Phenotypic and Genotypic Features of a Salmonella Heidelberg Strain Isolated in Broilers in Brazil and Their Possible Association to Antibiotics and Short-Chain Organic Acids Resistance and Susceptibility

Abstract

Salmonella enterica serovar Heidelberg is a human pathogen also found in broilers. A strain (UFPR1) has been associated with field reports of resistance to short-chain organic acids (SCOA) in broilers in the South of Brazil, but was susceptible to a Bacillus subtilis-based probiotic added in feed in a related study. This work aimed to (i) report clinical symptoms caused by SH UFPR1 in broilers, (ii) study its susceptibility to some antibiotics in vitro, and (iii) SCOA in vivo; and (iv) relate these phenotypic observations with its genome characteristics. Two in vivo trials used 1-day-old chicks housed for 21 days in 8 sterilized isolated negative pressure rooms with 4 battery cages of 12 birds each. Birds were challenged or not with 107 CFU/bird of SH UFPR1 orally and exposed or not to SCOA in a 2 × 2 factorial design. Zootechnical parameters were unaffected (P > 0.05), no clinical signs were observed, and few cecal and hepatic histologic and immune-related alterations were seen, in birds challenged with SH. Formic and propionic acids added together in drinking water, fumaric and benzoic acid in feed (Trial 1), and coated calcium butyrate in feed (Trial 2) did not reduce the SH isolation frequencies seen in cecum and liver in broilers after SH challenge (P > 0.05). SH UFPR1 was susceptible to amikacin, amoxicillin + clavulanate, ceftiofur, cephalexin, doxycycline and oxytetracycline; and mildly susceptible to ampicillin + sulbactam, cephalothin, ciprofloxacin, enrofloxacin, and gentamycin in an in vitro minimum inhibitory concentration model using Mueller–Hinton agar. The whole genome of SH UFPR1 was sequenced and consisted of a circular chromosome, spanning 4,760,321 bp with 52.18% of GC-content encoding 84 tRNA, 22 rRNA, and 4,427 protein-coding genes. The comparison between SH UFPR1 genome and a multidrug-resistant SL476 strain revealed 11 missing genomic fragments and 5 insertions related to bgt, bgr, and rpoS genes. The deleted genes codify proteins associated with cell cycle regulation, virulence, drug resistance, cellular adhesion, and salt efflux which collectively reveal key aspects of the evolution and adaptation of SH strains such as organic acids resistance and antibiotic sensitivity and provide information relevant to the control of SH in poultry.

Characterization and whole genome sequencing of closely related multidrug-resistant Salmonella enterica serovar Heidelberg isolates from imported poultry meat in the Netherlands

“…The environmental persistence of MDR S . Heidelberg in poultry farms may allow for continued exposure and the often asymptomatic infection of live poultry [46, 47]. Another reason that allowed these S .…”

Salmonella Typhimurium Vaccine to Control a Brazilian Salmonella Heidelberg Strain in Broiler Chickens

“…In some situations, IL-10 could act as a chemoattractant to CD8+ T cells (JINQUAN et al, 1993;XI et al, 2017), activate cytotoxic T cell activity (SANTIN et al, 2000), and increase the maturation of CD8+ T memory cells (LAIDLAW et al, 2015). Shanmugasundaram et al, (2015) and Kogut et al, (2016) have observed that Tregulatory cells increase expression of IL-10 cells after Salmonella infection, which suggests a "tolerogenic" response allowing the bacteria to persist in the lumen. Like the vaccine, this could be a mechanism to inhibit colonization, since maintaining the live vaccine in the lumen could have inhibited colonization after the Salmonella challenge.…”

“…The Brazilian SH strain (UFPR1) used in this trial was isolated from commercial broiler carcasses in the south of Brazil. A recent study reported its complete genome associated with high and intermediate resistance against short-chain organic acids and some antibiotics, respectively (SANTIN et al, 2017).…”

Emergence, Dissemination and Antimicrobial Resistance of the Main Poultry-Associated Salmonella Serovars in Brazil

“…This serovar has also shown AMR to several antibiotics, raising concern among veterinary and public health authorities [69,191,192]. Most S. Heidelberg strains are resistant to tetracycline, nalidixic acid, and ampicillin, as well as some other antimicrobials [49,69,135,[193][194][195][196][197][198] (Table 1). Furthermore, an MDR profile has been common in most isolates [49,135,194,195,197].…”