Abstract
The presence of psychrotrophic enterotoxigenic Bacillus cereus in ready-to-serve meats and meat products that have not been subjected to sterilization treatment is a public health concern. A study was undertaken to determine the survival, growth, and diarrheal enterotoxin production characteristics of four strains of psychrotrophic B. cereus in brain heart infusion (BHI) broth and beef gravy as affected by temperature and supplementation with nisin. A portion of unheated vegetative cells from 24-h BHI broth cultures was sensitive to nisin as evidenced by an inability to form colonies on BHI agar containing 10 micrograms of nisin/ml. Heat-stressed cells exhibited increased sensitivity to nisin. At concentrations as low as 1 microgram/ml, nisin was lethal to B. cereus, the effect being more pronounced in BHI broth than in beef gravy. The inhibitory effect of nisin (1 microgram/ml) was greater on vegetative cells than on spores inoculated into beef gravy and was more pronounced at 8 degrees C than at 15 degrees C. Nisin, at a concentration of 5 or 50 micrograms/ml, inhibited growth in gravy inoculated with vegetative cells and stored at 8 or 15 degrees C, respectively, for 14 days. Growth of vegetative cells and spores of B. cereus after an initial period of inhibition is attributed to loss of activity of nisin. One of two test strains produced diarrheal enterotoxin in gravy stored at 8 or 15 degrees C within 9 or 3 days, respectively. Enterotoxin production was inhibited in gravy supplemented with 1 microgram of nisin/ml and stored at 8 degrees C for 14 days; 5 micrograms of nisin/ml was required for inhibition at 15 degrees C. Enterotoxin was not detected in gravy in which less than 5.85 log10 CFU of B. cereus/ml had grown. Results indicate that as little as 1 microgram of nisin/ml may be effective in inhibiting or retarding growth of and diarrheal enterotoxin production by vegetative cells and spores of psychrotrophic B. cereus in beef gravy at 8 degrees C, a temperature exceeding that recommended for storage or for most unpasteurized, ready-to-serve meat products.
Full Text
The Full Text of this article is available as a PDF (237.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Becker H., Schaller G., von Wiese W., Terplan G. Bacillus cereus in infant foods and dried milk products. Int J Food Microbiol. 1994 Sep;23(1):1–15. doi: 10.1016/0168-1605(94)90218-6. [DOI] [PubMed] [Google Scholar]
- Christiansson A., Naidu A. S., Nilsson I., Wadström T., Pettersson H. E. Toxin production by Bacillus cereus dairy isolates in milk at low temperatures. Appl Environ Microbiol. 1989 Oct;55(10):2595–2600. doi: 10.1128/aem.55.10.2595-2600.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chung K. T., Dickson J. S., Crouse J. D. Effects of nisin on growth of bacteria attached to meat. Appl Environ Microbiol. 1989 Jun;55(6):1329–1333. doi: 10.1128/aem.55.6.1329-1333.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davies E. A., Adams M. R. Resistance of Listeria monocytogenes to the bacteriocin nisin. Int J Food Microbiol. 1994 Mar;21(4):341–347. doi: 10.1016/0168-1605(94)90064-7. [DOI] [PubMed] [Google Scholar]
- Delves-Broughton J., Blackburn P., Evans R. J., Hugenholtz J. Applications of the bacteriocin, nisin. Antonie Van Leeuwenhoek. 1996 Feb;69(2):193–202. doi: 10.1007/BF00399424. [DOI] [PubMed] [Google Scholar]
- Dufrenne J., Soentoro P., Tatini S., Day T., Notermans S. Characteristics of Bacillus cereus related to safe food production. Int J Food Microbiol. 1994 Sep;23(1):99–109. doi: 10.1016/0168-1605(94)90225-9. [DOI] [PubMed] [Google Scholar]
- Grant I. R., Nixon C. R., Patterson M. F. Effect of low-dose irradiation on growth of and toxin production by Staphylococcus aureus and Bacillus cereus in roast beef and gravy. Int J Food Microbiol. 1993 Mar;18(1):25–36. doi: 10.1016/0168-1605(93)90004-z. [DOI] [PubMed] [Google Scholar]
- Granum P. E. Bacillus cereus and its toxins. Soc Appl Bacteriol Symp Ser. 1994;23:61S–66S. [PubMed] [Google Scholar]
- Granum P. E., Brynestad S., Kramer J. M. Analysis of enterotoxin production by Bacillus cereus from dairy products, food poisoning incidents and non-gastrointestinal infections. Int J Food Microbiol. 1993 Feb;17(4):269–279. doi: 10.1016/0168-1605(93)90197-o. [DOI] [PubMed] [Google Scholar]
- Jarvis B., Farr J. Partial purification, specificity and mechanism of action of the nisin-inactivating enzyme from Bacillus cereus. Biochim Biophys Acta. 1971 Feb 10;227(2):232–240. doi: 10.1016/0005-2744(71)90056-8. [DOI] [PubMed] [Google Scholar]
- Jarvis B. Resistance to nisin and production of nisin-inactivating enzymes by several Bacillus species. J Gen Microbiol. 1967 Apr;47(1):33–48. doi: 10.1099/00221287-47-1-33. [DOI] [PubMed] [Google Scholar]
- Kalchayanand N., Sikes T., Dunne C. P., Ray B. Hydrostatic pressure and electroporation have increased bactericidal efficiency in combination with bacteriocins. Appl Environ Microbiol. 1994 Nov;60(11):4174–4177. doi: 10.1128/aem.60.11.4174-4177.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okereke A., Montville T. J. Nisin dissipates the proton motive force of the obligate anaerobe Clostridium sporogenes PA 3679. Appl Environ Microbiol. 1992 Aug;58(8):2463–2467. doi: 10.1128/aem.58.8.2463-2467.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruhr E., Sahl H. G. Mode of action of the peptide antibiotic nisin and influence on the membrane potential of whole cells and on cytoplasmic and artificial membrane vesicles. Antimicrob Agents Chemother. 1985 May;27(5):841–845. doi: 10.1128/aac.27.5.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutherland A. D., Murdoch R. Seasonal occurrence of psychrotrophic Bacillus species in raw milk, and studies on the interactions with mesophilic Bacillus sp. Int J Food Microbiol. 1994 Mar;21(4):279–292. doi: 10.1016/0168-1605(94)90058-2. [DOI] [PubMed] [Google Scholar]
- Thomas L. V., Wimpenny J. W., Davis J. G. Effect of three preservatives on the growth of Bacillus cereus, Vero cytotoxigenic Escherichia coli and Staphylococcus aureus, on plates with gradients of pH and sodium chloride concentration. Int J Food Microbiol. 1993 Feb;17(4):289–301. doi: 10.1016/0168-1605(93)90199-q. [DOI] [PubMed] [Google Scholar]
- van Netten P., van De Moosdijk A., van Hoensel P., Mossel D. A., Perales I. Psychrotrophic strains of Bacillus cereus producing enterotoxin. J Appl Bacteriol. 1990 Jul;69(1):73–79. doi: 10.1111/j.1365-2672.1990.tb02913.x. [DOI] [PubMed] [Google Scholar]