Blood−brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury

Prakash, Roshini; Carmichael, S. Thomas

doi:10.1097/wco.0000000000000248

Cited by 296Barrier Structure and Function StudiesTraumatic Brain Injury and Neurovascular DisturbancesAcute Ischemic Stroke Management

Blood−brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury

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Prakash, Roshini, Carmichael, S. Thomas·2015·Current Opinion in Neurology

DOI 10.1097/wco.0000000000000248PMC PMC5267616

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Abstract

PURPOSE OF REVIEW: Angiogenesis or vascular reorganization plays a role in recovery after stroke and traumatic brain injury (TBI). In this review, we have focused on two major events that occur during stroke and TBI from a vascular perspective - what is the process and time course of blood-brain barrier (BBB) breakdown? and how does the surrounding vasculature recover and facilitate repair? RECENT FINDINGS: Despite differences in the primary injury, the BBB changes overlap between stroke and TBI. Disruption of BBB involves a series of events: formation of caveolae, trans and paracellular disruption, tight junction breakdown and vascular disruption. Confounding factors that need careful assessment and standardization are the severity, duration and extent of the stroke and TBI that influences BBB disruption. Vascular repair proceeds through long-term neovascularization processes: angiogenesis, arteriogenesis and vasculogenesis. Enhancing each of these processes may impart beneficial effects in endogenous recovery. SUMMARY: Our understanding of BBB breakdown acutely after the cerebrovascular injury has come a long way; however, we lack a clear understanding of the course of BBB disruption and BBB recovery and the evolution of individual cellular events associated with BBB change. Neovascularization responses have been widely studied in stroke for their role in functional recovery but the role of vascular reorganization after TBI in recovery is much less defined.

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Blood-brain barrier dysfunction is a prominent pathological feature of both ischemic and hemorrhagic stroke and is typically associated with poor outcome.
“BBB dysfunction is a prominent pathological feature of both ischemic and hemorrhagic stroke and is typically associated with poor outcome (307, 312, 482).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [482]
The section “What is the blood–brain barrier?” (page unavailable) calls BBB dysfunction a common, prominent pathological feature of stroke, and “Blood–brain barrier breakdown in stroke” discusses it after ischemia. The copy does not establish this specifically for hemorrhagic stroke or say that BBB dysfunction is typically associated with poor outcome; searches for “hemorrhagic” and “poor outcome” did not find those claims. (LLM, conf=0.88)
Experimental — accuracy not yet measured
In preclinical models of ischemic stroke, opening of the blood-brain barrier has been shown to be a biphasic phenomenon.
“In preclinical models of ischemic stroke, opening of BBB has been shown to be a biphasic phenomenon (482).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [482]
The “Blood–brain barrier breakdown in stroke” section says animal-model research suggests an early and a delayed phase of BBB opening. It also says leakage can be monophasic or biphasic depending on the model and measurement method, so the claim overstates biphasic opening as a general finding across preclinical ischemic-stroke models. (LLM, conf=0.88)
Experimental — accuracy not yet measured
An increase of blood-brain barrier permeability could be determined by severe stress and/or traumatic brain injury.
“For instance, it has been suggested that an increase of the blood-brain barrier (BBB) permeability could be determined by severe stress and/or traumatic brain injury [35,36].”
From C-Reactive protein as a biomarker for major depressive disorder? (2022) · cites this paper as [35]

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Blood-Brain Barrier: From Physiology to Disease and Back
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Blocking C3d+/GFAP+ A1 Astrocyte Conversion with Semaglutide Attenuates Blood-Brain Barrier Disruption in Mice after Ischemic Stroke
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No-Reflow Post-Recanalization in Acute Ischemic Stroke: Mechanisms, Measurements, and Molecular Markers
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Gut microbial dysbiosis after traumatic brain injury modulates the immune response and impairs neurogenesis
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Harilal, S., Jose, J., Parambi, D. G. T., Kumar, R., Unnikrishnan, M. K., Uddin, M. S., Mathew, G. E., Pratap, R., Marathakam, A., & Mathew, B. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.03.018 · Cited by 124 · see citing works
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Medioresinol as a novel PGC-1α activator prevents pyroptosis of endothelial cells in ischemic stroke through PPARα-GOT1 axis
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Selective Liposomal Transport through Blood Brain Barrier Disruption in Ischemic Stroke Reveals Two Distinct Therapeutic Opportunities
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PDGFR-β restores blood-brain barrier functions in a mouse model of focal cerebral ischemia
Shen, J., Xu, G., Zhu, R., Yuan, J., Ishii, Y., Hamashima, T., Matsushima, T., Yamamoto, S., Takatsuru, Y., Nabekura, J., et al. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18769515 · Cited by 107 · see citing works
Borneol for Regulating the Permeability of the Blood-Brain Barrier in Experimental Ischemic Stroke: Preclinical Evidence and Possible Mechanism
Chen, Z., Xu, Q.-Q., Shan, C.-S., Shi, Y., Wang, Y., Chang, R. C., & Zheng, G. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2936737 · Cited by 97 · see citing works
The Proliferation and Differentiation of Adipose-Derived Stem Cells in Neovascularization and Angiogenesis
Hutchings, G., Janowicz, K., Moncrieff, L., Dompé, C., Strauss, E., Kocherova, I., Nawrocki, M. J., Kruszyna, Ł., Wąsiatycz, G., Antosik, P., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113790 · Cited by 96 · see citing works
Inhibition of Caspase-1 Ameliorates Ischemia-Associated Blood-Brain Barrier Dysfunction and Integrity by Suppressing Pyroptosis Activation
Liang, Y., Song, P., Chen, W., Xie, X., Luo, R., Su, J.-H., Zhu, Y., Xu, J., Liu, R., Zhu, P., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.540669 · Cited by 94 · see citing works
Humble beginnings with big goals: Small molecule soluble epoxide hydrolase inhibitors for treating CNS disorders
Zarriello, S., Tuazon, J. P., Corey, S., Schimmel, S. J., Rajani, M., Gorsky, A., Abraham, D. I., Hammock, B. D., & Borlongan, C. V. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.11.001 · Cited by 92 · see citing works
Executive (dys)function after traumatic brain injury: special considerations for behavioral pharmacology
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Glycocalyx is critical for blood‐brain barrier integrity by suppressing caveolin1‐dependent endothelial transcytosis following ischemic stroke
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The peripheral immune response after stroke—A double edge sword for blood‐brain barrier integrity
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Traumatic Brain Injury: A Comprehensive Review of Biomechanics and Molecular Pathophysiology
Orr, T. J., Lesha, E., Kramer, A. H., Cecia, A. F., Dugan, J. E., Schwartz, B., & Einhaus, S. L. (2024) · World Neurosurgery · doi:10.1016/j.wneu.2024.01.084 · Cited by 81 · see citing works
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Authors: Prakash, R., & Carmichael, S. T.
Affiliations: University of California, Los Angeles (US)
Corresponding author: Prakash, Roshini
ORCID: Prakash, Roshini
Carmichael, S. Thomas
Venue: Current Opinion in Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2015-12
Volume: 28
Issue: 6
Pages: 556-564
ISSN: 1350-7540 (ISSN-L)
DOI: 10.1097/wco.0000000000000248
PMC: PMC5267616
OpenAlex: W2341136898
Cited by: 296
References: 134
Citations by year: 2026: 16 · 2025: 27 · 2024: 32 · 2023: 29 · 2022: 33 · 2021: 38 · 2020: 36 · 2019: 31 · 2018: 24 · 2017: 19 · 2016: 11
FWCI: 1.44
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Current Opinion in Neurology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS081055, R01NS053957)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
Health Sciences › Medicine › Epidemiology › Acute Ischemic Stroke Management
Keywords: blood-brain barrier disruption, neovascularization, stroke, traumatic brain injury, angiogenesis, arteriogenesis, vasculogenesis, vascular repair, caveolae, tight junction disruption, paracellular permeability, functional recovery
MeSH terms: Blood-Brain Barrier, Brain Injuries, Humans, Neovascularization, Physiologic, Stroke

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Blood−brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury

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