Incidence of diabetes mellitus following hospitalisation for COVID-19 in the United Kingdom: A prospective observational study

Freya Tyrer; Safoora Gharibzadeh; Clare Gillies; Claire Lawson; Ash Routen; Nazrul Islam; Cameron Razieh; Francesco Zaccardi; Tom Yates; Melanie J Davies; Christopher E Brightling; James D Chalmers; Annemarie B Docherty; Omer Elneima; Rachael A Evans; Neil J Greening; Victoria C Harris; Ewen M Harrison; Ling-Pei Ho; Alex Horsley; Linzy Houchen-Wolloff; Olivia C Leavy; Nazir I Lone; Michael Marks; Hamish J C McAuley; Krisnah Poinasamy; Jennifer K Quint; Betty Raman; Matthew Richardson; Ruth Saunders; Marco Sereno; Aarti Shikotra; Amish Singapuri; Louise V Wain; Kamlesh Khunti; PHOSP‐COVID Study Collaborative Group

doi:10.1111/dom.16071

Incidence of diabetes mellitus following hospitalisation for COVID-19 in the United Kingdom: A prospective observational study

Diabetes Obes Metab. 2024 Nov 20. doi: 10.1111/dom.16071. Online ahead of print.

Authors

Freya Tyrer¹, Safoora Gharibzadeh¹, Clare Gillies¹, Claire Lawson¹, Ash Routen², Nazrul Islam³, Cameron Razieh¹, Francesco Zaccardi¹, Tom Yates⁴, Melanie J Davies⁴, Christopher E Brightling⁵, James D Chalmers⁶, Annemarie B Docherty⁷, Omer Elneima⁵, Rachael A Evans⁵, Neil J Greening⁵, Victoria C Harris⁵, Ewen M Harrison⁷, Ling-Pei Ho⁸, Alex Horsley⁹, Linzy Houchen-Wolloff¹⁰, Olivia C Leavy¹¹, Nazir I Lone⁷, Michael Marks¹², Hamish J C McAuley⁵, Krisnah Poinasamy¹³, Jennifer K Quint¹⁴, Betty Raman¹⁵, Matthew Richardson⁵, Ruth Saunders⁵, Marco Sereno⁵, Aarti Shikotra¹⁶, Amish Singapuri⁵, Louise V Wain¹¹, Kamlesh Khunti^{1

4}; PHOSP‐COVID Study Collaborative Group

Collaborators

PHOSP‐COVID Study Collaborative Group:
C E Brightling, R A Evans, L V Wain, J D Chalmers, V C Harris, L P Ho, A Horsley, M Marks, K Poinasamy, B Raman, A Shikotra, A Singapuri, C E Brightling, R A Evans, L V Wain, R Dowling, C Edwardson, O Elneima, S Finney, N J Greening, B Hargadon, V C Harris, L Houchen-Wolloff, O C Leavy, H J C McAuley, C Overton, T Plekhanova, R M Saunders, M Sereno, A Singapuri, A Shikotra, C Taylor, S Terry, C Tong, B Zhao, D Lomas, E Sapey, C Berry, C E Bolton, N Brunskill, E R Chilvers, R Djukanovic, Y Ellis, D Forton, N French, J George, N A Hanley, N Hart, L McGarvey, N Maskell, H McShane, M Parkes, D Peckham, P Pfeffer, A Sayer, A Sheikh, A A R Thompson, N Williams, C E Brightling, W Greenhalf, M G Semple, M Ashworth, H E Hardwick, L Lavelle-Langham, W Reynolds, M Sereno, R M Saunders, A Singapuri, V Shaw, A Shikotra, B Venson, L V Wain, A B Docherty, E M Harrison, A Sheikh, J K Baillie, C E Brightling, L Daines, R Free, R A Evans, S Kerr, O C Leavy, N I Lone, H J C McAuley, R Pius, J Quint, M Richardson, M Sereno, M Thorpe, L V Wain, M Halling-Brown, F Gleeson, J Jacob, S Neubauer, B Raman, S Siddiqui, J M Wild, S Aslani, P Jezzard, H Lamlum, W Lilaonitkul, E Tunnicliffe, J Willoughby, L V Wain, J K Baillie, H Baxendale, C E Brightling, M Brown, J D Chalmers, R A Evans, B Gooptu, W Greenhalf, H E Hardwick, R G Jenkins, D Jones, I Koychev, C Langenberg, A Lawrie, P L Molyneaux, A Shikotra, J Pearl, M Ralser, N Sattar, R M Saunders, J T Scott, T Shaw, D Thomas, D Wilkinson, L G Heaney, A De Soyza, D Adeloye, C E Brightling, J S Brown, J Busby, J D Chalmers, C Echevarria, L Daines, O Elneima, R A Evans, J Hurst, P Novotny, P Pfeffer, K Poinasamy, J Quint, I Rudan, E Sapey, M Shankar-Hari, A Sheikh, S Siddiqui, S Walker, B Zheng, J R Geddes, M Hotopf, K Abel, R Ahmed, L Allan, C Armour, D Baguley, D Baldwin, C Ballard, K Bhui, G Breen, M Broome, T Brugha, E Bullmore, D Burn, F Callard, J Cavanagh, T Chalder, D Clark, A David, B Deakin, H Dobson, B Elliott, J Evans, R Francis, E Guthrie, P Harrison, M Henderson, A Hosseini, N Huneke, M Husain, T Jackson, I Jones, T Kabir, P Kitterick, A Korszun, I Koychev, J Kwan, A Lingford-Hughes, P Mansoori, H McAllister-Williams, K McIvor, L Milligan, R Morriss, E Mukaetova-Ladinska, K Munro, A Nevado-Holgado, T Nicholson, S Paddick, C Pariante, J Pimm, K Saunders, M Sharpe, G Simons, R Upthegrove, S Wessely, G P McCann, S Amoils, C Antoniades, A Banerjee, R Bell, A Bularga, C Berry, P Chowienczyk, J P Greenwood, A D Hughes, K Khunti, L Kingham, C Lawson, K Mangion, N L Mills, A J Moss, S Neubauer, B Raman, A N Sattar, C L Sudlow, M Toshner, P J M Openshaw, D Altmann, J K Baillie, R Batterham, H Baxendale, N Bishop, C E Brightling, P C Calder, R A Evans, J L Heeney, T Hussell, P Klenerman, J M Lord, P Moss, S L Rowland-Jones, W Schwaeble, M G Semple, R S Thwaites, L Turtle, L V Wain, S Walmsley, D Wraith, M J Rowland, A Rostron, J K Baillie, B Connolly, A B Docherty, N I Lone, D F McAuley, D Parekh, A Rostron, J Simpson, C Summers, R G Jenkins, J Porter, R J Allen, R Aul, J K Baillie, S Barratt, P Beirne, J Blaikley, R C Chambers, N Chaudhuri, C Coleman, E Denneny, L Fabbri, P M George, M Gibbons, F Gleeson, B Gooptu, B Guillen Guio, I Hall, N A Hanley, L P Ho, E Hufton, J Jacob, I Jarrold, G Jenkins, S Johnson, M G Jones, S Jones, F Khan, P Mehta, J Mitchell, P L Molyneaux, J E Pearl, K Piper Hanley, K Poinasamy, J Quint, D Parekh, P Rivera-Ortega, L C Saunders, M G Semple, J Simpson, D Smith, M Spears, L G Spencer, S Stanel, I Stewart, A A R Thompson, D Thickett, R Thwaites, L V Wain, S Walker, S Walsh, J M Wild, D G Wootton, L Wright, S Heller, M J Davies, H Atkins, S Bain, J Dennis, K Ismail, D Johnston, P Kar, K Khunti, C Langenberg, P McArdle, A McGovern, T Peto, J Petrie, E Robertson, N Sattar, K Shah, J Valabhji, B Young, L S Howard, Mark Toshner, C Berry, P Chowienczyk, D Lasserson, A Lawrie, O C Leavy, J Mitchell, J Newman, L Price, J Quint, A Reddy, J Rossdale, N Sattar, C Sudlow, A A R Thompson, J M Wild, M Wilkins, S J Singh, W D-C Man, J M Lord, N J Greening, T Chalder, J T Scott, N Armstrong, E Baldry, M Baldwin, N Basu, M Beadsworth, L Bishop, C E Bolton, A Briggs, M Buch, G Carson, J Cavanagh, H Chinoy, E Daynes, S Defres, R A Evans, P Greenhaff, S Greenwood, M Harvie, M Husain, S MacDonald, A McArdle, H J C McAuley, A McMahon, M McNarry, G Mills, C Nolan, K O'Donnell, D Parekh, J Sargent, L Sigfrid, M Steiner, D Stensel, A L Tan, J Whitney, D Wilkinson, D Wilson, M Witham, D G Wootton, T Yates, D Thomas, N Brunskill, S Francis, S Greenwood, C Laing, K Bramham, P Chowdhury, A Frankel, L Lightstone, S McAdoo, K McCafferty, M Ostermann, N Selby, C Sharpe, M Willicombe, A Shaw, L Armstrong, B Hairsine, H Henson, C Kurasz, L Shenton, S Fairbairn, A Dell, N Hawkings, J Haworth, M Hoare, A Lucey, V Lewis, G Mallison, H Nassa, C Pennington, A Price, C Price, A Storrie, G Willis, S Young, P Pfeffer, K Chong-James, C David, W Y James, C Manisty, A Martineau, O Zongo, A Sanderson, L G Heaney, C Armour, V Brown, T Craig, S Drain, B King, N Magee, D McAulay, E Major, L McGarvey, J McGinness, R Stone, A Haggar, A Bolger, F Davies, J Lewis, A Lloyd, R Manley, E McIvor, D Menzies, K Roberts, W Saxon, D Southern, C Subbe, V Whitehead, H El-Taweel, J Dawson, L Robinson, D Saralaya, L Brear, K Regan, K Storton, J Fuld, A Bermperi, I Cruz, K Dempsey, A Elmer, H Jones, S Jose, S Marciniak, M Parkes, C Ribeiro, J Taylor, M Toshner, L Watson, J Weir McCall, J Worsley, R Sabit, L Broad, A Buttress, T Evans, M Haynes, L Jones, L Knibbs, A McQueen, C Oliver, K Paradowski, J Williams, E Harris, C Sampson, C Lynch, E Davies, C Evenden, A Hancock, K Hancock, M Rees, L Roche, N Stroud, T Thomas-Woods, M Babores, J Bradley-Potts, M Holland, N Keenan, S Shashaa, H Wassall, E Beranova, H Weston, T Cosier, L Austin, J Deery, T Hazelton, C Price, H Ramos, R Solly, S Turney, L Pearce, W McCormick, S Pugmire, W Stoker, A Wilson, N Hart, L A Aguilar Jimenez, G Arbane, S Betts, K Bisnauthsing, A Dewar, P Chowdhury, A Chiribiri, A Dewar, G Kaltsakas, H Kerslake, M M Magtoto, P Marino, L M Martinez, C O'Brien, M Ostermann, J Rossdale, T S Solano, E Wynn, N Williams, W Storrar, M Alvarez Corral, A Arias, E Bevan, D Griffin, J Martin, J Owen, S Payne, A Prabhu, A Reed, C Wrey Brown, C Lawson, T Burdett, J Featherstone, A Layton, C Mills, L Stephenson, N Easom, P Atkin, K Brindle, M G Crooks, K Drury, R Flockton, L Holdsworth, A Richards, D L Sykes, S Thackray-Nocera, C Wright, K E Lewis, A Mohamed, G Ross, S Coetzee, K Davies, R Hughes, R Loosley, L O'Brien, Z Omar, H McGuinness, E Perkins, J Phipps, A Taylor, H Tench, R Wolf-Roberts, L S Howard, O Kon, D C Thomas, S Anifowose, L Burden, E Calvelo, B Card, C Carr, E R Chilvers, D Copeland, P Cullinan, P Daly, L Evison, T Fayzan, H Gordon, S Haq, R G Jenkins, C King, K March, M Mariveles, L McLeavey, N Mohamed, S Moriera, U Munawar, J Nunag, U Nwanguma, L Orriss-Dib, D O'Regan, A Ross, M Roy, E Russell, K Samuel, J Schronce, N Simpson, L Tarusan, C Wood, N Yasmin, R Reddy, A-M Guerdette, M Hewitt, K Warwick, S White, A M Shah, C J Jolley, O Adeyemi, R Adrego, H Assefa-Kebede, J Breeze, M Brown, S Byrne, T Chalder, A Chiribiri, P Dulawan, N Hart, A Hayday, A Hoare, A Knighton, M Malim, C O'Brien, S Patale, I Peralta, N Powell, A Ramos, K Shevket, F Speranza, A Te, P Beirne, A Ashworth, J Clarke, C Coupland, M Dalton, E Wade, C Favager, J Greenwood, J Glossop, L Hall, T Hardy, A Humphries, J Murira, D Peckham, S Plein, J Rangeley, G Saalmink, A L Tan, B Whittam, N Window, J Woods, G Coakley, D G Wootton, L Turtle, L Allerton, A M All, M Beadsworth, A Berridge, J Brown, S Cooper, A Cross, D Cuthbertson, S Defres, S L Dobson, J Earley, N French, W Greenhalf, H E Hardwick, K Hainey, J Hawkes, V Highett, S Kaprowska, G Kemp, A L Key, S Koprowska, L Lavelle-Langham, N Lewis-Burke, G Madzamba, F Malein, S Marsh, C Mears, L Melling, M J Noonan, L Poll, J Pratt, E Richardson, A Rowe, M G Semple, V Shaw, K A Tripp, B Vinson, L O Wajero, S A Williams-Howard, J Wyles, S N Diwanji, P Papineni, S Gurram, S Quaid, G F Tiongson, E Watson, B Al-Sheklly, A Horsley, C Avram, J Blaikely, M Buch, N Choudhury, D Faluyi, T Felton, T Gorsuch, N A Hanley, T Hussell, Z Kausar, C Miller, N Odell, R Osbourne, K Piper Hanley, K Radhakrishnan, S Stockdale, A De Soyza, C Echevarria, A Ayoub, J Brown, G Burns, G Davies, H Fisher, C Francis, A Greenhalgh, P Hogarth, J Hughes, K Jiwa, G Jones, G MacGowan, D Price, A Sayer, J Simpson, H Tedd, S Thomas, S West, M Witham, S Wright, A Young, M J McMahon, P Neill, D Anderson, H Bayes, C Berry, D Grieve, I B McInnes, N Basu, A Brown, A Dougherty, K Fallon, L Gilmour, K Mangion, A Morrow, K Scott, R Sykes, R Touyz, E K Sage, F Barrett, A Donaldson, M Patel, D Bell, A Brown, M Brown, R Hamil, K Leitch, L Macliver, J Quigley, A Smith, B Welsh, G Choudhury, J K Baillie, S Clohisey, A Deans, A B Docherty, J Furniss, E M Harrison, S Kelly, N I Lone, D E Newby, A Sheikh, J D Chalmers, D Connell, A Elliott, C Deas, J George, S Mohammed, J Rowland, A R Solstice, D Sutherland, C J Tee, N Maskell, D Arnold, S Barrett, H Adamali, A Dipper, S Dunn, A Morley, L Morrison, L Stadon, S Waterson, H Welch, B Jayaraman, T Light, C E Bolton, P Almeida, J Bonnington, M Chrystal, E Cox, C Dupont, P Greenhaff, A Gupta, L Howard, W Jang, S Linford, L Matthews, R Needham, A Nikolaidis, S Prosper, K Shaw, A K Thomas, L P Ho, N M Rahman, M Ainsworth, A Alamoudi, M Beggs, A Bates, A Bloss, A Burns, P Carter, M Cassar, K M Channon, J Chen, F Conneh, T Dong, R I Evans, E Fraser, X Fu, J R Geddes, F Gleeson, P Harrison, M Havinden-Williams, P Jezzard, N Kanellakis, I Koychev, P Kurupati, X Li, E Lukaschuk, K McGlynn, H McShane, C Megson, K Motohashi, S Neubauer, D Nicoll, G Ogg, E Pacpaco, M Pavlides, Y Peng, N Petousi, J Propescu, N Rahman, B Raman, M J Rowland, K Saunders, M Sharpe, N Talbot, E Tunnicliffe, W D-C Man, B Patel, R E Barker, D Cristiano, N Dormand, M Gummadi, S Kon, K Liyanage, C M Nolan, S Patel, O Polgar, P Shah, S J Singh, J A Walsh, J Hurst, H Jarvis, S Mandal, S Ahmad, S Brill, L Lim, D Matila, O Olaosebikan, C Singh, M Toshner, H Baxendale, L Garner, C Johnson, J Mackie, A Michael, J Pack, K Paques, H Parfrey, J Parmar, N Diar Bakerly, P Dark, D Evans, E Hardy, A Harvey, D Holgate, S Knight, N Mairs, N Majeed, L McMorrow, J Oxton, J Pendlebury, C Summersgill, R Ugwuoke, S Whittaker, W Matimba-Mupaya, S Strong-Sheldrake, S L Rowland-Jones, A A R Thompson, J Bagshaw, M Begum, K Birchall, R Butcher, H Carborn, F Chan, K Chapman, Y Cheng, L Chetham, C Clark, Z Coburn, J Cole, M Dixon, A Fairman, J Finnigan, L Finnigan, H Foot, D Foote, A Ford, R Gregory, K Harrington, L Haslam, L Hesselden, J Hockridge, A Holbourn, B Holroyd-Hind, L Holt, A Howell, E Hurditch, F Ilyas, C Jarman, A Lawrie, E Lee, J-H Lee, R Lenagh, A Lye, I Macharia, M Marshall, A Mbuyisa, J McNeill, S Megson, J Meiring, L Milner, S Misra, H Newell, T Newman, C Norman, L Nwafor, D Pattenadk, M Plowright, J Porter, P Ravencroft, C Roddis, J Rodger, P Saunders, J Sidebottom, J Smith, L Smith, N Steele, G Stephens, R Stimpson, B Thamu, N Tinker, K Turner, H Turton, P Wade, S Walker, J Watson, I Wilson, A Zawia, R Aul, M Ali, A Dunleavy, D Forton, N Msimanga, M Mencias, T Samakomva, S Siddique, J Teixeira, V Tavoukjian, J Hutchinson, L Allsop, K Bennett, P Buckley, M Flynn, M Gill, C Goodwin, M Greatorex, H Gregory, C Heeley, L Holloway, M Holmes, J Kirk, W Lovegrove, T A Sewell, S Shelton, D Sissons, K Slack, S Smith, D Sowter, S Turner, V Whitworth, I Wynter, L Warburton, S Painter, J Tomlinson, C Vickers, T Wainwright, D Redwood, J Tilley, S Palmer, G A Davies, L Connor, A Cook, T Rees, F Thaivalappil, C Thomas, A Butt, M Coulding, H Jones, S Kilroy, J McCormick, J McIntosh, H Savill, V Turner, J Vere, E Fraile, J Ugoji, S S Kon, H Lota, G Landers, M Nasseri, S Portukhay, A Hormis, A Daniels, J Ingham, L Zeidan, M Chablani, L Osborne, M Marks, J S Brown, N Ahwireng, B Bang, D Basire, R C Chambers, A Checkley, R Evans, M Heightman, T Hillman, J Hurst, J Jacob, S Janes, R Jastrub, M Lipman, S Logan, D Lomas, M Merida Morillas, A Pakzad, H Plant, J C Porter, K Roy, E Wall, B Williams, M Xu, D Parekh, N Ahmad Haider, C Atkin, R Baggott, M Bates, A Botkai, A Casey, B Cooper, J Dasgin, K Draxlbauer, N Gautam, J Hazeldine, T Hiwot, S Holden, K Isaacs, T Jackson, S Johnson, V Kamwa, D Lewis, J M Lord, S Madathil, C McGhee, K Mcgee, A Neal, A Newton Cox, J Nyaboko, D Parekh, Z Peterkin, H Qureshi, B Rangelov, L Ratcliffe, E Sapey, J Short, T Soulsby, J Stockley, Z Suleiman, T Thompson, M Ventura, S Walder, C Welch, D Wilson, S Yasmin, K P Yip, P Beckett, C Dickens, U Nanda, C E Brightling, R A Evans, M Aljaroof, N Armstrong, H Arnold, H Aung, M Bakali, M Bakau, M Baldwin, M Bingham, M Bourne, C Bourne, N Brunskill, P Cairns, L Carr, A Charalambou, C Christie, M J Davies, S Diver, S Edwards, C Edwardson, O Elneima, H Evans, J Finch, S 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Affiliations

¹ Leicester Real World Evidence Unit, Diabetes Research Centre, University of Leicester, Leicester, UK.
² Centre for Ethnic Health, Diabetes Research Centre, University of Leicester, Leicester, UK.
³ School of Primary Care, Population Sciences and Medical Education, University of Southampton, Southampton, UK.
⁴ Leicester Diabetes Centre, Diabetes Research Centre, University of Leicester, Leicester, UK.
⁵ The Institute of Lung Health, NIHR Leicester Biomedical Research Centre, University of Leicester, Leicester, UK.
⁶ Ninewells Hospital and Medical School, University of Dundee, Dundee, UK.
⁷ Centre for Medical Informatics, The Usher Institute, University of Edinburgh, Edinburgh, UK.
⁸ MRC Human Immunology Unit, University of Oxford, Oxford, UK.
⁹ Division of Infection, Immunity and Respiratory Medicine, University of Manchester, Manchester, UK.
¹⁰ Centre for Exercise and Rehabilitation Science, NIHR Biomedical Research Centre, University of Leicester, Leicester, UK.
¹¹ Department of Population Health Sciences, University of Leicester, Leicester, UK.
¹² Department of Clinical Research, London School of Hygiene & Tropical Medicine, London, UK.
¹³ Asthma and Lung UK, London, UK.
¹⁴ School of Public Health, Imperial College London, London, UK.
¹⁵ Radcliffe Department of Medicine, University of Oxford, Oxford, UK.
¹⁶ NIHR Leicester Biomedical Research Centre, University of Leicester, Leicester, UK.

PMID: 39563623
DOI: 10.1111/dom.16071

Abstract

Background: People hospitalised for coronavirus disease 2019 (COVID-19) have elevated incidence of diabetes. However, it is unclear whether this is due to shared risk factors, confounding or stress hyperglycaemia in response to acute illness.

Methods: We analysed a multicentre prospective cohort study (PHOSP-COVID) of people ≥18 years discharged from NHS hospitals across the United Kingdom following COVID-19. Individuals were included if they attended at least one research visit with a HbA1c measurement within 14 months of discharge and had no history of diabetes at baseline. The primary outcome was new onset diabetes (any type), as defined by a first glycated haemoglobin (HbA1c) measurement ≥6.5% (≥48 mmol/mol). Follow-up was censored at the last HbA1c measurement. Age-standardised incidence rates and incidence rate ratios (adjusted for age, sex, ethnicity, length of hospital stay, body mass index, smoking, physical activity, deprivation, hypertension, hyperlipidaemia/hypercholesterolaemia, intensive therapy unit admission, invasive mechanical ventilation, corticosteroid use and C-reactive protein score) were calculated using Poisson regression. Incidence rates were compared with the control groups of published clinical trials in the United Kingdom by applying the same inclusion and exclusion criteria, where possible.

Results: Incidence of diabetes was 91.4 per 1000 person-years and was higher in South Asian (incidence rate ratios [IRR] = 3.60; 1.77, 7.32; p < 0.001) and Black ethnic groups (IRR = 2.36; 1.07, 5.21; p = 0.03) compared with White ethnic groups. When restricted to similar characteristics, the incidence rates were similar to those in UK clinical trials data.

Conclusion: Diabetes incidence following hospitalisation for COVID-19 is high, but it remains uncertain whether it is disproportionately higher than pre-pandemic levels.

Keywords: cohort study; population study; real‐world evidence; type 1 diabetes; type 2 diabetes.

Abstract

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