Association of serum C-reactive protein (CRP) and D-dimer concentration on the severity of COVID-19 cases with or without diabetes: a systematic review and meta-analysis

References

• Phelan AL, Katz R, Gostin LO. The novel coronavirus originating in Wuhan, China: challenges for Global Health Governance. J Am Med Assoc. 2020;323:709–710.
   PubMed Web of Science ®Google Scholar
• Gralinski LE, Menachery VD. Return of the coronavirus: 2019-nCoV. Viruses. 2020;12:1–8.
   Web of Science ®Google Scholar
• Qu Y-M, Kang E-M, Cong H-Y. Positive result of Sars-Cov-2 in sputum from a cured patient with COVID-19. Travel Med Infect Dis. 2020;34:1–2.
   Web of Science ®Google Scholar
• World Health Organization. n.d. Director-General’s opening remarks at the media briefing on COVID-19-28 May, 2020.
   Google Scholar
• Rothan HA, Byrareddy SN. The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak. J Autoimmun. 2020;109:1–5.
   Web of Science ®Google Scholar
• Tan L, Kang X, Ji X, et al. Validation of predictors of disease severity and outcomes in COVID-19 patients: a descriptive and retrospective study. Med. 2020;1(1):128–138.
   Google Scholar
• Zheng Z, Peng F, Xu B, et al. Risk factors of critical & mortal COVID-19 cases: a systematic literature review and meta-analysis. J Infect. 2020;81:16–25.
   PubMed Web of Science ®Google Scholar
• De Vito A, Geremia N, Fiore V, et al. Clinical features, laboratory findings and predictors of death in hospitalized patients with COVID-19 in Sardinia, Italy. Eur Rev Med Pharmacol Sci. 2020;24:7861–7868.
   PubMed Web of Science ®Google Scholar
• Geremia N, De Vito A, Gunnella S, et al. A case of vasculitis-like skin eruption associated with COVID-19. Infect Dis Clin Pract. 2020;28:e30–1.
   Web of Science ®Google Scholar
• Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72314 cases from the Chinese Center for Disease Control and Prevention. JAMA J Am Med Assoc. 2020;2019. DOI:https://doi.org/10.1001/jama.2020.2648.
   Google Scholar
• De Vito A, Fiore V, Princic E, et al. Predictors of infection, symptoms development, and mortality in people with SARS-CoV-2 living in retirement nursing homes. PLoS One. 2021;16:1–14.
   Web of Science ®Google Scholar
• Fois AG, Paliogiannis P, Scano V, et al. The systemic inflammation index on admission predicts in-hospital mortality in COVID-19 patients. Molecules. 2020;25:1–13.
   Web of Science ®Google Scholar
• Ji P, Zhu J, Zhong Z, et al. Association of elevated inflammatory markers and severe COVID-19: a meta analysis. Medicine (Baltimore). 2020;99:1–12.
   Web of Science ®Google Scholar
• Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–506.
   PubMed Web of Science ®Google Scholar
• Ullah W, Thalambedu N, Haq S, et al. Predictability of CRP and D-Dimer levels for in-hospital outcomes and mortality of COVID-19. J Community Hosp Intern Med Perspect. 2020;10:402–408.
   PubMed Web of Science ®Google Scholar
• Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395:1054–1062.
   PubMed Web of Science ®Google Scholar
• Argenzian MG, Bruc SL, Slate CL, et al. Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series. BMJ. 2020;369:1–9.
   Google Scholar
• Onder G, Rezza G, Brusaferro S. Case-fatality rate and characteristics of patients dying in relation to COVID-19 in Italy. JAMA J Am Med Assoc. 2020;323:1775–1776.
   PubMed Web of Science ®Google Scholar
• Caussy C, Pattou F, Wallet F, et al. Prevalence of obesity among adult inpatients with COVID-19 in France. Lancet Diabetes Endocrinol. 2020;8:562–564.
   PubMed Web of Science ®Google Scholar
• Gao C, Cai Y, Zhang K, et al. Association of hypertension and antihypertensive treatment with COVID-19 mortality: a retrospective observational study. Eur Heart J. 2020;41:2058–2066.
   PubMed Web of Science ®Google Scholar
• Yamada T, Mikami T, Chopra N, et al. Patients with chronic kidney disease have a poorer prognosis of coronavirus disease 2019 (COVID-19): an experience in New York City. Int Urol Nephrol. 2020;52:1405–1406.
   PubMed Web of Science ®Google Scholar
• Guan W, Ni Z, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382:1708–1720.
   PubMed Web of Science ®Google Scholar
• Wang G, Wu C, Zhang Q, et al. C-reactive protein level may predict the risk of COVID-19 aggravation. Open Forum Infect Dis. 2020;7:1–5.
   Web of Science ®Google Scholar
• Marnell L, Mold C, Du Clos TW. C-reactive protein: ligands, receptors and role in inflammation. Clin Immunol. 2005;117:104–111.
   PubMed Web of Science ®Google Scholar
• Young B, Gleeson M, Cripps AW. C-reactive protein: a critical review. Pathology. 1991;23:118–124.
   PubMed Web of Science ®Google Scholar
• Mishra Y, Pathak BK, Mohakuda SS, et al. Relation of D-dimer levels of COVID-19 patients with diabetes mellitus. Diabetes Metab Syndr Clin Res Rev. 2020;14:1927–1930.
   PubMedGoogle Scholar
• Chan JF, Kok K, Zhu Z, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020;382:727–733.
   PubMed Web of Science ®Google Scholar
• Sardu C, D’Onofrio N, Balestrieri ML, et al. Outcomes in patients with hyperglycemia affected by COVID-19: can we do more on glycemic control? Diabetes Care. 2020;43:1408–1415.
   PubMed Web of Science ®Google Scholar
• Gavriatopoulou M, Ntanasis-Stathopoulos I, Korompoki E, et al. Emerging treatment strategies for COVID-19 infection. Clin Exp Med. 2021;21:167–179.
   PubMed Web of Science ®Google Scholar
• Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6. doi:https://doi.org/10.1371/journal.pmed.1000100.
   Web of Science ®Google Scholar
• Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hosp Res Inst. 2012. doi:https://doi.org/10.1007/s11250-018-1782-5.
   Google Scholar
• DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials. 2007;28:105–114.
   PubMed Web of Science ®Google Scholar
• Wan X, Wang W, Liu J, et al. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 2014;14:1–13.
   PubMed Web of Science ®Google Scholar
• Luo D, Wan X, Liu J, et al. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Stat Methods Med Res. 2018;27:1785–1805.
   PubMed Web of Science ®Google Scholar
• Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088.
   PubMed Web of Science ®Google Scholar
• Sterne JAEM, Egger M. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis Jonathan. J Clin Epidemiol. 2001;54:1046–1055.
   PubMed Web of Science ®Google Scholar
• Akbariqomi M, Hosseini MS, Rashidiani J, et al. Clinical characteristics and outcome of hospitalized COVID-19 patients with diabetes: a single-center, retrospective study in Iran. Diabetes Res Clin Pract. 2020;169:108467.
   PubMed Web of Science ®Google Scholar
• Alguwaihes AM, Al-Sofiani ME, Megdad M, et al. Diabetes and Covid-19 among hospitalized patients in Saudi Arabia: a single-centre retrospective study. Cardiovasc Diabetol. 2020;19:1–12.
   PubMedGoogle Scholar
• Al-Salameh A, Lanoix JP, Bennis Y, et al. Characteristics and outcomes of COVID-19 in hospitalized patients with and without diabetes. Diabetes Metab Res Rev. 2021;37:1–9.
   Web of Science ®Google Scholar
• Alshukry A, Bu Abbas M, Ali Y, et al. Clinical characteristics and outcomes of COVID-19 patients with diabetes mellitus in Kuwait. Heliyon. 2021;7(4):1–6.
   Web of Science ®Google Scholar
• Chen Y, Yang D, Cheng B, et al. Clinical characteristics and outcomes of patients with diabetes and COVID-19 in association with glucose-lowering medication. Diabetes Care. 2020;43:1399–1407.
   PubMed Web of Science ®Google Scholar
• Chen Y, Chen J, Gong X, et al. Clinical Characteristics and Outcomes of Type 2 Diabetes Patients Infected with COVID-19: a Retrospective Study. Engineering. 2020;6:1170–1177.
   Web of Science ®Google Scholar
• Cheng X, Xin S, Chen Y, et al. Effects of metformin, insulin on COVID-19 patients with pre-existed type 2 diabetes: a multicentral retrospective study. Life Sci. 2021;275:1–10.
   Web of Science ®Google Scholar
• Ciardullo S, Zerbini F, Perra S, et al. Impact of diabetes on COVID-19-related in-hospital mortality: a retrospective study from Northern Italy. J Endocrinol Invest. 2021;44:843–850.
   PubMed Web of Science ®Google Scholar
• Conway J, Gould A, Westley R, et al. Characteristics of patients with diabetes hospitalised for COVID-19 infection-a brief case series report. Diabetes Res Clin Pract. 2020;169:1–17.
   Web of Science ®Google Scholar
• Fadini GP, Morieri ML, Boscari F, et al. Newly-diagnosed diabetes and admission hyperglycemia predict COVID-19 severity by aggravating respiratory deterioration. Diabetes Res Clin Pract. 2020;168:1–9.
   Web of Science ®Google Scholar
• Fox T, Ruddiman K, Lo KB, et al. The relationship between diabetes and clinical outcomes in COVID-19: a single-center retrospective analysis. Acta Diabetol. 2021;58(1):33–38.
   PubMed Web of Science ®Google Scholar
• Guo W, Li M, Dong Y, et al. Diabetes is a risk factor for the progression and prognosis of COVID-19. Diabetes Metab Res Rev. 2020;36:1–9.
   Web of Science ®Google Scholar
• Koh H, Moh AMC, Yeoh E, et al. Diabetes predicts severity of COVID-19 infection in a retrospective cohort: a mediatory role of the inflammatory biomarker C-reactive protein. J Med Virol. 2021;93:3023–3032.
   PubMed Web of Science ®Google Scholar
• Jing Liang J, Liu J, Chen Y, et al. Characteristics of laboratory findings of COVID-19 patients with comorbid diabetes mellitus. Diabetes Res Clin Pract. 2020;167:1–5.
   Web of Science ®Google Scholar
• Liu Z, Bai X, Han X, et al. The association of diabetes and the prognosis of COVID-19 patients: a retrospective study. Diabetes Res Clin Pract. 2020;169:108386.
   PubMed Web of Science ®Google Scholar
• Mirani M, Favacchio G, Carrone F, et al. Impact of comorbidities and glycemia at admission and dipeptidyl peptidase 4 inhibitors in patients with type 2 diabetes with covid-19: a case series from an academic hospital in lombardy, Italy. Diabetes Care. 2020;43:3042–3049.
   PubMed Web of Science ®Google Scholar
• Orioli L, Servais T, Belkhir L, et al. Clinical characteristics and short-term prognosis of in-patients with diabetes and COVID-19: a retrospective study from an academic center in Belgium. Diabetes Metab Syndr Clin Res Rev. 2021;15:149–157.
   PubMed Web of Science ®Google Scholar
• Shang J, Wang Q, Zhang H, et al. The relationship between diabetes mellitus and COVID-19 prognosis: a retrospective cohort study in Wuhan, China. Am J Med. 2020;134:e6–14.
   PubMed Web of Science ®Google Scholar
• Shi Q, Zhang X, Jiang F, et al. Clinical characteristics and risk factors for mortality of COVID-19 patients with diabetes in Wuhan, China: a two-center, retrospective study. Diabetes Care. 2020;43:1382–1391.
   PubMed Web of Science ®Google Scholar
• Shrestha E, Charkviani M, Musurakis C, et al. Type 2 diabetes is associated with increased risk of critical respiratory illness in patients COVID-19 in a community hospital. Obes Med. 2021;22:1–6.
   Google Scholar
• Soliman A, Nair AP, Al Masalamani MS, et al. Prevalence, clinical manifestations, and biochemical data of type 2 diabetes mellitus versus nondiabetic symptomatic patients with COVID-19: a comparative study. Acta Biomed. 2020;91:1–9.
   Google Scholar
• Sun G, Zhang Y, Liao Q, et al. Blood test results of pregnant COVID-19 patients: an updated case-control study. Front Cell Infect Microbiol. 2020;10:1–6.
   PubMed Web of Science ®Google Scholar
• Sutter W, Duceau B, Vignac M, et al. Association of diabetes and outcomes in patients with COVID-19: propensity score-matched analyses from a French retrospective cohort. Diabetes Metab. 2021;47:1–8.
   Web of Science ®Google Scholar
• Tomar BS, Singh M, Nathiya D, et al. Prevalence of symptoms in patients discharged from COVID care facility of NIMS hospital: is RT PCR negativity truly reflecting recovery? A single-centre observational study. Int J Gen Med. 2021;14:1069–1078.
   PubMed Web of Science ®Google Scholar
• Wu J, Zhang J, Sun X, et al. Influence of diabetes mellitus on the severity and fatality of SARS-CoV-2 (COVID-19) infection. Diabetes Obes Metab. 2020;22:1907–1914.
   PubMed Web of Science ®Google Scholar
• Yan Y, Yang Y, Wang F, et al. Clinical characteristics and outcomes of patients with severe covid-19 with diabetes. BMJ Open Diabetes Res Care. 2020;8:1–9.
   Web of Science ®Google Scholar
• Zhang P, Wang M, Wang Y, et al. Risk factors associated with the progression of COVID-19 in elderly diabetes patients. Diabetes Res Clin Pract. 2021;171:1–10.
   Web of Science ®Google Scholar
• Zhou W, Ye S, Wang W, et al. Clinical features of COVID-19 patients with diabetes and secondary hyperglycemia. J Diabetes Res. 2020;2020:1–9.
   Web of Science ®Google Scholar
• Zhang Y, Cui Y, Shen M, et al. Association of diabetes mellitus with disease severity and prognosis in COVID-19: a retrospective cohort study. Diabetes Res Clin Pract. 2020;165:1–26.
   Web of Science ®Google Scholar
• Ali N. Elevated level of C-reactive protein may be an early marker to predict risk for severity of COVID-19. J Med Virol. 2020;92:2409–2411.
   PubMed Web of Science ®Google Scholar
• Zhang ZL, Hou YL, Li DT, et al. Laboratory findings of COVID-19: a systematic review and meta-analysis. Scand J Clin Lab Invest. 2020;80:441–447.
   PubMed Web of Science ®Google Scholar
• Saha S, Al-Rifai RH, Saha S. Diabetes prevalence and mortality in COVID-19 patients: a systematic review, meta‐analysis, and meta‐regression. J Diabetes Metab Disord. 2021;20:939–950.
   Web of Science ®Google Scholar
• Cariou B, Hadjadj S, Wargny M, et al. Phenotypic characteristics and prognosis of inpatients with COVID-19 and diabetes: the CORONADO study. Diabetologia. 2020;63:1500–1515.
   PubMed Web of Science ®Google Scholar
• Jang JG, Hur J, Choi EY, et al. Prognostic factors for severe coronavirus disease 2019 in Daegu, Korea. J Korean Med Sci. 2020;35:1–10.
   Web of Science ®Google Scholar
• Das S, Anu KR, Sr B, et al. Role of comorbidities like diabetes on severe acute respiratory syndrome coronavirus-2: a review. Life Sci. 2020;258:1–12.
   Web of Science ®Google Scholar
• Erener S. Diabetes, infection risk and COVID-19. Mol Metab. 2020;39:1–10.
   Web of Science ®Google Scholar
• De Vito A, Geremia N, Princic E, et al. Does Angiotensin II receptor blockers increase the risk of SARS-CoV-2 infection? A real-life experience. Eur Rev Med Pharmacol Sci. 2021;25:523–526.
   PubMed Web of Science ®Google Scholar
• Zhu L, She ZG, Cheng X, et al. Association of blood glucose control and outcomes in patients with COVID-19 and pre-existing Type 2 diabetes. Cell Metab. 2020;31:1068–1077.
   PubMed Web of Science ®Google Scholar
• Pipeleers L, Wissing KM, Hilbrands R. Acid-base and electrolyte disturbances in patients with diabetes mellitus. Acta Clin Belgica Int J Clin Lab Med. 2019;74:28–33.
   PubMed Web of Science ®Google Scholar
• Han H, Yang L, Liu R, et al. Prominent changes in blood coagulation of patients with SARS-CoV-2 infection. Clin Chem Lab Med. 2020;58:1116–1120.
   PubMed Web of Science ®Google Scholar
• Conte G, Cei M, Evangelista I, et al. The meaning of D-Dimer value in Covid-19. Clin Appl Thromb. 2021;27:1–2.
   Google Scholar
• Ali A, Mohamed SOO, Elkhidir I, et al. The Association of Lymphocyte count and levels of CRP, D-Dimer, and LDH with severe coronavirus disease 2019 (COVID-19): a meta-analysis. Sudan J Med Sci. 2020;9–19. doi:https://doi.org/10.1101/2020.04.20.20072801.
   Google Scholar
• Paliogiannis P, Mangoni AA, Dettori P, et al. D-dimer concentrations and covid-19 severity: a systematic review and meta-analysis. Front Public Health. 2020;8:1–7.
   PubMed Web of Science ®Google Scholar
• Tang N, Bai H, Chen X, et al. Anticoagulant treatment is associated with decreased mortality in severe coronavirus disease 2019 patients with coagulopathy. J Thromb Haemost. 2020;18:1094–1099.
   PubMed Web of Science ®Google Scholar
• Barek MA, Aziz MA, Islam MS. Impact of age, sex, comorbidities and clinical symptoms on the severity of COVID-19 cases: a meta-analysis with 55 studies and 10014 cases. Heliyon. 2020;6:1–25.
   Web of Science ®Google Scholar
• de la Vega R, Ruíz-Barquín R, Boros S, et al. Could attitudes toward COVID-19 in Spain render men more vulnerable than women? Glob Public Health. 2020;15:1278–1291.
   PubMed Web of Science ®Google Scholar
• Conti P, Younes A. Coronavirus cov-19/sars-cov-2 affects women less than men: clinical response to viral infection. J Biol Regul Homeost Agents. 2020;34:339–343.
   PubMed Web of Science ®Google Scholar
• Qu G, Huang G, Zhang M, et al. Features of C-reactive protein in COVID-19 patients with different ages, clinical types and outcomes: a cohort study Gaojing. MedRxiv. 2020;49:1–21.
   Google Scholar
• Zhao R, Su Z, Komissarov AA, et al. Associations of D-Dimer on admission and clinical features of COVID-19 patients: a systematic review, meta-analysis, and meta-regression. Front Immunol. 2021;12:1–12.
   Web of Science ®Google Scholar
• Tini G, Duso BA, Bellerba F, et al. Semantic and geographical analysis of COVID-19 trials reveals a fragmented clinical research landscape likely to impair informativeness. Front Med. 2020;7:1–7.
   Web of Science ®Google Scholar