We assessed the quantitative contribution of pig farming to antimicrobial resistance in the commensal flora of pig farmers by comparing 113 healthy pig farmers from the major French porcine production areas to 113 nonfarmers, each matched for sex, age, and county of residence. All reported that they had not taken antiimicrobial agents within the previous month. Throat, nasal, and fecal swabs were screened for resistant microorganisms on agar containing selected antimicrobial agents. Nasopharyngeal carriage of Staphylococcus aureus was significantly more frequent in pig farmers, as was macrolide resistance of S. aureus from carriers. Nongroupable streptococci from the throat were more resistant to the penicillins in pig farmers. The intestinal isolation of enterococci resistant to erythromycin or vancomycin was not significantly higher in pig farmers in contrast to that of enterobacteria resistant to nalidixic acid, chloramphenicol, tetracycline, and streptomycin. Prevalence of resistance in predominant fecal enterobacteria was also significantly higher in pig farmers for cotrimoxazole, tetracycline, streptomycin, and nalidixic acid. We determined a significant association between pig farming and isolation of resistant commensal bacteria.

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BackgroundThere has been a strong implication of both the French swine industry and the national authorities on reducing the use of antimicrobials in swine production since 2010. The annual monitoring of antimicrobial sales by the French Veterinary Medicines Agency (Anses-ANMV) provides estimates but not detailed figures on actual on-farm usage of antimicrobials in swine production.ResultsIn order to provide detailed information on the 2010 and 2013 antimicrobial use in the French swine industry, the methodology of cross-sectional retrospective study on a representative sample of at least 150 farms has been elected. The analysis of the collected data shows a strong and significant decrease in antimicrobial exposure of pigs between 2010 and 2013. Over three years, the average number of days of treatment significantly decreased by 29% in suckling piglets and by 19% in weaned piglets. In fattening pigs, the drop (− 29%) was not statistically significant. Only usage in sows did increase over that period (+ 17%, non-significant), which might be associated with the transition to group-housing of pregnant sows that took place at the time. Also, over that period, the use of third- and fourth generation cephalosporins in suckling piglets decreased by 89%, and by 82% in sows, which confirms that the voluntary moratorium on these classes of antimicrobials decided at the end of 2010 has been effectively implemented.ConclusionsThe methodology of random sampling of farms appears as a precise and robust tool to monitor antimicrobial use within a production animal species, able to fulfil industry and national authorities’ objectives and requirements to assess the outcome of concerted efforts on antimicrobial use reduction. It demonstrates that the use of antimicrobials decreased in the French swine industry between 2010 and 2013, including the classes considered as critical for human medicine.

By 2010, systems set up to monitor the antimicrobial resistance of pathogenic bacteria and antimicrobial usage identified a sustained increase regarding third‐ and fourth‐generation cephalosporin resistance in French pig production. This sector mobilised and collectively committed to responsible action in the following months. This led to a multi‐professional voluntary stewardship programme that was started in 2011. A consensus of veterinary opinion led to the definition of restrictive rules on the prescription of the third‐ and fourth‐generation cephalosporins targeted by the antimicrobial stewardship programme (ASP). All pig sector professionals, including farmers, were informed. Existing monitoring systems for usage and resistance were supplemented by data from the records of veterinarians' cephalosporin deliveries and from individual pig farm surveys investigating antimicrobial usage. The second step, from 2014, entailed regulatory measures that consolidated the programme by setting quantitative reduction objectives and specifying the terms and conditions for prescribing and dispensing a list of critical antimicrobial molecules including cephalosporins. All the data sources confirmed a significant fall of more than 90% in cephalosporin usage in the French pig production sector between 2010 and 2016. Monitoring systems recorded that the resistance of commensal and pathogenic Escherichia coli isolates also tended to decrease over the same period. The stewardship programme proved highly effective in reducing usage and containing resistance, illustrating the efficiency of a well‐defined multi‐professional strategy.

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