Campylobacter jejuni colonization and transmission in broiler chickens: A modelling perspective

Journal of the Royal Society Interface

Volumn 4, Issue 16, 2007, Pages 818-829

  Conlan, Andrew J K ^a   Coward, Christopher ^a   Grant, Andrew J ^a   Maskell, Duncan J ^a   Gog, Julia R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Campylobacter jejuni; Colonization; Persistence; Population genetics; Stochasticity; Transmission

Indexed keywords

BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; CAMPYLOBACTER JEJUNI; CHICKEN; ECOLOGY; GENE EXPRESSION; MATHEMATICAL MODEL; NONHUMAN; PHENOTYPE; POPULATION MODEL; REVIEW; ANIMAL; BIOLOGICAL MODEL; DISEASE TRANSMISSION; GRAM NEGATIVE INFECTION; MICROBIOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; GALLUS GALLUS;

ANIMALS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CHICKENS; MODELS, BIOLOGICAL;

EID: 34948906224     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2007.1015     Document Type: Review

References (84)

1. Achen, M., Morishita, T. Y. & Ley, E. C. 1998 Shedding and colonization of Campylobacter jejuni in broilers from day-of-hatch to slaughter age. Avian Dis. 42, 732-737. (doi:10.2307/1592708)
2. Adkin, A., Hartnett, E., Jordan, L., Newell, D. & Davison, H. 2006 Use of a systematic review to assist the development of Campylobacter control strategies in broilers. J. Appl. Microbiol. 100, 306-315. (doi:10.1111/j.1365-2672.2005.02781.x)
3. Altekruse, S., Stern, N., Fields, P. & Swerdlow, D. 1999 Campylobacter jejuni - an emerging foodborne pathogen. Emerg. Infect. Dis. 5, 28-35.
4. Anderson, R. & May, R. 1979 Population biology of infectious diseases: part I. Nature 280, 361-367. (doi:10.1038/280361a0)
5. Anderson, R. & May, R. 1981 The population dynamics of microparasites and their invertebrate hosts. Phil. Trans. R. Soc. B 291, 451-524. (doi:10.1098/rstb.1981.0005)
6. Beery, J., Hugdahl, M. & Doyle, M. 1988 Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54, 2365-2370.
7. Berndtson, E., Danielsson-Tham, M. & Engvall, A. 1996a Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. Int. J. Food Microbiol. 32, 35-47. (doi:10.1016/0168-1605(96)01102-6)
8. Berndtson, E., Emanuelson, U., Engvall, A. & Danielsson-Tham, M. 1996b A 1-year epidemiological study of Campylobacters in 18 Swedish chicken farms. Prev. Vet. Med. 26, 167-185. (doi:10.1016/0167- 5877(95)01008-4)
9. Black, R., Levine, M., Clements, M., Hughes, T. & Blaser, M. 1988 Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157, 472-479.
10. Callicott, K. A. et al. 2006 Lack of evidence for vertical transmission of Campylobacter spp. in chickens. Appl. Environ. Microbiol. 72, 5794-5798. (doi:10.1128/AEM.02991-05)
11. Carrillo, C. D. et al. 2004 Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J. Biol. Chem. 279, 20 327-20 338. (doi:10.1074/jbc.M401134200)
12. Cawthraw, S., Ayling, R., Nuijten, P., Wassenaar, T. & Newell, D. 1994 Isotype, specificity, and kinetics of systemic and mucosal antibodies to Campylobacter jejuni antigens, including flagellin, during experimental oral infections of chickens. Avian Dis. 38, 341-349. (doi:10.2307/1591960)
13. Cawthraw, S., Wassenaar, T., Ayling, R. & Newell, D. 1996 Increased colonization potential of Campylobacter jejuni strain 81116 after passage through chickens and its implication on the rate of transmission within flocks. Epidemiol. Infect. 117, 213-215.
14. Chen, L., Geys, H., Cawthraw, S., Havelaar, A. & Teunis, P. 2006 Dose response for infectivity of several strains of Campylobacter jejuni in chickens. Risk Anal. 26, 1613-1621. (doi:10.1111/j.1539-6924.2006. 00850.x)
15. Chuma, T., Makino, K., Okamoto, K. & Yugi, H. 1997 Analysis of distribution of Campylobacter jejuni and Campylobacter coli in broilers by using restriction fragment length polymorphism of flagellin gene. J. Vet. Med. Sci. 59, 1011-1015. (doi:10.1292/jvms.59.1011)
16. Corry, J. & Atabay, H. 2001 Poultry as a source of Campylobacter and related organisms. J. Appl. Microbiol. 90, 96-114. (doi:10.1046/j.1365-2672.2001.01358.x)
17. Craven, S. E., Stern, N. J., Line, E., Bailey, J. S., Cox, N. A. & Fedorka-Cray, P. 2000 Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler chicken houses by sampling intestinal droppings. Avian Dis. 44, 715-720. (doi:10.2307/1593118)
18. De Jong, M. C. M., Diekmann, O. & Heesterbeek, J. A. P. 1995 Epidemic models: their structure and relation to data. In How does infection-transmission depend on population size? (ed. D. Mollison). Publications of the Newton Institute, ch. 5, pp. 84-94, Cambridge, UK: Cambridge University Press.
19. Dens, E. J., Vereecken, K. M. & Van Impe, J. F. 1999 A prototype model structure for mixed microbial populations in homogeneous food products. J. Theor. Biol. 201, 159-170. (doi:10.1006/jtbi.1999.1021)
20. Ekdahl, K., Normann, B. & Andersson, Y. 2005 Could flies explain the elusive epidemiology of campylobacteriosis? BMC Infect. Dis. 5, 11. (doi:10.1186/1471-2334-5-11)
21. Evans, S. J. & Sayers, A. R. 2000 A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Prev. Vet. Med. 46, 209-223. (doi:10.1016/S0167-5877(00)00143-4)
22. 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. (doi:10.1128/JB.186.2.503-517.2004)
23. Gog, J. R., Rimmelzwaan, G. F., Osterhaus, A. D. M. E. & Grenfell, B. T. 2003 Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. Proc. Natl Acad. Sci. USA 100, 11 143-11 147. (doi:10.1073/pnas.1830296100)
24. Grant, A. J., Coward, C., Jones, M. A., Woodall, C. A., Barrow, P. A. & Maskell, D. J. 2005 Signature-tagged transposon mutagenesis studies demonstrate the dynamic nature of cecal colonization of 2-week-old chickens by Campylobacter jejuni. Appl. Environ. Microbiol. 71, 8031-8041. (doi:10.1128/AEM.71.12.8031-8041.2005)
25. Gregory, E., Barnhart, H., Dreesen, D. W., Stern, N. J. & Corn, J. L. 1997 Epidemiological study of Campylobacter spp. in broilers: source, time of colonization, and prevalence. Avian Dis. 41, 890-898. (doi:10.2307/1592343)
26. Grenfell, B. T., Pybus, O. G., Gog, J. R.. Wood, J. L. N., Daly, J. M., Mumford, J. A. & Holmes, E. C. 2004 Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303, 327-332. (doi:10.1126/science.1090727)
27. Hartnett, E., Kelly, L., Newell, D., Wooldridge, M. & Gettinby, G. 2001 A quantitative risk assessment for the occurrence of Campylobacter in chickens at the point of slaughter. Epidemiol. Infect. 127, 195-206.
28. Havelaar, A. et al. 2007 Effectiveness and efficiency of controlling Campylobacter on broiler chicken meat. Risk Anal. OnlineEarly article. (doi:10.1111/j.1539-6924.2006.00835.x)
29. Hendrixson, D. & DiRita, V. J. 2004 Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52, 471-484. (doi:10.1111/j.1365-2958.2004.03988.x)
30. Hensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E. & Holden, D. W. 1995 Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400-403. (doi:10.1126/science. 7618105)
31. Heuer, O., Pedersen, K., Andersen, J. S. & Madsen, M. 2001 Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Lett. Appl. Microbiol. 33, 269-274. (doi:10.1046/j.1472-765X.2001.00994.x)
32. Hiett, K. L., Stern, N. J., Fedorka-Cray, P., Cox, N. A., Musgrove, M. T. & Ladely, S. 2002 Molecular subtype analyses of Campylobacter spp. from Arkansas and California poultry operations. Appl. Environ. Microbiol. 68, 6220-6236. (doi:10.1128/AEM.68.12.6220-6236.2002)
33. Hook, H., Fattah, M., Ericsson, H., Vagsholm, I. & Danielsson-Tham, M. 2005 Genotype dynamics of Campylobacter jejuni in a broiler flock. Vet. Microbiol. 106, 109-117. (doi:10.1016/j.vetmic.2004.12.017)
34. Jacobs-Reitsma, W. 1998 Experimental horizontal spread of Campylobacter amongst one-day-old broilers. In Campylobacter, Helicobacter and related organisms (eds. A. J. Lastovica, D. G. Newell & E. E. Lastovica), pp. 377-378, 1st edn. Cape Town, South Africa: University of Cape Town.
35. Jacobs-Reitsma, W., van de Giessen, A., Bolder, N. & Mulder, R. 1995 Epidemiology of Campylobacter spp. at two Dutch broiler farms. Epidemiol. Infect. 114, 413-421.
36. Jones, M. A., Marston, K. L., Woodall, C. A., Maskell, D. J., Linton, D., Karlyshev, A. V., Dorrell, N., Wren, B. W. & Barrow, P. A. 2004 Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72, 3769-3776. (doi:10.1128/IAI.72.7.3769-3776.2004)
37. Kimura, M. 1962 On the probability of fixation of mutant genes in a population. Genetics 47, 713-719.
38. Konkel, M. E., Christensen, J. E., Dhillon, A. S., Lane, A. B., Hare-Sanford, R., Schaberg, D. M. & Larson, C. L. 2007 Campylobacter jejuni strains compete for colonization in broiler chicks. Appl. Environ. Microbiol. 73, 2297-2305. (doi:10.1128/AEM.02193-06)
39. Kussell, E. & Leibler, S. 2005 Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075-2078. (doi:10.1126/science.1114383)
40. Li, W. & Graur, D. 1991 Fundamentals of molecular evolution. Sunderland, MA: Sinauer Associates.
41. Lotka, A. 1956 Elements of mathematical biology. New York, NY: Dover Publications, Inc.
42. Louis, V. R., Gillespie, I. A., O'Brien, S. J., Russek-Cohen, E., Pearson, A. D. & Colwell, R. R. 2004 Temperature-driven Campylobacter seasonality in England and Wales. Appl. Environ. Microbiol. 71, 85-92. (doi:10.1128/AEM.71.1.85-92.2005)
43. Mazurkiewicz, P., Tang, C. M., Boone, C. & Holden, D. W. 2006 Signature-tagged mutagenesis: barcoding mutants for genome-wide screens. Nat. Rev. Genet. 7, 929-939. (doi:10.1038/nrg1984)
44. Meldrum, R. J., Griffiths, J. K., Smith, R. M. M. & Evans, M. R. 2004 The seasonality of human Campylobacter infection and Campylobacter isolates from fresh, retail chicken in Wales. Epidemiol. Infect. 133, 49-52. (doi:10.1017/S0950268804003188)
45. Newell, D. G. & Fearnley, C. 2003 Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69, 4343-4351. (doi:10.1128/AEM.69.8.4343-4351.2003)
46. Nylen, G. et al. 2002 The seasonal distribution of Campylobacter infection in nine European countries and New Zealand. Epidemiol. Infect. 128, 383-390. (doi:10.1017/S0950268802006830)
47. Parkhill, J. et al. 2000 The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668. (doi:10.1038/35001088)
48. Patrick, M. E., Christiansen, L. E., Waino, M., Ethelberg, S., Madsen, H. & Wegener, H. C. 2004 Effects of climate on incidence of Campylobacterspp. in humans and prevalence in broiler flocks in Denmark. Appl. Environ. Microbiol. 70, 7474-7480. (doi:10.1128/AEM.70.12. 7474-7480.2004)
49. Pearson, A. D., Greenwood, M., Healing, T. D., Rollins, D., Shahamat, M., Donaldson, J. & Colwell, R. R. 1993 Colonization of broiler chickens by waterborne Campylobacter jejuni. Appl. Environ. Microbiol. 59, 987-996.
50. Petersen, L., Nielsen, E. M. & On, S. L. W. 2001 Serotype and genotype diversity and hatchery transmission of Campylobacter jejuni in commercial poultry flocks. Vet. Microbiol. 82, 141-154. (doi:10.1016/S0378-1135(01)00382-0)
51. Preston, A. & Murphy, L. 1989 Movement of broiler chickens reared in commercial conditions. Br. Poult. Sci. 30, 519-532.
52. Renshaw, E. 1991 Modelling biological populations in space and time. Cambridge, UK: Cambridge University Press.
53. Ring, M., Zychowska, M. A. & Stephan, R. 2005 Dynamics of Campylobacter spp. spread investigated in 14 broiler flocks in Switzerland. Avian Dis. 49, 390-396. (doi:10.1637/7319-010305R1.1)
54. Ringoir, D. D. & Korolik, V. 2003 Colonisation phenotype and colonisation potential differences in Campylobacter jejuni strains in chickens before and after passage in vivo. Vet. Microbiol. 92, 225-235. (doi:10.1016/S0378-1135(02)00378-4)
55. Rivoal, K., Denis, M., Salvat, G., Colin, P. & Ermel, G. 1999 Molecular characterization of the diversity of Campylobacter spp. isolates collected from a poultry slaughter-house: analysis of cross-contamination. Lett. Appl. Microbiol. 29, 370-374. (doi:10.1046/j.1472-765X.1999.00645.x)
56. Sahin, O., Morishita, T. & Zhang, Q. 2002 Campylobacter colonization in poultry: sources of infection and modes of transmission. Anim. Health Res. Rev. 3, 95-105. (doi:10.1079/AHRR200244)
57. Sahin, O., Luo, N., Huang, S. & Zhang, Q. 2003 Effect of campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl. Environ. Microbiol. 69, 5372-5379. (doi:10.1128/AEM.69.9.5372-5379.2003)
58. Saunders, N. J., Moxon, E. R. & Gravenor, M. B. 2003 Mutation rates: estimating phase variation rates when fitness differences are present and their impact on population structure. Microbiology 149, 485-495. (doi:10.1099/mic.0.25807-0)
59. Shanker, S., Lee, A. & Sorrell, T. 1986 Campylobacter jejuni in broilers: the role of vertical transmission. J. Hyg. 96, 153-159.
60. Shanker, S., Lee, A. & Sorrell, T. 1988 Experimental colonization of broiler chicks with Campylobacter jejuni. Epidemiol. Infect. 100, 27-34.
61. Shanker, S., Lee, A. & Sorrell, T. 1990 Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiol. Infect. 104, 101-110.
62. Shreeve, J. E., Toszeghy, M., Pattison, M. & Newell, D. G. 2000 Sequential spread of Campylobacter infection in a multipen broiler house. Avian Dis. 44, 983-988. (doi:10.2307/1593076)
63. Stanley, K., Wallace, J., Currie, J., Diggle, P. & Jones, K. 1998a Seasonal variation of thermophilic Campylobacters in lambs at slaughter. J. Appl. Microbiol. 84, 1111-1116. (doi:10.1046/j.1365- 2672.1998.00450.x)
64. Stanley, K. N., Wallace, J. S., Currie, J. E., Diggle, P. J. & Jones, K. 19986 The seasonal variation of thermophilic Campylobacters in beef cattle, dairy cattle and calves. J. Appl. Microbiol. 85, 472-480. (doi:10.1046/j.1365-2672.1998.853511.x)
65. Stern, N. J., Bailey, J. S., Blankenship, L. C., Cox, N. A. & McHan, F. 1988 Colonization characteristics of Campylobacter jejuniva chick ceca. Avian Dis. 80, 330-334. (doi:10.2307/1590822)
66. Stern, N. J., Myszewski, M. A., Barnhart, H. M. & Dreesen, D. W. 1997 Flagellin A gene restriction fragment length polymorphism patterns of Campylobacter spp. isolates from broiler production sources. Avian Dis. 32, 899-905. (doi:10.2307/1592344)
67. Stern, N., Cox, N., Bailey, J., Berrang, M. & Musgrove, M. 2001a Comparison of mucosal competitive exclusion and competitive exclusion treatment to reduce Salmonella and Campylobacter spp. colonization in broiler chickens. Poult. Sci. 41, 156-160.
68. Stern, N., Cox, N. & Musgrove, M. 20016 Incidence and levels of Campylobacter in broilers after exposure to an inoculated seeder bird. J. Appl. Poult. Res. 10, 315-318.
69. Thattai, M. & van Oudenaarden, A. 2004 Stochastic gene expression in fluctuating environments. Genetics 167, 523-530. (doi:10.1534/genetics.167.1.523)
70. Thomas, L., Long, K., Good, R., Panaccio, M. & Widders, P. 1997 Genotypic diversity among Campylobacter jejuni isolates in a commercial broiler flock. Appl. Environ. Microbiol. 63, 1874-1877.
71. van de Giessen, A., Mazurier, S. I., Jacobs-Reitsma, W., Jansen, W., Berkers, P., Ritmeester, W. & Wernars, K. 1992 Study on the epidemiology and control of Campylobacter jejuni in poultry broiler flocks. Appl. Environ. Microbiol. 58, 1913-1917.
72. van der Wielen, P. W. J. J., Biesterveld, S., Notermans, S., Hofstra, H., Urlings, B. A. P. & van Knapen, F. 2000 Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl. Environ. Microbiol. 66, 2536-2540. (doi:10.1128/AEM.66.6.2536-2540. 2000)
73. Van Gerwe, T. J. W. M., Bouma, A., Jacobs-Reitsma, W. F., van den Broek, J., Klinkenberg, D., Stegeman, J. A. & Heesterbeek, J. A. P. 2005 Quantifying transmission of Campylobacter spp. among broilers. Appl. Environ. Microbiol. 71. 5765-5770. (doi:10.1128/AEM.71.10.5765-5770. 2005)
74. Van Overbeke, I., Duchateau, L., De Zutter, L., Albers, G. & Ducatelle, R. 2006 A comparison survey of organic and conventional broiler chickens for infectious agents affecting health and food safety. Avian Dis. 50, 196-200. (doi:10.1637/7448-093005R.1)
75. Vereecken, K. M., Dens, E. J. & Van Impe, J. F. 2000 Predictive modeling of mixed microbial populations in food products: evaluation of two-species models. J. Theor. Biol. 205, 53-72. (doi:10.1006/jtbi.2000.2046)
76. Volterra, V. & Brelot, M. 1931 Leçons sur la théorie mathématique de la lutte pour la vie. Paris, France: Gauthier-Villars.
77. Wrahl, L. M. & Gerrish, P. J. 2001 The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55, 2606-2610. (doi:10.1554/0014-3820(2001)055[2606:TPTBMA]2.0.CO;2)
78. Wallace, J., Stanley, K., Currie, J., Diggle, P. & Jones, K. 1997 Seasonality of thermophilic Campylobacter populations in chickens. J. Appl. Microbiol. 82, 219-224. (doi:10.1046/j.1365-2672.1997.00378.x)
79. Wassenaar, T. M., Geilhausen, B. & Newell, D. G. 1998 Evidence of genomic instability in Campylobacter jejuni isolated from poultry. Appl. Environ. Microbiol. 64, 1816-1821.
80. Wearing, H., Rohani, P. & Keeling, M. J. 2005 Appropriate models for the management of infectious diseases. PLoS Med. 2, e174. (doi:10.1371/journal.pmed.0020174)
81. Wiles, S. 2006 Opinion: Modelling infectious disease: time to think outside the box? Nat. Rev. Microbiol. 4, 307-312. (doi:10.1038/nrmicro1386)
82. Willis, W., Murray, C. & Talbott, C. 2002 Campylobacter isolation trends of cage versus floor broiler chickens: a one-year study. Poult. Sci. 81, 629-631.
83. Wingfield, A., Miller, H. & Honhold, N. 2006 FMD control strategies. Vet. Rec. 158, 706-707.
84. Young, C. R., Ziprin, R. L., Hume, M. & Stanker, L. 1999 Dose response and organ invasion of day-of-hatch leghorn chicks by different isolates of Campylobacter jejuni. Avian Dis. 43, 763-767. (doi:10.2307/1592745)