https://doi.org/10.4081/ejh.2022.3328
Sufentanil alleviates cerebral ischemia-reperfusion injury by inhibiting inflammation and protecting the blood-brain barrier in rats
Submitted: 10 September 2021
Accepted: 19 December 2021
Published: 12 January 2022
Accepted: 19 December 2021
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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Stroke is a brain system disease with a high fatality rate and disability rate. About 80% of strokes are ischemic strokes. Cerebral ischemia-reperfusion injury (CIRI) caused by ischemic stroke seriously affects the prognosis of stroke patients. The purpose of this study is to investigate the effect of sufentanil (SUF) on CIRI model rats. We used middle cerebral artery occlusion (MCAO) to make the CIRI model in rats and monitored region cerebral blood flow (rCBF) to ensure that blood flow was blocked and recanalized. We used ELISA and RT-PCR to detect the expression of inflammatory factors in rat serum and brain tissue. In addition, we detected the expression of metalloproteinase (MMP) 2, MMP9 and collagen IV in brain tissues and performed Evans blue (EB) assay to determine the permeability of the blood-brain barrier (BBB). Finally, we clarified the apoptosis of brain tissue through the TUNEL staining and the detection of caspase3, Bcl2 and Bax. Various concentrations of SUF, especially 5, 10 and 25 μg/kg of SUF, all alleviated the infarct size, neurological function and brain edema of MCAO rats. SUF pretreatment also effectively reduced the expression of inflammatory cytokines in MCAO rats, including interleukin (IL)-1β, IL-4, IL-6, IL-8, IL-10 and tumor necrosis factor (TNF)-α. In addition, SUF also inhibited MMP2 and MMP9 and promoted the expression of collagen IV, indicating that SUF attenuated the destruction of the BBB. SUF also inhibited caspase3 and Bax rats and promoted Bcl2 in MCAO rats, thus inhibiting cell apoptosis. SUF pretreatment effectively improved the neurological function and cerebral infarction of MCAO rats, inhibited excessive inflammation in rats, protected the BBB, and inhibited cell apoptosis in brain tissue.
Elkind M, Boehme AK, Smith CJ, Meisel A, Buckwalter MS. Infection as a stroke risk factor and determinant of outcome after stroke. Stroke 2020;51:3156-68.
DOI: https://doi.org/10.1161/STROKEAHA.120.030429
Boot E, Ekker MS, Putaala J, Kittner S, De Leeuw FE, Tuladhar AM. Ischaemic stroke in young adults: a global perspective. J Neurol Neurosurg Psychiatry 2020;91:411-7.
DOI: https://doi.org/10.1136/jnnp-2019-322424
Oie LR, Kurth T, Gulati S, Dodick DW. Migraine and risk of stroke. J Neurol Neurosurg Psychiatry 2020;91:593-604.
DOI: https://doi.org/10.1136/jnnp-2018-318254
Bavarsad K, Barreto GE, Hadjzadeh MA, Sahebkar A. Protective effects of curcumin against ischemia-reperfusion injury in the nervous system. Mol Neurobiol 2019;56:1391-404.
DOI: https://doi.org/10.1007/s12035-018-1169-7
Cason BA, Gamperl AK, Slocum RE, Hickey RF. Anesthetic-induced preconditioning: previous administration of isoflurane decreases myocardial infarct size in rabbits. Anesthesiology 1997;87:1182-90.
DOI: https://doi.org/10.1097/00000542-199711000-00023
Nunes RR, Duval NG, de Alencar JC, Franco SB, de Andrade NQ, Dumaresq DM, et al. Anesthetics, cerebral protection and preconditioning. Braz J Anesthesiol 2013;63:119-28.
DOI: https://doi.org/10.1016/j.bjane.2012.06.003
Frey UH, Klaassen M, Ochsenfarth C, Murke F, Thielmann M, Kottenberg E, et al. Remote ischaemic preconditioning increases serum extracellular vesicle concentrations with altered micro-RNA signature in CABG patients. Acta Anaesthesiol Scand 2019;63:483-92.
DOI: https://doi.org/10.1111/aas.13296
Lian YH, Fang J, Zhou HD, Jiang HF, Xie KJ. Sufentanil preconditioning protects against hepatic ischemia-reperfusion injury by suppressing inflammation. Med Sci Monit 2019;25:2265-73.
DOI: https://doi.org/10.12659/MSM.913145
Zhou L, Yang X, Shu S, Wang S, Guo F, Yin Y, et al. Sufentanil protects the liver from ischemia/reperfusion-induced inflammation and apoptosis by inhibiting ATF4-induced TP53BP2 expression. Inflammation 2021;44:1160-1174.
DOI: https://doi.org/10.1007/s10753-020-01410-x
Tao H, Nuo M, Min S. Sufentanil protects the rat myocardium against ischemia-reperfusion injury via activation of the ERK1/2 pathway. Cytotechnology 2018;70:169-76.
DOI: https://doi.org/10.1007/s10616-017-0127-y
Wu Q, Shang Y, Bai Y, Wu Y, Wang H, Shen T. Sufentanil preconditioning protects against myocardial ischemia/reperfusion injury via miR-125a/DRAM2 axis. Cell Cycle 2021;20:383-391.
DOI: https://doi.org/10.1080/15384101.2021.1875668
Khosravi MB, Kahrom M, Tahari M, Alizadeh K, Soltani G, Ghanad MA. Effect of the aortic root infusion of sufentanil on ischemia-reperfusion injury in patients undergoing coronary artery bypass grafting: A randomized clinical trial. J Tehran Heart Cent 2019;14:177-182.
DOI: https://doi.org/10.18502/jthc.v14i4.2004
Li Z, Yulei J, Yaqing J, Jinmin Z, Xinyong L, Jing G, et al. Protective effects of tetramethylpyrazine analogue Z-11 on cerebral ischemia reperfusion injury. Eur J Pharmacol 2019;844:156-64.
DOI: https://doi.org/10.1016/j.ejphar.2018.11.031
Akpınar H, Nazıroğlu M, Övey İS, Çiğ B, Akpınar O. The neuroprotective action of dexmedetomidine on apoptosis, calcium entry and oxidative stress in cerebral ischemia-induced rats: Contribution of TRPM2 and TRPV1 channels. Sci Rep 2016;6:37196.
DOI: https://doi.org/10.1038/srep37196
Magalhaes JE, Sampaio RP. Migraine and cerebrovascular diseases: Epidemiology, pathophysiological, and clinical considerations. Headache 2018;58:1277-86.
DOI: https://doi.org/10.1111/head.13378
Nguyen H, Aum D, Mashkouri S, Rao G, Vega GJ, Reyes S, et al. Growth factor therapy sequesters inflammation in affording neuroprotection in cerebrovascular diseases. Expert Rev Neurother 2016;16:915-26.
DOI: https://doi.org/10.1080/14737175.2016.1184086
Sharma D, Maslov LN, Singh N, Jaggi AS. Remote ischemic preconditioning-induced neuroprotection in cerebral ischemia-reperfusion injury: Preclinical evidence and mechanisms. Eur J Pharmacol 2020;883:173380.
DOI: https://doi.org/10.1016/j.ejphar.2020.173380
He SF, Jin SY, Wu H, Wang B, Wu YX, Zhang SJ, et al. Morphine preconditioning confers cardioprotection in doxorubicin-induced failing rat hearts via ERK/GSK-3beta pathway independent of PI3K/Akt. Toxicol Appl Pharmacol 2015;288:349-58.
DOI: https://doi.org/10.1016/j.taap.2015.08.007
Fassini A, Scopinho AA, Fortaleza E, Resstel L, Correa F. Kappa-opioid receptors in the medial amygdaloid nucleus modulate autonomic and neuroendocrine responses to acute stress. Eur Neuropsychopharmacol 2021;43:25-37.
DOI: https://doi.org/10.1016/j.euroneuro.2020.11.020
Wojciechowski P, Andrzejewski K, Kaczynska K. Intracerebroventricular neuropeptide FF diminishes the number of apneas and cardiovascular effects produced by opioid receptors' activation. Int J Mol Sci 2020;21:8931.
DOI: https://doi.org/10.3390/ijms21238931
Reardon CE, Kane-Gill SL, Smithburger PL, Dasta JF. Sufentanil sublingual tablet: A new option for acute pain management. Ann Pharmacother 2019;53:1220-6.
DOI: https://doi.org/10.1177/1060028019863144
Stegner D, Klaus V, Nieswandt B. Platelets as modulators of cerebral ischemia/reperfusion injury. Front Immunol 2019;10:2505.
DOI: https://doi.org/10.3389/fimmu.2019.02505
Enzmann G, Kargaran S, Engelhardt B. Ischemia-reperfusion injury in stroke: impact of the brain barriers and brain immune privilege on neutrophil function. Ther Adv Neurol Disord 2018;11:1277015752.
DOI: https://doi.org/10.1177/1756286418794184
Tuttolomondo A, Di Sciacca R, Di Raimondo D, Renda C, Pinto A, Licata G. Inflammation as a therapeutic target in acute ischemic stroke treatment. Curr Top Med Chem 2009;9:1240-60.
DOI: https://doi.org/10.2174/156802609789869619
Parker LC, Luheshi GN, Rothwell NJ, Pinteaux E. IL-1 beta signalling in glial cells in wildtype and IL-1RI deficient mice. Br J Pharmacol 2002;136:312-20.
DOI: https://doi.org/10.1038/sj.bjp.0704715
Kim E, Kim HC, Lee S, Ryu HG, Park YH, Kim JH, et al. Dexmedetomidine confers neuroprotection against transient global cerebral ischemia/reperfusion injury in rats by inhibiting inflammation through inactivation of the TLR-4/NF-kappaB pathway. Neurosci Lett 2017;649:20-7.
DOI: https://doi.org/10.1016/j.neulet.2017.04.011
Hu Q, Wang Q, Han C, Yang Y. Sufentanil attenuates inflammation and oxidative stress in sepsis-induced acute lung injury by downregulating KNG1 expression. Mol Med Rep 2020;22:4298-4306.
DOI: https://doi.org/10.3892/mmr.2020.11526
Bai J, Lyden PD. Revisiting cerebral postischemic reperfusion injury: new insights in understanding reperfusion failure, hemorrhage, and edema. Int J Stroke 2015;10:143-52.
DOI: https://doi.org/10.1111/ijs.12434
Jia SW, Liu XY, Wang SC, Wang YF. Vasopressin hypersecretion-associated brain edema formation in ischemic stroke: Underlying mechanisms. J Stroke Cerebrovasc Dis 2016;25:1289-300.
DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.02.002
Xiao F. Bench to bedside: brain edema and cerebral resuscitation: the present and future. Acad Emerg Med 2002;9:933-46.
DOI: https://doi.org/10.1197/aemj.9.9.933
Rosenberg GA, Yang Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus 2007;22:E4.
DOI: https://doi.org/10.3171/foc.2007.22.5.5
Anik I, Kokturk S, Genc H, Cabuk B, Koc K, Yavuz S, et al. Immunohistochemical analysis of TIMP-2 and collagen types I and IV in experimental spinal cord ischemia-reperfusion injury in rats. J Spinal Cord Med 2011;34:257-64.
DOI: https://doi.org/10.1179/107902611X12972448729648
Rosell A, Cuadrado E, Ortega-Aznar A, Hernandez-Guillamon M, Lo EH, Montaner J. MMP-9-positive neutrophil infiltration is associated to blood-brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke 2008;39:1121-6.
DOI: https://doi.org/10.1161/STROKEAHA.107.500868
Hausburg MA, Banton KL, Roman PE, Salgado F, Baek P, Waxman MJ, et al. Effects of propofol on ischemia-reperfusion and traumatic brain injury. J Crit Care 2020;56:281-287.
DOI: https://doi.org/10.1016/j.jcrc.2019.12.021
Li L, Sun Y, Zhang N, Qiu X, Wang L, Luo Q. By regulating miR-182-5p/BCL10/CYCS, sufentanil reduces the apoptosis of umbilical cord mesenchymal stem cells caused by ropivacaine. Biosci Trends 2019;13:49-57.
DOI: https://doi.org/10.5582/bst.2018.01291
Ethics Approval
The animal experiment was approved by the Zhumadian Central Hospital Experimental Animal Ethics Committee.How to Cite
Wang, Z. ., Du, X. ., Yu, D. ., Yang, Y. ., Ma, G. ., Jia, X. ., & Cheng, L. (2022). Sufentanil alleviates cerebral ischemia-reperfusion injury by inhibiting inflammation and protecting the blood-brain barrier in rats. European Journal of Histochemistry, 66(1). https://doi.org/10.4081/ejh.2022.3328
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