Skip to main content
Top
Published in: Clinical Neuroradiology 1/2022

Open Access 01-03-2022 | Carotid Stenosis | Original Article

Comprehensive Evaluation of Cerebral Hemodynamics and Oxygen Metabolism in Revascularization of Asymptomatic High-Grade Carotid Stenosis

Authors: Bernardo Crespo Pimentel, Jan Sedlacik, Julian Schröder, Marlene Heinze, Leif Østergaard, Jens Fiehler, Christian Gerloff, Götz Thomalla, Bastian Cheng

Published in: Clinical Neuroradiology | Issue 1/2022

Login to get access

Abstract

Introduction

Revascularization procedures in carotid artery stenosis have shown a positive effect in the restoration of cerebral oxygen metabolism as assessed by T2’ (T2 prime) imaging as well as capillary homeostasis by measurement of capillary transit time heterogeneity (CTH); however, data in patients with asymptomatic carotid stenosis without manifest brain lesions are scarce.

Patients and Methods

The effect of revascularization on the hemodynamic profile and capillary homeostasis was evaluated in 13 patients with asymptomatic high-grade carotid stenosis without ischemic brain lesions using dynamic susceptibility contrast perfusion imaging and oxygenation-sensitive T2’ mapping before and 6–8 weeks after revascularization by endarterectomy or stenting. The cognitive performance at both timepoints was further assessed.

Results

Perfusion impairment at baseline was accompanied by an increased CTH (p = 0.008) in areas with a time to peak delay ≥ 2 s in the affected hemisphere compared to contralateral regions. Carotid intervention improved the overall moderate hemodynamic impairment at baseline by leading to an increase in normalized cerebral blood flow (p = 0.017) and a decrease in mean transit time (p = 0.027), oxygen extraction capacity (OEC) (p = 0.033) and CTH (p = 0.048). The T2’ values remained unchanged.

Conclusion

This study presents novel evidence of a state of altered microvascular function in patients with high-grade carotid artery stenosis in the absence of ischemic brain lesions, which shows sustained normalization after revascularization procedures.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gorelick PB, Wong KS, Bae HJ, Pandey DK. Large artery intracranial occlusive disease: a large worldwide burden but a relatively neglected frontier. Stroke. 2008;39:2396-9.CrossRef Gorelick PB, Wong KS, Bae HJ, Pandey DK. Large artery intracranial occlusive disease: a large worldwide burden but a relatively neglected frontier. Stroke. 2008;39:2396-9.CrossRef
2.
go back to reference de Weerd M, Greving JP, Hedblad B, Lorenz MW, Mathiesen EB, O’Leary DH, Rosvall M, Sitzer M, Buskens E, Bots ML. Prevalence of asymptomatic carotid artery stenosis in the general population: an individual participant data meta-analysis. Stroke. 2010;41:1294–7.CrossRef de Weerd M, Greving JP, Hedblad B, Lorenz MW, Mathiesen EB, O’Leary DH, Rosvall M, Sitzer M, Buskens E, Bots ML. Prevalence of asymptomatic carotid artery stenosis in the general population: an individual participant data meta-analysis. Stroke. 2010;41:1294–7.CrossRef
3.
go back to reference Inzitari D, Eliasziw M, Gates P, Sharpe BL, Chan RK, Meldrum HE, Barnett HJ. The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 2000;342:1693–700.CrossRef Inzitari D, Eliasziw M, Gates P, Sharpe BL, Chan RK, Meldrum HE, Barnett HJ. The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 2000;342:1693–700.CrossRef
4.
go back to reference Yamauchi H, Fukuyama H, Nagahama Y, Nabatame H, Ueno M, Nishizawa S, Konishi J, Shio H. Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. J Nucl Med. 1999;40:1992–8.PubMed Yamauchi H, Fukuyama H, Nagahama Y, Nabatame H, Ueno M, Nishizawa S, Konishi J, Shio H. Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. J Nucl Med. 1999;40:1992–8.PubMed
5.
go back to reference Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, Wright D, Hurtado-Rua S, Wang Y, Sanelli PC. Oxygen extraction fraction and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2014;35:250–5.CrossRef Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, Wright D, Hurtado-Rua S, Wang Y, Sanelli PC. Oxygen extraction fraction and stroke risk in patients with carotid stenosis or occlusion: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2014;35:250–5.CrossRef
6.
go back to reference Kaczmarz S, Göttler J, Petr J, Hansen MB, Mouridsen K, Zimmer C, Hyder F, Preibisch C. Hemodynamic impairments within individual watershed areas in asymptomatic carotid artery stenosis by multimodal MRI. J Cereb Blood Flow Metab. 2021;41:380–96.CrossRef Kaczmarz S, Göttler J, Petr J, Hansen MB, Mouridsen K, Zimmer C, Hyder F, Preibisch C. Hemodynamic impairments within individual watershed areas in asymptomatic carotid artery stenosis by multimodal MRI. J Cereb Blood Flow Metab. 2021;41:380–96.CrossRef
7.
go back to reference De Bruyn N, Meyer S, Kessner SS, Essers B, Cheng B, Thomalla G, Peeters A, Sunaert S, Duprez T, Thijs V, Feys H, Alaerts K, Verheyden G. Functional network connectivity is altered in patients with upper limb somatosensory impairments in the acute phase post stroke: A cross-sectional study. PLoS One. 2018;13:e0205693.CrossRef De Bruyn N, Meyer S, Kessner SS, Essers B, Cheng B, Thomalla G, Peeters A, Sunaert S, Duprez T, Thijs V, Feys H, Alaerts K, Verheyden G. Functional network connectivity is altered in patients with upper limb somatosensory impairments in the acute phase post stroke: A cross-sectional study. PLoS One. 2018;13:e0205693.CrossRef
8.
go back to reference Lal BK, Dux MC, Sikdar S, Goldstein C, Khan AA, Yokemick J, Zhao L. Asymptomatic carotid stenosis is associated with cognitive impairment. J Vasc Surg. 2017;66:1083–92.CrossRef Lal BK, Dux MC, Sikdar S, Goldstein C, Khan AA, Yokemick J, Zhao L. Asymptomatic carotid stenosis is associated with cognitive impairment. J Vasc Surg. 2017;66:1083–92.CrossRef
9.
go back to reference Mathiesen EB, Waterloo K, Joakimsen O, Bakke SJ, Jacobsen EA, Bønaa KH. Reduced neuropsychological test performance in asymptomatic carotid stenosis: The Tromsø Study. Neurology. 2004;62:695–701.CrossRef Mathiesen EB, Waterloo K, Joakimsen O, Bakke SJ, Jacobsen EA, Bønaa KH. Reduced neuropsychological test performance in asymptomatic carotid stenosis: The Tromsø Study. Neurology. 2004;62:695–701.CrossRef
10.
go back to reference Silvestrini M, Paolino I, Vernieri F, Pedone C, Baruffaldi R, Gobbi B, Cagnetti C, Provinciali L, Bartolini M. Cerebral hemodynamics and cognitive performance in patients with asymptomatic carotid stenosis. Neurology. 2009;72:1062–8.CrossRef Silvestrini M, Paolino I, Vernieri F, Pedone C, Baruffaldi R, Gobbi B, Cagnetti C, Provinciali L, Bartolini M. Cerebral hemodynamics and cognitive performance in patients with asymptomatic carotid stenosis. Neurology. 2009;72:1062–8.CrossRef
11.
go back to reference Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87:9868–72.CrossRef Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87:9868–72.CrossRef
12.
go back to reference Seiler A, Jurcoane A, Magerkurth J, Wagner M, Hattingen E, Deichmann R, Neumann-Haefelin T, Singer OC. T2’ imaging within perfusion-restricted tissue in high-grade occlusive carotid disease. Stroke. 2012;43:1831–6.CrossRef Seiler A, Jurcoane A, Magerkurth J, Wagner M, Hattingen E, Deichmann R, Neumann-Haefelin T, Singer OC. T2’ imaging within perfusion-restricted tissue in high-grade occlusive carotid disease. Stroke. 2012;43:1831–6.CrossRef
13.
go back to reference Seiler A, Kammerer S, Gühl A, Schüre JR, Deichmann R, Nöth U, Pfeilschifter W, Hattingen E, Keese M, Pilatus U, Wagner M. Revascularization of High-Grade Carotid Stenosis Restores Global Cerebral Energy Metabolism. Stroke. 2019;50:1742–50.CrossRef Seiler A, Kammerer S, Gühl A, Schüre JR, Deichmann R, Nöth U, Pfeilschifter W, Hattingen E, Keese M, Pilatus U, Wagner M. Revascularization of High-Grade Carotid Stenosis Restores Global Cerebral Energy Metabolism. Stroke. 2019;50:1742–50.CrossRef
14.
go back to reference Mouridsen K, Friston K, Hjort N, Gyldensted L, Østergaard L, Kiebel S. Bayesian estimation of cerebral perfusion using a physiological model of microvasculature. Neuroimage. 2006;33:570–9.CrossRef Mouridsen K, Friston K, Hjort N, Gyldensted L, Østergaard L, Kiebel S. Bayesian estimation of cerebral perfusion using a physiological model of microvasculature. Neuroimage. 2006;33:570–9.CrossRef
15.
go back to reference Jespersen SN, Østergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J Cereb Blood Flow Metab. 2012;32:264–77.CrossRef Jespersen SN, Østergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J Cereb Blood Flow Metab. 2012;32:264–77.CrossRef
16.
go back to reference Østergaard L, Jespersen SN, Mouridsen K, Mikkelsen IK, Jonsdottír KÝ, Tietze A, Blicher JU, Aamand R, Hjort N, Iversen NK, Cai C, Hougaard KD, Simonsen CZ, Von Weitzel-Mudersbach P, Modrau B, Nagenthiraja K, Riisgaard Ribe L, Hansen MB, Bekke SL, Dahlman MG, Puig J, Pedraza S, Serena J, Cho TH, Siemonsen S, Thomalla G, Fiehler J, Nighoghossian N, Andersen G. The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. J Cereb Blood Flow Metab. 2013;33:635–48.CrossRef Østergaard L, Jespersen SN, Mouridsen K, Mikkelsen IK, Jonsdottír KÝ, Tietze A, Blicher JU, Aamand R, Hjort N, Iversen NK, Cai C, Hougaard KD, Simonsen CZ, Von Weitzel-Mudersbach P, Modrau B, Nagenthiraja K, Riisgaard Ribe L, Hansen MB, Bekke SL, Dahlman MG, Puig J, Pedraza S, Serena J, Cho TH, Siemonsen S, Thomalla G, Fiehler J, Nighoghossian N, Andersen G. The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. J Cereb Blood Flow Metab. 2013;33:635–48.CrossRef
17.
go back to reference Nielsen RB, Egefjord L, Angleys H, Mouridsen K, Gejl M, Møller A, Brock B, Brændgaard H, Gottrup H, Rungby J, Eskildsen SF, Østergaard L. Capillary dysfunction is associated with symptom severity and neurodegeneration in Alzheimer’s disease. Alzheimers Dement. 2017;13:1143–53.CrossRef Nielsen RB, Egefjord L, Angleys H, Mouridsen K, Gejl M, Møller A, Brock B, Brændgaard H, Gottrup H, Rungby J, Eskildsen SF, Østergaard L. Capillary dysfunction is associated with symptom severity and neurodegeneration in Alzheimer’s disease. Alzheimers Dement. 2017;13:1143–53.CrossRef
18.
go back to reference Arsava EM, Hansen MB, Kaplan B, Peker A, Gocmen R, Arat A, Oguz KK, Topcuoglu MA, Østergaard L, Dalkara T. The effect of carotid artery stenting on capillary transit time heterogeneity in patients with carotid artery stenosis. Eur Stroke J. 2018;3:263–71.CrossRef Arsava EM, Hansen MB, Kaplan B, Peker A, Gocmen R, Arat A, Oguz KK, Topcuoglu MA, Østergaard L, Dalkara T. The effect of carotid artery stenting on capillary transit time heterogeneity in patients with carotid artery stenosis. Eur Stroke J. 2018;3:263–71.CrossRef
19.
go back to reference Mundiyanapurath S, Ringleb PA, Diatschuk S, Hansen MB, Mouridsen K, Østergaard L, Wick W, Bendszus M, Radbruch A. Capillary Transit Time Heterogeneity Is Associated with Modified Rankin Scale Score at Discharge in Patients with Bilateral High Grade Internal Carotid Artery Stenosis. PLoS One. 2016;11:e0158148.CrossRef Mundiyanapurath S, Ringleb PA, Diatschuk S, Hansen MB, Mouridsen K, Østergaard L, Wick W, Bendszus M, Radbruch A. Capillary Transit Time Heterogeneity Is Associated with Modified Rankin Scale Score at Discharge in Patients with Bilateral High Grade Internal Carotid Artery Stenosis. PLoS One. 2016;11:e0158148.CrossRef
20.
go back to reference Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, Rankin RN, Clagett GP, Hachinski VC, Sackett DL, Thorpe KE, Meldrum HE, Spence JD. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1998;339:1415–25.CrossRef Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, Rankin RN, Clagett GP, Hachinski VC, Sackett DL, Thorpe KE, Meldrum HE, Spence JD. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 1998;339:1415–25.CrossRef
21.
go back to reference Schröder J, Heinze M, Günther M, Cheng B, Nickel A, Schröder T, Fischer F, Kessner SS, Magnus T, Fiehler J, Larena-Avellaneda A, Gerloff C, Thomalla G. Dynamics of brain perfusion and cognitive performance in revascularization of carotid artery stenosis. Neuroimage Clin. 2019;22:101779.CrossRef Schröder J, Heinze M, Günther M, Cheng B, Nickel A, Schröder T, Fischer F, Kessner SS, Magnus T, Fiehler J, Larena-Avellaneda A, Gerloff C, Thomalla G. Dynamics of brain perfusion and cognitive performance in revascularization of carotid artery stenosis. Neuroimage Clin. 2019;22:101779.CrossRef
22.
go back to reference Mouridsen K, Hansen MB, Østergaard L, Jespersen SN. Reliable estimation of capillary transit time distributions using DSC-MRI. J Cereb Blood Flow Metab. 2014;34:1511–21.CrossRef Mouridsen K, Hansen MB, Østergaard L, Jespersen SN. Reliable estimation of capillary transit time distributions using DSC-MRI. J Cereb Blood Flow Metab. 2014;34:1511–21.CrossRef
23.
go back to reference Mouridsen K, Hansen MB, Østergaard L, Jespersen SN. Reliable estimation of capillary transit time distributions using DSC-MRI. J Cereb Blood Flow Metab. 2014;34:1511–21.CrossRef Mouridsen K, Hansen MB, Østergaard L, Jespersen SN. Reliable estimation of capillary transit time distributions using DSC-MRI. J Cereb Blood Flow Metab. 2014;34:1511–21.CrossRef
24.
go back to reference Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.CrossRef Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55.CrossRef
25.
go back to reference Sedlacik J, Boelmans K, Löbel U, Holst B, Siemonsen S, Fiehler J. Reversible, irreversible and effective transverse relaxation rates in normal aging brain at 3T. Neuroimage. 2014;84:1032–41.CrossRef Sedlacik J, Boelmans K, Löbel U, Holst B, Siemonsen S, Fiehler J. Reversible, irreversible and effective transverse relaxation rates in normal aging brain at 3T. Neuroimage. 2014;84:1032–41.CrossRef
26.
go back to reference Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001;5:143–56.CrossRef Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal. 2001;5:143–56.CrossRef
27.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825–41.CrossRef Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825–41.CrossRef
28.
go back to reference Griffanti L, Zamboni G, Khan A, Li L, Bonifacio G, Sundaresan V, Schulz UG, Kuker W, Battaglini M, Rothwell PM, Jenkinson M. BIANCA (Brain Intensity AbNormality Classification Algorithm): A new tool for automated segmentation of white matter hyperintensities. Neuroimage. 2016;141:191–205.CrossRef Griffanti L, Zamboni G, Khan A, Li L, Bonifacio G, Sundaresan V, Schulz UG, Kuker W, Battaglini M, Rothwell PM, Jenkinson M. BIANCA (Brain Intensity AbNormality Classification Algorithm): A new tool for automated segmentation of white matter hyperintensities. Neuroimage. 2016;141:191–205.CrossRef
29.
go back to reference Tatu L, Moulin T, Bogousslavsky J, Duvernoy H. Arterial territories of the human brain: cerebral hemispheres. Neurology. 1998;50:1699–708.CrossRef Tatu L, Moulin T, Bogousslavsky J, Duvernoy H. Arterial territories of the human brain: cerebral hemispheres. Neurology. 1998;50:1699–708.CrossRef
31.
go back to reference Wilkinson ID, Griffiths PD, Hoggard N, Cleveland TJ, Gaines PA, Macdonald S, McKevitt F, Venables GS. Short-term changes in cerebral microhemodynamics after carotid stenting. AJNR Am J Neuroradiol. 2003;24:1501–7.PubMedPubMedCentral Wilkinson ID, Griffiths PD, Hoggard N, Cleveland TJ, Gaines PA, Macdonald S, McKevitt F, Venables GS. Short-term changes in cerebral microhemodynamics after carotid stenting. AJNR Am J Neuroradiol. 2003;24:1501–7.PubMedPubMedCentral
32.
go back to reference Göttler J, Kaczmarz S, Kallmayer M, Wustrow I, Eckstein HH, Zimmer C, Sorg C, Preibisch C, Hyder F. Flow-metabolism uncoupling in patients with asymptomatic unilateral carotid artery stenosis assessed by multi-modal magnetic resonance imaging. J Cereb Blood Flow Metab. 2019;39:2132–43.CrossRef Göttler J, Kaczmarz S, Kallmayer M, Wustrow I, Eckstein HH, Zimmer C, Sorg C, Preibisch C, Hyder F. Flow-metabolism uncoupling in patients with asymptomatic unilateral carotid artery stenosis assessed by multi-modal magnetic resonance imaging. J Cereb Blood Flow Metab. 2019;39:2132–43.CrossRef
33.
go back to reference Geisler BS, Brandhoff F, Fiehler J, Saager C, Speck O, Röther J, Zeumer H, Kucinski T. Blood-oxygen-level-dependent MRI allows metabolic description of tissue at risk in acute stroke patients. Stroke. 2006;37:1778–84.CrossRef Geisler BS, Brandhoff F, Fiehler J, Saager C, Speck O, Röther J, Zeumer H, Kucinski T. Blood-oxygen-level-dependent MRI allows metabolic description of tissue at risk in acute stroke patients. Stroke. 2006;37:1778–84.CrossRef
34.
go back to reference Seiler A, Deichmann R, Pfeilschifter W, Hattingen E, Singer OC, Wagner M. T2-Imaging to Assess Cerebral Oxygen Extraction Fraction in Carotid Occlusive Disease: Influence of Cerebral Autoregulation and Cerebral Blood Volume. PLoS One. 2016;11:e0161408. Erratum in: PLoS One. 2016;11:e0164749.CrossRef Seiler A, Deichmann R, Pfeilschifter W, Hattingen E, Singer OC, Wagner M. T2-Imaging to Assess Cerebral Oxygen Extraction Fraction in Carotid Occlusive Disease: Influence of Cerebral Autoregulation and Cerebral Blood Volume. PLoS One. 2016;11:e0161408. Erratum in: PLoS One. 2016;11:e0164749.CrossRef
35.
go back to reference Engedal TS, Hjort N, Hougaard KD, Simonsen CZ, Andersen G, Mikkelsen IK, Boldsen JK, Eskildsen SF, Hansen MB, Angleys H, Jespersen SN, Pedraza S, Cho TH, Serena J, Siemonsen S, Thomalla G, Nighoghossian N, Fiehler J, Mouridsen K, Østergaard L. Transit time homogenization in ischemic stroke - A novel biomarker of penumbral microvascular failure? J Cereb Blood Flow Metab. 2018;38:2006–20.CrossRef Engedal TS, Hjort N, Hougaard KD, Simonsen CZ, Andersen G, Mikkelsen IK, Boldsen JK, Eskildsen SF, Hansen MB, Angleys H, Jespersen SN, Pedraza S, Cho TH, Serena J, Siemonsen S, Thomalla G, Nighoghossian N, Fiehler J, Mouridsen K, Østergaard L. Transit time homogenization in ischemic stroke - A novel biomarker of penumbral microvascular failure? J Cereb Blood Flow Metab. 2018;38:2006–20.CrossRef
36.
go back to reference Rasmussen PM, Jespersen SN, Østergaard L. The effects of transit time heterogeneity on brain oxygenation during rest and functional activation. J Cereb Blood Flow Metab. 2015;35:432–42.CrossRef Rasmussen PM, Jespersen SN, Østergaard L. The effects of transit time heterogeneity on brain oxygenation during rest and functional activation. J Cereb Blood Flow Metab. 2015;35:432–42.CrossRef
37.
go back to reference Quandt F, Fischer F, Schröder J, Heinze M, Kessner SS, Malherbe C, Schulz R, Cheng B, Fiehler J, Gerloff C, Thomalla G. Normalization of reduced functional connectivity after revascularization of asymptomatic carotid stenosis. J Cereb Blood Flow Metab. 2020;40:1838–48.CrossRef Quandt F, Fischer F, Schröder J, Heinze M, Kessner SS, Malherbe C, Schulz R, Cheng B, Fiehler J, Gerloff C, Thomalla G. Normalization of reduced functional connectivity after revascularization of asymptomatic carotid stenosis. J Cereb Blood Flow Metab. 2020;40:1838–48.CrossRef
38.
go back to reference Hirsch NM, Toth V, Förschler A, Kooijman H, Zimmer C, Preibisch C. Technical considerations on the validity of blood oxygenation level-dependent-based MR assessment of vascular deoxygenation. NMR Biomed. 2014;27:853–62.CrossRef Hirsch NM, Toth V, Förschler A, Kooijman H, Zimmer C, Preibisch C. Technical considerations on the validity of blood oxygenation level-dependent-based MR assessment of vascular deoxygenation. NMR Biomed. 2014;27:853–62.CrossRef
Metadata
Title
Comprehensive Evaluation of Cerebral Hemodynamics and Oxygen Metabolism in Revascularization of Asymptomatic High-Grade Carotid Stenosis
Authors
Bernardo Crespo Pimentel
Jan Sedlacik
Julian Schröder
Marlene Heinze
Leif Østergaard
Jens Fiehler
Christian Gerloff
Götz Thomalla
Bastian Cheng
Publication date
01-03-2022
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 1/2022
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-021-01077-3

Other articles of this Issue 1/2022

Clinical Neuroradiology 1/2022 Go to the issue

Information

Information