Risk factors and urinary biomarkers of non-albuminuric and albuminuric chronic kidney disease in patients with type 2 diabetes

doi:10.4239/wjd.v10.i11.517

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World Journal of Diabetes

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World J Diabetes. Nov 15, 2019; 10(11): 517-533
Published online Nov 15, 2019. doi: 10.4239/wjd.v10.i11.517

Table 1 Clinical characteristics of type 2 diabetic individuals with different patterns of chronic kidney disease

Parameter	CKD- (n = 89)	NA-CKD (n = 111)	A-CKD– (n = 87)	A-CKD+ (n = 73)
General clinical parameters
Sex, M/F, n (%)	20/69	13/98	45/42	22/51
	22.5/77.5	11.7/88.3^a^f^h	51.9/48.1^c^h	30.1/69.9^e
Age, yr	64 (58; 67)	68 (64; 73)^b^fⁱ	63 (59; 68)ⁱ	67 (61; 77)^a^e
BMI, kg/m²	33.4 (28.7; 36.9)	32.6 (29.4; 37.2)	33.6 (30.1; 38.2)	33.4 (30.0; 36.8)
WHR	0.97 (0.94; 1.03)	0.94 (0.89; 0.99)^f^h	1.04 (0.97; 1.11)^a	0.98 (0.95; 1.07)
Smoking, n (%)	7 (7.9)	6 (5.4)	18 (20.9)^a	3 (4.1)
Diabetes duration, yr	15 (12; 19)	18 (15; 25)^c^d	15 (13; 20)	18 (14; 22)^a
Diabetic complications and comorbidities
Diabetic retinopathy, n (%)	62 (69.7)	74 (66.7)	65 (74.7)	57 (78.1)
Arterial hypertension, n (%)	85 (95.5)	111 (100)	87 (98.9)	73 (100)
Coronary artery disease, n (%)	41 (46.1)	58 (52.3)	46 (52.9)	41 (56.2)
Myocardial infarction in anamnesis, n (%)	7 (7.9)	19 (17.1)	20 (23.0)^b	17 (23.3)^b
Chronic heart failure (NYHA class III-IV), n (%)	5 (5.6)	7 (6.3)	11 (12.6)	4 (5.5)
Carotid atherosclerosis, n (%)	15 (16.9)	51 (45.9)^c	33 (37.9)^a	40 (54.8)^c
Cerebrovascular event in anamnesis, n (%)	6 (6.7)	13 (11.7)^a	5 (5.8)	11 (15.1)^a
Peripheral artery disease, n (%)	60 (67.4)	84 (75.7)	59 (67.8)	57 (78.1)^a
Treatment
Metformin, n (%)	61 (68.5)	64 (57.7)	56 (64.4)	43 (58.9)
Sulfonylurea, n (%)	29 (32.6)	31 (27.9)^g	21 (24.1)	10 (13.7)^b
Insulin, n (%)	74 (83.1)	94 (84.7)^g	76 (87.5)	70 (95.9)^a
Duration of insulin therapy, yr	6 (4; 10)	10 (7; 13)^c^f	6 (3; 10)	8 (3; 11)
Daily insulin dose, IU	52 (36; 72)	46 (34; 62)^g	56 (40; 78)	60 (42; 74)
Daily insulin dose, IU/kg	0.60 (0.40; 0.80)	0.55 (0.40; 0.70)	0.60 (0.40; 0.80)	0.63 (0.45; 0.90)
RAS blockers, n (%)	67 (75.3)	93 (83.8)	69 (79.3)	61 (83.6)
Diuretics, n (%)	36 (40.4)	73 (65.8)^a^d^g	38 (43.7)	35 (47.9)
Calcium channel blockers, n (%)	27 (30.3)	38 (34.2)^g	34 (39.1)	36 (49.3)^a
Antiplatelet agents, n (%)	46 (51.7)	78 (70.3)^b^d	50 (57.5)^g	57 (78.1)^b^e
Statins, n (%)	28 (31.5)	59 (53.2)^b^d	31 (35.6)^g	39 (53.4)^b^e

^aP < 0.05,

^bP < 0.01,

^cP < 0.001 vs CKD–,

^dP < 0.05,

^eP < 0.01,

^fP < 0.001 vs A-CKD–,

^gP < 0.05,

^hP < 0.01,

ⁱP < 0.001 vs А-CKD+ (χ² test for discrete parameters and multiple comparisons of mean ranks for continuous parameters). BMI: Body mass index; WHR: Waist-to-hip ratio; CKD–: The group of individuals with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; NA-CKD: Non-albuminuric chronic kidney disease, the group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; A-CKD–: Group of patients with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol; A-CKD+: Group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol.

Table 2 Laboratory parameters of type 2 diabetic individuals with different patterns of chronic kidney disease

Parameter	CKD- (n = 89)	NA-CKD (n = 111)	A-CKD- (n = 87)	A-CKD+ (n = 73)
Renal tests
Serum creatinine, μmol/L	76 (67.3; 86.8)	111 (99.1; 124)^c^f	85.8 (76.1; 96.5)	116 (97.8; 144)^c^f
eGFR, mL/min × 1.73 m²	77 (69; 87)	52 (46; 56)^c^f	72 (66; 84)ⁱ	51 (46; 55.8)^c
UACR, mg/mmol	0.5 (0.3; 0.9)	0.7 (0.4; 1.0)^fⁱ	8.3 (4.8; 36.7)^c	11.4 (5.6; 42.1)^c
Urinary protein excretion, mg/day	65 (50; 100)	70 (50; 140)	170 (90; 530)^cⁱ	200 (130; 520)^cⁱ
Biochemistry
HbA1c, %	8.4 (7.5; 10.1)	8.1 (7.2; 9.5)^f	9.7 (8.5; 11.2)^b^g	8.6 (7.5; 9.8)
HbA1c, mmol/L	68 (58; 87)	65 (55; 80)^f	83 (69; 99)^b^g	70 (58; 84)
Fasting blood glucose, mmol/L	8.9 (6.8; 10.2)	8.8 (6.5; 10.1)	9.5 (8.0; 12.8)^a	9.6 (7.7; 12.0)
2h-postprandial blood glucose, mmol/L	10.7 (9.0; 13.7)	11.7 (8.9; 14.0)	13.1 (9.9; 15.0)^a	11.3 (10.0; 14.0)
Total cholesterol, mmol/L	5.1 (4.5; 5.9)	5.1 (4.3; 6.0)	4.9 (4.1; 6.0)	5.3 (4.1; 6.4)
LDL-cholesterol, mmol/L	3.3 (2.7; 3.9)	3.2 (2.5; 4.0)	3.1 (2.5; 3.8)	3.2 (2.5; 4.1)
HDL-cholesterol, mmol/L	1.2 (1.0; 1.4)	1.3 (1.1; 1.5)^e	1.2 (1.0; 1.3)	1.1 (1; 1.4)
Triglycerides, mmol/L	1.6 (1.3; 2.2)	1.6 (1.1; 2.4)	1.8 (1.2; 2.9)	1.8 (1.3; 2.8)
Uric acid, μmol/L	279 (218; 349)	327 (269; 381)^a	324 (276; 376)^a	349 (272; 390)^a
Hematology
Hemoglobin, g/L	137 (130; 144)	129 (123; 140)^b^d	138 (126; 147)	133 (123; 143)
RBC, × 10¹²/L	4.8 (4.5; 5.0)	4.5 (4.2; 4.8)^a^d	4.7 (4.5; 5.1)^g	4.5 (4.1; 4.9)^b
WBC, × 10⁹/L	6.5 (5.7; 8.0)	6.7 (5.7; 7.8)	6.6 (5.3; 7.9)	6.9 (5.7; 8.0)
Platelets, × 10⁹/L	238 (199; 270)	234 (195; 270)	233 (191; 281)	229 (189; 273)
ESR, mm/h	16.5 (10; 23)	22 (15; 31)^b	22.5 (15.5; 29.5)^b	23 (18; 33)^c
Coagulation tests
Fibrinogen, g/L	4.4 (3.9; 5.5)	4.4 (3.9; 5.1)	4.5 (3.8; 5.7)	4.1 (3.7; 5.1)
SFMCs, mg/dL	5.5 (3.5; 15)	12 (7; 16)	14 (8; 23)^a	12.5 (7; 21)
D-dimer, ng/mL	263 (235; 303)	287 (239; 351)	271 (232; 304)	290 (254; 363)

^aP < 0.05,

^bP < 0.01,

^cP < 0.001 vs CKD–,

^dP < 0.05,

^eP < 0.01,

^fP < 0.001 vs A-CKD–,

^gP < 0.05,

ⁱP < 0.001 vs А-CKD+ (χ² test for discrete parameters and multiple comparisons of mean ranks for continuous parameters, estimated glomerular filtration rate, mL/min × 1.73 m²). LDL: Low-density lipoprotein; HDL: High-density lipoprotein; UACR: Urinary albumin-to-creatinine ratio; eGFR: Estimated glomerular filtration rate; HbA1c: Hemoglobin A1c; RBC: Red blood cell; WBC: White blood cell; SFMC: Soluble fibrin monomer complex; CKD–: The group of individuals with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; NA-CKD: Non-albuminuric chronic kidney disease, the group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; A-CKD–: Group of patients with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol; A-CKD+: Group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol.

Table 3 Risk factors for different patterns of chronic kidney disease in patients with type 2 diabetes

Risk factor	Pattern of CKD
Risk factor	NA-CKD (n = 111)	A-CKD– (n = 87)	A-CKD+ (n = 73)
Age ≥ 65 yr	3.16 (1.76-5.70)	1.00 (0.55-1.80)	1.76 (0.94-3.28)
Age ≥ 65 yr	P = 0.0001	P = 0.99	P = 0.08
Duration of diabetes ≥ 15 yr	2.81 (1.53-5.17)	1.63 (0.89-3.01)	2.32 (1.19-4.53)
Duration of diabetes ≥ 15 yr	P = 0.0009	P = 0.12	P = 0.01
Male sex	0.46 (0.21-0.98)	2.32 (1.20-2.48)	1.49 (0.74-3.01)
Male sex	P = 0.04	P = 0.01	P = 0.24
Female sex	2.19 (1.02-4.69)	0.43 (0.22-0.83)	0.67 (0.33-1.36)
Female sex	P = 0.04	P = 0.01	P = 0.24
Smoking	0.81 (0.25-2.60)	3.49 (1.31-9.28)	0.56 (0.13-2.34)
Smoking	P = 0.72	P = 0.01	P = 0.43
WHR >1.0	0.61 (0.22-1.65)	3.64 (1.32-9.99)	1.53 (0.57-4.10)
WHR >1.0	P = 0.32	P = 0.01	P = 0.40
HbA1c > 8.0%	0.68 (0.38-1.20)	2.67 (1.35-5.27)	1.10 (0.58-2.09)
HbA1c > 8.0%	P = 0.18	P = 0.005	P = 0.76
Treatment with diuretics	2.80 (1.56-5.00)	1.10 (0.60-2.00)	1.30 (0.70-2.44)
Treatment with diuretics	P = 0.0005	P = 0.76	P = 0.41
Treatment with calcium channel blockers	1.20 (0.66-2.17)	1.47 (0.79-2.75)	2.23 (1.17-4.25)
Treatment with calcium channel blockers	P = 0.56	P = 0.22	P = 0.01

The data are presented as odds ratio, 95% confidence interval and P value. CKD: Chronic kidney disease; CKD–: The group of individuals with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; NA-CKD: Non-albuminuric chronic kidney disease, the group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio < 3.0 mg/mmol; A-CKD–: Group of patients with estimated glomerular filtration rate ≥ 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol; A-CKD+: Group of individuals with estimated glomerular filtration rate < 60 mL/min × 1.73 m² and urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol; HbA1c: Hemoglobin A1c; WHR: Waist-to-hip ratio.

Table 4 Logistic regression model for estimated glomerular filtration rate < 60 mL/min × 1.73 m², logit(P) = ln[P/(1–P)]

Parameter	Coefficient β	95%CI	P value
Constant	-3.5742	-6.1459, -1.0025	0.006
Age, years	+0.0751	0.0413, 0.1089	0.00001
HbA1c, %	-0.2277	-0.3645, -0.0908	0.001
Female sex (1 or 0)	+0.2277	0.0051, 0.5743	0.046
Use of diuretics (1 or 0)	-0.2521	-0.4895, -0.0143	0.04

Area under the receiver operating characteristic curve = 0.7441, P value for Kolmagorov-Smirnov statistics = 2 × 10^-11. CI: Confidence interval; HbA1c: Glycated hemoglobin; logit: Logit-function.

Table 5 Logistic regression model for urinary albumin-to-creatinine ratio ≥ 3.0 mg/mmol, logit(P) = ln[P/(1–P)]

Parameter	Coefficient β	95%CI	P value
Constant	-8.1206	-13.1599, -3.0813	0.002
WHR	+5.1228	0.3920, 9.8535	0.03
HbA1c, %	+0.3570	0.1169, 0.5971	0.004
Male sex, (1 or 0)	+0.6725	0.1920, 1.1531	0.006

Area under the receiver operating characteristic curve = 0.7612, P value for Kolmagorov-Smirnov statistics = 0.00004. CI: Confidence interval; HbA1c: Glycated hemoglobin; logit: Logit-function; WHR: Waist-to-hip ratio.

Citation: Korbut AI, Klimontov VV, Vinogradov IV, Romanov VV. Risk factors and urinary biomarkers of non-albuminuric and albuminuric chronic kidney disease in patients with type 2 diabetes. World J Diabetes 2019; 10(11): 517-533
URL: https://www.wjgnet.com/1948-9358/full/v10/i11/517.htm
DOI: https://dx.doi.org/10.4239/wjd.v10.i11.517