Characterization of foodborne outbreaks of salmonella enterica serovar enteritidis with whole-genome sequencing single nucleotide polymorphism-based analysis for surveillance and outbreak detection

Journal of Clinical Microbiology

Volumn 53, Issue 10, 2015, Pages 3334-3340

  Taylor, Angela J ^a   Lappi, Victoria ^a   Wolfgang, William J ^b   Lapierre, Pascal ^b   Palumbo, Michael J ^b   Medus, Carlota ^a   Boxrud, David ^a  

^a MINNESOTA DEPARTMENT OF HEALTH   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIUM DETECTION; BACTERIUM ISOLATE; CONTROLLED STUDY; DISEASE SURVEILLANCE; EPIDEMIC; GENE SEQUENCE; GENETIC DISTANCE; HUMAN; INTERMETHOD COMPARISON; MAJOR CLINICAL STUDY; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RETROSPECTIVE STUDY; SALMONELLA ENTERICA SEROVAR ENTERITIDIS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; WHOLE GENOME SEQUENCING; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; EPIDEMIOLOGICAL MONITORING; EVALUATION STUDY; FOODBORNE DISEASES; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; PROCEDURES; SALMONELLA INFECTIONS; UNITED STATES;

CLUSTER ANALYSIS; DISEASE OUTBREAKS; EPIDEMIOLOGICAL MONITORING; FOODBORNE DISEASES; GENOME, BACTERIAL; GENOTYPE; HUMANS; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; POLYMORPHISM, SINGLE NUCLEOTIDE; RETROSPECTIVE STUDIES; SALMONELLA ENTERITIDIS; SALMONELLA INFECTIONS; SEQUENCE ANALYSIS, DNA; UNITED STATES;

EID: 84941978846     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.01280-15     Document Type: Article

References (47)

1. Witt-Kushner J, Astles JR, Ridderhof JC, Martin RA, Wilcke B, Jr, Downes FP, Inhorn SL, Kelley HP, Kimsey PB, Mills DE, Salfinger M, Shult PA, Verma MP, Becker SJ, Drabkowski DJ. 2002. Core functions and capabilities of state public health laboratories: a report of the Association of Public Health Laboratories. MMWR Recommend Rep 51:1-8.
2. Foley SL, Zhao SH, Walker RD. 2007. Comparison of molecular typing methods for the differentiation of Salmonella foodborne pathogens. Foodborne Pathog Dis 4:253-276. http://dx. doi. org/10. 1089/fpd. 2007 . 0085.
3. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-15. http://dx. doi. org/10 . 3201/eid1701. P11101.
4. Guard-Petter J. 2001. The chicken, the egg and Salmonella enteritidis. Environ Microbiol 3:421-430. http://dx. doi. org/10. 1046/j. 1462-2920. 2001. 00213. x.
5. Centers for Disease Control and Prevention. 2013. Surveillance for foodborne disease outbreaks-United States, 1998-2008. MMWRSurveill Summ 62:1-34.
6. Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, Griffin PM. 2013. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerg Infect Dis 19:407-415. http://dx. doi. org/10 . 3201/eid1903. 111866.
7. Allard MW, Luo Y, Strain E, Pettengill J, Timme R, Wang C, Li C, Keys CE, Zheng J, Stones R, Wilson MR, Musser SM, Brown EW. 2013. On the evolutionary history, population genetics and diversity among isolates of Salmonella Enteritidis PFGE pattern JEGX01. 0004. PLoS One. 8(1): e55254. http://dx. doi. org/10. 1371/journal. pone. 0055254.
8. Saeed AM, Walk ST, Arshad M, Whittam TS. 2006. Clonal structure and variation in virulence of Salmonella Enteritidis isolated from mice, chickens, and humans. J AOAC Int 89:504-511.
9. Botteldoorn N, Van Coillie E, Goris J, Werbrouck H, Piessens V, Godard C, Scheldeman P, Herman L, Heyndrickx M. 2010. Limited genetic diversity and gene expression differences between egg-and nonegg-related Salmonella Enteritidis strains. Zoonoses Public Health 57: 345-357. http://dx. doi. org/10. 1111/j. 1863-2378. 2008. 01216. x.
10. Boxrud D, Pederson-Gulrud K, Wotton J, Medus C, Lyszkowicz E, Besser J, Bartkus JM. 2007. Comparison of multiple-locus variable-number tandem repeat analysis, pulsed-field gel electrophoresis, and phage typing for subtype analysis of Salmonella enterica serotype Enteritidis. J Clin Microbiol 45:536-543. http://dx. doi. org/10. 1128/JCM. 01595-06.
11. Deng X, Shariat N, Driebe EM, Roe CC, Tolar B, Trees E, Keim P, Zhang W, Dudley EG, Fields PI, Engelthaler DM. 2015. Comparative analysis of subtyping methods against a whole-genome-sequencing standard in Salmonella enterica serotype Enteritidis. J Clin Microbiol 53:212-218. http://dx. doi. org/10. 1128/JCM. 02332-14.
12. Köser CU, Ellington MJ, Cartwright EJP, Gillespie SH, Brown NM, Farrington M, Holden MTG, Dougan G, Bentley SD, Parkhill J, Peacock SJ. 2012. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 8(8):e1002824. http://dx. doi. org/10. 1371/journal. ppat. 1002824.
13. Cheung MK, Kwan HS. 2012. Fighting outbreaks with bacterial genomics: case review and workflow proposal. Public Health Genomics 15:341-351. http://dx. doi. org/10. 1159/000342770.
14. Didelot X, Bowden R, Wilson DJ, Peto TEA, Crook DW. 2012. Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 13:601-612. http://dx. doi. org/10. 1038/nrg3226.
15. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN, Segre JA, NISC Comparative Sequencing Program Group 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4(148):148ra116. http://dx. doi. org/10. 1126/scitranslmed. 3004129.
16. Cody AJ, McCarthy ND, van Rensburg MJ, Isinkaye T, Bentley SD, Parkhill J, Dingle KE, Bowler I, Jolley KA, Maiden MCJ. 2013. Real-time genomic epidemiological evaluation of human Campylobacter isolates by use of whole-genome multilocus sequence typing. J Clin Microbiol 51: 2526-2534. http://dx. doi. org/10. 1128/JCM. 00066-13.
17. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, FitzGerald M, Godfrey P, Haas BJ, Murphy CI, Russ C, Sykes S, Walker BJ, Wortman JR, Young S, Zeng Q, Abouelleil A, Bochicchio J, Chauvin S, DeSmet T, Gujja S, McCowan C, Montmayeur A, Steelman S, Frimodt-Møller J, Petersen AM, Struve C, Krogfelt KA, Bingen E, Weill F-X, Lander ES, Nusbaum C, Birren BW, Hung DT, Hanage WP. 2012. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc Natl Acad Sci U S A 109:3065-3070. http://dx. doi. org/10 . 1073/pnas. 1121491109.
18. Reuter S, Ellington MJ, Cartwright EJP, Köser CU, Török ME, Gouliouris T, Harris SR, Brown NM, Holden MTG, Quail M, Parkhill J, Smith GP, Bentley SD, Peacock SJ. 2013. Rapid bacterial whole-genome sequencing to enhance diagnostic and public health microbiology. JAMA Intern Med 173:1397-1404. http://dx. doi. org/10. 1001/jamainternmed . 2013. 7734.
19. Gilmour M, Graham M, Van Domselaar G, Tyler S, Kent H, Trout-Yakel K, Larios O, Allen V, Lee B, Nadon C. 2010. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 11:120. http://dx. doi. org/10 . 1186/1471-2164-11-120.
20. Chin CS, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK. 2011. The origin of the Haitian cholera outbreak strain. N Engl J Med 364:33-42. http://dx. doi. org/10. 1056/NEJMoa1012928.
21. Gardy JL, Johnston JC, Sui SJH, Cook VJ, Shah L, Brodkin E, Rempel S, Moore R, Zhao Y, Holt R, Varhol R, Birol I, Lem M, Sharma MK, Elwood K, Jones SJM, Brinkman FSL, Brunham RC, Tang P. 2011. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730-739. http://dx. doi . org/10. 1056/NEJMoa1003176.
22. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE. 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13:137-146. http://dx. doi . org/10. 1016/S1473-3099(12)70277-3.
23. Roetzer A, Diel R, Kohl TA, Rückert C, Nübel U, Blom J, Wirth T, Jaenicke S, Schuback S, Rüsch-Gerdes S, Supply P, Kalinowski J, Niemann S. 2013. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 10(2):e1001387. http://dx . doi. org/10. 1371/journal. pmed. 1001387.
24. Köser CU, Holden MTG, Ellington MJ, Cartwright EJP, Brown NM, Ogilvy-Stuart AL, Hsu LY, Chewapreecha C, Croucher NJ, Harris SR, Sanders M, Enright MC, Dougan G, Bentley SD, Parkhill J, Fraser LJ, Betley JR, Schulz-Trieglaff OB, Smith GP, Peacock SJ. 2012. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366:2267-2275. http://dx. doi. org/10 . 1056/NEJMoa1109910.
25. Eyre DW, Golubchik T, Gordon NC, Bowden R, Piazza P, Batty EM, Ip CLC, Wilson DJ, Didelot X, O'Connor L, Lay R, Buck D, Kearns AM, Shaw A, Paul J, Wilcox MH, Donnelly PJ, Peto TEA, Walker AS, Crook DW. 2012. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2(3):e001124. http://dx. doi. org/10. 1136/bmjopen-2012-001124.
26. Harrison EM, Paterson GK, Holden MTG, Larsen J, Stegger M, Larsen AR, Petersen A, Skov RL, Christensen JM, Zeuthen AB, Heltberg O, Harris SR, Zadoks RN, Parkhill J, Peacock SJ, Holmes MA. 2013. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol Med 5:509-515. http: //dx. doi. org/10. 1002/emmm. 201202413.
27. Lewis T, Loman NJ, Bingle L, Jumaa P, Weinstock GM, Mortiboy D, Pallen MJ. 2010. High-throughput whole-genome sequencing to dissect the epidemiology of Acinetobacter baumannii isolates from a hospital outbreak. J Hosp Infect 75:37-41. http://dx. doi. org/10. 1016/j. jhin. 2010. 01 . 012.
28. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, Aarestrup FM. 2014. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52:1501-1510. http://dx. doi. org/10. 1128/JCM . 03617-13.
29. den Bakker HC, Allard MW, Bopp D, Brown EW, Fontana J, Iqbal Z, Kinney A, Limberger R, Musser KA, Shudt M, Strain E, Wiedmann M, Wolfgang WJ. 2014. Rapid whole-genome sequencing for surveillance of Salmonella enterica serovar Enteritidis. Emerg Infect Dis 20:1306-1314. http://dx. doi. org/10. 3201/eid2008. 131399.
30. Allard MW, 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. BMC Genomics 13:32. http://dx. doi. org/10. 1186/1471-2164-13-32.
31. den Bakker HC, Switt AIM, 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 pulsedfield gel electrophoresis type. Appl Environ Microbiol 77:8648-8655. http://dx. doi. org/10. 1128/AEM. 06538-11.
32. Lienau EK, Strain E, Wang C, Zheng J, Ottesen AR, Keys CE, Hammack TS, Musser SM, Brown EW, Allard MW, Cao GJ, Meng JH, Stones R. 2011. Identification of a salmonellosis outbreak by means of molecular sequencing. N Engl J Med 364:981-982. http://dx . doi. org/10. 1056/NEJMc1100443.
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. http://dx. doi . org/10. 1089/fpd. 2006. 3. 59.
34. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx. doi . org/10. 1093/bioinformatics/btp324.
35. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079. http://dx. doi. org/10. 1093/bioinformatics/btp352.
36. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. http://dx. doi . org/10. 1093/bioinformatics/btq033.
37. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: A fast phage search tool. Nucleic Acids Res 39:W347-W352. http://dx. doi . org/10. 1093/nar/gkr485.
38. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. 2004. Versatile and open software for comparing large genomes. Genome Biol 5:9
39. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3. 0. Syst Biol 59:307-321. http://dx. doi. org/10. 1093/sysbio/syq010.
40. Braden CR. 2006. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43:512-517. http: //dx. doi. org/10. 1086/505973.
41. Leekitcharoenphon P, Nielsen EM, Kaas RS, Lund O, Aarestrup FM. 2014. Evaluation of whole genome sequencing for outbreak detection of Salmonella enterica. PLoS One 9(2):e87991. http://dx. doi. org/10. 1371 /journal. pone. 0087991.
42. Okoro CK, Kingsley RA, Quail MA, Kankwatira AM, Feasey NA, Parkhill J, Dougan G, Gordon MA. 2012. High-resolution single nucleotide polymorphism analysis distinguishes recrudescence and reinfection in recurrent invasive nontyphoidal Salmonella Typhimurium disease. Clin Infect Dis 54:955-963. http://dx. doi. org/10. 1093/cid/cir1032.
43. Ogunremi D, Kelly H, Dupras AA, Belanger S, Devenish J. 2014. Development of a new molecular subtyping tool for Salmonella enterica serovar Enteritidis based on single nucleotide polymorphism genotyping using PCR. J Clin Microbiol 52:4275-4285. http://dx. doi. org/10. 1128 /JCM. 01410-14.
44. Kohl TA, Diel R, Harmsen D, Rothgänger J, Walter KM, Merker M, Weniger T, Niemann S. 2014. Whole-genome-based Mycobacterium tuberculosis surveillance: a standardized, portable, and expandable approach. J Clin Microbiol 52:2479-2486. http://dx. doi. org/10. 1128/JCM . 00567-14.
45. McPherson JD. 2009. Next-generation gap. Nat Methods 6:S2-S5. http: //dx. doi. org/10. 1038/nmeth. f. 268.
46. Schürch AC, Siezen RJ. 2010. Genomic tracing of epidemics and disease outbreaks. Microb Biotechnol 3:628-633. http://dx. doi. org/10. 1111/j . 1751-7915. 2010. 00224. x.
47. Zhang S, Yin Y, Jones MB, Zhang Z, Deatherage Kaiser BL, Dinsmore BA, Fitzgerald C, Fields PI, Deng X. 2015. Salmonella serotype determination utilizing high-throughput genome sequencing data. J Clin Microbiol 53:1685-1692. http://dx. doi. org/10. 1128/JCM. 00323-15.