Antimicrobial Resistance and Virulence Determinants in European Salmonella Genomic Island 1-Positive Salmonella enterica Isolates from Different Origins

ABSTRACTSalmonellagenomic island 1 (SGI1) contains a multidrug resistance region conferring the ampicillin-chloramphenicol-streptomycin-sulfamethoxazole-tetracycline resistance phenotype encoded byblaPSE-1,floR,aadA2,sul1, andtet(G). Its increasing spread via interbacterial transfer and the emergence of new variants are important public health concerns. We investigated the molecular properties of SGI1-carryingSalmonella entericaserovars selected from a European strain collection. A total of 38 strains belonging toS. entericaserovar Agona,S. entericaserovar Albany,S. entericaserovar Derby,S. entericaserovar Kentucky,S. entericaserovar Newport,S. entericaserovar Paratyphi B dT+, andS. entericaserovar Typhimurium, isolated between 2002 and 2006 in eight European countries from humans, animals, and food, were subjected to antimicrobial susceptibility testing, molecular typing methods (XbaI pulsed-field gel electrophoresis [PFGE], plasmid analysis, and multilocus variable-number tandem-repeat analysis [MLVA]), as well as detection of resistance and virulence determinants (PCR/sequencing and DNA microarray analysis). Typing experiments revealed wide heterogeneity inside the strain collection and even within serovars. PFGE analysis distinguished a total of 26 different patterns. In contrast, the characterization of the phenotypic and genotypic antimicrobial resistance revealed serovar-specific features. Apart from the classical SGI1 organization found in 61% of the strains, seven different variants were identified with antimicrobial resistance properties associated with SGI1-A (S. Derby), SGI1-C (S. Derby), SGI1-F (S. Albany), SGI1-L (S. Newport), SGI1-K (S. Kentucky), SGI1-M (S.Typhimurium), and, eventually, a novel variant similar to SGI1-C with additional gentamicin resistance encoded byaadB. Only minor serovar-specific differences among virulence patterns were detected. In conclusion, the SGI1 carriers exhibited pathogenetic backgrounds comparable to the ones published for susceptible isolates. However, because of their multidrug resistance, they may be more relevant in clinical settings.

Download Full-text

Antimicrobial Resistance in Salmonella in the United States from 1948 to 1995

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.02536-15 ◽

2016 ◽

Vol 60 (4) ◽

pp. 2567-2571 ◽

Cited By ~ 17

Author(s):

Daniel A. Tadesse ◽

Aparna Singh ◽

Shaohua Zhao ◽

Mary Bartholomew ◽

Niketta Womack ◽

...

Keyword(s):

United States ◽

Retrospective Study ◽

Multidrug Resistance ◽

Antimicrobial Resistance ◽

Salmonella Enterica ◽

Antimicrobial Agents ◽

The United States ◽

Content Type ◽

The Past ◽

The 1950S

ABSTRACTWe conducted a retrospective study of 2,149 clinicalSalmonellastrains to help document the historical emergence of antimicrobial resistance. There were significant increases in resistance to older drugs, including ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline, which were most common inSalmonella entericaserotype Typhimurium. An increase in multidrug resistance was observed for each decade since the 1950s. These data help show howSalmonellaevolved over the past 6 decades, after the introduction of new antimicrobial agents.

Download Full-text

Epidemiology of a Salmonella enterica subsp. enterica Serovar Typhimurium Strain Associated with a Songbird Outbreak

Applied and Environmental Microbiology ◽

10.1128/aem.01408-12 ◽

2012 ◽

Vol 78 (20) ◽

pp. 7290-7298 ◽

Cited By ~ 26

Author(s):

Sonia M. Hernandez ◽

Kevin Keel ◽

Susan Sanchez ◽

Eija Trees ◽

Peter Gerner-Smidt ◽

...

Keyword(s):

United States ◽

Salmonella Enterica ◽

Variable Number Tandem Repeat ◽

Variable Number ◽

Pfge Type ◽

Eastern United States ◽

Typing Method ◽

Content Type ◽

Typhimurium Strain ◽

Serovar Typhimurium

ABSTRACTSalmonella entericasubsp.entericaserovar Typhimurium is responsible for the majority of salmonellosis cases worldwide. ThisSalmonellaserovar is also responsible for die-offs in songbird populations. In 2009, there was anS. Typhimurium epizootic reported in pine siskins in the eastern United States. At the time, there was also a human outbreak with this serovar that was associated with contaminated peanuts. As peanuts are also used in wild-bird food, it was hypothesized that the pine siskin epizootic was related to this human outbreak. A comparison of songbird and humanS. Typhimurium pulsed-field gel electrophoresis (PFGE) patterns revealed that the epizootic was attributed not to the peanut-associated strain but, rather, to a songbird strain first characterized from an American goldfinch in 1998. This sameS. Typhimurium strain (PFGE type A3) was also identified in the PulseNet USA database, accounting for 137 of 77,941 totalS. Typhimurium PFGE entries. A second molecular typing method, multiple-locus variable-number tandem-repeat analysis (MLVA), confirmed that the same strain was responsible for the pine siskin epizootic in the eastern United States but was distinct from a genetically related strain isolated from pine siskins in Minnesota. The pine siskin A3 strain was first encountered in May 2008 in an American goldfinch and later in a northern cardinal at the start of the pine siskin epizootic. MLVA also confirmed the clonal nature ofS. Typhimurium in songbirds and established that the pine siskin epizootic strain was unique to the finch family. For 2009, the distribution of PFGE type A3 in passerines and humans mirrored the highest population density of pine siskins for the East Coast.

Download Full-text

Extensive Genetic Variability Linked to IS26Insertions in thefljBPromoter Region of Atypical Monophasic Variants of Salmonella enterica Serovar Typhimurium

Applied and Environmental Microbiology ◽

10.1128/aem.00270-15 ◽

2015 ◽

Vol 81 (9) ◽

pp. 3169-3175 ◽

Cited By ~ 11

Author(s):

Cécile Boland ◽

Sophie Bertrand ◽

Wesley Mattheus ◽

Katelijne Dierick ◽

Vicky Jasson ◽

...

Keyword(s):

Salmonella Enterica ◽

Promoter Region ◽

Variable Number Tandem Repeat ◽

Genetic Alterations ◽

Variable Number ◽

Genomic Region ◽

Phase 2 ◽

Pathogenic Potential ◽

Content Type ◽

Serovar Typhimurium

ABSTRACTFifty-nine monophasicSalmonella entericaserovar Typhimurium isolates, collected in Belgium during the period from 2008 to 2011, have been serotyped as 4,[5]:i:− and shown to harbor anfljBcoding sequence. The genetic differences between these strains and phenotypically biphasicSalmonellaTyphimurium were analyzed through PCR and DNA sequencing. Genetic alterations in thefljBpromoter region affecting expression of the phase 2 flagellin were observed in 53 isolates. Other genetic events in the invertible region carrying thefljBpromoter were observed in 2 isolates. For the remaining 4 isolates, no molecular differences with a reference biphasicSalmonellaTyphimurium strain could be observed. Next-generation sequencing of one representative isolate affected in thefljBpromoter region revealed a 26-kb IS26composite transposon insertion along with a local genomic rearrangement. Several other IS26element-mediated alterations of this genomic region were observed. This group of monophasicSalmonellaTyphimurium isolates was genetically heterogeneous, as revealed by multilocus variable-number tandem-repeat analysis (MLVA), PCR, and sequencing. Pigs and pork represented a major source of such monophasic isolates in Belgium, as reported in other countries. Three out of 5 isolates of human origin presented genetic profiles identical to those of food isolates, demonstrating the pathogenic potential of the newly characterized variants and potential dissemination along the food chain. This study highlighted the key role played by IS26insertions in the loss of phase 2 flagellin expression and the subsequent generation of multiple monophasic variant lineages from biphasicSalmonellaTyphimurium ancestors.

Download Full-text

Comparative Analysis of Subtyping Methods against a Whole-Genome-Sequencing Standard for Salmonella enterica Serotype Enteritidis

Journal of Clinical Microbiology ◽

10.1128/jcm.02332-14 ◽

2014 ◽

Vol 53 (1) ◽

pp. 212-218 ◽

Cited By ~ 69

Author(s):

Xiangyu Deng ◽

Nikki Shariat ◽

Elizabeth M. Driebe ◽

Chandler C. Roe ◽

Beth Tolar ◽

...

Keyword(s):

Whole Genome Sequencing ◽

Genome Sequencing ◽

Salmonella Enterica ◽

Variable Number Tandem Repeat ◽

The United States ◽

Variable Number ◽

Whole Genome ◽

Molecular Subtyping ◽

Content Type ◽

Sporadic Cases

A retrospective investigation was performed to evaluate whole-genome sequencing as a benchmark for comparing molecular subtyping methods forSalmonella entericaserotype Enteritidis and survey the population structure of commonly encounteredS. entericaserotype Enteritidis outbreak isolates in the United States. A total of 52S. entericaserotype Enteritidis isolates representing 16 major outbreaks and three sporadic cases collected between 2001 and 2012 were sequenced and subjected to subtyping by four different methods: (i) whole-genome single-nucleotide-polymorphism typing (WGST), (ii) multiple-locus variable-number tandem-repeat (VNTR) analysis (MLVA), (iii) clustered regularly interspaced short palindromic repeats combined with multi-virulence-locus sequence typing (CRISPR-MVLST), and (iv) pulsed-field gel electrophoresis (PFGE). WGST resolved all outbreak clusters and provided useful robust phylogenetic inference results with high epidemiological correlation. While both MLVA and CRISPR-MVLST yielded higher discriminatory power than PFGE, MLVA outperformed the other methods in delineating outbreak clusters whereas CRISPR-MVLST showed the potential to trace major lineages and ecological origins ofS. entericaserotype Enteritidis. Our results suggested that whole-genome sequencing makes a viable platform for the evaluation and benchmarking of molecular subtyping methods.

Download Full-text

Characterization of Salmonella enterica Serovar Typhimurium Isolates from Pigs and Pig Environment–Related Sources and Evidence of New Circulating Monophasic Strains in Spain

Journal of Food Protection ◽

10.4315/0362-028x.jfp-15-430 ◽

2016 ◽

Vol 79 (3) ◽

pp. 407-412 ◽

Cited By ~ 5

Author(s):

SARA ANDRÉS-BARRANCO ◽

JUAN PABLO VICO ◽

CLARA MARÍA MARÍN ◽

SILVIA HERRERA-LEÓN ◽

RAÚL CARLOS MAINAR-JAIME

Keyword(s):

Multidrug Resistance ◽

Tandem Repeat ◽

Salmonella Enterica ◽

Salmonella Enterica Serovar Typhimurium ◽

Variable Number Tandem Repeat ◽

Variable Number ◽

Multiple Locus ◽

Repeat Analysis ◽

Major Cluster ◽

Serovar Typhimurium

ABSTRACT A total of 117 Salmonella enterica serovar Typhimurium and 59 monophasic Salmonella Typhimurium (S. enterica serovar 4,[5],12:i:–) strains isolated between 2008 and 2012 from pig, wild bird, rodent, and farm environment samples from the northeast of Spain were characterized by phage typing, antibiotic susceptibility testing, and multiple-locus variable-number tandem repeat analysis in order to evaluate their phenotypic and genetic relatedness. In Salmonella 4,[5],12:i:–, the most prevalent phage types were U311 (40.7%) and DT195 (22%), which did not correspond with the so-called Spanish clone and generally showed a different resistance pattern (ASSuT). Antibiotic resistance was found in 85.8% of the isolates, with 94.1% of them displaying multidrug resistance. Multiple-locus variable-number tandem repeat analysis identified 92 different profiles, six of them shared by both serovars. The minimum spanning tree showed one major cluster that included 95% of the Salmonella 4,[5],12:i:– isolates, which came from different animal sources, geographic locations, and time periods, suggesting high clonality among those Salmonella strains and the ability to spread among pig farms. Overall, isolates of Salmonella 4,[5],12:i:– were more similar to European strains than to the well-characterized Spanish clone. The spread of these new strains of Salmonella 4,[5],12:i:– would likely have been favored by the important pig trade between this Spanish region and other European countries. The overall high prevalence of multidrug resistance observed in these new strains should be noted.

Download Full-text

Comparison between Salmonella enterica Serotype Enteritidis Genotyping Methods and Phage Type

Journal of Clinical Microbiology ◽

10.1128/jcm.01122-15 ◽

2015 ◽

Vol 53 (9) ◽

pp. 3021-3031 ◽

Cited By ~ 3

Author(s):

Alessandra De Cesare ◽

Keshav Krishnamani ◽

Antonio Parisi ◽

Antonia Ricci ◽

Ida Luzzi ◽

...

Keyword(s):

Salmonella Enterica ◽

Phage Type ◽

Variable Number Tandem Repeat ◽

Variable Number ◽

Quantitative Comparison ◽

Pulsed Field Gel Electrophoresis ◽

Typing Method ◽

Content Type ◽

Repeat Analysis ◽

Automated Ribotyping

A quantitative comparison between discriminatory indexes and concordance among multilocus variable-number tandem-repeat analysis (MLVA), pulsed-field gel electrophoresis (PFGE), automated ribotyping, and phage typing has been performed, testing 238Salmonella entericaserotype Enteritidis isolates not epidemiologically correlated. The results show that MLVA is the best choice, but each typing method provides a piece of information for establishing clonal relationships between the isolates.

Download Full-text

Multidrug Resistance Salmonella Genomic Island 1 in a Morganella morganii subsp. morganii Human Clinical Isolate from France

mSphere ◽

10.1128/msphere.00118-17 ◽

2017 ◽

Vol 2 (2) ◽

Cited By ~ 21

Author(s):

Eliette Schultz ◽

Olivier Barraud ◽

Jean-Yves Madec ◽

Marisa Haenni ◽

Axel Cloeckaert ◽

...

Keyword(s):

Public Health ◽

Multidrug Resistance ◽

Resistance Genes ◽

Salmonella Enterica ◽

Genomic Island ◽

Multidrug Resistant ◽

Health Concern ◽

Human Pathogens ◽

Morganella Morganii ◽

Content Type

ABSTRACT Since its initial identification in epidemic multidrug-resistant Salmonella enterica serovar Typhimurium DT104 strains, several SGI1 variants, SGI1 lineages, and SGI1-related elements (SGI2, PGI1, and AGI1) have been described in many bacterial genera (Salmonella, Proteus, Morganella, Vibrio, Shewanella, etc.). They constitute a family of multidrug resistance site-specific integrative elements acquired by horizontal gene transfer, SGI1 being the best-characterized element. The horizontal transfer of SGI1/PGI1 elements into other genera is of public health concern, notably with regard to the spread of critically important resistance genes such as ESBL and carbapenemase genes. The identification of SGI1 in Morganella morganii raises the issue of (i) the potential for SGI1 to emerge in other human pathogens and (ii) its bacterial host range. Further surveillance and research are needed to understand the epidemiology, the spread, and the importance of the members of this SGI1 family of integrative elements in contributing to antibiotic resistance development. Salmonella genomic island 1 (SGI1) is a multidrug resistance integrative mobilizable element that harbors a great diversity of antimicrobial resistance gene clusters described in numerous Salmonella enterica serovars and also in Proteus mirabilis. A serious threat to public health was revealed in the recent description in P. mirabilis of a SGI1-derivative multidrug resistance island named PGI1 (Proteus genomic island 1) carrying extended-spectrum-β-lactamase (ESBL) and metallo-β-lactamase resistance genes, bla VEB-6 and bla NDM-1, respectively. Here, we report the first description of Salmonella genomic island 1 (SGI1) in a multidrug-resistant clinical Morganella morganii subsp. morganii strain isolated from a patient in France in 2013. Complete-genome sequencing of the strain revealed SGI1 variant SGI1-L carrying resistance genes dfrA15, floR, tetA(G), bla PSE-1 (now referred to as bla CARB-2), and sul1, conferring resistance to trimethoprim, phenicols, tetracyclines, amoxicillin, and sulfonamides, respectively. The SGI1-L variant was integrated into the usual chromosome-specific integration site at the 3′ end of the trmE gene. Beyond Salmonella enterica and Proteus mirabilis, the SGI1 integrative mobilizable element may thus also disseminate its multidrug resistance phenotype in another genus belonging to the Proteae tribe of the family Enterobacteriaceae. IMPORTANCE Since its initial identification in epidemic multidrug-resistant Salmonella enterica serovar Typhimurium DT104 strains, several SGI1 variants, SGI1 lineages, and SGI1-related elements (SGI2, PGI1, and AGI1) have been described in many bacterial genera (Salmonella, Proteus, Morganella, Vibrio, Shewanella, etc.). They constitute a family of multidrug resistance site-specific integrative elements acquired by horizontal gene transfer, SGI1 being the best-characterized element. The horizontal transfer of SGI1/PGI1 elements into other genera is of public health concern, notably with regard to the spread of critically important resistance genes such as ESBL and carbapenemase genes. The identification of SGI1 in Morganella morganii raises the issue of (i) the potential for SGI1 to emerge in other human pathogens and (ii) its bacterial host range. Further surveillance and research are needed to understand the epidemiology, the spread, and the importance of the members of this SGI1 family of integrative elements in contributing to antibiotic resistance development.

Download Full-text

Chromosome-Mediated Multidrug Resistance in Salmonella enterica Serovar Typhi

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.04081-14 ◽

2014 ◽

Vol 59 (1) ◽

pp. 721-723 ◽

Cited By ~ 15

Author(s):

Chien-Shun Chiou ◽

Munirul Alam ◽

Jung-Che Kuo ◽

Yen-Yi Liu ◽

Pei-Jen Wang

Keyword(s):

Multidrug Resistance ◽

Resistance Genes ◽

Salmonella Enterica ◽

Genomic Island ◽

Multidrug Resistant ◽

First Line ◽

Content Type ◽

Salmonella Enterica Serovar Typhi

ABSTRACTA salmonella genomic island, designated SGI11, was found in 18 of 26 multidrug-resistantSalmonella entericaserovar Typhi isolates from Bangladesh. SGI11 was an IS1composite transposon and carried 7 resistance genes that conferred resistance to 5 first-line antimicrobials. Eleven of the 18 SGI11-carryingS. Typhi isolates had developed resistance to high levels of ciprofloxacin.

Download Full-text

Predominant Mycobacterium tuberculosis Families and High Rates of Recent Transmission among New Cases Are Not Associated with Primary Multidrug Resistance in Lima, Peru

Journal of Clinical Microbiology ◽

10.1128/jcm.03585-14 ◽

2015 ◽

Vol 53 (6) ◽

pp. 1854-1863 ◽

Cited By ~ 17

Author(s):

Francesca Barletta ◽

Larissa Otero ◽

Bouke C. de Jong ◽

Tomotada Iwamoto ◽

Kentaro Arikawa ◽

...

Keyword(s):

Mycobacterium Tuberculosis ◽

Multidrug Resistance ◽

Variable Number Tandem Repeat ◽

Drug Susceptibility ◽

Variable Number ◽

Content Type ◽

Recent Transmission ◽

Study Population ◽

High Level ◽

A Prospective Study

Sputum samples from new tuberculosis (TB) cases were collected over 2 years as part of a prospective study in the northeastern part of Lima, Peru. To measure the contribution of recent transmission to the high rates of multidrug resistance (MDR) in this area,Mycobacterium tuberculosiscomplex (MTBc) isolates were tested for drug susceptibility to first-line drugs and were genotyped by spoligotyping and 15-locus mycobacterial interspersed repetitive-unit (MIRU-15)-variable-number tandem repeat (VNTR) analysis. MDR was found in 6.8% of 844 isolates, of which 593 (70.3%) were identified as belonging to a known MTBc lineage, whereas 198 isolates (23.5%) could not be assigned to these lineages and 12 (1.4%) represented mixed infections. Lineage 4 accounted for 54.9% (n= 463) of the isolates, most of which belonged to the Haarlem family (n= 279). MIRU-15 analysis grouped 551/791 isolates (69.7%) in 102 clusters, with sizes ranging from 2 to 46 strains. The overall high clustering rate suggests a high level of recent transmission in this population, especially among younger patients (odds ratio [OR], 1.6;P= 0.01). Haarlem strains were more prone to cluster, compared to the other families taken together (OR, 2.0;P< 0.0001), while Beijing (OR, 0.6;P= 0.006) and LAM (OR, 0.7;P= 0.07) strains clustered less. Whereas streptomycin-resistant strains were more commonly found in clusters (OR, 1.8;P= 0.03), clustering rates did not differ between MDR and non-MDR strains (OR, 1.8;P= 0.1). Furthermore, only 16/51 MDR strains clustered with other MDR strains, suggesting that patients with primary MDR infections acquired the infections mostly from index cases outside the study population, such as retreated cases.

Download Full-text

Draft Genome Sequences of Salmonella enterica subsp. enterica Serovar Dublin Strains from St. Nectaire and Morbier Cheeses Characterized by Multilocus Variable-Number Tandem-Repeat Analysis Profiles Associated with Two Fatal Outbreaks in France

Microbiology Resource Announcements ◽

10.1128/mra.01361-18 ◽

2019 ◽

Vol 8 (1) ◽

Cited By ~ 3

Author(s):

Sabrina Cadel-Six ◽

Marie-Leone Vignaud ◽

Manal Mohammed

Keyword(s):

Tandem Repeat ◽

Salmonella Enterica ◽

Draft Genome ◽

Variable Number Tandem Repeat ◽

Variable Number ◽

Genome Sequences ◽

Content Type ◽

Repeat Analysis

We report here the draft genome sequences of 2 Salmonella enterica subsp. enterica serovar Dublin strains from St. Nectaire and Morbier cheeses having multilocus variable-number tandem-repeat analysis (MLVA) profiles identified during the fatal outbreaks that occurred in France in 2012 and 2015 to 2016, respectively.

Download Full-text