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Status of phthalate esters contamination in agricultural soils across China and associated health risks
Environmental Pollution 195 (2014) 16e23
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Status of phthalate esters contamination in agricultural soils across China and associated health risks Lili Niu a, Yang Xu a, Chao Xu b, Lingxiang Yun a, Weiping Liu a, * a 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 b IJRC-PTS, College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou 310032, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 April 2014 Received in revised form 6 August 2014 Accepted 13 August 2014 Available online 3 September 2014
The extensive utilization of phthalate-containing products has lead to ubiquitous contamination of phthalate esters (PAEs) in various matrices. However, comprehensive knowledge of their pollution in Chinese farmland and associated risks is still limited. In this study, 15 PAEs were determined in soils from agricultural fields throughout the Mainland China. The concentrations of S15PAEs were in the range of 75.0e6369 mg kg1. Three provinces (i.e., Fujian, Guangdong and Xinjiang, China) showed the highest loadings of PAEs. Bis(2-Ethylhexyl) phthalate (DEHP) was found as the most abundant component and P contributed 71.5% to the 15PAEs. The major source of PAEs in arable soils was associated with the application of agricultural plastic films, followed by the activities for soil fertility. Furthermore, the noncancer and carcinogenic risks of target PAEs were estimated. The hazard indexes (HIs) of PAEs in all samples were below 1 and the carcinogenic risk levels were all within 104. Results from this study will provide valuable information for Chinese agricultural soil management and risk avoidance. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Phthalate ester Agricultural soil Spatial distribution Potential source Human health risk
1. Introduction Soil is an important environmental medium and a major reservoir for a diverse range of pollutants. With the rampant development of agriculture and industry, the soil environment has been extensively deteriorated. Many toxic pollutants have been introduced and remain in soils, such as organochlorine pesticides (OCPs), polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), heavy metals and phthalate esters (PAEs) (Cai et al., 2008; Niu et al., 2013a, b). Among these persistent toxic substances (PTSs), PAEs have been demonstrated to be the most abundant organic contaminant in soils (Cai et al., 2008). Phthalate esters, a group of flexible, pliable and elastic chemicals, are widely used in plastic products, pesticides, cosmetics and personal care products (Gomez-Hens and Aguilar-Caballos, 2003; Hu et al., 2003). It has been estimated that the global production and consumption of PAEs is approximately 6.0 million tons$year1 (Arbeitsgemeinschaft PVC and Umwelt e. V, 2006). Because of the widespread usage of phthalate-containing products, the residues of PAEs have been routinely detected in various matrices, such as soil,
* Corresponding author. E-mail address: [email protected] (W. Liu). http://dx.doi.org/10.1016/j.envpol.2014.08.014 0269-7491/© 2014 Elsevier Ltd. All rights reserved.
water, air and sediments (Cai et al., 2008; Wang et al., 2012; Sun et al., 2013; Liu et al., 2014). The application of agricultural plastic films is one of the important sources of PAEs in farmland soils. In 2011, the amount of plastic films applied agriculturally in China was approximately 2.29 million tons and the mulching area reached 19.8 million hectares (Department of Rural Survey National Bureau of Statistics of China, 2012). Another significant source of PAEs in farmland soil is associated with agricultural practices such as the application of sewage sludge, fertilizers, biosolids and irrigation wastewater, among others (Cai et al., 2007; Mo et al., 2008). In addition, the concentrations of PAEs in soils can also be influenced by atmospheric deposition, soil communities and meteorological conditions (Zeng et al., 2008, 2010). Although PAEs are not as toxic as persistent organic pollutants (POPs), their ubiquitous existence poses great threats to humans. A phthalate incident that happened in Taiwan in 2011 aroused strong public concerns on the adverse effects of PAEs on human health (Li and Ko, 2012). Many epidemiology and toxicology studies have demonstrated that some PAEs, such as bis(2-Ethylhexyl) phthalate (DEHP), dibutyl phthalate (DnBP), benzyl butyl phthalate (BBP), diethyl phthalate (DEP) and dihexyl phthalate (DHP), are endocrine disrupting compounds (Gomez-Hens and Aguilar-Caballos, 2003). Moreover, dimethyl phthalate (DMP), DEP, DnBP, BBP, DEHP and di-
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
n-octyl phthalate (DnOP) have been classified as priority environmental pollutants by the U.S. Environmental Protection Agency (U.S. EPA) (Keith and Telliard, 1979). Therefore, numerous studies have addressed the potential risks, occurrence and sources of PAEs in diverse media (Hu et al., 2003; Zeng et al., 2008; Wang et al., 2013; Kranich et al., 2014). However, previous studies have largely focused on a regional scale. Although a national investigation was carried out in 2003, the information is still not sufficient for well understanding the PAE pollution in Chinese arable soils due to the limited number of sites and PAE species analyzed in that study (Hu et al., 2003). In addition, the potential risks of PAEs to human health via multiple pathways have been infrequently estimated. Therefore, a full-scale study on the status of PAE pollution in farmland soils at the national scale and associated health risks are of considerable significance for setting strategies to minimize their pollution and exposure risks. In this study, 15 PAEs were measured in agricultural soils collected from 123 regions throughout China. Our aims were to characterize the spatial distribution features and congener profiles of PAEs, as well as to discern their possible sources. In addition, the non-cancer and carcinogenic risks of toxic PAEs in soils were also estimated for local residents via dietary and non-dietary routes. These results will provide baseline information for soil quality assessments and rational farming practices, thus protecting human health. 2. Materials and methods 2.1. Sample collection In total, 123 soil samples were collected from agricultural fields in 31 provinces, municipalities or autonomous regions across China in April and May of 2013. The sampling sites were chosen according to the distribution of farmland soils in China (National Bureau of Statistics of China, 2013) and located by GPS (Fig. S1 in Supporting Information, SI). Before collection, overlying vegetation was thoroughly excluded. At each sampling site, five agricultural soil sub-samples (0e20 cm) were collected with a pre-cleaned stainless steel scoop and mixed to form a composite sample in a pre-cleaned aluminum foil bag. Then, the soil samples were immediately transported to the laboratory and stored at 20 C until analysis. Soils for pH measurement were freeze-dried, ground and passed through a stainless steel sieve (2 mm). Then, the remaining soils were further sieved through a 0.154 mm sieve for the analysis of PAEs and soil organic matter (SOM).
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individual PAEs to quantify the amounts of analytes in samples using the internal calibration method. 2.3. Quality control and quality assurance During the analytical procedures, all data were subjected to strict quality control and quality assurance measures. Blank samples were included with every 15 field samples to check for the interference and contamination. Only small levels of DnBP, DiBP and DEHP were detected in procedural blank and ranged from 0.996 to 3.20 mg kg1. Then the concentrations of PAEs in soil samples were all blank corrected. All samples were spiked with surrogate standards to monitor the recovery, which ranged from 80.7 to 99.9%. The recoveries of the 15 PAEs in the spiked blank and spiked matrix samples ranged from 76.7 to 105.1 and 75.2 to 101.9%, respectively. PAE calibration standards of were employed to calibrate the instrument every day. The limits of detection (LOD) of individual PAEs were calculated as three times the signal-to-noise ratio and fell in the range of 0.008e0.295 mg kg1. 2.4. Analyses of soil organic matter and pH A pH electrode was used to determine soil pH with a soil/water (CO2-freed deionized) ratio of 1:2.5 (w/v). The soil organic matter content was measured by dichromate digestion at 180 C according to Lu (2000). 2.5. Health risk assessment The non-cancer and carcinogenic risks of PAEs were estimated according to the methods recommended by the U.S. EPA (2013). Because the local residents eat their own self-produced food, risks via non-dietary and dietary pathways were all involved. Among the individual PAE congeners studied, DEP, DnBP and DnOP were recognized as non-cancer compounds with respect to human health, while DEHP did present carcinogenic risk. In the non-cancer risk assessments of DEP, DnBP, DEHP and DnOP, their average daily doses (ADDs, mg kg1 day1) via dietary (only considering food grown in soils) and non-dietary (soil ingestion, dermal contact and inhalation) routes were calculated as follows. ADDintake ¼
Csoil BAF IRF EF ED CF BW AT
(1)
where Csoil is the concentration of target chemical in farmland soil (mg kg1); BAF is the bioaccumulation factor of individual PAEs from soil to foodstuff (vegetables and grains); IRF is the daily intake rate of food by inhabitants (mg/day), where the IRF for children is supposed to be 1/3 of that for adults; EF is the exposure frequency (days yr1); ED is the exposure duration (yr); BW is the body weight (kg); AT is the average lifetime (days); and CF is the conversion factor (kg mg1). ADDingest ¼
Csoil IRS EF ED CF BW AT
(2)
where IRS is the soil ingestion rate (mg day1); 2.2. Sample extraction and analysis A standard mixture of 15 PAEs, including DMP, DEP, diisobutyl phthalate (DiBP), DnBP, bis(2-Methoxyethyl) phthalate (DMGP), bis(4-Methyl-2-pentyl) phthalate (DMPP), bis(2-Ethoxyethyl) phthalate (DEEP), dipentyl phthalate (DnAP), DHP, BBP, bis(2-n-butoxyethyl) phthalate (DBEP), dicyclohexyl phthalate (DCHP), DEHP, DnOP and dinonyl phthalate (DNP) and a surrogate standard mixture, including dibenzyl phthalate, diphenyl isophthalate and diphenyl phthalate, were purchased from AccuStandard, Inc. (New Haven, CT, US). A solid internal standard of benzyl benzoate (99.5% purity) was acquired from Dr. Ehrenstorfer (Augsburg, Germany). Other solvents and reagents of residue analysis grade were obtained from J&K Chemical Ltd. (Beijing, China). Neutral silica gel, aluminum, florisil and anhydrous granular sodium sulfate (Na2SO4) were activated prior to use. After being spiked with surrogate standards of ibenzyl phthalate, diphenyl isophthalate and diphenyl phthalate, the soil samples containing activated copper granules were extracted with dichloromethane (DCM) using a Soxhlet apparatus. The extract was then solvent-exchanged into hexane and cleaned on a column filled with Na2SO4, florisil, neutral silica gel, neutral aluminum and Na2SO4 (from bottom to top). The column was first eluted with 20 mL of hexane and 70 mL of hexane/DCM (7/3, v/v). Then, the target analytes were recovered in the final eluate with 40 mL of hexane/acetone (4:1, v/v). After being concentrated and reduced to 0.5 mL, the extracts were spiked with the internal standard before instrumental analysis. The quantitative analysis of PAEs was carried out on an Agilent 7890 GC coupled to an Agilent 5975C MS (Agilent Technologies, Avondale, PA, USA). An HP-5MS capillary column (30 m 320 mm 0.25 mm film thickness, Agilent Technologies Inc., Santa Clara, CA) was used for separation. The selective ion monitoring mode and electron impact were employed and the temperature of the transfer line and the ion source were 280 C and 230 C, respectively. The gas chromatography temperature programs were as follows: initial temperate 80 C for 1.0 min, increase at a rate of 10 C min1 to 180 C (hold for 1.0 min), ramp at 2 C min1 to 260 C (hold for 1.0 min) and finally ramp to 300 C at 2 C min1 (hold for 5 min). The carrier helium gas was kept at a rate of 0.8 mL min1. A five-point calibration curve was made for
ADDdermal ¼
Csoil SA AF ABS EF ED CF BW AT 2
(3)
1
where SA is the soil surface area (cm day ); AF is the soil adherence factor (mg cm2); and ABS is the fraction of contaminant absorbed dermally from the soil (unitless). ADDinhale ¼
Csoil EF ED 103 PEF AT
(4)
where PEF is the particulate emission factor (m3 kg1) and a default PEF equal to 1.36 109 m3 kg1 was used. The hazard index (HI), which represents the total risks of a certain PAE in soil to human health through multiple exposure pathways, was calculated with the following equations. HQ ¼ HI ¼
ADD RfD
X
HQ i
(5) (6)
where HQ is the hazard quotient; i represents the different exposure pathways; RfD (mg kg1 day1) is defined as the daily maximum permissible level of contaminants, including the reference dose for ingestion and intake of contaminated food (RfDo, mg kg1 day1), the reference dose for dermal contact (RfDABS ¼ RfDo ABSGI , mg kg1 day1) and the reference dose of inhalation (RfCi, mg m3); ABSGI is the fraction of pollutant absorbed in the gastrointestinal tract (unitless). The local inhabitants are considered to be exposed to non-cancer risks if the value of HI is greater than 1. The ADD of DEHP via dietary pathways for carcinogenic risk assessment was calculated using Eq. (1) and these via non-dietary pathways were calculated based on the following.
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ADDingest
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Csoil EF IFSadj CF ¼ AT
(7)
where IFSadj is the age-adjusted soil ingestion rate (mg year kg1 day1). ADDdermal ¼
Csoil EF DFSadj ABS CF AT
(8)
where DFSadj is the age-adjusted soil dermal contact factor (mg year kg ADDinhale ¼
1
1
day
Csoil EF ED 103 PEF AT
)
(9)
The carcinogenic risks of DEHP were appraised using ADD multiplied by a slope factor (SF), which is composed of oral slope factors (SFO, (mg kg1 day1)1) for ingestion, dermal contact (SFO ABSGI (mg kg1 day1)1) and inhalation unit risk (IUR, (mg m3)1). The estimated carcinogenic risks may be considered very low if the value of risk is less than 106, low in the range of 106e104, moderate from 104 to 103, high from 103 to 101 and very high if the value is greater than 101. The values of parameters for non-cancer and carcinogenic risks are listed in Table S1 of SI.
P distribution of 15PAEs in agricultural soils across China. As shown in Fig. 1, the highest contents of total PAEs in soils were observed in Fujian, Guangdong and Xinjiang provinces. The sites in Chongqing City, Hubei and Henan provinces also showed higher P levels of 15PAEs in soils. However, the total PAE levels were relatively low in Northeast China. The relative contributions of individual PAEs in Chinese arable soils were further calculated and the congener profiles in each province are shown in Fig. 2. DEHP was the most abundant and its national average contribution to P 15PAEs was 71.5%, with the highest value of 91.51% in Fujian Province. DiBP was the second most dominant PAE in soils, followed by DNP and DnBP, which contributed 8.22, 7.22 and 6.89% to P 15PAEs, respectively. In total, DEHP, DiBP, DnBP and DNP together P 15PAEs concentrations. The accounted for 88.5e98.3% of the highest fraction of these 4 PAE congeners was also observed in Fujian Province. 3.2. Source analysis of PAEs
3. Results 3.1. Concentrations and spatial distribution of PAEs in Chinese agricultural soils A descriptive statistical summary of individual and total PAE concentrations in Chinese agricultural soils is shown in Table 1. Phthalate esters were detected in all the soil samples analyzed. The total concentrations of 15 PAEs in soils varied considerably and ranged from 75.0 to 6369 mg kg1, with a mean value of 1088 mg kg1. With regard to individual PAEs, DMP, DEP, DiBP, DnBP and DMGP were observed in all the samples, while the detectable frequencies of DMPP, DEEP, DnAP, DHP, BBP, DBEP, DCHP, DEHP, DnOP and DNP were 5.79, 16.5, 9.09, 57.0, 61.2, 95.9, 95.9, 95.9, 97.5, 99.2 and 99.2%, respectively. Among the analyzed PAE congeners, DEHP exhibited the highest concentration, followed by DiBP, DnBP and DNP, whose average residue levels were 821, 74.7, 65.8 and 69.6 mg kg1, respectively. The sum of the concentration of 6 PAEs (DMP, DEP, DnBP, DnOP, DEHP and BBP) ranged from 0.032 to 6.29 mg kg1, which were within the less stringent grade II limits for PAEs (10 mg kg1) in arable soils recommended by the Environmental Quality Standard for soil in China (GB-15618-2008) (China National Environmental Protection Agency, 2008). To provide a direct insight into PAE contamination, a geographic information system (GIS) was employed to map the spatial
Table 1 Descriptive statistical summary of individual concentrations of PAEs (mg/kg) and soil properties in agricultural soils across China.
DMP DEP DiBP DnBP DMGP DMPP DEEP DnAP DHP BBP DBEP DCHP DEHP DnOP DNP P PAEs OM(%) pH
Mean
Min
Max
Median
SD
CV (%)
DF (%)
14.8 2.79 74.7 65.8 4.96 ND ND ND 0.068 0.042 7.94 5.84 821 19.8 69.6 1088 2.32 6.94
1.19 0.236 4.93 4.04 0.597 ND ND ND ND ND ND ND ND ND ND 75.0 0.367 4.01
55.2 24.3 335 457 12.3 0.844 1.53 8.56 0.505 0.276 65.0 40.9 6218 298 606 6369 6.88 8.70
12.8 2.22 59.9 51.7 4.76 ND ND ND 0.029 0.037 6.55 4.47 562 14.0 49.5 847 2.06 7.01
9.56 2.49 47.1 54.2 2.09 0.118 0.268 0.784 0.094 0.044 8.06 5.63 756 30.0 78.1 794 1.27 0.981
64.7 89.1 63.1 82.3 42.2 408 197 694 139 106 102 96.4 92.1 151 112 72.9 5.48 14.1
100 100 100 100 100 5.79 16.5 9.09 57.0 61.2 95.9 95.9 97.5 99.2 99.2 100
Correlation analysis (CA) and principal component analysis (PCA) were conducted to identify the potential sources of PAEs in Chinese arable soils. Table S2 of SI lists the correlation coefficient matrixes among the individual concentrations of PAEs. DEHP P showed the strongest relationship with 15PAEs (R ¼ 0.959) at the 0.01 significance level, followed by DnBP (R ¼ 0.495) and DnOP (R ¼ 0.479). Of the PAE congeners analyzed, DMP, DEP, DiBP, DnBP, DMGP and DEEP were significantly correlated with each other (P < 0.01). There was also a close correlation among DEHP, DnOP, DNP, DBEP and DCHP (P < 0.01). The results were further confirmed by PCA. To maximize the variance of the loading factors and minimize ambiguity, matrix rotation was employed in this analysis. Two principal components were extracted to simplify the large dataset, explaining 32.3 and 19.2% of the total variance, respectively. The plot of loading factors for the two principal components is outlined in Fig. 3. It suggests that DEHP, DNP, DBEP, DHP, BBP, DnOP and DCHP were mainly loaded in the first component. Meanwhile, the second component was dominated by DMP, DEP, DnBP, DiBP, DEEP, DMGP, DnAP and DMPP. 3.3. Correlations of PAEs with plastic film consumption and soil properties The application of agricultural plastic films was considered as an important origin of PAEs in farmland soils. Therefore, to further discern the potential sources of PAEs, the relationships between PAE burdens in agricultural soils and the consumption of agricultural plastic films in each province were studied and are given in Fig. 4 (Department of Rural Survey National Bureau of Statistics of China, 2012). Before correlation analysis, the soil residue inventories of PAEs in agricultural fields were calculated with the following equation.
R ¼ ALDCsoil
(10) P
where R is the total residue of 15PAEs in the agricultural soils of each province (kg); A is the area of cultivated land in each province or region (National Bureau of Statistics of China, 2013); L is the depth of the soil (20 cm in this study); D is the density of the soil, assumed to be 1.16 g cm3, based on the study of Jia et al. (2009); P and Csoil is the provincial average concentration of 15PAEs. The residue inventories of PAEs in the arable soils of each province were in the range of 0.329e28.0 thousand tons, with a mean value of 9.41 thousand tons. In total, 292 thousand tons of PAEs remained in Chinese agricultural surface soils. In addition, the PAE burdens in soils increased with the consumption of agricultural
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
Fig. 1. Spatial distribution of the
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P 15PAEs in agricultural soils across the Mainland China.
plastic films and a significant correlation was observed between the two variables (R ¼ 0.607, P < 0.001). Soil properties such as SOM and pH are important factors revealing the sources and affecting the behaviors of organic pollutants. In this study, these two parameters were measured for all the soil samples across China (Table 1). The SOM content ranged
from 0.367 to 6.88%, with a mean value of 2.32%. For pH, the mean value was 6.94 and measurements ranged from 4.01 to 8.70. Then, the effect of SOM and pH on the distribution of PAEs in arable soils across China was elucidated. A close relationship was observed P between 15PAEs and SOM (R ¼ 0.185, P ¼ 0.04) (Fig. 5). For individual PAEs, 3 congeners showed significant positive correlations
Fig. 2. Congener profiles of PAEs in arable soils across China.
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Fig. 3. Factor loadings of PAE congeners on two principal components.
with SOM (P < 0.05). The relationship was observed to be the strongest for DnBP (R ¼ 0.301), followed by DiBP (R ¼ 0.269), DNP(R ¼ 0.197). DEHP and DMP showed weak correlations with SOM (R ¼ 0.163 and 0.161, respectively). However, no clear correlation was found between pH and the concentrations of PAEs. 3.4. Non-cancer and carcinogenic risk assessment The risks of toxic PAEs to local residents via non-dietary and dietary routes were estimated based on the concentrations of PAEs in arable soils across China. The results of risk assessment are outlined in Fig. 6. In terms of non-cancer risks via non-dietary and dietary routes, no sample exceeded the recommended allowable daily intake doses of DEP, DnBP, DEHP and DnOP (HI < 1). In addition, the HI values of the total toxic PAEs were all below 1 for both children and adults. The carcinogenic exposure risks of DEHP via non-dietary routes were below 1 106. However, the estimated national carcinogenic risk of DEHP via the dietary route was 7.37 106. In total, 96.7% of the samples across China had carcinogenic risk levels beyond 1 106. Luckily, the carcinogenic risks to human health of DEHP in all the samples were much lower than 1 104. 4. Discussion 4.1. Spatial distribution of PAEs in Chinese agricultural soils P The 15PAEs were detected in all the soils samples, indicating that they are ubiquitous pollutants in agricultural soils across China. The sum of the concentrations of 6 PAEs (DMP, DEP, DnBP, DnOP, DEHP and BBP) in soils were below the recommended value according to Environmental Quality Standard for soil. This suggests that PAE pollution in Chinese arable soils is relatively slight and is within safe limits. A comparison of the PAE concentrations found in this and other studies was conducted and is listed in Table S3 of SI. The national average concentrations of DMP, DEP, DnBP and DEHP in arable soils reported by Hu et al. (2003) ranged from 0.89 to 10.03 mg kg1 (n ¼ 23), which is higher than those found in this study. The differences in the number and properties of sampling sites might be responsible for this observation. The total PAE contents in Chinese soils in other studies were in the range of 0.050e1232 mg kg1. Similar to the findings in this study, relatively higher levels of PAEs in arable soils were also observed in Xinjiang and Guangdong provinces. Except for them, this study also
identified Fujian Province as an area with the greatest PAE pollution. The elevated PAE concentrations found in Xinjiang Province might be attributable to the large consumption of agricultural plastic films, which totaled 0.183 million tons and ranked the second place among 31 provinces or regions in China in 2011 (Department of Rural Survey National Bureau of Statistics of China, 2012). However, the amount of agricultural plastic films utilized in Guangdong and Fujian provinces is not very high (0.044 and 0.058 million tons, respectively). This implies that other sources, such as the application of wastewater irrigation, pesticides and inorganic or organic fertilizers, might be the reason for the elevated concentrations of PAEs in the soils from these two provinces. DEHP is the most common PAE and accounts for 50e60% of the commercial PAEs (Zeng et al., 2008). Therefore, it is not surprising that DEHP was found as the most abundant component in this and previous studies. In addition, the concentrations of DEHP and DnBP in this study were comparable to those in others: they were higher than previously reported values in Tianjin, Huizhou, Dongguan, Nanchang and Hangzhou, China, but lower than values in Guangzhou, Nanjing, Pearl River, Xinjiang and Qingdao, China. It is worth noting that the individual and total concentrations of PAEs determined in arable soils from China (including this and other studies) were all elevated above those in other countries, such as the Netherlands, the UK and Denmark (Vikelsøe et al., 2002; Gibson et al., 2005; Peijnenburg and Struijs, 2006). This implies heavier PAE contamination from human activities in China than abroad. Nevertheless, little information is available on the concentrations of DMGP, DMPP, DEEP, DnAP, DHP, DBEP, DCHP and DNP in other studies, which limited the possibility of comparison among studies. 4.2. Sources of PAEs in Chinese agricultural soils The source of pollutants is of primary interest to the public, because it can provide a detailed understanding of the environmental fates of chemicals. Many studies have suggested that the increased PAEs in agricultural soils might be caused by atmospheric deposition and the application of plastic films, wastewater irrigation, sewage sludge, fertilizers, biosolids and pesticides (Zeng et al., 2008, 2009, 2010; Wang et al., 2013). DEHP, DCHP, BBP, DnOP and DNP are mostly used as plasticizers in the polymer industry due to their flexibility, workability and general handing properties (Zeng et al., 2008). The phthalate content in a finished plastic product could achieve to 10e60% (Gomez-Hens and Aguilar-Caballos, 2003). In addition, DnBP, DiBP and DEP are often applied as solvents in pesticides (Gao et al., 2014), while DEHP, DBP and DMP have been most frequently detected in fertilizers (Mo et al., 2008). It has been previously reported that the contents of PAEs (DMP, DEP, DnBP, BBP, DnOP and DEHP) in some widely used fertilizers in China ranged from 0.001 to 2.80 mg kg1, and the highest values were found in organic fertilizer (Mo et al., 2008). Moreover, the residue levels of the 6 PAEs in sewage sludge ranged from 10 to 114 mg kg1 (Cai et al., 2007). Correlation analysis and PCA are effective statistical techniques that are often employed in the source apportionment of environmental contaminants (Niu et al., 2013a, b). In the study of Zeng et al. (2009), the results of PCA showed that DMP, DEP, DiBP, DnBP, DnAP, DEHP and DnOP shared a common source, while DMPP, DEEP, DNP and DCHP originated from another. However, the 15 PAEs measured in this study were classified into two different groups. One is composed of DEHP, DNP, DBEP, DHP, BBP, DnOP and DCHP, while the other includes DMP, DEP, DnBP, DiBP, DEEP, DMGP, DnAP and DMPP. It is worth noting that the PAEs related to the first component mostly have longer alkyl chains. This suggests that they may originate from the use of plasticizers. To the contrary, most of the PAEs in the second group have low molecular weight. They might derive
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
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soils were greatly impacted by SOM. Similar positive correlations between them were also observed by Zeng et al. (2008). Among the PAE congeners correlated with SOM, DEHP and DNP have a longer/ branching alkyl chain and higher octanol-water partition coefficient (Kow), which might result in their sequestration in SOM. However, the other PAEs affected by SOM were DnBP, DiBP and DMP, which are all short alkyl chain PAEs. It is well-known that wastewater, organic fertilizers and sewage sludge are enriched in organic matter and often employed in agricultural activities for soil fertility. However, these practices can also increase the contents of toxic pollutants, such as metals, OCPs, PCBs, PAHs and PAEs, in arable soils (Stevens et al., 2003; Singh et al., 2004; Cai et al., 2007). Based on the results of PCA, agro-practices such as wastewater irrigation and the application of organic fertilizers and sewage sludge are likely responsible for the strong correlations among DnBP, DiBP and DMP and SOM. Fig. 4. Correlation of the total PAE burdens in Chinese agricultural soils and the consumption of agricultural plastic films.
mainly from the application of pesticides, wastewater irrigation and fertilizers. The production and utilization of agricultural plastic films have increased in recent years in China and this is often recognized as a major source of PAEs in farmland soils (Hu et al., 2003; Department of Rural Survey National Bureau of Statistics of China, 2012). A similar conclusion can also be drawn from this study, which showed that the application of plastic films was the predominant source of PAEs in arable soils across China, followed by wastewater irrigation and fertilizers. This conclusion was further confirmed by the correlations between the soil burdens of PAEs and the consumption of agricultural plastic films. The PAE inventories in each province increased with the application amount of plastic films. This result is in accordance with the study by Hu et al., in which the close relationship between DEHP and the consumption of agricultural plastic films also suggested PAE pollution from the application of plastic films (Hu et al., 2003). Soil properties, such as SOM, have been proved to be important factors governing the environmental behavior of hydrophobic organic pollutants (Niu et al., 2013a, b). As shown in the relationP ship between of PAEs and SOM, the concentrations of 15PAEs in
4.3. Health risks of PAEs in Chinese agricultural soils Humans are exposed to the ubiquitous presence of PAEs on a daily basis. Therefore, it is crucial to estimate the potential risks of PAEs to residents near possible pollutant sources. Compared to the reference doses of PAEs as recommended by the U.S. EPA, the estimated average intake doses of DEP, DnBP, DEHP and DnOP via dietary and non-dietary routes were within acceptable levels (HIs < 1). This indicates that there was an absence of non-cancer risks of PAEs at all sites and they are relatively safe for local inhabitants. Likewise, the carcinogenic risks posed by DEHP in soils via the non-dietary routes were all very low (<106). It is in accordance with the risk assessment of PAEs in urban soils of Beijing, China, where the total cancer risk values were also below 106 (Xia et al., 2011). However, DEHP in 96.7% of the samples posed potential carcinogenic risks to the exposed population via the dietary route. The samples with the highest carcinogenic risks from DEHP were from Fujian, Guangdong, Guangxi, Xinjiang and Hubei provinces. This might be due to widespread plastic film application or intensive agricultural practices, which result in abundant DEHP in soils. Luckily, the carcinogenic risks of DEHP via the dietary route in Chinese arable soils were all within the low category (<104). Given that diet has been proved to be the primary exposure pathway to DEHP for humans (Wormuth et al., 2006), effective
Fig. 5. Relationships between the concentrations of PAE congeners and soil organic matter (SOM).
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their associated health risks. Fujian, Guangdong and Xinjiang provinces were identified as “hot-spots” due to their relatively higher PAE residues, which is consistent with other studies. The major source of PAEs in Chinese arable soils was from the utilization of agricultural plastic films. Agricultural practices for soil fertility, such as the application of irrigation water, sewage sludge, biosolids and fertilizers, were the second most significant source for the soil burdens of PAEs. Both adults and children are relatively safe regarding the non-cancer risks of PAEs in Chinese farmland soils (HIs < 1). The carcinogenic risk of DEHP to inhabitants via nondietary pathways was also in the very low risk category (<106). However, 96.7% of the samples posed some carcinogenic risks to human health (104e106). In general, the agricultural soils across China were slightly polluted by PAEs, and the associated health risks were all within the acceptable levels. These results will provide a full-scale knowledge of the pollution status and health risks of PAEs in arable soils across China, as well as a scientific basis for soil quality assessments and risk avoidance. However, in this study, the bioavailability and bioaccessibility of PAEs were not considered in the risk assessment. Further study is required to focus on the actual contents of PAEs into human bodies and the subsequent risks. Acknowledgment This work was funded in the part by the National Natural Science Foundation of China (No. 21177112, 21320102007) and the Ph.D. Programs Foundation of the Ministry of Education of China (No. 20120101110132). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2014.08.014. References
Fig. 6. Noncarcinogenic risks of PAEs to adults and children via (a) non-dietary and (b) dietary routes, and (c) carcinogenic risks of DEHP via non-dietary and dietary routes.
measures are still warranted to control the levels of DEHP in soils or reduce its transfer from soil to foodstuffs. This action will minimize the threats of PAEs to human health through long-term exposure. 5. Conclusion In this study, 123 soil samples from agricultural fields throughout China were collected and analyzed to fully understand the occurrence of PAE contamination in Chinese arable soils and
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L. Niu et al. / Environmental Pollution 195 (2014) 16e23 Mo, C.H., Cai, Q.Y., Li, Y.H., Zeng, Q.Y., 2008. Occurrence of priority organic pollutants in the fertilizers, China. J. Hazard. Mater. 152, 1208e1213. National Bureau of Statistics of China, 2013. China Statistical Yearbook. China Statistics Press. Niu, L.L., Xu, C., Yao, Y.J., Liu, K., Yang, F.X., Tang, M.L., Liu, W.P., 2013a. Status, influences and risk assessment of hexachlorocyclohexanes in agricultural soils across China. Environ. Sci. Technol. 47, 12140e12147. Niu, L.L., Yang, F.X., Xu, C., Yang, H.Y., Liu, W.P., 2013b. Status of metal accumulation in farmland soils across China: from distribution to risk assessment. Environ. Pollut. 176, 55e62. Peijnenburg, W., Struijs, J., 2006. Occurrence of phthalate esters in the environment of the Netherlands. Ecotoxicol. Environ. Saf. 63, 204e215. Singh, K.P., Mohan, D., Sinha, S., Dalwani, R., 2004. Impact assessment of treated/ untreated wastewater toxicants discharged by sewage treatment plants on health, agricultural, and environmental quality in the wastewater disposal area. Chemosphere 55, 227e255. Stevens, J.L., Northcott, G.L., Stern, G.A., Tomy, G.T., Jones, K.C., 2003. PAHs, PCBs, PCNs, organochlorine pesticides, synthetic musks, and polychlorinated n-alkanes in UK sewage sludge: survey results and implications. Environ. Sci. Technol. 37, 462e467. Sun, J.Q., Huang, J., Zhang, A.P., Liu, W.P., Cheng, W.W., 2013. Occurrence of phthalate esters in sediments in Qiantang River, China and inference with urbanization and river flow regime. J. Hazard. Mater. 248, 142e149. US EPA (United States Environmental Protection Agency), 2013. Mid Atlantic Risk Assessment. Regional Screening Level (RSL) Summary Table. Washington DC.
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Vikelsøe, J., Thomsen, M., Carlsen, L., 2002. Phthalates and nonylphenols in profiles of differently dressed soils. Sci. Total Environ. 296, 105e116. Wang, J., Luo, Y.M., Teng, Y., Ma, W.T., Christie, P., Li, Z.G., 2013. Soil contamination by phthalate esters in Chinese intensive vegetable production systems with different modes of use of plastic film. Environ. Pollut. 180, 265e273. Wang, W.X., Zhang, Y.L., Wang, S.L., Fan, C., Xu, H., 2012. Distributions of phthalic esters carried by total suspended particulates in Nanjing, China. Environ. Monit. Assess. 184, 6789e6798. Wormuth, M., Scheringer, M., Vollenweider, M., Hungerbuhler, K., 2006. What are the sources of exposure to eight frequently used phthalic acid esters in Europeans? Risk Anal. 26, 803e824. Xia, X.H., Yang, L.Y., Bu, Q.W., Liu, R.M., 2011. Levels, distribution, and health risk of phthalate esters in urban soils of Beijing, China. J. Environ. Qual. 40, 1643e1651. Zeng, F., Cui, K.Y., Xie, Z.Y., Wu, L.N., Liu, M., Sun, G.Q., Lin, Y.J., Luo, D.L., Zeng, Z.X., 2008. Phthalate esters (PAEs): emerging organic contaminants in agricultural soils in peri-urban areas around Guangzhou, China. Environ. Pollut. 156, 425e434. Zeng, F., Cui, K.Y., Xie, Z.Y., Wu, L.N., Luo, D.L., Chen, L.X., Lin, Y.J., Liu, M., Sun, G.X., 2009. Distribution of phthalate esters in urban soils of subtropical city, Guangzhou, China. J. Hazard. Mater. 164, 1171e1178. Zeng, F., Lin, Y.J., Cui, K.Y., Wen, J.X., Ma, Y.Q., Chen, H.L., Zhu, F., Ma, Z.L., Zeng, Z.X., 2010. Atmospheric deposition of phthalate esters in a subtropical city. Atmos. Environ. 44, 834e840.
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Status of phthalate esters contamination in agricultural soils across China and associated health risks Lili Niu a, Yang Xu a, Chao Xu b, Lingxiang Yun a, Weiping Liu a, * a 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 b IJRC-PTS, College of Biological and Environmental Engineering, Zhejiang University of Technology, Hangzhou 310032, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 10 April 2014 Received in revised form 6 August 2014 Accepted 13 August 2014 Available online 3 September 2014
The extensive utilization of phthalate-containing products has lead to ubiquitous contamination of phthalate esters (PAEs) in various matrices. However, comprehensive knowledge of their pollution in Chinese farmland and associated risks is still limited. In this study, 15 PAEs were determined in soils from agricultural fields throughout the Mainland China. The concentrations of S15PAEs were in the range of 75.0e6369 mg kg1. Three provinces (i.e., Fujian, Guangdong and Xinjiang, China) showed the highest loadings of PAEs. Bis(2-Ethylhexyl) phthalate (DEHP) was found as the most abundant component and P contributed 71.5% to the 15PAEs. The major source of PAEs in arable soils was associated with the application of agricultural plastic films, followed by the activities for soil fertility. Furthermore, the noncancer and carcinogenic risks of target PAEs were estimated. The hazard indexes (HIs) of PAEs in all samples were below 1 and the carcinogenic risk levels were all within 104. Results from this study will provide valuable information for Chinese agricultural soil management and risk avoidance. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Phthalate ester Agricultural soil Spatial distribution Potential source Human health risk
1. Introduction Soil is an important environmental medium and a major reservoir for a diverse range of pollutants. With the rampant development of agriculture and industry, the soil environment has been extensively deteriorated. Many toxic pollutants have been introduced and remain in soils, such as organochlorine pesticides (OCPs), polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), heavy metals and phthalate esters (PAEs) (Cai et al., 2008; Niu et al., 2013a, b). Among these persistent toxic substances (PTSs), PAEs have been demonstrated to be the most abundant organic contaminant in soils (Cai et al., 2008). Phthalate esters, a group of flexible, pliable and elastic chemicals, are widely used in plastic products, pesticides, cosmetics and personal care products (Gomez-Hens and Aguilar-Caballos, 2003; Hu et al., 2003). It has been estimated that the global production and consumption of PAEs is approximately 6.0 million tons$year1 (Arbeitsgemeinschaft PVC and Umwelt e. V, 2006). Because of the widespread usage of phthalate-containing products, the residues of PAEs have been routinely detected in various matrices, such as soil,
* Corresponding author. E-mail address: [email protected] (W. Liu). http://dx.doi.org/10.1016/j.envpol.2014.08.014 0269-7491/© 2014 Elsevier Ltd. All rights reserved.
water, air and sediments (Cai et al., 2008; Wang et al., 2012; Sun et al., 2013; Liu et al., 2014). The application of agricultural plastic films is one of the important sources of PAEs in farmland soils. In 2011, the amount of plastic films applied agriculturally in China was approximately 2.29 million tons and the mulching area reached 19.8 million hectares (Department of Rural Survey National Bureau of Statistics of China, 2012). Another significant source of PAEs in farmland soil is associated with agricultural practices such as the application of sewage sludge, fertilizers, biosolids and irrigation wastewater, among others (Cai et al., 2007; Mo et al., 2008). In addition, the concentrations of PAEs in soils can also be influenced by atmospheric deposition, soil communities and meteorological conditions (Zeng et al., 2008, 2010). Although PAEs are not as toxic as persistent organic pollutants (POPs), their ubiquitous existence poses great threats to humans. A phthalate incident that happened in Taiwan in 2011 aroused strong public concerns on the adverse effects of PAEs on human health (Li and Ko, 2012). Many epidemiology and toxicology studies have demonstrated that some PAEs, such as bis(2-Ethylhexyl) phthalate (DEHP), dibutyl phthalate (DnBP), benzyl butyl phthalate (BBP), diethyl phthalate (DEP) and dihexyl phthalate (DHP), are endocrine disrupting compounds (Gomez-Hens and Aguilar-Caballos, 2003). Moreover, dimethyl phthalate (DMP), DEP, DnBP, BBP, DEHP and di-
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
n-octyl phthalate (DnOP) have been classified as priority environmental pollutants by the U.S. Environmental Protection Agency (U.S. EPA) (Keith and Telliard, 1979). Therefore, numerous studies have addressed the potential risks, occurrence and sources of PAEs in diverse media (Hu et al., 2003; Zeng et al., 2008; Wang et al., 2013; Kranich et al., 2014). However, previous studies have largely focused on a regional scale. Although a national investigation was carried out in 2003, the information is still not sufficient for well understanding the PAE pollution in Chinese arable soils due to the limited number of sites and PAE species analyzed in that study (Hu et al., 2003). In addition, the potential risks of PAEs to human health via multiple pathways have been infrequently estimated. Therefore, a full-scale study on the status of PAE pollution in farmland soils at the national scale and associated health risks are of considerable significance for setting strategies to minimize their pollution and exposure risks. In this study, 15 PAEs were measured in agricultural soils collected from 123 regions throughout China. Our aims were to characterize the spatial distribution features and congener profiles of PAEs, as well as to discern their possible sources. In addition, the non-cancer and carcinogenic risks of toxic PAEs in soils were also estimated for local residents via dietary and non-dietary routes. These results will provide baseline information for soil quality assessments and rational farming practices, thus protecting human health. 2. Materials and methods 2.1. Sample collection In total, 123 soil samples were collected from agricultural fields in 31 provinces, municipalities or autonomous regions across China in April and May of 2013. The sampling sites were chosen according to the distribution of farmland soils in China (National Bureau of Statistics of China, 2013) and located by GPS (Fig. S1 in Supporting Information, SI). Before collection, overlying vegetation was thoroughly excluded. At each sampling site, five agricultural soil sub-samples (0e20 cm) were collected with a pre-cleaned stainless steel scoop and mixed to form a composite sample in a pre-cleaned aluminum foil bag. Then, the soil samples were immediately transported to the laboratory and stored at 20 C until analysis. Soils for pH measurement were freeze-dried, ground and passed through a stainless steel sieve (2 mm). Then, the remaining soils were further sieved through a 0.154 mm sieve for the analysis of PAEs and soil organic matter (SOM).
17
individual PAEs to quantify the amounts of analytes in samples using the internal calibration method. 2.3. Quality control and quality assurance During the analytical procedures, all data were subjected to strict quality control and quality assurance measures. Blank samples were included with every 15 field samples to check for the interference and contamination. Only small levels of DnBP, DiBP and DEHP were detected in procedural blank and ranged from 0.996 to 3.20 mg kg1. Then the concentrations of PAEs in soil samples were all blank corrected. All samples were spiked with surrogate standards to monitor the recovery, which ranged from 80.7 to 99.9%. The recoveries of the 15 PAEs in the spiked blank and spiked matrix samples ranged from 76.7 to 105.1 and 75.2 to 101.9%, respectively. PAE calibration standards of were employed to calibrate the instrument every day. The limits of detection (LOD) of individual PAEs were calculated as three times the signal-to-noise ratio and fell in the range of 0.008e0.295 mg kg1. 2.4. Analyses of soil organic matter and pH A pH electrode was used to determine soil pH with a soil/water (CO2-freed deionized) ratio of 1:2.5 (w/v). The soil organic matter content was measured by dichromate digestion at 180 C according to Lu (2000). 2.5. Health risk assessment The non-cancer and carcinogenic risks of PAEs were estimated according to the methods recommended by the U.S. EPA (2013). Because the local residents eat their own self-produced food, risks via non-dietary and dietary pathways were all involved. Among the individual PAE congeners studied, DEP, DnBP and DnOP were recognized as non-cancer compounds with respect to human health, while DEHP did present carcinogenic risk. In the non-cancer risk assessments of DEP, DnBP, DEHP and DnOP, their average daily doses (ADDs, mg kg1 day1) via dietary (only considering food grown in soils) and non-dietary (soil ingestion, dermal contact and inhalation) routes were calculated as follows. ADDintake ¼
Csoil BAF IRF EF ED CF BW AT
(1)
where Csoil is the concentration of target chemical in farmland soil (mg kg1); BAF is the bioaccumulation factor of individual PAEs from soil to foodstuff (vegetables and grains); IRF is the daily intake rate of food by inhabitants (mg/day), where the IRF for children is supposed to be 1/3 of that for adults; EF is the exposure frequency (days yr1); ED is the exposure duration (yr); BW is the body weight (kg); AT is the average lifetime (days); and CF is the conversion factor (kg mg1). ADDingest ¼
Csoil IRS EF ED CF BW AT
(2)
where IRS is the soil ingestion rate (mg day1); 2.2. Sample extraction and analysis A standard mixture of 15 PAEs, including DMP, DEP, diisobutyl phthalate (DiBP), DnBP, bis(2-Methoxyethyl) phthalate (DMGP), bis(4-Methyl-2-pentyl) phthalate (DMPP), bis(2-Ethoxyethyl) phthalate (DEEP), dipentyl phthalate (DnAP), DHP, BBP, bis(2-n-butoxyethyl) phthalate (DBEP), dicyclohexyl phthalate (DCHP), DEHP, DnOP and dinonyl phthalate (DNP) and a surrogate standard mixture, including dibenzyl phthalate, diphenyl isophthalate and diphenyl phthalate, were purchased from AccuStandard, Inc. (New Haven, CT, US). A solid internal standard of benzyl benzoate (99.5% purity) was acquired from Dr. Ehrenstorfer (Augsburg, Germany). Other solvents and reagents of residue analysis grade were obtained from J&K Chemical Ltd. (Beijing, China). Neutral silica gel, aluminum, florisil and anhydrous granular sodium sulfate (Na2SO4) were activated prior to use. After being spiked with surrogate standards of ibenzyl phthalate, diphenyl isophthalate and diphenyl phthalate, the soil samples containing activated copper granules were extracted with dichloromethane (DCM) using a Soxhlet apparatus. The extract was then solvent-exchanged into hexane and cleaned on a column filled with Na2SO4, florisil, neutral silica gel, neutral aluminum and Na2SO4 (from bottom to top). The column was first eluted with 20 mL of hexane and 70 mL of hexane/DCM (7/3, v/v). Then, the target analytes were recovered in the final eluate with 40 mL of hexane/acetone (4:1, v/v). After being concentrated and reduced to 0.5 mL, the extracts were spiked with the internal standard before instrumental analysis. The quantitative analysis of PAEs was carried out on an Agilent 7890 GC coupled to an Agilent 5975C MS (Agilent Technologies, Avondale, PA, USA). An HP-5MS capillary column (30 m 320 mm 0.25 mm film thickness, Agilent Technologies Inc., Santa Clara, CA) was used for separation. The selective ion monitoring mode and electron impact were employed and the temperature of the transfer line and the ion source were 280 C and 230 C, respectively. The gas chromatography temperature programs were as follows: initial temperate 80 C for 1.0 min, increase at a rate of 10 C min1 to 180 C (hold for 1.0 min), ramp at 2 C min1 to 260 C (hold for 1.0 min) and finally ramp to 300 C at 2 C min1 (hold for 5 min). The carrier helium gas was kept at a rate of 0.8 mL min1. A five-point calibration curve was made for
ADDdermal ¼
Csoil SA AF ABS EF ED CF BW AT 2
(3)
1
where SA is the soil surface area (cm day ); AF is the soil adherence factor (mg cm2); and ABS is the fraction of contaminant absorbed dermally from the soil (unitless). ADDinhale ¼
Csoil EF ED 103 PEF AT
(4)
where PEF is the particulate emission factor (m3 kg1) and a default PEF equal to 1.36 109 m3 kg1 was used. The hazard index (HI), which represents the total risks of a certain PAE in soil to human health through multiple exposure pathways, was calculated with the following equations. HQ ¼ HI ¼
ADD RfD
X
HQ i
(5) (6)
where HQ is the hazard quotient; i represents the different exposure pathways; RfD (mg kg1 day1) is defined as the daily maximum permissible level of contaminants, including the reference dose for ingestion and intake of contaminated food (RfDo, mg kg1 day1), the reference dose for dermal contact (RfDABS ¼ RfDo ABSGI , mg kg1 day1) and the reference dose of inhalation (RfCi, mg m3); ABSGI is the fraction of pollutant absorbed in the gastrointestinal tract (unitless). The local inhabitants are considered to be exposed to non-cancer risks if the value of HI is greater than 1. The ADD of DEHP via dietary pathways for carcinogenic risk assessment was calculated using Eq. (1) and these via non-dietary pathways were calculated based on the following.
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ADDingest
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
Csoil EF IFSadj CF ¼ AT
(7)
where IFSadj is the age-adjusted soil ingestion rate (mg year kg1 day1). ADDdermal ¼
Csoil EF DFSadj ABS CF AT
(8)
where DFSadj is the age-adjusted soil dermal contact factor (mg year kg ADDinhale ¼
1
1
day
Csoil EF ED 103 PEF AT
)
(9)
The carcinogenic risks of DEHP were appraised using ADD multiplied by a slope factor (SF), which is composed of oral slope factors (SFO, (mg kg1 day1)1) for ingestion, dermal contact (SFO ABSGI (mg kg1 day1)1) and inhalation unit risk (IUR, (mg m3)1). The estimated carcinogenic risks may be considered very low if the value of risk is less than 106, low in the range of 106e104, moderate from 104 to 103, high from 103 to 101 and very high if the value is greater than 101. The values of parameters for non-cancer and carcinogenic risks are listed in Table S1 of SI.
P distribution of 15PAEs in agricultural soils across China. As shown in Fig. 1, the highest contents of total PAEs in soils were observed in Fujian, Guangdong and Xinjiang provinces. The sites in Chongqing City, Hubei and Henan provinces also showed higher P levels of 15PAEs in soils. However, the total PAE levels were relatively low in Northeast China. The relative contributions of individual PAEs in Chinese arable soils were further calculated and the congener profiles in each province are shown in Fig. 2. DEHP was the most abundant and its national average contribution to P 15PAEs was 71.5%, with the highest value of 91.51% in Fujian Province. DiBP was the second most dominant PAE in soils, followed by DNP and DnBP, which contributed 8.22, 7.22 and 6.89% to P 15PAEs, respectively. In total, DEHP, DiBP, DnBP and DNP together P 15PAEs concentrations. The accounted for 88.5e98.3% of the highest fraction of these 4 PAE congeners was also observed in Fujian Province. 3.2. Source analysis of PAEs
3. Results 3.1. Concentrations and spatial distribution of PAEs in Chinese agricultural soils A descriptive statistical summary of individual and total PAE concentrations in Chinese agricultural soils is shown in Table 1. Phthalate esters were detected in all the soil samples analyzed. The total concentrations of 15 PAEs in soils varied considerably and ranged from 75.0 to 6369 mg kg1, with a mean value of 1088 mg kg1. With regard to individual PAEs, DMP, DEP, DiBP, DnBP and DMGP were observed in all the samples, while the detectable frequencies of DMPP, DEEP, DnAP, DHP, BBP, DBEP, DCHP, DEHP, DnOP and DNP were 5.79, 16.5, 9.09, 57.0, 61.2, 95.9, 95.9, 95.9, 97.5, 99.2 and 99.2%, respectively. Among the analyzed PAE congeners, DEHP exhibited the highest concentration, followed by DiBP, DnBP and DNP, whose average residue levels were 821, 74.7, 65.8 and 69.6 mg kg1, respectively. The sum of the concentration of 6 PAEs (DMP, DEP, DnBP, DnOP, DEHP and BBP) ranged from 0.032 to 6.29 mg kg1, which were within the less stringent grade II limits for PAEs (10 mg kg1) in arable soils recommended by the Environmental Quality Standard for soil in China (GB-15618-2008) (China National Environmental Protection Agency, 2008). To provide a direct insight into PAE contamination, a geographic information system (GIS) was employed to map the spatial
Table 1 Descriptive statistical summary of individual concentrations of PAEs (mg/kg) and soil properties in agricultural soils across China.
DMP DEP DiBP DnBP DMGP DMPP DEEP DnAP DHP BBP DBEP DCHP DEHP DnOP DNP P PAEs OM(%) pH
Mean
Min
Max
Median
SD
CV (%)
DF (%)
14.8 2.79 74.7 65.8 4.96 ND ND ND 0.068 0.042 7.94 5.84 821 19.8 69.6 1088 2.32 6.94
1.19 0.236 4.93 4.04 0.597 ND ND ND ND ND ND ND ND ND ND 75.0 0.367 4.01
55.2 24.3 335 457 12.3 0.844 1.53 8.56 0.505 0.276 65.0 40.9 6218 298 606 6369 6.88 8.70
12.8 2.22 59.9 51.7 4.76 ND ND ND 0.029 0.037 6.55 4.47 562 14.0 49.5 847 2.06 7.01
9.56 2.49 47.1 54.2 2.09 0.118 0.268 0.784 0.094 0.044 8.06 5.63 756 30.0 78.1 794 1.27 0.981
64.7 89.1 63.1 82.3 42.2 408 197 694 139 106 102 96.4 92.1 151 112 72.9 5.48 14.1
100 100 100 100 100 5.79 16.5 9.09 57.0 61.2 95.9 95.9 97.5 99.2 99.2 100
Correlation analysis (CA) and principal component analysis (PCA) were conducted to identify the potential sources of PAEs in Chinese arable soils. Table S2 of SI lists the correlation coefficient matrixes among the individual concentrations of PAEs. DEHP P showed the strongest relationship with 15PAEs (R ¼ 0.959) at the 0.01 significance level, followed by DnBP (R ¼ 0.495) and DnOP (R ¼ 0.479). Of the PAE congeners analyzed, DMP, DEP, DiBP, DnBP, DMGP and DEEP were significantly correlated with each other (P < 0.01). There was also a close correlation among DEHP, DnOP, DNP, DBEP and DCHP (P < 0.01). The results were further confirmed by PCA. To maximize the variance of the loading factors and minimize ambiguity, matrix rotation was employed in this analysis. Two principal components were extracted to simplify the large dataset, explaining 32.3 and 19.2% of the total variance, respectively. The plot of loading factors for the two principal components is outlined in Fig. 3. It suggests that DEHP, DNP, DBEP, DHP, BBP, DnOP and DCHP were mainly loaded in the first component. Meanwhile, the second component was dominated by DMP, DEP, DnBP, DiBP, DEEP, DMGP, DnAP and DMPP. 3.3. Correlations of PAEs with plastic film consumption and soil properties The application of agricultural plastic films was considered as an important origin of PAEs in farmland soils. Therefore, to further discern the potential sources of PAEs, the relationships between PAE burdens in agricultural soils and the consumption of agricultural plastic films in each province were studied and are given in Fig. 4 (Department of Rural Survey National Bureau of Statistics of China, 2012). Before correlation analysis, the soil residue inventories of PAEs in agricultural fields were calculated with the following equation.
R ¼ ALDCsoil
(10) P
where R is the total residue of 15PAEs in the agricultural soils of each province (kg); A is the area of cultivated land in each province or region (National Bureau of Statistics of China, 2013); L is the depth of the soil (20 cm in this study); D is the density of the soil, assumed to be 1.16 g cm3, based on the study of Jia et al. (2009); P and Csoil is the provincial average concentration of 15PAEs. The residue inventories of PAEs in the arable soils of each province were in the range of 0.329e28.0 thousand tons, with a mean value of 9.41 thousand tons. In total, 292 thousand tons of PAEs remained in Chinese agricultural surface soils. In addition, the PAE burdens in soils increased with the consumption of agricultural
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
Fig. 1. Spatial distribution of the
19
P 15PAEs in agricultural soils across the Mainland China.
plastic films and a significant correlation was observed between the two variables (R ¼ 0.607, P < 0.001). Soil properties such as SOM and pH are important factors revealing the sources and affecting the behaviors of organic pollutants. In this study, these two parameters were measured for all the soil samples across China (Table 1). The SOM content ranged
from 0.367 to 6.88%, with a mean value of 2.32%. For pH, the mean value was 6.94 and measurements ranged from 4.01 to 8.70. Then, the effect of SOM and pH on the distribution of PAEs in arable soils across China was elucidated. A close relationship was observed P between 15PAEs and SOM (R ¼ 0.185, P ¼ 0.04) (Fig. 5). For individual PAEs, 3 congeners showed significant positive correlations
Fig. 2. Congener profiles of PAEs in arable soils across China.
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L. Niu et al. / Environmental Pollution 195 (2014) 16e23
Fig. 3. Factor loadings of PAE congeners on two principal components.
with SOM (P < 0.05). The relationship was observed to be the strongest for DnBP (R ¼ 0.301), followed by DiBP (R ¼ 0.269), DNP(R ¼ 0.197). DEHP and DMP showed weak correlations with SOM (R ¼ 0.163 and 0.161, respectively). However, no clear correlation was found between pH and the concentrations of PAEs. 3.4. Non-cancer and carcinogenic risk assessment The risks of toxic PAEs to local residents via non-dietary and dietary routes were estimated based on the concentrations of PAEs in arable soils across China. The results of risk assessment are outlined in Fig. 6. In terms of non-cancer risks via non-dietary and dietary routes, no sample exceeded the recommended allowable daily intake doses of DEP, DnBP, DEHP and DnOP (HI < 1). In addition, the HI values of the total toxic PAEs were all below 1 for both children and adults. The carcinogenic exposure risks of DEHP via non-dietary routes were below 1 106. However, the estimated national carcinogenic risk of DEHP via the dietary route was 7.37 106. In total, 96.7% of the samples across China had carcinogenic risk levels beyond 1 106. Luckily, the carcinogenic risks to human health of DEHP in all the samples were much lower than 1 104. 4. Discussion 4.1. Spatial distribution of PAEs in Chinese agricultural soils P The 15PAEs were detected in all the soils samples, indicating that they are ubiquitous pollutants in agricultural soils across China. The sum of the concentrations of 6 PAEs (DMP, DEP, DnBP, DnOP, DEHP and BBP) in soils were below the recommended value according to Environmental Quality Standard for soil. This suggests that PAE pollution in Chinese arable soils is relatively slight and is within safe limits. A comparison of the PAE concentrations found in this and other studies was conducted and is listed in Table S3 of SI. The national average concentrations of DMP, DEP, DnBP and DEHP in arable soils reported by Hu et al. (2003) ranged from 0.89 to 10.03 mg kg1 (n ¼ 23), which is higher than those found in this study. The differences in the number and properties of sampling sites might be responsible for this observation. The total PAE contents in Chinese soils in other studies were in the range of 0.050e1232 mg kg1. Similar to the findings in this study, relatively higher levels of PAEs in arable soils were also observed in Xinjiang and Guangdong provinces. Except for them, this study also
identified Fujian Province as an area with the greatest PAE pollution. The elevated PAE concentrations found in Xinjiang Province might be attributable to the large consumption of agricultural plastic films, which totaled 0.183 million tons and ranked the second place among 31 provinces or regions in China in 2011 (Department of Rural Survey National Bureau of Statistics of China, 2012). However, the amount of agricultural plastic films utilized in Guangdong and Fujian provinces is not very high (0.044 and 0.058 million tons, respectively). This implies that other sources, such as the application of wastewater irrigation, pesticides and inorganic or organic fertilizers, might be the reason for the elevated concentrations of PAEs in the soils from these two provinces. DEHP is the most common PAE and accounts for 50e60% of the commercial PAEs (Zeng et al., 2008). Therefore, it is not surprising that DEHP was found as the most abundant component in this and previous studies. In addition, the concentrations of DEHP and DnBP in this study were comparable to those in others: they were higher than previously reported values in Tianjin, Huizhou, Dongguan, Nanchang and Hangzhou, China, but lower than values in Guangzhou, Nanjing, Pearl River, Xinjiang and Qingdao, China. It is worth noting that the individual and total concentrations of PAEs determined in arable soils from China (including this and other studies) were all elevated above those in other countries, such as the Netherlands, the UK and Denmark (Vikelsøe et al., 2002; Gibson et al., 2005; Peijnenburg and Struijs, 2006). This implies heavier PAE contamination from human activities in China than abroad. Nevertheless, little information is available on the concentrations of DMGP, DMPP, DEEP, DnAP, DHP, DBEP, DCHP and DNP in other studies, which limited the possibility of comparison among studies. 4.2. Sources of PAEs in Chinese agricultural soils The source of pollutants is of primary interest to the public, because it can provide a detailed understanding of the environmental fates of chemicals. Many studies have suggested that the increased PAEs in agricultural soils might be caused by atmospheric deposition and the application of plastic films, wastewater irrigation, sewage sludge, fertilizers, biosolids and pesticides (Zeng et al., 2008, 2009, 2010; Wang et al., 2013). DEHP, DCHP, BBP, DnOP and DNP are mostly used as plasticizers in the polymer industry due to their flexibility, workability and general handing properties (Zeng et al., 2008). The phthalate content in a finished plastic product could achieve to 10e60% (Gomez-Hens and Aguilar-Caballos, 2003). In addition, DnBP, DiBP and DEP are often applied as solvents in pesticides (Gao et al., 2014), while DEHP, DBP and DMP have been most frequently detected in fertilizers (Mo et al., 2008). It has been previously reported that the contents of PAEs (DMP, DEP, DnBP, BBP, DnOP and DEHP) in some widely used fertilizers in China ranged from 0.001 to 2.80 mg kg1, and the highest values were found in organic fertilizer (Mo et al., 2008). Moreover, the residue levels of the 6 PAEs in sewage sludge ranged from 10 to 114 mg kg1 (Cai et al., 2007). Correlation analysis and PCA are effective statistical techniques that are often employed in the source apportionment of environmental contaminants (Niu et al., 2013a, b). In the study of Zeng et al. (2009), the results of PCA showed that DMP, DEP, DiBP, DnBP, DnAP, DEHP and DnOP shared a common source, while DMPP, DEEP, DNP and DCHP originated from another. However, the 15 PAEs measured in this study were classified into two different groups. One is composed of DEHP, DNP, DBEP, DHP, BBP, DnOP and DCHP, while the other includes DMP, DEP, DnBP, DiBP, DEEP, DMGP, DnAP and DMPP. It is worth noting that the PAEs related to the first component mostly have longer alkyl chains. This suggests that they may originate from the use of plasticizers. To the contrary, most of the PAEs in the second group have low molecular weight. They might derive
L. Niu et al. / Environmental Pollution 195 (2014) 16e23
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soils were greatly impacted by SOM. Similar positive correlations between them were also observed by Zeng et al. (2008). Among the PAE congeners correlated with SOM, DEHP and DNP have a longer/ branching alkyl chain and higher octanol-water partition coefficient (Kow), which might result in their sequestration in SOM. However, the other PAEs affected by SOM were DnBP, DiBP and DMP, which are all short alkyl chain PAEs. It is well-known that wastewater, organic fertilizers and sewage sludge are enriched in organic matter and often employed in agricultural activities for soil fertility. However, these practices can also increase the contents of toxic pollutants, such as metals, OCPs, PCBs, PAHs and PAEs, in arable soils (Stevens et al., 2003; Singh et al., 2004; Cai et al., 2007). Based on the results of PCA, agro-practices such as wastewater irrigation and the application of organic fertilizers and sewage sludge are likely responsible for the strong correlations among DnBP, DiBP and DMP and SOM. Fig. 4. Correlation of the total PAE burdens in Chinese agricultural soils and the consumption of agricultural plastic films.
mainly from the application of pesticides, wastewater irrigation and fertilizers. The production and utilization of agricultural plastic films have increased in recent years in China and this is often recognized as a major source of PAEs in farmland soils (Hu et al., 2003; Department of Rural Survey National Bureau of Statistics of China, 2012). A similar conclusion can also be drawn from this study, which showed that the application of plastic films was the predominant source of PAEs in arable soils across China, followed by wastewater irrigation and fertilizers. This conclusion was further confirmed by the correlations between the soil burdens of PAEs and the consumption of agricultural plastic films. The PAE inventories in each province increased with the application amount of plastic films. This result is in accordance with the study by Hu et al., in which the close relationship between DEHP and the consumption of agricultural plastic films also suggested PAE pollution from the application of plastic films (Hu et al., 2003). Soil properties, such as SOM, have been proved to be important factors governing the environmental behavior of hydrophobic organic pollutants (Niu et al., 2013a, b). As shown in the relationP ship between of PAEs and SOM, the concentrations of 15PAEs in
4.3. Health risks of PAEs in Chinese agricultural soils Humans are exposed to the ubiquitous presence of PAEs on a daily basis. Therefore, it is crucial to estimate the potential risks of PAEs to residents near possible pollutant sources. Compared to the reference doses of PAEs as recommended by the U.S. EPA, the estimated average intake doses of DEP, DnBP, DEHP and DnOP via dietary and non-dietary routes were within acceptable levels (HIs < 1). This indicates that there was an absence of non-cancer risks of PAEs at all sites and they are relatively safe for local inhabitants. Likewise, the carcinogenic risks posed by DEHP in soils via the non-dietary routes were all very low (<106). It is in accordance with the risk assessment of PAEs in urban soils of Beijing, China, where the total cancer risk values were also below 106 (Xia et al., 2011). However, DEHP in 96.7% of the samples posed potential carcinogenic risks to the exposed population via the dietary route. The samples with the highest carcinogenic risks from DEHP were from Fujian, Guangdong, Guangxi, Xinjiang and Hubei provinces. This might be due to widespread plastic film application or intensive agricultural practices, which result in abundant DEHP in soils. Luckily, the carcinogenic risks of DEHP via the dietary route in Chinese arable soils were all within the low category (<104). Given that diet has been proved to be the primary exposure pathway to DEHP for humans (Wormuth et al., 2006), effective
Fig. 5. Relationships between the concentrations of PAE congeners and soil organic matter (SOM).
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their associated health risks. Fujian, Guangdong and Xinjiang provinces were identified as “hot-spots” due to their relatively higher PAE residues, which is consistent with other studies. The major source of PAEs in Chinese arable soils was from the utilization of agricultural plastic films. Agricultural practices for soil fertility, such as the application of irrigation water, sewage sludge, biosolids and fertilizers, were the second most significant source for the soil burdens of PAEs. Both adults and children are relatively safe regarding the non-cancer risks of PAEs in Chinese farmland soils (HIs < 1). The carcinogenic risk of DEHP to inhabitants via nondietary pathways was also in the very low risk category (<106). However, 96.7% of the samples posed some carcinogenic risks to human health (104e106). In general, the agricultural soils across China were slightly polluted by PAEs, and the associated health risks were all within the acceptable levels. These results will provide a full-scale knowledge of the pollution status and health risks of PAEs in arable soils across China, as well as a scientific basis for soil quality assessments and risk avoidance. However, in this study, the bioavailability and bioaccessibility of PAEs were not considered in the risk assessment. Further study is required to focus on the actual contents of PAEs into human bodies and the subsequent risks. Acknowledgment This work was funded in the part by the National Natural Science Foundation of China (No. 21177112, 21320102007) and the Ph.D. Programs Foundation of the Ministry of Education of China (No. 20120101110132). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2014.08.014. References
Fig. 6. Noncarcinogenic risks of PAEs to adults and children via (a) non-dietary and (b) dietary routes, and (c) carcinogenic risks of DEHP via non-dietary and dietary routes.
measures are still warranted to control the levels of DEHP in soils or reduce its transfer from soil to foodstuffs. This action will minimize the threats of PAEs to human health through long-term exposure. 5. Conclusion In this study, 123 soil samples from agricultural fields throughout China were collected and analyzed to fully understand the occurrence of PAE contamination in Chinese arable soils and
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