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SARS-CoV-2 omicron (B.1.1.529)-related COVID-19 sequelae in vaccinated and unvaccinated patients with cancer: results from the OnCovid registry - 28/03/23

Doi : 10.1016/S1470-2045(23)00056-6 
Alessio Cortellini, PhD a, b, , Josep Tabernero, ProfPhD c, Uma Mukherjee, PhD d, Ramon Salazar, PhD e, Anna Sureda, PhD f, Clara Maluquer, MD f, Daniela Ferrante, PhD g, Mark Bower, ProfPhD j, Rachel Sharkey j, Oriol Mirallas, MD c, Andrea Plaja, MD k, Marc Cucurull, MD k, Ricard Mesia, MD k, Alessia Dalla Pria, MD j, Thomas Newsom-Davis, PhD j, Mieke Van Hemelrijck, ProfPhD l, m, Ailsa Sita-Lumsden, PhD l, Eleanor Apthorp, BSc n, Bruno Vincenzi, ProfPhD b, o, Giuseppina Rita Di Fazio, MD b, o, Giuseppe Tonini, ProfPhD b, o, Francesco Pantano, PhD b, o, Alexia Bertuzzi, MD p, Sabrina Rossi, MD p, Joan Brunet, PhD q, Matteo Lambertini, PhD r, s, Paolo Pedrazzoli, MD t, u, Federica Biello, MD h, x, Francesca D’Avanzo, MD h, x, Alvin J X Lee, PhD v, Marianne Shawe-Taylor, MRes v, Lucy Rogers, MD v, Cian Murphy, PhD v, Lee Cooper, MD v, Ramis Andaleeb, MD v, Saira Khalique, PhD v, Samira Bawany, MD v, Sarah Ahmed, MD v, M Carmen Carmona-García, MD q, Roser Fort-Culillas, MD q, Raquel Liñan, MD q, Federica Zoratto, MD w, Gianpiero Rizzo, MD u, Marta Perachino, MD r, s, Kris Doonga, MD j, Gianluca Gaidano, ProfMD i, x, Riccardo Bruna, MD i, x, Andrea Patriarca, MD i, x, Clara Martinez-Vila, MD y, Ignacio Pérez Criado, MD y, Raffaele Giusti, MD z, Francesca Mazzoni, MD aa, Lorenzo Antonuzzo, PhD aa, Armando Santoro, ProfMD p, ab, Alessandro Parisi, MD ac, Paola Queirolo, MD ad, Avinash Aujayeb, MD ae, Lorenza Rimassa, MD p, ab, Nikolaos Diamantis, PhD d, Rossella Bertulli, MD af, Claudia A M Fulgenzi, MD a, o, Antonio D’Alessio, MD a, h, Isabel Ruiz-Camps, PhD ag, Nadia Saoudi-Gonzalez, MD c, David Garcia Illescas, MD c, Irene Medina, MD ah, Laura Fox, MD ah, Alessandra Gennari, MD h, x, Juan Aguilar-Company, MD c, ag, David J Pinato, PhD a, h
on behalf of the

OnCovid study group

Joanne S Evans, Judith Swallow, Georgina Hanbury, Chris Chung, Meera Patel, Gino Dettorre, Katherine Belessiotis, Dolly Saorise, Eleanor Jones, Eleanor Apthorp, Charlotte Moss, Beth Russell, Sarah Townsend, Amanda Jackson, Angela Loizidou, Martine Piccart, Fanny Pommeret, Emeline Colomba-Blameble, Aleix Prat, Claudia A Cruz, Roxana Reyes, Elia Segui, Javier Marco-Hernández, Margarita Viladot, Nadia Harbeck, Rachel Wuerstlein, Franziska Henze, Sven Mahner, Eudald Felip, Lorenza Scotti, Andrea Marrari, Federica Grosso, Vittorio Fusco, Sara Delfanti, Maura Rossi, Alberto Zambelli, Carlo Tondini, Lorenzo Chiudinelli, Michela Franchi, Michela Libertini, Salvatore Provenzano, Daniele Generali, Salvatore Grisanti, Alice Baggi, Valeria Tovazzi, Corrado Ficorella, Giampiero Porzio, Maristella Saponara, Marco Filetti, Marco Tucci, Rossana Berardi, Luca Cantini, Francesco Paoloni, Annalisa Guida, Sergio Bracarda, Maria Iglesias, Ana Sanchez de Torre, Marco Tagliamento

a Department of Surgery and Cancer, Imperial College London, London, UK 
b Medical Oncology, Fondazione Policlinico Universitario Campus Bio-Medico, Via Alvaro del Portillo, 200 - 00128 Roma, Italy 
c Medical Oncology, Vall d’Hebron University Hospital and Institute of Oncology, IOB-Quiron, UVic-UCC, Barcelona, Spain 
d Medical Oncology, Barts Health NHS Trust, London, UK 
e Catalan Institute of Oncology (ICO), University of Barcelona, Bellvitge Biomedical Research Institute (IDIBELL), CIBERONC, L’Hospitalet de Llobregat, Barcelona, Spain 
f Haematology Department, ICO Hospitalet, Hospitalet de Llobregat, IDIBELL, Universitat de Barcelona, Barcelona, Spain 
g Unit of Medical Statistics, Department of Translational Medicine, University of Piemonte Orientale, Novara, Italy 
h Division of Oncology, Department of Translational Medicine, University of Piemonte Orientale, Novara, Italy 
i Division of Haematology, Department of Translational Medicine, University of Piemonte Orientale, Novara, Italy 
j Department of Oncology and National Centre for HIV Malignancy, Chelsea and Westminster Hospital, London, UK 
k Medical Oncology Department, B-ARGO Group, IGTP, Catalan Institute of Oncology, Badalona, Spain 
l Medical Oncology, Guy’s and St Thomas’ NHS Foundation Trust, London, UK 
m Translational Oncology and Urology Research, School of Cancer and Pharmaceutical Sciences, King’s College London, London, UK 
n Medical School, King’s College London, London, UK 
o Department of Medicine and Surgery, Università Campus Bio-Medico di Roma, Via Alvaro del Portillo, 21 - 00128 Roma, Italy 
p Medical Oncology and Hematology Unit, Humanitas Cancer Center, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy 
q Department of Medical Oncology, Catalan Institute of Oncology, University Hospital Josep Trueta, Girona, Spain 
r Medical Oncology Department, UO Clinica di Oncologia Medica, IRCCS Ospedale Policlinico San Martino, Genova, Italy 
s Department of Internal Medicine and Medical Specialties, School of Medicine, University of Genova, Genova, Italy 
t Department of Internal Medicine and Medical Therapy, University of Pavia, Pavia, Italy 
u Medical Oncology Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy 
v Cancer Division, University College London Hospitals, London, UK 
w Medical Oncology, Santa Maria Goretti Hospital, Latina, Italy 
x Ospedale Maggiore della Caritá, Novara, Italy 
y Fundació Althaia Manresa, Manresa, Spain 
z Medical Oncology, St Andrea Hospital, Rome, Italy 
aa Medical Oncology, Careggi University Hospital, Florence, Italy 
ab Department of Biomedical Sciences, Humanitas University, Milan, Italy 
ac Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy 
ad Melanoma and Sarcoma Medical Treatment Unit, IEO, European Institute of Oncology IRCCS, Milan, Italy 
ae Respiratory Department, Northumbria Healthcare NHS Foundation Trust, North Shields, UK 
af Medical Oncology 2, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy 
ag Department of Infectious Diseases, Vall d’Hebron University Hospital and Institute of Oncology, Barcelona, Spain 
ah Department of Hematology, Vall d’Hebron University Hospital and Institute of Oncology, Barcelona, Spain 

* Correspondence to: Dr Alessio Cortellini, Department of Surgery and Cancer, Imperial College London, London W12 0NN, UK Department of Surgery and Cancer Imperial College London London W12 0NN UK

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Summary

Background

COVID-19 sequelae can affect about 15% of patients with cancer who survive the acute phase of SARS-CoV-2 infection and can substantially impair their survival and continuity of oncological care. We aimed to investigate whether previous immunisation affects long-term sequelae in the context of evolving variants of concern of SARS-CoV-2.

Methods

OnCovid is an active registry that includes patients aged 18 years or older from 37 institutions across Belgium, France, Germany, Italy, Spain, and the UK with a laboratory-confirmed diagnosis of COVID-19 and a history of solid or haematological malignancy, either active or in remission, followed up from COVID-19 diagnosis until death. We evaluated the prevalence of COVID-19 sequelae in patients who survived COVID-19 and underwent a formal clinical reassessment, categorising infection according to the date of diagnosis as the omicron (B.1.1.529) phase from Dec 15, 2021, to Jan 31, 2022; the alpha (B.1.1.7)–delta (B.1.617.2) phase from Dec 1, 2020, to Dec 14, 2021; and the pre-vaccination phase from Feb 27 to Nov 30, 2020. The prevalence of overall COVID-19 sequelae was compared according to SARS-CoV-2 immunisation status and in relation to post-COVID-19 survival and resumption of systemic anticancer therapy. This study is registered with ClinicalTrials.gov, NCT04393974.

Findings

At the follow-up update on June 20, 2022, 1909 eligible patients, evaluated after a median of 39 days (IQR 24–68) from COVID-19 diagnosis, were included (964 [50·7%] of 1902 patients with sex data were female and 938 [49·3%] were male). Overall, 317 (16·6%; 95% CI 14·8–18·5) of 1909 patients had at least one sequela from COVID-19 at the first oncological reassessment. The prevalence of COVID-19 sequelae was highest in the pre-vaccination phase (191 [19·1%; 95% CI 16·4–22·0] of 1000 patients). The prevalence was similar in the alpha–delta phase (110 [16·8%; 13·8–20·3] of 653 patients, p=0·24), but significantly lower in the omicron phase (16 [6·2%; 3·5–10·2] of 256 patients, p<0·0001). In the alpha–delta phase, 84 (18·3%; 95% CI 14·6–22·7) of 458 unvaccinated patients and three (9·4%; 1·9–27·3) of 32 unvaccinated patients in the omicron phase had sequelae. Patients who received a booster and those who received two vaccine doses had a significantly lower prevalence of overall COVID-19 sequelae than unvaccinated or partially vaccinated patients (ten [7·4%; 95% CI 3·5–13·5] of 136 boosted patients, 18 [9·8%; 5·8–15·5] of 183 patients who had two vaccine doses vs 277 [18·5%; 16·5–20·9] of 1489 unvaccinated patients, p=0·0001), respiratory sequelae (six [4·4%; 1·6–9·6], 11 [6·0%; 3·0–10·7] vs 148 [9·9%; 8·4–11·6], p=0·030), and prolonged fatigue (three [2·2%; 0·1–6·4], ten [5·4%; 2·6–10·0] vs 115 [7·7%; 6·3–9·3], p=0·037).

Interpretation

Unvaccinated patients with cancer remain highly vulnerable to COVID-19 sequelae irrespective of viral strain. This study confirms the role of previous SARS-CoV-2 immunisation as an effective measure to protect patients from COVID-19 sequelae, disruption of therapy, and ensuing mortality.

Funding

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

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© 2023  The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Publié par Elsevier Masson SAS. Tous droits réservés.
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