Interference of Bifidobacterium choerinum or Escherichia coli Nissle 1917 with Salmonella Typhimurium in gnotobiotic piglets correlates with cytokine patterns in blood and intestine - PubMed (original) (raw)

Interference of Bifidobacterium choerinum or Escherichia coli Nissle 1917 with Salmonella Typhimurium in gnotobiotic piglets correlates with cytokine patterns in blood and intestine

A Splichalova et al. Clin Exp Immunol. 2011 Feb.

Abstract

The colonization, translocation and protective effect of two intestinal bacteria - PR4 (pig commensal strain of Bifidobacterium choerinum) or EcN (probiotic Escherichia coli strain Nissle 1917) - against subsequent infection with a virulent LT2 strain of Salmonella enterica serovar Typhimurium were studied in gnotobiotic pigs after oral association. The clinical state of experimental animals correlated with bacterial translocation and levels of inflammatory cytokines [a chemokine, interleukin (IL)-8, a proinflammatory cytokine, tumour necrosis factor (TNF)-α and an anti-inflammatory cytokine, IL-10] in plasma and intestinal lavages. Gnotobiotic pigs orally mono-associated with either PR4 or EcN thrived, and bacteria were not found in their blood. No significant inflammatory cytokine response was observed. Mono-association with Salmonella caused devastating septicaemia characterized by high levels of IL-10 and TNF-α in plasma and TNF-α in the intestine. Di-associated gnotobiotic pigs were given PR4 or EcN for 24 h. Subsequently, they were infected orally with Salmonella and euthanized 24 h later. Pigs associated with bifidobacteria before Salmonella infection suffered from severe systemic infection and mounted similar cytokine responses as pigs infected with Salmonella alone. In contrast, EcN interfered with translocation of Salmonella into mesenteric lymph nodes and systemic circulation. Pigs pre-associated with EcN thrived and their clinical condition correlated with the absence of IL-10 in their plasma and a decrease of TNF-α in plasma and ileum.

© 2010 The Authors. Clinical and Experimental Immunology © 2010 British Society for Immunology.

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Figures

Fig. 1

Fig. 1

Bacteria counts in blood, intestine and mesenteric lymph nodes (MLN) of gnotobiotic pigs. (a) Bifidobacterium choerinum in mono-associated pigs (PR4) or 1 day after subsequent infection with S. Typhimurium (PR4 + LT2). Bifidobacteria were not found in blood. Salmonella reduced the number of bifidobacteria in the colon (P < 0·001). (b) Escherichia coli Nissle 1917 in mono-associated pigs (EcN) or 1 day after subsequent infection with S. Typhimurium (EcN + LT2). E. coli was not found in blood. Its numbers were not influenced by Salmonella. *P < 0·05; **P < 0·01; ***P < 0·001.

Fig. 2

Fig. 2

Salmonella Typhimurium counts in blood, intestine and mesenteric lymph nodes (MLN) of gnotobiotic pigs. Salmonella counts in pigs infected with S. Typhimurium alone (LT2), pigs associated with B. choerinum and infected with S. Typhimurium (PR4 + LT2) or pigs associated with Escherichia coli Nissle 1917 and infected with S. Typhimurium (EcN + LT2). EcN protected piglets against bacteraemia. Salmonella counts were reduced in the ileum and mesenteric lymph nodes (P < 0·01) in the presence of EcN, and in the ileum (P < 0·01) and colon (P < 0·05) in the presence of PR4. *P < 0·05; **P < 0·01; ***P < 0·001.

Fig. 3

Fig. 3

Cytokine levels. Inflammatory cytokines were absent in plasma and intestinal lavages of germfree (GF) pigs. Interleukin (IL)-8 was absent in all plasma samples and IL-10 was absent in all intestinal lavages. (a) Plasma. High levels of IL-10 and tumour necrosis factor (TNF)-α were detected in gnotobiotic pigs infected with S. Typhimurium alone (LT2) and pigs associated with Bifidobacterium choerinum and infected with S. Typhimurium (PR4 + LT2). Lower levels of IL-10 (P < 0·05) and TNF-α (P < 0·01) were detected in pigs associated with Escherichia coli Nissle 1917 and infected with S. Typhimurium (EcN + LT2). (b) Ileum. High levels of IL-8 and TNF-α were found in gnotobiotic pigs infected with S. Typhimurium alone (LT2) and pigs associated with B. choerinum and infected with S. Typhimurium (PR4 + LT2). Lower levels of TNF-α (P < 0·01) were found in pigs associated with E. coli Nissle 1917 and infected with S. Typhimurium (EcN + LT2). (c) Colon. High levels of IL-8 were detected in pigs infected with Salmonella alone (LT2). Lower levels of IL-8 (P < 0·01) were found both in pigs associated with E. coli Nissle 1917 (EcN + LT2) or B. choerinum (PR4 + LT2) and infected with S. Typhimurium. *P < 0·05; **P < 0·01; ***P < 0·001.

Fig. 4

Fig. 4

Correlation between bacteraemia and plasma cytokines in piglets infected with Salmonella Typhimurium. Colony-forming units (CFU)/ml of S. Typhimurium were highly correlated with (a) interleukin (IL)-10 (Pearson's r = 0·909, P < 0·01) and (b) tumour necrosis factor (TNF)-α (Pearson's r = 0·769, P < 0·01).

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