Studying the contamination of tea and herbal infu-sions with myсotoxins (Message 2)

View or download the full article: 
UDC: 
542.06;543.544.5.068.7;579.674
Authors: 

M.G. Kiseleva, Z.A. Chalyy, I.B. Sedova, L.P. Minaeva, S.A. Sheveleva

Organization: 

Federal Research Centre of Nutrition, Biotechnology and Food Safety, 2/14 Ustinsky lane, Moscow, 109240, Russian Federation

Abstract: 

The occurrence of wide spectrum of mycotoxins has been studied in C. sinensis and herbal tea available in the Russian Federation by ultra high performance liquid chromatography coupled to tandem mass spectrometer (UHPLC-MS/MS). The batch of 77 samples consisted of 54 samples of bulk loose (prepacked) and packed C. sinensis tea and 23 individual and mixed herbal teas. The list of determined analytes included 29 mycotoxins: regulated in food (aflatoxins, ochratoxin A, deoxinivalenol, fumonisins, T-2 toxin and zaeralenone), their derivatives and structural analogues (A- and B-trichothecenes, mycotoxins of zearalenone group) and emerging mycotoxins (sterigmatocystin, mycophenolic acid, enniatins, beauvericin, Alternaria toxins). Samples of green and black C. sinensis tea were almost negative or contaminated at about LOD levels. Herbal teas, especially multi component, proved to be the most contaminated. Co-occurrence of several analytes (over five), including regulated and emerging mycotoxins, has been detected. The most frequent pattern was mycopenolic acid, Alternaria mycotoxins (tentoxin, alternariol and its methyl ether), enniatin B, beauvericin and sterigmatocystin. Beauvericin, enniatin B and mycophenolic acid were common for all types of studied tea samples. The study of the toxinogenic properties of tea mycoflora in vitro showed the ability of toxigenic species of molds to produce significant quantities of several types of mycotoxins, including emergent, simultaneously. The production of mycotoxins by molds on a substrate of C. sinensis green tea leaves has been 290 and 5600 μg/kg of fumonisins B1 and B2 correspondingly, 130 μg/kg of zearalenone, 14 μg/kg of sterigmatocystin and 160 μg/kg of alternariol methyl ether. These results indicate a potential risk of herbal teas to human health associated with wide spectrum of mycotoxins, especially emerging ones. Their regular monitoring in tea and data accumulation is necessary to assess the safety of this type of food products. The present study is the first attempt to estimate contamination of tea available in Russia with toxigenic mold and their secondary metabolites.

Keywords: 
mycotoxins; emergent mycotoxins; fungal contamination; in vitro mycotoxin production; C. sinensis tea; herbal tea; UHPLC-MS/MS
Kiseleva M.G., Chalyy Z.A., Sedova I.B., Minaeva L.P., Sheveleva S.A. Studying the contamination of tea and herbal infu-sions with myсotoxins (Message 2). Health Risk Analysis, 2020, no. 1, pp. 38–51. DOI: 10.21668/health.risk/2020.1.04.eng
References: 
  1. Worldwide regulations for mycotoxins in foods and feeds in 2003. Food and Agriculture Organization (FAO). FAO Food and Nutrition Paper 81, Rome, Italy, 2004. Available at: http://www.fao.org/3/y5499e/y5499e00.htm (20.11.2019).
  2. Logrieco A.F., Miller J.D., Eskola M., Krska R., Ayalew A., Bandyopadhyay R., Battilani P., Bhatnagar D. [et al.]. The Mycotox Charter: Increasing Awareness of, and Concerted Action for, Minimizing Mycotoxin Exposure Worldwide. Toxins, 2018, vol. 10, no. 149, pp. E149. DOI: 10.3390/toxins10040149 3
  3. Njumbe Ediage E., Van Poucke C., De Saeger S. A multi-analyte LC-MS/MS method for the analysis of 23 mycotoxins in different sorghum varieties: the forgotten sample matrix. Food chemistry, 2015, vol. 15, no. 177, pp. 397–404. DOI: 10.1016/j.foodchem.2015.01.060
  4. García-Moraleja A., Font G., Mañes J., Ferrer E. Development of a new method for the simultaneous determination of 21 mycotoxins in coffee beverages by liquid chromatography tandem mass spectrometry. Food Research International, 2015, vol. 72, pp. 247–255. DOI: 10.1016/j.foodres.2015.02.030
  5. Abdallah M.F., Krska R., Sulyok M. Occurrence of Ochratoxins Fumonisin B2 Aflatoxins (B1 and B2) and Other Secondary Fungal Metabolites in Dried Date Palm Fruits from Egypt: A Mini-Survey. Journal of food science, 2018, vol. 83, no. 2, pp. 559–564. DOI: 10.1111/1750-3841.14046
  6. Juan C., Covarelli L., Beccari G., Colasante V., Manes J. Simultaneous analysis of twenty-six mycotoxins in durum wheat grain from Italy. Food Control, 2016, vol. 62, pp. 322–329. DOI: 10.1016/j.foodcont.2015.10.032
  7. Fraeyman S., Croubels S., Devreese M., Antonissen G. Emerging Fusarium and Alternaria Mycotoxins: Occurrence, Toxicity and Toxicokinetics. Toxins, 2017, vol. 18, no. 9 (7), pp. E228. DOI: 10.3390/toxins9070228
  8. Scientific Opinion on the risks for animal and public health related to the presence of Alternaria-toxins in feed and food. EFSA Journal, 2011, vol. 9, no. 10, pp. 2407. DOI: 10.2903/j.efsa.2011.2407
  9. Scientific Opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA Journal, 2014, vol. 12, no. 8, pp. 3802. DOI: 10.2903/j.efsa.2014.3802
  10. Sedova I.B., Kiseleva M.G., Zakharova L.P., Tutel'yan V.A. Toxicological and hygienic characteristics of mycotoxin sterigmatocystin and methods for its determination in food products. Gigiena i sanitariya, 2019, vol. 98, no. 1, pp. 105–117 (in Russian).
  11. Sedova I., Kiseleva M., Tutelyan V. Mycotoxins in Tea: Occurrence, Methods of Determination and Risk Evaluation. Toxins, 2018, vol. 10, no. 11, pp. 444. DOI: 10.3390/toxins10110444
  12. Rocha-Miranda F., Venancio A. Mycotoxigenic fungi in plant-based supplements and medicines. Current Opinion in Food Science, 2019, vol. 30, pp. 27–31. DOI: 10.1016/j.cofs.2018.08.003
  13. Minaeva L.P., Aleshkina A.I., Markova Y.M., Polyanina A.S., Pichugina T.V., Bykova I.B., Stetsenko V.V., Efimochkina N.R., Sheveleva S.A. Studying the contamination of tea and herbal infusions with mold fungi as potential mycotoxin producers: The first step to risk assessment (Message 1). Health Risk Analysis, 2019, no. 1, pp. 93–102 (in Russian). DOI: 10.21668/health.risk/2019.1.10.eng
  14. Han X., Xu W., Zhang J., Xu J., Li F. Co-Occurrence of Beauvericin and Enniatins in Edible Vegetable Oil Samples, China. Toxins, 2019, vol. 11, no. 2, pp. 100. DOI: 10.3390/toxins11020100
  15. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 56. Some Naturally Occurring Sub-stances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins. International Agency for Research on Cancer, Lyon, France, 1993, 609 p.
  16. Zhang Y., Skaar I., Sulyok M., Liu X., Rao M., Taylor J.W. The Microbiome and Metabolites in Fermented Pu-erh Tea as Revealed by High-Throughput Sequencing and Quantitative Multiplex Metabolite Analysis. PLoS ONE, 2016, vol. 11, pp. e0157847. DOI: 10.1371/journal.pone.0157847
  17. Wu J.-Y., Yang G.-Y., Chen J.-L., Li W.-X., Li J.-T., Fu C.-X., Jiang G.-F., Zhu W. Investigation for Pu-erh tea con-tamination caused by mycotoxins in a tea market in Guangzhou. J. Basic Appl. Sci, 2014, vol. 10, pp. 349–356. DOI: 10.6000/1927-5129.2014.10.46
  18. Haas D., Pfeifer B., Reiterich C., Partenheimer R., Reck B., Buzina W. Identification and quantification of fungi and mycotoxins from Pu-erh tea. Int. J. Food Microbiol, 2013, vol. 166, pp. 316–322. DOI: 10.1016/j.ijfoodmicro.2013.07.024
  19. Vinokurova N.G., Ivanushkina N.E., Kochkina G.A., Arinbasarov M.U., Ozerskaya S.M. Production of Mycophenolic acid by fungi of the genus Penicillium Link. Prikladnaya biokhimiya i mikrobiologiya, 2005, vol. 41, no. 1, pp. 95–98 (in Rus-sian).
  20. Burkin A.A., Kononenko G.P. Producers of mycophenolic acid in ensiled and grain feeds. Applied Biochemistry and Microbiology, 2010, vol. 46, no. 5, pp. 545–550. DOI: 10.1134/S0003683810050145
  21. Compendium of Guidelines for Herbal and Fruit Infusions. Tea & Herbal Infusions Europe (THIE). Available at: http://www.thie-online.eu/fileadmin/inhalte/Publications/HFI/2018/2018-0... (26.11.2019).
  22. Venkatesh N., Keller N.P. Mycotoxins in Conversation with Bacteria and Fungi. J. Front Microbiol, 2019, vol. 10, pp. 403. DOI: 10.3389/fmicb.2019.00403
  23. Reinholds I., Bogdanova E., Pugajeva I., Bartkevics V. Mycotoxins in herbal teas marketed in Latvia and dietary expo-sure assessment. J. Food Additives & Contaminants: Part B, 2019, vol. 12, no. 3, pp. 199–208. DOI: 10.1080/19393210.2019.1597927
  24. Santos L., Marın S., Sanchis V., Ramos A.J. Screening of mycotoxin multicontaminationin medicinal and aromatic herbs sampled in Spain. J. Sci Food Agric, 2009, vol. 89, pp. 1802–1807. DOI: 10.1002/jsfa.3647
  25. Burkin A.A., Kononenko G.P. Mycotoxin contamination of meadow grasses in European Russia. Sel'skokho-zyaistvennaya biologiya, 2015, vol. 50, no. 4, pp. 503–512 (in Russian). DOI: 10.15389/agrobiology.2015.4.503rus
  26. Speijers G.J.A., Speijers M.H.M. Combined toxic effects of mycotoxins. J. Toxicol Lett, 2004, vol. 153, pp. 91–98. DOI:10.1016/j.toxlet.2004.04.046
  27. Yang Y., Yu S., Tan Y., Liu N., A. Wu. Individual and Combined Cytotoxic Effects of Co-Occurring Deoxynivalenol Family Mycotoxins on Human Gastric Epithelial Cells. J. Toxins (Basel), 2017, vol. 9, no. 3, pp. 96. DOI: 10.3390/toxins9030096
  28. Hou L.L., Zhou X., Gan F., Liu Z.X., Zhou Y.J., Qian G., Huang K. Combination of selenomethionine and N-acety-lcysteine alleviates the joint toxicities of aflatoxin B1 and ochratoxin A by ERK MAPK signal pathway in porcine alveolar mac-rophages. J. Agric. Food Chem, 2018, vol. 66, no. 23, pp. 5913–5923. DOI: 10.1021/acs.jafc.8b01858
  29. Ruiz M.J., Franzova P., Juan-García A., Font G. Toxicological interactions between the mycotoxins beauvericin, deoxynivalenol and T-2 toxin in CHO-K1 cells in vitro. Toxicon, 2011, vol. 58, no. 4, pp. 315–326. DOI: 10.1016/j.toxicon.2011.07.015
  30. Smith M.C., Madec S., Coton E., Hymery N. Natural Co-Occurrence of Mycotoxins in Foods and Feeds and Their in Vitro Combined Toxicological Effects. Toxins (Basel), 2016, vol. 8, no. 4, pp. 94. DOI: 10.3390/toxins8040094
  31. Opinion on the potential microbiological risk arising from the presence of moisture in tea. Scientific Committee on Foods, European Union, 2016. Available at: http://www.thie-online.eu/tea/quality-assurance/ (26.11.2019).
  32. Mo H.Z., Zhang H., Wu Q.H., Hu L.B. Inhibitory effects of tea extract on aflatoxin production by Aspergillus flavus. Lett. Appl. Microbiol, 2013, vol. 56, pp. 462–466. DOI: 10.1111/lam.12073
  33. Carraturo F., De Castro O., Troisi J., De Luca A., Masucci A., Cennamo P., Trifuoggi M., Aliberti F. Comparative assessment of the quality of commercial black and green tea using microbiology analyses. BMC Microbiology, 2018, vol. 18, no. 1, pp. 4. DOI: 10.1186/s12866-017-1142-z
  34. Storari M., Dennert F.G., Bigler L., Gessler C., Broggini G.A.L. Isolation of mycotoxins producing black aspergilli in herbal teas available on the Swiss market. Food Control, 2012, vol. 26, pp. 157–161. DOI: 10.1016/j.foodcont.2012.01.026
  35. Shi W., Tan Y., Wang S., Gardiner D.M., De Saeger S., Liao Y., Wang C., Fan Y., Wang Z., Wu A. Mycotoxigenic Potentials of Fusarium Species in Various Culture Matrices Revealed by Mycotoxin Profiling. Toxins, 2017, vol. 9, no. 1, pp. 6. DOI: 10.3390/toxins9010006
  36. Mogensen J.M., Nielsen K.F., Samson R.A., Frisvad J.C., Thrane U. Effect of temperature and water activity on the production of fumonisins by Aspergillus niger and different Fusarium species. BMC Microbiol, 2009, vol. 31, no. 9, 281 p. DOI: 10.1186/1471-2180-9-281
Received: 
28.11.2020
Accepted: 
03.02.2020
Published: 
30.03.2020

You are here