Journal of Plant Pathology & Microbiology

Aflatoxin producing fungi and its management: A Review

Abera Olana^* Department of Plant Science, College of Natural and Environmental Sciences, Wollega University, Nekemte, Wollega, Ethiopia
^*Correspondence: Abera Olana, Department of Plant Science, College of Natural and Environmental Sciences, Wollega University, Nekemte, Wollega, Ethiopia, Email:

Received: 08-Nov-2022, Manuscript No. JPPM-22-18706; Editor assigned: 11-Nov-2022, Pre QC No. JPPM-22-18706 (PQ); Reviewed: 25-Nov-2022, QC No. JPPM-22-18706; Revised: 02-Dec-2022, Manuscript No. JPPM-22-18706 (R); Published: 09-Dec-2022, DOI: 10.35248/2157-7471.22.13.641

Introduction

The term mycotoxin was named in 1960 as a result of an unusual veterinary catastrophe near London, England, during which roughly 100,000 turkeys died [1]. When this unknown turkey X disease was associated with a groundnut (Arachis hypogea L.) meal contaminated with secondary metabolites from Aspergilus flavus [2-4]. Thus, the toxin was coined “aflatoxin” by virtue of its origin from A. flavus. Aflatoxins (AF) are produced via a polyketide pathway by various species of Aspergillus section Flavi, which includes A. flavus, A. parasiticus, A. parvisclerotegenus, A. minisclerotigenes and A. nomius [5]. Both A. flavus and A. parasiticus are most frequently detected in agricultural products because of their widespread distribution [6].

Aflatoxins are largely prevalent in major food crops such as maize (Zea mays L.), groundnuts, tree nuts, wheat (Triticum aestivum L), sorghum (Sorghum bicolor L), spices, milk and meat products [7]. Aflatoxin contamination depends on Aspergillus species, growing and storage conditions, management practices employed and other factors [8]. Aflatoxins can accumulate through the food chain posing a serious health concern to humans [9]. Aflatoxin contamination is common in tropical countries where drought is prevalent throughout the year, in such regions, changes in weather patterns may result in acute aflatoxicoses and deaths [10]. Biosynthesis of aflatoxin depends on pH, water activity, insect infestation and temperature [11]. Climate change is anticipated to have a pronounced effect on economically important crops and mycotoxigenic fungal infection and contamination with aflatoxins [8]. Undeniably, climate change may have impact on the interactions between various mycotoxigenic species and the relative mycotoxin contamination of staple commodities [12].

In order to minimize the effect of aflatoxin on our commodity, understanding of the factors that predispose the infection of the plant with aflatoxin-producing fungi and the conditions that encourage their formation is crucial [13]. As the presence of aflatoxin in food can be hazardous for human health and signify an enormous economic problem, one has all the reasons to allow for the implementation of new techniques providing for a safe food production. The first step in reducing aflatoxin contamination is through understanding pre and post-harvest management techniques. Pre-harvest bio control technologies can give us the greatest opportunity to reduce AF production on the spot [14]. This can be possible through proper curing, drying, sorting, storing, physical separation, microbial degradation and different chemical treatments. Therefore, the objective of this review is to summarize on aflatoxin producing fungi and its management strategies.

Literature Review

Aflatoxins: Serious threat to health and economy

Aflatoxins are toxic and carcinogenic mycotoxins produced by fungi belonging to Aspergillus section Flavi, primarily A. flavus and A. parasiticus [15-18]. Different types of aflatoxins have been identified, with aflatoxin B1, B2, G1, G2, M1 and M2 being the most frequent and toxic [19]. When ingested, aflatoxin B1 (AFB1) is hydroxylated to aflatoxin M1 (AFM1) and is secreted in the milk of animals whose feedstuffs have been contaminated by AFB1 and AFB2 [7,20,21]. A. flavus produces only AFB1 and AFB2, whereas A. parasiticus produces AFB1, AFB2, AFG1 and AFG2 [22]. The International Agency for Research on Cancer (IARC) has classified AFB1, AFB2, AFG1 and AFG2 as Group 1 mutagens, whereas AFM1 as Group 2B [23]. Aflatoxins B1 and B2 fluoresce blue, whereas AFG1 and AFG2 fluoresce green. Aflatoxins are carcinogenic, mutagenic, teratogenic and immunosuppressive and their presence in food commodities greatly impacts the food and feed industries [9,24,25]. In particular, co-occurrence of mycotoxins is a major concern because the possible synergetic toxicities are not well known.

High dose exposures of AFs on humans result in vomiting, abdominal pain, and even possible death, while small quantities of chronic exposure may lead to liver cancer [9]. Aflatoxins play a significant role in development of edema in malnourished people as well as in the pathogenesis of kwashiorkor in malnourished children [26,27]. Aflatoxin contamination of human food and animal feed causes severe health and economic risks worldwide, especially in low income countries where the majority of the people consume maize and groundnuts. As a result, most countries set legislation that restricts movement of aflatoxin contaminated commodities [28]. Safe limit of AFs for human consumption varies from one country to another and ranges from 4 to 30 µg/kg. European Union has set the maximum acceptable limit at 2 µg/kg for AFB1 and 4 µg/kg for total AFs and the US 20 µg/kg [29,30].

FAO estimates that 25 per cent of the world food crops are affected by mycotoxins each year and constitute a loss at post-harvest [31]. In the United States from 1990 to 1996, litigation costs of $34 million from aflatoxin contamination occurred. In 1998, as a consequence of aflatoxin contaminations, maize farmers lost $40 million [32]. In 2004 annual loss was more than $750 million in Africa due to aflatoxin contamination of agricultural crops. Ultimately, it contributes to increased costs to consumers [32]. A loss due to aflatoxin contamination costs about $100 million per year including $26 million loss in peanut ($69.34/ha). In Japan, AFB1 was detected in groundnuts imports from 20 of 31 countries, five lots of large type raw shelled and 269 lots of small type raw shelled groundnuts were rejected as having above the regulation level (10 ppb) of AFB1.

Effect of environmental factors on aflatoxin producing fungi and aflatoxin contamination

Warm and humid environments and insect damage promote the growth of fungi and the production of aflatoxins. Atmosphere composition has an immense impact on mould growth, with humidity being the most important variable for their growth [33,34]. Aflatoxin production is determined by a wide range of substrates due to non-visible spoilage at pre-harvest in the field and post-harvest during storage or processing. Poor storage conditions could also influence mold development and aflatoxin contamination in the stored products [35]. However, high contamination and toxin production occur in poorly stored commodities, because of inadequate moisture and high temperature [13]. Fungal growth can occur over a wider range of temperatures, pH and water activity levels on maize [36]. Optimum water activity and temperatures on groundnuts were: 0.94 aw and 34°C for growth and 0.99 aw and 3°C for AFB1 production respectively (Table 1). Similarly, in maize temperature ranged from 10°C to 43°C for fungal growth and from 13 to 37°C for AFB1 production. Water activity and temperature range vary for toxin production and for mould growth [37].

Table 1: Limits of mould growth and aflatoxin production by A. flavus and A. parasiticus (ICMSF 1996).

Relative humidity between 83%-88% has been found to be appropriate to influence the mold growth and aflatoxins production [38]. Hotter and drier summers are predicted which may prevent certain fungi from contaminating vegetation due to the lack of humidity [39]. The germination of the spores is greatly influenced by humidity and temperature, meaning that any change in climate will greatly affect these processes [8,40]. Significant correlations have been reported between agro-ecological zones and aflatoxin levels, with wet and humid climates after longer storage periods increasing aflatoxin risk [41]. Kaaya disclosed that aflatoxin levels were higher in more humid areas compared to the drier areas in maize samples collected from Uganda and this findings concords with maize samples collected from Nigeria [42,43].

When environmental conditions are favorable, wind and insect dispersal of conidia are transferred to plants results in colonization and infection within the susceptible hosts and production of aflatoxins [44]. Conidia serve as source of inoculum for secondary infections and reservoirs of A. flavus for subsequent dispersal to susceptible hosts [45]. Maize borers on maize, pink bollworm on cotton, lesser corn stalk borer on groundnut and the navel orange worm on pistachio vector aflatoxin-producing fungi resulting in increased aflatoxin contamination [46].

Discussion

Management of aflatoxin producing fungi and aflatoxin contamination

Cultural practices: Cultural practices that minimize the occurrence of aflatoxin contamination in the field comprises: timely planting, maintaining optimal plant densities, proper plant nutrition, avoiding drought stress, controlling pests and proper handling during harvesting. Waliyar reported reduction of A. flavus infection and aflatoxin contamination by 50%-90% through application of lime, farm yard manure and cereal crop residues as soil improvement [47]. Delayed the harvested crop in the field prior to storage encourages fungal infection and insect infestation [48]. Growths of toxigenic fungi in stored commodities are influenced by moisture and temperature content. Hell reported that when maize stored for three days, with a moisture content above 13%, aflatoxin contamination increase 10 fold and recommended cereal commodities should dried to a moisture levels of 10%-13% [49]. To decrease toxin contamination, technological solutions that assist in decreasing grain moisture quickly have been reviewed by Udomkun [13]. Farmers in lower-income countries store agricultural products in containers usually made from wood, bamboo, mud placed and covered with thatch or metal roofing sheets [50]. Recently, hermetic storage containers such as metal or cement bins have been established as alternatives to traditional storage methods, however, their high costs and difficulties with availability make acceptance by small-scale farms limited [51]. Hell investigated that although polypropylene bags are recently used for grains storage, they are still contaminated by fungal pathogens and aflatoxins especially when those reused bags contain A. flavus spores [41]. Williams point out that the Purdue Improved Crop Storage (PICS) bags effectively suppressed the development of A. flavus and minimize aflatoxin contamination in maize in wide range of moisture conditions [52]. Njoroge recorded less moisture absorbance in grains stored in PICS bags than grains stored in woven polypropylene bags [53].

Physical methods: Aflatoxin levels can be minimized in stored products using physical techniques such as color sorting, density flotation, blanching and roasting. Physical sorting of broken and infected grains from the intact commodity reduce aflatoxins levels by 40-80 per cent [54]. Hell reported that reduction of aflatoxin in cleaned stores as compared to non-cleaned stores [49].

Aflatoxins contamination in pistachio nuts is reduced by 95% through colour sorting [55]. However, such physical techniques are usually arduous and ineffective. Computer-based image processing techniques for large-scale screening of fungal and toxin contaminations in food and feed are promising modern techniques. Berardo quantified fungal infection and mycotoxins produced in maize grain by Fusarium verticillioides using Near Infrared Spectroscopy [56]. An additional image based sorting technology has been forwarded by Ozlüoymak, who revealed that approximately 98% of the aflatoxins in contaminated figs were effectively detected and separated by a UV light coupled with colour detection system [57].

Chemical methods: The use of chemicals to bind, inactivate or remove aflatoxins has been studied extensively using propionic acid, ammonia, copper sulfate, benzoic acid, urea and citric acid chemicals capable of reacting with aflatoxins [58]. Jalili and Jinap studied the effect of 2% Sodium hydrosulphite (Na2S2O4) on the reduction of aflatoxins in black pepper and found that a decrease in AFB1, AFB2, AFG1, and AFG2, without harm to the outer layer of black pepper [59]. Techniques other than the use of chemical sorbents and ammonization have achieved reduction in aflatoxin bioavailability that due to hydrated Sodium calcium Aluminosilicate binding [60]. Since 1988 there are several publications that reveal the use of Hydrated Sodium, Calcium Aluminosilicates as adsorbents for mycotoxins in vivo and in vitro. Ammonization method has been shown to efficiently destroy AFB1 in cottonseed and cottonseed meal, groundnuts and groundnut meal, and maize [61]. Although Ammonia, Sodium bisulfite, and Calcium hydroxide treatments are efficient, they do not fulfill food safety require­ments [62].

Biological methods: Among numerous research approaches, biological degradation of aflatoxins using microorganisms is one of the striking strategies for the management of these poisonous fungal toxins in food and feed [63]. Several microbes viz., bacteria, yeasts, actinomycetes, algae and non-toxigenic strains of A. flavus and A. parasiticus have been tested to minimize aflatoxin contamination in different crops such as maize and groundnut [64-66]. Bandyopadhyay R, Lewis M, and Senghor L, demonstrated that bio control non-afla toxigenic strains reduced AF concentrations in treated crops by more than 80% under both field and storage conditions [67-69]. A toxigenic strain of A. flavus in the USA has been approved and marketed as Afla-Guard®. Similarly, in Nigeria atoxigenic strains of A. flavus has gained provisional registration (AflaSafe) and confirmed to decrease aflatoxin concentrations up to 99% both in vitro and in vivo [70]. Farzaneh isolated Bacillus subtilis strain UTBSP1 from pistachio nuts and examined for the degradation of AFB1 and found that B. subtilis UTBSP1 significantly reduced AFB1 by 95 per cent [70]. Several studies showed that inhibition of mycelial growth and reduction of aflatoxin contamination when different crops are treated by Bacillus subtilis, Pseudomonas solanacearum, P. fluorescens and Rhodococcus erythropolis [71,72]. Several non-lactic acid bacteria, such as Bacillus spp., Brachybacterium spp., Brevundimonas spp., Cellulosimicrobium spp., Enterobacter spp., Escherichia spp., Klebsiella spp., Mycolicibacterium spp., Myxococcus spp., Nocardia spp., Pseudomonas spp., Rhodococcus spp., Streptomyces spp., and Stenotrophomonas spp., can also inhibit the growth and AF production of molds [14].

Plant extracts: Plants produce different secondary metabolites to fight against pathogen attack. Antimicrobial compounds produced by plants are safe for the environment and consumers, and are important to control postharvest diseases. They are classified as generally recognized as safe and have low hazard to the consumers [73]. Plant extracts have been reported to have antifungal activity against aflatoxins produced by A. flavus and A. parasiticus [74-76]. Hajare reported an 80% decrease in total aflatoxin content over the controls after treatment with aqueous extract of Trachyspermum ammi seeds [74]. Sandoss kumar incubated AFB1 with zimmu extract for five days and verified the potential of zimmu extract to degrade aflatoxin and reduce AFB1 by up to 90% [75]. In addition, when groundnut was intercropped with zimmu, a significant reduction in the population of A. flavus in the soil, kernel infection by A. flavus and aflatoxin contamination was observed. Hacise ferogullary evaluated the efficacy of garlic extract at different levels against A. flavus, A. fumigatus, A. niger, A. ochraceus, A. terreus, Penicillium chrysogenum, P. puberulum, P. citrinum, P. corylophilum, Rhizopus stolonifer, Stachybotrys chartarum, Eurotium chevalieri and Emericella nidulans growth [77]. Eighty four per cent reduction in toxin production occurred at 1% inclusion level.

Policy directions

In order to reduce aflatoxin contamination policies should focuses on:

•Improving awareness on sources of aflatoxin contamination along the value chain (farmers, consumers, processors, and traders) and health impacts;

•Implementing appropriate pre and post-harvest Aspergillus fungi control strategies and

•Developing accessible low cost technologies and infrastructure to monitor contamination levels.

Conclusion

Infection of crops with the fungi in the genus Aspergillus both at field and storage conditions leads to aflatoxin contamination in warm and humid areas. Aflatoxin contamination causes stunting in children, immune suppression, liver cancer and death. It is possible to reduce aflatoxin contamination by using management options such as sorting, crop rotation, irradiation, fumigation, chemical, botanical, biological control and improved storage structures to improve health conditions of people, and increase food safety and security. In the future multidisciplinary and inclusive research is vital to evaluate the effect of climate change and the potential benefits of integrated management technologies.

Competing Interests

The authors declare that they have no competing interests.

Acknowledgement

Not applicable.

REFERENCES

1. Blount WP. Turkey" X" disease. J Br Turkey Fed. 1961;9:52-77.

   [Crossref] [Google Scholar]

2. Bennett J, Klich MA. Mycotoxins. Clinic Microbiol Rev. 2003. 16 (3);497-516.

   [Crossref] [Google Scholar] [PubMed]

3. Perdoncini MR, Sereia MJ, Scopel FH, Formigoni M, Rigobello ES, Beneti SC, et al. Growth of fungal cells and the production of mycotoxins. Cell growth. 2019;23.

   [Google Scholar]

4. Joubrane K, Mnayer D, El Khoury A, El Khoury A, Awad E. Co-occurrence of aflatoxin B1 and ochratoxin A in Lebanese stored wheat. J Food Prot. 2020;83(9):1547-1552.

   [Crossref] [Google Scholar] [PubMed]

5. Pleadin J, Vulić A, Perši N, Škrivanko M, Capek B, Cvetnić Ž. Aflatoxin B1 occurrence in maize sampled from Croatian farms and feed factories during 2013. Food Control. 2014;40:286-291.

   [Crossref] [Google Scholar]

6. Frisvad JC, Hubka V, Ezekiel CN, Hong SB, Nováková A, Chen AJ, et al. Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Studies Mycol. 2018;91(1):37-59.

   [Crossref] [Google Scholar] [PubMed]

7. Iqbal SZ, Jinap S, Pirouz AA, Faizal AA. Aflatoxin M1 in milk and dairy products, occurrence and recent challenges: A review. Trends Food Sci Technol. 2015;46(1):110-119.

   [Crossref] [Google Scholar]

8. Paterson RR, Lima N. How will climate change affect mycotoxins in food?. Food Research international. 2010;43(7):1902-1914.

   [Crossref] [Google Scholar]

9. Sherif SO, Salama EE, Abdel-Wahhab MA. Mycotoxins and child health: The need for health risk assessment. International J Hygiene Environ Health. 2009;212(4):347-368.

   [Crossref] [Google Scholar] [PubMed]

10. Lewis L, Onsongo M, Njapau H, Schurz-Rogers H, Luber G, Kieszak S, et al. Aflatoxin contamination of commercial maize products during an outbreak of acute aflatoxicosis in eastern and central Kenya. Environ health Perspective. 2005;113(12):1763-1767.

    [Crossref] [Google Scholar] [PubMed]

11. Molina M, Giannuzzi L. Modelling of aflatoxin production by Aspergillus parasiticus in a solid medium at different temperatures, pH and propionic acid concentrations. Food Res International. 2002;35(6):585-594.

    [Crossref] [Google Scholar]

12. Magan N, Medina A, Aldred D. Possible climate‐change effects on mycotoxin contamination of food crops pre‐and postharvest. Plant Pathol. 2011;60(1):150-163.

    [Crossref] [Google Scholar]

13. Udomkun P, Wiredu AN, Nagle M, Müller J, Vanlauwe B, Bandyopadhyay R. Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application: A review. Food Control. 2017;76:127-138.

    [Crossref] [Google Scholar] [PubMed]

14. Peles F, Sipos P, Kovács S, Győri Z, Pócsi I, Pusztahelyi T. Biological control and mitigation of aflatoxin contamination in commodities. Toxins. 2021;13(2):104.

    [Crossref] [Google Scholar] [PubMed]

15. Amaike S, Keller NP. Aspergillus flavus. Annual Rev Phytopathol. 2011;49(1):107-33.

    [Crossref] [Google Scholar] [PubMed]

16. Baranyi N. Current trends in aflatoxin research. Acta Biologica Szegediensis. 2013;57(2):95-107.

    [Google Scholar]

17. Cotty PJ. Comparison of four media for the isolation of Aspergillus flavus group fungi. Mycopathologia. 1994;125(3):157-162.

    [Crossref] [Google Scholar] [PubMed]

18. Mahuku G, Nzioki HS, Mutegi C, Kanampiu F, Narrod C, Makumbi D. Pre-harvest management is a critical practice for minimizing aflatoxin contamination of maize. Food Control. 2019;96:219-226.

    [Crossref] [Google Scholar] [PubMed]

19. Akiyama H, Goda Y, Tanaka T, Toyoda M. Determination of aflatoxins B1, B2, G1 and G2 in spices using a multifunctional column clean-up. J Chromatography A. 2001;932(1-2):153-157.

    [Crossref] [Google Scholar] [PubMed]

20. Ketney O, Santini A, Oancea S. Recent aflatoxin survey data in milk and milk products: A review. International J Dairy Technol. 2017;70(3):320-331.

    [Crossref] [Google Scholar]

21. Serraino A, Bonilauri P, Kerekes K, Farkas Z, Giacometti F, Canever A, et al. Occurrence of aflatoxin M1 in raw milk marketed in Italy: Exposure assessment and risk characterization. Frontier Microbiol. 2019;10:2516.

    [Crossref] [Google Scholar] [PubMed]

22. Creppy EE. Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicology letters. 2002;127(1-3):19-28.

    [Crossref] [Google Scholar] [PubMed]

23. In IA. Mycotoxin control in low-and middle-income countries. Lyon (FR): International Agency Res Cancer. 2015.

    [Google Scholar] [PubMed]

24. Jalili M. A review on aflatoxins reduction in food. Iran J Health Saf Environ. 2015;3:445-459.

    [Google Scholar]

25. Peles F, Sipos P, Győri Z, Pfliegler WP, Giacometti F, Serraino A, et al. Adverse effects, transformation and channeling of aflatoxins into food raw materials in livestock. Frontier Microbiol. 2019;10:2861.

    [Crossref] [Google Scholar] [PubMed]

26. Ráduly Z, Szabó L, Madar A, Pócsi I, Csernoch L. Toxicological and medical aspects of Aspergillus-derived mycotoxins entering the feed and food chain. Frontier Microbiol. 2020;10:2908.

    [Crossref] [Google Scholar] [PubMed]

27. Coulter JB, Hendrickse RG, Lamplugh SM, Macfarlane SB, Moody JB, Omer MI, et al. Aflatoxins and kwashiorkor: Clinical studies in Sudanese children. Transaction Royal Society Trop Med Hygiene. 1986;80(6):945-951.

    [Crossref] [Google Scholar] [PubMed]

28. Juan C, Ritieni A, Mañes J. Determination of trichothecenes and zearalenones in grain cereal, flour and bread by liquid chromatography tandem mass spectrometry. Food Chem. 2012;134(4):2389-2397.

    [Crossref] [Google Scholar] [PubMed]

29. EC (European Commission). Commission regulation (EU) no 165/2010 of amending regulation (EC) no 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards aflatoxin. Official J European Union. 8-12. L 50. 2010.
30. Wu F. Mycotoxin reduction in Bt corn: Potential economic, health, and regulatory impacts. Transgenic Res. 2006;15(3):277-289.

    [Crossref] [Google Scholar] [PubMed]

31. FAO (Food and Agriculture Organization) (1997). Worldwide Regulations for Mycotoxins. A compendium.
32. AMCE (Aflatoxin mitigation center of excellence). Preventing health hazards and economic losses from aflatoxin. Texas Corn producers. 2010.
33. Cotty PJ, Jaime-Garcia R. Influences of climate on aflatoxin producing fungi and aflatoxin contamination. International J Food Microbiol. 2007;119(1-2):109-115.

    [Crossref] [Google Scholar] [PubMed]

34. Valencia-Quintana R, Milić M, Jakšić D, Šegvić Klarić M, Tenorio-Arvide MG, Pérez-Flores GA, et al. Environment changes, aflatoxins, and health issues: A review. International J Environ Res Pub Health. 2020;17(21):7850.

    [Crossref] [Google Scholar] [PubMed]

35. Tsehaynesh T, Abdi M, Hassen S, Taye W. Aspergillus species and aflatoxin contamination in pepper (Capsicum annuum L.) in West Gojjam, Ethiopia. African J Food Agric Nutri Develop. 2021;21(1):17178-17194.

    [Crossref] [Google Scholar]

36. Aldars-García L, Berman M, Ortiz J, Ramos AJ, Marín S. Probability models for growth and aflatoxin B1 production as affected by intraspecies variability in Aspergillus flavus. Food Microbiol. 2018;72:166-175.

    [Crossref] [Google Scholar] [PubMed]

37. ICMSF (International Commission on Microbiological Specifications for Food). Toxigenic Fungi: AspergillusMicroorganism in foods. Characteristics of food pathogens. London: Academic. 1996;347-381.
38. Agriopoulou S, Stamatelopoulou E, Varzakas T. Advances in occurrence, importance, and mycotoxin control strategies: Prevention and detoxification in foods. Foods. 2020;9(2):137.

    [Crossref] [Google Scholar] [PubMed]

39. West JS, Holdgate S, Townsend JA, Edwards SG, Jennings P, Fitt BD. Impacts of changing climate and agronomic factors on fusarium ear blight of wheat in the UK. Fungal Ecology. 2012;5(1):53-61.

    [Crossref] [Google Scholar]

40. Doohan FM, Brennan J, Cooke BM. Influence of climatic factors on Fusarium species pathogenic to cereals. InEpidemiology of mycotoxin producing fungi 2003;755-768.

    [Google Scholar]

41. Hell K, Cardwell KF, Setamou M, Poehling HM. The influence of storage practices on aflatoxin contamination in maize in four agroecological zones of Benin, West Africa. J Stored Product Res. 2000;36(4):365-382.

    [Crossref] [Google Scholar] [PubMed]

42. Kaaya AN, Kyamuhangire W, Kyamanywa S. Factors affecting aflatoxin contamination of harvested maize in the three agroecological zones of Uganda. J App Sci. 2006;6(11):2401-2407.

    [Crossref] [Google Scholar]

43. Atehnkeng J, Ojiambo PS, Cotty PJ, Bandyopadhyay R. Field efficacy of a mixture of atoxigenic Aspergillus flavus Link: Fr vegetative compatibility groups in preventing aflatoxin contamination in maize (Zea mays L.). Biological Control. 2014;72:62-70.

    [Crossref] [Google Scholar]

44. Payne GA. Process of contamination by aflatoxin-producing fungi and their impact on crops. Mycotoxin Agric Food Safety. 1998;9:279-306.

    [Google Scholar]

45. Jaime-Garcia R, Cotty PJ. Aspergillus flavus in soils and corncobs in south Texas: Implications for management of aflatoxins in corn-cotton rotations. Plant Disease. 2004;88(12):1366-1371.

    [Crossref] [Google Scholar] [PubMed]

46. Dowd PF, Johnson ET, Williams WP. Strategies for insect management targeted toward mycotoxin management. InAflatoxin and food safety 2005;542-567.

    [Google Scholar]

47. Waliyar F, Kumar PL, Traoré A, Ntare BR, Diarra B, Kodio O. Pre-and postharvest management of aflatoxin contamination in peanuts. Mycotoxins: detection methods, management, public health and agricultural trade. 2008:209-218.

    [Google Scholar]

48. Udoh JM, Cardwell KF, Ikotun T. Storage structures and aflatoxin content of maize in five agroecological zones of Nigeria. J Stored Product Res. 2000;36(2):187-201.

    [Crossref] [Google Scholar] [PubMed]

49. Hell K, Fandohan P, Ranajit Bandyopadhyay RB, Kiewnick S, Sikora R, Cotty PJ. Pre-and postharvest management of aflatoxin in maize: An African perspective. InMycotoxins: Detection Method, Manage, Public Health Agric Trade. 2008. 219-229.

    [Crossref] [Google Scholar]

50. Waliyar F, Umeh VC, Traore A, Osiru M, Ntare BR, Diarra B, et al. Prevalence and distribution of aflatoxin contamination in groundnut (Arachis hypogaea L.) in Mali, West Africa. Crop Prot. 2015;70:1-7.

    [Crossref] [Google Scholar]

51. Kerstin H, Charity M. Aflatoxin control and prevention strategies in key crops of Sub-Saharan Africa. African J Microbiol Res. 2011;5(5):459-466.

    [Google Scholar]

52. Williams SB, Baributsa D, Woloshuk C. Assessing Purdue Improved Crop Storage (PICS) bags to mitigate fungal growth and aflatoxin contamination. J Stored Product Res. 2014 ;59:190-196.

    [Crossref] [Google Scholar]

53. Njoroge AW, Affognon HD, Mutungi CM, Manono J, Lamuka PO, Murdock LL. Triple bag hermetic storage delivers a lethal punch to Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) in stored maize. J Stored Product Res. 2014;58:12-19.

    [Crossref] [Google Scholar]

54. Fandohan P, Zoumenou D, Hounhouigan DJ, Marasas WF, Wingfield MJ, Hell K. Fate of aflatoxins and fumonisins during the processing of maize into food products in Benin. International J Food Microbiol. 2005;98(3):249-259.

    [Crossref] [Google Scholar] [PubMed]

55. Shakerardekani A, Karim R, Mirdamadiha F. The effect of sorting on aflatoxin reduction of pistachio nuts. J Food Agric Environ. 2012;10(1):459-461.

    [Google Scholar]

56. Berardo N, Pisacane V, Battilani P, Scandolara A, Pietri A, Marocco A. Rapid detection of kernel rots and mycotoxins in maize by near-infrared reflectance spectroscopy. J Agric Food Chem. 2005;53(21):8128-8134.

    [Crossref] [Google Scholar] [PubMed]

57. Özlüoymak Ö. Development of a UV-based imaging system for real-time detection and separation of dried figs contaminated with aflatoxins. J Agric Sci. 2014;20(3):302-316.

    [Crossref] [Google Scholar]

58. Gowda NK, Malathi V, Suganthi RU. Effect of some chemical and herbal compounds on growth of Aspergillus parasiticus and aflatoxin production. Animal Feed Sci Technol. 2004;116(3-4):281-291.

    [Crossref] [Google Scholar]

59. Jalili M, Jinap S. Role of sodium hydrosulphite and pressure on the reduction of aflatoxins and ochratoxin A in black pepper. Food Control. 2012;27(1):11-15.

    [Crossref] [Google Scholar]

60. Phillips TD, Kubena LF, Harvey RB, Taylor DR, Heidelbaugh ND. Hydrated sodium calcium aluminosilicate: A high affinity sorbent for aflatoxin. Poultry Sci. 1988;67(2):243-247.

    [Crossref] [Google Scholar] [PubMed]

61. Park DL, Price WD. Reduction of aflatoxin hazards using ammoniation. Rev Environmental Contamination Toxicol. 2001;171:139-176.

    [Google Scholar]

62. Piva G, Galvano F, Pietri A, Piva AP. Detoxification methods of aflatoxins. A review. Nutrition Res. 1995;15(5):767-776.

    [Crossref] [Google Scholar]

63. Shetty PH, Jespersen L. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trend food Sci & Technol. 2006;17(2):48-55.

    [Crossref] [Google Scholar]

64. Dorner JW, Cole RJ, Wicklow DT. Aflatoxin reduction in corn through field application of competitive fungi. J Food Prot. 1999;62(6):650-656.

    [Crossref] [Google Scholar] [PubMed]

65. Vijayasamundeeswari A, Vijayanandraj S, Paranidharan V, Samiyappan R, Velazhahan R. Integrated management of aflatoxin B1 contamination of groundnut (Arachis hypogaea L.) with Burkholderia sp. and zimmu (Allium sativum L.× Allium cepa L.) intercropping. J Plant Interact. 2010;5(1):59-68.

    [Crossref] [Google Scholar]

66. Shifa H, Tasneem S, Gopalakrishnan C, Velazhahan R. Biological control of pre-harvest aflatoxin contamination in groundnut (Arachis hypogaea L.) with Bacillus subtilis G1. Archives Phytopathol Plant Prot. 2016;49(5-6):137-148.

    [Crossref] [Google Scholar]

67. Bandyopadhyay R, Ortega-Beltran A, Akande A, Mutegi C, Atehnkeng J, Kaptoge L, et al. Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change. World Mycotoxin J. 2016;9(5):771-789.

    [Crossref] [Google Scholar]

68. Lewis MH, Carbone I, Luis JM, Payne GA, Bowen KL, Hagan AK, et al. Biocontrol strains differentially shift the genetic structure of indigenous soil populations of Aspergillus flavus. Frontier Microbiol. 2019;10:1738.

    [Crossref] [Google Scholar] [PubMed]

69. Senghor LA, Ortega-Beltran A, Atehnkeng J, Callicott KA, Cotty PJ, Bandyopadhyay R. The atoxigenic biocontrol product Aflasafe SN01 is a valuable tool to mitigate aflatoxin contamination of both maize and groundnut cultivated in Senegal. Plant Dis. 2020;104(2):510-520.

    [Crossref] [Google Scholar] [PubMed]

70. Farzaneh M, Shi ZQ, Ghassempour A, Sedaghat N, Ahmadzadeh M, Mirabolfathy M, et al. Aflatoxin B1 degradation by Bacillus subtilis UTBSP1 isolated from pistachio nuts of Iran. Food control. 2012;23(1):100-106.

    [Crossref] [Google Scholar]

71. Nesci AV, Bluma RV, Etcheverry MG. In vitro selection of maize rhizobacteria to study potential biological control of Aspergillus section Flavi and aflatoxin production. European J Plant Pathol. 2005;113(2):159-171.

    [Crossref] [Google Scholar]

72. Reddy KR, Reddy CS, Muralidharan K. Potential of botanicals and biocontrol agents on growth and aflatoxin production by Aspergillus flavus infecting rice grains. Food control. 2009;20(2):173-178.

    [Crossref] [Google Scholar]

73. Tian J, Ban X, Zeng H, He J, Huang B, Wang Y. Chemical composition and antifungal activity of essential oil from Cicuta virosa L. var. latisecta Celak. International J Food Microbiol. 2011;145(2-3):464-470.

    [Crossref] [Google Scholar] [PubMed]

74. Hajare SS, Hajare SN, Sharma A. Aflatoxin inactivation using aqueous extract of ajowan (Trachyspermum ammi) seeds. J Food Sci. 2005;70(1):C29-C34.

    [Crossref] [Google Scholar]

75. Sandosskumar R, Karthikeyan M, Mathiyazhagan S, Mohankumar M, Chandrasekar G, Velazhahan R. Inhibition of Aspergillus flavus growth and detoxification of aflatoxin B1 by the medicinal plant zimmu (Allium sativum L. × Allium cepa L.). World J Microbiol Biotechnol. 2007;23(7):1007-1014.

    [Crossref] [Google Scholar]

76. Velazhahan R, Vijayanandraj S, Vijayasamundeeswari A, Paranidharan V, Samiyappan R, Iwamoto T, et al. Detoxification of aflatoxins by seed extracts of the medicinal plant, Trachyspermum ammi (L.) Sprague ex Turrill–structural analysis and biological toxicity of degradation product of aflatoxin G1. Food Control. 2010;21(5):719-725.

    [Crossref] [Google Scholar]

77. Hacıseferoğulları H, Özcan M, Demir F, Çalışır S. Some nutritional and technological properties of garlic (Allium sativum L.). J Food Engineer. 2005;68(4):463-469.

    [Crossref] [Google Scholar]