Differential outgrowth potential of Clostridium perfringens food-borne isolates with various cpe-genotypes in vacuum-packed ground beef during storage at 12°C

International Journal of Food Microbiology

Volumn 194, Issue , 2015, Pages 40-45

  Xiao, Yinghua ^a,b,c   Wagendorp, Arjen ^a   Abee, Tjakko ^b,c   Wells Bennik, Marjon H J ^a,b  

^a NIZO FOOD RESEARCH   (Netherlands)

^b TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Clostridium perfringens; Cpe; Growth; Low temperature

Indexed keywords

ENTEROTOXIN;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIAL STRAIN; BACTERIUM CONTAMINATION; BACTERIUM ISOLATE; BEEF; CLOSTRIDIUM PERFRINGENS; CONTROLLED STUDY; CPE GENE; FOOD CONTAMINATION; FOOD PACKAGING; FOOD PROCESSING; FOOD STORAGE; GENOTYPE; HEAT TOLERANCE; NONHUMAN; SPOROGENESIS; STORAGE TEMPERATURE; VACUUM; ANIMAL; BOVINE; COLD; FOOD HANDLING; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEAT; MICROBIOLOGY; PLASMID; STANDARDS;

CLOSTRIDIUM PERFRINGENS;

ANIMALS; CATTLE; CLOSTRIDIUM PERFRINGENS; COLD TEMPERATURE; ENTEROTOXINS; FOOD HANDLING; GENES, BACTERIAL; GENOTYPE; MEAT; PLASMIDS; SPORES, BACTERIAL; VACUUM;

EID: 84911408255     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.11.008     Document Type: Article

References (35)

1. Albini S., Brodard I., Jaussi A., Wollschlaeger N., Frey J., Miserez R., Abril C. Real-time multiplex PCR assays for reliable detection of Clostridium perfringens toxin genes in animal isolates. Vet. Microbiol. 2008, 127:179-185.
2. Baums C.G., Schotte U., Amtsberg G., Goethe R. Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. Vet. Microbiol. 2004, 100:11-16.
3. Deguchi A., Miyamoto K., Kuwahara T., Miki Y., Kaneko I., Li J., McClane B.A., Akimoto S. Genetic characterization of type A enterotoxigenic Clostridium perfringens strains. PLoS ONE 2009, 4:e5598.
4. Duncan C.L., Strong D.H. Improved medium for sporulation of Clostridium perfringens. Appl. Microbiol. 1968, 16:82-89.
5. Grant K.A., Kenyon S., Nwafor I., Plowman J., Ohai C., Halford-Maw R., Peck M.W., McLauchlin J. The identification and characterization of Clostridium perfringens by real-time PCR, location of enterotoxin gene, and heat resistance. Foodborne Pathog. Dis. 2008, 5:629-639.
6. Heikinheimo A., Lindstrom M., Korkeala H. Enumeration and isolation of cpe-positive Clostridium perfringens spores from feces. J. Clin. Microbiol. 2004, 42:3992-3997.
7. Huang L.H. Dynamic computer simulation of Clostridium perfringens growth in cooked ground beef. Int. J. Food Microbiol. 2003, 87:217-227.
8. Huang L.H. Estimation of growth of Clostridium perfringens in cooked beef under fluctuating temperature conditions. Food Microbiol. 2003, 20:549-559.
9. Juneja V.K., Thippareddi H. Control of Clostridium perfringens in a model roast beef by salts of organic acids during chilling. J. Food Saf. 2004, 24:95-108.
10. Juneja V., Marmer B.S., Miller J. Growth and sporulation potential of Clostridium perfringens in aerobic and vacuum packaged cooked beef. J. Food Prot. 1994, 57:393-398.
11. Juneja V.K., Thippareddi H., Bari L., Inatsu Y., Kawamoto S., Friedman M. Chitosan protects cooked ground beef and turkey against Clostridium perfringens spores during chilling. J. Food Sci. 2006, 71:M236-M240.
12. Juneja V.K., Thippareddi H., Friedman M. Control of Clostridium perfringens in cooked ground beef by carvacrol, cinnamaldehyde, thymol, or oregano oil during chilling. J. Food Prot. 2006, 69:1546-1551.
13. Juneja V.K., Porto-Fett A.C.S., Gartner K., Tufft L., Luchansky J.B. Potential for growth of Clostridium perfringens from spores in pork scrapple during cooling. Foodborne Pathog. Dis. 2010, 7:153-157.
14. Labbe R.G., Huang T.H. Generation times and modeling of enterotoxin-positive and enterotoxin-negative strains of Clostridium perfringens in laboratory media and ground beef. J. Food Prot. 1995, 58:1303-1306.
15. Lahti P., Heikinheimo A., Johansson T., Korkeala H. Clostridium perfringens type A strains carrying a plasmid-borne enterotoxin gene (genotype IS1151-cpe or IS1470-like-cpe) as a common cause of food poisoning. J. Clin. Microbiol. 2008, 46:371-373.
16. Lahti P., Lindström M., Somervuo P., Heikinheimo A., Korkeala H. Comparative genomic hybridization analysis shows different epidemiology of chromosomal and plasmid-borne cpe-carrying Clostridium perfringens type A. PLoS ONE 2012, 7:e46162.
17. Li J., McClane B.A. Comparative effects of osmotic, sodium nitrite-induced, and pH-induced stress on growth and survival of Clostridium perfringens type A isolates carrying chromosomal or plasmid-borne enterotoxin genes. Appl. Environ. Microbiol. 2006, 72:7620-7625.
18. Li J., McClane B.A. A novel small acid soluble protein variant is important for spore resistance of most Clostridium perfringens food poisoning isolates. PLoS Pathog. 2008, 4:e1000056.
19. Li J., Sayeed S., McClane B.A. Prevalence of enterotoxigenic Clostridium perfringens isolates in Pittsburgh (Pennsylvania) area soils and home kitchens. Appl. Environ. Microbiol. 2007, 73:7218-7224.
20. Li J., Paredes-Sabja D., Sarker M.R., McClane B.A. Further characterization of Clostridium perfringens small acid soluble protein-4 (Ssp4) properties and expression. PLoS ONE 2009, 4:e6249.
21. Li J., Adams V., Bannam T.L., Miyamoto K., Garcia J.P., Uzal F.A., Rood J.I., McClane B.A. Toxin plasmids of Clostridium perfringens. Microbiol. Mol. Biol. Rev. 2013, 77:208-233.
22. McClane B.A., Lyerly D.M., Wilkins T.D. Enterotoxic clostridia: Clostridium perfringens type A and Clostridium difficile. Gram-positive pathogens 2006, 703-714. ASM, Washington, DC. 2nd ed. V.A. Fischetti (Ed.).
23. Melville S.B., Labbe R., Sonenshein A.L. Expression from the Clostridium perfringens cpe promoter in C. perfringens and Bacillus subtilis. Infect. Immun. 1994, 62:5550-5558.
24. Miyamoto K., Wen Q., McClane B.A. Multiplex PCR genotyping assay that distinguishes between isolates of Clostridium perfringens type A carrying a chromosomal enterotoxin gene (cpe) locus, a plasmid cpe locus with an IS1470-like sequence, or a plasmid cpe locus with an IS1151 sequence. J. Clin. Microbiol. 2004, 42:1552-1558.
25. Myers G.S., Rasko D.A., Cheung J.K., Ravel J., Seshadri R., DeBoy R.T., Ren Q., Varga J., Awad M.M., Brinkac L.M., Daugherty S.C., Haft D.H., Dodson R.J., Madupu R., Nelson W.C., Rosovitz M.J., Sullivan S.A., Khouri H., Dimitrov G.I., Watkins K.L., Mulligan S., Benton J., Radune D., Fisher D.J., Atkins H.S., Hiscox T., Jost B.H., Billington S.J., Songer J.G., McClane B.A., Titball R.W., Rood J.I., Melville S.B., Paulsen I.T. Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res. 2006, 16:1031-1040.
26. Raju D., Sarker M.R. Comparison of the levels of heat resistance of wild-type, cpe knockout, and cpe plasmid-cured Clostridium perfringens type A strains. Appl. Environ. Microbiol. 2005, 71:7618-7620.
27. Sarker M.R., Shivers R.P., Sparks S.G., Juneja V.K., McClane B.A. Comparative experiments to examine the effects of heating on vegetative cells and spores of Clostridium perfringens isolates carrying plasmid genes versus chromosomal enterotoxin genes. Appl. Environ. Microbiol. 2000, 66:3234-3240.
28. Tanaka D., Isobe J., Hosorogi S., Kimata K., Shimizu M., Katori K., Gyobu Y., Nagai Y., Yamagishi T., Karasawa T., Nakamura S. An outbreak of food-borne gastroenteritis caused by Clostridium perfringens carrying the cpe gene on a plasmid. Jpn. J. Infect. Dis. 2003, 56:137-139.
29. USDA Appendix B Compliance Guidelines for Cooling Heat-Treated Meat and Poultry Products (Stabilization) 1999, Service, F.S.I, Washington, D.C., (Available at http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/95-033F/95-033F_Appendix_B.htm. Accessed April 22, 2014).
30. USDA Appendix B Compliance guidelines for cooling heat-treated meat and poultry products (stabilization) 1999, Food Safety Inspection Service, Washington, D.C., (Available at http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/95-033F/95-033F_Appendix_B.htm. Accessed April 22, 2014).
31. USDA Draft compliance guidelines for ready-to-eat meat and poultry product. Service, F.S.I. Fed. Regist 2001, (Available at Accessed April 22, 2014).
32. USDA Draft compliance guidelines for ready-to-eat meat and poultry product 2001, Food Safety Inspection Service, Washington, D.C., (Available at http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/97-013P/COMPLIANCEGUIDELINESFORRTEMEATANDPOULTRY.doc. Accessed April 22, 2014).
33. Wijnands L.M., van der Mey-Florijn A., Delfgou-van Asch E. Clostridium perfringens associated food borne disease. RIVM report 2011, (330371005).
34. Wijnands L.M., van der Mey-Florijn A., Delfgou-van Asch E. Clostridium perfringens associated food borne disease. RIVM report 2011, (330371005. Available at http://www.rivm.nl/bibliotheek/rapporten/330371005.pdf. Accessed April 22, 2014).
35. Xiao Y., Wagendorp A., Moezelaar R., Abee T., Wells-Bennik M.H.J. 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. 2012, 78:7060-7068.