Lu 18
Lu 18
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Environmental Research
journal homepage: www.elsevier.com/locate/envres
Review article
Soil contamination and sources of phthalates and its health risk in China: A T
review☆
Huixiong Lüa, Ce-Hui Mob, Hai-Ming Zhaob, Lei Xiangb, Athanasios Katsoyiannisc, Yan-Wen Lib,
⁎
Quan-Ying Caib, , Ming-Hung Wongb,d
a
College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
b
Guangdong Provincial Research Center for Environment Pollution Control and Remediation Materials, College of Life Science and Technology, Jinan University,
Guangzhou 510632, China
c
Norwegian Institute for Air Research (NILU) – FRAM High North Research Centre on Climate and the Environment, Hjalmar Johansens gt. 14, NO-9296 Tromsø, Norway
d
Consortium on Health, Environment, Education and Research (CHEER), Department of Science and Environmental Studies, the Education University of Hong Kong, Hong
Kong, China
A R T I C LE I N FO A B S T R A C T
Keywords: Phthalates (PAEs) are extensively used as plasticizers and constitute one of the most frequently detected organic
Phthalic acid esters contaminants in the environment. With the deterioration of eco-environment in China during the past three
Soil pollution decades, many studies on PAE occurrence in soils and their risk assessments have been conducted which allow us
Spatial distribution to carry out a fairly comprehensive assessment of soil PAE contamination on a nation-wide scale. This review
Uptake
combines the updated information available associated with PAE current levels, distribution patterns (including
Human exposure
urban soil, rural or agricultural soil, seasonal and vertical variations), potential sources, and human health
exposure. The levels of PAEs in soils of China are generally at the high end of the global range, and higher than
the grade II limits of the Environmental Quality Standard for soil in China. The most abundant compounds, di-n-
butyl phthalate (DBP) and di-(2-ethylhexyl) phthalate (DEHP), display obvious spatial distribution in different
provinces. It is noted that urbanization and industrialization, application of plastic film (especially plastic film
mulching in agricultural soil) and fertilizer are the major sources of PAEs in soil. Uptake of PAEs by crops, and
human exposure to PAEs via ingestion of soil and vegetables are reviewed, with scientific gaps highlighted.
1. Introduction et al., 2017; Sun et al., 2018), and biota (Mo et al., 2009; Wang et al.,
2015). The wide occurrence of PAEs in the environment can result in
Phthalic acid esters (PAEs, or simplier phthalates) are extensively human potential exposure to PAEs via ingestion, inhalation and dermal
used as plasticizers in industrial products such as plastics and poly- absorption from different sources (e.g., food, water, air, dust and soil)
vinylchloride to enhance their plasticity and versatility, and also widely (Guo et al., 2012; Net et al., 2015a), as confirmed by the high detection
used in non-polymeric products, such as solvents in adhesives, cos- frequencies of phthalate metabolites in human matrice samples (e.g.,
metics, paints, (Staples et al., 1997; Zolfaghari et al., 2014; Steinmetz urine, blood) from different countries (Guo et al., 2014; Net et al.,
et al., 2016). Global annual production of solid plastics was about 300 2015a; Bui et al., 2017; Polinski et al., 2018). Numerous epidemiolo-
million tones each year (Garcia1and Robertson, 2017) with China one gical and toxicological studies have demonstrated that some PAE
of the largest consumers. PAEs are not chemically bound to the poly- compounds are endocrine disrupting chemicals (Bui et al., 2017; Chen
meric and non-polymeric products, and hence, they can easily migrate et al., 2017a). Butyl benzyl phthalate (BBP) and di-(2-ethylhexyl)
from products and have been released as xenobiotic and hazardous phthalate (DEHP) are classified as probable and possible human car-
compounds into the environment (Kong et al., 2012; Benjamin et al., cinogens by US Environmental Protection Agency (USEPA), respec-
2015). tively (USEPA, 2007). The global occurrence of PAEs and their various
Many studies have reported the ubiquitous nature of PAEs in air and health effects have raised increasing concern of public, scientific and
water (Philip et al., 2018), sludge (Cai et al., 2007; Zolfaghari et al., governmental organizations. The environmental protection agencies of
2014), soil (Cai et al., 2008a; Niu et al., 2014; Net et al., 2015a; Wang various countries including US, Canada, China, and EU (European
☆
This work does not deal with research or studies on human subjects or experimental animals.
⁎
Corresponding author.
E-mail address: [email protected] (Q.-Y. Cai).
https://doi.org/10.1016/j.envres.2018.03.013
Received 15 January 2018; Received in revised form 28 February 2018; Accepted 8 March 2018
0013-9351/ © 2018 Elsevier Inc. All rights reserved.
H. Lü et al. Environmental Research 164 (2018) 417–429
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H. Lü et al. Environmental Research 164 (2018) 417–429
Table 1
Concentration (mg/kg) of phthalic acid esters (PAEs) in the soil of different regions, China.
Min Max Mean Median Min Max Mean Median Min Max Mean Median
Whole country Agricultural (123b) 0.004 0.46 0.066 0.052 ND 6.22 0.82 0.56 0.032c 6.29c 1.09c 0.85c Niu et al. (2014)
North China
Beijing Urban (30) 0.28 3.8 0.79 0.46 0.17 6.5 1.9 1.4 0.51 8.0 2.8 2.2 Li et al. (2006)
Beijing Urban (127) 0.0002 2.58 0.99 0.99 0.0002 1.35 0.14 0.019 0.002d 3.14d 1.14d 1.10d Xia et al. (2011)
Beijing Surface (62) 2.3e 24.7e Zhang et al.
(2014)
Beijing Surface (47) 0.09 0.11 0.02 1.36 – – Cheng et al.
(2015)
Beijing Vegetable (60) – 1.23 0.44 0.42 – 1.22 0.38 0.37 0.14c 2.13c 0.99c 0.96c Li et al. (2016a)
Tianjin Agricultural (85) 0.01 0.28 0.07 – 0.03 4.17 0.29 – 0.05 10.4 0.32 Kong et al. (2012)
Tianjin Surface (11) 0.10 1.03 0.34 0.23 0.22 0.83 0.50 0.46 0.53f 5.53f 1.05f 0.87f Zhu et al. (2010)
Shenyang Agricultural (41) 0.18 0.88 0.44 0.19 0.58 0.27 0.52 1.73 0.94 Li et al. (2017)
Hebei Agricultural (39) 0.035 0.054 0.045 0.045 0.066 0.26 0.14 0.13 0.19 0.46 0.29 0.29 Zhang et al.
(2015a)
Handan Agricultural (4) 3.18 29.4 14.1 – 1.15 7.99 4.86 – – – – – Xu et al. (2008)
Round-Bohai Bay- Agricultural (130) 0.16 0.046 Chen et al. (2016)
Region
Shijiazhuang Agricultural (13) 0.035 0.054 0.044 – – – – – 0.23 0.69 0.37 – Niu et al. (2014)b
Shijiazhuang Agricultural (13) – – 0.125 – – – 0.364 – – – – – Tan et al., 2016
North China Agricultural (4) 0.14 0.98 0.56 – 0.51 2.2 1.38 – 1.8g 3.8g 2.8g 2.4g Hu et al. (2003)
Northeast China
Northeast China Agricultural (3) 0.16 1.6 0.71 – 3.3 7.1 5.2 – 4.4g 10g 6.7g 2.7g Hu et al. (2003)
Northeast China Surface (27) 0.51 0.96 0.46 0.52 2.1 1.1 1.37c 4.90c – 2.83c Zhang et al.
(2015b)
Harbin Agricultural (4) 2.75 14.6 7.6 – 0.49 4.2 2.4 – – – – – Xu et al. (2008)
Sanjiang Plain Natural and reclaimed 0.001 0.13 0.28 – 0.003 0.11 0.28 – 0.07 0.38 Wang et al.
wetlands (23) (2013a)
Sanjiang Plain Agricultural (36) 0.02 0.35 – – 0.033 0.58 – – 0.16 0.95 0.37 – Wang et al.
(2017)
Northwest China
Xi’an Urban (62) 0.08 1.71 0.52 – 0.04 17.2 0.76 – 0.19 19.1 1.37 – Wang et al.
(2018)
Xianyang Vegetable (59) 0.037 6.31 0.31 – ND 3.87 0.16 – 0.13 10.3 0.63 – Xu et al. (2014)
South Xinjiang Cotton (3) 11.2 57.7 28.3 – 104 149 129 – 124 1232 – – Guo and Wu
(2011)
Jiamusi Agricultural (184) ND 1.85 0.24 – ND 8.58 2.00 – ND 10.3 2.26 Li (2014a)
Three Gorges Agricultural (32) 0.01 0.35 0.25 0.29 0.04 0.28 0.12 0.11 0.18 0.88 0.62 0.68 He et al. (2017)
Reservoir Region
Riparian (26) ND 0.34 0.22 0.28 ND 0.32 0.11 0.11 0.098 0.80 0.56 0.68 He et al. (2017)
East China
Yellow River Delta Surface (82) 0.14 2.06 1.92 – 0.43 6.32 0.74 – 0.79 8.53 2.98 – Yang et al. (2013)
Yangtze River Delta Agricultural (241) ND 1.50 0.095 0.074 ND 9.19 0.55 0.35 0.17c 9.37c 0.78c 0.56c Sun et al. (2016)
Shandong Agricultural (17) 0.092 1.65 0.76 – 0.17 1.08 0.44 – 0.34 2.81 1.22 – Cui et al. (2013)
Shandong Peninsula Vegetable (111) 0.016 15.7 1.47 – 0.073 5.32 1.46 – 1.94h 35.4h 6.75h – Chai et al. (2014)
Shandong Peninsula Agricultural (108) ND 9.86 1.99 – ND 2.94 0.29 – 1.37 18.8 6.47 – Li et al. (2016b)
Qingdao Agricultural (17) 9.02 13.0 11.2 – 12.5 35.8 20.0 – – – – – Zhang et al.
(2013)
East China Agricultural (7) 0.21 1.4 – – 0.20 6.0 – – 1.3g 7.1g 4.0g 2.6g Hu et al. (2003)
Xiangyang Non-industrialized area, 0.18 18.2 1.72 – 0.36 153 13.4 – 2.21 158 19.1 – Wu et al. (2015)
Surface (142)
Electronics manufa- 0.26 31.2 5.70 – 2.24 153 21.3 – 8.63 172 35.3 – Wu et al. (2015)
cturing area (145)
JiangHan Plain Surface (17) ND 0.29 0.082 – 0.009 0.60 0.33 – 0.023 5.30 0.93 – Liu et al. (2010a)
Wuhan Surface (4) ND 0.12 0.06 – 0.20 0.46 0.32 – 0.29 1.23 0.68 – Liu et al. (2010b)
Taizhou E-Waste Recycling Sites 12.6d 46.7d – – Liu et al., 2009
(9)
Ningbo Agricultural (1) – – 0.25 – – – 2.24 – – – 2.58 – Hu et al. (2003)
Huzhou Agricultural (74) ND 0.34 0.02 – ND 0.84 0.11 – ND 1.10 0.16 – Fei et al. (2010)
Nanjing Vegetable (127) ND 1.83 0.21 0.13 0.021 9.03 1.82 1.08 0.15 9.68 2.26 1.65 Wang et al.
(2013b)
Nanjing Vegetable (44) ND 2.08 0.17 0.08 0.24 4.18 1.84 1.94 0.40 6.20 2.23 2.24 Wang et al.
(2015)
Nanjing Vegetable (305) 0.30 0.95 0.22 1.60 0.87 3.95 Ma et al. (2015)
Hangzhou Vegetable (10) 0.14 0.35 0.21 0.81 2.20 1.48 – 1.90 4.36 2.75 – Chen et al. (2011)
Northwest China Agricultural (2) 0.38 0.39 – – 1.7 2.2 – – 2.2g 2.8g 2.5g – Hu et al. (2003)
Yintan Agricultural (1) – – 1.38 – – – 5.38 – – – 6.97 – Hu et al. (2003)
Xiamen Agricultural (1) – – 0.21 – – – 2.67 – – – 2.93 – Hu et al. (2003)
South China
South China Agricultural (4) ND 0.26 0.21 – 0.54 3.42 1.74 – 0.89g 3.2g 1.9g 1.7g Hu et al. (2003)
Pearl River Delta Vegetable (50) 3.8 18 9.5 9.2 6.2 16 11 9.3 3.0 46 21 21 Cai et al. (2005)
Guangdong Agricultural (444) ND 17.5 0.31 – ND 6.48 0.15 – ND 26.0 0.67 – Yang et al. (2007)
Guangzhou Urban (37) 0.21 30.1 4.06 1.80 0.89 264 35.8 14.8 1.67 h 322h – 17.7h Zeng et al. (2009)
(continued on next page)
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H. Lü et al. Environmental Research 164 (2018) 417–429
Table 1 (continued)
Min Max Mean Median Min Max Mean Median Min Max Mean Median
Guangzhou Agricultural (40) 0.009 2.74 0.34 – 0.11 29.4 1.76 – 0.20h 33.6 h 2.57h 0.68h Zeng et al. (2008)
Dongguan Vegetable (19) 0.01 0.28 0.14 – 0.07 1.47 0.41 – 0.37 1.71 0.76 – Zhang et al.
(2009)
Huizhou Agricultural (49) ND 0.39 0.15 – ND 0.44 0.088 – 0.087g 0.75g 0.31g – Tan et al., 2012
Leizhou Agricultural (71) ND 1.77 0.28 – ND 1.39 0.14 – ND 5.45 0.74 – Guan et al. (2007)
Southwest China
Southwest China Agricultural (3) 0.51 0.64 0.57 – 1.9 3.0 1.55 – 1.9g 30g 2.2g 1.9g Hu et al. (2003)
Guilin Agricultural (16) ND 0.41 0.13 – ND 0.58 0.25 – 0.001 1.17 – – Liu et al. (2013)
Anshun Agricultural (1) – – 0.51 – – – 2.08 – – – 2.96 – Hu et al. (2003)
Kunming Agricultural (1) – – 0.64 – – – 1.02 – – – 1.85 – Hu et al. (2003)
Other country
Denmark Agricultural (7) 0.0005 0.45 0.11 – 0.012 1.9 0.39 – 0.014 2.5 0.53 – Vikelsøe et al.
(2002)
Scotland Surface (182) – – – – 0.025 1.60 0.22 – – – – – Rhind et al.
(2012)
Netherlands Agricultural (34) ND – – 0.006h ND – 0.032h – – – – – Peijnenburg,
2006
Serbia Surface (30) 0.030 0.14 0.72 0.68 0.13 2.04 0.73 0.75 0.19 2.12 0.83 0.84 Škrbić et al.
(2016)
UK Agricultural (2) 0.008 0.0008 0.0008 – 0.022 0.076 0.049 – 0.042 0.099 0.071 – Gibson et al.
(2005)
a
Sum concentration of six USEPA priority PAEs, i.e., DMP, DEP, DBP, BBP, DOP and DEHP; Unless otherwise mentioned.
b
Number of samples or sampling sites.
c
Sum concentration of 15 PAE compounds, including six US EPA priority PAEs.
d
Sum concentration of DMP, DEP, DBP, DOP and DEHP.
e
Sum concentration of DMP, DEP, DBP, di-iso-butyl phthalate, and DEHP.
f
Sum concentration of 12 PAE compounds, including six US EPA priority PAEs.
g
Sum concentration of DMP, DEP, DBP and DEHP.
h
Sum concentration of 16 PAE compounds, including six US EPA priority PAEs.
Environmental Quality Standard in China (GB-15618–2008) (China 2009; Wang et al., 2013b, 2016; Niu et al., 2014). DMP, DEP, DBP and
National Environmental Protection Agency, 2008), implying that some DEHP showed higher detection frequencies (up to 100%) in most stu-
soil in China was contaminated by PAEs. dies, while dimethylglycol phthalate, di(2-n-butoxyethyl) phthalate, di-
The detection frequencies of individual PAE compounds varied n-nonyl phthalate, di(hexyl-2-ethylhexyl) phthalate, etc., displayed re-
greatly with the congeners of PAEs and sampling sites (Zeng et al., latively low detection frequencies or their concentrations were below
Fig. 2. Average concentrations of DBP and DEHP in soil of different cities and provinces. The concentrations referred to arithmetic average ones, calculated bases on all concentrations for
the same province or city reported in the literature.
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H. Lü et al. Environmental Research 164 (2018) 417–429
the detection limits. DBP and DEHP are the dominant PAEs detected in effusion, industrial processes, municipal sewage, and atmospheric de-
most soil samples. The concentrations of DBP varied from ND (not positions (Zeng et al., 2009; Wang et al., 2018). The urban districts are
detectable) to 31.2 mg/kg (Table 1), accounting in some cases for up to generally developed from the inner cities to exterior areas and showed a
85% of the ΣPAEs (Xia et al., 2011). The average concentration of DBP in decreasing urbanization history with increasing distance from the city
most soil samples was < 10 mg/kg (except in soil of Qingdao reported centers (Xia et al., 2011). The period of PAE accumulation would thus
by Zhang et al., 2013 and of South Xinjiang reported by Guo and Wu, decrease from the centers outward with the diminishing age of cities
2011), and < 1.0 mg/kg in at least 50% of studies. DEHP concentra- from the centers to the suburbs (Xia et al., 2011). Furthermore, the
tions were also among the dominants and ranged from ND to 264 mg/ usage amount of plastic products in daily lives of residents also affects
kg with a mean of < 25 mg/kg (except in soil of South Xinjiang re- the soil levels of PAEs (Zhang et al., 2014).
ported by Guo and Wu, 2011), accounting in some cases, similarly to Concerning the levels of PAEs in urban soils with different types of
DBP, for about 90% of the ΣPAEs (Niu et al., 2014). land use, the highest concentrations of DBP and DEHP as well as ΣPAEs
The average concentrations of DEHP in most regions of China were in Beijing were recorded in classical gardens, followed by culture and
higher than in soils reported from abroad, for example in Scotland educational areas, business areas, residential areas, while lower con-
(Rhind et al., 2012). In most cases, the concentrations of DEHP were centrations were observed in large public green space and roadside
higher than those of DBP in the same site (Kong et al., 2012; Wang areas (Xia et al., 2011). While relatively higher concentrations of PAEs
et al., 2013a, 2013b; Niu et al., 2014; Zhang et al., 2015a), but in some were observed in industrial, traffic, and residential areas than in parks
cases the former was lower than the latter (Xia et al., 2011). Regarding and educational areas in Xi’an (Wang et al., 2018). Different from
the other congeners, the concentrations of DMP, DEP, BBP, DOP, etc., Beijing and Xi’an, the highest concentrations of DBP, DEHP and ΣPAEs
were generally < 1.0 mg/kg, even < 0.1 mg/kg, accounting for gen- were found in the soils from roadside areas in Guangzhou; and con-
erally < 50% of the ΣPAEs (Zeng et al., 2009; Xia et al., 2011; Niu et al., centrations in soils of parks in Guangzhou were comparable or higher
2014; Zhang et al., 2015a). Compared to the recommended values of than those in residential areas (Zeng et al., 2009). Similarly, higher
soil cleanup guideline for PAEs (New York State Department of average concentrations of DBP, DEHP and ΣPAEs were found in roadside
Environmental Conservation, 2003), the levels of DMP, DEP, DBP and areas than residential areas of Xiangyang (Wu et al., 2015). The spatial
DEHP in some soils exceeded their limits (0.02, 0.071, 0.081, 4.35 mg/ distributions of PAEs in urban soil were related to the history of cities,
kg, respectively). In some cases, the standard exceeding rates of DMP intensity of industrial and commercial activities, which are confirmed
and DBP were up to 100% in topsoil soils (Zhang et al., 2014). by features of point sources in Beijing and Guangzhou.
The average concentrations of DEHP and DBP in each province or
autonomous region provide insights into the regional patterns (Table 1 2.3. PAE levels in rural or agricultural soils
and Fig. 2). The highest average concentrations of DEHP (6.60 mg/kg)
were observed in Guangdong Province, followed by Shandong and With agricultural modernization, plastic mulching and plastic film
Hubei provinces (4.9 mg/kg). Higher average concentrations of DBP greenhouses have become very popular for agricultural production
(> 2.0 mg/kg) were noted in Shandong, Heilongjiang, and Guangdong throughout China. The residue of PAEs in soil is of great concern. Thus,
provinces (Fig. 2). The average concentrations of DBP and DEHP many studies have investigated the occurrence and distribution of PAEs
were < 1.0 and 3.0 mg/kg, respectively, in other provinces or cities in rural or agricultural soils throughout China, including vegetable
(except DEHP in Xinjiang autonomous region). These results demon- field, paddy field, orchard, wasteland, etc. (Tables 1 and 3). The levels
strate regional variations in soil PAE levels in China. The variations are of PAEs in agricultural soil were generally less than those in urban soil
likely due to differences in urbanization levels, industrial discharges, in the same regions (Zeng et al., 2008, 2009; Yang et al., 2013). The
use of plastic films in agriculture, application of municipal biosolids and highest concentrations of DBP, DEHP and ΣPAEs (11.2–1232 mg/kg)
agricultural chemicals, and wastewater irrigation. were reported in cotton field in South Xinjiang (Guo and Wu, 2011),
being significantly higher than other agricultural soils. Relatively
2.2. PAE levels in urban soils higher concentrations of DBP, DEHP and ΣPAEs were also found in the
agricultural soil of Qingdao, Shandong Province (Zhang et al., 2013)
The distributions of PAEs in urban, suburban and rural soil have and vegetable soil of the Pearl River Delta, Guangdong Province (Cai
been investigated in Beijing, Tianjin, Guangzhou, Xiangyang, Xi’an, and et al., 2005). Nevertheless, Niu et al. (2014) reported that three pro-
Yellow River Delta (Table 2). The highest ΣPAEs was found in the urban vinces (i.e., Fujian, Guangdong and Xinjiang) showed the highest
soils of Guangzhou, with 322 mg/kg in the soil of a site around the loadings of PAEs in agricultural soil (Σ15PAEs < 6.37 mg/kg). The in-
refuse transfer station and 216 mg/kg in the soil of the largest elec- consistent trend of PAE levels in agricultural soil was probably due to
tronic/electrical commercial town in South China (Zeng et al., 2009). the variation in the sample numbers analyzed or calculated. In the
High ΣPAEs was also observed in soils from roadsides (and/or gutters) of study of Niu et al. (2014), soil samples (123 from 31 provinces and
Guangzhou, which resulted from the accumulation of the contaminants autonomous regions across China) were relatively limited, which may
washed off from roofs and/or grounds (Zeng et al., 2009). Relatively result in poorly representative, underestimated or overestimated levels
higher ΣPAEs (ranging from 2.21 to 158 mg/kg) was observed in the soil of PAEs in agricultural soils.
of roadsides, residential areas, and non-cultivated areas in Xiangyang In most agricultural soils, the maximum levels of DBP, DEHP and
(Wu et al., 2015). The ΣPAEs in soil from Beijing, Tianjin, Xi’an, and ΣPAEs were < 40 mg/kg, even < 10 mg/kg (Table 1). For example, the
Yellow River Delta were < 5.0 mg/kg, even < 1.0 mg/kg, far lower levels of DBP, DEHP and ΣPAEs were all less than 10 mg/kg in agri-
than those in Guangzhou (Tables 1 and 2), a city that is highly in- cultural soils from Beijing (Li et al., 2016a), Tianjin (Kong et al., 2012),
dustrialized. Xianyang (Xu et al., 2014), Nanjing (Wang et al., 2013b), Hangzhou
Elevated concentrations of PAEs in soil were found in city centers or (Chen et al., 2011), and Guilin (Liu et al., 2013), even < 1 mg/kg in
in sites located next to urban districts, and a general decreasing trend Sanjiang Plain of northeast China (Wang et al., 2017). Additionally,
was observed of the concentrations with the distance from the urban Chen et al. (2016) reported that PAEs were detected in only one out of
centers (Zeng et al., 2008; Xia et al., 2011). Nevertheless, Wang et al. 130 soil samples from solar greenhouse fields in Round-Bohai Bay-Re-
(2018) found that the concentrations of BBP, DEHP and Σ6PAEs in- gion, with the concentrations of DiBP, DBP, and DEHP being 0.14, 0.16,
creased while those of DnOP decreased from the first to third ring roads and 0.046 mg/kg, respectively, implying that solar greenhouse resulted
in Xi’an city. These results confirmed that anthropogenic activities have in lower PAE contamination than plastic film greenhouse.
heavily influenced the levels of PAEs in soil. PAEs in urban soil mainly Some studies have revealed that the PAE levels in soil were different
originate from application of plasticizers or additives, discarded plastic by land use types. For instance, in Guangdong province, the Σ6PAEs
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H. Lü et al. Environmental Research 164 (2018) 417–429
Table 2
Concentrations of PAEs (mg/kg) in urban and rural soils.
Range Mean ± SD Median Range Mean ± SD Median Range Mean Median Range Mean Median
a
Sum concentration of five PAE compounds, including DMP, DEP, DBP, DOP and DEHP. The ΣPAEs refer to sum concentration of six USEPA priority PAEs, unless otherwise mentioned.
b
Soil from traffic areas.
c
Soil from non-industrialized area.
d
Sum concentration of 16 PAE compounds, including six US EPA priority PAEs.
e
Soil with application of sewage sludge, and the ΣPAEs was sum concentration of 9 PAE compounds, including six US EPA priority PAEs.
decreased in the order of paddy soil > banana soil > vegetable soil > soil > farmland soil > orchard soil (Kong et al., 2012); in Guilin city
sugarcane soil > orchard soil (Yang et al., 2007); in Tianjin city, Σ6PAEs (Guangxi Zhuang Autonomous Region), Σ6PAEs decreased in order of
exhibited decreasing order as vegetable soil > wasteland farmland soil > vegetable soil > orchard soil (Liu et al., 2013); while in
Table 3
Concentrations of PAEs (mg/kg) in agricultural soils with different land use.
Range Mean Range Mean Range Mean Range Mean Range Mean
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H. Lü et al. Environmental Research 164 (2018) 417–429
Jianghan Plain (Hubei Province), vegetable and orchard fields showed In different soil layers, the predominant PAE compounds varied to
higher PAE concentrations than rice and cotton fields (Liu et al., some degree. For example, DnOP showed the highest proportion
2010a). The variations in PAE distribution of different land use types (27.1–45%) in 0–10 cm soil layer, whereas DEHP had the highest pro-
might be caused by the industrial activities, the use of plastic film, portion at 20–40 cm layer of greenhouse in Shandong Peninsula (Chai
fertilizer and pesticides applied to increase crop yield (Kong et al., et al., 2014). Differently, DBP and di(2-n-butoxyethyl) phthalate ac-
2012; Wang et al., 2013b; Wu et al., 2015). Additionally, PAEs in soil counted for a large proportion of PAEs in all layers of agricultural soil
from vegetable production farms with plastic film greenhouse or with plastic film mulching in Shandong Peninsula; the concentrations of
mulching have received increasing concern, and about 20 papers have di(2-n-butoxyethyl) phthalate decreased with the soil depth, while
been published on this field (Ma et al., 2015; Wang et al., 2015; Li et al., those of DBP increased from layers 0–10–10–20 cm but decreased from
2016a, 2016b). The Σ6PAEs in soils with plastic film greenhouse or 10 to 20–20–40 cm (Li et al., 2016b). Tan et al. (2016) found that the
mulching were generally less than 10 mg/kg (Chen et al., 2013; Wang ratio of priority Σ6PAEs to Σ14 PAEs increased from 81.7 ± 7.7% to
et al., 2013, 2015), while the maximum Σ16PAEs was up to 18.8 mg/kg 90.1 ± 12.1% with soil depth, implying that the six priority PAE
in agricultural soil with plastic film mulching in Shandong Peninsula compounds were more mobile relative to the non-priority ones. Some
(2016b). Extremely high values of PAEs (11.2–1232 mg/kg) were ob- anthropogenic activities (e.g., tillage) may cause the concentrations of
served in cotton field in Xinjiang Province due to its long-term use of PAEs in subsurface soil (20–40 cm) to be similar to those in surface soil
plastic film for cotton planting (Guo and Wu, 2011). Importantly, in (Wang et al., 2013a). Soil physico-chemical properties could influence
intensively managed suburban vegetable farms of Nanjing, Σ6PAEs in sorption/desorption and leaching of contaminants in soils, hence in-
soils with plastic film were far higher than the control soils without fluence their vertical distribution (Vikelsøe et al., 2002). In soils with
plastic film (except the system comprised vegetables and flooded rice in visible clay in the upper layers, the maximum levels of DEHP occurred
rotation) (Wang et al., 2013). at a depth of 10–20 cm, whereas in most sandy soils no such maximum
was observed (Vikelsøe et al., 2002). Additionally, Tan et al. (2016)
2.4. Seasonal and vertical variation in soil PAE levels reported that Σ14PAEs and six priority PAE compounds in soil layers of
0–40 cm contributed 70.1 ± 4.3% and 68.3 ± 5.9% to those in the
Only three studies have reported the seasonal variation of PAEs in entire soil profile, respectively. Moreover, the largest percentages of
soils (Liu, 2010a; Niu, 2014; Zhang et al., 2015b). Zhang et al. (2015b) PAE storages were always observed either in coarse sand or coarse silt,
investigated PAE distributions in black soils of Northeast China during which showed higher bioavailability for uptake by maize and wheat
the process of agricultural production (comprising spring, summer and (Tan et al., 2016).
autumn), and found the highest levels of DBP, DEHP and ΣPAEs in Facing the severe soil pollution of China, the Ministry of
summer when mulching film was used in the greenhouses. Never- Environmental Protection of China emphasized the need to strengthen
theless, in JiangHan Plain (Hubei Province), PAE compositions in detailed investigations of soil pollution and its remediation. Thus, more
winter (January 2008) were more complicated than those in summer investigations on vertical distribution of PAEs in soil, especially in the
(July 2007), and the average Σ16PAEs of the former (1.08 mg/kg) was sites with high DBP, DEHP and ΣPAEs in surface soil, are necessary.
higher than the latter (0.64 mg/kg) (Liu et al., 2010a). Whereas no
obvious seasonal variation in PAE levels was observed in the soil irri- 3. Sources of PAEs in soils
gated with wastewater in Shijiazhuang city (Hebei Province) (Niu,
2014). The different seasonal distribution might be related to mulching 3.1. Urbanization and industrial activities
film, agricultural production activities, soil physico-chemical proper-
ties, and microbial degradation. In the study of Zhang et al. (2015b), PAEs are widely used in a very broad range of industrial application
mulching film was used in the investigated area. High temperature or products, including solvents in perfumes, adhesives, waxes, inks,
could reduce the bond strength of the plasticizer and PVC chain, thus pharmaceutical products, insecticide materials, cosmetics, plastic bags
resulting in an increased discharge of PAEs into the surrounding soil and film (Net et al., 2015a). Though many countries banned the use of
(Chen et al., 2011). Summer is the most vigorous season for plant certain phthalates such as DEHP and diisodecyl phthalate, these che-
cultivation in Northeast China, application of fertilizers is the mostly micals are still used in an un-controlled manner over other parts of the
required activity as compared to spring and winter seasons. Our pre- world, especially in developing and underdeveloped countries
vious study indicated that the widely used-fertilizers contained PAEs (Benjamin et al., 2015). To date, the global annual production of
(ranging from 0.01 to 2.8 mg/kg) (Mo et al., 2008). In JiangHan Plain, plastics has reached 150 million tonnes (about 300 million metric
no mulching film was used in the studied areas (Liu et al., 2010a), tonnes), and 6–8 million tonnes of PAEs are consumed annually (Net
which might lead to relatively low PAE concentrations, compared with et al., 2015a; Lönnstedt and Eklöv, 2016). Plastic bags and plastic film
those in Northeast China (Table 1). accounted for 47–51% of the total plastic content for some cities
In the literature, data are abundant on the horizontal distribution of (Simoneit et al., 2005). It was estimated that mismanaged plastic waste
PAEs in soil, but are scarce about vertical counterpart. Most studies in China was 8.82 million metric tonnes in 2010, being top-ranked one
investigated the occurrence of PAEs in surface soil (or topsoil, 0–5 or among 20 countries (Jambeck et al., 2015).
0–20 cm) (Cai et al., 2008a; Niu, 2014; Li et al., 2016a). Nevertheless, PAEs can be released to the environment at all stages of their life
PAEs distributed across the entire soil profile, and their concentrations cycle, from synthesis to transformation or degradation. Urbanization
decreased generally with soil depth (Wang et al., 2013a; Chai et al., and industrialization play important roles for the elevated PAE levels in
2014; He et al., 2015; Chen et al., 2015; Li et al., 2016b; Tan et al., the environment. Lan et al. (2012) reported that commercial activity
2016). Cheng et al. (2015) reported that the average concentrations of and dense populations could lead to the elevated PAE levels in soil. The
DBP, DEHP and Σ6PAEs in surface soil of Beijing were higher than those concentrations of PAEs in topsoil increase significantly along the rur-
in deep soil. In a wastewater-irrigated area in the North China Plain, the al–urban gradient (Zeng et al., 2008, 2009; Yang et al., 2013), reflecting
Σ14PAEs and concentrations of individual PAE congeners (including DBP the noticeable effects of urbanization and industrialization. Yang et al.
and DEHP) gradually decreased with increased soil depth (0–100 cm), (2013) also found that higher concentrations of PAEs were detected
due to sorption and migration of PAEs with continuous irrigation (Tan from roadside soil (and/or gutters) of densely anthropogenic activities
et al., 2016). In soils of Shijiazhuang city (Hebei Province), the con- areas. The ΣPAEs in urban topsoil of Beijing were higher in the areas
centrations of DMP, DBP and DOP decreased with the depth of soil with intensive human activities than in other areas, suggesting that the
(0–60 cm), while those of DEP increased initially with the depth of soil greatest contributor may be the higher usage daily of plastic products
(0–20 cm) and then decreased (Niu, 2014). (Zhang et al., 2014). High ∑6PAEs in soil were found at sites with lots of
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domestic garbage piled up near these locations (Kong et al., 2012). elevated PAE levels (Wu et al., 2015). The PAE levels in agricultural
Additionally, Σ6PAEs in the electronics manufacturing areas were sig- soils of Shandong Province which had the highest usage amount of
nificantly higher than those in non-industrialized areas (Wu et al., plastic film in China were higher than those of some other provinces
2015). Illegal dismantling activities of electronic waste (E-waste) also (e.g., Hebei, Guangdong) (Tables 1 and 4). Thus, soil contamination by
elevated the concentrations of PAEs in soil, resulting in 12.6–46.7 mg/ PAEs is an issue of concern due to the large amounts of plastic film
kg of Σ5PAEs in E-waste soils of Taizhou city (Liu et al., 2009). PAE used.
concentrations decreased along with the distance away from the dis- The PAE levels in agricultural soils were influenced by the mode,
posal center of E-waste (Zeng et al., 2008; Liu et al., 2009). In agri- colors, thickness, recovery, and age of plastic film applied (Wang et al.,
cultural soils from the peri-urban areas of Guangzhou, the highest 2013b; Chai et al., 2014). For instance, Σ6PAEs in the vegetable farm soil
Σ16PAEs (33.6 mg/kg) was found at a site immediately close to the cultivated for 8–12 years with double polytunnels and a single layer of
biggest market of architecture in South China, where a significant mulch film were higher than that cultivated for over 10 years with a
amount of the plastic materials used is discarded (Zeng et al., 2008). single layer of polytunnel and mulch film (Wang et al., 2013b). Wang
Therefore, the high concentrations of PAEs in soils were related to in- et al. (2013b) reported that PAE concentrations in plastic film of var-
tense industries, population density, and surrounding pollution sources. ious colors were significantly different, with ∑6PAEs of 119 ± 26.8 and
50.8 ± 18.1 mg/kg in white and black mulching film, respectively. A
3.2. Plastic film positive correlation was found between Σ16PAEs and the age of vegetable
greenhouses in Shandong Peninsula, East China (Chai et al., 2014),
In the past decades, mulching soil with plastic film or natural ma- implying that PAEs in soils may be related with the cumulative use of
terials is used worldwide, especially in arid and semiarid areas. Plastic film greenhouses for vegetable cultivation. PAE levels estimated in soils
film mulching or greenhouse has become a globally used agricultural without recycling were higher than those with recycling (Chen et al.,
practice for its rapid production and economic benefits such as higher 2013). Additionally, adverse effects and risks may arise from plastic
yields and improvement of crop quality (Chen et al., 2013; Steinmetz mulching with regard to PAE contamination, waste treatment, life cycle
et al., 2016). In China, the quantity of plastic film used in agriculture balance and impact on soil quality (Steinmetz et al., 2016). Thus, ef-
increased dramatically between 1990 and 2016, from 0.48 to 2.60 fective plastic film management and conducting comprehensive re-
million tonnes (Fig. 1) (Department of Rural Survey National Bureau of search with the aim of gaining an extensive understanding of the pro-
Statistics of China, 2017). Especially for the plastic mulching, its usage cesses governing PAE contamination of film mulching is needed.
amount increased from 0.47 to 1.47 million tonnes from 2000 to 2016,
and its covered area increased corresponding from 6.49 to 18.4 million 3.3. Application of fertilizer
ha (Department of Rural Survey National Bureau of Statistics of China,
2017), being far higher than the covered surface in Europe (4270 km2) Fertilizer is an essential material for agricultural production. China's
(Steinmetz et al., 2016). The usage amount and covered area of plastic consumption of synthetic fertilizers has been increasing every year
mulching are different in various provinces or regions (Table 4). In since the early 1960s, and is now the largest producer and consumer of
some provinces or regions, such as Hebei, Inner Mongolia, Shandong, synthetic fertilizer in the world (Sun et al., 2012). Chemical fertilizers
Henan, Sichuan, Yunnan, Gansu, Xinjiang provinces, their usage consumption in China in 2015 was up to 60.2 million tonnes, being
amounts and covered areas of plastic mulching exceeded 60,000 t and more than twice of that in 1990 (25.9 million tonnes) (Fig. 1) (De-
one million ha in 2016, even up to 2.2 and 3.4 million ha in Shandong partment of Rural Survey National Bureau of Statistics of China, 2017).
Province and Xinjiang Uygur Autonomous Region, respectively In some regions, the average usage rates (kg/ha/year) of fertilizers are
(Table 4) (Department of Rural Survey National Bureau of Statistics of about 270–600 of nitrogen and 107–160 of phosphorus as chemical
China, 2017). compound fertilizers, even over 1000 kg N/ha for vegetable farm soils
PAEs are the major components of plastic films. Finished plastic in some counties or districts (Sun et al., 2012; Kong et al., 2014). Fer-
products contain 10–60% PAEs (mass basis). With the extensive use of tilizer input intensity of China is the third highest in the world after
plastic mulching, substantial amounts of plastic residues accumulate in Korea and Japan (Sun et al., 2012).
soil each year, resulting in potential pollution (e.g., microplastics, PAEs, Our previous study showed that fertilizers contained PAE com-
agrochemicals). Following the bulletin of the first national census on pounds, with Σ6PAEs from 0.01 to 2.8 mg/kg (Mo et al., 2008). The
pollution sources in China, the average residual rate of plastic mulching application of such fertilizers could lead to deposition and hence ac-
was 19.7% (The Ministry of Environmental Protection, 2010). The re- cumulation of PAEs in soil (Cai et al., 2008a; Zhang et al., 2015b). For
sidual rate of plastic mulching was higher under non-recycling than example, Zorníková et al. (2011) found that the more fertilizer is ap-
recycling scenarios (Chen et al., 2013). According to empirical esti- plied, the higher the PAE accumulation in soil. In China, the fertilizer
mation by Chen et al. (2013), extremely high loads (more than 10 kg/ consumption varied from 0.60 million tonnes in Tibet to 7.16 million
ha/year) of PAEs in soil were estimated in Beijing, Tibet, Liaoning tonnes in Henan Province in 2015, in which six provinces: Hebei,
Province, Jilin Province, and Fujian Province, with high PAE levels Henan, Jiangsu, Anhui, Shandong, and Hubei provinces exceeded 3.0
(> 4.0 mg/kg) in agricultural soils found in these places under non- million tonnes (Table 4). High application rates of fertilizers might lead
recycling scenarios. to PAE accumulation in soil, especially for Guangdong Province, lo-
Agricultural plastic film has been considered to be one of the most cated in subtropical area. Its fertilizer consumption and usage amount
important sources of PAEs in soil (Wang et al., 2013b, 2015, 2016; Chai of plastic film were lower than those of many provinces (Table 4), but
et al., 2014; Sun et al., 2016). As PAEs are loosely incorporated in the higher PAE levels were observed in vegetable farm soil of Guangdong
polymer structure without covalent bonding, they can be released into (Cai et al., 2005, 2008a). It might be attributed to its higher fertilizer
soil by leaching, migration, and abrasion (Steinmetz et al., 2016). Soil application rate with high multiple cropping index. Lin and Xu (2013)
PAE levels were correlated with PAEs released from plastic film re- reported that the fertilizer application rate in Guangdong was at an
sidues (Wang et al., 2016), and as expected higher PAE levels were alarmingly high level of 852 kg/ha/year, being much higher than that
recorded in the soil with plastic film. For example, in the suburban in other regions of China and 3.8-fold of alert level of developed
vegetable farm soils in Nanjing, east China, Σ6PAEs in soils with plastic countries. Moreover, in many areas, fertilizer application amounts in-
film were higher by 79.3–610% than soils without plastic film (Wang creased with plant cultivation activities in summer as compared to
et al., 2013b). The higher concentrations of PAEs in farm soils com- spring and winter seasons, which caused relatively high soil PAE levels
pared to non-cultivated soils suggest that extensive use of PAE-con- in summer (Zhang et al., 2015b). Fortunately, the Chinese government
taining products (e.g., plastic films) in agriculture might result in the recognized the effects of fertilizer application on the environment and
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Table 4
Consumption of fertilizer, plastic film and covered area of plastic mulching of different provinces in 2015 and 2016, China*.
Provinces or cities Total fertilizer load (Million Total plastic film load (t/year) Total plastic mulching load (t/ Area of plastic mulching (Ha/year)
t/year) year)
Beijing City 0.11 0.10 10402 9867 2663 2605 14131 13440
Tianjin City 0.22 0.21 10552 11644 4493 3942 65468 53740
Hebei Province 3.36 3.32 137983 138434 65655 65123 1068550 1065312
Shanxi Province 1.20 1.17 47864 48922 32407 32641 588444 587904
Inner Mongolia Autonomous 2.29 2.34 95021 95631 69669 73527 1181606 1279544
Region
Liaoning Province 1.52 1.48 141942 137273 40582 38114 323675 324903
Jilin Province 2.31 2.34 59164 59565 26864 28423 175632 179668
Heilongjiang Province 2.55 2.52 83097 82575 33128 32536 323379 306686
Shanghai City 0.10 0.09 18030 17062 4728 4536 19590 18152
Jiangsu Province 3.20 3.12 113243 113941 45563 45481 609443 610513
Zhejiang Province 0.88 0.84 67458 67300 29037 29082 162417 157962
Anhui Province 3.39 3.27 97943 96966 43539 42728 436963 428897
Fujian Province 1.24 1.24 62067 62424 30750 31547 141643 139880
Jiangxi Province 1.44 1.42 53977 52757 32371 32724 131253 132260
Shandong Province 4.64 4.56 301575 297961 123397 121014 2171923 2091689
Henan Province 7.16 7.15 162001 163149 74406 76081 1032096 1019290
Hubei Province 3.34 3.28 71321 67306 40440 38018 407710 405930
Hunan Province 2.47 2.46 83989 84679 55860 56630 716791 726204
Guangdong Province 2.57 2.61 46795 45505 26046 26166 138426 134642
Guangxi Zhuang Autonomous 2.60 2.62 46276 48445 35207 36953 415443 566702
Region
Hainan Province 0.50 0.51 32433 26704 15481 15057 44213 46174
Chongqing City 0.98 0.96 45162 45265 23819 24520 244539 255292
Sichuan Province 2.50 2.49 132170 132384 91857 92191 1002048 1007757
Guizhou Province 1.04 1.04 49403 51053 29700 30758 307461 312434
Yunnan Province 2.32 2.36 113104 115926 90865 92302 1011227 1046414
Tibet 0.06 0.06 1866 1784 1117 1510 3522 5003
Shaanxi Province 2.32 2.33 43068 43717 22147 22313 454135 437530
Gansu Province 0.98 0.93 183735 195092 114295 126954 1394900 1372748
Qinghai Province 0.10 0.09 7377 7944 6006 6410 70860 72981
Ningxia Hui Autonomous Region 0.40 0.41 15642 15137 11265 11521 197337 196305
Xinjiang Uygur Autonomous 2.48 2.50 268901 266198 231471 228703 3463530 3405247
Region
* These data from China Rural Statistical Yearbook (Department of Rural Survey National Bureau of Statistics of China, 2017).
soil quality, and the Ministry of Agriculture of China issued an an- areas of China is deteriorated largely due to the non-point source pol-
nouncement entitled “zero-growth action plan of fertilizer consumption lution from the wastewater generated from rural and agricultural ac-
by 2020” in 2015 (Ministry of Agriculture, 2015). Furthermore, the tivities (Sun et al., 2012).
Ministry of Agriculture of China encouraged that chemical fertilizers To date, only a few studies have reported the occurrence of PAEs in
should be replaced by organic fertilizers in the future. Nevertheless, soils due to wastewater irrigation (Zeng et al., 2008; Zhang et al.,
manure also contained PAE compounds as well as residual antibiotics 2015a; Tan et al., 2016). The results in the literature show that was-
(Wang et al., 2013b; Zhang et al., 2015b). For instance, ∑6PAEs in tewater irrigation is indeed one of the main factors that raise soil PAE
chicken manure, pig manure, cow manure, duck manure, and com- levels. Zeng et al. (2008) reported that the highest ∑16PAEs (33.6 mg/kg)
mercial organic fertilizer were 6.84 ± 6.54, 4.57 ± 2.84, and DEHP (29.4 mg/kg) in agricultural soils of Guangzhou were found
3.65 ± 0.59, 2.24 ± 0.90, and 2.95 ± 3.62 mg/kg, respectively at the site (close to the biggest market of architecture in South China)
(Wang et al., 2013b). Thus, fertilizer and manure might be important where a ditch with sewage and industrial wastewater past through the
potential sources of PAEs in soil. Special attention should be paid to the middle of the sampling field. PAEs were frequently detected in water
effects of manure and fertilizer on soil quality. and agricultural soil of a typical wastewater irrigation area in Hebei
Province (Zhang et al., 2015a; Tan et al., 2016). Kong et al. (2012)
observed that DEHP and DBP concentrations were relatively higher in
3.4. Wastewater irrigation suburban agricultural soils with long-term wastewater irrigation in
Tianjin city. Interestingly, the levels of DBP and DEHP in the soil with
In some regions of China, including North China, northeast China wastewater irrigation in both Hebei Province and Tianjin city were
and West China, severe water shortage has led to the prevalence of comparable with those in Mexico (wastewater irrigation for 90 years)
wastewater irrigation practice in suburbs around industrial cities since (Durán-Alvarez et al., 2009; Tan et al., 2016). Importantly, following
1950s (Chen et al., 2014; Tan et al., 2016). Wastewater contains various the PAE levels reported in literature, those in the soil with wastewater
organic contaminants including PAEs (Gao et al., 2014; Zolfaghari irrigation in both Hebei Province (wastewater irrigation > 20 years,
et al., 2014; Tan et al., 2016). PAEs in wastewater cannot be removed soil ∑6PAEs < 1.0 mg/kg with a mean of 0.29 mg/kg) (Zhang et al.,
thoroughly by means of biodegradation and sorption during wastewater 2015a) and Tianjin city (wastewater irrigation and sludge applica-
treatment processes (i.e., activated sludge process, membrane bior- tion > 40 years, soil ∑6PAEs < 10.4 mg/kg with a median value of
eactor) (Zolfaghari et al., 2014). ∑6PAEs were at 23.3–88.5 and 0.32 mg/kg (Kong et al., 2012) were relatively lower than those in the
6.95–61.5 ng/mL in influent and effluent (Supplementary Table 1S), soil with plastic film mulching (Wang et al., 2013b). In the soil with
respectively, from wastewater treatment plants of Harbin, for example wastewater irrigation in Tianjin city, higher ∑6PAEs (2.79–10.4 mg/kg)
(Gao et al., 2014). On the other hand, the water quality in the rural
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H. Lü et al. Environmental Research 164 (2018) 417–429
were observed at the sites with lots of domestic garbage piled up near environment and public health.
these locations (Kong et al., 2012). Thus, plastic film residue may be the
main source of soil PAEs, and wastewater irrigation might be a minor 4. Uptake of PAEs by crops and human exposure
one. Nevertheless, in view of residual organic contaminants, it is sug-
gested that agricultural soils should only be irrigated with reclaimed 4.1. Uptake and accumulation of PAEs by crops
water or wastewater after advance treatment.
PAEs in soils can be taken up and accumulated by plants. Todate,
3.5. Land application of sewage sludge about twenty papers have reported on the uptake, accumulation and
translocation of PAEs by different plants, especially vegetables (Cai
Land application of sewage sludge has been an important and en- et al., 2008c, 2015; Mo et al., 2009; Lü et al., 2014; Sun et al., 2015; Ma
couraged disposal way in the world with many benefits such as nutri- et al., 2015; Zhao et al., 2015; Chen et al., 2017b), which pose a po-
tion and organic matter recycling (Lowman et al., 2013; Bondarczuk tential threat to human health. Our previous studies showed that DBP
et al., 2016). In the United States, about 60% of the produced sewage and DEHP could be taken up by roots of vegetable and rice (Oryza sativa
sludge has been applied to farmland as a soil amendment or fertilizer L.), and then translocated to stems and leaves (and grains) (Cai et al.,
(National Research Council, 2002; Lowman et al., 2013). In some 2008c, 2015, 2017; Zhao et al., 2015). Six USEPA priority PAE com-
countries of the European Union, land application of sewage sludge was pounds were frequently detected in vegetable samples from different
as high as 62% (Kalogo and Monteith, 2008). In China, total sludge farms (Mo et al., 2009; Ma et al., 2015; Wang et al., 2015). The Σ6PAEs in
production was up to 6.25 million tonnes (dry solids) with an average vegetables collected from the conventional farms of the Pearl River
annual growth of 13% from 2007 to 2013, and more than 80% were Delta, China ranged from 0.073 to 11.2 mg/kg (Mo et al., 2009), and its
disposed by improper dumping (Yang et al., 2015). Land application average Σ6PAEs (3.20 mg/kg) was relatively higher than those from the
accounted for only 2.4% of sewage sludge produced in China (Yang other regions, being in agreement with the trend of Σ6PAEs in soils of the
et al., 2015). Nevertheless, sewage sludge contains various pollutants whole country (Cai et al., 2008a; Niu et al., 2014). The concentrations
including heavy metals and organic contaminants (e.g., PAEs, PAHs, in vegetables from Pearl River Delta were comparable or even higher
polyfluoroalkyl substances, antibiotics, etc) (Cai et al., 2007; Ruan than those (from 0.51 to 7.16 mg/kg with an average value of 2.56 mg/
et al., 2015; Bondarczuk et al., 2016). Our previous study showed that kg) from plastic film greenhouses in Nanjing, East China (Ma et al.,
Σ6PAEs in sewage sludge generated from 11 wastewater treatment plants 2015; Wang et al., 2015).
of China ranged from 10 to 114 mg/kg (with a mean of 30 mg/kg) Nevertheless, very high DEHP concentrations were observed in ve-
(Supplementary Table 1S) (Cai et al., 2007), while Σ16PAEs in sewage getables from greenhouses with the PVC film (from
sludge from Shanghai varied from 22.6 to 1350 mg/kg (with a mean of 15.8 ± 0.9–34.0 ± 2.5 mg/kg) and with PVC–PE composite film
123 mg/kg) (Meng et al., 2014). The estimated annual mass loadings (from 11.2 ± 1.8–27.3 ± 0.7 mg/kg) (Fu and Du, 2011), or high
via sludge of DEHP, DBP, and Σ16PAEs were 1042, 247, and 1314 t in Σ5PAEs (2.49 ± 0.91–6.12 ± 0.58 mg/kg fresh weight) in vegetables
China, respectively (Meng et al., 2014). In some cases, the concentra- of greenhouses from 10 cities of China (Chen et al., 2017b) These high
tions of DEHP in sludge exceeded the limit (100 mg/kg) proposed by levels of PAEs in vegetables from greenhouses are influenced by
the Europe Union for land application (Cai et al., 2007; Meng et al., greenhouse age and height, plastic film types and thickness. The lower
2014). the height of the greenhouse, the younger the age of the greenhouse,
Many studies have demonstrated that land application of sewage the thicker the film will be, the higher DEHP concentrations of film will
sludge could increase the levels of PAEs and other organic contaminants be, resulting in higher DEHP concentrations in vegetables (Fu and Du,
in soil (Vikelsøe et al., 2002; Cai et al., 2008b; Rhind et al., 2013; Meng 2011). Although high concentrations of PAEs were found in both ve-
et al., 2014). Our previous study showed that the concentrations of getables and soil, no clear relationship was observed for PAE con-
PAEs in soil increased after amended with sludge or its compost com- centrations between vegetables and field soils (Wang et al., 2015; Chen
pared to the control (only chemical fertilizer applied) (Cai et al., et al., 2017b), except PAE concentrations in maize and wheat tissues
2008b). Vikelsøe et al. (2002) reported that the use of sludge as soil correlated well with the PAE storage in soils a wastewater-irrigated
amendment below a certain limit (4.3 t dw/ha/year) did not result in area in the North China Plain (Tan et al., 2016). The bioconcentration
elevated levels of PAEs in soils, whereas heavy application (17 t dw/ha/ factors (the ratio of PAE concentrations in plant roots to soil, or shoots
year) led to PAE accumulation. Rhind et al. (2013) also found that soil to soil) of DBP and DEHP were less than 1.0 in general (Cai et al.,
concentration of DEHP was elevated after application of sewage sludge 2008c, 2015; Mo et al., 2009; Zhao et al., 2015). High bioconcentration
to pastures. In agricultural soil of Guangzhou, high Σ16PAEs (12.2 mg/ factors (5.8–17.9) were observed in plants grown near an electronic
kg) was observed at one site where sewage sludge was applied, while waste recycling site in East China (Ma et al., 2013).
the lowest one was observed in the vegetable field irrigated by In addition, the uptake, translocation and accumulation of PAEs
groundwater, without application of plastic films and sewage sludge varied with plant species and cultivars, tissues, growth stages (Cai et al.,
(Zeng et al., 2008). 2008c; Sun et al., 2015; Lü et al., 2014; Zhao et al., 2015; Chen et al.,
Nevertheless, it should be pointed out that, till now, very few stu- 2017b). Our previous studies showed that the average concentrations of
dies have reported the occurrence of organic contaminants (e.g., PAEs, DEHP in maize cultivars were lower than those in forage species (e.g.,
PAHs, polybrominated diphenyl ethers) in field soils with land appli- alfalfa, ryegrass, and teosinte) (Li et al., 2014b). Wang et al. (2015)
cation of sewage sludge in China, especially long-term land application found that stem and leaf vegetables accumulated more PAEs than root
(Li et al., 2015; Li and Ma, 2016), while most studies on soil con- vegetables, while Sun et al. (2015) demonstrated that uptake of both
tamination by sewage sludge have been conducted in pot and pilot DBP and DEHP decreased overall in the order of carrot >
trials (Cai et al., 2008b; Waqas et al., 2014). On the other hand, the strawberry > lettuce (P < 0.05). Moreover, genotypic variation was
estimated DEHP and DBP concentrations in soil (19.5 and 4.5 mg/kg, observed in the uptake, accumulation, and translocation of DBP and
respectively) with land application of sewage sludge by model (Meng DEHP by different cultivars of rice (Oryza sativa L.) (Cai et al., 2015,
et al., 2014) were considerable high, but they might be overestimated 2017) and Chinese flowering cabbage (Brassica parachinensis L.) (Zhao
because the loss of PAEs in sludge amended-soil via leaching, volatili- et al., 2015). Our studies also identified some cultivars of rice, Chinese
zation, and degradation was not considered. Therefore, systematic in- flowering cabbage, and Ipomoea aquatica with a low accumulation of
vestigation on the occurrence of PAE and other contaminants in the soil DBP and DEHP (Cai et al., 2008c, 2015; Zhao et al., 2015). These
with land application of sewage sludge (especially long-term applica- cultivars would be suitable for planting in low- to mid-level PAE-con-
tion) in China is necessary in view of their adverse effects on the taminated soils, resulting in lower PAE exposure through ingestion of
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H. Lü et al. Environmental Research 164 (2018) 417–429
these vegetables and grains. reduce the release of PAEs and result in a decreased contamination of
the soil. Moreover, research on release and transportation of PAEs from
4.2. Human exposure to PAEs plastics and fertilizer, as well as the contribution of wastewater irri-
gation and land application of sewage sludge to the PAE levels will be
As mentioned above, six PAE compounds are listed as priority pol- helpful to understand their polluting process of soil.
lutants by the US EPA, the Chinese National Environmental Monitoring Soil PAEs could be taken up and accumulated by plants. Though
Center, and other regulatory bodies. PAEs in soil can pose potential human exposure to PAEs via ingestion of soil and vegetables were re-
risks to the environment and human health, and most studies have latively low, high public concern of human exposure to PAEs remains.
focused on the exposure risks of relevant to human health (Niu et al., Moreover, Sui et al. (2014) reported that dietary intake of cereals in
2014; Wang et al., 2017, 2018). Human exposure to PAEs could be China contributed to the primary food sources of DEHP (44.6% for
through diet (the intake of food) and other non-dietary (soil ingestion, adults and 39.4% for children). Unfortunately, very few data are
dermal contact and inhalation) routes (Ma et al., 2015; Niu et al., 2014; available on the uptake of PAEs by cereal crops (Lu et al., 2017),
Wang et al., 2015). Some studies have assessed the risks of human especially about the occurrence of PAEs in cereal crops grown in the
health exposure to PAEs, and assumed that soil ingestion and daily field. Thus, further investigation is needed on the occurrence of PAEs in
vegetable consumption were the major intake sources of PAEs (Xia cereal crops and vegetables under field conditions. Furthermore, sui-
et al., 2011; Niu et al., 2014; Cheng et al., 2015; Wang et al., 2015, table and low-cost remediation methods for the large-scale soil con-
2018). Different methods and models were used to assess the non- taminated by PAEs are necessary to be developed.
cancer and carcinogenic risks of PAEs for farmers and children. Niu
et al. (2014) and Wang et al. (2015) calculated the average daily doses Acknowledgments
via dietary (only considering vegetables grown in soils) and non-dietary
routes, and found that the hazard indexes (or hazard quotient; defined This work was funded by the National Natural Science Foundation
as the ratio of average daily intake dose to the reference dose) of PAEs of China (Nos. 41573087, 41471265, and 41773108), the NSFC-
were below 1.0 for both children and adults, and the carcinogenic risk Guangdong Joint Fund (U1501233), the Research Team Project of the
levels were all less than 10−4. Similarly, the total cancer risk values of Natural Science Foundation of Guangdong Province
PAEs (especially BBP and DEHP) in urban soil of both Beijing and Xi’an (2016A030312009), the Program of the Guangdong Science and
were lower than the acceptable cancer risk value (10−6) and that the Technology Department (2016B020242005, 2015B020235008,
risk mainly came from dermal uptake and inhalation (Xia et al., 2011; 2015A030313418), and the Earmarked Fund of Integrate Microbiology
Wang et al., 2018). Cheng et al. (2015) assessed the eco-toxicological Research Center (IM20170105).
effect (following environmental risk limits) of PAEs in soil and found
that no environmental risk would occur in suburban surface and deep Conflict of interest
soil of Beijing.
Nevertheless, high concentrations of PAEs (especially for DBP and The authors declare that they have no conflict of interest.
DEHP) were found in soils and vegetables in some regions (e.g., Pearl
River Delta, and vegetables from plastic film greenhouses) (Cai et al., Appendix A. Supporting information
2005, 2008a; Mo et al., 2009; Fu and Du, 2011), in which no risk as-
sessments have been done. On the other hand, dietary exposure to Supplementary data associated with this article can be found in the
DEHP for general Chinese population estimated, in some cases, was online version at http://dx.doi.org/10.1016/j.envres.2018.03.013.
higher than the reference dose (20 μg/kg-bw-day) proposed by the
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