Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-23T20:34:06.982Z Has data issue: false hasContentIssue false

Factors affecting intestinal colonisation of poultry by campylobacter and role of microflora in control

Published online by Cambridge University Press:  18 September 2007

G.C. Mead
Affiliation:
Royal Veterinary College, Boltons Park, Hawkshead Road, Potters Bar, Hertfordshire EN6 1NB, United Kingdom, e-mail: geoffmead@hotmail.com
Get access

Abstract

Although thermophilic campylobacters have sometimes caused disease in poultry, both in challenge studies and under field conditions, the organisms are usually carried asymptomatically in the alimentary tract of infected individuals. There is, however, a significant association between campylobacters in poultry and human enteritis. Properties of Campylobacter jejuni that are associated with intestinal colonisation in the bird are discussed. The organism is morphologically and physiologically well adapted to its ecological niche in the mucus-filled crypts of villi, but establishment and maintenance of colonisation involve a complex interaction between bacterium and host that has yet to be fully elucidated. Bacterial factors include the possession of intact, functional flagella and the type of flagellin expressed. Also, colonisation has been shown to depend on the expression of certain stress-response and virulence genes.

Attempts to prevent or reduce campylobacter colonisation by establishing a competitive or antagonistic microflora in chicks have not always been successful, and possible reasons are considered. Some protection was obtained with bacteria such as mucin-utilising coliforms, but the protective potential of these organisms appears to be limited. In other studies, the natural occurrence of colonisation resistance has been demonstrated in broilers and its development followed. Experience suggests that the phenomenon depends on the presence of strictly anaerobic bacteria that have yet to be isolated and identified.

Type
Reviews
Copyright
Copyright © Cambridge University Press 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abu-ruwaida, A.S., Sawaya, W.N., Dashti, B.H., Murad, M. and Al-othman, H.A. (1994) Microbiological quality of broilers during processing in a modem commercial slaughterhouse in Kuwait. Journal of Food Protection 57: 887892.CrossRefGoogle Scholar
Achen, M., Morishita, T.Y. and Ley, E.C. (1998) Shedding and colonization of Campylobacter jejuni in broilers from day of hatch to slaughter age. Avian Diseases 42: 732737.CrossRefGoogle ScholarPubMed
Aho, M.A., Nuotio, L. and Nurmi, E.V. (1989) A bacterial preparation for use in poultry. A bacterial preparation useful for the prophylaxis of intestinal bacterial infections, especially Campylobacter infections in poultry comprises bacteria from an adult bird, from the microecological niche, especially the caecum, where the pathogenic bacteria mostly attach themselves in newly hatched chickens. Farmos, Turku, Finland, assignee. Great Britain Patent No. 2,233,343A.Google Scholar
Aho, M., Nuotio, L., Nurmi, E. and Kiiskinen, T. (1992) Competitive exclusion of campylobacters from poultry with K-bacteria and Broilact®. International Journal of Food Microbiology 15: 265275.CrossRefGoogle ScholarPubMed
Baig, B.H., Wachsmuth, I.K. and Morris, G.K. (1986) Utilization of exogenous siderophores by Campylobacter species. Journal of Clinical Microbiology 23: 431433.CrossRefGoogle ScholarPubMed
Baumgartner, A., Grand, M., Liniger, M. and Simmen, A. (1995) Campylobacter contamination of poultry liver – consequences for food handlers and consumers. Archiv. für Lebensmittelhygiene 46: 1112Google Scholar
Beery, J.T., Hugdahl, M.B. and Doyle, M.P. (1988) Colonization of the gastrointestinal tract of chicks by Campylobacter jejuni. Applied and Environmental Microbiology 54: 23652370.CrossRefGoogle ScholarPubMed
Berndtson, E., Tivemo, M. and Engvall, A. (1992) Distribution and numbers of Campylobacter in newly slaughtered broiler chickens and hens. International Journal of Food Microbiology 15: 4550.CrossRefGoogle ScholarPubMed
Berrang, M.E., Buhr, R.J. and Cason, J.A. (2000) Campylobacter recovery from external and internal organs of commercial broiler carcasses prior to scalding. Poultry Science 79: 286290.CrossRefGoogle ScholarPubMed
Bryan, F.L. and Doyle, M.P. (1995) Health risks and consequences of Salmonella and Campylobacter jejuni in raw poultry. Journal of Food Protection 58: 326344.CrossRefGoogle ScholarPubMed
Cawthraw, S., Ayling, R., Nuljten, P., Wassenaar, T. and Newell, D.G. (1994) Isotype, specificity and kinetics of systemic and mucosal antibodies to Campylobacter jejuni antigens, including flagellin, during experimental oral infection of chickens. Avian Diseases 38: 341349.CrossRefGoogle ScholarPubMed
Chang, M.H. and Chen, T.C. (2000) Reduction of Campylobacter jejuni in a simulated chicken digestive tract by lactobacilli cultures. Journal of Food Protection 63: 15941597.CrossRefGoogle Scholar
Chen, H.-C. and Stern, N.J. (2001) Competitive exclusion of heterologous Campylobacter spp. in chicks. Applied and Environmental Microbiology 67: 848851.CrossRefGoogle ScholarPubMed
Corry, J.E.L. and Atabay, H.I. (2001) Poultry as a source of Campylobacter and related organisms. Journal of Applied Microbiology 90: 96S–14S.CrossRefGoogle Scholar
Genigeorgis, C.A., Hassuneh, M. and Collins, P. (1986) Campylobacter jejuni infection on poultry farms and its effect on poultry meat contamination during slaughtering. Journal of Food Protection 49: 895903.CrossRefGoogle ScholarPubMed
Hakkinen, M. and Schneitz, C. (1999) Efficacy of a commercial competitive exclusion product against Campylobacter jejuni. British Poultry Science 40: 619621.CrossRefGoogle ScholarPubMed
Hald, B., Knudsen, K., Lind, P. and Madsen, M. (2001) Study of the infectivity of saline-stored Campylobacter jejuni for day-old chicks. Applied and Environmental Microbiology 67: 23882392.CrossRefGoogle ScholarPubMed
Hugdahl, M.B., Beery, J.T. and Doyle, M.P. (1988) Chemotactic behaviour of Campylobacter jejuni. Infection and Immunity 56: 15601566.CrossRefGoogle ScholarPubMed
Humphrey, T.J., Lanning, D.G. and Mead, G.C. (1989) Inhibition of Campylobacter jejuni in vitro by broiler chicken caecal contents. Veterinary Record 125: 272273.CrossRefGoogle ScholarPubMed
Humphrey, T.J., Henley, A. and Lanning, D.G. (1993) The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiology and infection 110: 601607.CrossRefGoogle ScholarPubMed
Jacobs-reitsma, W.F., Bolder, N.M. and Mulder, R.W.A.W. (1994) Cecal carriage of Campylobacter jejuni and Salmonella in Dutch broiler flocks at slaughter: a one-year study. Poultry Science 73: 12601266.CrossRefGoogle Scholar
Jacobs-reitsma, W.F., Van De Giessen, A.W., Bolder, N.M. and Mulder, R.W.A.W. (1995) Epidemiology of Campylobacter pp. at two Dutch broiler farms. Epidemiology and Infection 114: 413421.CrossRefGoogle Scholar
Kaino, K., Hayashidani, H., Kaneko, K. and Ogawa, M. (1988) Intestinal colonization of Campylobacter jejuni in chickens. Japanese Journal of Veterinary Science 50: 489494.Google ScholarPubMed
Kapperud, G., Skjerve, E., Vik, L., Hauge, K., Lysaker, A., Aalmen, I., Ostroff, S.M. and Potter, M. (1993) Epidemiological investigation of risk factors for Campylobucter colonisation in Norwegian broiler flocks. Epidemiology and Infection 111: 245255.CrossRefGoogle ScholarPubMed
Konkel, M.E., Garvis, S.G., Tipton, S.L., Anderson, D.E.J. and Cieplak, W.J. (1997) Identification and molecular cloning of a gene encoding a fibronectin-binding protein (cadF) from Campylobacter jejuni. Molecular Microbiology 24: 953963.CrossRefGoogle ScholarPubMed
Konkel, M.E., Kim, B.J., Klena, J.D., Young, C.R. and Ziprin, R. (1998) Characterization of the thermal stress response of Campylobacter jejuni. Infection and Immunity 66: 36663672.CrossRefGoogle ScholarPubMed
Lam, K.M., Damassa, A.J., Morishita, T.Y., Shiraprasad, H.L. and Bickford, A.A. (1992) Pathogenicity of Campylobacter jejuni for turkeys and chickens. Avian Diseases 36: 359363.CrossRefGoogle ScholarPubMed
Li, C.Y., Xue, P., Tian, W.Q., Liu, R.C. and Yang, C. (1996) Experimental Campylobacter jejuni infection in the chicken: an animal model of axonal Guillain-Barré syndrome. Journal of Neurology, Neurosurgery and Pshychiatry 61: 279284.CrossRefGoogle ScholarPubMed
Lindblom, G.-B., Sjogren, E. and Kaijser, B. (1986) Natural Campylobacter colonization in chickens raised under different environmental conditions. Journal of Hygiene, Cambridge 96: 385391.CrossRefGoogle ScholarPubMed
Line, J.E., Bailey, J.S., Cox, N.A. and Stern, N.J. (1997) Yeast treatment to reduce Salmonella and Campylobacter populations associated with broiler chickens subjected to transport stress. Poultry Science 76: 12271231.CrossRefGoogle ScholarPubMed
McSweegan, E. and Walker, R.I. (1986) Identification and characterisation of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infection and Immunity 53: 141148.CrossRefGoogle ScholarPubMed
Mead, G.C. (2001) Role of intestinal microflora in controlling campylobacter colonisation of broilers. Proceedings of the Fifteenth European Symposium on the Quality of Poultry MeatKusadasi, Turkey, pp. 223230.Google Scholar
Mead, G.C. and Impey, C.S. (1987) The present status of the Nurmi Concept for reducing carriage of food-poisoning salmonellae and other pathogens in live poultry. In: Elimination of Pathogenic Organisms from Meat and Poultry (Smulders, F.J.M., Ed.) Amsterdam, Elsevier Science Publishers pp. 5577.Google Scholar
Mead, G.C. and Scott, M.J. (1996) Studies on the anti-campylobacter activity of Escherichia coli strains isolated from caecal mucus of adult hens. British Poultry Science 37: S37S38.Google Scholar
Mead, G.C., Barrow, P.A., Hinton, M., Humbert, F., Impey, C.S., Lahellec, C., Mulder, R.W.A.W., Stavric, S. and Stern, N.J. (1989) Recommended assay for treatment of chicks to prevent salmonella colonization by ‘competitive exclusion’. Journal of Food Protection 52: 500502.CrossRefGoogle ScholarPubMed
Mead, G.C., Hudson, W.R. and Hinton, M.H. (1995) Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with campylobacter. Epidemiology and Infection 115: 495500.CrossRefGoogle ScholarPubMed
Mead, G.C., Scott, M.J, Humphrey, T.J. and McAlpine, K. (1996) Observations on the control of Campylobacter jejuni infection of poultry by ‘competitive exclusion’. Avian Parhology 25: 6979.CrossRefGoogle ScholarPubMed
Meinersmann, R.J., Stern, N.J. and Blankenship, L.C. (1990) Antigenic differences in congenic chicken-colonizing and noncolonizing strains of Campylobacter jejuni. Current Microbiology 21: 1721.CrossRefGoogle Scholar
Mulder, R.W.A.W. and Bolder, N.M. (1991) Reduction of Campylobacter infection of broilers by competitive exclusion treatment of day-old broiler chicks – a field study. In: Colonization Control of Human Bacterial Enteropathogens in Poultry (Blankenship, L.C., Ed.) San Diego, USA, Academic Press, pp. 359363.CrossRefGoogle Scholar
Myszewski, M.A. and Stern, N.J. (1990) Influence of Campylobacter jejuni cecal colonization on immunoglobulin response in chickens. Avian Diseases 34: 588594.CrossRefGoogle ScholarPubMed
Nachamkin, I., Yang, X.-H. and Stern, N.J. (1993) Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Applied and Environmental Microbiology 59: 12691273.CrossRefGoogle ScholarPubMed
Newell, D.G. and Wagenaar, J.A. (2000) Poultry infections and their control at farm level. In: Campylobacter 2nd edn. [Nachamkin, I. and Blaser, M.J., Eds] Washington D.C., ASM Press, pp. 497510.Google Scholar
Newell, D.G., McBride, H. and Dolby, J.M. (1985) Investigations on the role of flagella in the colonization of infant mice with Campylobacter jejuni and attachment of Campylobacter jejuni to human epithelial cell lines. Journal of Hygiene, Cambridge 95: 217227.CrossRefGoogle ScholarPubMed
Pokamunski, S., Kass, N., Borochovich, E., Marantz, B. and Rogol, M. (1986) Incidence of Campylobacter spp. in broiler flocks monitored from hatching to slaughter. Avian Pathology 15: 8392.CrossRefGoogle ScholarPubMed
Report (1996) Report on Poultry Meat. Advisory Committee on the Microbiological Safety of Food. HMSO, London, UK.Google Scholar
Sahin, O., Zhang, Q., Meitzler, J.C., Harr, B.S., Morishita, T.Y. and Mohan, R. (2001) Prevalence, antigenic specificity and bactericidal activity of poultry anti- campylobacter maternal antibodies. Applied and Environmental Microbiology 67: 39513957.CrossRefGoogle ScholarPubMed
Savage, D.C. (1977) Microbial ecology of the gastrointestinal tract. Annual Review of Microbiology 31: 107133.CrossRefGoogle ScholarPubMed
Schoeni, J.L. and Doyle, M.P. (1992) Reduction of Campylobacter jejuni colonization of chicks by cecum-colonizing bacteria producing anti-C.jejuni metabolites. Applied and Environmental Microbiology 59: 664670CrossRefGoogle Scholar
Schoeni, J.L. and Wong, A.C.L. (1994) Inhibition of Campylobacter jejuni colonization in chicks by defined competitive exclusion bacteria. Applied and Environmental Microbiology 60: 11911197.CrossRefGoogle ScholarPubMed
Shanker, S., Lee, A. and Sorrell, T.C. (1988) Experimental colonization of broiler chicks with Campylobacter jejuni. Epidemiology and Infection 100: 2734.CrossRefGoogle ScholarPubMed
Shanker, S., Lee, A. and Sorrell, T.C. (1990) Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiology and Infection 104: 101110.CrossRefGoogle ScholarPubMed
Soerjadi, A.S., Snoeyenbos, G.H. and Weinack, O.M. (1982) Intestinal colonization and competitive exclusion of Campylobacter fetus subsp. jejuni in young chicks. Avian Diseases 26: 520524.CrossRefGoogle ScholarPubMed
Soerjadi-liem, AS., Snoeyenbos, G.H. and Weinack, O.M. (1984) Comparative studies on competitive exclusion of three isolates of Campylobacter fetus subsp.jejuni in chickens by native gut microflora. Avian Diseases 28: 139146.CrossRefGoogle ScholarPubMed
Stas, T., Jordan, F.T.W. and Woldchiwet, Z. (1999) Experimental infection of chickens with Campylobacter jejuni: strains differ in their capacity to colonize the intestine. Avian Pathology 28: 6164.CrossRefGoogle ScholarPubMed
Stern, N.J. (1994) Mucosal competitive exclusion to diminish colonization of chickens by Campylobacter jejuni. Poultry Science 73: 402407.CrossRefGoogle ScholarPubMed
Stern, N.J., Bailey, J.S., Blankenship, L.C., Cox, N.A. and McHan, F. (1988) Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Diseases 32: 330334.CrossRefGoogle ScholarPubMed
Stern, N.J., Meinersmann, R.J., Cox, N.A., Bailey, J.S. and Blankenship, L.C. (1990) Influence of host lineage on cecal colonization by Campylobacter jejuni in chickens. Avian Diseases 34: 602606.CrossRefGoogle ScholarPubMed
Stern, N.J., Doyle, M.P. and Meinersmann, R.J. (1993) Influence of defined antagonistic flora on Campylobacter jejuni in broiler chicks. Poultry Science 72 (Supplement): 5.Google Scholar
Stern, N.J., Myszewski, M.A. and Barhart, H. (1997) Flagellin A gene restriction fragment length polymorphism patterns of Campylobacter spp. from broiler production sources. Avian Diseases 41: 899905.CrossRefGoogle ScholarPubMed
Stern, N.J., Bailey, J.S., Cox, N.A., Craven, S.E. and Cray, P.F. (1999) Flow of Campylobacter spp. through US poultry operations. In: 10th International Workshop on Campylobacter, Helicobacter and Related Organisms [Mobley, H.L.T, Nachamkin, I. and McGee, D., Eds] Abstract no. CF17, Baltimore, USA.Google Scholar
Stern, N.J., Cox, N.A., Bailey, J.S., Berrang, M.E. and Musgrove, M.T. (2001) Comparison of mucosal competitive exclusion and competitive exclusion treatment to reduce Salmonella and Campylobacter spp. colonization in broiler chickens. Poultry Science 80: 156160.CrossRefGoogle ScholarPubMed
Studer, E., Lüthy, J. and Hübner, P. (1999) Study of the presence of Campylobacter jejuni and C. coli in sand samples from four Swiss chicken farms. Research in Microbiology 150: 213219.CrossRefGoogle Scholar
Van De Giessen, A., Mazurier, S-I., Jacobs-reitsma, W.J., Berkers, P., Ritmeester, W. and Wernars, K. (1992) Study on the epidemiology and control of Campylobacter jejuni in poultry broiler flocks, Applied and Environmental Microbiology 58: 19131917.CrossRefGoogle Scholar
Wallace, J.S., Stanley, K.N., Currie, J.E., Diggle, P.J. and Jones, K. (1997) Seasonality of thermophilic Campylobacter populations in chickens. Journal of Applied Microbiology 82: 219224.CrossRefGoogle ScholarPubMed
Ziprin, R.L., Young, C.R., Stanker, L.H., Hume, M.E. and Konkel, M.E. (1999) The absence of cecal colonization of chicks by a mutant of Campylobacter jejuni not expressing bacterial fibronectin binding protein. Avian Diseases 43: 586589.CrossRefGoogle Scholar
Ziprin, R.L., Young, C.R., Byrd, J.A., Stanker, L.H., Hume, M.E., Gray, S.A., Kim, B.J. and Konkel, M.E. (2001) Role of Campylobacter jejuni potential virulence genes in cecal colonization. Avian Diseases 45: 549557.CrossRefGoogle ScholarPubMed