Environmental Science and Pollution Research (2018) 25:27090–27105

https://doi.org/10.1007/s11356-018-2705-8

RESEARCH ARTICLE

Ecological and human health risk assessments in the context of soil

heavy metal pollution in a typical industrial area of Shanghai, China
Jing Gao 1 & Lucang Wang 2

Received: 20 March 2018 / Accepted: 3 July 2018 / Published online: 17 July 2018
# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
The purpose of this study was to identify the concentrations, sources, and potential ecological and health risks of heavy metals in
soils from a typical industrial area in Shanghai, China. A total of 28 surface soil samples were collected and analyzed for As, Cd,
Cr, Cu, Pb, Ni, Zn, and Hg from the BAO steel industry in June and July 2016. Classic multivariate statistical and geostatistical
analysis methods were used to detect the sources of heavy metals, and the ecological risk index (RI) and hazard index (HI) were
calculated to assess the potential ecological and health risks. The results showed significant pollution levels, which were derived
from the industrial production process and closely related to the spatial layout of the functional areas of the industry. The
ecological risk assessment indicated that a very high concentration zone with values ranging from 2045 to 3417 mg kg−1
represented considerable ecological risk in the range of 300 to 600. The main dominant factor affecting the ecological risk is
toxicity rather than concentration. The health risk assessment indicated that noncarcinogenic risk was mainly caused by Cr, and
the average HI value for adults was 6.48, while it was 39.01 for children. Thus, children face higher threats to heavy metals in
soils. The average carcinogenic risk values for Ni, Cr, Cd, and As were 7.97E-09, 5.2E-07, 2.1E-10, and 2.1E-09, respectively, all
of which were below the threshold values (1.0E − 04). These results provide basic information for the control and environmental
management of heavy metal pollution in steel industrial regions.

Keywords Ecological risk . Health risk . Heavy metals . Soils . Spatial distribution

Introduction human activities in the industrial, mining, and farming sectors

Soil heavy metal pollution is a central ecological issue that
stems from rapid urbanization and industrialization around
the world (MichaelBaram 2010). Since the 1980s, China has
experienced rapid urbanization and industrialization processes
(Wei and Yang 2010). The soils in China have different levels
of pollution because of the increased deposition of different
heavy metals in soils (Zhou and Guo 2015). According to a 6-
year soil pollution study conducted by the Chinese
Government, the soils of China are dramatically polluted by
Responsible editor: Zhihong Xu
* Jing Gao
gaojing5997033@126.com
1
School of Ecological and Environmental Sciences, East China
Normal University, 200241 Shanghai, People’s Republic of China
2
College of Geography and Environment Science, Northwest Normal
University, 730070 Lanzhou, People’s Republic of China
(Council 2012). Moreover, among the three area types, the
soil in industrial areas is an important component of the envi-
ronmental pollution of urban soil. Hence, the soil in industrial
areas has become a hotspot of domestic soil pollution and
remediation research, especially since the Bsoil pollution con-
trol action plan^ was promulgated by the Chinese
Government in 2016 (Li et al. 2017; Liu et al. 2017; Xia et
al. 2017).
Heavy metal pollution in soils occurs and poses significant
biological toxicity when the concentrations of heavy metals
such as As, Cd, Cr, Cu, Pb, Ni, Zn, and Hg exceed the stan-
dard safety levels (Sepulveda et al. 2010). Heavy metal pol-
lution in soil has caused evident ecological and human health
issues (Toth et al. 2017) possibly due to the toxicity and dif-
ficult degradation of heavy metals (Zhao et al. 2014). With the
passage of time, heavy metals accumulate in soils, which can
lead to the loss of nutrient components and the degeneration of
biological function in the soil (Solgi et al. 2012). For instance,
Zhang et al. (2012) found that the growth of wheat is influ-
enced by significantly higher Fe concentrations in soils.
Environ Sci Pollut Res (2018) 25:27090–27105
Additionally, heavy metal elements can easily enter the bodies
of humans and animals through ingestion, dermal absorption,
or inhalation (Muchuweti et al. 2006). High concentrations of
soil heavy metals can cause serious threats to the health of
humans and animals (Ordonez et al. 2011). For example, Hg
in soils can be absorbed by the roots of crops, and as a con-
sequence, it could be harmful to human health when Hg ac-
cumulates to a certain extent in the human body (the normal
Hg content in soils is 3–10 μg kg−1) (Saeedi et al. 2012).
Natural factors and human activities are considered as the
two major causes of heavy metal pollution (Liu et al. 2013).
However, the spatial distribution patterns of heavy metals in
topsoil mainly result from the inputs of human activities such
as metal industries, mining, vehicle exhaust, agricultural prac-
tices, coal combustion, and atmospheric deposition
(Komnitsas and Modis 2006). Industries are recognized as
one of the most significant sources of heavy metal contami-
nation in cities and may cause serious impacts to human health
(Mari et al. 2009; Kien et al. 2010).
Most of the previous studies regarding soil heavy metal
pollution have been conducted at different spatial scales such
as global, national, and regional scales (Wei and Yang 2010;
Ordonez et al. 2011; Li et al. 2014; Liang et al. 2017). Many
studies have pointed out that industrial areas are the most
important source of soil heavy metal pollution (Lopez-Arce
et al. 2017). Due to the large scales of the study areas, only one
or a few samplings were used to represent industrial areas, and
in some cases, even samples near and not within industrial
areas were used to infer the results (Ordonez et al. 2015).
Research specifically in industrial areas remains scarce possi-
bly due to the difficulty of obtaining sampling data because of
the various conditions of the areas and the limitations from
enterprises and other departments (Rachwal et al. 2015). The
lack of detailed information from specialized industrial areas
has decreased the success of pollution prevention and effec-
tive management regulation (Yolcubal et al. 2016).
Consequently, it is necessary to investigate the pollution level,
identify the fundamental source, and then assess the potential
risks of soil heavy metals in industrial areas. In this study, we
selected Baoshan Iron & Steel Co., Ltd. (hereafter simply used
as the BBAO steel industry^) in Shanghai as a case study area,
which is the most prominent steel industry in China.
The aims of this study were to (1) determine the contents
and identify the sources of eight heavy metal elements (As,
Cd, Cr, Cu, Pb, Ni, Zn, and Hg) in soil at the BAO steel
industry using the classic multivariate statistical methods of
Pearson’s correlation analysis and principal component anal-
ysis (PCA), (2) simulate and ascertain the spatial distribution
and variation characteristics of each element using a
geostatistical model to further confirm the source and detailed
cause of soil pollution from spatial mapping, and (3) evaluate
the ecological and human health risks under the existing
heavy metal distribution, and the potential ecological risk
27091
index (RI) and hazard index (HI) were calculated to convey
the evaluated results. This research will provide a baseline and
effective information to prevent further heavy metal pollution
in soils in other industrial cities while providing basic research
information for future critical studies.
Materials and methods
Study area
This study was conducted at the BAO steel industry, which
has an area of 2020 hm2 and is located in the northeast of
Shanghai, which is 26 km away from the city center of
Shanghai. Approximately 120,000 persons work at BAO steel
in different positions. The soils of the study area are predom-
inantly quaternary loose sediments of the Yangtze River estu-
ary delta, where the soil quality ranges from light to heavy
soil, organic matter accounts for 2%, and soil pH ranges from
neutral to slightly alkaline. The BAO steel industry has a flat
terrain with a gentle slope from north to south.
Soil sampling and measurements
The BAO steel industry was designed for an eco-garden fac-
tory over an area of 580.13 hm2 (Fig. 1). In May 2016, a total
of 28 soil samples at depths of 0–20 cm were collected from
the functional area of the BAO steel industry, and the locations
of the sampling points were recorded using a global position-
ing system (GPS). At the same time, land use/land cover types
in the study area were also assessed through the artificial vi-
sual interpretation of aerial images with 0.25 m resolution
(Fig. 2). The aerial images of the BAO steel industry area were
bought from the Surveying and Mapping Institute of Shanghai
under the support of project funding. The pre-processing of
aerial images contained three steps of radiometric correction,
geometric correction, and image enhancement. The object-
oriented classification method for the high-resolution image
was used to interpret images based on the eCognition 8.7
software. The overall accuracy of classification was 96.02%
and the Kappa coefficient was 0.923. Due to the limitation of
impervious surfaces in other industrial areas, all samples were
taken from green land with different types of plant communi-
ties. Seven types of plant communities with different vertical
structures cover 28.72% of the total area of the BAO steel
industry, including arbor-shrubs-herbs, arbor-shrubs, arbor-
herbs, shrubs-herbs, arbor, shrubs, and herbs. Four samples
were randomly selected from each plant community structure.
Five subsamples were collected within 100 m2 from each of
the four selected samples within each community structure
and were well mixed to form a composite sample. Soil sam-
ples were placed in a self-locking polyethylene bag and trans-
ferred to the laboratory for the required measurements.
27092
Fig. 1 Map of the study area (top right is the national boundary of China
(red area is the location of Shanghai in China). Top left is the administrate
boundary of Shanghai (red area is the location of BAO steel in Shanghai).
All soil samples were air-dried and sieved to a dimension of
0.5 mm after removing stones, residual roots, and other unwant-
ed materials. Soil samples were then sealed in brown glass bottles
and stored in a refrigerator at − 4 °C until further analyses. Soil
samples were analyzed according to the methods of the
Environmental Protection Standards of the People’s Republic
of China (HJ 803-2016) proposed by the Ministry of
Environmental Protection (MEP 2015). Soil samples (0.25 g)
were digested on a hot plate with a mixture of concentrated
HF–HClO4–HNO3 (5 ml, 2 ml, 10 ml). The digested solution
was cooled, filtered, and finally diluted to 50 ml. An inductively
coupled plasma-atomic absorption mercury analyzer (DMA-80
Environ Sci Pollut Res (2018) 25:27090–27105
Bottom right is the BAO steel boundary and distribution of the function
area. Bottom left are two pictures of the landscape and community
structure in BAO steel)
Direct Mercury Analyzer) was used to detect the concentrations
of Pb, Zn, Cu, Cd, Cr, and Ni. After microwave digesting the soil
samples by using aqua regia, an atomic fluorescence spectropho-
tometer (AFS-9230/SA-10) was used to detect the concentrations
of As and Hg.
Reagent blanks, duplicate analyses, and standard reference
materials were used in the analyses for quality assurance and
control (QA/QC). The accepted recoveries of the elements
ranged from 83 to 108%. Detection methods were assessed
in each group of blank (n = 7) and duplicate (n = 13) samples.
The relative deviation of all replicate samples from all treat-
ment batches was < 8%.
Environ Sci Pollut Res (2018) 25:27090–27105 27093

Fig. 2 Distribution of sampling

points (contain samples, function
area, land use/land cover types)

Data analyses interpolation models were chosen to perform optimal and un-
biased spatial interpolation on the concentrations of the eight
Statistical analysis heavy metals using the geostatistical approach.
The prediction accuracy for all 28 samples was evaluated
The degree of dispersion and the necessity of the normal dis- with cross-validation (Hastie et al. 2009). In this way, predic-
tribution of the data were tested by using the statistical pack- tions of all soil properties for all samples were compared with
age of the SPSS version 19.0 software (SPSS Inc., Chicago, the observed data for the entire dataset. The mean error (ME),
IL, USA) (Cambardella et al. 1994). Descriptive statistics used the mean absolute error (MAE), and the root mean square
for the analysis of the heavy metals in the soil samples includ- error (RMSE) were calculated for each heavy metal interpo-
ed minimum, maximum, mean, standard deviation (SD), and lation result, by using the following equations (Eqs. 1, 2, and
coefficient of variation (CV). We used the classic multivariate 3):
statistical methods of Pearson’s correlation analysis and PCA
1 n
to process the data and identify the potential sources of the ME ¼ ∑ ðPi −Oi Þ ð1Þ
eight heavy metals. Pearson’s correlation coefficients were n i¼1


1  
used to test the strengths of the linear relationships between MAE ¼ ∑ni¼1  Pi −Oi  ð2Þ
the pairs of variables. In the PCA, varimax was used as the n
rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
rotation method following standardization of the data. The soil 1 n
properties were not considered because their contribution to RMSE ¼ ∑ ðPi −Oi Þ2 ð3Þ
n i¼1
the PCA appeared to be insignificant.
where Pi is the ith predicted value and Oi is the ith observed
Simulation of the spatial distribution value of each heavy metal.

Kriging is a common interpolation method based on the as-
sumption that the interpolated parameter can be treated as a
regionalized variable. The spatial distribution patterns of the
concentrations of the eight heavy metals were created by in-
terpolation, and the central spatial tendency was analyzed
using the Geostatistical Analyst module in the ArcGIS 10.3
software (Su et al. 2012). The semivariance parameters and
the appropriate interpolation models were calculated using the
GS+ version 9.0 software (Gamma Design Software,
Plainwell, MI, USA) (Trangmar et al. 1986). Appropriate
Ecological risk assessment
The evaluation of the ecological risks of heavy metals in the
topsoil is conducted by following the standard method of
Hakanson (1980). This method is widely used in most of the
previous studies because the effects of concentration and po-
tential toxic are both included in the analytical procedure
(Navas et al. 1998). Specifically, the sum of the individual
potential risk factor (EI (i)) and the potential ecological risk
index (RI) can be calculated by using the following equations
27094 Environ Sci Pollut Res (2018) 25:27090–27105

(Eqs. 4 and 5):
EIðiÞ ¼ T ðiÞ  C i =C 0 ð4Þ
RI ¼ ∑ni¼1 EI ðiÞ ð5Þ
where T(i) is the toxicity coefficient for a given heavy metals
(i.e., Hg = 40, Cd = 30, As = 10, Pb = Cu = Ni = 5, Cr = V = 2,
Zn = 1), Ci is the concentration of heavy metal in the top soil,
and C0 is background concentration value of heavy metal in
the top soil.
After the calculations of EI (i) and RI values for different
heavy metals, then the levels of different potential ecological
risk were further classified as follows (Hakanson 1980):
E ðiÞ < 40; RI < 150 ¼ lower potential ecological risk
40 < E ðiÞ < 80; 150 ≤ RI < 300
¼ moderate potential ecological risk
80 < E ðiÞ < 160; 300 ≤ RI < 600
¼ considerable potential ecological risk
160 < EðiÞ < 320; RI ≥ 600
Noncarcinogenic risk is often expressed by the hazard quo-
tient (HQ). Specifically, the HQ is an index for chronic daily
intake and is the ratio between the reference dose (RfD) and
the average daily dose for a specific chemical pollutant
(Eq. 8):
HQ ¼
ADI
ð8Þ
RfD
where RfD is the reference dose of a heavy metal
(mg kg−1 day−1) that belongs to a certain class (i), as listed
in Table 2. Considering the differences in the RfDinh values for
children and adults, we multiplied the soil reference dose by a
gastrointestinal absorption factor according to the USEPA
method (For and Oswer 2002) to assess dermal risk. Our stud-
ied environment (BAO steel industry) has many kinds of pol-
lutants, and therefore, we assessed the overall noncarcinogen-
ic effects from exposure to mixed chemicals (Eq. 9).
ADIi
HI ¼ ∑HQi ¼ ∑ ð9Þ
RfDi

¼ higher potential ecological risk An HI value greater than 1 indicates noncarcinogenic ef-
fects, and the risk will increase with the increase in HI value.
E ðiÞ ≥ 320 ¼ dangerous In contrast, HI values less than 1 indicate that the exposed
humans are unlikely to be influenced by the chemical sub-
stances (USEPA 1989).
Human health risk evaluation
(iii) Carcinogenic risk assessment
(i) Exposure coefficient
Carcinogenic risk refers to the probability of human beings
developing cancer due to the exposure to cancer hazards
Generally, humans are influenced by pollutants in three ways,
throughout their lifetime (Eq. 10) (Epa 2009):
ingestion, inhalation, and dermal absorption (Sepulveda et al.
2010). However, inhalation and dermal absorption are the ways
in which heavy metals in the soil around industries enter the Risk ¼ ADI  SF ð10Þ
body, which are the main ways that damage human health be-
cause of long-term exposure (Sun et al. 2013). According to a where SF is the carcinogenicity slope factor (mg kg−1 day−1),
previous study (Meers et al. 2010), we calculated the average as listed in Table 2. Risk values ranging from 1.0E − 04 to
daily intake (ADI) of heavy metals by the following equations 1.0E − 06 are generally considered normal, while those ex-
(Eqs. 6 and 7): ceeding 1.0E − 04 will have a lifetime cancer risk to the hu-
man body. If multiple cancer contaminants are present in the
IRinh  EF  ED study area, then the cancer risks from all chemicals and routes
ADIinh ¼ C  ð6Þ
BW  AT were summed (USEPA 1989).
SA  AF  ABS  EF  ED
ADIderm ¼ C  ð7Þ
BW  AT
Results and discussion
where ADIinh refers to the inhalation through the nose and
mouth, ADIderm refers to touch through the skin, and the other Characteristics of soil heavy metals
terms are explained in Table 1.
The results of the descriptive statistics showed that heavy
(ii) Noncarcinogenic risk assessment metal elements in soil exhibit three levels of pollution at the
BAO steel industry, which are not exceeding, intermediately
Environ Sci Pollut Res (2018) 25:27090–27105 27095

Table 1 The average daily intake

(ADI) of chemicals in soils is Parameter Unit Meaning Value
calculated using the following
parameter value Child Adult

C mg kg−1 Concentration of the heavy metals Measured source data

EF d a−1 Exposure frequency 320 350
ED a Exposure duration 6 30
BW kg Body weight 20 70
AT1 d Averaging time of noncarcinogenic risk ED × 365 (noncarcinogenic)
AT2 d Averaging time of carcinogenic risk 70 (lifetime) × 365 (carcinogenic)
IRinh m3 day−1 Inhalation rate 7.63 12.8
AF mg cm−2 Adherence factor 0.2 0.07
SA cm2 Exposed area 2800 5700
ABS / Dermal absorption factor 0.03 (As), 0.001 (other heavy metal)

Source: USEPA (2002) Supplemental guidance for developing soil screening levels for superfund sites. U.S.
Environmental Protection Agency, Office of Emergency and Remedial Response, Washington

exceeding, and highly exceeding the standard value. More
specifically, all samples with detected As did not exceed the
standard value, whereas 100, 100, 100, 57.14, 50, 57.14% and
42.86% of the samples with detected Pb, Zn, Cr, Hg, Cu, Cd,
and Ni exceeded the standard values, respectively (Table 3).
Here, we used the background values from a previous trust-
worthy study on the background values for soil heavy metals
in Shanghai (Feng 2009). In this study, we found that only one
sample of Hg exceeded the standard value by ten times,
whereas few Pb samples exceeded the background Pb values
by more than one hundred times. The mean concentrations of
Cd, Cr, Zn, and Cu were higher than those reported in back-
ground values of Shanghai. The mean concentrations of Ni
and As were higher than the reported background values for
Shanghai.
The spatial heterogeneities of Hg and Pb concentra-
tions in the soils were higher than that of the other
heavy metal elements, but their coefficients of variation
were 1.14 and 2.53, respectively (Table 3). The high
spatial heterogeneities of these two heavy metals might
be related to the layout of different production function-
al areas because the entire study area was located in an
urban industrial zone without significant differences in
the basic properties of the soils (Taghipour and Jalali
2015). The coefficient of variations for the Cd and Zn
soil concentrations were between 0.5 to 1, thereby
reflecting a higher possibility of being influenced by
extrinsic factors of industrial production (Ebrahimi et
al. 2012). The coefficient of variations of the concentra-
tions of As, Cu, Cr, and Ni in soil were all lower than
0.5, thereby suggesting that external impact on these
heavy metals was comparatively uniform and the homo-
geneity of their concentrations was slightly different all
over the region (Zanini et al. 1992; Trevors 2010).
Thus, the source of these heavy metals may be initiated
from the background of soil.

Table 2 Summary of reference

dose (RfD) and cancer slope Heavy Inhalation RfD Dermal RfD Inhalation SF Dermal SF
factor (SF) of heavy metals1,2,3 metal (mg kg−1 day−1) (mg kg−1 day−1) (mg kg−1 day−1) (mg kg−1 day−1)

Pb 1.40E − 03 5.24E − 04 NA NA
Cr 3.00E − 03 3.00E − 03 5.01E − 01 2.00E + 01
Cd 1.00E − 03 2.50E − 05 NA NA
Ni 2.00E − 02 5.40E − 03 1.70E + 00 4.25E + 01
Cu 4.00E − 02 1.20E − 02 NA NA
Zn 3.00E − 01 6.00E − 02 NA NA
As 3.00E − 04 1.23E − 04 1.50E + 00 3.66E + 00
Hg 3.00E − 04 2.14 E − 05 NA

NA not applicable
1
United States Environmental Protection Agency (USEPA) (2011)
2
United States Environmental Protection Agency (USEPA) (1999)
3
Ferreira-Baptista L and Miguel E (2005)
27096 Environ Sci Pollut Res (2018) 25:27090–27105

Table 3 Descriptive statistics of heavy metal concentrations in soils of the BAO steel industry

Heavy metal Min. Max. Mean Standard deviation Coefficient of variation (CV) Background value4 Standard-exceeding rate (%)

Hg (μg kg-1) 0.07 1235.7 232.75 235.31 1.14 150 57.14

As (mg kg−1) 0.58 2.1 0.84 0.34 0.46 9.1 0
Pb (mg kg−1) 28.4 2442.9 180.87 523.90 2.53 25.47 100
Zn (mg kg−1) 108.3 668 202.53 150.85 0.68 86.1 100
Cu (mg kg−1) 20.1 69.2 34.43 13.84 0.36 28.59 50
Cr (mg kg−1) 89.3 366 166.30 64.47 0.38 75 100
Cd (μg kg−1) 0.10 1205.7 431.40 335.75 0.88 240 57.14
Ni (mg kg−1) 7.86 60.5 32.85 10.32 0.34 31.9 42.86
4
Feng, D. 2009. A Preliminary Study on Background Levels of Thirteen Priority Metals in Soil of Shanghai. Shanghai Environmental Sciences

In the BAO steel industry, there were significantly positive
correlations between Zn and Cd (r = 0.88, P < 0.001), Cu and
Zn (r = 0.83, P < 0.001), Cu and Pb (r = 0.75, P < 0.001), Zn
and Pb (r = 0.72, P < 0.001), Cu and Cd (r = 0.62, P < 0.001),
and Cu and Ni (r = 0.67, P < 0.001) in the soils, whereas all
other remaining correlations were statistically not significant.
These results showed that Pb, Cd, Cu, and Zn have similar
geochemical sources and enrichment and migration character-
istics, whereas it is easier for Pb and Cd to coexist in soil than
Cu and Zn (Pan et al. 2016). The positive correlation between
Ni and Cu indicates that Ni promoted the storage of Cu in the
soil. The positive correlation between the pairs of Cr, Cu, and
Zn indicates that Cr is favorable for the storage of Cu and Zn,
and there is a common source of Cr and Cu and Zn.
Interestingly, Cu and Zn easily coexist due to the same source,
and hence, the treatment of pollution problems can be consid-
ered synergistic governance (Pan et al. 2015). There was no
significant negative correlation between all elements at the 1
or 5% level, which indicates that heavy metal elements were
probably from a common source of industrial production, and
hence, an intensive antagonistic effect did not exist (Table 4).
The first axis of the PCAwas mainly defined by Cu, Zn, Cr,
and Cd and explained 35.30% of the total variance (i.e.,
71.01%), whereas the second axis was explained by Pb and
Hg and accounted for 24.47% of the variation (Table 5). The
third axis was primarily loaded by As and Ni and explained
17.82% of the variation, which could be lithogenic compo-
nents and appeared to be associated with soil parent materials
(Pouyat et al. 2015). Based on the PCA result, the eight heavy
metals were classified into three groups, i.e., (1) Cu, Zn, Cr
and Cd; (2) Pb and Hg; and (3) As and Ni, and hence, may
indicate that there are three different sources of heavy metals
in the soils of the BAO steel industry. A previous study (Gao
et al. 2013) found that enrichment of Cd, Cu, and Zn in indus-
trial soils was closely correlated with industrial production. Cd
is an important industrial and environmental pollutant, which
mainly comes from the smelting of Zn, Cu, and Pb
(Rodriguez-Espinosa et al. 2017). The Cd in the atmosphere
mainly comes from industrial production, such as the smelting
of nonferrous metals, the sintering of ores, and the disposal of
Cd-containing wastes (Li et al. 2014). In general, the content
of Cd in soil is 0.01–2 mg/kg, and the average value is
0.35 mg/kg (Li et al. 2015). The concentrations of Cd in the
soil near the metal smelter and its downwind region are very
high, resulting in a wasteland. The Cd-containing waste resi-
due accumulates, allowing Cd compounds to enter the soil and
water bodies (Kandulu et al. 2014). Pb pollution in the envi-
ronment is caused by car emissions due to Pb-containing
wastes. Moreover, during the combustion of gasoline with
tetraethyl Pb as an antiknock agent (1 to 3 g per kilogram of

Table 4 Pearson’s correlation coefficients of the heavy metals in the soils of the BAO steel industry

Heavy metal Hg (μg kg−1) As (mg kg−1) Pb (mg kg−1) Zn (mg kg−1) Cu (mg kg−1) Cr (mg kg−1) Cd (μg kg−1) Ni (mg kg−1)

Hg (μg kg−1) 1.000

As (mg kg−1) 0.427 1.000
Pb (mg kg−1) 0.030 0.098 1.000
Zn (mg kg−1) 0.449* 0.248 0.718** 1.000
Cu (mg kg−1) 0.086 0.195 0.750** 0.830** 1.000
Cr (mg kg−1) −0.208 0.039 0.139 0.454* 0.456* 1.000
Cd (μg kg−1) 0.392 0.246 0.493* 0.876** 0.623** 0.503 1.000
Ni (mg kg−1) −0.096 −0.343 0.382 0.390 0.668** 0.218 0.321 1.000

*P < 0.05; **P < 0.01

Environ Sci Pollut Res (2018) 25:27090–27105 27097

Table 5 Principal component analysis (PCA) of 28 soil samples for which should be as small as possible for accurate interpola-
eight heavy metals in the BAO steel industry
tion. The corresponding accuracy statistics of the spatial dis-
Heavy metal Principal component analysis tribution demonstrated that the simulation results meet the
modeling requirements (Table 7).
PC 1 (35.30%) PC 2 (24.47%) PC 3 (17.82%) Although the concentrations of Cu and Zn were different,
Pb 0.82 0.76 − 0.15
their distribution trends were generally similar, indicating they
have the same source of origin (Dhawan et al. 2009). The
Cr 0.14 0.38 0.74
concentrations of Cu and Zn exhibited a dispersed distribu-
Cd 0.69 0.41 − 0.26
tion, and the highest values were located in the north, east, and
Ni 0.17 0.09 0.05
northeast of the BAO steel industry. Consequently, the
Cu 0.10 0.80 0.16
hotspots of concentrations had relationships with multifunc-
Zn 0.76 0.23 0.09
tion areas with busy traffic such as railway stations (P), and
As 0.08 − 0.12 0.05
material storage areas such as phase I and II raw material fields
Hg 0.89 0.50 0.24
(B); in particular, there were hotspots near processing and
Values in parentheses indicate the variance (%) accounted for by each manufacturing industries such as electric furnace and public
axis. Values in the table indicate the eigenvector scores of each of the auxiliary areas (K), initial rolling areas (S), and harbors near
heavy metal on the three PCA axes the river estuary such as finished terminals and steel pipe areas
(R), which cause diffusion of Cu and Zn (Figs. 2 and 3).
gasoline), Pb is discharged into the environment with the ex- Higher Cd concentrations were distributed in the southern area
haust gas from transportation tools or power machinery (Guo of the BAO steel industry where the main function is produc-
et al. 2014). The total global annual discharge of 400,000 tons tion and processing, which might have resulted from the emis-
is due to more than 200 million vehicles around the world, sions of wastewater or sludge influenced by production activ-
which have become the main source of Pb pollution. There is ities (Saeedi et al. 2012). In addition, Cd followed almost the
a consistent cognition of the composition of the pollution same distribution pattern as Zn and Cu, which was probably
sources and the relative importance of the pollution sources. due to the relatively discrete spatial distribution (Li et al.
The Hg enrichment in the soil mainly results from the emis- 2014). In contrast, Pb, Cr, and Ni did not follow the same
sions from burning fossil fuels, especially coal, which is the distribution patterns as Cd, Cu, and Zn. Their distribution
largest source of global Hg emissions in the environment pattern was characterized by the radial diffusion of a particular
(Islam et al. 2016). In 2015, the total Hg in anthropogenic hotspot area. The pain Pb hotspot was located in the southeast
emissions from Europe was 341.8 tons, of which 26% was corner of the BAO steel industry, and hence, was associated
produced from coal-fired power industries, which are one of with the functions of the finished terminal and steel pipe area
the largest sources of Hg pollution. Hence, Pb and Hg could (R) (Fig. 3). The high concentrations of Pb in the study area
be classified as additional fuel consumption related to indus- resulted from the fuel from the nearby cargo ship pier, which is
trial production, including coal combustion and gasoline con- consistent with the general sources of Pb pollution. Moreover,
sumption (Nanos et al. 2015). the pollution patterns were similar to the pollution of tradition-
al docks throughout the world (Basha et al. 2007). The Cr and
Stimulation of spatial distribution of heavy metal Ni hotspots were mainly associated with the functions of elec-
pollution in soils tric furnace and public auxiliary areas (K), and the central
machine repair area (U), while other areas were less variable.
We also found that the original Ni and Hg data did not meet These hotspots were comparable to standard concentrations
the assumptions of linearity and normality. Therefore, the data and were generally less polluted, thereby indicating that the
were natural-log transformed in order to meet the assumptions soils in the BAO steel industrial area have not been influenced
of the normal distribution (Table 6). The optimal fitting by emissions from the industry of these elements.
semivariance model and related parameters were determined The distribution of Hg was not similar to the distribution
from the concentrations of 28 samples in the soils of the BAO pattern of the six other heavy metal elements. However, the As
steel industry by using the GS+ (version 9.0) semivariance distribution almost followed that of Hg (Fig. 3), which was
analysis software. The spatial distribution patterns of soil probably due to the nonexistent hotspots for these two heavy
heavy metals in the BAO steel industry showed that the con- metal elements (Bai et al. 2011). The center of the distribution
centrations of heavy metals were greater in the red colored of Hg was focused on the functional areas of the power plant
areas than in the blue colored area (Fig. 3). The ME is a and evenly expanded outward (H), which was caused by ex-
measure of the bias of the interpolation and should be close haust emissions from coal combustion by the heating supply
to 0, and the RMSE should be close to 1 for unbiased methods. industry, which is consistent with the general sources of Hg
The MAE is a measure of the accuracy of the interpolation, pollution as mentioned above (Sundaray et al. 2011).
27098 Environ Sci Pollut Res (2018) 25:27090–27105

Table 6 Theoretical semivariogram models for soil heavy metal concentrations and the corresponding parameters

Heavy metal C0 C0 + C C0/ Range R2 RSS Model

(C0 + C)

Hg (μg kg−1) 1160 10,140 0.886 0.0189 0.143 4.17E + 07 Spherical

As (mg kg−1) 0.10509 0.10509 0.422 0.034 0.01 9.85E-03 Gaussian
Pb (mg kg−1) 2000 5.15E + 05 0.502 − 999 0.206 1.27E + 11 Exponential
Zn (mg kg−1) 3200 35,700 0.915 0.124 0.33 2.19E + 08 Linear
Cu (mg kg−1) 7.8 226.5 0.966 0.1435 0.308 7.87E + 03 Exponential
Cr (mg kg−1) 360 6380 0.947 0.0754 0.912 1.31E + 06 Linear
Cd (μg kg−1) 16,800 195,300 0.907 0.1329 0.401 3.41E + 09 Spherical
Ni (mg kg−1) 0.1 61.77 0.998 0.01 0 7.46E + 02 Spherical

However, the As pollution value was less than standard con-
centrations, hence indicating no pollution. This result suggests
that soils in the BAO steel industrial area were not affected by
As. The various ecological and health risks may be influenced
by the concentration and distribution patterns of the metals.
More research with additional calculations and assessments is
essential to convincingly determine the risk levels caused by
heavy metals.
It has been found that the simulation accuracy of the spatial
distribution of heavy metals in soil is positively correlated
with the sampling cost. A large number of soil samples need
to be collected for measurement and analysis to simulate spa-
tial distribution characteristics with high precision. Previous
studies (Lin et al. 2010; Yang et al. 2015) have shown that
when there is a reasonable number of samples within a certain
range, the sampling cost can be reduced while ensuring the
accuracy of the simulation. Our study is limited by the distri-
bution of impervious surfaces, the control of the plant area,
and the type of the vegetation around the industrial plant. As a
result, the uneven distribution and lack of samples will have
an influence on the simulation accuracy. Therefore, we should
pay more attention to determining the reasonable number of
samples and optimizing the sampling method in the future
(Nanos et al. 2015).
Ecological risk assessment
The ecological risk E(i) values of eight elements in the surface
soil of the BAO steel industry are shown in Fig. 4. The mean
E(i) values for As, Zn, Cu, Cr, and Ni were relatively less than
40, suggesting that these elements imposed low levels of eco-
logical risks (Li et al. 2014). However, Pb had a medium E(i)
mean value (38.7), which is nearly to the threshold value of
40. In contrast, Hg and Cd had higher mean E(i) values (58 for
Hg and 55 for Cd), which exceed the threshold value of 40.
With respect to the other six heavy metals, their mean E(i)
values ranged from 40 to 80. Meanwhile, several sampling
sites posed significantly dangerous levels of potential ecolog-
ical risk. For example, the maximum value of E(Hg) was 331,
and that of E(Pb) was 482, which are obviously more than
320. These levels are strongly associated with coal-fire in
thermal power plants for E(Hg) and fuel pollutant discharge
from cargo ship transport at docks for E(Pb). The values of
E(Cd) for the samples were high overall, and these values are
associated with industrial steel production with certain chem-
ical types (Ben Achiba et al. 2010). In general, the potential
ecological risks of Hg, Pb, and Cd, especially Hg and Pb,
should be considered in terms of the health of a local commu-
nity because they are much higher than the other heavy metals
assessed.
Our results are consistent with the previous studies con-
ducted in industrial and urban areas that assessed ecological
risk (Zhang et al. 2012). For instance, the horizontal and ver-
tical distribution characteristics of the seven heavy metal types
were reported around a Pb and Zn smelter from Midwest
Shaanxi Province. They found that the pollution levels of Cd
and Hg were severe, and the pollution level of Pb was mod-
erate, indicating the potential existence of an ecological haz-
ard (Pan et al. 2016). Within the soils of other megacities such
as Rome and Mexico, Cd and Hg also exhibited much higher
risks than other elements in terms of potential ecosystem
health in some studies (Rajbala 2012; Alam et al. 2016). The
above analogous achievements were analogous to a survey
conducted by Chen et al. (2015), who reported that Hg and
Cd mainly contributed to the heavy metal pollution of soil in
urban areas. In particular, the establishment of industrial op-
erations since the 1970s has resulted in the increased interfer-
ence of human behavior due to rapid economic development
and urbanization in China, which have drastically increased
industrial waste discharges, including exhaust gas settling,
wastewater infiltration, and waste residue abandonment
(Egiarte et al. 2009).
The RI values were computed to evaluate the ecological
risk of multiple heavy metals in soil. A total of 80.65% of the
RI values of all samples were less than 160, indicating low
ecological risk. The range of RI values from 160 to 300
accounted for 9.8% of all samples, indicating moderate eco-
logical risk. In addition, 4.85% of the topsoil samples have RI
Environ Sci Pollut Res (2018) 25:27090–27105 27099

Fig. 3 Spatial distribution

simulations of eight heavy metals,
namely arsenic (As), cadmium
(Cd), chromium (Cr), copper
(Cu), lead (Pb), nickel (Ni), zinc
(Zn), and mercury (Hg) in the
BAO steel industry soils

values in the range of 300 to 600, indicating potentially con-
siderable ecological risk. Additionally, the RI values of some
surface soil samples were higher than 600 (4.76% of samples),
posing potentially significant ecological risk resulting from
multiple metals in soil. The spatial distributions of RIs for
multiple heavy metals in the industrial plant soil are shown
in Fig. 5a, indicating that the hotspots were located in the
powerplant (H) and finished terminal and steel pipe area (R)
of the factory function area. This result indicates a very high
ecological risk, but the zones near hotspots represented con-
siderable ecological risk. In general, most of the BAO steel
area showed low to moderate potential ecological risks.
The highest RI values for some functional areas were con-
sistent with the spatial distribution patterns of Hg and Pb
(Fig. 3), indicating that Hg and Pb exposed the highest eco-
logical risk in the study area. A major source of the
27100 Environ Sci Pollut Res (2018) 25:27090–27105

Table 7 Cross-validation results

for kriging interpolation of Heavy metal Mean error (ME) Root mean square error (RMSE) Mean absolute error (MAE)
concentrations of heavy metals in
the BAO steel industrial soil Hg (μg kg−1) 0.03 0.85 29.50
As (mg kg−1) − 0.03 0.98 9.68
Pb (mg kg−1) 0.04 1.68 66.22
Zn (mg kg−1) 0.05 1.43 35.21
Cu (mg kg−1) 0.03 1.34 13.36
Cr (mg kg−1) 0.06 1.24 64.50
Cd (μg kg−1) 0.02 1.15 23.48
Ni (mg kg−1) 0.04 1.26 13.98

accumulation of Pb in soil may be attributable to fuel contam-
inants from a freighter at the pier (Singh et al. 2010). The
emission of coal contaminants from the thermal power plant
was considered as the key origin, which might have resulted
from to the accumulation of Hg in the topsoil. The spatial
distributions of the high concentrations of eight heavy metals
were located in the southeast corner and the central regions of
the power plant (H) and electric furnace and public auxiliary
area (K) (Fig. 5b). However, the spatial distribution of the total
concentrations of the eight elements was slightly different
from that of the RI values, suggesting that the main factor that
affected the potential ecosystem health of the soil was proba-
bly the high toxicity rather than the concentration (Ibrahim et
al. 2016).
Human health risk assessment
The main human exposure pathway to heavy metals in soil is
dermal absorption, while a more common exposure pathway
is inhalation (Sundaray et al. 2011). In terms of the ADI of
adults, the noncarcinogenic risk value reached the level of
2.45E − 06 mg/kg-day through the dermal absorption path-
way, whereas it was only 1.54E − 10 mg/kg-day through the
Fig. 4 The potential ecological risk of single factors of heavy metals in
the surface of the soil from the BAO steel industry (E(i), the maximum,
95th percentile, median, 5th percentile, and minimum values)
inhalation pathway (Fig. 6). Meanwhile, the ADI for children
was 1.36E − 05 mg/kg-day through the dermal absorption
pathway, whereas it was 6.24E − 07 mg/kg-day through the
inhalation pathway (Fig. 6). This difference suggests that chil-
dren were at higher risk of noncarcinogenic exposure than
adults.
Among all the heavy metals that were studied, people are
easily exposed to Hg, Cd, Cr, and Pb due to the high concen-
trations in the surrounding soil. In contrast, humans were less
exposed to the high concentrations of the four other heavy
metals. For example, a previous study reported that the pro-
portion of Hg, Cd, Cr, and Pb risks accounted for 24.7, 14.6,
3.6, and 53.2% of the total HI value, respectively, in the area
surrounding the steel industry next to the Queen Alia Airport,
Jordan (Al-Khashman and Shawabkeh 2009). Similarly, an-
other study reported that the proportion of Hg, Cd, Cr, and Pb
risks to the entire HI value was 96.8 in the Ansteel industrial
area in Liaoning Province of northeast of China (Xiao et al.
2015). In this study, we found that Cr was the main heavy
metal that caused the noncarcinogenic risk, and hence, the
average HI value for adults was 6.64, while it was 39.54 for
children (Fig. 6). By contrast, the other heavy metals with sub-
high noncarcinogenic risks for children were Pb and Hg, and
the values were 5.48 and 1.95, respectively. Analogously, for
adults, the heavy metals with sub-high noncarcinogenic risks
were Pb and Cd, and the values were 0.94 and 0.52, respec-
tively, which coincide with the results of previous studies on
metal smelting industrial areas or general urban industrial park
areas (Peng et al. 2013). These results indicate that the non-
carcinogenic risks of heavy metals in the BAO steel area are
the same as those in urban industrial park areas (Baghdadi et
al. 2012). The future process of repairing and governing soil
heavy metals in industrial areas should concentrate on purify-
ing these four heavy metals (Vareda and Duraes 2017).
Carcinogenic risk is the process of accumulation over time,
but it is not necessary to separately evaluate the risk assess-
ments for adults and children. The exposure pathways for As
include ingestion, inhalation, and dermal absorption, but the
main exposure pathway for Cr, Cd, and Ni is inhalation,
whereas ingestion and dermal absorption both act as general
exposure pathways and hence can be ignored (Wu et al. 2015).
Environ Sci Pollut Res (2018) 25:27090–27105 27101

a b

Fig. 5 Spatial distribution characteristics for total concentration (a) of eight heavy metals in the BAO steel industrial (b) and potential ecological risk
indices (RI)

The average carcinogenic risk values for Ni, Cr, Cd, and As in
the soil samples were 7.89E-09, 5.34E-07, 2.3E-10, and 2.2E-
09, respectively.
Generally, the levels of acceptable or inconsequential carcino-
genic risk ranged from 1.0E − 06 to 1.0E − 04. The results of the
majority carcinogenic risk laid between 1.0E − 07 and 1.0E − 10.
For BAO steel, no heavy metal surpassed the threshold value of
1.0E − 04, thereby leading to high-risk levels for metals such as
As, Cr, Cd, and Ni. The carcinogenic risk decreased in the fol-
lowing order Cr > As > Ni > Cd (Fig. 7).
The carcinogenic risk in the BAO steel factory fell within
the acceptable range, and hence, we could conclude that it
would not arouse long-term serious health impacts in the
BAO steel industry with respect to Ni, Cr, Cd, and As pollu-
tion in the soil samples. Moreover, we should illustrate that the
carcinogenic risks of Cr were notably far from the threshold
value, which is 1.0E − 04, and hence, the carcinogenic risk
caused by soil heavy metals should be neglected. Special at-
tention may be paid to other risk aspects rather than carcino-
genic risks.

child

adult

Fig. 6 Noncarcinogenic risk with inhalation and dermal contact caused by the eight soil heavy metals from 28 samples (containing adults and children)
27102 Environ Sci Pollut Res (2018) 25:27090–27105

Fig. 7 Potential carcinogenic risks through inhalation and dermal contact both for adults and children in the BAO steel industrial soil (contain caused by
arsenic (As), chromium (Cr), cadmium (Cd), and nickel (Ni))

Table 8 Worldwide concentrations of heavy metals in the soil of the steel industrial area (mg kg−1)

Area Hg As Pb Zn Cu Cr Cd Ni References Nation

Smederevo 0.8–3.0 – 42–57 29–58 57–121 50–58 – – (Dragovic et al. 2014) Serbia
Balanagar 0.4 – 3.42–6.03 – 2.32–3.96 1.06–2.40 0.09–0.18 1.26–2.16 (Machender et al. 2011) India
Lenjanat – – 19–69 1.89–2.70 – – – – (Mohajer et al. 2013) Iran
Balanagar 0.02–0.12 – 139–264 12–147 31–87 66–238 – 28–240 (Machender et al. 2014) India
Queen – – 14.4–19.1 – 10.9–22.1 – – (Al-Khashman and Shawabkeh Jordan
Alia 2009)
Newcastle 0.08–0.3 – 77–898 83.8–143 – – 0.7–2.2 – (Harvey et al. 2017) Australian
Osnabruck – – – 53–110 210–270 40–140 – 40–80 (Meuser and Blume 2001) Germany
Fashina 0.11–0.14 – 27.6–122 – – – – – (Isola et al. 2015) Nigeria
Aviles – – 110–220 86–570 20–403 65–264 0.06–3.94 – (Ordonez et al. 2015) Spain
Sinos – 1.32 41.57 119.86 28.01 22.89 0.59 25.36 (Schneider et al. 2014) Brazil
Alps 0.32–7.02 – 91.3–751 83.8–143 21.1–39.9 22.9–86.7 – 23.1–49.0 (Gallini et al. 2018) Italian
Zabrze – – 36.8–148 75–271 9.6–43.7 35.7–98.8 0.005–0.25 18.1–63.4 (Rachwal et al. 2015) Poland
Toulouse 1.70–9.60 – 22.3–89.4 48.7–117 11.9–42.4 18.8–216 0.01–0.04 46.5–152 (Lecoanet et al. 2003) France
Anshan – – 45.1 213 52.3 69.9 0.86 33.5 (Xiao et al. 2015) China
Our study 0.22 0.95 190.8 220.8 32.17 156.1 0.42 31.67 China

– not applicable
Environ Sci Pollut Res (2018) 25:27090–27105
The implication for pollution and risk control
Although BAO steel is a traditional iron and steel enterprise
that is categorized as a Bthree high^ (high pollution, high en-
ergy consumption, and high emission) industry, the soil heavy
metal pollution may need special attention. As China’s only
iron-steel joint enterprise near the sea, the construction, oper-
ation, and management of BAO steel have attached great im-
portance to environmental protection compared with other
iron and steel industries, such as Anshan Iron and Steel in
China (Xiao et al. 2015; Zong et al. 2016). Moreover, other
industrial steel areas were previously studied by other re-
searchers throughout the world, and the concentrations in
these areas are listed in Table 8. Although the BAO steel
industry is causing pollution during the process of production,
the overall pollution and risk levels can be controlled by tak-
ing the following measures during the production process. (1)
Ensure that the production process flows better during the
traditional production of steel to reduce the consumption of
energy. (2) Use the latest environmental protection facilities to
address and take advantage of various types of heavy metal
pollutants during the production process. (3) To control pol-
lution from the BAO steel industry, the renovation projects on
coal-fired units that aim to adapt to the ultra-low emission
standards should be completed before the deadline. (4) The
balance between energy consumption and environmental pro-
tection should be taken into consideration during the process.
(5) While continuing to enrich the management tools for emis-
sion reduction, the comprehensive efficiency of pollution con-
trol facilities also needs to be increased from the aspects of
operation management, equipment maintenance, and techni-
cal improvement. (6) Transform traditional docks by promot-
ing technical upgrades of a fully automated unmanned yard
wharf to avoid pollution and reduce the concentrations of Pb
pollution in soil.
Concluding remarks
The mean contents of Zn, Cr, Pb, Cd, Cu, and Hg are more
than the reference index values for Shanghai, suggesting an
enrichment of these metals in the soils around the BAO steel
industry, especially for Hg and Pb. The identification of pos-
sible sources of the eight heavy metals in industrial soils
showed that they came from three different sources. For ex-
ample, Cd, Zn, Cu, and Cr were closely related to iron and
steel production, and Pb was mainly related to fuel (especially
gasoline). Hg was caused by exhaust emissions from coal
combustion of a heating supply plant. The ecological risk
values suggest that Hg, Cd, and Pb exposed high and consid-
erable ecological risks. In addition, the health risks of heavy
metals caused by inhalation are more severe than those
brought through dermal contact with a human being.
27103
Children have higher noncarcinogenic health risks than adults,
as the values of the noncarcinogenic health risk levels for
children were higher than those for adults, indicating that chil-
dren are sensitive to noncarcinogenic risks. On the other hand,
serious carcinogenic risks do not currently exist at the BAO
steel industry. In particular, the cancer risk is lower than 1.0E
− 04 in all areas of BAO steel. This study concludes that the
soil heavy metal pollution in the BAO industry is due to ex-
ternal factors or immigration and not the environmental back-
ground; however, the pollution is also derived from the indus-
trial production processes.
Funding This work was financially supported by the National Key R&D
Program of China (Grant No. 2017YFC0505701), the National Natural
Science Foundation of China (Grant No. 31370482), and the project of
Bremote sensing survey and basic ecological information system con-
struction of BAO steel industry^ from BAO steel industry.
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