Vaccine breakthrough hypoxemic COVID-19 pneumonia in patients with auto-Abs neutralizing type I IFNs
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Published:2022-06-14
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ISSN:2470-9468
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Container-title:Science Immunology
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language:en
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Short-container-title:Sci. Immunol.
Author:
Bastard Paul1234, Vazquez Sara567, Liu Jamin89, Laurie Matthew T.8, Wang Chung Yu10, Gervais Adrian12, Le Voyer Tom12, Bizien Lucy12, Zamecnik Colin11, Philippot Quentin12, Rosain Jérémie12, Catherinot Emilie12, Willmore Andrew10, Mitchell Anthea M.10, Bair Rebecca11, Garçon Pierre13, Kenney Heather14, Fekkar Arnaud1215, Salagianni Maria16, Poulakou Garyphallia17, Siouti Eleni16, Sahanic Sabina18, Tancevski Ivan18, Weiss Günter18, Nagl Laurenz19, Manry Jérémy12, Duvlis Sotirija2021, Arroyo-Sánchez Daniel22, Paz Artal Estela22, Rubio Luis8, Perani Cristiano23, Bezzi Michela24, Sottini Alessandra25, Quaresima Virginia25, Roussel Lucie2627, Vinh Donald C.2627, Reyes Luis Felipe2829, Garzaro Margaux30, Hatipoglu Nevin31, Boutboul David32, Tandjaoui-Lambiotte Yacine333435, Borghesi Alessandro36, Aliberti Anna37, Cassaniti Irene38, Venet Fabienne394041, Monneret Guillaume3940, Halwani Rabih4243, Sharif-Askari Narjes Saheb42, Danielson Jeffrey14, Burrel Sonia44, Morbieu Caroline45, Stepanovskyy Yurii46, Bondarenko Anastasia46, Volokha Alla46, Boyarchuk Oksana47, Gagro Alenka48, Neuville Mathilde49, Neven Bénédicte50, Keles Sevgi51, Hernu Romain52, Bal Antonin53, Novelli Antonio54, Novelli Giuseppe55, Saker Kahina56, Ailioaie Oana57, Antolí Arnau58, Jeziorski Eric59, Rocamora-Blanch Gemma58, Teixeira Carla60, Delaunay Clarisse61, Lhuillier Marine62, Le Turnier Paul61, Zhang Yu1463, Mahevas Matthieu646566, Pan-Hammarström Qiang67, Abolhassani Hassan67, Bompoil Thierry68, Dorgham Karim69, Gorochov Guy6970, Laouenan Cédric337172, Rodríguez-Gallego Carlos7374, Ng Lisa F. P.75, Renia Laurent757677, Pujol Aurora78, Belot Alexandre5679, Raffi François61, Allende Luis M.22, Martinez-Picado Javier80818283, Ozcelik Tayfun84, Keles Sevgi51, Imberti Luisa25, Notarangelo Luigi D.14, Troya Jesus85, Solanich Xavier58, Zhang Shen-Ying123, Puel Anne123, Wilson Michael R11, Trouillet-Assant Sophie86, Abel Laurent123, Jouanguy Emmanuelle123, Ye Chun Jimmie1087888990, Cobat Aurélie123, Thompson Leslie M.91, Andreakos Evangelos16, Zhang Qian123, Anderson Mark S.792, Casanova Jean-Laurent123493, DeRisi Joseph L.810, Abel Laurent, Achille Cristian, Aiuti Alessandro, Al-Muhsen Saleh, Al-Mulla Fahd, Anderson Mark S., Andreakos Evangelos, Angelini Micol, Arias Andrés A., Aytekin Gokhan, Baldanti Fausto, Feldman Hagit Baris, Belot Alexandre, Bergami Federica, Biggs Catherine M., Bogunovic Dusan, Bolze Alexandre, Bondarenko Anastasiia, Bousfiha Ahmed A., Brodin Petter, Bryceson Yenan, Bustamante Carlos D., Butte Manish J., Casari Giorgio, Christodoulou John, Condino-Neto Antonio, Constantinescu Stefan N., Conti Francesca, Cooper Megan A., Dalgard Clifton L., Desai Murkesh, Drolet Beth A., El Baghdadi Jamila, Ergun Recai, Ergun Dilek, Espinosa-Padilla Sara, Fellay Jacques, Flores Carlos, Franco José Luis, Froidure Antoine, Ghirardello Stefano, Gregersen Peter K., Grimbacher Bodo, Haerynck Filomeen, Hagin David, Halwani Rabih, Hammarström Lennart, Heath James R., Henrickson Sarah E., Hsieh Elena W.Y., Husebye Eystein, Imai Kohsuke, Itan Yuval, Jarvis Erich D., Kanat Fikret, Karamitros Timokratis, Kisand Kai, Kopcha Vasyl, Korda Mykhaylo, Ku Cheng-Lung, Lau Yu-Lung, Ling Yun, Lucas Carrie L., Maniatis Tom, Mansouri Davood, Maródi László, Meyts Isabelle, Milner Joshua D., Mironska Kristina, Mogensen Trine H., Mojoli Francesco, Morandeira Francisco, Morio Tomohiro, Ng Lisa F.P., Notarangelo Luigi D., Novelli Antonio, Novelli Giuseppe, O'Farrelly Cliona, Okada Satoshi, Okamoto Keisuke, Ozcelik Tayfun, Pagani Michele, Pan-Hammarström Qiang, Pape Jean W., de Diego Rebeca Perez, Perlin David S., Pesole Graziano, Pession Andrea, Piralla Antonio, Planas Anna M., Prando Carolina, Pujol Aurora, Quintana-Murci Lluis, Ramaswamy Sathishkumar, Renia Laurent, Resnick Igor, Rigo-Bonnin Raúl, Rodríguez-Gallego Carlos, Sancho-Shimizu Vanessa, Sediva Anna, Seppänen Mikko R.J., Shahrooei Mohammed, Shcherbina Anna, Slaby Ondrej, Snow Andrew L., Soler-Palacín Pere, Spaan András N., Tancevski Ivan, Tangye Stuart G., Abou Tayoun Ahmad, Tulek Baykal, Turvey Stuart E., Uddin K M Furkan, Uddin Mohammed, Clément Bénédicte, Abe-Jones Yumiko, Asthana Saurabh, Bhide Sharvari, Calfee Carolyn S., Carrillo Sidney A., Chak Suzanna, Collins Zachary, Erle David J., Fragiadakis Gabriela K., Ghale Rajani, Hendrickson Carolyn M., Jauregui Alejandra, Kangelaris Kirsten N., Krummel Matthew F., Langelier Charles R., Lea Tasha, Lee Deanna, Leligdowicz Aleksandra, Leroux Carolyn, Lota Raphael, Matthay Michael, Nguyen Viet, Patel Ravi, Pierce Logan, Prasad Priya, Rao Arjun Arkal, Rashid Ahmad, Rodriguez Nicklaus, Samad Bushra, Shaw Cole, Sigman Austin, Tang Kevin, Altamirano Luz Torres, Ward Alyssa, Willmore Andrew, Wilson Michael, Woodruff Prescott G., Abel Laurent, Allavena Clotilde, Andrejak Claire, Angoulvant François, Azoulay Cecile, Bachelet Delphine, Bartoli Marie, Basmaci Romain, Behilill Sylvie, Beluze Marine, Benech Nicolas, Benkerrou Dehbia, Bhavsar Krishna, Bitker Laurent, Bouadma Lila, Bouscambert Maude, Paz Pauline Caraux, Cervantes-Gonzalez Minerva, Chair Anissa, Chirouze Catherine, Coelho Alexandra, Cordel Hugues, Couffignal Camille, Couffin-Cadiergues Sandrine, d’Ortenzio Eric, De Montmollin Etienne, Debard Alexa, Debray Marie-Pierre, Deplanque Dominique, Descamps Diane, Desvallée Mathilde, Diallo Alpha, Diehl Jean-Luc, Diouf Alphonsine, Dorival Céline, Dubos François, Duval Xavier, Eloy Philippine, Enouf Vincent, Epaulard Olivier, Esperou Hélène, Esposito-Farese Marina, Etienne Manuel, Garot Denis, Gault Nathalie, Gaymard Alexandre, Ghosn Jade, Gigante Tristan, Gilg Morgane, Goehringer François, Guedj Jérémie, Hoctin Alexandre, Hoffmann Isabelle, Houas Ikram, Hulot Jean-Sébastien, Jaafoura Salma, Kafif Ouifiya, Kaguelidou Florentia, Kali Sabrina, Kerroumi Younes, Khalil Antoine, Khan Coralie, Kimmoun Antoine, Laine Fabrice, Laouénan Cédric, Laribi Samira, Le Minh, Le Bris Cyril, Le Gac Sylvie, Le Hingrat Quentin, Le Mestre Soizic, Le Nagard Hervé, Lemaignen Adrien, Lemee Véronique, Lescure François-Xavier, Letrou Sophie, Levy Yves, Lina Bruno, Lingas Guillaume, Lucet Jean Christophe, Machado Moïse, Malvy Denis, Mambert Marina, Manuel Aldric, Mentré France, Meziane Amina, Mouquet Hugo, Mullaert Jimmy, Neant Nadège, Nguyen Duc, Noret Marion, Papadopoulos Aurélie, Paul Christelle, Peiffer-Smadja Nathan, Peigne Vincent, Petrov-Sanchez Ventzislava, Peytavin Gilles, Pham Huong, Picone Olivier, Piquard Valentine, Poissy Julien, Puéchal Oriane, Rosa-Calatrava Manuel, Rossignol Bénédicte, Rossignol Patrick, Roy Carine, Schneider Marion, Su Richa, Tardivon Coralie, Tellier Marie-Capucine, Téoulé François, Terrier Olivier, Timsit Jean-François, Tual Christelle, Tubiana Sarah, Van Der Werf Sylvie, Vanel Noémie, Veislinger Aurélie, Visseaux Benoit, Wiedemann Aurélie, Yazdanpanah Yazdan, , ,
Affiliation:
1. Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France. 2. University of Paris Cité, Imagine Institute, Paris, France. 3. St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA. 4. Department of Pediatrics, Necker Hospital for Sick Children, AP-HP, Paris, France. 5. Medical Scientist Training Program, University of California, San Francisco, San Francisco, CA 94143, USA. 6. Tetrad Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA. 7. Diabetes Center, University of California, San Francisco, San Francisco, CA 94143, USA. 8. Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA. 9. University of California, Berkeley-University of California, San Francisco Graduate Program in Bioengineering, University of California, San Francisco, California, United States. 10. Chan Zuckerberg Biohub, San Francisco, CA 94158, USA. 11. Weill Institute for Neurosciences, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. 12. Pneumology Department, Foch Hospital, Suresne, France. 13. Intensive Care Unit, Grand Hôpital de l'Est Francilien Site de Marne-la-Vallée, Jossigny, France. 14. Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD, USA. 15. Service de Parasitologie-Mycologie, Groupe Hospitalier Pitié Salpêtrière, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France. 16. Laboratory of Immunobiology, Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation of the Academy of Athens, Athens, Greece. 17. 3rd Department of Internal Medicine, National and Kapodistrian University of Athens, Medical School, ‘’Sotiria’’ General Hospital of Chest Diseases, Athens, Greece. 18. Department of Internal Medicine II, Medical University of Innsbruck, Innsbruck, Austria. 19. Department of Internal Medicine V, Medical University of Innsbruck, Innsbruck, Austria. 20. Faculty of Medical Sciences, University “Goce Delchev”, Stip, Republic of North Macedonia. 21. Institute of public health of Republic of North Macedonia. 22. Department of Immunology, Instituto de Investigación Sanitaria Hospital 12 de Octubre (imas12) and Department of Immunology, Ophthalmology and ENT, Complutense University School of Medicine, CIBERINFEC, Madrid, Spain. 23. Emergency Room, ASST Spedali Civili di Brescia, Brescia, Italy. 24. Covid Unit, ASST Spedali Civili, Brescia, Italy. 25. CREA Laboratory, Diagnostic Department, ASST Spedali Civili di Brescia, Brescia, Italy. 26. Department of Medicine, Division of Infectious Diseases, McGill University Health Centre, Montréal, Québec, Canada. 27. Infectious Disease Susceptibility Program, Research Institute-McGill University Health Centre, Montréal, Québec, Canada. 28. Department of Microbiology, Universidad de La Sabana, Chía, Colombia. 29. Department of Critical Care Medicine, Clínica Universidad de La Sabana, Chía, Colombia. 30. Department of Infectious Diseases, Necker Hospital for Sick Children, AP-HP, Paris, France. 31. Pediatric Infectious Diseases Unit, Bakirkoy Dr. Sadi Konuk Training and Research Hospital, University of Health Sciences, Istanbul, Turkey. 32. Department of Immunology, Saint-Louis Hospital, AP-HP, Paris, France. 33. INSERM UMR 1137 IAME, Paris, France. 34. INSERM UMR 1272 Hypoxie & Poumon, Bobigny, France. 35. Pneumology and infectiology department, CH Saint Denis, Saint-Denis, France. 36. Neonatal Intensive Care Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy. 37. Anesthesia and Intensive Care, Rianimazione I, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy. 38. Molecular Virology Unit, Microbiology and Virology Department, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy. 39. Laboratoire d’Immunologie, Hospices Civils de Lyon, Hôpital Edouard Herriot, Lyon, France. 40. EA 7426, Pathophysiology of Injury-Induced Immunosuppression, Université Claude Bernard Lyon 1, Hospices Civils de Lyon, Hôpital Edouard Herriot-BioMérieux, Lyon, France. 41. CIRI, INSERM U1111, CNRS, UMR5308, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, Lyon, France. 42. Sharjah Institute for Medical Research, College of Medicine, University of Sharjah, Sharjah, United Arab Emirates. 43. Immunology Research Laboratory, College of Medicine, King Saud University. 44. Sorbonne Université, INSERM U1136, Institut Pierre Louis d'Epidémiologie et de Santé Publique (iPLESP), AP-HP, Hôpital Pitié Salpêtrière, Service de Virologie, Paris, France. 45. Internal medicine department, Louis Mourier Hospital, AP-HP, Paris, France. 46. Shupyk National Healthcare University of Ukraine, Kyiv, Ukraine. 47. Department of Children's Diseases and Pediatric Surgery, I.Horbachevsky Ternopil National Medical University, Ternopil, Ukraine. 48. Department of Pediatrics, Children's Hospital Zagreb, University of Zagreb School of Medicine, Zagreb, Josip Juraj Strossmayer University of Osijek, Medical Faculty Osijek, Osijek, Croatia. 49. Intensive care unit, Foch Hospital, Suresne, France. 50. Department of Pediatrics Hematology Immunology and Rheumatology, Necker Hospital for Sick Children, AP-HP, Paris, France. 51. Meram Medical Faculty, Necmettin Erbakan University, Meram Medical Faculty, Konya, Turkey. 52. Service des Urgences, Groupement Hospitalier Nord, Hospices Civils de Lyon, Lyon, France. 53. Laboratoire de virologie, Institut agent infectieux, Groupement Hospitalier Nord, Hospices Civils de Lyon, Lyon, France. 54. Laboratory of Medical Genetics, IRCCS Bambino Gesù Children’s Hospital, Rome, Italy. 55. Department of Biomedicine and Prevention, Tor Vergata University of Rome, Rome, Italy. 56. Joint Research Unit, Hospices Civils de Lyon-bio Mérieux, Hospices Civils de Lyon, Lyon Sud Hospital, Pierre-Bénite, France; International Center of Research in Infectiology, Lyon University, INSERM U1111, CNRS UMR 5308, ENS, UCBL, Lyon, France. 57. Service de Génétique, Hôpital Raymond Poincaré, AP-HP, Garches, France. 58. Department of Internal Medicine, Hospital Universitari de Bellvitge, IDIBELL, Barcelona, Spain. 59. General pediatric department, PCCEI, CeRéMAIA, Univ Montpellier, CHU Montpellier, Montpellier, France. 60. Unidade de Infeciologia e Imunodeficiências, Centro Materno-infantil do Norte, Centro Hospitalar Universitário do Porto, Porto, Portugal. 61. Department of Infectious Diseases, CHU Nantes, and INSERM UIC 1413, CHU Nantes, France. 62. Geriatric department, CHU Nantes, Hopital Bellier, Nantes, France. 63. NIAID Clinical Genomics Program, National Institutes of Health, Bethesda, USA 64. Necker Enfants Malades Institute (INEM), INSERM U1151/CNRS UMR 8253, University of Paris Cité, Paris, France. 65. Departement of Internal Medicine, Henri Mondor University Hospital, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris-Est Créteil University (UPEC), Créteil, France. 66. INSERM U955, team 2. Mondor Biomedical Research Institute (IMRB), Paris-Est Créteil University (UPEC), Créteil, France. 67. Department of Biosciences and Nutrition, Karolinska Institutet, SE14183, Huddinge, Sweden. 68. Biologie/Pathologie, CHU-Nantes - Hôtel Dieu, Institut de Biologie, Nantes, France 69. Sorbonne Université, Inserm, Centre d’Immunologie et des Maladies Infectieuses, (CIMI- Paris), Paris, France. 70. Département d’Immunologie, Assistance Publique Hôpitaux de Paris (AP-HP), Hôpital Pitié-Salpétrière, Paris, France. 71. Université de Paris, IAME UMR-S 1137, INSERM, Paris, France. 72. AP-HP, Département Epidémiologie Biostatistiques et Recherche Clinique, Hôpital Bichat, Paris, France. 73. Department of Clinical Sciences, University Fernando Pessoa Canarias, Las Palmas de Gran Canaria, Canary Islands, Spain. 74. Department of Immunology, University Hospital of Gran Canaria Dr. Negrín, Canarian Health System, Las Palmas de Gran Canaria, Spain. 75. A*STAR Infectious Disease Labs, Agency for Science, Technology and Research, Singapore. 76. Lee Kong Chian School of Medicine, Nanyang Technology University, Singapore. 77. School of Biological Sciences, Nanyang Technology University, Singapore. 78. Neurometabolic Diseases Laboratory, IDIBELL-Hospital Duran i Reynals, CIBERER U759, and Catalan Institution of Research and Advanced Studies (ICREA), Barcelona, Spain. 79. CNRS UMR 5308, ENS, UCBL, Lyon, France; National Referee Centre for Rheumatic, and Autoimmune and Systemic Diseases in Children (RAISE), Lyon, France; Lyon; Immunopathology Federation LIFE, Hospices Civils de Lyon, Lyon, France. 80. IrsiCaixa AIDS Research Institute and Institute for Health Science Research Germans Trias i Pujol (IGTP), Badalona, Spain. 81. Infectious Diseases and Immunity, Center for Health and Social Care Research (CESS), Faculty of Medicine, University of Vic-Central University of Catalonia (UVic-UCC), Vic, Spain. 82. Catalan Institution for Research and Advanced Studies (ICREA), Barcelona, Spain. 83. CIBER de Enfermedades Infecciosas, Instituto de Salud Carlos III, Madrid, Spain. 84. Department of Molecular Biology and Genetics, Bilkent University, Bilkent - Ankara, Turkey. 85. Department of Internal Medicine, Infanta Leonor University Hospital, Madrid, Spain. 86. Hospices Civils de Lyon, Lyon, France; International Center of Research in Infectiology, Lyon University, INSERM U1111, CNRS UMR 5308, ENS, UCBL, Lyon, France. 87. ImmunoX Initiative, University of California, San Francisco, San Francisco, CA 94143, USA. 88. Departments of Epidemiology and Biostatistics and Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94143, USA. 89. Bakar Computational Health Sciences Institute, University of California, San Francisco, San Francisco, CA 94143, USA. 90. Parker Institute for Cancer Immunotherapy, San Francisco, CA 94129, USA. 91. Departments of Psychiatry and Human Behavior and Neurobiology and Behavior, University of California, Irvine, CA, USA. 92. Division of Endocrinology and Metabolism, Department of Medicine, University of California, San Francisco, San Francisco, CA 94143, USA. 93. Howard Hughes Medical Institute, New York, NY, USA.
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.
Publisher
American Association for the Advancement of Science (AAAS)
Subject
General Medicine,Immunology
Cited by
46 articles.
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