Daily intake of household-produced milk kefir on Salmonella Typhimurium infection in C57BL/6 mice: mortality, microbiota modulation, and immunological implications

J Appl Microbiol. 2024 Nov 4;135(11):lxae249. doi: 10.1093/jambio/lxae249.

Abstract

Aims: Salmonellosis, a major global cause of diarrheal diseases, significantly impacts the intestinal microbiome. Probiotic-rich beverages, such as kefir, are increasingly utilized as alternative health-promoting beverages associated with various microbiota benefits. This study investigated the repercussions of daily consumption of household-produced milk kefir on Salmonella enterica serovar Typhimurium infection in C57BL-6 mice.

Methods and results: Kefir consumption pre-infection reduced the presence of inflammatory cells in the colon and altered the cytokine profile by reducing IL-10 and increasing IFN-γ. Despite reducing intestinal inflammation, kefir intake did not yield a prompt response to an acute infection caused by the aggressive pathogen Salmonella. This contributed to increased mortality in the mice, evidenced by higher fecal Salmonella counts post-infection. Metabarcoding analysis demonstrated that the use of kefir before infection increases butyric acid by the higher abundance of Lachnospiraceae and Prevotellaceae families and genus in feces, coupled with an increase in Muribaculaceae family and Bacteroides genus among infected kefir-treated mice. While kefir hinted at microbiota alterations reducing enterobacteria (Helicobacter), decrease IL-10, and increased IFN-γ, butyric acid on pre-infection, the beverage potentially facilitated the systemic translocation of pathogens, intensifying the infection's severity by altering the immune response.

Conclusions: The use of kefir in the dosage of 10% w/v (109 CFU), for acute infections with Salmonella Typhimurium, may not be enough to combat the infection and worsen the prognosis, leaving the intestine less inflamed, favoring the replication and translocation of the pathogen. These findings underscore the importance of prudently evaluating the widespread use of probiotics and probiotic-rich beverages, especially during acute infections, given their potential association with adverse effects during these diseases.

Keywords: Salmonella; fermented foods; foodborne illnesses; foodborne pathogens; intestinal microbiology; microbiota; probiotics.

MeSH terms

  • Animals
  • Colon / microbiology
  • Cytokines / metabolism
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome*
  • Interleukin-10 / metabolism
  • Kefir* / microbiology
  • Mice
  • Mice, Inbred C57BL*
  • Milk / microbiology
  • Probiotics
  • Salmonella Infections / microbiology
  • Salmonella Infections / prevention & control
  • Salmonella Infections, Animal / immunology
  • Salmonella Infections, Animal / microbiology
  • Salmonella Infections, Animal / prevention & control
  • Salmonella typhimurium*

Substances

  • Interleukin-10
  • Cytokines