Dynamics of brain perfusion and cognitive performance in revascularization of carotid artery stenosis

Julian Schröder, Marlene Heinze, Matthias Günther, Bastian Cheng, Alina Nickel, Tanja Schröder, Felix Fischer, Simon S Kessner, Tim Magnus, Jens Fiehler, Axel Larena-Avellaneda, Christian Gerloff, Götz Thomalla, Julian Schröder, Marlene Heinze, Matthias Günther, Bastian Cheng, Alina Nickel, Tanja Schröder, Felix Fischer, Simon S Kessner, Tim Magnus, Jens Fiehler, Axel Larena-Avellaneda, Christian Gerloff, Götz Thomalla

Abstract

Introduction: There is evidence suggesting a detrimental effect of asymptomatic carotid artery stenosis on cognitive function even in the absence of ischemic cerebral lesions. Hypoperfusion has been suggested as pathophysiological mechanism causing cognitive impairment. We aimed to assess cognitive performance and cerebral perfusion changes in patients with carotid artery stenosis without ischemic lesions by arterial spin labeling (ASL) and contrast enhanced (CE) perfusion MRI before and after revascularization therapy.

Methods: 17 asymptomatic patients with unilateral high-grade (≥70%) carotid artery stenosis without evidence of structural brain lesions underwent ASL and CE perfusion MRI and cognitive testing (MMSE, DemTect, Clock-Drawing Test, Trail-Making Test, Stroop Test) before and 6-8 weeks after revascularization therapy by endarterectomy or stenting. Multiparametric perfusion maps (ASL: cerebral blood flow (ASL-CBF), bolus arrival time (ASL-BAT); CE: cerebral blood flow (CE-CBF), mean transit time (CE-MTT), cerebral blood volume (CE-CBV)) were calculated and analyzed by vascular territory. Relative perfusion values were calculated.

Results: Multivariate analysis revealed a significant impact of revascularization therapy on all perfusion measures analyzed. At baseline post-hoc testing showed significant hypoperfusion in MCA borderzones as assessed by ASL-CBF, ASL-BAT, CE-MTT and CE-CBV. All perfusion alterations normalized after revascularization. We did not observe any significant correlation of cognitive test results with perfusion parameters. There was no significant change in cognitive performance after revascularization.

Conclusion: We found evidence of traceable perfusion alterations in patients with high grade carotid artery stenosis in the absence of structural brain lesions, which proved fully reversible after revascularization therapy. In this cohort of asymptomatic patients we did not observe an association of hypoperfusion with cognitive performance.

Keywords: Carotid artery stenosis; Carotid artery stenting; Cognitive function; Magnetic resonance imaging; Perfusion imaging.

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
Multi-Slice image of MCA core (blue) and borderzone (red) masks used for perfusion analysis in MNI-2 mm space. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Multi-slice ASL and CE Perfusion maps of a patient with right-sided ICA stenosis before (A) and 6 weeks after (B) endarterectomy. Before revascularization there is a notable increase of ASL-CBF and decrease of ASL-BAT and CE-MTT in the right MCA borderzones (indicated by white arrows), as opposed to ASL-CBF there is no visible change on CE-CBF maps. After TEA hypoperfusion is markedly reduced.
Fig. 3
Fig. 3
Relative ASL-perfusion measures at baseline and after revascularization in ACA, MCA core and border territories. A: ASL relative cerebral blood flow B: ASL Bolus Arrival Time. pre indicates baseline, post 6–8 weeks post intervention. * indicates territories with significant changes of perfusion after revascularization according to post-hoc paired T-Test.
Fig. 4
Fig. 4
Relative CE-perfusion measures at baseline and after revascularization in MCA core (4) and border (5) territories. (A) CE relative cerebral blood flow (CBF) (B) CE mean transit time (MTT) (C) CE cerebral blood volume (CBV). pre indicates baseline, post 6–8 weeks post intervention * indicates territories with significant changes of perfusion after revascularization according to post-hoc paired T-Test. Additionally, baseline perfusion values were assessed by 1-sample t-test against 1 (indicating equal perfusion in both hemispheres). ASL-rBAT on the stenosis side was significantly increased in MCA core and MCA border territories, and ASL-rCBF was significantly reduced in the MCA border territory (see Table 2). CE-rMTT and CE-rCBV were significantly increased ipsilaterally to ICA stenosis. There were no significant changes in CE-rCBF at baseline.

References

    1. Ances B.M., McGarvey M.L., Abrahams J.M. Continuous arterial spin labeled perfusion magnetic resonance imaging in patients before and after carotid endarterectomy. J. Neuroimaging. 2004;14:133–138.
    1. Arvanitakis Z., Capuano A.W., Leurgans S.E. Relation of cerebral vessel disease to Alzheimer's disease dementia and cognitive function in elderly people: a cross-sectional study. Lancet Neurol. 2016;15:934–943.
    1. Bogousslavsky J., Regli F. Unilateral watershed cerebral infarcts. Neurology. 1986;36:373–377.
    1. Bokkers R.P.H., Van Laar P.J., Van De Ven K.C.C. Arterial spin-labeling MR imaging measurements of timing parameters in patients with a carotid artery occlusion. Am. J. Neuroradiol. 2008;29:1698–1703.
    1. Bowie C.R., Harvey P.D. Administration and interpretation of the trail making test. Nat. Protoc. 2006;1:2277–2281.
    1. Chen Y.-H., Lin M.-S., Lee J.-K. Carotid stenting improves cognitive function in asymptomatic cerebral ischemia. Int. J. Cardiol. 2012;157:104–107.
    1. Chen Y.F., Tang S.C., Wu W.C. Alterations of cerebral perfusion in asymptomatic internal carotid artery steno-occlusive disease. Sci. Rep. 2017;7:1–9.
    1. Cheng B., Golsari A., Fiehler J. Dynamics of regional distribution of ischemic lesions in middle cerebral artery trunk occlusion relates to collateral circulation. J. Cereb. Blood Flow Metab. 2010;31:36–40.
    1. Chida K., Ogasawara K., Suga Y. Postoperative cortical neural loss associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy 123I-iomazenil SPECT study. Stroke. 2009;40:448–453.
    1. De La Torre J.C. Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol. 2004;3:184–190.
    1. De Rango P., Caso V., Leys D. The role of carotid artery stenting and carotid endarterectomy in cognitive performance: a systematic review. Stroke. 2008;39:3116–3127.
    1. Folstein M.F., Folstein S.E., McHugh P.R. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975;12:189–198.
    1. Forkert N.D., Cheng B., Kemmling A. ANTONIA perfusion and stroke: a software tool for the multi-purpose analysis of MR perfusion-weighted datasets and quantitative ischemic stroke assessment. Methods Inf. Med. 2014;53:469–481.
    1. Günther M., Oshio K., Feinberg D.A. Single-shot 3D imaging techniques improve arterial spin labeling perfusion measurements. Magn. Reson. Med. 2005;54:491–498.
    1. Heller S., Hines G. Carotid stenosis and impaired cognition: the effect of intervention. Cardiol. Rev. 2017;25:211–214.
    1. Johnston S.C., O'Meara E.S., Manolio T.A. Cognitive impairment and decline are associated with carotid artery disease in patients without clinically evident cerebrovascular disease. Ann. Intern. Med. 2004;140:237–247.
    1. Kalbe E., Kessler J., Calabrese P. DemTect: a new, sensitive cognitive screening test to support the diagnosis of mild cognitive impairment and early dementia. Int. J. Geriatr. Psychiatry. 2004;19:136–143.
    1. Kougias P., Collins R., Pastorek N. Comparison of domain-specific cognitive function after carotid endarterectomy and stenting. J. Vasc. Surg. 2015;62:355–362.
    1. Lal B.K., Dux M.C., Sikdar S. Asymptomatic carotid stenosis is associated with cognitive impairment. J. Vasc. Surg. 2017;66:1083–1092.
    1. Lythgoe D.J., Østergaard L., Williams S.C. Quantitative perfusion imaging in carotid artery stenosis using dynamic susceptibility contrast-enhanced magnetic resonance imaging. Magn. Reson. Imaging. 2000;18:1–11.
    1. Marshall R.S., Asllani I., Pavol M.A. Altered cerebral hemodynamics and cortical thinning in asymptomatic carotid artery stenosis. PloS One. 2017;1:1–14.
    1. Martin S.Z., Madai V.I., Von Samson-Himmelstjerna F.C. 3D GRASE pulsed arterial spin labeling at multiple inflow times in patients with long arterial transit times: comparison with dynamic susceptibility-weighted contrast-enhanced MRI at 3 Tesla. J. Cereb. Blood Flow Metab. 2015;35:392–401.
    1. Mathiesen E.B., Waterloo K., Joakimsen O. Reduced neuropsychological test performance in asymptomatic carotid stenosis: the Tromso study. Neurology. 2004;62:695–701.
    1. Moneta G.L., Edwards J.M., Chitwood R.W. Correlation of North American Symptomatic Carotid Endarterectomy Trial (NASCET) angiographic definition of 70% to 99% internal carotid artery stenosis with duplex scanning. J. Vasc. Surg. 1993;17(152–7) (discussion 157–9)
    1. Mounier-Vehier F., Leys D., Godefroy O. Borderzone infarct subtypes: preliminary study of the presumed mechanism. Eur. Neurol. 1994;34:11–15.
    1. Nael K., Meshksar A., Liebeskind D.S. Periprocedural arterial spin labeling and dynamic susceptibility contrast perfusion in detection of cerebral blood flow in patients with acute ischemic syndrome. Stroke. 2013 Epub ahead of print 6 February 2013.
    1. Nanba T., Ogasawara K., Nishimoto H. Postoperative cerebral white matter damage associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy: a diffusion tensor magnetic resonance imaging study. Cerebrovasc. Dis. 2012;34:358–367.
    1. Oswald W.D., Fleischmann U.M. Hogrefe; Göttingen: 1997. Das Nürnberger-Alters-Inventar.
    1. Rimmele D.L., Larena-Avellaneda A., Alegiani A.C. Real-world experience of treatment decision-making in carotid stenosis in a neurovascular board. Neurology. 2017;89:399–407.
    1. Scherr M., Trinka E., Mc Coy M. Cerebral hypoperfusion during carotid artery stenosis can lead to cognitive deficits that may be independent of white matter lesion load. Curr. Neurovasc. Res. 2012;9:193–199.
    1. Soinne L., Helenius J., Tatlisumak T. Cerebral hemodynamics in asymptomatic and symptomatic patients with high-grade carotid stenosis undergoing carotid endarterectomy. Stroke. 2003;34:1655–1661.
    1. Staikov I.N., Nedeltchev K., Arnold M. Duplex sonographic criteria for measuring carotid stenoses. J. Clin. Ultrasound. 2002;30:275–281.
    1. Tatu L., Moulin T., Bogousslavsky J. Arterial territories of the human brain: cerebral hemispheres. Neurology. 1998;50:1699–1708.
    1. Torvik A. The pathogenesis of watershed infarcts in the brain. Stroke. 1984;15:221–223.
    1. Vermeer S.E., Prins N.D., den Heijer T. Silent brain infarcts and the risk of dementia and cognitive decline. N. Engl. J. Med. 2003;348:1215–1222.
    1. Wang T., Xiao F., Wu G. Impairments in brain perfusion, metabolites, functional connectivity, and cognition in severe asymptomatic carotid stenosis patients: an integrated MRI study. Neural Plast. 2017 Epub ahead of print 2017.
    1. Wang T., Sun D., Liu Y. The impact of carotid artery stenting on cerebral perfusion, functional connectivity, and cognition in severe asymptomatic carotid stenosis patients. Front. Neurol. 2017;8:1–7.
    1. Wang Q, Zhou M, Zhou Y, et al. Effects of carotid endarterectomy on cerebral reperfusion and cognitive function in patients with high grade carotid stenosis: a perfusion weighted magnetic resonance imaging study. Eur. J. Vasc. Endovasc. Surg. Epub ahead of print 2015. DOI: 10.1016/j.ejvs.2015.03.032.
    1. Wendell C.R., Waldstein S.R., Ferrucci L. Carotid atherosclerosis and prospective risk of dementia. Stroke. 2012;43:3319–3324.
    1. Yun T.J., Sohn C.-H., Han M.H. Effect of carotid artery stenting on cerebral blood flow: evaluation of hemodynamic changes using arterial spin labeling. Neuroradiology. 2013;55:271–281.

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