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. 2024 Mar 18:71:102553.
doi: 10.1016/j.eclinm.2024.102553. eCollection 2024 May.

Decoding the historical tale: COVID-19 impact on haematological malignancy patients-EPICOVIDEHA insights from 2020 to 2022

Jon Salmanton-García  1   2   3 , Francesco Marchesi  4 , Francesca Farina  5 , Barbora Weinbergerová  6 , Federico Itri  7 , Julio Dávila-Valls  8 , Sonia Martín-Pérez  8 , Andreas Glenthøj  9 , Ditte Stampe Hersby  9 , Maria Gomes da Silva  10 , Raquel Nunes Rodrigues  10 , Alberto López-García  11 , Raúl Córdoba  11 , Yavuz M Bilgin  12 , Iker Falces-Romero  13   14 , Shaimaa El-Ashwah  15 , Ziad Emarah  15   16 , Caroline Besson  17   18 , Milena Kohn  17   18 , Jaap Van Doesum  19 , Emanuele Ammatuna  19 , Monia Marchetti  20 , Jorge Labrador  21 , Giovanni Paolo Maria Zambrotta  22   23 , Luisa Verga  22   23 , Ozren Jaksic  24 , Marcio Nucci  25 , Klára Piukovics  26 , Alba Cabirta-Touzón  27 , Moraima Jiménez  27 , Elena Arellano  28 , Ildefonso Espigado  28 , Ola Blennow  29 , Anna Nordlander  29 , Stef Meers  30 , Jens van Praet  31 , Tommaso Francesco Aiello  32 , Carolina Garcia-Vidal  32 , Nicola Fracchiolla  33 , Mariarita Sciumè  33 , Guldane Cengiz Seval  34 , Pavel Žák  35 , Caterina Buquicchio  36 , Carlo Tascini  37 , Stefanie K Gräfe  38 , Martin Schönlein  39 , Tatjana Adžić-Vukičević  40 , Valentina Bonuomo  41 , Chiara Cattaneo  42 , Summiya Nizamuddin  43 , Martin Čerňan  44 , Gaëtan Plantefeve  45 , Romane Prin  46 , Tomas Szotkovski  44 , Graham P Collins  47 , Michelina Dargenio  48 , Verena Petzer  49 , Dominik Wolf  49 , Natasha Čolović  50 , Lucia Prezioso  51 , Toni Valković  52   53   54 , Francesco Passamonti  55 , Gustavo-Adolfo Méndez  56 , Uluhan Sili  57 , Antonio Vena  58 , Martina Bavastro  58 , Alessandro Limongelli  58 , Rafael F Duarte  59 , Marie-Pierre Ledoux  60 , Milche Cvetanoski  61 , Zlate Stojanoski  61 , Marina Machado  62 , Josip Batinić  53   63   64 , Gabriele Magliano  65 , Monika M Biernat  66 , Nikola Pantić  67 , Christian Bjørn Poulsen  68 , Annarosa Cuccaro  69   70 , Maria Ilaria Del Principe  71 , Austin Kulasekararaj  72 , Irati Ormazabal-Vélez  73 , Alessandro Busca  74 , Fatih Demirkan  75 , Marriyam Ijaz  43 , Nikolai Klimko  76 , Igor Stoma  77 , Sofya Khostelidi  76 , Noemí Fernández  78 , Ali S Omrani  79 , Rui Bergantim  80 , Nick De Jonge  81 , Guillemette Fouquet  82 , Milan Navrátil  83 , Ghaith Abu-Zeinah  84 , Michail Samarkos  85 , Johan Maertens  86 , Cristina De Ramón  87 , Anna Guidetti  88 , Ferenc Magyari  89 , Tomás José González-López  90 , Tobias Lahmer  91 , Olimpia Finizio  92 , Natasha Ali  93 , László Imre Pinczés  89 , Esperanza Lavilla-Rubira  94 , Alessandra Romano  95 , Maria Merelli  37 , Mario Delia  96 , Maria Calbacho  97 , Joseph Meletiadis  98 , Darko Antić  67 , José-Ángel Hernández-Rivas  99 , Joyce Marques de Almeida  100 , Murtadha Al-Khabori  101 , Martin Hoenigl  102   103 , Maria Chiara Tisi  104 , Nina Khanna  105 , Aleksandra Barać  67 , Noha Eisa  106   107 , Roberta Di Blasi  108 , Raphaël Liévin  108 , Carolina Miranda-Castillo  109 , Nathan C Bahr  110 , Sylvain Lamure  111 , Mario Virgilio Papa  112 , Ayel Yahya  106 , Avinash Aujayeb  113 , Jan Novák  114 , Nurettin Erben  115 , María Fernández-Galán  116 , José-María Ribera-Santa Susana  117 , Ikhwan Rinaldi  118 , Rita Fazzi  119 , Monica Piedimonte  120 , Rémy Duléry  121 , Yung Gonzaga  122 , Andrés Soto-Silva  123 , Giuseppe Sapienza  124 , Alexandra Serris  125 , Ľuboš Drgoňa  126 , Ana Groh  127 , Laura Serrano  128 , Eleni Gavriilaki  129 , Athanasios Tragiannidis  129 , Juergen Prattes  130 , Nicola Coppola  131 , Vladimir Otašević  67 , Miloš Mladenović  40 , Mirjana Mitrović  67 , Bojana Mišković  132 , Pavel Jindra  133 , Sofia Zompi  74 , Maria Vittoria Sacchi  20 , Carolin Krekeler  134 , Maria Stefania Infante  99 , Daniel García-Bordallo  94 , Gökçe Melis Çolak  57 , Jiří Mayer  6 , Marietta Nygaard  68 , Michaela Hanáková  135   136 , Zdeněk Ráčil  135   136 , Matteo Bonanni  137   138 , Philipp Koehler  1   2 , Laman Rahimli  1   2 , Oliver A Cornely  1   2   3   139 , Livio Pagano  137   138 ; EPICOVIDEHA registry
Collaborators, Affiliations

Decoding the historical tale: COVID-19 impact on haematological malignancy patients-EPICOVIDEHA insights from 2020 to 2022

Jon Salmanton-García et al. EClinicalMedicine. .

Abstract

Background: The COVID-19 pandemic heightened risks for individuals with hematological malignancies due to compromised immune systems, leading to more severe outcomes and increased mortality. While interventions like vaccines, targeted antivirals, and monoclonal antibodies have been effective for the general population, their benefits for these patients may not be as pronounced.

Methods: The EPICOVIDEHA registry (National Clinical Trials Identifier, NCT04733729) gathers COVID-19 data from hematological malignancy patients since the pandemic's start worldwide. It spans various global locations, allowing comprehensive analysis over the first three years (2020-2022).

Findings: The EPICOVIDEHA registry collected data from January 2020 to December 2022, involving 8767 COVID-19 cases in hematological malignancy patients from 152 centers across 41 countries, with 42% being female. Over this period, there was a significant reduction in critical infections and an overall decrease in mortality from 29% to 4%. However, hospitalization, particularly in the ICU, remained associated with higher mortality rates. Factors contributing to increased mortality included age, multiple comorbidities, active malignancy at COVID-19 onset, pulmonary symptoms, and hospitalization. On the positive side, vaccination with one to two doses or three or more doses, as well as encountering COVID-19 in 2022, were associated with improved survival.

Interpretation: Patients with hematological malignancies still face elevated risks, despite reductions in critical infections and overall mortality rates over time. Hospitalization, especially in ICUs, remains a significant concern. The study underscores the importance of vaccination and the timing of COVID-19 exposure in 2022 for enhanced survival in this patient group. Ongoing monitoring and targeted interventions are essential to support this vulnerable population, emphasizing the critical role of timely diagnosis and prompt treatment in preventing severe COVID-19 cases.

Funding: Not applicable.

Keywords: COVID-19; Haematological malignancy; ICU; Immunosuppression; Vaccination.

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Conflict of interest statement

JSG has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Gilead, Menarini, and Pfizer; and has participated on a Data Safety Monitoring Board or Advisory Board for Pfizer, outside of the submitted work. FI has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Novartis, AbbVie, Gilead; and has received support for attending meetings and/or travel from Novartis, AbbVie, Gilead, Astellas, Pfizer, Sanofi, BMS, Alexion, Astra-Zeneca, outside of the submitted work. MGdS has received grants or contracts from AstraZeneca, consulting fees from Roche, Janssen Cilag, Gilead, and Abbvie; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Janssen; support for attending meetings and/or travel from Abbvie, Gilead, and Takeda; and participation on a Data Safety Monitoring Board or Advisory Board for Roche, Janssen Cilag, Lilly, Gilead, Takeda, and Abbvie, outside of the submitted work. ALG has received consulting fees from AstraZeneca; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Roche, Janssen, and Abbvie; and support for attending from meetings and/or travel from Astrazeneca, Janssen, and Beigene, outside of the submitted work. CGV has received grants or contracts from Ministerio de Sanidad y Consumo, Instituto de Salud Carlos III, payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Gilead Science, MSD, Pfizer, Jannsen, Novartis, Basilea, GSK, Shionogi, AbbVie, Advanz Pharma, and a grant support from Gilead Science, Pfizer, GSK, MSD and Pharmamar, outside of the submitted work. MM has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Pfizer, GILEAD, MSD, and ViiV Healthcare; and support for attending meetings and/or travel from Pfizer, Pharmamar, Tillotts Pharma, outside of the submitted work. SKG has received grants or contracts from Else Kröner-Fresenius-Stiftung iPRIME Scholarship (2021_EKPK.10), UKE, Hamburg, outside of the submitted work. AV has received consulting fees from MSD and Takeda; Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Gilead Pharma; and support for attending meetings and/or travel from Tillots, outside of the submitted work. TFA has received a pre-doctoral grant supported by the Ministerio de Sanidad y Consumo, Instituto de Salud Carlos III [RH RH042953], CM23/00277, outside of the submitted work. OAC has received grants or contracts from BMBF, Cidara, EU-DG RTD (101037867), F2G, Gilead, MedPace, MSD, Mundipharma, Octapharma, Pfizer, Scynexis; consulting fees from Abbvie, AiCuris, Biocon, Cidara, Gilead, IQVIA, Janssen, Matinas, MedPace, Menarini, Moderna, Molecular Partners, MSG-ERC, Noxxon, Octapharm, Pfizer, PSI, Scynexis, Seres; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Abbott, Abbvie, Al-Jazeera Pharmaceuticals/Hikma, Gilead, Grupo Biotoscana/United Medical/Knight, MedScape, MedUpdate, Merck/MSD, Noscendo, Pfizer, Shionogi, streamedup!; Payment for expert testimony from Cidara; a German patent (“Geschlossene Inkubationssysteme mit verbessertem Atemwegszugang für Untersuchungsvorrichtungen”, DE 10 2021 113 007.7), filed by the University of Cologne and listing Oliver A. Cornely as one of three inventors; Participation on a Data Safety Monitoring Board or Advisory Board from Boston Strategic Partners, Cidara, IQVIA, Janssen, MedPace, PSI, Pulmocide, Shionogi, The Prime Meridian Group; Stock or stock options from CoRe Consulting, EasyRadiology; and Other financial or non-financial interests from Wiley, outside of the submitted work. JM has received consulting fees from Takeda, F2G, and Mundipharma; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Takeda, F2G, and Mundipharma; and participation on a data safety monitoring board or advisory board from Takeda and Mundipharma, outside of the submitted work. JB has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Janseen, Takeda and Pfizer and support for attending meetings and/or travel from Janssen and Pfizer, outside of the submitted work. ASO has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Pfizer, Gilead, MSD, and BioMeriuex, outside of the submitted work. CDR has received grants or contracts from Asociación Española Contra el Cáncer: Code Grant: CLJUN18010DERA (01/10/18–30/11/22), outside of the submitted work. NK has received propatient research grant: Third Party Donor Registry for personalized antiviral T-Cell immunotherapeutics, no. pp 20–34; SNSF: Epstein–Barr virus-specific T memory stem cell therapy, Projektförderung (Abt. I-III), no. 204944, SNSF: NCCR AntiResist, no. 180541; consulting fees from MSD Sharp & Dome, Pfizer, Gilead Sciences, and Takeda; patents planes, issued or pending for corss protective epitopes of Aspergillus fumigatus and Candida albicans; participation on a data safety mornitoing board or advisory board or Idorsia and Pulmocide; and Leadership or fiduciary role in other board, society, committee or advocacy groups, paid or unpaid for Fungal Infection Network of Switzerland (FUNGINOS), outside of the submitted work. RDB has been conference speaker to Novartis, Kite/Gilead, Pfizer, Abbie, and Incyte; has received travel accommodation from Kite/Gilead; and has participated in Scientific advisory board for Novartis, Kite/Gilead, Janssen, and BMS, outside of the submitted work. JAHR has received grants or contracts from BMS/Celgene, Janssen, Sanofi, and GSK; Consulting fees from Janssen, Roche, Abbvie, Gilead, BMS/Celgene, Amgen, Takeda, Rovi, AstraZeneca, Sandoz Novartis, Celltrion, EusaPharm, Sanofi, Beigene, and Lilly; and payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Janssen, Roche, Abbvie, Gilead, BMS/Celgene, Amgen, Takeda, AstraZeneca, Beigene, Lilly, and GSK, outside of the submitted work. LD has received payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Pfizer; and support for attending meetings and/or travel from Pfizer, outside of the submitted work. PK has received grants from German Federal Ministry of Research and Education (BMBF) B-FAST (Bundesweites Forschungsnetz Angewandte Surveillance und Testung) and NAPKON (Nationales Pandemie Kohorten Netz, German National Pandemic Cohort Network) of the Network University Medicine (NUM) and the State of North Rhine-Westphalia; consulting fees from Ambu GmbH, Gilead Sciences, Mundipharma Resarch Limited, Noxxon N.V., Pfizer Pharma; payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from Akademie für Infektionsmedizin e.V., Ambu GmbH, Astellas Pharma, BioRad Laboratories Inc., European Confederation of Medical Mycology, Gilead Sciences, GPR Academy Ruesselsheim, HELIOS Kliniken GmbH, Jazz Pharmaceuticals Germany GmbH, medupdate GmbH, MedMedia GmbH, MSD Sharp & Dohme GmbH, Pfizer Pharma GmbH, Scilink Comunicación Científica SC and University Hospital, LMU Munich; A German patent application (“Geschlossene Intubationssysteme mit verbessertem Atemwegszugang für Untersuchungsvorrichtungen”, official file number DE 10 2021 113 007.7) has been filed by the University of Cologne; Participation on a Data Safety Monitoring Board or Advisory Board from Ambu GmbH, Gilead Sciences, Pfizer Pharma, Mundipharma Resarch Limited, Noxxon N.V.; and Other financial or non-financial interests from Elsevier, Wiley, outside of the submitted work. PJ has received Payment or honoraria for lectures, presentations, speakers bureaus, manuscript writing or educational events from GSK; Payment for expert testimony from Takeda; Support for attending meetings and/or travel from AstraZeneca, Novartis; and Participation on a Data Safety Monitoring Board or Advisory Board Takeda, BMS, outside of the submitted work. All authors had full access to the data and had final responsibility for the decision to submit for publication.

Figures

Fig. 1
Fig. 1
EPICOVIDEHA 2020–2022 patients: mortality per baseline malignancy, malignancy status at COVID-19 onset, and last malignancy treatment. A) 2020–2022 mortality per baseline malignancy. B) 2020–2022 mortality per malignancy status at COVID-19 onset. C) 2020–2022 mortality per last malignancy treatmentAllo, allogeneic; auto, autologous; CAR-T, chimeric antigen T cell receptors; HSCT, hematopoietic stem cell transplantation.
Fig. 1
Fig. 1
EPICOVIDEHA 2020–2022 patients: mortality per baseline malignancy, malignancy status at COVID-19 onset, and last malignancy treatment. A) 2020–2022 mortality per baseline malignancy. B) 2020–2022 mortality per malignancy status at COVID-19 onset. C) 2020–2022 mortality per last malignancy treatmentAllo, allogeneic; auto, autologous; CAR-T, chimeric antigen T cell receptors; HSCT, hematopoietic stem cell transplantation.
Fig. 2
Fig. 2
EPICOVIDEHA 2020–2022 patients: COVID-19 severity prevalence and mortality rate, overall mortality rate, mortality per malignancy status at COVID-19 onset, and mortality per reason for mortality. A) 2020–2022 COVID-19 severity prevalence. B) 2020–2022 mortality rate overall. C) 2020–2022 mortality rate per reason for mortality. COVID-19, coronavirus disease 2019. ∗Arrows in this figure indicate the date when the respective medical product was made available for the very first time in the world. This is applicable to some of the contributing institutions, not to them all.
Fig. 2
Fig. 2
EPICOVIDEHA 2020–2022 patients: COVID-19 severity prevalence and mortality rate, overall mortality rate, mortality per malignancy status at COVID-19 onset, and mortality per reason for mortality. A) 2020–2022 COVID-19 severity prevalence. B) 2020–2022 mortality rate overall. C) 2020–2022 mortality rate per reason for mortality. COVID-19, coronavirus disease 2019. ∗Arrows in this figure indicate the date when the respective medical product was made available for the very first time in the world. This is applicable to some of the contributing institutions, not to them all.
Fig. 3
Fig. 3
EPICOVIDEHA 2020–2022 patients: survival probability per diagnosis semester, vaccination status, and COVID-19 treatment. A) 2020–2022 survival probability per semester. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S8. B) 2020–2022 survival probability per vaccine doses before COVID-19. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S9. C) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 0 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗ No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S10. D) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 1–2 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S11. E) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 3+ vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S12.
Fig. 3
Fig. 3
EPICOVIDEHA 2020–2022 patients: survival probability per diagnosis semester, vaccination status, and COVID-19 treatment. A) 2020–2022 survival probability per semester. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S8. B) 2020–2022 survival probability per vaccine doses before COVID-19. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S9. C) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 0 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗ No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S10. D) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 1–2 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S11. E) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 3+ vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S12.
Fig. 3
Fig. 3
EPICOVIDEHA 2020–2022 patients: survival probability per diagnosis semester, vaccination status, and COVID-19 treatment. A) 2020–2022 survival probability per semester. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S8. B) 2020–2022 survival probability per vaccine doses before COVID-19. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S9. C) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 0 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗ No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S10. D) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 1–2 vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S11. E) 2020–2022 survival probability per vaccine doses before COVID-19 and COVID-19 treatment, 3+ vaccines. AVs, antivirals; MoABs, monoclonal antibodies. ∗No treatment includes patients that did not need to receive treatment mainly due to lack of symptoms. This figure has been replicated with the survival probability ranging from 70% to 100% in Supplementary Fig. S12.
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