Investigating the Inhibitory Effect of Turmeric Extract in Reducing Aflatoxin Production by Aspergillus flavus and Aspergillus parasiticus

Shokoufeh Sharokhi Rezaei ¹ ( )
Leila Nouri ² ( )
Mansooreh Mazaheri ³ ( )
Laleh Adlnasab ⁴ ( )

Submited date : 2024-09-03 Accepted date : 2025-01-19

Keywords: Aflatoxins, Aspergillus flavus, Aspergillus parasiticus, Mycotoxins, Pistachio, Turmeric extract,

Abstract :

The consumption of pistachios (Pistacia vera L.) has been increasing due to their significant contribution to human health. Apart from being a valuable nutritional resource, they have been linked to potential chemical risks, including mycotoxins, which can lead to fungal contamination and secondary metabolism. In this study, after optimizing the extraction of turmeric extract based on the amount of total phenol and flavonoid compounds, treatments were applied using different concentrations of turmeric extract to assess its impact on the growth of Aspergillus flavus and Aspergillus parasiticus, and aflatoxin production. The treatments included various concentrations of turmeric extract and were implemented in a completely randomized design with three replications for each treatment. Results showed that the ultrasonic extraction method at 50 ºC for 60 minutes yielded the highest efficiency of turmeric extract. Specifically, the application of 300 μL turmeric extract significantly inhibited the mycelial growth of Aspergillus flavus, while 350 μL extract was more effective in inhibiting the growth of Aspergillus parasiticus. Furthermore, incubating both fungi with turmeric extract at 25°C for 3 days demonstrated a notable inhibitory effect on aflatoxin production. Additionally, the addition of turmeric extract to pistachios contaminated with both fungi effectively prevented aflatoxin production. Therefore, turmeric extract, particularly at concentrations of 300 μL and 350 μL, shows potential as a natural compound for preventing aflatoxin production in pistachios.

References:

Baum L, Ng A (2004) Curcumin interaction with copper and iron suggests one possible mechanism of action in Alzheimer's disease animal models. Journal of Alzheimer's Disease. 6(4), 367-77; https://doi.org/ 10.3233/JAD-2004-6403
Brown KL, Bren U, Stone MP, Guengerich FP (2009) Inherent stereospecificity in the reaction of aflatoxin B (1) 8,9-epoxide with deoxyguanosine and efficiency of DNA catalysis. Chemical Research in Toxicology. 22(5), 913-917. https://doi.org/10.1021/tx900002g
Cheng GW, Liang, HL, Chen, X, Zhang, Y (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis. 10(3), 178-182. https://doi.org/10.38212/2224-6614.2748
Clinical and Laboratory Standards Institute (CLSI) (2006) Performance Standards for Antimicrobial Susceptibility Testing; 16th Informational Supplement. CLSI document M100-S16. Wayne, PA: Clinical and Laboratory Standards Institute.
Colovic R, Puvaca N, Cheli F, Avantaggiato G, Greco D, Đuragic O, Kos J, Pinotti L (2019) Decontamination of mycotoxin-contaminated feedstuffs and compound feed. Toxins. 11, 617. https://doi.org/10.3390/toxins11110617
Dai C, Ciccotosto GD, Cappai R, Tang S, Li D, Xie S, Xiao X, Velkov T (2018) Curcumin attenuates colistin-induced neurotoxicity in N2a cells via anti-inflammatory activity, suppression of oxidative stress, and apoptosis. Molecular Neurobiology. 55, 421–434. https://doi.org/ 10.1007/s12035-016-0276-6
Gul P, Bakht J (2015) Antimicrobial activity of turmeric extract and its potential use in food industry. Journal of Food Science and Technology 52, 2272-2279. https://doi.org/ 10.1007/s13197-013-1195-4
Gupta SC, Prasad S, Kim JH, Patchva S, Webb LJ, Priyadarsini IK, Aggarwal BB (2011) Multitargeting by curcumin as revealed by molecular interaction studies. Natural Product Reports. 28(12), 1937-1955. https://doi.org/ 10.1039/c1np00051a
Habibi A, Yazdani N, Chatrabnous N, Koushesh Saba M, Vahdati K (2022) Inhibition of browning via aqueous gel solution of Aloe vera: a new method for preserving fresh fruits as a case study on fresh kernels of Persian walnut. Journal of Food Science and Technology 59, 2784–2793.
Habibi A, Yazdani N, Koushesh Saba M, Chatrabnous N, Molassiotis A, Sarikhani S, Vahdati K (2023) Natural preservation and improving lipid oxidation inhibition of fresh walnut. Horticulture, Environment, and Biotechnology. 64, 133–142.
Igas A, Wang C, Yang Y (2021) Ultrasonic-assisted extraction of curcumin from turmeric powder using ethanol and methanol solutions. Chemical and Biological Technologies in Agriculture. 9, 77-83. https://doi.org/10.1186/s40538-021-00234-7
INSO 5875: Preservatives, Determination of minimum Inhibitory concentration (MIC) - Microbiological test method- 2003.
INSO 5925, 2020. Food and feed, Maximum tolerated level of mycotoxins.
ISIRI 6872, 2013. Food and feed stuffs, determination of aflatoxins B&G by HPLC method using immunoaffinity column clean up-Test method
Jahanbani R, Bahramnejad E, Rahimi N, Shafaroodi H, Sheibani N, Moosavi-Movahedi AA, Dehpour A, Vahdati K (2021) Anti-seizure effects of walnut peptides in mouse models of induced seizure: The involvement of GABA and nitric oxide pathways. Epilepsy Research, p.106727.
Khan R, Mohamad Ghazali F, Mahyudin NA, Samsudin NIP (2021) Aflatoxin biosynthesis, genetic regulation, toxicity, and control strategies: A review. Journal of Fungi. 7(8), 606. https://doi.org/ 10.3390/jof7080606
Kihal A, Rodriguez-Prado M, Godoy C, Cristofol C, Calsamiglia S (2020) In vitro assessment of the capacity of certain mycotoxin binders to adsorb some amino acids and water-soluble vitamins. Journal of Dairy Science. 103, 3125–3132. https://doi.org/10.3168/jds.2019-17591
Kohiyama CY, Ribeiro MMY, Mossini SAG, Bando E, da Costa CL, da Silva Bomfim NS, Nerilo SB, Rocha GH, Grespan R, Mikcha JMG, Machinski M Jr (2015) Antifungal properties and inhibitory effects upon aflatoxin production of Thymus vulgaris L. by Aspergillus flavus Link. Food Chemistry. 173, 1006-1010. https://doi.org/ 10.1016/j.foodchem.2014.10.100
Lam P, Cheung F, Tan HY, Wang N, Yuen MF, Feng Y (2016) Hepatoprotective effects of Chinese medicinal herbs: A focus on anti-inflammatory and anti-oxidative activities. International Journal of Molecular Sciences. 17, 465. https://doi.org/ 10.3390/ijms17040465
List PH, Schmidt PC (1989) Phytopharmaceutical Technology. CRC Press, Boca Raton.
Luis Miguel HG, Ricardo S, Ana P (2023) Extraction and concentration of plant extracts using rotary evaporator. Environmental Science and Pollution Research. 30(5), 285-292. https://doi.org/10.1007/s11356-022-23678-9
Mahbobinejhad Z, Aminian H, Ebrahimi L, Vahdati K (2019) Reduction of aflatoxin production by exposing Aspergillus flavus to CO2. Journal of Crop Protection 8(4), 441-448.
Massomo SMS (2020) Aspergillus flavus and aflatoxin contamination in the maize value chain and what needs to be done in Tanzania. Scientific African 10: e00606. https://doi.org/ 10.1016/j.sciaf. 2020.e00606
Mullaicharam A, Maheswaran A (2012) Pharmacological effects of curcumin. International Journal of Nutrition, Pharmacology, Neurological Diseases. 2(2), 92-99. https://doi.org/ 10.4103/2231-0738.95960
Nazhand A, Durazzo A, Lucarini M, Souto EB, Santini A (2020) Characteristics, occurrence, detection and detoxification of aflatoxins in foods and feeds. Foods. 9, 644. https://doi.org/ 10.3390/foods9050644
Nazoori F, ZamaniBahramabadi E, Rezaei H (2024) Effect of sun-drying and roasting on pistachio quality and health benefits. International Journal of Horticultural Science and Technology. 11(3), 299-308. https://doi.org/10.22059/IJHST.2023.358161.635
Nazoori F, ZamaniBahramabadi E, Mirdehghan H, Yousefi M (2022) Preharvest application of sulfur as pesticide on fresh hull and kernel of pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9(1), 117-129. https://doi.org/10.22059/IJHST.2021.313206.408
Negi PS, Jayaprakasha GK, Jagan Mohan Rao L, Sakariah KK (1999) Antibacterial activity of turmeric oil: a byproduct from curcumin manufacture. Journal of Agricultural and Food Chemistry 47(10), 4297-300. https://doi.org/ 10.1021/jf990308d
Nerilo SB, Rocha GHO, Bauab TM, Machinski PA, Machinski MJr (2016) Antifungal properties and inhibitory effects upon aflatoxin production by Zingiber officinale essential oil in Aspergillus flavus. International Journal of Food Science and Technology. 51, 286-292. https://doi.org/ 10.1111/ijfs.12950
Norozi M, ValizadehKaji B, Karimi R, Nikoogoftar Sedghi M (2019) Effects of foliar application of potassium and zinc on pistachio (Pistacia vera L.) fruit yield. International Journal of Horticultural Science and Technology. 6(1), 113-123. https://doi.org/ 10.22059/ijhst.2019.278757.286
Sharifkhah M, Bakhshi D, Pourghayoumi M, Abdi S, Hokmabadi H (2020) Effect of pollination time on yield and antioxidant properties of some pistachio cultivars. International Journal of Horticultural Science and Technology. 7(1), 51-58. https://doi. org/10.22059/ijhst.2020.285527.306
Singh K, Srichairatanakool S, Chewonarin T, Prommaban A, Samakradhamrongthai RS, Brennan MA, Brennan CS, Utama-ang N. (2022) Impact of Green Extraction on Curcuminoid Content, Antioxidant Activities and Anti-Cancer Efficiency (In Vitro) from Turmeric Rhizomes (Curcuma longa L.). Foods. 11(22), 3633.doi: 10.3390/foods11223633
Vyvoda Martos A, González A M, Pérez AC (2011) Determination of total phenolic compounds in extracts produced by maceration and ultrasound methods using Folin-Ciocalteu method. Journal of Food Science and Technology. 48(4), 345-352. https://doi.org/10.1007/s13197-011-0293-3.
Willenbacher E, Khan SZ, Mujica SCA, Trapani D, Hussain S, Wolf D, Willenbacher W, Spizzo G, Seeber A (2019) Curcumin: New insights into an ancient ingredient against cancer. International Journal of Molecular Sciences 20:1808. https://doi.org/10.3390/ijms20081808
Ye T, Yan H, Wang X, Zhao W, Tao F, Zhou Y (2023) Determination of four aflatoxins on dark tea infusions and aflatoxin transfers evaluation during tea brewing. Food Chemistry. 405, 134969. https://doi.org/ 10.1016/j.foodchem.2022.134969
Zhai K, Brockmüller A, Kubatka P, Shakibaei M, Büsselberg D (2020) Curcumin's Beneficial Effects on Neuroblastoma: Mechanisms, Challenges, and Potential Solution. Biomolecules. 10(1469), doi: 10.3390/biom10111469.
Zhang D, Yang Y, Yao B, Hu T, Ma Z, Shi W, Ye Y (2023) Curcumin inhibits Aspergillus flavus infection and aflatoxin production possibly by inducing ROS burst. Food Research International. 167, 112646. https://doi.org/10.1016/j.foodres.2023.112646