Skip to main content
NCBI home page
EFSA Journal logoLink to EFSA Journal
. 2008 Jul 14;6(7):732. doi: 10.2903/j.efsa.2008.732

Technical guidance ‐ Update of the criteria used in the assessment of bacterial resistance to antibiotics of human or veterinary importance

European Food Safety Authority (EFSA)
PMCID: PMC10193621  PMID: 37213835

The content is available as a PDF (300.3 KB).

Technical guidance prepared by the Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) on the update of the criteria used in the assessment of bacterial resistance to antibiotics of human or veterinary importance. The EFSA Journal (2008) 732, 1–15: output obsolete

Panel members: Georges Bories, Paul Brantom, Joaquim Brufau de Barberà, Andrew Chesson, Pier Sandro Cocconcelli, Bogdan Debski, Noël Dierick, Anders Franklin, Jürgen Gropp, Ingrid Halle, Christer Hogstrand, Joop de Knecht, Lubomir Leng, Anne‐Katrine Lundebye Haldorsen, Alberto Mantovani, Miklós Mézes, Carlo Nebbia, Walter Rambeck, Guido Rychen, Atte von Wright and Pieter Wester

Acknowledgement: The European Food Safety Authority wishes to thank Dr Gianni Pozzi and Dr Lorenzo Morelli for their contribution to this opinion.

Adoption date: 18 June 2008

Published date: 14 July 2008

Question number: EFSA‐Q‐2008‐004

References

  1. ACE‐ART : Assessment and Critical Evaluation of Antibiotic Resistance Transferability in Food Chain, EU Project. (CT‐2004‐506214). (www.aceart.net/).
  2. Arbeloa, A. , Segal, H. , Hugonnet, J.E. , Josseaume, N. , Dubost, L. , Brouard, J.P. , Gutmann, L. , Mengin‐Lecreulx, D. and Arthur, M. , 2004. Role of class A penicillin‐binding proteins in PBP5‐mediated beta‐lactam resistance in Enterococcus faecalis . J. Bacteriol. 186, 1221–1228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beinlich, K.L. , Chuanchuen, R. and Schweizer, H.P. , 2001. Contribution of multidrug efflux pumps to multiple antibiotic resistance in veterinary clinical isolates of Pseudomonas aeruginosa . FEMS Microbiol. Lett. 198, 129–134. [DOI] [PubMed] [Google Scholar]
  4. Burrus, V. , and Waldor, M.K. , 2004. Shaping bacterial genomes with integrative and conjugative elements. Res. Microbiol. 155 (5), 376–86. [DOI] [PubMed] [Google Scholar]
  5. Cocconcelli, P.S. , Cattivelli, D. and Gazzola, S. , 2004. Gene transfer of vancomycin and tetracycline resistances among Enterococcus faecalis during cheese and sausage fermentation. Int. J. Food Microbiol. 88, 315–323. [DOI] [PubMed] [Google Scholar]
  6. Danielsen, M. , Andersen, H.S. and Wind, A. , 2004. Use of folic acid casei medium reveals trimethoprim susceptibility of Lactobacillus species. Lett. Appl. Microbiol. 38 (3), 206–10. [DOI] [PubMed] [Google Scholar]
  7. Danielsen, M. and Wind, A. , 2003. Susceptibility of Lactobacillus spp. to antimicrobial agents. Int. J. Food. Microbiol. 82, 1–11. [DOI] [PubMed] [Google Scholar]
  8. DANMAP 2006. Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. ISSN 1600–2032 (www.danmap.org).
  9. Doktor, S.Z. , Shortridge, V.D. , Beyer, J.M. and Flamm, R.K. , 2004. Epidemiology of macrolide and/or lincosamide resistant Streptococcus pneumoniae clinical isolates with ribosomal mutations. Diagn. Microbiol. Infect. Dis. 49, 47–52. [DOI] [PubMed] [Google Scholar]
  10. Franz, C. , Stiles, M. , Schleifer, K.H. and Holzapfel, W. , 2004. Enterococci in foods‐a conundrum for food safety. Int. J. Food. Microbiol. 88, 105–122. [DOI] [PubMed] [Google Scholar]
  11. Ferber, D. , 2003. Microbiology: Triple‐threat microbe gained powers from another bug. Science. 302, 1488. [DOI] [PubMed] [Google Scholar]
  12. FINRES‐Vet 2005–2006 (www.evira.fi).
  13. Flensburg, J. and Skold, O. , 1984. Regulatory changes in the formation of chromosomal dihydrofolate reductase causing resistance to trimethoprim. J. Bacteriol. 159, 184–190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Florez, A.B. , Delgado, S. and Mayo, B. , 2005. Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can. J. Microbiol. 51, 51–58. [DOI] [PubMed] [Google Scholar]
  15. Gevers, D. , Masco, L. , Baert, L. , Huys, G. , Debevere, J. and Swings, J. , 2003. Prevalence and diversity of tetracycline resistant lactic acid bacteria and their tet genes along the process line of fermented dry sausages. System. Appl. Microbiol. 26, 277–283. [DOI] [PubMed] [Google Scholar]
  16. Gfeller, K.Y. , Roth, M. , Meile, L. and Teuber, M. , 2003. Sequence and genetic organization of the 19.3‐kb erythromycin‐ and dalfopristin‐resistance plasmid pLME300 from Lactobacillus fermentum ROT1 Plasmid. 50, 190–201. [DOI] [PubMed] [Google Scholar]
  17. Grohmann, E. , Muth, G. and Espinosa, M. , 2003. Conjugative plasmid transfer in gram‐positive bacteria. Microbiol. Mol. Biol. Rev. 67, 277–301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goodyear, K.L. , 2002. DEFRA Antimicrobial Resistance Coordination Group. Veterinary surveillance for antimicrobial resistance. J. Antimicrob. Chemother. 50 (61), 2–4. [DOI] [PubMed] [Google Scholar]
  19. Hayes, J.R. English, L.L. , Carr, L.E. , Wagner, D.D. and Joseph, S.W. , 2004. Multiple‐antibiotic resistance of Enterococcus spp. isolated from commercial poultry production environments. Appl. Environ. Microbiol. 70, 6005–6011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Huys, G. , D'Haene, K. and Swings, J. , 2002. Influence of the culture medium on antibiotic susceptibility testing of food‐associated lactic acid bacteria with the agar overlay disc diffusion method. Lett. Appl. Microbiol. 34, 402–406. [DOI] [PubMed] [Google Scholar]
  21. Jensen, V.F. , Neimann, J. , Hammerum, A.M. , Molbak, K. and Wegener, H.C. , 2004. Does the use of antibiotics in food animals pose a risk to human health? An unbiased review? J. Antimicrob. Chemother. 54, 274–275. [DOI] [PubMed] [Google Scholar]
  22. Katla, A.K. , Kruse, H. , Johnsen, G. and Herikstad, H. , 2001. Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. Int. J. Food Microbiol. 67 (1–2), 147–152. [DOI] [PubMed] [Google Scholar]
  23. Leavis, H.L. , Willems, R.J. , Top, J. , Spalburg, E. , Mascini, E.M. , Fluit, A.C. , Hoepelman, A. , de Neeling, A.J. and Bonten, M.J.R. , 2003. Epidemic and nonepidemic multidrug‐resistant Enterococcus faecium . Emerg. Infect. Dis. 9, 1108–1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MARAN 2005. Monitoring of Antimicrobial Resistance and Antibiotic Usage in Animals in the Netherlands in 2002. (www.vwa.nl).
  25. Molbak, K. , 2004. Spread of Resistant Bacteria and Resistance Genes from Animals to Humans ‐ The Public Health Consequences. J. Vet. Med. B. Infect. Dis. Vet. Public Health. 51: 364–369. [DOI] [PubMed] [Google Scholar]
  26. Moreno, M.A. , Domínguez, L , Teshager, T , Herrero, I.A. and Porrero, M.C. , 2000. Antibiotic resistance monitoring: the Spanish programme. The VAV Network. Red de Vigilancia de Resistencias Antibioticas en Bacterias de Origen Veterinario. Int. J. Antimicrob. Agents. 14. 285‐290. [DOI] [PubMed] [Google Scholar]
  27. Naas, T. , Mikami, Y. , Imai, T. , Poirel, L. and Nordmann, P. , 2001. Characterization of In53, a class 1 plasmid‐ and composite transposon‐located integron of Escherichia coli which carries an unusual array of gene cassettes. J. Bacteriol. 183, 235–249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. NORM/NORM‐VET 2006. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway, ISSN:1502–2307. (www.antibiotikaresistens.no).
  29. Poole, K. , 2002. Mechanisms of bacterial biocide and antibiotic resistance. J. Appl. Microbiol. 92 (Suppl 1) 55–64S. [PubMed] [Google Scholar]
  30. Sanders et al. FARM 2004 (www.afssa.fr)
  31. SWEDRES/SVARM 2006, Swedish Veterinary Antimicrobial Resistance Monitoring/Swedish Antibiotic Utilisation and Resistance in Human Medicine. ISSN 1650‐6332. (www.sva.se).
  32. Threlfall, E.J. , Ward, L.R. , Frost, J.A. and Willshaw, G.A. , 2000. Spread of resistance from food animals to man‐the UK experience. Acta Vet. Scand. Suppl. 93, 63–74. [PubMed] [Google Scholar]
  33. Trieber, C.A. and Taylor, D.E. , 2002. Mutations in the 16S rRNA genes of Helicobacter pylori mediate resistance to tetracycline. J. Bacteriol. 184, 2131–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Witte, W. , 2000. Ecological impact of antibiotic use in animals on different complex microflora: environment. Int. J. Antimicrob. Agents. 14, 321–325. [DOI] [PubMed] [Google Scholar]
  35. Arias, C.A. Vallejo, M. , Reyes, J , Panesso, D. , Moreno, J. , Castañeda, E. , Villegas, M.V. , Murray, B.E. and Quinn, J.P. , 2008. Clinical and microbiological aspects of linezolid resistance mediated by the cfr gene encoding a 23S rRNA methyltransferase. J Clin Microbiol. 46, 892–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Charpentier, E. and Courvalin, P. , 1997. Emergence of the trimethoprim resistance gene dfrD in Listeria monocytogenes BM4293. Antimicr Agents Chemother. 41, 1134–1136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. EFSA (European Food Safety Authority) , 2008. Report from the Task Force on Zoonoses Data Collection including guidance for harmonized monitoring and reporting of antimicrobial in commensal Escherichia coli and Enterococcus spp. from food animals. <www.efsa.europa.eu/EFSA/efsa_locale‐1178620753812_1178697512165.htm>
  38. Egervarn, M. , Danielsen, M. , Roos, S. , Lindmark, H. , Lindgren, S. , 2007a. Antibiotic susceptibility profiles of Lactobacillus reuteri and Lactobacillus fermentum . J Food Prot. 70 (2), 412–8. [DOI] [PubMed] [Google Scholar]
  39. Egervarn, M. , Lindmark, H. , Roos, S. , Huys, G. and Lindgren, S. , 2007b. Effects of inoculum size and incubation time on broth microdilution susceptibility testing of lactic acid bacteria. Antimicrob Agents Chemother. 51 (1), 394–6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Flórez, A.B. , Egervärn, M. , Danielsen, M. , Tosi, L. , Morelli, L. , Lindgren, S. and Mayo, B. , 2006. Susceptibility of Lactobacillus plantarum strains to six antibiotics and definition of new susceptibility‐resistance cut‐off values. Microbiological Drug Resistance. 12, 252–256. [DOI] [PubMed] [Google Scholar]
  41. Florez, AB , Danielsen, M. , Korhonen, J. , Zycka, J , von Wright, A. , Bardowski, J. and Mayo, B. , 2007. Antibiotic survey of Lactococcus lactis strains to six antibiotics by Etest, and establishment of new susceptibility‐resistance cut‐off values.J Dairy Res. 74 (3), 262–8. [DOI] [PubMed] [Google Scholar]
  42. Huys, G , D'Haene, K. , Danielsen, M. , Mättö, J. , Egervärn, M. and Vandamme, P. , 2008. Phenotypic and molecular assessment of antimicrobial resistance in Lactobacillus paracasei strains of food origin. Journal of Food Protection. 71, 339–344. [DOI] [PubMed] [Google Scholar]
  43. Klare, I. , Konstabel, C. , Muller‐Bertling S., Reissbrodt, R. , Huys, G. , Vancanneyt, M. , Swings, J. , Goossens, H. and Witte, W. , 2005. Evaluation of new broth media for microdilution antibiotic susceptibility sesting of Lactobacilli, Pediococci, Lactococci, and Bifidobacteria. Appl. Environ. Microbiol. 71, 8982–8986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Korhonen, J.M. , Sclivagnotis, Y. and von Wright, A. , 2007. Characterization of dominant cultivable lactobacilli and their antibiotic resistance profiles from faecal samples of weaning piglets. J Appl Microbiol. 103, 2496–2503. [DOI] [PubMed] [Google Scholar]
  45. Young, H.K. Skurray, K.A. and Amyes, S.K. , 1987. Plasmid‐mediated trimethoprim‐resistance in Staphylococcus aureus. Characterization of the first gram‐positive plasmid dihydrofolate reductase (type S1). Biochem J. 243 (1), 309–312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Toh SM, Xiong L, Arias CA, Villegas MV, Lolans K, Quinn J and Mankin AS. (2007). Acquisition of a natural resistance gene renders a clinical strain of methicillin resistant Staphylococcus aureus resistant to the synthetic antibiotic linezolid. Mol. Microbiol. 64: 1506–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Tosi, L. , Berruti, G. , Danielsen, M. , Wind, A. , Huys, G. and Morelli, L. , 2007. Susceptibility of Streptococcus thermophilus to antibiotics. Antonie Van Leeuwenhoek. 92 (1), 21–8. [DOI] [PubMed] [Google Scholar]
  48. Matto, J. , Angela, van Hoek, H.A.M. , Domig, K.J. , Saarelaa, M. , Belén Flórez, A. , Brockmanne, E. , Amtmanne, E , Mayo, B. , Aarts, H.J.M. and Danielsen, M. , 2007. Susceptibility of human and probiotic Bifidobacterium spp. to selected antibiotics as determined by the Etest method. International Dairy Journal. 17, 1123–1131. [Google Scholar]
  49. Mory, F. , Fougnot, S. , Rabaud, C. , Schuhmacher, H. and Lozniewski, A. , 2005. In vitro activities of quinupristin/dalfopristin, linezolid and other antibiotics alone and in combination against Propionibacterium acnes isolates from central nervous system infections. Journal of Animicrobial Agents and Chemotherapy. 55, 265–268. [DOI] [PubMed] [Google Scholar]
  50. Oprica, C. and Nord, C. , 2005. European surveillance study on the antibiotic susceptibility of Propionibacterium acnes . Clinical Microbiology and Infection. 11, 204–213. [DOI] [PubMed] [Google Scholar]
  51. Roland, N. , Leclerc, A. , Fodrevez, M. , Thierry, A. , Jamet, E. and Chamba, J‐F. , 2007. Study on the antibioresistance in dairy propionic acid bacteria: a major criterion for safety evaluation. Poster in 2nd Int. Symposium on Propionibacteria & Bifidobacteria, Norway.
  52. Ross, J.I. , Snelling, A.M. , Eady, E.A. , Cove, J.H. , Cunlife, W.J. , Leyden, J.J. , Collignon, P. , Bredno, B. , Reynaud, A. , Fluhr, J. and Oshima, S. , 2001. Phenotypic and genotypic characterization of antibiotic resistant Propionibacterium acnes isolated from acne patients attending dermatology clinics in Europe, the U.S.A., Japan and Australia. British Journal of Dermatology. 144, 339–346. [DOI] [PubMed] [Google Scholar]
  53. Sidorchuk, II. , 1977. Sensitivity of Sherman's propionic acid bacilli to antibacterial preparations and vitamin B12 synthesis. Antibiotiki. 22, 1015–1017. [PubMed] [Google Scholar]

Articles from EFSA Journal are provided here courtesy of Wiley

RESOURCES