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Erschienen in: Translational Stroke Research 5/2019

15.11.2018 | Original Article

The Acute Phase of Experimental Subarachnoid Hemorrhage: Intracranial Pressure Dynamics and Their Effect on Cerebral Blood Flow and Autoregulation

verfasst von: Catharina Conzen, Katrin Becker, Walid Albanna, Miriam Weiss, Annika Bach, Nyanda Lushina, André Steimers, Sarah Pinkernell, Hans Clusmann, Ute Lindauer, Gerrit A. Schubert

Erschienen in: Translational Stroke Research | Ausgabe 5/2019

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Abstract

Clinical presentation and neurological outcome in subarachnoid hemorrhage (SAH) is highly variable. Aneurysmal SAH (aSAH) is hallmarked by sudden increase of intracranial pressure (ICP) and acute hypoperfusion contributing to early brain injury (EBI) and worse outcome, while milder or non-aneurysmal SAH with comparable amount of blood are associated with better neurological outcome, possibly due to less dramatic changes in ICP. Acute pressure dynamics may therefore be an important pathophysiological aspect determining neurological complications and outcome. We investigated the influence of ICP variability on acute changes after SAH by modulating injection velocity and composition in an experimental model of SAH. Five hundred microliters of arterial blood (AB) or normal saline (NS) were injected intracisternally over 1 (AB1, NS1), 10 (AB10, NS10), or 30 min (AB30) with monitoring for 6 h (n = 68). Rapid blood injection resulted in highest ICP peaks (AB1 median 142.7 mmHg [1.Q 116.7–3.Q 230.6], AB30 33.42 mmHg [18.8–38.3], p < 0.001) and most severe hypoperfusion (AB1 16.6% [11.3–30.6], AB30 44.2% [34.8–59.8]; p < 0.05). However, after 30 min, all blood groups showed comparable ICP elevation and prolonged hypoperfusion. Cerebral autoregulation was disrupted initially due to the immediate ICP increase in all groups except NS10; only AB1, however, resulted in sustained impairment of autoregulation, as well as early neuronal cell loss. Rapidity and composition of hemorrhage resulted in characteristic hyperacute hemodynamic changes, with comparable hypoperfusion despite different ICP ranges. Only rapid ICP increase was associated with pronounced and early, but sustained disruption of cerebral autoregulation, possibly contributing to EBI.
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Literatur
1.
Zurück zum Zitat Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet. 2017;389(10069):655–66.CrossRefPubMed Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet. 2017;389(10069):655–66.CrossRefPubMed
2.
Zurück zum Zitat 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(10):2391–5.CrossRefPubMed 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(10):2391–5.CrossRefPubMed
3.
Zurück zum Zitat Schubert GA, Seiz M, Hegewald AA, Manville J, Thome C. Acute hypoperfusion immediately after subarachnoid hemorrhage: a xenon contrast-enhanced CT study. J Neurotrauma. 2009;26(12):2225–31.CrossRefPubMed Schubert GA, Seiz M, Hegewald AA, Manville J, Thome C. Acute hypoperfusion immediately after subarachnoid hemorrhage: a xenon contrast-enhanced CT study. J Neurotrauma. 2009;26(12):2225–31.CrossRefPubMed
4.
Zurück zum Zitat Schubert GA, Seiz M, Hegewald AA, Manville J, Thome C. Hypoperfusion in the acute phase of subarachnoid hemorrhage. Acta Neurochir Suppl. 2011;110(Pt 1):35–8.PubMed Schubert GA, Seiz M, Hegewald AA, Manville J, Thome C. Hypoperfusion in the acute phase of subarachnoid hemorrhage. Acta Neurochir Suppl. 2011;110(Pt 1):35–8.PubMed
5.
Zurück zum Zitat Westermaier T, Jauss A, Eriskat J, Kunze E, Roosen K. Acute vasoconstriction: decrease and recovery of cerebral blood flow after various intensities of experimental subarachnoid hemorrhage in rats. J Neurosurg. 2009;110(5):996–1002.CrossRefPubMed Westermaier T, Jauss A, Eriskat J, Kunze E, Roosen K. Acute vasoconstriction: decrease and recovery of cerebral blood flow after various intensities of experimental subarachnoid hemorrhage in rats. J Neurosurg. 2009;110(5):996–1002.CrossRefPubMed
6.
Zurück zum Zitat Westermaier T, Jauss A, Eriskat J, Kunze E, Roosen K. Time-course of cerebral perfusion and tissue oxygenation in the first 6 h after experimental subarachnoid hemorrhage in rats. J Cereb Blood Flow Metab. 2009;29(4):771–9.CrossRefPubMed Westermaier T, Jauss A, Eriskat J, Kunze E, Roosen K. Time-course of cerebral perfusion and tissue oxygenation in the first 6 h after experimental subarachnoid hemorrhage in rats. J Cereb Blood Flow Metab. 2009;29(4):771–9.CrossRefPubMed
7.
Zurück zum Zitat Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery. 1998;42(2):352–60 discussion 60-2.CrossRefPubMed Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery. 1998;42(2):352–60 discussion 60-2.CrossRefPubMed
8.
Zurück zum Zitat Chen S, Feng H, Sherchan P, Klebe D, Zhao G, Sun X, et al. Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog Neurobiol. 2014;115:64–91.CrossRefPubMed Chen S, Feng H, Sherchan P, Klebe D, Zhao G, Sun X, et al. Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog Neurobiol. 2014;115:64–91.CrossRefPubMed
9.
10.
Zurück zum Zitat Foreman B. The pathophysiology of delayed cerebral ischemia. J Clin Neurophysiol. 2016;33(3):174–82.CrossRefPubMed Foreman B. The pathophysiology of delayed cerebral ischemia. J Clin Neurophysiol. 2016;33(3):174–82.CrossRefPubMed
11.
Zurück zum Zitat Rouchaud A, Lehman VT, Murad MH, Burrows A, Cloft HJ, Lindell EP, et al. Nonaneurysmal perimesencephalic hemorrhage is associated with deep cerebral venous drainage anomalies: a systematic literature review and meta-analysis. AJNR Am J Neuroradiol. 2016;37(9):1657–63.CrossRefPubMedPubMedCentral Rouchaud A, Lehman VT, Murad MH, Burrows A, Cloft HJ, Lindell EP, et al. Nonaneurysmal perimesencephalic hemorrhage is associated with deep cerebral venous drainage anomalies: a systematic literature review and meta-analysis. AJNR Am J Neuroradiol. 2016;37(9):1657–63.CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Suwatcharangkoon S, Meyers E, Falo C, Schmidt JM, Agarwal S, Claassen J, et al. Loss of consciousness at onset of subarachnoid hemorrhage as an important marker of early brain injury. JAMA Neurol. 2016;73(1):28–35.CrossRefPubMed Suwatcharangkoon S, Meyers E, Falo C, Schmidt JM, Agarwal S, Claassen J, et al. Loss of consciousness at onset of subarachnoid hemorrhage as an important marker of early brain injury. JAMA Neurol. 2016;73(1):28–35.CrossRefPubMed
13.
Zurück zum Zitat Marbacher S, Neuschmelting V, Andereggen L, Widmer HR, von Gunten M, Takala J, et al. Early brain injury linearly correlates with reduction in cerebral perfusion pressure during the hyperacute phase of subarachnoid hemorrhage. Intensive Care Med Exp. 2014;2(1):30.CrossRefPubMedPubMedCentral Marbacher S, Neuschmelting V, Andereggen L, Widmer HR, von Gunten M, Takala J, et al. Early brain injury linearly correlates with reduction in cerebral perfusion pressure during the hyperacute phase of subarachnoid hemorrhage. Intensive Care Med Exp. 2014;2(1):30.CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg. 2005;102(6):1046–54.CrossRefPubMed Prunell GF, Svendgaard NA, Alkass K, Mathiesen T. Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J Neurosurg. 2005;102(6):1046–54.CrossRefPubMed
15.
Zurück zum Zitat Santos GA, Petersen N, Zamani AA, Du R, LaRose S, Monk A, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.CrossRefPubMedPubMedCentral Santos GA, Petersen N, Zamani AA, Du R, LaRose S, Monk A, et al. Pathophysiologic differences in cerebral autoregulation after subarachnoid hemorrhage. Neurology. 2016;86(21):1950–6.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Budohoski KP, Czosnyka M, Smielewski P, Kasprowicz M, Helmy A, Bulters D, et al. Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke. 2012;43(12):3230–7.CrossRefPubMed Budohoski KP, Czosnyka M, Smielewski P, Kasprowicz M, Helmy A, Bulters D, et al. Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke. 2012;43(12):3230–7.CrossRefPubMed
17.
Zurück zum Zitat Jaeger M, Soehle M, Schuhmann MU, Meixensberger J. Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke. 2012;43(8):2097–101.CrossRefPubMed Jaeger M, Soehle M, Schuhmann MU, Meixensberger J. Clinical significance of impaired cerebrovascular autoregulation after severe aneurysmal subarachnoid hemorrhage. Stroke. 2012;43(8):2097–101.CrossRefPubMed
18.
Zurück zum Zitat Budohoski KP, Czosnyka M, Kirkpatrick PJ, Smielewski P, Steiner LA, Pickard JD. Clinical relevance of cerebral autoregulation following subarachnoid haemorrhage. Nat Rev Neurol. 2013;9(3):152–63.CrossRefPubMed Budohoski KP, Czosnyka M, Kirkpatrick PJ, Smielewski P, Steiner LA, Pickard JD. Clinical relevance of cerebral autoregulation following subarachnoid haemorrhage. Nat Rev Neurol. 2013;9(3):152–63.CrossRefPubMed
19.
Zurück zum Zitat Schmieder K, Moller F, Engelhardt M, Scholz M, Schregel W, Christmann A, et al. Dynamic cerebral autoregulation in patients with ruptured and unruptured aneurysms after induction of general anesthesia. Zentralblatt fur Neurochirurgie. 2006;67(2):81–7.CrossRefPubMed Schmieder K, Moller F, Engelhardt M, Scholz M, Schregel W, Christmann A, et al. Dynamic cerebral autoregulation in patients with ruptured and unruptured aneurysms after induction of general anesthesia. Zentralblatt fur Neurochirurgie. 2006;67(2):81–7.CrossRefPubMed
20.
Zurück zum Zitat Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke. 2007;38(3):981–6.CrossRefPubMed Jaeger M, Schuhmann MU, Soehle M, Nagel C, Meixensberger J. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke. 2007;38(3):981–6.CrossRefPubMed
21.
Zurück zum Zitat Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412.CrossRefPubMedPubMedCentral Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Schubert GA, Poli S, Mendelowitsch A, Schilling L, Thome C. Hypothermia reduces early hypoperfusion and metabolic alterations during the acute phase of massive subarachnoid hemorrhage: a laser-Doppler-flowmetry and microdialysis study in rats. J Neurotrauma. 2008;25(5):539–48.CrossRefPubMed Schubert GA, Poli S, Mendelowitsch A, Schilling L, Thome C. Hypothermia reduces early hypoperfusion and metabolic alterations during the acute phase of massive subarachnoid hemorrhage: a laser-Doppler-flowmetry and microdialysis study in rats. J Neurotrauma. 2008;25(5):539–48.CrossRefPubMed
23.
Zurück zum Zitat Steimers A, Gramer M, Takagaki M, Graf R, Lindauer U, Kohl-Bareis M. Simultaneous imaging of cortical blood flow and haemoglobin concentration with LASCA and RGB reflectometry. Adv Exp Med Biol. 2013;789:427–33.CrossRefPubMed Steimers A, Gramer M, Takagaki M, Graf R, Lindauer U, Kohl-Bareis M. Simultaneous imaging of cortical blood flow and haemoglobin concentration with LASCA and RGB reflectometry. Adv Exp Med Biol. 2013;789:427–33.CrossRefPubMed
24.
Zurück zum Zitat Sugawara T, Ayer R, Jadhav V, Zhang JH. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods. 2008;167(2):327–34.CrossRefPubMed Sugawara T, Ayer R, Jadhav V, Zhang JH. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods. 2008;167(2):327–34.CrossRefPubMed
26.
Zurück zum Zitat Czosnyka M, Smielewski P, Kirkpatrick P, Laing RJ, Menon D, Pickard JD. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery. 1997;41(1):11–7 discussion 7-9.CrossRefPubMed Czosnyka M, Smielewski P, Kirkpatrick P, Laing RJ, Menon D, Pickard JD. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery. 1997;41(1):11–7 discussion 7-9.CrossRefPubMed
27.
Zurück zum Zitat Donnelly J, Budohoski KP, Smielewski P, Czosnyka M. Regulation of the cerebral circulation: bedside assessment and clinical implications. Crit Care. 2016;20(1):129.CrossRefPubMedPubMedCentral Donnelly J, Budohoski KP, Smielewski P, Czosnyka M. Regulation of the cerebral circulation: bedside assessment and clinical implications. Crit Care. 2016;20(1):129.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Sanchez-Porras R, Santos E, Czosnyka M, Zheng Z, Unterberg AW, Sakowitz OW. ‘Long’ pressure reactivity index (L-PRx) as a measure of autoregulation correlates with outcome in traumatic brain injury patients. Acta Neurochir. 2012;154(9):1575–81.CrossRefPubMed Sanchez-Porras R, Santos E, Czosnyka M, Zheng Z, Unterberg AW, Sakowitz OW. ‘Long’ pressure reactivity index (L-PRx) as a measure of autoregulation correlates with outcome in traumatic brain injury patients. Acta Neurochir. 2012;154(9):1575–81.CrossRefPubMed
29.
Zurück zum Zitat Salary M, Quigley MR, Wilberger JE Jr. Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg. 2007;107(1):13–7.CrossRefPubMed Salary M, Quigley MR, Wilberger JE Jr. Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg. 2007;107(1):13–7.CrossRefPubMed
30.
Zurück zum Zitat Konczalla J, Schmitz J, Kashefiolasl S, Senft C, Seifert V, Platz J. Non-aneurysmal subarachnoid hemorrhage in 173 patients: a prospective study of long-term outcome. Eur J Neurol. 2015;22(10):1329–36.CrossRefPubMed Konczalla J, Schmitz J, Kashefiolasl S, Senft C, Seifert V, Platz J. Non-aneurysmal subarachnoid hemorrhage in 173 patients: a prospective study of long-term outcome. Eur J Neurol. 2015;22(10):1329–36.CrossRefPubMed
31.
Zurück zum Zitat Raya A, Zipfel GJ, Diringer MN, Dacey RG Jr, Derdeyn CP, Rich KM, et al. Pattern not volume of bleeding predicts angiographic vasospasm in nonaneurysmal subarachnoid hemorrhage. Stroke. 2014;45(1):265–7.CrossRefPubMed Raya A, Zipfel GJ, Diringer MN, Dacey RG Jr, Derdeyn CP, Rich KM, et al. Pattern not volume of bleeding predicts angiographic vasospasm in nonaneurysmal subarachnoid hemorrhage. Stroke. 2014;45(1):265–7.CrossRefPubMed
32.
Zurück zum Zitat Kapadia A, Schweizer TA, Spears J, Cusimano M, Macdonald RL. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: diagnosis, pathophysiology, clinical characteristics, and long-term outcome. World Neurosurg. 2014;82(6):1131–43.CrossRefPubMed Kapadia A, Schweizer TA, Spears J, Cusimano M, Macdonald RL. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: diagnosis, pathophysiology, clinical characteristics, and long-term outcome. World Neurosurg. 2014;82(6):1131–43.CrossRefPubMed
33.
Zurück zum Zitat Dickinson CJ. Reappraisal of the Cushing reflex: the most powerful neural blood pressure stabilizing system. Clin Sci. 1990;79(6):543–50.CrossRef Dickinson CJ. Reappraisal of the Cushing reflex: the most powerful neural blood pressure stabilizing system. Clin Sci. 1990;79(6):543–50.CrossRef
34.
Zurück zum Zitat Sorrentino E, Diedler J, Kasprowicz M, Budohoski KP, Haubrich C, Smielewski P, et al. Critical thresholds for cerebrovascular reactivity after traumatic brain injury. Neurocrit Care. 2012;16(2):258–66.CrossRefPubMed Sorrentino E, Diedler J, Kasprowicz M, Budohoski KP, Haubrich C, Smielewski P, et al. Critical thresholds for cerebrovascular reactivity after traumatic brain injury. Neurocrit Care. 2012;16(2):258–66.CrossRefPubMed
35.
Zurück zum Zitat Bijlenga P, Czosnyka M, Budohoski KP, Soehle M, Pickard JD, Kirkpatrick PJ, et al. “Optimal cerebral perfusion pressure” in poor grade patients after subarachnoid hemorrhage. Neurocrit Care. 2010;13(1):17–23.CrossRefPubMed Bijlenga P, Czosnyka M, Budohoski KP, Soehle M, Pickard JD, Kirkpatrick PJ, et al. “Optimal cerebral perfusion pressure” in poor grade patients after subarachnoid hemorrhage. Neurocrit Care. 2010;13(1):17–23.CrossRefPubMed
36.
Zurück zum Zitat Ebel H, Rust DS, Leschinger A, Ehresmann N, Kranz A, Hoffmann O, et al. Vasomotion, regional cerebral blood flow and intracranial pressure after induced subarachnoid haemorrhage in rats. Zentralblatt fur Neurochirurgie. 1996;57(3):150–5.PubMed Ebel H, Rust DS, Leschinger A, Ehresmann N, Kranz A, Hoffmann O, et al. Vasomotion, regional cerebral blood flow and intracranial pressure after induced subarachnoid haemorrhage in rats. Zentralblatt fur Neurochirurgie. 1996;57(3):150–5.PubMed
37.
Zurück zum Zitat Steiner L, Lofgren J, Zwetnow NN. Lethal mechanism in repeated subarachnoid hemorrhage in dogs. Acta Neurol Scand. 1975;52(4):268–93.CrossRefPubMed Steiner L, Lofgren J, Zwetnow NN. Lethal mechanism in repeated subarachnoid hemorrhage in dogs. Acta Neurol Scand. 1975;52(4):268–93.CrossRefPubMed
38.
Zurück zum Zitat Lee JY, Sagher O, Keep R, Hua Y, Xi G. Comparison of experimental rat models of early brain injury after subarachnoid hemorrhage. Neurosurgery. 2009;65(2):331–43 discussion 43.CrossRefPubMed Lee JY, Sagher O, Keep R, Hua Y, Xi G. Comparison of experimental rat models of early brain injury after subarachnoid hemorrhage. Neurosurgery. 2009;65(2):331–43 discussion 43.CrossRefPubMed
39.
Zurück zum Zitat Fragata I, Canto-Moreira N, Canhao P. Comparison of cerebral perfusion in perimesencephalic subarachnoid hemorrhage and aneurysmal subarachnoid hemorrhage. Neuroradiology. 2018;60(6):609–16.CrossRefPubMed Fragata I, Canto-Moreira N, Canhao P. Comparison of cerebral perfusion in perimesencephalic subarachnoid hemorrhage and aneurysmal subarachnoid hemorrhage. Neuroradiology. 2018;60(6):609–16.CrossRefPubMed
40.
Zurück zum Zitat Bederson JB, Germano IM, Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke. 1995;26(6):1086–91 discussion 91-2.CrossRefPubMed Bederson JB, Germano IM, Guarino L. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke. 1995;26(6):1086–91 discussion 91-2.CrossRefPubMed
41.
Zurück zum Zitat Ansar S, Edvinsson L. Equal contribution of increased intracranial pressure and subarachnoid blood to cerebral blood flow reduction and receptor upregulation after subarachnoid hemorrhage. Laboratory investigation. J Neurosurg. 2009 Nov;111(5):978–87.CrossRefPubMed Ansar S, Edvinsson L. Equal contribution of increased intracranial pressure and subarachnoid blood to cerebral blood flow reduction and receptor upregulation after subarachnoid hemorrhage. Laboratory investigation. J Neurosurg. 2009 Nov;111(5):978–87.CrossRefPubMed
42.
Zurück zum Zitat Boedtkjer E. Acid-base regulation and sensing: accelerators and brakes in metabolic regulation of cerebrovascular tone. J Cereb Blood Flow Metab. 2017:271678X17733868. Boedtkjer E. Acid-base regulation and sensing: accelerators and brakes in metabolic regulation of cerebrovascular tone. J Cereb Blood Flow Metab. 2017:271678X17733868.
43.
Zurück zum Zitat Schain AJ, Melo-Carrillo A, Strassman AM, Burstein R. Cortical spreading depression closes paravascular space and impairs glymphatic flow: implications for migraine headache. J Neurosci. 2017;37(11):2904–15.CrossRefPubMedPubMedCentral Schain AJ, Melo-Carrillo A, Strassman AM, Burstein R. Cortical spreading depression closes paravascular space and impairs glymphatic flow: implications for migraine headache. J Neurosci. 2017;37(11):2904–15.CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Balbi M, Koide M, Schwarzmaier SM, Wellman GC, Plesnila N. Acute changes in neurovascular reactivity after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab. 2015;16. Balbi M, Koide M, Schwarzmaier SM, Wellman GC, Plesnila N. Acute changes in neurovascular reactivity after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab. 2015;16.
45.
Zurück zum Zitat Balbi M, Koide M, Wellman GC, Plesnila N. Inversion of neurovascular coupling after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab. 2017:271678X16686595. Balbi M, Koide M, Wellman GC, Plesnila N. Inversion of neurovascular coupling after subarachnoid hemorrhage in vivo. J Cereb Blood Flow Metab. 2017:271678X16686595.
46.
Zurück zum Zitat Springborg JB, Ma X, Rochat P, Knudsen GM, Amtorp O, Paulson OB, et al. A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol. 2002;135(3):823–9.CrossRefPubMedPubMedCentral Springborg JB, Ma X, Rochat P, Knudsen GM, Amtorp O, Paulson OB, et al. A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol. 2002;135(3):823–9.CrossRefPubMedPubMedCentral
47.
Zurück zum Zitat Yamamoto S, Nishizawa S, Tsukada H, Kakiuchi T, Yokoyama T, Ryu H, et al. Cerebral blood flow autoregulation following subarachnoid hemorrhage in rats: chronic vasospasm shifts the upper and lower limits of the autoregulatory range toward higher blood pressures. Brain Res. 1998;782(1–2):194–201.CrossRefPubMed Yamamoto S, Nishizawa S, Tsukada H, Kakiuchi T, Yokoyama T, Ryu H, et al. Cerebral blood flow autoregulation following subarachnoid hemorrhage in rats: chronic vasospasm shifts the upper and lower limits of the autoregulatory range toward higher blood pressures. Brain Res. 1998;782(1–2):194–201.CrossRefPubMed
49.
Zurück zum Zitat Hollig A, Weinandy A, Nolte K, Clusmann H, Rossaint R, Coburn M. Experimental subarachnoid hemorrhage in rats: comparison of two endovascular perforation techniques with respect to success rate, confounding pathologies and early hippocampal tissue lesion pattern. PLoS One. 2015;10(4):e0123398.CrossRefPubMedPubMedCentral Hollig A, Weinandy A, Nolte K, Clusmann H, Rossaint R, Coburn M. Experimental subarachnoid hemorrhage in rats: comparison of two endovascular perforation techniques with respect to success rate, confounding pathologies and early hippocampal tissue lesion pattern. PLoS One. 2015;10(4):e0123398.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Schneider UC, Davids AM, Brandenburg S, Muller A, Elke A, Magrini S, et al. Microglia inflict delayed brain injury after subarachnoid hemorrhage. Acta Neuropathol. 2015;130(2):215–31.CrossRefPubMed Schneider UC, Davids AM, Brandenburg S, Muller A, Elke A, Magrini S, et al. Microglia inflict delayed brain injury after subarachnoid hemorrhage. Acta Neuropathol. 2015;130(2):215–31.CrossRefPubMed
51.
Zurück zum Zitat Hop JW, Rinkel GJ, Algra A, van Gijn J. Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke. 1999;30(11):2268–71.CrossRefPubMed Hop JW, Rinkel GJ, Algra A, van Gijn J. Initial loss of consciousness and risk of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke. 1999;30(11):2268–71.CrossRefPubMed
52.
Zurück zum Zitat Konczalla J, Platz J, Schuss P, Vatter H, Seifert V, Guresir E. Non-aneurysmal non-traumatic subarachnoid hemorrhage: patient characteristics, clinical outcome and prognostic factors based on a single-center experience in 125 patients. BMC Neurol. 2014;14:140.CrossRefPubMedPubMedCentral Konczalla J, Platz J, Schuss P, Vatter H, Seifert V, Guresir E. Non-aneurysmal non-traumatic subarachnoid hemorrhage: patient characteristics, clinical outcome and prognostic factors based on a single-center experience in 125 patients. BMC Neurol. 2014;14:140.CrossRefPubMedPubMedCentral
53.
Zurück zum Zitat Shimoda M, Hoshikawa K, Shiramizu H, Oda S, Yoshiyama M, Osada T, et al. Early infarction detected by diffusion-weighted imaging in patients with subarachnoid hemorrhage. Acta Neurochir. 2010;152(7):1197–205.CrossRefPubMed Shimoda M, Hoshikawa K, Shiramizu H, Oda S, Yoshiyama M, Osada T, et al. Early infarction detected by diffusion-weighted imaging in patients with subarachnoid hemorrhage. Acta Neurochir. 2010;152(7):1197–205.CrossRefPubMed
54.
Zurück zum Zitat Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery. 2003;52(1):165–75 discussion 75-6.PubMed Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA. Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery. 2003;52(1):165–75 discussion 75-6.PubMed
Metadaten
Titel
The Acute Phase of Experimental Subarachnoid Hemorrhage: Intracranial Pressure Dynamics and Their Effect on Cerebral Blood Flow and Autoregulation
verfasst von
Catharina Conzen
Katrin Becker
Walid Albanna
Miriam Weiss
Annika Bach
Nyanda Lushina
André Steimers
Sarah Pinkernell
Hans Clusmann
Ute Lindauer
Gerrit A. Schubert
Publikationsdatum
15.11.2018
Verlag
Springer US
Erschienen in
Translational Stroke Research / Ausgabe 5/2019
Print ISSN: 1868-4483
Elektronische ISSN: 1868-601X
DOI
https://doi.org/10.1007/s12975-018-0674-3

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