ESSENTIAL AND TOXIC ELEMENTS IN EDIBLE SEAWEEDS
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1 ESSENTIAL AND TOXIC ELEMENTS IN EDIBLE SEAWEEDS V.A. Maihara, C.B. L. Alves, P.S.C. Silva Laboratório de Análise por Ativação Neutrônica- LAN- Instituto de Pesquisas Energéticas e Nucleares (IPEN- CNEN/SP), Av. Professor Lineu Prestes 2242, São Paulo, Brazil, (11) vmaihara@ipen.br ABSTRACT Overtime, seaweeds have been used as a food mainly due to their high nutritional value. This type of food is considered as functional food and contributes to the nutritional human requirements, being beneficial to human health. In this study, 13 edible seaweed samples acquired in the marked of São Paulo city were analyzed and the concentrations of elements As, Br, Ca, K, Fe, Mg, Mn and Na were determined by Instrumental Neutron Activation Analysis (INAA) and Cd by Graphite Furnace Atomic Absorption Spectrometry (GF AAS). The following edible seaweeds were analyzed: Nori (Porphyra umbilicates); Hijiki (Hijikia fusiforme); Kombu (Laminaria sp.) and Wakame (Undaria pinnatifida) species from, USA, Japan and South. Hijiki specie showed to be source of Ca and Fe while Kombu specie for K. Cluster and factor analysis were applied and it can be seen that the seaweed species were joined in different groups indicating that the elemental composition is more affected by the species than the origin. KEYWORDS: seaweeds; toxic elements; essential elements; neutron activation analysis. 1-INTRODUCTION Japanese culture has been spreading thought the world and Brazil is no different. As a result there was a considerable increase of Japanese restaurants throughout the country. In Asiatic diets seaweed is present in many of the dishes consumed. Seaweeds (marine algae) are autotrophic and photosynthetic organisms that differ from plants and may be unicellular or multicellular (Vidotti & Rollemberg, 2004). It is also the base of the food chain for many systems, serving as food for zooplankton, which are heterotrophic microorganisms present in plankton, and are staple food for larger organisms. Thus, these algae have a fundamental role in maintaining life on the planet. Many species of seaweeds have been used as food for many years. They are widely consumed in Asia, Europe and America, and their chemical compositions depend on the species, habitat, maturity and environmental conditions in which they are submitted (Kuda et al., 2005). They are excellent sources of minerals because of the ability to absorb these inorganic substances from the environment and store them in their systems, and can be used as biological indicators in many studies (Dawczynski et al.., 2007, Rocha et al., 2009). In recent years, the consumption of seaweeds has increased due to the functional characteristic ingredient for the formulation of healthy food, helping in vegan diets to improve nutrition. The production of meat containing seaweed opens new perspectives for the use of these algae, even including the possibility of overcoming technological problems associated with products with low salt (Dawczynski et al., 2007).
2 Studies have been carried out to verify the effectiveness of seaweeds in alternative treatments of various diseases such as cardiovascular diseases due to its anti-oxidant properties (Shalaby, 2011, Ku et al., 2013). It is known that seaweeds contain vitamins, minerals and in particular have high concentrations of long chain polyunsaturated omega-3, which reduces the risk of atherosclerosis, and inflammatory heart diseases (Cofrades et al., 2010). On the other hand, seaweeds also are important in studies from the toxicological point of view, since it contains elements with high toxicity, such as As, Cd, Hg and Pb (Dawczynski et al., 2007; Khan et al., 2015). In this study four edible seaweed species commercialized in São Paulo were analyzed: Hijiki (Hijikia fusiforme), Kombu (Laminaria sp), Nori (Porphyra umbilicates) and Wakame (Undaria pinnatifida) seaweeds and the essential (Ca, Cl, K, Fe, Mg, Mn and Na) and toxic (As and Cd) elements were determined using the Instrumental Neutron Activation Analysis (INAA) and Graphite Furnace Absorption Atomic Spectrometry (GF AAS). These techniques are important in food research, providing reliable results for a number of elements which have great nutritional importance (Avegliano et al., 2011). 2- MATERIALS AND METHODS 2.1 Sampling and preparation of edible seaweeds Thirteen samples from four species of edible seaweeds commercially available to consumers were purchased from super markets all around São Paulo city. The samples were ground and homogenized using a household mixer, fitted with titanium blade, until they acquire a powder consistency. Table 1 shows the different species of seaweed and its origins. Table 1 Identification of seaweed and their respective origin Edible seaweed specie Origin Japan U.S.A. Hijikia fusiforme (Hijiki) Japan Hijikia fusiforme (Hijiki) Hijikia fusiforme (Hijiki) Undaria pinnatifida (Wakame) Undaria pinnatifida (Wakame) Undaria pinnatifida (Wakame) Laminaria sp (Kombu) Laminaria sp (Kombu) Japan Laminaria sp (Kombu) 2.2. Instrumental Neutron Activation Analysis (INAA) For the K, Na, Mg and Mn determination by INAA, about g of the seaweed samples were irradiated for 20 seconds in a thermal neutron flux of 1.0x10 12 n cm -2 s -1 in a pneumatic station of the nuclear research reactor IEA-R1 at IPEN-CNEN/SP. Primary K, Na,
3 Mg and Mn standards and biological certified reference materials were simultaneously irradiated with the samples for standardization and quality control purposes. About 200 mg of the sample and standard of the elements were irradiated for 8 hours in a thermal flux of 3.5 x10 12 n cm -2 s -1 for determination of the elements As, Br, Ca and Fe. Gamma ray measurements were performed using a GC2018 Canberra HPGe detector coupled to a Canberra DSA-1000 multichannel analyzer. Gamma ray spectra were collected and processed using a Canberra Genie 2000 version 3.1 spectroscopy software. Element content calculations were carried out using a Microsoft Excel spreadsheet Graphite Furnace Absorption Atomic Spectrometry (GFAAS) Cadmium concentrations were determined by GFAAS. Approximately 300 mg of the seaweed samples were digested in 4 ml of concentrated HNO 3 and 1 ml of 30% H 2 O 2 in closed PFA (perfluoralcoxi) vessels in a digestion block for 3 hours at 90 0 C. The digest was diluted with Milli-Q water up to a volume of 25 ml. A Perkin Elmer AAnalyst 800 atomic absorption spectrometer with Zeeman background correction at wavelengths of nm for cadmium and a EDL Cadmium lamp were used in the experiments. The calibration curve coefficients were obtained by a linear regression fit with least squares method performed by the spectrometer software. 20 µl aliquots of the sample solution and 10 µl of matrix modifier (NH 4 H 2 PO 4 0.5% (m/v) and Mg(NO 3 ) % (m/v)) were introduced to the furnace tube by the autosampler. After the atomization step, the Cd concentration was calculated by the spectrometer software after two replicate measurements. Blank background levels were below the detection limit. The analyses were carried out in duplicate with differences between the measurements of up to 10%. 3. RESULTS AND DISCUSSION 3.1 Quality control The validation of the analytical method applied was performed by analysis of biological reference materials Bovine Liver SRM 1577b, from the National Institute of Standards and Technology (NIST-USA) and Mixed Polish Herb (MPH-2) from the Institute of Nuclear Chemistry and Technology- (INCT- Poland). The results showed good agreement with the certified values, as can be verified in Table 2. Table 2- Concentrations of elements in the Certified Reference Materials Bovine Liver SRM 1577b INCT-MPH-2 (Mixed Polish Herb) x ± sd a Certified Value x ± sd a Certified Value As µg/kg nd nd 159 ± ± 23 Br mg/kg 11.0 ± 1.5 (9.7) 8.04 ± ± 0.61 Ca % nd ± ± ± 0.07 Cd mg/kg ± ± ± ± Fe mg/kg 170 ± ± ± 26 (460) K % 0.91 ± ± ± ± 0.12 Mg % ± ± ± ± Mn mg/kg 11.1 ± ± ± ± 12 Na % ± ± ± (0.0350) a :Average and Standard deviation of 3 individual determination; nd: not determined
4 3.2- Results of edible seaweeds Thirteen samples belonging to four species of edible seaweeds were analyzed by INAA and GF AAS. Table 3 shows mean results for the essential and toxic elements in seaweeds obtained of duplicate determinations. All results presented are related to the dry weight (dw) of the samples. In marine foodstuffs, such as seaweed, fish, shellfish, As concentrations range from 0.5 to 50 mg/kg. In this study, the As concentrations in seaweeds varied over a wide range (12.9 to 133 mg/kg dw). Hijikia fusiforme (Hijiki) species presented the highest values of As ( mg/kg). These values are in accordance with the literature. Almela et al. (2006) and Besada et al. (2009) reported similar values ( mg/kg) and (23.3 to 147 mg/kg) for the same species studied, respectively. The adverse health effects of arsenic have long been recognized. The acute toxicity of arsenic ranges from very toxic to completely non-toxic, inorganic arsenic being more toxic than organic arsenic compounds. Methylated forms of arsenic allow acute toxicity; arsenobetaine which is the principal arsenic form in marine foodstuffs is considered nontoxic. It is known that Hijiki contains higher concentrations of As (V) than the other species of algae, with the balance of the arsenic (As) load in Hijiki and the other species being arsenosugars (Narukawa et al., 2012). Therefore, to verify if the ingestion of this foodstuff does not represent human health risk it is necessary to determine which As species are presented in the seaweeds. Brazilian legislation (Brasil, 2006) establishes maximum tolerance level (MTL) of 1.0 mg/kg of As total in fish and other seafood. However there is no MTL for seaweeds. Cd concentrations varied from mg/kg dw in Porphyra umbilicates (Nori-Japan) to 2.31 mg/kg dw in Porphyra umbilicates (Nori-USA). Besada et al. (2009) observed that Cd concentrations in seaweeds are also highly variable. They found the highest Cd concentrations in wakame seaweeds (4.8 mg/kg dw). According to Kolb et al. (2004) a Western diet of 4 g of seaweed has been recommended. So, an ingestion of 4 g/day of Nori-USA seaweed (2.31 mg Cd/kg) the Cd daily intake is µg/kg bw for a 70kg person, which is lower than the PTWI (provisional tolerable weekly intake) of 7 µg Cd/kg bw (FAO/WHO, 2006). Of the essential elements determined the Undaria pinnatifida (Wakame) samples presented the Na highest values ( % dw), while the Laminaria sp (Kombu) showed to be a good source of K ( % dw). Hijikia fusiforme (Hijiki) samples presented the highest concentrations for Ca ( % dw) and for Fe ( mg/kg dw). The element concentrations in seaweeds are strongly dependent on the types of species, habitat, maturity and environmental conditions (Cofrades et al., 2010). In Figures 1a and 1b are showed the statistical results of cluster analysis and factor analysis. It can be seen that the algae species were joined in different groups (Fig 1a) indicating that the elemental composition is more affected by the species than the origin. The main elements responsible by the observed variation in factor are the pars Mn/Cd and Br/K negatively correlated. These elements are responsible for 37% of the explained variation. The elements As, Fe and Ca are the main elements responsible for the variation observed in factor 2 contributing with 25% of the explained variance.
5 Tree Diagram for 13 Cases Ward`s method Squared Euclidean distances 1a 1,0 0,8 Factor Loadings, Factor 1 vs. Factor 2 Rotation: Varimax normalized Extraction: Principal components As Ca Fe 1b (Dlink/Dmax)* Kombu Japan Kombu Kombu Wakame 1 Wakame Wakame Hijiki Hijiki Hijiki Japan Nori Japan Nori USA Nori Nori Factor 2 0,6 0,4 Mg 0,2 K 0,0 Br Mn Cd Na -0,2-0,4-1,0-0,8-0,6-0,4-0,2 0,0 0,2 0,4 0,6 0,8 1,0 Factor 1 4-CONCLUSION Concentrations of Ca, Br, K, Fe, Mg, Mn and Na and toxic elements As and Cd were determined in four edible seaweed species from different regions. The results indicated that the elemental composition is more affected by the species than the origin. High level of As and Cd obtained in this study and due to increasing of seaweed consumption by Brazilian population it is important to established the limit values for these toxic elements in this kind of food. 5-REFERENCE Avegliano, R.P, Maihara, V.A.,Silva,F.F. A. (2011) Brazilian Total Diet Study: Evaluation of essential elements. Journal of Food Composition and Analysis, 24, Almela, C., Clemente, M. J., Velez D., Montoro, R. (2006) Total arsenic, inorganic arsenic, lead and cadmium contents inedible seaweed sold in Spain. Food and Chemical Toxicology, 44, Brasil Agência Nacional de Vigilância Sanitária ANVISA (1998).Portaria n.685, de 27 de agosto de Aprova o Regulamento Técnico: Princípios Gerais para o Estabelecimento de Níveis Máximos de Contaminantes Químicos em Alimentos e seu Anexo: Limites máximos de tolerância para contaminantes inorgânicos. Disponível Besada, V., Andrade, J.M., Schultze, F. González, J.J.(2009). Heavy metals in edible seaweeds commercialised for human consumption. Journal of Marine Systems,75, Cofrades, S.I. López-López, L. Bravo, C. Ruiz-Capillas, S. Bastida, M.T. Larrea, F. Juménez-Colmenero (2010). Nutritional and Antioxidant Properties of Different Brown and Red Spanish Edible Seaweeds Food Science Technology International, 16, Dawczynski, C., Schäfer, U., Leiterer, M. and Jahreis, G. (2007) Nutritional and Toxicological Importance of Macro, Trace, and Ultra-Trace Elements in Algae Food Products. Journal of Agricultural and Food Chemistry, 55, Dawczynski, C., Schäfer, U., Leiterer, M. and Jahreis, G. (2007) Nutritional and Toxicological Importance of Macro, Trace, and Ultra-Trace Elements in Algae Food Products. Journal of Agricultural and Food Chemistry, 55,
6 FAO/WHO Codex Alimentarius Commission. Joint FAO/WHO Codex Committee on Food Additives and Contaminants (2006) CX/FAC 06/38/18. Khan N. Ryu K.Y., Choi J. Y, Nho E.Y., Habte G., Choi H., Kim M.H., Park K.S., Kim K.S.(2015). Determination of toxic heavy metals and speciation of arsenic in seaweeds from South. Food Chemistry 169, Kolb N., Vallorani L., Milanovi N., Stocchi V.(2004). Evaluation of Marine Algae Wakame (Undaria pinnatifida) and Kombu (Laminaria digitata japonica) as Food Supplements Food Technologyand Biotechnology. 42 (1), Ku, C.K., Yang, Y., Park, Y., Lee, J. (2013). Health Benefits of Blue-Green Algae: Prevention of Cardiovascular Disease and Nonalcoholic Fatty Liver Disease. Journal of Medicinal Food, 16, Kuda. T., Tsunekawa. M., Goto. H., Araki. Y. (2005). Antioxidant Properties of Four Edible Algae Harvested in the Noto Peninsula. Journal of Food Composition and Analysis, 18, Narukawa T., Inagaki K., Zhu Y., Kuroiwa T., Narushima I., Chiba K.oichi, Hioki A.(2012). Preparation and certification of Hijiki reference material,nmij CRM 7405-a, from the edible marine algae hijiki(hizikia fusiforme) Anal Bioanal Chem, 402, Rocha, S. R.,Sanchez-Muniz, F.J.Gómez-Juaristi, Marín, M.T. L (2009).Trace elements determination in edible seaweeds by an optimized and validated ICP-MS method. Journal of Food Composition and Analysis, 22, Rupérez, P. (2002). Mineral content of edible marine seaweeds. Food Chemistry, 79, Shalaby, E.(2011) Algae as promising organisms for environment and health Plant Signaling & Behavior, 6, Vidotti, E. C., Rollemberg, M. C. E. (2004) Algas: da Economia nos Ambientes Aquáticos à Bioremediação e à Química Analítica. Quimica. Nova, 27, ACKNOWLEDGEMENTS The author VA.Maihara would like to thank the CNPq (30296/2015-5) for the fellowship and IPEN/CNEN-SP for financial support.
7 Table 2 Element concentration in different samples of edible seaweeds (dry weight.) mg/kg % Species Origin As Cd Br Fe Mn Ca K Mg Na 19.7 ± ± ± ± ± ± ± ± ± Porphyra umbilicates (Nori) Hijikia fusiforme (Hijiki) Undaria pinnatifida (Wakame) Laminaria sp (Kombu) 17.3 ± ± ± ± ± ± ± ± ± Japan 12.9 ± ± ± ± ± ± ± ± ±0.033 U.S.A ± ± ± ± ± ± ± ± ± Japan 68.5± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.18 Japan 51.0 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 0.19
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