Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T04:55:37.667Z Has data issue: false hasContentIssue false
  • English
  • Français

Therapeutic Issues in Vascular Dementia: Studies, Designs and Approaches

Published online by Cambridge University Press:  02 December 2014

Sandra E. Black
Sandra E. Black*
Affiliation:
Department of Medicine, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, ON, Canada
*
Sunnybrook Health Sciences Centre, 2075 Bayview Ave.-A421, Toronto, Ontario, M4N 3M5, Canada.
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Vascular dementia (VaD) is a heterogeneous disorder resulting from various cerebrovascular diseases (CVD) causing cognitive impairment that reflects severity and location of damage. Epidemiological studies suggest VaD is the second commonest cause of dementia, but autopsy series report that pure VaD is infrequent, while combined CVD and Alzheimer's Disease(AD) is likely the commonest pathological-dementia correlate. Both diseases share vascular risk factors and benefit from their treatment. The most widely used diagnostic criteria for VaD are highly specific but not sensitive. Vascular Cognitive Impairment (VCI) is a dynamic, evolving concept that embraces VaD, Vascular Cognitive Impairment No Dementia (VCIND) and mixed AD and CVD. Clinical trials to date have focused on probable and possible VaD with beneficial effects evident for different drug classes, including cholinergic agents and NMDA agonists. Limitations have included use of cognitive tools suitable for AD that are insensitive to executive dysfunction. Disease heterogeneity has not been adequately controlled and subtypes require further study. Diagnostic VaD criteria now 13 years old need updating. More homogeneous subgroups need to be defined and therapeutically targeted to improve cognitive-behavioural outcomes including optimal control of vascular risk factors. More sensitive testing of executive function outlined in recent VCI Harmonization criteria and longer trial duration are needed to discern meaningful effects. Imaging criteria must be well-defined, with centralized review and standardized protocols. Serial scanning with quantification of tissue atrophy and lesion burden is becoming feasible, and cognitive interventions, including rehabilitation pharmacotherapy, with drugs strategically coupled to cognitive -behavioural treatments, hold promise and need further development.

Résumé:

RÉSUMÉ:

La démence vasculaire (DVa) est une entité hétérogène résultant de différentes maladies cérébrovasculaires (MCV) qui causent une atteinte cognitive reflétant la sévérité et la localisation des dommages. Les études épidémiologiques suggèrent que la DVa est la deuxième cause de démence, mais des études anatomopathologiques de matériel prélevé à l'autopsie démontrent que la MCV pure est rare et que l'association MCV et maladie d'Alzheimer (MA) est vraisemblablement le plus fréquent corrélat pathologie-démence. Les facteurs de risque vasculaires sont communs aux deux maladies et leur contrôle est bénéfique aux deux maladies. Les critères diagnostiques les plus utilisés pour la DVa sont très spécifiques mais ne sont pas sensibles. L'atteinte cognitive vasculaire (ACV) est un concept dynamique en évolution qui comprend la DVa, l'atteinte cognitive vasculaire sans démence (ACVSD) et la MA avec MCV. Jusqu'à maintenant, les essais cliniques ont ciblé la DVa probable et la DVa possible. Les bénéfices ont été évidents dans les essais portant sur différentes classes de médicaments, dont les agents cholinergiques et les agonistes de la NMDA. Une des limites de ces études est l'utilisation d'outils cognitifs appropriés à la MA qui sont insensibles à la dysfonction exécutive. On n'a pas suffisamment tenu compte de l'hétérogénéité de la maladie et on devra faire des études sur les sous-types de démence. Les critères diagnostiques de la DVa ont été établis il y a 13 ans et devraient être révisés. On doit définir des sous-groupes plus homogènes et cibler l'amélioration des résultats cognitifs et comportementaux ainsi que le contrôle optimal des facteurs de risque vasculaires. Les critères d'harmonisation de l'ACV établissent les grandes lignes de tests plus sensibles pour évaluer la fonction exécutive et des essais plus longs devront être faits pour faire ressortir les effets significatifs. Les critères d'imagerie devront être mieux définis, avec révision centrale et protocoles standardisés. L'imagerie en série avec quantification de l'atrophie tissulaire et du fardeau des lésions est maintenant possible et les interventions cognitives, dont la pharmacothérapie de réadaptation avec des médicaments ciblant stratégiquement la cognition et le comportement, sont prometteuses. On doit poursuivre leur développement.

Type
Original Articles
Information
Canadian Journal of Neurological Sciences , Volume 34 , Issue S1 , March 2007 , pp. S125 - S130
Copyright
Copyright © The Canadian Journal of Neurological 2007

References

1. Canadian Study of Health and Aging Working Group. Canadian study of health and aging: study methods and prevalence of dementia. Can Med Assoc J. 1994;150(6):899–913.Google Scholar
2. Lim, A, Tsuang, D, Kukull, W, Nochlin, D, Leverenz, J, McCormick, W, et al. Clinico-neuropathological correlation of Alzheimer’s disease in a community-based case series. J Am Geriatr Soc. 1999 May;47(5):564–9.CrossRefGoogle Scholar
3. Pathological correlates of late-onset dementia in a multicentre, community-based population in England and Wales. Neuropathology Group of the Medical Research Council Cognitive Function and Ageing Study (MRC CFAS). Lancet. 2001 Jan 20;357(9251):169–75.Google Scholar
4. Hachinski, VC. Multi-infarct dementia. A cause of mential deterioration in the elderly. Lancet. 1974;2(874):207–10.CrossRefGoogle ScholarPubMed
5. Hachinski, VC. The decline and resurgence of vascular dementia. Can Med Assoc J. 1990;142:107–11.Google ScholarPubMed
6. Hachinski, V. Vascular dementia: a radical redefinition. Dementia. 1994;5:130–2.Google ScholarPubMed
7. Rockwood, K, Wentzel, C, Hachinski, V, Hogan, DB, Macknight, C, McDowell, . Prevalence and outcomes of vascular cognitive impairment. Vascular Cognitive Impairment Investigators of the Canadian Study of Health and Aging. Neurology. 2000 Jan 25;54(2):447–51.CrossRefGoogle ScholarPubMed
8. Roman, GC, Sachdev, P, Royall, DR, Bullock, RA, Orgogozo, JM, Lopez-Pousa, S, et al. Vascular cognitive disorder: a new diagnostic category updating vascular cognitive impairment and vascular dementia. J Neurol Sci. 2004 Nov 15; 226(1-2):81–7.CrossRefGoogle ScholarPubMed
9. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 4 ed. Washington DC: American Psychiatric Association; 1994.Google Scholar
10. Roman, GC, Tatemichi, TK, Erkinjuntti, T, Cummings, JL, Masdeu, JC, Garcia, JH, et al. Vascular dementia: diagnostic criteria for research studies. Report of the NINDS-AIREN International Workshop. Neurology. 1993;43(2):250–60.CrossRefGoogle ScholarPubMed
11. Chui, HC, Victoroff, JI, Margolin, D, Jagust, W, Shankle, R, Katzman, R. Criteria for the diagnosis of ischemic vascular dementia proposed by the State of California Alzheimer’s Disease Diagnostic and Treatment Centers. Neurology. 1992;42:473-80.Google Scholar
12. Lopez, OL, Larumbe, MR, Becker, JT, Rezek, D, Rosen, J, Klunk, W, et al. Reliability of NINDS-AIREN clinical criteria for the diagnosis of vascular dementia. Neurology. 1994;44:1240–5.CrossRefGoogle ScholarPubMed
13. Roman, G. Diagnosis of vascular dementia and Alzheimer’s disease. Int J Clin Pract Suppl. 2001 May;(120):9–13.Google ScholarPubMed
14. Chui, HC, Mack, W, Jackson, JE, Mungas, D, Reed, BR, Tinklenberg, J, et al. Clinical criteria for the diagnosis of vascular dementia: a multicenter study of comparability and interrater reliability. Arch Neurol. 2000 Feb;57(2):191–6.CrossRefGoogle ScholarPubMed
15. Gold, G, Bouras, C, Canuto, A, Bergallo, MF, Herrmann, FR, Hof, PR, et al. Clinicopathological validation study of four sets of clinical criteria for vascular Dementia. Am J Psychiatry. 2002 Jan 1;159(1):82–7.CrossRefGoogle ScholarPubMed
16. Wilkinson, D, Doody, R, Helme, R, Taubman, K, Mintzer, J, Kertesz, A, et al. Donepezil in vascular dementia: a randomized, placebocontrolled study. Neurology. 2003 Aug 26;61(4):479–86.CrossRefGoogle Scholar
17. Black, S, Roman, GC, Geldmacher, DS, Salloway, S, Hecker, J, Burns, A, 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 Oct;34(10):2323–30.CrossRefGoogle ScholarPubMed
18. Holmes, C, Cairns, N, Lantos, P, Mann, A. Validity of current clinical criteria for Alzheimer’s disease, vascular dementia and dementia with Lewy bodies. Br J Psychiatry. 1999;174:45–50.CrossRefGoogle ScholarPubMed
19. 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 Mar 12;277(10):813–7.CrossRefGoogle ScholarPubMed
20. Esiri, MM, Nagy, Z, Smith, MZ, Barnetson, L, Smith, AD. Cerebrovascular disease and threshold for dementia in the early stages of Alzheimer’s disease. Lancet. 1999 Sep 11;354(9182):919–20.CrossRefGoogle ScholarPubMed
21. de la Torre, JC. Alzheimer disease as a vascular disorder: nosological evidence. Stroke. 2002 Apr 1;33(4):1152–62.CrossRefGoogle ScholarPubMed
22. Vinters, HV, Secor, DL, Read, SL, Frazee, JG, Tomiyasu, U, Stanley, TM, et al. Microvasculature in brain biopsy specimens from patients with Alzheimer’s disease: an immunohistochemical and ultrastructural study. Ultrastruct.Pathol. 1994 May;18(3):333–48.CrossRefGoogle ScholarPubMed
23. Tatemichi, TK, Desmond, DW, Mayeux, R, Paik, M, Stern, Y, Sano, M, et al. Dementia after stroke: baseline frequency, risks and clinical features in a hospitalized cohort. Neurology. 1992;42:1185–93.CrossRefGoogle Scholar
24. van Kooten, F, Koudstaal, PJ. Epidemiology of post-stroke dementia. Haemostasis. 1998 May;28(3-4):124–33.Google ScholarPubMed
25. Hom, J, Reitan, RM. Generalized cognitive function after stroke. J Clin Exp Neuropsychol. 1990;12(5):644–54.CrossRefGoogle ScholarPubMed
26. Ladurner, G, Iliff, LD, Lechner, H. Clinical factors associated with dementia in ischaemic stroke. J Neurol Neurosurg Psychiatry. 1982;45:97–101.CrossRefGoogle ScholarPubMed
27. Tatemichi, TK, Desmond, DW, Stern, Y, Paik, M, Sano, M, Bagiella, E. Cognitive impairment after stroke: frequency, patterns, and relationship to functional abilities. J Neurol Neurosurg Psychiatry 1994;57:202–7.CrossRefGoogle ScholarPubMed
28. Tatemichi, TK, Foulkes, MA, Mohr, JP. Dementia in stroke survivors in the Stroke Data Bank cohort. Prevalence, incidence, risk factors and computed tomographic findings. Stroke. 1990;21:858–66.CrossRefGoogle ScholarPubMed
29. Tatemichi, TK, Paik, M, Bagiella, E, Desmond, DW, Pirro, M, Hanzawa, LK. Dementia after stroke is a predictor of long-term survival. Stroke. 1994;25:1915–9.CrossRefGoogle ScholarPubMed
30. Longstreth, WT, Bernick, C, Manolio, TA, Bryan, N, Jungreis, CA, Price, TR. Lacunar infarcts defined by magnetic resonance imaging of 3660 elderly people: the Cardiovascular Health Study. Arch Neurol. 1998;55(9):1217–25.CrossRefGoogle ScholarPubMed
31. Vermeer, SE, Hollander, M, van Dijk, EJ, Hofman, A, Koudstaal, PJ, Breteler, MM. Silent brain infarcts and white matter lesions increase stroke risk in the general population: the Rotterdam Scan Study. Stroke. 2003 May;34(5):1126–9.CrossRefGoogle ScholarPubMed
32. Kramer, JH, Reed, BR, Mungas, D, Weiner, MW, Chui, HC. Executive dysfunction in subcortical ischaemic vascular disease. J Neurol Neurosurg Psychiatry. 2002 Feb;72(2):217–20.CrossRefGoogle ScholarPubMed
33. Erkinjuntti, T. Subcortical vascular dementia. Cerebrovasc Dis. 2002;13 Suppl 2:58–60.CrossRefGoogle ScholarPubMed
34. Roman, GC, Erkinjuntti, T, Wallin, A, Pantoni, L, Chui, HC. Subcortical ischaemic vascular dementia. Lancet Neurol. 2002 Nov;1(7):426–36.CrossRefGoogle ScholarPubMed
35. Gunning-Dixon, FM, Raz, N. The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology. 2000 Apr;14(2):224–32.CrossRefGoogle ScholarPubMed
36. DeCarli, C, Murphy, DGM, Tranh, M, Grady, CL, Haxby, JV, Gillette, JA, et al. The effect of white matter hyperintensity volume on brain structure, cognitive performance, and cerebral metabolism of glucose in 51 healthy adults. Neurology. 1995;45(11):2077–84.CrossRefGoogle ScholarPubMed
37. Boone, KB, Miller, BL, Lesser, IM, Mehringer, CM, Hill-Gutierrez, E, Goldberg, MA, et al. Neuropsychological correlates of whitematter lesions in healthy elderly subjects. Arch Neurol. 1992;49:549–54.CrossRefGoogle ScholarPubMed
38. Swartz, RH, Sahlas, DJ, Black, SE. Strategic involvement of cholinergic pathways correlates with visuospatial and executive dysfunction: does the location of white matter signal hyperintensities matter? Journal of Stroke and Cerebrovascular Diseases. 2003;12(1):29–36.CrossRefGoogle Scholar
39. Cummings, JL. Frontal-subcortical circuits and human behavior. Arch Neurol. 1993;50:873–80.CrossRefGoogle ScholarPubMed
40. Piert, M, Koeppe, RA, Giordani, B, Berent, S, Kuhl, DE. Diminished glucose transport and phosphorylation in Alzheimer’s disease determined by dynamic FDG-PET. J Nuc Med. 1996;37(2): 201–8.Google ScholarPubMed
41. Mungas, D, Jagust, WJ, Reed, BR, Kramer, JH, Weiner, MW, Schuff, N, et al. MRI predictors of cognition in subcortical ischemic vascular disease and Alzheimer’s disease. Neurology. 2001 Dec 26;57(12):2229–35.CrossRefGoogle ScholarPubMed
42. Looi, J, Sachdev, P, Brodaty, H, Valenzuela, M, Lorentz, L, Sims, J. Correlation of neuroimaging and neuropsychological function in the Sydney longitudinal study of stroke. Neurobiol Aging 2002;23 Suppl 1: S54.Google Scholar
43. Tullberg, M, Fletcher, E, DeCarli, C, Mungas, D, Reed, BR, Harvey, DJ, et al. White matter lesions impair frontal lobe function regardless of their location. Neurology. 2004 Jul 27;63(2): 246–53.CrossRefGoogle ScholarPubMed
44. Bocti, C, Swartz, RH, Gao, FQ, Sahlas, DJ, Behl, P, Black, SE. A new visual rating scale to assess strategic white matter hyperintensities within cholinergic pathways in dementia. Stroke. 2005 Oct;36(10):2126–31.CrossRefGoogle ScholarPubMed
45. Fein, G, DiSclafani, V, Tanabe, JL, Cardenas, V, Weiner, MW, Jagust, WJ, et al. Hippocampal and cortical atrophy predict dementia in subcortical ischemic vascular disease. Neurology. 2000;55(11): 1626–35.CrossRefGoogle ScholarPubMed
46. Burton, EJ, Kenny, RA, O’Brien, J, Stephens, S, Bradbury, M, Rowan, E, et al. White matter hyperintensities are associated with impairment of memory, attention, and global cognitive performance in older stroke patients. Stroke. 2004 Jun;35(6):1270–5.CrossRefGoogle ScholarPubMed
47. Royall, DR, Cordes, JA, Polk, M. CLOX: an executive clock drawing task. J Neurol Neurosurg Psychiatry. 1998 May;64(5):588–94.CrossRefGoogle ScholarPubMed
48. Dubois, B, Slachevsky, A, Litvan, I, Pillon, B. The FAB: a Frontal Assessment Battery at bedside. Neurology. 2000 Dec 12;55(11): 1621–6.CrossRefGoogle ScholarPubMed
49. Mathuranath, PS, Nestor, PJ, Berrios, GE, Rakowicz, W, Hodges, JR. A brief cognitive test battery to differentiate Alzheimer’s disease and frontotemporal dementia. Neurology. 2000 Dec 12;55(11): 1613–20.CrossRefGoogle ScholarPubMed
50. Darvesh, S, Leach, L, Black, SE, Kaplan, E, Freedman, M. The behavioural neurology assessment. Can J Neurol Sci. 2005 May;32(2):167–77.CrossRefGoogle ScholarPubMed
51. Tierney, MC, Black, SE, Szalai, JP, Snow, WG, Fisher, RH, Nadon, G, et al. Recognition memory and verbal fluency differentiate probable Alzheimer disease from subcortical ischemic vascular dementia. Arch Neurol. 2001 Oct;58(10):1654–9.CrossRefGoogle ScholarPubMed
52. Hachinski, V, Iadecola, C, Petersen, RC, Breteler, MM, Nyenhuis, DL, Black, SE, et al. National Institute of Neurological Disorders and Stroke-Canadian Stroke Network vascular cognitive impairment harmonization standards. Stroke. 2006 Sep;37(9):2220–41.CrossRefGoogle ScholarPubMed
53. Nasreddine, ZS, Phillips, NA, Bedirian, V, Charbonneau, S, Whitehead, V, Collin, I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005 Apr;53(4):695–9.CrossRefGoogle Scholar
54. Sahlas, DJ, Bilbao, JM, Swartz, RH, Black, SE. Clasmatodendrosis correlating with periventricular white matter signal hyperintensity in a case of mixed dementia. Ann Neurol. 2002 Sep;52(3):378–81.CrossRefGoogle Scholar
55. Vinters, HV, Mah, VH. Vascular diseases. In: Duckett, S, editor. The pathology of the aging human nervous system. Philadelphia: Lea & Febiger; 1991. p. 66–76.Google Scholar
56. Mantyla, R, Aronen, HJ, Salonen, O, Pohjasvaara, T, Korpelainen, M, Peltonen, T, et al. Magnetic resonance imaging white matter hyperintensities and mechanism of ischemic stroke. Stroke. 1999 Oct;30(10):2053–8.CrossRefGoogle ScholarPubMed
57. Basser, PJ, Mattiello, J, LeBihan, D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994 Jan;66(1):259–67.CrossRefGoogle ScholarPubMed
58. Jones, DK, Lythgoe, D, Horsfield, MA, Simmons, A, Williams, SCR, Markus, HS. Characterization of white matter damage in Ischemic Leukoaraiosis with diffusion tensor MRI. Stroke. 1999 Feb;30:393–7.CrossRefGoogle ScholarPubMed
59. Sachdev, P, Looi, J, Wen, W, Brodaty, H, Valenzuela, M, Lorentz, L, et al. A neuropsychological MR spectroscopic and MR perfusion study of signal hyperintensities on T2-weighted MRI. Neurobiol Aging. 2002; Suppl 1: S363. Ref Type: Abstract.Google Scholar
60. Capizzano, AA, Schuff, N, Amend, DL, Tanabe, JL, Norman, D, Maudsley, AA, et al. Subcortical ischemic vascular dementia: assessment with quantitative MR imaging and 1H MR spectroscopy. AJNR. 2000 Apr;21(4):621–30.Google Scholar
61. Forette, F, Seux, ML, Staessen, JA, Thijs, L, Birkenhager, WH, Babarskiene, MR, et al. Prevention of dementia in randomised double-blind placebo-controlled Systolic Hypertension in Europe (Syst-Eur) trial. Lancet. 1998 Oct 24;352(9137):1347–51.CrossRefGoogle ScholarPubMed
62. Gorelick, PB. New Horizons for stroke prevention: progress and HOPE. Lancet Neurology. 2002;1(3):149–56.CrossRefGoogle ScholarPubMed
63. Stewart, R. Vascular dementia: a diagnosis running out of time. Br J Psychiatry. 2002 Feb;180:152–6.CrossRefGoogle ScholarPubMed
64. Togashi, H, Matsumoto, M, Yoshioka, M, Hirokami, M, Tochihara, M, Saito, H. Acetylcholine measurement of cerebrospinal fluid by in vivo microdialysis in freely moving rats. Jpn J Pharmacol. 1994 Sep;66(1):67–74.CrossRefGoogle ScholarPubMed
65. Tohgi, H, Abe, T, Kimura, M, Saheki, M, Takahashi, S. Cerebrospinal fluid acetylcholine and choline in vascular dementia of Binswanger and multiple small infarct types as compared with Alzheimer-type dementia. J Neural Transm. 1996;103(10): 1211–20.CrossRefGoogle ScholarPubMed
66. Erkinjuntti, T, Kurz, A, Gauthier, S, Bullock, R, Lilienfeld, S, Damaraju, CV. Efficacy of galantamine in probable vascular dementia and Alzheimer’s disease combined with cerebrovascular disease: a randomised trial. Lancet. 2002 Apr 13;359(9314):1283–90.CrossRefGoogle ScholarPubMed
67. Auchus, A, Brashear, HR, Salloway, S, Schelte, P, Korczyn, A, Gassman-Mayer, C. Results of a trial of galantamine in subjects with vascular dementia confirmed by central MRI reading. Abstracts of the 56th Annual Meeting of the American Academy of Neurology, 2004 San Francisco, California. LBS.009.Google Scholar
68. Orgogozo, JM, Rigaud, AS, Stoffler, A, Mobius, HJ, Forette, F. Efficacy and safety of memantine in patients with mild to moderate vascular dementia: a randomized, placebo-controlled trial (MMM 300). Stroke. 2002 Jul;33(7):1834–9.CrossRefGoogle ScholarPubMed
69. 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 Nov;17(6):297–305.CrossRefGoogle ScholarPubMed
70. Stuss, DT, Levine, B. Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol. 2002;53:401–33.CrossRefGoogle ScholarPubMed
71. Grady, CL, McIntosh, AR, Beig, S, Keightley, ML, Burian, H, Black, SE. Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer’s disease. J Neurosci. 2003 Feb 1;23(3):986–93.CrossRefGoogle ScholarPubMed
72. Swartz, RH, Stuss, DT, Black, SE. Independent cognitive effects of atrophy, diffuse and strategic cerebrovascular disease in dementia. Abstract - 2nd International Congress on Vascular Dementia (Salzburg, Sept 2001).Google Scholar
73. DeCarli, C, Fletcher, E, Ramey, V, Harvey, D, Jagust, WJ. Anatomical mapping of white matter hyperintensities (WMH). Exploring the relationships between periventricular WMH, deep WMH, and total WMH burden. Stroke. 2005; Jan 36(1):50–5.CrossRefGoogle ScholarPubMed
74. Davis, PC, Gray, L, Albert, M, Wilkinson, W, Hughes, J, Heyman, A, et al. The consortium to establish a registry for Alzheimer’s disease (CERAD): Part III. Reliability of a standardized MRI evaluation of Alzheimer’s disease. Neurology. 1992;42:1676–80.CrossRefGoogle Scholar
75. Victoroff, J, Mack, WJ, Grafton, ST, Schreiber, SS, Chui, HC. A method to improve interrater reliability of visual inspection of brain MRI scans in dementia. Neurology. 1994;44:2267–76.CrossRefGoogle ScholarPubMed