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Article ; Online: Spatiotemporal profile of neutrophil extracellular trap formation in a mouse model of ischemic stroke.

De Wilde, Maaike / Desender, Linda / Tersteeg, Claudia / Vanhoorelbeke, Karen / De Meyer, Simon F

Research and practice in thrombosis and haemostasis

2022 Volume 7, Issue 1, Page(s) 100028

Abstract: Background: Thromboinflammatory processes modulate the complex pathophysiology of cerebral ischemia-reperfusion (I/R) injury in ischemic stroke, but the exact underlying mechanisms remain poorly understood. Emerging evidence indicates that neutrophil ... ...

Abstract	Background: Thromboinflammatory processes modulate the complex pathophysiology of cerebral ischemia-reperfusion (I/R) injury in ischemic stroke, but the exact underlying mechanisms remain poorly understood. Emerging evidence indicates that neutrophil extracellular traps (NETs) might play an important role in the thromboinflammatory cascade. In addition, the link between von Willebrand factor (VWF) and neutrophil recruitment in the ischemic brain might promote thromboinflammation, possibly by the formation of NETs. Objectives: To study NET formation in a murine model of cerebral I/R injury in ischemic stroke. Methods: The filament-induced transient middle cerebral artery occlusion model was used to induce 60 minutes of focal cerebral ischemia after which reperfusion was allowed. At different time points postischemia, NETs were identified in the ischemic mouse brain using quantitative immunofluorescence microscopy. Results: NETs could be identified in the ipsilateral brain hemisphere. Interestingly, NETs could already be detected at 6 hours poststroke. Their presence increased at 12 hours, was highest at 24 hours, and decreased again 48 hours postischemia. Remarkably, NETs were predominantly localized within the brain vasculature postischemia, suggesting that NETs play a role in secondary microthrombosis. Strikingly, NET formation was significantly decreased in VWF-deficient mice compared to littermate wild-type mice 24 hours postischemia, indicating a possible role for VWF in promoting NETosis in the ischemic brain. Conclusion: This study identified the spatiotemporal profile of NET formation in a mouse model of cerebral I/R injury in ischemic stroke. NETs, potentially in combination with VWF, might be attractive targets for the development of novel therapeutic strategies in ischemic stroke treatment.
Language	English
Publishing date	2022-12-23
Publishing country	United States
Document type	Journal Article
ISSN	2475-0379
ISSN (online)	2475-0379
DOI	10.1016/j.rpth.2022.100028
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Article ; Online: R-tPA Resistance Is Specific for Platelet-Rich Stroke Thrombi and Can Be Overcome by Targeting Nonfibrin Components.

Vandelanotte, Sarah / François, Olivier / Desender, Linda / Staessens, Senna / Vanhoorne, Alexander / Van Gool, Fréderick / Tersteeg, Claudia / Vanhoorelbeke, Karen / Vanacker, Peter / Andersson, Tommy / De Meyer, Simon F

Stroke

2024 Volume 55, Issue 5, Page(s) 1181–1190

Abstract: Background: Resistance to r-tPA (recombinant tissue-type plasminogen activator) is a well-known but poorly understood phenomenon that hampers successful recanalization in patients with acute ischemic stroke. Using clinically relevant thrombi from ... ...

Abstract	Background: Resistance to r-tPA (recombinant tissue-type plasminogen activator) is a well-known but poorly understood phenomenon that hampers successful recanalization in patients with acute ischemic stroke. Using clinically relevant thrombi from patients with acute ischemic stroke, we investigated if and how thrombus composition impacts r-tPA-mediated lysis. In addition, we explored strategies to overcome r-tPA resistance. Methods: Thrombi were split into 2 parts, 1 of which was used for thrombolysis and the other for detailed histological analysis. Thrombolysis was performed in normal human plasma using r-tPA alone, using r-tPA in combination with DNase-1 or using r-tPA in combination with N,N'-diacetyl-l-cystine. Thrombus lysis was calculated as the percentage of residual thrombus weight compared with its initial weight and the degree of lysis was linked to thrombus composition determined via histology. Results: Interestingly, we found that the efficacy of r-tPA-mediated thrombolysis was strongly correlated with the composition of the thrombi. Thrombi containing high amounts of red blood cells and low amounts of DNA and von Willebrand Factor were efficiently degraded by r-tPA, whereas thrombi containing low amounts of red blood cells and higher amounts of DNA and von Willebrand Factor were resistant to r-tPA. Importantly, combination of r-tPA with DNase-1 or N,N'-diacetyl-l-cystine significantly and specifically improved the lysis of these r-tPA-resistant thrombi. Conclusions: Using patient thrombus material, our results for the first time show that the composition of stroke thrombi largely determines their susceptibility to r-tPA-mediated thrombolysis. Red blood cell-poor thrombi have a specific resistance to r-tPA, which can be overcome by targeting nonfibrin components using DNase-1 or N,N'-diacetyl-l-cystine.
Language	English
Publishing date	2024-03-25
Publishing country	United States
Document type	Journal Article
ZDB-ID	80381-9
ISSN	1524-4628 ; 0039-2499 ; 0749-7954
ISSN (online)	1524-4628
ISSN	0039-2499 ; 0749-7954
DOI	10.1161/STROKEAHA.123.045880
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Article: Detailed histological analysis of a thrombectomy-resistant ischemic stroke thrombus: a case report.

Staessens, Senna / François, Olivier / Desender, Linda / Vanacker, Peter / Dewaele, Tom / Sciot, Raf / Vanhoorelbeke, Karen / Andersson, Tommy / De Meyer, Simon F

Thrombosis journal

2021 Volume 19, Issue 1, Page(s) 11

Abstract: Background: Mechanical removal of a thrombus by thrombectomy can be quite challenging. For reasons that are not fully understood, some thrombi require multiple passes to achieve successful recanalization, whereas other thrombi are efficiently removed in ...

Abstract	Background: Mechanical removal of a thrombus by thrombectomy can be quite challenging. For reasons that are not fully understood, some thrombi require multiple passes to achieve successful recanalization, whereas other thrombi are efficiently removed in a single pass. Since first pass success is associated with better clinical outcome, it is important to better understand the nature of thrombectomy resistant thrombi. The aim of this study was therefore to characterize the cellular and molecular composition of a thrombus that was very hard to retrieve via mechanical thrombectomy. Case presentation: In a patient that was admitted with a right middle cerebral artery M1-occlusion, 11 attempts using various thrombectomy devices and techniques were required for removal of the thrombus. This peculiar case provided a rare opportunity to perform an in-depth histopathological study of a difficult to retrieve thrombus. Thrombus material was histologically analyzed using hematoxylin and eosin, Martius Scarlet Blue stain (red blood cells and fibrin), Feulgen stain (DNA), von Kossa stain (calcifications) and immunohistochemical analysis of von Willebrand factor, platelets, leukocytes and neutrophil extracellular traps. Histological analysis revealed abnormally high amounts of extracellular DNA, leukocytes, von Willebrand factor and calcifications. Extracellular DNA stained positive for markers of leukocytes and NETs, suggesting that a significant portion of DNA is derived from neutrophil extracellular traps. Conclusion: In this unique case of a nearly thrombectomy-resistant stroke thrombus, our study showed an atypical composition compared to the common structural features found in ischemic stroke thrombi. The core of the retrieved thrombus consisted of extracellular DNA that colocalized with von Willebrand factor and microcalcifications. These results support the hypothesis that von Willebrand factor, neutrophil extracellular traps and microcalcifications contribute to mechanical thrombectomy resistance. Such information is important to identify novel targets in order to optimize technical treatment protocols and techniques to increase first pass success rates.
Language	English
Publishing date	2021-02-22
Publishing country	England
Document type	Journal Article
ISSN	1477-9560
ISSN	1477-9560
DOI	10.1186/s12959-021-00262-1
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Article: Unusual Histopathological Findings in Mechanically Removed Stroke Thrombi - A Multicenter Experience.

Aspegren, Oskar / Staessens, Senna / Vandelanotte, Sarah / Desender, Linda / Cordonnier, Charlotte / Puy, Laurent / Bricout, Nicolas / De Meyer, Simon F / Andersson, Tommy / Arnberg, Fabian

Frontiers in neurology

2022 Volume 13, Page(s) 846293

Abstract: Background: Several studies have investigated the histopathology of mechanically retrieved thrombi from stroke patients. Thrombi with unusual components constitute about 1-2% of all stroke thrombi in clinical practice. Knowledge about these rare ... ...

Abstract	Background: Several studies have investigated the histopathology of mechanically retrieved thrombi from stroke patients. Thrombi with unusual components constitute about 1-2% of all stroke thrombi in clinical practice. Knowledge about these rare components is limited. Objectives: To characterize the histopathology of unusual stroke thrombi from a real-world setting with relation to clinical presentation, patient characteristics and procedural aspects of mechanical thrombectomy. Methods: One-thousand and eight thrombi retrieved from stroke patients with mechanical thrombectomy at three different hospitals were retrospectively reviewed for unusual histological components. Fifteen thrombi were included in the study for further histopathological analysis. Clinical data and data on procedural aspects were collected. Results: We identified six cases with large amounts of extracellular DNA, of which three were calcified. All six cases except one received anticoagulant therapy. We describe two types of calcifications that differ with respect to general calcification morphology, von Kossa staining pattern, macrophage immunophenotype and presence of multinucleated giant cells. Cholesterol-rich ( Conclusion: In our retrospective multicenter study, we characterized stroke thrombi histopathologically and found subgroups of thrombi defined by presence of rarely seen components. These defined subgroups showed relation to underlying cardiovascular disease, patient characteristics, and mechanical thrombectomy technique. Knowledge about these components may increase our understanding of stroke pathophysiology and influence interventional procedures.
Language	English
Publishing date	2022-05-17
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564214-5
ISSN	1664-2295
ISSN	1664-2295
DOI	10.3389/fneur.2022.846293
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Article ; Online: Coculture Method to Obtain Endothelial Networks Within Human Tissue-Engineered Skeletal Muscle.

Gholobova, Dacha / Gerard, Melanie / Terrie, Lisanne / Desender, Linda / Shansky, Janet / Vandenburgh, Herman / Thorrez, Lieven

Methods in molecular biology (Clifton, N.J.)

2018 Volume 1889, Page(s) 169–183

Abstract: Skeletal muscle tissue engineering aims at creating functional skeletal muscle in vitro. Human muscle organoids can be used for potential applications in regenerative medicine, but also as an in vitro model for myogenesis or myopathology. However, the ... ...

Abstract	Skeletal muscle tissue engineering aims at creating functional skeletal muscle in vitro. Human muscle organoids can be used for potential applications in regenerative medicine, but also as an in vitro model for myogenesis or myopathology. However, the thickness of constructs is limited due to passive diffusion of nutrients and oxygen. Introduction of a vascular network in vitro may solve this limitation. Here, we describe tissue engineering of in vitro skeletal muscle consisting of human aligned myofibers with interspersed endothelial networks. To create bio-artificial muscle (BAM), human muscle progenitor cells are cocultured with human umbilical vein endothelial cells (HUVECs) in a fibrin hydrogel. The cell-gel mix is cast into silicone molds with end attachment sites and cultured in endothelial growth medium (EGM-2) for 1 week. The passive forces generated in the contracted hydrogel align the myogenic cells parallel to the long axis of the contracted gel such that they fuse into aligned multinucleated myofibers. This results in the formation of a 2 cm long and ~1.5 mm tick human BAM construct with endothelial networks.
MeSH term(s)	Biopsy ; Cells, Cultured ; Coculture Techniques ; Endothelial Cells/cytology ; Endothelial Cells/metabolism ; Human Umbilical Vein Endothelial Cells/cytology ; Human Umbilical Vein Endothelial Cells/metabolism ; Humans ; Muscle Development ; Muscle, Skeletal/cytology ; Muscle, Skeletal/metabolism ; Myoblasts/cytology ; Myoblasts/metabolism ; Tissue Engineering
Language	English
Publishing date	2018-10-23
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-8897-6_10
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Article ; Online: von Willebrand factor deficiency does not influence angiotensin II-induced abdominal aortic aneurysm formation in mice.

Portier, Irina / Martinod, Kimberly / Desender, Linda / Vandeputte, Nele / Deckmyn, Hans / Vanhoorelbeke, Karen / De Meyer, Simon F

Scientific reports

2018 Volume 8, Issue 1, Page(s) 16645

Abstract: Abdominal aortic aneurysm (AAA) refers to a localized dilation of the abdominal aorta that exceeds the normal diameter by 50%. AAA pathophysiology is characterized by progressive inflammation, vessel wall destabilization and thrombus formation. Our aim ... ...

Abstract	Abdominal aortic aneurysm (AAA) refers to a localized dilation of the abdominal aorta that exceeds the normal diameter by 50%. AAA pathophysiology is characterized by progressive inflammation, vessel wall destabilization and thrombus formation. Our aim was to investigate the potential involvement of von Willebrand factor (VWF), a thrombo-inflammatory plasma protein, in AAA pathophysiology using a dissection-based and angiotensin II infusion-induced AAA mouse model. AAA formation was induced in both wild-type and VWF-deficient mice by subcutaneous implantation of an osmotic pump, continuously releasing 1000 ng/kg/min angiotensin II. Survival was monitored, but no significant difference was observed between both groups. After 28 days, the suprarenal aortic segment of the surviving mice was harvested. Both AAA incidence and severity were similar in wild-type and VWF-deficient mice, indicating that AAA formation was not significantly influenced by the absence of VWF. Although VWF plasma levels increased after the infusion period, these increases were not correlated with AAA progression. Also detailed histological analyses of important AAA hallmarks, including elastic degradation, intramural thrombus formation and leukocyte infiltration, did not reveal differences between both groups. These data suggest that, at least in the angiotensin II infusion-induced AAA mouse model, the role of VWF in AAA pathophysiology is limited.
MeSH term(s)	Angiotensin II/toxicity ; Animals ; Aortic Aneurysm, Abdominal/chemically induced ; Aortic Aneurysm, Abdominal/metabolism ; Aortic Aneurysm, Abdominal/pathology ; Dilatation, Pathologic/chemically induced ; Dilatation, Pathologic/metabolism ; Dilatation, Pathologic/pathology ; Disease Models, Animal ; Inflammation/chemically induced ; Inflammation/metabolism ; Inflammation/pathology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Vasoconstrictor Agents/toxicity ; von Willebrand Factor/physiology
Chemical Substances	Vasoconstrictor Agents ; von Willebrand Factor ; Angiotensin II (11128-99-7)
Language	English
Publishing date	2018-11-09
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-018-35029-8
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Article ; Online: von Willebrand factor increases in experimental cerebral malaria but is not essential for late-stage pathogenesis in mice.

Kraisin, Sirima / Martinod, Kimberly / Desender, Linda / Pareyn, Inge / Verhenne, Sebastien / Deckmyn, Hans / Vanhoorelbeke, Karen / Van den Steen, Philippe E / De Meyer, Simon F

Journal of thrombosis and haemostasis : JTH

2020 Volume 18, Issue 9, Page(s) 2377–2390

Abstract: Background: Cerebral malaria (CM) is the most severe complication of malaria. Endothelial activation, cytokine release, and vascular obstruction are essential hallmarks of CM. Clinical studies have suggested a link between von Willebrand factor (VWF) ... ...

Abstract	Background: Cerebral malaria (CM) is the most severe complication of malaria. Endothelial activation, cytokine release, and vascular obstruction are essential hallmarks of CM. Clinical studies have suggested a link between von Willebrand factor (VWF) and malaria pathology. Objectives: To investigate the contribution of VWF in the pathogenesis of experimental cerebral malaria (ECM). Methods: Both Vwf Results: Plasma VWF levels significantly increased upon PbANKA infection in Vwf Conclusions: Our study suggests that increased VWF concentration is a hallmark of ECM. However, VWF does not have a major influence in modulating late-stage ECM pathogenesis.
MeSH term(s)	ADAMTS13 Protein/genetics ; Animals ; Blood Platelets ; Malaria, Cerebral ; Mice ; Plasmodium berghei ; Thrombocytopenia ; von Willebrand Factor
Chemical Substances	von Willebrand Factor ; ADAMTS13 Protein (EC 3.4.24.87)
Language	English
Publishing date	2020-08-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2112661-6
ISSN	1538-7836 ; 1538-7933
ISSN (online)	1538-7836
ISSN	1538-7933
DOI	10.1111/jth.14932
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Article ; Online: Structural analysis of ischemic stroke thrombi: histological indications for therapy resistance.

Staessens, Senna / Denorme, Frederik / Francois, Olivier / Desender, Linda / Dewaele, Tom / Vanacker, Peter / Deckmyn, Hans / Vanhoorelbeke, Karen / Andersson, Tommy / De Meyer, Simon F

Haematologica

2020 Volume 105, Issue 2, Page(s) 498–507

Abstract: Ischemic stroke is caused by a thromboembolic occlusion of cerebral arteries. Treatment is focused on fast and efficient removal of the occluding thrombus, ... ...

Abstract	Ischemic stroke is caused by a thromboembolic occlusion of cerebral arteries. Treatment is focused on fast and efficient removal of the occluding thrombus, either
MeSH term(s)	Brain Ischemia/therapy ; Humans ; Ischemic Stroke ; Stroke/therapy ; Thrombectomy ; Thrombosis/etiology ; Thrombosis/therapy
Language	English
Publishing date	2020-01-31
Publishing country	Italy
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2333-4
ISSN	1592-8721 ; 0017-6567 ; 0390-6078
ISSN (online)	1592-8721
ISSN	0017-6567 ; 0390-6078
DOI	10.3324/haematol.2019.219881
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Article ; Online: Thrombus formation during ECMO: Insights from a detailed histological analysis of thrombus composition.

Journal of thrombosis and haemostasis : JTH

2022 Volume 20, Issue 9, Page(s) 2058–2069

Abstract: Objectives: Intra-device thrombosis remains one of the most common complications during extracorporeal membrane oxygenation (ECMO). Despite anticoagulation, approximately 35% of patients develop thrombi in the membrane oxygenator, pump heads, or tubing. ...

Abstract	Objectives: Intra-device thrombosis remains one of the most common complications during extracorporeal membrane oxygenation (ECMO). Despite anticoagulation, approximately 35% of patients develop thrombi in the membrane oxygenator, pump heads, or tubing. The aim of this study was to describe the molecular and cellular features of ECMO thrombi and to study the main drivers of thrombus formation at different sites in the ECMO circuits. Approach and results: Thrombi (n = 85) were collected immediately after veno-arterial-(VA)-ECMO circuit removal from 25 patients: 23 thrombi from the pump, 25 from the oxygenator, and 37 from the tubing. Quantitative histological analysis was performed for the amount of red blood cells (RBCs), platelets, fibrin, von Willebrand factor (VWF), leukocytes, and citrullinated histone H3 (H3Cit). ECMO thrombi consist of a heterogenous composition with fibrin and VWF being the major thrombus components. A clustering analysis of the four major histological parameters identified two typical thrombus types: RBC-rich and RBC-poor/fibrin-rich thrombi with no significant differences in VWF and platelet content. Thrombus composition was not associated with the thrombus location, except for higher amounts of H3Cit that were found in pump and oxygenator thrombi compared to tubing samples. We observed higher blood leukocyte count and lactate dehydrogenase levels in patients with fibrin-rich thrombi. Conclusion: We found that thrombus composition is heterogenous, independent of their location, consisting of two types: RBC-rich and a fibrin-rich types. We also found that NETs play a minor role. These findings are important to improve current anticoagulation strategies in ECMO.
MeSH term(s)	Anticoagulants ; Extracorporeal Membrane Oxygenation/adverse effects ; Fibrin/analysis ; Humans ; Thrombosis ; von Willebrand Factor
Chemical Substances	Anticoagulants ; von Willebrand Factor ; Fibrin (9001-31-4)
Language	English
Publishing date	2022-07-03
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2112661-6
ISSN	1538-7836 ; 1538-7933
ISSN (online)	1538-7836
ISSN	1538-7933
DOI	10.1111/jth.15784
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Article ; Online: Neutrophil extracellular traps in ischemic stroke thrombi.

Laridan, Elodie / Denorme, Frederik / Desender, Linda / François, Olivier / Andersson, Tommy / Deckmyn, Hans / Vanhoorelbeke, Karen / De Meyer, Simon F

Annals of neurology

2017 Volume 82, Issue 2, Page(s) 223–232

Abstract: Objective: Neutrophil extracellular traps (NETs) have been shown to promote thrombus formation. Little is known about the exact composition of thrombi that cause ischemic stroke. In particular, no information is yet available on the presence of NETs in ... ...

Abstract	Objective: Neutrophil extracellular traps (NETs) have been shown to promote thrombus formation. Little is known about the exact composition of thrombi that cause ischemic stroke. In particular, no information is yet available on the presence of NETs in cerebral occlusions. Such information is, however, essential to improve current thrombolytic therapy with tissue plasminogen activator (t-PA). This study aimed at investigating the presence of neutrophils and more specifically NETs in ischemic stroke thrombi. Methods: Sixty-eight thrombi retrieved from ischemic stroke patients undergoing endovascular treatment were characterized by immunostaining using neutrophil markers (CD66b and neutrophil elastase) and NET markers (citrullinated histone H3 [H3Cit] and extracellular DNA). Neutrophils and NETs were quantified. In addition, extracellular DNA was targeted by performing ex vivo lysis of retrieved thrombi with DNase 1 and t-PA. Results: Neutrophils were detected extensively throughout all thrombi. H3Cit, a hallmark of NETs, was observed in almost all thrombi. H3Cit-positive area varied up to 13.45% of total thrombus area. Colocalization of H3Cit with extracellular DNA released from neutrophils confirmed the specific presence of NETs. H3Cit was more abundant in thrombi of cardioembolic origin compared to other etiologies. Older thrombi contained significantly more neutrophils and H3Cit compared to fresh thrombi. Interestingly, ex vivo lysis of patient thrombi was more successful when adding DNase 1 to standard t-PA. Interpretation: Neutrophils and NETs form important constituents of cerebral thrombi. Targeting of NETs with DNase 1 might have prothrombolytic potential in treatment of acute ischemic stroke. Ann Neurol 2017;82:223-232.
MeSH term(s)	Adolescent ; Adult ; Aged ; Aged, 80 and over ; Antigens, CD/metabolism ; Biomarkers ; Brain Ischemia/complications ; Brain Ischemia/metabolism ; Cell Adhesion Molecules/metabolism ; Cell Count/statistics & numerical data ; DNA/metabolism ; Extracellular Traps/metabolism ; Female ; GPI-Linked Proteins/metabolism ; Humans ; Leukocyte Elastase/metabolism ; Male ; Middle Aged ; Stroke/complications ; Stroke/metabolism ; Thrombosis/metabolism ; Young Adult
Chemical Substances	Antigens, CD ; Biomarkers ; CEACAM8 protein, human ; Cell Adhesion Molecules ; GPI-Linked Proteins ; DNA (9007-49-2) ; Leukocyte Elastase (EC 3.4.21.37)
Language	English
Publishing date	2017-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	80362-5
ISSN	1531-8249 ; 0364-5134
ISSN (online)	1531-8249
ISSN	0364-5134
DOI	10.1002/ana.24993
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Zs.MO 478: Show issues

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