Effect of Different Extracts of Ganoderma lucidum on Ochratoxin A Formation by Aspergillus ochraceus

Document Type : Original paper

Authors

1 Food Science and Technology Department, Sciences and Research Branch, Islamic Azad University, Tehran, Iran.

2 Food and Drug Laboratory Research Center (FDLRC), Iran Food and Drug Administration (IFDA), MOHME, Tehran, Iran.

Abstract

Background and objectives: Mycotoxins are secondary metabolites produced by fungi contaminated agricultural products and have toxic effect in human and animals. Ochratoxin A is produced by many filamentous fungi species such as Aspergillus and Penicillium, and is classified as a possible carcinogen and nephrotoxic. Ganoderma lucidum is a famous mushroom with antifungal properties and probably preventive effect on toxin production. The aim of this study was to investigate the antitoxigenic properties of Iranian strain of G. lucidum as a natural antitoxigenic agent against harmful filamentous fungi in food industry. Methods: Different extracts of G. lucidum were prepared and the antifungal and antitoxigenic effects were studied on toxigenic Aspergillus ochraceus. Ethanolic, hydroalcoholic and aqueous extracts were prepared by cold maceration method and compared with commercial extracts. Ochratoxin A was analyzed by high performance liquid chromatography (HPLC) coupled with fluorescence detector in A. ochraceus culture media which was treated with the extracts. Results: The results expressed that the alcoholic extracts could inhibit fungal growth but the aqueous extracts were able to significantly prevent toxin production while the fungus totally grew. Conclusion: Ganoderma lucidum and its products, may be used as a pharmaceutical and nutraceutical mushroom and could be considered as safe and useful agents for prevention of fungal growth and mycotoxin formation in food and agricultural products.

Keywords


  • Ayofemi Olalekan Adeyeye S. Aflatoxigenic fungi and mycotoxins in food: a review. Crit Rev Food Sci Nutr. 2020; 60(5): 709–721.
  • Logrieco A, Battilani P, Leggieri MC, Jiang Y, Haesaert G, Lanubile A, Mahuku G, Mesterhazy A, Ortega-Beltran A, Pasti M, Smeu I, Torres A, Xu J, Munkvold G. Perspectives on global mycotoxin issues and management from the MycoKey Maize Working Group. Plant Dis. 2021; 105(3): 525–537.
  • Palumbo R, Crisci A, Venâncio A, Cortiñas Abrahantes J, Dorne JL, Battilani P, Toscano P. Occurrence and co-occurrence of mycotoxins in cereal-based feed and food. Microorganisms. 2020; 8(1): 1–17.
  • Van den Brand AD, Bulder AS. An overview of mycotoxins relevant for the food and feed supply chain: using a novel literature screening method. Netherlands: RIVM official reports, 2020.
  • Camardo Leggieri M, Giorni P, Pietri A, Battilani P. Aspergillus flavus and Fusarium verticillioides interaction: modeling the impact on mycotoxin production. Front Microbiol. 2019; 10: 1–10.
  • Abarca ML, Accensi F, Bragulat MR, Cabañes FJ. Current importance of ochratoxin A–producing Aspergillus J Food Prot. 2001; 64(6): 903–906.
  • Ali BH, Hasan MS, Ibrahim ZY, Owain MS. Mycotoxins, detection and prevention, a review. Int J Pharm Res. 2020; 12(1): 1001–1010.
  • Schaarschmidt S, Fauhl‐Hassek C. The fate of mycotoxins during secondary food processing of maize for human consumption. Compr Rev Food Sci Food Saf. 2021; 20(1): 91–148.
  • El Khoury A, Atoui A. Ochratoxin a: general overview and actual molecular status. Toxins. 2010; 2(4): 461–493.
  • Onyedum SC, Adefolalu FS, Muhammad HL, Apeh DO, Agada MS, Imienwanrin MR, Makun HA. Occurrence of major mycotoxins and their dietary exposure in North-Central Nigeria staples. Sci Afr. 2020; 7: 1–9.
  • Battilani P, Palumbo R, Giorni P, Dall’Asta C, Dellafiora L, Gkrillas A, Toscano P, Crisci A, Brera C, De Santis B, Rosanna Cammarano R, Della Seta M, Campbell K, Elliot C, Venancio A, Lima N, Goncalves A, Terciolo C, Oswald IP. Mycotoxin mixtures in food and feed: holistic, innovative, flexible risk assessment modelling approach: MYCHIF. EFSA Support Publ. 2020; 17(1): 1–158.
  • Erceg S, Mateo EM, Zipancic I, Rodríguez Jiménez FJ, Pérez Aragó MA, Jiménez M, Miguel Soria J, Garcia-Esparza M. Assessment of toxic effects of ochratoxin A in human embryonic stem cells. Toxins. 2019; 11(4): 1–11.
  • Agriopoulou S, Stamatelopoulou E, Varzakas T. Advances in occurrence, importance, and mycotoxin control strategies: prevention and detoxification in foods. Foods. 2020; 9(2): 1–48.
  • Pakshir K, Mirshekari Z, Nouraei H, Zareshahrabadi Z, Zomorodian K, Khodadadi H, Hadaegh A. Mycotoxins detection and fungal contamination in black and green tea by HPLC-based method. J Toxicol. 2020; Article ID 2456210.
  • Tavakol Noorabadi M, Babaeizad V, Zare R, Asgari B, Haidukowski M, Epifani F, Gaetano S, Moretti A, Francesco Logrieco A, Susca A. Isolation, molecular identification, and mycotoxin production of Aspergillus species isolated from the rhizosphere of sugarcane in the south of Iran. Toxins. 2020; 12(2): 1–15.
  • Li LD, Mao PW, Shao KD, Bai XH, Zhou XW. Ganoderma proteins and their potential applications in cosmetics. Appl Microbiol Biotechnol. 2019; 103(23): 9239–9250.
  • Veljović S, Nikićević N, Nikšić M. Medicinal fungus Ganoderma lucidum as raw material for alcohol beverage production. Alcohol Beverage. 2019; 7: 161–197.
  • Islam MS, Rahi MS, Koli HK, Jerin I, Sajib SA, Hoque KMF, Reza MA. Evaluation of phytochemical, antioxidant, cytotoxicity and in vitro antibacterial activity of aqueous extract of Ganoderma lucidum cultivated in Bangladeshi habitat. Malaya J Biosci. 2018; 5(1): 1–13.
  • Arias-Londoño MA, Zapata-Ocampo PA, Mosquera-Arevalo AR, Sanchez-Torres JD, Atehortua-Garcés L. Antifungal protein determination for submerged cultures of the medicinal mushroom Ganoderma lucidum (Ganodermataceae) with activity over the phytopathogen fungus Mycosphaerella fijiensis (Mycosphaerellaceae). Actualidades Biológicas. 2019; 41(111): 53–64.
  • Heleno SA, Ferreira ICFR, Esteves AP, Ćirić A, Glamočlija J, Martins A, Sokovic M, Queiroz MJRP. Antimicrobial and demelanizing activity of Ganoderma lucidum extract, p-hydroxybenzoic and cinnamic acids and their synthetic acetylated glucuronide methyl esters. Food Chem Toxicol. 2013; 58: 95–100.
  • Ogidi OC, Oyetayo VO. Phytochemical property and assessment of antidermatophytic activity of some selected wild macrofungi against pathogenic dermatophytes. Mycology. 2016; 7(1): 9–14.
  • Clinical and Laboratory Standards Institutes. Reference method for broth dilution antifungal susceptibility testing of filamentus fungi, M38A2. 3rd Pennsylvania: Clinical and Laboratory Standards Institutes, 2017.
  • Entwisle AC, Williams AC, Mann PJ, Slack PT, Gilbert J. Liquid chromatographic method with immunoaffinity column cleanup for determination of ochratoxin a in barley: collaborative study. J AOAC Int. 2000; 83(6): 1377–1383.
  • Leitner A, Zöllner P, Paolillo A, Stroka J, Papadopoulou-Bouraoui A, Jaborek S, Anklam E, Lindner W. Comparison of methods for the determination of ochratoxin a in wine. Anal Chim Acta. 2002; 453(1): 33–41.
  • Stojković DS, Barros L, Calhelha RC, Glamočlija J, Ćirić A, Van Griensven LJ, Sokovic M, Ferreira IC. A detailed comparative study between chemical and bioactive properties of Ganoderma lucidum from different origins. Int J Food Sci Nutr. 2014; 65(1): 42–47.
  • Soliman KM, Badeaa Effect of oil extracted from some medicinal plants on different mycotoxigenic fungi. Food Chem Toxicol. 2002; 40(11): 1669–1675.
  • Loncar J, Bellich B, Parroni A, Reverberi M, Rizzo R, Zjalić S, Cescutti P. Oligosaccharides derived from tramesan: their structure and activity on mycotoxin inhibition in Aspergillus flavus and Aspergillus carbonarius. Biomolecules. 2021; 11(2): 1–13.
  • Shen HS, Shao S, Chen JC, Zhou T. Antimicrobials from mushrooms for assuring food safety. Compr Rev Food Sci Food Saf. 2017; 16(2): 316–329.