Elsevier

The Lancet Neurology

Volume 8, Issue 2, February 2009, Pages 165-174
The Lancet Neurology

Review
Cerebral microbleeds: a guide to detection and interpretation

https://doi.org/10.1016/S1474-4422(09)70013-4Get rights and content

Summary

Cerebral microbleeds (CMBs) are increasingly recognised neuroimaging findings in individuals with cerebrovascular disease and dementia, and in normal ageing. There has been substantial progress in the understanding of CMBs in recent years, particularly in the development of newer MRI methods for the detection of CMBs and the application of these techniques to population-based samples of elderly people. In this Review, we focus on these recent developments and their effects on two main questions: how CMBs are detected, and how CMBs should be interpreted. The number of CMBs detected depends on MRI characteristics, such as pulse sequence, sequence parameters, spatial resolution, magnetic field strength, and image post-processing, emphasising the importance of taking into account MRI technique in the interpretation of study results. Recent investigations with sensitive MRI techniques have indicated a high prevalence of CMBs in community-dwelling elderly people. We propose a procedural guide for identification of CMBs and suggest possible future approaches for elucidating the role of these common lesions as markers for, and contributors to, small-vessel brain disease.

Introduction

Small foci of chronic blood products in normal (or near normal) brain tissue, known as cerebral microbleeds (CMBs), have become increasingly recognised with the widespread use of MRI techniques that are sensitive to iron deposits.1, 2 Advances in software and hardware have led to substantial increases in the sensitivity of MRI to CMBs and improvements in the criteria for their identification. Another area of recent progress has been the use of sensitive MRI in community-dwelling elderly people, in whom the prevalence of CMBs detected is as high as 11·1–23·5%.3, 4 Data from population-based MRI analyses also suggest connections between normal ageing and asymptomatic stages of age-associated small-vessel diseases, such as hypertensive vasculopathy and cerebral amyloid angiopathy. Despite several comprehensive reviews of CMBs,5, 6, 7, 8, 9 recent advances warrant a new assessment of emerging technical features of image acquisition, specific criteria for lesion identification, and recent data from population-based studies.

Section snippets

Detection of CMBs

CMBs are primarily a radiological construct (ie, small MRI signal voids), but one that is indicative of specific underlying microscopic pathological changes (ie, perivascular collections of haemosiderin deposits that are foci of past haemorrhages). Here, we review advances in MRI for the detection of CMBs, the criteria used to include or exclude MRI lesions as genuine CMBs, and what is known of the correlation between MRI and underlying histopathology. A glossary of commonly used MRI terms is

Vascular pathological changes

One approach to the interpretation of CMBs is to regard them as a marker of accompanying vascular pathological change. Histopathological analyses of the vessels associated with CMBs, done primarily in brains with haemorrhagic stroke, have generally identified two types of vascular pathological changes: hypertensive vasculopathy and cerebral amyloid angiopathy.10, 35, 37 For example, among the 11 brains examined by Fazekas and co-workers,10 advanced hypertensive lipohyalinotic changes were seen

Recommendations and future directions

CMBs are a well defined pathological lesion that can be detected by use of T2*-weighted MRI techniques with high sensitivity (particularly by use of new methods), high reliability (with careful image interpretation and consideration of CMB mimics), and high specificity (proven for conventional T2*-weighted MRI, still to be established for the newer methods). The full brain coverage by MRI probably renders neuroimaging a more sensitive method for CMB detection than are histopathological

Search strategy and selection criteria

The content of this Review is based on the group consensus from a conference entitled “Cerebral Microbleeds: Detection and Definition”. Additional references for this Review were identified through searches of PubMed with the search terms “microbleed(s)”, “microh(a)emorrhage(s)”, or “petechial h(a)emorrhage(s)”; or “gradient-echo”, “T2*”, or “susceptibility” in conjunction with “h(a)emorrhage(s)”, from January, 1966 to October, 2008. References were also identified from the bibliography

References (71)

  • C Stehling et al.

    Detection of asymptomatic cerebral microbleeds a comparative study at 1.5 and 3.0 T

    Acad Radiol

    (2008)
  • M Akter et al.

    Detection of hemorrhagic hypointense foci in the brain on susceptibility-weighted imaging clinical and phantom studies

    Acad Radiol

    (2007)
  • H Offenbacher et al.

    MR of cerebral abnormalities concomitant with primary intracerebral hematomas

    AJNR Am J Neuroradiol

    (1996)
  • G Roob et al.

    MRI evidence of past cerebral microbleeds in a healthy elderly population

    Neurology

    (1999)
  • S Sveinbjornsdottir et al.

    Cerebral microbleeds in the population based AGES Reykjavik study: prevalence and location

    J Neurol Neurosurg Psychiatry

    (2008)
  • MW Vernooij et al.

    Prevalence and risk factors of cerebral microbleeds: the Rotterdam Scan Study

    Neurology

    (2008)
  • HC Koennecke

    Cerebral microbleeds on MRI: prevalence, associations, and potential clinical implications

    Neurology

    (2006)
  • A Viswanathan et al.

    Cerebral microhemorrhage

    Stroke

    (2006)
  • C Cordonnier et al.

    Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting

    Brain

    (2007)
  • J Fiehler

    Cerebral microbleeds: old leaks and new haemorrhages

    Int J Stroke

    (2006)
  • DJ Werring

    Cerebral microbleeds: clinical and pathophysiological significance

    J Neuroimaging

    (2007)
  • F Fazekas et al.

    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

    AJNR Am J Neuroradiol

    (1999)
  • Y Tsushima et al.

    MR detection of microhemorrhages in neurologically healthy adults

    Neuroradiology

    (2002)
  • Y Horita et al.

    Analysis of dot-like hemosiderin spots using brain dock system

    No Shinkei Geka

    (2003)
  • T Jeerakathil et al.

    Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham Study

    Stroke

    (2004)
  • KM Jones et al.

    Fast spin-echo MR imaging of the brain and spine: current concepts

    AJR Am J Roentgenol

    (1992)
  • SW Atlas et al.

    Intracranial hemorrhage: gradient-echo MR imaging at 1.5 T. Comparison with spin-echo imaging and clinical applications

    Radiology

    (1988)
  • SM Greenberg et al.

    Petechial hemorrhages accompanying lobar hemorrhage: detection by gradient-echo MRI

    Neurology

    (1996)
  • M Hermier et al.

    MRI of acute post-ischemic cerebral hemorrhage in stroke patients: diagnosis with T2*-weighted gradient-echo sequences

    Neuroradiology

    (2001)
  • T Kinoshita et al.

    Assessment of lacunar hemorrhage associated with hypertensive stroke by echo-planar gradient-echo T2*-weighted MRI

    Stroke

    (2000)
  • L Liang et al.

    Detection of intracranial hemorrhage with susceptibility-weighted MR sequences

    AJNR Am J Neuroradiol

    (1999)
  • MW Vernooij et al.

    Cerebral microbleeds: accelerated 3D T2*-weighted GRE MR imaging versus conventional 2D T2*-weighted GRE MR imaging for detection

    Radiology

    (2008)
  • S Tatsumi et al.

    Type of gradient recalled-echo sequence results in size and number change of cerebral microbleeds

    AJNR Am J Neuroradiol

    (2008)
  • M Henkelman et al.

    Optimization of gradient-echo MR for calcium detection

    AJNR Am J Neuroradiol

    (1994)
  • RNK Nandigam et al.

    MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength

    AJNR Am J Neuroradiol

    (2008)
  • K Kikuta et al.

    Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study

    J Neurosurg

    (2005)
  • R Scheid et al.

    Comparative magnetic resonance imaging at 1.5 and 3 Tesla for the evaluation of traumatic microbleeds

    J Neurotrauma

    (2007)
  • EM Haacke et al.

    Susceptibility weighted imaging (SWI)

    Magn Reson Med

    (2004)
  • SM Greenberg et al.

    Microbleeds versus macrobleeds: evidence for distinct processes

    Stroke

    (2008)
  • JM Zabramski et al.

    The natural history of familial cavernous malformations: results of an ongoing study

    J Neurosurg

    (1994)
  • R Al-Shahi Salman et al.

    Hemorrhage from cavernous malformations of the brain: definition and reporting standards

    Stroke

    (2008)
  • P Gaviani et al.

    Improved detection of metastatic melanoma by T2*-weighted imaging

    AJNR Am J Neuroradiol

    (2006)
  • RL Mittl et al.

    Prevalence of MR evidence of diffuse axonal injury in patients with mild head injury and normal head CT findings

    AJNR Am J Neuroradiol

    (1994)
  • C Cordonnier et al.

    Improving inter-rater agreement about brain microbleeds: development of the Brain Observer MicroBleed Scale (BOMBS)

    Stroke

    (2009)
  • A Tanaka et al.

    Small chronic hemorrhages and ischemic lesions in association with spontaneous intracerebral hematomas

    Stroke

    (1999)
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