Lettuce for human consumption collected in Costa Rica contains complex communities of culturable oxytetracycline- and gentamicin-resistant bacteria

Applied and Environmental Microbiology

Volumn 72, Issue 9, 2006, Pages 5870-5876

  Rodríguez, César ^a   Lang, Lore ^b   Wang, Amy ^b   Altendorf, Karlheinz ^a   García, Fernando ^b   Lipski, André ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL CULTURE; GENES; MEDICINE;

ANTIMICROBIAL-RESISTANT BACTERIA; MICROBIAL BIOTA; MOLECULAR FINGERPRINTING METHODS; RESISTANCE GENES;

PLANTS (BOTANY);

ANTIBIOTIC AGENT; GENTAMICIN; OXYTETRACYCLINE; STREPTOMYCIN;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOSPHERE; CROP PLANT; GENE; MEDICINE; MICROBIAL COMMUNITY; ORGANIC FARMING;

ALPHAPROTEOBACTERIA; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL TRANSMISSION; BACTERIUM CULTURE; BIOSPHERE; BURKHOLDERIA; CHEMOTAXONOMY; CHRYSEOBACTERIUM; CONTROLLED STUDY; COSTA RICA; CROP PRODUCTION; CUT FLOWER; DNA FINGERPRINTING; ENRICHMENT CULTURE; ENTEROBACTERIACEAE; FLAVOBACTERIA; FOOD CONTAMINATION; FOOD QUALITY; FOOD SAFETY; GENE TRANSFER; HORIZONTAL GENE TRANSFER; LETTUCE; NONHUMAN; POLYMERASE CHAIN REACTION; PREVOTELLA; RALSTONIA; SPHINGOMONAS; STENOTROPHOMONAS; XANTHOMONAS;

AGRICULTURE; BACTERIA; COSTA RICA; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; FECES; FOOD MICROBIOLOGY; GENES, BACTERIAL; GENTAMICINS; HUMANS; LETTUCE; OXYTETRACYCLINE; PLASMIDS; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; TETRACYCLINE RESISTANCE; WATER MICROBIOLOGY;

CENTRAL AMERICA; COSTA RICA;

LACTUCA;

EID: 33748800232     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00963-06     Document Type: Article

References (40)

1. Aendekerk, S., S. P. Diggle, Z. Song, N. Hoiby, P. Corneli, P. Williams, and M. Camara. 2005. The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151:1113-1125.
2. Aminov, R. I., N. Garrigues-Jeanjean, and R. I. Mackie. 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.
3. Blumenthal, U. J., D. D. Mara, A. Peasey, G. Ruíz-Palacios, and R. Stott. 2000. Guidelines for the microbiological quality of treated wastewater used in agriculture: recommendations for revising WHO guidelines. Bull. W. H. O. 78:1104-1116.
4. Boehme, S., G. Werner, I. Klare, R. Reissbrodt, and W. Witte. 2004. Occurrence of antibiotic-resistant enterobacteria in agricultural foodstuffs. Mol. Nutr. Food Res. 48:522-531.
5. Dunbar, J., L. O. Ticknor, and C. R. Kuske. 2000. Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl. Environ. Microbiol. 66:2943-2950.
6. Götz, A., R. Pukall, E. Smit, E. Tietze, R. Prager, H. Tschäpe, J. D. van Elsas, and K. Smalla. 1996. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl. Environ. Microbiol. 62:2621-2628.
7. Halling-Sørensen, B., G. Sengeløv, and J. Tørnelund. 2002. Toxicity of tetracyclines and tetracycline degradation products to environmentally relevant bacteria, including selected tetracycline-resistant bacteria. Arch. Environ. Contam. Toxicol. 42(3):263-271.
8. Hammer, Ø., D. Harper, and P. Ryan. 2001. PAST: paleontological statistics software package for education and data analysis. Paleontol. Electron. 4:9.
9. Heuer, H., E. Krogerrecklenfort, S. Egan, L. van Overbeek, G. Guillaume, T. L. Nikolakopoulou, E. M. H. Wellington, J. D. van Elsas, J.-M. Collard, A. D. Karagouni, and K. Smalla. 2002. Gentamicin resistance genes in environmental bacteria: prevalence and transfer. FEMS Microbiol. Ecol. 42:289-302.
10. Hogan, D., and R. Kolter. 2002. Why are bacteria refractory to antimicrobials? Curr. Opin. Microbiol. 5:472-477.
11. Honnorat-Benabbou, V. C., A. A. Lebugle, B. Sallek, and D. Duffaut-Lagarrigue. 2001. Stability study of tetracyclines with respect to their use in slow release systems. J Mater. Sci. Mater. Med. 12(2):107-110.
12. IUPAC-IUB Joint Commission on Biochemical Nomenclature. 1977. The nomenclature of lipids (recommendations 1976). Eur. J. Biochem. 79:11-21.
13. Johannessen, G. S., R. B. Frøseth, L. Solemdal, J. Jarp, Y. Wasteson, and M. L. Rørvik. 2004. Influence of bovine manure as fertilizer on the bacteriological quality of organic iceberg lettuce. J. Appl. Microbiol. 96:787-794.
14. Kent, A. D., D. J. Smith, B. J. Benson, and E. W. Triplett. 2003. Web-based phylogenetic assignment tool for analysis of terminal restriction fragment length polymorphism profiles of microbial communities. Appl. Environ. Microbiol. 69:6768-6776.
15. Lester, C. H., N. Frimodt-Moller, and A. M. Hammerum. 2004. Conjugal transfer of aminoglycoside and macrolide resistance between Enterococcus faecium isolates in the intestine of streptomycin-treated mice. FEMS Microbiol. Lett. 235:385-391.
16. Lester, C. H., N. Frimodt-Møller, T. L. Sørensen, D. L. Monnet, and A. M. Hammerum. 2006. In vivo transfer of the vanA resistance gene from an Enterococcus faecium isolate of animal origin to an E. faecium isolate of human origin in the intestines of human volunteers. Antimicrob. Agents Chemother. 50:596-599.
17. Lindow, S. E., and M. T. Brandl. 2003. Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69:1875-1883.
18. Lipski, A., and K. Altendorf. 1997. Identification of heterotrophic bacteria isolated from ammonia-supplied experimental biofilters. Syst. Appl. Microbiol. 20:448-457.
19. Liu, W. T., T. L. Marsh, H. Cheng, and L. J. Forney. 1997. Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl. Environ. Microbiol. 63:4516-4522.
20. Magnuson, J. A., A. D. King, and T. Torok. 1990. Microflora of partially processed lettuce. Appl. Environ. Microbiol. 56:3851-3854.
21. McManus, P. S., V. O. Stockwell, G. W. Sundin, and A. L. Jones. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-465.
22. Michel, C., O. Matte-Tailliez, B. Kerouault, and J. F. Bernardet. 2005. Resistance pattern and assessment of phenicol agents' minimum inhibitory concentration in multiple drug resistant Chryseobacterium isolates from fish and aquatic habitats. J. Appl. Microbiol. 99:323-332.
23. Miranda, C. D., C. Kehrenberg, C. Ulep, S. Schwarz, and M. C. Roberts. 2003. Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrob. Agents Chemother. 47:883-888.
24. Mora, D. 1998. Actualización de criterios microbiológicos para evaluar las aguas en sus diferentes usos. Revista Costarricense Salud Pública 7(15):15-24.
25. Nwosu, V. C. 2001. Antibiotic resistance with particular reference to soil microorganisms. Res. Microbiol. 152:421-430.
26. Österblad, M., O. Pensala, M. Peterzens, H. Heleniusc, and P. Huovinen. 1999. Antimicrobial susceptibility of Enterobacteriaceae isolated from vegetables. J. Antimicrob. Chemother. 43:503-509.
27. Petersen, A., J. S. Andersen, T. Kaewmak, T. Somsiri, and A. Dalsgaard. 2002. Impact of integrated fish farming on antimicrobial resistance in a pond environment. Appl. Environ. Microbiol. 68:6036-6042.
28. Poole, K. 2004. Efflux-mediated multiresistance in gram-negative bacteria. Clin. Microbiol. Infect. 10:12-26.
29. Riesenfeld, C. S., R. M. Goodman, and J. Handelsman. 2004. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ. Microbiol. 6:981-989.
30. Roberts, M. C. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiol. Lett. 245:195-203.
31. Rudi, K., S. L. Flateland, J. F. Hanssen, G. Bengtsson, and H. Nissen. 2002. Development and evaluation of a 16S ribosomal DNA array-based approach for describing complex microbial communities in ready-to-eat vegetable salads packed in a modified atmosphere. Appl. Environ. Microbiol. 68:1146-1156.
32. Schnabel, E. L., and A. L. Jones. 1999. Distribution of tetracycline resistance genes and transposons among phylloplane bacteria in Michigan apple orchards. Appl. Environ. Microbiol. 65:4898-4907.
33. Schutter, M. E., and R. P. Dick. 2000. Comparison of fatty acid methyl ester (FAME) methods for characterizing microbial communities. Soil Sci. Soc. Am. J. 64:1659-1666.
34. Schwarz, S., C. Kehrenberg, and T. R. Walsh. 2001. Use of antimicrobial agents in veterinary medicine and food animal production. Int. J. Antimicrob. Agents 17:431-437.
35. Shaw, K. J., P. N. Rather, R. S. Hare, and G. H. Miller. 1993. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57:138-163.
36. Sorum, H., and T. M. L'Abee-Lund. 2002. Antibiotic resistance in food-related bacteria-a result of interfering with the global web of bacterial genetics. Int. J. Food Microbiol. 78:43-56.
37. Tenover, F. C. 2001. Development and spread of bacterial resistance to antimicrobial agents: an overview. Clin. Infect. Dis. 33:S108-S115.
38. Threlfall, E. J., L. R. Ward, J. A. Frost, and G. A. Willshaw. 2000. The emergence and spread of antibiotic resistance in food-borne bacteria. Int. J. Food Microbiol. 62:1-5.
39. Vakulenko, S. B., and S. Mobashery. 2003. Versatility of aminoglycosides and prospects for their future. Clin. Microbiol. Rev. 16:430-450.
40. Vidaver, A. K. 2002. Uses of antimicrobials in plant agriculture. Clin. Infect. Dis. 34:S107-S110.