Topographic distribution of inflammation factors in a healing aneurysm.


Journal

Journal of neuroinflammation
ISSN: 1742-2094
Titre abrégé: J Neuroinflammation
Pays: England
ID NLM: 101222974

Informations de publication

Date de publication:
02 Aug 2023
Historique:
received: 23 05 2023
accepted: 26 07 2023
medline: 4 8 2023
pubmed: 3 8 2023
entrez: 2 8 2023
Statut: epublish

Résumé

Healing of intracranial aneurysms following endovascular treatment relies on the organization of early thrombus into mature scar tissue and neointima formation. Activation and deactivation of the inflammation cascade plays an important role in this process. In addition to timely evolution, its topographic distribution is hypothesized to be crucial for successful aneurysm healing. Decellularized saccular sidewall aneurysms were created in Lewis rats and coiled. At follow-up (after 3 days (n = 16); 7 days (n = 19); 21 days (n = 8)), aneurysms were harvested and assessed for healing status. In situ hybridization was performed for soluble inflammatory markers (IL6, MMP2, MMP9, TNF-α, FGF23, VEGF), and immunohistochemical analysis to visualize inflammatory cells (CD45, CD3, CD20, CD31, CD163, HLA-DR). These markers were specifically documented for five regions of interest: aneurysm neck, dome, neointima, thrombus, and adjacent vessel wall. Coiled aneurysms showed enhanced patterns of thrombus organization and neointima formation, whereas those without treatment demonstrated heterogeneous patterns of thrombosis, thrombus recanalization, and aneurysm growth (p = 0.02). In coiled aneurysms, inflammation markers tended to accumulate inside the thrombus and in the neointima (p < 0.001). Endothelial cells accumulated directly in the neointima (p < 0.0001), and their presence was associated with complete aneurysm healing. The presence of proinflammatory cells plays a crucial role in aneurysm remodeling after coiling. Whereas thrombus organization is hallmarked by a pronounced intra-thrombotic inflammatory reaction, neointima maturation is characterized by direct invasion of endothelial cells. Knowledge concerning topographic distribution of regenerative inflammatory processes may pave the way for future treatment modalities which enhance aneurysm healing after endovascular therapy.

Sections du résumé

BACKGROUND BACKGROUND
Healing of intracranial aneurysms following endovascular treatment relies on the organization of early thrombus into mature scar tissue and neointima formation. Activation and deactivation of the inflammation cascade plays an important role in this process. In addition to timely evolution, its topographic distribution is hypothesized to be crucial for successful aneurysm healing.
METHODS METHODS
Decellularized saccular sidewall aneurysms were created in Lewis rats and coiled. At follow-up (after 3 days (n = 16); 7 days (n = 19); 21 days (n = 8)), aneurysms were harvested and assessed for healing status. In situ hybridization was performed for soluble inflammatory markers (IL6, MMP2, MMP9, TNF-α, FGF23, VEGF), and immunohistochemical analysis to visualize inflammatory cells (CD45, CD3, CD20, CD31, CD163, HLA-DR). These markers were specifically documented for five regions of interest: aneurysm neck, dome, neointima, thrombus, and adjacent vessel wall.
RESULTS RESULTS
Coiled aneurysms showed enhanced patterns of thrombus organization and neointima formation, whereas those without treatment demonstrated heterogeneous patterns of thrombosis, thrombus recanalization, and aneurysm growth (p = 0.02). In coiled aneurysms, inflammation markers tended to accumulate inside the thrombus and in the neointima (p < 0.001). Endothelial cells accumulated directly in the neointima (p < 0.0001), and their presence was associated with complete aneurysm healing.
CONCLUSION CONCLUSIONS
The presence of proinflammatory cells plays a crucial role in aneurysm remodeling after coiling. Whereas thrombus organization is hallmarked by a pronounced intra-thrombotic inflammatory reaction, neointima maturation is characterized by direct invasion of endothelial cells. Knowledge concerning topographic distribution of regenerative inflammatory processes may pave the way for future treatment modalities which enhance aneurysm healing after endovascular therapy.

Identifiants

pubmed: 37533024
doi: 10.1186/s12974-023-02863-1
pii: 10.1186/s12974-023-02863-1
pmc: PMC10394867
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

182

Subventions

Organisme : Forschungsrat des Kantonsspitals Aarau
ID : FR 1410.000.122

Informations de copyright

© 2023. The Author(s).

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Auteurs

Basil E Grüter (BE)

Division of Neuroradiology, Department of Radiology, Kantonsspital Aarau, C/o NeuroResearch Office,Tellstrasse 1, 5001, Aarau, Switzerland. basil.grueter@ksa.ch.
Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland. basil.grueter@ksa.ch.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland. basil.grueter@ksa.ch.

Gwendoline Canzanella (G)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Joshua Hägler (J)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Jeannine Rey (J)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Stefan Wanderer (S)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Michael von Gunten (M)

Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.
Institute of Pathology Laenggasse, Ittigen, Switzerland.

José A Galvan (JA)

Translational Research Unit (TRU), Institute of Pathology, University of Bern, Bern, Switzerland.

Rainer Grobholz (R)

Institute of Pathology, Kantonsspital Aarau, Aarau, Switzerland.
Medical Faculty, University of Zurich, Zurich, Switzerland.

Hans-Rudolf Widmer (HR)

Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Luca Remonda (L)

Division of Neuroradiology, Department of Radiology, Kantonsspital Aarau, C/o NeuroResearch Office,Tellstrasse 1, 5001, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Lukas Andereggen (L)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

Serge Marbacher (S)

Department of Neurosurgery, Kantonsspital Aarau, Aarau, Switzerland.
Program for Regenerative Neuroscience, Department for BioMedical Research, University of Bern, Bern, Switzerland.

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Classifications MeSH