1887

Abstract

In 2013, an unusual increase in the number of Salmonella enterica serotype Paratyphi A (Salmonella Paratyphi A) infections was reported in patients in Phnom Penh, Cambodia, and in European, American and Japanese travellers returning from Cambodia. Epidemiological investigations did not identify a common source of exposure. To analyse the population structure and genetic diversity of these Salmonella Paratyphi A isolates, we used whole-genome sequencing on 65 isolates collected from 1999 to 2014: 55 from infections acquired in Cambodia and 10 from infections acquired in other countries in Asia, Africa and Europe. Short-read sequences from 80 published genomes from around the world and from 13 published genomes associated with an outbreak in China were also included. Pulsed-field gel electrophoresis (PFGE) was performed on a subset of isolates. Genomic analyses were found to provide much more accurate information for tracking the individual strains than PFGE. All but 2 of the 36 isolates acquired in Cambodia during 2013–2014 belonged to the same clade, C5, of lineage C. This clade has been isolated in Cambodia since at least 1999. The Chinese outbreak isolates belonged to a different clade (C4) and were resistant to nalidixic acid, whereas the Cambodian outbreak isolates displayed pan-susceptibility to antibiotics. Since 2014, the total number of cases has decreased, but there has been an increase in the frequency with which nalidixic acid-resistant C5 isolates are isolated. The frequency of these isolates should be monitored over time, because they display decreased susceptibility to ciprofloxacin, the first-choice antibiotic for treating paratyphoid fever.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000092
2016-11-30
2021-07-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/2/11/mgen000092.html?itemId=/content/journal/mgen/10.1099/mgen.0.000092&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  2. Ashton P. M., Nair S., Peters T. M., Bale J. A., Powell D. G., Painset A., Tewolde R., Schaefer U., Jenkins C. et al. 2016; Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 4:e1752 [View Article][PubMed]
    [Google Scholar]
  3. Baele G., Lemey P., Bedford T., Rambaut A., Suchard M. A., Alekseyenko A. V. 2012; Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157–2167 [View Article][PubMed]
    [Google Scholar]
  4. Baele G., Li W. L., Drummond A. J., Suchard M. A., Lemey P. 2013; Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 30:239–243 [View Article][PubMed]
    [Google Scholar]
  5. Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., Lesin V. M., Nikolenko S. I., Pham S. et al. 2012; SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477 [View Article][PubMed]
    [Google Scholar]
  6. Bhan M. K., Bahl R., Bhatnagar S. 2005; Typhoid and paratyphoid fever. Lancet 366:749–762 [View Article][PubMed]
    [Google Scholar]
  7. CA-SFM & EUCAST 2014; Comité de l’Antibiogramme de la Société Française de Microbiologie Recommandations 2014. http://www.sfm-microbiologie.org/UserFiles/files/casfm/CASFM_EUCAST_2014_V2_0.pdf
  8. Croucher N. J., Page A. J., Connor T. R., Delaney A. J., Keane J. A., Bentley S. D., Parkhill J., Harris S. R. 2015; Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 43:e15 [View Article][PubMed]
    [Google Scholar]
  9. Drummond A. J., Rambaut A. 2007; BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7,:214 [View Article][PubMed]
    [Google Scholar]
  10. ECDC 2013; Annual Epidemiological Report: Reporting on 2011 Surveillance Data and 2012 Epidemic Intelligence Data. Stockholm: European Centre for Disease Prevention and Control. http://ecdc.europa.eu/en/publications/Publications/annual-epidemiological-report-2013.pdf
  11. Grimont P. A., Weill F. X 2007; Antigenic formulae of the Salmonella serotypes, 9th edn. WHO Collaborating Centre for Reference and Research on Salmonella – Institut Pasteur, Paris, France. https://www.pasteur.fr/sites/www.pasteur.fr/files/wklm_en.pdf.
  12. Gu W., Yang Z., Chen Y., Yin J., Yang J., Li C., Zhou Y., Yin J., Xu W. et al. 2015; Molecular characteristics of Salmonella enterica Paratyphi A in Yunnan province, Southwest China. Infect Genet Evol 30:181–185 [View Article][PubMed]
    [Google Scholar]
  13. Judd M. C., Grass J. E., Mintz E. D., Bicknese A., Mahon B. E. 2015; Salmonella enterica Paratyphi A infections in travelers returning from Cambodia, United States. Emerg Infect Dis 21:1089–1091 [View Article]
    [Google Scholar]
  14. Karkey A., Thompson C. N., Tran Vu Thieu N., Dongol S., Le Thi Phuong T., Voong Vinh P., Arjyal A., Martin L. B., Rondini S. et al. 2013; Differential epidemiology of Salmonella Typhi and Paratyphi A in Kathmandu, Nepal: a matched case control investigation in a highly endemic enteric fever setting. PLoS Negl Trop Dis 7:e2391 [View Article][PubMed]
    [Google Scholar]
  15. Langmead B., Salzberg S. L. 2012; Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359 [View Article][PubMed]
    [Google Scholar]
  16. Le Hello S., Harrois D., Bouchrif B., Sontag L., Elhani D., Guibert V., Zerouali K., Weill F. X. 2013; Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: a microbiological study. Lancet Infect Dis 13:672–679 [View Article][PubMed]
    [Google Scholar]
  17. Leekitcharoenphon P., Nielsen E. M., Kaas R. S., Lund O., Aarestrup F. M. 2014; Evaluation of whole genome sequencing for outbreak detection of Salmonella enterica . PLoS One 9:e87991 [View Article][PubMed]
    [Google Scholar]
  18. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. et al. 2009; The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  19. McClelland M., Sanderson K. E., Clifton S. W., Latreille P., Porwollik S., Sabo A., Meyer R., Bieri T., Ozersky P. et al. 2004; Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet 36:1268–1274 [View Article][PubMed]
    [Google Scholar]
  20. Newton A. E., Routh J. A., Mahon B. E. 2016; Infectious diseases related to travel: typhoid & paratyphoid fever. In CDC Health Information for International Travel Edited by Brunette G. W. New York: Oxford University Press;
    [Google Scholar]
  21. Ochiai R. L., Wang X., von Seidlein L., Yang J., Bhutta Z. A., Bhattacharya S. K., Agtini M., Deen J. L., Wain J. et al. 2005; Salmonella Paratyphi A rates, Asia. Emerg Infect Dis 11:1764–1766 [View Article][PubMed]
    [Google Scholar]
  22. Page A. J., Cummins C. A., Hunt M., Wong V. K., Reuter S., Holden M. T., Fookes M., Falush D., Keane J. A., Parkhill J. 2015; Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31:3691–3693 [View Article][PubMed]
    [Google Scholar]
  23. Ribot E. M., Fair M. A., Gautom R., Cameron D. N., Hunter S. B., Swaminathan B., Barrett T. J. 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 [View Article][PubMed]
    [Google Scholar]
  24. Saitoh T., Morita M., Shimada T., Izumiya H., Kanayama A., Oishi K., Ohnishi M., Sunagawa T. 2016; Increase in paratyphoid fever cases in Japanese travellers returning from Cambodia in 2013. Epidemiol Infect 144:602–606 [View Article][PubMed]
    [Google Scholar]
  25. Seemann T. 2014; Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  26. Siguier P., Perochon J., Lestrade L., Mahillon J., Chandler M. 2006; ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32–D36 [View Article][PubMed]
    [Google Scholar]
  27. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013; mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  28. Teh C. S., Chua K. H., Thong K. L. 2014; Paratyphoid fever: splicing the global analyses. Int J Med Sci 11:732–741 [View Article][PubMed]
    [Google Scholar]
  29. Tien Y. Y., Wang Y. W., Tung S. K., Liang S. Y., Chiou C. S. 2011; Comparison of multilocus variable-number tandem repeat analysis and pulsed-field gel electrophoresis in molecular subtyping of Salmonella enterica serovars Paratyphi A. Diagn Microbiol Infect Dis 69:1–6 [View Article][PubMed]
    [Google Scholar]
  30. Tourdjman M., Le Hello S., Gossner C., Delmas G., Tubiana S., Fabre L., Kerléguer A., Tarantola A., Fruth A. et al. 2013; Unusual increase in reported cases of paratyphoid A fever among travellers returning from Cambodia, January to September 2013. Euro Surveill 18,:20594 [View Article][PubMed]
    [Google Scholar]
  31. Vlieghe E., Phe T., De Smet B., Veng C. H., Kham C., Sar D., van Griensven J., Lim K., Thai S. et al. 2013; Increase in Salmonella enterica serovar Paratyphi A infections in Phnom Penh, Cambodia, January 2011 to August 2013. Euro Surveill 18,:20592 [View Article][PubMed]
    [Google Scholar]
  32. Vollaard A. M., Ali S., van Asten H. A., Widjaja S., Visser L. G., Surjadi C., van Dissel J. T. 2004; Risk factors for typhoid and paratyphoid fever in Jakarta, Indonesia. JAMA 291:2607–2615 [View Article][PubMed]
    [Google Scholar]
  33. Weill F. X, Bertrand S., Guesnier F., Baucheron S., Cloeckaert A., Grimont P. A. 2006; Ciprofloxacin-resistant Salmonella Kentucky in travelers. Emerg Infect Dis 12:1611–1612
    [Google Scholar]
  34. Yan M., Yang B., Wang Z., Wang S., Zhang X., Zhou Y., Pang B., Diao B., Yang R. et al. 2015; A large-scale community-based outbreak of paratyphoid fever caused by hospital-derived transmission in Southern China. PLoS Negl Trop Dis 9:e0003859 [View Article][PubMed]
    [Google Scholar]
  35. Zankari E., Hasman H., Cosentino S., Vestergaard M., Rasmussen S., Lund O., Aarestrup F. M., Larsen M. V. 2012; Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644 [View Article][PubMed]
    [Google Scholar]
  36. Zhou Z., McCann A., Weill F. X., Blin C., Nair S., Wain J., Dougan G., Achtman M. 2014; Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever. Proc Natl Acad Sci U S A 111:12199–12204 [View Article][PubMed]
    [Google Scholar]
  37. 1. Salmonella enterica subsp. enterica serovar Choleraesuis strain SC-B67 complete genome: GenBank accession number AE017220
  38. 2. Salmonella enterica subsp. enterica serovar Dublin strain CT_02021853 complete genome: GenBank accession number CP001144
  39. 3. Salmonella enterica subsp. enterica serovar Enteritidis strain P125109 complete genome: GenBank accession number AM933172
  40. 4. Salmonella enterica subsp. enterica serovar Gallinarum strain 287/91 complete genome: GenBank accession number AM933173
  41. 5. Salmonella enterica subsp. enterica serovar Heidelberg strain SL476 complete genome: GenBank accession number CP001120
  42. 6. Salmonella enterica subsp. enterica serovar Newport strain SL254 complete genome: GenBank accession number CP001113
  43. 7. Salmonella enterica subsp. enterica serovar Agona strain SL483 complete genome: GenBank accession number CP000886
  44. 8. Salmonella enterica subsp. enterica serovar Paratyphi B strain SPB7 complete genome: GenBank accession number CP001120
  45. 9. Salmonella enterica subsp. enterica serovar Paratyphi C strain RKS4594 complete genome: GenBank accession number CP000857
  46. 10. Salmonella enterica subsp. enterica serovar Schwarzengrund strain CVM19633 complete genome: GenBank accession number CP001127
  47. 11. Salmonella enterica subsp. enterica serovar Typhi strain Ty2 complete genome: GenBank accession number AE014613
  48. 12. Salmonella enterica subsp. enterica serovar Typhimurium strain LT2 complete genome: GenBank accession number AE006468
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000092
Loading
/content/journal/mgen/10.1099/mgen.0.000092
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Supplementary File 2

EXCEL

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error