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TECHNICAL REPORT
Heavy Metals in the Environment

Cadmium Content of Wheat Grain from a Long-Term Field Experiment with Sewage Sludge

^a Agriculture and Environment Division, IACR-Rothamsted, Harpenden, Herts, AL5 2JQ, UK
^b Soil Science Dep., Faculty of Agriculture, Cairo Univ., Giza, Egypt
^c ADAS Gleadthorpe Research Centre, Meden Vale, Mansfield, Notts, NG20 9PF, UK

* Corresponding author (amar.chaudri{at}bbsrc.ac.uk)

Received for publication October 29, 2000.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 
Grain Cd concentrations were determined in the wheat (Triticum aestivum L.) cultivars Soissons, Brigadier, and Hereward grown in 1994, 1996, and 1999, respectively, in soils of a long-term field experiment to which sewage sludges contaminated with Zn, Cu, Ni, or Cr had previously been added. Soil pore water soluble Cd and free Cd²⁺ increased linearly with increasing total soil Cd (R² = 0.82 and 0.84, respectively; P < 0.001). Similarly, soil pore water free Cd²⁺ increased linearly with increasing soil pore water soluble Cd (R² = 0.98; P < 0.001). There was no evidence of a plateau in soil pore water Cd concentrations with increasing soil Cd concentrations. Grain Cd concentrations were significantly correlated with total soil Cd (P < 0.001), soil pore water Cd (P < 0.001), and free Cd²⁺ (P < 0.001). A slight curvilinear relationship between grain Cd and soil Cd was apparent, but there was no plateau, even at the maximum soil Cd concentration of about 2.7 mg kg^-1. The relationship between soil pore water Cd and grain Cd was linear for all three cultivars. The slopes were in the order 1994 > 1996 > 1999, with more Cd being taken up into the grain by Soissons grown in 1994, and least by Hereward grown in 1999. For Soissons, Cd concentration in the grain greater than the EU limit (0.24 mg kg^-1 dry wt.) occurred at soil Cd less than the current UK limit of 3 mg kg^-1 for soils receiving sewage sludge. In contrast, for Brigadier and Hereward, grain Cd concentrations were near to and less than the EU limit, respectively, at soil Cd concentrations of 3 mg kg^-1.

Abbreviations: GF–AAS, graphite furnace atomic absorption spectrometry • ICP–AES, inductively coupled plasma atomic emission spectrometry

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 
IN 1996 AND 1997, AN ESTIMATED 520000 Mg yr^-1 of sewage sludge dry solids, equivalent to 47% of total UK sludge production, were applied to only 0.5% of agricultural land, representing some 80000 ha (Gendebien et al., 1999). Total UK sludge production is predicted to increase to about 1.5 million Mg yr^-1 by 2006 (Gendebien et al., 1999). The ban on sewage sludge dumping in the North Sea took effect at the end of 1998, and has increased pressure for land application. Recycling of sludge to agricultural land is predicted to be a major outlet.

Sewage sludge is a useful source of nitrogen, phosphorus, and organic matter, and as a result of some conditioning processes some types have a liming value (Ministry of Agriculture, Fisheries and Food, 1986). However, concern arises from the fact that sewage sludges contain larger concentrations of heavy metals than most soils. Application to agricultural soils may result in elevated concentrations of potentially toxic metals, which may then enter the food chain. For example, the entry of Cd into the food chain is of particular concern as it can cause chronic health problems in humans such as bone disease, lung edema, renal dysfunction, liver damage, anemia, and hypertension (Nordberg, 1974; Nath et al., 1984). Because of this, Cd is one of a very small group of metals for which the Food and Agriculture Organization/World Health Organization (1978) have set a provisional daily intake limit for humans (70 µg Cd d^-1). Generally, the intake of Cd in very small concentrations by humans is unavoidable due to its ubiquitous nature, with agricultural foodstuffs being a major source. Of particular concern is the Cd content of grain and cereal products, as the consumption of these products is thought to contribute significantly to Cd in the human diet. For example, in the 1980s, the U.S. adult population was reported to receive about 20% of the Food and Agriculture Organization/World Health Organization (1978) allowable daily intake of Cd from the consumption of grain and cereal products (Wagner et al., 1984). In the European Community, grain and cereal products accounted for about 30 to 40% of the daily allowable Cd intake (Hutton, 1982).

Apart from human health concerns, the presence of nonessential and potentially toxic metals in agricultural produce can have serious implications for international trade. These quality issues can effectively become nontariff barriers to trade. Germany has had a limit for Cd in wheat grain of 0.10 mg kg^-1 fresh wt. (0.12 mg kg^-1 dry wt.) since 1986 (Bundesgesundheitsamt, 1986) and Australia and New Zealand had a limit of 0.05 mg kg^-1 dry wt., which was later increased to 0.1 mg kg^-1 (National Food Authority, 1993; Australia and New Zealand Food Authority, 1997, 1999). Other countries have as yet set no limits for grain Cd concentrations, although a recent EU regulation sets a limit of 0.1 mg kg^-1 fresh wt. for cereal products excluding bran, germ, and wheat grain, and 0.2 mg kg^-1 fresh wt. for bran, germ, and wheat grain (European Commission, 2001).

Because of the increase in sewage sludge recycling to agricultural land in the UK and elsewhere, and because of new legislation limiting grain Cd content being introduced, it is of paramount importance to determine possible long-term effects of soil Cd on wheat grain Cd. Few studies look at grain Cd content from long-term field experiments to which metal-contaminated sludges have previously been added. On the contrary, much data is produced using pot experiments where soils are either "spiked" with metal-contaminated sludges or metal salts. However, data on plant tissue metal concentrations from pot experiments cannot be directly compared with field data, because plant tissue concentrations can be one- to fivefold greater in pot experiments than field experiments (Logan and Chaney, 1983). In this study, we look at the grain Cd content of winter wheat grown over three seasons on plots of a long-term field experiment to which sludges contaminated predominantly with single metals were added in the past. Under field conditions, we studied the effect on wheat grain Cd of increasing soil Cd up to the current UK Cd limit of 3 mg kg^-1 for soils receiving sewage sludge.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 
Soils Used
The soils were sampled in spring 1999 from a long-term sewage field experiment at ADAS Rosemaund, Herefordshire, United Kingdom. Initially, the experiment was established in 1968 at the Luddington Experimental Husbandry Station, Warwickshire, on a sandy loam–textured soil (14% clay) of the Bishampton Association (Typic Ochraqualf). Sewage sludges obtained from sewerage works, which had sludges rich in either Zn, Cu, Ni, or Cr, were applied to attain a range of soil metal concentrations (Tables 1 and 2). The Cr-sludge was also contaminated with Cd (Table 2). Control non–metal enriched sludge was used where necessary to make up quantities, so that sludged plots received 125 Mg sewage sludge dry solids ha^-1 in 1968. Eight metal treatments were established along with an untreated soil and an uncontaminated sludge control treatment (Table 1). The design was a randomized block with four replicate plots per treatment. The initial soil pH was 6.2 and plot sizes were 1.8 x 4.5 m. In July 1991, the soils were excavated and transferred to ADAS Rosemaund, Herefordshire, where isolated plots (1.2 x 1.2 m) were established surrounded by oil-tempered hardboard.

Table 1 shows the treatments we sampled in April 1999, 30 yr after sludge addition ceased. Twenty soil cores were collected from each plot to a depth of 25 cm using a Dutch auger made of tempered steel, and bulked in the field to give representative samples of each plot. The samples were sieved moist to <3 mm, thoroughly mixed, and separated into 1 kg (oven-dry basis) portions to give triplicate samples for each plot.

Chemical Analysis of Soil and Soil Pore Water
Representative subsamples of the soils were air-dried, ground to <150 µm in an agate ball mill and digested using aqua regia (11.7 M HCl and 15.8 M HNO₃ acids, 4:1 v/v; McGrath and Cunliffe, 1985). The aqua regia–extractable metals are taken here to represent total soil metal concentrations, and were determined by inductively coupled plasma atomic emission spectrometry (ICP–AES) (Accuris, Applied Research Laboratories S.A., Ecublens, Switzerland), and graphite furnace atomic absorption spectrometry (GF–AAS; PerkinElmer [Norwalk, CT] GF-AAS-4100ZL), with Zeeman background correction, for Cd. Soil pH was determined in deionized distilled water (1:2.5 w/v), and soil percent C and percent N were determined using a Leco (St. Joseph, MI) CNS-2000 combustion analyzer. Soil Al, Fe, Mn, and P oxides were extracted using a mixture of ammonium oxalate and oxalic acids (0.114 and 0.086 mol L^-1, respectively) following the procedure of Janssen et al. (1997), before determination by ICP–AES.

Rhizon soil moisture samplers (Rhizosphere Research Products, Wageningen, the Netherlands) were used to extract soil pore water following the procedure of Knight et al. (1998). Briefly, these samplers consist of a length of inert porous (0.2 µm) plastic tubing, capped with nylon at one end, through which the soil pore water is extracted. The other end is attached to a 5-cm length of polyethylene tubing joined to a female luer lock. Two samplers were placed diagonally opposite each other from the lip of the pot to the base into each of three replicate 1.0-kg (dry wt.) pots of soil. Initially, the soil was made up to 50% water holding capacity (WHC) with deionized water, and two weeks prior to extraction, to 75% WHC. Acid-washed disposable syringes, attached to the luer lock, were used to extract pore water from the soil. Free Zn²⁺ and Cd²⁺ concentrations in soil pore water were determined using a calcium-saturated cation exchange resin method (Holm et al., 1995). It was not possible to determine free Cu²⁺ or Ni²⁺ concentrations in soil pore water, because the method was not sufficiently sensitive to detect the small concentrations. Therefore, soil pore water soluble Cu and Ni concentrations are reported instead.

Wheat Grain Chemical Analysis
The wheat was hand-harvested from the plots at Rosemaund in each respective year, and whole grain samples were milled into flour (<150 µm). Representative subsamples were dried at 80°C for 12 h, before digesting with concentrated HNO₃ acid (15.8 M) (Aristar, BDH/Merck Eurolab, Poole, England). Grain Cd was determined by GF–AAS. Ten percent of the samples from each year were analyzed in duplicate. The reliability of the digestion and analytical procedure was tested by including blanks and two National Institute of Standards and Technology (1988) standard wheat flour (SRM 1567a) samples with every batch of 50 sample digests.

Data Analysis
Wheat grain Cd concentration was expressed on a dry-weight basis. Genstat 5 (1987) was used for all statistical procedures. General linear regression analysis was used to determine relationships between grain Cd and total soil Cd, soil pore water soluble Cd, and free Cd²⁺.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 
Soil Chemical Analysis
The site was sampled 31 yr after the single sludge addition; the percent C, percent N, C to N ratio, and DOC in all plots were similar (Tables 2 and 3). Soil and soil pore water pHs ranged from 6.3 to 6.8 and from 6.8 to 7.4, respectively, with plots receiving Cr-sludge, and hence Cd, having the highest values. The concentrations of metal oxides were of the same order of magnitude in all plots of the experiment (Table 2).

As expected on a single soil type, soil pore water soluble Cd and free Cd²⁺ increased linearly with increasing total soil Cd (R² = 0.82 and 0.84, respectively; P < 0.001; Fig. 1a,b) across the range of soil Cd concentrations studied. Processes such as adsorption, desorption, and chelation will have resulted in some attenuation by the soil of the available Cd fraction in soil pore water over the past 30 yr, but since no measurements were made in the years immediately following the single sludge application in 1968, we cannot determine the extent of this. Nevertheless, in 1999 when this study was carried out, there was a substantial available Cd fraction in soil pore water some 30 yr after the single sludge addition. Similarly, Hamon et al. (1999) reported a linear increase in soil solution metal concentrations with increasing soil metal concentrations, with no plateau, in plots of a long-term field experiment where sludge addition had ceased some 35 yr previously. In selected archived soil samples from the same field experiment, spanning over 23 yr after sludge addition had ceased, Cd and Zn extractability was found to neither decrease nor increase (McGrath et al., 2000).

View larger version (24K): [in this window] [in a new window]   Fig. 1. Relationship between total soil Cd and (a) soil pore water soluble Cd and (b) soil pore water free Cd2+. (c) Relationship between soil pore water soluble Cd and soil pore water free Cd2+. Treatments: no-sludge control, uncontaminated control sludge, Zn-sludge, Cu-sludge, Ni-sludge, Cr-sludge.

Wheat Grain Cadmium
Ten replicate SRM 1567a wheat flour samples were included with the analysis of wheat grain samples from 1994 and 1996. The Cd concentration of the SRM wheat flour ranged from 0.024 to 0.027 mg kg^-1, with a mean of 0.025 mg kg^-1 (coefficient of variation [CV] 4.6%), and 0.025 to 0.028 mg kg^-1, with a mean of 0.026 mg kg^-1 (CV 4%), respectively. Five replicate SRM 1567a wheat flour samples were included with the analysis of wheat grain samples from 1999, and the Cd was found to range from 0.025 to 0.028 mg kg^-1, with a mean of 0.027 mg kg^-1 (CV 5.2%). The certified SRM 1567a wheat flour value for Cd is 0.026 ± 0.002 mg kg^-1 (±95% confidence limit). The digestion procedure used for the wheat grain samples, and the GF–AAS analysis of the Cd, therefore, gave reliable and reproducible results for the NIST standard wheat flour (SRM 1567a).

Grain Cd concentrations in 1994, 1996, and 1999 were significantly correlated with total soil Cd (R² = 0.90, 0.87, and 0.85, respectively; P < 0.001), and soil pore water soluble Cd (R² = 0.80, 0.79, and 0.79, respectively; P < 0.001) and free Cd²⁺ (R² = 0.81, 0.79, and 0.79, respectively; P < 0.001) (Fig. 2a,b,c). Grain Cd concentrations were highest in soils treated with the Cr-sludge contaminated with Cd. A slight curvilinear relationship between grain Cd and soil Cd and grain Cd and soil pore water free Cd²⁺ was apparent, but there were no clear plateaus within the range of soil Cd and soil pore water free Cd²⁺ concentrations in our study (Fig. 2a,c). The relationship between soil pore water Cd and grain Cd for all three cultivars was linear (Fig. 2b). The slopes and intercepts of the fitted curves within each graph were significantly (P < 0.001) different to each other confirming seasonal and/or cultivar variation in grain Cd content (Fig. 2a,b,c). The slope of the curves were in the order 1994 > 1996 > 1999, with more Cd being taken up into the grain by the cultivar Soissons grown in 1994, and least by the cultivar Hereward grown in 1999. No dilution of the Cd concentration in grain by increased yields was apparent within each year or between years. For example, for every year the Cr-sludge (Cd contaminated) treated plots gave the highest yields (data not shown), but also the highest concentrations of Cd in grain. There was little difference in yields between 1994 and 1996, but the yields for 1999 were lower than both the former years. However, there was no increase in grain Cd concentration in 1999 over that found in 1994 and 1996. In fact, the grain Cd concentrations were lower in 1999 compared with 1994 and 1996 (Fig. 2). Both seasonal and varietal differences are important factors in the uptake of Cd by crops (Grant et al., 1998). The experimental design over the three years studied does not allow the intrinsic seasonal and/or cultivar variations to be separated. However, it is important to note that in all three years and for all three cultivars, Cd accumulation in the grain up to the German limit of 0.1 mg kg^-1 fresh wt. (equivalent to 0.12 mg kg^-1 dry wt.) and above occurred at soil Cd concentrations less than the current UK limit of 3 mg kg^-1 for soils receiving sewage sludge. The EU limit for bran, germ, and wheat grain has been set at 0.2 mg Cd kg^-1 fresh wt. In our study, whole grain samples were finely ground to produce wholemeal flour, which was then dried and analyzed for Cd. Assuming the dry matter content to be 85%, the effective EU limit for dried wholemeal flour would be about 0.24 mg Cd kg^-1 dry wt. Even so, the grain Cd in 1994 for Soissons would exceed this calculated EU limit at total soil Cd concentrations less than 3 mg kg^-1 soil. For Brigadier grown in 1996 and Hereward grown in 1999, the grain Cd content would be near and less than the EU limit, respectively, even at the highest soil Cd concentration of 2.7 mg kg^-1.

View larger version (33K): [in this window] [in a new window]   Fig. 2. Relationship between (a) total soil Cd and wheat grain Cd, (b) soil pore water soluble Cd and wheat grain Cd, and (c) soil pore water free Cd2+ and wheat grain Cd. 1994, cv. Soisson; 1996, cv. Brigadier; 1999, cv. Hereward. Equations: (a) 1994, y = 0.02 + 0.195x - 0.033x2; 1996, y = 0.025 + 0.104x - 0.013x2; 1999, y = 0.018 + 0.073x - 0.0094x2. (b) 1994, y = 0.076x + 0.071; 1996, y = 0.049x + 0.048; 1999, y = 0.035x + 0.034. (c) 1994, y = 0.0696 + 0.096x - 0.0048x2; 1996, y = 0.049 + 0.056x - 0.0017x2; 1999, y = 0.035 + 0.0395x - 0.00067x2.

	CONCLUSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 
It is important when adding sludges to agricultural soils used for food production to consider both the immediate and long-term fate of any potentially toxic elements that may be introduced into the soil. At present there is very little evidence from field experiments with sludge that can be used to determine what soil concentrations would limit grain production due to new food quality regulations. In our study, based on total soil Cd, grain quality criteria were exceeded when soils contained less than the current UK limit of 3 mg Cd kg^-1. The Cr-sludge used at Luddington some 30 yr ago contained appreciable amounts of Cd. However, sludges presently produced in the UK are generally very low in Cd and may be used on agricultural land without limiting land use and/or cropping regimes for significant periods of time (Alloway et al., 1999; Gendebien et al., 1999). However, whether smaller additions of cleaner sludges over longer periods would reduce the risk of potentially toxic elements accumulating in edible plant parts has, as yet, to be determined experimentally.

In our study, soluble Cd gave a more linear relationship with grain Cd than with total soil Cd. Soluble and free Cd²⁺ were also highly correlated, as the samples were from the same soil type. Some crops may take up larger concentrations of metals into their edible parts at relatively low total soil exposure levels. In addition, there were clear seasonal and/or cultivar effects on grain Cd content, highlighting the multifactor influence on Cd content, and therefore the difficulty in trying to determine soil Cd concentrations that could affect food quality.

	ACKNOWLEDGMENTS

 
This work was supported by the United Kingdom Ministry of Agriculture, Fisheries and Food and the United Kingdom Home-Grown Cereals Authority. IACR-Rothamsted also receives grant-aided support from the UK Biotechnology and Biological Sciences Research Council. S.H. Badawy would like to thank the IAEA, Vienna for providing financial support (Project no. EGY/8/013), and the British Council for assistance during his stay at IACR-Rothamsted.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION CONCLUSION REFERENCES

 

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