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

Volumn 144, Issue 3, 2011, Pages 546-555

  De Oliveira, Thales Leandro Coutinho ^a   de Araújo Soares, Rodrigo ^a   Ramos, Eduardo Mendes ^a   das Graças Cardoso, Maria ^a   Alves, Eduardo ^a   Piccoli, Roberta Hilsdorf ^a  

^a FEDERAL UNIVERSITY OF LAVRAS   (Brazil)

Author keywords

Beef batter; Clostridium perfringens; Food safety; Spores; Transmission electron microscopy; Winter savory

Indexed keywords

1 OCTEN 3 OL; ALPHA THUJENE; BORNEOL; CAMPHOR; CARVACROL; CARYOPHYLLENE; CARYOPHYLLENE OXIDE; CINEOLE; ESSENTIAL OIL; LIMONENE; LINALOOL; MYRCENE; PARA CYMENE; PINENE; SABINENE; SODIUM NITRITE; SPATHULENOL; TERPINENE; TERPINEOL; THYMOL;

AGAR DIFFUSION; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; CLOSTRIDIUM PERFRINGENS TYPE A; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOLYSIS; DISTILLATION; INOCULATION; MASS FRAGMENTOGRAPHY; MEAT; MEDICINAL PLANT; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; SATUREJA MONTANA; SAVORY; TARGET ORGANISM; TRANSMISSION ELECTRON MICROSCOPY;

ANTI-INFECTIVE AGENTS; CLOSTRIDIUM PERFRINGENS; FOOD MICROBIOLOGY; FOOD PRESERVATION; MEAT PRODUCTS; MICROBIAL SENSITIVITY TESTS; OILS, VOLATILE; SATUREJA; SODIUM NITRITE;

CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM PERFRINGENS A; SATUREJA MONTANA;

EID: 78650017198     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2010.11.022     Document Type: Article

References (71)

1. Adams R.P. Identification of Essential Oils Components by Gas Chromatography/Mass Spectrometry 2007, Allured Publishing Corporation, Carol Stream, 804 pp. 4 ed.
2. Bakkali F., Averbeck S., Averbeck D., Idaomar M. Biological effects of essential oils - a review. Food and Chemical Toxicology 2008, 46:446-475.
3. Bezbradica D.I., Tomovic J.M., Vukasinovic M.S., Siler-Marinkovic S. Composition and antimicrobial activity of essential oil of Satureja montana L. collected in Serbia and Montenegro. Journal of Essential Oil Research 2005, 17:462-465.
4. Bozzola J.J., Russell L.D. Electron Microscopy 1998, Jones and Bartlett Publishers, Boston, 670 pp. 2nd ed.
5. Brazil, 2009. Ministry of Agriculture, Livestock and Supply. Department of Agricultural Defense. Use of preservatives/additives in meat products: procedures for the registration and inspection. Available from Acessed Oct 12, 2009. http://www.uba.org.br/.
6. Brynestad S., Granum P.E. Clostridium perfringens and foodborne infections. International Journal of Food Microbiology 2002, 74:195-202.
7. Burt S. Essential oils: their antibacterial properties and potential applications in foods: a review. International Journal of Food Microbiology 2004, 94:223-253.
8. Byrne B., Scannell A.G.M., Lyng J., Bolton D.J. An evaluation of Clostridium perfringens media. Food Control 2008, 19:1091-1095.
9. Cammack R., Joannou C.L., Cui X.Y., Martinez C.T., Maraj S.R.B., Martin N.H. Review - nitrite and nitrosyl compounds in food preservation. Biochimica et Biophysica Acta 1999, 1411:475-488.
10. Carman R.J., Sayeed S., Li J., Genheimer C.W., Hiltonsmith M.F., Wilkins T.D., Mcclane B.A. Clostridium perfringens toxin genotypes in the feces of healthy North Americans. Anaerobe 2008, 14:102-108.
11. Cassens R.G. Residual nitrite in cured meat. Food Technology 1997, 51:53-55.
12. Cava R., Nowak E., Taboada A., Marin-Iniesta F. Antimicrobial activity of clove and cinnamon essential oils against Listeria monocytogenes in pasteurized milk. Journal of Food Protection 2007, 70:2757-2763.
13. Ćavar S., Maksimović M., Šolic M.E., Mujkić A.J., Bešta R. Chemical composition and antioxidant and antimicrobial activity of two Satureja essential oils. Food Chemistry 2008, 111:648-653.
14. Ćetković G.S., Mandić A.I., Čanadanović-Brunet J.M., Djilas S.M., Tumbas V.T. HPLC screening of phenolic compounds in winter savory (Satureja montana L.) extracts. Journal of Liquid Chromatography and Related Technologies 2007, 30:293-306.
15. Cox S.D., Mann C.M., Markham J.L., Bell H.C., Gustafson J.E., Warmington T.R., Wyllie S.G. The mode of antimicrobial action of the essential oil of Melaleuca alternafolia (tea tree oil). Journal of Applied Microbiology 2000, 88:170-175.
16. Cui H., Gabriel A.A., Nakano H. Antimicrobial efficacies of plant extracts and sodium nitrite against Clostridium botulinum. Food Control 2010, 21:1030-1036.
17. Deans S.G., Ritchie G. Antibacterial properties of plant essential oils. International Journal of Food Microbiology 1987, 5:165-180.
18. 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.
19. Feiner G. Meat Products Handbook Practical Science and Technology 2006, CRC, Boca Raton, 627 pp.
20. 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.
21. 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 the essential oil of lemongrass (Cymbopogon citratus (D.C.) Stapf). Quimica Nova 2008, 31:1476-1480.
22. Gutierrez J., Barry-Ryan C., Bourke P. The antimicrobial efficacy of plant essential oil combinations and interactions with food ingredients. International Journal of Food Microbiology 2008, 124:91-97.
23. Gutierrez J., Barry-Ryan C., Bourke P. Antimicrobial activity of plant essential oils using food model media: efficacy, synergistic potential and interactions with food components. Food Microbiology 2009, 26:142-150.
24. Hao Y.Y., Brackett R.E., Doyle M.P. Efficacy of plant extracts in inhibiting Aeromonas hydrophila and Listeria monocytogenes in refrigerated cooked poultry. Food Microbiology 1998, 15:367-378.
25. Hayouni A., Chraief I., Abedrabba M., Bouix M., Leveau J., Mohammed H., Hamdi M. Tunisian Salvia officinalis L. and Schinus molle L. essential oils: their chemical compositions and their preservative effects against Salmonella inoculated in minced beef meat. International Journal of Food Microbiology 2008, 125:242-251.
26. Helander I.M., Alakomi H.-L., Latva-Kala K., Mattila-Sandholm T., Pol I., Smid E.J., Gorris L.G.M., Wright A. Characterization of the action of selected essential oil components on Gram-negative bacteria. Journal of Agricultural and Food Chemistry 1998, 46:3590-3595.
27. Ismaiel A.A., Pierson M.D. Effect of sodium nitrite and origanum oil on growth and toxin production of Clostridium botulinum in TYG broth and ground pork. Journal of Food Protection 1990, 53:958-960.
28. Jafari M., Eman-Djomeh Z. Reducing nitrite content in hot dogs by hurdle technology. Food Control 2007, 18:1488-1493.
29. Johnson S., Gerding D. Enterotoxemic infections. The Clostridia: Molecular Biology and Pathogenesis 1997, 117-140. Academic, London. J. Rood, B.A. Mcclane, J.G. Songer, R.W. Titball (Eds.).
30. Juneja V.K., Novak J.S., Huang L., Eblen B.S. Increased thermotolerance of Clostridium perfringens spores following sublethal heat shock. Food Control 2003, 14:163-168.
31. Juneja V.K., Marks H., Thippareddi H. Predictive model for growth of Clostridium perfringens during cooling of cooked ground chicken. Innovative Food Science & Emerging Technologies 2009, 10:260-266.
32. Juven B.J., Kanner J., Schved F., Weisslowicz H. Factors that interact with the antibacterial action of thyme essential oil and its active constituents. The Journal of Applied Bacteriology 1994, 76:626-631.
33. Karl-Otto H. The use and control of nitrate and nitrite for the processing of meat products. Meat Science 2008, 78:68-76.
34. Labbé R.G. Clostridium perfringens. The Microbiological Safety and Quality of Food 2000, 1110-1135. Aspen, Gaithersburg. B. Lund, T. Baird-Parker, G. Gould (Eds.).
35. Labbé R.G. Clostridium perfringens. Compendium of Methods for the Microbiological Examination of Foods 2001, 325-330. American Public Health, Washington, (chap. 34). 4 ed. F.P. Downes, K. Ito (Eds.).
36. Lambert R.J.W., Skandamis P.N., Coote P., Nychas G.-J.E. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. Journal of Applied Microbiology 2001, 91:453-462.
37. Lemay M., Choquette J., Delaquis P.J., Gariépy C., Rodrigue N., Saucier L. Antimicrobial effect of natural preservatives in a cooked andacidified chicken meat model. International Journal of Food Microbiology 2002, 78:217-226.
38. Marco A., Navarro J.L., Flores M. The influence of nitrite and nitrate on microbial, chemical and sensory parameters of slow dry fermented sausage. Meat Science 2006, 73:660-673.
39. Mastelić J., Jerković I. Gas chromatography-mass spectrometry analysis of free and glycoconjugated aroma compounds of seasonally collected Satureja montana L. Food Chemistry 2003, 80:135-140.
40. Mcclane B.A., Rood J.I. Clostridial toxins involved in human enteric and histotoxic infection. Clostridia: Biotechnology and Medical Applications 2001, 169-220. Wiley-VHC, Weinheim. H. Bahl, P. Dürre (Eds.).
41. Mejlholm O., Dalgaard P. Antimicrobial effect of essential oils on the seafood spoilage micro-organism Photobacterium phosphoreum in liquid media and fish products. Letters in Applied Microbiology 2002, 34:27-31.
42. Mirjana S., Nada B. Chemical composition and antimicrobial variability of Satureja montana L. essential oils produced during ontogenesis. Journal of Essential Oil Research 2004, 16:387-391.
43. Mitchell W.J. General biology and physiology. Clostridia: Biotechnology and Medical Applications 2001, 49-104. Wiley-VHC, Weinheim. H. Bahl, P. Dürre (Eds.).
44. O'leary V., Solberg M. Effect of sodium nitrite inhibition on intracellular thiol groups and on activity of certain glycolytic enzymes in Clostridium perfringens. Applied and Environmental Microbiology 1976, 31:208-212.
45. Ouattara B., Sabato S.F., Lacroix M. Combined effect of antimicrobial coating and gamma irradiation on shelf life extension of pre-cooked shrimp (Penaeus spp.). International Journal of Food Microbiology 2001, 68:1-9.
46. Oussalah M., Caillet S., Saucier L., Lacroix M. Inhibitory effects of selected plant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Salmonella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. Food Control 2007, 18:414-420.
47. Pimentel F.A., Cardoso M.G., Salgado A.P.S.P., Aguiar P.M., Silva V.F., Morais A.R., Nelson D.L. A convenient method for the determination of moisture in aromatic plants. Quimica Nova 2006, 29:373-375.
48. Pol I.E., Mastwijk H.C., Slump R.A., Popa M.E., Smid E.J. Influence of food matrix on inactivation on Bacillus cereus by combinations of nisin, pulsed electric field treatment and carvacrol. Journal of Food Protection 2001, 64:1012-1018.
49. R Development Core Team.R A Language and Environment for Statistical Computing 2004, R Foundation for Statistical Computing, Viena, R - project. org. Accessed: Jan 10, 2010.
50. Radonic A., Milos M. Chemical composition and in vitro evaluation of antioxidant effect of free volatile compounds from Satureja montana L. Free Radical Research 2003, 37:673-679.
51. Randrianarivelo R., Sarter S., Odoux E., Brat P., Lebrun M., Romestand B., Menut C., Andrianoelisoa H.S., Raherimandimby M., Danthu P. Composition and antimicrobial activity of essential oils of Cinnamosma fragrans. Food Chemistry 2009, 114:680-684.
52. Riha J.W.E., Solberg M. Clostridium perfringens inhibition by sodium nitrite as a function of pH, inoculum size and heat. Journal of Food Science 1975, 40:439-442.
53. Rowley C.R., Moran D.T. A simple procedure for mounting wrinkle free section on formvar-coated slot grids. Ultramicrotomy 1975, 1:151-155.
54. Rywotycki R. The effect of selected functional additives and heat treatment on nitrosamine content in pasteurized pork ham. Meat Science 2002, 60:335-339.
55. Scott V.N., Anderson J.E., Wang G. Mesophilic anaerobic sporeformers. Compendium of Methods for the Microbiological Examination of Foods 2001, 325-330. American Public Health Association, Washington, (chap. 34). 4 ed. F.P. Downes, K. Ito (Eds.).
56. Si W., Ni X., Gong J., Yu H., Tsao R., Han Y., Chambers J.R. Antimicrobial activity of essential oils and structurally related synthetic food additives towards Clostridium perfringens. Journal of Applied Microbiology 2009, 106:213-220.
57. Sikkema J., De Bont J.A.M., Poolman B. Interactions of cyclic hydrocarbons with biological membranes. The Journal of Biological Chemistry 1994, 269:8022-8028.
58. Sikkema J., De Bont J.A.M., Poolman B. Mechanisms of membrane toxicity of hydrocarbons. Microbiological Reviews 1995, 59:201-222.
59. Silva F.V.M., Martins A., Salta J., Neng N.R., Nogueira J.M.F., Mira D., Gaspar N., Justino J., Grosso C., Urieta J.S., Palavra A.M.S., Rauter A.P. Phytochemical profile and Anticholinesterase and antimicrobial activities of supercritical versus conventional extracts of Satureja montana. Journal of Agricultural and Food Chemistry 2009, 57:11557-11563.
60. Singh A., Singh R.K., Bhunia A.K., Singh N. Efficacy of plant essential oils as antimicrobial agents against Listeria monocytogenes in hotdogs. Lebensmittel-Wissenschaft und Technologie 2003, 36:787-794.
61. Skandamis P.N., Nychas G.-J.E. Development and evaluation of a model predicting the survival of Escherichia coli O157:H7 NCTC 12900 in homemade eggplant salad at various temperatures, pHs and oregano essential oil concentrations. Applied and Environmental Microbiology 2000, 66(4):1646-1653.
62. 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.
63. Skandamis P., Tsigarida E., Nychas G.-J.E. Ecophysiological attributes of Salmonella typhimurium in liquid culture and within a gelatin gel with or without the addition of oregano essential oil. World Journal of Microbiology & Biotechnology 2000, 16:31-35.
64. Skočibušić M., Bezić N. Chemical composition and antidiarrhoeal activities of winter savory (Satureja montana L.) essential oil. Pharmaceutical Biology 2003, 41:622-626.
65. Slavkovska V., Jancic R., Bojovic S., Milosavljevic S., Djokovic D. Variability of essential oils of Satureja Montana L. and Satureja Kitaibelli Wier. ex Heuff from the central part of the Balkan Peninsula. Phytochemistry: Chemistry, Biochemistry. Molecular Biology 2001, 57:71-76.
66. Smith-Palmer A., Stewart J., Fyfe L. Antimicrobial properties of plant essential oils and essences against five important food-borne pathogens. Letters in Applied Microbiology 1998, 26:118-122.
67. Smith-Palmer A., Stewart J., Fyfe L. The potential application of plant essential oils as natural food preservatives in soft cheese. Food Microbiology 2001, 18:463-470.
68. Tassou C.C., Drosinos E.H., Nychas G.-J.E. Effects of essential oil from mint (Mentha piperita) on Salmonella enteritidis and Listeria monocytogenes in model food systems at 4°C and 10°C. The Journal of Applied Bacteriology 1995, 78:593-600.
69. Tsigarida E., Skandamis P., Nychas G.-J.E. Behaviour of Listeria monocytogenes and autochthonous flora on meat stored under aerobic, vacuum and modified atmosphere packaging conditions with or without the presence of oregano essential oil at 5 jC. Journal of Applied Microbiology 2000, 89:901-909.
70. Ultee 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.
71. Vrinda Menon K., Garg S.R. Inhibitory effect of clove oil on Listeria monocytogenes in meat and cheese. Food Microbiology 2001, 18:647-650.