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Poult Sci 2007. 86:1149-1154
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METABOLISM AND NUTRITION

Effects of Fermented Soybean Meal on Digestive Enzyme Activities and Intestinal Morphology in Broilers

J. Feng1, X. Liu, Z. R. Xu, Y. Z. Wang and J. X. Liu

Animal Science College, Zhejiang University, The Key Laboratory of Molecular Animal Nutrition, Ministry of Education, HangZhou, 310029, China

1 Corresponding author: fengj{at}zju.edu.cn


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
The experiment was performed to compare the effects of fermented soybean meal (fermented with Aspergillus oryzae 3.042, FSBM) and soybean meal on digestive enzyme activities and intestinal morphology in broilers. Three hundred twenty 1-d-old Ross x Ross male broiler chicks were randomly allocated into 2 dietary treatments for a 6-wk feeding trial, including 0- to 21-d and 21- to 42-d periods. At the end of each stage, 8 broilers of each treatment were killed, and pancreas, small intestine digesta, and duodenum, jejunum, and ileum segments were collected for digestive enzymes and intestinal morphology evaluation. Results of the experiment showed that replacing soybean meal with FSBM in diet increased the activities of trypsin, lipase, and protease significantly in intestinal content of starter broilers (P < 0.05) and enhanced the protease activity of grower broilers (P < 0.05). Amylase activity was not affected in both feeding periods by the treatments. Compared with the control, broilers fed with FSBM had lower pancreatic trypsin activity (P < 0.05) in the starter phase. There were no significant differences on lipase, amylase, and protease activity between the treatments in both growth phases. Increased villus height (P < 0.05) and decreased crypt depth (P < 0.05) of jejunum mucosa could be observed in the whole growth stage of broilers fed with FSBM. Also, duodenal villus height of starter chicks was also significantly increased (P < 0.05).

Key Words: fermentation • soybean meal • digestive enzyme • intestinal morphology • broiler


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Soybean meal (SBM) is an important source of dietary protein in the poultry and swine industry. The presence of antinutritional factors (ANF) contained in soybeans has been recognized as the key factor that affects the nutritional value of SBM and other soy products (Dunsford et al., 1989; Batal and Parsons, 2003). Although the desolventization-toasting process reduces antinutrients in raw beans to low levels, the residual ANF, such as trypsin inhibitor (TI), lectins, and soya globulins, etc., could still interfere with digestion, absorption, and utilization of nutrients in the diet (Jiang et al., 2000; Fasina et al., 2004) and therefore limit the wide application of SBM in diets, especially for young animals (Li et al., 1990; Jiang et al., 2000).

Fermentation processes have been used to prepare traditional soybean foods, and these fermented soy foods are highly digestible and nutritious (Lee, 1998; Kim et al., 1999; Matsuo, 2006). Fermentation with Aspergillus oryzae, a fungus widely used in soy food preparation, could decrease TI and enhance the content of small-size peptide in soybean and SBM (Hong et al., 2004; Feng et al., 2007). Chah et al. (1975) showed that diets containing full-fat soybeans fermented by certain cultures of Aspergillus significantly improved broiler growth and feed utilization. Fermentation of SBM with Aspergillus increased weight gain and reduced phosphorus excretion in chicks (Hirabayashi et al., 1998a) and enhanced the availabilities of zinc and iron in rats (Hirabayashi et al., 1998b). Our previous study showed that chicks fed a diet with fermented soybean meal (FSBM) had greater average daily gain and average daily feed intake than chicks fed with SBM in the starter and grower phase (Feng et al., 2007). An in vitro study indicated that fermentation of soybean resulted an increase in nutrient solubility and digestibility (Kiers et al., 2003).

Nevertheless, data on the effect of FSBM on digestive function in poultry is scarce. Therefore, this experiment was conducted to evaluate the effects of SBM fermented with Aspergillus oryzae on digestive enzyme activity and intestinal mucosa morphology in broilers.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Preparation of Fermented Soybean Meal

The method of the fermentation of SBM was described previously (Feng et al., 2007). Dried soybean meals were soaked with distilled water for 60 min and then cooked in a steam tank at 60 to 70°C for 1 h. Cooked soybean meals were cooled to room temperature and inoculated with 0.3% Aspergillus oryzae 3.042 (±104 counts/g of SBM, provided by Microbial Institute of Zhejiang Province), mixed, and fermented in a bed-packed incubator for 48 h. Fresh fermented samples were dried in a hot-air oven at 80°C for 3 d. The dried samples were ground in a Fitz Mill and kept at room temperature until mixed in the diets.

Experimental Design and Diets

The experiment was carried out in accordance with the Chinese guidelines for animal welfare and approved by the animal welfare committee of Animal Science College, Zhejiang University. Three hundred twenty commercial Ross x Ross male broiler chicks were obtained from a commercial hatchery on day of hatch. Chicks were randomly allocated into the 2 dietary treatments with 4 replicates of 40 birds per group. The control birds were fed a corn-SBM based diet, and the treatment fed with a corn-FSBM based diet (Table 1Go). Two feeding phases were used, starter (0 to 21 d) and grower (21 to 42 d) phases. Nutrient levels of the diets (Table 1Go) met or exceeded NRC (1994) recommendations.


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  		Table 1. Composition of experiment diets for broilers1
 
The chicks were allowed free access to water and experimental diets. The initial room temperature for chicks was set at approximately 32°C and reduced by 2 to 3°C weekly until reaching 22°C at wk 4, which was maintained for the remaining 2 wk.

Sample Collection and Enzyme Analysis

Sampling Procedure. At 0800 h on d 21 and 42, 16 chicks (8 per treatment) were killed by cervical dislocation. The birds were immediately eviscerated for collection of pancreas and intestinal digesta. The pancreas sampling procedure was conducted according to the method described by Uni et al. (1999). The pancreas was homogenized in ice-cold 0.2 M Tris-HCl buffer, pH 8.0, containing 0.05 M NaCl in the ratio 1:4 (wt/vol). The homogenate was centrifuged at 3,000 x g for 15 min at 4°C, and the supernatant was stored for enzyme assays.

The following procedures were conducted using the method of Jin et al. (2000). Digesta from the small intestine was collected from the segment from the distal end of the duodenum to the ileo-cecal junction. A homogeneous intestinal digesta sample was collected by massaging the tract from both ends. And then immediately the small intestinal digesta samples were diluted 10-fold, based on the sample weight, with ice-cold PBS (pH 7.0), homogenized for 1 min, and sonicated for 1 min with 3 cycles at 30-s intervals. The samples were then centrifuged at 18,000 x g for 20 min at 4°C. The supernatants were divided into small portions and stored at –70°C for enzyme assays.

Digestive Enzyme Analysis. Assays for activity of trypsin (EC 3.4.4.4 [EC] ) were carried out as described by Engberg et al. (2004). Enterokinase was added to the homogenate and allowed to convert the trypsinogen into trypsin. Trypsin activity was then measured using benzoyl DL arginine p-nitroanilide as a substrate according to procedures described by Laine et al. (1993). One unit of enzyme activity was defined as the trypsin hydrolysis of 1 µmol of substrate in 1 min per mg of intestinal digesta protein or pancreas.

Amylase (EC 3.2.1.1 [EC] ) activity was determined using the method of Somogyi (1960). One unit of amylase activity was defined as the amount of amylase that caused formation of reducing power equivalent to 1 mg of glucose in 30 min at 38°C per mg of intestinal digesta protein or pancreas. The substrate used in the analysis was cornstarch.

Lipase (EC 3.1.1.3 [EC] ) activity was assayed using the method described by Tietz and Fiereck (1966). Lipase activity unit was equal to the volume (in mL) of 0.05 M NaOH required to neutralize the fatty acid liberated during a 6-h incubation with 3 mL of lipase substrate at 38°C per mg of intestinal digesta protein or pancreas. Olive oil was used as the substrate in this assay.

Protease activity was analyzed using the method of Lynn and Clevette-Radford (1984). The protease activity unit was defined as milligrams of azocasein degraded during 2 h incubation at 38°C per mg of intestinal digesta protein or pancreas. Azocasein was used as the substrate.

The intestinal digesta protein concentrations were determined by the method of Lowry et al. (1951). Ovine serum albumin was used as a standard.

Histomorphometry

Segments were removed from the duodenum, jejunum, and ileum as follows: 1) intestine from the gizzard to pancreatic and bile ducts was referred to as the duodenum, the middle section of which was taken for microscopy; 2) middle between the point of entry of the bile ducts and Meckel’s diverticulum (jejunum); and 3) 10 cm proximal to the ileo-cecal junction (ileum). The samples were flushed with physiological saline and fixed in 10% formalin. Three cross-sections for each sample were prepared after staining with hematoxylin and eosin using standard paraffin embedding procedures. Villus height was measured from the tip of the villus to the villus-crypt junction; crypt depth was defined as the depth of the invagination between adjacent villi. Morphological indices were measured using image processing and analysis system (Version 1, Leica Imaging System Ltd, Cambridge, UK).

Statistical Analysis

One-way ANOVA was performed using the GLM procedure of SAS software (SAS Institute, 1988). Pens were used as the experimental unit for all data. A significance level of P < 0.05 was used.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Digestive Enzyme Activities in Small Intestine and Pancreas

The digestive enzyme activities in the intestinal content and pancreas of chicks are shown in Tables 2Go and 3Go. Replacing SBM with FSBM in diet increased the activity of trypsin, lipase, and protease significantly in intestinal content of the starter broiler, and enhanced the protease activity of the grower broiler. However, amylase activity was not affected in both feeding periods by the treatments. Compared with the control, broilers fed with FSBM had lower pancreatic trypsin activity in the starter phase. There were no significant differences on lipase, amylase, and protease activity between the treatments in both growth phases.


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  		Table 2. Intestinal digestive enzyme activity of broiler fed with soybean meal (SBM) and fermented soybean meal (FSBM; U/mg of digesta protein)
 

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  		Table 3. Effect of fermented soybean meal (FSBM) on digestive enzyme activity of pancreas in broilers (U/mg of pancreas)
 
It is well known that ANF in SBM could impair digestion and increase endogenous protein excretion (Liener, 1989). Trypsin inhibitors and lectin have been implicated in reducing protein digestibility and in pancreatic hypertrophy (Liener, 1981). The ingestion of diets containing raw soybean or TI by chicks, rats, and mice caused a marked reduction in the total proteolytic activity in the small intestine (Gertler et al., 1967; Roy and Schneeman, 1981). In this study, increased intestinal protease and trypsin is in accordance with our previous study that broilers fed with FSBM had lower urea nitrogen excretion, and the reason may be that broilers fed fermented soybeans utilized dietary nitrogen more efficiently than broilers fed SBM (Chah et al., 1975). Lower urea nitrogen excretion and the improvement of enzyme activities in small intestinal contents of broilers may be mostly due to the inactivation of TI in FSBM. Fermentation may decrease or eliminate antinutritional constituents (Mital and Garg, 1990; Hachmeister and Fung, 1993). Hong et al. (2004) found fermentation with Aspergillus oryzae could decrease TI in soybean and soybean meal. Our previous study also proved that TI could be eliminated (2.63 mg/g vs. 0.00 mg/g) effectively by fermentation, and the FSBM applied in present study is same as the previous study (Feng et al., 2007).

Moreover, the increase in trypsin activities in pancreas of starter broiler was observed when with SBM, which could also reflect the presence of TI in the SBM diets. It was reported that fed on raw soybean flour elevated proteolytic activity in the pancreas of chicks and rats compared with heated soybean flour (Gertler and Nitsan, 1970; Konijn et al., 1970; Khalifa et al., 1994). It has been reported that TI induce a nonspecific increase of pancreatic enzyme synthesis by hormonal negative feedback (Mital and Garg, 1990; Batal and Parsons, 2003). The study did not find the significant changes on lipase and amylase activity in pancreas as well as other studies with raw soybean, this probably due to more ANF content in raw soybean.

Recent study suggested that depression of digestive enzyme activities was not only due to TI but other ANF (Escaffre et al., 1997). It was suggested that antigenic proteins (11S glycinin and 7S ß-conglycinin, 2 major antigenic materials in soybean proteins) in soybeans could impair the capacity to digest and absorb nutrients (Li et al., 1990, 1991). Kiers et al. (2000) reported that more or less complete breakdown of 3 subunits from ß-conglycinin and both polypeptides from glycinin in soybean were observed after fermentation. Hong et al. (2004) showed that large-size peptides, such as antigenic proteins, could be hydrolyzed to small-size peptides. Therefore, the improvement of activities of intestinal enzymes in broilers fed with FSBM presented here may be associated with degradation of soybean globulin, and this needs further research.

Morphological Measurement of the Small Intestinal Mucosa

Morphological measurements of the small intestinal mucosa of chicks are presented in Table 4Go. Increased villus height and decreased crypt depth of jejunum mucosa could be observed in the whole growth stage of broilers fed with FSBM. Also, duodenal villus height of starter chicks was also significantly increased. There were no significant effects of FSBM on chick ileum mucosa morphology.


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  		Table 4. Effects of fermented soybean meal (FSBM) on the morphology of the intestinal mucosa at different sites in the small intestine of broilers
 
Previous studies showed that ANF in SBM, such as TI and soybean globulins, etc., have an adverse effect on the morphology and function of digestive tract in animals (Dunsford et al., 1989; Li et al., 1991). The improvement of intestinal morphology in current study may be mostly due to the elimination of TI and the degradation of large-size protein in SBM after fermentation. It is well known that TI interfered with the proper function of trypsin and chymotrypsin leading to abnormal intestinal morphology (Liener and Kakade, 1993). Zarkadas and Wiseman (2000) demonstrated a negative correlation between the TI level SBM and villus height in weaned piglets. Additionally, many studies have been suggested that the morphological changes observed in young animal are also due to transient hypersensitivity to antigenic components of soybean diet (Lalles et al., 1993; Hong et al., 2004). Antigenic materials in soybean proteins are associated with villus atrophy, increased crypt cell mitosis, and crypt hyperplasia, and thereby cause a malabsorption syndrome (Kenworthy and Allen, 1966; Miller et al., 1984a,b). Similarly, the improvement of intestinal morphology may be associated with the degradation of antigenic materials after fermentation. It was reported that fermentation could degrade large-size protein to small-size peptides (Kiers et al., 2000; Hong et al., 2004).

The current study also showed that FSBM is more beneficial to starter than grower broilers on digestive enzyme activity and intestinal morphology, which may be because younger birds are more susceptible to the effects of ANF in SBM (Perez-Maldonado et al., 2003). As mentioned previously, fermentation has multiple effects on the nutritional value of soybean and soybean products; the improvement of digestive enzyme activity and intestinal mucosa morphology on broilers in present study may be partially responsible for the growth and feed conversion promotion effect of FSBM on broilers and piglets, which were studied previously.

In conclusion, digestive enzyme activities and intestinal morphology of broilers fed FSBM, especially in the starter phase, were improved compared with SBM. This suggested that fermentation with A. oryzae could improve the nutritional value of SBM and thus decrease or overcome the negative effect of ANF in SBM on broilers.


   ACKNOWLEDGMENTS
 
This work was supported by Grant Agreement 2004CB117506, a Key Science Project "973" Award, from National Science and Technology Committee, and Grant Agreement 2004C22027, a Key Science Project Award, from Zhejiang province Science and Technology Committee, P.R. China.

Received for publication October 7, 2006. Accepted for publication February 4, 2007.


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