Diabetes Metab J.  2020 Aug;44(4):602-613. 10.4093/dmj.2020.0146.

The Clinical Characteristics and Outcomes of Patients with Moderate-to-Severe Coronavirus Disease 2019 Infection and Diabetes in Daegu, South Korea

Affiliations
  • 1Department of Internal Medicine, Keimyung University Dongsan Hospital, Keimyung University School of Medicine, Daegu, Korea.
  • 2Department of Internal Medicine, Kyungpook National University Chilgok Hospital, School of Medicine, Kyungpook National University, Daegu, Korea.
  • 3Department of Internal Medicine, Daegu Catholic University Hospital, Daegu Catholic University School of Medicine, Daegu, Korea.
  • 4Department of Internal Medicine, Yeungnam University Hospital, Yeungnam University College of Medicine, Daegu, Korea.
  • 5Department of Internal Medicine, Kyungpook National University Hospital, School of Medicine, Kyungpook National University, Daegu, Korea.

Abstract

Background

Coronavirus disease 2019 (COVID-19) is a global pandemic that had affected more than eight million people worldwide by June 2020. Given the importance of the presence of diabetes mellitus (DM) for host immunity, we retrospectively evaluated the clinical characteristics and outcomes of moderate-to-severe COVID-19 in patients with diabetes.

Methods

We conducted a multi-center observational study of 1,082 adult inpatients (aged ≥18 years) who were admitted to one of five university hospitals in Daegu because of the severity of their COVID-19-related disease. The demographic, laboratory, and radiologic findings, and the mortality, prevalence of severe disease, and duration of quarantine were compared between patients with and without DM. In addition, 1:1 propensity score (PS)-matching was conducted with the DM group.

Results

Compared with the non-DM group (n=847), patients with DM (n=235) were older, exhibited higher mortality, and required more intensive care. Even after PS-matching, patients with DM exhibited more severe disease, and DM remained a prognostic factor for higher mortality (hazard ratio, 2.40; 95% confidence interval, 1.38 to 4.15). Subgroup analysis revealed that the presence of DM was associated with higher mortality, especially in older people (≥70 years old). Prior use of a dipeptidyl peptidase-4 inhibitor or a renin-angiotensin system inhibitor did not affect mortality or the clinical severity of the disease.

Conclusion

DM is a significant risk factor for COVID-19 severity and mortality. Our findings imply that COVID-19 patients with DM, especially if elderly, require special attention and prompt intensive care.


Keyword

COVID-19; Diabetes mellitus; Mortality; Prognosis

Figure

  • Fig. 1 Flow chart of the study. COVID-19, coronavirus disease 2019; KNUH, Kyungpook National University Hospital; DSMC, Dongsan Medical Center; KNUCH, Kyungpook National University Chilgok Hospital; DCMC, Daegu Catholic Medical Center; PCR, polymerase chain reaction; DM, diabetes mellitus; PS, propensity score.

  • Fig. 2 Mortality due to coronavirus disease 2019 in all patients (A) and propensity score-matched patients (B). The data were analyzed using the Kaplan-Meier method, and hazard ratios were calculated using a Cox proportional hazards model. Data are expressed as hazard ratio (HR) (95% confidence intervals [CI]). DM, diabetes mellitus

  • Fig. 3 Mortality of coronavirus disease 2019 patients in subgroups defined according to age and sex. Patients aged <70 years (A) and >70 years (B); and male (C) and female (D) patients. Data were analyzed using a Cox proportional hazards model. Data are expressed as hazard ratio (HR) (95% confidence intervals [CI]). The model was adjusted for age, sex, and the presence of underlying diseases.


Cited by  6 articles

Independent Impact of Diabetes on the Severity of Coronavirus Disease 2019 in 5,307 Patients in South Korea: A Nationwide Cohort Study (Diabetes Metab J 2020;44:737–46)
Sun Joon Moon, Eun-Jung Rhee, Won-Young Lee, Kun-Ho Yoon
Diabetes Metab J. 2020;44(6):942-943.    doi: 10.4093/dmj.2020.0266.

Dipeptidyl Peptidase 4 Inhibitor, an Update
Ju Hee Lee
J Korean Diabetes. 2021;22(2):91-96.    doi: 10.4093/jkd.2021.22.2.91.

Glucose-Lowering Agents and COVID-19
Ah Reum Khang
J Korean Diabetes. 2022;23(1):1-6.    doi: 10.4093/jkd.2022.23.1.1.

Clinical Outcomes of COVID-19 Patients with Type 2 Diabetes: A Population-Based Study in Korea
Ji Hong You, Sang Ah Lee, Sung-Youn Chun, Sun Ok Song, Byung-Wan Lee, Dae Jung Kim, Edward J. Boyko
Endocrinol Metab. 2020;35(4):901-908.    doi: 10.3803/EnM.2020.787.

High Fibrosis-4 Index Is Related with Worse Clinical Outcome in Patients with Coronavirus Disease 2019 and Diabetes Mellitus: A Multicenter Observational Study
Sung-Woo Kim, Jae-Han Jeon, Jun Sung Moon, Mi Kyung Kim
Endocrinol Metab. 2021;36(4):800-809.    doi: 10.3803/EnM.2021.1040.

COVID-19 Vaccination for Endocrine Patients: A Position Statement from the Korean Endocrine Society
Cheol Ryong Ku, Kyong Yeun Jung, Chang Ho Ahn, Jun Sung Moon, Ju Hee Lee, Eun Heui Kim, Hyemi Kwon, Hee Kyung Kim, Sunghwan Suh, Sangmo Hong, Jeonghoon Ha, Eun Roh, Jin Hwa Kim, Mi-kyung Kim
Endocrinol Metab. 2021;36(4):757-765.    doi: 10.3803/EnM.2021.404.


Reference

1. COVID-19 National Emergency Response Center. Epidemiology and Case Management Team. Korea Centers for Disease Control and Prevention. Coronavirus disease-19: summary of 2,370 contact investigations of the first 30 cases in the Republic of Korea. Osong Public Health Res Perspect. 2020; 11:81–84. PMID: 32257773.
2. COVID-19 National Emergency Response Center. Epidemiology and Case Management Team. Korea Centers for Disease Control and Prevention. Coronavirus disease-19: the first 7,755 cases in the Republic of Korea. Osong Public Health Res Perspect. 2020; 11:85–90. PMID: 32257774.
3. Kim SW, Lee KS, Kim K, Lee JJ, Kim JY. Daegu Medical Association. A brief telephone severity scoring system and therapeutic living centers solved acute hospital-bed shortage during the COVID-19 outbreak in Daegu, Korea. J Korean Med Sci. 2020; 35:e152. PMID: 32301298.
Article
4. Jafar N, Edriss H, Nugent K. The effect of short-term hyperglycemia on the innate immune system. Am J Med Sci. 2016; 351:201–211. PMID: 26897277.
Article
5. Turina M, Fry DE, Polk HC Jr. Acute hyperglycemia and the innate immune system: clinical, cellular, and molecular aspects. Crit Care Med. 2005; 33:1624–1633. PMID: 16003073.
Article
6. Cristelo C, Azevedo C, Marques JM, Nunes R, Sarmento B. SARS-CoV-2 and diabetes: new challenges for the disease. Diabetes Res Clin Pract. 2020; 164:108228. PMID: 32446801.
Article
7. Memish ZA, Perlman S, Van Kerkhove MD, Zumla A. Middle East respiratory syndrome. Lancet. 2020; 395:1063–1077. PMID: 32145185.
Article
8. Guan WJ, Liang WH, Zhao Y, Liang HR, Chen ZS, Li YM, Liu XQ, Chen RC, Tang CL, Wang T, Ou CQ, Li L, Chen PY, Sang L, Wang W, Li JF, Li CC, Ou LM, Cheng B, Xiong S, Ni ZY, Xiang J, Hu Y, Liu L, Shan H, Lei CL, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Cheng LL, Ye F, Li SY, Zheng JP, Zhang NF, Zhong NS, He JX. China Medical Treatment Expert Group for COVID-19. Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis. Eur Respir J. 2020; 55:2000547. PMID: 32217650.
Article
9. Kumar A, Arora A, Sharma P, Anikhindi SA, Bansal N, Singla V, Khare S, Srivastava A. Is diabetes mellitus associated with mortality and severity of COVID-19?: a meta-analysis. Diabetes Metab Syndr. 2020; 14:535–545. PMID: 32408118.
Article
10. Guo W, Li M, Dong Y, Zhou H, Zhang Z, Tian C, Qin R, Wang H, Shen Y, Du K, Zhao L, Fan H, Luo S, Hu D. Diabetes is a risk factor for the progression and prognosis of COVID-19. Diabetes Metab Res Rev. 2020; 3. 31. DOI: 10.1002/dmrr.3319. [Epub].
11. Docherty AB, Harrison EM, Green CA, Hardwick HE, Pius R, Norman L, Holden KA, Read JM, Dondelinger F, Carson G, Merson L, Lee J, Plotkin D, Sigfrid L, Halpin S, Jackson C, Gamble C, Horby PW, Nguyen-Van-Tam JS, Ho A, Russell CD, Dunning J, Openshaw PJ, Baillie JK, Semple MG. ISARIC4C investigators. Features of 20 133 UK patients in hospital with COVID-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study. BMJ. 2020; 369:m1985. PMID: 32444460.
12. Kim MK, Ko SH, Kim BY, Kang ES, Noh J, Kim SK, Park SO, Hur KY, Chon S, Moon MK, Kim NH, Kim SY, Rhee SY, Lee KW, Kim JH, Rhee EJ, Chun S, Yu SH, Kim DJ, Kwon HS, Park KS. Committee of Clinical Practice Guidelines, Korean Diabetes Association. 2019 Clinical practice guidelines for type 2 diabetes mellitus in Korea. Diabetes Metab J. 2019; 43:398–406. PMID: 31441247.
Article
13. Ministry of Health and Welfare. Central Disaster Management Headquarters. cited 2020 Jul 8. Available from: http://ncov.mohw.go.kr.
14. Hoffmann M, Kleine-Weber H, Pohlmann S. A multibasic cleavage site in the spike protein of SARS-CoV-2 is essential for infection of human lung cells. Mol Cell. 2020; 78:779–784. PMID: 32362314.
Article
15. Raj VS, Mou H, Smits SL, Dekkers DH, Muller MA, Dijkman R, Muth D, Demmers JA, Zaki A, Fouchier RA, Thiel V, Drosten C, Rottier PJ, Osterhaus AD, Bosch BJ, Haagmans BL. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature. 2013; 495:251–254. PMID: 23486063.
Article
16. Bornstein SR, Rubino F, Khunti K, Mingrone G, Hopkins D, Birkenfeld AL, Boehm B, Amiel S, Holt RI, Skyler JS, DeVries JH, Renard E, Eckel RH, Zimmet P, Alberti KG, Vidal J, Geloneze B, Chan JC, Ji L, Ludwig B. Practical recommendations for the management of diabetes in patients with COVID-19. Lancet Diabetes Endocrinol. 2020; 8:546–550. PMID: 32334646.
Article
17. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei CL, Hui DSC, Du B, Li LJ, Zeng G, Yuen KY, Chen RC, Tang CL, Wang T, Chen PY, Xiang J, Li SY, Wang JL, Liang ZJ, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Zhong NS. China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020; 382:1708–1720. PMID: 32109013.
18. Zhu L, She ZG, Cheng X, Qin JJ, Zhang XJ, Cai J, Lei F, Wang H, Xie J, Wang W, Li H, Zhang P, Song X, Chen X, Xiang M, Zhang C, Bai L, Xiang D, Chen MM, Liu Y, Yan Y, Liu M, Mao W, Zou J, Liu L, Chen G, Luo P, Xiao B, Zhang C, Zhang Z, Lu Z, Wang J, Lu H, Xia X, Wang D, Liao X, Peng G, Ye P, Yang J, Yuan Y, Huang X, Guo J, Zhang BH, Li H. Association of blood glucose control and outcomes in patients with COVID-19 and pre-existing type 2 diabetes. Cell Metab. 2020; 31:1068–1077. PMID: 32369736.
Article
19. Korean Society of Infectious Diseases. Korean Society of Pediatric Infectious Diseases. Korean Society of Epidemiology. Korean Society for Antimicrobial Therapy. Korean Society for Healthcare-associated Infection Control and Prevention. Korea Centers for Disease Control and Prevention. Report on the epidemiological features of coronavirus disease 2019 (COVID-19) outbreak in the Republic of Korea from January 19 to March 2, 2020. J Korean Med Sci. 2020; 35:e112. PMID: 32174069.
20. Katulanda P, Dissanayake HA, Ranathunga I, Ratnasamy V, Wijewickrama PSA, Yogendranathan N, Gamage KKK, de Silva NL, Sumanatilleke M, Somasundaram NP, Matthews DR. Prevention and management of COVID-19 among patients with diabetes: an appraisal of the literature. Diabetologia. 2020; 63:1440–1452. PMID: 32405783.
Article
21. Chung SM, Lee YY, Ha E, Yoon JS, Won KC, Lee HW, Hur J, Hong KS, Jang JG, Jin HJ, Choi EY, Shin KC, Chung JH, Lee KH, Ahn JH, Moon JS. The risk of diabetes on clinical outcomes in patients with coronavirus disease 2019: a retrospective cohort study. Diabetes Metab J. 2020; 44:405–413. PMID: 32602272.
Article
22. Cariou B, Hadjadj S, Wargny M, Pichelin M, Al-Salameh A, Allix I, Amadou C, Arnault G, Baudoux F, Bauduceau B, Borot S, Bourgeon-Ghittori M, Bourron O, Boutoille D, Cazenave-Roblot F, Chaumeil C, Cosson E, Coudol S, Darmon P, Disse E, Ducet-Boiffard A, Gaborit B, Joubert M, Kerlan V, Laviolle B, Marchand L, Meyer L, Potier L, Prevost G, Riveline JP, Robert R, Saulnier PJ, Sultan A, Thebaut JF, Thivolet C, Tramunt B, Vatier C, Roussel R, Gautier JF, Gourdy P. CORONADO investigators. Phenotypic characteristics and prognosis of inpatients with COVID-19 and diabetes: the CORONADO study. Diabetologia. 2020; 63:1500–1515. PMID: 32472191.
Article
23. Fadini GP, Morieri ML, Longato E, Bonora BM, Pinelli S, Selmin E, Voltan G, Falaguasta D, Tresso S, Costantini G, Sparacino G, Di Camillo B, Tramontan L, Cattelan AM, Vianello A, Fioretto P, Vettor R, Avogaro A. Exposure to dipeptidyl-peptidase-4 inhibitors and COVID-19 among people with type 2 diabetes: a case-control study. Diabetes Obes Metab. 2020; 5. 28. DOI: 10.1111/dom.14097. [Epub].
24. Bassendine MF, Bridge SH, McCaughan GW, Gorrell MD. COVID-19 and comorbidities: a role for dipeptidyl peptidase 4 (DPP4) in disease severity? J Diabetes. 2020; 12:649–658. PMID: 32394639.
Article
25. Brufsky A. Hyperglycemia, hydroxychloroquine, and the COVID-19 pandemic. J Med Virol. 2020; 92:770–775. PMID: 32293710.
Article
26. Ursini F, Ciaffi J, Landini MP, Meliconi R. COVID-19 and diabetes: is metformin a friend or foe? Diabetes Res Clin Pract. 2020; 164:108167. PMID: 32339534.
Article
27. Luo P, Qiu L, Liu Y, Liu XL, Zheng JL, Xue HY, Liu WH, Liu D, Li J. Metformin treatment was associated with decreased mortality in COVID-19 patients with diabetes in a retrospective analysis. Am J Trop Med Hyg. 2020; 103:69–72. PMID: 32446312.
Article
28. Chatterjee S. SGLT-2 inhibitors for COVID-19: a miracle waiting to happen or just another beat around the bush? Prim Care Diabetes. 2020; 5. 28. DOI: 10.1016/j.pcd.2020.05.013. [Epub].
29. Pal R, Bhadada SK. Should anti-diabetic medications be reconsidered amid COVID-19 pandemic? Diabetes Res Clin Pract. 2020; 163:108146. PMID: 32283128.
Article
Full Text Links
  • DMJ
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr