Increased liver markers are associated with higher risk of type 2 diabetes

doi:10.3748/wjg.v21.i24.7478

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World Journal of Gastroenterology

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1007-9327

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

Retrospective Cohort Study

World J Gastroenterol. Jun 28, 2015; 21(24): 7478-7487
Published online Jun 28, 2015. doi: 10.3748/wjg.v21.i24.7478

Table 1 Clinical characteristics of the participants n (%)

	Men			Women
	Nondiabetes	Diabetes	P value	Nondiabetes	Diabetes	P value
No.	2936	472		4923	532
Age (yr)	48.5 (0.35)	57.1 (0.60)	< 0.001	49.6 (0.29)	61.9 (0.76)	< 0.001
BMI (kg/m²)	24.1 (0.07)	24.5 (0.18)	0.012	23.4 (0.06)	25.6 (0.18)	< 0.001
Waist circumference (cm)	84.5 (0.21)	87.7 (0.53)	< 0.001	78.5 (0.20)	86.7 (0.52)	< 0.001
Systolic BP (mmHg)	121.1 (0.40)	125.1 (0.91)	< 0.001	117.2 (0.35)	129.4 (1.03)	< 0.001
Diastolic BP (mmHg)	80.0 (0.29)	78.3 (0.57)	0.006	74.7 (0.20)	75.5 (0.55)	0.178
Smoker, current	40.9 (1.17)	39.3 (2.69)	0.576	4.2 (0.37)	5.1 (1.21)	0.488
Drinking, mild to moderate	18.8 (0.90)	16.9 (2.14)	0.438	3.3 (0.33)	2.2 (0.89)	0.330
Regular exercise	22.8 (0.94)	22.7 (2.39)	0.983	18.9 (0.80)	13.7 (2.02)	0.030
Income, lowest quartile	13.7 (0.85)	26.7 (2.56)	< 0.001	18.1 (0.79)	35.7 (2.54)	< 0.001
Education, ≤ middle school	25.1 (1.12)	41.0 (2.88)	< 0.001	39.3 (1.11)	75.7 (2.64)	< 0.001
Rural area	20.6 (2.22)	24.5 (3.43)	0.140	21.6 (2.18)	26.5 (3.51)	0.045
Hypertension	31.3 (1.11)	54.3 (2.73)	< 0.001	24.8 (0.80)	63.8 (2.89)	< 0.001
Hypercholesterolemia	11.5 (0.70)	25.7 (2.50)	< 0.001	13.4 (0.60)	36.50 (2.4)	< 0.001
Metabolic syndrome	25.4 (1.03)	66.1 (2.74)	< 0.001	24.2 (0.68)	80.8 (2.33)	< 0.001
FPG (mg/dL)	94.3 (0.24)	147.4 (3.19)	< 0.001	91.6 (0.17)	138.5 (2.28)	< 0.001
Triglycerides (mg/dL)¹	128.2 (124.4-132.2)	146.1 (134.9-158.3)	0.003	94.6 (92.8-96.5)	137.3 (129.5-145.5)	< 0.001
Total cholesterol (mg/dL)	193.1 (0.81)	181.3 (2.32)	< 0.001	191.9 (0.66)	194.0 (2.18)	0.353
HDL-cholesterol (mg/dL)	49.0 (0.29)	45.7 (0.75)	< 0.001	55.5 (0.22)	49.5 (0.67)	< 0.001
LDL-cholesterol (mg/dL)	114.7 (0.78)	102.0 (2.02)	< 0.001	114.5 (0.55)	113.0 (2.04)	0.487
ALT (IU/L)¹	22.3 (21.8-22.8)	25.3 (23.8-26.9)	< 0.001	15.3 (15.0-15.5)	21.0 (20.0-22.1)	< 0.001
AST (IU/L)¹	22.3 (22.0-22.6)	24.0 (22.9-25.1)	0.003	19.2 (19.0-19.4)	22.1 (21.2-23.0)	< 0.001
AST/ALT	1.1 (0.01)	1.0 (0.03)	0.265	1.3 (0.01)	1.1 (0.02)	< 0.001
GGT¹	33.9 (32.9-34.9)	42.5 (39.3-46.0)	< 0.001	18.8 (18.4-19.1)	26.6 (25.1-28.1)	< 0.001

¹Geometric mean (95%CI). Data are presented as the mean ± SE, or percentage (SE). BMI: Body mass index; BP: Blood pressure; FPG: Fasting plasma glucose; HDL: High density lipoprotein; LDL: Low density lipoprotein; AST: Aspartate aminotransferase; ALT: Alanine aminotransferase; GGT: Gamma-glutamyltransferase.

Table 2 Adjusted odds ratios for the prevalence of type 2 diabetes according to quartile groups of liver markers

	Men				Women
	ALT	AST	AST/ALT	GGT	ALT	AST	AST/ALT	GGT
Model 1
Q1	1	1	1	1	1	1	1	1
Q2	1.04 (0.708-1.515)	0.62 (0.429-0.891)	0.58 (0.416-0.812)	1.81 (1.195-2.748)	1.54 (0.975-2.429)	1.16 (0.811-1.670)	0.44 (0.338-0.569)	0.84 (0.537-1.319)
Q3	1.61 (1.105-2.343)	0.75 (0.525-1.068)	0.37 (0.256-0.519)	2.07 (1.406-3.051)	2.74 (1.723-4.351)	0.78 (0.527-1.141)	0.16 (0.112-0.233)	1.68 (1.102-2.559)
Q4	2.63 (1.820-3.797)	1.16 (0.824-1.617)	0.24 (0.162-0.351)	3.47 (2.372-5.074)	5.31 (3.528-7.991)	1.27 (0.884-1.816)	0.17 (0.118-0.242)	3.99 (2.766-5.744)
P for trend	< 0.001	0.256	< 0.001	< 0.001	< 0.001	0.396	< 0.001	< 0.001
Model 2
Q1	1	1	1	1	1	1	1	1
Q2	1.07 (0.698-1.652)	0.55 (0.366-0.836)	0.67 (0.447-0.998)	1.61 (1.015-2.538)	1.27 (0.777-2.077)	1.08 (0.741-1.577)	0.51 (0.377-0.695)	0.69 (0.426-1.116)
Q3	1.43 (0.899-2.274)	0.74 (0.484-1.119)	0.42 (0.270-0.640)	2.03 (1.312-3.151)	1.90 (1.158-3.120)	0.70 (0.449-1.092)	0.23 (0.154-0.357)	1.11 (0.686-1.801)
Q4	2.22 (1.381-3.559)	0.96 (0.640-1.432)	0.30 (0.185-0.483)	3.05 (1.913-4.877)	3.16 (1.990-5.026)	1.06 (0.714-1.571)	0.28 (0.188-0.429)	2.23(1.459-3.397)
P for trend	< 0.001	0.681	< 0.001	< 0.001	< 0.001	0.926	< 0.001	< 0.001

Model 1: adjusted for age; Model 2: adjusted for age, BMI, smoking, alcohol intake, regular physical activity, education level, income level, hypertension, hypercholesterolemia, and hypertriglyceridemia; ALT quartile (IU/L): 15, 21, and 29 IU/L in men and 12, 15, and 20 IU/L in women; AST quartile (IU/L): 19, 22, and 26 IU/L in men and 16, 19, and 23 IU/L in women; AST/ALT quartile: 0.8, 1.1, and 1.3 in men and 1.1, 1.3, and 1.5 in women; GGT quartile (IU/L): 21, 29, and 47 IU/L in men and 13, 17, and 23 IU/L in women. AST: Aspartate aminotransferase; ALT: Alanine aminotransferase; GGT: Gamma-glutamyltransferase.

Table 3 Adjusted odds ratios for the prevalence of impaired fasting glucose according to quartile groups of liver markers

	Men				Women
	ALT	AST	AST/ALT	GGT	ALT	AST	AST/ALT	GGT
Model 1
Q1	1	1	1	1	1	1	1	1
Q2	1.29 (0.942-1.754)	1.40 (1.030-1.889)	0.65 (0.487-0.855)	1.46 (1.066-1.998)	1.50 (1.117-2.022)	1.15 (0.863-1.540)	0.63 (0.496-0.805)	2.05 (1.452-2.902)
Q3	1.69 (1.269-2.246)	1.57 (1.171-2.095)	0.46 (0.342-0.612)	2.54 (1.907-3.393)	1.98 (1.474-2.658)	1.09 (0.785-1.502)	0.37 (0.285-0.475)	3.74 (2.606-5.355)
Q4	2.76 (2.026-3.750)	2.08 (1.532-2.815)	0.39 (0.283-0.547)	3.63 (2.721-4.852)	3.24 (2.397-4.369)	1.70 (1.265-2.274)	0.32 (0.248-0.423)	5.56 (3.970-7.780)
P for trend	< 0.001	< 0.001	< 0.001	< 0.001	< 0.001	0.001	< 0.001	< 0.001
Model 2
Q1	1	1	1	1	1	1	1	1
Q2	1.07 (0.738-1.546)	1.29 (0.905-1.849)	0.77 (0.550-1.077)	1.27 (0.871-1.843)	1.27 (0.904-1.789)	1.04 (0.749-1.444)	0.72 (0.556-0.936)	1.98 (1.333-2.946)
Q3	1.07 (0.752-1.513)	1.33 (0.924-1.906)	0.63 (0.446-0.890)	1.97 (1.362-2.856)	1.53 (1.081-2.151)	0.92 (0.642-1.323)	0.48 (0.360-0.642)	2.97 (1.974-4.469)
Q4	1.69 (1.172-2.447)	1.46 (1.009-2.111)	0.70 (0.464-1.055)	2.32 (1.608-3.356)	2.00 (1.422-2.823)	1.34 (0.980-1.838)	0.49 (0.365-0.667)	4.00 (2.720-5.874)
P for trend	0.005	0.053	0.042	< 0.001	< 0.001	0.094	< 0.001	< 0.001

Model 1: adjusted for age; Model 2: adjusted for age, body mass index, smoking, alcohol intake, regular physical activity, education level, income level, hypertension, hypercholesterolemia, and hypertriglyceridemia; ALT quartile (IU/L): 15, 21, and 29 IU/L in men and 12, 15, and 20 IU/L in women; AST quartile (IU/L): 19, 22, and 26 IU/L in men and 16, 19, and 23 IU/L in women; AST/ALT quartile: 0.8, 1.1, and 1.3 in men and 1.1, 1.3, and 1.5 in women; GGT quartile (IU/L): 21, 29, and 47 IU/L in men and 13, 17, and 23 IU/L in women. AST: Aspartate aminotransferase; ALT: Alanine aminotransferase; GGT: Gamma-glutamyltransferase.

Table 4 Risk of diabetes and impaired fasting glucose examined by combinations of liver markers

	Men		Women
	OR (95%CI)	P value	OR (95%CI)	P value
In type 2 diabetes
ALT, highest quartile, and AST/ALT, lowest quartile	2.77 (1.749-4.371)	< 0.001	3.76 (2.731-5.175)	< 0.001
ALT, highest quartile, and GGT, highest quartile	2.37 (1.486-3.794)	< 0.001	4.03 (2.961-5.492)	< 0.001
GGT, highest quartile, and AST/ALT, lowest quartile	2.73 (1.614-4.634)	< 0.001	4.20 (2.987-5.903)	< 0.001
ALT, GGT, highest quartile, and AST/ALT, lowest quartile	3.21 (1.829-5.622)	< 0.001	4.60 (3.217-6.582)	< 0.001
In IFG
ALT, highest quartile, and AST/ALT, lowest quartile	2.04 (1.410-2.952)	< 0.001	1.88 (1.439-2.458)	< 0.001
ALT, highest quartile, and GGT, highest quartile	2.10 (1.413-3.105)	< 0.001	2.27 (1.676-3.072)	< 0.001
GGT, highest quartile, and AST/ALT, lowest quartile	1.79 (1.182-2.716)	0.006	2.38 (1.761-3.220)	< 0.001
ALT, GGT, highest quartile, and AST/ALT, lowest quartile	1.99 (1.264-3.131)	0.003	2.40 (1.720-3.354)	< 0.001

Adjusted for age, body mass index, smoking, alcohol intake, regular physical activity, education level, income level, hypertension, and hypercholesterolemia, and hypertriglyceridemia. ALT highest quartile (IU/L): ≥ 29 in men and ≥ 20 in women; AST highest quartile (IU/L): ≥ 26 in men and ≥ 23 in women; AST/ALT lowest quartile: < 0.8 in men and < 1.1 in women; GGT highest quartile (IU/L): ≥ 47 in men and ≥ 23 in women. AST: Aspartate aminotransferase; ALT: Alanine aminotransferase; GGT: Gamma-glutamyltransferase.

Citation: Ko SH, Baeg MK, Han KD, Ko SH, Ahn YB. Increased liver markers are associated with higher risk of type 2 diabetes. World J Gastroenterol 2015; 21(24): 7478-7487
URL: https://www.wjgnet.com/1007-9327/full/v21/i24/7478.htm
DOI: https://dx.doi.org/10.3748/wjg.v21.i24.7478