Transcript Mycotoxin

Mycotoxins
1
Introduction
Mycotoxins are secondary metabolites of fungi that are
recognized as toxic to other life forms.
“Myco” means fungal (mold) and “toxin” represents poison.
1. Fungal growth
Secondary metabolite: A compound that is not necessary
for growth or maintenance of cellular functions but is
synthesized, generally, for the protection of a cell or microorganism, during the stationary phase of the growth cycle.
Many are used in foods, pharmaceuticals, and other
industrial applications.)
• a. Field fungi : grow under conditions occurring prior to
harvest. (Fusarium)
• b. Storage fungi : do not invade intact grain prior to
harvest. ( Aspergillus & Penicillium)
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2. Characteristics of mycotoxin induced disease
a. Not transmitted among animals
b. Pharmaceutical treatment does not alter the course of
disease
c. Mycotoxicosis most often presents as a uncertain, subacute or chronic condition
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3.Treatment of mycotoxin - induced disease
a. For most mycotoxins, there is no specific treatment or
antidote
b. Supplement with vitamins & selenium may be helpful, and
provision of adequate high-quality protein
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4. Prevention of mycotoxin-induced disease
a. Avoiding
b. Diluting
c. Cleaning
d. Drying
e. Adding (organic acids will prevent mold growth)
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The most important Mycotoxins
A) Aflatoxin
1. Sources
Aspergillus flavus & A. paraciticus :
Corn, peanuts
2. Factor favoring production of aflatoxins
a. Temperature : 25-30 ๐c
b. Grain moisture
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3. Chemical characteristics
Exhibit intense blue or green fluorescence under UV.
: aflatoxins B1, B2, G1 and G2
: aflatoxin M1 is a metabolites of AFB1 found in
animal urine, milk or tissues.
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4. Mechanism of toxicologic damage
hepatic steatosis
Accumulation of large vacuoles
of triglyceride fat in liver cells via
the process of steatosis
Pathogenesis Aflatoxicosis
Aflatoxin bind to guanine in deoxyribonucleic acid (DNA) inhibiting the signal
for the formation of massenger ribonucleic acid (RNA). Interruption of protein
synthesis leads to deficiencies of structural protein. The long term effects of
impaired protein synthesis include hepatic steatosis and variety of metabolic
8 function derangements like:
and
a. Loss of enzyme
b. Lack of formation of lipid acceptor protein in liver
c. Decreased cellulose digestion, volatile fatty acid
formation & proteolysis (breakdown of proteins )
d. Necrosis
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5. Toxicity
• a. Young animals are more susceptible than adult.
• b. Nutrition deficiency increase susceptibility
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6. Diagnosis
• Clinical sign : decreased growth rate, reduced feed
efficiency,,, mild anemia, and increased susceptibility to
infectious disease.
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7. Treatment & Prevention
a. Detoxification : Hydrated sodium calcium aluminosilicate
(HSCAS) can absorb aflatoxins.
b. Supportive : Vitamin .E & selenium
c. Prevention
- Mold inhibitor
- Treatment of grain with anhydrous ammonia for
10-14 days.
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B) Zearalenone
1. Sources : Fusarium roseum
and F. graminearum
corn, wheat, barley, oats
2. Factor favoring production
a. High moisture 22% - 25%
b. Alternating high and low temp. (7-21 ๐c)
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3. Mechanism of toxicological damage
a. initiating specific RNA synthesis
b. Function as a weak estrogen.
4.Toxicity
a. Swine are most susceptible
b. low for all effects except reproductive function.
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C) Ergot
1.Source :
Claviceps purpurea :
barley, wheat & oats
2. Factor favoring :
Warm & humid
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3.Mechanism of toxic
• a. potent initiators of contraction in smooth muscle
• b. mimic the action of dopamine.
Dopamine a simple organic chemical
Dopamine plays a major role in the brain system that is responsible for reward-driven learning
Several important diseases of the nervous system are associated with dysfunctions of the dopamine system
Parkinson's disease
4.Clinical sign
a. necrosis of the feet, ears and tail
b. increased temperature., pulse & respiration rate
c. lactation does not occur
d. hyper-excitability & tremors
e. heat intolerance in cattle
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5. Treatment
a. animals should be provided with a warm, clean,
stress-free environment
b. control secondary bacterial infection
c. milk supplement
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D) Ochratoxin & Citrinin
• 1.Sources : Aspergillus orchraceus &
•
Penicillium viridicatum
• 2. Mechanism of toxic
target the renal proximal tubule
- Disrupt protein synthesis
- Bind strongly to protein (albumin)
- Interfere with synthesis of tRNA & mRNA
- Disrupt carbohydrate metabolism
- Increase the generation of free radical
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4. Clinical sign
a. Acute : vomiting, diarrhea, dehydration & depression
b. Subacute to chronic : weight loss, feed efficiency, & dehydration.
Immunosupression, teratogenicity, carcinogenesis & hemorrhage
‫تشوهات جنينية‬
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Mycotoxins 2
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Mycotoxin
Mycotoxin is a convenient generic term describing the toxic
secondary metabolites produced by fungi.
They encompass a considerable variety of low molecular
weight compounds with diverse chemical structures and
biological activities.
Some mycotoxins could also be toxic to plants or other
microorganisms; but these compounds are not classified as
antibiotics of fungal origin.
Like most microbial secondary metabolites, the benefit of
mycotoxins for the fungi themselves is still not clearly defined.
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• In considering the effects of mycotoxins on animals, it is
important to distinguish between “mycotoxicosis” and
“mycosis.”:
• Mycotoxicosis is used to describe the action of
mycotoxin(s) and is frequently mediated through a
number of organs, notably the liver, kidney, lungs, and
the nervous, endocrine, and immune systems.
• Mycosis” refers to a generalized invasion of living
tissue(s) by growing fungi.
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• Due to their diverse chemical structures, mycotoxins may
exhibit a number of biological effects, including both acute
and chronic toxic effects as well as carcinogenic, mutagenic,
genotoxic, and immunotoxic effects.
• The interaction of mycotoxins with cellular macromolecules
plays a dominant role in their toxic actions.
•
Recent studies on the effect of mycotoxins on apoptosis
have further revealed their mode of action at the cellular
level.
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PRODUCTION OF MYCOTOXINS BY TOXICOGENIC FUNGI
Invasion by fungi and production of mycotoxins in commodities can occur
under favorable conditions in the field, at harvest, and during processing,
transportation and storage
Fungi that are frequently found in the field include: A. flavus,
Alternaria
longipes, A. alternata, Claviceps purpura, Fusarium verticillioides
(previously called moniliforme), F. graminearum, and a number of other
Fusarium spp.
Species most likely introduced at harvest include:
F. sporotrichioides, Stachybotrys atra, Cladosporium sp., Myrothecium
verrucaria, Trichothecium roseum, as well as A. alternata.
Fungi that are frequently found in the storage are mostly from
genus penicillia and include: Penicillium citrinum, P. cyclopium, P.
citreoviride, P. islandicum, P. rubrum, P. viridicatum, P. urticae, P.
verruculosum,
P. palitans, P. puberulum, P. expansum, and P. roqueforti.
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• Other toxicogenic storage fungi are: A. parasiticus, A. flavus, A. versicolor,
A. ochraceus, A. clavatus, A. fumigatus, A. rubrum, A. chevallieri,
Fusarium verticillioides, F. tricinctum, F. nivale, and several other
Fusarium spp.
• It is apparent, most of the mycotoxin producing fungi belong to three
genera: Aspergillus, Fusarium, and Penicillium. However, not all
species in these genera are toxicogenic
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Factors Affecting Mycotoxin Production
• Genetics and environmental and nutritional factors greatly affect the
formation of mycotoxins.
• Depending on the susceptibility of the crop, geographic and seasonal
factors, as well as cultivation, harvesting, storage, and transportation
practices, mycotoxins are found worldwide.
•
In the field, weather conditions, plant stress, invertebrate vectors, species
and spore load of infective fungi, variations within plant and fungal
species, and microbial competition all significantly affect mycotoxin
production.
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Continue Factors Affecting…….
• Physical factors such as time of exposure, temperature during exposure,
humidity, and extent of insect or other damage to the commodity prior to
exposure determine mycotoxin contamination in the field or during
storage.
• Chemical factors including the nutritional status of the crops or chemicals
(such as fungicides) used in crop management could affect fungal
populations, and consequently toxin production
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Continue Factors Affecting…….
• In general, mycotoxins are optimally produced at 24–28C, but some toxins
such as T-2 toxin is maximally produced at 15C.
• Contamination during crop storage may be affected by changes in
temperature and water activity, that allow ecological succession of different
fungi as water activity and temperature of stored grain changes.
• During storage and transportation, water activity (aw), temperature, crop
damage, and a number of physical and chemical factors, such as aeration
(O2, CO2 levels), types of grains, pH, and presence or absence of specific
nutrients and inhibitors are important.
Water activity or aw was developed to account for the intensity with which water associates with various non-aqueous constituents
and solids. Simply stated, it is a measure of the energy status of the water in a system. It is defined as the vapor pressure of a
liquid divided by that of pure water at the same temperature; therefore, pure distilled water has a water activity of exactly one
1) Aflatoxins
Chemical Structure of Different Aflatoxins
A
R3
B
R1
R1
R4
R2
C
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R1
D
R1
• At least 16 structurally related toxins in this group are produced by
Asparagillus flavus and A. parasiticus and infrequently by A.
pseudotamarii and A. nominus A. ochraceoroseus has also been found
to produce aflatoxins
• The optimal temperatures and water activity (aw) for the growth of A.
flavus and A. parasiticus are around 35–37C (range from 6–54C) and
0.95 (range from 0.78–1.0), respectively; whereas for aflatoxin
production, they are 28–33C and 0.90–0.95 (range from 0.83–0.97),
respectively.
• Aflatoxin B1 is most toxic in this group and is one of the most potent
naturally occurring carcinogens).
• Other significant members of the aflatoxin family, such as M1 and M2,
are metabolites of AFB1 and AFB2, respectively, and originally isolated
from bovine milk.
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Natural Occurrence
• Aflatoxins have been found in corn, peanuts ‫ فول سوداني‬and peanut
products, cotton seeds, peppers, rice, pistachios, ‫ فستق‬tree nuts, pumpkin
‫ قرع‬seeds, sunflower seeds and other oil seeds, copra, ‫ جوز هند‬spices, and
dried fruits (figs, raisins).
• Among these products, frequent contamination with high levels of AF in
peanuts, corn, and cottonseed, mostly due to infestation with fungi in the
field, are of most concern.
• Soybeans ‫الصويا‬, beans ‫الفاصولياء‬, pulses (Pea)‫البازالء‬, cassava ‫منيهوت‬,
sorghum ‫ الذرة‬, millet ‫الدخن‬, wheat ‫القمح‬, oats ‫القطن‬, barley ‫الشعير‬, and rice‫رز‬
are resistant or only moderately susceptible to AF contamination in the
field.
•
It should be reiterated that resistance to AF contamination in the field
does not guarantee that the commodities are free of AF contamination
during storage. Inadequate storage conditions, such as high moisture and
warm temperatures (25–308C), can create conditions favorable for the
growth of fungus and production of AF.
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Toxic Effects
• Aflatoxins are mutagenic, teratogenic, and hepatocarcinogenic.
•
Aflatoxin B1 is one of the most potent naturally occurring carcinogen,
extensive research was primarily done on this toxin. The main target
organ of AF is the liver.
• AFB1 also affects other organs and tissues including the lungs and the
entire respiratory system.
•
For the carcinogenic effects, rats, rainbow trout, monkeys, and ducks
are most susceptible and mice are relatively resistant.
• Consumption of AFB1-contaminated feed by dairy cows results in the
excretion of AFM1 in milk. AFM1, a hydroxylated metabolite of AFB1, is
about 10 times less toxic than AFB1; but its presence in milk is of
concern for human health.
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Impact on Human Health
• Whereas AFB1 has been found to be a potent carcinogen in many
animal species, the role of AF in carcinogenesis in humans is
complicated by hepatitis B virus (HBV) infections in humans).
• Epidemiological studies have shown a strong positive correlation
between AF levels in the diet and primary hepatocellular carcinoma.
•
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Since multiple factors are important in carcinogenesis and
environmental contaminants such as AFs and other mycotoxins
may, either in combination with HBV or independently.
2) Ochratoxins
• Ochratoxins, are produced by a number of fungi in the genera Aspergillus
and Penicillium. The largest amounts ochratoxins are made by A.
ochraceus and P. cyclopium.
• Other fungi, such as Petromyces alliceus, Aspergillus ciricus, and
Aspergillus fonsecaeus (both in Aspergillus niger group), have also been
found to produce OA.
• Most of the OA producers are storage fungi and pre-harvest fungal
infection.
• Although most OA producers can grow in a range from 37Cto 48C and at
aw as low as 0.78, optimal conditions for toxin production are narrower
with temperature at 24–25C and aw values .0.97.
• Ochratoxins are produced primarily in cereal grains (barley, oats, corn,
wheat) and mixed feed during storage in temperate climatic conditions,
with levels higher than 1 ppm being reported.
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• OA has been found in other commodities, including beans, coffee, nuts,
olives, raisin, cheese, fish, pork, milk powder, fruit juices wine beer,
peppers.
• OA can be carried through the food chain because of the presence of OA
residues in animal products as result of its binding with serum albumin.
• Natural occurrence of OA in kidneys, blood serum, blood sausage.
Structure of the ochratoxins.
• These metabolites form different classes depending on the nature of
the amide group, and the presence or absence of a chlorine at R2 in the
phenyl group.
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•
Ochratoxin A, the most toxic member of this group of mycotoxins, has
been found to causing kidney damage as well as liver necrosis and
enteritis (Small Intestine) in many animal species.
•
The OA inhibits the activity of different enzymes like, carboxypeptidase
A, renal phosphoenolpyruvate carboxykinase, phenylalaninetRNA
synthetase, and phenylalanine hydroxylase.
•
Formation of free radicals has been considered as one of the
mechanisms for the carcinogenic/toxic effects of OA.
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3) Fumonisins
• Fumonisins (Fm) are a group of toxic metabolites produced primarily by
Fusarium verticillioides, F. proliferatum and other related species readily
colonize corn all over the world. Although F. anthophilum, F. nupiforme, and
F. nygamai are capable of producing Fms.
• More than 11 structurally related Fms (B1, B2, B3, B4, C1, C4, A1, A2,
etc.), have been found since the discovery of FmB1.
• Fumonisins are most frequently found in corn, corn-based foods, and other
grains.
•The level of contamination varies considerably with different regions and
year, ranging from negligible to more than 100 ppm; but is generally
reported to be between 1 and 2 ppm.
• FmB1 is the most common Fm in naturally contaminated samples; FmB2
generally accounts for 1/3 or less of the total. Although production of the
toxin generally occurs in the field, continued production of toxin during
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postharvest storage also contributes to the overall levels.
Toxicological Effects
Fumonisin B1 is primarily a hepatotoxin and carcinogen in rats. Feeding
culture material from F. verticillioides or pure FmB1 to rats resulted in
‫تليف كبدي‬
cirrhosis and hepatic nodules, carcinoma.
Kidney is also a target organ.
Mechanistically, Fms are inhibitors of ceramide synthase
(sphinganine/sphingosine N-acyltransferase), a key enzyme involved in the
biosynthesis of sphingolipids, which are heavily involved in cellular
regulation, including cell differentiation, mitogenesis and apoptosis
The ability of FmB1 to alter gene expression and signal transduction
pathways are considered necessary for its carcinogenic and toxic effects.
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4) Trichothecenes (TCTCs)
a) T-2 toxin,
b) Deoxynivalenol (DON)
Several species of Fusaria infect corn, wheat, barley, and rice.
Under favorable conditions, they elaborate a number of different types of
mycotoxins, more than 100 TCTCs have been identified.
Only a few frequently found in foods and feeds are potentially hazardous to
human and animal health.
Trichothecenes
Other fungal genera elaborate TCTCs are: Myrothecium, Trichoderma,
Trichothecium, Cephalosporium, Verticimonosporium, and Stachybotrys.
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The TCTC mycotoxicoses affect many organs, including the
gastrointestinal tract, nervous, immune, hepatobiliary, and
cardiovascular systems.
Mechanistically, inhibition of protein synthesis is one of the earlier
events in manifestation of TCTC toxic effects and they act at different
steps in the translation process.
Inhibitory effects of these mycotoxins vary considerably with the
chemical structure of the side chain.
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4-a) T-2 toxin
T-2 toxin, a highly toxic type of A TCTC. It is produced by F. tricinctum, F.
sporotrichioides (major), F. poae, F. sulphureum, F. acuminatum, and F.
sambucinum.
Unlike most mycotoxins, which are usually synthesized near 25C, the optimal
temperature for T-2 toxin production is around 15C.
Almost all the major TCTCs, including T-2 toxin, are cytotoxic and cause
hemorrhage, edema, and necrosis of skin tissues.
4-b) Deoxynivalenol (DON)
The DON is a major type B TCTC mycotoxin produced by:
F. graminearum (major) and other related fungi such as F. culmorum
and F. crookwellense.
Because DON causes feed refusal and emesis in swine, the name
“vomitoxin” is also used for this mycotoxin.
Worldwide frequent natural occurrence of DON in cereal grains has
been reported.
Contamination of this toxin in corn and wheat is generally high.
Although inadequate storage may lead to the production of some TCTC
mycotoxins, infestation of Fusaria in wheat and corn in the field is of
most concern for the DON problem
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• With wet and cold weather during maturation, grains are especially
susceptible to F. graminearum infection.
•
The optimal temperature for DON production is about 24C.
• Toxicologically, DON induces anorexia and emesis both in humans
and animals.
• Swine are most sensitive to feed contaminated with DON. Whereas
most TCTCs are immunosuppressors.
• DON is a hyperinducer of cytokines.
Edema is an abnormal accumulation of fluid beneath the skin
Anorexia is the symptom of poor appetite
Cytokines are small cell-signaling protein molecules that are secreted by cells of the nervous system
Mycotoxins and food chain
Fungal contamination
Vegetables
Many accidents
Animal
Production
Elimination
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rare accidents (cancer)
Man
Products
(Animal origin)
I- Preventive Measures
Management of Mycotoxin Contamination
• The economic implications of the mycotoxin problem and its potential
health threat to humans have clearly created a need to eliminate or at
least minimize mycotoxin contamination of food and feed.
• While an association between mycotoxin contamination and inadequate
storage conditions has long been recognized, studies have revealed that
seeds are contaminated with mycotoxins prior to harvest . Therefore,
management of mycotoxin contamination in commodities must include
both pre- and post- harvest control measures
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I-A- Pre-harvest Control
• Mycotoxin contamination can be reduced somewhat by using
of resistant varieties (most effective, but not all are
successful) and earlier harvest varieties:
– crop rotation,
– adequate irrigation,
– control of insect pests.
•
Significant control of toxin contamination is expected to be
dependent on a detailed understanding of the:
– physiological and environmental factors that affect the
biosynthesis of the toxin,
– the biology and ecology of the fungus,
– the parameters of the host plant–fungal interactions.
Efforts are underway to study these parameters primarily
for the most agriculturally significant toxins, namely AFs,
Fms, and TCTCs
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• Use of atoxigenic biocompetitive, native A. flavus strains
to out-compete the toxigenic isolates has been effective in
significantly reducing preharvest contamination with aflatoxin
in cotton and peanuts.
• However, the aflatoxin contamination process is so complex
that a combination of approaches will be required to
eliminate or even control the preharvest toxin contamination
problem.
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I-B- Post-harvest Control
•
After harvest, crop should not be allowed to over-winter in the field
as well as subjected to birds and insects damage or mechanical
damage.
•
Grains should be cleaned and dried quickly to less than 10–13%
moisture and stored in a clean area to avoid insect and rodent
infestation.
•
Postharvest mycotoxin contamination is prevalent in most tropical
countries due to:
•
•
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subadequate methods of harvesting,
a hot, wet climate coupled with handling, and storage practices
which often lead to severe fungal growth and mycotoxin
contamination of food and feed.
• Sometimes contaminated food has been diverted to animal feed to
prevent economic losses and health concerns. However, this is not a
solution to the contamination problem.
• Irradiation has been suggested as a possible means of controlling
insect and microbial populations in stored food, and consequently,
reducing the hazard of mycotoxin production under these conditions .
• Significant emphasis has been placed on detoxification methods to
eliminate the toxins from the contaminated lots or at least reduce the
toxin hazards by bringing down the mycotoxin levels under the
acceptable limits.
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II- Removal or Elimination of Mycotoxins.
• Since most of the mycotoxin burden in contaminated commodities is
localized to a relatively small number or seeds or kernels, removal of
these contaminated seeds/kernels is effective in detoxifying the commodity.
• Methods currently used include removal by :
– (a) physical separation by:
–
–
–
–
–
–
identification and removal of damaged seed;
mechanical or electronic sorting;
flotation and density separation of damaged or contaminated seed;
physical screening and subsequent removal of damaged kernels by air blowing;
washing with water
use of specific gravity methods
All these methods have shown some effect for some mycotoxins, including DON, FmB, AFB1
– (b) filtration and adsorption onto filter pads, clays, activated charcoal,
etc.,
– (c) solvent extraction removal of the mycotoxin by some specific
solvent
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III- Inactivation of Mycotoxins.
When removal or elimination of mycotoxins is not possible, mycotoxins can be
inactivated by:
(a) physical methods such as thermal inactivation, photochemical or gamma
irradiation,
(b) chemical methods such a treatment of commodities with acids, alkalies,
aldehydes, oxidizing agents, and gases like chlorine, sulfur dioxide, NaNO2,
ozone and ammonia,
(c) biological methods such as fermentations and enzymatic digestion that
cause the breakdown of mycotoxins.
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.
• The commercial application of some of these detoxifying mechanisms is
not feasible because, in a number of cases, the methods will be limited
by factors such as:
• the toxicity of the detoxifying agent, nutritional or aesthetic losses
of commodities during treatment, and the cost of the sophisticated
treatment
• Although several detoxification methods have been established for
aflatoxins, only the ammoniation process is an effective and practical
method.
• Other chemicals such as ozone, chlorine, and bisulfite have been tested
and some effect for some mycotoxins was shown in it.
• Solvent extractions have been shown to be effective but are not
economically feasible.
IV- Avoiding Human Exposure
Role of Rigorous Monitoring Programs
A tolerance level of 1 ppm for DON in grains for human consumption has
been set by a number of countries, including the United States. The FmB1
levels established by FDA in 2000 are limited to 5, 20, 60 100, 30, and 10
ppm, in corn and corn by-products to be used for horse and rabbit, catfish
and swine, and mink, poultry, respectively.
Among 77 countries which have regulations for different mycotoxins, eight
have specific regulations for OA, with limits ranging from 1 to 20 mg/kg in
different foods.
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CONCLUSIONS
• Mycotoxins are low molecular weight secondary
metabolites of fungi that are contaminants of agricultural
commodities, foods, and feeds.
• Fungi that produce these toxins do so both prior to
harvest and during storage. Although contamination of
commodities by toxigenic fungi occurs frequently in
areas with a hot and humid climate, they can also be
found in temperate conditions.
• Production of mycotoxins is dependent upon the type of
producing fungus and environmental conditions such as
the substrate, water activity (moisture and relative
humidity), duration of exposure to stress conditions, and
microbial, insect, or other animal interactions.
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• Although occurrences of mycotoxicoses in humans have
been documented, several of these have not been well
characterized, neither has a direct correlation between the
mycotoxin and resulting toxic effect been well established in
vivo.
• Even though the specific modes of action of most of the
toxins are not well established, acute and chronic effects in
prokaryotic and eukaryotic systems, including humans have
been reported.
• The toxicity of the mycotoxins varies considerably with the
toxin, the animal species exposed to it, and the extent of
exposure, age, and nutritional status.
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• Most of the toxic effects of mycotoxins are limited to specific
organs, but several mycotoxins affect many organs. Induction
of cancer by some mycotoxins is a major concern as a chronic
effect of these toxins.
• It is nearly impossible to eliminate mycotoxins from food and
feed in spite of the regulatory efforts at the national and
international levels to remove the contaminated commodities.
This is because mycotoxins are highly stable compounds, the
producing fungi are ubiquitous, and food contamination can
occur both before and after harvest. Nevertheless, good farm
management practices and adequate storage facilities
minimize the toxin contamination problems.
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• A combination of natural biocontrol competition fungi and
enhancement of host-resistance against fungal growth or toxin
production could prevent toxin formation to a very significant
extent.
• Rigorous programs for reducing the risk of human and animal
exposure to contaminated food and feed also include:
• economically feasible
• safe detoxification processes
• dietary modifications.
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• Additional, systematic epidemiological data for human
exposure is needed for establishing toxicological parameters
for mycotoxins and the safe dose for humans.
• It is unreasonable to expect complete elimination of the
mycotoxin problem, but multiple approaches will be needed
to minimize the negative economic impact of the toxins on
the entire agriculture industry as well as their harmful effects
on human and animal health.
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