1887

Abstract

causes gastroenteritis with a variety of symptoms in humans. In the absence of a suitable animal model, models have been used to study virulence traits such as invasion and toxin production. In this study, 113 isolates from poultry and poultry-related (=74) environments as well as isolates from human cases (=39) of campylobacteriosis and bacteraemia were tested for invasiveness using INT 407 cells. The method was sufficiently reproducible to observe a spectrum of invasiveness amongst strains. As a result, strains were classified as low, high and hyper-invasive. The majority of strains (poultry and human) were low invaders (82 % and 88 %, respectively). High invasion was found for 5 % of human strains and 11 % of poultry-related isolates. However, only 1 % of poultry strains were classified as hyperinvasive compared to 13 % of human isolates (=0.0182). Of those isolates derived from the blood of bacteraemic patients, 20 % were hyperinvasive, though this correlation was not statistically significant. An attempt was made to correlate invasiveness with the presence of seven genes previously reported to be associated with virulence. Most of these genes did not correlate with invasiveness, but gene was weakly over-represented, and a negative correlation was observed for the gene . This trend was stronger when the two genes were analysed together, thus was over-represented in high and hyperinvasive strains, with low invaders more commonly found to lack these genes (=0.0064).

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2008-05-01
2024-04-19
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References

  1. AbuOun M., Manning G., Cawthraw S. A., Ridley A. M., Ahmed I. H., Wassenaar T. M., Newell D. G. 2005; Cytolethal distending toxin (CDT)-negative Campylobacter jejuni strains and anti-CDT neutralizing antibodies induced during human infection but not chicken colonization. Infect Immun 73:3053–3062 [CrossRef]
    [Google Scholar]
  2. Adak G. K., Meakins S. M., Yip H., Lopman B. A., O'Brien S. J. 2005; Disease risks from foods, England and Wales, 1996–2000. Emerg Infect Dis 11:365–372 [CrossRef]
    [Google Scholar]
  3. Augeron C., Voisin T., Maoret J. J., Berthon B., Laburthe M., Laboisse C. L. 1992; Neurotensin and neuromedin N stimulate mucin output from human goblet cells (Cl.16E) via neurotensin receptors. Am J Physiol 262:G470–G476
    [Google Scholar]
  4. Bacon D. J., Alm R. A., Burr D. H., Hu L., Kopecko D. J., Ewing C. P., Trust T. J., Guerry P. 2000; Involvement of a plasmid in virulence of Campylobacter jejuni 81–176. Infect Immun 68:4384–4390 [CrossRef]
    [Google Scholar]
  5. Bacon D. J., Alm R. A., Hu L., Hickey T. E., Ewing C. P., Batchelor R. A., Trust T. J., Guerry P. 2002; DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81–176. Infect Immun 70:6242–6250 [CrossRef]
    [Google Scholar]
  6. Bang D. D., Scheutz F., Ahrens P., Pedersen K., Blom J., Madsen M. 2001; Prevalence of cytolethal distending toxin ( cdt ) genes and CDT production in Campylobacter spp. isolated from Danish broilers. J Med Microbiol 50:1087–1094
    [Google Scholar]
  7. Bang D. D., Nielsen E. M., Scheutz F., Pedersen K., Handberg K., Madsen M. 2003; PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates. J Appl Microbiol 94:1003–1014 [CrossRef]
    [Google Scholar]
  8. Biswas D., Itoh K., Sasakawa C. 2000; Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol 29:203–211 [CrossRef]
    [Google Scholar]
  9. Boudeau J., Glasser A. L., Masseret E., Joly B., Darfeuille-Michaud A. 1999; Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 67:4499–4509
    [Google Scholar]
  10. Bras A. M., Ketley J. M. 1999; Transcellular translocation of Campylobacter jejuni across human polarised epithelial monolayers. FEMS Microbiol Lett 179:209–215 [CrossRef]
    [Google Scholar]
  11. Carvalho A. C. T., Ruiz-Palacios G. M., Ramoscervantes P., Cervantes L. E., Pickering L. K. 2001; Molecular characterisation of invasive and non invasive Campylobacter jejuni and Campylobacter coli isolates. J Clin Microbiol 39:1353–1359 [CrossRef]
    [Google Scholar]
  12. Cawthraw S. A., Lind L., Kaijser B., Newell D. G. 2000; Antibodies, directed towards Campylobacter jejuni antigens, in sera from poultry abattoir workers. Clin Exp Immunol 122:55–60 [CrossRef]
    [Google Scholar]
  13. Coote J. G., Stewart-Tull D. E., Owen R. J., Bolton F. J., Siemer B. L., Candlish D., Thompson D. H., Wardlaw A. C., On S. L. other authors 2007; Comparison of virulence-associated in vitro properties of typed strains of Campylobacter jejuni from different sources. J Med Microbiol 56:722–732 [CrossRef]
    [Google Scholar]
  14. Datta S., Niwa H., Itoh K. 2003; Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains from humans, poultry meat and broiler and bovine faeces. J Med Microbiol 52:345–348 [CrossRef]
    [Google Scholar]
  15. De Melo M. A., Gabbiani G., Pechère J.-C. 1989; Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun 57:2214–2222
    [Google Scholar]
  16. Dingle K. E., Colles F. M., Wareing D. R., Ure R., Fox A. J., Bolton F. E., Bootsma H. J., Willems R. J., Urwin R., Maiden M. C. 2001; Multilocus sequence typing system for Campylobacter jejuni . J Clin Microbiol 39:14–23 [CrossRef]
    [Google Scholar]
  17. Dorrell N., Mangan J. A., Laing K. G., Hinds J., Linton D., Al-Ghusein H., Barrel B. G., Parkhill J., Stoker N. G. other authors 2001; Whole genome comparison of Campylobacter jejuni isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res 11:1706–1715 [CrossRef]
    [Google Scholar]
  18. Elsinghorst E. A. 1994; Measurement of invasion by gentamicin resistance. Methods Enzymol 236:405–420
    [Google Scholar]
  19. Everest P. H., Goossens H., Butzler J. P., Lloyd D., Knutton S., Ketley J. M., Williams P. H. 1992; Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli . J Med Microbiol 37:319–325 [CrossRef]
    [Google Scholar]
  20. Eyigor A., Dawson K. A., Langlois B. E., Pickett C. L. 1999; Detection of cytolethal distending toxin activity and cdt genes in Campylobacter spp. isolated from chicken carcasses. Appl Environ Microbiol 65:1501–1505
    [Google Scholar]
  21. Fauchère J. L., Rosenau A., Veron M., Moyen E. N., Richard S., Pfister A. 1986; Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces. Infect Immun 54:283–287
    [Google Scholar]
  22. Fernandez H., Trabulsi L. R. 1995; Invasive and enterotoxic properties in Campylobacter jejuni and Campylobacter coli strains isolated from humans and animals. Biol Res 28:205–210
    [Google Scholar]
  23. Finlay B. B., Falkow S. 1990; Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis 162:1096–1106 [CrossRef]
    [Google Scholar]
  24. Food Standards Agency. 2007 A Report of the Study of Infectious Intestinal Disease in England London: The Stationary Office;
    [Google Scholar]
  25. Fouts D. E., Mongodin E. F., Mandrell R. E., Miller W. G., Rasko D. A., Ravel J., Brinkac L. M., DeBoy R. T., Parker C. T. other authors 2005; Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol 3:e15 [CrossRef]
    [Google Scholar]
  26. Friis L. M., Pin C., Pearson B. M., Wells J. M. 2005; In vitro cell culture methods for investigating Campylobacter invasion mechanisms. J Microbiol Methods 61:145–160 [CrossRef]
    [Google Scholar]
  27. Gaynor E. C., Cawthraw S., Manning G., MacKichan J. K., Falkow S., Newell D. G. 2004; The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J Bacteriol 186:503–517 [CrossRef]
    [Google Scholar]
  28. Hänel I., Borrmann E., Müller J., Alter T. 2007; Relationships between bacterial genotypes and in vitro virulence properties of Campylobacter jejuni and Campylobacter coli isolated from turkeys. J Appl Microbiol 102:433–441
    [Google Scholar]
  29. Hofreuter D., Tsai J., Watson R. O., Novik V., Altman B., Benitez M., Clark C., Perbost C., Jarvie T. other authors 2006; Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74:4694–4707 [CrossRef]
    [Google Scholar]
  30. Honma Y., Sasakawa C., Tsuji T., Iwanaga M. 2000; Effect of erythromycin on Shigella infection of Caco-2 cells. FEMS Immunol Med Microbiol 27:139–145 [CrossRef]
    [Google Scholar]
  31. Huang X. Z., Tall B., Schwan W., Kopecko D. J. 1998; Salmonella typhi entry into intestinal epithelial cells. Jpn J Med Sci Biol 51 (Suppl.), S90: [CrossRef]
    [Google Scholar]
  32. Hugdahl M. B., Beery J. T., Doyle M. P. 1988; Chemotactic behavior of Campylobacter jejuni . Infect Immun 56:1560–1566
    [Google Scholar]
  33. Johnson W. M., Lior H. 1986; Cytotoxic and cytotonic factors produced by Campylobacter jejuni , Campylobacter coli , and Campylobacter laridis . J Clin Microbiol 24:275–281
    [Google Scholar]
  34. Jorgensen F., Bailey R., Williams S., Henderson P., Wareing D. R., Bolton F. J., Frost J. A., Ward L., Humphrey T. J. 2002; Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int J Food Microbiol 76:151–164 [CrossRef]
    [Google Scholar]
  35. Koenraad P. M., Ayling R., Hazeleger W. C., Rombouts F. M., Newell D. G. 1995; The speciation and subtyping of Campylobacter isolates from sewage plants and waste water from a connected poultry abattoir using molecular techniques. Epidemiol Infect 115:485–494 [CrossRef]
    [Google Scholar]
  36. Konkel M. E., Joens L. A. 1989; Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect Immun 57:2984–2990
    [Google Scholar]
  37. Konkel M. E., Mead D. J., Hayes S. F., Cieplak W. Jr 1992; Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J Infect Dis 166:308–315 [CrossRef]
    [Google Scholar]
  38. Konkel M. E., Garvis S. G., Tipton S. L., Anderson D. E. Jr, Cieplak W. Jr 1997; Identification and molecular cloning of a gene encoding a fibronectin-binding protein ( Cad F) from Campylobacter jejuni . Mol Microbiol 24:953–963 [CrossRef]
    [Google Scholar]
  39. Konkel M. E., Kim B. J., Rivera-Amill V., Garvis S. G. 1999; Bacterial secreted proteins are required for the internalisation of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol 32:691–701 [CrossRef]
    [Google Scholar]
  40. Krause-Gruszczynska M., Rohde M., Hartig R., Genth H., Schmidt G., Keo T., Konig W., Miller W. G., Konkel M. E. other authors 2007; Role of the small Rho GTPases Rac1 and Cdc42 in host cell invasion of Campylobacter jejuni . Cell Microbiol 9:2431–2444 [CrossRef]
    [Google Scholar]
  41. Lee A., O'Rourke J. L., Barrington P. J., Trust T. J. 1986; Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni : a mouse cecal model. Infect Immun 51:536–546
    [Google Scholar]
  42. Lindblom G. B., Cervantes L. E., Sjogren E., Kaijser B., Ruiz-Palacios G. M. 1990; Adherence, enterotoxigenicity, invasiveness and serogroups in Campylobacter jejuni and Campylobacter coli strains from adult humans with acute enterocolitis. APMIS 98:179–184 [CrossRef]
    [Google Scholar]
  43. Manninen K. I., Prescott J. F., Dohoo I. R. 1982; Pathogenicity of Campylobacter jejuni isolates from animals and humans. Infect Immun 38:46–52
    [Google Scholar]
  44. Manning G., Dowson C. G., Bagnall M. C., Ahmed I. H., West M., Newell D. G. 2003a; Multilocus sequence typing for comparison of veterinary and human isolates of Campylobacter jejuni . Appl Environ Microbiol 69:6370–6379 [CrossRef]
    [Google Scholar]
  45. Manning G., Grant A. J., Fearnley C., Woodall C. A., Coward C., Wassenaar T. M., Maskell D. J., Newell D. G. 2003b; Transposon mutagenesis in a hyperinvasive, clinical isolate of Campylobacter jejuni reveals mutants with reduced invasion, but not motility. Int J Med Microbiol 293:76
    [Google Scholar]
  46. Müller J., Schulze F., Müller W., Hänel I. 2006; PCR detection of virulence-associated genes in Campylobacter jejuni strains with differential ability to invade Caco-2 cells and to colonize the chick gut. Vet Microbiol 113:123–129 [CrossRef]
    [Google Scholar]
  47. Newell D. G. 2002; The ecology of Campylobacter jejuni in avian and human hosts and in the environment. Int J Infect Dis 6 (Suppl. 3):S16–S21
    [Google Scholar]
  48. Newell D. G., Pearson A. 1984; The invasion of epithelial cell lines and the intestinal epithelium of infant mice by Campylobacter jejuni / coli . J Diarrhoeal Dis Res 2:19–26
    [Google Scholar]
  49. Newell D. G., McBride H., Saunders F., Dehele Y., Pearson A. D. 1985; The virulence of clinical and environmental isolates of Campylobacter jejuni . J Hyg (Lond) 94:45–54 [CrossRef]
    [Google Scholar]
  50. Oelschlaeger T. A., Guerry P., Kopecko D. J. 1993; Unusual microtubule-dependent endocytosis mechanisms triggered by Campylobacter jejuni and Citrobacter freundii . Proc Natl Acad Sci U S A 90:6884–6888 [CrossRef]
    [Google Scholar]
  51. Palmer S. R., Gully P. R., White J. M., Pearson A. D., Suckling W. G., Jones D. M., Rawes J. C., Penner J. L. 1983; Water-borne outbreak of Campylobacter gastroenteritis. Lancet 1:287–290
    [Google Scholar]
  52. Parkhill J., Wren B. W., Mungall K., Ketley J. M., Churcher C., Basham D., Chillingworth T., Davies R. M., Feltwell T. other authors 2000; The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [CrossRef]
    [Google Scholar]
  53. Pearson B. M., Pin C., Wright J., I'Anson K., Humphrey T., Wells J. M. 2003; Comparative genome analysis of Campylobacter jejuni using whole genome microarrays. FEBS Lett 554:224–230 [CrossRef]
    [Google Scholar]
  54. Pearson B. M., Gaskin D. J., Segers R. P., Wells J. M., Nuijten P. J., Mvan Vliet A. H. 2007; The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J Bacteriol 189:8402–8403 [CrossRef]
    [Google Scholar]
  55. Pepe J. C., Miller V. L. 1993; Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A 90:6473–6477 [CrossRef]
    [Google Scholar]
  56. Rivera-Amill V., Konkel M. E. 1999; Secretion of Campylobacter jejuni Cia proteins is contact dependent. Adv Exp Med Biol 473:225–229
    [Google Scholar]
  57. Rozynek E., Dzierzanowska-Fangrat K., Jozwiak P., Popowski J., Korsak D., Dzierzanowska D. 2005; Prevalence of potential virulence markers in Polish Campylobacter jejuni and Campylobacter coli isolates obtained from hospitalized children and from chicken carcasses. J Med Microbiol 54:615–619 [CrossRef]
    [Google Scholar]
  58. Ruiz-Palacios G. M., Cervantes L. E., Newell D. G., Lopez-Vidal Y., Calva J. J. 2007; In vitro models for studying campylobacter infections. In Campylobacter jejuni: Current Status and Future Trends Edited by Nachamkin I., Blaser M. J., Tompkins L. S. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  59. Russell R. G., Blake D. C. Jr 1994; Cell association and invasion of Caco-2 cells by Campylobacter jejuni . Infect Immun 62:3773–3779
    [Google Scholar]
  60. Russell R. G., O'Donnoghue M., Blake D. C., Zulty J., DeTolla L. J. 1993; Early colonic damage and invasion of Campylobacter jejuni in experimentally challenged infant Macaca mulatta. J Infect Dis 168:210–215 [CrossRef]
    [Google Scholar]
  61. Tay S. T., Devi S., Pthucheary S., Kautner I. 1996; In vitro demonstration of the invasive ability of Campylobacters. Zentralbl Bakteriol 283:306–313 [CrossRef]
    [Google Scholar]
  62. Tompkins D. S., Hudson M. J., Smith H. R., Eglin R. P., Wheeler J. G., Brett M. M., Owen R. J., Brazier J. S., Cumberland P., other authors Jr. 1999; A study of infectious intestinal disease in England: microbiological findings in cases and controls. Commun Dis Public Health 2:108–113
    [Google Scholar]
  63. Wassenaar T. M., Blaser M. 1999; Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1:1023–1033 [CrossRef]
    [Google Scholar]
  64. Wassenaar T. M., Bleumink-Pluym N. M. C., van der Zeijst B. A. M. 1991; Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrate that flaA but not flaB is required for invasion. EMBO J 10:2055–2061
    [Google Scholar]
  65. Zheng J., Meng J., Zhao S., Singh R., Song W. 2006; Adherence to and invasion of human intestinal epithelial cells by Campylobacter jejuni and Campylobacter coli isolates from retail meat products. J Food Prot 69:768–774
    [Google Scholar]
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