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November 23, 2021; 97 (21) Research Article

Cerebral Venous Sinus Thrombosis and Thrombotic Events After Vector-Based COVID-19 Vaccines

A Systematic Review and Meta-analysis

Lina Palaiodimou, Maria-Ioanna Stefanou, Aristeidis H. Katsanos, View ORCID ProfileDiana Aguiar de Sousa, Jonathan M. Coutinho, Pagona Lagiou, Ioannis Michopoulos, Androniki Naska, View ORCID ProfileSotirios Giannopoulos, Konstantinos Vadikolias, Konstantinos I. Voumvourakis, Vasiliki Papaevangelou, Theodoros I. Vassilakopoulos, Sotirios Tsiodras, Georgios Tsivgoulis
First published October 5, 2021, DOI: https://doi.org/10.1212/WNL.0000000000012896
Lina Palaiodimou
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Maria-Ioanna Stefanou
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Aristeidis H. Katsanos
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Diana Aguiar de Sousa
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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  • ORCID record for Diana Aguiar de Sousa
Jonathan M. Coutinho
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Pagona Lagiou
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Ioannis Michopoulos
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Androniki Naska
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Sotirios Giannopoulos
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Konstantinos Vadikolias
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Konstantinos I. Voumvourakis
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Vasiliki Papaevangelou
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Theodoros I. Vassilakopoulos
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Sotirios Tsiodras
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Georgios Tsivgoulis
From the Second Department of Neurology (L.P., M.-I.S., A.H.K., S.G., K.I.V., G.T.), Second Department of Psychiatry (I.M.), and Fourth Department of Internal Medicine (S.T.), “Attikon” University Hospital, Department of Hygiene, Epidemiology and Medical Statistics (P.L., A.N.), School of Medicine, and Third Department of Critical Care Medicine, Evgenideio Hospital, Medical School (T.I.V.), and Third Department of Pediatrics (V.P.), National and Kapodistrian University of Athens, Greece; Division of Neurology (A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Canada; Department of Neurosciences and Mental Health (D.A.d.S.), Hospital de Santa Maria, CHULN, University of Lisbon, Portugal; Department of Neurology (J.M.C.), Amsterdam UMC, University of Amsterdam, the Netherlands; Department of Epidemiology (P.L.), Harvard T.H. Chan School of Public Health, Boston, MA; Department of Neurology (K.V.), University Hospital of Alexandroupolis, Democritus University of Thrace; Hellenic Centre for Disease Control and Prevention (S.T.), Athens, Greece; and Department of Neurology (G.T.), University of Tennessee Health Science Center, Memphis.
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Cerebral Venous Sinus Thrombosis and Thrombotic Events After Vector-Based COVID-19 Vaccines
A Systematic Review and Meta-analysis
Lina Palaiodimou, Maria-Ioanna Stefanou, Aristeidis H. Katsanos, Diana Aguiar de Sousa, Jonathan M. Coutinho, Pagona Lagiou, Ioannis Michopoulos, Androniki Naska, Sotirios Giannopoulos, Konstantinos Vadikolias, Konstantinos I. Voumvourakis, Vasiliki Papaevangelou, Theodoros I. Vassilakopoulos, Sotirios Tsiodras, Georgios Tsivgoulis
Neurology Nov 2021, 97 (21) e2136-e2147; DOI: 10.1212/WNL.0000000000012896

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Abstract

Background and Objectives There is accumulating evidence supporting an association between the thrombosis and thrombocytopenia syndrome (TTS) and adenovirus vector-based vaccines against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Yet TTS and TTS-associated cerebral venous sinus thrombosis (CVST) remain poorly characterized. We aim to systematically evaluate the proportion of CVST among TTS cases and assess its characteristics and outcomes.

Methods We performed a systematic review and meta-analysis of clinical trials, cohorts, case series, and registry-based studies with the aim to assess (1) the pooled mortality rate of CVST, TTS-associated CVST, and TTS and (2) the pooled proportion of patients with CVST among patients with any thrombotic event and TTS. Secondary outcomes comprised clinical characteristics of patients with postvaccination thrombotic event. This meta-analysis is reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines and was written according to the Meta-analysis of Observational Studies in Epidemiology proposal.

Results Sixty-nine studies were included in the qualitative analysis comprising 370 patients with CVST out of 4,182 patients with any thrombotic event associated with SARS-CoV-2 vector-based vaccine administration. Twenty-three studies were included further in quantitative meta-analysis. Among TTS cases, the pooled proportion of CVST was 51% (95% confidence interval [CI] 36%–66%; I2 = 61%). TTS was independently associated with a higher likelihood of CVST when compared to patients without TTS with thrombotic events after vaccination (odds ratio 13.8; 95% CI 2.0–97.3; I2 = 78%). The pooled mortality rates of TTS and TTS-associated CVST were 28% (95% CI 21%–36%) and 38% (95% CI 27%–49%), respectively. Thrombotic complications developed within 2 weeks of exposure to vector-based SARS-CoV-2 vaccines (mean interval 10 days; 95% CI 8–12) and affected predominantly women (69%; 95% CI 60%–77%) under age 45, even in the absence of prothrombotic risk factors.

Discussion Approximately half of patients with TTS present with CVST; almost one-third of patients with TTS do not survive. Further research is required to identify independent predictors of TTS following adenovirus vector-based vaccination.

Registration Information The prespecified study protocol has been registered in the International Prospective Register of Ongoing Systematic Reviews PROSPERO (CRD42021250709).

Glossary

CI=
confidence interval;
COVID-19=
coronavirus disease 2019;
CVST=
cerebral venous sinus thromboses;
HIT=
heparin-induced thrombocytopenia;
PF4-Abs=
platelet-activating antiplatelet factor 4 antibodies;
SARS-CoV-2=
severe acute respiratory syndrome coronavirus 2;
TTS=
thrombosis and thrombocytopenia syndrome

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.

  • ↵* L. Palaiodimou and M.-I. Stefanou contributed equally to this work as co–first authors.

  • COVID-19 Resources: NPub.org/COVID19

  • Received June 28, 2021.
  • Accepted in final form September 20, 2021.
  • © 2021 American Academy of Neurology
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    • References
  • Figures & Data
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