Quantity of the Tetracycline Resistance Genetet(M) Differs Substantially between Meat at Slaughterhouses and at Retail

Journal of Food Science

Volumn 76, Issue 6, 2011, Pages

  Hölzel, Christina Susanne ^a   Huther, Sabine Katharina ^a   Schwaiger, Karin ^a   Kämpf, Peter ^b   Bauer, Johann ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b NONE   (Germany)

Author keywords

Antimicrobial resistance; Bacterial prevalence; Quantitative PCR; Tet(M); Tetracycline resistance gene

Indexed keywords

BACTERIA (MICROORGANISMS); ENTEROCOCCUS; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; LISTERIA;

EID: 79961127996     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/j.1750-3841.2011.02239.x     Document Type: Article

References (54)

1. Aarestrup, FM. 2005. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol Toxicol 96:271-81.
2. Agersø Y, Sengeløv G, Jensen LB. 2004. Development of a rapid method for direct detection oftet(M) genes in soil from Danish farmland. Environ Int 30:117-22.
3. Aminov RI, Garrigues-Jeanjean N, Mackie RI. 2001. Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22-32.
4. Anon. 2006. Antimicrobial resistance: implications for the food system. Comp Rev Food Sci Food Safety 5:71-137. Available from: ift.org. Accessed Jun 1, 2011.
5. Aquilanti L, Garofalo C, Osimani A, Silvestri G, Vignaroli C, Clementi F. 2007. Isolation and molecular characterization of antibiotic-resistant lactic acid bacteria from poultry and swine meat products. J Food Prot 70:557-65.
6. Bejuk D, Begovac J, Gamberger D, Kucisec-Tepes N. 2000. Evaluation of phenotypic characteristics for differentiation of enterococcal species using an example based algorithm. Diagn Microbiol Infect Dis 38:201-5.
7. Bjorkroth KJ, Korkeala HJ. 1997. Use of rRNA gene restriction patterns to evaluate lactic acid bacterium contamination of vacuum-packaged sliced cooked whole-meat product in a meat processing plant. Appl Environ Microbiol 63:448-53.
8. Bryan A, Shapir N, Sadowsky MJ. 2004. Frequency and distribution of tetracycline resistance genes in genetically diverse nonselected and nonclinicalEscherichia colistrains isolated from diverse human and animal sources. Appl Environ Microbiol 70:2503-7.
9. Burdett V, Inamine J, Rajagopalan S. 1982. Heterogeneity of tetracycline resistance determinants in Streptococcus. J Bacteriol 149:995-1004.
10. Chopra I, Roberts M. 2001. Tetracycline antibiotics: mode of action applications molecular biology and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232-60.
11. Davis JA, Jackson CR. 2009. Comparative antimicrobial susceptibility ofListeria monocytogenes, L. innocua, andL. welshimeri. Microb Drug Res 15:27-32.
12. Devirgiliis C, Caravelli A, Coppola D, Barile S, Perozzi G. 2008. Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana. Int J Food Microbiol 128:378-84.
13. Devirgiliis C, Coppola D, Barile S, Colonna B, Perozzi G. 2009. Characterization of the Tn916 conjugative transposon in a food-borne strain ofLactobacillus paracasei. Appl Environ Microbiol 75:3866-71.
14. DIN 58940-81. 2002. Medical microbiology-susceptibility testing of pathogens to antimicrobial agents-Part 81: microdilution. Special requirements for testing of nonfastidious bacteria. Berlin: Beuth-Verlag.
15. DIN 58940-4/1. 2004. Medical microbiology-susceptibility testing of pathogens to antimicrobial agents-Part 4: evaluation classes of the minimum inhibitory concentration- mic-breakpoints of antibacterial agents. Berlin: Beuth-Verlag.
16. Edwards R, Dainty R, Hibbard C. 1983. The relationship of bacterial numbers and types to diamine concentration in fresh and aerobically stored beef, pork and lamb. Int J Food Sci Technol 18:777-88.
17. FEDESA. 1998. Consumption of antibiotics. Deutsches Tierärzteblatt 11:1093.
18. Garofalo C, Vignaroli C, Zandri G, Aquilanti L, Bordoni D, Osimani A, Clementi F, Biavasco F. 2007. Direct detection of antibiotic resistance genes in specimens of chicken and pork meat. Int J Food Microbiol 113:75-83.
19. Gevers D, Huys G, Swings J. 2003. In vitroconjugal transfer of tetracycline resistance fromLactobacillusisolates to other Gram-positive bacteria. FEMS Microbiol Lett 225:125-30.
20. Ghafir Y, China B, Dierick K, de Zutter L, Daube G. 2007. A seven-year survey of Campylobacter contamination in meat at different production stages in Belgium. Int J Food Microbiol 116:111-20.
21. Hayes JR, English LL, Carter PJ, Lee KY, Wagner DD, White DG. 2003. Prevalence and antimicrobial resistance of enterococcus species isolated from retail meats. Appl Environ Microbiol 69:7153-60.
22. Hölzel CS, Harms KS, Küchenhoff H, Kunz A, Müller C, Meyer K, Schwaiger K, Bauer J. 2010. Phenotypic and genotypic bacterial antimicrobial resistance in liquid pig manure is variously associated with contents of tetracyclines and sulfonamides. J. Appl. Microbiol. 108:1642-56.
23. Klare I, Witte W, Werner G, Fahr A-M. 2008. Antibiotic resistance in human medicine:Enterococcusspp. In: Bundesamt für Verbraucherschutz und Lebensmittelsicherheit ; Paul-Ehrlich- Gesellschaft für Chemotherapie e.V.; Infektiologie Freiburg: GERMAP 2008 -[Antibiotic resistance and consumption]. Rheinbach: Antiinfectives Intelligence. 149 p
24. Koutsoumanis KP, Stamatiou AP, Drosinos EH, Nychas GJ. 2008. Control of spoilage microorganisms in minced pork by a self-developed modified atmosphere induced by the respiratory activity of meat microflora. Food Microbiol 25:915-21.
25. Kraft AA, Ayres JC. 1966. Competitive growth of microorganisms and fluorescence development on inoculated chicken. J Food Sci 31:111-7.
26. Li MY, Zhou GH, Xu XL, Li CB, Zhu WY. 2006. Changes of bacterial diversity and main flora in chilled pork during storage using PCR-DGGE. Food Microbiol 23:607-11.
27. Luber P, Wagner J, Hahn H, Bartelt E. 2003. Antimicrobial resistance inCampylobacter jejuniandCampylobacter colistrains isolated in 1991 and 2001-2002 from poultry and humans in Berlin Germany. Antimicrob Agents Chemother 47:3825-30.
28. Lücke F.-K. 2000. Utilization of microbes to process and preserve meat. Meat Sci 56:105-15.
29. Mattila T, O'Boyle D, Frost AJ. 1988. Inability to transfer antibiotic resistance inEscherichia colion meat surface. J Food Sci 53:1309-11.
30. Mayrhofer S, Paulsen P, Smulders FJM, Hilbert F. 2004. Antimicrobial resistance profile of five major food-borne pathogens isolated from beef pork and poultry. Int J Food Microbiol 97:23-9.
31. Normanno G, La Salandra G, Dambrosio A, Quaglia NC, Corrente M, Parisi A, Santagada G, Firinu A, Crisetti E Celano GV. 2007. Occurrence characterization and antimicrobial resistance of enterotoxigenicStaphylococcus aureusisolated from meat and dairy products. Int J Food Microbiol 115:290-6.
32. Novotny CP, Lavin K. 1971. Some effects of temperature on the growth of F pili. J Bacteriol 107:671-82.
33. Olofsson TC, Ahrne S, Molin G. 2007. Composition of the bacterial population of refrigerated beef identified with direct 16S rRNA gene analysis and pure culture technique. Int J Food Microbiol 118:233-40.
34. Olsson C, Ahrne S, Pettersson B, Molin G. 2003. The bacterial flora of fresh and chill stored pork: analysis by cloning and sequencing of 16S rRNA genes. Int J Food Microbiol 83:245-52.
35. Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS, Graham DW. 2007. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9:143-51.
36. Pourshaban M, Ferrini AM, Mannoni V, Oliva B, Aureli P. 2002. Transferable tetracycline resistance inListeria monocytogenesfrom food in Italy. J Med Microbiol 51:564-6.
37. Poyart C, Celli J, Trieu-Cuot P. 1995. Conjugative transposition of Tn916-related elements fromEnterococcus faecalistoEscherichia coliandPseudomonas fluorescens. Antimicrob Agents Chemother 39:500-6.
38. Poyart-Salmeron C, Trieu-Cuot P, Carlier C, MacGowan A, McLauchlin J, Courvalin P. 1992. Genetic basis of tetracycline resistance in clinical isolates ofListeria monocytogenes. Antimicrob Agents Chemother 36:463-6.
39. Rizzotti L, La Gioia F, Dellaglio F, Torriani S. 2009. Molecular diversity and transferability of the tetracycline resistance genetet(M) carried on Tn916-1545 family transposons in enterococci from a total food chain. Antonie Van Leeuwenhoek 96:43-52.
40. Roberts MC. 1996. Tetracycline resistance determinants: mechanisms of action regulation of expression genetic mobility and distribution. FEMS MicrobiolRev. 19:1-24.
41. Roberts MC. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 245:195-203.
42. Salyers A, Gupta A, Wang Y. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 12:412-6.
43. Schroeter A, Hoog B, Helmuth R. 2004. Resistance of salmonella isolates in Germany. Zoonoses Public Health 51:389-92.
44. Schwaiger K, Schmied EM, Bauer J. 2008. Comparative analysis of antibiotic resistance characteristics of gram-negative bacteria isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria Germany. Zoonoses Public Health 55:330-41.
45. Schwaiger K, Harms K, Hölzel C, Meyer K, Karl M, Bauer J. 2009. Tetracycline in liquid manure selects for co-occurrence of the resistance genestet(M) andtet(L) inEnterococcus faecalis. Vet Microbiol 139:386-92.
46. Schwaiger K, Hölzel C, Bauer J. 2010a. Resistance gene patterns of tetracycline resistantEscherichia coliof human and porcine origin. Vet Microbiol 142:329-36.
47. Schwaiger K, Schmied EM, Bauer J. 2010b. Comparative analysis on antibiotic resistance characteristics ofListeriaspp andEnterococcusspp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria Germany. Zoonoses Public Health 57:171-80.
48. Simeoni D, Rizzotti L, Cocconcelli P, Gazzola S, Dellaglio F, Torriani S. 2008. Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities. Food Microbiol 25:196-201.
49. Smith MS, Yang RK, Knapp CW, Niu Y, Peak N, Hanfelt MM, Galland JC, Graham DW. 2004. Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR. Appl Environ Microbiol 70:7372-7.
50. Toomey N, Bolton D, Fanning S. 2010. Characterisation and transferability of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res Microbiol 161:127-35.
51. van Netten P, van De Moosdijk A, van Hoensel P, Mossel DA, Perales I. 1990. Psychrotrophic strains ofBacillus cereusproducing enterotoxin. J Appl Microbiol. 69:73-9.
52. Wilcks A, Andersen SR, Licht TR. 2005. Characterization of transferable tetracycline resistance genes inEnterococcus faecalisisolated from raw food. FEMS Microbiol Lett 243:15-9.
53. Wintzingerode F, Göbel U, Stackebrandt E. 1997. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:213-29.
54. Zonenschain D, Rebecchi A, Morelli L. 2009. Erythromycin- and tetracycline-resistant lactobacilli in Italian fermented dry sausages. J Appl Microbiol 107:1559-68.