Aflatoxin B1 in the Iranian pistachio nut and decontamination methods: A systematic review

Main Article Content

Mohsen Mokhtarian
Hamid Tavakolipour
Foroud Bagheri
Carlos Augusto Fernandes Oliveira
Carlos Humberto Corassin
Amin Mousavi Khaneghah


Pistachio nut; Aflatoxin B1; Prevalence; Systematic review; Decontamination


This study aimed to summarize the occurrence of aflatoxin B1 (AFB1) in the various cultivars of the Persian pistachio nut and the decontamination techniques, with the aid of a systematic review and meta-analysis. In this regard, all published studies up to November 2019 among international and national databases were screened, resulting in 23 articles. According to the findings, the main aflatoxin identified in the pistachio nut was AFB1, with AFB1 concentrations in ~28% of the studies being ? 5 µg/kg, in ~35% of the studies being ? 10 µg/kg, and in ~37% of the studies being ? 10 µg/kg. Generally, in most studies (~72%), AFB1 content in pistachio cultivars was higher than the acceptable level proposed by the Iranian National Standard. Although several physical and chemical techniques for AFB1 reduction have been introduced, most of them are not safe and/or suitable for human consumption.

Abstract 46 | PDF Downloads 42 HTML Downloads 2 XML Downloads 0


Abdallah, M.F., Ameye, M., De Saeger, S., Audenaert, K. and Haesaert, G., 2018. Biological control of mycotoxigenic fungi and their toxins: An update for the pre-harvest approach. In: Mycotoxins-impact and management strategies. IntechOpen. Patrick Berka Njobeh and Francois Stepman, London, UK,
Abdallah, M.F., Audenaert, K., Lust, L., Landschoot, S., Bekaert, B., Haesaert, G., De Boevre, M. and De Saeger, S., 2020. Risk characterization and quantification of mycotoxins and their producing fungi in sugarcane juice: A neglected problem in a widely-consumed traditional beverage. Food Control 108: 106811.
Abdolshahi, A., Shabani, A.A., Mortazavi, S.A. and Marvdashti, L.M., 2018. Aflatoxin binding efficiency of Saccharomyces cerevisiae mannoprotein in contaminated pistachio nuts. Food Control 87: 17–21. foodcont.2017.12.008
Afshari, H., Talaie, A., Mohammadi Moghadam, M. and Panahi, B., 2009. Differences of elements in early splitting of pistachio nuts and the effect of phenolic compounds and gallic acid on rate. Journal of Horticulture Science 23: 10–17. [In Persian]
Afsharmanesh, H., Perez-Garcia, A., Zeriouh, H., Ahmadzadeh, M. and Romero, D., 2018. Aflatoxin degradation by Bacillus subtilis UTB1 is based on production of an oxidoreductase involved in bacilysin biosynthesis. Food Control 94: 48–55. https://doi. org/10.1016/j.foodcont.2018.03.002
Aghamohammadi, M., Hashemi, J., Kram, G.A. and Alizadeh, N., 2007. Enhanced synchronous spectrofluorimetric determination of aflatoxin B1 in pistachio samples using multivariate analysis. Analytica Chimica Acta 582: 288–294. aca.2006.09.014
Alshannaq, A. and Yu, J.-H., 2017. Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Research and Public Health 14: 632. https://doi. org/10.3390/ijerph14060632
Aydin, S. and Ulvi, M., 2019. Residue levels of pesticides in nuts and risk assessment for consumers. Quality Assurance and Safety of Crops & Foods 11: 539–548. QAS2018.1405
Bashiri, P., Hadad Khodaparast, M.H., Sedaghat, N., Tabatabaei Yazdi, F. and Nasiri Mohalati, M., 2013. The effects of solution ozone in water on aflatoxin reduction of O’hadi pistachio cultivar. Iranian Food Science and Technology Research Journal 9: 215–221. [In Persian]
Batrinou, A., Houhoula, D. and Papageorgiou, E., 2020. Rapid detec-tion of mycotoxins on foods and beverages with enzyme linked immunosorbent assay. Quality Assurance and Safety of Crops & Foods 12: 40–49.
Bensassi, F., Rhouma, A., Ghrab, M., Bacha, H. and Hajlaoui, M.R., 2010. Evaluation of cultivar susceptibility and storage periods towards aflatoxin B1 contamination on pistachio nuts. Mycotoxin Research 26: 199–203. s12550-010-0054-7
Campagnollo, F.B., Ganev, K.C., Khaneghah, A.M., Portela, J.B., Cruz, A.G., Granato, D., Corassin, C.H., Oliveira, C.A.F. and Sant’Ana, A.S., 2016. The occurrence and effect of unit operations for dairy products processing on the fate of aflatoxin M1: A review. Food Control 68: 310–329. foodcont.2016.04.007
Chegini, S., Behbodi, K., Javan Nikkhah, M. and Farzaneh, M., 2013. Study of the effects of Trichoderma isolates on prevent of fungal growth of Aspergillus flavus and aflatoxin reduction on pistachio. Journal of Biological Control Pests Plant Diseases 2: 71–79. [In Persian]
Chen, R., Ma, F., Li, P.-W., Zhang, W., Ding, X.-X., Zhang, Q., Li, M., Wang, Y.-R. and Xu, B.-C., 2014. Effect of ozone on aflatoxins detoxification and nutritional quality of peanuts. Food Chemistry 146: 284–288. foodchem.2013.09.059
Cheraghali, A., Yazdanpanah, H., Doraki, N., Abouhossain, G., Hassibi, M., Ali-Abadi, S., Aliakbarpoor, M., Amirahmadi, M., Askarian, A. and Fallah, N., 2007. Incidence of aflatoxins in Iran pistachio nuts. Food and Chemical Toxicology 45: 812–816.
Dargahi, R., Moradi, M., Fani, S.R. and Masoumi, H., 2014. Evaluation of aflatoxin B1 in different parts of pistachio fruit and effects of processing stages. Journal of Food Hygiene 4: 21–31. [In Persian]
Dini, A., Khazaeli, P., Roohbakhsh, A., Madadlou, A., Pourenamdari, M., Setoodeh, L., Askarian, A., Doraki, N., Farrokhi, H. and Moradi, H., 2013. Aflatoxin contamination level in Iran’s pistachio nut during the years 2009–2011. Food Control 30: 540–544.
Ehrlich, K.C., Kobbeman, K., Montalbano, B.G. and Cotty, P.J., 2007. Aflatoxin-producing Aspergillus species from Thailand. International Journal of Food Microbiology 114: 153–159.
European Commission, 2010. Amending regulation setting maximum levels, for certain contaminants in foodstuffs as regards aflatoxins. Official Journal of the European Union 1881- L50: 8–12.
FAO, 2016. FAOSTAT-Statistical Service, FAO, Rome.
Farzaneh, M., Shi, Z.-Q., Ghassempour, A., Sedaghat, N.,
Ahmadzadeh, M., Mirabolfathy, M. and Javan-Nikkhah, M., 2012. Aflatoxin B1 degradation by Bacillus subtilis UTBSP1 isolated from pistachio nuts of Iran. Food Control 23: 100–106.
Georgiadou, M., Dimou, A. and Yanniotis, S., 2012. Aflatoxin contamination in pistachio nuts: A farm to storage study. Food Control 26: 580–586. foodcont.2012.02.014
Haji Mohammadi, B., Ehrampoush, M.H., Hashemi, S., Khalatbari Limaki, S., Zare, F. and Taheri Soudejani, M., 2016. The effect of electron irradiation on aflatoxin B1 in pistachio production process inoculated with Aspergillus flavus. Journal of Toloo-e-Behdasht 16: 1–8. [In Persian]
Heshmati, A., Zohrevand, T., Khaneghah, A.M., Mozaffari Nejad, A.S. and Sant’Ana, A.S., 2017. Co-occurrence of aflatoxins and ochratoxin A in dried fruits in Iran: Dietary exposure risk assessment. Food and Chemical Toxicology 106: 202–208.
Hussein, H.S. and Brasel, J.M., 2001. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 167: 101–134.
Ijabadeniyi, O., Mbedla, A. and Ajayeoba, T., 2020. Microbiological quality and antimicrobial efficacy of combined oregano essential oil and acetic acid on fresh lettuce. Italian Journal of Food Science 32(2): 399-409.
ISIRI (Institute of Standard and Industrial Research of Iran), 2002. Maximum tolerated limits of mycotoxins in foods and feeds. National Standard No.5925. ISIRI, Karaj, Iran.
Khaneghah, A.M., Fakhri, Y., Gahruie, H.H., Niakousari, M. and Sant’Ana, A.S., 2019. Mycotoxins in cereal-based products during 24 years (1983–2017): A global systematic review. Trends in Food Science & Technology 91: 95–105. https://doi. org/10.1016/j.tifs.2019.06.007
Khaneghah, A.M., Fakhri, Y., Raeisi, S., Armoon, B. and Sant’Ana, A.S., 2018. Prevalence and concentration of ochratoxin A, zearalenone, deoxynivalenol and total aflatoxin in cereal-based products: A systematic review and meta-analy-sis. Food and Chemical Toxicology 118: 830–848. https://doi. org/10.1016/j.fct.2018.06.037
Khorasani, S., Azizi, M.H., Barzegar, M., Hamidi-Esfahani, Z. and Kalbasi-Ashtari, A., 2017. Inhibitory effects of cinnamon, clove and celak extracts on growth of Aspergillus flavus and its aflatox-ins after spraying on pistachio nuts before cold storage. Journal of Food Safety 37: e12383.
Kola, O., Hayo?lu, ?., Türko?lu, H., Par?ld?, E., Ak, B.E. and Akkaya, M.R., 2018. Physical and chemical properties of some pistachio varieties (Pistacia vera L.) and oils grown under irrigated and non-irrigated conditions in Turkey. Quality Assurance and Safety of Crops & Foods 10: 383–388. https://doi. org/10.3920/QAS2017.1152
Krska, R. and Molinelli, A., 2009. Rapid test strips for analysis of mycotoxins in food and feed. Analytical and Bioanalytical Chemistry 393: 67–71. s00216-008-2424-y
Kwa?niewska, K., Gadza?a-Kopciuch, R. and Cendrowski, K., 2015. Analytical procedure for the determination of zearalenone in environmental and biological samples. Critical Reviews in Analytical Chemistry 45: 119–130. 08347.2014.896731
Maragos, C. and Busman, M., 2010. Rapid and advanced tools for mycotoxin analysis: A review. Food Additives and Contaminants 27: 688–700.
Mehrnezhad, M.R. and Panahi, B., 2005. The influence of hull cracking on aflatoxin contamination and insect infestation in pistachio nuts. Entomology and Phytopathology 73: 105–123. [In Persian]
Mohammadi Moghadam, M., Afshari, H., Mohammadi Goltape, E., Hokmabadi, H. and Rad, S., 2011. Investigation of the effects of testa in reducing growth of Aspergillus flavus fungi aflatoxin and production of aflatoxin B1 in different cultivars of pistachio ker-
nel. Journal of Horticulture Science 25: 73–81. [In Persian] Mokhtarian, M., 2015. Thermodynamic study of a solar dryer
equipped with air recycle and uses it to modeling of pistachio drying process by using genetic algorithm and artificial neural network approaches. PhD dissertation. Islamic Azad University, pp. 1–205. [In Persian]
Mokhtarian, M., Tavakolipour, H. and Ashtari, A.K., 2017. Effects of solar drying along with air recycling system on physicochemical and sensory properties of dehydrated pistachio nuts. LWT 75: 202–209.
Mokhtarian, M., Tavakolipour, H. and Kalbasi-Ashtari, A., 2016. Energy and exergy analysis in solar drying of pistachio with air recycling system. Drying Technology 34: 1484–1500. https://
Mortazavi, A. and Tabatabai, F., 1998. Mycotoxins, pp. 1–206. [In Persian]
Mousavi Khaneghah, A., Fakhri, Y. and Sant’Ana, A.S., 2018. Impact of unit operations during processing of cereal-based products on the levels of deoxynivalenol, total aflatoxin, ochratoxin A, and zearalenone: A systematic review and meta-analysis. Food Chemistry 268: 611–624. foodchem.2018.06.072
Nabizadeh, S., Shariatifar, N., Shokoohi, E., Shoeibi, S., Gavahian, M., Fakhri, Y., Azari, A. and Khaneghah, A.M., 2018. Prevalence and probabilistic health risk assessment of aflatoxins B 1, B 2, G 1, and G 2 in Iranian edible oils. Environmental Science and Pollution Research 25: 35562–35570. https://doi. org/10.1007/s11356-018-3510-0
Ostadrahimi, A., Ashrafnejad, F., Kazemi, A., Sargheini, N., Mahdavi, R., Farshchian, M. and Mahluji, S., 2014. Aflatoxin in raw and salt-roasted nuts (pistachios, peanuts and walnuts) sold in markets of Tabriz, Iran. Jundishapur Journal of Microbiology 7: 1-4.
Pak-kish, Z. and Rahemi, M., 2005. The effect of gibberellic acid on reduced cracking of pistachio hull, aflatoxin, and quality of dried pistachio fruit. Journal of Science and Technology of Agriculture and Natural Resources 9: 69–78. [In Persian]
Panahirad, S., Zaare-Nahandi, F., Mohammadi, N., Alizadeh-Salteh, S. and Safaie, N., 2014. Effects of salicylic acid on Aspergillus flavus infection and aflatoxin B1 accumulation in pistachio (Pistacia vera L.) fruit. Journal of the Science of Food and Agriculture 94: 1758–1763. jsfa.6488
Pascale, M.N., 2009. Detection methods for mycotoxins in cereal grains and cereal products. Zbornik Matice srpske za prirodne nauke 117: 15–25.
Pereira, V., Fernandes, J. and Cunha, S., 2014. Mycotoxins in cereals and related foodstuffs: A review on occurrence and recent methods of analysis. Trends in Food Science & Technology 36: 96–136.
Pig?owski, M., 2019. Comparative analysis of notifications regarding mycotoxins in the Rapid Alert System for Food and Feed (RASFF). Quality Assurance and Safety of Crops & Foods 11: 725–735.
Rahaie, S., Emam-Djomeh, Z., Razavi, S. and Mazaheri, M., 2010a. Immobilized Saccharomyces cerevisiae as a potential aflatoxin decontaminating agent in pistachio nuts. Brazilian Journal of Microbiology 41: 82–90. S1517-83822010000100014
Rahaie, S., Razavi, S.H. and Emam Jomeh, Z., 2010b. The ability of Saccharomyces Cerevisiae strain in Aflatoxin reduction in Pistachio nuts. Journal of Food Science and Technology 7: 81–88. [In Persian]
Rahmani, J., Alipour, S., Miri, A., Fakhri, Y., Riahi, S.-M., Keramati, H., Moradi, M., Amanidaz, N., Pouya, R.H., Bahmani, Z. and Mousavi Khaneghah, A., 2018. The prevalence of aflatoxin M1 in milk of Middle East region: A systematic review, meta-analysis and probabilistic health risk assessment. Food and Chemical Toxicology 118: 653–666. https://doi. org/10.1016/j.fct.2018.06.016
RASFF, 2016. The Rapid Alert System for Food and Feed — Annual report. Available at: (Accessed November 2017).
Rastegar, H., Shoeibi, S., Yazdanpanah, H., Amirahmadi, M., Khaneghah, A.M., Campagnollo, F.B. and Sant’Ana, A.S., 2017. Removal of aflatoxin B1 by roasting with lemon juice and/or citric acid in contaminated pistachio nuts. Food Control 71: 279– 284.
Ros, E., 2010. Health benefits of nut consumption. Nutrients 2: 652– 682.
Rossi, C.N., Takabayashi, C.R., Ono, M.A., Saito, G.H., Itano, E.N., Kawamura, O., Hirooka, E.Y. and Ono, E.Y.S., 2012. Immunoassay based on monoclonal antibody for aflatoxin detection in poultry feed. Food Chemistry 132: 2211–2216.
Sakamoto, S., Putalun, W., Vimolmangkang, S., Phoolcharoen, W., Shoyama, Y., Tanaka, H. and Morimoto, S., 2018. Enzyme-linked immunosorbent assay for the quantitative/qualitative analysis of plant secondary metabolites. Journal of Natural Medicines 72: 32–42.
Serra, M.S., Pulles, M.B., Mayanquer, F.T., Vallejo, M.C., Rosero, M.I., Ortega, J.M. and Naranjo, L.N., 2018. Evaluation of the use of gamma radiation for reduction of aflatoxin B1 in corn (zea mays) used in the production of feed for broiler chickens. Journal of Agricultural Chemistry and Environment 7: 21.
Shakeri, P. and Fazaeli, H., 2016. Microbial contamination and con-centration of aflatoxin in pistachio by-product. Journal of Food Microbiology 3: 61–72. [In Persian]
Siahmoshteh, F., Siciliano, I., Banani, H., Hamidi-Esfahani, Z., Razzaghi-Abyaneh, M., Gullino, M.L. and Spadaro, D., 2017. Efficacy of Bacillus subtilis and Bacillus amyloliquefaciens in the control of Aspergillus parasiticus growth and aflatoxins produc-tion on pistachio. International Journal of Food Microbiology 254: 47–53.
Suzuki, T., Munakata, Y., Morita, K., Shinoda, T. and Ueda, H., 2007. Sensitive detection of estrogenic mycotoxin zearalenone by open sandwich immunoassay. Analytical Sciences 23: 65–70.
Taghizadeh, S.F., Rezaee, R., Davarynejad, G., Asili, J., Nemati, S.H., Goumenou, M., Tsakiris, I., Tsatsakis, A.M., Shirani, K. and Karimi, G., 2018. Risk assessment of exposure to aflatoxin B1 and ochratoxin A through consumption of different Pistachio (Pistacia vera L.) cultivars collected from four geographical regions of Iran. Environmental Toxicology and Pharmacology 61: 61–66.
Tavakolipour, H., Javanmard Dakheli, M. and Zirjani, L., 2010. The inhibitory effect of edible coating of pistachio kernel basis of whey protein concentrate and Shirazi thyme extract on the production of aflatoxin toxin. Journal of Innovation in Food Science and Technology 2: 53–63. [In Persian]
Tavakolipour, H., Javanmard, M. and Zirjany, L., 2012. Antiaflatoxigenic activity of pistachio kernel coated by whey protein based edible film incorporated with zataria multiflura essential oil. Journal of Food Science and Technology 36: 11–19. [In Persian]
Tavakolipour, H. and Mokhtarian, M., 2014. Estimation of equilibrium moisture content of pistachio powder through the ANN and GA approaches. International Journal of Food Engineering 10: 747–755.
Tavakolipour, H. and Mokhtarian, M., 2016. New approach to the calculation of pistachio powder hysteresis. International Agrophysics 30: 245–251. intag-2015-0093
Tavakolipour, H., Mokhtarian, M. and Kalbasi-Ashtari, A., 2017. Lipid oxidation kinetics of pistachio powder during different storage conditions. Journal of Food Process Engineering 40: e12423.
Turner, N.W., Bramhmbhatt, H., Szabo-Vezse, M., Poma, A., Coker, R. and Piletsky, S.A., 2015. Analytical methods for determination of mycotoxins: An update (2009–2014). Analytica Chimica Acta 901: 12–33. aca.2015.10.013
Yazdanpanah, H., Mohammadi, T., Abouhossain, G. and Cheraghali, A.M., 2005. Effect of roasting on degradation of aflatoxins in contaminated pistachio nuts. Food and Chemical Toxicology 43: 1135–1139. fct.2005.03.004
Zhang, L., Dou, X.-W., Zhang, C., Logrieco, A.F. and Yang, M.-H., 2018. A review of current methods for analysis of mycotoxins in herbal medicines. Toxins 10: 65. toxins10020065