Comparison of multilocus sequence typing, pulsed-field gel electrophoresis, and antimicrobial susceptibility typing for characterization of Salmonella enterica serotype Newport isolates

Journal of Clinical Microbiology

Volumn 44, Issue 7, 2006, Pages 2449-2457

  Harbottle, H ^a,b   White, D G ^a   McDermott, P F ^a   Walker, R D ^a   Zhao, S ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; ANTIBIOTIC AGENT; CEFALOTIN; CEFOXITIN; CEFTIOFUR; CEFTRIAXONE; CHLORAMPHENICOL; CIPROFLOXACIN; COTRIMOXAZOLE; GENOMIC DNA; GENTAMICIN; KANAMYCIN; NALIDIXIC ACID; STREPTOMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE;

ANTIBIOTIC SENSITIVITY; AROC GENE; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; DNAN GENE; HEMD GENE; HISD GENE; INTERMETHOD COMPARISON; MEAT; MINIMUM INHIBITORY CONCENTRATION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; PURE GENE; SALMONELLA ENTERICA; SEROTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; SUCA GENE; THRA GENE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL TYPING TECHNIQUES; CATTLE; CHICKENS; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA FINGERPRINTING; DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FOOD MICROBIOLOGY; GENES, BACTERIAL; HUMANS; MEAT PRODUCTS; MICROBIAL SENSITIVITY TESTS; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL; SEQUENCE ANALYSIS, DNA; SEROTYPING; SWINE; TURKEYS;

ANIMALIA; BOS TAURUS; SALMONELLA; SALMONELLA ENTERICA; SUS SCROFA;

EID: 33746255244     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.00019-06     Document Type: Article

References (59)

1. Aanensen, D. M., and B. G. Spratt. 2005. The multilocus sequence typing network: mlst.net. Nucleic Acids Res. 33:W728-W733.
2. Alcaine, S. D., S. S. Sukhnanand, L. D. Warnick, W. L. Su, P. McGann, P. McDonough, and M. Wiedmann. 2005. Ceftiofur-resistant Salmonella strains isolated from dairy farms represent multiple widely distributed subtypes that evolved by independent horizontal gene transfer. Antimicrob. Agents Chemother. 49:4061-4067.
3. Berge, A. C., J. M. Adaska, and W. M. Sischo. 2004. Use of antibiotic susceptibility patterns and pulsed-field gel electrophoresis to compare historic and contemporary isolates of multi-drug-resistant Salmonella enterica subsp. enterica serovar Newport. Appl. Environ. Microbiol. 70:318-323.
4. Botteldoorn, N., L. Herman, N. Rijpens, and M. Heyndrickx. 2004. Phenotypic and molecular typing of Salmonella strains reveals different contamination sources in two commercial pig slaughterhouses. Appl. Environ. Microbiol. 70:5305-5314.
5. Centers for Disease Control and Prevention. 2003. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food-selected sites, United States. Morb. Mortal. Wkly. Rep. 53:338-343.
6. Centers for Disease Control and Prevention. 2005. National antimicrobial resistance monitoring system: enteric bacteria. 2000 annual report. [Online.] http://www.cdc.gov/narms/annual/2000/narms_2000_annual_a.htm.
7. Cimons, M. 2000. Rapid food-borne pathogen ID system is making a difference. ASM News 66:617-619.
8. Cooper, J. E., and E. J. Feil. 2004. Multilocus sequence typing-what is resolved? Trends Microbiol. 12:373-377.
9. Demczuk, W., G. Soule, C. Clark, H. W. Ackermann, R. Easy, R. Khakhria, F. Rodgers, and R. Ahmed. 2003. Phage-based typing scheme for Salmonella enterica serovar Heidelberg, a causative agent of food poisonings in Canada. J. Clin. Microbiol. 41:4279-4284.
10. Dingle, K. E., F. M. Colles, D. Falush, and M. C. Maiden. 2005. Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni. J. Clin. Microbiol. 43:340-347.
11. Dunman, P. M., W. Mounts, F. McAleese, F. Immermann, D. Macapagal, E. Marsilio, L. McDougal, F. C. Tenover, P. A. Bradford, P. J. Petersen, S. J. Projan, and E. Murphy. 2004. Uses of Staphylococcus aureus GeneChips in genotyping and genetic composition analysis. J. Clin. Microbiol. 42:4275-4283.
12. Enright, M. C., N. P. Day, C. E. Davies, S. J. Peacock, and B. G. Spratt. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38:1008-1015.
13. Ethelberg, S., M. Lisby, M. Torpdahl, G. Sorensen, J. Neimann, P. Rasmussen, S. M. Bang, U. Stamer, H. B. Hansson, K. Nygard, D. L. Baggesen, E. M. Nielsen, K. Molbak, and M. Helms. 2005. Prolonged restaurant-associated outbreak of multidrug resistant Salmonella typhimurium-secondary publication. Ugeskr. Laeger. 167:764-766.
14. Fakhr, M. K., L. K. Nolan, and C. M. Logue. 2005. Multilocus sequence typing lacks the discriminatory ability of pulsed-field gel electrophoresis for typing Salmonella enterica serovar Typhimurium. J. Clin. Microbiol. 43:2215-2219.
15. Feil, E. J., B. C. Li, D. M. Aanensen, W. P. Hanage, and B. G. Spratt. 2004. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J. Bacteriol. 186:1518-1530.
16. Foley, S. L., S. Simjee, J. Meng, D. G. White, P. F. McDermott, and S. Zhao. 2004. Evaluation of molecular typing methods for Escherichia coli O157:H7 isolates from cattle, food, and humans. J. Food Prot. 67:651-657.
17. Fontana, J., A. Stout, B. Bolstorff, and R. Timperi. 2003. Automated ribotyping and pulsed-field gel electrophoresis for rapid identification of multidrug-resistant Salmonella serotype Newport. Emerg. Infect. Dis. 9:496-499.
18. Garaizar, J., N. Lopez-Molina, I. Laconcha, B. D. Lau, A. Rementeria, A. Vivanco, A. Audicana, and I. Perales. 2000. Suitability of PCR fingerprinting, infrequent-restriction-site PCR, and pulsed-field gel electrophoresis, combined with computerized gel analysis, in library typing of Salmonella enterica serovar Enteritidis. Appl. Environ. Microbiol. 66:5273-5281.
19. Gorman, R., and C. C. Adley. 2004. Characterization of Salmonella enterica serotype Typhimurium isolates from human, food, and animal sources in the Republic of Ireland. J. Clin. Microbiol. 42:2314-2316.
20. Grundmann, H., S. Hori, M. C. Enright, C. Webster, A. Tami, E. J. Feil, and T. Pitt. 2002. Determining the genetic structure of the natural population of Staphylococcus aureus: a comparison of multilocus sequence typing with pulsed-field gel electrophoresis, randomly amplified polymorphic DNA analysis, and phage typing. J. Clin. Microbiol. 40:4544-4546.
21. Gudmundsdottir, S., H. Hardardottir, and E. Gunnarsson. 2003. Subtyping of Salmonella enterica serovar Typhimurium outbreak strains isolated from humans and animals in Iceland. J. Clin. Microbiol. 41:4833-4835.
22. Gupta, A., J. Fontana, C. Crowe, B. Bolstorff, A. Stout, S. Van Duyne, M. P. Hoekstra, J. M. Whichard, T. J. Barrett, and F. J. Angulo. 2003. Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. J. Infect. Dis. 188:1707-1716.
23. Homan, W. L., D. Tribe, S. Poznanski, M. Li, G. Hogg, E. Spalburg, J. D. Van Embden, and R. J. Willems. 2002. Multilocus sequence typing scheme for Enterococcus faccium. J. Clin. Microbiol. 40:1963-1971.
24. Hudson, C. R., M. Garcia, R. K. Gast, and J. J. Maurer. 2001. Determination of close genetic relatedness of the major Salmonella enteritidis phage types by pulsed-field gel electrophoresis and DNA sequence analysis of several Salmonella virulence genes. Avian Dis. 45:875-886.
25. Hunter, P. R., and M. A. Gaston. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J. Clin. Microbiol. 26:2465-2466.
26. Jefferies, J. M., A. Smith, S. C. Clarke, C. Dowson, and T. J. Mitchell. 2004. Genetic analysis of diverse disease-causing pneumococci indicates high levels of diversity within serotypes and capsule switching. J. Clin. Microbiol. 42:5681-5688.
27. Jolley, K. A., J. Kalmusova, E. J. Feil, S. Gupta, M. Musilek, P. Kriz, and M. C. Maiden. 2000. Carried meningococci in the Czech Republic: a diverse recombining population. J. Clin. Microbiol. 38:4492-4498.
28. Kirk, M. B., C. L. Little, M. Lem, M. Fyfe, D. Genobile, A. Tan, J. Threlfall, A. Paccagnella, D. Lightfool, H. Lyi, L. McIntyre, L. Ward, D. J. Brown, S. Surnam, and I. S. Fisher. 2004. An outbreak due to peanuts in their shell caused by Salmonella enterica serotypes Stanley and Newport-sharing molecular information to solve international outbreaks. Epidemiol. Infect. 132:571-577.
29. Kotetishvili, M., O. C. Stine, A. Kreger, J. G. Morris, Jr., and A. Sulakvelidze. 2002. Multilocus sequence typing for characterization of clinical and environmental Salmonella strains. J. Clin. Microbiol. 40:1626-1635.
30. Kubota, K., T. J. Barrett, M. L. Ackers, P. S. Brachman, and E. D. Mintz. 2005. Analysis of Salmonella enterica serotype Typhi pulsed-field gel electrophoresis patterns associated with international travel. J. Clin. Microbiol. 43:1205-1209.
31. Maiden, M. C., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. Zhou, K. Zurth, D. A. Caugant, I. M. Feavers, M. Achtman, and B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95:3140-3145.
32. Martinez-Urtaza, J., E. Liebana, L. Garcia-Migura, P. Perez-Pineiro, and M. Saco. 2004. Characterization of Salmonella enterica serovar Typhimurium from marine environments in coastal waters of Galicia (Spain). Appl. Environ. Microbiol. 70:4030-4034.
33. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
34. Murase, T., T. Okitsu, R. Suzuki, H. Morozumi, A. Matsushima, A. Nakamura, and S. Yamai. 1995. Evaluation of DNA fingerprinting by PFGE as an epidemiologic tool for Salmonella infections. Microbiol. Immunol. 39:673-676.
35. National Center for Infectious Diseases, CDC; Division of Bacterial and Mycotic Diseases, Foodborne and Diarrheal Diseases Branch, Public Health Practice Program Office, CDC, Division of Laboratory Services; and Association of Public Health Laboratories. 2002. Standardized molecular subtyping of foodborne bacterial pathogens by pulsed-field gel electrophoresis. Centers for Disease Control and Prevention, Atlanta, Ga.
36. Nayak, R., T. Stewart, R. F. Wang, J. Lin, C. E. Cerniglia, and P. B. Kenney. 2004. Genetic diversity and virulence gene determinants of antibiotic-resistant Salmonella isolated from preharvest turkey production sources. Int. J. Food Microbiol. 91:51-62.
37. NCCLS. 2002. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved standard, 2nd ed. NCCLS document M31-A2. NCCLS, Wayne, Pa.
38. NCCLS. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard, 6th ed. NCCLS document M7-A6. NCCLS, Wayne, Pa.
39. Nemoy, L. L., M. Kotetishvili, J. Tigno, A. Keefer-Norris, A. D. Harris, E. N. Perencevich, J. A. Johnson, D. Torpey, A. Sulakvelidze, J. G. Morris, Jr., and O. C. Stine. 2005. Multilocus sequence typing versus pulsed-field gel electrophoresis for characterization of extended-spectrum beta-lactamase- producing Escherichia coli isolates. J. Clin. Microbiol. 43:1776-1781.
40. Noller, A. C., M. C. McEllistrem, O. C. Stine, J. G. Morris, Jr., D. J. Boxrud, B. Dixon, and L. H. Harrison. 2003. Multilocus sequence typing reveals a lack of diversity among Escherichia coli O157:H7 isolates that are distinct by pulsed-field gel electrophoresis. J. Clin. Microbiol. 41:675-679.
41. Olsen, J. E., M. N. Skov, E. J. Threlfall, and D. J. Brown. 1994. Clonal lines of Salmonella enterica serotype Enteritidis documented by IS200-, ribo-, pulsed-field gel electrophoresis and RFLP typing. J. Med. Microbiol. 40:15-22.
42. Pitout, J. D., M. D. Reisbig, M. Mulvey, L. Chui, M. Louie, L. Crowe, D. L. Church, S. Elsayed, D. Gregson, R. Ahmed, P. Tilley, and N. D. Hanson. 2003. Association between handling of pet treats and infection with Salmonella enterica serotype Newport expressing the AmpC beta-lactamase. CMY-2. J. Clin. Microbiol. 41:4578-4582.
43. Prager, R., W. Rabsch, W. Streckel, W. Voigt, E. Tietze, and H. Tschape. 2003. Molecular properties of Salmonella enterica serotype Paratyphi B distinguish between its systemic and its enteric pathovars. J. Clin. Microbiol. 41:4270-4278.
44. Ramisse, V., P. Houssu, E. Hernandez, F. Denoeud, V. Hilaire, O. Lisanti, F. Ramisse, J. D. Cavallo, and G. Vergnaud. 2004. Variable number of tandem repeats in Salmonella enterica subsp. enterica for typing purposes. J. Clin. Microbiol. 42:5722-5730.
45. Rankin, S. C., H. Aceto, J. Cassidy, J. Holt, S. Young, B. Love, D. Tewari, D. S. Munro, and C. E. Benson. 2002. Molecular characterization of cephalosporin-resistant Salmonella enterica serotype Newport isolates from animals in Pennsylvania. J. Clin. Microbiol. 40:4679-4684.
46. Reche, M. P., M. A. Echeita, J. E. los Rios, M. A. Usera, P. A. Jimenez, A. M. Rojas, J. Colas, and I. Rodriguez. 2003. Comparison of phenotypic and genotypic markers for characterization of an outbreak of Salmonella serotype Havana in captive raptors. J. Appl. Microbiol. 94:65-72.
47. Ross, I. L., and M. W. Heuzenroeder. 2005. Discrimination within phenotypically closely related definitive types of Salmonella enterica serovar Typhimurium by the multiple amplification of phage locus typing technique. J. Clin. Microbiol. 43:1604-1611.
48. Seno, M., M. Sakaki, and H. Ogawa. 2004. Genotypic diversity of Salmonella Enteritidis isolates from sporadic patients in limited area during one year. J. Infect. 49:291-296.
49. Sivapalasingam, S., E. Barrett, A. Kimura, S. Van Duyne, W. De Witt, M. Ying, A. Frisch, Q. Phan, E. Gould, P. Shillam, V. Reddy, T. Cooper, M. Hoekstra, C. Higgins, J. P. Sanders, R. V. Tauxe, and L. Slutsker. 2003. A multistate outbreak of Salmonella enterica serotype Newport infection linked to mango consumption: impact of water-dip disinfestation technology. Clin. Infect. Dis. 37:1585-1590.
50. Spika, J. S., S. H. Waterman, G. W. Hoo, M. E. St Louis, R. E. Pacer, S. M. James, M. L. Bissett, L. W. Mayer, J. Y. Chiu, and B. Hall. 1987. Chloramphenicol-resistant Salmonella newport traced through hamburger to dairy farms. A major persisting source of human salmonellosis in California. N. Engl. J. Med. 316:565-570.
51. Sreevatsan, S., X. Pan, K. E. Stockbauer, N. D. Connell, B. N. Kreiswirth, T. S. Whittam, and J. M. Musser. 1997. Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionary recent global dissemination. Proc. Natl. Acad. Sci. USA 94:9869-9874.
52. Sukhnanand, S., S. Alcaine, L. D. Warnick, W. L. Su, J. Hof, M. P. Craver, P. McDonough, K. J. Boor, and M. Wiedmann. 2005. DNA sequence-based subtyping and evolutionary analysis of selected Salmonella enterica serotypes. J. Clin. Microbiol. 43:3688-3698.
53. Swaminathan, B., T. J. Barrett, S. B. Hunter, and R. V. Tauxe. 2001. PulseNet: the molecular suhtyping network for foodhorne bacterial disease surveillance, United States. Emerg. Infect. Dis. 7:382-389.
54. Torpdahl, M., M. N. Skov, D. Sandvang, and D. L. Baggesen. 2005. Genotypic characterization of Salmonella by multilocus sequence typing, pulsed-field gel electrophoresis and amplified fragment length polymorphism. J. Microbiol. Methods 63:173-184.
55. Urwin, R., and M. C. Maiden. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol. 11:479-487.
56. Voetsch, A. C., T. J. Van Gilder, F. J. Angulo, M. M. Farley, S. Shallow, R. Marcus, P. R. Cieslak, V. C. Deneen, and R. V. Tauxe. 2004. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin. Infect. Dis. 38(Suppl. 3):S127-S134.
57. Weide-Botjes, M., B. Kobe, C. Lange, and S. Schwarz. 1998. Molecular typing of Salmonella enterica subsp. enterica serovar Hadar: evaluation and application of different typing methods. Vet. Microbiol. 61:215-227.
58. Yong, D., Y. S. Lim, J. H. Yum, H. Lee, K. Lee, E. C. Kim, B. K. Lee, and Y. Chong. 2005. Nosocomial outbreak of pediatric gastroenteritis caused by CTX-M-14-type extended-spectrum beta-lactamase-producing strains of Salmonella enterica serovar London. J. Clin. Microbiol. 43:3519-3521.
59. Zhao, S., S. Qaiyumi, S. Friedman, R. Singh, S. L. Foley, D. G. White, P. F. McDermott, T. Donkar, C. Bolin, S. Munro, E. J. Baron, and R. D. Walker. 2003. Characterization of Salmonella enterica serotype Newport isolated from humans and food animals. J. Clin. Microbiol. 41:5366-5371.