Bioavailability and speciation of arsenic in carrots grown in contaminated soil
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1 Analyst, May 1998, Vol. 123 ( ) 791 Bioavailability and speciation of arsenic in carrots grown in contaminated soil Hans Helgesen a and Erik H. Larsen *b a Department of Chemistry, Technical University of Denmark, Building 207, DK-2800 Lyngby, Denmark b Danish Veterinary and Food Administration, Institute of Food Research and Nutrition, 19 Mørkhøj Bygade, DK-2860 Søborg, Denmark, ehl@vfd.dk Carrots were grown in seven experimental plots (A G) containing mixtures of arsenic-contaminated and uncontaminated soil at concentrations ranging from 6.5 to 917 mg g 21 (dry mass). The carrots harvested from plots A D ( mg g 21 arsenic in the soil mixtures) showed a gradually increasing depression of growth with increasing level of contamination. At the experimental plots E G with soil arsenic concentrations above 400 mgg 21 no carrots developed. Whether this effect was caused by arsenic or the concomitant copper content which ranged from 11 to 810 mg g 21 in the soil mixtures is unknown. The arsenic species extracted from the soils and carrots were separated and detected using anion-exchange HPLC coupled with ICP-MS. In the less contaminated soils from plots A and B arsenite (As III ) was more abundant than arsenate (As V ) in the soil using 1 mmole l 21 calcium nitrate as extractant. In the soils from plots C and D however, As V dominated over As III whereas in the corresponding carrots As V and As III were found at similar concentrations. Methylated arsenic species were sought after but not detected in any of the samples. The soil-to-carrot uptake rate (bioavailability) of arsenic was 0.47 ± 0.06% (average ± one standard deviation) of the arsenic content in the soils from plots A D. In contrast to arsenic, the increasing copper content in the soils from plot A through D was not available to the carrots as the concentration of this element did not increase with increasing soil copper content. The ingestion of the potentially toxic inorganic arsenic via consumption of carrots grown in soil contaminated at 30 mg g 21 in arsenic (plot B) was conservatively estimated at 37 mg week 21. This was equivalent to only 4% of the provisional tolerable weekly intake (PTWI) for inorganic arsenic as suggested by the WHO and was therefore toxicologically safe. Consumption of carrots grown in more intensely arsenic-contaminated soils, however, would lead to a higher intake of inorganic arsenic and is therefore not recommended. Keywords: Arsenic speciation; carrots; plant uptake; soil contamination; high-performance liquid chromatography inductively coupled plasma mass spectrometry Arsenic is a toxic element to humans and numerous studies have been conducted in order to assess the amount and chemical forms (species) of arsenic present in food and biological samples. The data generated have been used for evaluating whether ingestion of arsenic via consumption of food posed any health risk to humans. 1 Presented at The Third International Symposium on Speciation of Elements in Toxicology and in Environmental and Biological Sciences, Port Douglas, Australia, September 15 19, In nature, arsenic readily undergoes metabolic conversions mediated by microorganisms, plants and animals. 2 This explains the finding in food of a range of arsenic species which possess different toxicity to humans. Modern sensitive and selective analytical techniques such as high-performance liquid chromatography (HPLC) coupled on-line with inductively coupled plasma mass spectrometry (ICP-MS) have made possible the separation and selective detection of arsenic species in food and environmental samples at their naturally occurring concentration levels. 3 The concentration of arsenic in the terrestrial environment, including crop plants for human consumption, is generally low. 4 In contrast, food items of marine origin contain arsenic at much higher concentrations, primarily as the non-toxic species arsenobetaine, 5 whereas the toxic inorganic arsenic is present in seafood usually at a few per cent of the total arsenic content. 6 Studies of the environmental contamination following industrial wood preservation have shown highly elevated concentrations of arsenic and copper in the environment near the source of contamination. These elements were detected in locally grown crop plants and in soil following atmospheric deposition. 7 Furthermore, arsenic as arsenite (As III ) and arsenate (As V ) were detected at several hundred micrograms per litre in the ground water 8 sampled under the contaminated top soil. In order to evaluate the possible health risk to humans consuming crops cultivated in the contaminated soil, information is needed regarding the soil-to-plant uptake rate (bioavailability) of arsenic and speciation of the toxic element species in the crop plants. The bioavailability to crop plants of arsenic depends on several physical and chemical factors in the soil. The texture and chemical composition of the soil are important factors that govern the availability of arsenic to plants. Iron and aluminium oxides adsorb anionic arsenic species well in acidic soils, whereas calcium oxides in alkaline soils to a lesser extent adsorb anionic arsenic species. 9,10 Anionic arsenic species are therefore in general more available to crops grown in alkaline than in acidic soil. 11 Soil with a sandy texture is normally low in content of minerals and organic constituents which are capable of binding anionic arsenic species, and therefore a relatively high mobility of arsenic into the soil pore water may be observed. 12 Phosphate in soil may compete with arsenate in its uptake by plants owing to the chemical similarities of the two anions. Thus, a low content of phosphate in soils may result in a high uptake of arsenate. 13 Finally, the uptake of arsenic from soil to plant varies between plant species. In extreme cases this has led to an arsenic concentration in the edible mushroom species Laccaria amethystina sampled from arseniccontaminated soil 14 at more than 1000 mg g 21. In this case the arsenic was present in the mushroom as the low-toxic dimethylarsinic acid. In order to assess experimentally the bioavailability of arsenic from a contaminated soil to a crop plant, the selection of an extraction medium which simulates the plant-available fraction of the element is of importance. Extractants such as 0.1
2 792 Analyst, May 1998, Vol. 123 mol l 21 ammonium nitrate or ammonium acetate or calcium nitrate and water have been used for this purpose However, in general the concentrations of the buffers used were higher than the natural ion strength of the interstitial water in soil. There is therefore a risk of overestimating the plantavailable amount of arsenic due to an unrealistically high desorption efficiency. The aim of this study was to investigate the uptake of total arsenic, arsenic species and copper by carrots cultivated in soils at different levels of contamination by these elements. Furthermore, the possible implications to human health associated with consumption of the contaminated carrots were considered. Carrot (Daucus carota) was selected as the test crop owing to its high tolerance to water soluble arsenic 19 and because it is a commonly consumed vegetable. Design and conduction of field experiments The soil at a former industrial wood preservation site, located near Hillerød, Denmark, was contaminated by arsenic and copper because of spills that had occurred during impregnation of the wood by a mixture of arsenic pentaoxide, copper(ii) oxide and chromium trioxide. 7 The arsenic content in the soil varied from 500 to 2000 mg g 21 at particularly contaminated hot spots according to a characterisation carried out by Frederiksborg County Environmental Administration. In order to establish a field experiment, soil was sampled from such a contaminated hot spot and from an uncontaminated site nearby. The two soils were mixed using a cement mixer at a variety of ratios and included an uncontaminated soil (experimental plot A) and soils contaminated at gradually increasing levels of arsenic and copper (experimental plots B G). The contaminated soil was a loamy sand type which was low in content of organic matter, 18 whereas the uncontaminated soil was a loamy sand type rich in organic matter. Consequently, the mixtures of the two soils were loamy sand types rich in organic matter and loose in structure at plots A D whereas the soils at plots E G were denser owing to an increasingly higher fraction of the contaminated soil. The soil mixtures were filled into poly(vinyl chloride) (PVC) cylinders of m id, which were placed vertically in holes dug in the ground at the uncontaminated site where the field experiment was conducted. The rim of the cylinders reached 10 cm above the surrounding uncontaminated soil. A perforated PVC pipe of m id was placed in the soil at each experimental plot to facilitate drainage of water. Seeds of carrot (Daucus carota) were sown in the experimental soils. During growth, the experimental plots were sufficiently irrigated but neither fertilisers nor pesticides were used. After 17 weeks of growth the crops from experimental plots A D were harvested whereas no carrots were obtained from plots E G owing to strongly impaired growth or failure of the crops. The green tops of the carrots including 1 2 cm of the root were removed. The roots were rinsed thoroughly to remove all visible soil particles in order to prevent soil contamination. The carrots were separated into peel and core, and the samples were shredded and freeze-dried. The dried carrot samples were homogenised in a mortar to pass a 0.5 mm mesh sieve, and were stored dry in a desiccator until the time of chemical analysis. A representative soil sample (2 l volume) was taken from each experimental plot by mixing sub-samples taken by a soil drill. The soil samples were oven-dried at 60 C for 3 d followed by passage through a 0.5 mm mesh sieve. Chemical analysis of arsenic and copper in carrots and soil A sub-sample of carrot (0.5 g dry mass) was wet ashed using 4 ml of sub-boiling distilled nitric acid in a DAE II Teflon-lined pressure steel bomb (Berghof, Tübingen, Germany) at 160 C for 4 h. After cooling, the residue was diluted to 20 ml with water produced in a Super-Q apparatus (Millipore, Milford, MA, USA) prior to arsenic and copper determination as described in more detail elsewhere. 20 A sub-sample of soil (1.0 g dry mass) was mineralised following a standard method of analysis 21 in a 50 ml pressureresistant flask, and 20 ml of a mixture of nitric acid and water (1 + 1 v/v) was added. The Teflon-lined lid of the flask was tightened and the flask was placed in an autoclave for 1 h at 125 C. After cooling, the acid soil mixture was diluted to 100 ml with water. The total arsenic and copper contents of the diluted acidic residues of the carrot and soil samples were determined by Zeeman-effect electrothermal atomic absorption spectrometry, using atomisation from a graphite platform in pyrolytic graphite-coated graphite tubes (Zeeman 3030, Perkin-Elmer, Norwalk, CT, USA). The temperature and time programming and other settings used are given in Table 1. Quantification was based on peak area measurements using the method of standard additions for calibration as described in detail elsewhere. 20,22 The total arsenic and copper contents determined in the soils and in the carrots are given in Tables 2 and 3. Extraction of arsenic species from soils and carrots The dried soil sample (5.0 g) was transferred into a 50 ml Erlenmeyer flask and 25 ml of a 1 mmol l 21 calcium nitrate solution were added. The extraction of arsenic proceeded for 1 h with gentle mechanical shaking at room temperature. The supernatant was separated from the soil solids by centrifugation prior to injection into the HPLC ICP-MS system for arsenic speciation determination. The arsenic contained in the dried carrot sample (100 mg) was extracted for speciation determination in 5.00 ml of methanol water (1 + 9 v/v) using a microwave-assisted technique. The mixture, which was filled into a capped 10 ml centrifuge tube, was positioned in the focused microwave field of the microwave apparatus (Maxidigest MX 350, Prolabo, Paris, France). Prior to applying the microwave energy, 100 ml of cold water (ballast water) which surrounded the capped centrifuge tube holding the sample were added. Part of the microwave energy was absorbed by the ballast water, thus protecting the sample from overheating. In order to optimise the extraction efficiency, the microwave apparatus was operated at a range of power and time combinations. The optimum extraction efficiency was achieved using four treatments at 75 W power (25% of total power) for 8 min each, as shown in Fig. Table 1 Instrumental settings for Zeeman-effect atomic absorption spectrometric analyses Element Parameter Dry Dry Ash Atomise Clean Graphite furnace Arsenic Temperature/ C Ramp/hold time/s 5/20 5/50 20/30 0/5 1/3 Copper Temperature/ C Ramp/hold time/s 5/20 10/40 20/30 0/5 1/5 Ar flow rate/ml min Spectrometer Sample volume 20 ml Chemical modifier 10 ml of a mixture containing 1000 mg l 21 palladium and 2000 mg l 21 magnesium nitrate was used for the arsenic determinations Resonance wavelength nm (arsenic) and nm, (copper) Spectral bandpass 0.7 mm
3 Analyst, May 1998, Vol After each of the treatments the sample tube was cooled under running tap water and the ballast water was renewed. The clear supernatant was injected into the HPLC ICP-MS system without any further sample pre-treatment. Arsenic speciation by HPLC ICP-MS The use of HPLC for the separation and ICP-MS for the selective detection of arsenic for speciation studies in biological samples has been extensively described elsewhere. 8,20,23 In summary, the anionic arsenic species in the sample extracts were separated using an ION 120 organic polymeric strong anion-exchange HPLC column (Interaction Chromatography, San Jose, CA, USA), which was eluted isocratically at 1 ml min 21 with 45 mmol l 21 ammonium carbonate solution in water methanol (97 + 3) at ph 10.3 as the mobile phase. The eluate from the HPLC system was continuously introduced into the ICP-MS instrument (Elan 5000, Perkin-Elmer SCIEX, Thornhill, ON, Canada), which was adjusted to monitor the 75As signal intensity at m/z 75 versus time. Aqueous mixtures of As III, As V, monomethylarsonate (MMA) and dimethylarsinate (DMA) were injected into the anion-exchange HPLC ICP-MS system and their retention times (t r ) were recorded. In this way the chromatographic peaks emerging after the injection of the sample extracts were identified by their retention times as indicated in Fig. 2. The intensity of each chromatographic peak was quantified against corresponding calibration curves constructed by injection of standard mixtures of known concentrations into the HPLC ICP-MS system. Results and discussion Arsenic and copper in soils and carrots A pronounced depression of the growth of the carrots was observed with increasing contamination of the soils of the experimental plots, shown by a decrease in the height of the carrot tops at experimental plots A D. Furthermore, at plots C and D the carrot tops were wilted and partly yellow. The depression of growth was further illustrated by the average lengths of the harvested carrots, which were approximately 12, 10, 8 and 5 cm at plots A, B, C and D, respectively. No crop was obtained from experimental plots E G, at which the soil arsenic concentrations (average ± one standard deviation of duplicate determinations) were 406 ± 30, 679 ± 95 and 917 ± 59 mg g 21, respectively. The observed failure of the crops may have been caused by a phytotoxic effect of arsenic 19 or by copper. The arsenic and copper contents in the soil at experimental plot A (Table 2) were similar to those found in uncontaminated Danish soils. 24 Therefore, this plot was well suited as a reference for the results obtained from the contaminated experimental plots B D. The results in Tables 2 and 3 show that the concentration of arsenic in carrots increased with increasing arsenic concentrations in the soils. Furthermore, the data in Table 3 show that the arsenic concentration in the peels was Table 2 Arsenic, arsenic species and copper in experimental soils * Extractable arsenic Extraction plot Total As As III As V efficiency (%) Total Cu ph A 6.5 ± ± B 30.0 ± ± C 93.3 ± ± D 338 ± ± Danish monitoring Median values 95th percentile * All concentration values are given in mg As g 21 (dry mass). Values given as mean ± one standard deviation of duplicate determinations. Determined electrometrically after extraction using 0.01 mol l 21 of calcium chloride in water. Data from Jensen et al. 24. Table 3 Arsenic, arsenic species and copper in carrots grown in experimental soils * Extractable arsenic Extraction plot Sub-sample Total As As III As V efficiency (%) Total Cu A Core < < < n.d 4.27 ± 0.21 Peel < < < n.d 7.64 ± 0.38 B Core ± ± < n.d 2.93 ± 0.15 Peel ± ± < n.d 7.60 ± 0.38 C Core ± ± ± ± ± 0.17 Peel 1.04 ± ± ± ± ± 0.16 D Whole 1.85 ± ± ± ± ± 0.26 Danish monitoring Median < values 90th percentile < * All concentration values are given as mean ± one standard deviation of duplicate determinations in mg As g 21 (dry mass). Corresponds to whole carrots. Data from National Food Agency of Denmark. Data from Hansen and Andersen. 25
4 794 Analyst, May 1998, Vol. 123 higher than that in the core of the carrots by a factor of approximately three. In addition to arsenic, the soils were also contaminated with copper, as shown by the results in Table 2. The contents of copper in the corresponding carrots in Table 3 show that the concentration of this element did not change with a 23-fold increase in soil copper concentration from plot A to plot D. The copper content in the carrots from all experimental plots was within the normal range for uncontaminated carrots available on the Danish market, 25 as indicated in Table 3. Hence, the high concentration level of copper in the contaminated soils was not bioavailable to the carrots, and further chemical investigations were therefore not considered. Selection and optimisation of extraction methods for arsenic species in soils and carrots Procedures reported in the literature for extraction of arsenic from soil 15,16,18 often make use of physico-chemical conditions (ph, ionic strength) that deviate from those existing in natural soils. Thereby, there is a risk of over-estimating the fraction of Fig. 1 Extraction efficiency of arsenic from carrot against number of repeated microwave-assisted extraction treatments applied. See for details. arsenic which is soluble and available to the plant. Therefore, the requirements laid down in this study were that the extractant should approximate the ion strength and ph value of the interstitial water in the soils studied. To meet these requirements, an aqueous solution of calcium nitrate was used 18 at a concentration of 1 mmol l 21, which approximated the natural conditions in typical Danish soils. 24 Furthermore, this extractant did not possess any redox or acid base properties per se, which was of importance for the conservation of the original abundance of the As III As V redox pair during the extraction process. Furthermore, the extraction had to be carried out using a minimum of physical agitation to prevent the introduction of unrealistically high extraction forces to the system. Otherwise there was a risk of over-estimating the plant-available fraction of arsenic in the soils. The results in Table 2 show that the extractable arsenic in the soil was % of the total arsenic as estimated by leaching with hot nitric acid. The selection and optimisation of the extraction procedure of arsenic species from the carrots were aimed at obtaining a high extraction efficiency and at the same time conserving the arsenic species contained in the plant material. The application of continuous low-power microwave energy is advantageous for this purpose because the technique makes short extraction times possible with a reproducible and adjustable input of energy. 26 Water was chosen as extractant and methanol (10% v/ v) was added to eliminate the risk of microbial growth. The microwave-assisted extraction gave an extraction efficiency of arsenic of 69%, as shown in Fig. 1. With these experimental conditions the temperature of the extracts did not exceed 70 C. The conservation of the arsenic analytes was confirmed by the recovery of arsenic as As III spiked at 22 or 110 ng and as As V spiked at 39 or 197 ng to separate sub-samples of the dry carrot material from plot A. The chromatographed extracts showed that no conversions of the two spiked arsenic species had occurred. Arsenic speciation in soils and carrots The speciation results in Table 2 show that As III and As V were present in all soils. In the soils from plots C and D, As V was present at a higher concentration than As III, whereas at plots A and B As III dominated. Historically, the arsenicals used for the industrial wood preservation process were predominantly the pentavalent sodium arsenate(v) and arsenic(v) oxide. 18 The results obtained therefore indicate that a partial reduction to the trivalent form had occurred, possibly facilitated by the physicochemical or microbial conditions in the soil. The soil samples from plots A and B additionally contained a trace of the cationic arsenical trimethylarsine oxide (TMAO), which was detected in the extracts by cation-exchange HPLC ICP-MS. 20 Microbial activity may explain the finding of TMAO in these two soil samples. 2 The uptake of the hydrogenarsenate ion by the carrot is assumed to follow the same route as the chemically similar hydrogenphosphate ion, 12 whereas the uptake by carrots of As III, which is not ionised at the ph value of the soil, is unlikely. The results in Table 3, however, show that there are about equal concentrations of arsenic as As III and As V in the carrot samples. These results suggest that following uptake by the carrot, As V has been partially reduced to As III by bacteria associated with the root hairs or by the carrot itself. No methylated arsenic species were found in the carrots. Fig. 2 Anion-exchange HPLC ICP-MS of A, an extract of carrot from experimental plot D and B, a mixture of four anionic arsenic species at DMA 8.6, As III 11.9, MMA 8.7 and As V 21.3 ng As ml 21. Volume injected, 100 ml. See section for details. Bioavailability of arsenic from soils to carrots The results in Table 4 show that the availability of arsenic to carrots (whole) from plots A D is 0.47 ± 0.06% (RSD 13%) of
5 Analyst, May 1998, Vol Table 4 Bioavailability of arsenic in carrots Ratio of concentrations of arsenic Ratio of concentrations of arsenic in carrot in carrot to arsenic in soil (%) to arsenic in soil extracts * (%) plot Core Peel Whole Core Peel Whole A n.d. n.d n.d. n.d. n.d B C D Mean ± SD 0.39 ± ± ± ± ± ± 150 * Data for extraction efficiency from Table 2. Estimated from Danish monitoring data. 4,25 Weighed average based on a 10 : 1 mass ratio of core and peel, respectively. the arsenic concentration in the corresponding soils. The bioavailability of arsenic to the carrots expressed relative to the extractable arsenic in the corresponding soils is 580 ± 150% (RSD 25%). The higher RSD value of the latter estimate of the bioavailability is partly due to the inclusion of the extraction efficiency in these calculations, which contributes to the overall uncertainty. The former method of estimation of bioavailability is more practical because it only involves the relatively straightforward determination of total arsenic. For the discussion of the impact of ingested arsenic on human health, however, the speciation data in Table 3 are of great importance. Human health risk considerations Inorganic arsenic has been recognised as a human carcinogen which may cause skin or lung cancer. 27 The fact that arsenic in the carrots is present as the toxic arsenic species calls for an evaluation of the safe use of arsenic-contaminated carrots for human consumption. A provisional tolerable weekly intake (PTWI) for inorganic arsenic has been established as 15 mg kg 21 body mass from all food sources including water. There is only a small margin between the PTWI value and the adverse effects observed in epidemiological studies. 28 This intake value should therefore not be exceeded. The arsenic concentration in the soil at experimental plot B (30 mg g 21 ) is close in value to the soil quality criterion for total arsenic set by the Danish Environmental Protection Agency (EPA) 24 at 20 mg g 21. Soils contaminated by arsenic above this concentration level are not recommended for sensitive use such as cultivation of vegetables for human consumption. The results in Table 3 show that the carrots harvested from the same experimental plot B contain arsenic at 0.12 mg g 21 (weighed average of core and peel) or mg g 21 on a fresh mass basis. Furthermore, the speciation results in Table 2 show that the arsenic in the carrots is present as inorganic species. A recently conducted food intake study 29 showed that the adult Danes consume (90th percentile) up to 376 g (fresh mass) of vegetables per day. Assuming conservatively that this vegetable consumption rate is represented solely by carrots with an arsenic content equal to that found in carrots harvested from experimental plot B, the intake of inorganic arsenic amounts to 37 mg week 21 or 4% of the PTWI value. A fraction of the arsenic content, however, remained unaccounted for with respect to its speciation because of the incomplete extraction efficiency as indicated in Table 3. Assuming that all arsenic in the carrot is present as inorganic species, the estimated intake is sufficiently low to allow for a contribution by inorganic arsenic from other food sources and water 1,4 without any risk of exceeding the PTWI value for inorganic arsenic. It is therefore concluded that the 20 mg g 21 soil quality criterion for arsenic established by the Danish EPA is sufficiently safe to prevent any unacceptable intake of inorganic arsenic via consumption of carrots. We thank Senior Advisor Poul Aaboe Rasmussen of the Frederiksborg County Environmental Administration for supporting the planning and implementation of the field experiments, and Professor Elo H. Hansen of the Technical University of Denmark for academic supervision (H.H.) and for the use of laboratory facilities. References 1 Larsen, E. H., PhD Thesis, National Food Agency of Denmark, Søborg, Cullen, W. R., and Reimer, K. J., Chem. Rev., 1988, 89, Larsen, E. H., Fresenius J. Anal. Chem., 1995, 352, Food Monitoring in Denmark, Nutrients and Contaminants , Publication No. 195, National Food Agency of Denmark, Søborg, Francesconi, K. A., and Edmonds, J. S., Oceanogr. Mar. Biol. Annu. Rev., 1993, 31, Edmonds, J. S., and Francesconi, K. A., Mar. Pollut. Bull., 1993, 26, Larsen, E. H., Moseholm, L., and Møller, M. M., Sci. Total Environ., 1992, 126, Larsen, E. H., Spectrochim. Acta, Part B., in the press. 9 Woolson, E. A., Axley, J. H., and Kearney, P. C., Soil Sci. Soc. Am. Proc., 1971, 35, Wauchope, R. D., and McDowell, L. L., J. Environ. Qual., 1984, 13, Frost, R. R., and Griffin, R. A., Soil. Sci. Soc. Am. J., 1977, 41, Atkins, M. B., and Lewis, R. J., Soil Sci. Soc. Am. Proc., 1976, 40, Woolson, E. A., Axley, J. H., and Kearney, P. C., Soil Sci. Soc. Am. Proc., 1973, 37, Larsen, E. H., Hansen, M., and Gössler, W., Appl. Organomet. Chem., in the press. 15 Harper, M., and Haswell, S. J., Environ. Technol. Lett., 1988, 9, Räisänen, M. L., Hämäläinen, L., and Westerberg, L. M., Analyst, 1992, 117, Hlavay, J., Polyak, K., Bodog, K., and Csok, Z., Microchem. J., 1995, 51, Ottosen, L. M., PhD Thesis, Technical University of Denmark, Lyngby, Grant, C., and Dobbs, J., Environ. Pollut., 1977, 14, Larsen, E. H., Pritzl, G., and Hansen, S. H., J. Anal. At. Spectrom., 1993, 8, Danish Standard 259, DS Handbook 21.1., 1st edn., Dansk Standardiseringsråd, Copenhagen, Larsen, E. H., J. Anal. At. Spectrom., 1991, 6, Larsen, E. H., and Stürup, S., J. Anal. At. Spectrom., 1994, 9, Jensen, J., Bak, J., and Larsen, M. M., Heavy Metals in Danish Soils, Report 1996/4, National Environmental Research Institute, Roskilde, Hansen, H. H., and Andersen, A., Lead, Cadmium, Copper and Zinc in Fruit and Vegetables , Publication No. 84, National Food Agency of Denmark, Søborg, 1983.
6 796 Analyst, May 1998, Vol Szpunar, J., Schmitt, V. O., Donard, O. F. X., and Lobinski, R., Trends Anal. Chem., 1996, 15, International Agency for Research on Cancer, IARC Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Humans Some Metals and Metallic Compounds, Vol. 23, IARC, Lyon, World Health Organization, Toxicological Evaluation of Certain Food Additives and Contaminants, Food Additives Series, No. 24, WHO, Geneva, National Food Agency of Denmark, Danskernes Kostvaner 1995, Hovedresultater, Publication No. 235, National Food Agency of Denmark, Søborg, 1996 (in Danish with summary in English). Paper 7/08056E Received November 10, 1977 Accepted February 27, 1998
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