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September 27, 2022; 99 (13) Research Article

Association of Thrombin Generation With Leukocyte Inflammatory Profile in Patients With Acute Ischemic Stroke

View ORCID ProfileSarina Falcione, Danielle Munsterman, Twinkle Joy, View ORCID ProfileJoseph Kamtchum-Tatuene, Gina Sykes, Glen Jickling
First published July 5, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200909
Sarina Falcione
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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  • ORCID record for Sarina Falcione
Danielle Munsterman
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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Twinkle Joy
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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Joseph Kamtchum-Tatuene
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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Gina Sykes
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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Glen Jickling
From the Division of Neurology (S.F., D.M., T.J., G.S., G.J.), Department of Medicine, and Neuroscience and Mental Health Institute (J.K.-T.), Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada.
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Association of Thrombin Generation With Leukocyte Inflammatory Profile in Patients With Acute Ischemic Stroke
Sarina Falcione, Danielle Munsterman, Twinkle Joy, Joseph Kamtchum-Tatuene, Gina Sykes, Glen Jickling
Neurology Sep 2022, 99 (13) e1356-e1363; DOI: 10.1212/WNL.0000000000200909

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Abstract

Background and Objectives Thrombosis is central to the pathogenesis of acute ischemic stroke, with higher thrombin generation being associated with increased stroke risk. The immune system may contribute to thrombin generation in stroke and thus may offer novel strategies for stroke prevention. This study addresses the research question regarding the relationship of thrombin generation to leukocyte gene expression in patients with acute ischemic stroke.

Methods We isolated RNA from whole blood and examined the relationship to thrombin generation capacity in patients with acute ischemic stroke. Due to its effects on thrombin generation, patients on anticoagulants were excluded from the study. The relationship of gene expression with peak thrombin was evaluated by analysis of covariance across peak thrombin quartiles adjusted for sex and age.

Results In 97 patients with acute ischemic stroke, peak thrombin was variable, ranging from 252.0 to 752.4 nM. Increased peak thrombin was associated with differences in thromboinflammatory leukocyte gene expression, including a decrease in ADAM metallopeptidase with thrombospondin type 1 motif 13 and an increase in nuclear factor κB (NF-κB)–activating protein, protein disulfide isomerase family A member 5, and tissue factor pathway inhibitor 2. Pathways associated with peak thrombin included interleukin 6 signaling, thrombin signaling, and NF-κB signaling. A linear discriminant analysis model summarizing the immune activation associated with peak thrombin in a first cohort of stroke could distinguish patients with low peak thrombin from high peak thrombin in a second cohort of 112 patients with acute ischemic stroke.

Discussion The identified genes and pathways support a role of the immune system contributing to thrombus formation in patients with stroke. These may have relevance to antithrombotic strategies for stroke prevention.

Glossary

ADAMTS13=
ADAM metallopeptidase with thrombospondin type 1 motif 13;
FVIIa=
coagulation factor VIIa;
FX=
coagulation factor X;
IL=
interleukin;
LDA=
linear discriminant analysis;
NF-κB=
nuclear factor κB;
NKAP=
NF-κB–activating protein;
PDI=
protein disulfide isomerase;
PDIA5=
protein disulfide isomerase family A member 5;
TFPI2=
tissue factor pathway inhibitor 2

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editor was Brad Worrall, MD, MSc, FAAN.

  • Received December 3, 2021.
  • Accepted in final form May 16, 2022.
  • © 2022 American Academy of Neurology
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