Review of current methodologies to isolate and identify Campylobacter spp. from foods

Journal of Microbiological Methods

Volumn 95, Issue 1, 2013, Pages 84-92

  Gharst, Gregory ^a   Oyarzabal, Omar A ^b   Hussain, Syeda K ^c  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b IEH Laboratories and Consulting Group   (United States)

^c ALABAMA STATE UNIVERSITY   (United States)

Author keywords

Aerobic enrichment; Broiler; Campylobacter coli; Campylobacter jejuni; Chicken; Isolation

Indexed keywords

AMPHOTERICIN B; CEFOPERAZONE; CHARCOAL CEFOPERAZONE DEOXYCHOLATE; OXYGEN; UNCLASSIFIED DRUG;

AEROBIC CELL CULTURE; ARTICLE; BACTERIAL CELL; BACTERIUM COLONY; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BLOOD; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CELL COUNT; CHEMICAL MODIFICATION; CLINICAL PROTOCOL; CULTURE MEDIUM; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA DETERMINATION; DNA SEQUENCE; ENRICHMENT CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; EUROPE; FOOD ANALYSIS; FOOD AND DRUG ADMINISTRATION; FOOD CONTAMINATION; GENETIC VARIABILITY; GOVERNMENT; INCUBATION TEMPERATURE; ISOLATION PROCEDURE; LATEX AGGLUTINATION TEST; MEMBRANE FILTER; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PHASE CONTRAST MICROSCOPY; PLATING MEDIUM; POULTRY; PRIORITY JOURNAL; RAPID TEST; SENSITIVITY ANALYSIS; UNITED STATES;

CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI;

AEROBIC ENRICHMENT; BROILER; CAMPYLOBACTER COLI; CAMPYLOBACTER JEJUNI; CHICKEN; ISOLATION;

ANIMALS; BACTERIOLOGICAL TECHNIQUES; CAMPYLOBACTER; CHICKENS; EUROPE; FOOD MICROBIOLOGY; MEAT; MOLECULAR DIAGNOSTIC TECHNIQUES; UNITED STATES;

EID: 84884128001     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2013.07.014     Document Type: Article

References (77)

1. Adler H.I., Carrasco A., Crow W., Gill J.S. Cytoplasmic membrane fraction that promotes septation in an Escherichia coli lon mutant. J. Bacteriol. 1981, 147:326-332.
2. Anonymous Microbiology of food and animal feeding stuffs - horizontal method for detection and enumeration of Campylobacter spp. Part 1: Detection Methods. ISO 10272-1:2006 2006.
3. Anonymous Microbiology of Food and Animal Feeding Stuffs - General Requirements and Guidance for Microbiological Examinations. ISO 7218:2007 2007.
4. Anonymous Microbiology of Food and Animal Feed - Horizontal Method for Detection and Enumeration of Campylobacter - Part 1: Detection Method. ISO 10272-1A:2009 2009.
5. Anonymous New performance standards for Salmonella and Campylobacter in young chicken and turkey slaughter establishments: response to comments and announcement of implementation schedule. Fed. Reg. 2011, 76:15282-15290.
6. Anonymous Isolation, identification, and enumeration of method for the enumeration of Campylobacter jejuni/coli/lari from poultry rinse, sponge and raw poultry product samples. USDA FSIS Microbiology Laboratory Guidebook, Chapter 41.02 2013, (Available at http://www.fsis.usda.gov/wps/wcm/connect/0273bc3d-2363-45b3-befb-1190c25 f3c8b/MLG-41.pdf?MOD=AJPERES).
7. Anonymous Report on Campylobacter Testing of Poultry Products - Decision to Suspend the Qualitative Test (30mL) 2013, Food Safety and Inspection Services, U.S. Department of Agriculture, (Available at http://www.fsis.usda.gov/wps/wcm/connect/0c4adb75-51a4-4b77-9f13-07d6158 9812e/Campylobacter_Methods_Comparison_Report.pdf?MOD=AJPERES).
8. Anonymous R: a language and environment for statistical computing http://www.R-project.org.
9. Baggerman W.I., Koster T. A comparison of enrichment and membrane filtration methods for the isolation of Campylobacter from fresh and frozen foods. Food Microbiol. 1992, 9:87-94.
10. Baylis C.L., MacPhee S., Martin K.W., Humphrey T.J., Betts R.P. Comparison of three enrichment media for the isolation of Campylobacter spp. from foods. J. Appl. Microbiol. 2000, 89:884-891.
11. Bessede E., Delcamp A., Sifre E., Buissonniere A., Megraud F. New methods for detection of campylobacters in stool samples in comparison to culture. J. Clin. Microbiol. 2011, 49:941-944.
12. Black R.E., Levine M.M., Clements M.L., Hughes T.P., Blaser M.J. Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 1988, 157:472-479.
13. Bolton F.J., Coates D. Development of a blood-free Campylobacter medium: screening tests on basal media and supplements, and the ability of selected supplement to facilitate aerotolerance. J. Appl. Bacteriol. 1983, 54:115-125.
14. Bolton F.J., Robertson L. A selective medium for isolating Campylobacter jejuni/coli. J. Clin. Pathol. 1982, 35:462-467.
15. Border M.M., Firehammer B.D., Myers L.L. Tube culture method for viable counts of Campylobacter fetus (Vibrio fetus). Appl. Microbiol. 1974, 28:730-732.
16. Bowdre J.H., Krieg N.R., Hoffman P.S., Smibert R.M. Stimulatory effect of dihydroxyphenyl compounds on the aerotolerance of Spirillum volutans and Campylobacter fetus subspecies jejuni. Appl. Environ. Microbiol. 1976, 31:127-133.
17. Chon J.W., Hyeon J.Y., Park J.H., Song K.Y., Seo K.H. Comparison of 2 types of broths and 3 selective agars for the detection of Campylobacter species in whole-chicken carcass-rinse samples. Poult. Sci. 2012, 2012(91):2382-2385.
18. Cloak O.M., Fratamico P.M. A multiplex PCR for the differentiation of Campylobacter jejuni and C. coli from a swine processing facility and characterization of isolates by PFGE and antibiotic resistance profiles. J. Food Prot. 2002, 65:266-273.
19. Corry J.E.L., Post D.E., Colin P., Laisney M.J. Culture media for isolation of campylobacters. Int. J. Food Microbiol. 1995, 26:43-76.
20. Damborg P., Olsen K.E., Moller-Nielsen E., Guardabassi L. Occurrence of Campylobacter jejuni in pets living with human patients infected with C. jejuni. J. Clin. Microbiol. 2004, 42:1363-1364.
21. Ferrier P.M., Buzby J.C. The economic efficiency of sampling size: the case of beef trim. Risk Anal. 2013, 33:368-384.
22. Fitzgerald C., Patrick M., Jerris R., Watson R., Tobin-D'Angelo M., Gonzalez A., Polage C., Wymore K., Gillim-Ross L., Sadlowski J., Monahan J., Hurd S., Dahlberg S., DeMartino M., Pentella M., Razeq J., Leonard C., Jung C., Juni B., Robinson T., Gittelman R., Garrigan C., Nachamkin I., Campylobacter diagnostics working group Multicenter study to evaluate diagnostic methods for detection and isolation of Campylobacter from stool. Annual Meeting of the American Society for Microbiology, New Orleans, LA., (n.d.), 20 Sept 2011.
23. Friedman C.R., Hoekstra R.M., Samuel M., Marcus R., Bender, Shiferaw B., Reddy S., Ahuja S.D., Helfrick D.L., Hardnett F., Carter M., Anderson B., Tauxe R.V., Emerging Infections Program FoodNet Working Group Risk factors for sporadic Campylobacter infection in the United States: a case-control study in FoodNet sites. Clin. Infect. Dis. 2004, 38(Suppl. 3):S285-S296.
24. Gharst G., Bark D.H., Newkirk D., Guillen L., Wang Q., Abeyta C. Evaluation and single laboratory verification of a proposed modification to the U.S. Food and Drug Administration method for the detection and identification of Campylobacter jejuni or Campylobacter coli from raw silo milk. J. AOAC Int. 2013, (accepted for publication).
25. Gilliss D., et al. Incidence and trends of infection with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. sites, 1996-2012. MMWR Morb. Mortal. Wkly Rep. 2013, 62:283-287.
26. George H.A., Hoffman P.S., Smibert R.M., Krieg N.R. Improved media for growth and aerotolerance of Campylobacter fetus. J. Clin. Microbiol. 1978, 8:36-41.
27. Granato P., Chen L., Holiday I., Rawling R., Novak-Weekley S., Quinlan T., Musser K. Comparison of premier CAMPY enzyme immunoassay (EIA), ProSpecT Campylobacter EIA, and ImmunoCard STAT! CAMPY tests with culture for laboratory diagnosis of Campylobacter enteric infections. J. Clin. Microbiol. 2010, 48:4022-4027.
28. Habib I., Sampers I., Uyttendaele M., Berkvens D., De Zutter L. Performance characteristics and estimation of measurement uncertainty of three plating procedures for Campylobacter enumeration in chicken meat. Food Microbiol. 2008, 25:65-74.
29. Habib I., Uyttendaele M., De Zutter L. Evaluation of ISO 10272:2006 standard versus alternative enrich-ment and plating combinations for enumeration and detection of Campylobacter in chicken meat. Food Microbiol. 2011, 28:1117-1123.
30. He Y., Yao X., Gunther N.W., Xie Y., Tu S.-I., Shi X. Simultaneous detection and differentiation of Campylobacter jejuni, C. coli, and C. lari in chickens using a multiplex real-time PCR assay. Food Anal. Methods 2010, 3:321-329.
31. Heuvelink A.E., van Heerwaarden C., Zwartkruis-Nahuis A., Tilburg J.J., Bos M.H., Heilmann F.G., Hofhuis A., Hoekstra T., de Boer E. Two outbreaks of campylobacteriosis associated with the consumption of raw cow's milk. Int. J. Food Microbiol. 2009, 134:70-74.
32. Hunt J.M., Abeyta C., Tran T. Bacteriological Analytical Manual, Chapter 7 Campylobacter 2001, FDA, (http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/Bacteriologic alAnalyticalManualBAM/ucm072616.htm).
33. Hutchinson D.N., Bolton F.J. Improved blood free selective medium for the isolation of Campylobacter jejuni from faecal specimens. J. Clin. Pathol. 1984, 37:956-957.
34. Jarvis B. The distribution of microorganisms in foods in relation to sampling, Chapter 4. Statistical Aspects of the Microbiological Examination of Foods 2008, 45-277. Academic Press, Elsevier. 2nd Ed. B. Jarvis (Ed.).
35. Jay-Russell M.T., Mandrell R.E., Yuan J., Bates A., Manalac R., Mohle-Boetani J., Kimura A., Lidgard J., Miller W.G. Using MOMP typing as an epidemiologic tool to investigate milkborne Campylobacter jejuni outbreaks in California. J. Clin. Microbiol. 2013, 51:195-201.
36. Kaldor J., Speed B.R. GBS and Campylobacter jejuni: a serological study. Br. Med. J. 1984, 288:1867-1870.
37. King E.O. Human infections with Vibrio fetus and a closely related vibrio. J. Infect. Dis. 1957, 101:119-128.
38. Le Roux E., Lastovica A.J. The Cape Town protocol: how to isolate the most campylobacters for your dollar, pound, franc, yen, etc. Campylobacter, Helicobacter and related organisms 1998, 30-33. The Rustica Press, Pinelands, South Africa. A.J. Lastovica, D.G. Newell, E.E. Lastovica (Eds.).
39. Lejeune J.T., Rajala-Schultz P.J. Food safety: unpasteurized milk: a continued public health threat. Clin. Infect. Dis. 2009, 48:93-100.
40. Linton D., Lawson A.J., Owen R.J., Stanley J. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J. Clin. Microbiol. 1997, 35:2568-2572.
41. Liu L., Hussain S.K., Miller R.S., Oyarzabal O.A. Research note: efficacy of mini VIDAS for the detection of Campylobacter spp. from retail broiler meat enriched in Bolton broth with or without the supplementation of blood. J. Food Prot. 2009, 72:2428-2432.
42. Man S.M. The clinical importance of emerging Campylobacter species. Nat. Rev. Gastroenterol. Hepatol. 2011, 8:669-685.
43. Miller R.S., Speegle L., Lastovica A.J., Oyarzabal O.A. Letter to the Editor. An evaluation of three commercial latex agglutination tests for the identification of Campylobacter spp. J. Clin. Microbiol. 2008, 46:3546-3547.
44. Moon H., Kim S.B., Chen J.J., George N.I., Kodell R.L. Model uncertainty and model averaging in the estimation of infectious doses for microbial pathogens. Risk Anal. 2013, 33:220-231.
45. Morris G.K., el Sherbeeny M.R., Patton C.M., Kodaka H., Lombard G.L., Edmonds P., Hollis D.G., Brenner D.J. Comparison of four hippurate hydrolysis methods for identification of thermophilic Campylobacter spp. J. Clin. Microbiol. 1985, 22:714-718.
46. Oliver S.P., Boor K.J., Murphy S.C., Murinda S.E. Food safety hazards associated with consumption of raw milk. Foodborne Pathog. Dis. 2009, 6:793-806.
47. Oyarzabal O.A., Battie C. Immunological methods for the detection of Campylobacter spp. - current applications and potential use in biosensors. Trends in Immunolabelled and Related Techniques 2012, 203-226. InTech. E. Abuelzein (Ed.).
48. Oyarzabal O.A., Wesley I.V., Barbaree J.M., Lauerman L.H., Conner D.E. Specific detection of Campylobacter lari by PCR. J. Microbiol. Meth. 1997, 29:97-102.
49. Oyarzabal O.A., Macklin K.S., Barbaree J.M., Miller R.S. Evaluation of agar plates for direct enumeration of Campylobacter spp. from poultry carcass rinses. Appl. Environ. Microbiol. 2005, 71:3351-3354.
50. Oyarzabal O.A., Backert S., Nagaraj M., Miller R.S., Hussain S.K., Oyarzabal E.A. Efficacy of supplemented buffered peptone water for the isolation of Campylobacter jejuni and C. coli from broiler retail products. J. Microbiol. Methods 2007, 69:129-136.
51. Oyarzabal O.A., Williams A., Zhou P., Samadpour M. Improved protocol for isolation of Campylobacter spp. from retail broiler meat and use of pulsed field gel electrophoresis for the typing of isolates. J. Microbiol. Meth. 2013, (Available online 29 March 2013 (http://www.sciencedirect.com/science/article/pii/S0167701213001024)).
52. Oyofo B.A., Thornton S.A., Burr D.H., Trust T.J., Pavlovskis O.R., Guerry P. Specific detection of Campylobacter jejuni and Campylobacter coli by using polymerase chain reaction. J. Clin. Microbiol. 1992, 30:2613-2619.
53. Painter J.A., Hoekstra R.M., Ayers T., Tauxe R.V., Braden C.R., Angulo F.J., Griffin P.A. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerg. Infect. 2013, 19:407-415.
54. Persson S., Olsen K.E.P. Multiplex PCR for identification of Campylobacter coli and Campylobacter jejuni from pure cultures and directly on stool samples. J. Med. Microbiol. 2005, 54:1043-1047.
55. Plumer G.L., Duvall W.C., Shepler V.M. A preliminary report on a new technique for isolation of Vibrio fetus from carrier bulls. Gen. Vet. 1962, 52:110-122.
56. Potturi-Venkata L.P., Backert S., Lastovica A.J., Vieira S.L., Norton R.A., Miller R.S., Pierce S.J., Oyarzabal O.A. Evaluation of different plate media for direct cultivation of Campylobacter spp. from live broilers. Poult. Sci. 2007, 86:1304-1311.
57. Reiter M.G., López C., Jordano R., Medina L.M. Comparative study of alternative methods for food safety control in poultry slaughterhouses. Food Anal. Meth. 2010, 3:253-260.
58. Robinson D.A., Edgar W.M., Gibson G.L., Matchett A.A., Robertson L. Campylobacter enteritis associated with consumption of unpasteurized milk. Br. Med. J. 1979, 1:1171-1173.
59. Robinson D.A. Infective dose of Campylobacter jejuni in milk. Br. Med. J. 1981, 282:1584.
60. Sails A.D., Wareing D.R.A., Bolton F.J. Evaluation of three microaerobic systems for the growth and recovery of Campylobacter spp. Campylobacter, Helicobacter and related organisms 1998, 39-42. The Rustica Press, Pinelands, South Africa. A.J. Lastovica, D.G. Newell, E.E. Lastovica (Eds.).
61. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., Jones J.L., Griffin P.M. Foodborne illness acquired in the United States - major pathogens. Emerg. Infect. Dis. 2011, 17:7-15.
62. Schnaitman C.A. Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J. Bacteriol. 1970, 104:890-901.
63. Schildt M., Savolainen S., Hanninen M.L. Long-lasting Campylobacter jejuni contamination of milk associated with gastrointestinal illness in a farming family. Epidemiol. Infect. 2006, 134:401-405.
64. Smith M.V., Muldoon P.J. Campylobacter fetus subsp. jejuni (Vibrio fetus) from commercially processed poultry. Appl. Microbiol. 1974, 27:995-996.
65. Smith K., Reimers N., Barnes H.J., Lee B.C., Siletzky R., Kathariou S. Campylobacter colonization of sibling turkey flocks reared under different management conditions. J. Food Prot. 2004, 67:1463-1468.
66. Solomon E.B., Hoover D.G. Campylobacter jejuni: a bacterial paradox. J. Food Safety. 1999, 19:121-136.
67. Speed B., Kaldor J., Cavanagh P. Guillain-Barre syndrome associated with Campylobacter jejuni enteritis. J. Infect. 1984, 8:85-86.
68. Speegle L., Miller M.E., Backert S., Oyarzabal O.A. Research note: use of cellulose filters to isolate Campylobacter spp. from naturally contaminated retail broiler meat. J. Food Prot. 2009, 72:2592-2596.
69. Steele T.W., McDermott S.N. The use of the membrane filters applied directly to the surface of agar plates for the isolation of Campylobacter jejuni from feces. Pathology 1984, 16:263-265.
70. Suzuki H., Yamamoto S. Campylobacter contamination in retail poultry meats and by-products in the world: a literature survey. J. Vet. Med. Sci. 2009, 71:255-261.
71. Taylor E.V., Herman K.M., Ailes E.C., Fitzgerald C., Yoder J.S., Mahon B.E., Tauxe R.V. Common source outbreaks of Campylobacter infection in the USA, 1997-2008. Epidemiol. Inf. 2013, 141:987-996.
72. Tenkate T.D., Stafford R.J. Risk factors for Campylobacter infection in infants and young children: a matched case-control study. Epidemiol. Infect. 2001, 127:399-404.
73. Tribble D., Baqar S., Pang L., Mason C., Houng H., Pitarangsi C., Lebron C., Armstrong A., Sethabutr O., Sanders J. Diagnostic approach to acute diarrheal illness in a military population on training exercises in Thailand, a region of Campylobacter hyperendemicity. J. Clin. Microbiol. 2008, 46:1418-1425.
74. Vihavainen E.J., Björkroth J. Microbial ecology and spoilage of poultry meat and poultry meat products. Handbook of Poultry Science and Technology, Secondary Processing 2010, vol. 2:485-493. Blackwell-Wiley, New York, NY. Guerrero-Legarreta (Ed.).
75. Williams A., Oyarzabal O.A. Prevalence of Campylobacter spp. in skinless, boneless retail broiler meat from 2005 through 2011 in Alabama, USA. BMC Microbiol. 2012, 12:184.
76. Wonglumsom W., Vishnubhatl A., Kim J.M., Fung D.Y. Enrichment media for isolation of Campylobacter jejuni from inoculated ground beef and chicken skin under normal atmosphere. J. Food Prot. 2001, 64:630-634.
77. Zhou P., Hussain S.K., Liles M.R., Arias C.R., Backert S., Kieninger J.R., Oyarzabal O.A. A simplified and cost-effective enrichment protocol for the isolation of Campylobacter spp. from retail broiler meat without microaerobic incubation. BMC Microbiol. 2011, 11:175.