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Chemosphere: Rui Zhang, Tao Chen, Yu Zhang, Yuhao Hou, Qingrui Chang
Chemosphere: Rui Zhang, Tao Chen, Yu Zhang, Yuhao Hou, Qingrui Chang
Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere
h i g h l i g h t s g r a p h i c a l a b s t r a c t
a r t i c l e i n f o a b s t r a c t
Article history: The accumulation of heavy metals (HMs) in the soil poses a threat to human health. In this study, 62 pairs
Received 13 January 2020 of topsoil and wheat grain samples were collected from a typical industrial park in northwest China, and
Received in revised form the human health risks associated with cadmium (Cd), chromium (Cr), copper (Cu), mercury (Hg), nickel
10 March 2020
(Ni), lead (Pb) and zinc (Zn) were assessed through multiple exposure pathways. Meanwhile, the
Accepted 21 March 2020
Available online 24 March 2020
contribution of different environmental factors and their interactions were explored by using geo-
detector. Results showed that Cd concentration in the soil ranged from 0.307 to 2.491 mg kg1, with a
Handling Editor: A. Gies median value of 0.588 mg kg1, and almost half of the samples exceeded the pollution threshold. In
comparison, other elements in the soil were below their mandatory thresholds. However, it is note-
Keywords: worthy that in addition to the median Cd concentration in wheat grains of 0.062 mg kg1 (0.018
Heavy metals e0.246 mg kg1), the Pb concentration also reached 0.2 mg kg1 (0.1e0.7 mg kg1), with a sample over-
Health risk assessment standard rate of 48.39%. In addition, the health risk assessment results showed that the average total
Dietary exposure hazard index (HIt) for adults and children was 1.22 and 1.53, and the total carcinogenic risk (TCRt) was
Geo-detector
7.0 104 and 2.32 104, respectively, both above acceptable criteria. Dietary intake was the main
Industrial park
route of exposure. Among various factors, distance from industrial enterprises, altitude, and soil pH,
distance from major roads were the most influential contributors. Their interactions were more prom-
inent than the effects of single factors and this synergy deserves attention.
© 2020 Elsevier Ltd. All rights reserved.
https://doi.org/10.1016/j.chemosphere.2020.126591
0045-6535/© 2020 Elsevier Ltd. All rights reserved.
2 R. Zhang et al. / Chemosphere 252 (2020) 126591
Table 1
Statistical summary of heavy metal concentrations (mg kg1) in soil and wheat, and soil pH and OM (g kg1).
Elements Mean ± S.D. Min. Max. Median CV % Background valuesa Threshold valuesb
Elements Mean ± S.D. Min. Max. Median CV % Number of grain samples Threshold valuesc
over threshold (percent)
body weight (kg); AT, the average exposure time (days); SA, the (Cao et al., 2015). The acceptable risk for regulatory purposes is in
surface area of the skin exposed to pollutants (cm2); AF, the skin the range from 1.0 106 to 1.0 104 (USEPA, 2004).
adherence factor (mg (cm2 h)1); ABS, the dermal absorption factor
(unitless); IRi, the inhalation rate (m3 day1); PEF, the emission
factor (m3 kg1). Detailed parameter values are listed in Table S1. 2.6. Geo-detector analysis
The potential non-carcinogenic risk was quantified using Haz-
ard Quotients (HQ, unitless), as proposed by USEPA (1989). HQ is a Geo-detector is used to measure the spatial stratification het-
ratio of the estimated ADI to reference dose (RfD), as follows: erogeneity of dependent variable Y, and to explore how indepen-
dent variable X explains the spatial pattern of Y (Wu et al., 2016). Its
ADIij main principle is to investigate whether the spatial distributions of
HQ ¼ (8) Y and X tend to be the same. The more identical, the higher the
RfD
association is between them, which can be characterized by q
where i, the number of metal elements; j, the number of exposure statistic, defined as follows (Wang et al., 2016):
pathways; RfD, reference dose of each metal under different
exposure routes (Table S2). The Hazard Index (HI, unitless) refers to 1 XL
q¼1 N s2 (11)
the sum of more than one HQ for multiple substances and/or Ns h¼1 h h
2
multiple exposure pathways (USEPA, 2002).
X where q is the power determinant of each factor for the health risk,
HI ¼ HQ (9)
N is the number of samples, Nh refers to the number of samples in
For each HM, the HQ for all exposure routes can be summed to each category, and L represents the number of classification cate-
obtain the overall risk of an individual metal (HIi). Similarly, a gories. The s2 stands for the variance of Y and s2h is the variance for
hazard index HIj can account for the cumulative risk of all HMs each classification category Y. For q2[0,1], q ¼ 1 means that Y is
under a specific exposure pathway (Singh et al., 2018). The total completely determined by X, q ¼ 0 indicates that there is no as-
hazard index (HIt) was used to assess the total health risk posed by sociation between X and Y, and the q value indicates that X can
multiple metals under multiple exposure routes. If HQ or HI(x) explain 100 q% of Y. In this model, X must be a categorical vari-
is 1, the assumption is that there are no significant risks of non- able. If not, it needs to be discretized based on expert knowledge or
carcinogenic effects. In contrast, non-carcinogenic risks are likely to a categorization algorithm (Wang et al., 2010). The optimal
occur (USEPA, 2011). numbers of categorization were determined by the maximum q
The carcinogenic risk (CR) index is the probability of an indi- value and the corresponding p value used in significance test
vidual developing any type of cancer over a lifetime due to carci- (Wang et al., 2016).
nogenic exposure, as follows: In geo-detector model, the interaction detector is defined to
study the interactive effects between two factors (symbolized by ∩)
CR ¼ ADI SF (10) by comparing q (X1∩X2) with q (X1) and q (X2). X1∩X2 represents a
new stratum created by overlaying X1 and X2 (Shi et al., 2018). If q
where SF is the cancer slope factor of each metal under different (X1∩X2) ¼ q (X1) þ q (X2), then the two factors are independent of
exposure routes, as shown in Table S2. In this study, only Cd, Cr, Ni each other; if q (X1∩X2) > q (X1) þ q (X2), then the two factors
and Pb were treated as potential carcinogenic contaminants to nonlinearly enhance each other; if Max (q (X1), q (X2)) < q
calculate CR. Similar to HI(x), on the assumption that hazardous (X1∩X2) < q (X1) þ q (X2), then the two factors bi-enhance each
risks are additive, the CR for all carcinogens and/or all exposure other (Wang et al., 2010). Detailed principles can be found in
routes can be summed to different forms total cancer risk (TCR(x)) published literatures (Qiao et al., 2019; Wang et al., 2016).
R. Zhang et al. / Chemosphere 252 (2020) 126591 5
2.7. Data source and processing of influencing factors suggesting that they were at uncontaminated levels. However, the
PI value of Cd ranged from 0.51 to 4.15, indicating the presence of
Thirteen environmental factors were explored in this study. pollution. Specifically, 9.68% of sampled soils were moderately to
Among them, human activity factors are: distance from thermal severely contaminated with Cd, while 38.71% slightly polluted. This
power plant (DTPP), distance from LeadeZinc smelting plant eventually led to the SPI values higher than 1 in nearly a quarter of
(DLZSP), distance from coal chemical enterprise (DCCP), distance soil samples.
from main roads (DMR), distance from villages (DV) and road High HM concentrations in soil may pose a high risk of
density (RD); natural factors include: elevation (E), aspect (A) and contamination to crop growth. As can be seen from Table 1, Cd
slope (S), as well as soil pH, OM, soil type (ST) and Normalized concentration in wheat grains ranged from 0.018 to 0.246 mg kg1,
Vegetation Index (NDVI). Soil data came from the survey results of with a median value of 0.062 mg kg1, of which 22.58% of the
cultivated land quality in Shaanxi Province. Terrain parameters samples exceeded the maximum allowable concentration (MAC) of
were derived from DEM data (10 m) generated from a 1:50,000 0.1 mg kg1. Although Pb concentration in soil was below the
topographic map. Moreover, Sentinel-2 images acquired on May 12, pollution standard, its concentration in 48.39% of wheat grains
2018 were used to extract NDVI data. In ArcGIS, DTPP, DLZSP, DCCP exceeded the mandatory threshold of 0.2 mg kg1 (ranging from 0.1
and DMR were calculated by distance function, DV was obtained by to 0.7 mg kg1 with a median of 0.2 mg kg1). The highest Pb
buffer function, and RD was acquired by line density function. concentration in grains was about 3.5 times that of MAC. These may
Meanwhile, the natural breaks method was used to convert be attributed to the high availability and bio-accessibility of Pb in
continuous data into categorical data. Detailed rules are shown in the soil, which can be seen in Table S4. In this study, the average
Table S3. concentration of soil DTPA-extractable Pb reached 4.92 mg kg1
Descriptive statistics were implemented in SPSS 25. Maps were (ranging from 2.18 to 23.1 mg kg1), and the average bioavailability
produced with ArcGIS 10.3. Geo-detector software was used to was 11.16% (Max. ¼ 20.56%). Moreover, no excess Hg, Cr, Cu, Ni and
calculate the contribution of each factor, which could be down- Zn were observed in wheat grains in this study. Overall, wheat
loaded from http://www.geoddetector.org. cultivation in the area was mainly threatened by soil Pb and Cd
pollution.
3. Results and discussion
3.2. Health risk analysis
3.1. Summary statistics of heavy metal in soil and wheat
3.2.1. Non-carcinogenic risk assessment
As shown in Table 1, the median concentrations of Cd, Cr, Cu, Hg, The results for non-carcinogenic risks are shown in Table 3 and
Ni, Pb and Zn were 0.588 mg kg1, 68.2 mg kg1, 29.1 mg kg1, Fig. 2. The average HIt for adults and children was 1.22 and 1.53,
0.1018 mg kg1, 36.6 mg kg1, 37.95 mg kg1 and 97.5 mg kg1, respectively. For adults, 80.65% of the samples had HIt values
respectively. Compared with their background values, the average greater than 1, while for children, the proportion rose to 100%,
growth rate ((Median e Background value)/Background meaning that most residents in the area were at non-carcinogenic
value 100%) was ranked as follows: Cd (526%) > Hg (239%) > Pb risk associated with soil HMs. By contrast, the HIt for children was
(77%) > Zn (40%) > Cu (36%) > Ni (27%) > Cr (9%). Their mean EFs higher than that for adults, indicating that children were more
were 7.60, 3.87, 1.97, 1.50, 1.40, 1.31 and 1.10, respectively (Table 2). susceptible to adverse effects. The phenomenon has also been
The EFs of Cr, Cu and Ni in all soil samples were less than 2, indi- found elsewhere (Chen et al., 2018; Fan and Wang, 2017). The cause
cating only minimal enrichment. However, 64.52% and 20.97% of may be special behavior and physiological characteristics of chil-
the samples were significantly enriched for Cd and Hg, respectively. dren, such as pica, finger sucking, high respiration rate, etc. (Cheng
Besides, a moderate enrichment was observed for Pb in nearly one- et al., 2018).
third of samples. Overall, the significant increase of Cd, Hg and Pb in The contribution of different pathways and metals to non-
the topsoil relative to background levels deserves our attention. carcinogenic risk was similar between adults and children, so
According to national control standards, the PI values of Cr, Cu, only adult health risks were discussed here. From Fig. 2, it can be
Hg, Ni, Pb and Zn in all soil samples were below 0.7 (Table 2), found that dietary pathway contributed over 90% of non-
Table 2
Statistical summary of EFs and pollution assessment.
Metal Mean ± Std. Min. Max. Number (and percentage) of samples with different categories
Metal Mean ± Std. Min. Max. 0.7 0.7e1 1e2 2e3 >3
Table 3
Results of non-carcinogenic and carcinogenic risk of different pathways and elements.
Mean value for Adults (Min.Max.) Mean value for Children (Min.Max.) Mean value for Adults (Min.Max.) Mean value for Children (Min.Max.)
The mean value is in bold and black font, and the maximum and minimum values are normal font.
carcinogenic risk for adults, followed by soil ingestion, dermal 2e4 orders of magnitude higher than that of three non-dietary
contact and inhalation routes. The HIj value via food intake ranged exposure pathways. Thus, the consumption of home-grown crops
from 0.698 to 1.91, whereas the mean HIj values for soil ingestion, may be an important pathway for HM exposure in the area. This is
dermal contact and inhalation were only 0.058, 0.00782, and consistent with the findings in Kermanshah (Iran), Luanda
0.00051, respectively. In comparison, HIj of dietary intake route was (Angola), Huludao and Tianjing (China) (Doabi et al., 2018; Ferreira-
R. Zhang et al. / Chemosphere 252 (2020) 126591 7
Baptista and De Miguel, 2005; Ma et al., 2018; Zheng et al., 2010). distributed at the intersection of three enterprises, especially near
Moreover, compared with previous studies in the region, their the LZSP (position A), whereas lower HIt and TCRt were located far
estimated non-carcinogenic risks were significantly under- away from them. This reflects to some extent the impact of in-
estimated due to the neglect of dietary intake effects (Fan and dustrial activities on human health risks. Moreover, it could also be
Wang, 2017). Therefore, attention should be paid to the impor- found that high HIt or TCRt were mainly scattered in low altitude
tance of dietary exposure in future risk management. areas. Considering the local prevailing wind direction and terrain
In addition, it was also found from Table 3 that the average HIi of features, we inferred that the topographical conditions of the area
a single HM was as follows: Zn > Cu > Cr > Cd > Pb > Ni > Hg, which may also be an important factor in controlling the distribution of
was basically consistent with the research results of Yang et al. health risks.
(2019). Zn, Cu and Cr was the largest contributors, accounting for In this study, it should also be noted that although the human
24.96%, 23.21% and 19.34% of the total non-carcinogenic risk for health risks calculated using the total metal concentrations were
adults, respectively (Fig. 2C). Moreover, Ni and Hg had the least risk, not very high in the three non-dietary pathways, the results may
contributing less than 2%. Despite the high accumulation of Cd and still be overestimated. As can be seen from Table S4, except Pb and
Pb in wheat grains, the contribution of these two metals to the total Cd, the DTPA extraction of other metals was very low in this study,
risk was only about 15%, respectively. For children, the contribution with the average bioavailability less than 5%. Considerable metal
of individual metals to HIt was similar to that of adults. Overall, fractions adhere to the soil, with little harm to human health. Thus,
exposure to a single metal did not pose a significant health risk to the use of total metal indicators to estimate risk may lead to more
residents of this region. However, the combined effects of multiple aggressive governance measures.
metals cannot be ignored.
3.3. Influencing factor analysis
3.2.2. Carcinogenic risk assessment
The assessment results of carcinogenic risks are listed in Table 3 The results of various factors are shown in Table 4. Factors such
and Fig. 3. From Table, the average TCRt was 7.0 104 for adults as A, OM, NDVI, RD, DV, and ST did not pass the significance test
and 2.32 104 for children, both higher than the results of Yang (a ¼ 0.05), indicating their negligible influence. Meanwhile, slope
et al. (2019) in the region. The reason may be that in their study, (S) also had no significant effect on children’s HIt. In comparison,
a large number of samples from non-industrial areas pulled down the main influencing factors were DLZSP, DTPP, DCCP, E, pH, and
the overall risk level. Furthermore, TCRt of adults was 3 times that DMR.
of children, which was also different from the situation in Iran’s In geo-detector analysis, q statistic can characterize the influ-
Kermanshah agricultural region (Doabi et al., 2018). Higher TCRt for ence degree of each factor. In this study, the contribution of various
adults may be associated with longer exposure times and more factors for HIt was as follows: DLZSP (0.335e0.342) > DTPP
wheat intake. In addition, similar to non-carcinogenic risk, the (0.304e0.308) > DCCP (0.277e0.283) > E (0.255e0.272) > pH
main exposure route for carcinogenic risk in this study was still (0.155e0.157) > DMR (0.077e0.081) > S (0.075e0.078) > other
diet, much higher than non-dietary exposure. For each metal, factors (<0.063). However, for TCRt, the influence of elevation
children’s TCRi were generally within acceptable range (Fig. 3), increased significantly: DLZSP (0.340e0.347) > E
indicating no significant carcinogenic risk. However, the mean TCRi (0.329e0.332) > DTPP (0.306e0.310) > DCCP (0.223e0.224) > pH
values of Cd and Ni for adults were 3.35 104 and 2.54 104, (0.129e0.132) > S (0.084e0.085) > DMR (0.063e0.065) > other
accounting for 47.82% and 36.25% to TCRt, respectively. This means factors (<0.063). As can be seen from this, the distance factors
that about 3 per 10000 adults are at risk of cancer caused by Cd or associated with industrial activities are the most important. Among
Ni pollution. As for Cr, the average TCRi for adults was only them, DLZSP obtained the highest q, followed by DTPP and DCCP.
1.10 104, slightly above acceptable criterion. Overall, the long- This indicated that PbeZn smelting had the greatest impact on the
term health effects for children are not serious at current single health of residents. Moreover, E contributed about 26% to HIt and
metal level, but adults should pay more attention to the carcino- 33% to TCRt, implying an important natural factor. This can be
genic effects of Cd and Ni. observed intuitively from Fig. 4. Soil pH was another major natural
The HIt and TCRt at each sampling site were mapped, as shown factor, contributing about 16% and 13%, respectively. It is well
in Fig. 4. It was found that higher HIt and TCRt were mainly known that pH affects not only the solubility and mobility of HMs in
soil, but also their availability and toxicity to plants (Bravo et al.,
2017; Lu et al., 2018). Thus, it is not difficult to understand why
pH has an important effect on HIt and TCRt in this study. And be-
sides, soil OM can also affect the activity of HMs through adsorption
and complexation mechanisms (Kwiatkowska-Malina, 2018).
However, no significant effect of OM on HIt or TCRt was found in this
study, which was different from the results of Wang et al. (2018)
and Lu et al. (2018). The reason may be attributed to the differ-
ences in the local soil organic matter composition and weak alka-
line features.
The results of the interaction between any two factors are
shown in Table S5. Generally speaking, interactions can be greater
than, equal to, or less than the sum of the effects of two single
factors (Qiao et al., 2019). The first case is of the greatest concern. In
this study, except DLZSP∩DCCP, DLZSP∩DTPP and DLZSP∩pH, the
interaction of any two factors affecting HIt for Adults was greater
than their sum. Similarly, in addition to the effects of DLZSP∩DCCP
on HIt (for children) and DLZSP∩E on TCRt (for adults and children),
the interaction between other factors was also nonlinearly
Fig. 3. Cancinogenic risk of different metals for adults and children. enhanced. This suggested that the impact on health risk is not a
8 R. Zhang et al. / Chemosphere 252 (2020) 126591
Table 4
The contribution (q statistics) of different factors to HIt and TCRt.
Influencing factors HIt for Adults HIt for Children TCRt for Adults TCRt for Children
simple cumulative result of a single factor, but rather a synergistic small in the above analysis, DLZSP∩OM still yielded a high
effect of multiple factors. nonlinear interaction effect (q ¼ 0.67). In addition, the nonlinear
To highlight the interactive impact of major human activities in interaction of DLZSP∩DTPP also contributed more than 70% to TCRt
the region, all interactions related to DCCP, DLZSP and DTPP were (q ¼ 0.717 for adults and 0.718 for children), which indicated that
compared (Table S5). Results showed that DCCP∩E and DTPP∩E the synergistic effect between PbeZn smelting and thermoelectric
obtained the highest nonlinear interaction q values, indicating that production significantly increased the long-term carcinogenic
the combination of coal chemical (or thermoelectric) production impact of soil HMs on the local population. In summary, HIt or TCRt
with altitude factor greatly enhanced the impact of soil HMs on was influenced by both human and natural factors, but the inter-
human health. Although the effect of soil OM on HIt was found to be action between factors was more important than single factors.
R. Zhang et al. / Chemosphere 252 (2020) 126591 9
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