Status, Influences and Risk Assessment of Hexachlorocyclohexanes

Oct 4, 2013 - Large amounts of hexaclorocyclohexanes (HCHs) were historically applied to Chinese soils. However, there has been limited information on...
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Status, Influences and Risk Assessment of Hexachlorocyclohexanes in Agricultural Soils Across China Lili Niu,† Chao Xu,‡ Yijun Yao,† Kai Liu,§ Fangxing Yang,† Mengling Tang,† and Weiping Liu*,† †

International Joint Research Center for Persistent Toxic Substances (IJRC-PTS), MOE Key Laboratory of Environmental Remediation and Ecosystem Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China ‡ IJRC-PTS, College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou 310032, China § State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, POPs Research Center, Tsinghua University, Beijing 100084, China S Supporting Information *

ABSTRACT: Large amounts of hexaclorocyclohexanes (HCHs) were historically applied to Chinese soils. However, there has been limited information on the residue patterns of HCHs in soils at a national scale in China. In this study, surface soil samples were collected from agricultural fields across China, and the concentrations of HCHs and enantiomeric fractions (EFs) of α-HCH were measured. The results showed that the average concentrations of α-HCH, β-HCH, γ-HCH, and total HCHs in Chinese agricultural soils were 0.190, 1.31, 0.236, and 1.74 ng g−1, respectively. Residues of HCHs likely originated from past usage of technical HCHs. The isomers of α-HCH and γ-HCH tended to accumulate in the sites with lower total HCH concentrations, lower temperature, higher elevation, and less wet precipitation when compared to β-HCH. Enantiomeric analysis showed a preferential degradation of (−)-α-HCH. Human health risks via various exposure routes to HCHs in soils were further estimated. Overall, the mean hazard index (HI) linked to noncarcinogenic risks was below 1, suggesting an absence of noncarcinogenic risks of HCHs in Chinese soils. In addition, the cancer risk values were all below 10−4, which indicates low or very low risks.

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remain in soils after applications.9 In addition, soil is also regarded as a major secondary emission source of contaminants for groundwater, surface water, and the atmosphere.5 For POPs such as HCHs, this source may sustain for decades due to their large storage and long persistence. The redistribution of organic pollutants among diverse matrices is governed by the chemical properties of the chemicals and environmental factors, such as temperature, elevation, and soil organic matter content.6,10 Compared with other dissipation patterns of POPs from soils, for example, degradation, leaching into groundwater, and uptake by plant, volatilization is considered as the primary removal pathway.11,12 Due to the negative impacts of HCHs on both humans and ecosystems, the occurrence and toxicity of HCHs has been the focus of many studies. In China, the accumulation status of HCHs in soils has been investigated in some regions like Shanghai, and Guangzhou and Zhejiang provinces, among others.6,12,13 Even though lindane (i.e., γ-HCH) was con-

INTRODUCTION Hexaclorocyclohexanes (HCHs) were used as insecticides worldwide during the 1950s−1980s. They are environmentally persistent, bioaccumulative and toxic, posing potential risks to both humans and eco-systems. The agricultural application of HCHs was officially stopped in China in 1983, and they were later recognized as persistent organic pollutants (POPs) at the Stockholm Convention in 2009.1 China was one of the biggest producers and consumers of HCHs before the 1980s. Over 4.9 million tons of technical HCHs were produced in China over 30 years before the ban, which accounts for about 33% of the total global production.2 Though the use of HCHs has been restricted or terminated for many years, their residues are routinely detected in various environmental compartments, even in remote areas where they were never used, due to their persistence and long-distance migration.3−5 This raises great concerns about the continuing risks of HCHs to public health in China. Soil is an important reservoir for environmental pollutants such as pesticides and heavy metals.6,7 The residues of HCHs in soils mainly originate from industrial and agricultural practices through intentional applications, disposal, spills, and deposition.8 Approximately 20−70% of pesticides or their metabolites © XXXX American Chemical Society

Received: April 18, 2013 Revised: September 27, 2013 Accepted: October 4, 2013

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tinuously used until 2000 in China,14 the HCH residues were found to be relatively low and mainly originated from past usage of technical HCHs. However, previous studies only focused on one or a few regions. There has been little knowledge about the status of HCHs in agricultural soils at the national scale. Information about the residue levels, distribution characteristics and health risks of HCHs in agricultural soils across China can provide baseline information for both land use and management. In addition, the enantiomeric analysis of chiral pollutants is helpful for distinguishing their transport and fate pathways.15 Therefore, this study explored (a) residue status, (b) factors influencing the distribution patterns, (c) enantiomeric signature of α-HCH, and (d) potential human exposure risks of HCHs in agricultural soils in China. These results can lead to a better understanding of the redistribution of HCHs after their release, as well as scientific basis for contamination avoidance and control in China.

HCH enantiomers. More detailed chromatographic conditions are described in SI. Enantiomer fraction (EF), that is, the proportion of (+)-enantiomer to the sum of (+) and (−)-enantiomer peak areas, is often used to give a description of the relative composition of enantiomers in the chiral analysis. For a racemic mixture, EF is equal to 0.5. The values of EF > 0.5 and 1, while the risk may be absent when the value of HI is below 1. The cancer risk assessment on human was performed using ADD multiplied by each slope factor (SF) for ingestion, dermal contact and inhalation. The total cancer risks of each HCH isomer were calculated as the sum of cancer risks from diverse exposure routes. The cancer risks of a certain chemical in soils may be considered to be very low when the risk value is less than 10−6, low in the range of 10−6 and 10−4, moderate from 10−4 to 10−3, high from 10−3 to 10−1, and very high when it is over 10−1.

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MATERIALS AND METHODS The details of materials and methods used in this study are provided in the Supporting Information (SI). A brief description is given below. Reagents and Materials. The analytical standards of HCHs were purchased from Dr. Ehrenstorfer GmbH (Augsburg, Germany). All solvents and reagents used in this study were of high performance liquid chromatography (HPLC) grade or higher. Anhydrous granular sodium sulfate, Florisil, silica gel, aluminum, and superpurified copper powder were activated in advance. Sample Collection. In total, 131 soil samples were collected from the surface layer (0−20 cm) of agricultural fields in 31 provinces or regions across China during May of 2011. The sites were chosen according to the distribution of cultivated soils in China.16 The sampling sites are listed in SI (Figure SI-1 and Table SI-1). Details of the collection procedures were described in our previous study.7 The samples were transported back to the laboratory within 23 days after sample collection and stored at −4 °C before analysis. Sample Extraction and Cleanup. After freeze-drying, each soil sample was homogenized and sieved through 100 mesh (0.154 mm). An aliquot was extracted in a Soxhlet apparatus using dichloromethane (DCM) for 24 h. The extract was concentrated and solvent exchanged into hexane. The extract was then eluted through a column containing (from bottom to top) Na2SO4, Florisil, silica gel, aluminum, and Na2SO4 to remove the interferences. The target analytes were recovered in 70 mL of hexane/DCM (7:3). The final extract was concentrated, exchanged into hexane, and reduced to 0.5 mL. Before injection into a gas chromatography (GC) system, pentachloronitrobenzene (PCNB) was added as the internal standard. GC Analysis. The quantitative analysis of HCHs was carried out on an Agilent 7890 GC equipped with a Nickel-63 electron capture detector. Two columns, Zebron MultiResidue-1 (30 m × 0.25 mm ×0.25 μm, Phenomenex, Torrance, CA) and HP-5 (30 m × 0.32 mm ×0.25 μm, Agilent Technologies Inc., Santa Clara, CA) were used for the separation. The enantiomeric analysis of α-HCH was completed with an Agilent 7890 GC-5973 inert mass spectrometer operated in the selected ion monitoring mode. A BGB-172 chiral capillary column (20% tert-butyldimenthylsilylated-β-cyclodextrin in OV-1701, 30 m × 0.25 mm ×0.25 μm; BGB Analytik AG, Boeckten, Switzerland) was employed for the separation of αB

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Table 1. Descriptive Statistical Summary of HCH Concentrations in Agricultural Soils Across China (ng/g, Dry Weight) percentiles α-HCH β-HCH γ-HCH δ-HCH HCHsd a

mean

min

max

SDa

CVb(%)

5th

25th

50th

75th

95th

0.190 1.31 0.236 BDLc 1.74

0.051 0.029 0.054 BDLc 0.146

1.21 23.2 4.62 BDLc 23.9

0.210 2.91 0.499 BDLc 3.35

110 222 212

0.054 0.042 0.060 BDLc 0.180

0.064 0.083 0.070 BDLc 0.249

0.099 0.256 0.098 BDLc 0.524

0.203 1.15 0.232 BDLc 1.66

0.651 5.92 0.640 BDLc 6.85

193

SD: standard deviation. bCV: coefficient variation. cBDL: below detection level. dHCHs: sum of α-, β-, γ-, and δ-HCH.

each site as described in SI. In total, there were 491.3 t of HCHs left in Chinese agricultural soils. The HCH burden in this study was much smaller than that in other studies. For example, the amount of total HCH burden in the top 20 cm agricultural soils in Zhejiang Province alone was estimated to be 75.8 t by Zhang et al.,6 whereas it was only 16.2 t in this study. The volatilization half-lives of HCHs in agricultural soils across China were also estimated. The results showed that the volatilization half-lives of HCHs in soils from each province or region ranged from 28 to 1144 d, with a mean value of 271 days. It is worth noting that the mean volatilization half-life of HCHs in this study was much shorter than that of DDTs in the southern United States (11 years) and southern Ontario, Canada (220 years).22,23 This implies that the volatilization of HCHs from soils was more significant than that of DDTs, likely due to the differences in water solubility, biodegradability, and vapor pressure. Compositions of HCH Residues. The ratios of HCH isomers are often used to evaluate whether the residues are from past usage or fresh input. Usually, the technical mixture of HCHs consists of 60−70% α-HCH, 5−12% β-HCH, 10−12% γ-HCH, 6−10% δ-HCH, and 3−4% ε-HCH, while lindane contains 99.0% γ-HCH. Therefore, the ratios of α-HCH/γHCH and α-HCH/β-HCH are 4.64−5.83 and about 11.8, respectively, in technical HCHs.24 The ratio changes with time as the isomers degrade and dissipate at different rates.18,25 The ratios of α-HCH/γ-HCH and α-HCH/β-HCH in each soil from this study are shown in Figure SI-1 in SI. It is clear that the ratios of α-HCH/γ-HCH in soil samples from this study were all below 4.64, except for one sample, for which the ratio was 4.77 and might be slightly influenced by the new input of technical HCHs or the reduced input of γ-HCH in recent years. The ratios of α-HCH/β-HCH in all samples were below 11.8. These results are consistent with Zhang et al.,6 in which the ratios of α-HCH/γ-HCH and α-HCH/β-HCH in most soil samples were found to be lower than 5 and 11.8, respectively. Principal component analysis (PCA) was employed for further source analysis of HCHs. Two major components were extracted and they explained 58.3% and 30.8% of the total variance, respectively (Figure 1). The PCA analysis suggested that the samples in this study were all clustered together and were separate from technical HCHs. These results indicated that the residues of HCHs in this study were predominantly from the past use of technical HCHs. The isomer ratios of HCHs from several other studies are listed in SI (Table SI-2). Compared with specific cities or provinces in China, the ratios of α-HCH/β-HCH in most sites considered in this study were smaller. However, the ratios of α-HCH/γ-HCH were slightly higher in Tianjin, and Jilin and Anhui provinces in this study. In addition, the ratios of α-HCH/β-HCH and α-HCH/γ-HCH in other countries were all smaller than 4.64 and 11.8, respectively, which was in agreement with the findings of this study. Table

All parameters used in the noncancer and cancer risk assessment are listed in Table SI-1 in SI.

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RESULTS AND DISCUSSION Residue Levels of HCHs in Chinese Agricultural Soils. The descriptive statistical data including means, ranges, standard deviations (SD), coefficient variations (CV), and percentiles of HCH levels in agricultural soils across China are shown in Table 1. The concentrations of total HCHs ranged from 0.146 to 23.9 ng g−1, with a mean value of 1.74 ng g−1. The mean level of β-HCH was the highest among the isomers at 0.029−23.2 ng g−1, with an average value of 1.31 ng g−1. The water solubility and vapor pressure of β-HCH is the lowest, and it is more stable than other isomers of HCHs in soil.18 It is inclined to accumulate in biological media and resist to hydrolysis or enzymatic degradation.4 Furthermore, α-HCH and γ-HCH tend to transform to β-HCH in soil.4,19 These may contribute to the highest mean concentration of β-HCH in soils. The average concentrations of α-HCH and γ-HCH were 0.190 and 0.236 ng g−1, with the range from 0.051 to 1.21 and from 0.054 to 4.62 ng g−1, respectively. The concentrations of HCH isomers were mostly less than 1 ng·g−1, except β-HCH, the 75th percentile of which was 1.15 ng g−1. For the total HCH concentrations, the 5th, 25th, 50th, 75th, and 90th percentiles were 0.180, 0.249, 0.524, 1.66, and 6.85 ng·g−1, respectively. According to the Environmental Quality Standard for soil (GB-15618−2008) by the State Environmental Protection Administration of China, the less stringent grade II limits for HCHs in agricultural soils is 50 ng·g−1.20 The results of this study therefore suggest that the concentrations of HCHs in agricultural soils across China were all within 50 ng g−1. Compared to studies in other regions and countries (Table SI-2, SI), the residue levels of total HCHs in this study were relatively low. The large scale of sampling in this study may be responsible for this difference. In addition, variations of HCH levels between this and other studies may be attributed to the different soil background (e.g., industrial or agricultural use) and natural conditions (e.g., soil properties) of the sampled sites. For example, samples from areas impacted by industrial manufacturing plants exhibited higher residue levels of HCHs in the study in Germany.21 For a specific area, the concentrations of HCHs and isomers in this study were much lower than those in other studies. These results suggest that there was a decreasing trend in HCH residues in the agricultural soils in China since the usage of HCHs was restricted. The coefficients of variation of total HCHs and isomers were in the range of 110 to 222%, reflecting extensive variations in the usage and residues of HCHs in Chinese farmland. The residue inventories of total HCHs in cultivated soils across China were calculated based on their concentrations at C

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the fractions of γ-HCH were the highest and ranged from 36.4 to 50.7% of the total HCHs. This suggested that lindane might have been used recently in these regions. Another possible reason could be the different dissipation rates of HCH isomers under the vastly different soil and climatic conditions because of the large sampling scope. The residue levels and percentages of HCH isomers in the central, eastern, western, and northeastern large regions of China further showed these different distribution patterns (Table SI-4, SI). Factors Influencing HCH Compositions. The spatial variations of HCH residues in soil may depend on a diverse range of factors such as application amounts, durations, dissipation rates, among others.5 The correlations of HCH isomeric ratios and total HCH concentrations are presented in Table 2. The percentages of α-HCH and γ-HCH were significantly negatively correlated with β-HCH fractions and total HCH concentrations (P < 0.0001). Nevertheless, a significantly positive correlation was observed between the fractions of β-HCH and total HCH concentrations (P < 0.0001). Similar relationships were also observed in a previous study involving Haihe Plain, China.5 In that study, negative correlations were found between α-HCH/γ-HCH and total HCHs, as well as between γ-HCH/∑HCH and ∑HCH. Such findings suggest that the total concentration of HCHs could be an important factor influencing the HCH isomeric fractions in soils. This may result from the preferential breakdown of αHCH and γ-HCH in soils or their transformation to β-HCH induced by high total HCH concentrations.4,19 During the dissipation and redistribution processes of organic compounds in soils, factors such as natural and climate conditions can play a key role.28 Therefore, the influences of elevation, temperature, and amount of wet precipitation on the distribution patterns of HCHs in Chinese agricultural soils were explored in this study. According to the elevation of each sampling site, the sampling sites were classified into two groups: highland (elevation >500m, n = 39) and plain (elevation < 500m, n = 92). The average percentage of each HCH isomer was calculated for the highland and plain soils (Figure SI-2, SI). The percentages of α-HCH and γ-HCH were much higher in the highland soils than in the plain soils. However, the fraction of β-HCH was lower in the highland soils than in the plain soils. When the HCH isomer ratios and elevation of sampling sites were correlated (Table 3), the relationships for α-HCH and γ-HCH fractions were significantly positive (P = 0.006 and 0.004, respectively). To the contrary, the correlation between β-HCH fraction and elevation was significantly negative (P = 0.001). These results were in agreement with the comparison of the individual HCH isomeric ratios between the highland and plain soils. The relationships of HCH isomer fractions with the temperature of each sampling sites in 2010 are shown in Table 3.16 The α-HCH percentage decreased (P = 0.039), whereas the β-HCH percentage increased with temperature (P = 0.028). However, no significant correlation between the γHCH fraction and temperature was detected (P = 0.072). The percentages and concentrations of α-HCH and γ-HCH were good tracers for global transport of HCHs. In the study of OCPs in Arctic lake sediments by Muir et al., higher ratios of αHCH and γ-HCH were observed at sites with lower temperature.29 The concentrations of α-HCH and γ-HCH in snow were also found to increase with altitude, indicating longrange transport propency.30 Likewise, HCH isomer concentrations in mountains were higher than those in plains in

Figure 1. Principal component analysis of HCH compositions and ratios, and comparison with technical HCHs.

SI-3 in SI presents the relationships among concentrations of HCH isomers and total HCHs. Strong positive correlations (P < 0.0001) were observed, further suggesting that past use of technical HCHs was the possible source. The correlation coefficient between β-isomer and total HCHs was 0.99, the highest among all relationships, also implying that β-HCH was the most stable isomer in soil. Spatial Distribution of HCHs in Chinese Farmland Soils. To understand the regional variations in HCH residues in agricultural soils across China, Kriging interpolation was used to map the geographic distribution based on the measured concentrations of HCHs and soil organic matter (OM) contents (Figure 2). Higher residue levels of total HCHs were found in the central and southern China, such as Hunan and Guangxi provinces. In addition, the average concentration of HCHs in soils from Shanxi Province (6.51 ng g−1) was also much higher. The residue characteristics of organic pollutants were governed by numerous factors. It was previously reported that the extensive agricultural applications contributed the most to the remaining residues of HCHs.5 Therefore, the concentrations of HCHs were compared with the usage inventories of technical HCHs in China between 1952 and 1980.26 The areas with high residues of HCHs roughly superimposed the inventory map, suggesting that the current distribution of HCHs was greatly influenced by the past usage of technical HCHs. The OM contents were higher in the central, eastern, northeastern, and western regions of China, and the distribution pattern overlapped those of total HCHs and isomers. This suggested that OM content was also an important factor influencing the current distribution of HCH residues in agricultural soils in China. The spatial distribution of β-HCH isomer was similar to that of total HCHs. Nevertheless, for α-HCH and γ-HCH, their higher residues were found not only in Hunan, Jiangxi, and Shanxi provinces, but also in the northwestern China where the use of technical HCHs was limited. The fractions of HCH isomers in agricultural soils across China are also presented in the map of China (Figure 3). The β-HCH isomer was dominant in most samples across China, contributing 52.3% to the total HCHs at the national average level. This result was in agreement with studies on the predominance of β-HCH in Zhejiang Province and Hongze Lake.6,27 However, α-HCH was found to be the isomer of the highest proportion in Yunan and Qinghai provinces, accounting for 41.0 and 41.2%, respectively. In addition, in Shanghai and Guangdong, Hubei, Guizhou, Tibet, and Xinjiang provinces, D

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Figure 2. Spatial distribution of HCHs and organic matter in agricultural soils across China.

Zhejiang Province.6 Results from this and other studies suggest that elevation and temperature are significant factors determining the distribution features of HCH isomers in soils. Studies have shown that organocholorine pesticides (OCPs) may migrate from warmer regions and deposit in colder regions, known as the global distillation effect.31 Among the HCH isomers, the vapor pressure of α-HCH and γ-HCH are much higher than that of β-HCH. Therefore, at higher temperature and lower elevation, β-HCH may preferentially accumulate in soil. It has been reported that α-HCH was the major component detected in the atmosphere due to its higher vapor pressure.4 In addition, α-HCH and γ-HCH were more degradable than β-HCH and their degradation is faster at higher temperature.32 Diverse microbial populations in different

areas across China may be another reason for the variations in HCH isomer ratios, although information on microbial diversity was not obtained in this study. For organic pollutants, wet precipitation is likely an important pathway for them to enter soil.33 In addition, movement with rain can also influence the fate and distribution features of organic chemicals. The relationship of precipitation rates in 2010 and the HCH isomeric fractions are listed in Table 3.16 Precipitation rates showed a significantly positive correlation with β-HCH percentages (P = 0.043), and a negative relationship for γ-HCH fractions (P = 0.026), while no clear relationship was found for that with α-HCH percentage and total concentrations of HCHs (data not shown). It may be due to the runoff and erosion induced by rain, which can E

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relationship between HCHs with soil OM was also observed in agricultural soils in Hong Kong.36 Enantiomeric Profiles of Chiral α-HCH. Among the HCH isomers, α-HCH is the only one with chirality and has two enantiomers. The EF of α-HCH has been used to infer the role of microbial degradation and age of residue, as biodegradation is often chiral selective.37,38 For chiral analysis of α-HCH, 18 out of the 131 soil samples were selected on the basis of representation of geographic locations and concentration ranges to determine their EF values (Figure SI-5, SI). In general, the EFs of α-HCH in the selected soils varied from 0.391 to 0.667, with a mean value of 0.560. The enantiomeric profiles of α-HCH were generally nonracemic with EF values >0.5 for most samples. The deviation of EF from 0.5 implied that residues of HCHs in these selected regions were likely from past use. The derived EF values suggested preferential degradations of (−)-enantiomer in most soil samples. Bidleman et al. also found that (−)-enantiomer depleted more rapidly between the two enantiomers of α-HCH based on 270 samples obtained during a period from the 1990s to present at different locations in the world.15 The highest EF in this study was found in the soils from Shanxi Province, where the concentration of αHCH was also the highest among all 131 samples. Such case was quite different with the study by Zhang et al., who stated that high HCH residues might induce preferential biodegradation of (+)-α-HCH.6 The lowest EF was observed in samples collected from Gansu Province, where the elevation was above 1500 m and OM content was only 1.34%. Selective depletion of (+)-α-HCH was also observed in soils from Zhejiang Province in China in a previous study.6 Human Exposure Risk Assessment. The noncancer risks to human via nondietary (ingestion and dermal contact) and dietary routes (intake of vegetables and grains grown in local soils) based on the concentrations of HCH isomers and total HCHs in farmland soils are outlined in Figure 4. The average

Figure 3. Provincial fractions of HCH isomers in agricultural soils across China.

Table 2. Correlation Coefficient Matrix among Percentage of HCH Isomers and Total HCH Concentration (n = 131) α-HCH (%) β-HCH (%) γ-HCH (%) HCHs a

α-HCH (%)

β-HCH (%)

γ-HCH (%)

1a −0.832a 0.516a −0.488a

1a −0.904a 0.485a

1a −0.374a

At P < 0.0001 level.

Table 3. Relationships of HCH isomer percentages (IP) with elevation (E), temperature (T) and wet precipitation (P) of each site equation α-HCH

β-HCH

γ-HCH

IP IP IP IP IP IP IP IP IP

= = = = = = = = =

0.204 + 3.59 × 10−5E 0.280−0.004T 0.243−2.13 × 10−5P 0.573−8.44 × 10−5E 0.407 + 0.009T 0.459 + 7.29 × 10−5P 0.223 + 4.86 × 10−5E 0.313−0.005T 0.298−5.16 × 10−5P

R

p-value

0.223 −0.158 −0.056 −0.267 0.172 0.155 0.234 −0.132 −0.174

0.006 0.039 0.238 0.001 0.028 0.043 0.004 0.072 0.026

selectively remove HCH isomers from soil. Therefore, wet deposition is another crucial factor determining the residue characteristics of HCH isomers. Soil properties may also influence the HCH residues in soils.10 Soil OM may sequester organic pollutants, prolonging their persistence in soil.34 Distribution of hydrophobic compounds is expected to be proportional to OM content in an equilibrated soil−air system.35 The measurements of OM content in soils were completed in our previous study.7 The concentrations of α-HCH, β-HCH, γ-HCH, and total HCHs were much higher in soil samples with higher OM (OM ≥ 2.3%) than those in soils with lower OM (OM < 2.3%) (Figure SI-3, SI). The relationships between the OM contents and HCHs in all soil samples are given in Figure SI-4 in SI. Positive correlations were identified between OM and HCHs (P = 0.007, 0.048, 0.037, and 0.0007 for HCH, α-HCH, β-HCH, and γ-HCH with OM, respectively). A similar positive but weak

Figure 4. Noncarcinogenic exposure risk to adults and children via ingestion, dermal contact of soils, and intake of food grown in soils.

HIs for adults and children were all below 1, indicating an absence of noncancer risks for HCHs in Chinese arable soils. A similar absence of noncancer risk of HCHs in agricultural soils from Hong Kong was previously observed.36 Among the HCH isomers, the noncancer risks of β-HCH to adults and children were the highest. Overall, the risks to adults were relatively higher than those to children for HCHs. The exposure cancer risks of HCHs via nondietary (ingestion and dermal contact) and dietary routes (intake of vegetables and grains grown in local soils) to adults and children are listed F

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in SI (Table SI-5). The estimated mean cancer risk levels of HCHs were all less than 10−4, implying very low or low cancer risks to both adults and children. The cancer risks to adults were higher than those to children, which might be due to the larger consumption of food by adults than children. Among the isomers, the lowest mean cancer risk was found in γ-HCH to children (5.53 × 10−6), whereas the highest cancer risk was observed in β-HCH to adults (9.24 × 10−5). In addition, the risks of most samples were in the very low, low, or moderate category. However, high cancer risks of β-HCH and total HCHs to adults were still found in 1.53 and 2.29% of the samples, respectively, although no sample was identified to pose a very high cancer risk. It is worth noting that β-HCH posed higher cancer and noncancer risks to both adults and children than the other isomers. As the most persistent isomer, β-HCH tends to persist longer in soils. Therefore, β-HCH may induce relatively greater risks to eco-systems and human health over time. In the assessment of cancer and noncancer risks, human health risks from exposure to HCHs through intake of vegetables and grains contributed for over 99% of the total risks, suggesting that the consumption of contaminated food would be the primary contributor to the human risks of HCHs in soils. However, digestion, metabolism, and excretion of HCHs in human bodies were not considered in the prediction, which may lead to overestimation of the human exposure risks in this study. Further studies are needed to measure the actual concentrations of HCHs in human bodies and evaluate factors influencing their accumulation.

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ASSOCIATED CONTENT

S Supporting Information *

Detailed information of the materials and analytic methods of HCHs, sampling sites, parameters of the risk assessments, concentrations of HCHs in other studies, correlations between HCH isomers and HCHs, HCH residue levels in four regions of China, ratios of α-HCH/γ-HCH and α-HCH/β-HCH, distribution characteristics of HCH isomers in Mountain, Plain and in soils with higher and lower organic matter, enantiomeric fractions of α-HCH in selected soils and cancer risks of HCHs in soils across China. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*(W.L.) Phone: +86-571-8898-2341; fax: +86-571-8898-2341; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was funded in the part by the National Basic Research Program of China (No. 2009CB421603), the National Natural Science Foundation of China (No. 21177112, 20837002), and the Ph.D. Programs Foundation of Ministry of Education of China (No. 20120101110132).

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REFERENCES

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