Serum bile acid and unsaturated fatty acid profiles of non-alcoholic fatty liver disease in type 2 diabetic patients

doi:10.4239/wjd.v15.i5.898

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World J Diabetes. May 15, 2024; 15(5): 898-913
Published online May 15, 2024. doi: 10.4239/wjd.v15.i5.898

Table 1 Baseline characteristics of healthy control and type 2 diabetes mellitus with or without non-alcoholic fatty liver disease

Item	HC	T2DM without NAFLD	T2DM with NAFLD	F_0-1	F_2-4
Item	n = 113	n = 134	n = 152	n = 94	n = 58
Age in yr	59.65 ± 14.54	60.06 ± 16.60	53.61 ± 12.16^a^,^b	49.44 ± 10.32	61.72 ± 10.48^c
Sex, male, %	69 (61.06)	87 (64.93)	102 (67.11)	63 (67.02)	39 (67.24)
Duration of diabetes, month	/	84.00 [27.00, 153.00]	48.00 [2.00, 120.00]^b	36.00 [7.00, 93.00]	84.00 [24.00, 144.00]^c
SBP, mmHg	128.00 [116.00, 132.00]	130.00 [120.00, 138.50]	130.00 [120.00, 140.00]	130.00 [120.00, 138.00]	130.00 [120.00, 140.00]
DBP, mmHg	80.00 [74.00, 86.00]	81.00 [75.00, 89.00]	82.00 [76.00, 88.00]	81.00 [80.00, 88.00]	80.00 [76.00, 90.00]
BMI, Kg/m²	22.21 [21.54, 23.58]	23.38 [21.59, 25.98]	25.96 [23.76, 27.79]^a^,^b	26.39 [23.98, 29.37]	25.96 [24.22, 26.70]
TyG index	8.41 [8.21, 9.02]	9.88 [9.43, 10.40]^a	10.21 [9.69, 10.71]^a^,^b	10.27 [9.82, 10.66]	9.98 [9.57, 10.53]
FIB-4 index	/	/	/	0.85 [0.59, 1.02]	1.79 [1.51, 2.13]^c
HbA1c, %	/	9.00 [7.00, 10.50]	9.10 [7.65, 10.60]	9.15 [7.92, 10.60]	8.60 [7.52, 10.47]
FPG, mmol/L	5.21 [4.97, 5.83]	8.05 [5.99, 11.02]^a	8.13 [6.67, 10.68]^a	8.63 [6.43, 11.32]	7.86 [6.88, 9.84]
FC-P, ng/mL	/	1.33 [0.61, 2.17]	1.85 [1.16, 2.79]^b	1.92 [1.16, 3.04]	1.80 [1.41, 2.48]
2h C-P, ng/mL	/	2.83 [1.24, 5.00]	4.13 [2.17, 6.23]^b	4.29 [2.10, 6.39]	4.31 [2.34, 6.35]
TC, mmol/L	4.44 [3.91, 5.19]	4.19 [3.63, 4.97]	4.62 [3.91, 5.44]^b	4.63 [4.01, 5.21]	4.52 [3.69, 5.47]
TG, mmol/L	1.17 [0.88, 1.79]	1.35 [1.04, 1.98]^a	1.76 [1.29, 2.99]^a^,^b	1.95 [1.38, 3.08]	1.56 [1.21, 2.46]
HDL-C, mmol/L	1.24 [1.11, 1.42]	1.07 [0.91, 1.28]^a	0.93 [0.82, 1.10]^a^,^b	0.92 [0.80, 1.08]	0.98 [0.83, 1.17]
LDL-C, mmol/L	2.70 [2.31, 3.32]	2.77 [2.27, 3.28]	2.94 [2.22, 3.67]	2.94 [2.33, 3.59]	2.98 [2.07, 3.75]
ALT, U/L	14.10 [10.90, 21.42]	14.10 [10.10, 20.50]	25.00 [15.70, 36.30]^a^,^b	23.40 [15.17, 33.05]	28.50 [15.90, 41.25]
AST, U/L	15.45 [12.83, 19.25]	15.20 [12.70, 19.30]	18.90 [14.35, 25.85]^a^,^b	16.90 [13.80, 24.70]	22.50 [16.27, 36.47]^c
TBIL, μmol/L	10.75 [7.45, 13.67]	9.30 [7.60, 12.05]	11.30 [8.65, 14.30]^a^,^b	10.95 [8.00, 14.07]	11.70 [9.50, 14.77]
DBIL, μmol/L	3.90 [2.92, 5.47]	3.80 [2.95, 4.65]	4.40 [3.45, 5.55]^a^,^b	4.25 [3.30, 5.20]	4.85 [3.70, 6.10]^c
IBIL, μmol/L	5.95 [4.08, 8.05]	5.70 [4.50, 7.45]	6.90 [4.85, 8.50]^a^,^b	6.60 [4.45, 8.52]	6.90 [5.62, 8.55]
UA, μmol/L	277.00 [228.00, 330.00]	287.00 [234.00, 347.00]	313.50 [247.25, 374.00]^a^,^b	315.00 [248.50, 376.25]	315.50 [247.00, 356.50]
SCR, μmol/L	66.00 [54.12, 75.55]	67.35 [54.27, 79.55]	64.20 [52.90, 77.48]	65.20 [52.25, 80.10]	65.70 [56.92, 79.12]
BUN, mmol/L	5.42 [4.53, 6.34]	5.54 [4.75, 6.47]	5.38 [4.45, 6.06]	5.41 [4.46, 6.00]	5.36 [4.48, 6.45]
HT, yes, %	/	72 (53.73)	73(48.03)	42 (40.43)	31 (57.45)
Metformin, yes, %	/	50 (37.31)	60 (39.47)	38 (43.63)	22 (37.93)
Acarbose, yes, %	/	28 (20.90)	26 (17.11)	12 (12.77)	14 (24.14)
Sulfonylureas, yes, %	/	15 (11.19)	24 (15.79)	11 (11.70)	13 (24.41)
Glinides, yes, %	/	3 (2.24)	10 (6.58)	7 (7.45)	3 (5.17)
TZDs, yes, %	/	3 (2.24)	1 (0.66)	1 (1.06)	0 (0.00)
DPP-4 inhibitors, yes, %	/	13 (9.70)	16 (10.53)	10 (10.64)	6 (10.34)
SGLT-2 inhibitors, yes, %	/	16 (11.94)	14 (9.21)	9 (9.57)	5 (8.62)
GLP-1 agonists, yes, %	/	1 (0.75)	1 (0.66)	0 (0.00)	1 (1.72)
Insulin, yes, %	/	35 (26.12)	27 (17.76)	16 (17.02)	11 (18.97)
Statins, yes, %	/	12 (8.96)	18 (11.84)	11(11.70)	7 (12.07)

^aP < 0.05 when compared with health control (Wilcoxon rank sum test).

^bP < 0.05 when type 2 diabetes mellitus (T2DM) with non-alcoholic fatty liver disease (NAFLD) compared with T2DM without NAFLD (Wilcoxon rank sum test).

^cP < 0.05 when F_2-4 compared with F_0-1 (Wilcoxon rank sum test).

Values are n (%), mean ± SD, median [upper quartile, lower quartile]. 2h C-P: C-peptide 2 h after meal; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; BMI: Body mass index; BUN: Blood urea nitrogen; DBIL: Direct bilirubin; DBP: Diastolic blood pressure; DPP-4 inhibitor: Dipeptidyl peptidase-4 inhibitor; FC-P: Fasting C-peptide; F_0-1: FIB-4 < 1.3 in non-alcoholic fatty liver disease; F₀: Clinical liver fibrosis stage 0 (no fibrosis): F₁: Clinical liver fibrosis stage 1 (Mild fibrosis); F_2-4: Clinically significant fibrosis with FIB-4 ≥ 1.3 in non-alcoholic fatty liver disease: F₂: Clinical liver fibrosis stage 2 (moderate fibrosis): F₃: Clinical liver fibrosis stage 3 (severe fibrosis): F₄: Clinical liver fibrosis stage 4 (cirrhosis); FIB-4: Fibrosis 4 score; FPG: Fasting blood glucose; GLP-1 agonists: Glucagon-like peptide-1 agonists; HbA1c: Hemoglobin A1c; HC: Health control; HDL-C: High-density lipoprotein cholesterol; HT: Hypertension; IBIL: Indirect bilirubin; LDL-C: Low-density lipoprotein cholesterol; NAFLD: Non-alcoholic fatty liver disease; PLT: Platelet; SBP: Systolic blood pressure; SCR: Serum creatinine; SGLT-2 inhibitor: Sodium-dependent glucose transporters 2; T2DM: Type 2 diabetes mellitus; TBIL: Total bilirubin; TC: Total cholesterol; TG: Triglyceride; TZDs: Thiazolidinediones; TyG: Triglyceride-glucose; UA: Uric acid.

Table 2 Association between unsaturated fatty acids and risk of non-alcoholic fatty liver disease in type 2 diabetes mellitus

Characteristics	Univariate			Multivariable adjusted
Characteristics	OR	95%CI	P value	OR	95%CI	P value
MUFAs
C16:1 (≥ 12.90 μmol/L)	2.289	1.429-3.696	0.001^a	1.969	1.135-3.439	0.016^a
C18:1	1.002	1.000-1.004	0.032^a	1.002	1.000-1.004	0.100
C20:1	1.270	1.071-1.543	0.011^a	1.224	1.006-1.516	0.055
ω-3 PUFAs
α-C18:3 (≥ 9.21 μmol/L)	2.093	1.309-3.371	0.002^a	1.795	1.040-3.113	0.036^a
EPA	1.187	1.044-1.376	0.014^a	1.208	1.234-1.448	0.006^a
ω-3-C22:5	1.239	1.066-1.457	0.007^a	1.262	1.051-1.531	0.015^a
ω-6 PUFA
γ-C18:3	1.361	1.126-1.694	0.003^a	1.381	1.106-1.783	0.008^a
MUFAs ratio
ω-6/ω-3	0.904	0.838-0.969	0.006^a	0.908	0.832-0.986	0.026^a

^aP < 0.05: Statistically significant.

Multivariable adjusted analysis including age, body mass index, sex, systolic blood pressure, duration of diabetes, triglyceride-glucose, hemoglobin A1c, fasting C-Peptide, C-peptide 2 h after meal, uric acid, 8 kinds of hypoglycemic drugs (metformin, acarbose, sulfonylureas, glinides, thiazolidinediones, dipeptidyl peptidase-4 inhibitors, sodium-dependent glucose transporters-2 inhibitors, glucagon-like peptide-1 agonists, insulin) and Statins. BAs: Bile acids; CI: Confidence interval; DPP-4 inhibitor: Dipeptidyl peptidase-4 inhibitor; GLP-1 agonists: Glucagon-like peptide-1 agonists; MUFAs: Monounsaturated fatty acids; NAFLD: Non-alcoholic fatty liver disease; OR: Odds ratios; PUFAs: Polyunsaturated fatty acids; SGLT-2 inhibitor: Sodium-dependent glucose transporters 2; T2DM: Type 2 diabetes mellitus; TZDs: Thiazolidinediones.

Table 3 Association between unsaturated fatty acids and risk of clinically significant fibrosis in non-alcoholic fatty liver disease

Characteristics	Univariate			Multivariable adjusted
Characteristics	OR	95%CI	P value	OR	95%CI	P value
ω-3 PUFAs
α-C18:3	1.060	1.015-1.116	0.017^a	1.078	1.018-1.153	0.018^a
ω-3-C22:5	1.193	0.992-1.446	0.064	1.176	0.930-1.504	0.181
ω-6 PUFA
γ-C18:3	1.409	1.125-1.879	0.009^a	1.518	1.135-2.228	0.013^a

^aP < 0.05: Statistically significant.

Multivariable adjusted analysis including age, body mass index, sex, systolic blood pressure, duration of diabetes, triglyceride-glucose, hemoglobin A1c, fasting C-Peptide, C-peptide 2 h after meal, uric acid, 8 kinds of hypoglycemic drugs (metformin, acarbose, sulfonylureas, glinides, thiazolidinediones, dipeptidyl peptidase-4 inhibitors, sodium-dependent glucose transporters 2 inhibitors, glucagon-like peptide-1 agonists, and insulin), and Statins. NAFLD: Non-alcoholic fatty liver disease; F_2-4: Fibrosis 4 score ≥ 1.3; OR: Odds ratios; CI: Confidence interval; PUFA: Polyunsaturated fatty acid; TZDs: Thiazolidinediones; DPP-4 inhibitor: Dipeptidyl peptidase-4 inhibitor; SGLT-2 inhibitor: Sodium-dependent glucose transporters 2; GLP-1: Glucagon-like peptide-1.

Citation: Feng SS, Wang SJ, Guo L, Ma PP, Ye XL, Pan ML, Hang B, Mao JH, Snijders AM, Lu YB, Ding DF. Serum bile acid and unsaturated fatty acid profiles of non-alcoholic fatty liver disease in type 2 diabetic patients. World J Diabetes 2024; 15(5): 898-913
URL: https://www.wjgnet.com/1948-9358/full/v15/i5/898.htm
DOI: https://dx.doi.org/10.4239/wjd.v15.i5.898