A whole-genome sequencing approach to study cefoxitin-resistant Salmonella enterica serovar Heidelberg isolates from various sources

Antimicrobial Agents and Chemotherapy

Volumn 61, Issue 4, 2017, Pages

  Edirmanasinghe, Romaine ^a,b   Finley, Rita ^c   Parmley, E Jane ^c   Avery, Brent P ^c   Carson, Carolee ^c   Bekal, Sadjia ^d   Golding, George ^a,b   Mulvey, Michael R ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

Author keywords

Beta lactamase; Cefoxitin; Plasmid analysis; Qu bec; Salmonella Heidelberg; Whole genome sequencing

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; CEFTIOFUR; CEFTRIAXONE; ANTIINFECTIVE AGENT; BETA LACTAMASE; BETA-LACTAMASE CMY-2; CEFOXITIN; CEPHALOSPORIN DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; CEFOXITIN RESISTANT SALMONELLA ENTERICA SEROVAR HEIDELBERG ISOLATE; GENE; GENETIC BACKGROUND; HUMAN; PLASMID; POLYMERASE CHAIN REACTION; POULTRY; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; QUEBEC; SALMONELLA ENTERICA SEROVAR HEIDELBERG; SLAUGHTERHOUSE; WHOLE GENOME SEQUENCING; ANIMAL; BACTERIAL GENOME; CANADA; CHICKEN; CLASSIFICATION; DRUG EFFECTS; EPIDEMIOLOGICAL MONITORING; GENE EXPRESSION; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; MEAT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; PHYLOGENY; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSMISSION;

AMOXICILLIN-POTASSIUM CLAVULANATE COMBINATION; AMPICILLIN; ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; CANADA; CEFOXITIN; CEFTRIAXONE; CEPHALOSPORINS; CHICKENS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; EPIDEMIOLOGICAL MONITORING; GENE EXPRESSION; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MEAT; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SALMONELLA ENTERICA; SALMONELLA INFECTIONS;

EID: 85016998043     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01919-16     Document Type: Article

References (42)

1. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM. 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882-889. https://doi.org/10.1086/650733.
2. Public Health Agency of Canada. 2014. National Enteric Surveillance Program (NESP) annual report 2014. http://publications.gc.ca/collections/collection-2016/aspc-phac/HP37-15-2014-eng.pdf.
3. Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, Smith K, Angulo FJ. 2004. Invasive Salmonella infections in the United States, FoodNet, 1996-1999: incidence, serotype distribution, and outcome. Clin Infect Dis 38:S149-S156. https://doi.org/10.1086/381581.
4. Public Health Agency of Canada. 2012. National Enteric Surveillance Program (NESP) annual report 2012. http://publications.gc.ca/collections/collection-2014/aspc-phac/HP37-15-2012-eng.pdf.
5. Currie A, MacDougall L, Aramini J, Gaulin C, Ahmed R, Isaacs S. 2005. Frozen chicken nuggets and strips and eggs are leading risk factors for Salmonella Heidelberg infections in Canada. Epidemiol Infect 133:809-816. https://doi.org/10.1017/S0950268805004383.
6. Parmley EJ, Pintar K, Majowicz S, Avery B, Cook A, Jokinen C, Gannon V, Lapen DR, Topp E, Edge TA, Gilmour M, Pollari F, Reid-Smith R, Irwin R. 2013. A Canadian application of One Health: integration of Salmonella data from various Canadian surveillance programs (2005-2010). Foodborne Pathog Dis 10:747-756. https://doi.org/10.1089/fpd.2012.1438.
7. Seiffert SN, Hilty M, Perreten V, Endimiani A. 2013. Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health? Drug Resist Updat 16:22-45. https://doi.org/10.1016/j.drup.2012.12.001.
8. Public Health Agency Canada. 2013. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) annual report - design and methods. http://publications.gc.ca/collections/collection-2015/aspc-phac/HP2-4-2013-1-eng.pdf.
9. Dutil L, Irwin R, Finley R, Ng LK, Avery B, Boerlin P, Bourgault AM, Cole L, Daignault D, Desruisseau A, Demczuk W, Hoang L, Horsman GB, Ismail J, Jamieson F, Maki A, Pacagnella A, Pillai DR. 2010. Ceftiofur resistance in Salmonella enterica serovar Heidelberg from chicken meat and humans, Canada. Emerg Infect Dis 16:48-54. https://doi.org/10.3201/eid1601.090729.
10. Federal Drug Administration. 2003. Merck's Mefoxin (cefoxitin for injection). http://www.fda.gov/ohrms/dockets/dailys/03/jun03/060403/03p-0227-cp00001-03-exhibit-b-vol1.pdf.
11. Hawkey PM. 1998. The origins and molecular basis of antibiotic resistance. BMJ 317:657-660. https://doi.org/10.1136/bmj.317.7159.657.
12. Jacoby GA, Munoz-Price LS. 2005. The new beta-lactamases. N Engl J Med 352:380-391. https://doi.org/10.1056/NEJMra041359.
13. Miriagou V, Tassios PT, Legakis NJ, Tzouvelekis LS. 2004. Expanded-spectrum cephalosporin resistance in non-typhoid Salmonella. Int J Antimicrob Agents 23:547-555. https://doi.org/10.1016/j.ijantimicag.2004.03.006.
14. Jacoby GA. 2009. AmpC beta-lactamases. Clin Microbiol Rev 22:161-182. https://doi.org/10.1128/CMR.00036-08.
15. Mataseje LF, Xiao J, Kost S, Ng LK, Doré K, Mulvey MR. 2009. Characterization of Canadian cefoxitin-resistant non-typhoidal Salmonella isolates, 2005-06. J Antimicrob Chemother 64:723-730. https://doi.org/10.1093/jac/dkp249.
16. Labbé G, Edirmanasinghe R, Ziebell K, Nash JHE, Bekal S, Parmley EJ, Mulvey MR, Johnson RP. 2016. Complete genome and plasmid sequences of three Canadian isolates of Salmonella enterica subsp. enterica serovar Heidelberg from human and food sources. Genome Announc 4:e01526-15. https://doi.org/10.1128/genomeA.01526-15.
17. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV. 2012. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640-2644. https://doi.org/10.1093/jac/dks261.
18. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko DA, Fedorka-Cray PJ, Pedroso A, Whichard JM, LeClerc JE, White DG, Cebula TA, Ravel J. 2009. Antimicrobial resistance-conferring plasmids with similarity to virulence plasmids from avian pathogenic Escherichia coli strains in Salmonella enterica serovar Kentucky isolates from poultry. Appl Environ Microbiol 75:5963-5971. https://doi.org/10.1128/AEM.00786-09.
19. Laxminarayan R, Duse A, Wattal C, Zaidi AKM, Wertheim HFL, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H, Greko C, So AD, Bigdeli M, Tomson G, Woodhouse W, Ombaka E, Peralta AQ, Qamar FN, Mir F, Kariuki S, Bhutta ZA, Coates A, Bergstrom R, Wright GD, Brown ED, Cars O. 2013. Antibiotic resistance-the need for global solutions. Lancet Infect Dis 13:1057-1098. https://doi.org/10.1016/S1473-3099(13)70318-9.
20. Bekal S, Berry C, Reimer AR, Van Domselaar G, Beaudry G, Fournier E, Doualla-Bell F, Levac E, Gaulin C, Ramsay D, Huot C, Walker M, Sieffert C, Tremblay C. 2016. Usefulness of high-quality core genome single-nucleotide variant analysis for subtyping the highly clonal and the most prevalent Salmonella enterica serovar Heidelberg clone in the context of outbreak investigations. J Clin Microbiol 54:289-295. https://doi.org/10.1128/JCM.02200-15.
21. 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:e87991. https://doi.org/10.1371/journal.pone.0087991.
22. de Toro M, García P, Rodríguez I, Rojo-Bezares B, Helmuth R, Sáenz Y, Rodicio MR, Guerra B, Torres C. 2013. Characterisation of plasmids implicated in the mobilisation of extended-spectrum and AmpC beta-lactamase genes in clinical Salmonella enterica isolates and temporal stability of the resistance genotype. Int J Antimicrob Agents 42:167-172. https://doi.org/10.1016/j.ijantimicag.2013.04.016.
23. Public Health Agency of Canada. 2015. Foodbook report. http://healthycanadians.gc.ca/publications/eating-nutrition/foodbook-2015/index-eng.php.
24. 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(Database issue):D325-D328.
25. Naseer U, Haldorsen B, Simonsen GS, Sundsfjord A. 2010. Sporadic occurrence of CMY-2-producing multidrug-resistant Escherichia coli of ST-complexes 38 and 448, and ST131 in Norway. Clin Microbiol Infect 16:171-178. https://doi.org/10.1111/j.1469-0691.2009.02861.x.
26. Clinical and Laboratory Standards Institute. 2012. Performance standards for antimicrobial susceptibility testing; twenty-second informational supplement. M100-S22. Clinical and Laboratory Standards Institute, Wayne, PA.
27. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-9th ed. M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
28. Mataseje LF, Boyd DA, Willey BM, Prayitno N, Kreiswirth N, Gelosia A, Poutanen SM, Low DE, Jenkins SG, Katz K, Mulvey MR. 2011. Plasmid comparison and molecular analysis of Klebsiella pneumoniae harbouring bla(KPC) from New York City and Toronto. J Antimicrob Chemother 66:1273-1277. https://doi.org/10.1093/jac/dkr092.
29. Centers for Disease Control and Prevention. 2013. Pulsed-field gel electrophoresis (PFGE). http://www.cdc.gov/pulsenet/pathogens/pfge.html.
30. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. 2011. PHAST: a fast phage search tool. Nucleic Acids Res 39(Web Server issue):W347-W352. https://doi.org/10.1093/nar/gkr485.
31. Dhillon BK, Laird MR, Shay JA, Winsor GL, Lo R, Nizam F, Pereira SK, Waglechner N, McArthur AG, Langille MGI, Brinkman FSL. 2015. Island-Viewer 3: more flexible, interactive genomic island discovery, visualization and analysis. Nucleic Acids Res 43:W104-W108. https://doi.org/10.1093/nar/gkv401.
32. Delcher AL, Phillippy A, Carlton J, Salzberg SL. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30:2478-2483. https://doi.org/10.1093/nar/30.11.2478.
33. Sanger Institute. SMALT. http://www.sanger.ac.uk/science/tools/smalt-0.
34. Garrison E, Marth G. 2012. Haplotype-based variant detection from short-read sequencing. 1207.3907. https://arxiv.org/pdf/1207.3907.pdf.
35. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carrico JA. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13:87. https://doi.org/10.1186/1471-2105-13-87.
36. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455-477. https://doi.org/10.1089/cmb.2012.0021.
37. Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. https://doi.org/10.1093/bioinformatics/btu153.
38. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, Jelsbak L, Sicheritz-Pontén T, Ussery DW, Aarestrup FM, Lund O. 2012. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50:1355-1361. https://doi.org/10.1128/JCM.06094-11.
39. Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O, Villa L, Aarestrup FM, Hasman H. 2014. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58:3895-3903. https://doi.org/10.1128/AAC.02412-14.
40. Galardini M, Biondi EG, Bazzicalupo M, Mengoni A. 2011. CONTIGuator: a bacterial genomes finishing tool for structural insights on draft genomes. Source Code Biol Med 6:11. https://doi.org/10.1186/1751-0473-6-11.
41. Petkau A, Stuart-Edwards M, Stothard P, Van Domselaar G. 2010. Interactive microbial genome visualization with GView. Bioinformatics 26:3125-3126. https://doi.org/10.1093/bioinformatics/btq588.
42. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ, Tomita T, Zobel J, Holt KE. 2014. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 6:90. https://doi.org/10.1186/s13073-014-0090-6.