Atormac
Neurology India
menu-bar5 Open access journal indexed with Index Medicus
  Users online: 1702  
 Home | Login 
About Editorial board Articlesmenu-bullet NSI Publicationsmenu-bullet Search Instructions Online Submission Subscribe Videos Etcetera Contact
  Navigate Here 
 Search
 
  
 Resource Links
  »  Similar in PUBMED
 »  Search Pubmed for
 »  Search in Google Scholar for
 »Related articles
  »  Article in PDF (666 KB)
  »  Citation Manager
  »  Access Statistics
  »  Reader Comments
  »  Email Alert *
  »  Add to My List *
* Registration required (free)  

 
  In this Article
 »  Abstract
 »  Materials and Me...
 » Results
 » Discussion
 »  References
 »  Article Tables

 Article Access Statistics
    Viewed724    
    Printed10    
    Emailed0    
    PDF Downloaded21    
    Comments [Add]    

Recommend this journal

 


 
Table of Contents    
ORIGINAL ARTICLE
Year : 2020  |  Volume : 68  |  Issue : 2  |  Page : 378-382

Cerebral Amyloid Angiopathy: A Clinico-Radiological Study from South India


1 Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India
2 Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India
3 Department of Biostatistics, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala, India

Date of Web Publication15-May-2020

Correspondence Address:
Dr. Sapna Erat Sreedharan
Department of Neurology, Sree Chitra Tirunal Institute for Medical Sciences and Technology, Trivandrum, Kerala - 695 011
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.280646

Rights and Permissions

 » Abstract 


Introduction: Cerebral amyloid angiopathy (CAA) is a major cause of intracerebral hemorrhage (ICH) and cognitive decline in the elderly. Since it is rarely reported from the developing world, we looked into the clinical profile and neuroimaging associations of CAA.
Materials and Methods: Ours was a retrospective case series of subjects diagnosed with probable/possible CAA between January 2006 and December 2015 as per Boston criteria. Clinical profile and neuroimaging were reviewed for markers of CAA. Details of any recurrent clinical events and functional status were collected from follow-up records.
Results: We had 28 subjects in the series with men outnumbering women, and the mean age was 70.17 ± 8.85 years (55–87 years). At the initial presentation, ICH was most frequent—10/28 (35.7%) patients, followed by transient neurological events (TNE = 25%) and cognitive disturbances (21.4%). Less than half of the patients received a diagnosis of CAA at the initial presentation itself. In total, 68% of our patients had cognitive dysfunction at admission. In our series, 12 had seizures and 9 had a history of TNE. The majority of our patients had vascular risk factors also. Leukoaraiosis showed an association with cognitive dysfunction (P = 0.044). Superficial siderosis and subarachnoid hemorrhage (SAH) showed a positive association with seizures and TNE, respectively. However, ICH showed no association with risk factors or imaging markers of CAA.
Conclusions: CAA patients, with a high prevalence of vascular risk factors mostly presented with ICH. The presence of SAH and superficial siderosis on MRI was associated with presentation as TNE and seizures, respectively.


Keywords: Cerebral amyloid angiopathy, cognitive involvement, intracerebral hemorrhage, MRI
Key Messages: Our study on Clinico-radiological features of Cerebral amyloid angiopathy shows majority presenting with Intracerebral hemorrhage as the initial event and high prevalence of vascular risk factors and unrecognized cognitive symptoms at presentation.


How to cite this article:
Sreedharan SE, Thomas B, Sylaja P N, Sarma SP. Cerebral Amyloid Angiopathy: A Clinico-Radiological Study from South India. Neurol India 2020;68:378-82

How to cite this URL:
Sreedharan SE, Thomas B, Sylaja P N, Sarma SP. Cerebral Amyloid Angiopathy: A Clinico-Radiological Study from South India. Neurol India [serial online] 2020 [cited 2020 Jun 1];68:378-82. Available from: http://www.neurologyindia.com/text.asp?2020/68/2/378/280646




Cerebral amyloid angiopathy (CAA), characterized by β-amyloid deposition in small and medium-sized arteries of the cerebral cortex and leptomeninges has been reported as a cause of intracerebral hemorrhage (ICH) for the last 40 years.[1] Despite being reported as a major cause of spontaneous ICH in the Western population,[2] it is often underreported from the Indian subcontinent, where spontaneous ICH accounts for over 11% of all strokes at the community level.[3]

With the widespread availability of magnetic resonance imaging (MRI) with gradient and susceptibility sequences, probable/possible CAA can be diagnosed without autopsy or surgical biopsy using Boston criteria.[4] Hence, more elderly are receiving a diagnosis of CAA in their lifetime. With the aging of the population and improved control of vascular risk factors, especially hypertension, physicians and neurologists from the developing countries such as India are increasingly likely to see this uncommon condition, which has important implications on planning risk factor management and antithrombotic use, especially dual antiplatelet and anticoagulation.

Hence, we decided to conduct this hospital-based study to understand the clinical and radiological profile of the patients with a diagnosis of probable/possible CAA and study their long-term outcome.


 » Materials and Methods Top


The study was conducted in …… Our study was a retrospective case series, where patients with a diagnosis of probable/possible CAA [4] were recruited after screening the medical records. The study recruitment period was 10 years (January 2006 to December 2015). The study was approved by the Institutional Ethics Committee. Demographic and clinical details were extracted using a structured proforma. We collected details on symptomatology, mean delay in diagnosis, vascular risk factors and prior antiplatelet and statin usage from medical records. Cognitive involvement was assessed using the mini-mental status exam (MMSE) and detailed neuropsychological battery for lobar functions wherever possible. MMSE <22/30 for those with <9 years of education and <26/30 for those with ≥9 years of formal education were taken as cutoffs for cognitive involvement, as per normative data published from our part of India previously.[5] In cases where the formal cognitive assessment was not possible, we looked for any preceding self or spouse-reported cognitive symptoms. All the patients had undergone computerized axial tomography (CT)/MRI, which was reviewed from the patient archival and communication system (PACS) by a study neurologist (S.E.S.) and neuroradiologist (B.T.). All the subjects who had undergone MRI had T1, T2, FLAIR, GRE, susceptibility-weighted imaging, and diffusion-weighted imaging sequences along with vessel imaging—in the form of TOF–MR (time-of-flight–magnetic resonance) angiography of intra- and extracranial vessels. We looked for the presence of macro/microbleeds,[6] their number and distribution, presence or absence of cortical subarachnoid hemorrhage (cSAH) and cortical superficial siderosis (cSS),[7] defined as per standard definitions. We did not include cSS if it was contiguous with any ICH. The distribution of cSS and acute cSAH was classified as focal (restricted to ≤3 sulci) or disseminated (≥4 sulci).[7] Also, we looked for the presence of brain atrophy, acute and chronic infarcts, and white matter changes, which was graded as per Fazekas grading. Follow-up of all patients was obtained from medical records or telephonic interview. In the follow-up, we looked for cognitive progression and any acute neurological events—strokes-hemorrhagic or ischemic/seizures or transient neurological events (TNE).

Statistical analysis

SPSS software, version 16 (SPSS Inc, Chicago, IL, USA) was used for statistical analysis. Baseline data were expressed in means and percentages. Fischer's exact test and Chi-square test were used to test the strength of association between variables. We looked for the association between each presenting symptom with vascular risk factors, age, gender, and imaging markers such as CMBs, white matter changes, cSAH, and cSS.


 » Results Top


We had 28 subjects satisfying Boston criteria for probable/possible CAA during the study period who were included in the final analysis. The mean age of our cohort was 70.17 ± 8.85 years (range 55–87 years) with men outnumbering women (M: F ratio was 24:4). The majority of our patients were admitted with ICH (13/28, 46.4%). The diagnosis at admission is shown in [Table 1].
Table 1: Clinical presentation of CAA

Click here to view


We found that many subjects had been symptomatic for long (mean 32 ± 29.3 months), ranging between 1 and 84 months from the first symptom till the diagnosis was made. Cognitive symptoms were the first symptom in a significant percentage of subjects, even though presentation as frank dementia was less common. Less than half of the patients (12/28, 42.9%) received a diagnosis of CAA at first presentation itself, despite having MRI done. Our subjects had a high prevalence of vascular risk factors also, which is shown in [Table 2].
Table 2: Risk factor profile of the patients with CAA

Click here to view


Our 26 subjects had MRI (1.5 T Siemens Inc.) and two had only CT head for review. Imaging findings are summarized in [Table 3] and distribution of microbleeds is given in [Table 4].
Table 3: Neuroimaging characteristics

Click here to view
Table 4: Location and distribution of cerebral microbleeds

Click here to view


In total, 50% of our patients were discharged with moderate to severe disability (modified Rankin scale 3 or above). We had at least a 12-month follow-up of 22 subjects and the mean follow-up duration was 33 ± 29 months, range 1–96 months. Recurrent neurological events were seen in eight of the subjects, with three having seizures, two each having TNE and ICH and one subject having an ischemic stroke. However, one-third of the patients (9/28) had cognitive progression during the follow-up.

Univariate analysis to test associations showed that those presenting as intracerebral bleed has no association with age, gender, presence of hypertension, prior antiplatelet or statin use, or neuroimaging characteristics such as the presence of CMB, cortical SAH, or leukoaraiosis. Those with cognitive symptoms as presentation also had no positive association with clinical parameters. However, we could find a weak correlation with severe leukoaraiosis (Fazekas grade 2 and 3; P = 0.04). The presence of infarcts or bleeds, macro- or microbleeds or SAH failed to show an association with the cognitive presentation. Those who had cognitive progression on follow-up did not show any statistically significant association with any of the clinical or imaging parameters. Seizures during the clinical course had a significant association with the presence of CS (P = 0.01); however, they failed to show an association with clinical variables or the presence of macro/microbleeds. Also, those with TNE during illness had a significant association with cSAH (P = 0.003).


 » Discussion Top


With aging of the population and better primary and secondary prevention programs for lifestyle diseases, developing countries such as India are more likely to see neurodegenerative diseases and its myriad presentations in the coming years. There is a paucity of literature on CAA from the Indian subcontinent, with seven reports of nine patients so far.[8],[9],[10],[11],[12],[13],[14] CAA, an important cause of nontraumatic ICH and cognitive decline in the elderly in the West is probably under recognized by physicians and neurologists, which prompted us to conduct this study.

Ours were a predominantly male cohort in the seventh decade of life. Aging is considered as the strongest risk factor for developing CAA with pathological studies indicating an increase in an amyloid deposition from seventh to ninth decade of life. We could not find any specific gender predilection for CAA in existing literature, even though most of the reports from India were of male patients.

Even though ICH was the main event that made our patients present to the hospital, the majority were having prior cognitive symptoms. TNE was seen in the one-third of patients. Of the nine reported patients from India, ICH was seen in the majority (7/9), and three had dementia.[8],[9],[10],[11],[12],[13],[14] Surprisingly, none had seizures or ischemic symptoms at presentation. Asian literature on CAA indicates a lower incidence of spontaneous ICH related to CAA, which was explained by a higher incidence of hypertensive ICH in the Oriental population. Also, more cognitive involvement was found in the elderly secondary to CAA, especially in those with AD pathology.[15] In comparison, Western data show that CAA is a major cause of spontaneous ICH in elderly, accounting for 5%–20% of all ICHs.[16] Studies have also shown that the presence of CAA pathology increases the odds for developing dementia nine-fold, after adjusting for age and Alzheimer's pathology, and cognitive involvement has been reported to have association with CMB, micoinfarcts, and white mater changes as well.[17] Rapidly progressive dementia secondary to CAA-related inflammation has been rarely reported, with only one biopsy-proven case so far from our part of the country.[8]

After ICH, the most common acute clinical presentation described in CAA is TNE, also known as an amyloid spell.[18] Marching type of sensory phenomenon is described, often difficult to distinguish from a sensory seizure, which was seen in most of our patients. Also, therapeutic response to antiepileptics in many of these patients suggests common pathogenesis for TNE and epilepsy in CAA patients. Even though CAA is reported as a cause for the late-onset seizure, the strength of the association is still not clear.

We failed to find any association of risk factors with ICH or cognitive decline in our cohort. Even though CAA risk may not be increased by conventional vascular risk factors,[19] hypertension may contribute to CAA-related ICH in the Western population.[20] However, Asian reports have been contradictory with authors from Japan and China reporting a lower prevalence of hypertension in CAA-related ICH (41%–45%) as compared with all causes for ICH (75%–80%).[21],[22] Even though the prevalence of hypertension in our cohort was comparable to those with spontaneous ICH unrelated to CAA, it is difficult to explain the lack of positive association, which may have been confounded by the smaller sample size of those without hypertension. Statin use, which has been shown to increase the risk of spontaneous ICH,[23] has till now not shown any consistent association with CAA-related ICH or presence of CMBs. Unlike statins, prior antiplatelet use has shown an association with CAA-related ICH and the presence of CMBs on imaging.[24] However, we could not find a significant statistical association here also.

CAA-related macrobleeds, regardless of their size, exhibit a few common characteristics—distinctive cortico–subcortical distribution, multiplicity, and generally spares deep white mater (WM), basal ganglia, and brainstem, correlating well with the anatomic distribution of β-amyloid containing vessels.[25] Less commonly cerebellum can be involved. We also found a similar pattern, with the majority having multiple macrobleeds and some with intraventricular extension. Presence of macrobleeds in the deep WM, basal ganglia, infratentorial–brainstem location, classical for hypertensive ICH has been reported by many authors in CAA also. Association of lobar ICH with CAA has been consistently reported in the literature, unlike other locations, which failed to show a positive correlation. In our study, we had a very high prevalence of hypertension in our cohort, comparable to those with hypertensive ICH, which might have been the reason why we failed to find an association with CAA. We hypothesize that many of our subjects might have had dual pathology, which needs further biopsy studies from our part of the world for confirmation.

Regarding associations of CMB, most studied ones are ICH and dementia. In a recent study on long-term follow-up of the CAA patients with CMBs alone without macrobleeds, authors found a small but substantial risk for ICH in their follow-up.[26] Some have found CMBs increasing the risk of recurrent ICH in those with lobar ICH.[27] We could not look into the association of CMB-only subjects with future ICH risk due to very small sample numbers in that subgroup. Those with CMBs have been reported to have worse performance in vascular dementia/cognitive decline.[28] However, our analysis failed to find an association between lobar ICH and cognitive presentation/progression and CMBs, which might have been due to the high prevalence of hypertension and preexisting WM changes that can independently influence cognition and ICH risk.

Silent infarctions are well reported in the brains of patients with advanced CAA. Studies using MR-diffusion sequences have shown a high prevalence of silent infarcts in CAA, often associated with high CMB burden, recent ICH, and severe WM changes, suggesting a dynamic interplay of hemorrhagic and ischemic components of CAA.[29] Even though presentation as the ischemic stroke was less common in our cohort also, we found that half of the patients had evidence of silent ischemia on imaging. The subcortical location of infarction in the majority may suggest an added role of hypertension in its pathogenesis.

The majority of our patients had moderate to severe leukoaraiosis, even though we could not find a posterior predilection, as reported by a few authors.[30] We found a significant association for WM changes with cognitive impairment, which has been reported previously also.[31] However, we failed to find an association with hypertension or lobar ICH as the majority had long-standing vascular risk factors.

Cortical SAH and cSS are well-described imaging findings in sporadic CAA.[4] The largest cohort of isolated cSAH found that CAA was the most common etiology in patients over 60 years of age.[32] cSS in our cohort had a strong association with TNE, which has been reported in several large series as well.[33] Seizures are infrequently reported in CAA, often associated with CAA-related inflammation. Our finding of a strong association of seizures with cortical SAH has never been reported previously. Pathogenesis of TNE remains unclear and plausible explanations include focal seizure-like activity or migraine aura-like spreading depression. Common pathogenesis for TNE and seizure may be a logical explanation for our finding. Also, there are reports of patients with TNE responding to antiepileptics, which indirectly supports our hypothesis.[34]

Our study is not without its limitations. Only two patients underwent emergency hematoma evacuation and we did not have histopathology confirmation in any of our patients. However, we made the diagnosis of probable/possible CAA as per Boston criteria, which is well validated in literature. We could get follow-up of 22 subjects only. Also, cognitive involvement must have been underreported in our study due to the retrospective nature of data collection. Also, the number of subjects with isolated CMBs or cSAH/cSS without lobar bleeds was less, to see the effect of these surrogate markers on symptom presentation, progression, and recurrent events.

Despite these limitations, we believe our study brings to light several less known clinical and imaging findings in CAA, which has been infrequently been reported from Asia, especially the Indian subcontinent. Seizures, even though rarely reported in CAA may be more common than previously thought of and need to be recognized early as various treatment options are available. cSAH patients showed a strong correlation with seizures, whereas a significant percentage of those with TNE had cSS on imaging. Leukoaraiosis of the severe grade was consistently found in patients with cognitive involvement at presentation, which was independent of age and hypertension.

Financial support and sponsorship

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Conflicts of interest

The authors have no conflicts of interest.



 
 » References Top

1.
Jellinger K. Cerebral hemorrhage in amyloid angiopathy. Ann Neurol 1977;1:604.  Back to cited text no. 1
    
2.
Lovelock CE, Molyneux AJ, Rothwell PM. Oxford vascular study change in incidence and aetiology of intracerebral haemorrhage in Oxfordshire, UK, between 1981 and 2006: A population-based study. Lancet Neurol 2007;6:487-93.  Back to cited text no. 2
    
3.
Sridharan SE, Unnikrishnan JP, Sukumaran S, Sylaja PN, Nayak SD, Sarma PS, et al. Incidence, types, risk factors, and outcome of stroke in a developing country: The Trivandrum Stroke Registry. Stroke 2009;40:1212-8.  Back to cited text no. 3
    
4.
Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of cerebral amyloid angiopathy: Validation of the Boston criteria. Neurology 2001;56:537-9.  Back to cited text no. 4
    
5.
Mathuranath PS, Cherian JP, Mathew R, George A, Alexander A, Sarma SP. Mini mental state examination and the Addenbrooke's cognitive examination: Effect of education and norms for a multicultural population. Neurol India 2007;55:106-10.  Back to cited text no. 5
[PUBMED]  [Full text]  
6.
Greenberg SM, Vernooij MW, Cordonnier C, Viswanathan A, Al-Shahi Salman R, Warach S, et al. Cerebral microbleeds: A guide to detection and interpretation. Lancet Neurol 2009;8:165-74.  Back to cited text no. 6
    
7.
Linn J, Halpin A, Demaerel P, Ruhland J, Giese AD, Dichgans M, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 2010;74:1346-50.  Back to cited text no. 7
    
8.
Maramattom BV, Maramattom LV. Cerebral amyloid angiopathy presenting as a posterior leukoencephalopathy: A case report and review of the literature. Neurol India 2004;57:487-8.  Back to cited text no. 8
    
9.
Jalesh N, Panicker D, Nagaraja YT. Cerebral amyloid angiopathy: A clinicopathological study of three cases. Ann Indian Acad Neurol 2010;13:216-20.  Back to cited text no. 9
    
10.
Wani NA, Kosar TL, Rawa AA, Qayum AK. Superficial siderosis in cerebral amyloid angiopathy. Ann Indian Acad Neurol 2011;14:60-1.  Back to cited text no. 10
[PUBMED]  [Full text]  
11.
Bano S, Yadav SN, Garga UC, Chaudhary V. Sporadic cerebral amyloid angiopathy: An important cause of cerebral hemorrhage in the elderly. Neurosci Rural Pract 2011;2:87-91.  Back to cited text no. 11
    
12.
Jha S, Jose MJ. Non-hypertensive intracerebral haemorrhage: Some interesting observations. Assoc Physicians India 2006;54:485-7.  Back to cited text no. 12
    
13.
Alexander M, Patil AB, Mathew V, Sivadasan A, Chacko G, Mani SE. Recurrent craniospinal subarachnoid hemorrhage in cerebral amyloid angiopathy. Ann Indian Acad Neurol 2013;16:97-9.  Back to cited text no. 13
[PUBMED]  [Full text]  
14.
Sharma N, Vyas S. Cerebral amyloid angiopathy. BMJ Case Rep 2014. doi: 10.1136/bcr-2013-201558.  Back to cited text no. 14
    
15.
Keage HA, Carare RO, Friedland RP, Ince PG, Love S, Nicoll JA, et al. Population studies of sporadic cerebral amyloid angiopathy and dementia: A systematic review. BMC Neurol 2009;9:3.  Back to cited text no. 15
    
16.
Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: Recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry 2012;83:124-37.  Back to cited text no. 16
    
17.
Werring DJ, Gregoire SM, Cipolotti L. Cerebral microbleeds and vascular cognitive impairment. J Neurol Sci 2010;299:131-5.  Back to cited text no. 17
    
18.
Greenberg SM, Vonsattel JP, Stakes JW, Gruber M, Finklestein SP. The clinical spectrum of cerebral amyloid angiopathy: Presentations without lobar hemorrhage. Neurology 1993;43:2073-9.  Back to cited text no. 18
    
19.
Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke 1987;18:311-24.  Back to cited text no. 19
    
20.
Vonsattel JP, Myers RH, Hedley-Whyte ET, Ropper AH, Bird ED, Richardson EP Jr. Cerebral amyloid angiopathy without and with cerebral hemorrhages: A comparative histological study. Ann Neurol 1991;30:637-49.  Back to cited text no. 20
    
21.
Hosomi N, Naya T, Ohkita H, Mukai M, Nakamura T, Ueno M, et al. Predictors of intracerebral hemorrhage severity and its outcome in Japanese stroke patients. Cerebrovasc Dis 2009;27:67-74.  Back to cited text no. 21
    
22.
Yang QD, Niu Q, Zhou YH, Liu YH, Xu HW, Gu WP, et al. Incidence of cerebral hemorrhage in the Changsha community. A prospective study from 1986 to 2000. Cerebrovasc Dis 2004;17:303-13.  Back to cited text no. 22
    
23.
Goldstein LB, Amarenco P, Szarek M, Callahan A 3rd, Hennerici M, Sillesen H, et al. Hemorrhagic stroke in the stroke prevention by aggressive reduction in cholesterol levels study. Neurology 2008;70:2364-70.  Back to cited text no. 23
    
24.
Biffi A, Halpin A, Towfighi A, Gilson A, Busl K, Rost N, et al. Aspirin and recurrent intracerebral hemorrhage in cerebral amyloid angiopathy. Neurology 2010;75:693-8.  Back to cited text no. 24
    
25.
Wagle WA, Smith TW, Weiner M. Intracerebral hemorrhage caused by cerebral amyloid angiopathy: Radiographic-pathologic correlation. AJNR Am J Neuroradiol 1984;5:171-6.  Back to cited text no. 25
    
26.
van Etten ES, Auriel E, Haley KE, Ayres AM, Vashkevich A, Schwab KM, et al. Incidence of symptomatic hemorrhage in patients with lobar microbleeds. Stroke 2014;45:2280-5.  Back to cited text no. 26
    
27.
Greenberg SM, Eng JA, Ning M, Smith EE, Rosand J. Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke 2004;35:1415-20.  Back to cited text no. 27
    
28.
Uiterwijk R, Huijts M, Staals J, Duits A, Gronenschild E, Kroon AA, et al. Subjective cognitive failures in patients with hypertension are related to cognitive performance and cerebral microbleeds. Hypertension 2014;64:653-7.  Back to cited text no. 28
    
29.
Kidwell CS, Greenberg SM. Red meets white: Do microbleeds link hemorrhagic and ischemic cerebrovascular disease? Neurology 2009;73:1614-5.  Back to cited text no. 29
    
30.
Smith EE. Leukoaraiosis and stroke. Stroke 2010;41:S139-43.  Back to cited text no. 30
    
31.
Smith EE, Gurol ME, Eng JA, Engel CR, Nguyen TN, Rosand J, et al. White matter lesions, cognition, and recurrent hemorrhage in lobar intracerebral hemorrhage. Neurology 2004;63:1606-12.  Back to cited text no. 31
    
32.
Kumar S, Goddeau RP Jr, Selim MH, Thomas A, Schlaug G, Alhazzani A, et al. Atraumatic convexal subarachnoid hemorrhage: Clinical presentation, imaging patterns, and etiologies. Neurology 2010;74:893-9.  Back to cited text no. 32
    
33.
Charidimou A, Peeters A, Fox Z, Gregoire SM, Vandermeeren Y, Laloux P, et al. Spectrum of transient focal neurological episodes in cerebral amyloid angiopathy: Multicentre magnetic resonance imaging cohort study and meta-analysis. Stroke 2012;43:2324-30.  Back to cited text no. 33
    
34.
Roch JA, Nighoghossian N, Hermier M, Cakmak S, Picot M, Honnorat J, et al. Transient neurologic symptoms related to cerebral amyloid angiopathy: Usefulness of T2*-weighted imaging. Cerebrovasc Dis 2005;20:412-4.  Back to cited text no. 34
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

Top
Print this article  Email this article
   
Online since 20th March '04
Published by Wolters Kluwer - Medknow