Aflatoxin M1 Reduction by Probiotic Strains in Iranian Feta Cheese

Document Type : Research Article

Authors

1 Department of Food Science and Technology, School of Nutritional Sciences and Food Technology, Kermanshah University of Medical Sciences, Kermanshah, I.R. IRAN

2 Bel Rouzaneh Dairy Product Company, Qazvin, I.R. IRAN

3 Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences, Food Science and Technology, Shahid Beheshti University of Medical Sciences, I.R. IRAN

4 Department of Food Science and Technology, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, I.R. IRAN

5 Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences, Food Science and Technology, Shahid Beheshti University of Medical Sciences, Iran

6 Students Research Committee, Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences, Food Science and Technology, Shahid Beheshti University of Medical Sciences, I.R. IRAN

Abstract

Among the fermented products, cheese has a good potential to deliver probiotic microorganisms into the gastrointestinal system due to its high protein and fat contents. The contamination of milk with aflatoxin M deserves attention concerning cheese consumption due to the harmful effects on human health. The present research studied the reduction of aflatoxin M1 (AFM1) by two well-known probiotic strains in artificially aflatoxin-contaminated Feta cheese. Changes in pH, the viability of the probiotic strains, and the level of aflatoxin in the samples were analyzed during 60-day storage. The results showed that all samples containing probiotics dramatically reduced the AFM1 levels. From both the health and economic aspects, the B. bifidum species at an inoculation level of 107 CFU/mL has proven to be the best treatment, due to the lowest cost of probiotics, highest survival rate, and 30.12% reduction of AFM1.

Keywords

Main Subjects


[1] Cheese Ingredients Market by Cheese Type, https://www.researchandmarkets.com (2018)
[2] Tavakoli H.R., Riazipour M., Kamkar A., Shaldehi H.R., Mozaffari Nejad A.S., Occurrence of Aflatoxin M1 in White Cheese Samples from Tehran, Iran, Food Control (FC), 23:293-295 (2012).
[3] Anfossi L., Baggiani C., Giovannoli C., D’arco G., Passini C., Giraudi G., Occurrence of Aflatoxin M1 in Italian cheese: Results of a Survey Conducted in 2010 and Correlation with Manufacturing, Production Season, Milking Animals, and Maturation of Cheese, Food Control (FC), 25:125-130 (2012).
[4] Pecorelli I., Branciari R., Ortenzi R., Ciriaci, M., Checcarelli, S., Roila, R., Capotorti, A.,  Spaccini, G., Valiani, A., Evaluation of the Concentration Factor of Aflatoxin M1 in a Semi-Hard Pecorino Cheese Obtained from Naturally Contaminated Milk, Food Control (FC), 85:194-198 (2018).
[5] Fernandes A.M., Corrêa B., Rosim R.E., Kobashigawa E., Oliveira C.A.F., Distribution and Stability of Aflatoxin M1 During Processing and Storage of Minas Frescal Cheese, Food Control (FC), 24: 104-108 (2012).
[6] Pallavi R., Ramana D., Sashidhar R., A Simple Test Tube Screening Method for Identifying Aflatoxin-Producing Strains of Aspergillus sp. Using Coconut Milk Agar Medium, World J. Microbiol. Biotechnol. (WJMB), 13: 713-714 (1997).
[7] Siahmoshteh F., Hamidi-Esfahani, Z., Spadaro D., Shams-Ghahfarokhi M., Razzaghi-Abyaneh M. Unraveling the Mode of Antifungal Action of Bacillus Subtilis and Bacillus Amyloliquefaciens as Potential Biocontrol Agents Against Aflatoxigenic Aspergillus Parasiticus, Food Control (FC), 89:300-307(2018).
[8] Peng K.Y., Chen C.Y., Prevalence of Aflatoxin M1 in Milk and Its Potential Liver Cancer Risk in Taiwan, J. Food Protetc. (JFP), 72: 1025-1029 (2009).
[9] Iha M.H., Barbosa C.B., Okada I.A., Trucksess M.W., Aflatoxin M1 in Milk And Distribution and Stability of Aflatoxin M1 During Production and Storage of Yoghurt and Cheese, Food Control (FC), 29: 1-6 (2013).
[10] Chavarría G., Molina A., Leiva A., Méndez G., Wong-González E., Cortés-Muñoz M., Rodríguez C., Granados-Chinchilla F., Distribution, Stability, and Protein Interactions of Aflatoxin M1 in Fresh Cheese, Food Control (FC), 73: 581-586 (2017).
[11] Johnson M.E., A 100-Year Review: Cheese Production and Quality, J. Dairy Sci. (JDS), 100: 9952-9965 (2017).
[12] Campagnollo F.B., Ganev. K.C., Khaneghah. A.M., The Occurrence and Effect of Unit Operations for Dairy Products Processing on the Fate of Aflatoxin M1: A Review, 68: 310-329 (2016).
[13] Cavallarin L., Antoniazzi S., Giaccone D., Tabacco E., Borreani G. Transfer of Aflatoxin M1 from Milk to Ripened Cheese in Three Italian Traditional Production Methods, Food Control (FC), 38: 174-177 (2014).
[14] Blagojev N., Škrinjar M., Vesković-Moračanin S., Šošo V., Control of Mould Growth and Mycotoxin Production by Lactic Acid Bacteria Metabolites, Roman. Biotechnol. Lett. (RBL), 17: 7219-7226 (2012).
[15] Sarlak Z., Rouhi M., Mohammadi, R., Khaksar R.,  Mortazavian  A.M.,  Sohrabvandi, Garavand F., Probiotic Biological Strategies to Decontaminate Aflatoxin M1 in a Traditional Iranian Fermented Milk Drink (Doogh), Food Control (FC), 71: 152-159 (2017).
[16] Kabak B., Var I., Factors Affecting the Removal of Aflatoxin M1 From Food Model by Lactobacillus And Bifidobacterium Strains, J. Environ. Sci. Health Part B(JESH) 43: 617-624 (2008).
 [17] Karimi R., Mortazavian A.M., Karami M., Incorporation of Lactobacillus Casei in Iranian Ultrafiltered Feta Cheese Made by Partial Replacement of NaCl with KCl, J. Dairy Sci. (JDS), 95: 4209-4222 (2012).
[18] Rouhi, M., Mohammadi, R., Mortazavian, AM., Sarlak Z., Combined Effects of Replacement of Sucrose with D-Tagatose and Addition of Different Probiotic Strains on Quality Characteristics of Chocolate Milk. Dairy Sci  Technol (DST), 95: 115-133(2015).
 [19] Gomes A.M.P., Malcata F.X., Bifidobacterium spp. and Lactobacillus Acidophilus: Biological, Biochemical, Technological and Therapeutical Properties Relevant for Use as Probiotics, Trends Food Sci. Technol. (TFST),10: 139-157(1999).
[20] Hernandez-Mendoza A., Garcia H., Steele J., Screening of Lactobacillus Casei Strains for Their Ability to Bind Aflatoxin B1, Food Chem. Toxicol. (FCT),47: 1064-1068 (2009).
[21] Microbiology of Milk and Milk Products – Specifications And Test Methods, National Iranian Standard, NO. 2406 (2017).
[22] Vinderola G., Prosello W., Molinari F., Ghiberto D., Reinheimer J. Growth of Lactobacillus Paracasei A13 in Argentinian Probiotic Cheese and Its Impact on the Characteristics of the Product, Int. J. Food Microbiol. (IJFM), 135: 171-174(2009).
[23] Ahmadi, E., Mortazavian, AM., Fazeli, MR., Ezzatpanah, H., Mohammadi R ., The Effects of Inoculant Variables on the Physicochemical and Organoleptic Properties of Doogh, Int. J. Dairy Technolo(IJDT), 65: 274-281 (2012).
[24] Sperry M.F., Silva H.L.A., Balthazar C.F.,  Esmerino E.A., Verruck S., Prudencio E.S., Neto R.P.C. , Tavares M.I.B., Peixoto  J.C., Nazzaro F., Rocha R.S., Moraes J., Gomes A.S.G., Raices, R.S.L., Silva M.C., Granato D., Pimentel T.C., Freitas M.Q., Cruz AG., Probiotic Minas Frescal Cheese Added with L. casei 01: Physicochemical and Bioactivity Characterization and Effects on Hematological/Biochemical Parameters of Hypertensive Overweighted Women – A Randomized Double-Blind Pilot Trial, J. Funct. Foods (JFF), 45: 435-443 (2018).
[25] Fang H.H.M., Arthur C., Bifidobacteria and Lactobacilli Exhibited Different Mitogenic Activity on Murine Splenocytes, Int J. Prob. Preb. (IJPP), 1: 77-82 (2006).
[26] Bylund G., “Tetra Pak Dairy Processing Handbook”, AB,  Lund (1995).
[27] Karimi R., Mortazavian A.M., Da Cruz, A.G., Viability of Probiotic Microorganisms in Cheese During Production and Storage: A Review, Dairy Sci. Technol.(DST), 91(3): 283-308 (2011).
[28] Corbo M.R., Albenzio M., De Angelis M., Sevi A., Gobbetti M., Microbiological and Biochemical Properties of Canestrato Pugliese Hard Cheese Supplemented with Bifidobacteria, J. Dairy Sci. (JDS), 84: 551-561(2001).
[29] Pierides M., El-Nezami H., Peltonen K., Salminen S., Ahokas J., Ability of Dairy Strains of Lactic Acid Bacteria to Bind Aflatoxin M1 in a Food Model, J. Food Protect. (JFP), 63: 645-650 (2000).
 [30] Rašić J.L., Škrinjar M., Markov S., Decrease of Aflatoxin B1 in Yoghurt and Acidified Milks, Mycopathologia, 113: 117-119 (1991).
[31] Sarimehmetoğlu B., Küplülü Ö., Binding Ability of Aflatoxin M1 to Yoghurt Bacteria, Ankara Üniv. Vet. Fak. Derg. (AUVFD), 51: 195-198 (2004).
[32] Nilchian Z., Rahimi E., Aflatoxin ML in Yoghurts, Cheese and Ice-Cream In Shahrekord-Iran, World Appl. Sci. J. (WASJ), 19: 621-624 (2012).
[33] Peltonen K., El-Nezami H., Haskard C., Ahokas J., Salminen S., Aflatoxin B1 Binding by Dairy Strains of Lactic Acid Bacteria and Bifidobacteria, J. Dairy Sci. (JDS), 84: 2152-2156 (2001).
[34] Fuchs S., Sontag G., Stidl R., Ehrlich V., Kundi M., Knasmüller S., Detoxification of Patulin and Ochratoxin A, Two Abundant Mycotoxins, by Lactic Acid Bacteria, Food Chem. Toxicol. (FCT), 46: 1398-1407 (2008).
[35] El-Nezami H., Polychronaki N., Lee Y.K., Chemical Moieties and Interactions Involved in the Binding of Zearalenone to the Surface of Lactobacillus Rhamnosus Strains GG, J Agric. Food Chem. (JAFC), 52: 4577-4581(2004).
[36] Haskard C., Binnion C., Ahokas J., Factors Affecting the Sequestration of Aflatoxin by Lactobacillus Rhamnosus Strain GG, Chem.-Biol. Interact. (CBI), 128: 39-49 (2000).
[37] Shahin A., Removal of Aflatoxin B1 from Contaminated Liquid Media by Dairy Lactic Acid Bacteria, Int. J. Agric. Biol. (IJAB), 9:71-75 (2007).
[38] Shah N., Wu X., Aflatoxin B1 Binding Abilities of Probiotic Bacteria, Biosci. Microfl. (BM), 18: 43-48 (1999).
[39] Pizzolitto R.P., Bueno D.J., Armando M.R., Cavaglieri L., Dalcero A.M., Salvano M.A., Binding of aflatoxin B1 to Lactic Acid Bacteria and Saccharomyces Cerevisiae in Vitro: A Useful Model to Determine the Most Efficient Microorganism. in 
"Aflatoxins - Biochemistry and Molecular Biology", InTech, Rijeka  (2011).
[40] Kabak B., Var I., Binding of Aflatoxin M1 by Lactobacillus and Bifidobacterium Strains, Milchwissenschaft, 59:301-303 (2004).
[41] Sezer Ç., Güven A., Oral N.B., Vatansever L., Detoxification of Aflatoxin B1 by Bacteriocins and Bacteriocinogenic Lactic Acid Bacteria, Turk. J. Vet. Anim. Sci. (TJVAS), 37: 594-601 (2013).