Dissemination of non-typhoidal Salmonella during Plasmodium chabaudi infection affects anti-malarial immunity

Edrous Alamer, Victor H. Carpio, Akanni Adededji Abdoul Ibitokou, Michelle L. Kirtley, Inaia R. Phoenix, Michael M. Opata, Kyle D. Wilson, Yingzi Cong, Sara Dann-Grice, Ashok Chopra, Robin Stephens

Research output: Contribution to journalArticle

Abstract

Malaria-associated bacteremia accounts for up to one-third of deaths from severe malaria, and non-typhoidal Salmonella (NTS) has been reported as a major complication of severe malarial infection. Patients who develop NTS bacteremia during Plasmodium infection show higher mortality rates than individuals with malaria alone. Systemic bacteremia can be caused by a wound or translocation from epithelial or endothelial sites. NTS is an intestinal pathogen, however the contribution of bacterial translocation from the intestinal tract during Plasmodium infection is not well studied. Here, we investigated the integrity of the intestinal barrier function of P. chabaudi-infected mice using large molecules and Salmonella infection. Intestinal histology and the adaptive immune response to malaria were also studied using light microscopy and flow cytometry. P. chabaudi infection compromised intestinal barrier function, which led to increased intestinal cellular infiltration. In addition, we observed increased serum lipopolysaccharide binding protein and leakage of soluble molecules from the intestine into the blood in infected mice. Plasmodium infection also increased intestinal translocation and dissemination of NTS to the liver. The adaptive immune response to P. chabaudi infection was also significantly impacted by NTS translocation. Reduced B and T cell activation were observed in co-infected animals, suggesting interference in the malaria-specific immune responses by bacteremia. These studies demonstrate that P. chabaudi infection induces failure of the barrier function of the intestinal wall and enhanced intestinal bacterial translocation, affecting anti-malarial immunity.

Original languageEnglish (US)
JournalParasitology research
DOIs
StatePublished - Jan 1 2019

Fingerprint

Plasmodium chabaudi
antimalarials
Antimalarials
Salmonella
Malaria
Immunity
immunity
bacteremia
malaria
infection
Plasmodium
Bacteremia
Bacterial Translocation
intestines
Adaptive Immunity
mice
salmonellosis
blood serum
animal injuries
lipopolysaccharides

Keywords

  • Adaptive immunity
  • Malaria
  • Plasmodium
  • Salmonella
  • Translocation

ASJC Scopus subject areas

  • Parasitology
  • veterinary(all)
  • Insect Science
  • Infectious Diseases

Cite this

Dissemination of non-typhoidal Salmonella during Plasmodium chabaudi infection affects anti-malarial immunity. / Alamer, Edrous; Carpio, Victor H.; Ibitokou, Akanni Adededji Abdoul; Kirtley, Michelle L.; Phoenix, Inaia R.; Opata, Michael M.; Wilson, Kyle D.; Cong, Yingzi; Dann-Grice, Sara; Chopra, Ashok; Stephens, Robin.

In: Parasitology research, 01.01.2019.

Research output: Contribution to journalArticle

Alamer, Edrous ; Carpio, Victor H. ; Ibitokou, Akanni Adededji Abdoul ; Kirtley, Michelle L. ; Phoenix, Inaia R. ; Opata, Michael M. ; Wilson, Kyle D. ; Cong, Yingzi ; Dann-Grice, Sara ; Chopra, Ashok ; Stephens, Robin. / Dissemination of non-typhoidal Salmonella during Plasmodium chabaudi infection affects anti-malarial immunity. In: Parasitology research. 2019.
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AU - Opata, Michael M.

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AU - Stephens, Robin

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AB - Malaria-associated bacteremia accounts for up to one-third of deaths from severe malaria, and non-typhoidal Salmonella (NTS) has been reported as a major complication of severe malarial infection. Patients who develop NTS bacteremia during Plasmodium infection show higher mortality rates than individuals with malaria alone. Systemic bacteremia can be caused by a wound or translocation from epithelial or endothelial sites. NTS is an intestinal pathogen, however the contribution of bacterial translocation from the intestinal tract during Plasmodium infection is not well studied. Here, we investigated the integrity of the intestinal barrier function of P. chabaudi-infected mice using large molecules and Salmonella infection. Intestinal histology and the adaptive immune response to malaria were also studied using light microscopy and flow cytometry. P. chabaudi infection compromised intestinal barrier function, which led to increased intestinal cellular infiltration. In addition, we observed increased serum lipopolysaccharide binding protein and leakage of soluble molecules from the intestine into the blood in infected mice. Plasmodium infection also increased intestinal translocation and dissemination of NTS to the liver. The adaptive immune response to P. chabaudi infection was also significantly impacted by NTS translocation. Reduced B and T cell activation were observed in co-infected animals, suggesting interference in the malaria-specific immune responses by bacteremia. These studies demonstrate that P. chabaudi infection induces failure of the barrier function of the intestinal wall and enhanced intestinal bacterial translocation, affecting anti-malarial immunity.

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