Binswanger’s disease: toward a diagnosis agreement and therapeutic approach

References

• Gorelick PB, Scuteri A, Black SE, 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
   PubMed Web of Science ®Google Scholar
• O’Brien JT, Erkinjuntti T, Reisberg B, et al. Vascular cognitive impairment. Lancet Neurol 2003;2(2):89-98
   PubMed Web of Science ®Google Scholar
• Caplan LR. Binswanger’s disease–revisited. Neurology 1995;45(4):626-33
   PubMedGoogle Scholar
• Blass JP, Hoyer S, Nitsch R. A translation of Otto Binswanger’s article, ’The delineation of the generalized progressive paralyses’. 1894. Arch Neurol 1991;48(9):961-72
   Google Scholar
• Babikian V, Ropper AH. Binswanger’s disease: a review. Stroke 1987;18(1):2-12
   Google Scholar
• Bennett DA, Wilson RS, Gilley DW, Fox JH. Clinical diagnosis of Binswanger’s disease. J Neurol Neurosurg Psychiatry 1990;53(11):961-5
   PubMed Web of Science ®Google Scholar
• O’Sullivan M, Morris RG, Markus HS. Brief cognitive assessment for patients with cerebral small vessel disease. J Neurol Neurosurg Psychiatry 2005;76(8):1140-5
   PubMed Web of Science ®Google Scholar
• Dong Y, Sharma VK, Chan BP, et al. The Montreal Cognitive Assessment (MoCA) is superior to the Mini-Mental State Examination (MMSE) for the detection of vascular cognitive impairment after acute stroke. J Neurol Sci 2010;299(1-2):15-18
   PubMed Web of Science ®Google Scholar
• Grau-Olivares M, Arboix A. Mild cognitive impairment in stroke patients with ischemic cerebral small-vessel disease: a forerunner of vascular dementia? Expert Rev Neurother 2009;9(8):1201-17
   PubMed Web of Science ®Google Scholar
• Wolfson L, Wakefield DB, Moscufo N, et al. Rapid buildup of brain white matter hyperintensities over 4 years linked to ambulatory blood pressure, mobility, cognition, and depression in old persons. J Gerontol A Biol Sci Med Sci 2013;68(11):1387-94
   PubMed Web of Science ®Google Scholar
• Potter GM, Doubal FN, Jackson CA, et al. Enlarged perivascular spaces and cerebral small vessel disease. Int J Stroke 2013. [Epub ahead of print]
   Google Scholar
• Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol 2009;8(2):165-74
   PubMed Web of Science ®Google Scholar
• Pico F, Labreuche J, Touboul PJ, et al. Intracranial arterial dolichoectasia and small-vessel disease in stroke patients. Ann Neurol 2005;57(4):472-9
   PubMed Web of Science ®Google Scholar
• Grau-Olivares M, Arboix A, Junque C, et al. Progressive gray matter atrophy in lacunar patients with vascular mild cognitive impairment. Cerebrovasc Dis 2010;30(2):157-66
   PubMed Web of Science ®Google Scholar
• Prins ND, van Dijk EJ, den Heijer T, et al. Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain 2005;128(Pt 9):2034-41
   PubMedGoogle Scholar
• Jonsson M, Zetterberg H, van Straaten E, et al. Cerebrospinal fluid biomarkers of white matter lesions - cross-sectional results from the LADIS study. Eur J Neurol 2010;17(3):377-82
   Google Scholar
• Adair JC, Charlie J, Dencoff JE, et al. Measurement of gelatinase B (MMP-9) in the cerebrospinal fluid of patients with vascular dementia and Alzheimer disease. Stroke 2004;35(6):e159-62
   Web of Science ®Google Scholar
• Kidwell CS, el-Saden S, Livshits Z, et al. Transcranial Doppler pulsatility indices as a measure of diffuse small-vessel disease. J Neuroimaging 2001;11(3):229-35
   Google Scholar
• Schuff N, Matsumoto S, Kmiecik J, et al. Cerebral blood flow in ischemic vascular dementia and Alzheimer’s disease, measured by arterial spin-labeling magnetic resonance imaging. Alzheimers Dement 2009;5(6):454-62
   PubMed Web of Science ®Google Scholar
• Kato H, Yoshikawa T, Oku N, et al. Statistical parametric analysis of cerebral blood flow in vascular dementia with small-vessel disease using Tc-HMPAO SPECT. Cerebrovasc Dis 2008;26(5):556-62
   Google Scholar
• Gasparovic C, Prestopnik J, Thompson J, et al. 1H-MR spectroscopy metabolite levels correlate with executive function in vascular cognitive impairment. J Neurol Neurosurg Psychiatry 2013;84(7):715-21
   Google Scholar
• Iadecola C. The pathobiology of vascular dementia. Neuron 2013;80(4):844-66
   PubMed Web of Science ®Google Scholar
• Lawes CM, Vander Hoorn S, Rodgers A; International Society of H. Global burden of blood-pressure-related disease, 2001. Lancet 2008;371(9623):1513-18
   PubMed Web of Science ®Google Scholar
• Rashid P, Leonardi-Bee J, Bath P. Blood pressure reduction and secondary prevention of stroke and other vascular events: a systematic review. Stroke 2003;34(11):2741-8
   PubMed Web of Science ®Google Scholar
• Turnbull F; Blood Pressure Lowering Treatment Trialists C. Effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet 2003;362(9395):1527-35
   PubMed Web of Science ®Google Scholar
• Group SPSS, Benavente OR, Coffey CS, et al. Blood-pressure targets in patients with recent lacunar stroke: the SPS3 randomised trial. Lancet 2013;382(9891):507-15
   PubMed Web of Science ®Google Scholar
• van Dijk EJ, Prins ND, Vrooman HA, et al. Progression of cerebral small vessel disease in relation to risk factors and cognitive consequences: rotterdam Scan study. Stroke 2008;39(10):2712-19
   PubMed Web of Science ®Google Scholar
• Sachdev P, Wen W, Chen X, Brodaty H. Progression of white matter hyperintensities in elderly individuals over 3 years. Neurology 2007;68(3):214-22
   PubMed Web of Science ®Google Scholar
• Verhaaren BF, Vernooij MW, de Boer R, et al. High blood pressure and cerebral white matter lesion progression in the general population. Hypertension 2013;61(6):1354-9
   PubMed Web of Science ®Google Scholar
• Godin O, Tzourio C, Maillard P, et al. Antihypertensive treatment and change in blood pressure are associated with the progression of white matter lesion volumes: the Three-City (3C)-Dijon Magnetic Resonance Imaging Study. Circulation 2011;123(3):266-73
   PubMed Web of Science ®Google Scholar
• Dufouil C, Chalmers J, Coskun O, et al. Effects of blood pressure lowering on cerebral white matter hyperintensities in patients with stroke: the PROGRESS (Perindopril Protection Against Recurrent Stroke Study) Magnetic Resonance Imaging Substudy. Circulation 2005;112(11):1644-50
   PubMed Web of Science ®Google Scholar
• Weber R, Weimar C, Blatchford J, et al. Telmisartan on top of antihypertensive treatment does not prevent progression of cerebral white matter lesions in the prevention regimen for effectively avoiding second strokes (PRoFESS) MRI substudy. Stroke 2012;43(9):2336-42
   PubMed Web of Science ®Google Scholar
• Peters R, Beckett N, Forette F, et al. Incident dementia and blood pressure lowering in the Hypertension in the Very Elderly Trial cognitive function assessment (HYVET-COG): a double-blind, placebo controlled trial. Lancet Neurol 2008;7(8):683-9
   PubMed Web of Science ®Google Scholar
• Investigators SPS, Benavente OR, Hart RG, et al. Effects of clopidogrel added to aspirin in patients with recent lacunar stroke. N Engl J Med 2012;367(9):817-25
   PubMed Web of Science ®Google Scholar
• Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ 2010;341:c3666
   PubMed Web of Science ®Google Scholar
• Price JF, Stewart MC, Deary IJ, et al. Low dose aspirin and cognitive function in middle aged to elderly adults: randomised controlled trial. BMJ 2008;337:a1198
   PubMed Web of Science ®Google Scholar
• Amarenco P, Bogousslavsky J, Callahan A III, et al. High-dose atorvastatin after stroke or transient ischemic attack. N Engl J Med 2006;355(6):549-59
   PubMed Web of Science ®Google Scholar
• Mizuno Y, Jacob RF, Mason RP. Inflammation and the development of atherosclerosis. J Atheroscler Thromb 2011;18(5):351-8
   Google Scholar
• Hassan A, Hunt BJ, O’Sullivan M, et al. Markers of endothelial dysfunction in lacunar infarction and ischaemic leukoaraiosis. Brain 2003;126(Pt 2):424-32
   Google Scholar
• Stone NJ, Robinson J, Lichtenstein AH, et al. 2013 ACC/AHA Guideline on the Treatment of Blood Cholesterol to Reduce Atherosclerotic Cardiovascular Risk in Adults: A Report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2014;63(25 Pt B):2889-934
   Google Scholar
• Sofi F, Valecchi D, Bacci D, et al. Physical activity and risk of cognitive decline: a meta-analysis of prospective studies. J Intern Med 2011;269(1):107-17
   PubMed Web of Science ®Google Scholar
• Gons RA, Tuladhar AM, de Laat KF, et al. Physical activity is related to the structural integrity of cerebral white matter. Neurology 2013;81(11):971-6
   Google Scholar
• Verdelho A, Madureira S, Ferro JM, et al. Physical activity prevents progression for cognitive impairment and vascular dementia: results from the LADIS (Leukoaraiosis and Disability) study. Stroke 2012;43(12):3331-5
   PubMed Web of Science ®Google Scholar
• Ahlskog JE, Geda YE, Graff-Radford NR, Petersen RC. Physical exercise as a preventive or disease-modifying treatment of dementia and brain aging. Mayo Clin Proc 2011;86(9):876-84
   PubMed Web of Science ®Google Scholar
• McMahon JA, Green TJ, Skeaff CM, et al. A controlled trial of homocysteine lowering and cognitive performance. N Engl J Med 2006;354(26):2764-72
   Google Scholar
• Group VTS. B vitamins in patients with recent transient ischaemic attack or stroke in the VITAmins TO Prevent Stroke (VITATOPS) trial: a randomised, double-blind, parallel, placebo-controlled trial. Lancet Neurol 2010;9(9):855-65
   Google Scholar
• Durga J, van Boxtel MP, Schouten EG, et al. Effect of 3-year folic acid supplementation on cognitive function in older adults in the FACIT trial: a randomised, double blind, controlled trial. Lancet 2007;369(9557):208-16
   PubMed Web of Science ®Google Scholar
• Cogswell ME, Zhang Z, Carriquiry AL, et al. Sodium and potassium intakes among US adults: NHANES. 2003-2008. Am J Clin Nutr 2012;96(3):647-57
   PubMed Web of Science ®Google Scholar
• Bibbins-Domingo K, Chertow GM, Coxson PG, et al. Projected effect of dietary salt reductions on future cardiovascular disease. N Engl J Med 2010;362(7):590-9
   PubMed Web of Science ®Google Scholar
• Al-Solaiman Y, Jesri A, Zhao Y, et al. Low-Sodium DASH reduces oxidative stress and improves vascular function in salt-sensitive humans. J Hum Hypertens 2009;23(12):826-35
   PubMed Web of Science ®Google Scholar
• Ishii K, Kabata T, Oshika T. The impact of cataract surgery on cognitive impairment and depressive mental status in elderly patients. Am J Ophthalmol 2008;146(3):404-9
   PubMedGoogle Scholar
• Lin FR, Yaffe K, Xia J, et al. Hearing loss and cognitive decline in older adults. JAMA Intern Med 2013;173(4):293-9
   PubMed Web of Science ®Google Scholar
• Tomimoto H, Ohtani R, Shibata M, et al. Loss of cholinergic pathways in vascular dementia of the Binswanger type. Dement Geriatr Cogn Disord 2005;19(5-6):282-8
   PubMed Web of Science ®Google Scholar
• Keverne JS, Low WC, Ziabreva I, et al. Cholinergic neuronal deficits in CADASIL. Stroke 2007;38(1):188-91
   Google Scholar
• Erkinjuntti T, Kurz A, Gauthier S, et al. Efficacy of galantamine in probable vascular dementia and Alzheimer’s disease combined with cerebrovascular disease: a randomised trial. Lancet 2002;359(9314):1283-90
   PubMed Web of Science ®Google Scholar
• Wilkinson D, Doody R, Helme R, et al. Donepezil in vascular dementia: a randomized, placebo-controlled study. Neurology 2003;61(4):479-86
   PubMed Web of Science ®Google Scholar
• Black S, Roman GC, Geldmacher DS, et al. Efficacy and tolerability of donepezil in vascular dementia: positive results of a 24-week, multicenter, international, randomized, placebo-controlled clinical trial. Stroke 2003;34(10):2323-30
   PubMed Web of Science ®Google Scholar
• Dichgans M, Markus HS, Salloway S, et al. Donepezil in patients with subcortical vascular cognitive impairment: a randomised double-blind trial in CADASIL. Lancet Neurol 2008;7(4):310-18
   PubMed Web of Science ®Google Scholar
• Kavirajan H, Schneider LS. Efficacy and adverse effects of cholinesterase inhibitors and memantine in vascular dementia: a meta-analysis of randomised controlled trials. Lancet Neurol 2007;6(9):782-92
   PubMed Web of Science ®Google Scholar
• Wilcock G, Mobius HJ, Stoffler A. A double-blind, placebo-controlled multicentre study of memantine in mild to moderate vascular dementia (MMM500). Int Clin Psychopharmacol 2002;17(6):297-305
   PubMed Web of Science ®Google Scholar
• Orgogozo JM, Rigaud AS, Stoffler A, et al. Efficacy and safety of memantine in patients with mild to moderate vascular dementia: a randomized, placebo-controlled trial (MMM 300). Stroke 2002;33(7):1834-9
   PubMed Web of Science ®Google Scholar
• Rothwell PM, Howard SC, Dolan E, et al. Prognostic significance of visit-to-visit variability, maximum systolic blood pressure, and episodic hypertension. Lancet 2010;375(9718):895-905
   PubMed Web of Science ®Google Scholar
• Gorter JW. Major bleeding during anticoagulation after cerebral ischemia: patterns and risk factors. Stroke Prevention In Reversible Ischemia Trial (SPIRIT). European Atrial Fibrillation Trial (EAFT) study groups. Neurology 1999;53(6):1319-27
   PubMed Web of Science ®Google Scholar
• Smith EE, Rosand J, Knudsen KA, et al. Leukoaraiosis is associated with warfarin-related hemorrhage following ischemic stroke. Neurology 2002;59(2):193-7
   Google Scholar
• Tomimoto H. Subcortical vascular dementia. Neurosci Res 2011;71(3):193-9
   Google Scholar
• Anthony DC, Ferguson B, Matyzak MK, et al. Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol Appl Neurobiol 1997;23(5):406-15
   PubMed Web of Science ®Google Scholar
• Rosenberg GA, Sullivan N, Esiri MM. White matter damage is assoiciated with matrix metalloproteinases in vascular dementia. Stroke 2001;32:1162-8
   PubMed Web of Science ®Google Scholar
• Cammer W, Bloom BR, Norton WT, Gordon S. Degradation of basic protein in myelin by neutral proteases secreted by stimulated macrophages: a possible mechanism of inflammatory demyelination. Proc.Natl.Acad.Sci USA 1978;75:1554-8
   Web of Science ®Google Scholar
• Yong VW, Zabad RK, Agrawal S, et al. Elevation of matrix metalloproteinases (MMPs) in multiple sclerosis and impact of immunomodulators. J Neurol Sci 2007;259(1-2):79-84
   PubMed Web of Science ®Google Scholar
• Rosenberg GA. Neurological diseases in relation to the blood-brain barrier. J Cereb Blood Flow Metab 2012;32(7):1139-51
   PubMed Web of Science ®Google Scholar
• Liuzzi GM, Trojano M, Fanelli M, et al. Intrathecal synthesis of matrix metalloproteinase-9 in patients with multiple sclerosis: implication for pathogenesis. Mult Scler 2002;8(3):222-8
   Google Scholar
• Wallin A, Blennow K, Fredman P, et al. Blood brain barrier function in vascular dementia. Acta Neurol Scand 1990;81(4):318-22
   Google Scholar
• Candelario-Jalil E, Thompson J, Taheri S, et al. Matrix metalloproteinases are associated with increased blood-brain barrier opening in vascular cognitive impairment. Stroke 2011;42(5):1345-50
   Web of Science ®Google Scholar
• Jalal FY, Yang Y, Thompson J, et al. Myelin loss associated with neuroinflammation in hypertensive rats. Stroke 2012;43(4):1115-22
   Web of Science ®Google Scholar
• Hanyu H, Asano T, Tanaka Y, et al. Increased blood-brain barrier permeability in white matter lesions of Binswanger’s disease evaluated by contrast-enhanced MRI. Dement Geriatr Cogn Disord 2002;14(1):1-6
   Google Scholar
• Wardlaw JM, Doubal F, Armitage P, et al. Lacunar stroke is associated with diffuse blood-brain barrier dysfunction. Ann Neurol 2009;65(2):194-202
   Google Scholar
• Taheri S, Gasparovic C, Huisa BN, et al. Blood-brain barrier permeability abnormalities in vascular cognitive impairment. Stroke 2011;42(8):2158-63
   Google Scholar
• Topakian R, Barrick TR, Howe FA, Markus HS. Blood-brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis. J Neurol Neurosurg Psychiatry 2010;81(2):192-7
   PubMed Web of Science ®Google Scholar
• Wardlaw JM, Doubal FN, Valdes-Hernandez M, et al. Blood-brain barrier permeability and long-term clinical and imaging outcomes in cerebral small vessel disease. Stroke 2013;44(2):525-7
   PubMed Web of Science ®Google Scholar
• Choudhri AF, Chin EM, Blitz AM, Gandhi D. Diffusion tensor imaging of cerebral white matter: technique, anatomy, and pathologic patterns. Radiol Clin North Am 2014;52(2):413-25
   Google Scholar
• O’Sullivan M, Summers PE, Jones DK, et al. Normal-appearing white matter in ischemic leukoaraiosis: a diffusion tensor MRI study. Neurology 2001;57(12):2307-10
   Web of Science ®Google Scholar
• Reijmer YD, Freeze WM, Leemans A, Biessels GJ; Utrecht Vascular Cognitive Impairment Study Group. The effect of lacunar infarcts on white matter tract integrity. Stroke 2013;44(7):2019-21
   Google Scholar
• Maillard P, Fletcher E, Harvey D, et al. White matter hyperintensity penumbra. Stroke 2011;42(7):1917-22
   Google Scholar
• Maillard P, Carmichael O, Harvey D, et al. FLAIR and diffusion MRI signals are independent predictors of white matter hyperintensities. AJNR Am J Neuroradiol 2013;34(1):54-61
   Google Scholar
• Schmidt R, Ropele S, Ferro J, et al. Diffusion-weighted imaging and cognition in the leukoariosis and disability in the elderly study. Stroke 2010;41(5):e402-8
   Google Scholar
• Nitkunan A, Barrick TR, Charlton RA, et al. Multimodal MRI in cerebral small vessel disease: its relationship with cognition and sensitivity to change over time. Stroke 2008;39(7):1999-2005
   Google Scholar
• Jokinen H, Schmidt R, Ropele S, et al. Diffusion changes predict cognitive and functional outcome: the LADIS study. Ann Neurol 2013;73(5):576-83
   Google Scholar
• Erten-Lyons D, Woltjer R, Kaye J, et al. Neuropathologic basis of white matter hyperintensity accumulation with advanced age. Neurology 2013;81(11):977-83
   PubMed Web of Science ®Google Scholar
• Makedonov I, Black SE, Macintosh BJ. BOLD fMRI in the white matter as a marker of aging and small vessel disease. PLoS One 2013;8(7):e67652
   Google Scholar
• 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
   Google Scholar
• Wintermark M, Sesay M, Barbier E, et al. Comparative overview of brain perfusion imaging techniques. Stroke 2005;36(9):e83-99
   Google Scholar
• Pillai JJ, Mikulis DJ. Cerebrovascular reactivity mapping: an evolving standard for clinical functional imaging. AJNR Am J Neuroradiol 2014. [Epub ahead of print]
   Google Scholar
• Kuwabara Y, Ichiya Y, Otsuka M, et al. Cerebrovascular responsiveness to hypercapnia in Alzheimer’s dementia and vascular dementia of the Binswanger type. Stroke 1992;23(4):594-8
   Google Scholar