Subclinical Hypothyroidism Represents Visceral Adipose Indices, Especially in Women With Cardiovascular Risk

Meng-Ting Tsou

J Endo Soc. 2021;5(6)

Conclusion

SCH participants who were at an intermediate-to-high risk of developing CAD (AR_10y) were significantly more likely to exhibit region-specific CV fat tissue (TAT) and noninvasive visceral adipose indices (CVAI and BRI) than EU individuals, especially in Taiwanese women. These findings suggest that mild thyroid failure also independently contributes to the development of abnormal fatty distribution.

1 2 3 4 5

Next Section

Abbreviations
ABSI, a body shape index; AR_10y, absolute risk of cardiovascular event in 10 years; BMI, body mass index; BRI, body roundness index; CV, cardiovascular; CVAI, Chinese visceral adiposity index; CVD, cardiovascular disease; DM, diabetes mellitus; EAT, epicardial adipose tissue; EU, euthyroid; FRS, Framingham risk score; FT4, free thyroxine; HDL-C, high-density lipoprotein cholesterol; HTN, hypertension; LDL-C, low-density lipoprotein cholesterol; MDCT, multidetector computed tomography; Mets, metabolic syndrome; OR, odds ratio; PCF, pericardial fat; SBP, systolic blood pressure; SCH, subclinical hypothyroidism; TAT, thoracic periaortic fat; TG, triglycerides; TSH, thyrotropin; VAT, visceral adipose tissue; WC, waist circumference.

Additional Information
Data Availability
The data used in this study are available from the corresponding author on reasonable request.

Table 1. Baseline characteristics according to thyroid functional status by sex
Variables	Men (N = 1151)			Women (N = 493)
	SCH	EU	P	SCH	EU	P
	(n = 73)	(n = 1078)	P	(n = 52)	(n = 441)	P
Age, y	52.23 ± 10.29	48.76 ± 9.64	.003	53.83 ± 10.00	51.44 ± 9.85	.10
TSH, μIU/mL	5.82 ± 1.75	1.90 ± 0.78	< .001	6.12 ± 2.63	1.96 ± 0.81	< .001
FT4, ng/dL	1.26 ± 0.13	1.33 ± 0.15	< .001	1.20 ± 0.13	1.28 ± 0.15	.001
Smoking, n (%)	16 (21.9%)	219 (20.3%)	.74	0 (0.0%)	10 (2.3%)	.61
Diabetes, n (%)	5 (6.8%)	80 (7.4%)	.86	3(5.8%	29 (6.6%)	.99
HTN, n (%)	23 (31.5%)	226 (21.0%)	.03	11 (21.2%)	66 (15.0%)	.25
BMI	25.08 ± 3.18	25.29 ± 3.51	.62	24.43 ± 3.75	23.21 ± 3.43	.02
WC, cm	86.40 ± 13.52	87.45 ± 9.15	.36	80.26 ± 9.07	77.83 ± 9.37	.08
Obesity, n (%)	17 (23.3%)	285 (26.4%)	.55	10 (19.2%)	60 (13.6%)	.27
SBP, mm Hg	122.89 ± 15.81	123.52 ± 16.43	.75	122.58 ± 21.66	119.14 ± 18.29	.21
DBP, mm Hg	78.11 ± 11.11	78.24 ± 10.15	.91	72.98 ± 10.62	73.23 ± 10.37	.87
FPG, mg/dL	104.26 ± 28.63	103.97 ± 26.55	.93	98.75 ± 16.87	98.27 ± 20.39	.87
PPG, mg/dL	132.73 ± 63.56	124.63 ± 54.61	.24	124.35 ± 39.99	124.24 ± 42.37	.99
HbA_1c, %	6.03 ± 1.00	5.89 ± 0.95	.23	5.72 ± 0.57	5.80 ± 0.75	.45
TC, mg/dL	207.10 ± 35.25	202.60 ± 38.21	.33	208.92 ± 36.84	203.67 ± 37.97	.34
HDL-C, mg/dL	47.30 ± 11.36	48.37 ± 11.86	.45	59.87 ± 11.44	61.39 ± 15.00	.39
LDL-C, mg/dL	135.51 ± 29.32	133.22 ± 32.08	.55	131 ± 32.93	127.03 ± 34.61	.45
TGs, mg/dL	172.58 ± 128.88	156.44 ± 154.04	.38	126 ± 97.53	111.71 ± 64.06	.17
FRS (%)	15.29 ± 12.00	12.30 ± 11.62	.03	7.36 ± 8.94	5.69 ± 5.86	.19
Low AR10y, n (%)	26 (35.6%)	567 (52.6%)	.01	42 (80.8%)	360 (81.6%)	.31
Intermediate AR10y, n (%)	22 (30.1%)	277 (25.7%)		5 (9.6%)	59 (13.4%)
High AR10y, n (%)	25 (34.2%)	234 (21.7%)		5 (9.6%)	22 (5.0%)
PCF	83.04 ± 34.51	80.35 ± 31.47	.48	69.56 ± 36.37	65.35 ± 28.79	.33
TAT	8.67 ± 4.30	8.10 ± 3.90	.24	5.48 ± 3.43	4.24 ± 2.30	.01
ABSI	0.08 ± 0.01	0.08 ± 0.004	.60	0.08 ± 0.01	0.08 ± 0.01	.89
BRI	3.63 ± 1.12	3.72 ± 1.09	.51	3.69 ± 1.22	3.37 ± 1.22	.04
CVAI	98.58 ± 58.95	99.13 ± 42.10	.92	83.29 ± 36.50	69.29 ± 39.30	.01

Clinical characteristics are expressed as mean ± SD for continuous variables and n (%) for categorical variables. P values were derived from independent 2-sample t test for continuous variables, and categorical variables were expressed as percentages and compared with the χ² test or Fisher exact test.
Abbreviations: ABSI, a body shape index; AR10y, absolute risk of cardiovascular event in 10 years by FRS; BMI, body mass index; BRI, body roundness index; CVAI, Chinese visceral adiposity index; DBP, diastolic blood pressure; EU, euthyroid; FPG, fasting plasma glucose; FT4, free thyroxine; HTN, hypertension; HbA_1c, glycated hemoglobin A_1c; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; FRS, Framingham risk score; Obesity, BMI ≥ 27; PCF, pericardial fat; PPG, postprandial plasma glucose; SBP, systolic blood pressure; SCH, subclinical hypothyroidism; TAT, thoracic periaortic adipose tissue; TC, total cholesterol; TGs, triglycerides; TSH, thyrotropin; WC, waist circumference.

Table 2. Odds ratio of regional-specific cardiovascular fat tissue and noninvasive visceral adipose indices with risk of subclinical hypothyroidism
Variables	PCF^a			TAT^a			ABSI			BRI			CVAI
Variables	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P
Men
Model 1	0.97	(0.59–1.57)	.89	1.42	(0.88–2.88)	.15	1.67	(1.04–2.69)	.03	1.10	(0.67–1.79)	.71	1.10	(0.68–1.78)	.70
Model 2	0.81	(0.49–1.35)	.42	1.11	(0.66–1.85)	.70	1.39	(0.80–2.29)	.20	0.96	(0.58–1.58)	.87	0.94	(0.57–1.53)	.79
Model 3	0.81	(0.49–1.34)	.41	1.09	(0.66–1.83)	.73	1.38	(0.84–2.28)	.20	0.96	(0.58–1.57)	.86	0.93	(0.57–1.52)	.77
Model 4	0.78	(0.47–1.32)	.36	1.12	(0.65–1.92)	.69	1.37	(0.83–2.28)	.22	1.00	(0.58–1.71)	.99	0.95	(0.54–1.67)	.86
Women
Model 1	1.24	(0.62–2.46)	.54	2.43	(1.09–5.39)	.03	0.82	(0.42–1.62)	.57	2.18	(1.21–3.94)	.01	1.49	(0.74–2.97)	.26
Model 2s	0.99	(0.47–2.09)	.97	2.19	(0.98–5.31)	.05	0.71	(0.35–1.42)	.33	1.96	(1.04–3.68)	.04	1.17	(0.52–2.61)	.70
Model 3	0.98	(0.46–2.06)	.95	2.32	(1.02–5.65)	.04	0.71	(0.35–1.43)	.34	1.98	(1.05–3.72)	.03	1.21	(0.54–2.72)	.64
Model 4	1.07	(0.50–2.31)	.86	2.61	(1.03–6.97)	.04	0.70	(0.34–1.41)	.32	2.04	(1.07–3.92)	.03	1.56	(0.61–3.98)	.36

Model 1: Unadjusted.
Model 2: Adjusted for age.
Model 3: Adjusted for factors in model 2 plus smoking.
Model 4: Adjusted for factors in model 3 plus SBP, FPG, HDL-C, LDL-C, and FRS.
Abbreviations: ABSI, a body shape index; BMI, body mass index; BRI, body roundness index; CVAI, Chinese visceral adiposity index; FPG, fasting plasma glucose; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; FRS, Framingham risk score; OR, odds ratio; PCF, pericardial fat; SBP, systolic blood pressure; TAT, thoracic periaortic adipose tissue.
^aModel 3: Adjusted for factors in model 2 plus smoking and BMI.

Table 3. A comparison of the incidence of region-specific cardiovascular fat tissue and noninvasive visceral adipose indices according to thyroid functional status
Variables	Men			Women
Variables	SCH	EU	P	SCH	EU	P
PCF	83.04 ± 34.51	80.35 ± 31.47	.48	69.56 ± 36.37	65.35 ± 28.79	.33
PCF (3rd tertile, n/%)	28 (38.4%)	422 (39.1%)	.89	12 (23.1%)	86 (19.5%)	.54
TAT	8.67 ± 4.30	8.10 ± 3.90	.24	5.48 ± 3.43	4.24 ± 2.30	.01
TAT (3rd tertile, n/%)	38 (52.1%)	467 (43.3%)	.15	9 (17.3%)	35 (7.9%)	.04
ABSI	0.08 ± 0.01	0.08 ± 0.004	.60	0.08 ± 0.01	0.08 ± 0.01	.89
ABSI (3rd tertile, n/%)	35 (47.9%)	383 (35.5%)	.03	12 (23.1%)	118 (26.8%)	.57
BRI	3.63 ± 1.12	3.72 ± 1.09	.51	3.69 ± 1.22	3.37 ± 1.22	.04
BRI (3rd tertile, n/%)	28 (38.4%)	390 (36.2%)	.71	22 (42.3%)	111 (25.2%)	.01
CVAI	98.58 ± 58.95	99.13 ± 42.10	.92	83.29 ± 36.50	69.29 ± 39.30	.01
CVAI (3rd tertile, n/%)	31 (42.5%)	433 (40.2%)	.70	12 (23.1%)	74 (16.8%)	.04

Abbreviations: ABSI, a body shape index; BRI, body roundness index; CVAI, Chinese visceral adiposity index; EU, euthyroid; PCF, pericardial fat; SCH, subclinical hypothyroidism; TAT, thoracic periaortic adipose tissue.

Table 4. Baseline characteristics according to thyroid functional status and absolute risk of cardiovascular event in 10 years by Framingham risk score
Variables	Low risk										Intermediate/high risk
	Men					Women					Men					Women
	SCH (n = 26)		EU (n = 567)		P	SCH (n = 42)		EU (n = 360)		P	SCH (n = 47)		EU (n = 511)		P	SCH (n = 10)		EU (n = 81)		P
Age, y	45.5	12.0	43.0	9.0	.31	52.0	9.8	49.8	12.0	.14	57.0	14.0	54.0	10.0	.18	65.5	12.3	61.0	11.5	.47
TSH, μIU/mL	5.5	2.4	1.7	1.1	< .001	5.3	1.8	1.8	1.1	< .001	5.4	1.6	1.9	1.1	< .001	6.0	2.9	2.1	1.5	< .001
FT4, ng/dL	1.2	0.3	1.3	0.2	.01	1.2	0.2	1.3	0.2	.001	1.3	0.1	1.3	0.2	.001	1.2	0.3	1.3	0.2	.04
Smoking, %	2	7.7	53	9.3	.56	0	0.0	7	1.9	.46	14	29.8	166	32.5	.70	0	0.0	3	3.7	.99
Diabetes, %	0	0.0	5	0.9	.80	0	0.0	9	2.5	.37	5	10.6	75	14.7	.45	3	30.0	20	24.7	.71
HTN, %	1	3.8	29	5.1	.62	4	9.5	21	5.8	.26	22	46.8	197	38.6	.27	7	70.0	45	55.6	.51
BMI	23.9	4.0	24.2	3.9	.61	23.3	3.9	22.2	4.2	.06	25.4	3.9	25.6	4.3	.44	26.5	4.8	24.5	4.7	.10
WC, cm	84.5	7.8	85.0	11.0	.69	78.0	10.6	75.0	10.5	.14	88.0	8.0	90.0	11.0	.42	87.5	12.0	83.0	12.8	.05
Obesity, %	5	19.2	107	18.9	.56	6	14.3	37	10.3	.28	12	25.5	178	34.8	.20	4	40.0	23.00	28.4	.48
SBP, mm Hg	110.0	11.8	116.0	18.0	.42	116.0	20.0	110.0	18.0	.30	128.0	22.0	130.0	20.0	.24	143.0	27.0	138.0	21.0	.15
DBP, mm Hg	70.0	10.5	74.0	10.0	.32	70.0	16.3	70.0	15.0	.63	80.0	20.0	80.0	13.0	.68	87.0	13.5	80.0	13.5	.39
FBG, mg/dL	93.0	11.5	96.0	10.0	.36	92.0	10.5	93.0	9.0	.89	100.0	21.0	102.0	22.0	.43	107.0	39.0	106.0	22.0	.97
PC glucose, mg/dL	99.0	22.3	101.0	30.5	.34	107.0	32.0	110.0	34.0	.98	123.5	72.0	119.0	63.0	.50	145.0	124.8	140.5	76.5	.80
HbA_1c, %	5.6	0.6	5.6	0.3	.77	5.6	0.4	5.6	0.5	.63	6.0	0.8	5.9	0.8	.55	5.9	1.0	6.1	0.8	.40
TC, mg/dL	191.0	32.8	194.0	45.0	.78	201.5	46.3	197.0	49.0	.14	214.0	52.0	209.0	49.0	.32	211.5	109.3	218.0	47.0	.63
HDL-C, mg/dL	48.5	14.0	50.0	16.0	.49	60.0	15.8	61.0	18.8	.73	48.0	16.0	44.0	12.0	.38	51.5	13.3	53.0	19.0	.94
LDL-C, mg/dL	129.0	34.8	127.0	41.0	.69	124.0	36.3	120.0	42.0	.10	140.0	54.0	139.0	45.0	.85	118.5	75.3	144.0	52.0	.23
TGs, mg/dL	109.0	67.8	113.0	79.0	.82	96.0	68.0	88.0	53.0	.14	163.0	105.0	146.0	109.0	.47	181.0	108.5	140.0	84.5	.59
FRS, %	5.32	4.54	5.03	3.78	.67	4.0	2.6	3.2	3.2	.08	16.66	18.42	16.27	12.20	.65	18.3	20.5	13.8	6.1	.23
PCF	65.4	24.5	68.3	34.3	.43	54.9	25.4	57.0	28.1	.99	83.01	31.05	83.23	41.92	.77	105.4	74.8	81.3	42.0	.16
TAT	5.3	6.0	6.2	3.2	.37	3.7	2.5	3.3	1.8	.01	8.67	4.94	9.23	5.17	.98	9.2	8.9	6.4	4.3	.04
ABSI	0.1	0.0	0.1	0.0	.78	0.1	0.0	0.1	0.0	.74	0.1	0.004	0.1	0.005	.45	0.1	0.0	0.1	0.0	.87
BRI	3.2	1.1	3.2	1.1	.38	3.2	1.4	2.9	1.3	.10	3.82	1.07	3.98	1.27	.37	4.8	1.5	4.1	1.8	.03
CVAI	82.9	40.6	82.0	50.9	.73	71.8	45.7	59.3	44.1	.02	110.4	45.8	114.3	48.2	.47	132.9	37.4	112.3	40.5	.04

Clinical characteristics are expressed as median (interquartile range) for continuous variables and n (%) for categorical variables. P values were derived from Mann-Whitney for continuous variables, and categorical variables were expressed as percentages and compared with the χ ² test or Fisher exact test. Bold part mean statistical significant difference.
Abbreviations: ABSI, a body shape index; AR10y, absolute risk of cardiovascular event in 10 years by FRS; BMI, body mass index; BRI, body roundness index; CVAI, Chinese visceral adiposity index; DBP, diastolic blood pressure; EU, euthyroid; FPG, fasting plasma glucose; FT4, free thyroxine; HTN, hypertension; HbA_1c, glycated hemoglobin A_1c; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; FRS, Framingham risk score; Obesity, BMI ≥ 27; PCF, pericardial fat; PPG, postprandial plasma glucose; SBP, systolic blood pressure; SCH, subclinical hypothyroidism; TAT, thoracic periaortic adipose tissue; TC, total cholesterol; TGs, triglycerides; TSH, thyrotropin; WC, waist circumference.

Table 5. Odds ratio of region-specific cardiovascular fat tissue and noninvasive visceral adipose indices with risk of subclinical hypothyroidism according to absolute risk of cardiovascular event in 10 years by Framingham risk score
Variables	PCF^a			TAT^a			ABSI			BRI			CVAI
Variables	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P	OR	95% CI	P
Low risk
Men
Model 1	0.56	(0.21–1.50)	.25	1.32	(0.56–3.10)	.53	1.31	(0.56–3.07)	.54	0.79	(0.29–2.14)	.65	0.96	(0.26–3.14)	.93
Model 2	0.52	(0.19–1.41)	.20	1.24	(0.52–2.95)	.62	1.24	(0.52–2.94)	.62	0.80	(0.30–2.18)	.67	0.96	(0.38–2.45)	.93
Model 3	0.48	(0.17–1.32)	.15	1.24	(0.51–3.05)	.63	1.18	(0.49–2.82)	.71	0.80	(0.28–2.27)	.67	0.96	(0.35–2.66)	.94
Women
Model 1	0.84	(0.31–2.23)	.72	3.00	(0.78–11.55)	.11	0.69	(0.29–1.61)	.39	2.03	(1.00–4.13)	.049	0.91	(0.28–2.44)	.88
Model 2	0.64	(0.23–1.78)	.40	2.60	(0.67–10.15)	.17	0.61	(0.26–1.44)	.26	1.82	(0.89–3.73)	.10	0.71	(0.20–2.52)	.60
Model 3	0.64	(0.23–1.77)	.39	2.83	(0.71–11.34)	.14	0.60	(0.25–1.43)	.25	1.86	(0.87–3.96)	.11	0.87	(0.23–3.25)	.83
Men
Model 1	0.98	(0.54–1.79)	.96	1.02	(0.55–1.90)	.95	1.54	(0.84–2.81)	.16	0.93	(0.51–1.69)	.82	0.81	(0.45–1.48)	.50
Model 2	0.94	(0.51–1.72)	.84	0.94	(0.50–1.78)	.85	1.42	(0.76–2.65)	.28	0.92	(0.50–1.67)	.78	0.81	(0.44–1.47)	.48
Model 3	1.00	(0.53–1.90)	.99	1.04	(0.53–2.05)	.91	1.47	(0.78–2.77)	.23	1.03	(0.54–1.97)	.92	0.90	(0.46–1.77)	.76
Women
Model 1	2.92	(0.70–12.09)	.14	3.17	(1.02–5.22)	.03	1.19	(0.32–4.43)	.80	6.85	(1.08–10.61)	.02	6.85	(1.03–11.61)	.03
Model 2	2.69	(0.62–11.63)	.19	3.26	(1.07–5.54)	.03	1.16	(0.31–4.40)	.82	6.91	(1.03–10.23)	.03		(1.01–12.57)	.04
Model 3	4.05	(0.73–22.42)	.11	4.01	(1.01–6.64)	.04	1.39	(0.34–5.74)	.65	7.04	(1.02–11.29)	.03	7.81	(1.01–12.03)	.04

Model 1: Unadjusted.
Model 2: Adjusted for age and smoking.
Model 3: Adjusted for factors in model 2 plus SBP, FBG, LDL-C, and HDL-C.
Abbreviations: ABSI, a body shape index; BMI, body mass index; BRI, body roundness index; CVAI, Chinese visceral adiposity index; FPG, fasting plasma glucose; HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; OR, odds ratio; PCF, pericardial fat; SBP, systolic blood pressure; TAT, thoracic periaortic adipose tissue.
^aModel 2: Adjusted for age, smoking, and BMI.