Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage

Arend M. Hamming; Marieke J H Wermer; S. Umesh Rudrapatna; Christian Lanier; Hine J A Van Os; Walter M. Van Den Bergh; Michel D. Ferrari; A van der Toorn; Arn M J M Van Den Maagdenberg; Ann M. Stowe; Rick M. Dijkhuizen

doi:10.1177/0271678X15619189

Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage

Arend M. Hamming, Marieke J H Wermer, S. Umesh Rudrapatna, Christian Lanier, Hine J A Van Os, Walter M. Van Den Bergh, Michel D. Ferrari, A van der Toorn, Arn M J M Van Den Maagdenberg, Ann M. Stowe, Rick M. Dijkhuizen^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Spreading depolarizations may contribute to delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage, but the effect of spreading depolarizations on brain lesion progression after subarachnoid hemorrhage has not yet been assessed directly. Therefore, we tested the hypothesis that artificially induced spreading depolarizations increase brain tissue damage in a rat model of subarachnoid hemorrhage. Subarachnoid hemorrhage was induced by endovascular puncture of the right internal carotid bifurcation. After one day, brain tissue damage was measured with T 2 -weighted MRI, followed by application of 1 M KCl (SD group, N = 16) or saline (no-SD group, N = 16) to the right cortex. Cortical laser-Doppler flowmetry was performed to record spreading depolarizations. MRI was repeated on day 3, after which brains were extracted for assessment of subarachnoid hemorrhage severity and histological damage. 5.0 ± 2.7 spreading depolarizations were recorded in the SD group. Subarachnoid hemorrhage severity and mortality were similar between the SD and no-SD groups. Subarachnoid hemorrhage-induced brain lesions expanded between days 1 and 3. This lesion growth was larger in the SD group (241 ± 233mm³) than in the no-SD group (29 ± 54mm³) (p = 0.001). We conclude that induction of spreading depolarizations significantly advances lesion growth after experimental subarachnoid hemorrhage. Our study underscores the pathophysiological consequence of spreading depolarizations in the development of delayed cerebral tissue injury after subarachnoid hemorrhage.

Original language	English
Pages (from-to)	1224-1231
Number of pages	8
Journal	Journal of Cerebral Blood Flow and Metabolism
Volume	36
Issue number	7
DOIs	https://doi.org/10.1177/0271678X15619189
Publication status	Published - 1 Jul 2016

Keywords

animal models
brain imaging
magnetic resonance
spreading depression
Subarachnoid hemorrhage

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10.1177/0271678X15619189

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Hamming, A. M., Wermer, M. J. H., Umesh Rudrapatna, S., Lanier, C., Van Os, H. J. A., Van Den Bergh, W. M., Ferrari, M. D., van der Toorn, A., Van Den Maagdenberg, A. M. J. M., Stowe, A. M., & Dijkhuizen, R. M. (2016). Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage. Journal of Cerebral Blood Flow and Metabolism, 36(7), 1224-1231. https://doi.org/10.1177/0271678X15619189

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title = "Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage",

abstract = "Spreading depolarizations may contribute to delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage, but the effect of spreading depolarizations on brain lesion progression after subarachnoid hemorrhage has not yet been assessed directly. Therefore, we tested the hypothesis that artificially induced spreading depolarizations increase brain tissue damage in a rat model of subarachnoid hemorrhage. Subarachnoid hemorrhage was induced by endovascular puncture of the right internal carotid bifurcation. After one day, brain tissue damage was measured with T 2 -weighted MRI, followed by application of 1 M KCl (SD group, N = 16) or saline (no-SD group, N = 16) to the right cortex. Cortical laser-Doppler flowmetry was performed to record spreading depolarizations. MRI was repeated on day 3, after which brains were extracted for assessment of subarachnoid hemorrhage severity and histological damage. 5.0 ± 2.7 spreading depolarizations were recorded in the SD group. Subarachnoid hemorrhage severity and mortality were similar between the SD and no-SD groups. Subarachnoid hemorrhage-induced brain lesions expanded between days 1 and 3. This lesion growth was larger in the SD group (241 ± 233mm3) than in the no-SD group (29 ± 54mm3) (p = 0.001). We conclude that induction of spreading depolarizations significantly advances lesion growth after experimental subarachnoid hemorrhage. Our study underscores the pathophysiological consequence of spreading depolarizations in the development of delayed cerebral tissue injury after subarachnoid hemorrhage.",

keywords = "animal models, brain imaging, magnetic resonance, spreading depression, Subarachnoid hemorrhage",

author = "Hamming, {Arend M.} and Wermer, {Marieke J H} and {Umesh Rudrapatna}, S. and Christian Lanier and {Van Os}, {Hine J A} and {Van Den Bergh}, {Walter M.} and Ferrari, {Michel D.} and {van der Toorn}, A and {Van Den Maagdenberg}, {Arn M J M} and Stowe, {Ann M.} and Dijkhuizen, {Rick M.}",

year = "2016",

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doi = "10.1177/0271678X15619189",

language = "English",

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Hamming, AM, Wermer, MJH, Umesh Rudrapatna, S, Lanier, C, Van Os, HJA, Van Den Bergh, WM, Ferrari, MD, van der Toorn, A, Van Den Maagdenberg, AMJM, Stowe, AM & Dijkhuizen, RM 2016, 'Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage', Journal of Cerebral Blood Flow and Metabolism, vol. 36, no. 7, pp. 1224-1231. https://doi.org/10.1177/0271678X15619189

TY - JOUR

T1 - Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage

AU - Hamming, Arend M.

AU - Wermer, Marieke J H

AU - Umesh Rudrapatna, S.

AU - Lanier, Christian

AU - Van Os, Hine J A

AU - Van Den Bergh, Walter M.

AU - Ferrari, Michel D.

AU - van der Toorn, A

AU - Van Den Maagdenberg, Arn M J M

AU - Stowe, Ann M.

AU - Dijkhuizen, Rick M.

PY - 2016/7/1

Y1 - 2016/7/1

N2 - Spreading depolarizations may contribute to delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage, but the effect of spreading depolarizations on brain lesion progression after subarachnoid hemorrhage has not yet been assessed directly. Therefore, we tested the hypothesis that artificially induced spreading depolarizations increase brain tissue damage in a rat model of subarachnoid hemorrhage. Subarachnoid hemorrhage was induced by endovascular puncture of the right internal carotid bifurcation. After one day, brain tissue damage was measured with T 2 -weighted MRI, followed by application of 1 M KCl (SD group, N = 16) or saline (no-SD group, N = 16) to the right cortex. Cortical laser-Doppler flowmetry was performed to record spreading depolarizations. MRI was repeated on day 3, after which brains were extracted for assessment of subarachnoid hemorrhage severity and histological damage. 5.0 ± 2.7 spreading depolarizations were recorded in the SD group. Subarachnoid hemorrhage severity and mortality were similar between the SD and no-SD groups. Subarachnoid hemorrhage-induced brain lesions expanded between days 1 and 3. This lesion growth was larger in the SD group (241 ± 233mm3) than in the no-SD group (29 ± 54mm3) (p = 0.001). We conclude that induction of spreading depolarizations significantly advances lesion growth after experimental subarachnoid hemorrhage. Our study underscores the pathophysiological consequence of spreading depolarizations in the development of delayed cerebral tissue injury after subarachnoid hemorrhage.

AB - Spreading depolarizations may contribute to delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage, but the effect of spreading depolarizations on brain lesion progression after subarachnoid hemorrhage has not yet been assessed directly. Therefore, we tested the hypothesis that artificially induced spreading depolarizations increase brain tissue damage in a rat model of subarachnoid hemorrhage. Subarachnoid hemorrhage was induced by endovascular puncture of the right internal carotid bifurcation. After one day, brain tissue damage was measured with T 2 -weighted MRI, followed by application of 1 M KCl (SD group, N = 16) or saline (no-SD group, N = 16) to the right cortex. Cortical laser-Doppler flowmetry was performed to record spreading depolarizations. MRI was repeated on day 3, after which brains were extracted for assessment of subarachnoid hemorrhage severity and histological damage. 5.0 ± 2.7 spreading depolarizations were recorded in the SD group. Subarachnoid hemorrhage severity and mortality were similar between the SD and no-SD groups. Subarachnoid hemorrhage-induced brain lesions expanded between days 1 and 3. This lesion growth was larger in the SD group (241 ± 233mm3) than in the no-SD group (29 ± 54mm3) (p = 0.001). We conclude that induction of spreading depolarizations significantly advances lesion growth after experimental subarachnoid hemorrhage. Our study underscores the pathophysiological consequence of spreading depolarizations in the development of delayed cerebral tissue injury after subarachnoid hemorrhage.

KW - animal models

KW - brain imaging

KW - magnetic resonance

KW - spreading depression

KW - Subarachnoid hemorrhage

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U2 - 10.1177/0271678X15619189

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SN - 0271-678X

VL - 36

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EP - 1231

JO - Journal of Cerebral Blood Flow and Metabolism

JF - Journal of Cerebral Blood Flow and Metabolism

IS - 7

ER -

Spreading depolarizations increase delayed brain injury in a rat model of subarachnoid hemorrhage

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