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Aflatoxin M1: biological decontamination methods in milk and cheese

Abstract

Dairy cattle when fed on aflatoxin B1 may excrete aflatoxin M1 in milk as a consequence of dietary exposure. Once AFM1 is excreted in milk, it is present in dairy products such as cheese, yogurt, among others. This mycotoxin is quite resistant to temperature therefore heat treatments like pasteurization and ultra-pasteurization are not enough to inactivate it. In this context, this article provides an overview of the biological decontamination methods on milk and cheese of the last decade, as a contribution to evaluate the evolution of this strategy as well as its efficiency according to their authors. Relevant studies published between January 2009 and May 2019 were selected after a systematic search of the literature in PubMed, Science direct and Google Scholar databases. According with our research in the last decade few studies have been published on these methods and unfortunately none of the published studies tested such methods in cheese. Throughout the research many studies on decontamination methods were found, however, in phosphate buffered saline solution or in culture medium. Further studies on biological decontamination on milk and mainly on cheese are necessary for this technique to be better developed and applied to a large scale in the industries.

Keywords:
Aflatoxin; biological decontamination; cheese; milk; systematic review

1 Introduction

Aflatoxins are the most widely known and distributed mycotoxins in foods and feeds (Wochner et al., 2018Wochner, K. F., Becker-algeri, T. A., Colla, E., Badiale-Furlong, E., & Drunkler, D. A. (2018). The action of probiotic microorganisms on chemical contaminants in milk. Critical Reviews in Microbiology, 44(1), 112-123. http://dx.doi.org/10.1080/1040841X.2017.1329275. PMid:28537817.
http://dx.doi.org/10.1080/1040841X.2017....
). Aflatoxins, mainly aflatoxin B1 (AFB1) are potent carcinogenic, teratogenic and mutagenic agents. When lactating animals are fed with feed containing aflatoxins (mainly AFB1), these are biotransformed resulting in a new compound denominated aflatoxin M1 (AFM1), which is soluble and excreted in the milk of these animals (Fink-Gremmels, 2008Fink-Gremmels, J. (2008). The role of mycotoxins in the health and performance of dairy cows. Veterinary journal (London, England : 1997), 176(1), 84-92. http://dx.doi.org/10.1016/j.tvjl.2007.12.034. PMid:18342554.
http://dx.doi.org/10.1016/j.tvjl.2007.12...
; Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
). According to the World Health Organization and the International Agency for Research on Cancer both AFB1 and AFM1 are classified as belonging to group 1, carcinogenic to humans (World Health Organization, 2002World Health Organization – WHO, & International Agency for Research on Cancer – IARC. (2002). IARC monographs on the evaluation of carcinogenic risks to humans. Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. Paris: WIARC Press. Retrieved from: https://monographs.iarc.fr/wp-content/uploads/2018/06/mono82.pdf
https://monographs.iarc.fr/wp-content/up...
).

Several studies have demonstrated evidence of human exposure to aflatoxin M1 due to the consumption of contaminated milk and dairy products (Bovo et al., 2013Bovo, F., Corassin, C. H., Rosim, R. E., & de Oliveira, C. A. F. (2013). Efficiency of Lactic Acid Bacteria Strains for Decontamination of Aflatoxin M1 in Phosphate Buffer Saline Solution and in Skimmed Milk. Food and Bioprocess Technology, 6(8), 2230-2234. http://dx.doi.org/10.1007/s11947-011-0770-9.
http://dx.doi.org/10.1007/s11947-011-077...
; Campagnollo et al., 2016Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
; Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Fernandes et al., 2012Fernandes, A. M., Corrêa, B., Rosim, R. E., Kobashigawa, E., & Oliveira, C. A. F. (2012). Distribution and stability of aflatoxin M1 during processing and storage of Minas Frescal cheese. Food Control, 24(1-2), 104-108. http://dx.doi.org/10.1016/j.foodcont.2011.09.010.
http://dx.doi.org/10.1016/j.foodcont.201...
; Shundo et al., 2009Shundo, L., Navas, S. A., Lamardo, L. C. A., Ruvieri, V., & Sabino, M. (2009). Estimate of aflatoxin M1 exposure in milk and occurrence in Brazil. Food Control, 20(7), 655-657. http://dx.doi.org/10.1016/j.foodcont.2008.09.019.
http://dx.doi.org/10.1016/j.foodcont.200...
; Trombete et al., 2013Trombete, F. M., Fraga, M. E., & Saldanha, T. (2013). Contaminação de queijos por Aflatoxina M1: uma abordagem sobre a ocorrência e prevenção. Revista do Instituto de Latícinios Cândido Tostes, 68(392), 40-48. http://dx.doi.org/10.5935/2238-6416.20130027.
http://dx.doi.org/10.5935/2238-6416.2013...
; Womack et al., 2016Womack, E. D., Sparks, D. L., & Brown, A. E. (2016). Aflatoxin M1 in milk and milk products: a short review. World Mycotoxin Journal, 9(2), 305-315. http://dx.doi.org/10.3920/WMJ2014.1867.
http://dx.doi.org/10.3920/WMJ2014.1867...
).

Once in the milk, AFM1 is not degraded and can resist different industrial treatments including milk sterilization or to any other heat treatment (Campagnollo et al., 2016Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
; Assaf et al., 2019Assaf, J. C., Khoury, A. E., Chokr, A., Louka, N., & Atoui, A. (2019). A novel method for elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG biofilm. International Journal of Dairy Technology, 72(2), 1-9. http://dx.doi.org/10.1111/1471-0307.12578.
http://dx.doi.org/10.1111/1471-0307.1257...
). Milk and dairy products are frequently consumed by a portion of the population considered vulnerable, such as children and the elderly (Fallah et al., 2009Fallah, A. A., Jafari, T., Fallah, A., & Rahnama, M. (2009). Determination of aflatoxin M1 levels in Iranian white and cream cheese. Food and Chemical Toxicology, 47(8), 1872-1875. http://dx.doi.org/10.1016/j.fct.2009.04.042. PMid:19426778.
http://dx.doi.org/10.1016/j.fct.2009.04....
; Prandini et al., 2009Prandini, A., Tansini, G., Sigolo, S., Filippi, L., Laporta, M., & Piva, G. (2009). On the occurrence of aflatoxin M1 in milk and dairy products. Food and Chemical Toxicology, 47(5), 984-991. http://dx.doi.org/10.1016/j.fct.2007.10.005. PMid:18037552.
http://dx.doi.org/10.1016/j.fct.2007.10....
). For the reasons mentioned above, AFM1 contamination is a serious health problem.

Knowledge about the negative impacts of aflatoxins on the economy and health led to investigations for strategies to prevent their formation in food, as well as to eliminate, inactivate or reduce the bioavailability of these toxins in contaminated products (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Gonçalves et al., 2015aGonçalves, B. L., Rosim, R. E., Oliveira, C. A. F., & Corassin, C. H. (2015a). The in vitro ability of different Saccharomyces cerevisiae - based products to bind Aflatoxin B1. Food Control, 47, 298-300. http://dx.doi.org/10.1016/j.foodcont.2014.07.024.
http://dx.doi.org/10.1016/j.foodcont.201...
). Improvements in agricultural practices, antifungal agents and genetic engineering may be used as a means of prevention (González et al., 2005González, E., Felicio, M., Rossi, M. H., Nogueita, J. H., & Manginelli, S. (2005). Ocorrência de aflatoxina M1 em leite comercializado em alguns municípios do estado de são paulo. Arquivos do Instituto Biológico, 72(4), 435-438. http://dx.doi.org/10.5433/1679-0359.2014v35n1p371.
http://dx.doi.org/10.5433/1679-0359.2014...
). Aflatoxin elimination or inactivation may be achieved by physical, chemical and biological methods (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
).

Physical and chemical methods are not the most appropriate in terms of safety, economy and product quality, either because they are not efficient at removing contaminants, or high costs and nutritional and sensory damage to the product (Stoev, 2013Stoev, S. D. (2013). Food safety and increasing hazard of mycotoxin occurrence in foods and feeds. Critical Reviews in Food Science and Nutrition, 53(9), 887-901. http://dx.doi.org/10.1080/10408398.2011.571800. PMid:23768181.
http://dx.doi.org/10.1080/10408398.2011....
; Wochner et al., 2018Wochner, K. F., Becker-algeri, T. A., Colla, E., Badiale-Furlong, E., & Drunkler, D. A. (2018). The action of probiotic microorganisms on chemical contaminants in milk. Critical Reviews in Microbiology, 44(1), 112-123. http://dx.doi.org/10.1080/1040841X.2017.1329275. PMid:28537817.
http://dx.doi.org/10.1080/1040841X.2017....
). Thus, the biological methods emerged and gained popularity due to its friendliness to both environment and body health (Peng et al., 2018Peng, Z., Chen, L., Zhu, Y., Huang, Y., Hu, X., Wu, Q., Nussler, A. K., Liu, L., & Yang, W. (2018). Current major degradation methods for aflatoxins: a review. Trends in Food Science & Technology, 80, 155-166. http://dx.doi.org/10.1016/j.tifs.2018.08.009.
http://dx.doi.org/10.1016/j.tifs.2018.08...
).

In this context the aim of this study was to review the biological methods of aflatoxin M1 decontamination in milk and cheese published in the last decade as a contribution to evaluate the evolution of this strategy as well as its efficiency according to its authors.

2 Search strategy

The bibliographic research, inclusion and exclusion criteria and data collection were performed based on the protocol Cochrane (Higgins, 2011Higgins, J. P. (2011). Cochrane handbook for conducting systematic reviews. Londres: The Cochrane Collaboration. Retrieved from: http://handbook.cochrane.org/
http://handbook.cochrane.org/...
). Relevant studies published between January 2009 to May 2019 were selected after a systematic search in the following databases PubMed, Science Direct and Google Scholar databases, using key words like: “Aflatoxin M1, probiotics and lactic acid bacteria binding OR “Aflatoxin M1 in milk”, probiotics and lactic acid bacteria binding OR “biological degradation”, aflatoxin M1 in dairy products OR “biological binding”, aflatoxin M1 in milk.

2.1 Inclusion and exclusion criteria

During first screening, the full texts of potentially eligible articles were downloaded. Then, the citations transferred were examined twice for inclusion and final eligibility criteria. The inclusion criteria were: (1) Cross-sectional descriptive data, (2) Full-text article available (3) Original research studies, (4) Decontamination method used and (5) Type of product examined (milk or cheese). In addition, in order to avoid any error in the translation process and also the clarity of data expression, based on previously published meta-analysis studies in Food Science (Cherkani-Hassani et al., 2016Cherkani-Hassani, A., Mojemmi, B., & Mouane, N. (2016). Occurrence and levels of mycotoxins and their metabolites in human breast milk associated to dietary habits and other factors : A systematic literature review, 1984 e 2015. Trends in Food Science & Technology, 50, 56-69. http://dx.doi.org/10.1016/j.tifs.2016.01.024.
http://dx.doi.org/10.1016/j.tifs.2016.01...
; Khaneghah et al., 2018Khaneghah, A. M., Fakhri, Y., Raeisi, S., Armoon, B., & Sant, A. S. (2018). Prevalence and concentration of ochratoxin A, zearalenone, deoxynivalenol and total aflatoxin in cereal-based products : a systematic review and meta- analysis. Food and Chemical Toxicology, 118, 830-848. http://dx.doi.org/10.1016/j.fct.2018.06.037. PMid:29935247.
http://dx.doi.org/10.1016/j.fct.2018.06....
), only articles published in English were included. Citations that did not meet these criteria were excluded.

2.2 Data collection

After screening, 405 articles were retrieved and evaluated for eligibility. 394 articles were excluded in the initial evaluation due to duplicates or based on their title and abstract content. Finally, 11 articles met the inclusion criteria and were included in the review.

3 Aflatoxin M1, milk, cheese and decontamination methods

3.1 Aflatoxin M1 synthesis and excretion

One of the most widely known and largely distributed mycotoxin groups in food, with proven toxic properties are aflatoxins (Campagnollo et al., 2016Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
; Varga et al., 2015Varga, E., Wiesenberger, G., Hametner, C., Ward, T. J., Dong, Y., Schöfbeck, D., McCormick, S., Broz, K., Stuckler, R., Schuhmacher, R., Krska, R., Kistler, H. C., Berthiller, F., & Adam, G. (2015). New tricks of an old enemy: Isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environmental Microbiology, 17(8), 2588-2600. http://dx.doi.org/10.1111/1462-2920.12718. PMid:25403493.
http://dx.doi.org/10.1111/1462-2920.1271...
) can be produced by approximately twenty species of three different species of the genus Aspergillus, being Aspergillus flavus the main aflatoxins producer (Elsanhoty et al., 2014Elsanhoty, R. M., Salam, S. A., Ramadan, M. F., & Badr, F. H. (2014). Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control, 43, 129-134. http://dx.doi.org/10.1016/j.foodcont.2014.03.002.
http://dx.doi.org/10.1016/j.foodcont.201...
).

The occurrence of aflatoxins in food is unavoidable and influenced by environmental factors. The extent of its contamination is not predictable and may vary with agronomic practices and product susceptibility to fungus invasion during the pre-harvest, storage and processing stages (Araújo, 2012Araújo, A. J. M. (2012). Aflatoxinas. In A. J. M. Araújo. Química de alimentos: teoria e prática (5. ed., pp. 340–352). Viçosa: Universidade Federal de Viçosa.). Aspergillus spp. grows on a wide variety of substrates, and most food and feed are susceptible to invasion by aflatoxigenic strains at any stage of production, processing or storage (Oliveira & Corassin, 2014Oliveira, C. A. F., & Corassin, C. H. (2014). Aflatoxins. In S.C. Duarte, A. L. S. Pena & C.M. Lino (Eds.), Mycotoxins and their implications in food safety (pp. 113). London: Future Science Ltd. http://dx.doi.org/10.4155/ebo.13.468.
http://dx.doi.org/10.4155/ebo.13.468...
). In this context, aflatoxins can be found as natural contaminants in cereals, cereal by-products, oilseeds, cassava, and a whole set of foods for humans such as dried fruit, spices, oilseeds, milk and dairy products (Bhat et al., 2010Bhat, R., Rai, R. V., & Karim, A. A. (2010). Mycotoxins in food and feed : present status and future concerns. Comprehensive Reviews in Food Science and Food Safety, 9(1), 57-81. http://dx.doi.org/10.1111/j.1541-4337.2009.00094.x.
http://dx.doi.org/10.1111/j.1541-4337.20...
; Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
).

Aflatoxins are present throughout the world, but mainly in tropical climate areas. Their appearance in agricultural products occurs in hot and humid weather conditions, and in poor or inadequate storage facilities. The most influential factors on the growth and production of aflatoxins are air humidity and temperature, being optimum humidity above 80% and the maximum toxin production temperature between 25 and 27 °C (Abbas, 2005Abbas, H. K. (2005). Aflatoxin and food safety. Boca Raton: CRC Press. http://dx.doi.org/10.1201/9781420028171.
http://dx.doi.org/10.1201/9781420028171...
; Spinosa et al., 2008Spinosa, H. S., Górniak, S. L., & Palermo-Neto, J. (2008). Toxicologia aplicada à medicina veterinária. Barueri: Manole.). Aflatoxin production can be influenced by some other factors such as: substrate composition, pH, oxygen and carbon dioxide content, microbial competition, mechanical damage, contaminant fungus lineage, plant stress and use of fungicides (Hussein & Brasel, 2001Hussein, H. S., & Brasel, J. M. (2001). Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology, 167(2), 101-134. http://dx.doi.org/10.1016/S0300-483X(01)00471-1. PMid:11567776.
http://dx.doi.org/10.1016/S0300-483X(01)...
; Magan & Olsen, 2006Magan, N., & Olsen, M. (2006). Mycotoxins in food: detection and control. Boca Raton: CRC Press.).

Nutrition is one of the most important factors in dairy production, representing the main cost in this activity. Nutrient requirements of dairy cows vary according to the stage of pregnancy and lactation. The nutrients required by dairy cows are energy, fiber, protein, water, vitamins and minerals. Pasture provides a balanced source of feed, however is not enough to maintain high-producing dairy cows. Energy is the decisive factor in milk production: it determines milk yield and composition, as well as body weight. The main energy sources in dairy cow feed are carbohydrates and fiber (corn silage, ground corn, whole cottonseed, high moisture shelled corn, corn gluten meal, soybean hulls and meal). Protein and fats in feeds can also be used as energy sources (Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
).

Dairy cattle feed may be naturally and simultaneously contaminated by several fungi that are able to produce different toxins. According to Alonso et al. (2013)Alonso, V. A., Pereyra, C. M., Keller, L. A. M., Dalcero, A. M., Rosa, C. A. R., Chiacchiera, S. M., & Cavaglieri, L. R. (2013). Fungi and mycotoxins in silage: an overview. Journal of Applied Microbiology, 115(3), 637-643. http://dx.doi.org/10.1111/jam.12178. PMid:23445404.
http://dx.doi.org/10.1111/jam.12178...
most of the silage is made up from annual crops. Therefore, mycotoxin concentration in the feed may vary annually. Several species in the genera Aspergillus, Penicillium, Alternaria, Trichoderma, Claviceps and others make up the storage microbiota and are responsible for the production of mycotoxins found in grains and forage (Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
).

Dairy cattle are highly exposed to the action of mycotoxins due to their dependence on stored and bulky concentrates such as hay or silage (Jobim et al., 2001Jobim, C. C., Gonçalves, G. D., & Santos, G. T. (2001). Qualidade sanitária de grãos e de forragens conservadas versus desempenho animal e qualidade de seus produtos. In Simpósio sobre produção e utilização de forragens conservadas (pp. 242–261). Maringá: UEM.). Ruminants are less susceptible to the effects of mycotoxins because the rumen to be populated by microorganisms (fungi, bacteria, protozoa, archaea). Among these, protozoans are the major microorganisms responsible for mycotoxin detoxification (Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
). This process, however, is not always efficient and some toxic metabolites can be excreted in the milk (European Food Safety Auhority, 2004European Food Safety Auhority – EFSA. (2004). Opinion of the Scientific Panel on Contaminants in the Food Chain on request grom the Commission related to Aflatoxin B1 as undesirable substance in animal feed. The EFSA Journal, 39, 1-27. Retrieved from: https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2004.39
https://efsa.onlinelibrary.wiley.com/doi...
; Jouany & Diaz, 2005Jouany, J. P., & Diaz, D. E. (2005). Effects of mycotoxins in ruminants. In D. E. Diaz (Ed.). The mycotoxins blue book (pp. 295–321). Nottingham: University Press.).

When dairy cattle ingest feed containing aflatoxin (mainly AFB1), part of it is degraded by rumen microorganisms, resulting in the metabolite aflatoxicol (Kuilman et al., 1998Kuilman, E. M., Maas, R. F. M., Judah, D. J., & Fink-gremmels, J. (1998). Bovine hepatic metabolism of Aflatoxin B1. Journal of Agricultural and Food Chemistry, 8561(7), 2707-2713. http://dx.doi.org/10.1021/jf980062x.
http://dx.doi.org/10.1021/jf980062x...
). The remaining non-degraded fraction is absorbed by passive diffusion (Fink-Gremmels, 2008Fink-Gremmels, J. (2008). The role of mycotoxins in the health and performance of dairy cows. Veterinary journal (London, England : 1997), 176(1), 84-92. http://dx.doi.org/10.1016/j.tvjl.2007.12.034. PMid:18342554.
http://dx.doi.org/10.1016/j.tvjl.2007.12...
) and metabolized in the liver where the biotransformation to AFM1 occurs being excreted in milk and urine (Murphy et al., 2006Murphy, P., Hendrich, S., Landgren, C., & Bryant, C. (2006). Food mycotoxins : an update. Journal of Food Science, 71(5), R51-R65. http://dx.doi.org/10.1111/j.1750-3841.2006.00052.x.
http://dx.doi.org/10.1111/j.1750-3841.20...
; Oatley et al., 2000Oatley, J. T., Rarick, M. D., Ji, G. E. O. G., & Linz, J. E. (2000). Binding of Aflatoxin B1 to Bifidobacteria in vitro. Journal of Food Protection, 63(8), 1133-1136. http://dx.doi.org/10.4315/0362-028X-63.8.1133. PMid:10945592.
http://dx.doi.org/10.4315/0362-028X-63.8...
).

3.2 Prevalence of aflatoxin M1 in milk and cheese

Milk is the product of complete and uninterrupted milking under healthy conditions of healthy, well fed and rested cows. It is the first food consumed by man and one of the most complete. Milk has essential elements, micronutrients, amino acids and fatty acids in larger portions than in any other product. In addition, it contains high quality proteins, high percentage of calcium and some bioactive substances like enzymes, hormones and cytokines (Food and Agriculture Organization, 2019Food and Agriculture Organization – FAO. (2019). Milk. Rome: FAO. Retrieved from: http://www.fao.org/dairy-production-products/processing/en/
http://www.fao.org/dairy-production-prod...
).

Cheese is one of the oldest foods recorded in the entire history of humanity. The Egyptians are among the first people to domesticate goats and sheep, being also one of the first to use milk and cheese as a source of food (Cruz et al., 2017Cruz, A., Oliveira, C. A. F., Corassin, C., & Sá, P. (2017). Processamento de produtos lácteos: queijos, leites fermentados, bebidas lácteas, sorvete, manteiga, creme de leite, doce de leite, soro em pó e lácteos funcionais (Coleção Lácteos, Vol. 3). Rio de Janeiro: Elsevier.). The primitive cheese was only coagulated milk, devoid of whey and salty. In the nineteenth century the great boom occurred in the consumption of cheese, after all, its production switched from handmade industrial scale, and the process of pasteurization is fundamental for this shift (Chalita et al., 2009Chalita, M. A. N., Silva, R. O. P., Petti, R. H. V., & Silva, C. R. L. (2009). Algumas considerações sobre a fragilidade das concepções de qualidades no mercado de queijos no Brasil. Informações Econômicas, 39(6), 78-88.). Throughout the ages, cheese has evolved to what is known today and the great typological variation of cheeses is related to the adaptation of this product to the different tastes and cultural customs (Instituto Estadual do Patrimônio Histórico e Artístico de Minas Gerais, 2012Instituto Estadual do Patrimônio Histórico e Artístico de Minas Gerais – IEPHA. (2012). História do queijo. Belo Horizonte: IEPHA. Retrieved from: http://www.iepha.mg.gov.br
http://www.iepha.mg.gov.br...
).

The occurrence of aflatoxin M1 in cheese produced from milk contaminated with these toxin is a reality already described by several authors (Armorini et al., 2016Armorini, S., Altafini, A., Zaghini, A., & Roncada, P. (2016). Occurrence of aflatoxin M1 in conventional and organic milk offered for sale in Italy. Mycotoxin Research, 32(4), 237-246. http://dx.doi.org/10.1007/s12550-016-0256-8. PMid:27632224.
http://dx.doi.org/10.1007/s12550-016-025...
; Campagnollo et al., 2016Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
; Fernandes et al., 2012Fernandes, A. M., Corrêa, B., Rosim, R. E., Kobashigawa, E., & Oliveira, C. A. F. (2012). Distribution and stability of aflatoxin M1 during processing and storage of Minas Frescal cheese. Food Control, 24(1-2), 104-108. http://dx.doi.org/10.1016/j.foodcont.2011.09.010.
http://dx.doi.org/10.1016/j.foodcont.201...
; Hassan et al., 2018Hassan, Z., Al-Thani, R., Atia, F., Almeer, S., Balmas, V., Migheli, Q., & Jaoua, S. (2018). Evidence of low levels of aflatoxin M1 in milk and dairy products marketed in Qatar. Food Control, 92, 25-29. http://dx.doi.org/10.1016/j.foodcont.2018.04.038.
http://dx.doi.org/10.1016/j.foodcont.201...
; Iha et al., 2011Iha, M. H., Barbosa, C. B., Okada, I. A., & Trucksess, M. W. (2011). Occurrence of aflatoxin M1 in dairy products in Brazil. Food Control, 22(12), 1971-1974. http://dx.doi.org/10.1016/j.foodcont.2011.05.013.
http://dx.doi.org/10.1016/j.foodcont.201...
; Kav et al., 2011Kav, K., Col, R., & Kaan Tekinsen, K. (2011). Detection of aflatoxin M1 levels by ELISA in white-brined Urfa cheese consumed in Turkey. Food Control, 22(12), 1883-1886. http://dx.doi.org/10.1016/j.foodcont.2011.04.030.
http://dx.doi.org/10.1016/j.foodcont.201...
; Koluacik et al., 2015Koluacik, A., Sivri, G. T., & Kaptan, B. (2015). Aflatoxin M1 determination in Traditional Küp Cheese Samples of Turkey using immunoaffinity column and high-performance liquid chromatography. Turkish Journal of Agriculture - Food Science and Technology, 3(12), 916-919. http://dx.doi.org/10.24925/turjaf.v3i12.916-919.504.
http://dx.doi.org/10.24925/turjaf.v3i12....
; Manetta et al., 2009Manetta, A. C., Giammarco, M., Giuseppe, L. D., Fusaro, I., Gramenzi, A., Formigoni, A., Vignola, G., & Lambertini, L. (2009). Distribution of aflatoxin M1 during Grana Padano cheese production from naturally contaminated milk. Food Chemistry, 113(2), 595-599. http://dx.doi.org/10.1016/j.foodchem.2008.07.091.
http://dx.doi.org/10.1016/j.foodchem.200...
; Shahbazi et al., 2017Shahbazi, Y., Nikousefat, Z., & Karami, N. (2017). Occurrence, seasonal variation and risk assessment of exposure to aflatoxin M1 in Iranian traditional cheeses. Food Control, 79, 356-362. http://dx.doi.org/10.1016/j.foodcont.2017.04.021.
http://dx.doi.org/10.1016/j.foodcont.201...
; Xiong et al., 2018Xiong, J., Xiong, L., Zhou, H., Liu, Y., & Wu, L. (2018). Occurrence of aflatoxin B1 in dairy cow feedstuff and aflatoxin M1 in UHT and pasteurized milk in central China. Food Control, 92, 386-390. http://dx.doi.org/10.1016/j.foodcont.2018.05.022.
http://dx.doi.org/10.1016/j.foodcont.201...
; Yilmaz & Altinci, 2019Yilmaz, S. Ö., & Altinci, A. (2019). Incidence of aflatoxin M1 contamination in milk, white cheese, kashar and butter from Sakarya, Turkey. Food Science and Technology, 39(suppl 1), 190-194. http://dx.doi.org/10.1590/fst.40817.
http://dx.doi.org/10.1590/fst.40817...
; Yoon et al., 2016Yoon, B. R., Hong, S.-Y., Cho, S. M., Lee, K. R., Kim, M., & Chung, S. H. (2016). Aflatoxin M1 levels in dairy products from South Korea determined by high performance liquid chromatography with fluorescence detection. Journal of Food and Nutrition Research, 55(2), 171-180.; Zheng et al., 2017Zheng, N., Li, S. L., Zhang, H., Min, L., Gao, Y. N., & Wang, J. Q. (2017). A survey of aflatoxin M1 of raw cow milk in China during the four seasons from 2013 to 2015. Food Control, 78, 176-182. http://dx.doi.org/10.1016/j.foodcont.2017.02.055.
http://dx.doi.org/10.1016/j.foodcont.201...
). In relation to the presence of AFM1 in cheeses others factors, further to the presence of toxin in milk should be considered, as: kind of cheese, processing steps, kind of milk used to produce (raw or pasteurized), if there is period of maturation, addition of herbs among others (Campagnollo et al., 2016Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
).

Concerns with the negative impacts of aflatoxins on health and economics has led to the investigation of strategies to prevent their formation in food (mainly feed), as well as to eliminate, inactivate or reduce the availability of these mycotoxins in contaminated products (Bovo et al., 2010Bovo, F., Corassin, C. H., & Oliveira, C. A. F. (2010). Descontaminação de aflatoxinas em alimentos por bactérias ácido-láticas. Journal of Health Science, 12(2), 15-21. http://dx.doi.org/10.17921/2447-8938.
http://dx.doi.org/10.17921/2447-8938...
; Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Gonçalves et al., 2015aGonçalves, B. L., Rosim, R. E., Oliveira, C. A. F., & Corassin, C. H. (2015a). The in vitro ability of different Saccharomyces cerevisiae - based products to bind Aflatoxin B1. Food Control, 47, 298-300. http://dx.doi.org/10.1016/j.foodcont.2014.07.024.
http://dx.doi.org/10.1016/j.foodcont.201...
, 2017,Gonçalves, B. L., Gonçalves, J. L., Rosim, R. E., Cappato, L. P., Cruz, A. G., Oliveira, C. A. F., & Corassin, C. H. (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(7), 5701-5708. http://dx.doi.org/10.3168/jds.2016-12215. PMid:28478008.
http://dx.doi.org/10.3168/jds.2016-12215...
).

Contamination may be prevented by good agricultural practices, antifungal agents, genetic engineering and storage control. Mycotoxin elimination or inactivation may be achieved by physical, chemical and biological methods (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Trombete et al., 2013Trombete, F. M., Fraga, M. E., & Saldanha, T. (2013). Contaminação de queijos por Aflatoxina M1: uma abordagem sobre a ocorrência e prevenção. Revista do Instituto de Latícinios Cândido Tostes, 68(392), 40-48. http://dx.doi.org/10.5935/2238-6416.20130027.
http://dx.doi.org/10.5935/2238-6416.2013...
). However, since these foods are already contaminated, adsorbents can be used in the animal feed, in order to reduce the bioavailability of these mycotoxins and thus avoid the excretion of AFM1 in milk, as described by (Firmin et al., 2011Firmin, S., Morgavi, D. P., Yiannikouris, A., & Boudra, H. (2011). Effectiveness of modified yeast cell wall extracts to reduce aflatoxin B1 absorption in dairy ewes. Journal of Dairy Science, 94(11), 5611-5619. http://dx.doi.org/10.3168/jds.2011-4446. PMid:22032384.
http://dx.doi.org/10.3168/jds.2011-4446...
; Gonçalves et al., 2017Gonçalves, B. L., Gonçalves, J. L., Rosim, R. E., Cappato, L. P., Cruz, A. G., Oliveira, C. A. F., & Corassin, C. H. (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(7), 5701-5708. http://dx.doi.org/10.3168/jds.2016-12215. PMid:28478008.
http://dx.doi.org/10.3168/jds.2016-12215...
).

If the fore-mentioned methods are not applied, and AFM1 is present in milk, according to Fallah (2010)Fallah, A. A. (2010). Assessment of aflatoxin M1 contamination in pasteurized and UHT milk marketed in central part of Iran. Food and Chemical Toxicology, 48(3), 988-991. http://dx.doi.org/10.1016/j.fct.2010.01.014. PMid:20093164.
http://dx.doi.org/10.1016/j.fct.2010.01....
, Manetta et al. (2009)Manetta, A. C., Giammarco, M., Giuseppe, L. D., Fusaro, I., Gramenzi, A., Formigoni, A., Vignola, G., & Lambertini, L. (2009). Distribution of aflatoxin M1 during Grana Padano cheese production from naturally contaminated milk. Food Chemistry, 113(2), 595-599. http://dx.doi.org/10.1016/j.foodchem.2008.07.091.
http://dx.doi.org/10.1016/j.foodchem.200...
and Trombete et al. (2013)Trombete, F. M., Fraga, M. E., & Saldanha, T. (2013). Contaminação de queijos por Aflatoxina M1: uma abordagem sobre a ocorrência e prevenção. Revista do Instituto de Latícinios Cândido Tostes, 68(392), 40-48. http://dx.doi.org/10.5935/2238-6416.20130027.
http://dx.doi.org/10.5935/2238-6416.2013...
, it will be also present in its dairy products (cheese, yogurts, etc.). According to the same authors and Campagnollo et al. (2016)Campagnollo, F. B., Ganev, K. C., Khaneghah, A. M., Portela, J. B., Cruz, A. G., Granato, D., Corassin, C. H., Oliveira, C. A. F., & 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. http://dx.doi.org/10.1016/j.foodcont.2016.04.007.
http://dx.doi.org/10.1016/j.foodcont.201...
this occurs because AFM1 is stable at the various stages of processing for the manufacture of dairy products such as pasteurization, UHT, milk coagulation, acidification, etc. In addition Ardic et al. (2009)Ardic, M., Karakaya, Y., Atasever, M., & Adiguzel, G. (2009). Aflatoxin M1 levels of Turkish white brined cheese. Food Control, 20(3), 196-199. http://dx.doi.org/10.1016/j.foodcont.2008.04.003.
http://dx.doi.org/10.1016/j.foodcont.200...
emphasized that cheese is a potential source of AFM1 when compared to other dairy products, because AFM1 is associated with casein, which is highly concentrated during its production.

3.3 Biological methods for decontamination

Several methods have been used to reduce the availability of mycotoxins, especially aflatoxins, in food intended for humans. These methods may be physical, chemical or biological (Bovo et al., 2010Bovo, F., Corassin, C. H., & Oliveira, C. A. F. (2010). Descontaminação de aflatoxinas em alimentos por bactérias ácido-láticas. Journal of Health Science, 12(2), 15-21. http://dx.doi.org/10.17921/2447-8938.
http://dx.doi.org/10.17921/2447-8938...
).

The main physical methods used to reduce the availability of mycotoxins are thermal inactivation, ultraviolet light, ionizing radiation, or extraction with solvents. Chemical methods include chlorination and oxidant or hydrolytic agents (El-Nezami et al., 1998El-Nezami, H., Kankaanpaa, P., Salminen, S., & Ahokas, J. (1998). Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1. Food and Chemical Toxicology, 36(4), 321-326. http://dx.doi.org/10.1016/S0278-6915(97)00160-9. PMid:9651049.
http://dx.doi.org/10.1016/S0278-6915(97)...
; Oliveira & Corassin, 2014Oliveira, C. A. F., & Corassin, C. H. (2014). Aflatoxins. In S.C. Duarte, A. L. S. Pena & C.M. Lino (Eds.), Mycotoxins and their implications in food safety (pp. 113). London: Future Science Ltd. http://dx.doi.org/10.4155/ebo.13.468.
http://dx.doi.org/10.4155/ebo.13.468...
). However, both chemical and physical methods have advantages and disadvantages, as they do not completely remove completely the toxin, are expensive and cause nutritional and organoleptic losses to the products (Magan & Olsen, 2006Magan, N., & Olsen, M. (2006). Mycotoxins in food: detection and control. Boca Raton: CRC Press.). Therefore, the use of microorganisms to degrade mycotoxins has become an attractive alternative for control or reducing the bioavailability of these toxins in food (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Fazeli et al., 2009Fazeli, M. R., Hajimohammadali, M., Moshkani, A., Samadi, N., Jamalifar, H., Khoshayand, M. R., Vaghari, E., & Pouragahi, S. (2009). Aflatoxin B1 binding capacity of Autochthonous strains of lactic acid bacteria. Journal of Food Protection, 72(1), 189-192. http://dx.doi.org/10.4315/0362-028X-72.1.189. PMid:19205485.
http://dx.doi.org/10.4315/0362-028X-72.1...
; Gonçalves et al., 2015bGonçalves, B. L., Corassin, C. H., & Oliveira, C. A. F. (2015b). Mycotoxicoses in dairy cattle: a review. Asian Journal of Animal and Veterinary Advances, 10(11), 752-760. http://dx.doi.org/10.3923/ajava.2015.752.760.
http://dx.doi.org/10.3923/ajava.2015.752...
).

Biological methods are based on the action of microorganisms such as yeasts, molds, bacteria and algae on mycotoxins, through competition for nutrients and space, interaction and antibiosis (Fazeli et al., 2009Fazeli, M. R., Hajimohammadali, M., Moshkani, A., Samadi, N., Jamalifar, H., Khoshayand, M. R., Vaghari, E., & Pouragahi, S. (2009). Aflatoxin B1 binding capacity of Autochthonous strains of lactic acid bacteria. Journal of Food Protection, 72(1), 189-192. http://dx.doi.org/10.4315/0362-028X-72.1.189. PMid:19205485.
http://dx.doi.org/10.4315/0362-028X-72.1...
). In addition, these decontamination methods have been well studied since they are efficient, cost-effective, and in many cases are already used in food production, such as acid lactic bacteria and yeast Saccharomyces cerevisiae (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
; Gonçalves et al., 2015aGonçalves, B. L., Rosim, R. E., Oliveira, C. A. F., & Corassin, C. H. (2015a). The in vitro ability of different Saccharomyces cerevisiae - based products to bind Aflatoxin B1. Food Control, 47, 298-300. http://dx.doi.org/10.1016/j.foodcont.2014.07.024.
http://dx.doi.org/10.1016/j.foodcont.201...
).

According to the criteria of inclusion and exclusion of the research, eleven articles, published in the last decade, on biological methods of decontamination in milk and cheese, shown in Table 1, were selected.

Table 1
Biological methods of decontamination in milk in different countries in the last 10 years (2009 to date).

4 Challenges and implications of aflatoxin M1 methods of decontamination in milk and cheese

Although the occurrence of aflatoxins in milk and dairy products has been frequently reported, there is little information about biological decontaminating in these products. In the last decade, some studies around the world validated microbial decontamination of aflatoxin M1 as the most promising strategy due to their effectiveness, specificity and environmental friendly behavior to reduce or eliminate possible contamination by aflatoxins (Ismail et al., 2016Ismail, A., Akhtar, S., Levin, R. E., Ismail, T., Riaz, M., & Amir, M. (2016). Aflatoxin M1: Prevalence and decontamination strategies in milk and milk products. Critical Reviews in Microbiology, 42(3), 418-427. http://dx.doi.org/10.3109/1040841X.2014.958051. PMid:25853494.
http://dx.doi.org/10.3109/1040841X.2014....
) .

The main concern with exposure to aflatoxin M1 and consumption of dairy products is the exposure of children and the elderly (Fallah, 2010Fallah, A. A. (2010). Assessment of aflatoxin M1 contamination in pasteurized and UHT milk marketed in central part of Iran. Food and Chemical Toxicology, 48(3), 988-991. http://dx.doi.org/10.1016/j.fct.2010.01.014. PMid:20093164.
http://dx.doi.org/10.1016/j.fct.2010.01....
). Decontamination procedures may be physical, chemical and biological, should not modify the nutritional or technological milk and dairy products properties and be affordable and easy to use (Lee et al., 2015Lee, J., Her, J., & Lee, K. (2015). Reduction of aflatoxins (B1, B2, G1, and G2) in soybean-based model systems. Food Chemistry, 189, 45-51. http://dx.doi.org/10.1016/j.foodchem.2015.02.013. PMid:26190599.
http://dx.doi.org/10.1016/j.foodchem.201...
). Physical and chemical methods are not the most appropriate regarding safety, economy and the quality of treated products high costs or they result in nutritional and sensory damage to the product (Wochner et al., 2018Wochner, K. F., Becker-algeri, T. A., Colla, E., Badiale-Furlong, E., & Drunkler, D. A. (2018). The action of probiotic microorganisms on chemical contaminants in milk. Critical Reviews in Microbiology, 44(1), 112-123. http://dx.doi.org/10.1080/1040841X.2017.1329275. PMid:28537817.
http://dx.doi.org/10.1080/1040841X.2017....
). In this context the proposal of biological methods of decontamination, aflatoxins or mycotoxins in general, is to improve the quality and safety of the products.

The application of biological methods for decontamination of aflatoxins has been noticeably in recent years, resulting in new data as the studies reported in Table 1.

Foroughi et al. (2019)Foroughi, M., Sarabi Jamab, M., Keramat, J., & Najaf Najafi, M. (2019). The use of Saccharomyces cerevisiae immobilized on activated alumina, and alumina silicate beads for the reduction of Aflatoxin M1 in vitro. Journal of Food Processing and Preservation, 43(2), 1-7. http://dx.doi.org/10.1111/jfpp.13876.
http://dx.doi.org/10.1111/jfpp.13876...
tested the decontamination of milk samples contaminated with different concentrations of AFM1 (0.08; 0.13; 0.18; 0.23 μg/L) using S. cerevisiae 108 (CFU/mL) immobilized with perlite. The milk samples were passed through the biofilter at three different treatment times (20, 40 and 80 minutes). For the milk sample with a lower concentration of AFM1 (0.08 μg/L) 40 minutes treatment was sufficient to eliminate all the toxin. However, in the sample with the highest concentration (0.23 μg/L), the best result 81.3% was obtained only at the highest circulation time. According to the authors, the amount of AFM1 removed is related to the initial concentration of toxin and the time of circulation, in general the longer the treatment, the lower concentration of AFM1 residue is present in milk. In addition, the authors report that the processing influenced the microbial load of the milk, which increased linearly with the increase of the circulation time (P <0.05); concluding that the shortest circulation time would be the most desirable. Despite the increase in microbial load, the physicochemical properties of the milk did not change. The authors conclude that the use of S. cerevisiae immobilized with perlite may be a practical solution to address the problem of contamination of aflatoxins in dairy products.

Kuharić et al. (2018)Kuharić, Ž., Jakopović, Ž., Čanak, I., Frece, J., Bošnir, J., Pavlek, Ž., Ivešić, M., & Markov, K. (2018). Removing aflatoxin M1 from milk with native lactic acid bacteria, centrifugation and filtration. Archives of Industrial Hygiene and Toxicology, 69(4), 334-339. http://dx.doi.org/10.2478/aiht-2018-69-3160. PMid:30864375.
http://dx.doi.org/10.2478/aiht-2018-69-3...
selected, isolated and identified ten species of lactic acid bacteria from milk and dairy products with the objective to select a strain which binds more effectively to AFM1. In addition, they assessed whether the heat treatment of LAB would affect binding ability. For this, the authors selected 10 species of LAB, which could be used viable or treated at the concentration of 108 (CFU/mL). These BALs were added to milk containing AFM1 (0.05 μg/L) and the binding capacity was evaluated after 2, 4 and 24 hours. The authors reported that binding efficiency ranged from 21 to 92% for viable cells and from 26 to 94.5 for thermally treated cells. According to Kuharić et al. (2018)Kuharić, Ž., Jakopović, Ž., Čanak, I., Frece, J., Bošnir, J., Pavlek, Ž., Ivešić, M., & Markov, K. (2018). Removing aflatoxin M1 from milk with native lactic acid bacteria, centrifugation and filtration. Archives of Industrial Hygiene and Toxicology, 69(4), 334-339. http://dx.doi.org/10.2478/aiht-2018-69-3160. PMid:30864375.
http://dx.doi.org/10.2478/aiht-2018-69-3...
although the mechanisms of action of lactic acid bacteria on aflatoxins has not yet been fully elucidated, some studies suggest that AFM1 molecules bind physically to cell wall components, mainly polysaccharides and peptidoglycans, instead of creating covalent bonds with or being metabolized by lactic acid bacteria. In addition, they emphasize that the heat treatment seems to increase the binding surface for AFM1, providing not only the wall of the lactic acid bacteria cell, but also other components. Finally, these authors conclude that the binding of AFM1-LAB is reversible, and that the percentage of reversibility is greater in untreated cells.

Ismail et al. (2017)Ismail, A., Levin, R. E., Riaz, M., Akhtar, S., Gong, Y. Y., & Oliveira, C. A. F. (2017). Effect of different microbial concentrations on binding of aflatoxin M1 and stability testing. Food Control, 73, 492-496. http://dx.doi.org/10.1016/j.foodcont.2016.08.040.
http://dx.doi.org/10.1016/j.foodcont.201...
evaluated three strains of lactic acid bacteria, one strain of S. cerevisiae and a mixture of all, in relation to their ability to reduce AFM1 in milk. Samples were contaminated with different concentrations of AFM1 (0.05 and 0.01 μg/L) and four different concentrations of microorganisms were tested (107, 108, 109, 1010 CFU/mL). The authors reported that significant differences were observed in relation to the binding capacity of the different concentrations of microorganisms in the different concentrations of AFM1. They observed that the binding capacity of each microorganism is directly proportional to its concentration, i.e., maximum binding capacity was recorded at 1010 CFU/mL and minimum at 107 CFU/mL. The authors also reported that the general trend of binding by microorganisms was found in the following order S. cerevisiae > pool of microorganisms > Lactobaccilus helveticus > Lactobacillus plantarum > Lactococcus lactis. Finally, the authors concluded that the 1010 CFU/mL concentration can be used efficiently to reduce AFM1 levels to the limit considered safe by legislation; the AFM1-LAB binding is a reversible process, since lavage of the complex results in the release of AFM1. Similarly, (Corassin et al., 2013Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80-83. http://dx.doi.org/10.1016/j.foodcont.2012.09.033.
http://dx.doi.org/10.1016/j.foodcont.201...
) evaluated the ability of S. cerevisiae and pool of three different lactic acid bacteria (Lactobacillus rhamnosus, Lactobacillus delbrueckii spp. bulgaricus e Bifidobacterium lactis) alone or in combination to bind AFM1 in UHT milk skim spiked 0.5 µg AFM1/L. All the lactic acid bacteria (1010 CFU/mL) and S. cerevisiae (109 CFU/mL) cells were heat killed (100 °C, 60 minutes) and then used for checking the effect of contact time (30 or 60 minutes). These authors reported that S. cerevisiae showed higher capability to bind AFM1 in milk than lactic acid bacteria pool and when using S. cerevisiae and lactic acid bacteria pool associated a significant increase observed in the percentage of AFM1 bound. In agreement Abdelmotilib et al. (2018)Abdelmotilib, N., Hamad, G., Elderea, H., Salem, E., & Sohaimy, S. (2018). Aflatoxin M1 reduction in milk by a novel combination of probiotic bacterial and yeast strains. European Journal of Nutrition & Food Safety, 8(2), 83-99. http://dx.doi.org/10.9734/EJNFS/2018/39486.
http://dx.doi.org/10.9734/EJNFS/2018/394...
reported that lactic acid bacteria and yeast strains can detox AFM1 in contaminated milk. However, a combination of LABs and yeasts could be better for removal and elimination of AFM1 from milk. Furthermore, these authors emphasize that bacteria and yeasts could be used as food additives to reduce the bioavailability of the aflatoxins in dairy products.

El Khoury et al. (2011)El Khoury, A., Atoui, A., & Yaghi, J. (2011). Analysis of aflatoxin M1 in milk and yogurt and AFM1 reduction by lactic acid bacteria used in Lebanese industry. Food Control, 22(10), 1695-1699. http://dx.doi.org/10.1016/j.foodcont.2011.04.001.
http://dx.doi.org/10.1016/j.foodcont.201...
reported that when lactic acid bacteria cultures (Lactobacillus bulgaricus and Streptococcus thermophilus) in PBS and skimmed processing milk were compared, the binding was much greater in milk. According to these authors the main reason of that is may be due to the binding properties of AFM1 to milk casein. Furthermore, they emphasized that binding level of AFM1 by L. bulgaricus increased with time and as they expected S. thermophilus showed a lower binding capacity to removal AFM1 making in comparison to L. bulgaricus. In conclusion the authors reported that LAB seem to play a crucial role in AFM1 removal.

Bovo et al. (2013)Bovo, F., Corassin, C. H., Rosim, R. E., & de Oliveira, C. A. F. (2013). Efficiency of Lactic Acid Bacteria Strains for Decontamination of Aflatoxin M1 in Phosphate Buffer Saline Solution and in Skimmed Milk. Food and Bioprocess Technology, 6(8), 2230-2234. http://dx.doi.org/10.1007/s11947-011-0770-9.
http://dx.doi.org/10.1007/s11947-011-077...
compared treatments for binding AFM1 in skimmed milk in two different temperatures 4 and 37 °C (last T°C the results are show in Table 1. The binding percentage of AFM1 in UHT skimmed milk at 4 °C was 13.51, 19.7 and 37.75 for L. bulgaricus, L. rhamnosus and B. lactis, respectively. These Authors reported that the temperature is no significant difference for L. rhmanosus and B. lactis, only for L. bulgaricus at 37 °C. In addition, Bovo et al. (2013)Bovo, F., Corassin, C. H., Rosim, R. E., & de Oliveira, C. A. F. (2013). Efficiency of Lactic Acid Bacteria Strains for Decontamination of Aflatoxin M1 in Phosphate Buffer Saline Solution and in Skimmed Milk. Food and Bioprocess Technology, 6(8), 2230-2234. http://dx.doi.org/10.1007/s11947-011-0770-9.
http://dx.doi.org/10.1007/s11947-011-077...
emphasizes that the LAB/AFM1 complex was unstable and the amount of toxin released to the solution varied widely from strain to strain. Corroborating with this Serrano-Niño et al. (2013)Serrano-Niño, J. C., Cavazos-Garduño, A., Hernandez-Mendoza, A., Applegate, B., Ferruzzi, M. G., San Martin-González, M. F., & García, H. S. (2013). Assessment of probiotic strains ability to reduce the bioaccessibility of aflatoxin M1 in artificially contaminated milk using an in vitro digestive model. Food Control, 31(1), 202-207. http://dx.doi.org/10.1016/j.foodcont.2012.09.023.
http://dx.doi.org/10.1016/j.foodcont.201...
reported that AFM1 binding capacity was reversible process since all strain tested released a small portion of bound AFM1 after a single wash with PBS. Furthermore, these authors emphasized that variations in binding abilities among strains suggest that different binding sites could be present in different strain and there could be differences between sites in each bacterium.

5 Conclusions

Worldwide contamination of milk and cheese with aflatoxin M1 has been raised as a crucial issue, which becomes more critical mainly due to potential dietary exposure of children and the elderly. Some studies around the world validated microbial decontamination of aflatoxin M1 as the most promising strategy due to their effectiveness and environmentally friendly behavior.

Our study reviewed biological methods for decontamination of aflatoxin M1 in milk and cheese, as well as challenges and implications on these methods. We observed that in the last decade few studies have been published on these methods and unfortunately none of the published studies tested such methods in cheese. Throughout the research were found many studies on decontamination methods however in phosphate buffered saline solution or in culture medium. Further studies on biological methods for decontamination in milk and mainly in cheeses and dairy products are necessary for this technique to be better developed and applied to large scale industries.

Acknowledgements

The authors would like to thank São Paulo Research of Foundation (FAPESP) for the fellowship (Grant #2017/20081-6 and #2017/19683-1) and this study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) – Finance Code 001.

  • Practical Application: One of the main objectives of the food industry is to avoid mycotoxin contamination in processes and products. Microbial decontamination of aflatoxin M1 as the most promising strategy due to their effectiveness and environmentally friendly behavior.

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Publication Dates

  • Publication in this collection
    09 Oct 2020
  • Date of issue
    2022

History

  • Received
    17 June 2020
  • Accepted
    08 July 2020
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