Characterization of the campylobacter jejuni population in the barnacle geese reservoir

Zoonoses and Public Health

Volumn 62, Issue 3, 2015, Pages 209-221

  Llarena, A K ^a   Skarp de Haan, C P A ^a   Rossi, M ^a   Hanninen M L ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

MLST; Barnacle geese; Campylobacter jejuni; ClonalFrame; Full genome sequencing

Indexed keywords

CIPROFLOXACIN; ERYTHROMYCIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; TETRACYCLINE; BACTERIAL DNA;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENOME; BACTERIUM ISOLATE; BACTERIUM ISOLATION; BARNACLE; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; CLONAL VARIATION; CROSS-SECTIONAL STUDY; FECES ANALYSIS; GENE SEQUENCE; GOOSE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MINIMUM INHIBITORY CONCENTRATION; MONOPHYLY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; STRUCTURE ANALYSIS; ANIMAL; BACTERIUM IDENTIFICATION; CAMPYLOBACTER INFECTIONS; CHEMISTRY; DISEASE CARRIER; DNA SEQUENCE; FECES; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PREVALENCE; VETERINARY; ZOONOSIS;

ANATIDAE; BACTERIA (MICROORGANISMS); BRANTA LEUCOPSIS; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BASE SEQUENCE; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; DISEASE RESERVOIRS; DNA, BACTERIAL; FECES; GEESE; HUMANS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; PREVALENCE; SEQUENCE ANALYSIS, DNA; ZOONOSES;

EID: 84926221346     PISSN: 18631959     EISSN: 18632378     Source Type: Journal    
DOI: 10.1111/zph.12141     Document Type: Article

References (59)

1. Abascal, F., R. Zardoya, and M. J. Telford, 2010: TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38, W7-W13.
2. Allen, H. K., J. Donato, H. H. Wang, K. A. Cloud-Hansen, J. Davies, and J. Handelsman, 2010: Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251-259.
3. Aydin, F., H. I. Atabay, and M. Akan, 2001: The isolation and characterization of Campylobacter jejuni subsp. jejuni from domestic geese (Anser anser). J. Appl. Microbiol. 90, 637-642.
4. Aziz, R. K., D. Bartels, A. A. Best, M. DeJongh, T. Disz, R. A. Edwards, K. Formsma, S. Gerdes, E. M. Glass, M. Kubal, F. Meyer, G. J. Olsen, R. Olson, A. L. Osterman, R. A. Overbeek, L. K. McNeil, D. Paarmann, T. Paczian, B. Parrello, G. D. Pusch, C. Reich, R. Stevens, O. Vassieva, V. Vonstein, A. Wilke, and O. Zagnitko, 2008: The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9, 75.
5. Blaser, M., and J. Engberg, 2008: Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In: Nachamkin, I., C. Szymanski, and M. J. Blaser (eds), Campylobacter. ASM Press, Washington, DC.
6. Broman, T., H. Palmgren, S. Bergstrom, M. Sellin, J. Waldenström, M. L. Danielsson-Tham, and B. Olsen, 2002: Campylobacter jejuni in black-headed gulls (Larus ridibundus): prevalence, genotypes, and influence on C. jejuni epidemiology. J. Clin. Microbiol. 40, 4594-4602.
7. Burton, M., and R. Burton, 1988: Barnacle Goose. In: Hoare, B. (ed.), The International Wildlife Encyclopedia, vol 1. Brown Parn, New York, USA.
8. Bywater, R., H. Duluyker, E. Deroover, A. de Jong, H. Marion, M. McConville, T. Rowan, T. Shryock, D. Shuster, V. Thomas, M. Vallé, and J. Walters, 2004: A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals. J. Antimicrob. Chemother. 54, 744-754.
9. CLSI (Clinical and Laboratory Standards Institute), 2008: Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard-third editions. CLSI document M31-A3 (ISBN 1-56238-659-X) 28.
10. Colles, F. M., K. Jones, R. M. Harding, and C. J. Maiden, 2003: Genetic diversity of Campylobacter jejuni isolates from farm animals and the farm environment. Appl. Environ. Microbiol. 69, 7409-7413.
11. Colles, F. M., K. E. Dingle, A. J. Cody, and C. J. Maiden, 2008: 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.
12. Colles, F., N. McCarthy, J. C. Howe, C. L. Devereux, A. G. Gosler, and C. J. Maiden, 2009: Dynamics of Campylobacter colonization of a natural host, Sturnus vulgaris (European Starling). Environ. Microbiol. 11, 258-269.
13. Colles, F., J. S. Ali, S. K. Sheppard, N. McCarthy, and C. J. Maiden, 2011: Campylobacter populations in wild and domesticated Mallard ducks (Anas platyrhynchos). Environ. Microbiol. Rep. 3, 574-580.
14. Corander, J., P. Waldmann, and M. J. Sillanpaa, 2003: Bayesian analysis of genetic differentiation between populations. Genetics 163, 367-374.
15. Corander, J., P. Marttinen, J. Siren, and J. Tang, 2008: Enhanced bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539.
16. Denis, M., C. Soumet, K. Rivoal, G. Ermel, D. Blivet, G. Salvat, and P. Colin, 1999: Development of a m-PCR assay for simultaneous identification of Campylobacter jejuni and C. coli. Lett. Appl. Microbiol. 29, 406-410.
17. Didelot, X., and D. Falush, 2007: Inference of bacterial microevolution using multilocus sequence data. Genetics 175, 1251-1266.
18. Dingle, K. E., F. M. Colles, D. R. Wareing, R. Ure, A. J. Fox, F. E. Bolton, H. J. Bootsma, R. J. Willems, R. Urwin, and C. J. Maiden, 2001: Multilocus sequence typing system for Campylobacter jejuni. J. Clin. Microbiol. 39, 14-23.
19. EFSA (European Food Safety Authority), 2013: The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J. 11, 3129.
20. EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control), 2013: The European Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2011. EFSA J. 11, 3196.
21. Excofficer, L., and H. Lischer, 2010: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567.
22. Fajo-Pascual, M., P. Godoy, M. Ferrero-Cancer, and K. Wymore, 2010: Case-control study of risk factors for sporadic Campylobacter infections in northeastern Spain. Eur. J. Public Health 20, 443-448.
23. Griekspoor, P., F. Colles, N. McCarthy, P. M. Hansbro, C. Ashhurst-Smith, B. Olsen, D. Hasselquist, C. J. Maiden, and J. Waldenström, 2013: Marked host specificity and lack of phylogeographic population structure of Campylobacter jejuni in wild birds. Mol. Ecol. 22, 1463-1472.
24. Griggs, D. J., M. M. Johnson, J. A. Frost, T. Humphrey, F. Jorgensen, and L. J. Piddock, 2005: Incidence and mechanism of ciprofloxacin resistance in Campylobacter spp. isolated from commercial poultry flocks in the United Kingdom before, during, and after fluoroquinolone treatment. Antimicrob. Agents Chemother. 49, 699-707.
25. Gripp, E., D. Hlahla, X. Didelot, F. Kops, S. Maurischat, K. Tedin, T. Alter, L. Ellerbroek, K. Schreiber, D. Schomburg, T. Janssen, P. Bartholomaus, D. Hofreuter, S. Woltemate, M. Uhr, B. Brenneke, P. Gruening, G. Gerlach, L. Wieler, S. Suerbaum, and C. Josenhans, 2011: Closely related Campylobacter jejuni strains from different sources reveal a generalist rather than a specialist lifestyle. BMC Genomics 12, 584.
26. de Haan, C. P., R. Kivistö, M. Hakkinen, H. Rautelin, and M. L. Hänninen, 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.
27. de Haan, C. P., R. Kivistö, M. Hakkinen, J. Corander, and M. L. Hänninen, 2010b: Multilocus sequence types of Finnish bovine Campylobacter jejuni isolates and their attribution to human infections. BMC Microbiol. 10, 200.
28. de Haan, C. P., A. K. Llarena, J. Revez, and M. L. Hänninen, 2012: Association of Campylobacter jejuni metabolic traits with multilocus sequence types. Appl. Environ. Microbiol. 78, 5550-5554.
29. de Haan, C. P., K. Lampén, J. Corander, and M. L. Hänninen, 2013: Multilocus sequence types of environmental Campylobacter jejuni isolates and their similarities to those of human, poultry and bovine C. jejuni isolates. Zoonoses Public Health 60, 125-133.
30. Hakkinen, M., H. Heiska, and M. L. Hänninen, 2007: Prevalence of Campylobacter spp. in cattle in Finland and antimicrobial susceptibilities of bovine Campylobacter jejuni strains. Appl. Environ. Microbiol. 73, 3232-3238.
31. Hammer, Ø., D. A. T. Harper, and P. D. Ryan, 2001: PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontol. Elect. 4, 1-9.
32. Huson, D. H., and D. Bryant, 2006: Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254-267.
33. Jaakola, S., O. Lyytikäinen, R. Rimhanen-Finne, S. Salmilinna, J. Vuopio, M. Roivainen, H. Nohynek, J. Löflund, M. Kuusi, and P. Ruutu, 2013: Tartuntatauti Suomessa 2012. THL Raportti. 10, 15-16.
34. Kapperud, G., G. Espeland, E. Wahl, A. Walde, H. Herikstad, S. Gustavsen, I. Tveit, O. Natas, L. Bevanger, and A. Digranes, 2003: Factors associated with increased and decreased risk of Campylobacter infection: a prospective case-control study in Norway. Am. J. Epidemiol. 158, 234-242.
35. Kärenlämpi, R., H. Rautelin, D. Schönberg-Norio, L. Paulin, and M. L. Hänninen, 2007: Longitudinal study of Finnish Campylobacter jejuni and C. coli isolates from humans, using multilocus sequence typing, including comparison with epidemiological data and isolates from poultry and cattle. Appl. Environ. Microbiol. 73, 148-155.
36. Katoh, K., and D. M. Standley, 2013: MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.
37. Keller, J. I., and W. G. Shriver, 2013: Prevalence of three Campylobacter Species, C. jejuni, C. coli and C. lari, using multilocus sequence typing in wild birds of the Mid-Atlantic region, USA. J. Wildl. Dis. 50, 31-41.
38. Korczak, B. M., M. Zurfluh, S. Emler, J. Kuhn-Oertli, and P. Kuhnert, 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.
39. Lehtopolku, M., P. Kotilainen, P. Puukka, U. M. Nakari, A. Siitonen, E. Eerola, P. Huovinen, and A. J. Hakanen, 2012: Inaccuracy of the disk diffusion method compared with the agar dilution method for susceptibility testing of Campylobacter spp. J. Clin. Microbiol. 50, 52-56.
40. Li, L., C. J. Stoeckert, and D. S. Roos, 2003: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189.
41. Liu, K., C. R. Linder, and T. Warnow, 2011: RAxML and FastTree: comparing two methods for large-scale maximum likelihood phylogeny estimation. PLoS ONE 6, e27731.
42. Maiden, M. C., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. Zhou, K. Zurth, D. A. Caugant, I. M. Feavers, M. Achtman, and B. G. Spratt, 1998: Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95, 3140-3145.
43. Miller, W. G., S. L. On, G. Wang, S. Fontanoz, A. J. Lastovica, and R. E. Mandrell, 2005: Extended multilocus sequence typing system for Campylobacter coli, C. lari, C. upsaliensis and C. helveticus. J. Clin. Microbiol. 43, 2315-2329.
44. Moore, J. E., M. D. Barton, I. S. Blair, D. Corcoran, J. S. G. Dooley, S. Fanning, I. Kempf, A. J. Lastovica, C. J. Lowery, M. Matsuda, D. A. McDowell, A. McMahon, B. C. Millar, J. R. Rao, P. J. Rooney, B. S. Seal, W. J. Snelling, and O. Tolba, 2006: The epidemiology of antibiotic resistance in Campylobacter. Microbes Infect. 8, 1955-1966.
45. Price, M. N., P. S. Dehal, and A. P. Arkin, 2010: FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490.
46. Rutledge, M. D., R. Siletzky, W. Gu, L. A. Degerenes, C. E. Moorman, C. S. DePerno, and S. Kathariou, 2013: Characterization of Campylobacter from resident canada geese in an urban environment. J. Wildl. Dis. 49, 1-9.
47. Schönberg-Norio, D., J. Takkinen, M. L. Hänninen, M. L. Katila, S. S. Kaukoranta, L. Mattila, and H. Rautelin, 2004: Swimming and Campylobacter infections. Emerg. Infect. Dis. 10, 1474-1477.
48. Sheppard, S. K., J. F. Dallas, N. J. C. Strachan, M. MacRae, N. McCarthy, D. Wilson, G. J. Fraser, D. Falush, I. D. Ogden, C. J. Maiden, and K. J. Forbes, 2009: Campylobacter genotyping to determine the source of human infection. Clin. Infect. Dis. 48, 1072-1078.
49. Sheppard, S., F. Colles, N. McCarthy, N. J. C. Strachan, I. D. Ogden, K. J. Forbes, J. F. Dallas, and C. J. Maiden, 2011: Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Mol. Ecol. 20, 3484-3490.
50. Smeds, L., and A. Kunstner, 2011: ConDeTri-a content dependent read trimmer for Illumina data. PLoS ONE 6, e26314.
51. Sopwith, W., A. Birtles, M. Matthews, A. Fox, S. Gee, M. Painter, M. Regan, Q. Syed, and E. Bolton, 2008: Identification of potential environmentally adapted Campylobacter jejuni strain, United Kingdom. Emerg. Infect. Dis. 14, 1769-1773.
52. Strimmer, K., C. Wiuf, and V. Moulton, 2001: Recombination analysis using directed graphical models. Mol. Biol. Evol. 18, 97-99.
53. Taboadaa, E. N., S. L. Rossc, S. K. Mutschalla, J. M. MacKinnonb, M. J. Robertsa, C. J. Buchananc, P. Kruzkiewiczc, C. C. Jokinena, J. E. Thomasc, J. H. E. Nashb, V. P. J. Gannona, B. Marshalld, F. Pollarid, and C. G. Clarke, 2012: Development and validation of a comparative genomic fingerprinting method for high resolution genotyping of Campylobacter jejuni. J. Clin. Microbiol. 50, 788-797.
54. Tang, J., W. P. Hanage, C. Fraser, and J. Corander, 2009: Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Comput. Biol. 5, e1000455.
55. Valkama, J., and V. L. Vepsäläinen, 2011: Aleksi 2011: The Third Finnish Breeding Atlas. http://atlas3.lintuatlas.fi/english.
56. Varslot, M., J. Resell, and I. G. Fostad, 1996: Water-borne Campylobacter infection-probably caused by pink-footed geese. Two outbreaks in Nord-Tröndelag, Stjördal in 1994 and Verdal in 1995. Tidsskr. Nor. Laegeforen. 116, 3366-3369.
57. Waldenström, J., S. L. On, R. Ottvall, D. Hasselquist, and B. Olsen, 2007: Species diversity of campylobacteria in a wild bird community in Sweden. J. Appl. Microbiol. 102, 424-432.
58. Waldenström, J., D. Axelsson-Olsson, B. Olsen, D. Hasselquist, P. Griekspoor, L. Jansson, S. Teneberg, L. Svensson, and P. Ellström, 2010: Campylobacter jejuni colonization in wild birds: results from an infection experiment. PLoS ONE 5, e9082.
59. Wilson, D., G. Edith, A. J. Leatherbarrow, J. Cheesbrough, S. Gee, E. Bolton, A. Fox, P. Fearnhead, C. A. Hart, and P. J. Diggle, 2008: Tracing the source of Campylobacteriosis. PLoS Genet. 4, 1-9.