Characterisation of non-toxigenic Clostridium spp. strains, to use as surrogates for non-proteolytic Clostridium botulinum in chilled food challenge testing

Journal of Microbiological Methods

Volumn 108, Issue , 2015, Pages 83-91

  Parker, M D ^a   Barrett, P I ^a   Shepherd, J ^a   Price, L J ^a   Bull, S D ^a  

^a UNILEVER RESEARCH   (United Kingdom)

Author keywords

Challenge testing; Chilled foods; Clostridium botulinum; Surrogates

Indexed keywords

WATER;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; CONTROLLED STUDY; FOOD ANALYSIS; FOOD CONTROL; FOOD PROCESSING; FOOD SAFETY; NONHUMAN; PH; STRAIN DIFFERENCE; TEMPERATURE; TURBIDITY; COLD; GROWTH, DEVELOPMENT AND AGING;

CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM;

CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; COLD TEMPERATURE; FOOD MICROBIOLOGY;

EID: 84916899027     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2014.11.011     Document Type: Article

References (68)

1. Alderton G., Chen J.K., Ito K.A. Effect of lysozyme on the recovery of heated Clostridium botulinum spores. Appl. Microbiol. 1974, 27:613-615.
2. Anniballi F., Fenicia L., Franciosa G., Aureli P. Influence of pH and temperature on the growth of and toxin production by neurotoxigenic strains of Clostridium butyricum type E. J. Food Prot. 2002, 65:1267-1270.
3. Anon. Microbiological challenge testing. Compr. Rev. Food Sci. Food Saf. 2003, 2(issue 2 supplement):46-50.
4. Anon. Clostridium botulinum challenge testing of Ready-To-Eat foods. Food Directorate 2010, Health Products and Food Branch, Health Canada.
5. Artin I., Carter A.T., Holst E., Lo¨venklev M., Mason D.R., Peck M.W., Ra˚dstro¨m P. Effects of carbon dioxide on neurotoxin gene expression in nonproteolytic Clostridium botulinum type E. Appl. Environ. Microbiol. 2008, 74:2391-2397.
6. Barker G.C., Malakar P.K., Del Torre M., Stecchini M.L., Peck M.W. Probabilistic representation of the exposure of consumers to Clostridium botulinum neurotoxin in a minimally processed potato product. Int. J. Food Microbiol. 2005, 100:345-357.
7. Betts G. Challenge testing protocols for assessing the safety and quality of food and drink. Guideline no 63 2010, Campden BRI.
8. Blackburn C.de W. Microbiological analysis and food safety management: GMP and HACCP systems. Detecting Pathogens In Food 2003, 3-19. Woodhead Publishing Limited, Cambridge. T.A. McMeekin (Ed.).
9. Bradshaw M., Marshall K.M., Heap J.T., Tepp W.H., Minton N.P., Johnson E.A. Construction of a nontoxigenic Clostridium botulinum strain for food challenge studies. Appl. Environ. Microbiol. 2010, 76:387-393.
10. Brncˇic´ M. Eco-friendly food processing: 21st century challenges. NATO Science for Peace and Security Series C: Environmental Security 2012, 122:33-44.
11. Brown J.L., Tran-Dinh N., Chapman B. Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum. J. Food Prot. 2012, 75:779-792.
12. Busta F.F., Suslow T.V., Parish M.E., Beuchat L.R., Farber J.N., Garrett E.H., Harris L.J. The use of indicators and surrogate microorganisms for the evaluation of pathogens in fresh and fresh-cut produce. Compr. Rev. Food Sci. Food Saf. 2003, 2(Supplement):179-185.
13. Campbell K.D., Collins M.D., East A.K. Gene probes for identification of the botulinal neurotoxin gene and specific identification of neurotoxin types B, E, and F. J. Clin. Microbiol. 1993, 31:2255.
14. Campbell K.D., East A.K., Thompson D.E., Collins M.D. Studies on the large subunit ribosomal RNA genes and intergenic spacer regions of non-proteolytic Clostridium botulinum types B, E and F. Res. Microbiol. 1993, 144:171-180.
15. Campden BRI Challenge testing protocols for the assessing the safety and quality of food and drink. Guideline No. 63 Campden BRI Food and drink innovation 2010.
16. Carlin F., Peck M.W. Growth and toxin production by non-proteolytic Clostridium botulinum in cooked pureed vegetables at refrigeration temperatures. Appl. Environ. Microbiol. 1996, 62:3069-3072.
17. Carlin F., Girardin H., Peck M.W., Stringer S.C., Barker G.C., Martinez A., Fernandez A., Fernandez P., Waites W.M., Movahedi S., van Leusden F., Nauta M., Moezelaar R., Del Torre M., Litman S. Research on factors allowing a risk assessment of spore-forming pathogenic bacteria in cooked chilled foods containing vegetables: a FAIR collaborative project. Int. J. Food Microbiol. 2000, 60:117-135.
18. Carlin F., Broussolle V., Perelle S., Litman S., Fach P. Prevalence of Clostridium botulinum in food raw materials used in REPFEDs manufactured in France. Int. J. Food Microbiol. 2004, 91:141-145.
19. Daelman J., Jacxsens L., Devlieghere F., Uyttendaele M. Microbial safety and quality of various types of cooked chilled foods. Food Control 2013, 30:510-517.
20. Del Torre M., Stecchini M.L., Braconnier A., Peck M.W. Prevalence of Clostridium species and behaviour of Clostridium botulinum in gnocchi, a REPFED of Italian origin. Int. J. Food Microbiol. 2004, 96:115-131.
21. Dong Q., Tu K., Guo L., Li H., Zhao Y. Response surface model for prediction of growth parameters from spores of Clostridium sporogenes under different experimental conditions. Food Microbiol. 2007, 24:624-632.
22. Eklund M.W., Poysky F.T., Peterson M.E., Paranjpye R.N., Pelroy G.A. Competitive inhibition between different Clostridium botulinum types and strains. J. Food Prot. 2004, 67:2682-2687.
23. Everis L., Betts G. Evaluation of Listeria challenge testing protocols: a practical study using cooked sliced ham. Food Control 2013, 29:61-65.
24. 2 concentrations as influenced by chill temperature, pH and NaCl. Food Microbiol. 2001, 18:453-461.
25. Geeraerd A.H., Valdramidis V.P., Van Impe J.F. GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int. J. Food Microbiol. 2005, 102:95-105.
26. Gibbs P. Characteristics of spore-forming bacteria. Foodborne Pathogens 2002, 417-435. Woodhead Publishing Limited, Cambridge. C.D.W. Blackburn, P.J. McClure (Eds.).
27. Girardin H., Morris C.E., Albagnac C., Dreux N., Glaux C., Nguyen-The C. Behaviour of the pathogen surrogates Listeria innocua and Clostridium sporogenes during production of parsley in fields fertilized with contaminated amendments. FEMS Microbiol. Ecol. 2005, 54:287-295.
28. Gould G.W. Sous vide foods: conclusions of an ECFF botulinum working party. Food Control 1999, 10:47-51.
29. Hatheway C.L. Clostridium botulinum and other Clostridia that produce botulinum neurotoxin. Clostridium botulinum Ecology and Control in Foods 1992, 3-20. Marcel Dekker Inc., New York. A.H.W. Hauschild, K.L. Dodds (Eds.).
30. Hyytia¨-Trees E., Hielm S., Mokkila M., Kinnunen A., Korkeala H. Predicted and observed growth and toxigenesis by Clostridium botulinum type E in vacuum-packaged fishery product challenge tests. Int. J. Food Microbiol. 1999, 47:161-169.
31. Hyytia¨-Trees E., Skytta¨ E., Mokkila M., Kinnunen A., Lindstro¨m M., La¨hteenma¨ki L., Ahvenainen R., Korkeala H. Safety evaluation of sous vide processed products with respect to non-proteolytic Clostridium botulinum by use of challenge studies and predictive microbiological models. Appl. Environ. Microbiol. 2000, 66:223-229.
32. Johnston M.D., Lawson S., Otter J.A. Evaluation of hydrogen peroxide vapour as a method for the decontamination of surfaces contaminated with Clostridium botulinum spores. J. Microbiol. Methods 2005, 60:403-411.
33. Juneja V.K. Delayed Clostridium perfringens growth from a spore inocula by sodium lactate in sous-vide chicken products. Food Microbiol. 2006, 23:105-111.
34. Kim J.-M., Linton R.H. Identification of a non-pathogenic surrogate organism for chlorine dioxide gas treatment. Food Microbiol. 2008, 25:597-606.
35. Kizerwetter-S´wida M., Binek M. Clostridium botulinum toxicosis - still a serious problem. Postepy Microbiol. 2010, 49:75-85.
36. Licciardello J.J. Botulism and heat-processed seafoods. Marine Fisheries Review, National Oceanic and Atmospheric Administration 1983, 45:1-7.
37. Lindstro¨m M., Mokkila M., Skytta¨ E., Hyytia¨-Trees E., La¨hteenma¨ki L., Hielm S., Ahvenainen R., Korkeala H. Inhibition of growth of non-proteolytic Clostridium botulinum Type B in sous vide cooked meat products is achieved by using thermal processing but not nisin. J. Food Prot. 2001, 64(6):838-844.
38. Lindstro¨m M., Kiviniemi K., Korkeala H. Hazard and control of group II (non-proteolytic) Clostridium botulinum in modern food processing. Int. J. Food Microbiol. 2006, 108:92-104.
39. Lynt R.K., Kautter D.A., Solomon H.M. Heat-resistance of non-proteolytic Clostridium botulinum type-F in phosphate buffer and crabmeat. J. Food Sci. 1979, 44:108-111.
40. Lynt R.K., Kautter D.A., Solomon H.M. Effect of delayed germination by heat damaged spores on the estimates of heat-resistance of Clostridium botulinum type E and Type F. J. Food Sci. 1983, 48:226-229.
41. Mafart P., Couvert O., Gaillard S., Leguerinel I. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 2002, 72:107-113.
42. Miconnet N., Geeraerd A.H., Van Impe J.F., Rosso L., Cornu M. Reflections on the use of robust and least-squares non-linear regression to model challenge tests conducted in/on food products. Int. J. Food Microbiol. 2005, 104:161-177.
43. NACMCF Recommendations for Refrigerated Foods Containing Cooked, Uncured Meat or Poultry Products that are Packaged for Extended Refrigerated Shelf-Life and that are Ready-to-Eat or Prepared with Little or No Additional Heat Treatment 1990, National Advisory Committee on Microbiological Criteria for Foods, (http://www.fsis.usda.gov/OPHS/nacmcf/past/rec_rte1990.pdf).
44. NACMCF Vacuum or Modified Atmosphere Packaging for Refrigerated Raw Fishery Products 1992, National Advisory Committee on Microbiological Criteria for Foods, (http://www.fsis.usda.gov/OPHS/nacmcf/past/map_fishery.htm).
45. NACMCF Parameters for determining inoculated pack/challenge study protocols. J. Food Prot. 2010, 73:140-202.
46. Nguyen-The C. Biological hazards in processed fruits and vegetables - risk factors and impact of processing techniques. LWT Food Sci. Technol. 2012, 49:172-177.
47. Notermans S., In't Veld P. Microbiological challenge testing for ensuring safety of food products. Int. J. Food Microbiol. 1994, 24:33-39.
48. Ohye D.F., Scott W.J. Studies in the physiology of Clostridium botulinum type E. Aust. J. Biol. Sci. 1957, 10:85-94.
49. Peck M.W. Clostridium botulinum and the safety of refrigerated processed foods of extended durability. Trends Food Sci. Technol. 1997, 8:186-192.
50. Peck M.W. Clostridium botulinum and the safety of minimally heated, chilled foods: an emerging issue?. J. Appl. Microbiol. 2006, 101:556-570.
51. Peck M.W., Stringer S.C. The safety of pasteurised in-pack chilled meat products with respect to the foodborne botulism hazard. Meat Sci. 2005, 70:461-475.
52. Peck M.W., Goodburn K.E., Betts R.P., Stringer S.C. Assessment of the potential for growth and neurotoxin formation by non-proteolytic Clostridium botulinum in short shelf-life commercial foods designed to be stored chilled. Trends Food Sci. Technol. 2008, 19:207-216.
53. Pflug Microbiology and Engineering of Sterilisation Processes 2008, Environmental Sterilisation Laboratory, Otterbein.
54. Plowman J., Peck M.W. Use of a novel method to characterise the response of spores of non-proteolytic Clostridium botulinum types B, E and F to a wide range of germinants and conditions. J. Appl. Microbiol. 2002, 92:681-694.
55. Polese P., Del Torre M., Venir E., Stecchini M.L. A simplified modelling approach established to determine the Listeria monocytogenes behavior during processing and storage of a traditional (Italian) ready-to-eat food in accordance with the European Commission Regulation No 2073/2075. Food Control 2014, 36:166-173.
56. Potter M.D., Meng J.And, Kimsey P. An ELISA for detection of botulinal toxin types A, B and E in inoculated food samples. J. Food Prot. 1993, 56:856-861.
57. Rodgers S. Potential applications of protective cultures in cook-chill catering. Food Control 2003, 14:35-42.
58. Sakaguchi G., Tohyama Y., Saito S., Fujisawa S., Wada S. An outbreak of type E botulism in Akita prefecture due to gilthead-izushi. Jpn. J. Med. Sci. Biol. 1954, 7:539-546.
59. Schmidt C.F. Spores of C. botulinum: formation, resistance, germination. Botulism. Proceedings of a symposium 1964, US Department of Health Education and Welfare.
60. Scott V.N., Bernard D.T. Heat resistance of spores of non-proteolytic type B Clostridium botulinum. J. Food Prot. 1982, 45:909-912.
61. Scott V.N., Swanson K.M.J., Freier T.A., Payton Pruett W., Sveum W.H., Hall P.A., Smoot L.A., Brown D.G. Guidelines for conducting Listeria monocytogenes challenge testing of foods. Food Protect. Trends 2005, 25:818-825.
62. Shakila R.J., Raj B.E., Felix N. Quality and safety of fish curry processed by sous vide cook chilled and hot filled technology process during refrigerated storage. Food Sci. Technol. Int. 2012, 18:261-269.
63. Stringer S.C., Haque N., Peck M.W. Growth from spores of non-proteolytic Clostridium botulinum in heat-treated vegetable juice. Appl. Environ. Microbiol. 1999, 65:2136-2142.
64. Stringer S.C., Carter A.T., Webb M.D., Wachnicka E., Crossman L.C., Sebaihia M., Peck M.W. Genomic and physiological variability within group II (non-proteolytic) Clostridium botulinum. BMC Genomics 2013, 14. (article 333).
65. Us, DHHS - United States Department of Health and Human Services Biosafety in Microbiological and Biomedical Laboratories 1999, U.S. Government Printing Office, Washington, USA. Fourth edition.
66. Uyttendaele M., Rajkovic A., Benos G., Francois K., Devlieghere F., Debevere J. Evaluation of a challenge testing protocol to assess the stability of ready-to-eat cooked meat products against growth of Listeria monocytogenes. Int. J. Food Microbiol. 2004, 90:219-236.
67. Vestergaard E.M. Building product confidence with challenge studies. Dairy Food Environ. Sanit. 2001, 21(3):206-299.
68. Walker S.J., Betts G. Chilled foods microbiology. Chilled Foods 2000, 153-186. Woodhead Publishing Limited, Cambridge. second edition. M. Stringer, C. Dennis (Eds.).