Sepsis impairs the propagation of cortical spreading depression in rats and this effect is prevented by antioxidant extract

References

• Bennett SR. Sepsis in the intensive care unit. Surgery. 2012;30(12):673–8.
   Google Scholar
• Mayr FB, Yende A, Angus DC. Epidemiology of severe sepsis. Virulence. 2014;5(1):4–11. doi: 10.4161/viru.27372
   PubMed Web of Science ®Google Scholar
• Catalão CH, Santos-Júnior NN, da Costa LH, Souza AO, Alberici LC, Rocha MJ. Brain oxidative stress during experimental sepsis is attenuated by simvastatin administration. Mol Neurobiol. 2016;54(9):7008–18. doi: 10.1007/s12035-016-0218-3
   PubMed Web of Science ®Google Scholar
• Ning Q, Liu Z, Wang X, Zhang R, Zhang J, Yang M, et al. Neurodegenerative changes and neuroapoptosis induced by systemic lipopolysaccharide administration are reversed by dexmedetomidine treatment in mice. Neurol Res. 2017;39(4):357–66. doi: 10.1080/01616412.2017.1281197
   PubMed Web of Science ®Google Scholar
• Bavunoglu I, Genc H, Konukoglu D, Cicekci H, Sozer V, Gelisgen R, et al. Oxidative stress parameters and inflammatory and immune mediators as markers of the severity of sepsis. J InfectDevCtries. 2016;10(10):1045–52.
   Web of Science ®Google Scholar
• Oliveira YP, Pontes-de-Carvalho LC, Couto RD, Noronha-Dutra AA. Oxidative stress in sepsis. Possible production of free radicals through an erythrocyte-mediated positive feedback mechanism. Braz J Infect Dis. 2017;21(1):19–26. doi: 10.1016/j.bjid.2016.11.004
   PubMed Web of Science ®Google Scholar
• Helal SM, Hassan GA, Zalat SI, Azkol MA. Immunomodulation in critically ill septic patients. MenoufiaMed J. 2015;28(1):259–65. doi: 10.4103/1110-2098.156005
   Google Scholar
• Costa NA, Gut AL, Azevedo PS, Tanni SE, Cunha NB, Magalhães ES, et al. Erythrocyte superoxide dismutase as a biomarker of septic acute kidney injury. Ann IntensiveCare. 2016;6(5):1–8.
   PubMedGoogle Scholar
• Comim CM, Cassol-Jr OJ, Constantino LS, Felisberto F, Petronilho F, Rezin GT, et al. Alterations in inflammatory mediators, oxidative stress parameters and energetic metabolism in the brain of sepsis survivor rats. Neurochem Res. 2011;36(2):304–11. doi: 10.1007/s11064-010-0320-2
   PubMed Web of Science ®Google Scholar
• Sonneville R, Verdonk F, Rauturier C, Klein IF, Wolff M, Annane D, et al. Understanding brain dysfunction in sepsis. Ann Intensive Care. 2013;3(1):1–11. doi: 10.1186/2110-5820-3-15
   PubMedGoogle Scholar
• Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7(6):359–90. doi: 10.1152/jn.1944.7.6.359
   Google Scholar
• Sánchez-Porras R, Robles-Cabrera A, Santos E. Despolarización cortical extendida: um nuevo mecanismo fisiopatológico em lãs enfermedades neurológicas. Med Clin. 2014;142(10):457–62. doi: 10.1016/j.medcli.2013.05.029
   PubMedGoogle Scholar
• Pusic KM, Pusic AD, Kemme J, Kraig RP. Spreading depression requires microglia and is decreased by their M2a polarization from environmental enrichment. Glia. 2014;62(7):1176–94. doi: 10.1002/glia.22672
   PubMed Web of Science ®Google Scholar
• Grinberg YY, Van Drongelen W, Kraig RP. Insulin-like growth factor-1 lowers spreading depression susceptibility and reduces oxidative stress. J Neurochem. 2012;122(1):221–9. doi: 10.1111/j.1471-4159.2012.07763.x
   PubMed Web of Science ®Google Scholar
• Mariutti LRB, Rodrigues E, Chisté RC, Fernandes E, Mercadante AZ. The Amazonian fruit Byrsonimacrassifolia effectively scavenges reactive oxygen and nitrogen species and protects human erythrocytes against oxidative damage. Food Res Int. 2014;64:618–25. doi: 10.1016/j.foodres.2014.07.032
   PubMed Web of Science ®Google Scholar
• Pérez Gutiérrez RM, Muñiz Ramirez A. Hexane extract of the seeds of Byrsonimacrassifolia accelerates wound healing in streptozotocin-induced diabetic rats. Chin J Integr Med. 2013: 1–7. doi:10.1007/s11655-013-1556-x.
   Google Scholar
• Sousa MSB, Holanda IMS, Monteiro HMC, Amâncio-dos-Santos A. Antioxidant extract counteracts the effects of aging on cortical spreading depression and oxidative stress in the brain cortex. Acta Cir Bras. 2018;33(6):472–82. doi: 10.1590/s0102-865020180060000001
   PubMed Web of Science ®Google Scholar
• Hubbard WJ, Choudhry M, Schwacha MG, Kerby JD, Rued LW, Bland KL, et al. Cecal ligation and puncture. Shock. 2005;24:52–7. doi: 10.1097/01.shk.0000191414.94461.7e
   PubMed Web of Science ®Google Scholar
• Monteiro HMC, Barreto-Silva NL, Dos Santos EG, Santos AS, Sousa MSB, Amâncio-dos-Santos A. Physical exercise versus fluoxetine: antagonistic effects on cortical spreading depression in wistar rats. Eur J Pharmacol. 2015;762:49–54. doi: 10.1016/j.ejphar.2015.05.027
   PubMed Web of Science ®Google Scholar
• Lima CB, Soares GS, Vitor SM, Castellano B, Andrade-da-Costa BLS, Guedes RCA. Neonatal treatment with monosodium glutamate lastingly facilitates spreading depression in the rat cortex. Life Sci. 2013;93:388e392. doi: 10.1016/j.lfs.2013.07.009
   Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–54. doi: 10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–8. doi: 10.1016/0003-2697(79)90738-3
   PubMed Web of Science ®Google Scholar
• Misra P, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247(10):3170–5. doi: 10.1016/S0021-9258(19)45228-9
   PubMed Web of Science ®Google Scholar
• Aebi H. Catalase in vitro. Methods Enzymol. 1984;105:121–6. doi: 10.1016/S0076-6879(84)05016-3
   PubMed Web of Science ®Google Scholar
• Hissin PJ, Hilf RA. Fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem. 1976;74(1):214–26. doi: 10.1016/0003-2697(76)90326-2
   PubMed Web of Science ®Google Scholar
• Batista-de-Oliveira M, Lopes AA, Mendes-da-Silva RF, Guedes RC. Aging-dependent brain electrophysiological effects in rats after distinct lactation conditions, and treadmill exercise: a spreading depression analysis. ExpGerontol. 2012;47(6):452–7.
   Web of Science ®Google Scholar
• Guedes RC, Vasconcelos CA. Sleep-deprivation enhances in adult rats the antagonistic effects of pilocarpine on cortical spreading depression: a dose-response study. Neurosci Lett. 2008;442(2):118–22. doi: 10.1016/j.neulet.2008.07.011
   PubMed Web of Science ®Google Scholar
• Tejada S, Sureda A, Roca C, Gamundí A, Esteban S. Antioxidant response and oxidative damage in brain cortex after high dose of pilocarpine. Brain Res Bull. 2007;71(4):372–5. doi: 10.1016/j.brainresbull.2006.10.005
   PubMed Web of Science ®Google Scholar
• Reznik ME, Merkler AE, Mahta A, Murthy SB, Claassen J, Kamel H. Long-term risk of seizures in adult survivors of sepsis. Neurology. 2017;89(14):1476–82. doi: 10.1212/WNL.0000000000004538
   PubMed Web of Science ®Google Scholar
• Berisavac II, Padjen VV, Ercegovac MD, Beslać-Bumbaširević LG, Stanarčević PD, Stefanović-Budimkić MS, et al. Focal epileptic seizures, electroencephalography and outcome of sepsis associated encephalopathy—A pilot study. Clin Neurol Neurosurg. 2016;148:60–6. doi: 10.1016/j.clineuro.2016.06.013
   PubMed Web of Science ®Google Scholar
• Sewal RK, Modi M, Saikia UN, Chakrabarti A, Medhi B. Increase in seizure susceptibility in sepsis like condition explained by spiking cytokines and altered adhesion molecules level with impaired blood brain barrier integrity in experimental model of rats treated with lipopolysaccharides. Epilepsy Res. 2017;135:176–86. doi: 10.1016/j.eplepsyres.2017.05.012
   PubMed Web of Science ®Google Scholar
• Marchi N, Granata T, Ghosh C, Janigro D. Blood–brain barrier dysfunction and epilepsy: Pathophysiologic role and therapeutic approaches. Epilepsia. 2012;53(11):1877–86. doi: 10.1111/j.1528-1167.2012.03637.x
   PubMed Web of Science ®Google Scholar
• Kirkebøen KA, Strand OA. The role of nitric oxide in sepsis–an overview. ActaAnaesthesiol Scand. 1999;43(3):275–88. doi: 10.1034/j.1399-6576.1999.430307.x
   PubMed Web of Science ®Google Scholar
• Petzold GC, Haack S, Halbach OVB, Priller J, Lehmann T, Heinemann U, et al. Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke. 2008;39:1292–9. doi: 10.1161/STROKEAHA.107.500710
   PubMed Web of Science ®Google Scholar
• Amini-Khoei H, Kordjazy N, Haj-Mirzaian A, Amiri S, Haj-Mirzaian A, Shirzadian A, et al. Anticonvulsant effect of minocycline on pentylenetetrazole-induced seizure in mice: involvement of nitric oxide and N-methyl-D-aspartate receptor. Can J PhysiolPharmacol. 2018;96(8):742–50. doi: 10.1139/cjpp-2017-0673
   Google Scholar
• Hu S, Sheng WS, Ehrlich LC, Peterson PK, Chao CC. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation. 2000;7(3):153–9. doi: 10.1159/000026433
   PubMed Web of Science ®Google Scholar
• Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, et al. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci. 2001;4(7):702–10. doi: 10.1038/89490
   PubMed Web of Science ®Google Scholar
• Costa MS, Rocha JB, Perosa SR, Cavalheiro EA, Naffah-Mazzacoratti MG. Pilocarpine-induced status epilepticus increases glutamate release in rat hippocampal synaptosomes. Neurosci Lett. 2004;356(1):41–4. doi: 10.1016/j.neulet.2003.11.019
   PubMed Web of Science ®Google Scholar
• Dal-Pizzol F, Tomasi CD, Ritter C. Septic encephalopathy: does inflammation drive the brain crazy? RevistaBrasileira de Psiquiatria. 2014;36(3):251–8.
   PubMed Web of Science ®Google Scholar
• Kadoi Y, Saito S. An alteration in the gamma-aminobutyric acid receptor system in experimentally induced septic shock in rats. Crit Care Med. 1996;24(2):298–305. doi: 10.1097/00003246-199602000-00020
   PubMed Web of Science ®Google Scholar
• Holland RP, Akerman S, Goadsby PJ. Cortical spreading depression-associated cerebral blood flow changes induced by mechanical stimulation are modulated by AMPA and GABA receptors. Cephalalgia. 2010;30(5):519–27.
   PubMed Web of Science ®Google Scholar
• Li Y, Hadden C, Cooper A, Ahmed A, Wu H, Lupashin VV, Mayeux PR, et al. Sepsis induced elevation in plasma serotonin facilitates endothelial hyperpermeability. Sci Rep. 2016;6:1–13. doi:10.1038/srep22747 doi: 10.1038/s41598-016-0001-8
   PubMed Web of Science ®Google Scholar
• Shimizu I, Adachi N, Liu K, Lei B, Nagaro T, Arai T. Sepsis facilitates brain serotonin activity and impairs learning ability in rats. BrainResearch. 1999;830(1):94–100.
   PubMed Web of Science ®Google Scholar
• Guedes RC, Amâncio-Dos-Santos AA, Manhães-De-Castro R, Costa-Cruz RR. Citalopram has an antagonistic action on cortical spreading depression in well-nourished and early-malnourished adult rats. NutrNeurosci. 2002;5(2):115–23.
   Web of Science ®Google Scholar
• Monte-Guedes CK, Alves EV, Viana-da-Silva E, Guedes RC. Chronic treatment with ascorbic acid enhances cortical spreading depression in developing well-nourished and malnourished rats. NeurosciLett. 2011;496(3):191–4.
   PubMed Web of Science ®Google Scholar
• Mendes-da-Silva RF, Lopes-de-Morais AA, Bandim-da-Silva ME, Cavalcanti G de A, Rodrigues AR, Andrade-da-Costa BL, et al. Prooxidant versus antioxidant brain action of ascorbic acid in wellnourished and malnourished rats as a function of dose: a cortical spreading depression and malondialdehyde analysis. Neuropharmacology. 2014;86:155–60. doi: 10.1016/j.neuropharm.2014.06.027
   PubMed Web of Science ®Google Scholar
• Charles A, Brennan K. Cortical spreading depression-new insights and persistent questions. Cephalalgia. 2009;29(10):1115–24. doi: 10.1111/j.1468-2982.2009.01983.x
   PubMed Web of Science ®Google Scholar
• Guedes RCA, Araújo MDGR, Verçosa TC, Bion FM, de Sá AL, Pereira Jr A, et al. Evidence of an inverse correlation between serotonergic activity and spreading depression propagation in the rat cortex. Brain Res. 2017;1672:29–34. doi: 10.1016/j.brainres.2017.07.011
   PubMed Web of Science ®Google Scholar
• Marschollek C, Karimzadeh F, Jafarian M, Ahmadi M, Mohajeri SM, Rahimi S, et al. Effects of garlic extract on spreading depression: In vitro and in vivo investigations. NutrNeurosci. 2017;20(2):127–34.
   PubMed Web of Science ®Google Scholar
• Maitra SR, Wojnar MM, Lang CH. Alterations in tissue glucose uptake during the hyperglycemic and hypoglycemic phases of sepsis. Shock. 2000;13(5):379–85. doi: 10.1097/00024382-200005000-00006
   PubMed Web of Science ®Google Scholar
• Lewis AJ, Billiar TR, Rosengart MR. Biology and metabolism of sepsis: innate immunity, bioenergetics, and autophagy. Surg Infect (Larchmt. 2016;17(3):286–93. doi: 10.1089/sur.2015.262
   PubMed Web of Science ®Google Scholar
• Miller SI, Wallace RJ, Musher DM, Septimus EJ, Kohl S, Baughn RE. Hypoglycemia as a manifestation of sepsis. Am J Med. 1980;68(5):649–54. doi: 10.1016/0002-9343(80)90250-8
   PubMed Web of Science ®Google Scholar
• Sonn J, Mayevsky A. The effect of ethanol on metabolic, hemodynamic ans electrical responses to cortical spreading depression. BrainResearch. 2001;908(2):174–86.
   PubMed Web of Science ®Google Scholar
• Lorente L, Martín MM, Abreu-González P, Domínguez-Rodriguez A, Labarta L, Díaz C, et al. Sustained high serum malondialdehyde levels are associated with severity and mortality in septic patients. Crit Care. 2013;17(6):1–11. doi: 10.1186/cc13155
   Web of Science ®Google Scholar
• Yokoo H, Chiba S, Tomita K, Takashina M, Sagara H, Yagisita S, et al. Neurodegenerative evidence in Mice brains with cecal ligation and puncture-induced sepsis: preventive effect of the free radical scavenger edaravone. Plos One. 2012;7(12):e51539. doi: 10.1371/journal.pone.0051539
   PubMed Web of Science ®Google Scholar
• Liao YR, Lin JY. Intraperitoneal administration ameliorates lipopolysaccharide-induced systemic inflammation in mice. Life Sci. 2015;137:89–97. doi: 10.1016/j.lfs.2015.07.015
   PubMed Web of Science ®Google Scholar
• El-Gawad HM, Khalifa AE. Quercetin, coenzyme Q10, and L-canavanine as protective agents against lipid peroxidation and nitric oxide generation in endotoxin-induced shock in rat brain. Pharmacol Res. 2001;43(3):257–63. doi: 10.1006/phrs.2000.0781
   PubMed Web of Science ®Google Scholar
• Tang D, Kang R, Xiao W, Zhang H, Lotze MT, Wang H, et al. Quercetin prevents LPS-induced high-mobility group box 1 release and proinflammatory function. Am J Respir Cell Mol Biol. 2009;41(6):651–60. doi: 10.1165/rcmb.2008-0119OC
   PubMed Web of Science ®Google Scholar
• Lu CW, Lin TY, Wang SJ. Quercetin inhibits depolarization-evoked glutamate release in nerve terminals from rat cerebral cortex. Neurotoxicology. 2013;39:1–9. doi: 10.1016/j.neuro.2013.07.009
   PubMed Web of Science ®Google Scholar
• Wu W, Li Y, Wu Y, Zhang Y, Wang Z, Liu X. Lutein suppresses inflammatory responses through Nrf2 activation and NF-kB inactivation in lipopolysaccharide-stimulated BV-2 microglia. Mol Nutr Food Res. 2015;59(9):1663–73. doi: 10.1002/mnfr.201500109
   PubMed Web of Science ®Google Scholar
• Giustina AD, Goldim MP, Danielski LG, Florentino D, Mathias K, Garbossa L, et al. Alpha-lipoic acid attenuates acute neuroinflammation and long-term cognitive impairment after polymicrobial sepsis. Neurochem Int. 2017;108:436–47. doi: 10.1016/j.neuint.2017.06.003
   PubMed Web of Science ®Google Scholar
• Yamanaka D, Kawano T, Nishigaki A, Aoyama B, Tateiwa H, et al. Effects of epigallocatechin-3-gallate on systemic inflammation-induced cognitive dysfunction in aged rats. J Anesth. 2017;31(5):726–35. doi: 10.1007/s00540-017-2392-5
   PubMed Web of Science ®Google Scholar
• Bozza FA, D'Avila JC, Ritter C, Sonneville R, Sharshar T, Dal-Pizzol F. Bioenergetics, mitochondrial dysfunction, and oxidative stress in the pathophysiology of septic encephalopathy. Shock. 2013;39(7):10–6. doi: 10.1097/SHK.0b013e31828fade1
   PubMed Web of Science ®Google Scholar