Abstract
The objective of this study was to investigate the effects of soybean meal (SBM) treated with acetic or citric acids on growth performance, microbial population, digestive enzyme activities, nutrient digestibility, and jejunal morphology in broiler chickens. A total of 350 one-day-old male broiler chicks (Ross 308) were randomly distributed into 7 experimental groups with 5 replicates per each. Experimental treatments were diets containing untreated SBM (control) and SBM treated with two acid sources and their concentrations including 5, 10, and 15% acetic acid (A1, A2, and A3) or 0.25, 0.50, and 0.75% citric acid (C1, C2, and C3). Results showed that trypsin inhibitors and lectins as the main SBM anti-nutrients significantly reduced in acid-treated SBM compared with untreated SBM (P < 0.05). During 1–24 days, body weight gain increased in chicks fed the C2 diet (P < 0.05). Feeding of the C2 diet increased feed intake compared with A1, A2, and C3 groups (P < 0.05). Feed conversion ratio improved in chicks fed with C2, C3, and A2 diets compared with the control group (P < 0.05). The greatest villus length, villus length to crypt depth ratio, and villus surface area were observed in the C2 diet (P < 0.05). A significant increase in protease and lipase activity was found in broilers which received a C2 diet compared with the control group (P < 0.05). Broiler chickens fed with the C2 diet had a higher organic matter and crude protein digestibility than the chicks which received the control diet (P < 0.05) and dry matter digestibility was the lowest in broilers fed with the A3 diet (P < 0.05). In conclusion, the acid hydrolyzing process had a beneficial effect on the nutritional value of SBM. In addition, data showed that acid-hydrolyzed SBM had the potential to exert positive influences on growth performance, jejunal morphology, and nutrient utilization in broiler chickens.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
All data generated and analyzed during this study are included in this published article.
Code availability
Not applicable.
References
Abdollahi M, Zaefarian F, Gu Y, Xiao W, Jia J, Ravindran V. 2018. Influence of soybean bioactive peptides on performance, foot pad lesions and carcass characteristics in broilers. Journal of Applied Animal Nutrition. 6: e3, 1-7.
Ao T, Cantor AH, Pescatore AJ, Ford MJ, Pierce JL, Dawson KA. 2009. Effect of enzyme supplementation and acidification of diets on nutrient digestibility and growth performance of broiler chicks. Poultry Science. 88:111-117.
AOAC, 1990. Official Methods of Analysis, 15th ed., Association of Official Analytical Chemists: Arlington, VA, USA
Arce-Menocal J, Roa-Flores M, López-Coello C, Ávila-González E, Herrera-Camacho J, Cortes-Cuevas A. 2020. Use of organic acids in water and its effect on productive performance in broiler chicks. Abanico veterinario.10: 1-17.
Aviagen. 2019. Nutrition Specification for Ross 308. Aviagen Limited, Newbridge, Scotland.
Batal A, Parsons C. 2003. Utilization of different soy products as affected by age in chicks. Poultry Science.82:454-462.
Buttle L, Burrells A, Good J, Williams P, Southgate P, Burrells C. 2001. The binding of soybean agglutinin (SBA) to the intestinal epithelium of Atlantic salmon, Salmo salar and Rainbow trout, Oncorhynchus mykiss, fed high levels of soybean meal. Veterinary Immunology and Immunopathology.80:237-244.
Chen J, Wedekind K, Escobar J, Vazquez-Añón M. 2020. Trypsin Inhibitor and Urease Activity of Soybean Meal Products from Different Countries and Impact of Trypsin Inhibitor on Ileal Amino Acid Digestibility in Pig. Journal of the American Oil Chemists’ Society.97:1151-1163.
Clarke E, Wiseman J. 2005. Effects of variability in trypsin inhibitor content of soya bean meals on true and apparent ileal digestibility of amino acids and pancreas size in broiler chicks. Animal Feed Science and Technology.121:125-138.
Clarke E, Wiseman J. 2007. Effects of extrusion conditions on trypsin inhibitor activity of full fat soybeans and subsequent effects on their nutritional value for young broilers. British Poultry Science.48:703-712.
da Costa Lopes AM, Bogel ŁR. 2015. Acidic ionic liquids as sustainable approach of cellulose and lignocellulosic biomass conversion without additional catalysts. ChemSusChem.8:947-965.
Eftekhari A, Rezaeipour V, Abdullahpour R. 2015. Effects of acidified drinking water on performance, carcass, immune response, jejunum morphology, and microbiota activity of broiler chickens fed diets containing graded levels of threonine. Livestock Science. 180:158-163.
Erdaw MM, Beyene WT. 2018. Anti-nutrients reduce poultry productivity: influence of trypsin inhibitors on pancreas. Asian Journal of Poultry Science.12:1-12.
Feng J, Liu X, Xu Z, Wang Y, Liu J. 2007. Effects of fermented soybean meal on digestive enzyme activities and intestinal morphology in broilers. Poultry Science. 86:1149-1154.
Fenton T, Fenton M. 1979. An improved procedure for the determination of chromic oxide in feed and feces. Canadian Journal of Animal Science.59:631-634.
Heres L, Engel B, Urlings H, Wagenaar J, Van Knapen F. 2004. Effect of acidified feed on susceptibility of broiler chickens to intestinal infection by Campylobacter and Salmonella. Veterinary Microbiology. 99:259-267.
Horwitz W. 2010. Official methods of analysis of AOAC International. Volume I, agricultural chemicals, contaminants, drugs/edited by William Horwitz: Gaithersburg (Maryland): AOAC International.
Huang L, Xu Y. 2018. Effective reduction of antinutritional factors in soybean meal by acetic acid catalyzed processing. Journal of Food Processing and Preservation.42:e13775.
Huang L, Xu Y, Zhou Y. 2019. Improvement of nutritional quality of soybean meal by Fe (II)-assisted acetic acid treatment. Food Chemistry. 283:475-480.
Kiarie EG, Parenteau IA, Zhu C, Ward NE, Cowieson AJ. 2020. Digestibility of amino acids, energy, and minerals in roasted full-fat soybean and expelled-extruded soybean meal fed to growing pigs without or with multienzyme supplement containing fiber-degrading enzymes, protease, and phytase. Journal of Animal Science. 98: 1-10.
Kim S, Kim T, Lee S, Chang K, Cho S, Lee K, An B. 2016. The use of fermented soybean meals during early phase affects subsequent growth and physiological response in broiler chicks. Asian-Australasian Journal of Animal Sciences. 29:1287-1293.
Li D, Nelssen J, Reddy P, Blecha F, Hancock J, Allee G, Goodband R, Klemm R. 1990. Transient hypersensitivity to soybean meal in the early-weaned pig. Journal of Animal Science .68: 1790-1799.
Li C-Y, Lu J-J, Wu C-P, Lien T-F. 2014. Effects of probiotics and bremelain fermented soybean meal replacing fish meal on growth performance, nutrient retention and carcass traits of broilers. Livestock Science.163:94-101.
Lynn K, Clevette-Radford N. 1984. Purification and characterization of hevain, a serine protease from Hevea brasiliensis. Phytochemistry. 23: 963-964.
Marsman G, Gruppen H, Van der Poel A, Kwakkel R, Verstegen M, Voragen A. 1997. The effect of thermal processing and enzyme treatments of soybean meal on growth performance, ileal nutrient digestibilities, and chyme characteristics in broiler chicks. Poultry Science.76: 864-872.
Moss A, Truong H, Liu S, Selle P. 2018. Inclusion levels and modes of whole grain incorporation into wheat-based rations differentially influence the performance of broiler chickens. British Poultry Science.59:110-120.
Murashita K, Akimoto A, Iwashita Y, Amano S, Suzuki N, Matsunari H, Furuita H, Sugita T, Yamamoto T. 2013. Effects of biotechnologically processed soybean meals in a nonfishmeal diet on growth performance, bile acid status, and morphological condition of the distal intestine and liver of rainbow trout Oncorhynchus mykiss. Fisheries Science.79:447-457.
Norozi M, Rezaei M, Kazemifard M. 2022. Effect of different acid processing methodologies on the nutritional value and reduction of anti-nutrients in soybean meal. Journal of Food processing and Preservation. 46(1): e16205.
Pacheco W, Stark C, Ferket P, Brake J. 2014. Effects of trypsin inhibitor and particle size of expeller-extracted soybean meal on broiler live performance and weight of gizzard and pancreas. Poultry Science. 93:2245-2252.
Palliyeguru MCD, Rose S, Mackenzie A. 2011. Effect of trypsin inhibitor activity in soya bean on growth performance, protein digestibility and incidence of sub-clinical necrotic enteritis in broiler chicken flocks. British Poultry Science. 52:359-367.
Pearlin BV, Muthuvel S, Govidasamy P, Villavan M, Alagawany M, Ragab Farag M, Dhama K, Gopi M. 2020. Role of acidifiers in livestock nutrition and health: A review. Journal of Animal Physiology and Animal Nutrition.104:558-569.
Ravindran V, Abdollahi M, Bootwalla S. 2014. Nutrient analysis, metabolizable energy, and digestible amino acids of soybean meals of different origins for broilers. Poultry Science. 93:2567-2577.
Röhe I, Boroojeni FG, Zentek J. 2017. Effect of feeding soybean meal and differently processed peas on intestinal morphology and functional glucose transport in the small intestine of broilers. Poultry Science. 96:4075-4084.
Roofchaei A, Rezaeipour V, Vatandour S, Zaefarian F. 2019. Influence of dietary carbohydrases, individually or in combination with phytase or an acidifier, on performance, gut morphology and microbial population in broiler chickens fed a wheat-based diet. Animal Nutrition. 5:63-67.
Sakamoto K, Hirose H, Onizuka A, Hayashi M, Futamura N, Kawamura Y, Ezaki T. 2000. Quantitative study of changes in intestinal morphology and mucus gel on total parenteral nutrition in rats. The Journal of Surgical Research. 94:99-106.
Salavati ME, Rezaeipour V, Abdullahpour R, Mousavi N. 2020. Effects of graded inclusion of bioactive peptides derived from sesame meal on the growth performance, internal organs, gut microbiota and intestinal morphology of broiler chickens. International Journal of Peptide Research and Therapeutics. 26:1541-1548.
Sano K, Ogawa H. 2014. Hemagglutination (inhibition) assay. In: Lectins. Methods of Molecular Biology. 1200: 47–52.
SAS. 2001. SAS®/STAT Software, Release 5. SAS Institute, Inc., Cary, NC. USA.
Seifi M, Rezaei M, Teimouri Yansari A. 2018. Effect of different levels of soybean meal peptides on performance, intestinal morphology and intestinal bacterial population in broiler chicks. Research on Animal Production (Scientific and Research). 9:9-17.
Smith C, Van Megen W, Twaalfhoven L, Hitchcock C. 1980. The determination of trypsin inhibitor levels in foodstuffs. Journal of the Science of Food and Agriculture. 31:341-350.
Somogyi M. 1960. Modifications of two methods for the assay of amylase. Clinical Chemistry. 6:23-35.
Soumeh E, Mohebodini H, Toghyani M, Shabani A, Ashayerizadeh A, Jazi V. 2019. Synergistic effects of fermented soybean meal and mannan-oligosaccharide on growth performance, digestive functions, and hepatic gene expression in broiler chickens. Poultry Science. 98: 6797-6807.
Su L-W, Cheng Y-H, Hsiao FS-H, Han J-C, Yu Y-H. 2018. Optimization of mixed solid-state fermentation of soybean meal by Lactobacillus species and Clostridium butyricum. Polish journal of Microbiology. 67: 297.
Teirlynck E, Bjerrum L, Eeckhaut V, Huygebaert G, Pasmans F, Haesebrouck F, Dewulf J, Ducatelle R, Van Immerseel F. 2009. The cereal type in feed influences gut wall morphology and intestinal immune cell infiltration in broiler chickens. British Journal of Nutrition. 102:1453-1461.
Tietz N, Fiereck EA. 1966. A specific method for serum lipase determination. Clinica Chimica Acta. 13: 352-358.
Trzcinski AP, Stuckey DC. 2015. Contribution of acetic acid to the hydrolysis of lignocellulosic biomass under abiotic conditions. Bioresource Technology. 185: 441-444.
Wang J, Liu N, Song M, Qin C, Ma C. 2011. Effect of enzymolytic soybean meal on growth performance, nutrient digestibility and immune function of growing broilers. Animal Feed Science and Technology. 169: 224-229.
Yuan B, Ren J, Zhao M, Luo D, Gu L. 2012. Effects of limited enzymatic hydrolysis with pepsin and high-pressure homogenization on the functional properties of soybean protein isolate. LWT-Food Science and Technology. 46: 453-459.
Zhang Y, Yang R, Zhang W, Hu Z, Zhao W. 2017. Structural characterization and physicochemical properties of protein extracted from soybean meal assisted by steam flash-explosion with dilute acid soaking. Food Chemistry. 219: 48-53.
Zhao M, Xin P, Zhao Q, Chen N, Cai M. 2014. Structural variations in the subunits of peanut protein isolates under acidic conditions. Modern Food Science and Technology. 30: 37-42.
Zheng L, Li D, Li ZL, Kang LN, Jiang YY, Liu XY, Chi YP, Li YQ, Wang JH. 2017. Effects of Bacillus fermentation on the protein microstructure and anti-nutritional factors of soybean meal. Letters in Applied Microbiology. 65: 520-526.
Author information
Authors and Affiliations
Contributions
All authors contributed to the research conception and plan. Data collection was performed by M. Norozi. Data analysis and manuscript preparation were performed by M. Norozi, M. Rezaei, and M. Kazemifard. All authors edited, read, and approved the final draft manuscript.
Corresponding author
Ethics declarations
Ethical approval
All animal protocols for this study were approved by the Animal Care and Use Committee at the Department of Animal Science, Faculty of Animal Science and Fisheries, Sari Agricultural Sciences and Natural Resources University.
Consent to participate
Not applicable.
Consent for publication
All authors give consent for publication.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Norozi, M., Rezaei, M. & Kazemifard, M. Effects of acid-hydrolyzed soybean meal on growth performance, jejunal morphology, digestive enzyme activities, nutrient utilization, and intestinal microbial population in broiler chickens. Trop Anim Health Prod 54, 162 (2022). https://doi.org/10.1007/s11250-022-03167-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-022-03167-x