Integron-mediated Multidrug Resistance in a Global Collection of Nontyphoidal Salmonella enterica Isolates

Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania 15261, USA.
Emerging Infectious Diseases (Impact Factor: 6.75). 04/2009; 15(3):388-96. DOI: 10.3201/eid1503.081131
Source: PubMed


Salmonella enterica bacteria have become increasingly resistant to antimicrobial agents, partly as a result of genes carried on integrons. Clonal expansion and horizontal gene transfer may contribute to the spread of antimicrobial drug-resistance integrons in these organisms. We investigated this resistance and integron carriage among 90 isolates with the ACSSuT phenotype (resistance to ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline) in a global collection of S. enterica isolates. Four integrons, dfrA12/orfF/aadA2, dfrA1/aadA1, dfrA7, and arr2/blaOXA30/cmlA5/aadA2, were found in genetically unrelated isolates from 8 countries on 4 continents, which supports a role for horizontal gene transfer in the global dissemination of S. enterica multidrug resistance. Serovar Typhimurium isolates containing identical integrons with the gene cassettes blaPSE1 and aadA2 were found in 4 countries on 3 continents, which supports the role of clonal expansion. This study demonstrates that clonal expansion and horizontal gene transfer contribute to the global dissemination of antimicrobial drug resistance in S. enterica.

Full-text preview

Available from: PubMed Central
  • Source
    • "These are inserted into the host bacterium's genome or plasmids, have an integrase gene, have cassettes and promoters bounded by IS elements, can mobilize their cassettes, and may have a variable number of genes inserted into the cassettes, including AR genes. While there are also several kinds of integrons detected in Salmonella isolated from animals in the U.S., the most prevalent is IntI1 and its variants , which often encode several AR genes and consequently may confer MDR phenotypes (White et al., 2003; Ebner et al., 2004; Gebreyes et al., 2004; Evershed et al., 2009; Krauland et al., 2009; Frye et al., 2011; Glenn et al., 2011; Lindsey et al., 2011a). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The prevalence of antimicrobial resistance (AR) in bacteria isolated from U.S. food animals has increased over the last several decades as have concerns of AR foodborne zoonotic human infections. Resistance mechanisms identified in U.S. animal isolates of Salmonella enterica included resistance to aminoglycosides (e.g. alleles of aacC, aadA, aadB, ant, aphA, and StrAB), -lactams (e.g. blaCMY-2, TEM-1, PSE-1), chloramphenicol (e.g. floR, cmlA, cat1, cat2), folate pathway inhibitors (e.g. alleles of sul and dfr), and tetracycline (e.g. alleles of tet(A), (B), (C), (D), (G) and tetR). In the U.S., multidrug resistance (MDR) mechanisms in Salmonella animal isolates were associated with integrons, or mobile genetic elements (MGEs) such as IncA/C plasmids which can be transferred among bacteria. It is thought that AR Salmonella originates in food animals and is transmitted through food to humans. However, some AR Salmonella isolated from humans in the U.S. have different AR elements than those isolated from food animals, suggesting a different etiology for some AR human infections. The AR mechanisms identified in isolates from outside the U.S. are also predominantly different. For example the extended spectrum -lactamases (ESBLs) are found in human and animal isolates globally; however, in the U.S., ESBLs thus far have only been found in human and not food animal isolates. Commensal bacteria in animals including Escherichia coli and Enterococcus spp. may be reservoirs for AR mechanisms. Many of the AR genes and MGEs found in E. coli isolated from U.S. animals are similar to those found in Salmonella. Enterococcus spp. isolated from animals frequently carry MGEs with AR genes, including resistances to aminoglycosides (e.g. alleles of aac, ant, and aph), macrolides (e.g. erm(A), erm(B),and msrC), and tetracyclines (e.g. tet(K), (L), (M), (O), (S)). Continuing investigations are required to help understand and mitigate the impact of AR bacteria on human and animal health.
    Frontiers in Microbiology 05/2013; 4:135. DOI:10.3389/fmicb.2013.00135 · 3.99 Impact Factor
  • Source
    • "Association between class 1 integrons and MDR has been established for a number of S. eneterica serotypes [1] [2] [3] [4] [5]. Surveillance and epidemiological studies demonstrated a considerable geographic variation in the prevalence and types of integrons among clinical isolates [1] [2] [4] [5]. However, there is a lack of information on the occurrence of class 1 integrons in Salmonella isolates in Armenia. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Screening of non-typhoidal Salmonella enterica clinical isolates (n=20) by PCR revealed the high prevalence of class 1 integrons (45%). Multidrug-resistant (MDR) phenotypes were observed in all integron-positive isolates, regardless of the serotype. A significant correlation was found between the MDR phenotype and the presence of class 1 integrons in the isolates, especially in S. Typhimurium.
  • Source
    • "Factors thought to play major roles in the spread of antimicrobial resistance include the misuse of antimicrobials as well as bacterial genetic factors including mobile genetic elements, such as plasmids and transposons (Barlow et al. 2004; Fluit and Schmitz 2004; Krauland et al. 2009). Integrons, although nonmobile themselves, are often present on transposons and plasmids and have been linked to the spread of antimicrobial resistance because of their ability to excise and integrate resistancegene cassettes from the environment or other bacteria (Barlow et al. 2004; Nogrady et al. 2006; Walsh et al. 2007; Martin et al. 2008; Krauland et al. 2009). Integrons have been identified among clinical isolates, in farm animals and in aquatic environments (Rosser and Young 1999; Liebana et al. 2002; Martin et al. 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: While considerable foodborne pathogen research has been conducted on conventionally produced broilers and turkeys, few studies have focused on free-range (organic) or pastured poultry. The current surveillance study was designed to isolate, identify and genetically characterize Salmonella from pastured poultry farm environment and from retail samples. In this study, 59 isolates were collected from two pastured poultry farms (n = 164; pens, feed, water and insect traps) and retail carcasses (n = 36) from a local natural foods store and a local processing plant. All isolates were serotyped and analysed phenotypically (antimicrobial resistance profiles) and genotypically (DNA fingerprints, plasmid profiles and integron analysis). Salmonella enterica was detected using standard microbiological methods. Salmonella Kentucky was the most prevalent serotype detected from the sampled sources (53%), followed by Salmonella Enteritidis (24%), Bareilly (10%), Mbandaka (7%), Montevideo (5%) or Newport (2%). All isolates were resistant to sulfisoxazole and novobiocin, and the majority (40/59) possessed class I integrons shown by PCR detection. Each Salmonella serotype elicited a distinct pulsed-field gel electrophoresis fingerprint profile, and unique differences were observed among the serotypes.  The findings of this study show that Salmonella serotypes isolated from pasture-raised poultry exhibit antimicrobial resistance and class I integrons.  This study demonstrates that despite the cessation of antibiotic usage in poultry production, antibiotic resistant Salmonella may still be recovered from the environment and poultry products.
    Journal of Applied Microbiology 12/2010; 109(6):1957-66. DOI:10.1111/j.1365-2672.2010.04825.x · 2.48 Impact Factor
Show more