Science of the Total Environment 521–522 (2015) 144–151

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Science of the Total Environment

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Concentration and transportation of heavy metals in vegetables and risk

assessment of human exposure to bioaccessible heavy metals in soil near
a waste-incinerator site, South China
Ning Li, Yuan Kang ⁎, Weijian Pan, Lixuan Zeng, Qiuyun Zhang, Jiwen Luo
School of Chemistry & Environment, South China Normal University, Higher Education Mega Center, Guangzhou 510006, China
Guangdong Technology Research Center for Ecological Management and Remediation of Urban Water System, School of Chemistry & Environment, South China Normal University, Higher Educa-
tion Mega Center, Guangzhou 510006, China
Key Laboratory of Theoretical Chemistry of Environment, Ministry of Education, School of Chemistry & Environment, South China Normal University, Higher Education Mega Center, Guangzhou
510006, China

H I G H L I G H T S

• Similar pattern of heavy metal in settled air particle and aerial parts of vegetables
• Leaf lettuce accumulated the highest heavy metals concentrations
• The bioaccessibility of heavy metals in soil ranged from 2% to 71.78%.
• Cd and Pb in soil resulted in the highest non-cancer risk.
• Cd resulted in unacceptable cancer risk for children and risk.

a r t i c l e i n f o a b s t r a c t

Article history: There is limited study focusing on the bioaccumulation of heavy metals in vegetables and human exposure to bio-
Received 6 December 2014 accessible heavy metals in soil. In the present study, heavy metal concentrations (Cr, Ni, Cu, Pb and Cd) were mea-
Received in revised form 8 March 2015 sured in five types of vegetables, soil, root, and settled air particle samples from two sites (at a domestic waste
Accepted 20 March 2015
incinerator and at 20 km away from the incinerator) in Guangzhou, South China. Heavy metal concentrations
Available online 30 March 2015
in soil were greater than those in aerial parts of vegetables and roots, which indicated that vegetables
Editor: Charlotte Poschenrieder bioaccumulated low amount of heavy metals from soil. The similar pattern of heavy metal (Cr, Cd) was found
in the settled air particle samples and aerial parts of vegetables from two sites, which may suggest that foliar up-
Keywords: take may be an important pathway of heavy metal from the environment to vegetables. The highest levels of
Waste incinerator heavy metals were found in leaf lettuce (125.52 μg/g, dry weight) and bitter lettuce (71.2 μg/g) for sites A and
Heavy metals B, respectively, followed by bitter lettuce and leaf lettuce for sites A and B, respectively. Swamp morning glory
Bioaccessibility accumulated the lowest amount of heavy metals (81.02 μg/g for site A and 53.2 μg/g for site B) at both sites.
Risk assessment The bioaccessibility of heavy metals in soil ranged from Cr (2%) to Cu (71.78%). Risk assessment showed that
Cd and Pb in soil samples resulted in the highest non-cancer risk and Cd would result in unacceptable cancer
risk for children and risk. The non-dietary intake of soil was the most important exposure pathway, when the bio-
accessibility of heavy metals was taken into account.
© 2015 Elsevier B.V. All rights reserved.

1. Introduction important factor restricting economic and social sustainable develop-

ment. After 1988, waste burning was rapidly developed in our country
With the rapid increase of urbanization, great concerns have been (Chen, 2004). Municipal wastes such as leather waste shavings were
raised regarding the waste incinerators due to their potential impacts likely to contain toxic heavy metals (e.g. cadmium and chromium)
on the environment by the toxic chemicals emitted from incomplete The heavy metals were converted to their oxide or chloride forms dur-
combustion (Wang et al., 2008). Waste disposal has become an ing combustion process, and the heavy metal compounds were able to
volatilize and be carried out of the incinerator device with the hot flue
⁎ Corresponding author at: School of Chemistry & Environment, South China Normal
gases due to the high combustion temperature (Louhab and Akssas,
University, Higher Education Mega Center, Guangzhou 510006, China. 2006; Lu-shi et al., 2004). The burning activities have resulted in high
E-mail addresses: [email protected], [email protected] (Y. Kang). levels of pollution in the ambient environment and have further

http://dx.doi.org/10.1016/j.scitotenv.2015.03.081
0048-9697/© 2015 Elsevier B.V. All rights reserved.
 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151 145

threatened the local ecosystem and the health of surrounding inhabi- treat the flue gas in the waste incinerator. Site B is a less contaminated
tants. Emission is one of the important pathways for these chemicals en- area (about 20 km away from the incinerator; located in the upward di-
tering the environment. It is known that serious systemic health rection of the prevailing wind flow, and not directly exposed to industri-
problems will be caused as a result of excessive accumulation of dietary al or municipal emissions). Vegetables grown in these two sites are
and non-dietary heavy metals in the human body (Oliver, 1997; Chen, supplied to local markets.
2004). The prolonged consumption of unsafe concentrations of heavy At site A, five representative vegetable species, including leaf mus-
metals through foodstuffs may lead to the chronic accumulation of tard (Brassica juncea), leaf lettuce (Lactuca sativa L.), morning glory
heavy metals in the kidney and liver of humans causing disruption of (Ipomoea aquatica Forsk), lettuce (Mylopharyngodon), and bitter lettuce
numerous biochemical processes, leading to cardiovascular, nervous, (Cichorium endivia) were collected (n = 45). At site B, three vegetable
kidney and bone diseases (Jarup, 2003; Ali and Al-Qahtani, 2012). species, including leaf mustard (B. juncea), morning glory (I. aquatica
Some heavy metals such as Cu, Zn, and Ni act as micronutrients for Forsk), and bitter lettuce (C. endivia) were collected (n = 27). The
the growth of human beings when present in trace quantities, whereas exposure time and vegetative phase of these vegetables was about
others such as Cd, As, Pb, and Cr act as carcinogens (Feig et al., 1994; 3–4 months. The sample collection was described in detail in our
Trichopoulos, 1997) previous work (Zeng et al., 2014). Each rhizosphere soil or vegetable
Nowadays, many studies for calculating non-cancer risks from expo- sample was a composite of three subsamples. For rhizosphere soil
sure through the ingestion pathway are based on bioaccessible part of collection, when the vegetables were removed from the soil, they
pollutants instead of total concentration (Hu et al., 2012; Luo et al., were gently shaken to remove soil loosely adhering to the roots.
2012; Read et al., 2015). The total heavy metal concentrations only pro- The remaining adherent soils were separated from the roots as rhizo-
vide very limited information about their chemical behavior and poten- sphere soil. Three settled air particle samples were collected from
tial fate (Mench et al. 2006), whereas the bioaccessible fractions give the cement surface of a small house roof at each sampling site by a
results that are much closer to the actual risks involved. The bioaccessi- vacuum cleaner. Settled air particles on the cement surface located
ble fraction that can act as a toxicant in humans is the fraction of the in the vegetable garden may represent settled air particles on the
ingested dose that crosses the gastrointestinal epithelium and becomes vegetable leaves. All samples were wrapped with aluminum foil,
available to be distributed to internal target tissues and organs (Ruby, put into polythene zip-lock bags, and transported to the laboratory.
1993). The physiologically based extraction test (PBET) is commonly Afterward, the vegetable samples were thoroughly washed with
used in the scientific literature to simulate stomach and intestine liquids running tap water to remove airborne dust and soil particles. The
to evaluate the bioaccessibilities of pollutants in the human gastrointes- roots and aerial parts of vegetables were separated. Rhizosphere
tinal system (Tao et al., 2014). soil samples were air dried at room temperature and ground in a
A number of studies have reported levels of heavy metal contamina- grinder sufficiently to pass through a 2-mm sieve. Fine roots and ae-
tion in soil, sediment, and biota samples from open burning sites (Cao rial parts of vegetables were freeze-dried and ground with agate
and Hu, 2000; Nan et al., 2002; Singh et al., 2004; Mahmood and mortar. The settled air samples were sieved by a 100-μm mesh. All
Malik, 2014). Some studies indicated that air particle contributed to samples were kept frozen at − 18 °C until analysis.
heavy metals accumulation by plants (Sapkota and Cioppa, 2012;
Schreck et al., 2013). In the present study, we (1) measured the heavy 2.2. Determination of heavy metals
metal concentrations in settled air particles, rhizosphere soils, roots,
and vegetables, (2) investigated the contribution of settled air particles For all samples, 0.5 g of dried sample was digested with 15 mL of
and soil to heavy metal uptake in vegetables, and (3) performed risk as- HNO3 and HCl with 1:1 ratio at 90 °C until a transparent solution was
sessment of human exposure to heavy metals via non-dietary intake of obtained. The solution was filtered through Whatman No. 42 filter
soil considering the bioaccessibility. This provides a basis for guiding paper and the filtrate was diluted to 50 mL with distilled water.
further activities aimed at preventing excessive exposure of humans The concentrations of heavy metal in all samples were determined
through monitoring and control of amelioration of uptake to plants. with an atomic absorption spectrophotometer (Perkin-Elmer model
2130, USA) fitted with a specific lamp of a particular metal using appro-
2. Materials and methods priate drift blanks. Quality control measures were taken to assess the
contamination and reliability of data. Blank and drift standards were
2.1. Sampling run after three determinations to calibrate the instrument. The coeffi-
cient of variation of replicate analysis was determined for different
The samples, including soil, vegetables, and settled air particulates, determinations and for precision of analysis. Variations were found to
were collected from two sites in Guangzhou in July 2012. There is a sub- be less than 10%. Precision and accuracy of analysis were also ensured
tropical monsoon climate in Guangzhou. Site A is close to (b 0.5 km; through repeated analysis of samples, and standard reference material
located in the downward direction of the prevailing wind flow) a of the vegetables (GBW10015: spinach) and soils (GBW07430 (GSS-
domestic waste incinerator. The capacity of incinerator is about 16): soil from Pearl River Delta) for all the heavy metals. The recovery
346,660 t/y. The Selective Non-Catalytic Reduction (SNCR) Denitration of heavy metals in standard reference material of vegetables and soils
technology and Fly Ash Solidification technology are employed to ranged from 82% (Cd) to 114% (Pb).

Table 1
Heavy metal concentrations (μg/g dry weight) of soil, aerial parts of vegetables and roots from site A.

Samples Cr Cd Pb Cu Ni

Soil Mean 285.07 62.09 14.95 13.53 10.09

Median 283 63.45 15 13.8 9.1
Range 215–358 45.55–91 11.87–21.78 7.09–21.36 8–15.04
Aerial parts of vegetables Mean 55.68 11.69 27.65 7.65 24.72
Median 39.5 7 29.55 7.42 22.8
Range 24.50–60 3.25–15.75 9.3–45.8 3.92–11.67 7.8–38.55
Roots Mean 41.4 8.52 19.66 33.41 9.77
Median 52.71 9 16.75 35.87 9.84
Range 19.71–68.04 7–19.5 2.75–33.25 5.87–62.12 4.84–15.84
146 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151

Table 2
Heavy metal concentrations (μg/g dry weight) of soil, aerial parts of vegetables and roots in site B.

Samples Cr Cd Pb Cu Ni

Soil Mean 18.31 9.96 5.91 2.21 5.6

Median 12.75 6.85 5.03 1.5 5.95
Range 1–41.5 0.9–33.9 3.88–9.98 0.8–5.4 2.7–8.1
Aerial parts of vegetables Mean 24.63 7.21 24.84 2.31 13.16
Median 23.25 7.12 27.63 2.28 13
Range 18–31.5 6.5–8.25 12.25–30.75 0.65–3.65 8–16.75
Roots Mean 38.87 3.46 5.68 10.5 8.69
Median 31.63 3.63 4.81 10.75 7.92
Range 14.06–72 2.5–4.25 3.82–8.05 9.75–12.5 7.83–12.83

2.3. Physiologically based extraction test a shaker at 37 °C for 4 h. The simulated extracts of stomach phase
(GP) and intestine phase (IP) were filtered through 0.45 μm membrane
Bioaccessibility of heavy metals was estimated using the in vitro gas- filters and their pH values were kept within 0.5 pH units of the initial pH
trointestinal (IVG) method with modification (Kang et al., 2011; Man at all times. The filtrates were stored in a refrigerator at 4 °C until anal-
et al., 2010; Rodriguez et al., 1999). The IVG method is a two step se- ysis. The bioaccessibility (BA,%) of each heavy metal in samples from
quential extraction: gastric and intestinal extraction. A simulated stom- two sites was calculated using Eq. (1) (Lu et al., 2011).
ach liquid was made by dissolving 5 g pepsin, 2 g citrate, 2 g malate,
1.68 mL lactic acid, and 2 mL acetic acid in 4 L distilled water. A 1.0 g al-
iquot of a sample was added to 100 mL of the simulated stomach liquid, CIV VIV
BA% ¼  100% ð1Þ
then the mixture was placed in shaker at 37 °C for 1 h. The pH of the CS MS
mixture was adjusted to 1.5 with concentrated HCl. A 20 mL aliquot of
the solution was then adjusted to pH 7.0 with a saturated aqueous where CIV is the extractable heavy metal in the GP or the IP (mg L−1);
NaHCO3 solution, then 0.18 g bile salts and 0.06 g pancreatin were VIV is the volume of the extractant in the reaction vessel (L); Cs is the
added to simulate the intestinal liquid, and the mixture was placed in total heavy metal concentration in the samples (mg kg−1); Ms is the

Fig. 1. The relationships between heavy metal (Cu, Cr, Ni, and Pb) concentrations (μg/g dry weight) in soil.
 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151 147

0.60 adults and 200 mg day−1 for children), InhR is the inhalation rate
aerial parts of vegetable
0.55
air particle
(20 m3 day−1 for adults and 10 m3 day−1 for children), EF is the
0.50 exposure frequency (250 days year−1 for adults and 350 days year−1
0.45 for children), ED is the exposure duration (25 years for adults and
0.40 6 years for children), BW is the average body weight (70 kg for adults
0.35 and 15 kg for children), AT is the averaging time (AT = ED × 365 days
Percentage

0.30 for noncarcinogens and AT = 25,550 days for carcinogens), SA is the sur-
0.25
face area of the skin that the contaminants come into contact with
0.20
(3300 cm2 for adults and 2800 cm2 for children), SL is the skin adherence
factor (0.2 mg·cm−2 for both adults and children), ABS is the dermal ab-
0.15
sorption factor (0.001 for all of the heavy metals), and PEF is the particle
0.10
emission factor (1.316 × 109 m3·kg−1). All of the parameters given
0.05
above were taken from reports published by the USEPA (2001) and
0.00
other relevant literature sources (USEPA, 2001).
-0.05

Cr Cd Pb Cu Ni 2.4.2. Risk characterization

Individual heavy metal from siteA The risks of carcinogenic and non-carcinogenic effects occurring in
the workers and children were quantified. Cd and Cr known to cause
Fig. 2. Individual heavy metal percentage of settled air particle and aerial parts of vegetable the risk of cancer (CR) are used to calculate the cancer risk (Ferreira-
samples from site A. Baptista and De Miguel, 2005; Tao et al., 2014). However, slope factors
of Cd and Cr for the risk of cancer occurring in the long term through in-
mass of samples extracted (kg); and BAc (%) is the bioaccessibility of the gestion and dermal contact have not been published by the USEPA;
heavy metal. therefore, only the risk of cancer from inhalation was included in this
study.
2.4. Risk assessment The risk of cancer occurring in the long term through ingestion and
dermal contact has not been published by the USEPA (2001). A hazard
2.4.1. Exposure assessment quotient (HQ) for the risk of non-cancer toxicity was determined by di-
People living in the vicinity of such an incinerator were considered viding the daily dose by the reference dose (RfD), whereas the risk of
to be exposed to metal contaminated ash or soil, and the health risks cancer was calculated by multiplying the daily dose by the slope factor
should be estimated. The exposure pathways and risk estimates were de- (SF). The equations for calculating the HQ, HI, and CR (USEPA, 2001;
termined according to US Environmental Protection Agency (EPA) health Tao, et al., 2014) were:
risk handbook (USEPA, 2001). The risk of exposure was expressed in "
#



terms of the daily dose, which was determined separately for each Di Di Di
HI ¼ þ þ ð5Þ
heavy metal, and the risk of each exposure pathway was calculated R fD ingestion R fD inhalation R fD dermal
using the formulae below.
The dose through the ingestion of soil was calculated using CR ¼ D  BA  SF ð6Þ

Ing R  EF  ED −6 D  BA
Ding ¼ C   10 ð2Þ HQ ¼ : ð7Þ
BW  AT R fD

the dose through the inhalation of soil was calculated using An HQ of less than or equal to a value of 1 was assumed to suggest that
adverse health effects were unlikely, whereas an HQ of more than a value
Inh R  EF  ED
Dinh ¼ C  ð3Þ of 1 was assumed to indicate that adverse health effects were probable. A
BW  AT  PEF
CR of less than 1 × 10−6 is considered as acceptable level for regulatory
and the dose absorbed through dermal contact with soil was calculated purposes (USEPA, 2001). SF is the slope factor ((mg/kg bw/d)−1). D is
using the daily dose (mg/kg bw/d).

SA  SL  EF  ED  ABS −6
2.5. Statistical analysis
Ddermal ¼ C   10 ð4Þ
BW  AT
All statistical tests were performed with SPSS 16.0 software and Or-
where D is the daily dose (mg kg−1 day−1), C is the heavy metal concen- igin 8.0. Normality of the data was checked by Shapiro–Wilk test. Means
tration in the samples [mg kg−1, the PBET-extractable concentrations or of different groups were compared using one-way ANOVA test. For post
the total concentration]. IngR is the ingestion rate (100 mg day−1 for hoc test in ANOVA, Dunnett's T3 method was adopted. Mean, median,

Table 3
Heavy metal concentrations (μg/g dry weight) of different vegetables from two sites.

Sampling point Samples Cr Cd Pb Cu Ni

Median (range) Median (range) Median (range) Median (range) Median (range)

Site A Leaf mustard 32 (26–33.5) 14.25 (8.8–15.75) 28.55 (15–34.8) 9.17 (6.67–11.67) 20.3 (18.3–21.3)
Morning glory 29.5 (24.5–60.5) 12 (7–13.5) 22.8 (16.3–33.3) 8.67 (6.42–9.42) 24.8 (23.8–25.3)
Leaf lettuce 57 (52–58.5) 6.75 (4.5–7.5) 34.55 (9–45.05) 6.42 (5–42–7.42) 22.8 (20.8–38.3)
Bitter lettuce 39.5 (33.5–40) 7.5 (3.25–15.5) 33.05 (29.55–45.8) 7.67 (3.92–10.67) 35.8 (18.8–36.55)
Lettuce 40 (33.5–46) 5.25 (3.25–5.5) 12.3 (9.3–44.55) 6.92 (4.92–9.17) 16.55 (7.8–38.55)
Site B Leaf mustard 12.5 (10–13.5) 6.75 (6.5–8.25) 19.75 (12.25–27.25) 3.4 (1.9–3.65) 12.5 (10.5–16.75)
Morning glory 10.35 (11.21–12) 6.75 (5–7.75) 16.75 (10–20.25) 2.4 (1.65–2.45) 13.5 (8–14.5)
Bitter lettuce 31.5 (30.5–32) 7.25 (7–7.5) 18 (9.5–20.5) 2.1 (0.65–2.65) 14.35 (12.25–17)
148 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151

150 (11.87–21.78 μg/g) in the soil samples in the present study were lower
140 than that found in Nanjing (p b 0.05) (Cu: 38.67–72.40 μg/g; Pb: 49.95–
83.54 μg/g), China (Fang et al., 2011), however, Cd showed similar levels
130
in these two sites (Nanjing: 58.22–74.88 μg/g; site A in the present study:
Total heavy metal concentration

120 45.55–91 μg/g). The concentration of Cr (215–358 μg/g) and Ni

110 (8–15.04 μg/g) in soil observed in the present study is higher than
100 that reported in Varanasi by Kumar Sharma et al. (2007) (Cr:
30.69–172.75 μg/g; Ni: 9.77–14.72 μg/g) (p b 0.05). The concentra-
90
tions of all heavy metals showed spatial variations, which may be due
80
to the variations in heavy metal sources and the quantity of heavy metals
70 discharged from industrial area. The concentration of all heavy metals
60 from Site A is much higher than (p b 0.05) that from Site B in roots
(Tables 1–2) possibly due to that site A was close to a waste incinerator,
50
which produced atmospheric pollution to the surrounding area. The
40
heavy metals at site B were not directly from the emission of industrial
pollution, but they may have been subject to changes by complex envi-
M
Bi
M

Le
Le

Bi
Le
Le

or
or

tte

af

tte
af

ronmental processes, such as volatilization, leaching, deposition, advec-

ttu
af

ni
ni

rl

rl
let

ng
ng

ce
m

us
ett

ett
tu
us

tive transport, soil burial, and plant uptake and degradation (Zeng et al.,
tar

gl
gl

uc
ce

uc
tar

or
or

d
e

e
y
d

Site A Site B 2014). Significant positive correlations were observed between Cr and
Cu in soil (R2 = 0.383; p = 0.014 b 0.05), which may suggest that the sim-
Fig. 3. Concentrations of heavy metals in the various vegetables collected from the two
ilar pollution source of these two heavy metals. However, significant neg-
sites.
ative correlations were observed between Cr and Ni (R2 = 0.473; p =
0.005 b 0.01), and between Pb and Cd (R2 = 0.453; p = 0.006 b 0.01)
and range was used to assess the contamination levels of heavy metals in soil at site A (Fig. 1). This negative correlation may be attributed to
in soil, root and aerial parts of vegetable samples. Pearson regression was the antagonism between the heavy metals during their absorption in
used to evaluate the association between heavy metal concentrations in soil. During summer, presumably due to moisture limitation and high
soil, roots and aerial parts of vegetables. Two-group independent sample temperature, Cr and Cd interfered with the Ni and Pb absorption.
t-test was used to compare the heavy metal concentration between site A For site A, Cd and Cr showed the lowest levels in roots and the highest
and site B. Pair-sample T test was used to compare the bioaccessibility in contents of Cd and Cr were found in soil. The concentration of Cr
gastric phase and in intestinal phase. The probability value of p b 0.05 was (285.07 μg/g) in soil was significantly higher than the samples of roots
set as the level for statistical significance. and vegetables (p b 0.05). There was no significant correlation between
the soil and the roots or the aerial parts of vegetables, which may indicate
3. Results and discussion that vegetables bioaccumulated a low amount of heavy metals from soil.
The concentrations of Cd and Cr in aerial parts of vegetables were signif-
3.1. Concentrations of heavy metals in different samples from the two sites icantly greater than their roots at site A in the present study (Table 1). For
site B, Cd had the similar trend (soil N vegetable N root) with the sample in
Concentrations of Cr, Cd, Pb, Cu, and Ni in different samples collected site A (Table 2). The trend was also observed by other researchers (Ross,
from two cities are given in Tables 1–2. Cr showed the highest concentra- 1994), which may suggest that the bioaccumulation of heavy metal in ae-
tion in all samples, followed by Cd, Pb, Cu, and Ni in Site A. In Site B, the rial part of vegetables differed from the root and there was another accu-
concentration was increased in the order of Cr N Cd N Pb N Ni N Cu. The ob- mulation pathway of heavy metal in the aerial part of vegetables.
served value of Cd was above the China's Soil Environmental Quality Stan- On the other hand, the pattern of heavy metals in aerial parts of veg-
dard (GB15618, 1995), however, Cr, Pb, Ni and Cu concentrations were etables and settled air particles was investigated. These two kinds of
below the China's Soil Environmental Quality Standard (GB15618, samples showed similar pattern and the percentage of heavy metals
1995) in two sites. The concentrations of Cu (7.09–21.36 μg/g) and Pb was increased in the order of Cr N Pb N Ni N Cu N Cd (Fig. 2). This may

Table 4
Health risks of human exposure to heavy metals via non-dietary intake of soil (95% CI interval). The proportion of Cr(VI) and Cr(III) was assumed to be 31% and 69% of total Cr, respectively,
according to Louhab and Akssas (2006).

Heavy metals Non-carcinogenic risks for children Non-carcinogenic risks for adults Carcinogenic risks for children Carcinogenic risks for adults

Site A Site B Site A Site B Site A Site B Site A Site B

Cd Ing 0.079–0.086 0.037–0.069 0.057–0.069 0.03–0.042 16.135–16.274 9.794–10.012 12.994–13.006 7.494–7.506

Inh 10.23–11.177 6.11–7.01 13.874–13.89 8.384–8.40
Dem 0.074–0.086 0.044–0.056 0.01–0.08 0.001–0.0042
Cr Ing 0.006–0.054 0.003–0.005 0.027–0.04 0.002–0.009 6.495–6.585 1.234–1.256 0.490–0.502 0.087–0.099
Inh 4.45–5.35 0.275–1.177 6.264–6.276 0.796–0.930
Dem 0.024–0.036 0.001–0.01 0.018–0.108 0.016–0.056
Pb Ing 0.093–0.201 0.005–0.047 0.074–0.089 0.015–0.027
Inh 13.769–14.671 3.40–4.31 1.40–1.49 0.875–0.965
Dem 0.005–0.205 0.006–0.054 0.035–0.125 0.014–0.067
Cu Ing 0.003–0.015 0.0021–0.007 0.001–0.011 0.001–0.007
Inh 0.759–1.661 0.315–0.587 1.155–1.245 0.415–0.505
Dem 0.003–0.015 0.0046–0.0072 0.004–0.051 0.001–0.046
Ni Ing 0.004–0.012 0.002–0.013 0.001–0.012 0.001–0.007
Inh 0.975–1.471 0.315–0.811 0.937–1.314 0.324–0.526
Dem 0.0016–0.014 0.003–0.0089 0.001–0.006 0.001–0.002
 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151 149

100 100
R e s id u a l
90 90 in te s tin a l
g a s tr ic
80 80

Ratio of heavy metals 70 70

60 60

50 50

40 40

30 30

20 20

10 10

0 0
Cd Cr Cu Ni Pb Cd Cr Cu Ni Pb
S o il f r o m S ite A S o il f r o m S ite B

Fig. 4. Bioaccessibility of heavy metals in soil from two sites.

indicate that settled air particle by atmospheric emissions was an im- For site A, the concentration of Cr (57 μg/g) and Pb (34.55 μg/g) in
portant source for the heavy metal accumulation in the aerial parts of the leafy lettuce was higher than other vegetables (p b 0.05), however,
vegetables. the highest concentration of Ni (35.8 μg/g) was observed in bitter let-
tuce (Table 3). For site B, the highest concentration of Cr (31.5 μg/g),
3.2. Accumulation of heavy metals in vegetables Pb (18 μg/g) and Ni was found in bitter lettuce. The higher uptake of
heavy metals such as Cr, Pb, and Ni compared to Cu and Cd may be
Concentrations of heavy metals in the various vegetables collected due to high transpiration rates, high ambient temperature and high hu-
from the two sites are illustrated in Table 3 and Fig. 3. (See Table 4.) midity during summer (Kumar Sharma et al., 2007).

Fig. 5. Characterization of non-carcinogenic risks (hazard quotient) to children and adults from heavy metals in the soil from the two sites. Total hazard quotient is the sum of each heavy
metal's hazard quotient. Total = Cu + Cr + Ni + Cd + Pb.
150 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151

Total concentrations of heavy metals in the various vegetables col- (mouthing and chewing) (Moya et al., 2004; Tao et al., 2014). Children
lected from the two sites are illustrated in Fig. 3. However, the highest sometimes accompany their parents to the farmland and are often
heavy metal concentrations were found in leaf lettuce 125.52 μg/g and exposed to the contaminated environment without any protective mea-
lettuce 71.2 μg/g for sites A and B, respectively, followed by bitter lettuce sures, which caused them easily be exposed to soil containing heavy
and leaf lettuce for sites A and B, respectively. Swamp morning glory ac- metals (Leung et al., 2008).
cumulated the lowest amount (81.02 μg/g for site A and 53.2 μg/g for The cancer risk of Cd (1.6 × 10−6) and Cr (2.1 × 10−6) was above
site B) at both sites. Jouraeva et al. (2002) investigated that heavy 10−6 (accepted level) in samples from site A for children. In addition,
metal deposition could be attributed to the wax layer characteristics the cancer risk of Cd (1.3 × 10−6) was above 10− 6 in samples from
on the leaf. This may explain the fact that the highest heavy metal con- site A for adults (Fig. 6). The present study indicated that the farmer
centration was observed in lettuce with waxy leaf cuticle at both sites and children living around the waste incinerator would face un-
(Fig. 3). Absorption and accumulation of heavy metals in plant tissue de- acceptable risk derived from the Cd and Cr in soils. It should be noted
pend upon many factors including temperature, moisture, organic mat- that Cr in soil samples assumed to be 100% Cr(VI) would overestimate
ter, pH, and nutrient availability. Heavy metals in several vegetables the cancer risk. In addition, the exposure factors such as the exposure
(dry weight) including cabbage, cucumber, parsley, and spinach were time and dermal absorption factor of heavy metals for children and
measured in industrialized regions (Ali and Al-Qahtani, 2012), and adult were derived from the USEPA exposure handbook, which may
their levels were considerably lower than those vegetables collected be not suitable for Chinese. It needs further investigation in the future
from site A in Guangzhou. Site A was close to a waste incinerator, work.
which produced heavy metal pollution to the surrounding area (Chen,
2004). Atmospheric deposition is the common source of heavy metal 4. Conclusion
uptake for plant shoots. The distribution of heavy metal in vegetation
tissues (above-ground parts) could be probably explained by atmo- The study concludes that heavy metal concentrations in rhizosphere
spheric deposition (Itanna, 2002), which was consistent with our soil were greater than those in roots. Heavy metal concentrations in ae-
present study. rial parts of vegetables were greater than those in roots. The trend and
relationship of heavy metal (Cr, Cd) concentrations in the soil, root
3.3. Bioaccessibility of the heavy metals in the soil samples from two sites
Site A
The bioaccessibilities of the heavy metals in soil from two sites are a 16
SiteB
shown in Fig. 4, and it can be seen that the bioaccessibilities of heavy
metals were decreased in the order of Cu N Pb N Ni N Cd N Cr. The largest 20
14
bioaccessibility of Cu (site A: 71.78%; site B: 49.46%) and Pb (site A:

Total Carcinogenic Risk(10 )

-7
Children
Carcinogenic Risk(10 )

68.38%; site B: 46.56%) was found in all samples. The bioaccessibility

-7

12
of each heavy metal in gastric phase was higher than that in intestinal
15
phase (p b 0.05), except Cu. It is known that higher solubility for 10
heavy metals would be found in the acid environment (gastric phase)
than in neutral or weak alkaline environment (intestinal phase), as 8
10
they will be precipitated at higher pH. The lower bioaccessibility of Cd
and Cr would be attributed to their higher affinity to pepsin in intestinal 6
juice compared to other heavy metals and metal binding competition
4
between pepsin and carbonates (Poggio et al., 2009). 5

2
3.4. Risk assessment
0 0
The risks of non-cancer toxicity caused by heavy metals in soil sam-
Cr Cd Total
ples for three exposure pathways to children and adults living near the
incinerator are shown in Fig. 5a and b, respectively. The proportion of
Cr(VI) and Cr(III) was assumed to be 31% and 69% of total Cr, respective- b 14
14
ly, according to Louhab and Akssas (2006). Cr(VI) and Cr(III) were used
to estimate the cancer and non-cancer risk of human exposure to Cr via 12
Total Carcinogenic Risk(10 )

soil, respectively. The non-cancer risk by non-dietary ingestion of soil 12

-7
Carcinogenic Risk(10 )

considering the bioaccessibility of heavy metals was two orders of mag-

-7

10
nitude higher than those from dermal contact, and four orders of mag- 10
nitude higher than the risks from inhalation for both children and Adults
workers. Therefore, non-dietary ingestion appears to be the most im- 8
8
portant exposure pathway in terms of health risks (Tao et al., 2014).
For children, Cd and Pb in soil samples resulted in the highest HQs 6 6
(.5), and Cu and Ni led to the lowest HQs when considering three expo-
sure pathways in both sites. The HQs of human exposure to soil for all
4 4
five heavy metals were decreased in the order of ingestion N dermal
contact N inhalation. It indicated that non-dietary ingestion of soil was
the most important exposure pathway, which was consistent with the 2 2
results of Tao et al. (2014).
The risks for adults (Fig. 5.b) were lower than the risks for children, 0 0
and the contributions of each exposure pathway to non-cancer risk for Cr Cd Total
adults were similar to that for children. According to other survey,
children had higher HQ via non-dietary ingestion of soil than adult be- Fig. 6. Carcinogenic risk of children and adults' exposure to Cr and Cd in the soil from the
cause of more outdoor-playing times and hand-to-mouth activities two sites.
 N. Li et al. / Science of the Total Environment 521–522 (2015) 144–151 151

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