Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-14T11:15:51.018Z Has data issue: false hasContentIssue false

Innovative application of postbiotics, parabiotics and encapsulated Lactobacillus plantarum RM1 and Lactobacillus paracasei KC39 for detoxification of aflatoxin M1 in milk powder

Published online by Cambridge University Press:  23 December 2021

Karima Mogahed Fahim*
Affiliation:
Food Hygiene and Control Department, Faculty of Veterinary Medicine, Cairo University, Giza12211, Egypt
Ahmed Noah Badr
Affiliation:
Department of Food Toxicology and Contaminants, National Research Centre, Dokki, 12622Cairo, Egypt
Mohamed Gamal Shehata
Affiliation:
Department of Food Technology, Arid Lands Cultivation Research Institute, City of Scientific Research and Technological Application, Alexandria, Egypt
Eman Ibrahim Hassanen
Affiliation:
Department of Pathology, Faculty of Veterinary Medicine, Cairo University, Giza12211, Egypt
Lamiaa Ibrahim Ahmed
Affiliation:
Food Hygiene and Control Department, Faculty of Veterinary Medicine, Cairo University, Giza12211, Egypt
*
Author for correspondence: Karima Mogahed Fahim, Email: [email protected]

Abstract

This study aimed to evaluate aflatoxin M1 (AFM1) level in milk powder and infant milk formulae, in addition to applying innovative methods for AFM1 & AFB1 detoxification. Fifty random samples of milk powder and infant formulae (25 of each) were collected from the Egyptian markets for assessing AFM1 level using ELISA technique. Bioactive components comprising cell free supernatants (postbiotic), acid-dead cells (parabiotic) and the encapsulated-cells of Lactobacillus plantarum RM1 and Lactobacillus paracasei KC39 were evaluated for their antifungal activity against toxigenic mold strains and their impact on AFB1 and AFM1 reduction in reconstituted milk powder. AFM1 concentration in unpacked milk powder was higher than that of packed samples and infant formulae, although these differences were not significant (P > 0.05). About 96.0, 29.4 and 25.0% of the tested infant formulae, unpacked, and packed milk powder were unacceptable in terms of the AFM1 limit defined by Egyptian and European standards, while all samples were in accordance with the USA/FDA standard. All tested mycotoxigenic strains were sensitive to the different treatments of the probiotics with the highest sensitivity regarding Fusarium strain with L. paracasei KC39 compared to other genera. The degradation ratios of AFM1 using the bioactives of the L. paracasei KC39 were higher than that of L. plantarum RM1 bioactives. Additionally, KC39 parabiotic manifested the best AFB1 reduction (60.56%). In conclusion, the positive and highly significant relationship (P < 0.05) between these effective biocompounds mirrors their major detoxification role which gives a safe solution for AFs contamination issues in milk and milk products.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Razek, AG, Badr, AN, El-Messery, TM, El-Said, MM and Hussein, AMS (2018) Micro-nano encapsulation of black seed oil ameliorate its characteristics and its mycotoxin inhibition. Bioscience Research 15, 25912601.Google Scholar
Ahlberg, S, Grace, D, Kiarie, G, Kirino, Y and Lindahl, J (2018) A risk assessment of aflatoxin M1 exposure in low and mid-income dairy consumers in Kenya. Toxins 10, 348.CrossRefGoogle ScholarPubMed
Ahmed, KMF, Hafez, RS, Morgan, SD and Awad, AA (2015) Detection of some chemical hazards in milk and some dairy products. African Journal of Food Science 9, 187193.Google Scholar
Ahmed, LI, Awad, AA, Mohamed, SY and El Kutry, MS (2020) Biohazards and fat deterioration associated with fresh cream and cream filled pastries. Bioscience Research 17, 539549.Google Scholar
Ahmed, LI, Nehal, I, Abdel-Salam, AB and Fahim, KM (2021) Potential application of ginger, clove and thyme essential oils to improve soft cheese microbial safety and sensory characteristics. Food Bioscience 42, 101177.CrossRefGoogle Scholar
Assaf, JC, Atoui, A, Khoury, AE, Chokr, A and Louka, N (2017) A comparative study of procedures for binding of aflatoxin M1 to Lactobacillus rhamnosus GG. Brazilian Journal of Microbiology 49, 120127.CrossRefGoogle ScholarPubMed
Azab, RM, Tawakkol, WM, Hamad, A, Abou-Elmagd, MK, El-Agrab, HM and Refai, MK (2001) Detection and estimation of aflatoxin B1 in feeds and its biodegradation by bacteria and fungi. Egyptian Journal of Natural Toxins 2, 3956, (2005).Google Scholar
Badr, AN, Ali, HS, Abdel-Razek, AG, Shehata, MG and Albaridi, NA (2020) Bioactive components of pomegranate oil and their influence on mycotoxin secretion. Toxins 12, 12.CrossRefGoogle ScholarPubMed
Ben Taheur, F, Mansour, C, Ben Jeddou, K, Machreki, Y, Kouidhi, B, Abdulhakim, JA and Chaieb, K (2020) Aflatoxin B1 degradation by microorganisms isolated from Kombucha culture. Toxicon 179, 7683.CrossRefGoogle ScholarPubMed
EC European Commission Regulation (1881/2006) Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union 364, 524.Google Scholar
El-Nezami, H, Kankaanpaa, P, Salminen, S and Ahokas, J (1998) Physicochemical alterations enhance the ability of dairy strains of lactic acid bacteria to remove aflatoxin from contaminated media. Journal of Food Protection 61, 466468.CrossRefGoogle ScholarPubMed
El-Nezami, H, Mykkanen, H, Kankaanpaa, P, Suomalainen, T, Salminen, S and Ahokas, J (2000) Ability of a mixture of Lactobacillus and Propionibacterium to influence the faecal aflatoxin content in healthy Egyptian volunteers: a pilot clinical study. Bioscience and Microflora 19, 4145.CrossRefGoogle Scholar
Elsanhoty, RM, Salam, SA, Ramadan, MF and Badr, FH (2014) Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control 43, 129134.CrossRefGoogle Scholar
ES Egyptian Standard (7136/2010) Maximum Levels of for Certain Contaminants in Foodstuffs. Annex Section 2: Mycotoxins. Cairo, Egypt: Egyptian Organization for Standardization and Quality.Google Scholar
Faizan, AS, Bowen, Y, Fengwei, T, Jianxin, Z, Hao, Z and Wei, C (2019) LAB as antifungal and anti-mycotoxigenic agents: a comprehensive review. Comprehensive Reviews in Food Science and Food Safety 18, 14031436.Google Scholar
GadAllah, AH, Abou Zied, MA and Fahim, MK (2020) Risk profile of some food safety hazards associated with ice-cream sold in Egypt. International Journal of Dairy Science 15, 123133.CrossRefGoogle Scholar
Hashemi, SM and Amiri, MJ (2020) A comparative adsorption study of aflatoxin B1 and aflatoxin G1 in almond butter fermented by Lactobacillus fermentum and Lactobacillus delbrueckii subsp. lactis. LWT 128, 109500.CrossRefGoogle Scholar
Haskard, CA, El-Nezami, HS, Kankaanpää, PE, Salminen, S and Ahokas, JT (2001) Surface binding of aflatoxin B1 by lactic acid bacteria. Applied and Environmental Microbiology 67, 30863091.CrossRefGoogle ScholarPubMed
Huang, L, Duan, C, Zhao, Y, Gao, L, Niu, C, Xu, J and Li, S (2017) Reduction of aflatoxin B1 toxicity by Lactobacillus plantarum C88: a potential probiotic strain isolated from Chinese traditional fermented food ‘tofu’. PLoS One 12, 0170109.Google Scholar
IARC ‘International Agency of Research on Cancer’ (2002) Monograph on the evaluation of carcinogenic risks to humans. WHO-International Agency for Research on Cancer, Lyon, France 82, 171275.Google Scholar
Meucci, V, Razzuoli, E, Soldani, G and Massart, F (2009) Mycotoxin detection in infant formula milks in Italy. Food Additives and Contaminants 27, 6471.CrossRefGoogle Scholar
Mohammedi-Ameur, S, Dahmane, M, Brera, C, Kardjadj, M and Ben-Mahdi, MH (2020) Occurrence and seasonal variation of aflatoxin M1 in raw cow milk collected from different regions of Algeria. Veterinary World 13, 433439.CrossRefGoogle ScholarPubMed
Mohammadi, R, Abbaszadeh, S, Sharifzadeh, A, Sepandi, M, Taghdir, M, Miri, NY and Parastouei, K (2021) In vitro activity of encapsulated lactic acid bacteria on aflatoxin production and growth of Aspergillus spp. Food Science and Nutrition 9, 12821288.CrossRefGoogle ScholarPubMed
Moradi, M, Molaei, R and Guimarães, JT (2021) A review on preparation and chemical analysis of postbiotics from lactic acid bacteria. Enzyme and Microbial Technology 143, 109722.CrossRefGoogle ScholarPubMed
Moretti, A, Logrieco, AF and Susca, A (2017) Mycotoxins: an underhand food problem. Methods in Molecular Biology 1542, 312Google ScholarPubMed
Morsy, KH, Saif-Al-Islam, M and Ibrahim, EM (2018) Hepatocellular carcinoma in upper Egypt: a retrospective study. ARC Journal of Hepatology and Gastroenterology 3, 817.Google Scholar
Muaz, K and Riaz, M (2021) Decontamination of aflatoxin M1 in milk through integration of microbial cells with sorbitan monostearate, activated carbon and bentonite. The Journal of Animal & Plant Sciences 31, 235245.Google Scholar
Murshed, S (2020) Evaluation and assessment of aflatoxin M1 in milk and milk products in Yemen using high-performance liquid chromatography. Journal of Food Quality 2020, 8839060.CrossRefGoogle Scholar
Negera, M and Washe, AP (2019) Use of natural dietary spices for reclamation of food quality impairment by aflatoxin. Journal of Food Quality 2019, 4371206.CrossRefGoogle Scholar
Ren, X, Zhang, Q, Zhang, W, Mao, J and Li, P (2020) Control of aflatoxigenic molds by antagonistic microorganisms: inhibitory behaviors, bioactive compounds, related mechanisms, and influencing factors. Toxins 12, 24.CrossRefGoogle ScholarPubMed
Russo, P, Arena, MP, Fiocco, D, Capozzi, V, Drider, D and Spano, G (2017) Lactobacillus plantarum with broad antifungal activity: a promising approach to increase safety and shelf-life of cereal-based products. International Journal of Food Microbiology 247, 4854.CrossRefGoogle ScholarPubMed
Sani, MA, Khezri, M and Moradnia, H (2012) Determination of aflatoxin in milk by ELISA technique in Mashad (Northeast of Iran). ISRN Toxicology 2012, 121926.Google Scholar
Shah, NP (2007) Functional cultures and health benefits. International Dairy Journal 17, 12621277.CrossRefGoogle Scholar
Shehata, MG, Badr, AN and El Sohaimy, SA (2018) Novel antifungal bacteriocin from Lactobacillus paracasei KC39 with anti-mycotoxigenic properties. Bioscience Research 15, 41714183.Google Scholar
Shehata, MG, Badr, AN, El Sohaimy, SA, Asker, D and Awad, TS (2019) Characterization of antifungal metabolites produced by novel lactic acid bacterium and their potential application as food biopreservatives. Annals of Agricultural Sciences 64, 7178.CrossRefGoogle Scholar
Shetty, PH, Hald, B and Jespersen, L (2007) Surface binding of aflatoxin B1 by Saccharomyces cerevisiae strains with potential decontaminating abilities in indigenous fermented foods. International Journal of Food Microbiology 113, 4146.CrossRefGoogle ScholarPubMed
Suresh, G, Cabezudo, I, Pulicharla, R, Cuprys, A, Rouissi, T and Kaur Brar, S (2020) Biodegradation of aflatoxin B1 with cell-free extracts of Trametes versicolor and Bacillus subtilis. Research in Veterinary Science 133, 8591.CrossRefGoogle ScholarPubMed
USA/FDA ‘Food and Drug Administration’ (2005) CPG Sec. 527.400 Whole Milk, Low Fat Milk, Skim Milk–Aflatoxin M1. Rockville, MD, USA: Silver Spring.Google Scholar
Zhang, LY, Liu, S, Zhao, XJ, Wang, N, Jiang, X, Xin, HS and Zhang, YG (2019) Lactobacillus rhamnosus GG modulates gastrointestinal absorption, excretion patterns, and toxicity in Holstein calves fed a single dose of aflatoxin B1. Journal of Dairy Science 102, 13301340.CrossRefGoogle ScholarPubMed
Zhao, H, Shao, D, Jiang, C, Shi, J, Li, Q, Huang, Q, Rajoka, MSR, Yang, H and Jin, M (2017) Biological activity of lipopeptides from Bacillus. Applied Microbiology and Biotechnology 101, 59515960.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Mogahed Fahim et al. supplementary material

Mogahed Fahim et al. supplementary material

Download Mogahed Fahim et al. supplementary material(PDF)
PDF 248 KB