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Antimicrobial resistance and genomic characterization of Salmonella enterica isolates from chicken meat.

ABSTRACT: This study investigated genotypic and phenotypic antimicrobial resistance profiles, phylogenic relatedness, plasmid and virulence composition of 39 Salmonella enterica strains isolated from chicken meat samples using whole genome sequencing (WGS) technology. Four distinct serotypes were identified; Salmonella Minnesota (16/39, 41%), Salmonella Infantis (13/39, 33.3%), Salmonella Enteritidis (9/39, 23.1%), and one isolate was detected for Salmonella Kentucky (1/39, 2.6%), with sequence types (STs) as followed: ST548, ST32, ST11, and ST198, respectively. Phenotypic resistance to tetracycline (91.2%), ampicillin (82.4%), sulfisoxazole (64.7%), and nalidixic acid (61.6%) was the most observed. Resistome analysis revealed the presence of resistance genes to aminoglycosides, β-lactamase, sulfonamides, trimethoprim, phenicol, lincosamide, macrolides, and tetracyclines. Plasmidome showed the presence of eight incompatibility groups, including IncA/C2, IncFIB(K)_1_Kpn3, Col440I_1, IncR, IncX1, IncI1_1_Alpha, IncFIB(S)/IncFII(S), IncHI2/IncHI2A, IncX2 and ColpVC plasmids across the 39 genomes. Three resistance genes, sul2, tetA and bla_CMY-2, were predicted to be located on IncA/C2 plasmid in S. Minnesota isolates, whereas all S. Infantis isolates were positive to IncFIB(K)_1_Kpn3 plasmid that carries bla _CTX-M-65 gene. Eleven Salmonella pathogenicity islands and up to 131 stress and/or virulence genes were identified in the evaluated genomes. Phylogenetic analysis showed four phylogroups that were consistent with the identified ST profiles with a high level of inter-diversity between isolates. This is the first genomic characterization of Salmonella isolates from retail chicken meat in Saudi Arabia using WGS technology. The availability of Salmonella genomes from multiple geographic locations, including Saudi Arabia, would be highly beneficial in future source-tracking, especially during epidemiological surveillance and outbreak investigations.

SUBMITTER: Alzahrani KO

PROVIDER: S-EPMC10100587 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Antimicrobial resistance and genomic characterization of Salmonella enterica isolates from chicken meat.

Alzahrani Khaloud O KO Al-Reshoodi Fahad M FM Alshdokhi Elaf A EA Alhamed Ashwaq S AS Al Hadlaq Meshari A MA Mujallad Mohammed I MI Mukhtar Lenah E LE Alsufyani Amani T AT Alajlan Abdullah A AA Al Rashidy Malfi S MS Al Dawsari Mashan J MJ Al-Akeel Saleh I SI Al-Harthi Meshari H MH Al Manee Abdulaziz M AM Alghoribi Majed F MF Alajel Suliman M SM

Frontiers in microbiology 20230330

This study investigated genotypic and phenotypic antimicrobial resistance profiles, phylogenic relatedness, plasmid and virulence composition of 39 Salmonella enterica strains isolated from chicken meat samples using whole genome sequencing (WGS) technology. Four distinct serotypes were identified; Salmonella Minnesota (16/39, 41%), Salmonella Infantis (13/39, 33.3%), Salmonella Enteritidis (9/39, 23.1%), and one isolate was detected for Salmonella Kentucky (1/ ...[more]

PMID: 37065154

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Project description:Salmonella enterica remains one of the leading causes of foodborne bacterial disease. Retail meat is a major source of human salmonellosis. However, comparative genomic analyses of S. enterica isolates from retail meat from different sources in China are lacking. A total of 341 S. enterica strains were isolated from retail meat in sixteen districts of Beijing, China, at three different time points (January 1st, May 1st, and October 1st) in 2017. Comparative genomics was performed to investigate the genetic diversity, virulence and antimicrobial resistance gene (ARG) profiles of these isolates. The most common serotype was S. Enteritidis (203/341, 59.5%), which dominated among isolates from three different time points during the year. Laboratory retesting confirmed the accuracy of the serotyping results predicted by the Salmonella In Silico Typing Resource (SISTR) (96.5%). The pangenome of the 341 S. enterica isolates contained 13,931 genes, and the core genome contained 3,635 genes. Higher Salmonella phage 118970 sal3 (219/341, 64.2%) and Gifsy-2 (206/341, 60.4%) prevalence contributed to the diversity of the accessory genes, especially those with unknown functions. IncFII(S), IncX1, and IncFIB(S) plasmid replicons were more common in these isolates and were major sources of horizontally acquired foreign genes. The virulence gene profile showed fewer virulence genes associated with type III secretion systems in certain isolates from chicken. A total of 88 different ARGs were found in the 341 isolates. Three beta-lactamases, namely, bla CTX - M - 55 (n = 15), bla CTX - M - 14 (n = 11), and bla CTX - M - 65 (n = 11), were more prevalent in retail meats. The emergence of qnrE1 and bla CTX - M - 123 indicated a potential increase in the prevalence of retail meats. After the prohibition of colistin in China, three and four isolates were positive for the colistin resistance genes mcr-1.1 and mcr-9, respectively. Thus, we explored the evolution and genomic features of S. enterica isolates from retail meats in Beijing, China. The diverse ARGs of these isolates compromise food security and are a clinical threat.

Project description:Salmonella genomic island 1 (SGI1) contains a multidrug resistance region conferring the ampicillin-chloramphenicol-streptomycin-sulfamethoxazole-tetracycline resistance phenotype encoded by bla(PSE-1), floR, aadA2, sul1, and tet(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-carrying Salmonella enterica serovars selected from a European strain collection. A total of 38 strains belonging to S. enterica serovar Agona, S. enterica serovar Albany, S. enterica serovar Derby, S. enterica serovar Kentucky, S. enterica serovar Newport, S. enterica serovar Paratyphi B dT+, and S. enterica serovar 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 by aadB. 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.

Project description:In the USA, Salmonella enterica subspecies enterica serovar Senftenberg is among the top five serovars isolated from food and the top 11 serovars isolated from clinically ill animals. Human infections are associated with exposure to farm environments or contaminated food. The objective of this study was to characterize S. Senftenberg isolates from production animals by analyzing phenotypic antimicrobial resistance profiles, genomic features and phylogeny. Salmonella Senftenberg isolates (n = 94) from 20 US states were selected from NVSL submissions (2014-2017), tested against 14 antimicrobial drugs, and resistance phenotypes determined. Resistance genotypes were determined using whole genome sequencing analysis with AMRFinder and the NCBI and ResFinder databases with ABRicate. Plasmids were detected using PlasmidFinder. Integrons were detected using IntFinder and manual alignment with reference genes. Multilocus-sequence-typing (MLST) was determined using ABRicate with PubMLST database, and phylogeny was determined using vSNP. Among 94 isolates, 60.6% were resistant to at least one antimicrobial and 39.4% showed multidrug resistance. The most prevalent resistance findings were for streptomycin (44.7%), tetracycline (42.6%), ampicillin (36.2%) and sulfisoxazole (32.9%). The most commonly found antimicrobial resistance genes were aac(6')-Iaa (100%), aph(3″)-Ib and aph(6)-Id (29.8%) for aminoglycosides, followed by bla TEM-1 (26.6%) for penicillins, sul1 (25.5%) and sul2 (23.4%) for sulfonamides and tetA (23.4%) for tetracyclines. Quinolone-resistant isolates presented mutations in gyrA and/or parC genes. Class 1 integrons were found in 37 isolates. Thirty-six plasmid types were identified among 77.7% of the isolates. Phylogenetic analysis identified two distinct lineages of S. Senftenberg that correlated with the MLST results. Isolates were classified into two distinct sequence types (ST): ST14 (97.9%) and ST 185 (2.1%). The diversity of this serotype suggests multiple introductions into animal populations from outside sources. This study provided antimicrobial susceptibility and genomic characteristics of S. Senftenberg clinical isolates from production animals in the USA during 2014 to 2017. This study will serve as a base for future studies focused on the phenotypic and molecular antimicrobial characterization of S. Senftenberg isolates in animals. Monitoring of antimicrobial resistance to detect emergence of multidrug-resistant strains is critical.

Project description:Salmonella enterica is a foodborne zoonotic pathogen of significant public health concern. We have characterized the virulence and antimicrobial resistance gene content of 95 Salmonella isolates from 11 serovars by DNA microarray recovered from UK livestock or imported meat. Genes encoding resistance to sulphonamides (sul1, sul2), tetracycline [tet(A), tet(B)], streptomycin (strA, strB), aminoglycoside (aadA1, aadA2), beta-lactam (bla TEM), and trimethoprim (dfrA17) were common. Virulence gene content differed between serovars; S. Typhimurium formed two subclades based on virulence plasmid presence. Thirteen isolates were selected by their virulence profile for pathotyping using the Galleria mellonella pathogenesis model. Infection with a chicken invasive S. Enteritidis or S. Gallinarum isolate, a multidrug resistant S. Kentucky, or a S. Typhimurium DT104 isolate resulted in high mortality of the larvae; notably presence of the virulence plasmid in S. Typhimurium was not associated with increased larvae mortality. Histopathological examination showed that infection caused severe damage to the Galleria gut structure. Enumeration of intracellular bacteria in the larvae 24 h post-infection showed increases of up to 7 log above the initial inoculum and transmission electron microscopy (TEM) showed bacterial replication in the haemolymph. TEM also revealed the presence of vacuoles containing bacteria in the haemocytes, similar to Salmonella containing vacuoles observed in mammalian macrophages; although there was no evidence from our work of bacterial replication within vacuoles. This work shows that microarrays can be used for rapid virulence genotyping of S. enterica and that the Galleria animal model replicates some aspects of Salmonella infection in mammals. These procedures can be used to help inform on the pathogenicity of isolates that may be antibiotic resistant and have scope to aid the assessment of their potential public and animal health risk.

Project description:The purpose of this study was to characterize extensively drug-resistant Salmonella enterica serovar Kentucky sequence type 198 (ST198) isolates from chicken meat products. Ten S. Kentucky strains obtained from chicken meat products in Xuancheng, China, carried 12 to 17 resistance genes, such as blaCTX-M-55, rmtB, tet(A), floR, and fosA3, combined with mutations within gyrA (S83F and D87N) and parC (S80I), resulting in resistance to numerous antimicrobial agents, including the clinically important antibiotics cephalosporin, ciprofloxacin, tigecycline, and fosfomycin. These S. Kentucky isolates shared a close phylogenetic relationship (21 to 36 single-nucleotide polymorphisms [SNPs]) and showed close genetic relatedness to two human clinical isolates from China. Three S. Kentucky strains were subjected to whole-genome sequencing using Pacific Biosciences (PacBio) single-molecule real-time (SMRT) technology. All antimicrobial resistance genes were located on their chromosomes and clustered in one multiresistance region (MRR) and Salmonella genomic island (SGI) SGI1-K. The MRRs in three S. Kentucky strains were bounded by IS26 at both ends and were inserted downstream of the bcfABCDEFG cluster with 8-bp direct repeats. The MRRs were related to those of IncHI2 plasmids but differed by insertions, deletions, and rearrangements of multiple segments involving resistance genes and plasmid backbones. This finding suggests that the MRR fragment possibly originates from IncHI2 plasmids. Four SGI1-K variants with slight differences were identified in 10 S. Kentucky strains. Mobile elements, particularly IS26, play an essential role in forming distinct MRRs and SGI1-K structures. In conclusion, the emergence of extensively drug-resistant S. Kentucky ST198 strains containing numerous chromosomally located resistance genes is alarming and needs continued surveillance. IMPORTANCE Salmonella spp. are important foodborne pathogens, and multidrug-resistant (MDR) Salmonella strains have become a serious threat to clinical therapy. MDR S. Kentucky ST198 strains have been increasingly reported from various sources and have become a global risk. In this study, we described extensively drug-resistant S. Kentucky ST198 strains from chicken meat products from a city in China. Numerous resistance genes are clustered in the chromosomes of S. Kentucky ST198 strains, possibly acquired with the help of mobile elements. This would facilitate the spread of numerous resistance genes as intrinsic chromosomal genes within this global epidemic clone, with the potential to capture more resistance genes. The emergence and dissemination of extensively drug-resistant S. Kentucky ST198 pose a severe clinical and public health threat; therefore, continuous surveillance is warranted.

Project description:Antimicrobial-resistant Salmonella enterica poses a significant public health concern worldwide. However, the dissemination of Salmonella enterica among food animals in eastern China has not been fully addressed. Here, we demonstrated the antimicrobial resistance (AMR) patterns and the whole-genome characterization of 105 S. enterica isolates from 1,480 fecal samples and anal swabs collected from 22 different farms (chickens, ducks, and pigs) and two live animal markets located in Zhejiang and Fujian Provinces in eastern China in 2019. The prevalence of isolates in duck farms (19.17%, 23/120) was statistically significantly higher (P < 0.001) than that in chicken farms (6.61%, 37/523) and pig farms (3.50%, 7/200). Among these isolates, 75.26% (79/105) were multidrug resistant, with the highest rates of resistance to tetracycline (76.20%) and ampicillin (67.62%) and the lowest resistance rate to meropenem (0.00%). The serotypes were consistent with sequence types and were closely related to the sampling animal species and sites. S. enterica serotype Kentucky (20.95%, 22/105) was the most frequent serotype and harbored more AMR patterns and genes than others. Furthermore, IncFII(S) and IncHI2 were the most prevalent replicons. A total of 44 acquired AMR genes were found. Among those genes, aac(6')-Iaa, blaTEM-1B, floR, dfrA14, fosA7, mph(A), qnrS1, sul1, tet(A), and ARR-3 were the dominant AMR genes mediating the AMR toward aminoglycosides, β-lactams, phenicol, trimethoprim, fosfomycin, macrolide, quinolone, sulfonamides, tetracycline, and rifampin, respectively. The consistency of acquired AMR genes with AMR phenotypes for ampicillin, ceftiofur, ceftazidime, meropenem, sulfamethoxazole-trimethoprim, and tetracycline was >90%. Together, our study highlights the application of whole-genome sequencing to assess veterinary public health threats. IMPORTANCE Public health is a significant concern in China, and the foodborne pathogen Salmonella, which is spread via the animal-borne food chain, plays an important role in the overall disease burden in China annually. The development of advanced sequencing technologies has introduced a new way of understanding emerging pathogens. However, the routine surveillance application of this method in China remains in its infancy. Here, we applied a pool of all isolates from the prevalence data in Zhejiang and Fujian for whole-genome sequencing and combined these data with the cutting-edge bioinformatic analysis pipeline for one-step determination of the complete genetic makeup for all 105 genomes. The illustrated method could provide a cost-effective approach, without labor-intensive laboratory characterization, for predicting serotypes, genotypes, plasmid types, antimicrobial resistance genes, and virulence genes, and thus would provide essential knowledge for emerging pathogens. Our findings and perspectives are essential for delivering updated knowledge on foodborne pathogens in an understudied region in China.

Project description:Salmonella enterica subspecies enterica serotype Dublin is a host-adapted serotype in cattle, associated with enteritis and systemic disease. The primary clinical manifestation of Salmonella Dublin infection in cattle, especially calves, is respiratory disease. While rare in humans, it can cause severe illness, including bacteremia, with hospitalization and death. In the United States, S. Dublin has become one of the most multidrug-resistant serotypes. The objective of this study was to characterize S. Dublin isolates from sick cattle by analyzing phenotypic and genotypic antimicrobial resistance (AMR) profiles, the presence of plasmids, and phylogenetic relationships. S. Dublin isolates (n = 140) were selected from submissions to the NVSL for Salmonella serotyping (2014-2017) from 21 states. Isolates were tested for susceptibility against 14 class-representative antimicrobial drugs. Resistance profiles were determined using the ABRicate with Resfinder and NCBI databases, AMRFinder and PointFinder. Plasmids were detected using ABRicate with PlasmidFinder. Phylogeny was determined using vSNP. We found 98% of the isolates were resistant to more than 4 antimicrobials. Only 1 isolate was pan-susceptible and had no predicted AMR genes. All S. Dublin isolates were susceptible to azithromycin and meropenem. They showed 96% resistance to sulfonamides, 97% to tetracyclines, 95% to aminoglycosides and 85% to beta-lactams. The most common AMR genes were: sulf2 and tetA (98.6%), aph(6)-Id (97.9%), aph(3'')-Ib, (97.1%), floR (94.3%), and blaCMY-2 (85.7%). All quinolone resistant isolates presented mutations in gyrA. Ten plasmid types were identified among all isolates with IncA/C2, IncX1, and IncFII(S) being the most frequent. The S. Dublin isolates show low genomic genetic diversity. This study provided antimicrobial susceptibility and genomic insight into S. Dublin clinical isolates from cattle in the U.S. Further sequence analysis integrating food and human origin S. Dublin isolates may provide valuable insight on increased virulence observed in humans.

Dataset Information

Antimicrobial resistance and genomic characterization of Salmonella enterica isolates from chicken meat.

Publications

Antimicrobial resistance and genomic characterization of <i>Salmonella enterica</i> isolates from chicken meat.

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