Fast and sensitive LC–MS/MS method measuring human mycotoxin exposure using biomarkers in urine

Archives of Toxicology

Volumn 89, Issue 11, 2015, Pages 1993-2005

  Huybrechts, B ^a   Martins, J C ^b   Debongnie, Ph ^a   Uhlig, S ^c   Callebaut, A ^a  

^a VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Biomarkers; Glucuronides; LC MS MS; Mycotoxin exposure; Urine

Indexed keywords

AFLATOXIN B1; AFLATOXIN B2; AFLATOXIN G1; AFLATOXIN M1; AFLATOXIN P1; BIOLOGICAL MARKER; CITRININ; DEOXYNIVALENOL 3 GUCURONIDE; DIACETOXYSCIRPENOL; FUSARENON X; MYCOTOXIN; OCHRATOXIN; UNCLASSIFIED DRUG; VOMITOXIN; DEEPOXY-DEOXYNIVALENOL; DEOXYNIVALENOL-15-GLUCURONIDE; DEOXYNIVALENOL-3-GLUCURONIDE; DIHYDROCITRINONE; GLUCURONIDE; TRICHOTHECENE DERIVATIVE;

ANTIBODY AFFINITY; ARTICLE; DETOXIFICATION; FEMALE; HETERONUCLEAR MULTIPLE BOND CORRELATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; LIQUID CHROMATOGRAPHY; MALE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; URINALYSIS; ADULT; ANALOGS AND DERIVATIVES; BELGIUM; PROCEDURES; URINE; VALIDATION STUDY;

ADULT; BELGIUM; BIOMARKERS; CHROMATOGRAPHY, LIQUID; CITRININ; FEMALE; GLUCURONIDES; HUMANS; MALE; MYCOTOXINS; OCHRATOXINS; TANDEM MASS SPECTROMETRY; TRICHOTHECENES;

EID: 84947584230     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1358-8     Document Type: Article

References (70)

1. Ahn J, Kim D, Kim H, Jahng KY (2010) Quantitative determination of mycotoxins in urine by LC–MS/MS. Food Addit Contam 27:1674–1682
2. Baldwin TT, Riley RT, Zitomer NC, Voss KA, Coulombe RA Jr, Pestka JJ, Williams DE, Glenn AE (2011) The current state of mycotoxin biomarker development in humans and animals and the potential for application to plant systems. World Mycotoxin J 4:257–270
3. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516
4. Berthiller F, Crews C, Dall’Asta C, Saeger SD, Haesaert G, Karlovsky P, Oswald IP, Seefelder W, Speijers G, Stroka J (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57:165–186
5. Blaszkewicz M, Muñoz K, Degen GH (2013) Methods for analysis of citrinin in human blood and urine. Arch Toxicol 87:1087–1094
6. Bryden W (2007) Mycotoxins in the food chain: human health implications. Asia Pac J Clin Nutr 16(Suppl 1):95–101
7. Cano-Sancho G, Marin S, Ramos AJ, Sanchis V (2010) Biomonitoring of Fusarium spp. mycotoxins: perspectives for an individual exposure assessment tool. Food Sci Technol Int 16:266–276
8. Cano-Sancho G, Sanchis V, Ramos AJ, Marín S (2013) Effect of food processing on exposure assessment studies with mycotoxins. Food Addit Contam Part A 30:867–875
9. Commission Decision 2002/657/EC Implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results. http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2002D0657:20040110:EN:PDF
10. Commission Decision 401/2006/EC Laying down the methods of sampling and analysis for the official control of the levels ofmycotoxins in foodstuffs. http://eurlex.europa.eu/LexUriServ/LexUriServ.do?uri=CONSLEG:2006R0401:20100313:EN:PDF
11. Coronel MB, Marin S, Tarragό 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 49:1436–1442
12. Desalegn B, Nanayakkara S, Harada KH, Hitomi T, Chandrajith R, Karunaratne U, Abeysekera T, Koizumi A (2011) Mycotoxin detection in urine samples from patients with chronic kidney disease of uncertain etiology in Sri Lanka. Bull Environ Contam Toxicol 87:6–10
13. Duarte SC, Pena A, Lino CM (2011) Human ochratoxin A biomarkers—from exposure to effect. Crit Rev Toxicol 41:187–212
14. 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 12:283–289
15. EFSA (2012) EFSA Panel on Contaminants in the Food Chain (CONTAM) Scientific Opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA J 10(3):2605
16. Flajs D, Peraica M (2009) Toxicological properties of citrinin. Arh Hig Rada Toksikol 60:457–464
17. Föllmann W, Behm C, Degen GH (2014) Toxicity of the mycotoxin citrinin and its metabolite dihydrocitrinone and of mixtures of citrinin and ochratoxin A in vitro. Arch Toxicol 88:1097–1107
18. 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 18:1088–1093
19. Gong YY, Torres-Sanchez L, Lopez-Carrillo L, Peng JH, Sutcliffe AE, White KL, Humpf H-U, Turner PC, Wild CP (2008) Association between tortilla consumption and human urinary fumonisin B1 levels in a Mexican population. Cancer Epidemiol Biomarkers 17:688–694
20. Groopman JD, Kensler TW (2005) Role of metabolism and viruses in aflatoxin-induced liver cancer. Toxicol Appl Pharmacol 206:131–137
21. Han Z, Tangni EK, Di Mavungu JD, Vanhaecke L, De Saeger S, Wu A, Callebaut A (2013) In vitro glucuronidation of ochratoxin A by rat liver microsomes. Toxins 5:2671–2685
22. Kemilainen H, Mykkanen O, Salminen S, El-Nezami H (2005) Fecal and urinary excretion of aflatoxin B1 metabolites (AFQ1, AFM1 and AFB-N7-guanine) in young Chinese males. Int J Cancer 115:879–884
23. Kensler TW, Roebuck BD, Wogan GN, Groopman JD (2011) Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol Sci 120:S28–S48
24. Klapec T, Šarkanj B, Banjari I, Strelec I (2012) Urinary ochratoxin A and ochratoxin alpha in pregnant women. Food Chem Toxicol 50:4487–4492
25. Lattanzio VMT, Solfrizzo M, De Girolamo A, Chulze SN, Torres AM, Visconti A (2011) LC-MS/MS characterization of the urinary excretion profile of the mycotoxin deoxynivalenol in human and rat. J Chromatogr B Anal Technol Biomed Life Sci 879:707–715
26. Leong YH, Latiff AA, Ahmad NI, Rosma A (2012) Exposure measurement of aflatoxins and aflatoxin metabolites in human body fluids. A short review. Mycotoxin Res 28:79–87
27. Manique R, Pena A, Lino CM, Moltó JC, Mañes J (2008) Ochratoxin A in the morning and afternoon portions of urine from Coimbra and Valencian population. Toxicon 51:1281–1287
28. Maresca M (2013) From the gut to the brain: journey and pathophysiological effects of the food-associated trichothecene mycotoxin deoxynivalenol. Toxins 5:784–820
29. Märtlbauer E, Usleber E, Dietrich R, Schneider E (2009) Ochratoxin A in human blood serum—retrospective long-term data. Mycotoxin Res 25:175–186
30. Matuszewski BK, Constanzer ML, Chavez-Eng CM (2003) Strategies for the assessment of matrix effect in quantitative bioanalytical methods based on HPLC-MS/MS. Anal Chem 75:3019–3030
31. Meky FA, Turner PC, Ashcroft AE, Miller JD, Qiao YL, Roth MJ, Wild CP (2003) Development of a urinary biomarker of human exposure to deoxynivalenol. Food Chem Toxicol 41:265–273
32. Mirocha CJ, Pathre SV, Robison TS (1981) Comparative metabolism of zearalenone and transmission into bovine milk. Food Cosmet Toxicol 19:25–30
33. Muñoz K, Blaszkewicz M, Degen GH (2010) Simultaneous analysis of ochratoxin A and its major metabolite ochratoxin alpha in plasma and urine for an advanced biomonitoring of the mycotoxin. J Chromatogr B 878:2623–2629
34. Mykkänen H, Zhu HL, Salminen E, Juvonen RO, Ling WH, Ma J, Polychronaki N, Kemilainen H, Mykkänen O, Salminen S, El-Nezami H (2005) Fecal and urinary excretion of aflatoxin B1 metabolites (AFQ1, AFM1and AFB-N-7-guanine) in young Chinese males. Int J Cancer 115:879–884
35. Neal GE, Eaton DL, Judah DJ, Verma A (1998) Metabolism and toxicity of aflatoxins M1 and B1 in human-derived in vitro systems. Toxicol Appl Pharmacol 151:152–158
36. Neter J, Kutner MH, Wasserman W, Nachtscheim CJ (1996) Applied linear regression models. McGraw-Hill College, New York
37. Njumbe Ediage E, Diana Di Mavungu J, Song S, Wu A, Van Peteghem C, De Saeger S (2012) A direct assessment of mycotoxin biomarkers in human urine samples by liquid chromatography tandem mass spectrometry. Anal Chim Acta 741:58–69
38. Pena A, Seifrtová M, Lino C, Silveira I, Solich P (2006) Estimation of ochratoxin A in Portuguese population:new data on the occurrence in human urine by high performance liquid chromatography with fluorescence detection. Food Chem Toxicol 44:1449–1454
39. Pepeljnjak S, Klarić MS (2010) «Suspects» in etiology of endemic nephropathy: aristolochic acid versus mycotoxins. Toxins 2:1414–1427
40. Pestka JJ (2010) Toxicological mechanisms and potential health effects of deoxynivalenol and nivalenol. World Mycotoxin J 3:323–347
41. Phillips RD, Hayes AW, Berndt WO (1980) High pressure liquid chromatographic analysis of the mycotoxin citrinin and its application to biological fluids. J Chromatogr 190:419–427
42. Piekkola S, Turner PC, Abdel-Hamid M, Ezzat S, El-Daly M, El-Kafrawy S, Savchenko E, Poussa T, Woo JCS, Mykkänen H, El-Nezami H (2012) Characterisation of aflatoxin and deoxynivalenol exposure among pregnant Egyptian women. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 29:962–971
43. Ramsdell HS, Parkinson A, Eddy AC, Eaton DL (1991) Bioactivation of aflatoxin B1 by human liver microsomes: role of cytochrome P450 IIIA enzymes. Toxicol Appl Pharmacol 108:436–447
44. Richard JL (2007) Some major mycotoxins and their mycotoxicoses—an overview. Int J Food Microbiol 119:3–10
45. Riley RT, Torres O, Showker JL, Zitomer NC, Matute J, Voss KA, Gelineau-van Waes J, Maddox JR, Gregory SG, Ashley-Koch AE (2012) The kinetics of urinary fumonisin B1 excretion in humans consuming maize-based diets. Mol Nutr Food Res 56:1445–1455
46. Rubert J, Soriano JM, Manes J, Soler C (2011) Rapid mycotoxin analysis in human urine: a pilot study. Food Chem Toxicol 49:2299–2304
47. Scott PM (2005) Biomarkers of human exposure to ochratoxin A. Food Addit Contam 22:99–107
48. Shephard GS (2008a) Impact of mycotoxins on human health in developing countries. Food Addit Contam Part A 25:146–151
49. Shephard GS (2008b) Risk assessment of aflatoxins in food in Africa. Food Addit Contam Part A 25:1246–1256
50. Silva LJP, Pena A, Lino CL, Fernández M, Mañes J (2010) Fumonisins determination in urine by LC–MS–MS. Anal Bioanal Chem 396:809–816
51. Solfrizzo M, Gambacorta L, Lattanzio VMT, Powers S, Visconti A (2011) Simultaneous LC–MS/MS determination of aflatoxin M1, ochratoxin A, deoxynivalenol, de-epoxydeoxynivalenol, α and β-zearalenols and fumonisin B1 in urine as a multi-biomarker method to assess exposure to mycotoxins. Anal Bioanal Chem 401:2831–2841
52. Song S, Njumbe Ediage E, Wu A, De Saeger S (2013) Development and application of salting-out assisted liquid/liquid extraction for multi-mycotoxin biomarkers analysis in pig urine with high performance liquid chromatography/tandem mass spectrometry. J Chromatogr A 1292:111–120
53. Turner PC, Rothwell JA, White KL, Gong Y, Cade JE, Wild CP (2008) Urinary deoxynivalenol is correlated with cereal intake in individuals from the United Kingdom. Environ Health Perspect 116:21–25
54. Turner PC, Taylor EF, White KLM, Cade JE, Wild CP (2009) A comparison of 24 h urinary deoxynivalenol with recent average cereal consumption for UK adults. Br J Nutr 102:1276–1279
55. Turner PC, White KL, Burley VJ, Hopton RP, Rajendram A, Fisher J, Cade JE, Wild CP (2010) A comparison of deoxynivalenol intake and urinary deoxynivalenol in UK adults. Biomarkers 15:553–562
56. Turner PC, Hopton RP, White KLM, Fisher J, Cade JE, Wild CP (2011) Assessment of deoxynivalenol metabolite profiles in UK adults. Food Chem Toxicol 49:132–135
57. Turner PC, Flannery B, Isitt C, Ali M, Pestka J (2012) The role of biomarkers in evaluating health concerns from fungal contaminants in food. Nutr Res Rev 25:162–179
58. Uhlig S, Ivanova L, Fæste CK (2013) Enzyme-assisted synthesis and structural characterization of the 3-, 8-, and 15-glucuronides of deoxynivalenol. J Agric Food Chem 61:2006–2012
59. Van Der Westhuizen L, Shephard GS, Burger HM, Rheeder JP, Gelderblom WCA, Wild CP, Gong YY (2011) Fumonisin B1 as a urinary biomarker of exposure in a maize intervention study among South African subsistence farmers. Cancer Epidemiol Biomarkers Prev 20:483–489
60. Versilovskis A, Geys J, Huybrechts B, Goossens E, De Saeger S, Callebaut A (2012) Simultaneous determination of masked forms of deoxynivalenol and zearalenone after oral dosing in rats by LC–MS/MS. World Mycotoxin J 5:303–318
61. Warth B, Sulyok M, Berthiller F, Schuhmacher R, Fruhmann P, Hametner C, Adam G, Frohlich J, Krska R (2011) Direct quantification of deoxynivalenol glucuronide in human urine as biomarker of exposure to the Fusarium mycotoxin deoxynivalenol. Anal Bioanal Chem 401:195–200
62. Warth B, Sulyok M, Fruhmann P, Berthiller F, Schuhmacher R, Hametner C, Adam G, Frohlich J, Krska R (2012a) Assessment of human deoxynivalenol exposure using an LC–MS/MS based biomarker method. Toxicol Lett 211:85–90
63. Warth B, Sulyok M, Fruhmann P, Mikula H, Berthiller F, Schuhmacher R, Hametner C, Abia WA, Adam G, Fröhlich J, Krska R (2012b) Development and validation of a rapid multi-biomarker liquid chromatography/tandem mass spectrometry method to assess human exposure to mycotoxins. Rapid Commun Mass Spectrom 26:1533–1540
64. Warth B, Sulyok M, Krska R (2013a) LC-MS/MS-based multi-biomarker approaches for the assessment of human exposure to mycotoxins. Anal Bioanal Chem 405:5687–5695
65. Warth B, Sulyok M, Berthiller F, Schuhmacher R, Krska R (2013b) New insights into the human metabolism of the Fusarium mycotoxins deoxynivalenol and zearalenone. Toxicol Lett 220:88–94
66. Wild C, Gong Y (2010) Mycotoxins and human diseases: a largely ignored global health issue. Carcinogenesis 31:71–82
67. Wu X, Murphy P, Cunnick J, Hendrich S (2007) Synthesis and characterization of deoxynivalenol glucuronide: its comparative immunotoxicity with deoxynivalenol. Food Chem Toxicol 45:1846–1855
68. Xu L, Cai Q, Tang L, Wang S, Hu X, Su J, Sun G, Wang JS (2010) Evaluation offumonisin biomarkers in a cross-sectional study with two high-risk populations in China. Food Addit Contam 27:1161–1169
69. Zhu JQ, Zhang LS, Hu X (1987) Correlation of dietary aflatoxin B1 levels with excretion of aflatoxin M1 in human urine. Cancer Res 47:1848–1852
70. Zinedine A, Soriano JM, Molto JC, Manes J (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem Toxicol 45:1–18