Histopathological differences utilizing the nonalcoholic fatty liver disease activity score criteria in diabetic (type 2 diabetes mellitus) and non-diabetic patients with nonalcoholic fatty liver disease

doi:10.4254/wjh.v7.i25.2610

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World Journal of Hepatology

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Retrospective Cohort Study

World J Hepatol. Nov 8, 2015; 7(25): 2610-2618
Published online Nov 8, 2015. doi: 10.4254/wjh.v7.i25.2610

Table 1 Characteristics of patients with nonalcoholic fatty liver disease, divided according to nonalcoholic fatty liver disease without type 2 diabetes mellitus and nonalcoholic fatty liver disease with type 2 diabetes mellitus (mean ± SD)

Parameter	All patients (n = 235)	NAFLD (without T2DM) (n = 158)	NAFLD (with T2DM) (n = 77)	P value
Age (yr)	45.3 ± 11.9	43.0 ± 12.2	49.9 ± 9.8	< 0.01
Gender (male/female)	91/144	69/89	22/55	0.02
Race (% Caucasian)	65.1	63.9	67.5	0.9
BMI (kg/m²)	37.6 ± 11.5	35.9 ± 10.6	41.0 ± 12.6	< 0.01
Hypertension, n (%)	114 (48.1)	59 (37.3)	55 (71.4)	< 0.01
Dyslipidemia, n (%)	139 (68.8)	82 (61.2)	57 (83.8)	< 0.01
Metabolic syndrome, n (%)	115 (53.7)	52 (36.4)	63 (88.7)	< 0.01
Abnormal LFT’s as an indication of liver biopsy, n (%)	159 (67.6)	117 (74.0)	42 (54.5)	0.02
Platelets	257.5 ± 73.5	262.6 ± 67.7	247.4 ± 83.3	0.15
INR	0.99 ± 0.16	0.97 ± 0.10	1.02 ± 0.23	0.03
Protein (g/dL)	7.4 ± 0.72	7.4 ± 0.73	7.3 ± 0.70	0.12
Albumin (g/dL)	4.3 ± 0.5	4.3 ± 0.5	4.2 ± 0.46	0.06
AST (U/L)	49.8 ± 34.5	50.4 ± 38.4	48.3 ± 24.8	0.6
ALT (U/L)	72.6 ± 58.5	79.2 ± 65.4	59.2 ± 38	0.01
Bilirubin (mg/dL)	0.67 ± 0.4	0.68 ± 0.4	0.62 ± 0.3	0.3
Alkaline Phosphate	96.7 ± 61.8	94.9 ± 68.2	100.1 ± 46.9	0.5
Total cholesterol (mg/dL)	200.2 ± 47.3	200.9 ± 45.4	198.8 ± 50.9	0.8
HDL cholesterol (mg/dL)	44.3 ± 11.8	44.2 ± 12.0	44.6 ± 11.7	0.9
Triglycerides (mg/dL)	211.4 ± 119.9	209.7 ± 127.7	214.4 ± 105.9	0.8
LDL cholesterol (mg/dL)	118.9 ± 41.0	120.5 ± 41.3	116.4 ± 40.8	0.6
Fasting glucose (mg/dL)	125.6 ± 55.5	102.9 ± 28.3	167.0 ± 67.8	< 0.01
HbA1c	6.93 ± 2.09	5.83 ± 1.11	8.09 ± 2.26	< 0.01
Iron (μg/dL)	82.6 ± 38.7	89.3 ± 40.8	71.3 ± 32.0	< 0.01
Total iron binding capacity (μg/dL)	322.4 ± 72.3	317.16 ± 71.8	333.0 ± 72.9	0.2
Ferritin (ng/mL)	258.2 ± 306.0	281 ± 323.1	223.0 ± 276.7	0.3
AST/ALT	0.836 ± 0.432	0.781 ± 0.434	0.947 ± 0.41	< 0.01
FIB-4 index	1.26 ± 1.01	1.06 ± 0.77	1.65 ± 1.28	< 0.01
APRI	0.581 ± 0.471	0.549 ± 0.458	0.643 ± 0.493	0.16

NAFLD: Nonalcoholic fatty liver disease; T2DM: Type 2 diabetes mellitus; AST: Aspartate transaminase; ALT: Alanine transaminase; LDL: Low-density lipoprotein cholesterol; NAS: NAFLD activity score; HDL: High-density lipoprotein cholesterol; BMI: Body mass index; INR: International normalized ratio; APRI: AST to platelet ratio index; LFT: Liver function test.

Table 2 Characteristics of patients with nonalcoholic fatty liver disease, divided according to nonalcoholic steatohepatitis and steatosis (mean + SD)

Parameter	All patients (n = 235)	NASH	Steatosis	P value
Age (yr)	45.3 + 11.9	45.9 + 12.4	43.8 + 10.4	0.2
Gender (male/female)	91/144	67/101	24/43	0.6
Race (% caucasian)	65.1	64.9	65.7	0.1
BMI (kg/m²)	37.7 + 11.5	37 + 10.6	39.4 + 13.7	0.17
Hypertension, n (%)	114 (48.5)	82 + 48.8	32 + 63.9	1
Dyslipidemia, n (%)	139 (68.8)	100 (70.9)	39 (63.9)	0.3
Metabolic syndrome, n (%)	115 + 53.7	67 (42.7)	32 (56.1)	0.08
Platelets	258 + 73.5	247 + 72.1	283 + 71.1	< 0.01
INR	0.996 + 0.162	1 + 0.178	0.98 + 0.112	0.3
Protein (g/dL)	7.39 + 0.762	7.39 + 0.733	7.37 + 0.714	0.8
Albumin (g/dL)	4.27 + 0.536	4.27 + 0.555	4.26 + 0.487	0.8
AST (U/L)	49.8 + 34.5	54.2 + 36.3	38.3 + 26.1	< 0.01
ALT (U/L)	72.6 + 58.5	78.7 + 63.1	57 + 40.7	0.01
Bilirubin (mg/dL)	0.668 + 0.416	0.71 + 0.456	0.567 + 0.275	0.01
Alkaline Phosphate	96.7 + 61.8	100 + 70.9	88.3 + 28.3	0.1
Total cholesterol (mg/dL)	200 + 47.3	202 + 48.6	197 + 44.5	0.5
HDL cholesterol (mg/dL)	44.4 + 11.9	42.7 + 10.7	48.1 + 13.6	0.01
Triglycerides (mg/dL)	211 + 120	220 + 125	191 + 105	0.18
LDL cholesterol (mg/dL)	1119 + 41	121 + 41.6	114 + 39.8	0.33
Fasting glucose (mg/dL)	126 + 55.5	129 + 55.9	117 + 53.8	0.14
HbA1c	6.93 + 2.09	7.12 + 2.19	6.37 + 1.69	0.11
Iron (μg/dL)	82.6 + 38.7	83.8 + 40.5	78.6 + 31.9	0.52
Total iron binding capacity (μg/dL)	322 + 72.3	319 + 74.6	335 + 63.4	0.31
Ferritin (ng/mL)	258 + 306	276 + 324	201 + 232	0.21
Mallory bodies	50 + 21.3	50 + 29.8	0	< 0.01
CAD	67 + 28.9	50 + 29.9	17 + 26.2	0.63
Gastric bypass	21 + 8.94	14 + 8.33	7 + 10.4	0.61
Cirrhosis	14 + 5.96	14 + 8.33	0	0.01
Steatosis	1.92 + 0.861	2.1 + 0.83	1.46 + 0.765	< 0.01
Inflammation	0.44 + 0.62	0.625 + 0.663	0	< 0.01
Fibrosis	0.753 + 1.11	1.05 + 1.21	0	< 0.01
Ballooning	0.821 + 0.712	1.15 + 0.575	0	< 0.01
NAS score	3.18 + 1.69	3.86 + 1.45	1.46 + 0.765	< 0.01

AST: Aspartate transaminase; ALT: Alanine transaminase; HDL: High-density lipoprotein cholesterol; NAS: Nonalcoholic fatty liver disease activity score; NASH: Nonalcoholic steatohepatitis; LDL: Low-density lipoprotein cholesterol; BMI: Body mass index; INR: International normalized ratio; CAD: Coronary artery disease.

Table 3 Histological findings of patients with nonalcoholic fatty liver disease, divided according to nonalcoholic fatty liver disease without type 2 diabetes mellitus and nonalcoholic fatty liver disease with type 2 diabetes mellitus n (%)

Parameter	All patients (n = 235)	NAFLD (without T2DM) (n = 158)	NAFLD (with T2DM) (n = 77)	P value
NAS score (mean ± SD)	3.2 ± 1.7	3.0 ± 1.6	3.5 ± 1.7	0.03
Fibrosis score (mean ± SD)	0.75 ± 1.1	0.52 ± 0.9	1.2 ± 1.3	< 0.01
Fibrosis score				< 0.01
< 2	191 (81.3)	139 (88.0)	52 (67.5)
≥ 2	44 (18.7)	19 (12.0)	25 (32.5)
NAS score				0.12
< 5	179 (76.2)	125 (79.1)	54 (70.1)
≥ 5	56 (23.8)	33 (20.9)	23 (29.9)
NAS score				0.11
< 3	90 (38.3)	66 (41.7)	24 (31.2)
≥ 3	145 (61.7)	92 (58.3)	53 (68.8)
Steatosis				0.1
< 2	97 (41.3)	71 (44.9)	26 (33.8)
≥ 2	138 (58.7)	87 (55.1)	51 (66.2)
Ballooning				< 0.01
< 2	193 (82.1)	137 (86.7)	56 (72.7)
2	42 (17.9)	21 (13.3)	21 (27.3)
Inflammation				0.4
< 2	218 (92.7)	148 (93.7)	70 (90.9)
≥ 2	17 (7.3)	10 (6.3)	7 (9.1)
Mallory bodies	50 (21.3)	28 (17.7)	22 (28.6)	0.06

NAFLD: Nonalcoholic fatty liver disease; NAS: NAFLD activity score; T2DM: Type 2 diabetes mellitus.

Table 4 Variables associated with nonalcoholic steatohepatitis (nonalcoholic fatty liver disease activity score ≥ 5) (multivariate analysis)

Variables	P value	Odds ratio	95%CI
All patients
Presence of T2DM	< 0.01	3.27	1.43-7.50
ALT ≥ 36	0.029	3.88	1.15-13.1
Protein	0.045	1.84	1.01-3.35
Patients with NAFLD without T2DM
Protein	0.048	3.06	1.01-9.25
Patients with NAFLD with T2DM
ALT ≥ 36	0.03	4.21	1.13-15.6

ALT: Alanine transaminase; NAFLD: Nonalcoholic fatty liver disease; T2DM: Type 2 diabetes mellitus.

Table 5 Variables associated with advanced fibrosis (multivariate analysis)

Variables	P value	Odds ratio	95%CI
All patients
Presence of T2DM	< 0.01	3.45	1.53-7.77
Platelet	0.025	0.99	0.99-1.0
INR	< 0.01	4151	97.7-176426
Patients with NAFLD without T2DM
Platelet	0.03	0.99	0.98-0.99
INR	0.001	16950	62.4-4607293
Patients with NAFLD with T2DM
Platelet	0.045	0.99	0.98-0.99

NAFLD: Nonalcoholic fatty liver disease; T2DM: Type 2 diabetes mellitus; INR: International normalized ratio.

Citation: Puchakayala BK, Verma S, Kanwar P, Hart J, Sanivarapu RR, Mohanty SR. Histopathological differences utilizing the nonalcoholic fatty liver disease activity score criteria in diabetic (type 2 diabetes mellitus) and non-diabetic patients with nonalcoholic fatty liver disease. World J Hepatol 2015; 7(25): 2610-2618
URL: https://www.wjgnet.com/1948-5182/full/v7/i25/2610.htm
DOI: https://dx.doi.org/10.4254/wjh.v7.i25.2610