(Stroke. 2000;31:2665.)
© 2000 American Heart Association, Inc.
Original Contributions |
Frequency and Location of Microbleeds in Patients With Primary Intracerebral Hemorrhage
From the Department of Neurology (G.R., A.L., R.S., E.F., H.-P.H., F.F.) and the MR Institute (A.L., R.S., F.F.), Karl-Franzens University, Graz, Austria.
Correspondence to Franz Fazekas, MD, Department of Neurology, Karl-Franzens University, Auenbruggerplatz 22, A-8036 Graz, Austria. E-mail franz.fazekas{at}kfunigraz.ac.at
 |
Abstract |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Background and Purpose—MRI is known to detect clinically silent microbleeds (MBs) in patients with primary intracerebral hemorrhage (pICH), but the frequency and diagnostic and clinical significance of this finding are still debated. Therefore, we investigated a consecutive series of pICH patients and analyzed the patterns of MB distribution in the context of clinical variables and location of the symptomatic hematoma.
Methods—The study population consisted of 109 patients with pICH. There were 59 women and 50 men aged 22 to 91 years (mean 64.6 years). MRI was obtained on a 1.5-T system with use of a gradient-echo T2*-weighted sequence. A cohort of 280 community-dwelling asymptomatic elderly individuals who underwent the same imaging protocol served for comparison.
Results—MBs were seen in 59 (54%) patients and ranged in number from 1 to 90 lesions (mean 14, median 6). In the majority of patients, MBs were located simultaneously in various parts of the brain, with a preference for cortical-subcortical regions (39%) and the basal ganglia/thalami (38%). There was some tendency toward a regional association between MB location and the site of the symptomatic hematoma, but we could not discern specific patterns of MB distribution. Logistic regression analysis identified MBs, periventricular hyperintensity grades, and lacunes but not risk factors as independent variables contributing to a correct classification of pICH and control individuals.
Conclusions—MBs can be detected in more than half of the patients with pICH and appear to be quite general markers of various types of bleeding-prone microangiopathy.
Key Words: etiology • hemosiderin • intracerebral hemorrhage • magnetic resonance imaging • microcirculation
|
Introduction |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Magnetic resonance imaging (MRI) has the potential to reveal residues of intracerebral bleeding throughout life because of its high sensitivity for iron-containing compounds. At the site of intracerebral hemorrhage (ICH), hemosiderin remains stored in macrophages and leads to focal dephasing of the MRI signal. This causes areas of past bleeding to appear dark on T2-weighted images. Gradient-echo techniques with high sensitivity for differences in magnetic susceptibility enhance these effects of hemosiderin.1 Previous studies have called attention to the frequent observation of small areas of signal loss in patients with primary ICH (pICH), which were suggested to represent residues of earlier clinically silent microbleeds (MBs).2 3 Subsequently, this assumption was supported by correlative histopathologic data, which confirmed perivascular hemosiderin deposition around angiopathic arterioles as the predominant cause for such a finding.4 5 The association with small-vessel diseases explains that MBs were also reported in patients with cerebral ischemic damage5 6 and even in a small proportion of asymptomatic elderly individuals.7 However, the clinical and diagnostic significance of this finding is not yet fully understood.
In patients with pICH, the reported frequency of earlier MBs ranges from 17% to 80%.8 These large differences are probably a consequence of small patient groups examined, differences in patient selection, and the inconsistent use of either conventional spin-echo or gradient-echo MR techniques or both.8 Although hypertensive microangiopathy appears to be their prevailing cause, MBs have also been strongly associated with the presence of cerebral amyloid angiopathy.9 In this context, a cortical-subcortical appearance of MBs has been suggested to be an almost pathognomonic finding.3 On the basis of this assumption, it could be speculated that certain patterns in the distribution of MBs may serve to indicate different types of microangiopathy. The amount of predictive information contained in the detection of MBs and possible concerns regarding the use of anticoagulants in such patients have also been debated.
We attempted to provide further information on these aspects by performing a detailed analysis of the frequency and distribution patterns of MBs in the context of clinical variables and hematoma location in a large consecutive series of patients with pICH. We also performed a comparison with findings in a community-dwelling cohort of asymptomatic elderly individuals, and a logistic regression analysis was carried out to define the contribution of MBs to the correct identification of pICH patients.
|
Subjects and Methods |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The study population consisted of 109 patients with a final diagnosis of pICH from consecutive referrals to MRI by the neurology department of a university hospital. This included all patients admitted with intracerebral bleeding who were able to undergo such an examination. pICH was defined as spontaneous nontraumatic intracerebral bleeding without evidence of any kind of vascular malformation or a brain tumor as the source of the hematoma. The patients’ ages ranged from 22 to 91 years (mean 64.9 years); there were 59 women and 50 men. Other demographic and clinical variables are shown in Table 1
. Hypertension was diagnosed in the case
of a past history of increased blood pressure or if the blood pressure
recordings continued to repeatedly exceed 160/95 mm Hg
past the second week after the ICH. Diabetes mellitus was defined by
fasting blood sugar >140 mg% or previous treatment. Twenty-four
patients had suffered from a previous stroke, which was reportedly
hemorrhagic in 9 patients.
|
MRI was performed on a 1.5-T superconducting magnet. The imaging
protocol consisted of conventional spin-echo mixed intensity and
T2-weighted (repetition time [TR]/echo time [TE] 2300 to 2600/20 to
90 ms) or fast spin-echo T2-weighted (TR 29 900 ms, TE 120 ms) and
cerebrospinal fluid–suppressed T2-weighted (fluid-attenuated inversion
recovery; TE 130 ms, TR 6000 ms, and inversion time 1900 ms) scans, a
T1-weighted (TR/TE 600/15 ms) sequence, and a gradient-echo
T2*-weighted (TR/TE 600 to 800/16 to 20 ms, flip angle 20° to 25°)
imaging series. Slice thickness was uniformly 5 mm, and the
interslice gap was 10%. All scans were reviewed by an experienced
investigator who recorded the size and location of the clinically
symptomatic hematoma and the presence of additional
parenchymal abnormalities unaware of the patients’ clinical data.
Symptomatic hematomas were grouped as (1) lobar, involving
the cortex and/or deep white matter regions, (2) basal
ganglionic/thalamic, or (3) infratentorial, involving the brain stem
and/or the cerebellum. In accordance with previous studies, MBs were
defined on gradient-echo T2*-weighted images as homogeneous
rounded lesions with a diameter of 2 to 5 mm, and their location
and number in specific regions of the brain was recorded (Figures 1 and 2).2 4 Larger areas of
signal loss were considered to represent old hematomas.
Hyperintensities of the deep and subcortical white matter were
specified and graded into absent, punctate, early confluent, and
confluent. Periventricular hyperintensities were described
as caps or lining, bands, or irregular extending into the deep white
matter.10 Areas of ischemic parenchymal
destruction, ie, lesions exhibiting signal isointensity with
cerebrospinal fluid in their centers, were diagnosed as lacunes
(<10 mm in diameter) or infarcts.
|
|
A cohort of 280 asymptomatic elderly participants of the
Austrian Stroke Prevention Study (ASPS) who underwent the same imaging
protocol while our study group of pICH patients was being selected
served as a comparison. The rationale and design of the ASPS and the
MRI findings of this cohort have been published
previously.7 11 In short, MRI examinations with a
gradient-echo T2*-weighted sequence revealed that MBs may be found even
in neurologically normal elderly individuals. The clinical and imaging
data of the ASPS cohort that are relevant to the present study are
summarized in Table 1
.
Statistical analysis was performed with the Statistical Package
of Social Sciences (SPSS, Inc). We used the Pearson
2 test to compare the frequency distribution
of categorical variables between groups. Continuous variables
were compared with the Student t test. A logistic regression
analysis was used to define those demographic, clinical, and
morphological variables that independently contributed to a correct
classification of individuals as pICH patients or controls.
|
Results |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The clinically symptomatic hematoma was lobar in 43 (39%) patients, it was located in the basal ganglia/thalami in 50 (46%) patients, and it involved the brain stem/cerebellum in 14 (13%) patients. Two patients had >1 acute bleeding at different sites. MBs were seen in 59 (54%) of pICH patients, and their number ranged from 1 to 90 lesions (mean 14, median 6). Patients with MBs were significantly more often hypertensive and more frequently had a previous stroke history (Table 2
). Patients with MBs had
significantly higher grades of deep white matter and
periventricular hyperintensities, and they more commonly
showed lacunes and larger areas of hemosiderin
deposition from old hematomas (Table 3).
|
|
The majority of patients with MBs exhibited multiple lesions, which
were noted simultaneously in various parts of the brain
(Figures 1 and 2). MBs were observed in
cortical-subcortical regions in 43 patients, in the basal ganglia and
thalami in 41 patients, in the brain stem in 24 patients, in the
cerebellum in 23 patients, and in the deep white matter in 12 patients.
Figure 3 shows the regional distribution
of MBs according to the site of the acute hematoma. As can be seen,
there was some tendency toward a higher frequency of MBs in the basal
ganglia and infratentorial region in patients with basal
ganglionic/thalamic bleeds compared with those patients with a lobar
hematoma. However, these differences in the distribution of MBs reached
statistical significance only for cerebellar MBs, which were seen in 1
of 43 patients with a lobar bleed and in 17 of 33 patients with a
symptomatic hematoma in the basal ganglia or thalami
(P<0.001). In parallel, patients with basal
ganglionic/thalamic bleeds showed a significantly greater mean number
of MBs in the basal ganglia (3.1±5.9 versus 0.95±1.9,
P<0.02) and in the cerebellum (1.0±2.1 versus 0.02±0.15,
P<0.02) than did individuals with a lobar pICH (Figures 1 and 2). No significant differences between pICH
subgroups were noted in regard to the presence and number of MBs in
cortical-subcortical regions. We also did not find significant
differences in the distribution of MBs related to the presence or
absence of hypertension. Among the 15 patients with MBs and normal
blood pressure, 12 (80%) showed MBs in cortical-subcortical regions,
and 8 (53%) had MBs in the basal ganglia/thalami. MBs were seen in a
cortical-subcortical location in 31 (70%) of 44 patients with
hypertension and in the basal ganglia/thalami in 33 (75%) hypertensive
patients with MBs.
|
Comparison of the pICH study group with the cohort of neurologically
asymptomatic elderly individuals showed highly significant
differences in regard to almost all clinical and morphological
variables assessed (Table 1). Therefore, we used logistic
regression analysis to define those variables that would
best allow us to correctly separate pICH patients and control subjects.
Three variables emerged that independently contributed to such
classification. These variables were the presence of MBs, the grade
of periventricular hyperintensity, and the number of
lacunes (Table 4). No clinical or
demographic variable entered this model.
|
|
Discussion |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
We found evidence of old MBs in 54% of patients with pICH by using gradient-echo T2*-weighted MRI. This frequency corresponds closely to that of 57% recently reported by Tanaka et al5 in a smaller series of 30 patients. Earlier investigations that have reported a smaller rate of MBs in association with ICH have used conventional MRI sequences in all or most of their patients.2 12 Therefore, these lower numbers most likely resulted from the inferior sensitivity of conventional T2-weighted scans in the detection of small hemosiderin deposits. A much higher detection rate of MBs has recently been documented with the use of a gradient-echo technique compared with conventional T2 sequences in a direct comparison.5 Greenberg et al3 observed MBs in 80% of their patients, but this sample was small and was composed only of patients with lobar hemorrhage.
The overall number of MBs in individual patients in our series was
quite variable and ranged from 1 to 90 lesions. Most frequently,
MBs were seen in cortical-subcortical regions or in the basal ganglia
including the thalami. MBs in the brain stem and cerebellum were less
frequent, and the white matter was relatively spared. Typically
multiple MBs were found scattered throughout the brain. Therefore, a
separation of patient subgroups based on a specific location of MBs was
impossible, and a grading of regional preferences from the absolute
number of MBs appeared problematic because of differences
in the size of the regions to compare (eg, cortical-subcortical versus
brain stem). Therefore, we decided to compare the distribution of MBs
between patients on the basis of the site of the
symptomatic hematoma. This analysis revealed some
correspondence between pICH location and MB topography, as illustrated
in Figure 3; ie, frequency and number of MBs in the basal
ganglia/thalami and the infratentorial region were greater in patients
with a pICH at these sites than in patients with a lobar hematoma.
However, concerning cortical-subcortical MBs, no clear differences
emerged between pICH subgroups. Thus, we were unable to confirm a
specific pattern of MBs strongly suggestive of cerebral amyloid
angiopathy in this unselected series.3 In this context,
the probably rather small number of patients with cerebral amyloid
angiopathy in our sample has to be considered. Moreover,
histopathologic findings suggest a combination of cerebral amyloid
angiopathy with hypertensive microangiopathy as the cause of a more
widespread distribution of MBs in some patients.4
Interestingly, however, a preferential cortical-subcortical location of
MBs was not even found in the normotensive pICH patients of our study
population.
In line with previous studies,2 5 we found highly significant associations between the presence of MBs and other morphological signs of cerebral microangiopathy, such as lacunes and extensive periventricular and deep white matter damage,13 and we confirmed hypertension as the single most important clinical risk factor for the occurrence of MBs. A significantly higher frequency of a preceding stroke in patients with MBs can be viewed as further clinical evidence of a globally more pronounced vasculopathy of these patients. Comparison with a cohort of normal elderly control subjects showed the expected differences regarding a significantly higher rate of hypertension and also of diabetes mellitus in pICH patients. However, only MRI findings emerged as independent discriminating variables in a logistic regression model. These morphological variables were the presence of MBs and the grade of periventricular hyperintensity and the number of lacunes. CT studies have already associated lacunes and leukoaraiosis with a higher risk of intracerebral bleeding either spontaneously14 or after anticoagulant therapy.15 This analysis supports MBs as a further important marker of bleeding-prone small-vessel diseases. In this context, Greenberg et al16 have recently shown the accumulation of MBs over time on repeated MRI examination of a small group of patients with intracerebral bleeding. Large-scale prospective studies using gradient-echo T2*-weighted MRI in elderly individuals are now needed to substantiate these assumptions.
Received June 9, 2000; revision received July 3, 2000; accepted July 12, 2000.
|
References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Atlas SW, Mark AS, Grossmann RI, Gomori JM. Intracranial hemorrhage: gradient echo MR imaging at 1.5 T: comparison with spin-echo imaging and clinical implications. Radiology.. 1988;168:803–807.
2. Offenbacher H, Fazekas F, Schmidt R, Koch M, Fazekas G, Kapeller P. MR of cerebral abnormalities concomitant with primary intracerebral hematomas. AJNR Am J Neuroradiol.. 1996;17:573–578.[Abstract]
3.
Greenberg S, Finkelstein S, Schaefer P. Petechial
hemorrhages accompanying lobar hemorrhage: detection by
gradient echo MRI. Neurology.. 1996;46:1751–1754.
4.
Fazekas F, Kleinert R, Roob G, Kleinert G, Kapeller P,
Schmidt R, Hartung HP. Histopathologic analysis of foci of
signal loss in gradient-echo T2*-weighted MR images in patients with
spontaneous intracerebral hemorrhage: evidence
of microangiopathy-related microbleeds. AJNR Am J
Neuroradiol.. 1999;20:637–642.
5.
Tanaka A, Ueno Y, Nakayama Y, Takano K,
Takebayashi S. Small chronic hemorrhages and
ischemic lesions in association with spontaneous
intracerebral hematomas. Stroke.. 1999;30:1637–1642.
6. Kwa V, Franke CL, Verbeeten B Jr, Stam J. Silent intracerebral microhemorrhages in patients with ischemic stroke. Ann Neurol.. 1998;44:372–377.[Medline] [Order article via Infotrieve]
7.
Roob G, Schmidt R, Kapeller P, Lechner A, Hartung HP,
Fazekas F. MRI evidence of past cerebral microbleeds in a healthy
elderly population: the Austrian Stroke Prevention Study.
Neurology.. 1999;52:991–994.
8. Roob G, Fazekas F. Magnetic resonance imaging of cerebral microbleeds. Curr Opin Neurol.. 2000;13:69–73.[Medline] [Order article via Infotrieve]
9.
Greenberg S. Cerebral amyloid angiopathy:
prospects for clinical diagnosis and treatment. Neurology.. 1998;51:690–694.
10. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MRI signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJNR Am J Neuroradiol.. 1987;8:421–426.
11. Schmidt R, Lechner H, Fazekas F, Niederkorn K, Reinhart B, Grieshofer P, Horner S, Offenbacher H, Koch M, Eber B, Schumacher M, Kapeller P, Freidl W, Dusek T. Assessment of cerebrovascular risk profiles in healthy persons: definition of research goals and the Austrian Stroke Prevention Study. Neuroepidemiology.. 1994;13:308–313.[Medline] [Order article via Infotrieve]
12. Scharf J, Brauherr E, Forsting M, Sartor K. Significance of haemorrhagic lacunes on MRI in patients with hyperintense cerebrovascular diseases and intracerebral haemorrhage. Neuroradiology.. 1994;37:504–508.
13.
Fazekas F, Kleinert R, Offenbacher H, Schmidt R,
Kleinert G, Payer F, Radner H, Lechner H. Pathologic correlates of
incidental MRI white matter signal hyperintensities.
Neurology.. 1993;43:1683–1689.
14.
Inzitari D, Giordano GP, Ancona AL, Pracucci G,
Mascalchi M, Amaducci L. Leukoaraiosis,
intracerebral hemorrhage, and
arterial hypertension. Stroke.. 1990;21:1419–1423.
15. The Stroke Prevention in Reversible Ischemia Trial (SPIRIT) Study Group. A randomised trial of anticoagulants versus aspirin after cerebral ischemia of presumed arterial origin. Ann Neurol.. 1997;42:857–865.[Medline] [Order article via Infotrieve]
16. Greenberg SM, O’Donnell HC, Schaefer PW, Kraft E. MRI detection of new hemorrhages: potential marker of progression in cerebral amyloid angiopathy. Neurology.. 1999;22:1135–1138.
This article has been cited by other articles:
 |
|
 |
|
  S. M. Gregoire, U. J. Chaudhary, M. M. Brown, T. A. Yousry, C. Kallis, H. R. Jager, and D. J. Werring The Microbleed Anatomical Rating Scale (MARS): Reliability of a tool to map brain microbleeds Neurology, November 24, 2009; 73(21): 1759 - 1766. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. N. Orken, G. Kenangil, E. Uysal, and H. Forta Cerebral Microbleeds in Ischemic Stroke Patients on Warfarin Treatment Stroke, November 1, 2009; 40(11): 3638 - 3640. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. S. Staekenborg, E. L.G.E. Koedam, W. J.P. Henneman, P. Stokman, F. Barkhof, P. Scheltens, and W. M. van der Flier Progression of Mild Cognitive Impairment to Dementia: Contribution of Cerebrovascular Disease Compared With Medial Temporal Lobe Atrophy Stroke, April 1, 2009; 40(4): 1269 - 1274. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Yakushiji, M. Nishiyama, S. Yakushiji, T. Hirotsu, A. Uchino, J. Nakajima, M. Eriguchi, Y. Nanri, M. Hara, E. Horikawa, et al. Brain Microbleeds and Global Cognitive Function in Adults Without Neurological Disorder Stroke, December 1, 2008; 39(12): 3323 - 3328. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. H. Eckman, L. K.S. Wong, Y. O.Y. Soo, W. Lam, S. R. Yang, S. M. Greenberg, and J. Rosand Patient-Specific Decision-Making for Warfarin Therapy in Nonvalvular Atrial Fibrillation: How Will Screening With Genetics and Imaging Help? * Supplemental Appendix Stroke, December 1, 2008; 39(12): 3308 - 3315. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. R. Copenhaver, A. W. Hsia, J. G. Merino, R. E. Burgess, J. T. Fifi, L. Davis, S. Warach, and C. S. Kidwell Racial differences in microbleed prevalence in primary intracerebral hemorrhage Neurology, October 7, 2008; 71(15): 1176 - 1182. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Ueno, H. Naka, T. Ohshita, K. Kondo, E. Nomura, T. Ohtsuki, T. Kohriyama, S. Wakabayashi, and M. Matsumoto Association between Cerebral Microbleeds on T2*-Weighted MR Images and Recurrent Hemorrhagic Stroke in Patients Treated with Warfarin following Ischemic Stroke AJNR Am. J. Neuroradiol., September 1, 2008; 29(8): 1483 - 1486. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. W. Vernooij, A. van der Lugt, M. A. Ikram, P. A. Wielopolski, W. J. Niessen, A. Hofman, G. P. Krestin, and M.M.B. Breteler Prevalence and risk factors of cerebral microbleeds: The Rotterdam Scan Study Neurology, April 1, 2008; 70(14): 1208 - 1214. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Cordonnier, R. Al-Shahi Salman, and J. Wardlaw Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting Brain, August 1, 2007; 130(8): 1988 - 2003. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. I. Aguilar, R. G. Hart, C. S. Kase, W. D. Freeman, B. J. Hoeben, R. C. Garcia, J. E. Ansell, S. A. Mayer, B. Norrving, J. Rosand, et al. Treatment of Warfarin-Associated Intracerebral Hemorrhage: Literature Review and Expert Opinion Mayo Clin. Proc., January 1, 2007; 82(1): 82 - 92. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Cordonnier, W. M. van der Flier, J. D. Sluimer, D. Leys, F. Barkhof, and P. Scheltens Prevalence and severity of microbleeds in a memory clinic setting Neurology, May 9, 2006; 66(9): 1356 - 1360. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. S. Kim, D. H. Lee, C. W. Ryu, J. H. Lee, C. G. Choi, S. J. Kim, and D. C. Suh Multiple Cerebral Microbleeds in Hyperacute Ischemic Stroke: Impact on Prevalence and Severity of Early Hemorrhagic Transformation After Thrombolytic Treatment. Am. J. Roentgenol., May 1, 2006; 186(5): 1443 - 1449. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Naka, E. Nomura, T. Takahashi, S. Wakabayashi, Y. Mimori, H. Kajikawa, T. Kohriyama, and M. Matsumoto Combinations of the presence or absence of cerebral microbleeds and advanced white matter hyperintensity as predictors of subsequent stroke types. AJNR Am. J. Neuroradiol., April 1, 2006; 27(4): 830 - 835. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Viswanathan and H. Chabriat Cerebral Microhemorrhage Stroke, February 1, 2006; 37(2): 550 - 555. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H.-C. Koennecke Cerebral microbleeds on MRI: Prevalence, associations, and potential clinical implications Neurology, January 24, 2006; 66(2): 165 - 171. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Alemany, A. Stenborg, A. Terent, P. Sonninen, and R. Raininko Coexistence of Microhemorrhages and Acute Spontaneous Brain Hemorrhage: Correlation with Signs of Microangiopathy and Clinical Data Radiology, January 1, 2006; 238(1): 240 - 247. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Werring, L. J. Coward, N. A. Losseff, H. R. Jager, and M. M. Brown Cerebral microbleeds are common in ischemic stroke but rare in TIA Neurology, December 27, 2005; 65(12): 1914 - 1918. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Kim, H. J. Bae, J. Lee, L. Kang, S. Lee, S. Kim, J. E. Lee, K. M. Lee, B. W. Yoon, O. Kwon, et al. APOE {varepsilon}2/{varepsilon}4 polymorphism and cerebral microbleeds on gradient-echo MRI Neurology, November 8, 2005; 65(9): 1474 - 1475. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Werring, D. W. Frazer, L. J. Coward, N. A. Losseff, H. Watt, L. Cipolotti, M. M. Brown, and H. R. Jager Cognitive dysfunction in patients with cerebral microbleeds on T2*-weighted gradient-echo MRI Brain, October 1, 2004; 127(10): 2265 - 2275. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-H. Lee, S.-J. Kwon, K. S. Kim, B.-W. Yoon, and J.-K. Roh Topographical Distribution of Pontocerebellar Microbleeds AJNR Am. J. Neuroradiol., September 1, 2004; 25(8): 1337 - 1341. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Jeerakathil, P. A. Wolf, A. Beiser, J. K. Hald, R. Au, C. S. Kase, J. M. Massaro, and C. DeCarli Cerebral Microbleeds: Prevalence and Associations With Cardiovascular Risk Factors in the Framingham Study Stroke, August 1, 2004; 35(8): 1831 - 1835. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. -H. Lee, J. -M. Park, S. -J. Kwon, H. Kim, Y. H. Kim, J. K. Roh, and B. W. Yoon Left ventricular hypertrophy is associated with cerebral microbleeds in hypertensive patients Neurology, July 13, 2004; 63(1): 16 - 21. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S.-W. Jeong, K.-H. Jung, K. Chu, H.-J. Bae, S.-H. Lee, and J.-K. Roh Clinical and Radiologic Differences Between Primary Intracerebral Hemorrhage With and Without Microbleeds on Gradient-Echo Magnetic Resonance Images Arch Neurol, June 1, 2004; 61(6): 905 - 909. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Naka, E. Nomura, S. Wakabayashi, H. Kajikawa, T. Kohriyama, Y. Mimori, S. Nakamura, and M. Matsumoto Frequency of Asymptomatic Microbleeds on T2*-Weighted MR Images of Patients with Recurrent Stroke: Association with Combination of Stroke Subtypes and Leukoaraiosis AJNR Am. J. Neuroradiol., May 1, 2004; 25(5): 714 - 719. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S-H Lee, H-J Bae, S-B Ko, H Kim, B-W Yoon, and J-K Roh Comparative analysis of the spatial distribution and severity of cerebral microbleeds and old lacunes J. Neurol. Neurosurg. Psychiatry, March 1, 2004; 75(3): 423 - 427. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. van Gorp, Y. van der Graaf, B. A. J. M. de Mol, C. J. G. Bakker, T. D. Witkamp, L. M. P. Ramos, and W. P. T. M. Mali Bjork-Shiley Convexoconcave Valves: Susceptibility Artifacts at Brain MR Imaging and Mechanical Valve Fractures Radiology, March 1, 2004; 230(3): 709 - 714. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Lee, H. J. Bae, S. J. Kwon, H. Kim, Y. H. Kim, B. W. Yoon, and J. K. Roh Cerebral microbleeds are regionally associated with intracerebral hemorrhage Neurology, January 13, 2004; 62(1): 72 - 76. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. H. Fan, L. Zhang, W. W.M. Lam, V. C.T. Mok, and K. S. Wong Cerebral Microbleeds as a Risk Factor for Subsequent Intracerebral Hemorrhages Among Patients With Acute Ischemic Stroke Stroke, October 1, 2003; 34(10): 2459 - 2462. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. S. Packard, C. S. Kase, A. S. Aly, and G. D. Barest "Computed Tomography-Negative" Intracerebral Hemorrhage: Case Report and Implications for Management Arch Neurol, August 1, 2003; 60(8): 1156 - 1159. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Tsushima, J. Aoki, and K. Endo Brain Microhemorrhages Detected on T2*-Weighted Gradient-Echo MR Images AJNR Am. J. Neuroradiol., January 1, 2003; 24(1): 88 - 96. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. von Kummer MRI: The New Gold Standard for Detecting Brain Hemorrhage? Stroke, July 1, 2002; 33(7): 1748 - 1749. [Full Text] [PDF]
|
|
|
|
|
|
H. Kato, M. Izumiyama, K. Izumiyama, A. Takahashi, and Y. Itoyama Silent Cerebral Microbleeds on T2*-Weighted MRI: Correlation with Stroke Subtype, Stroke Recurrence, and Leukoaraiosis Stroke, June 1, 2002; 33(6): 1536 - 1540. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-H. Jeong, S. J. Yoon, S. J. Kang, K. G. Choi, and D. L. Na Hypertensive Pontine Microhemorrhage Stroke, April 1, 2002; 33(4): 925 - 929. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Nighoghossian, M. Hermier, P. Adeleine, K. Blanc-Lasserre, L. Derex, J. Honnorat, F. Philippeau, J.F. Dugor, J.C. Froment, and P. Trouillas Old Microbleeds Are a Potential Risk Factor for Cerebral Bleeding After Ischemic Stroke: A Gradient-Echo T2*-Weighted Brain MRI Study Stroke, March 1, 2002; 33(3): 735 - 742. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Dichgans, M. Holtmannspotter, J. Herzog, N. Peters, M. Bergmann, and T. A. Yousry Cerebral Microbleeds in CADASIL: A Gradient-Echo Magnetic Resonance Imaging and Autopsy Study Stroke, January 1, 2002; 33(1): 67 - 71. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. S. Kidwell, J. L. Saver, J. P. Villablanca, G. Duckwiler, A. Fredieu, K. Gough, M. C. Leary, S. Starkman, Y. P. Gobin, R. Jahan, et al. Magnetic Resonance Imaging Detection of Microbleeds Before Thrombolysis: An Emerging Application Stroke, January 1, 2002; 33(1): 95 - 98. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. A. J. Lesnik Oberstein, R. van den Boom, M. A. van Buchem, H. C. van Houwelingen, E. Bakker, E. Vollebregt, M. D. Ferrari, M. H. Breuning, and J. Haan Cerebral microbleeds in CADASIL Neurology, September 25, 2001; 57(6): 1066 - 1070. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||