Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial

Nicole Messina; Susie Germano; Rebecca McElroy; Rhian Bonnici; Branka Grubor-Bauk; David J. Lynn; Ellie McDonald; Suellen Nicholson; Kirsten Perrett; Laure Pittet; Rajeev Rudraraju; Natalie Stevens; Kanta Subbarao; Nigel Curtis; BRACE trial; Saoirse Benson; Stephen Blake; Miriam Lynn; Steve Wesselingh; Fiona McDonald

doi:10.1016/j.ebiom.2024.105100

Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial

Nicole Messina, Susie Germano, Rebecca McElroy, Rhian Bonnici, Branka Grubor-Bauk, David J. Lynn, Ellie McDonald, Suellen Nicholson, Kirsten Perrett, Laure Pittet, Rajeev Rudraraju, Natalie Stevens, Kanta Subbarao, Nigel Curtis, BRACE trial, Saoirse Benson, Stephen Blake, Miriam Lynn, Steve Wesselingh, Fiona McDonald

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Abstract

Background: The COVID-19 pandemic led to the rapid development and deployment of several highly effective vaccines against SARS-CoV-2. Recent studies suggest that these vaccines may also have off-target effects on the immune system. We sought to determine and compare the off-target effects of the adenovirus vector ChAdOx1-S (Oxford-AstraZeneca) and modified mRNA BNT162b2 (Pfizer-BioNTech) vaccines on immune responses to unrelated pathogens.

Methods: Prospective sub-study within the BRACE trial. Blood samples were collected from 284 healthcare workers before and 28 days after ChAdOx1-S or BNT162b2 vaccination. SARS-CoV-2-specific antibodies were measured using ELISA, and whole blood cytokine responses to specific (SARS-CoV-2) and unrelated pathogen stimulation were measured by multiplex bead array.

Findings: Both vaccines induced robust SARS-CoV-2 specific antibody and cytokine responses. ChAdOx1-S vaccination increased cytokine responses to heat-killed (HK) Candida albicans and HK Staphylococcus aureus and decreased cytokine responses to HK Escherichia coli and BCG. BNT162b2 vaccination decreased cytokine response to HK E. coli and had variable effects on cytokine responses to BCG and resiquimod (R848). After the second vaccine dose, BNT162b2 recipients had greater specific and off-target cytokine responses than ChAdOx1-S recipients.

Interpretation: ChAdOx1-S and BNT162b2 vaccines alter cytokine responses to unrelated pathogens, indicative of potential off-target effects. The specific and off-target effects of these vaccines differ in their magnitude and breadth. The clinical relevance of these findings is uncertain and needs further study.

Funding: Bill & Melinda Gates Foundation, National Health and Medical Research Council, Swiss National Science Foundation and the Melbourne Children's. BRACE trial funding is detailed in acknowledgements.

Original language	English
Article number	105100
Number of pages	16
Journal	EBioMedicine
Volume	103
Early online date	24 Apr 2024
DOIs	https://doi.org/10.1016/j.ebiom.2024.105100
Publication status	Published - May 2024

Keywords

Cytokine
Heterologous immunity
Immunoregulation
Off-target
SARS-CoV-2
Vaccine

UN SDGs

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

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Messina, N., Germano, S., McElroy, R., Bonnici, R., Grubor-Bauk, B., Lynn, D. J., McDonald, E., Nicholson, S., Perrett, K., Pittet, L., Rudraraju, R., Stevens, N., Subbarao, K., Curtis, N., BRACE trial, Benson, S., Blake, S., Lynn, M., Wesselingh, S., & McDonald, F. (2024). Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial. EBioMedicine, 103, Article 105100. https://doi.org/10.1016/j.ebiom.2024.105100

@article{23e0444d22984b96b635dde482cdf91a,

title = "Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial",

abstract = "Background: The COVID-19 pandemic led to the rapid development and deployment of several highly effective vaccines against SARS-CoV-2. Recent studies suggest that these vaccines may also have off-target effects on the immune system. We sought to determine and compare the off-target effects of the adenovirus vector ChAdOx1-S (Oxford-AstraZeneca) and modified mRNA BNT162b2 (Pfizer-BioNTech) vaccines on immune responses to unrelated pathogens. Methods: Prospective sub-study within the BRACE trial. Blood samples were collected from 284 healthcare workers before and 28 days after ChAdOx1-S or BNT162b2 vaccination. SARS-CoV-2-specific antibodies were measured using ELISA, and whole blood cytokine responses to specific (SARS-CoV-2) and unrelated pathogen stimulation were measured by multiplex bead array. Findings: Both vaccines induced robust SARS-CoV-2 specific antibody and cytokine responses. ChAdOx1-S vaccination increased cytokine responses to heat-killed (HK) Candida albicans and HK Staphylococcus aureus and decreased cytokine responses to HK Escherichia coli and BCG. BNT162b2 vaccination decreased cytokine response to HK E. coli and had variable effects on cytokine responses to BCG and resiquimod (R848). After the second vaccine dose, BNT162b2 recipients had greater specific and off-target cytokine responses than ChAdOx1-S recipients. Interpretation: ChAdOx1-S and BNT162b2 vaccines alter cytokine responses to unrelated pathogens, indicative of potential off-target effects. The specific and off-target effects of these vaccines differ in their magnitude and breadth. The clinical relevance of these findings is uncertain and needs further study. Funding: Bill & Melinda Gates Foundation, National Health and Medical Research Council, Swiss National Science Foundation and the Melbourne Children's. BRACE trial funding is detailed in acknowledgements.",

keywords = "Cytokine, Heterologous immunity, Immunoregulation, Off-target, SARS-CoV-2, Vaccine",

author = "Nicole Messina and Susie Germano and Rebecca McElroy and Rhian Bonnici and Branka Grubor-Bauk and Lynn, {David J.} and Ellie McDonald and Suellen Nicholson and Kirsten Perrett and Laure Pittet and Rajeev Rudraraju and Natalie Stevens and Kanta Subbarao and Nigel Curtis and {BRACE trial} and Andrew Davidson and Kaya Gardiner and Amanda Gwee and Tenaya Jamieson and Thilanka Morawakage and Susan Perlen and Amber Sastry and Teo, {Jia Wei} and Francesca Orsini and Katherine Lee and Cecilia Moore and Suzanna Vidmar and Rashida Ali and Ross Dunn and Peta Edler and Grace Gell and Casey Goodall and Richard Hall and Ann Krastev and Nathan La and Nick McPhate and Thao Nguyen and Jack Ren and Luke Stevens and Ahmed Alamrousi and Thanh Dang and Jenny Hua and Monica Razmovska and Scott Reddiex and Xiaofang Wang and Jeremy Anderson and Kristy Azzopardi and Vicki Bennett-Wood and Anna Czajko and Nadia Mazarakis and Conor McCafferty and Frances Oppedisano and Belinda Ortika and Casey Pell and Leena Spry and Ryan Toh and Sunitha Velagapudi and Amanda Vlahos and Ashleigh Wee-Hee and Pedro Ramos and {De La Cruz}, Karina and Dinusha Gamage and Anushka Karunanayake and Isabella Mezzetti and Benjamin Ong and Ronita Singh and Enoshini Sooriyarachchi and Natalie Cain and Rianne Brizuela and Han Huang and Veronica Abruzzo and Morgan Bealing and Patricia Bimboese and Kirsty Bowes and Emma Burrell and Joyce Chan and Jac Cushnahan and Hannah Elborough and Olivia Elkington and Kieran Fahey and Monique Fernandez and Catherine Flynn and Sarah Fowler and Andrit, {Marie Gentile} and Bojana Gladanac and Catherine Hammond and Norine Ma and Sam Macalister and Emmah Milojevic and Jesutofunmi Mojeed and Jill Nguyen and Liz O'Donnell and Nadia Olivier and Isabelle Ooi and Stephanie Reynolds and Lisa Shen and Barb Sherry and Judith Spotswood and Jamie Wedderburn and Angela Younes and Donna Legge and Jason Bell and Jo Cheah and Annie Cobbledick and Kee Lim and Sonja Elia and Lynne Addlem and Anna Bourke and Clare Brophy and Nadine Henare and Narelle Jenkins and Francesca Machingaifa and Skye Miller and Kirsten Mitchell and Sigrid Pitkin and Kate Wall and Paola Villanueva and Nigel Crawford and Wendy Norton and Niki Tan and Thilakavathi Chengodu and Diane Dawson and Victoria Gordon and Tony Korman and Jess O'Bryan and Sophie Agius and Samantha Bannister and Jess Bucholc and Alison Burns and Beatriz Camesella and John Carlin and Marianna Ciaverella and Maxwell Curtis and Stephanie Firth and Christina Guo and Matthew Hannan and Erin Hill and Sri Joshi and Katherine Lieschke and Megan Mathers and Sasha Odoi and Ashleigh Rak and Chris Richards and Leah Steve and Carolyn Stewart and Eva Sudbury and Helen Thomson and Emma Watts and Fiona Williams and Angela Young and Penny Glenn and Andrew Kaynes and {De Floy}, {Amandine Philippart} and Sandy Buchanan and Thijs Sondag and Ivy Xie and Harriet Edmund and Bridie Byrne and Tom Keeble and Belle Ngien and Fran Noonan and Michelle Wearing-Smith and Alison Clarke and Pemma Davies and Oliver Eastwood and Alric Ellinghaus and Rachid Ghieh and Zahra Hilton and Emma Jennings and Athina Kakkos and Iris Liang and Katie Nicol and Sally O'Callaghan and Helen Osman and Gowri Rajaram and Sophia Ratcliffe and Victoria Rayner and Ashleigh Salmon and Angela Scheppokat and Aimee Stevens and Rebekah Street and Nicholas Toogood and Nicholas Wood and Twinkle Bahaduri and Therese Baulman and Jennifer Byrne and Candace Carter and Mary Corbett and Aiken Dao and Maria Desylva and Andrew Dunn and Evangeline Gardiner and Rosemary Joyce and Rama Kandasamy and Craig Munns and Lisa Pelayo and Ketaki Sharma and Katrina Sterling and Caitlin Uren and Clinton Colaco and Mark Douglas and Kate Hamilton and Adam Bartlett and Brendan McMullan and Pamela Palasanthiran and Phoebe Williams and Justin Beardsley and Nikki Bergant and Renier Lagunday and Kristen Overton and Jeffrey Post and Yasmeen Al-Hindawi and Sarah Barney and Anthony Byrne and Lee Mead and Marshall Plit and Saoirse Benson and Stephen Blake and Rochelle Botten and Chern, {Tee Yee} and Georgina Eden and Liddy Griffith and Jane James and Miriam Lynn and Angela Markow and Domenic Sacca and Steve Wesselingh and Catriona Doran and Simone Barry and Alice Sawka and Sue Evans and Louise Goodchild and Christine Heath and Meredith Krieg and Helen Marshall and Mark McMillan and Mary Walker and Peter Richmond and Nelly Amenyogbe and Christina Anthony and Annabelle Arnold and Beth Arrowsmith and Rym Ben-Othman and Fiona McDonald and John Campbell and James Moore",

year = "2024",

month = may,

doi = "10.1016/j.ebiom.2024.105100",

language = "English",

volume = "103",

journal = "EBioMedicine",

issn = "2352-3964",

publisher = "Elsevier B.V.",

}

Messina, N, Germano, S, McElroy, R, Bonnici, R, Grubor-Bauk, B, Lynn, DJ, McDonald, E, Nicholson, S, Perrett, K, Pittet, L, Rudraraju, R, Stevens, N, Subbarao, K, Curtis, N, BRACE trial, Benson, S, Blake, S , Lynn, M, Wesselingh, S & McDonald, F 2024, 'Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial', EBioMedicine, vol. 103, 105100. https://doi.org/10.1016/j.ebiom.2024.105100

TY - JOUR

T1 - Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial

AU - Messina, Nicole

AU - Germano, Susie

AU - McElroy, Rebecca

AU - Bonnici, Rhian

AU - Grubor-Bauk, Branka

AU - Lynn, David J.

AU - McDonald, Ellie

AU - Nicholson, Suellen

AU - Perrett, Kirsten

AU - Pittet, Laure

AU - Rudraraju, Rajeev

AU - Stevens, Natalie

AU - Subbarao, Kanta

AU - Curtis, Nigel

AU - BRACE trial

AU - Davidson, Andrew

AU - Gardiner, Kaya

AU - Gwee, Amanda

AU - Jamieson, Tenaya

AU - Morawakage, Thilanka

AU - Perlen, Susan

AU - Sastry, Amber

AU - Teo, Jia Wei

AU - Orsini, Francesca

AU - Lee, Katherine

AU - Moore, Cecilia

AU - Vidmar, Suzanna

AU - Ali, Rashida

AU - Dunn, Ross

AU - Edler, Peta

AU - Gell, Grace

AU - Goodall, Casey

AU - Hall, Richard

AU - Krastev, Ann

AU - La, Nathan

AU - McPhate, Nick

AU - Nguyen, Thao

AU - Ren, Jack

AU - Stevens, Luke

AU - Alamrousi, Ahmed

AU - Dang, Thanh

AU - Hua, Jenny

AU - Razmovska, Monica

AU - Reddiex, Scott

AU - Wang, Xiaofang

AU - Anderson, Jeremy

AU - Azzopardi, Kristy

AU - Bennett-Wood, Vicki

AU - Czajko, Anna

AU - Mazarakis, Nadia

AU - McCafferty, Conor

AU - Oppedisano, Frances

AU - Ortika, Belinda

AU - Pell, Casey

AU - Spry, Leena

AU - Toh, Ryan

AU - Velagapudi, Sunitha

AU - Vlahos, Amanda

AU - Wee-Hee, Ashleigh

AU - Ramos, Pedro

AU - De La Cruz, Karina

AU - Gamage, Dinusha

AU - Karunanayake, Anushka

AU - Mezzetti, Isabella

AU - Ong, Benjamin

AU - Singh, Ronita

AU - Sooriyarachchi, Enoshini

AU - Cain, Natalie

AU - Brizuela, Rianne

AU - Huang, Han

AU - Abruzzo, Veronica

AU - Bealing, Morgan

AU - Bimboese, Patricia

AU - Bowes, Kirsty

AU - Burrell, Emma

AU - Chan, Joyce

AU - Cushnahan, Jac

AU - Elborough, Hannah

AU - Elkington, Olivia

AU - Fahey, Kieran

AU - Fernandez, Monique

AU - Flynn, Catherine

AU - Fowler, Sarah

AU - Andrit, Marie Gentile

AU - Gladanac, Bojana

AU - Hammond, Catherine

AU - Ma, Norine

AU - Macalister, Sam

AU - Milojevic, Emmah

AU - Mojeed, Jesutofunmi

AU - Nguyen, Jill

AU - O'Donnell, Liz

AU - Olivier, Nadia

AU - Ooi, Isabelle

AU - Reynolds, Stephanie

AU - Shen, Lisa

AU - Sherry, Barb

AU - Spotswood, Judith

AU - Wedderburn, Jamie

AU - Younes, Angela

AU - Legge, Donna

AU - Bell, Jason

AU - Cheah, Jo

AU - Cobbledick, Annie

AU - Lim, Kee

AU - Elia, Sonja

AU - Addlem, Lynne

AU - Bourke, Anna

AU - Brophy, Clare

AU - Henare, Nadine

AU - Jenkins, Narelle

AU - Machingaifa, Francesca

AU - Miller, Skye

AU - Mitchell, Kirsten

AU - Pitkin, Sigrid

AU - Wall, Kate

AU - Villanueva, Paola

AU - Crawford, Nigel

AU - Norton, Wendy

AU - Tan, Niki

AU - Chengodu, Thilakavathi

AU - Dawson, Diane

AU - Gordon, Victoria

AU - Korman, Tony

AU - O'Bryan, Jess

AU - Agius, Sophie

AU - Bannister, Samantha

AU - Bucholc, Jess

AU - Burns, Alison

AU - Camesella, Beatriz

AU - Carlin, John

AU - Ciaverella, Marianna

AU - Curtis, Maxwell

AU - Firth, Stephanie

AU - Guo, Christina

AU - Hannan, Matthew

AU - Hill, Erin

AU - Joshi, Sri

AU - Lieschke, Katherine

AU - Mathers, Megan

AU - Odoi, Sasha

AU - Rak, Ashleigh

AU - Richards, Chris

AU - Steve, Leah

AU - Stewart, Carolyn

AU - Sudbury, Eva

AU - Thomson, Helen

AU - Watts, Emma

AU - Williams, Fiona

AU - Young, Angela

AU - Glenn, Penny

AU - Kaynes, Andrew

AU - De Floy, Amandine Philippart

AU - Buchanan, Sandy

AU - Sondag, Thijs

AU - Xie, Ivy

AU - Edmund, Harriet

AU - Byrne, Bridie

AU - Keeble, Tom

AU - Ngien, Belle

AU - Noonan, Fran

AU - Wearing-Smith, Michelle

AU - Clarke, Alison

AU - Davies, Pemma

AU - Eastwood, Oliver

AU - Ellinghaus, Alric

AU - Ghieh, Rachid

AU - Hilton, Zahra

AU - Jennings, Emma

AU - Kakkos, Athina

AU - Liang, Iris

AU - Nicol, Katie

AU - O'Callaghan, Sally

AU - Osman, Helen

AU - Rajaram, Gowri

AU - Ratcliffe, Sophia

AU - Rayner, Victoria

AU - Salmon, Ashleigh

AU - Scheppokat, Angela

AU - Stevens, Aimee

AU - Street, Rebekah

AU - Toogood, Nicholas

AU - Wood, Nicholas

AU - Bahaduri, Twinkle

AU - Baulman, Therese

AU - Byrne, Jennifer

AU - Carter, Candace

AU - Corbett, Mary

AU - Dao, Aiken

AU - Desylva, Maria

AU - Dunn, Andrew

AU - Gardiner, Evangeline

AU - Joyce, Rosemary

AU - Kandasamy, Rama

AU - Munns, Craig

AU - Pelayo, Lisa

AU - Sharma, Ketaki

AU - Sterling, Katrina

AU - Uren, Caitlin

AU - Colaco, Clinton

AU - Douglas, Mark

AU - Hamilton, Kate

AU - Bartlett, Adam

AU - McMullan, Brendan

AU - Palasanthiran, Pamela

AU - Williams, Phoebe

AU - Beardsley, Justin

AU - Bergant, Nikki

AU - Lagunday, Renier

AU - Overton, Kristen

AU - Post, Jeffrey

AU - Al-Hindawi, Yasmeen

AU - Barney, Sarah

AU - Byrne, Anthony

AU - Mead, Lee

AU - Plit, Marshall

AU - Benson, Saoirse

AU - Blake, Stephen

AU - Botten, Rochelle

AU - Chern, Tee Yee

AU - Eden, Georgina

AU - Griffith, Liddy

AU - James, Jane

AU - Lynn, Miriam

AU - Markow, Angela

AU - Sacca, Domenic

AU - Wesselingh, Steve

AU - Doran, Catriona

AU - Barry, Simone

AU - Sawka, Alice

AU - Evans, Sue

AU - Goodchild, Louise

AU - Heath, Christine

AU - Krieg, Meredith

AU - Marshall, Helen

AU - McMillan, Mark

AU - Walker, Mary

AU - Richmond, Peter

AU - Amenyogbe, Nelly

AU - Anthony, Christina

AU - Arnold, Annabelle

AU - Arrowsmith, Beth

AU - Ben-Othman, Rym

AU - McDonald, Fiona

AU - Campbell, John

AU - Moore, James

PY - 2024/5

Y1 - 2024/5

N2 - Background: The COVID-19 pandemic led to the rapid development and deployment of several highly effective vaccines against SARS-CoV-2. Recent studies suggest that these vaccines may also have off-target effects on the immune system. We sought to determine and compare the off-target effects of the adenovirus vector ChAdOx1-S (Oxford-AstraZeneca) and modified mRNA BNT162b2 (Pfizer-BioNTech) vaccines on immune responses to unrelated pathogens. Methods: Prospective sub-study within the BRACE trial. Blood samples were collected from 284 healthcare workers before and 28 days after ChAdOx1-S or BNT162b2 vaccination. SARS-CoV-2-specific antibodies were measured using ELISA, and whole blood cytokine responses to specific (SARS-CoV-2) and unrelated pathogen stimulation were measured by multiplex bead array. Findings: Both vaccines induced robust SARS-CoV-2 specific antibody and cytokine responses. ChAdOx1-S vaccination increased cytokine responses to heat-killed (HK) Candida albicans and HK Staphylococcus aureus and decreased cytokine responses to HK Escherichia coli and BCG. BNT162b2 vaccination decreased cytokine response to HK E. coli and had variable effects on cytokine responses to BCG and resiquimod (R848). After the second vaccine dose, BNT162b2 recipients had greater specific and off-target cytokine responses than ChAdOx1-S recipients. Interpretation: ChAdOx1-S and BNT162b2 vaccines alter cytokine responses to unrelated pathogens, indicative of potential off-target effects. The specific and off-target effects of these vaccines differ in their magnitude and breadth. The clinical relevance of these findings is uncertain and needs further study. Funding: Bill & Melinda Gates Foundation, National Health and Medical Research Council, Swiss National Science Foundation and the Melbourne Children's. BRACE trial funding is detailed in acknowledgements.

AB - Background: The COVID-19 pandemic led to the rapid development and deployment of several highly effective vaccines against SARS-CoV-2. Recent studies suggest that these vaccines may also have off-target effects on the immune system. We sought to determine and compare the off-target effects of the adenovirus vector ChAdOx1-S (Oxford-AstraZeneca) and modified mRNA BNT162b2 (Pfizer-BioNTech) vaccines on immune responses to unrelated pathogens. Methods: Prospective sub-study within the BRACE trial. Blood samples were collected from 284 healthcare workers before and 28 days after ChAdOx1-S or BNT162b2 vaccination. SARS-CoV-2-specific antibodies were measured using ELISA, and whole blood cytokine responses to specific (SARS-CoV-2) and unrelated pathogen stimulation were measured by multiplex bead array. Findings: Both vaccines induced robust SARS-CoV-2 specific antibody and cytokine responses. ChAdOx1-S vaccination increased cytokine responses to heat-killed (HK) Candida albicans and HK Staphylococcus aureus and decreased cytokine responses to HK Escherichia coli and BCG. BNT162b2 vaccination decreased cytokine response to HK E. coli and had variable effects on cytokine responses to BCG and resiquimod (R848). After the second vaccine dose, BNT162b2 recipients had greater specific and off-target cytokine responses than ChAdOx1-S recipients. Interpretation: ChAdOx1-S and BNT162b2 vaccines alter cytokine responses to unrelated pathogens, indicative of potential off-target effects. The specific and off-target effects of these vaccines differ in their magnitude and breadth. The clinical relevance of these findings is uncertain and needs further study. Funding: Bill & Melinda Gates Foundation, National Health and Medical Research Council, Swiss National Science Foundation and the Melbourne Children's. BRACE trial funding is detailed in acknowledgements.

KW - Cytokine

KW - Heterologous immunity

KW - Immunoregulation

KW - Off-target

KW - SARS-CoV-2

KW - Vaccine

UR - http://www.scopus.com/inward/record.url?scp=85190838856&partnerID=8YFLogxK

U2 - 10.1016/j.ebiom.2024.105100

DO - 10.1016/j.ebiom.2024.105100

M3 - Article

AN - SCOPUS:85190838856

SN - 2352-3964

VL - 103

JO - EBioMedicine

JF - EBioMedicine

M1 - 105100

ER -

Specific and off-target immune responses following COVID-19 vaccination with ChAdOx1-S and BNT162b2 vaccines—an exploratory sub-study of the BRACE trial

Abstract

Keywords

UN SDGs

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