Differential single nucleotide polymorphism-based analysis of an outbreak caused by Salmonella enterica serovar Manhattan reveals epidemiological details missed by standard pulsed-field gel electrophoresis

Journal of Clinical Microbiology

Volumn 53, Issue 4, 2015, Pages 1227-1238

  Scaltriti, Erika ^a   Sassera, Davide ^b   Comandatore, Francesco ^b,c   Morganti, C Marina ^a   Mandalari, Carmen ^a   Gaiarsa, Stefano ^c,d   Bandi, Claudio ^c   Zehender, Gianguglielmo ^c   Bolzoni, Luca ^a   Casadei, Gabriele ^a   Pongolinia, Stefano ^a  

^a ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELLA LOMBARDIA E DELL EMILIA ROMAGNA   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIUM ISOLATE; BAYES THEOREM; CLINICAL ARTICLE; CODON; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; EPIDEMIC; FOOD; GENOME ANALYSIS; GENOTYPING TECHNIQUE; GOLD STANDARD; HUMAN; MAXIMUM LIKELIHOOD METHOD; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; RETROSPECTIVE STUDY; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR MANHATTAN; SALMONELLOSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; CASE REPORT; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; FOOD CONTROL; GENETICS; GENOTYPE; ISOLATION AND PURIFICATION; ITALY; MICROBIOLOGY; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; PROCEDURES; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL;

ANIMALIA; SALMONELLA ENTERICA;

BACTERIAL DNA;

ANIMALS; CLUSTER ANALYSIS; DISEASE OUTBREAKS; DNA, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FOOD MICROBIOLOGY; GENOTYPE; HUMANS; ITALY; MOLECULAR EPIDEMIOLOGY; MOLECULAR TYPING; POLYMORPHISM, SINGLE NUCLEOTIDE; RETROSPECTIVE STUDIES; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA INFECTIONS, ANIMAL;

EID: 84925262778     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02930-14     Document Type: Article

References (48)

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 nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882-889. http://dx.doi.org/10.1086/650733.
2. European Food Safety Authority (EFSA), European Centre for Disease Prevention and Control (ECDC). 2013. Scientific report of EFSA and ECDC: the European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J 11: 3129-3378. http://dx.doi.org/10.2903/j.efsa.2013.3129.
3. Wattiau P, Boland C, Bertrand S. 2011. Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol 77:7877-7885. http://dx.doi.org/10.1128/AEM.05527-11.
4. 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:e55254. http://dx.doi.org/10.1371/journal.pone.0055254.
5. Urwin R, Maiden MCJ. 2003. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 11:479-487. http://dx.doi.org/10.1016/j.tim.2003.08.006.
6. Achtman M, Wain J, Weill F-X, 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 sequencing typing as a replacement for serotyping in Salmonella enterica . PLoS Pathog 8:e1002776. http://dx.doi.org/10.1371/journal.ppat.1002776.
7. Fakhr MK, Nolan LK, Logue CM. 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. http://dx.doi.org/10.1128/JCM.43.5.2215-2219.2005.
8. Harris SR, Feil EJ, Holden MTG, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD. 2010. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474. http://dx.doi.org/10.1126/science.1182395.
9. 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.
10. Desai PT, Porwollik S, Long F, Cheng P, Wollam A, Clifton SW, Weinstock GM, McClelland M. 2013. Evolutionary genomics of Salmonella enterica subspecies. mBio 4:e00579-12. http://dx.doi.org/10.1128/mBio.00579-12.
11. Timme RE, Pettengill JB, Allard MW, Strain E, Barrangou R, Wehnes C, Van Kessel JS, Karns JS, Musser SM, Brown EW. 2013. Phylogenetic diversity of the enteric pathogen Salmonella enterica subsp. enterica inferred from genome-wide reference-free SNP characters. Genome Biol Evol 5:2109-2123. http://dx.doi.org/10.1093/gbe/evt159.
12. Hoffmann M, Zhao S, Pettengill J, Luo Y, Monday SR, Abbott J, Ayers SL, Cinar HN, Muruvanda T, Li C, Allard MW, Whichard J, Meng J, Brown EW, McDermott PF. 2014. Comparative genomic analysis and virulence differences in closely related Salmonella enterica serotype Heidelberg isolates from humans, retail meats, and animals. Genome Biol Evol 6:1046-1068. http://dx.doi.org/10.1093/gbe/evu079.
13. 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.
14. Lienau EK, Strain E, Wang C, Zheng J, Ottesen AR, Keys CE, Hammack TS, Musser SM, Brown EW, Allard MW, Cao G, Meng J, 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.
15. Cao G, Meng J, Strain E, Stones R, Pettengill J, Zhao S, McDermott P, Brown E, Allard M. 2013. Phylogenetics and differentiation of Salmonella Newport lineages by whole genome sequencing. PLoS One 8:e55687. http://dx.doi.org/10.1371/journal.pone.0055687.
16. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC, Harris SR, Brown DJ, Coia JE, Mulvey MR, Gilmour MW, Petrovska L, De Pinna E, Kuroda M, Akiba M, Izumiya H, Connor TR, Suchard MA, Lemey P, Mellor DJ, Haydon DT, Thomson NR. 2013. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 341:1514-1517. http://dx.doi.org/10.1126/science.1240578.
17. Pang S, Octavia S, Feng L, Liu B, Reeves PR, Lan R, Wang L. 2013. Genomic diversity and adaptation of Salmonella enterica serovar Typhimurium from analysis of six genomes of different phage types. BMC Genomics 14:718. http://dx.doi.org/10.1186/1471-2164-14-718.
18. Leekitcharoenphon P, Friis C, Zankari E, Svendsen CA, Price LB, Rahmani M, Herrero-Fresno A, Fashae K, Vandenberg O, Aarestrup FM, Hendriksen RS. 2013. Genomics of an emerging clone of Salmonella serovar Typhimurium ST313 from Nigeria and the Democratic Republic of Congo. J Infect Dev Ctries 7:696-706. http://dx.doi.org/10.3855/jidc.3328.
19. Noël H, Dominguez M, Weill FX, Brisabois A, Duchazeaubeneix C, Kerouanton A, Delmas G, Pihier N, Couturier E. 2006. Outbreak of Salmonella enterica serotype Manhattan infection associated with meat products, France, 2005. Euro Surveill 11:270-273. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=660.
20. Fisher I, Crowcroft N. 1998. Enter-net/EPIET investigation into the multinational cluster of Salmonella Livingstone. Euro Surveill 2:pii=1271. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=1271.
21. European Food Safety Authority. 2012. Technical report: manual for reporting of food-borne outbreaks in accordance with Directive/99/EC from the year 2011. Supporting publication 2012:EN-265. European Safety Food Authority, Parma, Italy. http://www.efsa.europa.eu/en/supporting/doc/265e.pdf.
22. PulseNet. 2010. One-day (24-28 h) standardized laboratory protocol for molecular subtyping of Escherichia coli O157:H7, non-typhoidal Salmonella serotypes, and Shigella sonnei, by pulsed field gel electrophoresis (PFGE). Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/pulsenet/protocols/ecoli-salmonella-shigella-protocols.pdf.
23. Magoc T, Salzberg SL. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963. http://dx.doi.org/10.1093/bioinformatics/btr507.
24. Chevreux B, Wetter T, Suhai S. 1999. Genome sequence assembly using trace signals and additional sequence information, p 45-56. In Computer science and biology. Proceedings of the German Conference on Bioinformatics, GCB '99. GCB, Hannover, Germany.
25. Chain PS1, Grafham DV, Fulton RS, Fitzgerald MG, Hostetler J, Muzny D, Ali J, Birren B, Bruce DC, Buhay C, Cole JR, Ding Y, Dugan S, Field D, Garrity GM, Gibbs R, Graves T, Han CS, Harrison SH, Highlander S, Hugenholtz P, Khouri HM, Kodira CD, Kolker E, Kyrpides NC, Lang D, Lapidus A, Malfatti SA, Markowitz V, Metha T, Nelson KE, Parkhill J, Pitluck S, Qin X, Read TD, Schmutz J, Sozhamannan S, Sterk P, Strausberg RL, Sutton G, Thomson NR, Tiedje JM, Weinstock G, Wollam A, Genomic Standards Consortium Human Microbiome Project Jumpstart Consortium, Detter JC. 2009. Genome Project standards in a new era of sequencing. Science 326:236-237. http://dx.doi.org/10.1126/science.1180614.
26. Sassera D, Gaiarsa S, Scaltriti E, Morganti M, Bandi C, Casadei G, Pongolini S. 2013. Draft genome sequence of Salmonella enterica subsp. enterica serovar Manhattan strain 111113, from an outbreak of human infections in northern Italy. Genome Announc 1:e00632-13. http://dx.doi.org/10.1128/genomeA.00632-13.
27. Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147. http://dx.doi.org/10.1371/journal.pone.0011147.
28. Gaiarsa S, Comandatore F, Gaibani P, Corbella M, Dalla Valle C, Epis S, Scaltriti E, Carretto E, Farina C, Labonia M, Landini MP, Pongolini S, Sambri V, Bandi C, Marone P, Sassera D. 2014. Genomic epidemiology of Klebsiella pneumoniae in Italy and novel insights into the origin and global evolution of its resistance to carbapenem antibiotics. Antimicrob Agents Chemother 59:389-396. http://dx.doi.org/10.1128/AAC.04224-14.
29. Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y, Jin Q. 2005. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33: D325-D328. http://dx.doi.org/10.1093/nar/gki008.
30. Yang J, Chen L, Sun L, Yu J, Jin Q. 2007. VFDB 2008 release: an enhanced Web-based resource for comparative pathogenomics. Nucleic Acids Res 36:D539-D542. http://dx.doi.org/10.1093/nar/gkm951.
31. Chen L, Xiong Z, Sun L, Yang J, Jin Q. 2011. VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40:D641-D645. http://dx.doi.org/10.1093/nar/gkr989.
32. Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. http://dx.doi.org/10.1186/1471-2105-11-119.
33. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. http://dx.doi.org/10.1038/nmeth.2109.
34. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758-771. http://dx.doi.org/10.1080/10635150802429642.
35. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. http://dx.doi.org/10.1093/bioinformatics/17.8.754.
36. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. http://dx.doi.org/10.1093/bioinformatics/btg180.
37. Bofkin L, Goldman N. 2006. Variation in evolutionary processes at different codon positions. Mol Biol Evol 24:513-521. http://dx.doi.org/10.1093/molbev/msl178.
38. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, Swaminathan B. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233-2239.
39. Rostagno MH. 2009. Can stress in farm animals increase food safety risk? Foodborne Pathog Dis 6:767-776. http://dx.doi.org/10.1089/fpd.2009.0315.
40. Rostagno MH, Callaway TR. 2012. Pre-harvest risk factors for Salmonella enterica in pork production. Food Res Int 45:634-640. http://dx.doi.org/10.1016/j.foodres.2011.04.041.
41. Uchida K, Aizawa SI. 2014. The flagellar soluble protein FliK determines the minimal length of the hook in Salmonella enterica serovar Typhimurium. J Bacteriol 196:1753-1758. http://dx.doi.org/10.1128/JB.00050-14.
42. Waters RC, O'Toole PW, Ryan KA. 2007. The FliK protein and flagellar hook-length control. Protein Sci 16:769-780. http://dx.doi.org/10.1110/ps.072785407.
43. Suez J, Porwollik S, Dagan A, Marzel A, Schorr YI, Desai PT, Agmon V, McClelland M, Rahav G, Gal-Mor O. 2013. Virulence gene profiling and pathogenicity characterization of non-typhoidal Salmonella accounted for invasive disease in humans. PLoS One 8:e58449. http://dx.doi.org/10.1371/journal.pone.0058449.
44. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Baumler AJ. 2005. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun 73:3358-3366. http://dx.doi.org/10.1128/IAI.73.6.3358-3366.2005.
45. Komoriya K, Shibano N, Higano T, Azuma N, Yamaguchi S, Aizawa S-I. 1999. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella Typhimurium. Mol Microbiol 34:767-779. http://dx.doi.org/10.1046/j.1365-2958.1999.01639.x.
46. Köplin R, Brisson J-R, Whitfield C. 1997. UDP-galactofuranose precursor required for formation of the lipopolysaccharide O antigen of Klebsiella pneumoniae serotype O1 is synthesized by the product of the rfbDKPO1 gene. J Biol Chem 272:4121-4128. http://dx.doi.org/10.1074/jbc.272.7.4121.
47. Leekitcharoenphon P, Lukjancenko O, Friis C, Aarestrup F, Ussery D. 2012. Genomic variation in Salmonella enterica core genes for epidemiological typing. BMC Genomics 13: 88. http://dx.doi.org/10.1186/1471-2164-13-88.
48. Lienau EK, Blazar JM, Wang C, Brown EW, Stones R, Musser S, Allard MW. 2013. Phylogenomic analysis identifies gene gains that define Salmonella enterica subspecies I. PLoS One 8:e76821. http://dx.doi.org/10.1371/journal.pone.0076821.