Characterization of Salmonella Resistome and Plasmidome in Pork Production System in Jiangsu, China
Qingxin LiuWenjing ChenMohammed ElbediwiHang PanLiqun WangChuang ZhouBin ZhaoXinguo XuDingguo LiXin YanXiao HanHanyuan LiYan LiMin Yue
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Abstract:
The prevalence of antimicrobial resistance in zoonotic Salmonella is a significant ongoing concern over the world. Several reports have investigated the prevalence of Salmonella infections in the farm animals in China; however, there is only limited knowledge about the Salmonella cross-contamination in the slaughterhouses. Moreover, the application of genomic approaches for understanding the cross-contamination in the food-animal slaughterhouses is still in its infancy in China. In the present study, we have isolated 105 Salmonella strains from pig carcasses and environment samples collected from four independent slaughterhouses in Jiangsu, China. All the Salmonella isolates were subjected to whole genome sequencing, bioinformatics analysis for serovar predictions, multi-locus sequence types, antimicrobial resistance genes, and plasmid types by using the in-house Galaxy platform. The antimicrobial resistance of Salmonella isolates was determined using a minimal inhibitory concentration assay with 14 antimicrobials. We found that the predominant serovar and serogroup was S. Derby and O:4(B), with a prevalence of 41.9 and 55%, respectively. All the isolates were multidrug-resistant and the highest resistance was observed against antimicrobials tetracycline (95.4%) and trimethoprim and sulfamethoxazole (90.9%). Additionally, the colistin-resistant determinant mcr-1 gene was detected in five (4.8%) strains. Our study demonstrated the prevalence of antimicrobial resistance in Salmonella strains isolated from pig slaughterhouses in China and suggested that the genomic platform can serve as routine surveillance along with the food-chain investigation.Keywords:
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Colistin
Sulfamethoxazole
Trimethoprim-sulfamethoxazole alone and combined with colistin was tested in vitro against six carbapenem-resistant Acinetobacter baumannii (CRAB) clinical strains. After 24 h, at achievable serum concentrations, trimethoprim-sulfamethoxazole effectively killed all strains, while colistin killed only one strain. Trimethoprim-sulfamethoxazole plus colistin rapidly killed all strains after 6 h and for up to 24 h. Trimethoprim-sulfamethoxazole, one of the few remaining antimicrobials that still has a degree of activity, particularly combined with colistin, might represent an effective therapy for severe CRAB infections.
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Abstract The concept of the antibiotic resistome was introduced just over a decade ago, and since then, active resistome studies have been conducted. In the present study, we describe the previously established concept of the resistome, which encompasses all types of antibiotic resistance genes (ARGs), and the important findings from each One-Health sector considering this concept, thereby emphasizing the significance of the One-Health approach in understanding ARG transmission. Cutting-edge research methodologies are essential for deciphering the complex resistome structure in the microbiomes of humans, animals, and the environment. Based on the recent achievements of resistome studies in multiple One-Health sectors, future directions for resistome research have been suggested to improve the understanding and control of ARG transmission: (1) ranking the critical ARGs and their hosts; (2) understanding ARG transmission at the interfaces of One-Health sectors; (3) identifying selective pressures affecting the emergence, transmission, and evolution of ARGs; and (4) elucidating the mechanisms that allow an organism to overcome taxonomic barriers in ARG transmission.
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By studying the entire human faecal resistome and associated microbiome, the diversity and abundance of faecal antimicrobial resistance genes (ARGs) can be comprehensively characterized. Prior culture-based studies have shown associations between occupational exposure to livestock and carriage of specific antimicrobial resistant bacteria. Using shotgun metagenomics, the present study investigated 194 faecal resistomes and bacteriomes from humans occupationally exposed to ARGs in livestock (i.e. pig and poultry farmers, employees and family members and pig slaughterhouse workers) and a control population (Lifelines cohort) in the Netherlands. In addition, we sought to identify determinants for the human resistome and bacteriome composition by applying a combination of multivariate (NMDS, PERMANOVA, SIMPER and DESeq2 analysis) and multivariable regression analysis techniques. Pig slaughterhouse workers and pig farmers carried higher total ARG abundances in their stools compared to broiler farmers and control subjects. Tetracycline, β-lactam and macrolide resistance gene clusters dominated the resistome of all studied groups. No significant resistome alpha diversity differences were found among the four populations. However, the resistome beta diversity showed a separation of the mean resistome composition of pig and pork exposed workers from broiler farmers and controls, independent of their antimicrobial use. We demonstrated differences in resistome composition between slaughter line positions, pig versus poultry exposed workers, as well as differences between farmers and employees versus family members. In addition, we found a significant correlation between the bacteriome and resistome, and significant differences in the bacteriome composition between and within the studied subpopulations. Finally, an in-depth analysis of pig and poultry farms – of which also farm livestock resistomes were analysed – showed positive associations between the number of on-farm working hours and human faecal AMR loads. We found that the total normalized faecal ARG carriage was larger in persons working in the Dutch pork production chain compared to poultry farmers and controls. Additionally, we showed significant differences in resistome and bacteriome composition of pig and pork exposed workers compared to a control group, as well as within-population (farms, slaughterhouse) compositional differences. The number of on-farm working hours and the farm type (pig or broiler) that persons live or work on are determinants for the human faecal resistome. Overall, our results may suggest direct or indirect livestock contact as a determinant for human ARG carriage. Future studies should further focus on the connection between the human and livestock resistome (i.e. transmission routes) to substantiate the evidence for livestock-associated resistome acquisition.
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The intestinal microbiome forms a major reservoir for antibiotic resistance genes (ARGs). Little is known about the neonatal intestinal resistome.The objective of this study was to investigate the intestinal resistome and factors that influence the abundance of ARGs in a large cohort of neonates.Shotgun metagenomics was used to analyse the resistome in stool samples collected at 1 week of age from 390 healthy, term-born neonates who did not receive antibiotics.Overall, 913 ARGs belonging to 27 classes were identified. The most abundant ARGs were those conferring resistance to tetracyclines, quaternary ammonium compounds, and macrolide-lincosamide-streptogramin-B. Phylogenetic composition was strongly associated with the resistome composition. Other factors that were associated with the abundance of ARGs were delivery mode, gestational age, birth weight, feeding method, and antibiotics in the last trimester of pregnancy. Sex, ethnicity, probiotic use during pregnancy, and intrapartum antibiotics had little effect on the abundance of ARGs.Even in the absence of direct antibiotic exposure, the neonatal intestine harbours a high abundance and a variety of ARGs.
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Purpose of review Fecal microbiome transplants (FMT) show promise in treating various diseases, such as Clostridioides difficile infections. FMT have also demonstrated the capacity to modulate the collection of antibiotic resistance genes (ARGs), termed the resistome, within the gut. The purpose of this review was to critically evaluate the literature regarding the interaction between FMT and the gut resistome and determine whether FMT could be used specifically to reduce ARG carriage in the gut. Recent findings Several studies have demonstrated a decrease in ARG carriage post-FMT administration in various disease states, including recurrent C. difficile infection and after antibiotic usage. However, other studies have reported an expansion of the resistome following FMT. Most studies contained small patient cohorts regardless of the outcome and showed heterogeneity in responses. Summary Research on resistome modulation by FMT is preliminary, and human studies currently lack consensus regarding benefits and risks. From a safety perspective, screening donor samples for ARGs in addition to antibiotic-resistant organisms may be advisable. Additional studies on the mechanisms underlying heterogeneity between studies and individuals are required before FMT is considered an efficient approach for resistome amelioration.
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Abstract Antimicrobial resistance is a global public health concern, and livestock play a significant role in selecting for resistance and maintaining such reservoirs. Here we study the succession of dairy cattle resistome during early life using metagenomic sequencing, as well as the relationship between resistome, gut microbiota, and diet. In our dataset, the gut of dairy calves serves as a reservoir of 329 antimicrobial resistance genes (ARGs) presumably conferring resistance to 17 classes of antibiotics, and the abundance of ARGs declines gradually during nursing. ARGs appear to co-occur with antibacterial biocide or metal resistance genes. Colostrum is a potential source of ARGs observed in calves at day 2. The dynamic changes in the resistome are likely a result of gut microbiota assembly, which is closely associated with diet transition in dairy calves. Modifications in the resistome may be possible via early-life dietary interventions to reduce overall antimicrobial resistance.
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The emergence and spread of antibiotic resistance have become emerging threats to human health. The human gut is a large reservoir for antibiotic resistance genes. The gut resistome may be influenced by many factors, but the consumption of antibiotics at both individual and country level should be one of the most significant factors. Previous studies have suggested that the gut resistome of different populations may vary, but lack quantitative characterization supported with relatively large datasets. In this study, we filled the gap by analyzing a large gut resistome dataset of 1,267 human gut samples of America, China, Denmark, and Spain. We built a stacking machine-learning model to determine whether the gut resistome can act as the sole feature to identify the nationality of an individual reliably. It turned out that the machine learning method could successfully identify American, Chinese, Danish, and Spanish populations with F1 score of 0.964, 0.987, 0.971, and 0.986, respectively. Our finding does highlight the significant differences in the composition of the gut resistome among different nationalities. Our study should be valuable for policy-makers to look into the influences of country-specific factors of the human gut resistome.
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Abstract Horizontal gene transfer is a major contributor to the evolution of bacterial genomes and can facilitate the dissemination of antibiotic resistance genes between environmental reservoirs and potential pathogens. Wastewater treatment plants (WWTPs) are believed to play a central role in the dissemination of antibiotic resistance genes. However, the contribution of the dominant members of the WWTP resistome to resistance in human pathogens remains poorly understood. Here we use a combination of metagenomic functional selections and comprehensive metagenomic sequencing to uncover the dominant genes of the WWTP resistome. We find that this core resistome is unique to the WWTP environment, with <10% of the resistance genes found outside the WWTP environment. Our data highlight that, despite an abundance of functional resistance genes within WWTPs, only few genes are found in other environments, suggesting that the overall dissemination of the WWTP resistome is comparable to that of the soil resistome.
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Carbapenem-resistant Klebsiella pneumoniae (CRKP) has emerged as a formidable health challenge in recent years owing to the shortage of effective antibiotics. Colistin is the last and sometimes the only therapeutic option for CRKP infections. Unfortunately, resistance to colistin monotherapy is likely to develop. CRKP in China reportedly exhibit low rates of resistance to trimethoprim–sulfamethoxazole. The aim of this study was to evaluate the in vitro efficacy of trimethoprim–sulfamethoxazole in combination with colistin against four CRKP clinical isolates. The trimethoprim–sulfamethoxazole/colistin combination rapidly killed all four of the tested isolates after 2 h up to 24 h. Trimethoprim–sulfamethoxazole is one of the few remaining antimicrobials with some activity against CRKP. In particular, combined with colistin, trimethoprim–sulfamethoxazole might be promising for the treatment of CRKP infections.
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