Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19

Nicole L. Messina; Susie Germano; Rebecca McElroy; Rajeev Rudraraju; Rhian Bonnici; Laure F. Pittet; Melanie R. Neeland; Suellen Nicholson; Kanta Subbarao; Nigel Curtis; the BRACE trial; Saoirse Benson; Stephen Blake; John Campbell; Andrew Dunn; Jane James; Tony Korman; David Lynn; Miriam Lynn; Natalie Stevens; Steve Wesselingh

doi:10.1002/cti2.1387

Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19

Nicole L. Messina, Susie Germano, Rebecca McElroy, Rajeev Rudraraju, Rhian Bonnici, Laure F. Pittet, Melanie R. Neeland, Suellen Nicholson, Kanta Subbarao, Nigel Curtis, the BRACE trial, Saoirse Benson, Stephen Blake, John Campbell, Andrew Dunn, Jane James, Tony Korman, David Lynn, Miriam Lynn, Natalie StevensSteve Wesselingh

Research output: Contribution to journal › Article › peer-review

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Abstract

Background and objectives: Because of its beneficial off-target effects against non-mycobacterial infectious diseases, bacillus Calmette–Guérin (BCG) vaccination might be an accessible early intervention to boost protection against novel pathogens. Multiple epidemiological studies and randomised controlled trials (RCTs) are investigating the protective effect of BCG against coronavirus disease 2019 (COVID-19). Using samples from participants in a placebo-controlled RCT aiming to determine whether BCG vaccination reduces the incidence and severity of COVID-19, we investigated the immunomodulatory effects of BCG on in vitro immune responses to SARS-CoV-2. Methods: This study used peripheral blood taken from participants in the multicentre RCT and BCG vaccination to reduce the impact of COVID-19 on healthcare workers (BRACE trial). The whole blood taken from BRACE trial participants was stimulated with γ-irradiated SARS-CoV-2-infected or mock-infected Vero cell supernatant. Cytokine responses were measured by multiplex cytokine analysis, and single-cell immunophenotyping was made by flow cytometry. Results: BCG vaccination, but not placebo vaccination, reduced SARS-CoV-2-induced secretion of cytokines known to be associated with severe COVID-19, including IL-6, TNF-α and IL-10. In addition, BCG vaccination promoted an effector memory phenotype in both CD4⁺ and CD8⁺ T cells, and an activation of eosinophils in response to SARS-CoV-2. Conclusions: The immunomodulatory signature of BCG’s off-target effects on SARS-CoV-2 is consistent with a protective immune response against severe COVID-19.

Original language	English
Article number	e1387
Number of pages	15
Journal	Clinical and Translational Immunology
Volume	11
Issue number	4
DOIs	https://doi.org/10.1002/cti2.1387
Publication status	Published - Jan 2022

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

BCG
COVID-19
cytokine
immunoregulation
SARS-CoV-2
T cell

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Messina, N. L., Germano, S., McElroy, R., Rudraraju, R., Bonnici, R., Pittet, L. F., Neeland, M. R., Nicholson, S., Subbarao, K., Curtis, N., the BRACE trial, Benson, S., Blake, S., Campbell, J., Dunn, A., James, J., Korman, T., Lynn, D., Lynn, M., ... Wesselingh, S. (2022). Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19. Clinical and Translational Immunology, 11(4), Article e1387. https://doi.org/10.1002/cti2.1387

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title = "Off-target effects of bacillus Calmette–Gu{\'e}rin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19",

abstract = "Background and objectives: Because of its beneficial off-target effects against non-mycobacterial infectious diseases, bacillus Calmette–Gu{\'e}rin (BCG) vaccination might be an accessible early intervention to boost protection against novel pathogens. Multiple epidemiological studies and randomised controlled trials (RCTs) are investigating the protective effect of BCG against coronavirus disease 2019 (COVID-19). Using samples from participants in a placebo-controlled RCT aiming to determine whether BCG vaccination reduces the incidence and severity of COVID-19, we investigated the immunomodulatory effects of BCG on in vitro immune responses to SARS-CoV-2. Methods: This study used peripheral blood taken from participants in the multicentre RCT and BCG vaccination to reduce the impact of COVID-19 on healthcare workers (BRACE trial). The whole blood taken from BRACE trial participants was stimulated with γ-irradiated SARS-CoV-2-infected or mock-infected Vero cell supernatant. Cytokine responses were measured by multiplex cytokine analysis, and single-cell immunophenotyping was made by flow cytometry. Results: BCG vaccination, but not placebo vaccination, reduced SARS-CoV-2-induced secretion of cytokines known to be associated with severe COVID-19, including IL-6, TNF-α and IL-10. In addition, BCG vaccination promoted an effector memory phenotype in both CD4+ and CD8+ T cells, and an activation of eosinophils in response to SARS-CoV-2. Conclusions: The immunomodulatory signature of BCG{\textquoteright}s off-target effects on SARS-CoV-2 is consistent with a protective immune response against severe COVID-19.",

keywords = "BCG, COVID-19, cytokine, immunoregulation, SARS-CoV-2, T cell",

author = "Messina, {Nicole L.} and Susie Germano and Rebecca McElroy and Rajeev Rudraraju and Rhian Bonnici and Pittet, {Laure F.} and Neeland, {Melanie R.} and Suellen Nicholson and Kanta Subbarao and Nigel Curtis and {the BRACE trial} and Carolinne Abreu and Veronica Abruzzo and Lynne Addlem and Sophie Agius and Barbosa, {Adelita Agripina Refosco} and Ahmed Alamrousi and {da Silva dos Santos}, {Ayla Alcoforado} and Yasmeen Al-Hindawi and Silveira, {Samyra Almeida Da} and {da Cruz}, {Lais Alves} and Amenyogbe Nelly and Jeremy Anderson and Christina Anthony and {dos Reis Pereira}, {Andrea Antonia Souza de Almeida} and {de las Revillas Almajano}, {Francisco Arnaiz} and Annabelle Arnold and Beth Arrowsmith and Kristy Azzopardi and Marti, {Cristina Badia} and Twinkle Bahaduri and Samantha Bannister and Sarah Barney and Lydia Barrera and Anabel Barriocanal and Dayanne Barros and Simone Barry and Adam Bartlett and Silva Muranaka and Therese Baulman and Morgan Bealing and Justin Beardsley and Gutierrez, {Ana Belen Martin} and Jason Bell and Rym Benothman and Saoirse Benson and Vicki Bennett-Wood and Nikki Bergant and Barbosa, {Fabiane Bianca} and Wouter Bijllaardt and Patricia Bimboese and {de Andrade}, {Camila Bitencourt} and Stephen Blake and Kitty Blauwendraat and Wim Boersma and Garcia, {Pilar Bohedo} and Marc Bonten and Anne Boon and Anna Bourke and Kirsty Bowes and Larissa Brasil and Clare Brophy and Rochelle Botten and Sandy Buchanan and Jess Bucholc and Alison Burns and Emma Burrell and Natalia Bustos and Bridie Byrne and Anthony Byrne and Esther Calbo and Montes, {Jorge Calvo} and Beatriz Camesella and John Campbell and Atsegi{\~n}e Cangas and John Carlin and Roque, {Maria Carmen} and Diogo, {Roberta Carolina Pereira} and Estela Carvalho and Irma Casas and Erika Castro and Ramon Castro and Helen Catterick and Escobar, {Rodrigo Cezar Dutra} and Joyce Chan and Jo Cheah and Chern, {Tee Yee} and Thilakavathi Chengodu and Marianna Ciaverella and Sharon Clark and Espindola, {Marie Alix Clement} and Annie Cobbledick and Clinton Colaco and Simone Collopy and Patricia Comella and Mary Corbett and Castro, {Gabriela Correa E.} and Erlane Costa and Raquel Coya and Nigel Crawford and Julio Croda and Alda Cruz and Maxwell Curtis and Jac Cushnahan and Anna Czajko and {da Costa Silva}, Renato and Bouchra Daitiri and Margareth Dalcolmo and Karen Dalton and Aiken Dao and Andrew Davidson and Phoebe Dawe and Diane Dawson and {de Jesus Costa}, Miriam and {De La Cruz}, Karina and {de la Serna}, Almudena and {de Morais Batista}, Fabiani and {de Oliveira}, Adriely and {del Alba Rey Morillo}, Rocio and Maria Desylva and Helga Dijkstra and Rachel Dixon and {del Toro Lopez}, {Maria Dolores} and Jose Dominguez and Catriona Doran and Castellano, {Angel Dominguez} and Santos, {Glauce Dos} and {dos Santos Lencina}, Joyce and {dos Santos Silva}, D{\'e}bora and Mark Douglas and Ross Dunn and Andrew Dunn and Jemma Dunnill and Georgina Eden and Peta Edler and Harriet Edmund and Nat Eiffler and Hannah Elborough and Sonja Elia and Olivia Elkington and Michelle England and Ayala, {Wellyngthon Espindola} and Maria Esteve and Nick Evans and Sue Evans and Krist Ewe and {\'A}lvarez, {Mar{\'i}a Carmen Fari{\~n}} and Kieran Fahey and Jill Fairweather and Denise Faustman and Silva, {Erica Fernandes} and Monique Fernandez and Galina Fidler and Filius, {P. 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year = "2022",

month = jan,

doi = "10.1002/cti2.1387",

language = "English",

volume = "11",

journal = "Clinical and Translational Immunology",

issn = "2050-0068",

publisher = "Nature Publishing Group",

number = "4",

}

Messina, NL, Germano, S, McElroy, R, Rudraraju, R, Bonnici, R, Pittet, LF, Neeland, MR, Nicholson, S, Subbarao, K, Curtis, N, the BRACE trial, Benson, S, Blake, S, Campbell, J, Dunn, A, James, J, Korman, T, Lynn, D , Lynn, M , Stevens, N & Wesselingh, S 2022, 'Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19', Clinical and Translational Immunology, vol. 11, no. 4, e1387. https://doi.org/10.1002/cti2.1387

TY - JOUR

T1 - Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2

T2 - implications for protection against severe COVID-19

AU - Messina, Nicole L.

AU - Germano, Susie

AU - McElroy, Rebecca

AU - Rudraraju, Rajeev

AU - Bonnici, Rhian

AU - Pittet, Laure F.

AU - Neeland, Melanie R.

AU - Nicholson, Suellen

AU - Subbarao, Kanta

AU - Curtis, Nigel

AU - the BRACE trial

AU - Abreu, Carolinne

AU - Abruzzo, Veronica

AU - Addlem, Lynne

AU - Agius, Sophie

AU - Barbosa, Adelita Agripina Refosco

AU - Alamrousi, Ahmed

AU - da Silva dos Santos, Ayla Alcoforado

AU - Al-Hindawi, Yasmeen

AU - Silveira, Samyra Almeida Da

AU - da Cruz, Lais Alves

AU - Nelly, Amenyogbe

AU - Anderson, Jeremy

AU - Anthony, Christina

AU - dos Reis Pereira, Andrea Antonia Souza de Almeida

AU - de las Revillas Almajano, Francisco Arnaiz

AU - Arnold, Annabelle

AU - Arrowsmith, Beth

AU - Azzopardi, Kristy

AU - Marti, Cristina Badia

AU - Bahaduri, Twinkle

AU - Bannister, Samantha

AU - Barney, Sarah

AU - Barrera, Lydia

AU - Barriocanal, Anabel

AU - Barros, Dayanne

AU - Barry, Simone

AU - Bartlett, Adam

AU - Muranaka, Silva

AU - Baulman, Therese

AU - Bealing, Morgan

AU - Beardsley, Justin

AU - Gutierrez, Ana Belen Martin

AU - Bell, Jason

AU - Benothman, Rym

AU - Benson, Saoirse

AU - Bennett-Wood, Vicki

AU - Bergant, Nikki

AU - Barbosa, Fabiane Bianca

AU - Bijllaardt, Wouter

AU - Bimboese, Patricia

AU - de Andrade, Camila Bitencourt

AU - Blake, Stephen

AU - Blauwendraat, Kitty

AU - Boersma, Wim

AU - Garcia, Pilar Bohedo

AU - Bonten, Marc

AU - Boon, Anne

AU - Bourke, Anna

AU - Bowes, Kirsty

AU - Brasil, Larissa

AU - Brophy, Clare

AU - Botten, Rochelle

AU - Buchanan, Sandy

AU - Bucholc, Jess

AU - Burns, Alison

AU - Burrell, Emma

AU - Bustos, Natalia

AU - Byrne, Bridie

AU - Byrne, Anthony

AU - Calbo, Esther

AU - Montes, Jorge Calvo

AU - Camesella, Beatriz

AU - Campbell, John

AU - Cangas, Atsegiñe

AU - Carlin, John

AU - Roque, Maria Carmen

AU - Diogo, Roberta Carolina Pereira

AU - Carvalho, Estela

AU - Casas, Irma

AU - Castro, Erika

AU - Castro, Ramon

AU - Catterick, Helen

AU - Escobar, Rodrigo Cezar Dutra

AU - Chan, Joyce

AU - Cheah, Jo

AU - Chern, Tee Yee

AU - Chengodu, Thilakavathi

AU - Ciaverella, Marianna

AU - Clark, Sharon

AU - Espindola, Marie Alix Clement

AU - Cobbledick, Annie

AU - Colaco, Clinton

AU - Collopy, Simone

AU - Comella, Patricia

AU - Corbett, Mary

AU - Castro, Gabriela Correa E.

AU - Costa, Erlane

AU - Coya, Raquel

AU - Crawford, Nigel

AU - Croda, Julio

AU - Cruz, Alda

AU - Curtis, Maxwell

AU - Cushnahan, Jac

AU - Czajko, Anna

AU - da Costa Silva, Renato

AU - Daitiri, Bouchra

AU - Dalcolmo, Margareth

AU - Dalton, Karen

AU - Dao, Aiken

AU - Davidson, Andrew

AU - Dawe, Phoebe

AU - Dawson, Diane

AU - de Jesus Costa, Miriam

AU - De La Cruz, Karina

AU - de la Serna, Almudena

AU - de Morais Batista, Fabiani

AU - de Oliveira, Adriely

AU - del Alba Rey Morillo, Rocio

AU - Desylva, Maria

AU - Dijkstra, Helga

AU - Dixon, Rachel

AU - del Toro Lopez, Maria Dolores

AU - Dominguez, Jose

AU - Doran, Catriona

AU - Castellano, Angel Dominguez

AU - Santos, Glauce Dos

AU - dos Santos Lencina, Joyce

AU - dos Santos Silva, Débora

AU - Douglas, Mark

AU - Dunn, Ross

AU - Dunn, Andrew

AU - Dunnill, Jemma

AU - Eden, Georgina

AU - Edler, Peta

AU - Edmund, Harriet

AU - Eiffler, Nat

AU - Elborough, Hannah

AU - Elia, Sonja

AU - Elkington, Olivia

AU - England, Michelle

AU - Ayala, Wellyngthon Espindola

AU - Esteve, Maria

AU - Evans, Nick

AU - Evans, Sue

AU - Ewe, Krist

AU - Álvarez, María Carmen Fariñ

AU - Fahey, Kieran

AU - Fairweather, Jill

AU - Faustman, Denise

AU - Silva, Erica Fernandes

AU - Fernandez, Monique

AU - Fidler, Galina

AU - Filius, P. M.G.

AU - Finn, Adam

AU - Finucane, Carolyn

AU - Firth, Stephanie

AU - Fletcher, Emily

AU - Flynn, Catherine

AU - Flynn, Lorraine

AU - Fouracre, Liam

AU - Fowler, Sarah

AU - Freitas, Thamires

AU - Furtado, Ana Carolina

AU - Oliveira, Maria Gabriela

AU - Santos, Anna Gabriela

AU - Gonçalves, Leandro Galdino Cavalcanti

AU - Galletta, Laura

AU - Gama, Larissa

AU - Gamage, Dinusha

AU - Ganpat, Radhika

AU - García, Carlos

AU - Croda, Mariana Garcia

AU - Gardiner, Kaya

AU - Gardiner, Evangeline

AU - Gell, Grace

AU - de Oliveira, Aline Gerhardt

AU - Germano, Susie

AU - Gibbons, Michael

AU - Gibson, Camille

AU - Gifford, Alison

AU - Poderos, Teresa Giménez

AU - Ginsberg, Ann

AU - Gisolf, Jet

AU - Gladanac, Bojana

AU - Glenn, Penny

AU - Godinho, Vanessa

AU - dos Santos, Mayara Góes

AU - Goikoetxea, Josune

AU - Goldenberg, Telma

AU - Gomes, Adriano

AU - Marcos, Susana Gonzalez

AU - Rico, Claudia González

AU - Goodall, Casey

AU - Goodchild, Louise

AU - Gordon, Victoria

AU - Greven, Frances

AU - Capella, Ana Greyce

AU - Griffith, Liddy

AU - Guo, Christina

AU - Campos, David Gutierrez

AU - Cuadra, Manuel Gutierrez

AU - Gwee, Amanda

AU - Hall, Richard

AU - Hall, Lydia

AU - Hamilton, Kate

AU - Hannan, Matthew

AU - Harbech, Houda

AU - Harding, Alex

AU - Harker, Neil

AU - Harrison, Robert

AU - Hassing, Robert Jan

AU - da Rosa, Thaynara Haynara Souza

AU - Haywood, Zaheerah

AU - Heath, Christine

AU - Henare, Nadine

AU - Andrade, Paulo Henrique

AU - Herrmann, Susan

AU - Hill, Erin

AU - Hilton, Sam

AU - Huijbens, Danique

AU - Hutton, Heidi

AU - James, Jane

AU - Jamieson, Tenaya

AU - Janssen, Axel

AU - Jardim, Bruno

AU - Jardim, Tyane

AU - Jarvis, Lance

AU - Jenkins, Narelle

AU - Jones, Jane

AU - Jones, Jan

AU - Jones, Karen

AU - Jorge, Leticia

AU - Vilegas, Maria Jose Rios

AU - Joshi, Sri

AU - Joyce, Rosemary

AU - Junior, Joel

AU - Kandasamy, Rama

AU - Karunanayake, Anushka

AU - Karuppasamy, Hana

AU - Keeble, Tom

AU - Kent, Jennifer

AU - Kloeg, Paul

AU - Kluytmans, Jan

AU - Knight, Bridget

AU - Kollmann, Tobias R.

AU - Korman, Tony

AU - Lynn, David

AU - Lynn, Miriam

AU - Stevens, Natalie

AU - Wesselingh, Steve

PY - 2022/1

Y1 - 2022/1

N2 - Background and objectives: Because of its beneficial off-target effects against non-mycobacterial infectious diseases, bacillus Calmette–Guérin (BCG) vaccination might be an accessible early intervention to boost protection against novel pathogens. Multiple epidemiological studies and randomised controlled trials (RCTs) are investigating the protective effect of BCG against coronavirus disease 2019 (COVID-19). Using samples from participants in a placebo-controlled RCT aiming to determine whether BCG vaccination reduces the incidence and severity of COVID-19, we investigated the immunomodulatory effects of BCG on in vitro immune responses to SARS-CoV-2. Methods: This study used peripheral blood taken from participants in the multicentre RCT and BCG vaccination to reduce the impact of COVID-19 on healthcare workers (BRACE trial). The whole blood taken from BRACE trial participants was stimulated with γ-irradiated SARS-CoV-2-infected or mock-infected Vero cell supernatant. Cytokine responses were measured by multiplex cytokine analysis, and single-cell immunophenotyping was made by flow cytometry. Results: BCG vaccination, but not placebo vaccination, reduced SARS-CoV-2-induced secretion of cytokines known to be associated with severe COVID-19, including IL-6, TNF-α and IL-10. In addition, BCG vaccination promoted an effector memory phenotype in both CD4+ and CD8+ T cells, and an activation of eosinophils in response to SARS-CoV-2. Conclusions: The immunomodulatory signature of BCG’s off-target effects on SARS-CoV-2 is consistent with a protective immune response against severe COVID-19.

AB - Background and objectives: Because of its beneficial off-target effects against non-mycobacterial infectious diseases, bacillus Calmette–Guérin (BCG) vaccination might be an accessible early intervention to boost protection against novel pathogens. Multiple epidemiological studies and randomised controlled trials (RCTs) are investigating the protective effect of BCG against coronavirus disease 2019 (COVID-19). Using samples from participants in a placebo-controlled RCT aiming to determine whether BCG vaccination reduces the incidence and severity of COVID-19, we investigated the immunomodulatory effects of BCG on in vitro immune responses to SARS-CoV-2. Methods: This study used peripheral blood taken from participants in the multicentre RCT and BCG vaccination to reduce the impact of COVID-19 on healthcare workers (BRACE trial). The whole blood taken from BRACE trial participants was stimulated with γ-irradiated SARS-CoV-2-infected or mock-infected Vero cell supernatant. Cytokine responses were measured by multiplex cytokine analysis, and single-cell immunophenotyping was made by flow cytometry. Results: BCG vaccination, but not placebo vaccination, reduced SARS-CoV-2-induced secretion of cytokines known to be associated with severe COVID-19, including IL-6, TNF-α and IL-10. In addition, BCG vaccination promoted an effector memory phenotype in both CD4+ and CD8+ T cells, and an activation of eosinophils in response to SARS-CoV-2. Conclusions: The immunomodulatory signature of BCG’s off-target effects on SARS-CoV-2 is consistent with a protective immune response against severe COVID-19.

KW - BCG

KW - COVID-19

KW - cytokine

KW - immunoregulation

KW - SARS-CoV-2

KW - T cell

UR - http://www.scopus.com/inward/record.url?scp=85133973951&partnerID=8YFLogxK

U2 - 10.1002/cti2.1387

DO - 10.1002/cti2.1387

M3 - Article

AN - SCOPUS:85133973951

SN - 2050-0068

VL - 11

JO - Clinical and Translational Immunology

JF - Clinical and Translational Immunology

IS - 4

M1 - e1387

ER -

Off-target effects of bacillus Calmette–Guérin vaccination on immune responses to SARS-CoV-2: implications for protection against severe COVID-19

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Keywords

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