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Abstract

Human campylobacteriosis, caused by the zoonotic bacteria and , remains a major cause of gastroenteritis worldwide. For many countries the implementation of effective interventions to reduce the burden of this disease is a high priority. Nucleotide sequence-based typing, including multilocus sequence typing (MLST) and antigen gene sequence typing (AGST), has provided unified, comprehensive, and portable isolate characterization, with curated databases of genotypes available (pubMLST.org/campylobacter). Analyses of large collections of isolates from various sources with these approaches have provided many insights into the epidemiology of these ubiquitous and diverse organisms. and populations are structured into clonal complexes, which reflect genealogy and are associated with specific phenotypes, e.g. the predisposition to infect particular animals, a property that has permitted the development of genetic means of attributing isolates from human disease to potential sources. This has identified retail meat, and especially chicken, as the likely cause of most human disease in many countries, although some human isolates have other likely origins. Such data have led directly to effective intervention studies and will be important in ongoing targeting of intervention strategies and the monitoring of their effectiveness. MLST and AGST data have also been employed in epidemiological investigations and studies of evolution and population biology. The sequence databases that have been established are compatible with the whole-genome sequencing (WGS) approaches likely to be implemented soon; indeed, the hierarchical approach adopted by MLST and AGST will be essential for the exploitation of WGS data.

Funding
This study was supported by the:
  • Department for Environment, Food and Rural Affairs (Award OZ0615)
  • Wellcome Trust
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2012-11-01
2024-03-28
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References

  1. Allen V. M., Bull S. A., Corry J. E., Domingue G., Jørgensen F., Frost J. A., Whyte R., Gonzalez A., Elviss N., Humphrey T. J. ( 2007). Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation. Int J Food Microbiol 113:54–61 [View Article] [PubMed]
    [Google Scholar]
  2. Allos B. M. ( 2001). Campylobacter jejuni infections: update on emerging issues and trends. Clin Infect Dis 32:1201–1206 [View Article] [PubMed]
    [Google Scholar]
  3. Allos B. M., Moore M. R., Griffin P. M., Tauxe R. V. ( 2004). Surveillance for sporadic foodborne disease in the 21st century: the FoodNet perspective. Clin Infect Dis 38:Suppl. 3S115–S120 [View Article] [PubMed]
    [Google Scholar]
  4. Alm R. A., Guerry P., Trust T. J. ( 1993). Distribution and polymorphism of the flagellin genes from isolates of Campylobacter coli and Campylobacter jejuni . J Bacteriol 175:3051–3057 [PubMed]
    [Google Scholar]
  5. Bessell P. R., Rotariu O., Innocent G. T., Smith-Palmer A., Strachan N. J. C., Forbes K. J., Cowden J. M., Reid S. W. J., Matthews L. ( 2012). Using sequence data to identify alternative routes and risk of infection: a case-study of campylobacter in Scotland. BMC Infect Dis 12:80 [View Article] [PubMed]
    [Google Scholar]
  6. Best E. L., Fox A. J., Frost J. A., Bolton F. J. ( 2005). Real-time single-nucleotide polymorphism profiling using Taqman technology for rapid recognition of Campylobacter jejuni clonal complexes. J Med Microbiol 54:919–925 [View Article] [PubMed]
    [Google Scholar]
  7. Brown P. E., Christensen O. F., Clough H. E., Diggle P. J., Hart C. A., Hazel S., Kemp R., Leatherbarrow A. J., Moore A. & other authors ( 2004). Frequency and spatial distribution of environmental Campylobacter spp. Appl Environ Microbiol 70:6501–6511 [View Article] [PubMed]
    [Google Scholar]
  8. Bryant D., Moulton V. ( 2004). Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265 [View Article] [PubMed]
    [Google Scholar]
  9. Bull S. A., Allen V. M., Domingue G., Jørgensen F., Frost J. A., Ure R., Whyte R., Tinker D., Corry J. E. & other authors ( 2006). Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl Environ Microbiol 72:645–652 [View Article] [PubMed]
    [Google Scholar]
  10. Bull S. A., Thomas A., Humphrey T., Ellis-Iversen J., Cook A. J., Lovell R., Jorgensen F. ( 2008a). Flock health indicators and Campylobacter spp. in commercial housed broilers reared in Great Britain. Appl Environ Microbiol 74:5408–5413 [View Article] [PubMed]
    [Google Scholar]
  11. Bull S. A., Thomas A., Humphrey T., Ellis-Iversen J., Cook A. J., Lovell R., Jorgensen F. ( 2008b). Flock health indicators and Campylobacter spp. in commercial housed broilers reared in Great Britain. Appl Environ Microbiol 74:5408–5413 [View Article] [PubMed]
    [Google Scholar]
  12. Caro-Quintero A., Rodriguez-Castaño G. P., Konstantinidis K. T. ( 2009). Genomic insights into the convergence and pathogenicity factors of Campylobacter jejuni and Campylobacter coli species. J Bacteriol 191:5824–5831 [View Article] [PubMed]
    [Google Scholar]
  13. Carter P. E., McTavish S. M., Brooks H. J., Campbell D., Collins-Emerson J. M., Midwinter A. C., French N. P. ( 2009). Novel clonal complexes with an unknown animal reservoir dominate Campylobacter jejuni isolates from river water in New Zealand. Appl Environ Microbiol 75:6038–6046 [View Article] [PubMed]
    [Google Scholar]
  14. Chan K., Miller W. G., Mandrell R. E., Kathariou S. ( 2007). The absence of intervening sequences in 23S rRNA genes of Campylobacter coli isolates from turkeys is a unique attribute of a cluster of related strains which also lack resistance to erythromycin. Appl Environ Microbiol 73:1208–1214 [View Article] [PubMed]
    [Google Scholar]
  15. Clark C. G., Bryden L., Cuff W. R., Johnson P. L., 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 43:2080–2091 [View Article] [PubMed]
    [Google Scholar]
  16. Clark C. G., Beeston A., Bryden L., Wang G., Barton C., Cuff W., Gilmour M. W., Ng L. K. ( 2007). Phylogenetic relationships of Campylobacter jejuni based on porA sequences. Can J Microbiol 53:27–38 [View Article] [PubMed]
    [Google Scholar]
  17. Clark C. G., Taboada E., Grant C. C., Blakeston C., Pollari F., Marshall B., Rahn K., Mackinnon J., Daignault D. & other authors ( 2012). Comparison of molecular typing methods useful for detecting clusters of Campylobacter jejuni and C. coli isolates through routine surveillance. J Clin Microbiol 50:798–809 [View Article] [PubMed]
    [Google Scholar]
  18. Cody A. J., Maiden M. J., Dingle K. E. ( 2009). Genetic diversity and stability of the porA allele as a genetic marker in human Campylobacter infection. Microbiology 155:4145–4154 [View Article] [PubMed]
    [Google Scholar]
  19. Cody A. J., Clarke L., Bowler I. C., Dingle K. E. ( 2010a). Ciprofloxacin-resistant campylobacteriosis in the UK. Lancet 376:1987 [View Article] [PubMed]
    [Google Scholar]
  20. Cody A. J., Colles F. M., Sheppard S. K., Maiden M. C. J. ( 2010b). Where does Campylobacter come from? A molecular odyssey. Adv Exp Med Biol 659:47–56 [View Article] [PubMed]
    [Google Scholar]
  21. Cody A. J., McCarthy N. M., Wimalarathna H. L., Colles F. M., Clark L., Bowler I. C., Maiden M. C., Dingle K. E. ( 2012). A longitudinal six-year study of the molecular epidemiology of clinical Campylobacter isolates in Oxfordshire, UK. J Clin Microbiol [View Article] [PubMed]
    [Google Scholar]
  22. Colles F. M., Jones K., Harding R. M., Maiden M. C. ( 2003). Genetic diversity of Campylobacter jejuni isolates from farm animals and the farm environment. Appl Environ Microbiol 69:7409–7413 [View Article] [PubMed]
    [Google Scholar]
  23. Colles F. M., Dingle K. E., Cody A. J., Maiden M. C. ( 2008a). Comparison of Campylobacter populations in wild geese with those in starlings and free-range poultry on the same farm. Appl Environ Microbiol 74:3583–3590 [View Article] [PubMed]
    [Google Scholar]
  24. Colles F. M., Jones T. A., McCarthy N. D., Sheppard S. K., Cody A. J., Dingle K. E., Dawkins M. S., Maiden M. C. ( 2008b). Campylobacter infection of broiler chickens in a free-range environment. Environ Microbiol 10:2042–2050 [View Article] [PubMed]
    [Google Scholar]
  25. Colles F. M., McCarthy N. D., Howe J. C., Devereux C. L., Gosler A. G., Maiden M. C. ( 2009). Dynamics of Campylobacter colonization of a natural host, Sturnus vulgaris (European starling). Environ Microbiol 11:258–267 [View Article] [PubMed]
    [Google Scholar]
  26. Colles F. M., McCarthy N. D., Sheppard S. K., Layton R., Maiden M. C. ( 2010). Comparison of Campylobacter populations isolated from a free-range broiler flock before and after slaughter. Int J Food Microbiol 137:259–264 [View Article] [PubMed]
    [Google Scholar]
  27. Colles F. M., McCarthy N. D., Layton R., Maiden M. C. ( 2011a). The prevalence of Campylobacter amongst a free-range broiler breeder flock was primarily affected by flock age. PLoS ONE 6:e22825 [View Article] [PubMed]
    [Google Scholar]
  28. Colles F. M., Ali J. S., Sheppard S. K., McCarthy N. D., Maiden M. C. ( 2011b). Campylobacter populations in wild and domesticated Mallard ducks (Anas platyrhynchos). Environ Microbiol Rep 3:574–580 [View Article] [PubMed]
    [Google Scholar]
  29. Corander J., Marttinen P. ( 2006). Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843 [View Article] [PubMed]
    [Google Scholar]
  30. D’lima C. B., Miller W. G., Mandrell R. E., Wright S. L., Siletzky R. M., Carver D. K., Kathariou S. ( 2007). Clonal population structure and specific genotypes of multidrug-resistant Campylobacter coli from turkeys. Appl Environ Microbiol 73:2156–2164 [View Article] [PubMed]
    [Google Scholar]
  31. de Haan C. P., Kivistö R., Hakkinen M., Rautelin H., Hänninen M. L. ( 2010a). Decreasing trend of overlapping multilocus sequence types between human and chicken Campylobacter jejuni isolates over a decade in Finland. Appl Environ Microbiol 76:5228–5236 [View Article] [PubMed]
    [Google Scholar]
  32. de Haan C. P., Kivistö R. I., Hakkinen M., Corander J., Hänninen M. L. ( 2010b). Multilocus sequence types of Finnish bovine Campylobacter jejuni isolates and their attribution to human infections. BMC Microbiol 10:200 [View Article] [PubMed]
    [Google Scholar]
  33. Didelot X., Maiden M. C. ( 2010). Impact of recombination on bacterial evolution. Trends Microbiol 18:315–322 [View Article] [PubMed]
    [Google Scholar]
  34. Didelot X., Achtman M., Parkhill J., Thomson N. R., Falush D. ( 2007). A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination?. Genome Res 17:61–68 [View Article] [PubMed]
    [Google Scholar]
  35. Dingle K. E., Van Den Braak N., Colles F. M., Price L. J., Woodward D. L., Rodgers F. G., Endtz H. P., Van Belkum A., Maiden M. C. J. ( 2001a). Sequence typing confirms that Campylobacter jejuni strains associated with Guillain-Barré and Miller-Fisher syndromes are of diverse genetic lineage, serotype, and flagella type. J Clin Microbiol 39:3346–3349 [View Article] [PubMed]
    [Google Scholar]
  36. Dingle K. E., Colles F. M., Wareing D. R. A., Ure R., Fox A. J., Bolton F. E., Bootsma H. J., Willems R. J. L., Urwin R., Maiden M. C. ( 2001b). Multilocus sequence typing system for Campylobacter jejuni . J Clin Microbiol 39:14–23 [View Article] [PubMed]
    [Google Scholar]
  37. Dingle K. E., Colles F. M., Ure R., Wagenaar J. A., Duim B., Bolton F. J., Fox A. J., Wareing D. R. A., Maiden M. C. J. ( 2002). Molecular characterization of Campylobacter jejuni clones: a basis for epidemiologic investigation. Emerg Infect Dis 8:949–955 [View Article] [PubMed]
    [Google Scholar]
  38. Dingle K. E., Colles F. M., Falush D., Maiden M. C. ( 2005). Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni . J Clin Microbiol 43:340–347 [View Article] [PubMed]
    [Google Scholar]
  39. Dingle K. E., McCarthy N. D., Cody A. J., Peto T. E., Maiden M. C. ( 2008). Extended sequence typing of Campylobacter spp., United Kingdom. Emerg Infect Dis 14:1620–1622 [View Article] [PubMed]
    [Google Scholar]
  40. Djordjevic S. P., Unicomb L. E., Adamson P. J., Mickan L., Rios R. Australian Campylobacter Subtyping Study Group ( 2007). Clonal complexes of Campylobacter jejuni identified by multilocus sequence typing are reliably predicted by restriction fragment length polymorphism analyses of the flaA gene. J Clin Microbiol 45:102–108 [View Article] [PubMed]
    [Google Scholar]
  41. Duim B., Godschalk P. C., van den Braak N., Dingle K. E., Dijkstra J. R., Leyde E., van der Plas J., Colles F. M., Endtz H. P. & other authors ( 2003). Molecular evidence for dissemination of unique Campylobacter jejuni clones in Curaçao, Netherlands Antilles. J Clin Microbiol 41:5593–5597 [View Article] [PubMed]
    [Google Scholar]
  42. Duong T., Konkel M. E. ( 2009). Comparative studies of Campylobacter jejuni genomic diversity reveal the importance of core and dispensable genes in the biology of this enigmatic food-borne pathogen. Curr Opin Biotechnol 20:158–165 [View Article] [PubMed]
    [Google Scholar]
  43. Egger R., Korczak B. M., Niederer L., Overesch G., Kuhnert P. ( 2012). Genotypes and antibiotic resistance of Campylobacter coli in fattening pigs. Vet Microbiol 155:272–278 [View Article] [PubMed]
    [Google Scholar]
  44. Engberg J., Nachamkin I., Fussing V., McKhann G. M., Griffin J. W., Piffaretti J. C., Nielsen E. M., Gerner-Smidt P. ( 2001). Absence of clonality of Campylobacter jejuni in serotypes other than HS : 19 associated with Guillain-Barré syndrome and gastroenteritis. J Infect Dis 184:215–220 [View Article] [PubMed]
    [Google Scholar]
  45. Falush D., Stephens M., Pritchard J. K. ( 2003). Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587 [PubMed]
    [Google Scholar]
  46. Feil E. J., Li B. C., Aanensen D. M., Hanage W. P., Spratt B. G. ( 2004). eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518–1530 [View Article] [PubMed]
    [Google Scholar]
  47. Forbes K. J., Gormley F. J., Dallas J. F., Labovitiadi O., MacRae M., Owen R. J., Richardson J., Strachan N. J., Cowden J. M. & other authors ( 2009). Campylobacter immunity and coinfection following a large outbreak in a farming community. J Clin Microbiol 47:111–116 [View Article] [PubMed]
    [Google Scholar]
  48. 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 7:1116–1126 [View Article] [PubMed]
    [Google Scholar]
  49. French N. P., Midwinter A., Holland B., Collins-Emerson J., Pattison R., Colles F., Carter P. ( 2009). Molecular epidemiology of Campylobacter jejuni isolates from wild-bird fecal material in children’s playgrounds. Appl Environ Microbiol 75:779–783 [View Article] [PubMed]
    [Google Scholar]
  50. Friedman C. J., Neiman J., Wegener H. C., Tauxe R. V. ( 2000). Epidemiology of Campylobacter jejuni infections in the United States and other industrialised nations. Campylobacter121–138 Nachamkin I., Blaser M. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  51. Gillespie I. A., O’Brien S. J., Frost J. A., Adak G. K., Swan A. V., Painter M. J., Neal K. R. and the Campylobacter Sentinel Surveillance System Collaborators ( 2002). A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg Infect Dis 8:937–942 [View Article] [PubMed]
    [Google Scholar]
  52. Gormley F. J., Macrae M., Forbes K. J., Ogden I. D., Dallas J. F., Strachan N. J. ( 2008). Has retail chicken played a role in the decline of human campylobacteriosis?. Appl Environ Microbiol 74:383–390 [View Article] [PubMed]
    [Google Scholar]
  53. Gormley F. J., Little C. L., Rawal N., Gillespie I. A., Lebaigue S., Adak G. K. ( 2011). A 17-year review of foodborne outbreaks: describing the continuing decline in England and Wales (1992–2008). Epidemiol Infect 139:688–699 [View Article] [PubMed]
    [Google Scholar]
  54. Griekspoor P., Engvall E. O., Olsen B., Waldenström J. ( 2010). Multilocus sequence typing of Campylobacter jejuni from broilers. Vet Microbiol 140:180–185 [View Article] [PubMed]
    [Google Scholar]
  55. Gripp E., Hlahla D., Didelot X., Kops F., Maurischat S., Tedin K., Alter T., Ellerbroek L., Schreiber K. & other authors ( 2011). Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 12:584 [View Article] [PubMed]
    [Google Scholar]
  56. Grove-White D. H., Leatherbarrow A. J., Cripps P. J., Diggle P. J., French N. P. ( 2011). Molecular epidemiology and genetic diversity of Campylobacter jejuni in ruminants. Epidemiol Infect 139:1661–1671 [PubMed] [CrossRef]
    [Google Scholar]
  57. Habib I., Miller W. G., Uyttendaele M., Houf K., De Zutter L. ( 2009a). Clonal population structure and antimicrobial resistance of Campylobacter jejuni in chicken meat from Belgium. Appl Environ Microbiol 75:4264–4272 [View Article] [PubMed]
    [Google Scholar]
  58. Habib I., Miller W. G., Uyttendaele M., Houf K., De Zutter L. ( 2009b). Clonal population structure and antimicrobial resistance of Campylobacter jejuni in chicken meat from Belgium. Appl Environ Microbiol 75:4264–4272 [View Article] [PubMed]
    [Google Scholar]
  59. Hald B., Skovgård H., Pedersen K., Bunkenborg H. ( 2008). Influxed insects as vectors for Campylobacter jejuni and Campylobacter coli in Danish broiler houses. Poult Sci 87:1428–1434 [View Article] [PubMed]
    [Google Scholar]
  60. Harrington C. S., Thomson-Carter F. M., Carter P. E. ( 1997). Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35:2386–2392 [PubMed]
    [Google Scholar]
  61. Hastings R., Colles F. M., McCarthy N. D., Maiden M. C., Sheppard S. K. ( 2011). Campylobacter genotypes from poultry transportation crates indicate a source of contamination and transmission. J Appl Microbiol 110:266–276 [View Article] [PubMed]
    [Google Scholar]
  62. Hepworth P. J., Ashelford K. E., Hinds J., Gould K. A., Witney A. A., Williams N. J., Leatherbarrow H., French N. P., Birtles R. J. & other authors ( 2011). Genomic variations define divergence of water/wildlife-associated Campylobacter jejuni niche specialists from common clonal complexes. Environ Microbiol 13:1549–1560 [View Article] [PubMed]
    [Google Scholar]
  63. Huson D. H. ( 1998). SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73 [View Article] [PubMed]
    [Google Scholar]
  64. Islam Z., van Belkum A., Wagenaar J. A., Cody A. J., de Boer A. G., Tabor H., Jacobs B. C., Talukder K. A., Endtz H. P. ( 2009). Comparative genotyping of Campylobacter jejuni strains from patients with Guillain-Barré syndrome in Bangladesh. PLoS ONE 4:e7257 [View Article] [PubMed]
    [Google Scholar]
  65. Jolley K. A., Maiden M. C. ( 2006). AgdbNet – antigen sequence database software for bacterial typing. BMC Bioinformatics 7:314 [View Article] [PubMed]
    [Google Scholar]
  66. Jolley K. A., Maiden M. C. ( 2010). BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595 [View Article] [PubMed]
    [Google Scholar]
  67. Jolley K. A., Chan M. S., Maiden M. C. ( 2004). mlstdbNet – distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5:86 [View Article] [PubMed]
    [Google Scholar]
  68. Jorgensen F., Ellis-Iversen J., Rushton S., Bull S. A., Harris S. A., Bryan S. J., Gonzalez A., Humphrey T. J. ( 2011). Influence of season and geography on Campylobacter jejuni and C. coli subtypes in housed broiler flocks reared in Great Britain. Appl Environ Microbiol 77:3741–3748 [View Article] [PubMed]
    [Google Scholar]
  69. Kimoto K., Koga M., Odaka M., Hirata K., Takahashi M., Li J., Gilbert M., Yuki N. ( 2006). Relationship of bacterial strains to clinical syndromes of Campylobacter-associated neuropathies. Neurology 67:1837–1843 [View Article] [PubMed]
    [Google Scholar]
  70. Kinana A. D., Cardinale E., Tall F., Bahsoun I., Sire J. M., Garin B., Breurec S., Boye C. S., Perrier-Gros-Claude J. D. ( 2006). Genetic diversity and quinolone resistance in Campylobacter jejuni isolates from poultry in Senegal. Appl Environ Microbiol 72:3309–3313 [View Article] [PubMed]
    [Google Scholar]
  71. Kittl S., Kuhnert P., Hächler H., Korczak B. M. ( 2011). Comparison of genotypes and antibiotic resistance of Campylobacter jejuni isolated from humans and slaughtered chickens in Switzerland. J Appl Microbiol 110:513–520 [View Article] [PubMed]
    [Google Scholar]
  72. Korczak B. M., Zurfluh M., Emler S., Kuhn-Oertli J., Kuhnert P. ( 2009). Multiplex strategy for multilocus sequence typing, fla typing, and genetic determination of antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolates collected in Switzerland. J Clin Microbiol 47:1996–2007 [View Article] [PubMed]
    [Google Scholar]
  73. Kwan P. S., Birtles A., Bolton F. J., French N. P., Robinson S. E., Newbold L. S., Upton M., Fox A. J. ( 2008a). Longitudinal study of the molecular epidemiology of Campylobacter jejuni in cattle on dairy farms. Appl Environ Microbiol 74:3626–3633 [View Article] [PubMed]
    [Google Scholar]
  74. Kwan P. S., Barrigas M., Bolton F. J., French N. P., Gowland P., Kemp R., Leatherbarrow H., Upton M., Fox A. J. ( 2008b). Molecular epidemiology of Campylobacter jejuni populations in dairy cattle, wildlife, and the environment in a farmland area. Appl Environ Microbiol 74:5130–5138 [View Article] [PubMed]
    [Google Scholar]
  75. Lang P., Lefebure T., Wang W., Pavinski Bitar P., Meinersmann R. J., Kaya K., Stanhope M. J. ( 2010). Expanded multilocus sequence typing and comparative genomic hybridization of Campylobacter coli isolates from multiple hosts. Appl Environ Microbiol 76:1913–1925 [View Article] [PubMed]
    [Google Scholar]
  76. Lefébure T., Pavinski Bitar P. D., Suzuki H., Stanhope M. J. ( 2010). Evolutionary dynamics of complete Campylobacter pan-genomes and the bacterial species concept. Genome Biol Evol 2:646–655 [View Article] [PubMed]
    [Google Scholar]
  77. Lévesque S., Frost E., Arbeit R. D., Michaud S. ( 2008). Multilocus sequence typing of Campylobacter jejuni isolates from humans, chickens, raw milk, and environmental water in Quebec, Canada. J Clin Microbiol 46:3404–3411 [View Article] [PubMed]
    [Google Scholar]
  78. Levin B. R. ( 1981). Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99:1–23 [PubMed]
    [Google Scholar]
  79. Litrup E., Torpdahl M., Nielsen E. M. ( 2007). Multilocus sequence typing performed on Campylobacter coli isolates from humans, broilers, pigs and cattle originating in Denmark. J Appl Microbiol 103:210–218 [View Article] [PubMed]
    [Google Scholar]
  80. Magnússon S. H., Guðmundsdóttir S., Reynisson E., Rúnarsson A. R., Harðardóttir H., Gunnarson E., Georgsson F., Reiersen J., Marteinsson V. T. ( 2011). Comparison of Campylobacter jejuni isolates from human, food, veterinary and environmental sources in Iceland using PFGE, MLST and fla-SVR sequencing. J Appl Microbiol 111:971–981 [View Article] [PubMed]
    [Google Scholar]
  81. Maiden M. C. ( 2006). Multilocus sequence typing of bacteria. Annu Rev Microbiol 60:561–588 [View Article] [PubMed]
    [Google Scholar]
  82. Maiden M. C., Dingle K. E. ( 2008). Population biology of Campylobacter jejuni and related organisms. Campylobacter27–40 Nachamkin I., Szymanski C. M., Blaser M. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  83. Maiden M. C. J., Bygraves J. A., Feil E., Morelli G., Russell J. E., Urwin R., Zhang Q., Zhou J., Zurth K. & other authors ( 1998). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95:3140–3145 [View Article] [PubMed]
    [Google Scholar]
  84. Manning G., Dowson C. G., Bagnall M. C., Ahmed I. H., West M., Newell D. G. ( 2003). Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni . Appl Environ Microbiol 69:6370–6379 [View Article] [PubMed]
    [Google Scholar]
  85. Maynard Smith J. M., Smith N. H., O’Rourke M., Spratt B. G. ( 1993). How clonal are bacteria?. Proc Natl Acad Sci U S A 90:4384–4388 [View Article] [PubMed]
    [Google Scholar]
  86. McCarthy N. D., Colles F. M., Dingle K. E., Bagnall M. C., Manning G., Maiden M. C., Falush D. ( 2007). Host-associated genetic import in Campylobacter jejuni . Emerg Infect Dis 13:267–272 [View Article] [PubMed]
    [Google Scholar]
  87. McCarthy N. D., Gillespie I. A., Lawson A. J., Richardson J., Neal K. R., Hawtin P. R., Maiden M. C., O’Brien S. J. ( 2012). Molecular epidemiology of human Campylobacter jejuni shows association between seasonal and international patterns of disease. [View Article] [PubMed]
    [Google Scholar]
  88. McTavish S. M., Pope C. E., Nicol C., Sexton K., French N., Carter P. E. ( 2008). Wide geographical distribution of internationally rare Campylobacter clones within New Zealand. Epidemiol Infect 136:1244–1252 [View Article] [PubMed]
    [Google Scholar]
  89. McTavish S. M., Pope C. E., Nicol C., Campbell D., French N., Carter P. E. ( 2009). Multilocus sequence typing of Campylobacter jejuni, and the correlation between clonal complex and pulsed-field gel electrophoresis macrorestriction profile. FEMS Microbiol Lett 298:149–156 [View Article] [PubMed]
    [Google Scholar]
  90. Medini D., Serruto D., Parkhill J., Relman D. A., Donati C., Moxon R., Falkow S., Rappuoli R. ( 2008). Microbiology in the post-genomic era. Nat Rev Microbiol 6:419–430 [PubMed]
    [Google Scholar]
  91. Meinersmann R. J., Helsel L. O., Fields P. I., Hiett K. L. ( 1997). Discrimination of Campylobacter jejuni isolates by fla gene sequencing. J Clin Microbiol 35:2810–2814 [PubMed]
    [Google Scholar]
  92. Meinersmann R. J., Patton C. M., Evins G. M., Wachsmuth I. K., Fields P. I. ( 2002). Genetic diversity and relationships of Campylobacter species and subspecies. Int J Syst Evol Microbiol 52:1789–1797 [View Article] [PubMed]
    [Google Scholar]
  93. Meinersmann R. J., Phillips R. W., Hiett K. L., Fedorka-Cray P. ( 2005). Differentiation of Campylobacter populations as demonstrated by flagellin short variable region sequences. Appl Environ Microbiol 71:6368–6374 [View Article] [PubMed]
    [Google Scholar]
  94. Mickan L., Doyle R., Valcanis M., Dingle K. E., Unicomb L., Lanser J. the Australian Campylobacter Subtyping Study Group ( 2007). Multilocus sequence typing of Campylobacter jejuni isolates from New South Wales, Australia. J Appl Microbiol 102:144–152 [View Article] [PubMed]
    [Google Scholar]
  95. Miller W. G., On S. L., Wang G., Fontanoz S., Lastovica A. J., Mandrell R. E. ( 2005). Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis, and C. helveticus . J Clin Microbiol 43:2315–2329 [View Article] [PubMed]
    [Google Scholar]
  96. Miller W. G., Englen M. D., Kathariou S., Wesley I. V., Wang G., Pittenger-Alley L., Siletz R. M., Muraoka W., Fedorka-Cray P. J., Mandrell R. E. ( 2006). Identification of host-associated alleles by multilocus sequence typing of Campylobacter coli strains from food animals. Microbiology 152:245–255 [View Article] [PubMed]
    [Google Scholar]
  97. Miller R. S., Miller W. G., Behringer M., Hariharan H., Matthew V., Oyarzabal O. A. ( 2010). DNA identification and characterization of Campylobacter jejuni and Campylobacter coli isolated from caecal samples of chickens in Grenada. J Appl Microbiol 108:1041–1049 [View Article] [PubMed]
    [Google Scholar]
  98. Mortensen N. P., Kuijf M. L., Ang C. W., Schiellerup P., Krogfelt K. A., Jacobs B. C., van Belkum A., Endtz H. P., Bergman M. P. ( 2009). Sialylation of Campylobacter jejuni lipo-oligosaccharides is associated with severe gastro-enteritis and reactive arthritis. Microbes Infect 11:988–994 [View Article] [PubMed]
    [Google Scholar]
  99. Mullner P., Jones G., Noble A., Spencer S. E., Hathaway S., French N. P. ( 2009a). Source attribution of food-borne zoonoses in New Zealand: a modified Hald model. Risk Anal 29:970–984 [View Article] [PubMed]
    [Google Scholar]
  100. Mullner P., Spencer S. E., Wilson D. J., Jones G., Noble A. D., Midwinter A. C., Collins-Emerson J. M., Carter P., Hathaway S., French N. P. ( 2009b). Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. Infect Genet Evol 9:1311–1319 [View Article] [PubMed]
    [Google Scholar]
  101. Müllner P., Collins-Emerson J. M., Midwinter A. C., Carter P., Spencer S. E. F., van der Logt P., Hathaway S., French N. P. ( 2010). Molecular epidemiology of Campylobacter jejuni in a geographically isolated country with a uniquely structured poultry industry. Appl Environ Microbiol 76:2145–2154 [View Article] [PubMed]
    [Google Scholar]
  102. Nachamkin I. ( 2002). Chronic effects of Campylobacter infection. Microbes Infect 4:399–403 [View Article] [PubMed]
    [Google Scholar]
  103. Newell D. G., Fearnley C. ( 2003). Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol 69:4343–4351 [View Article] [PubMed]
    [Google Scholar]
  104. Niederer L., Kuhnert P., Egger R., Büttner S., Hächler H., Korczak B. M. ( 2012). Genotypes and antibiotic resistances of Campylobacter jejuni and Campylobacter coli isolates from domestic and travel-associated human cases. Appl Environ Microbiol 78:288–291 [View Article] [PubMed]
    [Google Scholar]
  105. Nielsen L. N., Sheppard S. K., McCarthy N. D., Maiden M. C. J., Ingmer H., Krogfelt K. A. ( 2010). MLST clustering of Campylobacter jejuni isolates from patients with gastroenteritis, reactive arthritis and Guillain–Barré syndrome. J Appl Microbiol 108:591–599 [View Article] [PubMed]
    [Google Scholar]
  106. Ogden I. D., MacRae M., Johnston M., Strachan N. J., Cody A. J., Dingle K. E., Newell D. G. ( 2007). Use of multilocus sequence typing to investigate the association between the presence of Campylobacter spp. in broiler drinking water and Campylobacter colonization in broilers. Appl Environ Microbiol 73:5125–5129 [View Article] [PubMed]
    [Google Scholar]
  107. Ogden I. D., Dallas J. F., MacRae M., Rotariu O., Reay K. W., Leitch M., Thomson A. P., Sheppard S. K., Maiden M. & other authors ( 2009). Campylobacter excreted into the environment by animal sources: prevalence, concentration shed, and host association. Foodborne Pathog Dis 6:1161–1170 [View Article] [PubMed]
    [Google Scholar]
  108. Parsons B. N., Cody A. J., Porter C. J., Stavisky J. H., Smith J. L., Williams N. J., Leatherbarrow A. J. H., Hart C. A., Gaskell R. M. & other authors ( 2009). Typing of Campylobacter jejuni isolates from dogs by use of multilocus sequence typing and pulsed-field gel electrophoresis. J Clin Microbiol 47:3466–3471 [View Article] [PubMed]
    [Google Scholar]
  109. Parsons B. N., Porter C. J., Stavisky J. H., Williams N. J., Birtles R. J., Miller W. G., Hart C. A., Gaskell R. M., Dawson S. ( 2012). Multilocus sequence typing of human and canine C. upsaliensis isolates. Vet Microbiol 157:391–397 [View Article] [PubMed]
    [Google Scholar]
  110. Patriarchi A., Fox A., Maunsell B., Fanning S., Bolton D. ( 2011). Molecular characterization and environmental mapping of Campylobacter isolates in a subset of intensive poultry flocks in Ireland. Foodborne Pathog Dis 8:99–108 [View Article] [PubMed]
    [Google Scholar]
  111. Powell L. F., Lawes J. R., Clifton-Hadley F. A., Rodgers J., Harris K., Evans S. J., Vidal A. ( 2012). The prevalence of Campylobacter spp. in broiler flocks and on broiler carcases, and the risks associated with highly contaminated carcases. [View Article] [PubMed]
    [Google Scholar]
  112. Pritchard J. K., Stephens M., Donnelly P. ( 2000). Inference of population structure using multilocus genotype data. Genetics 155:945–959 [PubMed]
    [Google Scholar]
  113. 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 74:7715–7722 [View Article] [PubMed]
    [Google Scholar]
  114. Ridley A. M., Morris V. K., Cawthraw S. A., Ellis-Iversen J., Harris J. A., Kennedy E. M., Newell D. G., Allen V. M. ( 2011). Longitudinal molecular epidemiological study of thermophilic campylobacters on one conventional broiler chicken farm. Appl Environ Microbiol 77:98–107 [View Article] [PubMed]
    [Google Scholar]
  115. Rotariu O., Dallas J. F., Ogden I. D., MacRae M., Sheppard S. K., Maiden M. C., Gormley F. J., Forbes K. J., Strachan N. J. ( 2009). Spatiotemporal homogeneity of Campylobacter subtypes from cattle and sheep across northeastern and southwestern Scotland. Appl Environ Microbiol 75:6275–6281 [View Article] [PubMed]
    [Google Scholar]
  116. Rotariu O., Smith-Palmer A., Cowden J., Bessell P. R., Innocent G. T., Reid S. W. J., Matthews L., Dallas J., Ogden I. D. & other authors ( 2010). Putative household outbreaks of campylobacteriosis typically comprise single MLST genotypes. Epidemiol Infect 138:1744–1747 [View Article] [PubMed]
    [Google Scholar]
  117. Sails A. D., Swaminathan B., Fields P. I. ( 2003a). Utility of multilocus sequence typing as an epidemiological tool for investigation of outbreaks of gastroenteritis caused by Campylobacter jejuni . J Clin Microbiol 41:4733–4739 [View Article] [PubMed]
    [Google Scholar]
  118. Sails A. D., Swaminathan B., Fields P. I. ( 2003b). Clonal complexes of Campylobacter jejuni identified by multilocus sequence typing correlate with strain associations identified by multilocus enzyme electrophoresis. J Clin Microbiol 41:4058–4067 [View Article] [PubMed]
    [Google Scholar]
  119. Sanad Y. M., Kassem I. I., Abley M., Gebreyes W., LeJeune J. T., Rajashekara G. ( 2011). Genotypic and phenotypic properties of cattle-associated Campylobacter and their implications to public health in the USA. PLoS ONE 6:e25778 [View Article] [PubMed]
    [Google Scholar]
  120. Scallan E., Hoekstra R. M., Angulo F. J., Tauxe R. V., Widdowson M. A., Roy S. L., Jones J. L., Griffin P. M. ( 2011). Foodborne illness acquired in the United States – major pathogens. Emerg Infect Dis 17:7–15 [PubMed] [CrossRef]
    [Google Scholar]
  121. Schouls L. M., Reulen S., Duim B., Wagenaar J. A., Willems R. J., Dingle K. E., Colles F. M., Van Embden J. D. ( 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 41:15–26 [View Article] [PubMed]
    [Google Scholar]
  122. Selander R. K., Caugant D. A., Ochman H., Musser J. M., Gilmour M. N., Whittam T. S. ( 1986). Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol 51:873–884 [PubMed]
    [Google Scholar]
  123. Sheppard S. K., McCarthy N. D., Falush D., Maiden M. C. ( 2008). Convergence of Campylobacter species: implications for bacterial evolution. Science 320:237–239 [View Article] [PubMed]
    [Google Scholar]
  124. Sheppard S. K., Dallas J. F., MacRae M., McCarthy N. D., Sproston E. L., Gormley F. J., Strachan N. J., Ogden I. D., Maiden M. C., Forbes K. J. ( 2009a). Campylobacter genotypes from food animals, environmental sources and clinical disease in Scotland 2005/6. Int J Food Microbiol 134:96–103 [View Article] [PubMed]
    [Google Scholar]
  125. Sheppard S. K., Dallas J. F., Strachan N. J., MacRae M., McCarthy N. D., Wilson D. J., Gormley F. J., Falush D., Ogden I. D. & other authors ( 2009b). Campylobacter genotyping to determine the source of human infection. Clin Infect Dis 48:1072–1078 [View Article] [PubMed]
    [Google Scholar]
  126. Sheppard S. K., Maiden M. C. J., Falush D. ( 2010a). Population genetics of Campylobacter . Bacterial Population Genetics in Infectious Disease181–194 Robinson D. A., Falush D., Feil E. J. Hoboken, NJ: Wiley-Blackwell; [View Article]
    [Google Scholar]
  127. Sheppard S. K., Colles F., Richardson J., Cody A. J., Elson R., Lawson A., Brick G., Meldrum R., Little C. L. & other authors ( 2010b). Host association of Campylobacter genotypes transcends geographic variation. Appl Environ Microbiol 76:5269–5277 [View Article] [PubMed]
    [Google Scholar]
  128. Sheppard S. K., McCarthy N. D., Jolley K. A., Maiden M. C. J. ( 2011a). Introgression in the genus Campylobacter: generation and spread of mosaic alleles. Microbiology 157:1066–1074 [View Article] [PubMed]
    [Google Scholar]
  129. Sheppard S. K., Colles F. M., McCarthy N. D., Strachan N. J., Ogden I. D., Forbes K. J., Dallas J. F., Maiden M. C. ( 2011b). Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol Ecol 20:3484–3490 [View Article] [PubMed]
    [Google Scholar]
  130. Sheppard S. K., Jolley K. A., Maiden M. C. J. ( 2012). A gene-by-gene approach to bacterial population genomics: whole genome MLST of Campylobacter . Genes 3:261–277 [View Article]
    [Google Scholar]
  131. Skirrow M. B. ( 1977). Campylobacter enteritis: a “new” disease. BMJ 2:9–11 [View Article] [PubMed]
    [Google Scholar]
  132. Skirrow M. B., Jones D. M., Sutcliffe E., Benjamin J. ( 1993). Campylobacter bacteraemia in England and Wales, 1981-91. Epidemiol Infect 110:567–573 [View Article] [PubMed]
    [Google Scholar]
  133. Smith J. L., Fratamico P. M. ( 2010). Fluoroquinolone resistance in Campylobacter . J Food Prot 73:1141–1152 [PubMed]
    [Google Scholar]
  134. 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 12:1500–1507 [View Article] [PubMed]
    [Google Scholar]
  135. Sopwith W., Birtles A., Matthews M., Fox A., Gee S., James S., Kempster J., Painter M., Edwards-Jones V. & other authors ( 2010). Investigation of food and environmental exposures relating to the epidemiology of Campylobacter coli in humans in Northwest England. Appl Environ Microbiol 76:129–135 [View Article] [PubMed]
    [Google Scholar]
  136. Spencer S. E., Marshall J., Pirie R., Campbell D., Baker M. G., French N. P. ( 2012). The spatial and temporal determinants of campylobacteriosis notifications in New Zealand, 2001–2007. Epidemiol Infect 140:1663–1677 [View Article] [PubMed]
    [Google Scholar]
  137. Sproston E. L., Ogden I. D., MacRae M., Forbes K. J., Dallas J. F., Sheppard S. K., Cody A., Colles F., Wilson M. J., Strachan N. J. ( 2010). Multi-locus sequence types of Campylobacter carried by flies and slugs acquired from local ruminant faeces. J Appl Microbiol 109:829–838 [View Article] [PubMed]
    [Google Scholar]
  138. Sproston E. L., Ogden I. D., MacRae M., Dallas J. F., Sheppard S. K., Cody A. J., Colles F. M., Wilson M. J., Forbes K. J., Strachan N. J. ( 2011). Temporal variation and host association in the Campylobacter population in a longitudinal ruminant farm study. Appl Environ Microbiol 77:6579–6586 [View Article] [PubMed]
    [Google Scholar]
  139. Strachan N. J., Gormley F. J., Rotariu O., Ogden I. D., Miller G., Dunn G. M., Sheppard S. K., Dallas J. F., Reid T. M. & other authors ( 2009). Attribution of Campylobacter infections in northeast Scotland to specific sources by use of multilocus sequence typing. J Infect Dis 199:1205–1208 [View Article] [PubMed]
    [Google Scholar]
  140. Suerbaum S., Lohrengel M., Sonnevend A., Ruberg F., Kist M. ( 2001). Allelic diversity and recombination in Campylobacter jejuni . J Bacteriol 183:2553–2559 [View Article] [PubMed]
    [Google Scholar]
  141. Taboada E. N., van Belkum A., Yuki N., Acedillo R. R., Godschalk P. C., Koga M., Endtz H. P., Gilbert M., Nash J. H. ( 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 8:359 [View Article] [PubMed]
    [Google Scholar]
  142. Taboada E. N., Mackinnon J. M., Luebbert C. C., Gannon V. P., Nash J. H., Rahn K. ( 2008). Comparative genomic assessment of multi-locus sequence typing: rapid accumulation of genomic heterogeneity among clonal isolates of Campylobacter jejuni . BMC Evol Biol 8:229 [View Article] [PubMed]
    [Google Scholar]
  143. Tam C. C., O’Brien S. J., Tompkins D. S., Bolton F. J., Berry L., Dodds J., Choudhury D., Halstead F., Iturriza-Gómara M. & other authors ( 2012). Changes in causes of acute gastroenteritis in the United Kingdom over 15 years: microbiologic findings from 2 prospective, population-based studies of infectious intestinal disease. Clin Infect Dis 54:1275–1286 [View Article] [PubMed]
    [Google Scholar]
  144. Thakur S., Gebreyes W. A. ( 2005). Campylobacter coli in swine production: antimicrobial resistance mechanisms and molecular epidemiology. J Clin Microbiol 43:5705–5714 [View Article] [PubMed]
    [Google Scholar]
  145. Thakur S., White D. G., McDermott P. F., Zhao S., Kroft B., Gebreyes W., Abbott J., Cullen P., English L. & other authors ( 2009). Genotyping of Campylobacter coli isolated from humans and retail meats using multilocus sequence typing and pulsed-field gel electrophoresis. J Appl Microbiol 106:1722–1733 [View Article] [PubMed]
    [Google Scholar]
  146. van Bergen M. A., Dingle K. E., Maiden M. C., Newell D. G., van der Graaf-Van Bloois L., van Putten J. P., Wagenaar J. A. ( 2005). Clonal nature of Campylobacter fetus as defined by multilocus sequence typing. J Clin Microbiol 43:5888–5898 [View Article] [PubMed]
    [Google Scholar]
  147. Wang Y., Taylor D. E. ( 1990). Natural transformation in Campylobacter species. J Bacteriol 172:949–955 [PubMed]
    [Google Scholar]
  148. Wang X., Zhao S., Harbottle H., Tran T., Blickenstaff K., Abbott J., Meng J. ( 2011). Antimicrobial resistance and molecular subtyping of Campylobacter jejuni and Campylobacter coli from retail meats. J Food Prot 74:616–621 [View Article] [PubMed]
    [Google Scholar]
  149. Wassenaar T. M., Newell D. G. ( 2000). Genotyping of Campylobacter spp. Appl Environ Microbiol 66:1–9 [View Article] [PubMed]
    [Google Scholar]
  150. Williams N. J., Jones T. R., Leatherbarrow H. J., Birtles R. J., Lahuerta-Marin A., Bennett M., Winstanley C. ( 2010). Isolation of a novel Campylobacter jejuni clone associated with the bank vole, Myodes glareolus . Appl Environ Microbiol 76:7318–7321 [View Article] [PubMed]
    [Google Scholar]
  151. Wilson D. J., Gabriel E., Leatherbarrow A. J. H., Cheesbrough J., Gee S., Bolton E., Fox A., Fearnhead P., Hart C. A., Diggle P. J. ( 2008). Tracing the source of campylobacteriosis. PLoS Genet 4:e1000203 [View Article] [PubMed]
    [Google Scholar]
  152. Wilson D. J., Gabriel E., Leatherbarrow A. J., Cheesbrough J., Gee S., Bolton E., Fox A., Hart C. A., Diggle P. J., Fearnhead P. ( 2009). Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni . Mol Biol Evol 26:385–397 [View Article] [PubMed]
    [Google Scholar]
  153. Wirz S. E., Overesch G., Kuhnert P., Korczak B. M. ( 2010). Genotype and antibiotic resistance analyses of Campylobacter isolates from ceca and carcasses of slaughtered broiler flocks. Appl Environ Microbiol 76:6377–6386 [View Article] [PubMed]
    [Google Scholar]
  154. Zautner A. E., Herrmann S., Corso J., Tareen A. M., Alter T., Gross U. ( 2011). Epidemiological association of different Campylobacter jejuni groups with metabolism-associated genetic markers. Appl Environ Microbiol 77:2359–2365 [View Article] [PubMed]
    [Google Scholar]
  155. Zhang Q., Meitzler J. C., Huang S., Morishita T. ( 2000). Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect Immun 68:5679–5689 [View Article] [PubMed]
    [Google Scholar]
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