Abstract

The aim of this study was to evaluate the effect of the use of Rosemary Essential Oil (REO) and Lyophilized Rosemary Extract (LRE) on the oxidative stability of pork sausages stored at -12°C. Potential antioxidants in sausages were determined by thiobarbituric acid reactive substances (TBARS) and expressed in mg of malonaldehyde MDA/kg. Measurements were taken one day each week starting from production day until 49 days after. The TBARS values increased over time, starting with a value of 0.45 and ending with 2.89 mg MDA/kg. The control treatment suffered more intense oxidation than those with Sodium Erythorbate (SE) and natural antioxidants. The lipid oxidation of sausage was significantly inhibited at 49 days of frozen storage in the presence of LRE when compared to the control (47.28%). The sausage containing LRE and REO showed a 75.67% and 56.41% acceptance rate, respectively. The LRE exhibited an excellent inhibitory effect on lipid oxidation of sausage and it has potential to use in meat products.

Keywords:

Antioxidant activity, lipid oxidation, meat products, Rosmarinus officinalis, TBARS,

References

1. Afonso, M.S., A.M.D.O. Silva, E.B. Carvalho, D.P. Rivelli, S.B. Barros, M.M. Rogero, A.M. Lottenberg, R.P. Torres and J. Mancini-Filho, 2013. Phenolic compounds from rosemary (Rosmarinus officinalis L.) attenuate oxidative stress and reduce blood cholesterol concentrations in diet-induced hypercholesterolemic rats. Nutr. Metab., 10(1): 19.
   CrossRef    PMid:23374457 PMCid:PMC3586571    Direct Link
2. Ahn, M.R, S. Kumazawa, T. Hamasaka, K.S. Bang and T. Nakayama, 2004. Antioxidant activity and constituents of propolis collected in various areas of Korea. J. Agr. Food Chem., 52(24): 7286-7292.
   CrossRef    PMid:15563208    Direct Link
3. Almeida, J.F., A.S. dos Reis, L.F.S. Heldt, D. Pereira, M. Bianchin, C. de Moura, M.V. Plata-Oviedo, C.W.I. Haminiuk, I.S. Ribeiro, C.F.P. da Luz and S.T. Carpes, 2017. Lyophilized bee pollen extract: A natural antioxidant source to prevent lipid oxidation in refrigerated sausages. LWT-Food Sci. Technol., 76(Part B): 299-305.
   Direct Link
4. Aouadi, D., G. Luciano, V. Vasta, S. Nasri, D.M.R. Brogna, S. Abidi, A. Priolo and H.B. Salem, 2014. The antioxidant status and oxidative stability of muscle from lambs receiving oral administration of Artemisia herba alba and Rosmarinus officinalis essential oils. Meat Sci., 97(2): 237-243.
   CrossRef    PMid:24583334    Direct Link
5. Brand-Williams, W., M.E. Cuvelier and C. Berset, 1995. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol., 28(1): 25-30.
   CrossRef    
6. Brasil, 2000. Regulamentos tecnicos de identidade e qualidade de carne mecanicamente separada, de mortadela, de linguiça e de salsicha. Ministerio da Agricultura, Pecuaria e Abastecimento, Instruçao Normativa N4, de 31 de Março de 2000. Disponível, Brasília, DF, DOU.
   
7. Carpes, S.T., S.M. de Alencar, I.S.R. Cabral, T.L.C. Oldoni, G.B. Mourão, C.W.I. Haminiuk, C.F.P. da Luz and M.L. Masson, 2013. Polyphenols and palynological origin of bee pollen of Apis mellifera L. from Brazil. Characterization of polyphenols of bee pollen. CyTA - J. Food, 11(2): 150-161.
   CrossRef    Direct Link
8. Casarotti, S.N. and N. Jorge, 2012. Antioxidant activity of rosemary extract in soybean oil under thermoxidation. J. Food Process. Pres., 38(1): 136-145.
   CrossRef    Direct Link
9. Chen, X., Y. Zhang, Y. Zu, L. Yang, Q. Lu and W. Wang, 2014. Efeitos antioxidantes de extratos de alecrim em óleo de girassol em comparação com antioxidantes sintéticos. Int. J. Food Sci. Tech., 49: 385-391.
   CrossRef    
10. Das, A.K., V. Rajkumar, A.K. Verma and D. Swarup, 2012. Moringa oleiferia leaves extract: A natural antioxidant for retarding lipid peroxidation in cooked goat meat patties. Int. J. Food Sci. Tech., 47(3): 585-591.
    CrossRef    Direct Link
11. Dutcosky, S.D., 2007. Analise Sensorial de Alimentos. 2nd Edn., Champagnat, Curitiba, pp: 210.
    
12. Dvorackova, E., M. Snoblova and P. Hrdlicka, 2014. Content of phenolic compounds in herbs used in the Czech Republic. Int. Food Res. J., 21(4): 1495-1500.
    Direct Link
13. Erkan, N., G. Ayranci and E. Ayranci, 2008. Antioxidant activities of rosemary (Rosmarinus Officinalis L.) extract, blackseed (Nigella sativa L.) essential oil, carnosic acid, rosmarinic acid and sesamol. Food Chem., 110(1): 76-82.
    CrossRef    PMid:26050168    Direct Link
14. Falowo, A.B., P.O. Fayemi and V. Muchenje, 2014. Natural antioxidants against lipid–protein oxidative deterioration in meat and meat products: A review. Food Res. Int., 64: 171-181.
    CrossRef    Direct Link
15. Hac-Szymanczuk, E., E. Lipinska and M. Stasiuk, 2011. The effect of rosemary preparations on the microbial quality and tbars value of model pork batters. Acta Sci. Pol. Technol. Aliment., 10(2): 165-174.
    Direct Link
16. Haminiuk, C.W.I., M.S.V. Plata-Oviedo, A.R. Guedes, A.P. Stafussa, E. Bona and S.T. Carpes, 2011. Chemical, antioxidant and antibacterial study of Brazilian fruits. Int. J. Food Sci. Tech., 46(7): 1529-1537.
    CrossRef    Direct Link
17. Han, J. and K.S. Rhee, 2005. Antioxidant properties of selected Oriental non-culinary/nutraceutical herb extracts as evaluated in raw and cooked meat. Meat Sci., 70(1): 25-33.
    CrossRef    PMid:22063277    Direct Link
18. Hernández-Hernández, E., E. Ponce-Alquicira, M.E. Jaramillo-Flores and I. Guerrero Legarreta, 2009. Antioxidant effect rosemary (Rosmarinus officinalis L.) and oregano (Origanum vulgare L.) extracts on TBARS and colour of model raw pork batters. Meat Sci., 81(2): 410-417.
    CrossRef    PMid:22064182    Direct Link
19. Herrero, M., M. Plaza, A. Cifuentes and E. Ibá-ez, 2010. Green processes for the extraction of bioactives from rosemary: Chemical and functional characterization via ultra-performance liquid chromatography-tandem mass spectrometry and in-vitro assays. J. Chromatogr. A, 1217(16): 2512-2520.
    CrossRef    PMid:19945706    Direct Link
20. Hossain, M.B., C. Barry-Ryan, A.B. Martin-Diana and N.P. Brunton, 2011. Optimisation of accelerated solvent extraction of antioxidant compounds from rosemary (Rosmarinus officinalis L.), marjoram (Origanum majorana L.) and oregano (Origanum vulgare L.) using response surface methodology. Food Chem., 126(1): 339-346.
    CrossRef    Direct Link
21. Jongberg, S., M.A. Tørngren, A. Gunvig, L.H. Skibsted and M.N. Lund, 2013. Effect of green tea or rosemary extract on protein oxidation in Bologna type sausages prepared from oxidatively stressed pork. Meat Sci., 93(3): 538-546.
    CrossRef    PMid:23273462    Direct Link
22. Keokamnerd, T., J.C. Acton, I.Y. Han and P.L. Dawson, 2008. Effect of commercial Rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Sci., 87(1): 170-179.
    CrossRef    PMid:18079467    Direct Link
23. Kontogianni, V.G., G. Tomic, I. Nikolic, A.A. Nerantzaki, N. Sayyad, S. Stosic-Grujicic, I. Stojanovic, I.P. Gerothanassis and A.G. Tzakos, 2013. Phytochemical profile of Rosmarinus officinalis and Salvia officinalis extracts and correlation to their antioxidant and anti-proliferative activity. Food Chem., 136(1): 120-129.
    CrossRef    PMid:23017402    Direct Link
24. Lapornik, B., M. Prošek and A.G. Wondra, 2005. Comparison of extracts prepared from plant by-products using different solvents and extraction time. J. Food Eng., 71(2): 214-222.
    CrossRef    Direct Link
25. Lara, M.S., J.I. Gutierrez, M. Timón and A.I. Andrés, 2011. Evaluation of two natural extracts (Rosmarinus officinalis L. and Melissa officinalis L.) as antioxidants in cooked pork patties packed in MAP. Meat Sci., 88(3): 481-488.
    CrossRef    PMid:21345605    Direct Link
26. Lianhe, Z., H. Xing, W. Li and C. Zhengxing, 2012. Physicochemical properties, chemical composition and antioxidant activity of Dalbergia odorifera T. Chen seed oil. J. Am. Oil Chem. Soc., 89(5): 883-890.
    CrossRef    Direct Link
27. Maldini, M., P. Montoro, R. Addis, C. Toniolo, G.L. Petretto, M. Foddai, M. Nicoletti and G. Pintore, 2016. A new approach to discriminate Rosmarinus officinalis L. plants with antioxidant activity, based on HPTLC fingerprint and targeted phenolic analysis combined with PCA. Ind. Crop. Prod., 94: 665-672.
    CrossRef    Direct Link
28. Mariutti, L.R.B. and N. Bragagnolo, 2007. Review: Natural antioxidants from the Lamiaceae family. Application in food products. Braz. J. Food Technol., 10(2): 96-103.
    Direct Link
29. Mishra, K., H. Ojha and N.K. Chaudhury, 2012. Estimation of antiradical properties of antioxidants using DPPH assay: A critical review and results. Food Chem., 130(4): 1036-1043.
    CrossRef    Direct Link
30. Mulinacci, N., M. Innocenti, M. Bellumori, C. Giaccherini, V. Martini and M. Michelozzi, 2011. Storage method, drying processes and extraction procedures strongly affect the phenolic fraction of rosemary leaves: An HPLC/DAD/MS study. Talanta, 85(1): 167-176.
    CrossRef    PMid:21645686    Direct Link
31. Napoli, E.M., G. Curcuruto and G. Ruberto, 2010. Screening of the essential oil composition of wild Sicilian Rosemary. Biochem. Syst. Ecol., 38(4): 659-670.
    CrossRef    Direct Link
32. Naveena, B.M., S. Vaithiyanathan, M. Muthukumar, A.R. Sen, Y.P. Kumar, M. Kiran, V.A. Shaju and K.R. Chandran, 2013. Relationship between the solubility, dosage and antioxidant capacity of carnosic acid in raw and cooked ground buffalo meat patties and chicken patties. Meat Sci., 95(2): 195-202.
    CrossRef    PMid:23743029    Direct Link
33. Okpala, C.O.R., 2016. Lipid autoxidation in ozone-processed crustacea under cold storage: A treatise. Lipid Technol., 28(5-6): 93-95.
    CrossRef    Direct Link
34. Olmedo, R.H., C.M. Asensio and N.R. Grosso, 2015. Thermal stability and antioxidant activity of essential oils from aromatic plants farmed in Argentina. Ind. Crop. Prod., 69: 21-28.
    CrossRef    Direct Link
35. Osawa, C.C., P.E. de Felício and L.A.G. Gonçalves, 2005. TBA test applied to meats and their products: Traditional, modified and alternative methods. Quim. Nova, 28(4): 655-663.
    CrossRef    Direct Link
36. Pateiro, M., J.M. Lorenzo, I.R. Amado and D. Franco, 2014. Effect of addition of green tea, chestnut and grape extract on the shelf-life of pig liver pate. Food Chem., 147: 386-394.
    CrossRef    PMid:24206734    Direct Link
37. Pérez-Fons, L., M.T. Garzón and V. Micol, 2010. Relationship between the antioxidant capacity and effect of rosemary (Rosmarinus officinalis L.) polyphenols on membrane phospholipid order. J. Agr. Food Chem., 58(1): 161-171.
    CrossRef    PMid:19924866    Direct Link
38. Pulido, R., L. Bravo and F. Saura-Calixto, 2000. Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J. Agr. Food Chem., 48: 3396-3402.
    CrossRef    PMid:10956123    
39. Raharjo, S., J.N. Sofos and G.R. Schmidt, 1992. Improved speed, specificity, and limit of determination of an aqueous acid extraction thiobarbituric acid-C18 method for measuring lipid peroxidation in beef. J. Agr. Food Chem., 40(11): 2182-2185.
    CrossRef    Direct Link
40. Raškovic, A., I. Milanovic, N. Pavlovic, T. Cebovic, S. Vukmirovic and M. Mikov, 2014. Antioxidant activity of rosemary (Rosmarinus officinalis L.) essential oil and its hepatoprotective potential. BMC Complem. Altern. M., 14: 225.
    CrossRef    PMid:25002023 PMCid:PMC4227022    Direct Link
41. Re, R., N. Pellegrini, A. Proteggente, A. Pannala, M. Yang and C. Rice-Evans, 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Bio. Med., 26(9-10): 1231-1237.
    CrossRef    
42. Realini, C.E. and B. Marcos, 2014. Active and intelligent packaging systems for a modern society. Meat Sci., 98(3): 404-419.
    CrossRef    PMid:25034453    Direct Link
43. Rocha, F.D., A.R. Soares, P.J. Houghton, R.C. Pereira, M.A. Kaplan and V.L. Teixeira, 2007. Potential cytotoxic activity of some Brazilian seaweeds on human melanoma cells. Phytother. Res., 21(2): 170-175.
    CrossRef    PMid:17133653    Direct Link
44. Savadkoohi, S., H. Hoogenkamp, K. Shamsi and A. Farahnaky, 2014. Color, sensory and textural attributes of beef frankfurter, beef ham and meat-free sausage containing tomato pomace. Meat Sci., 97(4): 410-418.
    CrossRef    PMid:24769097    Direct Link
45. Sáyago-Ayerdi, S.G., A. Brenes, A. Viveros and I. Go-i, 2009. Antioxidative effect of dietary grape pomace concentrate on lipid oxidation of chilled and long-term frozen stored chicken patties. Meat Sci., 83(3): 528-533.
    CrossRef    PMid:20416664    Direct Link
46. Sebranek, J.G., V.J.H. Sewalt, K.L. Robbins and T.A. Houser, 2005. Comparison of a natural rosemary extract and BHA/BHT for relative antioxidant effectiveness in pork sausage. Meat Sci., 69(2): 289-296.
    CrossRef    PMid:22062821    Direct Link
47. Seneviratne, K.N., W.C. Prasadani and B. Jayawardena, 2016. Phenolic extracts of coconut oil cake: A potential alternative for synthetic antioxidants. Food Sci. Technol., 36(4): 591-597.
    CrossRef    Direct Link
48. Shah, M.A., S.J.D. Bosco and S.A. Mir, 2014. Plant extracts as natural antioxidants in meat and meat products. Meat Sci., 98(1): 21-33.
    CrossRef    PMid:24824531    Direct Link
49. Singleton, V.L., R. Orthofer and R.M. Lamuela-Raventós, 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Method. Enzymol., 299: 152-178.
    CrossRef    Direct Link
50. Sun-Waterhouse, D., J. Zhou, G.M. Miskelly, R. Wibisono and S.S. Wadhwa, 2011. Stability of encapsulated olive oil in the presence of caffeic acid. Food Chem., 126(3): 1049-1056.
    CrossRef    Direct Link
51. Švarc-Gajic, J., Z. Stojanovic, A.S. Carretero, D.A. Román, I. Borrás and I. Vasiljevic, 2013. Development of a microwave-assisted extraction for the analysis of phenolic compounds from Rosmarinus officinalis. J. Food Eng., 119(3): 525-532.
    CrossRef    Direct Link
52. Teruel, M.R., M.D. Garrido, M.C. Espinosa and M.B. Linares, 2015. Effect of different format-solvent rosemary extracts (Rosmarinus officinalis) on frozen chicken nuggets quality. Food Chem., 172: 40-46.
    CrossRef    PMid:25442521    Direct Link
53. Vallverdú-Queralt, A., J. Regueiro, M. Martínez-Huélamo, J.F.R. Alvarenga, L.N. Leal and R.M. Lamuela-Raventos, 2014. A comprehensive study on the phenolic profile of widely used culinary herbs and spices: Rosemary, thyme, oregano, cinnamon, cumin and bay. Food Chem., 154: 299-307.
    CrossRef    PMid:24518346    Direct Link
54. Venturini, A.C., A.D. Cavenaghi, C.J.C. Castillo and E.M. Qui-ones, 2011. Sensory and microbiological evaluation of uncured fresh chicken sausage with reduced fat content. Ciênc. Tecnol. Aliment., 31(3): 629-634.
    CrossRef    Direct Link
55. Vicente, G., S. Molina, M. González-Vallinas, M.R. García-Risco, T. Fornari, G. Reglero and A.R. de Molina, 2013. Supercritical rosemary extracts, their antioxidant activity and effect on hepatic tumor progression. J. Supercrit. Fluid., 79: 101-108.
    CrossRef    Direct Link
56. Windisch, W., K. Schedle, C. Plitzner and A. Kroismayr, 2008. Use of phytogenic products as feed additives for swine and poultry. J. Anim. Sci., 86(14 Suppl): E140-E148.
    CrossRef    PMid:18073277    Direct Link
57. Yosr, Z., C. Hnia, T. Rim and B. Mohamed, 2013. Changes in essential oil composition and phenolic fraction in Rosmarinus officinalis L. var. typicus Batt. organs during growth and incidence on the antioxidant activity. Ind. Crops Prod., 43: 412-419.
    CrossRef    Direct Link
58. Zaouali, Y., T. Bouzaine and M. Boussaid, 2010. Essential oils composition in two Rosmarinus officinalis L. varieties and incidence for antimicrobial and antioxidant activities. Food Chem. Toxicol., 48(11): 3144-3152.
    CrossRef    PMid:20728499    Direct Link

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