Spreading depolarizations in patients with spontaneous intracerebral hemorrhage: Association with perihematomal edema progression

Journal of Cerebral Blood Flow and Metabolism

Volumn 37, Issue 5, 2017, Pages 1871-1882

  Helbok, Raimund ^a   Schiefecker, Alois Josef ^a   Friberg, Christian ^b   Beer, Ronny ^a   Kofler, Mario ^a   Rhomberg, Paul ^a   Unterberger, Iris ^a   Gizewski, Elke ^a   Hauerberg, John ^b   Möller, Kirsten ^b   Lackner, Peter ^a   Broessner, Gregor ^a   Pfausler, Bettina ^a   Ortler, Martin ^a   Thome, Claudius ^a   Schmutzhard, Erich ^a   Fabricius, Martin ^b  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b Rigshospitalet   (Denmark)

Author keywords

electrocorticography; intracerebral hemorrhage; perihematomal edema; secondary brain damage; Spreading depolarization

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN EDEMA; BRAIN HEMATOMA; BRAIN HEMORRHAGE; CLINICAL ARTICLE; COMATOSE PATIENT; CORTICAL ELECTRODE; DISEASE COURSE; ELECTROCORTICOGRAPHY; FEMALE; HEMATOMA EVACUATION; HUMAN; INCIDENCE; MALE; NEUROSURGERY; OBSERVATIONAL STUDY; PATIENT MONITORING; PERIHEMATOMAL EDEMA; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROSPECTIVE STUDY; SPREADING CORTICAL DEPRESSION; SUBDURAL STRIP ELECTRODE; CEREBRAL HEMORRHAGE, TRAUMATIC; COMA; COMPLICATION; MIDDLE AGED; NEUROPHYSIOLOGICAL MONITORING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BRAIN EDEMA; CEREBRAL HEMORRHAGE, TRAUMATIC; COMA; CORTICAL SPREADING DEPRESSION; DISEASE PROGRESSION; ELECTROCORTICOGRAPHY; FEMALE; HUMANS; MALE; MIDDLE AGED; NEUROPHYSIOLOGICAL MONITORING; PROSPECTIVE STUDIES;

EID: 85018723457     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1177/0271678X16651269     Document Type: Article

References (58)

1. Poon MT, Fonville AF and Al-Shahi Salman R. Longterm prognosis after intracerebral haemorrhage: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2014; 85: 660-667.
2. Steiner T, Al-Shahi Salman R, Beer R, et al. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke 2014; 9: 840-855.
3. Hemphill JC 3rd, Greenberg SM, Anderson CS, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2015; 46: 2032-2060.
4. Ropper AH. Lateral displacement of the brain and level of consciousness in patients with an acute hemispheral mass. N Engl J Med 1986; 314: 953-958.
5. Davis SM, Broderick J, Hennerici M, et al. Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology 2006; 66: 1175-1181.
6. Leira R, Davalos A, Silva Y, et al. Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors. Neurology 2004; 63: 461-467.
7. Zazulia AR, Diringer MN, Derdeyn CP, et al. Progression of mass effect after intracerebral hemorrhage. Stroke 1999; 30: 1167-1173.
8. Kollmar R, Juettler E, Huttner HB, et al. Cooling in intracerebral hemorrhage (CINCH) trial: protocol of a randomized German-Austrian clinical trial. Int J Stroke 2012; 7: 168-172.
9. Rincon F, Friedman DP, Bell R, et al. Targeted temperature management after intracerebral hemorrhage (TTMICH): methodology of a prospective randomized clinical trial. Int J Stroke 2014; 9: 646-651.
10. Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol 1944; 7: 359-390.
11. Dohmen C, Sakowitz OW, Fabricius M, et al. Spreading depolarizations occur in human ischemic stroke with high incidence. Ann Neurol 2008; 63: 720-728.
12. Dreier JP, Major S, Manning A, et al. Cortical spreading ischaemia is a novel process involved in ischaemic damage in patients with aneurysmal subarachnoid haemorrhage. Brain 2009; 132(Pt 7): 1866-1881.
13. Dreier JP, Woitzik J, Fabricius M, et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain 2006; 129(Pt 12): 3224-3237.
14. Hartings JA, Bullock MR, Okonkwo DO, et al. Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet 2011; 10: 1058-1064.
15. Hartings JA, Watanabe T, Bullock MR, et al. Spreading depolarizations have prolonged direct current shifts and are associated with poor outcome in brain trauma. Brain 2011; 134(Pt 5): 1529-1540.
16. Strong AJ, Fabricius M, Boutelle MG, et al. Spreading and synchronous depressions of cortical activity in acutely injured human brain. Stroke 2002; 33: 2738-2743.
17. Sakowitz OW, Santos E, Nagel A, et al. Clusters of spreading depolarizations are associated with disturbed cerebral metabolism in patients with aneurysmal subarachnoid hemorrhage. Stroke 2013; 44: 220-223.
18. Fabricius M, Fuhr S, Bhatia R, et al. Cortical spreading depression and peri-infarct depolarization in acutely injured human cerebral cortex. Brain 2006; 129(Pt 3): 778-790.
19. Schiefecker AJ, Beer R, Pfausler B, et al. Clusters of cortical spreading depolarizations in a patient with intracerebral hemorrhage: a multimodal neuromonitoring study. Neurocrit Care 2015; 22: 293-298.
20. Kothari RU, Brott T, Broderick JP, et al. The ABCs of measuring intracerebral hemorrhage volumes. Stroke 1996; 27: 1304-1305.
21. Gebel JM Jr, Jauch EC, Brott TG, et al. Natural history of perihematomal edema in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 2002; 33: 2631-2635.
22. Venkatasubramanian C, Mlynash M, Finley-Caulfield A, et al. Natural history of perihematomal edema after intracerebral hemorrhage measured by serial magnetic resonance imaging. Stroke 2011; 42: 73-80.
23. The Brain Trauma Foundation, The American Association of Neurological Surgeons, The Joint Section on Neurotrauma and Critical Care. Computed tomography scan features. J Neurotrauma 2000; 17: 597-627.
24. Morgenstern LB, Hemphill JC 3rd, Anderson C, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2010; 41: 2108-2129.
25. Drenckhahn C, Winkler MK, Major S, et al. Correlates of spreading depolarization in human scalp electroencephalography. Brain 2012; 135(Pt 3): 853-868.
26. Dreier JP, Fabricius M, Ayata C, et al. Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group. J Cereb Blood Flow Metab 2017; 37: 1595-1625.
27. Hertle DN, Dreier JP, Woitzik J, et al. Effect of analgesics and sedatives on the occurrence of spreading depolarizations accompanying acute brain injury. Brain 2012; 135(Pt 8): 2390-2398.
28. Zeger SL and Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics 1986; 42: 121-130.
29. Dreier JP, Major S, Pannek HW, et al. Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain 2012; 135(Pt 1): 259-275.
30. Mun-Bryce S, Wilkerson AC, Papuashvili N, et al. Recurring episodes of spreading depression are spontaneously elicited by an intracerebral hemorrhage in the swine. Brain Res 2001; 888: 248-255.
31. Orakcioglu B, Uozumi Y, Kentar MM, et al. Evidence of spreading depolarizations in a porcine cortical intracerebral hemorrhage model. Acta Neurochir Suppl 2012; 114: 369-372.
32. Antunes AP, Schiefecker AJ, Beer R, et al. Higher brain extracellular potassium is associated with brain metabolic distress and poor outcome after aneurysmal subarachnoid hemorrhage. Crit Care 2014; 18: R119.
33. Ohta OOK, Siguma M, Yamamoto M, et al. Cerebral vasospasm following ruptured intracranial aneurysms, especially some contributions of potassium ion released from subarachnoid hematoma to delayed cerebral vasospasm. In: Bevan JA (ed.) Vascular neuroeffector mechanisms. New York: Raven Press, 1983, pp.353-358.
34. Doczi T. The pathogenetic and prognostic significance of blood-brain barrier damage at the acute stage of aneurysmal subarachnoid haemorrhage. Clinical and experimental studies. Acta Neurochir 1985; 77: 110-132.
35. Hubschmann OR and Kornhauser D. Effects of intraparenchymal hemorrhage on extracellular cortical potassium in experimental head trauma. J Neurosurg 1983; 59: 289-293.
36. Katayama Y, Becker DP, Tamura T, et al. Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 1990; 73: 889-900.
37. Reinert M, Khaldi A, Zauner A, et al. High extracellular potassium and its correlates after severe head injury: relationship to high intracranial pressure. Neurosurg Focus 2000; 8: e10.
38. Grafstein B. Mechanism of spreading cortical depression. J Neurophysiol 1956; 19: 154-171.
39. Obrenovitch TP and Zilkha E. High extracellular potassium, and not extracellular glutamate, is required for the propagation of spreading depression. J Neurophysiol 1995; 73: 2107-2114.
40. Dreier JP, Korner K, Ebert N, et al. 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 Cerebr Blood Flow Metab 1998; 18: 978-990.
41. Dreier JP, Ebert N, Priller J, et al. 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: 658-666.
42. Hartings JA, Strong AJ, Fabricius M, et al. Spreading depolarizations and late secondary insults after traumatic brain injury. J Neurotrauma 2009; 26: 1857-1866.
43. Herweh C, Juttler E, Schellinger PD, et al. Perfusion CT in hyperacute cerebral hemorrhage within 3 hours after symptom onset: is there an early perihemorrhagic penumbra? J Neuroimag 2010; 20: 350-353.
44. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, et al. Cortical spreading depression activates and upregulates MMP-9. J Clin Invest 2004; 113: 1447-1455.
45. Elijovich L, Patel PV and Hemphill JC 3rd. Intracerebral hemorrhage. Semin Neurol 2008; 28: 657-667.
46. Butcher KS, Baird T, MacGregor L, et al. Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke 2004; 35: 1879-1885.
47. Gingrich MB, Junge CE, Lyuboslavsky P, et al. Potentiation of NMDA receptor function by the serine protease thrombin. J Neurosci 2000; 20: 4582-4595.
48. Tejima E, Zhao BQ, Tsuji K, et al. Astrocytic induction of matrix metalloproteinase-9 and edema in brain hemorrhage. J Cereb Blood Flow Metab 2007; 27: 460-468.
49. Bereczki D, Kollar J, Kozak N, et al. Cortical spreading edema in persistent visual migraine aura. Headache 2008; 48: 1226-1229.
50. Kempski O, Otsuka H, Seiwert T, et al. Spreading depression induces permanent cell swelling under penumbra conditions. Acta Neurochir Suppl 2000; 76: 251-255.
51. de Crespigny AJ, Rother J, Beaulieu C, et al. Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia. Effects of hypoglycemia, hyperglycemia, and TTX. Stroke 1999; 30: 2212-2222.
52. Dreier JP and Reiffurth C. The stroke-migraine depolarization continuum. Neuron 2015; 86: 902-922.
53. Risher WC, Ard D, Yuan J, et al. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci 2010; 30: 9859-9868.
54. Hartings JA, Shuttleworth CW, Kirov SA, et al. The continuum of spreading mass depolarizations in acute cortical lesion development: redefining Leã o's legacy. J Cerebr Blood Flow Metab 2016; in press.
55. Oliveira-Ferreira AI, Milakara D, Alam M, 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 Cerebr Blood Flow Metab 2010; 30: 1504-1519.
56. Seule M, Keller E, Unterberg A, et al. The hemodynamic response of spreading depolarization observed by near infrared spectroscopy after aneurysmal subarachnoid hemorrhage. Neurocrit Care 2015; 23: 108-112.
57. Anderson CS, Heeley E, Huang Y, et al. Rapid bloodpressure lowering in patients with acute intracerebral hemorrhage. New Engl J Med 2013; 368: 2355-2365.
58. Sakowitz OW, Kiening KL, Krajewski KL, et al. Preliminary evidence that ketamine inhibits spreading depolarizations in acute human brain injury. Stroke 2009; 40: e519-22.