Evidence map›Paper›PMID 36028857›Full record

ArticleJournal of hematology & oncology2022

Thrombotic and bleeding complications in patients with chronic lymphocytic leukemia and severe COVID-19: a study of ERIC, the European Research Initiative on CLL.

Darko Antic, Natasa Milic, Thomas Chatzikonstantinou, Lydia Scarfò, Vladimir Otasevic, Nina Rajovic, David Allsup, Alejandro Alonso Cabrero, Martin Andres, Monica Baile Gonzales and 91 more

Open access · goldAbstract readMulticenter Study
In one paragraph

Article in Journal of hematology & oncology, 2022. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 9 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
9citing papers in PubMed, 1 pooled it
1.4field-weighted citation impact, top 18% 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

9 citing papers in PubMed, 1 synthesis or guideline pooled it, 9 citations in OpenAlex.

  1. Pooled it
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  5. Review
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

101 authors at 20 institutions in 22 countries.

Darko AnticLymphoma Center, Clinic for Hematology, University Clinical Center of Serbia, Belgrade, Serbia. darko.antic1510976@gmail.com.
Natasa MilicDepartment of Medical Statistics and Informatics, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
Thomas ChatzikonstantinouHematology Department and HCT Unit, G. Papanicolaou Hospital, Thessaloniki, Greece.
Lydia ScarfòUniversità Vita-Salute San Raffaele and IRCC Ospedale San Raffaele, Milan, Italy.
Vladimir OtasevicLymphoma Center, Clinic for Hematology, University Clinical Center of Serbia, Belgrade, Serbia.
Nina RajovicDepartment of Medical Statistics and Informatics, Faculty of Medicine, University of Belgrade, Belgrade, Serbia.
David AllsupCentre for Atherothrombosis and Metabolic Disease, Hull York Medical School, Hull, UK.
Alejandro Alonso CabreroHaematology Department, Hospital Universitario de La Princesa, Madrid, Spain.
Martin AndresDepartment of Hematology and Central Hematology Laboratory, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.
Monica Baile GonzalesHematology Department, University Hospital of Salamanca-IBSAL, Salamanca, Spain.
Antonella CapassoIRCSS Ospedale San Raffaele, Milan, Italy.
Rosa ColladoDepartment of Hematology, Hospital General Universitario, Valencia, Spain.
Raul CordobaDepartment of Hematology, Health Research Institute IIS-FJD, Fundacion Jimenez Diaz University Hospital, Madrid, Spain.
Carolina Cuéllar-GarcíaHematology Unit Terrassa Hospital, Terrassa, Spain.
Juan Gonzalo CorreaHospital Clínic de Barcelona, Barcelona, Spain.
Lorenzo De PaoliDivision of Internal Medicine, Hematology Unit, ASL Vercelli, Vercelli, Italy.
Maria Rosaria De PaolisUOC Ematologia PO Vito Fazzi Lecce, Lecce, Italy.
Giovanni Del PoetaDepartment of Biomedicine and Prevention Hematology, University Tor Vergata, Rome, Italy.
Maria Dimou1st Internal Medicine Department, Propaedeutic, Hematology Clinical Trial Unit, National and Kapodistrian University of Athens, Athens, Greece.
Michael DoubekDepartment of Internal Medicine - Hematology and Oncology, University Hospital, Brno, Czechia.
Maria EfstathopoulouDepartment of Haematology Athens Medical Center-Psychikon Branch, Athens, Greece.
Shaimaa El-AshwahClinical Hematology Unit, Oncology Center, Faculty of Medicine, Mansoura University, Mansoura, 35516, Egypt.
Alicia EnricoHospital Italiano La Plata, La Plata, Argentina.
Blanca EspinetDepartment of Hematology, Hospital del Mar, Barcelona, Spain.
Lucia FarinaHematology, Fondazione IRCCS Istituto Nazionale Tumori, Milan, Italy.
Angela FerrariHematology Unit, Azienda Unità Sanitaria Locale - IRCCS, Reggio Emilia, Italy.
Myriam FogliettaSC Ematologia, AO S. Croce e Carle, Cuneo, Italy.
Alberto Lopez-GarciaDepartment of Hematology, Health Research Institute IIS-FJD, Fundacion Jimenez Diaz University Hospital, Madrid, Spain.
José A García-MarcoHematology Department, Hospital Universitario Puerta de Hierro-Majadahonda, Madrid, Spain.
Rocío García-SerraDepartment of Hematology, Hospital General Universitario, Valencia, Spain.
Massimo GentileHematology Unit AO Cosenza, Cosenza, Italy.
Eva GimenoDepartment of Hematology, Hospital del Mar, Barcelona, Spain.
Maria Gomes da SilvaHematology Department, Portuguese Institute of Oncology Lisbon, Lisbon, Portugal.
Odit GutweinDepartment of Hematology, Shamir Medical Center, Zerifin, Israel.
Yervand K HakobyanHematology Center after Prof. Yeolyan MH RA, Yerevan, Armenia.
Yair HerishanuDepartment of Hematology, Tel Aviv Sourasky Medical Center and Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel.
José Ángel Hernández-RivasDepartment of Hematology, Infanta Leonor University Hospital, Madrid, Spain.
Tobias HeroldLaboratory for Leukemia Diagnostics, Department of Medicine III, University Hospital, LMU Munich, Munich, Germany.
Gilad ItchakiDivision of Hematology, Rabin Medical Center, Petah Tikva, and the Sackler School of Medicine, Tel-Aviv University, Tel Aviv, Israel.
Ozren JaksicDepartment of Hematology, University Hospital Dubrava, Zagreb, Croatia.
Ann JanssensDepartment of Hematology, Universitaire Ziekenhuizen Leuven, Leuven, Belgium.
Olga B KalashnikovaFederal State Budgetary Educational Institution of Higher Education Academician I.P. Pavlov, First St. Petersburg State Medical University of the Ministry of Healthcare of Russian Federation, St. Petersburg, Russia.
Elżbieta KalicińskaDepartment and Clinic of Hematology, Blood Neoplasms and Bone Marrow Transplantation, Wroclaw Medical University, Pasteura Street 4, 50-367, Wrocław, Poland.
Arnon P KaterDepartment of Hematology, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands.
Sabina KerstingDepartment of Hematology, Haga Teaching Hospital, The Hague, The Netherlands.
Maya Koren-MichowitzDepartment of Hematology, Shamir Medical Center, Zerifin, Israel.
Jorge LabradorHematology Department, Unit Research, Complejo Asistencial Universitario de Burgos, Burgos, Spain.
Deepesh LadDepartment of Internal Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh, India.
Luca LaurentiSezione di Ematologia, Dipartimento di Scienze Radiologiche ed Ematologiche, Università Cattolica del Sacro Cuore, Rome, Italy.
Alberto FresaSezione di Ematologia, Dipartimento di Scienze Radiologiche ed Ematologiche, Università Cattolica del Sacro Cuore, Rome, Italy.
Mark-David LevinDepartment of Internal Medicine, Albert Schweitzer Hospital, Dordrecht, The Netherlands.
Carlota Mayor BastidaHaematology Department, Hospital Universitario de La Princesa, Madrid, Spain.
Lara MalerbaHematology and Stem Cell Transplant Center Marche Nord Hospital, Pesaro, Italy.
Roberto MarascaSection of Hematology, Department of Medical Sciences, University of Modena and Reggio E., Modena, Italy.
Monia MarchettiHematology Unit & TMO Center, AO SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy.
Juan MarquetHematology Department, Ramón y Cajal University Hospital, Madrid, Spain.
Biljana MihaljevicLymphoma Center, Clinic for Hematology, University Clinical Center of Serbia, Belgrade, Serbia.
Ivana MilosevicClinical Centre of Vojvodina, Faculty of Medicine, University of Novi Sad, Novi Sad, Serbia.
Fatima MirásHematology Department, Hospital Universitario 12de Octubre, Madrid, Spain.
Marta MorawskaExperimental Hematooncology Department, Medical University of Lublin, Lublin, Poland.
Marina MottaS.C. Ematologia ASST Spedali Civili Brescia, Brescia, Italy.
Talha MunirConsultant Haematologist, St James's Hospital, Leeds, LS9 7TF, UK.
Roberta MurruHematology and Stem Cell Transplantation Unit, Ospedale Oncologico A. Businco, ARNAS "G. Brotzu", Cagliari, Italy.
Raquel NunesHematology Department, Portuguese Institute of Oncology Lisbon, Lisbon, Portugal.
Jacopo OlivieriHematology Clinic, ASUFC, Udine, Italy.
Miguel Arturo PavlovskyFUNDALEU, Clinical Research Center Buenos Aires, Buenos Aires, Argentina.
Inga PiskunovaConsultative Hematology Department with a Day Hospital for Intensive High-Dose Chemotherapy, National Research Center for Hematology, Moscow, Russia.
Viola Maria PopovHematology Department, Colentina Clinical Hospital, Bucharest, Romania.
Francesca Maria QuagliaDepartment of Medicine, Section of Hematology, University of Verona, Verona, Italy.
Giulia QuaresminiHematology, ASST Papa Giovanni XXIII, Bergamo, Italy.
Gianluigi RedaHematology Unit, Foundation IRCCS Ca' Granda Ospedale Maggiore Policlinico of Milan, Milan, Italy.
Gian Matteo RigolinSt. Anna University Hospital, Ferrara, Italy.
Amit ShresthaHematology Unit, Nepal Cancer Hospital and Research Center, Lalitpur, Nepal.
Martin Šimkovič4th Department of Internal Medicine - Haematology, Faculty of Medicine in Hradec Králové, University Hospital and Charles University in Prague, Hradec Kralove, Czech Republic.
Svetlana SmirnovaConsultative Hematology Department with a Day Hospital for Intensive High-Dose Chemotherapy, National Research Center for Hematology, Moscow, Russia.
Martin Špaček1st Department of Medicine - Hematology, First Faculty of Medicine, Charles University and General Hospital in Prague, Prague, Czech Republic.
Paolo SportolettiDepartment of Medicine and Surgery, Institute of Hematology and Center for Hemato-Oncological Research, Ospedale S. Maria della Misericordia, Perugia, Italy.
Oana StancaHematology Department from Coltea Clinical Hospital, "Carol Davila" University of Medicine and Pharmacy, Bucharest, Romania.
Niki StavroyianniHematology Department and HCT Unit, G. Papanicolaou Hospital, Thessaloniki, Greece.
Doreen Te RaaDepartment of Hematology, Gelderse Vallei Ede, Ede, The Netherlands.
Kristina TomicLymphoma Center, Clinic for Hematology, University Clinical Center of Serbia, Belgrade, Serbia.
Sanne ToninoDepartment of Hematology, Lymmcare, Cancer Center Amsterdam, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, The Netherlands.
Livio TrentinHematology and Clinical Immunology Unit, Department of Medicine, University of Padova, Padua, Italy.
Ellen Van Der SpekDepartment of Internal Medicine, Rijnstate Hospital, Arnhem, The Netherlands.
Michel van GelderDepartment Internal Medicine, Maastricht University Medical Center, Maastricht, The Netherlands.
Marzia VarettoniDivision of Hematology, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
Andrea VisentinHematology and Clinical Immunology Unit, Department of Medicine, University of Padova, Padua, Italy.
Candida VitaleDivision of Hematology, A.O.U. Cittàdella Salute e della Scienza di Torino and Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin, Italy.
Vojin VukovicLymphoma Center, Clinic for Hematology, University Clinical Center of Serbia, Belgrade, Serbia.
Ewa Wasik-SzczepanekDepartment Hematooncology and Bone Marrow Transplantation, Medical University in Lublin, Lublin, Poland.
Tomasz WróbelDepartment and Clinic of Hematology, Blood Neoplasms and Bone Marrow Transplantation, Wroclaw Medical University, Pasteura Street 4, 50-367, Wrocław, Poland.
Lucrecia Yáñez San SegundoUniversity Hospital and Research Institute of Marqués de Valdecilla (IDIVAL), Santander, Spain.
Mohamed YassinHematology Section, Department of Medical Oncology, National Center for Cancer Care and Research, Doha, Qatar.
Marta CosciaDivision of Hematology, A.O.U. Cittàdella Salute e della Scienza di Torino and Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin, Italy.
Alessandro RambaldiHematology, ASST Papa Giovanni XXIII, Bergamo, Italy.
Emili MontserratHospital Clínic de Barcelona, Barcelona, Spain.
Robin FoàHematology, Department of Translational and Precision Medicine, Sapienza University, Rome, Italy.
Antonio CuneoSt. Anna University Hospital, Ferrara, Italy.
Marc CarrierDepartment of Medicine, Ottawa Hospital Research Institute, University of Ottawa, Ottawa, ON, K1H 8L6, Canada.
Paolo Ghia *Università Vita-Salute San Raffaele and IRCC Ospedale San Raffaele, Milan, Italy.
Kostas Stamatopoulos *Institute of Applied Biosciences, Centre for Research and Technology Hellas, Thessaloniki, Greece.
Tel Aviv University · ILUniversity of Belgrade · RSCentre for Research and Technology Hellas · GRFederal State Institution Hematology Research Center · RUHospital Clínic de Barcelona · ESHospital Del Mar · ESHospital General Universitario De Valencia · ESHospital Universitario Fundación Jiménez Díaz · ESInstituto Português de Oncologia Francisco Gentil · PTIRCCS Ospedale San Raffaele · ITIstituti di Ricovero e Cura a Carattere Scientifico · ITMedical University of Lublin · PLOspedale Papa Giovanni XXIII · ITUniversity of Padua · ITUniversity of Turin · ITWroclaw Medical University · PLAlbert Schweitzer Ziekenhuis · NLAmsterdam University Medical Centers · NLAthens Medical Center · GRAzienda Ospedaliera di Cosenza · IT

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

Abstract

backgroundPatients with chronic lymphocytic leukemia (CLL) may be more susceptible to COVID-19 related poor outcomes, including thrombosis and death, due to the advanced age, the presence of comorbidities, and the disease and treatment-related immune deficiency. The aim of this study was to assess the risk of thrombosis and bleeding in patients with CLL affected by severe COVID-19.

methodsThis is a retrospective multicenter study conducted by ERIC, the European Research Initiative on CLL, including patients from 79 centers across 22 countries. Data collection was conducted between April and May 2021. The COVID-19 diagnosis was confirmed by the real-time polymerase chain reaction (RT-PCR) assay for SARS-CoV-2 on nasal or pharyngeal swabs. Severe cases of COVID-19 were defined by hospitalization and the need of oxygen or admission into ICU. Development and type of thrombotic events, presence and severity of bleeding complications were reported during treatment for COVID-19. Bleeding events were classified using ISTH definition. STROBE recommendations were used in order to enhance reporting.

resultsA total of 793 patients from 79 centers were included in the study with 593 being hospitalized (74.8%). Among these, 511 were defined as having severe COVID: 162 were admitted to the ICU while 349 received oxygen supplementation outside the ICU. Most patients (90.5%) were receiving thromboprophylaxis. During COVID-19 treatment, 11.1% developed a thromboembolic event, while 5.0% experienced bleeding. Thrombosis developed in 21.6% of patients who were not receiving thromboprophylaxis, in contrast to 10.6% of patients who were on thromboprophylaxis. Bleeding episodes were more frequent in patients receiving intermediate/therapeutic versus prophylactic doses of low-molecular-weight heparin (LWMH) (8.1% vs. 3.8%, respectively) and in elderly. In multivariate analysis, peak D-dimer level and C-reactive protein to albumin ratio were poor prognostic factors for thrombosis occurrence (OR = 1.022, 95%CI 1.007‒1.038 and OR = 1.025, 95%CI 1.001‒1.051, respectively), while thromboprophylaxis use was protective (OR = 0.199, 95%CI 0.061‒0.645). Age and LMWH intermediate/therapeutic dose administration were prognostic factors in multivariate model for bleeding (OR = 1.062, 95%CI 1.017-1.109 and OR = 2.438, 95%CI 1.023-5.813, respectively).

conclusionsPatients with CLL affected by severe COVID-19 are at a high risk of thrombosis if thromboprophylaxis is not used, but also at increased risk of bleeding under the LMWH intermediate/therapeutic dose administration.

Indexed as

COVID-19 Drug TreatmentLeukemia, Lymphocytic, Chronic, B-CellThrombosisVenous ThromboembolismAgedAnticoagulantsCOVID-19 TestingHemorrhageHeparin, Low-Molecular-WeightHumansSARS-CoV-2AnticoagulantsHeparin, Low-Molecular-WeightAgeAnticoagulation therapyBleedingCLLCOVID-19D-dimerLMWHThromboprophylaxisThrombosis

Identifiers

PMID36028857
PMCPMC9415249
OpenAlexW4293125198

What Socratic holds

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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 Socratic graph.