Diabetic kidney disease phenotypes and the risk of cardiovascular events: The Silesia Diabetes-Heart Project | Cardiovascular Diabetology

  • International Diabetes Federation. IDF Diabetes Atlas, 11th edn. Brussels, Belgium: 2025. Available at: https://www.diabetesatlas.org.

  • Hill CJ, Cardwell CR, Patterson CC, et al. Chronic kidney disease and diabetes in the national health service: a cross-sectional survey of the U.K. national diabetes audit. Diabet Med. 2014;31(4):448–54. https://doi.org/10.1111/dme.12312.

    Article 
    CAS 

    Google Scholar 

  • Low Wang CC, Hess CN, Hiatt WR, Goldfine AB. Clinical update: cardiovascular disease in diabetes mellitus: atherosclerotic cardiovascular disease and heart failure in type 2 diabetes mellitus-mechanisms, management, and clinical considerations. Circulation. 2016;133(24):2459–502. https://doi.org/10.1161/CIRCULATIONAHA.116.022194.

    Article 
    CAS 

    Google Scholar 

  • Lawson CA, Seidu S, Zaccardi F, et al. Outcome trends in people with heart failure, type 2 diabetes mellitus and chronic kidney disease in the UK over twenty years. EClinicalMedicine. 2021;32:100739. https://doi.org/10.1016/j.eclinm.2021.100739.

    Article 

    Google Scholar 

  • Renard CB, Kramer F, Johansson F, et al. Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. J Clin Invest. 2004;114(5):659–68. https://doi.org/10.1172/JCI17867.

    Article 
    CAS 

    Google Scholar 

  • Ndumele CE, Neeland IJ, Tuttle KR, et al. A synopsis of the evidence for the science and clinical management of cardiovascular-kidney-metabolic (CKM) syndrome: a scientific statement from the American Heart Association. Circulation. 2023;148(20):1636–64. https://doi.org/10.1161/CIR.0000000000001186.

    Article 

    Google Scholar 

  • Eeg-Olofsson K, Cederholm J, Nilsson PM, et al. Risk of cardiovascular disease and mortality in overweight and obese patients with type 2 diabetes: an observational study in 13,087 patients. Diabetologia. 2009;52(1):65–73. https://doi.org/10.1007/s00125-008-1190-x.

    Article 
    CAS 

    Google Scholar 

  • Mogensen CE, Christensen CK, Vittinghus E. The stages in diabetic renal disease. With emphasis on the stage of incipient diabetic nephropathy. Diabetes. 1983;32(Suppl 2):64–78. https://doi.org/10.2337/diab.32.2.s64.

    Article 

    Google Scholar 

  • Thomas MC, Macisaac RJ, Jerums G, et al. Nonalbuminuric renal impairment in type 2 diabetic patients and in the general population (national evaluation of the frequency of renal impairment cO-existing with NIDDM [NEFRON] 11). Diabetes Care. 2009;32(8):1497–502. https://doi.org/10.2337/dc08-2186.

    Article 

    Google Scholar 

  • Vistisen D, Andersen GS, Hulman A, Persson F, Rossing P, Jørgensen ME. Progressive decline in estimated glomerular filtration rate in patients with diabetes after moderate loss in kidney function-even without albuminuria. Diabetes Care. 2019;42(10):1886–94. https://doi.org/10.2337/dc19-0349.

    Article 

    Google Scholar 

  • Krolewski AS, Niewczas MA, Skupien J, et al. Early progressive renal decline precedes the onset of microalbuminuria and its progression to macroalbuminuria. Diabetes Care. 2014;37(1):226–34. https://doi.org/10.2337/dc13-0985.

    Article 
    CAS 

    Google Scholar 

  • Penno G, Russo E, Garofolo M, et al. Evidence for two distinct phenotypes of chronic kidney disease in individuals with type 1 diabetes mellitus. Diabetologia. 2017;60(6):1102–13. https://doi.org/10.1007/s00125-017-4251-1.

    Article 
    CAS 

    Google Scholar 

  • Scirica BM, Mosenzon O, Bhatt DL, et al. Cardiovascular outcomes according to urinary albumin and kidney disease in patients with type 2 diabetes at high cardiovascular risk: observations from the SAVOR-TIMI 53 trial. JAMA Cardiol. 2018;3(2):155–63. https://doi.org/10.1001/jamacardio.2017.4228.

    Article 

    Google Scholar 

  • Sheng CS, Wang D, Yuan J, et al. CVD risk in non-albuminuric chronic kidney disease in hypertensive, non-diabetic subjects: a post-hoc analysis from SPRINT. Front Cardiovasc Med. 2022;9:977938. https://doi.org/10.3389/fcvm.2022.977938.

    Article 
    CAS 

    Google Scholar 

  • Kim YJ, Hwang SW, Lee T, Lee JY, Uh Y. Association between urinary albumin creatinine ratio and cardiovascular disease. PLoS ONE. 2023;18(3):e0283083. https://doi.org/10.1371/journal.pone.0283083.

    Article 
    CAS 

    Google Scholar 

  • Choi Y, Jacobs DR Jr, Shroff GR, Kramer H, Chang AR, Duprez DA. Progression of chronic kidney disease risk categories and risk of cardiovascular disease and total mortality: coronary artery risk development in young adults cohort. J Am Heart Assoc. 2022;11(21):e026685. https://doi.org/10.1161/JAHA.122.026685.

    Article 
    CAS 

    Google Scholar 

  • Yokoyama H, Araki SI, Kawai K, et al. The prognosis of patients with type 2 diabetes and nonalbuminuric diabetic kidney disease is not always poor: implication of the effects of coexisting macrovascular complications (JDDM 54). Diabetes Care. 2020;43(5):1102–10. https://doi.org/10.2337/dc19-2049.

    Article 
    CAS 

    Google Scholar 

  • Nabrdalik K, Kwiendacz H, Drożdż K, et al. Machine learning predicts cardiovascular events in patients with diabetes: the Silesia Diabetes-Heart project. Curr Probl Cardiol. 2023;48(7):101694. https://doi.org/10.1016/j.cpcardiol.2023.101694.

    Article 

    Google Scholar 

  • KDIGO 2024 Clinical practice guideline for the evaluation and management of chronic kidney disease [Internet]. Available from: www.kidney-international.org

  • Kofod DH, Carlson N, Ballegaard EF, et al. Cardiovascular mortality in patients with advanced chronic kidney disease with and without diabetes: a nationwide cohort study. Cardiovasc Diabetol. 2023;22(1):140. https://doi.org/10.1186/s12933-023-01867-8.

    Article 
    CAS 

    Google Scholar 

  • Chao CT, Lee SY, Wang J, Chien KL, Hung KY. The risk trajectory of different cardiovascular morbidities associated with chronic kidney disease among patients with newly diagnosed diabetes mellitus: a propensity score-matched cohort analysis. Cardiovasc Diabetol. 2021;20(1):86. https://doi.org/10.1186/s12933-021-01279-6.

    Article 
    CAS 

    Google Scholar 

  • Liu WC, Tomino Y, Lu KC. Impacts of indoxyl sulfate and p-cresol sulfate on chronic kidney disease and mitigating effects of AST-120. Toxins (Basel). 2018;10(9):367. https://doi.org/10.3390/toxins10090367.

    Article 
    CAS 

    Google Scholar 

  • Harlacher E, Wollenhaupt J, Baaten CCFMJ, Noels H. Impact of uremic toxins on endothelial dysfunction in chronic kidney disease: a systematic review. Int J Mol Sci. 2022;23(1):531. https://doi.org/10.3390/ijms23010531.

    Article 
    CAS 

    Google Scholar 

  • Cook S, Schmedt N, Broughton J, Kalra PA, Tomlinson LA, Quint JK. Characterising the burden of chronic kidney disease among people with type 2 diabetes in England: a cohort study using the clinical practice research datalink. BMJ Open. 2023;13(3):e065927. https://doi.org/10.1136/bmjopen-2022-065927.

    Article 

    Google Scholar 

  • Afkarian M, Katz R, Bansal N, et al. Diabetes, kidney disease, and cardiovascular outcomes in the Jackson Heart Study. Clin J Am Soc Nephrol. 2016;11(8):1384–91. https://doi.org/10.2215/CJN.13111215.

    Article 

    Google Scholar 

  • Scilletta S, Di Marco M, Miano N, et al. Update on diabetic kidney disease (DKD): focus on non-albuminuric DKD and cardiovascular risk. Biomolecules. 2023;13(5):752. https://doi.org/10.3390/biom13050752.

    Article 
    CAS 

    Google Scholar 

  • Ninomiya T, Perkovic V, de Galan BE, et al. Albuminuria and kidney function independently predict cardiovascular and renal outcomes in diabetes. J Am Soc Nephrol. 2009;20(8):1813–21. https://doi.org/10.1681/ASN.2008121270.

    Article 

    Google Scholar 

  • Svensson MK, Cederholm J, Eliasson B, Zethelius B, Gudbjörnsdottir S; Swedish National Diabetes Register. Albuminuria and renal function as predictors of cardiovascular events and mortality in a general population of patients with type 2 diabetes: a nationwide observational study from the Swedish National Diabetes Register. Diab Vasc Dis Res. 2013;10(6):520–9. https://doi.org/10.1177/14791641135007

  • Drury PL, Ting R, Zannino D, et al. Estimated glomerular filtration rate and albuminuria are independent predictors of cardiovascular events and death in type 2 diabetes mellitus: the Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study. Diabetologia. 2011;54(1):32–43. https://doi.org/10.1007/s00125-010-1854-1.

    Article 
    CAS 

    Google Scholar 

  • Penno G, Solini A, Orsi E, et al. Non-albuminuric renal impairment is a strong predictor of mortality in individuals with type 2 diabetes: the Renal Insufficiency and Cardiovascular Events (RIACE) Italian multicentre study. Diabetologia. 2018;61(11):2277–89. https://doi.org/10.1007/s00125-018-4691-2.

    Article 
    CAS 

    Google Scholar 

  • Di Marco M, Scilletta S, Miano N, et al. Cardiovascular risk and renal injury profile in subjects with type 2 diabetes and non-albuminuric diabetic kidney disease. Cardiovasc Diabetol. 2023;22(1):344. https://doi.org/10.1186/s12933-023-02065-2.

    Article 
    CAS 

    Google Scholar 

  • Kramer HJ, Nguyen QD, Curhan G, Hsu CY. Renal insufficiency in the absence of albuminuria and retinopathy among adults with type 2 diabetes mellitus. JAMA. 2003;289(24):3273–7. https://doi.org/10.1001/jama.289.24.3273.

    Article 

    Google Scholar 

  • Shi S, Ni L, Gao L, Wu X. Comparison of nonalbuminuric and albuminuric diabetic kidney disease among patients with type 2 diabetes: a systematic review and meta-analysis. Front Endocrinol (Lausanne). 2022;13:871272. https://doi.org/10.3389/fendo.2022.871272.

    Article 

    Google Scholar 

  • Gaede P, Tarnow L, Vedel P, Parving HH, Pedersen O. Remission to normoalbuminuria during multifactorial treatment preserves kidney function in patients with type 2 diabetes and microalbuminuria. Nephrol Dial Transpl. 2004;19(11):2784–8. https://doi.org/10.1093/ndt/gfh470.

    Article 

    Google Scholar 

  • de Zeeuw D, Remuzzi G, Parving HH, et al. Proteinuria, a target for renoprotection in patients with type 2 diabetic nephropathy: lessons from RENAAL. Kidney Int. 2004;65(6):2309–20. https://doi.org/10.1111/j.1523-1755.2004.00653.x.

    Article 

    Google Scholar 

  • Jin Q, Luk AO, Lau ESH, et al. Nonalbuminuric diabetic kidney disease and risk of all-cause mortality and cardiovascular and kidney outcomes in type 2 diabetes: findings from the Hong Kong Diabetes Biobank. Am J Kidney Dis. 2022;80(2):196-206.e1. https://doi.org/10.1053/j.ajkd.2021.11.011.

    Article 
    CAS 

    Google Scholar 

  • de Boer IH, Khunti K, Sadusky T, et al. Diabetes management in chronic kidney disease: a consensus report by the American Diabetes Association (ADA) and kidney disease: improving global outcomes (KDIGO). Diabetes Care. 2022;45(12):3075–90. https://doi.org/10.2337/dci22-0027.

    Article 
    CAS 

    Google Scholar 

  • Gæde P, Oellgaard J, Carstensen B, et al. Years of life gained by multifactorial intervention in patients with type 2 diabetes mellitus and microalbuminuria: 21 years follow-up on the Steno-2 randomised trial. Diabetologia. 2016;59(11):2298–307. https://doi.org/10.1007/s00125-016-4065-6.

    Article 
    CAS 

    Google Scholar 

  • Zinman B, Wanner C, Lachin JM, et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373(22):2117–28. https://doi.org/10.1056/NEJMoa1504720.

    Article 
    CAS 

    Google Scholar 

  • The EMPA-KIDNEY Collaborative Group, Herrington WG, Staplin N, et al. Empagliflozin in patients with chronic kidney disease. N Engl J Med. 2023;388(2):117–27. https://doi.org/10.1056/NEJMoa2204233.

    Article 

    Google Scholar 

  • Wiviott SD, Raz I, Bonaca MP, et al. Dapagliflozin and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2019;380(4):347–57. https://doi.org/10.1056/NEJMoa1812389.

    Article 
    CAS 

    Google Scholar 

  • Heerspink HJL, Stefánsson BV, Correa-Rotter R, et al. Dapagliflozin in patients with chronic kidney disease. N Engl J Med. 2020;383(15):1436–46. https://doi.org/10.1056/NEJMoa2024816.

    Article 
    CAS 

    Google Scholar 

  • KDIGO 2020 Clinical practice guideline for the evaluation and management of chronic kidney disease [Internet]. Available from: www.kidney-international.org.

  • KDIGO 2022 Clinical practice guideline for the evaluation and management of chronic kidney disease [Internet]. Available from: www.kidney-international.org.

  • Summary of Product Characteristics FARXIGA® (dapagliflozin) tablets, for oral use Initial U.S. Approval: 2014 [Internet]. Available from: https://www.fda.gov/drugsatfda.

  • Summary of Product Characteristics JARDIANCE® (empagliflozin) tablets, for oral use Initial U.S. Approval: 2014 [Internet]. Available from: https://www.fda.gov/drugsatfda.

  • Bhandari S, Mehta S, Khwaja A, et al. Renin-angiotensin system inhibition in advanced chronic kidney disease. N Engl J Med. 2022;387(22):2021–32. https://doi.org/10.1056/NEJMoa2210639.

    Article 
    CAS 

    Google Scholar 

  • Continue Reading