AIMS Microbiology, 2018, 4(3): 439-454. doi: 10.3934/microbiol.2018.3.439

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Broiler chicken carcasses and their associated abattoirs as a source of enterotoxigenic Clostridium perfringens: Prevalence and critical steps for contamination

1 Research Chair in Meat Safety, Département de Pathologie et Microbiologie, Faculté de médecine vétérinaire, Université de Montréal, 3200 Sicotte, St-Hyacinthe, Québec, Canada
2 Swine and Poultry Infectious Diseases Research Centre (CRIPA), Faculté de médecine vétérinaire, Université de Montréal, 3200 Sicotte, St-Hyacinthe, Québec, Canada
3 Olymel S.E.C./L.P., Québec, Canada, 2200 Avenue Léon-Pratte, St-Hyacinthe, Québec, Canada

Clostridium perfringens ranks among the three most frequent bacterial pathogens causing human foodborne diseases in Canada, and poultry meat products are identified as a source of infection for humans. The objective of the current study was to estimate the proportion of broiler chicken flocks, carcasses and various environmental samples from critical locations of the slaughter plant positive for the presence of C. perfringens enterotoxin encoding gene (cpe). From the 16 visits conducted, 25% of the 79 flocks sampled, 10% of the 379 carcasses sampled and 5% of the 217 environmental samples collected were found positive for cpe. The proportion of cpe-positive carcasses was statistically different between surveyed plants, with 17.0% for one abattoir and 2.2% for the other. For the most contaminated plant, cpe-positive carcasses were identified at each step of the processing line, with prevalence varying between 10.0% and 25.0%, whereas this prevalence varied between 0% and 25.0% for the environmental surfaces sampled. Based on the results obtained, enterotoxigenic C. perfringens strains could potentially represent a risk for the consumer.
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1. Thomas MK, Murray R, Flockhart L, et al. (2015) Estimates of foodborne illness-related hospitalizations and deaths in Canada for 30 specified pathogens and unspecified agents. Foodborne Pathog Dis 12: 820–827.    

2. Thomas MK, Murray R, Flockhart L, et al. (2013) Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog Dis 10: 639–648.    

3. Scallan E, Hoekstra RM, Angulo FJ, et al. (2011) Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17: 7–15.    

4. Havelaar AH, Galindo AV, Kurowicka D, et al. (2008) Attribution of foodborne pathogens using structured expert elicitation. Foodborne Pathog Dis 5: 649–659.    

5. Guran HS, Oksuztepe G (2013) Detection and typing of Clostridium perfringens from retail chicken meat parts. Lett Appl Microbiol 57: 77–82.    

6. Kaneko I, Miyamoto K, Mimura K, et al. (2011) Detection of enterotoxigenic Clostridium perfringens in meat samples by using molecular methods. Appl Environ Microbiol 77: 7526–7532.    

7. Miki Y, Miyamoto K, Kaneko-Hirano I, et al. (2008) Prevalence and characterization of enterotoxin gene-carrying Clostridium perfringens isolates from retail meat products in Japan. Appl Environ Microbiol 74: 5366–5372.    

8. Wen Q, McClane BA (2004) Detection of enterotoxigenic Clostridium perfringens type A isolates in American retail foods. Appl Environ Microbiol 70: 2685–2691.    

9. Lin YT, Labbe R (2003) Enterotoxigenicity and genetic relatedness of Clostridium perfringens isolates from retail foods in the United States. Appl Environ Microbiol 69: 1642–1646.    

10. Khan M, Nazir J, Anjum AA, et al. (2015) Toxinotyping and antimicrobial susceptibility of enterotoxigenic Clostridium perfringens isolates from mutton, beef and chicken meat. J Food Sci Technol 52: 5323–5328.    

11. Miwa N, Nishina T, Kubo S, et al. (1997) Most probable number method combined with nested polymerase chain reaction for detection and enumeration of enterotoxigenic Clostridium perfringens in intestinal contents of cattle, pig and chicken. J Vet Med Sci 59: 89–92.    

12. Nowell VJ, Poppe C, Parreira VR, et al. (2010) Clostridium perfringens in retail chicken. Anaerobe 16: 314–315.    

13. Schalch B, Bjorkroth J, Eisgruber H, et al. (1997) Ribotyping for strain characterization of Clostridium perfringens isolates from food poisoning cases and outbreaks. Appl Environ Microbiol 63: 3992–3994.

14. McCrea BA, Macklin KS (2006) Effect of different cleaning regimens on recovery of Clostridium perfringens on poultry live haul containers. Poultry Sci 85: 909–913.    

15. Lahti P, Lindstrom M, Somervuo P, et al. (2012) Comparative genomic hybridization analysis shows different epidemiology of chromosomal and plasmid-borne cpe-carrying Clostridium perfringens type A. PLoS One 7: e46162.    

16. Lindstrom M, Heikinheimo A, Lahti P, et al. (2011) Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol 28: 192–198.    

17. Li JH, Sayeed S, McClane BA (2007) Prevalence of enterotoxigenic Clostridium perfringens isolates in Pittsburgh (Pennsylvania) area soils and home kitchens. Appl Environ Microbiol 73: 7218–7224.    

18. Mueller-Spitz SR, Stewart LB, Klump JV, et al. (2010) Freshwater suspended sediments and sewage are reservoirs for enterotoxin-positive Clostridium perfringens. Appl Environ Microbiol 76: 5556–5562.    

19. Abbona CC, Stagnitta PV (2016) Clostridium perfringens: Comparative effects of heat and osmotic stress on non-enterotoxigenic and enterotoxigenic strains. Anaerobe 39: 105–113.    

20. Li J, Paredes-Sabja D, Sarker MR, et al. (2016) Clostridium perfringens sporulation and sporulation-associated toxin production. Microbiol Spectrum 4: 1–27.

21. Xiao Y, Wagendorp A, Moezelaar R, et al. (2012) A wide variety of Clostridium perfringens type a food-borne isolates that carry a chromosomal cpe gene belong to one multilocus sequence typing cluster. Appl Environ Microbiol 78: 7060–7068.    

22. Rouger A, Tresse O, Zagorec M (2017) Bacterial contaminants of poultry meat: Sources, species, and dynamics. Microorganisms 5: 1–16.

23. Craven SE, Stern NJ, Bailey JS, et al. (2001) Incidence of Clostridium perfringens in broiler chickens and their environment during production and processing. Avian Dis 45: 887–896.    

24. Juneja VK, Novak JS, Labbe RL (2010) Clostridium perfringens, In: Juneja VK, Sofos JN, Pathogens and Toxins in Foods: Challenges and Interventions, Washington: ASM Press, 53–70.

25. Garcia-Sanchez L, Melero B, Jaime I, et al. (2017) Campylobacter jejuni survival in a poultry processing plant environment. Food Microbiol 65: 185–192.    

26. Seliwiorstow T, Bare J, Van Damme I, et al. (2016) Transfer of Campylobacter from a positive batch to broiler carcasses of a subsequently slaughtered negative batch: a quantitative approach. J Food Protect 79: 896–901.    

27. Seliwiorstow T, Bare J, Van Damme I, et al. (2015) Campylobacter carcass contamination throughout the slaughter process of Campylobacter-positive broiler batches. Int J Food Microbiol 194: 25–31.    

28. Seliwiorstow T, Bare J, Berkvens D, et al. (2016) Identification of risk factors for Campylobacter contamination levels on broiler carcasses during the slaughter process. Int J Food Microbiol 226: 26–32.    

29. Rivera-Perez W, Barquero-Calvo E, Zamora-Sanabria R (2014) Salmonella contamination risk points in broiler carcasses during slaughter line processing. J Food Protect 77: 2031–2034.    

30. Park HJ, Chon JW, Lim JS, et al. (2015) Prevalence analysis and molecular characterization of Salmonella at different processing steps in broiler slaughter plants in South Korea. J Food Sci 80: M2822–M2826.    

31. Zweifel C, Althaus D, Stephan R (2015) Effects of slaughter operations on the microbiological contamination of broiler carcasses in three abattoirs. Food Control 51: 37–42.    

32. Deguchi A, Miyamoto K, Kuwahara T, et al. (2009) Genetic characterization of type A enterotoxigenic Clostridium perfringens strains. PLoS One 4: e5598.    

33. US Department of Agriculture (2013) Fsis directives Salmonella and Campylobacter verification program for raw meat and poultry products, Washington.

34. Luning PA, Jacxsens L, Rovira J, et al. (2011) A concurrent diagnosis of microbiological food safety output and food safety management system performance: Cases from meat processing industries. Food Control 22: 555–565.    

35. Gaucher ML, Perron GG, Arsenault J, et al. (2017) Recurring Necrotic Enteritis Outbreaks in Commercial Broiler Chicken Flocks Strongly Influence Toxin Gene Carriage and Species Richness in the Resident Clostridium perfringens Population. Front Microbiol 8: 881.    

36. Miwa N, Nishina T, Kubo S, et al. (1998) Amount of enterotoxigenic Clostridium perfringens in meat detected by nested PCR. Int J Food Microbiol 42: 195–200.    

37. Singh RV, Bhilegaonkar KN, Agarwal RK (2005) Studies on occurrence and characterization of Clostridium perfringens from select meats. J Food Safety 25: 146–156.    

38. Lindblad M, Lindmark H, Lambertz ST, et al. (2006) Microbiological baseline study of broiler chickens at Swedish slaughterhouses. J Food Protect 69: 2875–2882.    

39. Tschirdewahn B, Notermans S, Wernars K, et al. (1991) The presence of enterotoxigenic Clostridium-Perfringens strains in faeces of various animals. Int J Food Microbiol 14: 175–178.    

40. Craven SE (2001) Occurrence of Clostridium perfringens in the broiler chicken processing plant as determined by recovery in iron milk medium. J Food Protect 64: 1956–1960.    

41. Craven SE, Cox NA, Bailey JS, et al. (2003) Incidence and tracking of Clostridium perfringens through an integrated broiler chicken operation. Avian Dis 47: 707–711.    

42. Charlebois A, Jacques M, Boulianne M, et al. (2017) Tolerance of Clostridium perfringens biofilms to disinfectants commonly used in the food industry. Food Microbiol 62: 32–38.    

43. BRC Global Standards (2011) Self-Assessment Tool BRC Global Standard for Food Safety Issue 7.

44. Heikinheimo A, Lindstrom M, Granum PE, et al. (2006) Humans as reservoir for enterotoxin gene-carrying Clostridium perfringens type A. Emerg Infect Dis 12: 1724–1729.    

45. Fraise A (2011) Currently available sporicides for use in healthcare, and their limitations. J Hosp Infect 78: 160–160.

46. Udompijitkul PAM, Paredes-Sabja D, Sarker MR (2013) Inactivation strategy for Clostridium perfringens spores adhered to food contact surfaces. Food Microbiol 34: 328–336.    

47. Briancesco R, Veschetti E, Ottaviani M, et al. (2005) Peracetic acid and sodium hypochlorite effectiveness in reducing resistant stages of microorganisms. Cent Eur J Publ Heal 13: 159–162.

48. Grant KA, Kenyon S, Nwafor I, et al. (2008) The identification and characterization of Clostridium perfringens by real-time PCR, location of enterotoxin gene, and heat resistance. Foodborne Pathog Dis 5: 629–639.    

49. Stopforth JD, O'Connor R, Lopes M, et al. (2007) Validation of individual and multiple-sequential interventions for reduction of microbial populations during processing of poultry carcasses and parts. J Food Protect 70: 1393–1401.    

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