Characteristics, Antioxidant, and Antihypertensive Activities of Probiotic Greek Yogurt with Roselle Extract Addition
Abstract
Yogurt is one example of a functional food that can improve health and reduce the risk of diseases. Certain ingredients, such as probiotic bacteria and roselle extract, are added to yogurt to enhance its benefits. The utilized probiotic, Lactobacillus plantarum IIA-1A5, provides notable antimicrobial benefits. Additionally, the incorporated roselle extract is established to possess antioxidant and antihypertensive properties. This study aims to analyze the characteristics, antioxidant, and antihypertensive activities of probiotic Greek yogurt (PGY) and probiotic Greek yogurt with roselle extract (PGYR). The roselle extract added to the Greek probiotic yogurt was 3%, and the bacteria used in the fermentation process for both treatments were S. thermophilus IFO 13957, L. bulgaricus IFO 13953, and L. plantarum IIA-1A5. Each treatment was replicated three times in duplicate. The results showed that the addition of roselle extract to probiotic Greek yogurt significantly influenced (p<0.05) the antioxidant and antihypertensive activity, water activity (aw), pH, total acidity (TAT), and the color aspect in the hedonic test and the flavor, color, and aroma aspects in the hedonic quality test. The antioxidant activity and antihypertensive activity tests yielded significantly different results. The antioxidant activity increased from 29.32% (PGY) to 44.93% (PGYR), while the antihypertensive activity increased from 35.68% (PGY) to 81.36% (PGYR). This study concluded that the characteristics of PGYR have met the SNI standards and have a higher antioxidant and antihypertensive activity value than PGY. PGYR also has a promising potential for commercial development due to its health benefits.
References
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Baliyan, S., R. Mukherjee, A. Priyadarshini, A. Vibhuti, A. Gupta, R. P. Pandey, & C. M. Chang. 2022. Determination of antioxidants by dpph radical scavenging activity and quantitative phytochemical analysis of Ficus religiosa. Molecules 27:1326. https://doi.org/10.3390/molecules27041326
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Chusman, D. W. & H. S Cheung. 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol. 20:1637-1648. https://doi.org/10.1016/0006-2952(71)90292-9
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Farida, F. Y. & P. Farasari. 2020. Effectiveness of roselle tea on decreasing blood pressure in hypertension patients in Tulungagung district. STRADA Jurnal Ilmiah Kesehatan 9:162–169. https://doi.org/10.30994/sjik.v9i1.277
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Ga Young, D., K. E. Young, K. Y. Jin, H. Youngji, K. Seong-Bo, K. Y. Hee, & C. Myung-Sook. 2019. Supplementation of non-dairy creamer-enriched high-fat diet with D-Allulose ameliorated blood glucose and body fat accumulation in C57BL/6J mice. Applied Sciences 9:2750. https://doi.org/10.3390/app9132750
Grajeda, I. C., E. M. C. Figueroa, N. Barouh, B. Baréa, A. Fernandes, F. V. De, & E. Salas. 2016. Isolation and characterization of anthocyanins from Hibiscus sabdariffa flowers. J. Nat. Prod. 79:1709-1718. https://doi.org/10.1021/acs.jnatprod.5b00958
Igwe, E. O., K. E. Charlton, & Y. C. Probst. 2019. Usual dietary anthocyaninintake, sources and their association with blood pressure in arepresentative sample of Australian adults. J. Hum. Nutr Diet. 32:578-90. https://doi.org/10.1111/jhn.12647
Jamil, N. H., N. R. A. Halim, & N. M. Sarbon. 2016. A response surface approach on hydrolysis condition of eel (Monopterus Sp.) protein hydrolysate with antioxidant activity. Int. Food Res. J. 24:1081-1093.
Khusnaini, M. 2014. Utilization of papaya fruit (Carica papaya l.) in the manufacture of fruit yogurt with different amounts of starter concentration and fermentation duration. Jurnal Agrina 1:23-30.
Kim, J., M. Kim, & I. Choi. 2023. Physicochemical characteristics, antioxidant properties and consumer acceptance of greek yogurt fortified with apple pomace syrup. Foods 12:1856. https://doi.org/10.3390/foods12091856
Kumar, B. V., S. V. Vijayendra, & O. V. Reddy. 2015. Trends in dairy and non-dairy probiotic products - A review. J. Food Sci Technol. 52:6112-6124. https://doi.org/10.1007/s13197-015-1795-2
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Meilanie, R., I. I. Arief, & E. Taufik. 2018. Karakteristik yoghurt probiotik dengan penambahan ekstrak bunga rosella (Hibiscus sabdariffa L.) selama penyimpanan suhu dingin. J. I. Produksi Teknol. Hasil Peternakan 6:36-44. https://doi.org/10.29244/jipthp.6.1.36-44
Moineau-Jean, A., Y. Raymond, H. Sabik, N. Graveline, C. P. Champagne, D. Roy, & G. LaPointe. 2020. Effect of manufacturing processes and storage on aroma compounds and sensory properties of yoghurt. Int. J. Dairy Sci. 105:104662. https://doi.org/10.1016/j.idairyj.2020.104662
Molyneux, P. 2004. The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J. 26:211-219.
Ndanuko, R. N., L. C. Tapsell, K. E. Charlton, E. P. Neale, & M. J. Batterham. 2016. Dietary patterns and blood pressure in adults: A systematic review and meta-analysis of randomized controlled trials. Adv. Nutr. 7:76–89. https://doi.org/10.3945/an.115.009753
Ngo, D. H., B. Ryu, & S. K. Kim. 2014. Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. Food Chem. 143:246–255. https://doi.org/10.1016/j.foodchem.2013.07.067
Ohnishi, M., H. Morishita, H. Iwahashi, S. Toda, Y. Shirataki, M. Kimura, & R. Kido. 1994. Inhibitory effects of chlorogenic acids on linoleic-acid peroxidation and 33 hemolysis. Phytochemistry 36:579–583. https://doi.org/10.1016/S0031-9422(00)89778-2
Ojeda, D., E. Jimenez-Ferrer, A. Zamilpa, A. Hererra-Arellano, J. Tortoriello, & L. Alvarez. 2010. Inhibiton of angiotensin converting enzyme activity by the anthocyanins delphinidin and cyanidin-3-O-sambubiosides from Hibiscus sabdariffa. J. Ethnopharmacol. 127:7-10. https://doi.org/10.1016/j.jep.2009.09.059
Patel, S., A. Rauf, H. Khan, & T. Abu-Izneid. 2017. Renin-Angiotensin-Aldosterone (RAAS): The ubiquitous system for homeostasis and pathologies. Biomed. Pharmacother 94:317–325. https://doi.org/10.1016/j.biopha.2017.07.091
Purbowati, I. S. M., Sujiman, & A. Maksum. 2018. Antibacterial activity of roselle (Hibiscus sabdariffa) extract phenolics compound produced with varying drying methods and duration. Journal Agroindustrial Technology 28:19-27.
Samadi, S. & F. R. Fard. 2020. Phytochemical properties, antioxidant activity and mineral content (Fe, Zn and Cu) in Iranian produced black tea, green tea and roselle calyces. Biocatal. Agric. Biotechnol. 23:101472. https://doi.org/10.1016/j.bcab.2019.101472
Saputri, F. C., D. Mun’im, S. N. Lukmanto, Aisyah, & J. S. Rinandy. 2015. Inhibition of angiotensin converting enzyme (ACE) activity by some Indonesia edible plants. Int. J. Pharm. Sci. Res. 6:1054–1059.
Sirag, N. M. M., Elhadi, A. M. Algaili, H. M. Hassan, & M. Ohaj. 2014. Determination of total phenolic content and antioxidant activity of roselle (Hibiscus sabdariffa L.) calyx ethanolic extract. Standard Research Journal Pharmacy Pharmacology 1:34-39.
Sorriento, D., L. N. De, B. Trimarco, & G. Iaccarino. 2018. The antioxidant therapy: New insights in the treatment of hypertension. Front. Physiol. 9:258 https://doi.org/10.3389/fphys.2018.00258
Suharto, E. L. S., I. I. Arief, & E. Taufik. 2016. Quality and antioxidant activity of yogurt supplemented with roselle during cold storage. Med Pet. 39:82-89. https://doi.org/10.5398/medpet.2016.39.2.82
Tangkanakul, P., P. Auttaviboonkul, B. Niyomwit, N. Lowvitoon, P. Charoenthamawat, & G. Trakoontivakorn. 2009. Antioxidant capacity, total phenolic content and nutritional composition of Asian foods after thermal processing. Int. Food Res. J. 16:571-580.
Tapia, M. S., S. M. Alzamora, & J. Chirife. 2020. Effects of Water Activity (aw) on microbial stability as a hurdle in food preservation. Water Activity Foods Fundamentals Applications. 2nd Ed. Chapter 14. pp. 323-355. https://doi.org/10.1002/9781118765982.ch14
Tayel, A. A. & W. F. El‐Tras. 2012. Plant extracts as potent biopreservatives for Salmonella typhimurium control and quality enhancement in ground beef. J. Food Saf. 32:115-121. https://doi.org/10.1111/j.1745-4565.2011.00357.x
Toffanin, V., M. De Marchi, N. Lopez-Villalobos, & M. Cassandro. 2015. Effectiveness of mid-infrared spectroscopy for prediction of the contents of calcium and phosphorus, and titratable acidity of milk and their relationship with milk quality and coagulation properties. Int. Dairy J. 41:68-73. https://doi.org/10.1016/j.idairyj.2014.10.002
Vendrame, S. & D. Klimis-Zacas. 2019. Potential factors influencing the effects of anthocyanins on blood pressure regulation in humans: A review. Nutrients 11:1-19. https://doi.org/10.3390/nu11061431
Widyastuti, Y. R. & A. Febrisiantosa. 2014.The role of lactic acid bacteria in milk fermentation. Food Nutr. Sci. 5:435-442. https://doi.org/10.4236/fns.2014.54051
Wihansah, R., I. I. Arief, & B. Irmanida. 2018. Antidiabetic potency and characteristics of probiotic goat-milk yogurt supplemented with roselle extract during cold storage. Trop. Anim. Sci. J. 41:191-9. https://doi.org/10.5398/tasj.2018.41.3.191
Wu, H. Y., K. M. Yang, & P. Y. Chiang. 2018. Roselle anthocyanins: Antioxidant properties and stability to heat and pH. Molecules 23:1357. https://doi.org/10.3390/molecules23061357
Zang, S., S. Tian, J. Jiang, D. Han, X. Yu, K. Wang, D. Li, D. Lu, A. Yu, & Z. Zhang. 2017. Determination of antioxidant capacity of diverse fruits by electron spin resonance (ESR) and UV–vis spectrometries. Food Chem. 221:1221-1225. https://doi.org/10.1016/j.foodchem.2016.11.036
Aloglu, H. S. 2013. The effect of various heat treatments on the antioxidant capacity of milk before and after simulated gastrointestinal digestion. Int. J. Dairy Technol. 66:170–174. https://doi.org/10.1111/1471-0307.12021
Amin, A. R., R. B. Kassab, A. E. A. Moneim, & H. K. Amin. 2020. Comparison among garlic, berberine, resveratrol, Hibiscus sabdariffa, genus Zizyphus, hesperidin, red beetroot, Catha edulis, Portulaca oleracea, and mulberry leaves in the treatment of hypertension and type 2 DM: A comprehensive review. Nat. Prod Commun. 15:1-24. https://doi.org/10.1177/1934578X20921623
AOAC. 2005. Official Methods of Analysis of AOAC International. Analysis. Ass of Anal. Chem., USA.
AOAC. 2007. Official Methods of Analysis. Ass of Anal. Chem., USA.
Arief, I. I., B. S. L. Jenie, M. Astawan, K. Fujiyama, & A. B. Witarto. 2015. Identification and probiotic characteristics of lactic acid bacteria isolated from Indonesian local beef. Asian J. Anim. Sci. 9:25-36. https://doi.org/10.3923/ajas.2015.25.36
Arief, I. I., C. Budiman, R. Hanifah, & M. S. Soenarno. 2016. Antihypertensive potency of goat milk yogurt supplemented by probiotic and roselle extract. Int. J. Sci. Basic Appl. Res. 30:207-214.
Arief, I. I., T. Suryati, Z. Wulandari, & E. Andreas. 2013. Isolation and characterization of plantaricin produced by Lactobacillus plantarum strains (IIA-1A5, IIA-1B1, IIA- 2B2). Med. Pet. 36:91-100. https://doi.org/10.5398/medpet.2013.36.2.91
Badan Standardisasi Nasional. 2006. Petunjuk Pengujian Organoleptik atau Sensori. SNI 01 2346-2006. BSNI, Jakarta.
Badan Standardisasi Nasional. 2009. Syarat Mutu Yoghurt. SNI: 2981-2009. BSNI, Jakarta.
Baliyan, S., R. Mukherjee, A. Priyadarshini, A. Vibhuti, A. Gupta, R. P. Pandey, & C. M. Chang. 2022. Determination of antioxidants by dpph radical scavenging activity and quantitative phytochemical analysis of Ficus religiosa. Molecules 27:1326. https://doi.org/10.3390/molecules27041326
Bridge, A., J. Brown, H. Snider, M. Nasato, W. E. Ward, B. D. Roy, & A. R. Josse. 2019. Greek yogurt and 12 weeks of exercise training on strength, muscle thickness and body composition in lean, untrained, university-aged males. Front. Nutr. 6:55. https://doi.org/10.3389/fnut.2019.00055
Chen, G. W., J. S. Tsai, & B. S. Pan. 2007. Purification of angiotensin I-converting enzyme inhibitory peptides and antihypertensive effect of milk produced by protease-facilitated lactic fermentation. Int. Dairy J. 17:641-647. https://doi.org/10.1016/j.idairyj.2006.07.004
Chen, W., A. Narbad, W. Wu, & H. Li. 2018. Metabolites of Lactic Acid Bacteria. Lactic Acid Bacteria in Foodborne Hazards Reduction: Physiology to Practice. Springer, Singapore. https://doi.org/10.1007/978-981-13-1559-6
Chusman, D. W. & H. S Cheung. 1971. Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol. 20:1637-1648. https://doi.org/10.1016/0006-2952(71)90292-9
Dinçoğlu, A. H., A. Ileri, & J. Rugji. 2023. Determination of bioactive properties of Capparis spinosa fruits and use in production of Tulum cheese. Emir. J. Food Agric. 35:1-12. https://doi.org/10.9755/ejfa.2023.3179
Fardiaz, S. 1993. Analisis Mikrobiologi Pangan. Raja Grafindo Persada, Jakarta.
Farida, F. Y. & P. Farasari. 2020. Effectiveness of roselle tea on decreasing blood pressure in hypertension patients in Tulungagung district. STRADA Jurnal Ilmiah Kesehatan 9:162–169. https://doi.org/10.30994/sjik.v9i1.277
Francenia, S. S. N., R. Salas-Coronado, C. Villanueva-Cañongo, & B. Hernández-Carlos. 2019. Antioxidant Compounds and Their Antioxidant Mechanism. Antioxidants. IntechOpen, London. pp. 1-29.
Ga Young, D., K. E. Young, K. Y. Jin, H. Youngji, K. Seong-Bo, K. Y. Hee, & C. Myung-Sook. 2019. Supplementation of non-dairy creamer-enriched high-fat diet with D-Allulose ameliorated blood glucose and body fat accumulation in C57BL/6J mice. Applied Sciences 9:2750. https://doi.org/10.3390/app9132750
Grajeda, I. C., E. M. C. Figueroa, N. Barouh, B. Baréa, A. Fernandes, F. V. De, & E. Salas. 2016. Isolation and characterization of anthocyanins from Hibiscus sabdariffa flowers. J. Nat. Prod. 79:1709-1718. https://doi.org/10.1021/acs.jnatprod.5b00958
Igwe, E. O., K. E. Charlton, & Y. C. Probst. 2019. Usual dietary anthocyaninintake, sources and their association with blood pressure in arepresentative sample of Australian adults. J. Hum. Nutr Diet. 32:578-90. https://doi.org/10.1111/jhn.12647
Jamil, N. H., N. R. A. Halim, & N. M. Sarbon. 2016. A response surface approach on hydrolysis condition of eel (Monopterus Sp.) protein hydrolysate with antioxidant activity. Int. Food Res. J. 24:1081-1093.
Khusnaini, M. 2014. Utilization of papaya fruit (Carica papaya l.) in the manufacture of fruit yogurt with different amounts of starter concentration and fermentation duration. Jurnal Agrina 1:23-30.
Kim, J., M. Kim, & I. Choi. 2023. Physicochemical characteristics, antioxidant properties and consumer acceptance of greek yogurt fortified with apple pomace syrup. Foods 12:1856. https://doi.org/10.3390/foods12091856
Kumar, B. V., S. V. Vijayendra, & O. V. Reddy. 2015. Trends in dairy and non-dairy probiotic products - A review. J. Food Sci Technol. 52:6112-6124. https://doi.org/10.1007/s13197-015-1795-2
Mattioli, R., A. Francioso, L. Mosca, & P. Silva. 2020. Anthocyanins: A comprehensive review of their chemical properties and health effects on cardiovascular and neurodegenerative diseases. Molecules 25:3809. https://doi.org/10.3390/molecules25173809
Meilanie, R., I. I. Arief, & E. Taufik. 2018. Karakteristik yoghurt probiotik dengan penambahan ekstrak bunga rosella (Hibiscus sabdariffa L.) selama penyimpanan suhu dingin. J. I. Produksi Teknol. Hasil Peternakan 6:36-44. https://doi.org/10.29244/jipthp.6.1.36-44
Moineau-Jean, A., Y. Raymond, H. Sabik, N. Graveline, C. P. Champagne, D. Roy, & G. LaPointe. 2020. Effect of manufacturing processes and storage on aroma compounds and sensory properties of yoghurt. Int. J. Dairy Sci. 105:104662. https://doi.org/10.1016/j.idairyj.2020.104662
Molyneux, P. 2004. The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J. 26:211-219.
Ndanuko, R. N., L. C. Tapsell, K. E. Charlton, E. P. Neale, & M. J. Batterham. 2016. Dietary patterns and blood pressure in adults: A systematic review and meta-analysis of randomized controlled trials. Adv. Nutr. 7:76–89. https://doi.org/10.3945/an.115.009753
Ngo, D. H., B. Ryu, & S. K. Kim. 2014. Active peptides from skate (Okamejei kenojei) skin gelatin diminish angiotensin-I converting enzyme activity and intracellular free radical-mediated oxidation. Food Chem. 143:246–255. https://doi.org/10.1016/j.foodchem.2013.07.067
Ohnishi, M., H. Morishita, H. Iwahashi, S. Toda, Y. Shirataki, M. Kimura, & R. Kido. 1994. Inhibitory effects of chlorogenic acids on linoleic-acid peroxidation and 33 hemolysis. Phytochemistry 36:579–583. https://doi.org/10.1016/S0031-9422(00)89778-2
Ojeda, D., E. Jimenez-Ferrer, A. Zamilpa, A. Hererra-Arellano, J. Tortoriello, & L. Alvarez. 2010. Inhibiton of angiotensin converting enzyme activity by the anthocyanins delphinidin and cyanidin-3-O-sambubiosides from Hibiscus sabdariffa. J. Ethnopharmacol. 127:7-10. https://doi.org/10.1016/j.jep.2009.09.059
Patel, S., A. Rauf, H. Khan, & T. Abu-Izneid. 2017. Renin-Angiotensin-Aldosterone (RAAS): The ubiquitous system for homeostasis and pathologies. Biomed. Pharmacother 94:317–325. https://doi.org/10.1016/j.biopha.2017.07.091
Purbowati, I. S. M., Sujiman, & A. Maksum. 2018. Antibacterial activity of roselle (Hibiscus sabdariffa) extract phenolics compound produced with varying drying methods and duration. Journal Agroindustrial Technology 28:19-27.
Samadi, S. & F. R. Fard. 2020. Phytochemical properties, antioxidant activity and mineral content (Fe, Zn and Cu) in Iranian produced black tea, green tea and roselle calyces. Biocatal. Agric. Biotechnol. 23:101472. https://doi.org/10.1016/j.bcab.2019.101472
Saputri, F. C., D. Mun’im, S. N. Lukmanto, Aisyah, & J. S. Rinandy. 2015. Inhibition of angiotensin converting enzyme (ACE) activity by some Indonesia edible plants. Int. J. Pharm. Sci. Res. 6:1054–1059.
Sirag, N. M. M., Elhadi, A. M. Algaili, H. M. Hassan, & M. Ohaj. 2014. Determination of total phenolic content and antioxidant activity of roselle (Hibiscus sabdariffa L.) calyx ethanolic extract. Standard Research Journal Pharmacy Pharmacology 1:34-39.
Sorriento, D., L. N. De, B. Trimarco, & G. Iaccarino. 2018. The antioxidant therapy: New insights in the treatment of hypertension. Front. Physiol. 9:258 https://doi.org/10.3389/fphys.2018.00258
Suharto, E. L. S., I. I. Arief, & E. Taufik. 2016. Quality and antioxidant activity of yogurt supplemented with roselle during cold storage. Med Pet. 39:82-89. https://doi.org/10.5398/medpet.2016.39.2.82
Tangkanakul, P., P. Auttaviboonkul, B. Niyomwit, N. Lowvitoon, P. Charoenthamawat, & G. Trakoontivakorn. 2009. Antioxidant capacity, total phenolic content and nutritional composition of Asian foods after thermal processing. Int. Food Res. J. 16:571-580.
Tapia, M. S., S. M. Alzamora, & J. Chirife. 2020. Effects of Water Activity (aw) on microbial stability as a hurdle in food preservation. Water Activity Foods Fundamentals Applications. 2nd Ed. Chapter 14. pp. 323-355. https://doi.org/10.1002/9781118765982.ch14
Tayel, A. A. & W. F. El‐Tras. 2012. Plant extracts as potent biopreservatives for Salmonella typhimurium control and quality enhancement in ground beef. J. Food Saf. 32:115-121. https://doi.org/10.1111/j.1745-4565.2011.00357.x
Toffanin, V., M. De Marchi, N. Lopez-Villalobos, & M. Cassandro. 2015. Effectiveness of mid-infrared spectroscopy for prediction of the contents of calcium and phosphorus, and titratable acidity of milk and their relationship with milk quality and coagulation properties. Int. Dairy J. 41:68-73. https://doi.org/10.1016/j.idairyj.2014.10.002
Vendrame, S. & D. Klimis-Zacas. 2019. Potential factors influencing the effects of anthocyanins on blood pressure regulation in humans: A review. Nutrients 11:1-19. https://doi.org/10.3390/nu11061431
Widyastuti, Y. R. & A. Febrisiantosa. 2014.The role of lactic acid bacteria in milk fermentation. Food Nutr. Sci. 5:435-442. https://doi.org/10.4236/fns.2014.54051
Wihansah, R., I. I. Arief, & B. Irmanida. 2018. Antidiabetic potency and characteristics of probiotic goat-milk yogurt supplemented with roselle extract during cold storage. Trop. Anim. Sci. J. 41:191-9. https://doi.org/10.5398/tasj.2018.41.3.191
Wu, H. Y., K. M. Yang, & P. Y. Chiang. 2018. Roselle anthocyanins: Antioxidant properties and stability to heat and pH. Molecules 23:1357. https://doi.org/10.3390/molecules23061357
Zang, S., S. Tian, J. Jiang, D. Han, X. Yu, K. Wang, D. Li, D. Lu, A. Yu, & Z. Zhang. 2017. Determination of antioxidant capacity of diverse fruits by electron spin resonance (ESR) and UV–vis spectrometries. Food Chem. 221:1221-1225. https://doi.org/10.1016/j.foodchem.2016.11.036
Authors
JuandiniP. A., AriefI. I., WulandariZ., & AbidinZ. (2024). Characteristics, Antioxidant, and Antihypertensive Activities of Probiotic Greek Yogurt with Roselle Extract Addition. Tropical Animal Science Journal, 47(2), 235-241. https://doi.org/10.5398/tasj.2024.47.2.235
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