Strengthening the understanding of normoalbuminuric diabetic kidney disease

doi:10.3877/cma.j.issn.2095-3216.2016.04.001

Abstract

Abstract:

Diabetic kidney disease (DKD) is a primary cause for end-stage renal disease (ESRD). Early diagnosis is very important for preventing the progression of DKD. Assessment of urinary albumin excretion rate (UAER) played a key role in the diagnosis and clinical stages of patients with DKD. Actually, many diabetic mellitus (DM) patients sometimes showed nonalbuminuric renal insufficiency, which was named normoalbuminuric diabetic kidney disease (NADKD), nonalbuminuric diabetic nephropathy, or nonalbuminuric renal impairment in diabetes. In this article, the authors discussed NADKD in epidemiology, pathology, clinical features, diagnosis and treatment, etc, hoping to attract attention from colleagues in nephrology.

Key words: Diabetes, Diabetic kidney disease, Normoalbuminuria, Renal insufficiency

Lin Sun, Chao Chen. Strengthening the understanding of normoalbuminuric diabetic kidney disease[J]. Chinese Journal of Kidney Disease Investigation(Electronic Edition), 2016, 05(04): 145-151.

/ / Recommend

Add to citation manager EndNote|Ris|BibTeX

URL: https://zhsbyjdzzz.cma-cmc.com.cn/EN/10.3877/cma.j.issn.2095-3216.2016.04.001

https://zhsbyjdzzz.cma-cmc.com.cn/EN/Y2016/V05/I04/145

References 60

[20]	Penno G,Solini A,Bonora E, et al. Clinical significance of nonalbuminuric renal impairment in type 2 diabetes[J]. J Hypertens, 2011, 29(9): 1802-1809.
[21]	Kramer HJ,Nguyen QD,Curhan G, et al. Renal insufficiency in the absence of albuminuria and retinopathy among adults with type 2 diabetes mellitus[J]. JAMA, 2003, 289(24): 3273-3277.
[22]	Penno G,Solini A,Zoppini G, et al. Rate and determinants of association between advanced retinopathy and chronic kidney disease in patients with type 2 diabetes: the Renal Insufficiency And Cardiovascular Events (RIACE) Italian multicenter study[J]. Diabetes Care, 2012, 35(11): 2317-2323.
[23]	New JP,Middleton RJ,Klebe B, et al. Assessing the prevalence, monitoring and management of chronic kidney disease in patients with diabetes compared with those without diabetes in general practice[J]. Diabet Med, 2007, 24(4): 364-369.
[24]	Boronat M,Garcia-Canton C,Quevedo V, et al. Non-albuminuric renal disease among subjects with advanced stages of chronic kidney failure related to type 2 diabetes mellitus[J]. Ren Fail, 2014, 36(2): 166-170.
[25]	Araki S,Haneda M,Sugimoto T, et al. Factors associated with frequent remission of microalbuminuria in patients with type 2 diabetes[J]. Diabetes, 2005, 54(10): 2983-2987.
[26]	Molitch ME,Steffes M,Sun W, et al. Development and progression of renal insufficiency with and without albuminuria in adults with type 1 diabetes in the diabetes control and complications trial and the epidemiology of diabetes interventions and complications study[J]. Diabetes Care, 2010, 33(7): 1536-1543.
[27]	Lane PH,Steffes MW,Mauer SM. Glomerular structure in IDDM women with low glomerular filtration rate and normal urinary albumin excretion[J]. Diabetes, 1992, 41(5): 581-586.
[28]	De Cosmo S,Lamacchia O,Pacilli A, et al. Normoalbuminuric renal impairment and all-cause mortality in type 2 diabetes mellitus[J]. Acta Diabetol, 2014, 51(4): 687-689.
[29]	Kamijo-Ikemori A,Sugaya T,Yasuda T, et al. Clinical significance of urinary liver-type fatty acid-binding protein in diabetic nephropathy of type 2 diabetic patients[J]. Diabetes Care, 2011, 34(3): 691-696.
[30]	Shimizu M,Furuichi K,Yokoyama H, et al. Kidney lesions in diabetic patients with normoalbuminuric renal insufficiency[J]. Clin Exp Nephrol, 2014, 18(2): 305-312.
[31]	Araki S,Haneda M,Sugimoto T, et al. Polymorphisms of the protein kinase C-beta gene (PRKCB1) accelerate kidney disease in type 2 diabetes without overt proteinuria[J]. Diabetes Care, 2006, 29(4): 864-868.
[32]	MacIsaac RJ,Panagiotopoulos S,McNeil KJ, et al. Is nonalbuminuric renal insufficiency in type 2 diabetes related to an increase in intrarenal vascular disease?[J]. Diabetes Care, 2006, 29(7): 1560-1566.
[33]	Mattock MB,Barnes DJ,Viberti G, et al. Microalbuminuria and coronary heart disease in NIDDM: an incidence study[J]. Diabetes, 1998, 47(11): 1786-1792.
[34]	Yagil C,Barak A,Ben-Dor D, et al. Nonproteinuric diabetes-associated nephropathy in the Cohen rat model of type 2 diabetes[J]. Diabetes, 2005, 54(5): 1487-1496.
[35]	Ekinci EI,Jerums G,Skene A, et al. Renal structure in normoalbuminuric and albuminuric patients with type 2 diabetes and impaired renal function[J]. Diabetes Care, 2013, 36(11): 3620-3626.
[36]	An JH,Cho YM,Yu HG, et al. The clinical characteristics of normoalbuminuric renal insufficiency in Korean type 2 diabetic patients: a possible early stage renal complication[J]. J Korean Med Sci, 2009, 24 Suppl: S75-S81.
[37]	Ruggenenti P,Fassi A,Ilieva AP, et al. Preventing microalbuminuria in type 2 diabetes[J]. N Engl J Med, 2004, 351(19): 1941-1951.
[38]	Porrini E,Ruggenenti P,Mogensen CE, et al. Non-proteinuric pathways in loss of renal function in patients with type 2 diabetes[J]. Lancet Diabetes Endocrinol, 2015, 3(5): 382-391.
[39]	Neugarten J,Acharya A,Silbiger SR. Effect of gender on the progression of nondiabetic renal disease: a meta-analysis[J]. J Am Soc Nephrol, 2000, 11(2): 319-329.
[40]	Sun L,Kanwar YS. Relevance of TNF-alpha in the context of other inflammatory cytokines in the progression of diabetic nephropathy[J]. Kidney Int, 2015, 88(4): 662-665.
[41]	Perkins BA,Krolewski AS. Early nephropathy in type 1 diabetes: the importance of early renal function decline[J]. Curr Opin Nephrol Hypertens, 2009, 18(3): 233-240.
[42]	Niewczas MA,Ficociello LH,Johnson AC, et al. Serum concentrations of markers of TNFalpha and Fas-mediated pathways and renal function in nonproteinuric patients with type 1 diabetes[J]. Clin J Am Soc Nephrol, 2009, 4(1): 62-70.
[43]	Onuigbo MA. Syndrome of rapid-onset end-stage renal disease: a new unrecognized pattern of CKD progression to ESRD[J]. Ren Fail, 2010, 32(8): 954-958.
[44]	Onuigbo MA,Agbasi N. Diabetic nephropathy and CKD-analysis of individual patient serum creatinine trajectories: a forgotten diagnostic methodology for diabetic CKD prognostication and prediction[J]. J Clin Med, 2015, 4(7): 1348-1368.
[45]	Shimizu M,Furuichi K,Toyama T, et al. Long-term outcomes of Japanese type 2 diabetic patients with biopsy-proven diabetic nephropathy[J]. Diabetes Care, 2013, 36(11): 3655-3662.
[46]	Perkins BA,Ficociello LH,Ostrander BE, et al. Microalbuminuria and the risk for early progressive renal function decline in type 1 diabetes[J]. J Am Soc Nephrol, 2007, 18(4): 1353-1361.
[47]	Ruggenenti P,Porrini E,Motterlini N, et al. Measurable urinary albumin predicts cardiovascular risk among normoalbuminuric patients with type 2 diabetes[J]. J Am Soc Nephrol, 2012, 23(10): 1717-1724.
[48]	Levey AS,Cattran D,Friedman A, et al. Proteinuria as a surrogate outcome in CKD: report of a scientific workshop sponsored by the National Kidney Foundation and the US Food and Drug Administration[J]. Am J Kidney Dis, 2009, 54(2): 205-226.
[49]	Penno G,Solini A,Zoppini G, et al. Independent correlates of urinary albumin excretion within the normoalbuminuric range in patients with type 2 diabetes: The Renal Insufficiency And Cardiovascular Events (RIACE) Italian Multicentre Study[J]. Acta Diabetol, 2015, 52(5): 971-981.
[1]	Xiao L,Wang M,Yang S, et al. A glimpse of the pathogenetic mechanisms of Wnt/beta-catenin signaling in diabetic nephropathy[J]. Biomed Res Int, 2013, 2013: 987064.
[2]	Kwak SH,Park KS. Genetic studies on diabetic microvascular complications: focusing on genome-wide association studies[J]. Endocrinol Metab (Seoul), 2015, 30(2): 147-158.
[3]	Xu X,Xiao L,Xiao P, et al. A glimpse of matrix metalloproteinases in diabetic nephropathy[J]. Curr Med Chem, 2014, 21(28): 3244-3260.
[50]	de Carvalho JA,Tatsch E,Hausen BS, et al. Urinary kidney injury molecule-1 and neutrophil gelatinase-associated lipocalin as indicators of tubular damage in normoalbuminuric patients with type 2 diabetes[J]. Clin Biochem, 2016, 49(3): 232-236.
[51]	Alter ML,Kretschmer A,Von Websky K, et al. Early urinary and plasma biomarkers for experimental diabetic nephropathy[J]. Clin Lab, 2012, 58(7-8): 659-671.
[52]	National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification[J]. Am J Kidney Dis, 2002, 39(2 Suppl 1): S1-S266.
[4]	KDOQI Work Group. KDOQI clinical practice guidelines and clinical practice recommendations for diabetes and chronic kidney disease[J]. Am J Kidney Dis, 2007, 49(2 Suppl 2): S12-S154.
[5]	Giordano AL,Siegel HI,Rosenblatt JS. Nuclear estrogen receptor binding in the preoptic area and hypothalamus of pregnancy-terminated rats: correlation with the onset of maternal behavior[J]. Neuroendocrinology, 1989, 50(3): 248-258.
[6]	Tsalamandris C,Allen TJ,Gilbert RE, et al. Progressive decline in renal function in diabetic patients with and without albuminuria[J]. Diabetes, 1994, 43(5): 649-655.
[53]	Levey AS,Bosch JP,Lewis JB, et al. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group[J]. Ann Intern Med, 1999, 130(6): 461-470.
[54]	Cockcroft DW,Gault MH. Prediction of creatinine clearance from serum creatinine[J]. Nephron, 1976, 16(1): 31-41.
[55]	Caramori ML,Fioretto P,Mauer M. Low glomerular filtration rate in normoalbuminuric type 1 diabetic patients: an indicator of more advanced glomerular lesions[J]. Diabetes, 2003, 52(4): 1036-1040.
[56]	Brenner BM,Cooper ME,de Zeeuw D, et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy[J]. N Engl J Med, 2001, 345(12): 861-869.
[57]	Lewis EJ,Hunsicker LG,Clarke WR, et al. Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes[J]. N Engl J Med, 2001, 345(12): 851-860.
[58]	Satirapoj B,Kaewput W,Supasyndh O, et al. Effect of sulodexide on urinary biomarkers of kidney injury in normoalbuminuric type 2 diabetes: a randomized controlled trial[J]. J Diabetes Res, 2015, 2015: 172038.
[7]	MacIsaac RJ,Tsalamandris C,Panagiotopoulos S, et al. Nonalbuminuric renal insufficiency in type 2 diabetes[J]. Diabetes Care, 2004, 27(1): 195-200.
[8]	Lacquaniti A,Donato V,Pintaudi B, et al. " Normoalbuminuric" diabetic nephropathy: tubular damage and NGAL[J]. Acta Diabetol, 2013, 50(6): 935-942.
[9]	Mottl AK,Kwon KS,Mauer M, et al. Normoalbuminuric diabetic kidney disease in the U. S. population[J]. J Diabetes Complications, 2013, 27(2): 123-127.
[10]	Macisaac RJ,Jerums G. Diabetic kidney disease with and without albuminuria[J]. Curr Opin Nephrol Hypertens, 2011, 20(3): 246-257.
[11]	American Diabetes Association. Standards of medical care in diabetes-2015 abridged for primary care providers[J]. Clin Diabetes, 2015, 33(2): 97-111.
[12]	Zelmanovitz T,Gross JL,Oliveira JR, et al. The receiver operating characteristics curve in the evaluation of a random urine specimen as a screening test for diabetic nephropathy[J]. Diabetes Care, 1997, 20(4): 516-519.
[13]	Dwyer JP,Parving HH,Hunsicker LG, et al. Renal Dysfunction in the presence of normoalbuminuria in type 2 diabetes: results from the DEMAND Study[J]. Cardiorenal Med, 2012, 2(1): 1-10.
[14]	Kramer CK,Leitao CB,Pinto LC, et al. Clinical and laboratory profile of patients with type 2 diabetes with low glomerular filtration rate and normoalbuminuria[J]. Diabetes Care, 2007, 30(8): 1998-2000.
[15]	Bhalla V,Zhao B,Azar KM, et al. Racial/ethnic differences in the prevalence of proteinuric and nonproteinuric diabetic kidney disease[J]. Diabetes Care, 2013, 36(5): 1215-1221.
[59]	Nielsen SE,Reinhard H,Zdunek D, et al. Tubular markers are associated with decline in kidney function in proteinuric type 2 diabetic patients[J]. Diabetes Res Clin Pract, 2012, 97(1): 71-76.
[60]	Dwyer JP,Lewis JB. Nonproteinuric diabetic nephropathy: when diabetics don't read the textbook[J]. Med Clin North Am, 2013, 97(1): 53-58.
[16]	Rigalleau V,Lasseur C,Raffaitin C, et al. Normoalbuminuric renal-insufficient diabetic patients: a lower-risk group[J]. Diabetes Care, 2007, 30(8): 2034-2039.
[17]	Retnakaran R,Cull CA,Thorne KI, et al. Risk factors for renal dysfunction in type 2 diabetes: UK Prospective Diabetes Study 74[J]. Diabetes, 2006, 55(6): 1832-1839.
[18]	Yokoyama H,Sone H,Oishi M, et al. Prevalence of albuminuria and renal insufficiency and associated clinical factors in type 2 diabetes: the Japan Diabetes Clinical Data Management study (JDDM15)[J]. Nephrol Dial Transplant, 2009, 24(4): 1212-1219.
[19]	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)[J]. Diabetes Care, 2009, 32(8): 1497-1502.

Please choose a citation manager

Content to export