甘油三酯葡萄糖指数联合肥胖指标与糖尿病视网膜病变的相关性

doi:10.3969/j.issn.1004-583X.2024.07.005

摘要/Abstract

摘要：

目的本研究旨在探讨甘油三酯葡萄糖指数(triglycerides-glucose index,TyG)及TyG联合肥胖指标与2型糖尿病(type 2 diabetes mellitus,T2DM)患者视网膜病变(diabetic retinopathy,DR)的相关性。分析TyG指数及TyG联合肥胖指标对DR的预测价值。方法本研究为回顾性研究,依据纳入标准以及排除标准,共收集了2018年9月至2021年5月于河北省人民医院内分泌科住院治疗的373名T2DM患者资料,依据是否合并DR,将其分为T2DM未合并DR组及合并DR组。收集患者临床资料,计算指标TyG、甘油三酯葡萄糖-腰围指数(triglyceride-glucose-waist circumference index,TyG-WC)、甘油三酯葡萄糖-体重指数(triglyceride-glucose-body mass index,TyG-BMI)、甘油三酯葡萄糖-腰臀比指数(tyG-waist-to-hip ratio,TyG-WHR)、甘油三酯葡萄糖-腰围身高比指数(tyG-waist-to-height ratio,TyG-WHtR)。采用二元Logistic回归分析其危险因素,绘制ROC曲线来评估TyG、TyG-WC、TyG-BMI、TyG-WHR、TyG-WHtR对DR的预测价值。结果 ①T2DM合并DR组的年龄、糖尿病病程、腰围、WHR、WHtR、甘油三酯、肌酐、尿素氮、空腹血糖、糖化血红蛋白、TyG、TyG-WC、TyG-BMI、TyG-WHR、TyG-WHtR均高于未合并DR组,肾小球滤过率低于未合并DR组。② DR与年龄、糖尿病病程、腰围、WHR、WHtR、甘油三酯、肌酐、尿素氮、空腹血糖、糖化血红蛋白、TyG、TyG-WC、TyG-BMI、TyG-WHR、TyG-WHtR呈正相关,与肾小球滤过率呈负相关。③TyG、TyG-WC、TyG-BMI、TyG-WHR、TyG-WHtR均是DR的独立危险因素。④ROC分析显示,TyG、TyG-WC、TyG-BMI、TyG-WHR、TyG-WHtR均对DR有预测价值,且TyG-WHR的AUC(0.623)最大。结论 TyG-WHR与DR密切相关,有望成为早期识别DR风险的一种新的临床有效标志物。

关键词: 糖尿病, 2型, 糖尿病视网膜病变, 甘油三酯葡萄糖乘积, 腰臀比, 肥胖指标

Abstract:

Objective To investigate the correlation of triglyceride-glucose index (TyG) and TyG combined with obesity indicators with diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM), and to analyze the predictive value of TyG and its combination with obesity indicators in DR. Methods This was a retrospective study. According to the inclusion and exclusion criteria, a total of 373 T2DM patients hospitalized in the Department of Endocrinology of Hebei General Hospital from September 2018 to May 2021 were recruited. They were assigned into T2DM group and DR group according to the presence of DR or not. The clinical data were collected. TyG, TyG-waist circumference index (TyG-WC), TyG-body mass index (TyG-BMI), TyG-waist-to-hip ratio (TyG-WHR), and TyG-waist-to-height ratio (TyG-WHtR) were calculated. Risk factors for DR were identified by binary logistic regression. The receiver operating characteristic (ROC) curves were plotted to determine the role of TyG, TyG-WC, TyG-BMI, TyG-WHR and TyG-WHtR in predicting DR. Results Patients in DR group had significantly higher age, course of T2DM, WC, WHR, WHtR, triglyceride (TG), serum creatinine (SCr), blood urea nitrogen (BUN), fasting blood glucose (FBG), glycosylated hemoglobin (HbA₁c), TyG, TyG-WC, TyG-BMI, TyG-WHR and TyG-WHtR, but lower glomerular filtration (GFR) than those of T2DM group (P<0.05). DR was positively correlated with age, course of T2DM, WC, WHR, WHtR, TG, SCr, BUN, FBG, HbA₁c, TyG, TyG-WC, TyG-BMI, TyG-WHR and TyG-WHtR, but negatively correlated with GFR. TyG, TyG-WC, TyG-BMI, TyG-WHR and TyG-WHtR were independent risk factors for DR. ROC curves showed the potential of TyG, TyG-WC, TyG-BMI, TyG-WHR and TyG-WHtR for predicting DR, with the largest area under the curve (AUC) of 0.623 in TyG-WHR. Conclusion TyG-WHR is closely related to DR in T2DM patients, and it may be a new clinical effective marker for early identification of the risk of DR in T2DM patients.

Key words: diabetes mellitus, type 2, diabetic retinopathy, triglyceride glucose product, waist-hip ratio, obesity index

中图分类号:

R587.26

延天美, 吴亚楠, 刘月影, 魏立民. 甘油三酯葡萄糖指数联合肥胖指标与糖尿病视网膜病变的相关性[J]. 临床荟萃, 2024, 39(7): 612-619.

Yan Tianmei, Wu Yanan, Liu Yueying, Wei Limin. Correlation of triglyceride-glucose index combined with obesity indicators with diabetic retinopathy[J]. Clinical Focus, 2024, 39(7): 612-619.

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链接本文: https://huicui.hebmu.edu.cn/CN/10.3969/j.issn.1004-583X.2024.07.005

https://huicui.hebmu.edu.cn/CN/Y2024/V39/I7/612

图/表 12

表1 两组一般资料比较

Tab.1 General data between groups

组别		例数	性别(男) [例(%)]		吸烟史 [例(%)]		饮酒史 [例(%)]		年龄 (岁)		糖尿病病程 (月)		身高 (cm)		体重 (kg)
非DR组		261	156(59.8)		68(26.1)		64(24.5)		56(46,66)		60(12,132)		168(160,174.25)		73±13.54
DR组		112	63(56.3)		32(28.6)		28(25.0)		61(50,67)		144(84,240)		168(159,172)		74(66,82)
χ²/ $Z$ / $t$ 值			0.401		1.256		0.443		-2.300		-7.065		-0.856		-0.990
P值			0.527		0.262		0.506		0.021		<0.001		0.392		0.322
组别	BMI (kg/m²)			WC (cm)		臀围 (cm)		WHR		WHtR		SBP (mmHg)		DBP (mmHg)
非DR组	25.95±3.54			92(86,100)		100.36±9.22		0.93(0.88,0.96)		0.55±0.06		132(121,146)		83.07±12.39
DR组	26.37(24.58,28.73)			95(88,101)		100(96,105)		0.94±0.07		0.56(0.53,0.61)		136(121,150)		81.39±11.66
$t$ / $Z$ 值	-1.683			-2.093		-0.335		-2.435		-2.405		-1.775		1.497
P值	0.092			0.036		0.738		0.015		0.016		0.076		0.135

表1 两组一般资料比较

Tab.1 General data between groups

组别		例数	性别(男) [例(%)]		吸烟史 [例(%)]		饮酒史 [例(%)]		年龄 (岁)		糖尿病病程 (月)		身高 (cm)		体重 (kg)
非DR组		261	156(59.8)		68(26.1)		64(24.5)		56(46,66)		60(12,132)		168(160,174.25)		73±13.54
DR组		112	63(56.3)		32(28.6)		28(25.0)		61(50,67)		144(84,240)		168(159,172)		74(66,82)
χ²/ $Z$ / $t$ 值			0.401		1.256		0.443		-2.300		-7.065		-0.856		-0.990
P值			0.527		0.262		0.506		0.021		<0.001		0.392		0.322
组别	BMI (kg/m²)			WC (cm)		臀围 (cm)		WHR		WHtR		SBP (mmHg)		DBP (mmHg)
非DR组	25.95±3.54			92(86,100)		100.36±9.22		0.93(0.88,0.96)		0.55±0.06		132(121,146)		83.07±12.39
DR组	26.37(24.58,28.73)			95(88,101)		100(96,105)		0.94±0.07		0.56(0.53,0.61)		136(121,150)		81.39±11.66
$t$ / $Z$ 值	-1.683			-2.093		-0.335		-2.435		-2.405		-1.775		1.497
P值	0.092			0.036		0.738		0.015		0.016		0.076		0.135

表2 两组生化指标比较[ M(P25,P75)]

Tab.2 Biochemical indicators between groups[ M(P25,P75)]

组别	例数	TC(mmol/L)		TG(mmol/L)		LDL-C(mmol/L)		HDL-C(mmol/L)		SCr(mmol/L)
非DR组	261	4.785(4.04, 5.53)		1.44(0.99, 2.02)		3.105(2.54, 3.68)		1.1(0.99, 1.28)		67.9(59.18, 74.1)
DR组	112	4.9(4.31, 5.86)		1.56(1.15, 2.44)		3.15(2.75, 3.86)		1.08(0.88, 1.24)		70.3(59.9, 85.7)
$Z$ 值		-1.363		-2.321		-1.269		-1.607		-3.024
P值		0.173		0.020		0.204		0.108		0.002
组别	BUN(mmol/L)		UA(mmol/L)		GFR (mL/min)		FBG(mmol/L)		HbA₁c(%)
非DR组	5.2(4.4, 6)		304.64(240.75, 356)		98.79(88.76, 107.3)		7.61(6.1, 9.485)		8.3(7.1, 9.9)
DR组	5.5(4.6, 7.3)		318.5(260.3, 371.3)		92.87(70.84, 103.07)		8.375(6.63, 11.585)		8.9(7.5, 10.7)
$Z$ 值	-3.197		-1.436		-3.924		-2.845		-2.810
P值	0.001		0.151		<0.001		0.004		0.005

表2 两组生化指标比较[ M(P25,P75)]

Tab.2 Biochemical indicators between groups[ M(P25,P75)]

组别	例数	TC(mmol/L)		TG(mmol/L)		LDL-C(mmol/L)		HDL-C(mmol/L)		SCr(mmol/L)
非DR组	261	4.785(4.04, 5.53)		1.44(0.99, 2.02)		3.105(2.54, 3.68)		1.1(0.99, 1.28)		67.9(59.18, 74.1)
DR组	112	4.9(4.31, 5.86)		1.56(1.15, 2.44)		3.15(2.75, 3.86)		1.08(0.88, 1.24)		70.3(59.9, 85.7)
$Z$ 值		-1.363		-2.321		-1.269		-1.607		-3.024
P值		0.173		0.020		0.204		0.108		0.002
组别	BUN(mmol/L)		UA(mmol/L)		GFR (mL/min)		FBG(mmol/L)		HbA₁c(%)
非DR组	5.2(4.4, 6)		304.64(240.75, 356)		98.79(88.76, 107.3)		7.61(6.1, 9.485)		8.3(7.1, 9.9)
DR组	5.5(4.6, 7.3)		318.5(260.3, 371.3)		92.87(70.84, 103.07)		8.375(6.63, 11.585)		8.9(7.5, 10.7)
$Z$ 值	-3.197		-1.436		-3.924		-2.845		-2.810
P值	0.001		0.151		<0.001		0.004		0.005

表3 两组TyG及TyG联合肥胖指标比较

Tab.3 TyG and TyG combined with obesity indicators between groups

组别	例数	TyG	TyG-WC	TyG-BMI	TyG-WHR	TyG-WHtR
非DR组	261	10.26±0.43	942.36(878.89, 1016.43)	266.32±38.74	9.48(8.98, 9.98)	5.63(5.24, 6.05)
DR组	112	10.43±0.44	975.19(906.71, 1055.61)	275.08(251.63, 303.48)	9.83±0.83	5.86(5.43, 6.48)
$t$ / $Z$ 值		-3.581	-3.151	-2.587	-3.762	-3.437
P值		<0.001	0.002	0.010	<0.001	0.001

表3 两组TyG及TyG联合肥胖指标比较

Tab.3 TyG and TyG combined with obesity indicators between groups

组别	例数	TyG	TyG-WC	TyG-BMI	TyG-WHR	TyG-WHtR
非DR组	261	10.26±0.43	942.36(878.89, 1016.43)	266.32±38.74	9.48(8.98, 9.98)	5.63(5.24, 6.05)
DR组	112	10.43±0.44	975.19(906.71, 1055.61)	275.08(251.63, 303.48)	9.83±0.83	5.86(5.43, 6.48)
$t$ / $Z$ 值		-3.581	-3.151	-2.587	-3.762	-3.437
P值		<0.001	0.002	0.010	<0.001	0.001

图1 两组TyG及TyG联合肥胖指标的箱式图 a. TyG;b. TyG-WC;c. TyG-BMI;d. TyG-WHR;e. TyG-WHtR。与非DR组比较,*P<0.05

Fig.1 Box plots of TyG and TyG combined with obesity indicators in the two groups a. TyG; b. TyG-WC; c. TyG-BMI; d. TyG-WHR; e. TyG-WHtR

表4 T2DM合并DR与各指标的相关性分析

Tab.4 Correlation analysis between DR and various indicators in T2DM patients

	T2DM合并DR
	$r$ 值	P值
年龄(岁)	0.119	0.021
性别	0.033	0.528
糖尿病病程(月)	0.366	<0.001
WC(cm)	0.109	0.036
WHR	0.126	0.015
WHtR	0.125	0.016
TC(mmol/L)	0.071	0.173
TG(mmol/L)	0.120	0.020
LDL-C(mmol/L)	0.066	0.205
HDL-C(mmol/L)	-0.083	0.108
SCr(mmol/L)	0.157	0.002
BUN(mmol/L)	0.166	0.001
UA(mmol/L)	0.074	0.151
GFR (mL/min)	-0.204	<0.001
FBG(mmol/L)	0.148	0.004
HbA₁c(%)	0.147	0.005
TyG	0.165	0.001
TyG-WC	0.163	0.002
TyG-BMI	0.134	0.010
TyG-WHR	0.195	<0.001
TyG-WHtR	0.178	0.001

表4 T2DM合并DR与各指标的相关性分析

Tab.4 Correlation analysis between DR and various indicators in T2DM patients

	T2DM合并DR
	$r$ 值	P值
年龄(岁)	0.119	0.021
性别	0.033	0.528
糖尿病病程(月)	0.366	<0.001
WC(cm)	0.109	0.036
WHR	0.126	0.015
WHtR	0.125	0.016
TC(mmol/L)	0.071	0.173
TG(mmol/L)	0.120	0.020
LDL-C(mmol/L)	0.066	0.205
HDL-C(mmol/L)	-0.083	0.108
SCr(mmol/L)	0.157	0.002
BUN(mmol/L)	0.166	0.001
UA(mmol/L)	0.074	0.151
GFR (mL/min)	-0.204	<0.001
FBG(mmol/L)	0.148	0.004
HbA₁c(%)	0.147	0.005
TyG	0.165	0.001
TyG-WC	0.163	0.002
TyG-BMI	0.134	0.010
TyG-WHR	0.195	<0.001
TyG-WHtR	0.178	0.001

表5 T2DM合并DR与TyG的回归分析

Tab.5 Regression analysis of DR and TyG in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.940	0.271	12.032	0.001	2.561	1.505	4.356
model2	1.190	0.309	14.823	<0.001	3.288	1.794	6.025
model3	0.921	0.466	3.911	0.048	2.513	1.008	6.261

表5 T2DM合并DR与TyG的回归分析

Tab.5 Regression analysis of DR and TyG in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.940	0.271	12.032	0.001	2.561	1.505	4.356
model2	1.190	0.309	14.823	<0.001	3.288	1.794	6.025
model3	0.921	0.466	3.911	0.048	2.513	1.008	6.261

表6 T2DM合并DR与TyG-WC的回归分析

Tab.6 Regression analysis of DR and TyG-WC in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.003	0.001	11.500	0.001	1.003	1.001	1.005
model2	0.013	0.003	15.313	<0.001	1.013	1.006	1.020
model3	0.011	0.005	4.634	0.031	1.011	1.001	1.021

表6 T2DM合并DR与TyG-WC的回归分析

Tab.6 Regression analysis of DR and TyG-WC in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.003	0.001	11.500	0.001	1.003	1.001	1.005
model2	0.013	0.003	15.313	<0.001	1.013	1.006	1.020
model3	0.011	0.005	4.634	0.031	1.011	1.001	1.021

表7 T2DM合并DR与TyG-BMI的回归分析

Tab.7 Regression analysis of DR and TyG-BMI in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.009	0.003	10.578	0.001	1.009	1.004	1.014
model2	0.016	0.005	11.526	0.001	1.016	1.007	1.026
model3	0.020	0.006	11.506	0.031	1.020	1.009	1.032

表7 T2DM合并DR与TyG-BMI的回归分析

Tab.7 Regression analysis of DR and TyG-BMI in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.009	0.003	10.578	0.001	1.009	1.004	1.014
model2	0.016	0.005	11.526	0.001	1.016	1.007	1.026
model3	0.020	0.006	11.506	0.031	1.020	1.009	1.032

表8 T2DM合并DR与TyG-WHR的回归分析

Tab.8 Regression analysis of DR and TyG-WHR in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.572	0.144	15.650	<0.001	1.771	1.334	2.351
model2	1.297	0.330	15.437	<0.001	3.660	1.916	6.991
model3	1.044	0.496	4.436	0.035	2.840	1.075	7.503

表8 T2DM合并DR与TyG-WHR的回归分析

Tab.8 Regression analysis of DR and TyG-WHR in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.572	0.144	15.650	<0.001	1.771	1.334	2.351
model2	1.297	0.330	15.437	<0.001	3.660	1.916	6.991
model3	1.044	0.496	4.436	0.035	2.840	1.075	7.503

表9 T2DM合并DR与TyG-WHtR的回归分析

Tab.9 Regression analysis of DR and TyG-WHtR in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.594	0.162	13.374	<0.001	1.811	1.317	2.490
model2	2.135	0.549	15.108	<0.001	8.455	2.882	24.810
model3	1.793	0.833	4.632	0.031	6.008	1.174	30.751

表9 T2DM合并DR与TyG-WHtR的回归分析

Tab.9 Regression analysis of DR and TyG-WHtR in T2DM patients

	回归系数	标准误	wald χ²值	P值	$O R$ 值	95% $C I$
	回归系数	标准误	wald χ²值	P值	$O R$ 值	下限	上限
model1	0.594	0.162	13.374	<0.001	1.811	1.317	2.490
model2	2.135	0.549	15.108	<0.001	8.455	2.882	24.810
model3	1.793	0.833	4.632	0.031	6.008	1.174	30.751

图2 各指标预测T2DM合并DR的ROC曲线

Fig.2 ROC curve of each index in predicting DR

表10 各指标对T2DM合并DR的预测价值

Tab.10 Predictive value of each index for DR in T2DM patients

	AUC	95% $C I$		P值	敏感度	特异性	约登指数	界值
	AUC	下限	上限	P值	敏感度	特异性	约登指数	界值
TyG	0.604	0.541	0.667	0.001	0.670	0.525	0.195	10.2834
TyG-WC	0.603	0.540	0.666	0.002	0.473	0.713	0.186	999.6353
TyG-BMI	0.584	0.521	0.428	0.010	0.696	0.441	0.137	259.0222
TyG-WHR	0.623	0.560	0.686	<0.001	0.527	0.678	0.205	9.8027
TyG-WHtR	0.612	0.549	0.676	0.001	0.571	0.636	0.207	5.8247

表10 各指标对T2DM合并DR的预测价值

Tab.10 Predictive value of each index for DR in T2DM patients

	AUC	95% $C I$		P值	敏感度	特异性	约登指数	界值
	AUC	下限	上限	P值	敏感度	特异性	约登指数	界值
TyG	0.604	0.541	0.667	0.001	0.670	0.525	0.195	10.2834
TyG-WC	0.603	0.540	0.666	0.002	0.473	0.713	0.186	999.6353
TyG-BMI	0.584	0.521	0.428	0.010	0.696	0.441	0.137	259.0222
TyG-WHR	0.623	0.560	0.686	<0.001	0.527	0.678	0.205	9.8027
TyG-WHtR	0.612	0.549	0.676	0.001	0.571	0.636	0.207	5.8247

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