Effect of dietary fumonisin B1 on laying Japanese quail

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A 28-d experiment was conducted to evaluate the effects of fumonisin B1 (FB1) on egg ... of young laying Japanese quail fed on fumonisin-contaminated rations.

British Poultry Science Volume 45, Number 6 (December 2004), pp. 798–801

Effect of dietary fumonisin B1 on laying Japanese quail P. BUTKERAITIS, C.A.F. OLIVEIRA1, D.R. LEDOUX2, R. OGIDO, R. ALBUQUERQUE, J.F. ROSMANINHO1 AND G.E. ROTTINGHAUS3 Departamento de Nutric¸a˜o e Produc¸a˜o Animal, Faculdade de Medicina Veterina´ria e Zootecnia, Universidade de Sa˜o Paulo, Pirassununga, SP, 1Departamento de Engenharia de Alimentos, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de Sa˜o Paulo, Pirassununga, SP, Brazil, 2Department of Animal Science, University of Missouri, Columbia, Missouri and 3 Veterinary Medical Diagnostic Laboratory, College of Veterinary Medicine, University of Missouri, Columbia, Missouri, USA

Abstract 1. A 28-d experiment was conducted to evaluate the effects of fumonisin B1 (FB1) on egg production and egg quality of young laying Japanese quail fed on fumonisin-contaminated rations. 2. To this end, 128 7-week-old birds were randomly distributed into 4 experimental groups (32 birds per group) and given rations containing 0 (control), 10, 50 and 250 mg FB1/kg feed. Each treatment consisted of 4 replicates of 8 quail. Egg production and egg weight were checked daily. Feed consumption and feed conversion were determined weekly. Eggs laid on the last day of each 7-d period were collected and subjected to individual analysis for specific gravity, Haugh units and percentage eggshell. 3. Compared with controls, quail given  50 mg FB1/kg had reduced feed intake and lower body weight gain. Feed conversion was reduced only in birds given 250 mg FB1/kg. 4. Mean egg production and egg weight were lower in birds given 250 mg FB1/kg. Eggshell weight was reduced in birds given  50 mg FB1/kg. However, mean specific gravity, Haugh units and percentage eggshell were not affected by FB1. 5. No histopathological changes were observed in liver, kidney or heart samples from any treatment group. 6. The results indicated that exposure to FB1 at concentrations  50 mg/kg could adversely affect quail performance, emphasising the importance of controlling fumonisin contamination of quail rations.

INTRODUCTION Fusarium spp. are common soil fungi that have been found to contaminate grains that may be used in poultry diets (Kubena et al., 1999). Fusarium verticillioides (formerly F. moniliforme) is known to produce the fumonisin mycotoxins (Kubena et al., 1995). Sixteen different fumonisins have been isolated and identified, namely fumonisins B1 (FB1), B2, B3, B4, A1, A2, A3, AK1, C1, C3, C4, P1, P2, P3, PH1a, PH1b (Musser and Plattner, 1997; Ah-Seo and Won Lee, 1999). The predominant molecular form produced by F. verticillioides strains is FB1 (Norred, 1993). Fumonisins are polar compounds that are soluble in water, more soluble in acetonitrile—water or methanol and insoluble in organic solvents (Leeson et al., 1995).

Since their identification, fumonisins have been associated with animal diseases such as equine leucoencephalomalacia (ELEM) and porcine pulmonary edema (PPE) (Diaz and Boermans, 1994). Fumonisins have been associated with poor performance, increased organ weights and hepatic necrosis in broilers (Ledoux et al., 1992). In turkeys, FB1 causes reduced performance, increased organ weights, hepatocellular hyperplasia and myocardial alterations (Weibking et al., 1993b). For laying hens, the long-term administration of FB1 decreases egg production (Kubena et al., 1999). However, there is no available information on the toxicity of fumonisins in laying quail. Thus, the objective of this research was to investigate and describe the major effects of feeding young Japanese laying quail on diets containing known concentrations of FB1.

Correspondence to: Dr. C.A.F. Oliveira, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de Sa˜o Paulo, Av. Duque de Caxias Norte, 225, CEP 13630-000, Pirassununga, SP, Brazil. Tel: þ55-(19)-3565-4173. Fax: þ55-(19)-3565-4114. E-mail: [email protected] Accepted for publication 4 July 2004.

ISSN 0007–1668(print)/ISSN 1466–1799(online)/04/060798—4 ß 2004 British Poultry Science Ltd DOI: 10.1080/00071660400012766

FUMONISIN IN LAYING QUAIL

MATERIALS AND METHODS One hundred and twenty-eight laying Japanese quail (Coturnix coturnix japonica) were purchased from a local commercial grower at 5 weeks of age. Birds were placed in two batteries of 8 wire cages each (8 birds per cage) and were maintained on an 18 h light: 6 h dark schedule. They were allowed access to feed and water ad libitum. The basal diet was a commercial maize—soybean meal diet formulated to meet or exceed the nutritional requirements of laying quail as recommended by the National Research Council (NRC, 1994). Fumonisin was supplied by F. verticillioides M-1325 culture material, prepared by the Veterinary Medical Diagnostic Laboratory of the University of Missouri, USA. Procedures for the production of fumonisin have been reported previously (Weibking et al., 1993a). Dietary FB1 concentrations were confirmed by analysis prior to the start of the experiment. A completely randomised design was used with 4 pen replicates of 8 quails assigned to each of 4 dietary treatments for 4 weeks. Dietary treatments included: (1) basal (B) diet containing no fumonisin; (2) B þ 10 mg FB1/kg diet; (3) B þ 50 mg FB1/kg diet; and (4) B þ 250 mg FB1/kg diet. The study was conducted in the Aviculture Section of the University of Sa˜o Paulo. Treatment rations were fed ad libitum for 28 d. Egg production and egg weight were checked daily. Feed consumption and feed conversion were determined weekly. Mortality was recorded as it occurred, and all dead birds were necropsied. In addition, birds were inspected daily and any health-related problems were recorded. Dietary treatments were prepared by adding fumonisin culture material to a typical maize—soybean meal basal diet. The culture material had previously been analysed for FB1, FB2 and FB3 by the procedure of Murphy et al. (1993). Measurement was achieved by high performance liquid chromatography, which revealed concentrations of 6500 mg FB1/kg, 2100 mg FB2/kg and 680 mg FB3/kg. Recoveries ranged from 81 to 101% for FB1, 74 to 96% for FB2 and 75 to 96% for FB3. The detection limits were 0.25, 0.50 and 0.5 mg/kg for FB1, FB2 and FB3, respectively. Fumonisin culture material was added to the basal diet in appropriate amounts, so as to obtain the required concentrations of fumonisin. Final mixtures were homogenised in a horizontal/ helicoidal mixer (Marconi). The concentrations of FB1 in final mixtures were confirmed following procedures proposed by Shephard et al. (1990). Analysis of spiked samples containing concentrations of 0.1 to 10 mg/kg of FB1, FB2 and FB3 gave mean recoveries of 93.4, 91.2 and 87.2%, respectively. The detection limits were 20,

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30 and 30 mg/kg for FB1, FB2 and FB3, respectively, as defined by the minimum amount of toxin that could generate a chromatographic peak 5 times over the height:noise rate of the baseline. Additionally, the basal diet was screened and found to be free of the following mycotoxins: the aflatoxins, ochratoxin A, vomitoxin and zearalenone (Rottinghaus et al., 1982). The assay detection limits were 20, 50, 500 and 500 mg/kg, respectively, for aflatoxins, ochratoxin A, vomitoxin and zearalenone. Fumonisin B1 was detected in the basal diet at 0.81 mg/g feed. Eggs laid on the last day of each 7-d period were collected and subjected to individual analysis for specific gravity (Hamilton, 1982), albumen height and percentage eggshell. Albumen height data were transformed to Haugh units (Stadelman and Cotterill, 1986). Post-mortem examinations were performed on 5 quail from each treatment group. Liver, kidney and heart samples were fixed in 10% neutral buffered formalin. Fixed tissues were trimmed, embedded in paraffin, sectioned at 5 mm and stained with haematoxylin and eosin stain. Sample sections were used for microscopic histological evaluation (Thomson, 1990). Data were analysed by one-way analysis of variance using the General Linear Model procedures of SASÕ (SAS Institute, 1992). The means for treatments showing significant differences in the analysis of variance were compared using the Tukey test. Treatment degrees of freedom for FB1 level were partitioned to test linear or quadratic response (Steele and Torrie, 1981). Statistical significance was accepted at P < 0.05.

RESULTS AND DISCUSSION The effects of dietary FB1 on quail performance are presented in Table 1. The increase in FB1 concentration in the diet resulted in a linear (P < 0.05) decrease in feed intake and egg production, and in linear and quadratic (P < 0.05) effects on egg weight and body weight gain. Compared with controls, quail given 50 and 250 mg FB1/kg had reduced (P < 0.05) feed intake and lower (P < 0.05) body weight gain. However, feed conversion was only reduced (P < 0.05) in birds receiving 250 mg FB1/kg. Average egg production was significantly lower (P < 0.05) in the group given 250 mg FB1/kg. Egg weight was significantly decreased (P < 0.05) in birds given 50 and 250 mg FB1/kg. The mortality during the 28-d experimental period consisted of one quail in the 10 mg FB1/kg treatment and three quail in the 250 mg FB1/kg treatment. Wang et al. (1991) proposed a possible mechanism of action for the biological effects

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P. BUTKERAITIS ET AL.

Table 1. Effects of fumonisin B1 on laying quail performance1 FB1 (mg/kg) 0 10 50 250

Egg production (eggs/quail.d)3

Feed intake (g/bird.d)3

Feed conversion (g feed/g eggs)

Body weight gain2 (g)3,4

Egg weight (g)3,4

0.87  0.11a 0.87  0.11a 0.85  0.07a 0.44  0.15b

27.71  3.09a 28.14  2.87a 24.57  1.14b 20.00  2.12c

2.88  0.30a 3.03  0.42a 2.89  0.29a 4.86  1.17b

5.63  3.68a 0.29  3.01ab 3.75  0.88bc 7.78  5.84c

11.16  0.23a 10.82  0.38a 10.18  0.30b 9.44  0.60c

1

Data are means  standard deviation of 4 replicate pens of 8 quail each. Body weight gain between d 1 and 28 of intoxication period. 3 Linear effect (P < 0.05). 4 Quadratic effect (P < 0.05). a—c Values within columns with no common superscript differ significantly (P < 0.05). 2

Table 2. Effects of fumonisin B1 on quail egg quality1 FB1 (mg/kg) 0 10 50 250

Specific gravity (wt/vol)

Haugh unit2

Eggshell weight (g)2,3

Eggshell (%)

1.070  0.001a 1.069  0.002a 1.069  0.002a 1.070  0.004a

89.99  2.63a 88.12  2.49a 90.72  2.59a 90.74  2.83a

0.88  0.04a 0.85  0.04ab 0.78  0.02bc 0.73  0.64c

7.93  0.34a 7.92  0.25a 7.79  0.24a 7.85  0.64a

1

Data are means  standard deviation of 4 replicate pens of 8 quail each. Linear effect (P < 0.05). 3 Quadratic effect (P < 0.05). a—c Values within columns with no common superscript differ significantly (P < 0.05). 2

of fumonisins. They theorised that FB1 might interfere with the biosynthesis of sphingolipids or sphingosine turnover. Stevens and Tang (1997) reported that inhibition of folate uptake through FB1-induced depletion of sphingolipids could lead to an intracellular deficiency of this vitamin. In chicks, severe anaemia is one of the earliest signs of folate deficiency, and it is followed by reduced feed intake (Combs, 1998). It remains to be determined whether the reductions in feed intake observed in this study may have occurred as a result of FB1-induced folate deficiency. Table 2 presents the effects of dietary FB1 on egg quality. Average specific gravity was not affected by FB1. Increasing FB1 in the diet decreased Haugh units linearly (P < 0.05) and resulted in linear and quadratic (P < 0.05) decreases in eggshell weight. Thus, eggshell weight was reduced (P < 0.05) in birds fed 50 and 250 mg FB1/kg. However, percentage eggshell was not affected by FB1. This could be explained by the fact that egg weight was also reduced by fumonisin. Thinner eggshells were also observed in birds receiving  50 mg FB1/kg. Thinner eggshells will not only contribute to a larger number of broken eggs during collection but may also negatively affect interior egg quality. Compared with controls, no histopathological changes were observed in liver, kidney or heart samples from any treatment group. During the experimental period, eggshell de-pigmentation was observed which became more marked with increasing concentrations of FB1, thus suggesting a dose-dependent

relationship. Consequences of this decrease in eggshell pigmentation are difficult to assess at this time. Consumers may associate decreased pigmentation with poor bird health and hence lower quality eggs. Decreased pigmentation may also suggest decreased nutrient content of eggs with negative effects on fertility and hatchability of eggs used to produce laying quail. Either of these scenarios would undoubtedly have a negative impact on the quail industry. The results of this study indicate that  50 mg FB1/kg diet can negatively affect laying quail performance. There are no published data on the effects of FB1 in laying quail. However, with respect to the quail industry the question is whether such high levels of FB1 contamination can be expected in quail rations under industry conditions. Fumonisin B1 and B2 were detected in 97.4 and 94.8% of 48 maize samples from Brazil—39 from Parana and 9 from Mato Grosso (Hirooka et al., 1996). Orsi et al. (2000) reported concentrations of 9.72 mg FB1/kg and 7.67 mg FB2/kg in naturally contaminated maize samples from Sa˜o Paulo State, Brazil. Fumonisin was also detected in 32% of 407 samples, at dietary concentrations of 0.086 to 78.92 mg FB1/kg in food and feedstuffs from southern Brazil (Mallmann et al., 2001). These data suggest that it is possible that laying quail in Brazil could be exposed to levels of FB1 that would negatively affect the quail industry. In conclusion, quail performance was adversely affected in this trial by concentrations of FB1 ( 50 mg FB1/kg diet) that can be found under natural conditions. The no-observed-effect value was 10 mg FB1/kg. Therefore, on the

FUMONISIN IN LAYING QUAIL

basis of FB1 concentrations used in the experiment, it is not possible to predict the absence of adverse effects in the range between 10 and 50 mg FB1/kg. These results suggest that quail are sensitive to the toxic effects of FB1 at concentrations > 10 mg/kg and that there is a potential risk for significant economic impact on the quail industry, thus emphasising the importance of controlling FB1 contamination of quail rations.

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