Production of a Novel Functional Fruit Beverage Consisting of Cornelian Cherry Juice and Probiotic Bacteria
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microorganism
2.2. Immobilized Biocatalyst Preparation
2.3. Cornelian Cherry Juice Fermentation
2.4. Microbiological Analysis
2.5. Ethanol and Residual Sugar Analysis
2.6. Organic Acid Analysis
2.7. Total Phenolics
2.8. Consumer Study
2.9. Statistical Analysis
3. Results and Discussion
3.1. Cell Survival
3.2. Ethanol, Organic Acids, and Residual Sugar Concentrations
3.3. Total Phenolics Content (TPC)
3.4. Consumer Study
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Brown, L.; Caligiuri, S.P.B.; Brown, D.; Pierce, G.N. Clinical trials using functional foods provide unique challenges. J. Funct. Foods. 2018, 45, 233–238. [Google Scholar] [CrossRef]
- Perricone, M.; Bevilacqua, A.; Altieri, C.; Sinigaglia, M.; Corbo, R.M. Challenges for the Production of Probiotic Fruit Juices. Beverages 2015, 1. [Google Scholar] [CrossRef]
- Corbo, M.R.; Bevilacqua, A.; Petruzzi, L.; Casanova, F.P.; Sinigaglia, M. Functional Beverages: The Emerging Side of Functional Foods. Compr. Rev. Food Sci. Food Saf. 2014, 13, 1192–1206. [Google Scholar] [CrossRef] [Green Version]
- Santeramo, F.G.; Carlucci, D.; De Devitiis, B.; Seccia, A.; Stasi, A.; Viscecchia, R.; Nardone, G. Emerging trends in European food, diets and food industry. Food Res. Int. 2018, 104, 39–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Menrad, K. Market and marketing of functional food in Europe. J. Food Eng. 2003, 56, 181–188. [Google Scholar] [CrossRef]
- Ye, Q.; Georges, N.; Selomulya, C. Microencapsulation of active ingredients in functional foods: From research stage to commercial food products. Trends Food Sci. Technol. 2018, 78, 167–179. [Google Scholar] [CrossRef]
- Fernandes Pereira, A.L.; Rodrigues, S. Chapter 15—Turning Fruit Juice into Probiotic Beverages. In Fruit Juices; Rajauria, G., Tiwari, B.K., Eds.; Academic Press: San Diego, CA, USA, 2018; pp. 279–287. [Google Scholar] [CrossRef]
- Tripathi, M.K.; Giri, S.K. Probiotic functional foods: Survival of probiotics during processing and storage. J. Funct. Foods 2014, 9, 225–241. [Google Scholar] [CrossRef]
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. J. Funct. Foods 2014, 11, 506–514. [Google Scholar] [CrossRef]
- Joshi, D.; Roy, S.; Banerjee, S. Chapter 19—Prebiotics: A Functional Food in Health and Disease. In Natural Products and Drug Discovery; Mandal, S.C., Mandal, V., Konishi, T., Eds.; Elsevier: Amsterdam, The Netherlands, 2018; pp. 507–523. [Google Scholar] [CrossRef]
- Terpou, A.; Gialleli, A.I.; Bosnea, L.; Kanellaki, M.; Koutinas, A.A.; Castro, G.R. Novel cheese production by incorporation of sea buckthorn berries (Hippophae rhamnoides L.) supported probiotic cells. LWT Food Sci. Technol. 2017, 79, 616–624. [Google Scholar] [CrossRef]
- Lule, V.K.; Garg, S.; Tomar, S.K.; Khedkar, C.D.; Nalage, D.N. Food Intolerance: Lactose Intolerance. In Encyclopedia of Food and Health; Caballero, B., Finglas, P.M., Toldrá, F., Eds.; Academic Press: Oxford, UK, 2016; pp. 43–48. [Google Scholar] [CrossRef]
- Da Silva, P.H.F.; Oliveira, V.C.D.; Perin, L.M. Chapter 14—Cow’s Milk Protein Allergy and Lactose Intolerance. In Raw Milk; Nero, L.A., De Carvalho, A.F., Eds.; Academic Press: Oxford, UK, 2019; pp. 295–309. [Google Scholar] [CrossRef]
- Panghal, A.; Janghu, S.; Virkar, K.; Gat, Y.; Kumar, V.; Chhikara, N. Potential non-dairy probiotic products—A healthy approach. Food Biosci. 2018, 21, 80–89. [Google Scholar] [CrossRef]
- Kazakos, S.; Mantzourani, I.; Nouska, C.; Alexopoulos, A.; Bezirtzoglou, E.; Bekatorou, A.; Plessas, S.; Varzakas, T. Production of low-alcohol fruit beverages through fermentation of pomegranate and orange juices with kefir grains. Curr. Res. Nutr. Food Sci. 2016, 4, 19–26. [Google Scholar] [CrossRef]
- Nouska, C.; Kazakos, S.; Mantzourani, I.; Alexopoulos, A.; Bezirtzoglou, E.; Plessas, S. Fermentation of cornus mas L. Juice for functional low alcoholic beverage production. Curr. Res. Nutr. Food Sci. 2016, 4, 119–124. [Google Scholar] [CrossRef]
- Di Cagno, R.; Filannino, P.; Gobbetti, M. Lactic acid fermentation drives the optimal volatile flavor-aroma profile of pomegranate juice. Int. J. Food Microbiol. 2017, 248, 56–62. [Google Scholar] [CrossRef] [PubMed]
- Filannino, P.; Azzi, L.; Cavoski, I.; Vincentini, O.; Rizzello, C.G.; Gobbetti, M.; Di Cagno, R. Exploitation of the health-promoting and sensory properties of organic pomegranate (Punica granatum L.) juice through lactic acid fermentation. Int. J. Food Microbiol. 2013, 163, 184–192. [Google Scholar] [CrossRef] [PubMed]
- Filannino, P.; Di Cagno, R.; Gobbetti, M. Metabolic and functional paths of lactic acid bacteria in plant foods: Get out of the labyrinth. Curr. Opin. Biotechnol. 2018, 49, 64–72. [Google Scholar] [CrossRef] [PubMed]
- Mousavi, Z.E.; Mousavi, S.M.; Razavi, S.H.; Emam-Djomeh, Z.; Kiani, H. Fermentation of pomegranate juice by probiotic lactic acid bacteria. World J. Microb. Biot. 2011, 27, 123–128. [Google Scholar] [CrossRef]
- Mousavi, Z.E.; Mousavi, S.M.; Razavi, S.H.; Hadinejad, M.; Emam-Djomeh, Z.; Mirzapour, M. Effect of Fermentation of Pomegranate Juice by Lactobacillus plantarum and Lactobacillus acidophilus on the Antioxidant Activity and Metabolism of Sugars, Organic Acids and Phenolic Compounds. Food Biotechnol. 2013, 27, 1–13. [Google Scholar] [CrossRef]
- Nematollahi, A.; Sohrabvandi, S.; Mortazavian, A.M.; Jazaeri, S. Viability of probiotic bacteria and some chemical and sensory characteristics in cornelian cherry juice during cold storage. Electron. J. Biotechnol. 2016, 21, 49–53. [Google Scholar] [CrossRef]
- Czyżowska, A.; Kucharska, A.Z.; Nowak, A.; Sokół-Łętowska, A.; Motyl, I.; Piórecki, N. Suitability of the probiotic lactic acid bacteria strains as the starter cultures in unripe cornelian cherry (Cornus mas L.) fermentation. J. Food Sci. Technol. 2017, 54, 2936–2946. [Google Scholar] [CrossRef] [PubMed]
- Dinda, B.; Kyriakopoulos, A.M.; Dinda, S.; Zoumpourlis, V.; Thomaidis, N.S.; Velegraki, A.; Markopoulos, C.; Dinda, M. Cornus mas L. (cornelian cherry), an important European and Asian traditional food and medicine: Ethnomedicine, phytochemistry and pharmacology for its commercial utilization in drug industry. J. Ethnopharmacol. 2016, 193, 670–690. [Google Scholar] [CrossRef] [PubMed]
- Kucharska, A.Z.; Szumny, A.; Sokół-Łętowska, A.; Piórecki, N.; Klymenko, S.V. Iridoids and anthocyanins in cornelian cherry (Cornus mas L.) cultivars. J. Food Compos. Anal. 2015, 40, 95–102. [Google Scholar] [CrossRef]
- Hosseinpour-Jaghdani, F.; Shomali, T.; Gholipour-Shahraki, S.; Rahimi-Madiseh, M.; Rafieian-Kopaei, M. Cornus mas: A review on traditional uses and pharmacological properties. J. Complement. Integr. Med. 2017, 14. [Google Scholar] [CrossRef] [PubMed]
- Plessas, S.; Bosnea, L.; Alexopoulos, A.; Bezirtzoglou, E. Potential effects of probiotics in cheese and yogurt production: A review. Eng. Life Sci. 2012, 12, 433–440. [Google Scholar] [CrossRef]
- Schoina, V.; Terpou, A.; Bosnea, L.; Kanellaki, M.; Nigam, P.S. Entrapment of Lactobacillus casei ATCC393 in the viscus matrix of Pistacia terebinthus resin for functional myzithra cheese manufacture. LWT-Food Sci. Technol. 2018, 89, 441–448. [Google Scholar] [CrossRef]
- Terpou, A.; Bekatorou, A.; Kanellaki, M.; Koutinas, A.A.; Nigam, P. Enhanced probiotic viability and aromatic profile of yogurts produced using wheat bran (Triticum aestivum) as cell immobilization carrier. Process Biochem. 2017, 55, 1–10. [Google Scholar] [CrossRef]
- Terpou, A.; Nigam, P.S.; Bosnea, L.; Kanellaki, M. Evaluation of Chios mastic gum as antimicrobial agent and matrix forming material targeting probiotic cell encapsulation for functional fermented milk production. LWT-Food Sci. Technol. 2018. [Google Scholar] [CrossRef]
- Terpou, A.; Gialleli, A.-I.; Bekatorou, A.; Dimitrellou, D.; Ganatsios, V.; Barouni, E.; Koutinas, A.A.; Kanellaki, M. Sour milk production by wheat bran supported probiotic biocatalyst as starter culture. Food Bioprod. Process. 2017, 101, 184–192. [Google Scholar] [CrossRef]
- Wang, P.; Wu, Z.; Wu, J.; Pan, D.; Zeng, X.; Cheng, K. Effects of Salt Stress on Carbohydrate Metabolism of Lactobacillus plantarum ATCC 14917. Curr. Microbiol. 2016, 73, 491–497. [Google Scholar] [CrossRef] [PubMed]
- Singleton, V.L.; Rossi, J. Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents. Am. J. Enol. Vitic. 1965, 16, 144–158. [Google Scholar]
- Sabokbar, N.; Khodaiyan, F. Total phenolic content and antioxidant activities of pomegranate juice and whey based novel beverage fermented by kefir grains. J. Food Sci. Technol. 2016, 53, 739–747. [Google Scholar] [CrossRef] [PubMed]
- Rodgers, S. Minimally Processed Functional Foods: Technological and Operational Pathways. J. Food Sci. 2016, 81, R2309–R2319. [Google Scholar] [CrossRef] [PubMed]
- Sadaghdar, Y.; Mortazavian, A.M.; Ehsani, M.R. Survival and activity of 5 probiotic lactobacilli strains in 2 types of flavored fermented milk. Food Sci. Biotechnol. 2012, 21, 151–157. [Google Scholar] [CrossRef]
- Valero-Cases, E.; Nuncio-Jáuregui, N.; Frutos, M.J. Influence of Fermentation with Different Lactic Acid Bacteria and in Vitro Digestion on the Biotransformation of Phenolic Compounds in Fermented Pomegranate Juices. J. Agric. Food Chem. 2017, 65, 6488–6496. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; He, J.; Pan, D.; Wu, Z.; Guo, Y.; Zeng, X.; Lian, L. Metabolomics analysis of Lactobacillus plantarum ATCC 14917 adhesion activity under initial acid and alkali stress. PLoS ONE 2018, 13. [Google Scholar] [CrossRef] [PubMed]
- Terpou, A.; Bosnea, L.; Kanellaki, M.; Plessas, S.; Bekatorou, A.; Bezirtzoglou, E.; Koutinas, A.A. Growth Capacity of a Novel Potential Probiotic Lactobacillus paracasei K5 Strain Incorporated in Industrial White Brined Cheese as an Adjunct Culture. J. Food Sci. 2018, 83, 723–731. [Google Scholar] [CrossRef] [PubMed]
- Ding, W.K.; Shah, N.P. Survival of free and microencapsulated probiotic bacteria in orange and apple juices. Int. Food Res. J. 2008, 15, 219–232. [Google Scholar]
- Ephrem, E.; Najjar, A.; Charcosset, C.; Greige-Gerges, H. Encapsulation of natural active compounds, enzymes, and probiotics for fruit juice fortification, preservation, and processing: An overview. J. Funct. Foods 2018, 48, 65–84. [Google Scholar] [CrossRef]
- Curiel, J.A.; Pinto, D.; Marzani, B.; Filannino, P.; Farris, G.A.; Gobbetti, M.; Rizzello, C.G. Lactic acid fermentation as a tool to enhance the antioxidant properties of Myrtus communis berries. Microb. Cell Fact. 2015, 14, 67. [Google Scholar] [CrossRef] [PubMed]
- Coda, R.; Lanera, A.; Trani, A.; Gobbetti, M.; Di Cagno, R. Yogurt-like beverages made of a mixture of cereals, soy and grape must: Microbiology, texture, nutritional and sensory properties. Int. J. Food Microbiol. 2012, 155, 120–127. [Google Scholar] [CrossRef] [PubMed]
- Nazarni, R.; Purnama, D.; Umar, S.; Eni, H. The effect of fermentation on total phenolic, flavonoid and tannin content and its relation to antibacterial activity in jaruk tigarun (Crataeva nurvala, Buch HAM)). Int. Food Res. J. 2016, 23, 309–315. [Google Scholar]
- Othman, N.B.; Roblain, D.; Chammen, N.; Thonart, P.; Hamdi, M. Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chem. 2009, 116, 662–669. [Google Scholar] [CrossRef]
- Kourkoutas, Y.; Bekatorou, A.; Banat, I.M.; Marchant, R.; Koutinas, A.A. Immobilization technologies and support materials suitable in alcohol beverages production: A review. Food Microbiol. 2004, 21, 377–397. [Google Scholar] [CrossRef]
- Luckow, T.; Sheehan, V.; Fitzgerald, G.; Delahunty, C. Exposure, health information and flavour-masking strategies for improving the sensory quality of probiotic juice. Appetite 2006, 47, 315–323. [Google Scholar] [CrossRef] [PubMed]
Time | Cell Counts (log cfu/mL) | |
---|---|---|
FC | IC | |
0 h | 11.15 ± 0.4 A,a | 11.15 ± 0.3 A,a |
24 h | 10.28 ± 0.2 A,b | 10.47 ± 0.2 A,b |
Week 1 | 9.21 ± 0.3 B,c | 10.41 ± 0.3 A,b |
Week 2 | 9.03 ± 0.2 B,c | 10.49 ± 0.1 A,b |
Week 3 | 7.86 ± 0.3 B,d | 10.08 ± 0.1 A,c |
Week 4 | 7.36 ± 0.2 B,d | 9.95 ± 0.1 A,c |
Parameter | Time | Lactobacillus plantarum ATCC 14917 | |
---|---|---|---|
FC | IC | ||
Sugars (g/l) | 24 h | 51.5 ± 0.3 A,a | 50.4 ± 0.3 B,a |
Week 1 | 47.3 ± 0.1 A,b | 42.3 ± 0.3 B,b | |
Week 2 | 37.2 ± 0.4 A,c | 33.1 ± 0.3 B,c | |
Week 3 | 24.2 ± 0.4 A,d | 21.8 ± 0.3 B,d | |
Week 4 | 20.9 ± 0.5 A,e | 18.9 ± 0.3 B,e | |
Lactic Acid (mg/100 mL) | 24 h | 11.2 ± 0.2 B,e | 24.2 ± 0.1 A,e |
Week 1 | 39.8 ± 0.2 B,d | 41.4 ± 0.1 A,d | |
Week 2 | 58.4 ± 0.2 B,c | 76.9 ± 0.2 A,c | |
Week 3 | 81.1 ± 0.1 B,b | 94.8 ± 0.3 A,b | |
Week 4 | 97.8 ± 0.3 B,a | 148.5 ± 0.4 A,a | |
Acetic Acid (mg/100 mL) | 24 h | ND | ND |
Week 1 | 1.2 ± 0.2 B,d | 3.4 ± 0.1 A,d | |
Week 2 | 3.9 ± 0.2 B,c | 7.6 ± 0.2 A,c | |
Week 3 | 6.4 ± 0.2 Bb | 9.2 ± 0.2 A,b | |
Week 4 | 8.2 ± 0.2 B,a | 15.4 ± 0.3 A,a | |
Ethanol (% v/v) | 24 h | 0.3 ± 0.1 A,b | 0.3 ± 0.1 A,c |
Week 1 | 0.3 ± 0.1 A,b | 0.3 ± 0.1 A,c | |
Week 2 | 0.4 ± 0.1 A,b | 0.6 ± 0.1 A,b | |
Week 3 | 0.4 ± 0.1 A,b | 0.6 ± 0.1 A,b | |
Week 4 | 0.7 ± 0.1 A,a | 0.9 ± 0.1 A,a |
Time | Total Phenolics Content (mg GAE/100 mL) | ||
---|---|---|---|
NFC | FC | IC | |
24 h | 169.32 ± 12.23 B,a | 165.02 ± 10.62 B,b | 214.41 ± 10.56 A,b |
Week 1 | 161.32 ± 11.30 B,a | 184.45 ± 10.23 B,a | 257.20 ± 17.11 A,a |
Week 2 | 136.28 ± 10.08 C,b | 199.72 ± 14.51 B,a | 264.71 ± 16.08 A,a |
Week 3 | 136.40 ± 10.53 C,b | 198.38 ± 19.06 B,a | 258.84 ± 13.24 A,a |
Week 4 | 135.19 ± 11.08 C,b | 195.02 ± 14.75 B,a | 249.61 ± 14.34 A,a |
Storage Time | Substrate | Aroma | Taste | Overall Quality |
---|---|---|---|---|
24 h | NFC | 8.5 ± 0.1 a | 9.0 ± 0.2 a | 9.1 ± 0.1 a |
FC | 8.6 ± 0.2 a | 9.1 ± 0.2 a | 8.9 ± 0.1 a | |
IC | 8.5 ± 0.1 a | 9.0 ± 0.2 a | 9.0 ± 0.2 a | |
Week 1 | NFC | 7.8 ± 0.2 a | 7.8 ± 0.1 a | 7.7 ± 0.2 a |
FC | 7.9 ± 0.1 a | 7.9 ± 0.2 a | 7.8 ± 0.2 a | |
IC | 7.7 ± 0.1 a | 7.6 ± 0.1 a | 7.7 ± 0.1 a | |
Week 2 | NFC | 7.0 ± 0.1 a | 6.9 ± 0.1 a | 7.0 ± 0.2 a |
FC | 7.1 ± 0.1 a | 6.8 ± 0.1 a | 7.1 ± 0.2 a | |
IC | 7.0 ± 0.1 a | 6.9 ± 0.1 a | 7.0 ± 0.1 a | |
Week 3 | NFC | 6.5 ± 0.1 a | 6.5 ± 0.2 a | 6.5 ± 0.2 a |
FC | 6.6 ± 0.1 a | 6.6 ± 0.1 a | 6.5 ± 0.2 a | |
IC | 6.4 ± 0.1 a | 6.5 ± 0.2 a | 6.5 ± 0.1 a | |
Week 4 | NFC | 6.3 ± 0.3 a | 6.1 ± 0.2 a | 6.1 ± 0.3 a |
FC | 6.2 ± 0.2 a | 6.1 ± 0.3 a | 6.3 ± 0.2 a | |
IC | 6.3 ± 0.2 a | 6.0 ± 0.4 a | 5.9 ± 0.2 a |
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mantzourani, I.; Nouska, C.; Terpou, A.; Alexopoulos, A.; Bezirtzoglou, E.; Panayiotidis, M.I.; Galanis, A.; Plessas, S. Production of a Novel Functional Fruit Beverage Consisting of Cornelian Cherry Juice and Probiotic Bacteria. Antioxidants 2018, 7, 163. https://doi.org/10.3390/antiox7110163
Mantzourani I, Nouska C, Terpou A, Alexopoulos A, Bezirtzoglou E, Panayiotidis MI, Galanis A, Plessas S. Production of a Novel Functional Fruit Beverage Consisting of Cornelian Cherry Juice and Probiotic Bacteria. Antioxidants. 2018; 7(11):163. https://doi.org/10.3390/antiox7110163
Chicago/Turabian StyleMantzourani, Ioanna, Chryssa Nouska, Antonia Terpou, Athanasios Alexopoulos, Eugenia Bezirtzoglou, Mihalis I. Panayiotidis, Alexis Galanis, and Stavros Plessas. 2018. "Production of a Novel Functional Fruit Beverage Consisting of Cornelian Cherry Juice and Probiotic Bacteria" Antioxidants 7, no. 11: 163. https://doi.org/10.3390/antiox7110163
APA StyleMantzourani, I., Nouska, C., Terpou, A., Alexopoulos, A., Bezirtzoglou, E., Panayiotidis, M. I., Galanis, A., & Plessas, S. (2018). Production of a Novel Functional Fruit Beverage Consisting of Cornelian Cherry Juice and Probiotic Bacteria. Antioxidants, 7(11), 163. https://doi.org/10.3390/antiox7110163