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1. Investigation of hospital discharge cases and SARS-CoV-2 introduction into Lothian care homes

Author

Robson, Samuel C., Connor, Thomas R., Loman, Nicholas J., Golubchik, Tanya, Martinez Nunez, Rocio T., Bonsall, David, Rambaut, Andrew, Snell, Luke B., Livett, Rich, Ludden, Catherine, Corden, Sally, Nastouli, Eleni, Nebbia, Gaia, Johnston, Ian, Prieto, Jacqui A., Saeed, Kordo, Jackson, David K., Houlihan, Catherine, Frampton, Dan, Hamilton, William L., Witney, Adam A., Bucca, Giselda, Pope, Cassie F., Moore, Catherine, Thomson, Emma C., Cutino-Moguel, Teresa, Harrison, Ewan M., Smith, Colin P., Rogan, Fiona, Beckwith, Shaun M., Murray, Abigail, Singleton, Dawn, Eastick, Kirstine, Sheridan, Liz A., Randell, Paul, Jackson, Leigh M., Ariani, Cristina V., Gonçalves, Sónia, Fairley, Derek J., Loose, Matthew W., Watkins, Joanne, Moses, Samuel, Nicholls, Sam, Bull, Matthew, Amato, Roberto, Smith, Darren L., Aanensen, David M., Barrett, Jeffrey C., Kele, Beatrix, Aggarwal, Dinesh, Shepherd, James G., Curran, Martin D., Parmar, Surendra, Parker, Matthew D., Williams, Catryn, Glaysher, Sharon, Underwood, Anthony P., Bashton, Matthew, Pacchiarini, Nicole, Loveson, Katie F., Byott, Matthew, Carabelli, Alessandro M., Templeton, Kate E., Peacock, Sharon J., de Silva, Thushan I., Wang, Dennis, Langford, Cordelia F., Sillitoe, John, Gunson, Rory N., Cottrell, Simon, O’Grady, Justin, Kwiatkowski, Dominic, Lillie, Patrick J., Cortes, Nicholas, Moore, Nathan, Thomas, Claire, Burns, Phillipa J., Mahungu, Tabitha W., Liggett, Steven, Beckett, Angela H., Holden, Matthew TG., Levett, Lisa J., Osman, Husam, Hassan-Ibrahim, Mohammed O., Simpson, David A., Chand, Meera, Gupta, Ravi K., Darby, Alistair C., Paterson, Steve, Pybus, Oliver G., Volz, Erik M., de Angelis, Daniela, Robertson, David L., Page, Andrew J., Martincorena, Inigo, Aigrain, Louise, Bassett, Andrew R., Wong, Nick, Taha, Yusri, Erkiert, Michelle J., Spencer Chapman, Michael H., Dewar, Rebecca, McHugh, Martin P., Mookerjee, Siddharth, Aplin, Stephen, Harvey, Matthew, Sass, Thea, Umpleby, Helen, Wheeler, Helen, McKenna, James P., Warne, Ben, Taylor, Joshua F., Chaudhry, Yasmin, Izuagbe, Rhys, Jahun, Aminu S., Young, Gregory R., McMurray, Claire, McCann, Clare M., Nelson, Andrew, Elliott, Scott, Lowe, Hannah, Price, Anna, Crown, Matthew R., Rey, Sara, Roy, Sunando, Temperton, Ben, Shaaban, Sharif, Hesketh, Andrew R., Laing, Kenneth G., Monahan, Irene M., Heaney, Judith, Pelosi, Emanuela, Silviera, Siona, Wilson-Davies, Eleri, Fryer, Helen, Adams, Helen, du Plessis, Louis, Johnson, Rob, Harvey, William T., Hughes, Joseph, Orton, Richard J., Spurgin, Lewis G., Bourgeois, Yann, Ruis, Chris, O'Toole, Áine, Gourtovaia, Marina, Sanderson, Theo, Fraser, Christophe, Edgeworth, Jonathan, Breuer, Judith, Michell, Stephen L., Todd, John A., John, Michaela, Buck, David, Gajee, Kavitha, Kay, Gemma L., Heyburn, David, Charalampous, Themoula, Alcolea-Medina, Adela, Kitchman, Katie, McNal, Alan, Pritch, David T., Dervisevic, Samir, Muir, Peter, Robinson, Esther, Vipond, Barry B., Ramadan, Newara A., Jeanes, Christopher, Weldon, Danni, Catalan, Jana, Jones, Neil, da Silva Filipe, Ana, Williams, Chris, Fuchs, Marc, Miskelly, Julia, Jeffries, Aaron R., Oliver, Karen, Park, Naomi R., Ash, Amy, Koshy, Cherian, Barrow, Magdalena, Buchan, Sarah L., Mantzouratou, Anna, Clark, Gemma, Holmes, Christopher W., Campbell, Sharon, Davis, Thomas, Tan, Ngee Keong, Brown, Julianne R., Harris, Kathryn A., Kidd, Stephen P., Grant, Paul R., Xu-McCrae, Li, Cox, Alison, Madona, Pinglawathee, Pond, Marcus, Randell, Paul A., Withell, Karen T., Williams, Cheryl, Graham, Clive, Denton-Smith, Rebecca, Swindells, Emma, Turnbull, Robyn, Sloan, Tim J., Bosworth, Andrew, Hutchings, Stephanie, Pymont, Hannah M., Casey, Anna, Ratcliffe, Liz, Jones, Christopher R., Knight, Bridget A., Haque, Tanzina, Hart, Jennifer, Irish-Tavares, Dianne, Witele, Eric, Mower, Craig, Watson DipHE, Louisa K., Collins, Jennifer, Eltringham, Gary, Crudgington, Dorian, Macklin, Ben, Iturriza-Gomara, Miren, Lucaci, Anita O., McClure, Patrick C., Carlile, Matthew, Holmes, Nadine, Moore, Christopher, Storey, Nathaniel, Rooke, Stefan, Yebra, Gonzalo, Craine, Noel, Perry, Malorie, Alikhan, Nabil-Fareed, Bridgett, Stephen, Cook, Kate F., Fearn, Christopher, Goudarzi, Salman, Lyons, Ronan A., Williams, Thomas, Haldenby, Sam T., Durham, Jillian, Leonard, Steven, Davies, Robert M., Batra, Rahul, Blane, Beth, Spyer, Moira J., Smith, Perminder, Yavus, Mehmet, Williams, Rachel J., Mahanama, Adhyana IK., Samaraweera, Buddhini, Girgis, Sophia T., Hansford, Samantha E., Green, Angie, Beaver, Charlotte, Bellis, Katherine L., Dorman, Matthew J., Kay, Sally, Prestwood, Liam, Rajatileka, Shavanthi, Quick, Joshua, Poplawski, Radoslaw, Reynolds, Nicola, Mack, Andrew, Morriss, Arthur, Whalley, Thomas, Patel, Bindi, Georgana, Iliana, Hosmillo, Myra, Pinckert, Malte L., Stockton, Joanne, Henderson, John H., Hollis, Amy, Stanley, William, Yew, Wen C., Myers, Richard, Thornton, Alicia, Adams, Alexander, Annett, Tara, Asad, Hibo, Birchley, Alec, Coombes, Jason, Evans, Johnathan M., Fina, Laia, Gatica-Wilcox, Bree, Gilbert, Lauren, Graham, Lee, Hey, Jessica, Hilvers, Ember, Jones, Sophie, Jones, Hannah, Kumziene-Summerhayes, Sara, McKerr, Caoimhe, Powell, Jessica, Pugh, Georgia, Taylor, Sarah, Trotter, Alexander J., Williams, Charlotte A., Kermack, Leanne M., Foulkes, Benjamin H., Gallis, Marta, Hornsby, Hailey R., Louka, Stavroula F., Pohare, Manoj, Wolverson, Paige, Zhang, Peijun, MacIntyre-Cockett, George, Trebes, Amy, Moll, Robin J., Ferguson, Lynne, Goldstein, Emily J., Maclean, Alasdair, Tomb, Rachael, Starinskij, Igor, Thomson, Laura, Southgate, Joel, Kraemer, Moritz UG., Raghwani, Jayna, Zarebski, Alex E., Boyd, Olivia, Geidelberg, Lily, Illingworth, Chris J., Jackson, Chris, Pascall, David, Vattipally, Sreenu, Freeman, Timothy M., Hsu, Sharon N., Lindsey, Benjamin B., James, Keith, Lewis, Kevin, Tonkin-Hill, Gerry, Tovar-Corona, Jaime M., Cox, MacGregor, Abudahab, Khalil, Menegazzo, Mirko, Taylor, Ben EW., Yeats, Corin A., Mukaddas, Afrida, Wright, Derek W., de Oliveira Martins, Leonardo, Colquhoun, Rachel, Hill, Verity, Jackson, Ben, McCrone, J.T., Medd, Nathan, Scher, Emily, Keatley, Jon-Paul, Curran, Tanya, Morgan, Sian, Maxwell, Patrick, Smith, Ken, Eldirdiri, Sahar, Kenyon, Anita, Holmes, Alison H., Price, James R., Wyatt, Tim, Mather, Alison E., Skvortsov, Timofey, Hartley, John A., Guest, Martyn, Kitchen, Christine, Merrick, Ian, Munn, Robert, Bertolusso, Beatrice, Lynch, Jessica, Vernet, Gabrielle, Kirk, Stuart, Wastnedge, Elizabeth, Stanley, Rachael, Idle, Giles, Bradley, Declan T., Killough, Nicholas F., Poyner, Jennifer, Mori, Matilde, Jones, Owen, Wright, Victoria, Brooks, Ellena, Churcher, Carol M., Delgado Callico, Laia, Fragakis, Mireille, Galai, Katerina, Jermy, Andrew, Judges, Sarah, Markov, Anna, McManus, Georgina M., Smith, Kim S., Thomas-McEwen, Peter MD., Westwick, Elaine, Attwood, Stephen W., Bolt, Frances, Davies, Alisha, De Lacy, Elen, Downing, Fatima, Edwards, Sue, Meadows, Lizzie, Jeremiah, Sarah, Smith, Nikki, Foulser, Luke, Patel, Amita, Berry, Louise, Boswell, Tim, Fleming, Vicki M., Howson-Wells, Hannah C., Joseph, Amelia, Khakh, Manjinder, Lister, Michelle M., Bird, Paul W., Fallon, Karlie, Helmer, Thomas, McMurray, Claire L., Odedra, Mina, Shaw, Jessica, Tang, Julian W., Willford, Nicholas J., Blakey, Victoria, Raviprakash, Veena, Sheriff, Nicola, Williams, Lesley-Anne, Feltwell, Theresa, Bedford, Luke, Cargill, James S., Hughes, Warwick, Moore, Jonathan, Stonehouse, Susanne, Atkinson, Laura, Lee, Jack CD., Shah, Divya, Ohemeng-Kumi, Natasha, Ramble, John, Sehmi, Jasveen, Williams, Rebecca, Chatterton, Wendy, Pusok, Monika, Everson, William, Castigador, Anibolina, Macnaughton, Emily, El Bouzidi, Kate, Lampejo, Temi, Sudhanva, Malur, Breen, Cassie, Sluga, Graciela, Ahmad, Shazaad SY., George, Ryan P., Machin, Nicholas W., Binns, Debbie, James, Victoria, Blacow, Rachel, Coupland, Lindsay, Smith, Louise, Barton, Edward, Padgett, Debra, Scott, Garren, Cross, Aidan, Mirfenderesky, Mariyam, Greenaway, Jane, Cole, Kevin, Clarke, Phillip, Duckworth, Nichola, Walsh, Sarah, Bicknell, Kelly, Impey, Robert, Wyllie, Sarah, Hopes, Richard, Bishop, Chloe, Chalker, Vicki, Harrison, Ian, Gifford, Laura, Molnar, Zoltan, Auckland, Cressida, Evans, Cariad, Johnson, Kate, Partridge, David G., Raza, Mohammad, Baker, Paul, Bonner, Stephen, Essex, Sarah, Murray, Leanne J., Lawton, Andrew I., Burton-Fanning, Shirelle, Payne, Brendan AI., Waugh, Sheila, Gomes, Andrea N., Kimuli, Maimuna, Murray, Darren R., Ashfield, Paula, Dobie, Donald, Ashford, Fiona, Best, Angus, Crawford, Liam, Cumley, Nicola, Mayhew, Megan, Megram, Oliver, Mirza, Jeremy, Moles-Garcia, Emma, Percival, Benita, Driscoll, Megan, Ensell, Leah, Lowe, Helen L., Maftei, Laurentiu, Mondani, Matteo, Chaloner, Nicola J., Cogger, Benjamin J., Easton, Lisa J., Huckson, Hannah, Lewis, Jonathan, Lowdon, Sarah, Malone, Cassandra S., Munemo, Florence, Mutingwende, Manasa, Nicodemi, Roberto, Podplomyk FD, Olga, Somassa, Thomas, Beggs, Andrew, Richter, Alex, Cormie, Claire, Dias, Joana, Forrest, Sally, Higginson, Ellen E., Maes, Mailis, Young, Jamie, Davidson, Rose K., Jackson, Kathryn A., Keeley, Alexander J., Ball, Jonathan, Byaruhanga, Timothy, Chappell, Joseph G., Dey, Jayasree, Hill, Jack D., Park, Emily J., Fanaie, Arezou, Hilson, Rachel A., Yaze, Geraldine, Lo, Stephanie, Afifi, Safiah, Beer, Robert, Maksimovic, Joshua, McCluggage, Kathryn, Spellman, Karla, Bresner, Catherine, Fuller, William, Marchbank, Angela, Workma, Trudy, Shelest, Ekaterina, Debebe, Johnny, Sang, Fei, Francois, Sarah, Gutierrez, Bernardo, Vasylyeva, Tetyana I., Flaviani, Flavia, Ragonnet-Cronin, Manon, Smollett, Katherine L., Broos, Alice, Mair, Daniel, Nichols, Jenna, Nomikou, Kyriaki, Tong, Lily, Tsatsani, Ioulia, O'Brien, Sarah, Rushton, Steven, Sanderson, Roy, Perkins, Jon, Cotton, Seb, Gallagher, Abbie, Allara, Elias, Pearson, Clare, Bibby, David, Dabrer, Gavin, Ellaby, Nicholas, Gallagher, Eileen, Hubb, Jonathan, Lackenby, Angie, Lee, David, Manesis, Nikos, Mbisa, Tamyo, Platt, Steven, Twohig, Katherine A., Morgan, Mari, Aydin, Alp, Baker, David J., Foster-Nyarko, Ebenezer, Prosolek, Sophie J., Rudder, Steven, Baxter, Chris, Carvalho, Sílvia F., Lavin, Deborah, Mariappan, Arun, Radulescu, Clara, Singh, Aditi, Tang, Miao, Morcrette, Helen, Bayzid, Nadua, Cotic, Marius, Balcazar, Carlos E., Gallagher, Michael D., Maloney, Daniel, Stanton, Thomas D., Williamson, Kathleen A., Manley, Robin, Michelsen, Michelle L., Sambles, Christine M., Studholme, David J., Warwick-Dugdale, Joanna, Eccles, Richard, Gemmell, Matthew, Gregory, Richard, Hughes, Margaret, Nelson, Charlotte, Rainbow, Lucille, Vamos, Edith E., Webster, Hermione J., Whitehead, Mark, Wierzbicki, Claudia, Angyal, Adrienn, Green, Luke R., Whiteley, Max, Betteridge, Emma, Bronner, Iraad F., Farr, Ben W., Goodwin, Scott, Lensing, Stefanie V., McCarthy, Shane A., Quail, Michael A., Rajan, Diana, Redshaw, Nicholas M., Scott, Carol, Shirley, Lesley, Thurston, Scott AJ., Rowe, Will, Gaskin, Amy, Le-Viet, Thanh, Bonfield, James, Liddle, Jennifier, Whitwham, Andrew, Cotton, S., McHugh, M.P., Dewar, R., Haas, J.G., and Templeton, K.

Published
2023
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2. Quantitative, multiplexed, targeted proteomics for ascertaining variant specific SARS-CoV-2 antibody response

Author

Abbass, Hakam, Abiodun, Aderonke, Alfarih, Mashael, Alldis, Zoe, Altmann, Daniel M., Amin, Oliver E., Andiapen, Mervyn, Artico, Jessica, Augusto, João B., Baca, Georgina L., Bailey, Sasha N.L., Bhuva, Anish N., Boulter, Alex, Bowles, Ruth, Boyton, Rosemary J., Bracken, Olivia V., O’Brien, Ben, Brooks, Tim, Bullock, Natalie, Butler, David K., Captur, Gabriella, Carr, Olivia, Champion, Nicola, Chan, Carmen, Chandran, Aneesh, Coleman, Tom, Couto de Sousa, Jorge, Couto-Parada, Xose, Cross, Eleanor, Cutino-Moguel, Teresa, D’Arcangelo, Silvia, Davies, Rhodri H., Douglas, Brooke, Di Genova, Cecilia, Dieobi-Anene, Keenan, Diniz, Mariana O., Ellis, Anaya, Feehan, Karen, Finlay, Malcolm, Fontana, Marianna, Forooghi, Nasim, Francis, Sasha, Gibbons, Joseph M., Gillespie, David, Gilroy, Derek, Hamblin, Matt, Harker, Gabrielle, Hemingway, Georgia, Hewson, Jacqueline, Heywood, Wendy, Hickling, Lauren M., Hicks, Bethany, Hingorani, Aroon D., Howes, Lee, Itua, Ivie, Jardim, Victor, Lee, Wing-Yiu Jason, Jensen, Melaniepetra, Jones, Jessica, Jones, Meleri, Joy, George, Kapil, Vikas, Kelly, Caoimhe, Kurdi, Hibba, Lambourne, Jonathan, Lin, Kai-Min, Liu, Siyi, Lloyd, Aaron, Louth, Sarah, Maini, Mala K., Mandadapu, Vineela, Manisty, Charlotte, McKnight, Áine, Menacho, Katia, Mfuko, Celina, Mills, Kevin, Millward, Sebastian, Mitchelmore, Oliver, Moon, Christopher, Moon, James, Sandoval, Diana Muñoz, Murray, Sam M., Noursadeghi, Mahdad, Otter, Ashley, Pade, Corinna, Palma, Susana, Parker, Ruth, Patel, Kush, Pawarova, Mihaela, Petersen, Steffen E., Piniera, Brian, Pieper, Franziska P., Rannigan, Lisa, Rapala, Alicja, Reynolds, Catherine J., Richards, Amy, Robathan, Matthew, Rosenheim, Joshua, Rowe, Cathy, Royds, Matthew, West, Jane Sackville, Sambile, Genine, Schmidt, Nathalie M., Selman, Hannah, Semper, Amanda, Seraphim, Andreas, Simion, Mihaela, Smit, Angelique, Sugimoto, Michelle, Swadling, Leo, Taylor, Stephen, Temperton, Nigel, Thomas, Stephen, Thornton, George D., Treibel, Thomas A., Tucker, Art, Varghese, Ann, Veerapen, Jessry, Vijayakumar, Mohit, Warner, Tim, Welch, Sophie, White, Hannah, Wodehouse, Theresa, Wynne, Lucinda, Zahedi, Dan, Doykov, Ivan, Baldwin, Tomas, Spiewak, Justyna, Gilmour, Kimberly C., Áine McKnight, Treibel, Thomas, Moon, James C., Kevin Mills, and Heywood, Wendy E.

Published
2022
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4. Blood transcriptional biomarkers of acute viral infection for detection of pre-symptomatic SARS-CoV-2 infection: a nested, case-control diagnostic accuracy study

Author

Abbass, Hakam, Abiodun, Aderonke, Alfarih, Mashael, Alldis, Zoe, Altmann, Daniel M, Amin, Oliver E, Andiapen, Mervyn, Artico, Jessica, Augusto, João B, Baca, Georgiana L, Bailey, Sasha NL, Bhuva, Anish N, Boulter, Alex, Bowles, Ruth, Boyton, Rosemary J, Bracken, Olivia V, O'Brien, Ben, Brooks, Tim, Bullock, Natalie, Butler, David K, Captur, Gabriella, Champion, Nicola, Chan, Carmen, Chandran, Aneesh, Collier, David, Couto de Sousa, Jorge, Couto-Parada, Xose, Cutino-Moguel, Teresa, Davies, Rhodri H, Douglas, Brooke, Di Genova, Cecilia, Dieobi-Anene, Keenan, Diniz, Mariana O, Ellis, Anaya, Feehan, Karen, Finlay, Malcolm, Fontana, Marianna, Forooghi, Nasim, Gaier, Celia, Gibbons, Joseph M, Gilroy, Derek, Hamblin, Matt, Harker, Gabrielle, Hewson, Jacqueline, Hickling, Lauren M, Hingorani, Aroon D, Howes, Lee, Hughes, Alun, Hughes, Gemma, Hughes, Rebecca, Itua, Ivie, Jardim, Victor, Lee, Wing-Yiu Jason, Jensen, Melaniepetra, Jones, Jessica, Jones, Meleri, Joy, George, Kapil, Vikas, Kurdi, Hibba, Lambourne, Jonathan, Lin, Kai-Min, Louth, Sarah, Maini, Mala K, Mandadapu, Vineela, Manisty, Charlotte, McKnight, Áine, Menacho, Katia, Mfuko, Celina, Mitchelmore, Oliver, Moon, Christopher, Moon, James C, Munoz Sandoval, Diana, Murray, Sam M, Noursadeghi, Mahdad, Otter, Ashley, Pade, Corinna, Palma, Susana, Parker, Ruth, Patel, Kush, Pawarova, Babita, Petersen, Steffen E, Piniera, Brian, Pieper, Franziska P, Pope, Daniel, Prossora, Maria, Rannigan, Lisa, Rapala, Alicja, Reynolds, Catherine J, Richards, Amy, Robathan, Matthew, Rosenheim, Joshua, Sambile, Genine, Schmidt, Nathalie M, Semper, Amanda, Seraphim, Andreas, Simion, Mihaela, Smit, Angelique, Sugimoto, Michelle, Swadling, Leo, Taylor, Stephen, Temperton, Nigel, Thomas, Stephen, Thornton, George D, Treibel, Thomas A, Tucker, Art, Veerapen, Jessry, Vijayakumar, Mohit, Welch, Sophie, Wodehouse, Theresa, Wynne, Lucinda, Zahedi, Dan, Gupta, Rishi K, Bell, Lucy C, Guerra-Assuncao, Jose A, Pollara, Gabriele, Whelan, Matthew, McKnight, Aine, and Chain, Benjamin M

Published
2021
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12. Immune boosting by B.1.1.529 (Omicron) depends on previous SARS-CoV-2 exposure

Author

Reynolds, Catherine J., Pade, Corinna, Gibbons, Joseph M., Otter, Ashley D., Lin, Kai-Min, Muñoz Sandoval, Diana, Pieper, Franziska P., Butler, David K., Liu, Siyi, Joy, George, Forooghi, Nasim, Treibel, Thomas A., Manisty, Charlotte, Moon, James C., Semper, Amanda, Brooks, Tim, McKnight, Áine, Altmann, Daniel M., Boyton, Rosemary J., Abbass, Hakam, Abiodun, Aderonke, Alfarih, Mashael, Alldis, Zoe, Amin, Oliver E., Andiapen, Mervyn, Artico, Jessica, Augusto, João B., Baca, Georgina L., Bailey, Sasha N. L., Bhuva, Anish N., Boulter, Alex, Bowles, Ruth, Bracken, Olivia V., O’Brien, Ben, Bullock, Natalie, Captur, Gabriella, Carr, Olivia, Champion, Nicola, Chan, Carmen, Chandran, Aneesh, Coleman, Tom, Couto de Sousa, Jorge, Couto-Parada, Xose, Cross, Eleanor, Cutino-Moguel, Teresa, D’Arcangelo, Silvia, Davies, Rhodri H., Douglas, Brooke, Di Genova, Cecilia, Dieobi-Anene, Keenan, Diniz, Mariana O., Ellis, Anaya, Feehan, Karen, Finlay, Malcolm, Fontana, Marianna, Francis, Sasha, Gillespie, David, Gilroy, Derek, Hamblin, Matt, Harker, Gabrielle, Hemingway, Georgia, Hewson, Jacqueline, Heywood, Wendy, Hickling, Lauren M., Hicks, Bethany, Hingorani, Aroon D., Howes, Lee, Itua, Ivie, Jardim, Victor, Lee, Wing-Yiu Jason, Jensen, Melaniepetra, Jones, Jessica, Jones, Meleri, Kapil, Vikas, Kelly, Caoimhe, Kurdi, Hibba, Lambourne, Jonathan, Lloyd, Aaron, Louth, Sarah, Maini, Mala K., Mandadapu, Vineela, Menacho, Katia, Mfuko, Celina, Mills, Kevin, Millward, Sebastian, Mitchelmore, Oliver, Moon, Christopher, Moon, James, Murray, Sam M., Noursadeghi, Mahdad, Otter, Ashley, Palma, Susana, Parker, Ruth, Patel, Kush, Pawarova, Mihaela, Petersen, Steffen E., Piniera, Brian, Rannigan, Lisa, Rapala, Alicja, Richards, Amy, Robathan, Matthew, Rosenheim, Joshua, Rowe, Cathy, Royds, Matthew, Sackville West, Jane, Sambile, Genine, Schmidt, Nathalie M., Selman, Hannah, Seraphim, Andreas, Simion, Mihaela, Smit, Angelique, Sugimoto, Michelle, Swadling, Leo, Taylor, Stephen, Temperton, Nigel, Thomas, Stephen, Thornton, George D., Tucker, Art, Varghese, Ann, Veerapen, Jessry, Vijayakumar, Mohit, Warner, Tim, Welch, Sophie, White, Hannah, Wodehouse, Theresa, Wynne, Lucinda, Zahedi, Dan, Chain, Benjamin, and Medical Research Council (MRC)

Subjects
QR355, B-Lymphocytes, Science & Technology, Multidisciplinary, SARS-CoV-2, General Science & Technology, T-Lymphocytes, Immunization, Secondary, COVID-19, Cross Reactions, Antibodies, Viral, T-CELL IMMUNITY, Antibodies, Neutralizing, Multidisciplinary Sciences, Mice, INFECTION, Spike Glycoprotein, Coronavirus, Science & Technology - Other Topics, Animals, Humans, COVIDsortium Investigators§, COVIDsortium Immune Correlates Network§, BNT162 Vaccine
Abstract

INTRODUCTION B.1.1.529 (Omicron) and its subvariants pose new challenges for control of the COVID-19 pandemic. Although vaccinated populations are relatively protected from severe disease and death, countries with high vaccine uptake are experiencing substantial caseloads with breakthrough infection and frequent reinfection. RATIONALE We analyzed cross-protective immunity against B.1.1.529 (Omicron) in triple-vaccinated health care workers (HCWs) with different immune-imprinted histories of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection during the ancestral Wuhan Hu-1, B.1.1.7 (Alpha), and B.1.617.2 (Delta) waves and after infection during the B.1.1.529 (Omicron) wave in previously infection-naïve individuals and those with hybrid immunity, to investigate whether B.1.1.529 (Omicron) infection could further boost adaptive immunity. Spike subunit 1 (S1) receptor binding domain (RBD) and whole spike binding, live virus neutralizing antibody (nAb) potency, memory B cell (MBC) frequency, and T cell responses against peptide pools and naturally processed antigen were assessed. RESULTS B and T cell recognition and nAb potency were boosted against previous variants of concern (VOCs) in triple-vaccinated HCWs, but this enhanced immunity was attenuated against B.1.1.529 (Omicron) itself. Furthermore, immune imprinting after B.1.1.7 (Alpha) infection resulted in reduced durability of antibody binding against B.1.1.529 (Omicron), and S1 RBD and whole spike VOC binding correlated poorly with live virus nAb potency. Half of triple-vaccinated HCWs showed no T cell response to B.1.1.529 (Omicron) S1 processed antigen, and all showed reduced responses to the B.1.1.529 (Omicron) peptide pool, irrespective of SARS-CoV-2 infection history. Mapping T cell immunity in class II human leukocyte antigen transgenics showed that individual spike mutations could result in loss or gain of T cell epitope recognition, with changes to T cell effector and regulatory programs. Triple-vaccinated, previously infection-naïve individuals infected during the B.1.1.529 (Omicron) wave showed boosted cross-reactive S1 RBD and whole spike binding, live virus nAb potency, and T cell immunity against previous VOCs but less so against B.1.1.529 (Omicron) itself. Immune imprinting from prior Wuhan Hu-1 infection abrogated any enhanced cross-reactive antibody binding, T cell recognition, MBC frequency, or nAb potency after B.1.1.529 (Omicron) infection. CONCLUSION Vaccine boosting results in distinct, imprinted patterns of hybrid immunity with different combinations of SARS-CoV-2 infection and vaccination. Immune protection is boosted by B.1.1.529 (Omicron) infection in the triple-vaccinated, previously infection-naïve individuals, but this boosting is lost with prior Wuhan Hu-1 imprinting. This “hybrid immune damping” indicates substantial subversion of immune recognition and differential modulation through immune imprinting and may be the reason why the B.1.1.529 (Omicron) wave has been characterized by breakthrough infection and frequent reinfection with relatively preserved protection against severe disease in triple-vaccinated individuals.

Published
2022

14. The Alpha variant was not associated with excess nosocomial SARS-CoV-2 infection in a multi-centre UK hospital study

Author

Boshier, Florencia A.T., Venturini, Cristina, Stirrup, Oliver, Guerra-Assunção, José Afonso, Alcolea-Medina, Adela, Becket, Angela H., Byott, Matthew, Charalampous, Themoula, Filipe, Ana da Silva, Frampton, Dan, Glaysher, Sharon, Khan, Tabassum, Kulasegara-Shylini, Raghavendran, Kele, Beatrix, Monahan, Irene M., Mollett, Guy, Parker, Matthew, Pelosi, Emanuela, Randell, Paul, Roy, Sunando, Taylor, Joshua F., Weller, Sophie J., Wilson-Davies, Eleri, Wade, Phillip, Williams, Rachel, Copas, Andrew J., Cutino-Moguel, Teresa, Freemantle, Nick, Hayward, Andrew C., Holmes, Alison, Hughes, Joseph, Mahungu, Tabitha W., Nebbia, Gaia, Nastouli, Eleni, Partridge, David G., Pope, Cassie F., Price, James R., Robson, Samuel C., Saeed, Kordo, Shin, Gee Yen, de Silva, Thushan I., Snell, Luke B., Thomson, Emma C., Witney, Adam A., Breuer, Judith, COG-UK HOCI Variant Substudy consortium, The COVID-19 Genomics UK (COG-UK) consortium, Bashton, Matthew, Nelson, Andrew, McCann, Clare, Smith, Darren, and Young, Greg

Subjects
Microbiology (medical), medicine.medical_specialty, lineage B.1.1.7, Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), B100, Alpha (ethology), variants of concern, Logistic regression, Article, Internal medicine, Epidemiology, medicine, Humans, transmissibility, Infection control, nosocomial outbreaks, Cross Infection, Nosocomial outbreak, SARS-CoV-2, business.industry, Transmission (medicine), COVID-19, Outbreak, C500, C700, Hospitals, United Kingdom, Infectious Diseases, Alpha variant, business
Abstract

Objectives : Recently emerging SARS-CoV-2 variants have been associated with an increased rate of transmission within the community. We sought to determine whether this also resulted in increased transmission within hospitals. Methods : We collected viral sequences and epidemiological data of patients with community and healthcare associated SARS-CoV-2 infections, sampled from 16th November 2020 to 10th January 2021, from nine hospitals participating in the COG-UK HOCI study. Outbreaks were identified using ward information, lineage and pairwise genetic differences between viral sequences. Results : Mixed effects logistic regression analysis of 4184 sequences showed healthcare-acquired infections were no more likely to be identified as the Alpha variant than community acquired infections. Nosocomial outbreaks were investigated based on overlapping ward stay and SARS-CoV-2 genome sequence similarity. There was no significant difference in the number of patients involved in outbreaks caused by the Alpha variant compared to outbreaks caused by other lineages. Conclusions : We find no evidence to support it causing more nosocomial transmission than previous lineages. This suggests that the stringent infection prevention measures already in place in UK hospitals contained the spread of the Alpha variant as effectively as other less transmissible lineages, providing reassurance of their efficacy against emerging variants of concern. 40 word summary: This UK multicentre study found no evidence to support the Alpha variant as having caused more nosocomial transmission that previous SARS-CoV-2 variants. This provides some reassurance that currently implemented IPC measures may be as effective against more transmissible variants.

Published
2021

15. Pre-existing polymerase-specific T cells expand in abortive seronegative SARS-CoV-2

Author

Swadling, Leo, Diniz, Mariana O., Schmidt, Nathalie M., Amin, Oliver E., Chandran, Aneesh, Shaw, Emily, Pade, Corinna, Gibbons, Joseph M., Le Bert, Nina, Tan, Anthony T., Jeffery-Smith, Anna, Tan, Cedric C. S., Tham, Christine Y. L., Kucykowicz, Stephanie, Aidoo-Micah, Gloryanne, Rosenheim, Joshua, Davies, Jessica, Johnson, Marina, Jensen, Melanie P., Joy, George, McCoy, Laura E., Valdes, Ana M., Chain, Benjamin M., Goldblatt, David, Altmann, Daniel M., Boyton, Rosemary J., Manisty, Charlotte, Treibel, Thomas A., Moon, James C., Abbass, Hakam, Abiodun, Aderonke, Alfarih, Mashael, Alldis, Zoe, Andiapen, Mervyn, Artico, Jessica, Augusto, João B., Baca, Georgina L., Bailey, Sasha N. L., Bhuva, Anish N., Boulter, Alex, Bowles, Ruth, Bracken, Olivia V., O’Brien, Ben, Brooks, Tim, Bullock, Natalie, Butler, David K., Captur, Gabriella, Champion, Nicola, Chan, Carmen, Collier, David, de Sousa, Jorge Couto, Couto-Parada, Xose, Cutino-Moguel, Teresa, Davies, Rhodri H., Douglas, Brooke, Di Genova, Cecilia, Dieobi-Anene, Keenan, Ellis, Anaya, Feehan, Karen, Finlay, Malcolm, Fontana, Marianna, Forooghi, Nasim, Gaier, Celia, Gilroy, Derek, Hamblin, Matt, Harker, Gabrielle, Hewson, Jacqueline, Hickling, Lauren M., Hingorani, Aroon D., Howes, Lee, Hughes, Alun, Hughes, Gemma, Hughes, Rebecca, Itua, Ivie, Jardim, Victor, Lee, Wing-Yiu Jason, Jensen, Melanie petra, Jones, Jessica, Jones, Meleri, Kapil, Vikas, Kurdi, Hibba, Lambourne, Jonathan, Lin, Kai-Min, Louth, Sarah, Mandadapu, Vineela, McKnight, Áine, Menacho, Katia, Mfuko, Celina, Mitchelmore, Oliver, Moon, Christopher, Murray, Sam M., Noursadeghi, Mahdad, Otter, Ashley, Palma, Susana, Parker, Ruth, Patel, Kush, Pawarova, Babita, Petersen, Steffen E., Piniera, Brian, Pieper, Franziska P., Pope, Daniel, Prossora, Mary, Rannigan, Lisa, Rapala, Alicja, Reynolds, Catherine J., Richards, Amy, Robathan, Matthew, Sambile, Genine, Semper, Amanda, Seraphim, Andreas, Simion, Mihaela, Smit, Angelique, Sugimoto, Michelle, Taylor, Stephen, Temperton, Nigel J., Thomas, Stephen, Thornton, George D., Tucker, Art, Veerapen, Jessry, Vijayakumar, Mohit, Welch, Sophie, Wodehouse, Theresa, Wynne, Lucinda, Zahedi, Dan, Dorp, Lucy van, Balloux, Francois, McKnight, Áine, Bertoletti, Antonio, Maini, Mala K., Swadling, Leo [0000-0002-0537-6715], Schmidt, Nathalie M [0000-0002-9841-8418], Gibbons, Joseph M [0000-0002-7238-2381], Le Bert, Nina [0000-0003-0502-2527], Tham, Christine YL [0000-0002-2913-7591], Kucykowicz, Stephanie [0000-0002-8849-218X], Rosenheim, Joshua [0000-0003-0171-2053], McCoy, Laura E [0000-0001-9503-7946], Valdes, Ana M [0000-0003-1141-4471], Chain, Benjamin M [0000-0002-7417-3970], Goldblatt, David [0000-0002-0769-5242], Boyton, Rosemary J [0000-0002-5608-0797], van Dorp, Lucy [0000-0002-6211-2310], Balloux, Francois [0000-0003-1978-7715], Noursadeghi, Mahdad [0000-0002-4774-0853], Bertoletti, Antonio [0000-0002-2942-0485], Maini, Mala K [0000-0001-6384-1462], Apollo - University of Cambridge Repository, Medical Research Council (MRC), and Multiple Sclerosis Society

Subjects
Male, Transcription, Genetic, 631/250/1619/554, medicine.disease_cause, DISEASE, Neutralization, Cohort Studies, 13/1, 631/250/2152/1566/1571, INFECTION, Coronaviridae, Asymptomatic Infections, Polymerase, Coronavirus, Multidisciplinary, biology, article, virus diseases, DNA-Directed RNA Polymerases, Multidisciplinary Sciences, 13/31, Seroconversion, Cohort, Science & Technology - Other Topics, VIRUS, Female, 82/75, HEALTH-CARE WORKERS, Antibody, ANTIBODY-RESPONSES, General Science & Technology, Health Personnel, 13/106, IMMUNITY, Evolution, Molecular, Memory T Cells, In vivo, Multienzyme Complexes, medicine, Humans, EXPOSURE, 631/326/596/4130, COVIDsortium Investigators, Cell Proliferation, PATHOGENS, Science & Technology, SARS-CoV-2, MEMORY, CORONAVIRUSES, COVID-19, Membrane Proteins, 631/250/254, biology.organism_classification, Virology, biology.protein
Abstract

Individuals with potential exposure to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) do not necessarily develop PCR or antibody positivity, suggesting that some individuals may clear subclinical infection before seroconversion. T cells can contribute to the rapid clearance of SARS-CoV-2 and other coronavirus infections1–3. Here we hypothesize that pre-existing memory T cell responses, with cross-protective potential against SARS-CoV-2 (refs. 4–11), would expand in vivo to support rapid viral control, aborting infection. We measured SARS-CoV-2-reactive T cells, including those against the early transcribed replication–transcription complex (RTC)12,13, in intensively monitored healthcare workers (HCWs) who tested repeatedly negative according to PCR, antibody binding and neutralization assays (seronegative HCWs (SN-HCWs)). SN-HCWs had stronger, more multispecific memory T cells compared with a cohort of unexposed individuals from before the pandemic (prepandemic cohort), and these cells were more frequently directed against the RTC than the structural-protein-dominated responses observed after detectable infection (matched concurrent cohort). SN-HCWs with the strongest RTC-specific T cells had an increase in IFI27, a robust early innate signature of SARS-CoV-2 (ref. 14), suggesting abortive infection. RNA polymerase within RTC was the largest region of high sequence conservation across human seasonal coronaviruses (HCoV) and SARS-CoV-2 clades. RNA polymerase was preferentially targeted (among the regions tested) by T cells from prepandemic cohorts and SN-HCWs. RTC-epitope-specific T cells that cross-recognized HCoV variants were identified in SN-HCWs. Enriched pre-existing RNA-polymerase-specific T cells expanded in vivo to preferentially accumulate in the memory response after putative abortive compared to overt SARS-CoV-2 infection. Our data highlight RTC-specific T cells as targets for vaccines against endemic and emerging Coronaviridae.

Published
2021

16. Delayed-onset myocarditis following COVID-19

Author

Bajaj, Retesh, Sinclair, Hannah C, Patel, Kush, Low, Ben, Pericao, Ana, Manisty, Charlotte, Guttmann, Oliver, Zemrak, Filip, Miller, Owen, Longhi, Paula, Proudfoot, Alastair, Lams, Boris, Agarwal, Sangita, Marelli-Berg, Federica M, Tiberi, Simon, Cutino-Moguel, Teresa, Carr-White, Gerry, and Mohiddin, Saidi A

Published
2021
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17. Prior SARS-CoV-2 infection rescues B and T cell responses to variants after first vaccine dose

Author

Reynolds, Catherine J., Pade, Corinna, Gibbons, Joseph M., Butler, David K., Otter, Ashley D., Menacho, Katia, Fontana, Marianna, Smit, Angelique, Sackville-West, Jane E., Cutino-Moguel, Teresa, Maini, Mala K., Chain, Benjamin, Noursadeghi, Mahdad, Brooks, Tim, Semper, Amanda, Manisty, Charlotte, Treibel, Thomas A., Moon, James C., Valdes, Ana M., Altmann, Daniel M., Boyton, Rosemary, UK COVIDsortium Immune Correlates Network, and UK COVIDsortium Investigators

Abstract

SARS-CoV-2 vaccine rollout has coincided with the spread of variants of concern. We investigated if single dose vaccination, with or without prior infection, confers cross protective immunity to variants. We analyzed T and B cell responses after first dose vaccination with the Pfizer/BioNTech mRNA vaccine BNT162b2 in healthcare workers (HCW) followed longitudinally, with or without prior Wuhan-Hu-1 SARS-CoV-2 infection. After one dose, individuals with prior infection showed enhanced T cell immunity, antibody secreting memory B cell response to spike and neutralizing antibodies effective against B.1.1.7 and B.1.351. By comparison, HCW receiving one vaccine dose without prior infection showed reduced immunity against variants. B.1.1.7 and B.1.351 spike mutations resulted in increased, abrogated or unchanged T cell responses depending on human leukocyte antigen (HLA) polymorphisms. Single dose vaccination with BNT162b2 in the context of prior infection with a heterologous variant substantially enhances neutralizing antibody responses against variants.

Published
2021

18. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Placental Infection Is Associated With Massive Perivillous Fibrin Deposition at the Maternal-Fetal Interface: A Preliminary Study.

Author

Kotiloglu-Karaa, Esin, Kele, Beatrix, Kulasegaran-Shylini, Raghavendran, Broad, Claire E, Owoyemi, Dola, Martin, Joanne, MacPhail, Graham, Iliodromiti, Stamatina, Riddell, Anna, Alexander, Eliza, and Cutino-Moguel, Teresa

Subjects
REVERSE transcriptase polymerase chain reaction, COVID-19, PLACENTA diseases, IMMUNOHISTOCHEMISTRY, SEVERITY of illness index, FIBRIN, DISEASE risk factors, PREGNANCY
Abstract

We observed an increased frequency of massive perivillous fibrin deposition (MPFD) during the second coronavirus disease 2019 (COVID-19) pandemic wave dominated by the Alpha variant of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). MPFD associated with 100% reverse transcription polymerase chain reaction (RT-PCR) positivity for SARS-CoV-2 and detection by immunohistochemistry. The Alpha variant was identified in all placentas with MPFD that could be sequenced. [ABSTRACT FROM AUTHOR]

Published
2022
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20. Generation of Novel Severe Acute Respiratory Syndrome Coronavirus 2 Variants on the B.1.1.7 Lineage in 3 Patients With Advanced Human Immunodeficiency Virus-1 Disease.

Author

Riddell, Anna C, Kele, Beatrix, Harris, Kathryn, Bible, Jon, Murphy, Maurice, Dakshina, Subathira, Storey, Nathaniel, Owoyemi, Dola, Pade, Corinna, Gibbons, Joseph M, Harrington, David, Alexander, Eliza, McKnight, Áine, and Cutino-Moguel, Teresa

Subjects
HIV infections, HIV-positive persons, IN vitro studies, SARS-CoV-2, COVID-19, GENETIC mutation, IN vivo studies, IMMUNOCOMPROMISED patients, RISK assessment, CASE studies
Abstract

The emergence of new severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants is of public health concern in case of vaccine escape. Described are 3 patients with advanced human immunodeficiency virus (HIV)-1 and chronic SARS-CoV-2 infection in whom there is evidence of selection and persistence of novel mutations that are associated with increased transmissibility and immune escape. [ABSTRACT FROM AUTHOR]

Published
2022
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21. Persistence of antibody response to SARS-CoV-2 in a cohort of haemodialysis patients with COVID-19.

Author

Forbes, Suzanne, Davari, Maria, Gnanasampanthan, Sahana, Roth, Noam, Young, Gregor, Rajakariar, Ravindra, Cove-Smith, Andrea, Yaqoob, Muhammed Magdi, Cutino-Moguel, Teresa, Mahalingasivam, Viyaasan, and McCafferty, Kieran

Subjects
COVID-19, ANTIBODY formation, HEMODIALYSIS patients, SARS-CoV-2, IMMUNOGLOBULIN M
Abstract

Background Haemodialysis (HD) patients are extremely vulnerable to coronavirus disease 2019 (COVID-19). Their immune response after infection is unclear. We have found high seroconversion rates in this population, with 95% developing antibodies. It is unclear if and how long these antibodies persist. Here we investigate this with serial antibody (Ab) testing. Methods We identified HD patients who had confirmedsevere acute respiratory syndrome coronavirus 2 between March and May 2020 and measured monthly antibodies (immunoglobulin G/immunoglobulin M) in those who survived. We used a semiquantitative cut-off index to create a qualitative result and plotted optical density (OD) over time. We used linear regression to examine the slope, as well as noting peak OD and time to peak OD. We correlated these against baseline demographics, markers of illness severity and comorbidities. Results A total of 122 patients were analysed. All remained Ab positive during follow-up for a minimum of 148 days. Seventy-one percent had a positive gradient indicating increasing Ab positivity over time. We found that age (P = 0.01), duration of polymerase chain reaction positivity (P = 0.06) and the presence of symptoms (P = 0.05) were associated with a longer time to peak OD. Immunosuppression did not alter peak OD but did lead to a non-significant increase in time to peak OD, and more patients had a subsequent decrease in Ab levels (P = 0.02). Diabetic patients were more likely to have a positive slope (odds ratio 2.26). Conclusions These results indicate that HD patients have a robust and sustained Ab response after confirmed COVID-19 infection with no suggestion that immunosuppression weakens this response. Although it is unclear what protection these antibodies confer, this is encouraging that HD patients should respond to vaccination. [ABSTRACT FROM AUTHOR]

Published
2021
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22. The difference in mortality between adult patients with laboratory documented influenza A and B, a single centre retrospective observational study.

Author

Mabayoje, Diana A., Cutino‐Moguel, Teresa, Haigh, John, Wilks, Mark, Welch, Catherine A., and Melzer, Mark

Subjects
SEASONAL influenza, SCIENTIFIC observation, INFLUENZA, MORTALITY, ADULTS
Abstract

Background: Seasonal influenza is an annual occurrence that leads to large community outbreaks and increased hospitalization. A number of studies have suggested that influenza A (FLUAV) is associated with increased rates of hospitalization and mortality compared with influenza B (FLUBV). This study compared demographic and clinical variables in patients diagnosed with FLUAV or FLUBV during the 2017–2018 UK Influenza season. Methods: Patient demographic and clinical information were obtained by accessing medical records of patients testing FLUAV or FLUBV positive using the Cepheid GXP. We used the χ2 test to compare variables in patients with laboratory‐confirmed FLUAV and FLUBV. Results: One hundred and twenty‐seven adult patients had confirmed Influenza, 71 (55.9%) had FLUAV, and 56 (44.1%) FLUBV. There was no significant difference between severity at presentation, admission to HDU/ITU or median length of stay. The overall mortality was 6 (4.5%) and 9 (7.1%) at 7 and 30 days, respectively. There was a statistically significant difference in 7‐day mortality between patients with FLUAV and FLUBV, 1 (1.4%) versus 5 (8.9%), respectively, p =.047) although this became nonsignificant at 30 days. Conclusions: With the exception of mortality, we did not observe significant differences between patients with FLUAV and FLUBV. Seven‐day mortality in patients with FLUBV was significantly higher with FLUAV, although this was was not apparent at 30 days. [ABSTRACT FROM AUTHOR]

Published
2021
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24. Confirmed Reinfection With Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Variant VOC-202012/01.

Author

Harrington, David, Kele, Beatrix, Pereira, Spiro, Couto-Parada, Xose, Riddell, Anna, Forbes, Suzanne, Dobbie, Hamish, and Cutino-Moguel, Teresa

Subjects
REVERSE transcriptase polymerase chain reaction, SARS-CoV-2, IMMUNOGLOBULINS, COVID-19, SINGLE nucleotide polymorphisms, REINFECTION, IMMUNOASSAY, SEVERITY of illness index, GENOMES, COVID-19 testing, POLYMERASE chain reaction
Abstract

A case study of 78-year-old man with a history of Type 2 diabetes mellitus, diabetic nephropathy on hemodialysis, chronic obstructive pulmonary disease (COPD), mixed central and obstructive sleep apnea, ischemic heart disease, is presented. Topics include Genomes were assembled with reference based assembly and a bioinformatics pipeline; and region of the genome and 50% cut-off for defining single nucleotide polymorphisms (SNPs).

Published
2021
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25. COVID-19: PCR screening of asymptomatic health-care workers at London hospital.

Author

Treibel, Thomas A, Manisty, Charlotte, Burton, Maudrian, McKnight, Áine, Lambourne, Jonathan, Augusto, João B, Couto-Parada, Xosé, Cutino-Moguel, Teresa, Noursadeghi, Mahdad, and Moon, James C

Subjects
*COVID-19, *MEDICAL personnel, *HOSPITAL personnel, *COVID-19 pandemic
Abstract

The exponential growth in coronavirus disease 2019 (COVID-19) caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) across the UK has been successfully reversed by social distancing and lockdown.[1] RNA testing for prevalent infection is a key part of the exit strategy, but the role of testing for asymptomatic infection remains unclear.[2] Understanding the determinants of asymptomatic or pauci-symptomatic infection will provide new opportunities for personalised risk stratification and reveal much-needed correlates of protective immunity, whether induced by vaccination or natural exposure. Taken together, these data suggest that the rate of asymptomatic infection among HCWs more likely reflects general community transmission than in-hospital exposure. Prospective patients should be reassured that as the overall epidemic wave recedes, asymptomatic infection among HCWs is low and unlikely to be a major source of transmission. [Extracted from the article]

Published
2020
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27. Immune boosting by B.1.1.529 ( Omicron) depends on previous SARS-CoV-2 exposure.

Author

Reynolds CJ, Pade C, Gibbons JM, Otter AD, Lin KM, Muñoz Sandoval D, Pieper FP, Butler DK, Liu S, Joy G, Forooghi N, Treibel TA, Manisty C, Moon JC, Semper A, Brooks T, McKnight Á, Altmann DM, Boyton RJ, Abbass H, Abiodun A, Alfarih M, Alldis Z, Altmann DM, Amin OE, Andiapen M, Artico J, Augusto JB, Baca GL, Bailey SNL, Bhuva AN, Boulter A, Bowles R, Boyton RJ, Bracken OV, O'Brien B, Brooks T, Bullock N, Butler DK, Captur G, Carr O, Champion N, Chan C, Chandran A, Coleman T, Couto de Sousa J, Couto-Parada X, Cross E, Cutino-Moguel T, D'Arcangelo S, Davies RH, Douglas B, Di Genova C, Dieobi-Anene K, Diniz MO, Ellis A, Feehan K, Finlay M, Fontana M, Forooghi N, Francis S, Gibbons JM, Gillespie D, Gilroy D, Hamblin M, Harker G, Hemingway G, Hewson J, Heywood W, Hickling LM, Hicks B, Hingorani AD, Howes L, Itua I, Jardim V, Lee WJ, Jensen M, Jones J, Jones M, Joy G, Kapil V, Kelly C, Kurdi H, Lambourne J, Lin KM, Liu S, Lloyd A, Louth S, Maini MK, Mandadapu V, Manisty C, McKnight Á, Menacho K, Mfuko C, Mills K, Millward S, Mitchelmore O, Moon C, Moon J, Muñoz Sandoval D, Murray SM, Noursadeghi M, Otter A, Pade C, Palma S, Parker R, Patel K, Pawarova M, Petersen SE, Piniera B, Pieper FP, Rannigan L, Rapala A, Reynolds CJ, Richards A, Robathan M, Rosenheim J, Rowe C, Royds M, Sackville West J, Sambile G, Schmidt NM, Selman H, Semper A, Seraphim A, Simion M, Smit A, Sugimoto M, Swadling L, Taylor S, Temperton N, Thomas S, Thornton GD, Treibel TA, Tucker A, Varghese A, Veerapen J, Vijayakumar M, Warner T, Welch S, White H, Wodehouse T, Wynne L, Zahedi D, Chain B, and Moon JC

Subjects
Animals, Antibodies, Neutralizing immunology, Antibodies, Viral immunology, Cross Reactions, Humans, Mice, Spike Glycoprotein, Coronavirus genetics, Spike Glycoprotein, Coronavirus immunology, B-Lymphocytes immunology, BNT162 Vaccine immunology, BNT162 Vaccine therapeutic use, COVID-19 immunology, COVID-19 prevention & control, Immunization, Secondary, SARS-CoV-2 genetics, SARS-CoV-2 immunology, T-Lymphocytes immunology
Abstract

The Omicron, or Pango lineage B.1.1.529, variant of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) carries multiple spike mutations with high transmissibility and partial neutralizing antibody (nAb) escape. Vaccinated individuals show protection against severe disease, often attributed to primed cellular immunity. We investigated T and B cell immunity against B.1.1.529 in triple BioNTech BNT162b2 messenger RNA-vaccinated health care workers (HCWs) with different SARS-CoV-2 infection histories. B and T cell immunity against previous variants of concern was enhanced in triple-vaccinated individuals, but the magnitude of T and B cell responses against B.1.1.529 spike protein was reduced. Immune imprinting by infection with the earlier B.1.1.7 (Alpha) variant resulted in less durable binding antibody against B.1.1.529. Previously infection-naïve HCWs who became infected during the B.1.1.529 wave showed enhanced immunity against earlier variants but reduced nAb potency and T cell responses against B.1.1.529 itself. Previous Wuhan Hu-1 infection abrogated T cell recognition and any enhanced cross-reactive neutralizing immunity on infection with B.1.1.529.

Published
2022
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28. The Alpha variant was not associated with excess nosocomial SARS-CoV-2 infection in a multi-centre UK hospital study.

Author

Boshier FAT, Venturini C, Stirrup O, Guerra-Assunção JA, Alcolea-Medina A, Becket AH, Byott M, Charalampous T, Filipe ADS, Frampton D, Glaysher S, Khan T, Kulasegara-Shylini R, Kele B, Monahan IM, Mollett G, Parker M, Pelosi E, Randell P, Roy S, Taylor JF, Weller SJ, Wilson-Davies E, Wade P, Williams R, Copas AJ, Cutino-Moguel T, Freemantle N, Hayward AC, Holmes A, Hughes J, Mahungu TW, Nebbia G, Nastouli E, Partridge DG, Pope CF, Price JR, Robson SC, Saeed K, Shin GY, de Silva TI, Snell LB, Thomson EC, Witney AA, and Breuer J

Subjects
Hospitals, Humans, SARS-CoV-2, United Kingdom epidemiology, COVID-19, Cross Infection epidemiology
Abstract

Objectives: Recently emerging SARS-CoV-2 variants have been associated with an increased rate of transmission within the community. We sought to determine whether this also resulted in increased transmission within hospitals., Methods: We collected viral sequences and epidemiological data of patients with community and healthcare associated SARS-CoV-2 infections, sampled from 16th November 2020 to 10th January 2021, from nine hospitals participating in the COG-UK HOCI study. Outbreaks were identified using ward information, lineage and pairwise genetic differences between viral sequences., Results: Mixed effects logistic regression analysis of 4184 sequences showed healthcare-acquired infections were no more likely to be identified as the Alpha variant than community acquired infections. Nosocomial outbreaks were investigated based on overlapping ward stay and SARS-CoV-2 genome sequence similarity. There was no significant difference in the number of patients involved in outbreaks caused by the Alpha variant compared to outbreaks caused by other lineages., Conclusions: We find no evidence to support it causing more nosocomial transmission than previous lineages. This suggests that the stringent infection prevention measures already in place in UK hospitals contained the spread of the Alpha variant as effectively as other less transmissible lineages, providing reassurance of their efficacy against emerging variants of concern., (Copyright © 2021. Published by Elsevier Ltd.)

Published
2021
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29. Blood transcriptional biomarkers of acute viral infection for detection of pre-symptomatic SARS-CoV-2 infection: a nested, case-control diagnostic accuracy study.

Author

Gupta RK, Rosenheim J, Bell LC, Chandran A, Guerra-Assuncao JA, Pollara G, Whelan M, Artico J, Joy G, Kurdi H, Altmann DM, Boyton RJ, Maini MK, McKnight A, Lambourne J, Cutino-Moguel T, Manisty C, Treibel TA, Moon JC, Chain BM, and Noursadeghi M

Subjects
Adolescent, Adult, Biomarkers, Case-Control Studies, Female, Humans, Male, Middle Aged, Prospective Studies, SARS-CoV-2 genetics, Sensitivity and Specificity, COVID-19 diagnosis
Abstract

Background: We hypothesised that host-response biomarkers of viral infections might contribute to early identification of individuals infected with SARS-CoV-2, which is critical to breaking the chains of transmission. We aimed to evaluate the diagnostic accuracy of existing candidate whole-blood transcriptomic signatures for viral infection to predict positivity of nasopharyngeal SARS-CoV-2 PCR testing., Methods: We did a nested case-control diagnostic accuracy study among a prospective cohort of health-care workers (aged ≥18 years) at St Bartholomew's Hospital (London, UK) undergoing weekly blood and nasopharyngeal swab sampling for whole-blood RNA sequencing and SARS-CoV-2 PCR testing, when fit to attend work. We identified candidate blood transcriptomic signatures for viral infection through a systematic literature search. We searched MEDLINE for articles published between database inception and Oct 12, 2020, using comprehensive MeSH and keyword terms for "viral infection", "transcriptome", "biomarker", and "blood". We reconstructed signature scores in blood RNA sequencing data and evaluated their diagnostic accuracy for contemporaneous SARS-CoV-2 infection, compared with the gold standard of SARS-CoV-2 PCR testing, by quantifying the area under the receiver operating characteristic curve (AUROC), sensitivities, and specificities at a standardised Z score of at least 2 based on the distribution of signature scores in test-negative controls. We used pairwise DeLong tests compared with the most discriminating signature to identify the subset of best performing biomarkers. We evaluated associations between signature expression, viral load (using PCR cycle thresholds), and symptom status visually and using Spearman rank correlation. The primary outcome was the AUROC for discriminating between samples from participants who tested negative throughout the study (test-negative controls) and samples from participants with PCR-confirmed SARS-CoV-2 infection (test-positive participants) during their first week of PCR positivity., Findings: We identified 20 candidate blood transcriptomic signatures of viral infection from 18 studies and evaluated their accuracy among 169 blood RNA samples from 96 participants over 24 weeks. Participants were recruited between March 23 and March 31, 2020. 114 samples were from 41 participants with SARS-CoV-2 infection, and 55 samples were from 55 test-negative controls. The median age of participants was 36 years (IQR 27-47) and 69 (72%) of 96 were women. Signatures had little overlap of component genes, but were mostly correlated as components of type I interferon responses. A single blood transcript for IFI27 provided the highest accuracy for discriminating between test-negative controls and test-positive individuals at the time of their first positive SARS-CoV-2 PCR result, with AUROC of 0·95 (95% CI 0·91-0·99), sensitivity 0·84 (0·70-0·93), and specificity 0·95 (0·85-0·98) at a predefined threshold (Z score >2). The transcript performed equally well in individuals with and without symptoms. Three other candidate signatures (including two to 48 transcripts) had statistically equivalent discrimination to IFI27 (AUROCs 0·91-0·95)., Interpretation: Our findings support further urgent evaluation and development of blood IFI27 transcripts as a biomarker for early phase SARS-CoV-2 infection for screening individuals at high risk of infection, such as contacts of index cases, to facilitate early case isolation and early use of antiviral treatments as they emerge., Funding: Barts Charity, Wellcome Trust, and National Institute of Health Research., Competing Interests: We declare no competing interests., (© 2021 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license.)

Published
2021
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30. Prior SARS-CoV-2 infection rescues B and T cell responses to variants after first vaccine dose.

Author

Reynolds CJ, Pade C, Gibbons JM, Butler DK, Otter AD, Menacho K, Fontana M, Smit A, Sackville-West JE, Cutino-Moguel T, Maini MK, Chain B, Noursadeghi M, Brooks T, Semper A, Manisty C, Treibel TA, Moon JC, Valdes AM, McKnight Á, Altmann DM, and Boyton R

Abstract

SARS-CoV-2 vaccine rollout has coincided with the spread of variants of concern. We investigated if single dose vaccination, with or without prior infection, confers cross protective immunity to variants. We analyzed T and B cell responses after first dose vaccination with the Pfizer/BioNTech mRNA vaccine BNT162b2 in healthcare workers (HCW) followed longitudinally, with or without prior Wuhan-Hu-1 SARS-CoV-2 infection. After one dose, individuals with prior infection showed enhanced T cell immunity, antibody secreting memory B cell response to spike and neutralizing antibodies effective against B.1.1.7 and B.1.351. By comparison, HCW receiving one vaccine dose without prior infection showed reduced immunity against variants. B.1.1.7 and B.1.351 spike mutations resulted in increased, abrogated or unchanged T cell responses depending on human leukocyte antigen (HLA) polymorphisms. Single dose vaccination with BNT162b2 in the context of prior infection with a heterologous variant substantially enhances neutralizing antibody responses against variants., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).)

Published
2021
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31. Disparities of SARS-CoV-2 Nucleoprotein-Specific IgG in Healthcare Workers in East London, UK.

Author

Choudhry N, Drysdale K, Usai C, Leighton D, Sonagara V, Buchanan R, Nijjar M, Thomas S, Hopkins M, Cutino-Moguel T, Gill US, Foster GR, and Kennedy PT

Abstract

Introduction: SARS-CoV-2 antibody detection serves as an important diagnostic marker for past SARS-CoV-2 infection and is essential to determine the spread of COVID-19, monitor potential COVID-19 long-term effects, and to evaluate possible protection from reinfection. A study was conducted across three hospital sites in a large central London NHS Trust in the UK, to evaluate the prevalence and duration of SARS-CoV-2 IgG antibody positivity in healthcare workers. Methods: A matrix equivalence study consisting of 228 participants was undertaken to evaluate the Abbott Panbio™ COVID-19 IgG/IgM rapid test device. Subsequently, 2001 evaluable healthcare workers (HCW), representing a diverse population, were enrolled in a HCW study between June and August 2020. A plasma sample from each HCW was evaluated using the Abbott Panbio™ COVID-19 IgG/IgM rapid test device, with confirmation of IgG-positive results by the Abbott Architect TM SARS-CoV-2 IgG assay. 545 participants, of whom 399 were antibody positive at enrolment, were followed up at 3 months. Results: The Panbio™ COVID-19 IgG/IgM rapid test device demonstrated a high concordance with laboratory tests. SARS-CoV-2 antibodies were detected in 506 participants (25.3%) at enrolment, with a higher prevalence in COVID-19 frontline (28.3%) than non-frontline (19.9%) staff. At follow-up, 274/399 antibody positive participants (68.7%) retained antibodies; 4/146 participants negative at enrolment (2.7%) had seroconverted. Non-white ethnicity, older age, hypertension and COVID-19 symptoms were independent predictors of higher antibody levels (OR 1.881, 2.422-3.034, 2.128, and 1.869 respectively), based on Architect™ index quartiles; participants in the first three categories also showed a greater antibody persistence at 3 months. Conclusion: The SARS-CoV-2 anti-nucleocapsid IgG positivity rate among healthcare staff was high, declining by 31.3% during the 3-month follow-up interval. Interestingly, the IgG-positive participants with certain risk factors for severe COVID-19 illness (older age, Black or Asian Ethnicity hypertension) demonstrated greater persistence over time when compared to the IgG-positive participants without these risk factors., Competing Interests: The authors declare that this study received funding from Abbott Rapid Diagnostics. The funder had the following involvement in the study: study concept, data analysis, statistical analysis, admin/technical support, ethics and critical review of manuscript, Electronic Data Capture database development and management, statistical programming., (Copyright © 2021 Choudhry, Drysdale, Usai, Leighton, Sonagara, Buchanan, Nijjar, Thomas, Hopkins, Cutino-Moguel, Gill, Foster and Kennedy.)

Published
2021
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32. Time series analysis and mechanistic modelling of heterogeneity and sero-reversion in antibody responses to mild SARS‑CoV-2 infection.

Author

Manisty C, Treibel TA, Jensen M, Semper A, Joy G, Gupta RK, Cutino-Moguel T, Andiapen M, Jones J, Taylor S, Otter A, Pade C, Gibbons J, Lee J, Bacon J, Thomas S, Moon C, Jones M, Williams D, Lambourne J, Fontana M, Altmann DM, Boyton R, Maini M, McKnight A, Chain B, Noursadeghi M, and Moon JC

Subjects
Antibodies, Neutralizing immunology, Antibodies, Viral immunology, COVID-19 diagnosis, Health Personnel statistics & numerical data, Humans, Immunoglobulin A blood, Immunoglobulin G blood, Phosphoproteins immunology, Protein Domains immunology, Antibodies, Neutralizing blood, Antibodies, Viral blood, COVID-19 blood, Coronavirus Nucleocapsid Proteins immunology, SARS-CoV-2 immunology, Spike Glycoprotein, Coronavirus immunology
Abstract

Background: SARS-CoV-2 serology is used to identify prior infection at individual and at population level. Extended longitudinal studies with multi-timepoint sampling to evaluate dynamic changes in antibody levels are required to identify the time horizon in which these applications of serology are valid, and to explore the longevity of protective humoral immunity., Methods: Healthcare workers were recruited to a prospective cohort study from the first SARS-CoV-2 epidemic peak in London, undergoing weekly symptom screen, viral PCR and blood sampling over 16-21 weeks. Serological analysis (n =12,990) was performed using semi-quantitative Euroimmun IgG to viral spike S1 domain and Roche total antibody to viral nucleocapsid protein (NP) assays. Comparisons were made to pseudovirus neutralizing antibody measurements., Findings: A total of 157/729 (21.5%) participants developed positive SARS-CoV-2 serology by one or other assay, of whom 31.0% were asymptomatic and there were no deaths. Peak Euroimmun anti-S1 and Roche anti-NP measurements correlated (r = 0.57, p<0.0001) but only anti-S1 measurements correlated with near-contemporary pseudovirus neutralising antibody titres (measured at 16-18 weeks, r = 0.57, p<0.0001). By 21 weeks' follow-up, 31/143 (21.7%) anti-S1 and 6/150 (4.0%) anti-NP measurements reverted to negative. Mathematical modelling revealed faster clearance of anti-S1 compared to anti-NP (median half-life of 2.5 weeks versus 4.0 weeks), earlier transition to lower levels of antibody production (median of 8 versus 13 weeks), and greater reductions in relative antibody production rate after the transition (median of 35% versus 50%)., Interpretation: Mild SARS-CoV-2 infection is associated with heterogeneous serological responses in Euroimmun anti-S1 and Roche anti-NP assays. Anti-S1 responses showed faster rates of clearance, more rapid transition from high to low level production rate and greater reduction in production rate after this transition. In mild infection, anti-S1 serology alone may underestimate incident infections. The mechanisms that underpin faster clearance and lower rates of sustained anti-S1 production may impact on the longevity of humoral immunity., Funding: Charitable donations via Barts Charity, Wellcome Trust, NIHR., Competing Interests: Declaration of Competing Interests DA and RB report consultancy fees from Oxford Immunotec, RKG reports grants from NIHR, during the conduct of the study; CM reports grants from Barts Charity during the conduct of the study; MN reports grants from Wellcome Trust, during the conduct of the study; DW reports personal fees from Barts Health NHS Trust during the conduct of the study. The authors declare no conflicts of interest., (Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.)

Published
2021
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33. Discordant neutralizing antibody and T cell responses in asymptomatic and mild SARS-CoV-2 infection.

Author

Reynolds CJ, Swadling L, Gibbons JM, Pade C, Jensen MP, Diniz MO, Schmidt NM, Butler DK, Amin OE, Bailey SNL, Murray SM, Pieper FP, Taylor S, Jones J, Jones M, Lee WJ, Rosenheim J, Chandran A, Joy G, Di Genova C, Temperton N, Lambourne J, Cutino-Moguel T, Andiapen M, Fontana M, Smit A, Semper A, O'Brien B, Chain B, Brooks T, Manisty C, Treibel T, Moon JC, Noursadeghi M, Altmann DM, Maini MK, McKnight Á, and Boyton RJ

Subjects
Antibodies, Neutralizing blood, Antibodies, Viral blood, Antibodies, Viral immunology, Case-Control Studies, Cross-Sectional Studies, Humans, SARS-CoV-2 immunology, Antibodies, Neutralizing immunology, Asymptomatic Infections, COVID-19 immunology, T-Lymphocytes immunology
Abstract

Understanding the nature of immunity following mild/asymptomatic infection with SARS-CoV-2 is crucial to controlling the pandemic. We analyzed T cell and neutralizing antibody responses in 136 healthcare workers (HCW) 16-18 weeks after United Kingdom lockdown, 76 of whom had mild/asymptomatic SARS-CoV-2 infection captured by serial sampling. Neutralizing antibodies (nAb) were present in 89% of previously infected HCW. T cell responses tended to be lower following asymptomatic infection than in those reporting case-definition symptoms of COVID-19, while nAb titers were maintained irrespective of symptoms. T cell and antibody responses were sometimes discordant. Eleven percent lacked nAb and had undetectable T cell responses to spike protein but had T cells reactive with other SARS-CoV-2 antigens. Our findings suggest that the majority of individuals with mild or asymptomatic SARS-CoV-2 infection carry nAb complemented by multispecific T cell responses at 16-18 weeks after mild or asymptomatic SARS-CoV-2 infection., (Copyright © 2020, American Association for the Advancement of Science.)

Published
2020
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34. Healthcare Workers Bioresource: Study outline and baseline characteristics of a prospective healthcare worker cohort to study immune protection and pathogenesis in COVID-19.

Author

Augusto JB, Menacho K, Andiapen M, Bowles R, Burton M, Welch S, Bhuva AN, Seraphim A, Pade C, Joy G, Jensen M, Davies RH, Captur G, Fontana M, Montgomery H, O'Brien B, Hingorani AD, Cutino-Moguel T, McKnight Á, Abbass H, Alfarih M, Alldis Z, Baca GL, Boulter A, Bracken OV, Bullock N, Champion N, Chan C, Couto-Parada X, Dieobi-Anene K, Feehan K, Figtree G, Figtree MC, Finlay M, Forooghi N, Gibbons JM, Griffiths P, Hamblin M, Howes L, Itua I, Jones M, Jardim V, Kapil V, Jason Lee WY, Mandadapu V, Mfuko C, Mitchelmore O, Palma S, Patel K, Petersen SE, Piniera B, Raine R, Rapala A, Richards A, Sambile G, Couto de Sousa J, Sugimoto M, Thornton GD, Artico J, Zahedi D, Parker R, Robathan M, Hickling LM, Ntusi N, Semper A, Brooks T, Jones J, Tucker A, Veerapen J, Vijayakumar M, Wodehouse T, Wynne L, Treibel TA, Noursadeghi M, Manisty C, and Moon JC

Abstract

Background : Most biomedical research has focused on sampling COVID-19 patients presenting to hospital with advanced disease, with less focus on the asymptomatic or paucisymptomatic. We established a bioresource with serial sampling of health care workers (HCWs) designed to obtain samples before and during mainly mild disease, with follow-up sampling to evaluate the quality and duration of immune memory. Methods : We conducted a prospective study on HCWs from three hospital sites in London, initially at a single centre (recruited just prior to first peak community transmission in London), but then extended to multiple sites 3 weeks later (recruitment still ongoing, target n=1,000). Asymptomatic participants attending work complete a health questionnaire, and provide a nasal swab (for SARS-CoV-2 RNA by RT-PCR tests) and blood samples (mononuclear cells, serum, plasma, RNA and DNA are biobanked) at 16 weekly study visits, and at 6 and 12 months. Results : Preliminary baseline results for the first 731 HCWs (400 single-centre, 331 multicentre extension) are presented. Mean age was 38±11 years; 67% are female, 31% nurses, 20% doctors, and 19% work in intensive care units. COVID-19-associated risk factors were: 37% black, Asian or minority ethnicities; 18% smokers; 13% obesity; 11% asthma; 7% hypertension and 2% diabetes mellitus. At baseline, 41% reported symptoms in the preceding 2 weeks. Preliminary test results from the initial cohort (n=400) are available: PCR at baseline for SARS-CoV-2 was positive in 28 of 396 (7.1%, 95% CI 4.9-10.0%) and 15 of 385 (3.9%, 2.4-6.3%) had circulating IgG antibodies. Conclusions : This COVID-19 bioresource established just before the peak of infections in the UK will provide longitudinal assessments of incident infection and immune responses in HCWs through the natural time course of disease and convalescence. The samples and data from this bioresource are available to academic collaborators by application  https://covid-consortium.com/application-for-samples/., Competing Interests: No competing interests were disclosed., (Copyright: © 2020 Augusto JB et al.)

Published
2020
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