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BioMed Research International
Volume 2014, Article ID 746859, 10 pages
http://dx.doi.org/10.1155/2014/746859
Research Article

Molecular Identification and Quantification of Tetracycline and Erythromycin Resistance Genes in Spanish and Italian Retail Cheeses

1Departamento de Microbiología y Bioquímica, Instituto de Productos Lácteos de Asturias (IPLA-CSIC), Paseo Río Linares s/n, Villaviciosa, 33300 Asturias, Spain
2Dipartimento di Biotecnologie, Università Degli Studi di Verona, Strada Le Grazie, 15, 37134 Verona, Italy

Received 4 July 2014; Revised 21 August 2014; Accepted 27 August 2014; Published 11 September 2014

Academic Editor: Gundlapally S. Reddy

Copyright © 2014 Ana Belén Flórez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Davies and D. Davies, “Origins and evolution of antibiotic resistance,” Microbiology and Molecular Biology Reviews, vol. 74, no. 3, pp. 417–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. V. M. D'Costa, C. E. King, L. Kalan et al., “Antibiotic resistance is ancient,” Nature, vol. 477, no. 7365, pp. 457–461, 2011. View at Publisher · View at Google Scholar
  3. G. D. Wright, “The antibiotic resistome: the nexus of chemical and genetic diversity,” Nature Reviews Microbiology, vol. 5, no. 3, pp. 175–186, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. S. B. Levy and B. Marshall, “Antibacterial resistance worldwide: causes, challenges and responses,” Nature Medicine, vol. 10, supplement 12, pp. S122–S129, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. A. H. A. M. van Hoek, D. Mevius, B. Guerra, P. Mullany, A. P. Roberts, and H. J. M. Aarts, “Acquired antibiotic resistance genes: an overview,” Frontiers in Microbiology, vol. 2, article 203, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. D. J. Donoghue, “Antibiotic residues in poultry tissues and eggs: human health concerns?” Poultry Science, vol. 82, no. 4, pp. 618–621, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. G. M. Durán and D. L. Marshall, “Ready-to-eat shrimp as an international vehicle of antibiotic-resistant bacteria,” Journal of Food Protection, vol. 68, no. 11, pp. 2395–2401, 2005. View at Google Scholar · View at Scopus
  8. H. H. Wang, M. Manuzon, M. Lehman et al., “Food commensal microbes as a potentially important avenue in transmitting antibiotic resistance genes,” FEMS Microbiology Letters, vol. 254, no. 2, pp. 226–231, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. X. Li and H. H. Wang, “Tetracycline resistance associated with commensal bacteria from representative ready-to-consume deli and restaurant foods,” Journal of Food Protection, vol. 73, no. 10, pp. 1841–1848, 2010. View at Google Scholar · View at Scopus
  10. V. Perreten, F. Schwarz, L. Cresta, M. Boeglin, G. Dasen, and M. Teuber, “Antibiotic resistance spread in food,” Nature, vol. 389, no. 6653, pp. 801–802, 1997. View at Google Scholar · View at Scopus
  11. K. P. Scott, C. M. Melville, T. M. Barbosa, and H. J. Flint, “Occurrence of the new tetracycline resistance gene tet (W) in bacteria from the human gut,” Antimicrobial Agents and Chemotherapy, vol. 44, no. 3, pp. 775–777, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. M. S. Ammor, A. B. Flórez, A. H. A. M. van Hoek et al., “Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria,” Journal of Molecular Microbiology and Biotechnology, vol. 14, pp. 6–15, 2008. View at Publisher · View at Google Scholar
  13. M. S. Smith, R. K. Yang, C. W. Knapp et al., “Quantification of tetracycline resistance genes in feedlot lagoons by real-time PCR,” Applied and Environmental Microbiology, vol. 70, no. 12, pp. 7372–7377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Y. Manuzon, S. E. Hanna, H. Luo, Z. Yu, W. J. Harper, and H. H. Wang, “Quantitative assessment of the tetracycline resistance gene pool in cheese samples by real-time TaqMan PCR,” Applied and Environmental Microbiology, vol. 73, no. 5, pp. 1676–1677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. R. I. Aminov, N. Garrigues-Jeanjean, and R. I. Mackie, “Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins,” Applied and Environmental Microbiology, vol. 67, no. 1, pp. 22–32, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. J. C. Chee-Sanford, R. I. Aminov, I. J. Krapac, N. Garrigues-Jeanjean, and R. I. Mackie, “Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities,” Applied and Environmental Microbiology, vol. 67, no. 4, pp. 1494–1502, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Yu, F. C. Michel Jr., G. Hansen, T. Wittum, and M. Morrison, “Development and application of real-time PCR assays for quantification of genes encoding tetracycline resistance,” Applied and Environmental Microbiology, vol. 71, no. 11, pp. 6926–6933, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. M. L. Diaz-Torres, R. McNab, D. A. Spratt et al., “Novel tetracycline resistance determinant from the oral metagenome,” Antimicrobial Agents and Chemotherapy, vol. 47, no. 4, pp. 1430–1432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. L. A. Seville, A. J. Patterson, K. P. Scott et al., “Distribution of tetracycline and erythromycin resistance genes among human oral and fecal metagenomic DNA,” Microbial Drug Resistance, vol. 15, no. 3, pp. 159–166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. M. O. A. Sommer, G. Dantas, and G. M. Church, “Functional characterization of the antibiotic resistance reservoir in the human microflora,” Science, vol. 325, no. 5944, pp. 1128–1131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. A. J. Patterson, R. Colangeli, P. Spigaglia, and K. P. Scott, “Distribution of specific tetracycline and erythromycin resistance genes in environmental samples assessed by macroarray detection,” Environmental Microbiology, vol. 9, no. 3, pp. 703–715, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Delgado, F. Fracchetti, B. Mayo, and S. Torriani, “Development and validation of a multiplex PCR-based DNA microarray hybridisation method for detecting bacterial antibiotic resistance genes in cheese,” International Dairy Journal, vol. 21, no. 3, pp. 149–157, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. K. J. Forsberg, A. Reyes, B. Wang, E. M. Selleck, M. O. A. Sommer, and G. Dantas, “The shared antibiotic resistome of soil bacteria and human pathogens,” Science, vol. 337, no. 6098, pp. 1107–1111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Mullany, E. Allan, and P. J. Warburton, “Tetracycline resistance genes and mobile genetic elements from the oral metagenome,” Clinical Microbiology and Infection, vol. 18, no. 4, pp. 58–61, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. T. M. Barbosa, K. P. Scott, and H. J. Flint, “Evidence for recent intergeneric transfer of a new tetracycline resistance gene, tet(W), isolated from Butyrivibrio fibrisolvens, and the occurrence of tet(O) in ruminai bacteria,” Environmental Microbiology, vol. 1, no. 1, pp. 53–64, 1999. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Gevers, G. Huys, and J. Swings, “In vitro conjugal transfer of tetracycline resistance from Lactobacillus isolates to other gram-positive bacteria,” FEMS Microbiology Letters, vol. 225, no. 1, pp. 125–130, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. M. C. Roberts, W. O. Chung, D. Roe et al., “Erythromycin-resistant Neisseria gonorrhoeae and oral commensal Neisseria spp. carry known rRNA methylase genes,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 6, pp. 1367–1372, 1999. View at Google Scholar · View at Scopus
  28. S. E. Denman and C. S. McSweeney, “Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen,” FEMS Microbiology Ecology, vol. 58, no. 3, pp. 572–582, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. A. B. Flórez, S. Delgado, and B. Mayo, “Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment,” Canadian Journal of Microbiology, vol. 51, no. 1, pp. 51–58, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. A. B. Flórez and B. Mayo, “Microbial diversity and succession during the manufacture and ripening of traditional, Spanish, blue-veined Cabrales cheese, as determined by PCR-DGGE,” International Journal of Food Microbiology, vol. 110, no. 2, pp. 165–171, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. A. B. Flórez, M. S. Ammor, P. Álvarez-Martín, A. Margolles, and B. Mayo, “Molecular analysis of tet(W) gene-mediated tetracycline resistance in dominant intestinal Bifidobacterium species from healthy humans,” Applied and Environmental Microbiology, vol. 72, no. 11, pp. 7377–7379, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. A. Salyers, A. Gupta, and Y. Wang, “Human intestinal bacteria as reservoirs for antibiotic resistance genes,” Trends in Microbiology, vol. 12, no. 9, pp. 412–416, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Devirgiliis, A. Caravelli, D. Coppola, S. Barile, and G. Perozzi, “Antibiotic resistance and microbial composition along the manufacturing process of Mozzarella di Bufala Campana,” International Journal of Food Microbiology, vol. 128, no. 2, pp. 378–384, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. C. L. Cain, “Antimicrobial resistance in staphylococci in small animals,” Veterinary Clinics of North America: Small Animal Practice, vol. 43, no. 1, pp. 19–40, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Zhao, H. Sun, H. Wang et al., “Antimicrobial resistance trends among 5608 clinical Gram-positive isolates in China: results from the Gram-Positive Cocci Resistance Surveillance program (2005–2010),” Diagnostic Microbiology and Infectious Disease, vol. 73, no. 2, pp. 174–181, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. L. L. McGowan-Spicer, P. J. Fedorka-Cray, J. G. Frye, R. J. Meinersmann, J. B. Barrett, and C. R. Jackson, “Antimicrobial resistance and virulence of Enterococcus faecalis isolated from retail food,” Journal of Food Protection, vol. 71, no. 4, pp. 760–769, 2008. View at Google Scholar · View at Scopus
  37. X. Li, Y. Li, V. Alvarez, W. J. Harper, and H. H. Wang, “Effective antibiotic resistance mitigation during cheese fermentation,” Applied and Environmental Microbiology, vol. 77, no. 20, pp. 7171–7175, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. H. H. Wang and D. W. Schaffner, “Antibiotic resistance: how much do we know and where do we go from here?” Applied and Environmental Microbiology, vol. 77, no. 20, pp. 7093–7095, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Chen, Z. Yu, F. C. Michel Jr., T. Wittum, and M. Morrison, “Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems,” Applied and Environmental Microbiology, vol. 73, no. 14, pp. 4407–4416, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. S.-M. Kim, H. C. Kim, and S.-W. S. Lee, “Characterization of antibiotic resistance determinants in oral biofilms,” Journal of Microbiology, vol. 49, no. 4, pp. 595–602, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Zhang, D. Kinkelaar, Y. Huang, Y. Li, X. Li, and H. H. Wang, “Acquired antibiotic resistance: are we born with it?” Applied and Environmental Microbiology, vol. 77, no. 20, pp. 7134–7141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Guarddon, J. M. Miranda, J. A. Rodríguez, B. I. Vázquez, A. Cepeda, and C. M. Franco, “Real-time polymerase chain reaction for the quantitative detection of tetA and tetB bacterial tetracycline resistance genes in food,” International Journal of Food Microbiology, vol. 146, no. 3, pp. 284–289, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Feld, S. Schjørring, K. Hammer et al., “Selective pressure affects transfer and establishment of a Lactobacillus plantarum resistance plasmid in the gastrointestinal environment,” Journal of Antimicrobial Chemotherapy, vol. 61, no. 4, pp. 845–852, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Jacobsen, A. Wilcks, K. Hammer, G. Huys, D. Gevers, and S. R. Andersen, “Horizontal transfer of tet(M) and erm(B) resistance plasmids from food strains of Lactobacillus plantarum to Enterococcus faecalis JH2-2 in the gastrointestinal tract of gnotobiotic rats,” FEMS Microbiology and Ecology, vol. 59, no. 1, pp. 158–166, 2007. View at Publisher · View at Google Scholar · View at Scopus