Bioaccessibility of Uranium in Soil Samples from Port Hope, Ontario

Aug 1, 2012 - We postulate that the most important reason for variability of measured bioaccessibility values in Port. Hope soil samples may be the di...
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Bioaccessibility of Uranium in Soil Samples from Port Hope, Ontario, Canada Slobodan V. Jovanovic,* Pujing Pan, and Larry Wong Canadian Nuclear Safety Commission Laboratory, 3484 Limebank Road, Ottawa, Ontario, Canada K1V 1E1 S Supporting Information *

ABSTRACT: Adequate assessment of human health risk of uranium contamination at hazardous waste sites, which is an important step in determining the cleanup strategy, is based on bioavailability data. Bioavailability of uranium from contaminated soil has not been properly determined yet. Bioaccessibility is an in vitro conservative estimate of bioavailability and is thus frequently used for site-specific risk assessment. Bioaccessibility of uranium was measured in 33 soil samples from the Port Hope area in Ontario, Canada, by the physiologically based extraction test (PBET). Higher bioaccessibility values in the gastric plus intestinal phase, 48.4% ± 16.8%, than in the gastric phase, 20.8% ± 11.7%, are very probably the result of more efficient extraction of uranium from soil by intestinal fluid rich in carbonate ions. The observed variability of measured bioaccessibility values is discussed in light of the results of scanning electron microscope examination of the soil samples. Uranium bioaccessibility values in both gastric (acidic) and gastric plus intestinal (neutral) phases are higher in soil samples with smaller uranium-bearing particles and lower in samples where the uraniumbearing particles are larger. We postulate that the most important reason for variability of measured bioaccessibility values in Port Hope soil samples may be the difference in particle size of uranium-bearing particles.

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contaminated soils4−6 by plants, worms, and microorganisms is low (a few percent of the available uranium). The uptake of highly water-soluble uranium hexafluoride, uranyl carbonate complexes, and uranyl nitrates is higher than that of practically insoluble uranium oxides as well as uranyl humic and fulvic acid complexes.3,8,9 Absolute bioavailability of uranium and its isotopes has been extensively studied.10−14 In general, the absolute bioavailability of ingested uranium measured in laboratory animals is low (up to a few percent of soluble uranium),10,13,14 which is consistent with the fractional gastrointestinal absorption factor of 0.02 proposed by the International Commission on Radiation Protection (ICRP) for internal dose calculation.15 It is influenced by (1) speciation of uranium, that is, less watersoluble uranium(IV) being considerably less toxic than more soluble uranium(VI) compounds;10 (2) presence of reducing or oxidizing agents, in particular iron compounds, which may reduce uranium(VI) compounds to uranium(IV), thus making U less bioavailable;14 and (3) whether the animals fasted before the introduction of uranium, which results in higher uranium uptake.13 Relative bioavailability of uranium in humans or in suitable animal models, which may be useful for environmental risk

INTRODUCTION Uranium is one of the heaviest naturally occurring elements on earth, with an average concentration of 2.8 mg/kg in the soil.1 It is a radioactive element, with three long-lived isotopes, U-238 (99.2745%), U-235 (0.720%), and U-234 (0.0055%). In contaminated soil, uranium is found both as a mixture of its naturally occurring isotopes and as a depleted (usually devoid of U-235 and U-234 isotopes and sometimes containing synthetic U-236) or enriched uranium (higher than natural concentration of U-235). Uranium is a ubiquitous contaminant in soils of communities neighboring uranium mining and processing facilities. The concentrations of uranium in the contaminated soil vary at different locations around the world, from tens to thousands of milligrams per kilogram. The main pathway of exposure of general population to uranium is from ingestion of food and water.2 The toxicity of uranium in humans can be high when in soluble form (for example, minimal risk level for highly soluble uranium compounds taken orally is set at 2 μg·kg−1·day−1),2 the chemical toxicity to kidneys being more of a concern than radiotoxicity to bones. Chemical toxicity does not depend on the isotopic composition of uranium; that is, all isotopes of uranium have similar chemical toxicity. The uptake of uranium by plants, worms, and microorganisms3−9 has been studied in order to assess the probability of its biogenic removal from the environment as well as to establish toxicity data and the influence of various other constituents on its uptake. Overall uptake of uranium from © 2012 American Chemical Society

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assessment, has not been extensively studied.2 To quote a recent Agency for Toxic Substances and Disease Registry document:2 “Information is needed on the comparative absorption of uranium compounds by the oral route, along with an assessment of its clearance from the skeleton. Quantitative data on the bioavailability of uranium from contaminated soil by the oral and dermal routes are also necessary to assess the risk of uranium-contaminated soil at hazardous waste sites.” The current Canadian environmental guideline for the level of uranium in soil is 23 mg/kg.16 This uranium guideline is based on the ecological risk model, which conservatively assumes the bioavailability of uranium from soil as 100%. In vitro determinations of the gastrointestinal (GI) fluids extractable fraction, termed bioaccessible fraction, which are easier to perform than in vivo bioavailability measurements, may be used as a conservative estimate of relative bioavailability.17 The rationale is that the bioaccessible fraction, which represents the proportion of contaminant soluble in the GI fluid, should be higher than or equal to the fraction transferred into the systemic circulation (bioavailable fraction). For example, bioaccessibility of lead from contaminated soil has been validated by use of the bioavailability data.18 In vitro bioaccessibility (IVBA) may routinely be used to predict sitespecific relative bioavailability (RBA) of lead from contaminated soil.18 The RBA is related to the IVBA by the equation RBA = 0.878IVBA − 0.028

levels of disturbance, thus containing little, if any, naturally occurring uranium minerals. To better understand the factors governing bioaccessibility of uranium in contaminated soils, we used the physiologically based extraction test (PBET)17,24 to determine the bioaccessibility of uranium in 33 Port Hope soil samples. The samples originate from six residential properties, two publicly accessible sites, and the remediated soil storage site.

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MATERIALS AND METHODS All chemicals used in this study were of high purity, suitable for trace metal analyses. HCl and HNO3 were Optima grade by Fisher. Lactic and acetic acid, pepsin, sodium citrate, and sodium carbonate (HPLC-grade) were also obtained from Fisher. Bile salts were from Fluka. Pancreatin from bovine pancreas was from Sigma, and DL-malic acid disodium salt from Aldrich. The inductively coupled plasma mass spectrometry (ICP-MS) standards, multielement solutions 1 and 2, multielement internal standard 1, instrument calibration standard 1, and tuning solution were obtained from Spex CertiPrep. All those standards are traceable to National Institute of Standards and Technology (NIST). For preparation of aqueous solutions, we used high-purity Millipore Milli-Q water, with resistivity better than 18.2 MΩ/cm. Uranium standard reference materials (SRMs) used in this study were obtained from the Canada Centre for Mineral and Energy Technology (CANMET).27 Standard reference material “Montana I Soil”, NIST 2710a, was obtained from the National Institute of Standards and Technology.28 Soil Sample Preparation and Analysis. A total of 56 Port Hope soil samples, deemed to be representative of various soil types in the Port Hope area, were first analyzed by the analytical sieve shaker (Retsch) to determine the particle size distribution. The fraction containing particle sizes smaller than 250 μm was used for the characterization of soil samples by scanning electron microscopy (SEM) and X-ray microanalysis (EDS) and for bioaccessibility testing. The 250 μm fraction was selected because it was considered to be the particle size most likely to adhere to children’s hands and thus most likely to be ingested.24 Uranium Analysis in Soil Samples. The concentration of uranium in soil samples was determined by the combination of the microwave digestion and inductively coupled plasma mass spectroscopy (ICP-MS) method. Microwave-assisted acid digestion (based on EPA Method 3051A)25 utilized partial digestion of the solid material by a mixture of hydrochloric and nitric acids (aqua regia). The weighed homogenized sample (0.5 g) was thoroughly wetted by 15 mL of the mixture of nitric and hydrochloric acids in a high-pressure Teflon cup and digested in the microwave (Ethos EZ, Milestone) at 200 °C for 30 min. An analysis blank was run with each batch of unknown and QC samples. Upon completion of the digestion, nondigested solid (usually siliceous particles) was separated by centrifugation for 5 min at 4000 rpm in an Eppendorf centrifuge 5810. A 2 mL aliquot of the supernatant was then diluted with water to 100 mL upon addition of the multielement internal standard solution (to have 50 ppb of internal standard (ISTD) in each sample) and analyzed by ICPMS (based on EPA Method 6020).25 For quality assurance and quality control (QA/QC), one of the standard reference materials containing uranium used for method calibration and validation was digested and analyzed with each batch of soil

(R2 = 0.924)

which shows that the RBA is approximately 88% of IVBA.18 In fact, U.S. Environmental Protection Agency (U.S. EPA) has approved the use of easier-to-perform bioaccessibility determinations18 in site-specific risk assessments of leadcontaminated soils. Bioaccessibility of uranium has been measured by use of cola drinks19 and by simulated gastric5 and gastric plus intestinal solubilization.20−22 In general, measured bioaccessibility of uranium is low, and only a few percent of uranium present in a soil sample can be extracted. However, the studied soil samples were composed of minerals with high silica content that were nearly completely insoluble in simulated gastric and/or intestinal fluids and often contained very low (at natural background levels) concentrations of uranium. Therefore, the results of those studies are of limited value for more general use in assessing the risks of exposure to uranium from contaminated industrial and residential lands. Historical low-level radioactive waste (LLRW), such as uranium, Ra-226, and Th-230, in the Port Hope area in Ontario, Canada, originates from radium and uranium refining during the period from 1932 to 1988. LLRW is found at various industrial, waste management, and residential sites within the municipality of Port Hope, including the Port Hope Harbor. According to some previous studies,23 the concentration of uranium in the Port Hope area ranges from 0.24 to 93.6 mg/kg in the top 15 cm soil horizon. It has recently been shown6 that there are two main types of soil in the contaminated area in Port Hope, such as medium sand over loam or sandy fill and lacustrine silt loam, but that their chemical properties were similar and the soils were uniform. On the basis of extensive measurements, the authors concluded that6 “the soils are sandy loams with pH 7.1, 4.1% organic matter, 11% clay and contain 200 mg carbonate kg−1 dry soil”. It is also noteworthy that contaminated soil in the Port Hope area is characteristic for urban setting with various 9013

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variety of contaminants relevant for human risk assessment. The protocol of that test is summarized below. Gastric Phase. Approximately 1 g of soil sample was mixed with 100 mL of gastric extraction fluid in a Nalgene 125 mL bottle. Gastric extraction fluid was made to mimic the composition of the human stomach by dissolving 1.25 g of pepsin, 0.50 g of sodium citrate, 0.50 g of DL-malic acid disodium, 420 μL of lactic acid (85%), and 500 μL of acetic acid in 1 L of Millipore water. The pH was then adjusted to 1.80 ± 0.05 with 33% HCl. Prior to mixing of the sample with the “gastric” fluid, the fluid was warmed to 37 °C in the incubator (Fisher Scientific IsoTherm). After the sample was mixed with the fluid, the pH was adjusted to 1.80 ± 0.05 with 33% HCl. The sample solution was then shaken for 0.5 h at 220 rpm and 37 °C, and the pH was checked and adjusted to pH 1.8 ± 0.1 if necessary. After the pH adjustment, the solution was returned to the incubator and shaken for another 0.5 h at 37 °C. At the end of the “gastric” phase, the pH was recorded, a 10 mL aliquot was collected into a 15 mL centrifuge tube, and adequate quantities of ISTD solution and HNO3 were added. The aliquot was then centrifuged at 4000 rpm for 5 min and analyzed by ICP-MS, via the same method as for the soil digest analysis (see Uranium Analysis in Soil Samples section). Gastric plus Intestinal Phase. The pH of the remaining sample solution was adjusted to 7.0 ± 0.2 with saturated sodium carbonate solution (usually around 1 mL was added to a 90 mL sample solution). Ten milliliters of “intestinal” fluid containing 175 mg of bile salts and 50 mg of pancreatin in water was added to the sample solution. The sample solution was then shaken for 4 h at 220 rpm and 37 °C. At the end of the 4 h “intestinal” phase, the samples were taken from the incubator and the pH of each solution was recorded. A 10 mL aliquot from the sample solution was collected into a 15 mL centrifuge tube, and adequate quantities of ISTD solution and HNO3 were added. The aliquot was then centrifuged at 4000 rpm for 5 min and analyzed by ICP-MS, via the same method as for soil digest analysis. For QA/QC of PBET, an analysis blank as well as a physiological fluid sample spiked with uranium was run with each set of soil samples. The recovery of uranium from the spiked sample was higher than 90%. We also performed repeated independent digestions of selected soil samples. The standard deviations of results obtained from the independent digestions were within the standard deviation of the triplicates in each digestion.

samples. The recovery of uranium from uranium SRMs was found to vary by less than ±10%. The ICP-MS instrument was Agilent 7700x, with AXS-520 autosampler and Micro-Mist nebulizer. The ICP-MS instrument was set for the high matrix introduction plasma correction, which resulted in dilution of the sample stream reaching the plasma by Ar gas to minimize the effects of high concentration of matrix. The sensitivity of analysis was lower at the high mass end by about a factor of 10, while there was no need to further dilute the sample. The instrument was also run in the He mode, which means that the ionized sample was treated by He gas in the octopole reaction cell prior to reaching the quadrupole and the detector to minimize molecular and double-charged ion interferences. For more information about the ICP-MS analysis combined with the microwave digestion, see Supporting Information. From the results of uranium analysis, the selection of Port Hope soil samples for bioaccessibility testing and SEM/EDS examination was made on the basis of the following criteria: • The samples were collected from depths of less than 50 cm (because the probability that soils deeper than 50 cm contribute to health risks was negligible). • The concentration of uranium was higher than 1 mg/kg in the sample. The 1 mg/kg limit was chosen as the lowest limit for a meaningful bioaccessibility test. This limit was similar to the average natural concentration of uranium in soil1 (2.8 mg/kg). By use of the above criteria, a set of 33 soil samples was chosen for bioaccessibility testing and SEM examination from the total of 56 analyzed. Scanning Electron Microscopy and Energy-Dispersive X-ray Spectroscopy. Selected Port Hope soil samples were examined on a Carl Zeiss EVO MA10 SEM equipped with a LaB6 filament, and analyzed by use of an Oxford X-Max 20 EDS. Prior to introduction into the SEM sample chamber, the soil samples were mounted on 12 mm aluminum stubs by use of double-sided sticky carbon discs without coating. Such preparation, without coating and with a conductive carbon layer, is ideal for examining the morphology of the soil particles but rendered soil samples poorly conductive, and high electron charging was always an issue. To avoid excessive charging, low accelerating voltages (1−5 kV) were used at high vacuum for imaging with both the secondary and the backscattered electron detector. For EDS analysis, where relatively high accelerating voltage (e.g., 20 kV) had to be used in order to detect the Xrays of elemental U, the variable pressure (VP) mode was used with a residual chamber pressure of 10−50 Pa. To ensure best energy calibration in EDS analysis, the X-ray energy of the XMax 20 was calibrated with a pure Cu standard prior to each session. Physiologically Based Extraction Test. Various in vitro bioaccessibility tests and their variants have been evaluated and some of them approved by environmental authorities18 for use in site-specific ecological risk assessments. One of the most important properties of any bioaccessibility test is whether it gives consistent and reproducible results. The Bioaccessibility Research Canada (BARC) was established in 2006 to further develop the scientific basis for using in vitro bioaccessibility models to measure and predict the relative bioavailability (RBA) of soil contaminants.24 A variant of the physiologically based extraction test (PBET)24 was proposed by BARC as the experimental procedure that gives consistent results for a

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RESULTS Soil Types. The soil types at sample locations used in this study were determined from the measured particle size distribution by using the methodology in ASTM 2487-06 and 2488.26 Partial soil classification using particle size analysis of selected dry soil samples (one sample for each property) yields the following: four samples were GW-GC-GM (well-graded gravel with clay and silt), three samples were SC-SM (clayey, silty sand), one sample was SM (silty sand), and one sample was GC (clayey gravel with sand). The pH of those soil samples, representative of sampling locations, was measured to be from 7.11 to 8.80. Previous study6 showed that there were two main types of soil in the contaminated area in Port Hope, namely (1) medium sand over loam or sandy fill and (2) lacustrine silt loam. It was also found that their chemical properties were 9014

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Table 1. Results of Uranium Bioaccessibility (BA) and SEM Analyses samplea

sample depth, cm

[U] in soil ±10%, ppm

ravine 1 ravine 2 ravine 4 ravine 3 property 24-1 property 24-2 property 26-1 property 26-2 property 26-3 property 26-4 property 26-5 property 26-6 property 26-7 property 26-8 property 27-1 property 27-2 property 27-3 property 27-4 property 29-1 property 30-1 property 30-2 property 30-3 property 33-1 property 33-2 property 33-3 property 33-4 park 1 park 3 park 2 waste soil 1 waste soil 2 waste soil 3 waste soil 4 BL-1b DL-1ab UTS-2b NIST 2710ac

0−5 5−10 15−20 10−15 10−15 15−25 15−30 15−30 20−30 0−10 10−20 0−15 15−25 35−45 15−20 20−30 30−40 10−20 10−20 10−15 0−10 10−20 10−20 10−20 20−25 25−30 0−5 10−15 5−10

10.6 12.0 13.3 12.2 4.5 5.0 6.9 12.8 150.2 19.1 8.0 7.1 6.0 4.9 3.3 13.8 123.1 5.4 31.6 1.1 116.1 116.7 110.3 134.9 219.3 94.5 89.8 482.1 382.0 9.2 14.9 8.3 26.7 220.0b 116.0b 56.0b 9.11c

gastric BA ± SD, % 14.6 16.9 21.8 10.4 14.4 10.2 15.5 17.3 30.9 17.6 14.9 12.3 21.7 52.0 15.8 38.4 53.7 10.0 14.6 11.9 32.5 26.9 20.8 11.2 26.8 27.1 6.3 7.8 5.6 27.9 21.5 31.9 26.2 46.8 27.4 10.1 34.1

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

4.5 3.5 2.9 0.8 5.5 3.4 1.6 0.1 2.3 1.6 0.7 2.2 0.4 14.9 1.2 3.8 8.3 1.0 0.6 3.0 7.5 3.9 4.4 0.8 0.9 4.5 1.2 0.5 2.0 2.9 1.9 12.5 6.5 2.1 4.5 1.0 1.6

gastric + intestinal BA ± SD, % 48.4 41.0 42.7 36.6 17.3 11.5 61.3 58.3 41.7 78.1 59.2 59.6 59.5 59.3 29.4 45.1 70.8 48.2 47.8 31.3 69.3 58.0 55.6 21.2 43.2 43.3 49.6 39.0 36.3 70.3 40.3 68.5 55.3 43.7 26.9 11.3 38.0

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

1.7 0.6 2.0 2.8 4.9 2.6 1.5 1.0 0.4 3.5 5.9 5.9 1.3 2.8 0.3 4.5 1.3 4.2 2.7 1.6 1.4 5.0 4.8 0.5 1.0 5.1 13.0 2.5 5.3 2.2 7.7 6.5 7.4 1.4 1.4 0.6 1.1

U-bearing particle size, μm 2−4

not found

1−2

1−2 2−4 1−2

5−25

5−10

∼1 ∼2 ∼1 1−5 1−5

a Samples taken from different residential properties are identified as property NN-N, where the first two digits identify the property and the last digit is the sample identifier. Samples taken from publicly accessible sites are labeled as ravine and park. Samples taken from the waste management site are identified as waste soil. Sample depth is irrelevant for the waste samples and for the ore standards. bCanada Centre for Mineral and Energy Technology SRM (see Materials and Methods and Supporting Information for details). [U] is the certified concentration. cNIST Montana I soil. [U] is the certified concentration.

Typical pH range measured in soil solutions upon the completion of the “gastric plus intestinal” phase was from 7.0 to 7.1. The measured uranium concentration in the “gastric plus intestinal” solution (corrected for dilution) is divided by uranium concentration in the soil sample, multiplied by 100, and expressed as gastric plus intestinal bioaccessibility (percentage) (since the concentration of U in the “gastric” phase adds to the “intestinal” yield). The results of the PBET of Port Hope soil samples for uranium are summarized in Table 1. The results are the average of at least three values (all samples in one batch were run in triplicate).

similar and the soils were uniform. Our results appear to be in full agreement with the results of that study. Bioaccessibility of Uranium. The concentrations of uranium in the Port Hope soil samples and in certified reference materials digested in aqua regia by following the microwave digestion protocol were measured by inductively coupled plasma mass spectroscopy (ICP-MS). The uranium concentration values given in Table 1 are the average of at least two independent digestions. Bioaccessibility of uranium was determined in 33 Port Hope soil samples and four certified reference materials. Typical pH range measured in soil sample solutions upon the completion of the “gastric” phase was from 1.7 to 2.1. The measured concentration of uranium in the aliquot taken from the “gastric” solution (corrected for dilution) is divided by uranium concentration in the soil sample, multiplied by 100, and expressed as gastric bioaccessibility (percentage).

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DISCUSSION The correlation between measured bioaccessibility and concentration of uranium in the Port Hope soil samples was tested by regression analysis. There was no significant 9015

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Figure 1. Results of the statistical analysis of the PBET digestion of Port Hope soil samples. The error bars represent one standard deviation from the mean.

Figure 2. SEM backscattered electron micrographs and EDS spectra. (Left) Soil sample park 2; (right) soil sample property 27-4. Note that the bright uranium-bearing particle in the middle of the left graph measures about 10 μm, and four uranium-bearing particles in the middle of the right graph measure about 1 μm or less. The EDS spectrum shown on the left was taken from a point near the center of the U-bearing particle, and that shown on the right was from the biggest of the four U-bearing particles.

correlation between measured bioaccessibility and the concentration of uranium in the Port Hope soil samples (R2 = 0.017 for gastric and 0.018 for gastric plus intestinal). Therefore, the concentration of uranium in the sample in the concentration range studied has very little influence on its extractability by simulated GI fluids. Similar results were previously obtained for the PBET bioaccessibility of arsenic and lead from soil.24

The results of the statistical analysis by descriptive statistics of the bioaccessibility results for Port Hope soil samples are summarized in Figure 1. The mean bioaccessibility of uranium in the gastric plus intestinal phase was significantly higher, 48.4% ± 16.8%, than in the gastric phase, 20.8% ± 11.7%. The F-test confirms such conclusion, with F = 0.544, f = 0.554; P(F ≤ f) = 0.045. 9016

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For the uranium ore standard reference materials DL-1a and BL-1, where only natural primary uranium minerals are present, the bioaccessibility values are lower than in contaminated soil reference material NIST 2710a. If any of the primary U minerals, such as davidite, or U-bearing minerals, such as monazite, are present, their dissolution will be much slower and would lead to lower bioaccessibility. Note that the gastric values for these reference materials are on the lower side but not as low as would be expected on the basis of the uranium mineralogy. This may readily be explained by the small particle sizes in these samples due to pulverization. As may be expected, the particle size effect is more pronounced in the gastric phase.

Higher values of bioaccessibility of uranium in the gastric plus intestinal phase than in the gastric phase are very probably due to more efficient extraction of uranium from soil by intestinal fluid rich in carbonate ions. In the presence of carbonate, which is used to simulate the “intestinal” conditions, U(VI) ion will apparently be incorporated in water-soluble uranyl carbonate complexes, thus increasing its extractability.3,29 Our measured values for bioaccessibility of uranium are considerably higher than the literature values (e.g., in Iqaluit soil samples21 the median values are 3.5% for gastric and 1.7% for intestinal bioaccessibility, and 0.49% for synthetic intestinal condition in the black sand samples from Camargue20). This could be due to the difference in soil composition, which greatly influences the solubility of uranium in simulated physiological fluids. Both Iqaluit21 and Camargue beach20 soil samples contain a considerable proportion of sand, which makes them poorly soluble in the simulated fluids. In general, poor solubility of soil components in simulated GI fluids would adversely affect the bioaccessibility of any contaminant. The bioaccessibility of uranium in certified uranium ore and tailing reference materials (BL-1, UTS-2, and DL-1a) and in highly contaminated soil standard reference material (NIST 2710a) was in the same range as that measured in the Port Hope soil samples. Those results can be used in the future determination of site-specific bioaccessibility values for standardization and quality control. It is noteworthy that the bioaccessibility of uranium in NIST 2710a, which is similar to the SRM (NIST 2710) often used for quality control of bioaccessibility of arsenic and lead,24 behaves comparable to the soil samples from Port Hope; that is, the gastric plus intestinal bioaccessibility is slightly higher than the gastric bioaccessibility. The variability of measured bioaccessibility values is relatively high, from 5.6% to 53.7% for gastric phase and from 11.5% to 70.8% for gastric plus intestinal phase (see Table 1). We used SEM−EDS in an attempt to rationalize the observed variability of bioaccessibility values. The SEM−EDS analysis of soil samples to determine the size of uranium-bearing particles is illustrated in Figure 2. A more complete summary of SEM micrographs may be found in Figure 1S (Supporting Information). An in vitro bioaccessibility test is basically a kinetic experiment of dissolution; the amount of uranium dissolved in simulated GI fluid is a function of many parameters, such as mineralogy of U-bearing particles, test duration, particle size, system redox potential, soil sample porosity, solid-to-liquid ratio, and liquid diffusion rate. In soil samples with similar uranium content, the smaller the particles are, the greater the total surface area will be. Greater surface area makes it more probable for the dissolving agents to be adsorbed onto the particle surface for reaction and results in faster dissolution kinetics and therefore higher bioaccessibility. Uranium bioaccessibility values in both gastric (acidic) and gastric plus intestinal (neutral) phases are generally higher in soil samples with smaller uranium-bearing particles, such as property 27-3 (53.7% and 70.8%, respectively), property 30-2 (32.5% and 69.3%), property 26-3 (30.9% and 41.7%), and waste soil 4 (26.2% and 55.3%), and lower where the uranium-bearing particles are bigger, such as park 3 (7.89% and 39.0%), ravine 2 (16.9% and 41.0%), and property 29-1 (14.6% and 47.8%). We postulate that the most important reason for the variability of bioaccessibility values in Port Hope soil samples may be the difference in particle size of uranium-bearing particles.

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ASSOCIATED CONTENT

S Supporting Information *

Two tables and one figure providing additional information on analytical method validation and on the size of uranium-bearing particles in soil samples from Port Hope. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]; phone: +1(613)-998-3855. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank the staff of the CNSC’s Waste and Decommissioning and Environmental Risk Assessment Divisions for their assistance in obtaining Port Hope soil samples. The assistance and helpful advice of the Environmental Sciences Group from the Royal Military College, Kingston, Ontario, Canada, in bioaccessibility method development and validation is gratefully acknowledged. We are also grateful to Drs. Said Hamlat and Patsy Thompson of Canadian Nuclear Safety Commission for their helpful suggestions for improvement of the manuscript.

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REFERENCES

(1) Supply of Uranium, World Nuclear Association; available at http://www.world-nuclear.org/info/inf75.html. (2) Markich, S. J. Uranium speciation and bioavailability in aquatic systems: An overview. Sci. World J. 2002, 2, 707−729. (3) Agency for Toxic Substances and Disease Registry (ATSDR), Toxicological Profile for Uranium; available at http://www.atsdr.cdc. gov/toxprofiles/tp150-c3.pdf (accessed on January 31, 2012). (4) Choi, J.; Park, J. W. Competitive adsorption of heavy metals and uranium on soil constituents and microorganism. Geosci. J. 2005, 9 (1), 53−61. (5) Dresssen, D. R.; Williams, J. M.; Marple, M. L.; Gladney, E. S.; Perrin, D. R. Mobility and bioavailability of uranium mill tailings contaminants. Environ. Sci. Technol. 1982, 16, 702−709. (6) Sheppard, S. C.; Sheppard, M. I.; Ilin, M.; Thompson, P. Soil-toplant transfers of uranium series radionuclides in natural and contaminated settings. Radioprotection 2005, 40 (Suppl. 1), S253− S259. (7) Ortiz-Bernard, I.; Anderson, R. T.; Vrionis, H. A.; Lovley, D. R. Resistance of solid phase U(VI) to microbial reduction during in situ bioremediation of uranium-contaminated groundwater. Appl. Environ. Microbiol. 2004, 70 (12), 7558−7560. (8) Trenfield, M. A.; McDonald, S.; Kovacs, K.; Lesher, E. K.; Pringle, J. M.; Markich, S. J.; Ng, J. C.; Noller, B.; Brown, P.; van Dam, R. A. Dissolved organic carbon reduces uranium bioavailability and toxicity. 1. Characterization of an aquatic fulvic acid and its

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dx.doi.org/10.1021/es3021217 | Environ. Sci. Technol. 2012, 46, 9012−9018