Aflatoxins are highly toxic and carcinogenic metabolites produced by Aspergillus parasiticus on food and agricultural commodities. Natural products may control the production of aflatoxins. The aims of this study were to evaluate the effects of the essential oils (EOs) of Cuminum cyminum, Ziziphora clinopodioides, and Nigella sativa on growth and aflatoxins production by A. parasiticus. Minimal inhibitory concentrations (MICs) and minimal fungicidal concentrations (MFCs) of the EOs were determined and compared with each other. Determination of aflatoxins (AFB1, AFB2, AFG1, and AFG2) was performed by immunoaffinity column extraction using reverse phase-high performance liquid chromatography. The major oil components were α-pinene (30%) in C. cyminum, pulegone (37%) in Z. clinopodioides, and trans-anthol (38.9%) in N. sativa oils. In broth microdilution method, C. cyminum oil exhibited the strongest activity (MIC90: 1.6; MFC: 3.5 mg/mL), followed by Z. clinopodioides (MIC90: 2.1; MFC: 5.5 mg/mL) and N. sativa (MIC90: 2.75; MFC: 6.25 mg/mL) oils against A. parasiticus (p<0.05). Aflatoxin production was inhibited at 0.25 mg/mL of C. cyminum and Z. clinopodioides oils, of which that of C. cyminum was a stronger inhibitor. C. cyminum EO caused significant reductions in values of 94.2% for AFB1, 100% for AFB2, 98.9% for AFG1, 100% for AFG2, and 97.5% for total aflatoxin. It is concluded that the EOs of C. cyminum, Z. clinopodioides, and N. sativa could be used as natural inhibitors in foods at low concentrations to protect from fungal and toxin contaminations by A. parasiticus.
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References
1.
AghajaniZ, AssadianF, MasoudiS, ChalabianF, EsmaeiliA, Tabatabaei-AnarakiM, RustaiyanA. Chemical composition and in vitro antibacterial activities of the oil of Ziziphora clinopodioides and Z. capitata subsp. capitata from Iran. Chem Natr Comp, 2008; 44:387–389.
2.
[AOAC] Association of Analytical Communities. Natural toxins. Official Methods of AOAC International. TrucksessMW. Gaithersburg: MD, 2000; 34–37.
3.
Avicenna. Al-Qanun fi al Tibb (The Canon of Medicine)Persian Edition bySharaf-KandiAR. 1985Book II1st. Tehran: Soroush Press, 980–1037AD.
4.
BankoleSA. Effect of essential oils of two Nigerian medicinal plants (Azadirachta indica and Morinda lucida) on growth and aflatoxin B1 production in maize grain by a toxigenic Aspergillus flavus. Lett Appl Microbiol, 1997; 24:190–192.
5.
BansodS, RaiM. Antifungal activity of essential oils from Indian medicinal plants against human pathogenic Aspergillus fumigatus and A. niger. World J Med Sci, 2008; 3:81–88.
6.
BathnagarD, GarciaS. Aspergillus. Guide to Foodborne Pathogens. LabbéRG, GarcíaS. New York: John Wiley and Sons, 2001; 35–49.
7.
BaydarH, SagdicO, OzcanG, KaradoganT. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Contr, 2004; 15:169–172.
8.
BehravanJ, RamezaniM, HassanzadehMK, EskandariM, KasaianJ, SabetiZ. Composition, antimycotic and antibacterial activity of Ziziphora clinopodioides Lam. essential oil from Iran. J Essential Oil Bearing Plants, 2007; 10:339–345.
9.
BhatnagarD, ClevelandTE. Genetics and biochemistry of aflatoxin formation and genomics approach for eliminating aflatoxin contamination. Recent Advance in Phytochemistry: Secondary Metabolism in Model Systems, 38RemeoJT. London: Academic Press, 2004; 224–242.
10.
BrunetonJ. Pharmacognosy, Phytochemistry of Medicinal Plants. Andover: Intercept Ltd., 1995.
11.
ClevelandTE, DowdPF, DesjardinsAE, BhatnagarD, CottyPJ. United States department of agriculture-agriculture research service research on pre-harvest prevention of mycotoxin and mycotoxigenic fungi in US crops. Pest Manage Sci, 2003; 59:629–642.
12.
[CLSI] Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Conidium-Forming Filamentous Fungi. Approved Standard M38-A: Wayne, 2002.
DaviesNW. Gas chromatographic retention index of monoterpenes and sesquiterpenes on methyl silicone and carbowax 20 M phases. J Chromatograph, 1998; 503:1–24.
15.
GachkarL, YadegariD, RezaeiMB, TaghizadehM, AstanehSA, RasooliI. Chemical and biological characteristics of Cuminum cyminum and Rosmarinus officinalis essential oils. Food Chem, 2007; 102:898–904.
16.
GeorgiannaDR, PayneGA. Genetic regulation of aflatoxin biosynthesis: from gene to genome. Fungal Genet Biol, 2009; 46:113–125.
17.
HammerKA, CarsonCF, RileyTV. Antifungal activity of the components of Melaleuca alternifolia (tea tree) oil. J Appl Microbiol, 2003; 95:853–860.
18.
IacobellisNS, Lo CantoreP, CapassoF, SenatoreF. Antibacterial activity of Cuminum cyminum L. and Carum carvi L. essential oils. J Agri Food Chem, 2005; 53:57–61.
19.
IheshiulorOOM, EsonuBO, ChuwukaOK, OmedeAA, OkoliIC, OgbuewuIP. Effects of mycotoxins in animal nutrition. Asian J Anim Sci, 2011; 5:19–33.
20.
KhosraviAR, MinooeianhaghighiMH, ShokriH, EmamiSA, AlaviSM, AsiliJ. The potential inhibitory effect of Cuminum cyminum, Ziziphora clinopodioides and Nigella sativa essential oils on the growth of Aspergillus fumigatus and Aspergillus flavus. Braz J Microbiol, 2011; 42:216–224.
21.
KumarR, MishraAK, DubeyNK, TripathiYB. Evaluation of Chenopodium ambrosioides as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. Int J Food Microbiol, 2007; 115:159–164.
22.
MarzougHNB, RomdhaneM, LebrihiA, MathieuF, CoudercF, AbderrabaM, KhoujaML, BouajilaJ. Eucalyptus oleosa essential oils: chemical composition and antimicrobial and antioxidant activities of the oils from different plant parts (stems, leaves, flowers and fruits)Molecules, 2011; 16:1695–1709.
23.
NaeiniA, KhosraviAR, ChitsazM, ShokriH, KamlnejadM. Anti-Candida albicans activity of some Iranian herbs used in traditional medicine. J Mycol Méd, 2009; 19:168–172.
24.
NamaziM, AllamehA, AminshahidiM, NoheeA, MalekzadehF. Inhibitory effects of ammonia solution on growth and aflatoxin production by Aspergillus parasiticus NRRL-2999. Acta Poloniae Toxicol, 2002; 10:65–72.
25.
NickavarB, MojabF, JavidniaK, Roodgar-AmoliMA. Chemical composition of the fixed and volatile oils of Nigella sativa L. from Iran. Z Naturforsch, 2003; 58:629–631.
26.
OzturkS, ErcisliS. Antibacterial activity and chemical constitutions of Ziziphora clinopodioides. Food Contr, 2007; 18:535–540.
27.
PatkarKL, UshaCM, ShettyHS, PasterN, LaceyJ. Effect of spice essential oil on growth and aflatoxin B1 production by Aspergillus flavus. Lett Appl Microbiol, 1993; 17:49–51.
28.
PolatU, YesilbagD, ErenM. Serum biochemical profile of broiler chickens fed diets containing rosemary and rosemary volatile oil. J Biol Environ Sci, 2011; 5:23–30.
29.
RasooliI, Razzaghi-AbyanehM. Inhibitory effects of thyme oils on growth and aflatoxin production by Aspergillus parasiticus. Food Contr, 2004; 1:479–483.
30.
Razzaghi-AbyanehM, Shams-GhahfarokhiM, EslamifarA, SchmidtOJ, GharebaghiR, KarimianM, NaseriA, SheikhiM. Inhibitory effects of Akacid®plus on growth and aflatoxin production by Aspergillus parasiticus. Mycopathologia, 2006; 161:245–249.
31.
Razzaghi-AbyanehM, Shams-GhahfarokhiM, YoshinariT, RezaeeMB, JaimandK, NagasawaH, SakudaS. Inhibitory effects of Satureja hortensis L. essential oil on growth and aflatoxin production by Aspergillus parasiticus. Int J Food Microbiol, 2008; 123:228–233.
32.
ReddyKRN, NurdijatiSB, SallehB. An overview of plant-derived products on control of mycotoxigenic fungi and mycotoxins. Asian J Plant Sci, 2010; 9:126–133.
SakudaS, OnoM, IkedaH, NakamuraT, InagakiY, KawachiR, NakayamaJ, SuzukiA, IsogaiA, NagasawaH. Blasticidin A as an inhibitor of aflatoxin production by Aspergillus parasiticus. J Antibiotics, 2000; 68:407–412.
35.
SalmanMT, KhanRA, ShuklaI. Antimicrobial activity of Nigella sativa Linn. seed oil against multi-drug resistant bacteria from clinical isolates. Natl Prod Radiat, 2008; 7:10–14.
36.
ShuCK, LawrenceBM. Reasons for the variation in composition of some commercial essential oils. ACS Symposium Series: Vol. 660. Spices, Flavor Chemistry and Antioxidant Properties. RischSJ, HoCT. Washington, DC: American Chemical Society, 1997; 138–159.
37.
TadjbakhshH. History of Human and Veterinary Medicine in Iran. Lion: Merial Co, 2003.
38.
VardonPJ. Mycotoxins: Risks in Plant, Animal and Human Systems, Potential Economic Costs of Mycotoxins in the United States. Wayne, PA: Cast Task Force, 2003; 136–142.
39.
WilliamsJH, PhillipsTD, JollyP, StylesJK, JollyCM, AggarwalD. Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr, 2004; 80:1106–1122.
40.
YahyaraeyatR, KhosraviAR. The Effect of Oil Extracted from Zataria multiflora on Aflatoxin Genes Expression in Aspergillus parasiticus. Ph.D. Thesis, University of Tehran: Iran, 2010.
41.
YoshinariT, AkiyamaT, NakamuraK, KondoT, TakahashiY, MuraokaY, NonomuraY, NagasawaH, SakudaS. Dioctatin A is a strong inhibitor of aflatoxin production by Aspergillus parasiticus. Microbiology, 2007; 153:2774–2780.
