Metabolic dysfunction-associated steatotic liver disease-associated fibrosis and cardiac dysfunction in patients with type 2 diabetes

doi:10.4330/wjc.v16.i10.580

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Oct 26, 2024 (publication date) through Feb 27, 2025

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World Journal of Cardiology

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1949-8462

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

Observational Study

World J Cardiol. Oct 26, 2024; 16(10): 580-594
Published online Oct 26, 2024. doi: 10.4330/wjc.v16.i10.580

Table 1 Lifestyle and clinical characteristics of the study population

Patients’ characteristics	Value
Systolic/diastolic BP (mmHg)	135.0 (95.0-190.0)/80.0 (51.0-107.5)
Heart rate (beats/min)	74.0 (50.0-112.0)
pO₂ (%)	97.0 (90.0-99.0)
Lifestyle
Smoking status
Current smoker	28 (10.49)
Former smoker	107 (40.07)
Never smoked	132 (49.44)
Coffee intake (cups/day)	1.25 ± 0.80
Alcohol intake (g/day)	2.85± 5.37
Anthropometric parameters
BMI (kg/m²)	34.11 ± 5.30
Waist circumference (cm)	109.16 ± 11.72 (F)
Waist circumference (cm)	114.92 ± 10.83 (M)
Hip circumference (cm)	110.21 ± 10.55 (F)
Hip circumference (cm)	108.86 ± 9.98 (M)
Comorbidities
Hypertension	251 (94.00)
Dyslipidemia	247 (92.51)
Coronary artery disease	137 (51.31)
Heart failure	99 (37.01)
Atrial fibrillation	17 (6.37)
Peripheral arterial disease	18 (6.74)
Stroke	19 (7.11)
Diabetic neuropathy	106 (39.70)
Diabetic retinopathy	36 (13.48)
Chronic kidney disease	49 (18.35)
Hyperuricemia	58 (21.72)
Antihyperglycemic therapy
Metformin	262 (98.13)
GLP-1 RA	85 (31.83)
SGLT2 inhibitors	62 (23.22)
DPP-4 inhibitors	19 (7.12)
Sulphonylureas	27 (10.11)
Insulin	66 (24.72)

Data are presented as mean ± SD, median (min-max), or as n (%). BP: Blood pressure; F: Female; M: Male; BMI: Body mass index; GLP-1 RA: Glucagon-like peptide-1 receptor agonists; SGLT2: Sodium-glucose co-transporter 2; DPP-4: Dipeptidyl peptidase-4.

Table 2 Laboratory parameters in the study population according to the liver fibrosis category

Parameter	Group 1 (advanced fibrosis), n = 84	Group 2 (indeterminate risk of fibrosis), n = 164	Group 3 (without fibrosis), n = 19	P value
Uric acid (mg/dL)	6.13 ± 1.44	5.86 ± 1.48	5.29 (3.59-8.17)	0.0484
Albumin (g/dL)	4.59 ± 0.22^a	4.68 ± 0.23^a	4.70 ± 0.28	0.0118
ALAT (U/L)	17.22 (2.32-80.94)	18.02 (4.18-92.79)	25.36 ± 12.56	0.0921
ASAT (U/L)	22.54 (11.48-130.85)^b	19.91 (9.75-49.95)^b	19.30 (13.16-39.16)	0.0034
Direct bilirubin (mg/dL)	0.21 (0.07-0.59)^a	0.20 (0.07-0.90)	0.17 ± 0.06^a	0.0335
GGT (U/L)	32.78 (4.97-338.18)^a	27.51 (4.02-313.66)^a	27.13 (9.17-173.63)	0.0360
Total cholesterol (mg/dL)	147.20 (91.38-279.48)	155.45 (96.75-376.17)	175.16 ± 51.20	0.1347
HDL cholesterol (mg/dL)	43.98 (27.86-65.09)	43.75 (22.48-75.75)	48.04 ± 11.77	0.3977
LDL cholesterol (mg/dL)	73.71 (36.57-186.09)	84.73 (31.2-270.6)	104.01 ± 39.94	0.0488
Triglycerides (mg/dL)	156.02 (70.06-573.36)^a	155.36 (62.37-609.08)^a	117.83 (68.15-382.84)^a	0.0305
Blood glucose (mg/dL)	137.59 (92.09-261.68)	136.58 (87.34-326.2)	142.75 ± 18.60	0.7290
HbA1c (%)	6.80 (4.6-10.01)	6.80 (5.7-10.20)	7.02 ± 0.72	0.5780
C-peptide (ng/mL)	3.68 (0.72-10.5)^a^,^b	3.00 (0.28-8.83)^a	2.62 ± 1.43^b	0.0039
HOMA-IR	3.04 (0.66-8.4)^a	2.61 (0.45-7.52)	2.23 ± 1.21^a	0.0067
eGFR (mL/min/1.73m²)	82.53 (26.70-117.25)^b^,^c	91.38 (40.36-114.59)^a^,^b	97.17 ± 14.60^a^,^c	< 0.0001
Haptoglobin (g/L)	1.59 ± 0.57	1.73 ± 0.61	1.73 ± 0.63	0.1997
Ferritin (ng/mL)	112.00 (8.79-781.00)	92.30 (6.41-811.00)	53.90 (9.72-543.0)	0.6226
SHBP (nmol/L)	37.41 ± 15.12	32.80 (7.62-118.00)	35.38 ± 15.68	0.3811

^aP < 0.05.

^bP < 0.01.

^cP < 0.001.

For triglycerides: Group 1 vs group 2, and group 2 vs group 3. Data are presented as mean ± SD or median (min-max). ASAT: Aspartate aminotransferase; ALAT: Alanine aminotransferase; GGT: Gamma glutamyl transpeptidase; HDL: High-density lipoprotein; LDL: Low-density lipoprotein; eGFR: Estimated glomerular filtration rate; HOMA-IR: Homeostatic Model Assessment for Insulin Resistance; SHBP: Sex-hormone binding protein.

Table 3 Echocardiographic structural and functional parameters according to liver fibrosis categories

Echocardiographic parameters	Group 1 (advanced fibrosis), n = 84	Group 2 (indeterminate risk of fibrosis), n = 164	Group 3 (without fibrosis), n = 19	P value
Morphologic parameters
LV diastolic diameter (mm)	51.37 ± 6.04	50.00 (38.00-71.00)	48.53 ± 4.50	0.1482
LV systolic diameter (mm)	37.00 (24.00-57.00)	36.00 (24.00-60.00)	34.89 ± 6.44	0.4832
IV septum thickness (mm)	12.00 (8.00-16.00)^b	11.00 (7.00-16.00)	10.00 (9.00-13.00)^b	0.0029
LV posterior wall thickness (mm)	12.00 (9.00-16.00)^a	11.00 (7.00-17.00)^a	11.00 (10.00-14.00)	0.0277
Left atrium diameter (mm)	39.07 ± 5.15^c	37.00 (26.00-52.00)^a	34.31 ± 4.26^a^,^c	0.0008
Right atrium diameter (mm)	36.96 ± 6.03^a	35.47 ± 5.28	33.47 ± 4.68^a	0.0224
Right ventricle diameter (mm)	36.34 ± 5.50	35.00 (12.00-50.00)	37.00 ± 5.18	0.5209
Aortic annular diameter (mm)	32.00 (20.00-42.00)	32.00 (23.00-40.00)	31.11 ± 3.05	0.2201
Descending aorta diameter (mm)	18.00 (13.00-33.00)^b	19.00 (10.00-30.00)^b	18.11 ± 1.60	0.0066
LV end-diastolic volume (mm³)	121.64 ± 31.18	109.00 (63.00-380.00)	108.74 ± 17.85	0.1388
LV end-systolic volume (mm³)	66.70 ± 22.25^a	57.00 (21.00-290.00)^a	54.35 ± 14.16	0.0101
Stroke volume (mm³)	55.42 ± 16.60	54.00 (24.00-112.00)	52.81 ± 13.48	0.7994
EATT (mm)	8.00 (3.00-17.00)^b	7.00 (3.00-14.00)^b	7.26 ± 2.51	0.0027
LVMi (g/m²)	119.16 ± 27.36	113.23 ± 24.82	104.39 ± 22.32	0.0474
Increased LVMi, n (%)	55 (66.27%)	99 (60.37%)	10 (52.63%)	0.4687
Functional parameters
EF, n (%)	49.19 ± 5.62	50.87 ± 5.14	52.00 ± 3.25^a	0.0030
EF, n (%)	49.00 (27.00-65.00)^a^,^b	50.00 (23.00-61.00)^a^,^b	52.00 (45.00-60.00)	0.0030
EF-normal range, n (%)	41 (49.40)	113 (68.90)	16 (84.21)	0.0017
E wave velocity (cm/second)	72.59 ± 19.24	70.00 (32.00-158.00)	71.83 ± 18.07	0.9292
A wave velocity (cm/second)	84.31 ± 21.25	86.10 ± 22.65	81.61 ± 27.54	0.6626
Mitral valve E/A	0.79 (0.38-1.52)	0.80 (0.44-2.07)	0.94 ± 0.28	0.5683
e’ septal (cm/second)	8.00 (3.00-16.00)^b	8.00 (4.00-15.00)	10.50 ± 2.94^b	0.0068
e’/a’ septal	0.70 (0.43-2.0)	0.78 (0.36-3.00)	0.84 ± 0.24	0.3637
E/e’ septal	9.64 ± 4.10^a	8.44 (2.43-26.33)	7.35 ± 2.62^a	0.0260
e’ lateral (cm/second)	8.00 (4.00-19.00)	8.00 (4.00-18.00)	8.00 (4.00-13.00)	0.9551
e’/a’ lateral	0.73(0.40-2.00)	0.71 (0.40-2.00)	0.79 ± 0.28	0.7655
E/e’ lateral	9.15 ± 3.76	8.27 (2.83-25.0)	8.15 (3.54-20.75)	0.8768
Average E/e’ ratio	9.17 ± 3.58	8.39 (2.62-22.57)	7.77 ± 2.34	0.3208
DcT (msec)	200.73 ± 59.07	194.59 ± 51.00	192.17 ± 43.19	0.6725
LVOT VTI (cm)	30.00 (11.20-78.00)	30.00 (11.90-76.00)	28.98 ± 7.27	0.5857
LV segmental kinetics
Total wall motion score index	1.10 ± 0.17	1.06 ± 0.13	1.02 ± 0.06	0.0352
Basal wall motion score index	1.06 ± 0.18	1.03 ± 0.12	1.02 ± 0.05	0.6358
Mid wall motion score index	1.11 ± 0.21	1.06 ± 0.15	1.03 ± 0.1	0.0240
Apical wall motion score index	1.15 ± 0.26	1.10 ± 0.24	1.02 ± 0.06	0.0548

^aP < 0.05.

^bP < 0.01.

^cP < 0.001.

For ejection fraction (%): Group 1 vs group 2, and group 1 vs group 3. Data are presented as mean ± SD or median (min-max). Ejection fraction-normal range ≥ 50%. LV: Left ventricular; IV: Interventricular; EATT: Epicardial adipose tissue thickness; LVMi: Left ventricular mass index; EF: Ejection fraction; LVOT VTI: Left ventricular outflow tract velocity time integral; DcT: Deceleration time.

Table 4 The bivariate correlations of the two liver fibrosis scores with echocardiographic parameters in type 2 diabetes mellitus patients with Metabolic dysfunction-associated steatotic liver disease

	FIB4, r (95%CI)	NFS, r (95%CI)
LV diastolic diameter	0.09 (-0.03; 0.22)	0.14 (0.02; 0.26)^a
IV septum thickness	0.19 (0.07; 0.31)^b	0.23 (0.11; 0.35)^c
LV posterior wall thickness	0.12 (-0.004; 0.24)	0.18 (0.06; 0.30)^b
Left atrium diameter	0.19 (0.07; 0.31)^b	0.17 (0.04; 0.29)^b
Right atrium diameter	0.17 (0.05; 0.29)^b	0.21 (0.09; 0.32)^d
Aortic annular diameter	0.13 (0.001; 0.25)^a	0.09 (-0.04; 0.21)
EATT	0.12 (-0.004; 0.24)	0.13 (0.01; 0.25)^a
LV end-systolic volume	0.08 (-0.05; 0.20)	0.14 (0.01; 0.26)^a
LVMi	0.15 (0.02; 0.26)^a	0.19 (0.06; 0.30)^b
EF (%)	-0.13 (-0.25; -0.01)^a	-0.21 (-0.33; -0.09)^d
e’ septal	-0.24 (-0.36; -0.12)^e	-0.19 (-0.31; -0.07)^b
a’ septal	-0.13 (-0.25; -0.004)^a	-0.10 (-0.22; 0.03)
e’/a’ septal	-0.14 (-0.27; -0.02)^a	-0.12 (-0.24; 0.01)
E/e’ septal	0.19 (0.06; 0.31)^b	0.19 (0.07; 0.31)^b
Total LV segmental kinetics score	0.14 (0.01; 0.26)^a	0.16 (0.04; 0.28)^b

^aP < 0.05.

^bP < 0.01.

^cP = 0.0001.

^dP < 0.001.

^eP < 0.0001.

FIB4: Fibrosis-4; NFS: Non-alcoholic fatty liver disease-Fibrosis Score; 95%CI: 95% confidence interval; IV: Interventricular; LV: Left ventricle; EATT: Epicardial adipose tissue thickness; LVMi: Left ventricular mass index; EF: Ejection fraction.

Table 5 The multiple regression analyses with fibrosis-4 and non-alcoholic fatty liver disease-fibrosis score as dependent variables in two models

	β (95%CI); t ratio	β (95%CI); t ratio
Model 1
Left atrium diameter	0.044 (0.007; 0.082); 2.307^a	0.039 (0.004; 0.074); 2.180^a
Right atrium diameter	0.019 (-0.014; 0.052); 1.107	0.041 (0.010; 0.072); 2.628^b
Sex	0.137 (-0.273; 0.546); 0.654	-0.560 (-0.941; -0.179); 2.881^b
Serum creatinine	0.748 (-0.025; 1.521); 1.897	1.467 (0.747; 2.186); 3.995^c
Model 2
Left atrium diameter	0.037 (0.0005; 0.073); 1.990^a	0.030 (-0.005; 0.065); 1.695
C-peptide	0.175 (0.071; 0.280); 3.282^b	0.099 (-0.002; 1.200); 1.920
Right atrium diameter	0.013 (-0.017; 0.043); 0.851	0.030 (0.001; 0.059); 2.021^a
Serum creatinine	0.410 (-0.328; 1.148); 1.089	0.843 (0.133; 1.533); 2.326^a

^aP < 0.05.

^bP < 0.01.

^cP < 0.0001.

Independent variables in Model 1: Left ventricular mass index (LVMi), left atrium diameter, right atrium diameter, sex, smoking status, systolic blood pressure, duration of diabetes, alcohol intake, atrial fibrillation, serum creatinine; in Model 2: LVMi, left atrium diameter, right atrium diameter, C-peptide, low-density lipoprotein cholesterol, serum creatinine). Only the parameters correlated with at least one score are mentioned in the table. 95%CI: 95% confidence interval; IV: Interventricular; LV: Left ventricle; LVMi: Left ventricular mass index; EF: Ejection fraction.

Table 6 Factors associated with left atrium diameter in the bivariate correlation analysis

Left atrium diameter	r (95%CI)
Uric acid	0.14 (0.01; 0.26)^a
Direct bilirubin	0.15 (0.03; 0.27)^a
GGT	0.15 (0.02; 0.27)^a
HDL cholesterol	-0.13 (-0.25; -0.01)^a
C-peptide	0.13 (0.005; 0.25)^a
SHBP	-0.14 (-0.26; -0.02)^a
Sex	0.23 (0.11; 0.34)^b
Atrial fibrillation	0.16 (0.04; 0.28)^c

^aP < 0.05.

^bP = 0.0001.

^cP < 0.01.

95%CI: 95% confidence interval; GGT: Gamma glutamyl transpeptidase; HDL: High-density lipoprotein; SHBP: Sex-hormone binding protein.

Table 7 The multiple regression analysis with left atrium diameter as the dependent variable

	β (95%CI), t ratio
GGT	0.015 (0.003; 0.028); 2.343^a
SHBP	-0.036 (-0.071; -0.001); 2.039^a
Atrial fibrillation	3.481 (1.232; 5.729); 3.034^b

^aP < 0.05.

^bP < 0.01.

95%CI: 95% confidence interval; GGT: Gamma glutamyl transpeptidase; SHBP: Sex-hormone binding protein.

Citation: Cernea S, Onișor D, Roiban AL, Benedek T, Rat N. Metabolic dysfunction-associated steatotic liver disease-associated fibrosis and cardiac dysfunction in patients with type 2 diabetes. World J Cardiol 2024; 16(10): 580-594
URL: https://www.wjgnet.com/1949-8462/full/v16/i10/580.htm
DOI: https://dx.doi.org/10.4330/wjc.v16.i10.580