Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
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Survey on Contamination of Beauvericin and Enniatins in Korean Ginger and Ginger Powder

국내산 생강 및 생강가루의 Beauvericin과 Enniatins 오염도 조사

  • Lee, Mi Jeong (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lim, Soo Bin (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Choi, Jung-Hye (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Jeomsoon (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Lee, Theresa (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Jang, Ja Yeong (Microbial Safety Division, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2022.10.12
  • Accepted : 2022.10.17
  • Published : 2022.10.30
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Abstract

Levels of beauvericin (BEA) and enniatins (ENNs: ENA, ENA1, ENB, and ENB1) were examined in fresh ginger (n = 43) and ginger powder (n = 31) samples from Korea. In the ginger samples, incidence of BEA contamination was highest, at 62.79%, with a maximum detected BEA level of 640.07 ㎍/kg. ENNs in were found in up to 11.63% (ENB, ENB1) of ginger samples, with a maximum detected level of 91.02 ㎍/kg (ENA). In the ginger powders, ENB contamination displayed the highest rate of incidence (70.97%), but the highest level of BEA (1,344.18 ㎍/kg) exceeded that of ENB (413.99 ㎍/kg). The incidences of ENA, ENA1, ENB, and ENB1 presence in ginger powders were 29.03%, 22.58%, 70.97%, and 35.48%, respectively, and their highest detected levels were 220.45, 156.61, 413.99, and 70.29 ㎍/kg, respectively. The incidence of BEA and ENN contamination was higher in ginger powder than in ginger. Respective co-occurrence rates of BEA and ENNs in ginger and ginger powder samples were 16.28% and 64.52%, indicating that the BEA and ENN co-contamination rate was highest in ginger powder as well. This is the first report on the presence and co-occurrence of BEA and ENNs in Korean ginger and ginger powder.

본 연구에서는 국내산 생강(n = 43)과 생강가루(n = 31)를 대상으로 beauvericin (BEA)과 enniatins (ENNs)의 오염 실태를 조사하였다. 생강 시료 중 62.79%가 BEA에 오염되었으며, 최대 오염농도는 640.07 ㎍/kg으로 오염률과 오염농도가 조사 대상 독소 중 가장 높았다. 생강에서 ENNs의 오염률은 최대 11.63% (ENB, ENB1)이었으며, 최대 오염농도는 91.02 ㎍/kg (ENA)였다. 생강가루에서는 ENB의 오염률이 70.97%로 가장 높았으나, 오염농도는 BEA이 최대 1, 344.18 ㎍/kg으로 조사 대상 독소 중 가장 높았다. 생강가루의 ENA, ENA1, ENB, ENB1의 오염률은 29.03%, 22.58%, 70.97%, 35.48%였으며, 최대 오염농도는 220.45 ㎍/kg, 156.61 ㎍/kg, 413.99 ㎍/kg, 70.29 ㎍/kg로 ENB의 오염률과 오염농도가 높았다. BEA과 ENNs은 생강보다 생강가루에서 오염농도가 높았다. 생강과 생강가루에서 BEA과 ENNs의 중복 오염률은 각각 16.28%와 64.52%로 생강에 비해 생강가루에서 독소의 중복오염률이 높았다. 본 연구는 한국산 생강과 생강가루의 BEA과 ENNs의 발생 및 이들의 중복 오염을 처음으로 보고하는 것이다.

Keywords

Acknowledgement

본 연구는 농촌진흥청 국립농업과학원 농업과학기술 연구개발사업(과제번호: PJ014811)의 지원에 의해 수행되었습니다.

References

  1. Nakai, V.K., de Oliveira Rocha, L., Goncalez, E., Fonseca, H., Ortega, E.M.M., Correa, B., Distribution of fungi and aflatoxins in a stored peanut variety. Food Chem., 106, 285-290 (2008). https://doi.org/10.1016/j.foodchem.2007.05.087
  2. Omotayo, O.P., Omotayo, A.O., Babalola, O.O., Mwanza, M., Comparative study of aflatoxin contamination of winter and summer ginger from the North West Province of South Africa. Toxicol. Rep., 6, 489-495 (2019). https://doi.org/10.1016/j.toxrep.2019.05.011
  3. Jajic, I., Dudas, T., Krstovic, S., Krska, R., Sulyok, M., Bagi, F., Savic, Z., Guljas, D., Stankov, A., Emerging Fusarium mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin in Serbian maize. Toxins, 11, 357 (2019). https://doi.org/10.3390/toxins11060357
  4. Song, H.-H., Lee, H.-S., Lee, C., Survey of beauvericin contamination in Korean grains by HPLC and the production of beauvericin and enniatin derivatives by Fusairum oxysporum KFCC 11363P. J. Food Hyg. Saf., 23, 73-79 (2008).
  5. Santini, A., Meca, G., Uhlig, S., Ritieni, A., Fusaproliferin, beauvericin and enniatins: occurrence in food-a review. World Mycotoxin J., 5, 71-81 (2012). https://doi.org/10.3920/WMJ2011.1331
  6. Tomoda, H., Nishida, H., Huang, X.-H., Masuma, R., KIim, Y.K., Omura, S., New cyclodepsipeptides, enniatins D, E and f produced by Fusarium sp. FO-1305Au. J. Antibiot. Res., 45, 1207-1215 (1992). https://doi.org/10.7164/antibiotics.45.1207
  7. Ganassi, S., Moretti, A., Pagliai, A.M.B., Logrieco, A., Sabatini, M.A., Effects of beauvericin on Schizaphis graminum (Aphididae). J. Invertebr. Pathol., 80, 90-96 (2002). https://doi.org/10.1016/S0022-2011(02)00125-8
  8. Calo, L., Fornelli, F., Ramires, R., Nenna, S., Tursi, A., Caiaffa, M.F., Macchia, L., Cytotoxic effects of the mycotoxin beauvericin to human cell lines of myeloid origin. Pharmacol. Res., 49, 73-77 (2004). https://doi.org/10.1016/j.phrs.2003.07.002
  9. Calo, L., Fornelli, F., Nenna, S., Tursi, A., Caiaffa, M.F., Macchia, L., Beauvericin cytotoxicity to the invertebrate cell line SF-9. J. Appl. Genet., 44, 515-520 (2003).
  10. Mahnine, N., Meca, G., Elabidi, A., Fekhaoui, M., Saoiabi, A., Font, G., Manes, J., Zinedine, A., Further data on the levels of emerging Fusarium mycotoxins enniatins (A, A1, B, B1), beauvericin and fusaproliferin in breakfast and infant cereals from Morocco. Food Chem., 124, 481-485 (2011). https://doi.org/10.1016/j.foodchem.2010.06.058
  11. Macchia, L., Di Paola, R., Fornelli, F., Nenna, S., Moretti, A., Napoletano, R., Logrieco, A., Caiaffa, M., Tursi, A., Bottalico, A. 1995. Cytotoxicity of beauvericin to mammalian cells. Book of asbstract International Seminar on Fusarium: Mycotoxins, Taxonomy and Pathogenicity, May 9-13, 1995, Martina Franca, Italy, pp. 72-73.
  12. Fornelli, F., Minervini, F., Logrieco, A., Cytotoxicity of fungal metabolites to lepidopteran (Spodoptera frugiperda) cell line (SF-9). J. Invertebr. Pathol., 85, 74-79 (2004). https://doi.org/10.1016/j.jip.2004.01.002
  13. Gruber-Dorninger, C., Novak, B., Nagl, V., Berthiller, F., Emerging mycotoxins: Beyond traditionally determined food contaminants. J. Agric. Food Chem., 65, 7052-7070 (2017). https://doi.org/10.1021/acs.jafc.6b03413
  14. Jestoi, M., Somma, M.C., Kouva, M., Veijalainen, P., Rizzo, A., Ritieni, A., Peltonen, K., Levels of mycotoxins and sample cytotoxicity of selected organic and conventional grainbased products purchased from Finnish and Italian markets. Mol. Nutr. Food Res., 48, 299-307 (2004). https://doi.org/10.1002/mnfr.200400026
  15. Tedjiotsop Feudjio, F., Dornetshuber, R., Lemmens, M., Hoffmann, O., Lemmens-Gruber, R., Berger, W., Beauvericin and enniatin: emerging toxins and/or remedies? World Mycotoxin J., 3, 415-430 (2010). https://doi.org/10.3920/WMJ2010.1245
  16. Altomare, C., Logrieco, A.F., Gallo, A., 2021. Mycotoxins and Mycotoxigenic Fungi: Risk and Management. A Challenge for Future Global Food Safety and Security. In: Zaragoza, O. (Ed.), Encyclopedia of Mycology, vol. 1. Elsevier, Amsterdam, Netherlands. pp. 64-93.
  17. Meca, G., Zinedine, A., Blesa, J., Font, G., Manes, J., Further data on the presence of Fusarium emerging mycotoxins enniatins, fusaproliferin and beauvericin in cereals available on the Spanish markets. Food Chem. Toxicol., 48, 1412-1416 (2010). https://doi.org/10.1016/j.fct.2010.03.010
  18. Bryla, M., Waskiewicz, A., Podolska, G., Szymczyk, K., Jedrzejczak, R., Damaziak, K., Sulek, A., Occurrence of 26 mycotoxins in the grain of cereals cultivated in Poland. Toxins, 8, 160 (2016). https://doi.org/10.3390/toxins8060160
  19. Juan, C., Manes, J., Raiola, A., Ritieni, A., Evaluation of beauvericin and enniatins in Italian cereal products and multicereal food by liquid chromatography coupled to triple quadrupole mass spectrometry. Food Chem., 140, 755-762 (2013). https://doi.org/10.1016/j.foodchem.2012.08.021
  20. Nazari, F., Sulyok, M., Kobarfard, F., Yazdanpanah, H., Krska, R., Evaluation of emerging Fusarium mycotoxins beauvericin, enniatins, fusaproliferin and moniliformin in domestic rice in Iran. Iran. J. Pham. Res., 14, 505 (2015).
  21. Yoshinari, T., Suzuki, Y., Sugita-Konishi, Y., Ohnishi, T., Terajima, J., Occurrence of beauvericin and enniatins in wheat flour and corn grits on the Japanese market, and their co-contamination with type B trichothecene mycotoxins. Food Addit. Contam. Part A, 33, 1620-1626 (2016). https://doi.org/10.1080/19440049.2016.1228126
  22. Reyes-Velazquez, W.P., Figueroa-Gomez, R.M., Barberis, M., Reynoso, M.M., Rojo, F.G., Chulze, S.N., Torres, A.M., Fusarium species (section Liseola) occurrence and natural incidence of beauvericin, fusaproliferin and fumonisins in maize hybrids harvested in Mexico. Mycotxin Res., 27, 187-194 (2011). https://doi.org/10.1007/s12550-011-0095-6
  23. Yang, X., Gao, J., Liu, Q., Yang, D., Co-occurrence of mycotoxins in maize and maize-derived food in China and estimation of dietary intake. Food Addit. Contam. Part B, 12, 124-134 (2019). https://doi.org/10.1080/19393210.2019.1570976
  24. Lin, X., Zhang, Q., Zhang, Y., Li, J., Zhang, M., Hu, X., Li, F., Further data on the levels of emerging Fusarium mycotoxins in cereals collected from Tianjin, China. Food Addit. Contam. Part B, 14, 74-80 (2021). https://doi.org/10.1080/19393210.2021.1873425
  25. Kim, D.-B., Song, N.-E., Nam, T.G., Lee, S., Seo, D., Yoo, M., Occurrence of emerging mycotoxins in cereals and cereal-based products from the Korean market using LCMS/MS. Food Addit. Contam. Part A, 36, 289-295 (2019). https://doi.org/10.1080/19440049.2018.1562233
  26. Trucksess, M.W., Weaver, C.M., Oles, C.J., Rump, L.V., White, K.D., Betz, J.M., Rader, J.I., Use of multitoxin immunoaffinity columns for determination of aflatoxins and ochratoxin A in ginseng and ginger. J. AOAC Int., 90, 1042-1049 (2007). https://doi.org/10.1093/jaoac/90.4.1042
  27. Lee, M.J., Lim, S.B., Choi, J.-H., Kim, J., Lee, T., Jang, J.Y., Occurrence of deoxynivalenol and nivalenol in Korean ginger and the optimal storage conditions for reducing mycotoxins. Korean J. Food Preserv., 28, 878-889 (2021). https://doi.org/10.11002/kjfp.2021.28.7.878
  28. De Colli, L., Elliott, C., Finnan, J., Grant, J., Arendt, E.K., McCormick, S.P., Danaher, M., Determination of 42 mycotoxins in oats using a mechanically assisted QuEChERS sample preparation and UHPLC-MS/MS detection. J. Chromatogr. B, 1150, 122187 (2020). https://doi.org/10.1016/j.jchromb.2020.122187
  29. Ministry of Food and Drug Safety, 2016. Guidelines on standard procedures for preparing analysis method. Cheongju, Korea, notice 2017-57.
  30. Hu, L., Rychlik, M., Occurrence of enniatins and beauvericin in 60 Chinese medicinal herbs. Food Addit. Contam. Part A, 31, 1240-1245 (2014).
  31. Jegal, S., Kim, J.-H., Joo, G.-S., Jung, S.-J., Na, H.-J., Jo, N.-G., Lee, J.-M., Kim, Y.-H., Survery of aflatoxin B1 and ochratoxin A on commercial dried red pepper and red pepper powder. J. Food Hyg. Saf., 28, 267-271 (2013). https://doi.org/10.13103/JFHS.2013.28.3.267
  32. EFSA, Scientific Opinion on the risks to human and animal health related to the presence of beauvericin and enniatins in food and feed. EFSA J., 12, 3802 (2014).
  33. Smith, M.-C., Madec, S., Coton, E., Hymery, N., Natural cooccurrence of mycotoxins in foods and feeds and their in vitro combined toxicological effects. Toxins, 8, 94 (2016). https://doi.org/10.3390/toxins8040094
  34. Grenier, B., Oswald, I., Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. World Mycotoxin J., 4, 285-313 (2011). https://doi.org/10.3920/WMJ2011.1281
  35. Juan, C., Ritieni, A., Manes, J., Occurrence of Fusarium mycotoxins in Italian cereal and cereal products from organic farming. Food Chem., 141, 1747-1755 (2013). https://doi.org/10.1016/j.foodchem.2013.04.061
  36. Blesa, J., Molto, J.-C., El Akhdari, S., Manes, J., Zinedine, A., Simultaneous determination of Fusarium mycotoxins in wheat grain from Morocco by liquid chromatography coupled to triple quadrupole mass spectrometry. Food Control, 46, 1-5 (2014). https://doi.org/10.1016/j.foodcont.2014.04.019