Impact of hepatitis C virus therapy on metabolism and public health

Liver International

Volumn 37, Issue , 2017, Pages 13-18

  Shiffman, Mitchell L ^a   Gunn, Nadege T ^a  

^a Bon Secours Health System   (United States)

Author keywords

hepatitis C virus; insulin resistance; metabolic syndrome; type 2 diabetes mellitus

Indexed keywords

CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; CHRONIC HEPATITIS C; CHRONIC KIDNEY FAILURE; DISEASE COURSE; END STAGE RENAL DISEASE; FATTY LIVER; HEPATITIS C VIRUS; HUMAN; INSULIN RESISTANCE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PUBLIC HEALTH; REVIEW; RISK FACTOR; VIRAL CLEARANCE; COMPLICATION; DISEASE EXACERBATION; HEPACIVIRUS;

ANTIVIRUS AGENT;

ANTIVIRAL AGENTS; CEREBROVASCULAR DISORDERS; DIABETES MELLITUS, TYPE 2; DISEASE PROGRESSION; FATTY LIVER; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INSULIN RESISTANCE; KIDNEY FAILURE, CHRONIC; LIVER CIRRHOSIS; METABOLIC SYNDROME; PUBLIC HEALTH; RISK FACTORS;

EID: 85007578571     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.13282     Document Type: Review

References (77)

1. Denniston MM, Jiles RB, Drobeniuc J, et al. Chronic hepatitis C virus infection in the United States, National Health and Nutrition Examination survey 2003 to 2010. Ann Intern Med. 2014;160:293–300.
2. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis. 2005;5:558–567.
3. Frank C, Mohamed MK, Strickland GT, Lavanchy D, Arthur RR, Magder LS. The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet. 2000;355:887–891.
4. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. Lancet. 1997;349:825–832.
5. Harris DR, Gonin R, Alter HJ, et al. The relationship of acute transfusion-associated hepatitis to the development of cirrhosis in the presence of alcohol abuse. Ann Intern Med. 2001;134:120–124.
6. Westin J, Lagging LM, Spak F, et al. Moderate alcohol intake increases fibrosis progression in untreated patients with hepatitis C virus infection. J Viral Hepat. 2002;9:235–241.
7. Ortiz V, Berenguer M, Rayon JM, Carrasco D, Berenguer J. Contribution of obesity to hepatitis C-related fibrosis progression. Am J Gastroenterol. 2002;97:2408–2414.
8. Thein HH, Yi Q, Dore GJ, Krahn MD. Natural history of hepatitis C virus infection in HIV-infected individuals and the impact of HIV in the era of highly active antiretroviral therapy: a meta-analysis. AIDS. 2008;22:1979–1991.
9. Zarski JP, Bohn B, Bastie A, et al. Characteristics of patients with dual infection by hepatitis B and C viruses. J Hepatol. 1998;28:27–33.
10. El-Serg HB. Epidemiology of hepatocellular carcinoma. Clin Liver Dis. 2001;5:87–106.
11. McGlynn KA, Petrick JL, London WT. Global epidemiology of hepatocellular carcinoma: an emphasis on demographic and regional variability. Clin Liver Dis. 2015 May;19:223–238.
12. Zignego AL, Craxì A. Extrahepatic manifestations of hepatitis C virus infection. Clin Liver Dis. 2008;12:611–636.
13. Sansonno D, Dammacco F. Hepatitis C virus, cryoglobulinaemia, and vasculitis: immune complex relations. Lancet Infect Dis. 2005;5:227–236.
14. Terrier B, Cacoub P. Cryoglobulinemia vasculitis: an update. Curr Opin Rheumatol. 2013;25:10–18.
15. Fabrizi F, Plaisier E, Saadoun D, Martin P, Messa P, Cacoub P. Hepatitis C virus infection, mixed cryoglobulinemia, and kidney disease. Am J Kidney Dis. 2013;61:623–637.
16. Tsui JI, Vittinghoff E, Shlipak MG, O'Hare AM. Relationship between hepatitis C and chronic kidney disease: results from the Third National Health and Nutrition Examination Survey. J Am Soc Nephrol. 2006;17:1168–1174.
17. Fiorino S, Bacchi-Reggiani L, de Biase D, et al. Possible association between hepatitis C virus and malignancies different from hepatocellular carcinoma: a systematic review. World J Gastroenterol. 2015;21:12896–12953.
18. Younossi Z, Park H, Henry L, Adeyemi A, Stepanova M. Extrahepatic manifestations of hepatitis C: a meta-analysis of prevalence, quality of life, and economic burden. Gastroenterology. 2016;150:1599–15608.
19. Stepanova M, Lam B, Younossi Y, Srishord MK, Younossi ZM. Association of hepatitis C with insulin resistance and type 2 diabetes in US general population: the impact of the epidemic of obesity. J Viral Hepat. 2012;19:341–345.
20. Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med. 2000;133:592–599.
21. Wang CS, Wang ST, Yao WJ, Chang TT, Chou P. Hepatitis C virus infection and the development of type 2 diabetes in a community-based longitudinal study. Am J Epidemiol. 2007;166:196–203.
22. Mehta SH, Brancati FL, Strathdee SA, et al. Hepatitis C virus infection and incident type 2 diabetes. Hepatology. 2003;38:50–56.
23. Hwang JC, Jiang MY, Lu YH, Weng SF. Impact of HCV infection in diabetes patients for the risk of end-stage renal failure. Medicine (Baltimore). 2016;95:e2431.
24. Arase Y, Suzuki F, Suzuki Y, et al. Sustained virological response reduces incidence of onset of type 2 diabetes in chronic hepatitis C. Hepatology. 2009;49:739–744.
25. Chen YC, Hwang SJ, Li CY, Wu CP, Lin LC. A Taiwanese nationwide cohort study shows interferon-based therapy for chronic hepatitis C reduces the risk of chronic kidney disease. Medicine (Baltimore). 2015;94:e1334.
26. Aytug S, Reich D, Sapiro LE, Bernstein D, Begum N. Impaired IRS-1/PI3-kinase signaling in patients with HCV: a mechanism for increased prevalence of type 2 diabetes. Hepatology. 2003;38:1384–1392.
27. Sheikh MY, Choi J, Qadri I, Friedman JE, Sanyal AJ. Hepatitis C virus infection: molecular pathways to metabolic syndrome. Hepatology. 2008;47:2127–2133.
28. Vanni E, Abate ML, Gentilcore E, et al. Sites and mechanisms of insulin resistance in nonobese, nondiabetic patients with chronic hepatitis C. Hepatology. 2009;50:697–706.
29. Bugianesi E, McCullough AJ, Marchesini G. Insulin resistance: a metabolic pathway to chronic liver disease. Hepatology. 2005;42:987–1000.
30. Ferrannini E, Natali A, Capaldo B, Lehtovirta M, Jacob S, Yki-Järvinen H. Insulin resistance, hyperinsulinemia, and blood pressure: role of age and obesity. European Group for the Study of Insulin Resistance (EGIR). Hypertension. 1997;30:1144–1149.
31. Harrison SA. Insulin resistance among patients with chronic hepatitis C: etiology and impact on treatment. Clin Gastroenterol Hepatol. 2008;6:864–876.
32. 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. 2008;134:416–423.
33. Negro F, Alaei M. Hepatitis C virus and type 2 diabetes. World J Gastroenterol. 2009;15:1537–1547.
34. 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. 2004;126:586–597.
35. Leandro G, Mangia A, Hui J, et al. The relationship between hepatic steatosis, inflammation and fibrosis in chronic hepatitis C: a meta-analysis of individual patient data. Gastroenterology. 2006;130:1636–1642.
36. Bochud PY, Cai T, Overbeck K, et al. Genotype 3 is associated with accelerated fibrosis progression in chronic hepatitis C. J Hepatol. 2009;51:655–666.
37. Kumar D, Farrell GC, Fung C, George J. Hepatitis C virus genotype 3 is cytopathic to epatocytes. Genotype-specific reversal of hepatic steatosis after sustained response to antiviral therapy. Hepatology. 2002;36:1266–1272.
38. Poynard T, Ratziu V, McHutchison J, et al. Effect of treatment with peginterferon or interferon alfa-2b and ribavirin on steatosis in patients infected with hepatitis C. Hepatology. 2003;38:75–85.
39. 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. 2001;33:1358–1364.
40. Fartoux L, Chazouillères O, Wendum D, Poupon R, Serfaty L. Impact of steatosis on progression of fibrosis in patients with mild hepatitis C. Hepatology. 2005;41:82–87.
41. 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. 2003;97:3036–3043.
42. 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. 2007;109:2490–2496.
43. Kurosaki M, Hosokawa T, Matsunaga K, et al. Hepatic steatosis in chronic hepatitis C is a significant risk factor for developing hepatocellular carcinoma independent of age, sex, obesity, fibrosis stage, and response to interferon therapy. Hepatol Res. 2010;40:870–877.
44. Hui JM, Sud A, Farrell GC, et al. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression. Gastroenterology. 2003;125:1695–1704.
45. Paradis V, Perlemuter G, Bonvoust F, et al. High glucose and hyperinsulinemia stimulate connective tissue growth factor expression: a potential mechanism involved in progression to fibrosis in nonalcoholic steatohepatitis. Hepatology. 2001;34:738–744.
46. Arase Y, Kobayashi M, Suzuki F, et al. Effect of type 2 diabetes on risk for malignancies includes hepatocellular carcinoma in chronic hepatitis C. Hepatology. 2013;57:964–973.
47. Dai CY, Huang JF, Hsieh MY, et al. Insulin resistance predicts response to peginterferon-alpha/ribavirin combination therapy in chronic hepatitis C patients. J Hepatol. 2009;50:712–718.
48. Yilmaz Y, Younossi ZM. Obesity-associated nonalcoholic fatty liver disease. Clin Liver Dis. 2014;18:19–31.
49. Asselah T, Rubbia-Brandt L, Marcellin P, Negro F. Steatosis in chronic hepatitis C: why does it really matter? Gut. 2006;55:123–130.
50. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413–1419.
51. Blonsky J, Harrison SA. Review article: nonalcoholic fatty liver disease and hepatitis C virus—partners in crime. Aliment Pharmacol Ther. 2008;27:855–865.
52. Sanyal AJ, Contos MJ, Sterling RK, et al. Nonalcoholic fatty liver disease in patients with hepatitis C is associated with features of the metabolic syndrome. Am J Gastroenterol. 2003;98:2064–2071.
53. Poynard T, Imbert-Bismut F, Ratziu V, et al. Biochemical markers of liver fibrosis in patients infected by hepatitis C virus: longitudinal validation in a randomized trial. J Viral Hepat. 2002;9:128–133.
54. Friedrich-Rust M, Ong MF, Martens S, et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology. 2008;34:960–974.
55. Chen J, Talwalkar JA, Yin M, Glaser KJ, Sanderson SO, Ehman RL. Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology. 2011;259:749–756.
56. Ishizaka N, Ishizaka Y, Takahashi E, et al. Association between hepatitis C virus seropositivity, carotid-artery plaque, and intima-media thickening. Lancet. 2002;359:133–135.
57. Ishizaka Y, Ishizaka N, Takahashi E, et al. Association between hepatitis C virus core protein and carotid atherosclerosis. Circ J. 2003;67:26–30.
58. Tomiyama H, Arai T, Hirose K, et al. Hepatitis C virus seropositivity, but not hepatitis B virus carrier or seropositivity, associated with increased pulse wave velocity. Atherosclerosis. 2003;166:401–403.
59. Targher G, Bertolini L, Padovani R, Rodella S, Arcaro G, Day C. Differences and similarities in early atherosclerosis between patients with nonalcoholic steatohepatitis and chronic hepatitis B and C. J Hepatol. 2007;46:1126–1132.
60. Butt AA, Xiaoqiang W, Budoff M, Leaf D, Kuller LH, Justice AC. Hepatitis C virus infection and the risk of coronary disease. Clin Infect Dis. 2009;49:225–232.
61. Younossi ZM, Stepanova M, Nader F, Younossi Z, Elsheikh E. Associations of chronic hepatitis C with metabolic and cardiac outcomes. Aliment Pharmacol Ther. 2013;37:647–652.
62. Guiltinan AM, Kaidarova Z, Custer B, et al. Increased all-cause, liver, and cardiac mortality among hepatitis C virusseropositive blood donors. Am J Epidemiol. 2008;167:743–750.
63. Lee MH, Yang HI, Lu SN, et al. Chronic hepatitis C virus infection increases mortality from hepatic and extrahepatic diseases: a community-based long-term prospective study. J Infect Dis. 2012;206:469–477.
64. Lee MH, Yang HI, Wang CH, et al. Hepatitis C virus infection and increased risk of cerebrovascular disease. Stroke. 2010;41:2894–2900.
65. Maruyama S, Koda M, Oyake N, et al. Myocardial injury in patients with chronic hepatitis C infection. J Hepatol. 2013;58:11–15.
66. Roed T, Kristoffersen US, Knudsen A, et al. Increased prevalence of coronary artery disease risk markers in patients with chronic hepatitis C—a cross-sectional study. Vasc Health Risk Manag. 2014;10:55–62.
67. Romero-Gómez M, Fernández-Rodríguez CM, Andrade RJ, et al. Effect of sustained virological response to treatment on the incidence of abnormal glucose values in chronic hepatitis C. J Hepatol. 2008;48:721–727.
68. Aghemo A, Prati GM, Rumi MG, et al. Sustained virological response prevents the development of insulin resistance in patients with chronic hepatitis C. Hepatology. 2012;56:1681–1687.
69. Kawaguchi T, Ide T, Taniguchi E, et al. Clearance of HCV improves insulin resistance, beta-cell function, and hepatic expression of insulin receptor substrate 1 and 2. Am J Gastroenterol. 2007;102:570–576.
70. 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. 2004;40:484–490.
71. 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. 2004;53:420–424.
72. Hézode C, Roudot-Thoraval F, Zafrani ES, Dhumeaux D, Pawlotsky JM. Different mechanisms of steatosis in hepatitis C virus genotypes 1 and 3 infections. J Viral Hepat. 2004;11:455–458.
73. Hsu YC, Lin JT, Ho HJ, et al. Antiviral treatment for hepatitis C virus infection is associated with improved renal and cardiovascular outcomes in diabetic patients. Hepatology. 2014;59:1293–1302.
74. Feng B, Eknoyan G, Guo ZS, et al. Effect of interferon-alpha-based antiviral therapy on hepatitis C virus-associated glomerulonephritis: a meta-analysis. Nephrol Dial Transplant. 2012;27:640–646.
75. Hsu CS, Kao JH, Chao YC, et al. Interferon-based therapy reduces risk of stroke in chronic hepatitis C patients: a population based cohort study in Taiwan. Aliment Pharmacol Ther. 2013;38:415–423.
76. Jemal A, Ward E, Hao Y, Thun M. Trends in the leading causes of death in the United States, 1970-2002. JAMA. 2005;294:1255–1259.
77. Shiffman ML. Universal screening for chronic hepatitis C virus. Liver Int. 2016;36(Suppl 1):62–66.