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Current Nutrition & Food Science

Author(s): Ramona Massoud* and Anousheh Sharifan

DOI: 10.2174/1573401319666221223142037

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Recent Advances in Biodecontamination of Aflatoxins in Foodstuffs: Using Biomass (2011-2021)

Page: [863 - 869] Pages: 7

  • * (Excluding Mailing and Handling)

Abstract

Background: Aflatoxin is one of the most hazardous toxins produced by Aspergillus spp. and contaminates animal feed and therefore human food. Aflatoxin exposure causes several health problems including liver, kidney, and intestine disorders for human beings. Therefore, an efficient decontamination method for food stuff seems essential.

Objective: The aim of this mini-review was to go over the recent advances in the decontamination of aflatoxins in foodstuffs and explain the bio-removal methods based on microorganisms during the last decade.

Methods: Literature research was performed using the keywords “aflatoxin”, “bio removal”, “decontamination”, “food”, and “biomass” individually or all together, in Scopus, Web of Science, and Pubmed in the last decade.

Results: LABs and yeasts are the most useful and successful microorganisms in this field. These methods are very efficient, specific, environmentally friendly, and cost-effective, also they do not affect the nutritional value of the foodstuffs, unlike the physical or chemical techniques. The bio-removal methods contain aflatoxin adsorption and degradation.

Conclusion: Although more studies and researches are required to evaluate the different types of toxin removal using various microorganisms and their practical aspects and the highest efficiency should be determined.

Graphical Abstract

[1]
Marshall H, Meneely JP, Quinn B, et al. Novel decontamination approaches and their potential application for post-harvest aflatoxin control. Trends Food Sci Technol 2020; 106: 489-96.
[http://dx.doi.org/10.1016/j.tifs.2020.11.001]
[2]
Meneely JP, Hajšlová J,, Krska R, Elliott CT. Assessing the combined toxicity of the natural toxins, aflatoxin B1, fumonisin B1 and microcystin-LR by high content analysis. Food Chem Toxicol 2018; 121: 527-40.
[http://dx.doi.org/10.1016/j.fct.2018.09.052]
[3]
Massoud R, Cruz A, Darani KK. Ochratoxin A: from safety aspects to prevention and remediation strategies. Curr Nutr Food Sci 2018; 14(1): 11-6.
[http://dx.doi.org/10.2174/1573401313666170517165500]
[4]
Hooshfar S, Khosrokhavar R, Yazdanpanah H, et al. Health risk assessment of aflatoxin M1 in infant formula milk in IR Iran. Food Chem Toxicol 2020; 55: 11-22.
[http://dx.doi.org/10.1016/j.fct.2020.111455]
[5]
Deng LZ, Tao Y, Mujumdar AS, et al. Recent advances in non-thermal decontamination technologies for microorganisms and mycotoxins in low-moisture foods. Trends Food Sci Technol 2020; 106: 104-12.
[http://dx.doi.org/10.1016/j.tifs.2020.10.012]
[6]
Mutua F, Lindahl J, Grace D. Availability and use of mycotoxin binders in selected urban and Peri-urban areas of Kenya. Food Secur 2019; 11(2): 359-69.
[http://dx.doi.org/10.1007/s12571-019-00911-4]
[7]
Eskola M, Kos G, Elliott CT, Hajšlová J,, Mayar S, Krska R. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit Rev Food Sci Nutr 2020; 60(16): 2773-89.
[http://dx.doi.org/10.1080/10408398.2019.1658570] [PMID: 31478403]
[8]
Massoud R, Hadiani MR, Hamzehlou P, Khosravi-Darani K. Bioremediation of heavy metals in food industry: Application of Saccharomyces cerevisiae. Electron J Biotechnol 2019; 37: 56-60.
[http://dx.doi.org/10.1016/j.ejbt.2018.11.003]
[9]
Pankaj SK, Shi H, Keener KM. A review of novel physical and chemical decontamination technologies for aflatoxin in food. Trends Food Sci Technol 2018; 71: 73-83.
[http://dx.doi.org/10.1016/j.tifs.2017.11.007]
[10]
Elzupir AO, Alamer AS, Dutton MF. The occurrence of aflatoxin in rice worldwide: a review. Toxin Rev 2015; 34(1): 37-42.
[http://dx.doi.org/10.3109/15569543.2014.984229]
[11]
Ismail A, Gonçalves BL, de Neeff DV, et al. Aflatoxin in foodstuffs: Occurrence and recent advances in decontamination. Food Res Int 2018; 113: 74-85.
[http://dx.doi.org/10.1016/j.foodres.2018.06.067] [PMID: 30195548]
[12]
Ismaiel AA, Tharwat NA, Sayed MA, Gameh SA. Two-year survey on the seasonal incidence of aflatoxin M1 in traditional dairy products in Egypt. J Food Sci Technol 2020; 57(6): 2182-9.
[13]
Tonon KGR, Reiter MM, Scussel V. Mycotoxins levels in human milk: a menace to infants and children health. Curr Nutr Food Sci 2013; 9(1): 33-42.
[14]
Khosravi AR, Shokri H, Eshghi S, Darvishi S. Global occurrence of aflatoxin M1 in milk with particular reference to Iran. Food Secur 2013; 5(4): 533-9.
[http://dx.doi.org/10.1007/s12571-013-0281-9]
[15]
Zivoli R. Almonds: A source of healthy molecules or a risk of aflatoxins human exposure? Curr Nutr Food Sci 2017; 13(4): 255-9.
[http://dx.doi.org/10.2174/1573401313666170802144257]
[16]
Yavarmanesh M, Balssini M, Dovom MR, Yazdi F, Barouei J. Inclusion of dietary zeolite reduces aflatoxin b1 levels in household bread waste used as cattle feed. Curr Nutr Food Sci 2014; 10(2): 107-11.
[http://dx.doi.org/10.2174/1573401310666140306225620]
[17]
Mousavi Khaneghah A, D Chaves R, Akbarirad H. Detoxification of aflatoxin M1 (AFM1) in dairy base beverages (acidophilus milk) by using different types of lactic acid bacteria-mini review. Curr Nutr Food Sci 2017; 13(2): 78-81.
[http://dx.doi.org/10.2174/1573401313666170102162930]
[18]
Majeed M, Khaneghah AM, Kadmi Y, Khan MU, Shariati MA. Assessment of ochratoxin A in commercial corn and wheat products. Curr Nutr Food Sci 2018; 14(2): 116-20.
[http://dx.doi.org/10.2174/1573401313666170330155823]
[19]
Tonon KM, Reiter MGR, de Oliveira Dutra M, Savi GD, Scussel VM. Dietary intake of mycotoxin susceptible foods by brazilian nursing mothers. Curr Nutr Food Sci 2020; 16(6): 953-62.
[http://dx.doi.org/10.2174/1573401315666191009094147]
[20]
Franco LT, Khaneghah AM, Lee SI, Oliveira CF. Biomonitoring of mycotoxin exposure using urinary biomarker approaches: A review. Toxin Rev 2019; 57: 1-21.
[http://dx.doi.org/10.1080/15569543.2019.1619086]
[21]
Sakudo A, Toyokawa Y, Misawa T, Imanishi Y. Degradation and detoxification of aflatoxin B1 using nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply. Food Control 2017; 73: 619-26.
[http://dx.doi.org/10.1016/j.foodcont.2016.09.014]
[22]
Karlovsky P, Suman M, Berthiller F, et al. Impact of food processing and detoxification treatments on mycotoxin contamination. Mycotoxin Res 2016; 32(4): 179-205.
[http://dx.doi.org/10.1007/s12550-016-0257-7] [PMID: 27554261]
[23]
Jalili M. A review on aflatoxins reduction in food. Iran J Health Saf Environ 2016; 3(1): 445-59.
[24]
Roohi R, Hashemi SMB, Mousavi KA. Kinetics and thermodynamic modelling of the aflatoxins decontamination: a review. Int J Food Sci Technol 2020; 55(12): 3525-32.
[http://dx.doi.org/10.1111/ijfs.14689]
[25]
Mahmood FH, Abbasi R, Mousavi KA. The detoxification of aflatoxin M1 by Lactobacillus acidophilus and Bifidobacterium spp.: A review. J Food Process Preserv 2018; 42(9): e13704.
[http://dx.doi.org/10.1111/jfpp.13704]
[26]
Adebo OA, Njobeh PB, Gbashi S, Nwinyi OC, Mavumengwana V. Review on microbial degradation of aflatoxins. Crit Rev Food Sci Nutr 2017; 57(15): 3208-17.
[http://dx.doi.org/10.1080/10408398.2015.1106440] [PMID: 26517507]
[27]
Rushing BR, Selim MI. Aflatoxin B1: A review on metabolism, toxicity, occurrence in food, occupational exposure, and detoxification methods. Food Chem Toxicol 2019; 124: 81-100.
[http://dx.doi.org/10.1016/j.fct.2018.11.047]
[28]
Herzallah S, Alshawabkeh K, Fataftah AA. Aflatoxin decontamination of artificially contaminated feeds by sunlight, γ-radiation, and microwave heating. J Appl Poult Res 2008; 17(4): 515-21.
[http://dx.doi.org/10.3382/japr.2007-00107]
[29]
Al-Jaal BA, Jaganjac M, Barcaru A, Horvatovich P, Latiff A. Aflatoxin, fumonisin, ochratoxin, zearalenone and deoxynivalenol biomarkers in human biological fluids: A systematic literature review, 2001–2018. Food Chem Toxicol 2019; 129: 211-28.
[http://dx.doi.org/10.1016/j.fct.2019.04.047] [PMID: 31034935]
[30]
Saalia FK, Phillips RD. Degradation of aflatoxins by extrusion cooking: Effects on nutritional quality of extrudates. Lebensm Wiss Technol 2011; 44(6): 1496-501.
[http://dx.doi.org/10.1016/j.lwt.2011.01.021]
[31]
Park JW, Kim YB. Effect of pressure cooking on aflatoxin B1 in rice. J Agric Food Chem 2006; 54(6): 2431-5.
[32]
Mendez AA, Campos AA, Moreno ME, Vazquez DA. Physical and chemical degradation of B-aflatoxins during the roasting and dutching of cocoa liquor. J Agric Sci Technol 2013; 15: 557-67.
[33]
Turcotte AM, Scott PM, Tague B. Analysis of cocoa products for ochratoxin A and aflatoxins. Mycotoxin Res 2013; 29(3): 193-201.
[http://dx.doi.org/10.1007/s12550-013-0167-x] [PMID: 23564311]
[34]
Carraro A, De Giacomo A, Giannossi ML, et al. Clay minerals as adsorbents of aflatoxin M1 from contaminated milk and effects on milk quality. Appl Clay Sci 2014; 88-89: 92-9.
[http://dx.doi.org/10.1016/j.clay.2013.11.028]
[35]
Govaris A, Roussi V, Koidis PA, Botsoglou NA. Distribution and stability of aflatoxin M1 during production and storage of yoghurt. Food Addit Contam 2002; 19(11): 1043-50.
[http://dx.doi.org/10.1080/0265203021000007831] [PMID: 12456275]
[36]
Durmuş E, Güneş A, Kalkan H. Detection of aflatoxin and surface mould contaminated figs by using Fourier transform near-infrared reflectance spectroscopy. J Sci Food Agric 2017; 97(1): 317-23.
[http://dx.doi.org/10.1002/jsfa.7735] [PMID: 27018345]
[37]
Shi H, Cooper B, Stroshine RL, Ileleji KE, Keener KM. Structures of degradation products and degradation pathways of aflatoxin B1 by high-voltage atmospheric cold plasma (HVACP) treatment. J Agric Food Chem 2017; 65(30): 6222-30.
[http://dx.doi.org/10.1021/acs.jafc.7b01604] [PMID: 28643515]
[38]
Siciliano I, Spadaro D, Prelle A, et al. Use of cold atmospheric plasma to detoxify hazelnuts from aflatoxins. Toxin 2016; 8(5): 125.
[http://dx.doi.org/10.3390/toxins8050125] [PMID: 27128939]
[39]
Rastegar H, Shoeibi S, Yazdanpanah H, et al. Removal of aflatoxin B1 by roasting with lemon juice and/or citric acid in contaminated pistachio nuts. Food Control 2017; 71: 279-84.
[http://dx.doi.org/10.1016/j.foodcont.2016.06.045]
[40]
Iram W, Anjum T, Iqbal M, Ghaffar A, Abbas M. Mass spectrometric identification and toxicity assessment of degraded products of aflatoxin B1 and B2 by Corymbia citriodora aqueous extracts. Sci Rep 2015; 5(1): 14672.
[http://dx.doi.org/10.1038/srep14672] [PMID: 26423838]
[41]
Xiong K, Liu H, Li L. Product identification and safety evaluation of aflatoxin B1 decontaminated by electrolyzed oxidizing water. J Agric Food Chem 2012; 60(38): 9770-8.
[http://dx.doi.org/10.1021/jf303478y] [PMID: 22950859]
[42]
Fan S, Zhang F, Liu S, Yu C, Guan D, Pan C. Removal of aflatoxin B1 in edible plant oils by oscillating treatment with alkaline electrolysed water. Food Chem 2013; 141(3): 3118-23.
[http://dx.doi.org/10.1016/j.foodchem.2013.06.013] [PMID: 23871067]
[43]
Hashemi SMB, Amiri MJ. A comparative adsorption study of aflatoxin B1 and aflatoxin G1 in almond butter fermented by Lactobacillus fermentum and Lactobacillus delbrueckii subsp. lactis. Lebensm Wiss Technol 2020; 128109500.
[http://dx.doi.org/10.1016/j.lwt.2020.109500]
[44]
Mechtcherine V, Reinhardt HW, Eds. Application of super absorbent polymers (SAP) in concrete construction: state-of-the-art report prepared by Technical Committee 225-SAP. Springer Science & Business Media 2012.
[http://dx.doi.org/10.1007/978-94-007-2733-5]
[45]
Zoghi A, Khosravi-Darani K, Sohrabvandi S. Surface binding of toxins and heavy metals by probiotics. Mini Rev Med Chem 2014; 14(1): 84-98.
[http://dx.doi.org/10.2174/1389557513666131211105554] [PMID: 24329992]
[46]
Alberts JF, Gelderblom WCA, Botha A, van Zyl WH. Degradation of aflatoxin B1 by fungal laccase enzymes. Int J Food Microbiol 2009; 135(1): 47-52.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2009.07.022] [PMID: 19683355]
[47]
Focker M, van der Fels-Klerx HJ, Oude Lansink AGJM. Financial losses for Dutch stakeholders during the 2013 aflatoxin incident in Maize in Europe. Mycotoxin Res 2021; 37(2): 193-204.
[http://dx.doi.org/10.1007/s12550-021-00429-9] [PMID: 33783759]
[48]
Massoud R, Sharifan A, Khosravi-Darani K, Asadi G. Mercury biosorption process by using Saccharomyces cerevisiae in milk. J Food Process Preserv 2021; 45(1): e15008.
[http://dx.doi.org/10.1111/jfpp.15008]
[49]
Massoud R, Khosravi-Darani K, Sharifan A, Asadi GH. Lead bioremoval from milk by Saccharomyces cerevisiae. Biocat Agricul Biotech 2019; 22: 101437.
[http://dx.doi.org/10.1016/j.bcab.2019.101437]
[50]
Liu A, Zheng Y, Liu L, et al. Decontamination of aflatoxins by lactic acid bacteria. Curr Microbiol 2020; 77(12): 3821-0.
[http://dx.doi.org/10.1007/s00284-020-02220-y]
[51]
Nazareth TD, Luz C, Torrijos R, et al. Potential application of lactic acid bacteria to reduce aflatoxin B1 and fumonisin B1 occurrence on corn kernels and corn ears. Toxins 2019; 12(1): 21.
[http://dx.doi.org/10.3390/toxins12010021]
[52]
Sarlak Z, Rouhi M, Mohammadi R, et al. Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food Control 2017; 71: 152-9.
[http://dx.doi.org/10.1016/j.foodcont.2016.06.037]
[53]
Gonçalves BL, Gonçalves C, Rosim RE, Oliveira CAF, Corassin CH. Evaluations of different sources of Saccharomyces cerevisiae to binding capacity of aflatoxin B1 utilizing their adsorption isotherms. J Food Chem Nanotechnol 2017; 3(4): 2017-48.
[http://dx.doi.org/10.17756/jfcn.2017-048]
[54]
Khosravi-Darani K, Zoghi A, Jazayeri S, Da Cruz AG. Decontamination of Aflatoxins with a focus on Aflatoxin B1 by probiotic bacteria and yeasts: a review. J Microb Biotechnol food Sci 2020; 10(3): 424-35.
[55]
Elsanhoty RM, Salam SA, Ramadan MF, Badr FH. Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control 2014; 43: 129-34.
[http://dx.doi.org/10.1016/j.foodcont.2014.03.002]
[56]
Zhou G, Chen Y, Kong Q, Ma Y, Liu Y. Detoxification of aflatoxin B1 by Zygosaccharomyces rouxii with solid state fermentation in peanut meal. Toxins 2017; 9(1): 42.
[http://dx.doi.org/10.3390/toxins9010042] [PMID: 28117705]
[57]
Harkai P, Szabó I, Cserháti M, et al. Biodegradation of aflatoxin-B1 and zearalenone by Streptomyces sp. collection. Int Biodeterior Biodegradation 2016; 108: 48-56.
[http://dx.doi.org/10.1016/j.ibiod.2015.12.007]
[58]
Chen Y, Kong Q, Chi C, Shan S, Guan B. Biotransformation of aflatoxin B1 and aflatoxin G1 in peanut meal by anaerobic solid fermentation of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. Int J Food Microbiol 2015; 211: 1-5.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2015.06.021] [PMID: 26143229]
[59]
Raksha Rao K, Vipin AV, Hariprasad P, Anu Appaiah KA, Venkateswaran G. Biological detoxification of Aflatoxin B1 by Bacillus licheniformis CFR1. Food Control 2017; 71: 234-41.
[http://dx.doi.org/10.1016/j.foodcont.2016.06.040]
[60]
Eshelli M, Harvey L, Edrada-Ebel R, McNeil B. Metabolomics of the bio-degradation process of aflatoxin B1 by actinomycetes at an initial pH of 6.0. Toxins 2015; 7(2): 439-56.
[http://dx.doi.org/10.3390/toxins7020439] [PMID: 25658510]
[61]
Byakika S, Mukisa IM, Wacoo AP, Kort R, Byaruhanga YB, Muyanja C. Potential application of lactic acid starters in the reduction of aflatoxin contamination in fermented sorghum-millet beverages. Int J Food Contamin 2019; 6(1): 4.
[http://dx.doi.org/10.1186/s40550-019-0074-9]
[62]
Corassin CH, Bovo F, Rosim RE, Oliveira CAF. Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control 2013; 31(1): 80-3.
[http://dx.doi.org/10.1016/j.foodcont.2012.09.033]
[63]
Assaf JC, Nahle S, Chokr A, Louka N, Atoui A, El Khoury A. Assorted methods for decontamination of aflatoxin M1 in milk using microbial adsorbents. Toxins 2019; 11(6): 304.
[http://dx.doi.org/10.3390/toxins11060304]
[64]
Shetty PH, Hald B, Jespersen L. Surface binding of aflatoxin B1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. Int J Food Microbiol 2007; 113(1): 41-6.
[http://dx.doi.org/10.1016/j.ijfoodmicro.2006.07.013] [PMID: 16996157]
[65]
Gonçalves BL, Rosim RE, de Oliveira CAF, Corassin CH. The in vitro ability of different Saccharomyces cerevisiae – Based products to bind aflatoxin B1. Food Control 2015; 47: 298-300.
[http://dx.doi.org/10.1016/j.foodcont.2014.07.024]
[66]
Oluwafemi F, Kumar M, Bandyopadhyay R, Ogunbanwo T, Ayanwande KB. Bio-detoxification of aflatoxin B1 in artificially contaminated maize grains using lactic acid bacteria. Toxin Rev 2010; 29(3-4): 115-22.
[http://dx.doi.org/10.3109/15569543.2010.512556]
[67]
Rahaie S, Emam-Djomeh Z, Razavi SH, Mazaheri M. Evaluation of aflatoxin decontaminating by two strains of Saccharomyces cerevisiae and Lactobacillus rhamnosus strain GG in pistachio nuts. Int J Food Sci Technol 2012; 47(8): 1647-53.
[http://dx.doi.org/10.1111/j.1365-2621.2012.03015.x]
[68]
Bovo F, Corassin CH, Rosim RE, de Oliveira CAF. Efficiency of lactic acid bacteria strains for decontamination of aflatoxin M1 in phosphate buffer saline solution and in skimmed milk. Food Bioprocess Technol 2013; 6(8): 2230-4.
[http://dx.doi.org/10.1007/s11947-011-0770-9]
[69]
Ansari F, Rezaei K, Khodaiyan F, Rahmani A. Optimisation of aflatoxin B1 reduction in pistachio nuts by kefir grains using statistical experimental methods. Qual Assur Saf Crops Foods 2016; 8(4): 509-18.
[http://dx.doi.org/10.3920/QAS2015.0619]
[70]
Abdelmotilib N, Hamad G, Elderea H, Salem E, Sohaimy S. Aflatoxin M1 reduction in milk by a novel combination of probiotic bacterial and yeast strains. Eur J Nutr Food Saf 2018; 8(2): 83-99.
[http://dx.doi.org/10.9734/EJNFS/2018/39486]
[71]
Shigute T, Washe AP. Reduction of aflatoxin M1 levels during Ethiopian traditional fermented milk (Ergo) production. J Food Qual 2018; 2018: 1-10.
[http://dx.doi.org/10.1155/2018/4570238]
[72]
Florina R, Sofia P, Lia R, Antoanela C, Butnariu M. Effect of some probiotic bacteria on the reduction of aflatoxin B1 production in stored arabica coffee beans. Int Multidiscip Sci Geo Conference Surv Geol 2018; 18(6.4): 135-42.
[73]
Sevim S, Topal GG, Tengilimoglu-Metin MM, Sancak B, Kizil M. Effects of inulin and lactic acid bacteria strains on aflatoxin M1 detoxification in yoghurt. Food Control 2019; 100: 235-9.
[http://dx.doi.org/10.1016/j.foodcont.2019.01.028]
[74]
Mosallaie F, Jooyandeh H, Hojjati M, Fazlara A. Biological reduction of aflatoxin B1 in yogurt by probiotic strains of Lactobacillus acidophilus and Lactobacillus rhamnosus. Food Sci Biotechnol 2020; 29(6): 793-803.
[http://dx.doi.org/10.1007/s10068-019-00722-5] [PMID: 32523789]
[75]
Muaz K, Riaz M. Decontamination of aflatoxin m1 in milk through integration of microbial cells with sorbitan monostearate, activated carbon and bentonite. J Anim Plant Sci 2021; 31(1)