(Stroke. 1995;26:1293-1301.)
© 1995 American Heart Association, Inc.
Articles |
The Significance of Cerebral White Matter Abnormalities 100 Years After Binswanger's Report
A Review
From the Department of Pathology (Neuropathology), Henry Ford Hospital, Detroit, Mich (L.P., J.H.G.); the Department of Pathology (Neuropathology), Case Western Reserve University, Cleveland, Ohio (J.H.G.); and the Department of Neurological and Psychiatric Sciences, University of Florence (Italy) (L.P.).
Correspondence to Julio H. Garcia, MD, Department of Pathology (Neuropathology), Henry Ford Hospital, K-6, 2799 W Grand Blvd, Detroit, MI 48202-2689.
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Abstract |
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Background Changes in the cerebral hemispheric white matter are detected with increasing frequency by CT and MRI among persons older than 60 years. The pathogenesis, clinical significance, and morphological substrate of these changes are incompletely understood. Patients who have such neuroimaging abnormalities are sometimes diagnosed with "Binswanger's disease," an eponym that has generated much confusion because of its imprecise meaning. The objectives of this study were to determine whether the term Binswanger's disease merits acceptance as a distinct clinicopathologic entity, to deduce the clinical significance of these white matter abnormalities from the analysis of appropriate publications, and to evaluate studies that correlate in vivo changes in the cerebral white matter with pathological features.
Summary of Review We evaluated Binswanger's original case description and, after conducting a Medline search, reviewed more than 160 publications, mostly in the English language, on the subject of white matter abnormalities detectable by currently used neuroimaging methods (ie, leukoaraiosis).
Conclusions Binswanger's original description appears to be insufficient for the purpose of defining a new nosological entity. After evaluating the vaguely outlined pathological correlates described in a few of these subcortical cerebral leukoencephalopathies, we conclude that the clinical significance of leukoaraiosis remains incompletely defined. However, its frequency increases with age independent of other risk factors, and in nondemented subjects leukoaraiosis is associated with deficits in selected cognitive functions. Moreover, leukoaraiosis correlates with an increased risk for the subsequent development of strokes. We make specific suggestions for future studies that may help to clarify this topic.
Key Words: leukoencephalopathy • small-vessel disease • leukoaraiosis • dementia
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Introduction |
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TopAbstractIntroductionHistorical OverviewLeukoaraiosisConclusionsReferences |
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The application of CT in the 1970s and the subsequent application of MRI to image the intracranial contents have revealed an unexpected number of changes in the cerebral white matter of both asymptomatic and cognitively impaired individuals.
The pathogenesis, clinical significance, and pathological substrate of these white matter alterations are incompletely understood. Even the optimal term to designate these changes is controversial; some authors assume that the cerebral white matter changes (demonstrated by CT or MRI) are synonymous with "Binswanger's disease" (an eponym of nebulous meaning), while others use the term leukoaraiosis to refer to all white matter changes visible on neuroimaging studies.
We reviewed a selected number of publications, most of which appeared after 1979, for the purpose of (1) determining whether the term Binswanger's disease merits its acceptance as a distinct clinicopathologic entity, (2) summarizing a large and controversial number of publications dealing with the clinical relevance of white matter abnormalities detected by either CT or MRI, and (3) evaluating studies based on the correlation observed between in vivo observations and histopathological analysis of cerebral white matter.
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Historical Overview |
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In 1894, in a lengthy manuscript dealing with the differential diagnosis of general paresis of the insane, Otto Binswanger described the case of a syphilitic man in his mid-fifties who had developed a progressive decline in mental functions characterized by speech and memory disorders, depression, and personality changes, accompanied by diminished motor power in the lower extremities and slight hand tremor.1 2 At autopsy, the dura mater at the base of the skull showed granular deposits; there was also minimal intracranial atherosclerosis, considerable enlargement of the lateral ventricles, marked atrophy of the cerebral white matter, and multiple ependymal thickenings.1 2
Binswanger neither provided microscopic descriptions nor illustrated any findings of this single case; an additional seven cases were mentioned in a footnote, but these cases were never further described. In subsequent publications Binswanger did not deal again with the topic of white matter disease, and in fact he did not attribute much significance to the case included in his 1894 report.3 In 1902 Alzheimer,4 5 referring to the case described by his mentor Otto Binswanger, added a short histological description of what he considered was an analogous case and intuitively attributed the white matter changes to arteriosclerosis of the long penetrating vessels. In 1962 J. Olszewski,6 after careful review of Binswanger's original report, suggested that the lesions in the dura mater and in the ependyma, together with the history of syphilis, made Binswanger's a likely case of neurosyphilis; accordingly, he proposed the term subcortical arteriosclerotic encephalopathy to describe "a form of cerebral arteriosclerosis in which vessels of the white matter and subcortical grey matter are affected predominantly."6 Significantly, as of 1987 when Babikian and Ropper7 wrote a review, the pathological diagnosis of this obscure entity (Binswanger's disease or subcortical arteriosclerotic encephalopathy) was limited to fewer than 50 cases.
Contemporaneously, the diagnosis of Binswanger's disease (ie, cerebral white matter abnormalities) had acquired new popularity after the introduction of CT and its first diagnosis based on clinical and CT findings.8 The increasing availability of CT and MRI led many to assume that Binswanger's disease could be diagnosed premortem.9 10 11 12 13 14 15 However, it soon became apparent that alterations of the hemispheric white matter (detected by either CT or MRI) were common in both symptomatic and asymptomatic subjects. Román16 17 suggested that among asymptomatic individuals, the white matter abnormalities seen on CT or MRI might represent an early form of Binswanger's disease.
Today it seems impossible to determine with certainty the nature of the disease affecting the patient vaguely described by Binswanger, but it seems reasonable to conclude that Binswanger's description cannot be applied to what was later considered a form of dementia secondary to cerebral atherosclerosis.16 Moreover, it may be futile to label patients showing radiological white matter abnormalities of unknown origin as having a disease for which definite clinical or pathological criteria do not exist. For these reasons we suggest that the eponym Binswanger's disease lacks medical significance or relevance.
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Leukoaraiosis |
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Definition
In an attempt to overcome the tendency to identify a neuroimaging abnormality with a vaguely defined disease process, Hachinski et al18 19 introduced the term leukoaraiosis (from the Greek leuko [white] and araiosis [rarefaction]) to designate periventricular or subcortical (centrum semiovale) areas of hypodensity on CT or hyperintensity on T2-weighted MRI whose origin deserves further elucidation. The term leukoaraiosis (LA) refers to both the CT- and MRI-detectable alterations, although the lesions are not completely superimposable as to number, site, and extension.20 21 22 23 24 25 26 27 Also, some authors suggest that MRI can detect LA at an earlier stage than CT.28 For these reasons, in this review we discuss LA as seen separately on CT and MRI.
Frequency
LA is frequently detected by CT and MRI both in asymptomatic
persons older than 60 years and in cognitively impaired individuals,
especially those who have evidence of either cerebrovascular disease or
risk factors associated with stroke.29 Among patients with
dementia of presumed vascular origin (VaD), LA is detected by CT in
41% to 100%20 30 31 32 33 34 35 36 37 38 39 and by MRI in 64% to 100% of the
cases.20 30 40 41 42 43 44 45 46 47 This increased frequency of LA among
patients who have risk factors associated with vascular disease is one
of the clues suggesting a possible ischemic pathogenesis for
LA. Thus, it is intriguing that a large proportion of
Alzheimer's disease (AD) patients (ranging from 19% to 78%
in CT-based studies20 30 31 32 33 34 35 38 39 48 49 50 51 52 53 54 55 and from 7.5% to
100% in MRI studies20 22 30 40 42 43 44 45 47 52 56 57 58 59 60 ) have
LA, although usually the changes in white matter density are less
severe in AD patients than in those with cerebrovascular
disorders.40 42 44 47 48 61 White matter abnormalities in
patients with AD, according to some authors, might be associated with
cerebral congophilic angiopathy, one of the microscopic hallmarks of
AD.62 63
LA in normal control subjects is usually less severe than in demented patients,45 57 64 yet LA is detected in up to 21% of asymptomatic subjects evaluated with CT30 31 32 39 49 50 52 65 and in up to 100% among those evaluated with MRI.22 27 30 40 42 43 44 45 52 56 57 60 61 66 67 68 69 70 71 72 73 74 75 Inference on the prevalence of LA in the normal population cannot be deduced from these investigations because the definition of normal subjects varies in each study. Two recent population-based studies76 77 reported MRI-detectable LA (MRI-LA) in 27% and 38% of subjects with a mean age greater than 65.
A wide discrepancy exists among reports dealing with the frequency of LA. This can be attributed to the inclusion of subjects with different ages, variably associated cerebrovascular risk factors and, in MRI studies, application of diverse strengths of magnetic field and variations in pulse sequence, as well as on different definitions of MRI-LA. A frequently used classification separates MRI-LA into periventricular and deep subcortical lesions and grades each according to its severity.40 Periventricular MRI-LA is detected more frequently than deep subcortical (centrum semiovale) MRI-LA; however, not all authors considered these lesions separately.22 25 61 78 79 80
Effect of Aging and Cerebrovascular Risk Factors
Both the frequency and the severity of CT-detectable LA
(CT-LA) and MRI-LA increase with aging, as reported in patients with
diverse diseases,15 25 30 44 56 72 78 79 80 81 82 83 84 85 86 87 88 89 90 in normal
volunteers,22 49 56 61 68 69 70 71 73 74 75 76 82 83 90 91 92 93 94 95 and in two
population-based studies.77 93 Only a minority of studies
found a lack of correlation between aging and either the presence or
severity of MRI-LA.41 44 71 96 With the exception of one
CT-based study,32 the association between LA and aging
exists independent of the increased presence of vascular risk factors
in persons older than 60 years
(Table
).47 76 82 84 87 95 97 98 99
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Arterial hypertension is commonly associated with changes in the white
matter detectable by CT. This association exists in patients with
cerebrovascular accidents and dementia35 50 54 81 100 101
as well as in asymptomatic control subjects.49 The
exclusion of patients with chronic hypertension from the diagnosis of
AD may explain why in some studies there was no increased frequency of
hypertension among AD patients with CT-LA.49 51 81
However, when the importance of history of stroke and of hypertension
are contemporaneously evaluated, the former becomes
equal97 to or more important32 99 than
hypertension as a predictor of LA (Table
). Evidence of CT-LA, in
particular, correlates with lacunar infarcts97 and
intracerebral hemorrhage,102 two entities
that have a close association with arterial hypertension. It seems
surprising that one study reported an association between CT-LA and a
systolic blood pressure lower than 130 mm Hg, together with evidence
of heart failure.39 Probably this is because hypertension
plays a fundamental role in the development of early changes affecting
the long penetrating arteries of the white matter.103
After arteriolosclerotic changes such as hyalinization begin to affect
many cerebral blood vessels, transient decreases in cerebral blood flow
(as elicited by cardiac dysrhythmia, improper administration of
antihypertensive therapy, or failure of autoregulatory mechanisms, as
recently demonstrated in patients with CT-LA104 ) could
lead to ischemic injury of the periventricular white matter.
The periventricular white matter corresponds to a terminal field, and
this could make it selectively vulnerable to changes in blood
pressure.105 The fact that the degree of carotid stenosis
does not influence the severity of LA99 indirectly
supports the view that LA is closely linked to disease of small
arteries and arterioles.
An association between LA and risk factors for cerebrovascular
disease has been shown repeatedly by MRI-based
studies.15 26 27 44 56 66 70 74 75 78 79 80 85 88 106 107 The
application of multivariate analysis does not provide concordant
results among all the studies reviewed (Table); nevertheless, it
appears reasonable that risk factors associated with cerebrovascular
disease may worsen a process such as LA, which is sensitively
influenced by aging.
Cognitive Impairment
Few topics in neurology are as controversial as the issue of
whether LA may influence the severity of cognitive impairment among
demented patients or the cognitive prowess of otherwise normal
subjects.
A correlation between cognitive impairment and the presence or severity of CT or MRI-LA has been inconsistently reported in AD patients40 43 45 53 55 56 59 96 108 and in studies that failed to specify the type of demented patients included.21 30 42 61 88 Among patients with dementia of presumed vascular origin, only the severity of LA (graded on MR images46 106 109 ) rather than its presence (on CT32 110 ) correlates with the degree of dementia.
Although seeking cognitive abnormalities in normal subjects with LA might appear tautological, a few studies have shown that CT-LA111 or MRI-LA43 67 68 69 107 does not significantly influence the general cognitive profile of normal volunteers.
Because aging as well as other associated factors may influence cognitive performances, the use of multivariate analyses is essential in this evaluation. After controlling for the possible confounding effects of age, sex, level of education, and the neuroimaging evidence of brain infarcts, CT-LA correlates with low neuropsychological scores in nondemented subjects.65 Among cognitively impaired patients, CT-LA is not associated with the diagnosis of dementia32 ; however, these patients show a trend toward low cognitive performance with respect to demented patients without CT-LA.48 In contrast, multivariate analysis results based on MRI data partially deny that LA would affect cognition in nondemented patients84 or in normal subjects.69 74 75 One possible explanation for the disparity in the results obtained by CT- and MRI-based studies is that MRI tends to detect a larger number of milder lesions than CT, and it is therefore less specific. In fact, a significant difference in cognitive and neurobehavioral functions is found when normal volunteers with a marked degree of MRI-LA are compared with those without LA.93 94 Quantitating the severity of MRI-LA may be necessary in future studies. A threshold exists between the extent of MRI-LA and subtle cognitive impairment; among 100 volunteers participating in a single study, those in whom MRI-LA involved an area greater than 10 cm2 had significant decreases in cognitive performances involving frontal lobe abilities, attention, and speed of information processing.73 An added possible cause of inconsistency among various studies may derive from the application of neuropsychological tests that are acceptable for screening purposes but are inadequate to detect subtle or specific cognitive functional changes; for example, among patients with the same severity of dementia, tests that evaluate individual cognitive areas revealed differences depending on the presence or absence of periventricular MRI-LA.42 44 Among nondemented subjects, MRI-LA influences mental tasks involving speed of mental processing and attention.28 75 90 95 107 Because not all of these differences are obvious, their clinical significance should be reexamined. Two studies report that subjective memory impairment is more frequently noted by subjects with MRI-LA than by those without LA.28 77
In evaluating the effect of neuroimaging abnormalities on cognitive prowess, atrophy of corpus callosum and enlarged caliber of the lateral ventricles should be weighed; both of these could be equally as important93 109 112 as or more important113 than LA in determining cognitive deterioration. The marked atrophy of the cerebral white matter in advanced stages of leukoencephalopathy may lead to ex vacuo enlargement of the lateral ventricles; at least one study has shown a positive correlation between the severity of MRI-LA and ventricular enlargement.93
Other Clinical Findings
In addition to cognitive impairment, gait
disturbances,31 49 65 68 97 tendency to
fall,111 extensor plantar reflex,48 65 97 and
primitive reflexes65 90 97 are the most common
neurological abnormalities associated with LA, and their existence is
thought to be related to injury to the subcortical brain regions. An
increased prevalence of MRI-LA has been recently described in a variety
of psychiatric disorders.80 114 115 116 117 118 119 120 121 122 123 124 125 However, some of these
studies are noncontrolled, are based on small numbers of patients, and
do not take into account associated risk factors; therefore, many of
these observations await corroboration.
Prognostic Significance
The presence of LA in patients with history of
cerebrovascular accidents101 126 or probable
AD55 suggests an increased incidence of subsequent stroke.
However, LA may be only one of the poor prognosis indicators; the true
determinants are aging, arterial hypertension, presence of lacunes on
CT, and electrocardiographic abnormalities.127 LA does not
seem to influence the progression of global cognitive impairment in AD
patients,86 108 128 and in normal subjects LA is
associated only with a more rapid decline in visuospatial, associative,
and psychomotor functions.92 A clinicopathologic study
showed early death occurrence and faster progression of mental
impairment among AD patients who had pathological evidence of more
severe decrease in the number of myelinated fibers,
suggesting that the severity of LA, rather than its presence, is a
reliable prognostic factor.62
CADASIL
Recently a condition first described in 1977129 and
characterized by multiple subcortical infarcts, leukoencephalopathy,
and an autosomal dominant pattern of inheritance (CADASIL [cerebral
autosomal dominant arteriopathy with subcortical infarcts and
leukoencephalopathy]) has received new attention after the genetic
defect was mapped to chromosome 19q12.130 CADASIL is
clinically characterized by recurrent strokes and a terminal picture of
dementia; pathologically, small deep infarcts and leukoencephalopathy
are associated with a concentric thickening of the wall of the small
vessels secondary to granular eosinophilic deposits in the tunica
media.131 132 At present, CADASIL accounts for only a
very small number of cases with LA,133 but close study of
this condition could shed light on the pathogenesis of white matter
abnormalities related to small-vessel disease.
Pathological Correlates
Understanding the pathological correlates of LA might help
to elucidate the pathogenesis of these lesions. The correlation between
LA and postmortem findings has been evaluated in cases in which CT or
MRI showed LA at a time closely related to autopsy or in cases in which
postmortem MRI examination of the brain was completed. Although fewer
white matter abnormalities are noted postmortem compared with in vivo
MRI,134 the postmortem observations are considered
valuable.135 136
Periventricular LA correlates with decreased myelin content,137 138 139 140 141 142 143 144 loss of ependymal cell layer and reactive gliosis (also called granular ependymitis) at the tip of the frontal horns,137 138 139 140 141 143 145 increased periependymal extracellular fluid content, and smaller and fewer axons.138 Some authors have also found enlarged perivascular spaces at this periventricular location.141 Small periventricular lesions exist in all age groups (including newborns)138 144 ; therefore, such findings probably do not constitute a true abnormality.
The histological correlates of deep subcortical MRI-LA are even less consistent than those noted for periventricular LA. Punctate abnormalities correspond to enlarged perivascular spaces,137 143 small cavitary infarcts (or lacunes),146 147 148 demyelinating plaques, brain cysts, and congenital diverticula of the lateral ventricles.147 MRI methods seem adequate to distinguish between enlarged Virchow-Robin spaces and lacunar infarcts,145 149 but in some cases the corresponding pathological abnormality of punctate lesions was undetectable.134 142 147 148 The more diffuse lesions in the centrum semiovale have been related to myelin rarefaction that spares the U fibers,135 137 sometimes accompanied by astrogliosis,139 and to diffuse vacuolization of the white matter.148 The myelin rarefaction does not correspond to true demyelination since the process also involves destruction of the axons.62 135 150 151 Thickening of the wall of the small vessels is also found in these areas.135 139 140 142 146 151 For these diffuse subcortical lesions the radiological-pathological correlation is not very tight: myelin loss is sometimes present in areas without LA151 or is more extensive than shown by MRI.151
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Nomenclature
According to some authors Binswanger's disease has well-defined neuropathological features,152 153 154 while others suggest validation of clinical criteria155 based on pathological characteristics attributed to Olszewski.6 However, the pathological criteria remain vaguely outlined, and Binswanger's original description is clearly insufficient to define a new nosological entity. Many cases described under the eponym Binswanger's disease share some pathological findings,7 16 156 157 but the same type of histological abnormalities can also be seen in a wide variety of unrelated conditions.63 158 159 We believe that the term Binswanger's disease should be avoided. Instead, the more descriptive terms of LA and subcortical leukoencephalopathy can be reserved for the radiological and pathological communications.
Clinical Significance of LA
The clinical significance of LA remains incompletely defined.
However, some conclusions seem warranted at this time. (1) LA is part
of the aging process; the addition of cerebrovascular risk factors
aggravates LA. (2) In subjects who have no or only moderate cognitive
impairment, LA, especially of the most severe degrees, influences
specific cognitive functions, such as those involving speed of mental
processes. LA may also contribute to the cognitive decline in patients
with AD and VaD, but to demonstrate a correlation once the dementia is
fully developed is extremely arduous. (3) Persons with LA have an
increased risk of cerebrovascular events. It remains to be shown
whether this conclusion can be applied only to specific categories of
patients, eg, those with previous cerebrovascular accidents.
Possible Causes of Inconsistency in Past Studies
Uncertainties regarding the significance of LA stem from our poor
understanding of its pathogenesis160 161 and the
incomplete definition of its pathological features. Factors that may
account for the discrepancy in results obtained in large numbers of
epidemiological studies include (1) small numbers and
heterogeneous cohorts of patients, (2) application of
different classifications of LA, and (3) use of disparate
neuropsychological tests. An added source of possible variability
includes poor interobserver agreement on the radiological assessment of
LA; among CT-based studies this agreement was substantial in
three96 102 162 and almost perfect in two
studies.99 163 The interobserver agreement in the
evaluation of MRI-LA was moderate in one,96 substantial in
three,56 87 164 and almost perfect in another
study.76
Future Approaches
Three future endeavors are recommended: (1) to define the
responses of white matter to various types of ischemic injury
in suitable experimental models, (2) to explore the potential vascular
pathogenesis of specific types of leukoencephalopathy associated with a
genetic pattern of inheritance, and (3) to investigate the clinical and
pathological correlates of distinct degrees of severity of LA
(especially MRI-LA) in well-defined populations and at specific brain
locations. In this context the adoption of a uniform neuroimaging
nomenclature and the application of uniform and specific
neuropsychological tests will be invaluable. A multicenter study could
provide the large number of observations necessary to conduct the
required statistical analyses.
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Acknowledgments |
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We thank Drs S.R. Levine (Detroit, Mich), G.G. Brown (Detroit, Mich), and G. Molinari (Easton, Md) for their valuable contributions during the embryonic stages of manuscript preparation and Paula McGee, Lisa Pietrantoni, and Kathy Zajas for their secretarial assistance.
Received February 28, 1995; revision received April 12, 1995; accepted April 12, 1995.
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A. Chamorro, J. Pujol, A. Saiz, N. Vila, J. C. Vilanova, M. Alday, and R. Blanc Periventricular White Matter Lucencies in Patients With Lacunar Stroke: A Marker of Too High or Too Low Blood Pressure? Arch Neurol, October 1, 1997; 54(10): 1284 - 1288. [Abstract] [PDF]
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R. Mantyla, T. Erkinjuntti, O. Salonen, H. J. Aronen, T. Peltonen, T. Pohjasvaara, and C.-G. Standertskjold-Nordenstam Variable Agreement Between Visual Rating Scales for White Matter Hyperintensities on MRI : Comparison of 13 Rating Scales in a Poststroke Cohort Stroke, August 1, 1997; 28(8): 1614 - 1623. [Abstract] [Full Text]
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V. I. H. Kwa, J. Stam, L. M. Blok, B. Verbeeten Jr, and f. t. A. V. M. Group T2-Weighted Hyperintense MRI Lesions in the Pons in Patients With Atherosclerosis Stroke, July 1, 1997; 28(7): 1357 - 1360. [Abstract] [Full Text]
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R. Schmidt, H. Schmidt, F. Fazekas, M. Schumacher, K. Niederkorn, P. Kapeller, V. Weinrauch, and G. M. Kostner Apolipoprotein E Polymorphism and Silent Microangiopathy-Related Cerebral Damage : Results of the Austrian Stroke Prevention Study Stroke, May 1, 1997; 28(5): 951 - 956. [Abstract] [Full Text]
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L. Pantoni and J. H. Garcia Pathogenesis of Leukoaraiosis : A Review Stroke, March 1, 1997; 28(3): 652 - 659. [Abstract] [Full Text]
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L. Pantoni, J. H. Garcia, J. A. Gutierrez, and W. I. Rosenblum Cerebral White Matter Is Highly Vulnerable to Ischemia Stroke, September 1, 1996; 27(9): 1641 - 1647. [Abstract] [Full Text]
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G. C. Roman From UBOs to Binswanger's Disease: Impact of Magnetic Resonance Imaging on Vascular Dementia Research Stroke, August 1, 1996; 27(8): 1269 - 1273. [Full Text]
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W.T. Longstreth, T. A. Manolio, A. Arnold, G. L. Burke, N. Bryan, C. A. Jungreis, P. L. Enright, D. O'Leary, and L. Fried Clinical Correlates of White Matter Findings on Cranial Magnetic Resonance Imaging of 3301 Elderly People: The Cardiovascular Health Study Stroke, August 1, 1996; 27(8): 1274 - 1282. [Abstract] [Full Text]
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N. Watanabe, Y. Imai, K. Nagai, I. Tsuji, H. Satoh, M. Sakuma, H. Sakuma, J. Kato, N. Onodera-Kikuchi, M. Yamada, et al. Nocturnal Blood Pressure and Silent Cerebrovascular Lesions in Elderly Japanese Stroke, August 1, 1996; 27(8): 1319 - 1327. [Abstract] [Full Text]
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