Battlefield against hepatitis B infection and HCC in Africa

Journal of Hepatology

Volumn 66, Issue 3, 2017, Pages 645-654

  Lemoine, Maud ^a   Thursz, Mark R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Africa; Antiviral agents; Cirrhosis; Global health; HBV; HCC; Immunization; Treatment

Indexed keywords

AFLATOXIN; HOST FACTOR; VACCINE; VIRUS DNA;

AFRICA; CANCER PALLIATIVE THERAPY; CHRONIC HEPATITIS B; DISEASE SURVEILLANCE; DRUG CONTROL; ENVIRONMENTAL FACTOR; EPIDEMIC; HEPATITIS B; HUMAN; INCIDENCE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MEDICAL HISTORY; MORTALITY RATE; PATIENT SELECTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; VACCINATION; VIREMIA; VIRUS TRANSMISSION; FEMALE; LIVER TUMOR; MALE; MASS SCREENING; NEWBORN; PREGNANCY; PREVENTION AND CONTROL; PREVENTIVE HEALTH SERVICE; VERTICAL TRANSMISSION;

AFRICA; CARCINOMA, HEPATOCELLULAR; EPIDEMICS; FEMALE; HEPATITIS B, CHRONIC; HUMANS; IMMUNIZATION PROGRAMS; INCIDENCE; INFANT, NEWBORN; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; LIVER NEOPLASMS; MALE; MASS SCREENING; PREGNANCY; RISK FACTORS;

EID: 85013499547     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.10.013     Document Type: Review

References (80)

1. [1] Stanaway, J.D., Flaxman, A.D., Naghavi, M., et al. The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013. Lancet 388 (2016), 1081–1088, 10.1016/S0140-6736(16)30579-7.
2. [2] IARC. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx, Last access 23 January 2016, 2012.
3. [3] Jemal, A., Bray, F., Forman, D., et al. Cancer burden in Africa and opportunities for prevention. Cancer 118 (2012), 4372–4384, 10.1002/cncr.27410 Review.
4. [4] Parkin, D.M., Sitas, F., Chirenje, M., Stein, L., Abratt, R., Wabinga, H., Part I: Cancer in Indigenous Africans–burden, distribution, and trends. Lancet Oncol 9 (2008), 683–692.
5. [5] Shimakawa, Y., Bah, E., Wild, C.P., Hall, A.J., Evaluation of data quality at the Gambia national cancer registry. Int J Cancer 132 (2013), 658–665.
6. [6] www.prolifica.org.uk NCT02129829 clinical trials org Last accessed 15 August 2016.
7. [7] Shimakawa, Y., Njai, H.F., Takahashi, K., et al. Hepatitis E virus infection and acute-on-chronic liver failure in West Africa: a case-control study from The Gambia. Aliment Pharmacol Ther 43 (2016), 375–384.
8. [8] Blachier, M., Leleu, H., Peck-Radosavljevic, M., Valla, D.C., Roudot-Thoraval, F., The burden of liver disease in Europe: a review of available epidemiological data. J Hepatol 58 (2013), 593–608.
9. [9] Kirk, G.D., Lesi, O.A., Mendy, M., et al. The Gambia Liver Cancer Study: Infection with hepatitis B and C and the risk of hepatocellular carcinoma in West Africa. Hepatology 39 (2004), 211–219.
10. [10] Yang, J.D., Gyedu, A., Afihene, M.Y., et al. Hepatocellular carcinoma occurs at an earlier age in Africans, particularly in association with chronic hepatitis B. Am J Gastroenterol 110 (2015), 1629–1631.
11. [11] de Martel, C., Maucort-Boulch, D., Plummer, M., Franceschi, S., World-wide relative contribution of hepatitis B and C viruses in hepatocellular carcinoma. Hepatology 62 (2015), 1190–1200.
12. [12] Shafritz, D.A., Shouval, D., Sherman, H.I., Hadziyannis, S.J., Kew, M.C., Integration of hepatitis B virus DNA into the genome of liver cells in chronic liver disease and hepatocellular carcinoma. Studies in percutaneous liver biopsies and post-mortem tissue specimens. N Engl J Med 305 (1981), 1067–1073.
13. [13] Kew, M.C., Welschinger, R., Viana, R., Occult hepatitis B virus infection in Southern African blacks with hepatocellular carcinoma. J Gastroenterol Hepatol 23 (2008), 1426–1430.
14. [14] Shaker, M.K., Abdella, H.M., Khalifa, M.O., El Dorry, A.K., Epidemiological characteristics of hepatocellular carcinoma in Egypt: a retrospective analysis of 1313 cases. Liver Int 33 (2013), 1601–1606.
15. [15] Andoulo, F.A., Noah, D.N., Djapa, R., et al. Epidemiology of hepatitis C: related hepatocellular carcinoma in Cameroon. Pan Afr Med J, 19, 2014, 379.
16. [16] Shi, Y., Wu, Y.H., Wu, W., Zhang, W.J., Yang, J., Chen, Z., Association between occult hepatitis B infection and the risk of hepatocellular carcinoma: a meta-analysis. Liver Int 32 (2012), 231–240.
17. [17] Schweitzer, A., Horn, J., Mikolajczyk, R.T., Krause, G., Ott, J.J., Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 386 (2015), 1546–1555, 10.1016/S0140-6736(15)61412-X Review.
18. [18] Whittle, H., Inskip, H., Bradley, A.K., et al. The pattern of childhood hepatitis B infection in two Gambian villages. J Infect Dis 161 (1990), 1112–1115.
19. [19] Lemoine, M., Shimakawa, Y., Njie, R., et al. Acceptability and feasibility of a screen-and-treat programme for hepatitis B virus infection in The Gambia: the Prevention of Liver Fibrosis and Cancer in Africa (PROLIFICA) study. Lancet Glob Health 4 (2016), e559–e567, 10.1016/S2214-109X(16)30130-9.
20. [20] Shimakawa, Y., Bottomley, C., Njie, R., Mendy, M., The association between maternal hepatitis B e antigen status, as a proxy for perinatal transmission, and the risk of hepatitis B e antigenaemia in Gambian children. BMC Public Health, 14, 2014, 532.
21. [21] Bernier, R.H., Sampliner, R., Gerety, R., Tabor, E., Hamilton, F., Nathanson, N., Hepatitis B infection in households of chronic carriers of hepatitis B surface antigen: factors associated with prevalence of infection. Am J Epidemiol 116 (1982), 199–211.
22. [22] Crook, P.D., Jones, M.E., Hall, A.J., Mortality of hepatitis B surface antigen-positive blood donors in England and Wales. Int J Epidemiol 32 (2003), 118–124.
23. [23] Chen, C.J., Yang, H.I., Su, J., et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 295 (2006), 65–73.
24. [24] Evans, A.A., O'Connell, A.P., Pugh, J.C., et al. Geographic variation in viral load among hepatitis B carriers with differing risks of hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev 7 (1998), 559–565.
25. [25] Shimakawa, Y., Lemoine, M., Njai, H.F., et al. Natural history of chronic HBV infection in West Africa: a longitudinal population-based study from The Gambia. Gut, 2015, 10.1136/gutjnl-2015-309892.
26. [26] Liaw, Y.F., Sung, J.J., Chow, W.C., et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 351 (2004), 1521–1531.
27. [27] Yang, H.I., Lu, S.N., Liaw, Y.F., et al. Hepatitis B e antigen and the risk of hepatocellular carcinoma. N Engl J Med 347 (2002), 168–174.
28. [28] Tang, B., Kruger, W.D., Chen, G., et al. Hepatitis B viremia is associated with increased risk of hepatocellular carcinoma in chronic carriers. J Med Virol 72 (2004), 35–40.
29. [29] Kew, M.C., Kramvis, A., Yu, M.C., Arakawa, K., Hodkinson, J., Increased hepatocarcinogenic potential of hepatitis B virus genotype A in Bantu-speaking sub-saharan Africans. J Med Virol 75 (2005), 513–521.
30. [30] Yousif, M., Mudawi, H., Hussein, W., et al. Genotyping and virological characteristics of hepatitis B virus in HIV-infected individuals in Sudan. Int J Infect Dis 29 (2014), 125–132.
31. [31] Shimakawa, Y., Lemoine, M., Bottomley, C., et al. Birth order and risk of hepatocellular carcinoma in chronic carriers of hepatitis B virus: a case-control study in The Gambia. Liver Int 35 (2015), 2318–2326, 10.1111/liv.12814.
32. [32] Liu, Y., Chang, C.C., Marsh, G.M., Wu, F., Population attributable risk of aflatoxin-related liver cancer: systematic review and meta-analysis. Eur J Cancer 48 (2012), 2125–2136.
33. [33] Montella, M., D'Arena, G., Crispo, A., et al. Role of sex hormones in the development and progression of hepatitis B virus-associated hepatocellular carcinoma. Int J Endocrinol, 2015, 2015, 854530.
34. [34] Bhaskaran, K., Douglas, I., Forbes, H., dos-Santos-Silva, I., Leon, D.A., Smeeth, L., Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5.24 million UK adults. Lancet 384 (2014), 755–765.
35. [35] Chen, C.L., Yang, H.I., Yang, W.S., et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan. Gastroenterology 135 (2008), 111–121.
36. [36] WHO. http://appswhoint/iris/bitstream/10665/112736/1/9789240692763_engpdf, Last access 28th January, 2016.
37. [37] Hall, A.J., Roberston, R.L., Crivelli, P.E., et al. Cost-effectiveness of hepatitis B vaccine in The Gambia. Trans R Soc Trop Med Hyg 87 (1993), 333–336.
38. [38] Beutels, P., Economic evaluations of hepatitis B immunization: a global review of recent studies (1994–2000). Health Econ 10 (2001), 751–774.
39. [39] WHO. http://www.who.int/immunization/monitoring_surveillance/Global_Immunization_Data.pdf?ua=1, Last accessed 1st February 2016, 2015.
40. [40] Chen, D.S., Hsu, N.H., Sung, J.L., et al. A mass vaccination program in Taiwan against hepatitis B virus infection in infants of hepatitis B surface antigen-carrier mothers. JAMA 257 (1987), 2597–2603.
41. [41] Hsu, H.M., Chen, D.S., Chuang, C.H., et al. Efficacy of a mass hepatitis B vaccination program in Taiwan. Studies on 3464 infants of hepatitis B surface antigen-carrier mothers. JAMA 260 (1988), 2231–2235.
42. [42] Hsu, H.M., Lu, C.F., Lee, S.C., Lin, S.R., Chen, D.S., Seroepidemiologic survey for hepatitis B virus infection in Taiwan: the effect of hepatitis B mass immunization. J Infect Dis 179 (1999), 367–370.
43. [43] Harpaz, R., McMahon, B.J., Margolis, H.S., et al. Elimination of new chronic hepatitis B virus infections: results of the Alaska immunization program. J Infect Dis 181 (2000), 413–418.
44. [44] Liang, X., Bi, S., Yang, W., et al. Epidemiological serosurvey of hepatitis B in China–declining HBV prevalence due to hepatitis B vaccination. Vaccine 27 (2009), 6550–6557.
45. [45] The Gambia Hepatitis Intervention Study, The Gambia Hepatitis Study Group. Cancer Res 47 (1987), 5782–5787.
46. [46] Peto, T.J., Mendy, M.E., Lowe, Y., Webb, E.L., Whittle, H.C., Hall, A.J., Efficacy and effectiveness of infant vaccination against chronic hepatitis B in the Gambia Hepatitis Intervention Study (1986–90) and in the nationwide immunisation program. BMC Infect Dis, 14, 2014, 7.
47. [47] Rey-Cuille, M.A., Njouom, R., Bekondi, C., et al. Hepatitis B virus exposure during childhood in Cameroon, Central African Republic and Senegal after the integration of HBV vaccine in the expanded program on immunization. Pediatr Infect Dis J 32 (2013), 1110–1115.
48. [48] Chang, M.H., Chen, C.J., Lai, M.S., et al. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N Engl J Med 336 (1997), 1855–1859.
49. [49] Chiang, C.J., Yang, Y.W., You, S.L., Lai, M.S., Chen, C.J., Thirty-year outcomes of the national hepatitis B immunization program in Taiwan. JAMA 310 (2013), 974–976.
50. [50] Chien, Y.C., Jan, C.F., Chiang, C.J., Kuo, H.S., You, S.L., Chen, C.J., Incomplete hepatitis B immunization, maternal carrier status, and increased risk of liver diseases: a 20-year cohort study of 3.8 million vaccinees. Hepatology 60 (2014), 125–132.
51. [51] Wichajarn, K., Kosalaraksa, P., Wiangnon, S., Incidence of hepatocellular carcinoma in children in Khon Kaen before and after national hepatitis B vaccine program. Asian Pac J Cancer Prev 9 (2008), 507–509.
52. [52] Hadler, S.C., Fuqiang, C., Averhoff, F., et al. The impact of hepatitis B vaccine in China and in the China GAVI Project. Vaccine 31 (2013), J66–J72.
53. [53] Edmunds, W.J., Medley, G.F., Nokes, D.J., Hall, A.J., Whittle, H.C., The influence of age on the development of the hepatitis B carrier state. Proc Biol Sci 253 (1993), 197–201.
54. [54] WHO, Hepatitis B vaccines. WHO position paper. Wkly Epidemiol Rec 84 (2009), 405–420.
55. [55] GAVI. Hepatitis B vaccine at birth GAVI responds to MSF, 2014. Available at: http://www.gavi.org/Library/News/Statements/2014/Hepatitis-B-vaccine-at-birth-GAVI-responds-to-MSF/, 2014.
56. [56] Ekra, D., Herbinger, K.H., Konate, S., et al. A non-randomized vaccine effectiveness trial of accelerated infant hepatitis B immunization schedules with a first dose at birth or age 6 weeks in Cote d'Ivoire. Vaccine 26 (2008), 2753–2761.
57. [57] WHO. World Health Organization. Guidelines for the Prevention, Care and Treatment of Persons with chronic Hepatitis B infection. http://whoint/hiv/pub/hepatitis/hepatitis-b-guidelines/en/2015; March, Last accessed July 2016.
58. [58] Brown, R.S. Jr., McMahon, B.J., Lok, A.S., et al. Antiviral therapy in chronic hepatitis B viral infection during pregnancy: A systematic review and meta-analysis. Hepatology 63 (2016), 319–333.
59. [59] Marcellin, P., Gane, E., Buti, M., et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet, 2012, 10.1016/S0140-6736(12)61425-1.
60. [60] Wu, C.Y., Lin, J.T., Ho, H.J., et al. Association of nucleos(t)ide analogue therapy with reduced risk of hepatocellular carcinoma in patients with chronic hepatitis B – a nationwide cohort study. Gastroenterology, 2014 PubMed PMID: 24704525. Epub 2014/04/08. Eng.
61. [61] Papatheodoridis, G.V., Chan, H.L., Hansen, B.E., Janssen, H.L., Lampertico, P., Risk of hepatocellular carcinoma in chronic hepatitis B: Assessment and modification with current antiviral therapy. J Hepatol, 2015 PubMed PMID: 25595883.
62. [62] Buti, M., Brosa, M., Casado, M.A., Rueda, M., Esteban, R., Modeling the cost-effectiveness of different oral antiviral therapies in patients with chronic hepatitis B. J Hepatol 51 (2009), 640–646.
63. [63] Lemoine, M., Eholie, S., Lacombe, K., Reducing the neglected burden of viral hepatitis in Africa: Strategies for a global approach. J Hepatol 62 (2015), 469–476.
64. [64] Nayagam, S., Conteh, L., Sicuri, E., et al. Cost-effectiveness of community-based screening and treatment for chronic hepatitis B in The Gambia: an economic modelling analysis. Lancet Glob Health 4 (2016), e568–e578.
65. [65] Nyan, D.C., Ulitzky, L.E., Cehan, N., et al. Rapid detection of hepatitis B virus in blood plasma by a specific and sensitive loop-mediated isothermal amplification assay. Clin Infect Dis 59 (2014), 16–23.
66. [66] Lemoine, M., Shimakawa, Y., Nayagam, S., et al. The gamma-glutamyl transpeptidase to platelet ratio (GPR) predicts significant liver fibrosis and cirrhosis in patients with chronic HBV infection in West Africa. Gut, 2015, 10.1136/gutjnl-2015-309260.
67. [67] Shimakawa, Y., Bonnard, P., El Kassas, M., Abdel-Hamid, M., Esmat, G., Fontanet, A., Diagnostic accuracy of the γ-glutamyl transpeptidase to platelet ratio to predict liver fibrosis in Egyptian patients with HCV genotype 4. Gut 65 (2016), 1577–1578, 10.1136/gutjnl-2016-312326.
68. [68] Boyd, A., Bottero, J., Lacombe, K., The gamma-glutamyl transpeptidase-to-platelet ratio as a predictor of liver fibrosis in patients co-infected with HBV and HIV. Gut, 2015, 10.1136/gutjnl-2015-310607.
69. [69] Stockdale, A.J., Phillips, R.O., Geretti, A.M., HEPIK Study Group. The gamma-glutamyl transpeptidase to platelet ratio (GPR) shows poor correlation with transient elastography measurements of liver fibrosis in HIV-positive patients with chronic hepatitis B in West Africa. Response to: ‘The gamma-glutamyl transpeptidase to platelet ratio (GPR) predicts significant liver fibrosis and cirrhosis in patients with chronic HBV infection in West Africa’ by Lemoine et al. Gut, 2016, 10.1136/gutjnl-2015-311133.
70. [70] Han, K.H., Kim do, Y., Park, J.Y., et al. Survival of hepatocellular carcinoma patients may be improved in surveillance interval not more than 6 months compared with more than 6 months: a 15-year prospective study. J Clin Gastroenterol 47 (2013), 538–544.
71. [71] Trinchet, J.C., Chaffaut, C., Bourcier, V., et al. Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: a randomized trial comparing 3- and 6-month periodicities. Hepatology 54 (2011), 1987–1997.
72. [72] Davila, J.A., Henderson, L., Kramer, J.R., et al. Utilization of surveillance for hepatocellular carcinoma among hepatitis C virus-infected veterans in the United States. Ann Intern Med 154 (2011), 85–93.
73. [73] Daniele, B., Bencivenga, A., Megna, A.S., Tinessa, V., Alpha-fetoprotein and ultrasonography screening for hepatocellular carcinoma. Gastroenterology 127 (2004), S108–S112.
74. [74] Ladep, N.G., Dona, A.C., Lewis, M.R., et al. Discovery and validation of urinary metabotypes for the diagnosis of hepatocellular carcinoma (HCC) in West Africans. Hepatology 60 (2014), 1291–1301, 10.1002/hep.27264.
75. [75] Shimakawa, Y., Takao, Y., Anderson, S.T., et al. The prevalence and burden of symptoms in patients with chronic liver diseases in The Gambia, West Africa. Palliat Med 29 (2015), 184–185.
76. [76] Colebunders, R., John, L., Muganzi, A., Lynen, L., Kambugu, A., Palliative care in sub-Saharan Africa. Lancet 366 (2005), 546–547.
77. [77] Magnussen, A., Parsi, M.A., Aflatoxins, hepatocellular carcinoma and public health. World J Gastroenterol 19 (2013), 1508–1512.
78. [78] Wild, C.P., Hall, A.J., Primary prevention of hepatocellular carcinoma in developing countries. Mutat Res 462 (2000), 381–393.
79. [79] Kao, J.H., Chen, D.S., Global control of hepatitis B virus infection. Lancet Infect Dis 2 (2002), 395–403.
80. [80] World Health Organization (WHO). http://www.worldhepatitissummit.org/docs/default-source/default-document-library/2015/resources/towards-elimination-dr-gottfried-hirnschall.pdf?sfvrsn=6; 2016 June, Last accessed 23th Nov 2016.