A meta-analysis of epidemiological studies on the combined effect of hepatitis B and C virus infections in causing hepatocellular carcinoma

International Journal of Cancer

Volumn 75, Issue 3, 1998, Pages 347-354

  Donato, Francesco ^a   Boffetta, Paolo ^b   Puoti, Massimo ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B SURFACE ANTIGEN; HEPATITIS C ANTIBODY;

ADULT; AGED; ARTICLE; CANCER EPIDEMIOLOGY; CANCER RISK; CASE CONTROL STUDY; DISEASE ASSOCIATION; FEMALE; HEPATITIS B; HEPATITIS C; HUMAN; LIVER CELL CARCINOMA; MAJOR CLINICAL STUDY; MALE; META ANALYSIS; PRIORITY JOURNAL; STATISTICAL ANALYSIS; SUPERINFECTION; VIRUS CARCINOGENESIS;

ADULT; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; FEMALE; HEPACIVIRUS; HEPATITIS B; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HEPATITIS C; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; RISK FACTORS; RNA, MESSENGER;

EID: 0032579547     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0215(19980130)75:3<347::AID-IJC4>3.0.CO;2-2     Document Type: Article

References (89)

1. ADACHI, H., KANEKO, S., MATSUSHITA, E., INAGAKI, I., UNOURA, M. and KOBAYASHI, K., Clearance of HBsAg in seven patients with chronic hepatitis B. Hepatology, 16, 1334-1337 (1992).
2. AL KARAWI, M.A., SHARIQ, S., EL SHIEK MOHAMED, A.R., SAEED, A.A. and AHMED, A.M.M., Hepatitis-C-virus infection in chronic liver diseases and hepatocellular carcinoma in Saudi Arabia. J. Gastroenterol. Hepatol., 7, 237-239 (1992).
3. BENVEGNÙ, L., FATTOVICH, G., NOVENTA, F., TREMOLADA, F., CHEMELLO, L., CECCHETTO, A. and ALBERTI, A., Concurrent hepatitis-B and -C-virus infection and risk of hepatocellular carcinoma in cirrhosis. Cancer, 74, 2442-2448 (1994).
4. BILE, K., ADEN, C., NORDER, H., MAGNIUS, L., LINDBERG, G. and NILSSON, L., Important role of hepatitis-C-virus infection as a cause of chronic liver disease in Somalia. Scand. J. infect. Dis., 24, 559-564 (1993).
5. BLUM, H.E., Comments to: Does hepatitis-C virus cause hepatocellular carcinoma? Hepetology, 19, 251-258 (1994).
6. BRUIX, J., BARRERA, J.M., CALVET, X., ERCILLA, G., COSTA, J., SANCHEZ-TAPIAS, J.M., VENTURA, M., VALL, M., BRUGUERA, M., BRU, C., CASTILLO, R. and RODES, J., Prevalence of antibodies to hepatitis-C virus in Spanish with hepatocellular carcinoma and hepatic cirrhosis. Lancet, II, 1004-1006 (1989).
7. CENAC, A., PEDROSO, M.L., DJIBO, A., DEVELOUX, M., PICHOUD, C., LAMOTHE, F., TREPO, C. and WARTER, A., Hepatitis-B, -C and -D-virus infections in patients with chronic hepatitis, cirrhosis and hepatocellular carcinoma: a comparative study in Niger. Amer. J. trop. Med. Hyg., 52, 293-296 (1995).
8. CHANG, C.-C., YU, M.-W., LU, C.-F. YANG, C.-S. and CHEN, C.-J., A nested case-control study on association between hepatitis-C-virus antibodies and primary liver cancer in a cohort of 9,775 men in Taiwan. J. med. Virol., 43, 276-280 (1994).
9. CHEN, D.-S. and 13 OTHERS, Hepatitis-C-virus infection in an area hyperendemic for hepatitis B and chronic liver disease: the Taiwan experience. J. infect. Dis., 162, 817-822 (1990).
10. CHUANG, W.L., CHANG, W.Y., LU, S.N., SU, W.-P., LIN, Z.-Y., CHEN, S.-C., HSIEH, M.-Y., WANG, L.-Y., YOU, S.-L. and CHEN, C.-J., The role of hepatitis B and C viruses in hepatocellular carcinoma in a hepatitis-B endemic area. Cancer, 69, 2052-2054 (1992).
11. COLOMBO, M., Hepatocellular carcinoma. J. Hepatol., 15, 225-236 (1992).
12. COLOMBO, M., DE FRANCHIS, R., DEL NINNO, E., SANGIOVANNI, A., DE FAZIO, C., TOMMASINI, M., DONATO, M.F., PIVA, A., DI CARLO, V. and DIOGUARDI, N., Hepatocellular carcinoma in Italian patients with cirrhosis. New Engl. J. Med., 325, 675-680 (1991).
13. CORDIER, S., THUY, LTB., VERGER, P., BARD, D., DAI, C.L., LAROUZE, B., DAZZA, M.C., QUINH, H.T. and ABENHAIM, L., Risk factors for hepatocellular carcinoma in Vietnam. Int. J. Cancer, 55, 196-201 (1993).
14. COURSAGET, P., LEBOULLEUX, D., LE CANN, P., BAO, O. and COLL-SECK, M., Hepatitis-C-virus infection in cirrhosis and primary hepatocellular carcinoma in Senegal. Trans. roy. Soc. trop. Med. Hyg., 86, 552-553 (1992).
15. CRESPO, J., LOZANO, J.L., DE LA CRUZ, F., RODRIGO, L., RODRIGUEZ, M., SAN MIGUEL, G., ARTINANO, E. and PONS-ROMERO, F., Prevalence and significance of hepatitis-C viremia in chronic active hepatitis B. Amer. J. Gastroenterol., 89, 1147-1151 (1994).
16. DAMEN, M., CUYPERS, H.T., ZAAIJER, H.L., REESINK, H.W., SCHAASBERG, W.P., GERLICH, W.H., NIESTERS, H.G. and LELIE, P.N., International collaborative study on the second EUROHEP HCV/RNA reference panel. J. virol. Methods, 58, 175-185 (1996).
17. DAZZA, M.-C., MENESES, L.V., GIRARD, P-M., ASTAGNEU, P., VILLAROEL, C., DELAPORTE, E. and LAROUZE, B., Absence of a relationship between antibodies to hepatitis C and hepatocellular carcinoma in Mozambique. J. trop. Med. Hyg., 48, 237-242 (1993).
18. DE MITRI, M.S., POUSSIN, K., BACCARINI, P., PONTISSO, P., D'ERRICO, A., SIMON, N., GRIGIONI, W., ALBERTI, A., BEAUGRAND, M., PISI, E., BRECHOT, C. and PATERLINI, P., HCV-associated liver cancer without cirrhosis. Lancet, 345, 413-415 (1995).
19. DIAMANTIS, I.D., MCGANDY, C.E., CHEN, T.-J., LIAW, Y.-F., GUDAT, F. and BIANCHI, L., Detection of hepatitis-B and -C viruses in liver tissue with hepatocellular carcinoma. J. Hepatol., 20, 405-409 (1994).
20. DI BISCEGLIE, A.M., ORDER, S.E., KLEIN, J.L., WAGGONER, J.G., SJOGREN, M.H., KUO, G., HOUGHTON, M., CHOO, Q.-L. and HOOFNAGLE, J.H., The role of chronic viral hepatitis in hepatocellular carcinoma in the United States. Amer. J. Gastroenterol., 86, 335-338 (1991).
21. DONATO, F., TAGGER, A., CHIESA, R., RIBERO, M.L., TOMASONI, V., FASOLA, M., GELATTI, U., PORTERA, G., BOFFETTA, P. and NARDI, G., Hepatitis-B and -C-virus infection, alcohol drinking and heputocellular carcinoma: a case-control study in Italy. Hepatology, 26, 579-584 (1997).
22. EDAMOTO, Y., TANI, M., KURATA, T. and ABE, K., Hepatitis-C- and -B-virus infections in hepatocellular carcinoma. Cancer, 77, 1787-91 (1996).
23. FARCI, P., ALTER, H.J., WONG, D., MILLER, R.H., SHIH, J.W., JETT, B. and PURCELL, R.H., A long-term study of hepatitis-C-virus replication in non-A. non-B hepatitis. New Engl. J. Med. 325, 98-104 (1991).
24. FONG, T.-L., DI BISCEGLIE, A.M., GERBER, M.A., WAGGONER, J.G. and HOOFNAGLE, J.H., Persistence of hepatitis-B-virus DNA in the liver after loss of HBsAg in chronic hepatitis B. Hepatology, 18, 1313-1318 (1993).
25. FONG, T.-L., DI BISCEGLIE, A.M., WAGGONER, J.G., BANKS, S.M. and HOOFNAGLE, J.H., The significance of antibody to hepatitis-C virus in patients with chronic hepatitis B. Hepatology, 14, 64-67 (1991).
26. FUKUDA, K., SHIBATA, A., HIROHATA, I., TANIKAWA, K., YAMAGUCHI, G. and ISHII, M., A hospital-based case-control study on hepatocellular carcinoma in Fukuoka and Saga prefectures, northern Kyushu, Japan, Jap. J. Cancer Rev., 84, 708-714 (1993).
27. HADZIYANNIS, S., TABOR, E., KAKLAMANI, E., TZONOU, A., STUVER, S., TASSOPOULOS, N., MUELLER, N. and TRICHOPOULOS, D., A case-control study of hepatitis-B- and -C-virus infection in the aetiology of hepatocellular carcinoma. Int. J. Cancer, 60, 627-631 (1995).
28. HENKLER, F. and KOSHY, R., Hepatitis-B-virus transcriptional activators: mechanisms and possible role in oncogenesis. J. viral Hepatol., 3, 109-121 (1996).
29. IARC, Hepatitis viruses. IARC monographs on the evaluation of carcinogenic risks to humans, Vol. 59, IARC, Lyon (1994).
30. IKEDA, K., SAITOH, S., KOIDA, I., ARASE, Y., TSUBOTA, A., CHAYAMA, K., KUMADA, H. and KAWANISHI, M., A multivariate analysis of risk factors for hepatocellular carcinogenesis: a prospective observation of 795 patients with viral and alcoholic cirrhosis. Hepatology, 18, 47-53 (1993).
31. KACZYNSKI, J., HANSSON, G., HERMODSSON, S., OLSSON, R. and WALLERSTEDT, S., Minor role of hepatitis-B- and -C-virus infection in the etiology of hepatocellular carcinoma in a low-endemic area. Scand. J. Gastroenterol. 31, 809-813 (1996).
32. KAKLAMANI, E., TRICHOPOULOS, D., TZONOU, A., ZAVITSANOS, X., HATZAKIS, A., HSIEH, C.C. and HATZIYANNIS, S., Hepatitis-B and -C viruses and their interaction in the origin of hepatocellular carcinoma. J. Amer. med. Ass., 265, 1974-1976 (1991).
33. KATO, Y., NAKATA, K., OMAGARI, FURUKAWA, R., KUSUMOTO, Y., MORI, I., TAJIMA, H., TANIOKA, H., YANO, M. and NAGATAKI, S., Risk of hepatocellular carcinoma in patients with cirrhosis in Japan. Cancer, 74, 2234-2238 (1994).
34. KEW, M.C., Hepatitis-B and -C viruses and hepatocellular carcinoma. Clin. Lab. Med., 16, 395-406 (1996).
35. KEW, M.C., YU, M.C., KEDDA, M.-A., COPPIN, A., SARKIN, A. and HODKINSON, J., The relative roles of hepatitis-B and -C viruses in the etiology of hepatocellular carcinoma in Southern African Blacks. Gastroenterology, 112, 184-187 (1997).
36. KIM, C.-M., KOIKE, K., SAITO, I., MIYAMURA, T. and JAY, G., HBx gene of hepatitis-B virus induces liver cancer in transgenic mice. Nature (Lond.), 351, 317-320 (1991).
37. KOIKE, K., YASUDA, K., YOTSUYANAGI, H., MORIYA, K., HINO, K., KUROKAWA, K. and IINO, S., Dominant replication of either virus in dual infection with hepatitis viruses B and C. J. med. Virol., 45, 236-239 (1995).
38. LAI, M.-Y., CHEN, P.-J., YANG, P.-M., SHEU, J.-C., SUNG, J.-L. and CHEN, D.-S., Identification and characterisation of intrahepatic hepatitis-B-virus DNA in HBsAg-seronegative patients with chronic liver disease and hepatocellular carcinoma in Taiwan. Hepatology, 12, 575-581 (1990).
39. LIANG, T.J., JEFFERS, L.J., REDDY, K.R., DE MEDINA, M., PARKER, I.T., CHEINQUER, H., IDROVO, V., RABASSA, A. and SCHIFF, E.R., Viral pathogenesis of hepatocellular carcinoma in the United States. Hepatology, 18, 1326-1333 (1993).
40. LIAW, Y.-F., Role of hepatitis-C virus in dual and triple hepatitis-virus infection. Hepatology, 22, 1101-1108 (1995).
41. MANDELL, G.L., DOUGLAS, R.G. and BENNETT, J.E., Principles and practice of infectious diseases. Churchill Livingstone, New York (1995).
42. MEHTA, C. and PATEL, N., StatXact-Turbo, statistical software for exact non-parametric inference. CYTEL Software, Cambridge. MA (1992).
43. NOMURA, A., STEMMERMANN, G.N., CHYOU, P.-H. and TABOR, E., Hepatitis-B- and -C-virus serologies among Japanese Americans with hepatocellular carcinoma. J. infect. Dis., 173, 1474-1476 (1996).
44. OKUNO, H., XIE, Z.-C., LU, B.-Y., QUIN, X., TAKASU, M., KANO, H., SHIOZAKI, Y. and INOUE, K., A low prevalence of anti-hepatitis-C-virus antibody in patients with hepatocellular carcinoma in Guangxi province, Southern China. Cancer, 73, 58-62 (1994).
45. PARK, B.C., HAN, B.H., AHN, S.Y. LEE, S.W., LEE, D.H., LEE, Y.N., SEO, J.H. and KIM, K.W., Prevalence of hepatitis-C antibody in patients with chronic liver disease and hepatocellular carcinoma in Korea. J. viral Hepatol., 2, 195-202 (1995).
46. PATERLINI, P. and BRECHOT, C., Hepatitis-B virus and primary liver cancer in hepatitis-B-surface-antigen-positive and -negative patients. Prog. Hepatol., 81-104 (1994).
47. PATERLINI, P., DRISS, F., NALPAS, B., PISI, E., FRANCO, D., BERTHELOT, P. and BRECHOT, C., Persistence of hepatitis-B- and hepatitis-C-viral genomes in primary liver cancer from HBsAg-negative patients: a study of a lowendemic area. Hepatology. 17, 20-29 (1993).
48. PATERLINI, P. and 12 OTHERS, Polymerase chain reaction to detect hepatitis-B-virus-DNA and -RNA sequences in primars liver cancer from patients negative for hepatitis-B surface antigen. New Engl. J. Med., 323, 80-85 (1990).
49. PATERLINI, P., POUSSIN, K., KEW, M.C., FRANCO, D. and BRECHOT, C., Selective accumulation of the X transcript of hepatitis-B virus in patients negative for hepatitis-B surface antigen with hepatocellular carcinoma. Hepatology, 21, 313-321 (1995).
50. PETITTI, D.B., Meta-analysis, decision analysis and cost-effectiveness analysis. Oxford University Press, Neu York (1994).
51. PONTISSO, P., RUVOLETTO, M.G., FATTOVICH, G., CHEMELLO, L., GALLORINI, A., RUOL, A. and ALBERTI, A., Clinical and virological profiles in patients with multiple hepatitis-virus infections. Gastroenterology, 105, 1529-1533 (1993).
52. PYONG, S.J., TSUKUMA, H. and HIYAMA, T., Case-control study of hepatocellular carcinoma among Koreans living in Osaka, Japan. Jap. J. Cancer Res., 85, 674-679 (1994).
53. RAY, R.B., LAGGING, L.M., MEYER, K., STEELE, R. and RAY, R., Transcriptional regulation of cellular and viral promoters by the hepatitis-C-virus core protein. Virus Res., 37, 209-220 (1995).
54. RAY, R.B., LAGGING, L.M., MEVER, K. and RAY, R., Hepatitis-C-virus core protein cooperates with ras and transforms primary rat-embryo fibroblasts to tumorigenic phenotype. J. Virol., 70, 4438-4443 (1996).
55. RESNICK, R.H. and KOFF, R., Hepatitis-C-related hepatocellular carcinoma. Arch. intern. Med., 153, 1672-1677 (1993).
56. ROTHMAN, K.J., Modern epidemiology. Little, Brown, Boston (1986).
57. RUIZ, J., SANGRO, B., CUENDE, J.I., BELOQUI, O., RIEZU-BOJ, J.I., HERRERO, J.I. and PRIETO, J., Hepatitis-B- and -C-viral infections in patients with HCC. Hepatology, 16, 637-641 (1992).
58. SAITO, I. and 12 OTHERS, Hepatitis-C-virus infection is associated with the development of hepatocellular carcinoma. Proc. nat. Acad. Sci. (Wash.), 87, 6547-6549 (1990).
59. SAKAMURO, D., FURUKAWA, T. and TAKEGAMI, T., Hepatitis-C-virus nonstructural protein NS3 transforms NIH 3T3 cells. J. Virol., 69, 3893-3896 (1995).
60. SHARARA, A.I., HUNT, C.M. and HAMILTON, J.D., Hepatitis C. Ann. intern. Med., 125, 658-668 (1996).
61. SHEU, J.-C., HUANG, G.-T., SHIH, L.-N., LEE, W.-C., CHOU, H.-C., WANG, J.-T., LEE, P.-H., LAI, M.-Y., WANG, C.-Y., YANG, P.-M., LEE, H.-S. and CHEN, D.-S., Hepatitis-C and -B viruses in hepatitis-B-surface-antigen-negative hepatocellular carcinoma. Gastroenterology, 103, 1322-1327 (1992).
62. SHIH, C.M., LO, S.J., MIYAMURA, T., CHEN, S.Y. and LEE, Y.H., Suppression of hepatitis-B-virus expression and replication by hepatitis-C-virus core protein in HuH-7 cells. J. Virol., 67, 5823-5832 (1993).
63. SHIN, H.R., LEE, C.-U., PARK, H.-J., SEOL, S.-Y. CHUNG, J.-M., CHOI, H.-C., AHN, Y.-O. and SHIGEMATSU, T., Hepatitis-B and -C virus. Clonorchis sinensis for the risk of liver cancer: a case-control study in Pusan, Korea. Int. J. Epidemiol. 25, 933-940 (1996).
64. SIMONETTI, R.G., CAMMÀ, C., FIORELLO, F., COTTONE, M., RAPICETTA, M., MARINO, L., FIORENTINO, G., CRAXI', A., CICCAGLIONE, A., GIUSEPPETTI, R., STROFFOLINI, T. and PAGLIARO, L., Hepatitis-C-virus infection as a risk factor for hepatocellular carcinoma in patients with cirrhosis: a case-control study. Ann. intern. Med., 116, 97-102 (1992).
65. STROFFOLINI, T., CHIARAMONTE, M., TIRIBELLI, C., VILLA, E., SIMONETTI, R.G., RAPICETTA, M., STAZI, M.A., BERTIN, T., CROCE, S.L., TRANDE, P., MAGLIOCCO, A. and CHIONNE, P., Hepatitis-C-virus infection, HBsAgcarrier state and hepatocellular carcinoma: relative risk and population attributable risk from a case-control study in Italy. J. Hepatol., 16, 360-363 (1992).
66. SUN, C.-A., FARZADEGAN, H., YOU, S.-L., LU, S.-N., WU, M.-H., WOLFE, L., HARDY, W., HUANG, G.-T., YANG, P.-M., LEE, H.-S. and CHEN, C.-J., Mutual confounding and interactive effects between hepatitis-C- and hepatitis-B-viral infections in hepatocellular carcinogenesis: a population-based case-control study in Taiwan. Cancer Epidemiol. Bio. Prev., 5, 173-178 (1996).
67. TANAKA, K. and 14 OTHERS, Hepatitis C and hepatitis B in the etiology of hepatocellular carcinoma in the Japanese population. Cancer Res., 51, 2842-2847 (1991).
68. TANAKA, K., IKEMATSU, H., HIROHATA, T. and KASHIWAGI, S., Hepatitis-C-virus infection and risk of hepatocellular carcinoma among Japanese: possible role of Type-1b(II) infection. J. nat. Cancer Inst., 88, 742-746 (1996).
69. TANAKA, N., CHIBA, T., MATSUZAKI, Y. OSUGA, T. AIKAWA, T. and MITAMURA, K., High prevalence of hepatitis-B- and -C-viral markers in Japanese patients with hepatocellular carcinoma. Gastroenterol. jpn., 28, 547-553 (1993).
70. TANAKA, S., TAKENAKA, K., MATSUMATA, T., MORI, R. and SUGIMACHI, K., Hepatitis-C-virus replication is associated with expression of transforming growth factor-α and insulin-like growth factor-II in cirrhotic livers. Dig. Dis. Sci., 41, 208-215 (1996).
71. TSAI, J.-F., CHANG, W.-Y., JENG, J.-E., HO, M.-S., WANG, L.-Y., HSIEH, M.-Y., CHEN, S.-C., CHUANG, W.-L., LIN, Z.-Y. and TSAI, J.-H., Hepatitis-C-virus infection as a risk factor for non-alcoholic liver cirrhosis in Taiwan. J. med. Virol., 41, 296-300 (1993).
72. TSAI, J.-F., JENG, J.-F., CHANG, W.-Y., HSIEH, M.-Y., LIN, Z.-Y. and TSAI, J.-H., Additive effect modification of hepatitis-B surface antigen and e antigen on the development of hepatocellular carcinoma. Brit. J. Cancer, 73, l498-1502 (1996a).
73. TSAI, J.-F., JENG, J.-E., HO, M.-S., CHANG, W.-Y. LIN, Z.-Y. and TSAI, J.-H., Independent and additive effect modification of hepatilis-C- and -B-viruses infection on the development of chronic infection. J. Hepatol., 24, 271-276 (1996b).
74. TSEGA, E., NORDKNFELT, E. and HANSSON, B.C., Hepatitis-C-virus infection and chronic liver disease in Ethiopia where hepatitis-B infection is hyperendemic. Trans. roy. Soc. trop. Med. Hyg., 89, 171-174 (1995).
75. UNSAL, H., YAKICIER, C., MARCAIS, C., KEW, M., VOLKMAN, M., ZENTGRAF, H., ISSELBACHER, K.J. and OZTURK, M., Genetic heterogeneity of hepatocellular carcinoma. Proc. nat. Acad. Sci. (Wash.), 91, 822-826 (1994).
76. URASHIMA, T., SAIGO, K., KOBAYASHI, S., IMASEKI, H., MATSUBARA, H., KOIDE, Y., ASANO, T., KONDO, Y., KOIKE, K. and ISONO, K., Identification of hepatitis-B-virus integration in hepatitis-C-virus-infected hepatocellular-carcinoma tissues. J. Hepatol., 26, 771-778 (1997).
77. WAKED, I.A., SALEH, S.M., MOUSTAFA, M.S., RAOUF, A.A., THOMAS, D.L. and STRICKLAND, G.T., High prevalence of hepatitis C in Egyptian patients with chronic liver disease. Gut. 37, 105-107 (1995).
78. WANG, X.W., GIBSON, M.K., VERMEULEN, W., YEH, H., FORRESTER, K., STURZBECHER, H.-W., HOEIJMAKERS, J.H.J. and HARRIS, C.C., Abrogation of p53-induced apoptosis by the hepatitis-B-virus x gene. Cancer Res., 55, 6012-6016 (1995).
79. XU, Z., SHENG, F.-M., XU, Z.-Y. and WANG, Q.-S., Relationship between HCV infection and primary hepatocellular carcinoma (PHC). Tumor, 10, 115 (1990).
80. YANG, J.-Y., LI, R.-C., GONG, J., WANG, S.-S., LI, Y.-P. and NONG, Y., Hepatitis-B- and -C-viruses infection in patients with hepatocellular carcinoma in Guungxi region. China. IX Triennal International Symposium on Viral Hepatitis and Liver Disease, p. 304. CpA, Rome (1996). (Abstract).
81. YOUNOSSI, Z.M. and MCHUTUCHINSON, J.G., Serological tests for HCV infection. Viral Hep. Rev., 2, 161-173 (1996).
82. YU, M.C., YUAN, J.-M., ROSS, R.K. and GOVINDARAJAN, S., Presence of antibodies to the hepatitis-B surface antigen is associated with an excess risk for hepatocellular carcinoma among non-Asians in Los Angeles County, California. Hepatology, 25, 226-228 (1997).
83. YU, M.-W., YOU, S.-L., CHANG, A.-S., LU, S.-N., LIAW, Y.-F and CHEN, C.-J., Association between hepatitis-C-virus antibodies and hepatocellular carcinoma in Taiwan. Cancer Res., 51, 5621-5625 (1991).
84. YU, S.-Z., ZI, X.-L., CHEN, G. and LI, J., The relationship between viral hepatitis and primary liver cancer in four areas of China. Chin. J. Epidemiol. (1997) (In press).
85. YUAN, J.-M., ROSS, R.K., STANCZYK, F.Z., GOVINDARAJAN, S., GAO, Y.-T., HENDERSON, B.E. and YU, M.C., A cohort study of serum testosterone and hepatocellular carcinoma in Shangai. China. Int. J. Cancer, 63, 491-493 (1995).
86. ZAAIJER, H.L., CUYPERS, H.T.M., REESINK, H.W., WINKEL, I.N., GERKEN, G. and LELIE, P.N., Reliability of polymerase chain reaction for detection of hepatitis-C virus. Lancet, 341, 722-724 (1993).
87. ZAVITSANOS, X., HATZAKIS, A., KAKLAMANI, E., TZONOU, A., TOUPADAKI, N., BROEKSMA, C., CHRISPEELS, J., TROONEN, H., HADZIYANNIS, S., HSIEH, C.-C., ALTER, H. and TRICHOPOULOS, D., Association between hepatitis-C virus and hepatocellular carcinoma using assays based on structural and non-structural hepatitis-C-virus peptides. Cancer Res., 52, 5364-5367 (1992).
88. ZHANG, Y.-Y., HANSSON, B.G., KUO, L.S., WIDELL, A. and NORDENFELT, E., Hepatitis-B-Virus DNA in serum and liver is commonly found in Chinese patients with chronic liver disease despite the presence of antibodies to HBsAg. Hepatology, 17, 538-544 (1993).
89. ZOLI, M., MAGALOTTI, D., BIANCHI, G., GUELI, C., MARCHESINI, G. and PISI, E., Efficacy of a surveillance program for early detection of hepatocellular carcinoma. Cancer, 78, 977-985 (1996).