Effect of Foeniculum vulgare seed essential oil on the Staphylococcus aureus in minced Cyprinus carpio
Subject Areas : Food Science and TechnologyS. Bahrami 1 , E. Alizadeh Doughikollaee 2 , M. Shahriari moghadam 3
1 - MSc Student of Fish Product Processing, Faculty of Natural Resources, University of Zabol, Zabol, Iran
2 - Associate Professor, Department of Fisheries, Faculty of Natural Resources, University of Zabol, Zabol, Iran
3 - Assistant Professor, Department of Environmental Science, Faculty of Natural Resources, University of Zabol, Zabol, Iran
Keywords: Staphylococcus aureus, Foeniculum vulgare seed, Cyprinus carpio mince,
Abstract :
Antimicrobial properties of medicinal plants essential oil increased its application as a natural preservative in foods. The aim of this study was to investigate the effect of Foeniculum vulgare seed essential oil on the quality of minced Cyprinus carpio inoculated (103 CFU/g) with Staphylococcus aureus during refrigerated (4˚C) storage. The essential oil was extracted using Clevenger apparatus with water distillation method and concentrations of 4, 6 and 8 µl/g were added to the Cyprinus carpiomeat inoculated with S. aureus. Microbial [S. aureus count, total viable count (TVC) and psychrophilic bacteria count (PTC)], chemical parameters [pH, Thiobarbituric acid (TBA) and Total volatile basic nitrogen (TVB-N)] were measured at 24, 72, 144, 216 and 218 hours. According to the results, in control samples the number of S. aureus increased during the storage period; however, S. aureus population in the sample groups treated with different concentrations of essential oil was decreased. The lowest count of TVC and PTC were observed in the mince containing 8 µl/g of essential oil. Significant differences (p>0.05) were observed between the pH value of control and treatments. The TBA and TVB-N values of treatments increased during storage but it was lower in essential-containing samples.The fillets containing 6 µl/g of essential oil had a better sensory quality.It was concluded that F. vulgare seed essential oil have antioxidant and antibacterial properties and increased the shelf life of minced C. carpio during refrigerated storage.
● Abdollahi, M., Rezaei, M. and Farzi, G. (2014). Influence of chitosan/clay functional bionanocomposite activated with rosemary essential oil on the shelf life of fresh silver carp. International Journal of Food Science and Technology, 49(3): 811-818.
● Abdollahzadeh, E., Rezaei, M. and Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35(1): 177-183.
● AOAC, (2002). Official Methods of Analysis of the Association of the Official Analytical Chemists. Association of Official Analytical Chemists, (14th ed.), Washington, DC.
● AOAC, (2005). Official methods of analysis of the association of the official analytical chemists. Association of Official Analytical Chemists, (17th ed.), Washington, DC.
● Arashisar, S., Hisar, O., Kaya, M. and Yanik, T. (2004). Effects of modified atmosphere and vacuum packaging on microbiological and chemical properties of rainbow trout (Oncorynchus mykiss) fillets. International Journal of Food Microbiology, 97(2): 209-214.
● Bellik,Y. (2014). Total antioxidant activity and antimicrobial potency of the essential oil and oleoresin of Zingiber officinale Roscoe. Asian Pacific Journal of Tropical Disease, 4(1): 40-44.
● Casaburi, A., Nasi, A., Ferrocino, I., Di Monaco, R., Mauriello, G., Villani, F. et al. (2011). Spoilage-related activity of Carnobacterium maltaromaticum strains in air-stored and vacuum-packed meat. Applied and Environmental Microbiology, 77(20): 7382-7393.
● Dadalioǧlu, I. and Evrendilek, G. A. (2004). Chemical compositions and antibacterial effects of essential oils of Turkish oregano (Origanum minutiflorum), bay laurel (Laurus nobilis), Spanish lavender (Lavandula stoechas L.), and fennel (Foeniculum vulgare) on common foodborne pathogens. Journal of Agricultural and Food Chemistry, 52(26): 8255-8260.
● Delbarre-Ladrat, C., Chéret, R., Taylor, R. and Verrez-Bagnis, V. (2006). Trends in postmortem aging in fish: understanding of proteolysis and disorganization of the myofibrillar structure. Critical Reviews in Food Science and Nutrition, 46(5): 409-421.
● Dinges, M.M., Orwin, P.M. and Schlievert, P.M. (2000). Exotoxins of Staphylococcus aureus.Clinical Microbiology Reviews, 13(1): 16-34.
● Fan, W., Chi, Y. and Zhang, S. (2008). The use of a tea polyphenol dip to extend the shelf life of silver carp (Hypophthalmicthys molitrix) during storage in ice. Food Chemistry, 108(1): 148-153.
● Gheisari, H.M. and Ranjbar, V.R. (2012). Antioxidative and antimicrobial effects of garlic in ground camel meat. Turkish Journal of Veterinary and Animal Sciences, 36(1): 13-20.
● Govaris, A., Solomakos, N., Pexara, A. and Chatzopoulou, P.S. (2010). 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, 137(2-3): 175-180.
● Jayasena, D.D. and Jo, Ch. (2013). Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends in Food Science and Technology, 34(2): 96-108.
● Kachele, R., Zhang, M., Gao, Z. and Adhikari, B. (2017). Effect of vacuum packaging on the shelf-life of silver carp (Hypophthalmichthys molitrix) fillets stored at 4° C. LWT-Food Science and Technology, 80: 163-168.
●Kim, Y.B., Seo, K.W., Jeon, H.Y., Lim, S.K. and Lee, Y.J. (2018). Characteristics of the antimicrobial resistance of Staphylococcus aureus isolated from chicken meat produced by different integrated broiler operations in Korea. Poultry Science, 97(3): 962-969.
● Kvenberg J.E. (1991). Nonindigenous Bacterial Pathogens, In: Ward D.R. and Hackney, C. (Editors), Microbiology of Marine Food Products, Springer, Boston, MA, pp 267-284.
● Kwon, Y.S., Choi, W.G., Kim, W.J., cKim, W.K., Kim, M.J., Kang, W.H., et al. (2002). Antimicrobial constituents of Foeniculum vulgare. Archives of Pharmacal Research, 25(2): 154-157.
● Lo Cantore, P., Iacobellis, N.S., De Marco, A., Capasso, F. and Senatore, F. (2004). Antibacterial activity of Coriandrum sativum L. and Foeniculum vulgare Miller var. vulgare (Miller) essential oils. Journal of Agricultural and Food Chemistry, 52(26); 7862-7866.
● Mahady, G.B., Pendland, S.L., Stoia, A., Hamill, F.A., Fabricant, D., Dietz, B.M. et al. (2005). In vitro susceptibility of Helicobacter pylori to botanical extracts used traditionally for the treatment of gastrointestinal disorders. Phytotherapy Research, 19(11): 988-991.
● Mohsenzadeh, M. (2007). Evaluation of antibacterial activity of selected Iranian essential oils against Staphylococcus aureus and Escherichia coli in nutrient broth medium. Pakistan Journal of Biological Sciences, 10(20): 3693-3697.
● Namulema, A., Muyonga, J.H. and Kaaya, A.N. (1999). Quality deterioration in frozen Nile perch (Lates niloticus) stored at –13 and –27˚C. Food Research International, 32(2): 151-156.
● Ojagh, S.M., Rezaei, M., Razavi, S.H. and Hosseini, S.M.H. (2010). Effect of chitosan coatings enriched with cinnamon oil on the quality of refrigerated rainbow trout. Food Chemistry, 120(1): 193-198.
● Oroojalian, F., Kasra-Kermanshahi, R., Azizi, M. and Bassami, M. R. (2010). Phytochemical composition of the essential oils from three Apiaceae species and their antibacterial effects on food-borne pathogens. Food Chemistry, 120(3): 765-770.
● Ozogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M. and Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT-Food Science and Technology, 75: 677-684.
● Patel, S. (2015). Plant essential oils and allied volatile fractions as multifunctional additives in meat and fish-based food products: a review. Food Additives and Contaminants: Part A, 32(7): 1049-1064.
● Rather, M.A., Bilal, A.D., Shahnawaz, N.S., Bilal, A.B. and Qurishi, M.A. (2016). Foeniculum vulgare: A comprehensive review of its traditional use, phytochemistry, pharmacology, and safety. Arabian Journal of Chemistry, 9(2): S1574-S1583.
● Rezaei, A. and Shamloofar, M. (2016). Effect of using nisin and rosemary essential oil on total number of mesophilic bacteria and Staphylococcus bacteria in farmed common carp fillets stored at 4°C. Electronic Journal of Biology: 12(4): 320-327.
● Roby, M.H.H., Sarhan, M.A., Selim, K.A.H. and Khalel, K.I. (2013). Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare L.) and chamomile (Matricaria chamomilla L.). Industrial Crops and Products, 44: 437-445.
● Sallam, K.I. (2007). Antimicrobial and antioxidant effects of sodium acetate, sodium lactate, and sodium citrate in refrigerated sliced salmon. Food Control, 18(5), 566-575.
● Savvaidis, I.N., Skandamis, P., Riganakos, K.A., Panagiotakis, N. and Kontominas, M.G. (2002). Control of natural microbial flora and Listeria monocytogenes in vacuum-packaged trout at 4 and 10 C using irradiation. Journal of Food Protection, 65(3), 515-522
● Sharopov, F., Valiev, A., Satyal, P., Gulmurodov, I., Yusufi, S., Setzer, W.N. et al. (2017). Cytotoxicity of the essential oil of Fennel (Foeniculum vulgare) from Tajikistan. Foods, 6(9): E73.
● Skandamis, P.N. and Nychas, G.J. (2001). Effect of oregano essential oil on microbiological and physicochemical attributes of minced meat stored in air and modified atmospheres. Journal of Applied Microbiology, 91(6): 1011-1022.
● Smaoui, S., Hsouna, A.B., Lahmar, A., Ennouri, K., Mtibaa-Chakchouk, A., Sellem, I. et al. (2016). Bio-preservative effect of the essential oil of the endemic Mentha piperita used alone and in combination with BacTN635 in stored minced beef meat. Meat Science, 117: 196-204.
● Solomakos, N., Govaris, A., Koidis, P. and Botsoglou, N. (2008). The antimicrobial effect of thyme essential oil, nisin, and their combination against Listeria monocytogenes in minced beef during refrigerated storage. Food Microbiology, 25(1): 120-127.
● Villarini, M., Pagiotti, R., Dominici, L., Fatigoni, C., Vannini, S., Levorato, S. et al. (2014). Investigation of the cytotoxic, genotoxic, and apoptosis-inducing effects of estragole isolated from fennel (Foeniculum vulgare). Journal of Natural Products, 77(4): 773–778.
● Wu, X. and Su, Y. (2014). Growth of Staphylococcus aureus and enterotoxin production in pre-cooked tuna meat. Food Control, 42: 63-70.
● Zolfaghari, M., Shabanpour, B. and Falahzadeh, S. (2011). Study of trend of chemical and microbial changes of rainbow trout (Oncorhynchus mykiss) to determine its optimum shelf-life during storage in refrigerator temperature (4°C). Journal of Fisheries (Iranian Journal of Natural Resources), 64 (2), 107-119. [In Persian]
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● Abdollahi, M., Rezaei, M. and Farzi, G. (2014). Influence of chitosan/clay functional bionanocomposite activated with rosemary essential oil on the shelf life of fresh silver carp. International Journal of Food Science and Technology, 49(3): 811-818.
● Abdollahzadeh, E., Rezaei, M. and Hosseini, H. (2014). Antibacterial activity of plant essential oils and extracts: The role of thyme essential oil, nisin, and their combination to control Listeria monocytogenes inoculated in minced fish meat. Food Control, 35(1): 177-183.
● AOAC, (2002). Official Methods of Analysis of the Association of the Official Analytical Chemists. Association of Official Analytical Chemists, (14th ed.), Washington, DC.
● AOAC, (2005). Official methods of analysis of the association of the official analytical chemists. Association of Official Analytical Chemists, (17th ed.), Washington, DC.
● Arashisar, S., Hisar, O., Kaya, M. and Yanik, T. (2004). Effects of modified atmosphere and vacuum packaging on microbiological and chemical properties of rainbow trout (Oncorynchus mykiss) fillets. International Journal of Food Microbiology, 97(2): 209-214.
● Bellik,Y. (2014). Total antioxidant activity and antimicrobial potency of the essential oil and oleoresin of Zingiber officinale Roscoe. Asian Pacific Journal of Tropical Disease, 4(1): 40-44.
● Casaburi, A., Nasi, A., Ferrocino, I., Di Monaco, R., Mauriello, G., Villani, F. et al. (2011). Spoilage-related activity of Carnobacterium maltaromaticum strains in air-stored and vacuum-packed meat. Applied and Environmental Microbiology, 77(20): 7382-7393.
● Dadalioǧlu, I. and Evrendilek, G. A. (2004). Chemical compositions and antibacterial effects of essential oils of Turkish oregano (Origanum minutiflorum), bay laurel (Laurus nobilis), Spanish lavender (Lavandula stoechas L.), and fennel (Foeniculum vulgare) on common foodborne pathogens. Journal of Agricultural and Food Chemistry, 52(26): 8255-8260.
● Delbarre-Ladrat, C., Chéret, R., Taylor, R. and Verrez-Bagnis, V. (2006). Trends in postmortem aging in fish: understanding of proteolysis and disorganization of the myofibrillar structure. Critical Reviews in Food Science and Nutrition, 46(5): 409-421.
● Dinges, M.M., Orwin, P.M. and Schlievert, P.M. (2000). Exotoxins of Staphylococcus aureus.Clinical Microbiology Reviews, 13(1): 16-34.
● Fan, W., Chi, Y. and Zhang, S. (2008). The use of a tea polyphenol dip to extend the shelf life of silver carp (Hypophthalmicthys molitrix) during storage in ice. Food Chemistry, 108(1): 148-153.
● Gheisari, H.M. and Ranjbar, V.R. (2012). Antioxidative and antimicrobial effects of garlic in ground camel meat. Turkish Journal of Veterinary and Animal Sciences, 36(1): 13-20.
● Govaris, A., Solomakos, N., Pexara, A. and Chatzopoulou, P.S. (2010). 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, 137(2-3): 175-180.
● Jayasena, D.D. and Jo, Ch. (2013). Essential oils as potential antimicrobial agents in meat and meat products: A review. Trends in Food Science and Technology, 34(2): 96-108.
● Kachele, R., Zhang, M., Gao, Z. and Adhikari, B. (2017). Effect of vacuum packaging on the shelf-life of silver carp (Hypophthalmichthys molitrix) fillets stored at 4° C. LWT-Food Science and Technology, 80: 163-168.
●Kim, Y.B., Seo, K.W., Jeon, H.Y., Lim, S.K. and Lee, Y.J. (2018). Characteristics of the antimicrobial resistance of Staphylococcus aureus isolated from chicken meat produced by different integrated broiler operations in Korea. Poultry Science, 97(3): 962-969.
● Kvenberg J.E. (1991). Nonindigenous Bacterial Pathogens, In: Ward D.R. and Hackney, C. (Editors), Microbiology of Marine Food Products, Springer, Boston, MA, pp 267-284.
● Kwon, Y.S., Choi, W.G., Kim, W.J., cKim, W.K., Kim, M.J., Kang, W.H., et al. (2002). Antimicrobial constituents of Foeniculum vulgare. Archives of Pharmacal Research, 25(2): 154-157.
● Lo Cantore, P., Iacobellis, N.S., De Marco, A., Capasso, F. and Senatore, F. (2004). Antibacterial activity of Coriandrum sativum L. and Foeniculum vulgare Miller var. vulgare (Miller) essential oils. Journal of Agricultural and Food Chemistry, 52(26); 7862-7866.
● Mahady, G.B., Pendland, S.L., Stoia, A., Hamill, F.A., Fabricant, D., Dietz, B.M. et al. (2005). In vitro susceptibility of Helicobacter pylori to botanical extracts used traditionally for the treatment of gastrointestinal disorders. Phytotherapy Research, 19(11): 988-991.
● Mohsenzadeh, M. (2007). Evaluation of antibacterial activity of selected Iranian essential oils against Staphylococcus aureus and Escherichia coli in nutrient broth medium. Pakistan Journal of Biological Sciences, 10(20): 3693-3697.
● Namulema, A., Muyonga, J.H. and Kaaya, A.N. (1999). Quality deterioration in frozen Nile perch (Lates niloticus) stored at –13 and –27˚C. Food Research International, 32(2): 151-156.
● Ojagh, S.M., Rezaei, M., Razavi, S.H. and Hosseini, S.M.H. (2010). Effect of chitosan coatings enriched with cinnamon oil on the quality of refrigerated rainbow trout. Food Chemistry, 120(1): 193-198.
● Oroojalian, F., Kasra-Kermanshahi, R., Azizi, M. and Bassami, M. R. (2010). Phytochemical composition of the essential oils from three Apiaceae species and their antibacterial effects on food-borne pathogens. Food Chemistry, 120(3): 765-770.
● Ozogul, Y., Yuvka, İ., Ucar, Y., Durmus, M., Kösker, A. R., Öz, M. and Ozogul, F. (2017). Evaluation of effects of nanoemulsion based on herb essential oils (rosemary, laurel, thyme and sage) on sensory, chemical and microbiological quality of rainbow trout (Oncorhynchus mykiss) fillets during ice storage. LWT-Food Science and Technology, 75: 677-684.
● Patel, S. (2015). Plant essential oils and allied volatile fractions as multifunctional additives in meat and fish-based food products: a review. Food Additives and Contaminants: Part A, 32(7): 1049-1064.
● Rather, M.A., Bilal, A.D., Shahnawaz, N.S., Bilal, A.B. and Qurishi, M.A. (2016). Foeniculum vulgare: A comprehensive review of its traditional use, phytochemistry, pharmacology, and safety. Arabian Journal of Chemistry, 9(2): S1574-S1583.
● Rezaei, A. and Shamloofar, M. (2016). Effect of using nisin and rosemary essential oil on total number of mesophilic bacteria and Staphylococcus bacteria in farmed common carp fillets stored at 4°C. Electronic Journal of Biology: 12(4): 320-327.
● Roby, M.H.H., Sarhan, M.A., Selim, K.A.H. and Khalel, K.I. (2013). Antioxidant and antimicrobial activities of essential oil and extracts of fennel (Foeniculum vulgare L.) and chamomile (Matricaria chamomilla L.). Industrial Crops and Products, 44: 437-445.
● Sallam, K.I. (2007). Antimicrobial and antioxidant effects of sodium acetate, sodium lactate, and sodium citrate in refrigerated sliced salmon. Food Control, 18(5), 566-575.
● Savvaidis, I.N., Skandamis, P., Riganakos, K.A., Panagiotakis, N. and Kontominas, M.G. (2002). Control of natural microbial flora and Listeria monocytogenes in vacuum-packaged trout at 4 and 10 C using irradiation. Journal of Food Protection, 65(3), 515-522
● Sharopov, F., Valiev, A., Satyal, P., Gulmurodov, I., Yusufi, S., Setzer, W.N. et al. (2017). Cytotoxicity of the essential oil of Fennel (Foeniculum vulgare) from Tajikistan. Foods, 6(9): E73.
● Skandamis, P.N. and Nychas, G.J. (2001). Effect of oregano essential oil on microbiological and physicochemical attributes of minced meat stored in air and modified atmospheres. Journal of Applied Microbiology, 91(6): 1011-1022.
● Smaoui, S., Hsouna, A.B., Lahmar, A., Ennouri, K., Mtibaa-Chakchouk, A., Sellem, I. et al. (2016). Bio-preservative effect of the essential oil of the endemic Mentha piperita used alone and in combination with BacTN635 in stored minced beef meat. Meat Science, 117: 196-204.
● Solomakos, N., Govaris, A., Koidis, P. and Botsoglou, N. (2008). The antimicrobial effect of thyme essential oil, nisin, and their combination against Listeria monocytogenes in minced beef during refrigerated storage. Food Microbiology, 25(1): 120-127.
● Villarini, M., Pagiotti, R., Dominici, L., Fatigoni, C., Vannini, S., Levorato, S. et al. (2014). Investigation of the cytotoxic, genotoxic, and apoptosis-inducing effects of estragole isolated from fennel (Foeniculum vulgare). Journal of Natural Products, 77(4): 773–778.
● Wu, X. and Su, Y. (2014). Growth of Staphylococcus aureus and enterotoxin production in pre-cooked tuna meat. Food Control, 42: 63-70.
● Zolfaghari, M., Shabanpour, B. and Falahzadeh, S. (2011). Study of trend of chemical and microbial changes of rainbow trout (Oncorhynchus mykiss) to determine its optimum shelf-life during storage in refrigerator temperature (4°C). Journal of Fisheries (Iranian Journal of Natural Resources), 64 (2), 107-119. [In Persian]