Journal ofNeurology, Neurosurgery, and Psychiatry 1990;53:961-965 961 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.11.961 on 1 November 1990. Downloaded from Clinical diagnosis of Binswanger's disease

David A Bennett, Robert S Wilson, David W Gilley, Jacob H Fox

Abstract MRI. Clearly, many of these patients do not To aid in the prospective study of Bins- have BD. Resolution of this dilemma requires wanger's disease, a poorly understood standardised criteria for the clinical diagnosis form of vascular dementia, a standar- of Binswanger's disease. The purpose of this dised criteria for its antemortem diag- paper is to propose such criteria. nosis was proposed. These criteria Although there is undoubtedly a prodromal include dementia, bilateral radiological phase of BD when dementia is not evident, abnormalities on computed tomography Binswanger considered this illness a dement- (CT) or magnetic resonance imaging ing disorder and a recent review by Babikian (MRI), and at least two of the following and Ropper concluded that the illness is three clinical findings: A) a vascular risk "characterized clinically by disorders of factor or evidence of systemic vascular memory, mood, and cognition".6 Therefore, disease; B) evidence of focal cerebro- we propose that the diagnosis be reserved for vascular disease; and C) evidence of patients who are demented. The identical res- "subcortical" cerebral dysfunction. triction is placed on the diagnosis of AD. For These criteria were validated in two research purposes, the presence of dementia ways. First, by retrospectively applying should be confirmed by neuropsychological them to a series of 30 demented patients testing. with various pathological diagnoses. Radiological criteria for BD are complicated Second, by prospectively applying them by the fact that several types of lesions are to a series of 184 patients with clinically identifiable on MRI. Periventricular caps and typical Alzheimer's disease. The sen- rims are nearly ubiquitous findings on MRI. sitivity and specificity of the criteria Pathologically, they represent areas of appear adequate for use in clinical subependymal gliosis, and probably do not research. have a vascular aetiology. Subcortical WMLs may be either small infarcts, focal areas of demyelination, or dilated perivascular Vascular disease is consistently reported as the spaces."'" It is difficult to distinguish between second leading cause of dementia.'2 Nonethe- these lesions. However, a recent MRI-path- less, neither its prevalence nor defining clin- ological study found that the majority of MRI ical, radiological or histopathological features lesions corresponding to dilated perivascular are settled.34 Much of the controversy stems spaces were round or linear, isointense relative http://jnnp.bmj.com/ from the heterogeneity of the vascular demen- to cerebrospinal fluid, and less than 2 x 2 tias.34 Therefore, recent reviews of vascular mm." Therefore, the radiological criteria for dementia stress the need to dinstinguish be- the diagnosis of BD requires bilateral leuk- tween the various vascular dementias and to oaraiosis on CT, or bilateral, multiple or Rush Presbyterian-St develop specific clinical, radiological and diffuse, subcortical high signal T2 weighted Lukes Medical Center, pathological criteria for each type."'

Chicago, Illinois, on September 28, 2021 by guest. Protected copyright. United States Binswanger's disease (BD), a forrn of vas- cular was for years considered a Rush Alzheimer's dementia, Table I Criteriafor the clinical diagnosis ofpossible Disease Center relatively rare disorder diagnosed only Ltt Binswanger's Disease D A Bennett necropsy.' The sensitivity of magnetic R S Wilson resonance imaging (MRI) to subcortical white 1 Dementia must be established by clinical examination and D W Gilley confirmed by neuropsychological tests. J H Fox matter pathology, however, has rekindled 2 One finding from two of the following three groups must be Department of interest in the disorder and raised the pos- present: sibility of its antemortem diagnosis. Unfor- A) the presence of a vascular risk factor or evidence of Neurology systemic vascular disease (for example, hypertension, D A Bennett tunately, the typical radiological lesions of BD diabetes, a history of myocardial infarction, cardiac J H Fox are routinely seen in both elderly demented arrhythmia, or congestive heart failure); Department of B) evidence of focal cerebrovascular disease (for example, a Psychology and Social and non-demented patients.67 Furthermore, history of stroke, or demonstration of a focal pyramidal or Sciences not all of the lesions visualised by MRI have a sensory sign); R S Wilson vascular basis."2 In fact, about 30% of C) evidence of "subcortical" cerebral dysfunction (for example, a Parkinsonian, magnetic, or "senile" gait, Correspondence to: patients with clinically typical Alzheimer's Parkinsonian or gegenhalten rigidity, or a history of Dr Bennett, Rush incontinence secondary to a spastic bladder). Alzheimer's Disease Center, disease (AD) have similar lesions.'3 710 S Paulina Street, For physicians evaluating demented 3 The radiological criteria requires bilateral leukoaraiosis on 8 North JRB, Chicago, computed tomography (CT), or bilateral and, multiple or Illinois 60612-3864, United patients, the controversy surrounding the diffuse, subcortical high signal T2 weighted lesions greater States. radiological abnormalities poses the clinical than 2 x 2 mm on magnetic resonance (MR) scan. The proposed criteria lose their validity in the presence of: Received II October 1989 dilemma of how to diagnose demented and in revised form 5 March 1 multiple or bilateral cortical lesions on CT or MR; or 1990. patients who have white matter lesions 2 severe dementia (for example, MMS < 10) Accepted 14 March 1990 (WMLs) on computed tomography (CT) or 962 Bennett, Wilson, Gilley, Fox J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.11.961 on 1 November 1990. Downloaded from lesions greater than 2 x 2 mm on MRI. To neuritic plaques (NP) were present throughout separate BD from other types of vascular the hippocampus and neocortex. After 1985, dementia, the radiological diagnosis of BD also NP were quantified and the diagnosis of requires the absence of either large or multiple AD followed the recommendations of cortical lesions which may contribute to the Khachaturian et al.' A diagnosis of Multi- patient's dementia. infarct dementia (MID) required large multi- The proposed clinical and historical features ple cortical strokes. No attempt was made to of BD which should accompany dementia and quantify the amount of infarcted tissue. Other the appropriate MRI or CT examination are diagnoses were made by contemporary based on a review of pathologically verified standards. cases ofBD in the English and French language literature. The criteria are outlined in table 1. Part II Clinical series Three classes of findings define BD. These The sample consisted of 795 consecutive include: A) a vascular risk factor or evidence of patients referred to the Rush Alzheimer's Dis- systemic vascular disease; B) evidence of focal ease Center (RADC) between 1985-88 for cerebrovascular disease; and C) evidence of evaluation of possible dementia. Evaluations "subcortical" cerebral dysfunction. We included a standard medical history, excluded reports of mixed AD/BD, mixed neurological examination, neuropsychological vascular dementia, and non-vascular testing, and standard laboratory procedures. demyelinating syndromes, as well as cases with Selection from this series required a diagnosis very atypical histories, unilateral involvement, of typical AD,39 a technically satisfactory MRI lack of clinical data, or lack of clinical evidence scan, and a modified ischaemic score less than of dementia. Of the 62 remaining path- three;40 184 patients met these criteria. The ologically verified cases of BD,8 1-38 41 (66%) MR scans were performed on a Technicare 0-5 met all three clinical criteria presented in table Tesla superconductive scanner at the 1, and 59 (95%) had at least two ofthree clinical RPSLMC. Examinations included TI weigh- findings. We therefore propose that two of the ted saggital and axial acquisitions and T2 three clinical findings outlined above are neces- weighted multislice multiecho saggital and sary for the diagnosis of BD. axial acquisitions. All MRIs were rated for the In this paper we report the results of two number and location of abnormalities. " The evaluations of the validity of these diagnostic proposed diagnostic criteria were then applied criteria. In the first study, the sensitivity of the to these 184 patients. To assess the incremental criteria was assessed by retrospectively apply- validity of the MRI, the cases were classified ing them to a series of 30 pathologically diag- both with and without the MRI criterion. nosed cases ofdementia ofvarying aetiology. In the second study, the specificity of the criteria was evaluated by applying them prospectively Results to a series of 184 patients with clinically typical Part I Pathological series Table 2 depicts the AD. pathological diagnoses of the retrospectively reviewed cases ofdementia. Four patients had a pathological diagnosis of BD and all four met Method BD criteria. One of two patients with mixed Part I Pathological series BD and AD met criteria. Two patients had http://jnnp.bmj.com/ One neurologist (DAB), blind to the path- MID, one of whom also had concomitant AD. ological diagnosis, reviewed the medical Both met the clinical criteria for BD, but not records of 45 patients who had a clinical the radiological criterion because of multiple diagnosis of dementia and a brain necropsy cortical lesions on their brain scans. Twelve performed at Rush Presbyterian-St Luke's patients had AD, only one of whom fulfilled Medical Center (RPSLMC) between 1975-88. the criteria. Of five cases of Creutzfeld-Jakob

Patients without clinical evidence of dementia, disease, one met the criteria. None of the on September 28, 2021 by guest. Protected copyright. a complete neurological examination, and a CT remaining cases, including patients with Pick's or MRI scan were excluded, leaving 30 cases. disease, thalamic gliosis, Parkinson's disease The clinical, radiological and pathological data with dementia, and two with no pathological were recorded on a standardised form. Only diagnosis met the criteria. The agreement be- variables explicitly mentioned in the chart were tween the clinical and pathological diagnoses scored as present. The diagnostic criteria was significant (Fisher's Exact Test, p = outlined in table 1 were then applied to the 0 0008, two-tailed). clinical and radiological data on the 30 cases. The pathological criteria for the diagnosis of Part II Clinical series Ofthe 184 patients with BD were those outlined by Olszewski.2' There a diagnosis of AD, 32 (17A4%) met at least two had to be diffuse areas ofdemyelination sparing of the three clinical criteria. However, only the subcortical U-fibres, arteriosclerosis of the three of these patients also met the radiological penetrating blood vessels, and small infarcts in criteria. Therefore, only 1 6% (3/184) of these the subcortical white or grey matter. Although patients with clinically typical AD met the controversial, additional subcortical gliosis was proposed criteria. In four of these 184 patients, supportive, but not necessary for the diagnosis. AD was confirmed pathologically. If other abnormalities were present, cases were Gait disorders and incontinence are common classified as mixed (for example, mixed BD/ findings in severely demented patients. We AD). therefore compared dementia severity in those A diagnosis ofAD was made when numerous who did and did not meet clinical criteria. The 963

Clinical diagnosis of Binswanger's disease J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.11.961 on 1 November 1990. Downloaded from

Table 2 Criteria for the clinical diagnosis ofBinswanger's disease in a retrospective pathologic series of30 cases of dementia Clinical Criteria Case Path Diagnosis Risk' Focal2 Subcor' Rad' Met Crit 1 BD + + + + Yes 2 BD + - + + Yes 3 BD + + + + Yes 4 BD + + + + Yes 5 BD/AD + - + + Yes 6 BD/AD - - - + No 7 MID + + + - No 8 MID/AD + + + - No 9 AD - - - - No 10 AD - - - - No 11 AD - - - - No 12 AD + - - - No 13 AD - - + - No 14 AD + + + - No 15 AD - - + + No 16 AD - - - + No 17 AD - - + - No 18 AD + + + - No 19 AD - - + - No 20 AD + - + + Yes 21 CJD - - - - No 22 CJD + + + - No 23 CJD - - + - No 24 CJD - + + + Yes 25 CJD - + + - No 26 Pick's + - - + No 27 Th + + + - No 28 PD - - + - No 29 No Diagnosis + - - - No 30 NoDiagnosis + - - - No 'Risk factor or evidence of atherosclerosis. 'History of stroke or evidence of focal cerebral disease. 3Evidence of "subcortical" cerebral dysfunction. 'CT or MRI. BD = Binswanger's disease; AD = Alzheimer's disease; BD/AD = BD with AD; MID = Multiple infarcts; MID/AD = MID with AD; CJD = Creutzfeldt-Jakob disease; Pick's = Pick's disease; Th = Thalamic gliosis; PD = Parkinson's disease.

former had an average Mini-Mental State stopped short of advocating a specific diagnos- (MMS) examination4' of 11-5 (5 9); the latter tic scheme. had a mean(SD) MMS of 14-2 (8 3). Although For the specific clinical criteria, vascular risk this trend is not statistically significant (t factors and focal cerebral dysfunction are (1,182) = 1-57, p = 0 057), it suggests caution widely recognised features of the syndrome.68 when applying these criteria to severely However, other features of the syndrome demented patients. remain controversial. Although both Binswanger and Alzheimer regarded BD as a dementing illness, Olszewski, Discussion in his trenchant 1962 review, advocated that http://jnnp.bmj.com/ Guided by reports of pathologically verified the diagnosis be made strictly on pathological cases, we developed an explicit diagnostic grounds.25 Recent reviews, however, have scheme for the antemortem diagnosis of BD reverted to the earlier position, thereby re- based on historical, clinical, and radiological introducing the clinical requisite that dementia information. Diagnoses based on these criteria be documented to make the diagnosis.467 We were in close agreement with pathological recognise that this represents a somewhat diagnoses in a retrospective series of 30 arbitrary limitation to the syndrome. However,

patients. Application ofthe criteria to a series of we were guided by the precedent set with on September 28, 2021 by guest. Protected copyright. 184 patients with clinically typical AD resulted Alzheimer's disease and by the belief that a in few diagnostic misclassifications (1 6%). We more uniform definition of BD will ultimately propose that these criteria may be useful in lead to a better understanding of the disease. clinical dementia research. Indeed, differences Our criteria include neurological signs of in memory and affective disturbances can be "subcortical" cerebral dysfunction such as a demonstrated between patients with AD and gait disorder, Parkinsonism or incontinence. those meeting our criteria.4243 We recognise, Although these findings are common in BD, however, that prospective clinicopathological they are not widely appreciated. However, gait studies are needed for both verification and disorders and Parkinsonism resulting from refinement of this scheme. subcortical vascular disease are well described Until 1978, the diagnosis of BD was made in the neurological literature. 45 In 1929 Crit- only at necropsy. Caplan and Schoene were the chley described several types of arteriosclerotic first to attempt an antemortum diagnosis of Parkinsonism occurring either alone, or in BD.8 They reviewed five cases ofpathologically combination with pseudobulbar, pyramidal or confirmed BD (one of whom had concomitant cerebellar signs.' All ofthem could merge with AD) and made clinical diagnoses in six other type 3, which was Parkinsonism with dementia patients. They emphasised many of the same and incontinence. Although the pathology of historical and clinical findings that we advance. these cases was heterogeneous, some included Babikian and Ropper also stressed similar data changes consistent with BD. Subsequent in a 1987 review of BD.6 However, both papers studies support Critchley's contention that 964 Fox Bennett, Wilson, Gilley, J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.11.961 on 1 November 1990. Downloaded from

vascular disease can result in pseudobulbar Hachinski's ischaemic score (IS)."52 First, the signs, Parkinsonian features and an akinetic- IS was not designed for BD though it has been rigid syndrome with dementia.' Although the used.53 In fact, less than half of the 62 patho- term "arteriosclerotic Parkinsonism" is logically verified cases ofBD in the English and currently out of vogue, in a recent survey of 33 French literature met IS criteria for multi- leading authorities in movement disorders infarct dementia. Second, we emphasise clini- from ten countries, 16 agreed that the designa- cal evidence of "subcortical" cerebral dys- tion is acceptable, while only six disagreed and function. Third, we incorporate radiological 11 were uncertain.47 confirmation of bilateral white matter path- In a recent clinical series, Parkinsonism was ology. Fourth, we eliminate items which are a common finding in vascular dementia in common in other dementias, for example, noc- general,48 and BD in particular.48 These turnal confusion, personality changes and patients had multiple strokes prohibiting pre- depression.54 And fifth, items which are cise clinico-anatomical correlations. However, difficult to assess and have poor interrater focal subcortical vascular lesions implicate the reliability are excluded.55 thalamus and putamen in disorders of stance, Although the diagnostic system presented gait and incontinence. Thus there is ample here holds promise, it is not without its limita- evidence to support the criteria of gait disor- tions. Most importantly, it cannot distinguish ders, Parkinsonism and incontinence. BD from mixed AD/BD. The same criticism is It is the role of neuroradiology in the diag- levied against the IS. Unfortunately, until nosis of BD which is perhaps the most con- there is a diagnostic marker for AD, this troversial. Rosenberg et al first reported limitation seems inevitable. Mixed AD/vas- bilateral white matter hypodensities on CT in a cular dementia probably represents the chance man with dementia, hypertension and spas- occurrence of two common diseases in the ticity, with pathologically proven BD.49 Loizou elderly. However, the combination of AD and et al followed this report by using similar CT BD may not always be fortuitous. Brun and findings to confirm the clinical diagnosis of BD England56 suggest that loss of myelin with in 15 patients.50 Their patients were clinically "incomplete" white matter infarction and reac- similar to Caplan's and one case of BD was tive gliosis are common histopathological find- verified at necropsy. In 1985, Kinkel et al ings in AD. These lesions are difficult to compared the sensitivity of MR in 23 patients distinguish from BD on MR scan and may (eight of whom were asymptomatic) with CT result from hypoperfusion.56 In addition, there documented "leukoencephalopathy of un- is some evidence implicating AD in the known origin".'5 MRI was unquestionably development of a neurogenic vasculopathy.57 more sensitive in delineating WMLs, and they Finally, the histopathological findings of BD concluded that "the lack of neurological find- may also be seen in patients with cerebral ings in this group is not necessarily inconsistent amyloid angiopathy with and without con- with the diagnosis of subcortical arterio- comitant AD.5859 sclerotic encephalopathy [BD].'5 A second problem is how to classify cases of A number of other investigators now mixed vascular dementia, that is mixed BD and advocate that WMLs on MRI are sufficient cortical strokes. In an effort to define a more evidence for a diagnosis of BD .7 Yet, several homogeneous sample of BD patients for studies have shown that not all white matter research purposes, we chose to exclude patients http://jnnp.bmj.com/ abnormalities on MR or CT are vascular."'2 In with more than one cortical stroke evident on fact, such lesions are seen in many individuals brain scan. Although Tomlinson et al recom- without neurological deficits and in about 30% mend that a diagnosis of MID requires at least of patients with typical AD.'3 They are highly 50 ml, and preferably 100 ml, ofinfarcted brain age-related among healthy elderly individuals tissue,1 this suggestion does not take into and also correlate with the presence of account lesion location, which studies demon-

cerebrovascular risk factors, though not neces- strate is important in the pathophysiology of on September 28, 2021 by guest. Protected copyright. sarily symptomatic cerebrovascular disease.9 0 vascular dementia.' In fact, in a recent clin- Despite this apparent lack of specificity, it does icopathological study of MID, only five of 23 appear that MRI scanning is exceptionally patients with a pathological diagnosis of vas- sensitive to vascular lesions. Furthermore, cular dementia had more than 50 ml of infarc- well-designed clinical studies have consistently ted tissue, and seven had less than 10 ml.6' demonstrated increased CT and MRI abnor- The status of BD resembles that of AD malities in vascular dementia, compared with before the seminal work of Tomlinson and his AD.5 Of the 62 pathologically verified reports colleagues 20 years ago. At that time, AD was of BD, 18 had a brain scan. Of those, 83-3% an underrecognised cause of mental deteriora- (15/18) showed leukoaraiosis on CT and 100% tion with poorly defined clinical features. Since (3/18) showed multiple bilateral white matter then the introduction of standardised criteria abnormalities on MRI. Finally, within our own for the clinical diagnosis of AD has greatly clinical series, the addition of the MRI increased diagnostic accuracy.396263 Standard criterion to the diagnostic system significantly ised criteria for BD are likely to have a similar reduced apparent misdiagnoses of patients impact on the study of this illness. Since CT with AD from 17-4% to. 1-6%. We submit and MRI abnormalities are common in the therefore that these radiological findings be elderly, clinical criteria must accompnay considered a necessary, but not sufficient, com- radiological findings when making the ponent of the clinical diagnosis of BD. antemortum diagnosis of BD. Such criteria Our criteria offer several advantages over should be specific enough to exclude patients Clinical diagnosis of Binswanger's disease 965 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.11.961 on 1 November 1990. Downloaded from

with AD from the sample. Our criteria meet matter involvement in subcortical arteriosclerotic ence- phalopathy (Binswanger disease). J Comput Assist Tomogr these objectives and should therefore prove 1980;4:14-9. useful in the prospective study of this puzzling 30 Goto K, Ishii N, Fukasawa H. Diffuse white matter disease in the geriatric population. Radiology 1981;141:687-95. disease. 31 Janota I. Dementia, deep white matter damage and hyper- tension: 'Binswanger's disease'. Psychol Med 1981; We are especially indebted to Dr Christopher Goetz, for 11(1):39-48. translating the French cases in addition to his perceptive 32 DeWitt LD, Kistler JP, Miller DC, Richardson EP Jr, criticism. We also thank Dr Raymond Clasen, for performing Buonanno FS. NMR-neuropathologic correlation in the pathology, Dr Michael Huckman, for reading our MRI scans stroke. Stroke 1987;18(2):342-51. and Cathy Mills for preparing the tables and references. This 33 study was supported in part by a grant from Garcia-Albea E, Cabello A, Franch 0. Subcortical arterio- the Chicago sclerotic encephalopathy (Binswanger's disease): a report Community Trust, Searle Fund. of five patients. Acta Neurol Scand 1987;75(5):295-303. 34 Mahler ME, Cumming JL, Tomiyasu U. Atypical dementia 1 Tomlinson BE, Blessed G, Roth M. Observations on the syndrome in an elderly man. J Am Geriat Soc 1987; brains of demented old people. J Neurol Sci 1970;11: 35:1116-26. 205-42. 35 Gupta SR, Naheedy MH, Young JC, Ghobrial M, Rubino 2 Schoenberg BS, Kokmen E, Okazaki H. Alzheimer's disease FA, Hindo W. Periventricular white matter changes and and other dementing illnesses in a defined United States dementia. Clinical, neuropsychological, radiological, and population: incidence rates and clinical features. Ann pathological correlation. Arch Neurol 1988;45:637-41. Neurol 1987;22:724-9. 36 Yvonneau M, Vital CL, Lafforgue J, Kinsala MS. L'en- 3 Brust JCM. Vascular dementia is overdiagnosed. Arch cephalopathie sous-corticale chronique de Binswanger. Neurol 1988;45:799-801. Bordeaux Med 1969;2:1135-41. 4 Scheinberg P. Dementia due to vascular disease-a multifac- 37 Huang K, Wu L, Luo Y. Binswanger's disease: progressive torial disorder. Stroke 1988;19:1291-9. subcortical encephalopathy or multi-infarct dementia? 5 Meyer JS, McClintic KL, Rogers RL, Simms P, Mortel KF. Can J Neurol Sci 1985;12(2):88-94. Etiological considerations and risk factors for multi- 38 Mikol J. Maladie de Binswanger et formes apparentees. Rev infarct dementia. J Neurol Neurosurg Psychiatry 1988; Neurol (Paris) 1968;118:111-32. 51:1489-97. 39 McKhann G, Drachman D, Folstein M, Katzman R, Price 6 Babikian V, Ropper AH. Binswanger's disease: a review. D, Stadlan EM. Clinical diagnosis ofAlzheimer's disease: Stroke 1987;18(1):2-12. report of the NINCDS-ADRDA Work Group under the 7 Roman GC. Senile dementia of the Binswanger type. A auspices of Department of Health and Human Services vascular form of dementia in the elderly. JAMA Task Force on Alzheimer's disease. Neurol 1984;34: 1987;258(13): 1782-8. 939-44. 8 Caplan LR, Schoene WC. Clinical features of subcortical 40 Rosen WG, Terry RD, Fuld PA, Katzman R, Peck A. arteriosclerotic encephalopathy (Binswanger's disease). Pathological verification of ischemic score in differentia- Neurology 1978;28:1206-15. tion of dementias. Ann Neurol 1980;7:486-8. 9 Awad IA, Spetzler RF, Hodak JA, Awad CA, Carey R. 41 Folstein MF, Folstein SE, McHugh PR. "Mini-Mental Incidental subcortical lesions identified on magnetic State": a practical method for grading the cognitive state resonance imaging in the elderly. I Correlation with age of patients for the clinician. J Psychiat Res 1975;12: and cerebrovascular risk factors. Stroke 1986;17:1084-9. 189-98. 10 Awad IA, Johnson PC, Spetzler RF, Hodak JA. Incidental 42 Gilley DW, Wilson RS, Bennett DA, Fox JH. Depression in subcortical lesions identifiedon magnetic resonance imag- putative Binswanger's disease. Ann Neurol 1989;26:154. ing in the elderly. II Postmortem pathological correla- 43 Bernard BA, Wilson RS, Gilley DW, Waters WF, Fox JH. tions. Stroke 1986;17:1090-7. Semantic encoding and episodic memory in Alzheimer's 11 Braffman BH, Zimmerman RA, Trojanowski JQ, et al. disease and multi-infarct dementia. J Clin Exp Neuro- Brain MR: pathological correlation with gross and his- psychol 1989;11:52-3. topathology. 1 Lacunar infarction and Virchow-Robin 44 Mancardi GL, Romangnoli P, Tassinari T, Gandolfo C, spaces. Am JNeuro Radiol 1988;9:621-8. Primavera A, Loeb C. Lacunae and cribiform cavities of 12 Braffman BH, Zimmerman RA, Trojanowski JQ, et al. the brain. Eur Neurol 1988;28:11-7. Brain MR: pathological correlation with gross and his- 45 Thompson PD, Marsden CD. Gait disorder of subcortical topathology. 2 Hyperintense white-matter foci in the arteriosclerotic encephalopathy: Binswanger's disease. elderly. Am J Neuro Radiol 1988;9:629-36. Mov Disord 1987;2(1):1-8. 13 Wilson RS, Bennett DA, Fox JH, et al. Alzheimer's disease: 46 Critchley M. Arteriosclerotic Parkinsonism. Brain 1929; prevalence and clinical significance of white-matter 52:23-83. lesions on magnetic resonance imaging. Ann Neurol 47 Duvoisin RC, Golbe LI. Towards a definition ofParkinson's 1988;24(1):160-1. disease. Neurology 1989;39:746. 14 Ladame C. Encephalite sous-corticale chronique. 48 Kotsoris H, Barclay LL, Kheyfets S, Hulyalkar A, Dough- L'Encephale 1912;7:13-39. erty J. Urinry and gait disturbance as markers for early 15 Kinkel WR, Jacobs L, Polachini I, Bates V, Heffner RR Jr. multi-infarct dementia. Stroke 1987;18:138-41. Subcortical arteriosclerotic encephalopathy (Binswan- 49 Rosenberg GA, Kornfeld M, Stovring J, Bicknell JM. ger's disease). Computed tomographic, nuclear magnetic Subcortical arteriosclerotic encephalopathy (Binswan- http://jnnp.bmj.com/ resonance, and clinical correlations. Arch Neurol 1985; ger): computerized tomography. Neurology 1979;29: 42(10):951-9. 1102-6. 16 Aronson SM, Perl DP, eds. Clinical neuropathological 50 Loizou LA, Kendall BE, Marshall J. Subcortical arterios- conference. Dis Nerv Syst 1974;35:286-91. clerotic encephalopathy: a clinical and radiological inves- 17 Biemond A. On Binswanger's subcortical arteriosclerotic tigation. JNeurol Neurosurg Psychiatry 1981;44:294-304. encephalopathy and the possibility of its clinical recogni- 51 Erkinjuntti T, Ketonen L, Sulkava R, Vuorialho M, Palo J. tion. Psychiatr Neurol Neurochir 1970;73:413-7. Do white matter changes on MRI and CT differentiate 18 Dubas F, Gray F, Roullet E, Escourolle R. Leucoence- vascular dementia from Alzheimer's disease? J Neurol phalopathies arteriopathiques. Rev Neurol (Paris) Neurosurg Psychiatry 1987;50:37-42. 1985;141 :93-108. 52 Hachinski VC, IliffLD, Zilhka E, et al. Cerebral blood flow 19 Dupuis M, Brucher JM, Gonsette RE. Anatomo-clinical in dementia. Arch Neurol 1975;32:632-7. observation of atherosclerotic subcortical encephalopathy 53 Hershey LA, Modic MT, Jaffe DF, Greenough PG. Natual on September 28, 2021 by guest. Protected copyright. ("Binswanger's disease") with hypodensity of the white history of the vascular dementias: a prospective study of matter on brain scan. Acta Neurol Belg 1984;84(3): seven cases. Can JNeurol Sci 1986;13:559-65. 131-40. 54 Gilley DW, Wilson RS, Bennett DA, Bernard BA, Fox JH. 20 Garcin R, Lapresle J, Lyon G. Encephalopathie sous- Predictions of behavioural disturbance in Alzheimer's corticale chronique de Binswanger. rev Neurol (Paris) disease. JGerontol (in press). 1960;102:423-40. 55 Gustafson L, Nilsson L. Differential diagnosis of presenile 21 Hurwitz BJ, Heyman A, Burger PC, Drayer BP. Subcortical dementia on clinical grounds. Acta Psychiatr Scand arteriosclerotic encephalopathy (Binswanger's disease). 1982;65:194-209. Report of a case simulating psychiatric disease and normal 56 Brun A, Englund E. A white matter disorder in dementia of pressure hydrocephalus. NC Med J 1987;48(4):182-6. the Alzheimer type: a pathoanatomical study. Ann Neurol 22 Ishino H, Higashi H, Hayahara T, Ikeda H, Otsuki S. A case 1986;19:253-62. of subcortical arteriosclerotic encephalopathy (Binswan- 57 Scheibel AB, Duong T, Tomiyasu U. Denervation micro- ger's disease). Folia Psychiatr Neurol Jpn 1972;26(1): angiopathy in senile dementia, Alzheimer type. Alzheimer 39-44. Disease Assoc Dis 1987;1:19-37. 23 Jelgersma HC. A case of encephalopathia subcorticalis 58 Gray F, Dubas F, Roullet E. Escourolle R. Leukoen- chronica (Binswanger's disease). Psychiatr Neurol 1964; cephalopathy in diffuse hemorrhagic cerebral amyloid 147:81-9. angiography. Ann Neurol 1985;18:54-9. 24 Rousseau P. Binswanger's disease: a cause of dementia in the 59 Bird TD, Sumi SM, Nemens EJ, et al. Phenotypic elderly. South Med J 1988;81(10): 1329-30. heterogeneity in familial Alzheimer's disease: a study of24 25 Olszewski J. Subcortical arteriosclerotic encephalopathy. kindreds. Ann Neurol 1989;25:12-25. World Neurol 1965j3:359-74. 60 Loeb C, Gandolfo C, Bino G. Intellectual impairment and 26 Earnest MP, Fahn S, Karp JH. Normal pressure hydro- cerebral lesions in multiple cerebral infarcts. A clinical- cephalus and hypertensive cerebrovascular disease. Arch computed tomography study. Stroke 1988;19:560-5. Neurol 1974;31:262-6. 61 Erkinjuntti T, Haltia M, Palo J, Sulkava R, Paetau A. 27 Burger PC, Burch JG, Kunze U. Subcortical arteriosclerotic Accuracy of the clinical diagnosis of vascular dementia: a encephalopathy (Binswanger's disease). A vascular prospective clinical and post-mortem neuropathological etiology of dementia. Stroke 1976;7(6):626-31. study. JNeurol Neurosurg Psychiatry 1988;51:1037-44. 28 Koto A, Rosenberg G, Zingesser LH, Horoupian D, Katz- 62 Khachaturian ZS. Diagnosis of Alzheimer's disease. Arch man R. Syndrome of normal pressure hydrocephalus: Neurol 1985;42:1097-105. possible relation to hypertensive and arteriosclerotic vas- 63 Fox JH, Penn R, Clasen R, et al. Pathological diagnosis in culopathy.J Neurol Neurosurg Psychiatry 1977;40:73-9. clinically typical Alzheimer's disease. New Engl J Med 29 Zeumer H, Schonsky B, Sturm KW. Predominant white 1985;313:1419-20.