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 26, Number 6—June 2020

Antimicrobial Resistance in Salmonella enterica Serovar Paratyphi B Variant Java in Poultry from Europe and Latin America

L. Ricardo Castellanos1, Linda van der Graaf-van Bloois, Pilar Donado-Godoy, Kees Veldman, Francisco Duarte, María T. Acuña, Claudia Jarquín, François-Xavier Weill, Dik J. Mevius, Jaap A. Wagenaar, Joost Hordijk2, and Aldert L. Zomer2Comments to Author 
Author affiliations: Utrecht University, Utrecht, the Netherlands (L.R. Castellanos, L. van der Graaf-van Bloois, D.J. Mevius, J.A. Wagenaar, J. Hordijk, A.L. Zomer); Corporación Colombiana de Investigación Agropecuaria–AGROSAVIA, Cundinamarca, Colombia (P. Donado-Godoy); Wageningen Bioveterinary Research, Lelystad, the Netherlands (K. Veldman, D.J. Mevius, J.A. Wagenaar); Instituto Costarricense de Investigación y Enseñanza en Nutrición y Salud, Tres Ríos, Costa Rica (F. Duarte, M.T. Acuña); Universidad del Valle de Guatemala, Guatemala City, Guatemala (C. Jarquín); Institut Pasteur, Paris, France (F.-X. Weill)

Main Article


Newly obtained and publicly available genomes of 155 Salmonella enterica serovar Paratyphi B variant Java sequence type 28

Source Total No. per source* Years isolated
Saudi Arabia† 2 2 human 1987–1992
1 poultry‡
Belgium§ 5 5 unknown 2014
Denmark§ 9 8 poultry, 1 unknown 2009–2015
Germany§ 5 3 poultry, 1 human, 1 unknown 2001–2013
Ireland§ 2 2 human 2015–2016
Nigeria§¶ 1 1 poultry 2009
The Netherlands† 19 18 poultry, 1 fish 2000–2016
United Kingdom§
18 unknown, 5 human, 1 bovine
Latin America
Colombia†# 67 67 poultry 2008–2013
Costa Rica† 16 15 poultry, 1 swine 2009–2014
Guatemala† 4 4 poultry 2012

*Source-metadata of publicly available genomes was obtained from EnteroBase (
†Newly obtained.
‡Sample from a turkey imported from Israel.
§Publicly available.
¶Phylogenetically related to the European clade.
#19 genomes from previous reports in Colombia were publicly available in EnteroBase (31).

Main Article

  1. De Moor  CE. Salmonella infection in Batavia (Java), with particular reference to the diagnosis of the type of infection [in German]. Mededeelingen van den Dienst der Volksgzondheid in Nederlandsch-Indië. 1935;24:98–118.
  2. Kristensen  M, Kauffmann  F. Bakteriologische und klinische Erfahrungen über Infektionen mit d-weinsäurevergärenden Paratyphus B-Bacillen. Z Hyg Infektionskr. 1937;120:14954. DOIGoogle Scholar
  3. Kauffmann  F. [Differential diagnosis and pathogenicity of Salmonella java and Salmonella paratyphi B] [in German]. Z Hyg Infektionskr. 1955;141:54650. DOIPubMedGoogle Scholar
  4. Barker  RM, Kearney  GM, Nicholson  P, Blair  AL, Porter  RC, Crichton  PB. Types of Salmonella paratyphi B and their phylogenetic significance. J Med Microbiol. 1988;26:28593. DOIPubMedGoogle Scholar
  5. Miko  A, Guerra  B, Schroeter  A, Dorn  C, Helmuth  R. Molecular characterization of multiresistant d-tartrate-positive Salmonella enterica serovar paratyphi B isolates. J Clin Microbiol. 2002;40:318491. DOIPubMedGoogle Scholar
  6. Brown  DJ, Mather  H, Browning  LM, Coia  JE. Investigation of human infections with Salmonella enterica serovar Java in Scotland and possible association with imported poultry. Euro Surveill. 2003;8:3540. DOIPubMedGoogle Scholar
  7. Weill  FX, Fabre  L, Grandry  B, Grimont  PAD, Casin  I. Multiple-antibiotic resistance in Salmonella enterica serotype Paratyphi B isolates collected in France between 2000 and 2003 is due mainly to strains harboring Salmonella genomic islands 1, 1-B, and 1-C. Antimicrob Agents Chemother. 2005;49:2793801. DOIPubMedGoogle Scholar
  8. Threlfall  J, Levent  B, Hopkins  KL, de Pinna  E, Ward  LR, Brown  DJ. Multidrug-resistant Salmonella Java. Emerg Infect Dis. 2005;11:1701. DOIPubMedGoogle Scholar
  9. Denny  J, Threlfall  J, Takkinen  J, Lofdahl  S, Westrell  T, Varela  C, et al. Multinational Salmonella Paratyphi B variant Java (Salmonella Java) outbreak, August - December 2007. Euro Surveill. 2007;12:E071220.2.PubMedGoogle Scholar
  10. Doublet  B, Praud  K, Nguyen-Ho-Bao  T, Argudín  MA, Bertrand  S, Butaye  P, et al. Extended-spectrum β-lactamase- and AmpC β-lactamase-producing D-tartrate-positive Salmonella enterica serovar Paratyphi B from broilers and human patients in Belgium, 2008-10. J Antimicrob Chemother. 2014;69:125764. DOIPubMedGoogle Scholar
  11. Meunier  D, Boyd  D, Mulvey  MR, Baucheron  S, Mammina  C, Nastasi  A, et al. Salmonella enterica serotype Typhimurium DT 104 antibiotic resistance genomic island I in serotype paratyphi B. Emerg Infect Dis. 2002;8:4303. DOIPubMedGoogle Scholar
  12. Mulvey  MR, Boyd  D, Cloeckaert  A, Ahmed  R, Ng  LK; Provincial Public Health Laboratories. Emergence of multidrug-resistant Salmonella Paratyphi B dT+, Canada. Emerg Infect Dis. 2004;10:130710. DOIPubMedGoogle Scholar
  13. Gaulin  C, Vincent  C, Ismaïl  J. Sporadic infections of Salmonella Paratyphi B, var. Java associated with fish tanks. Can J Public Health. 2005;96:4714. DOIPubMedGoogle Scholar
  14. Hassan  R, Tecle  S, Adcock  B, Kellis  M, Weiss  J, Saupe  A, et al. Multistate outbreak of Salmonella Paratyphi B variant L(+) tartrate(+) and Salmonella Weltevreden infections linked to imported frozen raw tuna: USA, March-July 2015. Epidemiol Infect. 2018;146:14617. DOIPubMedGoogle Scholar
  15. Heiman Marshall  KE, Booth  H, Harrang  J, Lamba  K, Folley  A, Ching-Lee  M, et al. New product, old problem(s): multistate outbreak of Salmonella Paratyphi B variant L(+) tartrate(+) infections linked to raw sprouted nut butters, October 2015. Epidemiol Infect. 2019;8:16. DOIPubMedGoogle Scholar
  16. Levings  RS, Lightfoot  D, Hall  RM, Djordjevic  SP. Aquariums as reservoirs for multidrug-resistant Salmonella Paratyphi B. Emerg Infect Dis. 2006;12:50710. DOIPubMedGoogle Scholar
  17. Djordjevic  SP, Cain  AK, Evershed  NJ, Falconer  L, Levings  RS, Lightfoot  D, et al. Emergence and evolution of multiply antibiotic-resistant Salmonella enterica serovar Paratyphi B D-tartrate-utilizing strains containing SGI1. Antimicrob Agents Chemother. 2009;53:231926. DOIPubMedGoogle Scholar
  18. Toboldt  A, Tietze  E, Helmuth  R, Fruth  A, Junker  E, Malorny  B. Human infections attributable to the D-tartrate-fermenting variant of Salmonella enterica serovar Paratyphi B in Germany originate in reptiles and, on rare occasions, poultry. Appl Environ Microbiol. 2012;78:734757. DOIPubMedGoogle Scholar
  19. van Pelt  W, van der Zee  H, Wannet  WJ, van de Giessen  AW, Mevius  DJ, Bolder  NM. Explosive increase of Salmonella Java in poultry in the Netherlands: consequences for public health. Euro Surveill. 2003;8:315. DOIPubMedGoogle Scholar
  20. Centrum voor Onderzoek in Diergeneeskunde en Agrochemie. Centre d’Etude et des Recherches Vétérinaires et Agrochimiques (CODA-CERVA). Salmonella serotypes analysed at the CODA-CERVA in 2013. Technical Report. Federal Public Service Health, Food Chain Security and Environment:Brussels: 2014.
  21. Achtman  M, Wain  J, Weill  FX, Nair  S, Zhou  Z, Sangal  V, et al.; S. Enterica MLST Study Group. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 2012;8:e1002776. DOIPubMedGoogle Scholar
  22. Connor  TR, Owen  SV, Langridge  G, Connell  S, Nair  S, Reuter  S, et al. What’s in a name? Species-wide whole-genome sequencing resolves invasive and noninvasive lineages of Salmonella enterica serotype Paratyphi B. MBio. 2016;7:19. DOIPubMedGoogle Scholar
  23. Doumith  M, Godbole  G, Ashton  P, Larkin  L, Dallman  T, Day  M, et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother. 2016;71:23005. DOIPubMedGoogle Scholar
  24. Borowiak  M, Fischer  J, Hammerl  JA, Hendriksen  RS, Szabo  I, Malorny  B. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother. 2017;72:331724. DOIPubMedGoogle Scholar
  25. Castellanos  LR, van der Graaf-van Bloois  L, Donado-Godoy  P, Mevius  DJ, Wagenaar  JA, Hordijk  J, et al. Phylogenomic investigation of IncI1-Iγ plasmids harboring blaCMY-2 and blaSHV-12 in Salmonella enterica and Escherichia coli in multiple countries. Antimicrob Agents Chemother. 2019;63:e0254618. DOIPubMedGoogle Scholar
  26. Donado-Godoy  P, Gardner  I, Byrne  BA, Leon  M, Perez-Gutierrez  E, Ovalle  MV, et al. Prevalence, risk factors, and antimicrobial resistance profiles of Salmonella from commercial broiler farms in two important poultry-producing regions of Colombia. J Food Prot. 2012;75:87483. DOIPubMedGoogle Scholar
  27. Donado-Godoy  P, Clavijo  V, León  M, Arevalo  A, Castellanos  R, Bernal  J, et al. Counts, serovars, and antimicrobial resistance phenotypes of Salmonella on raw chicken meat at retail in Colombia. J Food Prot. 2014;77:22735. DOIPubMedGoogle Scholar
  28. Donado-Godoy  P, Byrne  BA, León  M, Castellanos  R, Vanegas  C, Coral  A, et al. Prevalence, resistance patterns, and risk factors for antimicrobial resistance in bacteria from retail chicken meat in Colombia. J Food Prot. 2015;78:7519. DOIPubMedGoogle Scholar
  29. Jarquin  C, Alvarez  D, Morales  O, Morales  AJ, López  B, Donado  P, et al. Salmonella on raw poultry in retail markets in Guatemala: levels, antibiotic susceptibility, and serovar distribution. J Food Prot. 2015;78:164250. DOIPubMedGoogle Scholar
  30. Boscán-Duque  LA, Arzálluz-Fisher  AM, Ugarte  C, Sánchez  D, Wittum  TE, Hoet  AE. Reduced susceptibility to quinolones among Salmonella serotypes isolated from poultry at slaughter in Venezuela. J Food Prot. 2007;70:20305. DOIPubMedGoogle Scholar
  31. Castellanos  LR, van der Graaf-van Bloois  L, Donado-Godoy  P, León  M, Clavijo  V, Arévalo  A, et al. Genomic characterization of extended-spectrum cephalosporin-resistant Salmonella enterica in the Colombian poultry chain. Front Microbiol. 2018;9:2431. DOIPubMedGoogle Scholar
  32. Donado-Godoy  P, Castellanos  R, León  M, Arevalo  A, Clavijo  V, Bernal  J, et al. The establishment of the Colombian Integrated Program for Antimicrobial Resistance Surveillance (COIPARS): a pilot project on poultry farms, slaughterhouses and retail market. Zoonoses Public Health. 2015;62(Suppl 1):5869. DOIPubMedGoogle Scholar
  33. Ministerio de Agricultura y Ganadería, Instituto Costarricense de Investigación y Enseñanza en Nutrición y Salud, Ministerio de Salud. Prevalence of Salmonella spp. in meat and chicken products. Costa Rica, September–November 2009 [in Spanish]. Technical Report. Ministry of Agriculture and Livestock, Costa Rican Institute for Research and Training in Nutrition and Health and Ministry of Health. San Jose (Costa Rica); 2011.
  34. Veldman  K, Mevius  DJ, Wit  B, van Pelt  W, Heederik  D. MARAN. Monitoring of antimicrobial resistance and antibiotic usage in animals in the Netherlands in 2016. 2017 [cited 2019 Mar 7].
  35. Alikhan  NF, Zhou  Z, Sergeant  MJ, Achtman  M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14:e1007261. DOIPubMedGoogle Scholar
  36. Kuijpers  LMF, Phe  T, Veng  CH, Lim  K, Ieng  S, Kham  C, et al. The clinical and microbiological characteristics of enteric fever in Cambodia, 2008-2015. PLoS Negl Trop Dis. 2017;11:e0005964. DOIPubMedGoogle Scholar
  37. Bankevich  A, Nurk  S, Antipov  D, Gurevich  AA, Dvorkin  M, Kulikov  AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:45577. DOIPubMedGoogle Scholar
  38. Zankari  E, Hasman  H, Cosentino  S, Vestergaard  M, Rasmussen  S, Lund  O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:26404. DOIPubMedGoogle Scholar
  39. Carattoli  A, Zankari  E, García-Fernández  A, Voldby Larsen  M, Lund  O, Villa  L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895903. DOIPubMedGoogle Scholar
  40. Larsen  MV, Cosentino  S, Rasmussen  S, Friis  C, Hasman  H, Marvig  RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50:135561. DOIPubMedGoogle Scholar
  41. Treangen  TJ, Ondov  BD, Koren  S, Phillippy  AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014;15:524. DOIPubMedGoogle Scholar
  42. Croucher  NJ, Page  AJ, Connor  TR, Delaney  AJ, Keane  JA, Bentley  SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2015;43:e15. DOIPubMedGoogle Scholar
  43. Drummond  AJ, Rambaut  A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214. DOIPubMedGoogle Scholar
  44. Seemann  T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:20689. DOIPubMedGoogle Scholar
  45. Page  AJ, Cummins  CA, Hunt  M, Wong  VK, Reuter  S, Holden  MTG, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31:36913. DOIPubMedGoogle Scholar
  46. Parks  DH, Imelfort  M, Skennerton  CT, Hugenholtz  P, Tyson  GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:104355. DOIPubMedGoogle Scholar
  47. Arndt  D, Grant  JR, Marcu  A, Sajed  T, Pon  A, Liang  Y, et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44(W1):W16-21. DOIPubMedGoogle Scholar
  48. Mather  AE, Reid  SWJ, Maskell  DJ, Parkhill  J, Fookes  MC, Harris  SR, et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science. 2013;341:15147. DOIPubMedGoogle Scholar
  49. Molina  LF. Poultry farming in Colombia [in Spanish]. Federación Nacional de Avicultores de Colombia (Fenavi)-Fondo Nacional Avícola (Fonav): Bogotá (Colombia); 2002.
  50. Agersø  Y, Jensen  JD, Hasman  H, Pedersen  K. Spread of extended spectrum cephalosporinase-producing Escherichia coli clones and plasmids from parent animals to broilers and to broiler meat in a production without use of cephalosporins. Foodborne Pathog Dis. 2014;11:7406. DOIPubMedGoogle Scholar

Main Article

1Current affiliate: Quadram Institute Bioscience, Norwich, UK.

2These authors contributed equally to this article.

Page created: May 18, 2020
Page updated: May 18, 2020
Page reviewed: May 18, 2020
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.