Absorption of radiocaesium by sheep after ingestion of contaminated soils

the Science dthe Toullu A.--m-LI-“.yIyIELSEVIER

The Science of the Total Environment 192 (1996) 21-29

Absorption of radiocaesium by sheep after ingestion of contaminated soils A.I. Cooke”, N. Greenb, D.L. Rimmer”, T.E.C. Weekes”, B.T. Wilkinsb,*, N.A. Beresfordd, J.D. Fenwick” =+Department ‘Department

of Biological

and Nutritional Sciences, University of Newcastle-upon-Tyne, Newcastle upon Tyne. NE1 7RiJ. UK bNational Radiological Protection Board, Chilton, Didcot, OX1 1 ORQ, UK af Agricultural and Environmental Science, University of Newcastle upon Tyne. Newcastle upon Tyne, NE1 7RU, UK dlnstitute of Terrestrial Ecology, Merlewood Research Station, Grange over Sands, LA1 1 6JU. UK ‘Department of Medical Physics, General Hospital, Newcastle upon Tyne, NE4 6BE, UK

Received 9 May 1996; accepted 7 July 1996

Abstract The absorption of 13’Csby sheepfollowing ingestionof contaminatedsoil was studied using an establisheddual isotopemethod. Two agricultural soilswere studied:an alluvial gley contaminatedby dischargesto the seafrom the SellafieldReprocessingPlant, and a lowland organic soil that had been artificially contaminated. Values of the true absorptioncoefficient of radiocaesiumof 0.19f 0.03 and 0.03 + 0.01, respectively,were obtained for thesesoils.This impliesthat availability of soil-associatedradiocaesiumfor uptake following ingestion is up to about 20% of that when the activity is incorporated in vegetation. Theseresultshave beencomparedto estimatesof availability made using an in-vitro approach describedpreviously and found to be in good agreement.However, comparisonwith in-vitro data obtained for an upland peat indicated that absorptionfrom someupland organic soilscould be greater than from the lowland organic soil. Keywords: Radiocaesium;Absorption; Soil ingestion;Bioavailability

1. introduction Ingestion of contaminated soil has been identified as a potentially important pathway for the

* Corresponding author. Published by Elsevier Science B.V. PIZ SOO48-9697(96)05288-6

transfer of radionuclides to the tissues and products of grazing ruminants [1,2]. Soil ingestion occurs either after resuspension of soil particles on to fodder-plant surfaces or from inadvertent ingestion of particles directly from the soil surface. It is apparent that when soil-plant transfer of a radionuclide is low, soil-associated activity

can form the bulk of the animals’ intake. Broadly, when soil-plant transfer factors are lower than 0.1 (Bq/kg:Bq/kg), expressed in terms of the dry mass of both soil and plant, soil-associated activity could form a significant proportion of intake, independent of the degree of soil contamination of the fodder [3,4]. The availability of radiocaesium for transfer from soil to plant is variable and strongly influenced by soil characteristics [5,6]. Generally, in acid organic upland soils radiocaesium remains associated with the ion-exchange complex and is thus in a form available for uptake by vegetation. whilst in soils with a higher mineral component, a greater proportion of radiocaesium is fixed irreversibly within clay mineral structures and less is available for uptake via roots. Although the potential contribution of soil to radionuclide intake by grazing livestock has been recognised, few data exist on the extent to which soil-associated radionuclides are absorbed by the animal after inadvertent ingestion. Field measurements have indicated that when a significant proportion of the intake was associated with soil, radiocaesium transfer to cattle was substantially less than would have been expected had all the activity been incorporated in vegetation [7]. Similarly. in-vivo experiments conducted by Howard et al. [8] showed that Cs absorption by sheep was greater for vegetation contaminated by deposition from the Chernobyl accident than for saltmarsh vegetation, in which > 90% of the activity was present as contaminated silt. Radiocaesium associated with silt therefore appeared to be less hioavailable than that incorporated into, or deposited onto vegetation. Beresford et al. [9] fed a range of artificially and environmentally contaminated materials to sheep and found that. of those tested, radiocaesium associated with silt gave the lowest absorption. Feeding trials have also been used to study radiocaesium transfer from soil to animal products [lo 121. Although this does not provide a direct estimate of absorption, the results obtained suggested absorption from soil was low, but that variation between different soil types could be considerable. Despite the recognition that bioavailability may Y:K~ ;tccording to the origin of the activity, data

on absorption of radiocaesium from different soil types are still scarce. Radiological assessment models that make little differentiation between bioavailability from separate components of ingested activity could therefore overestimate transfer when part of the activity ingested was associated with soil. Measurement of absorption from different soil types would provide useful data for two purposes; firstly, for refinement of radiological assessment models; secondly, for comparison with data from parallel in-vitro studies which, when validated, may offer a rapid means of assessing bioavailability from different sources [13-151. The crudest estimate of absorption can be derived from a simple balance of activity ingested and faecal output to obtain the apparent absorption coefficient (A,). However, although this parameter has often been used to represent the gut absorption parameter fi in radiological assessment models, it does not take the process of endogenous excretion into account, and so can underestimate fractional absorption. Also, methods involving faecal balance are not sensitive when the source is of low bioavailability, as might be expected with soil [16]. For this reason, in the present study a dual isotope approach has been used to derive the true absorption coefficient (A,) of radiocaesium from two soil types from the calculated blood plasma turnover rate of the dietary isotope. Similar approaches have previously been applied to estimation of radiocaesium absorption from various sources [9,16,17]. The results obtained are of use for development of radiological assessment models as the true absorption coefficient is the same parameter as f,. The values of A, obtained can also provide a means of validating observations made using in-vitro experiments [13].

2. Materials

and methods

2.1. Soils Two soils were used in this study. The first was an alluvial gley soil, sampled from a tidally inundated pasture at Muncaster Bridge, on the south

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bank of the River Esk which forms part of the Ravenglass Estuary, West Cumbria, UK (Map Reference SD109962). Most of the activity in this soil is derived from marine discharges from the nearby Sellafield Nuclear Fuel Reprocessing Plant; a small proportion of the total activity discharged becomes associated with sediments, which can be transported to land and deposited on coastal pastures by tidal action. The second was a lowland peat soil, originally collected in East Anglia, but sampled from a lysimeter at the National Radiological Protection Board (NRPB), where it had been artificially contaminated with radionuclides some 10 years previously [18]. This soil is referred to as the lysimeter peat in the remainder of this paper. The physical characteristics of both soils are given in Table 1. In both cases soil cores were collected to a depth of about 100 mm using a 100 mm diameter percussion corer. Vegetation was carefully removed; the top 20 mm of soil was separated for experimental use and then sieved through a 2 mm mesh. Any roots passing through the sieve were included within the sample. Soils were stored in field-moist condition in a cold room at 3°C until used. Subsamples were dried in an oven at 80°C to determine the fresh:dry mass ratio. Three further subsamples of each soil were taken for the determination of radionuclide content. 2.2. Injimte A vial of ‘34CsC1 was obtained from Amersham International (Amersham Laboratory, Amersham, Bucks, UK), and an aliquot diluted with sterile saline solution to give a stock solution Table I Physical characteristics of experimental soils Characteristic

Alluvial gley

‘!;I of mineral fraction: 3 >60 pm 2 pm-60 pm 65 <3 pl?l 32 “% organic C 10.9 pH (distilled water) 6.5 CEC (cmol kg--‘) 44.1 -..___ .-

Lysimeter peat 26 35 39 35 5. 9 133

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containing about 370 Bq ml - ’ of ‘j4Cs. Of this stock solution, 5 ml was injected into each of the 32 1 1 sterile saline packs to be used in the experiment. 2.3. Experimental

unimals

Eight, l-year old male, cross-bred wether sheep were used in the experiment, divided into two groups of four animals. The mean weight at the beginning of the experiment was 51.5 kg. A silastic infusion catheter was implanted into the jugular vein of each sheep. 2.4. Experimental

protocol

Sheep were housed in individual metabolism cages throughout the experiment and were fed a diet of 100 g hay and 550 g of a blended concentrate feed (Dengie Sheep Blend 4s; Dengie Feeds, Southminster, Essex, UK) twice daily at about 08:OO and 16:00 h. Total faeces and urine collections began on day 1 and were made daily throughout the six-week duration of the experiment. Faeces were collected in faecal bags and urine in buckets containing 25 ml 4 M HCl. A muslin filter was used to guard against contamination of urine with faeces or soil. On days l--7 urine and faeces samples were collected solely to obtain background measurements. Administration of soil and infusate began simultaneously on the morning of day 8 of the experiment, and continued until the morning of day 36 (four weeks). The mean equivalent mass of soil administered daily, converted to a dry mass basis, was 29.15 g of the alluvial gley and 24.15 g of the lysimeter peat. Initially, soil was packed into gelatine capsules (18 x 35 mm, Davcaps, PO Box 48, Hitchin, Herts), two of which were administered twice daily, prior to feeding, using a bauling gun. This approach was discontinued after one week when some animals showed adverse effects; one animal from the group being fed peat soil was removed from the experiment. Subsequently, an equivalent mass of soil was mixed in with the feed. The infusate was supplied at about 110 ml per day using a calibrated peristaltic pump. Samples of infusate were collected from the delivery

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end of each infusion line at the beginning and end of the infusion period and the radiocaesium content determined. Infusate packs were changed weekly, and weighed before and after use. After day 36, when infusion and soil administration ceased, collection of faeces continued for a further week. On day 43 all animals were humanely slaughtered and samples of muscle and liver taken for analysis. These samples were stored in a freezer until required, then freeze-dried and ashed in a muffle furnace at 450°C. Urine samples were bulked on a weekly basis. Half of the total weekly urine output was discarded and the remainder stored in a cold room at 3°C until required for analysis. Before analysis, the volume of the urine samples was reduced to less than 1 1 by slow evaporation on a hotplate; the samples were then quantitatively transferred to 1 1 Marinelli containers. Daily outputs of faeces were weighed and then dried at 120°C; the output from each week was then bulked and homogenised. A subsample was then taken for determination of radiocaesium and plutonium content. The latter was required in order to estimate the proportion of the administered soil that had been ingested (Section 4). 2.5. Radiochemical

analysis

Analysis of radiocaesium isotopes in urine, faeces, tissues, infusate and soil was undertaken by gamma-ray spectrometry. Measurements were made using a hyperpure germanium detector that had been appropriately calibrated. All measurements of radiocaesium were decay corrected to the beginning of the experiment. Plutonium was determined in soil and faeces samples by dissolution, radiochemical separation and alpha spectrometry, using methods based on Krey and Beck [19]; these methods have been validated by NRPB, and are in regular operational use at its laboratories.

3. Calculation

of the true absorption coefficient

The true absorption coefficient (A,) is defined as the amount of an ingested radionuclide which is

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absorbed from the gut expressed, as a fraction of the total daily intake of the radionuclide [9]. The estimation of absorption across the gut by this method has an advantage over experiments such as those involving determinations of transfer to milk or tissue, in that it is not necessary for activity concentrations within the animal to be at equilibrium with the intake. Provided oral and intravenous administration begin simultaneously, the isotopic ratio in blood should soon reach equilibrium, and allow estimation of the blood plasma turnover rate (BPT) of the dietary isotope from the isotopic ratio in any tissue or fluid in which activity is derived exclusively from the blood plasma [9]. In this study the blood plasma turnover rate of radiocaesium, and hence A,, has been estimated primarily from the equilibrium isotopic ratio in urine using the following equations: BPTL3’Cs(Bq

d - *) =

Urine’37Cs(Bq d - ‘) Urine134Cs(Bq d - ‘>

x ‘34Cs infusion rate(Bq d-l)

(1)

BPTi37Cs(Bq d - ‘) ” = 13’Cs intake(Bq d - ‘) Liver and muscle also fulfil the required criterion, and the efficacy of using these tissues to estimate A, values was evaluated. For these calculations, the corresponding ratio was substituted for that of urine in Eq. (1).

4. Results

The mean activity concentration of ‘34Cs, measured from 13 samples of the infusate was 1.87 _+ The activity concentrations of 0.12 Bq ml-‘. radiocaesium isotopes and 239’240Pu measured in the experimental soils are shown in Table 2. For both soils the activity concentration of ‘34Cs was negligible compared to the daily rate of infusion ( > 200 Bq) of 134Cs, and would therefore not be expected to affect the ratio of isotopes in the blood plasma significantly.

A.I. Cooke et al. / The Science of the Total Environment 192 (1996) 21-29 Table 2 Activity concentrations experimental soils Radionuclide

of radionuclides

239,*40pu

of interest in the cl,20

Activity concentration (Bq kg-‘, dry weight) Alluvial gley

I‘4Cs I‘7Cs

16+11 3560+365 1mI+70

Lysimeter peat

0,15 i! 'iz 3 .E cn ;s"

110 4440+320 405Ok660

Uncertainties represent the standard deviation about the mean of three replicates.

Because of the change in method of administration of the soil during the course of the experiment, it was necessary to estimate the extent to which the supplied soil was ingested by the animals. 239/240Puprovided a convenient marker for this purpose. It was readily measurable in both soils, and the gastrointestinal absorption is low, typical fi values being around 5 x 10 -’ [20]. Consequently, essentially all of the activity ingested would be excreted in the faeces. The total amounts of 239/240Pu administered and excreted were estimated from the measured concentrations in soil and faeces. The results are shown in Table 3. These indicate that almost all of the soil supplied was ingested. The ratio of Cs isotopes in bulked weekly urine samples is shown in Fig. 1. The ratio in the fourth week of Cs administration (bulked collection from days 30-36) has been used to estimate A, for 137Cs, as isotopic equilibrium was not reached until the third week. Values of A, were derived for both soils based on the isotopic ratios in urine, muscle and liver; the results are shown in Table 4. Table 3 Total amounts of 2391240Pu(Bq) administered excreted in faeces Group Alluvial Gley Lysimeter Peat

25

n

4 3

0.10

Li 0 k 0.05

0.00

Day Fig. 1. Change into ratio of Cs isotopes in urine.

5. Discussion The isotopic equilibrium in urine, and therefore blood plasma, was not reached until the third week of administration. This was less rapid than in the study by Beresford et al. [9], where equilibrium was reached in less than a week. This was possibly due to two factors. First, the urine samples were bulked over a period of one week rather than the intervals of 3-4 days employed by Beresford et al. [9], which might give a less sensitive Table 4 Mean estimates of A, of Cs for two different soils estimated from the isotopic ratios in urine, muscle and liver samples

in soil and

239,240pu

239/24Opu

(administered)

(in faeces)

1473&18 2422+438"

1491+123 1925&453

Uncertainties represent the standard deviation about the mean of n replicates. “Adjusted for 35% refusals by one sheep.

Soil

n A, 13Cs calculated from the isotopic ratio Urine

Alluvial Gley 4 0.19 + 0.03 Lysimeter 3 0.03 * 0.01 Peat

Muscle

Liver

0.24 kO.05 0.03 + 0.01

0.30 + 0.08

0.05 + 0.01

Uncertainties represent the standard deviation about the mean of n replicates

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indication of changes in the isotopic ratio. Second, the ratio in blood plasma might have reached equilibrium more slowly because the animal initially accumulated ‘?‘Cs in its gastrointestinal tract due to the slower passage of soil compared to vegetation. It has been suggested by Mayes et al. [16] that differences in density between materials could influence the degree of retention in the gastrointestinal tract. The isotopic ratio in urine and muscle was similar. but values of A, based on the isotopic ratio in liver were significantly higher than those derived from the corresponding data for urine (P < 0.05). This observation could be the result of the continued absorption of 13’Cs from residual soil remaining in the gut after administration of “‘Cs infusate had ceased, liver being particularly responsive to such changes because of its high blood plasma turnover rate. This hypothesis was tested using the model of Galer et al. [21]: the predictions indicated that a short term increase in the ‘17Cs:‘3sCs ratio in the liver would be expected for a period of a few days after the cessation of isotope administration. In practical terms therefore, if the sheep had been slaughtered immediately after infusion ceased, then the isotopic ratios in tissue and urine are likely to have been similar. Consequently, if tissues are to be used to estimate ii,, then the animals must be slaughtered and tissue samples taken immediately after administration of activity ceases. The use of urine for this purpose would obviate this problem and also avoid the need to slaughter the animal, and so would be the preferred option. The remainder of this discussion is confined to the results obtained from urine. The value of A, obtained for the alluvial gley (0.19 &- 0.03) was comparable with a value of 0.12 obtained for Ravenglass silt also contaminated by marine discharges from the Sellafield nuclear fuel reprocessing plant [9]. The value for the lysimeter peat (0.03 & 0.01) was significantly lower than that for the alluvial gley (P < 0.01). For comparison. a value of 0.02 + 0.003 was obtained when a peaty podzol soil was administered to sheep, although the value obtained for cattle was somewhat higher [22], Values of the true absorption cc>cfticicnt of :Iround 0.80 0.90 have been found

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for radiocaesium administered in an available form [9,23]. Together, these results suggest that when associated with the alluvial gley and agricultural peat soil, absorption of radiocaesium is around 20 and 4%, respectively, of that administered in available form. The extent of absorption of soil-associated radiocaesium varies considerably according to factors such as soil type and the origin of the activity. For example, an A, value of about 0.01 can be inferred from the observed feed to milk transfer coefficients, F,, for sheep that were fed two artificially contaminated mineral soils [I I]. In contrast, the value that can be inferred from observed F,,, values for a mineral soil from Chernobyl were more than an order of magnitude higher [12], which could be a result of the peculiarities of the source-term, in particular the deposition of particulates in the near field. The relatively high value observed here for the alluvial gley could be the result of the particular characteristics of the sampling-site, which regularly receives fresh deposits of contaminated sediment. Fixation of radiocaesium to the sediments and soils of the Esk estuary has been studied in detail by Davies and Shaw [24], who found that the degree of fixation varied markedly according to such factors as the particle size distribution, clay mineral composition, and concentrations of competing ions, notably potassium and ammonium. Additionally, fixation may be affected by the soilwater status, which would in turn be influenced by the frequency of flooding, the time elapsed since the previous flood and fluctuations in the water table. In predicting availability of radiocaesium from ingested soil it may therefore be necessary to consider the physical and chemical characteristics of the deposit as well as those of the soil. The measured A, value observed for the lysimeter peat was at the lower end of the observed range. However, it has previously been demonstrated that fixation of radiocaesium varies considerably in different organic soils [6]. The soil used in this study was a well-developed lowland agricultural peat containing about 58% organic matter and originally collected from East Anglia. Clay-sized particles formed about 39% of the total mineral fraction (Table 2). Comparison with the

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Percentage of activity extracted from experimental soils after in-vitro incubation with rumen liquor [15] Soil

%I ‘37Cs extracted

Alluvial gley Lysimeter peat Peaty ranker _ Mean and standard deviation

7.44 & 0.92 1.14+0.09 12.58 + 2.53 of eight replicates.

observations of Valcke and Cremers [6] suggest that reasonably high fixation/low absorption might be expected in this soil, and the low availability observed in-vivo suggests that the ‘j’Cs was indeed fixed effectively. Estimates of A, can also be compared with the results of in-vitro extractions, to assess the usefulness of such procedures for estimation of bioavailability. For instance, Beresford et al. [9,23] observed a relationship between radiocaesium solubility from a variety of sources in 0.1 M CsCl, and absorption. However, few comparisons have been made between extractions from different soil types. A method has been developed at these laboratories in which in-vivo conditions in the rumen are replicated in-vitro [15]. This approach aimed to give an estimate of relative bioavailability for radionuclides associated with a range of soils after incubation with freshly-collected rumen liquor under appropriate conditions of pH and temperature. The percentage of activity extracted using this technique on the alluvial gley and the lysimeter peat are shown in Table 5. There appears to be a relationship between measurement of A, of 13’Cs from the two soils and parallel measurements of in-vitro extractibility, since in both cases the availability for the alluvial gley was greater than that for the lysimeter peat by approximately a factor of five. Furthermore it would appear that absorption in-vivo is proportionally greater than extraction in-vitro. This could be a consequence of further radiocaesium extraction under the more acidic conditions encountered by digesta after leaving the rumen. Significant differences were observed when the in-vitro extraction was applied to various organic soils. As an example, results for a peaty ranker,

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an acid organic upland soil, are also shown in Table 5. The proportion extracted from this soil was more than an order of magnitude greater than that extracted from the lysimeter peat. The peaty ranker has a higher organic matter content than the lysimeter peat (over 85%). It is established that soils with such high organic matter content fix radiocaesium very poorly [5,6]. Consequently, after inadvertent ingestion of some upland acid organic soils, A, could be higher than either of those obtained for the two soils tested in-vivo. The potential importance of soil ingestion in terms of transfer to animal products depends on other factors as well as the value of A,. For example, Crout et al. [25] have demonstrated that on upland British pastures soil ingestion is unlikely to be a significant mechanism for contamination of sheep. This is largely because of the higher soil-plant transfer found on upland organic soils, but a second factor could be that low bulk density organic soils may be less susceptible to resuspension and adherence to plant surfaces. The pastures adjoining the Ravenglass Estuary provide a contrasting situation: when soil constitutes about 10% of dry matter intake, then on the basis of an A, value of 0.2, soil ingestion not only dominates the intake of radiocaesium but would also be the major contributor to the activity absorbed [26]. The results of this study suggest that the true absorption technique gives a useful indication of differences in radiocaesium absorption from different soil-types and also appears to validate the use of the in-vitro extraction approach using rumen liquor to assess the bioavailability of soilassociated radionuclides. In view of the simple relationship between the absorption of radiocaesium and its solubility in rumen fluid, it appears that the proportion of radiocaesium extracted invitro, referred to by Cooke et al. [15] as the ‘availability factor’. can be manipulated to give an indication of potential absorption. Such an approach could therefore be applied rapidly and inexpensively to affected soils when needed. A variety of soils has already been investigated in this manner [26]. The incorporation of the availability factor into radiological assessment models is discussed elsewhere [27].

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Acknowledgements

AIC thanks NRPB and the UK Ministry of Agriculture, Fisheries and Food (MAFF) for financial support under the CASE studentship scheme. Part of the work reported in this paper was presented at the 3rd International Conference on the Biogeochemistry of Trace Elements, Paris, May 1995.

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