Technical specifications on the harmonised monitoring and reporting of antimicrobial resistance in methicillin-resistant Staphylococcus aureus in food-producing animals and food

EFSA Journal

Volumn 10, Issue 10, 2012, Pages

[No Author Info available]

Author keywords

antimicrobial resistance; Harmonisation; methicillin resistant Staphylococcus aureus; monitoring; reporting

Indexed keywords

EID: 85014899015     PISSN: None     EISSN: 18314732     Source Type: Journal    
DOI: 10.2903/j.efsa.2012.2897     Document Type: Article

References (75)

1. Agersø Y, Hasman H, Cavaco LM, Pedersen K and Aarestrup FM, 2012. Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Veterinary Microbiology, 157, 246–250.
2. Alt K, Fetsch A, Schroeter A, Guerra B, Hammerl JA, Hertwig S, Senkov N, Geinets A, Mueller-Graf C, Braeunig J, Kaesbohrer A, Appel B, Hensel A and Tenhagen BA, 2011. Factors associated with the occurrence of MRSA CC398 in herds of fattening pigs in Germany. BMC Veterinary Research, 7, 69.
3. Argudín MA, Rodicio MR and Guerra B, 2010. The emerging methicillin-resistant Staphylococcus aureus ST398 clone can easily be typed using the Cfr9I SmaI-neoschizomer. Letters in Applied Microbiology, 50, 127–130.
4. Bisdorff B, Scholhölter JL, Claußen K, Pulz M, Nowak D and Radon K, 2012. MRSA-ST398 in livestock farmers and neighbouring residents in a rural area in Germany. Epidemiology and Infection, 140, 1800–1808.
5. Böcher S, Middendorf B, Westh H, Mellmann A, Becker K, Skov R and Friedrich AW, 2010. Semi-selective broth improves screening for methicillin-resistant Staphylococcus aureus. Journal of Antimicrobial Chemotherapy, 65, 717–720.
6. Bosch T, de Neeling AJ, Schouls LM, van der Zwaluw KW, Kluytmans JA, Grundmann H and Huijsdens XW, 2010. PFGE diversity within the methicillin-resistant Staphylococcus aureus clonal lineage ST398. BMC Microbiology, 10, 40.
7. Broens EM, Graat EAM, Van Der Wolf PJ, Van De Giessen AW and De Jong MCM, 2011a. Prevalence and risk factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Preventive Veterinary Medicine, 102, 41–49.
8. Broens EM, Graat EAM, Van Der Wolf PJ, Van De Giessen AW and De Jong MCM, 2011b. Transmission of methicillin resistant Staphylococcus aureus among pigs during transportation from farm to abattoir. The Veterinary Journal, 189, 302–305.
9. Broens EM, Graat EAM, Engel B, van Oosterom RAA, van de Giessen AW and van der Wolf PJ, 2011c. Comparison of sampling methods used for MRSA-classification of herds with breeding pigs. Veterinary Microbiology, 147, 440–444.
10. Brown DFJ, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ and Wren MWD, 2005. Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA). Journal of Antimicrobial Chemotherapy, 56, 1000–1018.
11. Cameron AR and Baldock FC, 1998. A new probability formula for surveys to substantiate freedom from disease. Preventive Veterinary Medicine, 34, 1–17.
12. Centers for Disease Control and Prevention (CDC), 2002. Staphylococcus aureus resistant to vancomycin – United States, 2002. Morbidity and Mortality Weekly Report, 51, 565–567.
13. Ciccolini M, Dahl J, Chase-Topping ME and Woolhouse MEJ, in press. Disease transmission on fragmented contact networks: Livestock-associated Methicillin-resistant Staphylococcus aureus in the Danish pig-industry. Epidemics.
14. Crombé F, Willems G, Dispas M, Hallin M, Denis O, Suetens C, Gordts B, Struelens M and Butaye P, 2012. Prevalence and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus among pigs in Belgium. Microbial Drug Resistance, 18, 125–131.
15. Cuny C, Layer F, Strommenger B and Witte W, 2011. Rare occurrence of methicillin-resistant Staphylococcus aureus CC130 with a novel mecA homologue in humans in Germany. PLoS ONE, 6, e24360, 1–5.
16. DANMAP (The Danish Integrated Antimicrobial Resistance Monitoring and Research Programme), 2010. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, food and humans in Denmark, 103–104. Available from www.danmap.org
17. de Boer E, Zwartkruis-Nahuis JTM, Wit B, Huijsdens XW, de Neeling AJ, Bosch T, van Oosterom RAA, Vila A and Heuvelink AE, 2009. Prevalence of methicillin-resistant Staphylococcus aureus in meat. International Journal of Food Microbiology, 134, 52–56.
18. EFSA (European Food Safety Authority), 2009a. Scientific Opinion of the Panel on Biological Hazards on a request from the European Commission on Assessment of the Public Health significance of meticillin resistant Staphylococcus aureus (MRSA) in animals and foods. The EFSA Journal, 993, 1–73.
19. EFSA (European Food Safety Authority), 2009b. Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008, Part A: MRSA prevalence estimates. EFSA Journal, 7(11):1376, 82 pp.
20. EFSA (European Food Safety Authority), 2010. 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, 8(6):1597, 67 pp.
21. EFSA (European Food Safety Authority), 2012a. Technical specifications on the harmonised monitoring and reporting of antimicrobial resistance in Salmonella, Campylobacter and indicator Escherichia coli and Enterococcus spp. bacteria transmitted through food. EFSA Journal, 10(6):2742, 64 pp.
22. EFSA (European Food Safety Authority), 2012b. Manual for Reporting on Zoonoses, Zoonotic Agents and Antimicrobial Resistance in the framework of Directive 2003/99/EC and of some other pathogenic microbiological agents for information derived from the year 2011. Supporting publications 2012: EN-266, 111 pp.
23. EFSA (European Food Safety Authority), 2012c. Technical specifications for the analysis and reporting of data on antimicrobial resistance (AMR) in the European Union Summary Report. EFSA Journal, 10(2):2587, 53 pp.
24. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2012. The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2010. EFSA Journal, 10(3):2598, 233 pp.
25. Ellington MJ, Hope R, Livermore DM, Kearns AM, Henderson K, Cookson BD, Pearson A and Johnson AP, 2010. Decline of EMRSA-16 amongst methicillin-resistant Staphylococcus aureus causing bacteraemias in the UK between 2001 and 2007. Journal of Antimicrobial Chemotherapy, 65, 446–448.
26. Enright MC, Day NPJ, Davies CE, Peacock SJ and Spratt BG, 2000. Multilocus Sequence Typing for Characterization of Methicillin-Resistant and Methicillin-Susceptible Clones of Staphylococcus aureus. Journal of Clinical Microbiology, 38, 1008–1015.
27. Friedrich A, Rau J, Hörlacher S and Spohr M, 2011. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in milk from dairy farms in Northern Wurttemberg. Tierärztliche Umschau, 66, 195–200.
28. Friese A, Schulz J, Hoehle L, Fetsch A, Tenhagen BA, Hartung J and Roesler U, 2012. Occurrence of MRSA in air and housing environment of pig barns. Veterinary Microbiology, 158, 129–135.
29. García-Ålvarez L, Holden MTG, Lindsay H, Webb CR, Brown DFJ, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RLR, Larsen AR, Skov RL, Peacock SJ, Maskell DJ and Holmes MA, 2011. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. The Lancet Infectious Diseases, 11, 595–603.
30. Geenen PL, Graat EAM, Haenen A, Hengeveld PD, van Hoek AHAM, Huijsdens XW, Kappert CC, Lammers GAC, van Duijkeren E and van de Giessen AW, 2012. Prevalence of livestock-associated MRSA on Dutch broiler farms and in people living and/or working on these farms. Epidemiology and Infection, 25, 1–10.
31. Gómez-Sanz E, Torres C, Lozano C, Fernández-Pérez R, Aspiroz C, Ruiz-Larrea F and Zarazaga M, 2010. Detection, molecular characterization, and clonal diversity of methicillin-resistant Staphylococcus aureus CC398 and CC97 in Spanish slaughter pigs of different age groups. Foodborne Pathogens and Disease, 7, 1269–1277.
32. Graveland H, van Duijkeren E, van Nes A, Schoormans A, Broekhuizen-Stins M, Oosting-van Schothorst I, Heederik D and Wagenaar JA, 2009. Evaluation of isolation procedures and chromogenic agar media for the detection of MRSA in nasal swabs from pigs and veal calves. Veterinary Microbiology, 139, 121–125.
33. Graveland H, Wagenaar JA, Heesterbeek H, Mevius D, van Duijkeren E and Heederik D, 2010. Methicillin Resistant Staphylococcus aureus ST398 in Veal Calf Farming: Human MRSA Carriage Related with Animal Antimicrobial Usage and Farm Hygiene. PLoS ONE, 5, e10990, 1–6.
34. Haran KP, Godden SM, Boxrud D, Jawahir S, Bender JB and Sreevatsan S, 2012. Prevalence and characterization of Staphylococcus aureus, including methicillin resistant Staphylococcus aureus, isolated from bulk tank milk from Minnesota dairy farms. Journal of Clinical Microbiology, 50, 688–695.
35. Hartman BJ and Tomasz A, 1984. Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus. Journal of Bacteriology, 158, 513–516.
36. Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL and Aarestrup FM, 2010. spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Veterinary Microbiology, 141, 326–331.
37. Higuchi W, Takano T, Teng LJ and Yamamoto T, 2008. Structure and specific detection of staphylococcal cassette chromosome mec type VII. Biochemical and Biophysical Research Communications, 377, 752–756.
38. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Hori S, Fukuchi Y and Kobayashi I, 1997. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet, 350, 1670–1673.
39. Johne A, Fetsch A, Kraushaar B, 2012. Organisation, Durchfürhung and Erbebnisse eines Ringversuchs zu Validierung einer qualitativen und quantitativen Methode zum Nachweis von MRSA in Hackfleish. Rundschau für Fleischhygiene und Lebensmittelüberwachung, 3, 90–91.
40. Kadlec K, Pomba CF, Couto N and Schwarz S, 2010. Small plasmids carrying vga (A) or vga (C) genes mediate resistance to lincosamides, pleuromutilins and streptogramin A antibiotics in methicillin-resistant Staphylococcus aureus ST398 from swine. Journal of Antimicrobial Chemotherapy, 65, 2692–2698.
41. Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J and Hiramatsu K, 2007. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrobial Agents and Chemotherapy, 51, 264–274.
42. Kreausukon K, Fetsch A, Kraushaar B, Alt K, Müller K, Krömker V, Zessin K-H, Käsbohrer A and Tenhagen B-A, 2012. Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. Journal of Dairy Science, 95, 4382–4388.
43. Laurent F, Chardon H, Haenni M, Bes M, Reverdy ME, Madec JY, Lagier E, Vandenesch F and Tristan A, 2012. MRSA Harboring mecA Variant Gene mecC, France. Emerging Infectious Diseases, 18, 1465–1467.
44. LeClercq R and Courvalin P, 1991a. Bacterial resistance to macrolide, lincosamide, and streptogramin antibiotics by target modification. Antimicrobial Agents and Chemotherapy, 35, 1267–1272.
45. LeClercq R and Courvalin P, 1991b. Intrinsic and unusual resistance to macrolide, lincosamide, and streptogramin antibiotics in bacteria. Antimicrobial Agents and Chemotherapy, 35, 1273–1276.
46. Levin TP, Suh B, Axelrod P, Truant AL and Fekete T, 2005. Potential Clindamycin Resistance in Clindamycin-Susceptible, Erythromycin-Resistant Staphylococcus aureus: Report of a Clinical Failure. Antimicrobial Agents and Chemotherapy, 49, 1222–1224.
47. Livermore DM, Winstanley TG and Shannon KP, 2001. Interpretative reading: recognizing the unusual and inferring resistance mechanisms from resistance phenotypes. Journal of Antimicrobial Chemotherapy, 48, 87–102.
48. Manian FA, 2003. Asymptomatic nasal carriage of mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MRSA) in a pet dog associated with MRSA infection in household contacts. Clinical Infectious Diseases, 36, e26–28.
49. McClure JA, Conly JM, Elsayed S and Zhang K, 2010. Multiplex PCR assay to facilitate identification of the recently described staphylococcal cassette chromosome mec type VIII. Molecular and Cellular Probes, 24, 229–232.
50. Milheiriço C, Oliveira DC and de Lencastre H, 2007. Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 51, 3374–3377.
51. Monecke S, Slickers P and Ehricht R, 2008. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunology and Medical Microbiology, 53, 237–251.
52. Mulders MN, Haenen APJ, Geenen PL, Vesseur PC, Poldervaart ES, Bosch T, Huijsdens XW, Hengeveld PD, Dam-Deisz WDC, Graat EAM, Mevius D, Voss A and Van De Giessen AW, 2010. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiology and Infection, 138, 743–755.
53. Nemati M, Hermans K, Lipinska U, Denis O, Deplano A, Struelens M, Devriese LA, Pasmans F and Haesebrouck F, 2008. Antimicrobial Resistance of Old and Recent Staphylococcus aureus Isolates from Poultry: First Detection of Livestock-Associated Methicillin-Resistant Strain ST398. Antimicrobial Agents and Chemotherapy, 52, 3817–3819.
54. LGA251, is present in methicillin-resistant Staphylococcus aureus isolates from a diverse range of host species. Journal of Antimicrobial Chemotherapy.
55. Persoons D, Van Hoorebeke S, Hermans K, Butaye P, de Kruif A, Haesebrouck F and Dewulf J, 2009. Methicillin-Resistant Staphylococcus aureus in Poultry. Emerging Infectious Diseases, 15, 452–453.
56. Pletinckx LJ, De Bleecker Y, Dewulf J, Rasschaert G, Goddeeris BM and De Man I, 2012. Evaluation of salt concentrations, chromogenic media and anatomical sampling sites for detection of methicillin-resistant Staphylococcus aureus in pigs. Veterinary Microbiology, 154, 363–368.
57. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R and Aarestrup FM, 2012. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio., 3, e00305–11.
58. Richter A, Sting R, Popp C, Rau J, Tenhagen B-A, Guerra B, Hafez HM and Fetsch A, 2012. Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiology and Infection, 10, 1–10.
59. Schroeter A and Käsbohrer A (eds), 2012. Deutsche Antibiotikaresistenzsituation in der Lebensmittelkette - DARLink 2009. Series title: BfR Wissenschaft 5/2012 Publisher: Bundesinstitut für Risikobewertung Berlin, Germany, 321 pp. Available from www.bfr.bund.de/cm/350/deutsche-antibiotika-resistenzsituation-in-der-lebensmittelkette-darlink-2009.pdf
60. Schulz J, Friese A, Klees S, Tenhagen BA, Fetsch A, Rösler U and Hartung J, 2012. Longitudinal Study of the Contamination of Air and of Soil Surfaces in the Vicinity of Pig Barns by Livestock-Associated Methicillin-Resistant Staphylococcus aureus. Applied and Environmental Microbiology, 78, 5666–5671.
61. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S and Kreiswirth BN, 1999. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. Journal of Clinical Microbiology, 37, 3556–3563.
62. Shore AC, Deasy EC, Slickers P, Brennan G, O'Connell B, Monecke S, Ehricht R and Coleman DC, 2011. Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 55, 3765–3773.
63. Spohr M, Rau J, Friedrich A, Klittich G, Fetsch A, Guerra B, Hammerl JA and Tenhagen B-A, 2011. Methicillin-Resistant Staphylococcus aureus (MRSA) in three dairy herds in southwest Germany. Zoonoses and Public Health, 58, 252–261.
64. LGA251. Clinical Microbiology and Infection, 18, 395–400.
65. Tenhagen B-A, Fetsch A, Stührenberg B, Schleuter G, Guerra B, Hammerl JA, Hertwig S, Kowall J, Kämpe U, Schroeter A, Bräunig J, Käsbohrer A and Appel B, 2009. Prevalence of MRSA types in slaughter pigs in different German abattoirs. Veterinary Record, 165, 589–593.
66. Tenhagen B-A, Alt K, Fetsch A, Kraushaar B, and Käsbohrer A, 2011. Methicillin-resistente Staphylococcus aureus - Monitoringprogramme. In: Erreger von Zoonosen in Deutschland im Jahr 2009. Eds Hartung M and Käsbohrer A. Bundesinstitut für Risikobewertung, Berlin, Germany, 47–52.
67. Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K and Butaye P, 2010. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary Microbiology, 144, 166–171.
68. van Rijen MML, Van Keulen PH and Kluytmans JA, 2008. Increase in a Dutch Hospital of Methicillin-Resistant Staphylococcus aureus Related to Animal Farming. Clinical Infectious Diseases, 46, 261–263.
69. ™ medium for the detection of livestock-associated methicillin-resistant Staphylococcus aureus. European Journal of Clinical Microbiology & Infectious Diseases, 30, 109–112.
70. Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, Innis B, Low DE, 2006. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Veterinary Microbiology, 115, 148–55.
71. Weese JS, Avery BP and Reid-Smith RJ, 2010. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Letters in Applied Microbiology, 51, 338–342.
72. Wootton M, Howe RA, Hillman R, Walsh TR, Bennett PM and MacGowan AP, 2001. A modified population analysis profile (PAP) method to detect hetero-resistance to vancomycin in Staphylococcus aureus in a UK hospital. Journal of Antimicrobial Chemotherapy, 47, 399–403.
73. Wootton M, Walsh TR and MacGowan AP, 2005. Evidence for reduction in breakpoints used to determine vancomycin susceptibility in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 49, 3982–3983.
74. Wootton M, MacGowan AP, Walsh TR and Howe RA, 2007. A multicenter study evaluating the current strategies for isolating Staphylococcus aureus strains with reduced susceptibility to glycopeptides. Journal of Clinical Microbiology, 45, 329–332.
75. Zhang K, McClure JA, Elsayed S, Louie T and Conly JM, 2005. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology, 43, 5026–5033.