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“Is control of LA-MRSA in pigs possible and relevant? – Experiences from Norway”

Published: February 1, 2022
By: Carl Andreas Grøntvedt, DVM, Dipl.ECPHM / The Norwegian Veterinary Institute, P.O. Box 750 Sentrum, N-0106 Oslo, Norway.
Background
Staphylococcus aureus is an important cause of nosocomial and community-acquired human disease, and methicillin-resistant S. aureus (MRSA) is associated with increased morbidity, mortality and costs [1]. During the last decade, particular clones of MRSA called livestock-associated MRSA (LA-MRSA), due to their ability to colonize and persist in livestock, has emerged in most European countries [2]. The most widespread LA-MRSA in Europe and Northern America belongs to the clonal complex (CC) 398, and has been reported particularly from pigs and veal calves [3]. S. aureus, particularly LA-MRSA, is not regarded an important cause of illness in pigs, and pigs are predominately either colonized or contaminated without any signs of infection.
Internationally, the emergence of LA-MRSA in livestock has raised public health concerns [4]. For instance, in Denmark, a pig-dense country with a low prevalence of MRSA in the human population, CC398 has within a few years become the most commonly detected CC group among humans [5]. Studies has shown less human-to-human transmission of LA-MRSA than other MRSA, and that persons occupationally exposed to pigs or veal calves, and to a lesser extent their family members, are most at risk of being positive for LA-MRSA [3, 6]. More recently, LA-MRSA has also been described in persons not occupationally exposed to pigs, but living in areas with a high pig density [5, 7].
Experiences from Norway
The Norwegian pig population consists of approx. 1250 sow farms and 800 finishing pig farms with an annual production of 1.6 million slaughtered pigs. Average herd size per 2014 was 118 sows/year including sow pool systems (n=13). The production chain is organized in a pyramid structure with pure breed nucleus herds (n=40) at the top and multiplier herds (n=55) supplying the commercial sow herds (approx. 1150).
The first detection of MRSA CC398 spa-type t034 occurred through an anonymized abattoir survey in 2011 finding MRSA in samples from a single slaughterhouse [8]. The following year, an anonymized pig holding survey demonstrated CC398 in samples from a single farm of the 175 investigated [9]. In addition to the EU Baseline study investigating 252 farms [10] that only detected one human associated MRSA, these results indicated a very low prevalence of LA-MRSA in the Norwegian pig population before 2013.
Public health concerns were the rationale behind the decision made by the Norwegian authorities in 2013 to impose measures to eradicate LA-MRSA from the pig population. This “search and destroy” strategy aims to prevent pig holdings becoming a persisting domestic reservoir of MRSA with the potential of zoonotic transmission. To the authors’ knowledge, Norway is the only country having implemented such a strategy. This strategy was implemented following two separate and traceable detections of CC398 in early 2013; in samples from a fattening pig submitted for postmortem examination and a clinical isolate from a hospitalized farm worker, respectively. These findings led to two extensive outbreak investigations in the eastern and south western part of Norway, respectively, identifying a total of 24 pig farms positive for CC398.
The LA-MRSA eradication strategy includes restrictions on trade of live animals upon suspicion, depopulation of pigs in LA-MRSA positive pig holdings, thorough cleaning and disinfection of premises, a mandatory down-time and negative environmental samples from the pig barns before restocking with pigs from MRSA negative holdings. After restocking, samples are collected from animals and the environment several times to assess the effectiveness of MRSA eradication. The detailed plans and execution of the farm specific measures of cleaning and disinfection were the responsibility of the farm owner, often assisted by farm consultants from the Pig Health Service. Personnel in contact with positive pig holdings were sampled by local health care providers, and received treatment to eliminate carriage of MRSA if found positive. In Norway, MRSA in humans is a notifiable infection. Epidemiological information was collected through a purpose built questionnaire from all farms where MRSA was detected.
During 2014, all Norwegian sow farms with an inventory of more than 10 sows (n=986) were included in a national surveillance program for MRSA in pig holdings. From each farm, pooled swab cloths were collected from animals and the interior environment. This screening resulted in the finding of a single LA-MRSA positive sow farm [11]. In 2015, the surveillance program for MRSA in pigs included all nucleus and multiplier breeding farms and all fattening pig farms (n=821). In this screening, LA-MRSA was detected in four fattening pig farms and one multiplier breeding farm [12]. These two screening studies provide evidence of a continued low prevalence of LA-MRSA in the Norwegian pig population. The surveillance is continuing with a sow herd screening in 2016.
From the first traceable findings of MRSA CC398 in 2013 and until the end of December 2015, LA-MRSA has been detected in 6 separate outbreaks including a total of 60 herds in Norway. This includes all farms identified through active surveillance or outbreak investigations. In each outbreak, the primary introductions are suspected to be humans. This is in contrast to the 2010 EFSA report, identifying trade of live pigs as a major risk factor for transboundary spread of LA-MRSA [13]. Import of live pigs to Norway from other countries is negligible [14], and this is considered an important epidemiological and biosecurity feature of the Norwegian commercial pig population. However, the predominant route of further transmission within the country has been through the trade of live pigs. Whole genome sequencing was performed on MRSA isolates from all MRSA positive pig farms.
Results from follow-up testing after restocking are available from 32 pig farms that have performed MRSA eradication. In 29 (91%) of these farms, MRSA eradication was successful after the first attempt. One herd was closed after depopulation and has not been restocked. The remaining farms have not yet completed the eradication and/or followup sampling due to the short period of time that has passed since detection. Thereby, the conclusion is that MRSA eradication is possible in Norwegian pig farms.
Population surveillance, outbreak investigations and measure to eradicate LA-MRSA from pig farms is both a costly and labor intensive strategy. However, the imposed strategy has probably contributed substantially in preventing further dissemination of LA-MRSA, and in preventing an increased prevalence of LA-MRSA among pig farms and humans in Norway [15]. The strategy is therefore considered relevant under Norwegian conditions, presently characterized by; a low overall prevalence of MRSA (including LA-MRSA) in humans [15], few primary introductions of LA-MRSA to the pig population, effective eradication of MRSA from positive pig farms which thereby prevented further transmission among pig farms, and an essentially closed pig population. Any changes to any of these conditions may influence the authorities’ choice of strategy regarding LA-MRSA in the future.
   
Presented at the 24th International Pig Veterinary Society Congress. For information on the next edition, click here.

1. Köck, R., et al., Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. 2010.

2. Verkade, E. and J. Kluytmans, Livestock-associated Staphylococcus aureus CC398: Animal reservoirs and human infections. Infection Genetics and Evolution, 2014. 21: p. 523-530.

3. Graveland, H., et al., Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology, 2011. 301(8): p. 630-634.

4. Cuny, C., et al., Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. International Journal of Medical Microbiology, 2010. 300(2-3): p. 109-117.

5. DANMAP, Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark. 2014, Statens Serum Institut, National Veterinary Institute, Technical University of Denmark, National Food Institute, Technical University of Denmark.

6. Garcia-Graells, C., et al., Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398. Epidemiology and Infection, 2012. 140(3): p. 383-389.

7. Larsen, J., et al., Meticillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Eurosurveillance, 2015. 20(37): p. 5-13.

8. NORM-VET, NORM., Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway, in Tromsø/Oslo. 2011.

9. NORM-VET, NORM., Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway, in Tromsø/Oslo. 2012.

10. EFSA, Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008 [1] - Part A: MRSA prevalence estimates., in EFSA Journal 2009, EFSA (European Food Safety Authority). p. 82.

11. Urdahl, A.M., et al., The surveillance programme for methicillin resistant Staphylococcus aureus in pigs in Norway 2014, in Surveillance programmes for terrestrial and aquatic animals in Norway. 2014, The Norwegian Veterinary Institute: http://www.vetinst.no/.

12. Urdahl, A.M., et al., The surveillance programme for methicillin resistant Staphylococcus aureus in pigs in Norway 2015, in Surveillance programmes for terrestrial and aquatic animals in Norway. 2015, The Norwegian Veterinary Institute: http://www.vetinst.no.

13. EFSA, Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008 - Part B: factors associated with MRSA contamination of holdings, in EFSA Journal 2010, EFSA (European Food Safety Authority). p. 67.

14. KOORIMP, Årsmelding 2014 KOORIMP og KIF. 2014, Husdyrnæringens koordineringsenhet for smittebeskyttelse ved import.

15. NORM-VET, NORM., Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway, in Tromsø/Oslo. 2014.

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Authors:
Carl Andreas Grøntvedt
National Veterinary Institute (NVI)
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