Science of the Total Environment 523 (2015) 129–137

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Occurrence and risk assessment of phthalate esters (PAEs) in vegetables and soils of suburban plastic film greenhouses Jun Wang a,b, Gangcai Chen a, Peter Christie b, Manyun Zhang b, Yongming Luo b, Ying Teng b,⁎ a b

Chongqing Research Academy of Environmental Sciences, Chongqing 401147, China Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China

H I G H L I G H T S • We concurrently study phthalate esters (PAEs) in vegetables and soils in greenhouses of China. • We found that PAEs concentrations had no significant correlation between soil and vegetable. • PAEs had a potential carcinogenic risk to farmers working in greenhouses.

a r t i c l e

i n f o

Article history: Received 6 December 2014 Received in revised form 27 February 2015 Accepted 27 February 2015 Available online 8 April 2015 Editor: Adrian Covaci Keywords: Phthalates Greenhouse soils Vegetables Plastic film Risk assessment

a b s t r a c t Phthalate esters (PAEs) are suspected of having adverse effects on human health and have been frequently detected in soils and vegetables. The present study investigated their occurrence and composition in plastic film greenhouse soil–vegetable systems and assessed their potential health risks to farmers exposed to these widespread pollutants. Six priority control phthalates, namely dimethyl phthalate (DMP), diethyl phthalate (DEP), di-n-butyl phthalate (DnBP), butyl benzyl phthalate (BBP), di-(2-ethylhexyl) phthalate (DEHP) and di-n-octyl phthalate (DnOP), were determined in 44 plastic film greenhouse vegetables and corresponding soils. Total PAEs ranged from 0.51 to 7.16 mg kg−1 in vegetables and 0.40 to 6.20 mg kg−1 in soils with average concentrations of 2.56 and 2.23 mg kg−1, respectively. DnBP, DEHP and DnOP contributed more than 90% of the total PAEs in both vegetables and soils but the proportions of DnBP and DnOP in vegetables were significantly (p b 0.05) higher than in soils. The average concentrations of PAEs in pot herb mustard, celery and lettuce were N 3.00 mg kg−1 but were b 2.50 mg kg−1 in the corresponding soils. Stem and leaf vegetables accumulated more PAEs. There were no clear relationships between vegetable and soil PAEs. Risk assessment indicates that DnBP, DEHP and DnOP exhibited elevated non-cancer risk with values of 0.039, 0.338 and 0.038, respectively. The carcinogenic risk of DEHP was about 3.94 × 10−5 to farmers working in plastic film greenhouses. Health risks were mainly by exposure through vegetable consumption and soil ingestion. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Phthalate esters (PAEs) are plasticizers and additives that are widely used industrial chemicals. They exist in a free and leachable phase in the matrix of building materials, home furnishings, food packaging and polyvinylchloride (PVC) resins (Staples et al., 1997; Heudorf et al., 2007; Chen et al., 2008). Approximately 6 million tonnes of PAEs are produced and consumed globally each year (Niu et al., 2014) and about 2.2 million tonnes of PAEs are consumed annually in China (CPPIU, 2011). PAEs will be gradually released into the environment from PAE-containing products during their manufacture, use and disposal (Cadogan et al., 1993; Staples et al., 1997; Wang et al., 2013).

⁎ Corresponding author. E-mail address: [email protected] (Y. Teng).

http://dx.doi.org/10.1016/j.scitotenv.2015.02.101 0048-9697/© 2015 Elsevier B.V. All rights reserved.

PAEs have therefore been detected in a range of environmental media such as water (Liu et al., 2014), air (Wang et al., 2012), sediments (Cai et al., 2008; Wang et al., 2014), soils (Kong et al., 2012; Wang et al., 2013), plants (Wu et al., 2013; Ma et al., 2013), foods and beverages (Sakhi et al., 2014). PAE concentrations have reached mg kg− 1 in most agricultural soils across China (Zeng et al., 2008; Chen et al., 2012; Niu et al., 2014). Di-n-butyl phthalate (DnBP) and di-(2ethylhexyl) phthalate (DEHP) concentrations in Chinese agricultural soils are one to three orders of magnitude higher than in British clay soils and Danish agricultural soils (Gibson et al., 2005; Vikelsøe et al., 2002). Total PAE concentrations up to 58.9 mg kg−1 have been found in vegetable producing soils in south China and up to 1232 mg kg− 1 in a cotton field in Xinjiang province (Wang et al., 2013) and PAEs are of considerable public concern in China. High concentrations of PAEs represent a potential threat to human health. Numerous epidemiological and toxicological studies have

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J. Wang et al. / Science of the Total Environment 523 (2015) 129–137

Fig. 1. Schematic map showing the geographical location of the sampling areas.

demonstrated that some are endocrine disrupting compounds (van Wezel et al., 2000; Heudorf et al., 2007; Jurewicz and Hanke, 2011) and have potential carcinogenic, teratogenic and mutagenic effects (Hauser and Calafat, 2005; Chen et al., 2008; Cho et al., 2010; Ma et al., 2013). Studies on laboratory animals have shown that some PAEs and their metabolites are estrogenic with possible effects on general metabolism and the reproductive system (Bell, 1982; Jurewicz and Hanke, 2011). PAEs through their metabolites suppress estradiol production in the ovary and lead to problems with ovulation (LovekampSwan and Davis, 2003), and monoethylhexyl phthalate (MEHP) and the metabolite DEHP are associated with a higher occurrence of loss of pregnancy (Toft et al., 2012). An association has been found between high phthalate exposure and effects on the human endocrine or reproductive system, and on the intelligence and behavior of children (Cho et al., 2010; Weuve et al., 2010; Casas et al., 2011; Jurewicz and Hanke, 2011). Exposure to phthalates may also affect human semen quality and Leydig cell development (Franco et al., 2007; Jurewicz and Hanke, 2011; Liu et al., 2012). As a result, some phthalates such as DMP, DEP, DnBP, butyl benzyl phthalate (BBP), DEHP and di-n-octyl phthalate (DnOP) have been classified as priority control environmental pollutants by the United States Environmental Protection Agency (USEPA). Plastic film greenhouses have become very popular for vegetable production throughout China. By 2011 the cultivated area had reached 19.8 million ha and used approximately 2.29 million tonnes of plastic film (Department of Rural Survey National Bureau of Statistics of China, 2012), the most important sources of PAEs in greenhouse soils (Wang et al., 2013) together with sewage sludge, fertilizer and biosolid applications and waste-water irrigation (Cai et al., 2008; Mo et al., 2008). Dorney et al. (1985) reported PAE concentrations up to 23 mg kg−1 in wheat, beans and corn grown for 40 days in silty loam soil containing 600 mg kg− 1 of PAEs. Yin et al. (2003) found that DnBP decreased the vitamin C and capsaicin contents of pepper. Cai et al. (2008) found PAE concentrations in vegetables up to 11.2 mg kg−1 in the Pearl River Delta, south China. Mobility of PAEs in the soil–plant system may also represent a potential risk to human health via the food chain (Schmitzer et al., 1988; Toft et al., 2012; Wang et al., 2013). However, most studies have focused on PAEs in either the soil or vegetables without considering the soil–plant continuum. In addition, the potential risks of PAEs to human health via work exposure and vegetable consumption in the production of greenhouse vegetables have seldom been estimated. A detailed study of the

occurrence of PAE in the soil–vegetable system and associated health risks in plastic greenhouses will be of considerable benefit for improving greenhouse soil quality and minimizing the exposure risks for farmers and consumers. In the present study six priority control PAEs were determined in soils and vegetables collected from greenhouses in the suburbs of Nanjing city, east China. The main objectives were to characterize the contamination status and congener profiles of PAEs in greenhouse soils and vegetables, to identify the correlations between soil and vegetable PAE concentrations, to analyze the differences in PAE distributions among different vegetables, and to evaluate the toxicity risks of PAEs in soils and vegetables for farmers via dietary and work routes. The results will provide baseline information for soil quality assessments and rational farming practice and help to protect the health of farmers and consumers. 2. Materials and methods 2.1. Sample collection A total of 44 vegetable samples from ten vegetable species and 44 soil samples were concurrently collected from suburban plastic film greenhouses in Jiangning (30°38′–32°13′ N, 118°31′–119°04′ E) and Lishui (31°23′–31°48′ N, 118°51′–119°14′ E) districts of Nanjing (Fig. 1), east China, in January 2012. The 44 vegetable and 44 soil samples were collected from a total of 44 different greenhouses and each vegetable and soil sample collected from a plastic film greenhouse (about 60 × 10 m) comprised five sub-samples. The ten vegetable species sampled were capsicum (Capsicum annuum), cucumber (Cucumis sativus), Chinese cabbage (Brassica oleracea), radish (Raphanus sativus), green cabbage (Brassica chinensis), lettuce (Lactuca sativa), crown daisy chrysanthemum (Chrysanthemum coronarium), celery (Apium graveolens), spinach (Spinacia oleracea) and pot herb mustard (Brassica juncea). All of the vegetable samples were taken from plastic film greenhouse with mulch film covering the soil surface. The basic physico-chemical properties of the soils at the sampling sites were determined and the mean values were: pH (H2O), 7.4; soil organic carbon, 25.2 g kg−1; total N, 1.53 g kg−1; total P, 1.80 g kg−1 and clay, 15.2% (v/v). Soil samples were collected with a pre-cleaned stainless steel soil auger from the top 15 cm of the profile and small stones, pieces of vegetable litter and roots were removed. All the vegetable and soil samples were transferred to cloth bags and refrigerated during transport to the

J. Wang et al. / Science of the Total Environment 523 (2015) 129–137

laboratory. Precautions were taken during sampling and sample processing to avoid PAE contamination. Vegetable samples were rinsed clean with deionized water, freeze-dried, ground and homogenized by sieving through a stainless steel sieve (60-mesh) (the soil samples were also sieved) and sealed in brown glass bottles. All the vegetable and soil samples were stored at −20 °C until analysis. 2.2. Chemicals and reagents A standard mixture of six PAEs consisting of DMP, DEP, DnBP, BBP, DEHP and DnOP, each at a concentration of 1.0 g mL−1, and an isotope surrogate standard of di-n-butyl phthalate-d4 (DnBP-D4, 0.1 g mL−1) were purchased from Dr Ehrenstorfer (Augsburg, Germany). Neutral silica gel and alumina (100- to 200-mesh) and anhydrous sodium sulfate were activated at 400 ± 1 °C for 6 h. The acetone and n-hexane used were HPLC grade and purchased from Tedia Company Inc., Fairfield, OH. Before use, all glassware was washed in a detergent solution in a laboratory ultrasonic washer (KQ-600DB, Kun Shan Ultrasonic Instruments Co., Ltd., Jiangsu Province, East China), air dried and immersed in sulphuric acid (guaranteed reagent) and washed with tap water and ultra-pure water before oven-drying and rinsing with acetone and n-hexane. No plastic vessels were employed in the experimental procedures. 2.3. Extraction and instrumental analysis The vegetable and soil extraction procedures have been described in detail by Ma et al. (2013) and Wang et al. (2013). For each sample, 3 g (vegetable) or 5 g (soil) was weighed into a glass centrifuge bottle and mixed with 20 mL acetone:hexane (1:1 v/v), left overnight and then ultrasonicated for 30 min. The extracts were reduced by rotary evaporation to 1–2 mL in a water bath at 40 °C and 5 mL hexane was added to the remaining solvent and rotary evaporated to b1 mL but not to dryness. The concentrated sample was subjected to cleanup. Concentrated samples were loaded onto a combined column of neutral silica gel and alumina and anhydrous sodium sulfate. The glass chromatography column (25 cm long, 1 cm i.d.) was packed with 6 cm alumina plus 12 cm neutral silica gel, followed by 2 cm anhydrous sodium sulfate. The cleaned samples were analyzed by gas chromatography–mass spectrometry (GC–MS) using a Hewlett–Packard 7890/5975 GC-MSD (Agilent Technologies, Palo Alto, CA) equipped with a DB-5 trace analysis column (30 m × 0.25 mm × 0.25 μm) fused-silica capillary column for chromatographic separation. The GC oven temperature was held at 50 °C for 1 min and programmed to increase at 15 °C min−1 to 200 °C for 1 min, and finally held at 280 °C at 8 °C min−1 for 3 min. Each extract (1 mL) was injected into the GC–MS system in non-pulse and splitless mode with an injector temperature of 250 °C. The GC–MS transfer line was set at 280 °C and the post run temperature was 285 °C for 2 min. 2.4. Quality assurance and quality control During analysis whole procedure quality assurance and quality control were the same as described previously (Wang et al., 2013, 2014). In brief, the recovery rates of spiked soil and vegetable matrix of the six target PAEs ranged from 76.4 to 109.5% (relative standard deviation b9.1%) in vegetables and soils. The method detection limits of the six target PAEs were 0.03, 0.04, 0.05, 0.02, 0.08 and 0.11 mg kg− 1 for DMP, DEP, DnBP, BBP, DEHP and DnOP, respectively, and the instrumental detection limits were calculated by a signal-to-noise ratio three times the sample concentration and ranged from 0.10 to 0.31 mg kg−1. The limit of detection (LOD) was the lowest concentration that can be detected in the background signal, defined by a signal-to-noise ratio of 3:1, and each PAE concentration of the procedural blanks was subtracted from that of the vegetable and soil samples.

131

Table 1 Parameters for human risk assessment. Parameter Cancer Non-cancer Parameter

Cancer

Iv Is EF ED BW

350,000 200 350 30 65

Ii ABSGI RfDABS RfCi Phthalates

13.5 1 RfDo × ABSGI Assuming equal toRƒDo RƒDo (mg kg−1 CFS (mg kg−1

Non-cancer

AT SA AF ABS PEF

26,280 5300 10,950 0.07 0.1 1.36E+09

DMP DEP DnBP BBP DEHP DnOP

d−1) 10 0.8 0.1 0.2 0.02 0.04

d−1)−1 – – – 1.90E−03 1.40E−02 –

“–”, not available.

2.5. Health risk assessments The non-cancer and carcinogenic risks of PAEs to farmers and children in greenhouses were estimated according to the methods recommended by USEPA (2013). Among the individual PAE congeners studied DMP, DEP, DnBP and DnOP were recognized as non-cancer compounds with respect to human health, while BBP and DEHP did present carcinogenic risk. In the non-cancer and carcinogenic risk assessments of DMP, DEP, DnBP, BBP, DEHP and DnOP via the diet (only considering the intake of vegetables grown in plastic film greenhouse soils) and non-dietary (greenhouse soil ingestion, dermal contact and inhalation) routes were calculated as follows. CR ¼

 X ADD j  C FS

ð1Þ

ADDintake ¼

C v  Iv  E F  ED −6  10 BW  AT

ð2Þ

ADDingest ¼

C s  I s  E F  ED −6  10 BW  AT

ð3Þ

C s  SA  A F  ABS  E F  ED −6  10 BW  AT

ð4Þ

C s  Ii  E F  ED 3  10 PE F  AT

ð5Þ

ADDdermal ¼ ADDinhale ¼

HQ ¼

XADD j  Rf D

ð6Þ

where CR is the carcinogenic risk (unitless); ADDi (mg kg−1 day−1) is the average daily dose via dietary (ADDintake, vegetable intake) and non-dietary (ADDingest, ADDdermal, ADDinhale, soil ingestion, dermal contact and inhalation); CFS is the slope factor of carcinogenic (mg kg−1 days−1)−1; Cv and Cs is the target phthalate in greenhouse vegetable and soil (mg kg− 1); I is the daily intake rate of vegetable (Iv), soil (Is) (mg day−1) and respiratory rate (Ii, m3 day−1); EF is the exposure frequency (days year−1); ED is the exposure duration (years); BW is the body weight (kg); AT is the average lifetime exposure (days); SA is the dermal surface area (cm2 day−1); AF is the soil adherence factor (mg cm2); ABS is the fraction of contaminant dermally absorbed from the soil (unitless); PEF is the particulate emission factor (m3 kg− 1) and a default PEF equal to 1.36 × 109 m3 kg−1 was used; HQ is the hazard quotient; j represents the different exposure pathways; RfD (mg kg−1 day−1) is defined as the daily maximum permissible level of contaminants, including the reference dose for ingestion and intake of contaminated food (RfDo, mg kg−1 day−1), RfDABS is the reference dose for dermal contact (mg kg−1 day−1) and the reference dose of inhalation (RfCi, mg m3); and ABSGI is the fraction of pollutant absorbed in

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the gastrointestinal tract (unitless). It is assumed that the slope factor of carcinogenicity of PAEs via the non-dietary route was the same as CFS. Greenhouse farmers are considered to be exposed to non-cancer risks if the value of HQ is N1. The estimated carcinogenic risks may be considered very low if the value of risk is b 10−6. The values of parameters for non-cancer and carcinogenic risks refer to USEPA (2013), Ji et al. (2014) and Niu et al. (2014) listed in Table 1. 2.6. Statistical analysis Data were processed statistically by analysis of variance (ANONA) and Duncan's multiple range test was used to detect significant differences among mean values of PAEs at p b 0.05 using SPSS 20.0 for Windows (IBM SPSS Inc., Chicago, IL). Drawings were prepared using OriginPro 8.0 software for Windows (OriginLab Northampton, MA). 3. Results 3.1. Variation in PAEs in vegetables and soils The concentrations of the six priority control PAE in vegetables and soils collected from the suburban greenhouses are given in Table 2. The total concentration of the six priority control PAE ranged from 0.51 to 7.16 mg kg−1 and 0.40 to 6.20 mg kg−1 with mean values of 2.56 ± 1.54 mg kg− 1 and 2.23 ± 1.36 mg kg− 1 in vegetables and soils, respectively. The frequency of detection was noticeably different between vegetables and soils and ranged from 38.3 to 100% among the individual vegetables, soils and phthalates. DEHP and DnBP were detected in all vegetables examined. DEP, BBP and DnOP were present in about 90% of vegetable samples, and DMP was detected in only 38.3% of the samples with concentrations ranging from below the MDL to 0.15 mg kg−1. DEHP was also detected in all soil samples and the detection rate of the other five PAEs in soils ranged from 59.6 to 76.6%. In addition, the mean concentrations of DMP, DEP, DnBP and BBP in vegetables were about three to nine times that in corresponding soil samples. DnBP and DEHP were significantly (p b 0.05) higher than the other four PAEs in vegetables and soils with mean concentrations of 0.80 ± 0.48, 1.37 ± 1.28 mg kg− 1 and 0.17 ± 0.34, 1.84 ± 1.16 mg kg−1, respectively. 3.2. PAE concentrations and congener profiles in vegetables and soils Ten vegetables were collected from 44 different suburban plastic film greenhouses and the average concentration of the six priority PAEs was determined by gas chromatography mass spectrometry. The results show that the six priority PAEs can be divided into two groups, namely DEHP, DnBP and DnOP which were the dominant PAEs in the vegetables, and DMP, DEP and BBP which occurred at average concentrations b 0.35 mg kg−1 in the vegetables (Fig. 2). Generally, the individual PAEs in vegetables declined in the order DEHP, DnBP, DnOP, BBP, DEP and DMP. DEHP was the most common PAE in vegetables and ranged from 0.42 to 3.92 mg kg−1, while DMP was the opposite and ranged from below the detection limit to 0.05 mg kg−1. The individual

vegetable species had average PAE concentrations (all mg kg−1) in the descending sequence mustard (5.84 ± 1.62), celery (3.62 ± 1.99), lettuce (3.49 ± 0.89), cucumber (2.59 ± 1.89), Chinese cabbage (2.59 ± 1.80), capsicum (2.46 ± 0.50), spinach (2.04 ± 0.66), green cabbage (2.03 ± 1.32), chrysanthemum (1.80 ± 0.91) and radish (1.63 ± 1.01). The relative contributions of the six PAE congeners in the suburban greenhouse vegetables are shown in Fig. 3A. It is clear that DEHP was the predominant PAE detected in most vegetable samples with total PAE contributions ranging from 25.7 to 67.1%. The second dominant PAE was DnBP, varying from 20.0 to 46.9%, followed by DnOP with a relative contribution in the range of 2.9 to 23.7%. Total contributions of DMP, DEP and BBP were b4.5%, and only about 1.1 and 1.3% in celery and lettuce. The relative contribution and concentration of six PAEs in soils from different plastic film greenhouses are shown in Figs. 3B and 4. DEHP was also the predominant PAE in soil with different vegetables and the average concentrations ranged from 0.84 to 2.38 mg kg−1, and DnBP and DnOP average concentrations ranged from 0.08 to 0.30 mg kg−1, which contributed about 74.7–98.2%, 1.2– 20.3% and 0.6–18.2% to the six PAEs congeners in soil, respectively. The sum concentration of DMP, DEP and BBP was b 0.02 mg kg−1 and the contributions were b1.8% to the six PAE congeners. In addition, the soils planted with Chinese cabbage, lettuce, celery and mustard in greenhouses exhibited elevated total PAE levels. The relative contribution of DEHP to the six PAEs was significantly higher (p b 0.05) than that of the vegetables. 3.3. PAEs in different vegetables and correlations between vegetables and soils In the present study all ten vegetables were classified according to stem, leaf, fruit and roots as edible issues. The stem vegetables were lettuce and celery, the leaf vegetables Chinese cabbage, green cabbage, chrysanthemum, spinach and pot herb mustard, the fruit vegetables capsicum and cucumber, and radish was the only root vegetable studied. The distribution characteristics of PAEs in different types of vegetables are shown in Fig. 5. The total concentrations in stem, leaf, fruit and root vegetables were about 3.55 ± 0.10, 2.86 ± 1.69, 2.53 ± 0.09 and 1.63 ± 1.01 mg kg−1, with the leaf vegetables showing the highest concentrations. DEHP was the dominant PAE with significantly higher concentrations than other PAEs except in radish while DnBP and BBP showed no clear differences. The low molecular weight PAEs DMP and DEP were at higher concentrations in leaf vegetables. Total PAE concentrations in most of the vegetables were higher than in the corresponding soils and about 2.38 and 2.52 times higher in cucumber and mustard, followed by capsicum, lettuce and celery with about 1.5 times the corresponding soils (Fig. 6A). There was no significant (p b 0.05) linear correlation between vegetable and soil PAE concentrations (Fig. 6B). Total PAE concentrations (Fig. 7A) were higher but DEHP concentrations (Fig. 7B) were lower in stem and leaf vegetables than in the corresponding soils. Total PAEs and DEHP in fruit vegetables were higher and in radish were lower than in soils. The relative contribution of DEHP was about 25.7 to 57.9% in the vegetables and 80.9 to 94.3% in the soils across different types of vegetable. PAE

Table 2 Individual concentrations (mg kg−1) of PAEs in vegetables and soils from suburban plastic film greenhouses. Phthalate

DMP DEP DnBP BBP DEHP DnOP Total a

Vegetable

Soil

Min.

Max.

Mean

Median

Detectable rate (%)

Min.

Max.

Mean

Median

Detectable rate (%)

LODa LOD 0.13 LOD 0.12 LOD 0.51

0.15 0.35 1.81 0.09 5.82 1.31 7.16

0.014 ± 0.03 0.04 ± 0.06 0.80 ± 0.48 0.02 ± 0.02 1.37 ± 1.28 0.31 ± 0.35 2.56 ± 1.54

0.03 0.03 0.63 0.02 1.09 0.15 2.23

38.3 93.6 100.0 89.4 100.0 95.7 100.0

LOD LOD LOD LOD 0.24 LOD 0.40

0.04 0.02 2.08 0.10 4.18 2.64 6.20

0.004 ± 0.007 0.005 ± 0.005 0.17 ± 0.34 0.006 ± 0.02 1.84 ± 1.16 0.20 ± 0.43 2.23 ± 1.36

0.03 0.01 0.08 0.02 1.94 0.01 2.24

59.6 76.6 74.5 59.6 100.0 61.7 100.0

LOD, denotes that the value of the sample was b0 after subtracting the method detection limits.

J. Wang et al. / Science of the Total Environment 523 (2015) 129–137

0.35

Phthalate esters in vegetable (mg kg-1)

6.5 6.0 5.5

133

DEHP DnBP DnOP

DMP DEP BBP

0.30

5.0

0.25

4.5 4.0

0.20

3.5 3.0

0.15

2.5 2.0

0.10

1.5 1.0

0.05

0.5 0.0

CA CU CC RA GC LE CR CE SP PM

0.00

CA CU CC RA GC LE CR CE SP PM

Vegetable types Fig. 2. Mean concentrations of PAE and their distributions in different plastic film greenhouse vegetables. The abbreviations CA, CU, CC, RA, GC, LE, CR, CE, SP and PM represent capsicum, cucumber, Chinese cabbage, radish, green cabbage, lettuce, crown daisy chrysanthemum, celery, spinach and pot herb mustard, respectively.

concentrations in the vegetable showed no significant correlation with those in the soils.

4. Discussion 4.1. Occurrence of PAEs in soils

3.4. Risk assessment of greenhouse vegetables and soils

pe ty

DM P P

P

Es

DE

Dn BP OP

Dn

BB

HP

20

PMSP CE R C E Sa L GC A mp R C lin C U gs C A ite C

s

DE

Dn

BB

P

DM P P

0 HP BP

Dn OP

DE

Fig. 3. Relative contributions of six PAE congeners in (A) vegetables and (B) soils from different plastic film greenhouses.

bution (%)

relative contri

40

e

0

DE

PA

PMSP CE Sa CRLE mp C lin G RA gs ite CC U C A s C

60

Es ty p

20

80

PA

40

PAE congener

60

100

B

relative contri

80

Phthalate esters are one of the most ubiquitous group of organic pollutants worldwide (Gibson et al., 2005; Weuve et al., 2010; Wang et al., 2012, 2014; Kong et al., 2012; Sakhi et al., 2014). The six priority PAE concentrations in soils in the present study were 0.4 to 6.2 mg kg−1, similar to some previous studies (0.05 to 10.04 mg kg−1) (Niu et al., 2014; Kong et al., 2012). In Shandong province the total PAE concentrations in greenhouse soils were found to be about 1.94 to 35.44 mg kg−1 (Chai et al., 2014). PAE concentrations found in Chinese soils are significantly higher than in agricultural soils in Denmark (Vikelsøe et al., 2002) or the United Kingdom (Gibson et al., 2005). PAE contamination of greenhouse soils in China therefore seems to be particularly prominent and may be related to the use of plastic film greenhouses instead of glass greenhouses in China, together with differences in soil properties (Niu et al., 2014; Wang et al., 2013). It is well known that the most important source of PAEs in Chinese greenhouse soils is plastic film, with other sources associated with cultivation practices such as application of sewage sludges, manures, sediments, and irrigation

PAE congener

100

A

bution (%)

All six target PAEs may pose non-cancer risks and BBP and DEHP may also represent carcinogenic risk. The results of the risk assessment are summarized in Table 3. In terms of the non-cancer risks via dietary and non-dietary routes, no individual PAE non-cancer risk exceeded the recommended allowable level (HQ b 1) for DMP, DEP, DnBP, BBP, DEHP and DnOP. Non-cancer risks of DnBP, DEHP and DnOP by ingesting vegetables were close to the threshold, and the non-cancer risks of soil ingestion may also be notable. The carcinogenic exposure risks of BBP via dietary and non-dietary routes were much lower than 1 × 10−6 for intake of vegetables and soils. However, carcinogenic risk exposure of DEHP via vegetable ingestion routes was 3.94 ± 3.81 × 10−5, higher than 1 × 10−6, but the carcinogenic risks of DEHP via soils were b 1 × 10−6. In summary, DnBP, DEHP and DnOP represented the greatest threat to the health of farmers in terms of their non-cancer and carcinogenic risks, and ingestion of vegetables and soils was the main route.

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5.5

0.08 DEHP DnBP DnOP

Phthalate concentration (mg kg-1)

5.0 4.5

DMP DEP BBP

0.07 0.06

4.0 3.5

0.05

3.0 0.04 2.5 0.03

2.0 1.5

0.02

1.0 0.01

0.5 0.0

0.00 CA CU CC RA GC LE CR CE SP PM

CA CU CC RA GC LE CR CE SP PM

Greenhouse soils Fig. 4. Mean concentrations of PAEs and their distributions in different plastic film greenhouse vegetables. The abbreviations CA, CU, CC, RA, GC, LE, CR, CE, SP and PM represent the soil collected from capsicum, cucumber, Chinese cabbage, radish, green cabbage, lettuce, crown daisy chrysanthemum, celery, spinach and pot herb mustard greenhouses, respectively.

wastewater containing PAEs as contaminants (Cai et al., 2008; Mo et al., 2008, Wang et al., 2013, 2014). Plastic film is widely used to construct greenhouses throughout China and sediments and sewage sludge containing PAEs are generally used as fertilizers and applied to farmland in southeast China. This may lead to the accumulation of PAEs in soils (Zeng et al., 2008; Chen et al., 2012; Niu et al., 2014). On the other hand, the PAE concentrations and thickness of plastic films, as well as the height and age of the greenhouses, can also influence soil PAE concentrations (Du et al., 2010; Fu and Du, 2011). In addition, the present study demonstrates that DnBP, DEHP and DnOP are the most ubiquitous contaminants in suburban soils. The distribution characteristics of individual PAEs agree with other studies but the individual concentrations were lower (Kong et al., 2012; Wang et al., 2013; Niu et al., 2014; Chai et al., 2014). For example, the mean concentrations of DnBP and DEHP were 15.5 and 4.61 mg kg−1 in Handan, Hebei province, north China (Xu et al., 2008) and were 18.0 and 16.0 mg kg−1 in the Pearl River Delta in south China (Mo et al., 2009). The difference might be due to the type and mode of use of plastic film. Du et al. (2010) demonstrated that different plastic films can impact the PAE concentration in soils, and the ways in which plastic film and mulch film are used can influence soil PAE concentrations (Wang 5.0 Stem vegetable Leaf vegetable Fruit vegetable Root vegetable

4.5

Concentrations (mg kg-1)

4.0 3.5

0.12 0.10 0.08

3.0

0.06 0.04

2.5

0.02

2.0

0.00

1.5

-0.02

DMP

DEP

BBP

1.0 0.5 0.0 Total

DEHP

DnBP

DnOP

DMP

DEP

BBP

Phthalate esters Fig. 5. Corresponding (A) PAE concentrations and (B) correlations between vegetables and soils from suburban plastic film greenhouses.

et al., 2013). PAE contents in finished plastic products varied from 10 to 60% by weight with different PAE types (Staples et al., 1997). Soil physico-chemical properties such as soil organic carbon also influence soil PAE composition and concentrations (Kong et al., 2012; Wang et al., 2014). DnBP, DEHP and DnOP have relatively high molecular weights and low vapor pressures and thus readily absorbed to soil organic carbon (Schmitzer et al., 1988; Zeng et al., 2008; Niu et al., 2014). Therefore, the difference in DnBP, DEHP and DnOP relative concentrations between the present study and other studies is not unexpected. 4.2. Occurrence of PAEs in vegetables The total PAE concentrations in the present study ranged from 0.51 to 7.16 mg kg−1, markedly lower values than those reported in other studies (Mo et al., 2009; Wu et al., 2013; Du et al., 2010). Fu and Du (2011) reported that the accumulation of DEHP in vegetables such as pot herb mustard, bok choi, garlic, celery, spinach, cabbage, lettuce and amaranth and the total PAE concentrations was about 0 to 55.1 mg kg−1 in greenhouse vegetables (Chen et al., 2012). The vegetable PAEs differed notably from those in the soils in terms of the proportions of different target contaminants. The proportion of DEHP was lower but DnBP and DnOP were significantly higher (p b 0.05) in vegetables (Fig. 3). Schmitzer et al. (1988) found that soil DEHP was mineralized or converted into soil-bound residues and this restricted vegetable uptake. This may explain the absence of significant correlations between vegetable and soil PAE concentrations and especially DEHP. Furthermore, the concentrations and proportions of DMP and DEP in the vegetables were also higher than in the soils. This might be due to these lower molecular weight PAEs being readily emitted to the atmosphere and taken by the vegetables with their large surface area exposed to PAE vapors in the greenhouse atmosphere (Wang et al., 2012; Ma et al., 2013). Moreover, PAEs can accumulate in vegetables (Dorney et al., 1985) and are affected by several factors such as vegetable type, mode of use of plastic film, the time period over which the greenhouse is covered with film, greenhouse height and age and the type of plastic film (Mo et al., 2009; Du et al., 2010; Wang et al., 2013). Wu et al. (2013) found that Benincasa hispida absorbed DEHP from the air and accumulated it in the leaves, stems and fruits. Stem and leaf vegetable had higher PAE concentrations while fruit and root vegetables were lower in this study, perhaps because the stem and leaf vegetable had large surface areas and longer exposure times to the PAEs (Ma et al., 2013). DEHP concentrations in greenhouse pot

J. Wang et al. / Science of the Total Environment 523 (2015) 129–137

8

8

A

Total PAEs in vegetables Total PAEs in soil

B 7

Total PAEs in vegetables (mg kg-1)

Phthalate concentration (mg kg-1)

7

135

6 5 4 3 2 1

6 5 4 3 2 1

0 CA CU CC RA GC LE CR CE

SP

0 0.0

PM

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

4.5

5.0

Total PAEs in soils (mg kg-1)

Vegetable types

Fig. 6. Corresponding PAE concentration (A) and correlations (B) between vegetables and soils from suburban plastic film greenhouses.

herb mustard, celery and lettuce were up to 34.0, 22.0 and 25.0 mg kg−1 (Fu and Du, 2011), about six, six and seven times the values in the present study. The differences may be due to different types of plastic film and sampling times, as well as the height of each greenhouse and the mode of use of plastic film (Du et al., 2010; Wang et al., 2012). 4.3. Risk assessment of exposure to PAEs Previous studies show that concentrations of several PAEs such as dimethyl phthalate (DMP), diethyl phthalate (DEP), DnBP and DEHP in Chinese soils far exceed the allowable concentrations recommended by New York State Department of Environmental Conservation (2010) (Zeng et al., 2008; Wang et al., 2013). In the present study, in about 48% of the soil samples the DnBP concentration exceeded the recommended allowable concentration (DnBP, 0.08 mg kg− 1) set by New York State Department of Environmental Conservation (2010). The environmental risk limits for DnBP and DEHP in fresh soils and sediments with 10% organic matter are 0.7 and 1.0 mg kg−1, respectively, based on the (eco)toxicology and environmental chemistry data (van Wezel et al., 2000) and DnBP and DEHP concentrations in about 4.5 and 75% of all the soil samples analyzed exceeded these limits. In addition, PAEs can destroy the fluidity of cell membranes and thus affect the

activity of the soil microbial community and its metabolic diversity and enzyme activities (Xie et al., 2010). Moreover, PAEs can accumulate in vegetables and thus contaminate the human food chain (Hauser and Calafat, 2005; Franco et al., 2007; Chen et al., 2008; Ma et al., 2013). About 79.5 and 25.0% of vegetable samples in the present study exceeded the European food standard limits for DnBP (0.3 mg kg−1) and DEHP (1.5 mg kg−1) in vegetable (Laturnus and Grøn, 2007) limits. By controlling the mode of use of plastic film, cover time and cultivation method, the environmental risk of PAEs and their accumulation in soils and vegetables can be effectively reduced (Wang et al., 2012; Chai et al., 2014). However, only a few studies have reported PAE risks from vegetables. Ma et al. (2013) reported that PAEs might represent a human health risk due to the fact that intake of vegetables and DEHP might present the highest exposure risk. Daily intake of PAEs of nonoccupational consumers was mainly via the dietary route especially from vegetables and fruits (Franco et al., 2007; Chen et al., 2012). In the present study the risk to human health of exposure to PAEs via dietary and non-dietary routes was evaluated using the methods recommended by USEPA (Niu et al., 2014; Ji et al., 2014). The non-cancer risks of DEHP, DnBP and DnOP are higher but are still b 1, and this criterion is used to judge whether the risk is within an acceptable range.

5.0

A

4.0 3.5 3.0 2.5 2.0 1.5 1.0

vegetable soil

B DEHP concentration (mg kg-1)

Total PAEs concentration (mg kg-1)

4.5

3.5

vegetable soil

3.0 2.5 2.0 1.5 1.0 0.5

0.5 0.0

Stem vegetable Leaf vegetable Fruit vegetable Root vegetable

Vegetable type

0.0

Stem vegetable Leaf vegetable Fruit vegetable Root vegetable

Vegetable type

Fig. 7. Corresponding total PAEs (A) and DEHP (B) concentrations in vegetables and soils with different vegetable types.

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Table 3 Exposure risks to farmers from plastic film greenhouse vegetables and soils. Congener

HQvegetable

HQingest

HQdermal

HQinhale

DMP DEP DnBP BBP DEHP DnOP

(6.72 ± 15.51) × 10−6 (2.45 ± 3.61) × 10−4 (3.91 ± 2.54) × 10−2 (5.16 ± 4.64) × 10−4 (3.38 ± 3.26) × 10−1 (3.83 ± 4.47) × 10−2

(1.18 ± 2.07) × 10−9 (1.84 ± 1.84) × 10−8 (5.19 ± 9.59) × 10−6 (8.85 ± 25.08) × 10−8 (3.20 ± 2.17) × 10−4 (1.40 ± 3.08) × 10−5

(2.35 ± 4.11) × 10−10 (3.68 ± 3.68) × 10−9 (1.04 ± 1.92) × 10−6 (1.77 ± 5.02) × 10−8 (6.39 ± 4.33) × 10−5 (2.80 ± 6.15) × 10−6

(3.81 ± 6.67) × 10−12 (5.95 ± 5.95) × 10−11 (1.68 ± 3.09) × 10−8 (2.86 ± 8.10) × 10−10 (1.03 ± 0.70) × 10−6 (4.52 ± 9.92) × 10−8

CRvegetable

CRingest

CRdermal

CRinhale

(8.18 ± 7.36) × 10−8 (3.94 ± 3.81) × 10−5

(1.40 ± 3.97) × 10−11 (3.74 ± 2.53) × 10−8

(2.60 ± 7.37) × 10−12 (6.94 ± 4.70) × 10−9

(4.52 ± 12.81) × 10−14 (1.21 ± 0.82) × 10−10

BBP DEHP

DEHP exhibited elevated levels of non-cancer risk and this is consistent with previous studies (Chen et al., 2012; Ma et al., 2013). The carcinogenic risk of DEHP would be regarded as low with a value of about 3.94 × 10− 5 according to Niu et al. (2014). Almost all of the noncancer and carcinogenic risks to farmers of PAEs are due to direct intake of vegetables and soils. PAE intake can be especially harmful to pregnant women and school-age children (Lovekamp-Swan and Davis, 2003; Cho et al., 2010; Jurewicz and Hanke, 2011; Casas et al., 2011; Liu et al., 2012). Even when the overall health risk of PAEs is low in greenhouse vegetable–soil systems the long-term health risk from long-term exposure to low doses cannot be ignored. The potential damage of PAE compounds to human health should be taken into consideration in further comprehensive risk assessments of Chinese greenhouses. 5. Conclusions PAEs were detected in all greenhouse vegetable and soil samples analyzed. DnBP, DEHP and DnOP were the predominant PAE congeners present with higher concentrations and frequency of detection in the vegetables and soils. They contributed more than 90% of the total PAEs but their composition was significantly different between vegetables and soils. PAE concentrations in different vegetables varied widely and were not correlated with the corresponding soils. PAE concentrations decreased in the sequence stem, leaf, fruit and root vegetables. Additionally, DnBP and DEHP concentration in vegetable and soil samples exceeded the standard limits based on food security standards or environmental risks of countries other than China. The concentrations of PAEs found in this study were lower than those reported in other regions of China. This might be due to differences in types of plastic film and use mode, as well as soil type. Moreover, human health risks of PAEs to farmers in the vegetable–soil system are mainly derived from vegetable intake by the dietary route and ingestion of soils at work. The non-cancer risks of DnBP, DEHP and DnOP were close to the limits and the carcinogenic risk of DEHP exceeded the acceptance level. Further studies are required to further elucidate the risks to farmers and consumers from phthalates in vegetables produced using plastic film greenhouses. Acknowledgments This study was funded by the Chinese National Environmental Protection Special Fund for Scientific Research on Public Causes (2010467016 and 201209030), the Chinese National Critical Patented Projects in the Control and Management of Polluted Water Bodies (2012ZX07104-001) and the grants from Key Laboratory of Soil Environment and Pollution Remediation (SEPR2014-08), Institute of Soil Science, Chinese Academy of Sciences. References Bell, F.P., 1982. Effects of phthalate esters on lipid metabolism in various tissues, cells and organelles in mammals. Environ. Health Perspect. 45, 41–50.

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