No-reflow after stroke reperfusion therapy: An emerging phenomenon to be explored.

acute ischemic stroke endovascular thrombectomy microvascular disturbance no-reflow phenomenon reperfusion therapy

Journal

CNS neuroscience & therapeutics
ISSN: 1755-5949
Titre abrégé: CNS Neurosci Ther
Pays: England
ID NLM: 101473265

Informations de publication

Date de publication:
Feb 2024
Historique:
revised: 02 01 2024
received: 27 06 2023
accepted: 21 01 2024
medline: 15 2 2024
pubmed: 15 2 2024
entrez: 15 2 2024
Statut: ppublish

Résumé

In the field of stroke thrombectomy, ineffective clinical and angiographic reperfusion after successful recanalization has drawn attention. Partial or complete microcirculatory reperfusion failure after the achievement of full patency of a former obstructed large vessel, known as the "no-reflow phenomenon" or "microvascular obstruction," was first reported in the 1960s and was later detected in both experimental models and patients with stroke. The no-reflow phenomenon (NRP) was reported to result from intraluminal occlusions formed by blood components and extraluminal constriction exerted by the surrounding structures of the vessel wall. More recently, an emerging number of clinical studies have estimated the prevalence of the NRP in stroke patients following reperfusion therapy, ranging from 3.3% to 63% depending on its evaluation methods or study population. Studies also demonstrated its detrimental effects on infarction progress and neurological outcomes. In this review, we discuss the research advances, underlying pathogenesis, diagnostic techniques, and management approaches concerning the no-reflow phenomenon in the stroke population to provide a comprehensive understanding of this phenomenon and offer references for future investigations.

Identifiants

pubmed: 38358074
doi: 10.1111/cns.14631
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14631

Subventions

Organisme : Beijing Natural Science Foundation
ID : JQ22020
Organisme : Beijing Nova Program
ID : Z201100006820143
Organisme : National Natural Science Foundation of China
ID : 81801313
Organisme : National Natural Science Foundation of China
ID : 82001257
Organisme : National Natural Science Foundation of China
ID : 81971114

Informations de copyright

© 2024 The Authors. CNS Neuroscience & Therapeutics published by John Wiley & Sons Ltd.

Références

Campbell BCV, Khatri P. Stroke. Lancet. 2020;396(10244):129-142.
Powers WJ, Rabinstein AA, Ackerson T, et al. Guidelines for the early Management of Patients with Acute Ischemic Stroke: 2019 update to the 2018 guidelines for the early Management of Acute Ischemic Stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2019;50(12):e344-e418.
Suzuki K, Matsumaru Y, Takeuchi M, et al. Effect of mechanical thrombectomy without vs with intravenous thrombolysis on functional outcome among patients with acute ischemic stroke: the SKIP randomized clinical trial. JAMA. 2021;325(3):244-253.
Rubiera M, Garcia-Tornel A, Olivé-Gadea M, et al. Computed tomography perfusion after thrombectomy: an immediate surrogate marker of outcome after recanalization in acute stroke. Stroke. 2020;51(6):1736-1742.
Ng FC, Churilov L, Yassi N, et al. Prevalence and significance of impaired microvascular tissue reperfusion despite macrovascular angiographic reperfusion (No-reflow). Neurology. 2022;98(8):e790-e801.
Ames A 3rd, Wright RL, Kowada M, Thurston JM, Majno G. Cerebral ischemia. II. The no-reflow phenomenon. Am J Pathol. 1968;52(2):437-453.
Deng G, Chu YH, Xiao J, et al. Risk factors, pathophysiologic mechanisms, and potential treatment strategies of futile recanalization after endovascular therapy in acute ischemic stroke. Aging Dis. 2023;14(6):2096-2112.
Nie X, Leng X, Miao Z, Fisher M, Liu L. Clinically ineffective reperfusion after endovascular therapy in acute ischemic stroke. Stroke. 2023;54(3):873-881.
Heusch G. Coronary microvascular obstruction: the new frontier in cardioprotection. Basic Res Cardiol. 2019;114(6):45.
Harrison MJ, Sedal L, Arnold J, Russell RW. No-reflow phenomenon in the cerebral circulation of the gerbil. J Neurol Neurosurg Psychiatry. 1975;38(12):1190-1193.
del Zoppo GJ, Schmid-Schönbein GW, Mori E, Copeland BR, Chang CM. Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke. 1991;22(10):1276-1283.
Little JR, Kerr FW, Sundt TM Jr. Microcirculatory obstruction in focal cerebral ischemia: an electron microscopic investigation in monkeys. Stroke. 1976;7(1):25-30.
Fischer EG, Ames A 3d. Studies on mechanisms of impairment of cerebral circulation following ischemia: effect of hemodilution and perfusion pressure. Stroke. 1972;3(5):538-542.
Kochanek PM, Dutka AJ, Kumaroo KK, Hallenbeck JM. Effects of prostacyclin, indomethacin, and heparin on cerebral blood flow and platelet adhesion after multifocal ischemia of canine brain. Stroke. 1988;19(6):693-699.
Thomas WS, Mori E, Copeland BR, Yu JQ, Morrissey JH, del Zoppo GJ. Tissue factor contributes to microvascular defects after focal cerebral ischemia. Stroke. 1993;24(6):847-853. discussion 847.
Hallenbeck JM, Dutka AJ, Tanishima T, et al. Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke. 1986;17(2):246-253.
Del Zoppo GJ, Copeland BR, Harker LA, et al. Experimental acute thrombotic stroke in baboons. Stroke. 1986;17(6):1254-1265.
Cipolla MJ, Bullinger LV. Reactivity of brain parenchymal arterioles after ischemia and reperfusion. Microcirculation. 2008;15(6):495-501.
Yemisci M, Gursoy-Ozdemir Y, Vural A, Can A, Topalkara K, Dalkara T. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med. 2009;15(9):1031-1037.
Chiang J, Kowada M, Ames A 3rd, Wright RL, Majno G. Cerebral ischemia. III. vascular changes. Am J Pathol. 1968;52(2):455-476.
Hossmann KA. Reperfusion of the brain after global ischemia: hemodynamic disturbances. Shock. 1997;8(2):95-101. discussion 102-3.
Baird AE, Donnan GA, Austin MC, Fitt GJ, Davis SM, McKay WJ. Reperfusion after thrombolytic therapy in ischemic stroke measured by single-photon emission computed tomography. Stroke. 1994;25(1):79-85.
Goyal M, Menon BK, van Zwam W, et al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723-1731.
Zhao W, Wu C, Dornbos D 3rd, et al. Multiphase adjuvant neuroprotection: a novel paradigm for improving acute ischemic stroke outcomes. Brain Circ. 2020;6(1):11-18.
Shin J, Kim YS, Jang HS, et al. Perfusion recovery on TTP maps after endovascular stroke treatment might predict favorable neurological outcomes. Eur Radiol. 2020;30(12):6421-6431.
Cho TH, Nighoghossian N, Mikkelsen IK, et al. Reperfusion within 6 hours outperforms recanalization in predicting penumbra salvage, lesion growth, final infarct, and clinical outcome. Stroke. 2015;46(6):1582-1589.
Ter Schiphorst A, Charron S, Hassen WB, et al. Tissue no-reflow despite full recanalization following thrombectomy for anterior circulation stroke with proximal occlusion: a clinical study. J Cereb Blood Flow Metab. 2021;41(2):253-266.
Liu S, Connor J, Peterson S, Shuttleworth CW, Liu KJ. Direct visualization of trapped erythrocytes in rat brain after focal ischemia and reperfusion. J Cereb Blood Flow Metab. 2002;22(10):1222-1230.
El Amki M, Glück C, Binder N, et al. Neutrophils obstructing brain capillaries are a major cause of No-reflow in ischemic stroke. Cell Rep. 2020;33(2):108260.
Lo EH. A new penumbra: transitioning from injury into repair after stroke. Nat Med. 2008;14(5):497-500.
Mori E, del Zoppo GJ, Chambers JD, Copeland BR, Arfors KE. Inhibition of polymorphonuclear leukocyte adherence suppresses no-reflow after focal cerebral ischemia in baboons. Stroke. 1992;23(5):712-718.
Wong GJ, Yoo B, Liebeskind D, et al. Frequency, determinants, and outcomes of emboli to distal and new territories related to mechanical thrombectomy for acute ischemic stroke. Stroke. 2021;52(7):2241-2249.
Schonfeld MH, Kabiri R, Kniep HC, et al. Sub-angiographic peripheral emboli in high resolution DWI after endovascular recanalization. J Neurol. 2020;267(5):1401-1406.
Rapp JH, Pan XM, Sharp FR, et al. Atheroemboli to the brain: size threshold for causing acute neuronal cell death. J Vasc Surg. 2000;32(1):68-76.
Sporns PB, Krähling H, Psychogios MN, et al. Small thrombus size, thrombus composition, and poor collaterals predict pre-interventional thrombus migration. J Neurointerv Surg. 2021;13(5):409-414.
Chatterjee D, Nagarajan K, Narayan SK, Narasimhan RL. Regional leptomeningeal collateral score by computed tomographic angiography correlates with 3-month clinical outcome in acute ischemic stroke. Brain Circ. 2020;6(2):107-115.
Choudhri TF, Hoh BL, Zerwes HG, et al. Reduced microvascular thrombosis and improved outcome in acute murine stroke by inhibiting GP IIb/IIIa receptor-mediated platelet aggregation. J Clin Invest. 1998;102(7):1301-1310.
Shaik NF, Regan RF, Naik UP. Platelets as drivers of ischemia/reperfusion injury after stroke. Blood Adv. 2021;5(5):1576-1584.
Abumiya T, Fitridge R, Mazur C, et al. Integrin alpha(IIb)beta(3) inhibitor preserves microvascular patency in experimental acute focal cerebral ischemia. Stroke. 2000;31(6):1402-1409. discussion 1409-10.
Okada Y, Copeland BR, Fitridge R, Koziol JA, del Zoppo GJ. Fibrin contributes to microvascular obstructions and parenchymal changes during early focal cerebral ischemia and reperfusion. Stroke. 1994;25(9):1847-1853. discussion 1853-4.
Chen X, Wang J, Ge L, et al. A fibrin targeted molecular imaging evaluation of microvascular no-reflow in acute ischemic stroke. Brain Behav. 2022;12(2):e2474.
Zhang ZG, Chopp M, Goussev A, et al. Cerebral microvascular obstruction by fibrin is associated with upregulation of PAI-1 acutely after onset of focal embolic ischemia in rats. J Neurosci. 1999;19(24):10898-10907.
Grogaard B, Schürer L, Gerdin B, Arfors KE. Delayed hypoperfusion after incomplete forebrain ischemia in the rat. The role of polymorphonuclear leukocytes. J Cereb Blood Flow Metab. 1989;9(4):500-505.
Ritter LS, Orozco JA, Coull BM, McDonagh P, Rosenblum WI. Leukocyte accumulation and hemodynamic changes in the cerebral microcirculation during early reperfusion after stroke. Stroke. 2000;31(5):1153-1161.
Okada Y, Copeland BR, Mori E, Tung MM, Thomas WS, del Zoppo GJ. P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke. 1994;25(1):202-211.
Erdener SE, Tang J, Kılıç K, et al. Dynamic capillary stalls in reperfused ischemic penumbra contribute to injury: a hyperacute role for neutrophils in persistent traffic jams. J Cereb Blood Flow Metab. 2021;41(2):236-252.
Strinitz M, Pham M, März AG, et al. Immune cells invade the collateral circulation during human stroke: prospective replication and extension. Int J Mol Sci. 2021;22(17):9161.
Kollikowski AM, Schuhmann MK, Nieswandt B, Müllges W, Stoll G, Pham M. Local leukocyte invasion during hyperacute human ischemic stroke. Ann Neurol. 2020;87(3):466-479.
Peña-Martínez C, Durán-Laforet V, García-Culebras A, Cuartero MI, Moro MÁ, Lizasoain I. Neutrophil extracellular trap targeting protects against ischemic damage after fibrin-rich thrombotic stroke despite non-reperfusion. Front Immunol. 2022;13:790002.
Perez-de-Puig I, Miró-Mur F, Ferrer-Ferrer M, et al. Neutrophil recruitment to the brain in mouse and human ischemic stroke. Acta Neuropathol. 2015;129(2):239-257.
Zhou SY, Guo ZN, Zhang DH, Qu Y, Jin H. The role of pericytes in ischemic stroke: fom cellular functions to therapeutic targets. Front Mol Neurosci. 2022;15:866700.
Yang S, Jin H, Zhu Y, et al. Diverse functions and mechanisms of pericytes in ischemic stroke. Curr Neuropharmacol. 2017;15(6):892-905.
Hall CN, Reynell C, Gesslein B, et al. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;508(7494):55-60.
Nahirney PC, Reeson P, Brown CE. Ultrastructural analysis of blood-brain barrier breakdown in the peri-infarct zone in young adult and aged mice. J Cereb Blood Flow Metab. 2016;36(2):413-425.
Korte N, Ilkan Z, Pearson CL, et al. The Ca2+−gated channel TMEM16A amplifies capillary pericyte contraction and reduces cerebral blood flow after ischemia. J Clin Invest. 2022;132(9):e154118.
Zhang S, Liao XJ, Wang J, et al. Temporal alterations in pericytes at the acute phase of ischemia/reperfusion in the mouse brain. Neural Regen Res. 2022;17(10):2247-2252.
Hill RA, Tong L, Yuan P, Murikinati S, Gupta S, Grutzendler J. Regional blood flow in the Normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron. 2015;87(1):95-110.
Cipolla MJ, Chan SL, Sweet J, Tavares MJ, Gokina N, Brayden JE. Postischemic reperfusion causes smooth muscle calcium sensitization and vasoconstriction of parenchymal arterioles. Stroke. 2014;45(8):2425-2430.
Hills CP. The ultrastructure of anoxic-Ischaemic lesions in the cerebral cortex of the adult rat brain. Guys Hosp Rep. 1964;113:333-348.
Ito U, Hakamata Y, Kawakami E, Oyanagi K. Temporary [corrected] cerebral ischemia results in swollen astrocytic end-feet that compress microvessels and lead to delayed [corrected] focal cortical infarction. J Cereb Blood Flow Metab. 2011;31(1):328-338.
Mestre H, du T, Sweeney AM, et al. Cerebrospinal fluid influx drives acute ischemic tissue swelling. Science. 2020;367(6483):eaax7171.
Khatri P, Neff J, Broderick JP, Khoury JC, Carrozzella J, Tomsick T. Revascularization end points in stroke interventional trials: recanalization versus reperfusion in IMS-I. Stroke. 2005;36(11):2400-2403.
De Silva DA, Fink JN, Christensen S, et al. Assessing reperfusion and recanalization as markers of clinical outcomes after intravenous thrombolysis in the echoplanar imaging thrombolytic evaluation trial (EPITHET). Stroke. 2009;40(8):2872-2874.
Marks MP, Lansberg MG, Mlynash M, et al. Angiographic outcome of endovascular stroke therapy correlated with MR findings, infarct growth, and clinical outcome in the DEFUSE 2 trial. Int J Stroke. 2014;9(7):860-865.
Wintermark M, Flanders AE, Velthuis B, et al. Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke. 2006;37(4):979-985.
Kosior JC, Buck B, Wannamaker R, et al. Exploring reperfusion following endovascular thrombectomy. Stroke. 2019;50(9):2389-2395.
Yasaka M, O'Keefe GJ, Chambers BR, et al. Streptokinase in acute stroke: effect on reperfusion and recanalization. Australian Streptokinase Trial Study Group. Neurology. 1998;50(3):626-632.
Zaidat OO, Yoo AJ, Khatri P, et al. Recommendations on angiographic revascularization grading standards for acute ischemic stroke: a consensus statement. Stroke. 2013;44(9):2650-2663.
Bivard A, Stanwell P, Levi C, Parsons M. Arterial spin labeling identifies tissue salvage and good clinical recovery after acute ischemic stroke. J Neuroimaging. 2013;23(3):391-396.
Ng FC, Coulton B, Chambers B, Thijs V. Persistently elevated microvascular resistance Postrecanalization. Stroke. 2018;49(10):2512-2515.
Zhao W, Liu R, Yu W, et al. Elevated pulsatility index is associated with poor functional outcome in stroke patients treated with thrombectomy: a retrospective cohort study. CNS Neurosci Ther. 2022;28:1568-1575.
Claassen J, Thijssen DHJ, Panerai RB, et al. Regulation of cerebral blood flow in humans: physiology and clinical implications of autoregulation. Physiol Rev. 2021;101(4):1487-1559.
Chen CL, Wang RK. Optical coherence tomography based angiography [invited]. Biomed Opt Express. 2017;8(2):1056-1082.
Forti RM, Favilla CG, Cochran JM, et al. Transcranial optical monitoring of cerebral hemodynamics in acute stroke patients during mechanical thrombectomy. J Stroke Cerebrovasc Dis. 2019;28(6):1483-1494.
Zhou W, Kholiqov O, Zhu J, et al. Functional interferometric diffusing wave spectroscopy of the human brain. Sci Adv. 2021;7(20):eabe0150.
Pham T, Tgavalekos K, Sassaroli A, Blaney G, Fantini S. Quantitative measurements of cerebral blood flow with near-infrared spectroscopy. Biomed Opt Express. 2019;10(4):2117-2134.
Albers GW, Thijs VN, Wechsler L, et al. Magnetic resonance imaging profiles predict clinical response to early reperfusion: the diffusion and perfusion imaging evaluation for understanding stroke evolution (DEFUSE) study. Ann Neurol. 2006;60(5):508-517.
Soares BP, Tong E, Hom J, et al. Reperfusion is a more accurate predictor of follow-up infarct volume than recanalization: a proof of concept using CT in acute ischemic stroke patients. Stroke. 2010;41(1):e34-e40.
Eilaghi A, Brooks J, d'Esterre C, et al. Reperfusion is a stronger predictor of good clinical outcome than recanalization in ischemic stroke. Radiology. 2013;269(1):240-248.
Horsch AD, Dankbaar JW, Niesten JM, et al. Predictors of reperfusion in patients with acute ischemic stroke. AJNR Am J Neuroradiol. 2015;36(6):1056-1062.
Carbone F, Busto G, Padroni M, et al. Radiologic cerebral reperfusion at 24 h predicts good clinical outcome. Transl Stroke Res. 2019;10(2):178-188.
Luby M, Merino JG, Davis R, et al. Association of Multiple Passes during mechanical thrombectomy with incomplete reperfusion and lesion growth. Cerebrovasc Dis. 2021;51:1-9.
Brodie BR, Webb J, Cox DA, et al. Impact of time to treatment on myocardial reperfusion and infarct size with primary percutaneous coronary intervention for acute myocardial infarction (from the EMERALD trial). Am J Cardiol. 2007;99(12):1680-1686.
Svilaas T, Vlaar PJ, van der Horst IC, et al. Thrombus aspiration during primary percutaneous coronary intervention. N Engl J Med. 2008;358(6):557-567.
Kaesmacher J, Bellwald S, Dobrocky T, et al. Safety and efficacy of intra-arterial urokinase after failed, unsuccessful, or incomplete mechanical thrombectomy in anterior circulation large-vessel occlusion stroke. JAMA Neurol. 2020;77(3):318-326.
Moriguchi A, Maeda M, Mihara K, Aoki T, Matsuoka N, Mutoh S. FK419, a novel nonpeptide GPIIb/IIIa antagonist, restores microvascular patency and improves outcome in the Guinea-pig middle cerebral artery thrombotic occlusion model: comparison with tirofiban. J Cereb Blood Flow Metab. 2005;25(1):75-86.
Yang M, Huo X, Miao Z, Wang Y. Platelet glycoprotein IIb/IIIa receptor inhibitor tirofiban in acute ischemic stroke. Drugs. 2019;79(5):515-529.
Huo X, Raynald R, Jing J, et al. Safety and efficacy of oral antiplatelet for patients who had acute ischaemic stroke undergoing endovascular therapy. Stroke Vasc Neurol. 2020;6(2):230-237.
Zhao W, Che R, Shang S, et al. Low-dose tirofiban improves functional outcome in acute ischemic stroke patients treated with endovascular thrombectomy. Stroke. 2017;48(12):3289-3294.
Hase Y, Okamoto Y, Fujita Y, et al. Cilostazol, a phosphodiesterase inhibitor, prevents no-reflow and hemorrhage in mice with focal cerebral ischemia. Exp Neurol. 2012;233(1):523-533.
Denorme F, Martinod K, Vandenbulcke A, et al. The von Willebrand factor A1 domain mediates thromboinflammation, aggravating ischemic stroke outcome in mice. Haematologica. 2021;106(3):819-828.
Eerenberg ES, Teunissen PFA, van den Born BJ, et al. The role of ADAMTS13 in acute myocardial infarction: cause or consequence? Cardiovasc Res. 2016;111(3):194-203.
Desilles JP, Loyau S, Syvannarath V, et al. Alteplase reduces downstream microvascular thrombosis and improves the benefit of large artery recanalization in stroke. Stroke. 2015;46(11):3241-3248.
Goyal N, Tsivgoulis G, Pandhi A, et al. Impact of pretreatment with intravenous thrombolysis on reperfusion status in acute strokes treated with mechanical thrombectomy. J Neurointerv Surg. 2019;11(11):1073-1079.
Renu A, Millán M, San Román L, et al. Effect of intra-arterial alteplase vs placebo following successful thrombectomy on functional outcomes in patients with large vessel occlusion acute ischemic stroke: the CHOICE randomized clinical trial. JAMA. 2022;327(9):826-835.
Zinkstok SM, Roos YB. Early administration of aspirin in patients treated with alteplase for acute ischaemic stroke: a randomised controlled trial. Lancet. 2012;380(9843):731-737.
Hartmann DA, Berthiaume AA, Grant RI, et al. Brain capillary pericytes exert a substantial but slow influence on blood flow. Nat Neurosci. 2021;24(5):633-645.
Guo RB, Dong YF, Yin Z, et al. Iptakalim improves cerebral microcirculation in mice after ischemic stroke by inhibiting pericyte contraction. Acta Pharmacology Sin. 2021;43:1349-1359.
Gaudin A, Yemisci M, Eroglu H, et al. Squalenoyl adenosine nanoparticles provide neuroprotection after stroke and spinal cord injury. Nat Nanotechnol. 2014;9(12):1054-1062.
Terpolilli NA, Kim SW, Thal SC, et al. Inhalation of nitric oxide prevents ischemic brain damage in experimental stroke by selective dilatation of collateral arterioles. Circ Res. 2012;110(5):727-738.
Jaffe R, Dick A, Strauss BH. Prevention and treatment of microvascular obstruction-related myocardial injury and coronary no-reflow following percutaneous coronary intervention: a systematic approach. JACC Cardiovasc Interv. 2010;3(7):695-704.
Fraser JF, Maniskas M, Trout A, et al. Intra-arterial verapamil post-thrombectomy is feasible, safe, and neuroprotective in stroke. J Cereb Blood Flow Metab. 2017;37(11):3531-3543.
Lee H, Yun H, Ding Y. Timing is everything: exercise therapy and remote ischemic conditioning for acute ischemic stroke patients. Brain Circ. 2021;7(3):178-186.
Wills M, Ding Y. Mini-review (part II): a clinical consideration on exercise and ischemic conditioning in stroke rehabilitation. Brain Circ. 2021;7(4):225-229.
Pico F, Lapergue B, Ferrigno M, et al. Effect of in-hospital remote ischemic Perconditioning on BRAIN infarction growth and clinical outcomes in patients with acute ischemic stroke: the RESCUE BRAIN randomized clinical trial. JAMA Neurol. 2020;77(6):725-734.
Wu D, Chen J, Zhang X, Ilagan R, Ding Y, Ji X. Selective therapeutic cooling: to maximize benefits and minimize side effects related to hypothermia. J Cereb Blood Flow Metab. 2022;42(1):213-215.
Eren F, Yilmaz S. Neuroprotective approach in acute ischemic stroke: a systematic review of clinical and experimental studies. Brain Circ. 2022;8(4):172-179.
Hale SL, Herring MJ, Kloner RA. Delayed treatment with hypothermia protects against the no-reflow phenomenon despite failure to reduce infarct size. J Am Heart Assoc. 2013;2(1):e004234.
Dai W, Hale S, Kloner RA. Delayed therapeutic hypothermia protects against the myocardial no-reflow phenomenon independently of myocardial infarct size in a rat ischemia/reperfusion model. Int J Cardiol. 2017;236:400-404.
Li F, Gao J, Kohls W, Geng X, Ding Y. Perspectives on benefit of early and prereperfusion hypothermia by pharmacological approach in stroke. Brain Circ. 2022;8(2):69-75.
Schaeffer S, Iadecola C. Revisiting the neurovascular unit. Nat Neurosci. 2021;24(9):1198-1209.
Galli M, Niccoli G, de Maria G, et al. Coronary microvascular obstruction and dysfunction in patients with acute myocardial infarction. Nat Rev Cardiol. 2023. doi:10.1038/s41569-023-00953-4. Online ahead of print.
Bulluck H, Dharmakumar R, Arai AE, Berry C, Hausenloy DJ. Cardiovascular magnetic resonance in acute ST-segment-elevation myocardial infarction: recent advances, controversies, and future directions. Circulation. 2018;137(18):1949-1964.
Rezkalla SH, Stankowski RV, Hanna J, Kloner RA. Management of No-Reflow Phenomenon in the catheterization laboratory. JACC Cardiovasc Interv. 2017;10(3):215-223.

Auteurs

Milan Jia (M)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing, China.

Feiyang Jin (F)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing, China.

Sijie Li (S)

Department of Emergency, Xuanwu Hospital, Capital Medical University, Beijing, China.

Changhong Ren (C)

Beijing Key Laboratory of Hypoxic Conditioning Translational Medicine, Xuanwu Hospital, Capital Medical University, Beijing, China.

Mangal Ruchi (M)

Department of Neurosurgery, Wayne State University School of Medicine, Detroit, Michigan, USA.

Yuchuan Ding (Y)

Department of Neurosurgery, Wayne State University School of Medicine, Detroit, Michigan, USA.

Wenbo Zhao (W)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing, China.

Xunming Ji (X)

Department of Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, China.

Classifications MeSH