The oncologic burden of hepatitis C virus infection: A clinical perspective

CA Cancer Journal for Clinicians

Volumn 67, Issue 5, 2017, Pages 411-431

  Torres, Harrys A ^a   Shigle, Terri Lynn ^a   Hammoudi, Nassim ^b   Link, James T ^a   Samaniego, Felipe ^a   Kaseb, Ahmed ^a   Mallet, Vincent ^b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Cochin Port Royal Hospital ^*  (France)

Author keywords

cancer; direct acting antiviral; hepatitis C virus (HCV); hepatocellular carcinoma; non Hodgkin lymphoma; primary liver cancer

Indexed keywords

ANTINEOPLASTIC AGENT; ANTIVIRUS AGENT; CAPECITABINE; CARBOPLATIN; CHLORAMBUCIL; CISPLATIN; CYCLOPHOSPHAMIDE; DACLATASVIR; DASABUVIR PLUS OMBITASVIR PLUS PARITAPREVIR PLUS RITONAVIR; DOCETAXEL; DOXORUBICIN; ELBASVIR PLUS GRAZOPREVIR; ETOPOSIDE; FLUDARABINE; GEMCITABINE; IDARUBICIN; IRINOTECAN; LEDIPASVIR PLUS SOFOSBUVIR; MERCAPTOPURINE; METHOTREXATE; PACLITAXEL; RIBAVIRIN; RITUXIMAB; SIMEPREVIR; SOFOSBUVIR; SOFOSBUVIR PLUS VELPATASVIR; UNINDEXED DRUG; VINBLASTINE; VINCRISTINE; VINORELBINE TARTRATE;

ANTIVIRAL THERAPY; ARTICLE; BILE DUCT CARCINOMA; CANCER PATIENT; CHRONIC HEPATITIS C; DISEASE ASSOCIATION; DRUG CLEARANCE; DRUG COMPETITION; DRUG METABOLISM; EPIDEMIC; HEMATOLOGIC MALIGNANCY; HEPATITIS; HEPATITIS C; HIGH RISK POPULATION; HUMAN; INFECTION RISK; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; PATIENT SELECTION; PRACTICE GUIDELINE; PREVALENCE; PRIORITY JOURNAL; SCREENING; SOLID MALIGNANT NEOPLASM; VIRUS CARCINOGENESIS; VIRUS TRANSMISSION; COMPLICATION; HEPATITIS C, CHRONIC; LIVER NEOPLASMS; VIROLOGY;

ANTIVIRAL AGENTS; HEPATITIS C, CHRONIC; HUMANS; LIVER NEOPLASMS;

EID: 85021820287     PISSN: 00079235     EISSN: 15424863     Source Type: Journal    
DOI: 10.3322/caac.21403     Document Type: Article

References (189)

1. Webster DP, Klenerman P, Dusheiko GM. Hepatitis C. Lancet. 2015;385:1124-1135.
2. Allison RD, Tong X, Moorman AC, et al. Increased incidence of cancer and cancer-related mortality among persons with chronic hepatitis C infection, 2006-2010. J Hepatol. 2015;63:822-828.
3. Mahale P, Torres HA, Kramer JR, et al. Hepatitis C virus infection and the risk of cancer among elderly US adults: a registry-based case-control study. Cancer. 2017;123:1202-1211.
4. Plummer M, de Martel C, Vignat J, Ferlay J, Bray F, Franceschi S. Global burden of cancers attributable to infections in 2012: a synthetic analysis. Lancet Glob Health. 2016;4:e609-e616.
5. Mahale P, Kontoyiannis DP, Chemaly RF, et al. Acute exacerbation and reactivation of chronic hepatitis C virus infection in cancer patients. J Hepatol. 2012;57:1177-1185.
6. Torres HA, Mahale P, Blechacz B, et al. Effect of hepatitis C virus infection in patients with cancer: addressing a neglected population. J Natl Compr Canc Netw. 2015;13:41-50.
7. Torres HA, Chong PP, De Lima M, et al. Hepatitis C virus infection among hematopoietic cell transplant donors and recipients: American Society for Blood and Marrow Transplantation Task Force recommendations. Biol Blood Marrow Transplant. 2015;21:1870-1882.
8. Mahale P, Kaseb AO, Hassan MM, Torres HA. Hepatocellular carcinoma as a second primary cancer in patients with chronic hepatitis C virus infection. Dig Liver Dis. 2015;47:348-349.
9. Mallet V, van Bommel F, Doerig C, et al. Management of viral hepatitis in patients with haematological malignancy and in patients undergoing haemopoietic stem cell transplantation: recommendations of the 5th European Conference on Infections in Leukaemia (ECIL-5). Lancet Infect Dis. 2016;16:606-617.
10. Economides MP, Mahale P, Turturro F, et al. Development of non-Hodgkin lymphoma as a second primary cancer in hepatitis C virus-infected patients with a different primary malignancy. Leuk Lymphoma. 2016;58:485-488.
11. Torres HA, Economides MP, Kyvernitakis A, et al. Sofosbuvir-based therapy in patients with chronic hepatitis C virus infection and malignancies—a prospective observational study of 143 patients. The 53rd Annual Meeting of American Society of Clinical Oncology (ASCO), June 2–6, 2017. Chicago, IL. Abstract e18152
12. Peffault de Latour R, Levy V, Asselah T, et al. Long-term outcome of hepatitis C infection after bone marrow transplantation. Blood. 2004;103:1618-1624.
13. Kyvernitakis A, Mahale P, Popat UR, et al. Hepatitis C virus infection in patients undergoing hematopoietic cell transplantation in the era of direct-acting antiviral agents. Biol Blood Marrow Transplant. 2016;22:717-722.
14. Torres HA, Roach LR, Mahale P, et al. Transdisciplinary approach to managing hepatitis C virus infection in patients at a tertiary care cancer center. J Natl Compr Canc Netw. 2016;14:1185-1188.
15. American Association for the Study of Liver Diseases/Infectious Diseases Society of American (AASLD/IDSA) HCV Guidance Panel. Recommendations for testing, managing, and treating hepatitis C, 2017. hcvguidelines.org. Accessed March 29, 2017.
16. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ. 2008;336:924-926.
17. Degenhardt L, Charlson F, Stanaway J, et al. Estimating the burden of disease attributable to injecting drug use as a risk factor for HIV, hepatitis C, and hepatitis B: findings from the Global Burden of Disease Study 2013. Lancet Infect Dis. 2016;16:1385-1398.
18. Zibbell JE, Iqbal K, Patel RC, et al. Increases in hepatitis C virus infection related to injection drug use among persons aged ≤30 years—Kentucky, Tennessee, Virginia, and West Virginia, 2006-2012. MMWR Morb Mortal Wkly Rep. 2015;64:453-458.
19. Gower E, Estes C, Blach S, Razavi-Shearer K, Razavi H. Global epidemiology and genotype distribution of the hepatitis C virus infection. J Hepatol. 2014;61(suppl 1):S45-S57.
20. Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology. 2013;57:1333-1342.
21. Sievert W, Altraif I, Razavi HA, et al. A systematic review of hepatitis C virus epidemiology in Asia, Australia and Egypt Liver Int. 2011;31(suppl 2):61-80.
22. Stanaway JD, Flaxman AD, Naghavi M, et al. The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013. Lancet. 2016;388:1081-1088.
23. Edlin BR, Eckhardt BJ, Shu MA, Holmberg SD, Swan T. Toward a more accurate estimate of the prevalence of hepatitis C in the United States. Hepatology. 2015;62:1353-1363.
24. Denniston MM, Klevens RM, McQuillan GM, Jiles RB. Awareness of infection, knowledge of hepatitis C, and medical follow-up among individuals testing positive for hepatitis C: National Health and Nutrition Examination Survey 2001-2008. Hepatology. 2012;55:1652-1661.
25. Smith BD, Morgan RL, Beckett GA, et al. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945-1965. MMWR Recomm Rep 61(RR-4):1-32, 2012.
26. Freeman AJ, Dore GJ, Law MG, et al. Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology. 2001;34(4 pt 1):809-816.
27. Tong MJ, el-Farra NS, Reikes AR, Co RL. Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med. 1995;332:1463-1466.
28. Niederau C, Lange S, Heintges T, et al. Prognosis of chronic hepatitis C: results of a large, prospective cohort study. Hepatology. 1998;28:1687-1695.
29. Demitri MS, Poussin K, Baccarini P, et al. HCV-associated liver cancer without cirrhosis. Lancet. 1995;345:413-415.
30. Schwarzinger M, Baillot S, Yazdanpanah PY, Rehm PJ, Mallet V. Contribution of alcohol use disorders on the burden of chronic hepatitis C in France, 2008-2013: a nationwide retrospective cohort study [published online ahead of print April 7, 2017]. J Hepatol. doi: 10.1016/j.hep.2017.01.031.
31. von Wulffen M, Clark PJ, Macdonald GA, et al. Liver-related mortality in countries of the developed world: an ecological study approach to explain the variability. Aliment Pharmacol Ther. 2016;44:68-77.
32. Madden R, Mallet V. Editorial: the burden of chronic liver disease—an ecological method sees the wood for the trees. Aliment Pharmacol Ther. 2016;44:531-532.
33. Wiese M, Fischer J, Lobermann M, et al. Evaluation of liver disease progression in the German hepatitis C virus (1b)-contaminated anti-D cohort at 35 years after infection. Hepatology. 2014;59:49–57.
34. Butt AA, Yan P, Lo Re V Iii, et al. LIver fibrosis progression in hepatitis c virus infection after seroconversion. JAMA Intern Med. 2015;175:178–185.
35. World Health Organization. Global Health Observatory (GHO) Data: Overweight and Obesity. who.int/gho/ncd/risk_factors/overweight/en/. Accessed May 31, 2017.
36. Conti F, Buonfiglioli F, Scuteri A, et al. Early occurrence and recurrence of hepatocellular carcinoma in HCV-related cirrhosis treated with direct-acting antivirals. J Hepatol. 2016;65:727-733.
37. Reig M, Marino Z, Perello C, et al. Unexpected high rate of early tumor recurrence in patients with HCV-related HCC undergoing interferon-free therapy. J Hepatol. 2016;65:719-726.
38. Yang JD, Aqel BA, Pungpapong S, Gores GJ, Roberts LR, Leise MD. Direct acting antiviral therapy and tumor recurrence after liver transplantation for hepatitis C-associated hepatocellular carcinoma. J Hepatol. 2016;65:859-860.
39. Kozbial K, Moser S, Schwarzer R, et al. Unexpected high incidence of hepatocellular carcinoma in cirrhotic patients with sustained virologic response following interferon-free direct-acting antiviral treatment. J Hepatol. 2016;65:856-858.
40. Najafzadeh M, Andersson K, Shrank WH, et al. Cost-effectiveness of novel regimens for the treatment of hepatitis C virus. Ann Intern Med. 2015;162:407-419.
41. van der Meer AJ, Wedemeyer H, Feld JJ, et al. Life expectancy in patients with chronic HCV infection and cirrhosis compared with a general population. JAMA. 2014;312:1927-1928.
42. Innes HA, McDonald SA, Dillon JF, et al. Toward a more complete understanding of the association between a hepatitis C sustained viral response and cause-specific outcomes. Hepatology. 2015;62:355-364.
43. Vandenbulcke H, Moreno C, Colle I, et al. Alcohol intake increases the risk of HCC in hepatitis C virus-related compensated cirrhosis: a prospective study. J Hepatol. 2016;65:543-551.
44. ANRS Collaborative Study Group on Hepatocellular Carcinoma (ANRS CO22 HEPATHER, CO12 CirVir, and CO23 CUPILT Cohorts). Lack of evidence of an effect of direct-acting antivirals on the recurrence of hepatocellular carcinoma: data from three ANRS cohorts. J Hepatol. 2016;65:734-740.
45. Innes HA, Hutchinson SJ, Barclay S, et al. Quantifying the fraction of cirrhosis attributable to alcohol among chronic hepatitis C virus patients: implications for treatment cost-effectiveness. Hepatology. 2013;57:451-460.
46. Hwang JP, Suarez-Almazor ME, Torres HA, et al. Hepatitis C virus screening in patients with cancer receiving chemotherapy. J Oncol Pract. 2014;10:e167-e174.
47. Mahale P, Sturgis EM, Tweardy DJ, Ariza-Heredia EJ, Torres HA. Association between hepatitis C virus and head and neck cancers [serial online]. J Natl Cancer Inst. 2016;108. pii: djw035.
48. Silvestri F, Pipan C, Barillari G, et al. Prevalence of hepatitis C virus infection in patients with lymphoproliferative disorders. Blood. 1996;87:4296-4301.
49. Oguz A, Aykas F, Unal D, et al. Hepatitis B and C seroprevalence in solid tumors—necessity for screening during chemotherapy. Asian Pac J Cancer Prev. 2014;15:1411-1414.
50. Dal Maso L, Franceschi S. Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: a meta-analysis of epidemiologic studies. Cancer Epidemiol Biomarkers Prev. 2006;15:2078-2085.
51. 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.
52. Fiorino S, Chili E, Bacchi-Reggiani L, et al. Association between hepatitis B or hepatitis C virus infection and risk of pancreatic adenocarcinoma development: a systematic review and meta-analysis. Pancreatology. 2013;13:147-160.
53. Gisbert JP, Garcia-Buey L, Pajares JM, Moreno-Otero R. Prevalence of hepatitis C virus infection in B-cell non-Hodgkin's lymphoma: systematic review and meta-analysis. Gastroenterology. 2003;125:1723-1732.
54. Matsuo K, Kusano A, Sugumar A, Nakamura S, Tajima K, Mueller NE. Effect of hepatitis C virus infection on the risk of non-Hodgkin's lymphoma: a meta-analysis of epidemiological studies. Cancer Sci. 2004;95:745-752.
55. Negri E, Little D, Boiocchi M, La Vecchia C, Franceschi S. B-cell non-Hodgkin's lymphoma and hepatitis C virus infection: a systematic review. Int J Cancer. 2004;111:1-8.
56. Palmer WC, Patel T. Are common factors involved in the pathogenesis of primary liver cancers? A meta-analysis of risk factors for intrahepatic cholangiocarcinoma. J Hepatol. 2012;57:69-76.
57. Pozzato G, Mazzaro C, Dal Maso L, et al. Hepatitis C virus and non-Hodgkin's lymphomas: meta-analysis of epidemiology data and therapy options. World J Hepatol. 2016;8:107-116.
58. Shin HR, Oh JK, Masuyer E, et al. Epidemiology of cholangiocarcinoma: an update focusing on risk factors. Cancer Sci. 2010;101:579-585.
59. Wang Z, Sheng YY, Dong QZ, Qin LX. Hepatitis B virus and hepatitis C virus play different prognostic roles in intrahepatic cholangiocarcinoma: a meta-analysis. World J Gastroenterol. 2016;22:3038-3051.
60. Xu JH, Fu JJ, Wang XL, Zhu JY, Ye XH, Chen SD. Hepatitis B or C viral infection and risk of pancreatic cancer: a meta-analysis of observational studies. World J Gastroenterol. 2013;19:4234-4241.
61. Zhou YM, Zhao YF, Li B, et al. Hepatitis viruses infection and risk of intrahepatic cholangiocarcinoma: evidence from a meta-analysis [serial online]. BMC Cancer. 2012;12:289.
62. Bruix J, Barrera JM, Calvet X, et al. Prevalence of antibodies to hepatitis C virus in Spanish patients with hepatocellular carcinoma and hepatic cirrhosis. Lancet. 1989;2:1004-1006.
63. Colombo M, Kuo G, Choo QL, et al. Prevalence of antibodies to hepatitis C virus in Italian patients with hepatocellular carcinoma. Lancet. 1989;2:1006-1008.
64. GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1459-1544.
65. Moore MS, Ivanina E, Bornschlegel K, Qiao B, Schymura MJ, Laraque F. Hepatocellular carcinoma and viral hepatitis in New York City. Clin Infect Dis. 2016;63:1577-1583.
66. Shin HR, Lee CU, Park HJ, et al. Hepatitis B and C virus, Clonorchis sinensis for the risk of liver cancer: a case-control study in Pusan, Korea. Int J Epidemiol. 1996;25:933-940.
67. Donato F, Gelatti U, Tagger A, et al. Intrahepatic cholangiocarcinoma and hepatitis C and B virus infection, alcohol intake, and hepatolithiasis: a case-control study in Italy. Cancer Causes Control. 2001;12:959-964.
68. El-Serag HB, Engels EA, Landgren O, et al. Risk of hepatobiliary and pancreatic cancers after hepatitis C virus infection: a population-based study of US veterans. Hepatology. 2009;49:116-123.
69. Ferri C, Caracciolo F, Zignego AL, et al. Hepatitis C virus infection in patients with non-Hodgkin's lymphoma. Br J Haematol. 1994;88:392-394.
70. de Sanjose S, Benavente Y, Vajdic CM, et al. Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol. 2008;6:451-458.
71. Anderson LA, Pfeiffer R, Warren JL, et al. Hematopoietic malignancies associated with viral and alcoholic hepatitis. Cancer Epidemiol Biomarkers Prev. 2008;17:3069-3075.
72. 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.
73. Moriya K, Fujie H, Shintani Y, et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med. 1998;4:1065-1067.
74. Okuda M, Li K, Beard MR, et al. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology. 2002;122:366-375.
75. Ariumi Y, Kuroki M, Dansako H, et al. The DNA damage sensors ataxia-telangiectasia mutated kinase and checkpoint kinase 2 are required for hepatitis C virus RNA replication. J Virol. 2008;82:9639-9646.
76. Silini E, Bottelli R, Asti M, et al. Hepatitis C virus genotypes and risk of hepatocellular carcinoma in cirrhosis: a case-control study. Gastroenterology. 1996;111:199-205.
77. Torres HA, Nevah MI, Barnett BJ, et al. Hepatitis C virus genotype distribution varies by underlying disease status among patients in the same geographic region: a retrospective multicenter study. J Clin Virol. 2012;54:218-222.
78. El-Serag HB, Kanwal F, Richardson P, Kramer J. Risk of hepatocellular carcinoma after sustained virological response in veterans with hepatitis C virus infection. Hepatology. 2016;64:130-137.
79. Yu GY, He G, Li CY, et al. Hepatic expression of HCV RNA-dependent RNA polymerase triggers innate immune signaling and cytokine production. Mol Cell. 2012;48:313-321.
80. Tomasetti C, Li L, Vogelstein B. Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention. Science. 2017;355:1330-1334.
81. Guichard C, Amaddeo G, Imbeaud S, et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat Genet. 2012;44:694-698.
82. Fujimoto A, Furuta M, Totoki Y, et al. Whole-genome mutational landscape and characterization of noncoding and structural mutations in liver cancer. Nat Genet. 2016;48:500-509.
83. Barbaro G, Di Lorenzo G, Asti A, et al. Hepatocellular mitochondrial alterations in patients with chronic hepatitis C: ultrastructural and biochemical findings. Am J Gastroenterol. 1999;94:2198-2205.
84. Korenaga M, Wang T, Li Y, et al. Hepatitis C virus core protein inhibits mitochondrial electron transport and increases reactive oxygen species (ROS) production. J Biol Chem. 2005;280:37481-37488.
85. Nault JC, Calderaro J, Di Tommaso L, et al. Telomerase reverse transcriptase promoter mutation is an early somatic genetic alteration in the transformation of premalignant nodules in hepatocellular carcinoma on cirrhosis. Hepatology. 2014;60:1983-1992.
86. Takeda H, Takai A, Inuzuka T, Marusawa H. Genetic basis of hepatitis virus-associated hepatocellular carcinoma: linkage between infection, inflammation, and tumorigenesis. J Gastroenterol. 2017;52:26-38.
87. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology. 2004;127(5 suppl 1):S35-S50.
88. NCD Risk Factor Collaborative (NCD-RisC). Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19·2 million participants. Lancet. 2016;387:1377-1396.
89. Delarocque-Astagneau E, Roudot-Thoraval F, Campese C, Desenclos JC; Hepatitis C Surveillance System Steering Committee. Past excessive alcohol consumption: a major determinant of severe liver disease among newly referred hepatitis C virus infected patients in hepatology reference centers, France, 2001. Ann Epidemiol. 2005;15:551-557.
90. Komuta M, Spee B, Vander Borght S, et al. Clinicopathological study on cholangiolocellular carcinoma suggesting hepatic progenitor cell origin. Hepatology. 2008;47:1544-1556.
91. Nagao Y, Sata M, Noguchi S, et al. Detection of hepatitis C virus RNA in oral lichen planus and oral cancer tissues. J Oral Pathol Med. 2000;29:259-266.
92. Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S. The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood. 2001;98:3745-3749.
93. Chen CL, Huang JY, Wang CH, et al. Hepatitis C virus has a genetically determined lymphotropism through co-receptor B7.2 [serial online]. Nat Commun. 2017;8:13882.
94. Hartridge-Lambert SK, Stein EM, Markowitz AJ, Portlock CS. Hepatitis C and non-Hodgkin lymphoma: the clinical perspective. Hepatology. 2012;55:634-641.
95. Peveling-Oberhag J, Arcaini L, Hansmann ML, Zeuzem S. Hepatitis C-associated B-cell non-Hodgkin lymphomas. Epidemiology, molecular signature and clinical management. J Hepatol. 2013;59:169-177.
96. Hermine O, Lefrere F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002;347:89-94.
97. Sultanik P, Klotz C, Brault P, Pol S, Mallet V. Regression of an HCV-associated disseminated marginal zone lymphoma under IFN-free antiviral treatment. Blood. 2015;125:2446-2447.
98. Arcaini L, Besson C, Frigeni M, et al. Interferon-free antiviral treatment in B-cell lymphoproliferative disorders associated with hepatitis C virus infection. Blood. 2016;1128:2527-2532.
99. Maciocia N, O'Brien A, Ardeshna K. Remission of follicular lymphoma after treatment for hepatitis C virus infection. N Engl J Med. 2016;375:1699-1701.
100. Cabibbo G, Petta S, Barbara M, et al. Hepatic decompensation is the major driver of death in HCV-infected cirrhotic patients with successfully treated early hepatocellular carcinoma [published online ahead of print 2017]. J Hepatol. 2017. doi: 10.1016/j.jhep.2017.01.033.
101. Torres HA, Hosry J, Mahale P, Economides MP, Lok AS, Hepatitis C virus reactivation in patients with cancer: a prospective observational study of 91 patients. Paper presented at: The Liver Meeting; November 11-15, 2016; Boston, MA.
102. Navarro VJ, Senior JR. Drug-related hepatotoxicity. N Engl J Med. 2006;354:731-739.
103. Strasser SI, Myerson D, Spurgeon CL, et al. Hepatitis C virus infection and bone marrow transplantation: a cohort study with 10-year follow-up. Hepatology. 1999;29:1893-1899.
104. Oliver NT, Nieto YL, Blechacz B, Anderlini P, Ariza-Heredia E, Torres HA. Severe hepatitis C reactivation as an early complication of hematopoietic cell transplantation. Bone Marrow Transplant. 2017;52:138-140.
105. Nakasone H, Kurosawa S, Yakushijin K, et al. Impact of hepatitis C virus infection on clinical outcome in recipients after allogeneic hematopoietic cell transplantation. Am J Hematol. 2013;88:477-484.
106. Evans AT, Loeb KR, Shulman HM, et al. Fibrosing cholestatic hepatitis C after hematopoietic cell transplantation: report of 3 fatal cases. Am J Surg Pathol. 2015;39:212-220.
107. Torres HA, McDonald GB. How I treat hepatitis C virus infection in patients with hematologic malignancies. Blood. 2016;128:1449-1457.
108. McGovern BH, Birch CE, Bowen MJ, et al. Improving the diagnosis of acute hepatitis C virus infection with expanded viral load criteria. Clin Infect Dis. 2009;49:1051-1060.
109. Torres HA, Davila M. Reactivation of hepatitis B virus and hepatitis C virus in patients with cancer. Nat Rev Clin Oncol. 2012;9:156-166.
110. Vento S, Cainelli F, Mirandola F, et al. Fulminant hepatitis on withdrawal of chemotherapy in carriers of hepatitis C virus. Lancet. 1996;347:92-93.
111. Melisko ME, Fox R, Venook A. Reactivation of hepatitis C virus after chemotherapy for colon cancer. Clin Oncol (R Coll Radiol). 2004;16:204-205.
112. Goutte N, Sogni P, Bendersky N, Barbare JC, Falissard B, Farges O. Geographical variations in incidence, management and survival of hepatocellular carcinoma in a Western country. J Hepatol. 2017;66:537-544.
113. Kawaoka T, Aikata H, Teraoka Y, et al. Impact of hepatitis C virus eradication on the clinical outcome of patients with hepatitis C virus-related advanced hepatocellular carcinoma treated with sorafenib [published online ahead of print March 1, 2017]. Oncology. doi: 10.1159/000458532.
114. Cheung MC, Walker AJ, Hudson BE, et al. Outcomes after successful direct-acting antiviral therapy for patients with chronic hepatitis C and decompensated cirrhosis. J Hepatol. 2016;65:741-747.
115. Omata M, Kanda T, Wei L, et al. APASL consensus statements and recommendations for hepatitis C prevention, epidemiology, and laboratory testing. Hepatol Int. 2016;10:681-701.
116. European Association for the Study of the Liver (easloffice@easloffice.eu) EASL recommendations on treatment of hepatitis C 2016. J Hepatol. 2017;66:153-194.
117. Ryerson AB, Eheman CR, Altekruse SF, et al. Annual Report to the Nation on the Status of Cancer, 1975-2012, featuring the increasing incidence of liver cancer. Cancer. 2016;122:1312-1337.
118. Howlader N, Noone AM, Krapcho M, et al, eds. SEER Cancer Statistics Review, 1975-2013. Bethesda, MD: National Cancer Institute; 2016. seer.cancer.gov/csr/1975_2013/, based on the November 2015 SEER data submission, posted to the SEER web site, April 2016.
119. Weinbaum CM, Williams I, Mast EE, et al. Recommendations for identification and public health management of persons with chronic hepatitis B virus infection. MMWR Recomm Rep. 2008;57:1–20.
120. European Association for the Study of the Liver (easloffice@easloffice.eu) EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol. 2017. pii: S0168-0000(17)30185-X. doi: 10.1016/j.jhep.2017.03.021. [Epub ahead of print]
121. Hsieh YH, Rothman RE, Laeyendecker OB, et al. Evaluation of the Centers for Disease Control and Prevention recommendations for hepatitis C virus testing in an urban emergency department. Clin Infect Dis. 2016;62:1059-1065.
122. Saxena A, Hassan M, Mahale P, Kontoyiannis DP, Torres HA. Screening for hepatitis C viral infection in a tertiary care cancer center. Hepatology. 2012;56:662A-663A.
123. Brasseur M, Heurgue-Berlot A, Barbe C, et al. Prevalence of hepatitis B and C and sensibility of a selective screening questionnaire in patients receiving chemotherapy for solid tumors [serial online]. BMC Cancer. 2015;15:999.
124. US Preventive Services Task Force (USPSTF). Screening for Hepatitis C Virus Infection in Adults: US Preventive Services Task Force Recommendation Statement. Rockville, MD: US Preventive Services Task Force; 2013. uspreventiveservicestaskforce.org/uspstf/uspshepc.htm. Accessed May 3, 2017.
125. Torres HA, Mahale P, Miller ED, Oo TH, Frenette C, Kaseb AO. Coadministration of telaprevir and transcatheter arterial chemoembolization in hepatitis C virus-associated hepatocellular carcinoma. World J Hepatol. 2013;5:332-335.
126. Tien PC; Veterans Affairs Hepatitis C Resource Center Program; National Hepatitis C Program Office. Management and treatment of hepatitis C virus infection in HIV-infected adults: recommendations from the Veterans Affairs Hepatitis C Resource Center Program and National Hepatitis C Program Office. Am J Gastroenterol. 2005;100:2338-2354.
127. Vauthey JN, Pawlik TM, Ribero D, et al. Chemotherapy regimen predicts steatohepatitis and an increase in 90-day mortality after surgery for hepatic colorectal metastases. J Clin Oncol. 2006;24:2065-2072.
128. Yakushijin K, Atsuta Y, Doki N, et al. Sinusoidal obstruction syndrome after allogeneic hematopoietic stem cell transplantation: incidence, risk factors and outcomes. Bone Marrow Transplant. 2016;51:403-409.
129. McDonald GB. Hepatobiliary complications of hematopoietic cell transplantation, 40 years on. Hepatology. 2010;51:1450-1460.
130. Clavien P, Petrowsky H, DeOliveira ML, Graf R. Medical progress: strategies for safer liver surgery and partial liver transplantation. N Engl J Med. 2007;356:1545-1559.
131. Lewis JH, Stine JG. Review article: prescribing medications in patients with cirrhosis–a practical guide. Aliment Pharmacol Ther. 2013;37:1132-1156.
132. Castera L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128:343-350.
133. Sultanik P, Kramer L, Soudan D, et al. The relationship between liver stiffness measurement and outcome in patients with chronic hepatitis C and cirrhosis: a retrospective longitudinal hospital study. Aliment Pharmacol Ther. 2016;44:505-513.
134. Bravo AA, Sheth SG, Chopra S. Current concepts: liver biopsy. N Engl J Med. 2001;344:495-500.
135. Saunders JB, Walters JR, Davies AP, Paton A. A 20-year prospective study of cirrhosis. BMJ (Clin Res Ed). 1981;282:263-266.
136. D'Amico G, Garcia-Tsao G, Pagliaro L. Natural history and prognostic indicators of survival in cirrhosis: a systematic review of 118 studies. J Hepatol. 2006;44:217-231.
137. Superfin D, Iannucci AA, Davies AM. Commentary: oncologic drugs in patients with organ dysfunction: a summary. Oncologist. 2007;12:1070-1083.
138. Bruix J, Castells A, Bosch J, et al. Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology. 1996;111:1018-1022.
139. Iavarone M, Primignani M, Vavassori S, et al. Determinants of esophageal varices bleeding in patients with advanced hepatocellular carcinoma treated with sorafenib. United European Gastroenterol J. 2016;4:363-370.
140. de Franchis R. Expanding consensus in portal hypertension: report of the Baveno VI Consensus Workshop: stratifying risk and individualizing care for portal hypertension. J Hepatol. 2015;63:743-752.
141. Martin P, DiMartini A, Feng S, Brown R Jr, Fallon M. Evaluation for liver transplantation in adults: 2013 practice guideline by the American Association for the Study of Liver Diseases and the American Society of Transplantation. Hepatology. 2014;59:1144-1165.
142. Curry MP. Direct acting antivirals for decompensated cirrhosis. Efficacy and safety are now established. J Hepatol. 2016;64:1206-1207.
143. Welker MW, Luhne S, Lange CM, et al. Lactic acidosis in patients with hepatitis C virus cirrhosis and combined ribavirin/sofosbuvir treatment. J Hepatol. 2016;64:790-799.
144. Oberg CL, Hiensch RJ, Poor HD. Ombitasvir-paritaprevir-ritonavir-dasabuvir (Viekira Pak)-induced lactic acidosis. Crit Care Med. 2017;45:e321-e325.
145. Economides MP, Mahale P, Kyvernitakis A, et al. Concomitant use of direct-acting antivirals and chemotherapy in hepatitis C virus-infected patients with cancer. Aliment Pharmacol Ther. 2016;44:1235-1241.
146. Sarrazin C, Isakov V, Svarovskaia ES, et al. Late relapse versus hepatitis C virus reinfection in patients with sustained virologic response after sofosbuvir-based therapies. Clin Infect Dis. 2017;64:44-52.
147. Mahale P, Okhuysen PC, Torres HA. Does chemotherapy cause viral relapse in cancer patients with hepatitis C infection successfully treated with antivirals? Clin Gastroenterol Hepatol. 2014;12:1051-1054, e1051.
148. Lok AS, Everhart JE, Di Bisceglie AM, et al. Occult and previous hepatitis B virus infection are not associated with hepatocellular carcinoma in United States patients with chronic hepatitis C. Hepatology. 2011;54:434-442.
149. Ende AR, Kim NH, Yeh MM, Harper J, Landis CS. Fulminant hepatitis B reactivation leading to liver transplantation in a patient with chronic hepatitis C treated with simeprevir and sofosbuvir: a case report [serial online]. J Med Case Rep. 2015;9:164.
150. Wang C, Ji D, Chen J, et al. Hepatitis due to reactivation of hepatitis B virus in endemic areas among patients with hepatitis C treated with direct-acting antiviral agents. Clin Gastroenterol Hepatol. 2017;15:132-136.
151. Londono MC, Lens S, Marino Z, et al. Hepatitis B reactivation in patients with chronic hepatitis C undergoing anti-viral therapy with an interferon-free regimen. Aliment Pharmacol Ther. 2017;45:1156-1161.
152. Belperio PS, Shahoumian TA, Mole LA, Backus LI. Evaluation of hepatitis B reactivation among 62,920 veterans treated with oral hepatitis C antivirals [published online ahead of print February 27, 2017]. Hepatology. doi: 10.1002/hep.29135.
153. Di Bisceglie AM, Lok AS, Martin P, Terrault N, Perrillo RP, Hoofnagle JH. Recent US Food and Drug Administration warnings on hepatitis B reactivation with immune-suppressing and anticancer drugs: just the tip of the iceberg? Hepatology. 2015;61:703-711.
154. Hwang JP, Somerfield MR, Alston-Johnson DE, et al. Hepatitis B virus screening for patients with cancer before therapy: American Society of Clinical Oncology provisional clinical opinion update. J Clin Oncol. 2015;33:2212-2220.
155. van der Meer AJ, Veldt BJ, Feld JJ, et al. Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA. 2012;308:2584-2593.
156. Morgan RL, Baack B, Smith BD, Yartel A, Pitasi M, Falck-Ytter Y. Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma: a meta-analysis of observational studies. Ann Intern Med. 2013;158(5 pt 1):329-337.
157. Foster GR, Irving WL, Cheung MC, et al. Impact of direct acting antiviral therapy in patients with chronic hepatitis C and decompensated cirrhosis. J Hepatol. 2016;64:1224-1231.
158. Dyson JK, Hutchinson J, Harrison L, et al. Liver toxicity associated with sofosbuvir, an NS5A inhibitor and ribavirin use. J Hepatol. 2016;64:234-238.
159. van Schaik RH. CYP450 pharmacogenetics for personalizing cancer therapy. Drug Resist Updat. 2008;11:77-98.
160. Hosry J, Mahale P, Turturro F, et al. Antiviral therapy improves overall survival in hepatitis C virus-infected patients who develop diffuse large B-cell lymphoma. Int J Cancer. 2016;139:2519-2528.
161. National Comprehensive Cancer Network (NCCN). Splenic Marginal Zone Lymphoma. Version 3. Port Washington, PA: National Comprehensive Cancer Network; 2017. nccn.org/professionals/physician_gls/f_guidelines.asp. Accessed May 31, 2017.
162. Reig M, Boix L, Bruix J. The impact of direct antiviral agents on the development and recurrence of hepatocellular carcinoma. Liver Int. 2017;37(suppl 1):136-139.
163. Torres HA, Vauthey JN, Economides MP, Mahale P, Kaseb A. Hepatocellular carcinoma recurrence after treatment with direct-acting antivirals: first, do no harm by withdrawing treatment. J Hepatol. 2016;65:862-864.
164. Calleja JL, Crespo J, Rincon D, et al. Effectiveness, safety and clinical outcomes of direct-acting antiviral therapy in HCV genotype 1 infection: results from a Spanish real world cohort. J Hepatol. 2017;66:1138–1148.
165. Manthravadi S, Paleti S, Pandya P. Impact of sustained viral response postcurative therapy of hepatitis C-related hepatocellular carcinoma: a systematic review and meta-analysis. Int J Cancer. 2017;140:1042-1049.
166. Alanio C, Nicoli F, Sultanik P, et al. Bystander hyperactivation of preimmune CD8+ T cells in chronic HCV patients [serial online]. Elife. 2015;4. pii: 307916.
167. Langhans B, Nischalke HD, Kramer B, et al. Increased peripheral CD4+ regulatory T cells persist after successful direct-acting antiviral treatment of chronic hepatitis C. J Hepatol. 2017;66:888-896.
168. Tatsumi T, Takehara T. Impact of natural killer cells on chronic hepatitis C and hepatocellular carcinoma. Hepatol Res. 2016;46:416-422.
169. Villani R, Facciorusso A, Bellanti F, et al. DAAs rapidly reduce inflammation but increase serum VEGF level: a rationale for tumor risk during anti-HCV treatment [serial online]. PLoS One. 2016;11:e0167934.
170. Giacomini KM, Huang SM. Transporters in drug development and clinical pharmacology. Clin Pharmacol Ther. 2013;94:3-9.
171. Milazzo L, Biasin M, Gatti N, et al. Thalidomide in the treatment of chronic hepatitis C unresponsive to alfa-interferon and ribavirin. Am J Gastroenterol. 2006;101:399-402.
172. Caseiro MM. Treatment of chronic hepatitis C in non-responsive patients with pegylated interferon associated with ribavirin and thalidomide: report of six cases of total remission. Rev Inst Med Trop Sao Paulo. 2006;48:109-112.
173. Peyrin-Biroulet L, Cadranel JF, Nousbaum JB, et al. Interaction of ribavirin with azathioprine metabolism potentially induces myelosuppression. Aliment Pharmacol Ther. 2008;28:984-993.
174. Kraljacic BC, Arguello M, Amri A, Cormack G, Borden K. Inhibition of eIF4E with ribavirin cooperates with common chemotherapies in primary acute myeloid leukemia specimens. Leukemia. 2011;25:1197-1200.
175. Pardo-Yules B, Gallego-Duran R, Eslam M, et al. Thalidomide with peginterferon alfa-2b and ribavirin in the treatment of non-responders genotype 1 chronic hepatitis C patients: proof of concept [article in English, Spanish]. Rev Esp Enferm Dig. 2011;103:619-625.
176. Shi F, Len Y, Gong Y, et al. Ribavirin inhibits the activity of mTOR/eIF4E, ERK/Mnk1/eIF4E signaling pathway and synergizes with tyrosine kinase inhibitor imatinib to impair Bcr-Abl mediated proliferation and apoptosis in Ph+ leukemia [serial online]. PLoS One. 2015;10:e0136746.
177. Britnell SR, Willets AE, Vanderman AJ, Woodard CL, Britt RB. Influence of successful chronic hepatitis C virus treatment with ledipasvir/sofosbuvir on warfarin dosing requirements in four veterans. Pharmacotherapy. 2016;36:1173-1179.
178. DeCarolis DD, Westanmo AD, Chen YC, Boese AL, Walquist MA, Rector TS. Evaluation of a potential interaction between new regimens to treat hepatitis C and warfarin. Ann Pharmacother. 2016;50:909-917.
179. Schulman S. Inhibition of warfarin activity by ribavirin. Ann Pharmacother. 2002;36:72-74.
180. Gilead Sciences Inc. EPCLUSA (sofosbuvir and velpatasvir) [package inert]. Revised June 2016. Foster City, CA: Gilead Sciences Inc; 2016.
181. Bristol-Myers Squibb Company. DAKLINZA (daclatasvir) [package insert]. Revised April 2016. Princeton, NJ: Bristol-Myers Squibb Company; 2016.
182. Genentech Inc. COPEGUS (ribavirin) [package insert]. Revised August 2011. South San Francisco, CA: Genentech Inc; 2011.
183. Gilead Sciences Inc. HARVONI (ledipasvir and sofosbuvir) [package insert]. Revised June 2016. Foster City, CA: Gilead Sciences Inc; 2016.
184. Janssen Therapeutics. OLYSIO (simeprevir) [package insert]. Revised May 2016. Titusville, NJ: Janssen Therapeutics; 2016.
185. Gilead Sciences Inc. SOVALDI (sofosbuvir) [package insert]. Revised August 2015. Foster City, CA: Gilead Sciences Inc; 2015.
186. Merck Sharp & Dohme Corp. ZEPATIER (elbasvir and grazoprevir) [package insert]. Revised January 2016. Kenilworth, NJ: Merck Sharp & Dohme Corp; 2016.
187. AbbVie Inc. VIEKIRA PAK (ombitasvir paritaprevir and ritonavir tablets; dasabuvir tablets) [package insert]. Revised June 2016. North Chicago, IL: AbbVie Inc; 2016.
188. Puglisi GM, Smith SM, Jankovich RD, Ashby CR Jr, Jodlowski TZ. Paritaprevir/ritonavir/ombitasvir+dasabuvir plus ribavirin therapy and inhibition of the anticoagulant effect of warfarin: a case report. J Clin Pharm Ther. 2017;42:115-118.
189. Hoofnagle JH, Sherker AH. Hepatitis C: down but not out. Ann Intern Med. 2017;166:675-676.