Effects of Prolonged Administration of Aflatoxin B1 and Fumonisin B1 in Laying Japanese Quail R. Ogido,* C. A. F. Oliveira,†,1 D. R. Ledoux,‡ G. E. Rottinghaus,‡ B. Correˆa,§ P. Butkeraitis,* T. A. Reis,§ E. Gonc¸ales,# and R. Albuquerque* *Departamento de Nutric¸a˜o e Produc¸a˜o Animal, Faculdade de Medicina Veterina´ria e Zootecnia; †Departamento de Engenharia de Alimentos, Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de Sa˜o Paulo, Pirassununga, SP, 13630-000, Brazil; ‡Fusarium/Poultry Research Laboratory, University of Missouri, Columbia, Missouri 65211; §Departamento de Microbiologia, Instituto de Cieˆncias Biome´dicas, Universidade de Sa˜o Paulo, Sa˜o Paulo, Brazil; and #Centro de Pesquisa e Desenvolvimento de Sau´de Animal, Instituto Biolo´gico, Sa˜o Paulo, SP, 04014-002, Brazil ABSTRACT In the present study, 288 8-wk-old Japanese quail were randomly distributed into 6 experimental groups (48 birds per group) and fed the following diets for 140 d: 1) 0 (control); 2) 10 mg of fumonisin B1 (FB1); 3) 50 µg of aflatoxin B1 (AFB1); 4) 50 µg of AFB1 + 10 mg of FB1; 5) 200 µg of AFB1; and 6) 200 µg of AFB1 + 10 mg of FB1/kg of feed. Each treatment consisted of 4 replicates of 12 quail. Egg production and individual egg weight were checked daily. Feed intake and feed conversion were determined weekly. Results showed that by the end of the fifth cycle, average egg weight was lower (P < 0.05) in groups fed 10 mg of FB1/kg, 50 µg of AFB1/kg, 200
µg of AFB1/kg, and 10 mg of FB1 + 50 µg of AFB1/kg of feed. Egg production decreased (P < 0.05) in birds fed 10 mg of FB1/kg by the third, fourth, and fifth cycles. Feed intake was lower (P < 0.05) in birds fed 10 mg of FB1/kg by the fourth and fifth cycles, and in birds fed 50 and 200 µg of AFB1/kg in the fifth cycle. Birds fed 10 mg of FB1 + 50 µg of AFB1/kg consumed less feed (P < 0.05) in the first, second, and fifth cycles. Results indicated that prolonged administration of FB1 and AFB1, singly or in combination at the levels evaluated, may cause economic losses to quail egg producers.
(Key words: aflatoxin B1, fumonisin B1, quail, toxicity) 2004 Poultry Science 83:1953–1958
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 B1, B2, G1, and G2; with aflatoxin B1 (AFB1) 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, AFB1 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).
Oliveira et al. (2002) fed Japanese quail diets containing AFB1 at 25 to 100 µg/kg for 168 d and found that chronic exposure to AFB1 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 B1 (FB1) (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 1wk-old broiler chicks and turkey poults diets containing FB1 at 25 or 50 mg/kg of diet, for 7 (broilers) or 14 (tur-
2004 Poultry Science Association, Inc. Received for publication December 4, 2003. Accepted for publication August 3, 2004. 1 To whom correspondence should be addressed:
[email protected].
Abbreviation Key: AFB1 = aflatoxin B1; FB1 = fumonisin B1.
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keys) wk. They observed that 50 mg of FB1/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 FB1 on performance and egg production are not known. Furthermore, there are no data available on the possible interaction effects of AFB1 and FB1 in young laying quail. In Brazil, the quail egg industry is concentrated in the Southeast Region, particularly in the state of Sa˜o 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 AFB1 and FB1, 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 FB1, 3) 50 µg of AFB1, 4) 50 µg of AFB1 + 10 mg of FB1, 5) 200 µg of AFB1, and 6) 200 µg of AFB1 + 10 mg of FB1/kg of feed. The study was conducted in the Aviculture Section of the University of Sa˜o Paulo, in Pirassununga, State of Sa˜o 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 Laborato´rios, Piracicaba, SP, Brazil.
Aflatoxin Production Aflatoxin B1 used in the experiment was produced in the Mycotoxins laboratory of the Biomedical Science Institute (University of Sa˜o 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 AFB1 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 B1 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 0.946-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 FB1, FB2, and FB3 by HPLC using the procedure of Wilson et al. (1990).
Diet Preparation Aflatoxin B1 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 AFB1. To guarantee a balanced diet for all treatments, AFB1/oil mixtures were substituted for corn oil (1% vol/wt) in the feeds. Concentrations of AFB1 in final mixtures were confirmed by analyzing 1-kg samples following procedures proposed by Soares and Rodrigues-Amaya (1989). Fumonisin B1 culture material was added directly to the feed. Final mixtures were homogenized in a horizontal/helicoidal mixer (Marconi).2 The concentration of FB1 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
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EFFECT OF AFLATOXIN B1 AND FUMONISIN B1 ON LAYING QUAIL TABLE 1. Effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on feed consumption of laying Japanese quail1 Cycle2 AFG1 (µg/kg)
FB1
1
2
3
(mg/kg)
0 0 50 50 200 200
0 10 0 10 0 10
4
5
(g/bird per d) 25.06 25.25 26.14 24.58 25.01 25.74
± ± ± ± ± ±
0.71ab 1.03a 0.50a 0.63b 0.80ab 1.16a
26.83 27.04 27.57 25.57 26.59 26.85
± ± ± ± ± ±
0.35a 1.27a 0.40a 0.61b 0.73a 1.49a
28.56 27.81 28.80 27.49 28.21 27.97
± ± ± ± ± ±
0.87a 1.53a 0.40a 0.87a 0.57a 1.29a
27.44 26.57 27.81 26.30 26.51 26.22
± ± ± ± ± ±
1.01a 1.15b 0.72a 1.02b 0.94b 0.74b
29.03 26.98 28.27 24.40 25.37 25.27
± ± ± ± ± ±
0.41a 1.05c 1.03b 0.28d 0.64d 0.42d
Means within a column with no common superscript differ statistically (P < 0.05). Results are reported as means ± SD for 4 replicates of 12 quail each. 2 Laying periods of 28 d. a–d 1
were 20 µg/kg, 50 µg/kg, 500 µg/g, and 500 µg/kg, respectively, for aflatoxins, ochratoxin A, vomitoxin, and zearalenone. Fumonisin B1 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 AFB1 and FB1 contaminated diets on feed consumption of laying quail over 5 28-d periods are presented in Table 1. Feed intake of quail fed AFB1 alone did not differ from controls (P < 0.05) until the fourth cycle. The decrease in feed intake was higher in birds fed 200 µg of AFB1/kg of feed compared with birds fed 50 µg of AFB1/kg, demonstrating the dose-dependent effect of AFB1. Oliveira et al. (2002) observed decreased feed intake in laying quail fed 50 and 100 µg of AFB1/kg for 168 d. By the end of the fourth and
fifth cycles, birds fed 10 mg of FB1/kg of feed showed a decrease in feed consumption (P < 0.05). Broomhead et al. (2002) observed decreases in feed intake in turkeys fed 50 mg of FB1/kg of feed for 14 wk; however, a similar reduction was not observed in broilers fed 50 mg of FB1/kg for 7 wk. Although feed intake was reduced (P < 0.05) in birds fed the 50 µg of AFB1/kg + 10 mg of FB1/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 AFB1 + 10 mg of FB1/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 FB1 + 200 µg of AFB1/kg of feed for 21 d. Similar findings were reported by Kubena et al. (1995), who fed turkeys a combination of 200 mg of FB1 + 0.75 mg of AFB1/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 AFB1 + 10 mg of FB1/kg consumed less feed (P < 0.05) than birds fed only 10 mg of FB1/kg of diet or birds fed 50 µg of AFB1/kg of feed. However, feed intake was
TABLE 2. Effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on feed utilization of laying Japanese quail1 Cycle2 AFB1 (µg/kg) 0 0 50 50 200 200
FB1 (mg/kg) 0 10 0 10 0 10
1 2.34 2.37 2.34 2.33 2.33 2.35
± ± ± ± ± ±
2 0.04a 0.08a 0.06a 0.06a 0.09a 0.07a
2.53 2.56 2.49 2.53 2.45 2.53
± ± ± ± ± ±
3 0.14a 0.17a 0.06a 0.08a 0.04a 0.09a
(g of feed/g of eggs) 2.62 ± 0.08a 2.64 ± 0.17a 2.56 ± 0.07a 2.66 ± 0.12a 2.59 ± 0.07a 2.62 ± 0.07a
4 2.61 2.69 2.60 2.75 2.58 2.59
Means within a column with no common superscript differ statistically (P < 0.05). Results are reported as means ± SD for 4 replicates of 12 quail each. 2 Laying periods of 28 d. a 1
± ± ± ± ± ±
5 0.06a 0.08a 0.08a 0.20a 0.16a 0.08a
2.69 2.80 2.67 2.67 2.65 2.65
± ± ± ± ± ±
0.03a 0.19a 0.07a 0.11a 0.11a 0.05a
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OGIDO ET AL. TABLE 3. Effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on egg production of laying Japanese quail1 Cycle2 AFB1 (µg/kg) 0 0 50 50 200 200
FB1
1
2
3
(mg/kg) 0 10 0 10 0 10
4
5
(%) 93.30 93.30 96.50 93.97 95.46 95.98
± ± ± ± ± ±
3.68a 2.01a 1.06a 3.19a 3.76a 0.92a
93.35 93.25 95.93 91.76 96.43 94.74
± ± ± ± ± ±
5.81a 4.33a 2.15a 6.06a 1.25a 1.60a
93.23 91.22 95.60 90.45 94.21 92.63
± ± ± ± ± ±
1.27a 5.72b 2.14a 4.30b 1.66a 1.59ab
93.86 88.17 94.28 87.56 94.00 92.04
± ± ± ± ± ±
1.16a 3.21b 4.66a 6.47b 4.01a 1.52a
92.73 84.74 92.44 85.59 88.87 87.42
± ± ± ± ± ±
3.06a 3.21b 4.15a 2.49b 3.88a 1.31a
Means within a column with no common superscript differ statistically (P < 0.05). Results are reported as means ± SD for 4 replicates of 12 quail each. 2 Laying periods of 28 d. a,b 1
not decreased further by increasing the AFB1 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 AFB1 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 AFB1 (2 to 6 mg/kg of AFB1-equivalent for 6 wk). Table 3 presents egg production of laying quail during the 5 28-d periods. Birds fed 10 mg of FB1 alone or in combination with 50 µg of AFB1/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 FB1 in laying quail. However, in a study conducted by Kubena et al. (1999), laying hens fed 100 mg of FB1/kg of feed for 420 d showed a decrease in egg production starting in the ninth period; birds fed 200 mg of FB1/kg showed this decrease starting in the first period. Egg production was not affected by AFB1 (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 µg of AFB1/ kg for 168 d. Interestingly, egg production of birds fed the 200 µg of AFB1 + 10 mg of FB1/kg combination diet was not different from controls, suggesting that the
addition of AFB1 at that level to diets containing FB1 ameliorated the negative effect of FB1 on egg production. The results of feeding AFB1 and FB1 contaminated diets on quail egg weight are presented in Table 4. Egg weight was not affected by FB1 or AFB1 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 of AFB1 + 10 mg FB1/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 AFB1 and FB1 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 AFB1 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 of AFB1/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 AFB1/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 AFB1/kg for 168 d. Johri et al. (1990), Doerr and Ottinger (1980), and Chang
TABLE 4. Effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on egg weight of laying Japanese quail1 Cycle2 AFB1 (µg/kg) 0 0 50 50 200 200
FB1 (mg/kg) 0 10 0 10 0 10
1 11.43 11.42 11.55 11.20 11.23 11.38
± ± ± ± ± ±
2 0.11a 0.33a 0.05a 0.13b 0.17ab 0.14a
11.36 11.36 11.51 11.02 11.25 11.18
± ± ± ± ± ±
3 0.16a 0.33a 0.13a 0.24a 0.21a 0.24a
(g) 11.68 ± 11.55 ± 11.75 ± 11.41 ± 11.58 ± 11.51 ±
4 0.19a 0.33a 0.12a 0.22a 0.18a 0.29a
11.20 11.17 11.33 10.97 10.94 10.99
± ± ± ± ± ±
Means within a column with no common superscript differ statistically (P < 0.05). Results are reported as means ± SD for 4 replicates of 12 quail each. 2 Laying periods of 28 d. a–c 1
5 0.13a 0.46a 0.16a 0.28a 0.24a 0.24a
11.62 11.36 11.45 10.71 10.76 10.90
± ± ± ± ± ±
0.08a 0.06b 0.04b 0.14c 0.10c 0.21c
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EFFECT OF AFLATOXIN B1 AND FUMONISIN B1 ON LAYING QUAIL 1
TABLE 5. Effect of aflatoxin B1 (AFB1) and fumonisin B1 (FB1) on BW of laying Japanese quail Cycle2 AFB1
FB1
(µg/kg) 0 0 50 50 200 200
(mg/kg) 0 10 0 10 0 10
1 172.50 171.45 168.64 166.77 166.77 165.41
± ± ± ± ± ±
2 4.75a 5.64a 3.54a 2.02a 2.46a 7.36a
173.85 171.66 173.25 168.85 169.76 170.31
± ± ± ± ± ±
3 4.34a 6.66a 3.01a 2.16a 6.51a 5.22a
173.26 169.79 171.82 166.07 168.44 166.56
(g) ± ± ± ± ± ±
4 6.92a 6.65a 3.63a 4.82a 6.82a 4.57a
173.22 172.91 174.58 168.63 167.37 169.68
± ± ± ± ± ±
5 8.49a 5.83a 5.13a 2.85a 4.03a 6.44a
182.90 176.35 179.13 168.25 170.39 172.18
± ± ± ± ± ±
6.27a 4.91b 3.32ab 6.08c 5.51c 8.31c
Means within a column with no common superscript differ statistically (P < 0.05). Results are reported as means ± SD for 4 replicates of 12 quail each. 2 Laying periods of 28 d. a–c 1
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 of AFB1/ 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 FB1 in laying quail. In the present study, diets containing AFB1 at levels of 50 and 200 µg/kg of feed, and FB1 at a level of 10 mg of FB1/kg of feed, singly or combined, did not significantly affect feed conversion. However, long-term feeding of AFB1 and FB1, individually or in combination, decreased feed intake, egg weight, and BW. Egg production was affected only by FB1, singly or combined with AFB1. 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 FB1 ranging from 0.086 to 78.92 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 Fundac¸a˜o de Amparo a` Pesquisa do Estado de Sa˜o Paulo (FAPESP), Brazil, grant no. 01/04928-0, for financial support.
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