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 (Blout, 1961).
When this unknown turkey X disease was associated with a groundnut (Arachis hypogea L.)
meal contaminated with secondary metabolites from Aspergilus flavus
(Bennett and Klich, 2003, Perdoncini
M, et al., 2019, Joubrane
K, et al., 2020).
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 (Pleadin
et al., 2014). Both A. flavus and A. parasiticus are
most frequently detected in agricultural products because of their widespread
distribution (Frisvad, J, et al., 2019)
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 (Iqbal et al.,
2015). Aflatoxin contamination depends on Aspergillus species, growing and
storage conditions, management practices employed and other factors (Paterson
and Lima 2010). Aflatoxins
can accumulate through the food chain posing a serious health concern to humans
(Sherif et al., 2009). 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 (Lewis et al.,
2005). Biosynthesis of aflatoxin depends on pH, water activity, insect
infestation and temperature (Molina and Gianuzzi 2002). Climate change is
anticipated to have a pronounced effect on economically important crops and
mycotoxigenic fungal infection and contamination with aflatoxins
(Paterson and Lima, 2010). Undeniably, climate change may have impact on the
interactions between various mycotoxigenic species and the relative mycotoxin
contamination of staple commodities (Magan et al., 2011).
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 (Udomkun et
al., 2017).
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 (Peles,
F.et al., 2021). 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.
1.
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 (Amaike and
Keller, 2011; Baranyi et al., 2013; Cotty et al., 1994; Mahuku et al., 2019). Different types of aflatoxins
have been identified, with aflatoxin B1, B2, G1,
G2, M1 and M2 being the most frequent and
toxic (Akiama et
al., 2001).
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 (Iqbal et al., 2015; Ketney et al.,
2017; Serraino et
al., 2019). A. flavus produces only AFB1
and AFB2, whereas A. parasiticus produces AFB1, AFB2, AFG1 and AFG2 (Creppy, 2002). The
International Agency for Research on Cancer (IARC) has classified AFB1, AFB2, AFG1
and AFG2 as Group 1 mutagens, whereas AFM1
as Group 2B (IARC, 2015). 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 (Sherif et al.,
2009; Jalili M, 2015; Peles
F et al., 2019; Ráduly
Z et al., 2020). In particular,
co-occurrence of mycotoxins is a major concern
because the possible synergetic toxicities are not well known (Palumbo, R, et al., 2020)
High dose exposure of AFs on humans result in
vomiting, abdominal pain, and even possible death, while small quantities of
chronic exposure may lead to liver cancer (Sherif et al. 2009). Aflatoxins play a
significant role in development of edema in malnourished people as well as in
the pathogenesis of kwashiorkor in malnourished children (Coulter et al.,
1986). 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 (Juan et al., 2012). 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 (EC, 2010)
and the US 20 µg/kg (Wu, 2006).
FAO estimates that 25 per cent of the world food crops are affected by
mycotoxins each year and constitute a loss at post-harvest (FAO, 1997). 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 (AMCE, 2010). 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
(AMCE, 2010). 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.
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 (Cotty and Jaime-Garcia, 2007, Valencia-Quintana R,
et al., 2020). 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 (Abdi M, et al., 2021). However, high
contamination and toxin production occur in poorly stored commodities, because
of inadequate moisture and high temperature (Udomkun
et al., 2017). Fungal growth can occur over a wider range of temperatures, pH and water activity levels on maize
(Aldars-garcía L, 2018). Optimum water activity and
temperatures on groundnuts were: 0.94 aw and
34oC for growth and 0.99 aw and
32oC for AFB1 production respectively (Table 1).
Similarly, in maize temperature ranged from 10 to 43oC for fungal
growth and from 13 to 37oC for AFB1 production. Water activity and
temperature range vary for toxin production and for mould
growth (ICMSF, 1996).
Relative humidity between 83%-88% has been
found to be appropriate to influence the mold growth and aflatoxins
production (Agriopoulou, 2020). Hotter and drier summers are predicted which may prevent
certain fungi from contaminating vegetation due to the lack of humidity (West et al., 2012). The germination of the
spores is greatly influenced by humidity and temperature, meaning that any
change in climate will greatly affect these processes (Doohan
et al., 2003; Paterson and Lima, 2010).
Significant
correlations have been reported between agro-ecological zones and aflatoxin
levels, with wet and humid climates after longer storage periods increasing
aflatoxin risk (Hell et al., 2000).
Kaaya et al. (2006) 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 (Atehnkeng et al.,
2014).
When environmental conditions are favorable,
wind and insect dispersal of conidia to plants results in colonization,
infection and within susceptible hosts, production of aflatoxins
(Payne, 2015).
Conidia serve as source of inoculum for secondary infections and reservoirs of A.
flavus for subsequent dispersal to susceptible hosts (Jaime-Garcia and Cotty, 2004). 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 (Dowd
et al., 2005).
3.
Management of aflatoxin producing fungi and aflatoxin
contamination
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 et al.
(2008) 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. Delayed the harvested crop in the field prior to storage
encourages fungal infection and insect infestation (Udoh
et al., 2000). Growths of toxigenic fungi in stored commodities are influenced
by moisture and temperature content. Hell et al. (2008) 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%. To decrease toxin contamination, technological
solutions that assist in decreasing grain moisture quickly have been reviewed
by Udomkun et al. (2017). 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 (Waliyar et al., 2015).
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 (Hell and Mutegi, 2011). Hell et al. (2000)
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. Williams et al. (2014) 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. Njoroge
et al. (2014) recorded less moisture absorbance in grains stored in PICS bags
than grains stored in woven polypropylene bags.
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
(Fandohan et al., 2005). Hell et al. (2008) reported that reduction of aflatoxin in cleaned
stores as compared to non-cleaned stores.
Aflatoxins
contamination in pistachio nuts is reduced by 95% through colour sorting (Shakerardekani et al., 2012). 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 et al. (2005) quantified
fungal infection and mycotoxins produced in maize
grain by Fusarium verticillioides using
Near Infrared Spectroscopy. An additional image based sorting technology has
been forwarded by Ozlüoymak (2014), 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.
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
(Gowda et al., 2004). Jalili
and Jinap (2012) 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. Techniques
other than the use of chemical sorbents and ammonization have achieved
reduction in aflatoxin bioavailability that due to
hydrated sodium calcium aluminosilicate binding (Phillips et al., 1988). 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 (Park and Price,
2001). Although ammonia,
sodium bisulfite, and calcium hydroxide treatments are efficient, they do not
fulfill food safety requirements (Piva et al.,
1995).
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 (Shetty and
Jespersen, 2006). 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 (Dorner et al., 1999) and groundnut (Vijayasamundeeswari et al., 2010; Shifa
et al., 2016). Bandyopadhyay R et a.l
(2016); Lewis M et al. (2019), Senghor,
L.et al (2020) demonstrated that bio
control non-afla toxigenic strains reduced AF
concentrations in treated crops by more than 80% under both field and storage
conditions. 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 (Atehnkeng et al., 2014). Farzaneh
et al. (2012) 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. 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
(Nesci et
al., 2005; Reddy et al., 2009). 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 (Peles F et al., 2021).
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
(Tian et al., 2011). Plant extracts have been
reported to have antifungal activity against aflatoxins
produced by A. flavus and A. parasiticus
(Hajare et al.,
2005; Sandosskumar et al., 2007; Velazhahan et al., 2010). Hajare et
al. (2005) reported an 80% decrease in total aflatoxin
content over the controls after treatment with aqueous extract of Trachyspermum
ammi seeds. Sandosskumar et al. (2007) 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 %. 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. Haciseferogullary et al. (2005)
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. Eighty four per cent reduction in
toxin production occurred at 1% inclusion level.
4.
Policy directions
In order to reduce aflatoxin
contamination policies should focuses on: (1) improving awareness on sources of
aflatoxin contamination along the value chain (farmers, consumers, processors,
and traders) and health impacts; (2) implementing appropriate pre- and
post-harvest Aspergillus fungi control strategies and
(3) developing accessible low cost technologies and infrastructure to monitor
contamination levels.
CONCLUSIONS
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.
Acknowledgements
Not applicable
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