Association between large artery atherosclerosis and cerebral microbleeds: a systematic review and meta-analysis

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Abstract

Objective

The aim of this systematic review and meta-analysis was to provide evidence that biomarkers of large artery atherosclerosis, including arterial stenosis and greater carotid intima-media thickness (cIMT), may serve as clinical markers of subclinical haemorrhage-prone cerebral small vessel disease, reflected by cerebral microbleeds (CMBs).

Methods

We searched PubMed, MEDLINE, Web of Science, EMBASE and the Cochrane Library to identify relevant studies published before 1 July 2016. The association between arterial stenosis and CMBs was estimated by the OR and 95% CI. The association of cIMT and CMBs was calculated using the standardised mean difference (SMD). Heterogeneity and publication bias were explored.

Results

8 studies including a total of 7160 participants were pooled in the meta-analysis. 6 of the included studies were cross-sectional, except that 2 were prospective. We found a significant association between arterial stenosis >50% and the presence of CMBs (OR 1.95, 95% CI 1.13 to 3.36, I ²=56.1%). A fixed-effects model suggested that patients with CMBs were more likely to have a greater cIMT (SMD 0.20, 95% CI 0.11 to 0.28, I ²=24.7%).

Conclusions

This systematic review and meta-analysis found that there is a relationship between large artery atherosclerosis and CMBs. Future studies are needed to confirm the impact of atherosclerosis on the CMBs, which may have potential therapeutic implications.

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Most cited references 35

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Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases.

Eszter Farkas, Paul G. M. Luiten, Ferenc Bari (2007)

Chronic cerebral hypoperfusion has been associated with cognitive decline in aging and Alzheimer's disease. Moreover, the pattern of cerebral blood flow in mild cognitive impairment has emerged as a predictive marker for the progression into Alzheimer's disease. The reconstruction of a pathological condition in animal models is a suitable approach to the unraveling of causal relationships. For this reason, permanent, bilateral occlusion of the common carotid arteries (2VO) in rats has been established as a procedure to investigate the effects of chronic cerebral hypoperfusion on cognitive dysfunction and neurodegenerative processes. Over the years, the 2VO model has generated a large amount of data, revealing the 2VO-related pattern of cerebral hypoperfusion and metabolic changes, learning and memory disturbances, failure of neuronal signaling, and the neuropathological changes in the hippocampus. In addition, the model has been introduced in research into ischemic white matter injury and ischemic eye disease. The present survey sets out to provide a comprehensive summary of the achievements made with the 2VO model, and a critical evaluation and integration of the various results, and to relate the experimental data to human diseases. The data that have accumulated from use of the 2VO model in the rat permit an understanding of the causative role played by cerebral hypoperfusion in neurodegenerative diseases. Thorough characterization of the model suggests that 2VO in the rat is suitable for the development of potentially neuroprotective strategies in neurodegenerative diseases.

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Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam scan study.

Meike Vernooij, Albert Hofman, Ella Poels … (2010)

We previously reported on the high prevalence of cerebral microbleeds (CMBs) in community-dwelling people aged 60 years and older. Moreover, we found that their spatial distribution likely reflects differences in underlying etiology. We have since almost quadrupled the number of participants in our study and expanded it to include persons of 45 years and older. We examined the prevalence and determinants of microbleeds in this larger and younger cohort from the general population. In 3979 persons (mean age, 60.3 years), we performed brain MRI at 1.5T, including a sequence optimized for visualization of CMBs. Associations between APOE genotype, cardiovascular risk factors, and markers of cerebrovascular disease with the presence and location of CMBs were assessed by multiple logistic regression adjusted for age, sex, and relevant confounders. Microbleed prevalence gradually increased with age, from 6.5% in persons aged 45 to 50 years to 35.7% in participants of 80 years and older. Overall, 15.3% of all subjects had at least 1 CMB. Cardiovascular risk factors and presence of lacunar infarcts and white matter lesions were associated with microbleeds in a deep or infratentorial region, whereas APOE ε4 and diastolic blood pressure were related to microbleeds in a strictly lobar location. Findings in this larger population are in line with our previous results and, more importantly, extend these to a younger age group. CMBs are already present at middle age, and prevalence rises strongly with increasing age. We confirmed that determinants of the presence of cerebral microbleeds differ according to their location in the brain.

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Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds.

G Roob, H Hartung, R Kleinert … (1999)

Patients with spontaneous intracerebral hemorrhage (ICH) frequently have small areas of signal loss on gradient-echo T2*-weighted MR images, which have been suggested to represent remnants of previous microbleeds. Our aim was to provide histopathologic support for this assumption and to clarify whether the presence and location of microbleeds were associated with microangiopathy. We performed MR imaging and correlative histopathologic examination in 11 formalin-fixed brains of patients who had died of an ICH (age range, 45-90 years). Focal areas of signal loss on MR images were noted in seven brains. They were seen in a corticosubcortical location in six brains, in the basal ganglia/thalami in five, and infratentorially in three specimens. Histopathologic examination showed focal hemosiderin deposition in 21 of 34 areas of MR signal loss. No other corresponding abnormalities were found; however, hemosiderin deposits were noted without MR signal changes in two brains. All specimens with MR foci of signal loss showed moderate to severe fibrohyalinosis, and there was additional evidence of amyloid angiopathy in two of those brains. Small areas of signal loss on gradient echo T2*-weighted images indicate previous extravasation of blood and are related to bleeding-prone microangiopathy of different origins.

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Author and article information

Journal

Journal ID (nlm-ta): Stroke Vasc Neurol

Journal ID (iso-abbrev): Stroke Vasc Neurol

Journal ID (hwp): svnbmj

Journal ID (publisher-id): svn

Title: Stroke and Vascular Neurology

Publisher: BMJ Publishing Group (BMA House, Tavistock Square, London, WC1H 9JR )

ISSN (Electronic): 2059-8696

Publication date Collection: March 2017

Publication date (Electronic): 24 February 2017

Volume: 2

Issue: 1

Pages: 7-14

Affiliations

Department of Neurology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College (CAMS & PUMC) , Beijing, China

Author notes

[Correspondence to ] Dr Bin Peng; pengbin3@ 123456hotmail.com

Article

Publisher ID: svn-2016-000049

DOI: 10.1136/svn-2016-000049

PMC ID: 5435213

SO-VID: a24868a8-bfd5-40c3-b8a0-7db75f13ba6d

Copyright © Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://www.bmj.com/company/products-services/rights-and-licensing/

License:

This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/

History

Date received : 15 October 2016

Date revision received : 26 December 2016

Date accepted : 18 January 2017

Funding

Funded by: Natural Science Foundation of Beijing Municipality, http://dx.doi.org/10.13039/501100004826;

Award ID: 7152121

Funded by: National Natural Science Foundation of China, http://dx.doi.org/10.13039/501100001809;

Association between large artery atherosclerosis and cerebral microbleeds: a systematic review and meta-analysis

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Most cited references 35

Permanent, bilateral common carotid artery occlusion in the rat: a model for chronic cerebral hypoperfusion-related neurodegenerative diseases.

Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam scan study.

Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds.

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