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Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands

  • M. N. MULDERS (a1), A. P. J. HAENEN (a1), P. L. GEENEN (a1), P. C. VESSEUR (a2), E. S. POLDERVAART (a3), T. BOSCH (a1), X. W. HUIJSDENS (a1), P. D. HENGEVELD (a1), W. D. C. DAM-DEISZ (a1), E. A. M. GRAAT (a4), D. MEVIUS (a5) (a6), A. VOSS (a7) and A. W. VAN DE GIESSEN (a1)...

To determine methicillin-resistant Staphylococcus aureus (MRSA) carriage in poultry and slaughterhouse personnel, 40 Dutch broiler flocks, in six slaughterhouses and 466 personnel were sampled. Of the employees, 26 were positive (5·6%), indicating a higher risk of exposure when compared to the general Dutch population (0·1%). This risk was significantly higher for personnel having contact with live animals (5·2%) – especially hanging broilers on the slaughterline (20·0%) – than for all other personnel (1·9%). Conventional electric stunning conferred a significantly higher risk of MRSA carriage for employees than CO2 stunning (9·7% vs. 2·0%). A total of 405 broilers were sampled upon their arrival at the slaughterhouse, of which 6·9% were positive. These broilers originated from 40 Dutch slaughter flocks of which 35·0% were positive. MRSA contamination in the different compartments of slaughterhouses increased during the production day, from 8% to 35%. Of the 119 MRSA isolates, predominantly livestock-associated MRSA ST398 was found, although 27·7% belonged to ST9 (spa type t1430). There is an increased risk of MRSA carriage in personnel working at broiler slaughterhouses, particularly those having contact with live animals.

Corresponding author
*Author for correspondence: Dr M. N. Mulders, Epidemiology and Surveillance Unit, Centre for Infectious Disease Control Netherlands (CIb), National Institute of Public Health and the Environment (RIVM), P.O. Box 1, NL-3720 BA Bilthoven, The Netherlands. (Email:
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1.Grundmann H, et al. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 2006; 368: 874885.
2.Wertheim HF, et al. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. Journal of Hospital Infection 2004; 56: 321325.
3.Dutch Foundation of the Working Party on Antibiotic Policy (SWAB). Nethmap 2009 – Consumption of antimicrobial agents and antimicrobial resistance among medically important bacteria in the Netherlands. Amsterdam, 2009.
4.European Antimicrobial Resistance Surveillance System (EARSS). EARSS Annual Report 2008. Bilthoven, The Netherlands: National Institute for Public Health and the Environment (RIVM), 2009.
5.Huijsdens XW, et al. Community-acquired MRSA and pig-farming. Annals of Clinical Microbiology and Antimicrobials 2006; 5: 26.
6.van Loo I, et al. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerging Infectious Diseases 2007; 13: 18341839.
7.Voss A, et al. Methicillin-resistant Staphylococcus aureus in pig farming. Emerging Infectious Diseases 2005; 11: 19651966.
8.Haenen A, et al. Surveillance of MRSA in the Netherlands in 2007: an increasing trend of livestock-related MRSA. Infectieziekten Bulletin 2009; 20: 138145. Neeling AJ, et al. High prevalence of methicillin resistant Staphylococcus aureus in pigs. Veterinary Microbiology 2007; 122: 366772.
10.Van Den Broek IVF, et al. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiology and Infection 2009; 137: 700708.
11.Graveland HW, et al. Methicillin-resistant Staphylococcus aureus (MRSA) in veal calf farmers and veal calves in The Netherlands. In: ASM Conference on Antimicrobial Resistance in Zoonotic Bacteria and Foodborne Pathogens, Copenhagen. Copenhagen, Denmark, 2008, pp. 6263. Boer E, et al. Prevalence of methicillin-resistant Staphylococcus aureus in meat. International Journal of Food Microbiology 2008; 134: 5256.
13.Nemati M, et al. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrobial Agents and Chemotherapy 2008; 52: 38173819.
14.Persoons D, et al. Methicillin-resistant Staphylococcus aureus in poultry. Emerging Infectious Diseases 2009; 15: 452453.
15.Lee JH. Methicillin (Oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Applied Environmental Microbiology 2003; 69: 64896494.
16.Kitai S, et al. Characterization of methicillin-resistant Staphylococcus aureus isolated from retail raw chicken meat in Japan. Journal of Veterinary Medical Science 2005; 67: 107110.
17.Quddoumi S, et al. Isolation and characterisation of methicillin-resistant Staphylococcus aureus from livestock and poultry meats. Annals of Microbiology 2006; 56: 155161.
18.Lopez M, et al. Detection of Enterococcus faecium and methicillin-resistant Staphylococcus aureus in food of animal origin [in Spanish]. In: National Congress of the Spanish Society of Infectious Diseases and Clinical Microbiology (SEIMC). Madrid, Spain, 2008.
19.Leenders A, et al. Pig-MRSA on a poultry farm? [in Dutch]. Infectieziekten Bulletin 2007; 18: 4344.
20.Lwanga SK, et al. Sample Size Determinations in Health Studies. Geneva: World Health Organization, 1991.
21.Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 19th informational supplement M100-S19. Wayne, PA, USA: Clinical and Laboratory Standards Institute, 2009.
22.Martineau F, et al. Species-specific and ubiquitous-DNA-based assays for rapid identification of Staphylococcus aureus. Journal of Clinical Microbiology 1998; 36: 618623. Neeling AJ, et al. Resistance of staphylococci in The Netherlands: surveillance by an electronic network during 1989–1995. Journal of Antimicrobial Chemotherapy 1998; 41: 93–101.
24.Lina G, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clinical Infectious Diseases 1999; 29: 11281132.
25.Harmsen D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. Journal of Clinical Microbiology 2003; 41: 54425448.
26.Enright MC, et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. Journal of Clinical Microbiology 2000; 38: 10081015.
27.Liang KY, et al. Longitudinal data analysis using generalized linear models. Biometrika 1986; 73: 1322.
28.Fleiss JL. Statistical Methods for Rates and Proportions, 2nd edn. Oxford, UK: Wiley-Interscience, 1981, p. 223.
29.Thrusfield M. Veterinary Epidemiology, 2nd edn. Oxford, UK: Blackwell Science Ltd, 1995, pp. 483.
30.Rasschaert G, et al. Impact of the slaughter line contamination on the presence of Salmonella on broiler carcasses. Journal of Applied Microbiology 2007; 103: 333341.
31.Genigeorgis C, et al. Campylobacter jejuni infection on poultry farms and its effect on poultry meat contamination during slaughtering. Journal of Food Protection 1986; 49: 895903.
32.Armand-Lefevre L, et al. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerging Infectious Diseases 2005; 11: 711714.
33.Cui S, et al. Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. Journal of Antimicrobial Chemotherapy 2009; 64: 680683.
34.Kehrenberg C, et al. Methicillin-resistant and -susceptible Staphylococcus aureus strains of clonal lineages ST398 and ST9 from swine carry the multidrug resistance gene cfr. Antimicrobial Agents and Chemotherapy 2009; 53: 779781.
35.Wagenaar JA, 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. Veterinary Microbiology 2009; 139: 405409.
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Epidemiology & Infection
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