Effects of Prolonged Administration of Aflatoxin B 1 and Fumonisin B 1 in Laying Japanese Quail
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1 Effects of Prolonged Administration of Aflatoxin B 1 and Fumonisin B 1 in Laying Japanese Quail R. Ogido,* C. A. F. Oliveira,,1 D. R. Ledoux, G. E. Rottinghaus, B. Corrêa, P. Butkeraitis,* T. A. Reis, E. Gonçales, # and R. Albuquerque* *Departamento de Nutrição e Produção Animal, Faculdade de Medicina Veterinária e Zootecnia; Departamento de Engenharia de Alimentos, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, Pirassununga, SP, , Brazil; Fusarium/Poultry Research Laboratory, University of Missouri, Columbia, Missouri 65211; Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil; and #Centro de Pesquisa e Desenvolvimento de Saúde Animal, Instituto Biológico, São Paulo, SP, , Brazil ABSTRACT In the present study, wk-old Japanese µg ofafb 1 /kg, and 10 mg of FB 1 +50µg of AFB 1 /kg of quail were randomly distributed into 6 experimental feed. Egg production decreased (P < 0.05) in birds fed 10 groups (48 birds per group) and fed the following diets mg of FB 1 /kg by the third, fourth, and fifth cycles. Feed for 140 d: 1) 0 (control); 2) 10 mg of fumonisin B 1 (FB 1 ); intake was lower (P < 0.05) in birds fed 10 mg of FB 1 /kg 3) 50 µg of aflatoxin B 1 (AFB 1 ); 4) 50 µg of AFB 1 +10mg by the fourth and fifth cycles, and in birds fed 50 and of FB 1 ; 5) 200 µg of AFB 1 ; and 6) 200 µg ofafb 1 +10mg 200 µg of AFB of FB 1 /kg of feed. Each treatment consisted of 4 replicates 1 /kg in the fifth cycle. Birds fed 10 mg of of 12 quail. Egg production and individual egg weight FB 1 +50µg ofafb 1 /kg consumed less feed (P < 0.05) in were checked daily. Feed intake and feed conversion were the first, second, and fifth cycles. Results indicated that determined weekly. Results showed that by the end of prolonged administration of FB 1 and AFB 1, singly or in the fifth cycle, average egg weight was lower (P < 0.05) in groups fed 10 mg of FB 1 /kg, 50 µg ofafb 1 /kg, 200 combination at the levels evaluated, may cause economic losses to quail egg producers. (Key words: aflatoxin B 1, fumonisin B 1, quail, toxicity) 2004 Poultry Science 83: INTRODUCTION Mycotoxins are classified as secondary metabolites that have no biochemical significance in fungal growth and development (Moss, 1998); they are produced mainly by the mycelial structure of filamentous fungi (Hussein and Brasel, 2001). Aflatoxins are produced by storage fungi of the genus Aspergillus, particularly A. flavus, A. parasiticus, and A. nomius (Moss, 1998). Twenty aflatoxins have been identified, with the major ones being B 1,B 2,G 1, and G 2 ; with aflatoxin B 1 (AFB 1 ) being the most common and toxic compound (Hussein and Brasel, 2001). Effects of aflatoxins are dose- and time-dependent and 2 distinct forms of aflatoxicosis, acute and chronic, are observed (Osweiler, 1990). The liver is the main target organ (Sawhney et al., 1973). In poultry, AFB 1 causes immunosuppression and decreased BW gain and feed use. Reduced egg production and egg weight are the most frequently reported manifestations of aflatoxicosis in layers (Leeson et al., 1995) Poultry Science Association, Inc. Received for publication December 4, Accepted for publication August 3, To whom correspondence should be addressed: carlosaf@usp.br. Oliveira et al. (2002) fed Japanese quail diets containing AFB 1 at 25 to 100 µg/kg for 168 d and found that chronic exposure to AFB 1 at levels above 50 µg/kg can adversely affect quail performance, especially feed intake, egg weight, and percentage eggshell. Fumonisins are produced by fungi of the genus Fusarium, particularly F. verticillioides, F. proliferatum, F. anthophilum, F. nygamai, and F. napiforme (Moss, 1998). Eighteen fumonisins have been identified, and the major and most toxic compound is fumonisin B 1 (FB 1 ) (Ah-Seo and Won-Lee, 1999). Fumonisins have been associated with animal diseases such as equine leucoencephalomalacia and porcine pulmonary edema (Ross et al., 1990). It is known that fumonisins cause adverse effects in livestock and they have been correlated with increased incidences of esophageal cancer in humans in South Africa and some provinces of China (Diaz and Boermans, 1994). In a long-term study, Broomhead et al. (2002) fed 1- wk-old broiler chicks and turkey poults diets containing FB 1 at 25 or 50 mg/kg of diet, for 7 (broilers) or 14 (tur- Abbreviation Key: AFB 1 = aflatoxin B 1 ;FB 1 = fumonisin B
2 1954 OGIDO ET AL. keys) wk. They observed that 50 mg of FB 1 /kg of diet was detrimental to turkeys but was not toxic to broilers. The simultaneous feeding of 2 mycotoxins may cause enhanced toxicity (additive or synergistic toxicity), when compared with the toxicity of the individual mycotoxins (Kubena et al., 1995). For laying quail, the effects of FB 1 on performance and egg production are not known. Furthermore, there are no data available on the possible interaction effects of AFB 1 and FB 1 in young laying quail. In Brazil, the quail egg industry is concentrated in the Southeast Region, particularly in the state of São Paulo. Previous studies indicated that aflatoxins and fumonisins are frequently detected in corn and feedstuffs from this region (Sabino et al., 1989; Mallmann et al., 2001). The potential impact of low levels of these mycotoxins on quail performance and egg production parameters is not well understood. Therefore, the aim of the present work was to determine the effects of long-term exposure to AFB 1 and FB 1, singly or combined, in young laying quail that were fed rations containing low levels of the mycotoxins. MATERIALS AND METHODS Experimental Design and Quail Two hundred eighty-eight laying Japanese quail (Coturnix coturnix japonica) were purchased from a local commercial grower at 5 wk of age. Birds were placed in 3 batteries of 8 wire cages each (12 birds per cage) and allowed to consume feed and water ad libitum. Birds were allowed 3 wk to adapt to the cages, and during this period, they were fed a conventional corn and soybean meal basal diet, formulated to meet all the nutritional requirements of laying quail according to specifications of the National Research Council (1994). After this period, quail were randomly assigned to 1 of 6 dietary treatment groups. Each treatment group consisted of 4 replicate pens, each containing 12 birds. Dietary treatments were 1) no mycotoxins (control), 2) 10 mg of FB 1,3)50µg of AFB 1,4)50µg of AFB 1 +10mgofFB 1, 5) 200 µg ofafb 1, and 6) 200 µg of AFB 1 +10mgofFB 1 /kg of feed. The study was conducted in the Aviculture Section of the University of São Paulo, in Pirassununga, State of São Paulo, Brazil. A lighting schedule began with 16 h of light at 35 d of age increasing 60 min per wk until 18 h of light was reached at 63 d of age. This schedule was maintained throughout the remainder of the study. The treatment rations were fed ad libitum for 140 d (five 28-d laying periods/cycles). All laying quail were individually weighed on the first day of each 28-d period, and monitored daily for signs of morbidity and mortality. All eggs were recorded, collected, and individually weighed daily. Feed consumption and feed use were determined weekly. 2 Marconi Equipamentos para Laboratórios, Piracicaba, SP, Brazil. Aflatoxin Production Aflatoxin B 1 used in the experiment was produced in the Mycotoxins laboratory of the Biomedical Science Institute (University of São Paulo), using a toxigenic strain of Aspergillus flavus IMI-190 (International Mycology Institute, London), as described by Lin and Dianese (1976). Coconut agar cultures were extracted with chloroform (30 ml of chloroform per 10 g of culture) by shaking for 30 min. The contents were filtered through Whatman No.1 filter paper and evaporated to dryness. Quantification was achieved by densitometry according to Scott (1990). The chloroform solutions containing AFB 1 were evaporated in a waterbath at 60 C and subsequently resuspended in sterile corn oil (Almeida et al., 1996) previously tested for the presence of aflatoxins. Fumonisin Production Fumonisin B 1 used in the experiment was produced at the Veterinary Medical Diagnostic Laboratory, University of Missouri Columbia. Whole shelled corn (100 g) and 100 ml of distilled water were added to L jars, and autoclaved for 30 min at 121 C (Weibking et al., 1993). Fusarium verticillioides M-1325 was added to sterilized distilled water and 2 ml of the suspension was added to the autoclaved jars and shaken. After 24 h incubation at 27 C in the dark, the jars were shaken again to insure complete dispersal of the fungal mycelium. The jars were incubated in the dark for 5 wk at 27 C. Four hundred milliliters of a mixture of acetone:chloroform (75:25) was added directly to each 5-wk-old culture and allowed to stand overnight. The contents of each jar were blended in a blender for 30 s and then filtered. The solid culture residue was re-extracted, and allowed to dry overnight. The culture material was placed in a forced-air oven at 40 C for 48 h and then ground to a fine powder in a mill. The culture material was analyzed for FB 1,FB 2, and FB 3 by HPLC using the procedure of Wilson et al. (1990). Diet Preparation Aflatoxin B 1 test concentrations were obtained using sterile corn oil as the diluent, and appropriate amounts of these solutions were added to the basal diet to obtain the required levels of AFB 1. To guarantee a balanced diet for all treatments, AFB 1 /oil mixtures were substituted for corn oil (1% vol/wt) in the feeds. Concentrations of AFB 1 in final mixtures were confirmed by analyzing 1-kg samples following procedures proposed by Soares and Rodrigues-Amaya (1989). Fumonisin B 1 culture material was added directly to the feed. Final mixtures were homogenized in a horizontal/helicoidal mixer (Marconi). 2 The concentration of FB 1 in final mixtures was confirmed following procedures proposed by Shepard et al. (1990). Additionally, the basal diet was screened and found to be free of the following mycotoxins: aflatoxins, ochratoxin A, vomitoxin, and zearalenone (Rottinghaus et al., 1982). The assay detection limits
3 EFFECT OF AFLATOXIN B 1 AND FUMONISIN B1 ON LAYING QUAIL 1955 TABLE 1. Effect of aflatoxin B 1 (AFB 1 ) and fumonisin B 1 (FB 1 ) on feed consumption of laying Japanese quail 1 AFG 1 FB (µg/kg) (mg/kg) (g/bird per d) ± 0.71 ab ± 0.35 a ± 0.87 a ± 1.01 a ± 0.41 a ± 1.03 a ± 1.27 a ± 1.53 a ± 1.15 b ± 1.05 c ± 0.50 a ± 0.40 a ± 0.40 a ± 0.72 a ± 1.03 b ± 0.63 b ± 0.61 b ± 0.87 a ± 1.02 b ± 0.28 d ± 0.80 ab ± 0.73 a ± 0.57 a ± 0.94 b ± 0.64 d ± 1.16 a ± 1.49 a ± 1.29 a ± 0.74 b ± 0.42 d a d Means within a column with no common superscript differ statistically (P < 0.05). were 20 µg/kg, 50 µg/kg, 500 µg/g, and 500 µg/kg, respectively, for aflatoxins, ochratoxin A, vomitoxin, and zearalenone. Fumonisin B 1 was detected in the basal diet at 0.81µg/g of feed. Statistical Analysis Data (cage means) were subjected to ANOVA (Snedecor and Cochran, 1967) as a 2 3 factorial using the GLM procedure in the SAS software (SAS Institute, 1992). Variable means for treatments showing significant differences in the ANOVA were compared using Fisher s protected least significant difference procedure (Snedecor and Cochran, 1967). All statements of significance are based on the 0.05 level of probability. RESULTS AND DISCUSSION The results of feeding AFB 1 and FB 1 contaminated diets on feed consumption of laying quail over 5 28-d periods are presented in Table 1. Feed intake of quail fed AFB 1 alone did not differ from controls (P < 0.05) until the fourth cycle. The decrease in feed intake was higher in birds fed 200 µgofafb 1 /kg of feed compared with birds fed 50 µg ofafb 1 /kg, demonstrating the dose-dependent effect of AFB 1. Oliveira et al. (2002) observed decreased feed intake in laying quail fed 50 and 100 µgofafb 1 /kg for 168 d. By the end of the fourth and fifth cycles, birds fed 10 mg of FB 1 /kg of feed showed a decrease in feed consumption (P < 0.05). Broomhead et al. (2002) observed decreases in feed intake in turkeys fed50mgoffb 1 /kg of feed for 14 wk; however, a similar reduction was not observed in broilers fed 50 mg of FB 1 /kg for 7 wk. Although feed intake was reduced (P < 0.05) in birds fed the 50 µg of AFB 1 /kg + 10 mg of FB 1 /kg combination diet in the second cycle, feed intake returned to control levels for the third cycle, then decreased (P < 0.05) in the fourth and fifth cycles. In birds fed the 200 µg of AFB 1 +10mgofFB 1 /kg combination diet, feed intake was only reduced in the fourth and fifth cycles. In contrast, Weibking et al. (1994) did not observe a decrease in feed consumption by turkeys fed a combination of 75 mg of FB µg of AFB 1 /kgoffeedfor21d. Similar findings were reported by Kubena et al. (1995), who fed turkeys a combination of 200 mg of FB mg of AFB 1 /kg for 21 d. Difference among studies in length of exposure to the mycotoxins was undoubtedly a contributing factor in these contrasting results. In the present experiment, all mycotoxin treatments caused a decrease in feed intake by the end of the fifth cycle (P < 0.05). Birds fed the combination of 50 µg of AFB 1 +10mgofFB 1 /kg consumed less feed (P < 0.05) than birds fed only 10 mg of FB 1 /kg of diet or birds fed 50 µg of AFB 1 /kg of feed. However, feed intake was TABLE 2. Effect of aflatoxin B 1 (AFB 1 ) and fumonisin B 1 (FB 1 ) on feed utilization of laying Japanese quail 1 (µg/kg) (mg/kg) (g of feed/g of eggs) ± 0.04 a 2.53 ± 0.14 a 2.62 ± 0.08 a 2.61 ± 0.06 a 2.69 ± 0.03 a ± 0.08 a 2.56 ± 0.17 a 2.64 ± 0.17 a 2.69 ± 0.08 a 2.80 ± 0.19 a ± 0.06 a 2.49 ± 0.06 a 2.56 ± 0.07 a 2.60 ± 0.08 a 2.67 ± 0.07 a ± 0.06 a 2.53 ± 0.08 a 2.66 ± 0.12 a 2.75 ± 0.20 a 2.67 ± 0.11 a ± 0.09 a 2.45 ± 0.04 a 2.59 ± 0.07 a 2.58 ± 0.16 a 2.65 ± 0.11 a ± 0.07 a 2.53 ± 0.09 a 2.62 ± 0.07 a 2.59 ± 0.08 a 2.65 ± 0.05 a a Means within a column with no common superscript differ statistically (P < 0.05).
4 1956 OGIDO ET AL. TABLE 3. Effect of aflatoxin B 1 (AFB 1 ) and fumonisin B 1 (FB 1 ) on egg production of laying Japanese quail 1 (µg/kg) (mg/kg) (%) ± 3.68 a ± 5.81 a ± 1.27 a ± 1.16 a ± 3.06 a ± 2.01 a ± 4.33 a ± 5.72 b ± 3.21 b ± 3.21 b ± 1.06 a ± 2.15 a ± 2.14 a ± 4.66 a ± 4.15 a ± 3.19 a ± 6.06 a ± 4.30 b ± 6.47 b ± 2.49 b ± 3.76 a ± 1.25 a ± 1.66 a ± 4.01 a ± 3.88 a ± 0.92 a ± 1.60 a ± 1.59 ab ± 1.52 a ± 1.31 a a,b Means within a column with no common superscript differ statistically (P < 0.05). not decreased further by increasing the AFB 1 concentration in the combination diet to 200 µg/kg. Feed conversion values, summarized in Table 2, were not affected by any treatment (P > 0.05). This is consistent with a report by Oliveira et al. (2002), who fed AFB 1 to laying quail at levels up to 100 µg/kg for 168 d. Based on a report by Sawhney et al. (1973), it appears that feed conversion is only adversely affected when quail are exposed to much higher concentrations of AFB 1 (2 to 6 mg/kg of AFB 1 -equivalent for 6 wk). Table 3 presents egg production of laying quail during the 5 28-d periods. Birds fed 10 mg of FB 1 alone or in combination with 50 µg ofafb 1 /kg of diet showed a decrease in egg production (P < 0.05) by the end of the third cycle, and this decrease became more pronounced in the fourth and fifth periods. There are no published data on the effects of FB 1 in laying quail. However, in a study conducted by Kubena et al. (1999), laying hens fed 100 mg of FB 1 /kg of feed for 420 d showed a decrease in egg production starting in the ninth period; birds fed 200mgofFB 1 /kg showed this decrease starting in the first period. Egg production was not affected by AFB 1 (P > 0.05), which is in agreement with a report by Oliveira et al. (2002), who did not observe any effect on egg production of laying quail fed 25, 50, or 100 µgofafb 1 / kg for 168 d. Interestingly, egg production of birds fed the 200 µg ofafb 1 +10mgofFB 1 /kg combination diet was not different from controls, suggesting that the addition of AFB 1 at that level to diets containing FB 1 ameliorated the negative effect of FB 1 on egg production. The results of feeding AFB 1 and FB 1 contaminated diets on quail egg weight are presented in Table 4. Egg weight was not affected by FB 1 or AFB 1 until the fifth cycle when both toxins individually decreased (P < 0.05) egg weight. Although egg weight was reduced (P < 0.05) in birds fed the 50 µg ofafb 1 +10mgFB 1 /kg combination in the first cycle, egg weight returned to control levels for the second, third, and fourth cycles, then again decreased (P < 0.05) in the fifth cycle. All AFB 1 and FB 1 single or combination treatments resulted in decreased egg weights (P < 0.05) by the end of the fifth period. However, with the exception of the 200 µg/ kg AFB 1 treatment, the reduction in egg weight was much greater in birds fed the combination treatments. Oliveira et al. (2002) observed decreased egg weight in laying quail fed 50 or 100 µg ofafb 1 /kg for 168 d. The effects of dietary treatments on BW are summarized in Table 5. For the first 4 cycles, BW was not affected (P < 0.05) by any of the dietary treatments. However, in cycle 5, BW was decreased (P < 0.05) by all dietary treatments except for the group fed 50 µg of AFB 1 /kg of feed. The lack of effect of this treatment is consistent with a previous report by Oliveira et al. (2002), who observed no decrease in weight gain in laying quail fed 25, 50, or 100 µg of AFB 1 /kg for 168 d. Johri et al. (1990), Doerr and Ottinger (1980), and Chang TABLE 4. Effect of aflatoxin B 1 (AFB 1 ) and fumonisin B 1 (FB 1 ) on egg weight of laying Japanese quail 1 (µg/kg) (mg/kg) (g) ± 0.11 a ± 0.16 a ± 0.19 a ± 0.13 a ± 0.08 a ± 0.33 a ± 0.33 a ± 0.33 a ± 0.46 a ± 0.06 b ± 0.05 a ± 0.13 a ± 0.12 a ± 0.16 a ± 0.04 b ± 0.13 b ± 0.24 a ± 0.22 a ± 0.28 a ± 0.14 c ± 0.17 ab ± 0.21 a ± 0.18 a ± 0.24 a ± 0.10 c ± 0.14 a ± 0.24 a ± 0.29 a ± 0.24 a ± 0.21 c a c Means within a column with no common superscript differ statistically (P < 0.05).
5 EFFECT OF AFLATOXIN B 1 AND FUMONISIN B1 ON LAYING QUAIL 1957 TABLE 5. Effect of aflatoxin B 1 (AFB 1 ) and fumonisin B 1 (FB 1 ) on BW of laying Japanese quail 1 (µg/kg) (mg/kg) (g) ± 4.75 a ± 4.34 a ± 6.92 a ± 8.49 a ± 6.27 a ± 5.64 a ± 6.66 a ± 6.65 a ± 5.83 a ± 4.91 b ± 3.54 a ± 3.01 a ± 3.63 a ± 5.13 a ± 3.32 ab ± 2.02 a ± 2.16 a ± 4.82 a ± 2.85 a ± 6.08 c ± 2.46 a ± 6.51 a ± 6.82 a ± 4.03 a ± 5.51 c ± 7.36 a ± 5.22 a ± 4.57 a ± 6.44 a ± 8.31 c a c Means within a column with no common superscript differ statistically (P < 0.05). and Hamilton (1982) observed reductions in BW of laying quail fed aflatoxin concentrations ranging from 500 to 10,000 µg/kg for 28 to 100 d. Results of the current study indicate that levels as low as 200 µg ofafb 1 / kg of feed can reduce BW of laying quail fed dietary treatments for 140 d. There are no published data available on the effects of FB 1 in laying quail. In the present study, diets containing AFB 1 at levels of 50 and 200 µg/kg of feed, and FB 1 at a level of 10 mg of FB 1 /kg of feed, singly or combined, did not significantly affect feed conversion. However, long-term feeding of AFB 1 and FB 1, individually or in combination, decreased feed intake, egg weight, and BW. Egg production was affected only by FB 1, singly or combined with AFB 1.In surveys carried out in the southern and southeastern states of Brazil, aflatoxins have been reported in feedstuffs, such as corn, at average levels of 79 and 35 µg/ kg, respectively (Sabino et al., 1989). Mallmann et al. (2001) reported concentrations of FB 1 ranging from to µg/g, in cereals and feed of southern Brazil. The results of our experiment indicate that laying quail performance was adversely affected by levels of aflatoxin and fumonisin that can be found under natural conditions. This finding suggests that there is the potential for these mycotoxins to have a significant negative economic impact on the quail industry in Brazil. ACKNOWLEDGMENTS The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Brazil, grant no. 01/ , for financial support. REFERENCES Ah-Seo, J., and Y. Won-Lee Natural occurrence of the C series of fumonisin in mouldy corn. Appl. Environ. Microbiol. 65: Almeida, R. M. A., B. Corrêa, J. G. Xavier, M. A. B. Mallozzi, W. Gambale, and C. R. Paula Acute effect of aflatoxin B 1 on different inbred mouse strains II. Mycopathologia 133: Broomhead, J. N., D. R. Ledoux, A. J. Bermudez, and G. E. Rottinghaus Chronic effects of fumonisin B 1 in broilers and turkeys fed dietary treatments to market age. Poult. Sci. 81: Chang, C. F., and P. B. Hamilton Experimental aflatoxicosis in young Japanese quail. Poult. Sci. 61: Diaz, G. J., and H. J. Boermans Fumonisin toxicosis in domestic animals: A review. Vet. Hum. 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6 1958 OGIDO ET AL. Rottinghaus, G. E., B. Olsen, and G. D. Osweiler Rapid screening method for aflatoxin B 1, zearalenone, ochratoxin A, T-2 toxin, diacetoxyscirpenol and vomitoxin. Pages in Proceedings of the 25th Animal American Association of Veterinary Laboratory Diagnosticians. Nashville, TN. SAS Institute SAS User s Guide: Statistics. SAS Institute Inc., Cary, NC. Sawhney, D. S., D. V. Vadehra, and R. C. Baker Aflatoxicosis in the laying Japanese quail (Coturnix coturnix japonica). Poult. Sci. 52: Sabino, M., G. Prado, E. I. Inomata, M. O. Pedroso, and R. V. Garcia Natural occurrence of aflatoxins in maize in Brasil. Part II. Food Addit. Contam. 6: Scott, P. M Natural poisons. Pages in Official Methods of Analysis of the Association of Official Analytical Chemists. 15th ed. K. Helrich, ed. Association of Official Analytical Chemists, Gaithersburg, MD. Shepard, G. S., E. W. Sydenham, P. G. Thiel, and W. G. A. Gelderblom Quantitative determination of fumonisins B 1 and B2 by high-performance liquid chromatography with fluorescence detection. J. Liquid Chromatogr. 13: Snedecor, G. W., and W. G. Cochran Statistical Methods. 6th ed. Iowa State Univ. Press, Ames, IA. Soares, L. M. V., and D. B. Rodrigues-Amaya Survey of aflatoxins, ochratoxin A, zearalenone, and sterigmatocystin in some Brazilian foods by using multitoxin thin layer chromatographic method. J. AOAC Int. 72: Weibking, T. S., D. R. Ledoux, A. J. Bermudez, and G. E. Rottinghaus Individual and combined effects of feeding Fusarium moniliforme culture material, containing known levels of fumonisin B 1 and aflatoxin B 1 in the young turkey poult. Poult. Sci. 73: Weibking, T. S., D. R. Ledoux, A. J. Bermudez, J. R. Turk, and G. E. Rottinghaus Effects of feeding Fusarium moniliforme culture material, containing known levels of fumonisin B 1, on the young broiler chick. Poult. Sci. 72: Wilson, T. M., P. F. Ross, L. G. Rice, G. D. Osweiler, H. A. Nelson, D. L. Owens, R. D. Plattner, C. Reggiardo, T. H. Noon, and J. W. Pickrell Fumonisin B 1 levels associated with an epizootic of equine leukoencephalomalacia. J. Vet. Diagn. Invest. 2:
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