The Triglyceride–Glucose Index is Associated with Diabetic Retinopathy in Chinese Patients with Type 2 Diabetes: A Hospital-Based, Nested, Case–Control Study

Figures & data

Table 1 Characteristics of study participants by presence and severity of DR

	Overall (n=2,112)	Non-DR (n=1,516)	Mild NPDR (n=446)	Moderate NPDR (n=87)	VTDR (n=63)	P
Age (years)	56.08±13.85	55.32±14.36	57.11±12.46	61.89±11.37	58.94±10.75	<0.001
Sex (male), n (%)	1,223 (57.9)	896 (59.1)	252 (56.5)	46 (52.9)	29 (45.0)	0.122
Duration of diabetes, n (%)						<0.001
<5 years	911 (43.1)	721 (47.6)	154 (34.5)	18 (20.7)	18 (28.6)
5–<10 years	511 (24.2)	359 (23.7)	120 (26.9)	20 (23.0)	12 (19.0)
10–≤20 years	566 (26.8)	361 (23.8)	140 (31.4)	38 (43.7)	27 (42.9)
20 years	124 (5.9)	75 (4.9)	32 (7.2)	11 (12.6)	6 (9.5)
Antidiabetic-agent use (yes), n (%)	2,027 (96.0)	1,441 (95.1)	437 (98.0)	87 (100)	62 (98.4)	0.006
HR (bpm)	80.50±11.77	80.09±11.14	81.44±13.84	81.43±9.96	82.54±12.34	0.005
SBP (mmHg)	134.63±18.34	133.27±17.97	137.35±18.27	142.36±21.32	137.57±18.59	<0.001
DBP (mmHg)	82.67±11.20	82.48±11.15	82.98±11.22	83.83±12.38	83.33±10.63	0.591
PP (mmHg)	51.96±15.15	50.78±14.81	54.37±14.86	58.53±19.31	54.24±14.36	<0.001
Height (cm)	167.53±8.52	167.90±8.55	166.92±8.31	165.74±8.35	165.64±8.78	0.007
Weight (kg)	72.24±14.11	72.92±14.50	70.82±13.26	68.31±11.08	71.33±12.70	0.002
BMI (kg/m^2)	25.63±4.00	25.76±4.15	25.29±3.56	24.82±3.32	25.97±3.96	0.030
Smoker (yes), n (%)	534 (25.3)	396 (26.1)	97 (21.7)	25 (28.7)	16 (25.4)	0.255
Drinker (yes), n (%)	414 (19.6)	304 (20.1)	80 (17.9)	20 (23.0)	10 (15.9)	0.53,8
HbA1c, %, (mmol/mol)	8.46±2.39 (69.0±26.1)	8.47±2.23 (69.1±24.3)	8.60±2.94 (70.5±32.1)	7.84±2.16 (62.2±23.6)	8.24±2.01 (66.5±21.9)	0.046
FPG (mg/dL, mmol/L)	166.79±64.23 (9.27±3.57)	168.76±65.28 (9.38±3.63)	166.65±63.99 (9.26±3.55)	153.09±54.68 (8.50±3.04)	139.10±40.52 (7.73±2.25)	0.013
TC (mmol/L)	4.81±1.39	4.82±1.20	4.75±1.24	5.04±3.63	4.59±0.95	0.070
TGs (mg/dL)	195.87±150.99	200.73±153.89	189.63±152.17	176.99±117.41	149.40±93.27	0.010
HDL-C (mmol/L)	1.09±0.39	1.08±0.37	1.10±0.47	1.12±0.29	1.12±0.32	0.661
LDL-C (mmol/L)	3.03±0.99	3.04±0.98	3.04±1.05	2.93±0.93	2.98±0.87	0.728
Insulin (mU/L)	11.81±6.67	11.95±6.78	11.45±6.63	11.33±4.61	11.52±6.50	0.464
HOMA-IR	4.91±3.53	5.02±3.57	4.79±3.64	4.39±2.53	3.97±2.46	0.011
TyG index	9.41±0.81	9.44±0.83	9.39±0.78	9.28±0.73	9.08±0.54	0.005

Abbreviations: DR, diabetic retinopathy; NPDR, non-proliferative DR; VTDR, vision-threatening DR; HR, heart rate; SBP, systolic blood pressure; DBP, diastolic BP; PP, pulse pressure; BMI, body-mass index; HbA_1c, glycated hemoglobin; FPG, fasting plasma glucose; TC, total cholesterol; TGs, triglycerides; HDL-C, highdensity–lipoprotein cholesterol; LDL-C, lowdensity–lipoprotein cholesterol; HOMA-IR, homeostasis-model assessment of insulin resistance; TyG, triglyceride–glucose.

Table 2 Associations between TyG index and various stages of DR after controlling for confounding factors

	Mild NPDR		Moderate NPDR		VTDR		Any DR
	OR (95% CI)	P	OR (95% CI)	P	OR (95% CI)	P	OR (95% CI)	P
Model 1	0.92 (0.80–1.05)	0.198	0.78 (0.59–1.03)	0.081	0.54 (0.38–0.76)	<0.001	0.85 (0.76–0.96)	0.009
Model 2	0.88 (0.76–1.01)	0.073	0.88 (0.64–1.20)	0.417	0.53 (0.36–0.76)	0.001	0.83 (0.73–0.95)	0.006
Model 3	0.89 (0.76–1.03)	0.114	0.84 (0.61–1.15)	0.273	0.53 (0.36–0.79)	0.001	0.83 (0.72–0.95)	0.007

Notes: Model 1 adjusted for age and sex; model 2 adjusted for age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, and HbA_1c; model 3 adjusted for age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, HbA_1c, and TC.

Abbreviations: TyG, triglyceride-glucose index; DR, diabetic retinopathy; NPDR, nonproliferative DR; VTDR, vision-threatening DR.

Table 3 Associations between quartiles of TyG index and various stages of DR after controlling for confounding factors

		Mild NPDR		Moderate NPDR		VTDR		Any DR
		OR (95% CI)	P	OR (95% CI)	P	OR (95% CI)	P	OR (95% CI)	P
Model 1	TyG Q1	1.00		1.00		1.00		1.00
	TyG Q2	1.08 (0.80–1.45)	0.612	1.08 (0.61–1.90)	0.788	1.10 (0.59–2.05)	0.766	1.08 (0.83–1.41)	0.549
	TyG Q3	1.07 (0.80–1.44)	0.648	0.67 (0.36–1.27)	0.222	0.90 (0.47–1.72)	0.741	0.99 (0.76–1.29)	0.921
	TyG Q4	0.82 (0.60–1.11)	0.201	0.68 (0.37–1.28)	0.231	0.14 (0.04–0.47)	0.002	0.71 (0.54–0.94)	0.016
		Ptrend=0.178		P trend=0.118		P trend=0.001		P trend=0.010
Model 2	TyG Q1	1.00		1.00		1.00		1.00
	TyG Q2	1.03 (0.76–1.39)	0.874	1.07 (0.60–1.91)	0.825	1.06 (0.56–1.99)	0.866	1.03 (0.79–1.35)	0.808
	TyG Q3	1.01 (0.74–1.37)	0.957	0.76 (0.39–1.47)	0.410	0.88 (0.45–1.72)	0.697	0.95 (0.72–1.25)	0.723
	TyG Q4	0.73 (0.53–1.01)	0.060	0.85 (0.43–1.68)	0.634	0.13 (0.04–0.49)	0.001	0.66 (0.49–0.89)	0.007
		P trend=0.057		P trend=0.465		P trend=0.001		P trend=0.005
Model 3	TyG Q1	1.00		1.00		1.00		1.00
	TyG Q2	1.03 (0.76–1.40)	0.847	1.02 (0.57–1.83)	0.949	1.07 (0.56–2.01)	0.845	1.03 (0.79–1.35)	0.829
	TyG Q3	1.02 (0.75–1.39)	0.910	0.72 (0.37–1.40)	0.331	0.89 (0.45–1.76)	0.734	0.95 (0.72–1.25)	0.698
	TyG Q4	0.74 (0.53–1.05)	0.089	0.77 (0.38–1.54)	0.453	0.14 (0.04–0.48)	0.002	0.66 (0.48–0.89)	0.007
		P trend=0.088		P trend=0.321		P trend=0.002		P trend=0.006

Notes: Model 1 adjusted for age and sex; model 2 adjusted for age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, and HbA_1c; model 3 adjusted for age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, HbA_1c, and TC.

Abbreviations: TyG, triglyceride–glucose; DR, diabetic retinopathy; NPDR, nonproliferative DR; VTDR, vision-threatening DR.

Table 4 Prediction of DR and VTDR by TyG index and four biochemical blood parameters

	Cases/controls, n	AUC (95% CI)	P	Cutoff	Sensitivity	Specificity
DR	596/1516
HbA1c, %, (mmol/mol)		0.515 (0.487–0.542)	0.296	9.05 (75.4)	0.350	0.696
FPG (mg/dL, mmol/L)		0.529 (0.502–0.556)	0.035	182.79 (10.16)	0.354	0.703
TGs (mg/dL)		0.533 (0.507–0.560)	0.017	170.36	0.443	0.629
HOMA-IR		0.534 (0.507–0.561)	0.016	3.47	0.588	0.480
TyG index		0.534 (0.507–0.561)	0.015	9.67	0.363	0.710
VTDR	63/1516
HbA1c, %, (mmol/mol)		0.526 (0.458–0.594)	0.485	10.05 (86.3)	0.232	0.873
FPG (mg/dL, mmol/L)		0.608 (0.550–0.666)	0.004	167.85 (9.33)	0.420	0.825
TGs (mg/dL)		0.588 (0.528–0.648)	0.018	210.19	0.316	0.873
HOMA-IR		0.580 (0.513–0.647)	0.031	3.83	0.513	0.651
TyG index		0.624 (0.569–0.679)	0.001	9.77	0.319	0.937

Abbreviations: DR, diabetic retinopathy; VTDR, vision-threateningDR; TyG, triglyceride–glucose; AUC, area under curve; HbA_1c, glycated hemoglobin; FPG, fasting plasma glucose; TGs, triglycerides; HOMA-IR, homeostasis-model assessment of insulin resistance.

Table 5 Direct and indirect effects of DR on TyG index with HOMA-IR

	Model 1			Model 2
	β ^#	P		β ^#	P
Total effect c	–0.057	0.006	Proportion of mediation 35.1%^‡	–0.055	0.006	Proportion of mediation 36.0%^‡
Direct effect c’	–0.037	0.042		–0.035	0.044
Indirect effect a	–0.043	0.045		–0.043	0.047
Indirect effect b	0.466	<0.001		0.457	<0.001

Notes: Model 1 adjusted by age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, and HbA_1c; model 2 adjusted by age, sex, duration of diabetes, use of antidiabetic agents, HR, SBP, PP, height, weight, BMI, HbA_1c, and TC. ^#Standardized β coefficients (total, direct, and indirect effects) derived from regression-based mediation analysis. ^‡Calculated by $\frac{a\text{*}b}{\left(a\text{*}b\right)+c^{\prime }}$.

Abbreviations: DR, diabetic retinopathy; TyG, triglyceride–glucose; HOMA-IR, homeostasis-model assessment of insulin resistance.