DOI QR코드

DOI QR Code

Comparative effects of replacing soybean meal in feeds with processed soybean meal on intestinal health and growth of nursery pigs when fed pharmacological level of zinc

  • Lan Zheng (Department of Animal Science, North Carolina State University) ;
  • Jung Yeol Sung (Department of Animal Science, North Carolina State University) ;
  • Sung Woo Kim (Department of Animal Science, North Carolina State University)
  • 투고 : 2024.11.05
  • 심사 : 2025.01.20
  • 발행 : 2025.08.01

초록

Objective: The objective was to evaluate the effects of partially replacing soybean meal (SBM) in nursery pig diets with enzyme-treated soybean meal (ESBM), fermented soybean meal (FSBM), or fermented soybean meal containing probiotic microorganism (PFSBM) on jejunal mucosa-associated microbiota, immune responses, intestinal morphology, and growth performance of nursery pigs. Methods: Forty-eight weaned pigs (initial body weight = 7.8 ± 0.7 kg) were randomly allocated to four dietary treatments in a randomized complete block design and fed for 25 d in three phases (5, 10, and 12 d, respectively). Dietary treatments were corn-SBM-based diet (SBM diet) and the SBM diet in which 70 g/kg of SBM was replaced with ESBM (ESBM diet), FSBM (FSBM diet), or PFSBM (PFSBM diet). Zinc oxide was supplemented at 2.5 g/kg (2,000 mg/kg of zinc) in the experimental diets for phases 1 and 2. Pigs were housed individually in pens (1.50 m×0.74 m) equipped with a feeder and a nipple drinker. Serum was collected on d 24 and pigs were euthanized on d 27 to collect tissues and mucosa in the jejunum. Results: The PFSBM diet increased (p<0.05) the relative abundance of Lactobacillus, whereas it tended to decrease (p = 0.072) the abundance of Pseudomonas compared with the SBM diet. The ESBM diet increased (p<0.05) gain to feed ratio from d 5 to 15 compared with the SBM diet. However, partially replacing SBM at 70 g/kg with ESBM, FSBM, or PFSBM did not affect immune responses in serum and jejunal mucosa, intestinal morphology in the jejunum, and overall growth performance of nursery pigs. Conclusion: Partially replacing SBM with various processed SBM did not affect immune responses, intestinal morphology, and overall growth performance when diets were supplemented with zinc at pharmacological level in early phases.

키워드

과제정보

Technical supports from all members of the Kim Lab in animal handling, sampling, and lab analysis.

참고문헌

  1. Deng Z, Kim SW. Opportunities and challenges of soy proteins with different processing applications. Antioxidants 2024;13:569. https://doi.org/10.3390/antiox13050569
  2. Akhtar N, Cai HY, Kiarie EG, Li J. A novel Bacillus sp. with rapid growth property and high enzyme activity that allows efficient fermentation of soybean meal for improving digestibility in growing pigs. J Appl Microbiol 2022;133:3-17. https://doi.org/10.1111/jam.15268
  3. Shang QH, Ma XK, Li M, Zhang LH, Hu JX, Piao XS. Effects of α-galactosidase supplementation on nutrient digestibility, growth performance, intestinal morphology and digestive enzyme activities in weaned piglets. Anim Feed Sci Technol 2018;236:48-56. https://doi.org/10.1016/j.anifeedsci.2017.11.008
  4. Taliercio E, Loveless TM, Turano MJ, Kim SW. Identification of epitopes of the β subunit of soybean β-conglycinin that are antigenic in pigs, dogs, rabbits and fish. J Sci Food Agric 2014;94:2289-94. https://doi.org/10.1002/jsfa.6556
  5. Li DF, Nelssen JL, Reddy PG, et al. Transient hypersensitivity to soybean meal in the early-weaned pig. J Anim Sci 1990;68:1790-9. https://doi.org/10.2527/1990.6861790x
  6. Taliercio E, Kim SW. Epitopes from two soybean glycinin subunits are antigenic in pigs. J Sci Food Agric 2013;93:2927-32. https://doi.org/10.1002/jsfa.6113
  7. Zheng L, Duarte ME, Sevarolli Loftus A, Kim SW. Intestinal health of pigs upon weaning: challenges and nutritional intervention. Front Vet Sci 2021;8:628258. https://doi.org/10.3389/fvets.2021.628258
  8. Duarte ME, Kim SW. Significance of mucosa-associated microbiota and its impacts on intestinal health of pigs challenged with F18+ E. coli. Pathogens 2022;11:589. https://doi.org/10.3390/pathogens11050589
  9. Kim SW, Less JF, Wang L, et al. Meeting global feed protein demand: challenge, opportunity, and strategy. Annu Rev Anim Biosci 2019;7:221-43. https://doi.org/10.1146/annurevanimal-030117-014838
  10. Deng Z, Duarte ME, Kim SY, Hwang Y, Kim SW. Comparative effects of soy protein concentrate, enzyme-treated soybean meal, and fermented soybean meal replacing animal protein supplements in feeds on growth performance and intestinal health of nursery pigs. J Anim Sci Biotechnol 2023;14:89. https://doi.org/10.1186/s40104-023-00888-3
  11. Kim SW. Bio-fermentation technology to improve efficiency of swine nutrition. Asian-Australas J Anim Sci 2010;23:825-32. https://doi.org/10.5713/ajas.2010.r.02
  12. Cervantes-Pahm SK, Stein HH. Ileal digestibility of amino acids in conventional, fermented, and enzyme-treated soybean meal and in soy protein isolate, fish meal, and casein fed to weanling pigs. J Anim Sci 2010;88:2674-83. https://doi.org/10.2527/jas.2009-2677
  13. Hong KJ, Lee CH, Kim SW. Aspergillus oryzae GB-107 fermentation improves nutritional quality of food soybeans and feed soybean meals. J Med Food 2004;7:430-5. https://doi.org/10.1089/jmf.2004.7.430
  14. Kim SW, van Heugten E, Ji F, Lee CH, Mateo RD. Fermented soybean meal as a vegetable protein source for nursery pigs: I. effects on growth performance of nursery pigs. J Anim Sci 2010;88:214-24. https://doi.org/10.2527/jas.2009-1993
  15. Yun JH, Kwon IK, Lohakare JD, et al. Comparative efficacy of plant and animal protein sources on the growth performance, nutrient digestibility, morphology and caecal microbiology of early-weaned pigs. Asian-Australas J Anim Sci 2005;18:1285-93. https://doi.org/10.5713/ajas.2005.1285
  16. Ma X, Shang Q, Hu J, Liu H, Brøkner C, Piao X. Effects of replacing soybean meal, soy protein concentrate, fermented soybean meal or fish meal with enzyme-treated soybean meal on growth performance, nutrient digestibility, antioxidant capacity, immunity and intestinal morphology in weaned pigs. Livest Sci 2019;225:39-46. https://doi.org/10.1016/j.livsci.2019.04.016
  17. Roh SG, Carroll JA, Kim SW. Effects of fermented soybean meal on innate immunity-related gene expressions in nursery pigs acutely challenged with lipopolysaccharides. Anim Sci J 2015;86:508-16. https://doi.org/10.1111/asj.12319
  18. Sales J. Effects of pharmacological concentrations of dietary zinc oxide on growth of post-weaning pigs: a meta-analysis. Biol Trace Elem Res 2013;152:343-9. https://doi.org/10.1007/s12011-013-9638-3
  19. European Union. Commission implementing regulation (EU) 2016/1095 of 6 july 2016. Off J Eur Union L182 2016;59:7-27.
  20. Burrough ER, De Mille C, Gabler NK. Zinc overload in weaned pigs: tissue accumulation, pathology, and growth impacts. Vet Diagn Invest 2019;31:537-45. https://doi.org/10.1177/1040638719852144
  21. Schuck P, Perugini MA, Gonzales NR, Howlett GJ, Schubert D. Size-distribution analysis of proteins by analytical ultracentri-fugation: strategies and application to model systems. Bio-phys 3 2002;82:1096-111. https://doi.org/10.1016/S0006-3495(02)75469-6
  22. Knapp U, Tsai TC, Knapp J, et al. PSVI-18 establishing ideal inclusion rate of fermented soybean meal (FSBM) in nursery rations. 18 Anim Sci 2019;97:210-1. https://doi.org/10.1093/jas/skz122.370
  23. National Research Council (NRC). Nutrient requirements of swine. 11th rev. ed. National Academies Press; 2012.
  24. Jang KB, Kim SW. Supplemental effects of dietary nucleotides on intestinal health and growth performance of newly weaned pigs. J Anim Sci 2019;97:4875-82. https://doi.org/10.1093/jas/skz334
  25. Association of Official Analytical Chemists (AOAC) International. Official methods of analysis of AOAC International. 18th ed. AOAC; 2019.
  26. Sun Y, Park I, Guo J, Weaver AC, Kim SW. Impacts of low level aflatoxin in feed and the use of modified yeast cell wall extract on growth and health of nursery pigs. Anim Nutr 2015;1:177-83. https://doi.org/10.1016/j.aninu.2015.08.012
  27. Chen H, Zhang S, Park I, Kim SW. Impacts of energy feeds and supplemental protease on growth performance, nutrient digestibility, and gut health of pigs from 18 to 45 kg body weight. Anim Nutr 2017;3:359-65. https://doi.org/10.1016/j.aninu.2017.09.005
  28. Aaron DK, Hays VW. How many pigs? Statistical power considerations in swine nutrition experiments. J Anim Sci 2004; 82:E245-54. https://doi.org/10.2527/2004.8213_supplE245x
  29. Donadelli RA, Aldrich CG, Jones CK, Beyer RS. The amino acid composition and protein quality of various egg, poultry meal by-products, and vegetable proteins used in the production of dog and cat diets. Poult Sci 2019;98:1371-8. https://doi.org/10.3382/ps/pey462
  30. Sung JY, Park CS, Ragland D, Caroline González-Vega J, Wiltafsky-Martin MK, Adeola O. Autoclaving time-related reduction in amino acid digestibility of poultry meal in broiler chickens and growing pigs. J Anim Sci 2024:skad415. https://doi.org/10.1093/jas/skad415
  31. Kerr BJ, Urriola PE, Jha R, Thomson JE, Curry SM, Shurson GC. Amino acid composition and digestible amino acid con- tent in animal protein by-product meals fed to growing pigs. J Anim Sci 2019;97:4540-7. https://doi.org/10.1093/jas/skz294
  32. Balan P, Staincliffe M, Moughan PJ. Effects of spray-dried animal plasma on the growth performance of weaned piglets—a review. J Anim Physiol Anim Nutr 2021;105:699-714. https://doi.org/10.1111/jpn.13435
  33. Staswick PE, Hermodson MA, Nielsen NC. Identification of the cystines which link the acidic and basic components of the glycinin subunits. J Biol Chem 1984;25913431-5. http://doi.org/10.1016/S0021-9258(18)90712-X
  34. Thanh VH, Shibasaki K. Beta-conglycinin from soybean proteins. Isolation and immunological and physicochemical properties of the monomeric forms. Biochim Biophys Acta Protein Struct 1977;490:370-84. https://doi.org/10.1016/0005-2795(77)90012-5
  35. Lei X, Piao X, Ru Y, Zhang H, Péron A, Zhang H. Effect of Bacillus amyloliquefaciens-based direct-fed microbial on performance, nutrient utilization, intestinal morphology and cecal microflora in broiler chickens. Asian-Australas J Anim Sci 2015;28:239-46. https://doi.org/10.5713/ajas.14.0330
  36. Li Y, Zhang H, Su W, et al. Effects of dietary Bacillus amyloliquefaciens supplementation on growth performance, intestinal morphology, inflammatory response, and microbiota of intra-uterine growth retarded weanling piglets. J Anim Sci Biotechnol 2018;9:22. https://doi.org/10.1186/s40104-018- 0236-2
  37. Song J, Xiao K, Ke YL, et al. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult Sci 2014;93:581-8. https://doi.org/10.3382/ps.2013-03455
  38. Ten Have GAM, Engelen MPKJ, Wolfe RR, Deutz NEP. Inhibition of jejunal protein synthesis and breakdown in Pseudomonas aeruginosa-induced sepsis pig model. Am J Physiol Gastrointest Liver Physiol 2019;316:G755-62. https://doi. org/10.1152/ajpgi.00407.2018
  39. Althouse GC, Lu KG. Bacteriospermia in extended porcine semen. Theriogenology 2005;63:573-84. https://doi.org/10.1016/j.theriogenology.2004.09.031
  40. Tang S, Xin Y, Ma Y, Xu X, Zhao S, Cao J. Screening of microbes associated with swine growth and fat deposition traits across the intestinal tract. Front Microbiol 2020;11:586776. https://doi.org/10.3389/finicb.2020.586776
  41. Mazmanian SK, Round JL, Kasper DLA microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008;453:620-5. https://doi.org/10.1038/nature07008
  42. Li XQ Zhu YH, Zhang HF, et al. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLOS ONE 2012;7:240666. https://doi.org/10.1371/journal.pone.0040666
  43. Trevisi P, Casini L, Coloretti F, Mazzoni M, Merialdi G, Bosi P. Dietary addition of Lactobacillus rhamnosus GG impairs the health of Escherichia coli F4-challenged piglets. Animal 2011;5:1354-60. https://doi.org/101017/S1751731111000462 101017/S1751731111000462
  44. Duddeck KA, Petersen TE, Adkins HJ, et al. Dose-dependent effects of supplementing a two-strain Bacillus subtilis probiotic on growth performance, blood parameters, fecal metabolites, and microbiome in nursery pigs. Animals 2023;14:109. https://doi.org/10.3390/ani14010109
  45. Chen H, Zhang S, Kim SW. Effects of supplemental xylanase on health of the small intestine in nursery pigs fed diets with corn distillers' dried grains with solubles. J Anim Sci 2020; 98:skaa185. https://doi.org/10.1093/jas/skaa185
  46. Jang KB, Kim YI, Duarte ME, Kim SW. Effects of β-mannanase supplementation on intestinal health and growth of nursery pigs. J Anim Sci 2024;102:skae052. https://doi. org/10.1093/jas/skae052
  47. Vega-Lopez MA, Telemo E, Bailey M, Stevens K, Stokes CR. Immune cell distribution in the small intestine of the pig: immunohistological evidence for an organized compartmentalization in the lamina propria. Vet Immunol Immunopathol 1993;37:49-60. https://doi.org/10.1016/0165-2427(93)90015-V
  48. Adeola 0, King DE. Developmental changes in morphometry of the small intestine and jejunalsucrase activity during the first nine weeks of postnatal growth in pigs. J Anim Sci 2006;84:112-8. https://doi.org/10.2527/2006.841112x
  49. Jun X, Anguo Z, Zhisheng W, Dawei A. Influence of glycinin and Β-conglycinin of soybean on the proliferation and immune function of suckling piglets peripheral blood mononuclear cells in in vitro culture. J Anim Plant Sci 2009;19:115-8.
  50. Sun P, Li D, Dong B, Qiao S, Ma X. Effects of soybean glycinin on performance and immune function in early weaned pigs. Arch Anim Nutr 2008;62:313-21. https://doi.org/10.1080/17450390802066419
  51. Oda S, Hirasawa H, Shiga H, Nakanishi K, Matsuda K, Naka-mua M. Sequential measurement of IL-6 blood levels in patients with systemic inflammatory response syndrome (SIRS)/sepsis. Cytokine 2005;29:169-75. https://doi.org/10.1016/j.cyto2004.10.010
  52. Hunter CA, Jones SA. IL-6 as a keystone cytokine in health and disease. Nat Immunol 2015;16:448-57. https://doi,org/10.1038/ni.3153
  53. Ruckman LA, Petry AL, Gould SA, Kerr BJ, Patience JF. The effects of enzymatically treated soybean meal on growth performance and intestinal structure, barrier integrity, inflammation, oxidative status, and volatile fatty acid production of nursery pigs. Transl Anim Sci 2020:4:txaa170. https://doi.org/10.1093/tas/txaal70
  54. Bojarski C, Weiske J, Schoneberg T, et al. The specific fates of tight junction proteins in apoptotic epithelial cells. J Cell Sci 2004;117:2097-107. https://doi.org/10.1242/jcs.01071
  55. Zhao Y, Qin GX, Sun ZW, Zhang B, Wang T. Effects of glycinin and β-conglycinin on enterocyte apoptosis, proliferation and migration of piglets. Food Agric Immunol 2010;21: 209-18. https://doi.org/10.1080/09540101003596644
  56. Liu X, Ju Y, Huang L, et al. Effects of a new fermented soya bean meal on growth performance, serum biochemistry profile, intestinal immune status and digestive enzyme activities in piglets. J Anim Physiol Anim Nutr 2022;106:1046-59. https://doi.org/10.1111/jpn.13649
  57. Yan H, Jin JQ, Yang P, et al. Fermented soybean meal increases nutrient digestibility via the improvement of intestinal function, anti-oxidative capacity and immune function of weaned pig S. animal 2022;16:100557. https://doi.org/10.1016/j.animal.2022.100557
  58. Ma XK, Shang QH, Wang QQ, Hu JX, Piao XS. Comparative effects of enzymolytic soybean meal and antibiotics in diets on growth performance, antioxidant capacity, immunity, and intestinal barrier function in weaned pigs. Anim Feed Sci Technol 2019;248:47-58. https://doi.org/101016/j.anifeedsci.2018.12.003 101016/j.anifeedsci.2018.12.003
  59. Muniyappan M, Shanmugam S, Park JH, Han K, Kim IH. Effects of fermented soybean meal supplementation on the growth performance and apparent total tract digestibility by modulating the gut microbiome of weaned piglets. Sci Rep 2023;13:3691. https://doi.org/10.1038/s41598-023-30698-6
  60. Ao X, Kim HJ, Meng QW, Yan L, Cho JH, Kim IH. Effects of diet complexity and fermented soy protein on growth performance and apparent ileal amino acid digestibility in weanling pigs. Asian-Australas J Anim Sci 2010;23:1496-502. https://doi.org/10.5713/ajas.2010.10109
  61. Wang W, Wang Y, Hao X, et al. Dietary fermented soybean meal replacement alleviates diarrhea in weaned piglets challenged with enterotoxigenic Escherichia coli K88 by modulating inflammatory cytokine levels and cecal microbiota composition. BMC Vet Res 2020;16:245. https://doi.org/10.1186/s12917-020-02466-5
  62. Wang Y, Wang W, Wang R, et al. Dietary fermented soybean meal inclusion improves growth performance and ileal barrier function of the weaned piglets challenged by enterotoxigenic Escherichia coli K88. Anim Feed Sci Technol 2020;268:114596. https://doi.org/10.1016/j.anifeessi.2020.114596
  63. Tan K, Bian Z, Liang H, et al. Enzymolytic soybean meal-impact on growth performance, nutrient digestibility, antioxidative capacity, and intestinal health of weaned piglets. Front Vet Sci 2024;11:1381823. https://doi.org/10.3389/fvets.2024.1381823
  64. Wang L, Li W, Xin S, et al. Soybean glycinin and β-conglycinin damage the intestinal barrier by triggering oxidative stress and inflammatory response in weaned piglets. Eur J Nutr 2023;62:2841-54. https://doi.org/10.1007/s00394-023-03188-8
  65. Powell SR. The antioxidant properties of zinc. J Nutr 2000;130:1447S-54S. https://doi.org/10.1093/jn/130.5.1447S
  66. Tang X, Xiong K, Zeng Y, Fang R. The mechanism of zinc oxide in alleviating diarrhea in piglets after weaning: a review from the perspective of intestinal barrier function. Int J Mol Sci 2024;25:10040. https://doi.org/10.3390/ijms251810040