Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota

Science of the Total Environment xxx (xxxx) xxx

Contents lists available at ScienceDirect

Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota Huili Du a,b, Naiyi Yin a,b, Xiaolin Cai a,b, Pengfei Wang a,b, Yan Li a,b, Yaqi Fu a,b, Mst. Sharmin Sultana a,b, Guoxin Sun b, Yanshan Cui a,b,⇑ a b

College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 101408, People’s Republic of China Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China

h i g h l i g h t s

g r a p h i c a l a b s t r a c t


Pb bioaccessibility in most soils was

lower than 60%.
Mean of Pb bioaccessibility was

different in the acidic and alkaline soils.
The Pb bioaccessibility of farming soils was higher in the colon phase.
No significant change in Pb bioaccessibility of mining soils by human gut microbiota.

a r t i c l e

i n f o

Article history: Received 4 September 2019 Received in revised form 21 October 2019 Accepted 25 October 2019 Available online xxxx Editor: Xinbin Feng Keywords: Pb bioaccessibility PBET method SHIME method Soil properties Types Human gut microbiota

a b s t r a c t To better understand the risk assessment of Lead (Pb) in contaminated soils, 78 soil samples were collected from different locations in China and Pb bioaccessibility was assessed using the PBET (The Physiologically Based Extraction Test) method combined with SHIME (The Simulator of the Human Intestinal Microbial Ecosystem), and Pb bioaccessibility data from the PBET method on 88 soil samples that found in the literature were also used for the assessment. For all the soils, the mean Pb bioaccessibility was as follows: the gastric phase (31.25%) > colon phase (17.78%) > small intestinal phase (10.13%). The values of Pb bioaccessibility in most soils were lower than 60%, which is the typical default assumption for Pb (RBA, relatively bioavailability) by the US EPA. Mean Pb bioaccessibility (41.10% and 14.00% for gastric and small intestinal phases, respectively) in the present study was slightly higher than the values from the literature (24.80% and 8.68% for gastric and small intestinal phases, respectively) in the gastrointestinal tract. Mean Pb bioaccessibility was lower in acidic soil during the small intestinal phase, while the values for the alkaline soil were higher in the small intestinal and colon phases. In the gastric and small intestinal phases, mean Pb bioaccessibility in farming soils was slightly lower than it was in mining soils. However, the mean Pb bioaccessibility from farming soils was increased compared with mining soils in the colon phase given the action of human gut microbiota. Soil pH and type are important factors for predicting soil Pb bioaccessibility and health risk. Ó 2019 Elsevier B.V. All rights reserved.

1. Introduction ⇑ Corresponding Author at: College of Resources and Environment, University of Chinese Academy of Sciences, 380 Huaibeizhuang, Huairou District, Beijing 101408, China. E-mail address: [email protected] (Y. Cui).

Lead (Pb) is a very toxic element that is harmful for the environment, especially for soil environment (Li et al., 2014a; Yang et al., 2018). Human exposure to Pb in soils is a worldwide environmen-

https://doi.org/10.1016/j.scitotenv.2019.135227 0048-9697/Ó 2019 Elsevier B.V. All rights reserved.

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

2

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

tal problem because of its harm to human health, especially for children and infants (Hong et al., 2016). Soil ingestion is an essential Pb exposure pathway, particularly incidental ingestion (handto-mouth) of Pb-contaminated dust or soil (Li et al., 2015a; Mukerjee, 1998). Generally, the risk assessment of soil Pb is based on total concentration. However, only the Pb fraction that is dissolved in the gastrointestinal tract, and is absorbed into the systemic circulation may be harmful to human health, so this Pb fraction is defined as bioavailability. An in vivo method is often used to assess the bioavailability of soil Pb, however, the method also has some disadvantages, such as its time-consuming, expensive and some ethical problems. Assessment of Pb bioaccessibility using an in vitro method has been proposed to determine the Pb fraction that is soluble in the gastrointestinal tract and is available for absorption. To better understand bioavailability and bioaccessibility, many in vitro methods have been proposed to establish better correlation with animal models (Dong et al., 2016; Juhasz et al., 2009; Li et al., 2014b; Li et al., 2015b; Wragg et al., 2011). The physiologically based extraction test (PBET) method has been established for validation by Ruby et al. (1996) using an animal model to predict the Pb bioavailability, the method was modified in several different procedures, including different pH values for the gastric phase (1.5–2.5), different durations for the small intestinal phase (1– 4 h) and different mixing modes (shaking, argon gas) (Hettiarachchi and Pierzynski, 2002; Karadas and Kara, 2011; Ruby et al., 1996). The simulator of the human intestinal microbial ecosystem (SHIME) model is a dynamic in vitro method to investigate the bioaccessibility and metabolic potency of the human gut microbiome toward different elements (e.g., As, Cr) in the colon phase (Sun et al., 2012; Van de Wiele et al., 2010; Wang et al., 2019; Yin et al., 2015). Yin et al. (2015) have used the PBET combination with SHIME to determine soil As metabolism by human gut microbiota, the result showed that human gut microbiota increased As bioaccessibility, and adsorbed As(III) onto the soil solid phase. Wang et al. (2019) found that human gut microbiota increased the chromium (Cr) bioaccessibility and reduced more toxic Cr(VI) to less toxic Cr(III) from vegetables using SHIME model. Yet little research has explored Pb bioaccessibility using SHIME model. In addition, the US EPA also issued several guidelines describing in vitro methods to predict Pb relative bioavailability via the accidental soil ingestion pathway and suggested that 60% as the threshold of Pb bioavailability with human exposure and risk assessment (U.S. Environmental Protection Agency, 2007). However, Pb bioaccessibility in contaminated soils may be wideranging depending on its physicochemical properties (Finzgar et al., 2007; Jin et al., 2015). And the type of Pb in the soils is crucial to determining the bioaccessibility of Pb (Yan et al., 2019; Yan et al., 2017). To make better use of soil properties to predict the bioaccessibility of Pb, many researchers try to find the relationship between soil properties and Pb bioaccessibility (Finzgar et al., 2007; Jin et al., 2015). Using Pb spiked soils, researchers revealed that soil pH and clay content are significantly correlated with Pb bioaccessibility (Wijayawardena et al., 2015; Zheng et al., 2013). However, laboratory-spiked soils do not fully reflect the dissolution behaviour of real soils from different types. Many researchers have explored the relationship between soil properties and bioaccessibility with natural Pb contaminated soils. In some studies, a significant correlation between Pb bioaccessibility and soil properties such as pH, the content of total Pb, clay content and organic matter (OM) was found (Appleton et al., 2012; Caboche et al., 2010; Karadas and Kara, 2011; Poggio et al., 2009). Using an IVG (in vitro gastrointestinal test) method to assess the 25 soil samples from China, Pb bioaccessibility was positively correlated with total Pb concentration (R = 0.817, p < 0.01) and OM (R = 0.438, p < 0.05), in the gastric phase. Moreover, bioaccessibile Pb concentrations

also correlated with soil total Fe (R = 0.436, p < 0.05) and Mn (R = 0.590, p < 0.01) concentrations because Pb that is bound to Fe or Mn oxides are more potentially soluble (Lu et al., 2011). Poggio et al. (2009) showed Pb bioaccessibility is negatively correlated with OM and clay content in the gastric phase, but positively correlated with total Pb concentration; while, Pb bioaccessibility is positively correlated with pH, OM, sand and total Pb concentration in the small intestinal phase. Meanwhile, many researchers have explored soil Pb bioaccessibility from different types (Attanayake et al., 2017; Cai et al., 2017; De Miguel et al., 2012; Sanderson et al., 2012). However, no significant relationship was found between soil properties and Pb bioaccessibility when Pb contaminated soils are considered as one type (Yan et al., 2017). Poggio et al. (2009) concluded that there is no difference in Pb bioaccessibility based on types between farming and residential soils. Lu et al. (2011) showed no obvious difference in Pb bioaccessibility in central urban regions based on different types. The research on quantifying the relationship between Pb bioaccessibility with soil properties and various types of Pb in soils is limited. If we can determine a better demarcation for the range of Pb bioaccessibility based on a division of soil properties or types, more optimization models will be established to simplify bioaccessibility calculation. In the present study, 78 soil samples were collected from 27 provinces and autonomous regions in China that are impacted by different soil types of Pb. Then Pb bioaccessibility was studied using the PBET combined with SHIME method, and Pb bioaccessibility data from the PBET method on 88 soil samples were collected from the published literature, and these soil samples were all collected from Pb-contaminated soils (Table S1). All of these data were used to (1) illustrate the Pb bioaccessibility range in contaminated soils with different types and soil properties; (2) identify key factors influencing Pb bioaccessibility, and develop a simple model to predict the Pb bioaccessibility based on soil properties; (3) assess the effect of human gut microbiota on the bioaccessibility of Pb in soils. 2. Materials and methods 2.1. Lead-contaminated soils In this study, 78 soil samples were collected from a range of contaminated sites in different locations in China. All of soil samples were air-dried, sieved to 1 mm and 100 lm particle size fractions to assess physicochemical properties and sieved to a 250 lm particle size fraction for in vitro studies since this particle size is most easily to adhere to the hands of people who have been exposed to Pb soils (Kelly et al., 2002). Soil physicochemical properties and the total Pb concentrations were determined according to the method described in Yin et al. (2015) and summarized in Table 1. Moreover, the Pb bioaccessibility and soil property data of 88 soil samples were sorted from published data on Pb bioaccessibility in natural soils (not including urban and spiked soil) using the PBET method, and all the information is summarized in Table S1. Finally, all soils were classified into two groups based on type: farming soils and mining soils. Soils from farmland, grassland, deserts and gardens that unaffected by mines were defined as farming soils, and soils from mines, smelters and other sites related to mines were defined as mining soils. 2.2. Dynamic SHIME The colon microbial community that used in the in vitro experiments was cultured and maintained in a modified SHIME model that was described in Van de Wiele et al. (2004). The SHIME model

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

3

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx Table 1 Physicochemical properties of the collected soils. Type Present study

All (N = 78)

Farming soils (N = 46)

Mining soils (N = 32)

Literature

All (N = 88)

Farming soils (N = 41)

Mining soils (N = 47)

Mean Median Max Min Mean Median Max Min Mean Median Max Min Mean Median Max Min Mean Median Max Min Mean Median Max Min

consisted of five compartments which simulate the stomach, small intestine, ascending colon, transverse colon and descending colon respectively. The SHIME model has been described in detail by Yin et al. (2015). Briefly, the microorganisms obtained from an adult male volunteer with no antibiotic were used in six-months before the study, were inoculated into three colon compartments. The addition of feed solution, temperature (37 °C) and pH (5.6–5.9, 6.15–6.4, and 6.7–6.9) of the ascending colon, transverse colon and descending colon were automatically controlled respectively. The SHIME model solution were stirred by the magnetic stirrer continuously and flushed regularly with nitrogen to maintain anaerobic conditions. After 3–4 weeks of cultivation, the microbial communities in respective colon compartments inclined to be stable. The community composition and microbial fermentation activity of distal colon were investigated to ensure the consistency with operating parameters of previous SHIME model (Yin et al., 2015).

2.3. Estimation of Pb bioaccessibility In this study, the Pb bioaccessibility of 78 soil samples was investigated in the gastric, small intestinal and colon phases using PBET (Ruby et al., 1996) combined with SHIME. In brief, in the gastric phase, soils (0.3 g) and gastric digests (30 mL, 1L gastric digests including 0.15 M NaCl, 0.5 g citrate, 0.5 g malate, 0.42 mL lactic acid, 0.5 mL acetic acid and 1.25 g pepsin, then samples were adjusted to pH 1.5 with 12 M HCl) at specific soil/solution (s/s) ratios (1:100) were added to 50 mL polypropylene centrifuge tubes. Then, samples were shaken at 150 rpm and incubated at 37 °C for 1 h. After the gastric phase, the NaHCO3 powder were added into the digests to make the solution pH 7.0. Bile salts (1.75 g/L) and pancreatin (0.5 g/L) were added to the samples. Then samples were shaken at 150 rpm and incubated at 37 °C for 4 h, this process was regarded as the small intestinal phase. After the small intestinal phase, the soil residue and digestion were transferred to 100 mL anaerobic serum bottles and the same volume (30 mL) colon solution from the distal colon compartment were added. The bottles were flushed with N2 for 20–30 min to maintain anaerobic conditions and immediately capped with butyl rubber stoppers. Then samples were also shaken at 150 rpm and incubated at 37 °C for 48 h (Yin et al., 2015). The experiments were

pH

OM (%)

Clay (%)

T-Pb(mg/kg)

6.56 6.90 9.24 2.20 6.86 7.30 8.89 4.08 6.13 6.54 9.24 2.20 6.71 6.70 8.73 2.39 6.81 6.70 8.30 3.70 6.62 6.60 8.73 2.39

2.55 2.48 5.55 0.33 2.39 2.36 5.47 0.33 2.79 2.76 5.55 0.81 4.02 2.76 12.50 0.26 5.26 4.50 12.50 0.37 2.95 1.70 12.50 0.26

12.10 10.84 39.94 0.30 13.83 11.42 39.94 1.66 9.62 9.50 34.80 0.30 11.43 10.10 40.30 0.84 13.25 10.50 40.30 4.20 9.85 9.30 26.30 0.84

442.90 78.32 4904.65 7.86 152.62 35.43 1887.27 7.86 860.17 124.58 4904.65 8.86 3137.12 508.45 48,045 12.80 936.32 272.70 9585 12.80 5056.97 937.20 48,045 19.12

conducted in triplicate. After each phase, 7 mL digests of the suspension were collected and filtered (0.45 lm) and analysis by ICP-OES or ICP-MS. In vitro Pb bioaccessibility was calculated as follows:

Pb bioaccessibility ð%Þ ¼ ðin vitro Pb=total PbÞ  100 where in vitro Pb are the single bioaccessible Pb concentration in the gastric, small intestinal and colon phases, respectively, and total Pb is the concentration of total Pb in contaminated soils. 2.4. Statistical analysis Soil physicochemical property summary statistics for the present study and published data were analysis used Microsoft Excel 2016 to obtain the ranges and mean values. All the diagrams were drawn and fitted using Origin Pro 9.1. All the statistical analyses, including the Pearson coefficients and linear regression were performed by SPSS 20.0 (IBM). Stepwise multiple-linear regression analysis was used to explore factors that influence on Pb bioaccessibility and the construct regressions model to predict Pb bioaccessibility. Pearson coefficients was used to test the reliability of prediction results. 3. Results and discussion 3.1. Statistics of physicochemical properties of soils In total, 78 soil samples were tested in this study (46 for farming and 32 for mining) and data from 88 soil samples were collected from the literature (41 for farming and 47 for mining). The mean, median, and range of soil pH, OM, clay, and total Pb for farming, mining, and all samples were listed in Table 1, and other physicochemical properties of the soils were listed in Table S2. In the present study, the pH ranges from 2.20 to 9.24, the OM content was 0.30–5.47% and the clay content was 0.3–12.10%. Compared with mining soils, the mean and median of pH and clay content from farming soils were higher. Total Pb concentrations for all soils ranged from 7.86 to 4904.65 mg/kg, and the Pb concentrations of farming soils were lower than those of mining soils. A wide range

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

4

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

Table 2 Effect of soil pH on Pb bioaccessibility. Type

All

Farming soils

Literature pH

Gastric phase (%) Mean (Range)

Small Intestinal phase (%) Mean (Range)

pH

Gastric phase (%) Mean (Range)

Small Intestinal phase (%) Mean (Range)

Colon phase (%) Mean (Range)

<6.5 (N = 31)

18.20 (0.4–63.48) 14.31 (3.26–49.62) 28.44 (2.17–66.90) 29.52 (2.18–63.48) 11.26 (3.26–49.62) 24.23 (2.17–62.20) 11.97 (0.40–37) 18.75 (6–36.6) 31.75 (3.4–66.90)

3.95 (0.2–9.07) 5.26 (0.77–19.40) 6.83 (0.70–26.60) 5.40 (0.93–9.07) 3.59 (0.77–9.78) 9.38 (0.8–26.60) 3.15 (0.20–7.29) 7.69 (0.86–19.40) 4.82 (0.70–10.50)

<6.5 (N = 33)

35.67 (11.76–86.37) 57.9 (26.25–88.37) 36.54 (13.50–83.54) 37.14 (11.76–72.89) 58.13 (43.72–73.44) 36.34 (13.55–83.54) 33.92 (9.32–86.37) 57.75 (26.25–88.37) 37.22 (13.50–76.09)

10.94 (0.95–33.70) 15.40 (3.26–27.99) 16.82 (0.81–35.01) 13.00 (3.06–33.70) 15.50 (4.67–22.04) 17.36 (5.94–30.53) 8.46 (0.95–21.90) 15.34 (3.26–27.99) 14.91 (0.81–35.01)

14.39 (1.33–43.24) 13.54 (0.43–46.62) 29.34 (1.72–47.63) 18.50 (7.11–43.24) 22.33 (0.43–46.62) 30.09 (6.69–58.52) 9.47 (1.33–26.54) 7.95 (0.56–25.56) 26.71 (1.72–47.63)

6.5–7.5 (N = 32) >7.5 (N = 25) <6.5 (N = 11) 6.5–7.5 (N = 19) >7.5 (N = 11)

Mining soils

Present study

<6.5 (N = 20) 6.5–7.5 (N = 13) >7.5 (N = 14)

6.5–7.5 (N = 18) >7.5 (N = 27) <6.5 (N = 18) 6.5–7.5 (N = 7) >7.5 (N = 21) <6.5 (N = 15) 6.5–7.5 (N = 11) >7.5 (N = 6)

of soil physical and chemical properties and different concentrations of total Pb were covered in these soil samples (Table 2). Regarding data from the literature, the pH ranged from 2.39 to 8.37, the OM content was 0.26–12.50% and the clay content was 0.84–26.30%. Compared with mining soils, the mean and median pH and clay content values from farming soils were higher, especially OM content. The total Pb concentrations ranged from 12.80 to 48045 mg/kg, and the mean Pb concentrations of mining soils was 5.4-fold compared with farming soils. The median of the Pb concentrations of mining soils was 3.4-fold compared with farming soils. In addition, the mean Pb concentrations from literature were apparently higher than those in this study (6.13 and 5.88-fold increased for farming and mining, respectively). 3.2. Lead bioaccessibility in the gastric, small intestinal and colon phases The Pb bioaccessibility varies in different digestion phases (Fig. 1a). For all the data, the mean of Pb bioaccessibility was the highest in the gastric phase (31.25%) compared with the phases of the small intestinal phase (10.13%) and colon phase (17.78%). The range of Pb bioaccessibility were 0.40–88.37%, 0.20–35.01%, and 0.43 ~ 58.52% in the gastric, small intestinal and colon phases, respectively. The mean of Pb bioaccessibility for the present study was as following: gastric phase (41.10%) > colon phase (19.37) > small intestinal phase (14.00%). The mean Pb bioaccessibility for the literature was as follows: gastric phase (24.80%) > small intestinal phase (8.68%) (Table S1). The mean Pb bioaccessibility in the gastric phase was higher than it was in the small intestinal phase in both the literature and the present study, and the mean of Pb bioaccessibility in the present study was higher than it was in literature in both gastric and small intestinal phases. Compared with typical default assumptions of 60% for soil Pb (RBA, relatively bioavailability) by the US EPA (U.S. Environmental Protection Agency, 2007), the mean Pb bioaccessibility values in the different phases were significantly lower than this value. In the present study, Pb bioaccessibility in 80% of soil samples was <60% in the gastric phases, implying that the health risk assessment based on 60% of total soil Pb will overestimate the risk for most soil samples. Many researchers have explored the conversion coefficient between Pb relative bioavailability (RBA) and bioaccessibility (BAc) (Dong et al., 2016; Li et al., 2015b; Ruby et al., 1996).

With the conversion coefficient (RBA(%) = 1.41  BAc + 3.19 R2 = 0.93 pH = 2.5) reported by Ruby et al. (1996) and Li et al. (2015b), Pb-RBA (ranged from 16.33% to 127.79%) in 53% of soil samples was lower than 60% in the gastric phase for the present study, while, for the literature, the value (ranged from 3.75% to 97.52%) in 85% of soil samples was lower than 60%. With the another conversion coefficient (RBA(%) = 0.44  BAc + 6.8 R2 = 0.93 pH = 1.3) reported by Ruby et al. (1996), Pb-RBA in all soil samples was lower than 60% in the gastric phase (ranged from 10.90% to 45.68% and 6.98% to 36.24% for the present study and the literature, respectively). This implying that the health risk assessment based on 60% of total soil Pb will overestimate the risk for most soil samples. Zia et al. (2011) concluded that Pb bioaccessibility in some garden or orchard soils was <30%, which was the default value of absolute bioavailability by the US EPA (U.S. Environmental Protection Agency, 2007). In the gastric phases, Pb bioaccessibility in only 35% of soil samples was <30% for the present study, while Pb bioaccessibility in 80% of samples was <30% in the literature. In the small intestinal phase, Pb bioaccessibility in 95% of soil samples was <30% for the present study, while Pb bioaccessibility was <30% in all samples from the literature. In the colon phase, Pb bioaccessibility was <30% in almost all mining soils, and 62.5% in farming soils in the present study. The mean Pb bioaccessibility determined using PBET method was 41.10% in the gastric phase in this study, which was higher than that reported in the literature (24.80%) (Fig. 1b), this finding may be attributed to the use of different gastric pH values (1.3– 2.5) in PBET method (Table S1). The dissolution of Pb was largely related to the gastric pH, which can decreased by approximately 65% when gastric pH increased from 1.3 to 2.5 (used in many PBET methods) (Ruby et al., 1996). Other research using PBET at a gastric pH of 1.5 reported higher Pb bioaccessibility (Ngole-Jeme et al., 2018; Tang et al., 2008). In the literature, Tang et al. (2008) also reported higher Pb bioaccessibility (ranged from 49.62% to 63.48%) in the gastric phase with a gastric pH of 1.5 (Table S1). Compared with other in vitro methods (SBRC, the Solubility Bioaccessibility Research Consortium assay; RBALP, the Relative Bioavailability Leaching Procedure) where the pH value is 1.5 in the gastric phase, the mean and the range of Pb bioaccessibility were basically similar (Jorge Mendoza et al., 2017; Yan et al., 2016). The mean Pb bioaccessibility values for the soils from mining and farming in the present study were 42.72% and

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

5

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

100

100

a

80

Pb Bioaccessibility(%)

Pb Bioaccessibility(%)

80 60 40 20

G

I

40 20

G-L

C

c

60

Pb Bioaccessibility(%)

Pb Bioaccessibility(%)

60

0

0

40

b

20

G-L-F

G-L-M

G-P

G-P-F

G-P-M

d

40

20

0

0 I-L

I-L-F

I-L-M

I-P

I-P-F

I-P-M

C

C-P-F

C-P-M

Fig. 1. (a) Comparison of Pb bioaccessibility in the gastric (G) and small intestinal (I) and colon (C) phase in this study and literatures; (b) Comparison of Pb bioaccessibility from mining (M) and farming (F) in the gastric phase in this study (G-P) and literatures (G-L); (c) Comparison of Pb bioaccessibility from mining (M) and farming (F) in the small intestinal phase in this study (I-P) and literature (I-L); (d) Comparison of Pb bioaccessibility from mining (M) and farming (F) in the colon phase in this study (C-P).

39.97%, respectively, while these values for literature studies were 26.42% and 21.62%, respectively (Fig. 1b). Previous studies have reported similar variations of Pb bioaccessibility in mining and farming soils (Caboche et al., 2010). The mean Pb bioaccessibility was higher in mining soils than farming soils, which was due to the role of Pb mineral forms. Many Pb mineral phases from soils (i.e. organic Pb, Pb carbonate, Pb oxides, and Pb-goethite) were highly soluble in the acidic gastric phase, leading to the high Pb bioaccessibility in contaminated soils. Research reports a significant correlation between carbonate content with Pb-bioaccessible in gastric conditions (Gonzalez-Grijalva et al., 2019). Soil Fe oxyhydroxides is also a major source of the Pb solubilized, which depends on the particle size and crystalline nature of the Fe oxyhydroxides: Pb bioaccessibility increases as the particle size decreases (Ruby et al., 1999). In addition, soil samples that contain Pb-goethite also exhibit high bioaccessibility in the gastric phase (Fujimori et al., 2018). The mean Pb bioaccessibility determined using the PBET method was 14.00% in the small intestinal phase in this study, which was higher than the mean value in the literature (8.68%) (Fig. 1c). Compared with the bioaccessibility reported in the literature, the increased of Pb bioaccessibility in the small intestinal phase in the present study may be due to the propagated from high Pb bioaccessibility in the gastric phase to some extent (Turner et al., 2009). The duration in the small intestinal phase may be another factor attributed to this result. Yin et al. (2014) investigated the dynamic dissolution of metals in the gastrointestinal

tract and showed that Pb solubility varies from 1 to 4 h in the small intestinal phase. In the literature, Pb bioaccessibility from mining soils was higher in the small intestinal phase with a duration time of 4 h (Table S1). Mean Pb bioaccessibility values from mining and farming soils were 15.37% and 12.03% in the present study, respectively, while values in the literature were 11.32% and 5.63%, respectively (Table S1). This result indicated that the mean Pb bioaccessibility from farmland soils was lower than that of mining soils in the small intestinal phase. This result was largely due to the role of Pb mineral composition in soils. The soluble Pb in soil samples containing Pb phosphate originally was lower than galena (PbS, that is formed in acidic soils) (Ruby et al., 1999; Zia et al., 2011). Therefore, soils containing higher proportions of Pbphosphates will result in less bioaccessibility. Moreover, given the role of calcium, Pb bioaccessibility will be lower than before (Bi et al., 2015; Li et al., 2014c). From the gastric phase to the small intestinal phase, the Pb bioaccessibility decreased considerably. The widely accepted view was that metal absorption occurs in the small intestinal phase (Bruce et al., 2007). As soon as entering the small intestinal phase, soil Pb bioaccessibility was remarkably reduced, which was mainly attributed to the increase in pH from 1.5 to 7.0. Although the small intestinal pH strongly influences Pb behaviour, factors controlling the solubility of Pb in the small intestinal phase were complex. Other factor may be readsorption onto the soil matrix (Smith et al., 2011). Pb2+ adsorption increases as pH increase because fewer H+ ions can be used to compete for binding sites (Cao

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

6

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

et al., 2008). In the small intestinal phase, the increase in NaHCO3 may contributes to the adsorption of Pb onto clay edges and the formation of Pb carbonate minerals (Zia et al., 2011). In this study, the variability of soil Pb bioaccessibility in the colon phase with the SHIME model was described in detail for the first time. In the colon phase, the mean Pb bioaccessibility was increased by 1.38-fold compared with the small intestinal phase. The mean Pb bioaccessibility in farming and mining soils was 24.37% and 12.18%, respectively. Comparing with the small intestinal phase, the mean Pb bioaccessibility from farming soils in the colon phase exhibited a significant increase, while the mean Pb bioaccessibility from mining areas remains unchanged. This finding would imply that the Pb bioaccessibility from farming soils was significantly affected by human gut microbiota. Some research has shown that human gut microbiota have a great influence on the release of As and Cr (Wang et al., 2019; Yin et al., 2015). In this study, we found that human gut microbiota increased the Pb bioaccessibility in farmland soils and the reason may be that human gut microbiota play a key role in controlling Pb adsorption/desorption processes. In anaerobic environments, the reductive dissolution of Fe oxides in the presence of Fe-reducing bacteria weakened Pb adsorption, thus, Pb bioaccessibility from farming soils was greatly increased (Attanayake et al., 2017). For mining soils, other soil mineral grains may be encapsulated on the surface of lead minerals, such as quartz, which limited Pb bioaccessibility. In addition, PbS may be formed by the action of sulfate- reducing bacteria and was poorly soluble in mining soils (Ruby et al., 1999).

3.3. Effect of soil properties on Pb bioaccessibility In this part, we divide the soils into three parts according the soil pH: pH < 6.5, 6.5  pH  7.5, and pH > 7.5. These samples were defined as acidic soil, neutral soil and alkaline soil, respectively. The mean and range of Pb bioaccessibility in the gastric, small intestinal, and colon phases in this study and from published data were summarized according to the pH and provided in Table 2. A significant difference of the mean of Pb bioaccessibility was observed with different pH values (Table 2). In general, higher Pb bioaccessibility occurred in the alkaline soil from literature data, while the highest Pb bioaccessibility was found in neutral soil in the present study in the gastric phase. In the small intestinal phase, the Pb bioaccessibility values were lower in acidic soil in both the literature and the present study. The Pb bioaccessibility was also higher in the alkaline soil in the colon phase in the present study. In particular, the influence of soil pH on Pb bioaccessibility from mining and farmland soils is different. In this study, and in the literature, the mean Pb bioaccessibility from farming soils was significantly higher compared with mining soils in the acidic soil in both gastric and small intestinal phases. Mean Pb bioaccessibility was lower in the mining soil compared with farming soils for all pH ranges in the colon phase, especially for acidic and neutral soils. Based the influence of soil pH, we further explored other factors that affect on Pb bioaccessibility by regression analysis with other soil properties from literature and the present study, and the results were analysed and summarized in Table 3. Table 3 shown that OM and texture class were also the key factors influencing Pb bioaccessibility for acidic and neutral soils, while total Pb concentration influences Pb bioaccessibility for alkaline soil in the gastric and small intestinal phases. For acidic soil, Pb bioaccessibility in the gastric phase was affected by the content of silt and OM for farming soils and the content of sand for mining soils. For neutral soil, Pb bioaccessibility in the gastric phase was affected by silt and OM contents in farming and mining soils, and the R2 from farming soils was higher than that from mining soils. For alkaline

soil, no major influencing factors were found to affect Pb bioaccessibility in the gastric phase. To improve the linear regression results, other soil properties from literature and present data were added based on soil properties. Regarding Pb bioaccessibility data in the literature, CEC was added in the regression model, while total Fe, Mn, and Al as well as amorphous Fe, Mn, and Al were added in the regression model in the present study data. The linear regression results and R2 were listed in Table 4. As shown in Table 4, the major factors influence Pb bioaccessibility were different in different types and digestion phases, and R2 was improved to varying degrees by including other soil properties into the regression model. For acidic farming soils, the R2 was 0.39, and it was impacted by silt and OM, when total Fe and Al were only taken as the main factor of Pb bioaccessibility in the gastric phase in the present study, R2 increases to 0.67, and R2 increases to 0.69 when sand was used as the main factor for the published data. Without considering the soil pH, the Pb bioaccessibility of mining soils was also related to the content of total Fe to some extent (Caboche et al., 2010). The key factors influencing Pb bioaccessibility from farming and mining acidic soils were also different in the small intestinal phase for literature data, sand for farming soils and total Pb concentration for mining soils, respectively. For neutral soil, Pb bioaccessibility in the gastric phase from farming and mining soils can be better explained by the content of amorphous Al and Mn, and the R2 values increase to 0.74 and 0.82, respectively. If the content of amorphous Mn and Al and the total Pb concentration were considered, the interpretation rate of Pb bioaccessibility in the small intestinal phase would be as high as 99% in neutral farmland soils, and similar results were noted if the content of clay and amorphous Mn was considered for alkaline mining soils (Table S3). Soil properties play important roles in controlling Pb bioaccessibility. In the present study, the main factors controlling Pb bioaccessibility were various in different types of soils. More factors were considered, and a better explanation for Pb bioaccessibility may be obtained. There are also other soil properties that we did not consider that may influence soil Pb bioaccessibility. Some Pb minerals, including Pb-goethite, show highly bioaccessibility in the gastric phase (Fujimori et al., 2018). The effect of the composition of clay minerals on Pb bioaccessibility were discussed, and a significant correlation between bioaccessible Pb concentration in intestinal conditions and kaolinite content was obsereved (Gonzalez-Grijalva et al., 2019). Tang et al. (2008) reported that the Pb bioaccessibility were lower in acidic or alkali soils, which was attributed to the different compositions of clay minerals between strongly acidic soil (dominated by 1:1 clay mineral) and acidic or alkali soils (dominated by 2:1 clay minerals). In contrast, the Pb bioaccessibility was higher in acidic or alkali soils compared with strongly acidic soil for most soil samples in this study. This finding further indicates that soil Pb bioaccessibility was controlled by different factors in soils with different types.

3.4. Effect of soil types on Pb bioaccessibility The stepwise multiple-linear regression analysis showed that a significant correlation (p < 0.05) between Pb bioaccessibility and soil properties for all the soils were observed in gastrointestinal tract (Table 4). However, when all the soils from different types were considered, it emerged that soil pH, OM, clay content and the concentration of total Pb accounted for the different variability in Pb bioaccessibility in different phases. In the gastric phase, the influence of soil properties on Pb bioaccessibility was almost constant in all soil samples and farming or mining soils. In the small intestinal phase, the R2 for all soil samples was not better than that for farming or mining soils. In other words, the R2 value for differ-

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

7

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx Table 3 Comparison of regressions based on present study and literature data by different soil pH with different soil properties. Type

pH

Phases

Regression model

R2 (p value)

All

<6.5 (N = 64) 6.5 < pH < 7.5 (N = 50) pH > 7.5 (N = 52) <6.5 (N = 29) 6.5 < pH < 7.5 (N = 26) pH > 7.5 (N = 32) <6.5 (N = 35) 6.5 < pH < 7.5 (N = 23) pH > 7.5 (N = 20)

Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal

43.06–0.37*Sand 4.24 + 0.30*Clay 14.12 + 0.70*Silt-3.48*OM 2.42 + 0.21*GB 30.34 + 0.01*T-Pb 4.92–0.003*T-Pb + 0.30*GB 36.43–3.64*OM + 0.69*Clay 4.33–0.34*Clay 10.13 + 0.68*silt-3.50*OM 2.18 + 0.19*GB — 85.19 + 11.00*pH + 0.35*GB 37.90–0.31*sand 2.53 + 0.18*GB 16.21 + 0.70*Silt-2.78*OM 3.10 + 0.21*GB — —

0.26 0.30 0.55 0.51 0.13 0.36 0.39 0.27 0.62 0.44 — 0.74 0.22 0.33 0.51 0.53 — —

Farming soils

Mining soils

(p (p (p (p (p (p (p (p (p (p

< < < < < < < < < <

0.01) 0.01) 0.01) 0.01) 0.05) 0.01) 0.01) 0.01) 0.01) 0.01)

(p (p (p (p (p

< < < < <

0.01) 0.01) 0.01) 0.01) 0.01)

Note: Sand (%): the content of sand; Silt (%): the content of silt; Clay (%): the content of clay; OM (%): the content of organic matter; T-Pb (mg/kg): the concentration of total Pb in soils; GB (%): Pb bioaccessibility in the gastric phase; IB (%): Pb bioaccessibility in the small intestinal phase; CB (%): Pb bioaccessibility in the colon phase.

Table 4 Comparison of regressions based on data of literature data and present study. Type

Phase

Regression model

R2 (p value)

L+P (N = 166) L (N = 88) P (N = 78)

Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Colon Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Colon Gastric Small Intestinal Gastric Small Intestinal Gastric Small Intestinal Colon

GB = 50.34–2.21*OM + 0.31*Silt-0.001*T-Pb IB = 1.87 + 0.75*pH + 0.21*GB GB = 13.20–1.49*OM + 0.34*Silt IB = 3.37 + 0.35*OM + 0.06*sand + 0.21*GB GB = 27.87 + 0.01*T-Pb + 0.77*Clay IB = 2.05 + 1.62*pH-0.002*T-Pb + 0.16*GB CB = 24.47–0.31*Silt + 0.97*IB GB = 43.44–3.49*OM IB = 9.32 + 1.83*pH + 0.25*GB GB = 20.11–2.75*OM + 0.33*Silt IB = 3.60 + 0.10*sand + 0.23*GB — IB = 4.72 + 1.92*pH-0.01*T-Pb + 0.21*GB CB = 31.18–0.294*Silt + 0.71*IB GB = 47.11–0.40*sand IB = 2.53 + 0.19*GB GB = –23.05 + 6.46*pH IB = 1.18 + 0.37*OM + 0.13*GB GB = 17.69 + 1.96*Clay + 0.01*T-Pb — CB = 30.24–4.43*OM-0.38*Silt + 1.23*IB

0.26 0.39 0.20 0.47 0.25 0.28 0.38 0.21 0.47 0.32 0.57 — 0.49 0.29 0.22 0.36 0.26 0.43 0.44 — 0.67

P + L-F (N = 87) L-F (N = 41) P-F (N = 46) L + P-M (N = 79) L-M (N = 47) P-M (N = 32)

(p (p (p (p (p (p (p (p (p (p (p

< < < < < < < < < < <

0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01)

(p (p (p (p (p (p (p

< < < < < < <

0.01) 0.01) 0.01) 0.01) 0.01) 0.01) 0.01)

(p < 0.01)

Note: L: literature; P: the present study; F: farming soils; M: mining soils; Sand (%): the content of sand; Silt (%): the content of silt; Clay (%): the content of clay; OM (%): the content of organic matter; T-Pb (mg/kg): the concentration of total Pb in soils; GB (%): Pb bioaccessibility in the gastric phase; IB (%): Pb bioaccessibility in the small intestinal phase; CB (%): Pb bioaccessibility in the colon phase.

ent soil types is more optimistic than the value obtained using all data. The stepwise multiple-linear regression analysis was performed using the present data and the literature data, and the dependence of Pb bioaccessibility on the total Pb concentration and some soil properties such as pH, and the content of OM and clay, silt, and sand was studied. The variance explained by the linear model was very low when all the data were considered, no significant correlation between Pb bioaccessibility and soil properties was found in the gastric phase in the present study and previous literature (Hagens et al., 2009). However, the explained variance increased when soils were distinguished by the type in the small intestinal phase. OM and particle size were the two key parameters in predicting Pb bioaccessibility. The explained variance for Pb increased with organic matter in the gastric phase for farming by soil-specific adsorption reactions (Pinheiro et al., 1999). Pb associated with organic matter with various particle sizes will cause difference in lead speciation, which leads to difference in Pb bioaccessibility

(Landrot and Khaokaew, 2018). Certain predictions were obtained for both phases from different types, but Pb bioaccessibility in the gastric phase was still poor, although all available soil properties were considered. To simplify bioaccessibility calculation, the results of regression model were used to get the predicted Pb bioaccessibility. The reliability of prediction results was measured by the correlation between predicted and measured Pb bioaccessibility. Fig. 2 shown the relationship between predicted Pb bioaccessibility using equations in Table 4 and the measured Pb bioaccessibility determined using the PBET method. The predicted Pb bioaccessibility value correlated with the measured Pb bioaccessibility data for all soil samples with R2 values of 0.23 and 0.38 in the gastric and small intestinal phases, respectively (Fig. 2a). When the soil samples were classified by soil type, the R2 values were slightly different. The predicted Pb bioaccessibility from farming soils is more correlated with measured Pb bioaccessibility compared with that from mining soils in the small intestinal phase (Fig. 2b, Fig. 2c). At these

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

8

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

a

60

G

I

Fit line of G

Fit line of I

Predicted Pb Bioaccessibility(%)

Predicted Pb Bioaccessibility(%)

60

R2=0.23 (p<0.01)

40

20

R2=0.38 (p<0.01) 0

b

Fit line of G-F

Fit line of I-F

40

R2=0.20 (p<0.01) 20

R2=0.47 (p<0.01)

20

40

60

80

100

0

Measured Pb Bioaccessibility(%)

c

C-F

C-M

Fit line of G-M

60

Fit line of I-M

40

2

R =0.24 (p<0.01)

20

R2=0.36 (p<0.01) 20

40

40

60

60

80

d

100

R2=0.40 (p<0.01)

R2=0.46 (p<0.01)

40

R2=0.29 (p<0.01)

20

C-P Fit line of C-P C-P-F Fit line of C-P-F C-P-M Fit line of C-P-M

0

0 0

20

Measured Pb Bioaccessibility(%)

Predicted Pb Bioaccessibility(%)

Predicted Pb Bioaccessibility(%)

I-F

0 0

60

G-F

80

100

Measured Pb Bioaccessibility(%)

0

20

40

60

80

100

Measured Pb Bioaccessibility(%)

Fig. 2. (a) Correlations between measured and predicted Pb bioaccessibility from all data in the gastric (G) and small intestinal (I) phases. (b) Correlations between measured and predicted Pb bioaccessibility from farming soils in the gastric (G-F) and small intestinal (I-F) phases. (c) Correlations between measured and predicted Pb bioaccessibility from mining soils in the gastric (G-M) and small intestinal (I-M) phases. (d) Correlations between measured and predicted Pb bioaccessibility from the present study (C-P), and farming (C-P-F) or mining (C-P-M) soils in the colon phase.

values, the predicted Pb bioaccessibility overestimated measured Pb bioaccessibility in the gastric phase from farming and mining soils. In contrast, it underestimated Pb bioaccessibility in the small intestinal phase from mining soils. In the colon phase, for farming soils, when Pb bioaccessibility < 40%, there was a better correlation between predicted and measured data for Pb-contaminated farming and mining soils compared with all data. Soil type is an important factor worth considering when using soil properties to predict Pb bioaccessibility in small intestinal and colon phases. Although the R2 was lower and a subtle difference existed between our study and published data in specific methodological parameters, the variation in model parameters was inevitable. Equations in this study may underestimated Pb bioaccessibility to a certain extent, so it may conservatively estimate the risk to human health. Further research need to be designed and carried out to assess the relationships and changes induced by increased sample diversity and method consistency. 4. Conclusions For all the soils, the mean bioaccessibility of Pb was 31.25%, 10.13%, and 17.78% in the gastric, small intestinal and colon phases, respectively, which was lower than the default assumptions of 60% for soil Pb measured RBA by the US EPA. The mean of Pb bioaccessibility in the present study was higher than that

in the literature in both gastric and small intestinal phases. Soil pH and type are important factors worthy of consideration when using soil properties to predict Pb bioaccessibility in small intestinal and colon phases. A significant difference in the mean Pb bioaccessibility appears with different pH values. Soil Pb was more soluble in the small intestinal and colon phases for alkaline soil. When soils were distinguished by their type, the explained variance of soil properties increased in the small intestinal phase. Moreover, the Pb bioaccessibility in farmland soils was higher than it was in mining soils given the action of gut microbiota. Gut microbiota are also a factor to consider when predicting the Pb bioaccessibility in the colon phase.

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements The authors would like to acknowledge the support of the National Natural Science Foundation of China (No. 41877501).

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227

H. Du et al. / Science of the Total Environment xxx (xxxx) xxx

Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.scitotenv.2019.135227.

References Appleton, J.D., Cave, M.R., Wragg, J., 2012. Modelling lead bioaccessibility in urban topsoils based on data from Glasgow, London, Northampton and Swansea, UK. Environ. Pollut. 171, 265–272. Attanayake, C.P., Hettiarachchi, G.M., Ma, Q., Pierzynski, G.M., Ransom, M.D., 2017. Lead speciation and in vitro bioaccessibility of compost-amended urban garden soils. J. Environ. Qual. 46, 1215–1224. Bi, X.Y., Li, Z.G., Sun, G.Y., Liu, J.L., Han, Z.X., 2015. In vitro bioaccessibility of lead in surface dust and implications for human exposure: a comparative study between industrial area and urban district. J. Hazard. Mater. 297, 191–197. Bruce, S., Noller, B., Matanitobua, V., Ng, J., 2007. In vitro physiologically based extraction test (PBET) and bioaccessibility of arsenic and lead from various mine waste materials. J. Toxicol. Environ. Health A 70, 1700–1711. Caboche, J., Denys, S., Feidt, C., Delalain, P., Tack, K., Rychen, G., 2010. Modelling Pb bioaccessibility in soils contaminated by mining and smelting activities. J. Environ. Sci. Health A 45, 1264–1274. Cai, M.F., McBride, M.B., Li, K.M., Li, Z.A., 2017. Bioaccessibility of As and Pb in orchard and urban soils amended with phosphate, Fe oxide and organic matter. Chemosphere 173, 153–159. Cao, X.D., Ma, L.Q., Singh, S.P., Zhou, Q.X., 2008. Phosphate-induced lead immobilization from different lead minerals in soils under varying pH conditions. Environ. Pollut. 152, 184–192. De Miguel, E., Mingot, J., Chacon, E., Charlesworth, S., 2012. The relationship between soil geochemistry and the bioaccessibility of trace elements in playground soil. Environ. Geochem. Health 34, 677–687. Dong, Z.M., Yan, K.H., Liu, Y.J., Naidu, R., Duan, L.C., Wijayawardena, A., et al., 2016. A meta-analysis to correlate lead bioavailability and bioaccessibility and predict lead bioavailability. Environ. Int. 92–93, 139–145. Finzgar, N., Tlustos, P., Lestan, D., 2007. Relationship of soil properties to fractionation, bioavailability and mobility of lead and zinc in soil. Plant Soil Environ. 53, 225–238. Fujimori, T., Taniguchi, M., Agusa, T., Shiota, K., Takaoka, M., Yoshida, A., et al., 2018. Effect of lead speciation on its oral bioaccessibility in surface dust and soil of electronic-wastes recycling sites. J. Hazard. Mater. 341, 365–372. Gonzalez-Grijalva, B., Meza-Figueroa, D., Romero, F.M., Robles-Morua, A., MezaMontenegro, M., Garcia-Rico, L., et al., 2019. The role of soil mineralogy on oral bioaccessibility of lead: Implications for land use and risk assessment. Sci. Total Environ. 657, 1468–1479. Hagens, W.I., Walraven, N., Minekus, M., Havenaar, R., Lijzen, J., Oomen, A., 2009. Relative Oral Bioavailability of Lead from Dutch Made Grounds. RIVM. Hettiarachchi, G.M., Pierzynski, G.M., 2002. In situ stabilization of soil lead using phosphorus and manganese oxide: Influence of plant growth. J. Environ. Qual. 31, 564–572. Hong, J., Wang, Y., McDermott, S., Cai, B., Aelion, C.M., Lead, J., 2016. The use of a physiologically-based extraction test to assess relationships between bioaccessible metals in urban soil and neurodevelopmental conditions in children. Environ. Pollut. 212, 9–17. Jin, Z.F., Zhang, Z.J., Zhang, H., Liu, C.Q., Li, F.L., 2015. Assessment of lead bioaccessibility in soils around lead battery plants in east china. Chemosphere 119, 1247–1254. Jorge Mendoza, C., Tatiana Garrido, R., Cristian Quilodran, R., Matias Segovia, C., Jose Parada, A., 2017. Evaluation of the bioaccessible gastric and intestinal fractions of heavy metals in contaminated soils by means of a simple bioaccessibility extraction test. Chemosphere 176, 81–88. Juhasz, A.L., Weber, J., Smith, E., Naidu, R., Marschner, B., Rees, M., et al., 2009. Evaluation of SBRC-gastric and SBRC-intestinal methods for the prediction of in vivo relative lead bioavailability in contaminated soils. Environ. Sci. Technol. 43, 4503–4509. Karadas, C., Kara, D., 2011. In vitro gastro-intestinal method for the assessment of heavy metal bioavailability in contaminated soils. Environ. Sci. Pollut. Res. Int. 18, 620–628. Kelly, M.E., Brauning, S.E., Schoof, R.A., Ruby, M.V., 2002. Assessing Oral Bioavailability of Metals in Soils. Battelle Press, Columbus, OH. Landrot, G., Khaokaew, S., 2018. Lead speciation and association with organic matter in various particle-size fractions of contaminated soils. Environ. Sci. Technol. 52, 6780–6788. Li, H.B., Chen, K., Juhasz, A.L., Huang, L., Ma, L.Q., 2015a. Childhood lead exposure in an industrial town in China: Coupling stable isotope ratios with bioaccessible lead. Environ. Sci. Technol. 49, 5080–5087. Li, H.B., Cui, X.Y., Li, K., Li, J., Juhasz, A.L., Ma, L.Q., 2014b. Assessment of in vitro lead bioaccessibility in house dust and its relationship to in vivo lead relative bioavailability. Environ. Sci. Technol. 48, 8548–8555. Li, J., Li, K., Cave, M., Li, H.B., Ma, L.Q., 2015b. Lead bioaccessibility in 12 contaminated soils from China: Correlation to lead relative bioavailability and lead in different fractions. J. Hazard. Mater. 295, 55–62.

9

Li, Z., Ma, Z., van der Kuijp, T.J., Yuan, Z., Huang, L., 2014a. A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. Sci. Total Environ. 468–469, 843–853. Li, L., Scheckel, K.G., Zheng, L., Liu, G., Xing, W., Xiang, G., 2014c. Immobilization of lead in soil influenced by soluble phosphate and calcium: Lead speciation evidence. J. Environ. Qual. 43, 468–474. Lu, Y., Yin, W., Huang, L., Zhang, G., Zhao, Y., 2011. Assessment of bioaccessibility and exposure risk of arsenic and lead in urban soils of guangzhou city, china. Environ. Geochem. Health 33, 93–102. Mukerjee, D., 1998. Assessment of risk from multimedia exposures of children to environmental chemicals. J. Air Waste Manage. Assoc. 48, 483–501. Ngole-Jeme, V.M., Ekosse, G.E., Songca, S.P., 2018. An analysis of human exposure to trace elements from deliberate soil ingestion and associated health risks. J. Expo. Sci. Environ. Epidemiol. 28, 55–63. Pinheiro, J.P., Mota, A.M., Benedetti, M.F., 1999. Lead and calcium binding to fulvic acids: salt effect and competition. Environ. Sci. Technol. 33, 3398–3404. Poggio, L., Vrscaj, B., Schulin, R., Hepperle, E., Marsan, F.A., 2009. Metals pollution and human bioaccessibility of topsoils in grugliasco (Italy). Environ. Pollut. 157, 680–689. Ruby, M.V., Davis, A., Schoof, R., Eberle, S., Sellstone, C.M., 1996. Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ. Sci. Technol. 30, 422–430. Ruby, M.V., Schoof, R., Brattin, W., Goldade, M., Post, G., Harnois, M., et al., 1999. Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ. Sci. Technol. 33, 3697–3705. Sanderson, P., Naidu, R., Bolan, N., Bowman, M., McLure, S., 2012. Effect of soil type on distribution and bioaccessibility of metal contaminants in shooting range soils. Sci. Total Environ. 438, 452–462. Smith, E., Kempson, I.M., Juhasz, A.L., Weber, J., Rofe, A., Gancarz, D., et al., 2011. In vivo-in vitro and XANES spectroscopy assessments of lead bioavailability in contaminated periurban solis. Environ. Sci. Technol. 45, 6145–6152. Sun, G.X., Van de Wiele, T., Alava, P., Tack, F., Du Laing, G., 2012. Arsenic in cooked rice: Effect of chemical, enzymatic and microbial processes on bioaccessibility and speciation in the human gastrointestinal tract. Environ. Pollut. 162, 241– 246. Tang, X.Y., Cui, Y.S., Duan, J., Tang, L., 2008. Pilot study of temporal variations in lead bioaccessibility and chemical fractionation in some chinese soils. J. Hazard. Mater. 160, 29–36. Turner, A., Singh, N., Richards, J.P., 2009. Bioaccessibility of metals in soils and dusts contaminated by marine antifouling paint particles. Environ. Pollut. 157, 1526– 1532. U.S. Environmental Protection Agency. 2007. Estimation of relative bioavailability of lead in soil and soil-like materials using in vivo and in vitro methods. In: Office of Solid Waste and Emergency Response USEPA (Hrsg.). U.S. Environmental Protection Agency, Washington Van de Wiele, T., Gallawa, C.M., Kubachka, K.M., Creed, J.T., Basta, N., Dayton, E.A., et al., 2010. Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ. Health Perspect. 11, 1004–1009. Van de Wiele, T.R., Verstraete, W., Siciliano, S.D., 2004. Polycyclic aromatic hydrocarbon release from a soil matrix in the in vitro gastrointestinal tract. J. Environ. Qual. 33, 1343–1353. Wang, P.F., Yin, N.Y., Cai, X.L., Du, H.L., Li, Z.J., Sun, G.X., et al., 2019. Variability of chromium bioaccessibility and speciation in vegetables: The influence of in vitro methods, gut microbiota and vegetable species. Food Chem. 277, 347–352. Wijayawardena, M.A.A., Naidu, R., Megharaj, M., Lamb, D., Thavamani, P., Kuchel, T., 2015. Using soil properties to predict in vivo bioavailability of lead in soils. Chemosphere 138, 422–428. Wragg, J., Cave, M., Basta, N., Brandon, E., Casteel, S., Denys, S., et al., 2011. An interlaboratory trial of the unified barge bioaccessibility method for arsenic, cadmium and lead in soil. Sci. Total Environ. 409, 4016–4030. Yan, K.H., Dong, Z.M., Wijayawardena, M.A.A., Liu, Y.J., Li, Y., Naidu, R., 2019. The source of lead determines the relationship between soil properties and lead bioaccessibility. Environ. Pollut. 246, 53–59. Yan, K.H., Dong, Z.M., Liu, Y.J., Naidu, R., 2016. Quantifying statistical relationships between commonly used in vitro models for estimating lead bioaccessibility. Environ. Sci. Pollut. Res. 23, 6873–6882. Yan, K.H., Dong, Z.M., Wijayawardena, M.A.A., Liu, Y.J., Naidu, R., Semple, K., 2017. Measurement of soil lead bioavailability and influence of soil types and properties: a review. Chemosphere 184, 27–42. Yang, Q., Li, Z., Lu, X., Duan, Q., Huang, L., Bi, J., 2018. A review of soil heavy metal pollution from industrial and agricultural regions in china: pollution and risk assessment. Sci. Total Environ. 642, 690–700. Yin, N.Y., Cui, Y.S., Zhang, Z.Y., Wang, J.J., Wang, Z.Z., Cai, X.L., 2014. Bioaccessibility and dynamic dissolution of metals in contaminated soils. Ecolo. Environ. Sci. 23, 317–325. Yin, N.Y., Zhang, Z.N., Cai, X.L., Du, H.L., Sun, G.X., Cui, Y.S., 2015. In vitro method to assess soil arsenic metabolism by human gut microbiota: arsenic speciation and distribution. Environ. Sci. Technol. 49, 10675–10681. Zia, M.H., Codling, E.E., Scheckel, K.G., Chaney, R.L., 2011. In vitro and in vivo approaches for the measurement of oral bioavailability of lead (Pb) in contaminated soils: a review. Environ. Pollut. 159, 2320–2327. Zheng, S.A., Wang, F., Li, X.H., Wang, H., Wan, X.C., 2013. Application of in vitro digestion approach for estimating lead bioaccessibility in contaminated soils: influence of soil properties. Res. Environ. Sci. 2, 851–857.

Please cite this article as: H. Du, N. Yin, X. Cai et al., Lead bioaccessibility in farming and mining soils: The influence of soil properties, types and human gut microbiota, Science of the Total Environment, https://doi.org/10.1016/j.scitotenv.2019.135227