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Outcomes of the SARS-CoV-2 omicron (B.1.1.529) variant outbreak among vaccinated and unvaccinated patients with cancer in Europe: results from the retrospective, multicentre, OnCovid registry study - 28/06/22

Doi : 10.1016/S1470-2045(22)00273-X 
David J Pinato, PhD a, b, Juan Aguilar-Company, MD e, g, Daniela Ferrante, PhD d, Georgina Hanbury, MBChB a, Mark Bower, PhD h, Ramon Salazar, PhD i, Oriol Mirallas, MD e, Anna Sureda, PhD j, Andrea Plaja, MD k, Marc Cucurull, MD k, Ricard Mesia, MD k, Sarah Townsend l, Amanda Jackson, RN l, Alessia Dalla Pria, MD h, Thomas Newsom-Davis, PhD h, Jasmine Handford, MSc m, Ailsa Sita-Lumsden, PhD o, Eleanor Apthorp, BSc n, Bruno Vincenzi, PhD p, Alexia Bertuzzi, MD q, Joan Brunet, PhD r, Matteo Lambertini s, t, Clara Maluquer, MD j, Paolo Pedrazzoli, MD u, v, Federica Biello, MD b, Alasdair Sinclair, MBBS w, Samira Bawany, MD w, Saira Khalique, PhD w, Sabrina Rossi, MD q, Lucy Rogers, MD w, Cian Murphy, PhD w, Katherine Belessiotis, MBBS w, M Carmen Carmona-García, MD r, Rachel Sharkey, RN h, David García-Illescas, MD e, Gianpiero Rizzo, MD u, Marta Perachino, MD s, t, Nadia Saoudi-Gonzalez, MSc e, Kris Doonga, MD h, Laura Fox, MD f, Elisa Roldán, MD e, Gianluca Gaidano, MD c, x, Isabel Ruiz-Camps, PhD g, Riccardo Bruna, MD c, x, Andrea Patriarca, MD c, x, Clara Martinez-Vila, MD y, Luca Cantini, MD z, Alberto Zambelli, MD aa, Raffaele Giusti, MD ab, Francesca Mazzoni, MD ac, Enrico Caliman, MD ac, Armando Santoro, MD q, ad, Federica Grosso, PhD ae, Alessandro Parisi, MD ag, Paola Queirolo, MD ah, Avinash Aujayeb, MBBS ai, Lorenza Rimassa, MD q, ad, Aleix Prat, PhD aj, ak, Marco Tucci, PhD al, am, Michela Libertini, MD an, Salvatore Grisanti, PhD ao, Uma Mukherjee, PhD ap, Nikolaos Diamantis, PhD ap, Vittorio Fusco, MD af, Daniele Generali, PhD aq, ar, Salvatore Provenzano, MD as, Alessandra Gennari, PhD b, Josep Tabernero, PhD at, Alessio Cortellini, PhD a,
on behalf of the

OnCovid study group

Joanne S Evans, Judith Swallow, Chris Chung, Meera Patel, Gino Dettorre, Diego Ottaviani, Amani Chowdhury, Eve Merry, Neha Chopra, Alvin JX Lee, Christopher CT Sng, Tamara Yu, Marianne Shawe-Taylor, Hamish DC Bain, Yien Ning Sophia Wong, Myria Galazi, Sarah Benafif, Palma Dileo, Irina Earnshaw, Grisma Patel, Anjui Wu, Gehan Soosaipillai, Lee Cooper, Ramis Andaleeb, Saoirse Dolly, Eleanor Apthorp, Krishnie Srikandarajah, Eleanor Jones, Mieke Van Hemelrijck, Charlotte Moss, Beth Russell, John Chester, Angela Loizidou, Martine Piccart, Claudia A Cruz, Roxana Reyes, Elia Segui, Javier Marco-Hernández, Margarita Viladot, Simeon Eremiev, Roser Fort-Culillas, Isabel Garcia, Raquel Liñan, Ariadna Roqué Lloveras, Nadia Harbeck, Rachel Wuerstlein, Franziska Henze, Sven Mahner, Eudald Felip, Anna Pous, Francesca D’Avanzo, Lorenza Scotti, Marco Krengli, Andrea Marrari, Sara Delfanti, Antonio Maconi, Marta Betti, Giuseppe Tonini, Giuseppina Rita Di Fazio, Carlo Tondini, Lorenzo Chiudinelli, Michela Franchi, Michela Libertini, Rossella Bertulli, Alice Baggi, Valeria Tovazzi, Corrado Ficorella, Giampiero Porzio, Maristella Saponara, Marco Filetti, Federica Zoratto, Francesco Paoloni, Rossana Berardi, Annalisa Guida, Sergio Bracarda, Maria Iglesias, Ana Sanchez de Torre, Marco Tagliamento, Emeline Colomba, Fanny Pommeret

a Department of Surgery and Cancer, Imperial College London, Hammersmith Hospital, London, UK 
b Division of Oncology, University of Piemonte Orientale, Novara, Italy 
c Division of Haematology, University of Piemonte Orientale, Novara, Italy 
d Department of Translational Medicine, Unit of Medical Statistics, University of Piemonte Orientale, Novara, Italy 
e Medical Oncology, Vall d’Hebron University Hospital and Institute of Oncology (VHIO), Barcelona, Spain 
f Department of Hematology, Vall d’Hebron University Hospital and Institute of Oncology (VHIO), Barcelona, Spain 
g Infectious Diseases, Vall d’Hebron University Hospital, Barcelona, Spain 
h Department of Oncology and National Centre for HIV Malignancy, Chelsea and Westminster Hospital, London, UK 
i Department of Medical Oncology, ICO L’Hospitalet, Oncobell Program (IDIBELL), CIBERONC, Hospitalet de Llobregat, Barcelona, Spain 
j Haematology Department, ICO L’Hospitalet, Hospitalet de Llobregat, IDIBELL, Universitat de Barcelona, Barcelona, Spain 
k Medical Oncology Department, B-ARGO Group, IGTP, Catalan Institute of Oncology-Badalona, Spain 
l Velindre Cancer Centre, Cardiff, UK 
m Translational Oncology and Urology Research (TOUR), School of Cancer and Pharmaceutical Sciences, King’s College London, London, UK 
n Medical School, King’s College London, London, UK 
o Medical Oncology, Guy’s and St Thomas’ NHS Foundation Trust, London, UK 
p Policlinico Universitario Campus Bio-Medico, Rome, Italy 
q Medical Oncology and Hematology Unit, Humanitas Cancer Center, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy 
r Department of Medical Oncology, Catalan Institute of Oncology, University Hospital Josep Trueta, Girona, Spain 
s Medical Oncology Department, IRCCS Ospedale Policlinico San Martino, Genova, Italy 
t Department of Internal Medicine and Medical Specialties (DiMI), School of Medicine, University of Genova, Genova, Italy 
u Medical Oncology Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy 
v Department of Internal Medicine and Medical Therapy, University of Pavia, Pavia, Italy 
w Cancer Division, University College London Hospitals, London, UK 
x Maggiore della Carità Hospital, Novara, Italy 
y Fundació Althaia Manresa, Manresa, Spain 
z Medical Oncology, AOU Ospedali Riuniti, Polytechnic University of the Marche Region, Ancona, Italy 
aa Oncology Unit, ASST Papa Giovanni XXIII, Bergamo, Italy 
ab Medical Oncology, St Andrea Hospital, Rome, Italy 
ac Medical Oncology, Careggi University Hospital, Florence, Italy 
ad Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy 
ae Mesothelioma Unit, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy 
af Oncology Unit and Centro Documentazione Osteonecrosi, Azienda Ospedaliera SS Antonio e Biagio e Cesare Arrigo, Alessandria, Italy 
ag The Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy 
ah Melanoma and Sarcoma Medical Treatment Unit, IEO - Istituto Europeo di Oncologia, Milan, Italy 
ai Respiratory Department, Northumbria Healthcare NHS Foundation Trust, North Shields, UK 
aj Translational Genomics and Targeted Therapies in Solid Tumors, IDIBAPS, Barcelona, Spain 
ak Department of Medical Oncology, Hospital Clinic, Barcelona, Spain 
al Section of Medical Oncology, Department of Interdisciplinary Medicine (DIM), University of Bari ‘Aldo Moro’, Bari, Italy 
am IRCCS, Istituto Tumori Giovanni Paolo II, Bari, Italy 
an Medical Oncology Unit, Fondazione Poliambulanza Istituto Ospedaliero, Brescia, Italy 
ao Medical Oncology Unit, Spedali Civili, Brescia, Italy 
ap Medical Oncology, Barts Health NHS Trust, London, UK 
aq Multidisciplinary Breast Pathology and Translational Research Unit, ASST Cremona, Cremona, Italy 
ar Department of Medical, Surgical and Health Sciences, University of Trieste, Trieste, Italy 
as Medical Oncology 2, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy 
at Medical Oncology, Vall d’Hebron University Hospital and Institute of Oncology (VHIO), IOB-Quiron, UVic-UCC, Barcelona, Spain 

* Correspondence to: Dr Alessio Cortellini, Department of Surgery and Cancer, Imperial College London, Hammersmith Hospital, London SW7 2AZ, UK Department of Surgery and Cancer Imperial College London Hammersmith Hospital London SW7 2AZ UK

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Summary

Background

The omicron (B.1.1.529) variant of SARS-CoV-2 is highly transmissible and escapes vaccine-induced immunity. We aimed to describe outcomes due to COVID-19 during the omicron outbreak compared with the prevaccination period and alpha (B.1.1.7) and delta (B.1.617.2) waves in patients with cancer in Europe.

Methods

In this retrospective analysis of the multicentre OnCovid Registry study, we recruited patients aged 18 years or older with laboratory-confirmed diagnosis of SARS-CoV-2, who had a history of solid or haematological malignancy that was either active or in remission. Patient were recruited from 37 oncology centres from UK, Italy, Spain, France, Belgium, and Germany. Participants were followed up from COVID-19 diagnosis until death or loss to follow-up, while being treated as per standard of care. For this analysis, we excluded data from centres that did not actively enter new data after March 1, 2021 (in France, Germany, and Belgium). We compared measures of COVID-19 morbidity, which were complications from COVID-19, hospitalisation due to COVID-19, and requirement of supplemental oxygen and COVID-19-specific therapies, and COVID-19 mortality across three time periods designated as the prevaccination (Feb 27 to Nov 30, 2020), alpha-delta (Dec 1, 2020, to Dec 14, 2021), and omicron (Dec 15, 2021, to Jan 31, 2022) phases. We assessed all-cause case-fatality rates at 14 days and 28 days after diagnosis of COVID-19 overall and in unvaccinated and fully vaccinated patients and in those who received a booster dose, after adjusting for country of origin, sex, age, comorbidities, tumour type, stage, and status, and receipt of systemic anti-cancer therapy. This study is registered with ClinicalTrials.gov, NCT04393974, and is ongoing.

Findings

As of Feb 4, 2022 (database lock), the registry included 3820 patients who had been diagnosed with COVID-19 between Feb 27, 2020, and Jan 31, 2022. 3473 patients were eligible for inclusion (1640 [47·4%] were women and 1822 [52·6%] were men, with a median age of 68 years [IQR 57–77]). 2033 (58·5%) of 3473 were diagnosed during the prevaccination phase, 1075 (31·0%) during the alpha-delta phase, and 365 (10·5%) during the omicron phase. Among patients diagnosed during the omicron phase, 113 (33·3%) of 339 were fully vaccinated and 165 (48·7%) were boosted, whereas among those diagnosed during the alpha-delta phase, 152 (16·6%) of 915 were fully vaccinated and 21 (2·3%) were boosted. Compared with patients diagnosed during the prevaccination period, those who were diagnosed during the omicron phase had lower case-fatality rates at 14 days (adjusted odds ratio [OR] 0·32 [95% CI 0·19–0·61) and 28 days (0·34 [0·16–0·79]), complications due to COVID-19 (0·26 [0·17–0·46]), and hospitalisation due to COVID-19 (0·17 [0·09–0·32]), and had less requirements for COVID-19-specific therapy (0·22 [0·15–0·34]) and oxygen therapy (0·24 [0·14–0·43]) than did those diagnosed during the alpha-delta phase. Unvaccinated patients diagnosed during the omicron phase had similar crude case-fatality rates at 14 days (ten [25%] of 40 patients vs 114 [17%] of 656) and at 28 days (11 [27%] of 40 vs 184 [28%] of 656) and similar rates of hospitalisation due to COVID-19 (18 [43%] of 42 vs 266 [41%] of 652) and complications from COVID-19 (13 [31%] of 42 vs 237 [36%] of 659) as those diagnosed during the alpha-delta phase.

Interpretation

Despite time-dependent improvements in outcomes reported in the omicron phase compared with the earlier phases of the pandemic, patients with cancer remain highly susceptible to SARS-CoV-2 if they are not vaccinated against SARS-CoV-2. Our findings support universal vaccination of patients with cancer as a protective measure against morbidity and mortality from COVID-19.

Funding

National Institute for Health and Care Research Imperial Biomedical Research Centre and the Cancer Treatment and Research Trust.

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