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Blood−brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury
Open accessAbstract
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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“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“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]
Experimental — accuracy not yet measuredIn the citing paper
“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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“Moreover, high level of ROS contributes to TJs degradation and BBB breakdown and exacerbates brain damage by promoting the degradation of TJs (Prakash and Carmichael 2015; Yang et al. 2015).”
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Delayed Traumatic Intracerebral Hematoma: A Pathophysiological Classification and Literature Review
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“We defined DTICH type 1A as hematomas that develop within one week following a TBI in areas initially free of hemorrhage on CT imaging.”
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“After ischemia, the BBB opens within hours after infarction, permitting the influx of blood-borne components and immune cells into the brain [19, 20].”
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“Oxidative stress, characterised by the excessive availability of ROS, represents one of the key mechanisms involved in the pathophysiology of BBB damage following an ischaemic stroke (33-39).”
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“Ischemic insults disrupt TJs alignment and increase vessel permeability, rapidly leading to BBB dysfunction, and inducing cerebral edema (Prakash and Carmichael, 2015; Dharmasaroja, 2016).”
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“Blood–brain barrier injury is characterized by an increase in permeability and the degradation of structural proteins (Prakash and Carmichael 2015).”
BackgroundExamining the potential of psilocybin and 5-MeO-DMT as therapeutics for traumatic brain injury
Plummer, Z., Allen, J., Brand, J., Mayo, L. M., Shultz, S. R., & Christie, B. R. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111448 · Cited by 6
Naringin Supplementation Reduces Inflammatory Processes in the Cerebellum in Brain Ischemia of Rats
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“Cellular signaling continues acutely and postacutely to restore homeostasis in injured tissue, which, if not controlled, can exacerbate the injury.(8,17) Furthermore, studies suggest that brain tissue oxygen-based therapy can reduce mortality rate and ameliorate neurological outcome for TBI patients.”
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Zaharia, A. L., Tutunaru, D., Oprea, V. D., Tănase, C. E., Croitoru, A., Stan, B., Voinescu, D. C., Ionescu, A.-M., Coadǎ, C. A., & Lungu, M. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46010044 · Cited by 5
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“Ensuing Blood–Brain Barrier (BBB) breakdown and neurogenic inflammation [11, 12] will then reinforce brain edema and early/late apoptosis [7].”
BackgroundGoebel, J., Engelhardt, E., Pelzer, P., Sakthivelu, V., Jahn, H. M., Jevtic, M., Folz-Donahue, K., Kukat, C., Schauss, A., Frese, C. K., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/657999 · Cited by 5
“These types of injury often result in significant damage to the cerebrovasculature and are usually accompanied by blood-brain barrier breakdown, intracerebral hemorrhage, hypoxia, secondary inflammation and neurodegeneration (Prakash and Carmichael, 2015; Salehi et al., 2017).”
BackgroundCho, S. S., Shin, E. J., Kim, Y. G., & Kim, K. M. (2026) · Archives of Pharmacal Research · doi:10.1007/s12272-026-01593-1 · Cited by 4
“Chronic BBB disruption increases vascular permeability, allowing continued infiltration of peripheral immune cells, which propagates a cycle of inflammation, oxidative stress, and neurovascular injury (Prakash and Carmichael 2015).”
InfluentialHinwood, M., Nyberg, J., Leigh, L., Gustavsson, S., Attia, J., Oldmeadow, C. J., Ilicic, M., Linden, T. K. A., Åberg, N. D., Levi, C. R., et al. (2022) · BMJ Open · doi:10.1136/bmjopen-2021-058244 · Cited by 4
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The Role of Circular RNAs in Ischemic Stroke
Jiang, W., Long, X., Li, Z., Hu, M., Zhang, Y., Lin, H., Tang, W., Ouyang, Y., Jiang, L., Chen, J., et al. (2023) · Neurochemical Research · doi:10.1007/s11064-023-03935-7 · Cited by 4
“After IS, blood-derived cells, chemicals, and fluids infiltrate the brain parenchyma through the damaged BBB due to increased paracellular and transcellular permeability and severe damage to the endothelium, which disrupts water and ion homeostasis in the brain, leading to cerebral edema [98].”
Regulation of the Blood–Brain Barrier in Health and DiseasePreprint
Rada, C. C., Yuki, K., Ding, J., & Kuo, C. J. (2023) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041191 · Cited by 4
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Al‐Salihi, M. M., Al-Jebur, M. S., Elazim, A. A., Saha, R. K., Saleh, A., Siddiq, F., Ayyad, A., & Qureshi, A. I. (2025) · NeuroSci · doi:10.3390/neurosci6010021 · Cited by 3
“An increase in intracranial pressure and brain swelling, which lead to a reduction in cerebral perfusion pressure (CPP), are believed to disrupt autoregulation [26–28].”
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“This process is primarily mediated by synaptic plasticity, which adjusts synaptic strength based on activity-dependent demands, thus reestablishing disrupted connections and integrating new neural circuits essential for restoring function (Witkowski et al., 2019; Su and Xu, 2020; Kiani, 2024).”
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“As the structural component of the BBB, the EC regulates molecular exchange through two principal mechanisms: paracellular transport via TJ complexes and transcellular movement mediated by caveolae [34, 35].”
Increase of Meningitis Risk in Stroke Patients in Taiwan
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“The upregulation of MMP-9 was an early response of stroke; however, we still do not fully understand the impact of MMP-9 on BBB recovery and how the BBB recovers (27).”
Backgroundİnmede beyin ödemi ve kafa içi basınç artışı: Türk Beyin Damar Hastalıkları Derneği uzman görüşü
Güngör, L., ŞİRİN, H., Mengi, T., Kozak, H. H., Sorgun, M. H., Nazlıel, B., Çinleti, B. A., Öztürk, Ş., Pektezel, M. Y., Örken, D. N., et al. (2021) · Turkish Journal of Cerebrovascular Diseases · doi:10.5505/tbdhd.2021.76376 · Cited by 3
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“…oncotic pressure (impaired endothelial cell aquaporin 1 and 4 function) leads to a further increase in ICP with herniation and midline shift, and thus to a reduction in cerebral perfusion pressure (CPP), which is a surrogate for cerebral blood flow (CBF), and an increase in ischaemia [59,62,63].”
DETOX: An innovative dendritic nanosystem for the delivery of BoNT/A LC domain to ischemic neurons
Torrado, M., Sinthon, C., Silva, D., Moreira, D. A., Magalhães, N., Ferreira‐da‐Silva, F., Fonseca, F., Furihata, T., Piantino, M., Matsusaki, M., et al. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123684 · Cited by 2
Intracerebral haemorrhage and Guillain-Barré syndrome: an exploration of potential pathophysiology
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Late Subacute Cerebral Hematoma Mimicking a Metastasis on PSMA PET/CT
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“Stroke: Dysfunction of BBB is a prominent pathological feature of both ischemic and hemorrhagic stroke and is typically associated with poor outcome [86-88].”
BackgroundDoron, O., Wong, T., Ablyazova, F., Singha, S., Cavallaro, J., Ben-Shalom, N., D’Amico, R. S., Harshan, M., McKeown, A., Zlochower, A. B., et al. (2024) · Journal of Neuro-Oncology · doi:10.1007/s11060-024-04647-w · Cited by 2
“Analyses of these newly formed blood vessels show that the vessels that form either lack or have a substantially more permeable BBB relative to healthy brain tissue [12].”
BackgroundInfluentialЧернышева, Г. А., Smol’yakova, V. I., Плотников, М. Б., Aliev, O. I., Ulyakhina, O. A., Osipenko, A. N., Kovrizhina, A. R., & Khlebnikov, А. I. (2025) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-025-06459-y · Cited by 1
“After recirculation, the early BBB opening may also be due to pronounced reactive hyperemia that develops after elimination of arterial occlusion in ischemic areas, and disruption of cell membranes during reoxygenation [14].”
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“In hypoxic microenvironment like stroke, TBI, etc ., blood supply is limited in BMVEC resulting excitotoxicity, inflammation and cell death that led to the loss of TJ protein in the NVU 41 .”
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“For instance, alterations in aspartic acid (Asp), 5-hydroxytryptamine (5-HT), γ-aminobutyric acid (GABA), dopamine (DA), and glutamate (Glu) have been re-ported to be present in CI/RI [15, 16].”
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“CA, Cornu Ammonis; DG, Dentate Gyrus; GO, Gene Ontology; GSEA, Gene Set Enrichment Analysis; FC, Fold-change; TBI, traumatic brain injury. containment and repair (37–39).”
Paul, M., Paúl, J., Hinwood, M., Hood, R. J., Martin, K. L., Abdolhoseini, M., Johnson, S. J., Pollack, M. R. P., Nilsson, M., & WALKER, F. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062547 · Cited by 1
“Notably, one of the hallmarks of ischemic stroke is the disruption of the BBB [15,16].”
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“Impaired BBB integrity is an established pathogenic factor for PSCI in ischemic stroke patients (Prakash and Carmichael 2015 ; Panahpour et al. 2018 ; Jin et al. 2010 ).”
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“Stroke mostly affects the elderly population while the incidence of TBI extends to all age groups (5).”
BackgroundStewart, W. B., Jr., Hejl, C., Guleria, R. S., & Gupta, S. (2023) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2023.12167 · Cited by 1
“Disruption of the BBB due to injury can result in increased BBB permeability, which promotes several neurological diseases (7,11).”
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“This results in neurological deficits dependent upon the type of injury and specific location within the brain as well as vascular damage which results in immediate hemorrhage ((6)).”
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Memory deficits in males and females long after subchronic immune challengePreprint
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“The reason behind it could be that the region of active neovascularization acts as a niche for enhanced neuronal remodeling and tissue repair (Prakash & Carmichael, 2015; Shen et al., 2008).”
BackgroundEffect of integrin AV and B8 gene polymorphisms in patients with traumatic brain injury
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“The pathophysiology of TBI regarding the BBB has several aspects that have only just begun being elucidated; its disruption and recovery follow several complicated steps that have more extensively been studied in strokes and not in TBI (43).”
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Metadata
- Authors
- Prakash, R., & Carmichael, S. T.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Prakash, Roshini
- Venue
- Current Opinion in Neurology
- Published
- 2015-12
- Volume
- 28
- Issue
- 6
- Pages
- 556-564
- ISSN
- 1350-7540 (ISSN-L)
- 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 › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Clinical Neurology › 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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