Abstract

Probiotics are offered as dietary supplements in animal husbandry, and microencapsulation protects probiotic activity. Here, feed microencapsulated Enterococcus faecalis of weaned piglets on the growth performance, immune function, and cecal microbiota were investigated. A control diet (NC), a 0.05% Aureomycin (PC) diet or a microencapsulated E. faecalis–supplemented (1 × 109 cfu/kg of diet; ME) diet was fed to 90 weaned piglets for 28 days. Compared with the piglets fed the NC diet, those fed the PC and ME diets showed a significant increase (P<0.001) in final weight, ADG, and ADFI but a significant decrease in the F : G ratio (P<0.01) during the 28-day experimental period. Compared with the NC group, the PC and ME groups showed significant (P<0.05) decreases in serum TNF-α, IL-6, IL-1, IgG, IgM, and IgA concentrations. High-throughput sequencing revealed that the diet modulated cecal bacterial diversity, including an increase in Lactobacillus abundance. Thus, microencapsulated E. faecalis promotes the growth performance, immunity and optimal intestinal flora of weaned piglets.

Reference

Cao GT, Zeng XF, Chen AG, Zhou L and Zhang L et al., 2013. Effects of a probiotic, Enterococcus faecium on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poult Sci, 92(11): 2949-2955, doi: 10.3382/ps.2013-03366

Chen L, Li S, Zheng J, Li W, Jiang X et al., 2018. Effects of dietary clostridium butyricum supplementation on growth performance, intestinal development, and immune response of weaned piglets challenged with lipopolysaccharide. J Anim Sci Biotechnol, 9(1): 62, doi: 10.1186/s40104-018-0275-8

Deng B, Wu J, Li X, Men X and Xu Z, 2017. Probiotics and probiotic metabolic product improved intestinal function and ameliorated LPS-induced injury in rats. Curr Microbiol, 74(11): 1306-1315, doi: 10.1007/s00284-017-1318-7

Diraviyam T, Zhao B, Wang Y, Schade R, Michael A et al., 2014. Effect of chicken egg yolk antibodies (IgY) against diarrhea in domesticated animals: A systematic review and meta-analysis, PLoS One, 9(5): e97716, doi: 10.1371/journal.pone.0097716

Ermis E, 2021. A review of drying methods for improving the quality of probiotic powders and characterization. Drying Technol, 40(11): 1-18, doi: 10.1080/07373937.2021.1950169

Fuller R, 1991. Probiotics in human medicine. Gut, 32 (4): 439-442, doi: 10.1136/gut.32.4.439

Georgeta C, Mihaela D and Ionut S, 2020. Effect of chickpea and probiotics on broiler chicks’ performance and gut microflora populations. Anim Sci Biotechnol, 53(2): 1-7

Gerez CL, Font D, Valdez G, Gigante ML and Grosso CRF, 2012. Whey protein coating bead improves the survival of the probiotic Lactobacillus rhamnosus CRL 1505 to low pH. Lett Appl Microbiol, 54(6): 552-556, doi: 10.1111/j.1472-765X.2012.03247.x

Hemarajata P and Versalovic J, 2013. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol, 6 (1): 39-51, doi: 10.1177/1756283X12459294

Hou C, Zeng X, Yang F, Liu H and Qiao S, 2015. Study and use of the probiotic Lactobacillus reuteri in pigs: A review. J Anim. Sci Biotechnol, 6(14), doi: 10.1186/s40104-015-0014-3

Hou G, Peng W, Wei L, Li R, Huang X et al., 2021. Probiotics and Achyranthes bidentata polysaccharides improve growth performance via promoting intestinal nutrient utilization and enhancing immune function of weaned pigs. Animals, 11(9): 1-10, doi: 10.3390/ani11092617

Hu Y, Dun Y, Li S, Zhang D, Peng N et al., 2015. Dietary Enterococcus faecalis LAB31 improves growth performance, reduces diarrhea, and increases fecal Lactobacillus number of weaned piglets. PloS One, 10(1): e0116635, doi: 10.1371/journal.pone.0116635

Hulst M, Vastenhouw S, Smits M, Wit A, Niewold T et al., 2013. Transcription networks responsible for early regulation of Salmonella-induced inflammation in the jejunum of pigs. J Inflamm, 10(1): e18, doi:  10.1186/1476-9255-10-18

Humphrey B, Zhao J and Faris R, 2019. Review: Link between intestinal immunity and practical approaches to swine nutrition. Animal, 13: 2736-2744, doi: 10.1017/S1751731119001861

Ji F, Yang H, Wang Q, Li J, Zhou H et al., 2023. Porcine intestinal antimicrobial peptide as an in-feed antibiotic alternative improves intestinal digestion and immunity by shaping the gut microbiota in weaned piglets. Anim Nutr, 14: 43-55, doi: 10.1016/j.aninu.2023.04.001

Li L, Yin F, Wang X, Yang C, Yu H et al., 2023. Microencapsulation protected Lactobacillus viability and its activity in modulating the intestinal microbiota in newly weaned piglets. J Anim Sci, 101: 193, doi: 10.1093/jas/skad193

Liu C, Zhu Q, Chang J, Yin Q, Song A et al., 2017. Effects of Lactobacillus casei and Enterococcus faecalis on growth performance, immune function and gut microbiota of suckling piglets. Arch Anim Nutr, 71(2): 120-133, doi: 10.1080/1745039X.2017.1283824

Liu KY, Fang H, Cui FJ, Nyabako BA, Tao TL et al., 2020. ARTP mutation and adaptive laboratory evolution improve probiotic performance of Bacillus coagulans. Appl Microbiol Biot, 104: 6363-6373, doi: 10.1007/s00253-020-10703-y

Maykelly SG, Marcos ED, Alysson S, Leandro LO, Lucas MT et al., 2023. Effect of antibiotics and low-crude protein diets on growth performance, health, immune response, and fecal microbiota of growing pigs. J Anim Sci, 101: 362, doi: 10.1093/jas/skad362

Mo J, Lu Y, Jiang S, Yan G, Xing T et al., 2022. Effects of the probiotic, Lactobacillus delbrueckii subsp. bulgaricus, as a substitute for antibiotics on the gastrointestinal tract microbiota and metabolomics profile of female growing-finishing pigs. Animals, 12(14): 1778, doi: 10.3390/ani12141778

Pajarillo EAB, Chae JP, Balolong MP, Kim HB, Park CS et al., 2015. Effects of probiotic Enterococcus faecium, NCIMB 11181 administration on swine feces microbiota diversity and composition using barcoded pyrosequencing. Anim Feed Sci Technol, 201; 80-88, doi: 10.1016/j.anifeedsci.2015.01.011

Park JW, Jeong JS, Lee SI and Kim IH, 2016. Effect of dietary supplementation with a probiotic (Enterococcus faecium) on production performance, excreta microflora, ammonia emission, and nutrient utilization in ISA brown laying hen. Poult Sci, 95(12): 2829-2835, doi: 10.3382/ps/pew241

Peris MM, Eissa N, Bernstein CN, Khafipour E and Ghia JE, 2015. Antepartum antibiotic treatment increases offspring susceptibility to experimental colitis: A role of the gut microbiota. PLoS One, 10(11): e0142536, doi: 10.1371/journal.pone.0142536

Pupa P, Apiwatsiri P, Sirichokchatchawan W, Pirarat N, Maison T et al., 2021b. Use of Lactobacillus plantarum (strains 22F and 25F) and Pediococcus acidilactici (strain 72N) as replacements for antibiotic-growth promotants in pigs. Sci Rep, 11(1): 12028, doi: 10.1038/s41598-021-91427-5

Pupa P, Apiwatsiri P, Sirichokchatchawan W, Pirarat N, Muangsin N et al., 2021a. The efficacy of three double-microencapsulation methods for preservation of probiotic bacteria. Sci Rep, 11(1): 13753, doi: 10.1038/s41598-021-93263-z

Qi WT, Ma J, Yu WT, Xie YB, Wang W et al., 2006. Behavior of microbial growth and metabolism in alginate–chitosan–alginate (ACA) microcapsules. Enz Microb Technol, 38(5): 697-704, doi: 10.1016/j.enzmictec.2005.10.003

Salim HM, Kang HK, Akter N, Kim DW, Kim JH et al., 2013. Supplementation of direct-fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poult Sci, 92(8): 2084-2090, doi: 10.3382/ps.2012-02947

Shang Y, Kumar S, Oakley B and Kim WK, 2018. Chicken gut microbiota: importance and detection technology. Front Vet Sci, 5: 254, doi: 10.3389/fvets.2018.00254

Sichetti M, Marco S, Pagiotti R, Traina G and Pietrella D, 2018. Anti-inflammatory effect of multistrain probiotic formulation (L. rhamnosus, B. lactis, and B. longum). Nutrition, 53: 95-102, doi: 10.1016/j.nut.2018.02.005  

Szabó I, Wieler LH, Tedin K, Tedin LS, Taras D et al., 2009. Influence of a probiotic strain of Enterococcus faecium on Salmonella enterica serovar Typhimurium DE104 infection in a porcine animal infection model. Appl Environ Microb, 75: 2621-2628, doi: 10.1128/AEM.01515-08

Verstegen MWA and Williams BA, 2002. Alternatives to the use of antibiotics as growth promoters for monogastric animals. Animal Biotechnol, 13(1): 113-127, doi: 10.1081/ABIO-120005774

Vimon S, Angkanaporn K and Nuengjamnong C, 2023. Microencapsulation of Lactobacillus plantarum MB001 and its probiotic effect on growth performance, cecal microbiome and gut integrity of broiler chickens in a tropical climate. Anim Biosci, 36(8): 1252-1262, doi: 10.5713/ab.22.0426

Wang K, Cao G, Zhang H, Lia Q and Yang C, 2019. Effects of Clostridium butyricum and Enterococcus faecalis on growth performance, immune function, intestinal morphology, volatile fatty acids, and intestinal flora in a piglet model. Food Funct, 10: 7844-7854, doi: 10.1039/C9FO01650C

Wang W, Chen J, Zhou, H, Wang L, Ding S et al., 2018. Effects of microencapsulated Lactobacillus plantarum and fructooligosaccharide on growth performance, blood immune parameters, and intestinal morphology in weaned piglets. Food Agril Immunol, 29(1): 84-94, doi: 10.1080/09540105.2017.1360254

Xu X, Yang C, Chang J, Wang P and Yin Q, 2020. Dietary supplementation with compound probiotics and berberine alters piglet production performance and fecal microbiota, Animals, 10: 511, doi: 10.3390/ani10030511

Yao M, Xie J, Du H, McClements DJ, Xiao H et al., 2020. Progress in microencapsulation of probiotics: A review. Compr Rev Food Sci Food Saf, 19(2): 857-874, doi: 10.1111/1541-4337.12532

Yuan W, Jin HT, Ren ZH, Deng JL, Zuo ZC et al., 2015. Effects of antibacterial peptide on humoral immunity in weaned piglets. Food Agric Immunol, 26(5): 682-689, doi: 10.1080/09540105.2015.1007448

Zhang L, Li J, Yun TT, Qi WT, Liang XX et al., 2015. Effects of pre-encapsulated and pro-encapsulated Enterococcus faecalis on growth performance, blood characteristics, and cecal microflora in broiler chickens. Poult Sci, 94(11): 2821-2830, doi: 10.3382/ps/pev262

Zhang Q, Vasquez R, Yoo JM, Kim SH, Kang DK et al., 2022. Dietary supplementation of Limosilactobacillus mucosae LM1 enhances immune functions and modulates gut microbiota without affecting the growth performance of growing pigs. Front Vet Sci, 9: 1-12, doi: 10.3389/fvets.2022.918114

Zhang ZF and Kim IH, 2014. Effects of multistrain probiotics on growth performance, apparent ileal nutrient digestibility, blood characteristics, cecal microbial shedding, and excreta odor contents in broilers. Poult Sci, 93(2): 364-370, doi: 10.3382/ps.2013-03314

Zhaxi Y, Meng X, Wang W, Wang L, He Z et al., 2020. Duan-Nai-An, a yeast probiotic, improves intestinal mucosa integrity and immune function in weaned piglets. Sci Rep, 10: 4556, doi: 10.1038/s41598-020-61279-6