Evaluation of Anti-Aflatoxin M1 effects of heat-killed cells of Saccharomyces cerevisiae in Brazilian commercial yogurts
Main Article Content
Keywords
AFM1, decontamination, Saccharomyces cerevisiae, yeasts, yogurts
Abstract
This study aimed to assess the aflatoxin M1 (AFM1) levels in 72 samples of yogurt from eight processing plants in São Paulo, Brazil, and the ability of heat-killed cells of Saccharomyces cerevisiae (1010 yeast cells/g) to reduce AFM1 (0.5 µg/kg) in experimental yogurts (n = 3). Analyses were conducted by high performance liquid chromatography (HPLC). Only seven samples (9.8%) had AFM1 at a mean level of 0.071 ± 0.08 µg/kg. S. cerevisiae efficiently reduced (P < 0.05) the AFM1 levels in spiked yogurts, with a maximum reduction of 46% after 30 days of storage. Further studies should investigate potential effects of S. cerevisiae on the sensory properties of yogurts.
References
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Corassin, C., Bovo, F., Rosim, R. and Oliveira, C., 2013. Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control 31: 80–83. 10.1016/j.foodcont.2012.09.033
Cruz, A., Cavalcanti, R., Gherreiro, L., Sant’ana, A., Nogueira, L., Oliveira, C., Deliza, R., Cunha, R., Faria, J. and Bolini, H., 2013. Developing a prebiotic yogurt: rheological, physico-chemical and microbiological aspects and adequacy of survival analysis methodology. Journal of Food Engineering 114: 323–330. 10.1016/j.jfoodeng.2012.08.018
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Gonçalves, B., Corassin, C. and Oliveira, C., 2015. Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advance 10: 752–760. 10.3923/ajava.2015.752.760
Gonçalves, B., Gonçalves, J., Rosim, R., Cappato, L., Cruz, A., Oliveira, C. and Corassin, C., 2017. Effects of different sources of Saccharomyces cerevisiae biomass on milk production, composition, and aflatoxin M1 excretion in milk from dairy cows fed aflatoxin B1. Journal of Dairy Science 100: 5701–5708. 10.3168/jds.2016-12215
Gonçalves, B., Muaz, K., Coppa, C., Rosim, R., Kamimura, E., Oliveira, C. and Corassin, C., 2020. Aflatoxin M1 absorption by non-viable cells of lactic acid bacteria and Saccharomyces cerevisiae strains in Minas Frescal cheese. Food Research International 136: 109604. 10.1016/j.foodres.2020.109604
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Govaris, A., Roussi, V., Koidis, P. and Botsoglou, N., 2002. Distribution and stability of aflatoxin M1 during production and storage of yoghurt. Food Additives and Contaminants 19: 1043–1050. 10.1080/0265203021000007831
Greppi, A., Saubade, F., Botta, C., Humblot, C., Guyot, J.P. and Cocolin, L., 2017. Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiology 62: 169–177. 10.1016/j.fm.2016.09.016
Hassan, H. and Kassaify, Z., 2014. The risks associated with aflatoxin M1 occurrence in Lebanese dairy products. Food Control 37: 68–72. 10.1016/j.foodcont.2013.08.022
Hassan, Z., Al-Thani, R., Atia, F., Almeer, S., Balmas, V., Migheli, Q. and Jaoua, S., 2018. Evidence of low levels of aflatoxin M1 in milk and dairy products marketed in Qatar. Food Control 92: 25–29. 10.1016/j.foodcont.2018.04.038
Iha, M., Barbosa, C., Okada, I. and Trucksess, M., 2011. Occurrence of aflatoxin M1 in dairy products in Brazil. Food Control 22: 1971–1974. 10.1016/j.foodcont.2011.05.013
International Agency for Research on Cancer, 2002. IARC Monographs of the evaluation of carcinogenic risks to humans, vol. 82: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC, Lyon, France, pp. 171-300.
Iqbal, S., Asi, M. and Jinap, S., 2013. Variation of aflatoxin M1 contamination in milk and milk products collected during winter and summer seasons. Food Control 34: 714–718. 10.1016/j.foodcont.2013.06.009
Iqbal, S., Asi, M. and Malik, N., 2017. The seasonal variation of aflatoxin M1 in milk and dairy products and assessment of dietary intake in Punjab, Pakistan. Food Control 79: 292–296. 10.1016/j.foodcont.2017.04.015
Jager, A., Tedesco, M., Souto, P. and Oliveira, C., 2013. Assessment of aflatoxin intake in São Paulo, Brazil. Food Control 33: 87–92. 10.1016/j.foodcont.2013.02.016
Karazhiyan, H., Mehraban Sangatash, M., Karazhyan, R., Mehrzad, A. and Haghighi, E., 2016. Ability of different treatments of Saccharomyces cerevisiae to surface bind aflatoxin M1 in yoghurt. Journal of Agricultural Science and Technology 18: 1489–1498.
Kocasari, F., Tasci, F. and Mor, F., 2012. Survey of aflatoxin M1 in milk and dairy products consumed in Burdur, Turkey. International Journal Dairy Technology 65: 365–371. 10.1111/j.1471-0307.2012.00841.x
Kuharic, Z., Jakopovic, Z., Canak, I., Frece, J., Bosnir, J., Pavlek, Z., Ivesic, M. and Markov, K., 2018. Removing aflatoxin M1 from milk with native lactic acid bacteria, centrifugation, and filtration. Archives of Industrial Hygiene and Toxicology 69: 334–339. 10.2478/aiht-2018-69-3160
Makhdoumi, P., Hossini, H., Mohammadi, R. and Limoee, M., 2021. The prevalence of aflatoxin M1 (AFM1) in conventional and industrial dairy products (yogurt, cheese, kashk and dough) of Iran: a systematic review and meta-analysis. Reviews on Environmental Health 28: 1–11. 10.1515/reveh-2021-0028
Muaz, K., Riaz, M., Rosim, R., Akhtar, S., Corassin, C., Gonçalves, B. and Oliveira, C., 2021. In vitro ability of nonviable cells of lactic acid bacteria strains in combination with sorbitan monostearate to bind to aflatoxin M1 in skimmed milk. LWT-Food Science and Technology 147: 111666. 10.1016/j.lwt.2021.111666
Nilchian, Z. and Rahumi, A., 2012. Aflatoxin M1 in yoghurts, cheese and ice-cream in Shahrekord-Iran. World Applied Science Journal 19: 621–624.
Ondiek, W., Wang, Y., Sun, L., Zhou, L., On, S.L., Zheng, H. and Ravi, G., 2022. Removal of aflatoxin B1 and T-2 toxin by bacteria isolated from commercially available probiotic dairy foods. Food Science and Technology International 28: 15–25. 10.1177/1082013220987916
Paula, B.P., Chávez, D.W.H., Junior, W.J.F.L., Guerra, A.F., Corrêa, M.F.D., Pereira, K.S. and Coelho, M.A.Z., 2019. Growth parameters and survivability of Saccharomyces boulardii for probiotic alcoholic beverages development. Frontiers in Microbiology 10: 1–10. 10.3389/fmicb.2019.02092
Picinin, L., Cerqueira, M., Vargas, E., Lana, Â., Toaldo, I. and Bordignon-Luiz, M., 2013. Influence of climate conditions on aflatoxin M1 contamination in raw milk from Minas Gerais State, Brazil. Food Control 31: 419–424. 10.1016/j.foodcont.2012.10.024
Piotrowska, M., 2021. Microbiological decontamination of mycotoxins: opportunities and limitations. Toxins 13: 1–19. 10.3390/toxins13110819
SAS Institute, 2004. SAS⌧ User’s guide: statistics. SAS Institute Inc., Cary, NC.
Shahbazi, Y., Nikousefat, Z. and Karami, N., 2017. Occurrence, seasonal variation and risk assessment of exposure to aflatoxin M1 in Iranian traditional cheeses. Food Control 79: 356–362. 10.1016/j.foodcont.2017.04.021
Souza, C., Khaneghahi, A. and Oliveira, C., 2020. The occurrence of aflatoxin M1 in industrial and traditional fermented milk: a systematic review study. Italian Journal of Food Science 33: 53–64. 10.15586/ijfs.v33iSP1.1982
Souza, H.F., Carosia, M.J., Pinheiro, C., Carvalho, M.V., Oliveira, C.A.F and Kamimura, E.S., 2021. On probiotic yeasts in food development: Saccharomyces boulardii, a trend. Food Science and Technology Ahead of print: 1–7. 10.1590/fst.92321
Sumon, A., Islam, F., Mohanto, N., Kathak, R., Molla, N., Rana, S., Degen, G. and Ali, N., 2021. The presence of aflatoxin M1 in milk and milk products in Bangladesh. Toxins 13: 440–445. 10.3390/toxins13070440
Van der Hoek, S., Darbani, B., Zugaj, K., Prabhala, B., Biron, M., Randelovic, M., Medina, J., Kell, D. and Borodina, I., 2019. Engineering the yeast Saccharomyces cerevisiae for the production of L-(+)-ergothioneine. Frontiers in Bioengineering and Biotechnology 11: 262. 10.1101/667592
Wochner, K., Becker-Algeri, T., Colla, E., Badiale-Furlong, E. and Drunkler, D., 2018. The action of probiotic microorganisms on chemical contaminants in milk. Critical Review Microbiology 44: 112–123. 10.1080/1040841X.2017.1329275
Womack, E., Sparks, D. and Brown, A., 2016. Aflatoxin M1 in milk and milk products: a short review. World Mycotoxin Journal 9: 305–315. 10.3920/WMJ2014.1867
Assaf, J., Nahle, S., Chokr, A., Louka, N., Atoui, A. and El Khoury, A., 2019. Assorted methods for decontamination of aflatoxin M1 in milk using microbial adsorbents. Toxins 11: 1–23. 10.3390/toxins11060304
ANVISA Agência Nacional de Vigilância Sanitária, 2011. Resolução RDC nº 7, de 18 de fevereiro de 2011. Diário Oficial da União–Seção 1 37: 72–73. Available at: https://bvsms.saude.gov.br/bvs/saudelegis/anvisa/2011/res0007_18_02_2011_rep.html.
Campagnollo, F., Ganev, K., Khaneghah, A., Portela, J., Cruz, A., Granato, D., Corassin, C., Oliveira, C. and Sant’Ana, A.S., 2016. The occurrence and effect of unit operations for dairy products processing on the fate of aflatoxin M1: a review. Food Control 68: 310–329. 10.1016/j.foodcont.2016.04.007
Cano-Sancho, G., Marin, S., Ramos, A., Peris-Vicente, J. and Sanchis, V., 2010. Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Ibero-American Journal of Mycology 27: 130–135. 10.1016/j.riam.2010.05.003
Corassin, C., Bovo, F., Rosim, R. and Oliveira, C., 2013. Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control 31: 80–83. 10.1016/j.foodcont.2012.09.033
Cruz, A., Cavalcanti, R., Gherreiro, L., Sant’ana, A., Nogueira, L., Oliveira, C., Deliza, R., Cunha, R., Faria, J. and Bolini, H., 2013. Developing a prebiotic yogurt: rheological, physico-chemical and microbiological aspects and adequacy of survival analysis methodology. Journal of Food Engineering 114: 323–330. 10.1016/j.jfoodeng.2012.08.018
Ertas, N., Gonulalan, Z., Yildirim, Y. and Karadal, F., 2011. A survey of concentration of aflatoxin M1 in dairy products marketed in Turkey. Food Control 22: 1956–1959. 10.1016/j.foodcont.2011.05.009
Fallah, A., 2010. Aflatoxin M1 contamination in dairy products marketed in Iran during winter and summer. Food Control 21: 1478–1481. 10.1016/j.foodcont.2010.04.017
Franciosi, E., Settanni, L., Cavazza, A. and Poznanski, E., 2009. Biodiversity and technological potential of wild lactic acid bacteria from raw cows’ milk. International Dairy Journal 19: 3–11. 10.1016/j.idairyj.2008.07.008
Gonçalves, B., Corassin, C. and Oliveira, C., 2015. Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advance 10: 752–760. 10.3923/ajava.2015.752.760
Gonçalves, B., Gonçalves, J., Rosim, R., Cappato, L., Cruz, A., Oliveira, C. and Corassin, C., 2017. Effects of different sources of Saccharomyces cerevisiae biomass on milk production, composition, and aflatoxin M1 excretion in milk from dairy cows fed aflatoxin B1. Journal of Dairy Science 100: 5701–5708. 10.3168/jds.2016-12215
Gonçalves, B., Muaz, K., Coppa, C., Rosim, R., Kamimura, E., Oliveira, C. and Corassin, C., 2020. Aflatoxin M1 absorption by non-viable cells of lactic acid bacteria and Saccharomyces cerevisiae strains in Minas Frescal cheese. Food Research International 136: 109604. 10.1016/j.foodres.2020.109604
Gonçalves, B., Uliana, R., Coppa, C., Lee, S., Kamimura, E., Oliveira, C. and Corassin, C., 2021. Aflatoxin M1: biological decontamination methods in milk and cheese. Food Science and Technology 4: 1–8. 10.1590/fst.22920
Govaris, A., Roussi, V., Koidis, P. and Botsoglou, N., 2002. Distribution and stability of aflatoxin M1 during production and storage of yoghurt. Food Additives and Contaminants 19: 1043–1050. 10.1080/0265203021000007831
Greppi, A., Saubade, F., Botta, C., Humblot, C., Guyot, J.P. and Cocolin, L., 2017. Potential probiotic Pichia kudriavzevii strains and their ability to enhance folate content of traditional cereal-based African fermented food. Food Microbiology 62: 169–177. 10.1016/j.fm.2016.09.016
Hassan, H. and Kassaify, Z., 2014. The risks associated with aflatoxin M1 occurrence in Lebanese dairy products. Food Control 37: 68–72. 10.1016/j.foodcont.2013.08.022
Hassan, Z., Al-Thani, R., Atia, F., Almeer, S., Balmas, V., Migheli, Q. and Jaoua, S., 2018. Evidence of low levels of aflatoxin M1 in milk and dairy products marketed in Qatar. Food Control 92: 25–29. 10.1016/j.foodcont.2018.04.038
Iha, M., Barbosa, C., Okada, I. and Trucksess, M., 2011. Occurrence of aflatoxin M1 in dairy products in Brazil. Food Control 22: 1971–1974. 10.1016/j.foodcont.2011.05.013
International Agency for Research on Cancer, 2002. IARC Monographs of the evaluation of carcinogenic risks to humans, vol. 82: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC, Lyon, France, pp. 171-300.
Iqbal, S., Asi, M. and Jinap, S., 2013. Variation of aflatoxin M1 contamination in milk and milk products collected during winter and summer seasons. Food Control 34: 714–718. 10.1016/j.foodcont.2013.06.009
Iqbal, S., Asi, M. and Malik, N., 2017. The seasonal variation of aflatoxin M1 in milk and dairy products and assessment of dietary intake in Punjab, Pakistan. Food Control 79: 292–296. 10.1016/j.foodcont.2017.04.015
Jager, A., Tedesco, M., Souto, P. and Oliveira, C., 2013. Assessment of aflatoxin intake in São Paulo, Brazil. Food Control 33: 87–92. 10.1016/j.foodcont.2013.02.016
Karazhiyan, H., Mehraban Sangatash, M., Karazhyan, R., Mehrzad, A. and Haghighi, E., 2016. Ability of different treatments of Saccharomyces cerevisiae to surface bind aflatoxin M1 in yoghurt. Journal of Agricultural Science and Technology 18: 1489–1498.
Kocasari, F., Tasci, F. and Mor, F., 2012. Survey of aflatoxin M1 in milk and dairy products consumed in Burdur, Turkey. International Journal Dairy Technology 65: 365–371. 10.1111/j.1471-0307.2012.00841.x
Kuharic, Z., Jakopovic, Z., Canak, I., Frece, J., Bosnir, J., Pavlek, Z., Ivesic, M. and Markov, K., 2018. Removing aflatoxin M1 from milk with native lactic acid bacteria, centrifugation, and filtration. Archives of Industrial Hygiene and Toxicology 69: 334–339. 10.2478/aiht-2018-69-3160
Makhdoumi, P., Hossini, H., Mohammadi, R. and Limoee, M., 2021. The prevalence of aflatoxin M1 (AFM1) in conventional and industrial dairy products (yogurt, cheese, kashk and dough) of Iran: a systematic review and meta-analysis. Reviews on Environmental Health 28: 1–11. 10.1515/reveh-2021-0028
Muaz, K., Riaz, M., Rosim, R., Akhtar, S., Corassin, C., Gonçalves, B. and Oliveira, C., 2021. In vitro ability of nonviable cells of lactic acid bacteria strains in combination with sorbitan monostearate to bind to aflatoxin M1 in skimmed milk. LWT-Food Science and Technology 147: 111666. 10.1016/j.lwt.2021.111666
Nilchian, Z. and Rahumi, A., 2012. Aflatoxin M1 in yoghurts, cheese and ice-cream in Shahrekord-Iran. World Applied Science Journal 19: 621–624.
Ondiek, W., Wang, Y., Sun, L., Zhou, L., On, S.L., Zheng, H. and Ravi, G., 2022. Removal of aflatoxin B1 and T-2 toxin by bacteria isolated from commercially available probiotic dairy foods. Food Science and Technology International 28: 15–25. 10.1177/1082013220987916
Paula, B.P., Chávez, D.W.H., Junior, W.J.F.L., Guerra, A.F., Corrêa, M.F.D., Pereira, K.S. and Coelho, M.A.Z., 2019. Growth parameters and survivability of Saccharomyces boulardii for probiotic alcoholic beverages development. Frontiers in Microbiology 10: 1–10. 10.3389/fmicb.2019.02092
Picinin, L., Cerqueira, M., Vargas, E., Lana, Â., Toaldo, I. and Bordignon-Luiz, M., 2013. Influence of climate conditions on aflatoxin M1 contamination in raw milk from Minas Gerais State, Brazil. Food Control 31: 419–424. 10.1016/j.foodcont.2012.10.024
Piotrowska, M., 2021. Microbiological decontamination of mycotoxins: opportunities and limitations. Toxins 13: 1–19. 10.3390/toxins13110819
SAS Institute, 2004. SAS⌧ User’s guide: statistics. SAS Institute Inc., Cary, NC.
Shahbazi, Y., Nikousefat, Z. and Karami, N., 2017. Occurrence, seasonal variation and risk assessment of exposure to aflatoxin M1 in Iranian traditional cheeses. Food Control 79: 356–362. 10.1016/j.foodcont.2017.04.021
Souza, C., Khaneghahi, A. and Oliveira, C., 2020. The occurrence of aflatoxin M1 in industrial and traditional fermented milk: a systematic review study. Italian Journal of Food Science 33: 53–64. 10.15586/ijfs.v33iSP1.1982
Souza, H.F., Carosia, M.J., Pinheiro, C., Carvalho, M.V., Oliveira, C.A.F and Kamimura, E.S., 2021. On probiotic yeasts in food development: Saccharomyces boulardii, a trend. Food Science and Technology Ahead of print: 1–7. 10.1590/fst.92321
Sumon, A., Islam, F., Mohanto, N., Kathak, R., Molla, N., Rana, S., Degen, G. and Ali, N., 2021. The presence of aflatoxin M1 in milk and milk products in Bangladesh. Toxins 13: 440–445. 10.3390/toxins13070440
Van der Hoek, S., Darbani, B., Zugaj, K., Prabhala, B., Biron, M., Randelovic, M., Medina, J., Kell, D. and Borodina, I., 2019. Engineering the yeast Saccharomyces cerevisiae for the production of L-(+)-ergothioneine. Frontiers in Bioengineering and Biotechnology 11: 262. 10.1101/667592
Wochner, K., Becker-Algeri, T., Colla, E., Badiale-Furlong, E. and Drunkler, D., 2018. The action of probiotic microorganisms on chemical contaminants in milk. Critical Review Microbiology 44: 112–123. 10.1080/1040841X.2017.1329275
Womack, E., Sparks, D. and Brown, A., 2016. Aflatoxin M1 in milk and milk products: a short review. World Mycotoxin Journal 9: 305–315. 10.3920/WMJ2014.1867
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Feb 19, 2022
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Pires, R. C., Portinari, M. R. P., Moraes, G. Z., Khaneghah, A. M., Gonçalves, B. L., Rosim, R. E., Oliveira, C. A. F., & Corassin, C. H. (2022). Evaluation of Anti-Aflatoxin M1 effects of heat-killed cells of Saccharomyces cerevisiae in Brazilian commercial yogurts. Quality Assurance and Safety of Crops & Foods, 14(1), 75-81. https://doi.org/10.15586/qas.v14i1.1006
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This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
Pires, R. C., Portinari, M. R. P., Moraes, G. Z., Khaneghah, A. M., Gonçalves, B. L., Rosim, R. E., Oliveira, C. A. F., & Corassin, C. H. (2022). Evaluation of Anti-Aflatoxin M1 effects of heat-killed cells of Saccharomyces cerevisiae in Brazilian commercial yogurts. Quality Assurance and Safety of Crops & Foods, 14(1), 75-81. https://doi.org/10.15586/qas.v14i1.1006