Population attributable risk of aflatoxin-related liver cancer: Systematic review and meta-analysis
Open accessAbstract
BACKGROUND: Over 4 billion people worldwide are exposed to dietary aflatoxins, which cause liver cancer (hepatocellular carcinoma, HCC) in humans. However, the population attributable risk (PAR) of aflatoxin-related HCC remains unclear. METHODS: In our systematic review and meta-analysis of epidemiological studies, summary odds ratios (ORs) of aflatoxin-related HCC with 95% confidence intervals were calculated in HBV+ and HBV- individuals, as well as the general population. We calculated the PAR of aflatoxin-related HCC for each study as well as the combined studies, accounting for HBV status. RESULTS: Seventeen studies with 1680 HCC cases and 3052 controls were identified from 479 articles. All eligible studies were conducted in China, Taiwan, or sub-Saharan Africa. The PAR of aflatoxin-related HCC was estimated at 17% (14-19%) overall, and higher in HBV+ (21%) than HBV- (8.8%) populations. If the one study that contributed most to heterogeneity in the analysis is excluded, the summarised OR of HCC with 95% CI is 73.0 (36.0-148.3) from the combined effects of aflatoxin and HBV, 11.3 (6.75-18.9) from HBV only and 6.37 (3.74-10.86) from aflatoxin only. The PAR of aflatoxin-related HCC increases to 23% (21-24%). The PAR has decreased over time in certain Taiwanese and Chinese populations. CONCLUSIONS: In high exposure areas, aflatoxin multiplicatively interacts with HBV to induce HCC; reducing aflatoxin exposure to non-detectable levels could reduce HCC cases in high-risk areas by about 23%. The decreasing PAR of aflatoxin-related HCC reflects the benefits of public health interventions to reduce aflatoxin and HBV.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Extrapolating to other regions, aflatoxins amount to 127,330 cases and 1.6 million DALYs.
“Extrapolating to other regions, this amounts to 127,330 cases and 1.6 million DALYs.”
From Food Safety in Low and Middle Income Countries (2015) · cites this paper as [55]
The Discussion (page unavailable) extrapolates aflatoxin-attributable liver cancer to regions beyond Africa and Asia, estimating 105,000–142,000 potentially preventable cases annually; 127,330 falls within that range and equals 17% of the paper’s worldwide case estimate. The paper does not provide the claimed 1.6 million DALYs, and it cautions that its attributable-risk estimate may not apply to regions with much lower aflatoxin exposure. (LLM, conf=0.88)
Experimental — accuracy not yet measuredA second study suggested aflatoxins were responsible for 17% of hepato-cellular carcinoma or 88,400 cases (72,800-98,000) equivalent to 1.1 million DALYs.
“A second study by the same team based on literature from high aflatoxin areas (China and Sub-Saharan Africa) suggested aflatoxins were responsible for 17% of hepato-cellular carcinoma or 88,400 cases (72,800–98,000) equivalent to 1.1 million DALYs [55].”
From Food Safety in Low and Middle Income Countries (2015) · cites this paper as [55]
The Discussion (page not specified) estimates that aflatoxin accounts for 17% of HCC in the studied populations and projects 72,800–98,800 preventable cases annually across China, southeastern Asia, and sub-Saharan Africa. The cited sentence’s 88,400 cases is consistent with 17% of the paper’s roughly 520,000 annual cases, but its upper bound says 98,000 rather than 98,800. Our copy does not report the claimed 1.1 million DALYs. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & the PRISMA Group* (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00135 · Cited by 37,554 · see citing works
Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008
Ferlay, J., Shin, H., Bray, F., Forman, D., Mathers, C. D., & Parkin, D. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25516 · Cited by 21,271 · see citing works
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2009) · doi:10.1002/9780470743386 · Cited by 14,225 · see citing works
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2021) · doi:10.1002/9781119558378 · Cited by 9,799 · see citing works
Williams, J. H., Phillips, T. D., Jolly, P. E., Stiles, J. K., Jolly, C. M., & Aggarwal, D. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.5.1106 · Cited by 1,786 · see citing works
Global burden of aflatoxin-induced hepatocellular carcinoma: A risk assessment
Liu, Y., & Wu, F. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.0901388 · Cited by 1,224 · see citing works
Self-citationSome traditional herbal medicines, some mycotoxins, naphthalene and styrene.
(2002) · PubMed Central · Cited by 1,079 · see citing works
Mycotoxins and human disease: a largely ignored global health issue
Wild, C. P., & Gong, Y. Y. (2009) · Carcinogenesis · doi:10.1093/carcin/bgp264 · Cited by 987 · see citing works
Meta-Analysis, Decision Analysis, and Cost-Effectiveness Analysis
Petitti, D. B. (1999) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195133646.001.0001 · Cited by 928 · see citing works
Anttila, A., Bhat, R. V., Bond, J. A., Borghoff, S. J., Bosch, F. X., Carlson, G. P., Castegnaro, M., Cruzan, G., Gelderblom, W. C. A., Hass, U., et al. (2002) · Cited by 779 · see citing works
Urinary aflatoxin biomarkers and risk of hepatocellular carcinoma
Ross, R. K., Yu, M. C., Henderson, B. E., Yuan, J., Qian, G.-S., Tu, J.-T., Gao, Y.-T., Wogan, G. N., & Groopman, J. D. (1992) · The Lancet · doi:10.1016/0140-6736(92)91528-g · Cited by 725 · see citing works
Qian, G.-S., Ross, R. K., Yu, M. C., Yuan, J., Gao, Y. T., Henderson, B. E., Wogan, G. N., & Groopman, J. D. (1994) · PubMed · Cited by 666 · see citing works
Workgroup Report: Public Health Strategies for Reducing Aflatoxin Exposure in Developing Countries
Strosnider, H. M., Azziz‐Baumgartner, E., Bänziger, M., Bhat, R. V., Breiman, R. F., Bruné, M., DeCock, K. M., Dilley, A., Groopman, J. D., Hell, K., et al. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9302 · Cited by 539 · see citing works
Confidence Limits Made Easy: Interval Estimation Using a Substitution Method
Daly, L. (1998) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009523 · Cited by 289 · see citing works
Ming, L., Thorgeirsson, S. S., Gail, M. H., Lu, P., Harris, C. C., Wang, N.-J., Shao, Y., Wu, Z., Liu, G., Wang, X., et al. (2002) · Hepatology · doi:10.1053/jhep.2002.36366 · Cited by 233 · see citing works
Ser-249 p53 Mutations in Plasma DNA of Patients With Hepatocellular Carcinoma From The Gambia
Kirk, G. D., Camus-Randon, A.-M., Mendy, M. E., Goedert, J. J., Merle, P., TREPO, C. G., Bréchot, C., Hainaut, P. L., & Montesano, R. (2000) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/92.2.148 · Cited by 190 · see citing works
Kirk, G. D., Lesi, O. A., Mendy, M. E., Szymańska, K., Whittle, H. C., Goedert, J. J., Hainaut, P. L., & Montesano, R. (2005) · Oncogene · doi:10.1038/sj.onc.1208732 · Cited by 179 · see citing works
Climate change impacts on mycotoxin risks in US maize
Wu, F., Bhatnagar, D., Bui-Klimke, T. R., Carbone, I., Hellmich, R. L., Munkvold, G. P., Paul, P. A., Payne, G. A., & Takle, E. S. (2011) · World Mycotoxin Journal · doi:10.3920/wmj2010.1246 · Cited by 174 · see citing works
Self-citationElevated Aflatoxin Exposure and Increased Risk of Hepatocellular Carcinoma
Chen, C., Wang, L., Lu, S., Wu, M., You, S., Zhang, Y., Wang, L.-W., & Santella, R. M. (1996) · Hepatology · doi:10.1002/hep.510240108 · Cited by 173 · see citing works
Lunn, R. M., Zhang, Y. J., Wang, L., Chen, C., Lee, P., Lee, C. S., Tsai, W. Y., & Santella, R. M. (1997) · PubMed · Cited by 170 · see citing works
Aflatoxin B1 Exposure, Hepatitis B Virus Infection, and Hepatocellular Carcinoma in Taiwan
Wu, H.-C., Wang, Q., Yang, H., Ahsan, H., Tsai, W., Wang, L., Chen, S.-Y., Chen, C., & Santella, R. M. (2009) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0697 · Cited by 134 · see citing works
Yu, M., Lien, J.-P., Chiu, Y. H., Santella, R. M., Liaw, Y., & Chen, C. (1997) · Journal of Hepatology · doi:10.1016/s0168-8278(97)80178-x · Cited by 111 · see citing works
Chen, C., Yu, M., Liaw, Y., Wang, L. W., Chiamprasert, S., Matin, F., Hirvonen, A., Bell, D. A., & Santella, R. M. (1996) · PubMed Central · Cited by 109 · see citing works
Sun, C. (2001) · Carcinogenesis · doi:10.1093/carcin/22.8.1289 · Cited by 106 · see citing works
Confounding and Bias in the Attributable Fraction
Darrow, L. A., & Steenland, N. K. (2010) · Epidemiology · doi:10.1097/ede.0b013e3181fce49b · Cited by 96 · see citing works
Nia, A. B., Kim, S.-I., Hainaut, P. L., & Pfeifer, G. P. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.06.002 · Cited by 78 · see citing works
Omer, R. E., Kuijsten, A., Kadaru, A. M. Y., Kok, F. J., Idris, M. O., Khidir, I. M. E., & Veer, P. V. ’. (2004) · Nutrition and Cancer · doi:10.1207/s15327914nc4801_3 · Cited by 76 · see citing works
XPD codon 312 and 751 polymorphisms, and AFB1 exposure, and hepatocellular carcinoma risk
Long, X. D., Ma, Y., Zhou, Y. F., Yao, J. G., Ban, F., Huang, Y. Z., & Huang, B. C. (2009) · BMC Cancer · doi:10.1186/1471-2407-9-400 · Cited by 61 · see citing works
Huang, X. (2003) · World Journal of Gastroenterology · doi:10.3748/wjg.v9.i4.692 · Cited by 60 · see citing works
Szymańska, K., Chen, J., Cui, Y., Gong, Y. Y., Turner, P. C., Villar, S., Wild, C. P., Parkin, D. M., & Hainaut, P. L. (2009) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-1102 · Cited by 60 · see citing works
Peanut butter intake, GSTM1 genotype and hepatocellular carcinoma: a case–control study in Sudan
Omer, R. E., Verhoef, L. P. B., Veer, P. V., Idris, M. O., Kadaru, A. M. Y., Kampman, E., Bunschoten, A., & Kok, F. J. (2001) · Cancer Causes & Control · doi:10.1023/a:1008943200826 · Cited by 52 · see citing works
A case-control study of risk factors for hepatocellular carcinoma in Henan, China.
Zhang, J., Wang, X., Han, S. G., & Zhuang, H. (1998) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1998.59.947 · Cited by 46 · see citing works
Jiang, W., Wang, X. W., Unger, T., Forgues, M., Kim, J. W., Hussain, S. P., Bowman, E. D., Spillare, E. A., Lipsky, M. M., Meck, J. M., et al. (2009) · International Journal of Cancer · doi:10.1002/ijc.25118 · Cited by 42 · see citing works
Neoangiogenesis: A putative marker of malignancy in non-small-cell-lung-cancer (NSCLC) development
Fontanini, G., Vignati, S., Bigini, D., Lucchi, M., Mussi, A., Basolo, F., Angeletti, C. A., & Bevilacqua, G. (1996) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19960904)67:5 · Cited by 34 · see citing works
Efficacy of the nationwide hepatitis B infant vaccination program in Taiwan
Chen, S., Kung, C., Yang, W.-J., & Wang, H.-L. (2011) · Journal of Clinical Virology · doi:10.1016/j.jcv.2011.06.012 · Cited by 28 · see citing works
Iyer, S., & Groopman, J. D. (2011) · Molecular Carcinogenesis · doi:10.1002/mc.20767 · Cited by 26 · see citing works
Flagged first, then by citations
1 of the 39 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
A global view of hepatocellular carcinoma: trends, risk, prevention and management
Yang, J. D., Hainaut, P. L., Gores, G. J., Amadou, A., Plymoth, A., & Roberts, L. R. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0186-y · Cited by 4,233 · see citing works
Epidemiology of Hepatocellular Carcinoma
McGlynn, K. A., Petrick, J. L., & El‐Serag, H. B. (2020) · Hepatology · doi:10.1002/hep.31288 · Cited by 2,200 · see citing works
Global cancer in women: burden and trends.
Torre, L. A., Islami, F., Siegel, R. L., Ward, E. M., & Jemal, A. (2017) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-16-0858 · Cited by 1,245 · see citing works
Singal, A. G., Kanwal, F., & Llovet, J. M. (2023) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-023-00825-3 · Cited by 1,008 · 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
International trends in hepatocellular carcinoma incidence, 1978–2012
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. (2020) · International Journal of Cancer · doi:10.1002/ijc.32723 · Cited by 594 · see citing works
Public Health Impacts of Foodborne Mycotoxins
Wu, F., Groopman, J. D., & Pestka, J. J. (2014) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030713-092431 · Cited by 586 · see citing works
Self-citationFood Safety in Low and Middle Income Countries
Grace, D. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph120910490 · Cited by 544 · see citing works
Hepatocellular carcinoma epidemiology
Bosetti, C., Turati, F., & Vecchia, C. L. (2014) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2014.08.007 · Cited by 531 · see citing works
EASL Clinical Practice Guidelines on the management of hepatitis B virus infection
Cornberg, M., Sandmann, L., Jaroszewicz, J., Kennedy, P. T. F., Lampertico, P., Lemoine, M., Lens, S., Testoni, B., Wong, G. L., & Russo, F. P. (2025) · Journal of Hepatology · doi:10.1016/j.jhep.2025.03.018 · Cited by 480 · see citing works
Benefits and food safety concerns associated with consumption of edible insects
Imathiu, S. (2019) · NFS Journal · doi:10.1016/j.nfs.2019.11.002 · Cited by 440 · see citing works
Ochratoxin A and Human Health Risk: A Review of the Evidence
Bui-Klimke, T. R., & Wu, F. (2014) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2012.724480 · Cited by 401 · see citing works
Self-citationThe evolving epidemiology of hepatocellular carcinoma: a global perspective
Wallace, M. C., Preen, D. B., Jeffrey, G. P., & Adams, L. A. (2015) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2015.1028363 · Cited by 374 · see citing works
Edible insects as future food: chances and challenges
Lange, K. W., & Nakamura, Y. (2021) · Journal of Future Foods · doi:10.1016/j.jfutfo.2021.10.001 · Cited by 344 · see citing works
Projections of primary liver cancer to 2030 in 30 countries worldwide
Valery, P. C., Laversanne, M., Clark, P. J., Petrick, J. L., McGlynn, K. A., & Bray, F. (2017) · Hepatology · doi:10.1002/hep.29498 · Cited by 330 · see citing works
Hepatocellular carcinoma: updates on epidemiology, surveillance, diagnosis and treatment
Hwang, S. Y., Danpanichkul, P., Agopian, V. G., Mehta, N., Parikh, N. D., Abou‐Alfa, G. K., Singal, A. G., & Yang, J. D. (2024) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2024.0824 · Cited by 348 · see citing works
A Concise History of Mycotoxin Research
Pitt, J. I., & Miller, J. D. (2016) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.6b04494 · Cited by 302 · see citing works
Current cancer burden in China: epidemiology, etiology, and prevention
Cao, M., Li, H., Sun, D., He, S., Yan, X., Yang, F., Zhang, S., Xia, C., Lei, L., Peng, J., et al. (2022) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2022.0231 · Cited by 291 · see citing works
Worldwide incidence of hepatocellular carcinoma cases attributable to major risk factors
Baecker, A. S., Liu, X., Vecchia, C. L., & Zhang, Z. (2018) · European Journal of Cancer Prevention · doi:10.1097/cej.0000000000000428 · Cited by 277 · see citing works
Dietary mycotoxins, co-exposure, and carcinogenesis in humans: Short review
Ruyck, K. D., Boevre, M. D., Huybrechts, I., & Saeger, S. D. (2015) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2015.07.003 · Cited by 269 · see citing works
Comparison of hepatocellular carcinoma in <scp>E</scp> astern versus <scp>W</scp> estern populations
Choo, S. P., Tan, W. L., Goh, B. K. P., Tai, W. M., & Zhu, A. X. (2016) · Cancer · doi:10.1002/cncr.30237 · Cited by 264 · see citing works
Aflatoxins as a cause of hepatocellular carcinoma.
Kew, M. C. (2013) · PubMed · Cited by 263 · see citing works
Aflatoxin Exposure and Associated Human Health Effects, a Review of Epidemiological Studies
Gong, Y. Y., Watson, S., & Routledge, M. N. (2016) · Food Safety · doi:10.14252/foodsafetyfscj.2015026 · Cited by 255 · see citing works
Global impacts of aflatoxin in maize: trade and human health
Wu, F. (2014) · World Mycotoxin Journal · doi:10.3920/wmj2014.1737 · Cited by 231 · see citing works
Self-citationThe intestinal barrier as an emerging target in the toxicological assessment of mycotoxins
Akbari, P., Braber, S., Varasteh, S., Alizadeh, A., Garssen, J., & Fink‐Gremmels, J. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1794-8 · Cited by 211 · see citing works
Is it possible to halve the incidence of liver cancer in China by 2050?
Shi, J., Cao, M., Wang, Y., Bai, F., Lei, L., Peng, J., Feletto, E., Canfell, K., Qu, C., & Chen, W. (2020) · International Journal of Cancer · doi:10.1002/ijc.33313 · Cited by 180 · 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
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
Self-citationGenetic Features of Aflatoxin-Associated Hepatocellular Carcinoma
Zhang, W., He, H., Zang, M., Wu, Q., Zhao, H., Lu, L.-L., Ma, P., Zheng, H., Wang, N.-J., Zhang, Y., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.03.024 · Cited by 165 · see citing works
Aflatoxin contamination of milk and dairy feeds in the Greater Addis Ababa milk shed, Ethiopia
Gizachew, D., Szonyi, B., Tegegne, A., Hanson, J., & Grace, D. (2015) · Food Control · doi:10.1016/j.foodcont.2015.06.060 · Cited by 163 · see citing works
Changing epidemiology of hepatocellular carcinoma in Asia
Goh, G. B., Chang, J. P.-E., & Tan, C. (2015) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2015.09.007 · Cited by 149 · see citing works
Zheng, C., Zeng, H., Lin, H., Wang, J., Feng, X., Qiu, Z., Chen, J., Luo, J., Luo, Y., Huang, Y., et al. (2017) · Hepatology · doi:10.1002/hep.29310 · Cited by 149 · see citing works
Review of the Biological and Health Effects of Aflatoxins on Body Organs and Body Systems
Godfrey, S., Kitya, D., Lubega, A. M., Ogwal-Okeng, J. W., William, W., & David, B. P. (2013) · InTech eBooks · doi:10.5772/51201 · Cited by 142 · see citing works
Natural Occurrence of Mycotoxins in Food and Feed: Pakistan Perspective
Ashiq, S. (2014) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12122 · Cited by 139 · see citing works
Hepatocellular carcinoma: epidemiology and risk factors
Kew, M. C. (2014) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s44381 · Cited by 136 · see citing works
Feng, R., Su, Q., Huang, X., Basnet, T. B., Xu, X., & Ye, W. (2022) · 癌症：英文版 · doi:10.1002/cac2.12393 · Cited by 130 · see citing works
Wu, F., Stacy, S. L., & Kensler, T. W. (2013) · Toxicological Sciences · doi:10.1093/toxsci/kft132 · Cited by 119 · see citing works
Self-citationAttributable Causes of Liver Cancer Mortality and Incidence in China
Fan, J., Wang, J.-B., Jiang, Y. L., Xiang, W., Liang, H., Wei, W., Qiao, Y., & Boffetta, P. (2013) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2013.14.12.7251 · Cited by 116 · see citing works
Battlefield against hepatitis B infection and HCC in Africa
Lemoine, M., & Thursz, M. R. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.10.013 · Cited by 114 · see citing works
Liu, X., Guan, X., Xing, F., Lv, C., Dai, X., & Liu, Y. (2017) · Food Control · doi:10.1016/j.foodcont.2017.07.012 · Cited by 114 · see citing works
Self-citationMeta-analysis of DNA methylation biomarkers in hepatocellular carcinoma
Zhang, C., Li, J., Huang, T., Duan, S., Dai, D., Jiang, D., Sui, X., Li, D., Chen, Y., Ding, F., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.13221 · Cited by 105 · see citing works
Aflatoxin contamination of groundnut and maize in Zambia: observed and potential concentrations
Kachapulula, P. W., Akello, J., Bandyopadhyay, R., & Cotty, P. J. (2017) · Journal of Applied Microbiology · doi:10.1111/jam.13448 · Cited by 105 · see citing works
Mao, J., Li, P., Wang, J., Wang, H., Zhang, Q., Zhang, L., Lĭ, H., Zhang, W., & Peng, T. (2019) · Applied Catalysis B: Environmental · doi:10.1016/j.apcatb.2019.01.057 · Cited by 102 · see citing works
Hepatocellular Carcinoma in Sub-Saharan Africa
Mukthinuthalapati, V., Sewram, V., Ndlovu, N., Kimani, S., Abdelaziz, A., Chiao, E., & Abou-Alfa, G. (2021) · JCO Global Oncology · doi:10.1200/go.20.00425 · Cited by 76 · see citing works
Management of people with early- or very early-stage hepatocellular carcinoma
Majumdar, A., Roccarina, D., Thorburn, D., Davidson, B. R., Tsochatzis, E. A., & Gurusamy, K. S. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011650.pub2 · Cited by 94 · see citing works
Lin, H., Liu, W., Zeng, H., Pu, C., Zhang, R., Qiu, Z., Chen, J.-A., Wang, L., Tan, Y., Zheng, C., et al. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.6b01062 · Cited by 91 · see citing works
A review on the relation between soil and mycotoxins: Effect of aflatoxin on field, food and finance
Winter, G., & Pereg, L. L. (2019) · European Journal of Soil Science · doi:10.1111/ejss.12813 · Cited by 89 · see citing works
Tornesello, M., Buonaguro, L., Izzo, F., & Buonaguro, F. (2016) · OncoTarget · doi:10.18632/oncotarget.7837 · Cited by 79 · see citing works
Jin, S., Pang, Q., Yang, H., Diao, X., Shan, A., & Feng, X. (2021) · Food Chemistry · doi:10.1016/j.foodchem.2021.130263 · Cited by 86 · see citing works
Unravelling the pathways of air plasma induced aflatoxin B1 degradation and detoxification
Hojnik, N., Modic, M., Walsh, J. L., Žigon, D., Javornik, U., Plavec, J., Žegura, B., Filipič, M., & Cvelbar, U. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123593 · Cited by 81 · see citing works
Alcohol consumption and liver cancer risk: a meta-analysis
Chuang, S., Lee, Y.-C. A., Wu, G.-J., Straíf, K., & Hashibe, M. (2015) · Cancer Causes & Control · doi:10.1007/s10552-015-0615-3 · Cited by 79 · see citing works
Hepatocellular carcinoma and the risk of occupational exposure
Rapisarda, V., Loreto, C., Malaguarnera, M., Ardiri, A., Proiti, M., Giuseppe, R., Frazzetto, E., Ruggeri, M. I., Malaguarnera, G., Bertino, N., et al. (2016) · World Journal of Hepatology · doi:10.4254/wjh.v8.i13.573 · Cited by 79 · see citing works
Contamination of Aflatoxins Induces Severe Hepatotoxicity Through Multiple Mechanisms
Hua, Z., Liu, R., Chen, Y., Liu, G., Li, C., Song, Y., Cao, Z., Li, W., Lu, C. C., Lu, C. C., et al. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.605823 · Cited by 78 · see citing works
Self-citationZhang, Y., Zhang, J. C., Xu, W., Xiao, G., Ding, J., & Chen, X. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.07.021 · Cited by 75 · see citing works
Probabilistic risk assessment of dietary exposure to aflatoxin B1 in Guangzhou, China
Zhang, W., Liu, Y., Liang, B., Zhang, Y., Zhong, X., Luo, X., Huang, J., Wang, Y., Cheng, W., & Chen, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-64295-8 · Cited by 75 · see citing works
Self-citationKachapulula, P. W., Akello, J., Bandyopadhyay, R., & Cotty, P. J. (2017) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2017.08.014 · Cited by 73 · see citing works
Li, M., Cao, S., & Xu, R. (2025) · 癌症：英文版 · doi:10.1002/cac2.70017 · Cited by 80 · see citing works
Aflatoxin Regulations and Global Pistachio Trade: Insights from Social Network Analysis
Bui-Klimke, T. R., Güçlü, H., Kensler, T. W., Yuan, J., & Wu, F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092149 · Cited by 72 · see citing works
Self-citationNon-infective occupational risk factors for hepatocellular carcinoma: A review
Ledda, C., Loreto, C., Zammit, C., Marconi, A., Fago, L., Matera, S., Costanzo, V., Sanzà, G. F., Palmucci, S., Ferrante, M., et al. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.6046 · Cited by 70 · see citing works
Animal Models of Hepatocellular Carcinoma: The Role of Immune System and Tumor Microenvironment
Jílková, Z. M., Kurma, K., & Decaens, T. (2019) · Cancers · doi:10.3390/cancers11101487 · Cited by 70 · see citing works
Research progress in toxicological effects and mechanism of aflatoxin B 1 toxin
Li, C., Liu, X., Wu, J., Ji, X., & Xu, Q. (2022) · PeerJ · doi:10.7717/peerj.13850 · Cited by 67 · see citing works
Bioenzymatic detoxification of mycotoxins
Liu, M., Zhang, X., Luan, H., Zhang, Y., Xu, W., Feng, W., & Song, P. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1434987 · Cited by 67 · see citing works
Epidemiology of Primary Liver Cancer in Serbia and Possible Connection With Cyanobacterial Blooms
Svirčev, Z. B., Drobac, D., Tokodi, N., Vidović, M., Simeunović, J. B., Miladinov-Mikov, M., & Baltić, V. (2013) · Journal of Environmental Science and Health Part C · doi:10.1080/10590501.2013.824187 · Cited by 67 · see citing works
Smith, J. W., Kroker-Lobos, M. F., Lazo, M., Rivera‐Andrade, A., Egner, P. A., Wedemeyer, H. H., Torres, O. R., Freedman, N. D., McGlynn, K. A., Güallar, E., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0189255 · Cited by 69 · see citing works
Tai, B., Chang, J., Liu, Y., & Xing, F. (2020) · Food Quality and Safety · doi:10.1093/fqsafe/fyz040 · Cited by 66 · see citing works
Self-citationHuang, G., Tang, B., TANG, K., Dong, X., Deng, J., Liao, L., Liao, Z., Yang, H., & He, S. (2014) · Oncology Reports · doi:10.3892/or.2014.3099 · Cited by 66 · see citing works
RetractedGemede, H. F. (2025) · Toxins · doi:10.3390/toxins17070331 · Cited by 65 · see citing works
Perspective: Time to face the fungal threat
Wu, F. (2014) · Nature · doi:10.1038/516s7a · Cited by 63 · see citing works
Self-citationCancer “Causation” by Infections—Individual Contributions and Synergistic Networks
Hausen, H. Z., & de Villiers, E. (2014) · Seminars in Oncology · doi:10.1053/j.seminoncol.2014.10.003 · Cited by 62 · see citing works
Hepatocellular Carcinoma: Epidemiology, Screening, and Assessment of Hepatic Reserve
Frager, S. Z., & Schwartz, J. M. (2020) · Current Oncology · doi:10.3747/co.27.7181 · Cited by 60 · see citing works
Changing Epidemiology of Hepatocellular Carcinoma Within the United States and Worldwide
Rich, N. E. (2023) · Surgical Oncology Clinics of North America · doi:10.1016/j.soc.2023.06.004 · Cited by 60 · see citing works
Ortega‐Beltran, A., Moral, J., Picot, A., Puckett, R. D., Cotty, P. J., & Michailides, T. J. (2019) · Plant Disease · doi:10.1094/pdis-08-18-1333-re · Cited by 60 · see citing works
Risk factors for hepatocellular carcinoma: an umbrella review of systematic review and meta-analysis
Wang, J., Qiu, K., Zhou, S., Gan, Y., Jiang, K., Wang, D., & Wang, H. (2025) · Annals of Medicine · doi:10.1080/07853890.2025.2455539 · Cited by 59 · see citing works
Early‐life exposures to infectious agents and later cancer development
Vedham, V., Verma, M., & Mahabir, S. (2015) · Cancer Medicine · doi:10.1002/cam4.538 · Cited by 57 · see citing works
Chilaka, C. A., & Mally, A. (2020) · Foods · doi:10.3390/foods9111585 · Cited by 57 · see citing works
Hepatocellular carcinoma: From clinical practice to evidence-based treatment protocols
Galun, D. A. (2015) · World Journal of Hepatology · doi:10.4254/wjh.v7.i20.2274 · Cited by 56 · see citing works
Stella, L., Santopaolo, F., Gasbarrini, A., Pompili, M., & Ponziani, F. R. (2022) · World Journal of Gastroenterology · doi:10.3748/wjg.v28.i21.2251 · Cited by 52 · see citing works
Aflatoxins in food products consumed in Brazil: a preliminary dietary risk assessment
Andrade, P. D., Homem-de-Mello, M., de França, J. A., & Caldas, E. D. (2012) · Food Additives & Contaminants Part A · doi:10.1080/19440049.2012.720037 · Cited by 52 · see citing works
Liu, W., Wang, L., Yang, X., Zeng, H., Zhang, R., Pu, C., Zheng, C., Tan, Y., Luo, Y., Feng, X., et al. (2017) · Environmental Science & Technology · doi:10.1021/acs.est.6b05404 · Cited by 51 · see citing works
Li, J., Zhao, X., Chen, L., Qian, H., Wang, W., Yang, C., & Yan, X. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.9b03579 · Cited by 51 · see citing works
Hepatocellular carcinoma: measures to improve the outlook in sub-Saharan Africa
Spearman, C. W., Dusheiko, G. M., Jonas, E., Abdo, A. E., Afihene, M., Cunha, L., Desalegn, H., Kassianides, C., Katsidzira, L., Kramvis, A., et al. (2022) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(22)00041-3 · Cited by 50 · see citing works
Mahjoory, Y., Mohammadi, R., Hejazi, M. A., & Nami, Y. (2023) · Scientific Reports · doi:10.1038/s41598-023-27721-1 · Cited by 50 · see citing works
Balan, B., Dhaulaniya, A. S., Kumar, M., Kumar, M., & Kumar, P. (2024) · Food Safety and Health · doi:10.1002/fsh3.12030 · Cited by 55 · see citing works
How climate change and regulations can affect the economics of mycotoxins
Wu, F., & Mitchell, N. J. (2016) · World Mycotoxin Journal · doi:10.3920/wmj2015.2015 · Cited by 50 · see citing works
Self-citationAflatoxin Contamination of Dried Insects and Fish in Zambia
Kachapulula, P. W., Akello, J., Bandyopadhyay, R., & Cotty, P. J. (2018) · Journal of Food Protection · doi:10.4315/0362-028x.jfp-17-527 · Cited by 49 · see citing works
Thymol Induces Conidial Apoptosis in Aspergillus flavus via Stimulating K + Eruption
Hu, L., Ban, F., Li, H., Qian, P.-P., Shen, Q., Zhao, Y., Mo, H., & Zhou, X. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b02117 · Cited by 48 · see citing works
Toxopathological and cytogenetic effects of aflatoxin B1 (AFB1) on pregnant rats
Fetaih, H., Dessouki, A. A., Hassanin, A. A. I., & Tahan, A. S. (2014) · Pathology - Research and Practice · doi:10.1016/j.prp.2014.06.001 · Cited by 47 · see citing works
Quang, E. V., Shimakawa, Y., & Nahon, P. (2021) · Liver International · doi:10.1111/liv.14843 · Cited by 47 · see citing works
Risk Assessment of Upper Tract Urothelial Carcinoma Related to Aristolochic Acid
Wu, F., & Wang, T. (2013) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-12-1386 · Cited by 46 · see citing works
Self-citationBurden of Disease Associated with Dietary Exposure to Aflatoxins in China in 2020
Chen, T., Liu, J., Li, Y., & Wei, S. (2022) · Nutrients · doi:10.3390/nu14051027 · Cited by 46 · see citing works
Reduced Foodborne Toxin Exposure Is a Benefit of Improving Dietary Diversity
Wu, F., Mitchell, N. J., Male, D., & Kensler, T. W. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu137 · Cited by 45 · see citing works
Self-citationHan, C., Zhai, W., Wang, Y., Cao, J., & Wang, M. (2022) · Food Control · doi:10.1016/j.foodcont.2022.109228 · Cited by 45 · see citing works
A SERS-based competitive immunoassay for highly sensitive and specific detection of ochratoxin A
Ding, Y., Shang, H., Wang, X., & Chen, L. (2020) · The Analyst · doi:10.1039/d0an01220c · Cited by 44 · see citing works
Jin, S., Yang, H., Wang, Y., Pang, Q., Jiao, Y., Shan, A., & Feng, X. (2021) · Foods · doi:10.3390/foods10123086 · Cited by 43 · see citing works
Cold atmospheric pressure plasma‐assisted removal of aflatoxin B1 from contaminated corn kernels
Hojnik, N., Modic, M., Žigon, D., Kovač, J., Jurov, A., Dickenson, A., Walsh, J. L., & Cvelbar, U. (2020) · Plasma Processes and Polymers · doi:10.1002/ppap.202000163 · Cited by 42 · see citing works
Search for aflatoxin and trichothecene production inhibitors and analysis of their modes of action
Sakuda, S., Yoshinari, T., Furukawa, T., Jermnak, U., Takagi, K., Iimura, K., Yamamoto, T., Suzuki, M., & Nagasawa, H. (2015) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2015.1086261 · Cited by 41 · see citing works
Aflatoxin and the aetiology of liver cancer and its implications for Guatemala
Groopman, J. D., Smith, J. W., Rivera‐Andrade, A., Álvarez, C. S., Kroker-Lobos, M. F., Egner, P. A., Gharzouzi, E., Dean, M. C., McGlynn, K. A., & Ramírez‐Zea, M. (2021) · World Mycotoxin Journal · doi:10.3920/wmj2020.2641 · Cited by 41 · see citing works
Mycotoxin in the food supply chain—implications for public health program
Milićević, D. R., Nastasijević, I., & Petrović, Ž. (2016) · Journal of Environmental Science and Health Part C · doi:10.1080/10590501.2016.1236607 · Cited by 41 · see citing works
Environmental Health Research in Africa: Important Progress and Promising Opportunities
Joubert, B. R., Mantooth, S., & McAllister, K. A. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2019.01166 · Cited by 40 · see citing works
Fungal diversity and mycotoxin contamination in dried fish products in Zhanjiang market, China
Deng, Y., Wang, Y., Deng, Q., Sun, L., Wang, R., Ye, L., Tao, S., Liao, J., & Gooneratne, R. (2020) · Food Control · doi:10.1016/j.foodcont.2020.107614 · Cited by 40 · see citing works
- Authors
- Liu, Y., Chang, C.-C. H., Marsh, G. M., & Wu, F.
- Affiliations
- University of Pittsburgh (US)
- Corresponding author
- Wu, Felicia
- Venue
- European Journal of Cancer
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 48
- Issue
- 14
- Pages
- 2125-2136
- ISSN
- 0959-8049 (ISSN-L)
- PMC
- PMC3374897
- OpenAlex
- W1978322476
- Cited by
- 372
- References
- 39
- Citations by year
- 2026: 22 · 2025: 42 · 2024: 26 · 2023: 30 · 2022: 35 · 2021: 28 · 2020: 22 · 2019: 26 · 2018: 20 · 2017: 29 · 2016: 24 · 2015: 24 · 2014: 16 · 2013: 23 · 2012: 5
- FWCI
- 2.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- European Journal of Cancer (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA153073)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Mycotoxins in Agriculture and Food
- Health Sciences › Medicine › Hepatology › Hepatocellular Carcinoma Treatment and Prognosis
- Health Sciences › Medicine › Epidemiology › Hepatitis B Virus Studies
- Keywords
- aflatoxins, hepatocellular carcinoma, population attributable risk, hepatitis B virus, dietary exposure, cancer prevention, public health interventions
- MeSH terms
- Adolescent, Adult, Aflatoxins, Aged, Aged, 80 and over, China, Female, Food Contamination, Hepatitis B, Hepatitis B Surface Antigens, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Male, Middle Aged, Risk Factors, Taiwan, Biomarkers, Odds Ratio, Case-Control Studies, Africa South of the Sahara, Risk Assessment, Young Adult
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
