1887

Abstract

Purpose. Antimicrobial resistance (AMR) profiles of 754 strains of Shigella dysenteriae isolated between 2004 and 2017 from UK travellers reporting symptoms of gastrointestinal (GI) disease were reviewed to look for evidence of emerging AMR associated with travellers’ diarrhoea.

Methodology. A travel history was provided for 72.7 % (548/754) of cases, of which 90.9 % (498/548) reported travel outside the UK within 7 days of onset of symptoms, and 9.1 % (50/498) reported no travel in that time frame. During the course of this study, whole genome sequencing (WGS) was implemented for GI disease surveillance, and we compared phenotypic AMR profiles with those derived from WGS data (n=133).

Results/Key findings. The phenotypic and genotypic AMR results correlated well, with 90.1 % (121/133) isolates having concordant results to 10 classes of antimicrobials. Resistance to the first-line drugs commonly used in the treatment of shigellosis was observed throughout the study (ampicillin, 54.1%; chloramphenicol, 33.7 %; sulphonamides, 76.0 %; trimethoprim, 80.0%). Between 2004 and 2017, resistance to all classes of antimicrobials (except the phenicols) increased. The proportion of isolates exhibiting reduced susceptibility to ciprofloxacin increased from 3.8 % in 2004 to 75.7 % in 2017, and this was significantly associated with cases reporting travel to Asia compared to Africa (P<0.001). Of the 201 sequenced isolates, 3.0 % (20/201) had either bla CTX-M-15 or bla CMY-4.

Conclusions. Increasing MDR, along with resistance to the fluroquinolones and the third generation cephalosporins, in Shigella dysenteriae causing travellers’ diarrhoea provides further evidence for the need to regulatethe use of antimicrobial agents and continuous monitoring of emerging AMR.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000779
2018-06-29
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/67/8/1022.html?itemId=/content/journal/jmm/10.1099/jmm.0.000779&mimeType=html&fmt=ahah

References

  1. Njamkepo E, Fawal N, Tran-Dien A, Hawkey J, Strockbine N et al. Global phylogeography and evolutionary history of Shigella dysenteriae type 1. Nat Microbiol 2016;1:16027 [CrossRef][PubMed]
    [Google Scholar]
  2. Livio S, Strockbine NA, Panchalingam S, Tennant SM, Barry EM et al. Shigella isolates from the global enteric multicenter study inform vaccine development. Clin Infect Dis 2014;59:933–941 [CrossRef][PubMed]
    [Google Scholar]
  3. Chattaway MA, Schaefer U, Tewolde R, Dallman TJ, Jenkins C. Identification of Escherichia coli and Shigella species from whole-genome sequences. J Clin Microbiol 2017;55:616–623 [CrossRef][PubMed]
    [Google Scholar]
  4. Ewing WH. The genus Escherichia and the genus Shigella. Edwards and Ewing’s Identification of Enterobacteriaceae, 4th ed. New York: Elsevier Science Publishing Co., Inc; 1986; pp.93–172
    [Google Scholar]
  5. Bopp CA, Brenner FW, Fields PL, Wells JG, Strockbine NA et al. Escherichia, Shigella, and Salmonella. In Murray PR, Baron EJ, Jorgensen JH, Pfaller MA, Yolken RH. (editors) Manual of Clinical Microbiology, 8th ed. Washington, DC: Murray and others American Society for Microbiology; 2003; pp.654–671
    [Google Scholar]
  6. Talukder KA, Mondol AS, Islam MA, Islam Z, Dutta DK et al. A novel serovar of Shigella dysenteriae from patients with diarrhoea in Bangladesh. J Med Microbiol 2007;56:654–658 [CrossRef][PubMed]
    [Google Scholar]
  7. Hawker J, Begg N, Blair I, Reintjes R, Weinberg J et al. Communicable Disease Control and Health Protection Handbook, 3rd ed. West Sussex, UK: Wiley-Blackwell; 2012
    [Google Scholar]
  8. Christopher PR, David KV, John SM, Sankarapandian V. Antibiotic therapy for Shigella dysentery. Cochrane Database Syst Rev 2010;8:CD006784
    [Google Scholar]
  9. Chung The H, Rabaa MA, Pham Thanh D, de Lappe N, Cormican M et al. South Asia as a reservoir for the global spread of ciprofloxacin-resistant Shigella sonnei: a cross-sectional study. PLoS Med 2016;13:e1002055 [CrossRef][PubMed]
    [Google Scholar]
  10. Arcilla MS, van Hattem JM, Haverkate MR, Bootsma MCJ, van Genderen PJJ et al. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect Dis 2017;17:78–85 [CrossRef][PubMed]
    [Google Scholar]
  11. Dallman TJ, Chattaway MA, Mook P, Godbole G, Crook PD et al. Use of whole-genome sequencing for the public health surveillance of Shigella sonnei in England and Wales, 2015. J Med Microbiol 2016;65:882 [CrossRef][PubMed]
    [Google Scholar]
  12. Chattaway MA, Greig DR, Gentle A, Hartman HB, Dallman TJ et al. Whole-genome sequencing for national surveillance of Shigella flexneri. Front Microbiol 2017;8:8 [CrossRef][PubMed]
    [Google Scholar]
  13. Ashton PM, Nair S, Peters TM, Bale JA, Powell DG et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 2016;4:e1752 [CrossRef][PubMed]
    [Google Scholar]
  14. Nascimento DV, Day MR, Doumith M, Hopkins KL, Woodford N et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of enteroaggregative Escherichia coli isolated from cases of diarrhoeal disease in England, 2015–16. J Antimicrob Chemother 2017;72:3288–3297
    [Google Scholar]
  15. Sadouki Z, Day MR, Doumith M, Chattaway MA, Dallman TJ et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Shigella sonnei isolated from cases of diarrhoeal disease in England and Wales, 2015. J Antimicrob Chemother 2017;72:2496–2502
    [Google Scholar]
  16. 5 Day MR, Doumith M, Nascimento D V, Nair S, Ashton PM et al. Comparison of phenotypic and WGS-derived antimicrobial resistance profiles of Salmonella enterica serovars Typhi and Paratyphi. J Antimicrob Chemother 2017
    [Google Scholar]
  17. Gross RJ, Rowe B. Serotyping of Escherichia coli. In Sussman M. (editor) The Virulence of Escherichia coli: Reviews and Methods (Special Publication of the Society for General Microbiology No. 13 London: Academic Press; 1985; pp.345–360
    [Google Scholar]
  18. Liu B, Knirel YA, Feng L et al. Structure and genetics of Shigella O antigens. FEMS Microbiol Rev 2008;32:627–653
    [Google Scholar]
  19. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357–359
    [Google Scholar]
  20. Connor P, Porter CK, Swierczewski B, Riddle MS. Diarrhoea during military deployment: current concepts and future directions. Curr Opin Infect Dis 2012;25:546–554 [CrossRef][PubMed]
    [Google Scholar]
  21. Shakya G, Acharya J, Adhikari S, Rijal N. Shigellosis in Nepal: 13 years review of nationwide surveillance. J Health Popul Nutr 2016;35:36
    [Google Scholar]
  22. Ghosh S, Pazhani GP, Chowdhury G, Guin S, Dutta S et al. Genetic characteristics and changing antimicrobial resistance among Shigella spp. isolated from hospitalized diarrhoeal patients in Kolkata, India. J Med Microbiol 2011;60:1460–1466
    [Google Scholar]
  23. Mandal JVG, Emelda JSM, Parija SC. The Recent Trends of Shigellosis: a JIPMER perspective. J Clin Diagn Res 2012;6:1474–1477
    [Google Scholar]
  24. Das SK, Ahmed S, Ferdous F, Farzana FD, Chisti MJ et al. Changing emergence of Shigella sero-groups in Bangladesh: observation from four different diarrheal disease hospitals. PLoS One 2013;8:e62029
    [Google Scholar]
  25. Taneja N, Mewara A. Shigellosis: epidemiology in India. Indian J Med Res 2016;143:565–576
    [Google Scholar]
  26. Njuguna HN, Cosmas L, Williamson J, Nyachieo D, Olack B et al. Use of population-based surveillance to define the high incidence of shigellosis in an urban slum in Nairobi, Kenya. PLoS One 2013;8:e58437
    [Google Scholar]
  27. Talukder KA, Islam MA, Khajanchi BK, Dutta DK, Islam Z et al. Temporal shifts in the dominance of serotypes of Shigella dysenteriae from 1999 to 2002 in Dhaka, Bangladesh. J Clin Microbiol 2003;41:5053–5058
    [Google Scholar]
  28. Talukder KA, Khajanchi BK, Islam MA, Dutta DK, Islam Z et al. The emerging strains of Shigella dysenteriae type 2 in Bangladesh are clonal. Epidemiol Infect 2006;134:1249–1256
    [Google Scholar]
  29. Jenkins C. Whole-genome sequencing data for serotyping Escherichia coli-it's time for a Change!. J Clin Microbiol 2015;53:2402–2403
    [Google Scholar]
  30. Tyson GH, McDermott PF, Li C et al. WGS accurately predicts antimicrobial resistance in Escherichia coli. J Antimicrob Chemother 2015;70:2763–2769
    [Google Scholar]
  31. Sack BR, Rahman M, Yunus M, Khan HE. Antimicrobial resistance in organisms causing diarrheal disease. Clin Infect Dis 1997;24:S102–105
    [Google Scholar]
  32. Bennish ML, Salam MA, Hossain MA, Myaux J, Khan EH et al. Antimicrobial resistance of Shigella isolates in Bangladesh, 1983–1990: increasing frequency of strains multiply resistant to ampicillin, trimethoprimsulfamethoxazole, and nalidixic acid. Clin Infect Dis 1992;14:1055–1060
    [Google Scholar]
  33. Khan AI, Huq S, Malek MA, Hossain MI, Talukder KA et al. Shigella serotypes among hospitalized patients in urban Bangladesh and their antimicrobial resistance. Epidemiol Infect 2004;132:773–777
    [Google Scholar]
  34. Pazhani GP, Niyogi SK, Singh AK, Sen B, Taneja N et al. Molecular characterization of multidrug-resistant Shigella species isolated from epidemic and endemic cases of shigellosis in India. J Med Microbiol 2008;57:856–863
    [Google Scholar]
  35. Taneja N, Lyngdoh V, Vermani A, Mohan B, Rao P et al. Re-emergence of multi-drug resistant Shigella dysenteriae with added resistance to ciprofloxacin in north India & their plasmid profiles. Indian J Med Res 2005;122:348–354[PubMed]
    [Google Scholar]
  36. Khan S, Singh P, Ansari M, Asthana A. Isolation of Shigella species and their resistance patterns to a panel of fifteen antibiotics in mid and far western region of Nepal. Asian Pac J Trop Dis 2014;4:30–34
    [Google Scholar]
  37. Mensa L, Marco F, Vila J, Gascón J, Ruiz J. Quinolone resistance among Shigella spp. isolated from travellers returning from India. Clin Microbiol Infect 2008;14:279–281
    [Google Scholar]
  38. Sur D et al. Shigellosis: challenges and management issues. Indian J Med Res 2004;120:454–462
    [Google Scholar]
  39. Pons MJ, Gomes C, Martínez-Puchol S, Ruiz L, Mensa L et al. Antimicrobial resistance in Shigella spp. causing traveller's diarrhoea (1995–2010): a retrospective analysis. Travel Med Infect Dis 2013;11:315–319
    [Google Scholar]
  40. Tribble DR. Resistant pathogens as causes of traveller's diarrhea globally and impact(s) on treatment failure and recommendations. J Travel Med 2017;24:S6–S12
    [Google Scholar]
  41. Kotloff KL, Riddle MS, Platts-Mills JA, Pavlinac P, Zaidi AKM. Shigellosis. Lancet 2017;6736:33296–33298
    [Google Scholar]
  42. Goel N, Wattal C, Kaul D, Khanna VK. Emergence of ceftriaxone resistant Shigella. Indian J Paediatr 2013;80:70–71
    [Google Scholar]
  43. Tham J, Odenholt I, Walder M, Brolund A, Ahl J et al. Extended-spectrum beta-lactamase-producing Escherichia coli in patients with travellers' diarrhoea. Scand J Infect Dis 2010;42:275–280
    [Google Scholar]
  44. Taylor DN, Hamer DH, Shlim DR. Medications for the prevention and treatment of traveller’s diarrhoea. J Travel Med 2017;24:S17–S22
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000779
Loading
/content/journal/jmm/10.1099/jmm.0.000779
Loading

Data & Media loading...

Supplements

Supplementary File 2

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