3.1 Occurrence and concentrations of PAEs in protected agriculture soil
In the present investigation, DEHP, DBP, DOP, and BBP were detected in all soil samples, while DMP and DEP were negligible. Table S3 shows that ∑6PAEs concentrations ranged from 350.11 µg/kg to 767.10 µg/kg, with a mean value of 497.64 µg/kg. Additionally, DEHP was a predominant PAE, with concentration ranging from 199.82 µg/kg to 564.04 µg/kg, and a mean value of 318.68 µg/kg, markedly higher than those of the other PAEs (Figure 1(a,b)). DBP concentrations were the second-highest among the homologs, with concentrations ranging from 110.47 µg/kg to 166.31 µg/kg, and a mean value of 137.56 µg/kg. The DOP and BBP concentration were comparable in the present study, with an average value of 20.12 µg/kg and 21.29 µg/kg, respectively. Compared with the soil from other regions in China, ∑6PAEs in this study was slightly higher than that in agricultural soils from Zhongshan but significantly lower than that in vegetable soil from Beijing (Table 2). In addition, previous studies have shown that PAEs were detected in agricultural soils from other countries, such as Denmark and the Netherlands (Table 2). These results indicated that PAEs contamination varied spatially in agricultural soil within China, reflected by regional differences in concentration. Niu et al. (2014) found that PAEs contamination was relatively high in soils from densely populated and economically developed areas, suggesting that economic development, population density, soil utilization type, and agricultural film usage would affect PAEs concentrations in soil.
Table 2
Pollution levels of PEAs in soils of different region
Region | Sample type | PAEs concentration mg/kg | Major Contaminants | Reference |
Denmark | Agricultural soil | 0.039-3.268 | DEHP、DnBP | (Jørgen Vikelsøe, 2002) |
Netherlands | Agricultural soil | 0.0324 | DEHP | (Willie J.G.M. Peijnenburg, 2006) |
Serbia | Soil and street dust | 0.0004-2.04 | DEHP | (Skrbic et al., 2016) |
The United Kingdom | Agricultural soil | 0.113-0.171 | | (Gibson et al., 2005) |
India | Soil of electronic waste recycling workshops | 0.396 | DEHP | (Chakraborty et al., 2019) |
China | Farmland soil | 0.075-6.369 | DEHP | (Wang et al., 2013) |
Nanjing, China | Vegetable greenhouse soil | 0.15-9.68 | DnBP、DEHP、DnOP |
Beijing, China | Vegetable greenhouse soil | 0.14-2.13 | DEHP、DnBP | (Li et al., 2016a) |
Zhongshan, China | Agriculture soil | 0.14-1.14 | DnHP、DEHP | (Li et al., 2015) |
Northeast China | Facility agriculture soil(black soil) | 1.37-4.90 | DEHP、DnBP、DEP | (Zhang et al., 2015) |
Hainan, China | Facility agriculture soil | 0.046-0.614 | DEHP、DIBP | (Huan et al., 2021) |
Ningxia, China | Soil | 0.0843-8.728 | DEHP、DnBP、DIBP | (Zhang et al., 2020) |
Tianjin, China | Suburban Agricultural Soils | 0.05-10.4 | DEHP、DnBP | (Kong et al., 2012) |
Chongqing, China | Urban soil | 0.0931-0.312 | DEHP、DBP、DIBP | (Yang et al., 2018) |
Shandong Peninsula, northern of China. | Protected agriculture soil | 0.350-0.767 | DEHP | This study |
However, the actual degree of soil contamination cannot be entirely dependent on the total concentration of PAEs, and the concentration of phthalate monomer compounds should be considered. The relative contribution of each PAEs was studied in this work, and the results showed that DEHP had the highest proportion, accounting for more than 54% of the ∑PAEs concentration, followed (in decreasing order) by DBP > DOP > BBP. The latter three homologs collectively accounted for 46% the ∑PAEs concentration. These results suggested DEHP contamination in the protected agricultural soil may be more serious than that of the other PAEs measured in this study, consistent with measurements in various environmental matrices (Kong et al., 2013; Wang et al., 2013). Similar to protected agricultural soil, DEHP and DBP were also the most important PAE contaminations of in urban soils affected by intensive human activities (Yang et al., 2018; Zhao et al., 2018). PAEs are widely used synthetic additives that include many homologs with different properties, owing to their different alkyl chain lengths. DEHP and DOP, having long alkyl chains, are usually used as plasticizers in plastic products (Benjamin, S., et al.,2015). In contrast, PAEs with short alkyl side chains (DMP and DEP) are mostly used as solvents for fertilizers and pesticides (Gao et al., 2014). Therefore, different PAE-containing products may affect the PAE homologs profiles in agricultural soils (Sun et al., 2016). More importantly, DEHP and DBP have higher molecular weights and octanol-water partition coefficients than DMP and DEP, reducing their mobility, enhancing their persistence, and rendering them resistant to degradation in soils (Li et al., 2012).
3.2 Relationship between SOM, pH, and PAEs
As shown in Figure 2, DEHP was the most abundant PAE, and correlation analysis showed that there was a significant positive correlation between DEHP and the ∑PAEs concentration. In addition, soil pH and organic matter (Table 3) had opposite effects on PAEs. Soil pH was negatively correlated with the ∑PAEs concentration and four homologs, whereas SOM was positively correlated with PAEs (Figure 2). Some studies have reported that soil pH and organic matter were the main factors affecting the chemical behavior of organic contaminants in soil (Li et al., 2016; Zheng et al., 2016). Soil pH affects the adsorption behavior of hydrophobic organic pollutants in soil (Venkata Mohan et al., 2007). For instance, the adsorption of relatively polar PAEs in the soil increased with a decreasing pH, but as the pH increased, the ionization degree of soil organic matter increased and the soil's affinity for hydrophobic organics, such as phthalates, decreased, resulting in the desorption of adsorbed organic contaminants (Yang et al., 2013; Zheng et al., 2016). Furthermore, PAEs have low water solubility but can easily to dissolve in organic solvents, such as acetone and n-hexane. Studies have shown that the presence of SOM affects the solubilization of PAEs (e.g., surface sites of humic acid bind PAEs), and the increase of organic matter content may increase the number of adsorption sites, enhancing PAE adsorption (Cousins. and Mackay., 2000; Cui et al., 2010). The relationship between PAEs, soil pH, and organic matter was also investigated in previous studies (Li et al., 2016; Zheng et al., 2016). However, various biological and non-biological environmental factors in terrestrial soil ecosystems may affect the behavior of PAEs in soil. The use and inadequate cleaning of agricultural films and atmospheric deposition could affect the concentration of PAEs in soil (Wang et al., 2013). In addition, the application of pesticides and fertilizer impact soil properties, indirectly affecting the migration, transformation, and biodegradation. In summary, soil pH and organic matter may be the key mechanisms affecting the content of phthalates. Further study is warranted to improve understanding of the environmental fates of PAEs in the soil environment.
Table 3
Physical and chemical properties of collected soil samples
| pH | Soil organic matter (g/kg) | Alkali hydrolysable nitrogen (mg/kg) | Available phosphorus (mg/kg) | Available potassium (mg/kg) | Moisture content (%) | Soil texture (%) | Total nitrogen (g/kg) | Total salt content (g/kg) | Cultivation Ages |
Min | 5.54 | 14.76 | 35.00 | 166.46 | 189.21 | 11.52 | 5.67 | 1.29 | 1.42 | 7.00 |
Max | 7.33 | 34.74 | 274.40 | 468.64 | 589.44 | 21.56 | 10.48 | 2.29 | 5.32 | 25.00 |
Mean | 6.40 | 25.69 | 139.77 | 268.28 | 411.13 | 15.40 | 7.75 | 1.79 | 3.10 | 17.00 |
SD | 0.56 | 6.33 | 80.04 | 91.78 | 124.10 | 2.87 | 1.73 | 0.33 | 1.21 | 5.43 |
3.3 Risk assessment of PAEs exposure to human health
It is well known that terrestrial ecosystems become the depository of heavy metals and deleterious organic matter from human activities. Various contaminants are incorporated into the soil and promote detrimental effects on soil organisms (e.g., earthworms and vegetables) and humans through skin contact and oral inhalation. As the example, recent studies have shown that the concentration of PAEs in agricultural soils in some areas of China was relatively high and significantly exceeded the allowable concentrations recommended (Table 2, S4), and PAEs in agricultural soil with film was significantly higher than that in open-air soil, which also indicated that there was a higher environmental risk in protected agriculture (Wang et al., 2021).
In this study, we assessed the environmental risks of six priority phthalate substances, and the results showed that DMP and DEP were not observed in any of the soil samples, indicating that the concentration of these congeners did not exceed the allowable concentration standards, which meant that they presented low environmental risk to human health. For the other homologues, the highest concentrations were 564.04 µg/kg (DEHP), 166.31 µg/kg (DBP), 27.20 µg/kg (DOP), and 22.16 µg/kg (BBP), respectively. It was also observed that DEHP, DOP, and BBP in soil did not exceed the allowable concentration standard value, while DBP concentrations ranged from 110.47 µg/kg to 166.31 µg/kg, significantly exceeding the allowable concentration standard value of 81 µg/kg in all samples (i.e., exceedance rate of 100%), which was similar to results of Shouguang (Zheng et al., 2016) and Shenyang (Li et al., 2017), but higher than those of Zhongshan (93.85%)(Li et al., 2015) and Shantou (6.30%) (Wu et al., 2015). However, it should be noted that the concentration of DBP was far lower than the “cleanup objective” value and environmental risk limits (ERLs) that were derived using data on ecotoxicology and environmental chemistry (van Wezel et al., 2000).
Farming activities in protected agriculture (e.g., sowing, fertilization, harvest, etc.) may increase the probability of human exposure to PAEs pollutants. In addition, these contaminants may pose potential long-term exposure health risks to humans through multiple pathways. Since there were not issued relevant standards for PAEs pollutants in agricultural soil in China, in this study, we calculated the carcinogenic and non-carcinogenic risks of different PAE homologs in protected agricultural soil for different populations of people (adults and children) according to a risk assessment method recommended by the US EPA. Results showed that dermal contact was the major exposure pathway for adults and children to ingest PAEs, accounting for more than 75% of the total intake, followed by soil ingestion, accounting for 20.01-24.61% of the total intake. While studies indicated that PAEs were also present in the air (Ma et al., 2020), the proportion of PAEs inhaled in this study was low, accounting for only 0.02-0.14% (Table 4). It is worth considering about that although adults were mainly involved in agricultural production, children's intake of PAEs was significantly higher than that of adults, suggesting that children may be more likely to ingest contaminants from the soil environment. In addition, Figure 3 shows the non-carcinogenic and carcinogenic risks of PAEs form protected agriculture to adults and children. The results indicated that the hazard quotient values of the four PAE monomers were all less than 1, suggesting that their non-carcinogenic risk was relatively low. Furthermore, the hazard quotients of DEHP and DBP were higher than those of DOP and BBP, implying that these two pollutants have relatively higher health risks. Among the four PAE homologs, DEHP and DBP were considered potentially carcinogenic (Ji et al., 2014). In the present study, the carcinogenic risk of DEHP and DBP estimated was very low because their carcinogenic risk scores were lower than 10−6 (Figure 3). These results indicated that PAEs in protected agricultural soil posed an insignificant health risk to humans as they did not exceed the acceptable level. However, children exhibited a higher non-carcinogenic risk and carcinogenic risk than adults, illustrating that the toxic properties of PAEs may be more deleterious in children than in adults, possibly because detoxification and metabolism functions are weaker for children than those of adults.
Table 4
The average daily dose for adults and children via non-dietary
| Congener | Human | ADDingest | ADDdermal | ADDinhale |
Min | Max | Mean | Min | Max | Mean | Min | Max | Mean |
Non-carcinogenic intake | DEHP | adults | 2.74×10−7 | 7.73×10−7 | 4.37×10−7 | 1.09×10−6 | 3.08×10−6 | 1.74×10−6 | 1.90×10−9 | 5.37×10−9 | 3.03×10−9 |
children | 2.34×10−6 | 6.59×10−6 | 3.73×10−6 | 7.15×10−6 | 2.02×10−5 | 1.14×10−5 | 1.90×10−9 | 5.37×10−9 | 3.03×10−9 |
DBP | adults | 1.51×10−7 | 2.28×10−7 | 1.88×10−7 | 6.04×10−7 | 9.09×10−7 | 7.52×10−7 | 1.05×10−9 | 1.58×10−9 | 1.31×10−9 |
children | 1.29×10−6 | 1.94×10−6 | 1.61×10−6 | 3.95×10−6 | 5.95×10−6 | 4.92×10−6 | 1.05×10−9 | 1.58×10−9 | 1.31×10−9 |
DOP | adults | 2.76×10−8 | 3.73×10−8 | 2.92×10−8 | 1.10×10−7 | 1.49×10−7 | 1.16×10−7 | 1.92×10−10 | 2.59×10−10 | 2.03×10−10 |
children | 2.36×10−7 | 3.18×10−7 | 2.49×10−7 | 7.22×10−7 | 9.74×10−7 | 7.62×10−7 | 1.92×10−10 | 2.59×10−10 | 2.03×10−10 |
BBP | adults | 2.66×10−8 | 3.04×10−8 | 2.76×10−8 | 1.06×10−7 | 1.21×10−7 | 1.10×10−7 | 1.85×10−10 | 2.11×10−10 | 1.91×10−10 |
children | 2.27×10−7 | 2.59×10−7 | 2.35×10−7 | 6.94×10−7 | 7.93×10−7 | 7.20×10−7 | 1.85×10−10 | 2.11×10−10 | 1.91×10−10 |
Carcinogenic intake | DEHP | adults | 9.38×10−8 | 2.65×10−7 | 1.50×10−7 | 3.74×10−7 | 1.06×10−6 | 5.97×10−7 | 6.52×10−10 | 1.84×10-9 | 1.04×10-9 |
children | 2.19×10−7 | 6.18×10−7 | 3.49×10−7 | 6.13×10−7 | 1.73×10−6 | 9.78×10−7 | 1.63×10−10 | 4.60×10−10 | 2.60×10−10 |
BBP | adults | 9.11×10−9 | 1.04×10−8 | 9.45×10−9 | 3.63×10−8 | 4.15×10−8 | 3.77×10−8 | 6.33×10−11 | 7.23×10−11 | 6.57×10−11 |
children | 1.94×10−8 | 2.22×10−8 | 2.02×10−8 | 5.95×10−8 | 6.80×10−8 | 6.17×10−8 | 1.58×10−11 | 1.81×10−11 | 1.64×10−11 |
PAEs are typical environmental endocrine-disrupting substances. Studies have reported that the levels of T3 and T4 in adult blood are negatively correlated with PAE metabolites in urine (Park et al., 2017), and positive correlation between urinary PAE levels and overweight/obesity found in children (Xia et al., 2018). Thus, these studies indicated that human health could be threatened by PAE exposure, possibly for extended time. In this study, the risk assessment may be slightly underestimated because the health risks of PAEs under dietary routes were not considered. The ecological and health assessment of PAEs through the food chain requires further attention. Furthermore, studies on PAE toxicity to mammals are primarily focused on rats or mice (Ha et al., 2016), and more experimental date on PAE toxicity (and their metabolites) to other animals after long-term exposure are needed to fully understand the health risks and mechanisms of PAEs.