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Speciation, bioaccessibility and potential risk of chromium in Amazon

forest soils

Article  in  Environmental Pollution · April 2018

DOI: 10.1016/j.envpol.2018.04.025

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 Environmental Pollution 239 (2018) 384e391

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Speciation, bioaccessibility and potential risk of chromium in Amazon

forest soils*
Leo J.D. Moreira a, b, Evandro B. da Silva c, Maurício P.F. Fontes d, Xue Liu a, **,
Lena Q. Ma a, c, *
a
Research Center for Soil Contamination and Remediation, Southwest Forestry University, Kunming, 650224, China
b
Federal Rural University of Amazon, C. P 3017, Parauapebas, Para
, Brazil
c
Soil and Water Science Department, University of Florida, Gainesville, FL, 32611, USA
d
Department of Soils, Federal University of Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil

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

Article history: Even though the Amazon region is widely studied, there is still a gap regarding Cr exposure and its risk to
Received 6 March 2018 human health. The objectives of this study were to 1) determine Cr concentrations in seven chemical
Received in revised form fractions and 6 particle sizes in Amazon soils, 2) quantify hexavalent Cr (CrVI) concentrations using an
5 April 2018
alkaline extraction, 3) determine the oral and lung bioaccessible Cr, and 4) assess Cr exposure risks based
Accepted 5 April 2018
on total and bioaccessible Cr in soils. The total Cr in both A (0e20 cm) and B (80e100 cm) horizons was
high at 2346 and 1864 mg kg
1. However, sequential extraction indicated that available Cr fraction was
low compared to total Cr, with Cr in the residual fraction being the highest (74e76%). There was little
Keywords:
Speciation
difference in total Cr concentrations among particle sizes. Hexavalent Cr concentration was also low,
Particle size averaging 0.72 and 2.05 mg kg
1 in A and B horizon. In addition, both gastrointestinal (21e22 mg kg
1)
Bioavailability and lung (0.95e1.25 mg kg
1) bioaccessible Cr were low (<1.2%). The low bioavailability of soil Cr and its
Bioaccessibility uniform distribution in different particle sizes indicated that Cr was probably of geogenic origin.
Hexavalent Cr Exposure based on total Cr resulted in daily intake > the oral reference dose for children, but not when
Risk assessment using CrVI or bioaccessible Cr. The data indicated that it is important to consider both Cr speciation and
bioaccessibility when evaluating risk from Cr in Amazon soils.
Published by Elsevier Ltd.

1. Introduction CrIII is an essential nutrient for humans and animals (Eastmond

Chromium (Cr) occurs naturally in soils and it is mostly from the
parental material, averaging 54 mg kg
1 worldwide (Kabata-
Pendias, 2011). However, Cr concentrations in soils from ultra-
mafic rocks can be as high as 60,000 mg kg
1 (Alloway, 2013).
Chromium can present as trivalent (CrIII) and hexavalent form
(CrVI), with CrVI being of the most concern. Trivalent Cr is often
present as Cr(OH)3 and Cr2O3, which can be adsorbed onto soil
surfaces or form complexes with organic matter, thus presenting
low availability (da Silva et al., 2018b; Apte et al., 2006). Besides,
*
This paper has been recommended for acceptance by Joerg Rinklebe.
* Corresponding author. Research Center for Soil Contamination and Remedia-
tion, Southwest Forestry University, Kunming, 650224, China.
** Corresponding author.
E-mail addresses: leopontocom2004@hotmail.com (L.J.D. Moreira), ebsilva@ufl.
edu (E.B. da Silva), mpfontes@ufv.br (M.P.F. Fontes), liuxue20088002@126.com
(X. Liu), lqma@ufl.edu (L.Q. Ma).
et al., 2008). Oxidation of CrIII to CrVI in soils can occur in the
presence of O2 and MnO2 or due to human activity (Fendorf et al.,
1992; Gress et al., 2015). Hexavalent Cr occurs as anionic species


2
(CrO2

4 , HCrO4 and Cr2O7 ) and is poorly adsorbed onto soils,
thereby presenting high availability (Ko zuh et al., 2000). Due to its
similar structure to phosphate and sulfate, CrVI is toxic and causes
diseases including cancer (Costa, 2003).
Exposure to Cr causes nausea, fever, headache, and respiratory
distress, with high exposure leading to serious health problem
including lung cancer (Wilbur, 2000). Risk assessment is often
based on total metal concentration (Cox et al., 2013). However, only
a fraction of the metal is available to be absorbed by oral, respira-
tory or skin contact (Li et al., 2016). Various assays have been
employed to evaluate metal bioavailability by simulating digestive
or respiratory processes (Juhasz et al., 2007; Huang et al., 2016). The
simple bioaccessibility extraction test (SBET) and Gamble's solution
protocols are the most employed in bioavailability studies for

https://doi.org/10.1016/j.envpol.2018.04.025
0269-7491/Published by Elsevier Ltd.
 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391
human risk assessment studies, which have been applied to soil
and dust (De Miguel et al., 2012; Coufalík et al., 2016; Mendoza
et al., 2017).
The Amazon region presents remarkable features including high
biodiversity and forest density, extensive rivers, and upland and
lowland soils. Ultissols and oxisols are the main soils in the region,
which tend to have low metal concentration. However, some soils
in the region from mafic and ultramafic rocks exhibit high metal
concentrations (de Souza et al., 2017). During a highway con-
struction in the Amazon forest, Brazil, symptoms such as fever,
headache, body weakness and fainting were reported by local
workers. Those symptoms can be associated with various sources,
but probably including toxicity from heavy metals. Several studies
reported Hg contamination in the Amazon basin due to its use in
gold mining, thus it is the main metal studied in the region
(Castilhos et al., 2015; Faial et al., 2015).
However, there is a gap regarding exposure to other metals
including Cr and its risk to human health in the Amazon region. In
fact, high Cr concentration (142 mg kg
1) was reported in the
Amazon basin area, being much greater than the background
concentration of 44.8 mg kg
1 (dos Santos and Alleoni, 2013). Thus,
the objectives of this study was to 1) determine Cr concentrations
in seven chemical fractions and 6 particle sizes in Amazon soils, 2)
quantify hexavalent Cr (CrVI) using an alkaline extraction, 3)
determine the oral and lung bioaccessible Cr, and 4) assess Cr
exposure risks based on total and bioaccessible Cr in Amazon soils.
2. Materials and methods
2.1. Soil characterization
In October of 2013, aleatory Oxisol soil samples were collected
from a pristine area in the Amazon Forest, Brazil (0 200 21.3500 N;
66 380 8.9200 W) (Fig. 1). Five samples of each representative horizon
(A - 0e20 and B - 80e100 cm) were collected and homogenized.
Soil samples were air-dried and sieved through a 2 mm sieve and
Fig. 1. Soils sampling location in the Amazon Rainforest, Brazil.
385
kept in closed container at room temperature.
Soil characterization was performed following Donagema et al.
(2011). Briefly, pH was determined in water using a 1:2.5 soil:so-
lution ratio. The cation exchange capacity (CEC) was calculated by
summing exchangeable ions including Ca, Mg, Na, K, H and Al.
Organic carbon (OC) content was determined by the Walkley-Black
method (Burt, 2004). Particle size distribution was determined
using the pipette method with NaOH solution being the dispersing
agent (Gee and Bauder, 1986). Sand fraction was separated by
passing the soil through a 0.2 mm mesh sieve, while the silt and
clay fractions were separated by sedimentation.
Concentrations of As, Cd, Co, Cr, Cu, Mn, Ni, Pb, Se and Zn were
determined by digesting the soil using the USEPA Method 3050B
following da Silva et al. (2018a). Briefly, 1 g of soil sample was
suspended in 15 mL of 1:1 nitric acid:water solution and heated at
105  C for 6 h. After cooling, 1 mL of 30% H2O2 was added and
digested for an additional 30 min before bringing samples to a
50 mL volume with double DI water. Metal concentrations were
analyzed using inductively coupled plasma mass spectrometry
(ICP-MS NexIon 300x, PerkinElmer Corp., Norwalk, CT).
2.2. Chemical and size fractionation of soil Cr
Soil Cr was separated into 7 fractions following sequential
extraction method of Silveira et al. (2006). They included: (E1)
soluble-exchangeable, (S2) surface adsorbed, (O3) organic matter,
(M4) Mn oxides, (A5) poor crystalline Fe oxides, (C6) crystalline Fe
oxides, and (R7) residual fractions. Briefly, 1 g of soil was extracted
using: 15 mL 0.1 M CaCl2, 30 mL 1 M NaOAC at pH 5, 5 mL NaOCl at
pH 8.5, 30 mL 0.05 M NH2OH/HCl at pH 2, 30 mL 0.2 M oxalic acid þ
0.2 M NH4 oxalate at pH 3, 40 mL 6 M HCl and HNO3-HCl digestion.
After each extraction, samples were centrifuged at 2000 rpm for
10 min and then filtered using Q2 filter paper (Fisher). Chromium
concentration was determined by ICP-MS.
Soil Cr was also separated into 6 particle sizes including <2000,
425e2000, 250e425, 150e250, 105e150 and < 105 mm. Chromium
386 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391

concentration was analyzed by graphite furnace atomic absorption ingestion using Equation (1). The variables and equations followed
spectrophotometry (GFAAS; Varian AA240Z, Victoria, Australia). USEPA (2001).

C x IR x EF x ED
2.3. Hexavalent Cr ADD ¼ (1)
BW x AT
The modified alkaline digestion method 3060A (de Oliveira Where ADD (mg kg d
1) ¼ average daily dose; C (mg kg
1) ¼ con-
et al., 2015) was used to determine CrVI concentration in particle centration; IR (mg d
1) ¼ ingestion rate; EF (d y
1) ¼ exposure
sizes < 2000, 425e2000, 250e425, 150e250, 105e150 frequency; ED (y) ¼ exposure duration; BW (kg) ¼ body weight,
and < 105 mm. Briefly, alkaline solution was prepared using 0.28 M and AT ¼ average time, with no carcinogenic effects (ED x 365 d)
NaCO3 and 0.5 M NaOH (pH > 12). In 1 g of soil was added 40 mL of and carcinogenic effects (70 y x 365 d). The specific values used for
the alkaline solution. To suppress CrIII oxidation to CrVI, ~400 mg of adults and children for each variable are presented in Table 2.
MgCl and 1 M phosphate buffer (0.5 M K2HPO and 0.5 KH2PO4)
were added. Samples were heated to 90e95  C for 1 h, stirring
3. Results and discussions
every 15 min. After that, samples were centrifuged for 10 min at
3000 rpm and then filtered using Q2 filter paper (Fisher). Blanks
3.1. Soil characterization
and spike solution of CrIII and CrVI were used as quality control and
they were all within the limits. Cr concentrations were analyzed
Soil characterization and heavy metal concentrations are shown
using GFAAS.
in Table 3. The soil was classified as an Oxisol, having low CEC
(0.17e0.57 cmol dm
3), OC content (2.53e3.68%) and pH
2.4. Oral and lung bioavailability (4.45e4.84), typical of the Amazon region soils (Quesada et al.,
2010). The soil has a clayey texture, including hematite, goethite
In vitro assays are widely used to measure metal bioavailability and, gibbsite minerals besides kaolinite and quartz minerals (data
in soils using simulated human gastrointestinal and lung fluids (Li not shown).
et al., 2016; Juhasz et al., 2007). The simple bioaccessibility Overall, for both A and B horizons, Cr (2346 and 1864 mg kg
1),
extraction test (SBET) and Gamble's solution protocols were Ni (62 and 63 mg kg
1) and Zn (14.7 and 16.4 mg kg
1) concen-
selected (Coufalík et al., 2016; Mendoza et al., 2017). trations were higher than the Amazon region background con-
Chromium oral bioavailability was determined using SBET test centrations (44.8, 2.1 and 3.0 mg kg
1 for Cr, Ni and Zn) (dos Santos
(USEPA, 2012), which uses 0.4 M glycine to simulate gastric solution and Alleoni, 2013). Difference can be attributed to soil parental
at pH ¼ 1.5 adjusted with concentrated HCl. Briefly, in 0.5 g of soil material (ferruginous laterite crust), which is rich in heavy metals
was added 50 mL of gastric solution and placed in water bath and tend to enrich metals during weathering process (Garnier et al.,
(37  C) with shaking (60 rpm) for 1 h. Then, samples were centri- 2013).
fuged (4000 rpm) and filtered using Q2 filter paper (Fisher). To
simulate accidental ingestion by hand-to-mouth pathway, only
3.2. Soil Cr fractionation
particle sizes <250 mm were tested, including 150e250, 105e150
and < 105 mm.
According to Shaheen and Rinklebe (2014), metal bioavailability
Chromium lung bioavailability was determined following
varies with different fractions, decreasing in the order of soluble-
Midander et al. (2007). Gamble's solution was prepared by mixing
exchangeable (E1) > surface adsorbed (S2) > Mn oxides ¼ poor
the reagents in proper order to prevent precipitation (Table 1), then
50 mL of Gamble's solution was added in a 50 mL vial containing
0.5 g of soil. In dark conditions, samples were placed in water bath Table 2
(37  C ± 2) with shaking (25 rpm) during 1 h. After that, samples Human exposure and risk assessment variables values from USEPA (2001).
were centrifuged (4000 rpm) and filtered using Q2 filter paper Variable Values
(Fisher). Tested particle sizes included 53e105 mm and <53 mm and
Adults Children
Cr concentrations were determined by GFAAS.
Average Daily Dose - ADD (mg kg d
1) e e
Concentration - C (mg kg
1) e e
2.5. Risk assessment Ingestion rate - IR (mg d
1) 100 200
Exposure frequency - EF (d y
1) 279 279
Risk Assessment based on average daily dose (ADD) was con- Exposure duration - ED (y) 24 4
Body weight - BW (kg) 70 16
ducted to identify potential effects on humans health due to
Average time e AT
exposure to soil Cr (Cachada et al., 2016). The ADD was calculated to AT ¼ no carcinogenic effects (ED x 365 d) 1460 1460
evaluate the potential risks for adults and children based on soil AT ¼ carcinogenic effects (70 y x 365 d) 25,550 25,550

Table 1
Gamble's solution extraction composition (mg L
1) and addition order.

Addition order Compounds Concentration (mg L
1)

1 Magnesium Chloride - MgCl 95

2 Sodium chloride - NaCl 6019
3 Potassium chloride - KCl 298
4 Disodium hydrogen phosphate - Na2HPO4 126
5 Sodium sulphate - NaSO4 63
6 Calcium chloride dihydrate - CaCl2 $ 2H2O 368
7 Sodium acetate - C2H3O2Na 574
8 Sodium hydrogen carbonate - NaHCO3 2604
9 Sodium citrate dihydrate e C6H5Na3O7 $ 2H2O 97
 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391 387

Table 3 crystalline Fe oxides (M4 and A5) > organic matter (O3) > crystal-
Chemical and physical properties Amazon soil (n ¼ 3). line Fe oxides (C6) > residual (R7) fraction. The data showed that
Horizons 74e76% of the Cr was in the residual fraction, with only 24e26%
A (0e20 cm) B (80e100 cm)
being in the non-residual fraction for both A and B horizons (Fig. 2).

3
Soluble-exchangeable and surface adsorbed fractions (E1 þ S2)
CEC cmolc dm 0.57 0.17
were <1.5 mg kg
1 for both horizons, contributing < 0.5% to total Cr.
OM % 3.68 2.53
Sand 50 50 Those fractions are available and easily leached out, especially in
Silt 8 10 tropical regions. This is because metals in these fractions are likely
Clay 42 40 from anthropogenic contribution, therefore being more available
pH 4.45 4.84 (Shaheen and Rinklebe, 2014). Geogenic metals in E1 þ S2 fraction
V mg kg
1
105 102
usually present low bioavailability than anthropogenic sources. The
Mn 207 193 low values of E1 þ S2 fractions indicated limited anthropogenic
Cr 2346 1864 impact in this soil (Sierra et al., 2007).
Co 3.67 3.41 Fractions O3, M4 and A5 are potential available, being affected
Ni 62.8 63.5
by soil pH and Eh (Shaheen and Rinklebe, 2014; Ma and Rao, 1997).
Cu 6.55 6.14
Zn 14.7 16.4 The sum of M4 þ A5 fractions corresponded to 2.0e2.1% of total Cr
As <0.01 0.01 (40e46 mg kg
1) (Fig. 2). Despite of the low percentage, those
Se 0.56 0.41 fractions can be potentially available, causing risk to human health
Cd 0.02 0.02 (Agnieszka and Barbara, 2012). Furthermore, Mn oxides (M4 frac-
Pb 3.03 2.98
tion) can oxidize CrIII to CrVI, increasing its availability and thereby
the risk to human health (Garnier et al., 2013). In both horizons,
fractions associated with organic matter (O3; 123 and
157 mg kg
1), crystalline Fe oxides (C6; 403 and 273 mg kg
1) and
residual (R7; 1630 and 1493 mg kg
1) presented the highest con-
centrations. The high Cr in the residual fraction (R7) indicated that
Cr had low availability in soil.

3.3. Total Cr and CrVI in different particles sizes

Chromium concentrations can vary with particle sizes, so it is

Fig. 2. Chromium fractionation in A and B horizons in an Amazon soil. Numbers inside
bars represent Cr percentage from each fraction (n ¼ 3).
important to understand Cr distribution among different sizes to
assess its potential risk. Fine particles have great capacity to hold
metals due to their large specific surface area. Besides, fine particles
are also easily transported by water or dispersed as dust, thus
presenting greater risks to the environment (Gong et al., 2014). In
the Amazon soil, however, there was little difference in Cr con-
centrations among six particle sizes for both horizons, averaging
2020 mg kg
1 for all particles sizes excluding 0.425e2 mm size in A
horizon (2700 mg kg
1; Fig. 3AB). It was much greater than the
background concentration for Amazon soils (44.8 mg kg
1),
exceeding the Brazilian Investigation Value of 400 mg kg
1
(CONAMA, 2009). The even distribution of Cr concentrations
among 6 particle size fraction was another indication that soil Cr
was of geogenic origin. Otherwise, more metals tend to accumulate
in finer particles due to their large surface areas (Gasparatos, 2013).
In addition to total Cr, distributions of toxic CrVI among different
sizes are shown in Fig. 3CD. Average CrVI concentration was 0.72
and 2.05 mg kg
1 for A and B horizons. The lower CrVI content in
the surface horizon might be due to microbial activities and the
presence of OC, reducing CrVI to CrIII (Rajapaksha et al., 2013). In
comparison, CrVI in Amazon soil was lower than Glasgow soils at
6.4 mg kg
1 (Broadway et al., 2010), which were contaminated with
chromite ore processing residue. Besides, it was lower than ultra-
mafic soils in Brazil at 446 mg kg
1 (Garnier et al., 2009). In the A
horizon, there was no relation between particle size and CrVI
concentration, however, in the B horizon, CrVI concentrations
decreased as particle size decreased (Fig. 3CD). Moreover, CrVI
concentrations in 0.105e0.150 mm fraction were 1.2 and
1.5 mg kg
1 for A and B horizons. This fraction had high availability,
which can be dispersed by water and dust, which can be easily
ingested or inhaled. Although, only one fraction showed high CrVI
concentration in the A horizon, it still poses risk to health human as
human contacts with surface soil the most.
Hexavalent CrVI in different particles sizes accounted for
0.02e0.06% and 0.01e0.14% for A and B horizons. Although being
388 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391
Fig. 3. Total Cr (AB; mg kg
1) and hexavalent Cr (CD; mg kg
1) distribution within particles sizes of the A and B horizons in an Amazon soil. Numbers inside bars represent CrVI
percentage. Different letters indicate statistic difference at p < 0.05 (n ¼ 3).
<0.2%, it was at 0.72e2 mg kg
1, which is susceptible to leaching.
Becquer et al. (2003) showed that CrVI was less adsorbed into soil
than CrIII, hence presenting high availability with potential envi-
ronmental consequences.
3.4. Cr oral and lung bioaccessibility and risk assessment
Besides total Cr and Cr speciation in different size fractions, oral
bioaccessible Cr based on simulated gastrointestinal assay was
determined, which averaged 21e22 mg kg
1 (Fig. 4AB). The results
were higher than uncontaminated soils (3.39e8.84 mg kg
1), but
similar to urban soils (29.0e400 mg kg
1) and road soils (up to
~30 mg kg
1) (Cox et al., 2013; Okorie et al., 2011; Sialelli et al.,
2011). Even at low bioaccessibility of 1.4% for A horizon, it repre-
sented 27 mg kg
1 Cr, which still presents potential risk to humans.
In both horizons, bioaccessible Cr concentration increased as par-
ticle size decreased (Fig. 4AB). Particles <105 mm showed higher
bioaccessible Cr at 27 mg kg
1. Similar results were observed in
urban soils from Spain and Italy (Okorie et al., 2011). High Cr con-
centration in fine particles in the A horizon can cause health issues
as they are easily dispersed and digested by the gastric system
(Madrid et al., 2008).
Besides oral bioaccessibility, we also measured lung bio-
accessibility of Cr in the soil, averaging 1.25 and 0.95 mg kg
1 for A
and B horizon, much lower than oral bioaccessible Cr at
21e22 mg kg
1 (Fig. 4). Lung bioaccessible Cr from contaminated
soils was 17 times greater than those in Broadway et al. (2010). The
low value indicated that the soil probably was not contaminated by
human activities. Low lung bioaccessible Cr can be explained by the
low solubility of crystalline Fe oxides and residual fractions since
lung fluid simulates solution pH at 7.2. Besides, Cr from soluble and
exchangeable phases were low, consistent with soil fractionation
data (Fig. 2).
It is known that particle deposition in the respiratory tract de-
pends on particle size. While finer particles (<4 mm) are able to
penetrate deeper into the alveolar region of the respiratory system,
particles of 10e100 mm are inhalable and tend to be deposited in
the upper respiratory tract (Colombo et al., 2008). Similar to oral
bioaccessibility data, lung bioaccessible Cr was higher in the A
horizon, indicating higher risk with surface soils. In addition, bio-
accessible Cr increased as particle size decreased (Fig. 4CD). The
data suggested that the finest fraction of surface soil showed the
highest risk with both high oral and lung bioaccessible Cr.
Based on USEPA (2001), reference dose (RfD) is an estimated
daily exposure to humans that is likely not to cause risk during a
lifetime exposure. The potential negative effects by exposure to
Amazon soil with high Cr concentration from geogenic source were
assessed. The ADD was calculated based on total (2025 and
2022 mg kg
1), oral bioaccessible (27 and 26 mg kg
1) and CrVI (1.2
and 3.37 mg kg
1) concentrations in both A and B horizons (Fig. 5).
As expected, the ADD based on total Cr concentration was much
higher than oral bioaccessible Cr or CrVI. This difference was ex-
pected due to the much greater value of total Cr. Other studies also
noticed similar results (Gress et al., 2014; Hamad et al., 2014). Only
ADD for children based on total Cr was greater than the oral RfD at
3  10
3 mg kg
1 d
1 based on non-carcinogenic risks (Fig. 5BD).
 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391 389

Fig. 4. Oral (AB; mg kg
1) and lung (CD; mg kg
1) bioavailable Cr in different particle sizes of A and B horizons in an Amazon soil. Numbers inside bars represent bioaccessible Cr% in
relation total Cr. Different letters indicate statistic difference at p < 0.05 (n ¼ 3).

Fig. 5. Average daily dose (ADD) of Cr ingestion for carcinogenic (AC) and non-carcinogenic (BD) risks of the A horizon and B horizon in an Amazon soil (n ¼ 3).
390 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391
The data indicated that the risk from soil Cr was much lower after
considering Cr speciation or bioaccessible Cr. As such, it is impor-
tant to consider both Cr speciation and bioaccessibility when
evaluating the risk from soil Cr.
4. Conclusion
For the Amazon soils, Cr concentrations at 1864e2346 mg kg
1
were much greater than the background concentration in Amazon
State soils, most likely due to the parental material. The low
contribution of available fractions (E1 and S2) and little difference
in total Cr concentrations within particles sizes indicated low
anthropogenic impact in the area, i.e., soil Cr is of geogenic origin.
CrVI was higher in the subsurface horizon, which might be related
to soil biota activities due to larger amount of organic matter in the
surface horizon. Besides, in A horizon there was no relation be-
tween particle size and CrVI concentration, however, in the B ho-
rizon, CrVI concentrations decreased as particle size decreased.
Both oral and lung bioaccessible Cr increased as particle size
decreased in both horizons. ADD based on total Cr concentration
was much higher than oral bioaccessible Cr or CrVI, with only
children value being higher than the RfD based on non-
carcinogenic risks. The data indicated that it is important to
consider Cr speciation and bioaccessibility when evaluating the risk
from soil Cr.
Acknowledgments
Senior author was supported in part by the Brazilian National
Council of Scientific and Technological Development (CNPq) (Pro-
cess N 233939/2014-8), University of Florida and Federal Univer-
sity of Viçosa. Second author was supported by CNPq project N
246758/2012-0.
References
Agnieszka, J., Barbara, G., 2012. Chromium, nickel and vanadium mobility in soils
derived from fluvioglacial sands. J. Hazard. Mater 237, 315e322.
Alloway, B.J., 2013. Heavy Metals in Soils: Trace Metals and Metalloids in Soils and
Their Bioavailability Third Edition XVIII, 614 p.
Apte, A.D., Tare, V., Bose, P., 2006. Extent of oxidation of Cr (III) to Cr (VI) under
various conditions pertaining to natural environment. J. Hazard. Mater 128,
164e174.
Becquer, T., Quantin, C., Sicot, M., Boudot, J.P., 2003. Chromium availability in ul-
tramafic soils from. NewCaledonia. Sci. Total Environ. 301, 251e261.
Broadway, A., Cave, M.R., Wragg, J., Fordyce, F.M., Bewley, R.J.F., Graham, M.C.,
Ngwenya, B.T., Farmer, J.G., 2010. Determination of the bioaccessibility of
chromium in Glasgow soil and the implications for human health risk assess-
ment. Sci. Total Environ. 409, 267e277.
Burt, R., 2004. Soil Survey Laboratory Methods Manual.
Cachada, A., da Silva, E.F., Duarte, A.C., Pereira, R., 2016. Risk assessment of urban
soils contamination: the particular case of polycyclic aromatic hydrocarbons.
Sci. Total Environ. 551, 271e284.
^as, R., de Jesus, I.,
Castilhos, Z., Rodrigues-Filho, S., Cesar, R., Rodrigues, A.P., Villas-Bo
Lima, M., Faial, K., Miranda, A., Brabo, E., et al., 2015. Human exposure and risk
assessment associated with mercury contamination in artisanal gold mining
areas in the Brazilian Amazon. Environ. Sci. Pollut. Res. 22, 11255e11264.
Colombo, C., Monhemius, A.J., Plant, J.A., 2008. Platinum, palladium and rhodium
release from vehicle exhaust catalysts and road dust exposed to simulated lung
fluids. Ecotoxicol. Environ. Saf. 71, 722e730.
CONAMA, Conselho Nacional deMeio Ambiente, 2009. Resoluç~ ao CONAMA No 420.
Di
~o no 249 2013, pp. 81e84.
ario Of. da Unia
Costa, M., 2003. Potential hazards of hexavalent chromate in our drinking water.
Toxicol. Appl. Pharmacol. 188, 1e5.
Coufalík, P., Mikuska, P., Matousek, T., Ve ce\vra, Z., 2016. Determination of the
bioaccessible fraction of metals in urban aerosol using simulated lung fluids.
Atmos. Environ. 140, 469e475.
Cox, S.F., Chelliah, M.C.M., McKinley, J.M., Palmer, S., Ofterdinger, U., Young, M.E.,
Cave, M.R., Wragg, J., 2013. The importance of solid-phase distribution on the
oral bioaccessibility of Ni and Cr in soils overlying Palaeogene basalt lavas,
Northern Ireland. Environ. Geochem. Health 35, 553e567.
de Oliveira, L.M., Lessl, J.T., Gress, J., Tisarum, R., Guilherme, L.R.G., Ma, L.Q., 2015.
Chromate and phosphate inhibited each other's uptake and translocation in
arsenic hyperaccumulator Pteris vittata L. Environ. Pollut. 197, 240e246.
De Miguel, E., Mingot, J., Chaco
n, E., Charlesworth, S., 2012. The relationship be-
tween soil geochemistry and the bioaccessibility of trace elements in play-
ground soil. Environ. Geochem. Health 34, 677e687.
de Souza, E.S., Texeira, R.A., da Costa, H.S.C., Oliveira, F.J., Melo, L.C.A., Faial, K.,
do, C.F., Fernandes, A.R., 2017. Assessment of risk to human health from
simultaneous exposure to multiple contaminants in an artisanal gold mine in
Serra Pelada, Par
a, Brazil. Sci. Total Environ. 576, 683e695.
da Silva, E.B., de Oliveira, L.M., Wilkie, A.C., Liu, Y., Ma, L.Q., 2018a. Arsenic removal
from As-hyperaccumulator Pteris vittata biomass: Coupling extraction with
precipitation. Chemosphere 193, 288e294. https://doi.org/10.1016/j.
chemosphere.2017.10.116.
da Silva, E.B., Li, S., de Oliveira, L.M., Gress, J., Dong, X., Wilkie, A.C., Townsend, T.,
Ma, L.Q., 2018b. Metal leachability from coal combustion residuals under
different pHs and liquid/solid ratios. J. Hazard. Mater. 341, 66e74. https://doi.
org/10.1016/j.jhazmat.2017.07.010.
Donagema, G.K., de Campos, D.V.B., Calderano, S.B., Teixeira, W.G., Viana, J.H.M.,
2011. Manual de me
todos de an
alise de solo. Embrapa Solos-Documentos
(INFOTECA-E).
Dos Santos, S.N., Alleoni, L.R.F., 2013. Reference values for heavy metals in soils of
the Brazilian agricultural frontier in Southwestern Amazo ^ nia. Environ. Monit.
Assess. 185, 5737e5748.
Eastmond, D.A., MacGregor, J.T., Slesinski, R.S., 2008. Trivalent chromium: assessing
the genotoxic risk of an essential trace element and widely used human and
animal nutritional supplement. Crit. Rev. Toxicol. 38, 173e190.
Faial, K., Deus, R., Deus, S., Neves, R., Jesus, I., Santos, E., Alves, C.N., Brasil, D., 2015.
Mercury levels assessment in hair of riverside inhabitants of the Tapajos River,
Para State, Amazon, Brazil: fish consumption as a possible route of exposure.
J. Trace Elem. Med. Biol. 30, 66e76.
Garnier, J., Quantin, C., Echevarria, G., Becquer, T., 2009. Assessing chromate avail-
ability in tropical ultramafic soils using isotopic exchange kinetics. J. soils
sediments 9, 468e475.
Garnier, J., Quantin, C., Guimar~ aes, E.M., Vantelon, D., Montarge s-Pelletier, E.,
Becquer, T., 2013. Cr (VI) genesis and dynamics in Ferralsols developed from
ultramafic rocks: the case of Niquela ^ndia, Brazil. Geoderma 193, 256e264.
Gasparatos, D., 2013. Sequestration of heavy metals from soil with FeeMn con-
cretions and nodules. Environ. Chem. Lett. 11, 1e9.
Gee, G.W., Bauder, J.W., 1986. Particle-size analysis. Methods soil anal. Part
1dphysical mineral. methods 383e411.
Gong, C., Ma, L., Cheng, H., Liu, Y., Xu, D., Li, B., Liu, F., Ren, Y., Liu, Z., Zhao, C., others,
2014. Characterization of the particle size fraction associated heavy metals in
tropical arable soils from Hainan Island, China. J. Geochem. Explor 139,
109e114.
Gress, J., de Oliveira, L.M., da Silva, E.B., Lessl, J.M., Wilson, P.C., Townsend, T.,
Ma, L.Q., 2015. Cleaning-induced arsenic mobilization and chromium oxidation
from CCA-wood deck: potential risk to children. Environ. Int. 82, 35e40.
Gress, J.K., Lessl, J.T., Dong, X., Ma, L.Q., 2014. Assessment of children's exposure to
arsenic from CCA-wood staircases at apartment complexes in Florida. Sci. Total
Environ. 476, 440e446.
Hamad, S.H., Schauer, J.J., Shafer, M.M., Al-Rheem, E.A., Skaar, P.S., Heo, J., Tejedor-
Tejedor, I., 2014. Risk assessment of total and bioavailable potentially toxic el-
ements (PTEs) in urban soils of BaghdadeIraq. Sci. Total Environ. 494, 39e48.
Huang, X., Betha, R., Tan, L.Y., Balasubramanian, R., 2016. Risk assessment of bio-
accessible trace elements in smoke haze aerosols versus urban aerosols using
simulated lung fluids. Atmos. Environ. 125, 505e511.
Juhasz, A.L., Smith, E., Weber, J., Rees, M., Rofe, A., Kuchel, T., Sansom, L., Naidu, R.,
2007. Comparison of in vivo and in vitro methodologies for the assessment of
arsenic bioavailability in contaminated soils. Chemosphere 69, 961e966.
Kabata-Pendias, A., 2011. Trace Elements in Soils and Plants. CRC Press.
Ko 
zuh, N., Stupar, J., Gorenc, B., 2000. Reduction and oxidation processes of chro-
mium in soils. Environ. Sci. Technol. 34, 112e119.
Li, S.-W., Li, H.-B., Luo, J., Li, H.-M., Qian, X., Liu, M.-M., Bi, J., Cui, X.-Y., Ma, L.Q., 2016.
Influence of pollution control on lead inhalation bioaccessibility in PM 2.5: a
case study of 2014 Youth Olympic Games in Nanjing. Environ. Int. 94, 69e75.
Ma, L.Q., Rao, G.N., 1997. Chemical fractionation of cadmium, copper, nickel, and
zinc in contaminated soils. J. Environ. Qual. 26, 259e264.
Madrid, F., Biasioli, M., Ajmone-Marsan, F., 2008. Availability and bioaccessibility of
metals in fine particles of some urban soils. Arch. Environ. Contam. Toxicol. 55,
21e32.
Mendoza, C.J., Garrido, R.T., Quilodra
n, R.C., Segovia, C.M., Parada, A.J., 2017. Eval-
uation of the bioaccessible gastric and intestinal fractions of heavy metals in
contaminated soils by means of a simple bioaccessibility extraction test. Che-
mosphere 176, 81e88.
Midander, K., Wallinder, I.O., Leygraf, C., 2007. In vitro studies of copper release
from powder particles in synthetic biological media. Environ. Pollut. 145,
51e59.
Okorie, A., Entwistle, J., Dean, J.R., 2011. The application of in vitro gastrointestinal
extraction to assess oral bioaccessibility of potentially toxic elements from an
urban recreational site. Appl. Geochem. 26, 789e796.
Quesada, C.A., Lloyd, J., Schwarz, M., PatiA$\pm$o, ~ S., Baker, T.R., Czimczik, C.,
Fyllas, N.M., Martinelli, L., Nardoto, G.B., Schmerler, J., others, 2010. Variations in
chemical and physical properties of Amazon forest soils in relation to their
genesis. Biogeosciences 7.
Rajapaksha, A.U., Vithanage, M., Ok, Y.S., Oze, C., 2013. Cr (VI) formation related to Cr
(III)-muscovite and birnessite interactions in ultramafic environments. Environ.
Sci. Technol. 47, 9722e9729.
 L.J.D. Moreira et al. / Environmental Pollution 239 (2018) 384e391
Shaheen, S.M., Rinklebe, J., 2014. Geochemical fractions of chromium, copper, and
zinc and their vertical distribution in floodplain soil profiles along the Central
Elbe River, Germany. Geoderma 228, 142e159.
Sialelli, J., Davidson, C.M., Hursthouse, A.S., Ajmone-Marsan, F., 2011. Human bio-
accessibility of Cr, Cu, Ni, Pb and Zn in urban soils from the city of Torino. Italy.
Environ. Chem. Lett. 9, 197e202.
Sierra, M., Martínez, F.J., Aguilar, J., 2007. Baselines for trace elements and evalua-
tion of environmental risk in soils of Almería (SE Spain). Geoderma 139,
209e219.
Silveira, M.L., Alleoni, L.R.F., O’connor, G.A., Chang, A.C., 2006. Heavy metal
View publication stats
391
sequential extraction methodsda modification for tropical soils. Chemosphere
64, 1929e1938.
USEPA, 2012. EPA 9200.2e86 April 2012 Standard Operating Procedure for an
in Vitro Bioaccessibility Assay for Lead in Soil 1e16.
USEPA, 2001. Risk assessment Guidance for Superfund (RAGS) volume III - Part A:
process for conducting Probabilistic risk assessment, Appendix B. Off. Emerg.
Remedial Response U.S. Environ. Prot. Agency III, pp. 1e385.
Wilbur, S.B., 2000. Toxicological Profile for Chromium. US Department of Health
and Human Services. Public Health Service (Agency for Toxic Substances and
Disease Registry).