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Anti-cholesterol and Antioxidant Activities of Independent and Combined Microalgae Aqueous Extracts In Vitro

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Abstract

Algae are used as one of important medical sources for its therapeutic properties; and edible algae are acknowledged as complete foods which provide right balance of proteins, carbohydrates, vitamins, mineral salts, carotenoids, and antioxidants. The aim of the current study was to evaluate hot-water extracts of different marine microalgae species (Spirulina platensis, Anabaena oryzae, Scenedesmus obliquus and Chlorella vulgaris) in vitro for their cholesterol-lowering activity, individually or in combinations. The algal extracts (AEs) were prepared from different marine microalgae species and their in vitro anti-cholesterol activities were assessed spectrophotometrically. The algal growth and their bioactive constituents (polyphenol content, antioxidant capacity and tannin content) were quantified using Folin-Ciocalteu, DPPH, vanillin-HCl assays, respectively. The highest value of the biomass concentration (1.367 g) was recorded for S. platensis in 1000 mL of culture media after 21 days. Increasing anti-cholesterol activity by S. platensis extract was observed up to 60 min at a concentration of 15 mg/mL and a highest inhibition was found as 76.01% value (p < 0.05). The combined extracts from S. platensis with C. vulgaris showed maximum cholesterol-lowering effect (77.95%) value (p < 0.05), after the same incubation period. The phytochemical screening indicated the presence of tannins in all algal extracts, with highest tannin contents in S. platensis (4.66 μg TAE/g DW), followed by A. oryzae with (2.99 μg/g) and S. obliquus (2.13 μg/g), A. oryzae extract contained the highest concentration of phenolic compounds (503.67 μg GAE/g). The highest antioxidant activity was obtained by S. platensis extract (92.66%) value (p < 0.05) at 15 mg/mL, while the least one was observed by S. obliquus (16.81%). The extract of S. platensis, used individually or combined with C. vulgaris extract, is recommended as natural bioactive source, with anti-cholesterol and antioxidant potentialities.

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References

  1. Ohvo-Rekilä, H., Ramstedt, B., Leppimäki, P., Slotte, J.P.: Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 41(1), 66–97 (2002)

    Article  Google Scholar 

  2. Harvey, R.A., Ferrier, D.R.: Lippincott’s Illustrated Reviews: Biochemistry, 5th edn. Lippincott Williams & Wilkins, a Wolters Kluwer business. ISBN 978-1-60831-412-6 (2011)

  3. Van der Wulp, M.Y., Verkade, H.J., Groen, A.K.: Regulation of cholesterol homeostasis. Mol. Cell. Endocrinol. 368(1–2), 1–16 (2013). https://doi.org/10.1016/j.mce.2012.06.007

    Article  Google Scholar 

  4. Berger, S., Raman, G., Vishwanathan, R., Jacques, P.F., Johnson, E.J.: Dietary cholesterol and cardiovascular disease: a systematic review and meta-analysis. Am. J. Clin. Nutr. 102(2), 276–294 (2015)

    Article  Google Scholar 

  5. Mendis, S., Puska, P., Norrving, B.: Global Atlas on Cardiovascular Disease Prevention and Control. World Health Organization in Collaboration with the World Heart Federation and the World Stroke Organization, Geneva (2011)

    Google Scholar 

  6. Yamada, K., Tokunaga, Y., Ikeda, A., Ohkura, K., Kaku-Ohkura, S., Mamiya, S., Lim, B.O., Tachibana, H.: Effect of dietary fiber on the lipid metabolism and immune function of aged Sprague-Dawley rats. Biosci. Biotechnol. Biochem. 67, 429–433 (2003)

    Article  Google Scholar 

  7. De Smet, E., Mensink, R.P., Plat, J.: Effects of plant sterols and stanols on intestinal cholesterol metabolism: suggested mechanisms from past to present. Mol. Nutr. Food Res. 56(7), 1058–1072 (2012). https://doi.org/10.1002/mnfr.201100722

    Article  Google Scholar 

  8. Laden, B.P., Porter, T.D.: Resveratrol inhibits human squalene monooxygenase. Nutr. Res. 21(5), 747–753 (2001)

    Article  Google Scholar 

  9. Abe, I., Seki, T., Umehara, K., Miyase, T., Noguchi, H., Sakakibara, J., Ono, T.: Green tea polyphenols: novel and potent inhibitors of squaleneepoxidase. Biochem. Biophys. Res. Commun. 268(3), 767–771 (2000)

    Article  Google Scholar 

  10. Reichelt, J.L., Borowitzka, M.A.: Antimicrobial activity from marine alga: results of 393 a large scale screening programme. Hydrobiologia. 116(117), 158–168 (1984)

    Article  Google Scholar 

  11. Habib, M.A., Parvin, M., Huntington, T.C., Hassan, M.R.: A Review on Culture, Production and Use of Spirulina as Foods for Humans and Feeds for Domestic Animals and Fish FAO Fisheries and Aquaculture Circular. No:1034, p. 33. FAO, Rome (2008) ISBN 978-92-5-106106-0

    Google Scholar 

  12. Plaza, M., Cifuentes, A., Ibanez, E.: In the search of new functional food ingredients from algae. Trends Food Sci. Technol. 19(1), 31–39 (2008)

    Article  Google Scholar 

  13. Muthuraman, P., Senthilkumar, R., Srikumar, K.: Alterations in beta-islets of Langerhans in alloxan-induced diabetic rats by marine Spirulina platensis. J. Enzyme Inhib. Med. Chem. 24(6), 1253–1256 (2009)

    Article  Google Scholar 

  14. Lee, R.E.: Phycology, 4th edn. Cambridge university press, Cambridge. ISBN: 978-0-521-68277-0 (2008)

    Book  Google Scholar 

  15. Fawzy, M.A., Issa, A.A.: Bioremoval of heavy metals and nutrients from sewage plant by Anabaena oryzae and Cyanosarcina Fontana. Int. J. Phytoremediation. 18(4), 321–328 (2016). https://doi.org/10.1080/15226514.2015.1094448

    Article  Google Scholar 

  16. Brown, M.R., Hohmann, S.: Effects of irradiance and growth phase on the ascorbic acid content of Isochrysis sp. T.ISO (Prymnesiophyta). J. Appl. Phycol. 14, 211–214 (2002)

    Article  Google Scholar 

  17. Christenson, L., Sims, R.: Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol. Adv. 29(6), 686–702 (2011). https://doi.org/10.1016/j.biotechadv.2011.05.015

    Article  Google Scholar 

  18. Hosoyamada, Y., Takai, T., Kato, T.: Effects of water-soluble and insoluble fractions of Spirulina on serum lipid components and glucose tolerance in rats. J. Jpn. Soc. Nutr. Food. Sci. 44, 273–277 (1991)

    Article  Google Scholar 

  19. Afify, A.M.R., El Baroty, G.S., El Baz, F.K., Abd El Baky, H.H., Murad, S.A.: Scenedesmus obliquus: antioxidant and antiviral activity of proteins hydrolyzed by three enzymes. J. Genetic Eng. Biotechnol. 16, 399–408 (2018)

    Article  Google Scholar 

  20. Sano, T., Kumamoto, Y., Kamiya, N., Okuda, M., Tanaka, Y.: Effect of lipophilic extract of Chlorella vulgaris on alimentary hyperlipidemia in cholesterol-fed rats. Artery. 15(4), 217–224 (1988)

    Google Scholar 

  21. Chovanèíková, M., Šimek, V.: Effects of high-fat and Chlorella vulgaris feeding on changes in lipid metabolism in mice. Biol. Bratislava. 56(6), 661–666 (2001)

    Google Scholar 

  22. Hamouda, R.A., Sorour, N.M., Yehheia, D.S.: Biodegradation of crude oil by Anabaena oryzae, Chlorella kessleri and its consortium under mixotrophic conditions. Int. Biodeterioration Biodegredation. 112, 128–134 (2016)

    Article  Google Scholar 

  23. Bellinger, E., Sigee, D.: Freshwater Algae: Identification and Use as Bioindicators, p. 495. Wiley, New York (2010)

    Book  Google Scholar 

  24. Stevenson, R.J., Lowe, R.L.: Sampling and interpretation of algal patterns for water quality assessment. In: Isom, B.G. (ed.) Rationale for Sampling and Interpretation of Ecological Data in the Assessment of Freshwater Ecosystems ASTM STP 894, pp. 118–149. American Society for Testing and Materials, Philadelphia (1986)

    Chapter  Google Scholar 

  25. Zarrouk, C.: Contribution a létude d'une cyanobacterie: influence de divers facteurs physiques et chimiques sur lacroissance et la photosynthése de Spirulina maxima (Setch et Gardner) Geitler. Ph.D. thesis, University of Paris, France (1966)

  26. Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G.: Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35(2), 171–205 (1971)

    Article  Google Scholar 

  27. Rippka, R., Deruelles, J., Waterbury, J., Herdman, M., Stanier, R.: Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1–61 (1979). https://doi.org/10.1099/00221287-111-1-128

    Article  Google Scholar 

  28. Kuhl, A., Lorenzen, H.: Handling and culturing of Chlorella. In: Prescott, D.M. (ed.) Methods in Cell Physiology, vol. I, pp. 152–187. Academic Press, New York/London (1964)

    Google Scholar 

  29. Sharma, R., Singh, G.P., Sharma, V.K.: Effects of culture conditions on growth and biochemical profile of Chlorella Vulgaris. J. Plant. Pathol. Microb. 3(5), 131–133 (2012)

    Article  Google Scholar 

  30. Wetherell, D.F.: Culture of fresh water algae in enriched natural seawater. Plant Physiol. 14(1), 1–6 (1961) doc. https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1399-3054.1961.tb08131.x

    Article  MathSciNet  Google Scholar 

  31. Nigam, V.K., Verma, R., Kumar, A., Kundu, S., Ghosh, P.: Influence of medium constituents on the biosynthesis of cephalosporin-C. Electron J Biotechnol. (2007). https://doi.org/10.2225/vol10-issue2-fulltext-8

  32. Hamouda, R.A., Al-Saman, M.A., El-Sabbagh, S.M., Abo El-Seoud, G.W., Hendawy, A.N.: Approach to improve the productivity of bioactive compounds of the cyanobacterium Anabaena oryzae using factorial design. Egyp. Jour. Bas. App. Sci. 4(3), 190–195 (2017). https://doi.org/10.1155/2014/253875

    Article  Google Scholar 

  33. Richmond, W.: Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin. Chem. 19(12), 1350–1356 (1973)

    Article  Google Scholar 

  34. Pant, G., Simaria, C., Varsi, R.A.H., Bhan, P., Sibi, G.: In vitro anti-cholesterol and antioxidant activity of Methanolic extracts from flax seeds (Linum usitatissimum L.). Res. J. Med. Plant. 9(6), 300–306 (2015)

    Article  Google Scholar 

  35. Slinkard, K., Singleton, V.L.: Total phenol analyses: automation and comparison with manual methods. Am. J. Enol. Vitic. 28, 49–55 (1977)

    Article  Google Scholar 

  36. Chandra, S., Khan, S., Avula, B., Lata, H., Yang, M.H., El-Sohly, M.A., Khan, I.A.: Assessment of Total Phenolic and Flavonoid Content, Antioxidant Properties, and Yield of Aeroponically and Conventionally Grown Leafy Vegetables and Fruit Crops: a Comparative Study, p. 9. Hindawi Publishing Corporation Evidence-Based Complementary and Alternative Medicine. ID 253875, London (2014)

    Google Scholar 

  37. Earp, C.F., Akingbala, J.O., Ring, S.H., Rooney, L.W.: Evaluation of several methods to determine tannins in sorghums with varying kernel characteristics. Cereal Chem. 58(3), 234–238 (1981)

    Google Scholar 

  38. Sokal, R.R.: The principles and practice of statistics in biological research. Biometry. 39, 451–554 (1995)

    Google Scholar 

  39. Ilavarasi, A., Mubarakali, D., Praveenkumar, R., Baldev, E., Thajuddin, N.: Optimization of various growth media to freshwater microalgae for biomass production. Biotechnology. 10, 540–545 (2011)

    Article  Google Scholar 

  40. Kebede, E., Ahlgren, G.: Optimum growth conditions and light utilization efficiency of Spirulina platensis (= Arthrospira fusiformis) (Cyanophyta) from Lake Chitu. Ethiopia Hydrobiol. 332(2), 99–109 (1996)

    Article  Google Scholar 

  41. Sharma, R., Singh, G.P., Sharma, V.K.: Comparison of different media formulations on growth, morphology and chlorophyll content of green alga, Chlorella vulgaris. Int J Pharm. Bio. Sci. 2, 509–516 (2011)

    Google Scholar 

  42. Singh, G., Chauhan, V.S., Ramamurthy, V.: Effect of continuous and cyclic illumination on the growth of different Spirulina isolates. Microbios. 99(393), 83–88 (1999)

    Google Scholar 

  43. João, A., Manoel, C., Ranglová, K., Grivalský, T., Gergely, E.: Lakatos and Jiří Masojídek photosynthetic performance of green microalgae grown in centrate at light/dark and continuous illumination regime conference: 27th European Biomass conference and Exhibition )2019(

  44. Simopoulos, A.P.: Omega-3 essential fatty acid ratio and chronic diseases. Food Rev. Int. 20, 77–90 (2004)

    Article  Google Scholar 

  45. Sanchez-Machado, D.I., Lopez-Hernandez, J., Paseiro-Losada, P., Lopez-Cervantes, J.: An HPLC method for the quantification of sterols in edible seaweeds. Biomed. Chromatogr. 18(3), 183–190 (2004)

    Article  Google Scholar 

  46. Karkos, P.D., Leong, S.C., Karkos, C.D., Sivaji, N., Assimakopoulos, D.A.: Spirulina in clinical practice: evidence-based human applications. Evid. Based Complement. Alternat. Med. 2011(4) (2008) doc: https://doi.org/10.1093/ecam/nen058

  47. Kose, A., Ozen, M.O., Elibol, M., Oncel, S.S.: Investigation of in vitro digestibility of dietary microalga Chlorella vulgaris and cyanobacterium Spirulina platensis as a nutritional supplement. 3 Biotech. 7(3), 170 (2017)

    Article  Google Scholar 

  48. Belasco, W.: Algae burgers for a hungry world? The rise and fall of Chlorella cuisine. Technol. Cult. 38(3), 608–634 (1997) (https://doi.org/10.2307%2F3106856). JSTOR 3106856 (https://www.jstor.org/stable/3106856)

    Article  Google Scholar 

  49. Santhosh, S., Dhandapani, R., Hemalatha, N.: Bioactive compounds from microalgae and its different applications – a review. Adv. Appl. Sci. Res. 7, 153–158 (2016)

    Google Scholar 

  50. Kulshreshtha, A., Zacharia, A.J., Jarouliya, U., Bhadauriya, P., Prasad, G.B., Bisen, P.S.: Spirulina in health care management. Curr. Pharm. Biotechnol. 9(5), 400–405 (2008)

    Article  Google Scholar 

  51. El-Chaghaby, G.A., Rashad, S., Abdel-Kader, S.F., Rawash, E.A., Abdul Moneem, M.: Assessment of phytochemical components, proximate composition and antioxidant properties of Scenedesmus obliquus, Chlorella vulgaris and Spirulina platensis algae extracts. Egyptian J. Aquatic Biol. Fish. 23(4), 521–526 (2019)

    Article  Google Scholar 

  52. Rolle, I., Pabst, W.: Uber die cholesterinsenkende Wirkung der einzelligen Grunalge Scenedesmus acutus 276-3a. Nutr. Metab. 24, 291–301 (1980)

    Article  Google Scholar 

  53. Colla, L.M., Muccillo-Baisch, A.L., Costa, J.A.V.: Spirulina platensis effects on the levels of total cholesterol, HDL and triacylglycerols in rabbits fed with a hypercholesterolemic diet. Braz. Arch. Biol. Technol. 51(2), 405–411 (2008)

    Article  Google Scholar 

  54. Şahin, S., Işık, E., Demir, C., Prediction of total phenolic content in extracts of Prunella species from HPLC profiles by multivariate calibration. J. Int. Scholarly Res. Notices 2012, 120780, 7 (2012) https://doi.org/10.5402/2012/120780

  55. Eberhardt, M.V., Lee, C.Y., Liu, R.H.: Antioxidant activity of fresh apples. Nature. 405, 903–904 (2000)

    Article  Google Scholar 

  56. Balasundram, N., Sundram, K., Samman, S.: Phenolic compounds in plants and agriindustrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem. 99(1), 191–203 (2006)

    Article  Google Scholar 

  57. Colell, A., Marí, M., Morales, A., von Montfort, C., Garcia-Ruiz, C., Fernández-Checa, J.C.: Redox control of liver function in health and disease. Antioxid. Redox Signal. 12(11), 1295–1331 (2010). https://doi.org/10.1089/ars.2009.2634

    Article  Google Scholar 

  58. Furlan, C.M., Motta, L.B., Santos, D.Y.: Tannins: What Do they Represent in Plant Life? Nova Science Publishers, New York. ISBN: 978-1-61761-127-8 (2014)

    Google Scholar 

  59. Yoon, N.Y., Kim, H.R., Chung, H.Y., Choi, J.S.: Anti-hyperlipidemic effect of an edible brown algae, Ecklonia stolonifera, and its constituents on poloxamer 407-induced hyperlipidemic and cholesterol-fed rats. Arch. Pharm. Res. 31(12), 1564–1571 (2008). https://doi.org/10.1007/s12272-001-2152-8

    Article  Google Scholar 

  60. Abd El Mageid, M.M., Salama, N.A., Saleh, M.A.M., Abo Taleb, H.M.: Antioxidant and antimicrobial characteristics of red and brown algae extracts. 4th Conference on Recent Technologies in Agriculture, 818–827 (2009)

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Authors and Affiliations

  1. Department of Industrial Biotechnology, Genetic Engineering and Biotechnology Research Institute, University of Sadat City, Sadat City, Egypt

    Mohamed R. Ibrahim & Mahmoud A. Al-Saman

  2. Department of Biology, Faculty of Sciences and Arts, University of Jeddah, Jeddah, Saudi Arabia

    Ragaa A. Hamouda

  3. Department of Microbial Biotechnology, Genetic Engineering and Biotechnology Research Institute (GEBRI), University of Sadat City, Sadat City, Egypt

    Ragaa A. Hamouda

  4. Faculty of Aquatic and Fisheries Sciences, Kafrelsheikh University, Kafrelsheikh, Egypt

    Ahmed A. Tayel

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  1. Mohamed R. Ibrahim
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Ibrahim, M.R., Hamouda, R.A., Tayel, A.A. et al. Anti-cholesterol and Antioxidant Activities of Independent and Combined Microalgae Aqueous Extracts In Vitro. Waste Biomass Valor 12, 4845–4857 (2021). https://doi.org/10.1007/s12649-021-01349-6

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