Skip to main content

Effects of Lactobacillus acidophilus dietary supplementation on the performance, intestinal barrier function, rectal microflora and serum immune function in weaned piglets challenged with Escherichia coli lipopolysaccharide

Antonie van Leeuwenhoek volume 107, pages 883–891 (2015)Cite this article

Abstract

This study was conducted with a lipopolysaccharide (LPS)-challenged piglet model to determine the effects of diets containing Lactobacillus acidophilus on the performance, intestinal barrier function, rectal microflora and serum immune function. A total of 150 piglets (initial body weight (BW) 7.53 ± 0.21 kg) were allotted to one of the following diets, including a basal diet, a basal diet supplemented with 250 mg/kg Flavomycin, or basal diet plus 0.05, 0.1 or 0.2 % L. acidophilus. On day 28 of the trial, the pigs were given an intraperitoneal injection of LPS (200 μg/kg body weight) followed by blood collection 3 h later. Diets with either antibiotics, 0.1 or 0.2 % Lactobacillus increased (P < 0.05) the final BW and decreased (P < 0.05) feed gain ratio (F/G) compared with the control group. Pigs fed diets containing antibiotic or Lactobacillus had greater average daily gain (ADG) (P < 0.05) than pigs fed the control diet. The rectal content Lactobacillus counts for pigs fed diet containing Lactobacillus were significant higher (P < 0.01) than those fed antibiotic or control diet. Feeding the Lactobacillus diets decreased the Escherichia coli counts of rectal content (P < 0.01). Pigs fed diets containing 0.1 or 0.2 % Lactobacillus decreased serum DAO activity (P < 0.05) compared with pigs fed the control diet. Serum IL-10 concentration was enhanced in pigs fed the diet with Lactobacillus compared to pigs fed the control diet and antibiotic diet. Feeding a diet with Lactobacillus reduced (P < 0.05) IFN-γ concentration compared to the control diet. Inclusion of Lactobacillus in diets fed to pigs reduced TNF-α concentration compared with pigs fed no Lactobacillus (P < 0.05). These results indicate that feeding with L. acidophilus improved growth performance and protected against LPS-induced inflammatory status.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Bhandari SK, Xu B, Nyachoti CM, Giesting DW, Krause DO (2008) Evaluation of alternatives to antibiotics using an Escherichia coli K88+ model of piglet diarrhea: effects on gut microbial ecology. J Anim Sci 86:836–847

    Article  CAS  PubMed  Google Scholar 

  • Broom LJ, Miller HM, Kerr KG, Knapp JS (2006) Effects of zinc oxide and Enterococcus faecium SF68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Res Vet Sci 80:45–54

    Article  CAS  PubMed  Google Scholar 

  • Carroll IM, Andrus JM, Bruno-Barcena JM, Klaenhammer TR, Hassan HM, Threadgill DS (2007) Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am J Physiol Gastrointest Liver Physiol 293:G729–G738

    Article  CAS  PubMed  Google Scholar 

  • Castillo NA, Perdigón G, de Moreno de LeBlanc A (2011) Oral administration of a probiotic Lactobacillus modulates cytokine production and TLR expression improving the immune response against Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol 11:177–188

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Christensen HR, Frøkiær H, Pestka JJ (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168:171–178

    Article  CAS  PubMed  Google Scholar 

  • Cui C, Shen CJ, Jia G, Wang KN (2013) Effect of dietary Bacillus subtilis on proportion of Bacteroidetes and Firmicutes in swine intestine and lipid metabolism. Genet Mol Res 12:1766–1776

    Article  CAS  PubMed  Google Scholar 

  • de Lange CFM, Pluske J, Gong J, Nyachoti CM (2010) Strategic use of feed ingredients and feed additives to stimulate gut health and development in young pigs. Livest Sci 134:124–134

    Article  Google Scholar 

  • de Moreno de LeBlanc A, Castillo NA, Perdigón G (2010) Anti-infective mechanisms induced by a probiotic Lactobacillus strain against Salmonella enterica serovar Typhimurium infection. Int J Food Microbiol 138:223–231

    Article  CAS  Google Scholar 

  • Dieleman LA, Goerres MS, Arends A, Sprengers D, Torrice C, Hoentjen F, Grenther WB, Sartor RB (2003) Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 52:370–376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • FAO/WHO (2001) Health and nutritional properties of probiotics in food including powder milk with live Lactic acid bacteria. [http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf]

  • Goyal N, Shukla G (2013) Probiotic Lactobacillus rhamnosus GG Modulates the Mucosal Immune Response in Giardia intestinalis-Infected BALB/c Mice. Dig Dis Sci 58:1218–1225

    Article  CAS  PubMed  Google Scholar 

  • Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ, Nyachoti CM (2013) Gastrointestinal health and function in weaned pigs: a review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol Anim Nutr 97:207–237

    Article  CAS  Google Scholar 

  • Hou YQ, Wang L, Zhang W, Yang ZG, Ding BY, Zhu HL, Liu YL, Qiu YS, Yin YL, Wu GY (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242

    Article  CAS  PubMed  Google Scholar 

  • Huang CH, Qiao SY, Li DF, Piao XS, Ren JP (2004) Effects of Lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian-Aust J Anim Sci 17:401–409

    Article  Google Scholar 

  • Inoue R, Tsukahara T, Nakanishi N, Ushida K (2005) Development of the intestinal microbiota in the piglet. J Gen App MIcrobiol 51:257–265

    Article  CAS  Google Scholar 

  • Jost M, Bracher JA (1999) The effect of Sanobiotic RS, a multiactive probiotic growth promoter, in rearing piglets. Appl Environ Microbiol 66:4200–4204

    Google Scholar 

  • Kazmierczak SC, Robertson AF (1992) Evaluation of a spectrophotometric method for measurement of activity of diamine oxidase in newborn infants. Ann Clin Lab Sci 22:155–161

    CAS  PubMed  Google Scholar 

  • Lallès JP, Bosi P, Smidt H, Stokes CR (2007) Nutritional management of gut health in pigs around weaning. Proc Nutr Soc 66:260–268

    Article  PubMed  Google Scholar 

  • Lee JS, Awji EG, Lee SJ, Tassew DD, Park YB, Park KS, Kim MK, Kim B, Park SC (2012) Effect of Lactobacillus plantarum CJLP243 on the growth performance and cytokine response of weaning pigs challenged with enterotoxigenic Escherichia coli. J Anim Sci 90:3709–3717

    Article  CAS  PubMed  Google Scholar 

  • Li JY, Yu Y, Hu S, Sun D, Yao YM (2002) Preventive effect of glutamine on intestinal barrier dysfunction induced by severe trauma. World J Gastroenterol 8:168–171

    CAS  PubMed  Google Scholar 

  • Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, Omori M, Zhou B, Ziegler SF (2007) TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu Rev Immunol 25:193–219

    Article  CAS  PubMed  Google Scholar 

  • Liu YL, Huang JJ, Hou YQ, Zhu HL, Zhao SJ, Ding BY, Yin YL, Yi GF, Shi JY, Fan W (2008) Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. Br J Nutr 100:552–560

    Article  CAS  PubMed  Google Scholar 

  • Luk GD, Bayless TM, Baylin SB (1980) Diamine oxidase (histaminase): a circulating marker for rat intestinal mucosal maturation and integrity. J Clin Invest 66:66–70

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Luk GD, Bayless TM, Baylin SB (1983) Plasma postheparin diamine oxidase. Sensitive provocative test for quantitating length of acute intestinal mucosal injury in the rat. J Clin Invest 71:1308–1315

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Luongo D, Miyamoto J, Bergamo P, Nazzaro F, Baruzzi F, Sashihara T, Tanabe S, Rossi M (2013) Differential modulation of innate immunity in vitro by probiotic strains of Lactobacillus gasseri. BMC Microbiol 13:298–309

    Article  PubMed Central  PubMed  Google Scholar 

  • Mennigen R, Nolte K, Rijcken E, Utech M, Loeffler B, Senninger N, Bruewer W (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:G1140–G1149

    Article  CAS  PubMed  Google Scholar 

  • Mercer DW, Smith GS, Cross JM, Russell DH, Chang L, Cacioppo J (1996) Effects of lipopolysaccharide on intestinal injury: potential role of nitric oxide and lipid peroxidation. J Surg Res 63:185–192

    Article  CAS  PubMed  Google Scholar 

  • Metzler B, Bauer E, Mosenthin R (2005) Microfl ora management in the gastrointestinal tract of piglets. Asian-Aust. J Anim Sci 18:1353–1362

    Article  Google Scholar 

  • Mileti E, Matteoli G, Iliev ID, Rescigno M (2009) Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 4(9):e7056

    Article  PubMed Central  PubMed  Google Scholar 

  • NRC (2012) Nutrient requirements of swine. 11th Revised Edition. The National Academies Press, Washington, DC

  • Otte JM, Cario E, Podolsky DK (2004) Functional modulation of enterocytesby gram-positive and gram-negative microorganisms. Am J Physiol Gastrointest Liver Physiol 286:G613–G626

    Article  CAS  PubMed  Google Scholar 

  • Pluske JR, Hampson DJ, Williams IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livest Prod Sci 51:215–236

    Article  Google Scholar 

  • Roselli M, Finamore A, Britti MS, Konstantinov SR, Smidt H, de Vos WM, Mengheri E (2007) The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J Nutr 137:2709–2716

    CAS  PubMed  Google Scholar 

  • Ulisse S, Giochetti P, D’Alò S, Russo FP, Pesce I, Ricci G, Rizzello F, Helwig U, Cifone MG, Campieri M, De Simone C (2001) Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatment. Am J Gastroenterol 96:2691–2699

    Article  CAS  PubMed  Google Scholar 

  • Vella A, Farrugia G (1998) D-lactic acidosis: pathologic consequence of saprophytism. Mayo Clin Proc 73:451–456

    Article  CAS  PubMed  Google Scholar 

  • Villena J, Kitazawa H (2014) Modulation of intestinal TLR4-inflammatory signaling pathways by probiotic microorganisms: lessons learned from Lactobacillus jensenii TL2937. Front Immunol 4:512–523

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang A, Yu H, Gao X, Li X, Qiao S (2009) Influence of Lactobacillus fermentum I5007 on the intestinal and systemic immune responses of healthy and E. coli challenged piglets. Antonie Van Leeuwenhoek 96:89–98

    Article  CAS  PubMed  Google Scholar 

  • Weber TE, Ziemer CJ, Kerr BJ (2008) Effects of adding fibrous feedstuffs to the diet of young pigs on growth performance, intestinal cytokines, and circulating acute-phase proteins. J Anim Sci 86:871–881

    Article  CAS  PubMed  Google Scholar 

  • Yang KM, Jiang ZY, Zheng CT, Wang L, Yang XF (2014) Effect of Lactobacillus plantarum on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic Escherichia coli K88. J Anim Sci 92:1496–1503

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Wen K, Azevedo MS, Gonzalez A, Saif LJ, Li G, Yousef AE, Yuan L (2008) Lactic acid bacterial colonization and human rotavirus infection influence distribution and frequencies of monocytes/macrophages and dendritic cells in neonatal gnotobiotic pigs. Vet Immunol Immunopathol 121:222–231

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by grants (31402087) from the National Science Grant of China.

Conflict of interest

The authors would like to declare no conflict of interests.

Author information

Affiliations

  1. Tianjin Institute of Animal Husbandry and Veterinary Medicine, 17 km point of Jin-Jing Road, Tianjin, 300381, People’s Republic of China

    Jiayun Qiao, Haihua Li & Wenjie Wang

  2. College of Animal Science and Veterinary Medicine, Henan Agricultural University, 63# Nongye road, Zhengzhou, 450002, Henan, People’s Republic of China

    Zhixiang Wang

Authors
  1. Jiayun Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haihua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhixiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenjie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jiayun Qiao or Wenjie Wang.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Qiao, J., Li, H., Wang, Z. et al. Effects of Lactobacillus acidophilus dietary supplementation on the performance, intestinal barrier function, rectal microflora and serum immune function in weaned piglets challenged with Escherichia coli lipopolysaccharide. Antonie van Leeuwenhoek 107, 883–891 (2015). https://doi.org/10.1007/s10482-015-0380-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0380-z

Keywords

  • Lactobacillus acidophilus
  • Weaned piglet
  • Immune function
  • Lipopolysaccharide