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Elemental and radioactive analysis of commercially available seaweed
The Science of the Total Environment 255 Ž2000. 169]175
Elemental and radioactive analysis of commercially available seaweed C. van Netten a,U , S.A. Hoption Cannb,c , D.R. Morley d, J.P. van Netten b,c a
Department of Health Care and Epidemiology, James Mather Building, Uni¨ ersity of British Columbia, 5804 Fair¨ iew A¨ enue, Vancou¨ er, BC V6T 1Z3, Canada b Special De¨ elopment Laboratory, Royal Jubilee Hospital, Victoria, BC V8X 1P2, Canada c Department of Biology, Uni¨ ersity of Victoria, Victoria, BC V8W 3N5, Canada d Radiation Protection Branch, Ministry of Health, 4940 Canada Way, Burnaby, BC V5G 4K6, Canada Received 12 October 1999; accepted 25 February 2000
Abstract Edible seaweed products have been used in many countries, specifically Japan, as a food item. Recently these products have become popular in the food industry because of a number of interesting medicinal properties that have been associated with certain edible marine algae. Very little control exists over the composition of these products, which could be contaminated with a number of agents including heavy metals and certain radioactive isotopes. Fifteen seaweed samples Žsix local samples from the coast of British Columbia, seven from Japan, one from Norway and one undisclosed. were obtained. All samples were analyzed for multiple elements, using ICP mass spectrometry and for radioactive constituents. It was found that six of eight imported seaweed products had concentrations of mercury orders of magnitude higher than the local products. Lead was found at somewhat higher concentrations in only one local product. Laminaria japonica had the highest level of iodine content followed by Laminaria setchellii from local sources. Only traces of cesium-137 were found in a product from Norway and radium-226 was found in a product from Japan. Arsenic levels were found to be elevated. In order to estimate the effect of these levels on health, one needs to address the bioavalability and the speciation of arsenic in these samples. Q 2000 Elsevier Science B.V. All rights reserved. Keywords: Marine algae; Health foods; Iodine; Multi elemental analysis; Mercury; Lead; Nutrition; Radioactivity; Seaweed
U
Corresponding author. Tel.: q1-604-822-5688; fax: q1-604-822-4994. E-mail address: [email protected] ŽC. van Netten.. 0048-9697r00r$ - see front matter Q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 0 0 . 0 0 4 6 7 - 8
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C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
1. Introduction With the current trend in the consumption of health foods by the general public, health food stores are increasingly offering more exotic products. Often little is known about the history of these products except that they have been used for years in a number of foreign countries as remedies, as food items, or as food supplements. Although seaweed has been used historically as a source of alginates as an emulsifier in the food industry ŽKoppel, 1997., recent reports of interesting medicinal properties associated with a number of seaweeds have sparked consumer interest. Some of these properties include anti-HIV effects ŽBeres et al., 1993., anti-tumour activity in Laminaria japonica Žkombu., Undaria pinnatifida Žwakame., Hijiki fusiforme Žhijiki., and Pophyra tenera Žnori. ŽEllouali et al., 1993; Okai et al., 1993, 1996, 1997., potential contraceptive effects ŽPremakumara et al., 1995., and a source of iodine and other nutrient elements ŽLee et al., 1994; Cho et al., 1995; Hou et al., 1997.. The recent increased interest in the utilization of edible seaweeds by the general public ŽDarcy-Vrillon, 1993; Koppel, 1997. has, therefore, resulted in many seaweed varieties, and seaweed derived products, that are available from health food stores. As with other food items that can be purchased such as vegetables, the contents of these materials are generally not subject to chemical analysis and their composition does not have to be disclosed even if these were actually known. The controls over the quality of vegetables are instituted at the front end, i.e. there are strict regulation regarding soil conditions and the use of pesticides and fertilizers that are used to cultivate these items. No such controls exist when it relates to edible seaweeds that are grown in a media over which one has often little control. There is always the possibility of local anomalies andror activities in the region where seaweed crops are harvested that might pollute the local habitat ŽSharp et al., 1988. As it has been well documented that certain types of marine algae have a high affinity for
heavy metals ŽBryan et al., 1973; Volesky, 1994., a survey of the heavy metal content of a number of seaweed preparations, taken from the shelf of local health food stores, was performed. It has also been observed that seaweed can be contaminated with radioactive isotopes ŽDickson, 1984. and the samples were, therefore, selected to determine if naturally occurring radionuclides, or man-made nuclides, were being concentrated in the commercially available edible marine algae. This communication reports on the findings and significance of our results.
2. Methods The following local and imported seaweed samples were obtained in British Columbia in dried form: Alaria marginata, Laminaria saccharina, L. setchellii sil¨ a, Macrocystis integrifolia, Nereocystis leutkeana ŽCanadian Kelp Resources, source: Bamfield, BC, Canada.; kelp tablets a1, Fucus ¨ esiculosis ŽLondon Drugs, source: Norway.; kelp tablets a2, ŽLondon Drugs, source: undisclosed.; Undaria pinnatifida ŽCrown Trading Co Ltd, source: Japan.; L. japonica, Porphyra tenera ŽFujiya Foods, source: Japan.; Eisenia bicyclis, Hizikia fusiformis, P. tenera, Undaria pinnatifida ŽKoyo Food Ltd; source: Mitoku, Japan.. An effort was made to acquire a wide variety of different species. A 0.5-g sample was selected at random from each source, i.e. a packet of seaweed was opened, a pair of tweezers was inserted and 0.5 g was taken from the first leaf that was extracted. Samples for analyses were digested in concentrated nitric acid by a local commercial laboratory ŽElemental Research, Vancouver, BC, Canada. prior to the ICPMS multi elemental analysis for Al, V, Cr, Mn, Fe, Cu, Zn, As, Pb, Cd, Hg, Se, Mo, Sn, I, U, Ni, and Co. All final results were blank subtracted in order to compensate for the possible elemental interference from the blank as well as for argon oxide interference with the identification of Fe and Cr as a result of molecular ion formation in the argon plasma during the analysis. The accuracy of this procedure was verified against the NBS 1566A CRM ŽNational Institute of Standards and Technology.
Nereocytis leutkeana ŽBull kelp. Undaria pinnatifida ŽWakame . Eisenia bicyclis ŽArame . Hizikia fusiformis ŽHijiki. Porphyra tenera ŽAsakusa-nori. Laminaria japonica ŽMakombu . Porphyra tenera ŽAsakusa-nori. Undaria pinnatifida ŽWakame . Fucus ¨ esiculosis ŽBladderwrack . Kelp tablets ŽSpecies not listed. Laminaria Setchellii ŽSplit Kelp. Laminaria saccharina ŽSugar kelp. Alaria marginata ŽWinged kelp . Macrocystis integrifolia ŽGiant kelp. Nereocytis leutkeana ŽBull kelp.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 3.90
- 0.5
0.36 0.022
7.6 ]
10 ] 10]15 ] ]
40
20 40 80 30 110 80 190 20 520 1040 - 10 40 60 110
Fe
0.065 ]
0.5 ] ] 1.5]3 ]
- 0.5
0.9 1.1 3.3 0.9 6.3 - 0.5 8.9 - 0.5 1.4 2.2 - 0.5 - 0.5 - 0.5 - 0.5
Cu
0.27 0.029
0.05 ] 12]15 ] ]
8.1
10 13 14 4 31 13 37 14 24 23 22.3 8.5 23.6 6.9
Zn
c
b
Maximum allowable content in drinking water ŽHealth Canada, 1996 .. Recommended dietary allowance ŽNational Research Council, 1989 .. Estimated safe and adequate daily dietary intake ŽNational Research Council, 1989 .. d Estimated daily dietary intake ŽUthus and Seaborn, 1996 .. e Estimated daily intake based on an average consumption of 7.3 grday in Japan ŽToyokawa, 1978 ..
a
0.084 ]
0.029 0.0004
5.55 6.46 13.8 5.77 32.3 6.79 48.9 3.3 27.9 34.9 3.67 3.04 3.79 9.96
1.3 0.7 - 0.5 0.8 - 0.5 1.0 2.0 0.8 11.5 11.4 - 0.5 - 0.5 - 0.5 0.12
Mn
EDI Žmgrday.e Upper level Lower level
1.43
1.05 0.39 0.72 0.75 3.96 1.17 1.53 0.46 2.21 2.1 0.43 0.66 0.57 3.66
Cr
0.05 0.5 0.05 ] 0.05 ] ] ] ] ] 0.05]0.2 2]5 0.01]0.02 ] ]
V
Element content Žm grg dry wt..
Detection limit Žm grg. MAC Žmgrl.a RDA Žmgrday.b ESADDI Žmgrday.c EDDI Žmgrday.d
15
Species Žcommon name .
Sample no.
Table 1 Multi elemental analysis of selected essential elements in commercially available edible marine algae
0.11 ]
0.05 ] ] ] 0.1
0.94
2.83 - 0.05 8.15 - 0.05 10.17 - 0.05 - 0.05 - 0.05 15.29 9.82 1.31 0.57 1.51 1.48
Ni
0.64 0.12
0.045 ]
0.05
0.11 0.06 0.05 0.03 0.10 0.17 0.05 0.01 0.03 0.10 0.46 0.37 - 0.01 0.13
Sn
0.008 ]
]
0.003
0.01 0.01 ] ] ] ] 0.075]0.25 ] ] ]
- 0.01
0.2 0.25 0.34 0.26 0.59 0.2 0.61 0.07 0.61 1.13 - 0.01 - 0.01 0.07 0.08
Mo
0.1 0.01 0.05]0.07 ] ]
- 0.1
6 3 - 0.1 4 2 2 2 3 1 1 - 0.1 5.7 0.7 6.2
Se
0.5 0.025 ] ] 0.012] 0.015
66.3
79 55 31 88 29 29 29 20 20 17 58.5 76.2 39.5 53.1
As
0.042
0.449 0.026 0.200 0.061 0.566 0.449 0.470 0.098 0.386 0.594 0.185 0.084 0.151 0.163
Co
15 0.004 0.12 0.0002
1 0.005 ] ] 0.15 ] ] ] ]
80
734 102 600 436 17 2110 185 60 732 815 1070 238 151 240
I
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175 171
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
172
that both types of kelp tablets Žsamples a9 and a10. were two orders of magnitude higher in their aluminum content compared to most of the other samples and only one order of magnitude relative to the giant kelp sample. The same tablets were also consistently higher in their chromium and iron content. Both nori samples as well as the local giant kelp sample showed elevated iron, manganese, and zinc content. Imported kombu Ž L. japonica. had a much higher iodine content than the samples of kombu from local sources Ž L. saccharina, L. setchellii .. For example, locally derived L. setchellii had an iodine content of 1070 mgrg, half of the iodine content found in the imported L. japonica Ž2110 mgrg.. Virtually all locally grown seaweeds were much lower in their copper, molybdenum, mercury and uranium content compared to all other samples. In five of seven algae samples from Japan the mercury content was orders of magnitude higher
and dolt-2 CRM ŽNational Research Council, Canada. certified standards. The presence of gamma ray emitting radionuclides Žcesium-137, iodine-131, potassium-40, radium-226, tin-125. was assessed using an Aptec Phyge germanium detector and analyzed using Canberra Spectran-AT software. Samples were counted for a minimum of 8 h.
3. Results The results of the multi elemental analysis of the 15 samples identified have been summarized in Tables 1 and 2 along with some reference values. These include the maximum dietary concentration ŽMAC. in drinking water, a number of other dietary intake values, and an estimate based on an average Japanese consumption of 7.3 g of algae per day ŽToyokawa, 1978.. It can be noted
Table 2 Multi elemental analysis of non-essential metal Žmgrg. and radionuclide ŽBqrkg. content in dried commercially available edible marine algae. Sample no.
Name
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
N. leutkeana 5.0 U. pinnitifida 3.0 E. bicyclis 6.5 H. fusiformis 5.2 P. tenera 4.0 L. japonica 8.9 P. tenera 2.6 U. pinnitifida 1.9 F. ¨ esiculosis 228 Kelp tablets 280 L. setchellii 2.3 L. saccharina 7.0 A. marginata 7.3 M. integrifolia 51.4 N. leutkeana 9.8
Detection limit MAC Žmgrl.a MAC ŽBqrl.a EDI Žmgrday.b Upper level Lower level a b
Element content Al
Hg
Pb
U
Cd
131
- 0.05 0.24 - 0.05 0.32 0.44 0.40 0.24 - 0.05 1.08 0.24 - 0.05 - 0.05 - 0.05 - 0.05 - 0.05
- 0.01 0.14 0.31 0.16 0.28 0.22 0.14 0.21 0.38 0.57 - 0.01 - 0.01 0.64 0.19 0.08
- 0.01 0.03 0.94 0.82 0.27 0.50 - 0.01 0.72 0.85 1.01 - 0.01 - 0.01 - 0.01 - 0.01 0.26
2.76 0.71 0.57 0.32 0.27 0.02 0.83 0.51 0.34 0.13 0.10 2.80 0.45 0.90 0.30
- 7.4 - 7.0 - 6.2 - 1.4 - 6.5 - 3.7 - 14.0 - 34.0 - 0.7 - 0.8 - 3.7 - 6.4 - 7.0 - 9.3 - 7.4
0.5 ] ]
0.05 0.001 ]
0.01 0.01 ]
0.01 0.1 ]
0.01 0.005 ]
2.0 0.014
0.008 ]
0.005 ]
0.007 0.028 ] 0.0001
I
] 6.0
137
125
- 14.0 - 14.0 - 11.5 - 1.6 6.1" 3.2 - 7.1 - 21.0 - 53.0 0.8" 0.4 - 1.4 - 6.3 - 9.8 - 12.5 - 15.0 - 13.0
- 27 - 23 - 19 -3 - 17 - 13 - 41 - 98 -2 -3 - 12 - 22 - 20 - 30 - 21
Cs
] 10.0
Sn
] ]
Maximum allowable content in drinking water ŽHealth Canada, 1996.. Estimated daily intake based on an average consumption of 7.3 grday in Japan ŽToyokawa, 1978..
226
Ra
- 122 - 138 58 " 37 - 15 - 103 - 68 - 245 206 " 203 5"4 - 14 - 61 - 108 - 103 - 131 - 116 ] 0.6
40
K
4370 " 186 - 453 529 " 74 2450 " 37 1110 " 80 - 401 693 " 118 - 860 551 " 13 385 " 16 - 188 - 482 918 " 81 - 571 2860 " 145 ] ]
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
than the local samples. The Norwegian kelp tablets, sample a9, had a mercury content three orders of magnitude above the local samples. The lowest levels of lead were encountered in three of six of the locally grown samples. Cadmium content was elevated compared to other samples in two locally grown seaweed samples. In five of seven seaweed samples, from Japanese origin, the nickel content was quite low Ž- 0.05 mgrg.. The analysis of radionuclides is summarized in Table 2 and showed little activity above background. The Norwegian kelp tablets and P. tenera from Japan showed measurable traces of cesium137. Three samples, two from Japan Ž E. bicyclis and U. pinnaitifida. and one from Norway Ž F. ¨ esiculosis., showed traces of radium-226. The naturally occurring isotope, potassium-40, was found in most samples as expected based on its universal presence in seawater. It appears that the average daily intake, based on Japanese algae consumption estimates, and assuming exposure to algae with the highest elemental concentrations, is generally well below the various daily dietary intake values as shown in Tables 1 and 2 with the exception for arsenic, iodine, mercury, and cadmium.
4. Discussion It was interesting to note that mercury, copper and uranium were all below the detection limit in most of the locally grown seaweed samples. The lowest and highest levels of lead were also found in locally grown seaweed. Three out of six samples were below the detection limit indicating that lead is not an ubiquitous contaminant. The measurable levels of lead in the other three samples might very well be a reflection of a point source. Many point sources of lead can be expected as lead weights currently are, and have been for many years, used in the fishing industry in the region where these samples were harvested. The same argument could be made for the variation in zinc content which was double to triple in some of the local samples and even higher in two out of seven Japanese samples. Zinc is a known constituent in marine craft as anodic protection
173
against corrosion of brass components that are exposed to seawater. It could be argued that winged, giant, and bull kelp appear to have a special affinity for lead and perhaps some of the other elements. Although the other bull kelp sample showed a low lead content, but a much higher cadmium content, this could be due to variations in the presence of lead and cadmium. Another possibility that could explain the different uptake in kelp grown in the same environment would be the time of harvesting. It has been shown in wakame ŽIto and Miyosshi, 1990. for instance, that certain elements such as zinc appear to be taken up at different rates at different stages of growth. Local variation in salinity has also been shown to be an important factor in the biological uptake of a number of elements ŽCho et al., 1995; Struck et al., 1997.. Seaweed has long been regarded as an excellent source of iodine. The iodine content in a number of commercially available seaweeds in Britain, reported by Lee et al. Ž1994., are very similar to those observed in our analysis and compare as follows Žin mgrg dry wt..: wakame 104 vs. 102, arame 706 vs. 600, hijiki 319 vs. 436, nori 4.3 vs. 16.9, and kombu Ž L. japonica. 2660 vs. 2110. In this study, there appeared to be insufficient man-made radionuclides in the water or they are not being accumulated to produce concentrations in the algae that are of health significance. All samples were less than the drinking water guidelines and edible algae would not be nearly as significant a pathway for uptake as drinking water. The Canadian guidelines for radionuclides in drinking water are: iodine-131, 6 Bqrkg; cesium-137, 10 Bqrkg; and radium-226, 0.6 Bqrkg. There are no guidelines for potassium-40 as it just reflects the potassium content. There are no guidelines for tin-125. Iodine-131, cesium-137, tin-125 are the primary gamma-emitting radionuclides, residual from both nuclear bomb and nuclear power releases. In the event of a nuclear release cesium-137 and iodine-131 are considered more significant ŽUNCEIAR, 1988.. The traces of cesium]137 that were found in two samples could be a reflection of past nuclear accidents such as
174
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
Chernobyl ŽUNCEIAR, 1988; Druehl et al., 1988.. Iodine-131 is also used in medical procedures and thereby finds its way into the environment ŽWaller and Cole, 1999.. Radium-226 is a key decay product from the most abundant natural uranium decay series. It is found in seawater in concentrations ranging from 0.74 to 3.7 Bqrl ŽIAEA, 1990.. There was not sufficient material to reduce the detection limits for radium-226 to meaningful health values. It might be useful in the future to repeat using larger samples or a chemical analysis method. Some radium-226 may be concentrated in the algae from the seawater. Potassium-40 is found in a fixed ratio to non-radioactive potassium and, therefore, reflects the potassium content of the algae. The content in the soil is approximately 400 Bqrkg ŽAECB, 1995. and the average potassium-40 content of seawater is 12 Bqrl. Although the potassium-40 concentrations in the different algae varied widely these levels are considered to be of no health consequence because of the low activity associated with this isotope. Speciation and bioavalability of the various elements dealt with in this communication have not been addressed and needs to be assessed if one wants an accurate measure of the biological effects associated with intake of these seaweed products. This is particularly important for elements such as arsenic and chromium. It has been shown that arsenic III is taken up at a different rate than arsenic V ŽBertolero et al., 1987.. Similarly certain organic arsenic compounds such as the arseno betaines, commonly found in seafood, are not taken up and are therefore, not bioavailable ŽVahter et al., 1983.. These observations should be kept in mind when comparing the arsenic values in Table 1, which range from 71 to 88 mgrg, to the maximum allowable content ŽMAC. in drinking water ŽHealth Canada, 1996. for arsenic Ž0.025 mgrl., assuming an average daily consumption of 1.5 l per person. These principles do not apply to the mercury content measured in these samples and 1.5 kelp tablets from sample a9 has the equivalent mercury content of 1000 l of drinking water containing the MAC of 0.001 mgrl. Whether this mercury is in the organic form is also not known from this research but is,
in contrast to arsenic, extremely important as this form of mercury is more toxic than the inorganic form. It should also be pointed out that the results presented here are based on randomly selected single samples, and are not necessarily representative of the algal products that are currently available.
5. Conclusions Locally derived edible algae samples were generally much lower in their heavy metal content specifically mercury. The mercury content of some samples could prove to be a significant source of mercury exposure. Speciation and bioavailability of arsenic needs to be determined to assess the exposure to this metal. The iodine content of algae was found to vary widely with the highest concentrations in wakame from Japan. Some samples showed traces of cesium-137 and radium226. The former is likely related to the Chernobyl accident whereas the latter could be a reflection of naturally occurring uranium decay. References Atomic Energy Control Board ŽAECB.. Canada: living with radiation. 1995, p. 9. Beres A, Wasserman O, Bruhn T et al. A new procedure for the isolation of anti-HIV compounds Žpolysaccharides and polyphenols. from the marine alga Fucus ¨ esiculosus. J Nat Prod 1993;56:478]488. Bertolero F, Pozzi G, Sabbioni E, Saffiotti U. Cellular uptake and metabolic reduction of pentavalent to trivalent arsenic as determinants of cytotoxicity and morphological transformation. Carcinogenesis 1987;8:803. Bryan GW, Hummerstone LG. Brown seaweed is an indicator of heavy metals in estuaries in south-west England. J Mar Biol Assoc UK 1973;53:705]720. Cho DM, Kim DS, Lee DS, Kim HR, Pyeun JH. Trace components and functional saccharides in seaweed. 1: changes in proximate composition and trace elements according to harvest season and places. Bull Korean Fish Soc 1995;28:49]59. Darcy-Vrillon B. Nutritional aspects of the developing use of marine macroalgae for the human food industry. Int J Food Sci Nutr 1993;44:S23]S35. Dickson D. Radioactive seaweed stirs UK low-level waste fight. Science 1984;223:35.
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175 Druehl L, Cackette M, D’Auria JM. Temporal and spatial distribution of iodine-131 in the brown seaweed Fucus subsequent to the Chernobyl incident. J Mar Biol 1988;98:125]129. Ellouali M, Boisson-Vidal C, Durand P, Jozefonvicz J. Antitumour activity of low molecular weight fucans extracted from brown seaweed Ascophyllum nodosum. Anticancer Res 1993;13:2011]2019. Health Canada. Federal-Provincial Subcommittee on Drinking Water. Guidelines for Canadian Drinking Water Quality, Supporting Documentation, 1996:2]4. Hou X, Chai C, Qian Q, Yan X, Fan X. Determination of chemical species of iodine in some seaweeds ŽI.. Sci Total Environ 1997;204:215]221. International Atomic Energy Agency ŽIAEA.. The Environmental Behavior of Radium, vol 1. Vienna, 1990, p. 78. Ito S, Miyosshi T. Determination of Mg and Zn contents of Naruto ‘wakame’ ŽUndaria pinnatifida.. Nippon Eiseigaku Zasshi 1990;45:795]800. Koppel T. Forests of the Sea. Canadian Geographic 1997; MarchrApril: 68]76. Lee SM, Lewis J, Buss DH. Iodine in British foods and diets. Br J Nutr 1994;72:435]446. National Research Council, Food and Nutrition Board, Commission of Life Sciences. Recommended Dietary Allowances, 10th ed. Washington, DC: National Academy Press, 1989, pp. 284]285. Okai Y, Hagashi-Okai K, Yano Y, Otani S. Identification of antimutagenic substances in an extract of edible red alga, Porphyra tenera Žasakusa-nori .. Cancer Lett 1996;100: 235]240. Okai Y, Higashi-Okai K, Ishizaka S, Nakamura SI. Identification of heterogenous antimutagenic activities in the extract of edible brown seaweeds, Laminaria japonica Žmakobu., Undaria pinnatifida Žwakame. by the immu gene expression system in Salmonella typhimurium. Mutat Res 1993;303: 63]70.
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Okai Y, Higashi-Okai K, Ishizaka S, Yamashita U. Enhancing effect of polysaccharides from an edible brown alga, Hijikia fusiforme ŽHijiki. on release of tumour necrosis factoralpha from macrophages of endotoxin-nonresponder C3HrHeJ mice. Nutr Cancer 1997;27:74]79. Premakumara GA, Ratnosooriya WD, Tillekeratne LM. Studies on the post-coital contraceptive mechanism of crude extract of Sri Lankan red algae, Gelidiella acrosa. Contraception 1995;52:203]207. Sharp GJ, Samant HS, Vaidya OC. Selected metal levels of commercial valuable seaweed adjacent to and distant from point sources of contamination in Nova Scotia and New Brunswick. Bull Environ Contam Toxicol 1988;40:724]730. Struck BD, Pelzer R, Ostapzuk P, Emons H, Mohl C. Statistical evaluation of ecosystem properties influencing the uptake of As, Cd, Co, Cu, Hg, Mn, Ni, and Zn in seaweed Ž Fucus ¨ esiculosis. and common mussel Ž Mytilus edulis.. Sci Total Environ 1997;207:29]42. Toyokawa H. Nutritional status in Japan from the viewpoint of numerical ecology. Soc Sci Med 1978;12A:517]524. United Nations Committee on the Effects of Ionizing Atomic Radiation ŽUNCEIAR.. Sources, Effects and the Risks of Ionizing Radiation. 1988, p. 12. Uthus EO, Seaborn CD. Deliberations and evaluations of the approaches, endpoints and paradigms for dietary recommendations of the other trace elements. J Nutr 1996; 126:2452S]2459S. Vahter M, Marafanti E, Dencker L. Metabolism of arseno betaine in mice, rats, and rabbits. Sci Total Environ 1983;30:197. Volesky B. Advances in biosorption of metals: selection of biomass types. FEMS Microbiol Rev 1994;14:291]302. Waller EJ, Cole D. An environmental radionuclide baseline study near three Canadian naval ports. Health Phys 1999; 77:37]42.
Elemental and radioactive analysis of commercially available seaweed C. van Netten a,U , S.A. Hoption Cannb,c , D.R. Morley d, J.P. van Netten b,c a
Department of Health Care and Epidemiology, James Mather Building, Uni¨ ersity of British Columbia, 5804 Fair¨ iew A¨ enue, Vancou¨ er, BC V6T 1Z3, Canada b Special De¨ elopment Laboratory, Royal Jubilee Hospital, Victoria, BC V8X 1P2, Canada c Department of Biology, Uni¨ ersity of Victoria, Victoria, BC V8W 3N5, Canada d Radiation Protection Branch, Ministry of Health, 4940 Canada Way, Burnaby, BC V5G 4K6, Canada Received 12 October 1999; accepted 25 February 2000
Abstract Edible seaweed products have been used in many countries, specifically Japan, as a food item. Recently these products have become popular in the food industry because of a number of interesting medicinal properties that have been associated with certain edible marine algae. Very little control exists over the composition of these products, which could be contaminated with a number of agents including heavy metals and certain radioactive isotopes. Fifteen seaweed samples Žsix local samples from the coast of British Columbia, seven from Japan, one from Norway and one undisclosed. were obtained. All samples were analyzed for multiple elements, using ICP mass spectrometry and for radioactive constituents. It was found that six of eight imported seaweed products had concentrations of mercury orders of magnitude higher than the local products. Lead was found at somewhat higher concentrations in only one local product. Laminaria japonica had the highest level of iodine content followed by Laminaria setchellii from local sources. Only traces of cesium-137 were found in a product from Norway and radium-226 was found in a product from Japan. Arsenic levels were found to be elevated. In order to estimate the effect of these levels on health, one needs to address the bioavalability and the speciation of arsenic in these samples. Q 2000 Elsevier Science B.V. All rights reserved. Keywords: Marine algae; Health foods; Iodine; Multi elemental analysis; Mercury; Lead; Nutrition; Radioactivity; Seaweed
U
Corresponding author. Tel.: q1-604-822-5688; fax: q1-604-822-4994. E-mail address: [email protected] ŽC. van Netten.. 0048-9697r00r$ - see front matter Q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 8 - 9 6 9 7 Ž 0 0 . 0 0 4 6 7 - 8
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C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
1. Introduction With the current trend in the consumption of health foods by the general public, health food stores are increasingly offering more exotic products. Often little is known about the history of these products except that they have been used for years in a number of foreign countries as remedies, as food items, or as food supplements. Although seaweed has been used historically as a source of alginates as an emulsifier in the food industry ŽKoppel, 1997., recent reports of interesting medicinal properties associated with a number of seaweeds have sparked consumer interest. Some of these properties include anti-HIV effects ŽBeres et al., 1993., anti-tumour activity in Laminaria japonica Žkombu., Undaria pinnatifida Žwakame., Hijiki fusiforme Žhijiki., and Pophyra tenera Žnori. ŽEllouali et al., 1993; Okai et al., 1993, 1996, 1997., potential contraceptive effects ŽPremakumara et al., 1995., and a source of iodine and other nutrient elements ŽLee et al., 1994; Cho et al., 1995; Hou et al., 1997.. The recent increased interest in the utilization of edible seaweeds by the general public ŽDarcy-Vrillon, 1993; Koppel, 1997. has, therefore, resulted in many seaweed varieties, and seaweed derived products, that are available from health food stores. As with other food items that can be purchased such as vegetables, the contents of these materials are generally not subject to chemical analysis and their composition does not have to be disclosed even if these were actually known. The controls over the quality of vegetables are instituted at the front end, i.e. there are strict regulation regarding soil conditions and the use of pesticides and fertilizers that are used to cultivate these items. No such controls exist when it relates to edible seaweeds that are grown in a media over which one has often little control. There is always the possibility of local anomalies andror activities in the region where seaweed crops are harvested that might pollute the local habitat ŽSharp et al., 1988. As it has been well documented that certain types of marine algae have a high affinity for
heavy metals ŽBryan et al., 1973; Volesky, 1994., a survey of the heavy metal content of a number of seaweed preparations, taken from the shelf of local health food stores, was performed. It has also been observed that seaweed can be contaminated with radioactive isotopes ŽDickson, 1984. and the samples were, therefore, selected to determine if naturally occurring radionuclides, or man-made nuclides, were being concentrated in the commercially available edible marine algae. This communication reports on the findings and significance of our results.
2. Methods The following local and imported seaweed samples were obtained in British Columbia in dried form: Alaria marginata, Laminaria saccharina, L. setchellii sil¨ a, Macrocystis integrifolia, Nereocystis leutkeana ŽCanadian Kelp Resources, source: Bamfield, BC, Canada.; kelp tablets a1, Fucus ¨ esiculosis ŽLondon Drugs, source: Norway.; kelp tablets a2, ŽLondon Drugs, source: undisclosed.; Undaria pinnatifida ŽCrown Trading Co Ltd, source: Japan.; L. japonica, Porphyra tenera ŽFujiya Foods, source: Japan.; Eisenia bicyclis, Hizikia fusiformis, P. tenera, Undaria pinnatifida ŽKoyo Food Ltd; source: Mitoku, Japan.. An effort was made to acquire a wide variety of different species. A 0.5-g sample was selected at random from each source, i.e. a packet of seaweed was opened, a pair of tweezers was inserted and 0.5 g was taken from the first leaf that was extracted. Samples for analyses were digested in concentrated nitric acid by a local commercial laboratory ŽElemental Research, Vancouver, BC, Canada. prior to the ICPMS multi elemental analysis for Al, V, Cr, Mn, Fe, Cu, Zn, As, Pb, Cd, Hg, Se, Mo, Sn, I, U, Ni, and Co. All final results were blank subtracted in order to compensate for the possible elemental interference from the blank as well as for argon oxide interference with the identification of Fe and Cr as a result of molecular ion formation in the argon plasma during the analysis. The accuracy of this procedure was verified against the NBS 1566A CRM ŽNational Institute of Standards and Technology.
Nereocytis leutkeana ŽBull kelp. Undaria pinnatifida ŽWakame . Eisenia bicyclis ŽArame . Hizikia fusiformis ŽHijiki. Porphyra tenera ŽAsakusa-nori. Laminaria japonica ŽMakombu . Porphyra tenera ŽAsakusa-nori. Undaria pinnatifida ŽWakame . Fucus ¨ esiculosis ŽBladderwrack . Kelp tablets ŽSpecies not listed. Laminaria Setchellii ŽSplit Kelp. Laminaria saccharina ŽSugar kelp. Alaria marginata ŽWinged kelp . Macrocystis integrifolia ŽGiant kelp. Nereocytis leutkeana ŽBull kelp.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 3.90
- 0.5
0.36 0.022
7.6 ]
10 ] 10]15 ] ]
40
20 40 80 30 110 80 190 20 520 1040 - 10 40 60 110
Fe
0.065 ]
0.5 ] ] 1.5]3 ]
- 0.5
0.9 1.1 3.3 0.9 6.3 - 0.5 8.9 - 0.5 1.4 2.2 - 0.5 - 0.5 - 0.5 - 0.5
Cu
0.27 0.029
0.05 ] 12]15 ] ]
8.1
10 13 14 4 31 13 37 14 24 23 22.3 8.5 23.6 6.9
Zn
c
b
Maximum allowable content in drinking water ŽHealth Canada, 1996 .. Recommended dietary allowance ŽNational Research Council, 1989 .. Estimated safe and adequate daily dietary intake ŽNational Research Council, 1989 .. d Estimated daily dietary intake ŽUthus and Seaborn, 1996 .. e Estimated daily intake based on an average consumption of 7.3 grday in Japan ŽToyokawa, 1978 ..
a
0.084 ]
0.029 0.0004
5.55 6.46 13.8 5.77 32.3 6.79 48.9 3.3 27.9 34.9 3.67 3.04 3.79 9.96
1.3 0.7 - 0.5 0.8 - 0.5 1.0 2.0 0.8 11.5 11.4 - 0.5 - 0.5 - 0.5 0.12
Mn
EDI Žmgrday.e Upper level Lower level
1.43
1.05 0.39 0.72 0.75 3.96 1.17 1.53 0.46 2.21 2.1 0.43 0.66 0.57 3.66
Cr
0.05 0.5 0.05 ] 0.05 ] ] ] ] ] 0.05]0.2 2]5 0.01]0.02 ] ]
V
Element content Žm grg dry wt..
Detection limit Žm grg. MAC Žmgrl.a RDA Žmgrday.b ESADDI Žmgrday.c EDDI Žmgrday.d
15
Species Žcommon name .
Sample no.
Table 1 Multi elemental analysis of selected essential elements in commercially available edible marine algae
0.11 ]
0.05 ] ] ] 0.1
0.94
2.83 - 0.05 8.15 - 0.05 10.17 - 0.05 - 0.05 - 0.05 15.29 9.82 1.31 0.57 1.51 1.48
Ni
0.64 0.12
0.045 ]
0.05
0.11 0.06 0.05 0.03 0.10 0.17 0.05 0.01 0.03 0.10 0.46 0.37 - 0.01 0.13
Sn
0.008 ]
]
0.003
0.01 0.01 ] ] ] ] 0.075]0.25 ] ] ]
- 0.01
0.2 0.25 0.34 0.26 0.59 0.2 0.61 0.07 0.61 1.13 - 0.01 - 0.01 0.07 0.08
Mo
0.1 0.01 0.05]0.07 ] ]
- 0.1
6 3 - 0.1 4 2 2 2 3 1 1 - 0.1 5.7 0.7 6.2
Se
0.5 0.025 ] ] 0.012] 0.015
66.3
79 55 31 88 29 29 29 20 20 17 58.5 76.2 39.5 53.1
As
0.042
0.449 0.026 0.200 0.061 0.566 0.449 0.470 0.098 0.386 0.594 0.185 0.084 0.151 0.163
Co
15 0.004 0.12 0.0002
1 0.005 ] ] 0.15 ] ] ] ]
80
734 102 600 436 17 2110 185 60 732 815 1070 238 151 240
I
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175 171
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
172
that both types of kelp tablets Žsamples a9 and a10. were two orders of magnitude higher in their aluminum content compared to most of the other samples and only one order of magnitude relative to the giant kelp sample. The same tablets were also consistently higher in their chromium and iron content. Both nori samples as well as the local giant kelp sample showed elevated iron, manganese, and zinc content. Imported kombu Ž L. japonica. had a much higher iodine content than the samples of kombu from local sources Ž L. saccharina, L. setchellii .. For example, locally derived L. setchellii had an iodine content of 1070 mgrg, half of the iodine content found in the imported L. japonica Ž2110 mgrg.. Virtually all locally grown seaweeds were much lower in their copper, molybdenum, mercury and uranium content compared to all other samples. In five of seven algae samples from Japan the mercury content was orders of magnitude higher
and dolt-2 CRM ŽNational Research Council, Canada. certified standards. The presence of gamma ray emitting radionuclides Žcesium-137, iodine-131, potassium-40, radium-226, tin-125. was assessed using an Aptec Phyge germanium detector and analyzed using Canberra Spectran-AT software. Samples were counted for a minimum of 8 h.
3. Results The results of the multi elemental analysis of the 15 samples identified have been summarized in Tables 1 and 2 along with some reference values. These include the maximum dietary concentration ŽMAC. in drinking water, a number of other dietary intake values, and an estimate based on an average Japanese consumption of 7.3 g of algae per day ŽToyokawa, 1978.. It can be noted
Table 2 Multi elemental analysis of non-essential metal Žmgrg. and radionuclide ŽBqrkg. content in dried commercially available edible marine algae. Sample no.
Name
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
N. leutkeana 5.0 U. pinnitifida 3.0 E. bicyclis 6.5 H. fusiformis 5.2 P. tenera 4.0 L. japonica 8.9 P. tenera 2.6 U. pinnitifida 1.9 F. ¨ esiculosis 228 Kelp tablets 280 L. setchellii 2.3 L. saccharina 7.0 A. marginata 7.3 M. integrifolia 51.4 N. leutkeana 9.8
Detection limit MAC Žmgrl.a MAC ŽBqrl.a EDI Žmgrday.b Upper level Lower level a b
Element content Al
Hg
Pb
U
Cd
131
- 0.05 0.24 - 0.05 0.32 0.44 0.40 0.24 - 0.05 1.08 0.24 - 0.05 - 0.05 - 0.05 - 0.05 - 0.05
- 0.01 0.14 0.31 0.16 0.28 0.22 0.14 0.21 0.38 0.57 - 0.01 - 0.01 0.64 0.19 0.08
- 0.01 0.03 0.94 0.82 0.27 0.50 - 0.01 0.72 0.85 1.01 - 0.01 - 0.01 - 0.01 - 0.01 0.26
2.76 0.71 0.57 0.32 0.27 0.02 0.83 0.51 0.34 0.13 0.10 2.80 0.45 0.90 0.30
- 7.4 - 7.0 - 6.2 - 1.4 - 6.5 - 3.7 - 14.0 - 34.0 - 0.7 - 0.8 - 3.7 - 6.4 - 7.0 - 9.3 - 7.4
0.5 ] ]
0.05 0.001 ]
0.01 0.01 ]
0.01 0.1 ]
0.01 0.005 ]
2.0 0.014
0.008 ]
0.005 ]
0.007 0.028 ] 0.0001
I
] 6.0
137
125
- 14.0 - 14.0 - 11.5 - 1.6 6.1" 3.2 - 7.1 - 21.0 - 53.0 0.8" 0.4 - 1.4 - 6.3 - 9.8 - 12.5 - 15.0 - 13.0
- 27 - 23 - 19 -3 - 17 - 13 - 41 - 98 -2 -3 - 12 - 22 - 20 - 30 - 21
Cs
] 10.0
Sn
] ]
Maximum allowable content in drinking water ŽHealth Canada, 1996.. Estimated daily intake based on an average consumption of 7.3 grday in Japan ŽToyokawa, 1978..
226
Ra
- 122 - 138 58 " 37 - 15 - 103 - 68 - 245 206 " 203 5"4 - 14 - 61 - 108 - 103 - 131 - 116 ] 0.6
40
K
4370 " 186 - 453 529 " 74 2450 " 37 1110 " 80 - 401 693 " 118 - 860 551 " 13 385 " 16 - 188 - 482 918 " 81 - 571 2860 " 145 ] ]
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
than the local samples. The Norwegian kelp tablets, sample a9, had a mercury content three orders of magnitude above the local samples. The lowest levels of lead were encountered in three of six of the locally grown samples. Cadmium content was elevated compared to other samples in two locally grown seaweed samples. In five of seven seaweed samples, from Japanese origin, the nickel content was quite low Ž- 0.05 mgrg.. The analysis of radionuclides is summarized in Table 2 and showed little activity above background. The Norwegian kelp tablets and P. tenera from Japan showed measurable traces of cesium137. Three samples, two from Japan Ž E. bicyclis and U. pinnaitifida. and one from Norway Ž F. ¨ esiculosis., showed traces of radium-226. The naturally occurring isotope, potassium-40, was found in most samples as expected based on its universal presence in seawater. It appears that the average daily intake, based on Japanese algae consumption estimates, and assuming exposure to algae with the highest elemental concentrations, is generally well below the various daily dietary intake values as shown in Tables 1 and 2 with the exception for arsenic, iodine, mercury, and cadmium.
4. Discussion It was interesting to note that mercury, copper and uranium were all below the detection limit in most of the locally grown seaweed samples. The lowest and highest levels of lead were also found in locally grown seaweed. Three out of six samples were below the detection limit indicating that lead is not an ubiquitous contaminant. The measurable levels of lead in the other three samples might very well be a reflection of a point source. Many point sources of lead can be expected as lead weights currently are, and have been for many years, used in the fishing industry in the region where these samples were harvested. The same argument could be made for the variation in zinc content which was double to triple in some of the local samples and even higher in two out of seven Japanese samples. Zinc is a known constituent in marine craft as anodic protection
173
against corrosion of brass components that are exposed to seawater. It could be argued that winged, giant, and bull kelp appear to have a special affinity for lead and perhaps some of the other elements. Although the other bull kelp sample showed a low lead content, but a much higher cadmium content, this could be due to variations in the presence of lead and cadmium. Another possibility that could explain the different uptake in kelp grown in the same environment would be the time of harvesting. It has been shown in wakame ŽIto and Miyosshi, 1990. for instance, that certain elements such as zinc appear to be taken up at different rates at different stages of growth. Local variation in salinity has also been shown to be an important factor in the biological uptake of a number of elements ŽCho et al., 1995; Struck et al., 1997.. Seaweed has long been regarded as an excellent source of iodine. The iodine content in a number of commercially available seaweeds in Britain, reported by Lee et al. Ž1994., are very similar to those observed in our analysis and compare as follows Žin mgrg dry wt..: wakame 104 vs. 102, arame 706 vs. 600, hijiki 319 vs. 436, nori 4.3 vs. 16.9, and kombu Ž L. japonica. 2660 vs. 2110. In this study, there appeared to be insufficient man-made radionuclides in the water or they are not being accumulated to produce concentrations in the algae that are of health significance. All samples were less than the drinking water guidelines and edible algae would not be nearly as significant a pathway for uptake as drinking water. The Canadian guidelines for radionuclides in drinking water are: iodine-131, 6 Bqrkg; cesium-137, 10 Bqrkg; and radium-226, 0.6 Bqrkg. There are no guidelines for potassium-40 as it just reflects the potassium content. There are no guidelines for tin-125. Iodine-131, cesium-137, tin-125 are the primary gamma-emitting radionuclides, residual from both nuclear bomb and nuclear power releases. In the event of a nuclear release cesium-137 and iodine-131 are considered more significant ŽUNCEIAR, 1988.. The traces of cesium]137 that were found in two samples could be a reflection of past nuclear accidents such as
174
C. ¨ an Netten et al. r The Science of the Total En¨ ironment 255 (2000) 169]175
Chernobyl ŽUNCEIAR, 1988; Druehl et al., 1988.. Iodine-131 is also used in medical procedures and thereby finds its way into the environment ŽWaller and Cole, 1999.. Radium-226 is a key decay product from the most abundant natural uranium decay series. It is found in seawater in concentrations ranging from 0.74 to 3.7 Bqrl ŽIAEA, 1990.. There was not sufficient material to reduce the detection limits for radium-226 to meaningful health values. It might be useful in the future to repeat using larger samples or a chemical analysis method. Some radium-226 may be concentrated in the algae from the seawater. Potassium-40 is found in a fixed ratio to non-radioactive potassium and, therefore, reflects the potassium content of the algae. The content in the soil is approximately 400 Bqrkg ŽAECB, 1995. and the average potassium-40 content of seawater is 12 Bqrl. Although the potassium-40 concentrations in the different algae varied widely these levels are considered to be of no health consequence because of the low activity associated with this isotope. Speciation and bioavalability of the various elements dealt with in this communication have not been addressed and needs to be assessed if one wants an accurate measure of the biological effects associated with intake of these seaweed products. This is particularly important for elements such as arsenic and chromium. It has been shown that arsenic III is taken up at a different rate than arsenic V ŽBertolero et al., 1987.. Similarly certain organic arsenic compounds such as the arseno betaines, commonly found in seafood, are not taken up and are therefore, not bioavailable ŽVahter et al., 1983.. These observations should be kept in mind when comparing the arsenic values in Table 1, which range from 71 to 88 mgrg, to the maximum allowable content ŽMAC. in drinking water ŽHealth Canada, 1996. for arsenic Ž0.025 mgrl., assuming an average daily consumption of 1.5 l per person. These principles do not apply to the mercury content measured in these samples and 1.5 kelp tablets from sample a9 has the equivalent mercury content of 1000 l of drinking water containing the MAC of 0.001 mgrl. Whether this mercury is in the organic form is also not known from this research but is,
in contrast to arsenic, extremely important as this form of mercury is more toxic than the inorganic form. It should also be pointed out that the results presented here are based on randomly selected single samples, and are not necessarily representative of the algal products that are currently available.
5. Conclusions Locally derived edible algae samples were generally much lower in their heavy metal content specifically mercury. The mercury content of some samples could prove to be a significant source of mercury exposure. Speciation and bioavailability of arsenic needs to be determined to assess the exposure to this metal. The iodine content of algae was found to vary widely with the highest concentrations in wakame from Japan. Some samples showed traces of cesium-137 and radium226. The former is likely related to the Chernobyl accident whereas the latter could be a reflection of naturally occurring uranium decay. References Atomic Energy Control Board ŽAECB.. Canada: living with radiation. 1995, p. 9. Beres A, Wasserman O, Bruhn T et al. A new procedure for the isolation of anti-HIV compounds Žpolysaccharides and polyphenols. from the marine alga Fucus ¨ esiculosus. J Nat Prod 1993;56:478]488. Bertolero F, Pozzi G, Sabbioni E, Saffiotti U. Cellular uptake and metabolic reduction of pentavalent to trivalent arsenic as determinants of cytotoxicity and morphological transformation. Carcinogenesis 1987;8:803. Bryan GW, Hummerstone LG. Brown seaweed is an indicator of heavy metals in estuaries in south-west England. J Mar Biol Assoc UK 1973;53:705]720. Cho DM, Kim DS, Lee DS, Kim HR, Pyeun JH. Trace components and functional saccharides in seaweed. 1: changes in proximate composition and trace elements according to harvest season and places. Bull Korean Fish Soc 1995;28:49]59. Darcy-Vrillon B. Nutritional aspects of the developing use of marine macroalgae for the human food industry. Int J Food Sci Nutr 1993;44:S23]S35. Dickson D. Radioactive seaweed stirs UK low-level waste fight. Science 1984;223:35.
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