Comparison of typing methods with a new procedure based on sequence characterization for Salmonella serovar prediction

Journal of Clinical Microbiology

Volumn 51, Issue 6, 2013, Pages 1786-1797

  Ranieri, Matthew L ^a   Shi, Chunlei ^a,b   Moreno Switt, Andrea I ^a   Den Bakker, Henk C ^a   Wiedmann, Martin ^a  

^a Department of Obstetrics Gynecology   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

O ANTIGEN;

ARTICLE; GENE SEQUENCE; INTERMETHOD COMPARISON; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RIBOTYPING; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEQUENCE CHARACTERIZED AMPLIFIED REGION; SEROTYPE; SEROTYPING; WORLD HEALTH ORGANIZATION;

ANTIGENS, BACTERIAL; DNA, BACTERIAL; HUMANS; MOLECULAR TYPING; O ANTIGENS; POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA; SEQUENCE ANALYSIS, DNA; SEROTYPING;

SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA;

EID: 84878488611     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.03201-12     Document Type: Article

References (59)

1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM, International Collaboration on Enteric Disease "Burden of Illness" Studies. 2010. The global burden of non-typhoidal Salmonella gastroenteritis. Clin. Infect. Dis. 50:882-889.
2. Grimont P, Weill FX. 2007. Antigenic formulae of the Salmonella serovars, 9th ed. WHO Collaborating Centre for Reference and Research on Salmonella, Geneva, Switzerland.
3. Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PA, Weill FX. 2010. Supplement 2003-2007 (no. 47) to the White-Kauffmann-Le Minor scheme. Res. Microbiol. 161:26-29.
4. Centers for Disease Control and Prevention. 2011. Salmonella surveillance: annual summary, 2011. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
5. Samuel GG, Reeves PP. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519.
6. Reeves PR, Hobbs M, Valvano MA, Skurnik M, Whitfield C, Coplin D, Kido N, Klena J, Maskell D, Raetz CR, Rick PD. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4:495-503. (Pubitemid 27013225)
7. Fitzgerald C, Sherwood R, Gheesling LL, Brenner FW, Fields PI. 2003. Molecular analysis of the rfb O antigen gene cluster of Salmonella enterica serogroup O:6,14 and development of a serogroup-specific PCR assay. Appl. Environ. Microbiol. 69:6099-6105. (Pubitemid 37280334)
8. Herrera-León S, Ramiro R, Arroyo M, Díez R, Usera MA, Echeita MA. 2007. Blind comparison of traditional serotyping with three multiplex PCRs for the identification of Salmonella serotypes. Res. Microbiol. 158:122-127. (Pubitemid 46341716)
9. Luk JM, Kongmuang U, Reeves PR, Lindberg AA. 1993. Selective amplification of abequose and paratose synthase genes (rfb) by polymerase chain reaction for identification of Salmonella major serogroups (A, B, C2, and D). J. Clin. Microbiol. 31:2118-2123. (Pubitemid 23210505)
10. Joys TM. 1985. The covalent structure of the phase-1 flagellar filament protein of Salmonella Typhimurium and its comparison with other flagellins. J. Biol. Chem. 260:15758-15761.
11. McQuiston JR, Parrenas R, Ortiz-Rivera M, Gheesling L, Brenner F, Fields PI. 2004. Sequencing and comparative analysis of flagellin genes fliC, fljB, and flpA from Salmonella. J. Clin. Microbiol. 42:1923-1932. (Pubitemid 38637803)
12. Silverman M, Zieg J, Hilmen M, Simon M. 1979. Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc. Natl. Acad. Sci. U. S. A. 76:391-395. (Pubitemid 9110202)
13. Franklin K, Lingohr EJ, Yoshida C, Anjum M, Bodrossy L, Clark CG, Kropinski AM, Karmali MA. 2011. Rapid genoserotyping tool for classification of Salmonella serovars. J. Clin. Microbiol. 49:2954-2965.
14. Yoshida C, Franklin K, Konczy P, McQuiston JR, Fields PI, Nash JH, Taboada EN, Rahn K. 2007. Methodologies towards the development of an oligonucleotide microarray for determination of Salmonella serotypes. J. Microbiol. Methods 70:261-271. (Pubitemid 47198132)
15. McQuiston JR, Waters RJ, Dinsmore BA, Mikoleit ML, Fields PI. 2011. Molecular determination of H antigens of Salmonella by use of a microsphere-based liquid array. J. Clin. Microbiol. 49:565-573.
16. Zou W, Lin WJ, Hise KB, Chen HC, Keys C, Chen JJ. 2012. Prediction system for rapid identification of Salmonella serotypes based on pulsed-field gel electrophoresis fingerprints. J. Clin. Microbiol. 50:1524-1532.
17. Kérouanton A, Marault M, Lailler R, Weill FX, Feurer C, Espié E, Brisabois A. 2007. Pulsed-field gel electrophoresis subtyping database for foodborne Salmonella enterica serotype discrimination. Foodborne Pathog. Dis. 4:293-303. (Pubitemid 47518168)
18. Esteban E, Snipes K, Hird D, Kasten R, Kinde H. 1993. Use of ribotyping for characterization of Salmonella serotypes. J. Clin. Microbiol. 31:233-237. (Pubitemid 23028616)
19. Bailey JS, Fedorka-Cray PJ, Stern NJ, Craven SE, Cox NA, Cosby DE. 2002. Serotyping and ribotyping of Salmonella using restriction enzyme PvuII. J. Food Prot. 65:1005-1007. (Pubitemid 34609265)
20. Guard J, Sanchez-Ingunza R, Morales C, Stewart T, Liljebjelke K, Kessel J, Ingram K, Jones D, Jackson C, Fedorka-Cray P, Frye J, Gast R, Hinton A, Jr. 2012. Comparison of dkgB-linked intergenic sequence ribotyping to DNA microarray hybridization for assigning serotype to Salmonella enterica. FEMS Microbiol Lett. 337:61-72.
21. Wise MG, Siragusa GR, Plumblee J, Healy M, Cray PJ, Seal BS. 2009. Predicting Salmonella enterica serotypes by repetitive sequence-based PCR. J. Microbiol. Methods 76:18-24.
22. Chenu JW, Cox JM, Pavic A. 2011. Classification of Salmonella enterica serotypes from Australian poultry using repetitive sequence-based PCR. J. Appl. Microbiol. 112:185-196.
23. Kotetishvili M, Stine OC, Kreger A, Morris JG, Sulakvelidze A. 2002. Multilocus sequence typing for characterization of clinical and environmental Salmonella strains. J. Clin. Microbiol. 40:1626-1635. (Pubitemid 34493130)
24. Achtman MM, Wain JJ, Weill FX, Nair S, Zhou Z, Sangal V, Krauland MG, Hale JL, Harbottle H, Uesbeck A, Dougan G, Harrison LH, Brisse S, S. Enterica MLST Study Group. 2012. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 8:e1002776. doi:10.1371/journal. ppat.1002776.
25. Wattiau P, Weijers T, Andreoli P, Schliker C, Veken HV, Maas HM, Verbruggen AJ, Heck ME, Wannet WJ, Imberechts H, Vos P. 2008. Evaluation of the Premi Test Salmonella, a commercial low-density DNA microarray system intended for routine identification and typing of Salmonella enterica. Int. J. Food Microbiol. 123:293-298.
26. Kim S, Frye JG, Hu J, Fedorka-Cray PJ, Gautom R, Boyle DS. 2006. Multiplex PCR-based method for identification ofcommonclinical serotypes of Salmonella enterica subsp. enterica. J. Clin. Microbiol. 44:3608-3615. (Pubitemid 46768803)
27. Arrach N, Porwollik S, Cheng P, Cho A, Long F, Choi SH, McClelland M. 2008. Salmonella serovar identification using PCR-based detection of gene presence and absence. J. Clin. Microbiol. 46:2581-2589.
28. Leader BT, Frye JG, Hu J, Fedorka-Cray PJ, Boyle DS. 2009. Highthroughput molecular determination of Salmonella enterica serovars by use of multiplex PCR and capillary electrophoresis analysis. J. Clin. Microbiol. 47:1290-1299.
29. Soyer Y, Switt AM, Davis MA, Maurer J, McDonough PL, Schoonmaker-Bopp DJ, Dumas NB, Root T, Warnick LD, Gröhn YT, Wiedmann M. 2009. Salmonella enterica serotype 4,5,12:i:-, an emerging Salmonella serotype that represents multiple distinct clones. J. Clin. Microbiol. 47:3546-3556.
30. Moreno Switt AI, Soyer Y, Warnick LD, Wiedmann M. 2009. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i:-. Foodborne Pathog. Dis. 6:407-415.
31. Centers for Disease Control and Prevention. 2006. Salmonella surveillance: annual summary, 2006. U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
32. Galanis E, Lo Fo Wong Lo DM, Patrick ME, Binsztein N, Cieslik A, Chalermchikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC, World Health Organization Global Salm-Surv. 2006. Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg. Infect. Dis. 12:381-388.
33. Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, Barrett TJ. 2006. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog. Dis. 3:59-67.
34. Hunter SB, Vauterin P, Lambert-Fair MA, Van Duyne MS, Kubota K, Graves L, Wrigley D, Barrett T, Ribot E. 2005. Establishment of a universal size standard strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocols: converting the national databases to the new size standard. J. Clin. Microbiol. 43:1045-1050. (Pubitemid 40364915)
35. Kidgell C, Reichard U, Wain J, Linz B, Torpdahl M, Dougan G, Achtman M. 2002. Salmonella Typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect. Genet. Evol. 2:39-45.
36. Mortimer CKB, Peters TM, Gharbia SE, Logan JMJ, Arnold C. 2004. Towards the development of a DNA-sequence based approach to serotyping of Salmonella enterica. BMC Microbiol. 4:31. doi:10.1186/1471-2180-4-31.
37. Imre A, Olasz F, Nagy B. 2005. Development of a PCR system for the characterisation of Salmonella flagellin genes. Acta Vet. Hung. 53:163-172. (Pubitemid 40756596)
38. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
39. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9:286-298. (Pubitemid 351890825)
40. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. (Pubitemid 44642609)
41. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
42. Popoff MY, Le Minor L. 1985. Expression of antigenic factor O:54 is associated with the presence of a plasmid in Salmonella. Ann. Inst. Pasteur Microbiol. 136B:169-179. (Pubitemid 16208222)
43. Werber D, Dreesman J, Feil F, van Treeck U, Fell G, Ethelberg S, Hauri AM, Roggentin P, Prager R, Fisher IST, Behnke SC, Bartelt E, Weise E, Ellis A, Siitonen A, Andersson Y, Tschäpe H, Kramer MH, Ammon A. 2005. International outbreak of Salmonella Oranienburg due to German chocolate. BMC Infect. Dis. 5:7. doi:10.1186/1471-2334-5-7.
44. Elviss NC, Little CL, Hucklesby L, Sagoo S, Surman-Lee S, de Pinna E, Threlfall EJ, Food, Water and Environmental Surveillance. 2009. Microbiological study of fresh herbs from retail premises uncovers an international outbreak of salmonellosis. Int. J. Food Microbiol. 134:83-88.
45. Nicolay N, Thornton L, Cotter S, Garvey P, Bannon O, McKeown P, Cormican M, Fisher I, Little C, Boxall N, De Pinna E, Peters TM, Cowden J, Salmon R, Mason B, Irvine N, Rooney P, O'Flanagan D. 2011. Salmonella enterica serovar Agona European outbreak associated with a food company. Epidemiol. Infect. 139:1272-1280.
46. Weigel RM, Qiao B, Teferedegne B, Suh DK, Barber DA, Isaacson RE, White BA. 2004. Comparison of pulsed field gel electrophoresis and repetitive sequence polymerase chain reaction as genotyping methods for detection of genetic diversity and inferring transmission of Salmonella. Vet. Microbiol. 100:205-217. (Pubitemid 38625691)
47. Gaul SB, Wedel S, Erdman MM, Harris DL, Harris IT, Ferris KE, Hoffman L. 2007. Use of pulsed-field gel electrophoresis of conserved XbaI fragments for identification of swine Salmonella serotypes. J. Clin. Microbiol. 45:472-476.
48. Zou W, Lin WJ, Foley SL, Chen CH, Nayak R, Chen JJ. 2010. Evaluation of pulsed-field gel electrophoresis profiles for identification of Salmonella serotypes. J. Clin. Microbiol. 48:3122-3126.
49. Wattiau P, Van Hessche M, Schlicker C, Vander Veken H, Imberechts H. 2008. Comparison of classical serotyping and PremiTest assay for routine identification of common Salmonella enterica serovars. J. Clin. Microbiol. 46:4037-4040.
50. Soyer Y, Alcaine SD, Schoonmaker-Bopp DJ, Root TP, Warnick LD, McDonough PL, Dumas NB, Gröhn YT, Wiedmann M. 2010. Pulsedfield gel electrophoresis diversity of human and bovine clinical Salmonella isolates. Foodborne Pathog. Dis. 7:707-717.
51. Alcaine SD, Soyer Y, Warnick LD, Su WL, Sukhnanand S, Richards J, Fortes ED, McDonough P, Root TP, Dumas NB, Gröhn Y, Wiedmann M. 2006. Multilocus sequence typing supports the hypothesis that cow- and human-associated Salmonella isolates represent distinct and overlapping populations. Appl. Environ. Microbiol. 72:7575-7585. (Pubitemid 44927659)
52. Fitzgerald C, Collins M, van Duyne S, Mikoleit M, Brown T, Fields P. 2007. Multiplex, bead-based suspension array for molecular determination of common Salmonella serogroups. J. Clin. Microbiol. 45:3323-3334. (Pubitemid 47585658)
53. Fitzgerald C, Gheesling L, Collins M, Fields PI. 2006. Sequence analysis of the rfb loci, encoding proteins involved in the biosynthesis of the Salmonella enterica O17 and O18 antigens: serogroup-specific identification by PCR. Appl. Environ. Microbiol. 72:7949-7953. (Pubitemid 44927712)
54. den Bakker HC, Moreno Switt AI, Govoni G, Cummings CA, Ranieri ML, Degoricija L, Hoelzer K, Rodriguez-Rivera LD, Brown S, Bolchacova E, Furtado MR, Wiedmann M. 2011. Genome sequencing reveals diversification of virulence factor content and possible host adaptation in distinct subpopulations of Salmonella enterica. BMC Genomics 12:425. doi:10.1186/1471-2164-12-425.
55. Allard M, Luo Y, Strain E, Li C, Keys CE, Son I, Stones R, Musser SM, Brown EW. 2012. High resolution clustering of Salmonella enterica serovar Montevideo strains using a next-generation sequencing approach.BMCGenomics 13:32. doi: 10.1186/1471-2164-13-32.
56. Mehta G, Arya SC. 2002. Capsular Vi polysaccharide antigen in Salmonella enterica serovar Typhi isolates. J. Clin. Microbiol. 40:1127-1128. (Pubitemid 34208692)
57. Vangay P, Fugett EB, Sun Q, Wiedmann M. 2013. Food microbe tracker: a web-based tool for storage and comparison of food-associated microbes. J. Food Prot. 76:283-294.
58. Bakker HC, Switt AI, Cummings CA, Hoelzer K, Degoricija L, Rodriguez-Rivera LD, Wright EM, Fang R, Davis M, Root T, Schoonmaker-Bopp D, Musser KA, Villamil E, Waechter H, Kornstein L, Furtado MR, Wiedmann M. 2011. A whole-genome single nucleotide polymorphism-based approach to trace and identify outbreaks linked to a common Salmonella enterica subsp. enterica serovar Montevideo pulsed-field gel electrophoresis type. Appl. Environ. Microbiol. 77:8648-8655.
59. Diaz-Sanchez S, Hanning I, Pendleton S, D'Souza D. 2013. Next-generation sequencing: the future of molecular genetics in poultry production and food safety. Poult. Sci. 92:562-572.