Evidence map›Paper›PMID 33267656›Full record

ArticleArteriosclerosis, thrombosis, and vascular biology2021

Patients With COVID-19 Have Elevated Levels of Circulating Extracellular Vesicle Tissue Factor Activity That Is Associated With Severity and Mortality-Brief Report.

Axel Rosell, Sebastian Havervall, Fien von Meijenfeldt, Yohei Hisada, Katherina Aguilera, Steven P Grover, Ton Lisman, Nigel Mackman, Charlotte Thålin

Open access · greenAbstract read
In one paragraph

Article in Arteriosclerosis, thrombosis, and vascular biology, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 151 papers, 3 of them syntheses that pooled it.

0numbers the graph read from it
0cells of the map it votes in
151citing papers in PubMed, 3 pooled it
4.3field-weighted citation impact, top 4% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

151 citing papers in PubMed, 3 syntheses or guidelines pooled it, 218 citations in OpenAlex.

  1. Pooled it
  2. Pooled it
  3. Pooled it
  4. Trial
  5. Article
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  14. Microvesicle Tissue Factor Procoagulant Activity Is Elevated and Correlated With Disease Severity in Patients With Cirrhosis.Liver international : official journal of the International Association for the Study of the Liver · 2025
    Article
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  18. COVID-19: a vascular nightmare unfolding.Frontiers in immunology · 2025
    Review
  19. Article
  20. Article

91 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

9 authors at 3 institutions in 3 countries.

Axel Rosell *Division of Internal Medicine, Department of Clinical Sciences, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden (A.R., S.H., K.A., C.T.).
Sebastian Havervall *Division of Internal Medicine, Department of Clinical Sciences, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden (A.R., S.H., K.A., C.T.).
Fien von MeijenfeldtSurgical Research Laboratory, Department of Surgery, University of Groningen, University Medical Center Groningen, the Netherlands (F.v.M., T.L.).
Yohei HisadaUNC Blood Research Center, Division of Hematology, Department of Medicine, University of North Carolina at Chapel Hill (Y.H., S.P.G., N.M.).
Katherina AguileraDivision of Internal Medicine, Department of Clinical Sciences, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden (A.R., S.H., K.A., C.T.).
Steven P GroverUNC Blood Research Center, Division of Hematology, Department of Medicine, University of North Carolina at Chapel Hill (Y.H., S.P.G., N.M.).
Ton LismanSurgical Research Laboratory, Department of Surgery, University of Groningen, University Medical Center Groningen, the Netherlands (F.v.M., T.L.).
Nigel Mackman *UNC Blood Research Center, Division of Hematology, Department of Medicine, University of North Carolina at Chapel Hill (Y.H., S.P.G., N.M.).
Charlotte Thålin *Division of Internal Medicine, Department of Clinical Sciences, Karolinska Institutet, Danderyd Hospital, Stockholm, Sweden (A.R., S.H., K.A., C.T.).
Danderyds sjukhus · SEUniversity of North Carolina at Chapel Hill · USUniversity Medical Center Groningen · NL

Funding

Tissue factor-dependent coagulation in thrombosis and immune responsesR35HL155657 · NHLBI · UNIV OF NORTH CAROLINA CHAPEL HILL · PI Nigel Mackman · 2021 to 2026
$5.5M
Role of the Thrombin PAR-1 Pathway in Viral InfectionR01HL119523 · NHLBI · UNIV OF NORTH CAROLINA CHAPEL HILL · PI MACKMAN, NIGEL · 2013 to 2020
$3.0M
NHLBI NIH HHS R01 HL119523NHLBI NIH HHS R35 HL155657
6 · The paper itself

Abstract

objectivePatients with coronavirus disease 2019 (COVID-19) have a high rate of thrombosis. We hypothesized that severe acute respiratory syndrome coronavirus 2 infection leads to induction of TF (tissue factor) expression and increased levels of circulating TF-positive extracellular vesicles (EV) that may drive thrombosis. Approach and Results: We measured levels of plasma EV TF activity in 100 patients with COVID-19 with moderate and severe disease and 28 healthy controls. Levels of EV TF activity were significantly higher in patients with COVID-19 compared with controls. In addition, levels of EV TF activity were associated with disease severity and mortality. Finally, levels of EV TF activity correlated with several plasma markers, including D-dimer, which has been shown to be associated with thrombosis in patients with COVID-19.

conclusionsOur results indicate that severe acute respiratory syndrome coronavirus 2 infection induces the release of TF-positive EVs into the circulation that are likely to contribute to thrombosis in patients with COVID-19. EV TF activity was also associated with severity and mortality.

Indexed as

AgedAnticoagulantsCOVID-19Extracellular VesiclesFemaleHumansMaleMiddle AgedSARS-CoV-2Severity of Illness IndexThrombosisAnticoagulantscoronavirusCOVID-19extracellular vesiclesfibrinogenthrombosis

Identifiers

PMID33267656
PMCPMC7837685
OpenAlexW3110426240

What OpenQuestion holds

Textmetadata
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.