Endocrinol Metab.  2023 Apr;38(2):245-252. 10.3803/EnM.2023.1662.

Risk for Newly Diagnosed Type 2 Diabetes Mellitus after COVID-19 among Korean Adults: A Nationwide Matched Cohort Study

• Choi JH
• Kim KM
• Song K
• Seo GH

• KMID: 2541880
• DOI: http://doi.org/10.3803/EnM.2023.1662

Abstract

Background
Coronavirus disease 2019 (COVID-19) can cause various extrapulmonary sequelae, including diabetes. However, it is unclear whether these effects persist 30 days after diagnosis. Hence, we investigated the incidence of newly diagnosed type 2 diabetes mellitus (T2DM) in the post-acute phase of COVID-19.
Methods
This cohort study used data from the Health Insurance Review and Assessment Service, a representative national healthcare database in Korea. We established a cohort of 348,180 individuals diagnosed with COVID-19 without a history of diabetes between January 2020 and September 2021. The control group consisted of sex- and age-matched individuals with neither a history of diabetes nor COVID-19. We assessed the hazard ratios (HR) of newly diagnosed T2DM patients with COVID-19 compared to controls, adjusted for age, sex, and the presence of hypertension and dyslipidemia.
Results
In the post-acute phase, patients with COVID-19 had an increased risk of newly diagnosed T2DM compared to those without COVID-19 (adjusted HR, 1.30; 95% confidence interval [CI], 1.27 to 1.33). The adjusted HRs of non-hospitalized, hospitalized, and intensive care unit-admitted patients were 1.14 (95% CI, 1.08 to 1.19), 1.34 (95% CI, 1.30 to 1.38), and 1.78 (95% CI, 1.59 to 1.99), respectively. The risk of T2DM in patients who were not administered glucocorticoids also increased (adjusted HR, 1.29; 95% CI, 1.25 to 1.32).
Conclusion
COVID-19 may increase the risk of developing T2DM beyond the acute period. The higher the severity of COVID-19 in the acute phase, the higher the risk of newly diagnosed T2DM. Therefore, T2DM should be included as a component of managing long-term COVID-19.

Keyword

SARS-CoV-2; COVID-19; Post-acute COVID-19 syndrome; Diabetes mellitus, type 2

Figure

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  Fig. 1. Study flow for cohort selection and matched control. COVID-19, coronavirus disease 2019; COVID-19+, COVID-19 exposure group; COVID-19−, COVID-19 non-exposure control group; DM, diabetes mellitus; T2DM, type 2 diabetes mellitus.

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  Fig. 2. Kaplan-Meier curve for the cumulative incidence of newly diagnosed type 2 diabetes mellitus according to the status of coronavirus disease 2019 (COVID-19). COVID-19+, COVID-19 exposure group; COVID-19−, COVID-19 non-exposure control group.

Reference

1. Steenblock C, Schwarz PE, Ludwig B, Linkermann A, Zimmet P, Kulebyakin K, et al. COVID-19 and metabolic disease: mechanisms and clinical management. Lancet Diabetes Endocrinol. 2021; 9:786–98.

2. Garces CP, Oliveira E Silva L, Nunes SM, Cheik NC. Effects of social distancing caused by the COVID-19 pandemic on physical activity level, sitting time, and binge eating: a comparison between overweight/obese and normal-weight adults. Sport Sci Health. 2022; 18:1505–12.

3. Shao S, Yang Q, Pan R, Yu X, Chen Y. Interaction of severe acute respiratory syndrome coronavirus 2 and diabetes. Front Endocrinol (Lausanne). 2021; 12:731974.

4. RECOVERY Collaborative Group, Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, et al. Dexamethasone in hospitalized patients with Covid-19. N Engl J Med. 2021; 384:693–704.

5. Louis TJ, Qasem A, Abdelli LS, Naser SA. Extra-pulmonary complications in SARS-CoV-2 infection: a comprehensive multi organ-system review. Microorganisms. 2022; 10:153.

6. Cinek O, Slavenko M, Pomahacova R, Venhacova P, Petruzelkova L, Skvor J, et al. Type 1 diabetes incidence increased during the COVID-19 pandemic years 2020-2021 in Czechia: results from a large population-based pediatric register. Pediatr Diabetes. 2022; 23:956–60.

7. Mastromauro C, Blasetti A, Primavera M, Ceglie L, Mohn A, Chiarelli F, et al. Peculiar characteristics of new-onset type 1 diabetes during COVID-19 pandemic. Ital J Pediatr. 2022; 48:26.

8. Sathish T, Kapoor N, Cao Y, Tapp RJ, Zimmet P. Proportion of newly diagnosed diabetes in COVID-19 patients: a systematic review and meta-analysis. Diabetes Obes Metab. 2021; 23:870–4.

9. Montefusco L, Ben Nasr M, D’Addio F, Loretelli C, Rossi A, Pastore I, et al. Acute and long-term disruption of glycometabolic control after SARS-CoV-2 infection. Nat Metab. 2021; 3:774–85.

10. Barrett CE, Koyama AK, Alvarez P, Chow W, Lundeen EA, Perrine CG, et al. Risk for newly diagnosed diabetes >30 days after SARS-CoV-2 infection among persons aged <18 years: United States, March 1, 2020-June 28, 2021. MMWR Morb Mortal Wkly Rep. 2022; 71:59–65.

11. Xie Y, Al-Aly Z. Risks and burdens of incident diabetes in long COVID: a cohort study. Lancet Diabetes Endocrinol. 2022; 10:311–21.

12. Bull-Otterson L, Baca S, Saydah S, Boehmer TK, Adjei S, Gray S, et al. Post-COVID conditions among adult COVID-19 survivors aged 18–64 and ≥65 years: United States, March 2020-November 2021. MMWR Morb Mortal Wkly Rep. 2022; 71:713–7.

13. Rathmann W, Kuss O, Kostev K. Incidence of newly diagnosed diabetes after COVID-19. Diabetologia. 2022; 65:949–54.

14. Rezel-Potts E, Douiri A, Sun X, Chowienczyk PJ, Shah AM, Gulliford MC. Cardiometabolic outcomes up to 12 months after COVID-19 infection: a matched cohort study in the UK. PLoS Med. 2022; 19:e1004052.

15. Knebusch Toriello N, Prato Alterio NM, Ramirez Villeda LM. Newly diagnosed diabetes mellitus during COVID-19: the new pandemic: a literature review. Curr Trop Med Rep. 2022; 9:250–6.

16. Johns M, George S, Taburyanskaya M, Poon YK. A review of the evidence for corticosteroids in COVID-19. J Pharm Pract. 2022; 35:626–37.

17. Suh S, Park MK. Glucocorticoid-induced diabetes mellitus: an important but overlooked problem. Endocrinol Metab (Seoul). 2017; 32:180–9.

18. Ji W, Lee R, Huh K, Kang M, Hwang IC, Radnaabaatar M, et al. Overweight and obesity are risk factors for coronavirus disease 2019: a propensity score-matched case-control study. Endocrinol Metab (Seoul). 2021; 36:196–200.

19. You JH, Lee SA, Chun SY, Song SO, Lee BW, Kim DJ, et al. Clinical outcomes of COVID-19 patients with type 2 diabetes: a population-based study in Korea. Endocrinol Metab (Seoul). 2020; 35:901–8.

20. Ji W, Huh K, Kang M, Hong J, Bae GH, Lee R, et al. Effect of underlying comorbidities on the infection and severity of COVID-19 in Korea: a nationwide case-control study. J Korean Med Sci. 2020; 35:e237.

21. Tabak AG, Herder C, Rathmann W, Brunner EJ, Kivimaki M. Prediabetes: a high-risk state for diabetes development. Lancet. 2012; 379:2279–90.

22. Xie J, Wang M, Long Z, Ning H, Li J, Cao Y, et al. Global burden of type 2 diabetes in adolescents and young adults, 1990-2019: systematic analysis of the Global Burden of Disease Study 2019. BMJ. 2022; 379:e072385.

23. Gao M, Piernas C, Astbury NM, Hippisley-Cox J, O’Rahilly S, Aveyard P, et al. Associations between body-mass index and COVID-19 severity in 6.9 million people in England: a prospective, community-based, cohort study. Lancet Diabetes Endocrinol. 2021; 9:350–9.