Dinesh Nagi,1 Robert EJ Ryder,2 Yue Ruan,3,4 Benjamin CT Field,5,6 Parth Narendran,7,8 Rajiv Gandhi,9 Sophie Harris,10 Kinga A Várnai,4,11 Jim Davies,4,12 Sarah H Wild,13 Emma G Wilmot,14,15 Kamlesh Khunti,16 Rustam Rea3,4
1 Mid Yorkshire Hospitals NHS Trust, Pinderfields Hospital, Wakefield, UK
2 Sandwell and West Birmingham Hospitals NHS Trust, Birmingham, UK
3 Oxford Centre for Diabetes, Endocrinology and Metabolism, Oxford University Hospitals NHS Foundation Trust, UK
4 Oxford NIHR Biomedical Research Centre, UK
5 Department of Clinical & Experimental Medicine, Faculty of Health & Medical Sciences, University of Surrey, Guildford, UK (ORCiD 0000-0002-1883-1588)
6 Department of Diabetes & Endocrinology, Surrey & Sussex Healthcare NHS Trust, Redhill, Surrey, UK
7 Medical and Dental Sciences, University of Birmingham, Birmingham, UK
8 Diabetes Centre, The Queen Elizabeth Hospital, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK
9 Department of Diabetes & Endocrinology, Sheffield Teaching Hospitals NHS Foundation Trust, UK
10 Diabetes and Endocrinology Department, King’s College Hospital, UK
11 Oxford University Hospitals NHS Foundation Trust, UK
12 Department of Computer Science, University of Oxford, Oxford, UK
13 Usher Institute, University of Edinburgh, Edinburgh, UK
14 Diabetes Department, University Hospitals of Derby and Burton NHS FT, Derby, UK
15 University of Nottingham, Nottingham, UK
16 University Hospitals of Leicester NHS Trust, Diabetes Research Centre, Leicester General Hospital, Leicester, UK
Address for correspondence: Dr Dinesh Nagi
Edna Coates Diabetes & Endocrine Unit, Pinderfields Hospital, Wakefield, West Yorkshire WF1 4DG, UK
Tel: +44 (0)7738 754249 E-mail: d.nagi@nhs.net
https://doi.org/10.15277/bjd.2021.299
We describe the rationale, aims and objectives and the methodology of data collection for the ABCD nationwide audit of individuals admitted to hospital with coronavirus (SARS-CoV-2; COVID-19) and diabetes. The audit was inspired and undertaken by the urgent need to understand the clinical course of COVID-19 in patients with diabetes admitted to hospital in the UK during the pandemic. We wished to understand the clinical behaviour of diabetes per se, post hospital admission and the factors with may be associated with admission to the Intensive Care Unit (ICU) and death due to COVID-19. This was a clinically-led audit. We used existing infrastructure and expertise to collect data using an electronic tool specifically designed and piloted by the steering group members. The clinical variables were chosen to fulfil the main aim of this audit as stated above, and factors influencing the clinical course of COVID-19 in individuals with both type 1 and type 2 diabetes at the time of admission to hospital and during the whole length of stay, until discharge or death from COVID-19. The data collected so far represent a large, multicentre audit with more than 3,500 admissions during the pandemic. We plan to continue collecting additional data and publish ongoing reports of interest to diabetes clinicians with the aim of enhancing knowledge and understanding and thereby improving clinical care of, and outcomes for, people with diabetes who are admitted to hospital with COVID-19 in the UK.
Br J Diabetes 2021;21:96-99
Key words: COVID-19, diabetes, pandemic, COVID-Audit, risk factors and mortality, ABCD nationwide Audit
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2; COVID-19) was first reported in Wuhan, China in December 2019 and has since been responsible for over 2.5 million deaths from COVID-19 infection globally by February 2021.1 Several publications have reported that chronic co-morbidities such as hypertension, diabetes, cardiovascular disease, chronic kidney disease and chronic obstructive pulmonary disease are associated with an increased risk of severe COVID-19 and mortality.2 A population-based study from England (UK) reported that, up to 11 May 2020, 23,698 in-hospital COVID-19-related deaths had occurred, of which 1.5% were people with type 1 diabetes and 31.4% were people with type 2 diabetes.3 The study reported that, after adjustment for age, sex, deprivation, ethnicity and geographical region, the risk of in-hospital COVID-19-related death was 3.51 times greater for people with type 1 diabetes and 2.03 times greater for those with type 2 diabetes compared with people without diabetes.3
Other studies have reported associations between admission hyperglycaemia and in-hospital mortality in people with diabetes.4–6 However, sample sizes have typically been small, derived from single centres or single cities, which precludes differential reporting of outcomes by diabetes subtype. Few studies, except those drawing on large quantities of routinely-collected data, have had sufficient power to describe factors associated with poor outcomes among people with diabetes.7–9 One notable exception is the CORONADO study, based on data collected in centres across France, which has reported characteristics and outcomes for people with diabetes hospitalised for COVID-19 since 10 March 2020. The group’s latest report describes 2,796 patients, 88.2% of whom had type 2 diabetes, with 50.2% being discharged from hospital within 28 days of admission and 20.6% dying.10 In an age-adjusted regression analysis, male sex and history of either microvascular or macrovascular complications were among the baseline factors associated with a poor outcome.10
The impetus and rationale for the Association of British Clinical Diabetologists (ABCD) nationwide audit was the urgent requirement to learn and understand more about the clinical course of COVID-19 in the UK in individuals with diabetes. Early reports indicated a high risk of severe outcome for individuals with diabetes admitted to hospital. In addition, there were indications that the clinical course of diabetes itself was different from patients who were admitted to hospital with acute diabetes decompensation in the absence of a COVID-19 diagnosis. The audit was therefore developed to collect clinical data rapidly on the severity of diabetes at presentation, and the clinical course of diabetes and of COVID-19 during hospital care.
The ABCD has a longstanding, well-established infrastructure for nationwide audit.11 This infrastructure was originally created to allow diabetes specialist teams across the UK to collate real-world experience of new therapies for diabetes.11 More recently, this modus operandi has been extended to other clinical issues including newer glucose monitoring and insulin delivery technologies.11 The dissemination of results from the ABCD audit programme has added to knowledge and understanding of new therapies and technologies, beyond the scope of randomised clinical trials.12
ABCD COVID-19 diabetes audit tool development
A steering group was formed to include individuals with a variety of interests and expertise in clinical audit. The group adopted a pragmatic design, facilitating rapid collection of retrospective data from hospital records, with minimum burden on hard-pressed clinical teams and, through several rounds of iterative discussion, a pilot data collection tool was created. Parameters for data collection were selected for their relevance to diabetes clinical practice and to the emerging science of SARS-CoV-2 and COVID-19. The accessibility and likely reliability of these data within paper and electronic clinical records was assessed through testing by members of the steering group. A finalised set of variables was included in a bespoke tool created in Microsoft Excel. This allowed collection of data in a standardised format for submission to the NIHR Health Informatics Collaborative (NIHR HIC) coordinating centre, based in Oxford University Hospitals NHS Foundation Trust (OUH).13
At each participating centre, diabetes specialist teams assume responsibility for identifying patients with diabetes who have been admitted to hospital with COVID-19 since the beginning of the pandemic, and for collecting and reporting their clinical data in pseudonymised form. Only patients with a positive SARS-CoV-2 test are included in the audit. In practice, this means that identification of patients has occurred in most centres through systematic assessment of the clinical records of all people admitted with a positive SARS-CoV-2 test. In other centres, data have been reported only for patients with diabetes and COVID-19 who required clinical input from the diabetes specialist team. The audit therefore provides an augmented record of clinical experience of diabetes specialist teams across the UK, whilst recognising that it will not be a comprehensive record of all patients with diabetes admitted to hospital with COVID-19.
As of 10 February 2021, data collected from 3,542 patients with type 1 or type 2 diabetes and COVID-19 have been submitted by a total of 42 NHS centres around the UK. For the purpose of this audit, severe COVID-19 was defined as death in hospital and/or admission to the adult intensive care unit (AICU). The database comprises complete data on 212 inpatients with type 1 diabetes and 3,201 with type 2 diabetes hospitalised between March and December 2020. The data include outcomes to discharge or death, for up to 70 days from admission, reflecting the prolonged hospital course of many patients with severe COVID-19.
Data collection, storage and handling
Clinical teams based at UK hospitals were invited to contribute to the audit by word of mouth, by email and by announcement on the ABCD website.14 A centre-specific audit data collection tool was provided to each registered centre. At each centre the tool was maintained behind the NHS firewall in secure servers. As a final step before transfer of data to the NIHR HIC coordinating centre at OUH, pseudonymisation was achieved through replacement of all personal identifiers by a centre-specific code. Transfer of pseudonymised data occurred via secure NHS email. Submissions were checked by the NIHR HIC team and additional information sought from participating centres if necessary. Data were cleaned by the NIHR HIC team to standardise formats – for example, dates, units removed where only results were expected, invalid entries removed or corrected with additional information from the participating centre. The cleaned data were loaded into an MS SQL Server database, hosted on a secure server within OUH, and made available to the analysis team through a LabKey portal. The data analysis has taken place within the secure OUH information governance environment.
Ethical approval
The audit was registered with OUH and a Data Protection Impact Assessment carried out by the steering group was reviewed for use in England and Wales by the OUH Caldicott Guardian and for use in Scotland by the Public Benefit and Privacy Panel (reference 2021-0111). The NHS supports clinical audits, with clear guidance for all NHS trusts and health boards15 on the use of routinely collected clinical data, including submission in pseudonymised form via the secure NHS network. As this is an audit of clinical data gathered routinely during clinical care, there is no requirement for approval by a Research Ethics Committee.15
Variables
Inpatients’ demographic information, clinical characteristics, medication history and laboratory measurements are collected from electronic and paper medical record systems. Demographic data comprise age in years, sex, ethnicity and census-derived Index of Multiple Deprivation decile. Clinical characteristics include weight and height, or BMI; type of diabetes (see Table 1 for details of classification); duration of diabetes; presence or absence of diabetes complications including diabetic ketoacidosis, diabetic foot ulcer, diabetic nephropathy, diabetic peripheral neuropathy, diabetic retinopathy, peripheral vascular disease, ischemic heart disease, myocardial infarction and/or heart failure, cerebrovascular disease (stroke/transient ischemic attack) and other significant co-morbidities (hypertension, dementia, asthma, chronic obstructive pulmonary disease, malignant neoplasm, smoking status). Medication history includes antidiabetic medications and other selected classes (angiotensin converting enzyme inhibitor or angiotensin receptor antagonist, oral corticosteroid, statin, antiplatelet, anticoagulant and regular non-steroidal anti-inflammatory drug).
Laboratory data include latest pre-admission HbA1c and serum creatinine, and the COVID-19 admission blood glucose, pH, bicarbonate, lactate and capillary blood ketone concentration. Dates of the start and finish (if applicable) of each hospital admission are collected in individuals who had diabetes and a positive test for COVID-19, along with the date of the first positive SARS-CoV-2 test (a positive result is a prerequisite for inclusion in the audit). Recorded outcomes include vital status and admission to an AICU. The ABCD audit remains open with information on how to join and new centres can request the data collection sheet from the ABCD secretariat with details of the audit readily available online.16
To the best of our knowledge, this audit comprises the largest cohort yet assembled of people with diabetes admitted to NHS hospitals in the UK with COVID-19 infection for whom detailed clinical information is available. We believe that this audit has several strengths, in particular the detailed biochemical data and long-term outcomes of people admitted to hospital with COVID-19 and diabetes (Table 2). The steering group has started to analyse the data to explore a number of unanswered questions regarding the clinical characteristics and outcomes of the pandemic and its effect on people with diabetes. A summary of the analyses of interest is shown in Box 1. We would encourage hospitals across the UK to submit their data in order to ensure that these analyses are as robust and detailed as possible. Authorship of any publications will follow the usual ABCD guidelines, with all submitting centres referenced as collaborators and larger centres providing titled authorship.
There has been a large number of studies in relation to COVID-19 and diabetes. However, the majority of these have been undertaken using non-contemporaneous data. Few studies have collected data within hospital settings and these have, for the most part, been limited by coming from single centres, with small numbers of patients, limited ethnic diversity, short time frames for determination of outcomes, and a lack of differentiation by type of diabetes. The ABCD nationwide audit will therefore make a significant contribution to the literature on diabetes and COVID-19 as a result of its size, the systematic approach to in-hospital data collection, the multi-ethnic nature of the UK population and the collection of data through to discharge alive or to in-hospital death, reflecting the prolonged hospital course of some patients with severe COVID-19.
The audit is limited by incomplete case ascertainment and reporting of patients with diabetes and COVID-19 in some participating centres, by the absence of a comparator group of people suffering COVID-19 but not diabetes, and by rapid changes in prevalence and inpatient management of COVID-19 that have occurred throughout the pandemic. However, it will provide evidence on patterns of outcomes that are representative of the experience of people with diabetes admitted to hospital with COVID-19 in the UK. We envisage the findings will help to target diabetes-specific advice and interventions for people admitted with COVID-19.
This audit has been conducted using NIHR Health Informatics Collaborative (HIC) data resources at Oxford University Hospitals NHS Foundation Trust.
Acknowledgements: We are grateful to all the people who collected the data for this audit, to Ben Maylor and Joanne Miksza for data template development, and to Melissa Cull of the ABCD Secretariat for administrative support (see Appendix 1 at www.bjd-abcd.com).
Conflict of interest: YR is supported by a Novo Nordisk Post- doctoral Fellowship run in partnership with the University of Oxford. KK is supported by the National Institute for Health Research (NIHR) Applied Research Collaboration East Midlands (ARC EM) and the NIHR Leicester Biomedical Research Centre (BRC). RR is supported by the National Institute for Health Research (NIHR) Oxford Biomedical Research Centre.
Funding: YR’s salary was funded by Novo Nordisk Postdoctoral Fellowship run in partnership with the University of Oxford. RR is partly funded by the National Institute for Health Research (NIHR) Oxford Biomedical Research Centre (BRC).
1. Worldometer. Coronavirus. Available from: https://www.worldometers.info/coronavirus [Accessed 2 March 2021].
2. Singh AK, Gillies CL, Singh R, et al. Prevalence of co-morbidities and their association with mortality in patients with COVID-19: a systematic review and meta-analysis. Diabetes Obes Metab 2020;22(10):1915–24. https://doi.org/10.1111/dom.14124
3. Barron E, Bakhai C, Kar P, et al. Associations of type 1 and type 2 diabetes with COVID-19-related mortality in England: a whole-population study. Lancet Diabetes Endocrinol 2020;8(10):813–22. https://doi.org/10.1016/S2213-8587(20)30272-2
4. Marfella R, Paolisso P, Sardu C, et al. Negative impact of hyperglycaemia on tocilizumab therapy in Covid-19 patients. Diabetes Metab 2020; 46(5):403–5. https://doi.org/10.1016/j.diabet.2020.05.005
5. Li H, Tian S, Chen T, et al. Newly diagnosed diabetes is associated with a higher risk of mortality than known diabetes in hospitalized patients with COVID-19. Diabetes Obes Metab 2020;22(10):1897–906. https://doi.org/10.1111/dom.14099
6. Wang S, Ma P, Zhang S, et al. Fasting blood glucose at admission is an independent predictor for 28-day mortality in patients with COVID-19 without previous diagnosis of diabetes: a multi-centre retrospective study. Diabetologia 2020;63(10):2102–11. https://doi.org/10.1007/s00125-020-05209-1
7. Ebekozien OA, Noor N, Gallagher MP, Alonso GT. Type 1 diabetes and COVID-19: preliminary findings from a multicenter surveillance study in the U.S. Diabetes Care 2020;43(8):e83–e85. https://doi.org/10.2337/dc20-1088
8. Wargny M, Gourdy P, Ludwig L, et al. Type 1 diabetes in people hospitalized for COVID-19: new insights from the CORONADO study. Diabetes Care 2020;43(11):e174–e177. https://doi.org/10.2337/dc20-1217
9. Vamvini M, Lioutas VA, Middelbeek RJW. Characteristics and diabetes control in adults with type 1 diabetes admitted with COVID-19 infection. Diabetes Care 2020;43(10):e120–122. https://doi.org/10.2337/dc20-1540
10. Wargny M, Potier L, Gourdy P, et al. Predictors of hospital discharge and mortality in patients with diabetes and COVID-19: updated results from the nationwide CORONADO study. Diabetologia (published online 17 Feb 2021). https://doi.org/10.1007/s00125-020-05351-w
11. NIHR Health Informatics Collaborative. Available from: https://hic.nihr.ac.uk/ [Accessed 2 March 2021].
12. Association of British Clinical Diabetologists (ABCD). The history of the ABCD nationwide and worldwide audit programme. Available from: http://www.diabetologists-abcd.org.uk/n3/previous_ABCD_audits.htm [Accessed 2 March 2021].
13. Association of British Clinical Diabetologists (ABCD). ABCD Nationwide and Worldwide Audit Programme Publications. Available from: https://abcd.care/abcd-nationwide-and-worldwide-audit-programme-publications [Accessed 2 March 2021].
14. Association of British Clinical Diabetologists (ABCD). Launch of the Covid-19 and diabetes ABCD national audit. Available from: https://abcd.care/announcement/launch-covid-19-and-diabetes-abcd-national-audit (Accessed 2 March 2021].
15. Oxford University Hospitals. Is my project research? Available from: https://www.ouh.nhs.uk/researchers/planning/is-it-research/ [Accessed 2 March 2021].
16. Association of British Clinical Diabetologists (ABCD). ABCD COVID-19 and Diabetes: UK national audit. Available from: http://www.diabetologists-abcd.org.uk/Coronavirus/COVID-19._Diabetes_Nationwide_Audit.htm [Accessed 2 March 2021].
Barts Health NHS Trust, Newham University Hospital: Amy Edwards, Susan Gelding, Kirun Gunganah
Brighton and Sussex University Hospitals NHS Trust, Royal Sussex County Hospital: Ali Chakera, Dominique Rouse
Dartford and Gravesham NHS Trust, Darent Valley Hospital: Amir Hayat, Cynthia Mohandas
East and North Hertfordshire NHS Trust, Lister Hospital: Htet Htet Aung, Su Khant Chel, Nyan Lin, Kavitia Narula, Furruq Quadri, Su Lei Yin, Yin Yin
East Kent Hospitals University NHS Foundation Trust, William Harvey Hospital (Ashford): Alamin Alkundi, Abdelmajid Musa
East Suffolk and North Essex NHS Foundation Trust, Colchester General Hospital: Emma Birbeck, Charles Bodmer
East Sussex Healthcare NHS Trust, Conquest Hospital & Eastbourne District General Hospital: Irene Bossman, Sathis Kumar, Umesh Dashora, Elizabeth Toubi, Mansoor Zafar
George Eliot Hospital NHS Trust, Diabetes Care Team, George Eliot Hospital: Vinod Patel, Amitha Gopinath
Hull University Teaching Hospitals NHS Foundation Trust, Hull Royal Infirmary: Belinda Allan
King's College Hospital NHS Foundation Trust, King's College Hospital: Dharshana Appuhamillage, Khubaib Ayoub, Sophie Harris, Charmaine Ilangaratne, Maliha Iqbal, Rory Maclean, Omar Mustafa
Lancashire Teaching Hospitals NHS Foundation Trust, Royal Preston Hospital: Susan Baxter
London North West University Healthcare NHS Trust, Ealing Hospital: Malgorzata Adamus, Kevin Baynes
Maidstone and Tunbridge Wells NHS Trust, Maidstone Hospital: Siva Sivappriyan
Mid Yorkshire Hospitals NHS Trust, Pinderfields Hospital: Ryan D’Costa, Dinesh Nagi
North Bristol NHS Trust, Southmead Hospital: Vernon Parfitt
North West Anglia NHS Foundation Trust, Hinchingbrooke Hospital: Sadia Nasir
Oxford University Hospitals NHS Foundation Trust, John Radcliffe Hospital: Rustam Rea, Gail Roadknight, Kinga Várnai, Senthil Vasan
Pennine Acute Hospitals NHS Trust, Diabetes Centre, North Manchester General Hospital: Vilashini Arul Devah
Royal Berkshire NHS Foundation Trust (Berkshire Healthcare NHS Foundation Trust), Centre for Diabetes & Endocrinology: Foteini Kavvoura
Royal Devon and Exeter NHS Foundation Trust, Royal Devon and Exeter Hospital (Wonford): Lina Ficken, James Gilham, Vincent Simpson, Neil Walker
Royal Free London NHS Foundation Trust, Royal Free Hospital: Miranda Rosenthal, Efthimia Karra
Salford Royal NHS Foundation Trust, Salford Royal Hospital: Tracy Curran, Angela Paisley
Sandwell & West Birmingham NHS Trust, City Hospital, Birmingham: Melissa Cull, Parijat De P, Priscilla Sarker, Robert Ryder
Sheffield Teaching Hospitals NHS Foundation Trust, Northern General Hospital: Rajiv Gandi
Surrey & Sussex Healthcare NHS Trust, East Surrey Hospital: James Clark, Vesna Hogan, Lauren Jackson, Jamie-Leigh Williamson, Younes R Younes
The Newcastle Upon Tyne Hospitals NHS Foundation Trust, The Royal Victoria Infirmary: Lydia Grixti, Suann Tee
University Hospital of Derby and Burton NHS Foundation Trust, Royal Derby Hospital and Queen’s Hospital Burton: Abilash Sathya, Emma Wilmot
University Hospital Southampton NHS Foundation Trust, Diabetes at UHSNHSFT: Mayank Patel
University Hospitals Birmingham NHS Foundation Trust, Heartlands Hospital: Catherine Holmes
University Hospitals Birmingham NHS Foundation Trust, University Hospital of Birmingham: Wasim Hanif, Sandip Ghosh, Parth Narendran
University Hospitals of Leicester NHS Trust, Diabetes Research Centre, Leicester General Hospital: Ehtasham Ahmad, Ejaz Ahmed, Melanie Davies, Kamlesh Khunti, David Webb
University of Leicester: Ben Maylor
University of Oxford: Jim Davies, Oliver Freeman, Steve Harris, Yue Ruan
West Suffolk Hospital NHS Foundation Trust, West Suffolk Hospital: Anupam Brahma
Yeovil District Hospital NHS Foundation Trust, Yeovil District Hospital: Seshadri Pramodh
NHS Forth Valley, Forth Valley Royal Hospital: Katy Frew, Alison Mackenzie, Abigail Wild
NHS Greater Glasgow and Clyde, Queen Elizabeth University Hospital: Helen Casey, Deborah Morrison, Conor McKeag, Anne Sillars, Angus Stirling
Aneurin Bevan University Health Board, Nevill Hall Hospital: Fiona Smeeton
Aneurin Bevan University Health Board, Royal Gwent Hospital: Syed Muhammad, Kofi Obuobie, Win Yin
Cardiff & Vale University Health Board, University Hospital of Wales: Sai Ambati, Rahim Khan, Preethi Nalla, Arshiya Tabasum
Hywel Dda University Health Board, Glangwili General Hospital: Stamatios Zouras
Hywel Dda NHS Trust, Prince Philip Hospital: Akhila Mallipedhi
Swansea Bay University Health Board, Singleton Hospital: Richard Chudleigh, David Williams