Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study

Mei-Hwei Chang, San-Lin You, Chien-Jen Chen, Chun-Jen Liu, Chuan-Mo Lee, Shi-Ming Lin, Heng-Cheng Chu, Tzee-Chung Wu, Sheng-Shun Yang, Hsu-Sung Kuo, Ding-Shinn Chen

Research output: Contribution to journalArticle

376 Citations (Scopus)

Abstract

Background Hepatitis B virus (HBV) infection is a major cause of hepatocellular carcinoma. This population-based study aimed to investigate whether prevention of hepatocellular carcinoma by the universal Taiwanese HBV vaccine program, launched in July 1984, has extended beyond childhood and to identify the predictors of hepatocellular carcinoma for vaccinated birth cohorts.MethodsData on 1958 patients with hepatocellular carcinoma who were aged 6-29 years at diagnosis in Taiwan between 1983 and 2004 were collected from two national hepatocellular carcinoma registries. Age-and sex-specific incidence among vaccinated and unvaccinated birth cohorts were analyzed by using Poisson regression models. All statistical tests were two-sided. Records of 64 hepatocellular carcinoma patients and 5524435 HBV vaccinees who were born after the initiation of the vaccination program were compared for HBV immunization characteristics during infancy and prenatal maternal hepatitis B surface antigen (HBsAg) and e antigen (HBeAg) serostatus.ResultsHepatocellular carcinoma incidence was statistically significantly lower among children aged 6-19 years in vaccinated compared with unvaccinated birth cohorts (64 hepatocellular cancers among vaccinees in 37709304 person-years vs 444 cancers in unvaccinated subjects in 78496406 person-years, showing an age-and sex-adjusted relative risk of 0.31, P
Original languageEnglish
Pages (from-to)1348-1355
Number of pages8
JournalJournal of the National Cancer Institute
Volume101
Issue number19
DOIs
Publication statusPublished - 2009
Externally publishedYes

Fingerprint

Hepatitis B
Hepatocellular Carcinoma
Hepatitis B virus
Incidence
Parturition
Hepatitis B Vaccines
Hepatitis B e Antigens
Virus Diseases
Liver Neoplasms
Hepatitis B Surface Antigens
Taiwan
Registries
Immunization
Vaccination
Mothers
Carcinoma
Population
Neoplasms

Keywords

  • hepatitis B surface antigen
  • hepatitis B vaccine
  • hepatitis B(e) antigen
  • adult
  • article
  • child
  • controlled study
  • female
  • follow up
  • health program
  • hepatitis B
  • human
  • incidence
  • liver cell carcinoma
  • major clinical study
  • male
  • perinatal infection
  • preschool child
  • priority journal
  • risk factor
  • sex difference
  • Taiwan
  • Adolescent
  • Adult
  • Age Distribution
  • Carcinoma, Hepatocellular
  • Child
  • Female
  • Follow-Up Studies
  • Hepatitis B e Antigens
  • Hepatitis B Surface Antigens
  • Hepatitis B Vaccines
  • Humans
  • Incidence
  • Liver Neoplasms
  • Male
  • Mothers
  • Multivariate Analysis
  • Odds Ratio
  • Registries
  • Sex Distribution
  • Young Adult

Cite this

Chang, M-H., You, S-L., Chen, C-J., Liu, C-J., Lee, C-M., Lin, S-M., ... Chen, D-S. (2009). Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study. Journal of the National Cancer Institute, 101(19), 1348-1355. https://doi.org/10.1093/jnci/djp288

Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study. / Chang, Mei-Hwei; You, San-Lin; Chen, Chien-Jen; Liu, Chun-Jen; Lee, Chuan-Mo; Lin, Shi-Ming; Chu, Heng-Cheng; Wu, Tzee-Chung; Yang, Sheng-Shun; Kuo, Hsu-Sung; Chen, Ding-Shinn.

In: Journal of the National Cancer Institute, Vol. 101, No. 19, 2009, p. 1348-1355.

Research output: Contribution to journalArticle

Chang, M-H, You, S-L, Chen, C-J, Liu, C-J, Lee, C-M, Lin, S-M, Chu, H-C, Wu, T-C, Yang, S-S, Kuo, H-S & Chen, D-S 2009, 'Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study', Journal of the National Cancer Institute, vol. 101, no. 19, pp. 1348-1355. https://doi.org/10.1093/jnci/djp288
Chang, Mei-Hwei ; You, San-Lin ; Chen, Chien-Jen ; Liu, Chun-Jen ; Lee, Chuan-Mo ; Lin, Shi-Ming ; Chu, Heng-Cheng ; Wu, Tzee-Chung ; Yang, Sheng-Shun ; Kuo, Hsu-Sung ; Chen, Ding-Shinn. / Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study. In: Journal of the National Cancer Institute. 2009 ; Vol. 101, No. 19. pp. 1348-1355.
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abstract = "Background Hepatitis B virus (HBV) infection is a major cause of hepatocellular carcinoma. This population-based study aimed to investigate whether prevention of hepatocellular carcinoma by the universal Taiwanese HBV vaccine program, launched in July 1984, has extended beyond childhood and to identify the predictors of hepatocellular carcinoma for vaccinated birth cohorts.MethodsData on 1958 patients with hepatocellular carcinoma who were aged 6-29 years at diagnosis in Taiwan between 1983 and 2004 were collected from two national hepatocellular carcinoma registries. Age-and sex-specific incidence among vaccinated and unvaccinated birth cohorts were analyzed by using Poisson regression models. All statistical tests were two-sided. Records of 64 hepatocellular carcinoma patients and 5524435 HBV vaccinees who were born after the initiation of the vaccination program were compared for HBV immunization characteristics during infancy and prenatal maternal hepatitis B surface antigen (HBsAg) and e antigen (HBeAg) serostatus.ResultsHepatocellular carcinoma incidence was statistically significantly lower among children aged 6-19 years in vaccinated compared with unvaccinated birth cohorts (64 hepatocellular cancers among vaccinees in 37709304 person-years vs 444 cancers in unvaccinated subjects in 78496406 person-years, showing an age-and sex-adjusted relative risk of 0.31, P",
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author = "Mei-Hwei Chang and San-Lin You and Chien-Jen Chen and Chun-Jen Liu and Chuan-Mo Lee and Shi-Ming Lin and Heng-Cheng Chu and Tzee-Chung Wu and Sheng-Shun Yang and Hsu-Sung Kuo and Ding-Shinn Chen",
note = "被引用次數:249 Export Date: 22 March 2016 CODEN: JNCIA 通訊地址: Chang, M.-H.; Department of Pediatrics, College of Public Health, National Taiwan University, Chung-Shan S. Road, Taipei, Taiwan; 電子郵件: changmh@ntu.edu.tw 化學物質/CAS: Hepatitis B Surface Antigens; Hepatitis B Vaccines; Hepatitis B e Antigens 參考文獻: Larouze, B., Saimot, G., Lustbader, E.D., London, W.T., Werner, B.G., Payet, M., Host response to hepatitis B infection in patients with primary hepatic carcinoma and their families: A case control study in Senegal West Africa Lancet, 2 (7985), pp. 534-538; Beasley, R.P., Hwang, L.Y., Lin, C.C., Chien, C.S., Hepatocellular carcinoma and hepatitis B virus: A prospective study of 22,707 men in Taiwan (1981) Lancet, 2 (8256), pp. 1129-1133; Popper, H., Ma, G., Thung, S.N., The relation of hepatocellular carcinoma to infection with hepatitis B and related viruses in man and animals (1982) Hepatology, 2 (SUPPL.), pp. 1S-9S; Chen, D.S., Hepatitis B virus infection, its sequelae, and prevention in Taiwan (1987) Neoplasms of the Liver, pp. 71-80. , Okuda K, Ishak G, eds Tokyo, Japan : Springer-Verlag; Lee, C.M., Lu, S.N., Changchien, C.S., Age, gender, and local geographic variations of viral etiology of hepatocellular carcinoma in a hyperendemic area for hepatitis B virus infection (1999) Cancer, 86 (7), pp. 1143-1150; Chang, M.H., Chen, D.S., Hsu, H.C., Hsu, H.Y., Lee, C.Y., Maternal transmission of hepatitis B virus in childhood hepatocellular carcinoma (1989) Cancer, 64 (11), pp. 2377-2380; Chang, M.H., Chen, P.J., Chen, J.Y., Hepatitis B virus integration in hepatitis B virus-related hepatocellular carcinoma in childhood (1991) Hepatology, 13 (2), pp. 316-320; Chen, D.S., Hsu, N.H., Sung, J.L., A mass vaccination program in Taiwan against hepatitis B virus infection in infants of hepatitis B surface antigen-carrier mothers (1987) JAMA, 257 (19), pp. 2597-2603; Ni, Y.H., Chang, M.H., Huang, L.M., Hepatitis B virus infection in children and adolescents in a hyperendemic area: 15 years after universal hepatitis B vaccination (2001) Ann Intern Med, 135 (9), pp. 769-800; Chang, M.H., Chen, C.J., Lai, M.S., Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children (1997) N Engl J Med, 336 (26), pp. 1855-1859; Chang, M.H., Chen, T., Hsu, H.M., Problems in the prevention of childhood hepatocellular carcinoma in the era of universal hepatitis B immunization (2005) Clin Cancer Res., 11 (21), pp. 7953-7957; Bosch, F.X., Ribes, J., The epidemiology of primary liver cancer: Global epidemiology (2002) Viruses and Liver Cancer, pp. 1-16. , Tabor E, ed Amsterdam, the Netherlands : Elsevier; Ni, Y.H., Chang, M.H., Hsu, H.Y., Hepatocellular carcinoma in childhood: Clinical manifestations and prognosis (1991) Cancer, 68 (8), pp. 1737-1741; Kuo, C.Y., Liu, H.C., Chang, M.H., Hepatoblastoma in infancy and childhood: A clinical and pathological study of 32 cases (1991) Acta Paediatr Taiwan, 32 (2), pp. 79-87; (2008) Cancer Registry Annual Report 2005, , Bureau of Health Promotion (ROC) Taipei, Taiwan : Bureau of Health Promotion; Chen, C.N., Liu, P.K.C., An evaluation of Taiwan Census 2000: A comparison of census and registered populations (2002) J Popul Stud, 25 (1), pp. 1-56; Ni, Y.H., Huang, L.M., Chang, M.H., Two decades of universal hepatitis B vaccination in Taiwan: Impact and implication for future strategies (2007) Gastroenterology, 132 (4), pp. 1287-1293; Breslow, N.F., Day, N.E., Statistical methods in cancer research II: The design and analysis of cohort studies (1987) Fitting Models to Group Data, pp. 121-176. , Breslow NF, Day NE, eds Lyon : France International Agency for Research on Cancer (IARC) Scientifi c Publications No.82; Tang, J.R., Hsu, H.Y., Lin, H.H., Ni, Y.H., Chang, M.H., Hepatitis B surface antigenemia at birth: A long-term follow-up study (1998) J Pediatr, 133 (3), pp. 374-1137; Blonski, W., Reddy, K.R., Hepatitis C virus infection and hepatocellular carcinoma (2008) Clin Liver Dis, 12 (3), pp. 661-674; Chang, M.H., Lee, C.Y., Chen, D.S., Minimal role of hepatitis C virus infection in childhood liver diseases in an area hyperendemic for hepatitis B infection (1993) J Med Virol, 40 (4), pp. 322-325; Wang, L.Y., You, S.L., Lu, S.N., Risk of hepatocellular carcinoma and habits of alcohol drinking, betel quid chewing and cigarette smoking: A cohort of 2416 HBsAg-seropositive and 9421 HBsAg-seronegative male residents in Taiwan (2003) Cancer Causes Control, 14 (3), pp. 241-250; Kuper, H., Ye, W., Broom, U., The risk of liver and bile duct cancer in patients with chronic viral hepatitis, alcoholism, or cirrhosis (2001) Hepatology, 34 (4), pp. 714-718; Gouas, D., Shi, H., Hainaut, P., The afl atoxin-induced TP53 mutation at codon 249 (R249S): Biomarker of exposure, early detection and target for therapy (2009) Cancer Lett, , doi:10.1016/j.canlet.2009.02.057; Chou, S.Y., Lee, M.P., Liang, M., Prevalence of smoking, alcohol consumption, betal nut chewing and illicit drug use among adolescents in Taiwan (2006) Mid Taiwan J Med, 11 (3), pp. 177-186; Sheu, J.C., Huang, G.T., Lee, P.H., Mutation of p53 gene in hepatocel-lular carcinoma in Taiwan (1992) Cancer Res, 52 (21), pp. 6098-6100",
year = "2009",
doi = "10.1093/jnci/djp288",
language = "English",
volume = "101",
pages = "1348--1355",
journal = "Journal of the National Cancer Institute",
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}

TY - JOUR

T1 - Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: A 20-year follow-up study

AU - Chang, Mei-Hwei

AU - You, San-Lin

AU - Chen, Chien-Jen

AU - Liu, Chun-Jen

AU - Lee, Chuan-Mo

AU - Lin, Shi-Ming

AU - Chu, Heng-Cheng

AU - Wu, Tzee-Chung

AU - Yang, Sheng-Shun

AU - Kuo, Hsu-Sung

AU - Chen, Ding-Shinn

N1 - 被引用次數:249 Export Date: 22 March 2016 CODEN: JNCIA 通訊地址: Chang, M.-H.; Department of Pediatrics, College of Public Health, National Taiwan University, Chung-Shan S. Road, Taipei, Taiwan; 電子郵件: changmh@ntu.edu.tw 化學物質/CAS: Hepatitis B Surface Antigens; Hepatitis B Vaccines; Hepatitis B e Antigens 參考文獻: Larouze, B., Saimot, G., Lustbader, E.D., London, W.T., Werner, B.G., Payet, M., Host response to hepatitis B infection in patients with primary hepatic carcinoma and their families: A case control study in Senegal West Africa Lancet, 2 (7985), pp. 534-538; Beasley, R.P., Hwang, L.Y., Lin, C.C., Chien, C.S., Hepatocellular carcinoma and hepatitis B virus: A prospective study of 22,707 men in Taiwan (1981) Lancet, 2 (8256), pp. 1129-1133; Popper, H., Ma, G., Thung, S.N., The relation of hepatocellular carcinoma to infection with hepatitis B and related viruses in man and animals (1982) Hepatology, 2 (SUPPL.), pp. 1S-9S; Chen, D.S., Hepatitis B virus infection, its sequelae, and prevention in Taiwan (1987) Neoplasms of the Liver, pp. 71-80. , Okuda K, Ishak G, eds Tokyo, Japan : Springer-Verlag; Lee, C.M., Lu, S.N., Changchien, C.S., Age, gender, and local geographic variations of viral etiology of hepatocellular carcinoma in a hyperendemic area for hepatitis B virus infection (1999) Cancer, 86 (7), pp. 1143-1150; Chang, M.H., Chen, D.S., Hsu, H.C., Hsu, H.Y., Lee, C.Y., Maternal transmission of hepatitis B virus in childhood hepatocellular carcinoma (1989) Cancer, 64 (11), pp. 2377-2380; Chang, M.H., Chen, P.J., Chen, J.Y., Hepatitis B virus integration in hepatitis B virus-related hepatocellular carcinoma in childhood (1991) Hepatology, 13 (2), pp. 316-320; Chen, D.S., Hsu, N.H., Sung, J.L., A mass vaccination program in Taiwan against hepatitis B virus infection in infants of hepatitis B surface antigen-carrier mothers (1987) JAMA, 257 (19), pp. 2597-2603; Ni, Y.H., Chang, M.H., Huang, L.M., Hepatitis B virus infection in children and adolescents in a hyperendemic area: 15 years after universal hepatitis B vaccination (2001) Ann Intern Med, 135 (9), pp. 769-800; Chang, M.H., Chen, C.J., Lai, M.S., Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children (1997) N Engl J Med, 336 (26), pp. 1855-1859; Chang, M.H., Chen, T., Hsu, H.M., Problems in the prevention of childhood hepatocellular carcinoma in the era of universal hepatitis B immunization (2005) Clin Cancer Res., 11 (21), pp. 7953-7957; Bosch, F.X., Ribes, J., The epidemiology of primary liver cancer: Global epidemiology (2002) Viruses and Liver Cancer, pp. 1-16. , Tabor E, ed Amsterdam, the Netherlands : Elsevier; Ni, Y.H., Chang, M.H., Hsu, H.Y., Hepatocellular carcinoma in childhood: Clinical manifestations and prognosis (1991) Cancer, 68 (8), pp. 1737-1741; Kuo, C.Y., Liu, H.C., Chang, M.H., Hepatoblastoma in infancy and childhood: A clinical and pathological study of 32 cases (1991) Acta Paediatr Taiwan, 32 (2), pp. 79-87; (2008) Cancer Registry Annual Report 2005, , Bureau of Health Promotion (ROC) Taipei, Taiwan : Bureau of Health Promotion; Chen, C.N., Liu, P.K.C., An evaluation of Taiwan Census 2000: A comparison of census and registered populations (2002) J Popul Stud, 25 (1), pp. 1-56; Ni, Y.H., Huang, L.M., Chang, M.H., Two decades of universal hepatitis B vaccination in Taiwan: Impact and implication for future strategies (2007) Gastroenterology, 132 (4), pp. 1287-1293; Breslow, N.F., Day, N.E., Statistical methods in cancer research II: The design and analysis of cohort studies (1987) Fitting Models to Group Data, pp. 121-176. , Breslow NF, Day NE, eds Lyon : France International Agency for Research on Cancer (IARC) Scientifi c Publications No.82; Tang, J.R., Hsu, H.Y., Lin, H.H., Ni, Y.H., Chang, M.H., Hepatitis B surface antigenemia at birth: A long-term follow-up study (1998) J Pediatr, 133 (3), pp. 374-1137; Blonski, W., Reddy, K.R., Hepatitis C virus infection and hepatocellular carcinoma (2008) Clin Liver Dis, 12 (3), pp. 661-674; Chang, M.H., Lee, C.Y., Chen, D.S., Minimal role of hepatitis C virus infection in childhood liver diseases in an area hyperendemic for hepatitis B infection (1993) J Med Virol, 40 (4), pp. 322-325; Wang, L.Y., You, S.L., Lu, S.N., Risk of hepatocellular carcinoma and habits of alcohol drinking, betel quid chewing and cigarette smoking: A cohort of 2416 HBsAg-seropositive and 9421 HBsAg-seronegative male residents in Taiwan (2003) Cancer Causes Control, 14 (3), pp. 241-250; Kuper, H., Ye, W., Broom, U., The risk of liver and bile duct cancer in patients with chronic viral hepatitis, alcoholism, or cirrhosis (2001) Hepatology, 34 (4), pp. 714-718; Gouas, D., Shi, H., Hainaut, P., The afl atoxin-induced TP53 mutation at codon 249 (R249S): Biomarker of exposure, early detection and target for therapy (2009) Cancer Lett, , doi:10.1016/j.canlet.2009.02.057; Chou, S.Y., Lee, M.P., Liang, M., Prevalence of smoking, alcohol consumption, betal nut chewing and illicit drug use among adolescents in Taiwan (2006) Mid Taiwan J Med, 11 (3), pp. 177-186; Sheu, J.C., Huang, G.T., Lee, P.H., Mutation of p53 gene in hepatocel-lular carcinoma in Taiwan (1992) Cancer Res, 52 (21), pp. 6098-6100

PY - 2009

Y1 - 2009

N2 - Background Hepatitis B virus (HBV) infection is a major cause of hepatocellular carcinoma. This population-based study aimed to investigate whether prevention of hepatocellular carcinoma by the universal Taiwanese HBV vaccine program, launched in July 1984, has extended beyond childhood and to identify the predictors of hepatocellular carcinoma for vaccinated birth cohorts.MethodsData on 1958 patients with hepatocellular carcinoma who were aged 6-29 years at diagnosis in Taiwan between 1983 and 2004 were collected from two national hepatocellular carcinoma registries. Age-and sex-specific incidence among vaccinated and unvaccinated birth cohorts were analyzed by using Poisson regression models. All statistical tests were two-sided. Records of 64 hepatocellular carcinoma patients and 5524435 HBV vaccinees who were born after the initiation of the vaccination program were compared for HBV immunization characteristics during infancy and prenatal maternal hepatitis B surface antigen (HBsAg) and e antigen (HBeAg) serostatus.ResultsHepatocellular carcinoma incidence was statistically significantly lower among children aged 6-19 years in vaccinated compared with unvaccinated birth cohorts (64 hepatocellular cancers among vaccinees in 37709304 person-years vs 444 cancers in unvaccinated subjects in 78496406 person-years, showing an age-and sex-adjusted relative risk of 0.31, P

AB - Background Hepatitis B virus (HBV) infection is a major cause of hepatocellular carcinoma. This population-based study aimed to investigate whether prevention of hepatocellular carcinoma by the universal Taiwanese HBV vaccine program, launched in July 1984, has extended beyond childhood and to identify the predictors of hepatocellular carcinoma for vaccinated birth cohorts.MethodsData on 1958 patients with hepatocellular carcinoma who were aged 6-29 years at diagnosis in Taiwan between 1983 and 2004 were collected from two national hepatocellular carcinoma registries. Age-and sex-specific incidence among vaccinated and unvaccinated birth cohorts were analyzed by using Poisson regression models. All statistical tests were two-sided. Records of 64 hepatocellular carcinoma patients and 5524435 HBV vaccinees who were born after the initiation of the vaccination program were compared for HBV immunization characteristics during infancy and prenatal maternal hepatitis B surface antigen (HBsAg) and e antigen (HBeAg) serostatus.ResultsHepatocellular carcinoma incidence was statistically significantly lower among children aged 6-19 years in vaccinated compared with unvaccinated birth cohorts (64 hepatocellular cancers among vaccinees in 37709304 person-years vs 444 cancers in unvaccinated subjects in 78496406 person-years, showing an age-and sex-adjusted relative risk of 0.31, P

KW - hepatitis B surface antigen

KW - hepatitis B vaccine

KW - hepatitis B(e) antigen

KW - adult

KW - article

KW - child

KW - controlled study

KW - female

KW - follow up

KW - health program

KW - hepatitis B

KW - human

KW - incidence

KW - liver cell carcinoma

KW - major clinical study

KW - male

KW - perinatal infection

KW - preschool child

KW - priority journal

KW - risk factor

KW - sex difference

KW - Taiwan

KW - Adolescent

KW - Adult

KW - Age Distribution

KW - Carcinoma, Hepatocellular

KW - Child

KW - Female

KW - Follow-Up Studies

KW - Hepatitis B e Antigens

KW - Hepatitis B Surface Antigens

KW - Hepatitis B Vaccines

KW - Humans

KW - Incidence

KW - Liver Neoplasms

KW - Male

KW - Mothers

KW - Multivariate Analysis

KW - Odds Ratio

KW - Registries

KW - Sex Distribution

KW - Young Adult

U2 - 10.1093/jnci/djp288

DO - 10.1093/jnci/djp288

M3 - Article

VL - 101

SP - 1348

EP - 1355

JO - Journal of the National Cancer Institute

JF - Journal of the National Cancer Institute

SN - 0027-8874

IS - 19

ER -