Foodborne Campylobacter: Infections, metabolism, pathogenesis and reservoirs

International Journal of Environmental Research and Public Health

Volumn 10, Issue 12, 2013, Pages 6292-6304

  Epps, Sharon V R ^a,b   Harvey, Roger B ^a   Hume, Michael E ^a   Phillips, Timothy D ^b   Anderson, Robin C ^a   Nisbet, David J ^a  

^a SOUTHERN PLAINS AGRICULTURAL RESEARCH CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Campylobacter coli; Campylobacter jejuni; Diarrhea; Foodborne pathogen; Guillain Barr syndrome

Indexed keywords

AUTOANTIBODY; CEPHALOSPORIN; ERYTHROMYCIN; MACROLIDE; PENICILLIN DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFAMPICIN; SULFAMETHOXAZOLE; TRIMETHOPRIM; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; BACTERIUM; DIARRHEAL DISEASE; FOOD SAFETY; INFECTIOUS DISEASE; METABOLISM; NERVOUS SYSTEM DISORDER; PATHOGEN; PUBLIC HEALTH;

ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL TRANSMISSION; BACTERIUM ISOLATION; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; DISEASE CARRIER; FOOD POISONING; FOOD SAFETY; GUILLAIN BARRE SYNDROME; HUMAN; INCIDENCE; INFECTION CONTROL; INFECTION RISK; NONHUMAN; PATHOGENESIS; PUBLIC HEALTH; REVIEW; SYMPTOMATOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI;

CAMPYLOBACTER; CAMPYLOBACTER INFECTIONS; DISEASE RESERVOIRS; FOODBORNE DISEASES; HUMANS;

EID: 84888326216     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph10126292     Document Type: Review

References (84)

1. Penner, J. L. The Genus Campylobacter: A decade of progress. Clin. Microbiol. Rev. 1988, 1, 157-172.
2. Nachamkin, I. Campylobacter and Archobacter. In Manual of Clinical Microbiology, 8th ed.; Murray, P. R., Baron, E. J., Jorgensen, J. A., Eds.; American Society for Microbiology (ASM) Press: Washington DC., USA, 2003; pp. 902-914.
3. Parkhill, J.; Wren, B. W.; Mungall, K.; Ketley, J. M.; Churcher, C.; Basham, D.; Chillingworth, T.; Davies, R. M.; Feltwell, T.; Holroyd, S.; Jagels, K.; Karlyshev, A. V.; Moule, S.; Pallen, M. J.; Penn, C. W.; Quail, M. A.; Rajandream, M. A.; Rutherford, K. M.; van Vliet, A. H.; Whitehead, S.; Barrell, B. G. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000, 403, 665-668.
4. Gundogdu, O.; Bently, S. D.; Holden, M. T.; Parkhill, J.; Dorrell, N.; Wren, B. W. Re-annotation and re-analysis of the Campylobacter jejuni NCTC11168 genome sequence. BMC Genomics 2007, 8, 471-472.
5. Altekruse, S. F.; Stern, N. J.; Fields, P. I.; Swerdlow, D. L. Campylobacter jejuni and emerging foodborne pathogen. Emerg. Infect. Dis. 1999, 5, 28-35.
6. Nachamkin, I.; Szymanski, M. C.; Blaser, J. M. Campylobacter, 3rd ed.; ASM Press: Washington DC, USA, 2008.
7. Coker, O.; Akitoye, I.; Raphael, D.; Thomas, N.; Bolaji, A.; Kehinde, O.; Obi, L. C. Human campylobacteriosis in developing countries. Emerg. Infect. Dis. 2002, 8, 237-243.
8. Snelling, W. J.; Matsuda, M.; Moore, J. E.; Dooley, J. S. G. Under the microscope Campylobacter jejuni. Appl. Microbiol. 2005, 41, 297-302.
9. Silva, J.; Leite, D.; Fernandez, M.; Mena, C.; Gibbs, P. A.; Teixeira, P. Campylobacter spp. as a foodborne pathogen: A review. Front. Microbiol. 2011, 2, 1-12.
10. King, S.; Adams, M. C. Incidence in Campylobacter in prcessed poultry: Is it a concern for human health. J. Food Safety 2008, 28, 376-388.
11. Vandamme, P.; Debruyne, I.; de Brandt, E.; Falsen, E. Reclassification of Bacteroides ureolyticus as Campylobacter ureolyticus comb. nov., and emmended description of the genus Campylobacter. Int. J. Syst. Evol. Microbiol. 2010, 60, 2016-2022.
12. Skirrow, M. B. John McFadyean and the centenary of the first isolation of Campylobacter species. Clin. Infect. Dis. 2006, 43, 1213-1217.
13. Jones, F. S.; Orcutt, M.; Little, R. B. Vibrios (Vibrio jejuni, n. Sp.) associated with intestinal disorders of cows and calves. J. Exp. Med. 1931, 53, 853-863.
14. Butzler, J. P. Campylobacter, from obscurity to celebrity. Clin. Microbiol. Infect. 2004, 10, 868-876.
15. Levy, A. J. A gastro-enteritis outbreak probably due to a bovine strain vibrio. J. Infect. Dis. 1946, 18, 243-258.
16. Doyle, L. P. A vibrio associated with swine dysentery. Am. J. Vet. Res. 1944, 5, 3-5.
17. Doyle, P. M.; Roman, J. D. Recovery of Campylobacter jejuni and Campylobacter coli from inoculated foods by selective enrichment. Appl. Environ. Microbiol. 1982, 43, 1343-1353.
18. On, S. L. W. Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: Current status, future prospects and immediate concerns. J. Appl. Microbiol. 2001, 90, S1-S15.
19. Parker, C. T.; Miller, W. G.; Horn, S. T.; Lastovica, A. J. Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbio 2007, 7, 1471-2180.
20. Denny, J.; Boelaert, F.; Borck, B.; Heur, O. E.; Ammon, A.; Makela, P. Zoonotic infection in Europe: Trends and figures-A summary of the EFSA-ECDC annual report. Eur. Surviell. 2007, 51. Available online: http: //www. eurosurveillance. org/ViewArticle. aspx?ArticleId=3336 (accessed on 11 November 2013).
21. Ailes, E.; Demma, L.; Hurd, S.; Hatch, J.; Jones, T. F.; Vugia, D.; Cronquist, A.; Tobin-D'Angelo, M.; Larson, K.; Laine, E.; Edge, K.; Zansky, S.; Sallan, E. Continued decline in the incidence of Campylobacter infections. FoodNet 1996-2006. Foodborne Pathog. Dis. 2008, 5, 329-337.
22. Blaser, M. J. Campylobacter and related species. In Mandell, Douglas and Bennett's Principles and Practices of Infectious Diseases; Mandell, G. L., Bennett, J. E., Dolin, R., Eds.; American Society for Microbiology (ASM) Press: Washington DC, USA, 1995; pp. 1948-1956.
23. Blaser, M. J.; Engberg, J. Clinical aspects of Campylobacter jejuni and Campylobacter coli infections. In Campylobacter, 3rd ed.; Nachamkin, I., Blaser, J. M., Eds.; American Society for Microbiology (ASM) Press: Washington DC, USA, 2008; pp. 99-121.
24. Blaser, M. J.; Berkowitz, I. D.; LaForce, F. M.; Cravens, J.; Reller, L. B.; Wang, W. L. Campylobacter enteritis: Clinical and epidemiologic features. Ann. Intern. Med. 1979, 91, 179-185.
25. Salloway, S.; Mermael, I. A.; Seamans, M.; Aspinall, G. O.; Shin, J. E. N.; Kurjanczyk, L. A.; Penner, J. L. Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human GD3. Infect. Immun. 1996, 64, 2945-2949.
26. Nachamkin, I.; Allos, B. M.; Ho, T. Campylobacter species and Guillain-Barre syndrome. Clin. Microbiol. Rev. 1998, 11, 555-567.
27. Scharff, R. L. Economic burden from health losses due to foodborne illness in the United States. J. Food. Prot. 2012, 75, 123-131.
28. Heredia, N.; Wesley, I.; Garcia, S. Microbiologically Safe Foods. In Foodborne Pathogens and Toxins: Overview; John Wlley & Sons: Hoboken, NJ, USA, 2009; pp 20-22.
29. CDC. Incidence and Trends of Infection with Pathogens Transmitted Commonly through Food-foodborne Diseases Active Surveillance Network, 10 United States Sites, 1996-2012; U. S. Department of Health and Human Services Centers for Disease Control and Prevention: Atlanta, GA, USA, 2013; pp. 283-287.
30. Preliminary FoodNet Data on the Incidence of infeCtion with Pathogens Transmitted Commonly Through Food 10 States, United States; U. S. Department of Health and Human Services Centers for Disease Control and Prevention: Atlanta, GA, USA, 2006; pp 393-395.
31. EFSA. The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. EFSA J. 2007, 130, 130-155.
32. EFSA. The community summary report on trends and sources of zoonoses, zoonotic agents, and foodborne outbreaks in the European Union in 2008. EFSA J. 2010, 8, 1496-1906.
33. Oberhelman, R. A.; Taylor, D. N. Campylobacter infections in developing countries. In Campylobacter, 2nd ed.; Nachamkin, I., Blaser, M. J., Eds.; American Society of Microbiology (SAM) Press: Washington DC, USA, 2000; pp. 139-153.
34. Taylor, D. N. Campylobacter infections in developing countries. In Campylobacter jejuni: Current Status and Future Trends; American Society for Microbiology (ASM) Press: Washington DC, USA, 1992; pp. 20-30.
35. Tauxe, R. V. Epidiemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter jeuni: Current and Future Trends; Nachamkin, I., Blaser, M. J., Tompkins, L. S., Eds.; American Society of Microbiology (ASM) Press: Washington DC, USA, 1992; pp. 9-12.
36. Robinson, D. A. Infective dose of Campylobacter jejuni in milk. Brit. Med. J. 1981, 282, 1584.
37. Enberg, J.; Aarestrup, F. M.; Taylor, D. E.; Gerner-Smidt, P.; Nachamkin, I. Quinolone and macrolide resistance in Campylobacter jejuni and C. coli. Resistance mechanisms and trends in human isolates. Emerg. Infect. Dis. 2001, 7, 24-34.
38. Anderson, A. D.; Nelson, J. M.; Rossiter, S.; Angulo, F. J. Public health consequences of use of antimicrobial agents in food animals in the United States. Microb. Drug. Resist. 2003, 9, 373-379.
39. Thakur, S.; Gebreyes, W. A. Campylobacter coli in swine production: antimicrobial resistance mechanisms and molecular epideimiology. J. Clin. Microbiol. 2005, 43, 5705-5714.
40. Thakur, S.; Morrow, W. E. M.; Funk, J. A.; Bahnson, P. B.; Gebreyes, W. A. Molecular epidemiologic investigation of Campylobacter coli in swine production systems, using sequence typing. Appl. Environ. Microbiol. 2006, 72, 5666-5669.
41. Javid, M. H. Campylobacter infections. In Medscape Reference Drugs & Diseases and Procedures; Emedicine Medscape: New York, NY, USA, 2011; pp. 1-7.
42. Rozynek, E.; Dzierzanowska-Fangrat, K.; Szczezepa, A. B.; Wardak, S.; Szych, J.; Konieczny, P.; Albrecht, P.; Dzierzanowska, D. Trends in antimicrobial susceptibility of Campylobacter isolates in Poland. Pol. J. Microbiol. 2007, 58, 111-115.
43. Igimi, S.; Okada, Y.; Ishiwa, A.; Yamasaki, M.; Morisaki, N.; Kubo, Y.; Asakura, H.; Yamamoto, S. Antimicrobial resistance of Campylobacter: Prevalence and trends in Japan. Food Addit. Contam. 2008, 25, 1080-1083.
44. Molina, S. S.; Kurincic, C. M.; Krammer, A.; Urlicc, S.; Katalinic, V. Prevalence and resistance against different antimicrobial compounds of Campylobacter spp. in/from retail poultry. Meat Technol. 2009, 50, 112-120.
45. Luangtongkum, T.; Jeon, B.; Han, J.; Plummer, P.; Logue, C. M.; Zhang, Q. Antibiotic resistance in Campylobacter: Emergence, transmission, and persistence. Fut. Microbiol. 2009, 4, 189-200.
46. Moore, J. E.; Barton, M. D.; Blair, I. S. The epidemiology of antibiotic resistance in Campylobacter. Microb. Infec. 2006, 8, 1955-1966.
47. Alfredson, D. A.; Korolik, V. Antibiotic resistance and resistance mechanisms in Campylobacter jejuni and Campylobacter coli. FEMS Microbiol. Lett. 2007, 277, 123-132.
48. Aarestrup, F. M.; Endberg, J. Antimicrobial resistance of thermophilic Campylobacter. Vet. Res. 2001, 32, 311-321.
49. Gibreel, A.; Taylor, D. E. Macrolide resistance in Campylobacter jejuni and Campylobacter coli. J. Antimicrob. Chemother. 2006, 58, 243-255.
50. Stahl, M.; Butcher, J.; Stintzi, A. Nutrient aquisition and metabolism by Campylobacter jejuni. Front. Cell. Infect. Microbiol. 2012, 2, 1-10.
51. Velayudhan, J.; Kelly, D. J. Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni an essential role for phosphoenolpyruvate carboxykinase. Microbiology 2002, 148, 685-694.
52. Muraoka, W. T.; Wayne, T.; Zhang, Q. Phenotypic and genotypic evidence for L-Fucose utilization by Campylobacter jejuni. J. Bacteriol. 2011, 193, 1065-1075.
53. Stahl, M.; Friis, L. M.; Nothaft, H.; Liu, X.; Li, J.; Szymanski, C. M.; Stintzi, A. L-Fucose utilization provides Campylobacter jejuni with a competitve advantage. PNAS 2011, 108, 1-6.
54. Laanbroek, H. J.; Stal, L. J.; Veldkamp, H. Utilization of hydrogen and formate by Campylobacter spec. under aerobic and anaerobic conditions. Arch. Microbiol. 1978, 119, 99-102.
55. Hoffman, P. S.; Goodman, T. G. Respiratory physiology and energy conservation efficiency of Campylobacter jejuni. J. Bacteriol. 1982, 150, 319-326.
56. Smith, M. A.; Mendz, G. I.; Jorgensen, M. A.; Hazell, S. I. Fumarate metabolism and micraerophily of Campylobacter species. Int. J. Biochem. Cell. Biol. 1999, 31, 961-975.
57. Sellers, M. J.; Hall, S. J.; Kelly, D. J. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulf oxide requires oxygen. J. Bacteriol. 2002, 184, 4187-4196.
58. Hofreuter, D.; Novik, V.; Galan, J. E. Metabolic diversity in Campylobacter jejuni enhances specific tissue colonization. Cell. Host Microbe 2008, 4, 425-433.
59. Dickgiesser, N.; Czylwik, D. Chemically defined media for autotyping of Campylobacter jejuni. Zentraibl. Bakteriol. Mikrobiol. Hyg. A 1985, 260, 57-64.
60. Elharrif, Z.; Mergraud, F. Characterization of thermophillic Campylobacter. I. Carbon-substrate utilization test. Curr. Microbiol. 1986, 13, 117-122.
61. Larson, C. L.; Christensen, J. E.; Pacheco, S. A.; Minnich, S. A.; Konkel, M. E. Campylobacter jejuni secretes protein via flagellar type III secretion system that contribute to host cell invasion and gastroenteritis. In Campylobacter, 3rd ed.; Nachamkin, I., Szymanski, C., Blaser, M., Eds.; American Society for Microbiology (ASM) Press: Washington DC, USA, 2008; pp. 315-318.
62. Palyada, K.; Threadgill, D.; Stintzi, A. Iron aquisition and regulation in Campylobacter jejuni. J. Bacteriol. 2004, 186, 4714-4729.
63. Ketley, J. M. Pathogenesis of enteric infection by Campylobacter. Microbiology 1997, 143, 5-21.
64. Watson, R. O.; Galán, J. E. Interaction of Campylobacter with host cells. In Campylobacter; Nachamkin, I., Szymanski, C., Blaser, M., Eds.; American Society for Microbiology (ASM) Press: Washignton DC, USA, 2008; pp. 287-296.
65. Hu, L.; Kopecko, D. J. Cell biology of human host cell entry by Campylobacter jejuni. In Campylobacter; Nachamkin, I., Szymanski, C., Blaser, M., Eds.; American Society for Microbiology (ASM) Press: Washington DC, USA, 2008; pp. 297-313.
66. van Putten, J. P. M.; van Alphen, L. B.; Wosten, M. M. S.; de Zoete, M. R. Molecular mechanisms of Campylobacter infection. Curr. Topics Microbiol. Immunol. 2009, 337, 197-229.
67. Allos, B. M.; Lippy, F. T.; Carlsen, A.; Washburn, R. G.; Blaser, M. J. Campylobacter jejuni strains from patients with Guillain-Barre Syndrome. Emerg. Infect. Dis. 1998, 4, 263-268.
68. Shahrizaila, N.; Yuki, N. Guillain-Barrè Syndome animal model: The first proof molecular mimicry in human autoimmune disorder. J. Biomed. Biotechnol. 2011, 2011, 1-5.
69. van Doran, P. A.; Ruts, L.; Jacobs, B. C. Clinical features, pathogenesis, and treatment of Guillain-Barre syndome. Lancet Neurol. 2008, 7, 939-950.
70. Moore, J. E.; Corcoran, D.; Dooley, J. S. G.; Fanning, S.; Lucey, B.; Matsuda, M.; McDowell, D. A.; Megraud, F.; Millar, B. C.; Mahoney, R. O.; Riordan, L. O.; Rourke, M. O.; Rao, J. R.; Sails, A.; Whyte, P. Campylobacter. Vet. Res. 2005, 36, 351-382.
71. Horrocks, S. M.; Anderson, R. C.; Nisbet, D. J.; Ricke, S. C. Incidence and ecology of Campylobacter jejuni and coli in animals. Anaerobe 2009, 15, 18-25.
72. El-Shibiny, A.; Connerton, P. L.; Connerton, I. F. Enumeration and diversity of Campylobacters and bacteriophages isolated during the rearing cycles of free-range organic chickens. Appl. Environ. Microbiol. 2005, 71, 1259-1266.
73. Bull, S. A.; Allen, V. M.; Domingue, G.; Jorgensen, J. A.; Frost, R.; Ure, R.; Whyte, D.; Tinker, J. E.; Corry, J.; Gillard-King, J.; T. J., H. Sources of Campylobacter spp. colonizing housed broiler flocks during rearing. Appl. Environ. Microbiol. 2006, 72, 645-652.
74. Stern, N. J.; Fedorka-Cray, P.; Bailey, J. S.; Cox, N. A.; Craven, S. E.; Hiett, K. L.; Musgrove, M. T.; Ladely, S.; Cosby, D.; Mead, G. C. Distribution of Campylobacter spp. in selected U. S. poultry production and processing operations. J. Food Protect. 2001, 64, 1705-1710.
75. Berndtson, E.; Danielsson-Than, M. I.; Engvall, A. Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. Int. J. Food Protect. 1996, 32, 35-47.
76. Besser, T. E.; LeJeune, J. T.; Rice, D. H.; Berg, J.; Stillborn, R. P.; Kaya, K.; Bae, W.; Hancock, D. D. Increasing prevaence of Campylobacter jejuni in feedlot cattle through the feeding period. Appl. Environ. Microbiol. 2005, 71, 5752-5758.
77. Friedman, C. R.; Hoeckstra, M. S.; Marcus, R.; Bender, J.; Shiferaw, S.; Reddy, S.; Ahuja, S. D.; Helfrick, D. L.; Hardnett, F.; Carter, M.; Anderson, B.; Tauxe, R. V. Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin. Infect. Dis. 2004, 38, S285-S296.
78. Grahamm, C.; Simmons, N. L. Functional organization of the bovine rumen epitheilium. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 288, doi: 10. 1152/ajpregu. 00425. 2004.
79. Oporto, B. J.; Estaban, I.; Aduriz, G.; Juste, R. A.; Hurtado, A. Prevalence and strain diversity of thermophilic Campylobacters in cattle, sheep, and swine farms. J. Appl. Microbiol. 2007, 103, 977-984.
80. Young, C. R.; Harvey, R.; Anderson, R.; Nibet, D.; Stanker, L. H. Enteric colonisation following natural exposure to Campylobacter in pigs. Res. Vet. Sci. 2000, 68, 75-78.
81. Jensen, A. N.; Dalsgard, A.; Baggesen, D. I.; Nielsen, E. M. The occurrence and characterization of Campylobacter jeuni and C. coli in organic pigs and their outdoor environment. Vet. Microbiol. 2006, 116, 96-105.
82. Beach, J.; Murano, E.; Acuff, G. Prevalence of Salmonella and Campylobacter in beef cattle from transport to slaughter. J. Food. Protect. 2002, 65, 1687-1693.
83. Madden, R. H.; Moran, L.; Scates, P. Optimising recovery of Campylobacter spp. from the lower porcine gastrointestinal tract. J. Microbiol. Meth. 2000, 42, 115-119.
84. Alter, T.; Gaull, F.; Kasimir, S.; Gürtler, M.; Mielke, H.; Linnebur, M.; Fehlhaber, K. Prevalences and transmission routes of Campylobacter spp. strains within multiple pig farms. Vet. Microbiol. 2005, 108, 251-261.