Association between sensitivity to thyroid hormones and non-high-density lipoprotein cholesterol levels in patients with type 2 diabetes mellitus

doi:10.4239/wjd.v15.i10.2081

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World Journal of Diabetes

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Baishideng Publishing Group Inc, 7041 Koll Center Parkway, Suite 160, Pleasanton, CA 94566, USA

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World J Diabetes. Oct 15, 2024; 15(10): 2081-2092
Published online Oct 15, 2024. doi: 10.4239/wjd.v15.i10.2081

Table 1 Basic characteristics of the population

Characteristics	All (n = 994)	Non-HDL-C levels (mmol/L)			P value
Characteristics	All (n = 994)	< 3.4 (n = 605)	3.4-4.9 (n = 316)	> 4.9 (n = 73)	P value
Age (years)	65.8 (35.0-89.0)	66.0 (36.0-89.0)	64.0 (35.0-86.0)	64.0 (36.0-83.6)	0.010
Sex (male/female)	447/547	278/327	140/176	29/44	0.576
Disease duration of T2DM (years)	13.0 (0.0-40.0)	13.0 (0.0-35.0)	13.0 (0.0-40.0)	11.0 (0.02-30.0)	0.336
BMI (kg/m²)	25.6 (14.38-47.97)	25.6 (14.38-45.45)	25.6 (16.0-47.9)	25.6 (19.5-41.1)	0.743
SBP (mmHg)	130 (90-210)	130 (90-190)	130 (90-210)	130 (110-180)	0.294
DBP (mmHg)	80 (50-120)	80 (50-120)	80 (50-110)	80 (60-100)	0.162
FPG (mmol/L)	8.22 (2.88-24.52)	7.79 (3.12-24.17)	8.84 (2.88-23.49)	9.97 (3.25-24.52)	< 0.001
Fasting C peptide (ng/mL)	2.30 (0.01-16.34)	2.21 (0.01-13.35)	2.37 (0.17-16.34)	2.78 (0.27-6.93)	0.008
HOMA-IR	4.47 (0.04-279.63)	4.22 (0.05-243.20)	4.74 (0.47-279.63)	5.43 (0.04-34.27)	0.047
HbA1c (%)	8.1 (4.9-15.1)	7.8 (4.9-14.8)	8.7 (5.4-15.1)	9.2 (6.0-14.7)	< 0.001
Creatinine (μmoI/L)	62 (28-266)	62 (30-241)	60 (28-230)	65 (30-266)	0.016
eGFR [mL/min (1.73 m²)^-1]	101.1 (19.1-323.7)	100.7 (21.1-291.4)	103.5 (19.1-323.7)	95.0 (22.4-284.9)	0.009
UA (mmol/L)	324 (7-811)	324 (7-811)	321 (98-797)	338 (209-612)	0.126
UACR (mg/g)	4.0 (0.0-2404.2)	4.1 (0.0-1637.8)	2.6 (0.0-1796.2)	12.8 (0.1-2402.2)	0.013
25(OH)D (ng/mL)	16.80 (3.00-57.55)	17.52 (3.00-57.55)	16.57 (3.00-50.21)	14.73 (3.31-35.78)	0.039
Fatty liver, n (%)	533 (54.1)	304 (50.6)	180 (57.7)	49 (67.1)	0.002
Hypertension, n (%)	561 (56.8)	344 (57.2)	172 (54.8)	45 (61.6)	0.530
Cardiovascular disease, n (%)	155 (27.5)	111 (33.5)	34 (82.9)	10 (24.4)	0.002
Diabetic retinopathy, n (%)	238 (24.1)	142 (23.6)	68 (21.8)	28 (38.4)	0.011
Diabetic peripheral neuropathy, n (%)	411 (41.7)	248 (41.2)	123 (49.5)	40 (54.8)	0.055
Diabetic peripheral vascular disease, n (%)	157 (38.8)	89 (38.5)	55 (38.5)	13 (41.9)	0.931
Serum lipid level (mmol/L)
TG	1.35 (0.24-21.80)	1.37 (0.24-8.59)	1.69 (0.39-9.99)	2.51 (0.63-21.80)	< 0.001
TC	4.25 (2.03-10.35)	3.74 (2.03-5.74)	5.07 (4.13-7.20)	6.53 (5.58-10.35)	< 0.001
LDL-C	2.51 (0.15-6.88)	2.08 (0.15-3.80)	3.28 (1.12-4.66)	4.32 (1.37-6.88)	< 0.001
HDL-C	1.10 (0.33-3.42)	1.10 (0.33-3.42)	1.10 (0.47-2.66)	1.09 (0.58-1.90)	0.896
non-HDL-C	3.10 (1.02-9.30)	2.56 (1.02-3.39)	3.95 (3.40-4.89)	5.3 (4.90-9.30)	< 0.001
RC	0.53 (-1.31-7.93)	0.45 (-1.31-2.40)	0.67 (-0.34-3.66)	1.13 (-0.33-7.93)	< 0.001
Thyroid function and indices of thyroid hormone sensitivity
FT3 (pg/mL)	2.93 (0.91-4.49)	2.93 (0.91-4.19)	2.97 (1.01-4.49)	2.80 (1.15-3.97)	0.006
FT4 (ng/dL)	1.19 (0.72-1.59)	1.18 (0.72-1.92)	1.18 (0.75-1.96)	1.21 (0.76-1.59)	0.905
TSH (uIU/mL)	1.74 (0.01-9.89)	1.65 (0.07-9.89)	1.86 (0.07-9.48)	2.03 (0.16-9.12)	0.017
FT3/FT4	2.47 ± 0.47	2.47 ± 0.47	2.48 ± 0.45	2.34 ± 0.52	0.040
TT4RI	2.10 (0.01-12.23)	1.99 (0.10-9.89)	2.27 (0.1-12.23)	2.56 (0.20-8.43)	0.008
TSHI	0.72 (-4.43-2.42)	0.66 (-2.48-2.42)	0.79 (-4.43-2.42)	0.91 (-1.66-2.63)	0.010
TFQI	0.00 ± 0.35	-0.02 ± 0.36	0.03 ± 0.34	0.08 ± 0.34	0.026

The data are expressed as the means ± SDs, medians (upper and lower quartiles) or n (%). BMI: body mass index; SBP: systolic blood pressure; DBP: diastolic blood pressure; eGFR: estimated glomerular filtration rate; UA: uric acid; UACR: urinary albumin-creatinine ratio; FPG: fasting plasma glucose; HbA1c: glycosylated hemoglobin; TG: triglycerides; TC: total cholesterol; LDL-C: low-density lipoprotein cholesterol; HDL-C: high-density lipoprotein cholesterol; non-HDL-C: Non-high-density lipoprotein cholesterol; RC: remnant cholesterol; T2DM: Type 2 diabetes mellitus; HOMA-IR: Homeostasis Model Assessment of insulin resistance; 25(OH)D: 25-hydroxyvitamin D; FT3: Free triiodothyronine; FT4: Free thyrotropin; TSH: Thyroid-stimulating hormone; TSHI: Thyroid-stimulating hormone index; TT4RI: Thyrotrophic T4 resistance index; TFQI: Thyroid feedback quantile-based index.

Table 2 Correlations between non-high-density lipoprotein cholesterol levels and thyroid parameters in patients with type 2 diabetes mellitus

Variables		All		Male		Female
Variables		r	P value	r	P value	r	P value
FT3 (pg/mL)	Model 1	-0.090^a	0.005	-0.153^a	0.001	-0.062	0.147
	Model 2	-0.128^a	< 0.001	-0.187^a	< 0.001	-0.095	0.027
	Model 3	-0.113^a	< 0.001	-0.168^a	< 0.001	-0.082	0.059
FT4 (ng/dL)	Model 1	-0.008	0.795	-0.115^b	0.015	0.014	0.737
	Model 2	-0.013	0.693	-0.118^b	0.013	0.012	0.78
	Model 3	-0.024	0.451	-0.14^a	0.003	0	0.991
TSH (uIU/mL)	Model 1	0.073^b	0.022	0.141^a	0.003	0.007	0.867
	Model 2	0.079^b	0.014	0.143^a	0.002	0.016	0.714
	Model 3	0.093^a	0.004	0.154^a	0.001	0.024	0.575
FT3/FT4	Model 1	-0.051	0.107	-0.019	0.694	-0.075	0.078
	Model 2	-0.076^b	0.017	-0.037	0.441	-0.101^b	0.019
	Model 3	-0.033	0.301	-0.003	0.942	-0.052	0.228
TT4RI	Model 1	0.076^b	0.018	0.121^b	0.01	0.037	0.394
	Model 2	0.079^b	0.013	0.121^b	0.011	0.044	0.308
	Model 3	0.088^a	0.006	0.129^a	0.007	0.046	0.286
TSHI	Model 1	0.085^a	0.008	0.129^a	0.006	0.052	0.224
	Model 2	0.087^a	0.006	0.129^a	0.007	0.058	0.175
	Model 3	0.103^a	0.001	0.14^a	0.003	0.069	0.111
TFQI	Model 1	0.078^b	0.014	0.029	0.539	0.121^a	0.004
	Model 2	0.074^b	0.02	0.024	0.612	0.121^a	0.005
	Model 3	0.065^b	0.044	0.014	0.777	0.109^b	0.011

^aP < 0.01.

^bP < 0.05.

Model 1 was an unadjusted analysis. Model 2 was adjusted for age and sex. Model 3 was adjusted for age, sex, body mass index, and glycosylated hemoglobin. FT3: Free triiodothyronine; FT4: Free thyrotropin; TSH: Thyroid-stimulating hormone; TSHI: Thyroid-stimulating hormone index; TT4RI: Thyrotrophic T4 resistance index; TFQI: Thyroid feedback quantile-based index.

Table 3 Relationships between lipid profiles and thyroid-associated variables

Variables		TG		TC		LDL-C		HDL-C		RC
Variables		r	P value	r	P value	r	P value	r	P value	r	P value
FT3 (pg/mL)	Model 1	-0.092^a	0.004	-0.116^a	< 0.001	-0.086^a	0.007	-0.093^a	0.004	-0.037	0.246
	Model 2	-0.114^a	< 0.001	-0.149^a	< 0.001	-0.106^a	0.001	-0.083^a	0.009	-0.081^b	0.011
	Model 3	-0.099^a	0.002	-0.137^a	< 0.001	-0.094^a	0.003	-0.097^a	0.003	-0.068^b	0.035
FT4 (ng/dL)	Model 1	-0.007	0.838	0.001	0.971	0.008	0.8	0.03	0.352	-0.032	0.312
	Model 2	-0.01	0.764	-0.003	0.928	0.006	0.84	0.03	0.349	-0.039	0.224
	Model 3	-0.02	0.535	-0.012	0.717	-0.002	0.948	0.037	0.249	-0.048	0.139
TSH (uIU/mL)	Model 1	0.074^b	0.021	0.045	0.157	0.04	0.206	-0.080^b	0.013	0.083^a	0.01
	Model 2	0.077^b	0.016	0.05	0.12	0.043	0.177	-0.082^b	0.01	0.09^a	0.005
	Model 3	0.082^b	0.01	0.063	0.05	0.056	0.084	-0.08^b	0.012	0.095^a	0.003
FT3/FT4	Model 1	-0.082^b	0.01	-0.093^a	0.003	-0.065^b	0.041	-0.141^a	< 0.001	0.008	0.802
	Model 2	-0.095^a	0.003	-0.114^a	< 0.001	-0.078^b	0.015	-0.134^a	< 0.001	-0.021	0.519
	Model 3	-0.061	0.06	-0.082^b	0.011	-0.045	0.167	-0.163^a	< 0.001	0.01	0.749
TT4RI	Model 1	0.079^b	0.013	0.052	0.102	0.046	0.147	-0.066^b	0.039	0.078^b	0.014
	Model 2	0.081^b	0.011	0.055	0.087	0.048	0.133	-0.068^b	0.034	0.082^b	0.01
	Model 3	0.081^b	0.012	0.065^b	0.043	0.057	0.075	-0.061	0.057	0.083^b	0.01
TSHI	Model 1	0.099^a	0.002	0.061	0.056	0.048	0.135	-0.066^b	0.039	0.095^a	0.003
	Model 2	0.1^a	0.002	0.063^b	0.049	0.049	0.126	-0.067^b	0.036	0.098^a	0.002
	Model 3	0.103^a	0.001	0.079^b	0.014	0.064^b	0.047	-0.059	0.065	0.102^a	0.002
TFQI	Model1	0.087^a	0.006	0.074^b	0.02	0.059	0.066	-0.003	0.922	0.061	0.054
	Model2	0.085^a	0.008	0.071^b	0.026	0.056	0.078	< 0.001	0.989	0.057	0.076
	Model3	0.068^b	0.035	0.068^b	0.035	0.052	0.106	0.02	0.529	0.043	0.181

^aP < 0.01

^bP < 0.05.

Table 4 Logistic regression analysis of the relationship between non-high-density lipoprotein cholesterol and impaired sensitivity to thyroid hormones in patients with type 2 diabetes mellitus

Variables	All		Male		Female
Variables	OR (95%CI)	P value	OR (95%CI)	P value	OR (95%CI)	P value
FT3 (pg/mL)	0.91 (0.71-1.166)	0.456	0.698 (0.41-1.191)	0.187	1.002 (0.769-1.306)	0.987
FT4 (ng/dL)	0.919 (0.689-1.225)	0.564	0.194 (0.061-0.617)	0.005	1.012 (0.775-1.32)	0.932
TSH (uIU/mL)	1.091 (1.015-1.172)	0.018	1.136 (1.02-1.264)	0.02	1.037 (0.935-1.15)	0.49
FT3/FT4	1.01 (0.754-1.352)	0.949	1.369 (0.861-2.177)	0.184	0.846 (0.577-1.24)	0.392
TT4RI	1.075 (1.006-1.149)	0.032	1.086 (0.985-1.197)	0.097	1.055 (0.963-1.156)	0.252
TSHI	1.238 (1.034-1.482)	0.02	1.331 (1.003-1.766)	0.048	1.155 (0.918-1.452)	0.218
TFQI	1.584 (1.088-2.304)	0.016	0.961 (0.545-1.692)	0.89	2.337 (1.4-3.901)	0.001

Data were analyzed via logistic regression analysis adjusted for age, sex, body mass index and glycosylated hemoglobin. FT3: Free triiodothyronine; FT4: Free thyrotropin; TSH: Thyroid-stimulating hormone; TSHI: Thyroid-stimulating hormone index; TT4RI: Thyrotrophic T4 resistance index; TFQI: Thyroid feedback quantile-based index.

Citation: Duan XY, Fu JL, Sun LN, Mu ZJ, Xiu SL. Association between sensitivity to thyroid hormones and non-high-density lipoprotein cholesterol levels in patients with type 2 diabetes mellitus. World J Diabetes 2024; 15(10): 2081-2092
URL: https://www.wjgnet.com/1948-9358/full/v15/i10/2081.htm
DOI: https://dx.doi.org/10.4239/wjd.v15.i10.2081