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Performance and Histological Responses of Internal Organs of Broiler Chickens Fed Raw, Dehulled, and Aqueous and Dry-Heated Kidney Bean Meals

I. A. Emiola^*,1,2, A. D. Ologhobo and R. M. Gous

^* Department of Animal Production and Health, Ladoke Akintola University of Technology, PMB 4000, Ogbomoso, Nigeria; Department of Animal Science, University of Ibadan, Nigeria; and Discipline of Animal and Poultry Science, University of KwaZulu-Natal, 3200 Scottsville, Pietermartzburg, South Africa

¹ Corresponding author: emiola{at}cc.umanitoba.ca or walemiola{at}yahoo.com

	ABSTRACT

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The objective of the present study was to investigate the effect of raw and differently processed [aqueous heating, dehulled, and dry heating (toasted)] kidney bean meals on the performance, weights, and histology of internal organs of broiler chicken. The feeding trial lasted for 56 d. Two hundred twenty-five 1-d-old broiler chicks (Anak strain) were used for the study. There were 5 treatment groups of 3 replicates with 15 birds per replicate. Raw and processed kidney bean meals were used to replace 50% protein supplied by soybean in the control diet. Data collected were used to evaluate feed intake, weight gain, and efficiency of feed utilization. The weights of liver, pancreas, kidney, heart, and lungs were also recorded and tissue samples of each collected for histological examination. Average daily food intake, average daily gain, and efficiency of feed utilization were influenced by the dietary treatments. Average daily food intake and average daily gain in birds fed the control diet and heat-treated kidney bean meals were similar and significantly (P < 0.05) higher than those fed raw or dehulled meals. Feed conversion ratio was significantly (P < 0.05) higher in birds fed raw or dehulled meals compared with those fed the control diet. The relative weight of the pancreas was significantly (P < 0.05) increased as a result of acinar hypertrophy. The kidney had severe congestion of glomeruli and distention of the capillary vessels with numerous thrombi in birds fed raw and dehulled kidney bean meals. The weight of the liver was significantly (P < 0.05) reduced in birds fed raw and dehulled meals, and the liver was characterized by marked coagulative necrosis and degeneration of the hepatocytes. The structural alterations were attributed to intake of trypsin inhibitors and haemagglutinins in the processed seeds. In conclusion, aqueous heated kidney bean meal can be used to replace 50% protein supplied by soybean meal in broiler starter and finisher diets without any adverse effect on the performance and the internal organs.

Key Words: kidney bean seed • processing • performance • organ weight • histology

	INTRODUCTION

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Kidney bean (Phaseolus vulgaris) is considered as a potential component of diets of pigs and poultry. Kidney bean contains high amounts of protein and energy, and amino acids content is similar to that of soybean except for a lower level of methionine (Laurena et al., 1991). The inclusion of a high amount of raw kidney bean (Phaseolus vulgaris) in diets has been reported to have a detrimental effect on the performance of chickens (Jaffe, 1980; Liener, 1989) and rats (Apata, 1990). This was attributed to the presence in the seeds of various biologically active compounds usually referred to as antinutritional factors/toxic substances. According to Liener (1989), kidney beans contain trypsin inhibitors, amylase inhibitors, haemagglutinins, tannin, phytic acid, and oxalates. These antinutritional factors negatively affect the nutritive value of the bean through direct and indirect reactions: they inhibit protein and carbohydrate digestibility; induce pathological changes in intestine and liver tissue, thus affecting metabolism; inhibit a number of enzymes; and bind nutrients, making them unavailable (Bressani, 1993). Inclusion of raw kidney beans in the diet of growing animals as the only source of plant protein almost invariably leads to a significant impairment in growth (Ologhobo et al., 1993) and other undesirable physiological and biochemical alterations (Aletor and Aladetimi, 1989). Ologhobo (1981) reported alterations in the quantitative composition of the plasma, liver, and urine of rats poisoned with seed haemagglutinins, which led to the conclusion that the toxic action of haemagglutinins affects metabolic processes in the liver.

An experiment with chicks has shown that haemagglutinins in legumes exert their deleterious antinutritional effects via reduced nutrient absorption following extensive structural and functional disruption of the intestinal microvilli (Grant, 1991). Liener and Kakade (1980) also reported that the presence of protease inhibitors in the raw legumes is in part responsible for the depression in the nutritional value of proteins, inhibition of growth, and stimulation of pancreatic hyperplasia and hypertrophy. Similarly, Ortiz et al. (1994) found histological lesions in the ileum and liver of chicks and rats fed diets high in tannins extracted from faba bean (Vicia faba) suggesting a loss of digestive capacity. Degeneration of the hepatocytes was observed in the liver. Ortiz et al. attributed this to the high tannin content of the diet, which was estimated at 16 g of dried tannin per kg of diet, well above practical feeding or dietary levels.

These effects limit the use of raw kidney bean although various processing techniques tend to reduce the antinutritional factor content of the seed. Several studies indicate that heat processing [e.g., aqueous and dry heating (toasting)] increases the digestible nutrients available to young nonruminant animals, especially young chicks, resulting in improved growth. The hulls of legumes consist of poorly digestible glumes that completely enclose the seed. Removal of this hull should therefore increase the concentration of digestible nutrient level for broilers comparable with that of soybean. However, many authors reported suboptimal performance when broilers are fed processed mucuna bean meals (Emenalom and Udedibie, 1998; Emiola et al., 2003). This was attributed to varying concentrations of residual trypsin inhibitor and haemagglutinins in the meals. Emphasis has been placed on the various ways of inactivating the antinutritional factors in the legume seed and the improvement of the nutritive value. However, little attention has been given to the evaluation of the effects of intake of residual antinutritional factors in processed legume seeds on performance characteristics, weights, and histology of internal organs of broiler chickens. This study was therefore designed to address this issue.

	MATERIALS AND METHODS

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Samples
Mature dry seeds of raw kidney bean were obtained from Fasola Farm Center, Oyo State, Nigeria. The kidney bean was subjected to one of the following processing methods:

Aqueous Heating.
Dry legume seeds were poured into boiling water (100°C) in a cooking pot and heated for 1 h. Cooked beans were air dried for 4 d after which they were oven dried at 85°C for 48 h.

Dehulling.
The dry seeds were soaked in cold water for between 18 to 24 h, and the outer seed coats were removed by hand. The seeds were sun dried for 4 d after which they were oven dried at 85°C for 48 h.

Dry Heating (Toasting).
This involved spreading the seeds thinly in a pan placed in an oven (120°C). It was stirred from time to time to maintain uniform heating. Dry heating was considered adequate when the beans changed from whitish to light brown and became crispy to touch. The process lasted between 25 to 30 min.

The raw and processed seeds were ground using a 2-mm screen and stored separately in a sealed Kilner jar until required for chemical analysis and incorporation into diets.

Chemical Analysis
Diets and raw and processed kidney bean meals were milled to pass through 1-mm screen prior to chemical analyses. Samples were analyzed for DM, GE, and CP. Raw and processed kidney beans were subjected to proximate analysis using the methods of AOAC (1990). Concentration of haemagglutinins was determined using the haemagglutination assay as described by Valdebouze et al. (1980). For measurement of trypsin inhibitor activity, kidney bean seeds were ground with a mortar and pestle, and 100 mg of the powder produced was further homogenized in 10 mL of 0.001 M HCl with an all-glass Potter Elvelijam tissue grinder. Further extraction and trypsin inhibitor activity analyses were carried out as described by Van Oort et al. (1989). Tannins content were determined by the methods described by Hoff and Singleton (1977). Phytate content in the raw and processed kidney bean samples was determined using the methods of Haug and Lantzsch (1983). Briefly, 10 mL of 0.2 N HCl was added to 100 mg of raw and processed kidney bean seed, and the mixture was shaken for 3 h at room temperature and then filtered. Distilled water (0.5 mL) and 2 mL of ferric solution were then added to 0.5 mL of filtrate. The mixture was boiled for 30 min, centrifuged at 2,400 x g, after which 1.5 mL of bipyridine solution was added to 1 mL of the supernatant. The absorbance of the mixture was read against distilled water at 519 nm with a Pharmacia Ultrospec 2000 spectrophotometer (Perkin-Elmer, Amersham Pharmacia Biotech, Piscataway, NJ). Oxalate was assayed by a gravimetric method described by Apata and Ologhobo (1989). All analyses were done in duplicate (Table 1).

Measurements
Feed intake was recorded daily, and BW was recorded weekly. Feed consumption, weight gain, and efficiency of feed utilization were used as measures of chick performance. The study lasted for 56 d. On d 56, 2 birds per replicate (6 birds/treatment) were randomly selected, fasted for about 18 h to empty their gastrointestinal tract, weighed individually, slaughtered, and eviscerated. The weight of the liver, pancreas, kidney, heart, and lungs was recorded. For histological analysis, tissue samples of each organ were taken, immersed in formalin (1%), fixed in Bouin’s solution for 24 h, and embedded in paraffin wax. Sections from each organ were made at a thickness of 5 µm with a microtome, stained with hematoxylin-eosin, and examined by light microscope.

Data Analysis
Data collected were analyzed as a completely randomized design using the GLM procedures of SAS (SAS Inst. Inc., Cary, NC). When a significant F-value for treatment means (P < 0.05) was observed in the ANOVA, treatment means were compared using Duncan’s multiple range test (Duncan, 1955).

	RESULTS

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Aqueous heating and toasting reduced the crude protein content of kidney beans, whereas dehulling enhanced it (Table 1). Raw kidney bean contained 81.70 trypsin inhibitor units/mg of protein and 39.00 haemagglutinin units/mg of protein (Table 1). Dehulling marginally reduced the contents of trypsin inhibitors and haemagglutinin in kidney bean and caused substantial reduction in tannin content. Aqueous heating inactivates trypsin inhibitors and haemagglutinin, whereas toasting left residual amounts of these antinutritional factors. Heat treatment was less effective in the detoxification of tannin, phytate, and oxalate.

The performance of the chicks was significantly affected by the dietary treatments (P < 0.05). Average daily gain (ADG; see Table 4) was significantly (P < 0.05) reduced in birds fed diets containing raw or dehulled kidney bean compared with those fed aqueous and dry heated kidney bean meal diet. The ADG in broilers fed the control diet and aqueous and dry heat-treated kidney bean meal were similar. Average daily feed intake (ADFI) was influenced (P < 0.05) by the processing methods (Table 4). Heat treatment resulted in an improvement in feed intake, whereas ADFI (P < 0.05) was depressed in birds fed diets containing raw or dehulled kidney bean meal. Feed conversion ratio was higher (P < 0.05) in groups fed raw and processed kidney bean meals than the control diet.

	DISCUSSION

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The result of proximate composition revealed that kidney bean is a good source of protein. Aqueous and dry heating (toasting) tended to reduce the CP content possibly due to leaching and vaporization of some nitrogenous compound during processing. The crude fiber content of the bean is low, which makes it ideal for poultry. Dehulling marginally reduced the contents of trypsin inhibitor and haemagglutinins in kidney bean and caused substantial reduction in tannin. This is in agreement with the findings of Marquardt et al. (1978). Aqueous heating inactivates trypsin inhibitor and haemagglutinins, whereas toasting left residual amounts of these antinutritional factors. Heat treatments were less effective in the detoxification of tannin, phytate, and oxalate. Toasting appeared to be partially effective in inactivating the haemagglutinins and trypsin inhibitors in the seeds. This result reaffirms the earlier observations of Babar et al. (1988).

The ADFI was significantly (P < 0.05) affected by the dietary treatments (see Table 4). The ADFI was depressed in birds fed raw and dehulled kidney bean meal. This finding is in agreement with the report of other authors (Udedibie and Carlini, 2000; Ologhobo et al., 2003). These authors reported a significant reduction in feed intake when broilers were fed diets containing raw or improperly processed legume seed meals. In contrast, Liener (1989) reported a nonsignificant differences in ADFI when raw kidney been meal was fed to broiler chickens. The present study was conducted over a period of 56 d compared with a 21-d feeding trial reported by the author. The duration of the experiment could be responsible for the observed differences.

In the present study, the replacement of soybean meal in the control diet with raw and dehulled kidney bean meals caused a significantly poorer growth of chicks as a result of the structural alterations in the pancreas, kidney, and liver. The most significant effect was the enlargement of the pancreas caused by the hypertrophy and hyperplasia of the cells. There is evidence that the ingestion of trypsin inhibitors from legumes result in the hypertrophy and hyperplasia of the pancreas (Liener, 1989; Ologhobo et al., 2003), an indication of dysfunction of the pancreas. Liener and Kakade (1980) reported that the presence of protease inhibitors in legumes are in part responsible for the depression in the nutritive values of proteins, inhibition of growth, and stimulation of pancreatic hypertrophy and hyperplasia. Trypsin inhibitors have been implicated in growth depression in broiler chicks (Liener and Hasdai, 1986).

Significant (P < 0.05) differences in ADG and efficiency of feed utilization were observed. The depressed ADG in birds fed raw and dehulled kidney bean diets could be attributed to higher intake of trypsin inhibitors in these diets. Our observations on the hypertrophy and hyperplasia of the pancreas in chicks consuming diets rich in trypsin inhibitors offer histological support to this finding. According to Lyman and Lepkovsky (1957), the growth depression caused by trypsin inhibitors might be the consequence of an endogenous loss of essential amino acids being secreted by a hyperactive pancreas. This could be a result of a combination of endogenous losses of essential amino acids, especially threonine, which are important components of trypsin and decreased proteolysis of dietary proteins. The pancreatic hypertrophy and hyperplasia according to Lyman and Lepkovsky (1957) divert the amino acids from the synthesis of body protein to the synthesis of these enzymes. This loss in sulphur-containing amino acids exacerbates an already critical situation with respect to legume seeds, which are inherently deficient in these amino acids. Similarly, haemagglutinins are known to exert deleterious effects via structural and functional disruptions of the intestinal microvilli resulting in reduced nutrient absorption. The improvement in growth recorded in the groups fed aqueous-heated and toasted kidney bean meals could be attributed to the inactivation or reduction in trypsin inhibitors and haemagglutinins in the meals. Previously Ortiz et al. (1994) found histological lesions in the ileum and liver suggesting a loss of digestive capacity when chicks and rats were fed dried tannin extract from faba bean (Vicia faba). In the liver, degeneration of the hepatocytes was observed. They attributed this to the high tannin content of the diet, which was estimated at 16 g of dried tannin per kg of diet.

Efficiency of feed utilization was significantly influenced (P < 0.05) by the dietary treatments. This is consistent with the observation of Zarkadas and Wiseman (2005) who reported a reduction in the efficiency of feed utilization when diets containing trypsin inhibitor was fed to monogastric animals. The improvement in efficiency of feed utilization by broilers fed aqueous heated and toasted kidney bean meal diets is consistent with the finding of Bressani and Sosa (1990). The presence of residual trypsin inhibitor and haemagglutinins in the toasted meal could account for the observed differences in the efficiency of feed utilization of birds fed toasted and aqueous heated meals.

The toxic effects of antinutritional factors in raw and processed kidney bean caused significant (P < 0.05) reductions in the relative weights of the liver in birds fed raw and dehulled kidney bean meals. Alteration in the quantitative compositions of liver of rats acutely poisoned with seed haemagglutinins were reported by King et al. (1980). Aletor and Fetuga (1988) also reported focal necrosis and fatty acid changes in livers of rats fed raw lima bean. Weights of the pancreas and kidney were affected by the dietary treatments (P < 0.05; Table 5). These observations corroborate previous findings of Roebuck (1986). The raw and dehulled kidney bean meals caused an increased pancreatic weight; this implicates trypsin inhibitors as the key factors responsible for these physiological changes. Liddle et al. (1984) and Liener (1989) reported that inactivation of trypsin elicits continuous release of cholecystokinin, which stimulates pancreatic production of digestive enzymes including trypsin and chymotrypsin, which leads to an enlarged pancreas as a result of hypertrophy and hyperplasia.

The changes in the internal structure of organs and the associated intracellular components due to feeding raw and processed kidney bean indicates alterations in the metabolic and secretory functions of those organs (Table 6). The multifocal aggregations of lymphoid cells of liver, lymphatic infiltrations of the renal interstinum of kidney, and pancreatic necrosis are consistent with the pathological manifestations reported by Aletor and Fetuga (1988) and Ologhobo et al. (1993). The changes in the pancreatic acinar of birds fed raw and dehulled bean meals are in keeping with previous reports by Meyer et al. (1992), who observed decreased pancreatic enzyme activities in pigs fed diets containing kidney beans. The authors suggested that such effects are the consequences of poor protein digestibility and interference with systemic protein utilization, resulting in insufficient amino acids for protein synthesis. Similar alterations in the duodenum and pancreas have been reported in other studies with broilers fed different levels of faba bean and peas (Rubio et al., 1990; Yuste, 1993). The degeneration of the hepatocytes and coagulative necrosis in the liver and congestion of the glomerulus in the kidney were observed in birds fed raw and dehulled kidney bean meals and were less marked in birds fed toasted meal, whereas no changes were noticed in birds fed the aqueous heated meal. The absence of histological lesions in these birds could be attributed to the low concentrations of residual antinutritional factors in the toasted and aqueous heated kidney bean meal.

	ACKNOWLEDGMENTS

 
This project was funded by Nigerian Raw Material Development Council and Hope Agricultural Enterprises Limited, Ibadan, Nigeria.

	FOOTNOTES

 
² Present address: Department of Animal Science, University of Manitoba, Winnipeg, R3T 2N2, Manitoba, Canada.

Received for publication October 2, 2006. Accepted for publication February 20, 2007.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Emiola, I. A. Articles by Gous, R. M. Search for Related Content PubMed PubMed Citation Articles by Emiola, I. A. Articles by Gous, R. M.