Association Among Lipid Accumulation Product, Chinese Visceral Obesity Index and Diabetic Retinopathy in Patients with Type 2 Diabetes: A Cross-Sectional Study

Figures & data

Table 1 Clinical and Biochemical Characteristics of the Four Groups of Subjects

Variables	Controls (n = 94)	NDR (n = 61)	NPDR (n = 55)	PDR (n = 53)	P
Age (years)	46(36,54)	55(50,60) ^#	58(49,63) ^#	58(50,64) ^#	<0.05
Gender (male, %)	49(52.1%)	29(47.5%)	36(65.5%)	25(47.2%)	0.179
Duration of diabetes (years)	/	5(0,9) ^#	10(5,16) ^#&	15(9.5,22) ^#&*	<0.05
Hypertension (yes, %)	/	18(29.5%)^#	23(41.8%)^#	27(50.9%)^#	<0.001
BMI (kg/m2)	23.44±3.11	24.94±3.09^#	25.72±2.66^#	26.24±2.75^#&	<0.05
WC (cm)	83.37±7.52	87.87±7.77^#	91.99±6.79^#&	93.34±7.63^#&	<0.05
LAP	27.15 (16.40,37.51)	38.16(28.14,62.47)^#	52.02 (39.00,78.90) ^#	74.06 (56.41,122.56)^#&*	<0.05
HbA1c(%)	4.95(4.48,5.60)	8,40(7.05,9.90) ^#	8.40(7.00,9.70) ^#	9.20(8.25,10.35) ^#	<0.05
TG (mmol/L)	1.24(0.90,1.64)	1.59(1.13,2.04)^#	1.80(1.33,2.36)^#	2.32(1.63–3.34) ^#&	<0.05
HDL (mmol/L)	1.30(1.11,1.52)	1.20(1.04,1.47)	1.21(1.11,1.36)	1.23(1.03,1.35)	>0.05
LDL (mmol/L)	3.11(2.60,3.67)	2.79(2.54,3.16)	2.87(2.52,3.24)	3.17(2.76,3.79) ^&	<0.05
TC (mmol/L)	5.08(4.35,5.61)	4.61(4.21,5.37)	4.85(4.39,5.82)	5.36(4.63,6.50) ^&	<0.05
BUN (mmol/L)	4.60(4.04,5.37)	5.36(4.82,6.04)^#	5.77(4.87,7.47)^#	5.92(4.78,7.03)^#	<0.05
Cr(mmol/L)	63.40 (54.85,72.63)	60.80 (51.55,67.35)	64.10 (51.20,71.80)	62.00 (50.35,71.05)	>0.05
LEAD (%)	/	51(83.6%)^#	46(83.6%)^#	48(90.6%) ^#	<0.001
Carotid atherosclerosis (%)	/	41(67.2%)^#	38(69.1%)^#	22(41.5%)^#&*	<0.05
DSPN (%)	/	2(3.3%)	11(20.0%)^#&	20(37.7%)^#&	<0.05
DN (%)	/	5(8.2%)^#	12(21.8%)^#	27(50.9%)^#&*	<0.05
Statins use (%)	/	31(50.8%)^#	33(60.0%)^#	36(67.9%)^#	<0.001
Insulin use (%)	/	43(70.5%)^#	46(83.6%)^#	50(94.3%)^#&	<0.05
Metformin use (%)	/	42(68.9%)^#	43(78.2%)^#	31(58.5%)^#	<0.001
CVAI	78.31±32.63	108.20±33.80^#	125.70±30.60^#&	133.43±27.72^#&	<0.05

Notes: Compared with healthy control group, ^#P<0.05; compared with NDR group, ^&p<0.05; compared with NPDR group, *P<0.05.

Abbreviations: NDR, non-diabetic retinopathy; NPDR, non-proliferative diabetic retinopathy; PDR, proliferative diabetes retinopathy; BMI, body mass index; LAP, lipid accumulation product; HbA1c, hemoglobin A1c; TG, triglyceride; HDL, high-density lipoprotein; LDL, low-density lipoprotein; TC, total cholesterol; BUN, blood urea nitrogen; Cr, creatinine; LEAD, lower-extremity arterial disease; DSPN, diabetic peripheral neuropathy; DN, diabetic nephropathy; CVAI Chinese visceral adiposity index.

Table 2 General Characteristics of Patients Divided by Quartiles of LAP

Variables	Q1 (n = 42)	Q2 (n = 42)	Q3 (n = 42)	Q4 (n = 43)	P
Age (years)	55.52±8.75	58.93±8.70	54.67±9.91	55.33±9.23	0.143
Gender (male, %)	25(59.2%)	22(52.4%)	19(45.2%)	24(55.8%)	0.599
Duration of diabetes (years)	6(1.75,11.25)	10(2.5,17)	7.5(3.75,17)	13(9,20) ^#*	<0.05
Hypertension (yes, %)	15(35.7%)	16(38.1%)	17(40.5%)	20(46.5%)	0.767
BMI (kg/m^2)	23.44±2.27	25.20±2.57^#	26.38±2.20^#&	27.34±2.92^#&	<0.001
WC (cm)	84.43±6.85	90.93±6.25^#	92.66±5.51^#	95.61±7.67^#&*	<0.001
LAP	26.26 (21.48,32.14)	46.41 (40.2,51.23) ^#	66.08 (62.58,74.62) ^#&	96.14 (88.11,150.92) ^#&*	<0.05
HbA1c (%)	8.25±2.05	8.64±1.75	9.15±2.19 ^#	9.38±1.91 ^#	<0.05
TG (mmol/L)	1.16(0.9,1.31)	1.52(1.36,1.83) ^#	2.14(1.87,2.35) ^#&	3.21(2.53,4.60) ^#&*	<0.05
HDL (mmol/L)	1.27(1.09,1.50)	1.24(1.11,1.38)	1.15(1.02,1.29)	1.23(1.04,1.36)	>0.05
LDL (mmol/L)	2.69(2.48,3.04)	2.83(2.64,3.21)	3.29(2.62,3.95) ^#	3.05(2.73,3.54) ^#	<0.05
TC (mmol/L)	4.51(4.07,5.09)	4.78(4.47,5.25)	5.44(4.49,6.49) ^#	5.26(4.72,6.54) ^#&	<0.05
BUN (mmol/L)	5.28(4.56,6.22)	5.87(4.90,6.95)	5.69(4.63,6.87)	5.82(4.9,7.37)	>0.05
Cr(mmol/L)	61.25 (48.28,67.38)	63.7 (54.43,71.43)	59.15 (46.63,77.3)	62.3 (52.1,70.5)	>0.05
LEAD (%)	34(81.0%)	39(92.9%)	34(81.0%)	38(88.4%)	0.312
Carotid atherosclerosis (%)	32(76.2%)	30(71.4%)	20(47.6%) ^#	19(44.2%) ^#	<0.05
DSPN (%)	3(7.1%)	6(14.3%)	11(26.2%)	13(30.2%) ^#	<0.05
DN (%)	6(14.3%)	5(11.9%)	16(38.1%) ^&	17(39.5%) ^&	<0.05
Statins use (%)	18(42.9%)	24(57.1%)	29(69.0%)	29(67.4%)	0.055
Insulin use (%)	30(71.4%)	34(81.0%)	36(85.7%)	39(90.7%)	0.118
Metformin use (%)	24(57.1%)	29(69.0%)	29(69.0%)	34(79.1%)	0.190
CVAI	89.46±29.09	123.24±25.01^#	128.11±20.52^#	145.84±26.81^#&*	<0.001
DR (%)	16(38.1%)	28(64.3%)	26(61.9%)	39(90.7%) ^#&*	<0.001

Notes: Compared with healthy control group, ^#P<0.05; compared with NDR group, ^&p<0.05; compared with NPDR group, *P<0.05.

Abbreviations: NDR, non-diabetic retinopathy; NPDR, non-proliferative diabetic retinopathy; PDR, proliferative diabetes retinopathy; BMI, body mass index; LAP, lipid accumulation product; HbA1c, hemoglobin A1c; TG, triglyceride; HDL, high-density lipoprotein; LDL, low-density lipoprotein; TC, total cholesterol; BUN, blood urea nitrogen; Cr, creatinine; LEAD, lower-extremity arterial disease; DSPN, diabetic peripheral neuropathy; DN, diabetic nephropathy; CVAI Chinese visceral adiposity index.

Table 3 General Characteristics of Patients Divided by Quartiles of CVAI

Variables	Q1 (n = 42)	Q2 (n = 43)	Q3 (n = 41)	Q4 (n = 43)	P
Age (years)	51.76±8.72	54.30±8.41	58.76±8.96^#&	59.63±8.80^#&	<0.001
Gender (male, %)	17(40.5%)	21(48.8%)	23(56.1%)	29(67.4%)	0.082
Duration of diabetes (years)	5(0,10)	10(5,17) ^#	8(4.5,17)	14(8,20) ^#	<0.05
Hypertension (yes, %)	10(23.8%)	20(46.5%)	16(39.0%)	22(51.2%)	0.056
BMI (kg/m^2)	23.23±2.28	25.37±1.93^#	25.54±2.06^#	28.21±2.80^#&*	<0.001
WC (cm)	82.69±5.74	88.59±3.51^#	93.02±4.62^#&	99.33±5.02^#&*	<0.001
LAP	28.74 (21.78,38.97)	53.25 (39.0,70.5) ^#	66.08 (47.33,86.95) ^#	78.21 (53.63,105.93) ^#&	<0.05
HbA1c (%)	8.64±2.16	8.90±1.94	9.00±2.25	8.87±1.72	0.843
TG (mmol/L)	1.26(1.00,1.82)	2.01(1.40,2.52) ^#	2.02(1.58,2.62) ^#	2.08(1.48,2.87) ^#	<0.05
HDL (mmol/L)	1.32(1.19,1.68)	1.17(1.05,1.38)	1.21(1.01,1.34) ^#	1.15(0.99,1.35) ^#	<0.05
LDL (mmol/L)	2.88(2.60,3.66)	2.80(2.52,3.38)	2.97(2.55,3.56)	2.93(2.72,3.25)	>0.05
TC (mmol/L)	4.94(4.31,6.15)	4.87(4.26,5.89)	4.83(4.34,6.35)	4.85(4.52,5.49)	>0.05
BUN (mmol/L)	4.98(4.54,5.78)	5.59(4.86,6.67)	5.77(4.59,7.30)	6.14(5.00,7.48) ^#	<0.05
Cr(mmol/L)	52.45 (45.60,65.93)	61.00 (50.00,69.10)	69.50 (54.05,76.95) ^#	66.30 (5.80,71.80) ^#	<0.05
LEAD (%)	32(76.2%)	36(83.7%)	37(90.2%)	40(93.0%)	0.120
Carotid atherosclerosis (%)	28(66.7%)	22(51.2%)	27(65.9%)	24(55.8%)	0.382
DSPN (%)	6(14.3%)	5(11.6%)	9(22.0%)	13(30.2%)	0.125
DN (%)	5(11.9%)	7(16.3%)	12(29.3%)	20(46.5%) ^#&	<0.05
Statins use (%)	20(47.6%)	29(67.4%)	26(63.4%)	25(58.1%)	0.277
Insulin use (%)	29(69.0%)	38(88.4%)	34(82.9%)	38(88.4%)	0.065
Metformin use (%)	25(59.5%)	28(65.1%)	26(63.4%)	37(86.0%) ^#	<0.05
CVAI	80.63±21.92	112.24±6.65^#	132.95±5.72^#&	106.97±14.86^#*	<0.001
DR (%)	16(38.1%)	30(69.8%) ^#	27(65.9%)	35(81.4%) ^#	<0.001

Notes: Compared with healthy control group, ^#P<0.05; compared with NDR group, ^&p<0.05; compared with NPDR group, *P<0.05;

Abbreviations: NDR, non-diabetic retinopathy; NPDR, non-proliferative diabetic retinopathy; PDR, proliferative diabetes retinopathy; BMI, body mass index; LAP, lipid accumulation product; HbA1c, hemoglobin A1c; TG, triglyceride; HDL, high-density lipoprotein; LDL, low-density lipoprotein; TC, total cholesterol; BUN, blood urea nitrogen; Cr, creatinine; LEAD, lower-extremity arterial disease; DSPN, diabetic peripheral neuropathy; DN, diabetic nephropathy; CVAI Chinese visceral adiposity index.

Table 4 Associations Between LAP and Other Variables

Variables	r	P
Age (years)	0.275	<0.001
HbA1c (%)	0.558	<0.001
Duration of diabetes (years)	0.539	<0.001
TC	0.238	<0.001
TG	0.912	<0.001
HDL	−0.309	<0.001
LDL	0.188	0.002
BUN	0.309	<0.001
Cr	0.039	0.527

Abbreviations: HbA1c, hemoglobin A1c; HDL, high density lipoprotein; LDL, low density lipoprotein; TC, total cholesterol; BUN, blood urea nitrogen; Cr, creatinine.

Table 5 Associations Between CVAI and Other Variables

Variables	r	P
Age (years)	0.475	<0.001
HbA1c (%)	0.504	<0.001
Duration of diabetes (years)	0.581	<0.001
TC	−0.003	0.960
TG	0.575	<0.001
HDL	−0.399	<0.001
LDL	−0.009	0.884
BUN	0.389	<0.001
Cr	0.197	0.001

Abbreviations: HbA1c, hemoglobin A1c; HDL, high density lipoprotein; LDL, low density lipoprotein; TC, total cholesterol; BUN, blood urea nitrogen; Cr, creatinine.

Table 6 Association Among LAP, WC, CVAI and DR

		LAP		WC		CVAI
	P	OR (95% CI)	P	OR (95% CI)	P	OR (95% CI)
Model 1	<0.001	1.033 (1.018–1.048)	<0.001	1.093 (1.042–1.147)	<0.001	1.023 (1.011–1.034)
Model 2	<0.001	1.031 (1.014–1.048)	0.016	1.071 (1.013–1.133)	0.012	1.018 (1.004–1.032)
Model 3	0.003	1.030 (1.010–1.050)	0.016	1.077 (1.014–1.144)	0.031	1.018 (1.002–1.034)
Model 4	0.003	1.029 (1.010–1.049)	0.024	1.073 (1.009–1.141)	0.049	1.017 (1.000–1.033)

Notes: Model 1: Crude model; Model 2: Model 1+adjust for age, gender, duration of diabetes; Model 3: Model 2+ adjust for HbA1c, HDL, LDL, TC; Model 4: Model 3+ adjust for hypertension, statins use, insulin use and metformin use.

Table 7 Association Among LAP, WC, CVAI and DR Severity

Variables	OR (95% CI)	P
LAP	1.020 (0.100–0.290)	<0.001
WC	1.059 (−0.035–0.149)	0.226
CVAI	1.002 (−0.02–0.025)	0.829

Abbreviations: LAP, lipid accumulation product; CVAI Chinese visceral adiposity index.

Figure 1 The ROC curve of abdominal obesity indices for diagnosing.

Abbreviations: WC, waist circumference; LAP, Lipid accumulation product; CVAI, Chinese visceral adiposity index.