A longitudinal study of Staphylococcus aureus colonization in pigs in Ireland
Introduction
Staphylococcus aureus is a common commensal organism of the skin and mucosal membranes of both humans and animals (Werckenthin et al., 2001). Antimicrobial resistance in S. aureus, in particular methicillin-resistance, is a concern in both human and veterinary medicine. Livestock-associated methicillin-resistant S. aureus (LA-MRSA) ST398 was first identified in Europe in the early 2000s and was found chiefly in pigs and pig handlers (Voss et al., 2005, Meemken et al., 2010). This event refocused attention on staphylococci of animal origin as a potential public health problem, in particular staphylococci of intensively farmed animals such as pigs, which are frequently exposed to high levels of antimicrobials.
S. aureus, including MRSA, is a commensal organism in pigs and seldom results in clinical signs in this species although there are some reports of disease in pigs caused by methicillin-susceptible S. aureus (MSSA) or MRSA (Armand-Lefevre et al., 2005, Park et al., 2013, Schwarz et al., 2008, van Duijkeren et al., 2007). The transmission dynamics of S. aureus in individual pigs are of interest when examining possible control measures for MRSA and other multidrug-resistant S. aureus that may emerge in the future. This is especially true in light of recent findings in which colonization with MSSA was found to be protective against MRSA colonization in pig farmers (van Cleef et al., 2014). A small number of studies have investigated the host-organism relationship with S. aureus in pigs, focusing on LA-MRSA; however there are no previous studies on other strains of S. aureus. A longitudinal study by Weese et al. (2010) indicated that there was a significant association between sow and piglet colonization. In addition, their findings suggested that colonization was age related (Weese et al., 2010). Studies by Broens et al. (2011) and Verhegghe et al. (2011) also found an association between colonization status of sows and their piglets. However, these studies examined only MRSA and did not evaluate the isolates further, either phenotypically or genotypically (Broens et al., 2011, Verhegghe et al., 2011). No study to date has investigated and characterized strains of MSSA or MRSA colonizing pigs throughout each production stage. Such studies are essential to provide a better understanding of transmission patterns of this pathogen as a basis for the design of future control programmes. A primary objective of this study was to evaluate S. aureus colonization in individual pigs over time, including whether pigs carry the same strain of the bacterium throughout production. A second objective was to determine the effect of a sow's colonization status on her piglets. The final objective was to fully characterize S. aureus isolated during the different production stages, including antimicrobial resistance patterns. At the time of the study (2011), Irish pigs were considered free of MRSA (EFSA, 2009, Horgan et al., 2011).
Section snippets
Animals and sampling
Pigs in a large, 2000-sow farrow-to-finish commercial unit were sampled and found to be positive for S. aureus. The unit was selected because it was typical of large units in Ireland and the farmer was willing to cooperate. It was a closed farm whereby all the piglets were born on the farm and no pigs were purchased. There were 30 members of staff who were each assigned to work with pigs in a particular production stage only. First stage weaned pigs received in-feed antimicrobials for the
Sow status
Nasal swabs from a total of 16 of the 50 sows sampled seven days prior to farrowing were positive and of these, four sows were positive in both the vagina and nares. Six of the sows were chosen for inclusion in this study as follows; two nasal positive sows, two nasal and vaginal positive sows and two negative sows. Of the six sows that were chosen and sampled two days after farrowing both of the nasal positive sows remained colonized, one of the nasal and vaginal positive sows was positive at
Discussion
This study investigated the transmission and persistence of S. aureus in individual pigs throughout the production cycle. Significant findings include the identification and detailed characterization for the first time of S. aureus isolates from Irish pigs and demonstration of the influence of the S. aureus colonization status of the sow on the status of her piglets. In addition, this study provided further information on the possible influence of management practices at weaning on S. aureus
Acknowledgements
This research was funded by the Department of Agriculture, Food and the Marine under the Food Institutional Research Measure, project 08 RD D 680, National Development Programme. The authors wish to express their thanks to the farmer and staff who facilitated the study on their unit and to Dr. G. Sayers who assisted with the statistical analysis.
References (39)
- et al.
High prevalence of methicillin resistant Staphylococcus aureus in pigs
Vet. Microbiol.
(2007) - et al.
A study of the prevalence of methicillin-resistant Staphylococcus aureus in pigs and in personnel involved in the pig industry in Ireland
Vet. J.
(2011) - et al.
Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers
Vet. Microbiol.
(2008) - et al.
Genotyping of Staphylococcus aureus isolates from diseased poultry
Vet. Microbiol.
(2013) - et al.
Methicillin-resistant Staphylococcus aureus (MRSA) isolated from animals and veterinary personnel in Ireland
Vet. Microbiol.
(2005) - et al.
Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in China
Vet. Microbiol.
(2009) - et al.
Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs
Emerg. Infect. Dis.
(2005) - et al.
lme4: Linear Mixed-effects Models Using S4 Classes (2012). R Package Version 0.999999-0
(2012) - et al.
Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings
Vet. Microbiol.
(2009) - et al.
Longitudinal study on transmission of MRSA CC398 within pig herds
BMC Vet. Res.
(2011)
Performance Standards for Antimicrobial Disk Susceptibility Tests; Twenty-third informational supplement (M100-S3)
Transmission Dynamics of Methicillin-Resistant Staphylococcus aureus in Pigs
Front. Microbiol.
Sampling, prevalence and characterization of methicillin-resistant Staphylococcus aureus on two Belgian pig farms
Vet. Sci. Dev.
Prevalence, antibiotic resistance and molecular characterisation of Staphylococcus aureus in pigs at agricultural fairs in the USA
Vet. Rec.
Analysis of the baseline survey on the prevalence of meticillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU 2008 [1] – part A: MRSA prevalence estimates
EFSA J.
EUCAST breakpoint tables for interpretation of MICs and zone diameters Version 4.0, valid from 2014-01-01
Determining the genetic structure of the natural population of Staphylococcus aureus: a comparison of multilocus sequence typing with pulsed-field gel electrophoresis, randomly amplified polymorphic DNA analysis, and phage typing
J. Clin. Microbiol.
Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry
Vet. Microbiol.
Detection and characterisation of SCCmec remnants in multiresistant methicillin-susceptible Staphylococcus aureus causing a clonal outbreak in a Swedish country
Eur. J. Clin. Microbiol. Infect. Dis.
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Longitudinal study on the colonisation and transmission of methicillin-resistant Staphylococcus aureus in pig farms
2016, Veterinary MicrobiologyCitation Excerpt :To date, little is known about the dynamics of MRSA in pigs because only a few longitudinal studies have been conducted. Those longitudinal studies that have been conducted examined the MRSA status in pigs mostly until slaughter age (Broens et al., 2012; Burns et al., 2014; Verhegghe et al., 2013) or even just until the age of 70 days (Weese et al., 2011). Moreover, these studies did not provide results from individual pigs.
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These authors contributed equally to the work reported.