EBioMedicine (Jun 2022)
Breakthrough SARS-CoV-2 infections after COVID-19 mRNA vaccination in MS patients on disease modifying therapies during the Delta and the Omicron waves in Italy
- Maria Pia Sormani,
- Irene Schiavetti,
- Matilde Inglese,
- Luca Carmisciano,
- Alice Laroni,
- Caterina Lapucci,
- Valeria Visconti,
- Carlo Serrati,
- Ilaria Gandoglia,
- Tiziana Tassinari,
- Germana Perego,
- Giampaolo Brichetto,
- Paola Gazzola,
- Antonio Mannironi,
- Maria Laura Stromillo,
- Cinzia Cordioli,
- Doriana Landi,
- Marinella Clerico,
- Elisabetta Signoriello,
- Eleonora Cocco,
- Jessica Frau,
- Maria Teresa Ferrò,
- Alessia Di Sapio,
- Livia Pasquali,
- Monica Ulivelli,
- Fabiana Marinelli,
- Matteo Pizzorno,
- Graziella Callari,
- Rosa Iodice,
- Giuseppe Liberatore,
- Francesca Caleri,
- Anna Maria Repice,
- Susanna Cordera,
- Mario Alberto Battaglia,
- Marco Salvetti,
- Diego Franciotta,
- Antonio Uccelli,
- Alessandro Maglione,
- Alessia Di Sapio,
- Alessio Signori,
- Alice Laroni,
- Aniello Iovino,
- Anna Maria Repice,
- Antonio Mannironi,
- Antonio Uccelli,
- Carlo Serrati,
- Carolina Gabri Nicoletti,
- Caterina Lapucci,
- Chiara Rosa Mancinelli,
- Cinzia Cordioli,
- Daiana Bezzini,
- Daniele Carmagnini,
- Davide Brogi,
- Diego Franciotta,
- Doriana Landi,
- Eduardo Nobile Orazio,
- Eleonora Cocco,
- Elisabetta Signoriello,
- Enri Nako,
- Ester Assandrir,
- Fabiana Marinelli,
- Federica Baldi,
- Filippo Ansaldi,
- Francesca Bovis,
- Francesca Caleri,
- Gabriele Siciliano,
- Gaia Cola,
- Germana Perego,
- Giacomo Lus,
- Giampaolo Brichetto,
- Giancarlo Icardi,
- Gianmarco Bellucci,
- Giorgio Da Rin,
- Girolama Alessandra Marfia,
- Giulia Vazzoler,
- Giuseppe Liberatore,
- Giuseppe Trivelli,
- Graziella Callari,
- Ilaria Gandoglia,
- Ilaria Maietta,
- Irene Schiavetti,
- Jessica Frau,
- Laura Sticchi,
- Livia Pasquali,
- Lorena Lorefice,
- Luca Carmisciano,
- Lucia Ruggiero,
- Marcello Manzino,
- Marco Salvetti,
- Margherita Monti Bragadin,
- Maria Chiara Buscarinu,
- Maria Gagliardi,
- Maria Laura Stromillo,
- Maria Pia Sormani,
- Maria Teresa Ferrò,
- Maria Teresa Rilla,
- Marinella Clerico,
- Mario Alberto Battaglia,
- Marta Ponzano,
- Marzia Fronza,
- Massimo Del Sette,
- Matilde Inglese,
- Matteo Scialabba,
- Michele Bedognetti,
- Monica Ulivelli,
- Nicola De Rossi,
- Nicola De Stefano,
- Paola Gazzola,
- Rachele Bigi,
- Raffaele Dubbioso,
- Roberta Reniè,
- Rosa Iodice,
- Sabrina Fabbri,
- Sarah Rasia,
- Simona Rolla,
- Stefan Platzgummer,
- Susanna Cordera,
- Tiziana Tassinari,
- Valentina Carlini
Affiliations
- Maria Pia Sormani
- Department of Health Sciences, Section of Biostatistics, University of Genova, Italy; IRCCS Ospedale Policlinico San Martino, Genova, Italy; Corresponding author at: Department of Health Sciences, Section of Biostatistics, University of Genova, Via Pastore 1 16132, Italy.
- Irene Schiavetti
- Department of Health Sciences, Section of Biostatistics, University of Genova, Italy
- Matilde Inglese
- IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI) and Center of Excellence for Biomedical Research (CEBR), University of Genoa, Genoa, Italy
- Luca Carmisciano
- Department of Health Sciences, Section of Biostatistics, University of Genova, Italy
- Alice Laroni
- IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI) and Center of Excellence for Biomedical Research (CEBR), University of Genoa, Genoa, Italy
- Caterina Lapucci
- IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI) and Center of Excellence for Biomedical Research (CEBR), University of Genoa, Genoa, Italy
- Valeria Visconti
- Laboratory Medicine, IRCCS Ospedale Policlinico San Martino, Genova, Italy
- Carlo Serrati
- Department of Neurology, Imperia Hospital, Imperia, Italy
- Ilaria Gandoglia
- Neurology Unit, Galliera Hospital, Italy
- Tiziana Tassinari
- S.C. Neurologia - Ospedale Santa Corona Pietra Ligure (Sv), Italy
- Germana Perego
- SC Neurologia ASL 4 Chiavarese, Italy
- Giampaolo Brichetto
- AISM Rehabilitation Center, Genoa, Italy
- Paola Gazzola
- Centro Sclerosi Multipla S.C. Neurologia Asl 3 Genovese, Italy
- Antonio Mannironi
- Department of Neurology, Sant'Andrea Hospital, La Spezia, Italy
- Maria Laura Stromillo
- Clinica Neurologica e Malattie Neurometaboliche, Università degli Studi di Siena, Italy
- Cinzia Cordioli
- Centro Sclerosi Multipla ASST Spedali Civili di Brescia, Italy
- Doriana Landi
- Multiple Sclerosis Clinical and Research Unit, Department of Systems Medicine, Tor Vergata University and Hospital, Rome, Italy
- Marinella Clerico
- Dipartimento di Scienze Cliniche e Biologiche, Università di Torino, Italy
- Elisabetta Signoriello
- Centro Sclerosi Multipla, II Clinica Neurologica, Università della Campania Luigi Vanvitelli, Italy
- Eleonora Cocco
- Centro Sclerosi Multipla Ospedale Binaghi Cagliari - ATS Sardegna, Università di Cagliari, Italy
- Jessica Frau
- Centro Sclerosi Multipla Ospedale Binaghi Cagliari - ATS Sardegna, Università di Cagliari, Italy
- Maria Teresa Ferrò
- Neuroimmunology, Center for Multiple Sclerosis, Cerobrovascular Department, Neurological Unit, ASST Crema, Italy
- Alessia Di Sapio
- Department of Neurology, Regina Montis Regalis Hospital, Mondovì, Italy
- Livia Pasquali
- Department of Clinical and Experimental Medicine, Neurology Unit, University of Pisa, Italy
- Monica Ulivelli
- Department of Medicine, Surgery and Neuroscience, University of Siena, Italy
- Fabiana Marinelli
- Multiple Sclerosis Center, Fabrizio Spaziani Hospital, Frosinone, Italy
- Matteo Pizzorno
- Neurologia, Ospedale San Paolo, Savona, Italy
- Graziella Callari
- UOC Neurologia e Centro SM Fondazione Istituto G. Giglio, Cefalù, Italy
- Rosa Iodice
- Clinica Neurologica, DSNRO Università Federico II di Napoli, Italy
- Giuseppe Liberatore
- Neuromuscular and Neuroimmunology Service, IRCCS Humanitas Research Hospital, Rozzano, Italy
- Francesca Caleri
- MS Center, Department of Neurology, F. Tappeiner Hospital Meran (BZ), Italy
- Anna Maria Repice
- Department of Neurology 2, Careggi University Hospital, Florence, Italy
- Susanna Cordera
- Department of Neurology, Ospedale Regionale, Aosta, Italy
- Mario Alberto Battaglia
- Research Department, Italian Multiple Sclerosis Foundation, Genoa, Italy; Department of Life Sciences, University of Siena, Italy
- Marco Salvetti
- Centre for Experimental Neurological Therapies (CENTERS), Department of Neurosciences, Mental Health and Sensory Organs, Sapienza University of Rome, Italy; IRCCS Istituto Neurologico Mediterraneo Neuromed, Pozzilli, Italy
- Diego Franciotta
- Autoimmunology Laboratory, IRCCS Ospedale Policlinico San Martino, Genoa, Italy
- Antonio Uccelli
- IRCCS Ospedale Policlinico San Martino, Genova, Italy; Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI) and Center of Excellence for Biomedical Research (CEBR), University of Genoa, Genoa, Italy
- Alessandro Maglione
- Alessia Di Sapio
- Alessio Signori
- Alice Laroni
- Aniello Iovino
- Anna Maria Repice
- Antonio Mannironi
- Antonio Uccelli
- Carlo Serrati
- Carolina Gabri Nicoletti
- Caterina Lapucci
- Chiara Rosa Mancinelli
- Cinzia Cordioli
- Daiana Bezzini
- Daniele Carmagnini
- Davide Brogi
- Diego Franciotta
- Doriana Landi
- Eduardo Nobile Orazio
- Eleonora Cocco
- Elisabetta Signoriello
- Enri Nako
- Ester Assandrir
- Fabiana Marinelli
- Federica Baldi
- Filippo Ansaldi
- Francesca Bovis
- Francesca Caleri
- Gabriele Siciliano
- Gaia Cola
- Germana Perego
- Giacomo Lus
- Giampaolo Brichetto
- Giancarlo Icardi
- Gianmarco Bellucci
- Giorgio Da Rin
- Girolama Alessandra Marfia
- Giulia Vazzoler
- Giuseppe Liberatore
- Giuseppe Trivelli
- Graziella Callari
- Ilaria Gandoglia
- Ilaria Maietta
- Irene Schiavetti
- Jessica Frau
- Laura Sticchi
- Livia Pasquali
- Lorena Lorefice
- Luca Carmisciano
- Lucia Ruggiero
- Marcello Manzino
- Marco Salvetti
- Margherita Monti Bragadin
- Maria Chiara Buscarinu
- Maria Gagliardi
- Maria Laura Stromillo
- Maria Pia Sormani
- Maria Teresa Ferrò
- Maria Teresa Rilla
- Marinella Clerico
- Mario Alberto Battaglia
- Marta Ponzano
- Marzia Fronza
- Massimo Del Sette
- Matilde Inglese
- Matteo Scialabba
- Michele Bedognetti
- Monica Ulivelli
- Nicola De Rossi
- Nicola De Stefano
- Paola Gazzola
- Rachele Bigi
- Raffaele Dubbioso
- Roberta Reniè
- Rosa Iodice
- Sabrina Fabbri
- Sarah Rasia
- Simona Rolla
- Stefan Platzgummer
- Susanna Cordera
- Tiziana Tassinari
- Valentina Carlini
- Journal volume & issue
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Vol. 80
p. 104042
Abstract
Summary: Background: In this study we aimed to monitor the risk of breakthrough SARS-CoV-2 infection in patients with MS (pwMS) under different DMTs and to identify correlates of reduced protection. Methods: This is a prospective Italian multicenter cohort study, long-term clinical follow-up of the CovaXiMS (Covid-19 vaccine in Multiple Sclerosis) study. 1855 pwMS scheduled for SARS-CoV-2 mRNA vaccination were enrolled and followed up to a mean time of 10 months. The cumulative incidence of breakthrough Covid-19 cases in pwMS was calculated before and after December 2021, to separate the Delta from the Omicron waves and to account for the advent of the third vaccine dose. Findings: 1705 pwMS received 2 m-RNA vaccine doses, 21/28 days apart. Of them, 1508 (88.5%) had blood assessment 4 weeks after the second vaccine dose and 1154/1266 (92%) received the third dose after a mean interval of 210 days (range 90-342 days) after the second dose. During follow-up, 131 breakthrough Covid-19 infections (33 during the Delta and 98 during the Omicron wave) were observed. The probability to be infected during the Delta wave was associated with SARS-CoV-2 antibody levels measured after 4 weeks from the second vaccine dose (HR=0.57, p < 0.001); the protective role of antibodies was preserved over the whole follow up (HR=0.57, 95%CI=0.43-0.75, p < 0.001), with a significant reduction (HR=1.40, 95%CI=1.01-1.94, p=0.04) for the Omicron cases. The third dose significantly reduced the risk of infection (HR=0.44, 95%CI=0.21-0.90,p=0.025) during the Omicron wave. Interpretation: The risk of breakthrough SARS-CoV-2 infections is mainly associated with reduced levels of the virus-specific humoral immune response. Funding: Supported by FISM - Fondazione Italiana Sclerosi Multipla – cod. 2021/Special-Multi/001 and financed or co-financed with the ‘5 per mille’ public funding