Effects of Mycotoxins in Animal Nutrition: A Review
Mycotoxins are low molecular weight secondary metabolites produced by certain strains of filamentous fungi such as Aspergillus, Penicillium and Fusarium, which invade crops in the field and may grow on foods during storage under favourable conditions of temperature and humidity. They are regularly implicated in toxic syndromes in animals and humans. No region of the world escapes the problem of mycotoxins and its estimated that there are about 300 harmful mycotoxins. Food and Agricultural Organisation (FAO) estimates that about 25% of the world crops contain mycotoxins. Mycotoxins have been detected in various food commodities from many parts of the world and are presently considered as one of the most contaminants of food and feed. Mycotoxins causes mycotoxicoses and their toxicity depends on the amounts ingested, time-span of exposure, type of animal, their breed, age, sex, health status, but also other parameters such as density of animals, diseases and temperature. The mycotoxins of most concern due to their toxicity and occurrence are aflatoxin, vomitoxin, ochratoxin, zearaleone, fumonisin and T-2 toxins. They cause significant economic losses in animals due to reduced productivity, increased disease incidence, chronic damage of vital organs and decreased reproductive performance. Also, the productivity and nutritive value of infected grains and cereals drops after contamination by mould. Animals may have varying susceptibilities to mycotoxins depending on physiological, genetic and environmental factors. Preventing mould growth and subsequent mycotoxin production is essential to the feed manufacturer, livestock producer and for maximum animal performance.
March 07, 2010; Accepted: May 19, 2010;
Published: July 27, 2010
Mycotoxins are low molecular weight secondary metabolites produced by certain
strains of filamentous fungi such as Aspergillus, Penicillium and
Fusarium, which invade crops in the field and may grow on foods during
storage under favourable conditions of temperature and humidity. They are regularly
implicated in toxic syndromes in animals and humans (Smith
et al., 1995; Berry, 1998; Charoenpornsook
and Kavisarasai, 2006). Due to the diversity of their toxic effects and
their synergetic properties, mycotoxins are considered as risky to the consumers
of contaminated foods and feeds (Yiannikouris and Jonany,
2002; Omede, 2008).
Mycotoxins have been detected in various food commodities from many parts of
the world and are presently considered as one of the most dangerous contaminants
of food and animal feed (CAST, 1989; Okoli,
2005; Okoli et al., 2006a,
b, 2007a, b). No region
of the world escapes the problem of mycotoxins and according to Lawlor
and Lynch (2005) and Okoli et al. (2006b),
mycotoxins are estimated to affect as much as 25% of the worlds crops
each year. Mycotoxins are produced only under aerobic condition (Ratcliff,
2002). Adverse effects on animal health and production have been recognized
in intensively farmed animals such as poultry, swine and cattle as a consequence
of the consumption of high levels of cereals and oilseeds in the diet (Smith
and Anderson, 1991; Smith et al., 1994; Charoenpornsook
and Kavisarasai, 2006). Animals may have varying susceptibilities to mycotoxins
depending on physiological, genetic and environmental factors. Most mycotoxins
such as aflatoxin B1, T-2 toxin and ochratoxin A inhibit protein
synthesis (Charoenpornsook and Kavisarasai, 2006). This
inhibition may not be the primary mechanism involved in their immunotoxic effects.
They may have selective effects on various target organs, affect membranes or
interfere with macromolecular synthesis and function. They can directly or indirectly
influence immunological functions. Some of the mycotoxins are neurotoxic or
cause other organ pathology and these compounds may activate endocrine mechanisms
(e.g., stress-induced release of corticosteroids inhibits immune function (Sharma,
Mycotoxins occur sporadically both seasonally and geographically. The formation
of mycotoxins in nature is considered a global problem, however, in certain
geographical areas of the world, some mycotoxins are produced more readily than
others (Devegowda et al., 1998; Ratcliff,
2002; Lawlor and Lynch, 2005). Table
1 shows the mycotoxin that may be found in feeds that come from different
global locations. They occur naturally in a wide variety of feedstuffs used
in animal feeds. In most European countries aflatoxins are not considered to
be a major problem. In contrast, vomitoxin, ochratoxin, zearalenone are found
more frequently. Aflatoxins are common in humid climatic conditions like those
existing in Asian and African countries and certain parts of Australia (Cortyl,
2008). T he problem of m ycotoxins does not just end in animal feed or reduce
animal performance; many become concentrated in meat, egg and milk of animal
and can pose a threat to human health (Akande et al.,
2006). Some examples of foods, of animal origin which may be naturally contaminated
with mycotoxins are shown in Table 2.
Effects of major mycotoxins in poultry and swine
Aflatoxins: Aflatoxins are fluorescent compound, they are chemically classified
as difurocoumarolactones and their biosynthesis by the producing fungi is via
polyketide pathway (Smith and Moss, 1985; Akande
et al., 2006). Aflatoxins are the most well known mycotoxins and
extensive research has been done about these mycotoxins. There are four major
aflatoxins produced in feedstuffs: Aflatoxin B1, Aflatoxin B2,
Aflatoxin G1 and Aflatoxin G2. Today, it is agreed that
only four species of fungi produce aflatoxins.
|| Some food of animal origin which may be naturally contaminated
|Source: FAO (1998)
They are namely, Aspergillus flavus, Aspergillus parasiticus,
Aspergillus nomius and Aspergillus pseudotamarii (Kurtzman
et al., 1987; Payne, 1998;
Ito et al., 2001; Cortyl, 2008). However,
only A. flavus and A. parasiticus are economically important.
Aflatoxins are produced when adequate substrate and favourable environmental
conditions are present (tropical and subtropical climates, humid storage conditions).
While young animals are most susceptible to the effects of aflatoxin, all ages
are affected. Aflatoxin causes a variety of symptoms depending on the animal,
dose, length of exposure, species, breed and diet or nutritional status. However,
in all animals, aflatoxin can cause liver damage, gastrointestinal dysfunction,
reduced productivity, decreased feed utilization and efficiency, decreased reproductive
performance, reduced milk or egg production, embryonic death, teratogenicity
(birth defects), tumours and suppressed immune system function, even when low
levels are consumed (Jones et al., 1994; Cortyl,
2008). According to Devegowda et al. (1998),
aflatoxins are immune-suppressors and have different effects on pigs, varying
from poor growth rates in weaners and finishers to abortion and agalactia in
sows. Reports have that the first sign of an aflatoxin problem is decreased
feed intake and depending on the levels present, losses can result from deaths,
reduced growth rates, poor feed conversion efficiency and carcass condemnations.
Levels in excess of 0.5ppm in the diet of lactating sows will reduce piglet
growth rates due to aflatoxins in milk. For grower/finisher pigs reduced growth
rates can be expected at concentrations in excess of 0.2 ppm (Devegowda
et al., 1998).
In poultry, ducks are the most sensitive to aflatoxins, followed by turkey,
broiler and layers. Duration of exposure, as well as age, is as important as
the level of aflatoxins in feed. The following symptoms have been observed following
contamination with aflatoxins in poultry: fatty liver, kidney disorders, leg
and bone problems, pigmentation problems (carcasses, egg yolk), reduced hatchability,
smaller eggs and reduced eggshell quality, coccidiosis, vaccine failure, reduced
immunity, lower resistance to diseases, bacteria, viruses and of course reduced
performance (Cortyl, 2008).
Dersjant-Li et al. (2003) studied the impact
of low concentrations of aflatoxin, deoxynivalenol or fumonisins in diets on
growing pigs and poultry. In this study, they used simple linear regression
to summarize different trials from the literature and estimated the relationship
between mycotoxin level and for example, growth rate. The researchers estimated
that for each additional part per million (ppm) of aflatoxin in the feed, the
growth rate of pigs is depressed by 16%. For instance, a level of 0.3 ppm aflatoxin
in feed would result in a 5% reduction in daily weight gain when compared to
a non contaminated feed. For deoxynivalenol, the reduction in daily weight gain
was estimated at about 8% for each additional ppm. Similarly, it was calculated
that growth performance of pigs is reduced by 0.4% for each additional ppm of
fumonisins in the diet.
Ochratoxins: They are metabolites produced by certain species of the
genera Aspergillus and Penecillium (Wood,
1992). Ochratoxin A (OTA or OA) is the major metabolite of toxicological
significance and it is mainly a contaminant of cereal grains. There are other
compounds in this group, but they are less toxic. Aspergillus ochraceus produces
OTA in hot climates, while Penicillium verrucosum produces it in temperate
Ochratoxin A is teratogenic in rat, hamster and chick embryo and is an inhibitor
of hepatic mitochondrial transport systems (Akande et
al., 2006). Ochratoxin A is a nephrotoxin and has also been reported
to cause damage to the liver, gut, lymphoid tissue and renal tubular damage
particularly at higher doses (Harwig et al., 1974).
In poultry, OTA is often reported to have damaging effects and symptoms are
increased mortality, reduced growth and decreased feed conversion ratio and
feed refusal. At higher doses, one can observe diarrhoea, tremors and other
neural malfunctions (Cortyl, 2008). In laying birds,
OTA also reduces egg production and quality (Cortyl, 2008).
Gentles et al. (1999) have demonstrated the
negative effect of 2.5 ppm of OTA in feed of young broiler chickens. After 3
weeks, their body weights were reduced by 23% when compared to controls, while
feed conversion ratio was comparable. Stoev et al.
(2002) observed a dramatic effect of 5 ppm on bodyweight of chicks (-61%
after 42 days) while a level of 1 ppm resulted in a loss of 18%.
In pigs, OTA causes a typical disease called porcine nephropathy (kidney damage).
This can result in rejection of carcasses at the slaughter house. Indeed, OTA
has an affinity with serum proteins (it is bound to them), which makes it quite
stable. It can be found in pig meat and meat products. OTA also affects fertility
of boars. It crosses the placental barrier and can affect the development of
foetuses. Tail necrosis sometimes observed in newborn piglets is often associated
with OTA (Cortyl, 2008).
Zearalenone: Also called ZON, Zea, or ZEN. It is a non-steroidal estrogenic
mycotoxin produced by Fusarium fungi, mainly Fusarium graminearum (Gibberella
zeae and Fusarium culmorum) (Marasas et al.,
1984). It mimics the effects of the female hormone, oestrogen (Okoli
et al., 2008). At high concentrations (1-30 ppm), it can interfere
with ovulation, conception, implantation and foetal development. In pregnant
sows it can increase the incidence of abortions and still births, reduce litter
size and piglet viability. It may increase the weaning to service interval (Jones
et al., 1994). Young gilts are most sensitive, with concentrations
as low as 0.5 to 1 ppm causing pseudo-oestrus and vaginal or rectal prolapse.
The most striking clinical feature is the swollen red vulva of immature gilts.
Young boars may have reduced libido and decreased testicular size but mature
boars are rarely affected (Jones et al., 1994).
In poultry, Cortyl (2008) reported that Zearalenone
appears to be well tolerated by poultry. Chi et al.
(1980) observed that a single oral ingestion of 15 g kg-1 bodyweight
was not toxic. Allen et al. (1981) reported that
up to 800 ppm of ZON in feed from 6-9 weeks of age does not affect performance
of broilers. Allen et al. (1983) reported the
opposite for turkey. He observed reduced egg production (-20%) with 100 ppm
for 56 days.
Tricothecenes: This is a group of toxic fungal metabolites based on
the structure (6) and which are produced by a number of species of the genus
Fusarium. Trichothecenes are divided in 2 groups. Group A trichothecenes
include T-2 toxin, HT-2 toxin and diacetoxyscirpenol (DAS). Common group B trichothecenes
are deoxynivalenol (DON or vomitoxin), nivalenol (NIV) and Fusarenon X. T-2
toxin has been the most extensively studied tricothecene in poultry and it has
been found that the primary effect of T-2 toxicosis in young broiler chicks
is oral necrosis (Jewers, 1990). The ability of the three
tricothecenes, diacetoxyscirpenol, croticin and T-2 toxin, to cause oral necrosis
and to affect bodyweight gain has been studied in growing chicks. Jewers
(1990) reported that at a dietary inclusion rate of 5 ug g-1
of diacetoxyscirpenol, a bodyweight reduction of 24% resulted, whereas T-2 toxin
produced an 11% reduction at the same incorporation rate. A more severe oral
response was observed with diacetoxyscirpenol. No effect on bodyweight gain
or oral inflammation or necrosis was observed with croticin fed at10 ug g-1.
It is generally regarded that the presence of oral lesions in poultry is the
primary means of diagnosing tricothecene toxicoses in the field.
Dietary T-2 toxin has also been found to affect the nervous system by producing
an abnormal positioning of the wings, hysteroid seizures, or an impaired righting
reflex. In addition, it can induce abnormal feathering, drastically decrease
feed intake without impairing feed efficiency, decrease egg production and cause
thinning of egg shells and destruction of the haemotopoietic system (Wyatt,
1979). Jones et al. (1994) reported that T-2
toxin has been implicated to cause mouth and intestinal lesion as well as impair
the bird=s immune response, causing egg production declines, decreased feed
consumption, weight loss and altered feather patterns. Turkeys are also very
sensitive to T-2 toxin (reduced growth, beak lesions, reduced immunity). Kubena
et al. (1987) reported that DON at 18 ppm in feed of Leghorn chickens
did not affect their weight gain. However, nivalenol was reported to have negative
effects in poultry. Hedmand et al. (1995) studied
the effect of different doses of NIV in feed of 7 day old male broiler chickens.
Bodyweight gain was reduced by 11% for levels of 6 and 12 ppm, while at lower
doses no effect was observed. Feed intake and feed conversion ratio were also
affected. Gizzard erosions were found in one third of the birds given a feed
containing 12 ppm NIV and in 8% of those fed 3 or 6 mg kg-1. Such
damages were not observed in the control group. Also, absolute and relative
liver weights were reduced with levels of 6 and 12 ppm. Garaleviciene
et al. (2002) studied the effects of NIV in laying hens. For 7 weeks,
White Leghorn hens (55 weeks old) were given access to diets containing 0, 1,
3 or 5 ppm NIV. Feed intake was reduced by NIV, but there were no apparent effects
on bodyweight, egg production and egg quality. However, pathological examination
of the birds at the end of the trial revealed that 40 to 75% of hens fed a diet
containing NIV (3 and 5 ppm) had gizzard lesions, haemorrhages in the duodenum
and swollen cloaca and oviducts with immature eggs. Some of the birds in the
1 ppm NIV group had light and fragile livers.
Deoxynivalenol and T-2 toxin appear as the most harmful trichothecenes in pigs.
T-2 toxin and other type A Trichothecenes causes reduced productivity at feed
concentrations of 200 ppb or less. In sows, infertility with some lesions in
the uteri and ovaries can be observed after a feed contaminated with 1 to 2
ppm of T-2 toxin has been consumed. DON causes a disease called moldy corn toxicosis
of swine. The grain is unpalatable to pigs; feed intake is reduced and results
in poor weight gain or even weight loss, increased incidence of infectious diseases
and digestive disorders (Cortyl, 2008). In the farrowing
house, DON causes failure of mature sows to return to oestrus, reduced efficiency,
but also intestinal tract inflammation and acute diarrhoea of suckling piglets,
resulting in high mortality (Cortyl, 2008). Etienne
et al. (2006) also observed the negative effect of DON in sow feed
during lactation. When comparing a control group to a group of sows fed with
a diet containing 2 ppm of DON, they observed that the feed intake was depressed
by 21% on the whole lactation period. As a result, daily weight gain of the
piglets was less in the contaminated group (237 vs. 274 g day-1)
even if the difference was not significant due to high variability. The sows
eating the feed containing the mycotoxin lost more body weight (25.8 kg vs.
17.5 kg) during lactation than their counterparts. This is of course primarily
due to their lower feed intake.
Fumonisins: The fumonisins are a group of compounds originally isolated
from Fusarium moniliforme (Gelderblom et al.,
1988). Six different fumonisins (FA1, FA2, FB1,
FB2, FB3 and FB) have been reported, the A series are
amides and the B series have a free amine (Gelderblom et
al., 1992). In most animals fumonisin impairs immune function, causes
liver and kidney damage, decreases weight gains and increases mortality rates.
It also causes respiratory difficulties in swine (Jones et
al., 1994). The fumonosins (FB1 and FB2) have
been isolated from Fusarium moniliforme cultures and found to promote
cancer in rats (Gelderblom et al., 1988). These
toxins occur naturally in corn and have been associated with equine leukoencephalomalacia
(Ross et al., 1990). They often happen jointly
with other mycotoxins (aflatoxins, DON and ZON).
In poultry, relatively high levels are required to observe negative effects
of fumonisins (Cortyl, 2008). Broomhead
et al. (2002) report that feed intake, body weight gain and feed
conversion of chicks were not affected by fumonisin B1, despite levels
of 25 or 50 ppm was used. Ledoux et al. (1992)
observed that levels of 100 to 400 ppm were detrimental to the performances
in the case of day-old chicks. Kubena et al. (1987)
studied the effects of fumonisin B1, combined or not with Diacetoxyscirpenol
and OTA in Turkey. Reduced weight gain was observed with 300 ppm of fumonisin
B1. The reduction was 30% after 3 weeks when compared to control.
The feed conversion ratio was also affected. Since the toxicity of fumonisins
and DAS (or fumonisins and OTA) appeared to be additive, the authors stated
that even if a level of 300 ppm is very unlikely under practical conditions,
combinations of different mycotoxins at lower levels might put poultry at risk.
In pigs, the main symptom of fumonisin B1 exposure is called PPE
(porcine pulmonary oedema) which affects lungs and heart. At lower levels, liver
and pancreas damage can be observed, as well as immunosuppression. Production
parameters can also be affected: reduced weight gain (above 2 ppm), increased
FCR and reduced performances (Cortyl, 2008).
Effects of mycotoxins on ruminants: Ruminants such as cattle, sheep,
goats and deer are less known for their sensitivity to the negative effects
of mycotoxins than are non-ruminants. However, production (milk, beef, or wool),
reproduction and growth can be altered when ruminants consume mycotoxin-contaminated
feed for extended periods of time (Hussein and Brasel, 2001).
Beef and dairy cattle, sheep, goats and deer are among ruminants that have been
investigated. Acute aflatoxicosis in cattle has been thoroughly described. Clinical
signs consist of reduced feed consumption, dramatic drops in milk production,
weight loss, liver damage and reduced immune system function and rumen metabolism
in cattle (Bodine and Mertens, 1983, Lawloy
and Lynch, 2001). Increasing AF in cattle feed to levels such as 10, 26,
56.4, 81.1 and 108.5 μg kg-1 has been shown to significantly
reduce feed intake at each level in a dose-dependent manner (Choudhary
et al., 1998). In a 155 day feeding trial, AFB1 (600 μg
kg-1) was shown to depress feed efficiency and rate of gain in steers
(Helferich et al., 1986). Decreased feed efficiency
in cattle has been attributed to compromised ruminal function by reducing cellulose
digestion, volatile fatty acid production and rumen motility (Cook
et al., 1986; Helferich et al., 1986;
Diekrman and Green, 1992). Several mechanisms of bovine
immunosuppression by AFB1 have been illustrated in vitro.
Paul et al. (1977) demonstrated that AFB1
suppressed mitogen-induced stimulation of peripheral lymphocytes. In another
study of Bodine et al. (1984), AFB1
was shown to inhibit bovine lymphocyte blastogenesis. In a study by Cook
et al. (1986), radio telemetry was used to measure rumen motility
in cattle and the results showed that AF administration (200-800 μg kg-1)
slowed rumen motility in a dose-dependent manner. Ochratoxins, on the other
hand, do not cause significant toxicity to cattle when fed alone in naturally
occurring doses. Barley naturally-contaminated with OTA (390-540 μg kg-1)
and low levels of AFB1 (12-13 μg kg-1) did not induce
any significant clinical symptoms in 12 week-old calves. The absence of a toxic
effect may have been due to the ruminal microbial degradation and detoxification
(Patterson et al., 1981). Chronic exposure of
a dairy herd to aflatoxin contaminated corn (120 ppb) resulted in severe herd
health problems, including the birth of small, unhealthy calves, diarrhoea,
acute mastitis, respiratory disorders, prolapsed rectum, hair loss and reduced
feed consumption (Charoenpornsook and Kavisarasai, 2006).
Aflatoxins also affect the quality of milk produced by dairy cows and result
in carry-over of AFM1 from AF-contaminated feed (Applebaum
et al., 1982). In the study by Applebaum et
al. (1982), 10 ruminally-canulated lactating Holstein cows were given
AFB1 (13 mg per cow daily) via the rumen orifice for 7 days. Levels
of AFM1 in the milk of the treated cows ranged from 1.05 to 10.58
ng L-1. The AFB1-treated cows also had a significant reduction
in milk yield. In another study of Veldman et al.
(1992), the carry-over rate was shown to be higher (6.2 vs. 1.8) in early
lactation (2-4 week) when compared with late lactation (34-36 week).
The T-2 toxin is also believed to induce immunosuppression in cattle (Black
et al., 1992) by decreasing serum concentrations of IgM, IgG and
IgA (Mann et al., 1983), neutrophil functions
and lymphocyte blastogenensis (Mann et al., 1984)
and the response of lymphocytes to phytohemagglutinin (Mann
et al., 1984). This toxin was also shown to induce necrosis of lymphoid
tissues (Buening et al., 1982). Bovine infertility
and abortion in the final trimester of gestation also have resulted from consumption
of feed contaminated with T-2 toxin (Placinta et al.,
1999). Calves consuming T-2 toxin at 10-50 mg kg-1 of feed have
demonstrated ulcers in the abomasums and sloughing of the papilla in the rumen
(Cheeke, 1998a). A case investigation of dairy cattle
fed moldy corn containing 1 mg kg-1 T-2 toxin resulted in hemorrhagic
syndrome (Hsu et al., 1972). With the exception
of T-2 toxin, cattle have not been adversely affected by tricothecenes (Helferich
et al., 1986). Neither DON nor DAS are known to affect cattle health
or performance in the feedlot (Dicostanzo et al.,
1996). Charmley et al. (1993) has shown that
DON at levels as high as 6 mg kg-1 of feed had no adverse effects
on milk yield and did not show evidence of carry-over into milk. Zearelenone
has been suggested as a causative agent of infertility, reduced milk production
and hyperestrogenism in cattle (D'Mello and MacDonald, 1997).
Fescue foot, hyperthermia and fat necrosis in cattle have been linked to consumption
of tall fescue parasitized with Acremonium coenophialum (Cheeke,
1998b). Cattle consuming tall fescue contaminated with endophytic fungi
such as A. lolii also have shown symptoms of staggers, excitability,
increased rectal temperature, increased respiration rate and loss of body weight
(Ross et al., 1989).
Early studies suggested sheep as the most resistant species to mycotoxicosis
(Hussein and Brasel, 2001). Wogan,
(1966) illustrated a high LD50 (500 mg kg-1) in ovines
fed AF. However, lower LD50 of AF (e.g., 2 mg kg-1) have
been established (Miller and Wilson, 1994) by injection
of AF in sheep. As reviewed by Hussein and Brasel, (2001),
several studies, however, have shown notable effects of AF on sheep. Harvey
et al. (1995) showed that feeding diets contaminated with AF (79%
AFB1, 16% AFG1, 4%% AFB2 and 1% AFG2)
to ewe lambs (2.5 or 5.0 mg kg-1 of feed for 35 days) resulted in
hepatotoxicity. In another study (Fernandez et al.,
1997), lambs fed AF at 2.5 mg kg-1 of feed daily for 21 days
showed symptoms of clinical aflatoxicosis including hepatic and nephritic lesions,
altered mineral metabolism and increased size and weight of the liver and kidney.
Another study of Ramos et al. (1996) with the
same daily dose of AF (2.5 mg kg-1 of feed) examined the plasma mineral
concentrations on day 1, 2, 4 and 8 of the initial dose. On day 4 of intoxication,
significant reductions in plasma mineral concentrations were detected for Ca
(2.39 vs. 2.06 mM), P (2.95 vs. 2.50 mM), Mg (0.88 vs. 0.77 mM), K (4.40 vs.
3.81 mM) and Zn (13.2 vs. 11.6 μM). The resulting mineral deficiencies
due to aflatoxicosis were attributed to lower feed intake and to the liver and
kidney malfunctions as a result of AF intoxication. Exposure of lambs to AF
(2.5 mg kg-1 of feed for 3 week) revealed changes in extrinsic coagulation
factors as determined by increased fibrinogen concentration (Fernandez
et al., 1995). In a study by Fernandez et
al. (2000), 5 month old lambs were given feed contaminated with AF (2
mg kg-1 of feed) for 37 days. Average daily gain on day 35 of feeding
AF was significantly reduced from 125 to 79 g and the exposed lambs showed decreased
cellular immunity. After allowing for a clearance period of 30 days, the AF-exposed
lambs had average daily gain and cellular immunity similar to those for the
controls. Mechanisms for cellular immune response to AF in sheep have not been
elucidated. Contrary to in vitro findings indicating inhibition of bovine
lymphocyte blastogenesis by AF (Bodine et al., 1984).
Edrington et al. (1994) could not prove that
ovine mitogen-induced lymphocyte blastogenesis occurs in vivo. Fusaria
mycotoxins at high doses also appear to have some negative effects on sheep.
Exposing sheep to DON (15.6 mg kg-1 of feed) for 28 days had no effects
on average daily gain, hemacytology parameters, or liver function (Harvey
et al., 1986). However, weight loss (-0.6 vs. 2.4 kg day-1)
was reported after 34 days of feeding DAS (5 mg kg-1 of feed) to
lambs. Further weight loss (-2.7 vs. 24 kg day-1) also was reported
at 34 days of feeding lambs same level of DAS in combination with AF (2.5 mg
kg-1 of feed) suggesting a synergistic effect (Harvey
et al., 1995). It has been suggested that high dietary levels (12
mg kg-1 of feed) of ZEN for extended periods of time (10 days) may
affect reproductive performance of sheep negatively by reducing fertility and
ovulation rates (Dicostanzo et al., 1996). Fumonisins
at high doses (11.1-45.5 mg kg-1 of body weight) have been demonstrated
as acutely and fatally nephrotoxic and hepatotoxic in lambs (Edrington
et al., 1995). Perennial rye grass staggers have been observed in
sheep consuming rye grass contaminated with A. lollii. Symptoms have
included shaking with loss of coordination and inability to walk (Cheeke,
1998b). Staggers have been demonstrated when A. lolii-contaminated
rye grass had lolitrem B toxin at levels of 2.0-2.5 mg kg-1 (DiMenna
et al., 1992).
Ruminants other than cattle and sheep have shown variable resistance to mycotoxins
(Hussein and Brasel, 2001). Levels of AF at 95 mg kg-1
of feed offered to weanling goats had no effects on bodyweight gain and did
not show any noticeable signs of toxic effects (Gurung et
al., 1998). Signs of toxic effects were only detected through serum
profile and sphingolipid analysis. In a study with white-tailed deer fawn fed
800 mg kg-1 AF over an 8 week-period (Quist et
al., 1997), acute injuries in the liver were indicated by increased
serum bile acid concentrations and hepatic lesions.
Economic impact of mycotoxins: Mycotoxins have significant economic
and commercial impact, in that both the productivity and nutritive value of
the infected cereal and forage is affected (Ratcliff, 2002).
Also, its significant economic losses are associated with their impact on human
health, animal productivity and both domestic and international trade. It is
estimated that 25% of the world's food crops, including many basic foods, are
affected by mycotoxin producing fungi. According to FAO estimates global losses
of foodstuffs due to mycotoxins are in the range of 1000 million tonnes per
The nutritive value of grains and cereals drops after contamination by mould.
Contamination by moulds affects both the alimentary value and organoleptic characteristic
of feed and entails a risk of toxicosis. The biological effects of mycotoxins
depend on the ingested amounts, number of occurring toxins, duration of exposure
to mycotoxins and animal sensitivity (Akande et al.,
2006). Also mycotoxins can induce health problems that are specific to each
toxin or affect the immune status of animals, favouring infections. This is
the major reason for the difficulty of diagnosing mycotoxicoses (Yiannikouris
and Jonany, 2002). Mycotoxins produce a wide range of harmful effects in
animals. The economic impact of reduced animal productivity, increased incidence
of disease due to immunosuppression, damage to vital organs and interference
with reproductive capacity is many times greater than the impact caused by death
due to mycotoxin poisoning (Akande et al., 2006).
Mycotoxins in combination appear to exert greater negative impact on the health
and productivity of livestock in comparison to their individual effects (Smith
and Seddon, 1998).
There are multiple criteria for assessing the economic impact of mycotoxins
on humans and on animal agriculture. Considerations include loss of human and
animal life, health care and veterinary care costs, loss of livestock production,
loss of forage crops and feeds, regulatory costs and research cost focusing
on relieving the impact and severity of the mycotoxin problem (Hussein
and Brasel, 2001). Formulas for worldwide economic impact have been difficult
to develop and therefore, most reports on economic impact are on a single aspect
of mycotoxin exposure or contamination (Hussein and Brasel,
Studies have shown extensive mycotoxin contamination in both developing and
developed countries. Surveillance studies (Placinta et
al., 1999) showed that worldwide contamination of cereal grains and
other feeds with Fusarium mycotoxins is a global concern. In Yugoslavia,
studies on mycotoxigenic fungi in raw milk have indicated that 91% of the samples
tested were contaminated (Skrinjar et al., 1995).
In the US, a study was conducted in seven Midwestern states in 1988-1989 and
found mycotoxins in 19.5% of corn samples assayed prior to any induced environmental
stress and 24.7% of the samples following stress induction (Russel
et al., 1991). Shane (1994) estimated the
1980 losses due to AF in corn of eight South-Eastern states at 97 million dollars
with additional 100 million dollars in production losses at hog farms feeding
the contaminated corn.
In India, a study in the Bihar region from 1985 to 1987 (Ranjan
and Sinha, 1991), nearly 51% of the 387 samples tested were contaminated
with molds. Of the 139 samples containing AF, 133 had levels above 20 μg
kg-1. In another study (Phillips et al.,
1996), levels as high as 3700 μg kg-1 of AF was reported
in groundnut meal used for dairy cattle. Researchers also found 21 of 28 dairy
feed samples from farms in and around Ludhiana and Punjab to be contaminated
with AFB1 at levels ranging from 50 to 400 μg kg-1
(Dhand et al., 1998). It was estimated that 10
million dollars were lost in India's export within a decade due to groundnut
contamination with mycotoxins (Vasanthi and Bhat, 1998).
In Thailand, determination of mycotoxins showed that aflatoxin B1 was detected
in 23/25 samples (92%) and the average was 7.56 ppb. Ochratoxin A was detected
in 3/10 samples (30%) in levels of 10.48, 11.14 and 12.35 ppb. Deoxynivalenol
was detected in 13/15 samples (86%) and the average was 33.77 ppb. T-2 toxin
was detected in all samples (10 samples) and the average was 6.91 ppb. Extent
of mycotoxins contamination was determined from 10 samples. The results revealed
that 3 out of 10 samples were contaminated with 4 mycotoxins (aflatoxin B1,
ochratoxin A, deoxynivalenol and T-2 toxin) and 7 out of 10 samples were contaminated
with 3 mycotoxins (aflatoxin B1, deoxynivalenol and T-2 toxin) (Charoenpornsook
and Kavisarasai, 2006).
These results suggest a high risk for human health because of the possibility of indirect exposure through meat and other products from animals consuming contaminated feedstuffs.
It is clear that mycotoxins will be of increasing importance for all those involved in feed manufacturing, farming and food production. Mycotoxins are harmful to animals and can greatly affect their performances and productivity. Because there is a wide range of different mycotoxins, with different chemical structures, a simple approach cannot efficiently solve the problem. Quality of raw materials, prevention of the occurrence of mycotoxins, control and testing systems are all essential to reducing the exposure of humans and animals to mycotoxin.
Akande, K.E., M.M. Abubakar, T.A. Adegbola and S.E. Bogoro, 2006. Nutritional and health implications of mycotoxins in animal feeds: A review. Pak. J. Nutr., 5: 398-403.
CrossRef | Direct Link |
Allen, N., A. Peguri, C.J. Mirocha and J.A. Newman, 1983. Effects of Fusarium cultures, T-2 toxin and zearalenone on reproduction of turkey females. Poult. Sci., 62: 282-289.
PubMed | Direct Link |
Allen, N.K., C.J. Michora, G. Weaver, S. Aakhus-Allen and F. Bates, 1981. Effects of dietary zearalenone on finishing broiler chickens and young turkey poults. Poult. Sci., 62: 124-131.
Applebaum, R.S., R.E. Brackett, D.W. Wiseman and E.H. Marth, 1982. Response of dairy cows to dietary aflatoxin: Feed intake and yield, toxin content and quality of milk of cows treated with pure and impure aflatoxin. J. Dairy Sci., 65: 1503-1508.
Berry, C.L., 1998. The pathology of mycotoxin. J. Pathol., 154: 301-311.
Black, R.D., D.S. McVey and F.W. Oehme, 1992. Immunotoxicity in the bovine animal: A review. Vet. Human Toxicol., 34: 438-442.
Bodine, A.B. and D.R. Mertens, 1983. Toxicology, Metabolism and Physiological Effects of Aflatoxin in the Bovine. In: Aflatoxin and in Corn. Diener, U.L., R.L. Asquith and J.W. Dickens (Eds.). Alabama Ag. Exp. Sta., Auburn University, Alabama, pp: 46-50.
Bodine, A.B., S.F. Fisher and S. Gangjee, 1984. Effect of aflatoxin B1 and major metabolites on phytohemeagglutinin-stimulated lymphoblastogenesis of bovine lymphocytes. J. Dairy Sci., 67: 110-114.
Broomhead, J.N., D.R. Ledoux, A.J. Bermudez and G.E. Rottinghaus, 2002. Chronic effects of fumonisin B1 in broilers and turkeys fed dietary treatments to market age. Poult. Sci., 81: 56-61.
Direct Link |
Buening, G.M., D.D. Mann, B.S. Hook and G.D. Osweiller, 1982. The effect of T-2 toxin on bovine immune system: Cellular factors. Vet. Immunol. Immunopathol., 3: 411-418.
CAST, 1989. Mycotoxins: Economic and health risks. Task Force Report 16. Council for Agricultural Science and Technology, Ames, IA.
Charmley, E., H.L. Trenholm, B.K. Thompson, D. Vudathala and J.W.G. Nicholson et al., 1993. Influence of levels of deoxynivalenol in the diet of dairy cows on feed intake, milk production and its composition. J. Dairy Sci., 76: 3580-3587.
Charoenpornsook, K. and P. Kavisarasai, 2006. Mycotoxins in animal feedstuff of Thailand. KMILT Sci. Tech. J., 6: 25-28.
Direct Link |
Cheeke, P.R., 1998. Mycotoxins in Cereal Grains and Supplements. In: Natural Toxicants in Feeds, Forages and Poisonous Plants, Cheeke, P.R. (Ed.). Interstate Publishers Inc., Danville, IL., pp: 87-136.
Cheeke, P.R., 1998. Mycotoxins Associated with Forages. In: Natural Toxicants in Feeds, Forages, and Poisonous Plants, Cheeke, P.R. (Ed.). Interstate Publishers Inc., Danville, IL., pp: 243-274.
Chi, M.S., G.J. Mirocha, G.A. Weaver and H.J. Kurtz, 1980. Effect of zearalenone on female white leghorn chickens. Applied Environ. Microbiol., 39: 1026-1030.
Direct Link |
Choudhary, P.L., R.S. Sharma, V.N. Borkhataria and M.C. Desai, 1998. Effect of feeding aflatoxin B1 on feed consumption through naturally contaminated feeds. Indian J. Anim. Sci., 68: 400-401.
Cook, W.O., J.L. Richard, G.D. Osweiller and D.W. Trampel, 1986. Clinical and pathologic changes in acute bovine aflatoxicosis: Rumen motility and tissue and fluid concentrations of aflatoxins B1 and M1. Am. J. Vet. Res., 47: 1817-1825.
Cortyl, M., 2008. Mycotoxins in animal nutrition-problems and solutions. http://www.aquafeed.com/docs/fiaap2008/Cortyl.pdf.
D'Mello, J.P.F. and A.M.C. Macdonald, 1997. Mycotoxins. Anim. Feed Sci. Technol., 69: 155-166.
Direct Link |
Dersjant-Li, Y., M.W.A. Verstegen and W.J.J. Gerrits, 2003. The impact of low concentrations of aflatoxin, deoxynivalenol of fumonisin in diets on growing pigs and poultry. Nutr. Res. Rev., 16: 223-239.
PubMed | Direct Link |
Devegowda, G., M.V.L. Radu, A. Nazar and H.V.L.M. Swamy, 1998. Mycotoxin picture worldwide: Novel solutions for their counteraction. Proceedings of Alltech's 14th Annual Symposium on Biotechnology in Feed Industry: Passport of the Year 2000, (BFI`98), Nottingham University Press, pp: 241-255.
Dhand, N.K., D.V. Joshi and S.K. Jand, 1998. Aflatoxins in dairy feeds/ingredients. Indian J. Anim. Nutr., 15: 285-286.
DiMenna, M.E., P.H. Mortimer, R.A. Prestidge, A.D. Hawkes and J.M. Sprosen, 1992. Lolitrem B concentrations, counts of Acremonium lolii hyphae and the incidence of ryegrass stagger in lambs on plots of A. lolii-infected perennial ryegrass. N. Z. J. Agric. Res., 35: 211-217.
Dicostanzo, A., L.W.H. Johnston and M. Murphy, 1996. A review of the effects of molds and mycotoxins in ruminants. Prof. Anim. Sci., 12: 138-150.
Diekman, M.A. and M.L. Green, 1992. Mycotoxins and reproduction in domestic livestock. J. Anim. Sci., 70: 1615-1627.
Direct Link |
Edrington, T.S., R.B. Harvey and L.F. Kubena, 1994. Effects of aflatoxin in growing lambs fed ruminally degradable or escape protein sources. J. Anim. Sci., 72: 1274-1281.
Direct Link |
Edrington, T.S., R.B. Harvey and L.F. Kubena, 1995. Toxic effects of aflatoxin B1 and ochratoxin A, alone and in combination, on chicken embryos. Bull. Environ. Contam. Toxicol., 54: 331-336.
Etienne, M., I. Oswald, S. Bony, J.P. Lalles and P. Pinton et al., 2006. Effects de la contamination par le deoxynivalenol (DON) de l'aliment des truies reproductrices. Journees Recherche Porcine, 38: 233-240.
Direct Link |
FAO, 1998. Animal feeding and food safety: FAO food and nutrition paper 69. Rome Italy.
Fernandez, A., J.J. Ramos, T. Saez, M.C. Sanz and M.T. Verde, 1995. Changes in the coagulation profile of lambs intoxicated with aflatoxin in their feed. Vet. Res., 26: 180-184.
Fernandez, A., M. Hernandez, M.T. Verde and M. Sanz, 2000. Effect of aflatoxin on performance, haematology and clinic al immunology in lambs. Can. J. Vet. Res., 64: 53-58.
PubMed | Direct Link |
Fernandez, A., R. Belio, J.J. Ramos, M.C. Sanz and T. Saez, 1997. Aflatoxins and their metabolites in the tissues, faeces and urine from lambs feeding on an aflatoxin-contaminated diet. J. Sci. Food Agric., 74: 161-168.
CrossRef | Direct Link |
Garaleviciene, D., H. Pettersson and K. Elwinger, 2002. Effects on health and blood plasma parameters of laying hens by pure nivalenol in the diet. J. Anim. Physiol. Anim. Nutr., 86: 389-398.
Gelderblom, W.C., K. Jaskiewicz, W.F. Marasas, P.G. Thiel and R.M. Horak et al., 1988. Fumonisins novel mycotoxins with cancer promoting activity produced by Fusarium moniliforme. Applied Environ. Microbiol., 54: 1806-1811.
Direct Link |
Gelderblom, W.C.A., W.F.O. Marasas, R. Vleggar, P.G. Thiel and M.E. Cawood, 1992. Fumonisins: Isolation, chemical characterization and biological effects. Mycopathologia, 117: 11-16.
CrossRef | PubMed |
Gentles, A., E.E. Smith, L.F. Kubena, E. Duffus and P. Johnson et al., 1999. Toxicological evaluations of cyclopiazonic acid and ochratoxin A in broilers. Poult. Sci., 78: 1380-1384.
Gurung, N.K., D.L. Rankins Jr., R.A. Shelby and S. Goel, 1998. Effects of fumonisin B1-contaminated feeds on weanling angora goats. J. Anim. Sci., 76: 2863-2870.
Harvey, R.B., L.F. Kubena, D.E. Corrier, D.A. Witzel, T.D. Phillips and N.D. Heidelbaugh, 1986. Effects of deoxynivalenol in a wheat ration fed to growing lambs. Am. J. Vet. Res., 47: 1631-1632.
Harvey, R.B., T.S. Edrington, L.F. Kubena, M.H.C.D.E. Elissalde and G.E. Rottinghaus, 1995. Effect of aflatoxin and diacetoxyscirpenol in ewe lambs. Bull. Environ. Contam. Toxicol., 54: 325-330.
Harwig, J., Y.K. Chen and D.L. Collins-Thompson, 1974. Stability of ochratoxin A in beans during canning. Can. Inst. Food Sci. J., 7: 288-289.
Hedmand, R., H. Pettersson, B. Engstrom, K. Elwinger and O. Fossum, 1995. Effects of feeding nivalenol contaminated diets to male broiler chickens. Poult. Sci., 74: 620-625.
Helferich, W.G., W.N. Garrett, D.P.H. Hsieh and R.L. Baldwin, 1986. Feedlot performance and tissue residues of cattle consuming diets containing aflatoxins. J. Anim. Sci., 62: 691-696.
Hsu, I.C., E.B. Smalley, F.M. Strong and W.E. Ribelin, 1972. Identification of T-2 toxin in moldy corn associated with a lethal toxicosis in dairy cattle. Applied Microbiol., 24: 682-690.
Hussein, H.S. and J.M. Brasel, 2001. Toxicity, metabolism and impact of mycotoxins on humans and animals. Toxicology, 167: 101-134.
Ito, Y., S.W. Peterson and T.D. Wicklow, 2001. Aspergillus pseudotamarii, a new aflatoxin producing species in Aspergillus section flavi. Mycol. Res., 105: 233-239.
Direct Link |
Jewers, K., 1990. Mycotoxins and their effect on poultry production. http://ressources.ciheam.org/om/pdf/a07/CI901593.pdf.
Jones, F.T., M.B. Genter, W.M. Hagler, J.A. Hansen and B.A. Mowrey et al., 1994. Understanding and Coping with Effects of Mycotoxins in Livestock Feed and Forage. North Carolina Cooperative Extension Service, Carolina, pp: 1 14.
Kubena, L.F., R.B. Harvey, D.E. Corrier, W.E. Huff and T.D. Philips, 1987. Effects of feeding deoxynivalenol (DON, Vomitoxin)-contaminated wheat to female white leghorn chickens from day old through egg production. Poult. Sci., 66: 1612-1618.
Kurtzman, C.P., B.W. Horn and C.W. Hesseltine, 1987. Aspergillus nominus, a new aflatoxin- producing species related to Aspergillus flavus and Aspergillus tamarii. Antonie van Leeuwenhoek, 53: 147-158.
Lawlor, P.G. and P.B. Lynch, 2005. Mycotoxin management. Afr. Farming Food Process., 46: 12-13.
Lawloy, P.G. and P.B. Lynch, 2001. Mycotoxins in pig feed 1: Source of toxins, prevention and management of mycotoxicosis. Irish Vet. J., 54: 67-71.
Ledoux, D.R., T.P. Brown, T.S. Weibking and G.E. Rottinghaus, 1992. Fumonisin toxicity in broiler chicks. J. Vet. Diagn. Invest., 4: 330-333.
Direct Link |
Mann, D.D., G.M. Beuning and B.S. Hook, 1983. Effects of T-2 toxin on bovine serum proteins. Am. J. Vet. Res., 44: 1751-1759.
Mann, D.D., G.M. Buening, G.D. Osweiller and B.S. Hook, 1984. Effect of subclinical levels of T-2 toxin on the bovine cellular immune system. Can. J. Comp. Med., 43: 308-312.
Marasas, W.F.O., P.E. Nelson and T.A. Toussoun, 1984. Toxigenic Fusarium species: Identity and Mycotoxicology. The Pennsylvania State University Press, Pennsylvania.
Miller, D.M. and D.M. Wilson, 1994. Veterinary Diseases Related to Aflatoxin. In: The Toxicology of Aflatoxins: Human Health, Veterinary and Agricultural Significance, Eaton, D.L. and J.D. Groopman (Eds.). Academic Press, San Diego, pp: 347-364.
Okoli, I.C., 2005. Mycotoxin contamination of feedstuff and mycotoxicoses are neglected livestock production research topics in Nigeria. Proceedings of the Myco-Globe Conference, Sept. 13-16, Accra, Ghana, pp: 65-65.
Okoli, I.C., A.A. Omede, I.P. Ogbuewu, I.C. Ekwuagana and G.E. Ndujihe et al., 2007. Frequency of mycoflora from commercial poultry feeds and feed raw materials in the humid tropical environment of Imo State, Nigeria. Proceedings of 12th Annual Conference of Animal Science Association of Nigeria, Sept. 10-13, Osun State, Nigeria, pp: 115-115.
Okoli, I.C., A.A. Omede, M.N. Oparam and C.T. Ezeokeke, 2008. The significance of phytohormones in animal production. Int. J. Trop. Agric. Food Syst., 2: 89-104.
Okoli, I.C., C.U. Nweke, C.G. Okoli and M.N. Opara, 2006. Assessment of the mycoflora of commercial poultry feeds sold in the humid tropical environment of Imo state, Nigeria. Int. J. Environ. Sci. Technol., 3: 9-14.
CrossRef | Direct Link |
Okoli, I.C., G.E. Endujihe and I.P. Ogbuewu, 2006. Frequency of isolation of Salmonella from commercial poultry feeds and their anti-microbial resistance profiles, Imo State, Nigeria. Online J. Health Allied Sci., 5: 2-3.
Direct Link |
Okoli, I.C., I.P. Ogbuewu, J.O. Okorie, G.C. Okoli, M.C. Ucheghu, M.N. Opara and V.I. Ibekwe, 2007. Assessment of the mycoflora of poultry feed raw materials in the humid tropical environment. J. Am. Sci., 3: 5-9.
Omede, A.A., 2008. Critical issues in poultry feed quality evaluation in Nigeria. Proceedings of the 23rd Worlds Poultry Congress, June 29-July 4, Brisbane, Australia, pp: 455-.
Patterson, D.S., B.J. Shreeve, B.A. Roberts, S. Berrett, P.J. Brush and E.M. Glancy, 1981. Effect on calves of barley naturally contaminated with ochratoxin A and groundnut meal contaminated with low concentration of aflatoxin B1. Res. Vet. Sci., 31: 213-218.
Paul, P.S., D.W. Johnson, C.J. Mirocha, F.F. Soper and C.C. Thoen et al., 1977. In vitro stimulation of bovine peripheral blood lymphocytes: Suppression of phytomitogen and specific antigen lymphocyte responses by aflatoxin. Am. J. Vet. Res., 38: 2033-2035.
Payne, G.A., 1998. Process of Contamination by Aflatoxinproducing Fungi and Their Impacts on Crops. In: Mycotoxins in Agriculture and Food Safety, Sinha, K.K. and D. Bhatnagar (Eds.). Marcel Dekker, New York, pp: 279-306.
Phillips, S.I., P.W. Wareing, D. Ambika, S. Panigrahi and V. Medlock, 1996. The mycoflora and incidence of aflatoxin, zearalenone and sterigmatocystin in dairy feed and forage samples from Eastern India and Bangladesh. Mycopathologia, 133: 15-21.
CrossRef | Direct Link |
Placinta, C.M., J.P.F. D'Mello and A.M.C. Macdeoxynivalenolald, 1999. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Anim. Feed Sci. Technol., 78: 21-37.
Direct Link |
Quist, C.F., E.W. Howerth, J.R. Fischer, R.D. Wyatt, D.M. Miller and V.F. Nettles, 1997. Evaluation of low-level aflatoxin in the diet of white-tailed deer. J. Wildlife Dis., 33: 112-121.
Ramos, J.J., A. Fernandez, T. Saez, M.C. Sanz and M.C. Marca, 1996. Effect of aflatoxicosis on blood mineral constituents of growing lambs. Small Ruminant Res., 21: 233-238.
Direct Link |
Ranjan, K.S. and A.K. Sinha, 1991. Occurrence of mycotoxigenic fungi and mycotoxins in animal feed from Bihar, India. J. Sci. Food Agric., 56: 39-47.
Ratcliff, J., 2002. The Role of Mycotoxins in Food and Feed Safety. Animal Feed Manufacturers Association, South Africa.
Ross, A.D., W.L. Bryden, W. Bakua and L.W. Burgess, 1989. Induction of heat stress in beef cattle by feeding the ergots of Claviceps pupurea. Aust. Vet. J., 66: 247-249.
Ross, P.F., P.E. Nelson, J.L. Richard, G.D. Osweiler and L.G. Rice et al., 1990. Production of fumonisins by Fusarium moniliforme and Fusarium proliferatum isolates associated with equine leukoencephalomalacia and a pulmonary oedema syndrome in swine. Applied Environ. Microbiol., 56: 3225-3226.
PubMed | Direct Link |
Russel, L., D.F. Cox, G. Larsen, K. Bodwell and E.E. Nelson, 1991. Incidence of molds and mycotoxins in commercial animal feed mills in seven Midwestern States. J. Anim. Sci., 69: 5-12.
Shane, S.H., 1994. Economic Issues Associated with Aflatoxins. In: The Toxicology of Aflatoxins: Human Health, Veterinary and Agricultural Significance, Eaton, D.L. and J.D. Groopman (Eds.). Academic Press, San Diego, pp: 513-527.
Sharma, R.P., 1993. Immunotoxicity of mycotoxins. J. Dairy Sci., 76: 892-897.
CrossRef | Direct Link |
Skrinjar, M., M. Danev and G. Dimic, 1995. Investigation on the presence of toxigenic fungi and aflatoxins in raw milk. Acta Alimentaria, 24: 395-402.
Direct Link |
Smith, J.E. and M.O. Moss, 1985. Mycotoxins, Formation, Analysis and Significance. Wiley and Sons, Chichester, pp: 148.
Smith, J.E. and R.A. Anderson, 1991. Mycotoxins and Animal Foods. CRC Press, Boca Raton.
Smith, J.E., C.W. Lewis, J.G. Anderson and G.L. Solomons, 1994. Mycotoxins in Human Nutrition and Health. Eur. Commission, Brussels, pp: 300.
Smith, J.E., G. Solomon, C. Lewis and J.G. Anderson, 1995. The role of mycotoxins in human and animal nutrition and health. Nat. Toxins, 3: 187-192.
Smith, T.K. and I.R. Seddon, 1998. Toxicological Synergism between Fusarium Mycotoxins in Feeds. In: Biotechnology in the Feed Industry. Lyons, T.P. and K.A. Jacques, (Eds.). Nottingham University Press, Loughborough, UK., pp: 257-269.
Stoev, S.D., D. Djuvinov, T. Mirtcheva, D. Pavlov and P. Mantle, 2002. Studies on some feed additives giving partial protection against ochratoxin A toxicity in chicks. Toxicol. Lett., 135: 33-50.
CrossRef | Direct Link |
Vasanthi, S. and R.V. Bhat, 1998. Mycotoxins in foods-occurrence, health and economic significance & food control measures. Indian J. Med. Res., 108: 212-224.
Veldman, A., J.A.C. Meijs, G.J. Borggreve and J.J. Heeres van der Tol, 1992. Carry-over of aflatoxin from cows' food to milk. Anim. Prod., 55: 163-168.
Wogan, G.N., 1966. Chemical nature and biological effects of the aflatoxins. Bacteriol. Rev., 30: 460-470.
Direct Link |
Wood, G.E., 1992. Mycotoxins in foods and feeds in the United States. J. Anim. Sci., 70: 3941-3949.
Direct Link |
Wyatt, R.D., 1979. Biological effects of mycotoxins (other than aflatoxin) on poultry. Proceedings of the Symposium on Interactions of Mycotoxins in Animal Production, July 13, Michigan State University, pp: 87-95.
Yiannikouris, A. and J. Jonany, 2002. Mycotoxins in feeds and their fate in animals: A review. Anim. Res., 51: 81-99.
CrossRef | Direct Link |