Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies

Giraud, Étienne; Baucheron, Sylvie; Cloeckaert, Axel

doi:10.1016/j.micinf.2005.12.025

Cited by 86 publications

(82 citation statements)

References 69 publications

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“…Nalidixic acid resistance is predictive of fluoroquinolone resistance, as observed in this study: all of the nalidixic acidresistant strains presented reduced ciprofloxacin susceptibility. Fluoroquinolone resistance is an important concern that is less frequently reported in Salmonella than in other food-borne pathogens [27]; however, Salmonella with reduced susceptibility to fluoroquinolone has been reported worldwide [28,29] and in Brazil [30,31]. In fact, to the best of our knowledge, this study is the first to report ESBLproducing strains of S. Corvallis with reduced ciprofloxacin susceptibility in Brazil.…”

Section: Discussionmentioning

confidence: 66%

Clonal relatedness and resistance patterns of Salmonella Corvallis from poultry carcasses in a Brazilian slaughterhouse

Yamatogi

Oliveira

Camargo

et al. 2015

J Infect Dev Ctries

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Introduction: Salmonella is a major cause of foodborne disease, and poultry products are important contributors to the transmission of this zoonotic pathogen. Although considered to be rare in most countries, Salmonella Corvallis has been reported in specific geographic areas isolated from both human and non-human sources. The aim of this study was to report the occurrence, the antimicrobial resistance profiles including the extended-spectrum beta-lactamase (ESBL) production, and the clonal relatedness of S. Corvallis strains. Methodology: A total of 132 fragments of poultry carcasses from a slaughterhouse in São Paulo State, Brazil, were collected at different stages of the manufacturing process (post-bleeding, post-plucking, and post-chilling) and analyzed for the presence of Salmonella. Antimicrobial resistance was determined by disc diffusion method and Etest. Clonal relatedness was determined by pulsed-field gel electrophoresis (PFGE). Results: Among the 272 Salmonella strains recovered, fourteen were S. Corvallis. Ten (71.4%) showed ESBL production and resistance to at least three antimicrobial agents. Nalidixic acid resistance and reduced ciprofloxacin susceptibility was verified in four (28.6%) strains. PFGE analyses showed that all the S. Corvallis strains belonged to the same pulsotype. Conclusion: This study identified genetically related S. Corvallis strains exhibiting ESBL production and reduced susceptibility to quinolone. The results suggest the need to improve the sanitary conditions in the slaughterhouse. Moreover, from a public health perspective, continuous surveillance on Salmonella is needed to control the dissemination of this important zoonotic pathogen and its resistance determinants.

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Section: Discussionmentioning

confidence: 66%

Clonal relatedness and resistance patterns of Salmonella Corvallis from poultry carcasses in a Brazilian slaughterhouse

Yamatogi

Oliveira

Camargo

et al. 2015

J Infect Dev Ctries

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“…According to Tenover et al (1995), the random occurrence of genetic events, such as point mutations, insertions and deletions in DNA, may change PFGE patterns during the course of an outbreak. In some cases, distinct serovars or PTs show similar genotypes due to mutations associated with antimicrobial resistance that can occur by selection pressure after inadequate doses of treatment (Giraud et al, 2006;Shukun et al, 2010). In addition, S. Enteritidis strains can alter their phenotypes without changing their genotypes, and this can be done by the acquisition of antimicrobial resistance mechanisms (Nauerby et al, 2000).…”

Section: Resultsmentioning

confidence: 99%

“…Thus, the use of antimicrobial agents in poultry farming may be the main cause for the increase and spread of resistant Salmonella strains (Giraud et al, 2006;Vaz et al, 2010;Souza et al, 2010).…”

Section: Characterization Of S Enteritidis Pt4 and Pt9mentioning

confidence: 99%

Molecular characterization and resistance profile of Salmonella Enteritidis PT4 and PT9 strains isolated in Brazil

Kottwitz

Scheffer

Dalla-Costa

et al. 2011

Journal of Medical Microbiology

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A total of 41 Salmonella Enteritidis strains, including phago-types (PTs) PT4 and PT9, were characterized by antimicrobial resistance profiles and PFGE. Of these strains, 34 were isolated from patients and foods, and 7 were of poultry origin. All strains were susceptible to ampicillin, chloramphenicol, cefotaxime, ciprofloxacin and trimethoprim/sulfamethoxazole, and 41.5 % (n517) were resistant to nalidixic acid. PFGE analysis using XbaI and SpeI restriction enzymes resulted in X1S1 as the prevalent pattern, which was present in 48.8 % (n520) of epidemic strains and in one strain isolated from discarded hatching eggs. Distinct patterns were found for the other strains isolated from poultry (X3S1, X8S8, X11S12, X11S13, X16S1 and X13S15). The S. Enteritidis PT9 strains associated with outbreaks of salmonellosis were highly similar (¢0.90), suggesting clonality. The PFGE genotypes were related to the PTs, and it was possible to differentiate strains isolated from patients with salmonellosis from other strains of non-epidemic origin. The PFGE results suggested that the S. Enteritidis strains of poultry origin were a possible source of human salmonellosis during the study period. INTRODUCTIONSalmonella species are associated with food-borne diseases worldwide. Foods of animal origin, such as poultry meat, eggs and their products, are frequently implicated in outbreaks (Clavijo et al., 2006). In the period 1999-2008, Salmonella species were responsible for 1408 (23.2 %) of the 6062 outbreaks investigated in Brazil, and Salmonella species were responsible for 267 (43. According to epidemiological data from the Central Laboratory of Parana State (LACEN), egg products were associated with 45.0 % of the salmonellosis outbreaks occurring from 1999 to 2008, and Salmonella enterica subsp. enterica serovar Enteritidis was the predominant serovar found in patient samples (87.8 %) and foods (80.6 %) .Phenotypic methods, such as phago-typing, antimicrobial resistance profiling and molecular methods, including analysis of the macrorestriction pattern of chromosomal DNA after PFGE, have been used to characterize S. Enteritidis strains. PFGE has been widely utilized in the molecular characterization of Salmonella species due to the stability of patterns, reproducibility and excellent discriminatory power (Ribot et al., 2002;Peters et al., 2003;Woo, 2005;Zou et al., 2010).Salmonella strains isolated from different sources in the same temporal period and from the same geographical location are likely to be epidemiologically related and to have an identical PFGE restriction pattern independent of the restriction enzyme employed (Tenover et al., 1995). PFGE is capable of discriminating strains of Salmonella of the same serovar and phago-type (PT) (Ahmed et al., 2000; Liebana et al., 2001).The aim of the present study was to characterize S. Enteritidis PT4 and PT9 strains of poultry origin or isolated from patients and foods involved in salmonellosis outbreaks by antimicrobial resistance profiles and PFGE patterns. An epidemiological co...

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“…Currently well-recognized mechanisms of quinolone resistance in Salmonella include target gene mutations, increased efflux pump activity, and plasmid-mediated protection of target topoisomerases (13,18). The contribution of changes in the cell envelope, including porin loss or alterations of the lipopolysaccharide (LPS), to quinolone resistance is currently unclear (14,29,36).…”

mentioning

confidence: 99%

Multiple Regulatory Pathways Associated with High-Level Ciprofloxacin and Multidrug Resistance in Salmonella enterica Serovar Enteritidis: Involvement of ramA and Other Global Regulators

O'Regan

Quinn

Pagès

et al. 2009

Antimicrob Agents Chemother

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Mechanisms of antibiotic resistance were examined in nalidixic acid-resistant Salmonella enterica serovar Enteritidis field isolates displaying decreased susceptibility to ciprofloxacin and in in vitro-derived ciprofloxacin-resistant mutants (104-cip and 5408-cip). All field isolates harbored a single gyrA mutation (D87Y). Deletion of acrB and complementation with wild-type gyrA increased quinolone susceptibility. Selection for ciprofloxacin resistance was associated with the development of an additional gyrA (S83F) mutation in 104-cip, novel gyrB (E466D) and parE (V461G) mutations in 5408-cip, overexpression of acrB and decreased susceptibility to nonquinolone antibiotics in both mutants, and decreased OmpF production and altered lipopolysaccharide in 104-cip. Complementation of mutated gyrA and gyrB with wild-type alleles restored susceptibility to quinolones in 104-cip and significantly decreased the ciprofloxacin MIC in 5408-cip. Complementation of parE had no effect on quinolone MICs. Deletion of acrB restored susceptibility to ciprofloxacin and other antibiotics tested. Both soxS and marA were overexpressed in 104-cip, and ramA was overexpressed in 5408-cip. Inactivation of each of these global regulators lowered ciprofloxacin MICs, decreased expression of acrB, and restored susceptibility to other antibiotics. Mutations were found in soxR (R20H) and in soxS (E52K) in 104-cip and in ramR (G25A) in 5408-cip. In conclusion, both efflux activity and a single gyrA mutation contribute to nalidixic acid resistance and reduced ciprofloxacin sensitivity. Ciprofloxacin resistance and decreased susceptibility to multiple antibiotics can result from different genetic events leading to development of target gene mutations, increased efflux activity resulting from differential expression of global regulators associated with mutations in their regulatory genes, and possible altered membrane permeability.

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Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies

Cited by 86 publications

References 69 publications

Clonal relatedness and resistance patterns of Salmonella Corvallis from poultry carcasses in a Brazilian slaughterhouse

Clonal relatedness and resistance patterns of Salmonella Corvallis from poultry carcasses in a Brazilian slaughterhouse

Molecular characterization and resistance profile of Salmonella Enteritidis PT4 and PT9 strains isolated in Brazil

Multiple Regulatory Pathways Associated with High-Level Ciprofloxacin and Multidrug Resistance in Salmonella enterica Serovar Enteritidis: Involvement of ramA and Other Global Regulators

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