Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 22, Number 9—September 2016
Research

Travel- and Community-Based Transmission of Multidrug-Resistant Shigella sonnei Lineage among International Orthodox Jewish Communities

Kate S. Baker, Timothy J. Dallman, Adi Behar, François-Xavier Weill, Malika Gouali, Jeremy Sobel, Maria Fookes, Lea Valinsky, Ohad Gal-Mor, Thomas Connor, Israel Nissan, Sophie Bertrand, Julian Parkhill, Claire Jenkins, Dani Cohen, and Nicholas R. ThomsonComments to Author 
Author affiliations: University of Liverpool, Liverpool, UK (K.S. Baker); Wellcome Trust Sanger Institute, Hinxton, UK (K.S. Baker, M. Fookes, J. Parkhill, N.R. Thomson); Public Health England, London, UK (T.J. Dallman, C. Jenkins); Kimron Veterinary Institute, Bet Dagan, Israel (A. Behar); Institut Pasteur, Paris, France (F.X. Weill, M. Gouali); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (J. Sobel); Ministry of Health, Tel Aviv, Israel (L. Valinsky, I. Nissan); Tel Aviv University, Tel Aviv (O. Gal-Mor, D. Cohen); Cardiff University, Cardiff, UK (T.R. Connor); Scientific Institute of Public Health, Brussels, Belgium (S. Bertrand); The London School of Hygiene and Tropical Medicine, London (N.R. Thomson)

Main Article

Table 1

Origins of Shigella sonnei isolates used to track travel- and community-based transmission of multidrug-resistant Shigella sonnei among international Orthodox Jewish communities*

Region/community Country Year(s) Details References No. isolates
Europe OJCs Belgium 2008 Outbreak (22) 3
France 1996–2014 Multiple outbreaks This study, (21) 64

United Kingdom
2006–2014
Multiple outbreaks
This study, (23)
101
Europe non-OJCs
United Kingdom
2008–2014
Matched (time and phage-type) non-OJC cases
This study
45
United States and Canada OJCs
United States
1994–1995
Outbreak
(24)
3
Israel†
Israel
2000–2014
Sentinel laboratory surveillance
This study, (19)
221
Global context
Multiple
1943–2008
Used for background
(16)
118
Total
555
*OJC, Orthodox Jewish communities.
†90% known OJC ethnicity.

Main Article

References
  1. World Health Organization. WHO Global strategy for containment of antimicrobial resistance. Switzerland: The Organization; 2001.
  2. Centers for Disease Control and Prevention. Antibiotic resistance threats in the United States, 2013. Atlanta: US Department of Health and Human Services; 2013 [cited 2016 May 26]. http://www.cdc.gov/drugresistance/threat-report-2013/index.html
  3. van der Bij  AK, Pitout  JD. The role of international travel in the worldwide spread of multiresistant Enterobacteriaceae. J Antimicrob Chemother. 2012;67:2090100. DOIPubMedGoogle Scholar
  4. GBD 2013 Mortality and Causes of Death Collaborators. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;385:11771. DOIPubMedGoogle Scholar
  5. Kotloff  KL, Winickoff  JP, Ivanoff  B, Clemens  JD, Swerdlow  DL, Sansonetti  PJ, Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ. 1999;77:65166.PubMedGoogle Scholar
  6. Kothary  MH, Babu  US. Infective dose of foodborne pathogens in volunteers: a review. J Food Saf. 2001;21:4968. DOIGoogle Scholar
  7. Vinh  H, Baker  S, Campbell  J, Hoang  NV, Loan  HT, Chinh  MT, Rapid emergence of third generation cephalosporin resistant Shigella spp. in Southern Vietnam. J Med Microbiol. 2009;58:2813. DOIPubMedGoogle Scholar
  8. Ashkenazi  S, Levy  I, Kazaronovski  V, Samra  Z. Growing antimicrobial resistance of Shigella isolates. J Antimicrob Chemother. 2003;51:4279. DOIPubMedGoogle Scholar
  9. Kuo  CY, Su  LH, Perera  J, Carlos  C, Tan  BH, Kumarasinghe  G, Antimicrobial susceptibility of Shigella isolates in eight Asian countries, 2001–2004. J Microbiol Immunol Infect. 2008;41:10711.
  10. Vrints  M, Mairiaux  E, Van Meervenne  E, Collard  JM, Bertrand  S. Surveillance of antibiotic susceptibility patterns among Shigella sonnei strains isolated in Belgium during the 18-year period 1990 to 2007. J Clin Microbiol. 2009;47:137985. DOIPubMedGoogle Scholar
  11. Livio  S, Strockbine  NA, Panchalingam  S, Tennant  SM, Barry  EM, Marohn  ME, Shigella isolates from the global enteric multicenter study inform vaccine development. Clin Infect Dis. 2014;59:93341 .DOIGoogle Scholar
  12. Bangtrakulnonth  A, Vieira  AR, Lo Fo Wong  DM, Pornreongwong  S, Pulsrikarn  C, Sawanpanyalert  P, Shigella from humans in Thailand during 1993 to 2006: spatial-time trends in species and serotype distribution. Foodborne Pathog Dis. 2008;5:77384. DOIPubMedGoogle Scholar
  13. Qiu  S, Xu  X, Yang  C, Wang  J, Liang  B, Li  P, Shift in serotype distribution of Shigella species in China, 2003–2013. Clin Microbiol Infect. 2015;21:252.e58 .DOIGoogle Scholar
  14. Banga Singh  KK, Ojha  SC, Deris  ZZ, Rahman  RA. A 9-year study of shigellosis in Northeast Malaysia: antimicrobial susceptibility and shifting species dominance. J Public Health (Bangkok). 2011;19:2316. DOIGoogle Scholar
  15. Vinh  H, Nhu  NT, Nga  TV, Duy  PT, Campbell  JI, Hoang  NV, A changing picture of shigellosis in southern Vietnam: shifting species dominance, antimicrobial susceptibility and clinical presentation. BMC Infect Dis. 2009;9:204. DOIPubMedGoogle Scholar
  16. Holt  KE, Baker  S, Weill  FX, Holmes  EC, Kitchen  A, Yu  J, Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet. 2012;44:10569. DOIPubMedGoogle Scholar
  17. Holt  KE, Thieu Nga  TV, Thanh  DP, Vinh  H, Kim  DW, Vu Tra  MP, Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Natl Acad Sci U S A. 2013;110:175227. DOIPubMedGoogle Scholar
  18. Centers for Disease Control and Prevention. Multistate outbreak of Shigella sonnei gastroenteritis—United States. MMWR Morb Mortal Wkly Rep. 1987;36:4402, 448–9.
  19. Cohen  D, Bassal  R, Goren  S, Rouach  T, Taran  D, Schemberg  B, Recent trends in the epidemiology of shigellosis in Israel. Epidemiol Infect. 2014;142:258394. DOIPubMedGoogle Scholar
  20. Garrett  V, Bornschlegel  K, Lange  D, Reddy  V, Kornstein  L, Kornblum  J, A recurring outbreak of Shigella sonnei among traditionally observant Jewish children in New York City: the risks of daycare and household transmission. Epidemiol Infect. 2006;134:12316. DOIPubMedGoogle Scholar
  21. Boumghar-Bourtchai  L, Mariani-Kurkdjian  P, Bingen  E, Filliol  I, Dhalluin  A, Ifrane  SA, Macrolide-resistant Shigella sonnei. Emerg Infect Dis. 2008;14:12979. DOIPubMedGoogle Scholar
  22. De Schrijver  K, Bertrand  S, Gutierrez Garitano  I, Van den Branden  D, Van Schaeren  J. Outbreak of Shigella sonnei infections in the Orthodox Jewish community of Antwerp, Belgium, April to August 2008. Euro Surveill. 2011;16:19838.
  23. McDonnell  J, Dallman  T, Atkin  S, Turbitt  DA, Connor  TR, Grant  KA, Retrospective analysis of whole genome sequencing compared to prospective typing data in further informing the epidemiological investigation of an outbreak of Shigella sonnei in the UK. Epidemiol Infect. 2013;141:256875. DOIPubMedGoogle Scholar
  24. Sobel  J, Cameron  DN, Ismail  J, Strockbine  N, Williams  M, Diaz  PS, A prolonged outbreak of Shigella sonnei infections in traditionally observant Jewish communities in North America caused by a molecularly distinct bacterial subtype. J Infect Dis. 1998;177:14059. DOIPubMedGoogle Scholar
  25. Ashton  PM, Baker  KS, Gentle  A, Wooldridge  DJ, Thomson  NR, Dallman  TJ, Draft genome sequences of the type strains of Shigella flexneri held at Public Health England: comparison of classical phenotypic and novel molecular assays with whole genome sequence. Gut Pathog. 2014;6:7 .DOIGoogle Scholar
  26. Quail  MA, Kozarewa  I, Smith  F, Scally  A, Stephens  PJ, Durbin  R, A large genome center’s improvements to the Illumina sequencing system. Nat Methods. 2008;5:100510. DOIPubMedGoogle Scholar
  27. Quail  MA, Otto  TD, Gu  Y, Harris  SR, Skelly  TF, McQuillan  JA, Optimal enzymes for amplifying sequencing libraries. Nat Methods. 2011;9:101. DOIPubMedGoogle Scholar
  28. Baker  KS, Dallman  TJ, Ashton  PM, Day  M, Hughes  G, Crook  PD, Intercontinental dissemination of azithromycin-resistant shigellosis through sexual transmission: a cross-sectional study. Lancet Infect Dis. 2015;8:93321. DOIPubMedGoogle Scholar
  29. Croucher  NJ, Page  AJ, Connor  TR, Delaney  AJ, Keane  JA, Bentley  SD, Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43:e15. DOIPubMedGoogle Scholar
  30. Stamatakis  A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:268890. DOIPubMedGoogle Scholar
  31. Drummond  AJ, Rambaut  A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214. DOIPubMedGoogle Scholar
  32. Rambaut  A, Lam  TT, Max Carvalho  L, Pybus  OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evolution. 2016;2:1. DOIGoogle Scholar
  33. Carattoli  A, Zankari  E, Garcia-Fernandez  A, Voldby Larsen  M, Lund  O, Villa  L, In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895903. DOIPubMedGoogle Scholar
  34. Carver  TJ, Rutherford  KM, Berriman  M, Rajandream  MA, Barrell  BG, Parkhill  J. ACT: the Artemis Comparison Tool. Bioinformatics. 2005;21:34223. DOIPubMedGoogle Scholar
  35. Ye  C, Lan  R, Xia  S, Zhang  J, Sun  Q, Zhang  S, Emergence of a new multidrug-resistant serotype X variant in an epidemic clone of Shigella flexneri. J Clin Microbiol. 2010;48:41926. DOIPubMedGoogle Scholar

Main Article

Page created: August 16, 2016
Page updated: August 16, 2016
Page reviewed: August 16, 2016
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external