Insoluble Fibers Affected the Performance, Carcass Characteristics and Serum Lipid of Broiler Chickens Fed Wheat-Based Diet

Document Type: Research Articles

Authors

Department of Animal Science, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

Abstract

The current study was conducted to survey the influences of addition of alfalfa meal (AM), rice bran (RB) and wood shaving (WS) in wheat-based diets [contain soluble non starch polysaccharides (NSP)] on performance carcass characteristic and serum lipids of broilers from 11 to 42 d of age. Seven hundreds 10-d-old male Ross 308 chicks were placed into 35 pens and allocated to seven wheat-soybean meal-based dietary treatments which were a control (CT) diet (without any fiber source) and six fiber-included diets consisting of three sources of fiber (AM, RB and WS) and two levels of fiber inclusion (3 and 6%) in a 3 × 2 factorial arrangement. According to the results, the average daily gain (ADG), average daily feed intake (ADFI), feed conversion ratio (FCR), corrected-FCR (C-FCR) and crop, proventriculus, gizzard (relative full weights) and heart, abdominal fat, liver, breast and thigh (relative weights) and serum low density lipoprotein (LDL) were affected by different types of fibers (P<0.05). The inclusion of insoluble fibers in wheat-based diet improved ADG and FCR in broilers, so that, the highest amount of ADG and the lowest amount of C-FCR was related to 3% WS contained diet (P<0.05). The highest amount of gizzard weight was depended to 6% WS contained diet (P<0.05) and the lowest breast and thigh weight were also related to RB diets (P<0.05), but the aforementioned treatments had no effect on the different intestine sections weight (P>0.05). In general, the inclusion of 3 to 6% insoluble fibers, except for 6% WS, in wheat-based diet improved growth performance in broiler chickens.

Keywords


INTRODUCTION

Wheat based diet is mainly used in some parts of the world such as Europe and Canada (Mahammadi Ghasem Abadi et al. 2014). Variations in nutritive values and nature of NSP of wheat result in inefficiencies in diet formulations, particularly in terms of energy and amino acid (Mahammadi Ghasem Abadi et al. 2014). NSPs as components of several poultry feed ingredients have been the interest of researches in recent years. These polysaccharides include a large variety of molecules that divided to main groups of soluble NSP (S-NSP) and insoluble NSP (I-NSP) (Shakouri et al. 2006). Some previous studies (Jiménez-Moreno et al. 2013; Taheri et al. 2016) showed that anti-nutritive effects of S-NSP on intestinal microflora, gut histomorphology, excreta moisture and performance. In fact, S-NSPs produce high digesta viscosity in intestine and inhibit digestion and absorption of nutrients such as lipids, protein and starch and decreased the performance (Hetland et al. 2004; Kalmendal et al. 2011). In contrast, most research conducted on poultry feeding, I-NSP has been considered a diluent of the diet (Rezaei et al. 2011). It has been demonstrated, based on research conducted in recent years, that the inclusion of moderate amounts of different fiber sources in the diet improves digestive organ development (Mateos et al. 2012) and increases HCl, bile acids and enzyme secretion (Molist et al. 2009; Svihus et al. 2004). These changes might result in improvements in nutrient digestibility (Rogel et al. 1987), growth performance (González-Alvarado et al. 2007; Taheri et al. 2016), increase in gizzard weight and gizzard contents and increase in apparent metabolizable energy corrected for nitrogen (AMEn) (Amerah et al. 2009; Jiménez-Moreno et al. 2009), gastrointestinal tract (GIT) health and eventually, animal welfare (Mateos et al. 2012). Consequently, the effects of dietary fiber (DF) on aforementioned factors will differ depending on the source and inclusion level of the fiber (Molist et al. 2009) as well as on the nature of the basal diet (Jiménez-Moreno et al. 2013). The alfalfa, wood shaving and rice bran are as good source of insoluble fiber, which can be used in poultry nutrition.  Alfalfa is widely used in animal feeding. It is moderately rich in protein, vitamins K, A and minerals but has low levels of energy (Mansoub and Pooryousef Myandoab, 2012). Dehydrated alfalfa meal generally is used at very low levels in poultry feeding, due primarily to its high fiber and low energy content (Jiang et al. 2012). The use of alfalfa in diets for monogastric animals is limited (Tkacova et al. 2011) by its high fiber content (above 7%). Alfalfa is well balanced in amino acids and rich in vitamins, carotenoids and saponins (Jiang et al. 2012). Carotenoids are polyenoicterpenoids having conjugated trans double bonds. They include carotenes (β-carotene and lycopene), which are polyene hydrocarbons, and xanthophylls (lutein, zeaxanthin, capsanthin, canthaxanthin, astaxanthin, and violaxanthin) having oxygen in different form (Tkacova et al. 2011). Mansoub and Pooryousef Myandoab (2012) reported that inclusion of alfalfa meal to the layer diets at the levels of 50, 100, 150 and 200 g/kg had no effect on feed intake (FI), but an addition of more than 5% decreased egg production (EP). Guclu et al. (2004) indicated that addition of 90 g/kg alfalfa meal into the laying quail diets had no adverse effect on performance and increased some of egg quality parameters. Wood is essentially composed of cellulose, hemicelluloses, lignin, and some extractives compounds. The close to significant effect of wood shavings on total bile salt content of gizzard chyme in all layers, as well as the positive effect of wood shavings on jejuna amylase activity (U/g feed) observed in birds fed on whole wheat diets, indicate that stimulation of digestive processes may occur also in older birds (Hetland et al. 2003). The rice bran is a powdery fine and fluffy material that consists seeds or kernels, in addition to particles of pericarp, seed coat, aleurone, germ and fine starchy endosperm. Rice bran is rich in B-vitamins and tocopherols and its nutrient density and profiles of amino acids and fatty acids, including 74% of unsaturated fatty acids, are superior to cereal grains (Adrizal and Ohtani, 2002). Both rice bran protein and fat are of relatively high biological value (Ersin Samli et al. 2006). The results of a study carried out with poultry using rice bran at 0, 5, 10, 15, 20 and 25% levels indicated that use of 25% of mixed rice bran in layer diets had no adverse effect on the productive performance (Ersin Samli et al. 2006). With regard to effects of dietary inclusion of insoluble fibers on growth performance and digestive traits of birds, the aim of this research was to study the influence of AM, RB and WS in the wheat-based diet on growth performance, carcass traits and serum lipids of broilers in the grower phase.

 

MATERIALS AND METHODS

Experimental design and handling

The present study was conducted from June to July of 2015, when the climate condition was relative hot and humid. A total of 700 commercial broiler chicks (10-d-old male, Ross 308 strain) were divided into 35 groups, which consisted of 5 replications of 20 birds each and fed to seven wheat-based diets treatments which were a control diet (without any fiber source) and six fiber-included diets consisting of three sources (AM, RB and WS) and two levels of fiber inclusion (3 and 6%) in a 3 × 2 factorial arrangement. They were arranged using a completely randomized design (CRD). The photoperiod was 23 h light: 1 h dark, throughout the experiment. The rearing room (1.5×1.5 m) was provided with fans and coolers to adjust the environmental temperature to 24 ± 1 ˚C and this temperature were almost stable for total of experiment. Prophylactic measures against the most common infectious diseases were conducted. The experimental starter diets contained 3098 to 3102 kcal ME and 2147 to 2152 % CP (not showed) and the grower diets (Table 1) were formulated to meet the requirements of broiler chickens according to recommendations of Aviagen for Ross 308broilers (Aviagen, 2014).

 

Chemical evaluation of diets

The diets were analyzed for nutrient concentrations according to the standard procedures of AOAC (2000). Fiber sources and diets were analyzed for S-NSP and I-NSP according to the procedure of Englyst et al. (1994).

 

Growth performance

After an adaptation period, the ADG, ADFI and FCR were determined by pen from 25 to 42 d of age. Data were corrected by subtracting the amount of added WS from the total feed consumption (Hetland et al. 2003) to obtain C-FCR.

 

Table 1 Ingredient composition, nutrient content and particle size distribution of the experimental diets (% as-fed basis, unless otherwise indicated) from 25 to 42 d of age

 

1 Provided the following per kilogram of diets: Manganese (MnSO4H2O): 75 mg; Zinc (ZnO): 85 mg; Iron (FeSO47H2O): 50 mg; Copper (CuSO45H2O): 10 mg; Selenium (Na2SeO3): 0.2 mg; Iodine (Iodized NaCl): 0.8 mg and Choline: 250 mg.

2 Provided the following per kilogram of diets: vitamin A: 9000 IU; Cholecalciferol: 2000 IU; vitamin E: 36 IU; vitamin B12: 0.015 mg; Menadione: 2 mg; Riboflavin: 6.6 mg; Thiamine: 1.8 mg; Pantothenic acid: 7.3 mg; Niacin: 30 mg; Folic acid: 1 mg; Biotin: 0.1 mg and Pyridoxine: 3 mg.

3 According to NRC (1994).

S-NSP: soluble non-starch polysaccharide and I-NSP: insoluble non-starch polysaccharide.

 

Before weighing, the chicks were fasted for six h to ensure a consistent gut fill among all birds (Shirzadegan et al. 2014).

 

Carcass characteristics

Subsequent to the weighing of broiler chickens at the end of the experiment (42 days), three birds were selected from each of the replicate groups per treatments. These birds were slaughtered by severing the bronchial vein to determine some measurements of carcass yield involve internal organs (crop, heart, proventriculus, liver, abdominal fat, gizzard, small intestine, caecum and colon) as full digestive tractand external organs (carcass, breast and thigh). The weights of these organs were expressed as percentages of live body weight (Shirzadegan et al. 2014).

 

Serum metabolites

At the 42nd days of the experiment, blood samples (three bird each replicate) from the brachial veins of all chickens were collected for analysis. After coagulation, the blood samples were centrifuged at 3000 rpm for 10 min and the obtained serum was stored in a freezer at -20 ˚C for further analysis. In the blood serum, the following parameters were determined: total cholesterol (TC), triglyceride (TG) and low-density lipoproteins (LDL) by spectrophotometric method using commercially available kits (Parsazmun, Iran) (Shirzadegan et al. 2014).

 

Statistical analysis

Data were analyzed as a completely randomized design with seven treatments (diets) using the GLM procedure of SAS (SAS, 2003). Differences among treatments were considered significant at (P<0.05). Significant differences between means (diets) were separated by Fisher’s Least Significant Difference test (protected t-test). In addition, the effects of fiber source (AM, RB and WS), inclusion level (3 and 6%) of fiber and the interaction between source and level of fiber were studied as a 2 × 3 factorial arrangement analysis.

 

RESULTS AND DISCUSSION

Growth performance

The effect of fiber source and level of fiber on ADFI, ADG, FCR and C-FCR are shown inTable 2. Birds fed the RB or theWS diets showed the higher ADFI (P<0.001) than those fed the CT diet, however, the3% AM diet decreased the ADFI compared to the CT diet and the ADFI was higher for birds fed the WS diet than for birds fed theRB diet. Birds fed the fiber-included diets showed the higher ADG (P<0.001) comparedto the CT diet. The ADG was higher (P<0.01) for birds fed the WS or the RB dietsthan for birds fed the AM diet. Feeding the fiber-included diets, except the 6% WS,improved (P<0.001) the FCR compared to the CT diet. The birds fed the AM diet showed the lowest FCR (P<0.001) compared to other fiber sources, and FCR was higher for birds fed the WS diet thanfor birds fed the RB diet. Birds fed the fiber-included diets showed the lower C-FCR (P<0.001) than those fed the CT diet. The C-FCR was higher (P<0.001) for birds fed the WSor the RB diets than for birds fed the AM diet. Totally, an increase in the inclusion level of fiber inthe diet increased the FCR and the C-FCR, but the effects were more pronounced for theWS diets than for the AM or the RB diets. Likewise, the interaction effect (P<0.001) was observed on growth performance traits (ADFI, ADG, FCR and C-FCR) between the fiber source and the inclusion level offiber.

 

Organs weight

Influences of dietary fibers on full digestive tract weight (Table 3) and other carcass characteristic (Table 4) of broiler chicks are presented in below. Results indicated that the effects of treatments on carcass traits were statistically significant at 42 days old (P<0.05). However, the crop, proventriculus, gizzard (full relative weights) and heart, abdominal fat, liver, breast and thigh (relative weights) were affected by different sources of fibers, so that, the highest amount of gizzard weight was depended to 6% WS contained diet (P<0.05) and the lowest abdominal fat weight was related to 6% AM group (P<0.05). The lowest breast and thigh weight were also related to RB diets (P<0.05), but the treatments had no significant effect on the carcass yield, small intestine, ceca and colon weights of birds (P>0.05).

 

Serum lipids

Results of effects of dietary fibers on serum metabolites of broilers are presented in Table 5. These findings indicate that different inclusion of dietary fibers did not significantly (P>0.05) effect on the blood TG and TC concentrations, but plasma LDL percentages were affected (P<0.05) by treatments. According to results, the highest serum LDL at 40 days old was observed in the chicks fed on ration 3% WS compared to control. Moreover, the LDL level of birds fed 6% WS was lower than 6% RB (P<0.05), whereas, the other fiber-included diets not had different to control group (P>0.05). According to the results, the decreased feed intake of the birds on the diets containing wheat compared to the fiber included diets probably is because of increasing the intestinal digesta viscosity that causes increase of feed retention time in the gastrointestinal tract (Rogel et al. 1987; Mateos et al. 2012). Since, there is a relationship between rate of feed passage through the gut and feed consumption in young chickens (Taheri et al. 2016), inclusion of this S-NSP in the diet leads to less feed intake. In the present study, it was found that the inclusion of wood shavings increased ADFI and decreased the FCR and C-FCR in chickens compared to other fiber sources. Similarly, Shakouri et al. (2006) found that diluting the diet with cellulose increased feed intake, whereas, Hetland et al. (2003) found that diluting a wheat-based diet with oat hulls had no influence on the weight gain and feed intake, but, in turkeys, diluting a maize-based diet with wood shavings was reported to improve the gain/feed during the critical first 7 d posthatch period (Jiang et al. 2012). Taheri et al. (2016) also showed the broiler chickens receiving 4 and 8 % wheat bran in a barley-based diet had lower FCR than those fed the barley-based diet. It has been suggested that the birds are able to maintain normal weight gain when fed diets diluted with insoluble fibre by the increased capacity of the digestive system and/or faster passage through the digestive tract (Hetland et al. 2004). Consequently, the higher feed intake in birds fed on diets diluted with fibers in the present study can probably be explained by the larger gizzard sizes observed and faster gut emptying (Kalmendal et al. 2011). A large, well-developed gizzard improves gut motility and may increase cholecystokinin release (Svihus et al. 2004), which in turn stimulates the secretion of pancreatic enzymes and gastro-duodenal refluxes, as a result, the growth performance could be better in birds.

 

Table 2 Effect of fiber source and level of fiber on growth performance of broilers from 25 to 42 d

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

ADFI: average daily feed intake; ADG: average daily gain; FCR: feed conversion ratio.

* C-FCR: corrected-FCR, data were corrected by subtracting the amount of added wood shavings from the total feed consumption (Hetland et al. 2003).

SEM: standard error of the mean.

 

Table 3 Effect of fiber source and level of fiber on the relative weight (% live BW) of full digestive tract of broilers at 42 d of age

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the mean.

 

The lower weight gain and higher FCR of the broilers fed control diet are also predictable due to less feed intake and less nutrients utilization because of high viscosity of the chime in birds (Shakouri et al. 2006), but chickens fed the coarse insoluble fiber (such as WS or RB diets) showed the higher ADFI than those fed the control diet, which it may be due an increase in the flow rate of feed in GIT. The results of this study was in agreement with results of Gonzalez-Alvarado et al. (2007) and Jiménez-Moreno et al. (2009) when oat hulls, rice hulls or sunflower hulls were included in low fiber diets for broilers and suggests that the beneficial effects of dietary fiber on feed/gain ratio and growth performance of broilers were due primarily to an increase in diet digestibility and well-developed gizzard which resulted in more nutrients available for growth. Furthermore, in conjunction to better FCR in birds fed RB and AM diets, Guclu et al. (2004) indicated that adding alfalfa meal into the laying quail diets (90 g/kg) had no adverse effect on performance and increased some of egg quality parameters. Tkacova et al. (2011) also reported that broilers fed diets with high doses of alfalfa (60 g/kg diet) had lower feed conversion. However, it was reported that inclusion of alfalfa in diets of laying hens reduced performance expressed in terms of body weight and egg mass (EM) (Jiang et al. 2012). However, results of Ersin Samli et al. (2006) experiment showed that rice bran could be included up to 10% without any adverse effect on laying performance, egg quality and digestive organs. The higher ADG and better FCR showed in experimental birds in present study may be due to mainly vitamins and essential nutrients found in rice bran. Results of this experiment also indicated that addition of I-NSP to diet affected some characteristics of gastrointestinal tract of broilers. In this way, there was a significant effect of NSP solubility on cecum weight, with pigs fed the S-NSP diet having heavier cecum than those on the I-NSP diets on both days 6 and 14 (Wellock et al. 2008). As well as, asserted the treatments containing an equal or higher ratio of cellulose resulted in increased intestine weight of broilers at 21 days of age. This finding is conflicting with other researchers who have shown that cellulose usage decreases intestine weight in younger broilers (Sklan, 2003). Notably, broilers adapt to high levels of insoluble fibers by enlarging the GIT (Gonzalez-Alvarado et al. 2010). As a result, their weights increase. The relative empty weights of jejunum, ileum and small intestine of broilers were also affected by dietary insoluble fiber (Amerah et al. 2009). This adaptation is a rapid attempt to increase the absorptive surface area of the GIT in response to the lower diffusion rates, and it occurs by increasing the digesta viscosity levels (Jiménez-Moreno et al. 2009; Mateos et al. 2012). However, the breast, thigh and intestinal sections in our study were not improved by administration of fiber in diet. Moreover, reported, abdominal fat decreased at 20% rice bran inclusion in the diet. Oladunjoye and Ojebiyi (2010) also noted that body fat content of chicken reduced when 40% oat hull was included in their diet. Gizzard weight and the length of small intestine, large intestine, duodenum and ileum were however increased significantly at 20% rice bran inclusion level. This can be attributed to high fiber in this diet. Similarly reported, access to coarse hulls (such as wood shaving) stimulated gizzard development (Mateos et al. 2012), which this is in agreement with previous studies to fiber source such as wood shaving (Amerah et al. 2009) and alfalfa (Jiang et al. 2012).

 

Table 4 Effect of fiber source and level of fiber on the relative weight (% live BW) of carcass, breast, thigh + drumstick, abdominal fat, heart and liver in broiler at 42 d of age

 

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the mean.

 

Table 5 Effect of fiber source and level of fiber on serum lipid parameters (mg/dL) in broiler at 40 days old

 

TG: triglyceride; TC: total cholesterol and LDL: low density lipoprotein.

The means within the same column with at least one common letter, do not have significant difference (P>0.05).

SEM: standard error of the mean.

 

The coarse hull particles are retained in the gizzard until they are ground to certain critical size that allows them to pass through the pyloric sphincter (Hetland et al. 2003). This leads to an increase in the volume of the organ’s contents and a muscular adaptation to meet the greater demand for grinding. Showed that the increase in grinding activity of the gizzard, increase in digestive secretions, HCL, bile acid and endogenous enzymes together with a better mixing of digestive juices with the digesta (González-Alvarado et al. 2007) affect the functioning of the GIT and may modify microbial growth at specific digestive organ sites, might explain the positive effects of I-NSP on the digestibility of dietary components (Rezaei et al. 2011; Mateos et al. 2012). This study, the highest proventriculus and gizzard weights and the better growth performance were observed in fiber included diets that it could be refer to aforementioned subject. The result of this study showed that inclusion of different I-NSP in diet significantly altered the blood metabolites of broilers in grower phase. In depending to this result, Sarikhan et al. (2009) reported that at starter period, blood lipids levels were significantly affected by levels of insoluble fibers in grower phase. In their research, serum TG levels were significantly lower in broilers fed diets containing 0.75% insoluble fibers and higher levels of high density lipoprotein (HDL) and lower concentrations of very low density lipoprotein (VLDL) observed in the serum of 0.50 and 0.75% insoluble fibers dietary groups. Taheri et al. (2016) was also showed the broilers receiving 12% wheat bran in a barley-based diet had lower TC than those fed the corn-based diet. In contrast to our study, it showed that the blood TC and TG concentration were significantly reduced in bird fed diets supplemented to alfalfa powder (Oladunjoye and Ojebiyi, 2010). The main reason of cholesterol and triglyceride reduction in serum of chicks may be due to substances like carvacrol and thymol (Mansoub and Pooryousef Myandoab, 2012) and high levels (2 to 3% dry matter) of saponins present in alfalfa, which have showed hypocholesterolemic, anticarcinogenic, anti-inflammatory, hypocholesterolemic and antioxidant activity (Jiang et al. 2012). Furthermore, indicated that rice bran insoluble fiber function as lower agent of TC and coronary artery disease. These effects are due to tocols (0.2%) of crude rice bran, which about 70 % are tocotrienols. Tocol possess potent antioxidant activity and decreases serum cholesterol and hepatic cholesterol synthesis by the suppression of hydroxyl methyl glytaryl coenzyme A reductase (Ju and Vali, 2005). However, addition of fiber to diets in our study increased plasma LDL (3% WS diet) and abdominal fat, which it may be because of increase in nutrient passage rate and little degradation of bile salts by gut microorganisms and higher cholesterol absorption in broilers intestine.

 

CONCLUSION

Generally, based on the results of growth performance, the inclusion of 3 or 6% insoluble fiber, except for 6% WS, in wheat-based diet improved the ADG, FCR and gizzard function in broilers simultaneously from 25 to 42 d of age. The beneficial effect of insoluble fiber inclusion in the diet may be related to some extent to the longer feed passage in the upper part of the gastrointestinal tract, faster feed passage rate in the distal part of the gastrointestinal tract and the increase of nutrient retention. However, more research is needed to determine all the roles of I-NSPs on broilers performance.

 

ACKNOWLEDGEMENT

The authors sincerely thank Department of Animal Science, Faculty of Agriculture, University of Zanjan for this project.

Adrizal O. and Ohtani S. (2002). Defatted rice bran non starch polysaccharides in broiler diets: effects of supplements on nutrient digestibilities. J. Poult. Sci. 39, 67-76.

Amerah A.M., Ravindran V. and Lentle R.G. (2009). Influence of insoluble fibre and whole wheat inclusion on the performance, digestive tract development and ileal microbiota profile of broiler chickens. Br. Poult. Sci. 50, 366-375.

AOAC. (2000). Official Methods of Analysis. Vol. I. 17th Ed. Association of Official Analytical Chemists, Arlington, VA, USA.

Aviagen. (2014). Ross 308: Broiler Nutrition Specification. Aviagen Ltd., Newbridge, UK.

Englyst H.N., Quigley M.E. and Geoffrey J.H. (1994). Determination of dietary fibre as non starch polysaccharides with gas-liquid chromatographic, high performance liquid chromatographic or spectrophotometric measurement of constituent sugars. Analyst. 119, 1497-1509.

Ersin Samli H., Senkoylu N., Akyurek H. and Agma A. (2006). Using rice bran in laying hen diets. J. Center. Europ. Agric. 7, 135-140.

Gonzalez-Alvarado J.M., Jimenez-Moreno E., Lazaro R. and Mateos G.G. (2007). Effects of type of cereal, heat processing of the cereal, and inclusion of fiber in the diet onproductive performance and digestive traits of broilers. Poult. Sci. 86, 1705-1715.

Gonzalez-Alvarado J.M., Jimenez-Moreno E., Gonzalez-Sanchez D., Lazaro R. and Mateos G.G. (2010). Effect of inclusion of oat hulls and sugar beet pulp in the diet on productive performance and digestive traits of broilers from 1 to 42 d of age. Anim. Feed Sci. Technol. 162, 37-46.

Güçlü B., İşcan K.M., Uyanık F., Eren M. and Ağca A.C. (2004). Effect of alfalfa meal in diets of laying quails on performance, egg quality and some serum parameters. Arch. Anim. Nutr. 58, 255-263.

Hetland H., Svihus B. and Krögdahl A. (2003). Effects of oat hulls and wood shavings on digestion in broilers and layers fed diets based on whole or ground wheat. Br. Poult. Sci. 44, 275-282.

Hetland H., Choct M. and Svihus B. (2004). Role of insoluble non-starch polysaccharides in poultry nutrition. World. Poult. Sci. J. 60, 415-422.

Jiang J.F., Song X.M., Huang X., Zhou W.D., Wu J.L., Zhu Z.G., Zheng H.C. and Jiang Y.Q. (2012). Effects of alfalfa meal on growth performance gastrointestinal tract development of growing duck. Asia-Australas J. Anim. Sci. 25, 1445-1450.

Jiménez-Moreno E., Gonzalez-Alvarado J.M., de Coca Sinova A., Lazaro R. and Mateos G.G. (2009). Effects of source of fibre on the development and pH of the gastrointestinal tract of broilers. Anim. Feed Sci. Technol. 154, 93-101.

Jiménez-Moreno E., Gonzalez-Alvarado J.M., de Coca Sinova A., Lazaro R. and Mateos G.G. (2013). Oat hulls and sugar beet pulp in diets for broilers. Effects on the development of the gastrointestinal tract and on the structure of the jejunal mucosa. Anim. Feed Sci. Technol. 182, 44-52.

Ju Y.S. and Vali S.R. (2005). Rice bran oil as a potential resource for biodiesel: a review. J. Sci. Ind. Res. 64, 866-882.

Kalmendal R., Elwinger K., Holm L. and Tauson R. (2011). High fibre sunflower cake affects small intestinal digestion and health in broiler chickens. Br. Poult. Sci. 52, 86-96.

Mahammadi Ghasem Abadi M.H., Riahi M., Shivazad M., ZaliA. and Adibmoradi M. (2014). Efficacy of wheat based vs. corn based diets on growth performance, carcass traits, blood parameters, jejunum morphological development, immunity, cecal microflora and excreta moisture in broiler chicks. Iranian J. Appl. Anim. Sci. 4(1), 105-110.

Mansoub N.H. and Pooryousef Myandoab M. (2012). Effect of dietary inclusion of alfalfa (Medicago sativa) and black cumin (Nigella sativa) on performance and some blood metabolites of Japanese quail. Res. Open. Anim. Vet. Sci. 2(1), 7-9.

Mateos G.G., Jiménez-Moreno E., Serrano M.P. and Lázaro R.P. (2012). Poultry response to high levels of dietary fiber sources varying in physical and chemical characteristics. J. Appl. Poult. Res. 21, 156-174.

Molist F., Gomezde Segura A., Gasa J., Hermes R.G., Manzanill E.G., Anguit M. and Perez J.F. (2009). Effects of the insoluble and soluble dietary fibre on the physicochemical properties of digesta and the microbial activity in early weaned piglets. Anim. Feed Sci. Technol. 149, 346-353.

NRC. (1994). Nutrient Requirements of Poultry, 9th Rev. Ed. National Academy Press, Washington, DC., USA.

Oladunjoye I.O. and Ojebiyi O.O. (2010). Performance characteristics of broiler chicken (Gallus gallus) fed rice (Oriza sativa) bran with or without roxazyme. Int. J. Anim. Vet. Adv. 2(4), 135-140.

Rezaei M., Karimi Torshizi M.A. and Rouzbehan Y. (2011). The influence of different levels of micronized insoluble fiber on broiler performance and litter moisture. Poult. Sci. 90, 2008-2012.

Rogel A.M., Balnave D., Bryden W.L. and Annison E.F. (1987). Improvement of raw potato starch digestion in chicks by feeding oat hulls and other fibrous feedstuffs. AustralianJ. Agric. Res. 38, 629-637.

Sarikhan M., Shahryari H.A., Nazeradl K., Gholizadeh B. and Behesht B. (2009). Effects of insoluble fiber on serum biochemical characteristics in broiler. Int. J. Agric. Biol. 11, 73-76.

SAS Institute. (2003). SAS®/STAT Software, Release 9.2. SAS Institute, Inc., Cary, NC. USA.

Shakouri M.D., Kermanshahi H. and Mohsenzadeh M. (2006). Effect of different non starch polysaccharides in semi purified diets on performance and intestinal microflora of young broiler chickens. Int. J. Poult. Sci. 5(6), 557-561.

Shirzadegan K., Fallahpour P., Nickkhah I. and Taheri H.R. (2014). Black cumin (Nigella sativa) supplementation in the diets of broilers influences liver weight and its enzyms. Irania. J. Appl. Anim. Sci. 5(1), 173-178.

Sklan D., Smirnov A. and Plavnik I. (2003). The effect of dietary fibre on the small intestine and apparent digestion in the turkey. Br. Poult. Sci. 44, 735-740.

Svihus B., Juvik E., Hetland H. and Krogdahl A. (2004). Causes for improvement in nutritive value of broiler chicken diets with whole wheat instead of ground wheat. Br. Poult. Sci. 45, 55-60.

Taheri H.R., Tanha N. and Shahir M.H. (2016). Effects of wheat bran inclusion in barley-based diet on villus morphology of jejunum, serum cholesterol, abdominal fat and growth performance of broiler chickens. J. Livest. Sci. Technol. 4(1), 9-16.

Tkacova J., Angelovicova M., Mrazova L., Kliment M. and Kral M. (2011). Effect of different proportion of lucerne meal in broiler chickens. Anim. Sci. Biotechnol. 44, 141-144.

Wellock I.J., Fortomaris P.D., Houdijk J.G.M., Wiseman J. and Kyriazakis I. (2008). The consequences of non-starch polysaccharide solubility and inclusion level on the health and performance of weaned pigs challenged with enterotoxigenic Escherichia coli. Br. J. Nutr. 99, 520-530.