Vol. 23, No. 2 (2024), Poly24224 https://doi.org/10.24275/rmiq/Poly24224


Evaluation of the aflatoxin M1 retention capacity in a polysaccharide obtained by fermenting milk with kefir grains


 

Authors

C. Jiménez-Pérez, L. Roldán-Hernández, A. Cruz-Guerrero, S. Alatorre-Santamaría


Abstract

Currently, it has been reported a high incidence of aflatoxin M1 (AFM1) in milk. This poses a risk to human health, because AFM1 is considered a class 1 carcinogen. Among the various strategies that have been studied to reduce AFM1 contamination in milk, the use of lactic acid bacteria has attracted considerable attention. This approach takes advantage of exopolysaccharides (EPS) present in bacterial cells walls that show affinity to the mycotoxin and can form an EPS-AFM1 complex. In addition, during milk fermentation with kefir grains an EPS called kefiran is produced which has a potential for applications in food industry, e.g., improving the rheological and functional properties of foods. In this study, the capacity of isolated kefiran to retain AFM1 from milk matrix and aqueous system was evaluated. The results demonstrated a decrease in AFM1 content by 81% in milk matrix added with EPS, while in aqueous system in the presence of EPS it was observed a 75% reduction of AFM1 content. This led to the conclusion that kefiran does have mycotoxin retention potential and that in milk, higher retention value of AFM1 could be attributed to the interactions with milk proteins.


Keywords

aflatoxin M1, exopolysaccharides, kefir grains, milk.


References

  • Benkerroum, N. (2020). Aflatoxins: Producing‐molds, structure, health issues and incidence in southeast asian and sub‐saharan african countries. International Journal of Environmental Research and Public Health, 17(4). https://doi.org/10.3390/ijerph17041215
  • Blandón, L., Noseda, M., Islan, G., Castro, G., de Melo Pereira, G., Thomaz-Soccol, V., & Soccol, C. (2018). Optimization of culture conditions for kefiran production in whey: The structural and biocidal properties of the resulting polysaccharide. Bioactive Carbohydrates and Dietary Fibre, 16, 14–21. https://doi.org/10.1016/J.BCDF.2018.02.001
  • Botelho, P., Maciel, M., Bueno, L., Marques, M., Marques, D., & Sarmento S. (2014). Characterisation of a new exopolysaccharide obtained from of fermented kefir grains in soymilk. Carbohydrate Polymers, 107(1), 1–6. https://doi.org/10.1016/J.CARBPOL.2014.02.036
  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254. https://doi.org/doi.org/10.1016/0003-2697(76)90527-3
  • Bryden, W. (2019). Mycotoxins in the food chain and human health implications. In J. Nriagu (Ed.), Encyclopedia of Environmental Health (2nd ed.). Elsevier Inc. https://doi.org/10.1016/B978-0-12-409548-9.11776-2
  • Carrero-Puentes, S., Fuenmayor, C., Jiménez-Pérez, C., Guzmán-Rodríguez, F., Gómez-Ruiz, L., Rodríguez-Serrano, G., Alatorre-Santamaría, S., García-Garibay, M., & Cruz-Guerrero, A. (2022). Development and characterization of an exopolysaccharide ‐ functionalized acid whey cheese (requesón) using Lactobacillus delbrueckii ssp. bulgaricus. Journal of Food Processing and Preservation, 46(6), e16095. https://doi.org/doi.org/10.1111/jfpp.16095
  • Cheirsilp, B., & Radchabut, S. (2011). Use of whey lactose from dairy industry for economical kefiran production by Lactobacillus kefiranofaciens in mixed cultures with yeasts. New Biotechnology, 28(6), 574–580. https://doi.org/10.1016/j.nbt.2011.01.009
  • Contreras-López, E., Jaimez-Ordaz, J., Rodríguez-Serrano, G., Cruz-Guerrero, A., Ramírez-Godínez, J., Castañeda-Ovando, A., & González-Olivares, L. (2021). Contenido exopolysaccharide-producing bacteria improves survival and proteolytic profile of lactobacillus rhamnosus gg added to semi-ripened cheese volumen 8, número 3, 2009 / volume 8, number 3, 2009. Revista Mexicana de Ingeniera Quimica, 20(3). https://doi.org/10.24275/rmiq/Bio2483
  • Dubois, M., Gilles, K., Hamilton, J., Rebers, P., & Smith, F. (1956). Colorimetric Method for Determination of Sugars and Related Substances. Analytical Chemistry, 28(3), 350–356. https://doi.org/10.1021/ac60111a017
  • Elliott, C., Connolly, L., & Kolawole, O. (2020). Potential adverse effects on animal health and performance caused by the addition of mineral adsorbents to feeds to reduce mycotoxin exposure. Mycotoxin Research, 36(1), 115–126. https://doi.org/10.1007/s12550-019-00375-7
  • Exarhopoulos, S., Raphaelides, S., & Kontominas, M. (2018). Conformational studies and molecular characterization of the polysaccharide kefiran. Food Hydrocolloids, 77, 347–356. https://doi.org/10.1016/j.foodhyd.2017.10.011
  • Gagliarini, N., Diosma, G., Garrote, G., Abraham, A., & Piermaria, J. (2019). Whey protein-kefiran films as driver of probiotics to the gut. Lwt, 105(August 2018), 321–328. https://doi.org/10.1016/j.lwt.2019.02.023
  • Gagliarini, N., Figoli, C., Piermaria, J., Bosch, A., & Abraham, A. (2022). Unraveling molecular interactions in whey protein-kefiran composite films to understand their physicochemical and mechanical properties: Understanding whey protein-kefiran molecular interaction in composite film. Food Bioscience, 50(PA), 102012. https://doi.org/10.1016/j.fbio.2022.102012
  • Gentry, B., Cazón, P., & O’Brien, K. (2023). A comprehensive review of the production, beneficial properties, and applications of kefiran, the kefir grain exopolysaccharide. International Dairy Journal, 144. https://doi.org/10.1016/j.idairyj.2023.105691
  • Harshitha, C., Sharma, N., Singh, R., Sharma, R., Gandhi, K., & Mann, B. (2023). Interaction study of aflatoxin M1 with milk proteins using ATR-FTIR. Journal of Food Science and Technology, 60(1), 64–72. https://doi.org/10.1007/s13197-022-05587-x
  • Hernández-Rosas, F., Castilla-Marroquín, J., Loeza-Corte, J., Lizardi-Jiménez, M., & Hernández-Martínez, R. (2021). The importance of carbon and nitrogen sources on exopolysaccharide synthesis by lactic acid bacteria and their industrial importance. Revista Mexicana de Ingeniera Quimica, 20(3), 1–21. https://doi.org/10.24275/RMIQ/BIO2429
  • International Agency for Research on Cancer, (IARC). (2012). Aflatoxins. In IARC monographs on the evaluation of carcinogenic risks to humans, 100F (pp. 225–248).
  • Jimenez-Fernandez, M., Perez-Tirado, D., Peredo-Lovillo, A., & Luna-Solano, G. (2021). Physicochemical characteristics and survivability of lactobacillus paracasei encapsulated by a gum arabic-pectin mixture as wall material and added to fresh panela cheese. Revista Mexicana de Ingeniera Quimica, 20(3). https://doi.org/10.24275/rmiq/Alim2551
  • Jiménez-Pérez, C., Alatorre-Santamaría, S., Tello-Solís, S. R., Gómez-Ruiz, L., Rodríguez-Serrano, G., García- Garibay, M., & Cruz-Guerrero, A. (2021). Analysis of aflatoxin m1 contamination in milk and cheese produced in mexico: A review. World Mycotoxin Journal, 14(3), 269–285. https://doi.org/10.3920/WMJ2020.2668
  • Jiménez-Pérez, C., Tello-Solís, S. R., Gómez-Castro, C. Z., Alatorre-Santamaría, S., Gómez-Ruiz, L., Rodríguez-Serrano, G., Cruz-Borbolla, J., García-Garibay, M., & Cruz-Guerrero, A. (2020). Spectroscopic studies and molecular modelling of the aflatoxin M1-bovine α-lactalbumin complex formation. Journal of Photochemistry and Photobiology B: Biology, 209, 111957. https://doi.org/10.1016/j.jphotobiol.2020.111957
  • la Riviére, J., Kooiman, P., & Schmidt, K. (1967). Kefiran, a novel polysaccharide produced in the kefir grain by Lactobacillus brevis. Archiv Für Mikrobiologie, 59(1–3), 269–278. https://doi.org/10.1007/BF00406340/METRICS
  • Maeda, H., Zhu, X., Omura, K., Suzuki, S., & Kitamura, S. (2004). Effects of an exopolysaccharide (kefiran) on lipids, blood pressure, blood glucose, and constipation. BioFactors, 22(1–4), 197–200. https://doi.org/10.1002/BIOF.5520220141
  • Marshall, V., & Cole, W. (1985). Methods for making kefir and fermented milks based on kefir. Journal of Dairy Research, 52(3), 451–456. https://doi.org/10.1017/S0022029900024353
  • Micheli, L., Uccelletti, D., Palleschi, C., & Crescenzi, V. (1999). Isolation and characterisation of a ropy Lactobacillus strain producing the exopolysaccharide kefiran. Applied Microbiology and Biotechnology, 53(1), 69–74. https://doi.org/10.1007/S002530051616/METRICS
  • Moradi, Z., & Kalanpour, N. (2019). Kefiran, a branched polysaccharide: Preparation, properties and applications: A review. Carbohydrate Polymers, 223, 115100. https://doi.org/10.1016/J.CARBPOL.2019.115100
  • Muaz, K., Riaz, M., Oliveira, C., Akhtar, S., Ali, S., Nadeem, H., Park, S., & Balasubramanian, B. (2022). Aflatoxin M1 in milk and dairy products: global occurrence and potential decontamination strategies. Toxin Reviews, 41(2), 588–605. https://doi.org/10.1080/15569543.2021.1873387
  • Pankaj, S., Shi, H., & Keener, K. (2018). A review of novel physical and chemical decontamination technologies for aflatoxin in food. Trends in Food Science and Technology, 71(January 2017), 73–83. https://doi.org/10.1016/j.tifs.2017.11.007
  • Piermaria, J., de la Canal, M., & Abraham, A. (2008). Gelling properties of kefiran, a food-grade polysaccharide obtained from kefir grain. Food Hydrocolloids, 22(8), 1520–1527. https://doi.org/10.1016/J.FOODHYD.2007.10.005
  • Piermaria, J., López-Castejón, M., Bengoechea, C., Guerrero, A., & Abraham, A. (2021). Prebiotic emulsions stabilised by whey protein and kefiran. International Journal of Food Science and Technology, 56(1), 76–85. https://doi.org/10.1111/ijfs.14601
  • Rimada, P., & Abraham, A. (2003). Comparative study of different methodologies to determine the exopolysaccharide produced by kefir grains in milk and whey. Lait, 83, 79–87. https://doi.org/DOI: 10.1051/lait:2002051
  • Sabaghi, M., Maghsoudlou, Y., & Habibi, P. (2015). Enhancing structural properties and antioxidant activity of kefiran films by chitosan addition. Food Structure, 5, 66–71. https://doi.org/10.1016/j.foostr.2015.06.003
  • Salari, N., Kazeminia, M., Vaisi-Raygani, A., Jalali, R., & Mohammadi, M. (2020). Aflatoxin M1 in milk worldwide from 1988 to 2020: A systematic review and meta-analysis. Journal of Food Quality, 2020. https://doi.org/10.1155/2020/8862738
  • Taniguchi, M., Nomura, M., Itaya, T., & Tanaka, T. (2001). Kefiran production by Lactobacillus kefiranofaciens under the culture conditions established by mimicking the existence and activities of yeast in kefir grains. Food Science and Technology Research, 7(4), 333–337. https://doi.org/10.3136/fstr.7.333
  • Vila-Donat, P., Marín, S., Sanchis, V., & Ramos, A. (2018). A review of the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal feed decontamination. Food and Chemical Toxicology, 114, 246–259. https://doi.org/10.1016/j.fct.2018.02.044
  • Zannini, E., Waters, D., Coffey, A., & Arendt, E. (2016). Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Applied Microbiology and Biotechnology, 100(3), 1121–1135. https://doi.org/10.1007/s00253-015-7172-2