Helicobacter pylori infection might have a potential role in hepatocyte ballooning in nonalcoholic fatty liver disease

Journal of Gastroenterology

Volumn 50, Issue 9, 2015, Pages 996-1004

  Sumida, Yoshio ^a   Kanemasa, Kazuyuki ^b   Imai, Shunsuke ^b   Mori, Kojiro ^b   Tanaka, Saiyu ^b   Shimokobe, Hideto ^b   Kitamura, Yoko ^b   Fukumoto, Kohei ^b   Kakutani, Akira ^b   Ohno, Tomoyuki ^b   Taketani, Hiroyoshi ^a   Seko, Yuya ^a   Ishiba, Hiroshi ^a   Hara, Tasuku ^a   Okajima, Akira ^a   Yamaguchi, Kanji ^a   Moriguchi, Michihisa ^a   Mitsuyoshi, Hironori ^a   Yasui, Kohichiroh ^a   Minami, Masahito ^a   Itoh, Yoshito ^a   more..

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b Nara City Hospital   (Japan)

Author keywords

Helicobacter pylori; Hepatocyte ballooning; Nonalcoholic steatohepatitis

Indexed keywords

IMMUNOGLOBULIN G; IRON; BIOLOGICAL MARKER;

ADULT; ARTICLE; BIOCHEMICAL ANALYSIS; DISEASE SEVERITY; FEMALE; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; HELICOBACTER INFECTION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER CELL; LIVER FIBROSIS; LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MALE; NONALCOHOLIC FATTY LIVER; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL; SEX DIFFERENCE; BIOPSY; BLOOD; DISEASE COURSE; GLUCOSE TOLERANCE TEST; HELICOBACTER PYLORI; IMMUNOLOGY; LIVER; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY;

ADULT; BIOMARKERS; BIOPSY; DISEASE PROGRESSION; FEMALE; GLUCOSE TOLERANCE TEST; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HEPATOCYTES; HUMANS; IMMUNOGLOBULIN G; LIVER; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84941259285     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-015-1039-2     Document Type: Article

References (54)

1. Ludwig J, Viggiano TR, McGill DB, et al. Non-alcoholic steatohepatitis. Mayo Clinic experiences with a hitherto unnamed disease. Mayo Clin Proc. 1980;55:434–8.
2. Matteoni CA, Younossi ZM, Gramlich T, et al. Nonalcoholic fatty liver diseases: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413–9.
3. Rafiq N, Bai C, Fang Y, et al. Long-term follow-up of patients with nonalcoholic fatty liver. Clin Gastroenterol Hepatol. 2009;7:234–8.
4. Saibara T. Nonalcoholic steatohepatitis in Asia–Oceania. Hepatol Res. 2005;33:64–7.
5. Eguchi Y, Hyogo H, Ono M, et al. Prevalence and associated metabolic factors of nonalcoholic fatty liver disease in the general population from 2009 to 2010 in Japan: a multicenter large retrospective study. J Gastroenterol. 2012;47:586–95.
6. Marchesini G, Bugianesi E, Forlani G, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology. 2003;37:917–23.
7. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 2001;120:1183–92.
8. Oliveira CP, Costa Gayotto LC, Tatai C, et al. Oxidative stress in the pathogenesis of nonalcoholic fatty liver disease, in rats fed with a choline-deficient diet. J Cell Mol Med. 2002;6:399–406.
9. Sumida Y, Nakashima T, Yoh T, et al. Serum thioredoxin levels as a predictor of steatohepatitis in patients with nonalcoholic liver disease. J Hepatol. 2003;38:32–8.
10. Dunn BE, Cohen H, Blaser MJ. Helicobacter pylori. Clin Microbiol Rev. 1997;10:720–41.
11. Stalke P, Al-Soud WA, Bielawski KP, et al. Detection of Helicobacter species in liver and stomach tissues of patients with chronic liver diseases using polymerase chain reaction-denaturing gradient gel electrophoresis and immunohistochemistry. Scand J Gastroenterol. 2005;40:1032–41.
12. Pirouz T, Zounubi L, Keivani H, et al. Detection of Helicobacter pylori in paraffin-embedded specimens from patients with chronic liver diseases, using the amplification method. Dig Dis Sci. 2009;54:1456–9.
13. Cindoruk M, Cirak MY, Unal S, et al. Identification of Helicobacter species by 16S rDNA PCR and sequence analysis in human liver samples from patients with various etiologies of benign liver diseases. Eur J Gastroenterol Hepatol. 2008;20:33–6.
14. Huang Y, Fan XG, Wang ZM, et al. Identification of helicobacter species in human liver samples from patients with primary hepatocellular carcinoma. J Clin Pathol. 2004;57:1273–7.
15. Abenavoli L, Milic N, Masarone M, et al. Association between non-alcoholicfatty liver disease, insulin resistance and Helicobacter pylori. Med Hypotheses. 2013;81:913–5.
16. Polyzos SA, Kountouras J, Papatheodorou A, et al. Helicobacter pylori infection in patients with nonalcoholic fatty liver disease. Metabolism. 2013;62:121–6.
17. Li M, Shen Z, Li YM. Potential role of Helicobacter pylori infection in nonalcoholic fatty liver disease. World J Gastroenterol. 2013;19:7024–31.
18. Japanese Society for the Study of Obesity. New criteria of obesity (in Japanese). J Jpn Soc Study Obes. 2000;6:18–28.
19. American Diabetes Association. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 1997;20:1183–97.
20. National Cholesterol Education Program (NCEP) Expert Panel on Detection. Evaluation and treatment of high blood cholesterol in adults (Adult Treatment Panel III) executive summary of the third report. JAMA. 2001;285:2486e97.
21. Sumida Y, Yoneda M, Hyogo H, et al. A simple clinical scoring system using ferritin, fasting insulin, and type IV collagen 7S for predicting steatohepatitis in nonalcoholic fatty liver disease. J Gastroenterol. 2011;46:257–68.
22. Shah A, Lydecker A, Murray K, et al. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol. 2009;7:1104–12.
23. Sumida Y, Yoneda M, Hyogo H, et al. Validation of the FIB4 index in a Japanese nonalcoholic fatty liver disease population. BMC Gastroenterol. 2012;12:2.
24. Wai CT, Greenson JK, Fontana RJ, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38:518–26.
25. Kleiner DE, Brunt EM, Van Natta M, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005;41:1313–21.
26. Brunt EM, Janney CG, Di Bisceglie AM, et al. Non-alcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol. 1999;94:2467–74.
27. Di Bisceglie AM, Axiotis CA, Hoofnagle JH, et al. Measurements of iron status in patients with chronic hepatitis. Gastroenterology. 1992;102:2108–13.
28. Doğan Z, Filik L, Ergül B, et al. Association between Helicobacter pylori and liver-to-spleen ratio: a randomized-controlled single-blind study. Eur J Gastroenterol Hepatol. 2013;25:107–10.
29. Takuma Y. Helicobacter pylori infection and liver diseases. Gan To Kagaku Ryoho. 2011;38:362–4 (Article in Japanese).
30. Huang Y, Tian XF, Fan XG, et al. The pathological effect of Helicobacter pylori infection on liver tissues in mice. Clin Microbiol Infect. 2009;15:843–9.
31. Cindoruk M, Cirak MY, Unal S, et al. Identification of Helicobacter species by 16S rDNA PCR and sequence analysis in human liver samples from patients with various etiologies of benign liver diseases. Eur J Gastroenterol Hepatol. 2008;20:33–6.
32. Kamada Y, Akita M, Takeda Y, et al. Serum fucosylated haptoglobin as a novel diagnostic biomarker for predicting hepatocyte ballooning and nonalcoholic steatohepatitis. PLoS One. 2013;8:e66328.
33. Kamada Y, Fujii H, Fujii H, et al. Serum Mac-2 binding protein levels as a novel diagnostic biomarker for prediction of disease severity and nonalcoholic steatohepatitis. Proteomics Clin Appl. doi:10.1002/prca.201200137.
34. Gunji T, Matsuhashi N, Sato H, et al. Helicobacter pylori infection is significantly associated with metabolic syndrome in the Japanese population. Am J Gastroenterol. 2008;103:3005–10.
35. Gunji T, Matsuhashi N, Sato H, et al. Helicobacter pylori infection significantly increases insulin resistance in the asymptomatic Japanese population. Helicobacter. 2009;14:144–50.
36. Nwokolo CU, Freshwater DA, O’Hare P, et al. Plasma ghrelin following cure of Helicobacter pylori. Gut. 2003;52:637–40.
37. Wu MS, Lee WJ, Wang HH, et al. A case-control study of association of Helicobacter pylori infection with morbid obesity in Taiwan. Arch Intern Med. 2005;165:1552–5.
38. Polyzos SA, Kountouras J, Zavos C, et al. The association between Helicobacter pylori infection and insulin resistance: a systematic review. Helicobacter. 2011;16:79–88.
39. Horikawa C, Kodama S, Fujihara K, et al. Association of Helicobacter pylori infection with glycemic control in patients with diabetes: a meta-analysis. J Diabetes Res. 2014;2014:250620.
40. Ando T, Ishikawa T, Takagi T, et al. Impact of Helicobacter pylori eradication on circulating adiponectin in humans. Helicobacter. 2013;18:158–64.
41. Crabtree JE, Shallcross TM, Heatley RV, et al. Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut. 1991;32:1473–7.
42. Basso D, Plebani M, Kusters JG. Pathogenesis of Helicobacter pylori infection. Helicobacter. 2010;15(Suppl 1):14–20.
43. Suganuma M, Kuzuhara T, Yamaguchi K, et al. Carcinogenic role of tumor necrosis factor-alpha inducing protein of Helicobacter pylori in human stomach. J Biochem Mol Biol. 2006;39:1–8.
44. Miele L, Valenza V, La Torre G, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology. 2009;49:1877–87.
45. Fukuda Y, Bamba H, Okui M, et al. Helicobacter pylori infection increases mucosal permeability of the stomach and intestine. Digestion. 2001;63(Suppl 1):93–6.
46. Pellicano R, Ménard A, Rizzetto M, et al. Helicobacter species and liver diseases: association or causation? Lancet Infect Dis. 2008;8:254–60.
47. Satoh H, Saijo Y, Yoshioka E, et al. Helicobacter Pylori infection is a significant risk for modified lipid profile in Japanese male subjects. J Atheroscler Thromb. 2010;17:1041–8.
48. Kebapcilar L, Bilgir O, Cetinkaya E, et al. The effect of Helicobacter pylori eradication on macrophage migration inhibitory factor, C-reactive protein and fetuin-a levels. Clinics (Sao Paulo). 2010;65:799–802.
49. Akbas HS, Basyigit S, Suleymanlar I, et al. The assessment of carotid intima media thickness and serum paraoxonase-1 activity in Helicobacter pylori positive subjects. Lipids Health Dis. 2010;9:92.
50. Sumida Y, Yoshikawa T, Okanoue T. Role of hepatic iron in non-alcoholic steatohepatitis. Hepatol Res. 2009;39:213–22.
51. Barabino A. Helicobacter pylori-related iron deficiency anemia: a review. Helicobacter. 2002;7:71–5.
52. Sumida Y, Kanemasa K, Yamaoka Y, et al. Influence of Helicobacter pylori infection on iron accumulation in hepatitis C. Liver Int. 2006;26:827–33.
53. Salehi H, Minakari M, Yaghoutkar A, et al. The effect of Helicobacter pylori eradication on liver enzymes in patients referring with unexplained hypertransaminasemia. Adv Biomed Res. 2014;3:131.
54. Jamali R, Mofid A, Vahedi H, et al. The effect of helicobacter pylori eradication on liver fat content in subjects with non-alcoholic fatty liver disease: a randomized open-label clinical trial. Hepat Mon. 2013;13:e14679.