Effect of dietary inclusion level and particle size of barley hulls on intestinal morphology and bacteria population in broiler chickens


1 Department of Animal Science, University of Mohaghegh Ardabili, Ardabil, Iran

2 Department of Basic Sciences, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran


BACKGROUND: The insoluble fiber content of poultry feeds is often considered as an unfavorable factor which reduces the nutritive value of diet. OBJECTIVES: The effects of barley hulls on performance traits of broiler chickens were evaluated. METHODS: The experiment was carried out using 200 Ross 308 broiler chickens in a completely randomized design with 5 treatments and 4 replicates. The experimental diets  consisted of a control hulls-free diet and four diets containing 0.75 or 1.5 percent barley hulls with particle sizes of less than 1 mm or between 1-2 mm. RESULTS: The dietary type did not affect feed intake of the experimental groups. In the whole the experimental period, the weight gain and feed conversion ratio in the broiler chickens feed, the diet that contained 1.5% barley hulls with 1-2 mm particle size improved compared to the control group (p<0.05). In the jejunum, fiber feeding resulted in an increased goblet cell number as compared to the control group (p<0.05). Unexpectedly, barley hulls feeding reduced the villi height compared to the control group (p<0.05). In jejunum the crypt depth in control birds was more than the treatment fed 1.5% barley hulls with less than 1 mm particle size (p<0.05). The ratio of crypt depth to villus height in control group was more than the birds fed the diet that contained 1.5% barley hulls with less than 1 mm particle size (p< 0.05). In ileum the chickens fed the control diet had more lactobacillus and less Escherichia coli than the majority of the treatment fed barley hulls. CONCLUSIONS: Inclusion of 1.5% barley hulls with particle size of 1-2 mm in diet improved performance traits of broiler chickens. On the other hand, using 1.5% barley hulls as a lignocelluloses source increased lactobacillus growth and reduced Escherichia coli population. This alteration in intestinal micro flora suggests a prebiotic effect for barley hulls in the gastrointestinal tract of broiler chickens.


Adibmoradi, M., Navidshad, B., Seifdavati, M., Royan, M. (2006) Effect of dietary garlic meal on histological structure of small intestine in broiler chickens. J Poult Sci. 43: 378-383.
Aerni, V., El-Lethey, H., Wechsler, B. (2000) Effect of foraging material and food form on feather pecking in laying hens. Br Poult Sci. 41: 16-21.
Amerah, A.M., Ravindran, V., 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.
Amit-Romach, E., Sklan, D., Uni, Z. (2004) Environment, Health, and Behavior Microflora Ecology of the Chicken Intestine Using 16S Ribosomal DNA Primers. Poult Sci. 83: 1093-1098
AOAC International. (2000) Official Methods of Analysis. (18th ed.) AOAC International, Gaithersburg, MD.
Awad, W., Gharee, K., Abdel-Raheem, S., Bِhm, J. (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci. 88: 49-56.
Barnes, E.M. (1979) The intestinal microflora of poultry and game birds during life and after storage. J Appl Bacteriol 45: 407-419
Baurhoo, B., Phillip, L., Ruiz-Feria, C.A. (2007) Effects of purified lignin and mannan oligosaccharides on intestinal integrity and microbial populations in the ceca and litter of broiler chickens. Poult Sci. 86: 1070-1078.
Baurhoo, B., Ruiz-Feria, C.A., Zhao, X. (2008) Purified lignin: nutritional and health impacts on farm animals - a review. Anim Feed Sci Tech. 144: 175-184.
Bogusławska-Tryk, M., Piotrowska, A., Burlikowska, K. (2012) Dietary fructans and their potential beneficial influence on health and performance parameters in broiler chickens. J Centr Eur Agr. 13: 272-291.
Bogusławska-Tryk, M., Szymeczko, R., Piotrowska, A., Burlikowska, K., Śliżewska, K. (2015) Ileal and cecal microbial population and short-chain fatty acid profile in broiler chickens fed diets supplemented with lignocellulose. Pak Vet J. 35: 212-216.
Brashears, M.M., Jaroni, D., Trimble, J. (2003) Isolation, selection, and characterization of lactic acid bacteria for a competitive exclusion product to reduce shedding of Escherichia coli O157:H7 in cattle. J Food Prot. 66: 355-363.
Cao, B.H., Zhang, X.P., Guo, Y.M., Karasawa, Y., Kumao, T. (2003) Effects of dietary cellulose levels on growth, nitrogen utilization, retention time of diets in digestive tract and caecal microflora of chickens. Asian-Australas J Anim Sci. 16: 863-866.
Castanon, J.I.R. (2007) History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci. 86: 2466-2471.
Cherrington, C.A., Hinton, M., Chopra, I. (1990) Effect of short-chain organic acids on macromolecular synthesis in Escherichia coli. J Appl Bacteriol. 68: 69-74.
Correa-Matos, N.J., Donovan, S.M., Issacson, R.E., Gaskins, H.R., White, B.A., Tappenden, K.A. (2003) Fermentable fiber reduces recovery time and improves intestinal function in piglets following Salmonella typhimurium infection. J Nutr. 133: 1845-1852.
Dozois, C.M., Daigle, F., Curtiss, R. (2003) Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci USA. 100: 247-252.
Farran, M.T., Pietsch, M., Chabrillat, T. (2013) Effect of lignocellulose on the litter quality and the ready to cook carcass yield of male broilers. Poult Res Foie Gras. La Rochelle. France. 10: 36-42.
Filazi, A., Sireli, U., Cadirci. O. (2005) Residues of gentamicin in eggs following medication of laying hens. Br Poult Sci. 46: 580-583.
González-Alvarado, J.M., Jiménez-Moreno, E., Lázaro, R., Mateos, G.G. (2007) Effects of type of cereal, heat processing of the cereal, and inclusion of fiber in the diet on productive performance and digestive traits of broilers. Poult Sci. 86: 1705-1715.
González-Alvarado, J.M., Jiménez-Moreno, E., González-Sánchez, D., Lázaro, R., 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 days of age. Anim Feed Sci Technol. 162: 37-46.
Hampson, D.J. (1986) Alteration in piglet small intestine structure at weaning. Res Vet Sci. 40: 32-40.
Heilig, H.G.H.J., Zoetendal, E.G, Vaughan, E.E., Marteau, P., Akkermans, A.D.L., De Vos, W.M. (2002) Molecular Diversity of Lactobacillus spp. and Other Lactic Acid Bacteria in the Human Intestine as Determined by Specific Amplification of 16S Ribosomal DNA. Appl Environ Microbiol. 68: 114-123.
Hetland, H., Svihus, B. Krögdahl, Å. (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., Svihus, B. (2004) Role of insoluble nonstarch polysaccharides in poultry nutrition. World’s Poult Sci J. 60: 415-422.
Hetland, H.J., Svihus, B., Choct, M. (2005) Role of insoluble fiber on gizzard activity in layers. J Appl Poult Res. 14: 38-46.
Hetland, H., Svihus, B. (2007) Inclusion of dust bathing materials affects nutrient digestion and gut physiology of layers. J Appl Poult Res. 16: 22-26.
Jamroz, D., Jacobsen, K., Orda, J., Skorupinska, J., Wiliczkiewicz, A. (2001) Development of the gastrointestinal tract and digestibility of dietary fibre and amino acids in young chickens, ducks and geese fed diets with high amounts of barley. Comp Biochem Physiol A. 130: 643-652.
Jiménez-Moreno, E., Gonzalez-Alvarado, J.M., Gonzalez-Sanchez, D., Lozaro, R., Mateos, G.G. (2010) Effect of type and particle size of fiber source of the diet on productive performance and digestive traits of broilers from 1 to 21 days of age. Poult Sci. 89: 2197-2212.
Kalmendal, R., Elwinger, K., Holm, L., Tauson, R. (2011) High-fibre sunflower cake affects small intestinal digestion and health in broiler chickens. Br Poult Sci. 52: 86-96.
Kawai, Y., Ishii, Y., Arakawa, K., Uemura, K., Saitoh, B., Nishimura, J., Kitazawa, H., Yamazaki, Y., Tateno, Y., Itoh, T., Saito, T. (2004) Structural and functional differences in two cyclic bacteriocins with the same sequences produced by lactobacilli. Appl Environ Microbiol. 70: 2906-2911.
Kim, Y.S., Ho, S.B. (2010) Intestinal goblet cells and mucins in health and disease: Recent insights and progress. Curr Gastroenterol Rep. 12: 319-330.
Kim, G.B., Seo, Y.M., Kim, C.H., Paik, I.K. (2011) Effect of dietary prebiotic supplementation on the performance, intestinal microflora, and immune response of broilers. Poult Sci. 90: 75-82.
Krás, R.V., Kessler, A.M., Ribeiro, A.M.L., Henn, J.D.. dos Santos, I.I., Halfen, D.P., Bockor, L. (2013) Effect of dietary fiber and genetic strain on the performance and energy balance of broiler chickens. Braz J Poult Sci. 15: 15-20.
Larsen, F.M., Moughan, P.J., Wilson, M.N. (1993) Dietary fiber viscosity and endogenous protein excretion at the terminal ileum of growing rats. J Nutr. 123: 1898-1904.
Li, X., Liu, L., Li, K., Hao, K., Xu, C. (2007) Effect of fructooligosaccharides and antibiotics on laying performance of chickens and cholesterol content of egg yolk. Br Poult Sci. 48: 185-189.
Lu, J., Idris, U., Harmon, B., Hofacre, C., Maurer, J. J. and Lee, M. D. (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microb. 69: 6816-6824.
Mateos, G.G., Jiménez-Moreno, E., Serrano, M.P., 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.
Mead, G.C. (1997) Bacteria in the Gastrointestinal Tract of Birds. Mackie, R.J., White, B.A., Isaacson, R.E. (eds.). Gastrointestinal Microbiology. Chapman and Hall, New York.
Miller Jones, J. (2004) Dietary fibre intake, disease prevention, and health promotion. In: Dietary Fibre: Bio-active Carbohydrates for Food and Feed. Van der Kamp, J.W., Asp, N.G., Miller Jones, J., Schaafsma, G. (eds.). Wageningen Academic Publishers, Netherlands. p. 143-159.
Montagne, L., Pluske, J.R., Hampson, D.J. (2003) A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim Feed Sci Technol. 108: 95-117.
Montagne, L., Piel, C., Lalles, J.P. (2004) Effect of diet on mucin kinetics and composition: Nutrition and health implications. Nutr Rev. 62: 105-114.
Nabizadeh, A. (2012) The effect of inulin on broiler chicken intestinal microflora, gut morphology, and performance. J Anim Feed Sci. 21: 725-734.
Navidshad, B., Liang, J.B., Faseleh Jahromi, M., Akhlaghi, A., Abdullah, N. (2015) A comparison between a yeast cell wall extract (Bio-Mos®) and palm kernel expeller as mannan-oligosaccharides sources on the performance and ileal microbial population of broiler chickens. Ital J Anim Sci. 14: 3452.
Nelson, J.L., Alexander, J.W., Gianotti, L., Chalk, C.L., Pyles, T. (1994) Influence of dietary fiber on microbial growth in vitro and bacterial translocation after burn injury in mice. Nutrition 10: 32-36.
O’Shea, E.F., Cotter, P.D., Stanton, C., Ross, R.P., Hill, C. (2012) Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: Bacteriocins and conjugated linoleic acid. Int J Food Microbiol. 152: 189-205.
Perez, V.G., Jacobs, C.M. Barnes, J., Jenkins, M.C., Kuhlenschmidt, M.S., Fahey, G.C., Parsons, C.M., Pettigrew, J.E. (2011) Effect of corn distillers dried grains with solubles and Eimeria acervulina infection on growth performance and the intestinal microbiota of young chicks. Poult Sci. 90: 958-964.
Rehman, H.U., Vahjen, W., Awad, W.A., Zentek, J. (2007) Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Arch Anim Nut. 61: 319-335.
Rogel, A.M., Balnave, D., Bryden, W.L., Annison, E.F. (1987) Improvement of raw potato starch digestion in chickens by feeding oat hulls and other fibrous feedstuffs. Aust J Agric Res. 38: 629-637.
Sackey, B.A., Mensah, P., Collison, E., Sakyi-Dawson, E. (2001) Campylobacter, Salmonella, Shigella and Escherichia coli in live and dressed poultry from metropolitan Accra. Int J Food Microbiol. 71: 21-28
Saki, A.A., Hemati Matin, H.R., Tabatabai, M.M., Zamani, P., Naseri Harsini, R. (2010) Microflora population, intestinal condition and performance of broilers in response to various rates of pectin and cellulose in the diet. Arch Geflügelk, 74: 183-188.
Sarikhan, M., Shahryar, H.A., Gholizadeh, B., Hosseinzadeh, M.H., Beheshti, B., Mahmoodnejad, A. (2010) Effects of insoluble fiber on growth performance, carcass traits and ileum morphological parameters on broiler chick males. Int J Agric Biol. 12: 531-536.
Sklan, D., Smirnov, A., Plavnik, I. (2003) The effect of dietary fiber on the small intestines and apparent digestion in the turkey. Br Poult Sci. 44: 735-740.
Souli, M., Kontopidou, F.V., Papadomichelakis, E. (2008) Clinical experience of serious infections caused by Enterobacteriaceae producing VIM-1 metallo-betalactamase in a Greek University Hospital. Clin Infect Dis. 46: 847-854.
Svihus, B. (2011) The gizzard: Function, influence of diet structure and effects on nutrient availability. World’s Poult Sci J. 67: 207-224.
Svihus, B., Hetland, H. (2001) Ileal starch digestibility in growing broiler chickens fed on a wheat-based diet is improved by mash feeding, dilution with cellulose or whole wheat inclusion. Br Poult Sci. 42: 633-637.
Tannock, G.W. (2005) Probiotics and Probiotics: Scientific Aspects. Caister Academic Press. London, UK.
Tkáčová, J., Angelovičová, M. (2013) Effect of Lucerne Meal on Broiler Chickens Cecum. Anim Sci Biotechnol. 46: 2. 
Van der Wielen, P.W.J.J., Biesterveld, S., Notermans, S., Hofstra, H., Urlings, B.A.P., van Knapen, F. (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chicken during growth. Appl Environ Microbiol. 66: 2536-2540.
Van der Wielen, P.W., Biesterveld, S., Lipman, L. J.A., Van Knapen, F. (2001) Inhibition of a glucoselimited sequencing fed-batch culture of Salmonella enteric (Serovar Enteritidis) by volatile fatty representative of the ceca of broiler chickens. Appl Environ Microbiol. 67: 1979-1982.
Van Krimpen, M. M., Kwakkel, R.P., van Peet-Schwering, C.M.C., den Hartog, L.A. Verstegen, M.W.A. (2009) Effects of nutrient dilution and nonstarch polysaccharide concentration in rearing and laying diets on eating behavior and feather damage of rearing and laying hens. Poult Sci. 88: 759-773.
Van Soest, P.J. (1963) Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. J Assoc Offic Agric Chem. 46: 829-835.
Van Soest, P.J. (1985) Definition of fibre in animal feeds. In: Recent Advances in Animal Nutrition. Haresign W, Cole DJA. (eds.). Butterworths, London. UK. p. 55-70.
Wils-Plotz, E.L., Dilger, R.N. (2013) Combined dietary effects of supplemental threonine and purified fiber on growth performance and intestinal health of young chicks. Poult Sci. 92: 726-734.
Xu. Z.R., Hu, C.H., Xia, M.S., Zhan, X.A., Wang, M.Q. (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult Sci. 82: 1030-1036.