Elsevier

Veterinary Microbiology

Volume 174, Issues 3–4, 5 December 2014, Pages 504-513
Veterinary Microbiology

A longitudinal study of Staphylococcus aureus colonization in pigs in Ireland

https://doi.org/10.1016/j.vetmic.2014.10.009Get rights and content

Abstract

The emergence of methicillin-resistant Staphylococcus aureus (MRSA) in livestock has refocused attention on S. aureus colonization and transmission in pigs. This study investigated the effect of the S. aureus colonization status of a sow on the colonization status of her piglets, and whether pigs carry the same strain of S. aureus throughout production. Nasal swabs were collected from the piglets of six healthy sows two days after birth and two days before and two days after they were moved into each production stage. The average prevalence of S. aureus colonization varied between 26% and 73%. The odds of being S. aureus positive were almost 12 times higher for piglets born to nasal-positive sows than for those born to nasal-negative sows, and three times higher again for piglets born to sows that were both nasal- and vaginal-positive. Isolates recovered from piglets immediately after birth were indistinguishable from those of the dam as determined by phenotypic and molecular typing, including microarray analysis and optical mapping. All isolates belonged to clonal complex 9 and the majority exhibited a novel spa type, t10449. The findings show that the S. aureus colonization status of the sow influences the colonization status of her piglets in the early production stages but strains carried by pigs change over time. Multiresistant S. aureus was detected, in particular post-weaning. Results suggest that sow status and management practices, including mixing of pigs and antimicrobial usage at weaning, should be considered when implementing control measures for S. aureus on a farm.

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.

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    These authors contributed equally to the work reported.

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