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      Radiologic-Histopathologic Correlation of Cerebral Microbleeds Using Pre-Mortem and Post-Mortem MRI

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          Abstract

          Introduction

          Cerebral microbleeds (CMB), also known as cerebral microhemorrhages, are small areas of susceptibility on brain magnetic resonance imaging (MRI), that are increasingly detected due to the higher availability of high-field MRI systems and dedicated pulse sequences. The prevalence of CMBs increases in cases with cognitive decline. The current investigation assessed the poorly investigated radiologic–histopathologic correlation of CMBs on MRI.

          Methods

          The local ethical committee approved the current investigation. We retrospectively assessed a consecutive series of 1303 autopsy cases hospitalized in Geneva University Hospitals between 2000–2014. Of 112 cases with pre-mortem T2* sequences, we included 25 cases (mean age 77.3 ± 9.6, 9 females) with at least one CMB. We compared pre-mortem CMBs with targeted histopathology and post-mortem MRI.

          Results

          25 cases had 31 CMB lesions detected by pre-mortem MRI. 25 additional CMB were detected on histopathology. 4 CMBs on pre-mortem MRI were false positives, resulting in a total of 52 CMBs. 27 CMBs on pre-mortem MRI were confirmed on histopathology, corresponding to a sensitivity or true positive rate of 51.9% (95% CI 37.6–66.0%). The false negative rate of pre-mortem MRI was 48.1% (95% CI 34.0–62.4%). Post-mortem MRI showed only 3 cases with additional CMBs. Overall, pre-mortem MRI significantly underestimated CMBs (p = 0.0001).

          Conclusions

          Routine clinical brain MRI underestimates the prevalence of CMBs by approximately 50%, and 12% of radiologic pre-mortem MRI CMBs were false positives. Post-mortem MRI confirmed that this discordance is not explained by microbleeds occurring after the pre-mortem MRI.

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          Most cited references24

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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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            A spreadsheet for the calculation of comprehensive statistics for the assessment of diagnostic tests and inter-rater agreement.

            Andrew MacKinnon (2000)
            While advances in statistical methods allow greater insight into the characteristics of diagnostic tests and of raters, researchers frequently rely on incomplete or inappropriate indices of performance. Lack of available computer software is probably an important barrier to optimal use of data collected to evaluate diagnostic tests and agreement between raters. A spreadsheet has been designed to provide comprehensive statistics for the assessment of diagnostic tests and inter-rater reliability when these investigations yield data that can be summarized in a 2x2 table. As well as a wide range of indices of test or rater performance, confidence intervals for these quantities are also calculated by the spreadsheet.
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              MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength.

              Brian Skehan, Laura-Jane Smith, Andrew S. Greenberg … (2009)
              The emergence of cerebral microbleeds (CMB) as common MR imaging findings raises the question of how MR imaging parameters influence CMB detection. To evaluate the effects of modified gradient recalled-echo (GRE) MR imaging methods, we performed an analysis of sequence, section thickness, and field strength on CMB imaging properties and detection in subjects with cerebral amyloid angiopathy (CAA), a condition associated with microhemorrhage. Multiple MR images were obtained from subjects with probable CAA, with varying sequences (GRE versus susceptibility-weighted imaging [SWI]), section thicknesses (1.2-1.5 versus 5 mm), and magnetic field strengths (1.5T versus 3T). Individual CMB were manually identified and analyzed for contrast index (lesion intensity normalized to normal-appearing white matter signal intensity) and diameter. CMB counts were compared between 1.5T thick-section GRE and thin-section SWI for 3 subjects who underwent both protocols in the same scanning session. With other parameters constant, use of SWI, thinner sections, and a higher field strength yielded medium-to-large gains in CMB contrast index (CI; Cohen d 0.71-1.87). SWI was also associated with small increases in CMB diameter (Cohen d <0.3). Conventional thick-section GRE identified only 33% of CMB (103 of 310) seen on thin-section SWI. Lesions prospectively identified on GRE had significantly greater CI and diameter measured on the GRE image than those not prospectively identified. The examined alternatives to conventional GRE MR imaging yield substantially improved CMB contrast and sensitivity for detection. Future studies based on these techniques will most likely yield even higher prevalence estimates for CMB.
              Article 0 comments Cited 103 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Quan Jiang: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 9 December 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 12
                Electronic Location Identifier: e0167743
                Affiliations
                [1 ]Affidea Centre de Diagnostic Radiologique de Carouge CDRC, Carouge, Switzerland
                [2 ]Medical School of the University of Geneva, Geneva, Switzerland
                [3 ]Department of Surgical Sciences, Radiology, Uppsala University, Uppsala, Sweden
                [4 ]Department of Neuroradiology, University Hospital Freiburg, Freiburg im Breisgau, Germany
                [5 ]Department of Mental Health and Psychiatry, University Hospitals of Geneva, Geneva, Switzerland
                [6 ]Department of Radiology and Medical Informatics, University of Geneva, Geneva, Switzerland
                [7 ]Division of Geriatrics, Department of internal medicine, rehabilitation and geriatrics, Geneva University Hospitals, Geneva, Switzerland
                [8 ]Medical Direction, University Hospitals of Geneva, Geneva, Switzerland
                Henry Ford Health System, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: SH EK.

                • Data curation: MLM SH EK.

                • Formal analysis: SH MLM FH FL EK.

                • Funding acquisition: SH EK.

                • Investigation: SH MLM FH FL EK.

                • Methodology: SH EK MLM.

                • Project administration: SH EK.

                • Resources: SH EK.

                • Supervision: SH PG EK.

                • Validation: SH EK PG FH FL SM MS.

                • Visualization: SH MLM EK.

                • Writing – original draft: SH.

                • Writing – review & editing: SH MLM FL MS SM FH PG EK.

                Author information
                http://orcid.org/0000-0001-7433-0203
                Article
                Publisher ID: PONE-D-16-39115
                DOI: 10.1371/journal.pone.0167743
                PMC ID: 5147972
                PubMed ID: 27936213
                SO-VID: 77d41840-8659-4341-a8bd-7fd3c1750601
                Copyright © © 2016 Haller et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 30 September 2016
                Date accepted : 20 November 2016
                Page count
                Figures: 4, Tables: 1, Pages: 11
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 320030_159990/1
                Award Recipient :
                This work is supported in part by Swiss National Foundation Grant SNF 320030_159990/1 and an unrestricted grant from the Association Suisse pour la Recherche Alzheimer, Geneva.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Research and Analysis Methods
                Subject: Imaging Techniques
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Diagnostic Radiology
                Subject: Magnetic Resonance Imaging
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Anatomical Pathology
                Subject: Histopathology
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Science
                Subject: Cognitive Neuroscience
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Biology and Life Sciences
                Subject: Neuroscience
                Subject: Cognitive Neuroscience
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cognitive Neurology
                Subject: Cognitive Impairment
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Vascular Medicine
                Subject: Hemorrhage
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Lesions
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Lesions
                Subject: Medicine and Health Sciences
                Subject: Radiology and Imaging
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Cerebrovascular Diseases
                Subject: Vascular Dementia
                Subject: Medicine and Health Sciences
                Subject: Mental Health and Psychiatry
                Subject: Dementia
                Subject: Vascular Dementia
                Subject: Medicine and Health Sciences
                Subject: Neurology
                Subject: Dementia
                Subject: Vascular Dementia
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Histology
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Histology
                Custom metadata
                Data Availability The ethical committee of the Kanton of Geneva, including the University Hospitals of Geneva, does not allow to publicly share imaging data of patients without their explicit written informed consent [ http://ge.ch/sante/commission-cantonale-dethique-de-recherche-ccer/commission-cantonale-dethique-de-recherche-ccer]. In the current post-mortem radiologic-histopathologic correlation study, informed patient consent can evidently not be obtained. Consequently, imaging data cannot be publicly shared. MR imaging data can be assessed after discussion with Sven HALLER, sven.haller@ 123456gmail.com . Histopathologic imaging data can be assessed after discussion with Enikö Kövari, Eniko.Kovari@ 123456hcuge.ch .

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                ScienceOpen disciplines: Uncategorized

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