Evidence for a second genomic island conferring multidrug resistance in a clonal group of strains of Salmonella enterica serovar typhimurium and its monophasic variant circulating in Italy, Denmark, and the United Kingdom

Journal of Clinical Microbiology

Volumn 48, Issue 6, 2010, Pages 2103-2109

  Lucarelli, Claudia ^a   Dionisi, Anna Maria ^a   Torpdahl, Mia ^b   Villa, Laura ^a   Graziani, Caterina ^a   Hopkins, Katie ^c   Threlfall, John ^c   Caprioli, Alfredo ^a   Luzzi, Ida ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b STATENS SERUM INSTITUT   (Denmark)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CHROMOSOMAL LOCALIZATION; CLONAL SPECIES; CONTROLLED STUDY; DENMARK; GENE IDENTIFICATION; GENETIC VARIABILITY; GENOMIC ISLAND; ITALY; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SEROTYPE; UNITED KINGDOM;

ANTI-BACTERIAL AGENTS; BACTERIAL TYPING TECHNIQUES; CLUSTER ANALYSIS; DENMARK; DNA FINGERPRINTING; DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; GENES, BACTERIAL; GENOMIC ISLANDS; GENOTYPE; GREAT BRITAIN; HUMANS; ITALY; MOLECULAR EPIDEMIOLOGY; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM;

EID: 77952896056     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.01371-09     Document Type: Article

References (44)

1. Arlet, G., M. Rouveau, and A. Philippon. 1997. Substitution of alanine for aspartate at position 179 in the SHV-6 extended-spectrum beta-lactamase. FEMS Microbiol. Lett. 152:163-167.
2. Baggesen, D. L., D. Sandvang, and F. M. Aarestrup. 2000. Characterization of Salmonella enterica serovar Typhimurium DT104 isolated from Denmark and comparison with isolates from Europe and the United States. J. Clin. Microbiol. 38:1581-1586.
3. Best, E. L., M. D. Hampton, S. Ethelberg, E. Liebana, F. A. Clifton-Hadley, and E. J. Threlfall. 2009. Drug-resistant Salmonella Typhimurium DT 120: use of PFGE and MLVA in a putative international outbreak investigation. Microb. Drug Resist. 15:133-138.
4. Briggs, C. E., and P. M. Fratamico. 1999. Molecular characterization of an antibiotic resistance gene cluster of Salmonella typhimurium DT104. Antimicrob. Agents Chemother. 43:846-849.
5. Busani, L., C. Graziani, A. Battisti, A. Franco, A. Ricci, D. Vio, E. Digiannatale, F. Paterlini, M. D'Incau, S. Owczarek, A. Caprioli, and I. Luzzi. 2004. Antibiotic resistance in Salmonella enterica serotypes Typhimurium, Enteritidis and Infantis from human infections, foodstuffs and farm animals in Italy. Epidemiol. Infect. 132:245-251.
6. Carattoli, A., E. Filetici, L. Villa, A. M. Dionisi, A. Ricci, and I. Luzzi. 2002. Antibiotic resistance genes and Salmonella genomic island 1 in Salmonella enterica serovar Typhimurium isolated in Italy. Antimicrob. Agents Chemother. 46:2821-2828.
7. Casin, I., J. Breuil, A. Brisabois, F. Moury, F. Grimont, and E. Collatz. 1999. Multidrug-resistant human and animal Salmonella typhimurium isolates in France belong predominantly to a DT104 clone with the chromosome- and integron-encoded beta-lactamase PSE-1. J. Infect. Dis. 179:1173-1182.
8. Chen, C. Y., G. W. Nace, B. Solow, and P. Fratamico. 2007. Complete nucleotide sequences of 84.5- and 3.2-kb plasmids in the multi-antibiotic resistant Salmonella enterica serovar Typhimurium U302 strain G8430. Plasmid 57:29-43.
9. Clinical and Laboratory Standards Institute. 2006. Institute performance standards for antimicrobial susceptibility testing; 26th informational supplement. CLSI/NCCLS document M100-S16. Clinical and Laboratory Standards Institute, Wayne, PA.
10. CLSI/NCCLS. 2002. Institute performance standards for antimicrobial performance standard for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, approved standard. CLSI/NCCLS document M31-A2. CLSI/NCCLS, Wayne, PA.
11. Coque, T. M., A. Oliver, J. C. Perez-Diaz, F. Baquero, and R. Canton. 2002. Genes encoding TEM-4, SHV-2, and CTX-M-10 extended-spectrum beta-lactamases are carried by multiple Klebsiella pneumoniae clones in a single hospital (Madrid, 1989 to 2000). Antimicrob. Agents Chemother. 46:500-510.
12. Daly, M., L. Villa, C. Pezzella, S. Fanning, and A. Carattoli. 2005. Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. J. Antimicrob. Chemother. 55:558-561.
13. Dionisi, A. M., C. Graziani, C. Lucarelli, E. Filetici, L. Villa, S. Owczarek, A. Caprioli, and I. Luzzi. 2009. Molecular characterization of multidrug-resistant strains of Salmonella enterica serotype Typhimurium and monophasic variant (S. 4,[5],12:i:-) isolated from human infections in Italy. Foodborne Pathog. Dis. 6:711-717.
14. Echeita, M. A., S. Herrera, J. Garaizar, and M. A. Usera. 2002. Multiplex PCR-based detection and identification of the most common Salmonella second-phase flagellar antigens. Res. Microbiol. 153:107-113.
15. Emborg, H. D., D. L. Baggesen, and F. M. Aarestrup. 2008. Ten years of antimicrobial susceptibility testing of Salmonella from Danish pig farms. J. Antimicrob. Chemother. 62:360-363.
16. Ethelberg, S., M. Lisby, M. Torpdahl, G. Sorensen, J. Neimann, P. Rasmussen, S. Bang, U. Stamer, H. B. Hansson, K. Nygard, D. L. Baggesen, E. M. Nielsen, K. Molbak, and M. Helms. 2004. Prolonged restaurant-associated outbreak of multidrug-resistant Salmonella Typhimurium among patients from several European countries. Clin. Microbiol. Infect. 10:904-910.
17. Frech, G., and S. Schwarz. 2000. Molecular analysis of tetracycline resistance in Salmonella enterica subsp. enterica serovars Typhimurium, Enteritidis, Dublin, Choleraesuis, Hadar and Saintpaul: construction and application of specific gene probes. J. Appl. Microbiol. 89:633-641.
18. Frost, J. A. 1994. Testing for resistance to antibacterial drugs, p. 73-82. In H. Chart (ed.), Methods in Practical Laboratory Bacteriology. CRC Press, New York, NY.
19. Gebreyes, W. A., and C. Altier. 2002. Molecular characterization of multidrug-resistant Salmonella enterica subsp. enterica serovar Typhimurium isolates from swine. J. Clin. Microbiol. 40:2813-2822.
20. Graziani, C., L. Busani, A. M. Dionisi, C. Lucarelli, S. Owczarek, A. Ricci, M. Mancin, A. Caprioli, and I. Luzzi. 2008. Antimicrobial resistance in Salmonella enterica serovar Typhimurium from human and animal sources in Italy. Vet. Microbiol. 128:414-418.
21. Guerra, B., I. Laconcha, S. M. Soto, M. A. Gonzalez-Hevia, and M. C. Mendoza. 2000. Molecular characterisation of emergent multiresistant Salmonella enterica serotype [4,5,12:i:-] organisms causing human salmonellosis. FEMS Microbiol. Lett. 190:341-347.
22. Guerra, B., S. M. Soto, J. M. Arguelles, and M. C. Mendoza. 2001. Multidrug resistance is mediated by large plasmids carrying a class 1 integron in the emergent Salmonella enterica serotype [4,5,12:i:-]. Antimicrob. Agents Chemother. 45:1305-1308.
23. Guerra, B., E. Junker, A. Miko, R. Helmuth, and M. C. Mendoza. 2004. Characterization and localization of drug resistance determinants in multidrug-resistant, integron-carrying Salmonella enterica serotype Typhimurium strains. Microb. Drug Resist. 10:83-91.
24. Havlickova, H., H. Hradecka, I. Bernardyova, and I. Rychlik. 2009. Distribution of integrons and SGI1 among antibiotic-resistant Salmonella enterica isolates of animal origin. Vet. Microbiol. 133:193-198.
25. Heir, E., B. A. Lindstedt, I. Nygard, T. Vardund, V. Hasseltvedt, and G. Kapperud. 2002. Molecular epidemiology of Salmonella typhimurium isolates from human sporadic and outbreak cases. Epidemiol. Infect. 128:373-382.
26. Liu, S. L., A. Hessel, and K. E. Sanderson. 1993. Genomic mapping with I-Ceu I, an intron-encoded endonuclease specific for genes for ribosomal RNA, in Salmonella spp., Escherichia coli, and other bacteria. Proc. Natl. Acad. Sci. U. S. A. 90:6874-6878.
27. Lukinmaa, S., U. M. Nakari, A. Liimatainen, and A. Siitonen. 2006. Genomic diversity within phage types of Salmonella enterica ssp. enterica serotypes Enteritidis and Typhimurium. Foodborne Pathog. Dis. 3:97-105.
28. Maimone, F., B. Colonna, P. Bazzicalupo, B. Oliva, M. Nicoletti, and M. Casalino. 1979. Plasmids and transposable elements in Salmonella wien. J. Bacteriol. 139:369-375. (Pubitemid 9225566)
29. Meakins, S., I. S. Fisher, C. Berghold, P. Gerner-Smidt, H. Tschape, M. Cormican, I. Luzzi, F. Schneider, W. Wannett, J. Coia, A. Echeita, and E. J. Threlfall. 2008. Antimicrobial drug resistance in human nontyphoidal Salmonella isolates in Europe 2000-2004: a report from the Enter-net International Surveillance Network. Microb. Drug Resist. 14:31-35.
30. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. L. Mungall, S. D. Bentley, M. T. Holden, M. Sebaihia, S. Baker, D. Basham, K. Brooks, T. Chillingworth, P. Connerton, A. Cronin, P. Davis, R. M. Davies, L. Dowd, N. White, J. Farrar, T. Feltwell, N. Hamlin, A. Haque, T. T. Hien, S. Holroyd, K. Jagels, A. Krogh, T. S. Larsen, S. Leather, S. Moule, P. O'Gaora, C. Parry, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848-852.
31. Pasquali, F., A. De Cesare, A. Ricci, C. Kehrenberg, S. Schwarz, and G. Manfreda. 2004. Phage types, ribotypes and tetracycline resistance genes of Salmonella enterica subsp. enterica serovar Typhimurium strains isolated from different origins in Italy. Vet. Microbiol. 103:71-76.
32. Peters, T. M., C. Maguire, E. J. Threlfall, I. S. Fisher, N. Gill, and A. J. Gatto. 2003. The Salm-gene project - a European collaboration for DNA fingerprinting for food-related salmonellosis. Euro Surveill. 8:46-50.
33. Poppe, C., K. Ziebell, L. Martin, and K. Allen. 2002. Diversity in antimicrobial resistance and other characteristics among Salmonella typhimurium DT104 isolates. Microb. Drug Resist. 8:107-122.
34. Rabatsky-Ehr, T., J. Whichard, S. Rossiter, B. Holland, K. Stamey, M. Headrick, T. Barrett, F. Angulo, and the NARMS Working Group. 2004. Multidrug-resistant strains of Salmonella enterica Typhimurium, United States, 1997-1998. Emerg. Infect. Dis. 10:795-801.
35. Randall, L. P., S. W. Cooles, M. K. Osborn, L. J. Piddock, and M. J. Woodward. 2004. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J. Antimicrob. Chemother. 53:208-216.
36. Sambrook, J. E., and D. W. Russel. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Soler, P., R. Gonzalez-Sanz, M. J. Bleda, G. Hernandez, A. Echeita, and M. A. Usera. 2006. Antimicrobial resistance in non-typhoidal Salmonella from human sources, Spain, 2001-2003. J. Antimicrob. Chemother. 58:310-314. (Pubitemid 44294940)
38. Southern, E. M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
39. Threlfall, E. J., B. Rowe, and L. R. Ward. 1993. A comparison of multiple drug resistance in salmonellas from humans and food animals in England and Wales, 1981 and 1990. Epidemiol. Infect. 111:189-197.
40. Threlfall, E. J., L. R. Ward, J. A. Skinner, and A. Graham. 2000. Antimicrobial drug resistance in non-typhoidal salmonellas from humans in England and Wales in 1999: decrease in multiple resistance in Salmonella enterica serotypes Typhimurium, Virchow, and Hadar. Microb. Drug Resist. 6:319-325.
41. Threlfall, E. J. 2002. Antimicrobial drug resistance in Salmonella: problems and perspectives in food- and water-borne infections. FEMS Microbiol. Rev. 26:141-148.
42. Threlfall, E. J., I. S. Fisher, C. Berghold, P. Gerner-Smidt, H. Tschape, M. Cormican, I. Luzzi, F. Schnieder, W. Wannet, J. Machado, and G. Edwards. 2003. Antimicrobial drug resistance in isolates of Salmonella enterica from cases of salmonellosis in humans in Europe in 2000: results of international multi-centre surveillance. Euro Surveill. 8:41-45.
43. Weill, F. X., F. Guesnier, V. Guibert, M. Timinouni, M. Demartin, L. Polomack, and P. A. Grimont. 2006. Multidrug resistance in Salmonella enterica serotype Typhimurium from humans in France (1993 to 2003). J. Clin. Microbiol. 44:700-708.
44. Ziemer, C. J., and S. R. Steadham. 2003. Evaluation of the specificity of Salmonella PCR primers using various intestinal bacterial species. Lett. Appl. Microbiol. 37:463-469.