Environmental Science and Pollution Research

, Volume 23, Issue 17, pp 16955–16964 | Cite as

Health risk assessment of heavy metals in soil-plant system amended with biogas slurry in Taihu basin, China

Research Article


Biogas slurry is a product of anaerobic digestion of manure that has been widely used as a soil fertilizer. Although the use for soil fertilizer is a cost-effective solution, it has been found that repeated use of biogas slurry that contains high heavy metal contents can cause pollution to the soil-plant system and risk to human health. The objective of this study was to investigate effects of biogas slurry on the soil-plant system and the human health. We analyzed the heavy metal concentrations (including As, Pb, Cu, Zn, Cr and Cd) in 106 soil samples and 58 plant samples in a farmland amended with biogas slurry in Taihu basin, China. Based on the test results, we assessed the potential human health risk when biogas slurry containing heavy metals was used as a soil fertilizer. The test results indicated that the Cd and Pb concentrations in soils exceeded the contamination limits and Cd exhibited the highest soil-to-root migration potential. Among the 11 plants analyzed, Kalimeris indica had the highest heavy metal absorption capacity. The leafy vegetables showed higher uptake of heavy metals than non-leafy vegetables. The non-carcinogenic risks mainly resulted from As, Pb, Cd, Cu and Zn through plant ingestion exposure. The integrated carcinogenic risks were associated with Cr, As and Cd in which Cr showed the highest risk while Cd showed the lowest risk. Among all the heavy metals analyzed, As and Cd appeared to have a lifetime health threat, which thus should be attenuated during production of biogas slurry to mitigate the heavy metal contamination.


Biogas slurry Heavy metals Soil-plant system Risk assessment 


Heavy metal pollution of an agricultural ecosystem has been a growing concern throughout the world (Bermudez et al. 2011, 2012). Human activities are a major factor contributing to the heavy metal pollution, sewage irrigation and fertilization with livestock manure have been blamed for increased heavy metal concentrations in the environment in China (Cao et al. 2010; Shi et al. 2011). Repeated use of biogas slurry, a product of anaerobic digestion of manure, tended to enrich heavy metals in soils (Bolan et al. 2003). The continuously cumulative heavy metals in farmlands could enter vegetables and other crops, pollute food chain and eventually threaten human health (Xiong et al. 2010; Wang et al. 2011; Harmanescu et al. 2011; Al-Hwaiti and Al-Khashman 2015). Heavy metal concentrations that vary in plants depend on soil composition, heavy metal permissibility, selectivity and absorption ability of the plant species (Ahmad and Goni 2010; Baig and Kazi 2012; Jamali et al. 2009). Enrichment of heavy metals in plants is generally assessed using accumulation factor (AF) that describes the extent of heavy metals accumulated in the soils where the plants grow (Li et al. 2012a, b; Boshoff et al. 2015). However, the heavy metal enrichment is difficult to characterize by the existing models because many important parameters are difficult to determine which include diffusion coefficients of ions in the soil solution, root geometry and size, and kinetic parameters for the uptake of ions by the roots or simplicity, and an environmental risk assessment methodology can be utilized to estimate the fate and exposure of pollutants in the environment (Río et al. 2011).

In some developing countries such as Ethiopia, the relevant monitoring lacks and thus limited data of heavy metals in food is available. In these areas, biogas slurry that may be contaminated by heavy metals is commonly used as a fertilizer for farming. The continuous application of such biogas slurry may lead to the accumulation of toxic metals in the soils. Unfortunately, very little attention is paid to the heavy metal contamination in the food chain and the potential health risks of local residents in these areas (Wang et al. 2015). One of the widely used methods is to assess the human health risk using target hazard quotient (THQ) and hazard index (HI). Hazard quotients (HQs) that are formulated by the US Environmental Protection Agency (USEPA 2000) have been widely used to measure potential health risks due to the long-term exposure to heavy metals. The quantity of HQ is approximately equal to the ratio of the estimated daily intake (EDI) to the oral reference dose (RfD) (Chien et al. 2002). HQ is typically used to indicate the non-carcinogenic health risk. The target cancer risk (TCR) is for evaluation of carcinogenic health risk (USEPA 2006, 2010; Yang et al. 2011). Nowadays, the digested slurry is utilized to fertilize the farmlands in Taihu basin, China. If the digested slurry contains toxic heavy metals, people who consume the vegetables grown in the farmlands would be subjected to the potential health risks. At present, limited studies have been undertaken to address the effects of soils amended with biogas slurries on the transfer of heavy metals from soils to plants. However, they are particularly important for evaluation of food safety and potential risk to human health. The objectives of this study include (1) measurement of concentrations of six heavy metals and identification of the source of heavy metals existed in the soil-plant system, (2) estimation of the migration abilities of heavy metals from soil to plant, and (3) evaluation of the non-carcinogenic and carcinogenic risks of different plants to the local residents in general accordance with the Chinese health risk assessment guideline (Ministry of Environmental Protection the People’s Republic of China 2014).

Material and methods

Study area

The study area is a 330-km2 site located in the Taihu basin in China. Pig manure was collected from varying sizes of farms and at different pig developmental stages (Fig. 1). The collected manure was then mixed with straws for anaerobic digestion. The resultant biogas slurry and residues were utilized for soil amendment instead of chemical fertilizers. Plants that grow in the amended soils mainly included wheat, rice and vegetables.
Fig. 1

A study area map showing the locations in Taihu Lake basin in China

Sampling and pre-treatment

The above prepared biogas slurry has been used to improve the local agricultural soils since 2012. A farmland was located approximately 0.5 km from the biogas treatment plant. Biogas slurry was spread on the soil surface in 60 m3/ha in each cultivation cycle. The biogas slurry regarded as a base fertilizer has been used to improve the agricultural soils. The cultivation plants consisted of wheat, rice and vegetables. The corresponding species of vegetables included scallion, greens, garlic, water spinach, amaranth, Kalimeris indica, Chinese cabbage, leek and coriander. The sampled vegetables, wheat, rice and background soils were located using a global positioning system (Garmin GPS 76, Beijing UniStrong Science & Technology Co., Ltd., Beijing).

A total of 106 samples of soils amended with biogas slurry were collected in 106 locations in the farmland from May 2013 to October 2013. The samples were stored in sealed Kraft packages to transport to the laboratory for analytical testing. The sealed samples were first air-dried at room temperatures between 20 and 23 °C, and any unwanted materials, such as stones and other debris, were removed. The soils were subsequently ground in an agate grinder and sieved through a 0.149-mm mesh. The remaining soils were subjected to the chemical property testing [pH, total nitrogen (TN), total phosphorus (TP) and organic matter (OM)]. Soil samples were digested with an HCl–HNO3–HF–HClO4 solution for the subsequent measurements of the heavy metal concentrations. Firstly, approximately 0.5 g of the soil sample was weighed and digested with 10 mL of HCl on an electric hot plate at approximately 100 to 200 °C until the solution volume was reduced to 3 mL. Secondly, approximately 5 mL of HF, 5 mL of HNO3 and 3 mL of HClO4 were added until any black materials disappeared. The digestion continued with addition of 3 mL of HNO3, 3 mL of HF and 1 mL of HClO4 until the solution was completely clear. Finally, the digested solution was transferred to a flask and water was added as necessary until the solution reached a fixed volume for the heavy metal measurements.

A total of 58 plant samples (500 g edible and root parts per sample) were collected randomly in 2013, which included amaranth (6 pieces), kalimeris (5 pieces), garlic (5 pieces), scallion (5 pieces), water spinach (5 pieces), greens (5 pieces), caraway (6 pieces), leek (5 pieces), Chinese cabbage (4 pieces), wheat (6 pieces) and rice (6 pieces). The collected plants were washed with tap water to remove the attached soil particles and rinsed twice with deionized water. The washed samples were dried in an oven at 70 °C to a constant weight before ground in an agate grinder and sieved through a 0.149-mm mesh. Firstly, approximately 0.5 g of the plant samples was weighed and digested with 10 mL of HNO3 and 1 mL of HClO4, and HNO3 was added when the solution was dried up during the digestion process until the vegetation fibres disappeared in the digestion tube.

Sample analyses and quality assurance

Heavy metal concentrations were determined with an inductively coupled plasma optical emission spectrometer (Optima 5300, Perkin-Elmer SCIEX, USA) and an inductively coupled plasma mass spectrometer (ICP-MS) (Agilent Technologies 7700 Series). The blank reagent, standard reference soil and plant materials (GBW07603, GBW10010 and GBW07306 supplied by the National Research Centre for Standards in China) were used in each sample batch to verify the accuracy and precision of the digestion procedure.

Assessment method of heavy metals

An enrichment factor (EF) indicates the extent to which trace elements are enriched or reduced relative to their respective background values and assesses the degree of anthropogenic influence (Meza-Figueroa et al. 2007). Another parameter termed accumulation factor (AF) was used to evaluate the translocation capability of trace metals from soil to root of the plants (Khan et al. 2010; Li et al. 2012a, b). A transfer factor (TF) was used to describe the transfer ability of the heavy metals from the roots to the aerial parts (Li et al. 2012a, b; Szolnoki and Farsang 2013). The human health risk models are an effective tool to assess carcinogenic and non-carcinogenic risks and are adopted worldwide (USEPA 2010). The health risks of heavy metals in food were assessed using the THQs specified in the USEPA region III risk-based concentration table (USEPA 2000). Chien et al. (2002) developed a method for estimation of THQ, and details of this assessment method are shown in supporting information (SI).

Statistical analysis

The test data was statistically analyzed with the Statistical Package for the Social Sciences (SPSS, version 19.0) and Microsoft Excel (2010) to consider the uncertainties associated with the calculation process and exposure factors. The measurements were expressed in terms of mean and standard deviation. Moreover, the statistically significant differences were calculated by inter-metal correlation, principal component analysis (PCA) and cluster analysis (CA).

Results and discussion

Concentrations of heavy metals

In soil samples, pH values were measured to vary from 6.56 to 6.96; TN ranged from 1578.5 to 2310.5 mg kg−1; TP was between 720.8 and 849.5 mg kg−1; and organic matter varied from 34,600 to 43,500 mg kg−1 (Table S1). The measured heavy metal concentrations in the soil samples are presented in Fig. 2. The mean concentrations of Zn, Cd and Pb in the soils exceeded the limit of the Chinese Soil Environmental Quality Standard II (GB15618-2008). The mean concentrations of Cr and Cu were below the limits set forth in the above standards. The As concentrations met marginally the standard requirement. The heavy metal concentrations obtained in this study were much higher than in other studies (Cai et al. 2012). Overall, the above comparisons indicate that the contamination of Zn, Pb and Cd was severe in the study area. Moreover, concentrations for each heavy metal varied in a wide range. The concentrations of the heavy metals were in the order of Zn > Pb > Cu > Cr > As > Cd.
Fig. 2

Concentrations of heavy metals in biogas slurry-amended soils of the study area

The concentrations of heavy metals shown in Fig. 3 are for edible plants, which are expressed with respect to dry mass of the plants. The Ministry of Health of the People’s Republic of China has recommended different Chinese standards for different heavy metals in crops. The measured concentrations of Cd and Pb exceeded the limiting values by the Chinese standards while only the concentration of Cu was below the limit. The other heavy metals (i.e. As, Cr and Zn) were measured to exceed the limits in some crops but not in all crops. For example, the heavy metal with the highest concentration was Zn in garlic (18.12 mg kg−1), Pb in water spinach (1.28 mg kg−1), As in amaranth (0.56 mg kg−1), Cd in water spinach (0.52 mg kg−1) and Cr in garlic (0.78 mg kg−1), respectively. The mean concentrations of Cr in amaranth and kalimeris were 0.74 and 0.68 mg kg−1, respectively, which did not meet the criteria of Chinese standard (0.5 mg kg−1). The Cr concentrations in several water samples of spinach and greens also exceeded the limit. By reviewing the previous studies in this area, the heavy metal concentrations measured in the present study were higher than those obtained by Zheng et al. (2007). Zhou et al. (2005) showed that a positive correlation with heavy metal concentrations exists between soils and plants. Absorption rate of Zn was found to be the fastest in the selected vegetables, which was consistent with the findings by Zheng et al. (2007). Wang et al. (2006) confirmed that leafy vegetables, such as amaranth, accumulated high Pb and Cd concentrations in their edible parts, and the mobility of Pb and Cd in soils depended on physiological features of the plants. The mean concentrations of Cu and Pb in rice were higher than in wheat. The Cu concentration in rice was 6.70 mg kg−1 (on a dry weight basis), which was far higher than that in wheat (2.76 mg kg−1). The Cd concentration in rice was 0.11 to 0.25 mg kg−1, which was much lower than that around the Dabaoshan mine in southern China (Zhuang et al. 2009). But the values still exceeded the contamination limit. Reeves and Chaney (2001) suggested that Cd was the primary concern about contamination in soil and foods, particularly in the rice system. Huang et al. (2008) reported that the concentrations of Pb, As, Cd and Cr in wheat grain were measured to be 0.177, 0.038, 0.055 and 0.108 mg kg−1, respectively.
Fig 3

Concentrations of heavy metals in crops (mg kg−1). The concentration of Zn, Cu, Pb, As, Cd and Cr is represented in af, respectively. Safety Qualification for Agricultural Product-safety Requirements for Non-environmental Pollution Vegetable (GB18406.1-2001 for Pb, As, Cd and Cr); Tolerance Limit of Copper in Foods (GB15199-1994 for Cu); Tolerance Limit of Zinc in Foods (GB13106-1991 for Zn)

Risk assessment of heavy metals in crops

The EFs of the heavy metals were calculated for the soil samples as shown Fig. 4a. Based on the calculated mean EF values, the heavy metal contamination in soils can be divided into five categories according to supporting information. In this study, Pb and Cu were under a category of moderate contamination. Cr and As fell into the category of minimal contamination. Zn and Cd were a significant pollutant. The results implied that heavy metal contamination was evident in biogas slurry-amended soils, which should receive great attentions during the risk management. The values of HIt are calculated and summarized in Fig. 4b and Table S3. Among the heavy metals estimated for HIt, As, Pb, Cd and Cu exhibited relatively higher potential health risks than Zn and Cr. In addition, the non-carcinogenic risks of As, Pb and Cd were significantly higher in growing leafy vegetables (e.g. water spinach, amaranth and K. indica) and rice than in other vegetables and wheat. Since the HIt of Cr was low, the impact of Cr on human health was insignificant. The mean HQ of the measured heavy metals was higher than 1 except for Cr. In comparison, the HQ values decreased from As, Pb, Cd, Cu, Zn to Cr. This result indicated that the heavy metals in plants presented high non-carcinogenic risks to the local adults and the high risks were associated with As, Pb and Cd. The vegetables that showed potential non-cancer risk from high level to low level were amaranth, water spinach, K. indica, greens, leek, Chinese cabbage, garlic, scallion and coriander. The HI of all heavy metals was higher in rice than in wheat. Most of the plants had HI value greater than 1, which suggested that local residents would be at risk by consuming plants in the study area. Moreover, the non-carcinogenic risks of heavy metals in leafy vegetables were significantly higher than other vegetables. The ingestion exposure of these heavy metals largely contributed to the non-cancer effect. These results illustrate that the higher non-carcinogenic risks can also be explained by the fact that more toxic metals were considered in the integrated exposure pathway for the health effect in this study. Overall, the above findings indicated that the farmland soils and the plants in the study area showed high non-carcinogenic risks. Attention should be directed to contamination of As, Pb and Cd during the risk management.
Fig. 4

Risk assessments for heavy metals. a EF values of heavy metals in soil samples. b Mean total exposure Hazard Index (HIt) of heavy metals in plant samples. c Mean target cancer risk (TCR) of heavy metals in plant samples

The carcinogenic risks associated with As, Cd and Cr were also evaluated. The results are presented in Fig. 4c and Table S3. The mean total target cancer risk (TCR) values for As, Cd and Cr were 2.02 × 10−3, 6.28 × 10−4 and 3.39 × 10−3, respectively. The cancer risks resulting from the heavy metals decreased in the order of Cr, As and Cd. These values were significantly higher than the acceptable level of 1 × 10−4, which indicated that the cancer risks pertaining to As, Cd and Cr were also high in all crops in the study area. Cr is the main pollutant source. The carcinogenic risk through food ingestion was mainly attributed to As and Cd. The CR of individual heavy metals ranged from 3.96 × 10−7 for Cd in coriander to 6.11 × 10−4 for Cr in rice. Since the TCR of Cr was the highest among the three heavy metals, the risk of Cr was the highest. The TCR of all heavy metals decreased in the following vegetables: amaranth, K. indica, water spinach, greens, Chinese cabbage, leek, garlic, scallion and coriander. Rice was found to have a higher TCR than wheat. TCR values for all crops assessed except for garlic, scallion, coriander and wheat exceeded the tolerant level of 1 × 10−4. These results imply that vegetable and grain soils cultivated with biogas slurry could have a potential carcinogenic risk. A safe agricultural application of digested manure slurry needs to be considered to prevent the further pollution of farm products.

Accumulation and translocation of heavy metals in soil-plant system

Figure 5a presents the AF values calculated for rice, wheat, leafy and non-leafy vegetables. For all types of crops, Cd had the highest AF ranging between 0.005 and 0.60, and Zn had the second highest AF which ranged from 0.006 to 0.489. These results indicated that Cr and Zn were more likely to accumulate in plants in the study area. In general, the average AF of heavy metals decreased in the order of Cd, Zn, Cr, Pb, Cu and As. Different plants also showed various accumulation capacities. Based on the calculated AF, the vegetables showing the accumulation capability from high to low were water spinach, coriander, garlic, amaranth, leek, Chinese cabbage, K. indica, scallion and greens. Moreover, rice accumulated more heavy metals than wheat.
Fig. 5

Migration abilities of heavy metals in soils, vegetables and crops related. a Accumulation factor (AF) of heavy metals in different kinds of soils. b The translocation factors of heavy metals in different vegetables and crops

Translocation of heavy metals in plants

To assess the transfer ability of heavy metals from plant roots to the aerial parts, transfer factors (TFs) of five heavy metals (i.e. Cd, As, Cu, Zn, Pb and Cr) are calculated and presented in Fig. 5b. The heavy metals that were translocated from easy to difficult were Cd, As, Cu, Zn, Pb and Cr. The vegetables showing heavy metal transfer ability in a descent order were K. indica, water spinach, garlic, amaranth, coriander, greens, leek, Chinese cabbage and scallion. Wheat had a higher transfer ability than rice. The Cd, As and Cu showed relatively high TF with the average values above 0.2 (even 0.45 for Cd). As the vegetables, wheat and rice constituted mostly the edible parts, the accumulations of Cd in these plants were hazardous and residents who consume them would be at risk. Hyper-accumulating plant species for Cd with acropetal or no restricted movement has been reported (Fritioff and Greger 2006). Another heavy metal of Cu is an essential element in various enzymes that participate in photosynthesis aiding in the formation of chlorophyll (Demirevska-Kepova et al. 2004). As chlorophyll mostly exists in leaves, cabbage tends to transfer more Cu from root to leaves than to stems. Pb has been found to be immobile or has a low mobility via root-aerial part pathway in various plant species (Zheng et al. 2007). As TF of Zn was less than 0.16, the transfer of Zn seemed to be somewhat inhibited from root to aerial parts in vegetables. This might be due to the antagonistic effect between Zn and Cd (Green and Tibbett 2008; Zheng et al. 2007). The two elements possess similar chemical properties and may behave similarly in biological systems (Malik et al. 2010). Oliver (1997) found that Cd in plant cells could combine with enzyme, thereby inhibiting the normal functions of Zn. As such, a high migration ability of Cd in vegetables in this study inhibited the transfer of Zn.

Multivariate analysis of heavy metals in soil-plant system

Interrelationships among the heavy metal concentrations were investigated in soil and plant samples using correlation coefficient matrix in Table 1. In the soil samples, Cu showed strong associations with As (R = 0.707) and Pb (R = 0.552). Furthermore, Pb exhibited a significant correlation with As (R = 0.501) whereas Cr showed significant negative correlations with Cu (R = −0.560), Zn (R = −0.516) and Pb (R = −0.711). Overall, the heavy metals of Cu, Zn, As and Pb were interrelated and hence might share a common origin in the soil, while Cr and Cd exhibited diverse relationships which might be attributed to anthropogenic activities. An examination of the correlation data for the crops revealed that a strongest correlation existed between Cu and Zn (R = 0.896), followed by the correlations of Cu and As (R = 0.851), Cu and Cr (R = 0.804), Cu and Cd (R = 0.508) and Cu and Pb (R = 0.448). An important correlation was noted between Pb and Cd (R = 0.867). The correlation results indicated the mutual variations among Zn, Cu, Pb, As, Cd and Cr in the plants. As such, these heavy metals are believed to be the result of common sources. The repeated use of biogas slurry to soils would lead to accumulation of heavy metals in plants and soils.
Table 1

Correlation between heavy metals in soils (N = 106) and in plants (N = 58)'










































































*Significant at 0.05; **significant at 0.01

Multivariate principal component analysis (PCA) of trace metals in soils was performed, showing 87 % cumulative variance of the data. As shown in Fig. S1a, the first three principal components (PCs) were computed and the calculated variances were 50, 21.7 and 15.5 %, respectively. One group consisting of Cu, Zn, Pb, As, TN and OM was mostly contributed by anthropogenic activities and could originate from similar pollution sources. This result coincided with the significant positive correlations between OM and TN. In the first principal component (PC1, a contribution rate of 50 %), Cu, Zn, Pb, As, TN and OM can come from organic fertilizers (Wu et al. 2004). In the second component (PC2, a contribution rate of 21.7 %), the correlation analysis also indicated that Cd was significantly correlated with TP as well as with pH. pH was important for the uptake of Cd. Cd in soils ranged from strongly polluted to extremely polluted Cd in acidic soils. Overall, PCA showed significant anthropogenic contribution of heavy metals in soils (Khan, et al. 2013; Mahmood and Malik 2014; Shan et al. 2013).

Given the overall contamination of heavy metals in the plants, cluster analysis (CA) with the nearest neighbour method was adopted to divide the plant into several groups as shown in Fig. S1b dendrogram. Selected plants were clustered into four groups based on significance of correlations of heavy metal concentrations in the plants. The first cluster was composed of greens and scallion; the second cluster included coriander, Chinese cabbage and leek; the third consisted of amaranth, K. indica and water spinach; and the fourth cluster was formed by rice and wheat. Since the plants in each cluster resemble in terms of heavy metal distribution, the above four groups represented different levels of heavy metal contamination. Multivariate statistics is a powerful tool for identification of the main factors determining the variability of geochemical data and interpretation of the measurement results (Saadia and Nabila 2013).


This study assessed heavy metal contamination in soil-plant system amended with biogas slurry and the potential health risk. The potential risk to human health was evaluated by examining the transfer of heavy metals from soils to plants and from plant roots to aerial parts of the plants. Based on the results and discussions, the following conclusions can be drawn.
  1. (1)

    In the farmland soils amended by biogas slurry, the concentrations of Cd and Pb in the soil-plant system exceeded the contamination limits. Based on the mean values of measured EF, Cd and Pb fell into the categories of moderate and significant contamination.

  2. (2)

    The heavy metal of Cd showed the highest migration potential among the soil, root and aerial parts of the plants. Great attention should be paid to the edible plants that contain the elevated concentration of Cd. The vegetables investigated in this study had varying transfer abilities of the heavy metals, which in the descent order were K. indica, water spinach, garlic, amaranth, coriander, greens, leek, Chinese cabbage and scallion. This result indicated that leafy vegetables had a higher uptake of heavy metals than non-leafy vegetables.

  3. (3)

    The biogas slurry was the main source of heavy metal accumulation in the amended soils and crops. The combined multivariate analysis methods were able to identify the anthropogenic source of heavy metals.

  4. (4)

    The non-carcinogenic risks mainly resulted from As, Pb, Cd, Cu and Zn through plant ingestion exposure. The integrated carcinogenic risks were caused by Cr, As and Cd in which Cr showed the highest risk while Cd showed the lowest risk. The results also indicated that As and Cd in the plants would pose a lifetime health risk so that effective measures should be taken to remediate the heavy metal pollution.




Financial support for this study was provided by the Natural Science Fund Project in Jiangsu Province (BK20151596), the Program for “333” Excellent Talents in Jiangsu Province (BRA2015524).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2016_6712_MOESM1_ESM.doc (159 kb)
ESM 1(DOC 159 kb)


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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Jiangsu Provincial Academy of Environmental ScienceNanjingChina
  2. 2.Jiangsu Province Key Laboratory of Environmental EngineeringNanjingChina
  3. 3.Terracon Consultants, IncSavannahUSA

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