CLC number: S816.3
On-line Access: 2019-01-22
Received: 2018-01-15
Revision Accepted: 2018-06-06
Crosschecked: 2018-12-05
Cited: 0
Clicked: 4415
Yang Wang, Li Gong, Yan-ping Wu, Zhi-wen Cui, Yong-qiang Wang, Yi Huang, Xiao-ping Zhang, Wei-fen Li. Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets[J]. Journal of Zhejiang University Science B, 2019, 20(2): 180-192.
@article{title="Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets",
author="Yang Wang, Li Gong, Yan-ping Wu, Zhi-wen Cui, Yong-qiang Wang, Yi Huang, Xiao-ping Zhang, Wei-fen Li",
journal="Journal of Zhejiang University Science B",
volume="20",
number="2",
pages="180-192",
year="2019",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1800022"
}
%0 Journal Article
%T Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets
%A Yang Wang
%A Li Gong
%A Yan-ping Wu
%A Zhi-wen Cui
%A Yong-qiang Wang
%A Yi Huang
%A Xiao-ping Zhang
%A Wei-fen Li
%J Journal of Zhejiang University SCIENCE B
%V 20
%N 2
%P 180-192
%@ 1673-1581
%D 2019
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1800022
TY - JOUR
T1 - Oral administration of Lactobacillus rhamnosus GG to newborn piglets augments gut barrier function in pre-weaning piglets
A1 - Yang Wang
A1 - Li Gong
A1 - Yan-ping Wu
A1 - Zhi-wen Cui
A1 - Yong-qiang Wang
A1 - Yi Huang
A1 - Xiao-ping Zhang
A1 - Wei-fen Li
J0 - Journal of Zhejiang University Science B
VL - 20
IS - 2
SP - 180
EP - 192
%@ 1673-1581
Y1 - 2019
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1800022
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.
[1]Allen-Vercoe E, Strauss J, Chadee K, 2011. Fusobacterium nucleatum: an emerging gut pathogen? Gut Microbes, 2(5):294-298.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[9]Callewaert L, Michiels CW, 2010. Lysozymes in the animal kingdom. J Biosci, 35(1):127-160.
[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.
[11]Casserly C, Erijman L, 2003. Molecular monitoring of microbial diversity in an UASB reactor. Int Biodeterior Biodegrad, 52(1):7-12.
[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.
[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.
[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.
[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.
[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.
[17]Duerkop BA, Vaishnava S, Hooper LV, 2009. Immune responses to the microbiota at the intestinal mucosal surface. Immunity, 31(3):368-376.
[18]Eckburg PB, Bik EM, Bernstein CN, et al., 2005. Diversity of the human intestinal microbial flora. Science, 308(5728):1635-1638.
[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.
[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.
[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.
[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.
[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.
[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]
[25]Guarino A, Lo Vecchio A, Canani RB, 2009. Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol, 25(1):18-23.
[26]Guarner F, Malagelada JR, 2003. Gut flora in health and disease. Lancet, 361(9356):512-519.
[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.
[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.
[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.
[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.
[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.
[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.
[33]Hooper LV, 2004. Bacterial contributions to mammalian gut development. Trends Microbiol, 12(3):129-134.
[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.
[35]Kagnoff MF, Eckmann L, 1997. Epithelial cells as sensors for microbial infection. J Clin Invest, 100(1):6-10.
[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.
[37]Kemper N, 2008. Veterinary antibiotics in the aquatic and terrestrial environment. Ecol Indic, 8(1):1-13.
[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.
[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.
[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.
[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.
[42]Ley RE, Hamady M, Lozupone C, et al., 2008. Evolution of mammals and their gut microbes. Science, 320(5883):1647-1651.
[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.
[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.
[45]Lozupone CA, Stombaugh JI, Gordon JI, et al., 2012. Diversity, stability and resilience of the human gut microbiota. Nature, 489(7415):220-230.
[46]Mackie RI, Sghir A, Gaskins HR, 1999. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr, 69(5):1035S-1045S.
[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.
[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.
[49]McCracken VJ, Lorenz RG, 2001. The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol, 3(1):1-11.
[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.
[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.
[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.
[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.
[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.
[55]National Research Council, 1998. Nutrient Requirements of Swine, 10th Ed. The National Academies Press, Washington, DC, USA.
[56]Natividad JMM, Verdu EF, 2013. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol Res, 69(1):42-51.
[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.
[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.
[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.
[60]Rakoff-Nahoum S, Medzhitov R, 2008. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol, 1(1):S10-S14.
[61]Rescigno M, 2011. The intestinal epithelial barrier in the control of homeostasis and immunity. Trends Immunol, 32(6):256-264.
[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.
[63]Salyers AA, 1984. Bacteroides of the human lower intestinal tract. Annu Rev Microbiol, 38:293-313.
[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.
[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.
[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.
[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.
[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.
[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.
[70]Tannock GW, 2001. Molecular assessment of intestinal microflora. Am J Clin Nutr, 73(2):410S-414S.
[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.
[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.
[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.
[74]Turner JR, 2009. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol, 9(11):799-809.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[87]List of electronic supplementary materials
[88]Table S1 Composition of sows’ diet
[89]Table S2 Nutrient levels of sows’ diet
[90]Table S3 Composition of pre-starter feed
[91]Table S4 Nutrient levels of pre-starter feed
[92]Fig. S1 Experimental protocol design
Open peer comments: Debate/Discuss/Question/Opinion
<1>