Variations in polyphenol and heavy metal contents of wild-harvested and cultivated seaweed bulk biomass: Health risk assessment and implication for food applications

Food Control - Tập 95 - Trang 121-134 - 2019
Michael Y. Roleda1,2, Hélène Marfaing3, Natasa Desnica4, Rósa Jónsdóttir4, Jorunn Skjermo5, Céline Rebours1,6, Udo Nitschke7
1Norwegian Institute of Bioeconomy Research (NIBIO), 8027, Bodø, Norway
2The Marine Science Institute, College of Science, University of the Philippines Diliman, Quezon City, Philippines
3Centre d'Etude et Valorisation des Algues (CEVA), 22610, Pleubian, France
4Matis ohf, Vinlandsleid 12, 113 Reykjavik, Iceland
5SINTEF Ocean, 7465 Trondheim, Norway
6Møreforsking Ålesund AS, 6021, Ålesund, Norway
7Department of Biology, Skidmore College, Saratoga Springs, NY, 12866, United States

Tài liệu tham khảo

Abdala-Diaz, 2006, Daily and seasonal variations of optimum quantum yield and phenoloc compounds in Cystoseira tamariscifolia (Phaeophyta), Marine Biology, 148, 459, 10.1007/s00227-005-0102-6 Afssa Aguilera, 2002, Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress, Marine Biology, 140, 1087, 10.1007/s00227-002-0792-y Almela, 2002, Heavy metal, total arsenic, and inorganic arsenice contents of algae food products, Journal of Agricultural and Food Chemistry, 50, 918, 10.1021/jf0110250 Almela, 2006, Total arsenic, inorganic arsenic, lead and cadmium contents in edible seaweed sold in Spain, Food and Chemical Toxicology, 44, 1901, 10.1016/j.fct.2006.06.011 Andrade, 2010, Brown algae overproduce cell wall polysaccharides as a protection mechanism against the heavy metal toxicity, Marine Pollution Bulletin, 60, 1482, 10.1016/j.marpolbul.2010.05.004 Balboa, 2013, In vitro antioxidant properties of crude extracts and compounds from brown algae, Food Chemistry, 138, 1764, 10.1016/j.foodchem.2012.11.026 Besada, 2009, Heavy metals in edible seaweeds commercialised for human consumption, Journal of Marine Systems, 75, 305, 10.1016/j.jmarsys.2008.10.010 Bradl, 2005, Chapter 1. Sources and origins of heavy metals, vol. 6, 1 Carro, 2011, Adsorptive behaviour of mercury on algal biomass: Competition with divalent cations and organic compounds, Journal of Hazardous Materials, 192, 284 Chapman, 2015, Food or fad? Challenges and opportunities for including seaweeds in a Nordic diet, Botanica Marina, 58, 423, 10.1515/bot-2015-0044 Chaudhuri, 2007, Heavy metal biomonitoring by seaweeds on the Delmarva Peninsula, east coast of USA, Botanica Marina, 50, 151, 10.1515/BOT.2007.018 Cheney, 2016, Toxic and harmful seaweeds, 407 Chen, 2018, Distribution of metals and metalloids in dried seaweeds and health risk to population in southeastern China, Scientific Reports, 8, 3578, 10.1038/s41598-018-21732-z Connan, 2007, Influence of day-night and tidal cycles on phenol content and antioxidant capacity in three temperate intertidal brown seaweeds, Journal of Experimental Marine Biology and Ecology, 349, 359, 10.1016/j.jembe.2007.05.028 Connan, 2004, Interspecific and temporal variation in phlorotannin levels in an assemblage of brown algae, Botanica Marina, 47, 410, 10.1515/BOT.2004.057 Cruces, 2012, Pholorotannin and antioxidant responses upon short-term exposure to UV-radiation and elevated temperature in three South Pacific kelps, Photochemistry and Photobiology, 88, 58, 10.1111/j.1751-1097.2011.01013.x CSHPF, 1990 Delaney, 2016, Society and seaweed: Understanding the past and present, 7 Déléris, 2016, Seaweeds in human health, 319 Dewailly, 2008, Exposure and effects of seafood-borne contaminants in maritime populations, 181 Díaz, 2012, Total and inorganic arsenic concentrations in different species of economically important algae harvested from coastal zones of Chile, Food and Chemical Toxicology, 50, 744, 10.1016/j.fct.2011.11.024 Di, 2017, Antioxidant and immunostimulating activities in vitro of sulfated polysaccharides isolated from Gracilaria rubra, Journal of Functional Foods, 28, 64, 10.1016/j.jff.2016.11.005 EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain), 2009, Scientific opinion on arsenic in food, EFSA Journal, 7, 199 EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain), 2010, Scientific opinion on lead in food, EFSA Journal, 8, 151 EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain), 2011, Scientific Opinion on tolerable weekly intake for cadmium, EFSA Journal, 9, 19 EFSA CONTAM Panel (EFSA Panel on Contaminants in the Food Chain), 2012, Scientific Opinion on the risk for public health related to the presence of mercury and methylmercury in food, EFSA Journal, 10, 241 EFSA (European Food Safety Authority), 2014, Dietary exposure to inorganic arsenic in the European population, EFSA Journal, 12, 68 EFSA Scientific Committee, 2015, Statement on the benefits of fish/seafood consumption compared to the risks of methylmercury in fish/seafood, EFSA Journal, 13, 36, 10.2903/j.efsa.2015.3982 Fleurence, 2016, Seaweed as food, 149 Ganesan, 2008, Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds, Bioresource Technology, 99, 2717, 10.1016/j.biortech.2007.07.005 Gekeler, 1988, Algae sequester heavy metals via synthesis of phytochelatin complexes, Archives of Microbiology, 150, 197, 10.1007/BF00425162 Guiry, 1991 Güven, 1995, Selectivity of heavy metal binding by algal polysaccharides, Toxicological and Environmental Chemistry, 47, 65, 10.1080/02772249509358127 Haddock, 1991, Foodborne intoxication associated with seaweed, Lancet, 338, 195, 10.1016/0140-6736(91)90194-T Hanaoka, 2001, Arsenic in the prepared edible brown alga hijiki, Hizikia fusiforme. Applied Organometallic Chemistry, 15, 561, 10.1002/aoc.195 Heffernan, 2015, Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins, Marine Drugs, 13, 509, 10.3390/md13010509 Henriques, 2017, Bioaccumulation of Hg, Cd and Pb by Fucus vesiculosus in single and multi-metal contamination scenarios and its effect on growth rate, Chemosphere, 171, 208, 10.1016/j.chemosphere.2016.12.086 Henriques, 2017, A macroalgae-based biotechnology for water remediation: Simultaneous removal of Cd, Pb and Hg by living Ulva lactuca, Journal of Environmental Management, 191, 275, 10.1016/j.jenvman.2017.01.035 Holdt, 2011, Bioactive compounds in seaweed: Functional food applications and legislation, Journal of Applied Phycology, 23, 543, 10.1007/s10811-010-9632-5 Hsu, 2007, HPLC determination for prostaglandins from seaweed, Gracilaria gigas. Food Control, 18, 639, 10.1016/j.foodcont.2006.02.013 Hwang, 2010, Total arsenic, mercury, lead, and cadmium contents in edible dried seaweed in Korea, Food Additives and Contaminants: Part B, 3, 7, 10.1080/19440040903532079 Ichikawa, 2010, Ingestion and excretion of arsenic compounds present in edible brown algae, Hijikia fusiforme, by mice, Food and Chemical Toxicology, 48, 465, 10.1016/j.fct.2009.09.037 Kang, 2016, Popular edible seaweed, Gelidium amansii prevents against diet-induced obesity, Food and Chemical Toxicology, 90, 181, 10.1016/j.fct.2016.02.014 Khan, 2015, Determination of toxic heavy metals and speciation of arsenic in seaweeds from South Korea, Food Chemistry, 169, 464, 10.1016/j.foodchem.2014.08.020 Kuyucak, 1989, Accumulation of cobalt by marine alga, Biotechnology and Bioengineering, 33, 809, 10.1002/bit.260330703 Liu, 2015, Prebiotic effects of diet supplemented with the cultivated red seaweed Chondrus crispus or with fructo-oligo-saccharide on host immunity, colonic microbiota and gut microbial metabolites, BMC Complementary and Alternative Medicine, 15, 279, 10.1186/s12906-015-0802-5 Lomax, 2011, Methylated arsenic species in plants originate from soil microorganisms, New Phytologist, 193, 665, 10.1111/j.1469-8137.2011.03956.x Marfaing, 2017, Nutritional value of seaweed, present and future in western food diet, Cahiers de Nutrition et de Diététique, 52, 257, 10.1016/j.cnd.2017.05.003 Martinez, 2002, Seasonal variation of P content and major N pools in Palmaria palmata (Rhodophyta), Journal of Phycology, 38, 1082, 10.1046/j.1529-8817.2002.01217.x McHugh, 2003 Miranda, 2018, Impact of previous active dipping in Fucus spiralis extract on the quality enhancement of chilled lean fish, Food Control, 90, 407, 10.1016/j.foodcont.2018.03.020 Miranda, 2016, Effect of an icing medium containing the alga Fucus spiralis on the microbial activity and lipid oxidation in chilled megrim (Lepidorhombus whiffiagonis), Food Control, 59, 290, 10.1016/j.foodcont.2015.05.034 Mittler, 2002, Oxidative stress, antioxidants and stress tolerance, Trends in Plant Science, 7, 405, 10.1016/S1360-1385(02)02312-9 Mouritsen, 2013, On the human consumption of the red seaweed dulse (Palmaria palmata (L.) Weber & Mohr), Journal of Applied Phycology, 25, 1777, 10.1007/s10811-013-0014-7 Navarro, 2015, Isolation of polycavernoside D from a marine cyanobacterium, Environmental Science & Technology Letters, 2, 166, 10.1021/acs.estlett.5b00116 NMKL 186, 2007, Trace elements - As, Cd, Hg, Pb and other elements, Determination by ICP-MS after pressure digestion Nriagu, 1989, A global assessment of natural sources of atmospheric trace metals, Nature, 338, 47, 10.1038/338047a0 OJEU L364/5, 2006, Official journal of the European union L 364, 20 december 2006, pp. 5–24 OJEU L138/75, 2014, Official journal of the European union L 138, 13 may 2014, pp. 75–79 OJEU L161/9, 2015, Official journal of the European union L 161, 26 june 2015, pp. 9–13 OJEU L213/9, 2015, Official journal of the European union L 213, 12 August 2015, pp. 9–10 OJEU L78/16 Ragan, 1986, Phlorotannins, brown algal polyphenols, vol. 4, 130 Ragan, 1978, Quantitative studies on brown algal phenols. 2. Seasonal variations in polyphenol content of Ascophyllum nodosum (L) Le Jol and Fucus vesiculosus (L), Journal of Experimental Marine Biology and Ecology, 34, 245, 10.1016/S0022-0981(78)80006-9 Raiza, 2004, Mechanisms of biosorption of different heavy metals by brown marine macroalgae, Biotechnology and Bioengineering, 87, 451, 10.1002/bit.20136 Reddy, 1990, Heavy metal-binding protein/peptides: Occurrence, structure, synthesis and functions. A review, Environmental and Experimental Botany, 30, 251, 10.1016/0098-8472(90)90037-5 Rioux, 2017, Seaweeds: A traditional ingredients for new gastronomic sensation, Food Hydrocolloids, 68, 255, 10.1016/j.foodhyd.2017.02.005 Rodde, 2004, Seasonal and geographical variation in the chemical composition of the red alga Palmaria palmata (L.) Kuntze, Botanica Marina, 47, 125, 10.1515/BOT.2004.012 Roleda, 2018, Iodine content in bulk biomass of wild-harvested and cultivated edible seaweeds: Inherent variations determine species-specific daily allowable consumption, Food Chemistry, 254, 333, 10.1016/j.foodchem.2018.02.024 Ronan, 2017, High proportions of inorganic arsenic in Laminaria digitata but not in Ascophyllum nodosum samples from Ireland, Chemosphere, 186, 17, 10.1016/j.chemosphere.2017.07.076 Roohinejad, 2017, Application of seaweeds to develop new food products with enhanced shelf-life, quality and health-related beneficial properties, Food Research International, 99, 1066, 10.1016/j.foodres.2016.08.016 Rose, 2007, Arsenic in seaweed–forms, concentration and dietary exposure, Food and Chemical Toxicology, 45, 1263, 10.1016/j.fct.2007.01.007 Rubio, 2017, Metals in edible seaweed, Chemosphere, 173, 572, 10.1016/j.chemosphere.2017.01.064 Schiener, 2015, The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta, Journal of Applied Phycology, 27, 363, 10.1007/s10811-014-0327-1 Schmid, 2017, Ecological and commercial implications of temporal and spatial variability in the composition of pigments and fatty acids in five Irish macroalgae, Marine Biology, 164, 158, 10.1007/s00227-017-3188-8 Schoenwaelder, 2002, Physode distribution and the effect of “Thallus sunburn” in Hormosira banksii (Fucales, Phaeophyceae), Botanica Marina, 45, 262, 10.1515/BOT.2002.025 Singh, 2011, Heavy metals and living systems: An overview, Indian Journal of Pharmacology, 43, 246, 10.4103/0253-7613.81505 Skjermo Souza, 2011, Antioxidant potential of two red seaweeds from the Brazilian coasts, Journal of Agricultural and Food Chemistry, 59, 5589, 10.1021/jf200999n Stévant, 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, Journal of Applied Phycology, 30, 2047, 10.1007/s10811-017-1343-8 Taylor, 2017, Distinct arsenic metabolites following seaweed consumption in humans, Scientific Reports, 7, 3920, 10.1038/s41598-017-03883-7 Tchounwou, 2012, Heavy metal toxicity and the environment, Vol. 101, 131 US EPA (US Environmental Protection Agency), 2007 Valentão, 2010, Codium tomentosum and Plocamium cartilagineum: Chemistry and antioxidant potential, Food Chemistry, 119, 1359, 10.1016/j.foodchem.2009.09.015 Vonthron-Sénécheau, 2016, Medicinal properties: Antibiotic, tonic, and antiparasitic properties, 369 Wada, 2015, Mycosporine-like amino acids and their derivatives as natural antioxidants, Antioxidants, 4, 603, 10.3390/antiox4030603 Wang, 2013, Heavy metal pollution in coastal areas of South China: A review, Marine Pollution Bulletin, 76, 7, 10.1016/j.marpolbul.2013.08.025 Worlddata.info Yokoi, 2012, Toxicity of the so-called edible hijiki seaweed (Sargassum fusiforme) containing inorganic arsenic, Regulatory Toxicology and Pharmacology, 63, 291, 10.1016/j.yrtph.2012.04.006 Yotsu-Yamashita, 2004, Identification of polycavernoside A as the causative agent of the fatal food poisoning resulting from ingestion of the red alga Gracilaria edulis in the Philippines, Chemical Research in Toxicology, 17, 1265, 10.1021/tx0498556 Zava, 2011, Assessment of Japanese iodine intake based on seaweed consumption in Japan: A literature-based analysis, Thyroid Research, 4, 14, 10.1186/1756-6614-4-14