1887

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Volume 70, Issue 8

Editor's Choice Increasingly limited options for the treatment of enteric fever in travellers returning to England, 2014–2019: a cross-sectional analytical study Open Access

Abstract

Enteric fever (caused by serovars Typhi and Paratyphi) frequently presents as an acute, undifferentiated febrile illness in returning travellers, requiring timely empirical antibiotics.

Determining which empirical antibiotics to prescribe for enteric fever requires up-to-date knowledge of susceptibility patterns.

By characterising factors associated with antimicrobial resistance in cases of . Typhi and . Paratyphi imported to England, we aim to guide effective empirical treatment.

All English isolates of . Typhi and . Paratyphi 2014–2019 underwent antimicrobial susceptibility testing; results were compared to a previous survey in London 2005–2012. Risk factors for antimicrobial resistance were analysed with logistic regression models to predict adjusted odds ratios (aOR) for resistance to individual antibiotics and multi-drug resistance.

We identified 1088 cases of . Typhi, 729 . Paratyphi A, 93 . Paratyphi B, and one . Paratyphi C. In total, 93 % were imported. Overall, 90 % of . Typhi and 97 % of . Paratyphi A isolates were resistant to ciprofloxacin; 26 % of . Typhi were multidrug resistant to ciprofloxacin, amoxicillin, co-trimoxazole, and chloramphenicol (MDR+FQ). Of the isolates, 4 % of . Typhi showed an extended drug resistance (XDR) phenotype of MDR+FQ plus resistance to third-generation cephalosporins, with cases of XDR rising sharply in recent years (none before 2017, one in 2017, six in 2018, 32 in 2019). For . Typhi isolates, resistance to ciprofloxacin was associated with travel to Pakistan (aOR=32.0, 95 % CI: 15.4–66.4), India (aOR=21.8, 95 % CI: 11.6–41.2), and Bangladesh (aOR=6.2, 95 % CI: 2.8–13.6) compared to travel elsewhere, after adjusting for rising prevalence of resistance over time. MDR+FQ resistance in . Typhi isolates was associated with travel to Pakistan (aOR=3.5, 95 % CI: 2.4–5.2) and less likely with travel to India (aOR=0.07, 95 % CI 0.04–0.15) compared to travel elsewhere. All XDR cases were imported from Pakistan. No isolate was resistant to azithromycin. Comparison with the 2005–2012 London survey indicates substantial increases in the prevalence of resistance of . Typhi isolates to ciprofloxacin associated with travel to Pakistan (from 79–98 %) and Africa (from 12–60 %).

Third-generation cephalosporins and azithromycin remain appropriate choices for empirical treatment of enteric fever in most returning travellers to the UK from endemic countries, except from Pakistan, where XDR represents a significant risk.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Antimicrobial resistance , Enteric fever , Paratyphoid , Travel medicine and Typhoid
Funding
This study was supported by the:
  • Public Health England
    • Principle Award Recipient: NotApplicable
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-08-05
2024-04-24
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References

  1. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: Systematic review to estimate global morbidity and mortality for 2010. J Glob Health 2012; 2:010401 [View Article] [PubMed]
     [Google Scholar]
  2. Typhoid GBD, Paratyphoid C. The global burden of typhoid and paratyphoid fevers: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 2019; 19:369–381 [View Article] [PubMed]
     [Google Scholar]
  3. Appiah GD, Chung A, Bentsi-Enchill AD, Kim S, Crump JA et al. Typhoid outbreaks, 1989-2018: Implications for prevention and control. Am J Trop Med Hyg 2020; 102:1296–1305 [View Article] [PubMed]
     [Google Scholar]
  4. Jensenius M, Han PV, Schlagenhauf P, Schwartz E, Parola P. Acute and potentially life-threatening tropical diseases in western travelers--a GeoSentinel multicenter study, 1996-2011. Am J Trop Med Hyg 2013; 88:397–404 [View Article] [PubMed]
     [Google Scholar]
  5. Browne AJ, Kashef Hamadani BH, Kumaran EAP, Rao P, Longbottom J. Drug-resistant enteric fever worldwide, 1990 to 2018: A systematic review and meta-analysis. BMC Med 2020; 18:1 [View Article] [PubMed]
     [Google Scholar]
  6. Barkume C, Date K, Saha SK, Qamar FN, Sur D et al. Phase I of the surveillance for enteric fever in Asia Project (SEAP): An overview and lessons learned. J Infect Dis 2018; 218:S188–S194 [View Article] [PubMed]
     [Google Scholar]
  7. Crump JA, Mintz ED. Global trends in typhoid and paratyphoid Fever. Clin Infect Dis 2010; 50:241–246 [View Article] [PubMed]
     [Google Scholar]
  8. International Typhoid C, Wong VK, Holt KE, Okoro C, Baker S et al. Molecular surveillance identifies multiple transmissions of typhoid in West Africa. PLOS Negl Trop Dis 2016; 10:e0004781
     [Google Scholar]
  9. Britto CD, Wong VK, Dougan G, Pollard AJ. A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Negl Trop Dis 2018; 12:e0006779 [View Article]
     [Google Scholar]
  10. Al-Emran HM, Eibach D, Krumkamp R, Ali M, Baker S et al. A multicountry molecular analysis of Salmonella enterica serovar typhi with reduced susceptibility to ciprofloxacin in sub-saharan Africa. Clin Infect Dis 2016; 62:S42–46 [View Article] [PubMed]
     [Google Scholar]
  11. Gonzalez-Lopez JJ, Piedra-Carrasco N, Salvador F, Rodriguez V, Sanchez-Montalva A. ESBL-producing Salmonella enterica serovar Typhi in traveler returning from Guatemala to Spain. Emerg Infect Dis 2014; 20:1918–1920 [View Article] [PubMed]
     [Google Scholar]
  12. Pokharel BM, Koirala J, Dahal RK, Mishra SK, Khadga PK. Multidrug-resistant and extended-spectrum beta-lactamase (ESBL)-producing Salmonella enterica (serotypes Typhi and Paratyphi A) from blood isolates in Nepal: surveillance of resistance and a search for newer alternatives. Int J Infect Dis 2006; 10:434–438 [View Article] [PubMed]
     [Google Scholar]
  13. Chatham-Stephens K, Medalla F, Hughes M, Appiah GD, Aubert RD et al. Emergence of extensively Drug-resistant Salmonella typhi infections among travelers to or from Pakistan - United States, 2016-2018. MMWR Morb Mortal Wkly Rep 2019; 68:11–13 [View Article] [PubMed]
     [Google Scholar]
  14. Achtman M, Wain J, Weill FX, Nair S, Zhou Z. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica . PLoS Pathog 2012; 8:e1002776 [View Article] [PubMed]
     [Google Scholar]
  15. Chattaway MA, Dallman TJ, Larkin L, Nair S, McCormick J et al. The transformation of reference microbiology methods and surveillance for salmonella with the use of whole genome sequencing in England and Wales. Front Public Health 2019; 7:317 [View Article] [PubMed]
     [Google Scholar]
  16. ECDC European Centre for Disease Prevention and Control. Eu Protocol for Harmonised Monitoring of Antimicrobial Resistance in Human Salmonella and Campylobacter Isolates – June 2016 Stockholm: ECDC; 2016
     [Google Scholar]
  17. Howe RA, Andrews JM, BWPoS T. BSAC standardized disc susceptibility testing method (version 11. J Antimicrob Chemother 2012; 67:2783–2784 [View Article] [PubMed]
     [Google Scholar]
  18. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of mics and zone diameters version ; 2019; 9
  19. World Health Organization Background document: the diagnosis, treatment and prevention of typhoid fever; 2003 https://www.glowm.com/pdf/WHO-diagnosis%20treatment%20prevention%20of%20typhoid%20fever-2003-CustomLicense.pdf
  20. Freedman J, Lighton L, Jones J. Defining travel-associated cases of enteric fever. J Infect Public Health 2014; 7:377–385 [View Article] [PubMed]
     [Google Scholar]
  21. Ministry of Housing CLG The English Indices of Deprivation 2019: Technical Report London: 2019
     [Google Scholar]
  22. Dave J, Warburton F, Freedman J, de Pinna E, Grant K. What were the risk factors and trends in antimicrobial resistance for enteric fever in London 2005-2012?. J Med Microbiol 2017; 66:698–705 [View Article] [PubMed]
     [Google Scholar]
  23. Godbole G, McCann N, Jones SM, Dallman TJ, Brown M. Ceftriaxone-resistant Salmonella typhi in a traveller returning from a mass gathering in Iraq. The Lancet Infectious Diseases 2019; 19:467 [View Article]
     [Google Scholar]
  24. Threlfall EJ, Ward LR, Skinner JA, Smith HR, Lacey S. Ciprofloxacin-resistant Salmonella typhi and treatment failure. Lancet 1999; 353:1590–1591 [View Article] [PubMed]
     [Google Scholar]
  25. Cooke FJ, Wain J, Threlfall EJ. Fluoroquinolone resistance in Salmonella typhi . BMJ 2006; 333:353–354 [View Article] [PubMed]
     [Google Scholar]
  26. Rasheed F, Saeed M, Alikhan NF, Baker D, Khurshid M et al. Emergence of resistance to fluoroquinolones and third-generation cephalosporins in Salmonella typhi in Lahore, Pakistan. medRxiv 2020
     [Google Scholar]
  27. Nair S, Day M, Godbole G, Saluja T, Langridge GC et al. Genomic surveillance detects Salmonella enterica serovar Paratyphi A harbouring blaCTX-M-15 from a traveller returning from Bangladesh. PLoS One 2020; 15:e0228250
     [Google Scholar]
  28. Leder K, Torresi J, Libman MD, Cramer JP, Castelli F. GeoSentinel surveillance of illness in returned travelers, 2007-2011. Ann Intern Med 2013; 158:456–468 [View Article] [PubMed]
     [Google Scholar]
  29. Ashley EA, Recht J, Chua A, Dance D, Dhorda M. An inventory of supranational antimicrobial resistance surveillance networks involving low- and middle-income countries since 2000. J Antimicrob Chemother 2018; 73:1737–1749 [View Article] [PubMed]
     [Google Scholar]
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Increasingly limited options for the treatment of enteric fever in travellers returning to England, 2014–2019: a cross-sectional analytical study
J. Med. Microbiol. 70, 001359 (2021); https://doi.org/10.1099/jmm.0.001359
/content/journal/jmm/10.1099/jmm.0.001359
/content/journal/jmm/10.1099/jmm.0.001359
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