Retrospective Cohort Study
Copyright ©The Author(s) 2016.
World J Gastroenterol. Feb 28, 2016; 22(8): 2592-2600
Published online Feb 28, 2016. doi: 10.3748/wjg.v22.i8.2592
Table 1 Clinico-demographic characteristics of the study population n (%)
H. pylori (+)n = 1636H. pylori (-)n = 2027P value
Age (yr)54 (46-61)53.0 (43-60)< 0.001
Male988 (60.4)1153 (56.9)0.032
Body mass index (kg/m2)23.8 (21.8-25.7)23.5 (21.4-25.5)0.002
Diabetes215 (13.1)225 (11.1)0.059
Hypertension453 (27.7)483 (23.8)0.008
Metabolic syndrome334 (20.4)385 (19.0)0.281
Smoking699 (42.7)894 (44.1)0.403
Alcohol893 (54.6)1135 (56.0)0.394
Fasting glucose (mg/dL)93 (86-103)93 (86-102)0.611
Insulin (mIU/mL)5.9 (3.9-8.7)5.8 (3.9-8.5)0.732
HOMA-IR11.4 (0.9-2.2)1.3 (0.9-2.1)0.582
Hemoglobin A1c (%)5.5 (5.2-5.7)5.5 (5.2-5.8)0.763
Total cholesterol (mg/dL)201 (180-225)195 (173-220)< 0.001
Triglyceride (mg/dL)89 (58-137)86 (57-131)0.202
HDL-C (mg/dL)50 (43-59)51 (43-60)0.020
LDL-C (mg/dL)126 (104.0-147.8)120 (98-141)< 0.001
AST (IU/L)24 (20-30)24 (20-29)0.596
ALT (IU/L)24 (18-34)24 (18-34)0.249
AST/ALT1.0 (0.8-1.2)1.0 (0.8-1.2)0.198
GGT (IU/L)27 (18-43)25 (17-43)0.043
C-reactive protein (mg/dL)0.06 (0.03-0.13)0.06 (0.03-0.13)0.905
HSI233.2 (30.3-36.2)32.6 (29.8-36.0)0.005
HSI > 36505 (30.9)440 (21.7)0.173
NAFLD-LFS3-1.7 (-2.4 - -0.7)-1.8 (-2.4 - -0.7)0.122
NAFLD > -0.640469 (28.7)385 (19.0)0.778
1HOMA-IR = (fasting glucose × fasting insulin)/405;
2HSI = 8 × ALT/AST + body mass index (if diabetes mellitus, +2; if female, +2); 3NAFLD-LFS = -2.89 + 1.18 × metabolic syndrome (yes = 1, no = 0) + 0.45 × type 2 diabetes (yes = 2, no = 0) + 0.15 × insulin (mU/L) + 0.04 × AST (U/L) - 0.94 × AST/ALT. HOMA-IR: Homeostatic model assessment of insulin resistance; HDL-C: High-density lipoprotein cholesterol; LDL-C: Low-density lipoprotein cholesterol; AST: Aspartate aminotransferase; ALT: Alanine aminotransferase; GGT: Gamma-glutamyltransferase; HSI: Hepatic steatosis index; NAFLD: Nonalcoholic fatty liver disease; NAFLD-LFS: Nonalcoholic fatty liver disease liver fat score.
Table 2 Univariable analysis of nonalcoholic fatty liver disease according to hepatic steatosis index and nonalcoholic fatty liver disease liver fat score scores
HSI1
NAFLD-LFS2
OR95%CIP valueOR95%CIP value
Age0.9930.986-0.9990.0341.0171.010-1.024< 0.001
Male2.0431.731-2.410< 0.001
Body mass index1.4601.413-1.509< 0.001
Hypertension2.0011.703-2.350< 0.001
Metabolic syndrome4.7574.002-5.654< 0.001
Smoking1.3271.144-1.539< 0.0011.3011.115-1.5170.001
Alcohol1.0220.881-1.1860.7720.9020.773-1.0510.186
Presence of H. pylori1.1090.956-1.2860.1731.0220.876-1.1930.778
Fasting glucose1.0241.020-1.027< 0.001
Insulin1.2441.218-1.270< 0.001
HOMA-IR2.2402.076-2.417< 0.001
Total cholesterol1.0051.003-1.007< 0.0011.0041.001-1.0060.001
Triglyceride1.0091.007-1.010< 0.001
HDL-C0.9320.925-0.940< 0.001
LDL-C1.0081.006-1.010< 0.0011.0031.000-1.0050.021
C-reactive protein1.4101.163-1.710< 0.0011.6021.298-1.978< 0.001
Factors included in each scoring formula, such as sex, body mass index, diabetes, insulin, and metabolic syndrome components, were excluded from the analysis.
1HSI: 8 × ALT/AST + body mass index (if diabetes mellitus, +2; if female, +2);
2NAFLD-LFS: -2.89 + 1.18 × metabolic syndrome (yes = 1, no = 0) + 0.45 × type 2 diabetes (yes = 2, no = 0) + 0.15 × insulin (mU/L) + 0.04 × AST (U/L) - 0.94 × AST/ALT. NAFLD: Nonalcoholic fatty liver disease; HSI: Hepatic steatosis index; NAFLD-LFS: Nonalcoholic fatty liver disease liver fat score; HOMA-IR: Homeostatic model assessment of insulin resistance; HDL-C: High-density lipoprotein cholesterol; LDL-C: Low-density lipoprotein cholesterol.
Table 3 Multivariable analysis of nonalcoholic fatty liver disease according to hepatic steatosis index and nonalcoholic fatty liver disease-liver fat score scores
HSI1
NAFLD-LFS2
OR95%CIP valueOR95%CIP value
Age0.9930.986-1.0000.0381.0181.010-1.025< 0.001
Smoking1.3001.119-1.5110.0011.3421.148-1.568< 0.001
Presence of H. pylori1.1290.972-1.3110.1131.0070.862-1.1760.935
C-reactive protein1.4141.166-1.714< 0.0011.5461.254-1.906< 0.001
Factors included in the HSI or NAFLD-LFS formula, such as sex, body mass index, diabetes, insulin, or metabolic syndrome components, were excluded from the analysis.
1HSI = 8 × ALT/AST + body mass index (if diabetes mellitus, +2; if female, +2); 2NAFLD-LFS = -2.89 + 1.18 × metabolic syndrome (yes = 1, no = 0) + 0.45 × type 2 diabetes (yes = 2, no = 0) + 0.15 × insulin (mU/L) + 0.04 × AST (U/L) - 0.94 × AST/ALT. NAFLD: Nonalcoholic fatty liver disease; HSI: Hepatic steatosis index; NAFLD-LFS: Nonalcoholic fatty liver disease liver fat score.
Table 4 Characteristics of Studies Investigating Helicobacter pylori and nonalcoholic fatty liver disease
Ref.Type of studyCountryNo. of subjects (male)H. pylori detectionH. pylori % (female/male)NAFLD diagnosisNAFLD % (female/male)Association with H. pylori
Jamali et al[19], 2013RCT1Iran100 (49)13C UBT100% (N/A)Ultrasonography and elevated liver enzyme levels100%No association with H. pylori eradication
Polyzos et al[20], 2013Cross-sectionalGreece533Serum IgG, history of H. pylori eradication75.5% (N/A)Liver biopsy52.8% (39.6/13.2)Higher IgG seropositivity in NAFLD group
Okushin et al[21], 2015Cross-sectionalJapan5289 (1816)Serum IgG27.4% (27.5/27.1)Ultrasonography34.1% (25.4/50.7)None
Sumida et al[22], 2015Cross-sectionalJapan130 (65)Serum IgG40% (44.6/35.4)Liver biopsy100%Associated with hepatocyte ballooning
Polyzos et al[36], 2014Prospective2Greece12 (3)13C UBT50% (N/A)NAFLD-LFS HSENSI MRI-HFF100%Significant in HSENSI only
1Data compared between H. pylori eradication and lifestyle modification group vs lifestyle modification only group;
2Data collected at baseline and 12 months after H. pylori eradication;
328 (7 males) NAFLD cases vs 25 (5 males) controls. NAFLD: Nonalcoholic fatty liver disease; RCT: Randomized controlled trial; UBT: Urea breath test; N/A: Not available; IgG: Immunoglobulin G; NAFLD-FS: Nonalcoholic fatty liver disease liver fat score; HSENSI: Homocysteine, serum glutamic oxaloacetic transaminase, erythrocyte sedimentation rate, nonalcoholic steatohepatitis index; MRI-HFF: Magnetic resonance imaging hepatic fat fraction.