The predictive value of steatosis in hepatitis C virus infection

References

• Lonardo A, Adinolfi LE, Loria P, Carulli N, Ruggiero G, Day CP. Steatosis and hepatitis C virus: mechanisms and significance for hepatic and extrahepatic disease. Gastroenterology 126(2), 586–597 (2004).
   PubMed Web of Science ®Google Scholar
• Moriya K, Yotsuyanagi H, Shintani Y et al. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J. Gen. Virol. 78(Pt 7), 1527–1531 (1997).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Gambardella M, Andreana A, Tripodi MF, Utili R, Ruggiero G. Steatosis accelerates the progression of liver damage of chronic hepatitis C patients and correlates with specific HCV genotype and visceral obesity. Hepatology 33(6), 1358–1364 (2001).
   PubMed Web of Science ®Google Scholar
• Kumar D, Farrell GC, Fung C, George J. Hepatitis C virus genotype 3 is cytopathic to hepatocytes: Reversal of hepatic steatosis after sustained therapeutic response. Hepatology 36(5), 1266–1272 (2002).
   PubMed Web of Science ®Google Scholar
• Hourioux C, Patient R, Morin A et al. The genotype 3-specific hepatitis C virus core protein residue phenylalanine 164 increases steatosis in an in vitro cellular model. Gut 56(9), 1302–1308 (2007).
   PubMed Web of Science ®Google Scholar
• Perlemuter G, Sabile A, Letteron P et al. Hepatitis C virus core protein inhibits microsomal triglyceride transfer protein activity and very low density lipoprotein secretion: a model of viral-related steatosis. FASEB J. 16(2), 185–194 (2002).
   PubMed Web of Science ®Google Scholar
• Mirandola S, Realdon S, Iqbal J et al. Liver microsomal triglyceride transfer protein is involved in hepatitis C liver steatosis. Gastroenterology 130(6), 1661–1669 (2006).
   PubMed Web of Science ®Google Scholar
• Zampino R, Ingrosso D, Durante-Mangoni E et al. Microsomal triglyceride transfer protein (MTP)-493G/T gene polymorphism contributes to fat liver accumulation in HCV genotype 3 infected patients. J. Viral Hepat. 15(10), 740–746 (2008).
   PubMed Web of Science ®Google Scholar
• Mirandola S, Osterreicher CH, Marcolongo M et al. Microsomal triglyceride transfer protein polymorphism (-493G/T) is associated with hepatic steatosis in patients with chronic hepatitis C. Liver Int. 29(4), 557–565 (2009).
   PubMed Web of Science ®Google Scholar
• Lonardo A, Loria P, Adinolfi LE, Carulli N, Ruggiero G. Hepatitis C and steatosis: a reappraisal. J. Viral Hepat. 13(2), 73–80 (2006).
   PubMed Web of Science ®Google Scholar
• Rubbia-Brandt L, Quadri R, Abid K et al. Hepatocyte steatosis is a cytopathic effect of hepatitis C virus genotype 3. J. Hepatol. 33(1), 106–115 (2000).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE. Hepatitis C and fatty liver. In: Hot Topics in Viral Hepatitis, Hepatitis C and Metabolism. Negro F (Ed.). FB Communication, Modena, Italy, 21–29 (2008).
   Google Scholar
• Durante-Mangoni E, Zampino R, Marrone A et al. Hepatic steatosis and insulin resistance are associated with serum imbalance of adiponectin/tumour necrosis factor-α in chronic hepatitis C patients. Aliment. Pharmacol. Ther. 24(9), 1349–1357 (2006).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Ingrosso D, Cesaro G et al. Hyperhomocysteinemia and the MTHFR C677T polymorphism promote steatosis and fibrosis in chronic hepatitis C patients. Hepatology 41(5), 995–1003 (2005).
   PubMed Web of Science ®Google Scholar
• Valenti L, Rumi M, Galmozzi E et al. Patatin-like phospholipase domain-containing 3 I148M polymorphism, steatosis, and liver damage in chronic hepatitis C. Hepatology 53(3), 791–799 (2011).
   PubMed Web of Science ®Google Scholar
• Zampino R, Coppola N, Cirillo G et al. Abdominal fat interacts with PNPLA3 I148M, but not with the APOC3 variant in the pathogenesis of liver steatosis in chronic hepatitis C. J. Viral Hep. doi:10.1111/jvh.12053 (2013) (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Utili R, Attanasio V et al. Epidemiology, clinical spectrum and prognostic value of mixed cryoglobulinaemia in hepatitis C virus patients: a prospective study. Ital. J. Gastroenterol. 28(1), 1–9 (1996).
   PubMedGoogle Scholar
• Khattab MA, Eslam M, Alavian SM. Hepatitis C virus as a multifaceted disease: a simple and updated approach for extrahepatic manifestations of hepatitis C virus infection. Hepat. Mon. 10(4), 258–269 (2010).
   PubMed Web of Science ®Google Scholar
• Durante-Mangoni E, Iardino P, Resse M et al. Silent celiac disease in chronic hepatitis C: impact of interferon treatment on the disease onset and clinical outcome. J. Clin. Gastroenterol. 38(10), 901–905 (2004).
   PubMed Web of Science ®Google Scholar
• André P, Komurian-Pradel F, Deforges S et al. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 76(14), 6919–6928 (2002).
   PubMed Web of Science ®Google Scholar
• Serfaty L, Poujol-Robert A, Carbonell N, Chazouillères O, Poupon RE, Poupon R. Effect of the interaction between steatosis and alcohol intake on liver fibrosis progression in chronic hepatitis C. Am. J. Gastroenterol. 97(7), 1807–1812 (2002).
   PubMed Web of Science ®Google Scholar
• Choi J. Oxidative stress, endogenous antioxidants, alcohol, and hepatitis C: pathogenic interactions and therapeutic considerations. Free Radic. Biol. Med. 52(7), 1135–1150 (2012).
   PubMed Web of Science ®Google Scholar
• Sevastianos VA, Hadziyannis SJ. Nonalcoholic fatty liver disease: from clinical recognition to treatment. Expert Rev. Gastroenterol. Hepatol. 2(1), 59–79 (2008).
   PubMedGoogle Scholar
• Hourigan LF, Macdonald GA, Purdie D et al. Fibrosis in chronic hepatitis C correlates significantly with body mass index and steatosis. Hepatology 29(4), 1215–1219 (1999).
   PubMed Web of Science ®Google Scholar
• Fartoux L, Chazouillères O, Wendum D, Poupon R, Serfaty L. Impact of steatosis on progression of fibrosis in patients with mild hepatitis C. Hepatology 41(1), 82–87 (2005).
   PubMed Web of Science ®Google Scholar
• Rubbia-Brandt L, Fabris P, Paganin S et al. Steatosis affects chronic hepatitis C progression in a genotype specific way. Gut 53, 406–412 (2004).
   PubMed Web of Science ®Google Scholar
• Castéra L, Hézode C, Roudot-Thoraval F et al. Effect of antiviral treatment on evolution of liver steatosis in patients with chronic hepatitis C: indirect evidence of a role of hepatitis C virus genotype 3 in steatosis. Gut 53(3), 420–424 (2004).
   PubMed Web of Science ®Google Scholar
• Castéra L, Hézode C, Roudot-Thoraval F et al. Worsening of steatosis is an independent factor of fibrosis progression in untreated patients with chronic hepatitis C and paired liver biopsies. Gut 52(2), 288–292 (2003).
   PubMed Web of Science ®Google Scholar
• Cross TJ, Quaglia A, Hughes S, Joshi D, Harrison PM. The impact of hepatic steatosis on the natural history of chronic hepatitis C infection. J. Viral Hepat. 16(7), 492–499 (2009).
   PubMed Web of Science ®Google Scholar
• Hickman IJ, Jonsson JR, Prins JB et al. Modest weight loss and physical activity in overweight patients with chronic liver disease results in sustained improvements in alanine aminotransferase, fasting insulin, and quality of life. Gut 53(3), 413–419 (2004).
   PubMed Web of Science ®Google Scholar
• Restivo L, Guerrera B, Ciervo A et al. Factors and mechanisms involved in the progression of hepatic fibrosis in chronic HCV infection: which role for steatosis and insulin resistance? Intern. Emerg. Med. 7(Suppl. 4), S463–S464 (2012).
   PubMed Web of Science ®Google Scholar
• Leandro G, Mangia A, Hui J et al.; HCV Meta-Analysis (on) Individual Patients’ Data Study Group. Relationship between steatosis, inflammation, and fibrosis in chronic hepatitis C: a meta-analysis of individual patient data. Gastroenterology 130(6), 1636–1642 (2006).
   PubMed Web of Science ®Google Scholar
• Vidali M, Tripodi MF, Ivaldi A et al. Interplay between oxidative stress and hepatic steatosis in the progression of chronic hepatitis C. J. Hepatol. 48(3), 399–406 (2008).
   PubMed Web of Science ®Google Scholar
• Del Campo JA, Romero-Gómez M. Steatosis and insulin resistance in hepatitis C: a way out for the virus? World J. Gastroenterol. 15(40), 5014–5019 (2009).
   PubMed Web of Science ®Google Scholar
• Seidel N, Volkmann X, Länger F et al. The extent of liver steatosis in chronic hepatitis C virus infection is mirrored by caspase activity in serum. Hepatology 42, 113–120 (2005).
   PubMed Web of Science ®Google Scholar
• Moriya K, Fujie H, Shintani Y et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat. Med. 4(9), 1065–1067 (1998).
   PubMed Web of Science ®Google Scholar
• Ohata K, Hamasaki K, Toriyama K et al. Hepatic steatosis is a risk factor for hepatocellular carcinoma in patients with chronic hepatitis C virus infection. Cancer 97(12), 3036–3043 (2003).
   PubMed Web of Science ®Google Scholar
• Pekow JR, Bhan AK, Zheng H, Chung RT. Hepatic steatosis is associated with increased frequency of hepatocellular carcinoma in patients with hepatitis C-related cirrhosis. Cancer 109(12), 2490–2496 (2007).
   PubMed Web of Science ®Google Scholar
• Nkontchou G, Ziol M, Aout M et al. HCV genotype 3 is associated with a higher hepatocellular carcinoma incidence in patients with ongoing viral C cirrhosis. J. Viral Hepat. 18(10), e516–e522 (2011).
   PubMed Web of Science ®Google Scholar
• Tazawa J, Maeda M, Nakagawa M et al. Diabetes mellitus may be associated with hepatocarcinogenesis in patients with chronic hepatitis C. Dig. Dis. Sci. 47(4), 710–715 (2002).
   PubMed Web of Science ®Google Scholar
• Larsson SC, Wolk A. Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies. Br. J. Cancer 97(7), 1005–1008 (2007).
   PubMed Web of Science ®Google Scholar
• Chen CL, Yang HI, Yang WS et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan. Gastroenterology 135(1), 111–121 (2008).
   PubMed Web of Science ®Google Scholar
• Kumar D, Farrell GC, Kench J, George J. Hepatic steatosis and the risk of hepatocellular carcinoma in chronic hepatitis C. J. Gastroenterol. Hepatol. 20(9), 1395–1400 (2005).
   PubMed Web of Science ®Google Scholar
• Jahan S, Ashfaq UA, Qasim M, Khaliq S, Saleem MJ, Afzal N. Hepatitis C virus to hepatocellular carcinoma. Infect. Agents Cancer 7(1), 2 (2012).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Restivo L, Zampino R, Lonardo A, Loria P. Metabolic alterations and chronic hepatitis C: treatment strategies. Expert Opin. Pharmacother. 12(14), 2215–2234 (2011).
   PubMed Web of Science ®Google Scholar
• Hui JM, Sud A, Farrell GC et al. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression [corrected]. Gastroenterology 125(6), 1695–1704 (2003).
   PubMed Web of Science ®Google Scholar
• Moucari R, Asselah T, Cazals-Hatem D et al. Insulin resistance in chronic hepatitis C: association with genotypes 1 and 4, serum HCV RNA level, and liver fibrosis. Gastroenterology 134(2), 416–423 (2008).
   PubMed Web of Science ®Google Scholar
• Tsochatzis E, Manolakopoulos S, Papatheodoridis GV et al. Serum HCV RNA levels and HCV genotype do not affect insulin resistance in nondiabetic patients with chronic hepatitis C: a multicentre study. Aliment. Pharmacol. Ther. 30(9), 947–954 (2009).
   PubMed Web of Science ®Google Scholar
• Lonardo A, Adinolfi LE, Petta S, Craxì A, Loria P. Hepatitis C and diabetes: the inevitable coincidence? Expert Rev. Anti. Infect. Ther. 7(3), 293–308 (2009).
   PubMed Web of Science ®Google Scholar
• Petta S, Cammà C, Di Marco V et al. Insulin resistance and diabetes increase fibrosis in the liver of patients with genotype 1 HCV infection. Am. J. Gastroenterol. 103(5), 1136–1144 (2008).
   PubMed Web of Science ®Google Scholar
• Kwon SY, Kim SS, Kwon OS et al. Prognostic significance of glycaemic control in patients with HBV and HCV-related cirrhosis and diabetes mellitus. Diabet. Med. 22(11), 1530–1535 (2005).
   PubMed Web of Science ®Google Scholar
• Lonardo A, Ballestri S, Adinolfi LE et al. Hepatitis C virus-infected patients are ‘spared’ from the metabolic syndrome but not from insulin resistance. A comparative study of nonalcoholic fatty liver disease and hepatitis C virus-related steatosis. Can. J. Gastroenterol. 23(4), 273–278 (2009).
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Restivo L, Zampino R et al. Chronic HCV infection is a risk of atherosclerosis. Role of HCV and HCV-related steatosis. Atherosclerosis 221(2), 496–502 (2012).
   PubMed Web of Science ®Google Scholar
• Ishizaka N, Ishizaka Y, Takahashi E et al. Association between hepatitis C virus seropositivity, carotid-artery plaque, and intima-media thickening. Lancet 359(9301), 133–135 (2002).
   PubMed Web of Science ®Google Scholar
• Lonardo A, Ballestri S, Restivo L et al. Hepatitis C and cardiovascular risk: facts and controversies. In: Hot Topics in Viral Hepatitis, Hepatitis C and Metabolism (3rd Edition). Negro F (Ed.). FB Communication, Modena, Italy, 27–33 (2012).
   Google Scholar
• Boddi M, Abbate R, Chellini B et al. Hepatitis C virus RNA localization in human carotid plaques. J. Clin. Virol. 47, 72–75 (2010).
   PubMed Web of Science ®Google Scholar
• Petta S, Torres D, Fazio G et al. Carotid atherosclerosis and chronic hepatitis C: a prospective study of risk associations. Hepatology 55(5), 1317–1323 (2012).
   PubMed Web of Science ®Google Scholar
• Liao CC, Su TC, Sung FC, Chou WH, Chen TL. Does hepatitis C virus infection increase risk for stroke? A population-based cohort study. PLoS ONE 7(2), e31527 (2012).
   PubMed Web of Science ®Google Scholar
• Poynard T, Ratziu V, McHutchison J et al. Effect of treatment with peginterferon or interferon α-2b and ribavirin on steatosis in patients infected with hepatitis C. Hepatology 38(1), 75–85 (2003).
   PubMed Web of Science ®Google Scholar
• Patton HM, Patel K, Behling C et al. The impact of steatosis on disease progression and early and sustained treatment response in chronic hepatitis C patients. J. Hepatol. 40(3), 484–490 (2004).
   PubMed Web of Science ®Google Scholar
• Westin J, Lagging M, Dhillon AP et al.; DITTO-HCV Study Group. Impact of hepatic steatosis on viral kinetics and treatment outcome during antiviral treatment of chronic HCV infection. J. Viral Hepat. 14(1), 29–35 (2007).
   PubMed Web of Science ®Google Scholar
• Tarantino G, Conca P, Ariello M, Mastrolia M. Does a lower insulin resistance affect antiviral therapy response in patients suffering from HCV related chronic hepatitis? Gut 55(4), 585 (2006).
   PubMed Web of Science ®Google Scholar
• Shah SR, Patel K, Marcellin P et al. Steatosis is an independent predictor of relapse following rapid virologic response in patients with HCV genotype 3. Clin. Gastroenterol. Hepatol. 9(8), 688–693 (2011).
   PubMed Web of Science ®Google Scholar
• Restivo L, Zampino R, Guerrera B, Ruggiero L, Adinolfi LE. Steatosis is the predictor of relapse in HCV genotype 3- but not 2-infected patients treated with 12 weeks of pegylated interferon-α-2a plus ribavirin and RVR. J. Viral Hepat. 19(5), 346–352 (2012).
   PubMed Web of Science ®Google Scholar
• Shiffman ML, Suter F, Bacon BR et al.; ACCELERATE Investigators. Peginterferon α-2a and ribavirin for 16 or 24 weeks in HCV genotype 2 or 3. N. Engl. J. Med. 357(2), 124–134 (2007).
   PubMed Web of Science ®Google Scholar
• Gundez F, Adoulnasr FM, Chandra PK et al. Free fatty acids induce ER stress and block antiviral activity of interferon α against hepatitis C virus in cell culture. Virol. J. 9, 143 (2012).
   PubMed Web of Science ®Google Scholar
• Walch MJ, Johnson JR, Richardson MM et al. Non-response to antiviral therapy is associated with obesity and increased hepatic expression of suppressor of cytokine signaling 3 (SOCS-3) in patients with chronic hepatitis C, viral genotype 1. Gut 55, 529–535 (2006).
   PubMed Web of Science ®Google Scholar