Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-28T23:01:39.873Z Has data issue: false hasContentIssue false

Campylobacter colonization in poultry: sources of infection and modes of transmission

Published online by Cambridge University Press:  09 March 2007

Orhan Sahin
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 446911, USA Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH, 432102, USA
Teresa Y. Morishita
Affiliation:
Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH, 432102, USA
Qijing Zhang*
Affiliation:
Food Animal Health Research Program, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 446911, USA Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH, 432102, USA
*
*Corresponding author: Food Animal Health Research Program, Ohio Agricultural Research and Development Center, Department of Veterinary Preventive Medicine, The Ohio State University, 1680 Madison Avenue, Wooster, OH 44691, USA E-mail: zhang.234@osu.edu

Abstract

Since its recognition as a human pathogen in the early 1970s, Campylobacter jejuni has now emerged as the leading bacterial cause of food-borne gastroenteritis in developed countries. Poultry, particularly chickens, account for the majority of human infections caused by Campylobacter. Reduction or elimination of this pathogen in the poultry reservoir is an essential step in minimizing the public health problem; however, farm-based intervention measures are still not available because of the lack of understanding of the ecological aspects of C. jejuni on poultry farms. Although Campylobacter is highly prevalent in poultry production systems, how poultry flocks become infected with this organism is still unknown. Many investigations indicate that horizontal transmission from environmental sources is the primary route of flock infections by Campylobacter. However, some recent studies also suggest the possibility of vertical transmission from breeder to progeny flocks. The transmission of the organism is not well understood, but it is likely to be through both vertical and horizontal transmission and may be affected by the immune status of the poultry host and the environmental conditions in the production system. Intervention strategies for Campylobacter infection in poultry should consider the complex nature of its transmission and may require the use of multiple approaches that target different segments of the poultry production system.

Type
Research Article
Copyright
Copyright © CAB International 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

Achen, M, Morishita, TY and Ley, EC (1998). Shedding and colonization of Campylobacter jejuni in broilers from day-of-hatch to slaughter age. Avian Diseases 42: 732737.CrossRefGoogle ScholarPubMed
Altekruse, SF, Stern, NJ, Fields, PI and Swerdlow, DL (1999). Campylobacter jejuni—an emerging foodborne pathogen. Emerging Infectious Diseases 5: 2835.CrossRefGoogle ScholarPubMed
Annan-Prah, A and Janc, M (1988). The mode of spread of Campylobacter jejuni/coli to broiler flocks. Journal of Veterinary Medicine B 35: 1118.CrossRefGoogle ScholarPubMed
Aydin, F, Atabay, HI and Akan, M (2001). The isolation and characterization of Campylobacter jejuni subsp. jejuni from domestic geese (Anser anser). Journal of Applied Microbiology 90: 637642.CrossRefGoogle ScholarPubMed
Babakhani, FK, Bradley, GA and Joens, LA (1993). Newborn piglet model for Campylobacteriosis. Infection and Immunity 61: 34663475.CrossRefGoogle ScholarPubMed
Baker, RC, Paredes, MD and Qureshi, RA (1987). Prevalence of Campylobacter jejuni in eggs and poultry meat in New York State. Poultry Science 66: 17661770.CrossRefGoogle ScholarPubMed
Beery, JT, Hugdahl, MB and Doyle, MP (1988). Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Applied and Environmental Microbiology 54: 23652370.CrossRefGoogle ScholarPubMed
Berndtson, E, Danielsson-Tham, ML and Engvall, A (1994). Experimental colonization of mice with Campylobacter jejuni. Veterinary Microbiology 41: 183188.CrossRefGoogle ScholarPubMed
Berndtson, E, Danielsson-Tham, ML and Engvall, A (1996). Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. International Journal of Food Microbiology 32: 3547.CrossRefGoogle ScholarPubMed
Berndtson, E, Emanuelson, U, Engvall, A and Danielsson-Tham, ML (1996). A 1-year epidemiological study of Campylobacter in 18 Swedish chicken farms. Preventive Veterinary Medicine 26: 167185.CrossRefGoogle Scholar
Blaser, MJ (1997). Epidemiologic and clinical features of Campylobacter jejuni infections. Journal of Infectious Diseases 176 (Suppl.2), S103S105.CrossRefGoogle ScholarPubMed
Broman, T, Bergstrom, S, On, SL, Palmgren, H, McCafferty, DJ, Sellin, M and Olsen, B (2000). Isolation and characterization of Campylobacter jejuni subsp. jejuni from macaroni penguins (Eudyptes chrysolophus) in the subantarctic region. Applied and Environmental Microbiology 66: 449452.CrossRefGoogle ScholarPubMed
Byrd, JA, Corrier, DE, Hume, ME, Bailey, RH, Stanker, LH and Hargis, BM (1998). Effect of feed withdrawal on Campylobacter in the crops of market-age broiler chickens. Avian Diseases 42: 802806.CrossRefGoogle ScholarPubMed
Byrd, JA, Corrier, DE, Hume, ME, Bailey, RH, Stanker, LH and Hargis, BM (1998). Incidence of Campylobacter in crops of preharvest market-age broiler chickens. Poultry Science 77: 13031305.CrossRefGoogle ScholarPubMed
Caldwell, MB, Walker, RI, Stewart, SD and Rogers, JE (1983). Simple adult rabbit model for Campylobacter jejuni enteritis. Infection and Immunity 42: 11761182.CrossRefGoogle ScholarPubMed
Camarda, A, Newell, DG, Nasti, R and Di Modugnoa, G (2000). Genotyping Campylobacter jejuni strains isolated from the gut and oviduct of laying hens. Avian Diseases 44: 907912.CrossRefGoogle ScholarPubMed
Cappelier, JM, Minet, J, Magras, C, Colwell, RR and Federighi, M (1999). Recovery in embryonated eggs of viable but nonculturable Campylobacter jejuni cells and maintenance of ability to adhere to HeLa cells after resuscitation. Applied and Environmental Microbiology 65: 51545157.CrossRefGoogle ScholarPubMed
Chen, HC and Stern, NJ (2001). Competitive exclusion of heterologous Campylobacter spp. in chicks. Applied and Environmental Microbiology 67: 848851.CrossRefGoogle ScholarPubMed
Chuma, T, Yamada, T, Yano, K, Okamoto, K and Yugi, H (1994). A survey of Campylobacter jejuni in broilers from assignment to slaughter using DNA-DNA hybridization. Journal of Veterinary Medical Science 56: 697700.CrossRefGoogle ScholarPubMed
Chuma, T, Makino, K, Okamoto, K and Yugi, H (1997). Analysis of distribution of Campylobacter jejuni and Campylobacter coli in broilers by using restriction fragment length polymorphism of flagellin gene. Journal of Veterinary Medical Science 59: 10111015.CrossRefGoogle ScholarPubMed
Chuma, T, Yano, K, Omori, H, Okamoto, K and Yugi, H (1997). Direct detection of Campylobacter jejuni in chicken cecal contents by PCR. Journal of Veterinary Medical Science 59: 8587.CrossRefGoogle ScholarPubMed
Chuma, T, Hashimoto, S and Okamoto, K (2000). Detection of thermophilic Campylobacter from sparrows by multiplex PCR: the role of sparrows as a source of contamination of broilers with Campylobacter. Journal of Veterinary Medical Science 62: 12911295.CrossRefGoogle ScholarPubMed
Clark, AG and Bueschkens, DH (1985). Laboratory infection of chicken eggs with Campylobacter jejuni by using temperature or pressure differentials. Applied and Environmental Microbiology 49: 14671471.CrossRefGoogle ScholarPubMed
Corry, JE and Atabay, HI (2001). Poultry as a source of Campylobacter and related organisms. Journal of Applied Microbiology 90: 96S114S.CrossRefGoogle Scholar
Cox, NA, Stern, NJ, Hiett, KL and Berrang, ME (1999). Transmission of Campylobacter jejuni from breeders to commercial broiler chickens. Proceedings of the 10th International Workshop on Campylobacter,Helicobacter and Related Organisms.Maryland, Baltimore, USA. p.61.Google Scholar
Craven, SE, Stern, NJ, Line, E, Bailey, JS, Cox, NA and 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 Diseases 44: 715720.CrossRefGoogle ScholarPubMed
Doyle, MP (1984). Association of Campylobacter jejuni with laying hens and eggs. Applied and Environmental Microbiology 47: 533536.CrossRefGoogle ScholarPubMed
Evans, SJ (1992). Introduction and spread of thermophilic campylobacters in broiler flocks. Veterinary Record 131: 574576.Google ScholarPubMed
Evans, SJ and Sayers, AR (2000). A longitudinal study of Campylobacter infection of broiler flocks in Great Britain. Preventive Veterinary Medicine 46: 209223.CrossRefGoogle ScholarPubMed
Fallacara, DM, Monahan, CM, Morishita, TY and Wack, RF (2001). Fecal shedding and antimicrobial susceptibility of selected bacterial pathogens and a survey of intestinal parasites in free-living waterfowl. Avian Diseases 45: 128135.CrossRefGoogle Scholar
Friedman, CR, Neimann, J, Wegener, HC and Tauxe, RV (2000). Epidemiology of C. jejuni infections in the United States and other industrialized nations. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press, pp. 121138.Google Scholar
Gibbens, JC, Pascoe, SJ, Evans, SJ, Davies, RH and Sayers, AR (2001). A trial of biosecurity as a means to control Campylobacter infection of broiler chickens. Preventive Veterinary Medicine 48: 8599.CrossRefGoogle ScholarPubMed
Gregory, E, Barnhart, H, Dreesen, DW, Stern, NJ and Corn, JL (1997). Epidemiological study of Campylobacter spp. in broilers: source, time of colonization, and prevalence. Avian Diseases 41: 890898.CrossRefGoogle ScholarPubMed
Hazeleger, WC, Wouters, JA, Rombouts, FM and Abee, T (1998). Physiological activity of Campylobacter jejuni far below the minimal growth temperature. Applied and Environmental Microbiology 64: 39173922.CrossRefGoogle ScholarPubMed
Heuer, OE, Pedersen, K, Andersen, JS and Madsen, M (2001). Prevalence and antimicrobial susceptibility of thermophilic Campylobacter in organic and conventional broiler flocks. Letters in Applied Microbiology 33: 269274.CrossRefGoogle ScholarPubMed
Hiett, KL, Cox, NA and Stern, NJ (2002). Direct polymerase chain reaction detection of Campylobacter spp. in poultry hatchery samples. Avian Diseases 46: 219223.CrossRefGoogle ScholarPubMed
Humphrey, TJ, Lanning, DG and Mead, GC (1989). Inhibition of Campylobacter jejuni in vitro by broiler chicken caecal contents. Veterinary Record 125: 272273.CrossRefGoogle ScholarPubMed
Humphrey, TJ, Henley, A and Lanning, DG (1993). The colonization of broiler chickens with Campylobacter jejuni: some epidemiological investigations. Epidemiology and Infection 110: 601607.CrossRefGoogle ScholarPubMed
Jacobs-Reitsma, W (2000). Campylobacter in the food supply. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press, pp. 467481.Google Scholar
Jacobs-Reitsma, WF (1995). Campylobacter bacteria in breeder flocks. Avian Diseases 39: 355359.CrossRefGoogle ScholarPubMed
Jacobs-Reitsma, WF (1997). Aspects of epidemiology of Campylobacter in poultry. Veterinary Quarterly 19: 113117.CrossRefGoogle ScholarPubMed
Jacobs-Reitsma, WF, Bolder, NM and Mulder, RW (1994). Cecal carriage of Campylobacter and Salmonella in Dutch broiler flocks at slaughter: a one-year study. Poultry Science 73: 12601266.CrossRefGoogle Scholar
Jacobs-Reitsma, WF, van de Giessen, AW, Bolder, NM and Mulder, RW (1995). Epidemiology of Campylobacter spp. at two Dutch broiler farms. Epidemiology and Infection 114: 413421.CrossRefGoogle ScholarPubMed
Jeffrey, JS, Atwill, ER and Hunter, A (2001). Prevalence of Campylobacter and Salmonella at a squab (young pigeon) processing plant. Poultry Science 80: 151155.CrossRefGoogle Scholar
Jones, FT, Axtell, RC, Rives, DV, Scheideler, SE, Tarver, FR, Walker, RI and Wineland, MJ (1991). A survey of Campylobacter jejuni contamination on modern broiler production and processing plants. Journal of Food Protection 54: 259262.CrossRefGoogle Scholar
Jones, K (2001). Campylobacters in water, sewage and the environment. Journal of Applied Microbiology 90: 68S79S.CrossRefGoogle Scholar
Jones, K, Howard, S and Wallace, JS (1999). Intermittent shedding of thermophilic campylobacters by sheep at pasture. Journal of Applied Microbiology 86: 531536.CrossRefGoogle ScholarPubMed
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
Kaneuchi, C, Ashihara, M, Saito, K and Itoh, T (1989). Serogrouping of thermophilic Campylobacter from gulls by slide agglutination based on heat-labile antigenic factors. Japanese Journal of Veterinary Science 51: 431433.Google ScholarPubMed
Kapperud, G and Rosef, O (1983). Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp. and Salmonella spp. in Norway. Applied and Environmental Microbiology 45: 375380.CrossRefGoogle ScholarPubMed
Kapperud, G, Skjerve, E, Vik, L, Hauge, K, Lysaker, A, Aalmen, I, Ostroff, SM and Potter, M (1993). Epidemiological investigation of risk factors for Campylobacter colonization in Norwegian broiler flocks. Epidemiology and Infection 111: 245255.CrossRefGoogle ScholarPubMed
Kazwala, RR, Collins, JD, Hannan, J, Crinion, RA and O'Mahony, H (1990). Factors responsible for the introduction and spread of Campylobacter jejuni infection in commercial poultry production. Veterinary Record 126: 305306.Google ScholarPubMed
King, V, Bavetsia, A and Bumstead, N (1993). Effect of host lineage on the virulence of Campylobacter jejuni/coli in the chick embryo model. FEMS Microbiology Letters 106: 271274.CrossRefGoogle ScholarPubMed
Kinjo, T, Morishige, M, Minamoto, N and Fukushi, H (1983). Prevalence of Campylobacter jejuni in feral pigeons. Japanese Journal of Veterinary Science 45: 833835.Google ScholarPubMed
Konkel, ME, Kim, BJ, Klena, JD, Young, CR and Ziprin, R (1998). Characterization of the thermal stress response of Campylobacter jejuni. Infection and Immunity 66: 36663672.CrossRefGoogle ScholarPubMed
Korolik, V, Alderton, MR, Smith, SC, Chang, J and Coloe, PJ (1998). Isolation and molecular analysis of colonising and non-colonising strains of Campylobacter jejuni and Campylobacter coli following experimental infection of young chickens. Veterinary Microbiology 60: 239249.CrossRefGoogle ScholarPubMed
Ley, EC, Morishita, TY, Brisker, T and Harr, BS (2001). Prevalence of Salmonella, Campylobacter and Escherichia coli on ostrich carcasses and the susceptibility of ostrich-origin E. coli isolates to various antibiotics. Avian Diseases 45: 696700.CrossRefGoogle ScholarPubMed
Lindblom, GB, Sjorgren, E and Kaijser, B (1986). Natural Campylobacter colonization in chickens raised under different environmental conditions. Journal of Hygiene (London) 96: 385391.CrossRefGoogle ScholarPubMed
Luechtefeld, NA, Blaser, MJ, Reller, LB and Wang, WL (1980). Isolation of Campylobacter fetus subsp. jejuni from migratory waterfowl. Journal of Clinical Microbiology 12: 406408.CrossRefGoogle ScholarPubMed
Luechtefeld, NW, Cambre, RC and Wang, WL (1981). Isolation of Campylobacter fetus subsp. jejuni from zoo animals. Journal of the American Veterinary Medical Association 179: 11191122.Google ScholarPubMed
Maruyama, S and Katsube, Y (1990). Isolation of Campylobacter jejuni from the eggs and organs in experimentally infected laying Japanese quails (Coturnix coturnix japonica). Japanese Journal of Veterinary Science 52: 671674.Google ScholarPubMed
Maruyama, S, Morita, Y and Katsube, Y (1995). Invasion and viability of Campylobacter jejuni in experimentally contaminated Japanese quails' eggs. Journal of Veterinary Medical Science 57: 587590.CrossRefGoogle ScholarPubMed
Mead, GC (2002). Factors affecting intestinal colonization of poultry by Campylobacter and role of microflora in control. World Poultry Science Journal 58: 169178.CrossRefGoogle Scholar
Meinersmann, RJ, Stern, NJ and Blankenship, LC (1990). Antigenic differences in congenic chicken-colonizing and noncolonizing strains of Campylobacter jejuni. Current Microbiology 21: 1721.CrossRefGoogle Scholar
Meinersmann, RJ, Rigsby, WE, Stern, NJ, Kelley, LC, Hill, JE and Doyle, MP (1991). Comparative study of colonizing and noncolonizing Campylobacter jejuni. American Journal of Veterinary Research 52: 15181522.CrossRefGoogle ScholarPubMed
Montrose, MS, Shane, SM and Harrington, KS (1985). Role of litter in the transmission of Campylobacter jejuni. Avian Diseases 29: 392399.CrossRefGoogle ScholarPubMed
Morishita, TY, Aye, PP, Harr, BS, Cobb, CW and Clifford, JR (1997). Evaluation of an avian-specific probiotic to reduce the colonization and shedding of Campylobacter jejuni in broilers. Avian Diseases 41: 850855.CrossRefGoogle ScholarPubMed
Nachamkin, I, Allos, BM and Ho, T (1998). Campylobacter species and Guillain–Barré syndrome. Clinical Microbiology Reviews 11: 555567.CrossRefGoogle ScholarPubMed
Nachamkin, I, Yang, XH and Stern, NJ (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
Nesbit, EG, Gibbs, P, Dreesen, DW and Lee, MD (2001). Epidemiologic features of Campylobacter jejuni isolated from poultry broiler houses and surrounding environments as determined by use of molecular strain typing. American Journal of Veterinary Research 62: 190194.CrossRefGoogle ScholarPubMed
Newell, DG and Wagenaar, JA (2000). Poultry infections and their control at the farm level. In: Nachamkin, I and Blaser, MJ (editors). Campylobacter. Washington, DC: ASM Press, pp. 497509.Google Scholar
Pacha, RE, Clark, GW, Williams, EA and Carter, AM (1988). Migratory birds of central Washington as reservoirs of Campylobacter jejuni. Canadian Journal of Microbiology 34: 8082.CrossRefGoogle Scholar
Parkhill, J, Wren, BW, Mungall, K, Ketley, JM, Churcher, C, Basham, D, Chillingworth, T, Davies, RM, Feltwell, T, Holroyd, S, Jagels, K, Karlyshev, AV, Moule, S, Pallen, MJ, Penn, CW, Quail, MA, Rajandream, MA, Rutherford, KM, van Vliet, AH, Whitehead, S and Barrell, BG (2000). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665668.CrossRefGoogle ScholarPubMed
Payne, RE, Lee, MD, Dreesen, DW and Barnhart, HM (1999). Molecular epidemiology of Campylobacter jejuni in broiler flocks using randomly amplified polymorphic DNA-PCR and 23S rRNA-PCR and role of litter in its transmission. Applied and Environmental Microbiology 65: 260263.CrossRefGoogle ScholarPubMed
Pearson, AD, Greenwood, M, Healing, TD, Rollins, D, Shahamat, M, Donaldson, J and Colwell, RR (1993). Colonization of broiler chickens by waterborne Campylobacter jejuni. Applied and Environmental Microbiology 59: 987996.CrossRefGoogle ScholarPubMed
Pearson, AD, Greenwood, MH, Feltham, RK, Healing, TD, Donaldson, J, Jones, DM and Colwell, RR (1996). Microbial ecology of Campylobacter jejuni in a United Kingdom chicken supply chain: intermittent common source, vertical transmission, and amplification by flock propagation. Applied and Environmental Microbiology 62: 46144620.CrossRefGoogle Scholar
Petersen, L and Wedderkopp, A (2001). Evidence that certain clones of Campylobacter jejuni persist during successive broiler flock rotations. Applied and Environmental Microbiology 67: 27392745.CrossRefGoogle ScholarPubMed
Petersen, L, Nielsen, EM, Engberg, J, On, SL and Dietz, HH (2001). Comparison of genotypes and serotypes of Campylobacter jejuni isolated from Danish wild mammals and birds and from broiler flocks and humans. Applied and Environmental Microbiology 67: 31153121.CrossRefGoogle ScholarPubMed
Petersen, L, Nielsen, EM and On, SL (2001). Serotype and genotype diversity and hatchery transmission of Campylobacter jejuni in commercial poultry flocks. Veterinary Microbiology 82: 141154.CrossRefGoogle ScholarPubMed
Rivoal, K, Denis, M, Salvat, G, Colin, P and Ermel, G (1999). Molecular characterization of the diversity of Campylobacter spp. isolates collected from a poultry slaughterhouse: analysis of cross-contamination. Letters in Applied Microbiology 29: 370374.CrossRefGoogle ScholarPubMed
Rosef, O and Kapperud, G (1983). House flies (Musca domestica). as possible vectors of Campylobacter fetus subsp. jejuni. Applied and Environmental Microbiology 45: 381383.CrossRefGoogle ScholarPubMed
Rosef, O, Kapperud, G, Lauwers, S and Gondrosen, B (1985). Serotyping of Campylobacter jejuni, Campylobacter coli and Campylobacter laridis from domestic and wild animals. Applied and Environmental Microbiology 49: 15071510.CrossRefGoogle ScholarPubMed
Russell, RG, Sarmiento, JI, Fox, J and Panigrahi, P (1990). Evidence of reinfection with multiple strains of Campylobacter jejuni and Campylobacter coli in Macaca nemestrina housed under hyperendemic conditions. Infection and Immunity 58: 21492155.CrossRefGoogle ScholarPubMed
Russell, RG, O'Donnoghue, M, Blake, DC Jr, Zulty, J and DeTolla, LJ (1993). Early colonic damage and invasion of Campylobacter jejuni in experimentally challenged infant Macaca mulatta. Journal of Infectious Diseases 168: 210215.CrossRefGoogle ScholarPubMed
Sahin, O, Zhang, Q and Meitzler, JC (2001). Effect of anti-Campylobacter maternal antibody on the colonization of C. jejuni in poultry. Proceedings of the American Society for Microbiology, 101st General Meeting,Orlando, Florida, USA. pp. 742743.Google Scholar
Sahin, O, Kobalka, P and Zhang, Q (2001). Detection and survivability of Campylobacter jejuni in chicken eggs. Proceedings of the 82nd Annual Meeting of Conference of Research Workers in Animal Diseases (CRWAD),St. Louis, Missouri, USA, p. 47.Google Scholar
Sahin, O, Zhang, Q, Meitzler, JC, Harr, BS, Morishita, TY and Mohan, R (2001). Prevalence, antigenic specificity, and bactericidal activity of poultry anti-Campylobacter maternal antibodies. Applied and Environmental Microbiology 67: 39513957.CrossRefGoogle ScholarPubMed
Sahin, O, Zhang, Q and Morishita, T (2002). Contributing factors for the lack of colonization of young chickens by Campylobacter jejuni. Proceedings of the American Society for Microbiology, 102nd General Meeting,Salt Lake City, Utah, USA, p. 510.Google Scholar
Shane, SM (1992). The significance of C. jejuni infection in poultry: a review. Avian Pathology 21: 189213.CrossRefGoogle ScholarPubMed
Shane, SM, Montrose, MS and Harrington, KS (1985). Transmission of Campylobacter jejuni by the housefly (Musca domestica). Avian Diseases 29: 384391.CrossRefGoogle ScholarPubMed
Shane, SM, Gifford, DH and Yogasundram, K (1986). Campylobacter jejuni contamination of eggs. Veterinary Research Communications 10: 487492.CrossRefGoogle ScholarPubMed
Shanker, S, Lee, A and Sorrell, TC (1986). Campylobacter jejuni in broilers: the role of vertical transmission. Journal of Hygiene (London) 96: 153159.CrossRefGoogle ScholarPubMed
Shanker, S, Lee, A and Sorrell, TC (1988). Experimental colonization of broiler chicks with Campylobacter jejuni. Epidemiology and Infection 100: 2734.CrossRefGoogle ScholarPubMed
Shanker, S, Lee, A and Sorrell, TC (1990). Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiology and Infection 104: 101110.CrossRefGoogle ScholarPubMed
Shreeve, JE, Toszeghy, M, Pattison, M and Newell, DG (2000). Sequential spread of Campylobacter infection in a multipen broiler house. Avian Diseases 44: 983988.CrossRefGoogle Scholar
Solomon, NH and Hoover, DM (1999). Campylobacter jejuni: a bacterial paradox. Journal of Food Safety 19: 121136.CrossRefGoogle Scholar
Stanley, K, Cunningham, R and Jones, K (1998). Isolation of Campylobacter jejuni from groundwater. Journal of Applied Microbiology 85: 187191.CrossRefGoogle ScholarPubMed
Stanley, K, Wallace, JS, Currie, JE, Diggle, PJ and Jones, K (1998). The seasonal variation of thermophilic campylobacters in beef cattle, dairy cattle and calves. Journal of Applied Microbiology 85: 472480.CrossRefGoogle ScholarPubMed
Stern, NJ (1992). Reservoirs for C. jejuni and approaches for intervention in poultry. In: Nachamkin, I, Blaser, MJ and Tompkins, LS (editors). Campylobacter jejuni: Current Status and Future Trends. Washington, DC: ASM Press, pp. 4960.Google Scholar
Stern, NJ, Bailey, JS, Blankenship, LC, Cox, NA and McHan, F (1988). Colonization characteristics of Campylobacter jejuni in chick ceca. Avian Diseases 32: 330334.CrossRefGoogle ScholarPubMed
Stern, NJ, Meinersmann, RJ, Cox, NA, Bailey, JS and Blankenship, LC (1990). Influence of host lineage on cecal colonization by Campylobacter jejuni in chickens. Avian Diseases 34: 602606.CrossRefGoogle ScholarPubMed
Stern, NJ, Clavero, MR, Bailey, JS, Cox, NA and Robach, MC (1995). Campylobacter spp. in broilers on the farm and after transport. Poultry Science 74: 937941.CrossRefGoogle ScholarPubMed
Stern, NJ, Myszewski, MA, Barnhart, HM and Dreesen, DW (1997). Flagellin A gene restriction fragment length polymorphism patterns of Campylobacter spp. isolates from broiler production sources. Avian Diseases 41: 899905.CrossRefGoogle ScholarPubMed
Stern, NJ, Fedorka-Cray, P, Bailey, JS, Cox, NA, Craven, SE, Hiett, KL, Musgrove, MT, Ladely, S, Cosby, D and Mead, GC (2001). Distribution of Campylobacter spp. in selected U.S. poultry production and processing operations. Journal of Food Protection 64: 17051710.CrossRefGoogle ScholarPubMed
Studer, E, Luthy, J and Hubner, 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, SI, Jacobs-Reitsma, W, Jansen, W, 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
van de Giessen, AW, Tilburg, JJ, Ritmeester, WS and Van der, PJ (1998). Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiology and Infection 121: 5766.CrossRefGoogle ScholarPubMed
Wallace, JS, Stanley, KN and Jones, K (1998). The colonization of turkeys by thermophilic campylobacters. Journal of Applied Microbiology 85: 224230.CrossRefGoogle ScholarPubMed
Wassenaar, TM and Blaser, MJ (1999). Pathophysiology of Campylobacter jejuni infections of humans. Microbes and Infection 1: 10231033.CrossRefGoogle ScholarPubMed
Wassenaar, TM and Newell, DG (2000). Genotyping of Campylobacter spp. Applied and Environmental Microbiology 66: 19.CrossRefGoogle ScholarPubMed
Wassenaar, TM, van der Zeijst, BA, Ayling, R and Newell, DG (1993). Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. Journal of General Microbiology 139: 11711175.CrossRefGoogle ScholarPubMed
Wedderkopp, A, Rattenborg, E and Madsen, M (2000). National surveillance of Campylobacter in broilers at slaughter in Denmark in 1998. Avian Diseases 44: 993999.CrossRefGoogle ScholarPubMed
Wedderkopp, A, Gradel, KO, Jorgensen, JC and Madsen, M (2001). Pre-harvest surveillance of Campylobacter and Salmonella in Danish broiler flocks: a 2-year study. International Journal of Food Microbiology 68: 5359.CrossRefGoogle ScholarPubMed
Willis, WL, Murray, C and Talbott, C (2000). Effect of delayed placement on the incidence of Campylobacter jejuni in broiler chickens. Poultry Science 79: 13921395.CrossRefGoogle ScholarPubMed
Yogasundram, K, Shane, SM and Harrington, KS (1989). Prevalence of Campylobacter jejuni in selected domestic and wild birds in Louisiana. Avian Diseases 33: 664667.CrossRefGoogle ScholarPubMed
Young, CR, Ziprin, RL, Hume, ME and Stanker, LH (1999). Dose response and organ invasion of day-of-hatch Leghorn chicks by different isolates of Campylobacter jejuni. Avian Diseases 43: 763767.CrossRefGoogle ScholarPubMed
Zhu, XY, Zhong, T, Pandya, Y and Joerger, RD (2002). 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Applied and Environmental Microbiology 68: 124137.CrossRefGoogle ScholarPubMed
Ziprin, RL, Young, CR, Byrd, JA, Stanker, LH, Hume, ME, Gray, SA, Kim, BJ and Konkel, ME (2001). Role of Campylobacter jejuni potential virulence genes in cecal colonization. Avian Diseases 45: 549557.CrossRefGoogle ScholarPubMed
Ziprin, RL, Young, CR, Stanker, LH, Hume, ME and Konkel, ME (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