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Diversity in bacterium-host interactions within the species Helicobacter heilmannii sensu stricto.

Joosten M, Blaecher C, Flahou B, Ducatelle R, Haesebrouck F, Smet A - Vet. Res. (2013)

Bottom Line: A reduced antral expression of H+/K+ ATPase was seen in the stomach after infection with 3 highly colonizing strains and 2 highly colonizing strains caused an increased gastrin expression in the fundus.In none of the H. heilmannii s.s.-infected groups, IFN-γ expression was up-regulated.This study demonstrates diversity in bacterium-host interactions within the species H. heilmannii s.s. and that the pathogenesis of gastric infections with this microorganism is not identical to that of an H. pylori infection.

View Article: PubMed Central - HTML - PubMed

ABSTRACT
Helicobacter (H.) heilmannii sensu stricto (s.s.) is a zoonotic bacterium that naturally colonizes the stomach of dogs and cats. In humans, this microorganism has been associated with gastritis, peptic ulcer disease and mucosa associated lymphoid tissue (MALT) lymphoma. Little information is available about the pathogenesis of H. heilmannii s.s. infections in humans and it is unknown whether differences in virulence exist within this species. Therefore, a Mongolian gerbil model was used to study bacterium-host interactions of 9 H. heilmannii s.s. strains. The colonization ability of the strains, the intensity of gastritis and gene expression of various inflammatory cytokines in the stomach were determined at 9 weeks after experimental infection. The induction of an antrum-dominant chronic active gastritis with formation of lymphocytic aggregates was shown for 7 strains. High-level antral colonization was seen for 4 strains, while colonization of 4 other strains was more restricted and one strain was not detected in the stomach at 9 weeks post infection. All strains inducing a chronic active gastritis caused an up-regulation of the pro-inflammatory cytokine IL-1β in the antrum. A reduced antral expression of H+/K+ ATPase was seen in the stomach after infection with 3 highly colonizing strains and 2 highly colonizing strains caused an increased gastrin expression in the fundus. In none of the H. heilmannii s.s.-infected groups, IFN-γ expression was up-regulated. This study demonstrates diversity in bacterium-host interactions within the species H. heilmannii s.s. and that the pathogenesis of gastric infections with this microorganism is not identical to that of an H. pylori infection.

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Colonization capacity of H. heilmannii s.s. strains and gastric inflammation score after experimental infection. Colonization capacity is shown as log10 values of H. heilmannii s.s. bacteria per mg tissue, detected with quantitative RT-PCR in the fundus (a) and the antrum (c) of the stomach and the duodenum (b). Results below detection limit (log 2.39 bacteria per mg tissue) were set as 0. Antral inflammation (d) was scored on a scale of 0 to 4 (0: no infiltration with mononuclear and/or polymorphonuclear cells; 1: mild diffuse infiltration with mononuclear and/or polymorphonuclear cells or the presence of one small (50–200 cells) aggregate of inflammatory cells; 2: moderate diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of 2–4 inflammatory aggregates; 3: marked diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of at least five inflammatory aggregates; 4: diffuse infiltration of large regions with large aggregates of mononuclear and/or polymorphonuclear cells).Individual gerbils are depicted as figures around the mean (lines). Statistical significant differences compared to control animals are indicated by * (Mann-Whitney U test, p < 0.05).
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Figure 2: Colonization capacity of H. heilmannii s.s. strains and gastric inflammation score after experimental infection. Colonization capacity is shown as log10 values of H. heilmannii s.s. bacteria per mg tissue, detected with quantitative RT-PCR in the fundus (a) and the antrum (c) of the stomach and the duodenum (b). Results below detection limit (log 2.39 bacteria per mg tissue) were set as 0. Antral inflammation (d) was scored on a scale of 0 to 4 (0: no infiltration with mononuclear and/or polymorphonuclear cells; 1: mild diffuse infiltration with mononuclear and/or polymorphonuclear cells or the presence of one small (50–200 cells) aggregate of inflammatory cells; 2: moderate diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of 2–4 inflammatory aggregates; 3: marked diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of at least five inflammatory aggregates; 4: diffuse infiltration of large regions with large aggregates of mononuclear and/or polymorphonuclear cells).Individual gerbils are depicted as figures around the mean (lines). Statistical significant differences compared to control animals are indicated by * (Mann-Whitney U test, p < 0.05).

Mentions: The stomach of all control animals showed a normal histomorphology (Figure 1a). Inflammation in the stomach of gerbils infected with H. heilmannii s.s. strains ASB1, ASB2, ASB3, ASB6, ASB11, ASB13 and ASB14 was marked by a chronic active gastritis with formation of lymphocytic aggregates in the lamina propria and submucosa of the antrum of the stomach (Figure 1b). The mucosal thickness was slightly increased and only few neutrophils were detected. In contrast, H. heilmannii s.s. strains ASB7 and ASB9 did not cause explicit antral inflammation and only a mild increase in lymphocytic cell number was observed in the lamina propria of the antrum of the stomach (Figure 1c). In all H. heilmannii s.s.-infected gerbils, only limited signs of inflammation were detected in the fundus of the stomach (Additional file 1). The antral inflammation scores of each individual animal are shown in Figure 2d. A statistically significant difference between inflammation scores for gerbils inoculated with ASB1, ASB2, ASB3, ASB6, ASB11, ASB13 and ASB14 compared with the control group was demonstrated (Mann-Whitney U test, p < 0.05, Figure 2d).


Diversity in bacterium-host interactions within the species Helicobacter heilmannii sensu stricto.

Joosten M, Blaecher C, Flahou B, Ducatelle R, Haesebrouck F, Smet A - Vet. Res. (2013)

Colonization capacity of H. heilmannii s.s. strains and gastric inflammation score after experimental infection. Colonization capacity is shown as log10 values of H. heilmannii s.s. bacteria per mg tissue, detected with quantitative RT-PCR in the fundus (a) and the antrum (c) of the stomach and the duodenum (b). Results below detection limit (log 2.39 bacteria per mg tissue) were set as 0. Antral inflammation (d) was scored on a scale of 0 to 4 (0: no infiltration with mononuclear and/or polymorphonuclear cells; 1: mild diffuse infiltration with mononuclear and/or polymorphonuclear cells or the presence of one small (50–200 cells) aggregate of inflammatory cells; 2: moderate diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of 2–4 inflammatory aggregates; 3: marked diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of at least five inflammatory aggregates; 4: diffuse infiltration of large regions with large aggregates of mononuclear and/or polymorphonuclear cells).Individual gerbils are depicted as figures around the mean (lines). Statistical significant differences compared to control animals are indicated by * (Mann-Whitney U test, p < 0.05).
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Related In: Results  -  Collection

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Figure 2: Colonization capacity of H. heilmannii s.s. strains and gastric inflammation score after experimental infection. Colonization capacity is shown as log10 values of H. heilmannii s.s. bacteria per mg tissue, detected with quantitative RT-PCR in the fundus (a) and the antrum (c) of the stomach and the duodenum (b). Results below detection limit (log 2.39 bacteria per mg tissue) were set as 0. Antral inflammation (d) was scored on a scale of 0 to 4 (0: no infiltration with mononuclear and/or polymorphonuclear cells; 1: mild diffuse infiltration with mononuclear and/or polymorphonuclear cells or the presence of one small (50–200 cells) aggregate of inflammatory cells; 2: moderate diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of 2–4 inflammatory aggregates; 3: marked diffuse infiltration with mononuclear and/or polymorphonuclear cells and/or the presence of at least five inflammatory aggregates; 4: diffuse infiltration of large regions with large aggregates of mononuclear and/or polymorphonuclear cells).Individual gerbils are depicted as figures around the mean (lines). Statistical significant differences compared to control animals are indicated by * (Mann-Whitney U test, p < 0.05).
Mentions: The stomach of all control animals showed a normal histomorphology (Figure 1a). Inflammation in the stomach of gerbils infected with H. heilmannii s.s. strains ASB1, ASB2, ASB3, ASB6, ASB11, ASB13 and ASB14 was marked by a chronic active gastritis with formation of lymphocytic aggregates in the lamina propria and submucosa of the antrum of the stomach (Figure 1b). The mucosal thickness was slightly increased and only few neutrophils were detected. In contrast, H. heilmannii s.s. strains ASB7 and ASB9 did not cause explicit antral inflammation and only a mild increase in lymphocytic cell number was observed in the lamina propria of the antrum of the stomach (Figure 1c). In all H. heilmannii s.s.-infected gerbils, only limited signs of inflammation were detected in the fundus of the stomach (Additional file 1). The antral inflammation scores of each individual animal are shown in Figure 2d. A statistically significant difference between inflammation scores for gerbils inoculated with ASB1, ASB2, ASB3, ASB6, ASB11, ASB13 and ASB14 compared with the control group was demonstrated (Mann-Whitney U test, p < 0.05, Figure 2d).

Bottom Line: A reduced antral expression of H+/K+ ATPase was seen in the stomach after infection with 3 highly colonizing strains and 2 highly colonizing strains caused an increased gastrin expression in the fundus.In none of the H. heilmannii s.s.-infected groups, IFN-γ expression was up-regulated.This study demonstrates diversity in bacterium-host interactions within the species H. heilmannii s.s. and that the pathogenesis of gastric infections with this microorganism is not identical to that of an H. pylori infection.

View Article: PubMed Central - HTML - PubMed

ABSTRACT
Helicobacter (H.) heilmannii sensu stricto (s.s.) is a zoonotic bacterium that naturally colonizes the stomach of dogs and cats. In humans, this microorganism has been associated with gastritis, peptic ulcer disease and mucosa associated lymphoid tissue (MALT) lymphoma. Little information is available about the pathogenesis of H. heilmannii s.s. infections in humans and it is unknown whether differences in virulence exist within this species. Therefore, a Mongolian gerbil model was used to study bacterium-host interactions of 9 H. heilmannii s.s. strains. The colonization ability of the strains, the intensity of gastritis and gene expression of various inflammatory cytokines in the stomach were determined at 9 weeks after experimental infection. The induction of an antrum-dominant chronic active gastritis with formation of lymphocytic aggregates was shown for 7 strains. High-level antral colonization was seen for 4 strains, while colonization of 4 other strains was more restricted and one strain was not detected in the stomach at 9 weeks post infection. All strains inducing a chronic active gastritis caused an up-regulation of the pro-inflammatory cytokine IL-1β in the antrum. A reduced antral expression of H+/K+ ATPase was seen in the stomach after infection with 3 highly colonizing strains and 2 highly colonizing strains caused an increased gastrin expression in the fundus. In none of the H. heilmannii s.s.-infected groups, IFN-γ expression was up-regulated. This study demonstrates diversity in bacterium-host interactions within the species H. heilmannii s.s. and that the pathogenesis of gastric infections with this microorganism is not identical to that of an H. pylori infection.

Show MeSH
Related in: MedlinePlus