Prevalence of Salmonella in Free-Range Pigs: Risk Factors and Intestinal Microbiota Composition

Abstract

Extensive pig systems are gaining importance as quality production systems and as the standard for sustainable rural development and animal welfare. However, the effects of natural foods on Salmonella epidemiology remain unknown. Herein, we assessed the presence of Salmonella and the composition of the gut microbiota in pigs from both Salmonella-free and high Salmonella prevalence farms. In addition, risk factors associated with the presence of Salmonella were investigated. The pathogen was found in 32.2% of animals and 83.3% of farms, showing large differences in prevalence between farms. Most isolates were serovars Typhimurium monophasic (79.3%) and Bovismorbificans (10.3%), and exhibited a multi-drug resistance profile (58.6%). Risk factor analysis identified feed composition, type/variety of vegetation available, and silos’ cleaning/disinfection as the main factors associated with Salmonella prevalence. Clear differences in the intestinal microbiota were found between Salmonella-positive and Salmonella-negative populations, showing the former with increasing Proteobacteria and decreasing Bacteroides populations. Butyrate and propionate producers including Clostridium, Turicibacter, Bacteroidaceae_uc, and Lactobacillus were more abundant in the Salmonella-negative group, whereas acetate producers like Sporobacter, Escherichia or Enterobacter were more abundant in the Salmonella-positive group. Overall, our results suggest that the presence of Salmonella in free-range pigs is directly related to the natural vegetation accessible, determining the composition of the intestinal microbiota.

Intestine microbiota and SCFAs response in naturally Cryptosporidium-infected plateau yaks

“…Those increased genera may have contributed greatly to diarrhea caused by Cryptosporidium. The lower abundance of genera in yaks was in accordance with the results revealing Turicibacter and Lactobacillus in Salmonella-infected pigs (Garrido et al, 2021), Akkermansia and Roseburiain in colitis in mouse (Bu et al, 2021;Li et al, 2021), Adlercreutzia in influenza virus-infected mouse (Lu et al, 2021), Faecalibacterium in pre-eclampsia people (Chen et al, 2020), Methanosphaera in sheep without treatment of anthelmintic (Moon et al, 2021), Slackia in Vogt-Koyanagi-Harada patients (Li et al, 2022a;Li et al, 2022b), Gemmiger in immune-mediated inflammatory people (Forbes et al, 2018), and Dorea in HIV patients . Those deficient genera in Cryptosporidium-infected animals may be the reason for diarrhea in yaks.…”

Inflammatory Responses Induced by the Monophasic Variant of Salmonella Typhimurium in Pigs Play a Role in the High Shedder Phenotype and Fecal Microbiota Composition

“…In addition, the load of Salmonella can increase after transport, confirming that this phase of the production is also a critical point for the control of Salmonella contamination ( 10 ). Among serotypes infecting pigs, the monophasic variant of Salmonella Typhimurium is now one of the most prevalent ( 11 – 13 ) with S. Derby or S. Typhimurium, and its zoonotic importance in human salmonellosis is also highlighted ( 1 , 14 ).…”

Roadmap for the integration of gastro‐intestinal (GI) tract microbiomes (human and domestic animal) in risk assessments under EFSA's remit

“…On the other hand, Salmonella modified the composition of the phyla depending on the gastrointestinal section. Indeed, in the feces, Salmonella induced an increase in the abundance of Proteobacteria and Firmicutes to the detriment of Bacteroidetes (Bearson et al, 2013;Garrido et al, 2021). While in the cecum, an increase in Proteobacteria and Bacteroidetes was associated with a decrease in Firmicutes (Bescucci et al, 2020) and finally in the colon, a decrease in Firmicutes was associated with an increase in Bacteroidetes (Bescucci et al, 2020).…”

“…The other study showed no change in performance (W. Zhang et al, 2019). Regarding the microbiota, the effect of Salmonella on bacterial diversity and richness gave rise to highly variable results (Argüello et al, 2018;Bearson et al, 2013;Drumo et al, 2015;Garrido et al, 2021;Holman et al, 2019;W. Zhang et al, 2017.…”

“…At the genus level, if Salmonella induced variable results on the abundance of lactic acid-producing bacteria (Argüello et al, 2018;Bescucci et al, 2020;Drumo et al, 2015;W. Zhang et al, 2017, it induced on the other hand an increase in the abundance of Phascolarctobacterium, a SCFA producing-bacteria (Bearson et al, 2013;Drumo et al, 2015;Garrido et al, 2021). Moreover, the presence of Salmonella was associated with a decrease in the abundance of Prevotella (Bearson et al, 2013; and an increase in the abundance of Oscillibacter (Bearson et al, 2013;Garrido et al, 2021).…”