Determination of Fusarium mycotoxin exposure in humans based on urine samples, using One Health approach: Mini-review

Tamás Schieszl; Judit Szabó-Fodor; Melinda Kovács

doi:10.31914/aak.2601

Szerzők

Shieszl Tamás Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus
Szabó-Fodor Judit MATE Élettani és Takarmányozástani Intézet, MTA-KE-SZIE Mikotoxinok az Élelmiszerláncban Kutatócsoport
Kovács Melinda MATE Élettani és Takarmányozástani Intézet, MTA-KE-SZIE Mikotoxinok az Élelmiszerláncban Kutatócsoport

DOI:

https://doi.org/10.31914/aak.2601

Kulcsszavak:

Fusarium mycotoxins, human exposure, urinary biomarker

Absztrakt

The role of mycotoxins has been recognized in the etiology of a number of human diseases. Therefore, biomonitoring of human mycotoxin exposure is very important. One of the possible ways to do this is the urinary biomarker-based exposure determination. Over the past few decades, such studies have been conducted in many countries around the world on volunteers of different ages, genders, and eating habits, although these studies do not always use the same measurement, and calculation methods. This review focuses on the most important fusarium mycotoxins (deoxynivalenol (DON), zearalenone (ZEA), fumonisins (FUM), T-2, and HT-2 toxins). Because of the presence of mycotoxins in the environment-feed-food chain, One Health strategies should be adopted for the prevention of their exposure.

Információk a szerzőről

Shieszl Tamás, Magyar Agrár- és Élettudományi Egyetem (MATE) Kaposvári Campus

Levelező szerző
7400 Kaposvár, Guba Sándor u. 40., 82/505-800
E-mail: schieszltamas95@gmail.com

Hivatkozások

Abia W. A., Warth B., Sulyok M., Krska R., Tchana A., Njobeh P. B., Turner P. C., Kouanfack C., Eyonge-tah M., Dutton M., Moundipa P. F. (2013). Bio-monitoring of mycotoxin exposure in Cameroon using a urinary multi-biomarker approach. Food Chem. Toxicol., 62, 927-934. DOI: https://doi.org/10.1016/j.fct.2013.10.003

Antonissen G., Martel A., Pasmans F., Ducatelle R., Verbrugghe E., Vandenbroucke V., Li S., Haesebrouck F., Van Immerseel, F., Croubels S. (2014) a. The Impact of Fusarium Mycotoxins on Human and Animal Host Susceptibility to Infectious Diseases. Toxins, 6 (2), 430-452. DOI: https://doi.org/10.3390/toxins6020430

Antonissen G., Van Immerseel F., Pasmans F., Ducatelle R., Haesebrouck F., Timbermont L., Verlinden M., Janssens G. P. J., Eeckhout M., de Saeger S., Hessenberger S., Martel A., Croubels S. (2014) b. The mycotoxin deoxynivalenol predisposes for the development of Clostridium perfringens-induced necrotic enteritis in broiler chickens. PLoS One, 30 (9), DOI: https://doi.org/10.1371/journal.pone.0108775

Cetin Y., Bullerman L. B. (2005). Cytotoxicity of Fusarium mycotoxins to mammalian cell cultures as determined by the MTT bioassay. Food Chem. Toxicol. 43(5):755-64. DOI: https://doi.org/10.1016/j.fct.2005.01.016

Commission of the European Communities (2007). Commission Regulation (EC) No 1126/2007 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, Downloaded: Link: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32007R1126&from=HU (Last download: 16/08/2021)

European Commission (2013). Commission Recommendation of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products (Text with EEA relevance) (2013/165/EU) Of-ficial Journal of the European Union, Downloaded: Link: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32013H0165&from=HU (Last download: 16/08/2021)

European Food Safety Authority (EFSA) (2011 a). Scientific Opinion on the risks for public health related to the presence of zearalenone in food. DOI: 10.2903/j.efsa.2011.2197 (Last download: 17/08/2021)

European Food Safety Authority (EFSA) (2011 b). Scientific Opinion on the risks for animal and public health related to the presence of T-2 and HT-2 toxin in food and feed. DOI: 10.2903/j.efsa.2011.2481 (Last download: 17/08/2021)

European Food Safety Authority (EFSA) (2017). Risks to human and animal health related to the presence of deoxynivalenol and its acetylated and modified forms in food and feed. EFSA Journal, DOI: 10.2903/j.efsa.2017.4718 (Last download: 17/08/2021)

European Food Safety Authority (EFSA) (2018). Appropriateness to set a group health-based guid-ance value for fumonisins and their modified forms. EFSA Journal, DOI: 10.2903/j.efsa.2018.5172 (Last download: 26/10EFSA/2021)

Fan K., Xu J., Jiang K., Liu X., Meng J., Li H., et al. (2019). Determination of multiple mycotoxins in paired plasma and urine samples to assess human exposure in Nanjing, China. Environ. Pol-lut., 248, 865-873. DOI: https://doi.org/10.1016/j.envpol.2019.02.091

Franco L. T., Petta T., Rottinghaus G., Bordin K., Gomes G. A., Alvito P., Assunção R., Oliveira C.A.F. (2019). Assessment of mycotoxin exposure and risk characterization using occurrence data in foods and urinary biomarkers in Brazil. Food Chem. Toxicol., 128, 21-34. DOI: https://doi.org/10.1016/j.fct.2019.03.046

Gambacorta L., Solfrizzo M., Visconti A., Powers S., Cossalter A. M., Pinton P., Oswald I. P. (2013). Validation study on urinary biomarkers of exposure for aflatoxin B1, ochratoxin A, fumonisin B1, deoxynivalenol and zearalenone in piglet. World Mycotoxin Jour., 6 (3), 299–308. DOI: https://doi.org/10.3920/wmj2013.1549

Gambacorta L., Magistà D., Perrone G., Murgolo S., Logrieco A. F., Solfrizzo M. (2018). Co-occurrence of toxigenic moulds, aflatoxins, ochratoxin A, Fusarium and Alternaria mycotoxins in fresh sweet peppers (Capsicum annuum) and their processed products. World Mycotoxin Journal, 11 (1), 159-174. DOI: https://doi.org/10.3920/wmj2017.2271

Gerding J., Cramer B., Humpf H. U. (2014). Determination of mycotoxin exposure in Germany using an LC-MS/MS multibiomarker approach. Mol. Nutr. Food Res., 58 (12), 2358–2368. DOI: https://doi.org/10.1002/mnfr.201400406

Gerding J., Ali N., Schwartzbord J., Cramer B., Brown D. L., Degen G. H., et al. (2015). A comparative study of the human urinary mycotoxin excretion patterns in Bangladesh, Germany, and Haiti us-ing a rapid and sensitive LC-MS/MS approach. Mycotoxin Res., 31 (3), 127-136. DOI: https://doi.org/10.1007/s12550-015-0223-9

Girgis G. N., Sharif S., Barta J. R., Boermans H. J., Smith T. K. (2008). Immunomodulatory effects of feed-borne fusarium mycotoxins in chickens infected with Coccidia. Exp. Biol. Med. 233 (11), 1411–1420. DOI: https://doi.org/10.3181/0805-rm-173

Girgis G. N., Barta J. R., Girish C. K., Karrow N. A., Boermans H. J., Smith T. K. (2010). Effects of feed-borne Fusarium mycotoxins and an organic mycotoxin adsorbent on immune cell dynamics in the jejunum of chickens infected with Eimeria maxima. Vet. Immunol. Immun., 138 (3), 218–223. DOI: https://doi.org/10.1016/j.vetimm.2010.07.018

Gong Y. Y., Torres-Sanchez L., Lopez-Carrillo L., Peng J. H., Sutcliffe A. E., White K. L., Humpf H.-U., Turner P. C., Wild C. P. (2008). Association between Tortilla Consumption and Human Urinary Fumonisin B1 Levels in a Mexican Population. Cancer Epidemiol Biomarkers Prev, 17 (3), 688-694. DOI: https://doi.org/10.1158/1055-9965.epi-07-2534

Heyndrickx E., Sioen I., Huybrechts B., Callebaut A., Henauw S. D., Saeger S. D. (2015). Human biomon-itoring of multiple mycotoxins in the Belgian population: Results of the BIOMYCO study. Envi-ronment International, 84, 82-89. DOI: https://doi.org/10.1016/j.envint.2015.06.011

Huybrechts B., Martins J. C., Debongnie P., Uhlig S., Callebaut A. (2015). Fast and sensitive LC – MS/MS method measuring human mycotoxin exposure using biomarkers in urine. Arch. Toxicol., 89 (11), 1993-2005. DOI: https://doi.org/10.1007/s00204-014-1358-8

Imran M., Cao S., Wan S. F., Chen Z., Saleemi M. K., Wang N., Naseem M. N., Munawar J., (2020). Mycoto-xins – a global one health concern: A review. Agrobiological Records, 2, 1-16. DOI: https://doi.org/10.47278/journal.abr/2020.008

Jávor A. & Szigeti J. (2011) a. Termékminősítés és termékhigiénia; Downloaded: Link: https://regi.tankonyvtar.hu/hu/tartalom/tamop425/0010_1A_Book_17_Termekminosites_es_termekhigienia/ch03.html (Last download: 22/07/2021)

Jávor A. & Szigeti J. (2011) b. Termékminősítés és termékhigiénia; Downloaded: Link: https://regi.tankonyvtar.hu/hu/tartalom/tamop425/0010_1A_Book_17_Termekminosites_es_termekhigienia/ch03s05.html (Last down-load: 22/07/2021)

Joint FAO/WHO Expert Committee on Food Additives (JECFA) (2016): Eighty-third meeting Rome, 8–17 November 2016; Downloaded: Link: https://www.who.int/foodsafety/publications/JECFA83-Summary.pdf (Last download: 26/10/2021)

Kolosova, A. & Stroka, J. (2011). Substances for reduction of the contamination of feed by mycotox-ins: a review. World Mycotoxin Journal, 4 (3), 225-256. DOI: https://doi.org/10.3920/wmj2011.1288

Kovács M., Horn P., Magyar T., Tornyos G., Pósa R., Mézes M., Cseh S., Szabó A., Szabó-Fodor J. (2016). A fumonizin B1 mikotoxin a táplálékláncban és egészségkárosító hatásai. In Memoriam Kovács Ferenc Nemzetközi Állatorvos és Állattenyésztő Kongresszus, 38-43.

Ladeira C., Frazzoli C., Orisakwe O. E. (2017). Engaging One Health for Non-Communicable Diseases in Africa: Perspective for Mycotoxins. Frontiers in Public Health, 5, DOI: https://doi.org/10.3389/fpubh.2017.00266

Lattanzio V. M. T., Solfrizzo M., De Girolamo A., Chulze S. N., Torres A. M., Visconti A. (2011). LC – MS/MS characterization of the urinary excretion profile of the mycotoxin deoxynivalenol in hu-man and rat. J. Chromatogr. B, 879 (11–12), 707-715. DOI: https://doi.org/10.1016/j.jchromb.2011.01.029

Lemming E., Montes A. M., Schmidt J., Cramer B., Humpf H-U., Moraeus L., Olsen M. (2020). Mycotox-ins in blood and urine of Swedish adolescents-possible associations to food intake and other background characteristics. Mycotoxin Research, 36 (2), 193–206. DOI: https://doi.org/10.107/s12550-019-00381-9

Mally A., Solfrizzo M., Degen G. H. (2016). Biomonitoring of the mycotoxin Zearalenone: current state-of-the art and application to human exposure assessment. Arch. Toxicol., 90 (6), 1281-1292. DOI: https://doi.org/10.1007/s00204-016-1704-0

Manal M. Z., El-Midany S. A., Shaheen H. M., Riz L. (2012). Mycotoxins in animals: Occurrence, effects, prevention and management. A review. Journal of Toxicology and Environmental Health Scienc-es, 4 (1), 13-28. DOI: https://doi.org/10.5897/jtehs11.072

Manning B. B., Terhune J. S., Li M. H., Robinson E. H., Wise D. J., Rottinghaus G. E. (2005). Exposure to feedborne mycotoxins T-2 toxin or ochratoxin a causes increased mortality of channel catfish challenged with Edwardsiella ictaluri. J. Aquat. Anim. Health, 17 (2), 147–152. DOI: https://doi.org/10.1577/h03-063.1

Manning B. B., Abbas H. K., Wise D. J., Greenway T. (2013). The effect of feeding diets containing deox-ynivalenol contaminated corn on channel catfish (Ictalurus punctatus) challenged with Ed-wardsiella ictaluri. Aquac. Res. DOI: https://doi.org/10.1111/are.12123

Maul R., Warth B., Kant J. S., Schebb N. H., Krska R., Koch M. (2012). Investigation of the hepatic glucuronidation pattern of the Fusarium mycotoxin deoxynivalenol in various species. Chem. Res. Toxicol., 25 (12), 2715-2717. DOI: https://doi.org/10.1021/tx300348x

Mitropoulou A., Gambacorta L., Lemming E. W., Solfrizzo M., Olsen M.(2018). Extended evaluation of urinary multi-biomarker analyses of mycotoxins in Swedish adults and children. World Myco-toxin Journal, 11 (4), 647-659. DOI: https://doi.org/10.3920/wmj2018.2313

NNK (hungarian National Center for Public Health) (2020). A penészgombák és a mikotoxinok; Downloaded: Link: https://www.nnk.gov.hu/index.php/nnk-projektek/human-biomonitoring/a-peneszgombak-es-a-mikotoxinok (Last download: 20/07/2021)

Peng W.-X., Marchal J. L. M., van der Poel A. F. B. (2018). Strategies to prevent and reduce mycotoxins for compound feed manufacturing. Animal Feed Science and Technology, 237, 129-153. DOI: https://doi.org/10.1016/j.anifeedsci.2018.01.017

Piekkola S., Turner P. C., Abdel-Hamid M., Ezzat S., El-Daly M., El-Kafrawy S. (2012). Characterisation of aflatoxin and deoxynivalenol exposure among pregnant Egyptian women. Food Addit. Con-tam., 29 (6), 962-971. DOI: https://doi.org/10.1080/19440049.2012.658442

Riley R. T., Torres O., Showker J. L., Zitomer N. C., Matute J., Voss K. A., Gelineau-van Waes J., Maddox J. R., Gregory S. G., Ashley-Koch A. E. (2012). The Kinetics of Urinary Fumonisin B1 Excretion in Humans Consuming Maize-Based Diets. Mol. Nutr. Food Res., 56 (9), 1445-1455. DOI: https://doi.org/10.1002/mnfr.201200166

Schelstraete W., Devreese M., Croubels S. (2020). Comparative toxicokinetics of Fusarium mycotoxins in pigs and humans. Food Chem. Toxicol., 137, 111-140. DOI: https://doi.org/10.1016/j.fct.2020.111140

Shephard G. S., Burger H.-M., Gambacorta L., Gong Y. Y., Krska R., Rheeder J. P., Solfrizzo M., Srey C., Sulyok M., Visconti A., Warth B., van der Westhuizen L. (2013). Multiple mycotoxin exposure de-termined by urinary biomarkers in rural subsistence farmers in the former Transkei, South Af-rica. Food Chem. Toxicol., 62, 217-225. DOI: https://doi.org/10.1016/j.fct.2013.08.040

Solfrizzo M., Gambacorta L., Visconti A. (2014). Assessment of Multi-Mycotoxin Exposure in South-ern Italy by Urinary Multi-Biomarker Determination. Toxins, 6 (2), 523-538. DOI: https://doi.org/10.3390/toxins6020523

Tai J., Pestka J. (1988). Impaired murine resistance to Salmonella Typhimurium following oral expo-sure to the trichothecene T-2 toxin. Food Cem. Toxicol., 26 (8), 691–698. DOI: https://doi.org/10.1016/0278-6915(88)90068-3

Turner P. C., White K. L. M., Burley V. J., Hopton R. P., Rajendram A., Fisher J., Cade J.E., Wild C.P. (2010). A comparison of deoxynivalenol intake and urinary deoxynivalenol in UK adults. Biomarkers, 15 (6), 553-562. DOI: https://doi.org/10.3109/1354750x.2010.495787

Turner P. C., Van Der Westhuizen L., Da Costa A. N. (2011 a). Biomarkers of Exposure: Mycotoxins – Aflatoxin, Deoxynivalenol and Fumonisins. Issues in Toxicology 10 (2), 50-86. DOI: https://doi.org/10.1039/9781849733540-00050

Turner P. C., Hopton R. P., White K. L. M., Fisher J., Cade J. E., Wild C. P. (2011 b). Assessment of deox-ynivalenol metabolite profiles in UK adults. Food Chem. Toxicol., 49 (1), 132-135. DOI: https://doi.org/10.1016/j.fct.2010.10.007

Turner P. C., Flannery B., Isitt C., Ali M., Pestka J. (2012). The role of biomarkers in evaluating human health concerns from fungal contaminants in food. Nutrition Research Reviews, 25 (1), 162–179. DOI: https://doi.org/10.1017/s095442241200008x

Toora B. D. & Rajagopal G. (2002). Measurement of creatinine by Jaffe's reaction--determination of concentration of sodium hydroxide required for maximum color development in standard, uri-ne and protein free filtrate of serum. Indian J Exp Biol., 40 (3), 352-4. Downloaded: Link: https://pubmed.ncbi.nlm.nih.gov/12635710/ (Last download: 16/11/2021)

Van der Westhuizen L., Shephard G. S., Rheeder J. P., Somdyala N. I. M., Marasas W. F. O. (2008). Sphin-goid base levels in humans consuming fumonisin-contaminated maize in rural areas of the for-mer Transkei, South Africa: a cross-sectional study. Food Addit. Contam. 25 (11), 1385-1391. DOI: https://doi.org/10.1080/02652030802226195

Van der Westhuizen L., Shephard G. S., Burger H. M., P. Rheeder J. P., Gelderblom W. C. A., Wild C. P., Gong Y. Y. (2011). Fumonisin B1 as a Urinary Biomarker of Exposure in a Maize Intervention Study Among South African Subsistence Farmers. Cancer Epidemiol. Biomarkers Prev, 20 (3), 483-490. DOI: https://doi.org/10.1158/1055-9965.epi-10-1002

Vandenbroucke V., Croubels S., Martel A., Verbrugghe E., Goossens J., van Deun, K., Boyen F., Thomp-son A., Shearer N., de Backer P. (2011). The mycotoxin deoxynivalenol potentiates intestinal in-flammation by Salmonella Typhimurium in porcine ileal loops. PLoS One, 6 (8), DOI: https://doi.org/10.1371/journal.pone.0023871

Verbrugghe E., Vandenbroucke V., Dhaenens M., Shearer N., Goossens J., de Saeger S., Eeckhout M., D'herde K., Thompson A., Deforce D. (2012). T-2 toxin induced Salmonella Typhimuri-um intoxication results in decreased Salmonella numbers in the cecum contents of pigs, despite marked effects on Salmonella-host cell interactions. Vet. Res. 43 (1), 1-18. DOI: https://doi.org/10.1186/1297-9716-43-22

Vidal Corominas A., Mengelers M., Yang S., De Saeger S., De Boevre M. (2018). Mycotoxin biomarkers of Exposure: a comprehensive review. Compr. Rev. Food Sci. Food Saf., 17 (5), 1127-1155. DOI: https://doi.org/10.1111/1541-4337.12367

Wang E., Ross P. F., Wilson T. M., Riley R.T., Merrill A.H. Jr. (1992). Increases in serum sphingosine and sphinganine and decreases in complex sphingolipids in ponies given feed containing fumonizins, mycotoxins produced by Fusarium verticillioides. J. Nutr., 122 (8), 1706-1716. DOI: https://doi.org/10.1093/jn/122.8.1706

Warth B., Sulyok M., Fruhmann P., Berthiller F., Schuhmacher R., Hametner C. (2012). Assessment of human deoxynivalenol exposure using an LC – MS/MS based biomarker method. Toxicol. Lett., 211 (1), 85-90. DOI: https://doi.org/10.1016/j.toxlet.2012.02.023

Warth B., Sulyok M., Berthiller F., Schuhmacher R., Krska R. (2013). New insights into the human metabolism of the Fusarium mycotoxins deoxynivalenol and zearalenone. Toxicology Letters, 220 (1), 88–94. DOI: https://doi.org/10.1016/j.toxlet.2013.04.012

Warth B., Petchkongkaew A., Sulyok M., Krska R. (2014). Utilising an LC-MS/MS-based multi-biomarker approach to assess mycotoxin exposure in the Bangkok metropolitan area and sur-rounding provinces. Food Addit. Contam. Part A, 31 (12), 2040-2046. DOI: https://doi.org/10.1080/19440049.2014.969329

Zentai A., Szeitzné-Szabó M., Mihucz G., Szeli N., Szabó A., Kovács M. (2019). Occurrence and Risk Assessment of Fumonisin B1and B2 Mycotoxins in Maize-Based Food Products in Hungary. Toxins, 11 (12), 709-722. DOI: https://doi.org/10.3390/toxins11120709