Impact of enzyme- and ultrasound-assisted extraction methods on biological properties of red, brown, and green seaweeds from the Central West Coast of Portugal

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 12, 2015, Pages 3177-3188

  Rodrigues, Dina ^a   Sousa, Sérgio ^b   Silva, Aline ^b   Amorim, Manuela ^b   Pereira, Leonel ^c   Rocha Santos, Teresa A P ^a,d   Gomes, Ana M P ^b   Duarte, Armando C ^a   Freitas, Ana Cristina ^a,d  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSIDADE CATÓLICA PORTUGUESA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d INSTITUTO PIAGET   (Portugal)

Author keywords

biological properties; Codium tomentosum; Osmundea pinnatifida; Sargassum muticum; water based extraction

Indexed keywords

ENZYMES; PYRENE; SEAWEED; ULTRASONICS;

BIOLOGICAL PROPERTIES; CODIUM TOMENTOSUM; OSMUNDEA PINNATIFIDA; SARGASSUM MUTICUM; WATER BASED EXTRACTION;

EXTRACTION;

CODIUM TOMENTOSUM; OSMUNDEA PINNATIFIDA; SARGASSUM MUTICUM;

ANTIOXIDANT; CELLULASE; PLANT EXTRACT; PREBIOTIC AGENT;

CHEMISTRY; COMPARATIVE STUDY; GREEN ALGA; ISOLATION AND PURIFICATION; PORTUGAL; PROCEDURES; RED ALGA; SARGASSUM; SEAWEED; ULTRASOUND; VEGETABLE;

ANTIOXIDANTS; CELLULASE; CHLOROPHYTA; PLANT EXTRACTS; PORTUGAL; PREBIOTICS; RHODOPHYTA; SARGASSUM; SEAWEED; ULTRASONICS; VEGETABLES;

EID: 84926283808     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf504220e     Document Type: Article

References (56)

1. Holdt, S. L.; Kraan, S. Bioactive compounds in seaweed: functional food applications and legislation J. Appl. Phycol. 2011, 23, 543-597
2. Ibañez, E.; Cifuentes, A. Benefits of using algae as natural sources of functional ingredients J. Sci. Food Agric. 2013, 93, 703-709
3. Pangestuti, R.; Kim, S.-K. Biological activities and health benefit effects of natural pigments derived from marine algae J. Funct. Foods 2011, 3, 255-266
4. El Gamal, A. A. Biological importance of marine algae Saudi Pharm. J. 2010, 18, 1-25
5. Jeon, Y.-J.; Wijesinghe, W. A. J. P.; Kim, S.-K. Biotechnology and applied phycology. In Handbook of Marine Macroalgae; Kim, S.-K., Ed.; Wiley-Blackwell: Chichester, UK, 2012; online ISBN 978-0-470-97918-1.
6. Herrero, M.; Cifuentes, A.; Ibañez, E. Sub- and supercritical fluid extraction of functional ingredients from different natural sources: plants, food-by-products, algae and microalgae Food Chem. 2006, 98, 136-148
7. Heo, S.-J.; Jeon, Y.-J.; Lee, J.; Kim, H. T.; Lee, K.-W. Antioxidant effect of enzymatic hydrolyzate from a kelp, Ecklonia cava Algae 2003, 18, 341-347
8. Gil-Chávez, G. J.; Villa, J. A.; Ayala-Zavala, J. F.; Heredia, J. B.; Sepulveda, D.; Yahia, E. M.; González-Aguilar, G. A. Technologies for extraction and production of bioactive compounds to be used as nutraceuticals and food ingredients: an overview Compr. Rev. Food Sci. Food Saf. 2013, 12, 5-23
9. Wang, T.; Jónsdóttir, R.; Kristinsson, H. G.; Hreggvidsson, G. O.; Jónsson, J. O.; Thorkelsson, G.; Ólafsdóttir, G. Enzyme-enhanced extraction of antioxidant ingredients from red algae Palmaria palmate LWT-Food Sci. Technol. 2010, 43, 1387-1393
10. Domozych, D. S. Algal cell walls. In eLS; Wiley: Chichester, UK, 2011. http://www.els.net [DOI: 10.1002/9780470015902.a0000315.pub3 ].
11. Wijesinghe, W. A. J. P.; Jeon, Y.-J. Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review Fitoterapia 2012, 83, 6-12
12. Hardouin, K.; Burlot, A.-S.; Umami, A.; Tanniou, A.; Stiger-Pouvreau, V.; Widowati, I.; Bedoux, G.; Bourgougnon, N. Biochemical and antiviral activities of enzymatic hydrolysates from different invasive French seaweeds J. Appl. Phycol. 2014, 26, 1029-1042
13. Hahn, T.; Lang, S.; Ulber, R.; Muffler, K. Novel procedures for the extraction of fucoidan from brown algae Process Biochem. 2012, 47, 1691-1698
14. Kadam, S. U.; Tiwari, B. K.; O'Donnell, C. P. Application of novel extraction technologies for bioactives from marine algae J. Agric. Food Chem. 2013, 61, 4667-4675
15. Chandini, S. K.; Ganesan, P.; Bhaskar, N. In vitro antioxidant activities of three selected brown seaweeds of India Food Chem. 2008, 107, 707-713
16. Je, J.-Y.; Park, P.-J.; Kim, E.-K.; Park, J.-S.; Yoon, H.-D.; Kim, K.-R.; Ahn, C.-B. Antioxidant activity of enzymatic extracts from the brown seaweed Undaria pinnatifida by electron spin resonance spectroscopy LWT-Food Sci. Technol. 2009, 42, 874-878
17. Tanniou, A.; Vandanjon, L.; Incera, M.; Leon, E. S.; Husa, V.; Le Grand, J.; Nicolas, J.-L.; Poupart, N.; Kervarec, N.; Engelen, A.; Walsh, R.; Guerard, F.; Bourgougnon, N.; Stiger-Pouvreau, V. Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum samples along it European range from Norway to Portugal J. Appl. Phycol. 2014, 26, 1215-1230
18. Heo, S.-J.; Park, E.-J.; Lee, K.-W.; Jeon, Y.-J. Antioxidant activities of enzymatic extracts from brown seaweeds Bioresour. Technol. 2005, 96, 1613-1623
19. Farvin, K. H. S.; Jacobsen, C. Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast Food Chem. 2013, 138, 1670-1681
20. Al-Sheraji, S. H.; Ismail, A.; Manap, M. Y.; Mustafa, S.; Yusof, R. M.; Hassan, F. A. Prebiotics as functional foods: a review J. Funct. Foods 2013, 5, 1542-1553
21. Ali, H.; Houghton, P. J.; Soumyanath, A. α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus J. Ethnopharmacol. 2006, 107, 449-455
22. Senthil, S. L.; Kumar, T. V.; Geetharamani, D.; Maruthupandi, T. Screening of seaweeds collected from southeast coastal area of India for α-amylase inhibitory activity, antioxidant and biocompatibility Int. J. Pharm. Pharm. Sci. 2013, 5, 240-244
23. Guiry, M. D.; Guiry, G. M. AlgaeBase; National University of Ireland: Galway, 2013; http://www.algaebase.org (accessed June 6, 2013).
24. Huang, S.-Q.; Li, J.-W.; Wang, Z.; Pan, H.-X.; Chen, J. X.; Ning, Z.-X. Optimization of alkaline extraction of polysaccharides from Ganoderma lucidum and their effect on immune function in mice Molecules 2010, 15, 3694-3708
25. Dubois, M.; Gilles, K. A.; Hamilton, J. K.; Rebers, R. A.; Smith, F. Colorimetric method for determination of sugars and related substances Anal. Chem. 1956, 28, 350-356
26. Dodgson, K. S. Determination of inorganic sulphate in studies on the enzymic and non-enzymic hydrolysis of carbohydrate and other sulphate esters Biochem. J. 1961, 78, 312-319
27. Mulinacci, N.; Romani, A.; Galardi, C.; Pinelli, P.; Giaccherini, C.; Vincieri, F. F. Polyphenolic content in olive oil waste waters and related olive samples J. Agric. Food Chem. 2001, 49, 3509-3514
28. Gião, M. S.; González-Sanjosé, M. L.; Rivero-Pérez, M. D.; Pereira, C. I.; Pintado, M. E.; Malcata, F. X. Infusions of Portuguese medicinal plants: dependence of final antioxidant capacity and phenol content on extraction features J. Sci. Food Agric. 2007, 87, 2638-2647
29. Suresh, V.; Senthilkumar, N.; Thangam, R.; Rajkumarc, M.; Anbazhagana, C.; Rengasamy, R.; Gunasekaran, P.; Kannan, S.; Palani, P. Separation, purification and preliminary characterization of sulfated polysaccharides from Sargassum plagiophyllum and its in vitro anticancer and antioxidant activity Process Biochem. 2013, 48, 364-373
30. Sudha, G.; Priya, M. S.; Shree, R. I.; Vadivukkarasi, S. In vitro free radical scavenging activity of raw pepino fruit (Solanum muricatum Aiton) Int. J. Curr. Pharm. Res. 2011, 3, 137-140
31. Smirnoff, N.; Cumbes, Q. J. Hydroxyl radical scavenging activity of compatible solutes Phytochemistry 1989, 28, 1057-1060
32. Fiorentino, A.; D'Abrosca, B.; Pacifico, S.; Golino, A.; Mastellone, C.; Oriano, P.; Monaco, P. Reactive oxygen species scavenging activity of flavone glycosides from Melilotus neapolitana Molecules 2007, 12, 263-270
33. Miles, A. A.; Misra, S. S. The estimation of the bactericidal power of the blood J. Hyg. 1938, 38, 732-749
34. Kwon, Y.-I.; Apostolidis, E.; Shetty, K. In vitro studies of eggplant (Solanum melongena) phenolics as inhibitors of key enzymes relevant for type 2 diabetes and hypertension Bioresour. Technol. 2008, 99, 2981-2988
35. Rodrigues, D.; Freitas, A. C.; Pereira, L.; Rocha-Santos, T. A. P.; Vasconcelos, M. W.; Roriz, M.; Rodríguez-Alcalá, L. M.; Gomes, A. M. P.; Duarte, A. C. Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chem. 2014, DOI: 10.1016/j.foodchem.2015.03.057.
36. Plaza, M.; Amigo-Benavent, M.; del Castillo, M. D.; Ibáñez, E.; Herrero, M. Facts about the formation of new antioxidants in natural samples after subcritical water extraction Food Res. Int. 2010, 43, 2341-2348
37. Cian, R. E.; Alaiz, M.; Vioque, J.; Drago, S. R. Enzyme proteolysis enhanced extraction of ACE inhibitory and antioxidant compounds (peptides and polyphenols) from Porphyra columbina residual cake J. Appl. Phycol. 2013, 25, 1197-1206
38. Chemat, F.; Zill-e-Huma; Khan, M. K. Applications of ultrasound in food technology: processing, preservation and extraction Ultrason. Sonochem. 2011, 18, 813-835
39. Zhao, L.; Zhao, G.; Chen, F.; Wang, Z.; Wu, J.; Hu, X. Different effects of microwave and ultrasound on the stability of (all- E)-astaxanthin J. Agric. Food Chem. 2006, 54, 8346-8351
40. Lee, S.-H.; Kang, M.-C.; Moon, S.-H.; Jeon, B.-T.; Jeon, Y.-J. Potential use of ultrasound in antioxidant extraction from Ecklonia cava Algae 2013, 28, 371-378
41. Ale, M. T.; Meyer, A. S. Fucoidans from brown seaweeds: an update on structures, extraction techniques and use of enzymes as tools for structural elucidation RSC Adv. 2013, 3, 8131-8141
42. Guiry, M. D. The seaweed site: information on marine algae. http://www.seaweed.ie/uses-general/alginates.php (accessed April 10, 2014).
43. Shanmugan, M.; Mody, K. H. Heparinoid-active sulphated polysaccharides from marine algae as potential blood anticoagulant agents Curr. Sci. 2000, 79, 1672-1683
44. Jiménez-Escrig, A.; Gómez-Ordóñez, E.; Rupérez, P. Brown and red seaweeds as potential sources of antioxidant nutraceuticals J. Appl. Phycol. 2012, 24, 1123-1132
45. Budhiyanti, S. A.; Raharjo, S.; Marseno, D. W.; Lelana, I. Y. B. Antioxidant activity of brown algae Sargassum species extract from the coastline of Java Island Am. J. Agric. Biol. Sci. 2012, 7, 337-346
46. Freitas, A. C.; Andrade, J. C.; Silva, F. M.; Rocha-Santos, T. A. P.; Duarte, A.; Gomes, A. M. Antioxidative peptides: trends and perspectives for future research Curr. Med. Chem. 2013, 20, 4575-4594
47. Karadag, A.; Ozcelik, B.; Saner, S. Review of methods to determine antioxidant capacities Food Anal. Methods 2009, 2, 41-60
48. Balboa, E. M.; Conde, E.; Moure, A.; Falque, E.; Dominguez, H. In vitro antioxidant properties of crude extracts and compounds from brown algae Food Chem. 2013, 138, 1764-1785
49. Yangthong, M.; Hutadilok-Towatana, N.; Phromkunthong, W. Antioxidant activities of four edible seaweeds from the southern coast of Thailand Plant Foods Hum. Nutr. 2009, 64, 218-223
50. Zhao, X.; Li, B.; Xue, C.; Sun, L. Effect of molecular weight on the antioxidant property of low molecular weight alginate from Laminaria japonica J. Appl. Phycol. 2012, 24, 295-300
51. Valentão, P.; Trindade, P.; Gomes, D.; de Pinho, P. G.; Mouga, T.; Andrade, P. B. Codium tomentosum and Plocamium cartilagineum: chemistry and antioxidant potential Food Chem. 2010, 119, 1359-1368
52. Zaporozhets, T. S.; Besedova, N. N.; Kuznetsova, T. A.; Zvyagintseva, T. N.; Makarenkova, I. D.; Kryzhanovsky, S. P.; Melnikov, V. G. The prebiotic potential of polysaccharides and extracts from seaweeds Russ. J. Mar. Biol. 2014, 40, 1-9
53. Ramnani, P.; Chitarrari, R.; Tuohy, K.; Grant, J.; Hotchkiss, S.; Philp, K.; Campbell, R.; Gill, C.; Rowland, I. In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds Anaerobe 2012, 18, 1-6
54. Wu, S.-C.; Kang, S.-K.; Kazlowski, B.; Wu, C.-J.; Pan, C.-L. Antivirus and prebiotic properties of seaweed-oligosaccharides lysates derived from agarase AS-II J. Fish. Soc. Taiwan 2012, 39, 11-21
55. Hardoko; Siratantri, T.; Eveline; Yogabuana, M.; Olivia, S. Na in vitro of antidiabetic activity of Sargassum duplicatum and Turbinaria decurens seaweed Int. J. Pharm. Sci. Invent. 2014, 3, 13-18
56. Motshakeri, M.; Ebhrahimi, M.; Goh, Y. M.; Othman, H. H.; Hair-Bejo, M.; Mohamed, S. Effects of brown seaweed (Sargassum polycystum) extracts on kidney, liver, and pancreas of type 2 diabetic rat model Evidence-Based Complement. Altern. Med. 2014, 1-11