Incidence and Cofactors of Hepatitis C Virus-related Hepatocellular Carcinoma: A Prospective Study of 12,008 Men in Taiwan
Open accessAbstract
In a community-based prospective study, the authors examined the independent and interactive effects of hepatitis C virus (HCV) infection and cofactors, including hepatitis B virus (HBV) infection and lifestyle habits, on the incidence of hepatocellular carcinoma (HCC) in Taiwan. At baseline recruitment, subjects were evaluated with regard to second-generation HCV antibody (anti-HCV), hepatitis B surface antigen, and serum alanine aminotransferase, as well as cigarette smoking, alcohol drinking, and betel quid chewing habits. A total of 12,008 male residents aged 30-64 years without a history of HCC were included in the study. Between July 1990 and June 2001, 112 incident cases of HCC were identified among the subjects and included in the analysis. Persons with anti-HCV positivity alone had a 20-fold increased risk of developing HCC in comparison with those who were negative for anti-HCV. In statistical assessment of additive interaction, HCV and HBV tended to act independently in the pathogenesis of HCC. The results of this study suggest that HCV plays a significant role in hepatocarcinogenesis in an area endemic for chronic HBV infection.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Exposure fractions among prevalent liver cirrhosis cases were used as a proxy for population attributable fractions, following the direct method when relative risk is high.
“We used the resulting predicted exposure fractions among prevalent cases as a proxy for PAFs for liver cirrhosis. This follows from the direct method of approximating PAFs:”
From Liver cirrhosis mortality in 187 countries between 1980 and 2010: a systematic analysis (2014) · cites this paper as [32]
Cites
Cancer Epidemiology and Prevention
Schottenfeld, D. (2006) · doi:10.1093/acprof:oso/9780195149616.001.0001 · Cited by 3,376 · see citing works
Epidemiologic Research: Principles and Quantitative Methods.
Mayer, L. S., Kleinbaum, D. G., Kupper, L. L., & Morgenstern, H. (1984) · Journal of the American Statistical Association · doi:10.2307/2288427 · Cited by 2,905 · see citing works
Rising Incidence of Hepatocellular Carcinoma in the United States
El‐Serag, H. B., & Mason, A. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199903113401001 · Cited by 2,865 · see citing works
Nonparametric Inference for a Family of Counting Processes
Aalen, O. O. (1978) · The Annals of Statistics · doi:10.1214/aos/1176344247 · Cited by 1,505 · see citing works
Confidence interval estimation of interaction
Hosmer, D. W., & Lemeshow, S. (1992) · Epidemiology · doi:10.1097/00001648-199209000-00012 · Cited by 1,239 · see citing works
Hepatitis B e Antigen and the Risk of Hepatocellular Carcinoma
Yang, H., Lu, S., Liaw, Y., You, S., Sun, C., Wang, L., Hsiao, C. K., Chen, P., Chen, D., & Chen, C. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa013215 · Cited by 1,220 · see citing works
Self-citationYoshida, H., Shiratori, Y., Moriyama, M., Arakawa, Y., Ide, T., Sata, M., INOUE, O., Yano, M., Tanaka, M., Fujiyama, S., et al. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-131-3-199908030-00003 · Cited by 1,096 · see citing works
Occult papillary carcinoma of the thyroid. A “normal” finding in finland. A systematic autopsy study
Harach, H. R., Franssila, K., & Wasenius, V.-M. (1985) · Cancer · doi:10.1002/1097-0142(19850801)56:3 · Cited by 939 · see citing works
Significance of serum hepatitis C virus RNA levels in chronic hepatitis C
Lau, J. Y. N., Davis, G. L., Kniffen, J. C., et al. (1993) · The Lancet · doi:10.1016/0140-6736(93)90635-t · Cited by 815 · see citing works
Prevalence of chronic liver disease in the general population of northern Italy: The dionysos study
Bellentani, S., Tiribelli, C., Saccoccio, G., Sodde, M., Fratti, N., Martin, C. D., & Christianini, G. (1994) · Hepatology · doi:10.1002/hep.1840200611 · Cited by 515 · see citing works
Hepatitis C Virus Type 1b (II) Infection in France and Italy
Nousbaum, J., Pol, S., Nalpas, B., et al. (1995) · Annals of Internal Medicine · doi:10.7326/0003-4819-122-3-199502010-00001 · Cited by 497 · see citing works
Epidemiological characteristics and risk factors of hepatocellular carcinoma
CHEN, C., YU, M., & LIAW, Y. (1997) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.1997.tb00513.x · Cited by 470 · see citing works
Risk Factors for the Rising Rates of Primary Liver Cancer in the United States
El‐Serag, H. B., & Mason, A. C. (2000) · Archives of Internal Medicine · doi:10.1001/archinte.160.21.3227 · Cited by 418 · see citing works
Changing incidence of hepatocellular carcinoma in Japan.
Okuda, K., Fujimoto, I., Hanai, A., & Urano, Y. (1987) · PubMed · Cited by 328 · see citing works
Chen, D., Kuo, G. C., Sung, J. L., et al. (1990) · The Journal of Infectious Diseases · doi:10.1093/infdis/162.4.817 · Cited by 326 · see citing works
HCV-associated liver cancer without cirrhosis
Mitri, M. S. D., Pisi, E., Poussin, K., Paterlini-Bréchot, P., Bréchot, C., Baccarini, P., D’Errico, A., Grigiani, W., Alberti, A., Pontisso, P., et al. (1995) · The Lancet · doi:10.1016/s0140-6736(95)90400-x · Cited by 292 · see citing works
Yu, M., Hsu, F.-C., Sheen, I. S., Chu, C., Lin, D., Chen, C., & Liaw, Y. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009060 · Cited by 289 · see citing works
Kato, N., Yokosuka, O., Hosoda, K., et al. (1993) · Hepatology · doi:10.1002/hep.1840180104 · Cited by 256 · see citing works
Shakil, A., Conry‐Cantilena, C., Alter, H. J., Hayashi, P. H., Kleiner, D. E., Tedeschi, V., Krawczyński, K., Conjeevaram, H. S., Sallie, R., Bisceglie, A. M. D., et al. (1995) · Annals of Internal Medicine · doi:10.7326/0003-4819-123-5-199509010-00002 · Cited by 254 · see citing works
Hepatitis C virus antibodies in southern African blacks with hepatocellular carcinoma
Kew, M. C., Houghton, M., Choo, Q. L., & Kuo, G. C. (1990) · The Lancet · doi:10.1016/0140-6736(90)90474-j · Cited by 251 · see citing works
Chen, C., Liang, K., Chang, A.-S., Chang, Y.-C., Lu, S., Liaw, Y., Chang, W., Sheen, M., & Lin, T.-M. (1991) · Hepatology · doi:10.1002/hep.1840130303 · Cited by 245 · see citing works
Gretch, D. R., Corey, L., Wilson, J. L., et al. (1994) · The Journal of Infectious Diseases · doi:10.1093/infdis/169.6.1219 · Cited by 215 · see citing works
Hepatitis B and C Viruses and Their Interaction in the Origin of Hepatocellular Carcinoma
Kaklamani, E. (1991) · JAMA · doi:10.1001/jama.1991.03460150078027 · Cited by 198 · see citing works
Hepatitis C and hepatitis B in the etiology of hepatocellular carcinoma in the Japanese population.
Tanaka, K., Hirohata, T., Koga, S., Sugimachi, K., Kanematsu, T., Ohryohji, F., Nawata, H., Ishibashi, H., Maeda, Y., & Kiyokawa, H. (1991) · PubMed · Cited by 197 · see citing works
Yu, M. C., Henderson, B. E., Tong, M. J., & Govindarajan, S. (1991) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/83.24.1820 · Cited by 190 · see citing works
Yu, M., Yang, Y., Yang, S.-Y., Cheng, S., Liaw, Y., Lin, S., & Chen, C. (2001) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/93.21.1644 · Cited by 183 · see citing works
Hepatitis C virus genotypes and risk of hepatocellular carcinoma in cirrhosis: A case-control study
Silini, E. M., Bottelli, R., Asti, M., et al. (1996) · Gastroenterology · doi:10.1053/gast.1996.v111.pm8698200 · Cited by 180 · see citing works
Hagiwara, H., Hayashi, N., Mita, E., Naito, M., Kasahara, A., Fusamoto, H., & Kamada, T. (1993) · Hepatology · doi:10.1002/hep.1840170404 · Cited by 179 · see citing works
Yu, M. C., Tong, M. J., Coursaget, P., Ross, R. K., Govindarajan, S., & Henderson, B. E. (1990) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/82.12.1038 · Cited by 175 · see citing works
Benvegnù, L. (1997) · Hepatology · doi:10.1053/jhep.1997.v25.pm0008985292 · Cited by 152 · see citing works
Pozzato, G., Kaneko, S., Moretti, M., et al. (1994) · Journal of Medical Virology · doi:10.1002/jmv.1890430318 · Cited by 151 · see citing works
Relationship of aminotransferases to liver histological status in chronic hepatitis C.
Haber, M. M., Ab, W., Ad, H., & Reuben, A. (1995) · PubMed · Cited by 149 · see citing works
Mori, M., Hara, M., Wada, I., Hara, T., Yamamoto, K., Honda, M., & Naramoto, J. (2000) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a010180 · Cited by 144 · see citing works
Hepatitis B and C viruses in the development of hepatocellular carcinoma
Yu, M., & Chen, C. (1994) · Critical Reviews in Oncology/Hematology · doi:10.1016/1040-8428(94)90020-5 · Cited by 137 · see citing works
Association between hepatitis C virus antibodies and hepatocellular carcinoma in Taiwan.
Yu, M., You, S., Chang, A. S., Lu, S.-N., Liaw, Y., & Chen, C. (1991) · PubMed · Cited by 136 · see citing works
Association between HCV and HBV infection in hepatocellular carcinoma and alcoholic liver disease
Nalpas, B., Driss, F., Pol, S., et al. (1991) · Journal of Hepatology · doi:10.1016/0168-8278(91)90912-u · Cited by 126 · see citing works
Oshima, A., Tsukuma, H., Hiyama, T., et al. (1984) · International Journal of Cancer · doi:10.1002/ijc.2910340607 · Cited by 104 · see citing works
Hadziyannis, S. J., Tabor, E., Kaklamani, E., et al. (1995) · International Journal of Cancer · doi:10.1002/ijc.2910600510 · Cited by 85 · see citing works
Betel quid chewing as a risk factor for hepatocellular carcinoma: a case–control study
Tsai, J., Chuang, L., Jeng, J., et al. (2001) · British Journal of Cancer · doi:10.1054/bjoc.1999.1597 · Cited by 83 · see citing works
Chen, K. T., Chen, C., Fagot‐Campagna, A., & Narayan, K. M. V. (2001) · American Journal of Public Health · doi:10.2105/ajph.91.7.1130 · Cited by 80 · see citing works
Hirayama, T. T. (1989) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00647254 · Cited by 63 · see citing works
Current therapeutic trends in therapy for chronic viral hepatitis
Liaw, Y. (1997) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.1997.tb00520.x · Cited by 54 · see citing works
Sun, C., Farzadegan, H., You, S., Lu, S., Wu, M. H., Wolfe, L., Hardy, W., Huang, G., Yang, P., Lee, H., et al. (1996) · PubMed · Cited by 35 · see citing works
Self-citationGenotypes of hepatitis C virus in chronic liver disease in Taiwan
Chen, C., Sheu, J., Wang, J., et al. (1994) · Journal of Medical Virology · doi:10.1002/jmv.1890440304 · Cited by 35 · see citing works
Hadziyannis, S. J., Giannoulis, G., Hadziyannis, E. S., et al. (1993) · Journal of Hepatology · doi:10.1016/s0168-8278(05)80428-3 · Cited by 34 · see citing works
[Community-based hepatocellular carcinoma screening in seven townships in Taiwan].
Cj, C., Sn, L., Sl, Y., et al. (1995) · PubMed · Cited by 30 · see citing works
Small sample and efficiency results for the Nelson-Aalen estimator
Peña, E. A., & Rohatgi, V. K. (1993) · Journal of Statistical Planning and Inference · doi:10.1016/0378-3758(93)90088-n · Cited by 15 · see citing works
Serum Hepatitis C Virus Titers in the Progression of Type C Chronic Liver Disease
Kao, J., Lai, M., Chen, P., et al. (1996) · Journal of Clinical Gastroenterology · doi:10.1097/00004836-199612000-00008 · Cited by 9 · see citing works
The incidence of pediatric cancer in Florida, 1981 to 1986
Roush, S. W., Krischer, J. P., Pollock, N. C., Cox, M. W., Pollock, B. H., & Buyer, J. (1992) · Cancer · doi:10.1002/1097-0142(19920415)69:8 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Liver cirrhosis mortality in 187 countries between 1980 and 2010: a systematic analysis
Mokdad, A. A., Lopez, A. D., Shahraz, S., Lozano, R., Mokdad, A. H., Stanaway, J., Murray, C. J., & Naghavi, M. (2014) · BMC Medicine · doi:10.1186/s12916-014-0145-y · Cited by 1,129 · see citing works
Tanaka, H., Tsukuma, H., Yamano, H., Oshima, A., & Shibata, H. (2004) · International Journal of Cancer · doi:10.1002/ijc.20507 · Cited by 57 · see citing works
- Authors
- Sun, C.-A.
- Affiliations
- National Defense Medical Center (TW)
- Corresponding author
- Sun, C.-A.
- ORCID
- Sun, C.-A.
- Venue
- American Journal of Epidemiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-04-15
- Volume
- 157
- Issue
- 8
- Pages
- 674-682
- ISSN
- 0002-9262 (ISSN-L)
- OpenAlex
- W2110758352
- Cited by
- 234
- References
- 49
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 8 · 2016: 9 · 2015: 14 · 2014: 22 · 2013: 12 · 2012: 16
- FWCI
- 11.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- American Journal of Epidemiology (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Science Council
- Topics
- Health Sciences › Medicine › Hepatology › Hepatitis C virus research
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Epidemiology › Hepatitis B Virus Studies
- Keywords
- hepatitis C virus, hepatocellular carcinoma, hepatitis B virus, HBV/HCV coinfection, cofactors, lifestyle habits, cigarette smoking, alcohol consumption, betel quid chewing, hepatocarcinogenesis, anti-HCV antibodies, men, Taiwan
- MeSH terms
- Adult, Alanine Transaminase, Follow-Up Studies, Hepatitis B, Hepatitis C, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Male, Middle Aged, Prospective Studies, Risk Factors, Taiwan, Health Behavior, Confounding Factors, Epidemiologic, Incidence
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review