Sewage sludge is generated during the process of treating municipal wastewater, and it is rapidly increasing (Dong et al., 2013). In China, approximately 56% ofsludge is associated with disposed building materials, incineration waste, fertilizer, sanitary landfills, and the other sources; therefore, nearly half of the sludge has not been treated safely. Approximately one-third of the sludge is disposed of by “temporary means”, and morethan 10% of the sludge is disposed of by unknown means (He et al., 2016).

Sludge that is not treated in a timely manner continues to accumulate and occupy a large amount of land, and it can contain various heavy metals, organic pollutants and other toxic substances, which can cause secondary pollution (Lister & Line, 2001). Urban industrial sewage, domestic sewage, commercial water mixed emissions, and surface runoff inevitably lead to heavy metal accumulation in urban sludge, and these metals are not easily biodegraded once they reach into the soil environment and pose a threat to human health once they enter into the food chain (Dou et al., 2013; Grotto et al., 2015). Heavy metals in sewage sludge can eventually be taken up by humans, accumulating in fatty tissues and influencing the nervous system, immune system, endocrine system and hematopoietic function (Zhao et al., 2014; Xu et al., 2016). However, sludge can also be disposed in the form of soil conditioners or fertilizers, and improper disposal leads to a loss of organic matter and nutrient elements, thus representing a waste of resources. Sludge is rich in organic matter and nutrients, by improving soil physical and chemical properties and increasing soil organic matter, nitrogen and phosphorus, has positive and long-term effects on soil remediation or improvement (Singh & Agrawal, 2008; Kendir et al., 2014; Liu et al., 2015). To evaluate the environmental risk and sources of heavy E i r metals in sewage sludge, the geo-accumulation index (Igeo), single-factor pollution index (PI), Nemerow pollution index (PN), monomial potential ecological risk coefficient ( ) and potential ecological risk index (RI), together a multivariate statistical analysis have been widely applied (Abrahim & Parker, 2008; Shafie et al., 2013; Kowalska et al., 2016; Birch, 2017; Yang et al., 2017; Zhu et al., 2018).

To use sewage sludge in an environmentally safe manner in Wuhu City, a risk assessment should be implemented. The aims of this research were to assess the contamination status of five heavy metals (Hg, Pb, Cd, Cr, and As) from different angles via Igeo, PI, PN, E i r and RI and to identify the potential sources of the heavy metals via Pearson’s correlation coefficient analysis and a principal component analysis (PCA).

The city of Wuhu is located in southeastern Anhui Province in southeastern China, and ranks 10th out of 26 cities in the Yangtze River Delta City Group. The eight sewage treatment plants are located in: W1) Zhujiaqiao,in the Jinghu District; W2) Tianmenshan, in the Jiujiang District; W3) Binjiang, in the Yijiang District; W4) Chengnan, in the Sanshan District; W5) Wuhu Mingyuan, in the Nanling County; W6) Nanling County, in the Wuhu County; W7) Fanchang County, in the Fanchang County; and W8) Wuwei Modern, in the Wuwei County. The main sources of sewage were industrial and domestic effluents. The properties of these eight wastewater treatment plants are shown in Table 1.

Dry sludge was collected from the terminals of the sewage treatment plants in the second and fourth quarters of 2014. Each month, 3~5 500-g samples were collected from each of the sewage treatment plants. The collected samples were dried at room temperature, ground, and then separated into 0.149-mm particles through a sieve. The samples were weighed and digested with HNO3-HClH2O2 and then used to determine the content of Cd, Cr and Pb (USEPA, 1996). Cd was analyzed using an atomic absorption spectrophotometer (AA-6300 Atomic Absorption Spectrometer, Shimadzu International Trading Co., Ltd., Shanghai, China). Pb and Cr were calculated using inductively coupled plasma mass spectrometry (ICP-OES 700 Inductively Coupled Plasma Mass Spectrometer, Agilent Technologies Inc., Tokyo, Japan). The sludge samples were also digested with HNO3:HCl (10 mL, 1:1 v/v) at 95 °C for 2 h to determine the content of As and Hg (Lacerda et al., 2004) using the atomic fluorescence method (AFS-830 Dual-Channel Atomic Fluorescence Spectrometer, Beijing Titan Instruments Co., Ltd., Beijing, China).

The Igeo was introduced by Müller (1969) to assess the contamination of heavy metals in soils and sediments, and it is defined as follows:

where C_n is the content of heavy metal n in samples, mg/ kg; B_n is the background content of the metal n using the Nanjing background concentration of heavy metal in the soils (Hg = 0.12 mg/kg, Pb = 24.80 mg/kg, Cd = 0.19 mg/ kg, Cr = 59.00 mg/kg and As = 10.60 mg/kg); and 1.5 is a constant factor applied to address the lithospheric effects. The classification of the Igeo is shown in Table 2.

The PI was used to evaluate the comprehensive level of heavy metals for each study site (Tomlinson et al., 1980), and it is defined as follows:

where C_i is the concentration of the heavy metal i, mg/kg; and S_i is the standard of the heavy metal i according to CJT 309-2009 (Ministry of Housing and Urban-Rural Development, 2009). Nemerow’s synthetic pollution index (PN) was applied to assess heavy metal contamination caused by all the heavy metals at each study site. PN is defined as follows:

where Pave is the average value of the single-factor pollution index of the heavy metal i; and Pmax is the maximum value of the single-factor pollution index of the heavy metal i. The classification of PI and PN is shown in Table 3.

The RI was proposed by Hakanson (1980) and is widely utilized to assess potential ecological risk, including heavy metal pollution risk. The index is defined as follows:

where C_fⁱ is the pollution factor of the metal i; c_sⁱ is the concentration of heavy metal in samples; C_nⁱ is the standard of the heavy metal i according to Chinese Soil Environmental Standard (pH 6.5-7.5) GB15618-1995 (Ministry of Ecology and Environment, 1995) and the corresponding standard values C_nⁱ for Hg, Pb, Cd, Cr, and As are 0.5, 300, 0.6, 300 and 25 mg/kg, respectively; E_rⁱ is the monomial potential ecological risk coefficient; and T_rⁱ is the metal toxic response factor (Hg = 40, Pb= 5, Cd=30, Cr = 2 and As = 10). The classification of E_rⁱ and RI is displayed in Table 4.

The relationships among five heavy metals were determined using the Pearson’s correlation analysis. A principal component analysis (PCA) was used to reduce the dimensionality, and the highly correlated heavy metal elements were extracted into independent factors (Li et al., 2013; Lu et al., 2010).

The measured concentrations of heavy metals are presented in Table 5. According to the mean concentration values, the corresponding order of heavy metals in sewage sludge samples was Cr > Pb > As > Cd > Hg. The variation coefficients of heavy metals were ranked in de-creasing order as follows: Cd > Pb > Cr > Hg > As. Heavy metal content in the study area varied greatly among sewage treatment plants, which occurs probably because the sewage sludge samples were collected from different sites (Yang et al., 2014). The maximum concentrations of the heavy metals of the eight sewage treatment plants did not exceed the permissible content limits in the dis-charge standards (Class B) of CJT 309-2009, except for Cd at W1. Cd exceeded the permissible content limits at this site probably because the W1 sewage treatment plant collects water from an industrial area. The above results are consistent with other Chinese studies (e.g., Zhao et al., 2019), which showed that the electronics industry is a pollution source for Cd.

Geoaccumulation index values for heavy metals in sewage sludge

The I_geo values for five heavy metals are presented in Table 6. The mean Igeo values for five heavy metals were in the following decreasing order: Cd > Pb > Cr = As > Hg. The pollution order of stations was W1 > W5 > W6 > W8 > W3 > W4 > W2 > W7.

The Igeo values were less than zero for Hg at sites W1, W5, W6 and W7; Pb at sites W3, W6 and W7; Cd at sites W2 and W7; Cr at sites W3, W4, W6, W7 and W8; and As at sites W4 and W7; these findings indicate that these sites were not polluted by these metals. The Igeo values were between 0 and 1 for Hg at sites W2, W3, W4 and W8; Pb at sites W2, W4, W5 and W8; Cd at site W8; Cr at sites W1 and W2; and As at sites W1, W2, W3 and W8; these findings indicate that the pollution level of these metals at these stations ranged from unpolluted to moderately polluted. The Igeo values were between 1 and 2 for Hg at site W8, Cd at site W3 and As at sites W5 and W6; and these findings indicate that the pollution levels of these metals at these stations were moderate. The Igeo values were between 2 and 3 for Pb at site W1, Cd at site W4 and Cr at site W5; these findings indicate that these metals at these stations were polluted at moderate to heavy levels. The Igeo values were higher than 3 for Cd at sites W1, W5 and W6, what indicates that the pollution level of Cd at these stations was heavy.

Assessment of heavy metal pollution

The PI values of heavy metals are presented in Table 7. According to the mean PI values, heavy metals were sorted in the following decreasing order: Cd > As > Cr > Pb > Hg. According to these results, the sewage sludgein the study area exhibited low pollution levels for most heavy metals except for Cd at sites W1, W5 and W6 and As at sites 5 and 6. According to the mean PN values, the heavy metals were sorted in the following decreasing order: W1 > W5 > W6 > W2 > W3 > W8 > W4 > W7. The PN values for sites W2, W3, W4, W7 and W8 were lower than 0.7, and the maximum concentrations of the heavy metals of five sampling sites did not exceed the permissible content limits in the discharge standards (Class B) of CJT 309-2009. This finding suggests that the sewage sludge in these sites was safe in terms of heavy metal dis-charged into the environment and could be directly used in agriculture. The PN values for sites W5 and W6 were between 1 and 2, and the value at W1 was higher than 3, indicating that sewage sludge at these sites had risk levels of heavy metals; therefore, heavy metal pollution should be considered when using sewage sludge from these sites for land treatments.

The potential ecological risk

The RI and E_rⁱ values for each studied site are shown in Table 8. The mean Eri value of five heavy metals decreased in the following order: Cd > Hg > As > Pb > Cr. The E_rⁱ values for Hg, Pb, Cr and As in all sampling sites were lower than 40 except for Hg at site W1, suggesting that these sites did not pose a potential ecological risk. The Eri values for Cd at sites W5 and W6 were between 160 and 320, and the value for Cd at site W8 was higher than 320,suggesting that sewage sludge at these sites had high RI for Cd. W5 and W6 exhibited high risk, and W1 very high risk. The mean RI values for sites W2, W3, W4, W5, W7, and W8 were < 150, indicating that these sites had low RI. The RI values for sites W5 and W6 ranged from 150 to 300, indicating that these sites had moderate RI. For site W1, the RI values were > 600, indicating that this site had very high risk.

According to the results of Igeo, PI, PN, RI and Eri results show that the highest risk levels of heavy metal contamination in W1, W5 and W6 wastewater treatment plants, possibly may because W1 and W5 wastewater treatment plant is located near industrial area, and W6 sewage treatment plant is located in suburban areas, which is near steel woll, cement, textile and pharmaceutical manufacturing industries (Lin et al., 2002). Such heavy metal contamination emitted from industries is also consistent with other regions in China, In Shanxi Province, Cd pollution might be caused by the rich coal resources, and the large number of coal industries (Duan et al., 2017). In Guangzhou City, Cu and Cr pollution may be related to the industrial wastewater such as electroplating, chemical and machinery manufacturing industries (Li et al., 2015).

Table 9 displays the correlation coefficients as a linear correlation matrix. The results of the correlation analysissuggested a low correlation occurred between Hg and Pb (r = -0.279), Cd and Cr (r = 0.249) at 0.05 level and between Hg and Cr (r = -0.341), Hg and As (r = -0.440) and Cd and As (r = 0.394) at 0.01 level. Furthermore, high correlation was observed between Hg and Cd (r = -0.550), Pb and Cd (r = 0.862) and Cr and As (r = 0.555) at 0.01 level.

The positive correlations among metals may reflect the fact that these metals had similar pollution levels, the same behavior during transport, and common sources or at least one major source (Suresh et al., 2011). The negative correlation between Hg and Pb, Cd, Cr and As indicated that the adsorption capacity of Hg may be restrained because of the competitive adsorption of the other coexisting heavy metals in sediments (Zhang & Zheng, 2007).

PCA was a performed to identify the probable sources between the heavy metals when they were interrelated (Mirzaei Aminiyan et al., 2018). Table 10 depicts the factor loadings as well as the eigenvalues, percentile of variance, and cumulative percentages of the total loadings. According to Table 10, two principal components with eigenvalues of 2.15 and 1.39 were obtained, and they ac-counted for 78.61% of the total variance. The first principal component was dominated by Pb (0.96) and Cd (0.93) and accounted for 50.90% of the total variance. These observations show that Cd and Pb probably originated from a similar source. Previous studies (Kabata-Pendias & Mukherjee, 2007; Wei et al., 2009; Al-Khashman, 2013; Zhang et al., 2013) have reported that vehicle emissions, diesel fuel, and fossil fuel combustion are the primary sources of Cd and Pb pollution. Cd and its compounds are also known to originate from different manufactured pro-ducts, such as paints, batteries, and electrical appliances (Mico et al., 2006).Thus, the component loading of PC1can be defined as traffic emissions and the manufacturing industry. The second principal component was dominated by As (0.86) and Cr (0.85), and it accounted for 27.70% of the total variance. Based on the correlation analysis, a highly positive correlation was observed between As and Cr, suggesting that they may share a common source. A previous study reported that the main fertilizer products in China contain Cr, As and other harmful metals (Feng et al., 2009). Anhui is a major agricultural province, and the input of chemical pesticides and chemical fertilizers per unit area of cultivated land in Wuhu is well above the average level of Anhui Province of China as a whole. In addition, several studies (Yongming et al., 2006; Sharma et al., 2008; Duan & Tan, 2013) have reported that industrial and agricultural activities are major sources of As and Cr. In the study area, many industrial activities are observed, including cement and asphalt plants, a paperboard factory, a shipyard, sand mining operations, and electrical industries. Thus, the component loading of PC2 can be considered to be agriculture activities.

In summary, the maximum concentrations of the heavy metals in the eight sewage treatment plants did not exceed the permissible content limits in the discharge standards (Class B) of CJT 309-2009, except for Cd at W1. Based on the total concentration results and the Igeo, PI, PN, RI and Eri results described above, heavy metal pollution reached the highest contamination levels in the ecosystem for W1, W5 and W6 sewage sludge samples in the city of Wuhu. Pb at site W1, Cd at sites W5 and W6 and As at sites W5 and W6 were identified as the main contributors to metal pollution. Thus, measures should be taken to control these metals at these sampling sites. Cd exhibited the highest contamination level in the eight wastewater treatment plants, and the strongest ecological risk posed by Cd was primarily attributed to the fact that the toxicity coefficients of Cd were far higher than those of the other metals, although its concentration in the study area was relatively lower than those of the other metals. The correlation andPCA suggest that Pb and Cd mainly derived from traffic emissions and the manufacturing industry and that As and Cr originated from agriculture discharge.

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