Endocrinol Metab.  2016 Dec;31(4):577-585. 10.3803/EnM.2016.31.4.577.

Prevalent Rate of Nonalbuminuric Renal Insufficiency and Its Association with Cardiovascular Disease Event in Korean Type 2 Diabetes

Affiliations
  • 1Department of Internal Medicine, Pusan National University School of Medicine and Diabetes Center, Pusan National University Yangsan Hospital, Yangsan, Korea. sonsm@pusan.ac.kr

Abstract

BACKGROUND
Nonalbuminuric renal insufficiency is a unique category of diabetic kidney diseases. The objectives of the study were to evaluate prevalent rate of nonalbuminuric renal insufficiency and to investigate its relationship with previous cardiovascular disease (CVD) event in Korean patients with type 2 diabetes mellitus (T2DM).
METHODS
Laboratory and clinical data of 1,067 subjects with T2DM were obtained and reviewed. Study subjects were allocated into four subgroups according to the CKD classification. Major CVD events were included with coronary, cerebrovascular, and peripheral vascular events.
RESULTS
Nonalbuminuric stage ≥3 CKD group, when compared with albuminuric stage ≥3 CKD group, had shorter diabetic duration, lower concentrations of glycated hemoglobin, high density lipoprotein cholesterol, and high-sensitivity C-reactive protein, lower prevalent rates of retinopathy and previous CVD, and higher rate of treatment with angiotensin-converting enzyme inhibitors/angiotensin II receptor blockers. Nonalbuminuric stage ≥3 CKD group showed a greater association with prior CVD events than no CKD group; however, albuminuric stage ≥3 CKD group made addition to increase prevalence of prior CVD events significantly when CKD categories were applied as covariates. Association of prior CVD events, when compared with normal estimated glomerular filtration rate (eGFR) and nonalbuminuria categories, became significant for declined eGFR, which was higher for eGFR of <30 mL/min/1.73 m², and albuminuria.
CONCLUSION
The results show that subjects with nonalbuminuric stage ≥3 CKD is significantly interrelated with occurrence of prior CVD events than those with normal eGFR with or without albuminuria. Comparing with normal eGFR and nonalbuminuria categories, the combination of increased degree of albuminuria and declined eGFR is becoming significant for the association of prior CVD events.

Keyword

Nonalbuminuric renal insufficiency; Diabetes mellitus; Cardiovascular diseases

MeSH Terms

Albuminuria
C-Reactive Protein
Cardiovascular Diseases*
Cholesterol, HDL
Classification
Diabetes Mellitus
Diabetes Mellitus, Type 2
Diabetic Nephropathies
Glomerular Filtration Rate
Hemoglobin A, Glycosylated
Humans
Prevalence
Renal Insufficiency*
C-Reactive Protein
Cholesterol, HDL

Figure

  • Fig. 1 Prevalence of non-, micro-, and macroalbuminuria according to classes of estimated glomerular filtration rate (eGFR) by the Modification of Diet in Renal Disease (MDRD) study and the Chronic Kidney Disease-Epidemiology Collaboration (CKD-EPI) formulas.

  • Fig. 2 Prevalence of (A) previous cardiovascular disease (CVD) and (B) retinopathy according to degree of albuminuria and classes of estimated glomerular filtration rate (eGFR) by the Modification of Diet in Renal Disease study equation.


Cited by  1 articles

Soluble Dipeptidyl Peptidase-4 Levels Are Associated with Decreased Renal Function in Patients with Type 2 Diabetes Mellitus
Eun-Hee Cho, Sang-Wook Kim
Diabetes Metab J. 2019;43(1):97-104.    doi: 10.4093/dmj.2018.0030.


Reference

1. Huxley R, Barzi F, Woodward M. Excess risk of fatal coronary heart disease associated with diabetes in men and women: meta-analysis of 37 prospective cohort studies. BMJ. 2006; 332:73–78.
2. Brancati FL, Whelton PK, Randall BL, Neaton JD, Stamler J, Klag MJ. Risk of end-stage renal disease in diabetes mellitus: a prospective cohort study of men screened for MRFIT. Multiple Risk Factor Intervention Trial. JAMA. 1997; 278:2069–2074.
3. Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, et al. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001; 286:421–426.
4. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004; 351:1296–1305.
5. Anavekar NS, Gans DJ, Berl T, Rohde RD, Cooper W, Bhaumik A, et al. Predictors of cardiovascular events in patients with type 2 diabetic nephropathy and hypertension: a case for albuminuria. Kidney Int Suppl. 2004; 92:S50–S55.
6. Soveri I, Arnlov J, Berglund L, Lind L, Fellstrom B, Sundstrom J. Kidney function and discrimination of cardiovascular risk in middle-aged men. J Intern Med. 2009; 266:406–413.
7. Thomas MC, Weekes AJ, Broadley OJ, Cooper ME, Mathew TH. The burden of chronic kidney disease in Australian patients with type 2 diabetes (the NEFRON study). Med J Aust. 2006; 185:140–144.
8. Thomas MC, Macisaac RJ, Jerums G, Weekes A, Moran J, Shaw JE, 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; 32:1497–1502.
9. Afghahi H, Cederholm J, Eliasson B, Zethelius B, Gudbjornsdottir S, Hadimeri H, et al. Risk factors for the development of albuminuria and renal impairment in type 2 diabetes: the Swedish National Diabetes Register (NDR). Nephrol Dial Transplant. 2011; 26:1236–1243.
10. Ninomiya T, Perkovic V, de Galan BE, Zoungas S, Pillai A, Jardine M, et al. Albuminuria and kidney function independently predict cardiovascular and renal outcomes in diabetes. J Am Soc Nephrol. 2009; 20:1813–1821.
11. Drury PL, Ting R, Zannino D, Ehnholm C, Flack J, Whiting M, 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; 54:32–43.
12. Lane PH, Steffes MW, Mauer SM. Glomerular structure in IDDM women with low glomerular filtration rate and normal urinary albumin excretion. Diabetes. 1992; 41:581–586.
13. Tsalamandris C, Allen TJ, Gilbert RE, Sinha A, Panagiotopoulos S, Cooper ME, et al. Progressive decline in renal function in diabetic patients with and without albuminuria. Diabetes. 1994; 43:649–655.
14. Chronic Kidney Disease Prognosis Consortium. Matsushita K, van der Velde M, Astor BC, Woodward M, Levey AS, et al. Association of estimated glomerular filtration rate and albuminuria with all-cause and cardiovascular mortality in general population cohorts: a collaborative meta-analysis. Lancet. 2010; 375:2073–2081.
15. Bruno G, Merletti F, Bargero G, Novelli G, Melis D, Soddu A, et al. Estimated glomerular filtration rate, albuminuria and mortality in type 2 diabetes: the Casale Monferrato study. Diabetologia. 2007; 50:941–948.
16. Penno G, Solini A, Bonora E, Fondelli C, Orsi E, Zerbini G, et al. Clinical significance of nonalbuminuric renal impairment in type 2 diabetes. J Hypertens. 2011; 29:1802–1809.
17. Solini A, Penno G, Bonora E, Fondelli C, Orsi E, Arosio M, et al. Diverging association of reduced glomerular filtration rate and albuminuria with coronary and noncoronary events in patients with type 2 diabetes: the renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care. 2012; 35:143–149.
18. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med. 1999; 130:461–470.
19. Levey AS, Coresh J, Balk E, Kausz AT, Levin A, Steffes MW, et al. National Kidney Foundation practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Ann Intern Med. 2003; 139:137–147.
20. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009; 150:604–612.
21. Hostetter TH. Prevention of the development and progression of renal disease. J Am Soc Nephrol. 2003; 14:7 Suppl 2. S144–S147.
22. Heerspink HJ, Holtkamp FA, de Zeeuw D, Ravid M. Monitoring kidney function and albuminuria in patients with diabetes. Diabetes Care. 2011; 34:Suppl 2. S325–S329.
23. de Zeeuw D, Remuzzi G, Parving HH, Keane WF, Zhang Z, Shahinfar S, et al. Proteinuria, a target for renoprotection in patients with type 2 diabetic nephropathy: lessons from RENAAL. Kidney Int. 2004; 65:2309–2320.
24. Rowe DJ, Dawnay A, Watts GF. Microalbuminuria in diabetes mellitus: review and recommendations for the measurement of albumin in urine. Ann Clin Biochem. 1990; 27(Pt 4):297–312.
25. Croal BL, Mutch WJ, Clark BM, Dickie A, Church J, Noble D, et al. The clinical application of a urine albumin: creatinine ratio point-of-care device. Clin Chim Acta. 2001; 307:15–21.
26. Marshall SM. Screening for microalbuminuria: which measurement? Diabet Med. 1991; 8:706–711.
27. Rychlik I, Jancova E, Tesar V, Kolsky A, Lacha J, Stejskal J, et al. The Czech registry of renal biopsies. Occurrence of renal diseases in the years 1994-2000. Nephrol Dial Transplant. 2004; 19:3040–3049.
28. Matsushita K, Mahmoodi BK, Woodward M, Emberson JR, Jafar TH, Jee SH, et al. Comparison of risk prediction using the CKD-EPI equation and the MDRD study equation for estimated glomerular filtration rate. JAMA. 2012; 307:1941–1951.
29. 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; 289:3273–3277.
30. MacIsaac RJ, Panagiotopoulos S, McNeil KJ, Smith TJ, Tsalamandris C, Hao H, et al. Is nonalbuminuric renal insufficiency in type 2 diabetes related to an increase in intrarenal vascular disease? Diabetes Care. 2006; 29:1560–1566.
31. Rigalleau V, Lasseur C, Raffaitin C, Beauvieux MC, Barthe N, Chauveau P, et al. Normoalbuminuric renal-insufficient diabetic patients: a lower-risk group. Diabetes Care. 2007; 30:2034–2039.
32. Futrakul N, Sridama V, Futrakul P. Microalbuminuria: a biomarker of renal microvascular disease. Ren Fail. 2009; 31:140–143.
33. Fioretto P, Mauer M, Brocco E, Velussi M, Frigato F, Muollo B, et al. Patterns of renal injury in NIDDM patients with microalbuminuria. Diabetologia. 1996; 39:1569–1576.
34. Taniwaki H, Nishizawa Y, Kawagishi T, Ishimura E, Emoto M, Okamura T, et al. Decrease in glomerular filtration rate in Japanese patients with type 2 diabetes is linked to atherosclerosis. Diabetes Care. 1998; 21:1848–1855.
Full Text Links
  • ENM
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