Document Type : Research Paper

Authors

1 Department of Animal Science, Animal Science and Food Technology Faculty, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Iran. E-mail: Phd.imani@asnrukh.ac.ir

2 Corresponding Author, Department of Animal Science, Animal Science and Food Technology Faculty, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Iran. E-mail: S.Salari@asnrukh.ac.ir

3 Department of Biology, Faculty of Science, and Biorefinery Research Center, Shahid Chamran University of Ahvaz, Ahvaz, Iran. E-mail: motamedih@scu.ac.ir

10.22059/jap.2025.399776.623862

Abstract

Objective: The objective of this study was to evaluate the influence of the fermentation processing of rice bran and wheat bran (using bacterial, fungal, rumen liquor fermentation) on performance, intestinal morphology, and cecal microbial population of Ross 308 broiler chickens. Bran (rice and wheat), is a by-product of cereal processing that can be used as an alternative feed source in poultry nutrition because it is a rich source of nutrients and crude fiber. However, bran contains anti-nutritional compounds such as fiber and phytic acid, which reduce digestibility and absorption of nutrients. Therefore, fermentation processing may allow for the maximum utilization of bran by breaking down these anti-nutritional compounds and increasing their absorbability.
Method: In a completely randomized design with a factorial arrangement (2×4), 400 one-day-old commercial Ross 308 broiler chicks (mixed sex) were studied for 42 days to evaluate the effects of different processing methods (no processing, fermentation with Bacillus subtilis, fermentation with Aspergillus niger, fermentation with rumen liquor) and type of bran (wheat and rice at a 10% dietary inclusion level) on overall performance (feed intake, weight gain, feed conversion ratio (FCR)), intestinal morphology, cecal microbial population, and the pH of different parts of the gastrointestinal tract (gizzard, duodenum, jejunum, and ileum).
Results: The interaction between bran type and processing method was not significant in total period feed intake and weight gain, but it was significant for FCR, in which wheat bran and rice bran fermented with fungus had the lowest FCR. For main effect of the processing method, the fermentation of bran with fungus increased feed intake compared to raw bran and bran fermented with rumen liquor. Wheat bran intake compared to rice bran improved weight gain and reduced FCR. Duodenal villus height significantly greater in the fungal fermentation method compared to raw bran and bacterial fermentation method, but there was significant difference with the rumen liquor fermentation method. The duodenal villus height to crypt depth ratio was the highest in the fungal bran fermentation method. The results indicated that wheat bran significantly increased villus height and epithelial thickness and a decreased jejunal crypt depth compared to rice bran, while the jejunal villus height to crypt depth ratio was significantly higher in both the fungal and rumen liquor fermentation methods than in the raw bran groups. The ileal villus height to crypt depth ratio was highest in the groups receiving rice bran fermented with fungus and rumen liquor, as well as wheat bran fermented with fungus and lowest in the group receiving raw rice bran. The interaction of experimental factors on cecal lactobacillus population was also significant. Birds fed wheat bran fermented with rumen liquor showed a higher cecal lactobacillus population compared to other treatments, except for rice bran fermented with fungus. Birds fed fermented bran had lower cecal Escherichia coli and coliforms compared to birds fed raw bran.
Conclusion: The results indicate that the fermentation processing of wheat bran and rice bran, particularly by the fungus Aspergillus niger, may be an effective strategy in broiler chicken nutrition because of improved performance, increased villus height and reduced intestinal crypt depth, increased Lactobacillus bacteria counts, decreased pathogenic bacteria counts, and lower intestinal pH in broiler chickens.

Keywords

Reference
Akinfemi, A., & Ogunwole, O. A. (2012). Chemical composition and in vitro digestibility of rice straw treated with Pleurotus ostreatus, Pleurotus pulmonarius and Pleurotus tuber-regium. Slovak Journal of Animal Science, 45(1), 14-20.
Annunziata, G., Arnone, A., Ciampaglia, R., Tenore, G. C., & Novellino, E. (2020). Fermentation of foods and beverages as a tool for increasing availability of bioactive compounds. Focus on short-chain fatty acids. Foods, 9(8), 999. https://doi.org/10.3390/foods9080999.
Ashayerizadeh, A., Dastar, B., Shargh, M. S., Mahoonak, A. S., & Zerehdaran, S. (2017). Fermented rapeseed meal is effective in controlling Salmonella enterica serovar Typhimurium infection and improving growth performance in broiler chicks. Veterinary Microbiology, 201, 93-102. https://doi.org/10.1016/j.vetmic.2017.01.007.
Awad, W. A., Ghareeb, K., Abdel-Raheem, S., & Böhm, J. (2009). Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorpHology of broiler chickens. Poultry Science, 88(1), 49-56. https://doi.org/10.3382/ps.2008-00244.
Belal, E. (2017). Assessment of the performance of chicks fed with wheat bran solid fermented by Trichoderma longibrachiatum (SF1). Journal of Sustainable Agricultural Sciences, 43(2), 115-126.  https://doi.org/ 10.21608/jsas.2017.1162.1008.
Belewu, M. A. (2006). Conversion of Mansonia tree sawdust and cotton plant byproduct into feed by White rot fungus. African Journal of Biotechnology, 5 (19), 1763-1764.
Chiang, G., Lu, W. Q., Piao, X. S., Hu, J. K., Gong, L. M., & Thacker, P. A. (2009). Effects of feeding solid-state fermented rapeseed meal on performance, nutrient digestibility, intestinal ecology and intestinal morpHology of broiler chickens. Asian-Australasian Journal of Animal Sciences, 23(2), 263-271. https://doi.org/10.5713/ajas.2010.90145.
Chu, Y. T., Lo, C. T., Chang, S. C., & Lee, T. T. (2017). Effects of Trichoderma fermented wheat bran on growth performance, intestinal morphology and histological findings in broiler chickens. Italian Journal of Animal Science, 16(1), 82-92. https://doi.org/10.1080/1828051X.2016.1241133.
Chuang, W. Y., Lin, L. J., Hsieh, Y. C., Chang, S. C., & Lee, T. T. (2020). Effects of saccharomyces cerevisiae and phytase co-fermentation of wheat bran on growth, antioxidation, immunity and intestinal morphology in broilers. Animal Bioscience, 34(7), 1157.  https://doi.org/10.5713/ajas.20.0399.
Cong, Y., Weaver, C. T., Lazenby, A., & Elson, C. O. (2002). Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. The Journal of Immunology, 169(11), 6112-6119. https://doi.org/10.4049/jimmunol.169.11.6112.
Debi, M. R., Wichert, B. A., & Liesegang, A. (2018). Method development to reduce the fiber content of wheat bran and rice bran through anaerobic fermentation with rumen liquor for use in poultry feed. Asian-Australasian journal of Animal Sciences, 32(3), 395.  https://doi.org/ 10.5713/ajas.18.0446.
Debi, M. R., Wichert, B. A., & Liesegang, A. (2022). Anaerobic fermentation of rice bran with rumen liquor for reducing their fiber components to use as chicken feed. Heliyon, 8(4), e09275. https://doi.org/10.1016/j.heliyon.2022.e09275.
Diaz Carrasco, J.M., Casanova, N.A., & Fernández Miyakawa, M.E. (2019). Microbiota, gut health and chicken productivity: what is the connection?. Microorganisms, 7(10), 374. https://doi.org/10.3390/microorganisms7100374.
Donkor, O. N., Henriksson, A., Vasiljevic, T., & Shah, N. P. (2006). Effect of acidification on the activity of probiotics in yoghurt during cold storage. International Dairy Journal, 16(10), 1181-1189. https://doi.org/10.1016/j.idairyj.2005.10.008
Gungor, E., & Erener, G. (2020). Effect of dietary raw and fermented sour cherry kernel (Prunus cerasus L.) on digestibility, intestinal morpHology and caecal microflora in broiler chickens. Poultry Science, 99(1), 471-478. https://doi.org/10.3382/ps/pez538.
Gungor, E., Altop, A., & Erener, G. (2021). Effect of raw and fermented grape pomace on the growth performance, antioxidant status, intestinal morphology, and selected bacterial species in broiler chicks. Animals, 11(2), 364. https://doi.org/10.3390/ani11020364.
Gungor, E., Altop, A., Erener, G., & Coskun, I. (2021). Effect of raw and fermented pomegranate pomace on performance, antioxidant activity, intestinal microbiota and morphology in broiler chickens. Archives of Animal Nutrition, 75(2), 137-152. https://doi.org/10.1080/1745039X.2021.1894065.
Guo, L., Lv, J., Liu, Y., Ma, H., Chen, B., Hao, K., & Min, Y. (2021). Effects of different fermented feeds on production performance, cecal microorganisms, and intestinal immunity of laying hens. Animals, 11(10), 2799. https://doi.org/10.3390/ani11102799.
Huang, C. M., Chuang, W. Y., Lin, W. C., Lin, L. J., Chang, S. C., & Lee, T. T. (2020). Production performances and antioxidant activities of laying hens fed Aspergillus oryzae and phytase co-fermented wheat bran. Animal Bioscience, 34(3), 371.  https://doi.org/ 10.5713/ajas.20.0116
Jazi, V., Boldaji, F., Dastar, B., Hashemi, S. R., & Ashayerizadeh, A. (2017). Effects of fermented cottonseed meal on the growth performance, gastrointestinal microflora population and small intestinal morphology in broiler chickens. British Poultry Science, 58(4), 402-408. https://doi.org/10.1080/00071668.2017.1315051.
Jha, R., & Berrocoso, J.D. (2015). Dietary fiber utilization and its effects on physiological functions and gut health of swine. Animal, 9(9), 1441-1452. https://doi.org/10.1017/S1751731115000919.
Kim, C. H., Kim, G. B., Chang, M. B., Bae, G. S., Paik, I. K., & Kil, D. Y. (2012). Effect of dietary supplementation of Lactobacillus-fermented Artemisia princeps on growth performance, meat lipid peroxidation, and intestinal microflora in Hy-line Brown male chickens. Poultry Science, 91(11), 2845-2851. https://doi.org/10.3382/ps.2012-02467.
Kim, S. A., Rubinelli, P. M., Park, S. H., & Ricke, S. C. (2018). Ability of Arkansas LaKast and LaKast hybrid rice bran to reduce Salmonella Typhimurium in chicken cecal incubations and effects on cecal microbiota. Frontiers in Microbiology, 9, 134. https://doi.org/10.3389/fmicb.2018.00134.
Lawal, T. E., Ademola, S. G., Owoseni, A., Atobatele, O. E., & Oriye, L. O. (2013). Use of Aspergillus niger for improving the feeding value of rice offal. African Journal of Biotechnology, 12(20).  https://doi.org/ 10.5897/AJB12.2642.
Li, L., Li, W. F., Liu, S. Z., & Wang, H. H. (2020). Probiotic fermented feed improved the production, health and nutrient utilisation of yellow-feathered broilers reared in high altitude in Tibet. British Poultry Science, 61(6), 746-753. https://doi.org/10.1080/00071668.2020.1801988.
Lin, W.C., & Lee, T.T. (2020). Laetiporus sulphureus–fermented wheat bran enhanced the broiler growth performance by improving the intestinal microflora and inflammation status. Poultry Science, 99(7), pp.3606-3616. https://doi.org/10.1016/j.psj.2020.04.011.
Lin, W.C., Lee, M.T., Lo, C.T., Chang, S.C., & Lee, T.T. (2018). Effects of dietary supplementation of Trichoderma pseudokoningii fermented enzyme powder on growth performance, intestinal morpHology, microflora and serum antioxidantive status in broiler chickens. Italian Journal of Animal Science, 17(1), 153-164. https://doi.org/10.1080/1828051X.2017.1355273.
Liu, Y., Feng, J., Wang, Y., Lv, J., Li, J., Guo, L., & Min, Y. (2021). Fermented corn–soybean meal mixed feed modulates intestinal morphology, barrier functions and cecal microbiota in laying hens. Animals, 11(11), 3059. https://doi.org/10.3390/ani11113059.
Mahmood, T., & Guo, Y. (2020). Dietary fiber and chicken microbiome interaction: Where will it lead to?. Animal Nutrition, 6(1), 1-8. https://doi.org/10.1016/j.aninu.2019.11.004.
Ménard, S., Cerf-Bensussan, N., & Heyman, M. (2010). Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunology, 3(3), 247-259. https://doi.org/10.1038/mi.2010.5
Missotten, J. A., Michiels, J., Dierick, N., Ovyn, A., Akbarian, A., & De Smet, S. (2013). Effect of fermented moist feed on performance, gut bacteria and gut histo-morphology in broilers. British Poultry Science, 54(5), 627-634. https://doi.org/10.1080/00071668.2013.811718.
Muir, W.I., Bryden, W.L., & Husband, A.J. (2000). Immunity, vaccination and the avian intestinal tract. Developmental and Comparative Immunology, 24(2-3), 325-342. https://doi.org/10.1016/S0145-305X(99)00081-6.
Naji, S. A., Al-Zamili, I. F. B., Hasan, S. A., & Al-Gharawi, J. K. M. (2016). The Effects of Fermented Feed on Broiler Production and Intestinal MorpHology. Pertanika Journal of Tropical Agricultural Science, 39(4).
Nordberg Karlsson, E., Schmitz, E., Linares-Pastén, J. A., & Adlercreutz, P. (2018). Endo-xylanases as tools for production of substituted xylooligosaccharides with prebiotic properties. Applied Microbiology and Biotechnology102(21), 9081-9088.
Ogbuewu, I. P., Mabelebele, M., & Mbajiorgu, C. A. (2024). Determination of performance response of broilers to fermented tropical leaf meal supplementation using meta-analytical method. Tropical Animal Health and Production, 56(2), 98. https://doi.org/10.1007/s11250-024-03944.
Oguri, M., Okano, K., Ieki, H., Kitagawa, M., Tadokoro, O., Sano, Y., ..., & Kumagai, H. (2013). Feed intake, digestibility, nitrogen utilization, ruminal condition and blood metabolites in wethers fed ground bamboo pellets cultured with white‐rot fungus (Ceriporiopsis subvermispora) and mixed with soybean curd residue and soy sauce cake. Animal Science Journal, 84(9), 650-655. https://doi.org/10.1111/asj.12054.
Peng, W., Talpur, M. Z., Zeng, Y., Xie, P., Li, J., Wang, S., ..., & Zhang, H. (2022). Influence of fermented feed additive on gut morphology, immune status, and microbiota in broilers. BMC Veterinary Research, 18(1), 218. https://doi.org/10.1186/s12917-022-03322-4.
Predescu, N. C., Stefan, G., Rosu, M. P., & Papuc, C. (2024). Fermented feed in broiler diets reduces the antinutritional factors, improves productive performances and modulates gut microbiome—A review. Agriculture, 14(10), 1752. https://doi.org/10.3390/agriculture14101752.
Rinttilä, T., & Apajalahti, J. (2013). Intestinal microbiota and metabolites—Implications for broiler chicken health and performance. Journal of Applied Poultry Research, 22(3), 647-658. https://doi.org/10.3382/japr.2013-00742.
Slominski, B. A., Boros, D., Campbell, L. D., Guenter, W., & Jones, O. (2004). Wheat by-products in poultry nutrition. Part I. Chemical and nutritive composition of wheat screenings, bakery by-products and wheat mill run. Canadian Journal of Animal Science, 84(3), 421-428. https://doi.org/10.4141/A03-112.
Soltani Naseri, K., Ghanbari, F., Bayat Kouhsar, J., & Taliey, F. (2018). Effect of chemical and biological processing methods on chemical composition, gas production parameters and in vitro digestibility of Cicer arietinum wastes. Research on Animal Production, 9(22), 72-82. doi:10.29252/rap.9.22.72.
Souci, S.W., & Kirchhoff, E. (2008). Food Composition and Nutrition Tables. 7th ed. Stuttgart, Germany: MedpHarm Scientific Publ.
Sugiharto, S., & Ranjitkar, S. (2019). Recent advances in fermented feeds towards improved broiler chicken performance, gastrointestinal tract microecology and immune responses: A review. Animal Nutrition, 5(1), 1-10. https://doi.org/10.1016/j.aninu.2018.11.001.
Sun, H., Chen, D., Cai, H., Chang, W., Wang, Z., Liu, G., ..., & Chen, Z. (2022). Effects of fermenting the plant fraction of a complete feed on the growth performance, nutrient utilization, antioxidant functions, meat quality, and intestinal microbiota of broilers. Animals, 12(20), 2870. https://doi.org/10.3390/ani12202870.
Sun, H., Tang, J. W., Yao, X. H., Wu, Y. F., Wang, X., & Feng, J. (2013). Effects of dietary inclusion of fermented cottonseed meal on growth, cecal microbial population, small intestinal morphology, and digestive enzyme activity of broilers. Tropical Animal Health and Production, 45(4), 987-993. https://doi.org/10.1007/s11250-012-0322-y.
Sundu, B., Adjis, A., Sarjuni, S., Mozin, S., & Hatta, U. (2021, June). Fermented palm kernel meal by different fungi in broiler diets. In IOP Conference Series: Earth and Environmental Science (Vol. 788, No. 1, p. 012041). IOP Publishing.  https://doi.org/10.1088/1755-1315/788/1/012041.
Ti, H., Guo, J., Zhang, R., Wei, Z., Liu, L., Bai, Y., & Zhang, M. (2015). Phenolic profiles and antioxidant activity in four tissue fractions of whole brown rice. RSC Advances, 5(123), 101507-101518.
Wang, Y., Zheng, W., Deng, W., Fang, H., Hu, H., Zhu, H., & Yao, W. (2023). Effect of fermented heat-treated rice bran on performance and possible role of intestinal microbiota in laying hens. Frontiers in Microbiology, 14, 1144567. https://doi.org/10.3389/fmicb.2023.1144567.
Wizna, H. A., Rizal, Y., Dharma, A., & Kompiang, I. P. (2009). Improving the quality of tapioca by-products (onggok) as poultry feed through fermentation by Bacillus amyloliquefaciens. Pakistan Journal of Nutrition, 8(10), 1636-1640.
Wu, X., Li, F., & Wu, W. (2020). Effects of rice bran rancidity on the oxidation and structural characteristics of rice bran protein. Lwt, 120, 108943. https://doi.org/10.1016/j.lwt.2019.108943.
Xu, F. Z., Zeng, X. G., & Ding, X. L. (2012). Effects of replacing soybean meal with fermented rapeseed meal on performance, serum biochemical variables and intestinal morphology of broilers. Asian-Australasian Journal of Animal Sciences, 25(12), 1734. https://doi.org/10.5713/ajas.2012.12249.
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. Poultry Science82(6), 1030-1036. https://doi.org/10.1093/ps/82.6.1030.
Zhang, X., Cao, F., Sun, Z., Yu, W., Zhao, L., Wang, G., & Wang, T. (2012). Effect of feeding Aspergillus niger-fermented Ginkgo biloba-leaves on growth, small intestinal structure and function of broiler chicks. Livestock Science, 147(1-3), 170-180. https://doi.org/10.1016/j.livsci.2012.04.018.