Pedosphere 27(3): 439–451, 2017 doi:10.1016/S1002-0160(17)60340-0 ISSN 1002-0160/CN 32-1315/P c 2017 Soil Science Society of China ⃝ Published by Elsevier B.V. and Science Press
Contamination of Phthalate Esters in Vegetable Agriculture and Human Cumulative Risk Assessment CHEN Ning1,2 , SHUAI Wenjuan1,2 , HAO Xinmei3 , ZHANG Huichun4 , ZHOU Dongmei1 and GAO Juan1,∗ 1 Key
Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008 (China) 2 University of Chinese Academy of Sciences, Beijing 100049 (China) 3 College of Water Resources and Civil Engineering, China Agricultural University, Beijing 100083 (China) 4 Department of Civil and Environmental Engineering, Temple University, PA 19122 (USA) (Received February 8, 2017; revised April 1, 2017)
ABSTRACT Phthalate esters (PAEs), which can disturb human endocrine system, have been widely detected in vegetable greenhouse agriculture in China. To investigate the effects of environmental factors on PAEs in soils, pollution sources were identified, and the cumulative risks of PAEs to humans through vegetables in the diet were evaluated in this study. Ninety-eight vegetable samples were collected from 10 markets along with 128 vegetable and 111 soil samples from agricultural greenhouses and open field. All soil and vegetable samples were contaminated with PAEs, and the total concentrations of the 5 PAEs, including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), were in the ranges of 0.26–2.53 mg kg−1 for soils and 0.95–8.09 mg kg−1 for vegetables. Three components extracted from principle component analysis could explain 51.2%, 19.8%, and 15.3% of the total variance of the 5 PAEs in soils, which may represent three major sources of PAEs, i.e., wastewater irrigation, application of fertilizers and pesticides, and plastic film. Long-term greenhouse cultivation could accumulate DEHP in soils, and a higher soil FeOx content reduced the DnBP concentration. Based on a survey of vegetables in the diet, the hazard index of PAEs was < 0.15 for individuals in different cities. The exposure of PAEs through vegetable intake was higher than the total exposure from other food stuffs, inhalation, and dermal absorption. More attention should be given to controlling PAEs in greenhouse vegetables. Key Words:
average daily intake, dietary survey, environmental factors, greenhouse agriculture, hazard index
Citation: Chen N, Shuai W J, Hao X M, Zhang H C, Zhou D M, Gao J. 2017. Contamination of phthalate esters in vegetable agriculture and human cumulative risk assessment. Pedosphere. 27(3): 439–451.
INTRODUCTION Phthalate esters (PAEs) are a group of 1,2-benzene dicarboxylate esters that are widely applied in commercial products, including foods, cosmetics, cleaning products, building materials, polyvinyl chloride plastics, and toys (Rudel and Perovich, 2009; Wittassek et al., 2011; Dodson et al., 2012). Since no covalent bond exists between PAEs and the surrounding matrix, these compounds easily leach into the environment and have been ubiquitously detected (Tropea et al., 2010; Guo and Wu, 2011; Guo et al., 2011). It has been proven that PAEs are endocrine disrupters, which can interrupt reproductive system development (Mylchreest et al., 1999; Wang et al., 2012). Based on animal studies, di-n-butyl phthalate (DnBP) can interfere with androgen levels in rats during the period of reproduction gestation (Mylchreest et al., ∗ Corresponding
author. E-mail:
[email protected].
1999). A study by Wang et al. (2012) reported that di2-ethylhexyl phthalate (DEHP) could cause malfunction in the antral follicles of mouse ovaries. Thus, PAEs have been banned for use in toys and children clothes by the Council of the European Union (ECHA, 2016) and the U.S. Consumer Product Safety Commission (CPSC, 2008). Greenhouse agriculture in China began in the 1960s and grew vigorously since the 1970s–1980s all over the country, with 1 000 ha greenhouse area for agriculture purpose in 2007 (He and Ma, 2007). The temperature and humidity inside greenhouses are higher than those outside, especially in winter and spring, and vegetables inside can grow faster and have higher yields. The reported data showed that the total concentration of PAEs in agricultural soils was in the range of 0.51–7.16 mg kg−1 , including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), Dn-
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BP, DEHP, and benzyl butyl phthalate (BBP), among which DnBP and DEHP were the two most abundant PAEs detected in the soils (Ma et al., 2015). Vegetables grown in greenhouses can take up PAEs from soil through their roots and from the atmosphere through their leaves. Xiao et al. (2012) showed that the total concentration of PAEs in the vegetables from typical greenhouse agriculture was 0.46–12.0 mg kg−1 . The PAE levels in soils are correlated to soil properties. It has been reported that soil organic matter (SOM) can sequestrate hydrophobic compounds during the course of aging, and that higher amounts of SOM sequestrate more organic pollutants (Nam et al., 1998). The concentrations of dyes, pesticides, polychlorinated biphenyls, and polycyclic aromatic hydrocarbons in soils have been reported to increase with higher SOM content (Chiou et al., 1983; Sheng et al., 2001; Chen et al., 2003). The clay-silt content (particle size < 50 µm) is reported to play an important role in interacting with organic pollutants (Gillott, 1987; Wang et al., 2011). In our previous research, DEP was shown to intercalate into the interlayer spacings of montmorillonite clay minerals (Wu et al., 2015). The content of iron oxides (FeOx ) in soils has been defined as an index of soil activity (Patrick and Khalid, 1974; Waychunas et al., 1993; Bowell, 1994), as FeOx can effectively react with organic pollutants in soils. Soil FeOx can facilitate adsorption, oxidation, heterogeneous photoFenton reactions, and microorganism metabolisms to degrade organic compounds (Beller et al., 1992; Kwan and Voelker, 2002; Hug and Leupin, 2003; Barreiro et al., 2007). However, correlations between organic pollutants and soil properties have been lightly investigated, and most of the studies only focused on the impact of SOM within small regions with a bivariate correlation (Chiou et al., 1983; Sheng et al., 2001; Chen et al., 2003). To understand the impact of soil properties on organic pollutants, thorough and detailed analyses of a wide distribution of soil samples with varied properties are needed. Previous research has reported the observation of PAEs and their metabolites in human urine (Koch et al., 2007; Langer et al., 2014; Wang et al., 2015; Gao et al., 2016), which indicates that the general population, especially children, are highly exposed to this group of compounds. Previous cumulative risk assessments of PAEs focused on exposure pathways of PAEs through air, dust, oil, beverages, and fish (Guo et al., 2011, 2012; Schecter et al., 2013). These studies found that dietary intake was the major exposure pathway (Schettler, 2006; Tropea et al., 2010). However, limited attention has been given to vegetables, which have been
contaminated with PAEs, but have not raised enough attention yet (Ma et al., 2015). Vegetable dietary is an important part of our everyday diet; the average consumption of vegetables is 0.35 kg d−1 for adults and 0.12 kg d−1 for 6–11-year-old children (USEPA, 2011). Previous research has examined PAEs in vegetables and soils to estimate hazard index (HI) values (Niu et al., 2014; Ma et al., 2015); however, dietary habits and cooking styles (washing and stewing) were not included in the assessments, which could overestimate the average daily intake (ADI) of PAEs. The objectives of this study were to (i) investigate PAE contamination levels in vegetables both sold on the market and grown in greenhouses; (ii) examine the effects of environmental factors on PAE levels in greenhouse soils with varied soil properties (FeOx content, clay-silt content, and SOM content) and greenhouse cultivation times in 10 cities in China; and (iii) conduct a human cumulative risk assessment of PAEs from vegetables on a group of 6–11-year-old children and a group of > 11-year-old individuals based on a dietary survey. This research contributes to the understanding of PAE contamination in vegetable agriculture and provides a solid knowledge base for establishing PAE standards in greenhouse agriculture. MATERIALS AND METHODS Chemicals Phthalate ester standards of DMP, DEP, DnBP, DiBP, and DEHP were obtained from Sigma-Aldrich, USA; neutral silica gel (100- to 200-mesh) and anhydrous sodium sulfate were obtained from Sinopharm Co. Ltd. (Shanghai, China); HPLC-grade acetone and n-hexane were purchased from Tedia Company Inc., USA. All chemicals and reagents were > 99% pure and used without further purification. In this experiment, ultrapure water (18.2 MΩ cm−1 ) from a Synergy UV ultrapure water system equipped with a Millipak-40 filter unit (Merck KGaA, Germany) was used to make the solutions. The physical and chemical properties of these 5 PAEs can be found in Table I. Soil and vegetable samples from agricultural greenhouses In this study, 111 soil samples and 128 vegetable samples were collected during May–July in 2015 from greenhouses and open fields in 10 cities from north to south in China, including Shenyang, Beijing, Shouguang, Xianyang, Siyang, Haimen, Nanjing, Changshu, Fuzhou, and Kunming, where there was flourishing greenhouse agriculture in the suburban a-
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TABLE I Physical and chemical propertiesa) of the 5 phthalate esters Phthalate ester
CASb) No.
Chemical formula
Dimethyl phthalate
131-11-3
C10 H10 O4
Diethyl phthalate
84-66-2
Di-n-butyl phthalate
Molecular weight
lgKow c)
Solubility
Vapor pressure
194.19
mg L−1 4 000
Pa 1.33
1.6
C12 H14 O4
222.24
1 080
0.27
2.3
84-74-2
C16 H22 O4
278.34
13
0.009 3
4.7
Di-iso-butyl phthalate
84-69-5
C16 H22 O4
278.34
1
0.01
4.1
Di-(2-ethylhexyl) phthalate
117-81-7
C24 H38 O4
390.56
0.27
0.001 9
7.5
a) Most
Structure
of data were cited from Wikipedia and Schwarzenbach et al. (2002). Abstracts Service. = octanol-water partition coefficient.
b) Chemical c) K
ow
reas. The vegetables included bokchoy (Brassica rapa subsp. chinensis), cucumber (Cucumis sativus), eggplant (Solanum melongena), green bean (Phaseolus vulgaris), green pepper (Capsicum annuum), winter radish (Raphanus sativus), and tomato (Solanum lycopersicum). At each location, approximately 15 greenhouses with varying cultivation times (5–20 years) were selected. In each greenhouse, 5 “S” distributed topsoils at 0–20 cm depth were sampled and combined into one soil sample; vegetable leaves were collected from the same greenhouse. The fields without greenhouses nearby were defined as open fields, and both soil and vegetable samples were collected using the same methods at each location. The soil and vegetable samples were preserved in paper envelops to avoid contact with plastics and transported in a cooler to the laboratory.
In the lab, soil samples were crashed and dried in a hood until there was no moisture loss and then passed through a 100-mesh sieve and stored at room temperature. Vegetable samples were washed, freeze-dried, ground, and stored at −20 ◦ C until analysis. The content of SOM was determined by potassium dichromate reduction with a Shimadzu UV/Vis 2700 spectrophotometer (Shimadzu, Japan) at 590 nm (Wang et al., 1993). The particle size distributions of the soil samples were examined with a laser particle analyzer (LS230, Beckman Coulter, USA) after removing SOM and carbonite. The FeOx levels (in the equivalence of Fe2 O3 content, g kg−1 ) in the soils were determined by citrate-bicarbonate-dithionite treatment, and soil extracts were diluted with 1 mol L−1 HCl and analyzed with an atomic absorption spectroscopy (Z-2010,
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Hitachi, Japan). The information of soil properties is shown in Table II. Vegetable samples from markets To screen PAE levels in vegetables sold on the market, 10 markets were randomly selected in the districts of Nanjing, Jiangsu Province, China. In each market, the same 7 kinds of vegetables were bought for analysis, including bokchoy, cucumber, eggplant, green bean, green pepper, tomato, and winter radish. For comparison, these 7 kinds of vegetables were bought from one randomly selected market in Shenyang, Beijing, Fuzhou or Kunming. Vegetable samples were washed, freeze-dried, ground, and stored at −20 ◦ C until analysis. Extraction procedures for soil and vegetables The procedures of soil and plant sample extraction were following the methods of Chee et al. (1996). The extractants were purified and concentrated to 1 mL and analyzed with a Shimadzu GC/MS QP2010 Ultra system (Shimadzu, Japan) with a Rix-5Sil MS column (0.3 µm × 30 m × 0.25 mm) in a splitless mode at 250 ◦ C with selective ion monitoring (Sakamoto et al., 2011). The flow rate was 1.2 mL min−1 with helium as the carrier gas. The column temperature was held at 70 ◦ C for 1 min, increased to 140 ◦ C at a speed of 20 ◦ C min−1 , held for 2 min, increased to 280 ◦ C at a speed of 10 ◦ C min−1 and held for 5 min. The methods used for soil and vegetable extraction were validated for organic contaminants in environmental samples. In each batch of extractions, blank samples were treated in parallel under the same conditions to control contamination, and an internal standard (diallyl phthalate, DAP) was added to each sample to calculate its recovery of the real samples. The
average recoveries of DAP in the real samples and PAEs in the spiked samples were in the range of 85.2%– 115% and 84.3%–108%, respectively. The method detection limits (Huo et al., 2016) for PAEs are below 2.12 × 10−3 mg kg−1 for soil samples and 0.011 mg kg−1 for vegetable samples in this study. Principle component analysis and a multilinear regression model for soil samples The data analyses were carried out with the IBM SPSS Statistics 22 software (IBM, USA). Because the concentration data for each PAE at each location (n < 20) were not normally distributed in this study, the Kruskal-Wallis test was selected in nonparametric analysis to compare the difference among locations at P < 0.05. Principle component analysis (PCA) was conducted on the 5 PAEs in soil samples to classify them into different inner correlated groups and to speculate the sources of the 5 PAEs based on loadings in the extracted components (Kong et al., 2012, 2013; Meng et al., 2014; Niu et al., 2014; Zhang et al., 2014). In this study, the soil sample size (n = 111) was > 30 + (v +3)/2, where v is the number of variables (Kong et al., 2013), indicating that the results would be reliable and stable. Because the value of the Kaiser-Meyer-Olkin measure of the sampling adequacy was 0.589 and Bartlett’s test of sphericity was < 0.001, PCA was suitable for these data. In this study, a varimax normalized rotation was applied to optimize loading factors for each rotated principal component. A multilinear regression model (Eq. 1) was also applied to analyze correlations between PAEs and environmental factors, including greenhouse cultivation time (Y , year), SOM content (g kg−1 ), soil FeOx content (g kg−1 ), and clay-silt content (%). After exami-
TABLE II Selected properties of the soil samples from agricultural greenhouses and open fields in 10 cities from north to south in China City
Location
Soil organic matter
FeOx
Clay-silt
g kg−1 Shenyang Beijing Shouguang Xianyang Siyang Haimen Nanjing Changshu Fuzhou Kunming
41.870◦ 40.166◦ 36.797◦ 34.412◦ 33.702◦ 31.953◦ 31.777◦ 31.777◦ 26.123◦ 24.669◦
N, N, N, N, N, N, N, N, N, N,
122.976◦ 116.458◦ 118.965◦ 109.074◦ 118.656◦ 121.146◦ 118.872◦ 118.872◦ 119.118◦ 102.906◦
E E E E E E E E E E
20.2 31.9 30.8 24.1 20.1 30.9 24.4 14.0 33.3 32.6
± ± ± ± ± ± ± ± ± ±
9.8a) abb) 19.4ab 10.0ab 8.1ab 8.8ab 20.4ab 10.6ab 8.7b 14.8ab 10.0a
6.69 8.53 5.69 7.42 6.58 8.38 6.48 8.20 10.20 24.40
± ± ± ± ± ± ± ± ± ±
1.65cd 1.73bc 1.48d 0.93bcd 0.95d 1.12bc 1.92d 1.14bcd 3.19b 10.40a
% 63.9 74.9 73.7 83.3 67.4 86.9 68.7 92.7 64.7 91.9
± ± ± ± ± ± ± ± ± ±
12.0d 15.0cd 10.4cd 8.5bcd 21.3d 4.0bc 23.2d 1.0a 14.5d 8.0ab
± standard deviations (n = 111). followed by the same letter(s) within each column are not significantly different at P < 0.05 according to one-way analysis of variance by the Ryan-Einot-Gabriel-Welsch range test.
a) Means
b) Means
PHTHALATE ESTER CONTAMINATION AND RISK ASSESSMENT
ning bivariate correlations combined with eigenvalues, condition indexes, variance inflation factor values, and tolerance values, there was no multicollinearity between the independent factors, and the data were used directly in the multilinear regression model. Csoil,i = k1 ·Y + k2 ·SOM + k3 ·Clay-silt + k4 ·FeOx + ε
(1)
where Csoil,i (mg kg−1 , dry weight) is the concentration of the ith PAE (i = DMP, DEP, DiBP, DnBP or DEHP) in a soil sample; k1 , k2 , k3 , and k4 are the coefficients for the 4 independent variables, respectively; and ε is the residue of the model. Human cumulative risk assessment In order to estimate ADI of PAEs from vegetables, a dietary survey of vegetable intakes was conducted from March to April in 2016. The survey was carried out by answering question sheet. The individuals who eat vegetables from the market were qualified to answer question sheet in the survey. A wholeyear dietary recalls of vegetables, separated into spring (90 d), summer (91 d), autumn (92 d), and winter (92 d), were completed by 115 participants from Nanjing, Shouguang, and Beijing. The average intake rate (Ij , kg d−1 ) and annual exposure frequency (EFj , d year−1 ) of the jth vegetable (j = bokchoy, cucumber, eggplant, green bean, green pepper, tomato, and winter radish) for individuals in one city were estimated according to the survey results. The ADI value of the ith PAE from vegetables (ADIi , mg kg−1 d−1 ) was estimated as follows: ADIi =
∑ Cveg,ij ·RRij ·Ij ·EFj ·EDj j
BW·AT
443
PA, 2011): HQi =
ADIi RLVi
(3)
where RLVi (mg kg−1 d−1 ) was defined as the reference limited value of the ith PAE, such as the reference dose for anti-androgenicity (RfDAA ) (Kortenkamp and Faust, 2010) or tolerable daily intake (TDI) based on anti-androgenic results from animal models (EFSA, 2005a, b, c). The previous research reported that DiBP, DnBP, and DEHP have similar anti-androgenic effects on human health and that these effects are dose additive (NRCNA, 2008). Due to the combined exposure of PAEs from vegetables, a hazard index (HI) for the 3 PAEs from vegetables was calculated based on Eq. 4 (NRCNA, 2008; USEPA, 2011): HI = HQDiBP + HQDnBP + HQDEHP
(4)
When HI < 1, there is a limited probability of adverse effects after long-term consumption of these vegetables; otherwise, it will not be safe to consume these vegetables, and further analysis will be needed. RESULTS AND DISCUSSION PAE profiles in greenhouse soils PAEs were detected in all soil samples (Fig. 1). After careful statistical analyses, no significant difference was found in vegetables between open fields and greenhouses, which indicated that there were other sources of soil PAEs besides plastic films in greenhouse agriculture. The average concentration of DEHP in the
(2)
where Cveg,ij (mg kg−1 , fresh weight) is the average concentration of the ith PAE in the jth vegetable on the market analyzed in this study; RRij (%) is defined as the removal rate of PAEi from the jth vegetable through washing and cooking; EDj (year) is the exposure duration of consuming the jth vegetable; BW (kg) is the average body weight of the selected group in China, 31.9 kg for a 6–11-year-old child or 58.6 kg for a > 11-year-old individual (Duan, 2012); and AT (d) is the averaging exposure time. In this study, EDj was 5 years for a 6–11-year-old child or 30 years for a > 11-year-old individual. For non-carcinogenic assessment, AT was 1 825 d for a 6–11-year-old child or 10 950 d for a > 11-year-old individual. Based on ADIi , a non-cancer hazard quotient (HQi ) for the ith PAE was estimated as follows (USE-
Fig. 1 Average concentrations of phthalate esters (PAEs), including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), in soils and vegetable leaves from open fields and greenhouses. Vertical bars indicate standard deviations of the means.
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greenhouse soils was non-significantly higher than that in the open field soils. Because the data were obtained from field experiments, multi-parameters might influence PAE concentrations. This result indicated that there was a trend to accumulate DEHP in greenhouse soils. In the greenhouse soils, the average concentration of DnBP (0.552 ± 0.275 mg kg−1 ) was non-significantly higher than that of DEHP (0.396 ± 0.150 mg kg−1 ), and the concentrations of these two compounds were approximately 5 and 4 times, respectively, that of DEP (0.113 ± 0.053 mg kg−1 ) and 15 and 11 times that of DMP (0.034 ± 0.020 mg kg−1 ). The average concentration of DiBP (0.294 ± 0.104 mg kg−1 ) was lower than those of DnBP and DEHP, but higher than those of DEP and DMP (Fig. 1). Location is a significant factor influencing the concentrations of DMP, DiBP and DnBP in soils (P < 0.05), but not those of DEP and DEHP. The concentration of DiBP in Fuzhou soils was significantly higher (P < 0.05) than that in Nanjing soils; the soils in Shenyang had the highest DnBP concentration, while the soils in Changshu had the lowest (Table III). The levels of PAEs in this study were within the same magnitude order as the reported data (Stales et al., 1997; Huang et al., 2008; Kong et al., 2013). The results of the multilinear regression showed that the concentration of DEHP positively correlated (P < 0.05) with the greenhouse cultivation time (data not shown). One year of greenhouse cultivation added 0.007 5 ± 0.002 3 mg kg−1 DEHP to the soil, which is consistent with the conclusion that DEHP may be derived mainly from plastic films and it degrades slowly in soils (Adhoum and Monser, 2004; Amir et al.,
2005). A negative correlation was found between the concentration of DnBP and FeOx content in soils, and each 1 g kg−1 FeOx increment in the soil led to 0.010 5 ± 0.004 2 mg kg−1 less DnBP (data not shown). This is because FeOx is an active component in soil, which can degrade organic compounds through adsorption, oxidation, Fenton reactions and Fenton-like reactions (Chemat et al., 2001; Chen et al., 2016). Because DMP is the degradation product of PAEs with longer side chains, such as DnBP and DEHP (Quan et al., 2005), DMP concentration is positively correlated with the FeOx content in soil. In this study, the average value of FeOx in soils from Kunming was approximately 3 times that in soils from the other locations, and the amounts of PAEs in Kunming soils were significantly lower than those in soils from the other locations (Table III). There were negative correlations between DMP, DEP, DiBP, and DEHP and clay-silt content. No significant correlation was found between each PAE compound and SOM, and similar results have been reported by Zeng et al. (2008) and Niu et al. (2014). Identification of PAE sources in greenhouse soils In this study, 3 principal components (PC1, PC2, and PC3) were extracted based on PCA, which could explain 86.3% of the total variance in the 5 PAEs (Fig. 2). Table IV presents the loadings of PAEs, the eigenvalues, and the variance percentages corresponding to 3 PCs. PC1 explained 51.2% of the total variance and showed strong positive loadings of DMP, DEP, and DiBP (Fig. 2, Table IV). PC1 may be interpreted as a source associated with wastewater irrigation because DMP, DEP, and DiBP are the most wide-
TABLE III Concentrations of phthalate esters, including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), in soils (dry weight, DW) from greenhouses and open fields in 10 cities from north to south in China City
n
DMP
DEP
DiBP
DnBP
DEHP
kg−1
Shenyang Beijing Xianyang Shouguang Siyang Haimen Nanjing Changshu Fuzhou Kunming
16 12 6 12 11 12 13 5 12 12
0.032 0.047 0.038 0.046 0.023 0.026 0.031 0.022 0.040 0.032
± ± ± ± ± ± ± ± ± ±
0.023aa) 0.026a 0.021a 0.020a 0.010a 0.011a 0.018a 0.005a 0.023a 0.014a
0.114 0.116 0.147 0.149 0.095 0.090 0.108 0.108 0.128 0.088
± ± ± ± ± ± ± ± ± ±
0.049a 0.050a 0.079a 0.065a 0.044a 0.035a 0.035a 0.048a 0.068a 0.039a
mg 0.325 ± 0.315 ± 0.298 ± 0.341 ± 0.241 ± 0.243 ± 0.221 ± 0.223 ± 0.363 ± 0.311 ±
DW 0.084abb) 121ab 0.079ab 0.117ab 0.056ab 0.060ab 0.035b 0.036ab 0.137a 0.128ab
0.961 0.597 0.362 0.659 0.650 0.550 0.491 0.157 0.463 0.263
± ± ± ± ± ± ± ± ± ±
0.117a 0.183b 0.205bc 0.143bc 0.278b 0.165bc 0.219b 0.088c 0.252bc 0.145c
0.407 0.448 0.382 0.491 0.336 0.344 0.390 0.365 0.446 0.314
± ± ± ± ± ± ± ± ± ±
0.086a 0.166a 0.100a 0.216a 0.116a 0.160a 0.177a 0.046a 0.162a 0.096a
± standard deviations. followed by the same letter(s) within each column are not significantly different at P < 0.05 according to one-way analysis of variance by the Ryan-Einot-Gabriel-Welsch range test.
a) Means
b) Means
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Fig. 2 Loading plots of phthalate esters, including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), on 3 principal components (PC1, PC2, and PC3).
ly used PAEs in household products and they have been frequently detected in wastewater (Aurela, 2001; Berg´e et al., 2013). This result is also in accordance with the work of Kong et al. (2012), in which DMP and DEP were clustered in the PCA of wastewater treatment soils in Tianjin, China. PC2 explained 19.8% of the total variance and showed a strong positive loading of DEHP, which indicated that PC2 might represent a source of DEHP, such as plastic films (Jaworek and Czaplicka, 2013; Kong et al., 2013), for which DEHP was the most abundant PAE, where the concentration could be as high as 1.31 × 103 mg kg−1 . PC3 explained 15.3% of the total variance. The largely positive loading of DnBP in PC3 indicated a source associated with materials with high DnBP levels (Fig. 2, Table IV), such as fertilizers and pesticides. It has been reported that the average concentration of DnBP in fertilizers, pesticides and insect repellants is as high as 161 mg kg−1 (Luepke, 1978; Mo et al., 2008). This result can also explain the high detection frequency of DnBP in open fields without greenhouses. TABLE IV Loadings of phthalate esters, including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), eigenvalues, and variance percentages corresponding to 3 principle components (PC1, PC2, and PC3) Phthalate ester
PC1
PC2
PC3
DMP DEP DiBP DnBP DEHP
86.0 70.2 83.9 10.1 14.4
% 23.6 59.7 4.4 3.1 95.4
16.3 −2.6 4.8 99.3 4.6
Eigenvalue Variance (%) Cumulative variance (%)
2.560 51.2 51.2
0.989 19.8 71.0
0.764 15.3 86.3
DEP was loaded in both PC1 and PC2 (Fig. 2), which indicated that DEP might be from both wastewater irrigation and plastic films. This is supported by a previous work (Kong et al., 2013). In PC2 and PC3, DMP was also positively loaded, which may be because DMP is the degradation product of long-chain PAEs such as DEHP and DnBP (Quan et al., 2005). These indicate that managing wastewater irrigation, plastic coverage, and fertilizer application can be beneficial for controlling PAE contamination in soil. Concentrations of PAE in vegetable leaves from greenhouses Table V shows the PAEs profiles in vegetable leaves from greenhouses. The statistical analyses indicated no linear correlation for PAE levels between soils and vegetable leaves from the same greenhouses. There was more accumulation of PAEs in vegetable leaves compared with PAEs in soils. Vegetables can absorb PAEs not only through their roots from soil but also through their leaves from air. The concentrations of DEHP (2.21–2.62 mg m−3 ), DiBP (0.233–0.241 mg m−3 ), and DnBP (0.165–0.443 mg m−3 ) in the air inside the greenhouses were much higher than those outside (< 0.048 ± 0.005 mg m−3 ) in this study (data not shown). The measurement of PAE concentrations in air was following the methods of Rudel and Perovich (2009) and Kong et al. (2013). The concentrations of PAEs in the air inside the greenhouses are related to temperature, sunshine, greenhouse cultivation style, thickness of the plastic film, and coverage time of the plastics (Wang et al., 2013). The average concentrations of DiBP, DnBP and DEHP were nonsignificantly higher in vegetables growing in greenhouses covered with plastics than in open fields (Fig. 1). Location was not a significant factor influencing
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PAE levels in vegetable leaves from greenhouses (Table V). Soil properties, such as SOC, pH and texture, and greenhouse application time had limited effects (P > 0.05) on PAE levels in vegetable leaves. There was a weak positive correlation (n = 68, R2 = 0.344) for DnBP level between soils and vegetables from northern cities, including Shouguang, Beijing, and Shenyang, but not for those from southern cities. More biochemical degradation may occur in warmer locations, which would impact the DnBP concentration in soils and vegetables. No significant correlation for DEHP levels was observed between soils and vegetables. These results are consistent with a previous report, where most DnBP in vegetables was from root uptake, while most DEHP was from leaf absorption (Qin et al., 2006).
of vegetables from greenhouses, such as bokchoy, eggplant, green bean, green pepper, and tomato, in which more DiBP and DnBP were detected (Fig. 3). Further research should be conducted concerning the distribution of PAEs in the different parts of the vegetables. Table VI showed that vegetables from the markets in Nanjing had the highest concentration of PAEs, while the vegetables from Kunming and Fuzhou had the lowest concentrations of total PAEs. There was no consistent trend in the data about PAE levels in vegetables sold in different cities because multiple factors would affect the concentrations of PAEs in the vegetables, including the original PAE level before sale and pretreatment before packing. Washing would remove 7% ± 6% of the PAEs from the vegetables. In summary, the total concentration of PAEs in greenhouse soils was in the range of 0.26–2.53 mg kg−1 (dry weight), and the total concentrations of PAEs in vegetable leaves from greenhouses and vegetables sold on the market were in the ranges of 1.58–8.09 and 0.95– 6.36 mg kg−1 (fresh weight), respectively. These data are consistent with the previously reported data (Cai et al., 2005; Yang et al., 2007; Guo and Wu, 2011; Kong
Concentrations of PAEs in vegetables sold on the market All of the PAEs were detected (detection frequency for each PAE > 73%) in the 7 vegetables from the markets in the selected cities (Table VI). The average concentrations of total PAEs in the vegetables from the markets were slightly higher than those in leaves TABLE V
Concentrations of phthalate esters (PAEs) (fresh weight, FW), including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-isobutyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), in leaves of greenhouse vegetables (i.e., bokchoy, cucumber, eggplant, green bean, green pepper, tomato, and winter radish) in 10 cities from north to south in China City
DMP
DEP
DiBP
DnBP
DEHP
ΣPAEs
kg−1
Shenyang Beijing Shouguang Xianyang Siyang Haimen Nanjing Changshu Fuzhou Kunming
0.225 0.142 0.159 0.148 0.457 0.486 0.394 0.182 0.193 0.156
± ± ± ± ± ± ± ± ± ±
0.039a) ab) 0.037a 0.057a 0.050a 0.027a 0.251a 0.033a 0.063a 0.051a 0.013a
0.235 0.118 0.106 0.140 0.873 0.282 0.446 0.219 0.188 0.152
± ± ± ± ± ± ± ± ± ±
0.065a 0.033a 0.055a 0.034a 0.130a 0.073a 0.132a 0.024a 0.054a 0.025a
0.918 0.860 0.360 0.645 0.770 0.526 1.020 1.000 1.080 0.554
mg FW ± 0.199a 1.15 ± 0.17b ± 0.224a 1.16 ± 0.25b ± 0.109a 1.01 ± 0.18b ± 0.197a 0.50 ± 0.22b ± 0.094a 2.42 ± 0.23a ± 0.072a 1.26 ± 0.32b ± 0.250a 1.92 ± 0.34a ± 0.226a 2.10 ± 0.44a ± 0.170a 0.76 ± 0.30b ± 0.099a 0.80 ± 0.08b
0.81 1.25 1.31 1.04 1.68 0.82 1.03 1.41 1.14 1.24
± ± ± ± ± ± ± ± ± ±
0.18a 0.35a 0.27a 0.30a 0.12a 0.17a 0.21a 0.19a 0.39a 0.18a
3.32 3.53 2.95 2.48 6.12 3.38 4.81 4.91 3.36 2.90
± ± ± ± ± ± ± ± ± ±
0.91 0.90 1.00 0.91 0.58 0.48 1.79 1.50 1.46 1.31
± standard deviations (n = 128). followed by the same letter(s) within each column are not significantly different at P < 0.05 according to one-way analysis of variance by the Bonferroni method.
a) Means
b) Means
TABLE VI Concentrations of total phthalate esters in 7 vegetables (fresh weight, FW) sold on the market in 5 cities from north to south in China City
Bokchoy
Shenyang Beijing Nanjing Fuzhou Kunming
± ± ± ± ±
0.11a) 0.03 0.98 0.13 0.65
± standard deviations. detected.
a) Means b) Not
2.79 5.00 5.14 2.50 2.60
Cucumber 4.39 2.96 4.89 2.07 1.14
± ± ± ± ±
0.06 0.07 0.90 0.11 0.08
Eggplant 1.64 1.88 5.41 1.44 0.98
± ± ± ± ±
0.07 0.07 0.67 0.11 0.09
Green bean
Green pepper
mg kg−1 FW 3.03 ± 0.25 5.58 ± 0.17 3.42 ± 0.51 1.69 ± 0.08 1.94 ± 0.16
1.83 2.28 5.95 2.18 –b)
± ± ± ±
0.06 0.13 0.58 0.06
Tomato 4.67 3.99 4.84 1.94 1.04
± ± ± ± ±
0.10 0.17 0.71 0.08 0.09
Winter radish 2.30 2.95 4.06 1.68 1.97
± ± ± ± ±
0.09 0.15 0.24 0.10 0.13
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Fig. 3 Average concentrations of phthalate esters (PAEs), including dimethyl phthalate (DMP), diethyl phthalate (DEP), di-iso-butyl phthalate (DiBP), di-n-butyl phthalate (DnBP), and di-2-ethylhexyl phthalate (DEHP), in 7 vegetables, i.e., bokchoy (BC), cucumber (CC), eggplant (EP), green bean (GB), green pepper (GP), tomato (TM), and winter radish (WR), on the market and vegetable leaves from greenhouses.
et al., 2012; Wang et al., 2013, 2015). In all soil and vegetable samples, the concentrations of DiBP, DnBP and DEHP were higher than those of DMP and DEP.
Table VIII showed that the average estimated ADI values of DnBP and DEHP were 0.002 1 and 0.001 3 mg kg−1 d−1 , for a 6–11-year-old child and 0.002 3 and 0.001 5 mg kg−1 d−1 for a > 11-year-old individual, which were approximately 23% and 2.9% of the TDI of DnBP and DEHP, respectively. The two ADI values for children were similar to those for the group of > 11-year-old individuals, because children had less body weight (31.9 kg) and ate less vegetables (0.087 kg d−1 ) than adults (58.6 kg and 0.218 kg d−1 ). The 5 PAEs in this study belonged to Cramer Class I (0.03 mg kg−1 d−1 ) in the method of the threshold of toxicological concern (Kortenkamp et al., 2010). The ratios of the ADI value to the threshold of toxicological concern for DnBP and DEHP were 7.6% and 4.8%, respectively. However, it should be noted that only 7 vegetables were included in the ADI calculations and that the values of DnBP and DEHP were underestimated. Due to the higher concentrations of DnBP and DEHP in vegetables in the northern cities than those in southern cities, the ADI values of DnBP and DEHP in Shenyang
Human cumulative risk assessment The studied 7 vegetables from the markets were commonly consumed by local populations. The diet habits of these vegetables were surveyed in the present study (Table VII) and used to estimate the ADI value in the assessment. The estimated daily intake rates of these 7 vegetables were 0.087 kg d−1 for a 6–11year-old child and 0.218 kg d−1 for a > 11-year-old individual, which were slightly lower than those in a national survey (Wang et al., 2009), because most of the surveyed people in this study were living in cities and there were other vegetables not included in this survey. After washing and cooking, approximately 31% ± 13% of PAEs were removed. DMP (39% ± 9%) and DEP (45% ± 22%) were more easily removed than the other PAEs (15%–40%) due to their higher solubility and vapor pressure (Table I). TABLE VII
Survey results of average intake rate (I) and annual exposure frequency (EF) of one vegetable for individuals from Beijing, Shouguang and Nanjing Vegetable
Bokchoy Cucumber Eggplant Green pepper Green bean Tomato Winter radish
Beijing
Shouguang
Nanjing
I
EF
I
EF
I
EF
kg d−1 0.112 0 0.102 0 0.071 1 0.061 3 0.067 8 0.113 0 0.076 0
d year−1 158 118 71 92 72 170 74
kg d−1 0.145 9 0.101 0 0.073 1 0.060 5 0.049 8 0.113 0 0.091 1
d year−1 124 109 66 88 56 141 76
kg d−1 0.112 0 0.091 1 0.080 7 0.046 3 0.052 5 0.097 9 0.066 7
d year−1 192 86 76 60 41 130 67
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TABLE VIII Human cumulative risk assessment of phthalate estersa) in contaminated vegetables for individuals from Shenyang, Beijing, Nanjing, Fuzhou, and Kunming City
Average daily intake DnBP
Hazard index Based on RfDAA b)
DEHP
Based on TDIc)
6–11-year-old > 11-year-old 6–11-year-old > 11-year-old 6–11-year-old > 11-year-old 6–11-year-old > 11-year-old Shenyang Beijing Nanjing Fuzhou Kunming
0.003 6 0.002 0 0.003 9 0.000 8 0.000 2
0.004 0 0.002 2 0.004 3 0.000 8 0.000 3
mg kg−1 d−1 0.001 3 0.002 9 0.001 3 0.001 2 < 0.000 1
0.001 4 0.003 2 0.001 4 0.001 3 0.000 1
0.084 0.123 0.096 0.055 0.008
0.093 0.134 0.105 0.060 0.008
0.474 0.370 0.573 0.189 0.071
0.516 0.403 0.624 0.206 0.077
a) DnBP
= di-n-butyl phthalate; DEHP = di-2-ethylhexyl phthalate; DiBP = di-iso-butyl phthalate. dose for anti-androgenicity, including DiBP, DnBP, and DEHP. c) Tolerable daily intake, including DiBP, DnBP, and DEHP. b) Reference
and Beijing were about 4.5–30 times those in Kunming. For comparison, the ADI values of DnBP and DEHP in this study were approximately 3.2 and 0.85 times, respectively, of the total exposure (0.000 72 and 0.001 76 mg kg−1 d−1 ) from commercial food stuffs (Schettler, 2006; Guo et al., 2012), cosmetic products (Guo et al., 2014), and air (Guo and Kannan, 2011; Huo et al., 2016) for the Chinese population, whereas they were 12.5 and 2.2 times the values of the total daily intakes from dietary reported for US individuals (Schecter et al., 2013). These two ADI values for DnBP and DEHP in this study were comparable to the calculated total exposure values (0.003 5 and 0.002 7 mg kg−1 d−1 , respectively) for European adults (Wormuth et al., 2006), including food, drink, inhalation, and dermal absorption. For 6–11-year-old children, the ADI values for DnBP and DEHP in this study were 1.7 and 5.5 times the total exposure values for European children (Wormuth et al., 2006). The results indicated that special action should be taken to reduce the exposure of PAEs from vegetables to individuals in China. In Nanjing, the HI values, with RfDAA as the reference limited value, from the 7 vegetables were 0.096 for 6–11-year-old children and 0.105 for > 11-year-old individuals based on the average PAE concentrations in vegetables on the market (Table VIII). In HI calculation, the contributions of HQ values of DnBP and DEHP were greater than that of DiBP. In a high exposure scenario, the HI value increased to 0.15 for 6–11year-old children and 0.17 for > 11-year-old individuals based on the top 5% PAE concentrations in vegetables. Table VIII showed that exposure of PAEs from vegetables was higher for people living in northern cities than for those in southern cities. The HI value was only 0.008 for the individuals in Kunming due to low concentrations of DnBP and DEHP in vegetables on
the markets. If TDI was applied as the reference limited value, the HI values for 6–11-year-old children and > 11-yearold individuals in Nanjing increased to 0.573 and 0.624, respectively (Table VIII). That is because the TDI values for DnBP (0.01 mg kg−1 d−1 ) (EFSA, 2005b) and DiBP (0.01 mg kg−1 d−1 ) (Hannas et al., 2011) are a magnitude lower than the RfDAA values. Although all the HI values were below 1, attention should be given if considering other exposure pathways, including dietary intake from other commercial foodstuff, inhalation, and dermal absorption from personal care products. The estimated HI values for children in this study were a magnitude lower than those in the previous report of Ma et al. (2015), in which soil ingestion was a major exposure pathway for 0–6-year-old children. The removal effects of washing and cooking were also not included in their calculations for vegetable exposure. CONCLUSIONS Based on the results from the open field and greenhouse soils, PAEs were derived not only from greenhouse plastics but also from other sources, such as wastewater irrigation, fertilizers, and pesticides. The multilinear regression analyses showed that long-term greenhouse cultivation could accumulate DEHP in soil, and higher soil FeOx content could lower DnBP levels. It was suggested to control PAE contamination in soils by improving wastewater treatment and changing fertilizer composition and styles of greenhouse agriculture. Vegetables growing in greenhouse agriculture had higher DnBP and DEHP levels than those growing in open fields. The high detection frequency of PAEs in vegetables sold on the market indicates that exposure
PHTHALATE ESTER CONTAMINATION AND RISK ASSESSMENT
pathway of PAEs to humans through vegetable consumption should be of concern in cumulative risk assessments. People in northern cities in China had higher exposure of PAEs from vegetables than those in southern cities. The exposure of PAEs from vegetables for individuals in China was comparable or greater than the total exposure for European and USA individuals. In this study, the ADI values of DnBP and DEHP from vegetables were still below the TDI value, and the HI values (including DiBP, DnBP, and DEHP) in different cities indicated that the contamination of PAEs in vegetables may not cause anti-androgenic effects after long-term exposure. However, it should be noted that the values of HI may be underestimated because only 7 vegetables were considered in the survey. Special attention should be given to individuals who work in greenhouses due to high DEHP concentration inside greenhouse air. ACKNOWLEDGEMENTS CHEN Ning and SHUAI Wenjuan contributed equally to this research. This study was supported by the National Basic Research Program of China (No. 2014CB441105), the National Natural Science Foundation of China (No. 21377136), the One Hundred Person Project of Chinese Academy of Sciences (No. 2012133), and the 135 Research Program of Chinese Academy of Sciences. We appreciate the assistance of Mr. Yue YANG from the United BioScience Instrument Company, USA, Dr. LUO Yan from the Kunming Institute of Botany, CAS, Dr. LI Lu from the Southwest Forest University of China, and Mrs. CHEN Meijuan and Mrs. YAN Liu during the sampling processes. REFERENCES Adhoum N, Monser L. 2004. Removal of phthalate on modified activated carbon: application to the treatment of industrial wastewater. Sep Purif Technol. 38: 233–239. Amir S, Hafidi M, Merlina G, Hamdi H, Jouraiphy A, El Gharous M, Revel J C. 2005. Fate of phthalic acid esters during composting of both lagooning and activated sludges. Process Biochem. 40: 2183–2190. Aurela B. 2001. Migration of substances from paper and board food packaging materials. Ph. D. Thesis, Faculty of Science, the University of Helsinki. Barreiro J C, Capelato M D, Martin-Neto L, Hansen H C B. 2007. Oxidative decomposition of atrazine by a Fenton-like reaction in a H2 O2 /ferrihydrite system. Water Res. 41: 55– 62. Beller H R, Grbi´ c-Gali´ c D, Reinhard M. 1992. Microbial degradation of toluene under sulfate-reducing conditions and the influence of iron on the process. Appl Environ Microb. 58: 786–793. Berg´ e A, Cladi` ere M, Gasperi J, Coursimault A, Tassin B, Moilleron R. 2013. Meta-analysis of environmental contamina-
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