Table of Contents Author Guidelines Submit a Manuscript
Journal of Food Quality
Volume 2019, Article ID 3707219, 11 pages
https://doi.org/10.1155/2019/3707219
Research Article

Functional Composition, Nutritional Properties, and Biological Activities of Moroccan Spirulina Microalga

1Laboratory of Agro-Resources, Polymers and Process Engineering (LAR2PE), Department of Chemistry, Faculty of Sciences, Ibn Tofaïl University, B.P. 133, 14000 Kenitra, Morocco
2Biopharmaceutical and Toxicological Analysis Research Team, Laboratory of Pharmacology and Toxicology, Faculty of Medicine and Pharmacy, University Mohammed V, Rabat, Morocco

Correspondence should be addressed to Rajaa Seghiri; moc.liamg@irihges.aajar

Received 25 January 2019; Revised 28 April 2019; Accepted 20 May 2019; Published 3 July 2019

Academic Editor: Francisca Hernández

Copyright © 2019 Rajaa Seghiri et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. E. Blank and P. Sãnchez-baracaldo, “Timing of morphological and ecological innovations in the cyanobacteria-a key to understanding the rise in atmospheric oxygen,” Geobiology, vol. 8, no. 1, pp. 1–23, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. D. B. Stengel, S. Connan, and Z. A. Popper, “Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application,” Biotechnology Advances, vol. 29, no. 5, pp. 483–501, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. F. Shahidi, “Nutraceuticals and functional foods: whole versus processed foods,” Trends in Food Science and Technology, vol. 20, no. 9, pp. 376–387, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. F. P. Navacchi, J. C. M. De Carvalho, K. P. Takeuchi, and E. D. G. Danesi, “Development of cassava cake enriched with its own bran and Spirulina platensis,” ActaScientiarum Technology (Maringa), vol. 34, no. 4, pp. 465–472, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Spolaore, C. Joannis-Cassan, E. Duran, and A. Isambert, “Commercial applications of microalgae,” Journal of Bioscience and Bioengineering, vol. 101, no. 2, pp. 87–96, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. O. Pulz and W. Gross, “Valuable products from biotechnology of microalgae,” Applied Microbiology and Biotechnology, vol. 65, no. 6, pp. 635–648, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Li, K. Cheng, C. Wong, K. Fan, F. Chen, and Y. Jiang, “Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae,” Food Chemistry, vol. 102, no. 3, pp. 771–776, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Chamorro, M. Saläzar, K. G. Araujo, C. P. Dos Santos, G. Ceballos, and L. F. Castillo, “Update on the pharmacology of Spirulina (Arthrospira), and conventional food,” Archivos Latinoamericanos de Nutrición, vol. 52, no. 3, pp. 232–240, 2002. View at Google Scholar
  9. R. Balasubramani, S. K. Gupta, W. Cho et al., “Microalgae potential and multiple roles-current progress and future prospects-an overview,” Sustainability, vol. 8, no. 12, pp. 545-546, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. E. W. Becker, “Micro-algae as a source of protein,” Biotechnology Advances, vol. 25, no. 2, pp. 207–210, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. M. E. Gershwin and A. Belay, “Spirulina in human nutrition and health,” Journal of Applied Phycology, vol. 21, no. 6, pp. 747-748, 2009. View at Publisher · View at Google Scholar
  12. H. M. Amaro, A. C. Guedes, and F. X. Malcata, “Science against microbial pathogens: communicating current research and technological advances,” in Antimicrobial Activities of Microalgae: An Invited Review, A. Méndez-Vilas, Ed., pp. 1272–1280, 2011. View at Google Scholar
  13. R. Balasubramani, S. K. Gupta, W. Cho et al., “Microalgae potential and multiple roles-current progress and future prospects-an overview,” Sustainability, vol. 8, no. 12, pp. 545-546, 2016. View at Google Scholar
  14. T. M. Mata, A. A. Martins, and N. S. Caetano, “Microalgae for biodiesel production and other applications: a review,” Renewable and Sustainable Energy Reviews, vol. 14, no. 1, pp. 217–232, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. AACC, American Association of Cereal Chemists Approved Methods, AACC, Saint Paul, MN, USA, 8th edition, 1983.
  16. B. R. Brunner and R. D. Freed, “Oat grain β-glucan content as affected by nitrogen level, location, and year,” Crop Science, vol. 34, no. 2, pp. 473–476, 1994. View at Publisher · View at Google Scholar · View at Scopus
  17. AOAC Association of Official Analytical Chemists, Methods of Analysis for Nutrition Labeling, Airlington, TX, USA, 1993.
  18. P. J. Van Soest, J. B. Robertson, and B. A. Lewis, “Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition,” Journal of Dairy Science, vol. 74, no. 10, pp. 3583–3597, 1991. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Rinne, P. Huhtanen, and S. Jaakkola, “Grass maturity effects on cattle fed silage-based diets. 2. Cell wall digestibility, digestion and passage kinetics,” Animal Feed Science and Technology, vol. 67, no. 1, pp. 19–35, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. H. D. Chapman and P. F. Pratt, “Methods of analysis for soils, plants and waters,” in Book Review, Soil Sc, vol. 93, no. 1, pp. 162–165, 1962. View at Google Scholar
  21. M. Pinta, “Spectrométrie d’absorption atomique,” in Tom II, Application à l’Analyse Chimique, 1971. View at Google Scholar
  22. L. Duchoňová, P. Polakovičová, M. Rakická, and E. Šturdík, “Characterization and selection of cereals for preparation and utilization of fermented fiber-beta-glucan product,” Journal of Microbiology, Biotechnology and Food Sciences, vol. 2, no. 1, pp. 1384–1404, 2013. View at Google Scholar
  23. V. L. Singleton and J. A. Rossi, “Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents,” American Journal of Enology and Viticulture, vol. 16, pp. 144–153, 1965. View at Google Scholar
  24. T. Bahorun, B. Gressier, F. Trotin et al., “Oxygen species scavenging activity of phenolic extract from Hawthorn fresh plant organs and pharmaceutical preparations,” Arzneinmittel-Forschung, vol. 46, no. 11, pp. 1086–1089, 1996. View at Google Scholar
  25. Z. Liu and H. Nakano, “Antibacterial activity of spice extracts against food-related bacteria,” Journal of the Faculty of the Applied Biological Science, vol. 35, pp. 181–190, 1996. View at Google Scholar
  26. D. Lopes-Lutz, D. S. Alviano, C. S. Alviano, and P. P. Kolodziejczyk, “Screening of chemical composition, antimicrobial and antioxidant activities of Artemisia essential oils,” Phytochemistry, vol. 69, no. 8, pp. 1732–1738, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Tantaoui-Elaraki, A. Errifi, B. Benjilali, and N. Lattaoui, “Antimicrobial activity of four chemically different essential oils,” RivistaItaliana EPPOS, vol. 6, pp. 13–23, 1992. View at Google Scholar
  28. A. Remmal, T. Bouchikhi, K. Rhayour, M. Ettayebi, and A. Tantaoui-Elaraki, “Improved method for the determination of antimicrobial activity of essential oils in agar medium,” Journal of Essential Oil Research, vol. 5, no. 2, pp. 179–184, 1993. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Satrani, A. Farah, and M. Fechtal, “Composition chimique et activité antimicrobienne des huiles essentielles de Saturejacalaminthe et Satureja alpine du Maroc,” Annales des Falsifications et de l’Expertise Chimique et Toxicologique, vol. 94, no. 956, pp. 241–250, 2001. View at Google Scholar
  30. M. A. B. Habib and M. Parvin, “A review on culture, production and use of Spirulina as food for humans and feeds for domestic animals and fish,” FAO Fisheries and Aquaculture, pp. 10–34, 2008. View at Google Scholar
  31. F. F. Madkour, A. E.-W. Kamil, and H. S. Nasr, “Production and nutritive value of Spirulina platensis in reduced cost media,” The Egyptian Journal of Aquatic Research, vol. 38, no. 1, pp. 51–57, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Gouveia, A. P. Batista, I. Sousa, A. Raymundo, and N. M. Bandarra, Microalgae in Novel Food Product, 2008.
  33. E. N. Dewi, U. Amalia, and M. Mel, “The effect of different treatments to the amino acid contents of micro algae Spirulina sp,” Aquatic Procedia, vol. 7, pp. 59–65, 2016. View at Publisher · View at Google Scholar
  34. E. Christaki, P. Florou-Paneri, and E. Bonos, “Microalgae: a novel ingredient in nutrition,” International Journal of Food Sciences and Nutrition, vol. 62, no. 8, pp. 794–799, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. E. W. Becker, “Microalgae for human and animal nutrition,” in Handbook of Microalgal Culture, pp. 461–503, John Wiley & Sons, Ltd, Hoboken, NJ, USA, 2013. View at Google Scholar
  36. K. H. Wong and P. C. K. Cheung, “Nutritional evaluation of some subtropical red and green seaweeds,” Food Chemistry, vol. 71, no. 4, pp. 475–482, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Reboleira, R. Freitas, S. Pinteus et al., “Brown seaweeds,” in Nonvitamin and Nonmineral Nutritional Supplements, pp. 171–176, 2019. View at Publisher · View at Google Scholar
  38. M. G. Morais, C. C. Reichert, F. Dalcanton, A. J. Durante, L. F. Marins, and J. A. V. Costa, “Isolation and characterization of a new Arthrospira sp.,” Zeitschrift für Naturforschung C, vol. 63, no. 1-2, pp. 144–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. H. K. Maehre, L. Dalheim, G. K. Edvinsen, E. O. Elvevoll, and I. J. Jensen, “Protein determination method matters,” Foods, vol. 7, no. 1, p. 5, 2018. View at Google Scholar
  40. C. P. Wolk, “Physiology and cytological chemistry blue-green algae,” Bacteriological Reviews, vol. 37, pp. 32–101, 1973. View at Google Scholar
  41. S.M. Ametamey, M. Bruehlmeier, S. Kneifel et al., “PET studies of 18 F-memantine in healthy volunteers,” Nuclear Medicine and Biology, vol. 29, pp. 227–231, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Belay, “Spirulina (Arthrospira): production and quality assurance,” in Spirulina in Human Nutrition and Health, M. E. Gershwin and A. Belay, Eds., pp. 16–40, CRC Press, Boca Raton, FL, USA, 2008. View at Google Scholar
  43. J. Ortiz, E. Uquiche, P. Robert, N. Romero, V. Quitral, and C. Llantén, “Functional and nutritional value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis pyrifera,” European Journal of Lipid Science and Technology, vol. 111, no. 4, pp. 320–327, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Lunn and J. L. Buttriss, “Carbohydrates and dietary fibre,” Nutrition Bulletin, vol. 32, no. 1, pp. 21–64, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. O. Tokusoglu and M. K. Unal, “Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisisgalbana,” Journal of Food Science, vol. 68, no. 4, pp. 1144–1148, 2003. View at Google Scholar
  46. J. Volkman and M. Brown, “Nutritional value of microalgae and applications,” in Algal Cultures, Analogues of Blooms and Applications, D. V. Subba Rao, Ed., pp. 407–457, CABI, Wallingford, UK, 2006. View at Google Scholar
  47. P. Rupẽrez and F. Saura-Calixto, “Dietary fibre and physicochemical properties of edible Spanish seaweeds,” European Food Research and Technology, vol. 212, no. 3, pp. 349–354, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. WHO, Global Strategy on Diet, Physical Activity and Health, WHO, Geneva, Switzerland, 2004.
  49. K.-Y. Show, D.-J. Lee, and J.-S. Chang, “Algal biomass dehydration,” Bioresource Technology, vol. 135, pp. 720–729, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. N. Nicolucci, A. Monegato, and F. De Poli, “Produzioneindustriale di carta ottenuta dalle alghe in esuberonellalaguna di Venezia,” Cellulosa e Carta, vol. 5-6, pp. 41–47, 1994. View at Google Scholar
  51. C. Dawczynski, R. Schubert, and G. Jahreis, “Amino acids, fatty acids, and dietary fibre in edible seaweed products,” Food Chemistry, vol. 103, no. 3, pp. 891–899, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. P. Burtin, “Nutritional value of seaweeds,” Electronic Journal of Environmental, Agricultural and Food Chemistry, vol. 2, pp. 498–503, 2003. View at Google Scholar
  53. E. Marinho-Soriano, P. C. Fonseca, M. A. A. Carneiro, and W. S. C. Moreira, “Seasonal variation in the chemical composition of two tropical seaweeds,” Bioresource Technology, vol. 97, no. 18, pp. 2402–2406, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. P. V. S. Rao, V. A. Mantri, and K. Ganesan, “Mineral composition of edible seaweed Porphyra vietnamensis,” Food Chemistry, vol. 102, no. 1, pp. 215–218, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. S. M. Tibbetts, J. E. Milley, and S. P. Lall, “Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors,” Journal of Applied Phycology, vol. 27, no. 3, pp. 1109–1119, 2015. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Gebhardt and R. G. Thomas, Nutritive Value of Foods, vol. 95, U.S. Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory, Beltsville, MD, USA, 2002.
  57. P. Ruperez, “Mineral content of edible marine seaweeds,” Food Chemistry, vol. 79, no. 1, pp. 23–26, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Belay, “Spirulina (Arthrospira) production and quality assurance,” in Spirulina in Human Nutrition and Health, E. Gershwin and A. Belay, Eds., pp. 1–23, CRC Press, Taylor & France Group, Boca Raton, FL, USA, 2008. View at Google Scholar
  59. V. Kumar, A. K. Bhatnagar, and J. N. Srivastava, “Antibacterial activity of crude extracts of Spirulina platensis and its structural elucidation of bioactive compound,” Journal of Medicinal Plants Research, vol. 5, no. 32, pp. 7043–7048, 2011. View at Google Scholar
  60. P. Kaushik and A. Chauhan, “In vitro antibacterial activity of laboratory grown culture of Spirulina platensis,” Indian Journal of Microbiology, vol. 48, no. 3, pp. 348–352, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. T. Hirata, M. Tanaka, M. Ooike et al., “Antioxidant activities of phycocyanin prepared from Spirulina platensis,” Journal of Applied Phycology, vol. 12, no. 3-5, pp. 435–439, 2000. View at Publisher · View at Google Scholar
  62. M. Hajimahmoodi, M. A. Faramarzi, N. Mohammadi, N. Soltani, M. R. Oveisi, and N. Nafissi-Varcheh, “Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae,” Journal of Applied Phycology, vol. 22, no. 1, pp. 43–50, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. F. Ahmed, K. Fanning, M. Netzel, W. Turner, Y. Li, and P. M. Schenk, “Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters,” Food Chemistry, vol. 165, pp. 300–306, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. M. G. Morais, B. S. Vaz, E. G. Morais, and J. A. V. Costa, “Biologically active metabolites synthesized by microalgae,” BioMed Research International, vol. 2015, Article ID 835761, 15 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Connan and D. B. Stengel, “Impacts of ambient salinity and copper on brown algae: 2. Interactive effects on phenolic pool and assessment of metal binding capacity of phlorotannin,” Aquatic Toxicology, vol. 104, no. 1-2, pp. 1–13, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Safafar, J. van Wagenen, P. Møller, and C. Jacobsen, “Carotenoids, Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater,” Marine Drugs, vol. 13, no. 12, pp. 7339–7356, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. R. A. Kepekçi and S. D. Saygideger, “Enhancement of phenolic compound production in Spirulina platensis by two-step batch mode cultivation,” Journal of Applied Phycology, vol. 24, no. 4, pp. 897–905, 2012. View at Publisher · View at Google Scholar · View at Scopus
  68. I. Jerez-Martel, S. García-Poza, G. Rodríguez-Martel, M. Rico, C. Afonso-Olivares, and J. L. Gómez-Pinchetti, “Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains,” Journal of Food Quality, vol. 2017, Article ID 2924508, 8 pages, 2017. View at Google Scholar
  69. F. A. Pognussatt, E. M. Del Ponte, J. Garda-Buffon, and E. Badiale-Furlong, “Inhibition of Fusarium graminearum growth and mycotoxin production by phenolic extract from Spirulina sp,” Pesticide Biochemistry and Physiology, vol. 108, pp. 21–26, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. F. A. Pagnussatt, V. R. De Lima, C. L. Dora, J. A. V. Costa, J.-L. Putaux, and E. Badiale-Furlong, “Assessment of the encapsulation effect of phenolic compounds from Spirulina sp. LEB-18 on their antifusarium activities,” Food Chemistry, vol. 211, no. 211, pp. 616–623, 2016. View at Publisher · View at Google Scholar · View at Scopus
  71. P. Piñero-Estrada, P. Bermejo-Bescos, and A. M. Villar del Fresno, “Antioxidant activity of different fractions of Spirulina platensis protean extract,” II Farmaco, vol. 56, no. 5-7, pp. 497–500, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. W. L. Chu, Y. W. Lim, A. K. Radhakrishnan, and P. E. Lim, “Protective effect of aqueous extract from Spirulina platensis against cell death induced by free radicals,” BMC Complementary and Alternative Medicine, vol. 10, no. 53, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. T. W. Agustini, M. Suzery, D. Sutrisnanto, W. F. Ma’ruf, and Hadiyanto, “Comparative study of bioactive substances extracted from fresh and dried Spirulina sp,” Procedia Environmental Sciences, vol. 23, pp. 282–289, 2015. View at Publisher · View at Google Scholar
  74. M. Hetta, R. Mhmoud, W. El-Senousy, M. Ibrahim, G. El-Taweel, and G. Ali, “Antiviral and antimicrobial activities of Spirulina platensis,” World Journal of Pharmaceutical Sciences, vol. 3, pp. 31–39, 2014. View at Google Scholar
  75. J. A. Ross and C. M. Kasum, “Dietary flavonoids: bioavailability, metabolic effects, and safety,” Annual Review of Nutrition, vol. 22, no. 1, pp. 19–34, 2002. View at Publisher · View at Google Scholar · View at Scopus
  76. C. M. M. Sousa, H. R. Silva, G. M. Vieira Jr. et al., “Fenóis totais e atividade antioxidante de cinco plantas medicinais,” Química Nova, vol. 30, no. 2, pp. 351–355, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Xue, Y. Hu, H. Saito et al., “Molecular species composition of glycolipids from Sprirulina platensis,” Food Chemistry, vol. 77, no. 1, pp. 9–13, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. Y. Shai, “Mode of action of membrane active antimicrobial peptides,” Biopolymers, vol. 66, no. 4, pp. 236–248, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. M. F. Ramadan, M. M. S. Asker, and Z. K. Ibrahim, “Functional bioactive compounds and biological activities of Spirulina platensis lipids,” Czech Journal of Food Sciences, vol. 26, no. 3, pp. 211–222, 2008. View at Publisher · View at Google Scholar
  80. J. A. Mendiola, L. Jaime, S. Santoyo et al., “Screening of functional compounds in supercritical fluid extracts from Spirulina platensis,” Food Chemistry, vol. 102, no. 4, pp. 1357–1367, 2007. View at Publisher · View at Google Scholar · View at Scopus