Advertisement

Journal of Zhejiang University-SCIENCE B

, Volume 20, Issue 2, pp 180–192 | Cite as

Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets

  • Yang Wang
  • Li Gong
  • Yan-ping Wu
  • Zhi-wen Cui
  • Yong-qiang Wang
  • Yi Huang
  • Xiao-ping ZhangEmail author
  • Wei-fen LiEmail author
Article

Abstract

To understand the effects of Lactobacillus rhamnosus GG (ATCC 53103) on intestinal barrier function in pre-weaning piglets under normal conditions, twenty-four newborn littermate piglets were randomly divided into two groups. Piglets in the control group were orally administered with 2 mL 0.1 g/mL sterilized skim milk while the treatment group was administered the same volume of sterilized skim milk with the addition of viable L. rhamnosus at the 1st, 3rd, and 5th days after birth. The feeding trial was conducted for 25 d. Results showed that piglets in the L. rhamnosus group exhibited increased weaning weight and average daily weight gain, whereas diarrhea incidence was decreased. The bacterial abundance and composition of cecal contents, especially Firmicutes, Bacteroidetes, and Fusobacteria, were altered by probiotic treatment. In addition, L. rhamnosus increased the jejunal permeability and promoted the immunologic barrier through regulating antimicrobial peptides, cytokines, and chemokines via Toll-like receptors. Our findings indicate that oral administration of L. rhamnosus GG to newborn piglets is beneficial for intestinal health of pre-weaning piglets by improving the biological, physical, and immunologic barriers of intestinal mucosa.

Key words

Lactobacillus rhamnosus Gut microbiota Intestinal physical barrier Intestinal immunological barrier Piglet 

口服鼠李糖乳杆菌 GG 影响哺乳仔猪肠道屏障功能的研究

概 要

目 的

探究新生仔猪口服鼠李糖乳杆菌 GG 对肠道屏障功能的影响。

创新点

新生仔猪早期口服鼠李糖乳杆菌 GG 可明显改善其断奶前肠道菌群结构及免疫屏障功能。

方 法

二十四头新生仔猪分为对照组和实验组: 对照组仔猪在出生后第 1、 3、 5 天口服 2 mL 0.1 g/mL 的脱脂牛奶; 而实验组仔猪口服等体积的含有活鼠李糖乳杆菌 GG 的脱脂牛奶。 饲喂 25 天后, 收集仔猪血清、 肠道粘膜和盲肠内容物等样品。 通过分析肠道菌群、 紧密连接蛋白和细胞因子等指标, 评价鼠李糖乳杆菌对肠道屏障功能的影响。

结 论

在正常生理条件下, 新生仔猪口服鼠李糖乳杆菌 GG 可明显改变肠道菌群结构。 此外, 鼠李糖乳杆菌 GG 还可增加仔猪肠道的通透性, 并通过调控抗菌肽、 细胞因子和趋化因子的分泌以改善肠道的免疫屏障功能。

关键词

鼠李糖乳杆菌 肠道菌群 肠道物理屏障 肠道免疫屏障 仔猪 

CLC number

S816.3 

Supplementary material

11585_2019_331_MOESM1_ESM.pdf (211 kb)
Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets

References

  1. Allen-Vercoe E, Strauss J, Chadee K, 2011. Fusobacterium nucleatum: an emerging gut pathogen? Gut Microbes, 2(5):294–298. https://doi.org/10.4161/gmic.2.5.18603CrossRefGoogle Scholar
  2. Angelakis E, Raoult D, 2010. The increase of Lactobacillus species in the gut flora of newborn broiler chicks and ducks is associated with weight gain. PLoS ONE, 5(5): e10463. https://doi.org/10.1371/journal.pone.0010463CrossRefGoogle Scholar
  3. Ayala L, Bocourt R, Castro M, et al., 2015. Effect of the probiotic additive Bacillus subtilis and their endospores on milk production and immune response of lactating sows. Cuban J Agric Sci, 49(1):71–74.Google Scholar
  4. Balcázar JL, de Blas I, Ruiz-Zarzuela I, et al., 2007. Changes in intestinal microbiota and humoral immune response following probiotic administration in brown trout (Salmo trutta). Br J Nutr, 97(3):522–527. https://doi.org/10.1017/S0007114507432986CrossRefGoogle Scholar
  5. Bauer E, Williams BA, Smidt H, et al., 2006. Influence of the gastrointestinal microbiota on development of the immune system in young animals. Curr Issues Intest Microbiol, 7(2):35–51.Google Scholar
  6. Bocourt R, Savon L, Diaz J, et al., 2004a. Effect of the probiotic activity of Lactobacillus rhamnosus on productive and health indicators of piglets. Cuban J Agric Sci, 38(1): 75–79.Google Scholar
  7. Bocourt R, Savon L, Diaz J, 2004b. Effect of the probiotic activity of Lactobacillus rhamnosus on physiological indicators of suckling pigs. Cuban J Agric Sci, 38(4): 403–408.Google Scholar
  8. Brundel BJJM, van Gelder IC, Henning RH et al., 2001. Alterations in potassium channel gene expression in atria of patients with persistent and paroxysmal atrial fibrillation: differential regulation of protein and mRNA levels for K+ channels. J Am Coll Cardiol, 37(3):926–932. https://doi.org/10.1016/S0735-1097(00)01195-5CrossRefGoogle Scholar
  9. Callewaert L, Michiels CW, 2010. Lysozymes in the animal kingdom. J Biosci, 35(1):127–160. https://doi.org/10.1007/s12038-010-0015-5CrossRefGoogle Scholar
  10. Cammarota M, de Rosa M, Stellavato A, et al., 2009. In vitro evaluation of Lactobacillus plantarum DSMZ 12028 as a probiotic: emphasis on innate immunity. Int J Food Microbiol, 135(2):90–98. https://doi.org/10.1016/j.ijfoodmicro.2009.08.022CrossRefGoogle Scholar
  11. Casserly C, Erijman L, 2003. Molecular monitoring of microbial diversity in an UASB reactor. Int Biodeterior Biodegrad, 52(1):7–12. https://doi.org/10.1016/S0964-8305(02)00094-XCrossRefGoogle Scholar
  12. Chen RC, Xu LM, Du SJ, et al., 2016. Lactobacillus rhamnosus GG supernatant promotes intestinal barrier function, balances Treg and TH17 cells and ameliorates hepatic injury in a mouse model of chronic-binge alcohol feeding. Toxicol Lett, 241:103–110. https://doi.org/10.1016/j.toxlet.2015.11.019CrossRefGoogle Scholar
  13. Cushing SD, Berliner JA, Valente AJ, et al., 1990. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci USA, 87(13): 5134–5138. https://doi.org/10.1073/pnas.87.13.5134CrossRefGoogle Scholar
  14. Deng J, Li YF, Zhang JH, et al., 2013. Co-administration of Bacillus subtilis RJGP16 and Lactobacillus salivarius B1 strongly enhances the intestinal mucosal immunity of piglets. Res Vet Sci, 94(1):62–68. https://doi.org/10.1016/j.rvsc.2012.07.025CrossRefGoogle Scholar
  15. Deshmane SL, Kremlev S, Amini S, et al., 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interf Cytok Res, 29(6):313–326. https://doi.org/10.1089/jir.2008.0027CrossRefGoogle Scholar
  16. Dogi CA, Weill F, Perdigón G, 2010. Immune response of non-pathogenic Gram(+) and Gram(-) bacteria in inductive sites of the intestinal mucosa: study of the pathway of signaling involved. Immunobiology, 215(1):60–69. https://doi.org/10.1016/j.imbio.2009.01.005CrossRefGoogle Scholar
  17. Duerkop BA, Vaishnava S, Hooper LV, 2009. Immune responses to the microbiota at the intestinal mucosal surface. Immunity, 31(3):368–376. https://doi.org/10.1016/j.immuni.2009.08.009CrossRefGoogle Scholar
  18. Eckburg PB, Bik EM, Bernstein CN, et al., 2005. Diversity of the human intestinal microbial flora. Science, 308(5728): 1635–1638. https://doi.org/10.1126/science.1110591CrossRefGoogle Scholar
  19. Flint HJ, Scott KP, Louis P, et al., 2012. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol, 9(10):577–589. https://doi.org/10.1038/nrgastro.2012.156CrossRefGoogle Scholar
  20. Galdeano CM, Perdigón G, 2006. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol, 13(2):219–226. https://doi.org/10.1128/CVI.13.2.219-226.2006CrossRefGoogle Scholar
  21. Gareau MG, Sherman PM, Walker WA, 2010. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol, 7(9):503–514. https://doi.org/10.1038/nrgastro.2010.117CrossRefGoogle Scholar
  22. Gaskins HR, Croix JA, Nakamura N, et al., 2008. Impact of the intestinal microbiota on the development of mucosal defense. Clin Infect Dis, 46(S2):S80–S86. https://doi.org/10.1086/523336CrossRefGoogle Scholar
  23. Gmür R, Munson MA, Wade WG, 2006. Genotypic and phenotypic characterization of Fusobacteria from Chinese and European patients with inflammatory periodontal diseases. Syst Appl Microbiol, 29(2):120–130. https://doi.org/10.1016/j.syapm.2005.07.011CrossRefGoogle Scholar
  24. Goede D, Morrison R, 2015. Production impact study update. Swine Health Monitoring Project 08/01/2014. University of Minnesota. http://www.cvm.umn.edu/sdec/SwineDiseases/ pedv/SHMP_14/index.htm [Accessed on July 5, 2015]Google Scholar
  25. Guarino A, Lo Vecchio A, Canani RB, 2009. Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol, 25(1):18–23. https://doi.org/10.1097/MOG.0b013e32831b4455CrossRefGoogle Scholar
  26. Guarner F, Malagelada JR, 2003. Gut flora in health and disease. Lancet, 361(9356):512–519. https://doi.org/10.1016/S0140-6736(03)12489-0CrossRefGoogle Scholar
  27. Guo Y, Xiao P, Lei S, et al., 2008. How is mRNA expression predictive for protein expression? A correlation study on human circulating monocytes. Acta Biochim Biophys Sin, 40(5):426–436. https://doi.org/10.1111/j.1745-7270.2008.00418.xCrossRefGoogle Scholar
  28. Haakensen M, Dobson CM, Deneer H, et al., 2008. Real-time PCR detection of bacteria belonging to the Firmicutes Phylum. Int J Food Microbiol, 125(3):236–241. https://doi.org/10.1016/j.ijfoodmicro.2008.04.002CrossRefGoogle Scholar
  29. Han D, Walsh M, Choi Y, et al., 2015. TRAF6 expression in dendritic cells is essential for tolerance to dietary antigens (MUC8P.723). J Immunol, 194(1S):204.3.Google Scholar
  30. Hanke D, Jenckel M, Petrov A, et al., 2015. Comparison of porcine epidemic diarrhea viruses from Germany and the United States, 2014. Emerg Infect Dis, 21(3):493–496. https://doi.org/10.3201/eid2103.141165CrossRefGoogle Scholar
  31. Hayakawa T, Masuda T, Kurosawa D, et al., 2016. Dietary administration of probiotics to sows and/or their neonates improves the reproductive performance, incidence of post-weaning diarrhea and histopathological parameters in the intestine of weaned piglets. Anim Sci J, 87(12): 1501–1510. https://doi.org/10.1111/asj.12565CrossRefGoogle Scholar
  32. Hermann-Bank ML, Skovgaard K, Stockmarr A, et al., 2015. Characterization of the bacterial gut microbiota of piglets suffering from new neonatal porcine diarrhoea. BMC Vet Res, 11:139. https://doi.org/10.1186/S12917-015-0419-4CrossRefGoogle Scholar
  33. Hooper LV, 2004. Bacterial contributions to mammalian gut development. Trends Microbiol, 12(3):129–134. https://doi.org/10.1016/J.Tim.2004.01.001CrossRefGoogle Scholar
  34. Hou CL, Liu H, Zhang J, et al., 2015. Intestinal microbiota succession and immunomodulatory consequences after introduction of Lactobacillus reuteri I5007 in neonatal piglets. PLoS ONE, 10(3):e0119505. https://doi.org/10.1371/journal.pone.0119505CrossRefGoogle Scholar
  35. Kagnoff MF, Eckmann L, 1997. Epithelial cells as sensors for microbial infection. J Clin Invest, 100(1):6–10. https://doi.org/10.1172/Jci119522CrossRefGoogle Scholar
  36. Kelly JR, Kennedy PJ, Cryan JF, et al., 2015. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci, 9:392. https://doi.org/10.3389/Fncel.2015.00392Google Scholar
  37. Kemper N, 2008. Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic, 8(1):1–13. https://doi.org/10.1016/j.ecolind.2007.06.002CrossRefGoogle Scholar
  38. Klinge L, Vester U, Schaper J, et al., 2002. Severe Fusobacteria infections (Lemierre syndrome) in two boys. Eur J Pediatr, 161(11):616–618. https://doi.org/10.1007/s00431-002-1026-5CrossRefGoogle Scholar
  39. Koenig JE, Spor A, Scalfone N, et al., 2011. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA, 108(S1):4578–4585. https://doi.org/10.1073/pnas.1000081107CrossRefGoogle Scholar
  40. Lan JG, Cruickshank SM, Singh JC, et al., 2005. Different cytokine response of primary colonic epithelial cells to commensal bacteria. World J Gastroenterol, 11(22):3375–3384. https://doi.org/10.3748/wjg.v11.i22.3375CrossRefGoogle Scholar
  41. Lei K, Li YL, Yu DY, et al., 2013. Influence of dietary inclusion of Bacillus licheniformis on laying performance, egg quality, antioxidant enzyme activities, and intestinal barrier function of laying hens. Poult Sci, 92(9):2389–2395. https://doi.org/10.3382/ps.2012-02686CrossRefGoogle Scholar
  42. Ley RE, Hamady M, Lozupone C, et al., 2008. Evolution of mammals and their gut microbes. Science, 320(5883): 1647–1651. https://doi.org/10.1126/science.1155725CrossRefGoogle Scholar
  43. Li WF, Huang Y, Li YL, et al., 2012. Effect of oral administration of Enterococcus faecium Ef1 on innate immunity of sucking piglets. Pak Vet J, 33(1):9–13.Google Scholar
  44. Liu FN, Li GH, Wen K, et al., 2013. Lactobacillus rhamnosus GG on rotavirus-induced injury of ileal epithelium in gnotobiotic pigs. J Pediatr Gastroenterol Nutr, 57(6): 750–758. https://doi.org/10.1097/MPG.0b013e3182a356e1CrossRefGoogle Scholar
  45. Lozupone CA, Stombaugh JI, Gordon JI, et al., 2012. Diversity, stability and resilience of the human gut microbiota. Nature, 489(7415):220–230. https://doi.org/10.1038/nature11550CrossRefGoogle Scholar
  46. Mackie RI, Sghir A, Gaskins HR, 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr, 69(5):1035S-1045S. https://doi.org/10.1093/ajcn/69.5.1035sCrossRefGoogle Scholar
  47. Mao XB, Gu CS, Hu HY, et al., 2016. Dietary Lactobacillus rhamnosus GG supplementation improves the mucosal barrier function in the intestine of weaned piglets challenged by porcine rotavirus. PLoS ONE, 11(1):e0146312. https://doi.org/10.1371/journal.pone.0146312CrossRefGoogle Scholar
  48. Mazmanian SK, Liu CH, Tzianabos AO, et al., 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell, 122(1): 107–118. https://doi.org/10.1016/j.cell.2005.05.007CrossRefGoogle Scholar
  49. McCracken VJ, Lorenz RG, 2001. The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol, 3(1):1–11. https://doi.org/10.1046/J.1462-5822.2001.00090.XCrossRefGoogle Scholar
  50. Meijerink M, van Hemert S, Taverne N, et al., 2010. Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS ONE, 5(5): e10632. https://doi.org/10.1371/journal.pone.0010632CrossRefGoogle Scholar
  51. Meijerink M, Wells JM, Taverne N, et al., 2012. Immunomodulatory effects of potential probiotics in a mouse peanut sensitization model. FEMS Immunol Med Microbiol, 65(3):488–496. https://doi.org/10.1111/j.1574-695X.2012.00981.xCrossRefGoogle Scholar
  52. Meng Y, Zhang Y, Liu M, et al., 2016. Evaluating intestinal permeability by measuring plasma endotoxin and diamine oxidase in children with acute lymphoblastic leukemia treated with high-dose methotrexate. Anticancer Agents Med Chem, 16(3):387–392. https://doi.org/10.2174/1871520615666150812125955CrossRefGoogle Scholar
  53. Mennigen R, Nolte K, Rijcken E, et al., 2009. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol, 296(5):G1140–G1149. https://doi.org/10.1152/ajpgi.90534.2008CrossRefGoogle Scholar
  54. Nalle SC, Turner JR, 2015. Intestinal barrier loss as a critical pathogenic link between inflammatory bowel disease and graft-versus-host disease. Mucosal Immunol, 8(4):720–730. https://doi.org/10.1038/mi.2015.40CrossRefGoogle Scholar
  55. National Research Council, 1998. Nutrient Requirements of Swine, 10th Ed. The National Academies Press, Washington, DC, USA. https://doi.org/10.17226/6016Google Scholar
  56. Natividad JMM, Verdu EF, 2013. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res, 69(1):42–51. https://doi.org/10.1016/j.phrs.2012.10.007CrossRefGoogle Scholar
  57. Ngamwongsatit B, Tanomsridachchai W, Suthienkul O, et al., 2016. Multidrug resistance in Clostridium perfringens isolated from diarrheal neonatal piglets in Thailand. Anaerobe, 38:88–93. https://doi.org/10.1016/j.anaerobe.2015.12.012CrossRefGoogle Scholar
  58. Patil AK, Kumar S, Verma AK, et al., 2015. Probiotics as feed additives in weaned pigs: a review. Livest Res Int, 3: 31–39.Google Scholar
  59. Rajput IR, Li LY, Xin X, et al., 2013. Effect of Saccharomyces boulardii and Bacillus subtilis B10 on intestinal ultrastructure modulation and mucosal immunity development mechanism in broiler chickens. Poult Sci, 92(4):956–965. https://doi.org/10.3382/ps.2012-02845CrossRefGoogle Scholar
  60. Rakoff-Nahoum S, Medzhitov R, 2008. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol, 1(1):S10–S14. https://doi.org/10.1038/mi.2008.49CrossRefGoogle Scholar
  61. Rescigno M, 2011. The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol, 32(6):256–264. https://doi.org/10.1016/j.it.2011.04.003CrossRefGoogle Scholar
  62. Rumbo M, Anderle P, Didierlaurent A, et al., 2004. How the gut links innate and adaptive immunity. Ann N Y Acad Sci, 1029:16–21. https://doi.org/10.1196/annals.1309.003CrossRefGoogle Scholar
  63. Salyers AA, 1984. Bacteroides of the human lower intestinal tract. Annu Rev Microbiol, 38:293–313. https://doi.org/10.1146/Annurev.Mi.38.100184.001453CrossRefGoogle Scholar
  64. Shim SB, Verstegen MWA, Kim IH, et al., 2005. Effects of feeding antibiotic-free creep feed supplemented with oligofructose, probiotics or synbiotics to suckling piglets increases the preweaning weight gain and composition of intestinal microbiota. Arch Anim Nutr, 59(6):419–427. https://doi.org/10.1080/17450390500353234CrossRefGoogle Scholar
  65. Standiford TJ, Kunkel SL, Phan SH, et al., 1991. Alveolar macrophage-derived cytokines induce monocyte chemoattractant protein-1 expression from human pulmonary type II-like epithelial cells. J Biol Chem, 266(15):9912–9918.Google Scholar
  66. Stappenbeck TS, Hooper LV, Gordon JI, 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA, 99(24):15451–15455. https://doi.org/10.1073/pnas.202604299CrossRefGoogle Scholar
  67. Sun RQ, Cai RJ, Chen YQ, et al., 2012. Outbreak of porcine epidemic diarrhea in suckling piglets, China. Emerg Infect Dis, 18(1):161–163. https://doi.org/10.3201/eid1801.111259CrossRefGoogle Scholar
  68. Sun YJ, Cao HJ, Jin Q, et al., 2011. Effects of penehyclidine hydrochloride on rat intestinal barrier function during cardiopulmonary bypass. World J Gastroenterol, 17(16): 2137–2142. https://doi.org/10.3748/wjg.v17.i16.2137CrossRefGoogle Scholar
  69. Swank GM, Deitch EA, 1996. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg, 20(4):411–417. https://doi.org/10.1007/s002689900065CrossRefGoogle Scholar
  70. Tannock GW, 2001. Molecular assessment of intestinal microflora. Am J Clin Nutr, 73(2):410S-414S. https://doi.org/10.1093/ajcn/73.2.410sCrossRefGoogle Scholar
  71. Taras D, Vahjen W, Macha M, et al., 2006. Performance, diarrhea incidence, and occurrence of Escherichia coli virulence genes during long-term administration of a probiotic Enterococcus faecium strain to sows and piglets. J Anim Sci, 84(3):608–617. https://doi.org/10.2527/2006.843608xCrossRefGoogle Scholar
  72. Theuns S, Conceição-Neto N, Christiaens I, et al., 2015. Complete genome sequence of a porcine epidemic diarrhea virus from a novel outbreak in Belgium, January 2015. Genome Announc, 3(3):e00506–15. https://doi.org/10.1128/genomeA.00506-15CrossRefGoogle Scholar
  73. Toledo A, Gómez D, Cruz C, et al., 2012. Prevalence of virulence genes in Escherichia coli strains isolated from piglets in the suckling and weaning period in Mexico. J Med Microbiol, 61(1):148–156. https://doi.org/10.1099/jmm.0.031302-0CrossRefGoogle Scholar
  74. Turner JR, 2009. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol, 9(11):799–809. https://doi.org/10.1038/nri2653CrossRefGoogle Scholar
  75. Ukena SN, Westendorf AM, Hansen W, et al., 2005. The host response to the probiotic Escherichia coli strain Nissle 1917: specific up-regulation of the proinflammatory chemokine MCP-1. BMC Med Genet, 6:43. https://doi.org/10.1186/1471-2350-6-43CrossRefGoogle Scholar
  76. Vizoso Pinto MG, Gómez MR, Seifert S, et al., 2009. Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol, 133(1-2):86–93. https://doi.org/10.1016/j.ijfoodmicro.2009.05.013CrossRefGoogle Scholar
  77. Wang JJ, Tang H, Zhang CH, et al., 2015. Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J, 9(1):1–15. https://doi.org/10.1038/ismej.2014.99CrossRefGoogle Scholar
  78. Wang Y, Wu YP, Wang YB, 2017. Bacillus amyloliquefaciens SC06 alleviates the oxidative stress of IPEC-1 via modulating Nrf2/Keap1 signaling pathway and decreasing ROS production. Appl Microbiol Biotechnol, 101(7): 3015–3026. https://doi.org/10.1007/s00253-016-8032-4CrossRefGoogle Scholar
  79. Wen K, Tin C, Wang HF, et al., 2014. Probiotic Lactobacillus rhamnosus GG enhanced Th1 cellular immunity but did not affect antibody responses in a human gut microbiota transplanted neonatal gnotobiotic pig model. PLoS ONE, 9(4):e94504. https://doi.org/10.1371/journal.pone.0094504CrossRefGoogle Scholar
  80. Wen K, Liu FN, Li GH, et al., 2015. Lactobacillus rhamnosus GG dosage affects the adjuvanticity and protection against rotavirus diarrhea in gnotobiotic pigs. J Pediatr Gastroenterol Nutr, 60(6):834–843. https://doi.org/10.1097/MPG.0000000000000694CrossRefGoogle Scholar
  81. Wu SG, Rhee KJ, Albesiano E, et al., 2009. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med, 15(9): 1016–1022. https://doi.org/10.1038/nm.2015CrossRefGoogle Scholar
  82. Zeyner A, Boldt E, 2006. Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets. J Anim Physiol Anim Nutr, 90(1-2):25–31. https://doi.org/10.1111/j.1439-0396.2005.00615.xCrossRefGoogle Scholar
  83. Zhang L, Xu YQ, Liu HY, et al., 2010. Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: effects on diarrhoea incidence, faecal microflora and immune responses. Vet Microbiol, 141(1-2):142–148. https://doi.org/10.1016/j.vetmic.2009.09.003CrossRefGoogle Scholar
  84. Zhang Q, Eicher SD, Applegate TJ, 2015. Development of intestinal mucin 2, IgA, and polymeric Ig receptor expressions in broiler chickens and Pekin ducks. Poult Sci, 94(2):172–180. https://doi.org/10.3382/ps/peu064CrossRefGoogle Scholar
  85. Zhang XP, Shu MA, Wang YB, et al., 2014. Effect of photosynthetic bacteria on water quality and microbiota in grass carp culture. World J Microbiol Biotechnol, 30(9): 2523–2531. https://doi.org/10.1007/s11274-014-1677-1CrossRefGoogle Scholar
  86. Zhu QC, Jin ZM, Wu W, et al., 2014. Analysis of the intestinal lumen microbiota in an animal model of colorectal cancer. PLoS ONE, 9(3):e90849. https://doi.org/10.1371/journal.pone.0090849CrossRefGoogle Scholar

Copyright information

© Zhejiang University and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Molecular Animal Nutrition and Feed Science, Key Laboratory of Animal Feed and Nutrition of Zhejiang Province, College of Animal ScienceZhejiang UniversityHangzhouChina
  2. 2.Department of Animal SciencesOregon State UniversityCorvallisUSA
  3. 3.College of Animal Science and TechnologyGuangxi UniversityNanningChina
  4. 4.China National Bamboo Research CenterKey Laboratory of High Efficient Processing of Bamboo of Zhejiang ProvinceHangzhouChina

Personalised recommendations