Primary liver cancer deaths and related years of life lost attributable to hepatitis B and C viruses in India

Cancer Epidemiology

Volumn 40, Issue , 2016, Pages 79-86

  Islami, Farhad ^a   Dikshit, Rajesh ^b   Mallath, Mohandas K ^c   Jemal, Ahmedin ^a  

^a AMERICAN CANCER SOCIETY   (United States)

^b TATA MEMORIAL HOSPITAL   (India)

^c Tata Medical Center ^*  (India)

Author keywords

Hepatitis B virus; Hepatitis C virus; India; Liver cancer; Population attributable fraction

Indexed keywords

HEPATITIS B CORE ANTIBODY; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIBODY; VIRUS DNA; VIRUS RNA;

ARTICLE; BILE DUCT CARCINOMA; CANCER MORTALITY; GALLBLADDER CANCER; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; INDIA; LIVER CANCER; LIVER CELL CARCINOMA; PRIORITY JOURNAL; SYSTEMATIC REVIEW; COMPLICATION; EPIDEMIOLOGY; FACTUAL DATABASE; HEPACIVIRUS; LIVER NEOPLASMS; META ANALYSIS (TOPIC); MORTALITY; PROGNOSIS; RISK FACTOR; SURVIVAL RATE;

DATABASES, FACTUAL; HEPACIVIRUS; HEPATITIS B; HEPATITIS B VIRUS; HEPATITIS C; HUMANS; INDIA; LIVER NEOPLASMS; META-ANALYSIS AS TOPIC; PROGNOSIS; RISK FACTORS; SURVIVAL RATE;

EID: 84958744077     PISSN: 18777821     EISSN: 1877783X     Source Type: Journal    
DOI: 10.1016/j.canep.2015.11.012     Document Type: Article

References (80)

1. Bouvard V., Baan R., Straif K., Grosse Y., Secretan B., El Ghissassi F., et al. A review of human carcinogens-part B: biological agents. Lancet Oncol. 2009, 10:321-322.
2. Perz J.F., Armstrong G.L., Farrington L.A., Hutin Y.J., Bell B.P. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J. Hepatol. 2006, 45:529-538.
3. Qu C., Chen T., Fan C., Zhan Q., Wang Y., Lu J., et al. Efficacy of neonatal HBV vaccination on liver cancer and other liver diseases over 30-year follow-up of the Qidong hepatitis B intervention study: a cluster randomized controlled trial. PLoS Med. 2014, 11:e1001774.
4. Lahariya C., Subramanya B.P., Sosler S. An assessment of hepatitis B vaccine introduction in India: lessons for roll out and scale up of new vaccines in immunization programs. Indian J. Public Health 2013, 57:8-14.
5. Harris J.B., Gacic-Dobo M., Eggers R., Brown D.W., Sodha S.V., Centers for Disease C, et al. Global routine vaccination coverage, 2013. MMWR Morb. Mortal. Wkly. Rep. 2014, 63:1055-1058.
6. Liang X., Bi S., Yang W., Wang L., Cui G., Cui F., et al. Epidemiological serosurvey of hepatitis B in China-declining HBV prevalence due to hepatitis B vaccination. Vaccine 2009, 27:6550-6557.
7. Yang H.I., Lu S.N., Liaw Y.F., You S.L., Sun C.A., Wang L.Y., et al. Hepatitis B. e antigen and the risk of hepatocellular carcinoma. N. Engl. J. Med. 2002, 347:168-174.
8. Fattovich G., Bortolotti F., Donato F. Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J. Hepatol. 2008, 48:335-352.
9. Liu C.J., Kao J.H. Global perspective on the natural history of chronic hepatitis B: role of hepatitis B virus genotypes A to J. Semin. Liver Dis. 2013, 33:97-102.
10. Liu S., Zhang H., Gu C., Yin J., He Y., Xie J., et al. Associations between hepatitis B virus mutations and the risk of hepatocellular carcinoma: a meta-analysis. J. Natl. Cancer Inst. 2009, 101:1066-1082.
11. Raimondi S., Bruno S., Mondelli M.U., Maisonneuve P. Hepatitis C virus genotype 1b as a risk factor for hepatocellular carcinoma development: a meta-analysis. J. Hepatol. 2009, 50:1142-1154.
12. Chuang S.C., Lee Y.C., Hashibe M., Dai M., Zheng T., Boffetta P. Interaction between cigarette smoking and hepatitis B and C virus infection on the risk of liver cancer: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 2010, 19:1261-1268.
13. Loomba R., Yang H.I., Su J., Brenner D., Iloeje U., Chen C.J. Obesity and alcohol synergize to increase the risk of incident hepatocellular carcinoma in men. Clin. Gastroenterol. Hepatol. 2010, 8. 891-8 98 e1-2.
14. Zhang H., Zhai Y., Hu Z., Wu C., Qian J., Jia W., et al. Genome-wide association study identifies 1p36.22 as a new susceptibility locus for hepatocellular carcinoma in chronic hepatitis B virus carriers. Nat. Genet. 2010, 42:755-758.
15. Murhekar M.V., Zodpey S.P. Hepatitis B virus infection among Indian tribes: need for vaccination program. Indian J. Gastroenterol. 2005, 24:269-270.
16. Batham A., Narula D., Toteja T., Sreenivas V., Puliyel J.M. Sytematic review and meta-analysis of prevalence of hepatitis B in India. Indian Pediatr. 2007, 44:663-674.
17. Saraswat V., Norris S., de Knegt R.J., Sanchez Avila J.F., Sonderup M., Zuckerman E., et al. Historical epidemiology of hepatitis C virus (HCV) in select countries-volume 2. J. Viral. Hepat. 2015, 22(Suppl. 1):6-25.
18. Acharya S.K. This is hepatitis: know it, confront it. Indian J. Med. Res. 2013, 138:8-10.
19. Centers for Disease Control and Prevention. Viral Hepatitis Statistics and Surveillance-Disease burden from viral hepatitis A, B, and C in the United States. 03/04/2015 [cited 04/09/2015] available from: http://www.cdc.gov/hepatitis/Statistics/.
20. J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer available from: In, 2013. http://globocan.iarc.fr.
21. Dikshit R., Gupta P.C., Ramasundarahettige C., Gajalakshmi V., Aleksandrowicz L., Badwe R., et al. Cancer mortality in India: a nationally representative survey. Lancet 2012, 379:1807-1816.
22. Stroup D.F., Berlin J.A., Morton S.C., Olkin I., Williamson G.D., Rennie D., et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting: meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 2000, 283:2008-2012.
23. Anand S., Malaviya A.N. H.A.A. in primary liver-cell carcinoma. Lancet 1971, 2:1032-1033.
24. Nayak N.C., Dhar A., Sachdeva R., Mittal A., Seth H.N., Sudarsanam D., et al. Association of human hepatocellular carcinoma and cirrhosis with hepatitis B virus surface and core antigens in the liver. Int. J. Cancer 1977, 20:643-654.
25. Kelker S.S., Talib V.H., Khare P.M., Menon G.G., Raichur B.S. Hepatitis B antigen hepatomas. Indian J. Med. Sci. 1978, 31:90-93.
26. Nayak N.C., Sachdeva R., Dhar A., Seth H.N. Demonstration of hepatitis B virus surface component in human hepatocellular cancer cells. Indian J. Med. Res. 1979, 69:161-167.
27. Ramesh R., Munshi A., Panda S.K. Prevalence of hepatitis C virus antibodies in chronic liver disease and hepatocellular carcinoma patients in India. J. Gastroenterol. Hepatol. 1992, 7:393-395.
28. Ramesh R., Panda S.K., Jameel S., Rajasambandam P. Mapping of the hepatitis B virus genome in hepatocellular carcinoma using PCR and demonstration of a potential trans-activator encoded by the frequently detected fragment. J. Gen. Virol. 1994, 75(Pt 2):327-334.
29. Irshad M., Acharya S.K., Joshi Y.K. Prevalence of hepatitis C virus antibodies in the general population & in selected groups of patients in Delhi. Indian J. Med. Res. 1995, 102:162-164.
30. Panicker J.N., Shenoy K.T., Augustine J. A cytological study of hepatitis B surface antigen localization using orcein staining in hepatocellular carcinoma. Indian J. Med. Res. 1996, 104:374-376.
31. Katiyar S., Dash B.C., Thakur V., Guptan R.C., Sarin S.K., Das B.C. P53 tumor suppressor gene mutations in hepatocellular carcinoma patients in India. Cancer 2000, 88:1565-1573.
32. Sarin S.K., Thakur V., Guptan R.C., Saigal S., Malhotra V., Thyagarajan S.P., et al. Profile of hepatocellular carcinoma in India: an insight into the possible etiologic associations. J. Gastroenterol. Hepatol. 2001, 16:666-673.
33. Wang B.E., Ma W.M., Sulaiman A., Noer S., Sumoharjo S., Sumarsidi D., et al. Demographic, clinical, and virological characteristics of hepatocellular carcinoma in Asia: survey of 414 patients from four countries. J. Med. Virol. 2002, 67:394-400.
34. Joshi N., Kumar A., Rani M.S., Chandra N., Ramanjaneyulu E.R. Clinical and aetiological profile of hepatoma at a tertiary care centre. Trop. Gastroenterol. 2003, 24:73-75.
35. Radhika N.S., Duseja A., Rajwanshi A., Gupta S.K., Sehgal S., Suri S., et al. Clinico-cytopathological spectrum of hepatocellular carcinoma, its correlation with serum alpha-fetoprotein level, and hepatitis B and C viral markers. Trop. Gastroenterol. 2004, 25:116-120.
36. Saini N., Bhagat A., Sharma S., Duseja A., Chawla Y. Evaluation of clinical and biochemical parameters in hepatocellular carcinoma: experience from an Indian center. Clin. Chim. Acta 2006, 371:183-186.
37. Kumar M., Kumar R., Hissar S.S., Saraswat M.K., Sharma B.C., Sakhuja P., et al. Risk factors analysis for hepatocellular carcinoma in patients with and without cirrhosis: a case-control study of 213 hepatocellular carcinoma patients from India. J. Gastroenterol. Hepatol. 2007, 22:1104-1111.
38. Vaiphei K. Correlative analysis of histological profile of the adjoining liver parenchyma with liver enzyme levels in hepatocellular carcinoma and their comparison with chronic liver disease in autopsy cases. Indian J. Pathol. Microbiol. 2007, 50:711-717.
39. Amarapurkar D.N., Patel N.D., Kamani P.M. Impact of diabetes mellitus on outcome of HCC. Ann. Hepatol. 2008, 7:148-151.
40. Kumar R., Saraswat M.K., Sharma B.C., Sakhuja P., Sarin S.K. Characteristics of hepatocellular carcinoma in India: a retrospective analysis of 191 cases. QJM 2008, 101:479-485.
41. Murugavel K.G., Mathews S., Jayanthi V., Shankar E.M., Hari R., Surendran R., et al. Alpha-fetoprotein as a tumor marker in hepatocellular carcinoma: investigations in south Indian subjects with hepatotropic virus and aflatoxin etiologies. Int. J. Infect. Dis. 2008, 12:e71-e76.
42. Paul S.B., Chalamalasetty S.B., Vishnubhatla S., Madan K., Gamanagatti S.R., Batra Y., et al. Clinical profile, etiology and therapeutic outcome in 324 hepatocellular carcinoma patients at a tertiary care center in India. Oncology 2009, 77:162-171.
43. Paul S.B., Gamanagatti S., Sreenivas V., Chandrashekhara S.H., Mukund A., Gulati M.S., et al. Trans-arterial chemoembolization (TACE) in patients with unresectable Hepatocellular carcinoma: experience from a tertiary care centre in India. Indian J. Radiol. Imaging 2011, 21:113-120.
44. Saini N., Srinivasan R., Chawla Y., Sharma S., Chakraborti A., Rajwanshi A. Telomerase activity, telomere length and human telomerase reverse transcriptase expression in hepatocellular carcinoma is independent of hepatitis virus status. Liver Int. 2009, 29:1162-1170.
45. Mohana Devi S., Balachandar V., Murugan P., Sasikala K., Manikantan P., Venkatakrishnan L.K. Identification of chromosomal aberrations by using trypsin G-banding in hepatocellular carcinoma patients (HCC) in Tamil Nadu, India. Trop. Life Sci. Res. 2010, 21:31-46.
46. Sharma B., Srinivasan R., Chawla Y.K., Kapil S., Saini N., Singla B., et al. Clinical utility of prothrombin induced by vitamin K absence in the detection of hepatocellular carcinoma in Indian population. Hepatol. Int. 2010, 4:569-576.
47. Biplap N., Bhimo T., Suraj T., Brojendro T., Lalbiakdiki Clinical profile of chronic liver disease with reference to hepatocellular carcinoma in RIMS. J. Med. Soc. 2011, 25:15-19.
48. Thakur S., Singla A., Chawla Y., Rajwanshi A., Kalra N., Arora S.K. Expansion of peripheral and intratumoral regulatory T-cells in hepatocellular carcinoma: a case-control study. Indian J. Pathol. Microbiol. 2011, 54:448-453.
49. Sarma M.P., Asim M., Medhi S., Bharathi T., Diwan R., Kar P. Viral genotypes and associated risk factors of hepatocellular carcinoma in India. Cancer Biol. Med. 2012, 9:172-181.
50. Amarapurkar D.N., Dharod M., Gautam S., Patel N. Risk of development of hepatocellular carcinoma in patients with NASH-related cirrhosis. Trop. Gastroenterol. 2013, 34:159-163.
51. Arora A., Sharma P., Tyagi P., Singla V., Arora V., Bansal N., et al. Hepatitis B virus infection can cause hepatocellular carcinoma in less advanced liver cirrhosis: a comparative study of 142 patients from north india. J. Clin. Exp. Hepatol. 2013, 3:288-295.
52. Medhi S., Sarma M.P., Asim M., Kar P. Genetic variants of heat shock protein A1L2437 and A1B1267 as possible risk factors for hepatocellular carcinoma in India. J. Viral Hepat. 2013, 20:e141-e147.
53. Pal S., Ramachandran J., Kurien R.T., Eapen A., Ramakrishna B., Keshava S.N., et al. Hepatocellular carcinoma continues to be diagnosed in the advanced stage: profile of hepatocellular carcinoma in a tertiary care hospital in South India. Trop. Doct. oct 2013, 43:25-26.
54. Kohli A., Murphy A.A., Agarwal C., Shivakumar B., Kottilil S., Polis M.A., et al. HCC surveillance results in earlier HCC detection: results from an Indian cohort. Springerplus 2014, 3:610.
55. Sood A., Midha V., Goyal O., Goyal P., Sood N., Sharma S.K. Profile of hepatocellular carcinoma in a tertiary care hospital in Punjab in northern India. Indian J. Gastroenterol. 2014, 33:35-40.
56. Asim M., Sarma M.P., Thayumanavan L., Kar P. Role of aflatoxin B1 as a risk for primary liver cancer in north Indian population. Clin. Biochem. 2011, 44:1235-1240.
57. Asim M., Sarma M.P., Kar P. Etiological and molecular profile of hepatocellular cancer from India. Int. J. Cancer 2013, 133:437-445.
58. Miettinen O.S. Proportion of disease caused or prevented by a given exposure, trait or intervention. Am. J. Epidemiol. 1974, 99:325-332.
59. de M., artel C., Ferlay J., Franceschi S., Vignat J., Bray F., Forman D., et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012, 13:607-615.
60. Oh J.K., Shin H.R., Lim M.K., Cho H., Kim D.I., Jee Y., et al. Multiplicative synergistic risk of hepatocellular carcinoma development among hepatitis B and C co-infected subjects in HBV endemic area: a community-based cohort study. BMC Cancer 2012, 12:452.
61. European Association for The Study of the Liver EASL clinical practice guidelines: management of chronic hepatitis B virus infection. J. Hepatol. 2012, 57:167-185.
62. Boccaccio V., Bruno S. Optimal management of patients with chronic hepatitis C and comorbidities. Liver Int. 2015, 35(Suppl. 1):35-43.
63. Kohli A., Shaffer A., Sherman A., Kottilil S. Treatment of hepatitis C: a systematic review. JAMA 2014, 312:631-640.
64. Arama V., Leblebicioglu H., Simon K., Zarski J.P., Niederau C., Habersetzer F., et al. Chronic hepatitis B monitoring and treatment patterns in five European countries with different access and reimbursement policies. Antivir. Ther. 2014, 19:245-257.
65. Jayasekera C.R., Barry M., Roberts L.R., Nguyen M.H. Treating hepatitis C in lower-income countries. N. Engl. J. Med. 2014, 370:1869-1871.
66. Solomon S.S., Mehta S.H., Srikrishnan A.K., Solomon S., McFall A.M., Laeyendecker O., et al. Burden of hepatitis C virus disease and access to hepatitis C virus services in people who inject drugs in India: a cross-sectional study. Lancet Infect. Dis. 2015, 15:36-45.
67. Ditah I., Al Bawardy B., Gonzalez H.C., Saberi B., Ditah C., Kamath P.S., et al. Lack of health insurance limits the benefits of hepatitis C virus screening: insights from the National Health and Nutrition Examination Hepatitis C follow-up study. Am. J. Gastroenterol. 2015.
68. Kumar A., Acharya S.K., Singh S.P., Saraswat V.A., Arora A., Duseja A., et al. The Indian National Association for Study of the Liver (INASL) consensus on prevention, diagnosis and management of hepatocellular carcinoma in India: the Puri recommendations. J. Clin. Exp. Hepatol. 2014, 4:S3-26.
69. Chaudhuri V., Nanu A., Panda S.K., Chand P. Evaluation of serologic screening of blood donors in India reveals a lack of correlation between anti-HBc titer and PCR-amplified HBV DNA. Transfusion (Paris) 2003, 43:1442-1448.
70. Puri P., Anand A.C., Saraswat V.A., Acharya S.K., Dhiman R.K., Aggarwal R., et al. Consensus statement of HCV task force of the Indian National Association for Study of the Liver (INASL). Part I: status report of HCV infection in India. J. Clin. Exp. Hepatol. 2014, 4:106-116.
71. Spina A., Eramova I., Lazarus J.V. Policy responses to viral hepatitis B and C among people who inject drugs in Member States of the WHO European region: a sub-analysis of the WHO 2013 global hepatitis policy survey. BMC Infect. Dis. 2014, 14(Suppl. 6):S15.
72. Tandon B.N., Acharya S.K., Tandon A. Epidemiology of hepatitis B virus infection in India. Gut 1996, 38(Suppl. 2):S56-S59.
73. Gupta S., Gupta R., Joshi Y.K., Singh S. Role of horizontal transmission in hepatitis B virus spread among household contacts in north India. Intervirology 2008, 51:7-13.
74. Stuver S.O., Boschi-Pinto C., Trichopoulos D. Infection with hepatitis B and C viruses, social class and cancer. IARC Sci. Publ. 1997, 31:319-324.
75. Custer B., Sullivan S.D., Hazlet T.K., Iloeje U., Veenstra D.L., Kowdley K.V. Global epidemiology of hepatitis B virus. J. Clin. Gastroenterol. 2004, 38:S158-S168.
76. Hadziyannis S.J. Natural history of chronic hepatitis B in Euro-Mediterranean and African countries. J. Hepatol. 2011, 55:183-191.
77. Kew M.C. Synergistic interaction between aflatoxin B1 and hepatitis B virus in hepatocarcinogenesis. Liver Int. 2003, 23:405-409.
78. Toteja G.S., Mukherjee A., Diwakar S., Singh P., Saxena B.N., Sinha K.K., et al. Aflatoxin B1 contamination in wheat grain samples collected from different geographical regions of India: a multicenter study. J. Food Prot. 2006, 69:1463-1467.
79. Ott J.J., Stevens G.A., Groeger J., Wiersma S.T. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine 2012, 30:2212-2219.
80. Mohd H., anafiah K., Groeger J., Flaxman A.D., Wiersma S.T. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013, 57:1333-1342.