Korean Journal of Veterinary Research (대한수의학회지)

The Korean Society of Veterinary Science (대한수의학회)
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Prevalence of virulence and cytolethal distending toxin (CDT) genes in thermophilic Campylobacter spp. from dogs and humans in Gyeongnam and Busan, Korea

  • Cho, Hyun-Ho (Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Kim, Sang-Hyun (Viral infectious Disease Research Center, Korea Research Institute of Bioscience & Biotechnology) ;
  • Min, Wongi (College of Veterinary Medicine, Research Institute of Life Science, Institute of Animal medicine, Gyeongsang National University) ;
  • Ku, Bok-Kyung (Animal, Plant and Fisheries Quarantine and Inspection Agency) ;
  • Kim, Yong-Hwan (College of Veterinary Medicine, Research Institute of Life Science, Institute of Animal medicine, Gyeongsang National University)
  • Received : 2013.08.01
  • Accepted : 2014.03.10
  • Published : 2014.03.31
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Abstract

The prevalence of thermophilic Campylobacter (C.) spp. in stray, breeding, and household dogs was 25.2, 12.0, and 8.8%, respectively. C. jejuni and C. upsaliensis were the predominant Campylobacter spp. from household dogs. cdtA, cdtB, and cdtC were detected by PCR in all isolates. Despite the high cytolethal distending toxin (CDT) gene prevalence, only 26 (31%) C. jejuni strains and one (15.3%) C. coli strain showed evidence of CDT production in HEp-2 cell cytotoxicity assays. Virulence-associated genes detected in the C. jejuni and C. coli isolates were cadF, dnaJ, flaA, racR, ciaB, iamA, pldA, virB11, ceuE, and docC. cadF, dnaJ, flaA, and ceuE were found in all C. jejuni and C. coli isolates. When detecting Guillain-Barr$\acute{e}$ syndrome-associated genes (galE, cgtB, and wlaN), galE was identified in all isolates. However, cgtB and wlaN were more prevalent in C. jejuni isolates from humans than those from dogs. Adherence and invasion abilities of the C. jejuni and C. coli strains were tested in INT-407 cells. A considerable correlation (adjusted $R^2$= 0.678) existed between adherence and invasion activities of the Campylobacter spp. isolates.

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References

  1. Allos BM. Campylobcter jejuni infections: update on emerging issues and trends. Clin Infect Dis 2001, 32, 1201-1206. https://doi.org/10.1086/319760
  2. Anderson JD, MacNab AJ, Gransden WR, Damm SM, Johnson WM, Lior H. Gastroenteritis and encephalopathy associated with a strain of Escherichia coli O55:K59:H4 that produced a cytolethal distending toxin. Pediatr Infect Dis J 1987, 6, 1135-1136. https://doi.org/10.1097/00006454-198712000-00015
  3. Asakura M, Samosornsuk W, Taguchi M, Kobayashi K, Misawa N, Kusumoto M, Nishimura K, Matsuhisa A, Yamasaki S. Comparative analysis of cytolethal distending toxin (cdt) genes among Campylobacter jejuni, C. coli and C. fetus strains. Microb Pathog 2007, 42, 174-183. https://doi.org/10.1016/j.micpath.2007.01.005
  4. Bacon DJ, Alm RA, Burr DH, Hu L, Kopecko DJ, Ewing CP, Trust TJ, Guerry P. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 2000, 68, 4384-4390. https://doi.org/10.1128/IAI.68.8.4384-4390.2000
  5. Bang DD, Scheutz F, Ahrens P, Pedersen K, Blom J, Madsen M. Prevalence of cytolethal distending toxin (cdt) genes and CDT production in Campylobacter spp. isolated from Danish broilers. J Med Microbiol 2001, 50, 1087-1094. https://doi.org/10.1099/0022-1317-50-12-1087
  6. Biswas D, Itoh K, Sasakawa C. Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol 2000, 29, 203-211. https://doi.org/10.1111/j.1574-695X.2000.tb01524.x
  7. Bras AM, Chatterjee S, Wren BW, Newell DG, Ketley JM. A Novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J Bacteriol 1999, 181, 3298-3302.
  8. Coker AO, Isokpehi RD, Thomas BN, Amisu KO, Obi CL. Human campylobacteriosis in developing countries. Emerg Infect Dis 2002, 8, 237-243. https://doi.org/10.3201/eid0803.010233
  9. Datta S, Niwa H, Itoh K. Prevalence of 11 pathogenic genes of Campylobacter jejuni by PCR in strains isolated from humans, poultry meat and broiler, and bovine faeces. J Med Microbiol 2003, 52, 345-348. https://doi.org/10.1099/jmm.0.05056-0
  10. Dingle KE, Van Den Braak N, Colles FM, Price LJ, Woodward DL, Rodgers FG, Endtz HP, Van Belkum A, Maiden MCJ. Sequence typing confirms that Campylobacter jejuni strains associated with Guillain-Barre and Miller-Fisher syndromes are of diverse genetic lineage, serotype, and flagella type. J Clin Microbiol 2001, 39, 3346-3349. https://doi.org/10.1128/JCM.39.9.3346-3349.2001
  11. Fernandez H, Martin R. Campylobacter intestinal carriage among stray and pet dogs. Rev Saude Publica 1991, 25, 473-475. https://doi.org/10.1590/S0034-89101991000600009
  12. Florin I, Antillon F. Production of enterotoxin and cytotoxin in Campylobacter jejuni strains isolated in Costa Rica. J Med Microbiol 1992, 37, 22-29. https://doi.org/10.1099/00222615-37-1-22
  13. Garcia Roderigez LA, Ruigomez A, Panes J. Acute gastroenteritis followed by an increased of risk of inflammatory bowel disease. Gastroenterology 2006, 130, 1588-1594. https://doi.org/10.1053/j.gastro.2006.02.004
  14. Gonzalez I, Grant KA, Richerdson PT, Park SF, Collins MD. Specific Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli by using a PCR test based on the ceuE gene encoding a putative virulence determinant. J Clin Microbiol 1997, 35, 759-763.
  15. Hald B, Pedersen K, Waino M, Jorgensen JC, Madsen M. Longitudinal study of the excretion patterns of thermophilic Campylobacter spp. in young pet dogs in Denmark. J Clin Microbiol 2004, 42, 2003-2012. https://doi.org/10.1128/JCM.42.5.2003-2012.2004
  16. Johnson WM, Lior H. Production of Shiga toxin and a cytolethal distending toxin (CLDT) by serogroups of Shigella spp. FEMS Microbiol Lett 1987, 48, 235-238. https://doi.org/10.1111/j.1574-6968.1987.tb02548.x
  17. Konkel ME, Gray SA, Kim BJ, Gravis SG, Yoon J. Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J Clin Microbiol 1999, 37, 510-517.
  18. Krutkiewicz A, Klimuszko D. Genotyping and PCR detection of potential virulence genes in Campylobacter jejuni and Campylobacter coli isolates from different sources in Poland. Folia Microbiol 2010, 55, 167-175. https://doi.org/10.1007/s12223-010-0025-6
  19. Kumar SS, Malladi V, Sankaran K, Haigh R, Williams P, Balakrishnan A. Extrusion of actin-positive strands from Hep-2 and Int 407 cells caused by outer membrane preparations of enteropathogenic Escherichia coli and specific attachment of wild type bacteria to the strands. Can J Microbiol 2001, 47, 727-734. https://doi.org/10.1139/w01-058
  20. Lastovica AJ, Skirrow MB. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli. In: Nachamkin I, Blaser MJ (eds.). Campylobacter. 2nd ed. pp. 89-120, ASM Press, Washington, 2000.
  21. Linton D, Gilbert M, Hitshen PG, Dell A, Morris HR, Wakarchuk WW, Gregson NA, Wren BW. Phase variation of a ${\beta}$-1,3 galactosyltransferase involved in generation of the ganglioside $GM_1$-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 2000, 37, 501-514.
  22. Muller J, Schulze F, Muller W, Hanel I. 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 2006, 113, 123-129. https://doi.org/10.1016/j.vetmic.2005.10.029
  23. Nawaz MS, Wang RF, Khan SA, Khan AA. Detection of galE gene by polymerase chain reaction in campylobacters associated with Guillain-Barre syndrome. Mol Cell Probes 2003, 17, 313-317. https://doi.org/10.1016/j.mcp.2003.08.002
  24. Pang JC, Lin JS, Tsai CC, Tsen HY. The presence of major world-wide clones for phage type 4 and 8 Salmonella enterica serovar Enteritidis and the evaluation of their virulence levels by invasiveness assays in vitro and in vivo. FEMS Microbiol Lett 2006, 263, 148-154. https://doi.org/10.1111/j.1574-6968.2006.00398.x
  25. Park SF, Richardson PT. Molecular characterization of a Campylobacter jejuni lipoprotein with homology to periplasmic siderophore-binding proteins. J Bacteriol 1995, 177, 2259-2264. https://doi.org/10.1128/jb.177.9.2259-2264.1995
  26. Pickett CL, Pesci EC, Cottle DL, Russell G, Erdem AN, Zeytin H. Prevalence of cytolethal distending toxin production in Campylobacter jejuni and relatedness of Campylobacter sp. cdtB genes. Infect Immun 1996, 64, 2070-2078.
  27. Richardson PT, Park SF. Enterochelin acquisition in Campylobacter coli: characterization of components of a binding-protein-dependent transport system. Microbiology 1995, 141, 3181-3191. https://doi.org/10.1099/13500872-141-12-3181
  28. Ripabelli G, Tamburro M, Minelli F, Leone A, Sammarco ML. Prevalence of virulence-associated genes and cytolethal distending toxin production in Campylobacter spp. isolated in Italy. Comp Immunol Microbiol Infect Dis 2010, 33, 355-364. https://doi.org/10.1016/j.cimid.2008.12.001
  29. Robinson RA, Pugh RN. Dogs, zoonosis and immunosuppression. J R Soc Promot Health 2002, 122, 95-98. https://doi.org/10.1177/146642400212200210
  30. Talukder KA, Aslam M, Islam Z, Azmi IJ, Dutta DK, Hossain S, Nur-E-Kamal A, Nair GB, Cravioto A, Sack DA, Endtz HP. Prevalence of virulence genes and cytolethal distending toxin production in Campylobacter jejuni isolates from diarrheal patients in Bangladesh. J Clin Microbiol 2008, 46, 1485-1488. https://doi.org/10.1128/JCM.01912-07
  31. Tsai HJ, Huang HC, Lin CM, Lien YY, Chou CH. Salmonellae and Campylobacters in household and stray dogs in northern Taiwan. Vet Res Commun 2007, 31, 931-939. https://doi.org/10.1007/s11259-007-0009-4
  32. Wassenaar TM. Toxin production by Campylobacter spp. Clin Microbiol Rev 1997, 10, 466-476.
  33. Wassenaar TM, van der Zeijst BAM, Ayling R, Newell DG. Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 1993, 139, 1171-1175. https://doi.org/10.1099/00221287-139-6-1171
  34. Whitehouse CA, Balbo PB, Pesci EC, Cottle DL, Mirabito PM, Pickett CL. Campylobacter jejuni cytolethal distending toxin causes a $G_2$-phase cell cycle block. Infect Immun 1998, 66, 1934-1940.

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