Investigation of efficiency of Bifidobacterium bifidum and Saccharomyces cerevisiae for detoxification of aflatoxin M1 in skim milk using HPLC analysis
Subject Areas : Microbiology
mostafa
fakhrabadi
1
(PhD Student of the Department of Food Hygiene, Qeshm Branch, Islamic Azad University, Qeshm, Iran.)
Amireghbal
khajeh rahimi
2
(Assistant Professor of the Department of Aquatic Hygiene, North Tehran Branch, Islamic Azad University, Tehran, Iran.)
nakisa
sohrabi hagh doost
3
(Assistant Professor of the Department of Pathobiology, Science and Research Branch, Islamic Azad University, Tehran, Iran.)
AMIRALI
Anvar
4
(Assistant Professor of the Department of Food Hygiene, Science and Research Branch, Islamic Azad University, Tehran, Iran.)
maryam
tala
5
(Assistant Professor of the Department of Fisheries, Qeshm Branch, Islamic Azad University, Qeshm, Iran.)
Keywords: HPLC, Milk, Probiotic, Aflatoxin M1,
Abstract :
Introduction: Food contamination with aflatoxin is identified as a challenge for health and economics; therefore, global organizations have determined the minimum contamination of different foods. Aflatoxin M1 (AFM1) is a carcinogenic mycotoxin mostly found in dairy products and its removal has remained a challenge. This study aimed to evaluate the effect of anti-aflatoxin of Bifidobacterium bifidum and Saccharomyces cerevisiae in contaminated skim milk.Materials and Methods: In order to carry out this project, skim milk was spiked with three concentrations of AFM1 and treated with two levels of bacteria and fungi concentration, alone or mixed, and incubated at 4 and 37 ˚C for different time points (30, 60, 120 min, and 24h). High-performance liquid chromatography (HPLC) was used to detect the AFM1 in milk.Results: The results showed that the incubation time is a key factor in the removal process of AFM1. Also, the removal of AFM1 was dependent on other factors such as the concentration of microorganisms, incubation temperature, toxin concentration and type of treatment (alone or combination). The ability of these strains to remove AFM1 after 24 hours was shown to be 20-90%. The removal of AFM1 by Saccharomyces cerevisiae (66.8%) as compared to Bifidobacterium bifidum (51.3%), and the combination of probiotics increased their ability to remove the toxins (90%).Conclusion: The results of this study showed that probiotics alone or in combination with each other play an essential role in removing AFM1 from milk.
Abdelmotilib, N. M., Hamad, G. M., Elderea, H. B., Salem, E. G. & El Sohaimy, S. A. (2018). Aflatoxin M1 reduction in milk by a novel combination of probiotic bacterial and yeast strains. regulation, 9.
Afshar, P., Shokrzadeh, M., Raisi, S. N., Ghorbani-HAasansaraei, A. & Nnasiraii, L. R. (2020). Aflatoxins biodetoxification strategies based on probiotic bacteria. Toxicon, 178, 50-58.
Bovo, F., Corassin, C. H., Rosim, R. E. & De Oliveira, C. A. (2013). Efficiency of Lactic Acid Bacteria Strains for Decontamination of Aflatoxin M₁ in Phosphate Buffer Saline Solution and in Skimmed Milk.
Corassin, C. H., Bovo, F., Rosim, R. E. & Oliveira, C. A. F. D. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food control, 31, 80-83.
Ehsani, A., Barani, A. & Nasiri, Z. (2016). Occurrence of aflatoxin B1 contamination in dairy cows feed in Iran. Toxin Reviews, 35, 54-57.
Gibellato, S., Dalsoquio, L., Do Nascimento, I. & Alvarez, T. (2021). Current and promising strategies to prevent and reduce aflatoxin contamination in grains and food matrices. World Mycotoxin Journal, 14, 293-304.
Goncalves, B. L., Goncalves, J. L., Rosim, R. E., Cappato, L. P., Cruz, A. G. D., Oliveira, C. A. F. D. & 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, 5701-5708.
Goncalves, B. L., Muaz, K., Coppa, C. F. S. C., Rosim, R. E., Kamimura, E. S., Oliveira, C. A. F. & Corassin, C. H. (2020a). Aflatoxin M1 absorption by non-viable cells of lactic acid bacteria and Saccharomyces cerevisiae strains in Frescal cheese. Food research international, 136, 109604.
Goncalves, B. L., Uliana, R. D., Coppa, C. F. S. C., Lee, S. H. I., Kamimura, E. S., Oliveira, C. A. F. & Corassin, C. H. (2020b). Aflatoxin M 1: biological decontamination methods in milk and cheese. Food Science and Technology.
Guan, Y., Chen, J., Nepovimova, E., Long, M., Wu, W. & Kuca, K. (2021). Aflatoxin detoxification using microorganisms and enzymes. Toxins, 13, 46.
Igbafe, J., Kilonzo-Nthenge, A., Nahashon, S. N., Mafiz, A. I. & Nzomo, M. (2020). Probiotics and antimicrobial effect of Lactiplantibacillus plantarum, Saccharomyces cerevisiae, and Bifidobacterium longum against common foodborne pathogens in poultry. Agriculture, 10, 368.
Iqbal, S. Z., Jinap, S., Pirouz, A. & Faizal, A. A. (2015). Aflatoxin M1 in milk and dairy products, occurrence and recent challenges: A review. Trends in Food Science & Technology, 46, 110-119.
Ismail, 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, 418-427.
Ismail, A., Levin, R. E., Riaz, M., Akhtar, S., Gong, Y. Y. & De Oliveira, C. A. (2017). Effect of different microbial concentrations on binding of aflatoxin M1 and stability testing. Food Control, 73, 492-496.
Karazhiyan, H., Mehraban, S. M., Karazhyan, R., Mehrzad, A. & Haghighi, E. (2016). Ability of different treatments of Saccharomyces cerevisiae to surface bind aflatoxin M1 in yoghurt.
Khadivi, R., Razavilar, V., Anvar, S. & Akbari-Adergani, B. (2020). Aflatoxin M1-binding ability of selected lactic acid bacteria strains and Saccharomyces boulardii in the experimentally contaminated milk treated with some biophysical factors. Archives of Razi Institute, 75, 63.
Kumar, P., Mahato, D. K., Kamle, M., Mohanta, T. K. & Kang, S. G. (2017). Aflatoxins: A global concern for food safety, human health and their management. Frontiers in microbiology, 7, 2170.
Marchese, S., Polo, A., Ariano, A., Velotto, S., Costantini, S. & Severino, L. (2018). Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins, 10, 214.
Marhamatizadeh, M. H. & Goosheh, S. R. (2016). The combined effect of thymus vulgaris extract and probiotic bacteria (Lactobacillus acidophilus and Bifidobacterium bifidum) on aflatoxin M^ sub 1^ concentration in kefir beverage. Italian Journal of Food Science, 28, 517.
Min, L., Li, D., Tong, X., Sun, H., Chen, W., Wang, G., Zheng, N. & Wang, J. (2020). The challenges of global occurrence of aflatoxin M1 contamination and the reduction of aflatoxin M1 in milk over the past decade. Food Control, 117, 107352.
Muaz, K., Riaz, M., Oliveira, C. A. F. D., Akhtar, S., Ali, S. W., Nadeem, H., Park, S. & Balasubramanian, B. (2022). Aflatoxin M1 in milk and dairy products: Global occurrence and potential decontamination strategies. Toxin reviews, 41, 588-605.
Namvar Rad, M., Razavilar, V., Anvar, S. A. A. & Akbari‐Adergani, B. (2018). Selected bio‐physical factors affecting the efficiency of Bifidobacterium animalis lactis and Lactobacillus delbrueckii bulgaricus to degrade aflatoxin M1 in artificially contaminated milk. Journal of Food Safety, 38, e12463.
Negash, D. (2018). A review of aflatoxin: occurrence, prevention, and gaps in both food and feed safety. Journal of Applied Microbiological Research, 1, 35-43.
Panwar, R., Kumar, N., Kashyap, V., Ram, C. & KAPILA, R. (2019). Aflatoxin M 1 detoxification ability of probiotic Lactobacilli of Indian origin in in vitro digestion model. Probiotics and antimicrobial proteins, 11, 460-469.
Pires, R. C., Portinari, M. R., Moraes, G. Z., Khaneghah, A. M., Goncalves, B. L., Rosim, R. E., Oliveira, C. A. & 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, 14,75-81.
Pop, O. L., Suharoschi, R. & Gabbianelli, R. (2022). Biodetoxification and protective properties of probiotics. Microorganisms, 10, 1278.
Rahmani, F. and Faraki, A., (2020). Microbial methods effect on adsorption and reduction of Aflatoxin contamination in milk.Food& Health Journal, 13-18.
Rezasoltani, S., Ebrahimi, N. A., Boroujeni, R. K., Aghdaei, H. A. & Norouzinia, M. (2022). Detoxification of aflatoxin M1 by probiotics Saccharomyces boulardii, Lactobacillus casei, and Lactobacillus acidophilus in reconstituted milk. Gastroenterology and Hepatology from Bed to Bench.
Sarlak, Z., Rouhi, M., Mohammadi, R., Khaksar, R., Mortazavian, A. M., Sohrabvandi, S. & Garavand, F. (2017). Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food control, 71, 152-159.
Serrano-Nino, J., Cavazos-Garduno, A., Hernandez-Mendoza, A., Applegate, B., Ferruzzi, M., San Martin-Gonzalez, M. & Garcia, H. (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, 202-207.
Sevim, S., Topal, G. G., Tengilimoglu-Metin, M. M., Sancak, B. & Kizil, M. (2019). Effects of inulin and lactic acid bacteria strains on aflatoxin M1 detoxification in yoghurt. Food control, 100, 235-239.
Sipos, P., Peles, F., Brasso, D. L., Beri, B., Pusztahelyi, T., Pocsi, I. & Gyori, Z. (2021). Physical and chemical methods for reduction in aflatoxin content of feed and food. Toxins, 13, 204.
Sokoutifar, R., Razavilar, V., Anvar, A. A. & Shoeiby, S. (2018). Degraded aflatoxin M1 in artificially contaminated fermented milk using Lactobacillus acidophilus and Lactobacillus plantarum affected by some bio‐physical factors. Journal of food safety, 38, e12544.
Thakur, S., Singh, R., De, P. & Dey, A. (2022). Aflatoxins in feeds: Issues and concerns with safe food production. Indian Journal of Animal Health, 2.
Turna, N. S. & Wu, F. (2021). Aflatoxin M1 in milk: A global occurrence, intake, & exposure assessment. Trends in Food Science & Technology, 110, 183-192.
_||_Abdelmotilib, N. M., Hamad, G. M., Elderea, H. B., Salem, E. G. & El Sohaimy, S. A. (2018). Aflatoxin M1 reduction in milk by a novel combination of probiotic bacterial and yeast strains. regulation, 9.
Afshar, P., Shokrzadeh, M., Raisi, S. N., Ghorbani-HAasansaraei, A. & Nnasiraii, L. R. (2020). Aflatoxins biodetoxification strategies based on probiotic bacteria. Toxicon, 178, 50-58.
Bovo, F., Corassin, C. H., Rosim, R. E. & De Oliveira, C. A. (2013). Efficiency of Lactic Acid Bacteria Strains for Decontamination of Aflatoxin M₁ in Phosphate Buffer Saline Solution and in Skimmed Milk.
Corassin, C. H., Bovo, F., Rosim, R. E. & Oliveira, C. A. F. D. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food control, 31, 80-83.
Ehsani, A., Barani, A. & Nasiri, Z. (2016). Occurrence of aflatoxin B1 contamination in dairy cows feed in Iran. Toxin Reviews, 35, 54-57.
Gibellato, S., Dalsoquio, L., Do Nascimento, I. & Alvarez, T. (2021). Current and promising strategies to prevent and reduce aflatoxin contamination in grains and food matrices. World Mycotoxin Journal, 14, 293-304.
Goncalves, B. L., Goncalves, J. L., Rosim, R. E., Cappato, L. P., Cruz, A. G. D., Oliveira, C. A. F. D. & 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, 5701-5708.
Goncalves, B. L., Muaz, K., Coppa, C. F. S. C., Rosim, R. E., Kamimura, E. S., Oliveira, C. A. F. & Corassin, C. H. (2020a). Aflatoxin M1 absorption by non-viable cells of lactic acid bacteria and Saccharomyces cerevisiae strains in Frescal cheese. Food research international, 136, 109604.
Goncalves, B. L., Uliana, R. D., Coppa, C. F. S. C., Lee, S. H. I., Kamimura, E. S., Oliveira, C. A. F. & Corassin, C. H. (2020b). Aflatoxin M 1: biological decontamination methods in milk and cheese. Food Science and Technology.
Guan, Y., Chen, J., Nepovimova, E., Long, M., Wu, W. & Kuca, K. (2021). Aflatoxin detoxification using microorganisms and enzymes. Toxins, 13, 46.
Igbafe, J., Kilonzo-Nthenge, A., Nahashon, S. N., Mafiz, A. I. & Nzomo, M. (2020). Probiotics and antimicrobial effect of Lactiplantibacillus plantarum, Saccharomyces cerevisiae, and Bifidobacterium longum against common foodborne pathogens in poultry. Agriculture, 10, 368.
Iqbal, S. Z., Jinap, S., Pirouz, A. & Faizal, A. A. (2015). Aflatoxin M1 in milk and dairy products, occurrence and recent challenges: A review. Trends in Food Science & Technology, 46, 110-119.
Ismail, 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, 418-427.
Ismail, A., Levin, R. E., Riaz, M., Akhtar, S., Gong, Y. Y. & De Oliveira, C. A. (2017). Effect of different microbial concentrations on binding of aflatoxin M1 and stability testing. Food Control, 73, 492-496.
Karazhiyan, H., Mehraban, S. M., Karazhyan, R., Mehrzad, A. & Haghighi, E. (2016). Ability of different treatments of Saccharomyces cerevisiae to surface bind aflatoxin M1 in yoghurt.
Khadivi, R., Razavilar, V., Anvar, S. & Akbari-Adergani, B. (2020). Aflatoxin M1-binding ability of selected lactic acid bacteria strains and Saccharomyces boulardii in the experimentally contaminated milk treated with some biophysical factors. Archives of Razi Institute, 75, 63.
Kumar, P., Mahato, D. K., Kamle, M., Mohanta, T. K. & Kang, S. G. (2017). Aflatoxins: A global concern for food safety, human health and their management. Frontiers in microbiology, 7, 2170.
Marchese, S., Polo, A., Ariano, A., Velotto, S., Costantini, S. & Severino, L. (2018). Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins, 10, 214.
Marhamatizadeh, M. H. & Goosheh, S. R. (2016). The combined effect of thymus vulgaris extract and probiotic bacteria (Lactobacillus acidophilus and Bifidobacterium bifidum) on aflatoxin M^ sub 1^ concentration in kefir beverage. Italian Journal of Food Science, 28, 517.
Min, L., Li, D., Tong, X., Sun, H., Chen, W., Wang, G., Zheng, N. & Wang, J. (2020). The challenges of global occurrence of aflatoxin M1 contamination and the reduction of aflatoxin M1 in milk over the past decade. Food Control, 117, 107352.
Muaz, K., Riaz, M., Oliveira, C. A. F. D., Akhtar, S., Ali, S. W., Nadeem, H., Park, S. & Balasubramanian, B. (2022). Aflatoxin M1 in milk and dairy products: Global occurrence and potential decontamination strategies. Toxin reviews, 41, 588-605.
Namvar Rad, M., Razavilar, V., Anvar, S. A. A. & Akbari‐Adergani, B. (2018). Selected bio‐physical factors affecting the efficiency of Bifidobacterium animalis lactis and Lactobacillus delbrueckii bulgaricus to degrade aflatoxin M1 in artificially contaminated milk. Journal of Food Safety, 38, e12463.
Negash, D. (2018). A review of aflatoxin: occurrence, prevention, and gaps in both food and feed safety. Journal of Applied Microbiological Research, 1, 35-43.
Panwar, R., Kumar, N., Kashyap, V., Ram, C. & KAPILA, R. (2019). Aflatoxin M 1 detoxification ability of probiotic Lactobacilli of Indian origin in in vitro digestion model. Probiotics and antimicrobial proteins, 11, 460-469.
Pires, R. C., Portinari, M. R., Moraes, G. Z., Khaneghah, A. M., Goncalves, B. L., Rosim, R. E., Oliveira, C. A. & 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, 14,75-81.
Pop, O. L., Suharoschi, R. & Gabbianelli, R. (2022). Biodetoxification and protective properties of probiotics. Microorganisms, 10, 1278.
Rahmani, F. and Faraki, A., (2020). Microbial methods effect on adsorption and reduction of Aflatoxin contamination in milk.Food& Health Journal, 13-18.
Rezasoltani, S., Ebrahimi, N. A., Boroujeni, R. K., Aghdaei, H. A. & Norouzinia, M. (2022). Detoxification of aflatoxin M1 by probiotics Saccharomyces boulardii, Lactobacillus casei, and Lactobacillus acidophilus in reconstituted milk. Gastroenterology and Hepatology from Bed to Bench.
Sarlak, Z., Rouhi, M., Mohammadi, R., Khaksar, R., Mortazavian, A. M., Sohrabvandi, S. & Garavand, F. (2017). Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food control, 71, 152-159.
Serrano-Nino, J., Cavazos-Garduno, A., Hernandez-Mendoza, A., Applegate, B., Ferruzzi, M., San Martin-Gonzalez, M. & Garcia, H. (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, 202-207.
Sevim, S., Topal, G. G., Tengilimoglu-Metin, M. M., Sancak, B. & Kizil, M. (2019). Effects of inulin and lactic acid bacteria strains on aflatoxin M1 detoxification in yoghurt. Food control, 100, 235-239.
Sipos, P., Peles, F., Brasso, D. L., Beri, B., Pusztahelyi, T., Pocsi, I. & Gyori, Z. (2021). Physical and chemical methods for reduction in aflatoxin content of feed and food. Toxins, 13, 204.
Sokoutifar, R., Razavilar, V., Anvar, A. A. & Shoeiby, S. (2018). Degraded aflatoxin M1 in artificially contaminated fermented milk using Lactobacillus acidophilus and Lactobacillus plantarum affected by some bio‐physical factors. Journal of food safety, 38, e12544.
Thakur, S., Singh, R., De, P. & Dey, A. (2022). Aflatoxins in feeds: Issues and concerns with safe food production. Indian Journal of Animal Health, 2.
Turna, N. S. & Wu, F. (2021). Aflatoxin M1 in milk: A global occurrence, intake, & exposure assessment. Trends in Food Science & Technology, 110, 183-192.