Bioresource Technology 228 (2017) 218–226

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Cumulative effects of bamboo sawdust addition on pyrolysis of sewage

sludge: Biochar properties and environmental risk from metals
Junwei Jin a, Minyan Wang b,1, Yucheng Cao a, Shengchun Wu a, Peng Liang a, Yanan Li a, Jianyun Zhang a,
Jin Zhang a,c,⇑, Ming Hung Wong c, Shengdao Shan d, Peter Christie a,e
a
Key Laboratory of Soil Contamination Bioremediation of Zhejiang Province, School of Environmental and Resource Sciences, Zhejiang Agriculture and Forestry University, 88
Huancheng North Road, Lin’an, Hangzhou 311300, China
b
Jiyang College, Zhejiang Agriculture and Forestry University, 77 Puyang Road, Zhuji 311800, China
c
Consortium on Health, Environment, Education and Research (CHEER), Department of Science and Environmental Studies, The Education University of Hong Kong, 10 Lo Ping Road,
Tai Po, Hong Kong Special Administrative Region
d
Institute of Ecology and Environment, Zhejiang University of Science and Technology, 318 Liuhe Road, Hangzhou 310023, China
e
Institute of Soil Science, Chinese Academy of Sciences, 71 East Beijing Road, Nanjing 210008, China

h i g h l i g h t s g r a p h i c a l a b s t r a c t

Sludge was pyrolyzed with bamboo

sawdust for metal immobilization.

Metals were transformed from highly
available to stable forms after
pyrolysis.

Addition of bamboo sawdust in
sludge co-pyrolysis minimizes the
risk from metals.

Co-pyrolysis with bamboo sawdust at
600 °C is suitable for sludge metal
stabilization.

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

Article history: A novel type of biochar was produced by mixing bamboo sawdust with sewage sludge (1:1, w/w) via a co-
Received 25 October 2016 pyrolysis process at 400–600 °C. Changes in physico-chemical properties and the intrinsic speciation of
Received in revised form 22 December 2016 metals were investigated before and after pyrolysis. Co-pyrolysis resulted in a lower biochar yield but
Accepted 27 December 2016
a higher C content in the end product compared with use of sludge alone as the raw material. FT-IR anal-
Available online 30 December 2016
ysis indicates that phosphine derivatives containing PAH bonds were formed in the co-pyrolyzed bio-
chars. In addition, co-pyrolysis of sludge with bamboo sawdust transformed the potentially toxic
Keywords:
metals in the sludge into more stable fractions, leading to a considerable decrease in their direct toxicity
Sewage sludge
Bamboo sawdust
and bioavailability in the co-pyrolyzed biochar. In conclusion, the co-pyrolysis technology provides a fea-
Pyrolysis sible method for the safe disposal of metal-contaminated sewage sludge in an attempt to minimize the
Trace metals environmental risk from potentially toxic metals after land application.
Potential environmental risk assessment Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction
⇑ Corresponding author at: Key Laboratory of Soil Contamination Bioremediation
of Zhejiang Province, School of Environmental and Resource Sciences, Zhejiang The current annual production of municipal sewage sludge in
Agriculture and Forestry University, 88 Huancheng North Road, Lin’an, Hangzhou
311300, China.
the European Union is estimated to be >10 million tonnes on a
E-mail address: jzhang@zafu.edu.cn (J. Zhang). dry weight basis (Mininni et al., 2015). Approximately 13 million
1
Co-first author. tonnes (dry weight) of municipal sewage sludges will be produced

http://dx.doi.org/10.1016/j.biortech.2016.12.103
0960-8524/Ó 2016 Elsevier Ltd. All rights reserved.
 J. Jin et al. / Bioresource Technology 228 (2017) 218–226
In China in 2016 (Zhang et al., 2014). In addition, a very large quan-
tity of sludge will inevitably continue to be produced in China, with
a predicted annual rate of increase of around 10% over a ten-year
period (Havukainen et al., 2017; Zhang et al., 2014) due to rapid
continuing economic development and urbanization. The safe dis-
posal of sewage sludge will therefore continue to be a matter of
great concern, not only because of its very large volume but also
because of contamination with potentially toxic elements, micro-
organisms and a range of hazardous organic substances (Fytili
and Zabaniotou, 2008).
Conventional sludge treatment technologies adopted world-
wide include incineration, landfill and land application (Chen
et al., 2012; Fytili and Zabaniotou, 2008). Landfill disposal gener-
ates undesired emissions (e.g. leachate and landfill gas) to ambient
water, soil and air; and incineration is not broadly implemented,
primarily due to its poor public acceptance and high operational
cost. In addition, it has been well documented that land application
of sludge may pose a highly environmental risk to waters and soils
and even to human health since the contaminants released may
enter the food chain (Jin et al., 2016). Sludge is therefore allowed
to be applied only for non-food crop production in many countries
(Kirchmann et al., 2016). There remains an urgent need to develop
alternative technologies for the safe management of sewage
sludge.
Pyrolysis is a promising strategic approach to the sustainable
management of sewage sludges and has been extensively revis-
ited recently (Agrafioti et al., 2013; Chen et al., 2014a). Pyrolysis
minimizes the volume of sludge, kills the pathogens and parasites
present, and also (more importantly) transforms organic sub-
stances to bio-energy (e.g. bio-oil and pyrolytic gas) (Cao and
Pawłowski, 2012) and immobilizes metals in a charred residual
carbonaceous solid material (termed ‘sludge biochar’) (Agrafioti
et al., 2013; Chen et al., 2014a; Devi and Saroha, 2014; Jin
et al., 2016). Our previous study indicates that metals in the sew-
age sludge can be substantially transformed from weakly bound
forms to a more stable state (in oxidizable and residual forms)
via the pyrolysis process (Jin et al., 2016), thus lowering the envi-
ronmental risk involved in the land application of sludge bio-
chars. Taking into account the numerous metals and metalloids
co-existing in sewage sludges (Cheng et al., 2014), a more robust,
stable and efficient method of metal stabilization in sludge bio-
chars is a prerequisite for practical land application (e.g. as a soil
amendment or adsorbent) to minimize the environmental risk.
This may be achieved by using some additives which are able
to enhance the immobilization of potentially toxic elements dur-
ing the pyrolysis process.
Bamboo is a major biomass crop that is widely cultivated in
west and south China. In 2012 the annual production of bamboo
reached 1.64 million pieces nationwide (Li et al., 2016). Unavoid-
ably, large amounts of bamboo processing wastes were gener-
ated. Because of its very high lignocellulose content, bamboo is
regarded as an excellent raw material for biochar production.
It was reported that bamboo biochar had approximately ten
times the surface area and four times the sorption capacity of
charcoal (Xu et al., 2012). Moreover, it suspected to have a spe-
cial type of pore composed of onion-like fullerenes (C60) with a
structure of expanded carbon nanotubes (Xu et al., 2012). This
indicates that bamboo biochar might have great potential to
immobilize metals (Shao et al., 2015). In the present study bam-
boo sawdust was therefore selected as an additive in the pyrol-
ysis of sewage sludge for further stabilization of metals because
of its specific biological matrix and its structural and morpholog-
ical properties.
It has been postulated that the addition of bamboo sawdust to
sewage sludge during the co-pyrolysis process might lead to a syn-
ergistic enhancement effect on the immobilization of metals in the
219
biochar end product and consequently allow a further substantial
decline in environmental risk compared with the pyrolysis of
sludge alone. Hence, the objectives of the present work were (1)
to validate the synergistic effect of bamboo sawdust addition on
biochar properties and the intrinsic immobilization of metals, (2)
to reveal the changes in metal fractions in the biochars with
increasing pyrolysis temperature before and after addition of bam-
boo sawdust, and (3) to assess the potential environmental risk of
metals in the biochars.
2. Materials and methods
2.1. Preparation of biochar
The bamboo sawdust was collected from a moso bamboo (Phyl-
lostachys pubescens) processing factory in Lin’an city, Zhejiang pro-
vince, east China. The raw sewage sludge was sampled in the
dewatering room of the First Municipal Wastewater Treatment
Plant in the same city in which the triple oxidation ditch process
for wastewater treatment was used. The bamboo sawdust was
dried to constant weight in a laboratory oven (70 °C) and the
sewage sludge was air-dried at room temperature (20 °C). The
two feedstocks were then ground and passed through a 120-
mesh sieve, packed in sealed plastic bags and stored in a desiccator
for further use.
Co-pyrolysis of sewage sludge and bamboo sawdust was con-
ducted in a pyrolysis and carbonization furnace (Fig. 1) at 400,
500 or 600 °C. In detail, the furnace was first heated to the desig-
nated temperature and 400 g of thoroughly mixed feedstock (sew-
age sludge/bamboo sawdust, 1:1, w/w) was then fed into the
internal reaction zone of the furnace through the inlet tube at a
constant rate (Fig. 1). After pyrolysis for 1 h the residual biochar
was left to cool to room temperature (20 °C) and transferred to
a sealed plastic bag for further analysis. A constant flow of N2 of
1 Lmin1 was maintained throughout the pyrolysis and cooling
stages to ensure O2-free conditions in the internal reaction zone
of the furnace (Jin et al., 2016). A single pyrolysis process to convert
sewage sludge to biochar (as control) was conducted under the
same conditions as those used for the co-pyrolysis.
2.2. Elemental and physico-chemical properties of the biochar
The total carbon (C), hydrogen (H), nitrogen (N) and sulfur (S)
contents of the raw sewage sludge (SS), the bamboo sawdust
(BS), the sewage sludge biochar (SSB) and the sludge and bamboo
co-pyrolyzed biochar (SBB) samples were determined by dry com-
bustion at 950 °C using an automatic elemental analyzer (Vario EL
III, Hanau, Germany). An internal catalyst, tungsten (VI) oxide, was
added to each sample to accelerate its complete combustion.
External calibration standards, CaCO3 and sulfanilic acid, were ana-
lyzed after every ten samples for data quality control (Zhang et al.,
2013).
The pH values of the sewage sludge, sewage sludge biochar and
sludge and bamboo biochar samples (sample/water, 1:20, w/v)
were measured with a pH meter (SevenCompact, Mettler Toledo,
Greifensee, Switzerland) (Yuan et al., 2015). The ash content of
the samples was determined according to the standard Industrial
Analysis Method for Coal (GB/T 212-2001). The specific surface
area of the samples was tested using N2 sorption isotherms run
on an automated surface area and pore size analyzer (SI-MP-10,
Quantachrome Corp., Boynton Beach, FL) and were taken from
adsorption isotherms using the Brunauer, Emmett and Teller
(BET) equation (Ure et al., 1993). The detailed pH, elemental and
BET values of the raw materials and the biochars are listed in
Table 1.
220 J. Jin et al. / Bioresource Technology 228 (2017) 218–226

Fig. 1. Schematic diagram of the pyrolysis apparatus used.

2.3. Fractionation and determination of metals
The metals in the raw sewage sludge, sewage sludge biochars,
and the sludge and bamboo co-pyrolyzed biochars were sequen-
tially extracted using the modified three-step sequential extraction
procedure which was proposed by the Commission of the Euro-
pean Communities Bureau of Reference (BCR) (Long et al., 2009;
Sungur et al., 2014). The detailed extraction scheme is shown in
Table 2. Using BCR sequential extraction the metals can be divided
into four fractions, namely the exchangeable and acid soluble (F1),
the reducible (F2), the oxidizable (F3), and the residual (F4) frac-
tions (Huang and Yuan, 2016).
The concentrations of metals in the first three fractions (F1, F2,
and F3) were determined directly by inductively coupled plasma-
optical emission spectrometry (ICP-OES, Prodigy 7, Teledyne Lee-
man Labs, Hudson, NH). The residual fractions and the total con-
centrations of metals in the samples were firstly digested
according to the US EPA 3050B method (Lorentzen and Kingston,
1996) before detection by ICP-OES.
2.4. Statistical analysis
Statistical analysis was performed using the SPSS statistical
package (v. 20.0). The data were subjected to analysis of variance
procedures and mean values were separated using the protected
least significant difference test at the 0.05 level of probability.
3. Results and discussion
3.1. General properties of the biochars
The properties of the feedstocks (the sewage sludge and the
bamboo sawdust) and of the biochars derived from pyrolysis of
the sludge alone and from co-pyrolysis of the sludge and the bam-
boo sawdust are shown in Table 1. The percentage of sewage
sludge biochar yield declined steadily from 60.6 to 53.1% as the
pyrolysis temperature increased from 400 to 600 °C due to the
gradual decomposition of organic substances in the sludge (Jin
et al., 2016). Similar observations were reported by Chen et al.
(2014b) and Yuan et al. (2015). Addition of bamboo sawdust to
sewage sludge for co-pyrolysis led to a decrease in biochar yield
(Table 1) owing to the lower ash content of bamboo sawdust
(2.0%) than of sewage sludge (41.3%). Al-Wabel et al. (2013)
reported higher yields related to higher weights of inorganic con-
stituents of feedstock materials as indicated by their relatively high
ash contents. For example, Ahmad et al. (2012) observed that ani-
mal litter and solid waste generated a higher yield of biochar com-
pared to crop residues and wood biomass.

Table 1
Physico-chemical properties of the feedstocks and their biochars obtained under different pyrolysis temperatures.

Sample Yield C H N S H/C C/N pH Ash SSA

(%) (%) (%) (%) (%) (%) m2 g1
BS / 48.5 h 3.35 e 0.75 a 0.28 a 0.07 64.68 ND 2.04 a ND
SS / 26.5 da 6.24 f 4.08 g 0.90 d 2.83 7.59 7.19 a 41.3 b 0.68
SSB400 60.6 21.9 c 1.85 d 3.10 f 0.85 c 1.01 0.12 8.46 b 64.2 f 5.49
SSB500 57.0 21.2 b 1.20 b 2.83 e 0.84 c 0.68 0.11 9.75 d 69.8 g 7.73
SSB600 53.1 19.9 a 0.71 a 2.04 c 0.87 cd 0.43 0.09 11.70 g 74.0 h 5.99
SBB400 44.5 31.2 g 1.84 d 2.10 d 0.53 b 0.71 0.06 9.55 c 52.6 c 2.78
SBB500 44.5 30.4 f 1.63 c 2.01 c 0.56 b 0.64 0.06 10.11 e 58.3 d 4.50
SBB600 41.1 30.2 e 1.16 b 1.76 b 0.51 b 0.46 0.05 11.64 f 61.9 e 8.49

BS, bamboo sawdust; SS, sewage sludge; SSBx, biochar derived from sewage sludge pyrolysis at X (°C) temperature; SBBx, biochar derived from co-pyrolysis of the sewage
sludge and bamboo sawdust at X (°C) temperature.
SSA, specific surface area determined using sorption isotherms.
ND, not detected.
ɑ
Within each column, mean values followed by the same lowercase are not significantly different at the 5% level.

Table 2
Modified BCR three-step sequential extraction procedure.
Fraction
F1 Soluble and exchangeable metals
F2 Carbonates, oxides and reducible
metals
F3 Metals bound to organic matter,
oxidisable and sulphidic metals
F4 Residual metals such as silicates
3000
HMs total concentration (mg kg-1)
2000
1000
180
90
0
SS BS SSB400 SSB500 SSB600 SBB400 SBB500 SBB600
Fig. 2. Total concentrations of the metals in the raw sludge, the bamboo sawdust,
the sludge biochars, and the bamboo and sludge co-pyrolyzed biochars. SS, raw
sewage sludge; BS, the bamboo sawdust; SSBx, biochar derived from sewage sludge
pyrolysis at X (°C) temperature; SBBx, biochar derived from co-pyrolysis of the
sewage sludge and the bamboo sawdust at X (°C) temperature.
Pyrolysis led to a significant increase in the ash contents of the
residual biochars and the higher the temperature, the higher the
ash content (Table 1). However, addition of bamboo sawdust for
co-pyrolysis of the sewage sludge resulted in an approximately
16% decrease in ash content in the biochar compared to that
derived from single pyrolysis of the sludge irrespective of temper-
ature between 400 and 600 °C. A significant positive correlation
was observed between pyrolysis temperature and ash content of
the sludge biochars (r = 0.997, p < 0.01) and between ash content
of the sludge and bamboo biochars (r = 0.992, p < 0.01), suggesting
that most of the inorganic constituents in the feedstocks were con-
centrated and retained in the biochars during pyrolysis (Cha et al.,
2016).
The pH values of the raw sludge and the bamboo sawdust were
close to neutral. Pyrolysis increased the pH of the resultant bio-
chars to alkaline (Table 1) and the higher the temperature, the
more alkaline the biochars. Addition of bamboo sawdust and co-
pyrolysis with the sludge resulted in a slightly higher pH value
compared to pyrolysis of the sludge alone at the same temperature,
especially at the lower pyrolysis temperatures (e.g. 13% higher pH
at 400 °C), possibly due to the fact that bamboo sawdust addition
promoted the transformation of metallic compounds to the oxidiz-
able and residual fractions in the biochars (Fig. 3). Furthermore,
there was a substantial positive relationship between the ash con-
J. Jin et al. / Bioresource Technology 228 (2017) 218–226 221
tents and the pH values of both the sludge biochars (r = 0.980,
p < 0.01) and the sludge and bamboo co-pyrolyzed biochars
Extraction Extraction (r = 0.926, p < 0.01), suggesting that inorganic residues in the bio-
reagents conditions chars might be a major factor involved in the pH increase of the
20 mL, 0.01 M Oscillating, biochars (Yuan et al., 2011). However, it was observed that the
HAc 22 ± 5 °C, 16 h pH values of the sludge biochar and the sludge and bamboo co-
20 mL, 0.50 M Oscillating, pyrolyzed biochar were highly negatively correlated with the
NH2OHHCl 22 ± 5 °C, 16 h
First, 5 mL, 30% First, water
molar ratio of H/C of the biochars (r = 0.981, p < 0.01; r = 0.999,
(v/v) H2O2, bath, 85 ± 5 °C, p < 0.01, respectively), indicating that aromaticity during pyrolysis
Next, 5 mL, 30% 1 h, also had effect on the pH value of the biochar, a finding consistent
(v/v) H2O2, Next, water with the results of Chen et al. (2014b).
Last, 25 mL, bath, 85 ± 5 °C,
The specific surface area of the sludge biochar was approxi-
1.0 M 1 h,
CH2COONH4 Last, Oscillating, mately ten times higher than that of the sludge with pyrolysis tem-
22 ± 5 °C, 16 h perature ranging from 400 to 600 °C (Table 1). Compared with
5 mL, HNO3 Microwave 600 °C, lower specific surface areas of the biochars were observed
digestion when bamboo sawdust was added with co-pyrolysis of the sludge
system
at 400 and 500 °C (Table 1). Thermal degradation of hemicellulose
and cellulose in biomass has been reported to occur at 220–315 °C
and at 315–400 °C, respectively (Al-Wabel et al., 2013), and tar
produced in the process tends to adhere to the biochar surface,
Cu
Zn resulting in blockage of the porous structure (Singh et al., 2012).
Pb As the temperature continues to rise (e.g. to 600 °C) the continuing
Cr
Mn breakdown of the tar (partially transformed to pyrolytic gas) might
Ni favor the formation of micropores in the biochar.
Pyrolysis of sludge reduced the contents of C, H, N and S in the
resultant biochars, and the higher the temperature, the lower the
C, H and N (but not S) contents (Jin et al., 2016). Addition of bam-
boo sawdust and co-pyrolysis with the sludge led to increased C
and H contents and decreased N and S contents in the biochars
compared to the sludge biochars produced at the same tempera-
tures (Table 1). The H/C value was used to characterize the degree
of aromaticity of the biochars (Zhang et al., 2011). A molar H/C
ratio 60.3 generally indicates highly condensed aromatic ring sys-
tems whereas H/C P0.7 suggests non-condensed structures
-- (Uchimiya et al., 2011; Xiao et al., 2016; Zhang et al., 2011).
According to the index, the sludge biochar produced at 400 °C
(H/C = 1.01) had no condensed aromatic ring structure. Addition
of bamboo sawdust and co-pyrolysis with the sludge contributed
to condensation in which H/C ratio decreased to 0.71 at 400 °C
(Table 1). When the pyrolysis temperature was raised from 500
to 600 °C the H/C ratio of the biochar changed from 0.65 to
0.45 irrespective of whether bamboo sawdust was added, indi-
cating the occurrence of aromatic clusters. Furthermore, the
molecular structure and aromatic cluster of biochar can be pre-
dicted based on the rectangle-like polycyclic aromatic model
established by Xiao et al. (2016). For example, here the H/C values
of the sludge biochars and the sludge and bamboo co-pyrolyzed
biochar obtained at 400 °C were 1.01 and 0.71, respectively, and
the corresponding aromatic clusters in the two biochars were dis-
tributed in an approximately 1  1 rectangle (H/C = 1.0000 in the
model); the aromatic cluster of biochars obtained at 500 °C (H/
C = 0.68 and 0.64, respectively) was a 2  2 rectangle (H/
C = 0.6250 in the model) while the biochars produced at 600 °C
(H/C = 0.43 and 0.46, respectively) had a 3  3 rectangle aromatic
cluster structure (H/C = 0.4667 in the model). This may be attribu-
ted to the pyrolysis temperature rather than the biomass feedstock
determining the clustering of the aromatic structures in biochars in
the present study. This is consistent with the results of Wiedner
et al. (2013) who found that temperature was the main driver
determining the chemical composition of hydrochars in hydrother-
mal carbonization of agricultural and forestry by-products. On the
other hand, the stability of biochar increased with increasing
pyrolysis temperature as higher aromaticity formed. The molar
N/C ratio was consistent with the changing trend of H/C and
decreased with increasing pyrolysis temperature. This implies that
the contents of N-related functional groups in the biochars were
222 J. Jin et al. / Bioresource Technology 228 (2017) 218–226

Concentration percentage(%)
Concentration percentage(%)
100 gfe 100 g f ed
g dbc Zn cb
Cu fg a
80 e a 80
c d b gf
g
60 60 e ef d

40 40 c
f d
g f cba
ed b
20 g 20 e g
dfe dabcd ef
abdce f cba a abc a abcd
0 0
F1 F2 F3 F1+F2+F3 F4 F1 F2 F3 F1+F2+F3 F4
Concentration percentage(%)

Concentration percentage(%)
100 100
Pb g g g Cr g
fe f g f
80 d 80 g
e g f
e
60 60 f c d
fg e e d
f e d
40 40 b c
e c d c a
d d b c f b b
20 cb cb a ab 20 ed a
a g f ebdca cba
a a
0 0
F1 F2 F3 F1+F2+F3 F4 F1 F2 F3 F1+F2+F3 F4
Concentration percentage(%)

Concentration percentage(%)
100
Mn dg fe 100
Ni fg
c f e
80 80 dc e c cad b
g b b
f
60 a 60 g
e
d g g
40 cb e f f 40
g e
f
e
a egd f
20 d d e 20 ba c
ba c c da bc f
ab cbdaaa ecdab a
0 0
F1 F2 F3 F1+F2+F3 F4 F1 F2 F3 F1+F2+F3 F4

SS SSB400 SSB500 SSB600 SBB400 SBB500 SBB600

Fig. 3. Fraction distribution of metals in the raw sludge, the sludge biochars and the bamboo and sludge biochars. Within each fraction of each metal, bars with the same
lowercase letter are not significantly different at the 5% level. SS, raw sewage sludge; SSBx, biochar derived from sewage sludge pyrolysis at X (°C) temperature; SBBx, biochar
derived from co-pyrolysis of the sewage sludge and the bamboo sawdust at X (°C) temperature. F1, exchangeable and acid-soluble fraction; F2, reducible fraction; F3,
oxidizable fraction; F4, residual fraction.

declining as the temperature increased (Hu et al., 2016). Addition 3.2.2. BCR extractable fractions
of bamboo sawdust and co-pyrolysis with the sludge led to a 50% The bioavailability and toxicity of metals in the environment
reduction in N/C values in the biochars, mainly due to the ‘dilution depend mainly on their chemical speciation (Huang and Yuan,
effect’ caused by the addition of the bamboo sawdust which had a 2016) and this can be assessed using the modified BCR sequential
very low N content (0.8%, Table 1). extraction scheme (Chen et al., 2008; Rauret et al., 1999). In accor-
dance with the BCR results (Table 2), the metals in sludge can be
3.2. Metal analysis categorized into four fractions: the acid soluble and exchangeable
fraction (F1), the reducible fraction (F2), the oxidizable fraction
3.2.1. Total metal concentrations (F3) and the residual fraction (F4) (Huang and Yuan, 2016). The
The total concentrations of metals in the raw sludge, the bam- bioavailability and mobilization of metal fractions decrease in the
boo sawdust, the sludge biochars, and the sludge and bamboo following sequence: F1 > F2 > F3 > F4 (Chen et al., 2015) and can
co-pyrolyzed biochars are shown in Fig. 2. In general, concentra- be divided into three categories (Huang and Yuan, 2016). Metals
tions of metals in the bamboo sawdust were very low (e.g. Cu distributed in F1 and F2 are readily available for uptake by plants
3.64 mg kg1 DW, highest of all the metals determined). The total or in surface waters, and are thus identified as the directly toxic
concentrations of different metals in the sludge and its biochars and bioavailable species. The F3 fraction can be degraded, leading
followed the sequence Zn > Cu > Mn > Cr > Ni > Pb. Zinc was pre- to the release of soluble metals under oxidizing conditions, and is
sent at much higher concentrations than other metals in the raw thus identified as the potentially toxic and bioavailable species.
sludge (2580 mg kg1 DW) and may have been derived mainly The F4 fraction is recognized as non-toxic and non-bioavailable
from the galvanized sewer pipes used extensively in Chinese cities because the residual solids containing mainly primary and sec-
(Cheng et al., 2014; Weng et al., 2010) or some specific industrial ondary solids occlude the metals in their crystalline structures
sewage discharges. The total concentrations of the six metals (Devi and Saroha, 2014; Fuentes et al., 2008).
determined in the sludge biochars were enriched by pyrolysis Fig. 3 shows the percentage concentrations of the six metals in
and increased with increasing pyrolysis temperature (Fig. 2), sug- four BCR fractions in the raw sludge and its biochars (SS, SSBx, and
gesting that transfer of the metals into bio-oil or pyrolytic gas SBBx). Over 55% of all six metals in the raw sludge was accounted
was less important than the decomposition of organic compounds for in the reducible (F2) fraction and >82% in the directly and
in the sludge during pyrolysis (Lu et al., 2012), leading to accumu- potentially toxic and bioavailable category (F1 + F2 + F3). This indi-
lation of metals in the residual biochar. Addition of bamboo saw- cates the high environmental risk of the raw sludge applied to the
dust and co-pyrolysis with the sludge led to a reduction of land. A sharp decline occurred after conversion of the raw sludge to
approximately 50% in the concentrations of metals in the sludge biochar via pyrolysis and the higher the temperature, the lower the
and bamboo biochars at the corresponding temperatures (Fig. 2), percentage in the directly and potentially toxic or bioavailable
again, mainly due to a ‘‘dilution effect” owing to the added bamboo fractions (F1 + F2 + F3). Then a steady increase in the non-toxic
sawdust (Fig. 2). and bioavailable fraction (F4) in biochar with increasing pyrolysis
 J. Jin et al. / Bioresource Technology 228 (2017) 218–226
temperature from 400 to 600 °C was observed (Fig. 3). For example,
the percentage of Cu in the F4 fraction in the biochar obtained at
600 °C increased markedly by 4.4 times over that in the biochar
obtained at 400 °C. Similarly, the percentages of Zn, Pb, Cr, Mn,
and Ni in F4 fraction in biochar obtained at 600 °C increased
greatly by 2.5, 1.8, 6.1, 8.4, and 2.1 times, respectively, compared
to that in the biochar derived at 400 °C, suggesting on one hand
that a large percentage of unstable metals in raw sludge was
immobilized by pyrolysis. On the other hand, the percentage of
metals in potentially toxic forms decreased with increasing pyrol-
ysis temperature.
Further stabilization of these metals was achieved by addition
of bamboo sawdust and co-pyrolysis of the sludge (Fig. 3) in which
the ratio of Cu in the reducible fraction (F2) in the co-pyrolyzed
biochars declined significantly and in the residual fraction (F4,
non-toxic and non-bioavailable) increased dramatically, and the
percentage in the F4 fraction increased with increasing tempera-
ture (Fig. 3). After co-pyrolysis at 600 °C approximately one quarter
of the Cu was occluded in the F4 fraction in the residual biochar,
3.2 times more than in the single pyrolysis biochar. Zn showed a
similar trend to Cu (Fig. 3). Lead performed better than Cu or Zn,
with addition of bamboo sawdust significantly decreasing the per-
centage of Pb in F2 and F3 fractions and with 69.0–86.1% of Pb
occluded in the F4 fraction with increasing temperature from 400
to 600 °C. After addition of bamboo sawdust and co-pyrolysis with
the sludge there was no partitioning of Ni in the F1 fraction and the
percentage in F2 also clearly decreased, resulting in transfer of the
directly toxic and bioavailable forms of Ni to the relatively stable
state (72% occluded in the potentially toxic and bioavailable frac-
tion and 26% in the non-toxic and bioavailable fraction at
600 °C). Chromium showed a similar trend in the percentage in
the directly toxic and bioavailable category (F1 + F2) decreasing
markedly and approximately 70% of Cr occluded in the non-toxic
and bioavailable fraction (F4) pyrolyzed at 600 °C. After bamboo
sawdust addition the percentage of Mn in the F2 fraction decreased
markedly and the percentage in F3 more than tripled.
In summary, each metal differed in distribution pattern in the
four fractions. However, all the metals in the directly toxic and
bioavailable category (F1 + F2) in the sludge were found to decline
significantly as a result of pyrolysis (Fig. 3). Furthermore, addition
of bamboo sawdust and co-pyrolysis with the sludge led to further
transformation of the metals to more stable forms occluded in the
oxidizable and residual fractions. Shi et al. (2013) found similar
results in studies of rice husk (RH) addition on hydrothermal treat-
ment (HTT) of sewage sludge. They postulated that an RH-sludge
matrix was formed during HTT after RH addition in which the met-
als were further entrapped or chelated with some other functional
groups and then fixed, resulting in an enhanced immobilization
effect on the metals. However, the detailed mechanisms involved
need further elucidation, especially the contribution of organic
ingredients (such as P-H in phosphine formed at the peak of
2360 cm1 by Fourier transform - infrared spectroscopy analysis
during co-pyrolysis of bamboo and sludge, Fig. S1) and inorganic
substances (mainly carbonates and silicates in the feedstocks) in
addition to some functional groups formed during the pyrolysis
process.
3.2.3. Environmental risk assessment
The toxicity and bioavailability of metals in the sludge biochar
matrix must be determined to assess the risk to the environment
in deciding the suitability and the optimum application rate of
the biochar in nutrient recycling (Devi and Saroha, 2014). The
potential ecological risk index (RI) (Huang and Yuan, 2016) has
often been used to assess the degree of potential risk associated
with multiple metals in sewage sludges and their biochars by use
of the following formula as proposed by Hakanson (1980).
223
C f ¼ C i =C n ; ð1Þ
Er ¼ T r  C f ; ð2Þ
X
RI ¼ Er ð3Þ
where, Cf is the contamination factor of individual metals and Ci and
Cn are the metal concentrations in the available (F1 + F2 + F3) and
stable (F4) fractions, respectively (Table 3). Tr is the toxic response
factor of the metals which here are Cu (5), Zn (1), Pb (5), Cr (2), Mn
(1), and Ni (6) (Devi and Saroha, 2014; Hakanson, 1980). Er is
obtained by multiplying the contamination factor of each individual
metal with its toxic factor. RI of the sludge or biochars is the sum of
the potential index of the individual metal. The indices and signifi-
cance of Cf, Er and RI are shown in Table 4.
The Cf, Er and RI data were determined to clarify the risk level
of the metals in the raw sludge, in the sludge biochars and in
the bamboo and sludge biochars (Table 5). For example, com-
pared to the indices in Table 4, the values of Cf for Cu and Zn
in the raw sludge were 88.9 and 135.9, implying very high metal
contamination (Cf > 9 indicates high contamination). After pyrol-
ysis, the value declined significantly and gradually with increas-
ing temperature from 400 to 600 °C (from 55.1 to 11.9 for Cu
and from 58.8 to 23.2 for Zn). However, after addition of bamboo
sawdust to the sludge for co-pyrolysis the Cf value for the two
metals further declined, especially at 600 °C, to a level of moder-
ate contamination (3.1 for Cu and 6.4 for Zn compared to the
indices in Table 4), leading to a low degree of potential environ-
mental risk for Cu and Zn in the sludge and bamboo co-
pyrolyzed biochar produced at 600 °C. Similar changes were also
observed in respect of Pb, Cr, and Ni, with the sole exception of
Mn (Table 5). Although there was a slight increase in the Cf
value of Mn in the bamboo and sludge biochars produced at
500 and 600 °C its potential environmental risk (Er) remained
very low.
Consequently, the maximum value of the potential ecological
risk (RI) of the six metals in the raw sludge was 667.7, indicating
a high degree of environmental risk (RI > 600) of soil and water
pollution if applied directly to the environment. However, after
pyrolysis the RI of the resultant biochar declined substantially,
but only when the temperature increased to 600 °C did the RI
of the sludge biochar (109.1) reach a low degree of potential eco-
logical risk (RI 6 150). Nevertheless, after bamboo sawdust addi-
tion and co-pyrolysis, the RI value of the resultant biochar was
much lower than 150 irrespective of the pyrolysis temperature
within the range 400–600 °C (Table 5). After co-pyrolysis at
600 °C the RI value of the bamboo and sludge biochar strongly
decreased to the lowest value of 43.1, indicating a very low
degree of potential ecological risk if the biochar were recycled
in the environment.
Differences in the properties of biochars can significantly influ-
ence their effects on soil and water quality after return to the
environment. For example, Méndez et al. (2013) found that soil
field capacity and available water increased after amendment
with sewage sludge biochar obtained at 600 °C while differences
were not observed in the case of sludge biochar obtained at
400 °C. It should also be noted that pyrolysis is a thermochemical
decomposition process during which biomass is heated at ele-
vated temperatures (300–650 °C) in the absence of oxygen
(Kambo and Dutta, 2015), thus the net energy balance for pyrol-
ysis should be taken into account. It is believed that the cost
increases when using a pyrolysis process at higher temperatures.
However, Rafiq et al. (2016) found that the net energy balance
was higher at higher temperatures in the pyrolysis of corn stover
at 300–500 °C. Previous studies also indicate that pyrolysis tech-
nology has potential energy benefits in addition to sludge biochar
224 J. Jin et al. / Bioresource Technology 228 (2017) 218–226

Table 3
BCR-extractable fraction concentrations of metals in the sewage sludge, the sludge biochars and the sludge and bamboo biochars.

Metal Fraction Sample

SS SSB400 SSB500 SSB600 SBB400 SBB500 SBB600
Cu F1 137.6 ± 1.08ga 7.19 ± 0.13a 17.7 ± 0.41c 33.3 ± 1.52e 12.9 ± 1.67b 18.7 ± 1.52d 60.3 ± 0.63f
F2 1063 ± 27.1g 436.1 ± 6.04f 336.1 ± 26.94e 302.0 ± 21.69d 18.3 ± 0.57c 13.5 ± 0.58b 13.4 ± 1.29a
F3 2.96 ± 0.23a 1080 ± 34.9e 1257 ± 45.6g 1229 ± 55.6f 672.6 ± 7.14b 800.8 ± 19.37d 739.0 ± 25.49c
F4 13.5 ± 0.93a 27.6 ± 0.24b 62.3 ± 1.13c 132.1 ± 1.10f 90.4 ± 6.91d 100.9 ± 15.86e 264.8 ± 15.86g
Zn F1 693.7 ± 44.00g 179.9 ± 9.30d 156.2 ± 5.57c 217.0 ± 7.94e 112.9 ± 3.11a 135.7 ± 11.98b 284.2 ± 8.03f
F2 1867 ± 60.8g 1853 ± 16.1f 1526 ± 35.9e 1110 ± 5.7d 396.5 ± 14.45a 414.4 ± 12.74b 451.1 ± 19.44c
F3 ND 496.7 ± 15.41a 1086.7 ± 42.19c 1902 ± 65.3f 1004 ± 1.1b 1219 ± 20.7e 1128 ± 17.7d
F4 18.8 ± 1.74a 43.0 ± 2.31b 53.4 ± 3.35c 139.0 ± 11.67e 130.5 ± 12.01d 160.9 ± 41.30f 292.9 ± 41.30g
Pb F1 ND ND ND ND ND ND ND
F2 84.0 ± 1.80g 34.0 ± 0.82f 29.9 ± 1.74e 21.6 ± 5.17d 6.43 ± 0.26c 4.69 ± 0.28a 5.90 ± 0.28b
F3 ND 36.0 ± 0.85d 49.1 ± 0.94e 55.3 ± 3.36f 8.65 ± 0.71c 6.40 ± 0.09b 6.27 ± 0.45a
F4 11.1 ± 0.66a 14.7 ± 1.40b 19.8 ± 2.06c 33.8 ± 4.91e 33.5 ± 3.83d 43.3 ± 3.74f 75.2 ± 3.74g
Cr F1 22.4 ± 0.63f 19.4 ± 0.34e 18.4 ± 0.16c 19.2 ± 0.19d 6.49 ± 0.39a 6.46 ± 0.43a 7.13 ± 0.61b
F2 348.0 ± 6.48g 135.9 ± 3.35f 105.2 ± 2.51e 91.7 ± 9.35d 17.4 ± 0.98b 16.0 ± 0.74a 21.5 ± 0.99c
F3 0.58 ± 0.48a 431.8 ± 12.25f 443.3 ± 5.17g 285.6 ± 17.35e 242.8 ± 4.85d 221.1 ± 1.48c 178.2 ± 4.32b
F4 78.2 ± 18.10b 77.8 ± 2.40a 497.9 ± 8.58f 977.9 ± 88.77g 157.2 ± 3.66c 200.6 ± 17.23d 425.5 ± 17.23e
Mn F1 203.3 ± 11.70g 144.8 ± 5.51e 75.2 ± 2.17b 51.4 ± 2.08a 193.9 ± 1.21f 107.2 ± 5.53d 88.5 ± 1.66c
F2 477.0 ± 22.69d 515.1 ± 3.24e 554.4 ± 15.16g 554.3 ± 40.92f 187.4 ± 1.66a 227.8 ± 7.66b 257.3 ± 11.36c
F3 ND 33.5 ± 1.85a 81.6 ± 0.98b 179.7 ± 16.87c 259.1 ± 2.39d 297.3 ± 1.69e 306.4 ± 16.28f
F4 68.0 ± 19.32d 37.8 ± 0.44a 365.1 ± 17.94f 597.3 ± 48.56g 52.7 ± 5.17c 52.6 ± 8.75b 124.4 ± 8.75e
Ni F1 31.5 ± 1.13d 2.20 ± 0.10a 2.47 ± 0.12b 3.99 ± 0.12c ND ND ND
F2 64.2 ± 3.42g 16.8 ± 0.45f 7.76 ± 0.40e 5.63 ± 0.93d 3.08 ± 0.33c 2.21 ± 0.17a 2.74 ± 0.19b
F3 0.31 ± 0.21a 109.2 ± 3.97e 134.7 ± 2.02f 148.6 ± 12.79g 71.6 ± 1.31b 87.4 ± 0.05c 90.4 ± 3.79d
F4 16.0 ± 1.42a 19.1 ± 0.50d 42.4 ± 0.48f 60.3 ± 2.22g 18.8 ± 0.79c 18.6 ± 1.66b 32.5 ± 1.66e

ND, not detected.

SS, raw sewage sludge; SSBx, biochar derived from sewage sludge pyrolysis at X (°C) temperature, SBBx, biochar derived from co-pyrolysis of the sewage sludge and the
bamboo sawdust at X (°C) temperature.
F1, exchangeable and acid soluble fraction; F2, reducible fraction; F3, oxidizable fraction; F4, residual fraction.
a
Lowercase letters after the mean values show significant differences at the 5% level.

Table 4
Indices for the ecological risk assessment.

Cf Metal contamination Er Potential ecological risk RI Sludge/biochar contamination

Cf 6 1 Clean Er 6 40 Low RI 6 150 Low

1 < Cf 6 3 Low 40 < Er 6 80 Moderate 150 < RI 6 300 Moderate
3 < Cf 6 6 Moderate 80 < Er 6 160 Considerate 300 < RI 6 600 Considerate
6 < Cf 6 9 Considerate 160 < Er 6 320 High RI > 600 High
Cf > 9 High Er > 320 Very high

Cf , contamination factor of the individual heavy metal.

Er , potential ecological risk factor for the individual heavy metal.
RI, sum of the potential ecological risk index ðEr Þ of each heavy metal.

Table 5
Ecological risk assessment of the metals in the sewage sludge, the sludge biochars and the sludge and bamboo biochars.

Metal Tr Cf Er
SS SSB400 SSB500 SSB600 SBB400 SBB500 SBB600 SS SSB400 SSB500 SSB600 SBB400 SBB500 SBB600
Cu 5 88.9 55.1 25.9 11.8 7.78 8.26 3.07 444.5 275.7 129.3 59.2 38.9 41.3 15.3
Zn 1 135.8 58.8 51.8 23.2 11.6 11.0 6.36 135.8 58.8 51.8 23.2 11.6 11.0 6.36
Pb 5 7.57 4.76 3.98 2.28 0.45 0.26 0.16 37.9 23.8 19.9 11.4 2.25 1.28 0.81
Cr 2 4.74 7.54 1.14 0.41 1.70 1.21 0.49 9.49 15.1 2.28 0.81 3.39 2.43 0.97
Mn 1 10.0 18.3 1.95 1.31 12.2 12.0 5.24 10.0 18.3 1.95 1.31 12.2 12.0 5.24
Ni 6 5.98 6.70 3.42 2.62 3.97 4.82 2.87 29.9 33.5 17.1 13.1 19.8 24.1 14.3
RI 667.6 425.3 222.3 109.1 88.2 92.1 43.1

Tr, contamination factor of the individual metal; Cf, toxic response factor of the individual metal; Er, potential ecological risk factor for the individual metal obtained by
multiplying the contamination factor (Tr) by the toxic response factor (Cf); RI, sum of the potential ecological risk indices (Er) of the individual metals. (For interpretation of
the references to colour in this figure legend, the reader is referred to the web version of this article.)
SS, raw sewage sludge; SSBx, biochar derived from sewage sludge pyrolysis at X (°C) temperature; SBBx, biochar derived from co-pyrolysis of the sewage sludge and the
bamboo sawdust at X (°C) temperature.

for land application being more attractive as it is environmentally in the sludge, co-pyrolysis with bamboo sawdust at 600 °C was
friendly (Cao and Pawłowski, 2013; Liu et al., 2008). In the pre- found to be a suitable technique for the safe disposal of the
sent study which was concerned with potentially toxic metals sludge.
 J. Jin et al. / Bioresource Technology 228 (2017) 218–226
4. Conclusions
The present study indicates that pyrolysis is an appealing
scheme for sewage sludge treatment. After pyrolysis most of the
metals (Cu, Zn, Pb, Cr, Mn and Ni) are transformed from easily
available fractions to relatively stable states resulting in a large
decrease in direct toxicity and bioavailability of the residual bio-
char. Addition of bamboo sawdust has a synergetic effect on metal
immobilization in sewage sludge during co-pyrolysis. Further
decline in the toxicity and environmental risk of the metals in
the co-pyrolyzed biochar was achieved and co-pyrolysis at 600 °C
was optimal for the recycling of sewage sludge nutrients.
Acknowledgements
The authors gratefully acknowledge financial support from the
Natural Science Foundation of Zhejiang Province (LQ17B070001),
the Key Scientific and Technological Innovation Team of Zhejiang
Province (2013TD12/12) and the National Natural Science Founda-
tion of China (41201229). J. Zhang is also grateful for financial sup-
port from the Innovative Technology Commission of Hong Kong
(ITS/174/14FX) during his sabbatical leave at The Education
University of Hong Kong.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.biortech.2016.12.
103.
References
Agrafioti, E., Bouras, G., Kalderis, D., Diamadopoulos, E., 2013. Biochar production by
sewage sludge pyrolysis. J. Anal. Appl. Pyrolysis 101, 72–78.
Ahmad, M., Lee, S.S., Dou, X., Mohan, D., Sung, J.-K., Yang, J.E., Ok, Y.S., 2012. Effects
of pyrolysis temperature on soybean stover- and peanut shell-derived biochar
properties and TCE adsorption in water. Bioresour. Technol. 118, 536–544.
Al-Wabel, M.I., Al-Omran, A., El-Naggar, A.H., Nadeem, M., Usman, A.R.A., 2013.
Pyrolysis temperature induced changes in characteristics and chemical
composition of biochar produced from conocarpus wastes. Bioresour. Technol.
131, 374–379.
Cao, Y., Pawłowski, A., 2013. Life cycle assessment of two emerging sewage sludge-
to-energy systems: evaluating energy and greenhouse gas emissions
implications. Bioresour. Technol. 127, 81–91.
Cao, Y., Pawłowski, A., 2012. Sewage sludge-to-energy approaches based on
anaerobic digestion and pyrolysis: brief overview and energy efficiency
assessment. Renewable Sustainable Energy Rev. 16 (3), 1657–1665.
Cha, J.S., Park, S.H., Jung, S.-C., Ryu, C., Jeon, J.-K., Shin, M.-C., Park, Y.-K., 2016.
Production and utilization of biochar: a review. J. Ind. Eng. Chem. 40, 1–15.
Chen, D., Yin, L., Wang, H., He, P., 2014a. Pyrolysis technologies for municipal solid
waste: a review. Waste Manage. 34 (12), 2466–2486.
Chen, F.F., Hu, Y.Y., Dou, X.M., Chen, D.Z., Dai, X.H., 2015. Chemical forms of heavy
metals in pyrolytic char of heavy metal-implanted sewage sludge and their
impacts on leaching behaviors. J. Anal. Appl. Pyrolysis 116, 152–160.
Chen, H., Yan, S.H., Ye, Z.L., Meng, H.J., Zhu, Y.G., 2012. Utilization of urban sewage
sludge: Chinese perspectives. Environ. Sci. Pollut. Res. 19 (5), 1454–1463.
Chen, M., Li, X.-M., Yang, Q., Zeng, G.-M., Zhang, Y., Liao, D.-X., Liu, J.-J., Hu, J.-M.,
Guo, L., 2008. Total concentrations and speciation of heavy metals in municipal
sludge from Changsha, Zhuzhou and Xiangtan in middle-south region of China.
J. Hazard. Mater. 160 (2–3), 324–329.
Chen, T., Zhang, Y., Wang, H., Lu, W., Zhou, Z., Zhang, Y., Ren, L., 2014b. Influence of
pyrolysis temperature on characteristics and heavy metal adsorptive
performance of biochar derived from municipal sewage sludge. Bioresour.
Technol. 164, 47–54.
Cheng, M., Wu, L., Huang, Y., Luo, Y., Christie, P., 2014. Total concentrations of heavy
metals and occurrence of antibiotics in sewage sludges from cities throughout
China. J. Soil Sediment 14 (6), 1123–1135.
Devi, P., Saroha, A.K., 2014. Risk analysis of pyrolyzed biochar made from paper mill
effluent treatment plant sludge for bioavailability and eco-toxicity of heavy
metals. Bioresour. Technol. 162, 308–315.
Fuentes, A., Lloréns, M., Sáez, J., Isabel Aguilar, M., Ortuño, J.F., Meseguer, V.F., 2008.
Comparative study of six different sludges by sequential speciation of heavy
metals. Bioresour. Technol. 99 (3), 517–525.
Fytili, D., Zabaniotou, A., 2008. Utilization of sewage sludge in EU application of old
and new methods—a review. Renewable Sustainable Energy Rev. 12 (1), 116–
140.
225
Hakanson, L., 1980. An ecological risk index for aquatic pollution control: a
sedimentological approach. Water Res. 14 (8), 975–1001.
Havukainen, J., Zhan, M., Dong, J., Liikanen, M., Deviatkin, I., Li, X., Horttanainen, M.,
2017. Environmental impact assessment of municipal solid waste management
incorporating mechanical treatment of waste and incineration in Hangzhou,
China. J. Clean. Prod. 141, 453–461.
Hu, H., Jiang, B., Wu, H., Zhang, J., Chen, X., 2016. Bamboo (Acidosasa edulis) shoot
shell biochar: its potential isolation and mechanism to perrhenate as a chemical
surrogate for pertechnetate. J. Environ. Radioact. 165, 39–46.
Huang, H.-J., Yuan, X.-Z., 2016. The migration and transformation behaviors of
heavy metals during the hydrothermal treatment of sewage sludge. Bioresour.
Technol. 200, 991–998.
Jin, J., Li, Y., Zhang, J., Wu, S., Cao, Y., Liang, P., Zhang, J., Wong, M.H., Wang, M., Shan,
S., Christie, P., 2016. Influence of pyrolysis temperature on properties and
environmental safety of heavy metals in biochars derived from municipal
sewage sludge. J. Hazard. Mater. 320, 417–426.
Kambo, H.S., Dutta, A., 2015. A comparative review of biochar and hydrochar in
terms of production, physico-chemical properties and applications. Renewable
Sustainable Energy Rev. 45, 359–378.
Kirchmann, H., Borjesson, G., Katterer, T., Cohen, Y., 2016. From agricultural use of
sewage sludge to nutrient extraction: a soil science outlook. Ambio.
Li, Y., Meas, A., Shan, S., Yang, R., Gai, X., 2016. Production and optimization of
bamboo hydrochars for adsorption of Congo red and 2-naphthol. Bioresour.
Technol. 207, 379–386.
Liu, H., Jiang, G.M., Zhuang, H.Y., Wang, K.J., 2008. Distribution, utilization
structure and potential of biomass resources in rural China: with special
references of crop residues. Renewable Sustainable Energy Rev. 12 (5), 1402–
1418.
Long, Y.-Y., Hu, L.-F., Fang, C.-R., Wu, Y.-Y., Shen, D.-S., 2009. An evaluation of the
modified BCR sequential extraction procedure to assess the potential mobility
of copper and zinc in MSW. Microchem. J. 91 (1), 1–5.
Lorentzen, E.M., Kingston, H.S., 1996. Comparison of microwave-assisted and
conventional leaching using EPA method 3050B. Anal. Chem. 68 (24), 4316–
4320.
Lu, T., Yuan, H.R., Zhou, S.G., Huang, H.Y., Noriyuki, K., Chen, Y., 2012. On the
pyrolysis of sewage sludge: the influence of pyrolysis temperature on biochar,
liquid and gas fractions. Adv. Mater. Res., 3412–3420 Switzerland. Trans Tech
Publ.
Méndez, A., Terradillos, M., Gascó, G., 2013. Physicochemical and agronomic
properties of biochar from sewage sludge pyrolysed at different temperatures. J.
Anal. Appl. Pyrolysis 102, 124–130.
Mininni, G., Blanch, A.R., Lucena, F., Berselli, S., 2015. EU policy on sewage sludge
utilization and perspectives on new approaches of sludge management.
Environ. Sci. Pollut. Res. 22 (10), 7361–7374.
Rafiq, M.K., Bachmann, R.T., Rafiq, M.T., Shang, Z., Joseph, S., Long, R., 2016. Influence
of pyrolysis temperature on physico-chemical properties of corn stover (Zea
mays L.) biochar and feasibility for carbon capture and energy balance. PLoS One
11 (6), e0156894.
Rauret, G., Lopez-Sanchez, J.F., Sahuquillo, A., Rubio, R., Davidson, C., Ure, A.,
Quevauviller, P., 1999. Improvement of the BCR three step sequential extraction
procedure prior to the certification of new sediment and soil reference
materials. J. Environ. Monit. 1 (1), 57–61.
Shao, J., Yuan, X., Leng, L., Huang, H., Jiang, L., Wang, H., Chen, X., Zeng, G., 2015. The
comparison of the migration and transformation behavior of heavy metals
during pyrolysis and liquefaction of municipal sewage sludge, paper mill
sludge, and slaughterhouse sludge. Bioresour. Technol. 198, 16–22.
Shi, W., Liu, C., Shu, Y., Feng, C., Lei, Z., Zhang, Z., 2013. Synergistic effect of rice husk
addition on hydrothermal treatment of sewage sludge: fate and environmental
risk of heavy metals. Bioresour. Technol. 149, 496–502.
Singh, B.P., Cowie, A.L., Smernik, R.J., 2012. Biochar carbon stability in a clayey soil
as a function of feedstock and pyrolysis temperature. Environ. Sci. Technol. 46
(21), 11770–11778.
Sungur, A., Soylak, M., Ozcan, H., 2014. Investigation of heavy metal mobility and
availability by the BCR sequential extraction procedure: relationship between
soil properties and heavy metals availability. Chem. Speciation Bioavailability
26 (4), 219–230.
Uchimiya, M., Wartelle, L.H., Klasson, K.T., Fortier, C.A., Lima, I.M., 2011. Influence of
pyrolysis temperature on biochar property and function as a heavy metal
sorbent in soil. J. Agric. Food Chem. 59 (6), 2501–2510.
Ure, A.M., Quevauviller, P., Muntau, H., Griepink, B., 1993. Speciation of heavy
metals in soils and sediments. An account of the improvement and
harmonization of extraction techniques undertaken under the auspices of the
BCR of the commission of the European communities. Int. J. Environ. Anal.
Chem. 51 (1–4), 135–151.
Weng, H., Fu, F., Liu, Z., Zhang, J., Ji, Z., Ma, X., 2010. Mechanisms of heavy metal
stabilization during sludge drying. Acta Sci. Circum. 30 (7), 1401–1409.
Wiedner, K., Naisse, C., Rumpel, C., Pozzi, A., Wieczorek, P., Glaser, B., 2013.
Chemical modification of biomass residues during hydrothermal
carbonization–What makes the difference, temperature or feedstock? Org.
Geochem. 54, 91–100.
Xiao, X., Chen, Z., Chen, B., 2016. H/C atomic ratio as a smart linkage between
pyrolytic temperatures, aromatic clusters and sorption properties of biochars
derived from diverse precursory materials. Sci. Rep. 6, 22644.
Xu, T., Lou, L., Luo, L., Cao, R., Duan, D., Chen, Y., 2012. Effect of bamboo biochar on
pentachlorophenol leachability and bioavailability in agricultural soil. Sci. Total
Environ. 414, 727–731.
226 J. Jin et al. / Bioresource Technology 228 (2017) 218–226

Yuan, H., Lu, T., Huang, H., Zhao, D., Kobayashi, N., Chen, Y., 2015. Influence of
pyrolysis temperature on physical and chemical properties of biochar made
from sewage sludge. J. Anal. Appl. Pyrolysis 112, 284–289.
Yuan, J.-H., Xu, R.-K., Zhang, H., 2011. The forms of alkalis in the biochar produced
from crop residues at different temperatures. Bioresour. Technol. 102 (3), 3488–
3497.
Zhang, B., Xiong, S., Xiao, B., Yu, D., Jia, X., 2011. Mechanism of wet sewage sludge
pyrolysis in a tubular furnace. Int. J. Hydrogen Energy 36 (1), 355–363.
Zhang, J.-H., Lin, Q.-M., Zhao, X.-R., 2014. The hydrochar characters of municipal
sewage sludge under different hydrothermal temperatures and durations. J.
Integr. Agric. 13 (3), 471–482.
Zhang, J., Cornelia, M.-N., Wang, M., Cao, Z., Luo, X., Wong, M., Chen, W., 2013.
Change of PAHs with evolution of paddy soils from prehistoric to present over
the last six millennia in the Yangtze River Delta region, China. Sci. Total Environ.
449, 328–335.