Cholecystectomy is independently associated with nonalcoholic fatty liver disease in an Asian population

doi:10.3748/wjg.v21.i20.6287

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World Journal of Gastroenterology

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World J Gastroenterol. May 28, 2015; 21(20): 6287-6295
Published online May 28, 2015. doi: 10.3748/wjg.v21.i20.6287

Table 1 Baseline characteristics of control and nonalcoholic fatty liver disease subjects

	Control (P = 12275)	NAFLD (P = 5337)	P value
Age (yr)	47.4 ± 11.4	50.9 ± 10.5	< 0.001
Male	4839 (39.4)	3843 (72.0)	< 0.001
Waist circumference (cm)	80.3 ± 7.2	89.2 ± 6.9	< 0.001
Body mass index (kg/m²)	22.0 ± 2.6	25.4 ± 2.7	< 0.001
Systolic blood pressure (mmHg)	111.3 ± 14.3	119.3 ± 13.2	< 0.001
Diastolic blood pressure (mmHg)	71.4 ± 11.0	78.1 ± 10.5	< 0.001
Hypertension	1570 (12.8)	1451 (27.2)	< 0.001
Diabetes	373 (3.0)	498 (9.3)	< 0.001
Gamma-glutamyl transpeptidase (IU/L)	24.7 ± 31.3	42.7 ± 39.8	< 0.001
Alanine aminotransferase (IU/L)	19.1 ± 16.1	33.0 ± 23.5	< 0.001
Aspartate aminotransferase (IU/L)	20.7 ± 11.5	25.6 ± 12.8	< 0.001
Total cholesterol (mg/dL)	191.6 ± 32.9	200.5 ± 34.9	< 0.001
Triglycerides (mg/dL)	85.9 ± 50.0	144.8 ± 84.1	< 0.001
HDL-cholesterol (mg/dL)	57.6 ± 12.3	48.9 ± 9.6	< 0.001
Fasting glucose (mg/dL)	92.4 ± 12.7	102.5 ± 19.8	< 0.001
HbA1c (%)	5.7 ± 0.4	6.0 ± 0.7	< 0.001
Fasting insulin, μIU/mL (n = 8622)	5.8 ± 3.4	9.6 ± 5.5	< 0.001
HOMA-IR index (n = 8622)	1.4 ± 1.0	2.5 ± 1.6	< 0.001
Gallstones	421 (3.4)	292 (5.5)	< 0.001
Cholecystectomy	207 (1.7)	149 (2.8)	< 0.001
Gallstone disease	628 (5.1)	441 (8.3)	< 0.001
Smoking
Never-smoker	8300 (67.6)	2365 (44.3)	< 0.001
Current smoker	1419 (11.6)	1114 (20.9)
Ex-smoker	2556 (20.8)	1858 (34.8)
Regular physical activity	8112 (66.1)	3496 (65.5)	0.455

Data are presented as the mean ± SD or n (%). NAFLD: Nonalcoholic fatty liver disease; IR: Insulin resistance.

Table 2 Baseline characteristics of the subjects according to gallstone disease status

	Control (n = 16543)	Gallstone disease (n = 1069)	Gallstone disease (n = 1069)
	Control (n = 16543)	Gallstone disease (n = 1069)	Gallstones (n = 713)	Cholecystectomy (n = 356)
Age (yr)	48.1 ± 11.1	54.5 ± 11.4^a	53.8 ± 11.2^b	55.8 ± 11.5^c
Male	8122 (49.1)	560 (52.4)^a	377 (52.9)^b	183 (51.4)
Waist circumference (cm)	82.8 ± 8.2	86.4 ± 8.5^a	86.3 ± 8.2^b	86.3 ± 7.7^c
Body mass index (kg/m²)	23.0 ± 3.1	24.1 ± 3.2^a	24.0 ± 3.1^b	23.9 ± 2.9^c
Systolic blood pressure (mmHg)	113.5 ± 14.4	116.3 ± 15.2^a	117.0 ± 15.0^b	118.4 ± 14.5^c
Diastolic blood pressure (mmHg)	73.3 ± 11.3	75.2 ± 11.4^a	75.2 ± 11.2^b	75.2 ± 10.6^c
Hypertension	2710 (16.4)	311 (29.1)^a	205 (28.8)^b	106 (29.8)^c
Diabetes	771 (4.7)	100 (9.4)^a	67 (9.4)^b	33 (9.3)^c
Gamma-glutamyl transpeptidase (IU/L)	29.8 ± 32.9	34.6 ± 48.8^a	35.7 ± 58.8^b	38.0 ± 75.0^c
Alanine aminotransferase (IU/L)	23.1 ± 19.8	25.9 ± 18.6^a	26.0 ± 17.9^b	26.1 ± 16.4^c
Aspartate aminotransferase (IU/L)	22.1 ± 12.2	23.2 ± 11.1^a	23.6 ± 10.7^b	24.5 ± 9.9^c
Total cholesterol (mg/dL)	194.4 ± 33.7	193.4 ± 33.7	192.5 ± 33.6	190.6 ± 33.4^c
Triglycerides (mg/dL)	103.2 ± 68.0	111.1 ± 62.3^a	112.9 ± 65.9^b	116.4 ± 72.5^c
HDL-cholesterol (mg/dL)	55.1 ± 12.2	53.2 ± 12.1^a	53.3 ± 12.2^b	53.7 ± 12.6^c
Fasting glucose (mg/dL)	95.2 ± 15.5	99.6 ± 20.4^a	99.6 ± 20.8^b	99.5 ± 17.0^c
HbA1c (%)	5.8 ± 0.5	5.9 ± 0.7^a	5.9 ± 0.6^b	6.0 ± 0.5^c
Fasting insulin, μIU/mL (n = 8622)	6.9 ± 4.4	8.3 ± 6.2^a	8.3 ± 6.0^b	8.3 ± 5.7^c
HOMA- IR index (n = 8622)	1.7 ± 1.3	2.1 ± 1.7^a	2.1 ± 1.7^b	2.2 ± 1.7^c
NAFLD	4896 (29.6)	441 (41.3)^a	292 (41.0)^b	149 (41.9)^c
Smoking
Never-smoker	10042 (60.7)	623 (58.3)^a	419 (58.8)	204 (57.3)^c
Current smoker	2398 (14.5)	135 (12.6)^a	95 (13.3)	40 (11.2)^c
Ex-smoker	4103 (24.8)	311 (29.1)^a	199 (27.9)	112 (31.5)^c
Regular physical activity	10835 (65.5)	773 (72.3)^a	521 (73.1)^b	252 (70.8)^c

Data are presented as the mean ± SD or n (%).

^aP < 0.05, control vs gallstone disease;

^bP < 0.05, control vs gallstone;

^cP < 0.05, control vs cholecystectomy. NAFLD: Nonalcoholic fatty liver disease; GSD: Gallstone disease; IR: Insulin resistance.

Table 3 Univariate and multivariate analyses for the presence of nonalcoholic fatty liver disease according to gallstone disease status

Variable	Univariate model		Age, sex-adjusted model		Multivariate model¹
Variable	OR (95%CI)	P value	OR (95%CI)	P value	OR (95%CI)	P value
Gallstone disease
Control (n = 16543)	1		1		1
Gallstone disease (n = 1069)	1.67 (1.47-1.90)	< 0.001	1.47 (1.28-1.68)	< 0.001	1.22 (1.04-1.43)	0.016
Cholecystectomy
Control	1		1		1
Cholecystectomy (n = 356)	1.67 (1.35-2.07)	< 0.001	1.46 (1.16-1.83)	0.001	1.35 (1.03-1.77)	0.028
Gallstones
Control	1		1		1
Gallstones (n = 713)	1.65 (1.42-1.92)	< 0.001	1.46 (1.24-1.72)	< 0.001	1.15 (0.95-1.39)	0.153

¹The multivariate model was adjusted for age, sex, hypertension, diabetes, body mass index, smoking, physical activity, total cholesterol, triglycerides and HDL cholesterol. NAFLD: Nonalcoholic fatty liver disease; OR: Odds ratio.

Table 4 Comparison of characteristics between subjects who underwent fasting insulin testing and those who did not

	Fasting insulin absent (n = 8990)	Fasting insulin available (n = 8622)	P value
Age (yr)	45.8 ± 11.8	51.2 ± 9.9	< 0.001
Male	4808 (46.5)	4748 (55.1)	< 0.001
Waist circumference (cm)	82.8 ± 8.3	83.3 ± 8.1	< 0.001
Body mass index (kg/m²)	23.0 ± 3.1	23.1 ± 3.0	0.167
Systolic blood pressure (mmHg)	113.2 ± 14.2	114.3 ± 14.6	< 0.001
Diastolic blood pressure (mmHg)	73.3 ± 11.3	73.9 ± 11.3	0.020
Hypertension	1300 (14.5)	1721 (20.0)	< 0.001
Diabetes	356 (4.0)	515 (6.0)	< 0.001
Gamma-glutamyl transpeptidase (IU/L)	30.1 ± 30.7	30.3 ± 39.0	0.732
Alanine aminotransferase (IU/L)	23.1 ± 19.4	23.5 ± 20.0	0.142
Aspartate aminotransferase (IU/L)	21.8 ± 12.4	22.6 ± 11.8	< 0.001
Total cholesterol (mg/dL)	193.0 ± 33.3	195.6 ± 34.1	< 0.001
Triglycerides (mg/dL)	105.0 ± 70.2	102.5 ± 65.5	0.017
HDL-cholesterol (mg/dL)	55.0 ± 12.0	55.0 ± 12.5	0.693
Fasting glucose (mg/dL)	95.4 ± 14.9	95.6 ± 16.9	0.606
HbA1c (%)	5.77 ± 0.51	5.84 ± 0.56	< 0.001
NAFLD	2619 (29.1)	2718 (31.5)	0.001
Gallstone	336 (3.7)	377 (4.4)	0.033
Cholecystectomy	160 (1.8)	196 (2.3)	0.020
Gallstone disease	496 (5.5)	573 (6.6)	0.002
Smoking			< 0.001
Never-smoker	5300 (59.0)	5365 (62.2)
Current smoker	1440 (16.0)	1093 (12.7)
Ex-smoker	2250 (25.0)	2164 (25.1)
Regular physical activity	5559 (61.8)	6049 (70.2)	< 0.001

Data are presented as the mean ± SD or n (%). NAFLD: Nonalcoholic fatty liver disease; IR: Insulin resistance.

Table 5 Univariate and multivariate analyses for the presence of nonalcoholic fatty liver disease according to gallstone disease status in subjects in whom fasting insulin testing was performed

Variable	Univariate model		Age, sex-adjusted model		Multivariate model 1¹		Multivariate model 2²
Variable	OR (95%CI)	P value	OR (95%CI)	P value	OR (95%CI)	P value	OR (95%CI)	P value
Gallstone disease
Control (n = 8049)	1		1		1		1
Gallstone disease (n = 573)	1.67 (1.41-1.99)	< 0.001	1.51 (1.26-1.82)	< 0.001	1.27 (1.03-1.58)	0.029	1.25 (1.00-1.55)	0.052
Cholecystectomy
Control	1		1		1		1
Cholecystectomy (n = 196)	1.76 (1.32-2.35)	< 0.001	1.59 (1.17-2.16)	0.003	1.45 (1.01-2.07)	0.044	1.45 (1.01-2.08)	0.045
Gallstones
Control	1		1		1		1
Gallstones (n = 377)	1.63 (1.32-2.01)	< 0.001	1.48 (1.18-1.85)	0.001	1.18 (0.91-1.54)	0.21	1.14 (0.87-1.50)	0.336

¹The multivariate model 1 was adjusted for age, sex, hypertension, diabetes, body mass index, smoking, physical activity, total cholesterol, triglycerides and high-density lipoprotein cholesterol;

²The multivariate model 2 was adjusted for multivariate model 1 in addition to insulin resistance as assessed by HOMA-IR. NAFLD: Nonalcoholic fatty liver disease; IR: Insulin resistance; OR: Odds ratio; HOMA-IR: Homeostasis model assessment-estimated insulin resistance.

Citation: Kwak MS, Kim D, Chung GE, Kim W, Kim YJ, Yoon JH. Cholecystectomy is independently associated with nonalcoholic fatty liver disease in an Asian population. World J Gastroenterol 2015; 21(20): 6287-6295
URL: https://www.wjgnet.com/1007-9327/full/v21/i20/6287.htm
DOI: https://dx.doi.org/10.3748/wjg.v21.i20.6287