Llauradó et al. Cardiovascular Diabetology https://doi.org/10.1186/s12933-022-01657-8 (2022) 21:216 Cardiovascular Diabetology RESEARCH Open Access The association between macrovascular complications and intensive care admission, invasive mechanical ventilation, and mortality in people with diabetes hospitalized for coronavirus disease‑2019 (COVID‑19) Gemma Llauradó1,2†, Bogdan Vlacho3,4†, Matthieu Wargny5,6†, Yue Ruan7,8†, Josep Franch‑Nadal2,3,9, Pere Domingo10, Pierre Gourdy11, Pierre‑Jean Saulnier12, Samy Hadjadj5, Sarah H. Wild13, Rustam Rea7,8, Bertrand Cariou5, Kamlesh Khunti14, Dídac Mauricio2,15*†for the CORONADO, the ABCD COVID-19 diabetes national audit, HM Hospitales investigators and the Hospital del Mar - Hospital de la Santa Creu i Sant Pau Diabetes Research Group Abstract Background: It is not clear whether pre-existing macrovascular complications (ischemic heart disease, stroke or peripheral artery disease) are associated with health outcomes in people with diabetes mellitus hospitalized for COVID-19. Methods: We conducted cohort studies of adults with pre-existing diabetes hospitalized for COVID-19 infection in the UK, France, and Spain during the early phase of the pandemic (between March 2020—October 2020). Logistic regression models adjusted for demographic factors and other comorbidities were used to determine associations between previous macrovascular disease and relevant clinical outcomes: mortality, intensive care unit (ICU) admission and use of invasive mechanical ventilation (IMV) during the hospitalization. Output from individual logistic regression models for each cohort was combined in a meta-analysis. Results: Complete data were available for 4,106 (60.4%) individuals. Of these, 1,652 (40.2%) had any prior macrovas‑ cular disease of whom 28.5% of patients died. Mortality was higher for people with compared to those without previ‑ ous macrovascular disease (37.7% vs 22.4%). The combined crude odds ratio (OR) for previous macrovascular disease and mortality for all four cohorts was 2.12 (95% CI 1.83–2.45 with an ­I2 of 60%, reduced after adjustments for age, sex, † Gemma Llauradó, Bogdan Vlacho, Matthieu Wargny and Yue Ruan first co- authors equally contributed to the work † Kamlesh Khunti and Dídac Mauricio last co-authors equally contributed to this work *Correspondence: didacmauricio@gmail.com 2 Department of Endocrinology and Nutrition, Center for Biomedical Research on Diabetes and Associated Metabolic Diseases (CIBERDEM), Instituto de Salud Carlos III (ISCIII), Barcelona, Spain Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 2 of 18 type of diabetes, hypertension, microvascular disease, ethnicity, and BMI to adjusted OR 1.53 [95% CI 1.29–1.81]) for the three cohorts. Further analysis revealed that ischemic heart disease and cerebrovascular disease were the main contributors of adverse outcomes. However, proportions of people admitted to ICU (adjOR 0.48 [95% CI 0.31–0.75], ­I2 60%) and the use of IMV during hospitalization (adjOR 0.52 [95% CI 0.40–0.68], I­2 37%) were significantly lower for people with previous macrovascular disease. Conclusions: This large multinational study of people with diabetes mellitus hospitalized for COVID-19 demonstrates that previous macrovascular disease is associated with higher mortality and lower proportions admitted to ICU and treated with IMV during hospitalization suggesting selective admission criteria. Our findings highlight the importance correctly assess the prognosis and intensive monitoring in this high-risk group of patients and emphasize the need to design specific public health programs aimed to prevent SARS-CoV-2 infection in this subgroup. Keywords: Diabetes, Macrovascular disease, Mortality, COVID-19 Background Our study aimed to assess whether the presence of Coronavirus disease 2019 (COVID-19) is caused by the macrovascular complications (ischemic heart disease, severe acute respiratory syndrome coronavirus 2 (SARS- stroke, or peripheral artery disease) prior to hospital CoV-2) and is characterized by a variable clinical pres- admission is associated with intensive care unit admis- entation that ranges from asymptomatic infection to sion, mechanical ventilation, and mortality in people fatal multi-organ damage and mortality [1, 2]. Since the with diabetes mellitus hospitalized for COVID-19 in emergence of SARS-CoV-2 in December 2019, cases four European cohorts. of COVID-19 have rapidly increased worldwide. The updated WHO estimates on August 19th, 2022, reported 590,659,276 confirmed cases, including 6,440,163 deaths Methods worldwide (https://​covid​19.​who.​int). The case fatality Study design and participants for COVID-19 has been estimated to be 0.5–1.0% [3, 4]. Retrospective data from hospitalized adults with pre- Nevertheless, certain characteristics, including increas- existing diabetes and concomitant COVID-19 infection ing age, male sex, ethnicity, socio-economic deprivation, were collected in the UK, France, and Spain. Adults and comorbidities, have been associated with a higher with hyperglycaemia at admission but not pre-existing risk of severe COVID-19 or death [5–7]. or subsequent diagnosis of diabetes (based on WHO COVID-19 pandemic has had a large negative impact criteria) were excluded from the analysis [16]. COVID- on both diabetes management [8] and diabetes-related 19 was defined as a SARS-CoV-2 infection confirmed mortality [9]. As well, pre-existing diabetes mellitus has by quantitative PCR (qPCR) performed on nasopharyn- been considered a risk factor for increased COVID-19 geal samples obtained by trained personnel and/or by severity and worse outcomes, including higher mortal- fulfilling clinical and radiological diagnostic criteria at ity, irrespective of age and comorbidity status [7]. The hospital admission. Further descriptions of each data- estimates of diabetes prevalence in those who have died set have been published previously [17]. of COVID-19 range from 20 to 30% [10, 11]. A recent meta-analysis showed that people with diabetes were at higher risk of COVID-19-related mortality in compari- United Kingdom: association of British clinical son to people without diabetes [11]. In addition, dia- diabetologists (ABCD) COVID‑19 audit betes is associated with more than double the risk for The NHS supports audits with clear guidance for the con- ICU admission and more than triple the risk of death tributing centers on using routine clinical practice data compared to people without diabetes [12]. Therefore, submitted anonymously via the secure NHS network [18]. identifying which clinical factors are associated with Clinicians participating in the ABCD COVID-19 audit sub- greater morbidity and mortality would be useful for mitted data for adults with pre-existing type 1 and type 2 the prevention and management of high-risk groups diabetes admitted with COVID-19 from hospitals across the during future waves of the pandemic. In that sense, few UK. The audit is registered with Oxford University Hospitals studies have examined the possibility that micro- and NHS Foundation Trust (OUH), a Data Protection Impact macrovascular complications contribute to susceptibil- Assessment was carried out and the audit was approved by ity to acute organ injury [13, 14] but with contradictory the OUH Caldicott Guardian and the Public Benefit and results [15]. Privacy Panel in Scotland (reference 2021-0111). Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 3 of 18 France: CORONADO (CORONAvirus‑SARS‑CoV‑2 of admission was collected with particular focus on those and diabetes outcomes) medications associated with diabetes or diabetes-related The CORONADO study described the phenotypic comorbidities. Microvascular disease (including retin- characteristics and prognosis of people with diabetes opathy, neuropathy, and nephropathy) was collected for admitted with COVID-19 between March 10 and April the UK, French and Spanish (Barcelona cohort) cohorts. 10, 2020 [13, 19]. CORONADO is a cohort study from The Spanish cohort (HM Hospitales) collected data French hospitals volunteering to share data on hospi- on the presence of chronic kidney disease (CKD) alone talized COVID-19 patients with diabetes. The study based on clinical coding records. CKD was defined by was sponsored by the Nantes University Hospital and eGFR < 60 ml/min or the presence of macroalbuminuria designed in accordance with the Declaration of Helsinki. (urinary albumin-to-creatinine ratio ≥ 300 mg/g) [21]. It obtained all regulatory approvals. Definition of macrovascular complications Spain—HM Hospitales cohort History of macrovascular disease was collected for all The six hospitals in the HM Hospitales group collected datasets. The presence of macrovascular complications anonymized observational data for people infected with was defined according to the presence of a previous his- COVID-19 during the first wave of the pandemics. This tory of ischemic heart disease (including a history of dataset is made available to researchers via “Covid Data myocardial infarction and/or coronary artery revascular- Save Lives” [20]. The electronic hospital health records ization or heart failure), cerebrovascular disease (includ- were collected for admitted persons, including pre- ing history of stroke or transient ischemic attack – TIA-) existing disease status, medication use, demographic, and/or peripheral artery disease (amputation owing to and outcome. A subset of people with pre-existing dia- ischemic disease and/or lower limb artery revasculari- betes from this cross-sectional database was used in this zation). Data were obtained based on the information study. Before access was granted, a formal petition, spe- recorded in medical records or according international cific study protocol, and ethics committee approval were ICD10 classification. Of the 6,795 people included, 4,106 obtained. The study was approved by the Ethics Com- had complete data for macrovascular complications (all mittee of the Primary Health Care University Research four cohorts) and/or the rest of the variables included Institute (IDIAP) Jordi Gol, Barcelona (approval number: (French, UK and Spanish HM Hospitales cohorts). 20/089-PCV). The flowchart of the study is summarized in Fig. 1. The descriptive analysis compared the characteristics of peo- Spain—Barcelona cohort ple with and without complete data for macrovascular An observational cohort study was conducted at the Hos- disease. The comparison of the clinical characteristics pital del Mar and Hospital de la Santa Creu i Sant Pau, of people with complete data compared with those with two tertiary hospitals in Barcelona providing healthcare missing data for macrovascular complications is shown to 800,000 people. The two hospitals from Barcelona in Table 1. (Catalonia) collected anonymized observational data for people infected with COVID-19 during the first wave. Outcomes Demographic, clinical, epidemiological, and whole- The primary outcome was all-cause mortality (French episode (laboratory workup, vital signs, treatment) data data were collected to day 28 after admission, and Span- were extracted from electronic medical records using a ish and UK data included mortality during the whole standardized data collection method. All patients with hospital episode). The secondary outcomes were inten- type 2 diabetes mellitus admitted for COVID-19 between sive care unit (ICU) admission for all four cohorts and March and April 2020 were included. The Hospital del use of invasive mechanical ventilation (IMV) during the Mar Institutional Ethics Committee (CEIm-2020/9352) hospitalization for the French and the Spanish HM Hos- and the Hospital de la Santa Creu I Sant Pau Ethics Com- pitales cohorts for which IMV data were available. mittee (HSCSP-20/117) approved the study and waived the informed consent need due to the study’s nature. Statistical analysis All quantitative data were tested for normality. Clini- Data collection: definitions and outcomes cal characteristics were expressed as the number Demographic data included: age, sex, and type of dia- (percentage) of participants for categorical variables, betes. UK and France collected ethnicity data (White/ mean ± standard deviation (SD) for normally distrib- Europid, Black/African, Asian/Asian, Other/Middle East uted continuous variables, or median (25–75th percen- and North African (MENA)). Medication use at the point tile) for non-normally distributed continuous variables. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 4 of 18 Assessed for eligibility Complete Data for Macrovascular complications (n=6,795) Excluded (n= 2,689) • Missing (n=2,689) Analysed sample (n= 4,160) No macrovascular Any macrovascular (n=2,454) (n=1,652) • Death (n=875) • Death (n=623) • ICU admission (n=509) • ICU admission (n=190) • Use of IMV (n=218) • Use of IMV (n=88) Fig. 1 Inclusion and exclusion criteria Regulatory issues prevented us from sharing and com- Results bining individual level data from each contributing The UK ABCD COVID-19 audit collected data on 3,179 country, so, multivariable logistic regression models people with diabetes from over 40 hospitals between were used to analyse the association between the pres- March and October 2020. Of these, 1,846 (58.1%) had ence of macrovascular disease (main exposure) and pri- complete data required for this study and were included mary (death) and secondary outcomes (ICU admission in the analysis. CORONADO investigators collected data and IMV) in each country’s data separately. Logistic on 2,843 people with diabetes from 68 hospitals, with regression models were then used to adjust for poten- 1,510 (53.1%) having complete data. Spanish investigators tial confounders: age and sex (model 1), age, sex, type from the HM Hospitales collected data on 2,310 indi- of diabetes, arterial hypertension, and the presence of viduals at six hospitals. There was complete data for 406 microvascular disease (model 2) and age, sex, type of individuals (100.0%) with pre-existing diabetes. Finally, diabetes, arterial hypertension, microvascular disease, the Spanish investigators from Hospital del Mar and ethnicity, and BMI (model 3–data not available for HM Hospital de la Santa Creu i Sant Pau collected data on cohort). Logistic regressions were performed using R in 367 individuals, with 344 (93.7%) having complete data. each contributing country; country-specific odds ratios A comparison of the complete dataset to that with miss- were then pooled in both common effect and random ing data within all the countries (Table 1). Ethnicity data effect meta-analysis (as needed according to I­2 statis- were not available for the Spain – HM Hospitales cohort. tic) and using the inverse variance method. Heteroge- The baseline characteristics of the cohort of patients in neity across studies was evaluated using the I­ 2 statistic. each country are summarized in Table 2. Data related to Results were expressed as odds ratio (OR) and 95% macrovascular disease status was available for 4,106 peo- confidence interval (95% CI) and p-values < 0.05 were ple. Of these, 1,652 (40.2%) had any prior macrovascular considered statistically significant. Statistical analyses disease, 1,339 (32.6%) had a previous history of ischemic were performed with R statistical software version 3.6.1 heart disease, 520 (12.7%) had previous cerebrovascular (https://​w ww.r-​proje​ct.​org/). disease, and 457 (11.1%) had previous peripheral artery disease. In the four included cohorts, people with a Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 5 of 18 Table 1 Comparison of the clinical characteristics of people with complete vs missing data for macrovascular complications UK FRANCE Spain—HM Spain—Barcelona Complete Missing Complete Missing Complete Missing Complete Missing data (n = 23) data data data data data data data (n = 1846) (n = 1333) (n = 1510) (n = 1333) (n = 406) (n = 0) (n = 344) Age (mean, SD) years 72.5 (13.9) 70.8 (14.4) 70.1 (13.0) 69.1 (13.3) 74.7 (11.9) – 71.1 (13.9) 74.0 (14.7) Missing, n 0 6 0 0 0 – 1 0 Men, n (%) 1140 (62) 802 (60) 933 (62) 882 (66) 250 (62) – 202 (59) 11 (48) Missing, n 0 5 0 0 0 – 0 0 BMI (mean, SD) kg/m2 29.3 (7.2) 28.6 (6.9) 29.9 (5.7) 28.9 (6.1) NA – 29.8 (6.6) 33.2 (5.8) Missing, n 0 860 0 124 NA – 295 21 Ethnicity – White, n (%) 1291 (70) 624 (60) 893 (59) 517 (56) NA – 77 (87) 18 (86) Asian, n (%) 275 (15) 167 (16) 55 (4) 33 (4) NA – 1 (1) 1 (5) Black, n (%) 116 (6) 94 (9) 242 (16.0) 179 (20) NA – 2 (2) 0 (0) Other, n (%) 164 (9) 157 (15) 320 (21) 187 (20) NA – 9 (10) 2 (10) Missing, n 0 291 0 417 NA – 255 2 Type of diabetes Type 1, n (%) 93 (5) 62 (5) 48 (3) 13 (1) 4 (1) – 5 (5) 0 (0.0) Type 2, n (%) 1753 (95) 1163 (95) 1462 (97) 1079 (99) 402 (99) 88 (95) 23 (100.0) Missing, n 0 108 0 241 0 – 251 0 Hypertension, n (%) 1286 (70) 774 (66) 1204 (80) 953 (73.0) 286 (70) – 278 (81) 18 (78) Missing, n 0 166 0 28 0 – 0 0 Dyslipidaemia, n (%) NA NA 767 (51) 521 (42) 198 (49) – NA NA Missing, n - - 0 81 0 – – – Microvascular disease, 807 (44) 242 (39) 701 (46) 206 (42) 38 (9) – 15 (17) 0 n (%) Missing, n 0 710 0 848 0 – 257 23 Macrovascular disease, 804 (44) 272 (40) 640 (42) 477 (39) 98 (24) – 110 (32) NA n (%) Missing, n 0 652 0 109 0 – 0 23 Death (in-hospital 715 (39) 524 (39) 290 (19) 294 (22) 79 (20) – 88 (28) 8 (36) mortality), n (%) Missing, n 0 0 0 7 0 – 18 1 ICU admission, n (%) 193 (10) 125 (13) 412 (27) 439 (33) 35 (9) – 59 (17) 1 (5) Missing, n 0 337 0 14 0 – 1 1 Use of IMV, n (%) NA NA 269 (18) 297 (23) 37 (9) – NA NA Missing, n - - 0 14 0 – – – BMI body mass index, ICU intensive care unit, IMV Mechanical ventilation, SD Standard deviation history of macrovascular disease were older, had a higher adjusting for age and sex (model 1: OR 1.39 [95% CI percentage of men and had a higher prevalence of hyper- 0.86–2.26]) (Fig. 2B) and age, sex, type of diabetes, arte- tension, dyslipidemia, and microvascular complications rial hypertension, and the presence of microvascular dis- than the group with no history of macrovascular disease. ease (model 2: OR 1.38 [95% CI 0.93–2.04]) (Fig. 2C). The In total, 1,172 (28.5%, range 19.2–39.0%) people died. final model and additional adjustment for ethnicity and Mortality was higher for people with compared to with- BMI (in a subset including 3 of the 4 cohorts) showed out previous macrovascular disease (37.7% vs 22.4%). The similar results (OR 1.53 [95% CI 1.29–1.81]) (Fig. 2D). combined crude odds ratio (OR) for previous macrovas- Further, each component of macrovascular complications cular disease and mortality was 2.12 (95% CI 1.83–2.45) was analysed separately, to know which of the 3 diseases (Fig. 2A), with moderate heterogeneity (­I2 60%). In the contributed the most. Both ischemic heart disease (unad- multivariable analyses, the results were attenuated after justed OR 1.78 [95% CI 1.20–2.63]), cerebrovascular Table 2 Clinical characteristics of subjects according to macrovascular status UK FRANCE Spain—HM Spain—Barcelona All No MACRO Any P All (n = 1510) No Any MACRO P All (n = 406) No Any MACRO P All No Any p (n = 1846) (n = 1042) MACRO MACRO (n = 640) MACRO (n = 98) (n = 344) MACRO MACRO (n = 804) (n = 870) (n = 308) (n = 234) (n = 110) Age (mean, 72.5(13.9) 69.1(14.8) 76.8(11.2) < 0.001 70.1(13.0) 66.7(13.0) 74.7(11.5) < 0.001 74.7(11.9) 72.8(11.9) 80.6(9.7) < 0.001 71.1(13.9) 69.3(13.9) 74.8(13.0) < 0.001 SD) years Men, n (%) 1140(62) 610 (59) 530 (66) 0.001 933 (62) 495(57) 438 (68.4) < 0.001 250(62) 185(60) 65(66) 0.322 202 (58.9) 129 (55.1) 73 (67.0) 0.038 Ethnicity, < 0.001 < 0.001 NA 0.688 n (%) Llauradó et al. Cardiovascular Diabetology White 1291(70) 655(63) 626(78) 893(59) 467(54) 426(66.6) NA NA NA 77(87) 58(84) 19(95) Asian 275(15) 200(19) 75 (9) 55(4) 39(5) 16(2.5) NA NA NA 1 (1) 1 (2) 0 (0) Black 116(6) 64(6) 52 (6) 242(16) 173(20) 69(10.8) NA NA NA 2 (2) 2 (3) 0 (0) Other 164(9) 123(12) 41 (5) 320(21) 191(22) 129(20.2) NA NA NA 9 (10) 8 (12) 1 (5) Type of diabetes (2022) 21:216 Type 1, n 93(5) 59(6) 34(4) 0.200 48(3) 33(4) 15(2.3) 0.107 4 (1) 3 (1) 1 (1) 1.000 5 (5) 5 (7) 0 (0.0) 0.642 (%) Type 2, n 1753(95) 983(94) 770(96) 1462(97) 837(96) 625(97.7) 402(99) 305(99) 97(99) 88 (95) 68 (93) 20(100.0) (%) Oral 1123(61) 673(65) 450(56) < 0.001 1092(72) 684(79) 408(64) < 0.001 83 (20) 68 (22) 15(15) 0.192 274 (80) 189 (81) 85 (78) 0.452 agents, n (%) Insulin,n (%) 696(38) 402(39) 294(37) 0.40 678(44.9) 320(36.8) 358(56) < 0.001 79 (20) 61 (20) 18 (18) 0.868 97 (28) 55 (24) 42 (39) 0.004 Hyper‑ 1286(70) 713(68) 573(71) 1204(80) 635(73) 569(88.9) < 0.001 286(70) 207(67) 79(81) 0.016 278(81) 176(75) 102(93) < 0.001 tension, n (%) RAASi, n 1319(71) 715(69) 604(75) 0.003 858(56.9) 446(51.3) 412(64.5) < 0.001 153 (38) 115 (37) 38 (39) 0.892 199 (58) 131 (56) 68 (62) 0.194 (%) Dyslipi‑ NA NA NA NA 767(51) 363(42) 404(63.1) < 0.001 198(49) 141(46) 57(58) 0.043 NA NA NA NA daemia, n (%) Statins, n 1158(63) 625(60) 533(66) 0.006 764(50.6) 353(40.6) 411(64.3) < 0.001 107 (26) 60 820) 47 (48) < 0.001 193 (56) 112 (48) 81 (74) < 0.001 (%) BMI 29.3 (7.2) 29.9 (7.2) 28.6 (7.1) < 0.001 29.5 (5.9) 29.9 (5.7) 28.9 (6.1) 0.02 NA NA NA NA 29.8 (6.7) 29.3 (6.4) 33.3 (8.1) 0.176 Diabetes NA NA NA NA 12 [6; 20] 10 [5; 18] 15 [10; 23] < 0.001 NA NA NA NA NA NA NA NA duration HbA1c 7.8 (4.2) 7.9 (4.3) 7.8 (4.1) 0.270 8.1 (1.8) 8.3 (2.0) 7.9 (1.7) < 0.001 8.1 (1.7) 8.3 (1.8) 7.7 (1.4) 0.230 7.5 (1.5) 7.3 (1.4) 8.3 (1.8) 0.022 (%), mean (SD) Page 6 of 18 Table 2 (continued) UK FRANCE Spain—HM Spain—Barcelona All No MACRO Any P All (n = 1510) No Any MACRO P All (n = 406) No Any MACRO P All No Any p (n = 1846) (n = 1042) MACRO MACRO (n = 640) MACRO (n = 98) (n = 344) MACRO MACRO (n = 804) (n = 870) (n = 308) (n = 234) (n = 110) HbA1c 62 (22) 63 (23) 62 (21) 0.270 65.2(20.2) 67.1(21.5) 62.7(18.2) < 0.001 65.0(18.2) 67.2(20.2) 60.7(15.4) 0.230 58.9(16.9) 56.6(15.4) 67.2(19.7) 0.022 mmol/ mol, mean (SD) Microvascu‑ Llauradó et al. Cardiovascular Diabetology lar disease, n (%) Diabetic 449(24) 216(22) 233(30) < 0.001 252(17) 104(12) 148(23) < 0.001 1(0.2) 1(0.3) 0(0.0) 1.000 8/87 (9) 7/71 (10) 1/16 (6) 0.652 retin‑ opathy, n (%) (2022) 21:216 Diabetic 420(23) 156(15) 264(33) < 0.001 569 (38) 220(25) 349(54.5) < 0.001 31(7.6) 12(4) 19(19) < 0.001 6/87 (7) 5/71 (7) 1/16 (6) 0.910 kidney disease, n (%) Macrovascu‑ lar disease, n (%) Ischemic 560(30) 0 (0.0) 560(70) – 410(27)/185(13) 0(0) 410(64)/185(39) – 54(13.3)/34(8.4) 0 (0.0) 54(55)/34(35) – 96 (28) 0 (0.0) 96 (88) – heart disease/ Heart failure, n (%) TIA/ 295(16) 0 (0.0) 295(37) – 188(13) 0(0) 188(29.4) – 25 (6.2) 0 (0.0) 25(26) – 12 (3.5) 0 (0.0) 12 (11) – Stroke, n (%) Periph‑ 246(13) 0 (0.0) 246(31) – 198(13) 0(0) 198(31.0) – 10 (2.5) 0 (0.0) 10(10) – 3 (1) 0 (0.0) 3 (2.7) – eral artery disease, n (%) CKD, n NA NA NA NA NA NA NA NA 51 (12.6) 22(7) 29(30) < 0.001 NA NA NA NA (%) Death 715(39) 326(31) 389(48) < 0.001 290(19) 118(14) 172(26.9) < 0.001 79(19.5) 59(19) 20(20) 0.900 88(25.6) 46(19.7) 42(38.3) < 0.001 (in- hospital mortal‑ ity), n (%) Page 7 of 18 Llauradó et al. Cardiovascular Diabetology Table 2 (continued) (2022) 21:216 UK FRANCE Spain—HM Spain—Barcelona All No MACRO Any P All (n = 1510) No Any MACRO P All (n = 406) No Any MACRO P All No Any p (n = 1846) (n = 1042) MACRO MACRO (n = 640) MACRO (n = 98) (n = 344) MACRO MACRO (n = 804) (n = 870) (n = 308) (n = 234) (n = 110) ICU 193(10) 155(15) 38(5) < 0.001 412(27) 282(32) 130(20.3) < 0.001 35(8.6) 28(9) 7 (7) 0.695 59(17.2) 44(18.8) 15(13.6) 0.249 admis‑ sion, n (%) Use of NA NA NA NA 269 (18) 189(22) 80 (12.5) < 0.001 37 (9.1) 29 (9) 8 (8) 0.862 NA NA NA NA IMV, n (%) BMI body mass index, CKD chronic kidney disease, ICU intensive care unit, IMV Mechanical ventilation, SD Standard deviation, Page 8 of 18 Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 9 of 18 Fig. 2 Odds ratio for the association between mortality and the presence of previous macrovascular disease in each of the four cohorts and overall (A). ­I2 indicates heterogeneity in the estimates. Odds ratio estimates adjusted for: model 1: age and sex (B); model 2: model 1 + type of diabetes, arterial hypertension, and the presence of microvascular disease (C); model 3: model 2 + ethnicity and BMI (D). HM cohort is excluded from model 3 due to lack of ethnicity data disease (unadjusted OR 1.91 [95% CI 1.57–2.34]) and (Additional file 1: Fig. S1, Additional file 2: Fig. S2, Addi- peripheral artery disease (unadjusted OR 1.70 [95% CI tional file 3: Fig. S3). The results were maintained sig- 2.38–2.10]) were associated with higher mortality (Addi- nificant after further adjustments in all cases (Additional tional file 1: Fig. S1, Additional file 2: Fig. S2, Additional file 1: Fig. S1, Additional file 2: Fig. S2, Additional file 3: file 3: Fig. S3). The results were maintained significant Fig. S3). Finally, the overall odds ratio (OR) for previous after further adjustments except for peripheral artery dis- macrovascular disease and use of IMV during hospi- ease (Additional file 1: Fig. S1, Additional file 2: Fig. S2, talization was 0.52 (95% CI 0.40–0.68) in the unadjusted Additional file 3: Fig. S3). analyses (Fig. 4A), with little evidence of heterogeneity (­ I2 Regarding the secondary outcomes, 699 people (15.7%, 37%). In the multivariable analyses, the results were simi- range 8.6–22.3%) were admitted to ICU, and 306 (13.6%, lar after adjusting for age and sex (model 1: OR 0.63 [95% range 9.1–17.8%) required IMV during hospitalization. CI 0.47–0.85]) (Fig. 4B) and age, sex, type of diabetes, The proportions admitted to ICU or treated with IMV arterial hypertension, and the presence of microvascular during hospitalization were lower for those patients with disease (model 2: OR 0.61 [95% CI 0.45–0.83]) (Fig. 4C). previous macrovascular disease (11.5% vs 20.7% and Ischemic heart disease (unadjusted OR 0.55 [95% CI 11.9% vs 18.5%, respectively). The overall odds ratio (OR) 0.43–0.71]) was associated with lower mortality (Addi- for previous macrovascular disease and ICU admission tional file 1: Fig. S1, Additional file 2: Fig. S2, Additional was 0.48 (95% CI 0.31–0.75) in the unadjusted analyses file 3: Fig. S3). The results were maintained significant (Fig. 3A), with moderate heterogeneity (­I2 68%). In the after further adjustments in all cases (Additional file 1: multivariable analyses, the estimates were similar after Fig. S1, Additional file 2: Fig. S2, Additional file 3: Fig. adjusting for age and sex (model 1: OR 0.61 [95% CI S3). The association between cerebrovascular disease and 0.49–0.77]) (Fig. 3B); age, sex, type of diabetes, arterial peripheral artery disease and use of IMV during hospital- hypertension, and the presence of microvascular disease ization was not tested for insufficient number of events. (model 2: OR 0.58 [95% CI 0.47–0.72]) (Fig. 3C); and age, sex, type of diabetes, arterial hypertension, microvascu- Discussion lar disease, ethnicity, and BMI (model 3: OR 0.57 [95% This is the first European retrospective study to specifi- CI 0.44–0.74]) (Fig. 3D). Both ischemic heart disease cally investigate the association between previous mac- (unadjusted OR 0.53 [95% CI 0.44–0.64]), cerebrovas- rovascular disease and severe outcomes of people with cular disease (unadjusted OR 0.32 [95% CI 0.12–0.84]) diabetes mellitus hospitalized for COVID-19. The pre- and peripheral artery disease (unadjusted OR 0.48 [95% sent study demonstrates that the presence of macro- CI 0.34—0.66]) were associated with lower mortality vascular complications (ischemic heart disease, stroke, Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 10 of 18 Fig. 3 Odds ratio for the association between intensive care unit admission and the presence of previous macrovascular disease in each of the four cohorts and overall (A). ­I2 indicates heterogeneity in the estimates. Odds ratio estimates adjusted for: model 1: age and sex (B); model 2: model 1 + type of diabetes, arterial hypertension, and the presence of microvascular disease (C); model 3: model 2 + ethnicity and BMI (D). HM cohort is excluded from model 3 due to lack of ethnicity data Fig. 4 Odds ratio for the association between use of invasive mechanical ventilation during the hospitalization and the presence previous of macrovascular disease in each of the two cohorts and overall (A). ­I2 indicates heterogeneity in the estimates. Odds ratio estimates adjusted for: model 1: age and sex (B); model 2: model 1 + type of diabetes, arterial hypertension, and the presence of microvascular disease (C) peripheral artery disease) was associated with higher deprivation, and other comorbidities such as obesity, mortality. These findings remain significant after further hypertension and cardiovascular disease contribute to adjustments for age, sex, type of diabetes, arterial hyper- the increased risk [23]. The underlying mechanisms tension, microvascular disease, ethnicity, and BMI. How- resulting in adverse outcomes in subjects with diabe- ever, the proportions admitted to ICU and treated with tes hospitalized for COVID-19 are therefore complex IMV during hospitalization were lower for patients with and unknown. In that sense, it has been suggested that previous macrovascular disease, reflecting clinical deci- both impaired glucose regulation and hyperglycemia sions around ICU admission. [24] and the visceral adipose tissue expansion (and its COVID-19 is known to be associated with poorer associated ectopic fat depots) that characterize patients outcomes for those with long-term conditions such with diabetes and/or obesity activate the inflammatory as diabetes, and several potential mechanisms have cascade, increasing the production of interleukin-6, been proposed [22]. Moreover, age, sex, ethnicity, which has been proposed as a determinant factor of Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 11 of 18 the “cytokine storm” associated with severe forms of mortality compared to people with no history of mac- COVID-19 [25]. rovascular disease after adjusting for all available con- A recent meta-analysis, including 158 observational founding factors and that ischemic heart disease and studies with a total of 270,212 participants, of whom stroke are the main contributors to this higher risk. 57,801 had diabetes, reported that people with diabe- However, proportions admitted to ICU or treated with tes were at higher risk of COVID-19-related mortality IMV during hospitalization were lower for people with with an OR 1.87 (95% CI 1.61–2.17) and higher risk of previous macrovascular disease. These results suggest ICU admission (1.59 [95% CI 1.15–2.18]) and ventilation unmeasured differences that may explain these oppos- requirements (1.44 [95% CI 1.20–1.73]) in comparison to ing relationships, such as (1) the severity of the disease, subjects without diabetes [11]. In addition, cardiovascu- (2) early mortality leading to potentially fewer patients lar disease is common comorbidity observed in patients admitted to ICU or meeting intubation criteria in the with COVID-19, associated with increased severity and group of people with macrovascular disease or (3) the mortality [22]. In that sense, it has been reported that criteria used for ICU admission or IMV. In addition, it patients with COVID-19 who have either hypertension should be emphasized that our analysis revealed mod- or cardiovascular disease have an approximately 3–four- erate heterogeneity in mortality and ICU admission for fold higher risk of developing severe disease [26]. By con- people with diabetes and previous cardiovascular dis- trast, recent observational studies have demonstrated a ease with differences in the strength of the relationship significant association between statins (with anti-inflam- between cohorts. While the higher mortality among matory and vasculo-protective effects) and reduced mor- people with history of macrovascular disease was con- tality in patients hospitalized with COVID-19, especially sistently higher across the four cohorts, there were those with diabetes [27]. more marked differences regarding ICU admission and Moreover, an adverse effect on outcomes of diabetic the use of IMV, being lower compared to the Spanish complications in patients with diabetes during the cohorts in the UK (ICU admission) and French cohorts COVID-19 pandemic has been recently identified. In a (both ICU admission and use of IMV). national population-based study in Scotland, associa- Our study is limited by the heterogeneity of data collec- tions with fatal or critical care unit treated COVID-19 tion methods across the nations due to the use of data- among people with diabetes adjusted for age, sex, dia- bases that were designed separately and not specifically betes duration, and type of diabetes were reported for to answer the study question and, also by missing data. 35 factors, including heart disease (OR 2.43 [95% CI The meta-analysis combines the individual datasets to 2.14–2.75]), history of hospital admission with diabetic increase power but masks heterogeneity across nations. ketoacidosis (OR 2.87 [95% CI 1.85–4.46]), microalbu- The relatively large proportion of people with miss- minuria (OR 1.35 [95% CI 1.16–1.58]), macroalbuminu- ing data on one or more variables in the UK and French ria 1.92 [95% CI 1.52–2.43]) and severe retinopathy (OR cohorts has occurred as a consequence of using routinely 1.92 [95% CI 1.52–2.43]) [28]. The CORONADO study collected data from clinical practice and could intro- found that both microvascular (OR 2.14 [95% CI:1.16– duce bias if data are not missing at random. As shown in 3.94]) and macrovascular (OR 2.54 [95% CI: 1.44–4.50]) Table 1, summary measures of the distribution of most complications were independently associated with the variables used in model 3 (age, sex, type of diabetes, arte- risk of death on day seven of admission after adjusting rial hypertension, BMI, microvascular disease, macro- for age, sex, comorbidities/complications, and glucose- vascular disease, death and ICU admission) were similar lowering and anti-hypertensive treatment [13, 14, 19]. or had only modest differences between people with and By contrast, no association was found between mor- without missing data in both UK and French cohorts. tality (death by day seven of admission) and micro- or People of non-white ethnicity were over-represented in macrovascular complications in the ACCREDIT Study the missing data group in the UK cohort but not in the [15]. Nevertheless, both cohorts differ in several aspects French cohort. Clinical data of the whole-episode, such such as mean age (69.8 in the CORONADO study vs. as vital signs or arterial gasometry parameters, clinical 74.1 for the ACCREDIT study cohort), median BMI severity scores (i.e. MEWS or CURB-65 score) or mark- (28.4 kg/m2 vs. 27.6 kg/m2), the mean HbA1c (8.1% vs. ers of inflammation (PCR, IL-6, serum ferritin) were not 7.7%), which may partially explain the different results collected, as well as other potential confounding factors. regarding the outcomes [13–15, 19]. Our analysis sug- In addition, the small sample size of patients with type gests that participants living with diabetes hospitalized 1 diabetes included made it impossible to analyze both for COVID-19 with previous macrovascular complica- groups separately to evaluate the potential differences tions (ischemic heart disease, stroke, peripheral artery between both. Lastly, we focused on people hospitalized disease) have an approximately 50% higher risk of for COVID-19; thus, our results cannot be generalized to Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 12 of 18 all people with diabetes and COVID-19, especially those Acknowledgements The contributors to national studies are listed below. with less severe forms of the disease. List of Contributors of the Spanish research group: Juan Antonio Arroyo: Department of Internal Medicine, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain; Juan-José Chillarón: Department of Endocrinology and Nutrition, Hospital del Mar; Institut Hospital del Mar Conclusions d’Investigacions Mèdiques (IMIM), Barcelona, Spain; Rosa Corcoy: Department In conclusion, this large multinational study of peo- of Endocrinology and Nutrition, Hospital de la Santa Creu i Sant Pau; Depart‑ ple with diabetes mellitus hospitalized for COVID-19 ment of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain; CIBER of Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN), Instituto demonstrates significant associations between previous de Salud Carlos III (ISCIII), Spain; Roberto Güerri: Department of Infectious macrovascular disease and higher mortality and with Diseases, Hospital del Mar; Institut Hospital del Mar d’Investigacions Mèdiques lower ICU admission and the use of IMV during hospi- (IMIM), Barcelona, Spain; Manel Mata-Cases: Primary Health Care Center La Mina, Gerència d’Àmbit d’Atenció Primària Barcelona Ciutat, Institut Català talization. This study is the first specifically designed to de la Salut, Sant Adrià de Besòs, Spain. Emilio Ortega: CIBER of physiopathol‑ evaluate the association of macrovascular complications ogy of Obesity and Nutrition (CIBEROBN), Instituto de Salud Carlos III (ISCIII), (ischemic heart disease, stroke, or peripheral artery dis- Spain; Department of Endocrinology and Nutrition, Institut d’Investigacions Biomèdiques August Pi i Suñer, Hospital Clinic, Barcelona, Spain. ease) as main exposure with mortality, intensive care List of Contributors for the CORONADO study: unit admission and mechanical ventilation in people For CORONADO study, we thank the sponsor (DRCI, Nantes University with diabetes mellitus hospitalized for COVID-19 in Hospital), translational project manager (Matthieu Pichelin), Clinical Project Manager (Maëva Saignes) and assistant (Jeanne Saunier), Clinical Research Europe. Our findings highlight the importance correctly Associates (Selma El Andaloussi, Joëlle Martin-Gauthier, Emily Rebouilleau) assess the prognosis and intensive monitoring in this and data manager (Tanguy Roman). We also thank the Société Francophone high-risk group of patients and emphasize the need to du Diabète (SFD) and Société Française d’Endocrinologie (SFE) for disseminat‑ ing CORONADO study design and organization, the Fédération Française des design specific public health programs aimed to prevent Diabétiques (FFD) for participating in the organization of the study. We are SARS-CoV-2 infection in this subgroup (i.e. reinforcing grateful to all the people who collected the data for this study. vaccination campaigns). Nevertheless, further studies are List of Contributors for CORONADO study: Bertrand CARIOU, CHU de Nantes, Nantes, bertrand.cariou@univ-nantes.fr. required to confirm and extend these findings in these Samy HADJADJ, CHU de Nantes, Nantes, samy.hadjadj@univ-nantes.fr. and other populations. Matthieu WARGNY, CHU de Nantes, Nantes, matthieu.wargny@chu-nantes.fr. Pascale MAHOT, CHU de Nantes, Nantes, pascale.moreau@chu-nantes.fr. Matthieu PICHELIN, CHU de Nantes, Nantes, matthieu.pichelin@univ-nantes.fr. Abbreviations Anne-Laure FOURNIER-GUILLOUX, CHU de Nantes, Nantes, annelaure.fournier‑ CKD: Chronic kidney disease; COVID-19: Coronavirus disease 2019; ICU: guilloux@chu-nantes.fr. Intensive care unit; IMV: Invasive mechanical ventilation; OR: Odds ratio; Nicolas MAUDUIT, CHU de Nantes, Nantes, nicolas.mauduit@chu-nantes.fr. SARS-CoV-2: Severe acute respiratory syndrome coronavirus 2; SD: Standard Edith BIGOT- CORBEL, CHU de Nantes, Nantes, edith.bigot@chu-nantes.fr. deviation; 95% CI: 95% Confidence interval. Anne-Sophie BOUREAU, CHU de Nantes, Nantes, annesophie.boureau@chu- nantes.fr. Laure DE DEKCER, CHU de Nantes, Nantes, laure.dedecker@chu-nantes.fr. Supplementary Information Audrey ERNOULD, CHU de Nantes, Nantes, audrey.ernould@chu-nantes.fr. The online version contains supplementary material available at https://​doi.​ Claire PRIMOT, CHU de Nantes, Nantes, claire.primot@chu-nantes.fr. org/​10.​1186/​s12933-​022-​01657-8. Anne SEGUIN, CHU de Nantes, Nantes, anne.seguin@chu-nantes.fr. Marielle JOLIVEAU, CHU de Nantes, Nantes, marielle.joliveau@chu-nantes.fr. Sonia POUVREAU, CHU de Nantes, Nantes, sonia.pouvreau@chu-nantes.fr. Additional file 1: Figure S1. Odds ratio for the association between Chloé FOURNIER, CHU de Nantes, Nantes, chloe.fournier@chu-nantes.fr. mortality (1A–C), intensive care unit admission (2A–C) and use of invasive Jeremy THUREAU, CHU de Nantes, Nantes, jeremy.thureau@chu-nantes.fr. mechanical ventilation during the hospitalization (3A–C) and ischemic Edith FONTENEAU, CHU de Nantes, Nantes, edith.fonteneau@chu-nantes.fr. heart disease in each of the four cohorts and overall. I­2 indicates heteroge‑ Pamela HUBLAIN, CHU de Nantes, Nantes, Pamela.HUBLAIN@chu-nantes.fr. neity in the estimates. Odds ratio estimates adjusted for: model 1: age and Carole AGASSE, CHU de Nantes, Nantes, Carole.AGASSE@chu-nantes.fr. sex (B); model 2: model 1 + type of diabetes, arterial hypertension, and the Mathilde DE KERGARADEC, CHU de Nantes, Nantes, laurence.dekergaradec@ presence of microvascular disease (C). chu-nantes.fr. Additional file 2: Figure S2. Odds ratio for the association between Vincent MINVILLE, CHU Toulouse, Toulouse, minville.v@chu-toulouse.fr. mortality (1A–C), intensive care unit admission (2A–C) and and stroke in Fanny VARDON-BOUNES, CHU Toulouse, Toulouse, bounes.f@chu-toulouse.fr. each of the four cohorts and overall. I­2 indicates heterogeneity in the esti‑ Guillaume MARTIN-BLONDEL, CHU Toulouse, Toulouse, martin-blondel.g@ mates. Odds ratio estimates adjusted for: model 1: age and sex (B); model chu-toulouse.fr. 2: model 1 + type of diabetes, arterial hypertension, and the presence of Pierre GOURDY, CHU Toulouse, Toulouse, pierre.gourdy@inserm.fr. microvascular disease (C). Blandine TRAMUNT, CHU Toulouse, Toulouse, blandine.tramunt@orange.fr. Marie-Christine TURNIN, CHU Toulouse, Toulouse, turnin.mc@chu-toulouse.fr. Additional file 3: Figure S3. Odds ratio for the association between mor‑ Hélène HANAIRE, CHU Toulouse, Toulouse, hanaire.h@chu-toulouse.fr. tality (1A–C), intensive care unit admission (2A–C) and peripheral artery Jean-Michel MANSUY, CHU Toulouse, Toulouse, mansuy.jm@chu-toulouse.fr. disease in each of the four cohorts and overall. I­2 indicates heterogeneity Didier FABRE, CHU Toulouse, Toulouse, fabre.d@chu-toulouse.fr. in the estimates. Odds ratio estimates adjusted for: model 1: age and sex Marie-Blanche ARHAINX, CHU Toulouse, Toulouse, arhainx.mb@chu-toulouse. (B); model 2: model 1 + type of diabetes, arterial hypertension, and the fr. presence of microvascular disease (C). Laurent CAZALS, CHU Toulouse, Toulouse, cazals.l@chu-toulouse.fr. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 13 of 18 Laure COMBES, CHU Toulouse, Toulouse, combes.l@chu-toulouse.fr. Blandine RAMMAERT, CHU Poitiers, Poitiers, blandine.rammaert@chu-poitiers. Emmanuelle LAMI, CHU Toulouse, Toulouse, lami.e@chu-toulouse.fr. fr. Mallory CIANFERANI, CHU Toulouse, Toulouse, cianferani.m@chu-toulouse.fr. Pierre Jean SAULNIER, CHU Poitiers, Poitiers, pierrejean.saulnier@gmail.com. Bruno MEGARBANE, Hôpital LARIBOISIERE, Paris, bruno.megarbane@aphp.fr. Xavier PIGUEL, CHU Poitiers, Poitiers, xavier.piguel@chu-poitiers.fr. Pierre LEROY, Hôpital LARIBOISIERE, Paris, pierre.leroy@aphp.fr. Nesrine BENHENDA, CHU Poitiers, Poitiers, Nesrine.BENHENDA@chu-poitiers.fr. Jean-François GAUTIER, Hôpital LARIBOISIERE, Paris, jean-francois.gautier@ Camille HUSSON, CHU Poitiers, Poitiers, Camille.HUSSON@chu-poitiers.fr. aphp.fr. Celine OLIVIER, CHU Poitiers, Poitiers, celine.olivier@chu-poitiers.fr. Tiphaine VIDAL-TRECAN, Hôpital LARIBOISIERE, Paris, tiphaine.vidal-trecan@ Florence TORREMOCHA, CHU Poitiers, Poitiers, florence.torremocha@chu- aphp.fr. poitiers.fr. Jean-Pierre RIVELINE, Hôpital LARIBOISIERE, Paris, jeanpierre.riveline@aphp.fr. Mathilde FRATY, CHU Poitiers, Poitiers, mathilde.fraty@chu-poitiers.fr. Jean-Louis LAPLANCHE, Hôpital LARIBOISIERE, Paris, jean-louis.laplanche@ Marie FLAMEN D’ASSIGNY, CHU Poitiers, Poitiers, marie.flamen-dassigny@ aphp.fr. chu-poitiers.fr. Stéphane MOULY, Hôpital LARIBOISIERE, Paris, stephane.mouly@aphp.fr. Aurelie MIOT, CHU Poitiers, Poitiers, aurelie.miot@chu-poitiers.fr. Louis POTIER, Hôpital BICHAT, Paris, louis.potier@gmail.com. Valentin BOSSARD, CHU Poitiers, Poitiers, valentin.bossard988@gmail.com. Ronan ROUSSEL, Hôpital BICHAT, Paris, ronan.roussel@aphp.fr. Kada KLOUCHE, Hôpital Lapeyronie, Chu Montpellier, k-klouche@chu-mont‑ Malak TAHER, Hôpital BICHAT, Paris, malak.taher@aphp.fr. pellier.fr. Yawa ABOULEKA, Hôpital BICHAT, Paris, yawa.abouleka@aphp.fr. Alain MAKINSON, Hôpital Lapeyronie, Chu Montpellier, a-makinson@chu- Fetta YAKER, Hôpital BICHAT, Paris, fettaamel.yaker@aphp.fr. montpellier.fr. Aurelie CARLIER, Hôpital BICHAT, Paris, aurelie.carlier@aphp.fr. Ariane SULTAN, Hôpital Lapeyronie, Chu Montpellier, a-sultan@chu-montpel‑ Anne BOUTTEN, Hôpital BICHAT, Paris, anne.boutten@aphp.fr. lier.fr. Marilyne HALLOT-FERON, Hôpital BICHAT, Paris, marilyne.feron@aphp.fr. Jean-Baptiste BONNET, Hôpital Lapeyronie, Chu Montpellier, jean-baptiste- Fadila MOURAH, Hôpital BICHAT, Paris, fadila.mourah@gmail.com. bonnet@chu-montpellier.fr. Charles THIVOLET, Hôpital Lyon Sud, Pierre Bénite, charles.thivolet@chu-lyon.fr. Vincent FOULONGNE, Hôpital St Eloi, Chu Montpellier, v-foulongne@chu- Emilie BLOND, Hôpital Lyon Sud, Pierre Bénite, emilie.blond@chu-lyon.fr. montpellier.fr. Muriel ROLLAND, Hôpital Lyon Sud, Pierre Bénite, muriel.rolland@chu-lyon.fr. Florence GALTIER, Hôpital St Eloi, Chu Montpellier, f-galtier@chu-montpellier.fr. Josep VERDECHO MENDEZ, Hôpital Lyon Sud, Pierre Bénite, josep.verdecho- Cécile AUBRON, CHU de Brest, Brest, cecile.aubron@ch-brest.fr. mendez@chu-lyon.fr. Séverine ANSART, CHU de Brest, Brest, severine.ansart@chu-brest.fr. Marine ALEXANDRE, Hôpital Lyon Sud, Pierre Bénite, marine.alexandre@chu- Véronique KERLAN, CHU de Brest, Brest, veronique.kerlan@chu-brest.fr. lyon.fr. Pascale QUINIOU, CHU de Brest, Brest, pascale.quiniou@chu-brest;fr. Julien POTTECHER, Nouvel hôpital civil, Strasbourg, julien.pottecher@ Jean- Luc CARRE, CHU de Brest, Brest, jean-luc.carre@chu-brest.fr. chru-strasbourg,fr. Stéphane QUESNOT, CHU de Brest, Brest, stephane.quesnot@chu-brest.fr. Emilie RICHER, Nouvel hôpital civil, Strasbourg, emilie.richerdupont@chru- Bruno LAVIOLLE, CHU de Rennes, Rennes, bruno.laviolle@chu-rennes.fr. strasbourg.fr. Carole SCHWEBEL, CHU Grenoble Alpes, Grenoble, Cschwebel@chu-grenoble. Laurent MEYER, Nouvel hôpital civil, Strasbourg, laurent.meyer@chru-stras‑ fr. bourg.fr. Olivier EPAULARD, CHU Grenoble Alpes, Grenoble, OEpaulard@chu-grenoble.fr. Florina LUCA, Hôpital Hautepierre, Strasbourg, florina.luca@chru-strasbourg,fr. Pierre-Yves BENHAMOU, CHU Grenoble Alpes, Grenoble, PYBenhamou@chu- Jean-Marc LESSINGER, Nouvel hôpital civil, Strasbourg, Jean-Marc.LESSINGER@ grenoble.fr. chru-strasbourg.fr. Cécile BETRY, CHU Grenoble Alpes, Grenoble, Cbetry@chu-grenoble.fr. Thibault BAHOUGNE, Hospices civils, Strasbourg, thibault.bahougne@ Anne-Laure BOREL, CHU Grenoble Alpes, Grenoble, ALBorel@chu-grenoble.fr. chru-strasbourg,fr. Sandrine LABLANCHE, CHU Grenoble Alpes, Grenoble, Slablanche@chu- Bruno GUERCI, CHU Brabois Université de Lorraine, Nancy, b.guerci@chru- grenoble.fr. nancy.fr. Dorra GUERGOUR, CHU Grenoble Alpes, Grenoble, Dguergour@chu-grenoble. Lisa LUDWIG, CHU Brabois Université de Lorraine, Nancy, L.LUDWIG@chru- fr. nancy.fr. Catherine DUCLOS, Hôpital AVICENNE, Bobigny, catherine.duclos@aphp.fr. Siham BENZIRAR, CHU Brabois Université de Lorraine, Nancy, s.benzirar@ Emmanuel COSSON, Hôpital AVICENNE, Bobigny, emmanuel.cosson@aphp.fr. chru-nancy.fr. Erwan GUYOT, Hôpital AVICENNE, Bobigny, erwan.guyot@aphp.fr. Catherine MALAPLATE, CHU Brabois Université de Lorraine, Nancy, Aurore DENIAU, Hôpital AVICENNE, Bobigny, aurore.deniau@aphp.fr. c.malaplate@chu-nancy.fr. Phucthutrang NGUYEN, Hôpital AVICENNE, Bobigny, phucthutrang.nguyen@ Thierry MATTON, CHU Brabois Université de Lorraine, Nancy, t.matton@chru- aphp.fr. nancy.fr. Yves REZNIK, CHU Caen Normandie, Caen, reznik-y@chu-caen.fr. Julien POISSY, Hôpital salengro CHU, Lille, julien.poissy@chru-lille.fr. Michael JOUBERT, CHU Caen Normandie, Caen, joubert-m@chu-caen.fr. Karine FAURE, Hôpital Huriez CHRU, Lille, karine.faure@chru-lille.fr. Stéphane ALLOUCHE, CHU Caen Normandie, Caen, allouche-s@chu-caen.fr. Pierre FONTAINE, Hôpital Huriez CHRU, Lille, pierre.fontaine@chru-lille.fr. Lydia GUITTET, CHU Caen Normandie, Caen, guittet-l@chu-caen.fr. Florence BAUDOUX, Hôpital Huriez CHRU, Lille, florence.baudoux@chru-lille.fr. Steven GRANGE, CHU Rouen, Rouen, steven.grange@chu-rouen.fr. Anne VAMBERGUE, Hôpital Huriez CHRU, Lille, anne.vambergue@chru-lille.fr. Manuel ETIENNE, CHU Rouen, Rouen, manuel.etienne@chu-rouen.fr. Jean David PEKAR, Hôpital Huriez CHRU, Lille, jeandavid.PEKAR@chru-lille.fr. Gaëtan PRÉVOST, CHU Rouen, Rouen, gaetan.prevost@chu-rouen.fr. Marc LAMBERT, Hôpital Calmette CHU, Lille, marc.lambert@chru-lille.fr. Valéry BRUNEL, CHU Rouen, Rouen, valery.brunel@chu-rouen.fr. Cécile YELNIK, Hôpital Calmette CHU, Lille, cecile.yelnik@chru-lille.fr. Jean-Christophe LAGIER, IHU Marseille, Marseille, JeanChristophe.LAGIER@ Amélie BRUANDET, Hôpital Huriez CHRU, Lille, amelie.bruandet@chru-lille.fr. ap-hm.fr. Laurent PETIT, CHU de Bordeaux, Bordeaux, laurent.petit@chu-bordeaux.fr. Didier RAOULT, IHU Marseille, Marseille, didier.raoult@ap-hm.fr. Didier NEAU, CHU de Bordeaux, Bordeaux, didier.neau@chu-bordeaux.fr. Anne DUTOUR, CHU Nord et Conception, Marseille, anne.dutour@ap-hm.fr. Vincent RIGALLEAU, CHU de Bordeaux, Pessac, vincent.rigalleau@chu-bor‑ Bénédicte GABORIT, CHU Nord et Conception, Marseille, benedicte.gaborit@ deaux.fr. ap-hm.fr. Annie BERARD, CHU de Bordeaux, Bordeaux, annie.berard@chu-Bordeaux.fr. Sandrine BOULLLU, CHU Nord, Marseille, sandrine.boullu@ap-hm.fr. Amandine GALIOOT, CHU de Bordeaux, Pessac, amandine.galioot@chu- Patrice DARMON, CHU Nord et Conception, Marseille, patrice.darmon@ap-hm. bordeaux.fr. fr. Remy COUDROY, CHU Poitiers, Poitiers, Remi.COUDROY@chu-poitiers.fr. Adèle LASBLEIZ, CHU Nord et Conception, Marseille, adele.lasbleiz@ap-hm.fr. Arnaud THILLE, CHU Poitiers, Poitiers, arnaud.thille@chu-poitiers.fr. Mathieu CERINO, CHU Conception, Marseille, mathieu.cerino@ap-hm.fr. René ROBERT, CHU Poitiers, Poitiers, rene.robert@chu-poitiers.fr. Fanny ROMAIN, CHU Conception, Marseille, fanny.romain@ap-hm.fr. France ROBLOT-CAZENAVE, CHU Poitiers, Poitiers, France.CAZENAVE-ROBLOT@ Marie HOUSSAYS, CHU Conception, Marseille, marie.houssays@ap-hm.fr. chu-poitiers.fr. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 14 of 18 Jean Pierre QUENOT, CHU François Mitterand, Dijon, jean-pierre.quenot@ Michel MARRE, Clinique Ambroise Paré, Paris, marre.michel@gmail.com. chu-dijon.fr. Johann AUCHABIE, CH Cholet, Cholet, johann.auchabie@ch-cholet.fr. Lionel PIROTH, CHU François Mitterand, Dijon, lionel.piroth@chu-dijon.fr. Roxane COURTOIS, CH Cholet, Cholet, roxane.courtois@ch-cholet.fr. Bruno VERGÈS, CHU François Mitterand, Dijon, bruno.verges@chu-dijon.fr. Thierry DURIEZ, CH Cholet, Cholet, thierry.duriez@ch-cholet.fr. Laurence DUVILLARD, CHU François Mitterand, Dijon, laurence.duvillard@ Tiphaine MERGEY, CH Cholet, Cholet, tiphaine.mergey@ch-cholet.fr. chu-dijon.fr. Laura VALLEE, CH Cholet, Cholet, laura.vallee@ch-cholet.fr. Bernard BONNOTTE, CHU François Mitterand, Dijon, bernard.bonnotte@chu- Laetitia SEGUIN, CH Cholet, Cholet, laetitia.seguin@ch-cholet.fr. dijon.fr. Abdallah AL-SALAMEH, CHU Amiens- Picardie, Amiens, al-salameh.abdallah@ Alain MERCAT, CHU ANGERS, Angers, almercat@chu-angers.fr. chu-amiens.fr. Vincent DUBEE, CHU ANGERS, Angers, vincent.dubee@chu-angers.fr. Jean-Philippe LANOIX, CHU Amiens- Picardie, Amiens, lanoix.jean-philippe@ Ingrid ALLIX, CHU ANGERS, Angers, inallix@chu-angers.fr. chu-amiens.fr. Patrice RODIEN, CHU ANGERS, Angers, parodien@chu-angers.fr. Sandrine SORIOT-THOMAS, CHU Amiens- Picardie, Amiens, soriot-thomas. Robin DHERSIN, CHU ANGERS, Angers, Robin.Dhersin@chu-angers.fr. sandrine@chu-amiens.fr. Maylis LEBEAULT, CHU ANGERS, Angers, maylis.lebeault@chu-angers.fr. Anne-Marie BOURGEOIS-DESCOULS, CHU Amiens- Picardie, Amiens, bour‑ wojciech TRZEPIZUR, CHU ANGERS, Angers, WoTrzepizur@chu-angers.fr. geois.anne-marie@chu-amiens.fr. Jocelyne LOISON, CHU ANGERS, Angers, jocelyne.loison@chu-angers.fr. Rachel DESAILLOUD, CHU Amiens- Picardie, Amiens, dessaillud.rachelàchu- Antoine BRANGIER, CHU ANGERS, Angers, antoine.brangier@chu-angers.fr. amiens.fr. Pierre ASFAR, CHU ANGERS, Angers, piasfar@chu-angers.fr. Natacha GERMAIN, CHU de Saint Etienne, Saint Etienne, natacha.germain@ Pascal REYNIER, CHU ANGERS, Angers, pareynier@chu-angers.fr. chu-st-etienne.fr. Françoise LARCHER, CHU ANGERS, Angers, frlarcher@chu-angers.fr. Bogdan GALUSCA, CHU de Saint Etienne, Saint Etienne, bogdan.galusca@ Françoise JOUBAUD, CHU ANGERS, Angers, frjoubaud@chu-angers.fr. chu-st-etienne.fr. Marie-Rita ANDREU, CHU ANGERS, Angers, marierita.andreu@chu-angers.fr. Gwenaelle BELLETON, CHU de Saint Etienne, Saint Etienne, gwenaelle.bel‑ Geoffrey URBANSKI, CHU ANGERS, Angers, geoffrey.urbanski@chu-angers.fr. leton@chu-st-etienne.fr. Laurent HUBERT, CHU ANGERS, Angers, lahubert@chu-angers.fr. Nesrine MAROUANI, CHU de Saint Etienne, Saint Etienne, nesrine.marouani@ Cedric ANNWEILER, CHU ANGERS, Angers, ceannweiler@chu-angers.fr. chu-st-etienne.fr. Jean DELLAMONICA, CHU de Nice—Hôpital de l’Archet, Nice, dellamonica.j@ Delia PALAGHIU, CHU de Saint Etienne, Saint Etienne, delia.palaghiu@chu-st- chu-nice.fr. etienne.fr. Johan COURJON, CHU de Nice—Hôpital de l’Archet, Nice, courjon.j@chu-nice. Amira HAMMOUR, CHU de Saint-Etienne, Saint-Etienne, amira.hammour@ fr. chu-st-etienne.fr. Nicolas CHEVALIER, CHU de Nice—Hôpital de l’Archet, Nice, chevalier.n@ Fernando BERDAGUER, Hôpital Nord Franche-Comté, Belfort, fberdaguer@ chu-nice.fr. hotmail.com. Giulia CHINETTI, CHU de Nice—Hôpital Pasteur, Nice, chinetti.g@chu-nice.fr. Thimothée KLOPFENSTEIN, Hôpital Nord Franche-Comté, Belfort, Timothee. Magda CHAFAI, CHU de Nice—Hôpital de l’Archet, Nice, chafai.m@chu-nice.fr. KLOPFENSTEIN@hnfc.fr. Bruno MOURVILLIER, CHU de Reims, Reims, bmourvillier@chu-reims.fr. Hajer ZAYET, Hôpital Nord Franche-Comté, Belfort, Hajer.ZAYET@hnfc.fr. Firouze BANI-SADR, CHU de Reims, Reims, fbanisadr@chu-reims.fr. Patrice WINISZEWSKI, Hôpital Nord Franche-Comté, Belfort, Patrice.WINISZE‑ Sarra BARRAUD, CHU de Reims, Reims, sbarraud@chu-reims.fr. WSKI@hnfc.fr. Brigitte DELEMER, CHU de Reims, Reims, bdelemer@chu-reims.fr. Marie ZANUSSO, Hôpital Nord Franche-Comté, Belfort, marie.zanusso@hnfc.fr. Philippe GILLERY, CHU de Reims, Reims, pgillery@chu-reims.fr. Pauline GARNIER, Hôpital Nord Franche-Comté, Belfort, pauline.garnier@hnfc. Pascale LABEDADE, Centre Hospitalier Sud-Francilien, Corbeil-Essonnes, fr. pascale.labedade@chsf.fr. Ingrid JULIER, CH de Ales, Ales, dr.julier@ch-ales.fr. Amélie CHABROL, Centre Hospitalier Sud-Francilien, Corbeil-Essonnes, amelie. Karim HAMZAOUI, CH de Ales, Ales, dr.hamzaoui@ch-ales.fr. chabrol@chsf.fr. Sophie MARTY-GRES, CH de Ales, Ales, biologie@ch-ales.fr. Alfred PENFORNIS, Centre Hospitalier Sud-Francilien, Corbeil-Essones, alfred. Tarik EL SADKI, CH de Ales, Ales, biologie@ch-ales.fr. penfornis@chsf.fr. Lucile CADOT, CH de Ales, Ales, biologie@ch-ales.fr. Catherine PETIT, Centre Hospitalier Sud-Francilien, Corbeil-Essones, catherine. Jean-Louis DUBOST, CH de Pontoise, Pontoise, jean-louis.dubost@ght-novo.fr. petit@chsf.fr. Céline GONFROY, CH de Pontoise, Pontoise, celine.gonfroy@ght-novo.fr. Coralie AMADOU, Centre Hospitalier Sud-Francilien, Corbeil-Essonnes, coralie. Catherine CAMPINOS, CH de Pontoise, Pontoise, catherine.campinos@ght- amadou@chsf.fr. novo.fr. Maxime ADLER, Centre Hospitalier Sud-Francilien, Corbeil-Essonnes, maxime. Pascale MARTRES, CH de Pontoise, Pontoise, pascale.martres@ght-novo.fr. adler@chsf.fr. Marie Pierre COULHON, CH de Pontoise, Pontoise, marie-pierre.coulhon@ Clément DUBOST, HIA Bégin, Saint Mandé, clement.dubost@intradef.gouv.fr. ght-novo.fr. Pierre-Louis CONAN, HIA Bégin, Saint Mandé, pierre-louis.conan@intradef. Nicolas ALLOU, CHU Felix Guyon, Saint Denis, nicolas.allou@chu-reunion.fr. gouv.fr. Marwa BACHIR, CHU Felix Guyon, Saint Denis, marwa.bachir@chu-reunion.fr. Lyse BORDIER, HIA Bégin, Saint Mandé, lyse.bordier@intradef.gouv.fr. Stella HOANG, CHU Felix Guyon, Saint Denis, stella.hoang@chu-reunion.fr. Franck CEPPA, HIA Bégin, Saint Mandé, franck.ceppa@intradef.gouv.fr. Candice KEMBELLEC, CHU Felix Guyon, Saint Denis, candice.kembellec@chu- Cyril GARCIA, HIA Bégin, Saint Mandé, cyril1.garcia@intradef.gouv.fr. reunion.fr. Mathilde SOLLIER, HIA Bégin, Saint Mandé, mathilde.sollier@intradef.gouv.fr. Olivia SUPLY, CHU Felix Guyon, Saint Denis, olivia.suply@chu-reunion.fr. Olivier DUPUY, GH Paris Saint Joseph, Paris, odupuy@hpsj.fr. Fatima KHARCHA, CHU Felix Guyon, Saint Denis, fatima.kharcha@chu-reunion. Sophie LAPLANCE, GH Paris Saint Joseph, Paris, slaplanche@hpsj.fr. fr. Olivier BILLUART, GH Paris Saint Joseph, Paris, obilluart@hpsj.fr. Anne-Claire DEVOUGE, CHU Felix Guyon, Saint Denis, anne-claire.devouge@ Marie Joseph AROULANDA, GH Paris Saint Joseph, Paris, mjaroulanda@hpsj.fr. chu-reunion.fr. Frédérique OLIVIER, CH CAHORS, Cahors, frederique.olivier@ch-cahors.fr. Anna FLAUS-FURMANUK, CHU Felix Guyon, Saint Denis, anna.flaus-furma‑ Florence AYON, CH CAHORS, Cahors, florence.ayon@ch-cahors.fr. niuk@chu-reunion.fr. Nathalie WILHELM, CH CAHORS, Cahors, nathalie.wilhelm@ch-cahors.fr. Isabelle MADELINE, CHU Felix Guyon, Saint Denis, isabelle.madeline@chu- Loic EPELBOIN, CHU Cayennes, Cayenne, loic.epelboin@ch-cayenne.fr. reunion.fr. Nadia SABBAH, CHU Cayennes, Cayenne, nadia.sabbah@ch-cayenne.fr. Vincent EHINGER, CHU Felix Guyon, Saint Denis, vincent.ehinger@chu-reunion. Aurelie CHARPIN, CHU Cayennes, Cayenne, aurelie.charpin@ch-cayenne.fr. fr. Pierre SQUARA, Clinique Ambroise Paré, Paris, pierre.squara@orange.fr. Sophie BASTARD, CHU Felix Guyon, Saint Denis, sophie.bastard@chu-reunion. Olivier BELLIARD, Clinique Ambroise Paré, Paris, olivier_belliard@yahoo.fr. fr. Claude DUBOIS, Clinique Ambroise Paré, Paris, claude.dubois@clinique-a-pare. Loic RAFFRAY, CHU Felix Guyon, Saint Denis, loic.raffray@chu-reunion.fr. fr. Frederic RENOU, CHU Felix Guyon, Saint Denis, frederic.renou@chu-reunion.fr. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 15 of 18 Aude BOJARSKI, CHU Felix Guyon, Saint Denis, aude.bojarski@chu-reunion.fr. Mariam RONCATO-SABERAN, Saint Louis, La Rochelle, mariam.roncato@ch- Caroline PAUL, CHU Felix Guyon, Saint Denis, caroline.paul@chu-reunion.fr. larochelle.fr. Karine BORSU, CHU Felix Guyon, Saint Denis, karine.borsu@chu-reunion.fr. Didier GOUET, Saint Louis, La Rochelle, didier.gouet@ch-larochelle.fr. Angelique GORLIN, CHU Felix Guyon, Saint Denis, angelique.gorlin@chu- Romain LEMARIE, Saint Louis, La Rochelle, romain.lemarie@ch-larochelle.fr. reunion.fr. Hong_An ALLANO, Saint Louis, La Rochelle, hong-an.allano@ght-atlantique17. Servane DI BERNARDO, CHU Felix Guyon, Saint Denis, servane.dibernardo@ fr. chu-reunion.fr. Emmanuel VIVIER, Saint-Joseph Saint-Luc, Lyon, evivier@ch-stjoseph-stluc- Carole TRUONG VAN UT, CHU Felix Guyon, Saint Denis, carole.truong-van-ut@ lyon.fr. chu-reunion.fr. Caroline PARISET, Saint-Joseph Saint-Luc, Lyon, cpariset@ch-stjoseph-stluc- Stephane RENAUD, CHU Felix Guyon, Saint Denis, stephane.renaud@chu- lyon.fr. reunion.fr. Cédric LUYTON, Saint-Joseph Saint-Luc, Lyon, cluyton@ch-stjoseph-stluc-lyon. Antoine VIGNOLES, CHU Felix Guyon, Saint Denis, antoine.vignoles@chu- fr. reunion.fr. Lucien MARCHAND, Saint-Joseph Saint-Luc, Lyon, lmarchand@ch-stjoseph- Emilie FOCH, CHU Felix Guyon, Saint Denis, emilie.foch@chu-reunion.fr. stluc-lyon.fr. Laurie MASSE, CHU Felix Guyon, Saint Denis, laurie.masse@chu-reunion.fr. Fanny DOROSZEWSKI, Saint-Joseph Saint-Luc, LYON, fdoroszewski@ch- Hubert GRAND, robert boulin, Libourne, hubert.grand@ch-libourne.fr. stjoseph-stluc-lyon.fr. Helene FERRAND, robert boulin, Libourne, helene.ferrand@ch-libourne.fr. Matthieu PECQUET, Saint-Joseph Saint-Luc, Lyon, mpecquet@ch-stjoseph- Christelle RAFFAITIN-CARDIN, robert boulin, Libourne, christelle.raffaitin@ stluc-lyon.fr. ch-libourne.fr. Laurent PERARD, Saint-Joseph Saint-Luc, Lyon, lperard@ch-stjoseph-stluc-lyon. Hadjer ZELLAGUI, robert boulin, Libourne, hadjer.zellagui@ch-libourne.fr. fr. Celine CASTANG-BRACHET, robert boulin, Libourne, celine.castang@ch- Sylvie VUILLERMOZ-BLAS, Saint-Joseph Saint-Luc, Lyon, svuillermoz@ch- libourne.fr. stjoseph-stluc-lyon.fr. Frederique BOURY, robert boulin, Libourne, frederique.boury@ch-libourne.fr. Nicolas KACKI, CHD de Vendée, La Roche Sur Yon, nicolas.kacki@chd-vendée.fr. Ana ALVAREZ TENA, CH Albi, Albi, ana.alvareztena@ch-albi,fr. Patricia CHARRIER, CHD de Vendée, La Roche Sur Yon, patricia.charrier@chd- Isabelle MOURA, CH Albi, Albi, isabelle.moura@ch-albi.fr. vendée.fr. Pierre KALFON, LOUIS PASTEUR, Le Coudray, pkalfon@ch-chartres.fr. Amélie DUCET-BOIFFARD, CHD de Vendée, La Roche Sur Yon, amelie.ducet- Juliana DARASTEANU, LOUIS PASTEUR, Le Coudray, jdarasteanu@ch-cahrtres.fr. boiffard@chd-vendee.fr. Arnaud MONIER, LOUIS PASTEUR, Le Coudray, amonier@ch-chartres.fr. Françoise DESROYS DU ROURE, CHD de Vendée, La Roche Sur Yon, francois. Pascal FOUCAULT, LOUIS PASTEUR, Le Coudray, pfoucault@ch-chartres.fr. desroysduroure@chd-vendee.fr. Alexandra DEPUILLE, LOUIS PASTEUR, Le Coudray, adepuille@ch-chartres.fr. Olivier BOURRON, Pitié-Salpêtrière, Paris, olivier.bourron@aphp.fr. Stéphanie LAUGIER-ROBIOLLE, CH D’AUCH, 32,000, s.laugier-robiolle@ch-auch. Dominique BONNEFONT-ROUSSELOT, Pitié-Salpêtrière, Paris, dominique.rous‑ fr. selot@aphp.fr. Patrick CANEIRO, CH D’AUCH, 32,000, p.caneiro@ch-auch.fr. Suzanne LAROCHE, Pitié-Salpêtrière, Paris, Suzanne.laroche@aphp.fr. Maud BASSO, CH D’AUCH, 32,000, maud.basso@ch-auch.fr. Franck PHAN, Pitié-Salpêtrière, Paris, franck.phan@aphp.fr. Etienne LARGER, Hôpital COCHIN, Paris, etienne.larger@aphp.fr. Agnès HARTEMANN, Pitié-Salpêtrière, Paris, agnes.hartemann@aphp.fr. Samir BOUAM, Hôpital COCHIN, Paris, samir.bouam@aphp.fr. Cyrielle CAUSSY, CHU LYON SUD, Pierre Benite, cyrielle.caussy@chu-lyon.fr. Wahiba BENZENATI, Hôpital COCHIN, Paris, wahiba.benzenati-ext@aphp.fr. Emmanuel DISSE, CHU LYON SUD, Pierre Benite, emmanuel.disse@chu-lyon.fr. Leila AIT BACHIR, Hopital francobritannique, Levallois, leila.aitbachir@ihfb.org. Emilie BLOND, CHU LYON SUD, Pierre Benite, emilie.blond@chu-lyon.fr. Camille CUSSAC PILLEGAND, Hopital francobritannique, Levallois, camille. Claude GUERIN, Hôpital Croix Rousse, Lyon, claude.guerin@chu-lyon.fr. cussac-pillegand@ihfb.org. Thomas PERPOINT, Hôpital Croix Rousse, Lyon, thomas.perpoint@chu-lyon.fr. Marc VASSE, Hopital francobritannique, Suresnes, marc.vasse@hopital-foch.fr. Philippe MOULIN, Hôpital Louis pradel, Lyon, philippe.moulin@chu-lyon.fr. Christophe MICHARD, CH du Forez, Montbrison, christophe.michard@ch-forez. Régine CARTIER, Hôpital Louis pradel, Lyon, regine.cartier@chu-lyon.fr. fr. Geoffroy HARIRI, Hôpital Saint-Antoine, Paris, geoffroy.hariri@aphp.fr. Nathanaëlle MONTANIER, CH du Forez, Montbrison, nathanaelle.montanier@ Dorothée CHOPIN, Hôpital Saint-Antoine, Paris, dorothee.chopin@aphp.fr. ch-forez.fr. Camille VATIER, Hôpital Saint-Antoine, Paris, camille.vatier@aphp.fr. Luc MILLOT, CH du Forez, Montbrison, luc.millot@ch-forez.fr. Nathalie BOURCIGAUX, Hôpital Saint-Antoine, Paris, nathalie.bourcigaux@ Françoise CREPET, CH du Forez, Montbrison, francoise.crepet@ch-forez.fr. aphp.fr. Danielle RATSIMBA, CH du Forez, Montbrison, danielle.ratsimba@ch-forez.fr. Emmanuelle CHAIGNEAU, Hôpital Saint-Antoine, Paris, emmanuelle. Kevin BOUILLER, CHU JEAN MINJOZ, Besancon, kbouiller@chu-besancon.fr. chaigneau@aphp.fr. Sophie BOROT, CHU JEAN MINJOZ, Besancon, sophie.borot@univ-fcomte.fr. Sophie CHRISTIN-MAITRE, Hôpital Saint-Antoine, Paris, sophie.christin-maitre@ Isabelle BRUCKERT, CHU JEAN MINJOZ, Besancon, ibruckert@chu-besancon.fr. aphp.fr. Annie CLERGEOT, CHU JEAN MINJOZ, Besancon, aclergeot@chu-besancon.fr. Bruno DONADILLE, Hôpital Saint-Antoine, Paris, bruno.donadille@aphp.fr. Franck SCHILLO, CHU JEAN MINJOZ, Besancon, fschillo@chu-besancon.fr. Bruno FEVE, Hôpital Saint-Antoine, Paris, bruno.feve@aphp.fr. Dorothée VIGNES, CHU Antoine Béclère, Clamart, dorothée.vignes@aphp.fr. Sophie LAMOTHE, Hôpital Saint-Antoine, Paris, sophie.lamothe@aphp.fr. Muriel BOURGEON-GHITTORI, CHU Antoine Béclère, Clamart, muriel.bour‑ Julie SARFATI, Hôpital Saint-Antoine, Paris, julie.sarfati@aphp.fr. geon@aphp.fr. Pascal PERNET, Hôpital Saint-Antoine, Paris, pascal.pernet@aphp.fr. Hamoud LACHGAR, CHU Antoine Béclère, Clamart, hamoud.lachgar@aphp.fr. Anne CHAMBON, CH Côtes Basques, Bayonne, achambon@ch-cotebasque.fr. Claire LAMBERT DE CURSAY, CHU Antoine Béclère, Clamart, claire.lambertde‑ Delphine DEMARSY, CH Côtes Basques, Bayonne, ddemarsy@ch-cotebasque.fr. cursay@aphp.fr. Hugo CAMPAGNE, CH Côtes Basques, Bayonne, hcampagne@ch-cotebasque. Stéphane LEVANTE, CHU Antoine Béclère, Clamart, stephane.levante@aphp.fr. fr. Jean Charles AUREGAN, CHU Antoine Béclère, Clamart, jean-charles.auregan@ Françoise LATIL-PLAT, CH Avignon, Avignon, fplat@ch-avignon.fr. aphp.fr. Monica BERNE, CH Avignon, Avignon, MBeyrne@ch-avignon.fr. Antoine MERLET, CH Bretagne Atlantique, Vannes, antoine.merlet@ch- Marilyne GRINAND, CH Avignon, Avignon, GRINAND.Marilyne@ch-avignon.fr. bretagne-atlantique.fr. Marion TOUZET, CH Avignon, Avignon, TOUZET.Marion@ch-avignon.fr. Cécile ZARAGOZA, CH Bretagne Atlantique, Vannes, cecile.zaragora@ch- Aydrey ZABULON, CHU Martinique, Fort de France, audrey.zabulon@chu- bretagne-atlantique.fr. martinique.fr. Gwénaëlle ARNAULT, CH Bretagne Atlantique, Vannes, gwenaelle.arnault@ Jocelyne CRASPAG, CHU Martinique, Fort de France, jocelyne.craspag@chu- ch-bretagne-atlantique.fr. martinique.fr. Anne-Gaëlle LE LOUPP, CH Bretagne Atlantique, Vannes, anne-gaelle-le8l‑ Catherine LEDOUX, CHU Martinique, Fort de France, catherine.ledoux@chu- oupp@ch-bretagne-atlantique.fr. martinique.fr. Olivier LESIEUR, Saint Louis, La Rochelle, olivier.lesieur@ch-larochelle.fr. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 16 of 18 Cedric CONTARET, CHU Martinique, Fort de France, Cedric.CONTARET@chu- Parfitt; North West Anglia NHS Foundation Trust, Hinchingbrooke Hospital: martinique.fr. Mazharul Islam, Sadia Nasir; Oxford University Hospitals NHS Foundation Trust, Blandine JANAND-DELENNE, CH du Pays d’Aix, Aix en Provence, bdelenne@ Oxford Centre for Diabetes, Endocrinology and Metabolism, Churchill Hospital: ch-aix.fr. Rustam Rea, Gail Roadknight, Kinga Várnai, Senthil Vasan; Pennine Acute Hos‑ Anaïs GIRAUD, CH du Pays d’Aix, Aix en Provence, agiraud@ch-aix.fr. pitals NHS Trust, Diabetes Centre, North Manchester General Hospital: Vilashini Marie Lou LACRIMINI, CH du Pays d’Aix, Aix en Provence, mlacrimini@ch-aix.fr. Arul Devah; Royal Berkshire NHS Foundation Trust (Berkshire Healthcare NHS Joëlle ARRIVIE, CH de Bigorre, Tarbes, jarrivie@ch-tarbes-vic.fr. Foundation Trust), Centre for Diabetes & Endocrinology: Foteini Kavvoura; Deborah ANCELLE, CH Le Havre, Le Havre, deborah.ancelle@ch-havre.fr. Royal Devon and Exeter NHS Foundation Trust, Royal Devon and Exeter Carine GUILLOIS, CH Le Havre, Le Havre, carine.guillois@ch-havre.fr. Hospital (Wonford): Lina Ficken, James Gilham, Vincent Simpson, Neil Walker; Bénédicte FREMY, CH Agen, Agen, fremyb@ch-agen-nerac.fr. Royal Free London NHS Foundation Trust, Royal Free Hospital: Umaira Aziz, Amina CHAALAL, CH Agen, Agen, chaalalam@ch-agen-nerac.fr. Efthimia Karra, Dipesh Patel, Miranda Rosenthal; Salford Royal NHS Foundation Gaëlle BARRANDE, CH Argenteuil, Argenteuil, gaelle.barrande@ch-argenteuil.fr. Trust, Salford Royal Hospital: Tracy Curran, Angela Paisley; Sandwell & West Anne DORANGE, CH Le Mans, Le Mans, adorange@ch-lemans.fr. Birmingham NHS Trust, Diabetes at SWBH: Melissa Cull, Parijat De P, May Thin Eglantine ROUANET, CH Le Mans, Le Mans, erouanet@ch-lemans.fr. Khine, Pari Qayyam, Robert Ryder, Priscilla Sarkar; Sheffield Teaching Hospitals Dominique SERET-BEGUE, CH Gonesse, Gonesse, dominique.seret-begue@ NHS Foundation Trust, Northern General Hospital: Rajiv Gandhi; Surrey & ch-gonesse.fr. Sussex Healthcare NHS Trust, East Surrey Hospital: Ben Field, James Clark, Audrey SAOUD, CH Gonesse, Gonesse, audrey.saoud@ch-gonesse.fr. Vesna Hogan, Lauren Jackson, Jamie-Leigh Williamson, R Younes;Taunton Anne-Marie GUEDJ, CH Nîmes, Nîmes, anne.marie.guedj@chu-nimes.fr. and Somerset NHS Foundation Trust—Musgrove Park Hospital: Lucy Robin; Nathalie BEDOS, CH Nîmes, Nîmes, nathalie.bedos@chu-nimes.fr. The Newcastle Upon Tyne Hospitals NHS Foundation Trust, The Royal Victoria Fritz-Line VELAYOUDOM, CHU Guadeloupe, Les Abymes, fritz-line.velayou‑ Infirmary: Lydia Grixti, Suann Tee; University Hospital of Derby and Burton NHS dom@univ-antilles.fr. Foundation Trust, Royal Derby Hospital and Queen’s Hospital Burton: Abilash Marie DUMAS, Hôpital St Vincent de Paul, Lille, dumas.marie@ghicl.net. Sathya, Emma Wilmot; University Hospital Southampton NHS Foundation Benoite GONDA, Hôpital St Vincent de Paul, Lille, Gonda.Benoite@ghicl.net. Trust, Diabetes at UHSNHSFT: Mayank Patel; University Hospitals Birmingham Christine COFFIN, CH Perigueux, Perigueux, christine.coffin@ch-perigueux.fr. NHS Foundation Trust, Heartlands Hospital: Catherine Holmes; University Hos‑ Stéphanie GIBIAT, CH Perigueux, Perigueux, urc@ch-perigueux.fr. pitals Birmingham NHS Foundation Trust, University Hospital of Birmingham: Myriam LUNGO, CH de Bastia, Bastia, myriam.lungo@gmail.com. Wasim Hanif, Sandip Ghosh, Parth Narendran; University Hospitals of Leicester Chantal BULLY, Les Portes du Sud, Venissieux, C.BULLY@LESPORTESDUSUD.NET. NHS Trust, Diabetes Research Centre, Leicester General Hospital: Ehtasham Pierre SERUSCLAT, Les Portes du Sud, Venissieux, p.serusclat@lesportesdusud. Ahmad, Ejaz Ahmed, Melanie Davies, Steven Hartshorn, Kamlesh Khunti, Lee net. Simons, David Webb; University of Leicester: Ben Maylor. Stella BULLY, Les Portes du Sud, Venissieux, stellabully.ecsel@gmail.com. University of Oxford: Jim Davies, Oliver Freeman, Steve Harris, Yue Ruan; West Patricia CARRE, Les Portes du Sud, Venissieux, patcarre69@gmail.com. Suffolk Hospital NHS Foundation Trust, West Suffolk Hospital: Anupam Brahma; Jean-Philippe LEBERRE, Medipôle Hôpital Mutualiste, Villeurbanne, j.leberre@ Yeovil District Hospital NHS Foundation Trust, Yeovil District Hospital: Seshadri resamut.fr. Pramodh. Carlos ELKHOURY, Medipôle Hôpital Mutualiste, Villeurbanne, c.elkhoury@ Scotland resamut.fr. NHS Forth Valley, Forth Valley Royal Hospital: Katy Frew, Alison Mackenzie, Marine THIEUX, Medipôle Hôpital Mutualiste, Villeurbanne, m.thieux@resamut.fr. Abigail Wild; NHS Greater Glasgow and Clyde, Queen Elizabeth University Laetitia PARADISI-PRIEUR, Medipôle Hôpital Mutualiste, Villeurbanne, l.paradisi- Hospital: Helen Casey, Deborah Morrison, Conor McKeag, Anne Sillars, Angus prieur@resamut.fr. Stirling. List of Contributors for the ABCD nationwide Covid 19 and Diabetes audit: Wales ABCD nationwide Covid 19 and Diabetes audit – initial setup, maintenance Aneurin Bevan University Health Board, Nevill Hall Hospital: Fiona Smeeton; and nationwide analysis: Rustam Rea, Emma Wilmot, Kamlesh Khunti, Sarah Aneurin Bevan University Health Board, Royal Gwent Hospital: Syed Muham‑ Wild, Ben Field, Parth Narendran, Rajiv Gandhi, Sophie Harris, Dinesh Nagi, mad, Kofi Obuobie, Win Yin; Cardiff & Vale University Health Board, University Robert Ryder, Jim Davies, Steve Harris, Oliver Freeman, Ben Maylor, Kinga A Hospital Llandough: Neera Agarwal, Mike Atkinson; Cardiff & Vale University Várnai, Gail Roadknight, Melissa Cull. Statistician: Yue Ruan. Health Board, University Hospital of Wales: Sai Ambati, Rahim Khan, Preethi England Nalla, Arshiya Tabasum; Hywel Dda University Health Board, Glangwili General Barts Health NHS Trust, Newham University Hospital: Amy Edwards, Susan Hospital: Stamatios Zouras; Hywel Dda NHS Trust, Prince Philip Hospital: Akhila Gelding, Kirun Gunganah; Bolton NHS Foundation Trust,Royal Bolton Hospital: Mallipedhi; Swansea Bay University Health Board, Singleton Hospital: Richard Pyei Aung, Moulinath Banerjee; Brighton and Sussex University Hospitals NHS Chudleigh, David Williams. Trust (Univeristy Hospitals Sussex NHS Foundation Trust), Royal Sussex County Hospital: Ali Chakera, Dominique Rouse; Countess of Chester Hospital NHS Author contributions Foundation Trust, Countess of Chester Hospital: Syed Haris Ahmed, Ho Yee GL, PD, DM collected the Hospital del Mar-Hospital de la Santa Creu I Sant Pau Cheung, Hywel Roberts, Susan Seal, Syed Saah Shah; Dartford and Gravesham cohort and BV and JFN collected the cohort from HM Hospìtales. GL, BV and NHS Trust, Darent Valley Hospital: Amir Hayat, Cynthia Mohandas. DM drafted the first version of the manuscript. BC, MW, PG and SaH designed East and North Hertfordshire NHS Trust, Lister Hospital: Htet Htet Aung, Su and conducted the CORONADO study. PJS conducted the CORONADO study. Khant Chel, Nyan Lin, Kavitia Narula, Furruq Quadri, Su Lei Yin, Yin Yin; East Kent RR, SHW, YR and KK (with additional colleagues) designed the ABCD COVID-19 Hospitals University NHS Foundation Trust, William Harvey Hospital (Ashford): national audit. YR conducted the statistical analysis of the ABCD data. All Alamin Alkundi, Abdelmajid Musa; East Suffolk and North Essex NHS Founda‑ authors approved the final manuscript. tion Trust, Colchester General Hospital: Emma Birbeck, Charles Bodmer; East Sussex Healthcare NHS Trust, Conquest Hospital & Eastbourne District General Funding Hospital: Irene Bossman, Sathis Kumar, Umesh Dashora, Elizabeth Toubi, This research was supported by CIBER-Consorcio Centro de Investigación Mansoor Zafar; George Eliot Hospital NHS Trust, Diabetes Care Team, George Biomédica en Red- (CB15/00071), Instituto de Salud Carlos III, Ministerio de Eliot Hospital: Vinod Patel, Amitha Gopinath; Hull University Teaching Hospitals Ciencia e Innovación. CORONADO study received the following funding: NHS Foundation Trust, Hull Royal Infirmary: Belinda Allan, Remat Karim; King’s the Fondation Francophone de Recherche sur le Diabète (FFRD), supported College Hospital NHS Foundation Trust, King’s College hospital: Dharshana by Novo Nordisk, MSD, Abbott, AstraZeneca, Lilly and FFD (Fédération Appuhamillage, Khubaib Ayoub, Sophie Harris, Charmaine Ilangaratne, Française des Diabétiques) – CORONADO initiative emergency grant; Société Maliha Iqbal, Rory Maclean, Omar Mustafa; Lancashire Teaching Hospitals NHS Francophone du Diabète (SFD) – CORONADO initiative emergency grant; Air Foundation Trust, Royal Preston Hospital: Susan Baxter; London North West Liquide Health Care international. CORONADO initiative emergency grant; University Healthcare NHS Trust, Ealing Hospital: Malgorzata Adamus, Kevin Allergan. CORONADO initiative emergency grant; AstraZeneca. CORONADO Baynes; Maidstone and Tunbridge Wells NHS trust, Maidstone Hospital: Siva initiative emergency grant; Elivie. CORONADO initiative emergency grant; Sivappriyan; Mid Yorkshire Hospitals NHS Trust, Pinderfields Hospital: Ryan Fortil. CORONADO initiative emergency grant; Lifescan. CORONADO initiative D’Costa, Dinesh Nagi; North Bristol NHS Trust, Southmead Hospital: Vernon emergency grant; CORONADO initiative emergency grant; Nantes Métroplole. Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 17 of 18 NHC. CORONADO initiative emergency grant; Novo Nordisk. CORONADO ini‑ References tiative emergency grant; Sanofi. CORONADO emergency grant; PHRC National 1. Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, et al. A pneumonia COVID-19 Hospitalization and Care Organization Division (DGOS) as part of outbreak associated with a new coronavirus of probable bat origin. the Hospital Clinical Research Program (PHRC COVID-19–20-0138). All research Nature. 2020. https://​doi.​org/​10.​1038/​s41586-​020-​2951-z. facilities are acknowledged for providing research associates and research 2. Lippi G, Sanchis-Gomar F, Henry BM. COVID-19: unravelling the clinical technicians for clinical investigations pro bono. The funders of the study had progression of nature’s virtually perfect biological weapon. Ann Transl no role in study design, data collection, data analysis, data interpretation, or Med. 2020. https://​doi.​org/​10.​21037/​atm-​20-​3989. writing of the report. The ABCD nationwide COVID-19 and Diabetes audit is an 3. Verity R, Okell LC, Dorigatti I, Winskill P, Whittaker C, Imai N, et al. Estimates independent audit which has received support from Public Health Wales and of the severity of coronavirus disease 2019: a model-based analysis. Novo Nordisk. Lancet Infect Dis. 2020. https://​doi.​org/​10.​1101/​2020.​03.​09.​20033​357v1. 4. Perez-Saez J, Lauer SA, Kaiser L, Regard S, Delaporte E, Guessous I, et al. Availability of data and materials Serology-informed estimates of SARS-CoV-2 infection fatality risk in Data are available on request from corresponding author and/or national Geneva, Switzerland. Lancet Infect Dis. 2021. https://​doi.​org/​10.​1016/​ study leads with appropriate data governance permission. S1473-​3099(20)​30584-3. 5. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk fac‑ tors for mortality of adult inpatients with COVID-19 in Wuhan, China: Declarations a retrospective cohort study. Lancet. 2020. https://​doi.​org/​10.​1038/​ s41598-​021-​89548-y. Ethics approval and consent to participate 6. Williamson EJ, Walker AJ, Bhaskaran K, Bacon S, Bates C, Morton CE, et al. United Kingdom: association of British clinical diabetologists (ABCD) COVID-19 Factors associated with COVID-19-related death using OpenSAFELY. audit: The audit is registered with Oxford University Hospitals NHS Foundation Nature. 2020. https://​doi.​org/​10.​1038/​s41586-​020-​2521-4. Trust (OUH), a Data Protection Impact Assessment was carried out and the 7. Cariou B, Wargny M, Boureau A-S, Smati S, Tramunt B, Desailloud R, et al. audit was approved by the OUH Caldicott Guardian and the Public Benefit Impact of diabetes on COVID-19 prognosis beyond comorbidity burden: and Privacy Panel in Scotland (reference 2021-0111). France: CORONADO: the CORONADO initiative. Diabetologia. 2022;65:1436–49. The study was sponsored by the Nantes University Hospital and designed in 8. Bellini B, Nreu B, Francesconi P, Mannucci E. Covid-19 pandemic, diabetes accordance with the Declaration of Helsinki. It obtained all regulatory approv‑ and glycemic control: results of a retrospective cohort study of 230.000 als. Spain – HM Hospitales cohort: The study was approved by the Ethics persons with diabetes in tuscany. Nutr Metab Cardiovasc Dis. 2022. Committee of the Primary Health Care University Research Institute (IDIAP) https://​doi.​org/​10.​1016/j.​numecd.​2022.​07.​017. Jordi Gol, Barcelona (approval number: 20/089-PCV). Spain – Barcelona cohort: 9. Fedeli U, Casotto V, Schievano E, Bonora E, Zoppini G. Diabetes as a cause The Hospital del Mar Institutional Ethics Committee (CEIm-2020/9352) and of death across different COVID-19 epidemic waves. Diabetes Res Clin the Hospital de la Santa Creu I Sant Pau Ethics Committee (HSCSP-20/117) Pract. 2022;190: 109984. approved the study and waived the informed consent need due to the study’s 10. Barron E, Bakhai C, Kar P, Weaver A, Bradley D, Ismail H, et al. Associa‑ nature. tions of type 1 and type 2 diabetes with COVID-19-related mortality in England: a whole-population study. Lancet Diabetes Endocrinol. 2020. Consent for publication https://​doi.​org/​10.​2139/​ssrn.​36052​25. All authors approved the final manuscript and give consent for the 11. Kastora S, Patel M, Carter B, Delibegovic M, Myint PK. Impact of diabetes publication. on COVID-19 mortality and hospital outcomes from a global perspective: an umbrella systematic review and meta-analysis. Endocrinol diabetes Competing interests Metab. 2022;5: e00338. All other authors declare no competing interests. 12. Roncon L, Zuin M, Rigatelli G, Zuliani G. Diabetic patients with COVID-19 infection are at higher risk of ICU admission and poor short-term out‑ Author details come. J Clin Virol Off Publ Pan Am Soc Clin Virol. 2020;127: 104354. 1 Department of Endocrinology and Nutrition, Hospital del Mar, Institut Hospi‑ 13. Cariou B, Hadjadj S, Wargny M, Pichelin M, Al-Salameh A, Allix I, et al. tal del Mar d’Investigacions Mèdiques (IMIM), Barcelona, Spain. 2 Department Phenotypic characteristics and prognosis of inpatients with COVID-19 of Endocrinology and Nutrition, Center for Biomedical Research on Diabetes and diabetes: the CORONADO study. Diabetologia. 2020. https://​doi.​org/​ and Associated Metabolic Diseases (CIBERDEM), Instituto de Salud Carlos 10.​1007/​s00125-​020-​05180-x. III (ISCIII), Barcelona, Spain. 3 DAP_CAT Group, Unitat de Suport a la Recerca 14. Feldman EL, Savelieff MG, Hayek SS, Pennathur S, Kretzler M, Pop-Busui R. Barcelona, Fundació Institut Universitari Per a la Recerca a l’Atenció Primària COVID-19 and diabetes: a collision and collusion of two diseases. Diabe‑ de Salut Jordi Gol i Gorina (IDIAPJGol), Barcelona, Spain. 4 Institut de Recerca tes. 2020. https://​doi.​org/​10.​2337/​dbi20-​0032. Hospital de la Santa Creu i Sant Pau, Barcelona, Spain. 5 L’Institut du Thorax, 15. Llanera DK, Wilmington R, Shoo H, Lisboa P, Jarman I, Wong S, et al. Université de Nantes, CHU Nantes, CNRS, Nantes, Inserm, France. 6 CHU de Clinical characteristics of COVID-19 patients in a regional population Nantes, CIC Inserm 1413, Clinique Des Données, Nantes, France. 7 Oxford Cen‑ with diabetes mellitus: the ACCREDIT study. Front Endocrinol (Lausanne). tre for Diabetes, Endocrinology and Metabolism, Oxford University Hospitals 2021;12: 777130. NHS Foundation Trust, Oxford, UK. 8 Oxford NIHR Biomedical Research Centre, 16. World Health Organization. Global report on diabetes. World Health Oxford, UK. 9 Primary Health Care Center Raval Sud, Gerència d’Àmbit d’Atenció Organization; 2016. Primaria, Institut Català de la Salut, Barcelona, Spain. 10 Infectious Diseases, Hos‑ 17. Harris S, Ruan Y, Wild SH, Wargny M, Hadjadj S, Delasalle B, et al. Associa‑ pital de la Santa Creu i Sant Pau and Sant Pau Biomedical Research Institute tion of statin and/or renin-angiotensin-aldosterone system modulating (IIB Sant Pau), Barcelona, Spain. 11 CHU de Toulouse & UMR1297/I2MC, Inserm, therapy with mortality in adults with diabetes admitted to hospital with Université de Toulouse, Toulouse, France. 12 Centre d’Investigation Clinique COVID-19: a retrospective multicentre European study. Diabetes Metab CIC 1402, Université de Poitiers, Inserm, CHU de Poitiers, Poitiers, France. Syndr. 2022;16: 102484. 13 Usher Institute, University of Edinburgh, Edinburgh, UK. 14 Diabetes Research 18. Nagi D, Ryder RE, Ruan Y, Field BC, Narendran P, Gandhi R, Harris S, Várnai Centre, Leicester General Hospital, University Hospitals of Leicester NHS Trust, KA, Davies J, Wild SH, Wilmot EG. An audit of people admitted to hospital‑ Leicester, UK. 15 Department of Endocrinology and Nutrition, Hospital de la with diabetes and coronavirus (SARS-CoV-2):data collection methods. The Santa Creu i Sant Pau and Sant Pau Biomedical Research Institute (IIB Sant Association of British Clinical Diabetologists (ABCD) Nationwide Audit. Br Pau), Barcelona, Spain. J Diabetes. 2021;21:96–9. 19. Wargny M, Potier L, Gourdy P, Pichelin M, Amadou C, Benhamou P-Y, et al. Received: 21 August 2022 Accepted: 24 September 2022 Predictors of hospital discharge and mortality in patients with diabetes and COVID-19: updated results from the nationwide CORONADO study. Diabetologia. 2021;64:778–94. 20. Ortega E, Corcoy R, Gratacòs M, Cos Claramunt FX, Mata-Cases M, Puig- Treserra R, et al. Risk factors for severe outcomes in people with diabetes Llauradó et al. Cardiovascular Diabetology (2022) 21:216 Page 18 of 18 hospitalised for COVID-19: a cross-sectional database study. BMJ Open. 2021;11: e051237. 21. Draznin B, Aroda VR, Bakris G, Benson G, Brown FM, Freeman R, et al. 11. Chronic kidney disease and risk management: standards of medical care in diabetes-2022. Diabetes Care. 2022;45:S175–84. 22. Singh AK, Gillies CL, Singh R, Singh A, Chudasama Y, Coles B, et al. Preva‑ lence of co-morbidities and their association with mortality in patients with COVID-19: a systematic review and meta-analysis. Diabetes Obes Metab. 2020;22:1915–24. 23. Apicella M, Campopiano MC, Mantuano M, Mazoni L, Coppelli A, Del PS. COVID-19 in people with diabetes: understanding the reasons for worse outcomes. Lancet Diabetes Endocrinol. 2020;8:782–92. 24. Lim S, Bae JH, Kwon HS, Nauck MA. COVID-19 and diabetes mellitus: from pathophysiology to clinical management. Nat Rev Endocrinol. 2020;17:11–30. 25. Phan F, Boussouar S, Lucidarme O, Zarai M, Salem J-E, Kachenoura N, et al. Cardiac adipose tissue volume and IL-6 level at admission are comple‑ mentary predictors of severity and short-term mortality in COVID-19 diabetic patients. Cardiovasc Diabetol. 2021;20:165. 26. Wang X, Fang X, Cai Z, Wu X, Gao X, Min J, et al. Comorbid chronic diseases and acute organ injuries are strongly correlated with disease severity and mortality among COVID-19 patients: a systemic review and meta-analysis. Research. 2020. https://​doi.​org/​10.​34133/​2020/​24029​61. 27. Lohia P, Kapur S, Benjaram S, Cantor Z, Mahabadi N, Mir T, et al. Statins and clinical outcomes in hospitalized COVID-19 patients with and with‑ out diabetes mellitus: a retrospective cohort study with propensity score matching. Cardiovasc Diabetol. 2021;20:140. 28. McGurnaghan SJ, Weir A, Bishop J, Kennedy S, Blackbourn LAK, McAllister DA, et al. Risks of and risk factors for COVID-19 disease in people with dia‑ betes: a cohort study of the total population of Scotland. Lancet Diabetes Endocrinol. 2021;9:82–93. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ lished maps and institutional affiliations. Ready to submit your research ? Choose BMC and benefit from: • fast, convenient online submission • thorough peer review by experienced researchers in your field • rapid publication on acceptance • support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations • maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions