SARS-CoV-2-specific nasal IgA wanes 9 months after hospitalisation with COVID-19 and is not induced by subsequent vaccination

著者: Felicity Liew, Shubha Talwar, Andy Cross, Brian J. Willett, Sam Scott, Nicola Logan, Matthew K. Siggins, Dawid Swieboda, Jasmin Sidhu, Claudia Efstathiou, Shona C. Moore, Christopher Davis, Noura Mohamed, J Nunag, Clara King, A. A. Roger Thompson, Sarah Rowland‐Jones, Annemarie B Docherty, James D. Chalmers, Ling‐Pei Ho, Alex Horsley, Betty Raman, Krisnah Poinasamy, Michael Marks, Onn Min Kon, Luke Howard, Dan Wootton, Susanna Dunachie, Jennifer K Quint, Rachael A Evans, Louise V. Wain, Sara Fontanella, Thushan I. de Silva, Antonia Ho, Ewen Harrison, J. Kenneth Baillie, Malcolm G. Semple, Christopher E. Brightling, Ryan S. Thwaites, Lance Turtle, Peter Openshaw, J. Kenneth Baillie, Peter Openshaw, Malcolm G. Semple, Beatrice Alex, Petros Andrikopoulos, Benjamin Bach, William Barclay, Debby Bogaert, Meera Chand, Kanta Chechi, G Cooke, Ana da Silva Filipe, Thushan I. de Silva, Annemarie B Docherty, Gonçalo dos Santos Correia, Marc‐Emmanuel Dumas, Jake Dunning, Tom Fletcher, Christopher Green, William Greenhalf, Julian L. Griffin, Rishi K Gupta, Ewen M. Harrison, Antonia Ho, Karl Holden, Peter Horby, Samreen Ijaz, Say Khoo, Paul Klenerman, Andrew Law, Matthew Lewis, Sonia Liggi, Wei Shen Lim, Lynn Maslen, Alexander J. Mentzer, Laura Merson, Alison M Meynert, Shona C. Moore, Mahdad Noursadeghi, Michael Olanipekun, Anthonia Osagie, Massimo Palmarini, Carlo Palmieri, William A. Paxton, Georgios Pollakis, Nicholas Price, Andrew Rambaut, David L. Robertson, Clark D Russell, Vanessa Sancho‐Shimizu, Caroline Sands, J. T. Scott, Louise Sigfrid, Tom Solomon, Shiranee Sriskandan, David I. Stuart, Charlotte Summers, Olivia Swann, Zoltán Takáts, Panteleimon G. Takis, Richard S. Tedder, A. A. Roger Thompson, Emma C. Thomson, Ryan S. Thwaites, Lance Turtle, Maria Zambon, Thomas M Drake, Cameron J Fairfield, Stephen R Knight, Kenneth A McLean, Derek Murphy, Lisa Norman, Riinu Pius, Catherine A. Shaw, Marie Connor, Jo Ann Dalton, Carrol Gamble, Michelle Girvan, Sophie Halpin, Janet Harrison, Clare Jackson, James Lee, Laura Marsh, Daniel Plotkin, Stephanie Roberts, Egle Saviciute, Sara Clohisey, Ross Hendry, Susan Knight, Eva Lahnsteiner, Andrew Law, Gary Leeming, Lucy Norris, James Scott-Brown, Sarah Tait, Murray Wham, Richard Clark, Audrey Coutts, Lorna Donelly, Angie Fawkes, Tammy Gilchrist, Katarzyna Hafezi, Louise MacGillivray, Alan Maclean, Sarah McCafferty, Kirstie Morrice, Lee Murphy, Nicola Wrobel, Gail Carson, Kayode Adeniji, Daniel Agranoff, Ken Agwuh, Dhiraj Ail, Erin L. Aldera, Ana Alegria, Sam Allen, Brian Angus, Abdul Ashish, Dougal Atkinson, Shahedal Bari, Gavin Barlow, Stella Barnass, Nicholas Barrett, Christopher Bassford, Sneha Basude, David Baxter, Michael Beadsworth, Jolanta Bernatoniene, John C. Berridge, Colin Berry, Nicola Best, Pieter Bothma, Robin Brittain-Long, Naomi Bulteel, Tom Burden, Andrew Burtenshaw, Vikki Caruth, David Chadwick, David Chadwick, Duncan Chambler, Nigel Chee, Jenny Child, Srikanth Chukkambotla, Tom Clark, Paul Collini, Catherine Cosgrove, Jason Cupitt, Maria-Teresa Cutino-Moguel, Paul Dark, Chris Dawson, Samir Dervisevic, Phil Donnison, Sam Douthwaite, Andrew Drummond, Ingrid DuRand, Ahilanadan Dushianthan, Tristan Dyer, Cariad Evans, Chi Eziefula, Chrisopher Fegan, Adam Finn, Duncan Fullerton, Sanjeev Garg, Sanjeev Garg, Atul Garg, Effrossyni Gkrania‐Klotsas, Jo Godden, Arthur Goldsmith, Clive Graham, Tassos Grammatikopoulos, Elaine Hardy, Stuart Hartshorn, Daniel Harvey, Peter Havalda, Daniel B. Hawcutt, Maria Hobrok, Luke Hodgson, Anil Hormis, Joanne Howard, Michael Jacobs, Susan Jain, Paul Jennings, Agilan Kaliappan, Vidya Kasipandian, Stephen Kegg, Michael Kelsey, Jason Kendall, Caroline Kerrison, Ian Kerslake, Oliver Koch, Gouri Koduri, George Koshy, Shondipon Laha, Steven Laird, Susan Larkin, Tamás Leiner, Patrick Lillie, James Limb, Vanessa Linnett, Jeff Little, Mark D Lyttle, Michael MacMahon, Emily MacNaughton, Ravish Mankregod, Huw Masson, Elijah Matovu, Katherine McCullough, Ruth McEwen, Manjula Meda, Gary Mills, Jane Minton, Kavya Mohandas, Quen Mok, James Moon, Elinoor Moore, Patrick Morgan, Craig Morris, Katherine Mortimore, Samuel Moses, Mbiye Mpenge, Rohinton Mulla, Michael Murphy, Thapas Nagarajan, Megan Nagel, Mark Nelson, Lillian Norris, Matthew K. O’Shea, Marlies Ostermann, Igor Otahal, Mark Pais, Carlo Palmieri, Selva Panchatsharam, Danai Papakonstantinou, Padmasayee Papineni, Hassan Paraiso, Brij Patel, Natalie Pattison, Justin Pepperell, Mark Peters, Mandeep Phull, Stefania Pintus, Tim Planche, Frank A. Post, David Price, Rachel Prout, Nikolas Rae, Henrik Reschreiter, Tim Reynolds, Neil Richardson, Mark Roberts, Devender Roberts, Alistair Rose, Guy Rousseau, Bobby Ruge, Brendan Ryan, Taranprit Saluja, Sarah Sarah, Matthias Schmid, Aarti Shah, Manu Shankar‐Hari, Prad Shanmuga, Anil Kumar Sharma, Anna Shawcross, Jagtur Singh Pooni, Jeremy Sizer, Richard Smith, Catherine Snelson, Nick Spittle, Nikki Staines, Tom Stambach, Richard Stewart, Pradeep Subudhi, Tamás Szakmány, Kate Tatham, J. Regan Thomas, Chris Thompson, Robert Thompson, Ascanio Tridente, Darell Tupper-Carey, Mary Twagira, Nick Vallotton, Rama Vancheeswaran, Rachel Vincent, Lisa Vincent-Smith, Shico Visuvanathan, Alan Vuylsteke, Sam Waddy, Rachel Wake, Andrew Walden, Ingeborg Welters, Tony Whitehouse, Paul Whittaker, Ashley Whittington, Meme Wijesinghe, Martin Williams, Lawrence Wilson, Stephen Winchester, Martin Wiselka, Adam Wolverson, Dan Wootton, Andrew Workman, Bryan Yates, Peter Young, Sarah E. McDonald, Victoria Shaw, Katie A. Ahmed, J. A. Armstrong, Milton Ashworth, Innocent G. Asiimwe, Siddharth Bakshi, Samantha L Barlow, Laura Booth, Benjamin Brennan, Katie Bullock, Nicola Carlucci, Emily Cass, Benjamin WA Catterall, Jordan J Clark, Emily A Clarke, Sarah Cole, Louise Cooper, Helen Cox, Christopher Davis, Oslem Dincarslan, Alejandra Doce Carracedo, Chris Dunn, Philip Dyer, Angela Elliott, Anthony Evans, Lorna Finch, Lewis WS Fisher, Lisa Flaherty, Terry Foster, Isabel García-Dorival, Philip Gunning, Catherine Hartley, Anthony Holmes, Rebecca L. Jensen, Christopher B. Jones, Trevor R. Jones, Shadia Khandaker, Katharine King, Robyn T. Kiy, Chrysa Koukorava, Annette Lake, Suzannah Lant, Diane Latawiec, Lara Lavelle-Langham, Daniella Lefteri, Lauren Lett, Lucia A Livoti, Maria Vittoria Mancini, Hannah Massey, Nicole Maziere, Sarah E. McDonald, Laurence McEvoy, John McLauchlan, Soeren Metelmann, Nahida S Miah, Joanna Middleton, Joyce Mitchell, Shona C. Moore, E. Gordon Murphy, Rebekah Penrice-Randal, Jack Pilgrim, Tessa Prince, Will Reynolds, Paul Ridley, Debby Sales, Victoria Shaw, Rebecca K. Shears, Benjamin Small, Krishanthi Subramaniam, Agnieska Szemiel, Aislynn Taggart, Jolanta Tanianis-Hughes, Jordan Thomas, Erwan Trochu, Libby van Tonder, Eve Wilcock, Jinyan Zhang, Seán Keating, Cara Donegan, Rebecca G. Spencer, Chloe Donohue, Fiona Griffiths, Hayley Hardwick, Wilna Oosthuyzen, Kathryn M. Abel, Huzaifa Adamali, Davies Adeloye, O Adeyemi, R Adrego, L A Aguilar Jimenez, Shazaad Ahmad, Nafees Haider, Rizwan Ahmed, N Ahwireng, Mark Ainsworth, B Al-Sheklly, A Alamoudi, Mohammad Ali, M Aljaroof, A.M. All, Louise Allan, R Allen, L. Allerton, Lynne Allsop, P. Almeida, Doris Altmann, Maria Alvarez Corral, S Amoils, Debra Anderson, Chrystalina A. Antoniades, G. 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Mukaetova‐Ladinska, U Munawar, Jennifer Murira, Uttam Nanda, H Nassa, M Nasseri, A Neal, R. Needham, P Neill, Stefan Neubauer, David E. Newby, Helen Newell, Tom Newman, A. Newton-Cox, Timothy R. Nicholson, D Nicoll, A. Nikolaidis, Claire M. Nolan, Maria Noonan, Chris Norman, P. Novotný, J Nunag, Lorenza Nwafor, U Nwanguma, J Nyaboko, Conor O’Brien, Kate O’Donnell, David O’Regan, L O'Brien, N Odell, Graham S. Ogg, O Olaosebikan, C Oliver, Z Omar, Peter Openshaw, L. Orriss-Dib, Lynn Osborne, R Osbourne, Marlies Ostermann, Christopher E. Overton, J. Owen, J Oxton, Jamie Pack, Edmund Pacpaco, Stella‐Maria Paddick, S Painter, Ashkan Pakzad, S. Palmer, Padmasayee Papineni, Kitty Paques, Kerry Paradowski, Manish Pareek, Dhruv Parekh, Helen Parfrey, Carmine M. Pariante, Sean Parker, Miles Parkes, J. Parmar, S Patale, Brij Patel, Manish Patel, Suresh Patel, D Pattenadk, M Pavlides, Sarah Payne, Lyndsay Pearce, John E. Pearl, D. 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Short, S Siddique, Salman Siddiqui, J Sidebottom, Louise Sigfrid, G Simons, Jennifer Simpson, Nicholas Simpson, Amisha Singapuri, Claire Singh, Stephen Singh, Stephen Singh, D Sissons, J Skeemer, Katie Slack, Andrew Smith, D Smith, Susan M. Smith, John A. Smith, Lauren C. Smith, M Soares, T S Solano, Reanne Solly, A R Solstice, T Soulsby, David Southern, D. Sowter, Mark Spears, Lisa Spencer, F Speranza, Louise Stadon, Stefan Stanel, N Steele, Michael Steiner, David J. Stensel, G Stephens, L Stephenson, M Stern, Iain Stewart, R Stimpson, Skye Stockdale, James Stockley, William Thornley Stoker, Richard Stone, W Storrar, A. Storrie, Kim Storton, Jeffrey S. A. Stringer, Sophia Strong-Sheldrake, Natalie Stroud, Christian P Subbe, Cathie Sudlow, Z Suleiman, Charlotte Summers, Christina Summersgill, D Sutherland, Dominic L. Sykes, Robert Sykes, Nick P. Talbot, Ai Lyn Tan, L Tarusan, Vera Tavoukjian, Alex H. Taylor, C Taylor, J Taylor, A Te, H Tedd, C J Tee, J Teixeira, Helen Tench, S. Terry, S. Thackray-Nocera, Favas Thaivalappil, B Thamu, David Thickett, C Thomas, David Thomas, S Thomas, Andrew Thomas, T Thomas-Woods, T Thompson, A. A. Roger Thompson, T Thornton, Mathew Thorpe, Ryan S. Thwaites, J Tilley, N Tinker, Gerlynn Tiongson, Martin D. Tobin, James Tomlinson, Catherine Tong, Mark Toshner, Rhian M. Touyz, K A Tripp, Elizabeth M. Tunnicliffe, Alison E. Turnbull, Emma L. Turner, Steve Turner, Victoria Turner, K. Turner, Sharon Turney, Lance Turtle, H. Turton, J Ugoji, R Ugwuoke, Rachel Upthegrove, Jonathan Valabhji, M. Ventura, Joanne Vere, Carinna Vickers, B Vinson, Erin A. Wade, Phillip Wade, Louise V. Wain, Thomas W. Wainwright, L O Wajero, S Walder, S Walker, S Walker, Emma Wall, T Wallis, Sharon Walmsley, Jessica A. Walsh, S Walsh, L Warburton, Tom Ward, K Warwick, Helen Wassall, Sharon Waterson, Eleanor Watson, Lea C. Watson, Judith Watson, J. Weir McCall, Carly Welch, H Welch, B Welsh, Simon Wessely, S West, H Weston, Helen Wheeler, Simon R. White, Victor Whitehead, Julie Whitney, Spence Whittaker, B. Whittam, V Whitworth, Andrew Wight, Jim M. Wild, M Wilkins, Dean Wilkinson, Bryan Williams, Nefyn Williams, Nefyn Williams, Justin Williams, S A Williams-Howard, Michelle Willicombe, Guillermo B. Willis, J Willoughby, A Wilson, David M. Wilson, Iseult Wilson, Nicola Window, Miles D. Witham, R Wolf-Roberts, C Wood, Felix Woodhead, Jeffrey A. Woods, Dan Wootton, Joanne Wormleighton, J Worsley, David C. Wraith, C Wrey Brown, Clinton B. Wright, L Wright, S Wright, J Wyles, Inez Wynter, Mengxin Xu, N Yasmin, S Yasmin, Thomas Yates, Kay Por Yip, Bob Young, Scott Young, Alison L. Young, Ahmed Yousuf, A. Zawia, Lisa Zeidan, Boya Zhao, Bang Zheng, O Zongo - EBioMedicine 2022 被引用: 121

BACKGROUND: Most studies of immunity to SARS-CoV-2 focus on circulating antibody, giving limited insights into mucosal defences that prevent viral replication and onward transmission. We studied nasal and plasma antibody responses one year after hospitalisation for COVID-19, including a period when SARS-CoV-2 vaccination was introduced. METHODS: In this follow up study, plasma and nasosorption samples were prospectively collected from 446 adults hospitalised for COVID-19 between February 2020 and March 2021 via the ISARIC4C and PHOSP-COVID consortia. IgA and IgG responses to NP and S of ancestral SARS-CoV-2, Delta and Omicron (BA.1) variants were measured by electrochemiluminescence and compared with plasma neutralisation data. FINDINGS: Strong and consistent nasal anti-NP and anti-S IgA responses were demonstrated, which remained elevated for nine months (p < 0.0001). Nasal and plasma anti-S IgG remained elevated for at least 12 months (p < 0.0001) with plasma neutralising titres that were raised against all variants compared to controls (p < 0.0001). Of 323 with complete data, 307 were vaccinated between 6 and 12 months; coinciding with rises in nasal and plasma IgA and IgG anti-S titres for all SARS-CoV-2 variants, although the change in nasal IgA was minimal (1.46-fold change after 10 months, p = 0.011) and the median remained below the positive threshold determined by pre-pandemic controls. Samples 12 months after admission showed no association between nasal IgA and plasma IgG anti-S responses (R = 0.05, p = 0.18), indicating that nasal IgA responses are distinct from those in plasma and minimally boosted by vaccination. INTERPRETATION: The decline in nasal IgA responses 9 months after infection and minimal impact of subsequent vaccination may explain the lack of long-lasting nasal defence against reinfection and the limited effects of vaccination on transmission. These findings highlight the need to develop vaccines that enhance nasal immunity. FUNDING: This study has been supported by ISARIC4C and PHOSP-COVID consortia. ISARIC4C is supported by grants from the National Institute for Health and Care Research and the Medical Research Council. Liverpool Experimental Cancer Medicine Centre provided infrastructure support for this research. The PHOSP-COVD study is jointly funded by UK Research and Innovation and National Institute of Health and Care Research. The funders were not involved in the study design, interpretation of data or the writing of this manuscript.