Blood-Brain Barrier Leakage and Microvascular Lesions in Cerebral Amyloid Angiopathy

Freeze, Whitney M.; Bacskai, Brian J.; Frosch, Matthew P.; Jacobs, Heidi I.L.; Backes, Walter H.; Greenberg, Steven M.; van Veluw, Susanne J.

doi:10.1161/strokeaha.118.023788

Cited by 85Intracerebral and Subarachnoid Hemorrhage ResearchCerebrovascular and genetic disordersBarrier Structure and Function Studies

Blood-Brain Barrier Leakage and Microvascular Lesions in Cerebral Amyloid Angiopathy

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Freeze, Whitney M., Bacskai, Brian J., Frosch, Matthew P., Jacobs, Heidi I.L., Backes, Walter H., Greenberg, Steven M., van Veluw, Susanne J.·2019·Stroke

DOI 10.1161/strokeaha.118.023788PMC PMC6415745

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Abstract

Background and Purpose—: Cerebral amyloid angiopathy (CAA) is a common small vessel disease that independently effects cognition in older individuals. The pathophysiology of CAA and CAA-related bleeding remains poorly understood. In this postmortem study, we explored whether blood-brain barrier leakage is associated with CAA and microvascular lesions. Methods—: Eleven CAA cases (median [IQR] age=69 years [65–79 years], 8 males) and 7 cases without neurological disease or brain lesions (median [IQR] age=77 years [68–92 years], 4 males) were analyzed. Cortical sections were sampled from each lobe, and IgG and fibrin extravasation (markers of blood-brain barrier leakage) were assessed with immunohistochemistry. We hypothesized that IgG and fibrin extravasation would be increased in CAA cases compared with controls, that this would be more pronounced in parietooccipital brain regions compared with frontotemporal brain regions in parallel with the posterior predilection of CAA, and would be associated with CAA severity and number of cerebral microbleeds and cerebral microinfarcts counted on ex vivo magnetic resonance imaging of the intact brain hemisphere. Results—: Our results demonstrated increased IgG positivity in the frontotemporal ( P =0.044) and parietooccipital ( P =0.001) cortex in CAA cases compared with controls. Within CAA cases, both fibrin and IgG positivity were increased in parietooccipital brain regions compared with frontotemporal brain regions ( P =0.005 and P =0.006, respectively). The percentage of positive vessels for fibrin and IgG was associated with the percentage of amyloid-β–positive vessels (Spearman ρ=0.71, P =0.015 and Spearman ρ=0.73, P =0.011, respectively). Moreover, the percentage of fibrin and IgG-positive vessels, but not amyloid-β–positive vessels, was associated with the number of cerebral microbleeds on magnetic resonance imaging (Spearman ρ=0.77, P =0.005 and Spearman ρ=0.70, P =0.017, respectively). Finally, we observed fibrin deposition in walls of vessels involved in cerebral microbleeds. Conclusions—: Our results raise the possibility that blood-brain barrier leakage may be a contributory mechanism for CAA-related brain injury.

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In postmortem brain tissue of individuals with CAA, circulating plasma proteins fibrin(ogen) and immunoglobulin G have been observed in the walls of blood vessels without hemorrhage, indicative of a leaky BBB.
“In postmortem brain tissue of individuals with CAA, circulating plasma proteins fibrin(ogen) and immunoglobin G (IgG) have been observed in the walls of blood vessels without hemorrhage,7,8 indicative of a leaky BBB.”
From In Vivo Imaging of Blood-Brain Barrier Leakage Using a Contrast Agent in Patients With Cerebral Amyloid Angiopathy: An Exploratory Study (2025) · cites this paper as [7]

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Additional file 5 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
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Additional file 2 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
Jäkel, L., Kuiperij, H. B., Gerding, L. P., Custers, E., van den Berg, E., Jolink, W. M. T., Schreuder, F. H. B. M., Küsters, B., Klijn, C. J. M., & Verbeek, M. M. (2020) · Figshare · doi:10.6084/m9.figshare.12617913
Additional file 3 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
Jäkel, L., Kuiperij, H. B., Gerding, L. P., Custers, E., van den Berg, E., Jolink, W. M. T., Schreuder, F. H. B. M., Küsters, B., Klijn, C. J. M., & Verbeek, M. M. (2020) · Figshare · doi:10.6084/m9.figshare.12617916
Additional file 1 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
Jäkel, L., Kuiperij, H. B., Gerding, L. P., Custers, E., van den Berg, E., Jolink, W. M. T., Schreuder, F. H. B. M., Küsters, B., Klijn, C. J. M., & Verbeek, M. M. (2020) · Figshare · doi:10.6084/m9.figshare.12617910
Additional file 6 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
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Additional file 1 of Deep learning assisted quantitative assessment of histopathological markers of Alzheimer’s disease and cerebral amyloid angiopathy
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Additional file 4 of Disturbed balance in the expression of MMP9 and TIMP3 in cerebral amyloid angiopathy-related intracerebral haemorrhage
Jäkel, L., Kuiperij, H. B., Gerding, L. P., Custers, E., van den Berg, E., Jolink, W. M. T., Schreuder, F. H. B. M., Küsters, B., Klijn, C. J. M., & Verbeek, M. M. (2020) · Figshare · doi:10.6084/m9.figshare.12617919
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P2‐479: BLOOD‐BRAIN BARRIER LEAKAGE AND MICROVASCULAR LESIONS IN CEREBRAL AMYLOID ANGIOPATHY: A POSTMORTEM MRI AND HISTOPATHOLOGY STUDY
Freeze, W. M., Greenberg, S. M., Frosch, M. P., Jacobs, H. I. L., Backes, W. H., Bacskai, B. J., & van Veluw, S. J. (2018) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.06.1172
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IC‐P‐051: BLOOD‐BRAIN BARRIER LEAKAGE AND MICROVASCULAR LESIONS IN CEREBRAL AMYLOID ANGIOPATHY: A POSTMORTEM MRI AND HISTOPATHOLOGY STUDY
Freeze, W. M., Greenberg, S. M., Frosch, M. P., Jacobs, H. I. L., Backes, W. H., Bacskai, B. J., & van Veluw, S. J. (2018) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.06.2116
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Blood–brain barrier leakage and perivascular inflammation in cerebral amyloid angiopathy
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In Vivo Imaging of Blood-Brain Barrier Leakage Using a Contrast Agent in Patients With Cerebral Amyloid Angiopathy: An Exploratory Study
van den Brink, H., Kozberg, M. G., Makkinejad, N., Kirsch, J. E., Thrippleton, M. J., van Harten, T. W., Voigt, S., Freeze, W. M., Van Osch, M. J. P., Viswanathan, A., et al. (2025) · Neurology · doi:10.1212/wnl.0000000000214336 · Cited by 11 · see citing works
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Contrasting patterns of leptomeningeal and parenchymal gadolinium extravasation in cerebral amyloid angiopathy: An MRI-based evaluation
Voigt, S., de Jong, J., Voorter, P., Koemans, E. A., Schipper, M. R., van der Plas, M. C., Kaushik, K., van der Zwet, R. G. J., van Dort, R., van den Brink, H., et al. (2026) · International Journal of Stroke · doi:10.1177/17474930261424089 · Cited by 3 · see citing works
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Authors: Freeze, W. M., Bacskai, B. J., Frosch, M. P., Jacobs, H. I. L., Backes, W. H., Greenberg, S. M., & van Veluw, S. J.
Affiliations: Harvard University (US)
Massachusetts General Hospital (US)
Maastricht University Medical Centre (NL)
MassGeneral Institute for Neurodegenerative Disease (MIND), Massachusetts General Hospital, Charlestown (W.M.F., B.J.B., M.P.F., S.J.v.V.)
ORCID: Freeze, Whitney M.
Bacskai, Brian J.
Frosch, Matthew P.
Jacobs, Heidi I.L.
Backes, Walter H.
Greenberg, Steven M.
Venue: Stroke
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2019-02
Volume: 50
Issue: 2
Pages: 328-335
ISSN: 0039-2499 (ISSN-L)
1524-4628
DOI: 10.1161/strokeaha.118.023788
PMC: PMC6415745
OpenAlex: W2911060979
Cited by: 85
References: 37
Citations by year: 2026: 9 · 2025: 8 · 2024: 6 · 2023: 7 · 2022: 14 · 2021: 20 · 2020: 17 · 2019: 4
FWCI: 9.31
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Stroke (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion, other-oa)
PubMed Central (acceptedVersion)
Leiden Repository (Leiden University) (submittedVersion, cc-by)
Research Publications (Maastricht University) (submittedVersion, other-oa)
Funders: National Institute on Aging (P30AG062421)
National Institute of Neurological Disorders and Stroke (RF1NS110054, R01NS096730)
Topics: Health Sciences › Medicine › Neurology › Intracerebral and Subarachnoid Hemorrhage Research
Health Sciences › Medicine › Neurology › Cerebrovascular and genetic disorders
Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Keywords: cerebral amyloid angiopathy, blood-brain barrier disruption, IgG extravasation, fibrin deposition, cerebral microbleeds, cerebral microinfarcts, cerebral small vessel disease, postmortem brain, frontotemporal cortex, intracerebral hemorrhage
MeSH terms: Aged, Aged, 80 and over, Autopsy, Blood Proteins, Blood-Brain Barrier, Capillary Permeability, Cerebral Cortex, Exudates and Transudates, Female, Fibrin, Humans, Immunoglobulin G, Magnetic Resonance Imaging, Male, Amyloid beta-Peptides, Cerebral Amyloid Angiopathy, Microvessels, Neuroimaging

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Blood-Brain Barrier Leakage and Microvascular Lesions in Cerebral Amyloid Angiopathy

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