An Overview of the Risks of Latent Aflatoxin Contamination in Pistachio Products (from Production to Export): A Comprehensive Analysis

Subject Areas : Journal of Chemical Health Risks

Mehdi Mohammadi-Moghadam ^{1 *} , Hossein Hokmabadi ² , Mohammad Moradi ³ , Seyedhamidreza Ziaolhagh ⁴ , Mostafa Ghasemi ⁵

1 - Crop and Horticultural Sciences Research Department, Agricultural and Natural Resources Research and Education Center of Semnan Province (Shahrood), AREEO, Shahrood, Iran
2 - Institute of Agricultural Education and Extension, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran
3 - Pistachio Research Center, Horticultural Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Rafsanjan, Iran
4 - Agricultural Engineering Research Department, Agricultural and Natural Resources Research and Education Center of Semnan Province (Shahrood), AREEO, Shahrood, Iran
5 - Horticulture Crops Research Department, Qazvin Agricultural and Natural Resources Research and Education Center, AREEO, Qazvin, Iran

Received: 2024-11-21 Accepted : 2025-03-11 Published : 2025-09-28

Keywords: Fungi spore, Washing systems, Aflatoxin contamination, Pistachio, Export,

Abstract :

Aflatoxin contamination of products is a worldwide food safety concern and a major challenge in food safety and security, mainly produced by two closely related fungi, Aspergillus flavus and A. parasiticus. Despite receiving a health certificate at the origin, many export shipments are rejected at the destination due to aflatoxin contamination, which is a result of latent contamination by fungi. Research has shown that Aspergillus is soil-borne in pistachio cultivation areas, with its populations in the soil influenced by the irrigation cycle and time. As harvest timing nears, the population density of aflatoxin-producing fungi on pistachio fruits rises. Investigations into pistachio processing terminals have revealed that traditional terminals have higher contamination levels compared to semi-mechanized ones. Comparing various washing systems, it has been found that using a water shower system is more effective than ponds with static or flowing water in reducing contamination. Fungi spores on pistachio fruits during storage and transportation can lead to aflatoxin contamination, especially in improper storage conditions. This is particularly crucial during the sea transportation of exported pistachios, as high humidity can promote the growth of fungi spores. These instances highlight how even seemingly healthy pistachios can be affected by latent infections. The available information about the latent risks of aflatoxin contamination in different stages of pre-harvest, during harvesting, transportation, processing and its effect on the export and marketing of pistachio product is reviewed. Finally, new perspectives on how to successfully control contamination by implementing these strategies are explored.

References:

1. FAO. 2022. Food and Agriculture Organization of the United Nations Statistics Division.
2. Alshannaq A.F., Gibbons J.G., Lee M.K., Han K.H., Hong S.B., Yu J.H., 2018. Controlling aflatoxin contamination and propagation of Aspergillus flavus by a soy-fermenting Aspergillus oryzae strain. Scientific Reports. 8,16871
3. Alshannaq A., Yu J.H., 2017. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. Int J Env Res Public Health. 14(6), 632.
4. Ráduly Z., Szabó L., Madar A., Pócsi I., Csernoch L., 2020. Toxicological and medical aspects of Aspergillus-derived mycotoxins entering the feed and food chain. Front. Microbiol. 10, 2908.
5. Peles F., Sipos P., Győri Z., Pfliegler W.P., Giacometti F., Serraino A., Pagliuca G., Gazzotti T., Pócsi I., 2019. Adverse effects, transformation, and channeling of aflatoxins into food raw materials in livestock. Front Microbiol. 10, 2861.
6. Jalili M., 2015. A review on aflatoxins reduction in food. Iran J Health Saf Environ. 3, 445–459.
7. Kimanya M.E., Routledge M.N., Mpolya E., Ezekiel Chibundu N., Shirima Candida P., Gong Y.Y., 2021. Estimating the risk of aflatoxin-induced liver cancer in tanzania based on biomarker data. PLoS One. 16(3), e0247281
8. Mgandu F.A., Mirau S., Nyerere N. Chirove F., 2023. Optimal control and cost effectiveness analysis of contamination associated with aflatoxins in maize kernels, livestock and humans. Results in Control and Optimization. 13 (2023), 100313.
9. Wu F., Groopman J.D, Pestka J.J., 2014. Public health impacts of foodborne mycotoxins. Annu Rev Food Sci Technol. 5(1), 351–72.
10. Mahroudi A, Eslami H, Mehrabpour M, Dolatabadi M., 2020. Aflatoxin contamination of pistachio and the problems and strategies of decontamination; A review study. Pistachio and Health Journal. 3(4), 21-32.
11. Marin S, Hodzic I, Ramos AJ, Sanchis V., 2008. Predicting the growth/no-growth boundary and ochratoxin A production by Aspergillus carbonarius in pistachio nuts. Food microbiology. 25(5), 683-9.
12. Setamou M., Cord well K.F., Hell K., 1997. Aspergillus flavus infection and aflatoxin contamination of preharvest maize- in Benin. Plant Dis. 81, 1323-1327.
13. Spanjer MC, Rensen PM, Scholten JM., 2008. LC–MS/MS multi-method for mycotoxins after single extraction, with validation data for peanut, pistachio, wheat, maize, cornflakes, raisins and figs. Food Addit Contam. 25(4), 472-89.
14. Dorner JW., 2008. Management and prevention of mycotoxins in peanuts. Food Addit Contam. 25(2), 203–208.
15. Bhatnagar D, Cary JW, Ehrlich K, Yu J, Cleveland TE., 2006. Understanding the genetics of regulation of aflatoxin production and Aspergillus flavus development. Mycopathologia. 162(3), 155–166.
16. Yin Y., Lou T., Jiang J., Yan L., Michailides T.J., Ma Z., 2008. Molecular characterization of toxigenic and atoxigenic Aspergillus flavus isolates collected from soil in various agroecosystems in China. Food Microbiol.14,5(1), 351–72.
17. Mojthahedi H., Rabie C.J., Lubben A., Steyn M., Danesh D., 1979. Toxic Aspergillus from pistachio nuts. Mycopathologia. 67, 123-127.
18. Moradi M., Ershad J., 2000. Determination of density of the molds Aspergillus species in the Kerman pistachio orchards in different months of years. Proceeding of the 14th Iranian Plant Protection Congress, Isfahan, Iran. pp.128.
19. Klich M.A., 2007. Aspergillus flavus: the major producer of aflatoxin. Mol. Plant Pathol. 8, 713–722.
20. Payne G.A., Brown M., 1998. Genetics and physiology of aflatoxin Biosynthesis. Ann. Rev. Phytopathol. 36, 329-62.
21. Tajabadipur A., Moradi M., 2003. The relationship between the formation history of early splitting pistachio and changing their morphological and aflatoxin contamination in commercial cultivars of pistachio (Oudadi, kallehghuchi and Ahmad Aghaee), Iran's Pistachio Research Institute, Final Report, pp: 21.
22. Van Egmond HP, Jonker MA., 2004. Worldwide regulations on aflatoxins—the situation in 2002. J Toxicol Toxin Rev. 23(2&3), 273–293.
23. Danesh D., Mojtahedi H., Barnett R., Cambell A., 1979. Correlation between climatic data and aflatoxin contamination of Iranian pistachio nuts. Phytophthology 69, 715-716.
24. Denizel T., Jarvis B., Rolfe E.J., 1976. A field survey of pistachio (Pistacia vera) nut production and storage in Turkey with particular reference to aflatoxin contamination. J Sci Food Agric. 27, 1021-1026.
25. Mojthahedi H., Danesh D., Haghighi B., Barnett R., 1978. Postharvest pathology and mycotoxin contamination of Iranian pistachio nuts. Phytopathology. 68, 1800-1804.
26. Mirabolfathy M., 1981. Study of pistachio molds. Annual Report of Laboratory of Plant Pests and Diseases Research Institute, Rafsanjan, Iran.
27. Jones R.K., Duncan H.E., Hamilton P.B., 1981. Planting date. harvest date, and irrigation effects on infection and aflatoxin production by Aspergillus flavus in field corn. Phytopathology. 71, 810-16.
28. Michailides T.J., Morgan D.P., 1990. Mycoflora of pistachio fruits throughout the season and manipulation trials. Pages 112-117. In california pistachio industry. Annual report crop year 1989-1990. California pistachio commission fresno.
29. Doster M.A., Michailides T.J., 1999. Relationship between shell discoloration of pistachio nuts and incidence of fungal decay and insect infestation. Plant Dis. 83, 259-264.
30. Klick M.A., Tiffany L.H., knaphus G., 1992. Ecology of the. Aspergillus of soils and litter pages 329-353 in: Aspergillus: Biology and Industrid Application. J. W. Bennett and M. A. Klich (eds). Butterworth-Heineman, stonehlam, M.A.
31. Schmidt-Heydt M., Abdel-Hadi A., Magan N., Geisen R., 2009. Complex regulation of the aflatoxin biosynthesis gene cluster of Aspergillus flavus in relation to various combinations of water activity and temperature. Int J Food Microbiol. 135, 231–237.
32. Abdel-Hadi A., Schmidt-Heydt M., Parra R., Geisen R., Magan N., 2012. A systems approach to model the relationship between aflatoxin gene cluster expression, environmental factors, growth and toxin production by Aspergillus flavus. J R Soc Interface. 9,757–767.
33. Cotty P.J., BaymanP., 1993. Competitive exclusion of a toxigenic strain of Aspergillus flavus by an atoxigenic strain. phytopathology 83, 1283-1287.
34. Jarvis B.D., Seiler A.L., Ould A.J.L., Williams A.P., 1983. Observation on the enumeration of molds in food and feedings. J Appl Bact. 55, 325-336.
35. McGee D.C., Olanya O.M., Hoyos G.M., Tiffany L.H., 1996. Population of Aspergillus flavus in the Lowa cornfield ecosystem in years not favorable for aflatoxin concentration of corn grain. Plant Dis. 80, 742-746.
36. Mojthahedi H., Danesh D., Haghighi B., Fathy S., 1980. Storage relative humidity in Rafsanjan and impossiblity of pistachio aflatoxicosis after nut processing. Iran J Plant Path. 16, 80-85.
37. Moradi M., Hokmabadi H., 2011. Control of Mycotoxin Bioactives in Nuts: Farm to Fork. pp: 253-273. In: Fruit and Cereal Bioactives Sources, Chemistry, and Applications. Ö. Tokusoglu (ed). CRC Press.
38. Purcell S.L., Phillips D.J., Mackey B.E., 1980. Distribution of Aspergillus flavus and other fungi in several almond-growingareas of California. Phytopathology. 70, 926-929.
39. Rodriguez-del- Bosque L.A., 1996. Impact of agronomic factors on aflatoxin contamination in preharvest field corn in northeastern mexico. Plant Dis. 80, 988-993.
40. Doster M., Michailides T.J., 1994. Aspergillus molds and aflatoxin in pistachio nuts in california. Phytopathology. 84, 583-590.
41. Doster W.A., Michailides T.J., 1995. The relationship between date of hull splitting and decay of pistachio nuts by Aspergillus species. Plant Dis. 79, 766-769.
42. Danesh D., Mojtahedi H., Barnett R., Cambell A., 1979. Correlation between climatic data and aflatoxin contamination of Iranian pistachio nuts. Phytophthology. 69,715-716.
43. Suzangar M., Mojtahedi H., Emami A., Dunesh D., Farivar H., BarnettR., 1976. First and second stage aflatoxin contamination of pistachio nuts (Combination of 3 years study). In: I.U.P.A.C. symposium on mycotoxin in foodstuffs, Sept 15-18, Paris, France. pp 3-3.
44. Sommer N.F., Buchanan J.R., Fortlage R.J., 1986. Relation of early splitting and tattering of pistachio nuts to aflatoxin in the orchard. Phytopathology. 76, 692-694.
45. Thomson S.V., Mehdy M.C., 1978. Occurrence of Aspergillus flavus in pistachio nuts prior to harvest. Phytopathology 68, 1112-1114.
46. Topuz F.C., Akfırat S., 2022. Aflatoxin Problem in International Trade of Pistachios and Solution Suggestions. BSEU Journal of Science. 9(1), 625-632,
47. Doster M.A., Michailides T.J., 1994. Development of Aspergillus molds in litter from pistachio trees. Plant Dis. 78, 393- 397.
48. Esmailpour A., Dehghani H., Mirdamadiha F., 2000. Effects of delay on harvesting and processing time on aflatoxin rate in pistachio. Proceeding of the 14 th Iranian Plant Protection Congress, Isfahan, Iran. p:129.
49. Doster M.A., Michaildes T.J., Gold Hamer D.A., Morgan, D.P., 2001. In Sufficient Spirng Irrigation Increases Abnormal Splitting of Pistachio Nuts. Calif Agric. 55, 28-31.
50. Emami A., Suzangar M., Barnett R., 1977. Contamination of pistachio nuts with aflatoxin while on the trees and in storage. Zesz Probl Postęp Nauk Rol. 189, 135-140.
51. Mohammadi Moghadam M., 2009. Study of pistachio contamination in processing terminals of Semnan province and evaluation of resistance of pistachio cultivars to Aspergillus flavus and aflatoxin B1 (Final report). Agricultural Research, Education and Extention Organization. Iranian Pistachio Research Institute. 24. pp. [In Persian]
52. Ahmadi F., Tajabadipour A., 2011. Investigation of Aflatoxin Contamination in Indehiscence and Mechanical Splitting Pistachios. Inter J Nuts and Related Sci. 2(1), 31-36.
53. Moradi M., Javanshah A., 2006. Distribution of Aflatoxin in processed pistachio nut terminals. Acta Hort. (ISHS), 726, 431-436.
54. Pfliegler V., Pócsi I., Győri Z., Pusztahelyi T., 2020. The Aspergilli and their mycotoxins: Metabolic interactions with plants and the soil biota. Front Microbiol. 10, 1–45.
55. Jasutiene I., Garmiene G, Kulikauskiene M., 2006. Pasteurisation and fermentation effects on Aflatoxin M1 stability. Milchwissenschaft. 61, 75–79.
56. Raters M., Matissek R., 2008. Thermal stability of aflatoxin B1 and ochratoxin A. Mycotoxin Res. 24, 130–134.
57. Dorner JW., 2004. Biological control of aflatoxin contamination of crops. J Toxicol Toxin Rev. 23(2&3),425–450.
58. Pitt JI, Hocking AD., 2006. Mycotoxins in Australia: biocontrol of aflatoxin in peanuts. Mycopathologia.162(3), 233–243.