Skip to main content
Top
Published in: Translational Stroke Research 1/2015

Open Access 01-02-2015 | Original Article

Seizure Activity Occurs in the Collagenase but not the Blood Infusion Model of Striatal Hemorrhagic Stroke in Rats

Authors: Ana C. Klahr, Clayton T. Dickson, Frederick Colbourne

Published in: Translational Stroke Research | Issue 1/2015

Login to get access

Abstract

Seizures are a frequent complication of brain injury, including intracerebral hemorrhage (ICH), where seizures occur in about a third of patients. Rodents are used to study pathophysiology and neuroprotective therapies after ICH, but there have been no studies assessing the occurrence of seizures in these models. Thus, we compared seizure incidence and characteristics after infusing collagenase (0.14 U), which degrades blood vessels, and autologous blood (100 μL) into the striatum of rats. Saline was infused in others as a negative control, whereas iron, a by-product of degrading erythrocytes, served as a positive control. Ipsilateral and contralateral electroencephalographic (EEG) activity was continuously monitored with telemetry probes for a week after the stroke. There were no electrographic abnormalities during baseline recordings. As expected, saline did not elicit any epileptiform activity whereas iron caused seizure activity. Seizures occurred in 66 % of the collagenase group between 10 and 36 h, their duration ranged from 5 to 90 s, and these events were mostly observed bilaterally. No such activity occurred after blood infusion despite comparable lesion sizes of 32.5 and 40.9 mm3 in the collagenase and blood models, respectively (p = 0.222). Therefore, seizures are a common acute occurrence in the collagenase but not whole blood models of striatal ICH (p = 0.028, for incidence). These findings have potential implications for ICH studies such as for understanding model differences, helping select which model to use, and determining how seizures may affect or be affected by treatments applied after stroke.
Literature
1.
go back to reference Broderick JP, Phillips SJ, Whisnant JP, O'Fallon WM, Bergstralh EJ. Incidence rates of stroke in the eighties: the end of the decline in stroke? Stroke. 1989;20(5):577–82.PubMedCrossRef Broderick JP, Phillips SJ, Whisnant JP, O'Fallon WM, Bergstralh EJ. Incidence rates of stroke in the eighties: the end of the decline in stroke? Stroke. 1989;20(5):577–82.PubMedCrossRef
3.
go back to reference Passero S, Rocchi R, Rossi S, Ulivelli M, Vatti G. Seizures after spontaneous supratentorial intracerebral hemorrhage. Epilepsia. 2002;43(10):1175–80.PubMedCrossRef Passero S, Rocchi R, Rossi S, Ulivelli M, Vatti G. Seizures after spontaneous supratentorial intracerebral hemorrhage. Epilepsia. 2002;43(10):1175–80.PubMedCrossRef
4.
go back to reference Bladin CF, Alexandrov AV, Bellavance A, Bornstein N, Chambers B, Cote R, etal. Seizures after stroke: a prospective multicenter study. Arch Neurol. 2000;57(11):1617–22. Bladin CF, Alexandrov AV, Bellavance A, Bornstein N, Chambers B, Cote R, etal. Seizures after stroke: a prospective multicenter study. Arch Neurol. 2000;57(11):1617–22.
7.
go back to reference Meldrum BS, Nilsson B. Cerebral blood flow and metabolic rate early and late in prolonged epileptic seizures induced in rats by bicuculline. Brain. 1976;99(3):523–42.PubMedCrossRef Meldrum BS, Nilsson B. Cerebral blood flow and metabolic rate early and late in prolonged epileptic seizures induced in rats by bicuculline. Brain. 1976;99(3):523–42.PubMedCrossRef
8.
go back to reference Goodman JH, Homan RW, Crawford IL. Kindled seizures elevate blood pressure and induce cardiac arrhythmias. Epilepsia. 1990;31(5):489–95.PubMedCrossRef Goodman JH, Homan RW, Crawford IL. Kindled seizures elevate blood pressure and induce cardiac arrhythmias. Epilepsia. 1990;31(5):489–95.PubMedCrossRef
9.
go back to reference Vespa PM, Miller C, McArthur D, Eliseo M, Etchepare M, Hirt D, etal. Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med. 2007;35(12):2830–6. Vespa PM, Miller C, McArthur D, Eliseo M, Etchepare M, Hirt D, etal. Nonconvulsive electrographic seizures after traumatic brain injury result in a delayed, prolonged increase in intracranial pressure and metabolic crisis. Crit Care Med. 2007;35(12):2830–6.
11.
go back to reference Alberti A, Paciaroni M, Caso V, Venti M, Palmerini F, Agnelli G. Early seizures in patients with acute stroke: frequency, predictive factors, and effect on clinical outcome. Vasc Health Risk Manag. 2008;4(3):715–20.PubMedCentralPubMed Alberti A, Paciaroni M, Caso V, Venti M, Palmerini F, Agnelli G. Early seizures in patients with acute stroke: frequency, predictive factors, and effect on clinical outcome. Vasc Health Risk Manag. 2008;4(3):715–20.PubMedCentralPubMed
12.
go back to reference Arboix A, Garcia-Eroles L, Massons JB, Oliveres M, Comes E. Predictive factors of early seizures after acute cerebrovascular disease. Stroke. 1997;28(8):1590–4.PubMedCrossRef Arboix A, Garcia-Eroles L, Massons JB, Oliveres M, Comes E. Predictive factors of early seizures after acute cerebrovascular disease. Stroke. 1997;28(8):1590–4.PubMedCrossRef
15.
go back to reference Morgenstern LB, Hemphill 3rd JC, Anderson C, Becker K, Broderick JP, Connolly Jr ES, etal. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2010;41(9):2108–29. doi:10.1161/STR.0b013e3181ec611b. Morgenstern LB, Hemphill 3rd JC, Anderson C, Becker K, Broderick JP, Connolly Jr ES, etal. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2010;41(9):2108–29. doi:10.​1161/​STR.​0b013e3181ec611b​.
16.
19.
go back to reference Lee KR, Drury I, Vitarbo E, Hoff JT. Seizures induced by intracerebral injection of thrombin: a model of intracerebral hemorrhage. J Neurosurg. 1997;87(1):73–8.PubMedCrossRef Lee KR, Drury I, Vitarbo E, Hoff JT. Seizures induced by intracerebral injection of thrombin: a model of intracerebral hemorrhage. J Neurosurg. 1997;87(1):73–8.PubMedCrossRef
21.
go back to reference Bullock R, Mendelow AD, Teasdale GM, Graham DI. Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol Res. 1984;6(4):184–8.PubMed Bullock R, Mendelow AD, Teasdale GM, Graham DI. Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol Res. 1984;6(4):184–8.PubMed
22.
go back to reference Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke. 1990;21(5):801–7.PubMedCrossRef Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke. 1990;21(5):801–7.PubMedCrossRef
23.
go back to reference MacLellan CL, Silasi G, Poon CC, Edmundson CL, Buist R, Peeling J, etal. Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J Cereb Blood Flow Metab. 2008;28:516–25. doi:10.1038/sj.jcbfm.9600548. MacLellan CL, Silasi G, Poon CC, Edmundson CL, Buist R, Peeling J, etal. Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J Cereb Blood Flow Metab. 2008;28:516–25. doi:10.​1038/​sj.​jcbfm.​9600548.
24.
go back to reference MacLellan CL, Auriat AM, McGie SC, Yan RH, Huynh HD, De Butte MF, etal. Gauging recovery after hemorrhagic stroke in rats: implications for cytoprotection studies. J Cereb Blood Flow Metab. 2006;26:1031–42. MacLellan CL, Auriat AM, McGie SC, Yan RH, Huynh HD, De Butte MF, etal. Gauging recovery after hemorrhagic stroke in rats: implications for cytoprotection studies. J Cereb Blood Flow Metab. 2006;26:1031–42.
25.
go back to reference Colbourne F, Auer RN, Sutherland G. Characterization of postischemic behavioral deficits in gerbils with and without hypothermic neuroprotection. Brain Res. 1998;803:69–78.PubMedCrossRef Colbourne F, Auer RN, Sutherland G. Characterization of postischemic behavioral deficits in gerbils with and without hypothermic neuroprotection. Brain Res. 1998;803:69–78.PubMedCrossRef
27.
go back to reference Nakamura T, Keep RF, Hua Y, Nagao S, Hoff JT, Xi G. Iron-induced oxidative brain injury after experimental intracerebral hemorrhage. Acta Neurochir Suppl. 2006;96:194–8.PubMedCrossRef Nakamura T, Keep RF, Hua Y, Nagao S, Hoff JT, Xi G. Iron-induced oxidative brain injury after experimental intracerebral hemorrhage. Acta Neurochir Suppl. 2006;96:194–8.PubMedCrossRef
28.
go back to reference Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.PubMedCrossRef Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–5.PubMedCrossRef
31.
32.
34.
go back to reference Hartings JA, Williams AJ, Tortella FC. Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent rhythmic delta activity in rat focal ischemia. Exp Neurol. 2003;179(2):139–49.PubMedCrossRef Hartings JA, Williams AJ, Tortella FC. Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent rhythmic delta activity in rat focal ischemia. Exp Neurol. 2003;179(2):139–49.PubMedCrossRef
35.
go back to reference MacLellan CL, Paquette R, Colbourne F. A critical appraisal of experimental intracerebral hemorrhage research. J Cereb Blood Flow Metab. 2012;32:612–7.PubMedCentralPubMedCrossRef MacLellan CL, Paquette R, Colbourne F. A critical appraisal of experimental intracerebral hemorrhage research. J Cereb Blood Flow Metab. 2012;32:612–7.PubMedCentralPubMedCrossRef
37.
go back to reference Barratt HE, Lanman TA, Carmichael ST. Mouse intracerebral hemorrhage models produce different degrees of initial and delayed damage, axonal sprouting, and recovery. J Cereb Blood Flow Metab. 2014. doi:10.1038/jcbfm.2014.107.PubMed Barratt HE, Lanman TA, Carmichael ST. Mouse intracerebral hemorrhage models produce different degrees of initial and delayed damage, axonal sprouting, and recovery. J Cereb Blood Flow Metab. 2014. doi:10.​1038/​jcbfm.​2014.​107.PubMed
39.
go back to reference Auriat AM, Silasi G, Wei Z, Paquette R, Paterson P, Nichol H, etal. Ferric iron chelation lowers brain iron levels after intracerebral hemorrhage in rats but does not improve outcome. Exp Neurol. 2012;234:136–43. doi:10.1016/j.expneurol.2011.12.030. Auriat AM, Silasi G, Wei Z, Paquette R, Paterson P, Nichol H, etal. Ferric iron chelation lowers brain iron levels after intracerebral hemorrhage in rats but does not improve outcome. Exp Neurol. 2012;234:136–43. doi:10.​1016/​j.​expneurol.​2011.​12.​030.
40.
41.
go back to reference Song S, Hua Y, Keep RF, He Y, Wang J, Wu J, etal. Deferoxamine reduces brain swelling in a rat model of hippocampal intracerebral hemorrhage. Acta Neurochir Suppl. 2008;105:13–8. Song S, Hua Y, Keep RF, He Y, Wang J, Wu J, etal. Deferoxamine reduces brain swelling in a rat model of hippocampal intracerebral hemorrhage. Acta Neurochir Suppl. 2008;105:13–8.
42.
go back to reference Adeoye O, Clark JF, Khatri P, Wagner KR, Zuccarello M, Pyne-Geithman GJ. Do current animal models of intracerebral hemorrhage mirror the human pathology? Transl Stroke Res. 2010;in press. Adeoye O, Clark JF, Khatri P, Wagner KR, Zuccarello M, Pyne-Geithman GJ. Do current animal models of intracerebral hemorrhage mirror the human pathology? Transl Stroke Res. 2010;in press.
46.
go back to reference Ninds ICH Workshop. Priorities for clinical research in intracerebral hemorrhage: report from a National Institute of Neurological Disorders and Stroke workshop. Stroke. 2005;36(3):e23–41.CrossRef Ninds ICH Workshop. Priorities for clinical research in intracerebral hemorrhage: report from a National Institute of Neurological Disorders and Stroke workshop. Stroke. 2005;36(3):e23–41.CrossRef
Metadata
Title
Seizure Activity Occurs in the Collagenase but not the Blood Infusion Model of Striatal Hemorrhagic Stroke in Rats
Authors
Ana C. Klahr
Clayton T. Dickson
Frederick Colbourne
Publication date
01-02-2015
Publisher
Springer US
Published in
Translational Stroke Research / Issue 1/2015
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-014-0361-y

Other articles of this Issue 1/2015

Translational Stroke Research 1/2015 Go to the issue