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Reaction of different poultry types to the combinations of mycotoxins and feed naturally contaminated by mycotoxins
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Bonnie A. Nahm and Kee H. Nahm
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Feed and Nutrition Lab. in Illinois
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25001 Cashel Bay Rd.
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Manhattan, IL 60442
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USA
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Phone and FAX: (815) 478-5069 Email: khnahm1@cs.com
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Running head: Mycotoxin contaminated feed and poultry
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Cereal grains and animal feeds are often contaminated with mycotoxins including the trichothecenes [ochratoxins (OA), dexyniralenal (DON), nivalenol (NIV), T-2 toxin and diacetoxoyscirpenol (DAS)], zealaleone (ZEN) and the fumonisins, the major mycotoxins of Fusarium fungi. Body weight gains of male broilers were depressed by aflatoxins (AF) and T-2 toxins singly, but further depressed by the combination of the two toxins. The AF plus T-2 toxin combination also increased relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights. The immune system of chickens has low sensitivity to Fusarium mycotoxins while mycotoxin contaminated diets have been related to clinical signs of toxicosis and reduced feed intake, egg production and egg quality. Feeding turkey poults pure T-2 toxin or diacetoxyscripenol (DAS) adversely affected small intestine morphology, but did not affect growth or antibody production. Growing Pekin ducks were not adversely affected in regards to health or performance by dietary DON and ZEN concentrations up to 6 and 0.6 mg/kg.
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Introduction
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Filamentous fungi produce low molecular weight, secondary metabolites which are mycotoxins. While cereal grains and associated by-products constitute important sources of energy for poultry, there is increasing evidence worldwide that these cereal grains for animal feedstuffs are commonly contaminated with Fusarium mycotoxins, especially in swine. This contamination of food and feedstuffs with mycotoxins is a significant health risk, with estimates of up to 25 % of the world’s crops being contaminated with mycotoxins (Fink-Gremmels, 1999). Annual economic losses estimated for the animal production industries related to mycotoxin contamination are up to several million dollars (Hussein and Brasel, 2001).
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Mycotoxicoses are feed-related, nontransferable and non-infectious diseases (Bennett and Kish, 2003). Acute mycotoxicoses are rare in poultry production, but chronic exposure to low levels of mycotoxins results in reduced productivity and increased susceptibility to infectious diseases (Hussein and Brasel, 2001).The type and concentration of mycotoxin, the duration of exposure, gender, age and health status affects the severity of mycotoxicosis. In animals, the order of decreasing sensitivity to mycotoxins is generally acknowledged as pigs > mice > rats > poultry > ruminants (Rotter et al., 1996).
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Fusarium moniliforme, which produces the mycotoxins known as fumonisins, is a common contaminant of corn and other grains. The fumonisins include fumonisin B1, B2, B3 and B4, with fumonisin B1 being the major metabolite (Gelderblom et al., 1992). In grains worldwide, Fusarium mycotoxins, DON (vomitoxin) and ZEN are common (Scott, 1989). Analyses of Canadian feeds and feedstuffs for Fusarium mycotoxins have shown DON and fusaric acid as frequent contaminants while ZEN is a less common problem (Smith and Sousadias, 1993; Scott, 1997).
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Trichothecene mycotoxins include DON, nivalenol (NIV), T-2 toxins, 3-ADON and DAS (D’Mello et al. 1999) (Table1). These mycotoxins are potent inhibitors of protein synthesis and can increase disease susceptibility of animals when ingested in sufficient quantities (Bondy and Pestka, 2000).
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D’Mello et al. (1999) have presented a superficial account of the toxicology of Fusarium mycotoxins focusing on structural diversity, biological activity and interactions involving fusaric acid. D’Mello and Macdonald (1997) summarized wide-raging aspects including factors affecting mycotoxin production.
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Mycotoxins from naturally contaminated grain sources may show more toxicity than an equivalent dose of the purified toxin (Harvey et al., 1991).The cause of this phenomenon may be due to the presence of unidentified mycotoxins and the resulting synergistic effects among mycotoxins (Smith et al., 1997). FB1 and DAS or FB1 and OA have not been observed to occur together in a single potential feed grain source. The possibility exists for co-contamination with FB1 and DAS or FB1 and OA due to multiple grain sources used in poultry and livestock diets. Individual toxicities of mycotoxins cannot be used to predict the toxicity of combinations of mycotoxins (Huff et al., 1985). The question of synergism among co-occurring mycotoxins has remained largely unexplored. “Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity” by D’Mello et al. (1999) showed details in swine and rat, but the effects of combinations of mycotoxins have not been previously reported in poultry. This study will investigate and describe the major effects of feeding poultry diets contaminated with multiple mycotoxins.
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Types of mycotoxins
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Fusarium monoliforme contaminates corn and other grains and produces mycotoxins known as fumonisins. Fumonisins are classified as fumonisin B1, B2, B3 and B4, with Fumonisins B1 (FB1) as the major metabolite (Huff et al. 1988a). In many tropical countries including China, Thailand and South Africa, FB1 is the contaminant of maize and animal feed while FB2 was predominant form of mycotoxin in Argentinian maize according to the study. Aflatoxins (AF) are mycotoxins produced by fungi of flavus-parasiticus group of the genus Aspergillus and include AF B1, B2, G1 and G2 (Edds and Bortell, 1983). Several species of the fungi in the genus Fusarium produce the mycotoxin T-2 toxin (T-2) (Bamburg et al., 1970), and T-2 has been shown to produce numerous symptoms of toxicity in poultry, as reported by Kubena et al. (1989b).Several parameters of growing broiler chicks are affected by a synergistic interaction between AF and T-2 (Huff et al., 1988b).
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The trichothecenes include over 150 secondary fungal metabolites (Rocha et al., 2005) that show multiple inhibitory effects on eukaryotic cells, including inhibition of protein, DNA and RNA synthesis, mitosis inhibition, interference with cell-membrane integrity and apoptosis induction (Rocha et al., 2005). These mycotoxins primarily affect rapidly proliferating cells and tissues with high rates of protein turnover, including the immune system, liver and small intestine (Feinberg and McLaughlin, 1989).
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One of the trichothecene mycotoxins is deoxynivalenol (DON), while others include nivalenol (NIV), T-2 toxin and diacetoxoyscirpenol (DAS) (Pathre and Mirocha, 1979). DON, commonly called vomitoxin, is a secondary metabolite of Fusarium gramineariam (Schwabe telemorph Gibberella zeac Petch) in the field (Neish et al., 1983; Neish and Cohen, 1981). Among the trichothecenes, DON and NIV co-occur regularly throughout the world, with cereal grains in Poland, Germany, Japan, New Zealand and the Americas having unacceptably high levels (Placinta et al., 1999). Other trichothecenes that co-occur in grains and feeds include 3-acetyl DON (3-ADON), DAS, T-2 toxin and HT-2 toxin. Concentrations of ZEN are generally low, but cereal grains and animal feeds in Japan, New Zealand and South Africa have been reported to have above average values.
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Ochratoxin A (OA) is a secondary metabolite produced by some strains of Aspergillus ochraceus and Penicillium verrucosum that is found in various feed ingredients. OA is considered to be substance which is nephrotoxic, hepatoxic and immunosuppressive (Stormer and Lea, 1995) in all mammals, and it is classified as a possible carcinogen to humans by the International Agency for Research on Cancer (1991). The mechanism of toxicity of OA is unclear.
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Placinta et al. (1999) concluded that cereal grains and animal feeds on a global scale may be subject to contamination with trichothecenes, ZEN and fumonisins, the major mycotoxin of Fusarium fungi. There is now compelling evidence that Fusarium mycotoxins are involved in livestock disorders in different parts of the world. Enhanced awareness of the debilitating effects of mycotoxin has not diminished the risk of continued exposure to the mycotoxins.
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A significant synergistic interaction between AF and T-2 has been shown to affect several parameters of growing broiler chicks (Huff et al., 1988). Another study indicated that both AF and OA adversely affected energy and protein utilization in broilers and this effect was exacerbated when both mycotoxins were fed simultaneously. The toxicity of AF (3.5 g) and OA (2.0 g) resulted in decreased body weight, serum protein, albumin, cholesterol and decreased the relative weights of the liver, kidney and proventriculus (Verma et al., 2002). Effects of chronic feeding of Fusarium mycotoxins on the immunocompetence of a relatively resistant species such as laying hens has not been extensively studied.
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Exposure of mice to ZEN at a dose of 10 mg/kg of diet reduced their resistance to listeriosis. Co-administration of DON and ZEN reduced resistance to Listeria monocytogene to a greater extent even though indices of humoral and cell-mediated immune competence were unaffected (Pestka et al., 1987). ZEN is not only reduced to a- and B-ZEN, but it also is conjugated to glucose according to studied of ZEN metabolism by cell suspension cultures of maize (Zea mavs), wheat (Triticum aestivum) and different fungal species (Rhizopus sp., Thamnidium elefans, Mucor baqinieri). (Engelhardt et al., 1989).
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Mycotoxins from naturally contaminated grains may be more highly toxic than an equivalent dose of purified toxins (Harvey et al., 1991). This may be the result of the presence of unidentified mycotoxins and precursors in contaminated grain and the synergistic effects of these mycotoxins (Smith et al., 1997). Dietary inclusion if a polymeric glucomannan mycotoxin adsorbent (GMA), extracted from the cell wall of yeast, has benefits in preventing the adverse effects of Fusarium mycotoxin in laying hens (Chowdhury and Smith, 2004) and ducklings (Chowdhury et al., 2005b).
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How do mycotoxins affect the utilization of poultry?
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1. Broilers
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For the poultry industry, the frequent AF contamination of agricultural commodities and exposure of poultry to these toxins can mean the difference between profit and loss (Jones et al., 1982; Nicholas, 1985; Hamilton, 1984). The combination of mycotoxins may pose a greater problem than mycotoxins individually (Kubena et al., 1989a) (Table 2). AF and T-2 interact to farm a synergistic toxicity which threatens poultry production due to the prevalence of these mycotoxins and their interactive toxicity (Huff et al., 1988). The incidence and severity of oral lesions induced by T-2 toxins was increased in the DON/T-2 toxin combination.
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Broiler chicks have been found to be susceptible to Fusarium mycotoxicosis when naturally contaminated grains are fed containing a combination of mycotoxins (Swamy et al., 2002). These feeds contained DON, fusaric acid (FA) and ZEN. Broiler chickens are susceptible during extended feeding of grains naturally contaminated with Fusarium mycotoxins (Swamy et al., 2004). These feeds also contained DON, FA and ZEN. Efficiency of feed utilization by broilers was not affected by diet (Swamy et al., 2002, 2004). The production parameters in these studies were not significantly affected by supplementation of polymeric glycomannan mycotoxin adsorbent (GMA or GM polymer).
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Body weight gains of male broilers were significantly depressed by AF and T-2 singly, and further decreased by the combination of the two toxins (Kubena et al., 1990). Feed utilization was not affected. The AF alone and the AF plus T-2 combination caused increases in relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights. Oral lesions were seen only in chicks receiving theT-2. Addition of a hydrated sodium calcium aluminosilicate (HSCAS) did not alter any of the parameters measured but it did diminish the toxicity of AF, but did not alter the toxicity of T-2. Another study (Kubena et al., 1990) showed the addition of HSCAS to an AF plus T-2 diet diminished some of the effects of AF in the chicken, but it has no effect on T-2 toxicity.
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Huff et al., (1988) observed the effects of AF and T-2 on several parameters of growing broiler chicks. Treatment related changes were seen in red blood cell counts and serum levels of protein, albumin, glucose, cholesterol, calcium, magnesium, lactic dehydrogenase and alkaline phosphatase. There were also significant increases in the relative weights of the liver, kidney, spleen and proventriculus (Kubena et al., 1990).
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2. Layers
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In commercial birds, consumption of OA contaminated diets has been corrected with clinical toxicosis and reductions in feed intake, egg production and egg quality (Pior and Sisodia, 1978; Verma et al., 2003). Consumption of OA by layers has also been associated with the presence of the toxin and its derivatives in eggs (Piskorska- Plisczynka and Juszkiewica, 1990).Osborne and Hamilton (1981) reported reduced pancreatic digestive secretions in broiler chicks fed AF, while Richardson and Hamilton (1989) noted increased pancreatic digestive enzyme production in egg type chicks fed AF. It has not been ascertained if this is due to an effect on nutrient metabolisability alone or due to an effect on the intestine, or both, which results in increased endogenous or reduced nutrient digestibility, or both. Verma et al. (2003) reported that AF, or both (AF and DON), can have a direct effect on gastrointestinal tract functionality.
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There is very little information on immunocompetence regarding the response or sensitivity of a comparatively resistance species, such as laying hens to mycotoxins. In a study where both of the feeds were contaminated with AF or DON, or with two or more toxins mixed, most immunotoxic effects were short term, but prolonged consumption of purified DON and ZEN resulted in disappearance of adverse effects, which were mainly attributed to feed refusal rather than systemic toxicity. Host resistance to Listeria monocycytogenes and the delayed-type hypersensitivity (DTH) response in mice was altered by 10 mg of purified DON/kg feed (Pestka et al., 1987), but 50 mg/kg was required to alter splenocyte blastogenic response to phytohemagglutinin-P of laying hens (Harvey et al., 1991). Thus, it appears that there is a low sensitivity to Fusarium mycotoxins by the immune system of chickens. Chowdhury and Smith (2005) (Table 3) concluded that chronic consumption of grains contaminated with Fusarium mycotoxins of levels usually found in practice were not systemically immunosuppressive or hematotoxic, but mucosal immunocompetence needs to be explored further in “Effects of feed-borne Fusarium mycotoxins on hematology and immunology of laying hens”.
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Research results did not show much information about AF or T-2 toxin, but there were results showing that addition of Ochratoxin A (OTA) + Ocratox (Ochratoxin-Binding Agent or containing 5 g OCra Tox/kg of feed)(containing 2 g OTA and 5 g ochratoxin/kg of feed) counteracted the deleterious effects OTA in 47 week old laying hens (Denli et al., 2008). They concluded Ocratax counteracted the deleterious effects of OTA in laying hens.
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3) Turkeys
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Fusaria fungi are commonly associated with corn, a major component of most poultry diets and toxic effects of these Fusaria include immunosuppression (Marijanovoc et al., 1991), diarrhea, reduced growth and feed utilization (Brown et al., 1992), cardiotoxicity (Engelhardt et al., 1989), leg shape deformities (Sharby et al., 1973), rickets (Gedek et al., 1978; Brown et al., 1992), and high mortality in the turkeys (Jeschke et al., 1987). Another major finding by Wu et al. (1994) was that culture materials of some Fusaria increased the redness of turkey breast muscle without causing obvious hemorrhages in the musculature or internal organs. F. proliferatum (Javed et al., 1993) containing FB1 caused poor performance, increased organ weights and hepatitis in broilers, while in turkeys it was associated with reduced performance and increased organ weights (Weibking et al., 1993; Kubena et al., 1995a,b).
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There are very few reports of the effects of feeding of grains naturally contaminated with Fusarium mycotoxins to turkeys. Minor adverse effects on the hematology and some immunological indices of turkeys were seen with chronic consumption of grains naturally contaminated with Fusarium mycotoxins (Chowdhury et al., 2005c). Increased susceptibility of turkeys to infectious agents against which CD58 + T cells play a major role in defense has been associated with consumption of grains naturally contaminated with Fusarium mycotoxins. Girish et al. (2008) concluded turkey performance and some blood and immunological parameters were adversely affected by feed borne Fusarium mycotoxins, and EMA prevented many of these effects.
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Effects of other mycotoxins have been reported on certain parameters in turkeys. Resistance to Listeria monocytogenes was reduced to a greater extent by coadministration of DON with ZEN even though indices of humoral and cell-mediated immune competence were not affected (Pestka et al., 1987). Feeding pure T-2 toxin or DAS to turkey poults at levels up to 1 mg/kg of feed for 32 days adversely influenced small intestine morphology but had no effect on growth or antibody production (Sklan et al., 2003). The feeding of a combination of T-2 toxin and DAS resulted in severe oral lesions (Awad et al., 2006). Fairchild et al. (2005) also observed that feeding a combination of FA (300 mg/kg of feed) and DAS (4 mg/kg of feed) to turkey poults for 18 d decreased enterocyte height at mid villus by 59 %. Feeding FA alone reduced the relative weight of the intestine serosal thickness while feeding DAS alone increased serosal thickness.
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In turkey poults 7 to 14 days of age, McMillan and Moran (1985) found that neither vomitoxin (75 mg/kg) nor ZET (50 mg/kg) decreased growth or feed consumption. Salinomycin fed at or below dosages recommended for broilers (60 mg/kg) caused mortality and clinical lesions in adult turkey, but not growing turkey (Halvorson et al., 1982). In a study by Manley et al. (1988),turkey poults fed the suspect commercial diet had significantly lower feed consumption and higher mortality than poults fed a control diet. There were no significant decreases in feed consumption, body weight gain or viability in poults (0 to 3 wks of age) fed diets containing vomitoxin (4.4 mg/kg), salinomycin (22 mg/kg) or both. When turkey poults were fed diets containing moniliformin (M) alone or with the DON-M combination, there was an increased incidence of variable sized cardiomyocyte nuclei, with numerous large giant nuclei, and a generalized loss of cardiomyocyte cross striations. In the poults fed the M and combination DON-M treatments. Mild diffuse mineralizations were noted in isolated renal tubule sections of the kidney. None of the response variables measured were noted in the DON treatments alone (Morris et al., 1999) (Table 4). Kubena et al. (1989a) noted a similar reaction between DON and T-2 toxin in chicks. When compared with controls, body weight gains of turkey poults were reduced by 30 % (Study 1.) and 24 % (Study 2.) by FB1, 30 % by DAS, 8 % by OA, 46 % by the FB1 and DAS combination and 37 % by the FB1 and OA combination. The impact of these mycotoxins on the health and performance of poultry could be altered under field conditions by other stress factors (Kubena et al., 1997a).
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4) Ducklings
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In studies with ducklings, DAS (4,15-Dicetoxyseripental) has been implicated in reduced feed intake, feed refusal or toxicity (Steyn et al., 1978). DAS is a toxic secondary metabolite that is naturally occurring and is predominantly associated with Fusarium species (Pathre and Mirocha, 1979).
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When a diet containing 1.2 mg DON/kg, 4.5 mg fumonisin/kg and 0.01 mg AFB1/kg was fed to white Pekin ducklings, 50 % morality was reported after 7 d of feeding because of total feed refusal (Davis et al., 1980). However, another study (Boston et al., 1996) reported no adverse effects on feed intake, body weight gain, organ weights or plasma chemistry when adult Mallard ducks were feed wheat naturally contaminated with 5.8 mg DON/kg for 2 wks. These animals may become susceptible to infections agents such as viruses against which the CD8+ T cell provides necessary defense when fed mycotoxin-contaminated feeds. According to a report by Chowdhury et al. (2005b) (Table 5), glucomannan mycotoxin-adsorbent was not effective in preventing alterations in ducklings caused by Fusarium mycotoxin. They reported mean corpuscular hemoglobin concentrations and hematocrit decreased when ducks were fed contaminated grains for 4 or 6 wks, respectively. In contrast, total numbers of white blood cells and lymphocytes increased transiently in birds fed contaminated gains for 4 wks.
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In anther study by Danicke et al. (2002) concentrations of DON and its de-epoxydised metabolite in the plasma and bile of ducks were lower than the detection limits of 6 and 16 µg/ml, respectively. ZON or its metabolites were not detectable in plasma or livers. Taken together, it can be concluded that dietary DON and ZON concentrations up to 6 and 0.06 mg/kg, respectively, did not affect the performance and health of growing Pekin ducks.
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The acute toxicity (LD 50) of fusarium toxins have been frequently titrated using 1-day-old ducklings (Ueno, 1985). One-day-old ducklings showed an LD50 dose of DON estimated at 27 mg/kg, while 1-day-old broiler chicks had a much higher LD 50 dose of 140 mg/kg body weight (Huff et al., 1981). Conclusions about chronic toxicity of DON in ducks can not be drawn from information on acute toxicity.
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5. Broiler breeders
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Egg production was not significantly affected by feeding of mycotoxin contaminated grains. Eggshell thickness was decreased at the end of wks 4, but dietary GMA supplementation prevented this effect. Other egg parameters measured were not affected by the diet (Yegani et al., 2006) (Table 5). There was a significant increase in early (1 to 7 d) embryonic mortality from birds fed contaminated grins at wk 4, but diet did not affect mid (8 to 14 d) and late (15 to 21 d) embryonic mortality. Feeding of the contaminated grains did not affect ratio of chick weight to egg weight (Yegani et al., 2006). This research also found that rooster semen volume and sperm concentration, viability and motility weight were not affected by feeding the contaminated diets.
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The trichothecenes, which include over 150 fungal metabolites, are known to have multiple inhibitory effects on eukaryotic cells, including inhibition of protein, DNA and RNA synthesis; inhibition of mitosis; interference with cell membrane integrity; and induction of apoptosis (Bennett and Klich, 2003; Rocha et al ., 2005). Dietary inclusion of a GMA, extracted from the cell wall of yeast, has some beneficial effects of Fusarium mycotoxins in broilers (Swamy et al., 2002, 2004), laying hens (Chowdhury and Smith, 2004) and ducklings (Chowdhury et al., 2005b).
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CONCLUSION
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Different poultry show different affects of feeds contaminated with mycotoxin, either singly or in combinations of two or more mycotoxins. Body weight gains of male broiler were significantly depressed by AF and T-2 singly, and further decreased by the combination of the two toxins. Feed utilization was not affected, but the AF alone and the AF plus T-2 combination caused increases in relatives in relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights (Hamilton, 1984).
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When feeds containing DON, FA and ZEN were fed in another study (Swamy et al., 2004), the efficiency of feed utilization was not affected by polymeric glucomannan mycotoxin adsorbent (GMA) supplementation. FA has been shown to have a direct or indirect effect, or both, on functionality of the gastrointestinal tract of laying birds Santin et al., 2002). Chowdhury et al. (2005a) concluded that chronic consumption of grains naturally contaminated with Fusarium mycotoxins of levels likely to be encountered in practice were not systemically immumsuppressive or hepatotoxic, even though the immune system of chickens has low sensitivity to Fusarium mycotoxins. Clinical signs of toxicosis and reduced feed intake, egg production have been related to consumption at OA contaminated feeds by commercial birds (Pior and Sisodia, 1978; Raymond et al., 2003).
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Diets contaminated with F. proliferatum (Javed et al., 1993) containing FB1 have been associated with poor performance, increased organ weights and hepatitis in broilers, while turkeys showed reduced performance and increased organ weights (Weibking et al., 1993; Kubena et al., 1995 a,b). Coadministration of DON and ZEN reduced in greater reductions of resistance to Listeria monocytogene (Pestka et al., 1990). Severe oral lesions resulted from feeding both T-2 and DAS. The redness of turkey breast meat was increased by feeding of fusarial culture materials (Wu et al., 1994). In another study (Kubena et al., 1997b), body weight gains compared to the control were reduced by 30 % (study 1) and 24 % (study 2) by FB1, 30 % by DAS, 8 % by OA, 46 % by the FB1 and DAS combination and 37 % by the FB1 and OA combination. Feeding turkey poults pure T-2 and DAS on levels up to 1 mg/kg of feed for 32 days adversely influenced small intestinal morphology but did not affect growth or antibody production (Sklan et al., 2003).
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In White Pekin ducklings, 50 % mortality was seen after feeding a diet containing 1.2 mg or DON/kg, 4.5 mg of fumonisin/kg and 0.01 AFB1 /kg for 7 days because of total feed refusal (Davis et al., 1980). Dietary DON and ZEN concentrations up to 6 and 0.6 mg/kg did not adversely affect performance and health of growing Pekin ducks (Danicke et al., 2002).
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Mycotoxins contaminated diets were shown to decrease egg shell thickness at the end of 4 wks of feeding, but dietary supplementation with GMA prevented this effect (Yegani et al., 2006). There was no effect of diet on other egg parameters, rooster semen volume and sperm, concentration and viability.
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  +
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  +
  +
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Table 1. Effects of individual trichothecenes in poultry
  +
Trichothecene Poultry type Effects Data Source
  +
DON Laying hens Transmission to eggs following oral administration Prelusky et al. (1987)
  +
DAS Broiler Chickens Reduced bodyweight; dose-related mouth lesions Ademoyero and Hamilton (1991)
  +
T-2 toxin Ducklings Reduced bodyweight and weights of thymus, spleen, and bursa of Faricii; oral and esophageal ulcerations Neiger et al. (1994)
  +
T-2 toxin Geese Decreased egg yields and hatchability; mortality Vanyi et al. (1994a)
  +
T-2 toxin Geese Dose-dependent cessation of follicle maturation in ovaries; follicle degeneration; involution of oviduct; lymphocyte depletion; lesions in adrenal and thyroid glands. Vanyi et al. (1994b)
  +
NIV Broiler chickens Reduced feed consumption and weight gain: gizzard erosions; reduced relative liver weight Hedman et al. (1995)
  +
T-2 toxin Turkey poults Reduced bodyweight gain; oral lesions Kubena et al. (1995a)
  +
DAS Turkey poults Reduced feed intake, weight gain and feed efficiency; oral lesions Kubena et al. (1997b)
  +
DON Broiler Chickens Increased relative weights of gizzard, bursa of Fabricus and heart Kubena et al. (1997a)
  +
T-2 toxin Broiler Chickens Reduced bodyweight gain; oral lesions Kubena et al. (1997a)
  +
  +
  +
  +
  +
  +
  +
  +
  +
Table 2. Feeding and effects of mixed mycotoxins on broilers
  +
Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source
  +
AF and T-2 2.5 µg AF/g and 4.0 µg T-2/g Decreased BW, increased weights of kidney, gizzard and heart, decreased mean corpuscular volume and serum potassium Huff et al. (1988)
  +
OA and T-2 2.0 mg/kg OA and 4.0 mg/kg T-2 Increased liver, kidney, proventriculus and gizzard weights, decreased body weight gains, mean corpuscular volume and serum protein levels Kubena et al. (1989a)
  +
DON and T-2 16 mg DON/kg and 4 mg T-2/kg Decreased total body weight gains and final body weights, increased incidence and severity of oral lesions Kubena et al. (1989b)
  +
AF and T-2 3.5 mg AF/kg and 8.0 mg T-2/kg Depressed BW gains, increased weights of liver, kidney, proventriculus, gizzard, spleen and pancreas Kubena et al. (1990)
  +
DON, FA and ZEN 0.14 to 9.7 mg DON/kg, 20.6 to 21.6 mg FA/kg, 0.2 to 0.8 mg ZEN/kg Decreased BW, increased blood erythrocyte count and serum uric acid, decreased serum lipase, reduced breast muscle redness. Swamy et al. (2002)
  +
AF and OA 0.5 to 2.0 mg AF/kg and 1.0 to 4.0 mg OA/kg Decreased energy and protein utilization Verma et al. (2002)
  +
DON, FA and ZEN 5.9 to 9.5 mg DON/kg, 19.1 to 1.4 mg FA/ kg and 0.4 to 0.7 mg ZEN/kg Decreased BW gains and feed consumption, decreased peripheral blood monocytes, decreased B-cell and T-cell counts Swamy et al. (2004)
  +
AF and OA 0.5 to 2 mg AF/kg and 1 to 4 mg OA/kg Growth depression, reduced food consumption and poor food conversion efficiency. Decreased weight of bursa of Fabricius, reduced cell mediated immunity. Verma et al. (2004)
  +
AF: Aflatoxin: BW: Body weight; DON: Deoxynivalenol; FA: Fusaric Acid; OA: Ochratoxin A; ZEN: Zearalenone
  +
Table 3. Feeding and effects of mixed mycotoxins on laying hens
  +
Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source
  +
DON, FA and ZEN 11.7 to 12.1 µg DON/g, 18 µg FA/g and 0.6 µg ZEN/g Decreased feed consumption, egg production, egg and eggshell mass. Increased plasma uric acid concentrations and kidney wieghts. Chowdhury and Smith (2004)
  +
DON, 15-acetyl-DON, and ZEN 12.6 µg DON/g, 1.2 µg 15-acetyl-DON and 0.7 µg ZEN/g Decreased fractional protein synthesis rate. Chowdhury and Smith (2005)
  +
DON, 15-acetyl-DON, and ZEN 12 mg DON/kg, 0.5 mg 15-acetyl DON/kg and 0.6 mg ZEN/kg Decreased hematocrit values, total numbers of white blood cells, lymphocytes and biliary IgA concentration. Chowdhury et al. (2005a)
  +
DON and ZEN 17,630 µg DON/kg and 1,580 µg ZEN/kg Depressed feed intake, nutrient digestibility,metabolizability of gross energy, serum titers to Newcastle disease virus. Increased yolk titers to antigen K88. Danicke et al. (2002)
  +
OA 2 mg OA/kg Decreased daily feed consumption, egg mass production and serum triglyceride concentrations. Increased relative liver weight, serum alkaline phosphatase and uric acid. Denli, et al. (2008)
  +
DON: Deoxynivalenol; FA: Fusaric Acid; OA: Ochratoxin A; ZEN: Zearalenone
  +
  +
  +
  +
  +
  +
  +
  +
  +
  +
  +
Table 4. Feeding and effects of mixed mycotoxins on turkeys
  +
Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source
  +
DON and Salinomycin 4.4 mg DON/kg and 2.2 mg Salinomycin/kg Lower feed consumption and higher mortality Manley et al. (1988)
  +
FB1 and DAS or OA 300 mg FB1/kg, 4 mg DAS/kg and 3 mg OA/kg Decreased BW gains and efficiency of feed utilization, increased liver weight, increased serum cholesterol and increased AST and LDH Kubena et al. (1997b)
  +
DON and Monoliformin 20 mg DON/kg and 100 mg Monoliformin/kg Decreased mean cell volume, increased incidence of variable sized cardiomyocyte nuclei, mild diffuse mineralization of real tubules Morris et al. (1999)
  +
DON, 15-acetyl-DON and ZEN 6.8 to 13.6 mg DON/kg, 0.6 to 1.3 mg 15-acetyl-DON/kg and 0.4 to 0.7 mg ZEN/kg Transient changes in hematocrit and hemoglobin concentrations as well as blood basophil and monocyte counts Chowdhury et al. (2005c)
  +
DON, 15-acetyl-DON, ZEN and FA 0.5 to 3.1 µg DON/g, 0.2 g 15-acetyl-DON/g, 0.2 to 0.3 µg ZEN/g and 5.4 to 13.1 µg FA/g Decreased VH in duodenum, decreased VH and AVSA in jejunum at the end of the starter phase.Significant reductions in villus width and AVSA of duodenum, VH and AVSA of jejunum and submucosal thickness of ileum at end of growth phase. Girish et al. (2008)
  +
AST: Aspartate aminotransferase; AF: Aflatoxin: BW: Body weight; DAS: Diacetoxyscirpenol; DON: Deoxynivalenol; FB1: Fumonisin B1; LDH: Lactate dehydrogenase; OA: Ocratoxin A; ZEN: Zearalenone VH: Villus Height AVSA: Apparent Villus Surface Area
  +
  +
  +
  +
  +
  +
  +
  +
  +
Table 5. Feeding and effects of mixed mycotoxins on ducks and broiler breeders
  +
Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source
  +
DON and ZEN (Ducks) 6 to 7 mg DON/kg and 0.05 to 0.06 mg ZEN/kg No effect on feed intake, live weight gain and feed to gain ratio. Decreased weight of the bursa of Fabricius. Danicke et al. (2004)
  +
DON, 15-acetyl-DON and ZEN (Ducks) 0.5 to 17.7 mg DON/kg, 0.2 to 1.0 mg 15-acetyl-DON/kg and 0.5 to 1.3 mg ZEN/kg Mean corpuscular volume and hematocrit decreased, total numbers of white blood cells and lymphocytes increased. Minor adverse effects on plasma chemistry and hematology, and production parameters were unaffected. Chowdbury et al. (2005b)
  +
DON, 15-acetyl-DON and ZEN (Broiler Breeders) 0.2 to 13.8 mg DON/kg, 0.5 to 1.2 mg 15-acetyl-DON/kg and 0.3 to 0.6 mg ZEN/kg Decreased eggshell thickness, increased early embryonic mortality, decreased antibody titers against infectious bronchitis virus. Yegani et al. (2006)
  +
DON: Deoxynivalenol; ZEN: Zearalenone
  +
  +
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Reaction of different poultry types to the combinations of mycotoxins and feed naturally contaminated by mycotoxins


Bonnie A. Nahm and Kee H. Nahm Feed and Nutrition Lab. in Illinois 25001 Cashel Bay Rd. Manhattan, IL 60442 USA Phone and FAX: (815) 478-5069 Email: khnahm1@cs.com



Running head: Mycotoxin contaminated feed and poultry


Cereal grains and animal feeds are often contaminated with mycotoxins including the trichothecenes [ochratoxins (OA), dexyniralenal (DON), nivalenol (NIV), T-2 toxin and diacetoxoyscirpenol (DAS)], zealaleone (ZEN) and the fumonisins, the major mycotoxins of Fusarium fungi. Body weight gains of male broilers were depressed by aflatoxins (AF) and T-2 toxins singly, but further depressed by the combination of the two toxins. The AF plus T-2 toxin combination also increased relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights. The immune system of chickens has low sensitivity to Fusarium mycotoxins while mycotoxin contaminated diets have been related to clinical signs of toxicosis and reduced feed intake, egg production and egg quality. Feeding turkey poults pure T-2 toxin or diacetoxyscripenol (DAS) adversely affected small intestine morphology, but did not affect growth or antibody production. Growing Pekin ducks were not adversely affected in regards to health or performance by dietary DON and ZEN concentrations up to 6 and 0.6 mg/kg.


Introduction

Filamentous fungi produce low molecular weight, secondary metabolites which are mycotoxins. While cereal grains and associated by-products constitute important sources of energy for poultry, there is increasing evidence worldwide that these cereal grains for animal feedstuffs are commonly contaminated with Fusarium mycotoxins, especially in swine. This contamination of food and feedstuffs with mycotoxins is a significant health risk, with estimates of up to 25 % of the world’s crops being contaminated with mycotoxins (Fink-Gremmels, 1999). Annual economic losses estimated for the animal production industries related to mycotoxin contamination are up to several million dollars (Hussein and Brasel, 2001).

  Mycotoxicoses are feed-related, nontransferable and non-infectious diseases (Bennett and Kish, 2003). Acute mycotoxicoses are rare in poultry production, but chronic exposure to low levels of mycotoxins results in reduced productivity and increased susceptibility to infectious diseases (Hussein and Brasel, 2001).The type and concentration of mycotoxin, the duration of exposure, gender, age and health status affects the severity of mycotoxicosis. In animals, the order of decreasing sensitivity to mycotoxins is generally acknowledged as pigs > mice > rats > poultry > ruminants (Rotter et al., 1996). 
  Fusarium moniliforme, which produces the mycotoxins known as fumonisins, is a common contaminant of corn and other grains. The fumonisins include fumonisin B1, B2, B3 and B4, with fumonisin B1 being the major metabolite (Gelderblom et al., 1992). In grains worldwide, Fusarium mycotoxins, DON (vomitoxin) and ZEN are common (Scott, 1989). Analyses of Canadian feeds and feedstuffs for Fusarium mycotoxins have shown DON and fusaric acid as frequent contaminants while ZEN is a less common problem (Smith and Sousadias, 1993; Scott, 1997).
  Trichothecene mycotoxins include DON, nivalenol (NIV), T-2 toxins, 3-ADON and DAS (D’Mello et al. 1999) (Table1). These mycotoxins are potent inhibitors of protein synthesis and can increase disease susceptibility of animals when ingested in sufficient quantities (Bondy and Pestka, 2000).
  D’Mello et al. (1999) have presented a superficial account of the toxicology of Fusarium mycotoxins focusing on structural diversity, biological activity and interactions involving fusaric acid. D’Mello and Macdonald (1997) summarized wide-raging aspects including factors affecting mycotoxin production.
  Mycotoxins from naturally contaminated grain sources may show more toxicity than an equivalent dose of the purified toxin (Harvey et al., 1991).The cause of this phenomenon may be due to the presence of unidentified mycotoxins and the resulting synergistic effects among mycotoxins (Smith et al., 1997). FB1 and DAS or FB1 and OA have not been observed to occur together in a single potential feed grain source.  The possibility exists for co-contamination with FB1 and DAS or FB1 and OA due to multiple grain sources used in poultry and livestock diets. Individual toxicities of mycotoxins cannot be used to predict the toxicity of combinations of mycotoxins (Huff et al., 1985). The question of synergism among co-occurring mycotoxins has remained largely unexplored. “Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity” by D’Mello et al. (1999) showed details in swine and rat, but the effects of combinations of mycotoxins have not been previously reported in poultry. This study will investigate and describe the major effects of feeding poultry diets contaminated with multiple mycotoxins.


Types of mycotoxins

Fusarium monoliforme contaminates corn and other grains and produces mycotoxins known as fumonisins. Fumonisins are classified as fumonisin B1, B2, B3 and B4, with Fumonisins B1 (FB1) as the major metabolite (Huff et al. 1988a). In many tropical countries including China, Thailand and South Africa, FB1 is the contaminant of maize and animal feed while FB2 was predominant form of mycotoxin in Argentinian maize according to the study. Aflatoxins (AF) are mycotoxins produced by fungi of flavus-parasiticus group of the genus Aspergillus and include AF B1, B2, G1 and G2 (Edds and Bortell, 1983). Several species of the fungi in the genus Fusarium produce the mycotoxin T-2 toxin (T-2) (Bamburg et al., 1970), and T-2 has been shown to produce numerous symptoms of toxicity in poultry, as reported by Kubena et al. (1989b).Several parameters of growing broiler chicks are affected by a synergistic interaction between AF and T-2 (Huff et al., 1988b).

  The trichothecenes include over 150 secondary fungal metabolites (Rocha et al., 2005) that show multiple inhibitory effects on eukaryotic cells, including inhibition of protein, DNA and RNA synthesis, mitosis inhibition, interference with cell-membrane integrity and apoptosis induction (Rocha et al., 2005). These mycotoxins primarily affect rapidly proliferating cells and tissues with high rates of protein turnover, including the immune system, liver and small intestine (Feinberg and McLaughlin, 1989).
  One of the trichothecene mycotoxins is deoxynivalenol (DON), while others include nivalenol (NIV), T-2 toxin and diacetoxoyscirpenol (DAS) (Pathre and Mirocha, 1979). DON, commonly called vomitoxin, is a secondary metabolite of Fusarium gramineariam (Schwabe telemorph Gibberella zeac Petch) in the field (Neish et al., 1983; Neish and Cohen, 1981). Among the trichothecenes, DON and NIV co-occur regularly throughout the world, with cereal grains in Poland, Germany, Japan, New Zealand and the Americas having unacceptably high levels (Placinta et al., 1999). Other trichothecenes that co-occur in grains and feeds include 3-acetyl  DON (3-ADON), DAS, T-2 toxin and HT-2 toxin. Concentrations of ZEN are generally low, but cereal grains and animal feeds in Japan, New Zealand and South Africa have been reported to have above average values.
  Ochratoxin A (OA) is a secondary metabolite produced by some strains of Aspergillus ochraceus and Penicillium verrucosum that  is found in various feed ingredients. OA is considered to be substance which is nephrotoxic,  hepatoxic and immunosuppressive (Stormer and Lea,  1995) in all mammals, and it is classified as a possible carcinogen to humans by the International Agency for Research on Cancer (1991). The mechanism of toxicity of OA is unclear. 
  Placinta et al. (1999) concluded that cereal grains and animal feeds on a global scale may be subject to contamination with trichothecenes, ZEN and fumonisins, the major mycotoxin of Fusarium fungi.  There is now compelling evidence that Fusarium mycotoxins are involved in livestock disorders in different parts of the world. Enhanced awareness of the debilitating effects of mycotoxin has not diminished the risk of continued exposure to the mycotoxins.   
  A significant synergistic interaction between AF and T-2 has been shown to affect several parameters of growing broiler chicks (Huff et al., 1988). Another study indicated that both AF and OA adversely affected energy and protein utilization in broilers and this effect was exacerbated when both mycotoxins were fed simultaneously. The toxicity of AF (3.5 g) and OA (2.0 g) resulted in decreased body weight, serum protein, albumin, cholesterol and decreased the relative weights of the liver, kidney and proventriculus (Verma et al., 2002). Effects of chronic feeding of Fusarium mycotoxins on the immunocompetence of a relatively resistant species such as laying hens has not been extensively studied.
  Exposure of mice to ZEN at a dose of 10 mg/kg of diet reduced their resistance to listeriosis. Co-administration of DON and ZEN reduced resistance to Listeria monocytogene to a greater extent even though indices of humoral and cell-mediated immune competence were unaffected (Pestka et al., 1987). ZEN is not only reduced to a- and B-ZEN, but it also is conjugated to glucose according to studied of ZEN metabolism by cell suspension cultures of maize (Zea mavs), wheat (Triticum aestivum) and different fungal species (Rhizopus sp., Thamnidium elefans, Mucor baqinieri). (Engelhardt et al., 1989). 
  Mycotoxins from naturally contaminated grains may be more highly toxic than an equivalent dose of purified toxins (Harvey et al., 1991). This may be the result of the presence of unidentified mycotoxins and precursors in contaminated grain and the synergistic effects of these mycotoxins (Smith et al., 1997). Dietary inclusion if a polymeric glucomannan mycotoxin adsorbent (GMA), extracted from the cell wall of yeast, has benefits in preventing the adverse effects of Fusarium mycotoxin in laying hens (Chowdhury and Smith, 2004) and ducklings (Chowdhury et al., 2005b). 

How do mycotoxins affect the utilization of poultry?

1. Broilers For the poultry industry, the frequent AF contamination of agricultural commodities and exposure of poultry to these toxins can mean the difference between profit and loss (Jones et al., 1982; Nicholas, 1985; Hamilton, 1984). The combination of mycotoxins may pose a greater problem than mycotoxins individually (Kubena et al., 1989a) (Table 2). AF and T-2 interact to farm a synergistic toxicity which threatens poultry production due to the prevalence of these mycotoxins and their interactive toxicity (Huff et al., 1988). The incidence and severity of oral lesions induced by T-2 toxins was increased in the DON/T-2 toxin combination.

  Broiler chicks have been found to be susceptible to Fusarium mycotoxicosis when naturally contaminated grains are fed containing a combination of mycotoxins (Swamy et al., 2002). These feeds contained DON, fusaric acid (FA) and ZEN. Broiler chickens are susceptible during extended feeding of grains naturally contaminated with Fusarium mycotoxins (Swamy et al., 2004). These feeds also contained DON, FA and ZEN. Efficiency of feed utilization by broilers was not affected by diet (Swamy et al., 2002, 2004). The production parameters in these studies were not significantly affected by supplementation of polymeric glycomannan mycotoxin adsorbent (GMA or GM polymer).
  Body weight gains of male broilers were significantly depressed by AF and T-2 singly, and further decreased by the combination of the two toxins (Kubena et al., 1990). Feed utilization was not affected. The AF alone and the AF plus T-2 combination caused increases in relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights. Oral lesions were seen only in chicks receiving theT-2. Addition of a hydrated sodium calcium aluminosilicate (HSCAS) did not alter any of the parameters measured but it did diminish the toxicity of AF, but did not alter the toxicity of T-2. Another study (Kubena et al., 1990) showed the addition of HSCAS to an AF plus T-2 diet diminished some of the effects of AF in the chicken, but it has no effect on T-2 toxicity.
  Huff et al., (1988) observed the effects of AF and T-2 on several parameters of growing broiler chicks. Treatment related changes were seen in red blood cell counts and serum levels of protein, albumin, glucose, cholesterol, calcium, magnesium, lactic dehydrogenase and alkaline phosphatase. There were also significant increases in the relative weights of the liver, kidney, spleen and proventriculus (Kubena et al., 1990). 

2. Layers In commercial birds, consumption of OA contaminated diets has been corrected with clinical toxicosis and reductions in feed intake, egg production and egg quality (Pior and Sisodia, 1978; Verma et al., 2003). Consumption of OA by layers has also been associated with the presence of the toxin and its derivatives in eggs (Piskorska- Plisczynka and Juszkiewica, 1990).Osborne and Hamilton (1981) reported reduced pancreatic digestive secretions in broiler chicks fed AF, while Richardson and Hamilton (1989) noted increased pancreatic digestive enzyme production in egg type chicks fed AF. It has not been ascertained if this is due to an effect on nutrient metabolisability alone or due to an effect on the intestine, or both, which results in increased endogenous or reduced nutrient digestibility, or both. Verma et al. (2003) reported that AF, or both (AF and DON), can have a direct effect on gastrointestinal tract functionality.

  There is very little information on immunocompetence regarding the response or sensitivity of a comparatively resistance species, such as laying hens to mycotoxins. In a study where both of the feeds were contaminated with AF or DON, or with two or more toxins mixed, most immunotoxic effects were short term, but prolonged consumption of purified DON and ZEN resulted in disappearance of adverse effects, which were mainly attributed to feed refusal rather than systemic toxicity. Host resistance to Listeria monocycytogenes and the delayed-type hypersensitivity (DTH) response in mice was altered by 10 mg of purified DON/kg feed (Pestka et al., 1987), but 50 mg/kg was required to alter splenocyte blastogenic response to phytohemagglutinin-P of laying hens (Harvey et al., 1991). Thus, it appears that there is a low sensitivity to Fusarium mycotoxins by the immune system of chickens. Chowdhury and Smith (2005) (Table 3) concluded that chronic consumption of grains contaminated with Fusarium mycotoxins of levels usually found in practice were not systemically immunosuppressive or hematotoxic, but mucosal immunocompetence needs to be explored further in “Effects of feed-borne Fusarium mycotoxins on hematology and immunology of laying hens”.
  Research results did not show much information about AF or T-2 toxin, but there were results showing that addition of Ochratoxin A (OTA) + Ocratox (Ochratoxin-Binding Agent or containing 5 g OCra Tox/kg of feed)(containing 2 g OTA and 5 g ochratoxin/kg of feed) counteracted the  deleterious effects OTA in 47 week old laying hens (Denli et al., 2008). They concluded Ocratax counteracted the deleterious effects of OTA in laying hens.      

3) Turkeys Fusaria fungi are commonly associated with corn, a major component of most poultry diets and toxic effects of these Fusaria include immunosuppression (Marijanovoc et al., 1991), diarrhea, reduced growth and feed utilization (Brown et al., 1992), cardiotoxicity (Engelhardt et al., 1989), leg shape deformities (Sharby et al., 1973), rickets (Gedek et al., 1978; Brown et al., 1992), and high mortality in the turkeys (Jeschke et al., 1987). Another major finding by Wu et al. (1994) was that culture materials of some Fusaria increased the redness of turkey breast muscle without causing obvious hemorrhages in the musculature or internal organs. F. proliferatum (Javed et al., 1993) containing FB1 caused poor performance, increased organ weights and hepatitis in broilers, while in turkeys it was associated with reduced performance and increased organ weights (Weibking et al., 1993; Kubena et al., 1995a,b).

  There are very few reports of the effects of feeding of grains naturally contaminated with Fusarium mycotoxins to turkeys. Minor adverse effects on the hematology and  some immunological indices of turkeys were seen with chronic consumption of grains naturally contaminated with Fusarium mycotoxins (Chowdhury et al., 2005c). Increased susceptibility of turkeys to infectious agents against which CD58 + T cells play a major role in defense has been associated with consumption of grains naturally contaminated with Fusarium mycotoxins. Girish et al. (2008) concluded turkey performance and some blood and immunological parameters were adversely affected by feed borne Fusarium mycotoxins, and EMA prevented many of these effects.
   Effects of other mycotoxins have been reported on certain parameters in turkeys. Resistance to Listeria monocytogenes was reduced to a greater extent by coadministration of DON with ZEN even though indices of humoral and cell-mediated immune competence were not affected (Pestka et al., 1987). Feeding pure T-2 toxin or DAS to turkey poults at levels up to 1 mg/kg of feed for 32 days adversely influenced small intestine morphology but had no effect on growth or antibody production (Sklan et al., 2003). The feeding of a combination of T-2 toxin and DAS resulted in severe oral lesions (Awad et al., 2006). Fairchild et al. (2005) also observed that feeding a combination of FA (300 mg/kg of feed) and DAS (4 mg/kg of feed) to turkey poults for 18 d decreased enterocyte height at mid villus by 59 %. Feeding FA alone reduced the relative weight of the intestine serosal thickness while feeding DAS alone increased serosal thickness.
  In turkey poults 7 to 14 days of age, McMillan and Moran (1985) found that neither vomitoxin (75 mg/kg) nor ZET (50 mg/kg) decreased growth or feed consumption. Salinomycin fed at or below dosages recommended for broilers (60 mg/kg) caused mortality and clinical lesions in adult turkey, but not growing turkey (Halvorson et al., 1982). In a study by Manley et al. (1988),turkey poults fed the suspect commercial diet had significantly lower feed consumption and higher mortality than poults fed a control diet. There were no significant decreases in feed consumption, body weight gain or viability in poults (0 to 3 wks of age) fed diets containing vomitoxin (4.4 mg/kg), salinomycin (22 mg/kg) or both. When turkey poults were fed diets containing moniliformin (M) alone or with the DON-M combination, there was an increased incidence of variable sized cardiomyocyte nuclei, with numerous large giant nuclei, and a generalized loss of cardiomyocyte cross striations. In the poults fed the M and combination DON-M treatments. Mild diffuse mineralizations were noted in isolated renal tubule sections of the kidney. None of the response variables measured were noted in the DON treatments alone (Morris et al., 1999) (Table 4). Kubena et al. (1989a) noted a similar reaction between DON and T-2 toxin in chicks. When compared with controls, body weight gains of turkey poults were reduced by 30 % (Study 1.) and 24 % (Study 2.) by FB1, 30 % by DAS, 8 % by OA, 46 % by the FB1 and DAS combination and 37 % by the FB1 and OA combination.  The impact of these mycotoxins on the health and performance of poultry could be altered under field conditions by other stress factors (Kubena et al., 1997a).   

4) Ducklings In studies with ducklings, DAS (4,15-Dicetoxyseripental) has been implicated in reduced feed intake, feed refusal or toxicity (Steyn et al., 1978). DAS is a toxic secondary metabolite that is naturally occurring and is predominantly associated with Fusarium species (Pathre and Mirocha, 1979).

  When a diet containing 1.2 mg DON/kg, 4.5 mg fumonisin/kg and 0.01 mg AFB1/kg was fed to white Pekin ducklings, 50 % morality was reported after 7 d of feeding because of total feed refusal (Davis et al., 1980). However, another study (Boston et al., 1996) reported no adverse effects on feed intake, body weight gain, organ weights or plasma chemistry when adult Mallard ducks were feed wheat naturally contaminated with 5.8 mg DON/kg for 2 wks. These animals may become susceptible to infections agents such as viruses against which the CD8+ T cell provides necessary defense when fed mycotoxin-contaminated feeds. According to a report by Chowdhury et al. (2005b) (Table 5), glucomannan mycotoxin-adsorbent was not effective in preventing alterations in ducklings caused by Fusarium mycotoxin. They reported mean corpuscular hemoglobin concentrations and hematocrit decreased when ducks were fed contaminated grains for 4 or 6 wks, respectively. In contrast, total numbers of white blood cells and lymphocytes increased transiently in birds fed contaminated gains for 4 wks.
  In anther study by Danicke et al. (2002) concentrations of DON and its de-epoxydised metabolite in the plasma and bile of ducks were lower than the detection limits of 6 and 16 µg/ml, respectively. ZON or its metabolites were not detectable in plasma or livers. Taken together, it can be concluded that dietary DON and ZON concentrations up to 6 and 0.06 mg/kg, respectively, did not affect the performance and health of growing Pekin ducks.
  The acute toxicity (LD 50) of fusarium toxins have been frequently titrated using 1-day-old ducklings (Ueno, 1985). One-day-old ducklings showed an LD50 dose of DON estimated at 27 mg/kg, while 1-day-old broiler chicks had a much higher LD 50 dose of 140 mg/kg body weight (Huff et al., 1981). Conclusions about chronic toxicity of DON in ducks can not be drawn from information on acute toxicity.   

5. Broiler breeders Egg production was not significantly affected by feeding of mycotoxin contaminated grains. Eggshell thickness was decreased at the end of wks 4, but dietary GMA supplementation prevented this effect. Other egg parameters measured were not affected by the diet (Yegani et al., 2006) (Table 5). There was a significant increase in early (1 to 7 d) embryonic mortality from birds fed contaminated grins at wk 4, but diet did not affect mid (8 to 14 d) and late (15 to 21 d) embryonic mortality. Feeding of the contaminated grains did not affect ratio of chick weight to egg weight (Yegani et al., 2006). This research also found that rooster semen volume and sperm concentration, viability and motility weight were not affected by feeding the contaminated diets.

  The trichothecenes, which include over 150 fungal metabolites, are known to have multiple inhibitory effects on eukaryotic cells, including inhibition of protein, DNA and RNA synthesis; inhibition of mitosis; interference with cell membrane integrity; and induction of apoptosis (Bennett and Klich, 2003; Rocha et al ., 2005). Dietary inclusion of a GMA, extracted from the cell wall of yeast, has some beneficial effects of Fusarium mycotoxins in broilers (Swamy et al., 2002, 2004), laying hens (Chowdhury and Smith, 2004) and ducklings (Chowdhury et al., 2005b). 

CONCLUSION

Different poultry show different affects of feeds contaminated with mycotoxin, either singly or in combinations of two or more mycotoxins. Body weight gains of male broiler were significantly depressed by AF and T-2 singly, and further decreased by the combination of the two toxins. Feed utilization was not affected, but the AF alone and the AF plus T-2 combination caused increases in relatives in relative liver, kidney, proventriculus, gizzard, spleen and pancreas weights (Hamilton, 1984).

  When feeds containing DON, FA and ZEN were fed in another study (Swamy et al., 2004), the efficiency of feed utilization was not affected by polymeric glucomannan mycotoxin adsorbent (GMA) supplementation. FA has been shown to have a direct or indirect effect, or both, on functionality of the gastrointestinal tract of laying birds Santin et al., 2002). Chowdhury et al. (2005a) concluded that chronic consumption of grains naturally contaminated with Fusarium mycotoxins of levels likely to be encountered in practice were not systemically immumsuppressive or hepatotoxic, even though the immune system of chickens has low sensitivity to Fusarium mycotoxins. Clinical signs of toxicosis and reduced feed intake, egg production have been related to consumption at OA contaminated feeds by commercial birds (Pior and Sisodia, 1978; Raymond et al., 2003). 
  Diets contaminated with F. proliferatum (Javed et al., 1993) containing FB1 have been associated with poor performance, increased organ weights and hepatitis in broilers, while turkeys showed reduced performance and increased organ weights (Weibking et al., 1993; Kubena et al., 1995 a,b). Coadministration of DON and ZEN reduced in greater reductions of resistance to Listeria monocytogene (Pestka et al., 1990). Severe oral lesions resulted from feeding both T-2 and DAS. The redness of turkey breast meat was increased by feeding of fusarial culture materials (Wu et al., 1994). In another study (Kubena et al., 1997b), body weight gains compared to the control were reduced by 30 % (study 1) and 24 % (study 2) by FB1, 30 % by DAS, 8 % by OA, 46 % by the FB1 and DAS combination and 37 % by the FB1 and OA combination. Feeding turkey poults pure T-2 and DAS on levels up to 1 mg/kg of feed for 32 days adversely influenced small intestinal morphology but did not affect growth or antibody production (Sklan et al., 2003).
  In White Pekin ducklings, 50 % mortality was seen after feeding a diet containing 1.2 mg or DON/kg, 4.5 mg of fumonisin/kg and 0.01 AFB1 /kg for 7 days because of total feed refusal (Davis et al., 1980). Dietary DON and ZEN concentrations up to 6 and 0.6 mg/kg did not adversely affect performance and health of growing Pekin ducks (Danicke et al., 2002).
  Mycotoxins contaminated diets were shown to decrease egg shell thickness at the end of 4 wks of feeding, but dietary supplementation with GMA prevented this effect (Yegani et al., 2006). There was no effect of diet on other egg parameters, rooster semen volume and sperm, concentration and viability.   

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Table 1. Effects of individual trichothecenes in poultry Trichothecene Poultry type Effects Data Source DON Laying hens Transmission to eggs following oral administration Prelusky et al. (1987) DAS Broiler Chickens Reduced bodyweight; dose-related mouth lesions Ademoyero and Hamilton (1991) T-2 toxin Ducklings Reduced bodyweight and weights of thymus, spleen, and bursa of Faricii; oral and esophageal ulcerations Neiger et al. (1994) T-2 toxin Geese Decreased egg yields and hatchability; mortality Vanyi et al. (1994a) T-2 toxin Geese Dose-dependent cessation of follicle maturation in ovaries; follicle degeneration; involution of oviduct; lymphocyte depletion; lesions in adrenal and thyroid glands. Vanyi et al. (1994b) NIV Broiler chickens Reduced feed consumption and weight gain: gizzard erosions; reduced relative liver weight Hedman et al. (1995) T-2 toxin Turkey poults Reduced bodyweight gain; oral lesions Kubena et al. (1995a) DAS Turkey poults Reduced feed intake, weight gain and feed efficiency; oral lesions Kubena et al. (1997b) DON Broiler Chickens Increased relative weights of gizzard, bursa of Fabricus and heart Kubena et al. (1997a) T-2 toxin Broiler Chickens Reduced bodyweight gain; oral lesions Kubena et al. (1997a)





Table 2. Feeding and effects of mixed mycotoxins on broilers Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source AF and T-2 2.5 µg AF/g and 4.0 µg T-2/g Decreased BW, increased weights of kidney, gizzard and heart, decreased mean corpuscular volume and serum potassium Huff et al. (1988) OA and T-2 2.0 mg/kg OA and 4.0 mg/kg T-2 Increased liver, kidney, proventriculus and gizzard weights, decreased body weight gains, mean corpuscular volume and serum protein levels Kubena et al. (1989a) DON and T-2 16 mg DON/kg and 4 mg T-2/kg Decreased total body weight gains and final body weights, increased incidence and severity of oral lesions Kubena et al. (1989b) AF and T-2 3.5 mg AF/kg and 8.0 mg T-2/kg Depressed BW gains, increased weights of liver, kidney, proventriculus, gizzard, spleen and pancreas Kubena et al. (1990) DON, FA and ZEN 0.14 to 9.7 mg DON/kg, 20.6 to 21.6 mg FA/kg, 0.2 to 0.8 mg ZEN/kg Decreased BW, increased blood erythrocyte count and serum uric acid, decreased serum lipase, reduced breast muscle redness. Swamy et al. (2002) AF and OA 0.5 to 2.0 mg AF/kg and 1.0 to 4.0 mg OA/kg Decreased energy and protein utilization Verma et al. (2002) DON, FA and ZEN 5.9 to 9.5 mg DON/kg, 19.1 to 1.4 mg FA/ kg and 0.4 to 0.7 mg ZEN/kg Decreased BW gains and feed consumption, decreased peripheral blood monocytes, decreased B-cell and T-cell counts Swamy et al. (2004) AF and OA 0.5 to 2 mg AF/kg and 1 to 4 mg OA/kg Growth depression, reduced food consumption and poor food conversion efficiency. Decreased weight of bursa of Fabricius, reduced cell mediated immunity. Verma et al. (2004)

AF: Aflatoxin: BW: Body weight;  DON: Deoxynivalenol;  FA: Fusaric Acid;   OA: Ochratoxin A;                       ZEN: Zearalenone     

Table 3. Feeding and effects of mixed mycotoxins on laying hens Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source DON, FA and ZEN 11.7 to 12.1 µg DON/g, 18 µg FA/g and 0.6 µg ZEN/g Decreased feed consumption, egg production, egg and eggshell mass. Increased plasma uric acid concentrations and kidney wieghts. Chowdhury and Smith (2004) DON, 15-acetyl-DON, and ZEN 12.6 µg DON/g, 1.2 µg 15-acetyl-DON and 0.7 µg ZEN/g Decreased fractional protein synthesis rate. Chowdhury and Smith (2005) DON, 15-acetyl-DON, and ZEN 12 mg DON/kg, 0.5 mg 15-acetyl DON/kg and 0.6 mg ZEN/kg Decreased hematocrit values, total numbers of white blood cells, lymphocytes and biliary IgA concentration. Chowdhury et al. (2005a) DON and ZEN 17,630 µg DON/kg and 1,580 µg ZEN/kg Depressed feed intake, nutrient digestibility,metabolizability of gross energy, serum titers to Newcastle disease virus. Increased yolk titers to antigen K88. Danicke et al. (2002) OA 2 mg OA/kg Decreased daily feed consumption, egg mass production and serum triglyceride concentrations. Increased relative liver weight, serum alkaline phosphatase and uric acid. Denli, et al. (2008) DON: Deoxynivalenol; FA: Fusaric Acid; OA: Ochratoxin A; ZEN: Zearalenone






Table 4. Feeding and effects of mixed mycotoxins on turkeys Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source DON and Salinomycin 4.4 mg DON/kg and 2.2 mg Salinomycin/kg Lower feed consumption and higher mortality Manley et al. (1988) FB1 and DAS or OA 300 mg FB1/kg, 4 mg DAS/kg and 3 mg OA/kg Decreased BW gains and efficiency of feed utilization, increased liver weight, increased serum cholesterol and increased AST and LDH Kubena et al. (1997b) DON and Monoliformin 20 mg DON/kg and 100 mg Monoliformin/kg Decreased mean cell volume, increased incidence of variable sized cardiomyocyte nuclei, mild diffuse mineralization of real tubules Morris et al. (1999) DON, 15-acetyl-DON and ZEN 6.8 to 13.6 mg DON/kg, 0.6 to 1.3 mg 15-acetyl-DON/kg and 0.4 to 0.7 mg ZEN/kg Transient changes in hematocrit and hemoglobin concentrations as well as blood basophil and monocyte counts Chowdhury et al. (2005c) DON, 15-acetyl-DON, ZEN and FA 0.5 to 3.1 µg DON/g, 0.2 g 15-acetyl-DON/g, 0.2 to 0.3 µg ZEN/g and 5.4 to 13.1 µg FA/g Decreased VH in duodenum, decreased VH and AVSA in jejunum at the end of the starter phase.Significant reductions in villus width and AVSA of duodenum, VH and AVSA of jejunum and submucosal thickness of ileum at end of growth phase. Girish et al. (2008) AST: Aspartate aminotransferase; AF: Aflatoxin: BW: Body weight; DAS: Diacetoxyscirpenol; DON: Deoxynivalenol; FB1: Fumonisin B1; LDH: Lactate dehydrogenase; OA: Ocratoxin A; ZEN: Zearalenone VH: Villus Height AVSA: Apparent Villus Surface Area





Table 5. Feeding and effects of mixed mycotoxins on ducks and broiler breeders Mycotoxins fed Concentration of Mycotoxin in Feed Effects Data Source DON and ZEN (Ducks) 6 to 7 mg DON/kg and 0.05 to 0.06 mg ZEN/kg No effect on feed intake, live weight gain and feed to gain ratio. Decreased weight of the bursa of Fabricius. Danicke et al. (2004) DON, 15-acetyl-DON and ZEN (Ducks) 0.5 to 17.7 mg DON/kg, 0.2 to 1.0 mg 15-acetyl-DON/kg and 0.5 to 1.3 mg ZEN/kg Mean corpuscular volume and hematocrit decreased, total numbers of white blood cells and lymphocytes increased. Minor adverse effects on plasma chemistry and hematology, and production parameters were unaffected. Chowdbury et al. (2005b) DON, 15-acetyl-DON and ZEN (Broiler Breeders) 0.2 to 13.8 mg DON/kg, 0.5 to 1.2 mg 15-acetyl-DON/kg and 0.3 to 0.6 mg ZEN/kg Decreased eggshell thickness, increased early embryonic mortality, decreased antibody titers against infectious bronchitis virus. Yegani et al. (2006)

 DON: Deoxynivalenol;      ZEN: Zearalenone     

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