Evaluation of antimicrobial effects of aqueous and alcoholic extracts of Spirulina platensis in UF white cheese
Subject Areas :
Food Hygiene
E. Zanganeh
1
(Ph.D Graduate of Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran)
H. Mirzaei
2
(Associate Professor, Department of Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran)
S.M. Jafari
3
(Department of Food Materials and Process Design Engineering, Gorgan University of Agricultural Science and Natural Resources, Gorgan, Iran)
M. R. Afshar Mogaddam
4
(Assistant Professor, Food and Drug Safety Research Center, Tabriz University of Medical Sciences, Tabriz, Iran; Pharmaceutical Analysis Research Center, Tabriz University of Medical Sciences, Tabriz, Irann)
َA. Javadi
5
(Professor, Department of Food Hygiene, Faculty of Veterinary Medicine, Tabriz Medical Sciences Branch, Islamic Azad University, Tabriz, Iran)
Received: 2022-08-08
Accepted : 2022-09-01
Published : 2022-11-22
Keywords:
Extract,
Natural preservatives,
UF white cheese,
Spirulina platensis,
Antimicrobial Effects,
Abstract :
One of the most widely used cheeses in Iran is UF white cheese. The presence of nutrients in different types of cheese, make that susceptible to the growth of various microorganisms. Therefore, the use of preservatives to maintain the quality of this high-consumption dairy product is inevitable. In this study, the effect of concentrations of 0.3 and 0.5% aqueous and methanolic extracts of Spirulina platensis on growth inhibition of Listeria monocytogenes, Staphylococcus aureus and Escherichia coli and also the effect of these extracts in preventing the growth of A.flavus in the UF white cheese has been investigated during 60 days of storage of the product in the refrigerator. In addition, the effect of extracts on texture, taste, color and overall acceptance of the product was evaluated. According to the results, a significant inhibitory effect (p≤0.05) of concentrations of 0.3 and 0.5 aqueous and methanolic extracts was observed on Listeria monocytogenes and Escherichia coli from the 15th day of the storage period and on Staphylococcus aureus from the 30th day of the storage period. The antibacterial effect of 0.5 concentration of methanolic extract was significantly higher than other treatments (p≤0.05). All treatments had a significant antifungal effect on Aspergillus flavus strains (p≤0.05). According to the results of the present research, the used extracts did not have a significant adverse effect on the sensory characteristics of the cheese samples, although the concentration of 0.5 methanolic extract insignificantly decreased the quality of the sensory characteristics of the cheese samples. In general, it can be said that concentrations of 0.5 aqueous extract and 0.3 concentration of methanolic extract of Spirulina platensis can be used as natural preservatives in UF white cheese.
References:
Abedin, R.M. and Taha, H.M. (2008). Antibacterial and antifungal activity of cyanobacteria and green microalgae. Evaluation of medium components by Plackett-Burman design for antimicrobial activity of Spirulina platensis. Global Journal of Biotechnology and Biochemistry, 3(1): 22-31.
Adigüzel, A., Güllüce, M., Şengül, M., Öğütcü, H., Şahin, F. and Karaman, İ. (2005). Antimicrobial effects of Ocimum basilicum (Labiatae) extract. Turkish Journal of Biology, 29(3): 155-160.
Alizadeh, M., Hamedi, M. and Khosroshahi, A. (2006). Modeling of proteolysis and lipolysis in Iranian white brine cheese. Food Chemistry, 97(2): 294-301.
Azizkhani, M., Tooryan, F. and Boreiry, M. (2016). Effects of Ocimum basilicum and Salvia sclarea essential oils on Listeria monocytogenes and Aspergillus flavus in Iranian white cheese. Iranian Food Science and Technology Research Journal, 12(2): 286-295. [In Persian]
Banjara, N., Suhr, M. J. and Hallen-Adams, H. E. (2015). Diversity of yeast and mold species from a variety of cheese types. Current Microbiology, 70(6): 792-800.
Baydar, H., Sağdiç, O., Özkan, G. and Karadoğan, T. (2004). Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control, 15(3): 169-172.
Behbahani, B.A., Tabatabaei-Yazdi, F., Shahidi, F. and Mortazavi, A. (2013). Antimicrobial effects of Lavandula stoechas L. and Rosmarinus officinalis L. extracts on Escherichia coli and Staphylococcus aureus. Scientific Journal of Microbiology, 2(1): 15-22.
Behbahani, B.A., Yazdi, F.T., Shahidi, F. and Mohebbi, M. (2014). Antimicrobial effect of the aqueous and ethanolic Avicennia marina extracts on Staphylococcus epidermidis, Streptococcus pyogenes and Pseudomonas aeruginosa" in vitro". Iranian South Medical Journal, 17(5): 879-888. [In Persian]
Beigomi, M., Ghods Rohani, M., Mohammadifar, A., Hashemi, M., Valizadeh, M. and Ghanati, K. (2013). Comparision of textural and sensory characteristics of ultrafiltrated white cheese produced by paneer bad (Witania Coagulans) protease and fungal renet. Journal of Nutrition Sciences and Food Technology, 8(1): 253-262. [In Persian]
Bonyadian, M. and Karim, G. (2002). Study of the effects of some volatile oils of herbs (pennyroyal, peppermint, tarragon, caraway seed and thyme) against E. coli and S. aureus in broth media. Journal of Faculity of Veterinary Medicin of University of Tehran, 57:81-83. [In Persian]
Christ-Ribeiro, A., Graça, C.S., Kupski, L., Badiale-Furlong, E., and de Souza-Soares, L.A. (2019). Cytotoxicity, antifungal and anti mycotoxins effects of phenolic compounds from fermented rice bran and SpirulinaProcess Biochemistry, 80, 190-196.
Chu,W.L. (2012). Biotechnological applications of microalgae. International e-Journal of Science, Medicine and Education, 6 (1): 24-37.
Darderafshi, M., Bahrami, G., Sadeghi, E., Khanahmadi, M., Mohammadi, M. and Mohammadi, R. (2014). The effect of Ferulago angulata essential oil on Staphylococcus aureus during the manufacture and preservation of Iranian white cheese. Iranian Journal of Nutrition Sciences and Food Technology, 8(4): 13-20. [In Persian]
Dorman, H.D. and Deans, S.G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88(2): 308-316.
Duffy, C.F. and Power, R.F. (2001). Antioxidant and antimicrobial properties of some Chinese plant extracts. International Journal of Antimicrobial Agents, 17(6): 527-529.
El-Baz, F., El-Senousy, W., El-Sayed, A. and Kamel, M. (2013). In vitro antiviral and antimicrobial activities of Spirulina platensis extract. Journal of Applied Pharmaceutical Science, 3(12): 52-56.
Fadaei Noghani, V., Mazinani, S., Khosravi Darani, K., Islami Meshkanani, A., and Mirzadeh, A. (2014). The effect of Spirulina platensis biomass powder on some physicochemical and sensory characteristics of probiotic Iranian white cheese containing oregano powder prepared by ultra-refining method. Innovative Food Science and Technologies, 2(7): 1-10. [In Persian]
Farshbaf Derhami, S., Giyami Rad, M., Mahmoudi, R. and Asadi Nadari, M.R. (2018). Comparaitive Studies of Antibacterial Activity of Extracts Nasturtium Officinale and Coriandrum Sativum Against Some of Pathogenic Bacteria. Journal of Veterinary Microbiology, 13(2), 47-55. [In Persian]
Fischer, A.J., Bayer, D.E., Carriere, M.D., Ateh, C.M. and Yim, K.O. (2000). Mechanisms of resistance to bispyribac-sodium in an Echinochloa phyllopogon accession. Pesticide Biochemistry and Physiology, 68(3): 156-165.
Gammariello, D., Conte, A., Attanasio, M. and Del Nobile, M.A. (2010). Study on the combined effects of essential oils on microbiological quality of Fior di Latte cheese. The Journal of Dairy Research, 77(2): 144-150.
Gandomi, H., Misaghi, A., Basti, A.A., Bokaei, S., Khosravi, A., Abbasifar, A. and Javan, A.J. (2009). Effect of Zataria multiflora essential oil on growth and aflatoxin formation by Aspergillus flavus in culture media and cheese. Food and Chemical Toxicology, 47(10): 2397-2400.
Ghalem, B.R. and Mohamed, B. (2008). Antibacterial activity of leaf essential oils of Eucalyptus globulus and Eucalyptus camaldulensis. African Journal of Pharmacy and Pharmacology, 2(10): 211-215.
Hosseini, M., Habibi Najafi, M., Mohebbi, M. (2013). Assessment of physico-chemical and sensory properties of imitation cheese containing whey protein concentrate and enzyme-modified Lighvan cheese, Iranian Journal of Nutrition Sciences and Food Technology, 8(2): 91-102.
Hussain, A.I., Anwar, F., Sherazi, S.T.H. and Przybylski, R. (2008). Chemical composition, antioxidant and antimicrobial activities of basil (Ocimum basilicum) essential oils depends on seasonal variations. Food Chemistry, 108(3): 986-995.
Islam, M., Barua, S., Das, S., Khan, M. and Ahmed, A. (2008). Antibacterial activity of some indigenous medicinal plants. Journal of Soil and Nature, 2(3): 26-28.
Karim, G. (2003). Microbial Examination of Foods. 4nd Edition, University of Tehran Publication, pp. 65. [In Persian]
Kedia, A., Prakash, B., Mishra, P. K. and Dubey, N. (2014). Antifungal and antiaflatoxigenic properties of Cuminum cyminum (L.) seed essential oil and its efficacy as a preservative in stored commodities. International journal of Food Microbiology, 168, 1-7.
Lianou, A., Panagoun, E.Z. and Nychas, J.E. (2016). Microbiological spoilage of foods and beverages, In: Kilcast, D. and Subramaniam, P. (Editors), Food and beverage stability and shelf life, 2nd Edition, Woodhead Publishing, pp. 3-28.
Mahmoudi, R., Ehsani, A. and Zare, P. (2012). Phytochemical, antibacterial and antioxidant properties of Cuminum cyminum L. essential oil. Journal of Food Research, 22(3): 311-322. [In Persian]
Manafi, M, and Mazaheri M. (2014). Production of analogue UF white cheese by replacement of milk fat with margarine. Journal of Food Research, 23(4): 545-552. [In Persian]
Neyestani, T. (2007). The inhibitory effects of black and green teas (Camellia sinensis) on growth of pathogenic Escherichia coli in vitro. Iranian Journal of Nutrition Sciences and Food Technology, 1(3): 33-38. [In Persian]
Rasouli, F., Berenji, S. and Lavasani, A.S. (2017). Optimization of Traditional Iranian Ice Cream Formulation Enriched with Spirulina Using Response Surface Methodology. Journal of Food Technology and Nutrition, 14(3): 15-28. [In Persian]
Priya, S. (2012). Analysis of value- added biochemical compounds and antimicrobial activity of green algae Chlorella vulgaris. Journal of Chemical and Pharmaceutical Research, 4(5): 2577-2579.
Sajilata, M., Singhal, R. and Kamat, M. (2008). Fractionation of lipids and purification of γ-linolenic acid (GLA) from Spirulina platensis. Food Chemistry, 109(3): 580-586.
Saranraj, P. and Sivasakthi, S. (2014). Spirulina platensis–food for future: a review. Asian Journal of Pharmaceutical Science and Technology, 4(1): 26-33.
Sengul, M., Ercisli, S., Yildiz, H., Gungor, N., Kavaz, A. and Çetin, B. (2011). Antioxidant, antimicrobial activity and total phenolic content within the aerial parts of Artemisia absinthum, Artemisia santonicum and Saponaria officinalis. Iranian journal of Pharmaceutical Research, 10(1): 49-56.
Shahidi, F. (2004). Functional Foods: their role in health promotion and disease prevention. Journal of Food Science, 69(5): 146-149.
Shariatifar, N., Pirali, M., Hamedani, Moazzen, M., Ahmadloo, M. and Yazdani, D. (2019). Study of the Antimicrobial Effects of Aqueous Extract of Olea europaea, Solanum nigrum, Artemisia sieberi, Teucrium polium, Glycyrrhiza glabra on some Food-borne Pathogenic Bacteria. Journal of Medicinal Plants, 18(72): 264-273. [In Persian]
Souza, M.M.D., Prietto, L., Ribeiro, A.C., Souza, T.D.D., and Badiale-Furlong, E. (2011). Assessment of the antifungal activity of Spirulina platensis phenolic extract against Aspergillus flavus. Ciência e Agrotecnologia, 35, 1050-1058.
Usharani, G., Srinivasan, G., Sivasakthi, S. and Saranraj, P. (2015). Antimicrobial activity of Spirulina platensis solvent extracts against pathogenic bacteria and fungi. Advances in Biological Research, 9(5): 292-298.
Wan, J., Zhong, S., Schwarz, P., Chen, B. and Rao, J. (2019). Physical properties, antifungal and mycotoxin inhibitory activities of five essential oil nanoemulsions: Impact of oil compositions and processing parameters. Food Chemistry, 291: 199-206.
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Abedin, R.M. and Taha, H.M. (2008). Antibacterial and antifungal activity of cyanobacteria and green microalgae. Evaluation of medium components by Plackett-Burman design for antimicrobial activity of Spirulina platensis. Global Journal of Biotechnology and Biochemistry, 3(1): 22-31.
Adigüzel, A., Güllüce, M., Şengül, M., Öğütcü, H., Şahin, F. and Karaman, İ. (2005). Antimicrobial effects of Ocimum basilicum (Labiatae) extract. Turkish Journal of Biology, 29(3): 155-160.
Alizadeh, M., Hamedi, M. and Khosroshahi, A. (2006). Modeling of proteolysis and lipolysis in Iranian white brine cheese. Food Chemistry, 97(2): 294-301.
Azizkhani, M., Tooryan, F. and Boreiry, M. (2016). Effects of Ocimum basilicum and Salvia sclarea essential oils on Listeria monocytogenes and Aspergillus flavus in Iranian white cheese. Iranian Food Science and Technology Research Journal, 12(2): 286-295. [In Persian]
Banjara, N., Suhr, M. J. and Hallen-Adams, H. E. (2015). Diversity of yeast and mold species from a variety of cheese types. Current Microbiology, 70(6): 792-800.
Baydar, H., Sağdiç, O., Özkan, G. and Karadoğan, T. (2004). Antibacterial activity and composition of essential oils from Origanum, Thymbra and Satureja species with commercial importance in Turkey. Food Control, 15(3): 169-172.
Behbahani, B.A., Tabatabaei-Yazdi, F., Shahidi, F. and Mortazavi, A. (2013). Antimicrobial effects of Lavandula stoechas L. and Rosmarinus officinalis L. extracts on Escherichia coli and Staphylococcus aureus. Scientific Journal of Microbiology, 2(1): 15-22.
Behbahani, B.A., Yazdi, F.T., Shahidi, F. and Mohebbi, M. (2014). Antimicrobial effect of the aqueous and ethanolic Avicennia marina extracts on Staphylococcus epidermidis, Streptococcus pyogenes and Pseudomonas aeruginosa" in vitro". Iranian South Medical Journal, 17(5): 879-888. [In Persian]
Beigomi, M., Ghods Rohani, M., Mohammadifar, A., Hashemi, M., Valizadeh, M. and Ghanati, K. (2013). Comparision of textural and sensory characteristics of ultrafiltrated white cheese produced by paneer bad (Witania Coagulans) protease and fungal renet. Journal of Nutrition Sciences and Food Technology, 8(1): 253-262. [In Persian]
Bonyadian, M. and Karim, G. (2002). Study of the effects of some volatile oils of herbs (pennyroyal, peppermint, tarragon, caraway seed and thyme) against E. coli and S. aureus in broth media. Journal of Faculity of Veterinary Medicin of University of Tehran, 57:81-83. [In Persian]
Christ-Ribeiro, A., Graça, C.S., Kupski, L., Badiale-Furlong, E., and de Souza-Soares, L.A. (2019). Cytotoxicity, antifungal and anti mycotoxins effects of phenolic compounds from fermented rice bran and SpirulinaProcess Biochemistry, 80, 190-196.
Chu,W.L. (2012). Biotechnological applications of microalgae. International e-Journal of Science, Medicine and Education, 6 (1): 24-37.
Darderafshi, M., Bahrami, G., Sadeghi, E., Khanahmadi, M., Mohammadi, M. and Mohammadi, R. (2014). The effect of Ferulago angulata essential oil on Staphylococcus aureus during the manufacture and preservation of Iranian white cheese. Iranian Journal of Nutrition Sciences and Food Technology, 8(4): 13-20. [In Persian]
Dorman, H.D. and Deans, S.G. (2000). Antimicrobial agents from plants: antibacterial activity of plant volatile oils. Journal of Applied Microbiology, 88(2): 308-316.
Duffy, C.F. and Power, R.F. (2001). Antioxidant and antimicrobial properties of some Chinese plant extracts. International Journal of Antimicrobial Agents, 17(6): 527-529.
El-Baz, F., El-Senousy, W., El-Sayed, A. and Kamel, M. (2013). In vitro antiviral and antimicrobial activities of Spirulina platensis extract. Journal of Applied Pharmaceutical Science, 3(12): 52-56.
Fadaei Noghani, V., Mazinani, S., Khosravi Darani, K., Islami Meshkanani, A., and Mirzadeh, A. (2014). The effect of Spirulina platensis biomass powder on some physicochemical and sensory characteristics of probiotic Iranian white cheese containing oregano powder prepared by ultra-refining method. Innovative Food Science and Technologies, 2(7): 1-10. [In Persian]
Farshbaf Derhami, S., Giyami Rad, M., Mahmoudi, R. and Asadi Nadari, M.R. (2018). Comparaitive Studies of Antibacterial Activity of Extracts Nasturtium Officinale and Coriandrum Sativum Against Some of Pathogenic Bacteria. Journal of Veterinary Microbiology, 13(2), 47-55. [In Persian]
Fischer, A.J., Bayer, D.E., Carriere, M.D., Ateh, C.M. and Yim, K.O. (2000). Mechanisms of resistance to bispyribac-sodium in an Echinochloa phyllopogon accession. Pesticide Biochemistry and Physiology, 68(3): 156-165.
Gammariello, D., Conte, A., Attanasio, M. and Del Nobile, M.A. (2010). Study on the combined effects of essential oils on microbiological quality of Fior di Latte cheese. The Journal of Dairy Research, 77(2): 144-150.
Gandomi, H., Misaghi, A., Basti, A.A., Bokaei, S., Khosravi, A., Abbasifar, A. and Javan, A.J. (2009). Effect of Zataria multiflora essential oil on growth and aflatoxin formation by Aspergillus flavus in culture media and cheese. Food and Chemical Toxicology, 47(10): 2397-2400.
Ghalem, B.R. and Mohamed, B. (2008). Antibacterial activity of leaf essential oils of Eucalyptus globulus and Eucalyptus camaldulensis. African Journal of Pharmacy and Pharmacology, 2(10): 211-215.
Hosseini, M., Habibi Najafi, M., Mohebbi, M. (2013). Assessment of physico-chemical and sensory properties of imitation cheese containing whey protein concentrate and enzyme-modified Lighvan cheese, Iranian Journal of Nutrition Sciences and Food Technology, 8(2): 91-102.
Hussain, A.I., Anwar, F., Sherazi, S.T.H. and Przybylski, R. (2008). Chemical composition, antioxidant and antimicrobial activities of basil (Ocimum basilicum) essential oils depends on seasonal variations. Food Chemistry, 108(3): 986-995.
Islam, M., Barua, S., Das, S., Khan, M. and Ahmed, A. (2008). Antibacterial activity of some indigenous medicinal plants. Journal of Soil and Nature, 2(3): 26-28.
Karim, G. (2003). Microbial Examination of Foods. 4nd Edition, University of Tehran Publication, pp. 65. [In Persian]
Kedia, A., Prakash, B., Mishra, P. K. and Dubey, N. (2014). Antifungal and antiaflatoxigenic properties of Cuminum cyminum (L.) seed essential oil and its efficacy as a preservative in stored commodities. International journal of Food Microbiology, 168, 1-7.
Lianou, A., Panagoun, E.Z. and Nychas, J.E. (2016). Microbiological spoilage of foods and beverages, In: Kilcast, D. and Subramaniam, P. (Editors), Food and beverage stability and shelf life, 2nd Edition, Woodhead Publishing, pp. 3-28.
Mahmoudi, R., Ehsani, A. and Zare, P. (2012). Phytochemical, antibacterial and antioxidant properties of Cuminum cyminum L. essential oil. Journal of Food Research, 22(3): 311-322. [In Persian]
Manafi, M, and Mazaheri M. (2014). Production of analogue UF white cheese by replacement of milk fat with margarine. Journal of Food Research, 23(4): 545-552. [In Persian]
Neyestani, T. (2007). The inhibitory effects of black and green teas (Camellia sinensis) on growth of pathogenic Escherichia coli in vitro. Iranian Journal of Nutrition Sciences and Food Technology, 1(3): 33-38. [In Persian]
Rasouli, F., Berenji, S. and Lavasani, A.S. (2017). Optimization of Traditional Iranian Ice Cream Formulation Enriched with Spirulina Using Response Surface Methodology. Journal of Food Technology and Nutrition, 14(3): 15-28. [In Persian]
Priya, S. (2012). Analysis of value- added biochemical compounds and antimicrobial activity of green algae Chlorella vulgaris. Journal of Chemical and Pharmaceutical Research, 4(5): 2577-2579.
Sajilata, M., Singhal, R. and Kamat, M. (2008). Fractionation of lipids and purification of γ-linolenic acid (GLA) from Spirulina platensis. Food Chemistry, 109(3): 580-586.
Saranraj, P. and Sivasakthi, S. (2014). Spirulina platensis–food for future: a review. Asian Journal of Pharmaceutical Science and Technology, 4(1): 26-33.
Sengul, M., Ercisli, S., Yildiz, H., Gungor, N., Kavaz, A. and Çetin, B. (2011). Antioxidant, antimicrobial activity and total phenolic content within the aerial parts of Artemisia absinthum, Artemisia santonicum and Saponaria officinalis. Iranian journal of Pharmaceutical Research, 10(1): 49-56.
Shahidi, F. (2004). Functional Foods: their role in health promotion and disease prevention. Journal of Food Science, 69(5): 146-149.
Shariatifar, N., Pirali, M., Hamedani, Moazzen, M., Ahmadloo, M. and Yazdani, D. (2019). Study of the Antimicrobial Effects of Aqueous Extract of Olea europaea, Solanum nigrum, Artemisia sieberi, Teucrium polium, Glycyrrhiza glabra on some Food-borne Pathogenic Bacteria. Journal of Medicinal Plants, 18(72): 264-273. [In Persian]
Souza, M.M.D., Prietto, L., Ribeiro, A.C., Souza, T.D.D., and Badiale-Furlong, E. (2011). Assessment of the antifungal activity of Spirulina platensis phenolic extract against Aspergillus flavus. Ciência e Agrotecnologia, 35, 1050-1058.
Usharani, G., Srinivasan, G., Sivasakthi, S. and Saranraj, P. (2015). Antimicrobial activity of Spirulina platensis solvent extracts against pathogenic bacteria and fungi. Advances in Biological Research, 9(5): 292-298.
Wan, J., Zhong, S., Schwarz, P., Chen, B. and Rao, J. (2019). Physical properties, antifungal and mycotoxin inhibitory activities of five essential oil nanoemulsions: Impact of oil compositions and processing parameters. Food Chemistry, 291: 199-206.
