Toxicology Mechanisms and Methods, 12:265-276,2002Copyright © 2002 Taylor & Francis1537 -6524/02 $12.00 + .00DOl: 10.1080/10517230290075459

~. Taylor&Francis• healthsciences

CADMIUM UPTAKE BY RADISHES FROM SOILCONTAMINATED WITH NICKEL-CADMIUM BATTERIES:

TOXICITY AND SAFETY CONSIDERATIONS

James Dorris and Bassam H. AtiehDepartment of Occupational Safety and Health, Murray State University, Murray, Kentucky, USA

Ramesh C. GuptaMurray State University, Toxicology Department, Breathitt Veterinary Center, Hopkinsville,

Kentucky; USA

The objective of this investigation was twofold: (1) to determine the contami­nation of soil by cadmium (Cd) from commonly used nickel-cadmium (Ni-Cd)batteries utilized in electronic devices and (2) to determine the uptake of Cd in.common garden radishes. Under normal controlled conditions, the study uti­lized depleted batteries; new, undamaged batteries; and new, damaged batter­ies. The data revealed that the contamination ofthe soil by Cd was significantlygreater in the presence ofnew, damaged batteries than in the presence ofthe new;undamaged batteries or depleted batteries. In another set ofexperiments, the up-.take ofCd was determined in radishes grown in the control soil as well as in theCd-contaminated soil. The findings revealed that Cd uptake was significantlygreater by the leafand stem grown in the soil contaminated with new, damaged'batteries. These results indicate that improper disposal ofNi-Cd batteries con­taminates the soil and leads to enhanced Cd levels in garden vegetables, whichcan pose a serious threat to human health.

Keywords cadmium, cadmium contamination, cadmium food safety

Currently, contamination of the environment by metals is of paramountconcern from the point of view of public health safety. Cadmium (Cd) is awidely but sparsely distributed element that is found in the earth's crustat concentrations ranging from 0.1 to 1 ppm (Elinder 1985). Cd occurs asa byproduct in the mining and smelting of zinc and lead. Cd has manyuses in industry and consumer products, such as in electroplating or gal­vanizing processes, batteries, pigments, dyes, metal coatings, plastics,

Received 1 February 2002; accepted 15 June 2002.Presented in part at the Annual Meeting of the Semiconductors Safety Association, April 10,

2001, New Orleans, LA.The authors thank the Semiconductor Safety Association and the Dean, Dr. Betty Blodgett, for

their encouragement and support; Dr. Harry Fannin for analyzing the data; and Mrs. Debra M.Britton and Mrs. Robin B. Doss for their assistance in the preparation of this manuscript.

Address correspondence to Dr. Ramesh C. Gupta, Murray State University; Toxicology Depart­ment, Breathitt Veterinary Center, P.O. Box 2000, Hopkinsville, KY 42240-2000, USA. E-mail:ramesh.gupta®murraystate.edu

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266 J. Dorris et al.

metal alloys, fungicides, and fertilizers, but 70% of the Cd used goes'into cathode material for nickel-cadmium (Ni-Cd) batteries (ATSDR1999; WHO 1992). Therefore, improper disposal of Ni-Cd batteries inmunicipal and industrial treatment plants, disposal sites, and wasteincineration facilities presents a potential source of environmental con­tamination. The average level of Cd in unpolluted soil is about 250 ppb.At hazardous waste sites, Cd levels have been measured in the soil atabout 4 ppm and in water at 6 ppm (ATSDR 1999). Cd has been found insignificant amounts in at least 776 of the 1467 National Priorities List(NPL) sites targeted for a long-term federal cleanup.

Uptake of heavy metals by plants and vegetables grown in pollutedland has been one of the principal focuses of environmental researchsince the outbreak of itai-itai disease (Goyer and Clarkson 2001; Nanand Cheng 2001; Yamagata and Shigematsu 1970). Contamination ofthe agricultural environment by trace metals has now become a growingconcern worldwide because of unsafe levels of trace metals in the foodchain. The general population and people living near hazardous wastesites may be exposed to Cd from contaminated food, dust, or water fromunregulated releases or accidental releases. Currently, each year morethan 512,000 workers in the United States are placed in environmentsin which Cd exposure may occur (ATSDR 1999). Total daily intake of Cdfrom food, water, and air in North America is estimated to be about 10to 40 p.,g Cd per day, and average Cd levels in U.S. foods range from 2to 40 ppb (ATSDR 1999). Eating food or drinking water with very highCd levels for a short period can severely irritate the stomach, leading tovomiting, diarrhea, and sometimes death. Exposure to Cd at lower levelsover a long period of time can lead to a buildup of .Cd in the kidneys,causing structural and functional damage. If levels are high enough,Cd in the liver and kidneys causes damage and may also cause bones tobecome fragile and weak (Brzoska and Moniuszko-Jakoniuk 1998; Wangand Bhattacharyya 1993). For details of the toxicological effects of Cd,refer to the reviews by Friberg and colleagues (1986), WHO (1992), EPA(1997), and ATSDR (1999). The International Agency for Research onCancer (IARC) has also determined that Cd is carcinogenic to humans(IARC 1993), as Cd exposure has been associated with cancer of thebreast, lung, large intestine, and urinary bladder (Newberne 19·87).

The present investigation was undertaken with two specific objec­tives: (1) to determine Cd contamination in soil resulting from Ni-Cdbatteries utilized in electronic devices and (2) to determine the uptakeof Cd in radishes grown in contaminated soil. The findings gatheredfrom these experiments has also allowed us to determine whether veg­etables such as radishes grown in Cd-contaminated soils are safe forhuman consumption.

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Cadmium Contamination

MATERIALS AND METHODS

267

This investigation was conducted in two sets of experiments, with fourgroups in each set. In Set I, experiments were conducted to determinethe contamination of soil by Cd from Ni-Cd batteries. In Group I (thecontrol), three 5-gallon containers held topsoil but no batteries of anykind. In Group II, each of three 5-galloll containers held three depletedAA batteries that had been placed in the middle of the pot, 4 inchesbelow the surface of the topsoil. Similarly, in Groups III and I~ eachcontainer held topsoil and three new, undamaged batteries or three new,damaged batteries, respectively. (It is important to mention that the de­pleted batteries used in Group II were comparable to the batteries usedin Groups III and IV) The product labels indicated that each batterycontained 26% cadmium (Cd) and 26% cadmium hydroxide [Cd(OH)21.In Set II, four radish plants taken from the same batch and having ap­proximately the same physical condition were planted in each of thefour containers at the same time the batteries were placed in the soil.At the time of planting, the root length of each radish plant was about 1inch, and the batteries were about 3 inches below the roots so as to avoidany direct contact, because Cd at higher concentrations is phytotoxic.All containers were attended daily to ensure proper soil moisture, anda 12-h light/dark cycle was maintained for the entire 45-day durationof the experiment. Soil samples were collected on the 15th, 30th, and45th days of the experiment. The pulp samples were collected on the30th and 45th days of the experiment. The stem and leaf samples werecollected on the very last day, the 45th day. All samples were prepared',digested, and quantitatively analyzed for Cd using an atomic absorptionspectrometer coupled with a graphite furnace.

Sample Collection

The samples were collected at three different times. After the first in­terval, 15 days, soil samples were collected from the control and experi­mental groups. After the second interval, 30 days, soil and pulp sampleswere collected. After the final interval, 45 days after the experiment wasbegun, samples of soil, pulp, stem, and leaf were collected. For each ofthe collections, sterile tools and sterile glass containers with polypropy­lene caps were used to collect and store the samples so as to avoid anycontamination by Cd.

Sample Preparation

After collection, the samples were oven-dried for 2 to 3 days at gOoe.The oven was cleaned prior to each dehydration to prevent any

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268 J. Dorris et al.

cross-contamination. After the samples were dried, they were trans-'ferred into a desiccator to prevent their rehydration. Prior to digestion,the samples were ground into a fine powder in a glass mortar, returnedto their original containers, and placed back into the desiccator. All pos­sible measures were taken to avoid any cross-contamination.

Sample Digestion

Approximately 1 g of sample was weighed and transferred into aTeflon bomb liner (Parr, Moline, IL). In the case of the plant samples,2.5 mL of trace-metal-grade, concentrated nitric acid (Fisher Scientific,Pittsburgh, PA) was added to the liner. To the soil samples, 2.4 ml, nitricacid was added, followed by 0.2 mL of concentrated (48%).hydrofluoricacid (GFS Chemicals, Columbus, OR). The liners were placed in a bomb(Parr, Moline, IL) and microwaved for 30 s on high power. The bombswere removed and allowed to cool for 30 min; then the contents of theliners were quantitatively transferred to a 10-mL volumetric flask anddiluted to volume. The contents of the flask were transferred into a dry;clean (acid-rinsed) 100 mL size bottle prior to analysis.

Sample Analysis

A standard curve of Cd was prepared by serial dilution of a 1000-ppmstandard (HPS, Charleston, Se) at concentrations of 0, o.i, 0.4, and1 ppb. The acid content of the standards was adjusted with trace-metal­grade nitric acid to match the samples, and the standards were broughtto the required volume with deionized water. The Cd concentrations inthe standard and the samples were determined using an atomic absorp­tion spectrometer coupled with a graphite furnace (Perkin-Elmer, model5100 Zeeman, Norwalk, CT). The absorbance was measured using a Cdlamp at 228.8 nm, with a slit ofO.7. The instrument detection limit basedon 30" was determined to be 0.04 ppb. The analytical conditions for Cd as­say are standard and have been reported in detail elsewhere (Demirozu­Erdinc and Saldamli 2001). A predigested sample spiked with 2 ppb Cdshowed a recovery of 88%.

Statistical Analysis

The concentrations of Cd in soil and radishes were determined in termsofppb and expressed as mean ± SEM. Data were analyzed using anal­ysisofvariance coupled with the Tukey-Kramer multicomparison test.Differences of p <' .05 were considered statistically significant.

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Cadmium Contamination

RESULTS AND DISCUSSION

269

This investigation was conducted with two major objectives in mind:(1) to determine the soil contamination by Cd from Ni-Cd batteries and(2) to determine the uptake of Cd by radishes. The data concerning theCd content in the soil and radishes (pulp, stem, and leaf) are presentedin Figures 1,2, and 3. The findings revealed that the Cd concentrationin the soil was significantly higher in the presence of new, damagedbatteries than in controls or in the presence' of depleted batteries ornew, undamaged batteries (see Fig. 1). The value was about three timesgreater than that in the soil holding no batteries and about twice the re­ported value of unpolluted U.S. soil (ATSDR 1999). Results also revealedthat after 45 days, the Cd level was significantly higher in the soil hold­ing new, undamaged batteries than in the soil holding no batteries ordepleted batteries, probably due to some leakage of Cd. The finding thatat 45 days, soil holding new, damaged batteries had a higher Cd levelthan it had at 30 days was unexpected.

CADMIUM IN SOIL

IJNo Battery lSIDepleted Batteries EJ New Undamaged Batteries I!lNew Damaged Batt~rieS I400

a,b

350

300

:Q 250Q.

~cjc8·200E~

E-c~ 150

100

50

o .15 DAYS 30 DAYS 45 DAYS

FIGURE 1. Cd concentrations in soil (ppb). Values are means ± SEM (n = 3). a, significant differ­ence between Cd values in soil holding no batteries (control) and soil holding batteries (p < .05);b, significant difference between Cd values in soil holding new, damaged batteries and soil holdingdepleted or new, undamaged batteries (p < .05).

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21New Damaged Batteries

270 J. Dorris et al.

CADMIUM IN RADISH PULP

~~o Battery lSIDepleted Batteries EI New Undamaged BatteriesL- , ' __~---_----l

250 ..,---------------

200 ~

:c! 150(.)co<J

E:J

~ 100too

50

o30 DAYS 45 DAYS

FIGURE 2. Cd concentrations in radish pulp (ppb). Values are means ± SEM (n = 3). a significantdifference between Cd values in pulp of radishes grown in soil holding no batteries (control) andsoil holding batteries (p < .05).,

It has been reported that 90% of the Cd in soils ,remains in the top6 inches (FAO 1994). The mobility of Cd in soilscan be influenced byvarious factors, including pH, oxidation-reduction reactions, and forma­tion of complexes (Bermond and Bourgeois 1992; Callahan et al. 1979;Elinder 1985; Herrero and Martin 1993; Roy et al. 1993). The Cd metalitself does not break down in the environment, but it can change intodifferent forms. The transformation processes of Cd in soil are mediatedby sorption to water, and include precipitation, dissolution, complexa­tion, and ion exchange. Important factors affectingtransformation insoil include the cation exchange capacity, the pH, and the content ofclay minerals, carbonate minerals, oxides, organic matter, and oxygen(McColllish and Ong 1988). Examples of Cd compounds found in soilare cadmium phosphate [Cd3(P04)2], cadmium carbonate (CdC03 ) , andcadmium hydroxide Cd(OH)2 (Herrero and Martin 1993). These com­P9~ndE.?·are formed as the pH rises. It is documented that Cd 'exists inmany-forms and that some forms are more toxic than others. For ex­~~~l~'t'the relatively more soluble cadmium chloride (CdClz), cadmium

:;f~:-:g~*g~:'{OdO),and CdC03 are more toxic than the relatively less soluble'

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Cadmium Contamination

CADMIUM IN LEAF & STEM

271

CNo Battery SfDepleted Batteries EINew Undamaged Batteries EINew Damaged Batteries

1000

900

800

700

::0C- 600.8:t.ic0 500 -0

E:3

'E400"C

l'G0

300 -

200

100

0

a.b

45 DAYS

FIGURE 3. Cd concentrations in radish leaf and stem (ppb). Values are means ± SEMen = 3).a, significant difference between Cd values in leaf and stem of radishes grown in soil holding nobatteries (control) and soil holding batteries (p < .05). b, significant difference between Cd valuesin leaf and stem of radishes grown in soil holding new, damaged batteries and soil holding depletedor new,undamaged batteries (p < .05).

cadmium sulfide (CdS) (Klimisch 1993). Therefore, it appears that Cdmay change forms in the soil, and that appears to be an important factorin determining the risk of potential adverse health effects. It should benoted that Cd does not disappear from the environment.

Contamination of soil by Cd is of major concern because Cd is takenup efficiently by plants and, therefore, enters the food chain of humansand animals. Low soil pH, which is becoming prevalent in many areas ofthe world due to acid rain, increases the uptake of Cd by plants (Elinder1992). The findings that radish pulp grown in soil with no batterieshad a higher Cd level at 45 days than it had had at 30 days could beexplained by the occurrence of some contamination from the soil (seeFig. 2). The uptake of Cd by radishes was significantly greater in thepresence of new; damaged batteries. This finding could be explained bythe higher Cd content in new batteries and its leakage due to physicaldamage, which allowed more Cd to leak into the soil and thus be avail­able for increased uptake by the radishes. Furthermore, Cd uptake wassignificantly greater in the stem and leaf than in the pulp, suggesting a

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272 J. Dorris et ale

differential distribution of Cd within the plant. In fact, the Cd concen- 'tration in the leaf and stem was directly proportional to the amount ofCd in the soil, which was dependent upon the physical condition of thebatteries. It is well established that Cd bioaccumulates at all levels ofthe food chain. The metal burden of plants depends on uptake by theroot system, direct foliar uptake and translocation within the plant, andsurface deposition of particulate matter (Nwosu et a1. 1995). It has beensuggested that leafy vegetables, such as spinach and lettuce, containgreater amounts of Cd than do root vegetables, such as potatoes andonions (FAD 1994). These data, along with those reported by Demirozu­Erdinc and Saldamli (2001), supported our finding of greater Cd con­centration in the stem and leaf than in the pulp (see Figs. 2 and 3). Theobserved low Cd content in the pulp could be due to a washout effect. Itappears that Cd translocates into the parts of a plant that have a higherwater content. In general, Cd accumulates in the leaves of plants and,therefore, is more of a risk in leafy vegetables grown in contaminatedsoil than in seed and root crops (Alloway et a1. 1990; He and Singh 1994).Nwosu et a1. (1995) demonstrated that Cd is translocated freely in thesoil and taken up in plants by means of passive diffusion. Furthermore,pH, soil type, and other properties of soil are important factors that in­fluence Cd uptake by plants (Davies 1992; He and Singh 1994; Smith1994; Thornton 1992).

During the course of this study, it was noted that the plants grownin the pot containing new, damaged batteries were in poor conditioncompared to the control, suggesting the phytotoxic effects of Cd, as wellas those of Ni, which may have been released simultaneously, Thesefindings were in agreement with those reported earlier-that Cd andNi are known to cause phytotoxicity (Barmen et ale 2000; Palacioset al,1999; Peles et a11996; Ramachandran and D'Souza 1998).

There has been increased interest in the health effects of Cd, as itis a ubiquitous environmental contaminant (Conrad et a1. 1997). Cd ispresent in almost everything we eat and drink and frequently in theair we breathe. As a result, Cd is considered one of the most dangerousoccupational and environmental poisons. Earlier studies documentedthat in the general population, Cd exposure takes place primarily viarespiration, for example, in cigarette smoke (Commission of EuropeanCommunities 1978; Elinder et al. 1983). However, several reports doc­ument the transfer of potentially toxic elements from soils to plants(Barmen et ale 2000; Chen 1996; Nan and Cheng 2001; Nwosu et ale 1995;Peles et al. 1996; Ramachandran and D'Souza 1998; Schumacher et a1.1994; Wenzel and Jockwer 1999), suggesting food as the main source ofexposure to Cd. These reports, along with others, revealed that in con­trast to other toxic heavy metals, Cd is easily transported from soil toplants and can be greatly concentrated in the food chain (ATSDR 1999;'

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Cadmium Contamination 273

Demirozu-Erdinc and Saldamli 2001; IPCS 1992; Pahren et al. 1979).Demirozu-Erdinc and Saldamli (2001) reported that vegetables are par­ticularly important sources of Cd, as well as of lead and arsenic (Dunnickand Fowler 1988; Robards and Worsfold 1991).

It is well documented that gastrointestinal absorption of Cd is about5 to 8%. Both human and animal studies have revealed that this rate ofCd absorption could be enhanced by dietary deficiencies of calcium, iron,and protein in adults as well as in children and young animals (Goyerand Clarkson 2001). After absorption, Cd accumulates particularly inthe kidney and liver, and it has a biological half-life of 7 to 30 years(Kjellsrom and Nordberg 1985; Shaikh et al. 1999). The leaves and stemsof radishes grown in the soil holding new damaged batteries containedmore than 900 ppb Cd (see Fig. 3). This level is about 45 times greaterthan the average level of Cd present in American foods, which rangesfrom 2 to 40 ppb (ATSDR 1999). Therefore, the Cd level found in theradishes might not be enough to cause acute renal failure, but prolongeddaily exposure may result in chronic kidney damage, as Cd is known toaccumulate in the kidney (Klimisch 1993; Kotsonis and Klaassen 1978)..

Chronic exposure to low doses of Cd is known to cause nephrotoxi­city and hepatotoxicity, and acute exposure to large doses can result indamage to numerous tissues (Bagchi et al. 1996; Dudley et ale 1985;Friberg 1984; Rana and Verma 1996; Sarkar et al. 1995; Webb andCaine 1982). Several studies have demonstrated that Cd also has the.potential to cause neurotoxicity (Andersson et al. 1997), reproductivetoxicity (Sorell and Graziano 1990; Yu et al. 1985), embryotoxicityandfetotoxicity (Fein et ale 1997; Levin and Miller 1981), placental toxicity(diSant' Agnese et al. 1983; Gupta and Sastry 2000), teratogenicity (P~

et al. 1990, 1993; Webster 1990), and carcinogenicity (Gunn et al. 1963;'Haddow et al. 1964; Takenaka et al. 1983; Waalkes et al. 1988). There isdefinitive evidence that Cd is a human carcinogen, as Cd exposure hasbeen well associated with cancer of the breast, lung, large intestine, and.urinary bladder (IARC 1993; Newberne 1987).

Internationally, the risk of exposure to Cd emanates primarily fromeffects on occupationally exposed adults. The current provisional tol­erance weekly intake set by the Joint FAOIWHO Expert Committee on.Food Additives is 7 J-Lg/kg body weight (WHO 1993). In the United States,adult intake of Cd in food has been estimated to be about 10 to 50 J-Lg/day,based on the Total Diet Study, with the largest contribution coming fromvegetables, grains, and cereal products (Gartrell et al. 1986; Goyer andClarkson 2001; Klaassen 2001).

Our results indicate that improper disposal of Ni-Cd batteries cancontaminate soil with Cd to the extent that garden vegetables such asradishes can uptake significant amounts of Cd, posing serious adversehealth effects in humans.

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