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Agriculture  2013 

Identification of Multiple Subtypes of Campylobacter jejuni in Chicken Meat and the Impact on Source Attribution

DOI: 10.3390/agriculture3030579

Keywords: multiple subtypes, chicken carcass, diversity, enrichment, C. jejuni

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Abstract:

Most source attribution studies for Campylobacter use subtyping data based on single isolates from foods and environmental sources in an attempt to draw epidemiological inferences. It has been suggested that subtyping only one Campylobacter isolate per chicken carcass incurs a risk of failing to recognise the presence of clinically relevant, but numerically infrequent, subtypes. To investigate this, between 21 and 25 Campylobacter jejuni isolates from each of ten retail chicken carcasses were subtyped by pulsed-field gel electrophoresis (PFGE) using the two restriction enzymes SmaI and KpnI. Among the 227 isolates, thirteen subtypes were identified, the most frequently occurring subtype being isolated from three carcasses. Six carcasses carried a single subtype, three carcasses carried two subtypes each and one carcass carried three subtypes. Some subtypes carried by an individual carcass were shown to be potentially clonally related. Comparison of C. jejuni subtypes from chickens with isolate subtypes from human clinical cases ( n = 1248) revealed seven of the thirteen chicken subtypes were indistinguishable from human cases. None of the numerically minor chicken subtypes were identified in the human data. Therefore, typing only one Campylobacter isolate from individual chicken carcasses may be adequate to inform Campylobacter source attribution.

References

[1]  Notifiable and Other Diseases in New Zealand. Annual Report 2006; ESR: Porirua, New Zealand, 2006; p. 13.
[2]  Mullner, P.; Spencer, S.E.; Wilson, D.J.; Jones, G.; Noble, A.D.; Midwinter, A.C.; Collins-Emerson, J.M.; Carter, P.; Hathaway, S.; French, N.P. Assigning the source of human campylobacteriosis in New Zealand: A comparative genetic and epidemiological approach. Infect. Genet. Evol. 2009, 9, 1311–1319, doi:10.1016/j.meegid.2009.09.003.
[3]  Notifiable and Other Diseases in New Zealand. Annual Report 2012; ESR: Porirua, New Zealand, 2012; p. 25.
[4]  Devane, M.L.; Nicol, C.; Ball, A.; Klena, J.D.; Scholes, P.; Hudson, J.A.; Baker, M.G.; Gilpin, B.J.; Garrett, N.; Savill, M.G. The occurrence of Campylobacter subtypes in environmental reservoirs and potential transmission routes. J. Appl. Microbiol. 2005, 98, 980–990, doi:10.1111/j.1365-2672.2005.02541.x.
[5]  Kramer, J.M.; Frost, J.A.; Bolton, F.J.; Wareing, D.R. Campylobacter contamination of raw meat and poultry at retail sale: Identification of multiple types and comparison with isolates from human infection. J. Food Prot. 2000, 63, 1654–1659.
[6]  Gillespie, I.A.; O’Brien, S.J.; Adak, G.K.; Tam, C.C.; Frost, J.A.; Bolton, F.J.; Tompkins, D.S. Point source outbreaks of Campylobacter jejuni infection—Are they more common than we think and what might cause them? Epidemiol. Infect. 2003, 130, 367–375.
[7]  Kuusi, M.; Nuorti, J.P.; Hanninen, M.L.; Koskela, M.; Jussila, V.; Kela, E.; Miettinen, I.; Ruutu, P. A large outbreak of campylobacteriosis associated with a municipal water supply in Finland. Epidemiol. Infect. 2005, 133, 593–601, doi:10.1017/S0950268805003808.
[8]  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. Infect. 2013, 141, 987–996, doi:10.1017/S0950268812001744.
[9]  Garrett, N.; Devane, M.L.; Hudson, J.A.; Nicol, C.; Ball, A.; Klena, J.D.; Scholes, P.; Baker, M.G.; Gilpin, B.J.; Savill, M.G. Statistical comparsion of Campylobacter jejuni subtypes from human cases and environmental sources. J. Appl. Microbiol. 2007, 103, 2113–2121, doi:10.1111/j.1365-2672.2007.03437.x.
[10]  Michaud, S.; Menard, S.; Arbeit, R.D. Role of real-time molecular typing in the surveillance of Campylobacter enteritis and comparison of pulsed-field gel electrophoresis profiles from chicken and human isolates. J. Clin. Microbiol. 2005, 43, 1105–1111, doi:10.1128/JCM.43.3.1105-1111.2005.
[11]  Nichols, G.L.; Richardson, J.F.; Sheppard, S.K.; Lane, C.; Sarran, C. Campylobacter epidemiology: A descriptive study reviewing 1 million cases in England and Wales between 1989 and 2011. BMJ Open 2012, 2, doi:10.1136/bmjopen-2012-001179.
[12]  Pebody, R.G.; Ryan, M.J.; Wall, P.G. Outbreaks of Campylobacter infection: Rare events for a common pathogen. Commun. Dis. Rep. CDR Rev. 1997, 7, R33–R37.
[13]  Nielsen, E.M.; Fussing, V.; Engberg, J.; Nielsen, N.L.; Neimann, J. Most Campylobacter subtypes from sporadic infections can be found in retail poultry products and food animals. Epidemiol. Infect. 2006, 134, 758–767, doi:10.1017/S0950268805005509.
[14]  Dopfer, D.; Buist, W.; Soyer, Y.; Munoz, M.A.; Zadoks, R.N.; Geue, L.; Engel, B. Assessing genetic heterogeneity within bacterial species isolated from gastrointestinal and environmental samples: How many isolates does it take? Appl. Environ. Microbiol. 2008, 74, 3490–3496, doi:10.1128/AEM.02789-07.
[15]  Forbes, K.J.; Gormley, F.J.; Dallas, J.F.; Labovitiadi, O.; MacRae, M.; Owen, R.J.; Richardson, J.; Strachan, N.J.; Cowden, J.M.; Ogden, I.D.; et al. Campylobacter immunity and coinfection following a large outbreak in a farming community. J. Clin. Microbiol. 2009, 47, 111–116, doi:10.1128/JCM.01731-08.
[16]  Gilpin, B.; Robson, B.; Lin, S.; Scholes, P.; On, S. Pulsed-field gel electrophoresis analysis of more than one clinical isolate of Campylobacter spp. from each of 49 patients in New Zealand. J. Clin. Microbiol. 2012, 50, 457–459, doi:10.1128/JCM.05928-11.
[17]  Godschalk, P.C.R.; Gilbert, M.; Jacobs, B.C.; Kramers, T.; Tio-Gillen, A.P.; Ang, C.W.; van den Braak, N.; Li, J.; Verbrugh, H.A.; van Belkum, A.; et al. Co-infection with two different Campylobacter jejuni strains in a patient with the Guillain-Barré Syndrome. Microbes Infect. 2006, 8, 248–253, doi:10.1016/j.micinf.2005.06.022.
[18]  Richardson, J.F.; Frost, J.A.; Kramer, J.M.; Thwaites, R.T.; Bolton, F.J.; Wareing, D.R.; Gordon, J.A. Coinfection with Campylobacter species: An epidemiological problem? J. Appl. Microbiol. 2001, 91, 206–211, doi:10.1046/j.1365-2672.2001.01377.x.
[19]  Balmer, O.; Tanner, M. Prevalence and implications of multiple-strain infections. Lancet Infect. Dis. 2011, 11, 868–878, doi:10.1016/S1473-3099(11)70241-9.
[20]  Hiett, K.L.; Stern, N.J.; Fedorka-Cray, P.; Cox, N.A.; Musgrove, M.T.; Ladely, S. Molecular subtype analyses of Campylobacter spp. from Arkansas and California poultry operations. Appl. Environ. Microbiol. 2002, 68, 6220–6236, doi:10.1128/AEM.68.12.6220-6236.2002.
[21]  Simmons, M.; Hiett, K.L.; Stern, N.J.; Frank, J.F. Comparison of poultry exudate and carcass rinse sampling methods for the recovery of Campylobacter spp. subtypes demonstrates unique subtypes recovered from exudate. J. Microbiol. Methods 2008, 74, 89–93, doi:10.1016/j.mimet.2008.03.007.
[22]  Denis, M.; Rose, V.; Huneau-Salaun, A.; Balaine, L.; Salvat, G. Diversity of pulsed-field gel electrophoresis profiles of Campylobacter jejuni and Campylobacter coli from broiler chickens in France. Poult. Sci. 2008, 87, 1662–1671, doi:10.3382/ps.2008-00010.
[23]  Schlager, T.A.; Hendley, J.O.; Bell, A.L.; Whittam, T.S. Clonal diversity of Escherichia coli colonizing stools and urinary tracts of young girls. Infect. Immun. 2002, 70, 1225–1229, doi:10.1128/IAI.70.3.1225-1229.2002.
[24]  Barton, C.; Ng, L.K.; Tyler, S.D.; Clark, C.G. Temperate bacteriophages affect pulsed-field gel electrophoresis patterns of Campylobacter jejuni. J. Clin. Microbiol. 2007, 45, 386–391, doi:10.1128/JCM.01513-06.
[25]  Lindmark, H.; Harbom, B.; Thebo, L.; Andersson, L.; Hedin, G.; Osterman, B.; Lindberg, T.; Andersson, Y.; Westoo, A.; Olsson Engvall, E. Genetic characterization and antibiotic resistance of Campylobacter jejuni isolated from meats, water, and humans in sweden. J. Clin. Microbiol. 2004, 42, 700–706, doi:10.1128/JCM.42.2.700-706.2004.
[26]  Dickins, M.; Franklin, S.; Stefanova, R.; Schutze, G.; Eisenach, K.; Wesley, I.; Cave, M. Diversity of Campylobacter isolates from retail poultry carcasses and from humans as demonstrated by pulsed-field gel electrophoresis. J. Food Prot. 2002, 65, 957–962.
[27]  Lindmark, H.; Diedrich, I.C.; Andersson, L.; Lindqvist, R.; Engvall, E.O. Distribution of Campylobacter genotypes on broilers during slaughter. J. Food Prot. 2006, 69, 2902–2907.
[28]  Hunter, S.M.; Berrang, M.E.; Meinersmann, R.J.; Harrison, M.A. Genetic diversity of Campylobacter on broiler carcasses collected pre evisceration and postchill in 17 U.S. poultry processing plants. J. Food Prot. 2009, 72, 49–54.
[29]  Scates, P.; Moran, L.; Madden, R.H. Effect of incubation temperature on isolation of Campylobacter jejuni genotypes from foodstuffs enriched in Preston broth. Appl. Environ. Microbiol. 2003, 69, 4658–4661, doi:10.1128/AEM.69.8.4658-4661.2003.
[30]  Sheppard, S.K.; Dallas, J.F.; Strachan, N.J.C.; MacRae, M.; McCarthy, N.D.; Wilson, D.J.; Gormley, F.J.; Falush, D.; Ogden, I.D.; Maiden, M.C.J.; et al. Campylobacter genotyping to determine the source of human infection. Clin. Infect. Dis. 2009, 48, 1072–1078, doi:10.1086/597402.
[31]  Skanseng, B.; Trosvik, P.; Zimonja, M.; Johnsen, G.; Bjerrum, L.; Pedersen, K.; Wallin, N.; Rudi, K. Co-infection dynamics of a major food-borne zoonotic pathogen in chicken. PLoS Pathog. 2007, 3, e175, doi:10.1371/journal.ppat.0030175.
[32]  Schouls, L.; Reulen, S.; Duim, B.; Wagenaar, J.; Willems, R.; Dingle, K.; Colles, F.; van Embden, J. Comparative genotyping of Campylobacter jejuni by amplified fragment length polymorphism, multilocus sequence typing, and short repeat sequencing: Strain diversity, host range, and recombination. J. Clin. Microbiol. 2003, 41, 15–26, doi:10.1128/JCM.41.1.15-26.2003.
[33]  Tenover, F.C.; Arbeit, R.D.; Goering, R.V.; Mickelsen, P.A.; Murray, B.E.; Persing, D.H.; Swaminathan, B. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: Criteria for bacterial strain typing. J. Clin. Microbiol. 1995, 33, 2233–2239.
[34]  Melero, B.; Cocolin, L.; Rantsiou, K.; Jaime, I.; Rovira, J. Comparison between conventional and qPCR methods for enumerating Campylobacter jejuni in a poultry processing plant. Food Microbiol. 2011, 28, 1353–1358, doi:10.1016/j.fm.2011.06.006.
[35]  H??k, H.; Fattah, M.A.; Ericsson, H.; V?gsholm, I.; Danielsson-Tham, M. Genotype dynamics of Campylobacter jejuni in a broiler flock. Vet. Microbiol. 2005, 106, 109–117, doi:10.1016/j.vetmic.2004.12.017.
[36]  Manning, G.; Duim, B.; Wassenaar, T.; Wagenaar, J.A.; Ridley, A.; Newell, D.G. Evidence for a genetically stable strain of Campylobacter jejuni. Appl. Environ. Microbiol. 2001, 67, 1185–1189, doi:10.1128/AEM.67.3.1185-1189.2001.
[37]  H?nninen, M.L.; Pajarre, S.; Klossner, M.L.; Rautelin, H. Typing of human Campylobacter jejuni isolates in Finland by pulsed-field gel electrophoresis. J. Clin. Microbiol. 1998, 36, 1787–1789.
[38]  Wong, T.; Devane, M.; Hudson, J.A.; Scholes, P.; Savill, M.; Klena, J. Validation of a PCR method for Campylobacter detection on poultry packs. Br. Food J. 2004, 106, 642–650, doi:10.1108/00070700410558175.
[39]  Fraser, A.D.; Chandan, V.; Yamazaki, H.; Brooks, B.W.; Garcia, M.M. Simple and economical culture of Campylobacter jejuni and Campylobacter coli in CO2 in moist air. Int. J. Food Microbiol. 1992, 15, 377–382, doi:10.1016/0168-1605(92)90071-A.
[40]  Griffiths, P.L.; Park, R.W.A. Campylobacters associated with human diarrhoeal disease. J. Appl. Bacteriol. 1990, 69, 281–301, doi:10.1111/j.1365-2672.1990.tb01519.x.
[41]  Barros-Velázquez, J.; Jimenez, A.; Villa, T.G. Isolation and typing methods for the epidemiologic investigation of thermotolerant campylobacters. Int. Microbiol. 1999, 2, 217–226.
[42]  Ribot, E.M.; Fitzgerald, C.; Kubota, K.; Swaminathan, B.; Barrett, T.J. Rapid pulsed-field gel electrophoresis protocol for subtyping of Campylobacter jejuni. J. Clin. Microbiol. 2001, 39, 1889–1894, doi:10.1128/JCM.39.5.1889-1894.2001.
[43]  Hunter, S.B.; Vauterin, P.; Lambert-Fair, M.A.; van Duyne, M.S.; Kubota, K.; Graves, L.; Wrigley, D.; Barrett, T.; Ribot, E. Establishment of a universal size standard strain for use with the pulsenet standardized pulsed-field gel electrophoresis protocols: Converting the national databases to the new size standard. J. Clin. Microbiol. 2005, 43, 1045–1050, doi:10.1128/JCM.43.3.1045-1050.2005.
[44]  Speck, M.L. Sampling Plans, 2nd ed. ed.; American Public Health Association: Washington, DC, USA, 1984.
[45]  Ribot, E.; National Center for Infectious Diseases; CDC Division of Bacterial and Mycotic Diseases; Foodborne and Diarrheal Diseases Branch; Public Health Practice Program Office; CDC, Division of Laboratory Services; CDC, and Association of Public Health Laboratories. Standardized Molecular Subtyping of Foodborne Bacterial Pathogens by Pulsed-Field Gel Electrophoresis; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2002.

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