The Health-Promoting Properties of Seaweeds: Clinical Evidence based on Wakame and Kombu
DOI:
https://doi.org/10.18311/jnr/2023/30820Keywords:
Brown Algae, Clinical Trials, Saccharina japonica, Undaria pinnatifidaAbstract
In this review, the botany, uses, bioactive metabolites, and health-promoting benefits of Undaria pinnatifida (wakame) and Saccharina japonica (kombu) are highlighted. Their clinical evidence is focused on clinical studies conducted in Japan and in other countries. These two species are brown seaweeds (Phaeophyta). In Japan, wakame and kombu seaweeds are popular food items consumed almost daily. Laboratory evidence shows that carotenoids (fucoxanthin and fucoxanthinol), polysaccharides (fucoidan) and sterols (fucosterol) are bioactive metabolites in wakame and kombu. Wakame displays antioxidant, anti-inflammatory, anticancer, antihypertensive, antidiabetic, antiviral, anticoagulant, antiosteoporotic, hepatoprotective, and antiobesity properties. Kombu possesses anticoagulant, antithrombotic, anticancer, hypolipidemic, hypoglycemic, antiobesity, antithrombotic, antiatherosclerosis, renal protective, vascular protective, antioxidant, antimicrobial, anti-inflammatory, immunomodulatory, gut biota regulatory, hypoglycemic, hypolipidemic, and neuroprotective activities. Clinical evidence on the effects of wakame intake was based on eight studies in Japan and eight studies in other countries. Clinical evidence on the effects of kombu intake was based on five studies in Japan. One case study on kombu dealt with severe alopecia areata. Some areas for future research on wakame and kombu are suggested. Information and data used in this review were from databases such as Google, Google Scholar, PubMed, PubMed Central, Science Direct, J-Stage, PubChem, China Academic Journals, and ClinicalTrials.gov.
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Copyright (c) 2022 Eric Wei Chiang Chan, Siu Kuin Wong, Mio Kezuka, Hung Tuck Chan
This work is licensed under a Creative Commons Attribution 4.0 International License.
Accepted 2023-07-06
Published 2023-08-31
References
Bedoux G, Hardouin K, Burlot AS, Bourgougnon N. Bioactive components from seaweeds: Cosmetic applications and future development. Adv Bot Res. 2014; 71:345-78. https://doi.org/10.1016/B978-0-12- 408062-1.00012-3 DOI: https://doi.org/10.1016/B978-0-12-408062-1.00012-3
Moghadamtousi SZ, Karimian H, Khanabdali R, Razavi M, Firoozinia M, Zandi K, et al. Anticancer and antitumor potential of fucoidan and fucoxanthin, two main metabolites isolated from brown algae. Sci World J. 2014. https://doi.org/10.1155/2014/768323 DOI: https://doi.org/10.1155/2014/768323
Murai U, Yamagishi K, Kishida R, Iso H. Impact of seaweed intake on health. Eur J Clin Nutr. 2021; 75(6):877-89. https://doi.org/10.1038/s41430-020- 00739-8 DOI: https://doi.org/10.1038/s41430-020-00739-8
Murata M, Nakazoe JI. Production and use of marine algae in Japan. Jpn Agric Res Quart. 2001; 35(4):281- 90. https://doi.org/10.6090/jarq.35.281 DOI: https://doi.org/10.6090/jarq.35.281
Brown EM, Allsopp PJ, Magee PJ, Gill CI, Nitecki S, Strain CR, et al. Seaweed and human health. Nutr Rev. 2014; 72(3):205-16. https://doi.org/10.1111/ nure.12091 DOI: https://doi.org/10.1111/nure.12091
Zava TT, Zava DT. Assessment of Japanese iodine intake based on seaweed consumption in Japan: A literature-based analysis. Thyroid Res. 2011; 4:14-21. https://doi.org/10.1186/1756-6614-4-14 DOI: https://doi.org/10.1186/1756-6614-4-14
Cherry P, Yadav S, Strain CR, Allsopp PJ, McSorley EM, Ross RP, et al. Prebiotics from seaweeds: An ocean of opportunity? Mar Drugs. 2019; 17(6):327- 62. https://doi.org/10.3390/md DOI: https://doi.org/10.3390/md17060327
Yamori Y, Miura A, Taira K. Implications from and for food cultures for cardiovascular diseases: Japanese food, particularly Okinawan diets. Asia Pac J Clin Nutr. 2001; 10:144-5. https://doi.org/10.1111/j.1440- 6047.2001.00227.x DOI: https://doi.org/10.1111/j.1440-6047.2001.00227.x
Taylor VF, Li Z, Sayarath V, Palys TJ, Morse KR, Scholz-Bright RA, et al. Distinct arsenic metabolites following seaweed consumption in humans. Sci Rep. 2017; 7(1):1-9. https://doi.org/10.1038/s41598-017- 03883-7 DOI: https://doi.org/10.1038/s41598-017-03883-7
Hata A, Yamanaka K, Endo G, Yamano Y, Haba R, Fujitani N, et al. Arsenic metabolites in humans after ingestion of wakame seaweed. In: E3S Web of Conferences, 2013; 1. https://doi.org/10.1051/ e3sconf/20130126006 DOI: https://doi.org/10.1051/e3sconf/20130126006
Fung A, Hamid N, Lu J. Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem. 2013; 136:1055-62. https://doi.org/10.1016/j. foodchem.2012.09.024 DOI: https://doi.org/10.1016/j.foodchem.2012.09.024
Nadeeshani H, Hassouna A, Lu J. Proteins extracted from seaweed Undaria pinnatifida and their potential uses as foods and nutraceuticals. Crit Rev Food Sci Nutr. 2002; 62(22):6187-203. https://doi.org/10.1080 /10408398.2021.1898334 DOI: https://doi.org/10.1080/10408398.2021.1898334
Yamanaka R, Akiyama K. Cultivation and utilization of Undaria pinnatifida (wakame) as food. J Appl Phycol. 1993; 5(2):249-53. https://doi.org/10.1007/ BF00004026 DOI: https://doi.org/10.1007/BF00004026
Lane CE, Mayes C, Druehl LD, Saunders GW. A multigene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J Phycol. 2006; 42(2):493-512. https://doi.org/10.1111/j.1529-8817.2006.00204.x DOI: https://doi.org/10.1111/j.1529-8817.2006.00204.x
Balakirev ES, Krupnova TN, Ayala FJ. Symbiotic associations in the phenotypically-diverse brown alga Saccharina japonica. PLoS One. 2012; 7(6):e39587. https://doi.org/10.1371/journal.pone.0039587 DOI: https://doi.org/10.1371/journal.pone.0039587
Kawai T, Galanin D, Krupnova T, Yotsukura N. Harvest and cultivation of Saccharina japonica in Northern Hokkaido, Japan, and southern Sakhalin and Primorye, Russia: A review. Algal Resour. 2015; 8(2):155-63.
Li HY, Yi YL, Guo S, Zhang F, Yan H, Zhan ZL, et al. Isolation, structural characterization and bioactivities of polysaccharides from Laminaria japonica: A review. Food Chem. 2022; 370:131010. https://doi. org/10.1016/j.foodchem.2021.131010 DOI: https://doi.org/10.1016/j.foodchem.2021.131010
Zhao Y, Zheng Y, Wang J, Ma S, Yu Y, White WL, et al. Fucoidan extracted from Undaria pinnatifida: Source for nutraceuticals /functional foods. Mar Drugs. 2018; 16(9):321-38. https://doi.org/10.3390/md16090321 DOI: https://doi.org/10.3390/md16090321
Zarekarizi A, Hoffmann L, Burritt D. Approaches for the sustainable production of fucoxanthin, a xanthophyll with potential health benefits. J Appl Phycol. 2019; 31(1):81-99. https://doi.org/10.1007/ s10811-018-1558-3
Zhang H, Tang Y, Zhang Y, Zhang S, Qu J, Wang X, et al. Fucoxanthin: A promising medicinal and nutritional ingredient. Evid-based Complement Altern Med. 2015; 2015:10 pp. https://doi.org/10. 1155/2015/723515 DOI: https://doi.org/10.1155/2015/723515
Bae M, Kim MB, Park YK, Lee JY. Health benefits of fucoxanthin in the prevention of chronic diseases. Biochim Biophys Acta - Mol Cell Biol Lipids. 2020; 1865(11):158618. https://doi.org/10.1016/j.bbalip. 2020.158618 DOI: https://doi.org/10.1016/j.bbalip.2020.158618
Fletcher HR, Biller P, Ross AB, Adams JM. The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res. 2017; 22:79-86. https://doi.org/10.1016/j.algal.2016.10.015 DOI: https://doi.org/10.1016/j.algal.2016.10.015
Koh HS, Lu J, Zhou W. Structure characterization and antioxidant activity of fucoidan isolated from Undaria pinnatifida grown in New Zealand. Carbohydr Polym. 2019; 212:178-85. https://doi.org/10.1016/j. carbpol.2019.02.040 DOI: https://doi.org/10.1016/j.carbpol.2019.02.040
Bang MH, Kim HH, Lee DY, Han MW, Baek YS, Chung DK, et al. Antiosteoporotic activities of fucosterol from sea mustard (Undaria pinnatifida). Food Sci Biotechnol. 2011; 20(2):343-7. https://doi. org/10.1007/s10068-011-0048-z DOI: https://doi.org/10.1007/s10068-011-0048-z
Zhang H, Pang Z, Han C. Undaria pinnatifida (wakame): A seaweed with pharmacological properties. Sci. Int. 2014; 2:32-6. https://doi. org/10.17311/sciintl.2014.32.36 DOI: https://doi.org/10.17311/sciintl.2014.32.36
Wang L, Park YJ, Jeon YJ, Ryu B. Bioactivities of the edible brown seaweed, Undaria pinnatifida: A review. Aquaculture. 2018; 495:873-80. https://doi. org/10.1016/j.aquaculture.2018.06.079 DOI: https://doi.org/10.1016/j.aquaculture.2018.06.079
Luan F, Zou J, Rao Z, Ji Y, Lei Z, Peng L, et al. Polysaccharides from Laminaria japonica: An insight into the current research on structural features and biological properties. Food Funct. 2021; 12(10):4254- 83. https://doi.org/10.1039/D1FO00311A DOI: https://doi.org/10.1039/D1FO00311A
Peng J, Yuan JP, Wu CF, Wang JH. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: metabolism and bioactivities relevant to human health. Mar Drugs. 2011; 9:1806-28. https:// doi.org/10.3390/md9101806 DOI: https://doi.org/10.3390/md9101806
D’Orazio N, Gemello E, Gammone MA, De Girolamo M, Ficoneri C, Riccioni G. Fucoxantin: A treasure from the sea. Mar. Drugs. 2012; 10(3):604-16. https:// doi.org/10.3390/md DOI: https://doi.org/10.3390/md10030604
Saeed M, Arain MA, Fazlani SA, Marghazani IB, Umar M, Soomro J, et al. A comprehensive review on the health benefits and nutritional significance of fucoidan polysaccharide derived from brown seaweeds in human, animals and aquatic organisms. Aquac Nutr. 2021; 27(3):633-54. https://doi. org/10.1111/anu.13233 DOI: https://doi.org/10.1111/anu.13233
Abdul QA, Choi RJ, Jung HA, Choi JS. Health benefit of fucosterol from marine algae: A review. J Sci Food Agric. 2016; 96(6):1856-66. https://doi.org/10.1002/ jsfa.7489 DOI: https://doi.org/10.1002/jsfa.7489
Negishi H, Mori M, Mori H, Yamori Y. Supplementation of elderly Japanese men and women with fucoidan from seaweed increases immune responses to seasonal influenza vaccination. J Nutr. 2013; 143:1794-8. https://doi.org/10.3945/ jn.113.179036 DOI: https://doi.org/10.3945/jn.113.179036
Hata Y, Nakajima K, Uchida Ji, Hidaka H, Nakano T. Clinical effects of brown seaweed, Undaria pinnatifida (wakame), on blood pressure in hypertensive subjects. J Clin Biochem Nutr. 2001; 30:43-53. https://doi. org/10.3164/jcbn.30.43 DOI: https://doi.org/10.3164/jcbn.30.43
Wada K, Nakamura K, Tamai Y, Tsuji M, Sahashi Y, Watanabe K, et al. Seaweed intake and blood pressure levels in healthy pre-school Japanese children. Nutr J. 2011; 10(1):83-90. https://doi.org/10.1186/1475- 2891-10-83 DOI: https://doi.org/10.1186/1475-2891-10-83
Tanemura Y, Yamanaka-Okumura H, Sakuma M, Nii Y, Taketani Y, Takeda E. Effects of the intake of Undaria pinnatifida (wakame) and its sporophylls (mekabu) on post-prandial glucose and insulin metabolism. J Med Investig. 2014; 61:291-7. https:// doi.org/10.2152/jmi.61.291 DOI: https://doi.org/10.2152/jmi.61.291
Yoshinaga K, Mitamura R. Effects of Undaria pinnatifida (wakame) on post-prandial glycaemia and insulin levels in humans: A randomized crossover trial. Plant Foods Hum Nutr. 2019; 74(4):461-7. https://doi.org/10.1007/s11130-019-00763-5 DOI: https://doi.org/10.1007/s11130-019-00763-5
Yoshinaga K, Maruya R, Koikeda T, Nakano T. Effects of Undaria pinnatifida (wakame) on the human intestinal environment. Funct Foods Health Dis. 2018; 8(10):488-504. https://doi.org/10.31989/ffhd. v8i10.543 DOI: https://doi.org/10.31989/ffhd.v8i10.543
Mitamura R, Yoshinaga K. Effects of Undaria pinnatifida (wakame) on post-prandial glycaemia: in vitro and in vivo studies. Res Square. 2022. p. 1-14. https://doi.org/10.21203/rs.3.rs-1675303/v1 DOI: https://doi.org/10.21203/rs.3.rs-1675303/v1
Takano S, Yoshizumi K, Kobayashi H, Iwamoto N, Taga M. Suppression of blood glucose level elevation and promotion of GLP-1 secretion by ingestion of Undaria pinnatifida sporophylls (mekabu): Openlabel crossover design. Funct Foods Health Dis. 2022; 12(2):93-102. https://doi.org/10.31989/ffhd.v12i2.891 DOI: https://doi.org/10.31989/ffhd.v12i2.891
Cooper R, Drager C, Elliot K, Fitton JH, Godwin J, Thompson K. GFS, a preparation of Tasmanian Undaria pinnatifida is associated with healing and inhibition of reactivation of herpes. BMC Complement Altern Med. 2002; 2:11. https://doi. org/10.1186/1472-6882-2-11 DOI: https://doi.org/10.1186/1472-6882-2-11
Teas J, Baldeón ME, Chiriboga DE, Davis JR, Sarriés AJ, Braverman LE. Could dietary seaweed reverse the metabolic syndrome? Asia Pac J Clin Nutr. 2009; 18(2):145-57.
Izaola O, Primo D, Rico BD, Martín-Diana AB, Martínez VC, Miranda J, et al. Effects of a snack enriched with carob and Undaria pinnatifida (wakame) on metabolic parameters in a double blind, randomized clinical trial in obese patients. Nutr Hosp. 2020; 37(3):1-9. https://doi.org/10.20960/nh.02906
Teas J, Irhimeh MR. Dietary algae and HIV/AIDS: Proof of concept clinical data. J Appl Phycol. 2012; 24(3):575-82. https://doi.org/10.1007/s10811-011- 9766-0 DOI: https://doi.org/10.1007/s10811-011-9766-0
Tocaciu S, Oliver LJ, Lowenthal RM, Peterson GM, Patel R, Shastri M, et al. The effect of Undaria pinnatifida fucoidan on the pharmacokinetics of letrozole and tamoxifen in patients with breast cancer. Integr Cancer Therap. 2018; 17(1):99-105. https://doi. org/10.1177/1534735416684014 DOI: https://doi.org/10.1177/1534735416684014
van Den Driessche JJ, Plat J, Mensink RP. Spirulina or wakame consumption does not affect intestinal cholesterol absorption in non-hypercholesterolemic men and women. Atherosclerosis. 2019; 287:e81. https://doi.org/10.1016/j.atherosclerosis.2019.06.234 DOI: https://doi.org/10.1016/j.atherosclerosis.2019.06.234
van Den Driessche JJ, Plat J, Konings MC, Mensink RP. Effects of spirulina and wakame consumption on intestinal cholesterol absorption and serum lipid concentrations in non-hypercholesterolemic adult men and women. Eur J Nutr. 2019; 1-8. https://doi. org/10.1007/s00394-019-02073-7 DOI: https://doi.org/10.1007/s00394-019-02073-7
Yun H, Lee B, Lee SJ, Park CY. Marine healing, but not additional intake of Undaria pinnatifida, benefits physical and emotional exhaustion symptoms of menopause. Clin Nutr Res. 2020; 9(1):1-10. https:// doi.org/10.7762/cnr.2020.9.1.1 DOI: https://doi.org/10.7762/cnr.2020.9.1.1
Zaharudin N, Tullin M, Pekmez CT, Sloth JJ, Rasmussen RR, Dragsted LO. Effects of brown seaweeds on postprandial glucose, insulin and appetite in humans – A randomized, 3-way, blinded, cross-over meal study. Clin Nutr. 2021; 40(3):830-8. https://doi.org/10.1016/j.clnu.2020.08.027 DOI: https://doi.org/10.1016/j.clnu.2020.08.027
Miyai K, Tokushige T, Kondo M, Suppression of thyroid function during ingestion of seaweed kombu (Laminaria japonica) in normal Japanese adults. Endocr J. 2008; 55(6):1103-8. https://doi.org/10.1507/ endocrj.K08E-125 DOI: https://doi.org/10.1507/endocrj.K08E-125
Nishimura M, Sugawara M, Kudo M, Kinoshita Y, Yoshino H, Nishihira J. Effects of daily intake of Harudori-kombu: A randomized, double-blind, placebo-controlled, parallel-group study. Funct Foods Health Dis. 2019; 9(4):205-23. https://doi. org/10.31989/ffhd.v9i4.594 DOI: https://doi.org/10.31989/ffhd.v9i4.594
Nishiumi S, Izumi Y, Kobayashi T, Yoshida M. A pilot study: Effects of kombu intake on lifestyle-related diseases-possibility that kombu intake is effective in individuals with abnormally high serum triglyceride levels. Food Sci Technol Res. 2019; 25(6):827-34. https://doi.org/10.3136/fstr.25.827 DOI: https://doi.org/10.3136/fstr.25.827
Nishiumi S, Izumi Y, Kobayashi T, Yoshida M. Possible involvement of lipids in the effectiveness of kombu in individuals with abnormally high serum triglyceride levels. J Nutr Sci Vitaminol. 2020; 66(2):185-90. https://doi.org/10.3177/jnsv.66.185 DOI: https://doi.org/10.3177/jnsv.66.185
Aoe S, Yamanaka C, Ohtoshi H, Nakamura F, Fujiwara S. Effects of daily kelp (Laminaria japonica) intake on body composition, serum lipid levels, and thyroid hormone levels in healthy japanese adults: A randomized, double-blind study. Mar Drugs. 2021; 19(7):352-64. https://doi.org/10.3390/md DOI: https://doi.org/10.3390/md19070352
Inui S, Tsujimoto N, Toda N, Itami S. Suppression of thyroid function by seaweed kombu (Laminaria japonica) supplement seen in a patient with alopecia areata: A case report. Open Dermatol J. 2010; 4:108-9. https://doi.org/10.2174/1874372201004010108 DOI: https://doi.org/10.2174/1874372201004010108