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Accumulation and health risk of heavy metals in a plot-scale vegetable production system in a peri-urban vegetable farm near Nanjing, China Wenyou Hu a , Biao Huang a,n , Xuezheng Shi b , Weiping Chen c , Yongcun Zhao a , Wentao Jiao c a Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China b State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China c State Key Laboratory of Urban and Regional Ecology Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China article info Article history: Received 9 July 2013 Received in revised form 27 September 2013 Accepted 30 September 2013 Available online 24 October 2013 Keywords: Heavy metal balance Vegetable production system Soils Mass balance model Hazard quotient abstract Accumulation and potential health risk of cadmium (Cd), lead (Pb), copper (Cu), and zinc (Zn) in a plot-scale vegetable production peri-urban area near Nanjing city, China was investigated through element balance method, model simulation and dietary risk assessment. The heavy metals accumulated in the surface soils were due to long-term and heavy application of organic fertilizers, among which the accumulation of Cu and Zn were greater than those of Cd and Pb. The result of a mass balance model simulation indicated that intensive vegetable production would result in accumulation of Cd, Pb, Cu and Zn in soils exceeding the target values in 55, 36, 34 and 71 years, respectively. The estimated dietary intakes of Cd, Pb, Cu, and Zn were far below the tolerable limits and the hazard quotient values were below one for both children and adults. Although there is no imminent health risk from heavy metals through vegetable consumption, more attention should be paid to the long-term accumulation and risk, especially for children. & 2013 Elsevier Inc. All rights reserved. 1. Introduction The analysis of input and output uxes of heavy metals such as cadmium (Cd), lead (Pb), copper (Cu) and zinc (Zn), and their long- term accumulation in agricultural soils is necessary to develop strategies for sustainable management of these metals in agricultural systems (Moolenaar and Lexmond, 1999). Heavy metal balance method provides a source-oriented way for monitoring soil quality (Dach and Starmans, 2005; Kong and Ni, 2006; Moolenaar and Lexmond, 1999; Moolenaar and Beltrami, 1998). Conventional soil survey assesses existing pollution situation, it cannot predict the future occurrence (Keller et al., 2001). The common pathways of heavy metal input into agricultural soils include atmospheric deposition, applica- tion of commercial or organic fertilizers and irrigation water, and accumulation rate of heavy metals through those pathways is rather slow. Hence, it may take decades to detect the accumulation trends by repeatedly sampling soils. On the other hand, mass balance approach uses the input at the soil surface and the output through crop harvest, leaching and surface runoff to determine heavy metal accumulation in soil. In a certain scale, this method may be more effective to predict heavy metal accumulation trends and develop strategies for sustain- able management of agricultural soils. Vegetables are an important source of human diet due to their containing many kinds of proteins, carbohydrates, vitamins and minerals. As vegetables can be grown in small-scale or plot-scale elds within a short period of time, the production of fresh vegetables in peri-urban areas is a common practice in many developing countries (Sharma et al., 2007; Singh et al., 2012). In China, peri-urban vegetable farms are mainly small-scale family businesses, commonly accompanied with high input of organic fertilizers and other agrochemicals over year round (Huang et al., 2006). This common operational pattern has caused some concerns about potential contamination of heavy metals in soils and vegeta- bles as well as their impact on human health (John and Kakulu, 2012; Singh et al., 2012; Wang et al., 2012a, 2012b). As vegetables acquire necessary nutrients, such as nitrogen, phosphorus and potassium, they also accumulate metals such as Cd and Pb (Cobb et al., 2000), which may result in adverse health effect on human beings due to excessive dietary intake of those vegetables (Hough et al., 2004; Oliver, 1997). Although Cu and Zn are essential elements, excessive concentration in food can be of a great concern because of their toxicity to humans (Kabata-Pendias and Mukherjee, 2007; Xu et al., 2013). Thus, it is important to understand heavy metal status in vegetables obtained from peri-urban areas and the potential health risk. The objectives of this study are to (1) analyze the input and output uxes of Cd, Pb, Cu and Zn and their balances in plot-scale vegetable production system in selected a peri-urban area near Nanjing in China; (2) evaluate the long-term accumulation Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/ecoenv Ecotoxicology and Environmental Safety 0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ecoenv.2013.09.040 n Corresponding author. Fax: þ86 25 86881000. E-mail address: [email protected] (B. Huang). Ecotoxicology and Environmental Safety 98 (2013) 303309

Accumulation and health risk of heavy metals in a plot-scale vegetable production system in a peri-urban vegetable farm near Nanjing, China

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  • Accumulation and health risk of heavy metals in a plot-scale vegetableproduction system in a peri-urban vegetable farm near Nanjing, China

    Wenyou Hu a, Biao Huang a,n, Xuezheng Shi b, Weiping Chen c, Yongcun Zhao a,Wentao Jiao c

    a Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, Chinab State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, Chinac State Key Laboratory of Urban and Regional Ecology Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China

    a r t i c l e i n f o

    Article history:Received 9 July 2013Received in revised form27 September 2013Accepted 30 September 2013Available online 24 October 2013

    Keywords:Heavy metal balanceVegetable production systemSoilsMass balance modelHazard quotient

    a b s t r a c t

    Accumulation and potential health risk of cadmium (Cd), lead (Pb), copper (Cu), and zinc (Zn) in a plot-scalevegetable production peri-urban area near Nanjing city, China was investigated through element balancemethod, model simulation and dietary risk assessment. The heavy metals accumulated in the surface soilswere due to long-term and heavy application of organic fertilizers, among which the accumulation of Cu andZn were greater than those of Cd and Pb. The result of a mass balance model simulation indicated thatintensive vegetable production would result in accumulation of Cd, Pb, Cu and Zn in soils exceeding thetarget values in 55, 36, 34 and 71 years, respectively. The estimated dietary intakes of Cd, Pb, Cu, and Znwerefar below the tolerable limits and the hazard quotient values were below one for both children and adults.Although there is no imminent health risk from heavy metals through vegetable consumption, moreattention should be paid to the long-term accumulation and risk, especially for children.

    & 2013 Elsevier Inc. All rights reserved.

    1. Introduction

    The analysis of input and output uxes of heavy metals such ascadmium (Cd), lead (Pb), copper (Cu) and zinc (Zn), and their long-term accumulation in agricultural soils is necessary to developstrategies for sustainable management of these metals in agriculturalsystems (Moolenaar and Lexmond, 1999). Heavy metal balancemethod provides a source-oriented way for monitoring soil quality(Dach and Starmans, 2005; Kong and Ni, 2006; Moolenaar andLexmond, 1999; Moolenaar and Beltrami, 1998). Conventional soilsurvey assesses existing pollution situation, it cannot predict the futureoccurrence (Keller et al., 2001). The common pathways of heavy metalinput into agricultural soils include atmospheric deposition, applica-tion of commercial or organic fertilizers and irrigation water, andaccumulation rate of heavy metals through those pathways is ratherslow. Hence, it may take decades to detect the accumulation trends byrepeatedly sampling soils. On the other hand, mass balance approachuses the input at the soil surface and the output through crop harvest,leaching and surface runoff to determine heavy metal accumulation insoil. In a certain scale, this method may be more effective to predictheavy metal accumulation trends and develop strategies for sustain-able management of agricultural soils.

    Vegetables are an important source of human diet due to theircontaining many kinds of proteins, carbohydrates, vitamins andminerals. As vegetables can be grown in small-scale or plot-scaleelds within a short period of time, the production of freshvegetables in peri-urban areas is a common practice in manydeveloping countries (Sharma et al., 2007; Singh et al., 2012).In China, peri-urban vegetable farms are mainly small-scale familybusinesses, commonly accompanied with high input of organicfertilizers and other agrochemicals over year round (Huang et al.,2006). This common operational pattern has caused some concernsabout potential contamination of heavy metals in soils and vegeta-bles as well as their impact on human health (John and Kakulu, 2012;Singh et al., 2012; Wang et al., 2012a, 2012b). As vegetables acquirenecessary nutrients, such as nitrogen, phosphorus and potassium,they also accumulate metals such as Cd and Pb (Cobb et al., 2000),which may result in adverse health effect on human beings due toexcessive dietary intake of those vegetables (Hough et al., 2004;Oliver, 1997). Although Cu and Zn are essential elements, excessiveconcentration in food can be of a great concern because of theirtoxicity to humans (Kabata-Pendias and Mukherjee, 2007; Xu et al.,2013). Thus, it is important to understand heavy metal status invegetables obtained from peri-urban areas and the potentialhealth risk.

    The objectives of this study are to (1) analyze the input andoutput uxes of Cd, Pb, Cu and Zn and their balances in plot-scalevegetable production system in selected a peri-urban area nearNanjing in China; (2) evaluate the long-term accumulation

    Contents lists available at ScienceDirect

    journal homepage: www.elsevier.com/locate/ecoenv

    Ecotoxicology and Environmental Safety

    0147-6513/$ - see front matter & 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ecoenv.2013.09.040

    n Corresponding author. Fax: 86 25 86881000.E-mail address: [email protected] (B. Huang).

    Ecotoxicology and Environmental Safety 98 (2013) 303309

  • potential of Cd, Pb, Cu and Zn in surface soils through a method ofmodel simulation; and (3) assess the potential health risk of Cd,Pb, Cu and Zn to the local residents through vegetable consump-tion by calculating the daily intake and hazard quotient of heavymetals.

    2. Materials and methods

    2.1. The study plots

    The study was conducted in plot-scale vegetable production system in a peri-urban area outside Nanjing (118154E, 32120N), Jiangsu province, China (Fig. 1).The study area is located 5 km east of Nanjing in a gently undulating landscapecomprised mainly of Ustic Argosols (Gong et al., 2003) with clay loam to claytexture derived from loess parent material. The area belongs to a subtropicalmonsoon climate zone with a mean annual temperature, precipitation andevaporation of about 1516 1C, 1100 mm and 1200 mm, respectively (SSONC,1984). Vegetable production was the main business in this area, and mostvegetables produced here were sold in the local urban market and consumed bylocal residents. Six vegetable plots from three households were selected formonitoring, and selection was based on local landscape, soil management history,the literacy and social economic status of the vegetable grower families. Three plots(N1, N3 and N5) were on the undulating area at the east side of the village road, andother three plots (N2, N4 and N6) were on the level area at the west side of theroad. The vegetable plots are located 4001000 m away from the major transporta-tion throughways such as Nanjing Rim highway and NanjingWuhu Railway(Fig. 1). A city moat ow in the western part of the area and villages are distributedon the undulating area to the north-west and east with sparsely distributed pondsof various sizes functioning as reservoirs of rainfall and water sources for irrigation.

    2.2. Monitoring of element balance in vegetable plots

    Element balance in the six selected vegetable plots was closely monitored fortwo vegetable production years. In the past three decades, this area was alwaysplanted with vegetables, and a large amount of organic fertilizer was used in lasttwo decades. Traditional agronomic practices were employed by utilizing moreorganic fertilizers such as cow manure, pig manure, and human feces thaninorganic fertilizers such as urea and composite fertilizer. Organic and inorganicfertilizers and irrigation water were important inputs, while vegetable productionand vegetable plant residues were major outputs. All these were quantitativelyrecorded for 2 years. Identical quantitative containers (bucket) for irrigation waterwere provided to vegetable growers for the quantication. At each harvest season,vegetables were weighed and daily revenue was also recorded for correctingpurposes. At the end of each crop season, straw and residue were collected and

    weighed. Heavy metals in atmospheric deposition, leaching or erosion wereobtained from results of the same or similar areas from the literature (Kong andNi, 2006; Ni, 2006). Heavy metal balance per hectare (ha) was then calculated foreach plot. For every season, vegetable species were chosen by vegetable growers.Table S1 shows the summary of characteristics of the vegetable plots, includingarea of the plots, application amounts of fertilizers and irrigation water, andvegetable rotation species. Input and output of heavy metals are calculatedaccording to

    Q n

    i 1MiCi 1

    where Q is amount of input or output of heavy metal; n is number of time ofagronomic practice, such as fertilizer, irrigation and vegetable harvest; M isquantity of fertilizer, irrigation and harvest vegetable; C is the content of heavymetals in fertilizer, irrigation water and vegetable. Element balance in vegetableplot is amount of input minus amount of output.

    2.3. Sampling, processing and analysis

    Samples of soils and vegetables were collected from each plot. Total 18 surfacesoil (020 cm in depth) samples were taken from six plots (three samples for eachplot) using a stainless steel trowel; each soil sample was 1 kg in weight, which wascombined ve sub-samples within an area of 55 m and then reduced to about1 kg with sample quartering in the eld. Three representative soil prole samples(ve layers of 020 cm, 2040 cm, 4060 cm, 6080 cm, and 80100 cm) were alsocollected from the vegetable plots before and after monitoring period, and from thesurrounding paddy soils, respectively. The surrounding paddy soils were selected asbackground reference soils and collected at the end of the monitoring period.All soil samples were air-dried at room temperature and sieved through 0.149 mmnylon sieve for chemical analysis. The vegetable and plant residue samplescollected at the end of harvest seasons were thoroughly washed with tap water,rinsed with de-ionized water, primarily air-dried at room temperature and thendried to constant weight in an oven at 70 1C. Dried plant tissues were ground andsieved (0.4 mm) before chemical analysis. Ten organic waste and seven chemicalfertilizer samples were collected from elds or farm households. For organicfertilizer, fresh samples were taken at 1 m depth at ve points inside the manurepile using a soil sampler, and were mixed and brought to the laboratory foranalysis. Water was sampled three times each crop season from four or ve pointsin ponds or ditches around plots using stainless steel containers. The samples werethen mixed and placed in 1-L plastic bottles, and brought to the laboratory foranalysis.

    To determine the concentrations of heavy metals in the soils and chemicalfertilizers, the samples were rst digested by reverse aqua-regia (HNO3:HCl3:1)(Huang et al., 2006), then the concentrations of Pb, Cu and Zn were determinedusing a ame atomic absorption spectrophotometer (AAS) (Varian Spectr AA 110/220) and Cd using a graphite furnace AAS. All plant tissue and manure sampleswere digested by HNO3 and HClO4, followed by measurements of Cu and Zn using

    Fig. 1. The setting of the vegetable plots in the study area.

    W. Hu et al. / Ecotoxicology and Environmental Safety 98 (2013) 303309304

  • ame AAS, Cd and Pb using graphite furnace AAS depending on the concentrationsof these metals in the samples. The concentrations of Cd, Pb, Cu and Zn in soilsolution were determined based on a soil-to-water ratio of 1:0.5 (w/v) as outlinedin Chen et al. (2007b). The soil and water mixtures were allowed to equilibrate for48 h on a reciprocating shaker (at 20 rpm). The samples were then centrifuged andthe supernatant was decanted and ltered through a 0.45 m hydrophilic PVDFmembrane lter.

    2.4. Assessing long-term accumulation of heavy metals using model approach

    A generalized trace element mass balance model (STEM-single layer model)was used to evaluate the long-term accumulation of Cd, Pb, Cu and Zn in vegetablesoils and the following vegetable uptake. The approach and operational processof this model are similar to those described earlier (Chen et al., 2007a, 2009).The major parameters of the model include the heavy metal concentration in soiland soil solution, soil properties, plant uptake factors and heavy metal inputs in thestudied plots (Table 1). The initial concentrations of Cd, Pb, Cu and Zn in soil andsoil solution were measured based on the mean levels in the soil and soil solutionbefore 15 days of eld monitoring. The bulk density is calculated as the dry weightof soil divided by its volume (g/cm3). The percolation rate (Kh) is given by the linearrelation Kh[mean annual irrigation amount (200 cm)mean annual precipita-tion (110 cm) mean annual evaporation (120 cm)]/[8760 h (1 year)]0.02 cm/h.Soil volumetric water content was measured directly in the eld using the portablesoil moisture content analyzer (SPW-1, Nanjing, China). The plant uptake iscalculated in terms of Cd, Pb, Cu and Zn concentrations, the root density (R), andthe plant uptake ux (J), which is expressed in terms of the MichaelisMentonkinetics involving maximum ux, Jmax, root permeability factor, Km, and soilsolution (C) (Chen et al., 2007a). Adsorption constant is described by solidsolutionpartition coefcient, Kd (L/kg) that is given by the linear relation Kd[Totalconcentration of heavy metals in soil (mg/kg)]/[Total concentration of heavy metalsin soil solution (mg/L)].

    2.5. Health risk assessment of heavy metals through the food chain

    The hazard quotient (HQ) is used to characterize the health risk of consumingvegetables by the local residents (Hough et al., 2004; Xu et al., 2013; Zhuang et al.,2009), and this is frequently used to assess the non-cancer health risk associatedwith heavy metals ingested through consumption (Chary et al., 2008; Liu et al.,2005; USEPA, 2007; Yang et al., 2011). The HQ is a ratio of the determined dose of apollutant to a reference dose. If the ratio is less than 1, the exposed population isunlikely to experience adverse effects. The HQ of heavy metals is determined by thefollowing equation:

    HQ EDIRfD

    CvegIRvegEFveg EDBW AT RfD 2

    where EDI is the estimated daily intake of heavy metals, which depends on boththe heavy metal concentrations in vegetables and the amount of vegetableconsumption. RfD is the oral reference dose, which is regarded as an estimationof a daily exposure to the human population that is likely to be without anappreciable risk of deleterious effects during a lifetime (USEPA, 2007). The values ofRfD for Cd and Zn were 0.001 and 0.3 mg/kg day, which were obtained from U.S.

    EPA Integrated Risk Information System (Hu et al., 2013 and USEPA, 2007). Thevalues of RfD for Pb and Cu were 0.004 and 0.04 mg/kg day, which were obtainedfrom State Environment Protection Administration of China (Hu et al., 2013; SEPAC,2009a). Cveg is the measured concentration of heavy metals in the edible part ofindividual vegetable (mg/kg, fresh weight). IRveg is the amount of daily vegetableconsumption. As previously reported, the average IRveg for children and adults inChina were 0.223 and 0.355 kg/day per person, respectively (CMH, 2006). EF is theexposure frequency (350 days/year), ED is the exposure duration (6 years for child,30 years for adult), and BW is the body weight (24.5 kg for child, 60.3 kg for adult).These parameters are based on China's Health Statistical Yearbook (CMH, 2006).AT is the average life time for non-carcinogens (ED365 days/year). The HQ ofheavy metals is calculated separately for children (312 years old) and adults (1845 years old).

    The hazard index (HI) can be expressed as the sum of the hazard quotients (HQ)for all heavy metals (Abbasi et al., 2013). The HI is calculated as follows:

    HI n

    i 1HQ i 3

    2.6. Data analysis

    Statistical analysis of the data was performed using the software of SPSS 17.0 andMicrosoft Excel 2007. Figures were constructed with Origin 8.0 and SigmaPlot 11.0software. The data were normally distributed through the KolmogorovSmirnov test.Independent-samples T-test procedures were performed to determine the signicanceof heavy metals between different plots of soils.

    3. Results and discussions

    3.1. Concentrations of heavy metals in vegetable prole soils

    Soil represents a major sink for heavy metals in the terrestrialenvironment, and can identify the source of heavy metals fromanthropogenic activities and natural factors. Fig. 2 shows thecomparison of heavy metals in soil proles from the vegetableplots before and after the monitoring period and from thesurrounding paddy soils. The concentrations of Cd, Pb, Cu and Znwere the highest in surface soils compared with the lower layers,and decreased signicantly with increasing soil depth. Accordingto the environmental quality evaluation standard for greenhousevegetables production set by China (SEPAC, 2007), the maximumpermitted concentration of Cd, Pb, Cu and Zn in the soil should beless than 0.3, 50, 50 and 200 mg/kg in order to ensure the safety ofvegetable products. The concentrations of Cd, Pb, Cu and Zn inthese surface soils were generally lower than the mandatory safetyvalues. Compared with the surrounding paddy soils, the vegetable

    Table 1Parameter values for the simulation of heavy metal mass balance of soils.

    Parameters Cd Pb Cu Zn

    Initial trace element pools of soilTotal content (CT, mg/kg) 0.11 42.2 28.9 81.0Soil solution concentration (C, g/L) 0.35 62.0 34.5 151.9

    Soil propertiesSoil depth (d, cm) 20 20 20 20Bulk density (, g/cm3) 1.26 1.26 1.26 1.26Percolation rate (Kh, cm/h) 0.02 0.02 0.02 0.02Volumetric water content (, L/L) 0.20 0.20 0.20 0.20

    Plant uptakeRoot permeability coefcient (Km, M) 0.20 0.65 30 150Maximum inux (Jmax, mol/cm/h) 7.5108 2.5106 1.93103 6.8104Root density (R, cm/cm) 4.5 4.5 4.5 4.5Biomass return factor (Rf, dimensionless) 0.15 0.15 0.15 0.15Adsorption constant (Kd, L/kg) 314 681 838 533

    Trace element inputs (I, g/ha year)Inorganic fertilizers 0.13 7.67 12.33 55.37Organic fertilizers 6.62 238.1 1361.8 4312.3Irrigation water 0.00 5.67 7.50 2.80Atmospheric deposition 5.30 310.6 208.5 745.6

    W. Hu et al. / Ecotoxicology and Environmental Safety 98 (2013) 303309 305

  • soils had greater contents of heavy metals before and after themonitoring for both surface and prole soils. The result wasconsistent with a previous study (Huang et al., 2006), in which anaccumulation of Cd, Pb, Cu and Zn was identied in vegetable soils.

    3.2. Heavy metal input, output and balance based on eldmonitoring

    3.2.1. Heavy metal input by agronomic practicesBased on the 2-year eld monitoring on the contribution of Cd,

    Pb, Cu and Zn by the different input materials in the six plots (Fig. S1),the input of heavy metals by organic fertilizer contributed as much asabout 98% of the total input, account for the highest in vegetableproduction system. Although the application amount of irrigationwater was highest, its heavy metal contents were relatively low, andthus the heavy metal contribution by irrigation water was minimaland accounted for only 13% of the total input. Compared with organicfertilizer, the heavy metal contributed by chemical fertilizer was loweras well regardless of the input amounts or the concentration of heavymetals in the chemical fertilizers. The average input contribution of Cd,Pb, Cu and Zn by chemical fertilizers was only account for about 0.5%.The average input of Cd, Cu and Zn per years in the Netherlands was1.5 g/ha (0.23.7 g/ha), 350 g/ha and 1000 g/ha (611083 g/ha),respectively (Moolenaar and Lexmond, 1998). Compared to the inputof heavy metals from the Dutch agriculture soils, the input of heavymetals in this vegetable production system was relatively higher.Concerning the specic plots, the inputs of Cd, Pb, Cu and Zn in soils

    from N5 and N6 were signicantly higher than those of N3 and N4(Po0.05), and also signicantly higher than those of N1 and N2(Po0.01). These results indicated that the input of heavy metalsmainly depended on the amount of fertilizer application, especially theorganic fertilizer application (Table S1).

    In fact, the most important factor inuencing the input of heavymetals is the heavy metal concentration of the input material. Newmandatory limits on heavy metals in fertilizers were currently beingenacted in China to protect soils from heavy metal accumulation bythis major source (SEPAC, 2009b). According to the mandatory limitsfor fertilizers, heavy metal contents in organic and inorganic fertilizersin this study were all below the maximum levels (Table S2). However,even though none of the four heavy metals in any kind of fertilizersexceeded the maximum mandatory limits of China, a large amountof fertilizer application could cause a potential risk (Tu et al., 2011).Mean concentrations of Cd, Cu and Zn in organic fertilizer weresignicantly higher than those of inorganic fertilizer and irrigationwater, causing high proportion of total heavy metal input by organicfertilizer (Fig. S1). The result was consistent with the previousmeasurements in the Netherlands and other European areas(Moolenaar and Lexmond, 1999, 1998; Stanners and Bourdeau, 1995).

    3.2.2. Heavy metal outputs by vegetablesThe heavy metal contents were compared with the recom-

    mended maximum intake levels set by China (CMH, 2005). Theconcentrations of Cd and Pb in edible parts of all vegetables were

    Fig. 2. Comparison of heavy metals in soil proles before and after monitoring and surrounding paddy soils.

    W. Hu et al. / Ecotoxicology and Environmental Safety 98 (2013) 303309306

  • found to be much lower than the maximum levels (Table S3),indicating that all vegetables were safe to enter the food chain.Because Cu and Zn are essential elements for human body, theywere not regulated in foods in China. However, FAO/WHO (2001)regulated the maximum level for Cu and Zn to be 9.4 and 73.3 mg/kg (based on fresh weight) (FAO/WHO, 2001). The concentrationsfor Cu and Zn in the edible parts of vegetables were greatly lowerthan the limits set by FAO/WHO.

    Based on the annual output of heavy metals in each eld plot(Fig. S2), output of Cd in N6 was higher than those of other plots,and the outputs of Pb, Cu and Zn in N3, N4, N5 and N6 were higherthan those of N1 and N2. There were tomatoes planted in the plotsof N3, N4, N5, N6, and two rotations of tomato and celery wereplanted in N6. According to the experimental analysis, Cd contentin celery was higher than other vegetables, and the contents of Cd,Pb, Cu, and Zn in tomato plant residue were signicantly higherthan those in other vegetables (Table S3). It can be concluded thatthe output of heavy metals is affected by the management patternand cultivation intensity in different vegetable plots as well as thevegetable rotation (Tables S1 and S3).

    3.2.3. Heavy metal balanceThe balance of heavy metals in vegetable soils is not only

    affected by the input of agricultural materials and the output ofharvested vegetables, but also inuenced by the atmosphericdeposition, soil surface runoff and leaching. Atmospheric deposi-tion has been identied as the principal source of heavy metalsentering into plants and soils especially around peri-urban areas(Wang et al., 2012c). The annual atmospheric deposition ux of Cd,Pb, Cu and Zn in Nanjing were 5.3 g/ha, 310.6 g/ha, 208.5 g/ha and745.6 g/ha, respectively (Ni, 2006), implying that the contributionof atmospheric deposition to the heavy metal accumulation insoils may not be ignored (Sharma et al., 2008; Singh and Pandey,2012). As to the output of heavy metals, except for the output uxof heavy metals through harvested vegetables, soil surface runoffmay also be an important output (Moolenaar and Lexmond, 1998).In view of the similar soil and morphological characteristics of thestudy area, we referenced the annual output ux of Cd, Pb, Cu andZn through runoff in the literature as 0.06 g/ha, 0.05 g/ha, 4.3 g/haand 7.5 g/ha, respectively (Kong and Ni, 2006).

    With the total input (including agricultural materials andatmospheric deposition) minus the total output (including cropsabsorption and soil runoff), the total balance amounts were shownin Table 2. The balance of Cd, Pb Cu and Zn in the vegetable plotsshowed that the heavy metals input in soils were greater than theoutput. The surplus amounts of Cd, Pb, Cu and Zn were 10.3 g/ha,537.2 g/ha, 1504.2 g/ha and 4570.6 g/ha, respectively, indicatingnet increases of Cd, Pb, Cu and Zn, particularly large increases of Cuand Zn, in the vegetable plots. The accumulation of heavy metalsin vegetable soils resulted from high application of organicfertilizers and a relatively low uptake by vegetables (Table S1,Figs. S2 and S3). The net increases of Cd, Pb, Cu and Zn in thevegetable plots were signicant greater than those in Switzerlandand the Netherlands, where the net increases of Cd were only

    0.21.0 g/ha per year (Keller et al., 2001; Moolenaar and Lexmond,1998). As a result of the limitation of this study, uncertainty canenter the balance calculation of heavy metals in the vegetableplots. In the case of deterministic variables, such as heavy metalcontents in soils, vegetables and agricultural materials as well assoil properties, there is no uncertainty associated with a certainvalue. As the ux of heavy metals due to atmospheric deposition,leaching and erosionwere obtained from other studies, and shouldthus be considered uncertain.

    3.3. Assessing long-term accumulations of heavy metals based onmodel simulation

    We used STEM model to simulate 100 years of temporal changesof Cd, Pb, Cu and Zn concentrations in the soils (Fig. 3). The resultsindicated that intensive cultivation caused a signicant long-termaccumulation of Cd, Pb, Cu and Zn in surface vegetable soils. Thecontents of Cd, Pb, Cu and Zn in soils would increase by more thanthree times over the 100 years, from 0.11 to 0.42 mg/kg for Cd, 42.2to 64.0 mg/kg for Pb, 28.9 to 91.9 mg/kg for Cu and 81.0 to 245.3 mg/kg for Zn, respectively. If the vegetable soil were cultivated accordingto the conditions dened in Table 1 for another 55 and 36 years, thecontents of Cd and Pb in the surface soils would exceed themaximum permitted level set by China (SEPAC, 2007). In 34 and71 years later, total Cu and Zn contents in soils would exceed theirmandatory target safe values in China (SEPAC, 2007). The comparisonbetween Polish and Dutch heavy metal balances and uxes alsoclearly indicated that the development of intensive agronomy causedheavy metal accumulation during a time period and stronglyinuenced the degree of pollution of agro-ecosystems (Dach andStarmans, 2005). The long-term and heavy application of organicfertilizers would strongly cause the excessive input of Cd, Pb, Cu andZn into soils. Thus, the precautionary controls on the maximumannual input of Cd, Pb, Cu and Zn should be proposed to protect soilquality, crop security and human health.

    3.4. Health risk assessment of heavy metals through vegetableconsumption

    An appropriate assessment of the health risk of heavy metals invegetables can provide good guidance for vegetable productionand fertilizer utilization. The estimated daily intake (EDI) andhazard quotient (HQ) of heavy metals in different kind of vege-tables were calculated for both child and adult population accord-ing to the average heavy metal concentrations in each vegetableand the respective consumption. The highest EDI of Cd, Pb, Cu andZn came from the consumption of lettuce, eggplant, celery andspinach, respectively, for both children and adults, although theEDI of Cd, Pb, Cu and Zn were far below the reference dose (RfD)set by the USEPA and China (SEPAC. 2009a; USEPA, 2007). The HQof heavy metals decreased in the order of Pb4Cd4Cu4Zn, andthe individual HQ values and hazard index (HI) of Cd, Pb, Cu andZn were generally lower than one for all vegetables, suggestinglocal residents were not subject to a signicant health risk fromtheir diet. However, the HQ of heavy metals for children washigher than those for adults, indicating that attention should bepaid to the vegetable consumption for children. Among thedifferent vegetables, the highest HQ and HI of Cd, Pb, Cu and Znwere from the consumption of spinach, lettuce, eggplant andcelery, respectively. The EDI of Cd, Pb, Cu and Zn were far belowthe RfD and the HQ values were less than 1, which were consistentwith the results reported by Wang et al. (2012c) and the HQ valueswere greatly lower than those from industrial polluted eldsin Shaoguan, southern China, where HQ of Cd and Pb in the vegetableswere greater than one (Wang et al., 2012b), wastewater irrigated soilsalong Musi River, India (Sharma et al., 2008), and urban site located in

    Table 2Heavy metal balance in the vegetable plots (mean7standard deviation, g/ha year).

    Balances Cd Pb Cu Zn

    Input 12.174.1 562.17144.5 1590.271292.5 5116.172771.0Output 1.670.8 24.9715.1 86.0742.1 545.57201.2Balancea 10.373.9 537.27138.3 1504.271255.0 4570.672622.2Efciencyb 13.477.3 4.472.3 5.472.2 10.773.6

    a Balance inputoutput.b Efciencyoutput/input100.

    W. Hu et al. / Ecotoxicology and Environmental Safety 98 (2013) 303309 307

  • the West Midlands of England, United Kingdom (Hough et al., 2004).These ndings manifested that local residents were not exposed tohealth risk from dietary intake of Cd, Pb, Cu and Zn in vegetables in thestudy eld plots.

    4. Conclusions

    The intensive vegetable production had resulted in accumula-tion of Cd, Pb, Cu and Zn in surface soils in the plot-scale vegetableproduction system in a peri-urban vegetable farm near Nanjing,China. The long-term and excessive application of organic fertili-zers was the major source of Cd, Pb, Cu and Zn in vegetable soils.Under the current agronomic practices, the Cd, Pb, Cu and Zn insurface vegetable soils would be expected to exceed the permis-sible concentration within 100 years. The estimated dietaryintakes (EDI) of Cd, Pb, Cu and Zn were far below the referencedose, and the hazard quotient (HQ) and hazard index (HI) valueswere lower than 1.0 for both children and adults, suggesting localinhabitants were not exposed to health risk from dietary intake ofCd, Pb, Cu and Zn in vegetables.

    Acknowledgments

    This study was supported by the funding from the NationalNatural Science Foundation of China (Grant nos. 41101491 andU1202236), the Special Research Foundation of the Public NaturalResource Management Department from Ministry of Environmen-tal Protection of China (201109018) and the frontier project of theknowledge innovation engineering eld of Institute of Soil Science,Chinese Academy of Sciences (ISSASIP1106).

    Appendix A. Supplementary material

    Supplementary data associated with this article can be found inthe online version at http://dx.doi.org/10.1016/j.ecoenv.2013.09.040.

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    Accumulation and health risk of heavy metals in a plot-scale vegetable production system in a peri-urban vegetable farm...IntroductionMaterials and methodsThe study plotsMonitoring of element balance in vegetable plotsSampling, processing and analysisAssessing long-term accumulation of heavy metals using model approachHealth risk assessment of heavy metals through the food chainData analysis

    Results and discussionsConcentrations of heavy metals in vegetable profile soilsHeavy metal input, output and balance based on field monitoringHeavy metal input by agronomic practicesHeavy metal outputs by vegetablesHeavy metal balance

    Assessing long-term accumulations of heavy metals based on model simulationHealth risk assessment of heavy metals through vegetable consumption

    ConclusionsAcknowledgmentsSupplementary materialReferences