| Peer-Reviewed

Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage

Received: 13 August 2020    Accepted: 24 August 2020    Published: 21 September 2020
Views:       Downloads:
Abstract

Sausage is one of the well-liked foodstuffs in many areas. However, its quality is vulnerable to deteriorate owing to the lipid oxidation and microbial contamination. This research aimed to study the influence of thyme and clove essential oils (EOs) with or without nitrite on the chemical composition, microbial growth, and lipid oxidation rate in sausage during frozen storage-18°C for three months. The obtained results showed that the main component in clove EO and thyme EO is eugenol and thymol. Adding sodium nitrite to sausage resulted in declines in moisture and crude lipids and increases in protein and ash contents of sausage. Adding the tested EOs increased nitrite's effect on the chemical composition of sausage. Besides, these EOs lowered TBARS values, residual nitrite, and TBC in sausage. They also resulted in the rise of nitrite's efficacy in reducing TBARS values and TBC in sausage. Proteus was more sensitive than Klebsiella, whereas E. coli showed more resistance when adding nitrite or EO to sausage. The tested EOs increased the inhibitory influence of nitrite on Proteus, Klebsiella, Aspergillus niger, and Candida albicans in sausage. We concluded that the EOs of clove and thyme have antioxidant and antimicrobial efficacies in raw beef sausage during frozen storage. Also, they have a synergistic impact on nitrite. Therefore, it is suggested that these EOs, especially thyme, could be utilized to prolong shelf-life, prevent deterioration of sausage, and lessen the added nitrite's proportion to sausage for avoiding the formation of carcinogenic N-nitrosamines‏.

Published in Journal of Food and Nutrition Sciences (Volume 8, Issue 5)
DOI 10.11648/j.jfns.20200805.11
Page(s) 117-126
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Clove Essential Oil, Thyme Essential Oil, Antioxidant Activity, Antimicrobial Activity, Nitrite, Beef Sausage

References
[1] Pal, M., & Devrani, M. (2018). Application of various techniques for meat preservation. Journal of Experimental Food Chemistry, 4 (4), 134. http://doi.org/10.4172/2472-0542.1000134.
[2] Škrlep, M., Čandek-Potokar, M., Batorek-Lukač, N., Tomažin, U., & Flores, M. (2019). Aromatic profile, physicochemical and sensory traits of dry-fermented sausages produced without nitrites using pork from Krškopolje pig reared in organic and conventional husbandry. Animals, 9 (55), 1-13. https://doi.org/10.3390/ani9020055.
[3] Cai, C., Ma, R., Duan, M., & Lu, D. (2019). Preparation and antimicrobial activity of thyme essential oil microcapsules prepared with gum arabic. RSC Advances, 9, 19740–19747. http://doi.org/ 10.1039/c9ra03323h.
[4] Wińska, K., Mᶐczka, W., Łyczko, J., Grabarczyk, M., Czubaszek, A., & Szumny, A. (2019). Essential oils as antimicrobial agents—myth or real alternative?. Molecules, 24, 2130. https://doi.org/10.3390/molecules24112130.
[5] Kamkar, A., Tooriyan, F., Jafari, M., Bagherzade, M., Saadatjou, S. & Molaee, A. E. (2014). Antioxidant activity of methanol and ethanol extracts of Satureja hortensis L. in soybean oil. Journal of Food Quality and Hazards Control, 1, 113-119. http://jfqhc.ssu.ac.ir.
[6] Shaltout, F. A., Thabet, M. G., & Koura, H. A. (2017). Impact of some essential oils on the quality aspect and shelf life of meat. Journal of Nutrition & Food Sciences, 7, 647. http://doi:10.4172/2155-9600.1000647.
[7] Ghadermazi, R., Keramat, J., & Goli, S. A. H. (2017). Antioxidant activity of clove (Eugenia caryophyllata Thunb), oregano (Oringanum vulgare L) and sage (Salvia officinalis L) essential oils in various model systems. International Food Research Journal, 24 (4), 1628-1635. http://www.ifrj.upm.edu.my
[8] Purkait, S., Bhattacharya, A., Bag, A., & Chattopadhyay, R. R. (2018). Antibacterial and antioxidant potential of essential oils of five spices. Journal of Food Quality and Hazards Control, 5, 61-71. DOI: 10.29252/jfqhc.5.2.6 http://www.jfqhc.com.
[9] Pancevska, N. A,, Bogdanov, J., & Kungulovski, D. (2017). In Vitro antimicrobial activity and chemical composition of two essential oils and eugenol from flower buds of Eugenia caryophyllata. Open Biological Sciences Journal, 3, 16-25. http://dx.doi.org/10.2174/2352633501703010016.
[10] Boskovic, M., Glisic, M., Djordjevic, J., Starcevic, M., Glamoclija, N., Djordjevic, V., & Baltic, M. Z. (2019). Antioxidative activity of thyme (Thymus vulgaris) and oregano (Origanum vulgare) essential oils and their effect on oxidative stability of minced pork packaged under vacuum and modified atmosphere. Journal of Food Science, 84 (9), 2467-2474. https://doi.org/10.1111/1750-3841.14788.
[11] Gedikoğlu, A., Sökmen, M., & Çivit, A. (2019). Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food Science & Nutrition, 7, 1704-1714. https://dx.doi.org/10.1002%2Ffsn3.1007.
[12] El-Zainy, A. R., Morsy, A. E., Sedki, A. G., & Mosa, N. M. (2016). Polyphenols Grape seeds extract as antioxidant and antimicrobial in Beef sausage. International Journal of Current Science, 19 (2), E 112-121. www.currentsciencejournal.info.
[13] Hassan, F. (2010). Studies on microbiological and chemical characteristics of some meat products. Ph.D. Thesis, Faculty of Agriculture, Mansoura University, Egypt.
[14] Oliveira, T. L., Malfitano de Carvalho, S., Soares, R. A., Andrade, M. A., Cardoso, M. G., & Ramos, E. M. (2012). Antioxidant effects of Satureja montana L. essential oil on TBARS and color of mortadella-type sausages formulated with different levels of sodium nitrite. LWT-Food Science and Technology, 45, 204-212. https://doi.org/10.1016/j.lwt.2011.09.006.
[15] A. O. A. C. (2005). Official Methods of Analysis, 18th edn. Association of Official Analytical Chemists, Washington, D.C.
[16] Uddin, M. A., Shahinuzzaman, M., Rana, M. S., & Yaakob, Z. (2017). Study of chemical composition and medicinal properties of volatile oil from clove buds (Eugenia caryophyllus). International Journal of Pharmaceutical Sciences and Research, 8 (2), 895-99. http://doi.org/10.13040/IJPSR.0975-8232.8(2).895-99.
[17] Siu, G. M., & Draper, H. H. (1978). A Survey of the Malonaldehyde Content of Retail Meats and Fish. Journal of Food Science, 43, 1147-1149. https://doi.org/10.1111/j.1365-2621.1978.tb15256.x.
[18] Montgomery, G. A. & Dymock, J. F. (1961). The determination of nitrite in water. Analyst, 86, 414.
[19] Difco Manual (1966). Dehydrated Culture Media and Reagents Procedures. 9th edn. USA: Difco Laboratories.
[20] Ahmed, A. A. & Sabiel, Y. A. (2016). Detection of microbial contamination of processed beef meat by using Api strips and automated Vitek 2 compact system. British Microbiology Research Journal, 13 (2), 1-8. www.sciencedomain.org.
[21] Anwer, S. S., Ali, G. A., Hamadamin, C. Z., & Jaafar, H. Y. (2017). Isolation and identification of fungiform fast food restaurants in Langa Bazar. International Journal of Environment, Agriculture and Biotechnology, 2 (4), 1517-1522. https://dx.doi.org/10.22161/ijeab/2.4.10.
[22] El-Abasy, A. E, Abou-Gharbia, H. A., Mousa, H. M., Youssef, M. M. (2012). Mixes of carrot juice and some fermented dairy products: potentiality as novel functional beverages. Food and Nutrition Sciences, 3, 233-239. http://dx.doi.org/10.4236/fns.2012.32034.
[23] Graph Pad Prism (1999). GraphPad Prism version 3.00 for windows. GraphPad Software, San Diego, CA, USA.
[24] Egyptian Organization for Standardization and Quality. (2005). Egyption Standard, Egypt. http://www.eos.org.eg/en/standards.
[25] Aminzare. M,, Aliakbarlu, J., & Tajik, H. (2015). The effect of Cinnamomum zeylanicum essential oil on chemical characteristics of Lyoner- type sausage during refrigerated storage. Veterinary Research Forum, 6 (1), 31-39. vrf.iranjournals.ir.
[26] Wójciak, K. M., Stasiak, D. M. & Kȩska, P. (2019). The influence of different levels of sodium nitrite on the safety, oxidative stability, and color of minced roasted beef. Sustainability, 11, 3795. https://doi.org/10.3390/su11143795.
[27] Alahakoon, A. U., Jayasena, D. D., Ramachandra, S., & Jo, C. (2015). Alternatives to nitrite in processed meat: Up to date. Trends in Food Science & Technology, 45, 37- 49. https://doi.org/10.1016/j.tifs.2015.05.008.
[28] Zengin, H., & Baysal, A. H. (2015). Antioxidant and antimicrobial activities of thyme and clove essential oils and application in minced beef. Journal of Food Processing and Preservation, 39 (6), 1261–1271. https://doi.org/10.1111/jfpp.12344.
[29] Sharma, H., Mendiratta, S. K., Agrawal, R. K., Gurunathan, K., Kumar, S., & Singh, T. P. (2017a). 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. www.elsevier.com/locate/lwt.
[30] Viuda-Martos, M., Ruiz-Navajas, Y., Fernández-López, J., & Pérez-Álvarez, J. A. (2009). Effect of adding citrus waste water, thyme and oregano essential oil on the chemical, physical and sensory characteristics of a bologna sausage. Innovative Food Science and Emerging Technologies, 10, 655–660. https://doi.org/10.1016/j.ifset.2009.06.001.
[31] El Adab, S., & Hassouna, M. (2016). Proteolysis, lipolysis and sensory characteristics of a Tunisian dry fermented poultry meat sausage with oregano and thyme essential oils. Journal of Food Safety, 36, 19-32. https://doi.org/10.1111/jfs.12209.
[32] Blanco-Lizarazo, C. M., Betancourt-Cortés, R., Lombana, A., Carrillo-Castro, K., & Sotelo-Díaz, I. (2017). Listeria monocytogenes behaviour and quality attributes during sausage storage affected by sodium nitrite, sodium lactate and thyme essential oil. Food Science and Technology International, 23 (3), 277–288. https://doi.org/10.1177%2F1082013216686464.
[33] El Ghallab, Y., Al Jahid, A., Jamal Eddine, J., Said, A. A., Zarayby, L., & Derfoufi, S. (2019). Syzygium aromaticum L.: phytochemical investigation and comparison of the scavenging activity of essential oil, extracts and eugenol. Oriental Pharmacy and Experimental Medicine, published online: 06 December 2019. https://doi.org/10.1007/s13596-019-00416-7.
[34] Stagos, D. (2020). Antioxidant activity of polyphenolic plant extracts. Antioxidants, 9, 19. https://doi.org/10.3390/antiox9010019.
[35] Govari, M., & Pexara, A. (2015). Nitrates and nitrites in meat products. Journal of the Hellenic Veterinary Medical Society, 66 (3), 127-140. http://dx.doi.org/10.12681/jhvms.15856.
[36] Merino, L., Darnerud, P. O., Toldrá, F., & Ilbäck, N-G. (2016). Time-dependent depletion of nitrite in pork/beef and chicken meat products and its effect on nitrite intake estimation. Food Additives & Contaminants, Part A, 33 (2), 186-192. https://dx.doi.org/10.1080%2F19440049.2015.1125530.
[37] Melngaile, A., Ciekure, E., & Valcina, O. (2014). Microbiological quality of meat preparations and meat products. Foodbalt, 61-65. http://llufb.llu.lv/conference/foodbalt/2014/FoodBalt_Proceedings_2014-61-65.pdf
[38] Lee, S., Lee, H., Kim, S., Lee, J., Ha, J., Choi, Y., Oh, H., Choi, K-H., & Yoon, Y. (2018). Microbiological safety of processed meat products formulated with low nitrite concentration- A review. Asian-Australasian Journal of Animal Sciences, 00, 1-5. https://doi.org/10.5713/ajas.17.0675.
[39] Man, A., Santacroce, L., Jacob, R., Mare, A., & Man, L. (2019). Antimicrobial activity of six essential oils against a group of human pathogens: A comparative study. Pathogens, 8, 15, https://doi.org/10.3390/pathogens8010015.
[40] Ibrahim, H. M., El Sabagh, R. A., Abou El-Roos, N. A., & Abd El Fattah, H. (2016). Antimicrobial effect of some essential oils on Staphylococcus aureus in minced meat. Benha Veterinary Medical Journal, 30 (1), 183-191. https://dx.doi.org/10.21608/bvmj.2016.31362.
[41] Sindelar, J. J., & Milkowski, A. L. (2012). Human safety controversies surrounding nitrate and nitrite in the diet. Nitric Oxide, 26, 259–266. https://doi.org/10.1016/j.niox.2012.03.011.
[42] De Alba, M., Bravo, D., Medina, M., Park, S. F., & Mackey, B. M. (2012). Combined effect of sodium nitrite with high-pressure treatments on the inactivation of Escherichia coli BW25113 and Listeria monocytogenes NCTC 11994. Letters in Applied Microbiology, 56, 155-160. https://doi.org/10.1111/lam.12031.
[43] Badhe, S. R., Fairoze, M. N., Raghunath, B. V., Sudharshan, S., Ruban, W. S., & Chandrashekaran, V. (2013). Evaluation of antimicrobial efficacy of aqueous extract and essential oil of clove (Eugenia caryophylata thunb) in chicken meat against various food borne pathogens. Journal of Cell and Tissue Research, 13 (1): 3507-3511. http://www.tcrjournals.com%29/.
[44] Tompkin, R. B. (2005). Nitrite. In Davidson, P. M., Sofos, J. N., & Branen, A. L. (ed.), Antimicrobials in food. Taylor & Francis, Boca Raton, FL., p. 169-236. http://www.fsis.usda.gov/OPPDE/rdad/FSISDirectives/7620-3.pdf.
[45] Ozturk, I. (2015). Antifungal activity of propolis, thyme essential oil and hydrosol on natural mycobiota of sucuk, a Turkish fermented sausage: monitoring of their effects on microbiological, color and aroma properties. Journal of Food Processing and Preservation, 39:1148–1158. https://doi.org/10.1111/jfpp.12329.
[46] Sakkas, H., Gousia, P., Economou, V., Petsios, S., & Papadopoulou, C. (2016). Antifungal activity of four essential oils against Candida clinical isolates. Asian Journal of Ethnopharmacology and Medicinal Foods, 2, 22-25.
[47] Gonçalves, N. D., Pena, F. L., Sartoratto, A., Derlamelina, C., Duarte, M. C., Antunes, A. E., & Prata, A. S. (2017). Encapsulated thyme (Thymus vulgaris) essential oil used as a natural preservative in bakery product. Food Research International, 96: 154–160. https://doi.org/10.1016/j.foodres.2017.03.006.
Cite This Article
  • APA Style

    Amal Gamil Sedki, Ashraf Refaat El-Zainy, Basma Tarek Rajab. (2020). Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage. Journal of Food and Nutrition Sciences, 8(5), 117-126. https://doi.org/10.11648/j.jfns.20200805.11

    Copy | Download

    ACS Style

    Amal Gamil Sedki; Ashraf Refaat El-Zainy; Basma Tarek Rajab. Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage. J. Food Nutr. Sci. 2020, 8(5), 117-126. doi: 10.11648/j.jfns.20200805.11

    Copy | Download

    AMA Style

    Amal Gamil Sedki, Ashraf Refaat El-Zainy, Basma Tarek Rajab. Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage. J Food Nutr Sci. 2020;8(5):117-126. doi: 10.11648/j.jfns.20200805.11

    Copy | Download

  • @article{10.11648/j.jfns.20200805.11,
      author = {Amal Gamil Sedki and Ashraf Refaat El-Zainy and Basma Tarek Rajab},
      title = {Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage},
      journal = {Journal of Food and Nutrition Sciences},
      volume = {8},
      number = {5},
      pages = {117-126},
      doi = {10.11648/j.jfns.20200805.11},
      url = {https://doi.org/10.11648/j.jfns.20200805.11},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.jfns.20200805.11},
      abstract = {Sausage is one of the well-liked foodstuffs in many areas. However, its quality is vulnerable to deteriorate owing to the lipid oxidation and microbial contamination. This research aimed to study the influence of thyme and clove essential oils (EOs) with or without nitrite on the chemical composition, microbial growth, and lipid oxidation rate in sausage during frozen storage-18°C for three months. The obtained results showed that the main component in clove EO and thyme EO is eugenol and thymol. Adding sodium nitrite to sausage resulted in declines in moisture and crude lipids and increases in protein and ash contents of sausage. Adding the tested EOs increased nitrite's effect on the chemical composition of sausage. Besides, these EOs lowered TBARS values, residual nitrite, and TBC in sausage. They also resulted in the rise of nitrite's efficacy in reducing TBARS values and TBC in sausage. Proteus was more sensitive than Klebsiella, whereas E. coli showed more resistance when adding nitrite or EO to sausage. The tested EOs increased the inhibitory influence of nitrite on Proteus, Klebsiella, Aspergillus niger, and Candida albicans in sausage. We concluded that the EOs of clove and thyme have antioxidant and antimicrobial efficacies in raw beef sausage during frozen storage. Also, they have a synergistic impact on nitrite. Therefore, it is suggested that these EOs, especially thyme, could be utilized to prolong shelf-life, prevent deterioration of sausage, and lessen the added nitrite's proportion to sausage for avoiding the formation of carcinogenic N-nitrosamines‏.},
     year = {2020}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Thyme and Clove Essential Oils as Antioxidants and Antimicrobial in Beef Sausage
    AU  - Amal Gamil Sedki
    AU  - Ashraf Refaat El-Zainy
    AU  - Basma Tarek Rajab
    Y1  - 2020/09/21
    PY  - 2020
    N1  - https://doi.org/10.11648/j.jfns.20200805.11
    DO  - 10.11648/j.jfns.20200805.11
    T2  - Journal of Food and Nutrition Sciences
    JF  - Journal of Food and Nutrition Sciences
    JO  - Journal of Food and Nutrition Sciences
    SP  - 117
    EP  - 126
    PB  - Science Publishing Group
    SN  - 2330-7293
    UR  - https://doi.org/10.11648/j.jfns.20200805.11
    AB  - Sausage is one of the well-liked foodstuffs in many areas. However, its quality is vulnerable to deteriorate owing to the lipid oxidation and microbial contamination. This research aimed to study the influence of thyme and clove essential oils (EOs) with or without nitrite on the chemical composition, microbial growth, and lipid oxidation rate in sausage during frozen storage-18°C for three months. The obtained results showed that the main component in clove EO and thyme EO is eugenol and thymol. Adding sodium nitrite to sausage resulted in declines in moisture and crude lipids and increases in protein and ash contents of sausage. Adding the tested EOs increased nitrite's effect on the chemical composition of sausage. Besides, these EOs lowered TBARS values, residual nitrite, and TBC in sausage. They also resulted in the rise of nitrite's efficacy in reducing TBARS values and TBC in sausage. Proteus was more sensitive than Klebsiella, whereas E. coli showed more resistance when adding nitrite or EO to sausage. The tested EOs increased the inhibitory influence of nitrite on Proteus, Klebsiella, Aspergillus niger, and Candida albicans in sausage. We concluded that the EOs of clove and thyme have antioxidant and antimicrobial efficacies in raw beef sausage during frozen storage. Also, they have a synergistic impact on nitrite. Therefore, it is suggested that these EOs, especially thyme, could be utilized to prolong shelf-life, prevent deterioration of sausage, and lessen the added nitrite's proportion to sausage for avoiding the formation of carcinogenic N-nitrosamines‏.
    VL  - 8
    IS  - 5
    ER  - 

    Copy | Download

Author Information
  • Department of Home Economics, Mansoura University, Mansoura, Egypt

  • Department of Home Economics, Mansoura University, Mansoura, Egypt

  • Department of Home Economics, Mansoura University, Mansoura, Egypt

  • Sections