Neuroimaging in vascular cognitive impairment: a state-of-the-art review
Tóm tắt
Imaging is critical in the diagnosis and treatment of dementia, particularly in vascular cognitive impairment, due to the visualization of ischemic and hemorrhagic injury of gray and white matter. Magnetic resonance imaging (MRI) and positron emission tomography (PET) provide structural and functional information. Clinical MRI is both generally available and versatile – T2-weighted images show infarcts, FLAIR shows white matter changes and lacunar infarcts, and susceptibility-weighted images reveal microbleeds. Diffusion MRI adds another dimension by showing graded damage to white matter, making it more sensitive to white matter injury than FLAIR. Regions of neuroinflammatory disruption of the blood–brain barrier with increased permeability can be quantified and visualized with dynamic contrast-enhanced MRI. PET shows metabolism of glucose and accumulation of amyloid and tau, which is useful in showing abnormal metabolism in Alzheimer’s disease. Combining MRI and PET allows identification of patients with mixed dementia, with MRI showing white matter injury and PET demonstrating regional impairment of glucose metabolism and deposition of amyloid. Excellent anatomical detail can be observed with 7.0-Tesla MRI. Imaging is the optimal method to follow the effect of treatments since changes in MRI scans are seen prior to those in cognition. This review describes the role of various imaging modalities in the diagnosis and treatment of vascular cognitive impairment.
Tài liệu tham khảo
Rockwood K, Wentzel C, Hachinski V, Hogan DB, MacKnight C, McDowell I. Prevalence and outcomes of vascular cognitive impairment. Vascular Cognitive Impairment Investigators of the Canadian Study of Health and Aging. Neurology. 2000;54(2):447–51.
De Reuck J, Deramecourt V, Cordonnier C, Pasquier F, Leys D, Maurage CA, Bordet R. The incidence of post-mortem neurodegenerative and cerebrovascular pathology in mixed dementia. J Neurol Sci. 2016;366:164–6.
Jellinger KA. The enigma of vascular cognitive disorder and vascular dementia. Acta Neuropathol. 2007;113(4):349–88.
Knopman DS, Parisi JE, Boeve BF, Cha RH, Apaydin H, Salviati A, Edland SD, Rocca WA. Vascular dementia in a population-based autopsy study. Arch Neurol. 2003;60(4):569–75.
Korczyn AD. Mixed dementia--the most common cause of dementia. Ann N Y Acad Sci. 2002;977:129–34.
Rosenberg GA, Bjerke M, Wallin A. Multimodal markers of inflammation in the subcortical ischemic vascular disease type of vascular cognitive impairment. Stroke. 2014;45(5):1531–8.
Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, Launer LJ, Laurent S, Lopez OL, Nyenhuis D, et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2011;42(9):2672–713.
Roman GC, Erkinjuntti T, Wallin A, Pantoni L, Chui HC. Subcortical ischaemic vascular dementia. Lancet Neurol. 2002;1(7):426–36.
Vermeer SE, Longstreth Jr WT, Koudstaal PJ. Silent brain infarcts: a systematic review. Lancet Neurol. 2007;6(7):611–9.
Hunt AL, Orrison WW, Yeo RA, Haaland KY, Rhyne RL, Garry PJ, Rosenberg GA. Clinical significance of MRI white matter lesions in the elderly. Neurology. 1989;39(11):1470–4.
Hachinski VC, Potter P, Merskey H. Leuko-araiosis. Arch Neurol. 1987;44(1):21–3.
Wattjes MP, Henneman WJ, van der Flier WM, de Vries O, Traber F, Geurts JJ, Scheltens P, Vrenken H, Barkhof F. Diagnostic imaging of patients in a memory clinic: comparison of MR imaging and 64-detector row CT. Radiology. 2009;253(1):174–83.
Wahlund LO, Barkhof F, Fazekas F, Bronge L, Augustin M, Sjogren M, Wallin A, Ader H, Leys D, Pantoni L, et al. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke. 2001;32(6):1318–22.
Vitali P, Migliaccio R, Agosta F, Rosen HJ, Geschwind MD. Neuroimaging in dementia. Semin Neurol. 2008;28(4):467–83.
Brainin M, Tuomilehto J, Heiss WD, Bornstein NM, Bath PM, Teuschl Y, Richard E, Guekht A, Quinn T. Post stroke cognition study group. Post-stroke cognitive decline: an update and perspectives for clinical research. Eur J Neurol. 2015;22(2):229–38. e13–6.
Wardlaw JM, Smith EE, Biessels GJ, Cordonnier C, Fazekas F, Frayne R, Lindley RI, O’Brien JT, Barkhof F, Benavente OR, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–38.
Grysiewicz R, Gorelick PB. Key neuroanatomical structures for post-stroke cognitive impairment. Curr Neurol Neurosci Rep. 2012;12(6):703–8.
Roman GC. Senile dementia of the Binswanger type. A vascular form of dementia in the elderly. JAMA. 1987;258(13):1782–8.
Boone KB, Miller BL, Lesser IM, Mehringer CM, Hill Gutierrez E, Goldberg MA, Berman NG. Neuropsychological correlates of white-matter lesions in healthy elderly subjects. A threshold effect. Arch Neurol. 1992;49:549–54.
van Straaten EC, Scheltens P, Knol DL, van Buchem MA, van Dijk EJ, Hofman PA, Karas G, Kjartansson O, de Leeuw FE, Prins ND, et al. Operational definitions for the NINDS-AIREN criteria for vascular dementia: an interobserver study. Stroke. 2003;34(8):1907–12.
Cordonnier C, van der Flier WM, Sluimer JD, Leys D, Barkhof F, Scheltens P. Prevalence and severity of microbleeds in a memory clinic setting. Neurology. 2006;66(9):1356–60.
Koennecke HC. Cerebral microbleeds on MRI: prevalence, associations, and potential clinical implications. Neurology. 2006;66(2):165–71.
De Reuck J, Deramecourt V, Cordonnier C, Leys D, Pasquier F, Maurage CA. Prevalence of small cerebral bleeds in patients with a neurodegenerative dementia: a neuropathological study. J Neurol Sci. 2011;300(1-2):63–6.
De Reuck JL, Auger F, Durieux N, Cordonnier C, Deramecourt V, Pasquier F, Maurage CA, Leys D, Bordet R. The topography of cortical microinfarcts in neurodegenerative diseases and in vascular dementia: a postmortem 7.0-Tesla magnetic resonance imaging study. Eur Neurol. 2016;76(1-2):57–61.
Wardlaw JM, Allerhand M, Doubal FN, Valdes Hernandez M, Morris Z, Gow AJ, Bastin M, Starr JM, Dennis MS, Deary IJ. Vascular risk factors, large-artery atheroma, and brain white matter hyperintensities. Neurology. 2014;82(15):1331–8.
Ihara M, Yamamoto Y. Emerging evidence for pathogenesis of sporadic cerebral small vessel disease. Stroke. 2016;47(2):554–60.
Wardlaw JM. Post-mortem MR, brain imaging comparison with macro- and histopathology: useful, important and underused. Cerebrovasc Dis. 2011;31(5):518–9.
van Veluw SJ, Zwanenburg JJ, Engelen-Lee J, Spliet WG, Hendrikse J, Luijten PR, Biessels GJ. In vivo detection of cerebral cortical microinfarcts with high-resolution 7 T MRI. J Cereb Blood Flow Metab. 2013;33(3):322–9.
Ii Y, Maeda M, Kida H, Matsuo K, Shindo A, Taniguchi A, Tomimoto H. In vivo detection of cortical microinfarcts on ultrahigh-field MRI. J Neuroimaging. 2013;23(1):28–32.
Landi D, Maggio P, Lupoi D, Palazzo P, Altamura C, Falato E, Altavilla R, Vollaro S, Coniglio AD, Tibuzzi F, et al. Cortical ischemic lesion burden measured by DIR is related to carotid artery disease severity. Cerebrovasc Dis. 2015;39(1):23–30.
De Reuck J, Auger F, Cordonnier C, Deramecourt V, Durieux N, Pasquier F, Bordet R, Maurage CA, Leys D. Comparison of 7.0-T T*-magnetic resonance imaging of cerebral bleeds in post-mortem brain sections of Alzheimer patients with their neuropathological correlates. Cerebrovasc Dis. 2011;31(5):511–7.
De Reuck J, Auger F, Durieux N, Deramecourt V, Cordonnier C, Pasquier F, Maurage CA, Leys D, Bordet R. Topography of cortical microbleeds in Alzheimer’s disease with and without cerebral amyloid angiopathy: a post-mortem 7.0-Tesla MRI study. Aging Dis. 2015;6(6):437–43.
De Reuck J, Deramecourt V, Auger F, Durieux N, Cordonnier C, Devos D, Defebvre L, Moreau C, Caparros-Lefebvre D, Bordet R, et al. Post-mortem 7.0-tesla magnetic resonance study of cortical microinfarcts in neurodegenerative diseases and vascular dementia with neuropathological correlates. J Neurol Sci. 2014;346(1-2):85–9.
De Reuck JL, Deramecourt V, Auger F, Durieux N, Cordonnier C, Devos D, Defebvre L, Moreau C, Capparos-Lefebvre D, Pasquier F, et al. The significance of cortical cerebellar microbleeds and microinfarcts in neurodegenerative and cerebrovascular diseases. A post-mortem 7.0-tesla magnetic resonance study with neuropathological correlates. Cerebrovasc Dis. 2015;39(2):138–43.
De Reuck J, Deramecourt V, Cordonnier C, Auger F, Durieux N, Bordet R, Maurage CA, Leys D, Pasquier F. Detection of microbleeds in post-mortem brains of patients with frontotemporal lobar degeneration: a 7.0-Tesla magnetic resonance imaging study with neuropathological correlates. Eur J Neurol. 2012;19(10):1355–60.
De Reuck J, Deramecourt V, Cordonnier C, Auger F, Durieux N, Pasquier F, Bordet R, Defebvre L, Caparros-Lefebvre D, Maurage CA, et al. Superficial siderosis of the central nervous system: a post-mortem 7.0-tesla magnetic resonance imaging study with neuropathological correlates. Cerebrovasc Dis. 2013;36(5-6):412–7.
De Reuck JL, Deramecourt V, Auger F, Durieux N, Cordonnier C, Devos D, Defebvre L, Moreau C, Caparros-Lefebvre D, Leys D, et al. Iron deposits in post-mortem brains of patients with neurodegenerative and cerebrovascular diseases: a semi-quantitative 7.0 T magnetic resonance imaging study. Eur J Neurol. 2014;21(7):1026–31.
O’Sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, Markus HS. Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology. 2001;57(4):632–8.
Sabri O, Ringelstein EB, Hellwig D, Schneider R, Schreckenberger M, Kaiser HJ, Mull M, Buell U. Neuropsychological impairment correlates with hypoperfusion and hypometabolism but not with severity of white matter lesions on MRI in patients with cerebral microangiopathy. Stroke. 1999;30(3):556–66.
O’Sullivan M, Morris RG, Huckstep B, Jones DK, Williams SC, Markus HS. Diffusion tensor MRI correlates with executive dysfunction in patients with ischaemic leukoaraiosis. J Neurol Neurosurg Psychiatry. 2004;75(3):441–7.
Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med. 1996;36(6):893–906.
Beaulieu C, Allen PS. Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn Reson Med. 1994;32(5):579–83.
Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex. 2008;44(8):936–52.
Wheeler-Kingshott CA, Cercignani M. About “axial” and “radial” diffusivities. Magn Reson Med. 2009;61(5):1255–60.
Jones DK, Knosche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage. 2013;73:239–54.
Nitkunan A, Barrick TR, Charlton RA, Clark CA, Markus HS. Multimodal MRI in cerebral small vessel disease: its relationship with cognition and sensitivity to change over time. Stroke. 2008;39(7):1999–2005.
Molko N, Pappata S, Mangin JF, Poupon F, LeBihan D, Bousser MG, Chabriat H. Monitoring disease progression in CADASIL with diffusion magnetic resonance imaging: a study with whole brain histogram analysis. Stroke. 2002;33(12):2902–8.
Holtmannspotter M, Peters N, Opherk C, Martin D, Herzog J, Bruckmann H, Samann P, Gschwendtner A, Dichgans M. Diffusion magnetic resonance histograms as a surrogate marker and predictor of disease progression in CADASIL: a two-year follow-up study. Stroke. 2005;36(12):2559–65.
O’Sullivan M. Diffusion in chronic stroke and small vessel disease. In: Jones DK, editor. Diffusion MRI. Theory, methods and applications. New York: Oxford University Press; 2011.
Berlot R, Metzler-Baddeley C, Jones DK, O’Sullivan MJ. CSF contamination contributes to apparent microstructural alterations in mild cognitive impairment. Neuroimage. 2014;92:27–35.
O’Sullivan M, Barrick TR, Morris RG, Clark CA, Markus HS. Damage within a network of white matter regions underlies executive dysfunction in CADASIL. Neurology. 2005;65(10):1584–90.
van der Holst HM, Tuladhar AM, van Norden AG, de Laat KF, van Uden IW, van Oudheusden LJ, Zwiers MP, Norris DG, Kessels RP, de Leeuw FE. Microstructural integrity of the cingulum is related to verbal memory performance in elderly with cerebral small vessel disease: the RUN DMC study. Neuroimage. 2013;65:416–23.
Correia S, Lee SY, Voorn T, Tate DF, Paul RH, Zhang S, Salloway SP, Malloy PF, Laidlaw DH. Quantitative tractography metrics of white matter integrity in diffusion-tensor MRI. Neuroimage. 2008;42(2):568–81.
Lawrence AJ, Chung AW, Morris RG, Markus HS, Barrick TR. Structural network efficiency is associated with cognitive impairment in small-vessel disease. Neurology. 2014;83(4):304–11.
Reijmer YD, Fotiadis P, Martinez-Ramirez S, Salat DH, Schultz A, Shoamanesh A, Ayres AM, Vashkevich A, Rosas D, Schwab K, et al. Structural network alterations and neurological dysfunction in cerebral amyloid angiopathy. Brain. 2015;138(Pt 1):179–88.
Sappey Marinier D, Calabrese G, Hetherington HP, Fisher SN, Deicken R, Van Dyke C, Fein G, Weiner MW. Proton magnetic resonance spectroscopy of human brain: applications to normal white matter, chronic infarction, and MRI white matter signal hyperintensities. Magn Reson Med. 1992;26:313–27.
Brooks WM, Wesley MH, Kodituwakku PW, Garry PJ, Rosenberg GA. 1H-MRS differentiates white matter hyperintensities in subcortical arteriosclerotic encephalopathy from those in normal elderly. Stroke. 1997;28(10):1940–3.
Maillard P, Fletcher E, Lockhart SN, Roach AE, Reed B, Mungas D, DeCarli C, Carmichael OT. White matter hyperintensities and their penumbra lie along a continuum of injury in the aging brain. Stroke. 2014;45(6):1721–6.
Taheri S, Gasparovic C, Huisa BN, Adair JC, Edmonds E, Prestopnik J, Grossetete M, Shah NJ, Wills J, Qualls C, et al. Blood-brain barrier permeability abnormalities in vascular cognitive impairment. Stroke. 2011;42(8):2158–63.
Huisa BN, Caprihan A, Thompson J, Prestopnik J, Qualls CR, Rosenberg GA. Long-term blood-brain barrier permeability changes in Binswanger disease. Stroke. 2015;46(9):2413–8.
Rosenberg GA, Wallin A, Wardlaw JM, Markus HS, Montaner J, Wolfson L, Iadecola C, Zlokovic BV, Joutel A, Dichgans M, et al. Consensus statement for diagnosis of subcortical small vessel disease. J Cereb Blood Flow Metab. 2016;36(1):6–25.
Heiss WD, Zimmermann-Meinzingen S. PET imaging in the differential diagnosis of vascular dementia. J Neurol Sci. 2012;322(1-2):268–73.
Benson DF, Kuhl DE, Hawkins RA, Phelps ME, Cummings JL, Tsai SY. The fluorodeoxyglucose 18 F scan in Alzheimer’s disease and multi-infarct dementia. Arch Neurol. 1983;40(12):711–4.
Mielke R, Herholz K, Grond M, Kessler J, Heiss WD. Severity of vascular dementia is related to volume of metabolically impaired tissue. Arch Neurol. 1992;49(9):909–13.
Herholz K, Salmon E, Perani D, Baron JC, Holthoff V, Frolich L, Schonknecht P, Ito K, Mielke R, Kalbe E, et al. Discrimination between Alzheimer dementia and controls by automated analysis of multicenter FDG PET. Neuroimage. 2002;17(1):302–16.
Bohnen NI, Djang DS, Herholz K, Anzai Y, Minoshima S. Effectiveness and safety of 18 F-FDG PET in the evaluation of dementia: a review of the recent literature. J Nucl Med. 2012;53(1):59–71.
Su L, Cai Y, Xu Y, Dutt A, Shi S, Bramon E. Cerebral metabolism in major depressive disorder: a voxel-based meta-analysis of positron emission tomography studies. BMC Psychiatry. 2014;14:321.
Herholz K, Weisenbach S, Kalbe E, Diederich NJ, Heiss WD. Cerebral acetylcholine esterase activity in mild cognitive impairment. Neuroreport. 2005;16(13):1431–4.
Hilker R, Thomas AV, Klein JC, Weisenbach S, Kalbe E, Burghaus L, Jacobs AH, Herholz K, Heiss WD. Dementia in Parkinson disease: functional imaging of cholinergic and dopaminergic pathways. Neurology. 2005;65(11):1716–22.
Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82(4):239–59.
Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergstrom M, Savitcheva I, Huang GF, Estrada S, et al. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B. Ann Neurol. 2004;55(3):306–19.
Villemagne VL, Mulligan RS, Pejoska S, Ong K, Jones G, O’Keefe G, Chan JG, Young K, Tochon-Danguy H, Masters CL, et al. Comparison of 11C-PiB and 18 F-florbetaben for Abeta imaging in ageing and Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2012;39(6):983–9.
Aizenstein HJ, Nebes RD, Saxton JA, Price JC, Mathis CA, Tsopelas ND, Ziolko SK, James JA, Snitz BE, Houck PR, et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol. 2008;65(11):1509–17.
Herholz K, Ebmeier K. Clinical amyloid imaging in Alzheimer’s disease. Lancet Neurol. 2011;10(7):667–70.
Yotter RA, Doshi J, Clark V, Sojkova J, Zhou Y, Wong DF, Ferrucci L, Resnick SM, Davatzikos C. Memory decline shows stronger associations with estimated spatial patterns of amyloid deposition progression than total amyloid burden. Neurobiol Aging. 2013;34(12):2835–42.
Maruyama M, Shimada H, Suhara T, Shinotoh H, Ji B, Maeda J, Zhang MR, Trojanowski JQ, Lee VM, Ono M, et al. Imaging of tau pathology in a tauopathy mouse model and in Alzheimer patients compared to normal controls. Neuron. 2013;79(6):1094–108.
Small GW, Bookheimer SY, Thompson PM, Cole GM, Huang SC, Kepe V, Barrio JR. Current and future uses of neuroimaging for cognitively impaired patients. Lancet Neurol. 2008;7(2):161–72.
Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol. 2013;12(6):609–22.
Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA. 1997;277(10):813–7.
Pendlebury ST. Dementia in patients hospitalized with stroke: rates, time course, and clinico-pathologic factors. Int J Stroke. 2012;7(7):570–81.
Whitehead SN, Hachinski VC, Cechetto DF. Interaction between a rat model of cerebral ischemia and beta-amyloid toxicity: inflammatory responses. Stroke. 2005;36(1):107–12.
Thiel A, Heiss WD. Imaging of microglia activation in stroke. Stroke. 2011;42(2):507–12.
Stefaniak J, O’Brien J. Imaging of neuroinflammation in dementia: a review. J Neurol Neurosurg Psychiatry. 2016;87(1):21–8.
Schmitt AB, Brook GA, Buss A, Nacimiento W, Noth J, Kreutzberg GW. Dynamics of microglial activation in the spinal cord after cerebral infarction are revealed by expression of MHC class II antigen. Neuropathol Appl Neurobiol. 1998;24(3):167–76.
Thiel A, Radlinska BA, Paquette C, Sidel M, Soucy JP, Schirrmacher R, Minuk J. The temporal dynamics of poststroke neuroinflammation: a longitudinal diffusion tensor imaging-guided PET study with 11C-PK11195 in acute subcortical stroke. J Nucl Med. 2010;51(9):1404–12.
Radlinska BA, Blunk Y, Leppert IR, Minuk J, Pike GB, Thiel A. Changes in callosal motor fiber integrity after subcortical stroke of the pyramidal tract. J Cereb Blood Flow Metab. 2012;32(8):1515–24.
Thiel A, Cechetto DF, Heiss WD, Hachinski V, Whitehead SN. Amyloid burden, neuroinflammation, and links to cognitive decline after ischemic stroke. Stroke. 2014;45(9):2825–9.