, Y.; Chung, H. T.; Ha, T. Y.; Yu, R. Quercetin Reduces Tumor Necrosis Factor Alpha-Induced Muscle Atrophy by Upregulation of Heme Oxygenase-1. J. Med. Food. 2018, 21(6), 551–559. DOI: 10.1089/jmf.2017.4108.
  • Amin, R. H.; Mathews, S. T.; Camp, H. S.; Ding, L.; Leff, T. Selective Activation of PPAR Gamma in Skeletal Muscle Induces Endogenous Production of Adiponectin and Protects Mice from Diet-Induced Insulin Resistance. Am. J. Physiol. Endocrinol. Metab. 2010, 298(1), E28–37. DOI: 10.1152/ajpendo.00446.2009.
  • Funakoshi, T.; Kanzaki, N.; Otsuka, Y.; Izumo, T.; Shibata, H.; Machida, S. Quercetin Inhibits Adipogenesis of Muscle Progenitor Cells in Vitro. Biochem. Biophys. Rep. 2018, 13, 39–44. DOI: 10.1016/j.bbrep.2017.12.003.
  • Lin, J.; Wu, H.; Tarr, P. T.; Zhang, C. Y.; Wu, Z.; Boss, O.; Michael, L. F.; Puigserver, P.; Isotani, E.; Olson, E. N., et al. Transcriptional co-Activator PGC-1 Alpha Drives the Formation of Slow-Twitch Muscle Fibres. Nature. 2002, 418(6899), 797–801. DOI: 10.1038/nature00904.
  • Gurd, B. J.;; Deacetylation of PGC-1α by SIRT1: Importance for Skeletal Muscle Function and Exercise-Induced Mitochondrial Biogenesis. Appl. Physiol. Nutr. Metab. 2011, 36(5), 589–597. DOI:10.1139/h11-070.