Research Article | Volume: 12, Issue: 8, August, 2022

Protective impact of encapsulated probiotics and Ziziphus spinachristi against liver oxidative stress and DNA damage induced by aflatoxin M1

Ahmed N. Badr Karem Fouda Rasha S. Mohamed Abdel-Razek H. Farag Ahmed H. Zaghloul Ahmed M. Abdel-Salam   

Open Access   

Published:  Mar 30, 2022

DOI: 10.7324/JAPS.2022.120809

Dairy products are exposed to contamination by aflatoxin M1 (AFM1) directly or by cross-contamination with aflatoxin B1. Strategies applied to reduce their impacts include probiotics and prebiotics. Zizyphus (Ziziphus spina-christi) fruit contains bioactive compounds that may act as prebiotics. The objective of this research was to discover what function encapsulated probiotics, Zizyphusz fruit, and their combination play in preventing oxidative liver damage and genotoxicity in rats. Probiotics (Streptococcus thermophilus, Lactobacillus acidophilus,, and Bifidobacterium bifidum) and Zizyphusz were encapsulated separately using a soy protein concentrate and maltodextrin as carriers. Encapsulated probiotics and Zizyphusz as well as their combination with camel milk were evaluated in both normal and AFM1 -exposed rats. Biochemical alterations and histological changes were determined. Also, DNA damage was assessed by the comet assay protocol. At the studied doses, the encapsulated probiotics (2.7 × 1011 CFU/ml) and Zizyphusz (1 mg) reduced the elevation of liver functions, oxidative marker (malondialdehyde), inflammatory marker (tumor necrosis factor-alphaα), and DNA damage in rats exposed to AFM1. Possibly, the encapsulated probiotics or Zizyphusz can effectively protect the liver from oxidative stress and DNA damage caused by AFM1 .

Keyword:     Aflatoxin M1 DNA damage encapsulation probiotic Zizyphusz fruit


Badr A, Fouda K, Mohamed R, Farag AR, Zaghloul A, AbdelSalam A. Protective impact of encapsulated probiotics and Ziziphus spina-christi against liver oxidative stress and DNA damage induced by aflatoxin M1 . J Appl Pharm Sci, 2022; 12(08):082–094.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

HTML Full Text


Abdel-Fattah SM, Badr AN, Seif FAHA, Ali SM, Hassan RA. Antifungal and anti-mycotoxigenic impact of eco-friendly extracts of wild stevia. J Biol Sci, 2018; 18(8):488-99.

Abdel-Salam AM, Badr AN, Zaghloul AH, Farrag ARH. Functional yogurt aims to protect against the aflatoxin B1 toxicity in rats. Toxicol Rep, 2020; 7:1412-20.

Afshar P, Shokrzadeh M, Raeisi SN, Ghorbani-HasanSaraei A, Nasiraii LR. Aflatoxins biodetoxification strategies based on probiotic bacteria. Toxicon, 2020.

Badr AN, Gromadzka K, Shehata MG, Stuper-Szablewska K, Drzewiecka K, Abdel-Razek AG, Youssef MM. Encapsulated Bioactive Ingredients of grape by-products applicate in fresh-cut fruit and juices diminished the ochratoxins. J Food Process Preserv, 2021a; 45(2):e15112.

Badr AN, Youssef M, Abdel-Razek AG, Shehata MG, Hassanien MM, Amra H. Natural antioxidants: preservation roles and mycotoxicological safety of food. Egypt J Chem, 2021b; 64(1):285-98.

Beers RF, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biolo Chem, 1952; 195(1):133-40.

Ben Salah-Abbès J, Abbès S, Jebali R, Haous Z, Oueslati R. Potential preventive role of lactic acid bacteria against aflatoxin M- immunotoxicity and genotoxicity in mice. J Immunotoxicol, 2015; 12(2):107-14.

Ben Salah-Abbès J, Belgacem H, Ezdini K, Mannai M, Oueslati R, Abbès S. Immunological effects of AFM1 in experimental subchronic dosing in mice prevented by lactic acid bacteria. Immunopharmacol Immunotoxicol, 2020; 42(6):572-81.

Benkerroum N. Chronic and acute toxicities of aflatoxins: mechanisms of action. Int J Environ Res Public Health, 2020; 17(2):423.

Bessey OA, Lowry OH, Brock MJ. A method for the rapid determination of alkaline phosphates with five cubic millimeters of serum. J Biol Chem, 1946; 164:321-9.

Betts CA, Stuart B. Determination of serum total ironbinding capacity. J Clin Pathol, 1973; 26(6):457.

Blasiak J, Arabski M, Krupa R, Wozniak K, Zadrozny M, Kasznicki J, Zurawska M, Drzewoski J. DNA damage and repair in type 2 diabetes mellitus. Mutat Res, 2004; 554(1):297-304.

Cavalcante Caetano M, Ortiz Ortiz TT, Lopes Da Silva SG, Suano De Souza FI, Saccardo Sarni ROJR. Complementary feeding: inappropriate practices in infants. Rev Chil Pediatr, 2012; 83(5):503.

Cencic A, Chingwaru W. The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients, 2010; 2(6):611-25.

Collins A, Dušinská M, Franklin M, Somorovská M, Petrovská H, Duthie S, Fillion L, Panayiotidis M, Rašlová K, Vaughan N. Comet assay in human biomonitoring studies: Reliability, validation, and applications. Environ Mol Mutagen, 1997; 30:139-46.<139::AID-EM6>3.0.CO;2-I

BT, Watson WA, Biggs HG. Albumin standards and the measurement of serum albumin with bromcresol green. Clinica Chimica Acta, 1997; 258(1):21-30.

Drabkin DL. The standardization of hemoglobin measurement. Am J Med Sci, 1949; 292:386-99.

El-Hefny M, Mohamed AA, Salem MZM, Abd El-Kareem MSM, Ali HM. Chemical composition, antioxidant capacity and antibacterial activity against some potato bacterial pathogens of fruit extracts from Phytolacca dioica and Ziziphus spina-christi grown in Egypt. Sci Hortic, 2018; 233:225-32.

Fawcett JK, Scott JE. A rapid and precise method for the determination of Urea. J Clin Pathol, 1960; 13(2):156-9.

Kamyar S, Movassaghghazani M. Reduction of aflatoxin m1 in milk using kefir starter. Iran J Toxicol, 2017; 11(6):27-31.

Kao TH, Chen BH. Functional components in zizyphus with emphasis on polysaccharides, in polysaccharides: bioactivity and biotechnology. In: Ramawat KG, Mérillon JM (eds.). Springer International Publishing Cham, Switzerland, pp 795-827, 2015.

Khadivi R, Razavilar V, Anvar A, Akbari-adergani B. Aflatoxin M1-binding ability of selected lactic acid bacteria strains and Saccharomyces boulardii in the experimentally contaminated milk treated with some biophysical factors. Arch Razi Inst, 2020; 75(1):63-73.

Khorshidian N, Yousefi Asli M, Hosseini H, Shadnoush M, Mortazavian AM. Potential anticarcinogenic effects of lactic acid bacteria and probiotics in detoxification of process-induced food toxicants. Iran J Cancer Prev, 2016; 9(5):1-13.

Kumar P, Mahato DK, Kamle M, Mohanta TK, Kang SG. Aflatoxins: a global concern for food safety, human health and their management. Front Microbiol, 2017; 7:2170.

Larsen K. Creatinine assay by a reaction-kinetic principle. Clinica Chimica Acta, 1972; 41:209-17.

Li H, Xing L, Zhang M, Wang J, Zheng N. The toxic effects of aflatoxin B1 and aflatoxin M1 on kidney through regulating l-proline and downstream apoptosis. BioMed Res Int, 2018; 2018:9074861.

Loi M, Paciolla C, Logrieco AF, Mulè G. Plant bioactive compounds in pre- and postharvest management for aflatoxins reduction. Front Microbiol, 2020; 11:243.

Mahmood Fashandi H, Abbasi R, Mousavi Khaneghah A. The detoxification of aflatoxin M1 by Lactobacillus acidophilus and Bifidobacterium spp.: a review. J Food Process Preserv, 2018; 42(9):e13704.

Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L. Aflatoxin B1 and M1: biological properties and their involvement in cancer development. Toxins, 2018; 10(6):214.

Messina A, Luce E, Hussein M, Dubart-Kupperschmitt A. Pluripotent-stem-cell-derived hepatic cells: hepatocytes and organoids for liver therapy and regeneration. Cells, 2020; 9(2):420.

Montgomery HAC, Dymock JF. The determination of nitrite in water. Analyst, 1961; 86:414-6.

Nishikimi M, Rao NA, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun. 1972; 46(2):849-54.

Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 1979; 95(2):351-8.

DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med, 1967; 70(1):158-69.

Pandey KR, Naik SR, Vakil BV. Probiotics, prebiotics and synbiotics- a review. J Food Sci Technol, 2015; 52(12):7577-87.

Rasheed Z. Medicinal values of bioactive constituents of camel milk: a concise report. Int J Health Sci, 2017; 11(5):1-2.

Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76a rodent diet. J Nutr, 1993; 123(11):1939-51.

S, Frankel S. A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am J Clin Pathol, 1957; 28(1):56-63.

Rheinhold J, Seligron D. Total protein, albumin and globulin in standard methods of clinical chemistry. J Academic press, Inc., New York, NY, 88 p, 1953.

Saha Turna N, Wu F. Aflatoxin M1 in milk: a global occurrence, intake, & exposure assessment. Trends Food Sci Technol, 2021; 110:183- 92.

Samedi L, Charles AL. Viability of 4 probiotic bacteria microencapsulated with arrowroot starch in the simulated gastrointestinal tract (GIT) and yoghurt. Foods, 2019; 8(5):175.

Shirani K, Riahi Zanjani B, Mehri S, Razavi-Azarkhiavi K, Badiee A, Hayes AW, Giesy JP, Karimi G. miR-155 influences cell-mediated immunity in Balb/c mice treated with aflatoxin M1. Drug Chem Toxicol, 2021; 44(1):39-46.

Shirani K, Zanjani BR, Mahmoudi M, Jafarian AH, Hassani FV, Giesy JP, Karimi G. Immunotoxicity of aflatoxin M1: as a potent suppressor of innate and acquired immune systems in a subacute study. J Sci Food Agric, 2018; 98(15):5884-92.

Stookey LL. Ferrozine--a new spectrophotometric reagent for iron. Anal Chem, 1970; 42(7):779-81.

Szasz G. A kinetic photometric method for serum γ-glutamyl transpeptidase. Clin Chem, 1969; 15(2):124-36.

Var I, Kabak B. Removal of aflatoxins by viable and heat-killed lactic acid bacteria and bifidobacteria. Archiv Für Lebensmittelhygiene, 2004; 55(5):106-9.

Vaz A, Cabral Silva AC, Rodrigues P, Venâncio A. Detection methods for Aflatoxin M1 in dairy products. Microorganisms, 2020; 8(2):246.

Yousof SSM, El Zubeir IEM. Chemical composition and detection of Aflatoxin M1 in camels and cow's milk in Sudan. Food Addit Contam: Part B, 2020; 13(4):298-304.

Article Metrics

8 Absract views 4 PDF Downloads 12 Total views

   Abstract      Pdf Download

Related Search

By author names

Citiaion Alert By Google Scholar

Name Required
Email Required Invalid Email Address

Comment required