Phenotypic and genotypic characterizations of Campylobacter jejuni isolated from the broiler meat production process

Current Microbiology

Volumn 65, Issue 4, 2012, Pages 398-406

  Kudirkiene, Egle ^a   Cohn, Marianne Thorup ^b   Stabler, Richard A ^c   Strong, Philippa C R ^c   Serniene, Loreta ^a   Wren, Brendan W ^c   Nielsen, Eva Møller ^d   Malakauskas, Mindaugas ^a   Brøndsted, Lone ^b  

^a LITHUANIAN UNIVERSITY OF HEALTH SCIENCES   (Lithuania)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM ISOLATION; BIOFILM; CAMPYLOBACTER JEJUNI; CONTROLLED STUDY; CORRELATION ANALYSIS; DISINFECTION; DNA MICROARRAY; ENVIRONMENTAL STRESS; FOOD PROCESSING; GENOTYPE PHENOTYPE CORRELATION; INCUBATION TIME; MEAT; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SLAUGHTERHOUSE; TEMPERATURE;

ANIMALS; BIOFILMS; CAMPYLOBACTER JEJUNI; CHICKENS; CLUSTER ANALYSIS; COLONY COUNT, MICROBIAL; COMPARATIVE GENOMIC HYBRIDIZATION; FLAGELLIN; FOOD INDUSTRY; GENOTYPE; MEAT; MICROARRAY ANALYSIS; MICROBIAL VIABILITY; MULTILOCUS SEQUENCE TYPING; PHENOTYPE; PHYLOGENY; TEMPERATURE;

CAMPYLOBACTER JEJUNI;

EID: 84865994053     PISSN: 03438651     EISSN: 14320991     Source Type: Journal    
DOI: 10.1007/s00284-012-0170-z     Document Type: Article

References (58)

1. Allen VM, Bull SA, Corry JE, Domingue G, Jorgensen F, Frost JA, Whyte R, Gonzalez A, Elviss N, Humphrey TJ (2007) Campylobacter spp. contamination of chicken carcasses during processing in relation to flock colonisation. Int J Food Microbiol 113:54-61
2. Alter T, Gaull F, Froeb A, Fehlhaber K (2005) Distribution of Campylobacter jejuni strains at different stages of a turkey slaughter line. Food Microbiol 22:345-351
3. Annous BA, Fratamico PM, Smith JL (2009) Quorum sensing in biofilm: why do bacteria behave they do. J Food Sci 74:24-37
4. Anonymous (2011) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J 9:109-135
5. Bell JA, St Charles JL, Murphy AJ, Rathinam VA, Plovanich-Jones AE, Stanley EL, Wolf JE, Gettings JR, Whittam TS, Mansfield LS (2009) Multiple factors interact to produce responses resembling spectrum of human disease in Campylobacter jejuni infected C57BL/6 IL-10-/-mice. BMC Microbiol 9:57
6. Birk T, Ingmer H, Andersen MT, Jorgensen K, Brøndsted L (2004) Chicken juice, a food-based model system suitable to study survival of Campylobacter jejuni. Lett Appl Microbiol 38:66-71
7. Butler JL, Stewart JC, Vanderzant C, Carpenter ZL, Smith GC (1979) Attachment of microorganisms to pork skin and surfaces of beef and lamb carcasses. J Food Prot 42:401-406
8. Champion OL, Gaunt MW, Gundogdu O, Elmi A, Witney AA, Hinds J, Dorrell N, Wren BW (2005) Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc Natl Acad Sci USA 102:16043-16048
9. Chan KF, Tran HL, Kanenaka RY, Kathariou S (2001) Survival of clinical and poultry-derived isolates of Campylobacter jejuni at a low temperature (4°C). Appl Environ Microbiol 67:4186-4191
10. de Haan CP, Kivistö R, Hänninen ML (2010) Association of Campylobacter jejuni Cj0859c gene (fspA) variants with different C. jejuni multilocus sequence types. Appl Environ Microbiol 76:6942-6943
11. 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 39:14-23
12. Djordjevic SP, Unicomb LE, Adamson PJ, 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
13. Dorrell N, Mangan JA, Laing KG, Hinds J, Linton D, Al-Ghusein H, Barrell BG, Parkhill J, Stoker NG, Karlyshev AV, Butcher PD, Wren BW (2001) Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity. Genome Res 11:1706-1715
14. Flanagan RC, Neal-McKinney JM, Dhillon AS, Miller WG, Konkel ME (2009) Examination of Campylobacter jejuni putative adhesins leads to the identification of a new protein, designated FlpA, required for chicken colonization. Infect Immun 77:2399-2407
15. Flint SH, Brooks JD, Bremer PJ (1997) The influence of cell surface properties of thermophilic streptococci on attachment to stainless steel. J Appl Microbiol 83:508-517
16. Gilbert M, Godschalk P, Parker C, Endtz H, Wakarchuk WW (2005) Genetic basis for the variation in the lipooligosaccharide outer core of Campylobacter jejuni and possible association of glycosyltransferase genes with post-infectious neuropathies. In: Ketley J, Konkel ME (eds) Campylobacter jejuni: new perspectives in molecular and cellular biology. Horizon Scientific Press, Norfolk, pp 219-248
17. Gundogdu O, Mills DC, Elmi A, Martin MJ, Wren BW, Dorrell N (2011) The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J Bacteriol 193:4238-4249
18. Gunther NW, Chen C (2009) The biofilm forming potential of bacterial species in the genus Campylobacter. Food Microbiol 26:44-51
19. Habib I, Uyttendaele M, De Zutter L (2010) Survival of poultryderived Campylobacter jejuni of multilocus sequence type clonal complexes 21 and 45 under freeze, chill, oxidative, acid and heat stresses. Food Microbiol 27:829-834
20. Haddad N, Burns CM, Bolla JM, Prévost H, Fédérighi M, Drider D, Cappelier JM (2009) Long term survival of Campylobacter jejuni at low temperature is dependent on polynucleotide phosphorylase activity. Appl Environ Microbiol 75:7310-7318
21. Harrington CS, Thomson-Carter FM, Carter PE (1997) Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35:2386-2392
22. Harrington CS, Moran L, Ridley AM, Newell DG, Madden RH (2003) Inter-laboratory evaluation of three flagellin PCR/RFLP methods for typing Campylobacter jejuni and C. coli: the CAMPYNET experience. J Appl Microbiol 95:1321-1333
23. Hofreuter D, Tsai J, Watson RO, Novik V, Altman B, Benitez M, Clark C, Perbost C, Jarvie T, Du L, Galán JE (2006) Unique features of a highly pathogenic Campylobacter jejuni strain. Infect Immun 74:4694-4707
24. Humphrey T, O'Brien S, Madsen M (2007) Campylobacters as zoonotic pathogens: a food production perspective. Int J Food Microbiol 117:237-257
25. Jackson DN, Davis B, Tirado SM, Duggal M, van Frankenhuyzen JK, Deaville D, Wijesinghe MA, Tessaro M, Trevors JT (2009) Survival mechanisms and culturability of Campylobacter jejuni under stress conditions. Antonie Van Leeuwenhoek 96:377-394
26. Johnsen G, Kruse H, Hofshagen M (2006) Genotyping of Campylobacter jejuni from broiler carcasses and slaughterhouse environment by amplified fragment length polymorphism. Poult Sci 85:2278-2284
27. Jolley KA, Maiden MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinform 11:595
28. Jones MA, Marston KL, Woodall CA, Maskell DJ, Linton D, Karlyshev AV, Dorrell N, Wren BW, Barrow PA (2004) Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 72:3769-3776
29. Joshua GW, Guthrie-Irons C, Karlyshev AV, Wren BV (2006) Biofilm formation in Campylobacter jejuni. Microbiology 152:387-396
30. Kalmokoff M, Lanthier P, Tremblay TL, Foss M, Lau PC, Sanders G, Austin J, Kelly J, Szymanski CM (2006) Proteomicanalysis of Campylobacter jejuni 11168 biofilms reveals role for the motility complex in biofilm formation. J Bacteriol 188:4312-4320
31. Kanipes MI, Akelatis A, Guerry P, Monterio MA (2006) Mutation of waaC encoding heptosyltransferase I in Campylobacter jejuni 81-176 affects the structure of both lipooligosaccharide and capsular carbohydrate. J Bacteriol 188:3273-3279
32. Kanipes MI, Tan X, Akelaitis A, Li J, Rockabrand D, Guerry P, Monteiro MA (2008) Genetic analysis of lipooligosaccharide core biosynthesis in Campylobacter jejuni 81-176. J Bacteriol 190:1568-1574
33. Karlyshev AV, McCrossan MV, Wren BW (2001) Demonstration of polysaccharide capsule in Campylobacter jejuni using electron microscopy. Infect Immun 69:5921-5924
34. Karlyshev AV, Champion OL, Churcher C, Brisson JR, Jarrell HC, Gilbert M, Brochu D, St Michael F, Li J, Wakarchuk WW, Goodhead I, Sanders M, Stevens K, White B, Parkhill J, Wren BW, Szymanski CM (2005) Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol Microbiol 55:90-103
35. Kim CC, Joyce EA, Chan K, Falkow S (2002) Improved analytical methods for microarray-based genome-composition analysis. Genome Biol 3:1-17
36. Klein G, Beckmann L, Vollmer HM, Bartelt E (2007) Predominant strains of thermophilic Campylobacter spp. in a German poultry slaughterhouse. Int J Food Microbiol 117:324-328
37. Klena JD, Gray SA, Konkel ME (1998) Cloning, sequencing, and characterization of the lipopolysaccharide biosynthetic enzyme heptosyltransferase I gene (waaC) from Campylobacter jejuni and Campylobacter coli. Gene 222:177-185
38. Kudirkiene E, Malakauskas M, Malakauskas A, Bojesen AM, Olsen JE (2010) Demonstration of persistent strains of C. jejuni within broiler farms over one year period in Lithuania. J Appl Microbiol 108:868-877
39. Kudirkiene E, Bunevičiene J, Brøndsted L, Ingmer H, Olsen JE, Malakauskas M (2011) Evidence of broiler meat contamination with post-disinfection strains of Campylobacter jejuni from slaughterhouse. Int J Food Microbiol 145:S116-S120
40. Mead GC, Hudson WR, Hinton MH (1995) Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with campylobacter. Emerg Infect Dis 115: 495-500
41. Miller WG, Pearson BM, Wells JM, Parker CT, Kapitonov VV, Mandrell RE (2005) Diversity within the Campylobacter jejuni type I restriction-modification loci. Microbiology 151:337-351
42. Murphy C, Carroll C, Jordan KN (2006) Environmental survival mechanism of the foodborne pathogen Campylobacter jejuni. J Appl Microbiol 100:623-632
43. Naito M, Frirdich E, Fields JA, Pryjma M, Li J, Cameron A, Gilbert M, Thompson SA, Gaynor EC (2010) Effects of sequential Campylobacter jejuni 81-176 lipooligosaccharide core truncations on biofilm formation, stress survival, and pathogenesis. J Bacteriol 192:2182-2192
44. Newell DG (2002) The ecology of Campylobacter jejuni in avian and human hosts and in the environment. Int J Infect Dis 6:3516-3521
45. Newell DG, Shreeve JE, Toszeghy M, Domingue G, Bull S, Humphrey T, Mead G (2001) Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl Environ Microbiol 67:2636-2640
46. 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 43:2771-2781
47. Parker CT, Quiñones B, Miller WG, Horn ST, Mandrell RE (2006) Comparative genomic analysis of Campylobacter jejuni strains reveals diversity due to genomic elements similar to those present in C. jejuni strain RM1221. J Clin Microbiol 44: 4125-4135
48. Peyrat MB, Soumet C, Maris P, Sanders P (2008) Phenotypes and genotypes of campylobacter strains isolated after cleaning and disinfection in poultry slaughterhouses. Vet Microbiol 128:313-326
49. Poly F, Ewing C, Goon S, Hickey TE, Rockabrand D, Majam G, Lee L, Phan J, Savarino NJ, Guerry P (2007) Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect Immun 75:3859-3867
50. Reeser RJ, Medler RT, Billington SJ, Jost BH, Joens LA (2007) Characterization of Campylobacter jejuni biofilms under defined growth conditions. Appl Environ Microbiol 73:1908-1913
51. Reich F, Atanassova V, Haunhorst E, Klein G (2008) The effect of Campylobacter numbers in ceaca on the contamination of broiler carcasses with Campylobacter. Int J Food Microbiol 127:116-120
52. Revez J, Hänninen ML (2012) Lipooligosaccharide locus classes are associated with certain Campylobacter jejuni multilocus sequence types. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-012-1556-3
53. Rodin S, Andersson AF, Wirta V, Eriksson L, Ljungström M, Björkholm B, Lindmark H, Engstrand L (2008) Performance of a 70-mer oligonucleotide microarray for genotyping of Campylobacter jejuni. BMC Microbiol 8:73
54. Schoenhofen IC, Vinogradov E, Whitfield DM, Brisson JR, Logan SM (2009) The CMP-legionaminic acid pathway in Campylobacter: biosynthesis involving novel GDP-linked precursors. Glycobiology 19:715-725
55. Taboada EN, Acedillo RR, Carrillo CD, Findlay WA, Medeiros DT, Mykytczuk OL, Roberts MJ, Valencia CA, Farber JM, Nash JH (2004) Large-scale comparative genomics meta-analysis of Campylobacter jejuni isolates reveals low level of genome plasticity. J Clin Microbiol 42:4566-4576
56. Tam CC, Higgins CD, Neal KR, Rodrigues LC, Millership SE, O'Brien SJ (2009) Chicken consumption and use of acid-suppressing medications as risk factors for Campylobacter enteritis, England. Emerg Infect Dis 15:1402-1408
57. Uyttendaele M, Baert K, Ghafir Y, Daube G, De Zutter L, Herman L, Dierick K, Pierard D, Dubois JJ, Horion B, Debevere J (2006) Quantitative risk assessment of Campylobacter spp. In poultry based meat preparations as one of the factors to support the development of risk-based microbiological criteria in Belgium. Int J Food Microbiol 111:149-163
58. Vegge CS, Brondsted L, Li YP, Bang DD, IngmerH(2009) Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth. Appl Environ Microbiol 75:5308-5314