Prevalence, molecular epidemiology, and antimicrobial resistance of methicillin-resistant Staphylococcus aureus from swine in southern Italy

Mattia Pirolo,Rossella Di Natale,Daniela Visaggio,Monica Gherardi,Francesco Casalinuovo,Paolo Visca,Angela Gioffrè,Giovanna Spatari,Grazia Pavia,Lucia Ciambrone,Pasquale Samele

doi:10.1186/s12866-019-1422-x

Abstract

BackgroundColonization by livestock-associated MRSA (LA-MRSA) has increasingly been reported in the swine population worldwide. The aim of this study was to assess the prevalence of MRSA nasal carriage in healthy pigs, including the black (Calabrese) breed, from farms in the Calabria Region (Southern Italy). Between January and March 2018, a total of 475 healthy pigs reared in 32 farms were sampled by nasal swabbing. MRSA isolates were characterized by spa, MLST and SCCmec typing, and susceptibility testing to 17 antimicrobials.Results22 of 32 (66.8%) pig farms resulted positive for MRSA. The prevalence of MRSA was 46.1% (219 MRSA culture-positive out of 475 samples). MRSA colonization was significantly higher in intensive farms and in pigs with a recent or ongoing antimicrobial treatment. All 219 MRSA isolates were assigned to ST398. The most common spa types were t011 (37.0%), t034 (22.4%) and t899 (15.1%). A novel spa type (t18290) was detected in one isolate. An insertion of IS256 in the ST398-specific A07 fragment of the SAPIG2195 gene was detected in 10 out of 81 t011 isolates. Nearly all isolates carried the SCCmec type V element, except 11 isolates that carried the SCCmec type IVc. None of the isolates was positive for the Panton-Valentine leukocidin. All isolates were resistant to tetracycline. High resistance rates were also found for clindamycin (93.1%), trimethoprim/sulfamethoxazole (68.4%), fluoroquinolones (47.9–65.3%) and erythromycin (46.1%). None of the isolates was resistant to vancomycin and fusidic acid. Overall, a multidrug resistant phenotype was observed in 88.6% of isolates.ConclusionsWe report a high prevalence of MRSA among healthy swine in Southern Italy farms, with higher isolation frequency associated with intensive farming. The epidemiological types identified in our study reflect those reported in other European countries. Our findings underscore the importance of monitoring the evolution of LA-MRSA in pig farms in order to implement control measures and reduce the risk of spread in the animal population.

Highlights

Colonization by livestock-associated Methicillin-resistant Staphylococcus aureus (MRSA) (LA-MRSA) has increasingly been reported in the swine population worldwide
After the first isolation from pigs in France [17], ST398 was increasingly detected throughout Europe, accounting for 92.5% of the MRSA isolates from breeding or production holdings of 17 European Union (EU) Member States [18]
Given the serious threat of zoonotic MRSA transmission and the high isolation rate of livestock-associated MRSA (LA-MRSA) from intensive pig farms in Italy, the aims of the present study were: (i) to assess the prevalence of MRSA among asymptomatic swine, including the autochthonous black (Calabrese) pig breed [28, 29], from farms located in the Calabria region (Southern Italy); (ii) to investigate differences in MRSA carriage between intensive and non-intensive farming; (iii) to determine the clonal profiles of pig-associated MRSA isolates; (iv) to investigate the antimicrobial resistance patterns and the staphylococcal chromosomal cassette mec (SCCmec) type of MRSA isolates

Summary

Introduction

Colonization by livestock-associated MRSA (LA-MRSA) has increasingly been reported in the swine population worldwide. The World Health Organization has urged a ban on growth-promoting antibiotics in fatten farm animals [3], a practice already banned in European Union (EU) and United States [4] Despite these precautions, antimicrobial resistance among bacterial pathogens in the animal husbandry is progressively increasing, contributing to the spread of multi-drug resistant (MDR) microorganism in the community [5]. Methicillin-resistant Staphylococcus aureus (MRSA) has for long time been considered a prototypic nosocomial pathogen, showing highest prevalence in healthcare-associated infections (HA-MRSA) [6]. This view has changed over the last decades, since MRSA has become increasingly frequent in community acquired infections (CA-MRSA) in healthy people [7]. In line with the “One World, One Health” principles [20], an integrated multi-sectorial surveillance including both healthcare and veterinary sources, to systematically map potential reservoirs and epidemiological trajectories of MRSA, has become mandatory [19]

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