G Model

NBT 911 No. of Pages 15

New Biotechnology xxx (2016) xxx–xxx

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Biosorption of lead ions from aqueous effluents by rapeseed biomass

Irina Morosanu, Carmen Teodosiu*, Carmen Paduraru, Dumitrita Ibanescu, Lavinia Tofan
Department of Environmental Engineering and Management, Faculty of Chemical Engineering and Environmental Protection, “Gheorghe Asachi” Technical University of Iasi, 73 Prof.
Dr. D. Mangeron Street, 700050, Iasi, Romania

A R T I C L E I N F O A B S T R A C T

Article history:
Received 27 February 2016 Lead, as well as other heavy metals, is regarded as priority pollutant due to its non-biodegradability,
Received in revised form 26 July 2016 toxicity and persistence in the environment. In this study, rapeseed biomass was used in the
Accepted 23 August 2016
biosorption of Pb(II) ions in batch and dynamic conditions, as well as with tests for industrial
Available online xxx
wastewater. The influence of initial concentration (5–250 mg/L), pH and contact time (0.5–6 h) was
investigated. The kinetic data modeling resulted in good correlations with the pseudo-second order
Keywords:
and intraparticle diffusion models. The maximum sorption capacities of Pb(II) were 18.35, 21.29 and
Biosorption
22.7 mg/L at 4, 20 and
Lead
Rapeseed
50 C, respectively. Thermodynamic parameters indicated the spontaneity and endothermic nature
Batch conditions of lead biosorption on rapeseed biomass. The biosorption mechanism involves both physical and
Fixed-bed column chemical interactions. The breakthrough curves at 50 and 100 mg/L were determined and
Wastewater evaluated under dynamic conditions. The breakthrough time lowered with increasing the influent
Pb(II) concentration. The experimental data obtained from fixed-bed column tests were well
fitted by Thomas and Yoon-Nelson models. The calculated sorption capacities were in good
agreement with the uptake capacity of Langmuir model. The applicability of rapeseed to be used as a
sorbent for Pb(II) ions from real wastewater was tested, and Pb(II) removal efficiency of 94.47% was
obtained.
ã 2016 Elsevier B.V. All rights reserved.

1. Introduction
http://dx.doi.org/10.1016/j.nbt.2016.08.0 02
Human activities, through industrial and agricultural 1871-6784/ã 2016 Elsevier B.V. All rights reserved.

processes, causes surface water quality degradation, leading to

problems related to supply of drinking water or recycling of
wastewater. Among the multitude of pollutants found in
wastewater dis- charges, heavy metals generate serious
environmental and health concerns. These compounds are
known for their ability to migrate between environmental
compartments (e.g. from sediments into water) and to
accumulate in living organisms [1,2]. Heavy metals present toxic
and non-biodegradable features, which is why once they reach
the aquatic environment, they produce impacts on the aquatic
biota, as well as to the crops near the water body, and then arrive
in the human body in a more concentrated form than that of the
lower food chain segments.
From the heavy metals category, lead has raised multiple
concerns due to its frequent occurrence in wastewaters and its
significant impacts on human health. Lead is present in effluents
coming from smelters and refineries, battery manufacturing,
steel industry, printing, glass manufacturing [3,4]. In humans,
lead poisoning readily affects young children,
causing

* Corresponding author.
E-mail address: cteo@ch.tuiasi.ro (C. Teodosiu).

Please cite this article in press as: I. Morosanu, et al., Biosorption of lead ions from aqueous effluents by rapeseed biomass, New Biotechnol.
(2016), http://dx.doi.org/10.1016/j.nbt.2016.08.002
G Model
NBT 911 No. of Pages 15

neurodevelopmental problems even at low concentrations. Pb

(II) ions present high affinity for thio ( SH), oxo (¼O) and
phosphate (PO43 ) groups that are found in some enzymes, and
also ligands and biomolecules from the human organism and
affect the membrane permeability of organs and haemoglobin
synthesis [5]. Lead bioaccumulates in bones (half-time over 20
years), and affects the nervous and reproductive systems, red
blood cells and kidney, and due to its enzyme inhibitor
effects, is a probable carcinogenic [3,6]. Lead is listed as a
priority pollutant by the US Environmental Protection Agency
[7]. In drinking water, World Health Organization has set up as
maximum allowable concentra- tion for Pb(II) the limit value of
0.01 mg/L. In another classification [8], Pb is a metal of high
priority for both removal and recovery from water and
wastewater before discharge into the environment.
A number of processes are applied to minimize lead concen-
tration in wastewater and they involve chemical precipitation,
reduction, electrochemical methods, ion exchange, adsorption,
flotation [9–13]. These methods have several disadvantages that
influence their applicability, including significant capital and
operational costs, addition of chemical reagents and generation of
hazardous wastes, energy demand, low efficiency for diluted
wastewaters [14–16]. In this context, biosorption, a subcategory
of adsorption, has gain interest in recent years due to its
efficiency in

Please cite this article in press as: I. Morosanu, et al., Biosorption of lead ions from aqueous effluents by rapeseed biomass, New Biotechnol.
(2016), http://dx.doi.org/10.1016/j.nbt.2016.08.0 02
2 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx
mitigating heavy metals pollution of aqueous effluents, in
particularly of low concentration [13].
Biosorption is based on the potential of any biological material
(i.e. biomolecules or different biomass) to sequester metals and
other pollutants from aqueous solutions in a metabolically-free
manner [17]. In this way, biosorption is regarded as a passive
process based on the affinity between the sorbate and the
biomass, as opposed to bioaccumulation, which involves an active
metabolic process [18]. The main advantages and
disadvantages of bio- sorption are illustrated in Fig. 1 [8,19].
A wide variety of biological materials have been explored for
heavy metal removal. Such biosorbents include low-cost,
available and renewable materials, like: macroalgae, agricultural
residues, industrial waste, animal materials, raw plants, sludge
etc. [9,19–
22]. Among the agricultural and forestry originating sorbents,
Phytolacca americana biomass [23], olive tree pruning [24], Marula
seed husk [16], cedar leaf [25], maize stover [26], peanut shells
[27], cork waste [28] have been used in recent years for treating
lead-containing wastewaters. Rapeseed is a member of the family
Brassicaceae and has become a major crop harvested mainly for
its animal feed and oil production potential. The major producers
are European Union (20 Mt/yr), Canada (15 Mt/yr) and
China (12 Mt/yr) [29]. In Romania, the total production of
rapeseed has increased threefold between 2007 and 2014 [30]. To
obtain one tone of biodiesel, 3.3 tons of rapeseed are
needed, whereas approximately 2.1 tons is rapeseed meal [31].
Such high quantity of by-products and wastes needs to be handled
in an environmentally safe way. An interesting alternative is its
utilization as a low-cost biosorbent of pollutants from aqueous
solutions [22,32–36]. Rapeseed is rich in specific
macromolecules such as fatty acids and proteins [34], but also
has lignin, cellulose and hemicellulose as major constituents.
Such components offer a large variety and abundance of
functional groups that can act as active sites on the surface of
the biomaterial.
Over the years, biosorption experiments were carried out
intensively in batch mode of operation [25–28,37]. Several papers
reported lead biosorption by agricultural or vegetable biomass in
dynamic conditions [24,38,39]. The use of a column in continuous
operation is more practical at industrial scale, because of its
simplicity and lower costs, while it can be more easily scaled-up
from laboratory to the pilot and industrial scale [40].
The main objective of this study is to evaluate the potential of
rapeseed biomass to remove lead ions from synthetic aqueous
solution both in batch as well as continuous systems. The surface
of the sorbent was studied by infrared (IR) spectroscopy and
high resolution microscopy. The influence of initial
concentration and contact time, related isotherm and kinetic
models, and thermody- namic parameters were investigated in
batch mode for a better understanding of the biosorption
process. Column studies were done at different initial metal
concentrations and several models were applied to analyse the
breakthrough curves. In addition, the applicability of the
biosorbent to remove Pb(II) ions from more complex matrices in
a fixed bed column was verified by using a real industrial
wastewater. To our best knowledge, this type of experiments
used to test the biosorption affinity of rapeseed biomass have
not been reported so far.
2. Materials and methods
2.1. Biosorbent preparation and characterization
Rapeseed (RS) originating from agricultural units around Iasi
(Romania) was used in the present investigation. The biological
material was prepared according to [36]. In short, the rapeseed
was washed several times with Grade I water (Adrona Crystal E),
dried at 40 C for 24 h and crushed to obtain particle sizes
between 0.1 and 0.2 mm.
Attenuated total reflection Fourier transform infrared
(ATR-FTIR) spectroscopy (Platinum ATR ALPHA Bruker, Germany)
was used to determine the major functional groups on the
surface of sorbent. Spectra before and after biosorption were
recorded with a resolution of 2 cm 1 in the range 400–4000 cm 1,
with 128 acquisition scans.
The surface morphological features of loaded and unloaded
rapeseed biomass were analysed using Scanning Electron
Fig. 1. Advantages and disadvantages of biosorption.
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx 3

Microscopy coupled with Energy Dispersive X-ray Spectroscopy
(SEM/EDX). The images were executed using FEI Nova NanoSEM
230, operating at an accelerating voltage of 3 kV.
2.2. Reagents
All chemicals used were analytical grade. Stock solution of 1 g/L
Pb(II) was prepared from Pb(NO3)2 dissolution in deionized water
(Adrona Crystal E, Grade I). The working solutions were obtained
by diluting the stock solution in deionized water.
2.3. Batch sorption experiments
Biosorption experiments in the batch mode of operation were
performed by using 0.5 g of rapeseed and 50 mL of Pb(II) test
solutions, under intermittent agitation and at 20 C, unless
otherwise mentioned. The influence of initial pH of the solution
was studied in the range 2–6 ( 0.1), at 20 C and a contact time
of
24 h. The initial pH was adjusted with 0.1 M HNO3, except of the
pH value around 5. The pH was not controlled during the
experiments. The initial and final pH of the solutions was
measured with Consort C863 multi parameter analyzer. The
effect of initial sorbate concentration was done by varying the
Pb(II) initial concentrations from 5 to 125 mg/L, at a contact time
of 24 h. In all cases, the initial pH of the Pb(II) solution was
around 5.2 (unmodified pH of the solution) and no further
adjustments were made during the tests. Kinetics measurements
were done at two initial concentrations
(50 and 100 mg/L) and aliquots were taken at different time
intervals (0.5–6 h) to determine Pb(II) concentration. The initial pH
of the solution was approximately 5.2. The effect of the
temperature was studied at three different temperatures (4, 20
and 50 C) by modifying the initial Pb(II) concentration for the test
solutions between 5 and 125 mg/L, at pH around 5.2 and a
contact time of 3 h. The biosorption isotherms were obtained
from these data.
The metal solution was separated from the sorbent by
centrifugation (Hettich Universal 320) at 4000 rpm for 15 min.
All tests were realised in duplicate and the average values were
reported. The equilibrium concentrations (Ce) were determined by
4(2-pyridylazo)-resorcinol at l = 530 nm, using Jasco V-530 UV–
Vis spectrophotometer. The amount of metal ion retained at
equilibrium (qe) and the Pb(II) removal efficiency (R) were
calculated with the following equations:
C 0 Ce
qe ðmg=gÞ ¼ V ð1Þ
G
C0
C
Rð%Þ ¼ e 100
C0
where C0 is the initial Pb(II) concentration (mg/L), G is the weight
of
rapeseed (g) and V is the volume of solution (mL).
2.4. Kinetic models
Kinetics investigation provides information on the rapidity of
the biosorption. In this study, pseudo-first-order, pseudo-second-
order and intraparticle diffusion kinetic models in linearized form
have been used to determine the rate-controlling steps in Pb(II)
biosorption on rapeseed (Table 1).
2.5. Equilibrium isotherm models
Two empirical isotherm models, i.e. Langmuir and Freundlich,
were used to analyse the equilibrium data obtained from the
study. The Langmuir isotherm describes a homogenous
monolayer adsorption, where all the active sites (identical and
in a fixed number) have an equal affinity for the sorbate, with no
interaction between the sorbate molecules in the plane of the
surface [42]. The Freundlich model was developed for adsorption
at lower concen- trations on heterogeneous surfaces and
assumes the adsorbed molecules interact with their adjacent
neighbours [43]. The model equation states that the adsorption
energy is reduced exponen- tially with the decreasing in the
number of active sites of an adsorbent [44]. Linear Langmuir
and Freundlich isotherm equa- tions are presented in Table 2.
A dimensionless coefficient, usually named as separation factor
or equilibrium parameter (RL), can be derived based on the
Langmuir constant [44] and can be determined with Eq. (3):
1
RL ¼ ð3Þ
1 þ K L C0
2.6. Thermodynamic parameters
The thermodynamic parameters determination is in close
correlation with the effect of temperature on biosorption and the
Langmuir constant. In order to assess the thermodynamic nature of
the process and its feasibility, the changes in enthalpy (DH),
entropy (DS) and Gibbs free energy (DG) were calculated
according to Eqs. (4)–(6) [34,46]:
DG ¼ RT lnð55:5K L Þ ð4Þ
lnK L ¼
DH þ Y ð5Þ
RT
DS ¼ DH D
G
ð6Þ
T
ð2Þ where R is the gas constant (8.31 J/mol K), T is the temperature (K),
KL(L/mol) is the Langmuir equilibrium constant, 55.5 (mol/L) is the
solvent (water) concentration and Y is a constant. Zhou and Zhou
[47] proposed Eq. (3) to calculate DG for sorption systems

Table 1
Kinetic models used for Pb(II) biosorption on RS.

Kinetic model Linear equation Parameters Plot

representation

Pseudo-first Kid
logðqe qt Þ¼ logðqe Þ k1
t qe (mg/g) and qt (mg/g) are the adsorption capacity at equilibrium and time t (min), respectively, k1
order [14] 2:30
(1/ 3
min) and k2 (g/mg min) are the pseudo-first- and pseudo-second-order rate constants, respectively,
 log(qe-qt) vs t
Pseudo-second t 1 t (mg/g min
0.5
) is the intraparticle diffusion rate constant. t/qt vs t
þ
¼ e
order [16] qt k2 q2 qe

Intraparticle qt ¼ K id t 0:5 qt vs t0.5

diffusion [41]
4 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

Table 2
Isotherm models used for Pb(II) biosorption on RS.

Isotherm Linear equation Parameters Plot

model representation

Langmuir C C 1 qe – sorption capacity at equilibrium (mg/g), qm – maximum sorption capacity (mg/g), Ce (mg/L)– Ce/qe vs Ce
e e equilibrium
¼ þ
[42] qe qm K L qm
concentration, KL – Langmuir constant (L/mg), KF and n are the Freundlich constants
n
Freundlich log qe ¼ log K F þ 1log C e log qe vs logCe
[45]

Table 3
Dynamic characterization models used for Pb(II) biosorption on RS-packed column.

Model Linear equation Parameters Plot

representation

Thomas K q 0ð K T C 0ð C0 is the initial metal ion concentration (mg/L), Ct is the equilibrium concentration (mg/L) at time t (min), ln(C0/ Ct 1) vs
TÞ mT TÞ KT
C0
ln 1 ¼ V
[50]
Ct F F is the Thomas constant (L/min/mg), F is the volumetric flow rate (L/min), q0(T) is the maximum column V
Yoon- capacity (mg/g) determined by the Thomas model, m is the mass of sorbent (g) and V is the volume (L), kYN ln(Ct/ C0-Ct) vs t
ln Ct
C0 Ct
¼ kYN t t kYN is
Nelson
the Yoon-Nelson constant (1/min), t is the time required for 50% adsorbate breakthrough.
[51]

considering an exchange mechanism. The plot of lnKL against 1/T lead/rapeseed system investigated. The Thomas and Yoon-Nelson
gives the enthalpy change value. models are presented in the linearized form as depicted in Table
3.
2.7. Fixed-bed column experiments The uptake capacity, q0(YN), can be calculated with Eq. (8) [49]:
C0 Q t
Fixed-bed column experiments were realised in order to assess q 0ðYNÞ ¼ ð 8Þ
the capacity of lead removal of rapeseed in dynamic conditions. 1000w
The experimental set-up included a down flow glass column of where C0 is the inlet metal ion concentration (mg/L), Q is the flow
1.5 cm inner diameter and 15 cm in length. A 0.7 g of rapeseed rate (mL/min) and w is the weight of sorbent (g).
was mixed with a commercially available resin (Purolite
MN200) in a ratio 1:2 to avoid column clogging. To ensure that 2.10. Experiments with industrial wastewater
no adsorption phenomena occurs on the used polymer, tests with
Pb(II) solutions (50 and 100 mg/L) were done. There was no Industrial wastewaters contain a large variety of organic and
significant change in lead concentration after the experiments. inorganic contaminants, constituting a complex matrix of inter-
Therefore, the men- tioned resin can be considered an inert acting species. In order to observe the behaviour of RS biosorbent
material for the studied process. The bed height of the mixture in the retention of Pb(II) from such a matrix, while other
rapeseed/resin achieved was 6 cm. A layer of wadding glass was compounds may interfere and/or compete for the sorption sites,
fitted at the bottom of the column to support the sorbent during a column experiment using real wastewater spiked with Pb(II)
studies. The influent feed flow was established at 2.5 mL/min. was performed. The wastewater sample was obtained from a
The initial Pb(II) concen- trations in test solutions were 50 factory located near Iasi, Romania. A volume of 200 mL of
and 100 mg/L. The working temperature was 20 C. The initial industrial effluent was treated through the column at a bed
pH of the solution was around height of 6 cm and a flow rate of 2.5 mL/min. The physico-
5.2 and it wasn’t controlled during the experiment. Effluent chemical characteristics of the wastewater used in the
samples were collected at the bottom of the column at certain experiment were analysed before and after the column by
time intervals and analysed for Pb(II) ions content. standard methods and the concentration of lead ions was
determined by spectroscopy, as previously mentioned. The initial
2.8. Breakthrough curve parameters wastewater characteristics are presented in Table 4.

The breakthrough curve is plotted as the effluent

concentration at a certain time (Ct) against effluent volume.
The sorption capacity, qdyn (mg/g), in fixed-bed studies can be
determined by Eq. (7) [48]:
VtZ
C0 Ct
qdyn ¼ 1 dV ð7Þ
m C0
0
Table 4
where m is the bed mass (g), C0 is the initial influent In order to process the breakthrough data, two widely used
concentration (mg/L), Ct is the effluent concentration at any time t models have been used and evaluated for their applicability to the
(mg/L), V is the volume (L).

2.9. Theoretical models

Water characteristics before biosorption.

Quality indicator (units) Raw wastewater

pH 7.78
TSS (mg/L) 69
COD (mg/L) 515.65
2+
Pb (mg/L) 4.88
Cl (mg/L) 150
Total hardness ( G) 12.4
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx 5

Fig. 2. Influence of initial pH and pH changes during Pb(II) biosorption on RS (C0 = 50 mg/L, biosorbent dose = 10 g/L, pH = 5.2, T = 20 C, t = 24 h).

3. Results and discussions biosorption has increased over the pHPZC. The deprotonation of
biosorbent’s surface determines higher removal efficiencies. Other
3.1. Batch sorption experiments authors have noticed a similar trend in the variation of pHf when
studying removal of Cu(II) and Ni(II) on grape stalks [54] or Cd(II)
3.1.1. Effect of solution pH biosorption on chemically modified maize straw [55].
Functionalization of biosorbent surface and metal speciation At the natural pH of the Pb(II) solution (around 5.2),
are influenced by the pH of the solution. At pH under 6, lead can biosorption by electrostatic forces and ion exchange
be found predominantly in its divalent cationic form (Pb2+). At mechanism could be responsible for the large quantity of metal
more basic pH, hydrolyzed species of lead are starting to be ions removed from aqueous phase. Hence, the pH of the
formed, such Pb(II) solutions in the
+
as Pb(OH) , Pb(OH)2 and Pb(OH)3 [52,53]. Accordingly, to avoid following sorption experiments will not be adjusted. By working at
the sorption of other species of lead and Pb(OH)2 precipitation, pH (pHf) was measured. As shown in Fig. 2 for pHi 4, the pH after
the effect of solution acidity on lead biosorption on RS was
studied for initial pH (pHi) values between 2 and 6. In Fig. 2, the
variation of Pb (II) removal efficiency and final solution pH with
initial acidity of medium is illustrated. The initial pH profile
shows an increase in the removal efficiency of Pb(II) ions from
46.25% at initial pH 2 to a maximum of 94.04% at initial pH
around 5. At initial pH of 6, the removal efficiency is still high
(91.13%). In very acidic conditions, a competing effect for the
sorption sites between the protons and Pb2+ ions existing in
solution can cause lower removal rates [26,52]. As the pH
+
increases, the repulsive forces between the H and metal ions
decrease and the access to the sorption sites is easier.
Another explanation regarding the removal efficiency (R%)-pHi
profile is linked to the pH at zero point of charge (pHPZC) of the
solid. Paduraru et al. [36] have determined the pHPZC of rapeseed
biomass to be 5. Therefore, the surface of the biosorbent will be
positively charged at pH < 5. Consequently, the metal ions
+
from solution could replace the H of the active centers of the
sorbent. This could be the reason for the small change in the
final solution pH (from 2.1 to 2.78). In contrast, at higher values
of pH, the sorption sites having negative charge will
predominate. In this case, Pb2+ ions will be electrostatically
attracted to the solid surface.
In order to investigate the mechanism of biosorption, the final
the natural pH of the solution, addition of foreign ions in the
system is avoided, while reducing the costs for pH adjustments
before and after the biosorption.

3.1.2. Effect of initial concentration

In order to see the correlation between the initial amount of
metal ions in aqueous phase and the metal-binding capacity of
the rapeseed biomass, the initial concentration of lead was
varied between 5 and 250 mg/L. As shown in Fig. 3, the lead
uptake of rapeseed is dependent on the initial
concentration and is increasing with the increase of metal
ions availability in test solutions. The observed results may be
explained by the enhancement in the motivating gradient force
dependent on the initial metal concentration. In a specific
amount of sorbent, an increase of the quantity of metal ions
entails a greater driving force to transport the ions from the
aqueous phase to the surface of the sorbent, and therefore the
possibility of interaction between the metal ions and the active
binding sites increases [15,36,56].

3.1.3. Effect of contact time

The results obtained from the influence of the contact time on
the biosorption of Pb(II) solutions of 50 and 100 mg/L concentra-
tion at 20 C and natural solution pH are depicted in Fig. 4. In the
first 60 min, an abrupt increase in the retained amount of lead
ions can be observed. This may be explained by the large
availability of the active sites that can be easily accessed. As they
are occupied by
6 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

Fig. 3. Influence of initial Pb(II) concentration on the biosorption on rapeseed (biosorbent dose = 10 g/L, pH = 5.2, T = 20 C, t = 24 h).

the metallic ions, the rapeseed surface becomes saturated and a Fig. 4. Effect of contact time for the biosorption of lead(II) onto RS biomass
(biosorbent dose = 10 g/L, pH = 5.2, T = 20
competition for the remaining sites will take place by the C).
remaining metal ions in the aqueous phase [16,39,57]. At this
point, a diffusion barrier occurs as the lead ions are migrating to
the active sites found in the inner pores. At the same time, the
gradient concentration of lead ions decreases. Therefore, the
process rate decreases until equilibrium is reached. This can be
recognized in Fig. 4 by the slower increase in the sorption
capacity until a plateau was reached and the sorption capacity
was cvasi- constant. According to these results, a time of 3 h was
considered to be sufficient for ensuring the liquid-solid
equilibrium.

3.1.4. Effect of temperature

Temperature is an important parameter that influences the
biosorption process. The effect of temperature on lead uptake by
rapeseed was investigated and this dependence is described by
Fig. 5. The obtained isotherms of “L”-type (concave curve) indicate
a progressive saturation of the biomass, as the ratio between the
Pb (II) ions in solution and adsorbed decreases as the initial
concentration increases [58]. Comparing the three isotherms, it
can easily be observed that the amount of metal ions adsorbed
per unit of sorbent mass increases with rise of temperature,
indicating the endothermic nature of the process, this feature
being typical for a chemical reaction. A reason may be that a
higher temperature could strengthen the bonds between the Pb(II)
ions and active sites of the biomass and between adjacent
sorbate species of the adsorbed phase [59]. Another
explanation may be the fact that a
higher temperature induces more mobility in the particles and
reduces liquid viscosity and that the affinity of sorbate on the solid
is higher at high temperatures [60,61].

3.1.5. Biosorption isotherms

An adsorption isotherm describes the dependence between the
metal ions adsorbed and those in aqueous phase in conditions of
equilibrium and constant temperature. The adsorption isotherms
is very important for the design of a sorption system, as these
graphic representations provide information about the sorption
capacity [27]. The experimental data was evaluated by the
Langmuir and Freundlich isotherm models and the biosorption
equilibrium at different temperatures is well described by these
models, as illustrated in Fig. 6. The Langmuir constants, KL and qe,
were calculated from the slope and intercept of the linear plot
Ce/qe against Ce (Fig. 6a). Fig. 6b presents the plot log qe versus
log Ce from which the Freundlich parameters, KF and n, were
determined from the slope and intercept of the line. The models’
parameters and the correlation coefficients are presented in Table
5.
In the case of Langmuir isotherm model, very good correlation
with the sorption data was observed based on coefficients
2
R > 0.99. The maximum biosorption capacities by monolayer
adsorption hypothesis are 18.35, 21.29 and 22.7 mg/g at 4, 20 and
50 C, respectively (Table 5).
The separation factor RL was calculated for the three isotherms
and all the values were obtained between 0.01 and 0.43, indicating
a favourable biosorption of Pb(II) onto rapeseed. The maximum
capacity of Pb(II) retention obtained on rapeseed biomass is
comparable with other lignocellulosic biomaterials used for
removal of lead from aqueous solutions (Table 6). The ability of
rapeseed to remove lead ions from aqueous solutions is compara-
ble with Marula seed husk [16], maize stover [26], olive tree
pruning waste [62], cashew nut shell [63] and porous lignin-
based sphere [39]. This proves the feasibility of agricultural
wastes and vegetable biomass for decontamination of wastewater
containing lead ions.

3.1.6. Biosorption kinetics

The rate at which a sorption process takes place is of practical
importance being helpful also for the process design. It is well
known that there are several rate-controlling steps in the sorption
process, including transport of the sorbate in the bulk solution
to the sorbent surface, diffusion through the boundary layer
surrounding the sorbent particles, transport from surface to the
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx
Fig. 5. Influence of temperature on Pb(II) removal on rapeseed sorbent (biosorbent dose = 10 g/L, pH = 5.2, t = 3 h).
interior active sites, and sorption via physical interactions or
chemical bonding [65–67].
In order to investigate the mechanism and rate-controlling
steps of the lead biosorption on rapeseed, the kinetic data was
modeled by using the pseudo-first-order, pseudo-second-order
and intraparticle models. The value of the sorption capacity at
equilibrium and the rate constant can be determined from the
slope and intercept of the linear plots corresponding to the
pseudo-first and pseudo-second order kinetic models, which are
presented in Fig. 7(a and b). Table 7 shows the kinetic
parameters obtained from the analysis of experimental data. The
information deducted from applying the mentioned kinetic
models indicates that biosorption of Pb(II) on rapeseed
corresponds better to the pseudo-second-order kinetic model. In
many cases, it was reported that the Lagergren pseudo-first order
equation is not suitable for the whole range of the considered
contact times for biosorbents [68]. According to the plot in Fig.
7a, the model describes well the
Fig. 6. Biosorption isotherm models of Pb(II)-rapeseed system: a. Langmuir
model, b. Freundlich model.
7
data corresponding to the first 60 min, when rapid sorption
occurs, whereas afterwards it deviates, resulting in lower R2
coefficients.
Conversely, the pseudo-second order kinetic model plots
shown in Fig. 7b were found to fit the experimental data for the
entire study period. Consequently, higher correlation factors
2
(R > 0.99) were obtained and the predicted equilibrium sorption
capacity was closer to the experimental uptake, as can be seen
from Table 7. According to the pseudo-second-order kinetic
model, the biosorption of lead ions onto RS is based on chemical
reaction, involving sharing or exchange of electrons between
sorbent and sorbate [36,56,60]. Literature review reveals the same
kinetic trend for lead biosorption on Marula seed husk [16],
Cyclosorus interruptus [21], lentil husk [45], rice husk [59] and
peanut shells [27]. Furthermore, the rate of biosorption depends
on the initial concentration (Table 7).
In order to observe the influence of the diffusion mechanism
on the rate of the sorption process, the intraparticle model was
0.5
tested. The linear plots of qt versus t for the two
concentrations considered are presented in Fig. 7c. If the plot is a
line that passes through the origin, then the intraparticle
diffusion is the sole rate- controlling step. It can be easily
observed that in both cases the result is not a straight line and
that it also doesn’t pass through the origin. This indicates that
other mechanisms besides diffusion from the solid-liquid
interface are occurring. In this study, the plots are presented as
curves with three linear portions. They corre- spond to the
stages of metal sorption by sorbents. The first portion, with a
higher slope, depicts the rapid uptake of lead ions on the
exterior surface of rapeseed biomass (diffusion from bulk
solution). Then follows the gradual sorption stage, in which the
metal ions enter the biosorbent pores. As the pores become
crowded with sorbate, the diffusion rate decreases and is the rate-
controlling step. This could be attributed to diffusion into the
mesopores. In the final region (region III), the intraparticle
diffusion into micropores slows down considerable, while the
equilibrium between the metal ions in the solution and on the
sorbent surface is being reached. Table 8 presents the diffusion
rates for each stage. The correlation coefficients R2 were between
0.93 and 1. The low values of Kid,III implied that the intraparticle
diffusion into micropores was the rate-limiting step in the
biosorption process. Other authors have reported similar multi-
linearity of intraparticle diffusion plot regarding biosorption of
lead onto mansonia wood sawdust [66], Phytolacca americana L.
biomass [23] and activated carbon derived from Mangostana
Garcinia shell [69] removal of Cu(II), Co(II) and Fe(III) by rice husk,
palm leaf and water hyacinth [41] and of Cu(II) by Tamarindus
indica seed powder [60].
8 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

Table 5
bands of the native RS and Pb-loaded RS with the respective
Quantitative description of Pb(II)-rapeseed biomass system on the basis of
Langmuir and Freundlich isotherm models. assignments are indicated in Table 10. By comparing the two
spectra from Fig. 8, one can observe distinctive changes on the
Model Langmuir Freundlich
biosorbent surface, as result of sorption process on the RS. The
1
Parameters qe (mg/g) K L(L/mg) R2 KF n R2 broad peak at 3292 cm corresponding to the deformation of
Temperature 4 C 18.35 1.70 0.81 0.958
O H and N H groups present in alcohols, phenols, primary and
0.266 0.997
20 C 21.29 0.400 0.997 3.02 0.94 0.989 secondary amides has sharply decreased and slightly shifted to
1
50 C 22.70 0.508 0.991 4.92 1.09 0.985 3274 cm . A similar trend may be observed for the next pair
of
1 1
high
2848 intensity
cm ) thatpeakscan be(from 2923 and
attributed to CH2854 cm vibration
2 group to 2917of and
the
3.1.7. Biosorption thermodynamics
lipid moiety of rapeseed [18]. Several overlapping bands
The results of the thermodynamic parameters calculation are 1
appearing at 1710 and 1651 cm indicate that carbonyl moiety
reported in Table 9. The negative values for the Gibbs free energy
of aldehydes, ketones, carboxylic acids, esters or amides have
change show the spontaneity of lead biosorption. It can be
disappeared or shifted to lower wavenumbers. A reduction of
observed that DG values decrease with increasing temperature,
peak also occurred at
affirming once again the favourability of the process at higher 1535 cm 1, which marks the presence of proteins. The peak at
temperatures. Literature reports that values of the free energy 1
1241 cm , related to P- and S-containing compounds, has
change in the range 20 to 0 kJ/mol are typical for physical 1 1
shifted to 1174 cm . The region 1200–1000 cm is
adsorption and for chemical sorption are between 80 and
believed to be characteristic of C O stretching [25]. A high
400 kJ/mol [70,71]. As it may be observed in Table 9, the values
intensity peak at
obtained in this study are between the two intervals mentioned. 1
1037 cm characteristic to C O C stretching of
It may be concluded that retention of Pb(II) ions by RS is rather polysaccharides
a combination of physical and chemical sorption processes
or C O P stretching of phosphodiesters is reduced and shifted to
rather than a pure physical or chemical sorption process.
a lower band. The infrared spectrum of lead loaded rapeseed
The enthalpy change value DH was estimated from the slope 1
shows the appearance of two peaks at 1090 and 960 cm ,
of
respectively, that in the native RS might be hidden by the more
the line obtained from the plot lnKL versus 1/T (figure not shown).
intense ether features. The peak at 1090 cm 1 is characteristic to
A positive value was obtained, that shows that the 1
biosorption reaction is endothermic. The endothermic nature of SiO deforma- tion [72], while the band at 960 cm
the process may be explained by the fact that more than one corresponds to the C¼C stretching of alkenes [73]. The
molecule of water had to be displaced from the surface of disappearance, reduction and/or shifting of the peaks in the
biosorbent so that the metal ions can reach it [60,71]. Because FTIR diagram of Pb-loaded rapeseed suggest the implication of
the heat consumed in the diffusion step is higher than the heat hydroxyl, carboxyl, amine, C¼O, C O, C¼S and P¼C groups in
produced by adsorption, the overall enthalpy change becomes the biosorption process. A shift to lower wavenumbers indicates
positive. the weakening of the bond, while a shift to higher frequencies
denotes a stronger bond [23].
The positive value of entropy, DS, indicates the existence of
FTIR spectroscopy results proved that, beside electrostatic
randomness of the process at the liquid/solid interface, caused
attraction, other mechanism based on chemical interactions is
by the affinity of the metal ions towards the sorbent [34,51] and
involved in the removal of lead from the aqueous phase. These
the translational entropy of the displaced water molecules
interactions may be ion-exchange or complexation, or even both.
[71]. 2+
According to Eq. (5), a negative value for DG, while DS > 0, In the case of ion-exchange, one Pb ion will take the place of
+
corresponds of a reaction to be feasible, indicating the chemisorp- two monovalent anions (e.g. H ) or one divalent anion existing on
tion involved. the biosorbent surface. Biosorption of Pb(II) based on an ion-
exchange mechanism has been reported by many researchers
3.2. Biosorbent characterization [57,78]. A complexation reaction implicates four electron donor
atoms (i.e. N, O, S, P) and one divalent lead ion. Torres-
In order to understand the biosorption mechanism, ATR-FTIR Blanca et al. [79] considered that lead biosorption by de-oiled
spectroscopy was employed to identify the functional groups allspice husk involves complexation and proposed a complex
formation mechanism between Pb(II) ions and cellulose
that may be involved in the studied process. The FTIR spectra
molecules of the biosorbent. In the present study, the
were recorded before and after biosorption, in the range of 1
4000– disappearance of the peak at 1710 cm characteristic of C¼O
1
400 cm . Fig. 8 illustrates the complex nature of this material, stretching indicated surface complexion
by through Cp-cation interactions [80,81]. Based on the Hard Soft
revealing a plethora of characteristic peaks. The most important Acid Base Theory, lead is considered a soft acid or at the limit
between soft and hard acid and will interact with soft donors,
like S, P or N of the rapeseed constituents [82]. According to the
Table 6 FTIR spectra (Fig. 8 and Table 10), functionalities containing
Comparison of Pb(II) Langmuir sorption capacity (mg/g) of RS with various 1
these elements appear modified between 1700–1000 cm ,
biosorbents from literature (at room temperature).
indicating their involvement in the binding of Pb(II) ions. In
another study,
Biosorbent q max(mg/g) Ref.
Paduraru et al. [36] argued that biosorption onto rapeseed waste
was determined by the cross linking as function of Zn(II) ions
Sugarcane bagasse untreated 6.36 [64]
Sugarcane bagasse treated with H2SO4 7.297
intermolecular complexation.
Moringa olifera bark 34.6 [53] SEM images in Fig. 9 reveal the morphological changes after
Olive tree pruning waste 26.24 [62] metal sorption. Initially, the native RS surface (Fig. 9a) was
Cashew nut shell 28.65 [63]
characterized by irregularity, increased roughness and heteroge-
Raw maize stover T ea d maize stover
r te
19.65 27.1 [26]
neous pore distribution. Some distortions present on the surface
Cedar leaf ash 8.04 [25] can offer the favourable conditions for metal ions retention
Porous lignin-based sphere 27.1 [39] between the interstices. After metal binding, the material exhibits
Marula seed husk 20 [16]
smoother, with lesser porosity features (Fig. 9b). EDX analysis
Phytolacca americana 10.83 [23] indicates the elements present on the sorbent. As Fig. 9c shows, the
HNO3-modified P.americana 12.66
Rapeseed 21.29 Present study
unloaded biomass contains elements like C, O, Mg, P, S, K, Ca.
Among the constituents of rapeseed are included phytic acid, rich
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx 9

Fig. 7. Biosorption kinetics representations of Pb(II) onto rapeseed: a. pseudo-first order model, b. pseudo-second-order model. c. intraparticle diffusion model.

in phosphate groups and with affinities to Ca, K, Mg, sinapine (a
choline ester of sinapic acid), and glucosinolates, containing
sulfur and nitrogen. The EDX diagram of RS after biosorption
(Fig. 9d) shows the presence of an additional evident peak
characteristic to Pb. This clearly indicates lead retention on
rapeseed. The disappearance of some peaks of Mg, K, Ca may
suggest an ion- exchange mechanism for Pb(II) uptake.
The good correlation with the pseudo-second-order kinetic
model accompanied by the results obtained from FTIR spectrosco-
py and EDX analysis demonstrate the complexity of the
biosorption process. The high affinity of rapeseed for lead ions
most likely due to various mechanisms operating simultaneously:
(i) electrostatic interactions and (ii) chemical interactions,
including ion exchange reactions (with K+, Ca2+, Mg2+ or H+ of the
carboxyl and hydroxyl

Table 7
Kinetic description of Pb(II) biosorption on rapeseed biomass by pseudo-first and pseudo-second order models.

C0(mg/g) Pseudo-first order model Pseudo-second order model qexp(mg/g)

3 2 3 2
k1 10 (1/min) qe(mg/g) R k210 (mg/g min) qe(mg/g) R

50 11.28 2.43 0.973 8.81 6.79 0.999 6.52

100 7.6 3.82 0.919 5.41 13.24 0.999 13.08
10 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

Table 8
process under study. However, at larger scale where continuous
Intraparticle diffusion model rates for RS.
operation is preferred and the contact time is limited, this data is
C0(mg/ Intraparticle diffusion model not sufficient [38].
g)
0.5 0.5
Kid,I(mg/g min ) Kid,II(mg/ Kid,III(mg/g min )
g min
0.5
) 3.3.1. Breakthrough curve parameters
50 0.7052 0.1247 0.0608 Under dynamic conditions, a breakthrough curve is a requisite
100 1.0799 0.2338 0.1100 in order to better evaluate and understand the biosorption
behaviour and the limited capacity of the sorbent to upload
metal ions. As depicted in Fig. 11, the breakthrough curve
obtained for Pb (II) biosorption on rapeseed has a characteristic
Table 9
Thermodynamic parameters for the biosorption of Pb(II) on
“S” shape and is dependent on the inlet concentration. At lower
rapeseed. lead concentration, the curve is more lengthened and the
breakthrough point occurs later. This behaviour can be explained
Temperature ( C) DG(kJ/mol) DH(kJ/mol) DS(kJ/mol)
by the fact that at higher initial concentration the active
4 34.39 10.05 0.160
sorption sites are more rapidly covered by the metal ions [48].
20 35.33 0.155
50 35.88 0.142 From the breakthrough curve, the experimental time and
volume at breakthrough and saturation point, respectively, and
the total dynamic uptake capacity (qdyn) were determined. The
results are shown in Table 11. An increase in the feed
concentration is associated with a higher amount of metal
ions for the same quantity of sorbent and as result a smaller
volume of treated water was obtained before the sorption bed
became saturated. An increase in the Pb(II) sorption capacity
is observed at elevated concentrations. This fact could be
explained by the greater driving mass transfer force caused by a
larger metal concentration gradient between the surface of the
biomass and the solution [83,84].

3.3.2. Thomas and Yoon-Nelson models

Fig. 8. IR spectra for unloaded and metal loaded rapeseed.
groups) and/or complexation reactions. Based on the FTIR spectra
and EDX diagrams, the possible interactions that occur
between lead ions and the active sites at the surface of rapeseed
biomass can be schematized according to Fig. 10.
3.3. Fixed-bed column experiments
Biosorption investigations in batch mode of operation
provided important information about the equilibrium and
kinetics of the
The experimental data of Pb(II) biosorption on RS was
correlated with Thomas and Yoon-Nelson models (Fig. 12). Table
12 reports the findings regarding to the model parameters and
the correlation coefficient.
From Fig. 12 it can be observed that the Thomas model fitted
well the data obtained in laboratory. The correlation values for
this model were 0.930 and 0.947 for the two concentrations,
also showing good fitting with the experimental data. Thomas
model implies monolayer adsorption and describes sorption
processes where external and internal diffusion limitations are
not present [85]. This is in good agreement with the previous
batch studies. The rate constant, KT, was lower at smaller initial
concentration, while an opposite trend was observed in the case
of the maximum solid phase concentration, q0(T), which
increased at a higher inlet concentration.
Another widely used model for predicting breakthrough curves
is the Yoon-Nelson model. According to Table 12 the correlation
coefficient values obtained were comparable with the case of the
previous model. It can be affirmed that the experimental data is
verified by both models. As shown in Table 12, the time required
to accomplish 50% retention decreases with the inlet
Pb(II)

Table 10
Location of relevant IR bands and their possible assignment.
1
Transmission band (cm ) Vibration Ref.

Unloaded Loaded

3292 3274 O H and N H stretching [45,74]

2923 and 2854 2917 and 2848 H C H asymmetrical and symmetrical stretching [36,75]
1710 – C¼O stretching [4,16,73]
1651 and 1535 1647 and 1535 C¼O, C N and N H stretching [18,74]
1241 1174 C O, C¼S, P¼O stretching [25,45,76]
1037 1017 C O C or C O P stretching [72,77]
529 520 Si or sulphate stretching [67]
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx 11

Fig. 9. SEM images of rapeseed before (a) and after (b) biosorption and EDX spectra of rapeseed before (c) and after (d) biosorption.
12 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

Fig. 10. Schematic representation of possible interactions involved in the Pb(II)/RS sorption process.

Fig. 11. Breakthrough curves for biosorption of Pb(II) on rapeseed at different influent concentrations.

Table 11
Experimental parameters of the breakthrough curves for Pb(II) biosorption.

C0(mg/L) tb(min) Vb(L) ts(min) Vs(L) qt(mg/g)

50 100.78 0.25 188.48 0.47 20.37

100 89.91 0.22 181.63 0.45 40.04

C0 (mg/L) – influent concentration, tb (min)– breakthrough time (Ct/C0 = 0.1), Vb (L) – breakthrough volume, ts (min) – saturation time (Ct/C0 = 0.9), Vs (L) – saturation
volume,
qdyn (mg/g) – total dynamic uptake capacity.

concentration of tested solutions, implying a faster column
saturation at higher concentration.
Thomas model, as well as Yoon-Nelson model, has given
sorption capacities which are higher than the one provided by
Langmuir equation, i.e. 21.29 mg/g at room temperature.
This implies that the rapeseed biomass has preference for
diffusion in fixed bed column mode rather than in batch
conditions [83].
3.4. Experiments with industrial wastewater
The physico-chemical characteristics of the industrial waste-
water before and after column treatment are presented in Table
13. After 200 mL of the water has passed through the rapeseed-
packed column, the content of Pb(II) was reduced with over 94%.
This fact clearly indicates the affinity of rapeseed biomass for lead
ions even
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx 13

Fig. 12. Representations of Thomas (a) and Yoon-Nelson (b) models for lead(II) biosorption on RS-packed column.

Table 12
Thomas and Yoon-Nelson models parameters for the sorption of Pb(II) in fixed bed column.

C0(mg/L) Thomas model Yoon-Nelson model

KT10
3
(L/min/mg) q0(T)(mg/g) R
2
kYN(1/min) t (min) q0(YN)(mg/g) R
2

50 1.55 23.98 0.930 0.0367 197.47 35.17 0.916

100 0.58 48.81 0.947 0.0479 143.11 51.11 0.927

*
in the presence of other compounds. In addition, the other Calculated as RE (%) = (Cinitial–Cfinal)*100/Cinitial.
quality indicators considered in this experiment, like chemical
oxygen demand (COD), total suspended solids (TSS), chloride
and water hardness showed a significant improvement (Table
13). In conclusion, these results reflect the ability of rapeseed to
remove Pb(II) ions and organic compounds from real
wastewater.

Table 13
Treated water characteristics.
*
Quality indicator (units) Treated water Removal efficiency (RE,%)

pH 7.01 9.89
TSS (mg/L) 48 30.43
COD (mg/L) 256 50.35
2+
Pb (mg/L) 0.27 94.47
Cl (mg/L) 124 17.33
Total hardness ( G) 3.52 71.61
4. Conclusions

The present study investigated Pb(II) biosorption on rapeseed

biomass in batch conditions and fixed bed columns. The use of
this biosorbent can help alleviate two environmental
problems – wastewater contamination and agricultural waste
disposal.
Equilibrium studies in batch conditions have shown that
lead biosorption is strongly influenced by the initial metal
concentration, contact time and temperature, as higher uptake
capacities are obtained by increasing each of these operating
parameters. Kinetic modeling indicated the applicability of
pseudo-second-order model to better describe the Pb(II)/RS
system, but the intraparticle diffusion also played an important
role in the biosorption process. Langmuir isotherm model
describes very well the experimental data, with high correlation
coefficients for all the studied temperatures. The
negative value of DG and the positive values for DH and DS
indicated the spontaneity, endothermic nature and randomness of
the process under study. FTIR analysis suggested that the
hydroxyl, carboxyl, amine groups as well as C¼O, C O, C¼S and
P¼C groups may interact with Pb(II), while SEM/EDX analysis
confirmed the
14 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx

presence of lead on RS surface and indicated that an ion- doi:http://dx.doi.org/

10.1016/j.seppur.2015.12.0 08.
exchange mechanism would be involved in addition to [13] Fu F, Wang Q. Removal of heavy metal ions from wastewaters: a review.
electrostatic interactions and complexation reactions. J Environ Manage 2011;92:407–18, doi:http://dx.doi.org/10.1016/j.
Biosorption capacity for 50 mg/L and 100 mg/L feed concentra- jenvman.2010.11.011.
tion of lead ions for dynamic tests were higher than the batch
conditions for the same initial concentrations, indicating the
suitability of the biosorbent in the column mode operation. The
breakthrough curve obtained for Pb(II) biosorption on rapeseed
presented a steeper slope for a higher metal inlet concentration.
Thomas model successfully predicted breakthrough curves and
the calculated sorption capacity from this model was in
agreement with the value of Langmuir isotherm. Column
studies with real industrial wastewater presented a removal
efficiency of 94.47% for Pb(II) and a general improvement of the
other quality indicators from the effluent showed the practical
utility of the biosorbent.
Further research includes more investigations regarding the
operating parameters of continuous biosorption process, sorbent
regeneration and metal recovery options.

Acknowledgement

This work was supported by a grant of the Romanian National

Authority for Scientific Research, CNDI–UEFISCDI, project no. 60/
2012, “Integrated System for Reducing Environmental and
Human- related Impacts and Risks in the Water Use Cycle”
(WATUSER).
The support of the University of Basel, Switzerland (research
group of Prof.dr. Cornelia Palivan) is also gratefully acknowledged
for the contribution to some of the characterization tests.

References

[1] Jitar O, Teodosiu C, Oros A, Plavan G, Nicoara M. Bioaccumulation of heavy

metals in marine organisms from the Romanian sector of the Black Sea. N
Biotechnol 2015;32:369–78, doi:http://dx.doi.org/10.1016/j.nbt.2014.11.0 04.
[2] Olguín EJ, Sánchez-Galván G. Heavy metal removal in phytofiltration and
phycoremediation: the need to differentiate between bioadsorption and
bioaccumulation. N Biotechnol 2012;30:3–8, doi:http://dx.doi.org/10.1016/j.
nbt.2012.05.020.
[3] Largitte L, Lodewyckx P. Modeling the influence of the operating conditions
upon the sorption rate and the yield in the adsorption of lead(II).
Microporous Mesoporous Mater 2015;202:147–54,
doi:http://dx.doi.org/10.1016/j. micromeso.2014.09.045.
[4] Meitei MD, Prasad MNV. Lead (II) and cadmium (II) biosorption on spirodela
polyrhiza (L.) schleiden biomass. J Environ Chem Eng 2013;1:20 0–7, doi:
http://dx.doi.org/10.1016/j.jece.2013.04.016.
[5] Pawar RR, Lalhmunsiama PL, Bajaj Lee HCS-M. Activated bentonite as a
low-
cost adsorbent for the removal of Cu(II) and Pb(II) from aqueous solutions:
batch and column studies. J Ind Eng Chem 2016;34:213–23,
doi:http://dx.doi. org/10.1016/j.jiec.2015.11.014.
[6] World Health Organization International Agency for Reseach on Cancer.
Inorganic and organic lead compounds, vol. 87. Lyon, France: International
Agency for Research on Cancer; 20 06.
[7] USEPA. Code of Federal Regulations 40 EPA Part 423 Appendix A. US EPA;
2014. [8] Volesky B. Detoxification of metal-bearing effluents: biosorption for
the next century. Hydrometallurgy 20 01;59:203–16,
doi:http://dx.doi.org/10.1016/
S0304-386X(00)0 0160-2.
[9] Vijayaraghavan K, Balasubramanian R. Is biosorption suitable for
decontamination of metal-bearing wastewaters? A critical review on the
state-of-the-art of biosorption processes and future directions. J Environ
Manage 2015;160:283–96, doi:http://dx.doi.org/10.1016/j.
jenvman.2015.06.030.
[10] Al-Zoubi H, Ibrahim KA, Abu-Sbeih KA. Removal of heavy metals from
wastewater by economical polymeric collectors using dissolved air flotation
process. J Water Process Eng 2015;8:19–27, doi:http://dx.doi.org/10.1016/j.
jwpe.2015.08.002.
[11] Misra RK, Jain SK, Khatri PK. Iminodiacetic acid functionalized cation
exchange resin for adsorptive removal of Cr(VI), Cd(II), Ni(II) and Pb(II)
from their aqueous solutions. J Hazard Mater 2011;185:1508–12,
doi:http://dx.doi.org/
10.1016/j.jhazmat.2010.10.077.
[12] Huang Y, Wu D, Wang X, Huang W, Lawless D, Feng X. Removal of heavy
metals from water using polyvinylamine by polymer-enhanced
ultrafiltration and flocculation. Sep Purif Technol 2016;158:124–36,
[14] Gundogdu A, Ozdes D, Duran C, Bulut VN, Soylak M, Senturk HB. Biosorption of removal of lead ions from aqueous media. J Hazard Mater 2015;285:77–83,
Pb(II) ions from aqueous solution by pine bark (Pinus brutia Ten.). Chem Eng J doi:http://dx.doi.org/10.1016/j.jhazmat.2014.11.033.
20 09;153:62–9, doi:http://dx.doi.org/10.1016/j.cej.20 09.0 6.017.
[15] Nguyen TAH, Ngo HH, Guo WS, Zhang J, Liang S, Yue QY, et al. Applicability of
agricultural waste and by-products for adsorptive removal of heavy metals
from wastewater. Bioresour Technol 2013;148:574–85,
doi:http://dx.doi.org/
10.1016/j.biortech.2013.08.124.
[16] Moyo M, Guyo U, Mawenyiyo G, Zinyama NP, Nyamunda BC. Marula seed
husk (Sclerocarya birrea) biomass as a low cost biosorbent for removal of
Pb(II) and Cu(II) from aqueous solution. J Ind Eng Chem 2015;27:126–32,
doi:http://dx.
doi.org/10.1016/j.jiec.2014.12.026.
[17] Altenor S, Gaspard S. Biomass for water treatment: biosorbent, coagulants
and
flocculants. Biomass Sustain Appl Pollut Remediat Energy R Soc Chem 2014;1–
45, doi:http://dx.doi.org/10.1039/9781849737142-0 0 0 01.
[18] Araujo CST, Carvalho DC, Rezende HC, Almeida ILS, Coelho LM, Coelho NMM,
et al. Bioremediation of waters contaminated with heavy metals using
Moringa oleifera seeds as biosorbent. Appl Biorem Act Passive Approach
InTech 2013;227–55, doi:http://dx.doi.org/10.5772/56157.
[19] Fomina M, Gadd GM. Biosorption: current perspectives on concept, definition
and application. Bioresour Technol 2014;160:3–14, doi:http://dx.doi.org/
10.1016/j.biortech.2013.12.102.
[20] Hlihor RM, Diaconu M, Leon F, Curteanu S, Tavares T, Gavrilescu M.
Experimental analysis and mathematical prediction of Cd(II) removal by
biosorption using support vector machines and genetic algorithms. N
Biotechnol 2015;32:358–68,
doi:http://dx.doi.org/10.1016/j.nbt.2014.08.0 03.
[21] Zhou K, Yang Z, Liu Y, Kong X. Kinetics and equilibrium studies on
biosorption of Pb(II) from aqueous solution by a novel biosorbent: cyclosorus
interruptus. J Environ Chem Eng 2015;3:2219–28,
doi:http://dx.doi.org/10.1016/j. jece.2015.08.0 02.
[22] Feizi M, Jalali M. Removal of heavy metals from aqueous solutions using
sunflower, potato, canola and walnut shell residues. J Taiwan Inst Chem Eng
2015;54:125–36, doi:http://dx.doi.org/10.1016/j.jtice.2015.03.027.
[23] Wang G, Zhang S, Yao P, Chen Y, Xu X, Li T, et al. Removal of Pb(II) from
aqueous solutions by Phytolacca americana L. biomass as a low cost
biosorbent. Arab J Chem 2016;2014:0–11,
doi:http://dx.doi.org/10.1016/j.arabjc.2015.0 6.011.
[24] Ronda A, Calero M, Blázquez G, Pérez A, Martín-Lara MA. Optimization of the
use of a biosorbent to remove heavy metals: regeneration and reuse of
exhausted biosorbent. J Taiwan Inst Chem Eng 2015;51:109–18,
doi:http://dx. doi.org/10.1016/j.jtice.2015.01.016.
[25] Hafshejani LD, Nasab SB, Gholami RM, Moradzadeh M, Izadpanah Z,
Hafshejani SB, et al. Removal of zinc and lead from aqueous solution by
nanostructured cedar leaf ash as biosorbent. J Mol Liq 2015;211:448–56,
doi:http://dx.doi.org/
10.1016/j.molliq.2015.07.04 4.
[26] Guyo U, Mhonyera J, Moyo M. Pb(II) adsorption from aqueous solutions by
raw and treated biomass of maize stover—a comparative study. Process Saf
Environ Prot 2015;93:192–20 0,
doi:http://dx.doi.org/10.1016/j.psep.2014.06.0 09.
[27] Taşar Ş, Kaya F, Özer A. Biosorption of lead(II) ions from aqueous solution
by peanut shells: equilibrium, thermodynamic and kinetic studies. J Environ
Chem Eng 2014;2:1018–26, doi:http://dx.doi.org/10.1016/j.jece.2014.03.015.
[28] López-Mesas M, Navarrete ER, Carrillo F, Palet C. Bioseparation of Pb(II) and
Cd (II) from aqueous solution using cork waste biomass. Modeling and
optimization of the parameters of the biosorption step. Chem Eng J
2011;174:9–17, doi:http://dx.doi.org/10.1016/j.cej.2011.07.026.
[29] Carré P, Pouzet A. Rapeseed market, worldwide and in Europe. OCL 2014;21:
D102, doi:http://dx.doi.org/10.1051/ocl/2013054.
[30] No Title n.d. http://www.madr.ro/culturi-de-camp/plante-tehnice/rapita-
pentru-ulei.html (accessed 23.02.16).
[31] Ga˛siorek E, Wilk M. Possibilities of utilizing the solid by-products of
biodiesel production—a review. Polish J Chem Technol 2011;13:58–62,
doi:http://dx.doi. org/10.2478/v10 026-011-0 012-y.
[32] Al-Asheh S, Duvnjak Z. Sorption of heavy metals by canola meal. Water Air Soil
Pollut 1999;114:251–76, doi:http://dx.doi.org/10.1023/A:10 05093821620.
[33] Németh D, Labidi J, Gubicza L, Bélafi-Bakó K. Comparative study on heavy
metal removal from industrial effluents by various separation methods.
Desalin Water Treat 2011;35:242–6, doi:http://dx.doi.org/10.50 04/
dwt.2011.2438.
[34] Tofan L, Paduraru C, Volf I, Toma O. Waste of rapeseed from biodiesel
production as a potential biosorbent for heavy metal ions. Bioresources
2011;6:3727–41.
[35] Štefušová K, Lovás M, Zubrik A, Matik M, Václavíková M. Removal of Cd2+ and
Pb2+ from aqueous solutions using bio-char residues. Nova Biotechnol Chim
2012;2:139–46, doi:http://dx.doi.org/10.2478/v10296-012-0 016-x.
[36] Paduraru C, Tofan L, Teodosiu C, Bunia I, Tudorachi N, Toma O. Biosorption of
zinc(II) on rapeseed waste: equilibrium studies and thermogravimetric
investigations. Process Saf Environ Prot 2015;94:18–28, doi:http://dx.doi.org/
10.1016/j.psep.2014.12.0 03.
[37] Bhatnagar A, Sillanpää M, Witek-Kr owiak A. Agricultural waste peels as
versatile biomass for water purification–A review. Chem Eng J 2015;270:244–
71, doi:http://dx.doi.org/10.1016/j.cej.2015.01.135.
[38] Cruz-Olivares J, Pérez-Alonso C, Barrera-Díaz C, Ureña-Nuñez F, Chaparro-
Mercado MC, Bilyeu B. Modeling of lead (II) biosorption by residue of allspice
in a fixed-bed column. Chem Eng J 2013;228:21–7, doi:http://dx.doi.org/
10.1016/j.cej.2013.04.101.
[39] Li Z, Ge Y, Wan L. Fabrication of a green porous lignin-based sphere for the
 I. Morosanu et al. / New Biotechnology xxx (2016) xxx–xxx
[40] Long Y, Lei D, Ni J, Ren Z, Chen C, Xu H. Packed bed column studies on
lead(II) removal from industrial wastewater by modified Agaricus bisporus.
Bioresour Technol 2014;152:457–63, doi:http://dx.doi.org/10.1016/j.
biortech.2013.11.039.
[41] Sadeek SA, Negm NA, Hefni HHH, Wahab MMA. Metal adsorption by
agricultural biosorbents: adsorption isotherm, kinetic and biosorbents
chemical structures. Int J Biol Macromol 2015;81:40 0–9,
doi:http://dx.doi.org/
10.1016/j.ijbiomac.2 015.08.031.
[42] Foo KY, Hameed BH. Insights into the modeling of adsorption isotherm
systems. Chem Eng J 2010;156:2–10, doi:http://dx.doi.org/10.1016/j.
cej.20 09.09.013.
[43] Gautam RK, Mudhoo A, Lofrano G, Chattopadhyaya MC. Biomass-derived
biosorbents for metal ions sequestration: adsorbent modification and
activation methods and adsorbent regeneration. J Environ Chem Eng
2014;2:239–59, doi:http://dx.doi.org/10.1016/j.jece.2013.12.019.
[44] Rangabhashiyam S, Anu N, Giri Nandagopal MS, Selvaraju N. Relevance of
isotherm models in biosorption of pollutants by agricultural byproducts. J
Environ Chem Eng 2014;2:398–414, doi:http://dx.doi.org/10.1016/j.
jece.2014.01.014.
[45] Basu M, Guha AK, Ray L. Biosorptive removal of lead by lentil husk. J Environ
Chem Eng 2015;3:1088–95, doi:http://dx.doi.org/10.1016/j.jece.2015.04.024.
[46] Anastopoulos I, Kyzas GZ. Are the thermodynamic parameters correctly
estimated in liquid-phase adsorption phenomena? J Mol Liq 2016;218:174–
85, doi:http://dx.doi.org/10.1016/j.molliq.2016.02.059.
[47] Zhou X, Zhou X. The unit problem in the thermodynamic calculation of
adsorption using the langmuir equation. Chem Eng Commun
2014;201:1459–
67, doi:http://dx.doi.org/10.1080/009864 45.2013.818541.
[48] Bhaumik M, Setshedi K, Maity A, Onyango MS. Removal from water using
fixed bed column of polypyrrole/Fe 3O4 nanocomposite. Sep Purif Technol
2013;110:11–9, doi:http://dx.doi.org/10.1016/j.seppur.2013.02.037.
[49] Sotelo JL, Rodríguez A, Álvarez S, García J. Removal of caffeine and diclofenac
on activated carbon in fixed bed column. Chem Eng Res Des 2012;90:967–
74, doi:http://dx.doi.org/10.1016/j.cherd.2011.10.012.
[50] Al-Ghouti MA, Khraisheh MAM, Ahmad MN, Allen SJ. Microcolumn studies of
dye adsorption onto manganese oxides modified diatomite. J Hazard Mater
20 07;146:316–27, doi:http://dx.doi.org/10.1016/j.jhazmat.20 06.12.024.
[51] Li Q, Tang X, Sun Y, Wang Y, Long Y, Jiang J, et al. Removal of Rhodamine B
from wastewater by modified Volvariella volvacea: batch and column study.
RSC Adv 2015;5:25337–47, doi:http://dx.doi.org/10.1039/C4RA17319H.
[52] Xu D, Tan X, Chen C, Wang X. Removal of Pb(II) from aqueous solution by
oxidized multiwalled carbon nanotubes. J Hazard Mater 20 08;154:407–16,
doi:http://dx.doi.org/10.1016/j.jhazmat.20 07.10.059.
[53] Reddy DHK, Seshaiah K, Reddy AVR, Rao MM, Wang MC. Biosorption of Pb2+
from aqueous solutions by Moringa oleifera bark: equilibrium and kinetic
studies. J Hazard Mater 2010;174:831–8, doi:http://dx.doi.org/10.1016/j.
jhazmat.20 09.09.128.
[54] Villaescusa I, Fiol N, Martı’nez M, Miralles N, Poch J, Serarols J. Removal of
copper and nickel ions from aqueous solutions by grape stalks wastes. Water
Res 20 04;38:992–10 02, doi:http://dx.doi.org/10.1016/j.watres.2003.10.040.
[55] Guo H, Zhang S, Kou Z, Zhai S, Ma W, Yang Y. Removal of cadmium(II)
from aqueous solutions by chemically modified maize straw. Carbohydr
Polym
2015;115:177–85, doi:http://dx.doi.org/10.1016/j.carbpol.2014.08.041.
[56] Flores-Garnica JG, Morales-Barrera L, Pineda-Camacho G, Cristiani-Urbina E.
Biosorption of Ni(II) from aqueous solutions by Litchi chinensis seeds.
Bioresour Technol 2013;136:635–43, doi:http://dx.doi.org/10.1016/j.
biortech.2013.02.059.
[57] Abdolali A, Ngo HH, Guo W, Lu S, Chen SS, Nguyen NC, et al. A breakthrough
biosorbent in removing heavy metals: equilibrium, kinetic, thermodynamic
and mechanism analyses in a lab-scale study. Sci Total Environ
2016;542:603–
11, doi:http://dx.doi.org/10.1016/j.scitotenv.2015.10.095.
[58] Limousin G, Gaudet J-P, Charlet L, Szenknect S, Barthès V, Krimissa M.
Sorption isotherms: a review on physical bases, modeling and measurement.
Appl Geochem 20 07;22:249–75, doi:http://dx.doi.org/10.1016/j.
apgeochem.2006.09.010.
[59] Naiya TK, Bhattacharya AK, Mandal S, Das SK. The sorption of lead(II) ions on
rice husk ash. J Hazard Mater 20 09;163:1254–64, doi:http://dx.doi.org/
10.1016/j.jhazmat.20 08.07.119.
[60] Chowdhury S, Das Saha P. Biosorption kinetics, thermodynamics and
isosteric heat of sorption of Cu(II) onto Tamarindus indica seed powder.
Colloids Surf B Biointerfaces 2011;88:697–705,
doi:http://dx.doi.org/10.1016/j. colsurfb.2011.08.0 03.
[61] Saha P, Chowdhury S. Insight into adsorption thermodynamics. Thermodyn
InTech 2011, doi:http://dx.doi.org/10.5772/13474.
[62] Blázquez G, Martín-Lara MA, Tenorio G, Calero M. Batch biosorption of
lead(II) from aqueous solutions by olive tree pruning waste: equilibrium,
kinetics and thermodynamic study. Chem Eng J 2011;168:170–7,
doi:http://dx.doi.org/
10.1016/j.cej.2010.12.059.
[63] Coelho GF, Gonçalves Jr. AC, Tarley CRT, Casarin J, Nacke H, Francziskowski
MA .
Removal of metal ions Cd (II), Pb (II), and Cr (III) from water by the cashew
nut
15
shell Anacardium occidentale L. Ecol Eng 2014;73:514–25,
doi:http://dx.doi. org/10.1016/j.ecoleng.2014.09.103.
[64] Martín-Lara MA, Rico ILR, Vicente I de la CA, García GB, de Hoces MC.
Modification of the sorptive characteristics of sugarcane bagasse for
removing lead from aqueous solutions. Desalination 2010;256:58–63,
doi:http://dx.doi. org/10.1016/j.desal.2010.02.015.
[65] Mushtaq M, Bhatti HN, Iqbal M, Noreen S. Eriobotrya japonica seed
biocomposite efficiency for copper adsorption: isotherms, kinetics,
thermodynamic and desorption studies. J Environ Manage 2016;176:21–33,
doi:http://dx.doi.org/10.1016/j.jenvman.2016.03.013.
[66] Ofomaja AE. Intraparticle diffusion process for lead(II) biosorption onto
mansonia wood sawdust. Bioresour Technol 2010;101:5868–76,
doi:http://dx. doi.org/10.1016/j.biortech.2010.03.033.
[67] Nadeem R, Manzoor Q, Iqbal M, Nisar J. Biosorption of Pb(II) onto
immobilized and native Mangifera indica waste biomass. J Ind Eng Chem
2015;22–5, doi: http://dx.doi.org/10.1016/j.jiec.2015.12.030.
[68] Ho YS, Ng JCY, McKay G. Kinetics of pollutant sorption by biosorbents: review.
Sep Purif Rev 200 0;29:189–232, doi:http://dx.doi.org/10.1081/SPM-
10 01000 09.
[69] Chowdhury ZZ, Zain SM, Khan RA. Studies of lead (II) cations from aqueous
solutions onto granular activated carbon derived from mangostana garcinia.
BioResources 2012;7:2895–915, doi:http://dx.doi.org/10.15376/
biores.7.3.2895-2915.
[70] Liang S, Guo X, Feng N, Tian Q. Isotherms, kinetics and thermodynamic
studies of adsorption of Cu2+ from aqueous solutions by Mg2+/K+ type
orange peel adsorbents. J Hazard Mater 2010;174:756–62,
doi:http://dx.doi.org/10.1016/j. jhazmat.20 09.09.116.
[71] Anirudhan TS, Radhakrishnan PG. Thermodynamics and kinetics of adsorption
of Cu(II) from aqueous solutions onto a new cation exchanger derived from
tamarind fruit shell. J Chem Thermodyn 20 08;40:702–9, doi:http://dx.doi.org/
10.1016/j.jct.2007.10.005
.
[72] Smidt E, Böhm K, Schwanninger M. The application of FT-IR spectroscopy in
waste management. fourier transform. New Anal Approach FTIR Strateg
InTech
2011;405–30, doi:http://dx.doi.org/10.5772/15998.
[73] Kuppusamy S, Thavamani P, Megharaj M, Venkateswarlu K, Lee YB, Naidu R.
Potential of Melaleuca diosmifolia leaf as a low-cost adsorbent for
hexavalent chromium removal from contaminated water bodies. Process Saf
Environ Prot
2016;10 0:173–82,
doi:http://dx.doi.org/10.1016/j.psep.2016.01.0 09.
[74] Yuvaraja G, Krishnaiah N, Subbaiah MV, Krishnaiah A. Biosorption of Pb(II)
from aqueous solution by Solanum melongena leaf powder as a low-cost
biosorbent prepared from agricultural waste. Colloids Surf B Biointerfaces
2014;114:75–81,
doi:http://dx.doi.org/10.1016/j.colsurfb.2013.09.039.
[75] Smidt E, Eckhardt KU, Lechner P, Schulten HR, Leinweber P. Characterization
of different decomposition stages of biowaste using FT-IR spectroscopy and
pyro lysis-field ionization mass spectrometry. Biodegradation 20 05;16:67–79,
doi:http://dx.doi.org/10.10 07/s10531-0 04-0430-8.
[76] Qi W, Zhao Y, Zheng X, Ji M, Zhang Z. Adsorption behavior and mechanism of
Cr (VI) using Sakura waste from aqueous solution. Appl Surf Sci
2016;360:470–6, doi:http://dx.doi.org/10.1016/j.apsusc.2015.10.088.
[77] Cui X, Hao H, Zhang C, He Z, Yang X. Capacity and mechanisms of ammonium
and cadmium sorption on different wetland-plant derived biochars. Sci Total
Environ 2016;539:566–75, doi:http://dx.doi.org/10.1016/j.
scitotenv.2015.09.022.
[78] Chojnacka K. Biosorption and bioaccumulation—the prospects for practical
applications. Environ Int 2010;36:299–307, doi:http://dx.doi.org/10.1016/j.
envint.2009.12.0 01.
[79] Torres-Blancas T, Roa-Morales G, Fall C, Barrera-Díaz C, Ureña-Nuñez F, Pavón
Silva TB. Improving lead sorption through chemical modification of de-oiled
allspice husk by xanthate. Fuel 2013;110:4–11,
doi:http://dx.doi.org/10.1016/j. fuel.2012.11.013.
[80] Xu X, Cao X, Zhao L, Wang H, Yu H, Gao B. Removal of Cu Zn, and Cd from
aqueous solutions by the dairy manure-derived biochar. Environ Sci Pollut
Res
2013;20:358–68, doi:http://dx.doi.org/10.10 07/s11356-012-0873-
5.
[81] Tran HN, You S-J, Chao H-P. Effect of pyrolysis temperatures and times on
the adsorption of cadmium onto orange peel derived biochar. Waste Manag
Res
2016;34:129–38,
doi:http://dx.doi.org/10.1177/0734242X15615698.
[82] Naja G, Murphy V, Volesky B. Biosorption. Metals. Encycl. Ind. Biotechnol.
2010;1–29.
[83] Tofan L, Paduraru C, Teodosiu C, Toma O. Fixed bed column study on the
removal of chromium (III) ions from aqueous solutions by using hemp fibers
with improved sorption performance. Cell. Chem. Technol. 2015;49:219–29.
[84] Luo X, Deng Z, Lin X, Zhang C. Fixed-bed column study for Cu2+ removal from
solution using expanding rice husk. J Hazard Mater 2011;187:182–9, doi:
http://dx.doi.org/10.1016/j.jhazmat.2011.01.019.
[85] Muthusamy S, Venkatachalam S. Competitive biosorption of Cr(VI) and Zn(II)
ions in single- and binary-metal systems onto a biodiesel waste residue using
batch and fixed-bed column studies. RSC Adv 2015;5:45817–26,
doi:http://dx. doi.org/10.1039/C5RA05962C.