SAGE ESSENTIAL OIL EXHIBITS ANTIOXIDATIVE AND ANTIMICROBIAL ACTIVITY IN CHICKEN COOKED SAUSAGES
Keywords:
sage essential oil; cooked sausage; novel antioxidants; antimicrobial activity
Abstract
Sage (Salvia officinalis L.) represents medicinal plant from Lamiaceae family, which has been recognized for various biological activities due to its complex chemical profile. Besides widely used application in pharmaceutical industry, sage has found application as flavoring agent in food products. The effect of sage essential oil (SEO) obtained from sage (Salvia officinalis L.) on antioxidative and antimicrobial activity in cooked chicken sausages was investigated. pH, instrumental parameters of color (CIE L*, CIE a* and CIE b*), thiobarbituric acid-reactive substance (TBARS) value, microbial profile and sensory panel scores were examined. The addition of SEO in concentrations from 0.010 to 0.100 µl/g significantly (p<0.05) affected the color of the product by reducing in lightness (CIE L*) and increasing in redness (CIE a*). The inclusion of SEO in concentrations of 0.075 and 0.100 µL/g significantly (p<0.05) reduced the lipid oxidation defined by TBARS test. All five tested concentrations of SEO resulted in significant (p<0.05) inhibition of bacterial growth. This study shows that the sage essential oil could be used in processing of cooked chicken sausages in order to improve oxidative and microbial stability as well as to enhance their color characteristics, without negative implications on flavor of the final meat products.
References
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Danilović, B., Đorđević, N., Karabegović, I., Šojić, B., Pavlić, B., & Savić, D. (2021). The effect of sage herbal dust products on Listeria monocytogenes growth in minced pork. Journal of Food Processing and Preservation, 45(10). https://doi.org/10.1111/jfpp.15802
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Honikel, K.-O. (2008). The use and control of nitrate and nitrite for the processing of meat products. Meat Science, 78(1–2), 68–76. https://doi.org/10.1016/j.meatsci.2007.05.030
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ISO (2003). Horizontal method for the enumeration of microorganisms – Colony- counttechnique at 30 degrees C. ISO 4833. International standards microbiology of food and animal feeding stuffs. Geneva, Switzerland: International Organization for Standardization.
Liu, D. C., Tsau, R. T., Lin, Y. C., Jan, S. S., & Tan, F. J. (2009). Effect of various levels of rosemary or Chinese mahogany on the quality of fresh chicken sausage during refrigerated storage. Food Chemistry, 117(1), 106–113. https://doi.org/ 10.1016/J. FOODCHEM.2009.03.083
Meilgaard, M. C. (1993). Individual differences in sensory threshold for aroma chemicals added to beer. Food Quality and Preference, 4(3), 153–167. https://doi.org/ 10.1016/0950-3293(93)90158-3
Mujović, M., Šojić, B., Danilović, B., Kocić-Tanackov, S., Ikonić, P., Đurović, S., Milošević, S., Bulut, S., Đorđević, N., Savanović, J., & Pavlić, B. (2023). Fennel (Foeniculum vulgare) essential oil and supercritical fluid extracts as novel antioxidants and antimicrobial agents in beef burger processing. Food Bioscience, 56, 103283. https://doi.org/10.1016/J. FBIO.2023.103283
Munekata, P. E. S., Rocchetti, G., Pateiro, M., Lucini, L., Domínguez, R., & Lorenzo, J. M. (2020). Addition of plant extracts to meat and meat products to extend shelf-life and health-promoting attributes: an overview. Current Opinion in Food Science, 31, 81–87. https://doi.org/10.1016/ J.COFS.2020.03.003
Ozaki, M. M., Munekata, P. E. S., Jacinto-Valderrama, R. A., Efraim, P., Pateiro, M., Lorenzo, J. M., & Pollonio, M. A. R. (2021). Beetroot and radish powders as natural nitrite source for fermented dry sausages. Meat Science, 171, 108275. https:// doi.org/10.1016/ j.meatsci.2020.108275
Ozaki, M. M., Munekata, P. E. S., Lopes, A. D. S., Nascimento, M. D. S. D., Pateiro, M., Lorenzo, J. M., & Pollonio, M. A. R. (2020). Using chitosan and radish powder to improve stability of fermented cooked sausages. Meat Science, 167. https://doi.org/10.1016/ j.meatsci. 2020.108165
Pavlić, B., Bera, O., Teslić, N., Vidović, S., Parpinello, G., & Zeković, Z. (2018). Chemical profile and antioxidant activity of sage herbal dust extracts obtained by supercritical fluid extraction. Industrial Crops and Products, 120, 305–312. https://doi.org/10.1016/j.indcrop.2018.04.044
Pavlić, B., Šojić, B., Teslić, N., Putnik, P., & Kovačević, D. B. (2021). Extraction of bioactive compounds and essential oils from herbs using green technologies. In Aromatic Herbs in Food (pp. 233–262). Elsevier. https://doi.org/10.1016/b978-0-12-822716-9.00007-x
Riel, G., Boulaaba, A., Popp, J., & Klein, G. (2017). Effects of parsley extract powder as an alternative for the direct addition of sodium nitrite in the production of mortadella-type sausages – Impact on microbiological, physicochemical and sensory aspects. Meat Science, 131, 166–175. https://doi.org/10.1016/J.MEATSCI.2017.05.007
Schmidt, M. M., Dornelles, R. C. P., Vidal, A. R., Fontoura, A., Kubota, E. H., Mello, R. O., Kempka, A. P., & Demiate, I. M. (2017). Development of cooked and smoked chicken sausage with reduced sodium and fat. Journal of Applied Poultry Research, 26(1), 130–144. https://doi.org/10.3382/JAPR/PFW054
Sharma, H., Mendiratta, S. K., Agrawal, R. K., Gurunathan, K., Kumar, S., & Singh, T. P. (2017). Use of various essential oils as bio preservatives and their effect on the quality of vacuum packaged fresh chicken sausages under frozen conditions. LWT - Food Science and Technology, 81, 118–127. https://doi.org/10.1016/j.lwt.2017.03.048
Šojić, B., Pavlić, B., Ikonić, P., Tomović, V., Ikonić, B., Zeković, Z., Kocić-Tanackov, S., Jokanović, M., Škaljac, S., & Ivić, M. (2019). Coriander essential oil as natural food additive improves quality and safety of cooked pork sausages with different nitrite levels. Meat Science. https://doi.org/10.1016/j.meatsci.2019.107879
Šojić, B., Pavlić, B., Tomović, V., Kocić-Tanackov, S., Đurović, S., Zeković, Z., Belović, M., Torbica, A., Jokanović, M., Uromović, N., Ivić, M., & Škaljac, S. (2020). Tomato pomace extract and organic peppermint essential oil as effective sodium nitrite replacement in cooked pork sausages. Food Chemistry, 330. https://doi.org/10.1016/j.foodchem.2020.127202
Šojić, B., Pavlić, B., Zeković, Z., Tomović, V., Ikonić, P., Kocić-Tanackov, S., & Džinić, N. (2018). The effect of essential oil and extract from sage (Salvia officinalis L.) herbal dust (food industry by-product) on the oxidative and microbiological stability of fresh pork sausages. LWT - Food Science and Technology, 89. https://doi.org/10.1016/j.lwt.2017.11.055
Šojić, B., Tomović, V., Kocić-Tanackov, S., Škaljac, S., Ikonić, P., Džinić, N., Živković, N., Jokanović, M., Tasić, T., & Kravić, S. (2015). Effect of nutmeg (Myristica fragrans) essential oil on the oxidative and microbial stability of cooked sausage during refrigerated storage. Food Control, 54. https://doi.org/10.1016/j.foodcont.2015.02.007
Šojić, B., Tomović, V., Savanović, J., Kocić-Tanackov, S., Pavlić, B., Jokanović, M., Milidrag, A., Martinović, A., Vujadinović, D., & Vukić, M. (2021). Sage (Salvia officinalis L.) essential oil as a potential replacement for sodium nitrite in dry fermented sausages. Processes, 9(3), 1–15. https://doi.org/10.3390/pr9030424
Sucu, C., & Turp, G. Y. (2018). The investigation of the use of beetroot powder in Turkish fermented beef sausage (sucuk) as nitrite alternative. Meat Science, 140, 158–166. https://doi.org/10.1016/j.meatsci.2018.03.012
Yazgan, H. (2020). Investigation of antimicrobial properties of sage essential oil and its nanoemulsion as antimicrobial agent. LWT, 130, 109669. https://doi.org/10.1016/J. LWT.2020.109669
Zhang, L., Lin, Y. H., Leng, X. J., Huang, M., & Zhou, G. H. (2013). Effect of sage (Salvia officinalis) on the oxidative stability of Chinese-style sausage during refrigerated storage. Meat Science, 95(2), 145–150. https://doi.org/10.1016/j.meatsci.2013.05.005
Burt, S. (2004). Essential oils: Their antibacterial properties and potential applications in foods - A review. International Journal of Food Microbiology, 94(3), 223–253. https://doi.org/10.1016/j.ijfoodmicro. 2004.03.022
Da Silveira, S. M., Luciano, F. B., Fronza, N., Cunha, A., Scheuermann, G. N., & Vieira, C. R. W. (2014). Chemical composition and antibacterial activity of Laurus nobilis essential oil towards foodborne pathogens and its application in fresh Tuscan sausage stored at 7°C. LWT - Food Science and Technology, 59(1), 86–93. https://doi.org/10.1016/j.lwt.2014.05.032
Danilović, B., Đorđević, N., Karabegović, I., Šojić, B., Pavlić, B., & Savić, D. (2021). The effect of sage herbal dust products on Listeria monocytogenes growth in minced pork. Journal of Food Processing and Preservation, 45(10). https://doi.org/10.1111/jfpp.15802
Danilović, B., Đorđević, N., Milićević, B., Šojić, B., Pavlić, B., Tomović, V., & Savić, D. (2021). Application of sage herbal dust essential oils and supercritical fluid extract for the growth control of Escherichia coli in minced pork during storage. LWT, 141. https://doi.org/10.1016/j. lwt.2021.110935
Guerra, C. A., Costa, L. M., de Oliveira, V. S., de Paula, B. P., Junior, W. J. F. L., Luchese, R. H., Corich, V., Giacomini, A., & Guerra, A. F. (2023). Correlation between natural microbial load and formation of ropy slime affecting the superficial color of vacuum-packaged cooked sausage. Meat Science, 201, 109197. https://doi.org/10.1016/J.MEATSCI.2023.109197
Hassoun, A., & Emir Çoban, Ö. (2017). Essential oils for antimicrobial and antioxidant applications in fish and other seafood products. Trends in Food Science & Technology, 68, 26–36. https://doi.org/10.1016/J.TIFS.2017.07.016
Honikel, K.-O. (2008). The use and control of nitrate and nitrite for the processing of meat products. Meat Science, 78(1–2), 68–76. https://doi.org/10.1016/j.meatsci.2007.05.030
ISO (2008). Horizontal method for the detection of Salmonella spp. ISO 6579. International standards microbiology of food and animal feeding stuffs. Geneva, Switzerland: International Organization for Standardization.
ISO (2005). Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli – Part 2: Colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide. ISO 16649-2. International standards microbiology of food and animal feeding stuffs. Geneva, Switzerland: International Organization for Standardization.
ISO (2014). Horizontal method for the detection and enumeration of Listeria monocytogenes – part 2: Enumeration method. ISO 11290-2. International standards microbiology of food and animal feeding stuffs. Geneva, Switzerland: International Organization for Standardization.
ISO (2003). Horizontal method for the enumeration of microorganisms – Colony- counttechnique at 30 degrees C. ISO 4833. International standards microbiology of food and animal feeding stuffs. Geneva, Switzerland: International Organization for Standardization.
Liu, D. C., Tsau, R. T., Lin, Y. C., Jan, S. S., & Tan, F. J. (2009). Effect of various levels of rosemary or Chinese mahogany on the quality of fresh chicken sausage during refrigerated storage. Food Chemistry, 117(1), 106–113. https://doi.org/ 10.1016/J. FOODCHEM.2009.03.083
Meilgaard, M. C. (1993). Individual differences in sensory threshold for aroma chemicals added to beer. Food Quality and Preference, 4(3), 153–167. https://doi.org/ 10.1016/0950-3293(93)90158-3
Mujović, M., Šojić, B., Danilović, B., Kocić-Tanackov, S., Ikonić, P., Đurović, S., Milošević, S., Bulut, S., Đorđević, N., Savanović, J., & Pavlić, B. (2023). Fennel (Foeniculum vulgare) essential oil and supercritical fluid extracts as novel antioxidants and antimicrobial agents in beef burger processing. Food Bioscience, 56, 103283. https://doi.org/10.1016/J. FBIO.2023.103283
Munekata, P. E. S., Rocchetti, G., Pateiro, M., Lucini, L., Domínguez, R., & Lorenzo, J. M. (2020). Addition of plant extracts to meat and meat products to extend shelf-life and health-promoting attributes: an overview. Current Opinion in Food Science, 31, 81–87. https://doi.org/10.1016/ J.COFS.2020.03.003
Ozaki, M. M., Munekata, P. E. S., Jacinto-Valderrama, R. A., Efraim, P., Pateiro, M., Lorenzo, J. M., & Pollonio, M. A. R. (2021). Beetroot and radish powders as natural nitrite source for fermented dry sausages. Meat Science, 171, 108275. https:// doi.org/10.1016/ j.meatsci.2020.108275
Ozaki, M. M., Munekata, P. E. S., Lopes, A. D. S., Nascimento, M. D. S. D., Pateiro, M., Lorenzo, J. M., & Pollonio, M. A. R. (2020). Using chitosan and radish powder to improve stability of fermented cooked sausages. Meat Science, 167. https://doi.org/10.1016/ j.meatsci. 2020.108165
Pavlić, B., Bera, O., Teslić, N., Vidović, S., Parpinello, G., & Zeković, Z. (2018). Chemical profile and antioxidant activity of sage herbal dust extracts obtained by supercritical fluid extraction. Industrial Crops and Products, 120, 305–312. https://doi.org/10.1016/j.indcrop.2018.04.044
Pavlić, B., Šojić, B., Teslić, N., Putnik, P., & Kovačević, D. B. (2021). Extraction of bioactive compounds and essential oils from herbs using green technologies. In Aromatic Herbs in Food (pp. 233–262). Elsevier. https://doi.org/10.1016/b978-0-12-822716-9.00007-x
Riel, G., Boulaaba, A., Popp, J., & Klein, G. (2017). Effects of parsley extract powder as an alternative for the direct addition of sodium nitrite in the production of mortadella-type sausages – Impact on microbiological, physicochemical and sensory aspects. Meat Science, 131, 166–175. https://doi.org/10.1016/J.MEATSCI.2017.05.007
Schmidt, M. M., Dornelles, R. C. P., Vidal, A. R., Fontoura, A., Kubota, E. H., Mello, R. O., Kempka, A. P., & Demiate, I. M. (2017). Development of cooked and smoked chicken sausage with reduced sodium and fat. Journal of Applied Poultry Research, 26(1), 130–144. https://doi.org/10.3382/JAPR/PFW054
Sharma, H., Mendiratta, S. K., Agrawal, R. K., Gurunathan, K., Kumar, S., & Singh, T. P. (2017). Use of various essential oils as bio preservatives and their effect on the quality of vacuum packaged fresh chicken sausages under frozen conditions. LWT - Food Science and Technology, 81, 118–127. https://doi.org/10.1016/j.lwt.2017.03.048
Šojić, B., Pavlić, B., Ikonić, P., Tomović, V., Ikonić, B., Zeković, Z., Kocić-Tanackov, S., Jokanović, M., Škaljac, S., & Ivić, M. (2019). Coriander essential oil as natural food additive improves quality and safety of cooked pork sausages with different nitrite levels. Meat Science. https://doi.org/10.1016/j.meatsci.2019.107879
Šojić, B., Pavlić, B., Tomović, V., Kocić-Tanackov, S., Đurović, S., Zeković, Z., Belović, M., Torbica, A., Jokanović, M., Uromović, N., Ivić, M., & Škaljac, S. (2020). Tomato pomace extract and organic peppermint essential oil as effective sodium nitrite replacement in cooked pork sausages. Food Chemistry, 330. https://doi.org/10.1016/j.foodchem.2020.127202
Šojić, B., Pavlić, B., Zeković, Z., Tomović, V., Ikonić, P., Kocić-Tanackov, S., & Džinić, N. (2018). The effect of essential oil and extract from sage (Salvia officinalis L.) herbal dust (food industry by-product) on the oxidative and microbiological stability of fresh pork sausages. LWT - Food Science and Technology, 89. https://doi.org/10.1016/j.lwt.2017.11.055
Šojić, B., Tomović, V., Kocić-Tanackov, S., Škaljac, S., Ikonić, P., Džinić, N., Živković, N., Jokanović, M., Tasić, T., & Kravić, S. (2015). Effect of nutmeg (Myristica fragrans) essential oil on the oxidative and microbial stability of cooked sausage during refrigerated storage. Food Control, 54. https://doi.org/10.1016/j.foodcont.2015.02.007
Šojić, B., Tomović, V., Savanović, J., Kocić-Tanackov, S., Pavlić, B., Jokanović, M., Milidrag, A., Martinović, A., Vujadinović, D., & Vukić, M. (2021). Sage (Salvia officinalis L.) essential oil as a potential replacement for sodium nitrite in dry fermented sausages. Processes, 9(3), 1–15. https://doi.org/10.3390/pr9030424
Sucu, C., & Turp, G. Y. (2018). The investigation of the use of beetroot powder in Turkish fermented beef sausage (sucuk) as nitrite alternative. Meat Science, 140, 158–166. https://doi.org/10.1016/j.meatsci.2018.03.012
Yazgan, H. (2020). Investigation of antimicrobial properties of sage essential oil and its nanoemulsion as antimicrobial agent. LWT, 130, 109669. https://doi.org/10.1016/J. LWT.2020.109669
Zhang, L., Lin, Y. H., Leng, X. J., Huang, M., & Zhou, G. H. (2013). Effect of sage (Salvia officinalis) on the oxidative stability of Chinese-style sausage during refrigerated storage. Meat Science, 95(2), 145–150. https://doi.org/10.1016/j.meatsci.2013.05.005
Published
2025/03/19
Section
Papers