Dataset Information

Zoonotic Transfer of Clostridium difficile Harboring Antimicrobial Resistance between Farm Animals and Humans.

ABSTRACT: The emergence of Clostridium difficile as a significant human diarrheal pathogen is associated with the production of highly transmissible spores and the acquisition of antimicrobial resistance genes (ARGs) and virulence factors. Unlike the hospital-associated C. difficile RT027 lineage, the community-associated C. difficile RT078 lineage is isolated from both humans and farm animals; however, the geographical population structure and transmission networks remain unknown. Here, we applied whole-genome phylogenetic analysis of 248 C. difficile RT078 strains from 22 countries. Our results demonstrate limited geographical clustering for C. difficile RT078 and extensive coclustering of human and animal strains, thereby revealing a highly linked intercontinental transmission network between humans and animals. Comparative whole-genome analysis reveals indistinguishable accessory genomes between human and animal strains and a variety of antimicrobial resistance genes in the pangenome of C. difficile RT078. Thus, bidirectional spread of C. difficile RT078 between farm animals and humans may represent an unappreciated route disseminating antimicrobial resistance genes between humans and animals. These results highlight the importance of the "One Health" concept to monitor infectious disease emergence and the dissemination of antimicrobial resistance genes.

SUBMITTER: Knetsch CW

PROVIDER: S-EPMC5824051 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Zoonotic Transfer of Clostridium difficile Harboring Antimicrobial Resistance between Farm Animals and Humans.

Knetsch C W CW Kumar N N Forster S C SC Connor T R TR Browne H P HP Harmanus C C Sanders I M IM Harris S R SR Turner L L Morris T T Perry M M Miyajima F F Roberts P P Pirmohamed M M Songer J G JG Weese J S JS Indra A A Corver J J Rupnik M M Wren B W BW Riley T V TV Kuijper E J EJ Lawley T D TD

Journal of clinical microbiology 20180222 3

The emergence of Clostridium difficile as a significant human diarrheal pathogen is associated with the production of highly transmissible spores and the acquisition of antimicrobial resistance genes (ARGs) and virulence factors. Unlike the hospital-associated C. difficile RT027 lineage, the community-associated C. difficile RT078 lineage is isolated from both humans and farm animals; however, the geographical population structure and transmission networks remain unknown. He ...[more]

PMID: 29237792

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Project description:BACKGROUND:Clostridioides (Clostridium) difficile is an important pathogen of healthcare- associated diarrhea, however, an increase in the occurrence of C. difficile infection (CDI) outside hospital settings has been reported. The accumulation of antimicrobial resistance in C. difficile can increase the risk of CDI development and/or its spread. The limited number of antimicrobials for the treatment of CDI is matter of some concern. OBJECTIVES:In order to summarize the data on antimicrobial resistance to C. difficile derived from humans, a systematic review and meta-analysis were performed. METHODS:We searched five bibliographic databases: (MEDLINE [PubMed], Scopus, Embase, Cochrane Library and Web of Science) for studies that focused on antimicrobial susceptibility testing in C. difficile and were published between 1992 and 2019. The weighted pooled resistance (WPR) for each antimicrobial agent was calculated using a random- effects model. RESULTS:A total of 111 studies were included. The WPR for metronidazole and vancomycin was 1.0% (95% CI 0-3%) and 1% (95% CI 0-2%) for the breakpoint >?2?mg/L and 0% (95% CI 0%) for breakpoint ?32??g/ml. Rifampin and tigecycline had a WPRs of 37.0% (95% CI 18-58%) and 1% (95% CI 0-3%), respectively. The WPRs for the other antimicrobials were as follows: ciprofloxacin 95% (95% CI 85-100%), moxifloxacin 32% (95% CI 25-40%), clindamycin 59% (95% CI 53-65%), amoxicillin/clavulanate 0% (0-0%), piperacillin/tazobactam 0% (0-0%) and ceftriaxone 47% (95% CI 29-65%). Tetracycline had a WPR 20% (95% CI 14-27%) and meropenem showed 0% (95% CI 0-1%); resistance to fidaxomicin was reported in one isolate (0.08%). CONCLUSION:Resistance to metronidazole, vancomycin, fidaxomicin, meropenem and piperacillin/tazobactam is reported rarely. From the alternative CDI drug treatments, tigecycline had a lower resistance rate than rifampin. The high-risk antimicrobials for CDI development showed a high level of resistance, the highest was seen in the second generation of fluoroquinolones and clindamycin; amoxicillin/clavulanate showed almost no resistance. Tetracycline resistance was present in one fifth of human clinical C. difficile isolates.

Project description:The data on antimicrobial resistance in zoonotic and indicator bacteria in 2016, submitted by 28 EU Member States (MSs), were jointly analysed by the EFSA and ECDC. Resistance in bacterial isolates of zoonotic Salmonella and Campylobacter from humans, animals and food, and resistance in indicator Escherichia coli as well as in meticillin-resistant Staphylococcus aureus from animals and food were addressed. 'Microbiological' resistance was assessed using epidemiological cut-off (ECOFF) values; for some countries, qualitative data on isolates from humans were interpreted in a way that corresponds closely to ECOFF-defined 'microbiological' resistance. In Salmonella from humans, the occurrence of resistance to ampicillin, sulfonamides and tetracyclines was high, whereas resistance to third-generation cephalosporins was low. In Salmonella and E. coli isolates from broilers, fattening turkeys and their meat, resistance to ampicillin, (fluoro)quinolones, tetracyclines and sulfonamides was frequently high, whereas resistance to third-generation cephalosporins was rare. The occurrence of ESBL-/AmpC producers was low in Salmonella and E. coli from poultry and in Salmonella from humans. The prevalence of ESBL-/AmpC-producing E. coli, assessed in poultry and its meat for the first time, showed marked variations among MSs. Fourteen presumptive carbapenemase-producing E. coli were detected from broilers and its meat in two MSs. Resistance to colistin was observed at low levels in Salmonella and E. coli from poultry and meat thereof and in Salmonella from humans. In Campylobacter from humans, broilers and broiler meat, resistance to ciprofloxacin and tetracyclines was high to extremely high, whereas resistance to erythromycin was low to moderate. Combined resistance to critically important antimicrobials in isolates from both humans and animals was generally uncommon, but very high to extremely high multidrug resistance levels were observed in certain Salmonella serovars. Specific serovars of Salmonella (notably Kentucky) from both humans and animals exhibited high-level resistance to ciprofloxacin, in addition to findings of ESBL.

Project description:The data on antimicrobial resistance in zoonotic and indicator bacteria in 2017, submitted by 28 EU Member States (MSs), were jointly analysed by EFSA and ECDC. Resistance in zoonotic Salmonella and Campylobacter from humans, animals and food, and resistance in indicator Escherichia coli as well as meticillin-resistant Staphylococcus aureus in animals and food were addressed, and temporal trends assessed. 'Microbiological' resistance was assessed using epidemiological cut-off (ECOFF) values; for some countries, qualitative data on human isolates were interpreted in a way which corresponds closely to the ECOFF-defined 'microbiological' resistance. In Salmonella from humans, as well as in Salmonella and E. coli isolates from fattening pigs and calves of less than 1 year of age, high proportions of isolates were resistant to ampicillin, sulfonamides and tetracyclines, whereas resistance to third-generation cephalosporins was uncommon. Varying occurrence/prevalence rates of presumptive extended-spectrum beta-lactamase (ESBL)/AmpC producers in Salmonella and E. coli monitored in meat (pork and beef), fattening pigs and calves, and Salmonella monitored in humans, were observed between countries. Carbapenemase-producing E. coli were detected in one single sample from fattening pigs in one MS. Resistance to colistin was observed at low levels in Salmonella and E. coli from fattening pigs and calves and meat thereof and in Salmonella from humans. In Campylobacter from humans, high to extremely high proportions of isolates were resistant to ciprofloxacin and tetracyclines, particularly in Campylobacter coli. In five countries, high to very high proportions of C. coli from humans were resistant also to erythromycin, leaving few options for treatment of severe Campylobacter infections. High resistance to ciprofloxacin and tetracyclines was observed in C. coli isolates from fattening pigs, whereas much lower levels were recorded for erythromycin. Combined resistance to critically important antimicrobials in both human and animal isolates was generally uncommon but very high to extremely high multidrug resistance levels were observed in S. Typhimurium and its monophasic variant in both humans and animals. S. Kentucky from humans exhibited high-level resistance to ciprofloxacin, in addition to a high prevalence of ESBL.

Project description:The prevalence and propagation of antimicrobial resistance (AMR) are serious global public health concerns. The large and the ever-increasing use of antibiotics in livestock is also considered a great concern. The extent of the similarity of acquired antibiotic resistance genes (ARGs) between humans and food animals and the driving factors underlying AMR transfer between them are not clear, although a link between ARGs in both hosts was proposed. To address this question, with swine and chicken as examples of food animals, we analyzed over 1,000 gut metagenomes of humans and food animals from over the world. A relatively high abundance and diversity of ARGs were observed in swine compared with those in humans as a whole. Commensal bacteria, particularly species from Clostridiales, contribute the most ARGs associated with mobile genetic elements (MGEs) and were found in both humans and food animals. Further studies demonstrate that overrepresented MGEs, namely, Tn4451/Tn4453 and TnAs3, are attributed mainly to the sharing between humans and food animals. A member of large resolvase family site-specific recombinases, TnpX, is found in Tn4451/Tn4453 which facilitates the insertions of the transient circular molecule. Although the variance in the transferability of ARGs in humans is higher than that in swine, a higher average transferability was observed in swine than that in humans. In conclusion, the potential antibiotic resistance hot spots with higher transferability in food animals observed in the present study emphasize the importance of surveillance for emerging resistance threats before they spread. IMPORTANCE Antimicrobial resistance (AMR) has proven to be a global public health concern. To conquer this increasingly worrying trend, an overarching, One Health approach has been used that brings together different sectors, but the fundamental knowledge of the relationship between humans, food animals, and their environments is not mature yet or is lacking in some aspect. With swine and chicken as examples of food animals, a large global data set of over 1,000 human and food animal gut metagenomes was analyzed with a focus on acquired antibiotic resistance genes (ARGs) associated with mobile genetic elements (MGEs) to answer this question. Outputs from this work open a new avenue to further our understanding of ARG transferability in food animals. It is a necessary milestone to better equip governmental agencies to monitor and pre-empt antibiotic resistance hot spots. This work will assist and give guidance on how to decipher other links within any One Health initiatives with expected positive feedback to human health.

Project description:Data on antimicrobial resistance (AMR) in zoonotic and indicator bacteria from humans, animals and food are collected annually by the EU Member States (MSs), jointly analysed by EFSA and ECDC and reported in a yearly EU Summary Report. The annual monitoring of AMR in animals and food within the EU is targeted at selected animal species corresponding to the reporting year. The 2017 monitoring specifically focussed on pigs and calves under 1 year of age, as well as their derived carcases/meat, while the monitoring performed in 2018 specifically focussed on poultry and their derived carcases/meat. Monitoring and reporting of AMR in 2017/2018 included data regarding Salmonella, Campylobacter and indicator Escherichia coli isolates, as well as data obtained from the specific monitoring of ESBL-/AmpC-/carbapenemase-producing E. coli isolates. Additionally, some MSs reported voluntary data on the occurrence of meticillin-resistant Staphylococcus aureus in animals and food, with some countries also providing data on antimicrobial susceptibility. This report provides, for the first time, an overview of the main findings of the 2017/2018 harmonised AMR monitoring in the main food-producing animal populations monitored, in related carcase/meat samples and in humans. Where available, data monitoring obtained from pigs, calves/cattle, broilers, laying hens and turkeys, as well as from carcase/meat samples and humans were combined and compared at the EU level, with particular emphasis on multiple drug resistance, complete susceptibility and combined resistance patterns to critically important antimicrobials, as well as Salmonella and E. coli isolates exhibiting presumptive ESBL-/AmpC-/carbapenemase-producing phenotypes. The outcome indicators for AMR in food-producing animals, such as complete susceptibility to the harmonised panel of antimicrobials in E. coli and the prevalence of ESBL-/AmpC-producing E. coli have been also specifically analysed over the period 2014-2018.

Dataset Information

Zoonotic Transfer of Clostridium difficile Harboring Antimicrobial Resistance between Farm Animals and Humans.

Publications

Zoonotic Transfer of Clostridium difficile Harboring Antimicrobial Resistance between Farm Animals and Humans.

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