Comparative population structure analysis of Campylobacter jejuni from human and poultry origin in Bangladesh

  • Z. IslamEmail author
  • A. van Belkum
  • J. A. Wagenaar
  • A. J. Cody
  • A. G. de Boer
  • S. K. Sarker
  • B. C. Jacobs
  • K. A. Talukder
  • H. P. Endtz


Campylobacter jejuni is the most important cause of antecedent infections leading to Guillain–Barré syndrome (GBS) and Miller Fisher syndrome (MFS). The objective of the present study was to define the genetic diversity, population structure, and potential role of poultry in the transmission of Campylobacter to humans in Bangladesh. We determined the population structure of C. jejuni isolated from poultry (n = 66) and patients with enteritis (n = 39) or GBS (n = 10). Lipooligosaccharide (LOS) typing showed that 50/66 (76 %) C. jejuni strains isolated from poultry could be assigned to one of five LOS locus classes (A–E). The distribution of neuropathy-associated LOS locus classes A, B, and C were 30/50 (60 %) among the typable strains isolated from poultry. The LOS locus classes A, B, and C were significantly associated with GBS and enteritis-related C. jejuni strains more than for the poultry strains [(31/38 (82 %) vs. 30/50 (60 %), p < 0.05]. Multilocus sequence typing (MLST) defined 15 sequence types (STs) and six clonal complexes (CCs) among poultry isolates, including one ST-3740 not previously documented. The most commonly identified type, ST-5 (13/66), in chicken was seen only once among human isolates (1/49) (p < 0.001). Amplified fragment length polymorphism (AFLP) revealed three major clusters (A, B, and C) among C. jejuni isolated from humans and poultry. There seems to be a lack of overlap between the major human and chicken clones, which suggests that there may be additional sources for campylobacteriosis other than poultry in Bangladesh.


Amplify Fragment Length Polymorphism Amplify Fragment Length Polymorphism Analysis Campylobacteriosis Miller Fisher Syndrome Amplify Fragment Length Polymorphism Pattern 
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This research was funded by the Erasmus University Medical Center, Rotterdam, the Netherlands and the International Centre for Diarrheal Disease Research, Dhaka, Bangladesh (ICDDR,B). The ICDDR,B acknowledges with gratitude the commitment of the Government of Bangladesh to the Centre’s research efforts. The ICDDR,B also gratefully acknowledges the following donors which provide unrestricted support to the Centre’s research efforts: Australian Agency for International Development (AusAID), Government of the People’s Republic of Bangladesh, Canadian International Development Agency (CIDA), Swedish International Development Cooperation Agency (Sida), and the Department for International Development (DFID), UK. We are indebted to all the neurologists who referred their patients to us.

Conflict of interest

The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors declare that they have no conflict of interest.


  1. 1.
    Butzler JP (2004) Campylobacter, from obscurity to celebrity. Clin Microbiol Infect 10(10):868–876CrossRefPubMedGoogle Scholar
  2. 2.
    Winer JB (2008) Guillain–Barré syndrome. BMJ 337:a671CrossRefPubMedGoogle Scholar
  3. 3.
    Tauxe RV, Hargrett-Bean N, Patton CM, Wachsmuth IK (1988) Campylobacter isolates in the United States, 1982–1986. MMWR CDC Surveill Summ 37(2):1–13PubMedGoogle Scholar
  4. 4.
    Schouls LM, Reulen S, Duim B, Wagenaar JA, Willems RJ, Dingle KE, Colles FM, Van Embden JD (2003) Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: strain diversity, host range, and recombination. J Clin Microbiol 41(1):15–26CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Butzler JP, Oosterom J (1991) Campylobacter: pathogenicity and significance in foods. Int J Food Microbiol 12(1):1–8CrossRefPubMedGoogle Scholar
  6. 6.
    Gormley FJ, Macrae M, Forbes KJ, Ogden ID, Dallas JF, Strachan NJ (2008) Has retail chicken played a role in the decline of human campylobacteriosis? Appl Environ Microbiol 74(2):383–390CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Wilson DJ, Gabriel E, Leatherbarrow AJ, Cheesbrough J, Gee S, Bolton E, Fox A, Fearnhead P, Hart CA, Diggle PJ (2008) Tracing the source of campylobacteriosis. PLoS Genet 4(9):e1000203CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Wassenaar TM, Newell DG (2000) Genotyping of Campylobacter spp. Appl Environ Microbiol 66(1):1–9CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Clark CG, Bryden L, Cuff WR, Johnson PL, Jamieson F, Ciebin B, Wang G (2005) Use of the Oxford multilocus sequence typing protocol and sequencing of the flagellin short variable region to characterize isolates from a large outbreak of waterborne Campylobacter sp. strains in Walkerton, Ontario, Canada. J Clin Microbiol 43(5):2080–2091CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, Bootsma HJ, Willems RJ, Urwin R, Maiden MC (2001) Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 39(1):14–23CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Dingle KE, Colles FM, Ure R, Wagenaar JA, Duim B, Bolton FJ, Fox AJ, Wareing DR, Maiden MC (2002) Molecular characterization of Campylobacter jejuni clones: a basis for epidemiologic investigation. Emerg Infect Dis 8(9):949–955CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Miller WG, On SL, Wang G, Fontanoz S, Lastovica AJ, Mandrell RE (2005) Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus. J Clin Microbiol 43(5):2315–2329CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    On SLW, McCarthy N, Miller WG, Gilpin BJ (2008) Molecular epidemiology of Campylobacter species. In: Nachamkin I, Szymanski CM, Blaser MJ (eds) Campylobacter, 3rd edn. ASM Press, Washington, p 195Google Scholar
  14. 14.
    Duim B, Godschalk PC, van den Braak N, Dingle KE, Dijkstra JR, Leyde E, van der Plas J, Colles FM, Endtz HP, Wagenaar JA, Maiden MC, van Belkum A (2003) Molecular evidence for dissemination of unique Campylobacter jejuni clones in Curaçao, Netherlands Antilles. J Clin Microbiol 41(12):5593–5597CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Duim B, Wagenaar J (2006) Amplified fragment-length polymorphism and protein profiling for identification of Campylobacter lari subgroups. Methods Mol Biol 345:119–130PubMedGoogle Scholar
  16. 16.
    Johnsen G, Kruse H, Hofshagen M (2007) Genotyping of thermotolerant Campylobacter from poultry slaughterhouse by amplified fragment length polymorphism. J Appl Microbiol 103(2):271–279CrossRefPubMedGoogle Scholar
  17. 17.
    Siemer BL, Nielsen EM, On SL (2005) Identification and molecular epidemiology of Campylobacter coli isolates from human gastroenteritis, food, and animal sources by amplified fragment length polymorphism analysis and Penner serotyping. Appl Environ Microbiol 71(4):1953–1958CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Wittwer M, Keller J, Wassenaar TM, Stephan R, Howald D, Regula G, Bissig-Choisat B (2005) Genetic diversity and antibiotic resistance patterns in a Campylobacter population isolated from poultry farms in Switzerland. Appl Environ Microbiol 71(6):2840–2847CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Parker CT, Horn ST, Gilbert M, Miller WG, Woodward DL, Mandrell RE (2005) Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. J Clin Microbiol 43(6):2771–2781CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Islam Z, Jacobs BC, van Belkum A, Mohammad QD, Islam MB, Herbrink P, Diorditsa S, Luby SP, Talukder KA, Endtz HP (2010) Axonal variant of Guillain–Barre syndrome associated with Campylobacter infection in Bangladesh. Neurology 74(7):581–587CrossRefPubMedGoogle Scholar
  21. 21.
    Islam Z, van Belkum A, Cody AJ, Tabor H, Jacobs BC, Talukder KA, Endtz HP (2009) Campylobacter jejuni HS:23 and Guillain–Barre syndrome, Bangladesh. Emerg Infect Dis 15(8):1315–1317CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Talukder KA, Aslam M, Islam Z, Azmi IJ, Dutta DK, Hossain S, Nur-E-Kamal A, Nair GB, Cravioto A, Sack DA, Endtz HP (2008) Prevalence of virulence genes and cytolethal distending toxin production in Campylobacter jejuni isolates from diarrheal patients in Bangladesh. J Clin Microbiol 46(4):1485–1488CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Asbury AK, Cornblath DR (1990) Assessment of current diagnostic criteria for Guillain–Barré syndrome. Ann Neurol 27(Suppl):S21–S24CrossRefPubMedGoogle Scholar
  24. 24.
    Godschalk PC, Heikema AP, Gilbert M, Komagamine T, Ang CW, Glerum J, Brochu D, Li J, Yuki N, Jacobs BC, van Belkum A, Endtz HP (2004) The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain–Barre syndrome. J Clin Invest 114(11):1659–1665CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Duim B, Ang CW, van Belkum A, Rigter A, van Leeuwen NW, Endtz HP, Wagenaar JA (2000) Amplified fragment length polymorphism analysis of Campylobacter jejuni strains isolated from chickens and from patients with gastroenteritis or Guillain–Barré or Miller Fisher syndrome. Appl Environ Microbiol 66(9):3917–3923CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Jolley KA, Chan MS, Maiden MC (2004) mlstdbNet—distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5:86CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Habib I, Louwen R, Uyttendaele M, Houf K, Vandenberg O, Nieuwenhuis EE, Miller WG, van Belkum A, De Zutter L (2009) Correlation between genotypic diversity, lipooligosaccharide gene locus class variation, and caco-2 cell invasion potential of Campylobacter jejuni isolates from chicken meat and humans: contribution to virulotyping. Appl Environ Microbiol 75(13):4277–4288CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Islam Z, van Belkum A, Wagenaar JA, Cody AJ, de Boer AG, Tabor H, Jacobs BC, Talukder KA, Endtz HP (2009) Comparative genotyping of Campylobacter jejuni strains from patients with Guillain–Barré syndrome in Bangladesh. PLoS One 4(9):e7257CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kinana AD, Cardinale E, Tall F, Bahsoun I, Sire JM, Garin B, Breurec S, Boye CS, Perrier-Gros-Claude JD (2006) Genetic diversity and quinolone resistance in Campylobacter jejuni isolates from poultry in Senegal. Appl Environ Microbiol 72(5):3309–3313CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Colles FM, Jones K, Harding RM, Maiden MC (2003) Genetic diversity of Campylobacter jejuni isolates from farm animals and the farm environment. Appl Environ Microbiol 69(12):7409–7413CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Sopwith W, Birtles A, Matthews M, Fox A, Gee S, Painter M, Regan M, Syed Q, Bolton E (2006) Campylobacter jejuni multilocus sequence types in humans, northwest England, 2003–2004. Emerg Infect Dis 12(10):1500–1507CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Parsons BN, Cody AJ, Porter CJ, Stavisky JH, Smith JL, Williams NJ, Leatherbarrow AJ, Hart CA, Gaskell RM, Dingle KE, Dawson S (2009) Typing of Campylobacter jejuni isolates from dogs by use of multilocus sequence typing and pulsed-field gel electrophoresis. J Clin Microbiol 47(11):3466–3471CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    French N, Barrigas M, Brown P, Ribiero P, Williams N, Leatherbarrow H, Birtles R, Bolton E, Fearnhead P, Fox A (2005) Spatial epidemiology and natural population structure of Campylobacter jejuni colonizing a farmland ecosystem. Environ Microbiol 7(8):1116–1126CrossRefPubMedGoogle Scholar
  34. 34.
    Kwan PS, Birtles A, Bolton FJ, French NP, Robinson SE, Newbold LS, Upton M, Fox AJ (2008) Longitudinal study of the molecular epidemiology of Campylobacter jejuni in cattle on dairy farms. Appl Environ Microbiol 74(12):3626–3633CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Ragimbeau C, Schneider F, Losch S, Even J, Mossong J (2008) Multilocus sequence typing, pulsed-field gel electrophoresis, and fla short variable region typing of clonal complexes of Campylobacter jejuni strains of human, bovine, and poultry origins in Luxembourg. Appl Environ Microbiol 74(24):7715–7722CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    McTavish SM, Pope CE, Nicol C, Campbell D, French N, Carter PE (2009) Multilocus sequence typing of Campylobacter jejuni, and the correlation between clonal complex and pulsed-field gel electrophoresis macrorestriction profile. FEMS Microbiol Lett 298(2):149–156CrossRefPubMedGoogle Scholar
  37. 37.
    Endtz HP, Ang CW, van Den Braak N, Duim B, Rigter A, Price LJ, Woodward DL, Rodgers FG, Johnson WM, Wagenaar JA, Jacobs BC, Verbrugh HA, van Belkum A (2000) Molecular characterization of Campylobacter jejuni from patients with Guillain–Barré and Miller Fisher syndromes. J Clin Microbiol 38(6):2297–2301PubMedPubMedCentralGoogle Scholar
  38. 38.
    Taboada EN, van Belkum A, Yuki N, Acedillo RR, Godschalk PC, Koga M, Endtz HP, Gilbert M, Nash JH (2007) Comparative genomic analysis of Campylobacter jejuni associated with Guillain–Barré and Miller Fisher syndromes: neuropathogenic and enteritis-associated isolates can share high levels of genomic similarity. BMC Genomics 8:359CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Z. Islam
    • 1
    Email author
  • A. van Belkum
    • 2
    • 3
  • J. A. Wagenaar
    • 4
    • 5
  • A. J. Cody
    • 6
  • A. G. de Boer
    • 4
  • S. K. Sarker
    • 1
  • B. C. Jacobs
    • 7
  • K. A. Talukder
    • 1
  • H. P. Endtz
    • 1
    • 2
  1. 1.Emerging Diseases and Immunobiology Research Group, Centre for Food and Waterborne Diseases (CFWD), International Centre for Diarrheal Diseases Research (ICDDR,B)DhakaBangladesh
  2. 2.Department of Medical Microbiology and Infectious DiseasesErasmus MCRotterdamThe Netherlands
  3. 3.Microbiology R&DbioMérieuxLa Balme Les GrottesFrance
  4. 4.Department of Bacteriology and TSEsCentral Veterinary Institute of Wageningen URLelystadThe Netherlands
  5. 5.Department of Infectious Diseases and Immunology, Faculty of Veterinary MedicineUtrecht UniversityUtrechtThe Netherlands
  6. 6.The Tinbergen Building, Department of ZoologyUniversity of OxfordOxfordUK
  7. 7.Departments of Neurology and ImmunologyErasmus MCRotterdamThe Netherlands

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