1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Animal Biosciences
  4. Volume 5, 2017
  5. Article

Annual Review of Animal Biosciences

Volume 5, 2017

in Swine: Microbiota Interactions

Abstract

For the important foodborne pathogen to cause disease or persist in pigs, it has evolved an intricate set of interactions between itself, the host, and the indigenous microflora of the host. must evade the host's immune system and must also overcome colonization resistance mediated by the pig's indigenous microflora. The inflammatory response against provides the bacteria with unique metabolites and is thus exploited by for competitive advantage. During infection, changes in the composition of the indigenous microflora occur that have been associated with a breakdown in colonization resistance. Healthy pigs that are low-level shedders of also exhibit alterations in their indigenous microflora similar to those in ill animals. Here we review the literature on the interactions that occur between swine, , and the indigenous microflora and discuss methods to reduce or prevent colonization of pigs with .

Keyword(s): control of Salmonella enterica, gut, health, innate immunity, metabolism, microbiome
Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-022516-022834
2017-02-08
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/animal/5/1/annurev-animal-022516-022834.html?itemId=/content/journals/10.1146/annurev-animal-022516-022834&mimeType=html&fmt=ahah

Literature Cited

  1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA. 1.  et al. 2011. Foodborne illness acquired in the United States—major pathogens. Emerg. Infect. Dis. 17:7–15 [Google Scholar]
  2. Batz MB, Hoffmann S, Morris JG. 2.  2011. Ranking the Risks: The 10 Pathogen-Food Combinations with the Greatest Burden on Public Health Gainesville: Emerg. Pathog. Inst., Univ. Fla. https://folio.iupui.edu/bitstream/handle/10244/1022/72267report.pdf
  3. Pardon P, Sanchis R, Marly J, Lantier F, Pepin M, Popoff M. 3.  1988. Ovine salmonellosis caused by Salmonella abortusovis. Ann. Rech. Vet. 19:221–35 [Google Scholar]
  4. Knetter SM, Bearson SM, Huang TH, Kurkiewicz D, Schroyen M. 4.  et al. 2015. Salmonella enterica serovar Typhimurium–infected pigs with different shedding levels exhibit distinct clinical, peripheral cytokine and transcriptomic immune response phenotypes. Innate Immun 21:227–41 [Google Scholar]
  5. Taylor DN, Bied JM, Munro JS, Feldman RA. 5.  1982. Salmonella dublin infections in the United States, 1979–1980. J. Infect. Dis. 146:322–27 [Google Scholar]
  6. Tischer I, Mields W, Wolff D, Vagt M, Griem W. 6.  1986. Studies on epidemiology and pathogenicity of porcine circovirus. Arch. Virol. 91:271–76 [Google Scholar]
  7. Coburn B, Grassl GA, Finlay BB. 7.  2007. Salmonella, the host and disease: a brief review. Immunol. Cell Biol. 85:112–18 [Google Scholar]
  8. Fierer J, Guiney DG. 8.  2001. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J. Clin. Investig. 107:775–80 [Google Scholar]
  9. Baumler AJ, Tsolis RM, Ficht TA, Adams LG. 9.  1998. Evolution of host adaptation in Salmonella enterica. Infect. Immun. 66:4579–87 [Google Scholar]
  10. Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C. 10.  et al. 2009. Life in the inflamed intestine, Salmonella style. Trends Microbiol 17:498–506 [Google Scholar]
  11. Valdez Y, Ferreira RB, Finlay BB. 11.  2009. Molecular mechanisms of Salmonella virulence and host resistance. Curr. Top. Microbiol. Immunol. 337:93–127 [Google Scholar]
  12. Ibarra JA, Steele-Mortimer O. 12.  2009. Salmonella—the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 11:1579–86 [Google Scholar]
  13. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL. 13.  et al. 2010. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467:426–29 [Google Scholar]
  14. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. 14.  2000. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2:145–56 [Google Scholar]
  15. van Asten AJ, van Dijk JE. 15.  2005. Distribution of “classic” virulence factors among Salmonella spp. FEMS Immunol. Med. Microbiol 44:251–59 [Google Scholar]
  16. Schmitt CK, Ikeda JS, Darnell SC, Watson PR, Bispham J. 16.  et al. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619–25 [Google Scholar]
  17. Sano G, Takada Y, Goto S, Maruyama K, Shindo Y. 17.  et al. 2007. Flagella facilitate escape of Salmonella from oncotic macrophages. J. Bacteriol. 189:8224–32 [Google Scholar]
  18. Jones BD. 18.  1997. Host responses to pathogenic Salmonella infection. Genes Dev 11:679–87 [Google Scholar]
  19. Fields PI, Groisman EA, Heffron F. 19.  1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:1059–62 [Google Scholar]
  20. Groisman EA, Chiao E, Lipps CJ, Heffron F. 20.  1989. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. PNAS 86:7077–81 [Google Scholar]
  21. Velge P, Wiedemann A, Rosselin M, Abed N, Boumart Z. 21.  et al. 2012. Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis. MicrobiologyOpen 1:243–58 [Google Scholar]
  22. Salcedo SP, Noursadeghi M, Cohen J, Holden DW. 22.  2001. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell. Microbiol. 3:587–97 [Google Scholar]
  23. Figueira R, Holden DW. 23.  2012. Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology 158:1147–61 [Google Scholar]
  24. Round JL, Mazmanian SK. 24.  2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:313–23 [Google Scholar]
  25. Santos RL. 25.  2014. Pathobiology of Salmonella, intestinal microbiota, and the host innate immune response. Front. Immunol. 5:252 [Google Scholar]
  26. Drumo R, Pesciaroli M, Ruggeri J, Tarantino M, Chirullo B. 26.  et al. 2016. Salmonella enterica serovar Typhimurium exploits inflammation to modify swine intestinal microbiota. Front. Cell. Infect. Microbiol. 5:106 [Google Scholar]
  27. Hallstrom K, McCormick BA. 27.  2011. Salmonella interaction with and passage through the intestinal mucosa: through the lens of the organism. Front. Microbiol. 2:88 [Google Scholar]
  28. Sassone-Corsi M, Raffatellu M. 28.  2015. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J. Immunol. 194:4081–87 [Google Scholar]
  29. Fernández-Santoscoy M, Wenzel UA, Yrlid U, Cardell S, Bäckhed F, Wick MJ. 29.  2015. The gut microbiota reduces colonization of the mesenteric lymph nodes and IL-12-independent IFN-γ production during Salmonella infection. Front. Cell. Infect. Microbiol. 5:93 [Google Scholar]
  30. Behnsen J, Jellbauer S, Wong CP, Edwards RA, George MD. 30.  et al. 2014. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40:262–73 [Google Scholar]
  31. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M. 31.  et al. 2007. Salmonella enterica serovar Typhimurium exploits inflammation to compete with the intestinal microbiota. PLOS Biol 5:2177–89 [Google Scholar]
  32. Zhou D, Galan J. 32.  2001. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 3:1293–98 [Google Scholar]
  33. Abrahams GL, Hensel M. 33.  2006. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell. Microbiol. 8:728–37 [Google Scholar]
  34. Tam MA, Rydstrom A, Sundquist M, Wick MJ. 34.  2008. Early cellular responses to Salmonella infection: dendritic cells, monocytes, and more. Immunol. Rev. 225:140–62 [Google Scholar]
  35. Kumar T, Rajora VR, Arora N. 35.  2014. Prevalence of Salmonella in pigs and broilers in the Tarai region of Uttarakhand, India. Indian J. Med. Microbiol 32:99–101 [Google Scholar]
  36. Meurens F, Berri M, Auray G, Melo S, Levast B. 36.  et al. 2009. Early immune response following Salmonella enterica subspecies enterica serovar Typhimurium infection in porcine jejunal gut loops. Vet. Res. 40:5 [Google Scholar]
  37. Boyen F, Haesebrouck F, Maes D, Van Immerseel F, Ducatelle R, Pasmans F. 37.  2008. Non-typhoidal Salmonella infections in pigs: a closer look at epidemiology, pathogenesis and control. Vet. Microbiol. 130:1–19 [Google Scholar]
  38. Gray JT, Stabel TJ, Fedorka-Cray PJ. 38.  1996. Effect of dose on the immune response and persistence of Salmonella choleraesuis infection in swine. Am. J. Vet. Res. 57:313–19 [Google Scholar]
  39. Lichtensteiger CA, Vimr ER. 39.  2003. Systemic and enteric colonization of pigs by a hilA signature-tagged mutant of Salmonella choleraesuis. Microb. Pathog. 34:149–54 [Google Scholar]
  40. Chiu CH, Su LH, Chu C. 40.  2004. Salmonella enterica serotype Choleraesuis: epidemiology, pathogenesis, clinical disease, and treatment. Clin. Microbiol. Rev. 17:311–22 [Google Scholar]
  41. Chiu CH, Tang P, Chu C, Hu S, Bao Q. 41.  et al. 2005. The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. Nucleic Acids Res 33:1690–98 [Google Scholar]
  42. Tanaka T, Imai Y, Kumagae N, Sato S. 42.  2010. The effect of feeding lactic acid to Salmonella Typhimurium experimentally infected swine. J. Vet. Med. Sci 72:827–31 [Google Scholar]
  43. Yin F, Farzan A, Wang QC, Yu H, Yin Y. 43.  et al. 2014. Reduction of Salmonella enterica serovar Typhimurium DT104 infection in experimentally challenged weaned pigs fed a Lactobacillus-fermented feed. Foodborne Pathog. Dis. 11:628–34 [Google Scholar]
  44. Verbrugghe E, Boyen F, Van Parys A, Van Deun K, Croubels S. 44.  et al. 2011. Stress induced Salmonella Typhimurium recrudescence in pigs coincides with cortisol induced increased intracellular proliferation in macrophages. Vet. Res. 42:118 [Google Scholar]
  45. Gradassi M, Pesciaroli M, Martinelli N, Ruggeri J, Petrucci P. 45.  et al. 2013. Attenuated Salmonella enterica serovar Typhimurium lacking the ZnuABC transporter: an efficacious orally-administered mucosal vaccine against salmonellosis in pigs. Vaccine 31:3695–701 [Google Scholar]
  46. Nollet N, Maes D, Duchateau L, Hautekiet V, Houf K. 46.  et al. 2005. Discrepancies between the isolation of Salmonella from mesenteric lymph nodes and the results of serological screening in slaughter pigs. Vet. Res. 36:545–55 [Google Scholar]
  47. Wilkins EG, Roberts C. 47.  1988. Extraintestinal salmonellosis. Epidemiol. Infect. 100:361–68 [Google Scholar]
  48. Reed WM, Olander HJ, Thacker HL. 48.  1986. Studies on the pathogenesis of Salmonella Typhimurium and Salmonella Choleraesuis var Kunzendorf infection in weanling pigs. Am. J. Vet. Res. 47:75–83 [Google Scholar]
  49. Tamang MD, Gurung M, Nam HM, Moon DC, Kim SR. 49.  et al. 2015. Prevalence and characterization of Salmonella in pigs from conventional and organic farms and first report of S. serovar 1,4,[5],12:i:- from Korea. Vet. Microbiol. 178:119–24 [Google Scholar]
  50. Clothier KA, Kinyon JM, Frana TS. 50.  2010. Comparison of Salmonella serovar isolation and antimicrobial resistance patterns from porcine samples between 2003 and 2008. J. Vet. Diagn. Investig. 22:578–82 [Google Scholar]
  51. Zhao S, McDermott PF, Friedman S, Abbott J, Ayers S. 51.  et al. 2006. Antimicrobial resistance and genetic relatedness among Salmonella from retail foods of animal origin: NARMS retail meat surveillance. Foodborne Pathog. Dis. 3:106–17 [Google Scholar]
  52. Arce C, Lucena C, Moreno A, Garrido JJ. 52.  2014. Proteomic analysis of intestinal mucosa responses to Salmonella enterica serovar Typhimurium in naturally infected pig. Comp. Immunol. Microbiol. Infect. Dis. 37:59–67 [Google Scholar]
  53. Chang CH, Chen YS, Chiou MT, Su CH, Chen DS. 53.  et al. 2013. Application of Scutellariae radix, Gardeniae fructus, and probiotics to prevent Salmonella enterica serovar Choleraesuis infection in swine. Evid.-Based. Complement. Altern. Med 2013:568528 [Google Scholar]
  54. Pedersen K, Sørensen G, Löfström C, Leekitcharoenphon P, Nielsen B. 54.  et al. 2015. Reappearance of Salmonella serovar Choleraesuis var. Kunzendorf in Danish pig herds. Vet. Microbiol. 176:282–91 [Google Scholar]
  55. Briggs CE, Fratamico PM. 55.  1999. Molecular characterization of an antibiotic resistance gene cluster of Salmonella Typhimurium DT104. Antimicrob. Agents Chemother. 43:846–49 [Google Scholar]
  56. Barrell RA. 56.  1987. Isolations of salmonellas from humans and foods in the Manchester area: 1981–1985. Epidemiol. Infect. 98:277–84 [Google Scholar]
  57. Chen YH, Chen TP, Tsai JJ, Hwang KP, Lu PL. 57.  et al. 1999. Epidemiological study of human salmonellosis during 1991–1996 in southern Taiwan. Kaohsiung J. Med. Sci. 15:127–36 [Google Scholar]
  58. Cota I, Blanc-Potard AB, Casadesus J. 58.  2012. STM2209-STM2208 (opvAB): a phase variation locus of Salmonella enterica involved in control of O-antigen chain length. PLOS ONE 7:e36863 [Google Scholar]
  59. van der Woude MW, Baumler AJ. 59.  2004. Phase and antigenic variation in bacteria. Clin. Microbiol. Rev. 17:581611 [Google Scholar]
  60. van der Woude MW. 60.  2011. Phase variation: how to create and coordinate population diversity. Curr. Opin. Microbiol. 14:205–11 [Google Scholar]
  61. Stewart MK, Cummings LA, Johnson ML, Berezow AB, Cookson BT. 61.  2011. Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. PNAS 108:20742–47 [Google Scholar]
  62. Hoskisson PA, Smith MC. 62.  2007. Hypervariation and phase variation in the bacteriophage “resistome.”. Curr. Opin. Microbiol. 10:396–400 [Google Scholar]
  63. Srikhanta YN, Fox KL, Jennings MP. 63.  2010. The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol. 8:196–206 [Google Scholar]
  64. Aldridge PD, Wu C, Gnerer J, Karlinsey JE, Hughes KT, Sachs MS. 64.  2006. Regulatory protein that inhibits both synthesis and use of the target protein controls flagellar phase variation in Salmonella enterica. PNAS 103:11340–45 [Google Scholar]
  65. Isaacson RE, Kinsel M. 65.  1992. Adhesion of Salmonella Typhimurium to porcine intestinal epithelial surfaces: identification and characterization of two phenotypes. Infect. Immun. 60:3193–200 [Google Scholar]
  66. Bearson SM, Allen HK, Bearson BL, Looft T, Brunelle BW. 66.  et al. 2013. Profiling the gastrointestinal microbiota in response to Salmonella: low versus high Salmonella shedding in the natural porcine host. Infect. Genet. Evol. 16:330–40 [Google Scholar]
  67. Hanson DL, Loneragan GH, Brown TR, Nisbet DJ, Hume ME, Edrington TS. 67.  2016. Evidence supporting vertical transmission of Salmonella in dairy cattle. Epidemiol. Infect. 144:962–67 [Google Scholar]
  68. Lawley TD, Bouley DM, Hoy YE, Gerke C, Relman DA, Monack DM. 68.  2008. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect. Immun. 76:403–16 [Google Scholar]
  69. Walsh MC, Rostagno MH, Gardiner GE, Sutton AL, Richert BT, Radcliffe JS. 69.  2012. Controlling Salmonella infection in weanling pigs through water delivery of direct-fed microbials or organic acids. Part I: effects on growth performance, microbial populations, and immune status. J. Anim. Sci. 90:261–71 [Google Scholar]
  70. Hedemann MS, Mikkelsen LL, Naughton PJ, Jensen BB. 70.  2005. Effect of feed particle size and feed processing on morphological characteristics in the small and large intestine of pigs and on adhesion of Salmonella enterica serovar Typhimurium DT12 in the ileum in vitro. J. Anim. Sci. 83:1554–62 [Google Scholar]
  71. Mikkelsen LL, Naughton PJ, Hedemann MS, Jensen BB. 71.  2004. Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica serovar Typhimurium in the pig gastrointestinal tract. Appl. Environ. Microbiol. 70:3485–92 [Google Scholar]
  72. Papenbrock S, Stemme K, Amtsberg G, Verspohl J, Kamphues J. 72.  2005. Investigations on prophylactic effects of coarse feed structure and/or potassium diformate on the microflora in the digestive tract of weaned piglets experimentally infected with Salmonella Derby. J. Anim. Physiol. Anim. Nutr. 89:84–87 [Google Scholar]
  73. Visscher CF, Winter P, Verspohl J, Stratmann-Selke J, Upmann M. 73.  et al. 2009. Effects of feed particle size at dietary presence of added organic acids on caecal parameters and the prevalence of Salmonella in fattening pigs on farm and at slaughter. J. Anim. Physiol. Anim. Nutr. 93:423–30 [Google Scholar]
  74. Eisemann JH, Argenzio RA. 74.  1999. Effects of diet and housing density on growth and stomach morphology in pigs. J. Anim. Sci. 77:2709–14 [Google Scholar]
  75. Mavromichalis I, Hancock JD, Senne BW, Gugle TL, Kennedy GA. 75.  et al. 2000. Enzyme supplementation and particle size of wheat in diets for nursery and finishing pigs. J. Anim. Sci. 78:3086–95 [Google Scholar]
  76. Wondra KJ, Hancock JD, Behnke KC, Stark CR. 76.  1995. Effects of mill type and particle size uniformity on growth performance, nutrient digestibility, and stomach morphology in finishing pigs. J. Anim. Sci. 73:2564–73 [Google Scholar]
  77. Wondra KJ, Hancock JD, Behnke KC, Hines RH, Stark CR. 77.  1995. Effects of particle size and pelleting on growth performance, nutrient digestibility, and stomach morphology in finishing pigs. J. Anim. Sci. 73:757–63 [Google Scholar]
  78. Afema JA, Byarugaba DK, Shah DH, Atukwase E, Nambi M, Sischo WM. 78.  2016. Potential sources and transmission of Salmonella and antimicrobial resistance in Kampala, Uganda. PLOS ONE 11:e0152130 [Google Scholar]
  79. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M. 79.  et al. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50:882–89 [Google Scholar]
  80. Rajtak U, Boland F, Leonard N, Bolton D, Fanning S. 80.  2012. Roles of diet and the acid tolerance response in survival of common Salmonella serotypes in feces of finishing pigs. Appl. Environ. Microbiol. 78:110–19 [Google Scholar]
  81. Hurd HS, Gailey JK, McKean JD, Rostagno MH. 81.  2001. Rapid infection in market-weight swine following exposure to a Salmonella Typhimurium-contaminated environment. Am. J. Vet. Res. 62:1194–97 [Google Scholar]
  82. Lurette A, Belloc C, Touzeau S, Hoch T, Ezanno P. 82.  et al. 2008. Modelling Salmonella spread within a farrow-to-finish pig herd. Vet. Res. 39:49 [Google Scholar]
  83. Berends BR, Urlings HA, Snijders JM, Van Knapen F. 83.  1996. Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int. J. Food Microbiol. 30:37–53 [Google Scholar]
  84. Hurd HS, McKean JD, Griffith RW, Wesley IV, Rostagno MH. 84.  2002. Salmonella enterica infections in market swine with and without transport and holding. Appl. Environ. Microbiol. 68:2376–81 [Google Scholar]
  85. Callaway TR, Morrow JL, Edrington TS, Genovese KJ, Dowd S. 85.  et al. 2006. Social stress increases fecal shedding of Salmonella Typhimurium by early weaned piglets. Curr. Issues Intest. Microbiol. 7:65–71 [Google Scholar]
  86. Blecha F, Pollmann DS, Nichols DA. 86.  1983. Weaning pigs at an early age decreases cellular immunity. J. Anim. Sci. 56:396–400 [Google Scholar]
  87. Merlot E, Mounier AM, Prunier A. 87.  2011. Endocrine response of gilts to various common stressors: a comparison of indicators and methods of analysis. Physiol. Behav. 102:259–65 [Google Scholar]
  88. Murani E, Ponsuksili S, D'Eath RB, Turner SP, Evans G. 88.  et al. 2011. Differential mRNA expression of genes in the porcine adrenal gland associated with psychosocial stress. J. Mol. Endocrinol. 46:165–74 [Google Scholar]
  89. Dhabhar FS. 89.  2009. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation 16:300–17 [Google Scholar]
  90. Khansari DN, Murgo AJ, Faith RE. 90.  1990. Effects of stress on the immune system. Immunol. Today 11:170–75 [Google Scholar]
  91. Cho IJ, Lee NK, Hahm YT. 91.  2009. Characterization of Lactobacillus spp. isolated from the feces of breast-feeding piglets. J. Biosci. Bioeng. 108:194–98 [Google Scholar]
  92. Yin Q, Zheng Q. 92.  2005. Isolation and identification of the dominant Lactobacillus in gut and faeces of pigs using carbohydrate fermentation and 16S rDNA analysis. J. Biosci. Bioeng. 99:68–71 [Google Scholar]
  93. Proux K, Cariolet R, Fravalo P, Houdayer C, Keranflech A, Madec F. 93.  2001. Contamination of pigs by nose-to-nose contact or airborne transmission of Salmonella Typhimurium. Vet. Res. 32:591–600 [Google Scholar]
  94. Oliveira CJB, Garcia TB, Carvalho LFOS, Givisiez PEN. 94.  2007. Nose-to-nose transmission of Salmonella Typhimurium between weaned pigs. Vet. Microbiol. 125:355–61 [Google Scholar]
  95. Fedorka-Cray PJ, Kelley LC, Stabel TJ, Gray JT, Laufer JA. 95.  1995. Alternate routes of invasion may affect pathogenesis of Salmonella Typhimurium in swine. Infect. Immun. 63:2658–64 [Google Scholar]
  96. Wood RL, Pospischil A, Rose R. 96.  1989. Distribution of persistent Salmonella Typhimurium infection in internal organs of swine. Am. J. Vet. Res. 50:1015–21 [Google Scholar]
  97. Strockbine NA, Bopp CA, Fields PI, Kaper JB, Nataro JP. 97.  2015. Escherichia, Shigella, and Salmonella.. Manual of Clinical Microbiology J Jorgensen, MA Pfaller, K Carroll, G Funke, M Landry, et al. Washington, DC: ASM Press, 11th ed.. [Google Scholar]
  98. Mowat CG, Rothery E, Miles CS, McIver L, Doherty MK. 98.  et al. 2004. Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation. Nat. Struct. Mol. Biol. 11:1023–24 [Google Scholar]
  99. Bertin Y, Girardeau JP, Chaucheyras-Durand F, Lyan B, Pujos-Guillot E. 99.  et al. 2011. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ. Microbiol. 13:365–77 [Google Scholar]
  100. Thiennimitr P, Winter SE, Baumler AJ. 100.  2012. Salmonella, the host and its microbiota. Curr. Opin. Microbiol. 15:108–14 [Google Scholar]
  101. Obradors N, Badía J, Baldomà L, Aguilar J. 101.  1988. Anaerobic metabolism of the l-rhamnose fermentation product 1,2-propanediol in Salmonella typhimurium. J. Bacteriol. 170:2159–62 [Google Scholar]
  102. Staib L, Fuchs TM. 102.  2014. From food to cell: nutrient exploitation strategies of enteropathogens. Microbiology 160:1020–39 [Google Scholar]
  103. Derrien M, Vaughan EE, Plugge CM, de Vos WM. 103.  2004. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int. J. Syst. Evol. Microbiol. 54:1469–76 [Google Scholar]
  104. Klumpp J, Fuchs TM. 104.  2007. Identification of novel genes in genomic islands that contribute to Salmonella Typhimurium replication in macrophages. Microbiology 153:1207–20 [Google Scholar]
  105. Patterson SK, Borewicz K, Johnson T, Xu W, Isaacson RE. 105.  2012. Characterization and differential gene expression between two phenotypic phase variants in Salmonella enterica serovar Typhimurium. PLOS ONE 7:e43592 [Google Scholar]
  106. Nuccio SP, Baumler AJ. 106.  2014. Comparative analysis of Salmonella genomes identifies a metabolic network for escalating growth in the inflamed gut. mBio 5:e00929–14 [Google Scholar]
  107. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP. 107.  et al. 2009. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5:476–86 [Google Scholar]
  108. Borewicz KA, Kim HB, Singer RS, Gebhart CJ, Sreevatsan S. 108.  et al. 2015. Changes in the porcine intestinal microbiome in response to infection with Salmonella enterica and Lawsonia intracellularis. PLOS ONE 10:e0139106 [Google Scholar]
  109. Videnska P, Sisak F, Havlickova H, Faldynova M, Rychlik I. 109.  2013. Influence of Salmonella enterica serovar Enteritidis infection on the composition of chicken cecal microbiota. BMC Vet. Res. 9:140 [Google Scholar]
  110. Mon KK, Saelao P, Halstead MM, Chanthavixay G, Chang HC. 110.  et al. 2015. Salmonella enterica serovars Enteritidis infection alters the indigenous microbiota diversity in young layer chicks. Front. Vet. Sci. 2:61 [Google Scholar]
  111. Deatherage Kaiser BL, Li J, Sanford JA, Kim YM, Kronewitter SR. 111.  et al. 2013. A multi-omic view of host-pathogen-commensal interplay in Salmonella-mediated intestinal infection. PLOS ONE 8:e67155 [Google Scholar]
  112. Salyers AA, West SE, Vercellotti JR, Wilkins TD. 112.  1977. Fermentation of mucins and plant polysaccharides by anaerobic bacteria from the human colon. Appl. Environ. Microbiol. 34:529–33 [Google Scholar]
  113. Ganesh BP, Klopfleisch R, Loh G, Blaut M. 113.  2013. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella Typhimurium-infected gnotobiotic mice. PLOS ONE 8:e74963 [Google Scholar]
  114. Brogden KA, Guthmiller JM, Taylor CE. 114.  2005. Human polymicrobial infections. Lancet 365:253–55 [Google Scholar]
  115. Isaacson R, Kim HB. 115.  2012. The intestinal microbiome of the pig. Anim. Health Res. Rev. 13:100–9 [Google Scholar]
  116. Beloeil PA, Fravalo P, Fablet C, Jolly JP, Eveno E. 116.  et al. 2004. Risk factors for Salmonella enterica subsp. enterica shedding by market-age pigs in French farrow-to-finish herds. Prev. Vet. Med. 63:103–20 [Google Scholar]
  117. McOrist S, Gebhart CJ, Boid R, Barns SM. 117.  1995. Characterization of Lawsonia intracellularis gen. nov., sp. nov., the obligately intracellular bacterium of porcine proliferative enteropathy. Int. J. Syst. Bacteriol. 45:820–25 [Google Scholar]
  118. Lawson GH, Gebhart CJ. 118.  2000. Proliferative enteropathy. J. Comp. Pathol. 122:77–100 [Google Scholar]
  119. Schauder S, Shokat K, Surette MG, Bassler BL. 119.  2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41:463–76 [Google Scholar]
  120. Miller MB, Bassler BL. 120.  2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165–99 [Google Scholar]
  121. Clarke MB, Sperandio V. 121.  2005. Events at the host-microbial interface of the gastrointestinal tract III. Cell-to-cell signaling among microbial flora, host, and pathogens: There is a whole lot of talking going on. Am. J. Physiol. Gastrointest. Liver Physiol. 288:G1105–9 [Google Scholar]
  122. Kaper JB, Sperandio V. 122.  2005. Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect. Immun. 73:3197–209 [Google Scholar]
  123. Bearson BL, Bearson SM. 123.  2008. The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb. Pathog. 44:271–78 [Google Scholar]
  124. Lawley TD, Walker AW. 124.  2013. Intestinal colonization resistance. Immunology 138:1–11 [Google Scholar]
  125. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk L. 125.  1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. 69:405–11 [Google Scholar]
  126. Genovese KJ, Anderson RC, Harvey RB, Callaway TR, Poole TL. 126.  et al. 2003. Competitive exclusion of Salmonella from the gut of neonatal and weaned pigs. J. Food Prot. 66:1353–59 [Google Scholar]
  127. Rasschaert G, Michiels J, Tagliabue M, Missotten J, De Smet S, Heyndrickx M. 127.  2016. Effect of organic acids on Salmonella shedding and colonization in pigs on a farm with high Salmonella prevalence. J. Food Prot. 79:51–58 [Google Scholar]
  128. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. 128.  2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54:92325–40 [Google Scholar]
  129. Van Immerseel F, Russell JB, Flythe MD, Gantois I, Timbermont L. 129.  et al. 2006. The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathol. 35:3182–88 [Google Scholar]
  130. Lawhon SD, Maurer R, Suyemoto M, Altier C. 130.  2002. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46:51451–64 [Google Scholar]
  131. Sunkara LT, Jiang W, Zhang G. 131.  2012. Modulation of antimicrobial host defense peptide gene expression by free fatty acids. PLOS ONE 7:11e49558 [Google Scholar]
  132. Sunkara LT, Achanta M, Schreiber NB, Bommineni YR, Dai G. 132.  et al. 2011. Butyrate enhances disease resistance of chickens by inducing antimicrobial host defense peptide gene expression. PLOS ONE 6:11e27225 [Google Scholar]
  133. Kim HB, Isaacson RE. 133.  2015. The pig gut microbial diversity: understanding the pig gut microbial ecology through the next generation high throughput sequencing. Vet. Microbiol. 177:242–51 [Google Scholar]
  134. Tanner SA, Chassard C, Zihler Berner A, Lacroix C. 134.  2014. Synergistic effects of Bifidobacterium thermophilum RBL67 and selected prebiotics on inhibition of Salmonella colonization in the swine proximal colon PolyFermS model. Gut Pathog 6:44 [Google Scholar]
  135. Le Moal VL, Fayol-Messaoudi D, Servin AL. 135.  2013. Compound(s) secreted by Lactobacillus casei strain shirota YIT9029 irreversibly and reversibly impair the swimming motility of Helicobacter pylori and Salmonella enterica serovar Typhimurium, respectively. Microbiology 159:1956–71 [Google Scholar]
  136. Sabag-Daigle A, Blunk HM, Gonzalez JF, Steidley BL, Boyaka PN, Ahmer BM. 136.  2016. The use of attenuated but metabolically competent Salmonella as a probiotic to prevent or treat Salmonella infection. Infect. Immun. 84:72131–40 [Google Scholar]
  137. Casey PG, Gardiner GE, Casey G, Bradshaw B, Lawlor PG. 137.  et al. 2007. A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol. 73:1858–63 [Google Scholar]
  138. Revolledo L, Ferreira CS, Ferreira AJ. 138.  2009. Prevention of Salmonella Typhimurium colonization and organ invasion by combination treatment in broiler chicks. Poult. Sci. 88:734–43 [Google Scholar]
  139. Correa-Matos NJ, Donovan SM, Isaacson RE, Gaskins HR, White BA, Tappenden KA. 139.  2003. Fermentable fiber reduces recovery time and improves intestinal function in piglets following Salmonella typhimurium infection. J. Nutr. 133:1845–52 [Google Scholar]
  140. Raybaudi-Massilia RM, Mosqueda-Melgar J, Martín-Belloso O. 140.  2006. Antimicrobial activity of essential oils on Salmonella enteritidis, Escherichia coli, and Listeria innocua in fruit juices. J. Food Prot. 69:1579–86 [Google Scholar]
/content/journals/10.1146/annurev-animal-022516-022834
Loading
Salmonella in Swine: Microbiota Interactions
Annual Review of Animal Biosciences 5, 43 (2017); https://doi.org/10.1146/annurev-animal-022516-022834
/content/journals/10.1146/annurev-animal-022516-022834
/content/journals/10.1146/annurev-animal-022516-022834
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error