Abstract
There is evidence that kombucha beverage (KB), a traditional fermented beverage, has a preventive effect on experimental brain ischemia. According to our previous studies, pre-treatment of KB attenuates brain edema and improves motor skills and oxidative stress in a rat model of global brain ischemia. This study was designed to evaluate the effects of the pre-treatment of KB, as a novel agent, on pro-inflammatory parameters and brain histopathology changes following global brain ischemia. Adult male Wistar rats were randomly divided into the sham, the control, and the groups treated with kombucha (KB1 and KB2 groups). KB at doses 1 and 2 mL/kg was prescribed two-week consecutive days before induction of global brain ischemia. Global brain ischemia was induced by blocking common carotid arteries for 60 min and the following reperfusion by 24 h. The serum and brain levels of tumor necrosis factor-α(TNF-α), IL-1β, histopathological change, and infarct volume are determined using the ELISA, hematoxylin and eosin (H&E), and 2,3,5-triphenyl tetrazolium chloride (TTC) staining, respectively. This study indicated that pre-treatment of KB significantly reduced infarct volume, the serum, and brain levels of TNF-α and IL-1β. The histopathological finding of the brain tissue confirmed a protective role for pre-treatment KB in the ischemic rats. Thus, the present study showed that the beneficial effects of KB pre-treatment on brain ischemic may be mediated by decreasing pro-inflammatory parameters.
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The datasets of this study are available from the corresponding author upon reasonable request.
References
Gaggia F, Baffoni L, Galiano M, Nielsen DS, Jakobsen RR, Castro-Mejía JL, Bosi S, Truzzi F, Musumeci F, Dinelli G, Di Gioia D (2018) Kombucha beverage from green, black and rooibos teas: a comparative study looking at microbiology, chemistry and antioxidant activity. Nutrients 11(1):1. https://doi.org/10.3390/nu11010001
Wu S, Yu Q, Shen S, Shan X, Hua J, Zhu J, Qiu J, Deng Y, Zhou Q, Jiang Y, Yuan H (2022) Non-targeted metabolomics and electronic tongue analysis reveal the effect of rolling time on the sensory quality and nonvolatile metabolites of congou black tea. LWT 169:113971
Jayabalan R, Malbasa RV, Loncar ES, Vitas JS, Sathishkumar M (2014) A review on kombucha tea-microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Compr Rev Food Safety 13(4):538–550. https://doi.org/10.1111/1541-4337.12073
Wang Y, Ji B, Wu W, Wang R, Yang Z, Zhang D, Tian W (2014) Hepatoprotective effects of kombucha tea: identification of functional strains and quantification of functional components. J SciFood Agric 94(2):265–272. https://doi.org/10.1002/jsfa.6245
Batista P, Penas MR, Pintado M, Oliveira-Silva P (2022) Kombucha: perceptions and future prospects. Foods 11(13):1977. https://doi.org/10.3390/foods11131977
Bhattacharya S, Gachhui R, Sil PC (2013) Effect of kombucha, a fermented black tea in attenuating oxidative stress mediated tissue damage in alloxan-induced diabetic rats. Food Chem Toxicol 60:328–340. https://doi.org/10.1016/j.fct.2013.07.051
Jessica Martínez Leal MJ, Suárez LV, Jayabalan R, Oros JH, Escalante-Aburto A (2018) A review on health benefits of kombucha nutritional compounds and metabolites, CyTA -. J Food 16(1):390–399. https://doi.org/10.1080/19476337.2017.1410499
Murugesan GS, Sathishkumar M, Jayabalan R, Binupriya AR, Swaminathan K, Yun SE (2009) Hepatoprotective and curative properties of Kombucha tea against carbon tetrachloride-induced toxicity. J Microbiol Biotechnol 19(4):397–402. https://doi.org/10.4014/jmb.0806.374
Diez-Ozaeta I, Astiazaran OJ (2022) Recent advances in kombucha tea: microbial consortium, chemical parameters, health implications and biocellulose production. Int J Food Microbiol 16:377:109783. https://doi.org/10.1016/j.ijfoodmicro
Marzban F, Azizi G, Afraei S, Sedaghat R, Seyedzadeh MH, Razavi A, Mirshafiey A (2015) Kombucha tea ameliorates experimental autoimmune encephalomyelitis in mouse model of multiple sclerosis. Food and Agricultural Immunology 2(6):782–793. https://doi.org/10.1080/09540105.2015.1036353
Haghmorad D, Yazdanpanah E, Sadighimoghaddam B, Yousefi B, Sahafi P, Ghorbani N, Rashidy-Pour A, Kokhaei P (2021) Kombucha ameliorates experimental autoimmune encephalomyelitis through activation of Treg and Th2 cells. Acta Neurol Belg 121(6):1685–1692. https://doi.org/10.1007/s13760-020-01475-3
Mousavi SM, Hashemi SA, Zarei M, Gholami A, Lai CW, Chiang WH, Omidifar N, Bahrani S, Mazraedoost S (2020) Recent progress in chemical composition, production, and pharmaceutical effects of kombucha beverage: A complementary and alternative medicine. Evid Based Complement Alternat Med. 18; 2020:4397543. doi: https://doi.org/10.1155/2020/4397543
Kabiri N, Setorki M (2016) Protective effect of kombucha tea on brain damage induced by transient cerebral ischemia and reperfusion in rat. Bangladesh J Pharmacol 11(3):675–683
Mesgari-Abbasi M, Eskandari Vaezi F, Hossienzadeh F (2022) Chronic pre-treatment of kombucha tea protects brain injury induced by ischemia/reperfusion in global brain ischemia, PREPRINT (Version 1) available. https://doi.org/10.21203/rs.3.rs-1482869/v1]. at Research Square [
Vázquez-Cabral BD, Larrosa-Pérez M, Gallegos-Infante JA, Moreno-Jiménez MR, González-Laredo RF, Rutiaga-Quiñones JG, Gamboa-Gomez CI, Rocha-Guzman NE (2017) Oak kombucha protects against oxidative stress and inflammatory processes. Chem Biol Interact 25:272:1–9. https://doi.org/10.1016/j.cbi.2017.05.001
Pawluk H, Woźniak A, Grzesk G, Kołodziejska R, Kozakiewicz M, Kopkowska E, Grzechowiak E, Kozera G (2020) The role of selected pro-inflammatory cytokines in pathogenesis of ischemic stroke. Clin Interv Aging 15:469–484. https://doi.org/10.2147/CIA.S233909
Zhu H, Hu S, Li Y, Sun Y, Xiong X, Hu X, Chen J, Qiu Sh (2022) Interleukins and ischemic stroke. Front Immunol 13:828447. https://doi.org/10.3389/fimmu.2022.828447
Chen AQ, Fang Z, Chen XL, Yang S, Zhou YF, Mao L, Xia YP, Jin HJ, Li YN, You MF, Wang XX (2019) Microglia-derived TNF-α mediates endothelial necroptosis aggravating blood brain–barrier disruption after ischemic stroke. Cell Death Dis 10(7):487. https://doi.org/10.1038/s41419-019-1716-9
Muller S, Kufner A, Dell’Orco A, Rackoll T, Mekle R, Piper SK, Fiebach JB, Villringer K, Flöel A, Endres M, Ebinger M, Nave AH) 2021(evolution of blood-brain barrier permeability in subacute ischemic stroke and associations with serum biomarkers and functional outcome. Front Neurol 20; 12:730923. doi: https://doi.org/10.3389/fneur.2021.730923
Nian K, Harding IC, Herman IM, Ebong EE (2020) Blood-brain barrier damage in ischemic stroke and its regulation by endothelial mechano transduction. Front Physiol. 2020; 11:605398. doi:https://doi.org/10.3389/fphys.2020.605398
Vakili A, Mojarrad S, Akhavan MM, Rashidy-Pour A (2011) Pentoxifylline attenuates TNF-α protein levels and brain edema following temporary focal cerebral ischemia in rats. Brain Res 1377:119–125. https://doi.org/10.1016/j.brainres.2011.01.001
Klopfleisch R (2013) Multiparametric and semiquantitative scoring systems for the evaluation of mouse model histopathology–a systematic review. BMC Vet Res 9:123. https://doi.org/10.1186/1746-6148-9-123
Lakshminarayanashastry Viswanatha G, Venkatanarasappa Venkataranganna M, Lingeswara Prasad NB (2019) Methanolic leaf extract of Punica granatum attenuates ischemia-reperfusion brain injury in Wistar rats: potential antioxidant and anti-inflammatory mechanisms. Iran J Basic Med Sci 22(2):187–196. https://doi.org/10.22038/ijbms.2018.30660.7389
Viswanatha GL, Kumar LM, Rafiq M, Kavya KJ, Thippeswamy AH, Yuvaraj HC, Azeemuddin M, Anturlikar SD, Patki PS, Babu UV, Ramakrishnan S (2015) LC-MS/MS profiling and neuroprotective effects of Mentat® against transient global ischemia and reperfusion-induced brain injury in rats. Nutrition 31(7–8):1008–1017. https://doi.org/10.1016/j.nut.2015.02.009
Bemeur C, Qu H, Desjardins P, Butterworth RF (2010) IL-1 or TNF receptor gene deletion delays onset of encephalopathy and attenuates brain edema in experimental acute liver failure. Neurochem Int 56(2):213–215. https://doi.org/10.1016/j.neuint.2009.11.010
Rama Rao KV, Jayakumar AR, Tong X, Alvarez VM, Norenberg MD (2010) Marked potentiation of cell swelling by cytokines in ammonia-sensitized cultured astrocytes. J Neuroinflammation 7:66. https://doi.org/10.1186/1742-2094-7-66
Jang DI, Lee AH, Shin HY, Song HR, Park JH, Kang TB, Lee SR, Yang SH (2021) The role of tumor necrosis factor alpha (TNF-α) in autoimmune disease and current TNF-α inhibitors in therapeutics. Int J Mol Sci 8(22):2719. https://doi.org/10.3389/fphys.2020.605398
Liu LR, Liu JC, Bao JS, Bai QQ, Wang GQ (2020) Interaction of microglia and astrocytes in the neurovascular unit. Front Immunol 8. https://doi.org/10.3389/fimmu.2020.01024. ,11:1024
Shreeniwas R, Koga S, Karakurum M, Pinsky D, Kaiser E, Brett J, Wolitzky BA, Norton C, plocinski J, Benjamin W (1992) Hypoxia-mediated induction of endothelial cell interleukin-1 alpha. An autocrine mechanism promoting expression of leukocyte adhesion molecules on the vessel surface. J Clin Invest 90(6):2333–2339. https://doi.org/10.1172/JCI116122
Liu FQ, Liu Y, Lui VC, Lamb JR, Tam PK, Chen Y (2008) Hypoxia modulates lipopolysaccharide induced TNF-alpha expression in murine macrophages. Exp CellRes 314(6):1327–1336. https://doi.org/10.1016/j.yexcr.2008.01.007
Petronilho F, P ́erico SR, Vuolo F, MinaF, Constantino L, Comim CM, Quevedo J, Souza DO, Dal-PizzolF (2012) Protective effects of guanosine against sepsis-induced damage in rat brain and cognitive impairment. Brain Behav Immun 26:904–910. https://doi.org/10.1016/j.bbi.2012.03.007
Yli-Karjanmaa M, Clausen BH, Degn M, Novrup HG, Ellman DG, Toft-Jensen P, Szymkowski DE, Stensballe A, Meyer M, Brambilla R, Lambertsen KL (2019) Topical administration of a soluble TNF inhibitor reduces infarct volume after focal cerebral ischemia in mice. Front Neurosci 7:13:781. https://doi.org/10.3389/fnins.2019.00781
Yang C, Hawkins KE, Doré S, Candelario-Jalil E (2019) Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am J Physiol Cell Physiol. 1;316(2):C135-C153. doi: https://doi.org/10.1152/ajpcell.00136.2018
Fischer R, Maier O (2015) Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxid Med Cell Longev. 2015:610813. doi: https://doi.org/10.1155/2015/610813
Murray KN, Parry-Jones AR, Allan SM (2015) Interleukin-1 and acute brain injury. Front Cell Neurosci 9:18. https://doi.org/10.3389/fncel.2015.00018PMID: 25705177; PMCID: PMC4319479
Hasegawa T, Hall CJ, Crosier PS, Abe G, Kawakami K, Kudo A, Kawakami A (2017) Transient inflammatory response mediated by interleukin-1β is required for proper regeneration in zebrafish fin fold. Elife 23:6: e22716. https://doi.org/10.7554/eLife.22716
Hsieh HL, Yang CM (2013) Role of redox signaling in neuroinflammation and neurodegenerative diseases. Biomed Res Int. 2013:484613. doi: https://doi.org/10.1155/2013/484613
Hasegawa T, Hall CJ, Crosier PS, Abe G, Kawakami K, Kudo A, Kawakami A (2017) Transient inflammatory response mediated by interleukin-1β is required for proper regeneration in zebrafish fin fold. Elife 6:e22716. https://doi.org/10.7554/eLife.22716
Tarkowski E, Ringqvist A, Rosengren L, Jensen C, Ekholm S, Wennmalm A (2000) Intrathecal release of nitric oxide and its relation to final brain damage in patients with stroke. Cerebrovasc Dis 10(3):200–206. https://doi.org/10.1159/000016057
Gharib OA (2009) Effects of Kombucha on oxidative stress induced nephrotoxicity in rats. Chin Med 27: 4:23. doi: https://doi.org/10.1186/1749-8546-4-23
Jurcau A, Simion A (2021) Neuroinflammation in cerebral ischemia and ischemia/reperfusion injuries: from pathophysiology to therapeutic strategies. Int J Mol Sci 21(1):14. https://doi.org/10.3390/ijms23010014
McGarry T, Biniecka M, Veale DJ, Fearon U (2018) Hypoxia, oxidative stress and inflammation. Free Radic Biol Med 125:15–24. https://doi.org/10.1016/j.freeradbiomed.2018.03.042
Kruk J, Aboul-Enein HY, Kładna A, Bowser JE (2019) Oxidative stress in biological systems and its relation with pathophysiological functions: the effect of physical activity on cellular redox homeostasis. Free Radic Res 4(5):497–521. https://doi.org/10.1080/10715762.2019.1612059
Aloulou A, Hamden K, Elloumi D, Ali MB, Hargafi K, Jaouadi B, Ayadi F, Elfeki A, Ammar E (2012) Hypoglycemic and antilipidemic properties of kombucha tea in alloxan-induced diabetic rats. BMC Complement Altern Med 16:12:63. https://doi.org/10.1186/1472-6882-12-63
Neumann JT, Cohan CH, Dave KR, Wright CB, Perez-Pinzon MA (2013) Global cerebral ischemia: synaptic and cognitive dysfunction. Curr Drug Targets 14(1):20–35. https://doi.org/10.2174/138945013804806514
Stradecki-Cohan HM, Cohan CH, Raval AP, Dave KR, Reginensi D, Gittens RA, Youbi M, Perez-Pinzon MA (2017) Cognitive deficits after cerebral ischemia and underlying dysfunctional plasticity: potential targets for recovery of cognition. J Alzheimers 60(s1):S87–S105. https://doi.org/10.3233/JAD-170057
Cheng X, Yang YL, Li WH, Liu M, Zhang SS, Wang YH, Du GH (2020) Dynamic alterations of brain injury, functional recovery, and metabolites profile after cerebral ischemia/reperfusion in rats contributes to potential biomarkers. J Mol Neurosci 70(5):667–676. https://doi.org/10.1007/s12031-019-01474-x
Chen C, Zhang X, Huang H, Bao H, Li X, Cheng Y, Zhang J, Ding Y, Yang Y, Gu H, Xia D (2021) Bi-enzymes treatments attenuate cognitive impairment associated with oxidative damage of heavy metals. R Soc Open Sci 13(1):201404. https://doi.org/10.1098/rsos.201404
Bellassoued K, Ghrab F, Makni-Ayadi F, Van Pelt J, Elfeki A, Ammar E (2015) Protective effect of kombucha on rats fed a hypercholesterolemic diet is mediated by its antioxidant activity. Pharm Biol 53(11):1699–1709. https://doi.org/10.3109/13880209.2014.1001408
Acknowledgements
The authors thank Mr. Mahmud Reza Hassanzadeh for his helpful surgery assistance.
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This study was financially supported by the Drug Applied Research Center of Tabriz University of Medical Sciences (Grant no. 66949), and Author F.H. has received this research support.
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Fariba Ghiasi and Fezzeh Hosseinzadeh conceived and designed the study and wrote the paper. Mehran Mesgari-Abbasi, Monireh Khordadmehr, and Sepideh Imani performed laboratory experiments and contributed to the analysis. All authors approved the final version of the manuscript.
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The study was approved by the research and ethics committee of Tabriz University of Medical Sciences in Iran (the ethics code was (IR.TBZMED.VCR.REC.1400.115). All procedures were performed according to guidelines for the care and use of laboratory animals at Tabriz University of Medical Sciences.
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Ghiasi, F., Mesgari-Abbasi, M., Khordadmehr, M. et al. Chronic Kombucha Beverage Consumption Attenuates Inflammatory Markers and Histopathology of Brain Tissue in Transnet Global Brain Ischemia in Rats. Neurochem Res 48, 3202–3211 (2023). https://doi.org/10.1007/s11064-023-03980-2
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DOI: https://doi.org/10.1007/s11064-023-03980-2