Fumonisins in China: update on occurrence, epidemiology, exposure and regulation

Main Article Content

J. Chen
Z. Jia
J. Song
Y. Yuan
L. Zhang

Keywords

China, contamination, exposure, fumonisins, legislation

Abstract



Fumonisins (FBs) are one of the most frequently occurring mycotoxins in China. FBs have attracted worldwide attention because of the significant economic losses they cause as well as their impact on human health and animal productivity. FBs have been associated with high incidences of oesophageal and liver cancer in several areas in China. However, the extrapolation of the effects of FBs on humans has always been inaccurate, which can be explained by the lack of adequate food consumption data, lack of knowledge about related health risks associated with specifically proposed limits, and the possibility of synergism with other mycotoxins present in the same food commodities. Domestic legislation is necessary to control contamination by FBs. The assessment of fumonisin exposure and development of preventative strategies in China depend not only on the determination of fumonisin levels in food contributors but also on the distinct dietary patterns of a specific population. Although limited data is available, this review aims to critically evaluate the extent of fumonisin contamination in China as well as epidemiologic studies and human exposure estimates. This review also aims to establish perspectives to aid future research and legislation.




 
Abstract 321 | PDF Downloads 323

References

Abnet, C.C., Borkowf, C.B., Qiao, Y.L., Albert, P.S., Wang, E., Merrill Jr., A.H., Mark, S.D., Dong, Z.W., Taylor, P.R. and Dawsey, S.M., 2001a. Sphingolipids as biomarkers of fumonisin exposure and risk of esophageal squamous cell carcinoma in China. Cancer Causes Control 12: 821-828.
Abnet, C.C., Borkowf, C.B., Qiao, Y.-L., Albert, P.S., Wang, E., Merrill Jr., A.H., Mark, S.D., Dong, Z.W., Taylor, P.R. and Dawsey, S.M., 2001b. A cross-sectional study of human serum sphingolipids, diet and physiologic parameters. Journal of Nutrition 131: 2748-2752.
Arino, A., Juan, T., Estopanan, G. and Gonzalez-Cabo, J.F., 2007. Natural occurrence of Fusarium species, fumonisin production by toxigenic strains, and concentrations of fumonisins B1 and B2 in conventional and organic maize grown in Spain. Journal of Food Protection 70: 151-156.
Burger, H.M., Lombard, M.J., Shephard, G.S., Rheeder, J.R., Van der Westhuizen, L. and Gelderblom, W.C., 2010. Dietary fumonisin exposure in a rural population of South Africa. Food and Chemical Toxicololgy 48: 2103-2108.
Castells, M., Marin, S., Sanchis, V. and Ramos, A.J., 2008. Distribution of fumonisins and aflatoxins in corn fractions during industrial cornflake processing. International Journal of Food Microbiology 123: 81-87.
Chu, F.S. and Li, G.Y., 1994. Simultaneous occurrence of fumonisin B1 and other mycotoxins in moldy corn collected from the people’s Republic of China in regions with high incidences of esophageal cancer. Applied and Environmental Microbiology 60: 847-852.
Delongchamp, R.R. and Young, J.F., 2001. Tissue sphinganine as a biomarker of fumonisin-induced apoptosis. Food Additives and Contaminants 18: 255-261.
De Nijs, M., Van Egmond, H.P., Nauta, M., Rombouts, F.M. and Notermans, S.H., 1998. Assessment of human exposure to fumonisin B1. Journal of Food Protection 61: 879-884.
Domijan, A.M., Peraica, M., Jurjevic, Z., Ivic, D. and Cvjetkovic, B., 2005. Fumonisin B1, fumonisin B2, zearalenone and ochratoxin A contamination of maize in Croatia. Food Additives and Contaminants 22: 677-680.
European Commission (EC), 2007. Commission Regulation (EC) no. 2007/1126 of 28 September 2007 amending Regulation (EC) no. 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards Fusarium toxins in maize and maize products. Official Journal of the European Union L255: 14-17.
European Food Safety Authority (EFSA), 2011. Joint guidance of EFSA, FAO and WHO. Towards a harmonised total diet study approach: a guidance document. EFSA, Parma, Italy. Available at: http://www.efsa.europa.eu/en/efsajournal/doc/2450.pdf.
Feng, Y.Z., Lu, X.H., Tao, B., Pang, M.H., Liu, Y.C. and Dong, J.G., 2011. Natural occurrence of fumonisins B1 and B2 in corn from three main production provinces in China. Journal of Food Protection 74: 1374-1378.
Food and Drug Administration (FDA), 2001. Fumonisin levels in human foods and animal feeds. Guidance for industry. Available at: http://www.fda.gov/food/guidanceregulation/guidancedocumentsregulatoryinformation/chemicalcontaminantsmetalsnaturaltoxinspesticides/ucm109231.htm.
Franceschi, S., Bidoli, E., Baron, A.E. and La Vecchia, C., 1990. Maize and risk of cancers of the oral cavity, pharynx and esophagus in Northeastern Italy. Journal of National Cancer Institute 82: 1407-1411.
Gao, H.P. and Yoshizawa, T., 1997. Further study on Fusarium mycotoxins in corn and wheat from a high-risk area for human esophageal cancer in China. Mycotoxins 45: 51-55.
Gelderblom, W.C., Abel, S., Smuts, C.M., Marnewick, J., Marasas, W.F., Lemmer, E.R. and Ramljak, D., 2001. Fumonisin-induced hepatocarcinogenesis: mechanisms related to cancer initiation and promotion. Environmental Health Perspectives 109: 291-300.
Gelderblom, W.C.A., Jaskiewicz, K., Marasas, W.F.O., Thiel, P.G., Horak, R.M., Vleggar, R. and Kriek, N.P., 1988. Fumonisins-novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Applied and Environmental Microbiology 54: 1806-1811.
Gelderblom, W.C.A., Kriek, N.P., Marasas, W.F. and Thiel, P.G., 1991. Toxicity and carcinogenicity of the Fusarium moniliformemetabolite, fumonisin B1, in rats. Carcinogenesis 12: 1247-1251.
Gelderblom, W.C.A., Semple, E., Marasas, W.F.O. and Farber, E., 1992. The cancer initiating potential of the fumonisin mycotoxins produced by Fusarium moniliforme. Carcinogenesis 13: 433-437.
Gelderblom, W.C.A. and Snyman, S.D., 1991. Mutagenicity of potentially carcinogenic mycotoxins produced by Fusarium moniliforme. Mycotoxin Research 7: 46-52.
Gong, H.Z., Ji, R., Li, Y.X., Zhang, H.Y., Li, B., Zhao, Y., Sun, L., Yu, F. and Yang J., 2009. Occurrence of fumonisin B(1) in corn from the main corn-producing areas of China. Mycopathologia 167: 31-36.
Groves, F.D., Zhang, L., Chang, Y.S., Ross, P.F., Casper, H., Norred, W.P., You, W.C. and Fraumeni Jr., J.F., 1999. Fusarium mycotoxins in corn and corn products in a high-risk area for gastric cancer in Shandong Province, China.Journal of AOAC International 82: 657-662.
Guo, Y., Liu, X. and Liu, J., 1999. Studies on immunoassay for detecting fumonisin B1. Journal of Hygienic Research 28: 238-241.
Harrison, L.R., Colvin, B.M., Green, J.T., Newman, L.E. and Cole Jr., J.R., 1990. Pulmonary edema and hyfrotorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. Journal of Veterinary Diagnostic Investigation 2: 217-221.
He, S., Xin, Y. and Liu, J., 1999. An investigation on the contamination of fungi and mycotoxins in staple crops in Sichuan province. Journal of Preventive Medicine Information 15: 199-202.
Hennigen, M.R., Valente Soares, L.M., Sanchez, S., Di Benedetto, N.M., Longhi, A., Eyherabide, G., Torroba, J. and Zanelli, M., 2000. Fumonisins in corn hybrids grown in Argentina for 2 consecutive seasons. In: De Koe, W.J., Samson, R.A., Van Egmond, H.P., Gilbert, J. and Sabino, M. (eds.) Proceedings of the Xth international IUPAC symposium on mycotoxins and phycotoxins May 21-25, 2000, Guaruja, Brazil, pp. 331-339.
International Agency for Research on Cancer (IARC), 1993. Toxins derived from Fusarium moniliforme: fumonisins B1 and B2 and fusarin C. In: Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, volume 56. IARC, Lyon, France, pp. 445-466.
Joint FAO/WHO Expert Committee on Food Additives (JECFA), 2001. Safety evaluation of certain mycotoxins in food. WHO Food Additives Series 47: 103-279.
Kellerman, T.S., Marasas, W.F., Thiel, P.G., Gelderblom, W.C., Cawood, M. and Coetzer J.A., 1990. Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. Onderstepoort Journal of Veterinary Research 57: 269-275.
Kuiper-Goodman, T., Scott, P.M., McEwen, N.P., Lombaert G.A. and Ng, W., 1996. Approaches to the risk assessment of fumonisins in corn-based foods in Canada. Advances in Experimental and Medicine Biology 392: 369-393.
Li, F.Q., Yoshizawa, T., Kawamura, O., Luo, X.Y. and Li, Y.W., 2001. Aflatoxins and fumonisins in corn from the high-incidence area for human hepatocellular carcinoma in Guangxi, China. Journal of Agricultural and Food Chemistry 49: 4122-4126.
Li, J.Y., Ershow, A.G., Chen, Z.J., Wacholder, S., Li, G.Y., Guo, W., Li, B. and Blot, W.J., 1989. A case-control study of cancer of the esophagus and gastric cardia in Linxian.International Journal of Cancer 43: 755-761.
Lineback, D.R., Pirlet, A., Van der Kamp, J.W. and Wood, R., 2009. Globalization, food safety issues and role of international standards. Quality Assurance and Safety of Crops & Foods 1: 23-27.
Lino, C.M., Silva, L.G., Pena, A.L. and Silveira, M.I., 2006. Determination of fumonisins B1 and B2 in Portuguese maize and maize-based samples by HPLC with fluorescence detection. Analytical and Bioanalytical Chemistry 384: 1214-1220.
Liu, Q., Liu, G. and Liu, H., 2008. Investigation into the status of contamination of strong carcinogen – fumonisin in peanut and corn and their products and rapid detection. China Tropical Medicine 8: 1906-1909.
Lv, B., Xie, M. and Yang, X., 2005. Contamination of fumonisin B(1) in staple crops in Hubei province of China. Journal of Public Health and Prevention Medince 16: 60-61.
Marasas, W.F., Kellerman, T.S., Gelderblom, W. C., Coetzer, J.A., Thiel, P. G. and Van der Lugt J.J., 1988. Leukoencephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme. Onderstepoort Journal of Veterinary Research 55: 197-203.
Marasas, W.F.O., Riley, R.T., Hendricks, K.A., Stevens, V.L., Sadler, T.W., Gelineau-Van Waes, J., Missmer, S.A., Cabrera, J., Torres, O., Gelderblom, W.C., Allegood, J., Martínez, C., Maddox, J., Miller, J.D., Starr, L., Sullards, M.C., Roman, A.V., Voss, K.A., Wang, E. and Merrill Jr., A.H., 2004. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin contaminated maize. Journal of Nutrition134: 711-716.
Martins, M.L., Martins, H.M. and Bernardo, F., 2001. Fumonisins B1and B2 in black tea and medicinal plants. Journal of Food Protection 64: 1268-1270.
Missmer, S.A., Suarez, L., Felkner, M., Wang, E., Merrill Jr., A.H., Rothman, K.J. and Hendricks K.A., 2006. Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environmental Health Perspect 114: 237-241.
Moore, C.A., Li, S., Li, Z., Hong, S., Gu, H., Berry, R.J., Mulinare, J. and Erickson, J.D., 1997. Elevated rates of severe neural tube defects in a high-prevalence area in northern China. American Journal of Medical Genetics 73: 113-118.
National Toxicology Program (NTP), 2001. Technical report on the toxicology and carcinogenesis studies of fumonisin B1 (CAS no. 116355-83-0) in F344 rats and B6C3F1 mice (feed studies). NTP Technical Report 496. NTP, Research Triangle Park, NC, USA.
Norred, W.P., Plattner, R.D., Vesonder, R.F., Bacon, C.W. and Voss, K.A., 1992. Effects of selected secondary metabolites of Fusarium moniliforme on unscheduled synthesis of DNA by rat primary hepatocytes. Food and Chemical Toxicology 30: 233-237.
Omurtag, G.Z. and Yazicioglu, D., 2004. Determination of fumonisins B1 and B2 in herbal tea and medical plants in Turkey by high-performance liquid chromatography. Journal of Food Protection 67: 1782-1786.
Persson, E.C., Sewram, V., Evans, A.A., London, W.T., Volkwyn, Y., Shen, Y.J., Van Zyl, J.A., Chen, G., Lin, W., Shephard, G.S., Taylor, P.R., Fan, J.H., Dawsey, S.M., Qiao, Y.L., McGlynn, K.A. and Abnet, C.C., 2012. Fumonisin B1 and risk of hepatocellular carcinoma in two Chinese cohorts. Food and Chemical Toxicology 50: 679-683.
Pietri, A., Bertuzzi, T., Agosti, B. and Donadini, G., 2010. Transfer of aflatoxin B1 and fumonisin B1 from naturally contaminated raw materials to beer during an industrial brewing process. Food Additives and Contaminants Part A 27: 1431-1439.
Pocsfalvi, G., Ritieni, A., Randazzo, G., Dobó, A. and Malorni, A., 2000. Interaction of Fusarium mycotoxins, fusaproliferin and fumonisin B1 with DNA studied by electrospray ionization mass spectrometry. Journal of Agricultural and Food Chemistry 48: 5795-5801.
Qiu, M. and Liu, X., 2001. Determination of sphinganine, sphingosine and Sa/So ratio in urine of humans exposed to dietary fumonisin B1. Food Additives and Contaminants Part A 18: 263-269.
Rheeder, J.P., Marasas, W.F.O., Thiel, P.G., Sydenham, E.W., Shepard, G.S. and Van Schalkwyk, D.J., 1992. Fusarium moniliforme and fumonisins in corn in relation to human oesophageal cancer in Transkei. Phytopathology 82: 353-357.
Riley, R.T., Hinton, D.M., Chamberlain, W.J., Bacon, C.W., Wang, E., Merrill Jr., A.H. and Voss, K.A., 1994. Dietary fumonisin B1 induces disruption of sphingolipid metabolism in Sprague–Dawley rats: a new mechanism of nephrotoxicity. Journal of Nutrition 124: 594-603.
Scientific Committee on Food (SCF), 2000. Opinion of the scientific committee on food on Fusarium toxins. Part 3: fumonisin B1 (FB1). SCF, Brussels, Belgium. Available at: http://ec.europa.eu/food/fs/sc/scf/out73_en.pdf.
Scientific Committee on Food (SCF), 2003. Updated opinion of the scientific committee on food on fumonisin B1, B2 and B3. S C F, Brussels, Belgium. Available at: http://ec.europa.eu/food/fs/sc/scf/out185_en.pdf.
Scott, P.M. and Lawrence, G.A., 1995. Analysis of beer for fumonisins. Journal of Food Protection 58: 1379-1382.
Shale, K., Mukamugema, J., Lues, R.J. and Venter, P., 2012. Toxicity profile of commercially produced indigenous banana beer. Food Additives and Contaminants Part A 29: 1300-1306.
Shephard, G.S., Leggott, N.L., Stockenström, S., Somdyala, N.I.M. and Marasas, W.F.O., 2002. Preparation of South African maize porridge: effect on fumonisin levels.South African Journal of Science 98: 393-396.
Shephard, G.S., Marasas, W.F., Leggott, N.L., Yazdanpanah, H., Rahimian, H. and Safavi, N., 2000. Natural occurrence of fumonisins in corn from Iran. Journal of Agriculture and Food Chemistry 48: 1860-1864.
Shephard, G.S., Van der Westhuizen, L. and Sewram, V., 2007. Biomarkers of exposure to fumonisin mycotoxins: a review. Food Additives and Contaminants Part A 24: 1196-1201.
Shi, J., Han, W. and Gu, M., 2003. Contamination of AFB, FB, SET in spices in China. Journal of Health Laboratory Technology 13: 589-594.
Solovey, M.M., Somoza, C., Cano, G., Pacin, A. and Resnik, S., 1999. A survey of fumonisins, deoxynivalenol, zearalenone and aflatoxins contamination in corn-based food products in Argentina. Food Additives and Contaminants Part A 16: 325-329.
Soriana, J.M. and Dragacci, S., 2004. Intake, decontamination and legislation of fumonisins in foods.Food Research International 37: 367-374.
Sui, W., Liu, G., Huang, M., Kang, Y., Zhang, W., Liu, Y., Xin, L. and Liang, Y., 2003. Contamination of fumonisin and Fusarium moniliforme in staple crops in Jilin province of China. Journal of Health Laboratory Technology 13: 80-81.
Sun, G., Wang, S., Hu, X., Su, J., Huang, T., Yu, J., Tang, L., Gao, W. and Wang, J.S., 2007. Fumonisin B1 contamination of home-grown corn in high-risk areas for esophageal and liver cancer in China. Food Additives and Contaminants Part A 24: 181-185.
Sun, G., Wang, S., Hu, X., Su, J., Zhang, Y., Xie, Y., Zhang, H., Tang, L. and Wang, J.S., 2011. Co-contamination of aflatoxin B1 and fumonisin B1 in food and human dietary exposure in three areas of China. Food Additives and Contaminants Part A 28: 461-470.
Sydenham, E.W., Thiel, P.G., Marasas, W.F.O., Shepard, G.S., Van Schalkwyk, D.J. and Koch, K.R., 1990. Natural occurrence of some Fusarium mycotoxins in corn from low and high esophageal cancer prevalence areas of Transkei, Southern Africa. Journal of Agriculture and Food Chemistry 38: 1900-1903.
Tamura, M., Takahashi, A., Uyama, A. and Mochizuki, N., 2012. A method for multiple mycotoxin analysis in wines by solid phase extraction and multifunctional cartridge purification, and ultra-high-performance liquid chromatography coupled to tandem mass spectrometry. Toxins 4: 476-486.
Tamura, M., Uyama, A. and Mochizuki, N., 2011. Development of a multi-mycotoxin analysis in beer-based drinks by a modified QuEChERS method and ultra-high-performance liquid chromatography coupled with tandem mass spectrometry. Analytic Sciences 27: 629-635.
Ueno, Y., Iijima, K., Wang, S.D., Sugiura, Y., Sekijima, M., Tanaka, T., Chen, C. and Yu, S.Z., 1997. Fumonisins as a possible contributory risk factor for primary liver cancer: a 3-year study of corn harvested in Haimen, China, by HPLC and ELISA.Food and Chemical Toxicology 35: 1143-1150.
United States Department of Agriculture (USDA), 2003. Countries and regions. China. Available at: http://www.fas.usda.gov/regions/east-asia-and-pacific/china.
Van der Westhuizen, L., Brown, N.L., Marasas, W.F.O., Swanevelder, S. and Shephard, G.S., 1999. Sphinganine/sphingosine ratio in plasma and urine as a possible biomarker for fumonisin exposure in humans in rural areas of Africa. Food and Chemical Toxicology 37: 1153-1158.
Van der Westhuizen, L., Shephard, G.S., Gelderblom, W.C.A., Torres, O. and Riley, R.T., 2013. Fumonisin biomarkers in maize eaters and implications for human disease. World Mycotoxin Journal 6: 223-232.
Voss, K.A., Chamberlain, W.J., Bacon, C.W., Herbert, R.A., Walters, D.B. and Norred, W.P., 1995. Subchronic feeding study of the mycotoxin fumonisin B1 in B6C3F1 mice and Fischer 344 rats. Fundamental and Applied Toxicology 24: 102-110.
Wang, Z., Li, X., Tong, Z., Cheng, S., Gao, W., Zhu, X., Feng, J. and Cai, H., 2001. Correlation study between fumonisin contamination and generate-sources in foodstuffs. Chinese Journal of Health Laboratory Technology 11: 9-13.
Wang, J., Zhou, Y. and Wang, Q., 2008a. Analysis of mycotoxin fumonisins in corn products by high-performance liquid chromatography coupled with evaporative light scattering detection. Food Chemistry 107: 970-976.
Wang, J., Zhou, Y., Liu, W., Zhu, X., Du, L. and Wang, Q., 2008b. Fumonisin level in corn-based food and feed from Linxian County, a high-risk area for esophageal cancer in china. Food Chemistry 106: 241-246.
World Health Organization (WHO), 2000. Fumonisin B1(environmental health criteria 219). International programme on chemical safety. WHO, Geneva, Switzerland. Available at: http://whqlibdoc.who.int/ehc/WHO_EHC_219.pdf.
World Health Organization (WHO), 2001. Safety evaluation of certain mycotoxins in food. International programme on chemical safety. WHO food additives series 47: 103-279.
World Health Organization (WHO), 2002. WHO global strategy for food safety: safer food for better health. Food Safety Programme 2002. WHO, Geneva, Switzerland.
World Health Organization (WHO), 2005. Total diet studies: a recipe for safer food. Available at: WHO, Geneva, Switzerland. http://www.who.int/foodsafety/publications/chem/en/gems_brochure.pdf
Wu, F., 2004. Mycotoxin risk assessment for the purpose of setting international regulatory standards. Environmental Science and Technology 38: 4049-4055.
Yan, Y., Zhang, Y. and Li, R., 1999. Contamination of fumonisin in staple crops in Shandong province of China. Chinese Journal of Health Laboratory Technology 9: 201–204.
Yoshizawa, T., Yamashita, A. and Luo, Y., 1994. Fumonisin occurrence in corn from high- and low-risk areas for human esophageal cancer in China. Applied and Environmental Microbiology 60: 1626-1629.
Yu, Y., Taylor, P.R., Li, J.Y., Dawsey, S.M., Wang, G.Q., Guo, W.D., Wang, W., Liu, B.Q., Blot, W.J. and Shen, Q., 1993. Retrospective cohort study of risk-factors for esophageal cancer in Linxian, People’s Republic of China. Cancer Causes Control 4: 195-202.
Zhang, W.W., Ye, Z.M., Jin, Y., Wang, S.Y., Zhang, L.S. and Pei, X.F., 2014. Management of mycotoxin contamination in food and feed in China. World Mycotoxin Journal 7 :53-62.
Zhou, P., Zhao, Y., Li, J., Wu, G., Zhang, L., Liu, Q., Fan, S., Yang, X., Li, X. and Wu Y., 2012. Dietary exposure to persistent organochlorine pesticids in 2007 Chinese total diet study. Environmental International 42: 152-159.
Zoller, O., Sager, F. and Zimmerli, B., 1994. Vorkommen von Fumonisinen in Lebensmitteln. Mitteilungen aw dem Gebiete der Lebensmitteluntersuchung und Hygiene 85: 81-99.