International trends in hepatocellular carcinoma incidence, 1978–2012
Open accessAbstract
Primary liver cancer, the major histology of which is hepatocellular carcinoma (HCC), is the second leading cause of cancer death worldwide. We comprehensively examined recent international trends of primary liver cancer and HCC incidence using population‐based cancer registry data. Incidence for all primary liver cancer and for HCC by calendar time and birth cohort was examined for selected countries between 1978 and 2012. For each successive 5‐year period, age‐standardized incidence rates were calculated from Volumes V to XI of the Cancer Incidence in Five Continents (CI5) series using the online electronic databases, CI5 plus. Large variations persist in liver cancer incidence globally. Rates of liver cancer remain highest in Asian countries, specifically in the East and South‐East, and Italy. However, rates in these high‐risk countries have been decreasing in recent years. Rates in India and in most countries of Europe, the Americas and Oceania are rising. As the population seroprevalence of hepatitis B virus (HBV) continues to decline, we anticipate rates of HCC in many high‐risk countries will continue to decrease. Treatment of hepatitis C virus (HCV) is likely to bring down rates further in some high‐rate, as well as low‐rate, countries with access to effective therapies. However, such gains in the control of liver cancer are at risk of being reversed by the growing obesity and diabetes epidemics, suggesting diabetes treatment and primary prevention of obesity will be key in reducing liver cancer in the longer‐term.
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Incidence rates in formerly low-risk countries, most countries across Europe, North America, Australia/New Zealand, and South America, have increased or stabilized at a higher level in recent years, possibly in part because of increasing prevalence of metabolic risk factors, such as excess body weight, diabetes, nonalcoholic fatty liver disease, and alcohol consumption.
“Likewise, incidence rates in formerly low-risk countries, most countries across Europe, North America, Australia/New Zealand, and South America have increased or stabilized at a higher level in recent years, 125,128 possibly in part because of increasing prevalence of metabolic risk factors, such as excess body weight, diabetes, nonalcoholic fatty liver disease, and alcohol consumption.”
From Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. (2024) · cites this paper as [125]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredIn countries like Thailand, where HCC represents less than 30% of liver cancer, liver cancer incidence rates continue to rise despite the decline in HCC rates.
“In contrast, in countries like Thailand, where HCC represents less than 30% of liver cancer, liver cancer incidence rates continue to rise despite the decline in HCC rates.125”
From Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. (2024) · cites this paper as [125]
The Results report that HCC accounted for 27% of liver cancers with microscopic verification in Thailand, and that primary liver cancer incidence rose while HCC incidence fell sharply since 2000. The claim accurately describes the opposing trends but omits that the percentage applies only to microscopically verified cancers. (LLM, conf=0.86)
Experimental — accuracy not yet measuredWith declines in the population seroprevalence of HBV and HCV, as well as a reduction in aflatoxin exposure, liver cancer rates have been declining steadily in many high-risk countries in East and South-Eastern Asia since the late 1970s and in Japan and China since the 1990s.
“With declines in the population seroprevalence of HBV and HCV, as well as a reduction in aflatoxin exposure, liver cancer rates have been declining steadily in many high-risk countries in East and South-Eastern Asia since the late 1970s and in Japan and China since the 1990s.63,125,126”
From Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. (2024) · cites this paper as [125]
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Cites
Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R. L., Torre, L. A., & Jemal, A. (2018) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21492 · Cited by 84,109 · see citing works
Self-citationGlobal estimates of the prevalence of diabetes for 2010 and 2030
Shaw, J. E., Sicree, R. A., & Zimmet, P. Z. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2009.10.007 · Cited by 7,216 · see citing works
Cancer Incidence in Five Continents
(1966) · doi:10.1007/978-3-642-85849-9 · Cited by 5,936 · see citing works
Marrero, J. A., Kulik, L., Sirlin, C. B., Zhu, A. X., Finn, R. S., Abecassis, M. M., Roberts, L. R., & Heimbach, J. K. (2018) · Hepatology · doi:10.1002/hep.29913 · Cited by 4,549 · see citing works
Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up
Escudier, B. J., Porta, C., Schmidinger, M., Ferran Algaba, B., Patard, J., Khoo, V. S., Eisen, T. G., & Horwich, A. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu259 · Cited by 2,253 · see citing works
Akinyemiju, T., Abera, S. F., Ahmed, M. B., Alam, N., Alemayohu, M. A., Allen, C., Al-Raddadi, R. M., Alvis‐Guzmán, N., Amoako, Y. A., Artaman, A., et al. (2017) · JAMA Oncology · doi:10.1001/jamaoncol.2017.3055 · Cited by 1,985 · see citing works
Epidemic obesity and type 2 diabetes in Asia
Yoon, K.-H., Lee, J.-H., Kim, J.-W., Cho, J. H., Choi, Y.-H., Ko, S.-H., Zimmet, P., & Son, H.-Y. (2006) · The Lancet · doi:10.1016/s0140-6736(06)69703-1 · Cited by 1,580 · see citing works
Daclatasvir plus Sofosbuvir for Previously Treated or Untreated Chronic HCV Infection
Sulkowski, M., Gardiner, D., Rodriguez‐Torres, M., Reddy, K. R., Hassanein, T., Jacobson, I. M., Lawitz, E., Lok, A. S.-F., Hinestrosa, F., Thuluvath, P. J., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1306218 · Cited by 1,187 · see citing works
New trends on obesity and NAFLD in Asia
Fan, J.-G., Kim, S. U., & Wong, V. W. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.06.003 · Cited by 1,088 · see citing works
Hepatocellular carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up
Vogel, A., Cervantes, A. M. R., Chau, I., Daniele, B., Llovet, J. M., Meyer, T., Nault, J., Neumann, U. P., Ricke, J., Sangro, B., et al. (2018) · Annals of Oncology · doi:10.1093/annonc/mdy308 · Cited by 1,047 · see citing works
Smith, B. D., Morgan, R. L., Beckett, G. A., Falck-Ytter, Y. T., Holtzman, D. J., Teo, C., Jewett, A., Baack, B. N., Rein, D. B., Patel, N., et al. (2012) · PubMed · Cited by 991 · see citing works
Models for temporal variation in cancer rates. I: Age-period and age-cohort models.
Clayton, D., & Schifflers, E. (1987) · Statistics in Medicine · doi:10.1002/sim.4780060405 · Cited by 882 · see citing works
Liu, Z., Jiang, Y., Yuan, H., Fang, Q., Cai, N., Suo, C., Li, J., Zhang, T., & Chen, X. (2018) · Journal of Hepatology · doi:10.1016/j.jhep.2018.12.001 · Cited by 826 · see citing works
Marrero, J. A., Kulik, L., Sirlin, C. B., Zhu, A. X., Finn, R. S., Abecassis, M. M., Roberts, L. R., Heimbach, J. K., et al. (2019) · Clinical Liver Disease · doi:10.1002/cld.802 · Cited by 646 · see citing works
Global trends and predictions in hepatocellular carcinoma mortality
Bertuccio, P., Turati, F., Carioli, G., Rodriguez, T., Vecchia, C. L., Malvezzi, M., & Negri, E. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.03.011 · Cited by 635 · see citing works
Bray, F., & Parkin, D. M. (2008) · European Journal of Cancer · doi:10.1016/j.ejca.2008.11.032 · Cited by 634 · see citing works
Self-citationEvaluation of data quality in the cancer registry: Principles and methods Part II. Completeness
Parkin, D. M., & Bray, F. (2009) · European Journal of Cancer · doi:10.1016/j.ejca.2008.11.033 · Cited by 536 · see citing works
Self-citationGender Differences in Cancer Susceptibility: An Inadequately Addressed Issue
Dorak, M. T., & Karpuzoglu, E. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00268 · Cited by 495 · see citing works
Population attributable risk of aflatoxin-related liver cancer: Systematic review and meta-analysis
Liu, Y., Chang, C.-C. H., Marsh, G. M., & Wu, F. (2012) · European Journal of Cancer · doi:10.1016/j.ejca.2012.02.009 · Cited by 372 · see citing works
Meta‐analysis: treatment of hepatitis B infection reduces risk of hepatocellular carcinoma
Sung, J. J. �., Tsoi, K. K. F., Wong, V. W., LI, K. C. T., & Chan, H. L. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2008.03816.x · Cited by 369 · see citing works
Epidemiology of Hepatitis B Virus Infection and Impact of Vaccination on Disease
Nelson, N. P., Easterbrook, P., & McMahon, B. J. (2016) · Clinics in Liver Disease · doi:10.1016/j.cld.2016.06.006 · Cited by 365 · see citing works
International trends in liver cancer incidence, overall and by histologic subtype, 1978–2007
Petrick, J. L., Braunlin, M., Laversanne, M., Valery, P. C., Bray, F., & McGlynn, K. A. (2016) · International Journal of Cancer · doi:10.1002/ijc.30211 · Cited by 343 · see citing works
Self-citationTanaka, Y., Hanada, K., Mizokami, M., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242608099 · Cited by 333 · see citing works
Population attributable fractions of risk factors for hepatocellular carcinoma in the United States
Makarova‐Rusher, O. V., Altekruse, S. F., McNeel, T. S., Ulahannan, S. V., Duffy, A. G., Graubard, B. I., Greten, T. F., & McGlynn, K. A. (2016) · Cancer · doi:10.1002/cncr.29971 · Cited by 332 · see citing works
Self-citationLong-term Effects of Hepatitis B Immunization of Infants in Preventing Liver Cancer
Chang, M., You, S., Chen, C., Liu, C., Lai, M., Wu, T., Wu, S., Lee, C., Yang, S., Chu, H.-C., et al. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.05.048 · Cited by 258 · see citing works
Trickey, A., Fraser, H., Lim, A. G., Peacock, A., Colledge‐Frisby, S., Walker, J. G., Leung, J., Grebely, J., Larney, S., Martin, N. K., et al. (2019) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(19)30085-8 · Cited by 241 · see citing works
Epidemiology of liver cancer in South Korea
Kim, B. H., & Park, J. (2017) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2017.0112 · Cited by 190 · see citing works
A model of interaction: Aflatoxins and hepatitis viruses in liver cancer aetiology and prevention
Wild, C. P., & Montesano, R. (2009) · Cancer Letters · doi:10.1016/j.canlet.2009.02.053 · Cited by 186 · see citing works
The Changing Epidemiology of Primary Liver Cancer
Petrick, J. L., & McGlynn, K. A. (2019) · Current Epidemiology Reports · doi:10.1007/s40471-019-00188-3 · Cited by 173 · see citing works
Self-citationDifferent seroprevalence and molecular epidemiology patterns of hepatitis C virus infection in Italy
Ansaldi, F., Bruzzone, B. M., Salmaso, S., et al. (2005) · Journal of Medical Virology · doi:10.1002/jmv.20376 · Cited by 167 · see citing works
Obesity in Asia – is it different from rest of the world
Ramachandran, A., Snehalatha, C., Shetty, S. A., Nanditha, A., & Susairaj, P. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2353 · Cited by 166 · see citing works
Reduced Aflatoxin Exposure Presages Decline in Liver Cancer Mortality in an Endemic Region of China
Chen, J., Egner, P. A., Ng, D. K., Jacobson, L. P., Muñoz, A., Zhu, Y., Qian, G., Wu, F., Yuan, J., Groopman, J. D., et al. (2013) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-13-0168 · Cited by 166 · see citing works
Reducing the neglected burden of viral hepatitis in Africa: Strategies for a global approach
Lemoine, M., Eholié, S. P., & Lacombe, K. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.10.008 · Cited by 161 · see citing works
Graphical Presentation of Trends in Rates
Devesa, S. S., Donaldson, J., & Fears, T. R. (1995) · American Journal of Epidemiology · doi:10.1093/aje/141.4.300 · Cited by 160 · see citing works
Declining Incidence of Hepatocellular Carcinoma in Osaka, Japan, from 1990 to 2003
Tanaka, H., Imai, Y., Hiramatsu, N., Ito, Y., Imanaka, K., Oshita, M., Hijioka, T., Katayama, K., Yabuuchi, I., Yoshihara, H., et al. (2008) · Annals of Internal Medicine · doi:10.7326/0003-4819-148-11-200806030-00004 · Cited by 127 · see citing works
Liver Fluke-Associated Biliary Tract Cancer
Prueksapanich, P., Piyachaturawat, P., Aumpansub, P., Ridtitid, W., Chaiteerakij, R., & Rerknimitr, R. (2018) · Gut and Liver · doi:10.5009/gnl17102 · Cited by 118 · see citing works
Histological classification of liver and intrahepatic bile duct cancers in SEER registries.
Altekruse, S. F., Devesa, S. S., Dickie, L. A., McGlynn, K. A., & Kleiner, D. E. (2011) · PubMed · Cited by 116 · see citing works
Self-citationChoi, J., Han, S., Kim, N., & Lim, Y. (2017) · Hepatology · doi:10.1002/hep.29321 · Cited by 108 · see citing works
Sun, Z., Chen, T., Thorgeirsson, S. S., et al. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt007 · Cited by 97 · see citing works
Testing the equality of two dependent kappa statistics
Donner, A. P., Shoukri, M. M., Klar, N. S., & Bartfay, E. (2000) · Statistics in Medicine · doi:10.1002/(sici)1097-0258(20000215)19:3 · Cited by 90 · see citing works
Segi, M., Fujisaku, S., & Kurihara, M. (1957) · PubMed · Cited by 66 · see citing works
International trends in primary liver cancer incidence from 1973 to 2007
Zhang, Y., Ren, J., Shi, J., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1113-4 · Cited by 60 · see citing works
The silent epidemic killing more people than HIV, malaria or TB
Graber-Stiehl, I. (2018) · Nature · doi:10.1038/d41586-018-07592-7 · Cited by 59 · see citing works
The spread of hepatitis C virus genotype 1a in North America: a retrospective phylogenetic study
Joy, J. B., McCloskey, R. M., Nguyen, T. N., Liang, R. H., Khudyakov, Y. E., Olmstead, A. D., Krajden, M., Ward, J. W., Harrigan, P. R., Montaner, J. S. G., et al. (2016) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(16)00124-9 · Cited by 49 · see citing works
Mora, M., Romano, C. M., Gomes‐Gouvêa, M. S., et al. (2010) · Journal of Medical Virology · doi:10.1002/jmv.21908 · Cited by 30 · see citing works
Recent status of mycotoxin research in the Philippines
ARIM, H. (2000) · JSM Mycotoxins · doi:10.2520/myco1975.50.23 · Cited by 4 · see citing works
Update of Hepatitis C in Colombia
Hinestrosa, F., Marín, J. I., Maya, O. G. M., et al. (2018) · Current Tropical Medicine Reports · doi:10.1007/s40475-018-0147-5 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [6]McGlynn KA, Petrick JL, London WT. Chaper 33. Liver Cancer In: Thun MJ, Linet MS, Cerhan JR, Haiman C, Schottenfeld D, eds. Schottenfeld and Fraumeni cancer epidemiology and prevention. New York, NY: Oxford University Press, 2018: xix, 1308 pages.
- [17]Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med 2000; 19: 335– 51. 10649300
- [18]Ferlay J, Rous B. Chapter 4: Histological groups In: Bray F, Colombet M, Mery L, Piñeros M, Znaor A, Zanetti R,, eds. Cancer Incidence in Five Continents, Vol XI IARC Scientific Publication No 166. Lyon: International Agency for Research on Cancer, 2019.
Cited by
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Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2021) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21660 · Cited by 108,699 · see citing works
Self-citationBray, F., Laversanne, M., Sung, H., Ferlay, J., Siegel, R. L., Soerjomataram, I., & Jemal, A. (2024) · CA: a cancer journal for clinicians · doi:10.3322/caac.21834 · Cited by 27,064 · see citing works
“…countries across Europe, North America, Australia/New Zealand, and South America have increased or stabilized at a higher level in recent years, 125,128 possibly in part because of increasing prevalence of metabolic risk factors, such as excess body weight, diabetes, nonalcoholic fatty liver…”
BackgroundSelf-citationVogel, A., Meyer, T., Sapisochin, G., Salem, R., & Saborowski, A. (2022) · The Lancet · doi:10.1016/s0140-6736(22)01200-4 · Cited by 2,427 · see citing works
Global burden of primary liver cancer in 2020 and predictions to 2040
Rumgay, H., Arnold, M., Ferlay, J., Lesi, O., Cabasag, C. J., Vignat, J., Laversanne, M., McGlynn, K. A., & Soerjomataram, I. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.08.021 · Cited by 2,197 · see citing works
Self-citationGlobal Burden of 5 Major Types of Gastrointestinal Cancer
Arnold, M., Abnet, C. C., Neale, R. E., Vignat, J., Giovannucci, E. L., McGlynn, K. A., & Bray, F. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.02.068 · Cited by 2,027 · see citing works
Self-citationAASLD Practice Guidance on prevention, diagnosis, and treatment of hepatocellular carcinoma
Singal, A. G., Llovet, J. M., Yarchoan, M., Mehta, N., Heimbach, J. K., Dawson, L. A., Jou, J. H., Kulik, L. M., Agopian, V. G., Marrero, J. A., et al. (2023) · Hepatology · doi:10.1097/hep.0000000000000466 · Cited by 2,052 · see citing works
Global, regional and national burden of primary liver cancer by subtype
Rumgay, H., Ferlay, J., de Martel, C., Georges, D., Ibrahim, A. S., Zheng, R., Wei, W., Lemmens, V. E. P. P., & Soerjomataram, I. (2022) · European Journal of Cancer · doi:10.1016/j.ejca.2021.11.023 · Cited by 615 · see citing works
Self-citationMASLD: Prevalence, Mechanisms, and Sex-Based Therapies in Postmenopausal Women
Milani, I., Chinucci, M., Leonetti, F., & Capoccia, D. (2025) · Biomedicines · doi:10.3390/biomedicines13040855 · Cited by 38 · see citing works
“In liver cancer, MASH has surpassed alcohol-related liver disease as the leading cause of HCC [42], with men generally experiencing rates two to four times higher than women [44,45].”
Poręba-Chabros, A., Kolańska-Stronka, M., Mamcarz, P., & Mamcarz, I. (2022) · Supportive Care in Cancer · doi:10.1007/s00520-022-06880-3 · Cited by 17 · see citing works
- Authors
- Petrick, J. L., Florio, A. A., Znaor, A., Ruggieri, D., Laversanne, M., Alvarez, C. S., Ferlay, J., Valery, P. C., Bray, F., & McGlynn, K. A.
- Affiliations
- Boston University (US)
- National Cancer Institute (US)
- Centre international de recherche sur le cancer (FR)
- Information Management Services (US)
- Division of Cancer Epidemiology and Genetics National Cancer Institute Bethesda MD
- QIMR Berghofer Medical Research Institute (AU)
- Corresponding author
- Petrick, Jessica L.
- ORCID
- Venue
- International Journal of Cancer
- Publisher
- Wiley
- Published
- 2019-11-05
- Volume
- 147
- Issue
- 2
- Pages
- 317-330
- ISSN
- 0020-7136 (ISSN-L)
- 1097-0215
- PMC
- PMC7470451
- OpenAlex
- W2980064491
- Cited by
- 594
- References
- 47
- Citations by year
- 2026: 49 · 2025: 100 · 2024: 116 · 2023: 129 · 2022: 117 · 2021: 63 · 2020: 17 · 2019: 1
- FWCI
- 31.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- International Journal of Cancer (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute
- Topics
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Oncology › Global Cancer Incidence and Screening
- Health Sciences › Medicine › Epidemiology › Hepatitis B Virus Studies
- Keywords
- hepatocellular carcinoma, primary liver cancer, cancer incidence trends, birth cohort analysis, age-standardized incidence rate, hepatitis B virus, hepatitis C virus, obesity, diabetes mellitus, global cancer epidemiology, incidence decline
- MeSH terms
- Africa, Asia, Europe, Female, Hepatitis B, Hepatitis C, Carcinoma, Hepatocellular, Humans, India, Liver Neoplasms, Male, Registries, Incidence, Seroepidemiologic Studies
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