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Journal Articles Science Immunology Year : 2022

Vaccine breakthrough hypoxemic COVID-19 pneumonia in patients with auto-Abs neutralizing type I IFNs

Paul Bastard (1, 2, 3) , Sara Vazquez , Jamin Liu , Matthew T Laurie , Chung Yu Wang , Adrian Gervais , Tom Le Voyer (4) , Lucy Bizien (1) , Colin Zamecnik , Quentin Philippot (2) , Jérémie Rosain (5, 6) , Emilie Catherinot (7) , Andrew Willmore , Anthea M Mitchell , Rebecca Bair , Pierre Garçon (8) , Heather Kenney , Arnaud Fekkar (9) , Maria Salagianni , Garyphallia Poulakou (10) , Eleni Siouti , Sabina Sahanic (11) , Ivan Tancevski (11) , Günter Weiss (11) , Laurenz Nagl , Jérémy Manry (12, 13) , Sotirija Duvlis (14) , Daniel Arroyo-Sánchez , Estela Paz Artal , Luis Rubio , Cristiano Perani , Michela Bezzi , Alessandra Sottini , Virginia Quaresima , Lucie Roussel , Donald C Vinh , Luis Felipe Reyes , Margaux Garzaro , Nevin Hatipoglu , David Boutboul , Yacine Tandjaoui-Lambiotte , Alessandro Borghesi , Anna Aliberti , Irene Cassaniti , Fabienne Venet , Guillaume Monneret , Rabih Halwani , Narjes Saheb Sharif-Askari , Jeffrey Danielson , Sonia Burrel , Caroline Morbieu , Yurii Stepanovskyy , Anastasia Bondarenko , Alla Volokha , Oksana Boyarchuk , Alenka Gagro , Mathilde Neuville , Bénédicte Neven , Sevgi Keles , Romain Hernu , Antonin Bal , Antonio Novelli , Giuseppe Novelli , Kahina Saker , Oana Ailioaie , Arnau Antolí , Eric Jeziorski (15, 16) , Gemma Rocamora-Blanch , Carla Teixeira , Clarisse Delaunay , Marine Lhuillier , Paul Le Turnier , Yu Zhang , Matthieu Mahevas , Qiang Pan-Hammarström , Hassan Abolhassani , Thierry Bompoil , Karim Dorgham , Guy Gorochov , Cédric Laouenan , Carlos Rodríguez-Gallego , Lisa F P Ng , Laurent Renia , Aurora Pujol , Alexandre Belot , François Raffi , Luis M Allende , Javier Martinez-Picado , Tayfun Ozcelik , Sevgi Keles , Luisa Imberti , Luigi D Notarangelo , Jesus Troya , Xavier Solanich , Shen-Ying Zhang , Anne Puel , Michael R Wilson , Sophie Trouillet-Assant , Laurent Abel , Emmanuelle Jouanguy , Chun Jimmie Ye , Aurélie Cobat , Leslie M Thompson , Evangelos Andreakos , Qian Zhang , Mark S Anderson , Jean-Laurent Casanova (17) , Joseph L Derisi , Laurent Abel , Cristian Achille , Alessandro Aiuti , Saleh Al-Muhsen , Fahd Al-Mulla , Mark S Anderson , Evangelos Andreakos , Micol Angelini , Andrés A Arias , Gokhan Aytekin , Fausto Baldanti , Hagit Baris Feldman , Alexandre Belot , Federica Bergami , Catherine M Biggs , Dusan Bogunovic , Alexandre Bolze , Anastasiia Bondarenko , Ahmed A Bousfiha , Petter Brodin , Yenan Bryceson , Carlos D Bustamante , Manish J Butte , Giorgio Casari , John Christodoulou , Antonio Condino-Neto , Stefan N Constantinescu , Francesca Conti , Megan A Cooper , Clifton L Dalgard , Murkesh Desai , Beth A Drolet , Jamila El Baghdadi , Recai Ergun , Dilek Ergun , Sara Espinosa-Padilla , Jacques Fellay , Carlos Flores , José Luis Franco , Antoine Froidure , Stefano Ghirardello , Peter K Gregersen , Bodo Grimbacher , Filomeen Haerynck , David Hagin , Rabih Halwani , Lennart Hammarström , James R Heath , Sarah E Henrickson , Elena W Y Hsieh , Eystein Husebye , Kohsuke Imai , Yuval Itan , Erich D Jarvis , Fikret Kanat , Timokratis Karamitros , Kai Kisand , Vasyl Kopcha , Mykhaylo Korda , Cheng-Lung Ku , Yu-Lung Lau , Yun Ling , Carrie L Lucas , Tom Maniatis , Davood Mansouri , László Maródi , Isabelle Meyts , Joshua D Milner , Kristina Mironska , Trine H Mogensen , Francesco Mojoli , Francisco Morandeira , Tomohiro Morio , Lisa F P Ng , Luigi D Notarangelo , Antonio Novelli , Giuseppe Novelli , Cliona O'Farrelly , Satoshi Okada , Keisuke Okamoto , Tayfun Ozcelik , Michele Pagani , Qiang Pan-Hammarström , Jean W Pape , Rebeca Perez de Diego , David S Perlin , Graziano Pesole , Andrea Pession , Antonio Piralla , Anna M Planas , Carolina Prando , Aurora Pujol , Lluis Quintana-Murci (17) , Sathishkumar Ramaswamy , Laurent Renia , Igor Resnick , Raúl Rigo-Bonnin , Carlos Rodríguez-Gallego , Vanessa Sancho-Shimizu , Anna Sediva , Mikko R J Seppänen , Mohammed Shahrooei , Anna Shcherbina , Ondrej Slaby , Andrew L Snow , Pere Soler-Palacín , András N Spaan , Ivan Tancevski , Stuart G Tangye , Ahmad Abou Tayoun , Baykal Tulek , Stuart E Turvey , K M Furkan Uddin , Mohammed Uddin , Bénédicte Clément , Yumiko Abe-Jones , Saurabh Asthana , Sharvari Bhide , Carolyn S Calfee , Sidney A Carrillo , Suzanna Chak , Zachary Collins , David J Erle , Gabriela K Fragiadakis , Rajani Ghale , Carolyn M Hendrickson , Alejandra Jauregui , Kirsten N Kangelaris , Matthew F Krummel , Charles R Langelier , Tasha Lea , Deanna Lee , Aleksandra Leligdowicz , Carolyn Leroux , Raphael Lota , Michael Matthay , Viet Nguyen , Ravi Patel , Logan Pierce , Priya Prasad , Arjun Arkal Rao , Ahmad Rashid , Nicklaus Rodriguez , Bushra Samad , Cole Shaw , Austin Sigman , Kevin Tang , Luz Torres Altamirano , Alyssa Ward , Andrew Willmore , Michael R Wilson , Prescott G Woodruff , Laurent Abel , Clotilde Allavena , Claire Andrejak , François Angoulvant , Cecile Azoulay , Delphine Bachelet , Marie Bartoli , Romain Basmaci , Sylvie Behilill , Marine Beluze , Nicolas Benech , Dehbia Benkerrou , Krishna Bhavsar , Laurent Bitker , Lila Bouadma , Maude Bouscambert , Pauline Caraux Paz , Minerva Cervantes-Gonzalez , Anissa Chair , Catherine Chirouze , Alexandra Coelho , Hugues Cordel , Camille Couffignal , Sandrine Couffin-Cadiergues , Eric D’ortenzio , Etienne de Montmollin , Alexa Debard , Marie-Pierre Debray , Dominique Deplanque , Diane Descamps , Mathilde Desvallée , Alpha Diallo , Jean-Luc Diehl , Alphonsine Diouf , Céline Dorival , François Dubos , Xavier Duval , Philippine Eloy , Vincent Enouf , Olivier Epaulard , Hélène Esperou , Marina Esposito-Farese , Manuel Etienne , Denis Garot , Nathalie Gault , Alexandre Gaymard , Jade Ghosn , Tristan Gigante , Morgane Gilg , François Goehringer , Jérémie Guedj , Alexandre Hoctin , Isabelle Hoffmann , Ikram Houas , Jean-Sébastien Hulot , Salma Jaafoura , Ouifiya Kafif , Florentia Kaguelidou , Sabrina Kali , Younes Kerroumi , Antoine Khalil , Coralie Khan , Antoine Kimmoun , Fabrice Laine , Cédric Laouénan , Samira Laribi , Minh Le , Cyril Le Bris , Sylvie Le Gac , Quentin Le Hingrat , Soizic Le Mestre , Hervé Le Nagard , Adrien Lemaignen , Véronique Lemee , François-Xavier Lescure , Sophie Letrou , Yves Levy , Bruno Lina , Guillaume Lingas , Jean Christophe Lucet , Moïse Machado , Denis Malvy , Marina Mambert , Aldric Manuel , France Mentré , Amina Meziane , Hugo Mouquet , Jimmy Mullaert , Nadège Neant , Duc Nguyen , Marion Noret , Aurélie Papadopoulos , Christelle Paul , Nathan Peiffer-Smadja , Vincent Peigne , Ventzislava Petrov-Sanchez , Gilles Peytavin , Huong Pham , Olivier Picone , Valentine Piquard , Julien Poissy , Oriane Puéchal , Manuel Rosa-Calatrava , Bénédicte Rossignol , Patrick Rossignol , Carine Roy , Marion Schneider , Richa Su , Coralie Tardivon , Marie-Capucine Tellier , François Téoulé , Olivier Terrier , Jean-François Timsit , Christelle Tual , Sarah Tubiana , Sylvie van der Werf , Noémie Vanel , Aurélie Veislinger , Benoit Visseaux , Aurélie Wiedemann , Yazdan Yazdanpanah
Sara Vazquez
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Jamin Liu
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Matthew T Laurie
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Chung Yu Wang
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Adrian Gervais
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Colin Zamecnik
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Andrew Willmore
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Anthea M Mitchell
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Rebecca Bair
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Heather Kenney
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Maria Salagianni
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Eleni Siouti
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Laurenz Nagl
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Daniel Arroyo-Sánchez
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Estela Paz Artal
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Luis Rubio
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Cristiano Perani
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Michela Bezzi
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Alessandra Sottini
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Virginia Quaresima
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Lucie Roussel
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Donald C Vinh
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Luis Felipe Reyes
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Margaux Garzaro
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Nevin Hatipoglu
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David Boutboul
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Yacine Tandjaoui-Lambiotte
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Alessandro Borghesi
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Anna Aliberti
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Irene Cassaniti
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Fabienne Venet
Guillaume Monneret
Rabih Halwani
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Narjes Saheb Sharif-Askari
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Jeffrey Danielson
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Sonia Burrel
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Caroline Morbieu
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Yurii Stepanovskyy
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Anastasia Bondarenko
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Alla Volokha
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Oksana Boyarchuk
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Alenka Gagro
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Mathilde Neuville
Bénédicte Neven
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Sevgi Keles
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Romain Hernu
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Antonin Bal
Antonio Novelli
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Giuseppe Novelli
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Kahina Saker
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Oana Ailioaie
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Arnau Antolí
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Gemma Rocamora-Blanch
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Carla Teixeira
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Clarisse Delaunay
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Marine Lhuillier
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Paul Le Turnier
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Yu Zhang
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Matthieu Mahevas
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Qiang Pan-Hammarström
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Hassan Abolhassani
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Thierry Bompoil
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Karim Dorgham
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Guy Gorochov
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Cédric Laouenan
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Carlos Rodríguez-Gallego
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Lisa F P Ng
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Laurent Renia
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Aurora Pujol
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Alexandre Belot
François Raffi
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Luis M Allende
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Javier Martinez-Picado
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Tayfun Ozcelik
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Sevgi Keles
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Luisa Imberti
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Luigi D Notarangelo
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Jesus Troya
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Xavier Solanich
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Shen-Ying Zhang
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Anne Puel
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Michael R Wilson
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Sophie Trouillet-Assant
Laurent Abel
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Emmanuelle Jouanguy
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Aurélie Cobat
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Leslie M Thompson
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Evangelos Andreakos
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Qian Zhang
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Mark S Anderson
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Joseph L Derisi
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Laurent Abel
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Cristian Achille
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Alessandro Aiuti
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Saleh Al-Muhsen
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Fahd Al-Mulla
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Mark S Anderson
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Evangelos Andreakos
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Micol Angelini
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Andrés A Arias
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Gokhan Aytekin
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Fausto Baldanti
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Hagit Baris Feldman
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Alexandre Belot
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Federica Bergami
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Catherine M Biggs
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Dusan Bogunovic
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Alexandre Bolze
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Anastasiia Bondarenko
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Petter Brodin
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Yenan Bryceson
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Murkesh Desai
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Beth A Drolet
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Recai Ergun
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Dilek Ergun
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Sara Espinosa-Padilla
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Jacques Fellay
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Carlos Flores
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Antoine Froidure
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Stefano Ghirardello
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Lennart Hammarström
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James R Heath
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Eystein Husebye
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Jérémie Guedj
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Alexandre Hoctin
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Ikram Houas
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Aldric Manuel
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France Mentré
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Amina Meziane
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Hugo Mouquet
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Jimmy Mullaert
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Nadège Neant
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Duc Nguyen
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Marion Noret
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Aurélie Papadopoulos
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Christelle Paul
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Nathan Peiffer-Smadja
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Vincent Peigne
Ventzislava Petrov-Sanchez
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Gilles Peytavin
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Huong Pham
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Olivier Picone
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Valentine Piquard
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Julien Poissy
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Oriane Puéchal
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Manuel Rosa-Calatrava
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Patrick Rossignol
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Carine Roy
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Marion Schneider
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Richa Su
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Coralie Tardivon
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Marie-Capucine Tellier
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François Téoulé
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Olivier Terrier
Jean-François Timsit
Christelle Tual
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Sarah Tubiana
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Sylvie van der Werf
Noémie Vanel
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Benoit Visseaux
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Aurélie Wiedemann
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Yazdan Yazdanpanah
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Abstract

Life-threatening ‘breakthrough’ cases of critical COVID-19 are attributed to poor or waning antibody response to the SARS-CoV-2 vaccine in individuals already at risk. Pre-existing autoantibodies (auto-Abs) neutralizing type I IFNs underlie at least 15% of critical COVID-19 pneumonia cases in unvaccinated individuals; however, their contribution to hypoxemic breakthrough cases in vaccinated people remains unknown. Here, we studied a cohort of 48 individuals (age 20-86 years) who received 2 doses of an mRNA vaccine and developed a breakthrough infection with hypoxemic COVID-19 pneumonia 2 weeks to 4 months later. Antibody levels to the vaccine, neutralization of the virus, and auto-Abs to type I IFNs were measured in the plasma. Forty-two individuals had no known deficiency of B cell immunity and a normal antibody response to the vaccine. Among them, ten (24%) had auto-Abs neutralizing type I IFNs (aged 43-86 years). Eight of these ten patients had auto-Abs neutralizing both IFN-α2 and IFN-ω, while two neutralized IFN-ω only. No patient neutralized IFN-β. Seven neutralized 10 ng/mL of type I IFNs, and three 100 pg/mL only. Seven patients neutralized SARS-CoV-2 D614G and the Delta variant (B.1.617.2) efficiently, while one patient neutralized Delta slightly less efficiently. Two of the three patients neutralizing only 100 pg/mL of type I IFNs neutralized both D61G and Delta less efficiently. Despite two mRNA vaccine inoculations and the presence of circulating antibodies capable of neutralizing SARS-CoV-2, auto-Abs neutralizing type I IFNs may underlie a significant proportion of hypoxemic COVID-19 pneumonia cases, highlighting the importance of this particularly vulnerable population.

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Immunology
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hal-03948899 , version 1 (20-01-2023)

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Paul Bastard, Sara Vazquez, Jamin Liu, Matthew T Laurie, Chung Yu Wang, et al.. Vaccine breakthrough hypoxemic COVID-19 pneumonia in patients with auto-Abs neutralizing type I IFNs. Science Immunology, 2022, 8 (90), ⟨10.1126/sciimmunol.abp8966⟩. ⟨hal-03948899⟩
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