Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020

Craig P Thompson; Nicholas E Grayson; Robert S Paton; Jai S Bolton; José Lourenço; Bridget S Penman; Lian N Lee; Valerie Odon; Juthathip Mongkolsapaya; Senthil Chinnakannan; Wanwisa Dejnirattisai; Matthew Edmans; Alex Fyfe; Carol Imlach; Kreepa Kooblall; Nicholas Lim; Chang Liu; César López-Camacho; Carol McInally; Anna L McNaughton; Narayan Ramamurthy; Jeremy Ratcliff; Piyada Supasa; Oliver Sampson; Beibei Wang; Alexander J Mentzer; Marc Turner; Malcolm G Semple; Kenneth Baillie; ISARIC4C Investigators; Heli Harvala; Gavin R Screaton; Nigel Temperton; Paul Klenerman; Lisa M Jarvis; Sunetra Gupta; Peter Simmonds

doi:10.2807/1560-7917.ES.2020.25.42.2000685

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Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020
Craig P Thompson^1,2 , Nicholas E Grayson^2,3,4 , Robert S Paton^1,2 , Jai S Bolton^1,2 , José Lourenço^1,2 , Bridget S Penman⁵ , Lian N Lee^2,4 , Valerie Odon^2,4 , Juthathip Mongkolsapaya⁶ , Senthil Chinnakannan^2,4 , Wanwisa Dejnirattisai⁶ , Matthew Edmans^2,4 , Alex Fyfe^1,2 , Carol Imlach⁷ , Kreepa Kooblall⁸ , Nicholas Lim^2,3 , Chang Liu⁶ , César López-Camacho⁶ , Carol McInally⁷ , Anna L McNaughton^2,4 , Narayan Ramamurthy^2,4 , Jeremy Ratcliff^2,4 , Piyada Supasa⁶ , Oliver Sampson^2,3 , Beibei Wang⁶ , Alexander J Mentzer⁹ , Marc Turner⁷ , Malcolm G Semple¹⁰ , Kenneth Baillie¹¹ , ISARIC4C Investigators¹² , Heli Harvala¹³ , Gavin R Screaton⁶ , Nigel Temperton¹⁴ , Paul Klenerman^2,4 , Lisa M Jarvis⁷ , Sunetra Gupta^1,2 , Peter Simmonds^2,4
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Affiliations: ¹ Department of Zoology, University of Oxford, Oxford, United Kingdom ² Peter Medawar Building for Pathogen Research, Oxford, United Kingdom ³ Department of Paediatric Medicine, University of Oxford, University of Oxford, Oxford, United Kingdom ⁴ Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom ⁵ Zeeman Institute for Systems Biology and Infectious Disease Epidemiology Research, School of Life Sciences, The University of Warwick, Coventry, United Kingdom ⁶ Wellcome Centre for Human Genetics, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom ⁷ National Microbiology Reference Unit, Scottish National Blood Transfusion Service, Edinburgh, United Kingdom ⁸ Oxford Centre for Diabetes, Endocrinology and Metabolism, Churchill Hospital, University of Oxford, Oxford, United Kingdom ⁹ Wellcome Centre for Human Genetics, University of Oxford, Roosevelt Drive, Oxford, United Kingdom ¹⁰ Health Protection Unit in Emerging and Zoonotic Infection, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, United Kingdom ¹¹ NIHR Health Protection Research Unit in Emerging and Zoonotic Infections, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, United Kingdom ¹² The members of the ISARIC4C Investigators are listed under the investigator tab ¹³ Infection and Immunity, University College London, London, United Kingdom ¹⁴ Viral Pseudotype Unit, Medway School of Pharmacy, University of Kent, Chatham, United Kingdom

Correspondence:
Craig Thompson
craig.thompson zoo.ox.ac.uk
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The ISARIC4C Investigators: J Kenneth Baillie, Malcolm G Semple, Peter JM Openshaw, Gail Carson, Beatrice Alex, Benjamin Bach, Wendy S Barclay, Debby Bogaert, Meera Chand, Graham S Cooke, Annemarie B Docherty, Jake Dunning, Ana da Silva Filipe, Tom Fletcher, Christopher A Green, Ewen M Harrison, Julian A Hiscox, Antonia Ying Wai Ho, Peter W Horby, Samreen Ijaz, Saye Khoo, Paul Klenerman, Andrew Law, Wei Shen Lim, Alexander J Mentzer, Laura Merson, Alison M Meynert, Mahdad Noursadeghi, Shona C Moore, Massimo Palmarini, William A Paxton, Georgios Pollakis, Nicholas Price, Andrew Rambaut, David L Robertson, Clark D Russell, Vanessa Sancho-Shimizu, Janet T Scott, Thushan de Silva, Louise Sigfrid, Tom Solomon, Shiranee Sriskandan, David Stuart, Charlotte Summers, Richard S Tedder, Emma C Thomson, Roger Thompson AA, Ryan S Thwaites, Lance CW Turtle, Maria Zambon, Hayley Hardwick, Chloe Donohue, Ruth Lyons, Fiona Griffiths, Wilna Oosthuyzen, Lisa Norman, Riinu Pius, Tom M Drake, Cameron J Fairfield, Stephen Knight, Kenneth A Mclean, Derek Murphy, Catherine A Shaw, Jo Dalton, James Lee, Daniel Plotkin, Michelle Girvan, Egle Saviciute, Stephanie Roberts, Janet Harrison, Laura Marsh, Marie Connor, Sophie Halpin, Clare Jackson, Carrol Gamble, Gary Leeming, Andrew Law, Murray Wham, Sara Clohisey, Ross Hendry, James Scott-Brown, . William Greenhalf, Victoria Shaw, Sarah McDonald, Seán Keating, Katie A. Ahmed, Jane A Armstrong, Milton Ashworth, Innocent G Asiimwe, Siddharth Bakshi, Samantha L Barlow, Laura Booth, Benjamin Brennan, Katie Bullock, Benjamin WA Catterall, Jordan J Clark, Emily A Clarke, Sarah Cole, Louise Cooper, Helen Cox, Christopher Davis, Oslem Dincarslan, Chris Dunn, Philip Dyer, Angela Elliott, Anthony Evans, Lorna Finch, Lewis WS Fisher, Terry Foster, Isabel Garcia-Dorival, Willliam Greenhalf, Philip Gunning, Catherine Hartley, Antonia Ho, Rebecca L Jensen, Christopher B Jones, Trevor R Jones, Shadia Khandaker, Katharine King, Robyn T. Kiy, Chrysa Koukorava, Annette Lake, Suzannah Lant, Diane Latawiec, L Lavelle-Langham, Daniella Lefteri, Lauren Lett, Lucia A Livoti, Maria Mancini, Sarah McDonald, Laurence McEvoy, John McLauchlan, Soeren Metelmann, Nahida S Miah, Joanna Middleton, Joyce Mitchell, Shona C Moore, Ellen G Murphy, Rebekah Penrice-Randal, Jack Pilgrim, Tessa Prince, Will Reynolds, P. Matthew Ridley, Debby Sales, Victoria E Shaw, Rebecca K Shears, Benjamin Small, Krishanthi S Subramaniam, Agnieska Szemiel, Aislynn Taggart, Jolanta Tanianis-Hughes, Jordan Thomas, Erwan Trochu, Libby van Tonder, Eve Wilcock, J. Eunice Zhang, Kayode Adeniji, Daniel Agranoff, Ken Agwuh, Dhiraj Ail, Ana Alegria, Brian Angus, Abdul Ashish, Dougal Atkinson, Shahedal Bari, Gavin Barlow, Stella Barnass, Nicholas Barrett, Christopher Bassford, David Baxter, Michael Beadsworth, Jolanta Bernatoniene, John Berridge, Nicola Best, Pieter Bothma, David Brealey, Robin Brittain-Long, Naomi Bulteel, Tom Burden, Andrew Burtenshaw, Vikki Caruth, 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, 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, Elaine Hardy, Stuart Hartshorn, Daniel Harvey, Peter Havalda, Daniel B Hawcutt, Maria Hobrok, Luke Hodgson, Anil Hormis, 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, Tamas Leiner, Patrick Lillie, James Limb, Vanessa Linnett, Jeff Little, Michael MacMahon, Emily MacNaughton, Ravish Mankregod, Huw Masson, Elijah Matovu, Katherine McCullough, Ruth McEwen, Manjula Meda, Gary Mills, Jane Minton, Mariyam Mirfenderesky, Kavya Mohandas, Quen Mok, James Moon, Elinoor Moore, Patrick Morgan, Craig Morris, Katherine Mortimore, Samuel Moses, Mbiye Mpenge, Rohinton Mulla, Michael Murphy, Megan Nagel, Thapas Nagarajan, Mark Nelson, Igor Otahal, Mark Pais, Selva Panchatsharam, Hassan Paraiso, Brij Patel, Natalie Pattison, Justin Pepperell, Mark Peters, Mandeep Phull, Stefania Pintus, Jagtur Singh Pooni, Frank Post, David Price, Rachel Prout, Nikolas Rae, Henrik Reschreiter, Tim Reynolds, Neil Richardson, Mark Roberts, Devender Roberts, Alistair Rose, Guy Rousseau, Brendan Ryan, Taranprit Saluja, Aarti Shah, Prad Shanmuga, Anil Sharma, Anna Shawcross, Jeremy Sizer, Manu Shankar-Hari, Richard Smith, Catherine Snelson, Nick Spittle, Nikki Staines, Tom Stambach, Richard Stewart, Pradeep Subudhi, Tamas Szakmany, Kate Tatham, Jo Thomas, Chris Thompson, Robert Thompson, Ascanio Tridente, Darell Tupper-Carey, Mary Twagira, Andrew Ustianowski, Nick Vallotton, 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, Sarah Wilson, Stephen Winchester, Martin Wiselka, Adam Wolverson, Daniel G Wooton, Andrew Workman, Bryan Yates, Peter Young

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Citation style for this article: Thompson Craig P, Grayson Nicholas E, Paton Robert S, Bolton Jai S, Lourenço José, Penman Bridget S, Lee Lian N, Odon Valerie, Mongkolsapaya Juthathip, Chinnakannan Senthil, Dejnirattisai Wanwisa, Edmans Matthew, Fyfe Alex, Imlach Carol, Kooblall Kreepa, Lim Nicholas, Liu Chang, López-Camacho César, McInally Carol, McNaughton Anna L, Ramamurthy Narayan, Ratcliff Jeremy, Supasa Piyada, Sampson Oliver, Wang Beibei, Mentzer Alexander J, Turner Marc, Semple Malcolm G, Baillie Kenneth, ISARIC4C Investigators, Harvala Heli, Screaton Gavin R, Temperton Nigel, Klenerman Paul, Jarvis Lisa M, Gupta Sunetra, Simmonds Peter. Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020. Euro Surveill. 2020;25(42):pii=2000685. https://doi.org/10.2807/1560-7917.ES.2020.25.42.2000685 Received: 17 Apr 2020; Accepted: 11 Aug 2020

Abstract

Background

The progression and geographical distribution of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in the United Kingdom (UK) and elsewhere is unknown because typically only symptomatic individuals are diagnosed. We performed a serological study of blood donors in Scotland in the spring of 2020 to detect neutralising antibodies to SARS-CoV-2 as a marker of past infection and epidemic progression.

Aim

Our objective was to determine if sera from blood bank donors can be used to track the emergence and progression of the SARS-CoV-2 epidemic.

Methods

A pseudotyped SARS-CoV-2 virus microneutralisation assay was used to detect neutralising antibodies to SARS-CoV-2. The study comprised samples from 3,500 blood donors collected in Scotland between 17 March and 18 May 2020. Controls were collected from 100 donors in Scotland during 2019.

Results

All samples collected on 17 March 2020 (n = 500) were negative in the pseudotyped SARS-CoV-2 virus microneutralisation assay. Neutralising antibodies were detected in six of 500 donors from 23 to 26 March. The number of samples containing neutralising antibodies did not significantly rise after 5–6 April until the end of the study on 18 May. We found that infections were concentrated in certain postcodes, indicating that outbreaks of infection were extremely localised. In contrast, other areas remained comparatively untouched by the epidemic.

Conclusion

Although blood donors are not representative of the overall population, we demonstrated that serosurveys of blood banks can serve as a useful tool for tracking the emergence and progression of an epidemic such as the SARS-CoV-2 outbreak.

This work is licensed under a Creative Commons Attribution 4.0 International License.

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Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020

Citation style for this article: <a href="/search?value1=Craig+P+Thompson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Thompson Craig P</a>, <a href="/search?value1=Nicholas+E+Grayson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Grayson Nicholas E</a>, <a href="/search?value1=Robert+S+Paton&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Paton Robert S</a>, <a href="/search?value1=Jai+S+Bolton&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bolton Jai S</a>, <a href="/search?value1=Jos%C3%A9+Louren%C3%A7o&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lourenço José</a>, <a href="/search?value1=Bridget+S+Penman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Penman Bridget S</a>, <a href="/search?value1=Lian+N+Lee&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lee Lian N</a>, <a href="/search?value1=Valerie+Odon&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Odon Valerie</a>, <a href="/search?value1=Juthathip+Mongkolsapaya&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mongkolsapaya Juthathip</a>, <a href="/search?value1=Senthil+Chinnakannan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chinnakannan Senthil</a>, <a href="/search?value1=Wanwisa+Dejnirattisai&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Dejnirattisai Wanwisa</a>, <a href="/search?value1=Matthew+Edmans&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Edmans Matthew</a>, <a href="/search?value1=Alex+Fyfe&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fyfe Alex</a>, <a href="/search?value1=Carol+Imlach&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Imlach Carol</a>, <a href="/search?value1=Kreepa+Kooblall&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kooblall Kreepa</a>, <a href="/search?value1=Nicholas+Lim&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lim Nicholas</a>, <a href="/search?value1=Chang+Liu&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Liu Chang</a>, <a href="/search?value1=C%C3%A9sar+L%C3%B3pez-Camacho&option1=author&noRedirect=true" class="nonDisambigAuthorLink">López-Camacho César</a>, <a href="/search?value1=Carol+McInally&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McInally Carol</a>, <a href="/search?value1=Anna+L+McNaughton&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McNaughton Anna L</a>, <a href="/search?value1=Narayan+Ramamurthy&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ramamurthy Narayan</a>, <a href="/search?value1=Jeremy+Ratcliff&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Ratcliff Jeremy</a>, <a href="/search?value1=Piyada+Supasa&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Supasa Piyada</a>, <a href="/search?value1=Oliver+Sampson&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sampson Oliver</a>, <a href="/search?value1=Beibei+Wang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wang Beibei</a>, <a href="/search?value1=Alexander+J+Mentzer&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mentzer Alexander J</a>, <a href="/search?value1=Marc+Turner&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Turner Marc</a>, <a href="/search?value1=Malcolm+G+Semple&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Semple Malcolm G</a>, <a href="/search?value1=Kenneth+Baillie&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Baillie Kenneth</a>, <a href="/search?value1=ISARIC4C+Investigators&option1=author&noRedirect=true" class="nonDisambigAuthorLink">ISARIC4C Investigators</a>, <a href="/search?value1=Heli+Harvala&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Harvala Heli</a>, <a href="/search?value1=Gavin+R+Screaton&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Screaton Gavin R</a>, <a href="/search?value1=Nigel+Temperton&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Temperton Nigel</a>, <a href="/search?value1=Paul+Klenerman&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Klenerman Paul</a>, <a href="/search?value1=Lisa+M+Jarvis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jarvis Lisa M</a>, <a href="/search?value1=Sunetra+Gupta&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Gupta Sunetra</a>, <a href="/search?value1=Peter+Simmonds&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Simmonds Peter</a>. Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020. <a href="/content/ecdc">Euro Surveill.</a> 2020;25(42):pii=2000685. <a href="https://doi.org/10.2807/1560-7917.ES.2020.25.42.2000685" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2020.25.42.2000685</a> Received: 17 Apr 2020;   Accepted: 11 Aug 2020

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Detection of neutralising antibodies to SARS-CoV-2 to determine population exposure in Scottish blood donors between March and May 2020

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