The Effect of Alginate Microcapsules of Linseed and Black Seed Oil on the Microbiological and Sensorial Properties of Chocolate Ganache During Storage

Document Type : Research Article


Department of Food Science and Technology, Faculty of Biological Science, North Tehran Branch, Islamic Azad University, Tehran, I.R. IRAN


The application of bioactive natural oils in the food industry is limited due to their instability and poor solubility in hydrophilic media. This study aimed to investigate the effect of alginate microcapsules of linseed and black oil on microbial and sensorial properties of chocolate ganache during 28 days of storage. The results showed that both evaluated oils had considerable antibacterial effects against tested microorganisms (Salmonella Typhimurium, Escherichia coli, Staphylococcus aureus, Aspergillus niger, and Candida albicans) and gram-negative than gram-positive bacteria were more resistant to linseed oil. Therefore, Black seed oil showed higher antibacterial activity and both linseed and black seed oil microcapsules had lower antibacterial effects than their free form. The incorporation of encapsulated oils in chocolate ganache was not significantly different from the control samples. Although, the free form has shown higher antibacterial activity, due to the characteristics of protecting the bioactivity of oils from undesirable conditions, controlled release, and marketability of the product, loading the oils in an alginate bead is a suitable way for the application of black seed and linseed oil in food products.


Main Subjects

[1] Li X., Deng J., Shen S., Li T., Yuan M., Yang R., Antioxidant Activities and Functional Properties
of Enzymatic Protein Hydrolysates from Defatted Camellia Oleifera Seed Cake
, J. Food Sci. Technol., 52: 5681-90 (2015).
[3] Astrup A., Dyerberg J., Elwood P., Hermansen K., Hu F.B., Jakobsen M.U., et al., The Role of Reducing Intakes of Saturated Fat in the Prevention of Cardiovascular Disease: Where Does the Evidence Stand In 2010?, Am. J. Clin. Nutr., 93: 684-8 (2011).
[4] Mann J., Truswell A.S., "Essentials of Human Nutrition", Oxford University Press (2017).
[5] Khattab R., Zeitoun M., Quality Evaluation of Flaxseed Oil Obtained by Different Extraction Techniques, LWT Food Sci. Technol., 53: 338–345 (2013).
[6] Kajla P., Sharma A., Sood D.R.,  Flaxseed—A Potential Functional Food Source, J. Food Sci. Technol., 52:1857-71 (2015).
[7] Rajesha J., Rao A.R., Madhusudhan B., Karunakumar M., Antibacterial Properties of Secoisolariciresinol Diglucoside Isolated from Indian Flaxseed Cultivars, Curr. Trends Biotechnol. Pharm., 4: 551-560 (2010).
[8] Alijabre S., Alakloby O., Randhawa M., Dermatological Effect of Nagellasative, J. Dermatol. Dermatol. Surg., 19: 92-8 (2015).
[9] Kokoska L., Havlik J., Valterova I., Sovova H., Sajfrtova M., Jankovska I., Comparison of Chemical Composition and Antibacterial Activity of Nigella Sativa Seed Essential Oils Obtained by Different Extraction Methods, J. Food Protect., 71:2475-80 (2008).
[10] Agbaria R., Gabarin A., Dahan A., Ben-Shabat S., Anticancer Activity of Nigella Sativa (Black Seed) and its Relationship with the Thermal Processing and Quinone Composition of the Seed, Drug Des. Devel. Ther., 9:3119 (2015).
[11] Piornos J.A., Burgos-Díaz C., Morales E., Rubilar M., Acevedo F., Highly Efficient Encapsulation of Linseed Oil into Alginate/Lupin Protein Beads: Optimization of the Emulsion Formulation, Food Hydrocoll., 63:139-48 (2017).
[12] Nakajima M., Wang Z., Chaudhry Q., Park H.J., Juneja LR., Nano-Science-Engineering-Technology Applications to Food and Nutrition, J. Nutr. Sci. Vitaminol., 61:S180-S2 (2015).
[13] Azad AK., Al-Mahmood SMA., Chatterjee B., Wan Sulaiman WMA., Elsayed TM., Doolaanea AA,. Encapsulation of Black Seed Oil in Alginate Beads as a Ph-Sensitive Carrier for Intestine-Targeted Drug Delivery: in Vitro, in Vivo and Ex Vivo Study, Pharmaceutics, 12: 219 (2020).
[14] Chan E-S., Lee BB., Ravindra P., Poncelet D., Prediction Models for Shape and Size of Ca-Alginate Macrobeads Produced Through Extrusion–Dripping Method, J. Colloid Interface Sci., 338:63-72 (2009).
[15] Wang H., Gong X., Guo X., Liu C., Fan YY., Zhang J., et al., Characterization, Release, and Antioxidant Activity of Curcumin-Loaded Sodium Alginate/Zno Hydrogel Beads, Int. J. Biol. Macromol., 121:1118-25 (2019).
[17] Vickers NJ., Animal Communication: When I’m Calling You, Will You Answer Too?, Curr. Biol., 27 (14): 713-715 (2017).
[20] Özcan M.M., Al-Juhaimi F.Y., Ahmed I.A.M., Osman M.A., Gassem M.A,. Effect of Soxhlet and Cold Press Extractions on the Physico-Chemical Characteristics of Roasted and Non-Roasted Chia Seed Oils, J. Food Meas. Charact., 13: 648-55 (2019).
[21] Horwitz W., Official Methods of Analysis of AOAC International. Volume I, “Agricultural Chemicals, Contaminants, Drugs”, Edited by William Horwitz: Gaithersburg (Maryland): AOAC International (2010).
[23] Zhang ZS., Wang L.J., Li D., Jiao S.S., Chen X.D., Mao Z.H., Ultrasound-Assisted Extraction of Oil from Flaxseed, Sep. Purif. Technol., 62:192-8 (2008).
[25] Huang X., Kakuda Y., Cui W., Hydrocolloids in Emulsions: Particle Size Distribution and Interfacial Activity, Food Hydrocoll., 15: 533-42 (2001).
[27] Oroojalian F., Kasra-Kermanshahi R., Azizi M., Bassami M.R., Phytochemical Composition of the Essential Oils from Three Apiaceae Species and Their Antibacterial Effects on Food-Borne Pathogens, Food Chem., 120: 765-70 (2010).
[29] Ivanov D.S., Čolović R.R., Lević J.D., Sredanović S.A., Optimization of Supercritical Fluid Extraction of Linseed Oil Using RSM, Eur. J. Lipid Sci. Technol., 114: 807-15 (2012).
[30] Kasote D.M., Badhe Y.S., Hegde M.V., Effect of Mechanical Press Oil Extraction Processing on Quality of Linseed Oil, Ind. Crops Prod., 42: 3-10 (2013).
[31] Mohammed N.K., Manap A., Yazid M., Tan C.P., Muhialdin BJ., Alhelli AM., et al,. The Effects of Different Extraction Methods on Antioxidant Properties, Chemical Composition, and Thermal Behavior of Black Seed (Nigella Sativa L.) Oil, Evid.-Based Complement. Altern. Med., 1-11 (2016).
[32] Khoddami A., Ghazali H.M., Yassoralipour A., Ramakrishnan Y., Ganjloo A., Physicochemical Characteristics of Nigella Seed (Nigella Sativa L.) Oil as Affected by Different Extraction Methods, J. Am. Oil Chem. Soc., 88: 533-40 (2011).
[33] Nykter M., Kymäläinen H.R., Gates F., Quality Characteristics of Edible Linseed Oil, Agric. Food Sci., 15: 402-13 (2006).
[35] Bayrak A., Kiralan M., Ipek A., Arslan N., Cosge B., Khawar K., Fatty Acid Compositions of Linseed (Linum Usitatissimum L.) Genotypes of Different Origin Cultivated in Turkey, Biotechnol. Biotechnol. Equip., 24: 1836-42 (2010).
[37] Kiralan M., Özkan G., Bayrak A., Ramadan MF., Physicochemical Properties and Stability of Black Cumin (Nigella Sativa) Seed Oil as Affected by Different Extraction Methods, Ind. Crops. Prod., 57: 52-8 (2014).
[40] Cheikh-Rouhou S., Besbes S., Hentati B., Blecker C., Deroanne C., Attia H.,  Nigella Sativa L.: Chemical Composition and Physicochemical Characteristics of Lipid Fraction, Food Chem., 101: 673-81 (2007).
[44] Corstens M.N., Berton-Carabin C.C., Elichiry-Ortiz P.T., Hol K., Troost F.J., Masclee A.A., et al., Emulsion-Alginate Beads Designed to Control In Vitro Intestinal Lipolysis: Towards Appetite Control, J. Func. Food., 34: 319-28 (2017).
[45] Mattazi N., Farah A., Fadil M., Chraibi M., Benbrahim K., Essential Oils Analysis and Antibacterial Activity of the Leaves of Rosmarinus Officinalis, Salvia Officinalis and Mentha Piperita Cultivated in Agadir (Morocco), Int. J. Pharm. Pharm. Sci., 7:73-9 (2015).
[47] Mohammed S.J., Amin H.H., Aziz S.B., Sha A.M., Hassan S., Abdul Aziz J.M., et al., Structural Characterization, Antimicrobial Activity, and in Vitro Cytotoxicity Effect of Black Seed Oil, Evid.-based Complement. Altern. Med., 1-10 (2019).
[48] Nair M.K.M., Vasudevan P., Venkitanarayanan K., Antibacterial Effect of Black Seed Oil on Listeria Monocytogenes, Food Control, 16: 395-8 (2005).
[49] Woo C.C., Loo S.Y., Gee V., Yap C.W., Sethi G., Kumar A.P., et al., Anticancer Activity of Thymoquinone in Breast Cancer Cells: Possible Involvement of PPAR-Γ Pathway, Biochem. Pharmacol., 82: 464-75 (2011).
[50] Al-Mathkhury H.J.F., Al-Dhamin A.S., Al-Taie K.L., Antibacterial and Antibiofilm Activity of Flaxseed Oil, Iraqi J. Sci., 57: 1086-95 (2016).
[51] Heyman H.M., Senejoux F., Seibert I., Klimkait T., Maharaj V.J., Meyer J.J.M., Identification of Anti-HIV Active Dicaffeoylquinic-and Tricaffeoylquinic Acids in Helichrysum Populifolium by NMR-Based Metabolomic Guided Fractionation, Fitoterapia, 103:155-64 (2015).
[52] Duffy C.F., Power R.F., Antioxidant and Antimicrobial Properties of Some Chinese Plant Extracts, Int. J. Antimicrob., 17: 527-9 (2001).
[53] Amin T., Thakur M., A Comparative Study on Proximate Composition, Phytochemical Screening, Antioxidant and Antimicrobial Activities of Linum Usitatisimum L.(Flaxseeds), Int. J. Curr. Microbiol. Appl. Sci., 3: 465-81 (2014).
[54] Georgescu M., Tăpăloagă P.R., Tăpăloagă D., Furnaris F., Ginghină O., Negrei C., et al., Evaluation of Antimicrobial Potential of Nigella Sativa Oil in a Model Food Matrix, Farmacia, 66: 1028-36 (2018).
[55] Adolphe J.L., Whiting S.J., Juurlink B.H., Thorpe L.U., Alcorn J., Health Effects with Consumption of the Flax Lignan Secoisolariciresinol Diglucoside, Br. J. Nutr., 103: 929-38 (2010).
[57] Torpol K., Sriwattana S., Sangsuwan J., Wiriyacharee P., Prinyawiwatkul W., Optimising Chitosan–Pectin Hydrogel Beads Containing Combined Garlic and Holy Basil Essential Oils and Their Application as Antimicrobial Inhibitor, Int. Food Sci. Technol., 54: 2064-74 (2019).
[58] Cox S., Mann C., Markham J., Bell H.C., Gustafson J., Warmington J., et al., The Mode of Antimicrobial Action of the Essential Oil of Melaleuca Alternifolia (Tea Tree Oil), J Appl. Microb., 88:170-5 (2000).
[59] Nzeako B., Al-Kharousi Z.S., Al-Mahrooqui Z., Antimicrobial Activities of Clove and Thyme Extracts, Sultan Qaboos Univ. Med. J., 6 (33) (2006).
[60] Radünz M., da Trindade M.L.M., Camargo T.M., Radünz A.L., Borges C.D., Gandra E.A., et al., Antimicrobial and Antioxidant Activity of Unencapsulated and Encapsulated Clove (Syzygium Aromaticum, L.) Essential Oil, Food Chem., 276: 180-6 (2019).
[61] Haggag M.G., Shafaa M.W., Kareem H.S., El-Gamil A.M., El-Hendawy HH., Screening and Enhancement of the Antimicrobial Activity of Some Plant Oils Using Liposomes as Nanoscale Carrier, Bull. Natl. Res. Cent., 45: 1-14 (2021).
[62] Hashim A.F., Hamed S.F., Hamid H.A.A., Abd-Elsalam K.A., Golonka I., Musiał W., et al., Antioxidant and Antibacterial Activities of Omega-3 Rich Oils/Curcumin Nanoemulsions Loaded in Chitosan and Alginate-Based Microbeads, Int. J.Biol. Macromol., 140: 682-96 (2019).
[65] Khalili ST., Mohsenifar A., Beyki M., Zhaveh S., Rahmani-Cherati T., Abdollahi A., et al., Encapsulation of Thyme Essential Oils in Chitosan-Benzoic Acid Nanogel with Enhanced Antimicrobial Activity Against Aspergillus Flavus, LWT-Food Sci. Technol., 60: 502-8 (2015).
[66] Perdones A., Sánchez-González L., Chiralt A., Vargas M., Effect of Chitosan–Lemon Essential Oil Coatings on Storage-Keeping Quality of Strawberry, Postharvest Biol. Technol., 70: 32-41 (2012).
[67] Sangsuwan J., Pongsapakworawat T., Bangmo P., Sutthasupa S., Effect of Chitosan Beads Incorporated with Lavender or Red Thyme Essential Oils in Inhibiting Botrytis Cinerea and Their Application in Strawberry Packaging System, LWT-Food Sci. Technol., 74: 14-20 (2016).