Comparative aspects of Fusarium mycotoxicoses in broiler chickens, laying hens and turkeys and the efficacy of a polymeric glucomannan mycotoxin adsorbent

Fusarium fungi thrive in temperate climates around the world and Fusarium mycotoxins are the mycotoxins most commonly found in feed grains and forages (Wood, 1992). There are numerous pathologies characteristic of Fusarium mycotoxicoses and this is due to the several chemically distinct groups of Fusarium mycotoxins, which have very different effects on animal metabolism and behavior. Swine are usually considered to be the most sensitive species to feed-borne mycotoxins both with respect to feed refusal and to reproductive failure. Ruminant animals are thought to be the most resistant because of the detoxifying effect of rumen microorganisms. Poultry are generally considered to be less sensitive than swine and are often the recipients of contaminated grains diverted from swine feeds.

The Fusarium mycotoxin most often detected in Canadian-grown grains is the trichothecene deoxynivalenol (DON, vomitoxin) (Scott, 1997). Trichothecene toxicosis is characterized by reduced appetite, lesions of the intestinal tract and immunosuppression. Another frequently detected compound is zearalenone, an estrogenic mycotoxin that impairs mammalian reproduction.

It has been reported that broiler chicks can tolerate up to 15 ppm DON from naturally-contaminated wheat and oats without adverse effects on performance (Hulan and Proudfoot, 1982; Kubena et al., 1987). Others, however, observed reduced performance and changes in immune function, hematology and serum chemistry in broiler chicks fed 16 to 18 ppm DON from naturally contaminated sources (Huff et al., 1986; Kubena et al., 1988; 1989; Harvey et al., 1991). It is clear however, that broiler chickens are far less sensitive than swine to DON contaminated feeds, particularly with respect to reduced feed intake (Smith et al., 1997).

It has been reported that the feeding of 100 ppm zearalenone had no effect on layer performance, fertility or hatchability (Marks and Bacon, 1976). The feeding of DON at 5 ppm (Hamilton et al., 1985) or 18 ppm (Kubena et al., 1987) did not affect layer performance. A combination of DON (2-3 ppm) and zearalenone (0.4–0.5) also resulted in no adverse effects on layer performance (Kesharvarz, 1993).

Layer performance was adversely affected, however, when a corn-based diet was fed containing 17.6 ppm DON and 1.6 ppm zearalenone (Danicke et al., 2002). Adverse effects on layer performance are often greater under field conditions (Keshavarz, 1993). It is often difficult, however, to explain why this occurs (Williams et al., 1992).

There is less information available regarding the feeding of contaminated grains to turkeys. Hamilton et al. (1985) indicated that turkey poults can tolerate diets containing at least 5 ppm DON. Manley et al. (1988) described feed refusal and high mortality in a commercial turkey flock fed diets containing 81 ppb DON + 2.2 ppm salinomycin. The feeding of 4.4 ppm DON + 22 ppm salinomycin had no effect on feed consumption or viability. Morris et al. (1999) observed that the feeding of 20 ppm DON had no adverse effects on poults and no toxicological interaction was observed between DON and moniliformin.

The discrepancy between the relative tolerance of poultry to Fusarium mycotoxins in literature reports and the seeming susceptibility of poultry under commercial conditions may be due to several factors.

Many of the experiments conducted in literature reports were for fairly short periods. This is often necessary to conserve valuable stocks of purified mycotoxins or fungal culture materials. The use of purified mycotoxins, fungal culture materials or artificially inoculated corn can also bias findings because the toxicological synergism arising from the feeding of combinations of mycotoxins does not take place.

Polymeric mycotoxin adsorbents prevent mycotoxicoses by adsorbing mycotoxins in the intestinal lumen and preventing transfer through the blood to target tissues (Ramos et al., 1996). The current studies were conducted to determine the efficacy of Mycosorb®, a glucomannan polymer extracted from the cell wall of yeast, in preventing the adverse effects of blends of grains naturallycontaminated with Fusarium mycotoxins on poultry.


Materials and methods

EXPERIMENTAL FEEDSTUFFS

Mycotoxins in the current experiments were provided by a blend of naturally contaminated corn and wheat purchased from producers in Southwestern Ontario. The complete diets were analyzed for DON, 3-acetyl- DON, 15-acetyl-DON, nivalenol, T-2 toxin, iso T-2 toxin, acetyl-T-2 toxin, HT-2 toxin, T-2 triol, T-2 tetraol, fusarenon-X, diacetoxyscirpenol, scirpentriol, 15-acetoxyscirpentriol, neosolaniol, zearalenone, zearalenol, aflatoxin and fumonisin by gas chromatography and mass spectrometry at the Veterinary Diagnostic Laboratory, North Dakota State University, Fargo, North Dakota (Raymond et al., 2003). Fusaric acid was determined by the high performance liquid chromatographic method of Matsui and Watanabe (1988) as modified by Smith and Sousadias (1993) and confirmed by Porter et al. (1995).


EXPERIMENTAL DESIGN

Broilers

Broiler chicks were fed starter (0 – 3 weeks), grower (3 – 6 weeks) and finisher (6 – 8 weeks) diets in two 56-day experiments (Swamy et al., 2002; 2004a). Diets included: 1) control, 2) low level of contaminated grains, 3) high level of contaminated grains, and 4) high level of contaminated grains + 0.2% Mycosorb®. Growth rates and feed consumption were monitored weekly. At the end of the study, blood and tissue samples were taken for hematology and serum chemistry measurements.


Laying hens

One hundred and forty-four, 45-week-old laying hens were fed for 12 weeks diets including: 1) control, 2) contaminated grains, and 3) contaminated grains + 0.2% Mycosorb®. Parameters measured included feed consumption, egg production, egg shell measurements, egg quality measurements, relative organ weights and plasma chemistry.


Turkeys

Two hundred and twenty-five day-old male turkey poults were fed corn, wheat and soybean meal-based starter (0-3 weeks), grower (3-6 weeks), developer (6 – 9 weeks) and finisher (10 – 12 weeks) diets in a 12-week experiment. Diets included: 1) control, 2) contaminated grains, and 3) contaminated grains + 0.2% Mycosorb®. Parameters measured included weight gain, feed consumption, relative organ weights and plasma chemistry.


Results

MYCOTOXIN ANALYSES

Of the twenty different mycotoxins analyzed for, only DON, 15-acetyl DON, zearalenone and fusaric acid were found in detectable quantities in all experimental diets. DON was found to be approximately 0.5 ppm, 5.0 ppm, 9.0 ppm and 10.0 ppm for the four experimental broiler diets. The concentrations of 15- acetyl DON were about 0.5 ppm, zearalenone was about 0.5 ppm and fusaric acid was about 17 ppm.

Diets fed to laying hens which contained contaminated grains had an average of 12.0 ppm DON with the other three mycotoxins in the same ratios as were seen in the broiler trials. In the turkey trial, diets containing contaminated grains averaged 6.5 ppm, 7.6 ppm, 10.6 ppm and 13.3 ppm DON for the starter, grower, developer and finisher phases with the other three mycotoxins present in the same proportions as were seen for the broiler and layer experiments.


BROILERS

There was a significant linear decrease in growth rate and feed consumption in the grower period when increasing levels of contaminated grains were fed to rapidly growing broilers (Swamy et al., 2004a; Table 1). No significant effect of diet was seen in the starter or finisher periods. When broilers were growing more slowly, growth depression was observed in the finisher phase (Swamy et al., 2002). At the end of the finisher phase in the earlier study, it was observed that the feeding of contaminated grains elevated red blood cell count and blood concentrations of hemoglobin and uric acid (Table 2). Biliary concentrations of immunoglobulin A were reduced while breast meat redness increased. The feeding of 0.2% Mycosorb® prevented all of the above dietary effects.


LAYING HENS

The feeding of contaminated grains decreased feed consumption compared to controls in the first month (P<0.05) (Table 3). Feed intake increased, however, in the second and third months. The feeding of Mycosorb® prevented this increase in the third month and also prevented a decrease in feed efficiency. At the end of the experiment, it was observed that hens fed contaminated grains had an increased relative kidney weight compared to controls; this effect was prevented by the feeding of Mycosorb®.

Egg production and egg mass decreased (P<0.05) compared to controls in the first two months when contaminated grains were fed. The feeding of Mycosorb® prevented this in the first month. The most obvious effect of feeding contaminated grains on plasma chemistry was on uric acid concentrations (Table 4). In each month, plasma uric acid concentrations were significantly increased with the feeding of contaminated grains. In each case, this increase was prevented by the feeding of Mycosorb®.


TURKEYS

The feeding of contaminated grains reduced growth rates in the starter, developer and finisher phases and overall (Table 5). The feeding of Mycosorb® prevented these effects. The most obvious effect of diet on plasma chemistry was on plasma uric acid concentrations (Table 6). After 4 and 8 weeks of feeding contaminated grains, plasma uric acid concentrations were significantly reduced. This effect was not seen, however, when birds received Mycosorb®. At the end of the experiment, turkeys fed contaminated grains + Mycosorb® had significantly smaller spleens and kidneys and significantly larger bursas than birds fed unsupplemented contaminated grains.


Table 1.Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on weight gain and feed consumption of broiler chickens.<sup>1


1</sup>From Swamy et al., 2004a.
²Values are least square means; n = 3.
³Values are least square means; n = 90.
⁴Not significant (P>0.05).


Table 2.Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on hematology, serum chemistry and breast meat coloration of broiler chickens.<sup>1


1</sup>From Swamy et al., 2002.
²Red blood corpuscle counts (1012/L); n = 12.
³Hemoglobin concentration (ppm); n = 12.
⁴Uric acid concentration (μmoles /L); n = 12.
⁵Unitless scale, 0 = green, 1 = red; n = 15.
⁶mm precipitate; n = 15.


Table 3.Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on feed consumption and feed efficiency of laying hens.


¹n = 12. ²n = 12. ³Not significant (P>0.05).


Table 4.Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on organ weights and plasma uric acid concentrations of laying hens.


¹n = 12.
²Not significant (P>0.05).


Table 5. Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on growth of turkeys (g/bird/week).




Table 6. Effect of feeding blends of grains naturally-contaminated with Fusarium mycotoxins on organ weights and plasma uric acid concentrations of turkeys.


¹n = 12.
²Not significant (P>0.05).


Discussion

Broilers, layers and turkeys are all sensitive to Fusarium mycotoxicoses. The adverse effects of the diets fed in the current studies are greater than literature reports based on the DON content. This is likely because of the relatively short duration of previously reported trials. The blending of different naturally contaminated grains, moreover, also results in a more complex mixture of mycotoxins thereby increasing the chances of toxicological synergy between mycotoxins.


BROILERS

The observation that feeding contaminated grains to broilers reduced growth only in the grower and finisher phases supports the concept that broilers do not exhibit feed refusal in a manner similar to swine fed Fusarium mycotoxin contaminated diets (Smith et al., 1997). The reason for this species difference has been shown to be differences in the effects on brain neurochemistry (Swamy et al., 2004b). The feeding of contaminated grains to pigs elevated brain serotonin concentrations. In broilers, such treatments elevated both serotonin and catecholamines thereby canceling the effect of serotonin on appetite suppression. It is likely that mycotoxin-induced growth suppression in broilers was due to gradual alterations in metabolism that occurred with extended feeding of contaminated grains.

The mycotoxin-induced elevation in red blood cell count and hemoglobin is similar to the changes seen in ascites. It is possible that the hypotensive effect of fusaric acid may be reducing blood flow to the lungs resulting in an increased need for oxygen trapping capacity of blood. Elevations in blood uric acid concentrations were likely due to the inhibition of protein synthesis caused by trichothecenes such as DON and 15-acetyl DON. This would result in increased hepatic oxidation of amino acids and increased uric acid excretion. Red discoloration of breast meat has been reported in turkeys fed Fusarium culture filtrates (Wu et al., 1994). The discoloration seen in the current study was likely due to increased red blood cell count and hemoglobin concentrations as well as to edema arising from the hypotensive effects of fusaric acid. The reduced biliary immunoglobulin A concentrations may have arisen from trichothecene-induced inhibition of protein synthesis.


LAYING HENS

The effect of feeding contaminated grains on feed intake of laying hens is in contrast to that seen in broilers. It would seem that after an initial reduction in feed intake and egg production, layers increased feed intake perhaps in an attempt to boost egg production. The result, however was a very dramatic deterioration in feed efficiency (feed consumed/egg mass). This may be due, in part, to increased hepatic amino acid oxidation due to the trichothecene-induced reduction in protein synthesis. It is notable that the mycotoxin-induced elevation in blood uric acid concentrations is similar to, but greater in magnitude than, the response seen in broilers. The increased kidney weight seen when contaminated grains were fed is likely due to the increased metabolic burden of excretion arising from increased uric acid synthesis.


TURKEYS

Feeding contaminated grains significantly reduced weight gain of turkey poults as early as the second week of feeding. This is a more rapid effect than was seen in broilers but little effect of diet was seen on feed consumption. It would appear that turkeys are more sensitive to this mycotoxin challenge than broilers. The significant depression in blood uric acid concentrations after 4 and 8 weeks of feeding is in marked contrast to the responses seen in broilers and laying hens. The metabolic reason for this remains to be determined as other indices of blood chemistry were largely unaffected by diet.


EFFECTS OF MYCOSORB®

Mycosorb® proved to be a very effective preventative treatment for Fusarium mycotoxicoses in broilers, layers and turkeys. The mode of action of Mycosorb® is to prevent intestinal uptake of mycotoxins and subsequent transfer of mycotoxins to sensitive target tissues such as liver, kidney, brain and reproductive tract. It is clear from the efficacy of Mycosorb® in these trials that it is capable of adsorbing a combination of Fusarium mycotoxins and minimizing the potential for toxicological synergism.


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