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Published in: Translational Stroke Research 1/2016

01-02-2016 | Original Article

Matched Cohort Analysis of the Effects of Limb Remote Ischemic Conditioning in Patients with Aneurysmal Subarachnoid Hemorrhage

Authors: Azim N. Laiwalla, Yinn Cher Ooi, Raymond Liou, Nestor R. Gonzalez

Published in: Translational Stroke Research | Issue 1/2016

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Abstract

Remote ischemic conditioning (RIC) is a powerful innate response to transient subcritical ischemia that protects against severe ischemic insults at distant sites. We have previously shown the safety and feasibility of limb RIC in aneurysmal subarachnoid hemorrhage (aSAH) patients, along with changes in neurovascular and cerebral metabolism. In this study, we aim to detect the potential effect of an established lower-limb conditioning protocol on clinical outcomes of aSAH patients. Neurologic outcome (modified Rankin Scale (mRS)) of patients enrolled in a prospective trial (RIPC-SAH) was measured. A matching algorithm was applied to identify control patients with aSAH from an institutional departmental database. RIC patients underwent four lower-limb conditioning sessions, consisting of four 5-min cycles per session over nonconsecutive days. Good functional outcome was defined as mRS of 0 to 2. The study population consisted of 21 RIC patients and 61 matched controls. There was no significant intergroup difference in age, gender, aneurysm location, clipping vs coiling, Fisher grades, Hunt and Hess grades, or vasospasm. RIC was independently associated with good outcome (OR 5.17; 95 % confidence interval (CI) 1.21–25.02). RIC also showed a trend toward lower incidence of stroke (28.6 vs. 47.5 %) and death (4.8 vs. 19.7 %). Lower-limb RIC following aSAH appears to have a positive effect in the functional outcomes of patients with aSAH. While this effect is consistent with prior preclinical studies, future trials are necessary to conclusively evaluate the effects of RIC for aSAH.
Literature
2.
go back to reference Zhao H-G, Li W-B, Li Q-J, Chen X-L, Liu H-Q, Feng R-F, et al. Limb ischemic preconditioning attenuates apoptosis of pyramidal neurons in the CA1 hippocampus induced by cerebral ischemia-reperfusion in rats. Sheng Li Xue Bao. 2004;56:407–12.PubMed Zhao H-G, Li W-B, Li Q-J, Chen X-L, Liu H-Q, Feng R-F, et al. Limb ischemic preconditioning attenuates apoptosis of pyramidal neurons in the CA1 hippocampus induced by cerebral ischemia-reperfusion in rats. Sheng Li Xue Bao. 2004;56:407–12.PubMed
6.
go back to reference Bilgin-Freiert A, Dusick JR, Stein NR, Etchepare M, Vespa P, Gonzalez NR. Muscle microdialysis to confirm sublethal ischemia in the induction of remote ischemic preconditioning. Trans Stroke Res. 2012;3:266–72. doi:10.1007/s12975-012-0153-1.CrossRef Bilgin-Freiert A, Dusick JR, Stein NR, Etchepare M, Vespa P, Gonzalez NR. Muscle microdialysis to confirm sublethal ischemia in the induction of remote ischemic preconditioning. Trans Stroke Res. 2012;3:266–72. doi:10.​1007/​s12975-012-0153-1.CrossRef
7.
go back to reference Gonzalez NR, Hamilton R, Bilgin-Freiert A, Dusick J, Vespa P, Hu X, et al. Cerebral hemodynamic and metabolic effects of remote ischemic preconditioning in patients with subarachnoid hemorrhage. Acta Neurochir Suppl. 2013;115:193–8. doi:10.1007/978-3-7091-1192-5_36.PubMed Gonzalez NR, Hamilton R, Bilgin-Freiert A, Dusick J, Vespa P, Hu X, et al. Cerebral hemodynamic and metabolic effects of remote ischemic preconditioning in patients with subarachnoid hemorrhage. Acta Neurochir Suppl. 2013;115:193–8. doi:10.​1007/​978-3-7091-1192-5_​36.PubMed
12.
go back to reference Walsh SR, Nouraei SA, Tang TY, Sadat U, Carpenter RH, Gaunt ME. Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vasc Endovasc Surg. 2010;44:434–9. doi:10.1177/1538574410369709.CrossRef Walsh SR, Nouraei SA, Tang TY, Sadat U, Carpenter RH, Gaunt ME. Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vasc Endovasc Surg. 2010;44:434–9. doi:10.​1177/​1538574410369709​.CrossRef
14.
go back to reference Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20. doi:10.1161/hs0901.095677.CrossRefPubMed Claassen J, Bernardini GL, Kreiter K, Bates J, Du YE, Copeland D, et al. Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke. 2001;32:2012–20. doi:10.​1161/​hs0901.​095677.CrossRefPubMed
15.
16.
go back to reference Gonzalez NR, Boscardin WJ, Glenn T, Vinuela F, Martin NA. Vasospasm probability index: a combination of transcranial Doppler velocities, cerebral blood flow, and clinical risk factors to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2007;107:1101–12. doi:10.3171/JNS-07/12/1101.CrossRefPubMed Gonzalez NR, Boscardin WJ, Glenn T, Vinuela F, Martin NA. Vasospasm probability index: a combination of transcranial Doppler velocities, cerebral blood flow, and clinical risk factors to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2007;107:1101–12. doi:10.​3171/​JNS-07/​12/​1101.CrossRefPubMed
17.
go back to reference Oskouian RJ, Martin NA, Lee JH, Glenn TC, Guthrie D, Gonzalez NR, et al. Multimodal quantitation of the effects of endovascular therapy for vasospasm on cerebral blood flow, transcranial Doppler ultrasonographic velocities, and cerebral artery diameters. Neurosurgery. 2002;51:30–43. doi:10.1097/00006123-200207000-00005.CrossRefPubMed Oskouian RJ, Martin NA, Lee JH, Glenn TC, Guthrie D, Gonzalez NR, et al. Multimodal quantitation of the effects of endovascular therapy for vasospasm on cerebral blood flow, transcranial Doppler ultrasonographic velocities, and cerebral artery diameters. Neurosurgery. 2002;51:30–43. doi:10.​1097/​00006123-200207000-00005.CrossRefPubMed
20.
go back to reference Kelsey JL, Whittemore AS, Evans AS, Thompson WD. Methods in observational epidemiology. New York: Oxford University Press; 1996. Kelsey JL, Whittemore AS, Evans AS, Thompson WD. Methods in observational epidemiology. New York: Oxford University Press; 1996.
21.
go back to reference Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.CrossRefPubMed Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke. 1997;28:660–4.CrossRefPubMed
24.
go back to reference Duckwiler G. Balloon angioplasty and intra-arterial papaverine for vasospasm. J Stroke Cerebrovasc Dis. 1997;6:261–3.CrossRefPubMed Duckwiler G. Balloon angioplasty and intra-arterial papaverine for vasospasm. J Stroke Cerebrovasc Dis. 1997;6:261–3.CrossRefPubMed
25.
go back to reference Vespa PM, Nuwer MR, Juhász 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.CrossRefPubMed Vespa PM, Nuwer MR, Juhász 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.CrossRefPubMed
26.
go back to reference Vespa PM. Acute presentation and early intensive care of acute aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis. 1997;6:230–4.CrossRefPubMed Vespa PM. Acute presentation and early intensive care of acute aneurysmal subarachnoid hemorrhage. J Stroke Cerebrovasc Dis. 1997;6:230–4.CrossRefPubMed
27.
go back to reference Vespa PM, Nenov V, Nuwer MR. Continuous EEG monitoring in the intensive care unit: early findings and clinical efficacy. J Clin Neurophysiol. 1999;16:1–13.CrossRefPubMed Vespa PM, Nenov V, Nuwer MR. Continuous EEG monitoring in the intensive care unit: early findings and clinical efficacy. J Clin Neurophysiol. 1999;16:1–13.CrossRefPubMed
Metadata
Title
Matched Cohort Analysis of the Effects of Limb Remote Ischemic Conditioning in Patients with Aneurysmal Subarachnoid Hemorrhage
Authors
Azim N. Laiwalla
Yinn Cher Ooi
Raymond Liou
Nestor R. Gonzalez
Publication date
01-02-2016
Publisher
Springer US
Published in
Translational Stroke Research / Issue 1/2016
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-015-0437-3

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