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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

EFSA Journal 2010; 8(6):1597 [67 pp.]. doi:10.2903/j.efsa.2010.1597
European Food Safety Authority Acknowledgment EFSA wishes to thank the members of the Task Force on Zoonoses Data Collection that reviewed and endorsed this report: Andrea Ammon, Alenka Babusek, Lisa Barco, Marta Bedriova, Susan Chircop, Marianne Chriel, Georgi Chobanov, Ingrid Dan, Jürg Danuser, Noel Demicoli, Kris De Smet, Sylvie Francart, Matthias Hartung, Birgitte Helwigh, Merete Hofshagen, Patrícia Inácio, Sarolta Idei, Elina Lahti, Lesley Larkin, Peter Much, Edith Nagy, Lisa O’Connor, Rob Van Oosterom, Jacek Osek, José Luis Saez Llorente, Antonio Petrini, Melanie Picherot, Christodoulos Pipis, Saara Raulo, Petr Šatrán, Joseph Schon, Jelena Sõgel, Snieguole Sceponaviciene, Ana María Troncoso González, Kilian Unger, Luc Vanholme, Dimitris Vourvidis, Nicole Werner-Keišs. The contribution of the members of the working group that prepared this scientific report is gratefully acknowledged: Antonio Battisti, Hanne-Dorthe Emborg, Concepción Porrero, Pascal Sanders, Gertraud Schuepbach, Christopher Teale, Bernd-Alois Tenhagen, and Jaap Wagenaar; and that of EFSA’s contractors: Hendriek Boshuizen from National Institute for Public Health and Environment (RIVM); Frank Aarestrup, Henrik Hasman, and Antonio Vieira from Danish Technical University, National Food Institute, as well as EFSA’s staff members: Pierre-Alexandre Belœil, Giusi Amore, Francesca Riolo, and Frank Boelaert for the support provided to this EFSA scientific output. Contact zoonoses@efsa.europa.eu
Type: Scientific Report of EFSA On request from: European Commission Question number: EFSA-Q-2008-417B Approved: 10 May 2010 Published: 03 June 2010 Affiliation: European Food Safety Authority (EFSA), Parma, Italy
Abstract

A European Union-wide baseline survey on methicillin-resistant Staphylococcus aureus (MRSA) was conducted in 2008 in holdings with breeding pigs. A total of 1,600 holdings housing and selling mainly breeding pigs (breeding holdings), and 3,473 holdings housing breeding pigs and selling mainly pigs for fattening or slaughter (production holdings) from 24 Member States and two other European countries were included in the survey. Pooled dust samples collected from holdings were tested for MRSA. The likelihood of a limited set of holding-level factors to be potentially associated with MRSA-positive holdings were analysed by multiple regression analysis, separately for breeding and for production holdings. These analyses showed that the risk of holdings of being contaminated with MRSA increased as the number of breeding pigs in the holding increased, in both breeding and production holdings. Analyses at country-level demonstrated a strong positive association between the prevalence of MRSA-positive breeding holdings and MRSA-positive production holdings, suggesting a vertical dissemination of MRSA between the holdings. A complementary country-level analysis using TRAde Control and Expert System data on intra-Community trade further disclosed strong positive associations between the prevalence of MRSA-positive holdings with breeding pigs and the volume of imported breeding pigs, and a proxy for numbers of imported breeding pigs at risk of being colonised with MRSA. Further investigation of the diversity of MRSA Staphylococcus protein A types (spa-types) showed that the distribution of spa-types differed significantly between countries. Spa-types belonging to lineages MRSA ST1, ST5, and ST8 tested negative for Panton-Valentine leukocidin (PVL) toxin genes, suggesting that these strains were not related to the PVL-positive MRSA strains known in human medicine. Further investigations of risk factors for MRSA holding contamination at country level, as well as investigations on prevention and intervention measures to contain MRSA contamination in pig holdings are recommended.

© European Food Safety Authority, 2010

Summary

A European Union-wide survey was carried out in parallel with a baseline survey on Salmonella in holdings with breeding pigs to assess the prevalence and diversity of methicillin-resistant Staphylococcus aureus (MRSA) in pig primary production and to provide information on potential factors associated with its prevalence. The survey distinguished between breeding holdings (holdings housing breeding pigs and delivering replacement breeding pigs to breeding holdings and production holdings) and production holdings with breeding pigs (holdings housing breeding pigs and producing mainly pigs for fattening or slaughter). The samples for MRSA detection were taken concomitantly in the same holdings that were selected for the Salmonella spp. investigation, between January and December 2008. Environmental dust samples were collected from five different pens per holding. These samples were pooled per holding and analysed to determine whether the holding was contaminated with MRSA or not. All isolates were sub-typed by Staphylococcus protein A typing (spa-typing). A total of 5,073 holdings with breeding pigs with validated results from the European Union (24 Member States), Norway and Switzerland were included in the survey analyses, corresponding to information on 1,600 breeding holdings and 3,473 production holdings. The analysis of the prevalence of MRSA-positive holdings was carried out earlier and was published by the European Food Safety Authority on 24 November 2009 in the Part A report. The present Part B report contains a risk factor analysis for MRSA contamination of breeding and of production holdings, a correlation analysis between MRSA prevalence in breeding and in production holdings, as well as an investigation of the association between intra-Community imports of breeding pigs and MRSA prevalence of a country. In addition, further analyses of the distribution of the spa-types of MRSA isolates across Europe, as well as the results of the tests for Panton-Valentine leukocidin (PVL) genes in a subset of isolates originating from the baseline survey, are also included.

Additional data on a limited set of holding-level factors collected by the participating countries as part of the Salmonella survey, were investigated with respect to their association with the likelihood of a holding to be MRSA-positive. This included the date of sampling during the year, the types of breeding holdings (nucleus or multiplier) and production holdings (farrow-to-finish, farrow-to-weaner or farrow-to-grower), the size of the holding, the gilt and boar replacement policies of the holding, and the days of delay between sampling and testing in the laboratory. The likelihood of these factors to be potentially associated with MRSA-positive holdings were analysed by multiple regression analysis, separately for breeding and production holdings. The results showed that the risk of holdings of being contaminated with MRSA increased as the number of breeding pigs in the holding increased, both among breeding and production holdings. This effect might reflect a greater risk of introduction and/or of within-holding diffusion of MRSA in larger holdings, for example through a more intensive introduction of replacement breeding stock, but also the impact of other unmeasured underlying risk factors that are associated with structural characteristics and/or managerial practices typical for larger holdings. In addition, the risks of breeding holdings and production holdings being contaminated with MRSA varied significantly between countries even when accounting for the effect of the holding size.

As breeding pigs are intensively traded within and between Member States and may, once colonised, disseminate MRSA to destination holdings, the association between the prevalence of MRSA-positive breeding holdings and the prevalence of MRSA-positive production holdings in a country was investigated and a strong, positive association was observed. Moreover, country-level analyses using TRACES (TRAde Control and Expert System of the Community) data on intra-Community trade of breeding pigs further disclosed a strong, positive association between the prevalence of MRSA-positive holdings and the volume of imported breeding pigs in the country. This association was particularly strong with a proxy for the number of imported breeding pigs that are at risk of being colonised with MRSA. This proxy was obtained by summing the country-of-origin-specific combinations of the number of imported breeding pigs and MRSA holding prevalence. These positive associations are suggesting of a vertical (top-down) dissemination of MRSA in the pig production pyramid within the country and also that the risk of MRSA contamination of holdings with breeding pigs in a country increases as the volume of imports of breeding pigs from countries with MRSA increases.

An important diversity in MRSA spa-types was observed in the European Union, and the spa-type distributions of MRSA isolates were found to vary significantly between participating countries. MRSA isolates with spa-types belonging to lineages ST1, ST5 and ST8, which are spa-types known in human medicine, were tested for PVL toxin genes. None of the tested isolates tested positive for PVL toxin genes, suggesting that those strains were not related to PVL-positive, Community-Associated MRSA strains prevalent in some parts of the world in humans.

Since only a limited set of factors potentially associated with MRSA-positive holdings were analysed in the framework of the survey, it would be useful to perform further national studies to identify more closely the factors that put holdings with breeding pigs at risk of MRSA contamination in specific countries. Also investigations on the impact of addressing MRSA through on-farm biosecurity and managerial practices are needed as a basis for the development of potential, future, measures of prevention and intervention. In particular, it would be important to investigate measures to prevent the introduction of MRSA into MRSA-negative holdings, such as the checking of the MRSA status of replacement breeding pigs. Furthermore, it is advisable to characterise MRSA isolates derived from pigs by using molecular typing methods in order to follow the diversity of the MRSA population.

 

Keywords

MRSA, spa-typing, pigs, breeding pigs, baseline survey, risk factors, EU