Correlates of spreading depolarization in human scalp electroencephalography

Brain

Volumn 135, Issue 3, 2012, Pages 853-868

  Drenckhahn, Christoph ^a   Winkler, Maren K L ^a   Major, Sebastian ^a   Scheel, Michael ^a   Kang, Eun Jeung ^a   Pinczolits, Alexandra ^a   Grozea, Cristian ^b   Hartings, Jed A ^c   Woitzik, Johannes ^a   Dreier, Jens P ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b FRAUNHOFER FIRST   (Germany)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

delayed cerebral ischaemia; electroencephalography; ischaemic stroke; spreading depression; subarachnoid haemorrhage

Indexed keywords

ADULT; AGED; ALTERNATING CURRENT; ARTICLE; BRAIN ARTERY ANEURYSM; BRAIN FUNCTION; BRAIN INFARCTION; CLINICAL ARTICLE; DECOMPRESSIVE CRANIECTOMY; DEPOLARIZATION; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAPHY; FEMALE; HUMAN; MALE; MALIGNANT HEMISPHERIC STROKE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SCALP; SPREADING CORTICAL DEPOLARIZATION; SPREADING CORTICAL DEPRESSION; STROKE; SUBARACHNOID HEMORRHAGE;

EID: 84857550474     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws010     Document Type: Article

References (59)

1. Back T, Kohno K, Hossmann KA. Cortical negative DC deflections following middle cerebral artery occlusion and KCl-induced spreading depression: effect on blood flow, tissue oxygenation, and electroencephalogram. J Cereb Blood Flow Metab 1994;14:12-9.
2. Bosche B, Graf R, Ernestus RI, Dohmen C, Reithmeier T, Brinker G, et al. Recurrent spreading depolarizations after SAH decrease oxygen availability in human cerebral cortex. Ann Neurol 2010;67:607-17.
3. Canals S, Makarova I, Lopez-Aguado L, Largo C, Ibarz JM, Herreras O. Longitudinal depolarization gradients along the somatodendritic axis of CA1 pyramidal cells: a novel feature of spreading depression. J Neurophysiol 2005;94:943-51.
4. Claassen J, Hirsch LJ, Kreiter KT, Du EY, Connolly ES, Emerson RG, et al. Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage. Clin Neurophysiol 2004;115:2699-710.
5. Claassen J, Mayer SA, Hirsch LJ. Continuous EEG monitoring in patients with subarachnoid hemorrhage. J Clin Neurophysiol 2005;22:92-8.
6. Cohn R, Raines GN, Mulder DW, Neumann MA. Cerebral vascular lesions; electroencephalographic and neuropathologic correlations. Arch Neurol Psychiatry 1948;60:165-81.
7. Dohmen C, Sakowitz OW, Fabricius M, Bosche B, Reithmeier T, Ernestus RI, et al. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 2008;63:720-8.
8. Donnan GA. The 2007 Feinberg lecture: a new road map for neuroprotection. Stroke 2008;39:242.
9. Dreier JP. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat Med 2011;17:439-47.
10. Dreier JP, Major S, Manning A, Woitzik J, Drenckhahn C, Steinbrink J, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009;132:1866-81.
11. Dreier JP, Major S, Pannek HW, Woitzik J, Scheel M, Wiesenthal D, et al. Spreading convulsions, spreading depolarization, and epileptogenesis in human cerebral cortex. Brain 2012;135:259-76.
12. Dreier JP, Sakowitz OW, Harder A, Zimmer C, Dirnagl U, Valdueza JM, et al. Focal laminar cortical MR signal abnormalities after subarachnoid hemorrhage. Ann Neurol 2002;52:825-9.
13. Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006;129:3224-37.
14. Durduran T, Choe R, Baker WB, Yodh AG. Diffuse optics for tissue monitoring and tomography. Rep Progr Phys 2010;73:076701.
15. Espinosa J, Olivier A, Andermann F, Quesney F, Dubeau F, Savard G. Morbidity of chronic recording with intracranial depth electrodes in 170 patients. Stereotact Funct Neurosurg 1994;63:63-5.
16. Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab 2011;31:1443-51.
17. Fabricius M, Fuhr S, Bhatia R, Boutelle M, Hashemi P, Strong AJ, et al. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006;129:778-90.
18. Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol 2008;119:1973-84.
19. Feuerstein D, Manning A, Hashemi P, Bhatia R, Fabricius M, Tolias C, et al. Dynamic metabolic response to multiple spreading depolarizations in patients with acute brain injury: an online microdialysis study. J Cereb Blood Flow Metab 2010;30:1343-55.
20. Hartings JA, Bullock MR, Okonkwo DO, Murray LS, Murray GD, Fabricius M, et al. Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol 2011a;10:1058-64.
21. Hartings JA, Strong AJ, Fabricius M, Manning A, Bhatia R, Dreier JP, et al. Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 2009;26:1857-66.
22. Hartings JA, Watanabe T, Dreier JP, Major S, Vendelbo L, Fabricius M. Recovery of slow potentials in AC-coupled electrocorticography: application to spreading depolarizations in rat and human cerebral cortex. J Neurophysiol 2009;102:2563-75.
23. Hartings JA, Watanabe T, Bullock MR, Okonkwo DO, Fabricius M, Woitzik J, et al. Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain 2011b;134:1529-40.
24. Herreras O, Somjen GG. Analysis of potential shifts associated with recurrent spreading depression and prolonged unstable spreading depression induced by microdialysis of elevated K + in hippocampus of anesthetized rats. Brain Res 1993;610:283-94.
25. Hossmann KA. Viability thresholds and the penumbra of focal ischemia. Ann Neurol 1994;36:557-65.
26. Juttler E, Bosel J, Amiri H, Schiller P, Limprecht R, Hacke W, et al. DESTINY II: DEcompressive Surgery for the Treatment of malignant INfarction of the middle cerebral arter Y II. Int J Stroke 2011;6:79-86.
27. Kistler JP, Crowell RM, Davis KR, Heros R, Ojemann RG, Zervas T, et al. The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study. Neurology 1983;33:424-36.
28. Klatzo I. Pathophysiological aspects of brain edema. Acta Neuropathol 1987;72:236-9.
29. Klem GH, Luders HO, Jasper HH, Elger C. The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52:3-6.
30. Labar DR, Fisch BJ, Pedley TA, Fink ME, Solomon RA. Quantitative EEG monitoring for patients with subarachnoid hemorrhage. Electroencephalogr Clin Neurophysiol 1991;78:325-32.
31. La Manna JC, Rosenthal M. Effect of ouabain and phenobarbital on oxidative metabolic activity associated with spreading cortical depression in cats. Brain Res 1975;88:145-9.
32. Leão A A P. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol 1947;10:409-14.
33. Lee WS, Lee JK, Lee SA, Kang JK, Ko TS. Complications and results of subdural grid electrode implantation in epilepsy surgery. Surg Neurol 2000;54:346-51.
34. Lehmenkühler A, Richter F, Poppelmann T. Hypoxia-and hypercapnia-induced DC potential shifts in rat at the scalp and the skull are opposite in polarity to those at the cerebral cortex. Neurosci Lett 1999;270:67-70.
35. Lehmenkühler A, Richter F, Scheller D, Speckmann EJ. Non-invasive DC recordings from the skull and the skin during cortical spreading depression: a model of detection of migraine. In: Olesen J, editor. Frontiers in headache research Migraine and other headaches: The vascular mechanisms. New York: Raven Press; 1991. p. 167-70.
36. Lo EH. A new penumbra: transitioning from injury into repair after stroke. Nat Med 2008;14:497-500.
37. Miller JW, Kim W, Holmes MD, Vanhatalo S. Ictal localization by source analysis of infraslow activity in DC-coupled scalp EEG recordings. Neuroimage 2007;35:583-97.
38. Minhas PS, Menon DK, Smielewski P, Czosnyka M, Kirkpatrick PJ, Clark JC, et al. Positron emission tomographic cerebral perfusion disturbances and transcranial Doppler findings among patients with neurological deterioration after subarachnoid hemorrhage. Neurosurgery 2003;52:1017-22 discussion 22-4.
39. Nakamura H, Strong AJ, Dohmen C, Sakowitz OW, Vollmar S, Sue M, et al. Spreading depolarizations cycle around and enlarge focal ischaemic brain lesions. Brain 2010;133:1994-2006.
40. Neil-Dwyer G, Lang DA, Doshi B, Gerber CJ, Smith PW. Delayed cerebral ischaemia: the pathological substrate. Acta Neurochir (Wien) 1994;131:137-45.
41. Obrig H, Villringer A. Beyond the visible-imaging the human brain with light. J Cereb Blood Flow Metab 2003;23:1-18.
42. Oliveira-Ferreira AI, Milakara D, Alam M, Jorks D, Major S, Hartings JA, et al. Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J Cereb Blood Flow Metab 2010;30:1504-19.
43. Oliveira-Ferreira AI, Winkler M K L, Reiffurth C, Milakara D, Woitzik J, Dreier JP. Spreading depolarization, a pathophysiological mechanism of stroke and migraine aura. Future Neurol 2012;7:45-64.
44. Risher WC, Ard D, Yuan J, Kirov SA. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci 2010;30:9859-68.
45. Rivierez M, Landau-Ferey J, Grob R, Grosskopf D, Philippon J. Value of electroencephalogram in prediction and diagnosis of vasospasm after intracranial aneurysm rupture. Acta Neurochir (Wien) 1991;110:17-23.
46. Sharbrough FW, Messick JM Jr, Sundt TM Jr. Correlation of continuous electroencephalograms with cerebral blood flow measurements during carotid endarterectomy. Stroke 1973;4:674-83.
47. Shimoda M, Takeuchi M, Tominaga J, Oda S, Kumasaka A, Tsugane R. Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery 2001;49:1341-8 discussion 8-50.
48. Somjen GG. Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol Rev 2001;81:1065-96.
49. Strong AJ, Fabricius M, Boutelle MG, Hibbins SJ, Hopwood SE, Jones R, et al. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002;33:2738-43.
50. Takano T, Tian GF, Peng W, Lou N, Lovatt D, Hansen AJ, et al. Cortical spreading depression causes and coincides with tissue hypoxia. Nat Neurosci 2007;10:754-62.
51. Tallgren P, Vanhatalo S, Kaila K, Voipio J. Evaluation of commercially available electrodes and gels for recording of slow EEG potentials. Clin Neurophysiol 2005;116:799-806.
52. van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001;124:249-78.
53. Vergouwen MD, Etminan N, Ilodigwe D, Macdonald RL. Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 2011;31:1545-53.
54. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke 2010;41:2391-5.
55. Vespa PM, Nuwer MR, Juhasz C, Alexander M, Nenov V, Martin N, et al. Early detection of vasospasm after acute subarachnoid hemorrhage using continuous EEG ICU monitoring. Electroencephalogr Clin Neurophysiol 1997;103:607-15.
56. Vora YY, Suarez-Almazor M, Steinke DE, Martin ML, Findlay JM. Role of transcranial Doppler monitoring in the diagnosis of cerebral vasospasm after subarachnoid hemorrhage. Neurosurgery 1999;44:1237-47 discussion 47-8.
57. Wadman WJ, Juta AJ, Kamphuis W, Somjen GG. Current source density of sustained potential shifts associated with electrographic seizures and with spreading depression in rat hippocampus. Brain Res 1992;570:85-91.
58. Weidauer S, Vatter H, Beck J, Raabe A, Lanfermann H, Seifert V, et al. Focal laminar cortical infarcts following aneurysmal subarachnoid haemorrhage. Neuroradiology 2008;50:1-8.
59. Woitzik J, Dreier JP, Hecht N, Fiss I, Sandow N, Major S, et al. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2011. Advance Access published on December 7, 2011, doi:10.1038/jcbfm.2011.169.1.