Bioactivity of Pomegranate (Punica granatum L.) Peels Flour to Improve Probiotics Viability in Micro Co-Encapsulation by Ionic Gelation

References

• Abouloifa, H., N. Khodaei, Y. Rokni, S. Karboune, M. Brasca, G. D’Hallewin, R. Ben Salah, E. Saalaoui, and A. Asehraou. 2020. The prebiotics (Fructo-oligosaccharides and xylo-oligosaccharides) modulate the probiotic properties of Lactiplantibacillus and Levilactobacillus strains isolated from traditional fermented olive. World J. Microbiol. Biotech 36 (12):185. doi:10.1007/s11274-020-02961-9.
   PubMed Web of Science ®Google Scholar
• Afzaal, M., F. Saeed, H. Ateeq, A. Imran, I. Yasmin, A. Shahid, A. Javed, Y. A. Shah, F. Islam, C. E. Ofoedu, et al. 2022. Survivability of probiotics under hostile conditions as affected by prebiotic-based encapsulating materials. Int. J. Food Prop. 25 (1):2044–2054. doi:10.1080/10942912.2022.2121836.
   Web of Science ®Google Scholar
• Akhtar, S., T. Ismail, D. Fraternale, and P. Sestili. 2015. Pomegranate peel and peel extracts: Chemistry and food features. Food Chem. 174:417–425. doi:10.1016/j.foodchem.2014.11.035.
   PubMed Web of Science ®Google Scholar
• Al-Hindi, R. R., and S. Abd El Ghani. 2020. Production of functional fermented milk beverages supplemented with pomegranate peel extract and probiotic lactic acid bacteria. J. Food. Qual. 2020 (10):1–9. doi:10.1155/2020/4710273.
   Google Scholar
• Ali, A., Y. Chen, H. Liu, L. Yu, Z. Baloch, S. Khalid, J. Zhu, and L. Chen. 2019. Starch-based antimicrobial films functionalized by pomegranate peel. Int. J. Biol. Macromol. 129:1120–1126. doi:10.1016/j.ijbiomac.2018.09.068.
   PubMed Web of Science ®Google Scholar
• Álvarez-Martínez, F. J., E. Barrajón-Catalán, J. A. Encinar, J. C. Rodríguez-Díaz, and V. Micol. 2020. Antimicrobial capacity of plant polyphenols against Gram-positive bacteria: A comprehensive review. Curr. Med. Chem. 27 (15):2576–2606. doi:10.2174/0929867325666181008115650.
   PubMed Web of Science ®Google Scholar
• AOAC. 1999. Official method of analysis of AOAC international. 16th ed. Washington, DC: AOAC International.
   Google Scholar
• Aqil, F., R. Munagala, M. V. Vadhanam, H. Kausar, J. Jeyabalan, D. J. Schultz, and R. C. Gupta. 2012. Anti-proliferative activity and protection against oxidative DNA damage by punicalagin isolated from pomegranate husk. Food Res. Int. 49 (1):345–253. doi:10.1016/j.foodres.2012.07.059.
   PubMed Web of Science ®Google Scholar
• Balli, D., M. Khatib, L. Cecchi, A. Adessi, P. Melgarejo, C. Nunes, M. A. Coimbra, and N. Mulinacci. 2022. Pomegranate peel as a promising source of pectic polysaccharides: A multi-methodological analytical investigation. Food Chem. 397:133550. doi:10.1016/j.foodchem.2022.133550.
   PubMed Web of Science ®Google Scholar
• Barragán-Martínez, L. P., A. Totosaus, and M. L. Pérez-Chabela. 2020. Probiotication of cooked sausages employing agroindustrial coproducts as prebiotic co-encapsulant in ionotropic alginate–pectin gels. Int. J. Food Sci. Technol. 55 (3):1088–1096. doi:10.1111/ijfs.14259.
   Web of Science ®Google Scholar
• Bauer, A. W., W. M. M. Kirby, J. C. Sherris, and M. Turck. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45 (4):493–496. doi:10.1093/ajcp/45.4_ts.493.
   PubMed Web of Science ®Google Scholar
• Blaak, E. E., E. E. Canfora, S. Theis, G. Frost, A. K. Groen, G. Mithieux, A. Nauta, K. Scott, B. Stahl, J. van Harsselaar, et al. 2020. Short chain fatty acids in human gut and metabolic health. Benef. Microb. 11 (5):411–455. doi:10.3920/BM2020.0057.
   PubMed Web of Science ®Google Scholar
• Böger, M., S. S. van Leeuwen, A. Lammerts van Bueren, and L. Dijkhuizen. 2019. Structural identity of galactooligosaccharide molecules selectively utilized by single cultures of probiotic bacterial strains. J. Agr. Food Chem. 67 (50):13969–13977. doi:10.1021/acs.jafc.9b05968.
   PubMed Web of Science ®Google Scholar
• Bustamante, P., L. Mayorga, H. Ramírez, P. Martínez, E. Barranco, and A. Azazola. 2006. Evaluación microbiológica de compuestos con actividad prebiótica. Rev. Mex. C. Far. 37 (2):5–10.
   Google Scholar
• Çam, M., and N. C. İ̇çyer. 2015. Phenolics of pomegranate peels: Extraction optimization by central composite design and alpha glucosidase inhibition potential. J. Food Sci. Technol. 52 (3):1489–1497. doi:10.1007/s13197-013-1148-y.
   PubMed Web of Science ®Google Scholar
• Campos-Espinoza, F., J. Castaño-Agudelo, and S. Rodriguez-Llamazares. 2022. Polysaccharides systems for probiotic bacteria microencapsulation: Mini review. Food Sci. Technol. 42:e95121. doi:10.1590/fst.95121.
   Web of Science ®Google Scholar
• Ceppa, F., A. Mancini, and K. Tuohy. 2018. Current evidence linking diet to gut microbiota and brain development and function. Int. J. Food. Sci. Nutr. 70 (1):1–19. doi:10.1080/09637486.2018.1462309.
   PubMed Web of Science ®Google Scholar
• Chan, C.-L., R. Y. Gan, N. P. Shah, and H. Corke. 2018. Enhancing antioxidant capacity of Lactobacillus acidophilus-fermented milk fortified with pomegranate peel extracts. Food Biosci. 26:185–192. doi:10.1016/j.fbio.2018.10.016.
   Web of Science ®Google Scholar
• Delgado-Ospina, J., R. Lucas-González, M. Viuda-Martos, J. Fernández-López, J. A. Pérez-Álvarez, M. Martuscelli, and C. Chaves-López. 2021. Bioactive compounds and techno-functional properties of high-fiber co-products of the cacao agro-industrial chain. Heliyon 7 (4):e06799. doi:10.1016/j.heliyon.2021.e06799.
   PubMed Web of Science ®Google Scholar
• Der, G., and B. S. Everitt. 2001. A handbook of statistical analyses using SAS. London: Chapman & Hall/CRC.
   Google Scholar
• Dubois, M., K. Gilles, J. Hamilton, P. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28 (3):350–356. doi:10.1021/ac60111a017.
   Web of Science ®Google Scholar
• Fu, X., Z. Liu, C. Zhu, H. Mou, and Q. Kong. 2018. Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria. Crit. Rev. Food Sci. Nutr. 59 (sup1):s130–s152. doi:10.1080/10408398.2018.1542587.
   PubMedGoogle Scholar
• Genskowsky, E., L. A. Puente, J. A. Pérez-Álvarez, J. Fernández-López, L. A. Muñoz, and M. Viuda-Martos. 2016. Determination of polyphenolic profile, antioxidant activity and antibacterial properties of maqui [Aristotelia chilensis (Molina) Stuntz] a Chilean blackberry. J. Sci. Food Agric. 96 (12):4235–3242. doi:10.1002/jsfa.7628.
   PubMed Web of Science ®Google Scholar
• Gibson, G. R., H. M. Probert, J. V. Loo, R. A. Rastall, and M. B. Roberfroid. 2004. Dietary modulation of the human colonic microbiota: Updating the concept of prebiotics. Nutr. Res. Rev. 17 (2):259–275. doi:10.1079/NRR200479.
   PubMed Web of Science ®Google Scholar
• Gibson, G. R., and M. B. Roberfroid. 1995. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J. Nutr. 125 (6):1401–1412. doi:10.1093/jn/125.6.1401.
   PubMed Web of Science ®Google Scholar
• Gullon, B., M. E. Pintado, J. A. Pérez-Álvarez, and M. Viuda-Martos. 2016. Assessment of polyphenolic profile and antibacterial activity of pomegranate peel (Punica granatum) flour obtained from co-product of juice extraction. Food Control. 59:94–98. doi:10.1016/j.foodcont.2015.05.025.
   Web of Science ®Google Scholar
• Havsteen, B. H. 2002. The biochemistry and medical significance of the flavonoids. Pharmacol. Therap. 96 (2):67–202. doi:10.1016/S0163-7258(02)00298-X.
   PubMed Web of Science ®Google Scholar
• Hill, C., F. Guarner, G. Reid, G. R. Gibson, D. J. Merenstein, B. Pot, L. Morelli, R. B. Canani, H. J. Flint, S. Salminen, et al. 2014. The International scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol Hepatol. 11 (8):506–514. doi:10.1038/nrgastro.2014.66.
   PubMed Web of Science ®Google Scholar
• Homayouni, A., M. R. Ehsani, A. Azizi, M. S. Yarmand, and H. Razavi. 2007. Effect of lecithin and calcium chloride solution on the microencapsulation process yield of calcium alginate beads. Iranian Pol. J. 16 (9):597–606.
   Web of Science ®Google Scholar
• Hu, D. L., and A. Nakane. 2014. Mechanisms of staphylococcal enterotoxin-induced emesis. Eur. J. Pharmacol. 722:95–107. doi:10.1016/j.ejphar.2013.08.050.
   PubMed Web of Science ®Google Scholar
• Huebner, J., R. L. Wehling, and R. W. Hutkins. 2007. Functional activity of commercial prebiotics. Int. Dairy J. 17 (7):770–775. doi:10.1016/j.idairyj.2006.10.006.
   Web of Science ®Google Scholar
• Kavas, N., G. Kavas, Ö. Kinik, M. Ateş, M. Kaplan, and G. Şatir. 2021. Symbiotic microencapsulation to enhance Bifidobacterium longum and lactobacillus paracasei survival in goat cheese. Food Sci. Technol. 42:e55620. doi:10.1590/fst.55620.
   Web of Science ®Google Scholar
• Kok, C. R., D. F. Gomez Quintero, C. Niyirora, D. Rose, A. Li, and R. Hutkins. 2019. An in vitro strategy for formulating synergistic synbiotics. App. Environ. Microbiol. 85 (16):e01073–19. doi:10.1128/AEM.01073-19.
   PubMed Web of Science ®Google Scholar
• Krumbeck, J. A., J. Walter, and R. W. Hutkins. 2018. Synbiotics for improved human health: Recent developments, challenges, and opportunities. An. Rev. Food Sci. Technol. 25 (9):451–479. doi:10.1146/annurev-food-030117-012757.
   Google Scholar
• Kushwaha, S. C., M. B. Bera, and P. Kumar. 2013. Nutritional composition of detanninated and fresh pomegranate peel powder. IOSR J. Environ. Sci. Tox. Food Technol. 7 (1):38–42. doi:10.9790/2402-0713842.
   Google Scholar
• Li, H., T. Zhang, C. Li, S. Zheng, H. Li, and J. Yu. 2020. Development of a microencapsulated synbiotic product and its application in yoghurt. LWT-Food Sci. Technol. 122:109033. doi:10.1016/j.lwt.2020.109033.
   Web of Science ®Google Scholar
• Lima, M. C., C. Paiva de Sousa, C. Fernandez-Prada, J. Harel, and E. L. de Souza. 2019. A review of the current evidence of fruit phenolic compounds as potential antimicrobials against pathogenic bacteria. Microb. Pathog. 130:259–270. doi:10.1016/j.micpath.2019.03.025.
   PubMed Web of Science ®Google Scholar
• Mansour, E., A. Ben Khaled, B. Lachiheb, M. Abid, K. Bachar, and A. Ferchichi. 2013. Phenolic compounds, antioxidant, and antibacterial activities of peel extract from Tunisian pomegranate. J. Agr. Sci. Technol. 15 (7):1393–1403.
   Google Scholar
• Martinez, R. C., R. Bedani, and S. M. Saad. 2015. Scientific evidence for health effects attributed to the consumption of probiotics and prebiotics: An update for current perspectives and future challenges. Brit. J. Nutr. 114 (12):1993–2015. doi:10.1017/S0007114515003864.
   PubMed Web of Science ®Google Scholar
• Naqash, F., F. A. Masoodi, S. A. Rather, S. M. Wani, and A. Gani. 2017. Emerging concepts in the nutraceutical and functional properties of pectin – a review. Carbohyd. Polym. 168:227–239. doi:10.1016/j.carbpol.2017.03.058.
   PubMed Web of Science ®Google Scholar
• O’Flaherty, S., N. Cobian, and R. Barrangou. 2023. Impact of pomegranate on probiotic growth, viability, transcriptome and metabolism. Microorganisms 11 (2):404. doi:10.3390/microorganisms11020404.
   PubMed Web of Science ®Google Scholar
• Ozcan, T., and E. Eroglu. 2022. Effect of stevia and inulin interactions on fermentation profile and short-chain fatty acid production of Lactobacillus acidophilus in milk and in vitro systems. Int. J. Dairy Technol. 75 (1):171–181. doi:10.1111/1471-0307.12814.
   Web of Science ®Google Scholar
• Pérez-Chabela, M. L., and A. M. Hernández-Alcántara. 2018. Agroindustrial coproducts as sources of novel functional ingredients. In Food processing for increased quality and consumption, ed., A. M. Grumezescu and A. M. Holban. London: Academic Press. doi:10.1016/B978-0-12-811447-6.00008-4.
   Google Scholar
• Polat Yemis, G., S. Bach, and P. Delaquis. 2019. Antibacterial activity of polyphenol-rich pomegranate peel extract against Cronobacter sakazakii. Int. J. Food Prop. 22 (1):985–993. doi:10.1080/10942912.2019.1622564.
   Web of Science ®Google Scholar
• Re, R., N. Pellegrini, A. Proteggente, A. Pannala, M. Yang, and C. Rice-Evans. 1999. Antioxidant activity applying an improved ABTS radical cation decoloration assay. Free Rad. Biol. Med. 26 (9–10):1231–1237. doi:10.1016/S0891-5849(98)00315-3.
   PubMed Web of Science ®Google Scholar
• Rivas, M. Á., M. J. Benito, S. Ruíz-Moyano, A. Martín, M. G. Córdoba, A. V. Merchán, and R. Casquete. 2021. Improving the viability and metabolism of intestinal probiotic bacteria using fibre obtained from vegetable by-products. Foods 10 (9):2113. doi:10.3390/foods10092113.
   PubMed Web of Science ®Google Scholar
• Saccaro, D. M., A. Y. Tamime, A. L. O. P. S. Pilleggi, and M. N. Oliveira. 2009. The viability of three probiotic organisms grown with yoghurt starter cultures during storage for 21 days at 4 °C. Int. J. Dairy Technol. 62 (3):397–404. doi:10.1111/j.1471-0307.2009.00497.x.
   Web of Science ®Google Scholar
• Shakhmatov, E. G., E. N. Makarova, and V. A. Belyy. 2019. Structural studies of biologically active pectin-containing polysaccharides of pomegranate Punica granatum. Int. J. Biol. Macromol. 122:29–36. doi:10.1016/j.ijbiomac.2018.10.146.
   PubMed Web of Science ®Google Scholar
• Shakhmatov, E. G., P. V. Toukach, and E. N. Makarova. 2020. Structural studies of the pectic polysaccharide from fruits of Punica granatum. Carbohyd. Polym. 235:115978. doi:10.1016/j.carbpol.2020.115978.
   PubMed Web of Science ®Google Scholar
• Singh, B., J. P. Singh, A. Kaur, and N. Singh. 2018. Phenolic compounds as beneficial phytochemicals in pomegranate (Punica granatum L.) peel: A review. Food Chem. 261:75–86. doi:10.1016/j.foodchem.2018.04.039.
   PubMed Web of Science ®Google Scholar
• Singh, R. P., S. Prakash, R. Bhatia, M. Negi, J. Singh, M. Bishnoi, and K. K. Kondepudi. 2020. Generation of structurally diverse pectin oligosaccharides having prebiotic attributes. Food Hydrocollod. 108:105988. doi:10.1016/j.foodhyd.2020.105988.
   Web of Science ®Google Scholar
• Singlenton, V., and J. Rossi. 1965. Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid reagents. Am. J. Vit. Enol. 16 (3):144–158. doi:10.5344/ajev.1965.16.3.144.
   Google Scholar
• Sulieman, A. M. E., W. A. Babiker, S. B. Elhardallou, E. A. Elkhalifa, and V. N. Veettil. 2016. Influence of enrichment of wheat bread with pomegranate (Punica granatum L) peels by-products. Int. J. Food Sci. Nutr. Eng. 6 (1):9–13.
   Google Scholar
• Sun, Y., and M. X. D. O‘riordan. 2013. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv. App. Microbiol. 85:93–118. doi:10.1016/B978-0-12-407672-3.00003-4.
   PubMed Web of Science ®Google Scholar
• Viuda-Martos, M., E. Sánchez Zapata, A. Martin Sánchez, Y. Ruiz Navajas, J. Fernández López, E. Sendra, E. Sayas Barbera, C. Navarro, and J. A. Pérezálvarez. 2012. Technological properties of pomegranate peel extract obtained as coproduct of juice processing. In Dietary fiber and health, ed. S. Cho and N. Almeida, 443–452. Boca Raton: CRC Press.
   Google Scholar
• Willey, J., I. M. Sherwood, and C. J. Woolverton. 2008. Microbiología de Prescott, Harley and Klein. Madrid: Mc Graw Hill.
   Google Scholar
• Wu, D., X. Ma, and W. Tian. 2013. Pomegranate husk extract, punicalagin and ellagic acid inhibit fatty acid synthase and adipogenesis of 3T3-L1 adipocyte. J. Funct. Foods 5 (2):633–641. doi:10.1016/j.jff.2013.01.005.
   Web of Science ®Google Scholar
• Yáñez-Fernández, J., E. Ramos-Ramírez, and J. Salazar-Montoya. 2007. Rheological characterization of dispersions and emulsions used in the preparation of microcapsules obtained by interfacial polymerization containing Lactobacillus sp. Eur. Food Res. Technol. 226 (5):957–966. doi:10.1007/s00217-007-0617-9.
   Web of Science ®Google Scholar
• Yeung, T. W., I. J. Arroyo-Mata, D. J. McClements, and D. A. Sela. 2016. Microencapsulation of probiotics in hydrogel particles: Enhancing Lactococcus lactis subsp. cremoris LM0230 viability using calcium alginate beads. Food Funct. 7 (4):1797–1804. doi:10.1039/c6fo90021f.
   PubMed Web of Science ®Google Scholar
• Zuñiga, M., M. J. Yebra, and V. Monedero. 2021. Complex oligosaccharide utilization pathways in Lactobacillus. Curr. Issues Mol. Biol. 40:49–80. doi:10.21775/cimb.040.049.
   PubMed Web of Science ®Google Scholar