Characterization by culture-dependent and culture-independent methods of the bacterial population of suckling-lamb packaged in different atmospheres

Food Microbiology

Volumn 36, Issue 2, 2013, Pages 216-222

  Osés, Sandra M ^a   Diez, Ana M ^a   Melero, Beatriz ^a   Luning, Pieternel A ^b   Jaime, Isabel ^a   Rovira, Jordi ^a  

^a UNIVERSITY OF BURGOS   (Spain)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

MAP; PCR DGGE; QPCR; Shelf life; Suckling lamb

Indexed keywords

ANIMAL; ARTICLE; ATMOSPHERE; BACTERIAL COUNT; BACTERIUM; COMPARATIVE STUDY; FOOD PACKAGING; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MAP; MEAT; METHODOLOGY; MICROBIOLOGY; PCR-DGGE; POLYMERASE CHAIN REACTION; QPCR; SHEEP; SHELF-LIFE; SUCKLING LAMB;

MAP; PCR-DGGE; QPCR; SHELF-LIFE; SUCKLING LAMB;

ANIMALS; ATMOSPHERE; BACTERIA; COLONY COUNT, MICROBIAL; FOOD PACKAGING; MEAT; POLYMERASE CHAIN REACTION; SHEEP;

EID: 84880299606     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2013.05.005     Document Type: Article

References (59)

1. Al-Sheddy I.A., Fung D.Y.C., Kastner C.L. Microbiology of fresh and restructured lamb meat: a review. Critical Reviews in Microbiology 1995, 21:31-52.
2. Ampe F., Ben Omar N., Moizan C., Wacher C., Guyot J.P. 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. Applied and Environmental Microbiology 1999, 65:5464-5473.
3. Aslam Z., Lim J.J., Im W.T., Yasir M., Chung Y.R., Lee S.T. Salinicoccus jeotgali sp. nov., isolated from jeotgal, a traditional Korean fermented seafood. International Journal of Systematic and Evolutionary Microbiology 2007, 57(3):633-638.
4. Balamatsia C.C., Patsias A., Kontominas M.G., Savvaidis I.N. Possible role of volatile amines as quality-indicating metabolites in modified atmosphere-packaged chicken fillets: correlation with microbiological and sensory attributes. Food Chemistry 2007, 104:1622-1628.
5. Barrera O., Rodríguez-Calleja J.M., Santos J.A., Otero A., García-López M.L. Effect of different storage conditions on E.coli O157:H7 and the indigenous bacterial microflora on lamb meat. International Journal of Food Microbiology 2007, 115:244-251.
6. Berruga M.I., Vergara H., Gallego L. Influence of packaging conditions on microbial and lipid oxidation in lamb meat. Small Ruminant Research 2005, 57:257-264.
7. Blanco M., Blanco J.E., Mora A., Rey J., Alonso J.M., Hermoso M., Alonso M.P., Dahbi G., González E.A., Bernárdez M.I., Blanco J. Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain. Journal of Clinical Microbiology 2003, 41:1351-1356.
8. Chen Y.G., Zhang Y.Q., Shi J.X., Xiao H.D., Tang S.K., Liu Z.X., Huang K., Cui X.L., Li W.J. Jeotgalicoccus marinus sp. nov., a marine bacterium isolated from a sea urchin. International Journal of Systematic and Evolutionary Microbiology 2009, 59(7):1625-1629.
9. Cocolin L., Diez A., Urso R., Rantsiou K., Comi G., Bergmaier I., Beimfohr C. Optimization of conditions for profiling bacterial populations in food by culture-independent methods. International Journal of Food Microbiology 2007, 120:100-109.
10. Corbiere Morot-Bizot S., Leroy S., Talon R. Monitoring of staphylococcal starters in two French processing plants manufacturing dry fermented sausages. Journal of Applied Microbiology 2007, 102:238-244.
11. Dainty R.H., Mackey B.M. The relationship between the phenotypic properties of bacteria from chill-stored meat and spoilage processes. Journal of Applied Bacteriology 1992, 21:103S-114S.
12. Diez A.M., Urso R., Rantsiou K., Jaime I., Rovira J., Cocolin L. Spoilage of blood sausages morcilla de Burgos treated with high hydrostatic pressure. International Journal of Food Microbiology 2008, 123:246-253.
13. Doulgeraki A.,I., Ercolini D., Vallani F., Nychas G.J.E. Spoilage microbiota associated to the storage of raw meat in different conditions. International Journal of Food Microbiology 2012, 157:130-141.
14. Doulgeraki A.I., Nychas G.J.E. Monitoring the succession of the biota grown on a selective medium for pseudomonads during storage of minced beef with molecular-based methods. Food Microbiology 2013, 34:62-69.
15. Drosinos E.H., Board R.G. Microbial and physicochemical attributes of minced lamb: sources of contamination with pseudomonas. Food Microbiology 1995, 12:189-197.
16. EFSA The community summary report on food-borne outbreaks in the European Union in 2007. The EFSA Journal 2009, 271.
17. Ege M.J., Mayer M., Schwaiger K., Mattes J., Pershagen G., Van Hage M., Scheynius A., Bauer J., Von Mutius E. Environmental bacteria and childhood asthma. Allergy: European Journal of Allergy and Clinical Immunology 2012, 67(12):1565-1571.
18. Ercolini D., Russo F., Torrieri E., Masi P., Villani F. Changes in the spoilage-related microbiota of beef during refrigerated storage under different packaging conditions. Applied and Environmental Microbiology 2006, 72:4663-4671.
19. Eurostat (accessed 12.07.12). http://appsso.eurostat.ec.europa.eu/nui/submitViewTableAction.do.
20. Fontana C., Cocconcelli P.S., Vignolo G. Direct molecular approach to monitoring bacterial colonization on vacuum-packaged beef. Applied and Environmental Microbiology 2006, 72:5618-5622.
21. García-López M.L., Prieto M., Otero A. The physiological attributes of Gram-negative bacteria associated with spoilage of meat and meat products. The Microbiology of Meat and Poultry 1998, 1-34. Blackie Academic and Professional, London. A. Davies, R. Board (Eds.).
22. Jasson V., Jacxsens L., Luning P., Rajkovic A., Uyttendaele M. Alternative microbial methods: an overview and selection criteria. Food Microbiology 2010, 27:710-730.
23. Jiang Y., Gao F., Xu X., Ye K., Zhou G. Changes in the composition of the bacterial flora on tray-packaged pork during chilled storage analyzed by PCR-DGGE and Real-Time PCR. Journal of Food Science 2011, 76(1):M27-M33.
24. Kalchayanand N., Arthur T.M., Bosilevac J.M., Brichta-Harhay D.M., Guerini M.N., Shackelford S.D., Wheeler T.L., Koohmaraie M. Microbiological characterization of lamb carcasses at commercial processing plants in the United States. Journal of Food Protection 2007, 70:1811-1819.
25. Kennedy C., Buckley D.J., Kerry J.P. Display life of sheep meats retail packaged under atmospheres of various volumes and compositions. Meat Science 2004, 68:649-658.
26. Labadie J. Consequences of packaging on bacterial growth. Meat is an ecological niche. Meat Science 1999, 52:299-305.
27. Lambert A.D., Smith J.P., Dodds K.L. Shelf life extension and microbiological safety of fresh meat - a review. Food Microbiology 1991, 8:267-297.
28. Laursen B.G., Bay L., Cleenwerck I., Vancanneyt M., Swings J., Dalgaard P., Leisner J.J. Carnobacterium divergens and Carnobacterium maltaromaticum as spoilers or protective cultures in meat and seafood: phenotypic and genotypic characterization. Systematic and Applied Microbiology 2005, 28:151-164.
29. Lenahan M., O'Brien S., Kinsella K., Sweeney T., Sheridan J.J. Prevalence and molecular characterization of Escherichia coli O157:H7 on Irish lamb carcasses, fleece and in faeces samples. Journal of Applied Microbiology 2007, 103:2401-2409.
30. Leng J., Cheng Y.M., Zhang C.Y., Zhu R.J., Yang S.L., Gou X., Deng W.D., Mao H.M. Molecular diversity of bacteria in Yunnan yellow cattle (Bos taurus) from Nujiang region, China. Molecular Biology Reports 2012, 39(2):1181-1192.
31. Leroy S., Lebert I., Chacornac J.P., Chavant P., Bernardi T., Talon R. Genetic diversity and biofilm formation of Staphylococcus equorum isolated from naturally fermented sausages and their manufacturing environment. International Journal of Food Microbiology 2009, 134:46-51.
32. Liu W.Y., Jiang L.L., Guo C.J., Yang S.S. Jeotgalicoccus halophilus sp. nov., isolated from salt lakes. International Journal of Systematic and Evolutionary Microbiology 2011, 61(7):1720-1724.
33. Luciano G., Monahan F.J., Vasta V., Pennisi P., Bella M., Priolo A. Lipid and color stability of meat from lambs fed fresh herbage or concentrate. Meat Science 2009, 82:193-199.
34. MARM El consumo alimentario en España 2011 2011, Ministerio de agricultura, alimentación y medio ambiente, (accessed 12.07.12). http://www.magrama.gob.es/es/alimentacion/temas/consumo-y-comercializacion-y-distribucion-alimentaria/el_consumo_alimentario_en_espa%25C3%2591a_2011_tcm7-197862.pdf.
35. Martin E., Gessner A., Gärtner A., Jäckel U. Molecular characterization of airborne bacteria in emission samples of broiler houses. Gefahrstoffe Reinhaltung der Luft 2012, 72(3):99-103.
36. Miguélez E., Zumalacárregui J.M., Osorio M.T., Beteta O., Mateo J. Carcass characteristics of suckling lamb protected by the PGI "Lechazo de Castilla y León" European quality label: effect of breed, sex and carcass weight. Meat Science 2006, 73:82-89.
37. Miguélez E., Zumalacárregui J.M., Osorio M.T., Figueira A.C., Fonseca B., Mateo J. Quality traits of suckling-lamb meat covered by the protected geographical indication "Lechazo de Castilla y León" European quality label. Small Ruminant Research 2008, 77:65-70.
38. Muyzer G., De Waal E.C., Uitterlinden A.G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 1993, 59:695-700.
39. Nychas G.J.E., Drosinos E.H. Meat and pooultry spoilage. Encyclopedia of Food Microbiology 1999, 1253-1259. Academic Press, San Diego, California. R.K. Robinson, C.A. Batt, P.D. Patel (Eds.).
40. Nychas G.J.E., Skandamis P.N., Tassou C.C., Koutsoumanis K.P. Meat spoilage during distribution. Meat Science 2008, 78:77-89.
41. Osés S.M.., Rantsiou K., Cocolin L., Jaime I., Rovira J. Prevalence and quantification of Shiga-toxin producing Escherichia coli along the lamb food chain by quantitative PCR. International Journal of Food Microbiology 2010, 141:S163-S169.
42. Paauw A., Caspers M.P.M., Leverstein-van Hall M.A., Schuren F.H.J., Montijn R.C., Verhoef J., Fluit A.C. Identification of resistance and virulence factors in an epidemic Enterobacter hormaechei outbreak strain. Microbiology 2009, 155:1478-1488.
43. Pennacchia C., Ercolini D., Villani F. Spoilage-related microbiota associated with chilled beef stored in air or vacuum pack. Food Microbiology 2011, 28:84-93.
44. Pin C., Garcia de Fernando G., Ordoñez J.A. Effect of modified atmosphere composition on the metabolism of glucose by Brochothrix thermosphacta. Applied Environmental Microbiology 2002, 68:4441-4447.
45. Prieto M., Garcia-Lopez M.L., Garcia-Armesto M.R., Otero A., Lopez T.M., Moreno B. Factors affecting spoilage microflora succession on lamb carcasses at refrigeration temperatures. Journal of Applied Bacteriology 1993, 74:521-525.
46. Rantsiou K., Cocolin L. Detection and quantification of shiga-like toxin producing Escherichia coli and determination of their vitality in food. Abstract of the 21st International Committee on Food Microbiology and Hygiene Symposium 1-4 September 2008, 98. Aberdeen, Scotland.
47. Rantsiou K., Urso R., Lacumin L., Cantoni C., Cattaneo P., Comi G., Cocolin L. Culture-dependent and independent methods to investigate the microbial ecology of Italian fermented sausages. Applied and Environmental Microbiology 2005, 71(4):1977-1986.
48. Rey J., Blanco J.E., Blanco M., Mora A., Dahbi G., Alonso J.M., Hermoso M., Hermoso J., Alonso M.P., Usera M.A., González E.A., Bernárdez M.I., Blanco J. Serotypes, phage types and virulence genes of Shiga-producing Escherichia coli isolated from sheep in Spain. Veterinary Microbiology 2003, 94:47-56.
49. Sañudo C., Alfonso M., San Julián R., Thorkelsson G., Valdimardottir T., Zygoyiannis D., Stamataris C., Piasentier E., Mills C., Berge P., Dransfield E., Nute G.R., Enser M., Fisher A.V. Regional variation in the hedonic evaluation of lamb meat from diverse production systems by consumers in six European countries. Meat Science 2007, 75:610-621.
50. Schwaiger K., Hölzel C., Mayer M., Bauer J. Notes on the almost unknown genus Jeotgalicoccus. Letters in Applied Microbiology 2010, 50(4):441-444.
51. Senter S.D., Arnold J.W., Chew V. APC values and volatile compounds formed in commercially processed, raw chicken parts during storage at 4 and 13°C under simulated temperature abuse conditions. Journal of the Science of Food and Agriculture 2000, 80:1559-1564.
52. Shelfield V.C., Cox D.R., Lerman L.S., Myers R.M. Attachment of a 40-base pair G+C-rich sequence (GC-clamp) to genomic DNA fragments by the polymerase chain reaction results in improved detection of single-base changes. Proceedings of the National Academy of Sciences of the United States of America 1989, 86:297-303.
53. Sheridan J.J., Doherty A.M., Allen P., McDowell D.A., Blair I.S., Harrington D. The effect of vacuum and modified atmosphere packaging on the shelf-life of lamb primals, stored at different temperatures. Meat Science 1997, 45:107-117.
54. Sun X.D., Holley R.A. Antimicrobial and antioxidative strategies to reduce pathogens and extend the shelf life of fresh red meats. Comprehensive Reviews in Food Science and Food Safety 2012, 11:340-354.
55. Vergara H., Gallego L. Effects of gas composition in modified atmosphere packaging on the meat quality of Spanish Manchega lamb. Journal of the Science of Food and Agriculture 2001, 81:1353-1357.
56. Vettorato M.P., De Castro A.F.P., Cergole-Novella M.C., Camargo F.L.L., Irino K., Guth B.E.C. Shiga toxin-producing Escherichia coli and atypical enteropathogenic Escherichia coli strains isolated from healthy sheep of different populations in Sao Paulo, Brazil. Letters in Applied Microbiology 2009, 49:53-59.
57. Wang J., Ma T., Zhao L., Lv J., Li G., Liang F., Liu R. PCR-DGGE method for analysing the bacterial community in a high temperature petroleum reservoir. World Journal of Microbiology and Biotechnology 2008, 24:1981-1987.
58. Wolffs P., Rådström P. Real-Time PCR for the detection of pathogens in meat. Advanced Technologies for Meat Processing 2006, 131-153. CRC Press. Taylor & Francis Group, Boca Ratón, Florida, USA. L.M.L. Nollet, F. Toldrá (Eds.).
59. Yoon J.H., Lee K.C., Weiss N., Kang K.H., Park Y.H. Jeotgalicoccus halotolerans gen. nov., sp. nov. and Jeotgalicoccus psychrophilus sp. nov., isolated from thetraditional Korean fermented seafood jeotgal. International Journal of Systematic and Evolutionary Microbiology 2003, 53:595-602.