Changes in gut microbial populations, intestinal morphology, expression of tight junction proteins, and cytokine production between two pig breeds after challenge with Escherichia coli K88: A comparative study

Journal of Animal Science

Volumn 91, Issue 12, 2013, Pages 5614-5625

  Gao, Y ^a   Han, F ^a   Huang, X ^a   Rong, Y ^a   Yi, H ^a   Wang, Y ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Cytokine; Escherichia coli K88; Gut microbe; Intestinal morphology; Jinhua pigs; Landrace pigs

Indexed keywords

CYTOKINE; MESSENGER RNA; TIGHT JUNCTION PROTEIN;

ANIMAL; ANIMAL DISEASE; ARTICLE; CLASSIFICATION; COMPARATIVE STUDY; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HISTOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SWINE; SWINE DISEASE;

ANIMALS; CYTOKINES; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; INTESTINES; RNA, MESSENGER; SWINE; SWINE DISEASES; TIGHT JUNCTION PROTEINS;

EID: 84888142722     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2013-6528     Document Type: Article

References (43)

1. Albin, D. M., J. E. Wubben, J. M. Rowlett, K. A. Tappenden, and R. A. Nowak. 2007. Changes in small intestinal nutrient transport and barrier function after lipopolysaccharide exposure in two pig breeds. J. Anim. Sci. 85:2517-2523.
2. Berkes, J., V. K. Viswanathan, S. D. Savkovic, and G. Hecht. 2003. Intestinal epithelial responses to enteric pathogens: Effects on the tight junction barrier, ion transport, and inflammation. Gut 52:439-451.
3. Bhandari, S. K., B. Xu, C. M. Nyachoti, D. W. Giesting, and D. O. Krause. 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.
4. Bosi, P., L. Casini, A. Finamore, C. Cremokolini, G. Merialdi, P. Trevisi, F. Nobili, and E. Mengheri. 2004. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J. Anim. Sci. 82:1764-1772.
5. Brandtzaeg, P. 2010. Homeostatic impact of indigenous microbiota and secretory immunity. Benef. Microbes 1:211-227.
6. Capaldo, C. T., and A. Nusrat. 2009. Cytokine regulation of tight junctions. Biochim. Biophys. Acta 1788:864-871.
7. Castillo, M., S. M. Martin-Orue, J. A. Taylor-Pickard, J. F. Perez, and J. Gasa. 2008. Use of mannan-oligosaccharides and zinc chelate as growth promoters and diarrhea preventative in weaning pigs: Effects on microbiota and gut function. J. Anim. Sci. 86:94-101.
8. Duchetsuchaux, M. F., A. M. Bertin, and P. S. Menanteau. 1991. Susceptibility of Chinese Meishan and European large white-pigs to enterotoxigenic Escherichia coli strains bearing colonization factor K88, 987P, K99, or F41. Am. J. Vet. Res. 52:40-44.
9. Ewaschuk, J. B., G. K. Murdoch, I. R. Johnson, K. L. Madsen, and C. J. Field. 2011. Glutamine supplementation improves intestinal barrier function in a weaned piglet model of Escherichia coli infection. Br. J. Nutr. 106:870-877.
10. Furet, J. P., O. Firmesse, M. Gourmelon, C. Bridonneau, J. Tap, S. Mondot, J. Dore, and G. Corthier. 2009. Comparative assessment of human and farm animal faecal microbiota using realtime quantitative PCR. FEMS Microbiol. Ecol. 68: 351-362.
11. Guo, X. L., X. J. Xia, R. Y. Tang, and K. N. Wang. 2008. Real-time PCR quantification of the predominant bacterial divisions in the distal gut of Meishan and Landrace pigs. Anaerobe 14:224-228.
12. Halas, D., C. F. Hansen, D. J. Hampson, B. P. Mullan, J. C. Kim, R. H. Wilson, and J. R. Pluske. 2010. Dietary supplementation with benzoic acid improves apparent ileal digestibility of total nitrogen and increases villous height and caecal microbial diversity in weaner pigs. Anim. Feed Sci. Technol. 160:137-147.
13. Hojberg, O., N. Canibe, H. D. Poulsen, M. S. Hedemann, and B. B. Jensen. 2005. Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl. Environ. Microbiol. 71:2267-2277.
14. Kim, J. C., C. F. Hansen, B. P. Mullan, and J. R. Pluske. 2012. Nutrition and pathology of weaner pigs: Nutritional strategies to support barrier function in the gastrointestinal tract. Anim. Feed Sci. Technol. 173:3-16.
15. Konstantinov, S. R., A. A. Awati, B. A. Williams, B. G. Miller, P. Jones, C. R. Stokes, A. D. L. Akkermans, H. Smidt, and W. M. De Vos. 2006. Post-natal development of the porcine microbiota composition and activities. Environ. Microbiol. 8:1191-1199.
16. Konstantinov, S. R., H. Smidt, A. D. L. Akkermans, L. Casini, P. Trevisi, M. Mazzoni, S. De Filippi, P. Bosi, and W. M. de Vos. 2008. Feeding of Lactobacillus sobrius reduces Escherichia coli F4 levels in the gut and promotes growth of infected piglets. FEMS Microbiol. Ecol. 66:599-607.
17. Lambert, G. P. 2009. Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J. Anim. Sci. 87:E101-E108.
18. Layton, A., L. McKay, D. Williams, V. Garrett, R. Gentry, and G. Sayler. 2006. Development of bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl. Environ. Microbiol. 72:4214-4224.
19. Lessard, M., M. Dupuis, N. Gagnon, E. Nadeau, J. J. Matte, J. Goulet, and J. M. Fairbrother. 2009. Administration of Pediococcus acidilactici or Saccharomyces cerevisiae boulardii modulates development of porcine mucosal immunity and reduces intestinal bacterial translocation after Escherichia coli challenge. J. Anim. Sci. 87:922-934.
20. Li, X. Q., Y. H. Zhu, H. F. Zhang, Y. Yue, Z. X. Cai, Q. P. Lu, L. Zhang, X. G. Weng, F. Zhang, D. Zhou, J. C. Yang, and J. F. Wang. 2012. Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: Intestinal microbiota and immune imbalances. PLoS ONE 7(7):e40666.
21. Lippolis, J. D. 2008. Immunological signaling networks: Integrating the body's immune response. J. Anim. Sci. 86:E53-E63.
22. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408.
23. Madec, F., N. Bridoux, S. Bounaix, R. Cariolet, Y. Duval-Iflah, D. J. Hampson, and A. Jestin. 2000. Experimental models of porcine post-weaning colibacillosis and their relationship to post-weaning diarrhoea and digestive disorders as encountered in the field. Vet. Microbiol. 72:295-310.
24. Melin, L., S. Mattson, M. Katouli, and P. Wallgren. 2004. Development of post-weaning diarrhoea in piglets. Relation to presence of Escherichia coli strains and rotavirus. J. Vet. Med. B Infect. Dis. Vet. Public Health 51:12-22.
25. Moeser, A. J., L. B. Borst, B. L. Overman, and J. S. Pittman. 2012. Defects in small intestinal epithelial barrier function and morphology associated with peri-weaning failure to thrive syndrom (PFTS) in swine. Res. Vet. Sci. 93:975-982.
26. Moreto, M., and A. Perez-Bosque. 2009. Dietary plasma proteins, the intestinal immune system, and the barrier functions of the intestinal mucosa. J. Anim. Sci. 87:E92-E100.
27. Nabuurs, M. J. A. 1998. Weaning piglets as a model for studying pathophysiology of diarrhea. Vet. Q. 20(Suppl. 3):42-45.
28. Nataro, J. P., and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142.
29. Petersson, A., K. J. Domig, K. Schedle, W. Windisch, and W. Kneifel. 2010. Comparison of three methods to enumerate gut microbiota of weanling piglets fed insoluble dietary fibre differing in lignin content. J. Agric. Sci. 148:225-232.
30. Pluske, J. R., Z. Durmic, H. G. Payne, J. Mansfield, B. P. Mullan, D. J. Hampson, and P. E. Vercoe. 2007. Microbial diversity in the large intestine of pigs born and reared in different environments. Livest. Sci. 108:113-116.
31. Pluske, J. R., D. J. Hampson, and I. H. Williams. 1997. Factors influencing the structure and function of the small intestine in the weaned pig: A review. Livest. Prod. Sci. 51:215-236.
32. Price, K. L., H. R. Totty, H. B. Lee, M. D. Utt, G. E. Fitzner, I. Yoon, M. A. Ponder, and J. Escobar. 2010. Use of Saccharomyces cerevisiae fermentation product on growth performance and microbiota of weaned pigs during Salmonella infection. J. Anim. Sci. 88:3896-3908.
33. Qi, H. 2011. Effects of different protein sources on intestinal micro flora and intestinal health of weaned piglets. PhD diss., Sichuan Agricultural University, Ya'an, China.
34. Qi, H., Z. Xiang, G. Han, B. Yu, Z. Huang, and D. Chen. 2011. Effects of different dietary protein sources on cecal microflora in rats. Afr. J. Biotechnol. 10:3704-3708.
35. Sekirov, I., S. L. Russell, L. C. M. Antunes, and B. B. Finlay. 2010. Gut microbiota in health and disease. Physiol. Rev. 90:859-904.
36. Shan, T., T. Wu, Y. Reng, and Y. Wang. 2009. Breed difference and regulation of the porcine adipose triglyceride lipase and hormone sensitive lipase by TNF alpha. Anim. Genet. 40:863-870.
37. Snoeck, V., N. Huyghebaert, E. Cox, A. Vermeire, S. Vancaeneghem, J. P. Remon, and B. M. Goddeeris. 2003. Enteric-coated pellets of F4 fimbriae for oral vaccination of suckling piglets against enterotoxigenic Escherichia coli infections. Vet. Immunol. Immunopathol. 96:219-227.
38. Sutherland, M. A., S. R. Niekamp, S. L. Rodriguez-Zas, and J. L. Salak-Johnson. 2006. Impacts of chronic stress and social status on various physiological and performance measures in pigs of different breeds. J. Anim. Sci. 84:588-596.
39. Suzuki, M. T., L. T. Taylor, and E. F. DeLong. 2000. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl. Environ. Microbiol. 66:4605-4614.
40. Wellock, I. J., P. D. Fortomaris, J. G. Houdijk, and I. Kyriazakis. 2008a. Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: Health. Animal 2:834-842.
41. Wellock, I. J., P. D. Fortomaris, J. G. Houdijk, and I. Kyriazakis. 2008b. Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: Performance. Animal 2:825-833.
42. Yi, G. F., J. A. Carroll, G. L. Allee, A. M. Gaines, D. C. Kendall, J. L. Usry, Y. Toride, and S. Izuru. 2005. Effect of glutamine and spray-dried plasma on growth performance, small intestinal morphology, and immune responses of Escherichia coli K88(+)-challenged weaned pigs. J. Anim. Sci. 83:634-643.
43. Zhao, J., A. F. Harper, M. J. Estienne, K. E. Webb Jr., A. P. McElroy, and D. M. Denbow. 2007. Growth performance and intestinal morphology responses in early weaned pigs to supplementation of antibiotic-free diets with an organic copper complex and spray-dried plasma protein in sanitary and nonsanitary environments. J. Anim. Sci. 85:1302-1310.