Changes in the spoilage-related microbiota of beef during refrigerated storage under different packaging conditions

Applied and Environmental Microbiology

Volumn 72, Issue 7, 2006, Pages 4663-4671

  Ercolini, Danilo ^a   Russo, Federica ^a   Torrieri, Elena ^a   Masi, Paolo ^a   Villani, Francesco ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; ELECTROPHORESIS; ENZYME KINETICS; FOOD PRESERVATION; MEATS; MICROBIOLOGY; ORGANIC ACIDS; REFRIGERATION;

DENATURING GRADIENT GEL ELECTROPHORESIS (DGGE) ANALYSIS; GAS COMPOSITION; MICROBIAL COLONIES; WEIGHT LOSS;

BACTERIA;

BACTERIUM; FOOD STORAGE; MEAT;

ANIMAL TISSUE; ARTICLE; BACTERIAL FLORA; CATTLE; CELL VIABILITY; DENATURING GRADIENT GEL ELECTROPHORESIS; FOOD PACKAGING; FOOD STORAGE; FREEZING; LACTIC ACID BACTERIUM; MICROBIAL COLONIZATION; MONITORING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SAMPLING; SEQUENCE ANALYSIS; WATER CONTENT;

ANIMALS; BACTERIA; CARBON DIOXIDE; CATTLE; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; DNA, RIBOSOMAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FOOD MICROBIOLOGY; FOOD PACKAGING; MEAT; MOLECULAR SEQUENCE DATA; OXYGEN; POLYMERASE CHAIN REACTION; REFRIGERATION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

BROCHOTHRIX THERMOSPHACTA; CARNOBACTERIUM DIVERGENS; ENTEROBACTERIACEAE; LACTOBACILLUS SAKEI; PSEUDOMONAS; RAHNELLA; RAHNELLA AQUATILIS;

EID: 33746101830     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00468-06     Document Type: Article

References (56)

1. Ampe, F., N. ben Omar, C. Moizan, C. Wacher, and J.-P. Guyot. 1999. Polyphasic study of the spatial distribution of microorganisms in Mexican pozol, a fermented maize dough, demonstrates the need for cultivation-independent methods to investigate traditional fermentations. Appl. Environ. Microbiol. 65:5464-5473.
2. Bartkowski, L., F. D. Dryden, and J. A. Marchello. 1982. Quality changes of beef steaks stored in controlled gas atmosphere containing high or low levels of oxygen. J. Food Prot. 45:41-45.
3. Bellingham, N. F., J. A. W. Morgan, J. R. Saunders, and C. Winstanley. 2001. Flagellin gene sequence variation in the genus Pseudomonas. Syst. Appl. Microbiol. 24:157-165.
4. Bennik, M. H. J., W. Vorstman, E. J. Smid, and L. G. M. Gorris. 1998. The influence of oxygen and carbon dioxide on the growth of prevalent Enterobacteriaceae and Pseudomonas species isolated from fresh and controlled-atmosphere-stored vegetables. Food Microbiol. 15:459-469.
5. Borch, E., M.-L. Kant-Muermans, and Y. Blixt. 1996. Bacterial spoilage of meat and cured meat product. Int. J. Food Microbiol. 33:103-120.
6. Brenner, D. J., H. E. Muller, A. G. Steigerwalt, A. M. Whitney, C. M. O'Hara, and P. Kampfer. 1998. Two new Rahnella genomospecies that cannot be phenotypically differentiated from Rahnella aquatilis. Int. J. Syst. Bacteriol. 48:141-149.
7. Brody, A. L. 1996. Integrating aspect and modified atmosphere packaging to fulfill a vision of tomorrow. Food Technol. 50:56-66.
8. Chung, K.-T., J. S. Dickson, and J. D. Crouse. 1989. Attachment and proliferation of bacteria on meat. J. Food Prot. 52:173-177.
9. Cocolin, L., K. Rantsiou, L. Iacumin, R. D'Urso, C. Cantoni, and G. Comi. 2004. Study of the ecology of fresh sausages and characterization of populations of lactic acid bacteria by molecular methods. Appl. Environ. Microbiol. 70:1883-1894.
10. Costerson, J. W., R. T. Irvin, and K.-J. Cheng. 1981. The bacterial glycocalyx in nature and disease. Annu. Rev. Microbiol. 35:299-324.
11. Dainty, R. H., R. A. Edwards, and C. M. Hibbard. 1985. Time course of volatile compounds formation during refrigerated storage of naturally contaminated beef in air. J. Appl. Bacteriol. 59:303-309.
12. Dainty, R. H., and B. M. Mackey. 1992. The relationship between the phenotypic properties of bacteria from chill-stored meat and spoilage processes. J. Appl. Bacteriol. 73:1035-1145.
13. Ellis, D. I., and R. Goodacre. 2001. Rapid and quantitative detection of the microbial spoilage of muscle foods: current status and future trends. Trends Food Sci. Technol. 12:414-424.
14. Ercolini, D., G. Moschetti, G. Blaiotta, and S. Coppola. 2001. The potential of a polyphasic PCR-DGGE approach in evaluating microbial diversity of natural whey cultures for water-buffalo mozzarella cheese production: bias of "culture dependent" and "culture independent" approaches. Syst. Appl. Microbiol. 24:610-617.
15. Ercolini, D., P. J. Hill, and C. E. R. Dodd. 2003. Bacterial community structure and location in Stilton cheese. Appl. Environ. Microbiol. 69:3540-3548.
16. Ercolini, D., G. Mauriello, G. Blaiotta, G. Moschetti, and S. Coppola. 2004. PCR-DGGE fingerprints of microbial succession during a manufacture of traditional water buffalo mozzarella cheese. J. Appl. Microbiol. 96:263-270.
17. Ercolini, D. 2004. PCR-DGGE fingerprinting: novel strategies for detection of microbes in food. J. Microbiol. Methods 56:297-314.
18. Ercolini, D., A. La Storia, F. Villani, and G. Mauriello. 2006. Effect of a bacteriocin-activated polyethylene film on Listeria monocytogenes as evaluated by viable staining and epifluorescence microscopy. J. Appl. Microbiol. 100:765-772.
19. Faber, J. M. 1991. Microbiological aspect of modified atmosphere packaging technology. J. Food Prot. 54:58-70.
20. Firstenberg-Eden, K. 1981. Attachment of bacteria to meat surfaces: a review. J. Food Prot. 44:602-607.
21. Garcia de Fernando, G. D., G. J. E. Nychas, M. W. Peck, and J. A. Ordonez. 1995. Growth/survival of psychrotrophic pathogens on meat packaged under modified atmospheres. Int. J. Food Microbiol. 28:221-231.
22. Gill, C. O. 1996. Extending the storage life of raw chilled meats. Meat Sci. 43:S99-S109.
23. Gill, C. O. 2003. Active packaging in practice: meat, p. 378-396. In H. Ahvenainem (ed.), Novel food packaging technology. Woodhead Publishing Limited and CRC Press LLC, Boca Raton, Fla.
24. Gram, L., L. Ravn, M. Rasch, J. B. Bruhn, A. B. Christensen, and M. Givskov. 2002. Food spoilage-interactions between food spoilage bacteria. Int. J. Food Microbiol. 78:79-97.
25. Hastings, J. W., M. E Stiles, and A, Vonholy. 1994. Bacteriocins of leuconostocs isolated from meat. Int. J. Food Microbiol. 24:75-81.
26. Hilario, E., T. R. Buckley, and J. M. Young. 2004. Improved resolution of the phylogenetic relationships among Pseudomonas by the combined analysis of atpD, carA, recA and 16S rDNA. Antonie Leeuwenhoek 86:51-64.
27. Huis in't Veld, J. H. J. 1996. Microbial and biochemical spoilage of foods: an overview. Int. J. Food Microbiol. 33:1-18.
28. Jackson, T. C., G. R. Acuff, and J. S. Dickson. 1997. Meat, poultry, and seafood, p. 83-100. In M. P. Doyle and T. J. Beuchat (ed.), Food microbiology: fundamentals and frontiers. ASM Press, Washington, D.C.
29. Jay, J. M. 2000. Food preservation with modified atmospheres, p. 283-295. in D. R. Heldman (ed.), Modern food microbiology. Aspen Publishers, Inc., Gaithersburg, Md.
30. Jay, J. M., J. P. Vilai, and M. E. Hughes. 2003. Profile and activity of the bacterial biota of ground beef held from freshness to spoilage at 5-7°C. Int. J. Food Microbiol. 81:105-111.
31. Jensen, N., P. Varelis, and F. B. Whitfield. 2001. Formation of guaiacol in chocolate milk by psychrotrophic bacterium Rahnella aquatilis. Lett. Appl. Microbiol. 33:339-343.
32. Jeremiah, L. E. 2001. Packaging alternatives to deliver fresh meats using short- or long-term distribution. Food Res. Int. 34:749-772.
33. Kennedy, C., D. J. Buckley, and J. P. Kerry. 2004. Display life of sheep meat retail packaged under atmospheres of various volumes and compositions. Meat Sci. 68:649-658.
34. Koutsoumanis, K., A. Stamatiou, P. Skandamis, and J.-G. Nychas. 2006. Development of microbial model of temperature and pH on spoilage of ground beef, and validation of the model under dynamic temperature conditions. Appl. Environ. Microbiol. 72:124-134.
35. Labadie, J. 1999. Consequences of packaging on bacterial growth. Meat is an ecological niche. Meat Sci. 52:299-305.
36. Lindberg, A. M., A. Ljungh, S. Ahrne, S. Lofdahl, and G. Molin. 1998. Enterobacteriaceae found in high numbers in fish, minced meat and pasteurized milk or cream and the presence of toxin encoding genes. Int. J. Food Microbiol. 39:11-17.
37. Mancini, R. A., and M. C. Hunt. 2005. Current research in meat color. Meat Sci. 71:100-121.
38. Mauriello, G., D. Ercolini, A. La Storia, A. Casaburi, and F. Villani. 2004. Development of polyethylene films for food packaging activated with an antilisterial bacteriocin from Lactobacillus curvatus 32Y. J. Appl. Microbiol. 97:314-322.
39. McMullen, L. M., and M. E. Stiles. 1996. Potential for use of bacteriocin-producing lactic acid bacteria in the preservation of meats. J. Food Prot. 8:64-71.
40. Miambi, E., J.-P. Guyot, and F. Ampe. 2003. Identification, isolation and quantification of representative bacteria from fermented cassava dough using an integrated approach of culture-dependent and culture-independent methods. Int. J. Food Microbiol. 82:111-120.
41. Muyzer, G., E. C. De Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
42. Nattress, F. M., and L. E. Jeremiah. 2000. Bacterial mediated off-flavours in retail-ready beef after storage in controlled atmospheres. Food Res. tnt. 33:743-748.
43. Nychas, G.-J. E., and E. H. Drosinos. 1999. Meat and poultry spoilage, p. 1253-1259. In R. K. Robinson, C. A. Batt, and P. D. Patel (ed.), Encyclopedia of food microbiology. Academic Press, San Diego, Calif.
44. Paludan-Muller, C., P. Dalgaard, H. H. Huss, and L. Gram. 1998. Evaluation of the role of Carnobacterium piscicola in spoilage of vacuum- and modified-atmosphere-packed cold-smoked salmon stored at 5 degrees C. Int. J. Food Microbiol. 39:155-166.
45. Pin, C., G. Garcia de Fernando, and J. A, Ordonez. 2002. Effect of modified atmosphere composition on the metabolism of glucose by Brochothrix thermosphacta. Appl. Environ. Microbiol. 68:4441-4447.
46. Ruling, W. F. M., J. Kerler, M. Braster, A. Apriyantono, H. Stam, and H. W. van Verseveld. 2001. Microorganisms with a taste for vanilla: microbial ecology of traditional Indonesian vanilla curing. Appl. Environ. Microbiol. 67:1995-2003.
47. Sivertsvik, M., J. T. Rosnes, and W. K. Jeksrud. 2004. Solubility and absorption rate of carbon dioxide into non-respiring foods. Part 2. Raw fish fillets. J. Food Eng. 63:451-458.
48. Skandamis, P., and G.-J. E. Nychas. 2005. Fresh meat spoilage and modified atmosphere packaging (MAP), p. 461-493. In J. Sofos (ed.), Improving safety of fresh meat. Woodhead Publishers, Cambridge, United Kingdom.
49. Skandamis, P. N., and G.-J. E. Nychas. 2001. Effect of oregano essential oil on microbiological and physico-chemical attributes of minced meat stored in air and modified atmospheres. J. Appl. Microbiol. 91:1011-1022.
50. Skandamis, P. N., and G.-J. E. Nychas. 2002. Preservation of fresh meat with active and modified atmosphere packaging conditions. Int. J. Food Microbiol. 79:35-45.
51. Stanbridge, L. H., and A. R. Davies. 1998. The microbiology of chill-stored meat, p. 175-177. In A. Davies and R. Board (ed.), Microbiology of meat and poultry. Blackie Academic & Professional, London, United Kingdom.
52. Tash, K. 2005. Rahnella aquatilis bacteremia from a suspected urinary source. J. Clin. Microbiol. 43:2526-2528.
53. Tsai, Y. H., H. D. Kung, T. M. Lee, G. T. Lin, and D. F. Hwang. 2004. Histamine-related hygienic qualities and bacteria found in popular commercial scombroid fish fillets in Taiwan. J. Food Prot. 67:407-412.
54. Yamamoto, S., H. Kasai, D. L. Arnold, R. W. Jackson, A. Viavian, and S. Harayama. 2000. Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 146:2385-2394.
55. Whitfield, F. B., N. Jensen, and K. J. Shaw. 2000. Role of Yersinia intermedia and Pseudomonas putida in the development of a fruity off-flavour in pasteurized milk. J. Dairy Res. 67:561-569.
56. Zoetendal, E. G., A. D. Akkermans, and W. M. de Vos. 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 64:3854-3859.