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Bioactive and nutritional potential of Alaria esculenta and Saccharina latissima

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Abstract

The brown seaweed species Alaria esculenta and Saccharina latissima are commercial edible resources in Norway. There are knowledge gaps regarding these species. Accordingly, they were characterized and their bioactivity and bioaccessibility evaluated. The fatty acid (FA) analysis revealed an ω-3/ω-6 ratio of almost 2 in A. esculenta vs 1 in S. latissima. The FAs 18:4 ω-3 (stearidonic acid) and 20:5 ω-3 (eicosapentaenoic acid) were the main contributors to the relative ω-3 polyunsaturated FA richness in A. esculenta. This seaweed was also rich in fucoxanthin (66.1 ± 20.1 mg (100 g)−1 dw), representing approximately 4.1% of the total lipids. Hence, this species may be a source of natural fucoxanthin. Anti-inflammatory activity was significantly stronger (p < 0.001) in the ethanolic than in the aqueous extracts of the algal biomass, 48.3–60.4% vs 18.2–38.6% cyclooxygenase-2 (COX-2) inhibition. In the bioaccessible fraction of both species, phenolic content and antioxidant activity were low. Moreover, the anti-inflammatory capacity was largely lost in this fraction, especially in the case of S. latissima. Regarding elemental composition, there were no large differences between the two brown seaweed species, being As levels high (53.11–58.93 mg kg−1 dw). However, this As is mostly organic and accordingly poses a lower risk to human health. The I content was high, especially in S. latissima, 2829 ± 58 mg kg−1 dw (557 ± 17 mg kg−1 dw in A. esculenta). Taking into account I levels, only 0.05 g and 0.39 g of S. latissima per day (based on I levels before digestion) are enough to reach I DRI and I TUIL, respectively, or 0.07 g and 0.57 g per day (based on I levels after digestion), for I DRI and I TUIL, respectively. The attained results point to an untapped potential regarding development of functional foods and other products with high-added value—particularly in the case of A. esculenta.

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References

  • Afonso C, Costa S, Cardoso C, Bandarra NM, Batista I, Coelho I, Castanheira I, Nunes ML (2015) Evaluation of the risk/benefit associated to the consumption of raw and cooked farmed meagre based on the bioaccessibility of selenium, eicosapentaenoic acid and docosahexaenoic acid, total mercury, and methylmercury determined by an in vitro digestion model. Food Chem 170:249–256

    Article  CAS  PubMed  Google Scholar 

  • Algaebase (2018). Global algal database of taxonomic, nomenclatural and distributional information. http://www.algaebase.org/ Accessed on 19th September 2018

  • Bandarra NM, Batista I, Nunes ML, Empis JMA, Christie WW (1997) Seasonal changes in lipid composition of sardine Sardina pilchardus. J Food Sci 62:40–43

    Article  CAS  Google Scholar 

  • Bhattacharya PT, Misra SR, Hussain M (2016) Nutritional aspects of essential trace elements in oral health and disease: an extensive review. Scientifica (Cairo) 2016:5464373

    Google Scholar 

  • Biancarosa I, Belghit I, Bruckner CG, Liland NS, Waagbø R, Amlund H, Heesch S, Lock EJ (2018) Chemical characterization of 21 species of marine macroalgae common in Norwegian waters: benefits of and limitations to their potential use in food and feed. J Sci Food Agric 98:2035–2042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bischof K, Gómez I, Molis M, Hanelt D, Karsten U, Lüder U, Roleda MY, Zacher K, Wiencke C (2006) Ultraviolet radiation shapes seaweed communities. Rev Env Sci Bio/Technol 5:141–166

    Article  CAS  Google Scholar 

  • Burtin P (2003) Nutritional value of seaweeds. El J Env Agric Food Chem 2:498–503

    Google Scholar 

  • Campos AM, Matos J, Afonso C, Gomes R, Bandarra NM, Cardoso C (2019) Azorean macroalgae (Petalonia binghamiae, Halopteris scoparia, and Osmundea pinnatifida) bioprospection: a study of fatty acid profiles and bioactivity. Int J Food Sci Technol 54:880–890

    Article  CAS  Google Scholar 

  • Cardoso C, Afonso C, Lourenço H, Costa S, Nunes ML (2015) Bioaccessibility assessment methodologies and their consequences for the risk-benefit evaluation of food. Trends Food Sci Technol 41:5–23

    Article  CAS  Google Scholar 

  • Cherry P, O'Hara C, Magee PJ, McSorley EM, Allsopp PJ (2019) Risks and benefits of consuming edible seaweeds. Nutr Rev 77:307–329

    Article  PubMed  PubMed Central  Google Scholar 

  • Circuncisão AR, Catarino MD, Cardoso SM, Silva A (2018) Minerals from macroalgae origin: health benefits and risks for consumers. Mar Drugs 16:400

    Article  PubMed Central  CAS  Google Scholar 

  • Coelho I, Matos AS, Teixeira R, Nascimento A, Bordado J, Donard O, Castanheira I (2019) Combining multielement analysis and chemometrics to trace the geographical origin of Rocha pear. J Food Compos Anal 77:1–8

    Article  CAS  Google Scholar 

  • Coelho JP (2019) Arsenic speciation in algae: case studies in Europe. In: Duarte AC, Reis V (eds) Comprehensive Analytical Chemistry. Elsevier, Amsterdam, pp 179–198

    Google Scholar 

  • Demirel Z, Yilmaz-Koz FF, Karabay-Yavasoglu UN, Ozdemir G, Sukatar A (2009) Antimicrobial and antioxidant activity of brown algae from the Aegean Sea. J Serb Chem Soc 74:619–628

    Article  CAS  Google Scholar 

  • EFSA (2010) Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J 8:1461

    Google Scholar 

  • EFSA (2014) Scientific opinion on dietary reference values for iodine. EFSA J 12:3660

    Google Scholar 

  • EPA (1998) Test method 7473: Mercury in solids and solutions by thermal decomposition, amalgamation and atomic absorption spectrometry. SW-846, USA

  • EU (2012) Regulation 744/2012 amending annexes I and II to directive 2002/32/EC of the European Parliament and of the council as regards maximum levels for arsenic, fluorine, lead, mercury, endosulfan, dioxins, Ambrosia spp., diclazuril and lasalocid a sodium and action thresholds for dioxins. OJ L 219:5–12

    Google Scholar 

  • FAO/WHO (2005) Vitamin and mineral requirements in human nutrition, 2nd edn. World Health Organization, Geneva

    Google Scholar 

  • FAO/WHO (2011) Safety evaluation of certain contaminants in food, prepared by the seventy-second meeting of the Joint FAO/WHO Expert Committee on food additives. WHO Food Additives Series 63:153–316

    Google Scholar 

  • Farasat M, Khavari-Nejad RA, Nabavi SMB, Namjooyan F (2013) Antioxidant properties of two edible green seaweeds from northern coasts of the Persian Gulf. Jundishapur J Nat Pharm Prod 8:47–52

    Article  PubMed  PubMed Central  Google Scholar 

  • Farvin KHS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681

    Article  CAS  Google Scholar 

  • Francisco J, Cardoso C, Bandarra N, Brito P, Horta A, Pedrosa R, Gil MM, Delgado IM, Castanheira I, Afonso C (2018) Bioaccessibility of target essential elements and contaminants from Fucus spiralis. J Food Compos Anal 74:10–17

    Article  CAS  Google Scholar 

  • Francisco J, Horta A, Pedrosa R, Afonso C, Cardoso C, Bandarra NM, Gil MM (2020) Bioaccessibility of antioxidants and fatty acids from Fucus spiralis L. Foods 9:440

    Article  CAS  PubMed Central  Google Scholar 

  • Gosch BJ, Magnusson M, Paul NA, de Nys R (2012) Total lipid and fatty acid composition of seaweeds for the selection of species for oil-based biofuel and bioproducts. GCB Bioenergy 4:919–930

    Article  CAS  Google Scholar 

  • IOM (2004) Dietary reference intakes (DRIs): recommended intakes for individuals. Vitamins. Institute of Medicine. https://web.archive.org/web/20091030004039/http://iom.edu/en/Global/News%20Announcements/~/media/Files/Activity%20Files/Nutrition/DRIs/DRISummaryListing2.ashx/ Accessed 8 Oct 2018

  • Jaswir I, Noviendri D, Salleh HM, Taher M, Miyashita K (2013) Isolation of fucoxanthin and fatty acids analysis of Padina australis and cytotoxic effect of fucoxanthin on human lung cancer (H1299) cell lines. Af J Biotechnol 10:18855–18862

    Google Scholar 

  • Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio MD, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512

    Article  CAS  Google Scholar 

  • Jin DQ, Lim CS, Sung JY, Choi HG, Ha I, Han JS (2006) Ulva conglobata, a marine algae, has neuroprotective and anti-inflammatory effects in murine hippocampal and microglial cells. Neurosci Lett 402:154–158

    Article  CAS  PubMed  Google Scholar 

  • Kellogg J, Lila MA (2013) Chemical and in vitro assessment of Alaskan coastal vegetation antioxidant capacity. J Agric Food Chem 61:11025–11032

    Article  CAS  PubMed  Google Scholar 

  • Kim SM, Kang SW, Kwon ON, Chung D, Pan CH (2012) Fucoxanthin as a major carotenoid in Isochrysis aff. galbana: characterization of extraction for commercial application. J Korean Soc Appl Biol Chem 55:477–483

    Article  CAS  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332:392–397

    Article  CAS  PubMed  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Miyashita K (2007) Dietary combination of fucoxanthin and fish oil attenuates the weight gain of white adipose tissue and decreases blood glucose in obese/diabetic KK-Ay mice. J Agric Food Chem 55:7701–7706

    Article  CAS  PubMed  Google Scholar 

  • Maehre HK, Malde MK, Eilertsen KE, Elvevoll EO (2014) Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J Sci Food Agric 94:3281–3290

    Article  CAS  PubMed  Google Scholar 

  • Mai K, Mercer JP, Donlon J (1996) Comparative studies on the nutrition of abalone, Haliotis tuberculata L and Haliotis discus hannai Ino V. The role of polyunsaturated fatty acids of macroalgae in abalone nutrition. Aquaculture 139:77–89

    Article  CAS  Google Scholar 

  • Makris DP, Boskou D (2014) Plant-derived antioxidants as food additives. In: Dubey NK (ed) Plants as a source of natural antioxidants. CABI, Oxfordshire, pp 169–190

    Google Scholar 

  • Marinho GS, Holdt SL, Jacobsen C, Angelidaki I (2015) Lipids and composition of fatty acids of Saccharina latissima cultivated year-round in integrated multi-trophic aquaculture. Mar Drugs 13:4357–4374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montalvão S, Demirel Z, Devi P, Lombardi V, Hongisto V, Perälä M, Hattara J, Imamoglu E, Tilvi SS, Turan G, Dalay MC, Tammela P (2018) Large-scale bioprospecting of cyanobacteria, micro- and macroalgae from the Aegean Sea. New Biotechnol 33:399–406

    Article  CAS  Google Scholar 

  • Mrad ND, Boudhrioua N, Kechaou N, Courtois F, Bonazzi C (2012) Influence of air drying temperature on kinetics, physicochemical properties, total phenolic content and ascorbic acid of pears. Food Bioprod Process 90:433–441

    Article  CAS  Google Scholar 

  • Nielsen CW, Holdt SL, Sloth JJ, Marinho GS, Sæther M, Funderud J, Rustad T (2020) Reducing the high iodine content of Saccharina latissima and improving the profile of other valuable compounds by water blanching. Foods 9:569

    Article  CAS  PubMed Central  Google Scholar 

  • Nitschke U, Stengel DB (2015) A new HPLC method for the detection of iodine applied to natural samples of edible seaweeds and commercial seaweed food products. Food Chem 172:326–334

    Article  CAS  PubMed  Google Scholar 

  • NRC (2000) Dietary reference intakes for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. National Academies Press, New York, pp 258–259

    Google Scholar 

  • Nwosu F, Morris J, Lund VA, Stewart D, Ross HA, McDougall GJ (2011) Anti-proliferative and potential anti-diabetic effects of phenolic-rich extracts from edible marine algae. Food Chem 126:1006–1012

    Article  CAS  Google Scholar 

  • Oh J-H, Kim J, Lee Y (2016) Anti-inflammatory and anti-diabetic effects of brown seaweeds in high-fat diet-induced obese mice. Nutr Res Pract 10:42–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ometto F, Steinhovden KB, Kuci H, Lunnbäck J, Berg A, Karlsson A, Handa Å, Wollan H, Ejlertsson J (2018) Seasonal variation of elements composition and biomethane in brown macroalgae. Biomass Bioenergy 109:31–38

    Article  CAS  Google Scholar 

  • Paiva L, Lima E, Patarra RF, Neto AI, Baptista J (2014) Edible Azorean macroalgae as source of rich nutrients with impact on human health. Food Chem 164:128–135

    Article  CAS  PubMed  Google Scholar 

  • Pereira L (2016) Edible seaweeds of the world. CRC Press, Boca Raton

    Book  Google Scholar 

  • Quideau S, Deffieux D, Douat-Casassus C, Pouységu L (2011) Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem 50:586–621

    Article  CAS  Google Scholar 

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

    Article  CAS  PubMed  Google Scholar 

  • Ripol A, Cardoso C, Afonso C, Varela J, Quental-Ferreira H, Pousão-Ferreira P, Bandarra NM (2018) Composition, anti-inflammatory activity, and bioaccessibility of green seaweeds from fish pond aquaculture. Nat Prod Commun 13:603–608

    Google Scholar 

  • Rodrigues D, Freitas AC, Pereira L, Rocha-Santos TAP, Vasconcelos MW, Roriz M, Rodríguez-Alcalá LM, Gomes AMP, Duarte AC (2015) Chemical composition of red, brown and green macroalgae from Buarcos bay in central west coast of Portugal. Food Chem 183:197–207

    Article  CAS  PubMed  Google Scholar 

  • Roleda MY, Skjermo J, Marfaing H, Jónsdóttir R, Rebours C, Gietl A, Stengel DB, Nitschke U (2018) Iodine content in bulk biomass of wild-harvested and cultivated edible seaweeds: inherent variations determine species-specific daily allowable consumption. Food Chem 254:333–339

    Article  CAS  PubMed  Google Scholar 

  • Romarís-Hortas V, García-Sartal C, Barciela-Alonso MC, Domínguez-González R, Moreda-Piñeiro A, Bermejo-Barrera P (2011) Bioavailability study using an in-vitro method of iodine and bromine in edible seaweed. Food Chem 124:1747–1752

    Article  CAS  Google Scholar 

  • Sappati PK, Nayak B, VanWalsum GP, Mulrey OT (2019) Combined effects of seasonal variation and drying methods on the physicochemical properties and antioxidant activity of sugar kelp (Saccharina latissima). J Appl Phycol 31:1311–1332

    Article  CAS  Google Scholar 

  • Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    Article  CAS  Google Scholar 

  • Schmid M, Guihéneuf F, Stengel DB (2014) Fatty acid contents and profiles of 16 macroalgae collected from the Irish coast at two seasons. J Appl Phycol 26:451–463

    Article  CAS  Google Scholar 

  • Shannon E, Abu-Ghannam N (2017) Optimisation of fucoxanthin extraction from Irish seaweeds by response surface methodology. J Appl Phycol 29:1027–1036

    Article  CAS  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Stévant P, Marfaing H, Duinker A, Fleurence J, Rustad T, Sandbakken I, Chapman A (2018) Biomass soaking treatments to reduce potentially undesirable compounds in the edible seaweeds sugar kelp (Saccharina latissima) and winged kelp (Alaria esculenta) and health risk estimation for human consumption. J Appl Phycol 30:2047–2060

    Article  CAS  Google Scholar 

  • Tanaka N, Ishida T, Nagao M, Mori T, Monguchi T, Sasaki M, Mori K, Kondo K, Nakajima H, Honjo T, Irino Y, Toh R, Shinohara M, Hirata K (2014) Administration of high dose eicosapentaenoic acid enhances anti-inflammatory properties of high-density lipoprotein in Japanese patients with dyslipidemia. Atherosclerosis 237:577–583

    Article  CAS  PubMed  Google Scholar 

  • Taylor VF, Li Z, Sayarath V, Palys JT, Morse KR, Rachel A, Scholz-Bright RA, Karagas MR (2017) Distinct arsenic metabolites following seaweed consumption in humans. Sci Rep 7:3920

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vilg JV, Nylund GM, Werner T, Qvirist L, Mayers JJ, Pavia H, Undeland I, Albers E (2015) Seasonal and spatial variation in biochemical composition of Saccharina latissima during a potential harvesting season for Western Sweden. Bot Mar 58:1–12

    Article  CAS  Google Scholar 

  • Yea SS, Choi CY, Jo G-H, Seo Y (2009) Antioxidant and anti-inflammatory potential of Arctic seaweeds: activity screening and mechanism identification. Drug Metab Rev, in 3rd Asian Pacific Regional International Society for the study of xenobiotics Meeting

  • Zemke-White WL, Ohno M (1999) World seaweed utilisation: an end-of-century summary. J Appl Phycol 11:369–376

    Article  Google Scholar 

  • Zubia M, Fabre MS, Kerjean V, Le Lann K, Stiger-Pouvreau V, Fauchon M, Deslandes E (2009) Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts. Food Chem 116:693–701

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the following Grants: Ref.: SFRH/BPD/102689/2014 (“Fundação para a Ciência e a Tecnologia”, FCT) for Carlos Cardoso and Ref.: SFRH/BD/129795/2017 (FCT) for Joana Matos.

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The study was funded by the project AQUAMAX (Ref.: 16-02-01-FMP-0047).

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Afonso, C., Matos, J., Guarda, I. et al. Bioactive and nutritional potential of Alaria esculenta and Saccharina latissima. J Appl Phycol 33, 501–513 (2021). https://doi.org/10.1007/s10811-020-02298-8

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