Environmental Pollution 260 (2020) 113887

Contents lists available at ScienceDirect

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

Effect of biochars on bioaccumulation and human health risks of

potentially toxic elements in wheat (Triticum aestivum L.) cultivated on
industrially contaminated soil*
Nisar Muhammad a, *, Mohammad Nafees a, Muhammad Haya Khan a, Liya Ge b,
Grzegorz Lisak b, c, **
a
Department of Environmental Sciences, University of Peshawar, Peshawar, 25120, Pakistan
b
Residues and Resource Reclamation Centre, Nanyang Environment and Water Research Institute, Nanyang Technological University, 1 Cleantech Loop,
Singapore, 637141, Singapore
c
School of Civil and Environmental Engineering, Nanyang Technological University, Singapore, 637141, Singapore

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

Article history: In the present study, biochars (BCs) derived from naturally grown green waste (Cynodon dactylon L.) were
Received 23 August 2019 investigated regarding their impacts on bioaccumulation of potentially toxic elements (PTEs), agronomic
Received in revised form properties and human health risks of wheat crop cultivated on long-term industrially contaminated soil.
15 December 2019
Typically, three types of BCs were pyrolyzed at different highest temperature of treatment (HTT), i.e.
Accepted 26 December 2019
400
C, 600
C and 800
C, in a horizontal reactor and applied to the contaminated soil with 2% and 5%
Available online 7 January 2020
(w/w) ratio. The characterization results of the BCs showed that significant positive changes in funda-
mental characteristics such as porosity, surface area, cation exchange capacity, dissolved organic carbon,
Keywords:
Biochar
phosphorus and potassium have occurred with increased HTT. The analytical results of wheat crop
Green waste indicated that the BCs applications significantly (p  0.05) reduced concentration of PTEs in roots (48
Potentially toxic elements e95%), shoots (38e91%), leaves (30e91%) and grains (38e93%) of wheat plants. After the BCs application,
Wheat crop the agronomic properties were enhanced up to 6e18%, 18e38%, 17e46%, 13e45%, 15e42%, 22e55% and
Human health risks 34e57% for germination rate, shoot length, shoot biomass, spike length, spike biomass, grain biomass
and root biomass respectively. The human health risks of PTEs were significantly (p  0.05) decreased (31
e93%) from toxicity level to safe level (except for Mn and Cu), after the BCs application. Based on the
current study, the BCs (especially 800BC5) were recommended for reducing bioaccumulation of PTEs in
different parts of the wheat plant, increasing growth and yield of wheat crop and decreasing human
health risks via consumption of wheat grains.
© 2020 Elsevier Ltd. All rights reserved.

1. Introduction an alternative sources of irrigation particularly in Pakistan (Idress

Contamination of agricultural soils with potentially toxic ele-
ments (PTEs) as a common environmental problem that have
received more and more attentions (Ifon et al., 2019). As the surface
water is not sufficient for irrigation of crops, the farmers used
potentially toxic elements (PTEs) enriched untreated wastewater as
*
This paper has been recommended for acceptance by Wen Chen.
* Corresponding author.
** Corresponding author. Residues and Resource Reclamation Centre, Nanyang
Environment and Water Research Institute, Nanyang Technological University, 1
Cleantech Loop, Singapore, 637141, Singapore.
E-mail addresses: nisar5609@gmail.com (N. Muhammad), g.lisak@ntu.edu.sg
(G. Lisak).
et al., 2006; Jaramillo and Restrepo, 2017). These practices
enriched the concentrations of PTEs in agricultural soil, and further
led to bioaccumulation in crops (Muhammad and Nafees, 2018).
The bioaccumulation of PTEs in crops, such as wheat (Triticum
aestivum L.) is of great concerns, because it poses potential risks to
crop yield, food quality and human health (Nagajyoti et al., 2010).
According to Tasrina and Rowshon (2015), the root is a very sen-
sitive part compared to the rest parts of the plant, because it first
comes into contact with PTEs, and then bioaccumulate in excessive
quantities (Gramss and Voigt, 2016), which results in root necrosis
and decreasing its nutrients uptake (Geckil et al., 2002; Kuhar and
Gorensek, 2000), biomass and length (Alia et al., 2015). Further-
more, higher bioaccumulation of PTEs in roots leads to higher
translocation and bioaccumulation to shoots (Gramss and Voigt,

https://doi.org/10.1016/j.envpol.2019.113887
0269-7491/© 2020 Elsevier Ltd. All rights reserved.
2 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
2016), leaves (Karak and Bhattacharyya, 2010) and grains (Bose and
Bhattacharyya, 2008; Gramss and Voigt, 2016; Jamali et al., 2009).
Besides, the translocation and bioaccumulation of PTEs into the
upper parts of the crops decrease the length and biomass of shoots
and leaves (Alia et al., 2015; Geckil et al., 2002; Kukier and Chaney,
2004), adversely affect the yield of crops (e.g. wheat) and cause
phytotoxicity (Geckil et al., 2002; Mohamed et al., 2017).
As one of the main food crops in the human diet, wheat is
considered as the predominant pathway for human exposure to
PTEs (Khan et al., 2013). Because of the high phytoextraction po-
tential of wheats, people are more likely to be exposed to PTEs
through dietary intake of them, and can exceed maximum
permissible levels of PTEs (Liu et al., 2013; Yousaf et al., 2016a). The
long-term and continuous intake of PTEs through dietary route can
cause great adverse impacts for physiological and clinical health
(Augustsson et al., 2015; Liu et al., 2013). Several studies have
indicated that excessive doses of PTEs have a tendency to aggravate
non-carcinogenic health hazards, including both acute and chronic
toxicities (Liu et al., 2013; Muhammad et al., 2018). Furthermore, it
has also been noted that some PTEs even in a small amount could
cause severe human health risks by developing carcinogenicity
from lifetime of humans (Itoh et al., 2014; Lin et al., 2013). In order
to protect the environment and human health, it is obligatory to
restrict and control crops (e.g. wheat) from the toxic PTEs. In light of
the issue, it necessary to develop techniques for the remediation of
PTEs contaminated soil. Recently, various modern remediation
strategies have progressively focused on mitigating, eliminating
and controlling the levels of PTEs in crops. Biochar (BC) is one of the
cost-effective, environmental-friendly and safe remediation ap-
proaches (Rinklebe et al., 2016; Yousaf et al., 2017a), which has
obtained noteworthy attention due to its impressive capability to
in-situ stabilize PTEs (Zhang et al., 2016). The BC is a carbon-rich
solid product obtained by pyrolysis of organic materials at rela-
tive low temperatures (Lehmann and Joseph, 2009). The major
difference from other solid products obtained from biomass py-
rolysis is that the main usage of BC is the long-term carbon storage
in soils rather than the creation of feedstock for processing in-
dustries or fuels (Cross et al., 2010). The BC has been used in soil of
the Amazon basin for at least 2000 years (Kim et al., 2007). More
recently, it has been noticed that the potential impacts of BC on soil
could significantly reduce the uptake and bioaccumulation of PTEs
in cereal crops. Because BC has high surface area and the large
number of functional groups on the surface, it is very suitable for
adsorbing PTEs, and thus reducing the bioaccumulation of PTEs in
crops and ultimately reducing human health risks (Gul et al., 2015;
Rajapaksha et al., 2015). To the best of our knowledge, there has
been no research on the green waste derived BC that demonstrated
its role to decrease bioaccumulation of PTEs in wheat crops with
respect to decreasing human health risks.
In view of the importance for reducing bioaccumulation and
health risks, the present study was conducted with the objectives
to (i) investigate impacts of the green waste derived BCs application
on reducing bioaccumulation and of PTEs in different parts of
wheat plants, (ii) highlight the impacts of BCs on the growth and
yield of wheat crop, and (iii) estimate efficacy of the BCs on
reducing human health risks caused by the consumption of wheat
grains.
2. Materials and methods
2.1. Preparation and characterization of biochars
Naturally grown green waste (Cynodon dactylon L.) was pyro-
lyzed at different highest temperature of treatment (HTT), namely
400
C, 600
C and 800
C in a horizontal fixed-bed (internal
diameter of 5.5 cm and 100 cm long) reactor. The pyrolysis tem-
perature was increased at a rate of 10
C min1 until the desired
temperatures were reached, and then 20 min residence time was
applied to perform slow pyrolysis process under 100 L min1 ni-
trogen gas atmosphere, after which cooled down to 50
C with the
continuous flow of nitrogen. The solid yields were the BCs, which
were further ground through a 40 mesh (0.45 mm) sieve. The ob-
tained BCs were henceforth named and labeled as 400BC, 600BC
and 800BC, where BC stands for biochar and the numerical
numbers represent the HTT at which the BCs were pyrolyzed. After
that, the BCs were characterized for pH (Seven2Go™), surface area,
pore size and pore volume (Autosorb-1-C gas sorption system,
Quantachrome USA), elemental analyses that is C, H, N and S by
CHNS PerkinElmer 2400 Series II CHNS/O analyzer (PerkinElmer,
Shelton, CT) (Tan et al., 2014), water holding capacity (WHC) by
gravimetric method (Nguyen and Lehmann, 2009), cation exchange
capacity (CEC) by Flame Atomic Absorption Spectrophotometer,
PerkinElmer 700 (Gaskin et al., 2008), dissolved organic carbon
(DOC) by Shimadzu TOC-V CSH analyzer (Cabrera et al., 2011) and
major elements (Ca, Mg, Na, K and P) and PTEs (As, Cd, Cr, Co, Cu, Fe,
Mn, Ni, Pb and Zn) by Inductively Coupled Plasma Optical Emission
Spectrometer (ICP-OES), PerkinElmer Optima 8300 ICP-OES (ASTM,
1996).
2.2. Experimental design
A pot experiment was conducted in greenhouse under 12/12 h
day-night light, 26 ± 4
C and 22 ± 3
C temperature at day and
night respectively and 70 ± 5% relative humidity. The pots were
manually irrigated with deionized water and 60 ± 2% of soil
moisture was maintained. About 2.5 kg of PTEs enriched soil was
used, which has been irrigated with industrial wastewater for the
last three decades (1987e2017). Briefly, the soil is acidic in nature
with a pH 5.88 ± 0.1, CEC 10.0 ± 0.2 cmol kg1, DOC
9.26 ± 0.1 mg kg1, WHC 45.6 ± 1%, C 1.92 ± 0.3%, N 0.17 ± 0.03%, P
262 ± 4 mg kg1, K 515 ± 8 mg kg1 and having extensive con-
centration of PTEs as discussed by (Muhammad and Nafees, 2018).
The soil was added to each pot and was treated separately with the
400BC, 600BC and 800BC at a ratio of 2% and 5% (w/w) while one
pot was kept as control (without BC treatment). Four replicates of
each condition were carried out to evaluate the reliability of results.
Chemical fertilizers (half dosage of N with full dosage of P and K as
the basal dose: 120 kg ha1 N, 50 kg ha1 P and 25 kg ha1 K) were
mixed with soil. Remaining half dosage of N was applied in 2 steps,
that is one quarter at first irrigation and the other quarter during
milking stage (Yousaf et al., 2017b). From wheat seeds (RCA seed-
2016), 30 uniform shape seeds were soaked in H2O2 solution
(30%) for 15 min, then incubated at approx. 28
C overnight in
deionized water with availability of air, and finally germinated in
50 g soil collected from each pot on November 22, 2016. All the
petri dishes were randomly kept in environmental chamber at
25
C in dark conditions. After five days, the completely germinated
seeds with 2 mm long emergence of radicle were counted, and
length of the wheat shoot for each seedling was measured for
germination test. The germinated seeds were transferred to the
parental pots and grown. Subsequently, four uniform plants per pot
were left when each seedling have 3e4 leaves. The pot were irri-
gated with double deionized water till harvesting (April 25, 2017).
For reduction of potential biasness, the pots were randomized at
specific intervals for uniform light distribution (Mohamed et al.,
2017; Yousaf et al., 2018).
2.3. Post-experiment analysis
At maturity (153 days of complete life cycle) the wheat crops
 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887 3

were harvested at 2 cm above the surface of the soil, and agronomic

parameters (growth and yield) such as shoot length, shoot biomass,
spike length, spike biomass, grains biomass and root biomass per
pot were measured. Roots were carefully collected by digging the
around area to obtain its maximum length as possible. All the
samples were washed with double deionized water to remove
undesirable materials, cut into separate parts of roots, shoots,
leaves and seeds, sealed and shifted to laboratory for further ana-
lyses. For determination and quantification of PTEs and major ele-
ments, each sample was dried for 2e3 days in an oven at 60
C.
After completely drying, the samples were ground to powder form
by a grinder (Galal, 2016), and then digested through microwave
assisted acid digestion of siliceous and organically based matrices
method (ASTM, 1996). Briefly, 0.5 g of the prepared samples was
taken in Teflon beaker and 9 mL concentrated nitric acid (65%) and
1 mL hydrogen peroxide was added. The samples were heated at
180 ± 5
C for 15 min in microwave system. After cooling down, the
vessel contents were filtered, diluted with DI water to 50 mL and
analyzed the concentrations of the major elements and PTEs
through ICP-OES following standard working procedures.
2.4. Statistical analysis
Bioaccumulation factor (BAF) in Eq. (1) is the ratio of concen-
tration of PTE(s) in soil to concentration of PTE(s) in plants (Farahat
and Linderholm, 2015), translocation factor (TF) in Eq. (2) is an
index used for determining the relative translocation of a metal
from root to shoot of the plant (Galal and Shehata, 2015) and metal
pollution index (MPI) in Eq. (3) is used for precisely monitoring of
PTE(s) bioaccumulation in the edible part(s) of a plant which is
calculated as “the n-root from the n-Cf” (Singh et al., 2010).
BAF ¼ Croot =Csoil
TF ¼ Cshoot =Croot
 
MPI mgkg1 ¼ ðCf 1  Cf 2  Cf 3 /Cf n Þ1 = n
where Croot, Csoil, Cshoot, and Cf are the concentration of PTE in root,
soil, shoot and grains, respectively.
2.5. Health risk assessment
Average daily dose (ADD) in Eq. (4) is the daily exposure via
consumption of wheat grains (Cui et al., 2005) and hazard risk in-
dex (HRI) in Eq. (5) is the non-carcinogenic hazard risk index
caused due to consumption of the wheat grains (Yousaf et al., 2018).
ADD ¼ Cmetal  Dfi=BW (4)
HRI ¼ ADD=RfD (5)
where Cmetal, Dfi, BW, ADD and RfD are the concentration of PTE(s)
in wheat grain, approximate daily intake of wheat grains, body
weight, average daily dose and reference dose, respectively. The Dfi
of wheat grains are 0.345 and 0.232 kg person1day1 for adults
and children, respectively; and BW is 72 kg for adults and 32.7 kg
for children (Nawab et al., 2018a). The RfD is the reference dose
defined as “the maximum permissible risks to human population
by conserving a sensitive group during a lifetime” (Wei et al., 2015).
The HRI >1 is considered as significant non-carcinogenic health risk
(Muhammad and Nafees, 2018; USEPA, 2011).
2.6. Quality control and data analysis
For accuracy and precision of data, the certified standards were
used in each batch of plant extraction. Each sample was analyzed in
triplicate; thus measurement uncertainties were calculated. After
each batch of 10 samples, the ICP-OES was calibrated for stan-
dardization (R2 > 0.99). Furthermore, the data was statistically
analyzed through Statistix 10 (Analytical software, TN, USA); Origin
version 2018 (OriginLab) was used for graph plotting; and signifi-
cant difference was assessed by LSD test.
3. Results and discussion
3.1. Properties of biochars
Table 1 summarizes the properties (mean ± SD) of prepared BCs.
(1) The basic properties of the BCs (i.e. pH, CEC, WHC, surface area, pore
volume, pore size, yield and ash contents) varied, depending upon
the HTTs. All the three types of BCs were alkaline, with the pH of
(2)
9.06, 10.34 and 11.88 for 400BC, 600BC and 800BC, respectively.
Among the three BCs, the 800BC had the highest pH of 11.88, which
(3) can be explained by pyrolysis process where the metal oxides and
minerals remained in BCs and finally turned into alkaline media

ndez et al. (2013) had reported that high pH is
(Tan et al., 2014). Me
correlated with HTT, due to the release of alkali salts from the py-
rolytic structure (Chen et al., 2011) and decrease of acidic surface
functional groups due to the loss of oxygen (Filippis et al., 2013). In
general, the alkaline pH of BCs was found to contribute to immo-
bilization of PTEs, owning to PTEs transformation into precipitates
of low solubility in soil (Kistler et al., 1987). Moreover, the alkaline
pH of BCs does not allow to leach down their own PTEs to soil, thus
confirms the safety of soil. The surface area, pore volume and pore
size increased enormously with the increase of HTT as shown in

Table 1
Properties of biochars pyrolyzed at 400
C, 600
C and 800
C highest temperature of treatment.

Parameter 400BC 600BC 800BC Parameter 400BC 600BC 800BC

pH 9.1 ± 0.2 10.3 ± 0.2 11.9 ± 0.2 O/C 0.25 ± 0.004 0.16 ± 0.003 0.10 ± 0.002
WHC (%) 42.8 ± 0.7 48.7 ± 0.8 56.3 ± 0.9 H/C 0.06 ± 0.001 0.04 ± 0.001 0.03 ± 0.001
Surface area (m2 g1) 17.3 ± 0.3 36.5 ± 0.6 48.8 ± 0.8 P (mg kg1) 2030 ± 46 2440 ± 53 2920 ± 68
Pore volume (cm3 g1) 0.041 ± 0.001 0.052 ± 0.001 0.089 ± 0.001 Ca (mg kg1) 5640 ± 120 8640 ± 190 11680 ± 221
Pore diameter (nm) 3.735 ± 0.05 3.759 ± 0.06 3.778 ± 0.08 Mg (mg kg1) 2430 ± 53 3630 ± 72 4420 ± 88
CEC (cmol kg1) 51.2 ± 1.7 71.4 ± 1.8 94.8 ± 1.8 Na (mg kg1) 228 ± 5.7 363 ± 8.5 472 ± 11.6
DOC (mg kg1) 19.6 ± 0.3 22.3 ± 0.4 25.9 ± 0.4 K (mg kg1) 8130 ± 190 10270 ± 220 13820 ± 260
C (%) 56.6 ± 0.9 65.3 ± 1.1 72.8 ± 1.2 VM (%) 28.7 ± 0.1 20.9 ± 0.1 13.7 ± 0.1
H (%) 3.56 ± 0.06 2.78 ± 0.05 1.98 ± 0.03 FC (%) 53.0 ± 0.1 61.3 ± 0.1 67.8 ± 0.1
N (%) 1.88 ± 0.03 1.62 ± 0.03 1.22 ± 0.02 Yield (%) 38.3 ± 1.06 34.3 ± 1.00 32.6 ± 0.93
S (%) 1.93 ± 0.03 1.67 ± 0.03 1.19 ± 0.02 Moisture (%) 1.36 ± 0.06 1.33 ± 0.04 1.29 ± 0.03
O (%) 14.1 ± 0.23 10.6 ± 0.17 7.23 ± 0.12 Ash (%) 13.2 ± 0.13 17.8 ± 0.18 22.5 ± 0.26
4 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
Fig. 1. Nitrogen adsorption-desorption isotherms and pore size distribution curves
(inside) of biochars.
Fig. 1, which is further supported by the SEM image (Fig. S-1).
Similar findings had been reported by others, e.g. Me
ndez et al.
(2013) and Tan et al. (2014) using sewage sludge derived BCs and
Yuan et al. (2011) with different crops (canola, corn, soyabean and
peanut) BCs. The nitrogen adsorption also significantly increased
with the increase of HTT. The nitrogen adsorption-desorption iso-
therms of the BCs corresponds to type IV isotherm of IUPAC clas-
sification (Pavan and Andrew, 2019; Sing et al., 1985), which
showed that the BCs had (i) mesoporous structure (2e50 nm), (ii)
narrow necks and wide bodies (ink bottle pores) and (iii) capillary
condensation to occur in the mesopores of BCs (Tan et al., 2014).
The pore size curves of BCs showed that the pores distributions in
all the BCs were similar at the peak position (3.82 nm), whereas all
the pores structure were uniform and channelized (Fig. 1, inside).
The results of mesopores formation are consistent with the sewage
sludge derived BC reported by Rio et al. (2005). The CEC of the BCs
was significantly increased with the increase of HTT, which is
consistent with the findings of Tan et al. (2014) and Me
ndez et al.
(2013) using sewage sludge BCs. Similarly, the DOC concentra-
tions were 19.58, 22.28 and 25.94 mg kg1 at 400
C, 600
C and
800
C HTT, respectively, which increased with the increase of HTT.
Cheng et al. (2016) has also reported similar DOC of 19.81 and
14.40 mg kg1 for BCs pyrolyzed from peanut shell and sewage
sludge, respectively. The C and P concentrations in the BC pyrolyzed
at 800
C were comparatively higher than at 600
C and 400
C,
which indicated consistency with the findings of Zhao et al. (2017)
for C and Tan et al. (2014) for P in apple tree branches and sewage
sludge BCs, respectively. As the increase of HTT, the surface func-
tional groups based on N, H and O as well as S contents were lost
with volatile matter, which is why the concentration of N, S, H and
O declined rapidly from 400
C to 800
C, while the C remained as a
fixed carbon (FC) and a volatile matter (VM). As a result, the atomic
ratio decreased, amorphous carbon increased and micro structures
developed enormously. Similar findings had been reported by Tan
et al. (2014) for different sewage sludge derived BCs. Compared
with 400
C, the molar O/C and H/C ratios were decreased at
maximum HTT (800
C). The decrease in O/C and H/C ratios also
illustrated that the significant loss of oxygen and aliphatic
hydrogen leads to dehydrogenative polymerization and dehy-
dartive polycondensation processes during pyrolysis of BCs (Filippis
et al., 2013). The high molar O/C ratio of BC showed the availability
of more polar groups with higher hydrophilic properties (Chun
et al., 2004). While the molar H/C of the BCs as a carbonization
degree is always lower than 0.5, indicated that strong carbonization
and high aromaticity are therefore resistant to decomposition of
the BCs (Yuan et al., 2013). The concentrations of major elements
were increased with the increase of HTT. Compared to 400
C, the
Ca, Mg, Na and K concentrations at 800
C were increased 51.8%,
45.0%, 51.7% and 41.1%, respectively. Our findings were consistent
with the apple tree derived BCs used by Zhao et al. (2017).
Furthermore, the yield, moisture and VM of BCs production
reduced while ash contents increased with the increase of HTT. The
gasification of VM at high HTT could lead to an increase in FC
contents (Yang and Sheng, 2012). Whereas, FC is considered as an
indicator for evaluating the recalcitrance and stability property of
BCs (Masek et al., 2013; Zhao et al., 2013). Moreover, BCs with low
VM contents are more suitable for agronomic use, because of their
role in microbial activity and nitrification (Deenik et al., 2009).
Similar findings had been reported from a number of studies such
as Me
ndez et al. (2013) for sewage sludge derived BCs and Yuan
et al. (2013) for canola, corn, soyabean and peanut crops derived
BCs.
3.2. Impacts of biochars on wheat
3.2.1. Impacts on bioaccumulation and translocation of PTEs into
wheat plant
The concentration of PTEs in the wheat plant parts (roots,
shoots, leaves and grains) of BCs treated soils were significantly
(p  0.05) decreased as compared to control soil wheat plant parts
(Figs. 2 and 3). For example, the Cu concentration was decreased by
65e84%, the Cr concentration was decreased by 78e95%, the Pb
concentration was decreased by 75e94%, the Ni concentration was
decreased by 67e87%, the Fe concentration was decreased by
30e43%, the Zn concentration was decreased by 11e22%, the Mn
concentration was decreased by 48e63%, the Cd concentration was
decreased by 76e91%, the As concentration was decreased by
66e82% and the Co concentration was decreased by 51e68% in the
roots, as shown in Fig. 2 (a). Similarly, in the shoots, the concen-
trations of Cu, Cr, Pb, Ni, Fe, Zn, Mn, Cd, As and Co were reduced by
47e62%, 66e85%, 75e91%, 58e78%, 25e38%, 13e25%, 38e54%,
72e89%, 50e68% and 43e58%, respectively, as shown in Fig. 2 (b).
Likewise, in the leaves, the concentrations of Cu, Cr, Pb, Ni, Fe, Zn,
Mn, Cd, As and Co were reduced by 57e73%, 70e88%, 72e91%,
53e71%, 30e46%, 17e29%, 26e41%, 69e86%, 65e81% and 48e64%,
respectively, as shown in Fig. 2 (c). In the grains, the concentrations
of all PTEs (except Mn, Cu, Co and As) exceeded the maximum
permissible limits (MPLs) set by Joint FAO/WHO (2007, Joint FAO/
WHO, 2001, Joint FAO/WHO, 2001) . The concentrations of Fe, Zn,
Mn, Cu, Cr, Ni, Pb, Co, Cd and As were significantly (p  0.05)
decreased by 38e51%, 30e36%, 38e48%, 53e68%, 78e93%, 61e76%,
78e93%, 55e67%, 77e92% and 60e73%, which was found below
their MPLs values (Fig. 3) after application of the BCs.
Roots are severely sensitive than other parts of plants because it
comes first in contact with PTEs. The PTEs bioaccumulation in roots
depends on the concentration of PTEs, plant species, plants parts,
and soil properties (Tasrina and Rowshon, 2015). Similarly, shoots
and leaves bioaccumulate more PTEs than grains, indicates exclu-
sively distribution and translocation of PTEs into wheat tissues. The
bioaccumulation of PTEs in roots showed positive correlation with
the concentration in shoots, leaves and grains which had also been
reported by Karak and Bhattacharyya (2010). Gramss and Voigt
(2016) had found Cd, Cu, Fe, Mn, Ni and Zn up to 96%, 63%, 24%,
45%, 73% and 97% higher in roots, 98%, 68%, 23%, 63%, 16% and 92%
higher in shoots and 93%, 20%, 33%, 10%, 80% and 78% higher in
grains, respectively of wheat cultivated on contaminated soil than
 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
Fig. 2. Decrease in PTEs bioaccumulation in roots (a), shoots (b) and leaves (c) after applying biochars.
non-contaminate soil. Farahat et al. (2017) had also found PTEs (Cd,
Fe, Mn, Pb and Zn), 15e47 times higher in wheat grains cultivated
on contaminated soil than non-contaminated soil. Other studies
(Bose and Bhattacharyya, 2008; Jamali et al., 2009) had reported
dominant bioaccumulation of PTEs in wheat grains cultivated on
contaminated soil.
The PTEs bioaccumulation in roots, shoots and leaves causing
toxicity in term of growth, biomass and nutrients uptake (Geckil
et al., 2002; Kuhar and Gorensek, 2000; Kukier and Chaney,
2004). Alia et al. (2015) have also reported phytotoxicity of PTEs
and reported 35e42% and 25e47% decrease in roots and shoots
biomass and 16e22% and 13e21% decrease in roots and shoots
length. Chandra et al. (2009) have also reported PTEs (Cd, Cr, Cu, Fe,
Ni, Mn and Zn) in wheat grains higher than FAO/WHO MPLs and
strongly condemned wastewater irrigated wheat crops for con-
sumption of human and animals due to its severe health problems.
The decreased concentration of PTEs in roots, shoots, leaves and
grains cultivated on BCs treated soil showed that the BCs has
significantly (p  0.05) immobilized the PTEs in soil, thus reduced
its bioaccumulation and translocation to wheat plant. The BC re-
duces bioaccumulation of PTEs in roots due to (i) formation of
soluble PTEs-DOC complexes, which cannot diffuse into the tissues
of plants (Vithanage et al., 2017), (ii) change in soil pH (from acidic
to alkaline), because at alkaline pH PTEs transform into precipita-
tion of low solubility (Bian et al., 2016; Tan et al., 2014), (iii)
adsorption of PTEs on BC surface due to reduction of acid functional
groups (Kołodyn
ska et al., 2012), and (iv) increased DOC concen-
tration of soil as it motivates stable complexes formation and
adsorption of PTEs on BC surface (Zheng et al., 2013, 2012). The BC
application decreased translocation of PTEs from roots to shoots,
leaves and grains and reduced its phytotoxicity because it enhanced
5
microbes growth in soil, which adsorbed PTEs and stored them in
different cell parts or bound it by microbial metabolism as a result
of precipitation and crystallization (Lahori et al., 2017). Decrease in
PTEs bioaccumulation and translocation to upper parts of plant
with BCs application has reported by various studies, such as
Akhtar et al. (2015) have reduced PTEs up to 53% by 5% application
of commercially available BCs. Li et al. (2016) have reported a
decrease of PTEs up to 12.2%, 15.6% and 18.5% in roots, shoots and
grains, respectively, after applying of wheat straw derived BCs.
Furthermore, Zhu et al. (2015) have also reported significant
decrease in PTEs (Cd, Cr, Cu, Ni, Pb and Zn) bioaccumulation in
roots, shoots, leaves and grains with application of wheat, corn, rice
and sorghum straws derived BCs. Other study (Rizwan et al., 2018)
stated that 5% application of rice straw derived BCs has reduced
PTEs (61%) in shoots. Abbas et al. (2017) and Younis et al. (2016) has
stated that 5% application of rice straw and cotton stalk derived BCs
respectively, increased photosynthesis and leaf chlorophyll con-
tents and reduced oxidative stress due to PTEs reduction. Qiao et al.
(2018) has reduced PTEs up to 61e93% in grains with 5% oil palm
fibers derived BCs application due to reduction of the phytoavail-
ability of PTEs in the amended soil (Beesley et al., 2013; Vithanage
et al., 2017). Rizwan et al. (2018) have stated that 5% application of
rice straw derived BCs significantly reduced PTEs in grains. Simi-
larly, Abbas et al. (2018) have reduced PTEs up to 55% in grains with
rice straw derived BCs. Furthermore, the overall concentrations of
PTEs in the roots, shoots, leaves and grains were found in the
decreasing order of 800BC5 > 600BC5 > 400BC5 > 800BC2 >
600BC2 > 400BC2 > control, which indicates (i) the efficacy of
higher HTT pyrolyzed BC and 5% application rate than lower HTT
pyrolyzed BC and 2% application rate and (ii) free mobility of PTEs
in the control soil and potential toxicity to wheat plant.
6 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887

Fig. 3. Decrease in PTEs bioaccumulation in grains after applying biochars. aJoint FAO/WHO, 2001a; bJoint FAO/WHO, 2001b; cJoint FAO/WHO 2007
 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887 7

3.2.2. Impacts on wheat crop statistics health complications, and are higher than Tasrina and Rowshon
The BAF and TF results revealed that bioaccumulation and (2015). Furthermore, Yousaf et al. (2016b) had studied effects of
translocation of the PTEs to wheat plants had significantly Eucalyptus wood derived BC and traditional organics amendments
(p  0.05) decreased in the BCs treated soil as compared to control (farm manure, poultry manure, compost, press mud and sewage
soil wheat plants (Fig. 4). As shown in Fig. 4 (a), the BAFs of Cu, Cd, sludge) on reduction in TF of PTEs in wheat plant. Their findings
Pb, Cr, As, Fe, Ni, Zn, Co and Mn were decreased 65e84%, 76e91%, indicated that BC application has significantly (p  0.05) lowered
75e94%, 78e95%, 66e82%, 28e43%, 67e87%, 11e22%, 51e68% and the TF quotient compared to the organic amendments, because of
48e63%, respectively. Similarly, as shown in Fig. 4 (b), the TFs of Fe, high carbon contents availability in the BC (Roth et al., 2012;
Zn, Cd, Co, Mn, Cu, As, Cr, Pb and Ni were decreased 25e38%, Uchimiya et al., 2011).
13e25%, 72e89%, 43e58%, 38e54%, 50e68%, 47e62%, 66e85%, The metal pollution index of control grains was 9817.19, which
75e91% and 58e78%, respectively. The BAF and TF results in the was reduced to 6.69 by 800BC5 application. Significant (p  0.05)
control soil were found in the decreasing order of Cu > Cd > Pb > Cr decrease in MPI was in the order of 99.9%, 99.8%, 99.7%, 99.5%, 99.3%
> As > Fe > Ni > Zn > Co > Mn and Fe > Zn > Cd > Co > Mn > As > Cu and 99.0% by the 800BC5, 600BC5, 400BC5, 800BC2, 600BC2 and
> Cr > Pb > Ni, respectively. In addition, the overall BAF and TF 400BC2 application, respectively (Fig. 5). High MPI shows more
results in decrease of PTEs concentration after the BCs application bioaccumulation of PTEs concentration in wheat grains and hence
was is in the order of 800BC5 > 600BC5 > 400BC5 > 800BC2 > pose more human health risks than lower MPI of wheat grains. The
600BC2 > 400BC2 > control, which indicates that higher HTT py- overall results revealed that higher HTT pyrolyzed BC and 5%
rolyzed BC and 5% application rate are more efficient than lower application have comparatively lower MPI results than lower HTT
HTT pyrolyzed BC and 2% application. pyrolyzed BC and 2% application. Moreover, all the three BCs with
The BAF and TF results might help to evaluate the incorporation both 2% and 5% application showed significant (p  0.05) reduction
of PTEs by wheat crop. Higher the BAF or TF quotient (BAF or TF > 1)
greater will be potential of wheat crop in PTEs bioaccumulation and
translocation, respectively and lower the BAF quotient (BAF or
TF < 1) represent stabilization of PTEs in soil and low translocation
of PTEs to upper parts of plants (Cui et al., 2004; Farahat et al.,
2017). Furthermore, plants having BAF >1 can be used either for
phyto-extraction (Christou et al., 2017), which declare that wheat
crop cannot be used for phyto-extraction of PTEs as the BAF is lower
than 1. The TF quotient is comparatively more than the BAF quo-
tient, which clarifies that the roots have low phyto-stabilization
potential of PTEs thus increases phytotoxicity to upper parts of
wheat plant. This study results are consistent with Chandra et al.
(2009) who had found BAF < 1 and discouraged use of wheat
plant for hyper bioaccumulation of PTEs. Conversely, Farahat et al.
(2017) had reported more BAF values for PTEs (Cd, Cr, Co, Fe and
Ni) than the present study results in wheat cultivated on waste-
water irrigated soil. Furthermore, BAF less than 1 for Cr, Co, Cu and
Fe in wheat had been reported by Khan et al. (2017) and for Cd, Cu,
Ni and Zn by Ran et al. (2016). Similarly, the TF results of the present
study are lower than Khanum et al. (2017) and Opaluwa et al.
(2012) who declared that continuous consumption of such TF
level species may lead to bioaccumulation of PTEs and causes
Fig. 5. Decrease in metal pollution index of wheat grains after applying biochars.

Fig. 4. Decrease in bioaccumulation factor (a) and translocation factor (b) of wheat plant after applying biochars.
8 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
in MPI than control site. This indicates that control soil tends to
bioaccumulate more PTEs in edible parts (grains) than BCs amen-
ded soil.
3.2.3. Impacts on agronomic properties of wheat crop
Table 2 summarizes the agronomic importance of the BCs on
germination rate, growth and yield of wheat crop. The results
indicated that soil irrigated with industrial wastewater (control)
had negatively affected the germination rate, growth and yield of
wheat crop. Conversely, the BCs treated soil showed significant
positive effects on germination rate, growth and yield parameters.
The germination rate of control soil was 81.1%, while the BC treated
soil with 800BC5 was 98.8% (highest germination rate). The
germination rates were 18.0%, 16.8%, 15.2%, 10.8%, 8.7% and 6.2%
higher than the control for 800BC5, 600BC5, 400BC5, 800BC2,
600BC2 and 400BC2, respectively. Shoots length was increased up
to 38.2% compared to control. The shoots lengths were increased
38.2%, 35.5%, 29.9%, 24.8%, 22.3% and 17.7% for 800BC5, 600BC5,
400BC5, 800BC2, 600BC2 and 400BC2, respectively. Compared to
control, the shoots biomass was increased up to 45.8%, 39.4%, 31.6%,
25.8%, 21.2% and 17.1% for 800BC5, 600BC5, 400BC5, 800BC2,
600BC2 and 400BC2, respectively. Spikes lengths were increased
45.3%, 34.4%, 25.8%, 17.7%, 15.2% and 12.6% for 800BC5, 600BC5,
400BC5, 800BC2, 600BC2 and 400BC2, respectively. The spikes
biomasses for 800BC5, 600BC5, 400BC5, 800BC2, 600BC2 and
400BC2 were increased up to 45.8%, 39.4%, 31.6%, 25.8%, 21.2%, and
17.1%, respectively. Compared to control, the grains biomasses were
increased up to 55.5%, 48.7%, 43.1%, 37.8%, 33.5% and 22.5% for
800BC5, 600BC5, 400BC5, 800BC2, 600BC2 and 400BC2, respec-
tively. Compared with the control, the root biomasses for 800BC5,
600BC5, 400BC5, 800BC2, 600BC2, and 400BC2 increased by 55.7%,
51.7%, 48.3%, 46.2%, 41.3%, and 34.5%, respectively.
The overall results revealed that highest HTT and 5% application
rate produced highest germination rate, growth and yield.
Furthermore, germination rate, growth and yield parameters were
in the decreasing order of 800BC5 > 600BC5 > 400BC5 > 800BC2 >
600BC2 > 400BC2 > control as shown in Table 2. The decreased
germination rate, growth and yield in the control soil might be the
result of increased phytotoxicity of PTEs (Geckil et al., 2002;
Mohamed et al., 2017). While the comparatively significant
(p  0.05) increase in germination rate, growth and yield in BCs
amended soils, could be linked with increased pH, WHC, CEC, DOC,
C, N, P, S, K levels and decreased the concentrations of PTEs in soil
(Akhtar et al., 2015; Makarfi, 2014; Vaccari et al., 2011) and
increased concentrations of plant nutrients (N, P and K) and its
chlorophyll contents (Akhtar et al., 2018; Khan et al., 2019). The
current findings are consistent with a number of previous studies
(Sial et al., 2019), who reported 41.5% and 35.3% increase in shoot
biomass, 41.1% and 37.0% increase in root biomass and 58.5% and
51.9% increase in wheat yield with 2% application of tea waste and
banana peel derived BC, respectively. The higher plant growth and
grains yield with 800BC than 400BC application, is because of the
higher concentration of N and K and lower ratio of C/N (Sadaf et al.,
Table 2
Improvements in germination rate, growth and yield of wheat crops by applying biochars.
Parameter Control 400BC2
Germination rate (%) 81.14 ± 1.33 86.38 ± 1.42
Shoot length (cm plant1) 45.37 ± 0.75 55.12 ± 0.91
Shoot biomass (g pot1) 10.15 ± 0.17 12.25 ± 0.20
Spike length (cm plant1) 8.67 ± 0.14 9.92 ± 0.16
Spike biomass (g pot1) 2.83 ± 0.05 3.34 ± 0.05
Grains biomass (g pot1) 8.35 ± 0.14 10.77 ± 0.18
Root biomass (g pot1) 2.13 ± 0.04 3.25 ± 0.05
2017) and comparatively high pore size and surface area (Sial et al.,
2019), shown in Table 1 and Figs. 1 and S-1. Similar results of in-
crease in growth and yield with BCs application for other crops
have also reported by previous studies (Arif et al., 2018; Khan et al.,
2019; Sadaf et al., 2017). Furthermore, Mohamed et al. (2017), has
reported 32% increase in growth and 60% increase in yield of wheat
crop after applying switchgrass derived BCs. Furthermore, Akhtar
et al. (2015) found 14.2% increase in germination rate, 8.6% in
shoot length, 22.3% in shoot biomass, 10.2% in spike length and
37.8% in grains yield of wheat crop using commercially available BC.
3.3. Impacts of biochars on human health risks
3.3.1. Impacts on hazard risk index of wheat grains
Fig. 6 summarize adults and children HRI results calculated for
consumption of wheat grains cultivated on the BCs treated soil and
industrial wastewater irrigated soil. While percent decrease in HRI
of adults and children is shown in Fig. 7 of both adults and children.
The overall results revealed that wheat (grains) cultivated on con-
trol soil has highest HRI (especially for adults) results for all the
PTEs which shows free mobility of PTEs from soil to grains. While
conversely, the BCs amended soils have comparatively lower values
of HRI in adults for all PTEs which indicate the efficacy of the BCs on
immobilization of PTEs in BCs treated soil. The HRI of Zn in children
was found in the toxicity limit while in adults it was in the safe level
in control samples. The BCs application of 2% did not show any
efficient results in decrease of the children HRI, while 5% applica-
tion showed more efficient results and decreased it to the safe limit
(HRI < 1). In control samples, the HRI of As in children exceeding
the safe limit, which was significantly (p  0.05) decreased by both
2% and 5% BCs application and found in the safe limit. While the
adults HRI was already in the safe limit. The decrease in the HRI was
73%, 71%, 69%, 65%, 62% and 60% by 800BC5, 600BC5, 400BC5,
800BC2, 600BC2 and 400BC2 application, respectively in both
adults and children. The HRI of Ni in children was found in the
toxicity level, while its’s adults HRI was in the safe limit in control
samples. Both 2% and 5% application of the BCs could reduce the
toxicity level of children’s HRI to safe level, and 800BC5, 600BC5,
400BC5, 800BC2, 600BC2 and 400BC2 could decrease up to 76%,
73%, 72%, 68%, 64% and 61% HRI, respectively, in both adults and
children. The HRI of Pb was exceeding the safe limit in both adults
and children in control samples. The BCs application could reduce
the HRI of Pb significantly (p  0.05) to the safe limit (HRI < 1). The
HRI of Cd was found in the toxicity level (HRI > 1) in control
samples. All the BCs (except 400BC2 in children) showed significant
(p  0.05) reduction (both adults and children) in its toxicity. The
HRI of Mn was found in the toxicity level in control samples. None
of the BCs by 2% or 5% application could efficiently decrease its
toxicity level, even though its HRI was decreased 38e48% by the
BCs. The HRI of Cu was exceeding the safe limit in control samples.
The BCs application (2% and 5%) reduced the adults HRI below the
toxicity level (except 400BC2) but no BC neither 2% nor 5%
decreased the children HRI to the safe limit, although a decrease of
600BC2 800BC2 400BC5 600BC5 800BC5
88.73 ± 1.46 90.83 ± 1.49 95.48 ± 1.57 97.38 ± 1.60 98.84 ± 1.63
58.35 ± 0.96 60.35 ± 0.99 64.73 ± 1.06 70.37 ± 1.16 73.38 ± 1.21
12.88 ± 0.21 13.68 ± 0.22 14.83 ± 0.24 16.76 ± 0.28 18.73 ± 0.31
10.23 ± 0.17 10.54 ± 0.17 11.68 ± 0.19 13.28 ± 0.22 15.85 ± 0.26
3.67 ± 0.06 3.94 ± 0.07 4.02 ± 0.07 4.24 ± 0.07 4.84 ± 0.08
12.56 ± 0.21 13.43 ± 0.22 14.67 ± 0.24 16.28 ± 0.27 18.77 ± 0.31
3.63 ± 0.06 3.96 ± 0.07 4.12 ± 0.07 4.41 ± 0.07 4.94 ± 0.08
 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
Fig. 6. Decrease in adults and children hazard risk index of wheat grains after applying biochars.
Fig. 7. Percent decrease in hazard risk index of wheat grains after applying biochars.
68%, 65%, 63%, 58%, 55% and 53% was recorded for 800BC5, 600BC5,
400BC5, 800BC2, 600BC2 and 400BC2, respectively (both in adults
and children). Among all the PTEs, Co, Cr and Fe HRI’s were found in
the safe limit for both adults and children causing no significant
health risks, but these were still decreased 55e67% (Co), 78e93%
(Cr) and 38e51% (Fe) with the BCs application. The control samples
HRI of both adults and children was found in the decreasing order
of Pb > Cd > Mn > Cu > Zn > As > Ni > Co > Fe > Cr. Furthermore,
the decrease in the overall HRI of the PTEs after the BCs application
9
was found in the decreasing order of 800BC5 > 600BC5 > 400BC5 >
800BC2 > 600BC2 > 400BC2 > control in both adults and children.
The overall results revealed that higher HTT pyrolyzed BC and 5%
application have comparatively lower HRI results than lower HTT
pyrolyzed BC and 2% application. Moreover, the highest HTT
(800
C) and 5% application rate pyrolyzed BC (i.e. 800BC5) showed
the most optimum results in the decrease of HRI in both adults and
children than the other BCs and application rate. In a nutshell,
wheat cultivated on wastewater irrigated soil causes significant
health risks while BCs application diminishes it and ensures food-
safety-security throughout food chain. The results of the present
study are consistent with Khan et al. (2014), who has found HRI for
As, Cd, Cu, Mn, Pb and Zn > 1 in contaminated soil and reported
high toxicity, and Khan et al. (2016) who found HRI for Cd, Cr and
Ni > 1 in wheat and declared health risk for the residents of the
study area. Chary et al. (2008) and Khan et al. (2017) have also
found higher HRI for Cr and Zn and Cd and Zn and lower HRI for Co,
Cu, Ni and Pb and Co, Cr, Cu, Fe, Mn and Ni, respectively than this
study results and declared that intake with such HRI values induce
health risks and reported skin diseases attributed especially to Cr,
Pb and Zn. Other studies (Farahat et al., 2017; Bermudez et al., 2011)
had found lower HRI than the present study for Cd, Cr, Cu, Ni, Pb
and Zn and Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn, respectively in
wheat cultivated on wastewater irrigated soil and in the vicinity of
an industrial estate. Furthermore, this study most results in
decrease of HRI are consistent with Yousaf et al. (2018), who re-
ported significant (p  0.01) reduction in HRI of Cd (77%), Cr (73%),
Ni (68%) and Pb (78%) in wheat crops treated with 2% application of
pinewood saw dust derived BC. They have recommended BC
application to industrial wastewater irrigated soil for (i) alleviation
of health risks associated with consumption of PTEs contaminated
10 N. Muhammad et al. / Environmental Pollution 260 (2020) 113887
wheat and (ii) ensuring food safety and security. Similarly, Nawab
et al. (2018b) has decreased HRI of As, Cd, Cr, NI, Pb and Zn up to
73%, 36%, 64%, 74%, 69% and 38% with 5% application of BC (pro-
vided by institute of urban environment, Chinese academy of sci-
ences, China). They conclusively stated that 5% application of BC has
significantly (p  0.05) decreased HRI than 1% and 2% application
and declared that BC are more efficient than other organic
amendments (i.e. farmyard manure and peat moss) in reduction of
HRI (both in adults and children). Other studies (e.g. Khan et al.,
2014) have also significantly (p  0.05) reduced As (67%), Cd
(68%), Cu (29%), Mn (39%), Pb (38%), Zn (22%) after applying of
sewage sludge derived BC.
4. Conclusion
In the present study, the impacts of various BCs were investi-
gated on the bioaccumulation of PTEs, agronomic properties and
human health risks of wheat crop cultivated on long-term indus-
trially contaminated soil. The characterization results of BCs indi-
cated that there was a significant positive correlation between
fundamental characteristics of BCs and high HTT. The analytical
results of wheat crop showed that the application of BCs signifi-
cantly (p  0.05) decreased the concentration of PTEs in roots,
shoots, leaves and grains of the wheat plant, while the agronomic
properties were enhanced dramatically. The human health risks of
PTEs were significantly (p  0.05) decreased from toxicity level to
safety level (except for Mn and Cu) after the BCs application. Based
on the current study, the BCs (especially 800BC5) were recom-
mended for decreasing bioaccumulation of the PTEs in wheat plant,
increasing growth and yield of wheat crop and mitigating human
health risks.
CRediT authorship contribution statement
Nisar Muhammad: Conceptualization, Methodology, Formal
analysis, Data curation, Writing - original draft. Mohammad
Nafees: Funding acquisition, Resources. Muhammad Haya Khan:
Software, Writing - review & editing. Liya Ge: Data curation,
Writing - review & editing. Grzegorz Lisak: Supervision, Writing -
review & editing.
Acknowledgments
This research was financially supported by Higher Education
Commission Pakistan under International Research Support
Initiative Program (No: 1-8/HEC/HRD/2018/8939, PIN: IRSIP 41 BMS
83). We acknowledge Residues and Resource Reclamation Centre,
Nanyang Technological University Singapore for providing instru-
mental facilities. The authors declare no conflict of interests.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.envpol.2019.113887.
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