Spreading Depolarization Waves in Neurological Diseases: A Short Review about its Pathophysiology and Clinical Relevance

Author(s): Yağmur Çetin Taş, İhsan Solaroğlu, Yasemin Gürsoy-Özdemir*.

Journal Name: Current Neuropharmacology

Volume 17 , Issue 2 , 2019

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Graphical Abstract:


Lesion growth following acutely injured brain tissue after stroke, subarachnoid hemorrhage and traumatic brain injury is an important issue and a new target area for promising therapeutic interventions. Spreading depolarization or peri-lesion depolarization waves were demonstrated as one of the significant contributors of continued lesion growth. In this short review, we discuss the pathophysiology for SD forming events and try to list findings detected in neurological disorders like migraine, stroke, subarachnoid hemorrhage and traumatic brain injury in both human as well as experimental studies. Pharmacological and non-pharmacological treatment strategies are highlighted and future directions and research limitations are discussed.

Keywords: Spreading Depression, Peri-infarct depolarization, Stroke, Subarachnoid hemorrhage, traumatic brain injury, migraine.

Leão, A. Spreading depression of activity in the cerebral cortex. J. Neurophysiol., 1944, 7(6), 359-390.
Hartings, J.A.; Shuttleworth, C.W.; Kirov, S.A.; Ayata, C.; Hinzman, J.M.; Foreman, B.; Andrew, R.D.; Boutelle, M.G.; Brennan, K.C.; Carlson, A.P.; Dahlem, M.A.; Drenckhahn, C.; Dohmen, C.; Fabricius, M.; Farkas, E.; Feuerstein, D.; Graf, R.; Helbok, R.; Lauritzen, M.; Major, S.; Oliveira-Ferreira, A.I.; Richter, F.; Rosenthal, E.S.; Sakowitz, O.W.; Sánchez-Porras, R.; Santos, E.; Schöll, M.; Strong, A.J.; Urbach, A.; Westover, M.B.; Winkler, M.K.; Witte, O.W.; Woitzik, J.; Dreier, J.P. The continuum of spreading depolarizations in acute cortical lesion development: Examining Leão’s legacy. J. Cereb. Blood Flow Metab., 2016.
Dreier, J. P.; Fabricius, M.; Ayata, C.; Sakowitz, O. W.; William Shuttleworth, C.; Dohmen, C.; Graf, R.; Vajkoczy, P.; Helbok, R.; Suzuki, M.; Schiefecker, A.J.; Major, S.; Winkler, M. K.; Kang, E.-J.; Milakara, D.; Oliveira-Ferreira, A.I.; Reiffurth, C.; Revankar, G. S.; Sugimoto, K.; Dengler, N. F.; Hecht, N.; Foreman, B.; Feyen, B.; Kondziella, D.; Friberg, C. K.; Piilgaard, H.; Rosenthal, E. S.; Westover, M. B.; Maslarova, A.; Santos, E.; Hertle, D.; Sánchez-Porras, R.; Jewell, S. L.; Balança, B.; Platz, J.; Hinzman, J. M.; Lückl, J.; Schoknecht, K.; Schöll, M.; Drenckhahn, C.; Feuerstein, D.; Eriksen, N.; Horst, V.; Bretz, J.S.; Jahnke, P.; Scheel, M.; Bohner, G.; Rostrup, E.; Pakkenberg, B.; Heinemann, U.; Claassen, J.; Carlson, A. P.; Kowoll, C.M.; Lublinsky, S.; Chassidim, Y.; Shelef, I.; Friedman, A.; Brinker, G.; Reiner, M.; Kirov, S. A.; Andrew, R. D.; Farkas, E.; Güresir, E.; Vatter, H.; Chung, L. S.; Brennan, K.; Lieutaud, T.; Marinesco, S.; Maas, A. I.; Sahuquillo, J.; Dahlem, M. A.; Richter, F.; Herreras, O.; Boutelle, M. G.; Okonkwo, D. O.; Bullock, M. R.; Witte, O. W.; Martus, P.; van den Maagdenberg, A. M.; Ferrari, M. D.; Dijkhuizen, R. M.; Shutter, L. A.; Andaluz, N.; Schulte, A. P.; MacVicar, B.; Watanabe, T.; Woitzik, J.; Lauritzen, M.; Strong, A. J.; Hartings, J. A. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group. J. Cereb. Blood Flow Metab.,2016, 0271678X16654496
Lashley, K.S. Richter (in Bumke, O., and Foerster, O.; (J.; Poliak, S.; Lorente de Nó, R.; Filimonoff, I.N.; Poppelreuter, W.; Lashley, K.S.; Klüver, H.; Lorente de Nó, R.; Lashley, K.S.; Fuchs, W. Patterns of cerebral integration indicated by the scotomas of migraine. Arch. Neurol. Psychiatry, 1941, 46 (2), 331.
[http://dx.doi.org/10. 1001/archneurpsyc.1941.02280200137007]
Leão, A.; Morison, R.S. Propagation of spreading cortical depression. J. Neurophysiol., 1945, 8, 33-45.
[http://dx.doi.org/10.1097/ 00005053-194511000-00029]
Milner, P.M. Note on a possible correspondence between the scotomas of migraine and spreading depression of Leão. Electroencephalogr. Clin. Neurophysiol., 1958, 10(4), 705.
Hadjikhani, N.; Sanchez, M.; Wu, O.; Schwartz, D.; Bakker, D.; Fischl, B.; Kwong, K.K.; Cutrer, F.M.; Rosen, B.R.; Tootell, R.B.H.; Sorensen, A.G.; Moskowitz, M.A. Mechanisms of migraine aura revealed by functional MRI in human visual cortex. Proc. Natl. Acad. Sci. USA, 2001, 98(8), 4687-4692.
Olesen, J.; Larsen, B.; Lauritzen, M. Focal hyperemia followed by spreading oligemia and impaired activation of rCBF in classic migraine., Ann. Neurol.,1981, 9(4), 344-352.
[http://dx.doi.org/10. 1002/ana.410090406]
Lauritzen, M. Pathophysiology of the migraine aura. The spreading depression theory. Brain, 1994, 117(Pt 1 (1), 199-210.
Ayata, C.; Lauritzen, M. Spreading depression, spreading depolarizations, and the cerebral vasculature. Physiol. Rev., 2015, 95(3), 953-993.
Bolay, H.; Reuter, U.; Dunn, A.K.; Huang, Z.; Boas, D. a; Moskowitz, M. a. Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model. Nat. Med., 2002, 8(2), 136-142.
Woitzik, J.; Hecht, N.; Pinczolits, A.; Sandow, N.; Major, S.; Winkler, M.K.L.; Weber-Carstens, S.; Dohmen, C.; Graf, R.; Strong, A. J.; Dreier, J.P.; Vajkoczy, P. Propagation of cortical spreading depolarization in the human cortex after malignant stroke., Neurology,2013, 80(12), 1095-1102.
[http://dx.doi.org/10.1212/wnl.0b013 e3182886932]
Hartings, J.A. Spreading depolarization monitoring in neurocritical care of acute brain injury. Curr. Opin. Crit. Care, 2017, 23(2), 1.
Kraig, R.P.; Nicholson, C. Extracellular ionic variations during spreading depression. Neuroscience, 1978, 3(11), 1045-1059.
Larrosa, B.; Pastor, J.; López-Aguado, L.; Herreras, O. A role for glutamate and glia in the fast network oscillations preceding spreading depression. Neuroscience, 2006, 141(2), 1057-1068.
Vyskočil, F.; Kříž, N.; Bureš, J. Potassium-selective microelectrodes used for measuring the extracellular brain potassium during spreading depression and anoxic depolarization in rats., Brain Res., 1972, 39(1), 255-259. (72) 90802-5.
Grafstein, B. Mechanism of spreading spreading depression. J. Neurophysiol., 1956, 19(2), 154-171.
Kunkler, P.E. Optical current source density analysis in Hippocampal organotypic culture shows that spreading depression Occurs with uniquely reversing currents. J. Neurosci., 2005, 25(15), 3952-3961.
Lauritzen, M.; Rice, M.E.; Okada, Y.; Nicholson, C. Quisqualate, kainate and NMDA can initiate spreading depression in the turtle cerebellum. Brain Res., 1988, 475(2), 317-327.
Somjen, G.G. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev., 2001, 81(3), 1065-1096.
Mutch, W.A.; Hansen, A.J. Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J. Cereb. Blood Flow Metab., 1984, 4(1), 17-27.
Kow, L.M.; van Harreveld, A. Ion and water movements in isolated chicken retinas during spreading depression. Neurobiology, 1972, 2(2), 61-69.
Takano, T.; Tian, G-F.; Peng, W.; Lou, N.; Lovatt, D.; Hansen, A.J.; Kasischke, K.A.; Nedergaard, M. Cortical spreading depression causes and coincides with tissue hypoxia. Nat. Neurosci., 2007, 10(6), 754-762.
Zhou, N.; Gordon, G. R. J.; Feighan, D.; MacVicar, B. A. Transient swelling, acidification, and mitochondrial depolarization occurs in neurons but not astrocytes during spreading depression., Cereb. Cortex, 2010, 20(11), 2614-2624.
[http://dx.doi.org/10.1093/cercor/ bhq018]
Takano, T.; Kang, J.; Jaiswal, J.K.; Simon, S.M.; Lin, J.H-C.; Yu, Y.; Li, Y.; Yang, J.; Dienel, G.; Zielke, H.R.; Nedergaard, M. Receptor-mediated glutamate release from volume sensitive channels in astrocytes. Proc. Natl. Acad. Sci. USA, 2005, 102(45), 16466-16471.
Van Harreveld, A.; Fifková, E. Glutamate release from the retina during spreading depression. J. Neurobiol., 1970, 2(1), 13-29.
Fabricius, M.; Jensen, L.H.; Lauritzen, M. Microdialysis of interstitial amino acids during spreading depression and anoxic depolarization in rat neocortex. Brain Res., 1993, 612(1-2), 61-69.
Rungta, R.L.; Choi, H.B.; Tyson, J.R.; Malik, A.; Dissing-Olesen, L.; Lin, P.J.C.; Cain, S.M.; Cullis, P.R.; Snutch, T.P.; MacVicar, B.A. The cellular mechanisms of neuronal swelling underlying cytotoxic edema., Cell, 2015, 161(3), 610-621.
[http://dx.doi.org/10. 1016/j.cell.2015.03.029]
Gursoy-Ozdemir, Y.; Qiu, J.; Matsuoka, N.; Bolay, H.; Bermpohl, D.; Jin, H.; Wang, X.; Rosenberg, G.A.; Lo, E.H.; Moskowitz, M.A. Cortical spreading depression activates and upregulates MMP-9., J. Clin. Invest.,2004, 113(10), 1447-1455
[http://dx.doi.org/10. 1172/jci200421227]
Cunningham, L.A.; Wetzel, M.; Rosenberg, G.A. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia, 2005, 50(4), 329-339.
Jander, S.; Schroeter, M.; Peters, O.; Witte, O.W.; Stoll, G. Cortical spreading depression induces proinflammatory cytokine gene expression in the rat brain. J. Cereb. Blood Flow Metab., 2001, 21(3), 218-225.
Sharp, F.R.; Lu, A.; Tang, Y.; Millhorn, D.E. Multiple molecular penumbras after focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2000, 20(7), 1011-1032.
Fabricius, M.; Akgoren, N.; Lauritzen, M. Arginine-nitric oxide pathway and cerebrovascular regulation in cortical spreading depression. Am. J. Physiol., 1995, 269(1 Pt 2), H23-H29.
Piilgaard, H.; Lauritzen, M. Persistent increase in oxygen consumption and impaired neurovascular coupling after spreading depression in rat neocortex. J. Cereb. Blood Flow Metab., 2009, 29(9), 1517-1527.
Dreier, J.P.; Körner, K.; Ebert, N.; Görner, A.; Rubin, I.; Back, T.; Lindauer, U.; Wolf, T.; Villringer, A.; Einhäupl, K.M.; Lauritzen, M.; Dirnagl, U. Nitric oxide scavenging by hemoglobin or nitric oxide synthase inhibition by N-nitro-L-arginine induces cortical spreading ischemia when K+ is increased in the subarachnoid space. J. Cereb. Blood Flow Metab., 1998, 18(9), 978-990.
Dreier, J.P.; Ebert, N.; Priller, J.; Megow, D.; Lindauer, U.; Klee, R.; Reuter, U.; Imai, Y.; Einhäupl, K.M.; Victorov, I.; Dirnagl, U. Products of hemolysis in the subarachnoid space inducing spreading ischemia in the cortex and focal necrosis in rats: a model for delayed ischemic neurological deficits after subarachnoid hemorrhage?, J. Neurosurg., 2000, 93(4), 658-666.
[http://dx.doi.org/10. 3171/jns.2000.93.4.0658]
Strong, A.J.; Anderson, P.J.; Watts, H.R.; Virley, D.J.; Lloyd, A.; Irving, E.A.; Nagafuji, T.; Ninomiya, M.; Nakamura, H.; Dunn, A.K.; Graf, R. Peri-infarct depolarizations lead to loss of perfusion in ischaemic gyrencephalic cerebral cortex. Brain, 2007, 130(4), 995-1008.
von Bornstädt, D.; Houben, T.; Seidel, J.L.; Zheng, Y.; Dilekoz, E.; Qin, T.; Sandow, N.; Kura, S.; Eikermann-Haerter, K.; Endres, M.; Boas, D.A.; Moskowitz, M.A.; Lo, E.H.; Dreier, J.P.; Woitzik, J.; Sakadžić, S.; Ayata, C. Supply-demand mismatch transients in susceptible peri-infarct hot zones explain the origins of spreading injury depolarizations. Neuron, 2015, 85(5), 1117-1131.
Shinohara, M.; Dollinger, B.; Brown, G.; Rapoport, S.; Sokoloff, L. Cerebral glucose utilization: local changes during and after recovery from spreading cortical depression. Science (80-.), 1979, 203(4376), 188-190.
LaManna, J.C.; Rosenthal, M. Effect of ouabain and phenobarbital on oxidative metabolic activity associated with spreading cortical depression in cats. Brain Res., 1975, 88(1), 145-149.
Kislin, M.; Sword, J.; Fomitcheva, I.V.; Croom, D.; Pryazhnikov, E.; Lihavainen, E.; Toptunov, D.; Rauvala, H.; Ribeiro, A.S.; Khiroug, L.; Kirov, S.A. Reversible disruption of neuronal mitochondria by ischemic and traumatic injury revealed by quantitative two-photon imaging in the neocortex of anesthetized mice., J. Neurosci.2017, 37(2), 333-348. http://dx.doi.org/10.1523/jneurosci. 1510-16.2017.
Zhou, N.; Rungta, R.L.; Malik, A.; Han, H.; Wu, D.C.; MacVicar, B.A. Regenerative glutamate release by presynaptic NMDA receptors contributes to spreading depression. J. Cereb. Blood Flow Metab., 2013, 33(10), 1582-1594.
Iadecola, C. Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat. Rev. Neurosci., 2004, 5(5), 347-360.
Steffensen, A.B.; Sword, J.; Croom, D.; Kirov, S. a; MacAulay, N. chloride cotransporters as a molecular mechanism underlying spreading depolarization-induced dendritic beading. J. Neurosci., 2015, 35(35), 12172-12187.
Lauritzen, M.; Hansen, A.J.; Kronborg, D.; Wieloch, T. Cortical spreading depression is associated with arachidonic acid accumulation and preservation of energy charge. J. Cereb. Blood Flow Metab., 1990, 10(1), 115-122.
Parkin, M.M.; Hopwood, S.S.; Jones, D.A.; Hashemi, P.P.; Landolt, H.H.; Fabricius, M.M.; Lauritzen, M.M.; Boutelle, M.G.M.G.; Strong, A.J. Dynamic changes in brain glucose and lactate in pericontusional areas of the human cerebral cortex, monitored with rapid sampling on-line microdialysis: relationship with depolarisation-like events. J. Cereb. Blood Flow Metab., 2005, 25(3), 402-413.
Feuerstein, D.; Manning, A.; Hashemi, P.; Bhatia, R.; Fabricius, M.; Tolias, C.; Pahl, C.; Ervine, M.; Strong, A.J.; Boutelle, M.G. Dynamic metabolic response to multiple spreading depolarizations in patients with acute brain injury: an online microdialysis study. J. Cereb. Blood Flow Metab., 2010, 30(7), 1343-1355.
Ayata, C.; Shin, H. K.; Salomone, S.; Ozdemir-Gursoy, Y.; Boas, D.A.; Dunn, A.K.; Moskowitz, M.A. Pronounced hypoperfusion during spreading depression in mouse cortex. J. Cereb. Blood Flow Metab.,2004, 24(10), 1172-1182 http://dx.doi.org/10.1097/01. wcb.0000137057.92786.f3.
World Health Organization. Neurological disorders: a public health approach. Neurol. Disord. Public Heal. Challenges,2006, 41-176. http://dx.doi.org/10.1001/archneurol.2007.19.
Lauritzen, M. Cortical spreading depression in migraine. Cephalalgia, 2001, 21(7), 757-760.
Largo, C.; Ibarz, J.M.; Herreras, O. Effects of the gliotoxin fluorocitrate on spreading depression and glial membrane potential in rat brain in situ. J. Neurophysiol., 1997, 78(1), 295-307.
Moskowitz, M.A.; Reinhard, J.F.; Romero, J.; Melamed, E.; Pettibone, D.J. Neurotransmitters and the fifth cranial nerve: is there a relation to the headache phase of migraine? Lancet (London, England), 1979, 2(8148), 883-885.
Karatas, H.; Erdener, S.E.; Gursoy-Ozdemir, Y.; Lule, S.; Eren-Koçak, E.; Sen, Z.D.; Dalkara, T. Spreading depression triggers headache by activating neuronal Panx1 channels. Science, 2013, 339(6123), 1092-1095.
Takizawa, T.; Shibata, M.; Kayama, Y.; Toriumi, H.; Ebine, T.; Koh, A.; Shimizu, T.; Suzuki, N. Temporal profiles of high-mobility group box 1 expression levels after cortical spreading depression in mice. Cephalalgia, 2016, 36(1), 44-52.
Risher, W.C.; Ard, D.; Yuan, J.; Kirov, S.A. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J. Neurosci., 2010, 30(29), 9859-9868.
Zaidi, N.; Maurer, A.; Nieke, S.; Kalbacher, H. Cathepsin, D. A cellular roadmap. Biochem. Biophys. Res. Commun., 2008, 376(1), 5-9.
Barrett, C.F.; van den Maagdenberg, A.M.J.M.; Frants, R.R.; Ferrari, M.D. Familial hemiplegic migraine. Adv. Genet., 2008, 63, 57-83.
Hansen, J.M. Familial hemiplegic migraine. Dan. Med. Bull., 2010, 57(9), B4183.
Van Den Maagdenberg, A.M.J.M.; Pizzorusso, T.; Kaja, S.; Terpolilli, N.; Shapovalova, M.; Hoebeek, F.E.; Barrett, C.F.; Gherardini, L.; Van De Ven, R.C.G.; Todorov, B.; Broos, L.A.M.; Tottene, A.; Gao, Z.; Fodor, M.; De Zeeuw, C.I.; Frants, R.R.; Plesnila, N.; Plomp, J.J.; Pietrobon, D.; Ferrari, M.D. High cortical spreading depression susceptibility and migraine-associated symptoms in Ca(v)2.1 S218L mice. Ann. Neurol., 2010, 67(1), 85-98.
Eikermann-Haerter, K.; Yuzawa, I.; Qin, T.; Wang, Y.; Baek, K.; Kim, Y.R.; Hoffmann, U.; Dilekoz, E.; Waeber, C.; Ferrari, M.D.; van den Maagdenberg, A.M.J.M.; Moskowitz, M.A.; Ayata, C. Enhanced subcortical spreading depression in familial hemiplegic migraine Type 1 mutant mice. J. Neurosci., 2011, 31(15), 5755-5763.
Capuani, C.; Melone, M.; Tottene, A.; Bragina, L.; Crivellaro, G.; Santello, M.; Casari, G.; Conti, F.; Pietrobon, D. Defective glutamate and K+ clearance by cortical astrocytes in familial hemiplegic migraine type 2. EMBO Mol. Med., 2016, 8(8), 967-986.
Ferrari, M.D.; Klever, R.R.; Terwindt, G.M.; Ayata, C.; van den Maagdenberg, A.M.J.M. Migraine pathophysiology: lessons from mouse models and human genetics. Lancet Neurol., 2015, 14(1), 65-80.
Timm, F.P.; Houle, T.T.; Grabitz, S.D.; Lihn, A-L.; Stokholm, J.B.; Eikermann-Haerter, K.; Nozari, A.; Kurth, T.; Eikermann, M. Migraine and risk of perioperative ischemic stroke and hospital readmission: hospital based registry study. BMJ, 2017, 356, i6635.
Sacco, S.; Ornello, R.; Ripa, P.; Tiseo, C.; Degan, D.; Pistoia, F.; Carolei, A. Migraine and risk of ischaemic heart disease: A systematic review and meta-analysis of observational studies., Eur. J. Neurol.,2015, 22(6), 1001-1011. http://dx.doi.org/10.1111/ene. 12701.
Schain, A.J.; Melo-Carrillo, A.; Strassman, A.M.; Burstein, R.; Melo, A.; Strassman, A.M.; Burstein, R. Cortical spreading depression closes the paravascular space and impairs glymphatic flow: Implications for migraine headache. J. Neurosci., 2017, 37(11), 3390-16.
Branston, N.M.; Strong, A.J.; Symon, L. Extracellular potassium activity, evoked potential and tissue blood flow., Relationships during progressive ischaemia in baboon cerebral cortex. J. Neurol. Sci.,1977, 32(3), 305-321. http://dx.doi.org/10.1016/0022-510x (77)90014-4.
Strong, A.J.; Venables, G.S.; Gibson, G. The cortical ischaemic penumbra associated with occlusion of the middle cerebral artery in the cat: 1. Topography of changes in blood flow, potassium ion activity, and EEG. J. Cereb. Blood Flow Metab., 1983, 3(1), 86-96.
Dreier, J.P.; Woitzik, J.; Fabricius, M.; Bhatia, R.; Major, S.; Drenckhahn, C.; Lehmann, T.N.; Sarrafzadeh, A.; Willumsen, L.; Hartings, J.A.; Sakowitz, O.W.; Seemann, J.H.; Thieme, A.; Lauritzen, M.; Strong, A.J. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain, 2006, 129(12), 3224-3237.
Nedergaard, M.; Astrup, J. Infarct rim: effect of hyperglycemia on direct current potential and [14C]2-deoxyglucose phosphorylation. J. Cereb. Blood Flow Metab., 1986, 6(5), 607-615.
Astrup, J.; Siesjö, B.K.; Symon, L. Thresholds in cerebral ischemia - the ischemic penumbra. Stroke, 1981, 12(6), 723-725.
Hossmann, K.A. Periinfarct depolarizations. Cerebrovasc. Brain Metab. Rev., 1996, 8(3), 195-208.
Mies, G.; Iijima, T.; Hossmann, K.A. Correlation between peri-infarct DC shifts and ischaemic neuronal damage in rat. Neuroreport, 1993, 4(6), 709-711.
Back, T.; Ginsberg, M.D.; Dietrich, W.D.; Watson, B.D. Induction of spreading depression in the ischemic hemisphere following experimental middle cerebral artery occlusion: effect on infarct morphology. J. Cereb. Blood Flow Metab., 1996, 16(2), 202-213.
Busch, E.; Gyngell, M.L.; Eis, M.; Hoehn-Berlage, M.; Hossmann, K.A. Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J. Cereb. Blood Flow Metab., 1996, 16(6), 1090-1099.
Takano, K.; Latour, L.L.; Formato, J.E.; Carano, R. A.D.; Helmer, K.G.; Hasegawa, Y.; Sotak, C.H.; Fisher, M. The role of spreading depression in focal ischemia evaluated bv dffusion mapping., Ann. Neurol.,1996, 39(3), 308-318. http://dx.doi.org/10.1002/ana. 410390307.
Fabricius, M.; Fuhr, S.; Willumsen, L.; Dreier, J.P.; Bhatia, R.; Boutelle, M.G.; Hartings, J.A.; Bullock, R.; Strong, A.J.; Lauritzen, M. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin. Neurophysiol., 2008, 119(9), 1973-1984.
Fabricius, M.; Fuhr, S.; Bhatia, R.; Boutelle, M.; Hashemi, P.; Strong, A.J.; Lauritzen, M. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain, 2006, 129(3), 778-790.
Dohmen, C.; Sakowitz, O.W.; Fabricius, M.; Bosche, B.; Reithmeier, T.; Ernestus, R-I.; Brinker, G.; Dreier, J.P.; Woitzik, J.; Strong, A.J.; Graf, R. Co-Operative study of brain injury depolarisations (COSBID). Spreading depolarizations occur in human ischemic stroke with high incidence. Ann. Neurol., 2008, 63(6), 720-728.
Lauritzen, M.; Jørgensen, M.B.; Diemer, N.H.; Gjedde, A. Hansen, A.J. Persistent oligemia of rat cerebral cortex in the wake of spreading depression. Ann. Neurol., 1982, 12(5), 469-474.
Strong, A.J.; Gibson, G.; Miller, S.A.; Venables, G.S. Changes in vascular and metabolic reactivity as Indices of ischaemia in the penumbra. J. Cereb. Blood Flow Metab., 1988, 8(1), 79-88.
Kocher, M. Metabolic and hemodynamic activation of postischemic rat brain by cortical spreading depression. J. Cereb. Blood Flow Metab., 1990, 10(4), 564-571.
Mayevsky, A.; Weiss, H. R. Cerebral blood flow and oxygen consumption in cortical spreading depression., J. Cereb. Blood Flow Metab.,1991, 11(5), 829-836.
[http://dx.doi.org/10.1038/jcbfm. 1991.142]
Shin, H.K.; Dunn, A.K.; Jones, P.B.; Boas, D.A.; Moskowitz, M.A.; Ayata, C. Vasoconstrictive neurovascular coupling during focal ischemic depolarizations. J. Cereb. Blood Flow Metab., 2006, 26(8), 1018-1030.
Pinczolits, A.; Zdunczyk, A.; Dengler, N. F. F.; Hecht, N.; Kowoll, C. M.M.; Dohmen, C.; Graf, R.; Winkler, M. K.K.; Major, S.
Hartings, J.A.A.; Dreier, J.P.P.; Vajkoczy, P.; Woitzik, J. Standard-sampling microdialysis and spreading depolarizations in patients with malignant hemispheric stroke. J. Cereb. Blood Flow Metab., 2017, 37(5), 1896-1905.
[http://dx.doi.org/10.1177/ 0271678x17699629]
Rogers, M.L.L.; Leong, C.L.L.; Gowers, S.A.A.; Samper, I.C.C.; Jewell, S.L.L.; Khan, A.; McCarthy, L.; Pahl, C.; Tolias, C.M.M.; Walsh, D.C.C.; Strong, A.J.J.; Boutelle, M.G.G. Simultaneous monitoring of potassium, glucose and lactate during spreading depolarization in the injured human brain - Proof of principle of a novel real-time neurochemical analysis system, continuous online microdialysis. J. Cereb. Blood Flow Metab., 2017, 37(5), 1883-1895.
Lapilover, E.G.; Lippmann, K.; Salar, S.; Maslarova, A.; Dreier, J.P.; Heinemann, U.; Friedman, A. Peri-infarct blood-brain barrier dysfunction facilitates induction of spreading depolarization associated with epileptiform discharges. Neurobiol. Dis., 2012, 48(3), 495-506.
Dreier, J.P.; Major, S.; Pannek, H.W.H-W.; Woitzik, J.; Scheel, M.; Wiesenthal, D.; Martus, P.; Winkler, M.K.L.; Hartings, J.A.; Fabricius, M.; Speckmann, E-J.E.J.; Gorji, A. COSBID study group. Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain, 2012, 135(1), 259-275.
Fonarow, G.C.; Reeves, M.J.; Zhao, X.; Olson, D.M.; Smith, E.E.; Saver, J.L.; Schwamm, L.H. Age-related differences in characteristics, Performance measures, treatment trends, and outcomes in patients eith ischemic stroke. Circulation, 2010, 121(7), 879-891.
Knoflach, M.; Matosevic, B.; Rücker, M.; Furtner, M.; Mair, A.; Wille, G.; Zangerle, A.; Werner, P.; Ferrari, J.; Schmidauer, C.; Seyfang, L.; Kiechl, S.; Willeit, J. Austrian Stroke Unit Registry Collaborators. F. The A. S. U. R. Functional recovery after ischemic stroke--a matter of age: data from the Austrian Stroke Unit Registry. Neurology, 2012, 78(4), 279-285.
Ay, H.; Arsava, E.M.; Koroshetz, W.J.; Sorensen, A.G. Middle cerebral artery infarcts encompassing the insula are more prone to growth. Stroke, 2008, 39(2), 373-378.
Copen, W.A.A.; Schwamm, L.H.H.; González, R.G.G.; Wu, O.; Harmath, C.B.B.; Schaefer, P.W.W.; Koroshetz, W.J.J.; Sorensen, A.G.G. Ischemic stroke: Effects of etiology and patient age on the time course of the core apparent diffusion coefficient. Radiology, 2001, 221(1), 27-34.
Ungvari, Z.; Kaley, G.; de Cabo, R.; Sonntag, W.E.; Csiszar, A. Mechanisms of vascular aging: new perspectives. J. Gerontol. Ser. A Biol. Sci. Med. Sci., 2010, 65A(10), 1028-1041.
Weimar, C.; König, I.R.; Kraywinkel, K.; Ziegler, A.; Diener, H.C. German stroke study collaboration. Age and national institutes of health stroke scale score within 6 hours after onset are accurate predictors of outcome after cerebral ischemia: Development and external validation of prognostic models. Stroke, 2003, 35(1), 158-162.
Clark, D.; Institoris, Á.; Kozák, G.; Bere, Z.; Tuor, U.; Farkas, E.; Bari, F. Impact of aging on spreading depolarizations induced by focal brain ischemia in rats. Neurobiol. Aging, 2014, 35(12), 2803-2811.
Farkas, E.; Bari, F. Spreading depolarization in the ischemic brain: Does aging have an impact? J. Gerontol. Ser. A Biol. Sci. Med. Sci., 2014, 69(11), 1363-1370.
Menyhárt, Á.; Makra, P.; Szepes, B.É.; Tóth, O.M.; Hertelendy, P.; Bari, F.; Farkas, E. High incidence of adverse cerebral blood flow responses to spreading depolarization in the aged ischemic rat brain. Neurobiol. Aging, 2015, 36(12), 3269-3277.
Menyhárt, Á.; Zölei-Szénási, D.; Puskás, T.; Makra, P.; Orsolya, M.T.T.; Szepes, B.É.É.; Tóth, R.; Ivánkovits-Kiss, O.; Obrenovitch, T.P.P.; Bari, F.; Farkas, E. Spreading depolarization remarkably exacerbates ischemia-induced tissue acidosis in the young and aged rat brain. Sci. Rep., 2017, 7(1), 1154.
Dorsch, N.W.; King, M.T. A review of cerebral vasospasm in aneurysmal subarachnoid haemorrhage Part I: Incidence and effects. J. Clin. Neurosci., 1994, 1(1), 19-26.
Macdonald, R.L.; Weir, B.K. A review of hemoglobin and the pathogenesis of cerebral vasospasm. Stroke, 1991, 22(8), 971-982.
Feelisch, M.; Noack, E.A. Correlation between nitric oxide formation during degradation of organic nitrates and activation of guanylate cyclase. Eur. J. Pharmacol., 1987, 139(1), 19-30.
Shiga, T.; Hwang, K.J.; Tyuma, I. Electron paramagnetic resonance studies of nitric oxide hemoglobin derivatives. I. Human hemoglobin subunits. Biochemistry, 1969, 8(1), 378-383.
Rein, H.; Ristau, O.; Scheler, W. On the influence of allosteric effectors on the electron paramagnetic spectrum of nitric oxide hemoglobin. FEBS Lett., 1972, 24(1), 24-26.
Henry, Y.; Banerjee, R. Electron paramagnetic studies of nitric oxide haemoglobin derivatives: isolated subunits and nitric oxide hybrids. J. Mol. Biol., 1973, 73(4), 469-482.
Perutz, M.F.; Kilmartin, J.V.; Nagai, K.; Szabo, A.; Simon, S.R. Influence of globin structures on the state of the heme. Ferrous low spin derivatives. Biochemistry, 1976, 15(2), 378-387.
Sakowitz, O.W.; Wolfrum, S.; Sarrafzadeh, A.S.; Stover, J.F.; Dreier, J.P.; Dendorfer, A.; Benndorf, G.; Lanksch, W.R.; Unterberg, A.W. Relation of cerebral energy metabolism and extracellular nitrite and nitrate concentrations in patients after aneurysmal subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2001, 21(9), 1067-1076.
Dreier, J.P.; Petzold, G.; Tille, K.; Lindauer, U.; Arnold, G.; Heinemann, U.; Einhäupl, K.M.; Dirnagl, U. Ischaemia triggered by spreading neuronal activation is inhibited by vasodilators in rats. J. Physiol., 2001, 531(Pt 2), 515-526.
Petzold, G.C.; Haack, S.; von Bohlen Und Halbach, O.; Priller, J.; Lehmann, T-N.N.; Heinemann, U.; Dirnagl, U.; Dreier, J.P. Nitric oxide modulates spreading depolarization threshold in the human and rodent cortex. Stroke, 2008, 39(4), 1292-1299.
Hubschmann, O.R.; Kornhauser, D. Cortical cellular response in acute subarachnoid hemorrhage. J. Neurosurg., 1980, 52(4), 456-462.
Hubschmann, O.R.; Kornhauser, D. Effect of subarachnoid hemorrhage on the extracellular microenvironment. J. Neurosurg., 1982, 56(2), 216-221.
Oka, F.; Hoffmann, U.; Lee, J.H.; Shin, H.K.; Chung, D.Y.; Yuzawa, I.; Chen, S.-P.; Atalay, Y. B.; Nozari, A.; Hopson, K.P.; Qin, T.; Ayata, C. Requisite ischemia for spreading depolarization occurrence after subarachnoid hemorrhage in rodents., J. Cereb. Blood Flow Metab.,2016, 37(5), 1829-184. 00271678X16659303 http://dx.doi.org/10.1177/0271678x16659303.
Hinzman, J.M.; Andaluz, N.; Shutter, L.A.; Okonkwo, D.O.; Pahl, C.; Strong, A.J.; Dreier, J.P.; Hartings, J.A. Inverse neurovascular coupling to cortical spreading depolarizations in severe brain trauma., Brain, 2014, 137(11), 2960-2972. http://dx.doi.org/10. 1093/brain/awu241.
Suzuki, H.; Shiba, M.; Nakatsuka, Y.; Nakano, F.; Nishikawa, H. Higher cerebrospinal fluid pH may contribute to the development of delayed cerebral ischemia after aneurysmal subarachnoid Hemorrhage. Transl. Stroke Res., 2016, 8(2), 165-173.
Sakowitz, O.W.W.; Santos, E.; Nagel, A.; Krajewski, K.L.L.; Hertle, D.N.N.; Vajkoczy, P.; Dreier, J.P.P.; Unterberg, A.W.W.; Sarrafzadeh, A.S.S. Clusters of spreading depolarizations are associated with disturbed cerebral metabolism in patients with aneurysmal subarachnoid hemorrhage. Stroke, 2012, 44(1), 220-223.
Saatman, K.E.; Duhaime, A-C.; Bullock, R.; Maas, A.I.R.; Valadka, A.; Manley, G.T. Workshop scientific team and advisory panel members. Classification of traumatic brain injury for targeted therapies. J. Neurotrauma, 2008, 25(7), 719-738.
Bogdanov, V.B.B.; Middleton, N.A.A.; Theriot, J.J.J.; Parker, P.D.D.; Abdullah, O.M.M.; Ju, Y.S.S.; Hartings, J.A.A.; Brennan, K.C.C. Susceptibility of primary sensory cortex to spreading depolarizations. J. Neurosci., 2016, 36(17), 4733-4743.
Strong, A.J.; Hartings, J. a; Dreier, J. P. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr. Opin. Crit. Care,2007, 13(2), 126-133 http://dx.doi.org/10.1097/mcc. 0b013e32807faffb.
Mayevsky, A.; Doron, A.; Manor, T.; Meilin, S.; Zarchin, N.; Ouaknine, G.E. Cortical spreading depression recorded from the human brain using a multiparametric monitoring system. Brain Res., 1996, 740(1-2), 268-274.
Strong, A.J.; Fabricius, M.; Boutelle, M.G.; Hibbins, S.J.; Hopwood, S.E.; Jones, R.; Parkin, M.C.; Lauritzen, M. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke, 2002, 33(12), 2738-2743.
Hartings, J.A.; Strong, A.J.; Fabricius, M.; Manning, A.; Bhatia, R.; Dreier, J.P.; Mazzeo, A.T.; Tortella, F.C.; Bullock, M.R. Co-operative study of brain injury depolarizations. spreading depolarizations and late secondary insults after traumatic brain injury. J. Neurotrauma, 2009, 1866, 1857-1866.
[http://dx.doi.org/10.1089/ neu.2009-0961]
Vespa, P. M.; McArthur, D.; O’Phelan, K.; Glenn, T.; Etchepare, M.; Kelly, D.; Bergsneider, M.; Martin, N. A.; Hovda, D. A. Persistently low extracellular glucose correlates with poor outcome 6 months after human traumatic brain injury despite a lack of increased lactate: a microdialysis study., J. Cereb. Blood Flow Metab,.2003, 23(7), 865-877. http://dx.doi.org/10.1097/01.wcb.0000076701. 45782.ef.
Hinzman, J.M.; Wilson, J.A.; Mazzeo, A.T.; Bullock, M.R.; Hartings, J.A.; Bullock, R.; Hartings, J.A. Excitotoxicity and metabolic crisis are associated with spreading depolarizations in severe traumatic brain injury patients. J. Neurotrauma, 2015, 9(513), 1-9.
Marcoux, J.; McArthur, D. a; Miller, C.; Glenn, T.C.; Villablanca, P.; Martin, N. a; Hovda, D. a; Alger, J. R.; Vespa, P.M. Persistent metabolic crisis as measured by elevated cerebral microdialysis lactate-pyruvate ratio predicts chronic frontal lobe brain atrophy after traumatic brain injury. Crit. Care Med., 2008, 36(10), 2871-2877.
Ozawa, Y.; Nakamura, T.; Sunami, K.; Kubota, M.; Ito, C.; Murai, H.; Yamaura, A.; Makino, H. Study of regional cerebral blood flow in experimental head injury: changes following cerebral contusion and during spreading depression. Neurol. Med. Chir. (Tokyo), 1991, 31(11), 685-690.
Nilsson, P.; Hillered, L.; Olsson, Y.; Sheardown, M. J.; Hansen, A. J. Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J. Cereb. Blood Flow Metab.,1993, 13(2), 183-192. http://dx.doi.org/10.1038/jcbfm. 1993.22.
Sánchez-Porras, R.; Santos, E.; Schöll, M.; Stock, C.; Zheng, Z.; Schiebel, P.; Orakcioglu, B.; Unterberg, A.W.; Sakowitz, O.W. The effect of ketamine on optical and electrical characteristics of spreading depolarizations in gyrencephalic swine cortex. Neuropharmacology, 2014, 84, 52-61.
[http://dx.doi.org/10.1016/ j.neuropharm.2014.04.018]
Hernándéz-Cáceres, J.; Macias-González, R.; Brožek, G.; Bureš, J. Systemic ketamine blocks cortical spreading depression but does not delay the onset of terminal anoxic depolarization in rats., 1987, 437 (2), 360-4.
Sánchez-Porras, R.; Santos, E.; Schöll, M.; Kunzmann, K.; Stock, C.; Silos, H.; Unterberg, A. W.W.; Sakowitz, O. W.W. Ketamine modulation of the haemodynamic response to spreading depolarization in the gyrencephalic swine brain., J. Cereb. Blood Flow Metab.,2017, 37(5), 1720-1734. http://dx.doi.org/10.1177/0271678 x16646586.
Sakowitz, O.W.; Kiening, K.L.; Krajewski, K.L.; Sarrafzadeh, A.S.; Fabricius, M.; Strong, A.J.; Unterberg, A.W.; Dreier, J.P. Preliminary evidence that ketamine inhibits spreading depolarizations in acute human brain injury. Stroke, 2009, 40(8), e519.
Hertle, D.N.; Dreier, J.P.; Woitzik, J.; Hartings, J.A.; Bullock, R.; Okonkwo, D.O.; Shutter, L.A.; Vidgeon, S.; Strong, A.J.; Kowoll, C.; Dohmen, C.; Diedler, J.; Veltkamp, R.; Bruckner, T.; Unterberg, A.W.; Sakowitz, O.W. Cooperative study of brain Injury Depolarizations (COSBID). Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain, 2012, 135(8), 2390-2398.
Takagaki, M.; Feuerstein, D.; Kumagai, T.; Gramer, M.; Yoshimine, T.; Graf, R. Isoflurane suppresses cortical spreading depolarizations compared to propofol - implications for sedation of neurocritical care patients. Exp. Neurol., 2014, 252, 12-17.
Patel, P. M.; Drummond, J.C.; Cole, D.J. lsoflurane and Pentobarbital reduce the frequency of transient ischemic depolarizations during focal ischemia in rats. Anesth. Analg., 1998, 86(86), 896- 908, 773-780. http://dx.doi.org/10.1213/00000539-199804000- 00018.
Bar-Klein, G.; Klee, R.; Brandt, C.; Brankstahl, M.; Tollner, K.; Dalipaj, H.; Friedman, A.; Steinhauser, C. Isoflurane prevents acquired epilepsy in two rat models of temporal lobe epilepsy. Ann. Neurol., 2016, 80(6)
Kudo, C.; Toyama, M.; Boku, A.; Hanamoto, H.; Morimoto, Y.; Sugimura, M.; Niwa, H. Anesthetic effects on susceptibility to cortical spreading depression. Neuropharmacology, 2013, 67, 32-36.
Ayata, C.; Jin, H.; Kudo, C.; Dalkara, T.; Moskowitz, M. A. Suppression of cortical spreading depression in migraine prophylaxis., Ann. Neurol., 2006, 59(4), 652-661. http://dx.doi.org/10.1002/ana. 20778.
Hauge, A.W.; Asghar, M.S.; Schytz, H.W.; Christensen, K.; Olesen, J. Effects of tonabersat on migraine with aura: a randomised, double-blind, placebo-controlled crossover study., Lancet, Neurol.2009, 8(8), 718-723. http://dx.doi.org/10.1016/s1474-4422(09) 70135-8.
Cain, S.M.; Bohnet, B.; LeDue, J.; Yung, A.C.; Garcia, E.; Tyson, J. R.; Alles, S.R.A.; Han, H.; van den Maagdenberg, A.M.J.M.; Kozlowski, P.; MacVicar, B.A.; Snutch, T.P. In vivo imaging reveals that pregabalin inhibits cortical spreading depression and propagation to subcortical brain structures. Proc. Natl. Acad. Sci., 2017, 114(9), 201614447. http://dx.doi.org/10.1073/pnas. 1614447114.
Shin, H.K.; Dunn, A.K.; Jones, P. B.; Boas, D.A.; Lo, E.H. Moskowitz, M.A.; Ayata, C. Normobaric hyperoxia improves cerebral blood flow and oxygenation, and inhibits peri-infarct depolarizations in experimental focal ischaemia. Brain, 2007, 130(Pt 6), 1631-1642.
Chen, Q.; Chopp, M.; Bodzin, G.; Chen, H. Temperature modulation of cerebral depolarization during focal cerebral ischemia in rats: correlation with ischemic injury. J. Cereb. Blood Flow Metab., 1993, 13(3), 389-394.
Hoffmann, U.; Sukhotinsky, I.; Eikermann-Haerter, K.; Ayata, C. Glucose modulation of spreading depression susceptibility. J. Cereb. Blood Flow Metab., 2013, 33(2), 191-195.
Strong, A.J.; Smith, S.E.; Whittington, D.J.; Meldrum, B.S.; Parsons, A.A.; Krupinski, J.; Hunter, A.J.; Patel, S.; Robertson, C. Factors influencing the frequency of fluorescence transients as markers of peri-infarct depolarizations in focal cerebral ischemia., Stroke, 2000, 31(1), 214-222. http://dx.doi.org/10.1161/01.str.31.1. 214.
Strong, A.J.; Boutelle, M.G.; Vespa, P. M.; Bullock, M.R.; Bhatia, R.; Hashemi, P. Treatment of critical care patients with substantial acute ischemic or traumatic brain injury. Crit. Care Med.,2005, 33(9), 2147-9. author reply 2149.
Krivanek, J. Some metabolic changes accompanying Leao’s spreading cortical depression in the rat. J. Neurochem., 1961, 6, 183-189.
Mies, G.; Paschen, W. Regional changes of blood flow, glucose, and ATP content determined on brain sections during a single passage of spreading depression in rat brain cortex. Exp. Neurol., 1984, 84(2), 249-258.
Hashemi, P.; Bhatia, R.; Nakamura, H.; Dreier, J.P.; Graf, R.; Strong, A.J.; Boutelle, M.G. Persisting depletion of brain glucose following cortical spreading depression, despite apparent hyperaemia: evidence for risk of an adverse effect of Leao’s spreading depression. J. Cereb. Blood Flow Metab., 2009, 29(1), 166-175.
Krivanek, J. Concerning the dynamics of the metabolic changes accompanying cortical spreading depression. Physiol. Bohemoslov., 1962, 11, 383-391.
Hopwood, S.E.; Parkin, M.C.; Bezzina, E.L.; Boutelle, M.G.; Strong, A.J. Transient changes in cortical glucose and lactate levels associated with peri-infarct depolarisations, studied with rapid-sampling microdialysis. J. Cereb. Blood Flow Metab., 2005, 25(3), 391-401.
Silver, I.A.; Erecińska, M. Extracellular glucose concentration in mammalian brain: continuous monitoring of changes during increased neuronal activity and upon limitation in oxygen supply in normo-, hypo-, and hyperglycemic animals. J. Neurosci., 1994, 14(8), 5068-5076.
Csiba, L.; Paschen, W.; Mies, G. Regional changes in tissue pH and glucose content during cortical spreading depression in rat brain. Brain Res., 1985, 336(1), 167-170.
Gidö, G.; Katsura, K.; Kristian, T.; Siesjö, B.K. Influence of plasma glucose concentration on rat brain extracellular calcium transients during spreading depression. J. Cereb. Blood Flow Metab., 1993, 13(1), 179-182.
Nedergaard, M.; Astrup, J. Infarct rim: Effect of hyperglycemia on direct current potential and [ 14 C]2-Deoxyglucose phosphorylation. J. Cereb. Blood Flow Metab., 1986, 6(5), 607-615.
Schiefecker, A.J.; Kofler, M.; Gaasch, M.; Beer, R.; Unterberger, I.; Pfausler, B.; Broessner, G.; Lackner, P.; Rhomberg, P.; Gizewski, E.; Hackl, W. O.; Mulino, M.; Ortler, M.; Thome, C.; Schmutzhard, E.; Helbok, R. Brain temperature but not core temperature increases during spreading depolarizations in patients with spontaneous intracerebral hemorrhage., J. Cereb. Blood Flow Metab.,2017, 38(3), 549-558. http://dx.doi.org/10.1177/0271678 x17703940.
Needham, E.; McFadyen, C.; Newcombe, V.; Synnot, A.J.; Czosnyka, M.; Menon, D. Cerebral perfusion pressure targets individualized to pressure-reactivity index in moderate to severe traumatic brain injury: A systematic review. J. Neurotrauma, 2017, 34(5), 963-970.
Dias, C.; Silva, M.J.; Pereira, E.; Monteiro, E.; Maia, I.; Barbosa, S.; Silva, S.; Honrado, T.; Cerejo, A.; Aries, M.J.H.; Smielewski, P.; Paiva, J-A.; Czosnyka, M. Optimal cerebral perfusion pressure management at bedside: A single-center pilot sudy. Neurocrit. Care, 2015, 23(1), 92-102.
Sukhotinsky, I.; Yaseen, M.A.; Sakadžić, S.; Ruvinskaya, S.; Sims, J.R.; Boas, D.A.; Moskowitz, M.A.; Ayata, C. Perfusion Pressure-dependent recovery of cortical spreading depression is Independent of tissue oxygenation over a wide physiologic range. J. Cereb. Blood Flow Metab., 2010, 30(6), 1168-1177.
Sukhotinsky, I.; Dilekoz, E.; Moskowitz, M.A.; Ayata, C. Hypoxia and hypotension transform the blood flow response to cortical spreading depression from hyperemia into hypoperfusion in the rat. J. Cereb. Blood Flow Metab., 2008, 28(7), 1369-1376.
Winkler, M.K.; Dengler, N.; Hecht, N.; Hartings, J.A.; Kang, E.J.; Major, S.; Martus, P.; Vajkoczy, P.; Woitzik, J.; Dreier, J.P. Oxygen availability and spreading depolarizations provide complementary prognostic information in neuromonitoring of aneurysmal subarachnoid hemorrhage patients. J. Cereb. Blood Flow Metab., 2017, 37(5), 1841-1856.
[http://dx.doi.org/10.1177/ 0271678x16641424]
Helbok, R.; Schiefecker, A.J.; Friberg, C.; Beer, R.; Kofler, M.; Rhomberg, P.; Unterberger, I.; Gizewski, E.; Hauerberg, J.; Möller, K.; Lackner, P.; Broessner, G.; Pfausler, B.; Ortler, M.; Thome, C.; Schmutzhard, E.; Fabricius, M. Spreading depolarizations in patients with spontaneous intracerebral hemorrhage: Association with perihematomal edema progression. J. Cereb. Blood Flow Metab., 2017, 37(5), 1871-1882.
Hänggi, D.; Etminan, N.; Aldrich, F.; Steiger, H.J.; Mayer, S.A.; Diringer, M.N.; Hoh, B.L.; Mocco, J.; Faleck, H.J.; Macdonald, R.L. Randomized, open-Label, phase 1/2a study to determine the maximum tolerated dose of intraventricular sustained release Nimodipine for subarachnoid hemorrhage (NEWTON nimodipine microparticles to enhance recovery while reducing toxicity after subarachnoid. Stroke, 2017, 48(1), 145-151.
Draganski, B.; Gaser, C.; Busch, V.; Schuierer, G.; Bogdahn, U.; May, A. Neuroplasticity: changes in grey matter induced by training. Nature, 2004, 427(6972), 311-312.
[http://dx.doi.org/10.1038/ 427311a]
Tardif, C.L.; Steele, C.J.; Lampe, L.; Bazin, P-L.; Ragert, P.; Villringer, A.; Gauthier, C.J. Investigation of the confounding effects of vasculature and metabolism on computational anatomy studies. Neuroimage, 2017, 149, 233-243.
[http://dx.doi.org/10.1016/ j.neuroimage.2017.01.025]
Khalil, A. A.; Ostwaldt, A.-C.; Nierhaus, T.; Ganeshan, R.; Audebert, H. J.; Villringer, K.; Villringer, A.; Fiebach, J. B. Relationship between changes in the temporal dynamics of the blood-oxygen-level-dependent signal and hypoperfusion in acute ischemic stroke., Stroke, 2017, 48(4), 925-931. http://dx.doi.org/10.1161/strokeaha. 116.015566.
Viggiano, E.; Monda, V.; Messina, A.; Moscatelli, F.; Valenzano, A.; Tafuri, D.; Cibelli, G.; De Luca, B.; Messina, G.; Monda, M. Cortical spreading depression produces a neuroprotective effect activating mitochondrial uncoupling protein-5. Neuropsychiatr. Dis. Treat., 2016, 12, 1705-1710.
Nakase, T.; Yoshida, Y.; Nagata, K. Amplified expression of uncoupling proteins in human brain ischemic lesions. Neuropathology, 2007, 27(5), 442-447.
Fan, Y-Y.; Shen, Z.; He, P.; Jiang, L.; Hou, W.; Shen, Y.; Zhang, X-N.; Hu, W-W.; Chen, Z. A Novel neuroprotective strategy for ischemic stroke: Transient mild acidosis treatment by CO2 Inhalation at reperfusion. J. Cereb. Blood Flow Metab., 2014, 34(2), 275-283.
Helmy, M.M.; Tolner, E.A.; Vanhatalo, S.; Voipio, J.; Kaila, K. Brain alkalosis causes birth asphyxia seizures, suggesting therapeutic strategy. Ann. Neurol., 2011, 69(3), 493-500.
Khacho, M.; Tarabay, M.; Patten, D.; Khacho, P.; MacLaurin, J.G.; Guadagno, J.; Bergeron, R.; Cregan, S.P.; Harper, M-E.; Park, D.S.; Slack, R.S. Acidosis overrides oxygen deprivation to maintain mitochondrial function and cell survival. Nat. Commun., 2014, 5, 418-428.
Laffey, J.G. Protective effects of acidosis. Anaesthesia, 2001, 56(10), 1013-1014.
Laffey, J.G.; Kavanagh, B.P. Carbon dioxide and the critically ill—too little of a good thing? Lancet, 1999, 354(9186), 1283-1286.
Simon, R.P.; Niro, M.; Gwinn, R. Brain acidosis induced by hypercarbic ventilation attenuates focal ischemic injury. J. Pharmacol. Exp. Ther., 1993, 267(3), 1428-1431.
Swenson, E. R. Therapeutic hypercapnic acidosis., Am. J. Respir. Crit. Care Med.,2004, 169(1), 8-9. http://dx.doi.org/10.1164/rccm. 2310008.
Kawahara, N.; Croll, S.D.D.; Wiegand, S.J.J.; Klatzo, I. Cortical spreading depression induces long-term alterations of BDNF levels in cortex and hippocampus distinct from lesion effects: implications for ischemic tolerance. Neurosci. Res., 1997, 29(1), 37-47.
Matsushima, K.; Hogan, M.J.J.; Hakim, A.M.M. Cortical spreading depression protects against Subsequent focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab., 1996, 16(2), 221-226.
Kobayashi, S.; Harris, V.A.A.; Welsh, F.A.A. Spreading depression induces tolerance of cortical neurons to ischemia in rat Brain. J. Cereb. Blood Flow Metab., 1995, 15(5), 721-727.
Kawahara, N.; Ruetzler, C.A.A.; Klatzo, I. Protective effect of spreading depression against neuronal damage following cardiac arrest cerebral ischaemia. Neurol. Res., 1995, 17(1), 9-16.
Taga, K.; Patel, P.M.M.; Drummond, J.C.C.; Cole, D.J.J.; Kelly, P.J.J. Transient neuronal depolarization induces tolerance to subsequent forebrain ischemia in rats. Anesthesiology, 1997, 87(4), 918-925.
Shpargel, K.B.B.; Jalabi, W.; Jin, Y.; Dadabayev, A.; Penn, M.S.S.; Trapp, B.D.D. Preconditioning paradigms and pathways in the brain. Cleve. Clin. J. Med., 2008, 75(Suppl. 2), S77-S82.
Kawahara, N.; Ruetzler, C.A.A.; Mies, G.; Klatzo, I. Cortical spreading depression increases protein synthesis and upregulates basic fibroblast growth factor. Exp. Neurol., 1999, 158(1), 27-36.
Otori, T.; Greenberg, J.H.H.; Welsh, F.A.A. Cortical spreading depression causes a long-lasting decrease in cerebral blood flow and induces tolerance to permanent focal ischemia in rat brain. J. Cereb. Blood Flow Metab., 2003, 23(1), 43-50.
Douen, A. G.G.; Akiyama, K.; Hogan, M. J.J.; Wang, F.; Dong, L.; Chow, A.K.K.; Hakim, A. Preconditioning with cortical spreading depression decreases intraischemic cerebral glutamate levels and Down-regulates excitatory amino acid transporters EAAT1 and EAAT2 from rat cerebal cortex plasma membranes., J. Neurochem.,2002, 75(2), 812-818. http://dx.doi.org/10.1046/j.1471-4159.2000. 0750812.x.
Witte, O.W.W.; Bidmon, H-J.; Schiene, K.; Redecker, C.; Hagemann, G. Functional differentiation of multiple perilesional zones after focal cerebrali. J. Cereb. Blood Flow Metab., 2000, 20(8), 1149-1165.
Yanamoto, H.; Miyamoto, S.; Tohnai, N.; Nagata, I.; Xue, J-H.J.H.; Nakano, Y.; Nakajo, Y.; Kikuchi, H. Induced spreading depression activates persistent neurogenesis in the subventricular zone, generating cells with markers for divided and early committed neurons in the caudate putamen and cortex. Stroke, 2005, 36(7), 1544-1550.
Urbach, A.; Redecker, C.; Witte, O.W.W. Induction of neurogenesis in the adult dentate gyrus by cortical spreading depression. Stroke, 2008, 39(11)
Santos, E.; Sánchez-Porras, R.; Sakowitz, O.W.W.; Dreier, J.P.P.; Dahlem, M.A.A. Heterogeneous propagation of spreading depolarizations in the lissencephalic and gyrencephalic brain. J. Cereb. Blood Flow Metab., 2017, 37(7), 2639-2643.
Santos, E.; Schöll, M.; Sánchez-Porras, R.; Dahlem, M.A.A.; Silos, H.; Unterberg, A.; Dickhaus, H.; Sakowitz, O.W.W. Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. Neuroimage, 2014, 99, 244-255.
Schöll, M.J.J.; Santos, E.; Sanchez-Porras, R.; Kentar, M.; Gramer, M.; Silos, H.; Zheng, Z.; Gang, Y.; Strong, A.J.J.; Graf, R.; Unterberg, A.; Sakowitz, O.W.W.; Dickhaus, H. Large field-of-view movement-compensated intrinsic optical signal imaging for the characterization of the haemodynamic response to spreading depolarizations in large gyrencephalic brains. J. Cereb. Blood Flow Metab., 2017, 37(5), 1706-1719.
[http://dx.doi.org/10.1177/ 0271678x16668988]

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Year: 2019
Page: [151 - 164]
Pages: 14
DOI: 10.2174/1570159X15666170915160707
Price: $58

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