A Weibull model to describe antimicrobial kinetics of oregano and lemongrass essential oils against Salmonella Enteritidis in ground beef during refrigerated storage

Meat Science

Volumn 93, Issue 3, 2013, Pages 645-651

  De Oliveira, Thales Leandro Coutinho ^a   Soares, Rodrigo de Araújo ^b   Piccoli, Roberta Hilsdorf ^b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b FEDERAL UNIVERSITY OF LAVRAS   (Brazil)

Author keywords

Cymbopogon citratus; Food safety; Foodborne; Origanum vulgare; Salmonella enterica Enteritidis; Weibull model

Indexed keywords

CYMBOPOGON; FOODBORNE; ORIGANUM VULGARE; SALMONELLA ENTERICA; WEIBULL MODELS;

FOOD SAFETY; MEATS; MICROORGANISMS; OILS AND FATS; SALMONELLA;

ESSENTIAL OILS;

BACTERIA (MICROORGANISMS); BOVINAE; CYMBOPOGON CITRATUS; ORIGANUM; ORIGANUM VULGARE; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS;

ANTIINFECTIVE AGENT; ESSENTIAL OIL;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CATTLE; CHEMISTRY; CYMBOPOGON; DRUG EFFECT; EVALUATION; FOOD CONTROL; FOOD STORAGE; FREEZING; MEAT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; ORIGANUM; SALMONELLA ENTERITIDIS;

ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; CYMBOPOGON; FOOD MICROBIOLOGY; FOOD STORAGE; MEAT; MICROBIAL SENSITIVITY TESTS; MODELS, BIOLOGICAL; OILS, VOLATILE; ORIGANUM; REFRIGERATION; SALMONELLA ENTERITIDIS;

EID: 84870807950     PISSN: 03091740     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meatsci.2012.11.004     Document Type: Article

References (56)

1. Albert I., Mafart P. A modified Weibull model for bacterial inactivation. International Journal of Food Microbiology 2005, 100:197-211.
2. Almeida R.C.C., Schneider I.S. Microbiological and chemical aspects of food products made with ground meat, sold at retail in the city of Campinas. Revista Higiene Alimentar 1983, 2:37-41.
3. Bakkali F., Averbeck S., Averbeck D., Idaomar M. Biological effects of essential oils: A review. Food and Chemical Toxicology 2008, 46:446-475.
4. Baty F., Delignette-Muller M.L. Nlstools: Tools for nonlinear regression diagnostics 2011, R-package, (Available at: . Accessed: June 2012).
5. Baydar H., Sagdiç O., Özkan G., Karadogan T. Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control 2004, 15:169-172.
6. Bialka K., Demirci A., Puri V.M. Modeling the inactivation of Escherichia coli O157:H7 and Salmonella enterica on raspberries and strawberries resulting from exposure to ozone or pulsed UV-light. Journal of Food Engineering 2008, 85:444-449.
7. BRAZIL Resolution RDC n° 12 of 02/01/2001. Technical Regulation on Microbiological Standards for Foods 2001, Official Gazette, Brasília.
8. Burt S. Essential oils: Their antibacterial properties and potential applications in foods - A review. International Journal of Food Microbiology 2004, 94:223-253.
9. Carson C.F., Mee B.J., Riley T.V. Mechanism of action of Malaleuca artenifolia (tea tree) oil on Staphylococcus aureus and coliform bacteria. Food Microbiology 2002, 18:1914-1920.
10. CDC (Centers for Disease Control, Prevention) CDC estimates of foodborne illness in the United States Available at:, (Accessed: July, 2011). http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html#annual.
11. Chun H., Kim J., Chung K., Won M., Song K.B. Inactivation kinetics of Listeria monocytogenes, Salmonella enterica serovar Typhimurium, and Campylobacter jejuni in ready-to-eat sliced ham using UV-C irradiation. Meat Science 2009, 83:599-603.
12. Cutter C.N., Hruska L. Antimicrobial effect of herb extracts against Escherichia coli O157:H7, Listeria monocytogenes and Salmonella typhimurium associated with beef. Journal of Food Protection 2000, 63:601-607.
13. Daferera D.J., Ziogas B.N., Polissiou M.G. The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. Michiganensis. Crop Protection 2003, 22:39-44.
14. Deans S.G., Ritchie G. Antibacterial proprieties of plant essential oils. International Journal of Food Microbiology 1987, 5:165-180.
15. Delaquis P.J., Stanich K., Girard B., Mazza G. Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils. International Journal of Food Microbiology 2002, 74:101-109.
16. Dorman H.J.D., Deans S.G. Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. Journal of Applied Microbiology 2000, 88:308-316.
17. Emiroǧlu Z.K., Yemiş G.P., Coşkun B.K., Candoǧan K. Antimicrobial activity of soy edible films incorporated with thyme and oregano essential oils on fresh ground beef patties. Meat Science 2010, 86:283-288.
18. Farag R.S., Daw Z.Y., Hewedi F.M., El-Barotyel G.S.A. Antimicrobial activity of some Egyptian spice oils. Journal of Food Protection 1989, 52:665-667.
19. Ferreira M.G.A.B., Sobrinho A.J.C. Assessment of bacteriological quality of minced beef and pork (pernil) "in natura" and/or chilled in supermarkets, stores and markets in São Luís City, MA. Revista Higiene Alimentar 2003, 17:87-93.
20. Florentino E.R., Leite A.F., Sá S.N., Araújo M.S.O., Martins R.S. Avaliação da qualidade microbiológica da carne moída comercializada em Campina Grande, PB. Revista Higiene Alimentar 1997, 11:38-41.
21. Forsythe S.J. Food safety microbiology 2002, Artmed.
22. González M., Skandamis P.N., Hänninen M. A modified Weibull model for describing the survival of Campylobacter jejuni in minced chicken meat. International Journal of Food Microbiology 2009, 136:52-58.
23. Govaris A., Solomakos N., Pexara A., Chatzopoulou P.S. The antimicrobial effect of oregano essential oil, nisin and their combination against Salmonella Enteritidis in minced sheep meat during refrigerated storage. International Journal of Food Microbiology 2010, 137:175-180.
24. Guimarães L.G.L., Cardoso M.G., Zacaroni L.M., Lima R.K., Pimentel F.A., Morais A.R. Influence of light and temperature on the oxidation of essential oil lemongrass (Cymbopogon citratus (D.C.) Stapf). Química Nova 2008, 31(6):1476-1480.
25. Hayouni E.A., Chraief I., Abedrabba I.C., Bouix M., Leveau J., Mohammed H., et al. Tunisian Salvia officinalis L. and Schinus molle L. essential oils: Their chemical compositions and their preservative effects against Salmonella inoculated in minced meat. International Journal of Food Microbiology 2008, 125:242-251.
26. Humphrey T., Jorgensen F. Pathogens on meat infection in animals - Establishing a relationship using Campylobacter and Salmonella as examples. Meat Science 2006, 74:89-97.
27. Kotzekidou P., Giannakidis P., Boulamatsis A. Antimicrobial activity of some plant extracts and essential oils against foodborne pathogens in vitro and on the fate of inoculated pathogens in chocolate. LWT - Food Science and Technology 2008, 41:119-127.
28. Kulisic T., Radonic A., Katalinic V., Milos M. Use of different methods for testing antioxidative activity of oregano essential oil. Food Chemistry 2004, 85:633-640.
29. Lambert R.J.W., Skandamis P.N., Coote P., Nychas G.J.E. A study of minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology 2001, 91:453-462.
30. Mafart P., Couvert O., Gaillard S., Leguerinel I. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. International Journal of Food Microbiology 2002, 72:107-113.
31. Mastromatteo M., Conte A., Del Nobile M.A. Combined use of modified atmosphere packaging and natural compounds for food preservation. Food Engineering Review 2010, 2:28-38.
32. Milos M., Mastelic J., Lerkivic I. Chemical composition and antioxidant effect of glycosidically bound volatile compounds from oregano (Origanum vulgare L. ssp. hirtum). Food Chemistry 2000, 71:79-83.
33. Motta M.R.A., Belmonte M.A., Panetta J.C. Avaliação microbiológica de amostras de carne moída comercializada em supermercados da região oeste de São Paulo. Revista Higiene Alimentar 2000, 14:59-62.
34. Oliveira M.M.M., Brugnera D.F., Cardoso M.G., Alves E., Piccoli R.H. Disinfectant action of Cymbopogon sp. essential oils in different phases of biofilm formation by Listeria monocytogenes on stainless steel surface. Food Control 2010, 21:549-553.
35. Oliveira M.M.M., Brugnera D.F., Mendonça A.T., Piccoli R.H. Sanitary conditions of machines grind meat handlers' hands and microbiological quality of ground beef. Ciência e Agrotecnologia 2008, 32:1893-1898.
36. Oliveira T.L.C., Soares R.A., Ramos E.M., Cardoso M.G., Alves E., Piccoli R.H. Antimicrobial activity of Satureja montana L. essential oil against Clostridium perfringens type A inoculated in mortadella-type sausages formulated with different levels of sodium nitrite. International Journal of Food Microbiology 2011, 144:546-555.
37. Oussalah M., Caillet S., Saucier L., Lacroix M. Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli 0157:H7, Salmonella typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 2007, 18:414-420.
38. Pandit V.A., Shelef L.A. Sensitivity of Listeria monocytogenes to rosemary (Rosmarinus officinalis L.). Food Microbiology 1994, 11:57-63.
39. Plotto A., Roberts D.D., Roberts R.G. Evaluation of plant essential oils as natural postharvest disease control of tomato (Lycopersicon esculentum). Acta Horticulturae 2003, 628:737-745.
40. R Development Core Team A language and environment for statistical computing 2012, R Foundation for Statistical Computing, Vienna, (2004. Available at: http://www.R-project.org. Accessed: 12 June 2012).
41. Rabsch W., Tschäpe H., Andreas J., Bäumler A.J. Review, non-typhoidal salmonellosis: Emerging problems. Microbes and Infection 2001, 3:237-247.
42. Raybaudi-Massilia R.M., Mosqueda-Melgar J., Martin-Belloso O. Edible alginate-based coating as carrier of antimicrobials to improve shelf-life and safety of fresh-cut melon. International Journal of Food Microbiology 2008, 121:313-327.
43. Saddiq A.A., Khayyat S.A. Chemical and antimicrobial studies of monoterpene: Citral. Pesticide Biochemistry and Physiology 2010, 98:89-93.
44. San Martin M.F., Sepulvelda D.P., Altunaker B., Gongora-Niteto M.M., Sawnson B.G., Barbosa-Canovas B.G. Evaluation of selected mathematical models to predict the inactivation of Listeria innocua by pulsed electric fields. Lebensmittel-Wissenschaft und Technologie 2007, 40:1271-1279.
45. Santurio J.M., Santurio D.F., Pozzatti P., Moraes C., Franchin P.R., Alves S.H. Antimicrobial activity of essential oils of oregano, thyme and cinnamon against Salmonella enterica serovars of poultry products. Ciência Rural 2007, 37:803-808.
46. Serrano M., Martinez-Romero D., Castillo S., Guillen F., Valero D. The use of natural antifungal compounds improves the beneficial effect of MAP in sweet cherry storage. Innovative Food Science and Emerging Technologies 2005, 6:115-123.
47. Shelef L.A., Jyothi E.K., Bulgarelli M.A. Growth of enteropathogenic and spoilage bacteria in sage-containing broth and foods. Journal of Food Science 1984, 49:737-740.
48. Sikkema J., Bont J.A.M., Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews 1995, 59:201-222.
49. Silva J.P.L., Duarte-Almeida J.M., Perez D.V., Franco B.D.G.M. Óleo essencial de orégano: interferência da composição química na atividade frente a Salmonella Enteritidis. Ciência e Tecnologia de Alimentos 2010, 30:136-141.
50. Silva N., Junqueira V.C.A., Silveira N.F.A., Taniwaki M.H., Santos R.F.S., Gomes R.A.R. Manual of methods for microbiological analysis of food 2007.
51. Singh A., Singh R.K., Bhunia A.K., Singh N. Efficacy of plant essential oils as antimicrobial agents against Listeria monocytogenes in hotdogs. LWT - Food Science and Technology 2003, 36:787-794.
52. Skandamis P.N., Nychas G.-J.E. Effect of oregano essential oil on microbiological and physico-chemical attributes of minced meat stored in air and modified atmospheres. Journal of Applied Microbiology 2001, 91:1011-1022.
53. Skandamis P.N., Tsigarida E., Nychas G.-J.E. The effect of oregano essential oil on survival/death of Salmonella typhimurium in meat stored at 5°C under aerobic, VP/MAP conditions. Food Microbiology 2002, 19:97-103.
54. Souza E.L., Stamford T.L.M., Lima E.O. Sensitivity of spoiling and pathogen food-related bacteria to Origanum vulgare L. (Lamiaceae) essential oil. Brazilian Journal of Microbiology 2006, 37:527-532.
55. Tajkarimi M.M., Ibrahim S.A., Cliver D.O. Antimicrobial herb and spice compounds in food. Food Control 2010, 21:1199-1218.
56. Utlee A., Bennink M.H.J., Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology 2002, 68:1561-1568.