Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children

Paul Bastard; Adrian Gervais; Maki Taniguchi; Liisa Saare; Karita Särekannu; Tom Le Voyer; Quentin Philippot; Jérémie Rosain; Lucy Bizien; Takaki Asano; Marina Garcia-Prat; Alba Parra-Martínez; Mélanie Migaud; Miyuki Tsumura; Francesca Conti; Alexandre Belot; Jacques G Rivière; Tomohiro Morio; Junko Tanaka; Etienne Javouhey; Filomeen Haerynck; Sotirija Duvlis; Tayfun Ozcelik; Sevgi Keles; Yacine Tandjaoui-Lambiotte; Simon Escoda; Maya Husain; Qiang Pan-Hammarström; Lennart Hammarström; Gloria Ahlijah; Anthony Abi Haidar; Camille Soudee; Vincent Arseguel; Hassan Abolhassani; Sabina Sahanic; Ivan Tancevski; Yoko Nukui; Seiichi Hayakawa; George P Chrousos; Athanasios Michos; Elizabeth-Barbara Tatsi; Filippos Filippatos; Agusti Rodriguez-Palmero; Jesus Troya; Imran Tipu; Isabelle Meyts; Lucie Roussel; Sisse Rye Ostrowski; Laire Schidlowski; Carolina Prando; COVID
                                        Clinicians; Jean-Laurent Casanova

doi:10.1084/jem.20231353

Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children

Paul Bastard^*, Adrian Gervais, Maki Taniguchi, Liisa Saare, Karita Särekannu, Tom Le Voyer, Quentin Philippot, Jérémie Rosain, Lucy Bizien, Takaki Asano, Marina Garcia-Prat, Alba Parra-Martínez, Mélanie Migaud, Miyuki Tsumura, Francesca Conti, Alexandre Belot, Jacques G Rivière, Tomohiro Morio, Junko Tanaka, Etienne JavouheyFilomeen Haerynck, Sotirija Duvlis, Tayfun Ozcelik, Sevgi Keles, Yacine Tandjaoui-Lambiotte, Simon Escoda, Maya Husain, Qiang Pan-Hammarström, Lennart Hammarström, Gloria Ahlijah, Anthony Abi Haidar, Camille Soudee, Vincent Arseguel, Hassan Abolhassani, Sabina Sahanic, Ivan Tancevski, Yoko Nukui, Seiichi Hayakawa, George P Chrousos, Athanasios Michos, Elizabeth-Barbara Tatsi, Filippos Filippatos, Agusti Rodriguez-Palmero, Jesus Troya, Imran Tipu, Isabelle Meyts, Lucie Roussel, Sisse Rye Ostrowski, Laire Schidlowski, Carolina Prando, COVID Clinicians, Jean-Laurent Casanova^*

^*Corresponding author af dette arbejde

Afdeling for Klinisk Immunologi

14 Citationer (Scopus)

Abstract

We found that 19 (10.4%) of 183 unvaccinated children hospitalized for COVID-19 pneumonia had autoantibodies (auto-Abs) neutralizing type I IFNs (IFN-α2 in 10 patients: IFN-α2 only in three, IFN-α2 plus IFN-ω in five, and IFN-α2, IFN-ω plus IFN-β in two; IFN-ω only in nine patients). Seven children (3.8%) had Abs neutralizing at least 10 ng/ml of one IFN, whereas the other 12 (6.6%) had Abs neutralizing only 100 pg/ml. The auto-Abs neutralized both unglycosylated and glycosylated IFNs. We also detected auto-Abs neutralizing 100 pg/ml IFN-α2 in 4 of 2,267 uninfected children (0.2%) and auto-Abs neutralizing IFN-ω in 45 children (2%). The odds ratios (ORs) for life-threatening COVID-19 pneumonia were, therefore, higher for auto-Abs neutralizing IFN-α2 only (OR [95% CI] = 67.6 [5.7-9,196.6]) than for auto-Abs neutralizing IFN-ω only (OR [95% CI] = 2.6 [1.2-5.3]). ORs were also higher for auto-Abs neutralizing high concentrations (OR [95% CI] = 12.9 [4.6-35.9]) than for those neutralizing low concentrations (OR [95% CI] = 5.5 [3.1-9.6]) of IFN-ω and/or IFN-α2.

Originalsprog	Engelsk
Artikelnummer	e20231353
Tidsskrift	Journal of Experimental Medicine
Vol/bind	221
Udgave nummer	2
ISSN	0022-1007
DOI	https://doi.org/10.1084/jem.20231353
Status	Udgivet - 5 feb. 2024

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10.1084/jem.20231353Licens: CC BY

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Bastard, P., Gervais, A., Taniguchi, M., Saare, L., Särekannu, K., Le Voyer, T., Philippot, Q., Rosain, J., Bizien, L., Asano, T., Garcia-Prat, M., Parra-Martínez, A., Migaud, M., Tsumura, M., Conti, F., Belot, A., Rivière, J. G., Morio, T., Tanaka, J., ... Casanova, J.-L. (2024). Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children. Journal of Experimental Medicine, 221(2), Artikel e20231353. https://doi.org/10.1084/jem.20231353

Bastard, P, Gervais, A, Taniguchi, M, Saare, L, Särekannu, K, Le Voyer, T, Philippot, Q, Rosain, J, Bizien, L, Asano, T, Garcia-Prat, M, Parra-Martínez, A, Migaud, M, Tsumura, M, Conti, F, Belot, A, Rivière, JG, Morio, T, Tanaka, J, Javouhey, E, Haerynck, F, Duvlis, S, Ozcelik, T, Keles, S, Tandjaoui-Lambiotte, Y, Escoda, S, Husain, M, Pan-Hammarström, Q, Hammarström, L, Ahlijah, G, Abi Haidar, A, Soudee, C, Arseguel, V, Abolhassani, H, Sahanic, S, Tancevski, I, Nukui, Y, Hayakawa, S, Chrousos, GP, Michos, A, Tatsi, E-B, Filippatos, F, Rodriguez-Palmero, A, Troya, J, Tipu, I, Meyts, I, Roussel, L, Ostrowski, SR, Schidlowski, L, Prando, C, COVID Clinicians & Casanova, J-L 2024, 'Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children', Journal of Experimental Medicine, bind 221, nr. 2, e20231353. https://doi.org/10.1084/jem.20231353

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title = "Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children",

abstract = "We found that 19 (10.4%) of 183 unvaccinated children hospitalized for COVID-19 pneumonia had autoantibodies (auto-Abs) neutralizing type I IFNs (IFN-α2 in 10 patients: IFN-α2 only in three, IFN-α2 plus IFN-ω in five, and IFN-α2, IFN-ω plus IFN-β in two; IFN-ω only in nine patients). Seven children (3.8%) had Abs neutralizing at least 10 ng/ml of one IFN, whereas the other 12 (6.6%) had Abs neutralizing only 100 pg/ml. The auto-Abs neutralized both unglycosylated and glycosylated IFNs. We also detected auto-Abs neutralizing 100 pg/ml IFN-α2 in 4 of 2,267 uninfected children (0.2%) and auto-Abs neutralizing IFN-ω in 45 children (2%). The odds ratios (ORs) for life-threatening COVID-19 pneumonia were, therefore, higher for auto-Abs neutralizing IFN-α2 only (OR [95% CI] = 67.6 [5.7-9,196.6]) than for auto-Abs neutralizing IFN-ω only (OR [95% CI] = 2.6 [1.2-5.3]). ORs were also higher for auto-Abs neutralizing high concentrations (OR [95% CI] = 12.9 [4.6-35.9]) than for those neutralizing low concentrations (OR [95% CI] = 5.5 [3.1-9.6]) of IFN-ω and/or IFN-α2.",

keywords = "COVID-19, Immunodeficiency, Infectious disease and host defense, Innate immunity and inflammation",

author = "Paul Bastard and Adrian Gervais and Maki Taniguchi and Liisa Saare and Karita S{\"a}rekannu and {Le Voyer}, Tom and Quentin Philippot and J{\'e}r{\'e}mie Rosain and Lucy Bizien and Takaki Asano and Marina Garcia-Prat and Alba Parra-Mart{\'i}nez and M{\'e}lanie Migaud and Miyuki Tsumura and Francesca Conti and Alexandre Belot and Rivi{\`e}re, {Jacques G} and Tomohiro Morio and Junko Tanaka and Etienne Javouhey and Filomeen Haerynck and Sotirija Duvlis and Tayfun Ozcelik and Sevgi Keles and Yacine Tandjaoui-Lambiotte and Simon Escoda and Maya Husain and Qiang Pan-Hammarstr{\"o}m and Lennart Hammarstr{\"o}m and Gloria Ahlijah and {Abi Haidar}, Anthony and Camille Soudee and Vincent Arseguel and Hassan Abolhassani and Sabina Sahanic and Ivan Tancevski and Yoko Nukui and Seiichi Hayakawa and Chrousos, {George P} and Athanasios Michos and Elizabeth-Barbara Tatsi and Filippos Filippatos and Agusti Rodriguez-Palmero and Jesus Troya and Imran Tipu and Isabelle Meyts and Lucie Roussel and Ostrowski, {Sisse Rye} and Laire Schidlowski and Carolina Prando and {COVID Clinicians} and Jean-Laurent Casanova",

note = "{\textcopyright} 2024 Bastard et al.",

year = "2024",

month = feb,

day = "5",

doi = "10.1084/jem.20231353",

language = "English",

volume = "221",

journal = "Journal of Experimental Medicine",

issn = "0022-1007",

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TY - JOUR

T1 - Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children

AU - Bastard, Paul

AU - Gervais, Adrian

AU - Taniguchi, Maki

AU - Saare, Liisa

AU - Särekannu, Karita

AU - Le Voyer, Tom

AU - Philippot, Quentin

AU - Rosain, Jérémie

AU - Bizien, Lucy

AU - Asano, Takaki

AU - Garcia-Prat, Marina

AU - Parra-Martínez, Alba

AU - Migaud, Mélanie

AU - Tsumura, Miyuki

AU - Conti, Francesca

AU - Belot, Alexandre

AU - Rivière, Jacques G

AU - Morio, Tomohiro

AU - Tanaka, Junko

AU - Javouhey, Etienne

AU - Haerynck, Filomeen

AU - Duvlis, Sotirija

AU - Ozcelik, Tayfun

AU - Keles, Sevgi

AU - Tandjaoui-Lambiotte, Yacine

AU - Escoda, Simon

AU - Husain, Maya

AU - Pan-Hammarström, Qiang

AU - Hammarström, Lennart

AU - Ahlijah, Gloria

AU - Abi Haidar, Anthony

AU - Soudee, Camille

AU - Arseguel, Vincent

AU - Abolhassani, Hassan

AU - Sahanic, Sabina

AU - Tancevski, Ivan

AU - Nukui, Yoko

AU - Hayakawa, Seiichi

AU - Chrousos, George P

AU - Michos, Athanasios

AU - Tatsi, Elizabeth-Barbara

AU - Filippatos, Filippos

AU - Rodriguez-Palmero, Agusti

AU - Troya, Jesus

AU - Tipu, Imran

AU - Meyts, Isabelle

AU - Roussel, Lucie

AU - Ostrowski, Sisse Rye

AU - Schidlowski, Laire

AU - Prando, Carolina

AU - COVID Clinicians

AU - Casanova, Jean-Laurent

PY - 2024/2/5

Y1 - 2024/2/5

N2 - We found that 19 (10.4%) of 183 unvaccinated children hospitalized for COVID-19 pneumonia had autoantibodies (auto-Abs) neutralizing type I IFNs (IFN-α2 in 10 patients: IFN-α2 only in three, IFN-α2 plus IFN-ω in five, and IFN-α2, IFN-ω plus IFN-β in two; IFN-ω only in nine patients). Seven children (3.8%) had Abs neutralizing at least 10 ng/ml of one IFN, whereas the other 12 (6.6%) had Abs neutralizing only 100 pg/ml. The auto-Abs neutralized both unglycosylated and glycosylated IFNs. We also detected auto-Abs neutralizing 100 pg/ml IFN-α2 in 4 of 2,267 uninfected children (0.2%) and auto-Abs neutralizing IFN-ω in 45 children (2%). The odds ratios (ORs) for life-threatening COVID-19 pneumonia were, therefore, higher for auto-Abs neutralizing IFN-α2 only (OR [95% CI] = 67.6 [5.7-9,196.6]) than for auto-Abs neutralizing IFN-ω only (OR [95% CI] = 2.6 [1.2-5.3]). ORs were also higher for auto-Abs neutralizing high concentrations (OR [95% CI] = 12.9 [4.6-35.9]) than for those neutralizing low concentrations (OR [95% CI] = 5.5 [3.1-9.6]) of IFN-ω and/or IFN-α2.

AB - We found that 19 (10.4%) of 183 unvaccinated children hospitalized for COVID-19 pneumonia had autoantibodies (auto-Abs) neutralizing type I IFNs (IFN-α2 in 10 patients: IFN-α2 only in three, IFN-α2 plus IFN-ω in five, and IFN-α2, IFN-ω plus IFN-β in two; IFN-ω only in nine patients). Seven children (3.8%) had Abs neutralizing at least 10 ng/ml of one IFN, whereas the other 12 (6.6%) had Abs neutralizing only 100 pg/ml. The auto-Abs neutralized both unglycosylated and glycosylated IFNs. We also detected auto-Abs neutralizing 100 pg/ml IFN-α2 in 4 of 2,267 uninfected children (0.2%) and auto-Abs neutralizing IFN-ω in 45 children (2%). The odds ratios (ORs) for life-threatening COVID-19 pneumonia were, therefore, higher for auto-Abs neutralizing IFN-α2 only (OR [95% CI] = 67.6 [5.7-9,196.6]) than for auto-Abs neutralizing IFN-ω only (OR [95% CI] = 2.6 [1.2-5.3]). ORs were also higher for auto-Abs neutralizing high concentrations (OR [95% CI] = 12.9 [4.6-35.9]) than for those neutralizing low concentrations (OR [95% CI] = 5.5 [3.1-9.6]) of IFN-ω and/or IFN-α2.

KW - COVID-19

KW - Immunodeficiency

KW - Infectious disease and host defense

KW - Innate immunity and inflammation

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U2 - 10.1084/jem.20231353

DO - 10.1084/jem.20231353

M3 - Journal article

C2 - 38175961

SN - 0022-1007

VL - 221

JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

IS - 2

M1 - e20231353

ER -

Higher COVID-19 pneumonia risk associated with anti-IFN-α than with anti-IFN-ω auto-Abs in children

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