Abstract
An improved “dilute and shoot” LC-MS/MS multibiomarker approach was used to monitor urinary excretion of 23 mycotoxins and their metabolites in human populations from Asia (Bangladesh), Europe (Germany), and the Caribbean region (Haiti). Deoxynivalenol (DON), deoxynivalenol-3-glucuronide (DON-3-GlcA), T-2-toxin (T-2), HT-2-toxin (HT-2), HT-2-toxin-4-glucuronide (HT-2-4-GlcA), fumonisin B1 (FB1), aflatoxins (AFB1, AFB2, AFG1, AFG2, AFM1), zearalenone (ZEA), zearalanone (ZAN), their urinary metabolites α-zearalanol (α-ZEL) and β-zearalanol (β-ZEL), and corresponding 14-O-glucuronic acid conjugates (ZEA-14-GlcA, ZAN-14-GlcA, β-ZEL, α/β–ZEL-14-GlcA), ochratoxin A (OTA), and ochratoxin alpha (OTα) as well as enniatin B (EnB) and dihydrocitrinone (DH-CIT) were among these compounds. Eight urinary mycotoxin biomarkers were detected (AFM1, DH-CIT, DON, DON-GLcA, EnB, FB1, OTA, and α-ZEL). DON and DON-GlcA were exclusively detected in urines from Germany and Haiti whereas urinary OTA and DH-CIT concentrations were significantly higher in Bangladeshi samples. AFM1 was present in samples from Bangladesh and Haiti only. Exposure was estimated by the calculation of probable daily intakes (PDI), and estimates suggested occasional instances of toxin intakes that exceed established tolerable daily intakes (TDI). The detection of individual mycotoxin exposure by biomarker-based approaches is a meaningful addition to the classical monitoring of the mycotoxin content of the food supply.
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References
Abia WA, Warth B, Sulyok M, Krska R, Tchana A, Njobeh PB et al (2013) Bio-monitoring of mycotoxin exposure in Cameroon using a urinary multi-biomarker approach. Food Chem Toxicol 62:927–934
Ali N, Blaszkewicz M, Manirujjaman M, Perveen R, Al Nahid A, Mahmood S et al (2014) Biomonitoring of ochratoxin A in blood plasma and exposure assessment of adult students in Bangladesh. Mol Nutr Food Res 11:2219–2225
Ali N, Blaszkewicz M, Degen GH (2015) Biomarkers of citrinin and ochratoxin A exposure in humans. Naunyn Schmiedebergs Arch Pharmacol: in press
Ali N, Blaszkewicz M, Degen GH (2015b) Occurrence of the mycotoxin citrinin and its metabolite dihydrocitrinone in urines of German adults. Arch Toxicol 4:573–578
Ali N, Blaszkewicz M, Mohanto NC, Rahman M, Alim A, Hossain K, Degen GH (2015c) First results on citrinin biomarkers in urines from rural and urban cohorts in Bangladesh. Mycotoxin Res 1:9–16
Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 3:497–516
Beyer M, Ferse I, Humpf H (2009) Large-scale production of selected type A trichothecenes: the use of HT-2 toxin and T-2 triol as precursors for the synthesis of d3-T-2 and d3-HT-2 toxin. Mycotoxin Res 1:41–52
Bittner A, Cramer B, Humpf H (2013) Matrix binding of ochratoxin A during roasting. J Agric Food Chem 51:12737–12743
Bretz M, Beyer M, Cramer B, Knecht A, Humpf H (2006) Thermal degradation of the Fusarium mycotoxin deoxynivalenol. J Agric Food Chem 17:6445–6451
Bundesministerium für Ernährung und Landwirtschaft (2013) Besondere Ernte und Qualitätsermittelung 2013. URL: http://berichte.bmelv-statistik.de/EQB-1002000-2013.pdf (accessed on 05.01.2015)
Castor LL (1987) Aflatoxin occurrence in maize samples collected in Haitian markets. Plant Dis 11:969
Coronel MB, Marin S, Tarragó M, Cano-Sancho G, Ramos AJ, Sanchis V (2011) Ochratoxin A and its metabolite ochratoxin alpha in urine and assessment of the exposure of inhabitants of Lleida, Spain. Food Chem Toxicol 6:1436–1442
Cramer B, Bretz M, Humpf H (2007) Stable isotope dilution analysis of the fusarium mycotoxin zearalenone. J Agric Food Chem 21:8353–8358
Cramer B, Harrer H, Nakamura K, Uemura D, Humpf H (2010) Total synthesis and cytotoxicity evaluation of all ochratoxin A stereoisomers. Bioorg Med Chem 1:343–347
Dawlatana M, Coker RD, Nagler MJ, Wild CP, Hassan MS, Blunden G (2002) The occurrence of mycotoxins in key commodities in Bangladesh: surveillance results from 1993 to 1995. J Nat Toxins 4:379–386
Duarte SC, Pena A, Lino CM (2011) Human ochratoxin A biomarkers—from exposure to effect. Crit Rev Toxicol 3:187–212
Dunn BB, Stack ME, Park DL, Joshi A, Friedman L, King RL (1983) Isolation and identification of dihydrocitrinone, a urinary metabolite of citrinin in rats. J Toxicol Environ Health 12(2-3):283–289
EFSA (2006) Opinion of the Scientific Panel on contaminants in the Food Chain of the EFSA on a request from the Commission related to ochratoxin A in food. EFSA J 365:1–56
EFSA (2010) Scientific opinion on dietary reference values for water. EFSA J 3:1459
EFSA (2011) 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. EFSA J 12:2481
EFSA (2012) Scientific opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA J 3:2605
Filbert ME, Brown DL (2012) Aflatoxin contamination in Haitian and Kenyan peanut butter and two solutions for reducing such contamination. J Hunger Environ Nutr 7(2-3):321–332
Gambacorta S, Solfrizzo H, Visconti A, Powers S, Cossalter AM, Pinton P, Oswald IP (2013) Validation study on urinary biomarkers of exposure for aflatoxin B1, ochratoxin A, fumonisin B1, deoxynivalenol and zearalenone in piglets. World Mycotoxin J 3:299–308
Gerding J, Cramer B, Humpf H (2014) Determination of mycotoxin exposure in Germany using an LC-MS/MS multibiomarker approach. Mol Nutr Food Res 12:2358–2368
Gilbert J, Brereton P, MacDonald S (2001) Assessment of dietary exposure to ochratoxin A in the UK using a duplicate diet approach and analysis of urine and plasma samples. Food Addit Contam 12:1088–1093
Hübner F, Harrer H, Fraske A, Kneifel S, Humpf H (2012) Large scale purification of B-type fumonisins using centrifugal partition chromatography (CPC). Mycotoxin Res 1:37–43
Jestoi M (2008) Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: a review. Crit Rev Food Sci Nutr 1:21–49
Juan C, Mañes J, Raiola A, Ritieni A (2013) Evaluation of beauvericin and enniatins in Italian cereal products and multicereal food by liquid chromatography coupled to triple quadrupole mass spectrometry. Food Chem 4:755–762
Klapec T, Šarkanj B, Banjari I, Strelec I (2012) Urinary ochratoxin A and ochratoxin alpha in pregnant women. Food Chem Toxicol 12:4487–4492
Marin S, Ramos AJ, Cano-Sancho G, Sanchis V (2013) Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol 60:218–237
Muñoz K, Blaszkewicz M, Campos V, Vega M, Degen GH (2014) Exposure of infants to ochratoxin A with breast milk. Arch Toxicol 3:837–846
Nguyen M, Tozlavanu M, Tran T, Pfohl-Leszkowicz A (2007) Occurrence of aflatoxin B1, citrinin and ochratoxin A in rice in five provinces of the central region of Vietnam. Food Chem 1:42–47
Njumbe Ediage E, Di Mavungu JD, Song S, Sioen I, De Saeger S (2013) Multimycotoxin analysis in urines to assess infant exposure: a case study in Cameroon. Environ Int 57-58:50–59
Riley RT, Torres O, Showker JL, Zitomer NC, Matute J, Voss KA et al (2012) The kinetics of urinary fumonisin B1 excretion in humans consuming maize-based diets. Mol Nutr Food Res 9:1445–1455
Roy M, Harris J, Afreen S, Deak E, Gade L, Balajee SA et al (2013) Aflatoxin contamination in food commodities in Bangladesh. Food Addit Contam Part B Surveill 1:17–23
Šarkanj B, Warth B, Uhlig S, Abia WA, Sulyok M, Klapec T et al (2013) Urinary analysis reveals high deoxynivalenol exposure in pregnant women from Croatia. Food Chem Toxicol 62:231–237
SCF (2000) Opinion of the scientific committee on food on Fusarium-toxins part 2: Zearalenone (ZEA) (expressed on 22 June 2000)
SCF (2002) Opinion of the scientific committee on food on Fusarium-toxins part 6: group evaluation of T-2 toxin, HT-2 toxin, nivalenol and deoxynivalenol. (adopted on 26 February 2002)
SCF (2003) Updated opinion of the scientific committee on food on Fumonisin B1, B2 and B3 (expressed on 4 April 2003)
Schwartzbord JR, Emmanuel E, Brown DL (2013) Haiti’s food and drinking water: a review of toxicological health risks. Clin Toxicol (Phila) 9:828–833
Shephard GS, Burger H, Gambacorta L, Gong YY, Krska R, Rheeder JP et al (2013) Multiple mycotoxin exposure determined by urinary biomarkers in rural subsistence farmers in the former Transkei, South Africa. Food Chem Toxicol 62:217–225
Solfrizzo M, Gambacorta L, Visconti A (2014) Assessment of multi-mycotoxin exposure in Southern Italy by urinary multi-biomarker determination. Toxins 2:523–538
Torres O, Matute J, Gelineau-van Waes J, Maddox JR, Gregory SG, Ashley-Koch AE et al (2014) Urinary fumonisin B1 and estimated fumonisin intake in women from high- and low-exposure communities in Guatemala. Mol Nutr Food Res 5:973–983
Turner PC, White KLM, Burley VJ, Hopton RP, Rajendram A, Fisher J et al (2010) A comparison of deoxynivalenol intake and urinary deoxynivalenol in UK adults. Biomarkers 6:553–562
Uhlig S, Torp M, Heier BT (2006) Beauvericin and enniatins A, A1, B and B1 in Norwegian grain: a survey. Food Chem 2:193–201
van Egmond HP, Schothorst RC, Jonker MA (2007) Regulations relating to mycotoxins in food. Anal Bioanal Chem 1:147–157
Warth B, Sulyok M, Berthiller F, Schuhmacher R, Krska R (2013a) New insights into the human metabolism of the Fusarium mycotoxins deoxynivalenol and zearalenone. Toxicol Lett 1:88–94
Warth B, Sulyok M, Krska R (2013b) LC-MS/MS-based multibiomarker approaches for the assessment of human exposure to mycotoxins. Anal Bioanal Chem 17:5687–5695
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 surrounding provinces. Food Addit Contam Part A 12:2040–2046
Welsch T, Humpf H (2012) HT-2 toxin 4-glucuronide as new T-2 toxin metabolite: enzymatic synthesis, analysis, and species specific formation of T-2 and HT-2 toxin glucuronides by rat, mouse, pig, and human liver microsomes. J Agric Food Chem 40:10170–10178
Yogendrarajah P, Jacxsens L, de Saeger S, de Meulenaer B (2014) Co-occurrence of multiple mycotoxins in dry chilli (Capsicum annum L.) samples from the markets of Sri Lanka and Belgium. Food Control 46:26–34
Zhu JQ, Zhang LS, Hu X, Xiao Y, Chen JS, Xu YC et al (1987) Correlation of dietary aflatoxin B1 levels with excretion of aflatoxin M1 in human urine. Cancer Res 7:1848–1852
Acknowledgments
Nurshad Ali is supported by a stipend from the German Academic Exchange Service (DAAD). Sample collection in Port au Prince and Quartier Morin were made possible by grants from the US Agency for International Development through the Peanut Collaborative Research Support Program and the US Borlaug Fellows in Global Food Security Program.
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Gerding, J., Ali, N., Schwartzbord, J. et al. A comparative study of the human urinary mycotoxin excretion patterns in Bangladesh, Germany, and Haiti using a rapid and sensitive LC-MS/MS approach. Mycotoxin Res 31, 127–136 (2015). https://doi.org/10.1007/s12550-015-0223-9
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DOI: https://doi.org/10.1007/s12550-015-0223-9