Journal of Cleaner Production 150 (2017) 58e64

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Journal of Cleaner Production

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Biosorption of nickel(II) and copper(II) ions in batch and fixed-bed

columns by free and immobilized marine algae Sargassum sp.
C.E.R. Barquilha a, *, E.S. Cossich a, C.R.G. Tavares a, E.A. Silva b
a
Department of Chemical Engineering, State University of Maringa
, Av. Colombo 5790, CEP 47020-900, Maringa
, PR, Brazil
b
, Rua da Faculdade 2550, CEP 85903-000, Toledo, PR, Brazil
School of Chemical Engineering, State University of West Parana

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

Article history: In this study, the brown algae harvested in the State of Pernambuco - Brazil, Sargassum species, and the
Received 15 September 2016 commercial sodium alginate were used as free and immobilized biosorbents for the removal of nickel
Received in revised form and copper ions in batch and continuous experiments from aqueous solutions. The alginate beads and
23 February 2017
immobilized biosorbent were produced from the ionic polymerization using the drip method in calcium
Accepted 28 February 2017
Available online 7 March 2017
chloride solution. Equilibrium data show that the calcium alginate matrix increased the maximum
biosorption capacity in immobilization, and both biosorbent materials presented greater affinity and
uptake capacity for copper ions than for nickel ions. The experimental results were better fitted to the
Keywords:
Sargassum species
Langmuir model than to the Freundlich model, obtaining favorable type isotherms. Continuous systems
Alginate showed a different equilibrium condition, once the experiments carried out in fixed-bed columns pre-
Biosorbents sented higher biosorption capacity than those performed in batch experiments, also suggesting that the
Immobilized bed packed with immobilized biosorbent was not affected by the low porosity. The immobilized bio-
Fixed-bed columns sorbent also had easy packing.
© 2017 Elsevier Ltd. All rights reserved.

1. Introduction treating highly diluted solutions (Mata et al., 2009). As an alter-

Heavy metals are metallic elements that have density over
5.0 g cm3, such as nickel and copper, are very important for global
development (Ja €rup, 2003). Many activities use heavy metals in
their manufacturing process or product. Nickel is intensely used in
its pure form as coating of metal pieces, because it presents great
resistance to corrosion and oxidation. Copper is an excellent
conductor of heat and electricity, it is used in different areas, such
as electrical industry, construction, galvanization, agricultural
products, among others (de-Bashan and Bashan, 2010). However,
heavy metals can represent a significant pollution source. Although
these metals are essential for living beings, some species and high
concentrations can be highly toxic, persistent in the environment
(non-biodegradable), and bioaccumulative in food chain (He and
Chen, 2014).
Treatment technologies for removal of metals from industrial
effluents include chemical precipitation, electrochemical, mem-
branes filtration, ion exchange, adsorption and evaporation. How-
ever, these methods are usually expensive or inappropriate for
* Corresponding author.
E-mail address: eng.amb_barq@hotmail.com (C.E.R. Barquilha).
native, biosorption is a process that uses inexpensive biomass in
order to remove metal ions from complex and highly diluted so-
lutions. According to Naja and Volesky (2011), biosorption is a
complex process that can involve mechanisms of ion exchange,
physical adsorption, chemical adsorption, including complexation/
chelation, and precipitation. There are several biomass evaluated
for removal of metals, such as bacteria, fungi, algae and agro-
industrial residues (Gadd, 2009; Wang and Chen, 2009). Marine
algae are identified as a promising biosorbents due to their high
biosorption capacities, low cost, renewability and abundance in
many regions of the world (He and Chen, 2014). Among the diverse
species of marine algae, brown algae has been attracting attention
because it presents polysaccharides alginate and fucoidan, which
are active in ion exchange processes (Davis et al., 2003; Romera
et al., 2006).
Biosorption as a technology for the removal and recovery of
metals will only be competitive when utilized in continuous sys-
tems to treat large volumes, such as the fixed-bed columns (Cossich
et al., 2004). Fixed-bed column is easy to operate, it requires small
space, ensures high concentration gradient, and allows the treat-
ment of large volumes of metal solutions (Da Silva et al., 2002). In
scaling up the biosorption process, the use of free particulate

http://dx.doi.org/10.1016/j.jclepro.2017.02.199
0959-6526/© 2017 Elsevier Ltd. All rights reserved.
 C.E.R. Barquilha et al. / Journal of Cleaner Production 150 (2017) 58e64 59

biosorbents has some drawbacks including small particle size, low

mechanical strength, strong densification and poor distribution in
bed. These disadvantages cause problems in columns, such as the
decrease of the process efficiency, difficulties in separation process,
poor regeneration/reuse (Fomina and Gadd, 2014). Biomass
immobilization in polymeric matrices (as alginate) can then
improve the bed packing, producing biosorbent with particle size,
mechanical resistance, and rigidity adequate for use in fixed-bed
column. Alginate is a polymer that occurs in all brown algae and
have the property of reacting with polyvalent cations such as cal-
cium, producing strong gels (Romera et al., 2006).
Abu Al-Rub et al. (2004) analyzed Chlorella vulgaris immobilized
in alginate beads in nickel removal. They have observed that the
immobilization enhanced the biosorption ability and enabled the
use of the biosorbent in various sorption/desorption cycles with the
same removal potential. Other studies also have evaluated the
immobilization of seaweed (Mata et al., 2009), fungus (Hanif et al.,
2015), and agricultural wastes (Kausar et al., 2016) biomass in
alginate matrix; however, all these studies were carried out in
batch experiments.
Therefore, the objective of this work was to evaluate seaweed
Sargassum sp. immobilized in alginate for the removal of copper
and nickel through a fixed-bed column system.
Fig. 1. Production of Ca-alginate beads by drip method.

2. Materials and methods

2.1. Materials
Seaweed Sargassum sp., purchased from algae collectors coop-
erative of Pernambuco State e Brazil, was washed with distilled
water, dried at 60
C, mashed in blender, separated in sieve from
Tyler’s series and stored in closed recipients. Particles with an
average diameter of 1.5 mm were used in batch experiments;
particles with an average diameter of 2.2 mm were used in column
experiments, and particles with diameter smaller than 150 mm
were used in the immobilization. Commercial sodium alginate
^
(Exodo Científica, Brazil) was used for biomass immobilization.
The metal solutions were prepared from the dissolution of
nickel sulfate (NiSO4.6H2O, Synth, Brazil) and copper sulfate
(CuSO4.5H2O, Synth, Brazil) in distilled water.
2.2. Biomass immobilizations
Immobilized biosorbents were prepared in form of alginate
beads by ionic polymerization in calcium chloride solution, ac-
cording to the method used by Abu Al-Rub et al. (2004). An amount
of up to 0.50% (w=v) of Sargassum sp. powdered was mixed in 2%
sodium alginate solution. This mixture was then dropped into a 4%
^ qe ¼
calcium chloride solution (CaCl2.2H2O, Exodo Científica, Brazil)
using a peristaltic pump. The beads were kept in the calcium so-
lution for at least 4 h for complete gelation. After that, the beads
were washed with distilled water to remove excess CaCl2 and
stored in sealed recipient at room temperature until next use. For
Ca-alginate beads only, similar procedures were used, but without
brown algae. The biosorbents moisture was determined in oven at
105
C for at least 24 h.
Fig. 1 depicts the experimental apparatus used for immobiliza-
tion, where a syringe was coupled into the tubing and dripping
height was fixed at 20 cm.
placed in contact with 0.1 g of biosorbent (free biomass, immobi-
lized algae in alginate beads and alginate beads) at a constant
temperature of 30
C, stirred at 150 rpm and pH 5.0, periodically
adjusted with sulfuric acid. Assays duration was determined by
biosorption kinetics carried out previously, obtaining 4 h for nickel
and 6 h for copper. Initial and equilibrium concentrations were
determined by atomic absorption spectroscopy (VARIAN - SpectrAA
50B). The amount of metal biosorbed was calculated using the
equation:
ðCi  Ce ÞV
qe ¼ (1)
ms
where qe is the amount of metal uptake in equilibrium (mmol g 1 ),
Ci e Ce are the initial and equilibrium metal concentrations in the
solution (mmol L1 ), V is the volume of the solution (L), and ms is
the biosorbent dry weight (g).
The Langmuir (Equation (2)) and Freundlich (Equation (3)) iso-
therms were fitted to equilibrium data by non-linear regression
using the software Origin 7.0 (Langmuir, 1918; Freundlich, 1906;
apud Wang and Chen, 2009).
Qmax bCe
(2)
1 þ bCe
1=n
qe ¼ KF Ce (3)
In Langmuir model, Qmax ðmmol g 1 Þ
is the maximum bio-
sorption capacity (i.e., when the surface is completely covered with
metal ions), and b ðg mmol1 Þ is a Langmuir constant that repre-
sents the affinity between the biosorbent and the metal ion. While
in Freundlich model, kF ððL mmol1 Þ1=n ðmmol g 1 ÞÞ is Freundlich
constant related to uptake capacity and n is Freundlich exponent
known as biosorbent intensity (Akbari et al., 2015).

2.3. Biosorption isotherm of Ni2þand Cu2þ ions 2.4. Continuous system e fixed bed-column

Batch sorption experiments were carried out to obtain the Continuous system experiments were carried out in a jacketed
mono-component equilibrium data. A series of solutions (75 mL) stainless steel column with an internal diameter of 2.8 cm and
with different initial metal concentrations (0e7 mmol L1) were height of 50 cm. Bed height was fixed at 30.6 cm for all
60 C.E.R. Barquilha et al. / Journal of Cleaner Production 150 (2017) 58e64
experiments. Feed metal solution had its pH adjusted at 5.0 with
sulfuric acid and it was fed into the bottom of the column by a
peristaltic pump (Cole-Parmer 6e600 rpm), with a constant flow
rate of 6 mL min1 and initial concentration of
0.775e0.903 mmol L1 (equivalent to 50 mg L1 of copper or
nickel). The column was kept at constant temperature of 30
C
through of an ultra-thermostatic water bath.
Biosorption capacity of the metal ion was calculated from the
breakthrough curve obtained experimentally, according to Equa-
tion (4) (Da Silva et al., 2002):
Zt
C0 Q
q¼ ð1  C=C0 Þdt
1000 ms
0
where:
q ¼ biosorption capacity (mmol g 1 );
C ¼ metal ion concentration at the column outlet (mmol L1 );
C0 ¼ initial metal ion concentration at the column inlet
(mmol L1 );
Q ¼ flow rate (cm3 min1 );
t ¼ time (min);
ms ¼ biosorbent dry weight (g).
2.5. Determination of bed porosity
Bed porosity was determined at the end of each experiment. The
column containing nickel or copper solution was drained by letting
the solution flow away during 24 h. After that, a peristaltic pump
(6e600 rpm) fed the column with a known volume of distilled
water so that necessary volume to fill the column (VV ) was deter-
mined by the difference between the initially contained volume
and the remaining volume (Cossich et al., 2004).
Porosity was calculated by means of Equation (5):
VV
εb ¼
Vb
where Vb is the bed volume.
2.6. Modeling of the breakthrough curves
Thomas model is widely used to adjust adsorption in fixed-bed
column, it takes into consideration that the adsorption rate as-
sumes the Langmuir kinetics in adsorption-desorption process. The
dynamic behavior in fixed bed column can then be represented by
equations (Thomas, 1944):
vC rL vq vC
þ þ u0 ¼0
vt εL vt vz
vq
¼ ka ðqmax  qÞC  kd q
vt
where ka is the adsorption kinetic constant (L mmol1 min1 ); kd is
the desorption kinetic constant (min1 ); qmax is the maximum
sorption capacity of the biosorbent (mmol g 1 ); q is the adsorbate
concentration in the solid phase (mmol g 1 ); C is the adsorbate
concentration in the solution (mmol L1 ); u0 is the interstitial ve-
locity (cm min1 ); rL bed density (g L1 ); and ε is bed porosity.
The first term in Equation (6) represents the adsorption rate,
which is proportional to the amount of available sites in the bio-
sorbent and the ions concentration in the fluid phase; the second
term constitutes the desorption rate, which is represented by a
first-order reaction in relation to amount of adsorbed ion (Chu,
2010).
Equations (8) and (9) give the initial and boundary conditions
employed in the resolution of Thomas model:
Cð0; zÞ ¼ 0 e qð0; zÞ ¼ 0 (8)

0 t¼0
Cðt; 0Þ ¼ (9)
C0 t > 0
Values of the parameters ka and kd of Equation (6) have been
estimated from the experimental breakthrough curve. These pa-
(4)
rameters are obtained by means of an objective function minimi-
zation (Fobj ), represented by Equation (9), through downhill
simplex optimization method (Da Silva et al., 2002):
n 
X 2 
Fobj ¼ EXP
Cout MOD
 Cout (10)
i¼1
where:
n ¼ number of samples;
EXP ¼ metal ion experimental concentration at the column
COUT
outlet (mmol L1 );
MOD ¼ metal ion fitted initial concentration at the column inlet
COUT
(mmol L1 );
3. Results and discussions
3.1. Biomass immobilization
The optimized structure made possible to obtain spherical beads
with an average diameter of 2.5 mm, given that the alginate beads
without biomass presented 95.99% of average moisture, beads with
0.25% (w=v) biomass get 95.52% moisture and beads with 0.50%
(w=v) biomass get 94,83% moisture. The production capacity of
beads was about 250 mL of alginate solution (with and without
(5)
biomass) per hour.
3.2. Equilibrium data
Fig. 2 shows equilibrium experimental data, as well as Langmuir
and Freundlich models fitted to them. The obtained isotherms were
favorable type, considering that they represent processes where
large amounts of metals can be biosorbed in very dilute concen-
trations. The parameters of Langmuir (b and Qmax ) and Freundlich
models (KF and n), as well as their coefficients of correlation R2, are
shown in Tables 1 and 2.
Although the Ca-alginate beads has presented lager uptake ca-
pacity than others biosorbents, at low metal concentrations the
(6)
results were very similar. In nickel biosorption, the coefficient b of
Langmuir model was smaller for Ca-alginate. This coefficient is
related to affinity biosorbent-biosorbate, suggesting that the Ca2þ
(7) ions can compete with metal ions, especially with Ni2þ ions that
presents lower affinity than Cu2þ ions.
For high metal concentrations, the biosorption capacity in-
creases as the calcium alginate concentration also increases, ac-
cording to qmax parameters, since the alginate has large amount of
carboxyl functional groups and the calcium ions act as ionic ex-
changers (Fourest and Volesky, 1996; Chen et al., 2002).
Biosorption capacity of Sargassum sp. immobilized biomass has
presented values between the calcium alginate beads and the free
Sargassum sp. biomass, for both ions. Since the functional groups
present in the alginate of brown algae are the main groups involved
 C.E.R. Barquilha et al. / Journal of Cleaner Production 150 (2017) 58e64 61

(a) (b)

(c) (d)

Fig. 2. Biosorption isotherms of Ni2þ and Cu2þ ions by: (a) free Sargassum sp. biomass; (b) Sargassum sp. biomass immobilized in Ca-alginate (0.50% w=v); (c) Sargassum sp. biomass
immobilized in Ca-alginate (0.25% w=v); (d) calcium alginate beads.

Table 1
Parameters of isotherm models fitted to Ni2þ ions biosorption.

Model Parameter Calcium Alginate Immobilized Biomass 0.25% Immobilized Biomass 0.50% Free Biomass

Langmuir Qmax (mmol/g) 1.221 1.128 1.054 0.913

b (L/mmol) 0.981 1.179 1.118 1.624
R2 0.976 0.991 0.991 0.979
Freundlich KF (L/mmol)1/n (mmol/g) 0.595 0.589 0.542 0.542
n 2.819 3.075 3.021 3.613
R2 0.988 0.986 0.974 0.960

Table 2
Parameters of isotherm models fitted to Cu2þions biosorption.

Model Parameter Calcium alginate Immobilized Biomass 0.25% Immobilized Biomass 0.50% Free Biomass

Langmuir Qmax (mmol/g) 1.863 1.909 1.780 1.483

b (L/mmol) 6.078 3.226 4.871 4.331
R2 0.992 0.993 0.992 0.995
Freundlich KF (L/mmol)1/n (mmol/g) 1.420 1.294 1.299 1.052
n 3.857 3.048 3.636 3.815
R2 0.954 0.975 0.954 0.930

in adsorption/ionic exchange of metal ions, the higher alginate
content will correspond to greater uptake capacity by the bio-
sorbent (Kratochvil and Volesky, 1998; Davis et al., 2003).
According to Aryal and Liakopoulou-Kyriakides (2014), the
Langmuir model explains the monolayer sorption, while Freundlich
models explains multilayer sorption and these models can not be
applied simultaneously. Correlation coefficients values indicate
that the Langmuir model fitted better to the experimental results,
whereas Freundlich model is an empirical equation that does not
predict any biosorbent saturation, and has only well-adjusted low
concentrations (Volesky, 2004).
Table 3 shows the maximum uptake capacity (qmax ) of nickel
and copper ions obtained in other works involving calcium alginate
and Sargassum sp., as well as those obtained in this current work.
3.3. Biosorption in fixed-bed column
The immobilized biomass used for the experiments in fixed-bed
column was the one that presented Sargassum sp. content of 0.50%
(w=v), since it contained the largest amount of unprocessed
biomass, presented equivalent behavior to the Ca-alginate beads in
terms of biosorption capacity at low metal concentrations and
allowed formation of beads with higher density, increasing the
operation time of the column.
62 C.E.R. Barquilha et al. / Journal of Cleaner Production 150 (2017) 58e64

Table 3
Comparison of the maximum uptake with other authors.

Metal Biomass pH T (
C) qmax ðmmol g1 Þ Reference

Nickel Sargassum sp. 5.0 30 0.913 The current work

Ca-alginate 5.0 30 1.221 The current work
Sargassum sp. 5.5 22 0.61 Sheng et al., 2004.
S. filipendula 4.0 30 0.857 Seolatto, 2005.
S. wightii 4.0 30 1.383 Vijayaraghavan et al., 2006.
Ca-alginate 4.5 20 0.71e1.21 Kleinübing, 2009.
Copper Sargassum sp. 5.0 30 1.483 The current work
Ca-alginate 5.0 30 1.863 The current work
Sargassum sp. 5.0 25 1.21 Liu et al., 2011.
Sargassum sp. 5.0 22 0.99 Sheng et al., 2004.
S. filipendula 4.5 20 1.324 Kleinübing, 2009.
Ca-alginate 4.5 20 1.13e1.25 Kleinübing, 2009.
Ca-alginate 3.6 20 1.684 Jang et al., 1995.

Table 4
Operational conditions and dynamic absorption capacity of Ni2þ and Cu2þ.

Biosorbent Metal ions Average feed concentration (mmol/L) ms (g) rL (g/L) εL q*Ni (exp.) (mmol/g)

Free Sargassum sp. Nickel 0.876 8.21 43.55 0.902 1.234

Copper 0.775 8.31 44.12 0.904 1.515
Immobilized Sargassum sp. Nickel 0.903 6.06 32.15 0.105 1.689
Copper 0.781 5.84 30.95 0.260 2.057

Table 4 exhibits the operational conditions of the column and
the capacity of nickel and copper ions removal. Due to the bed
porosity and the uptake capacity achieved by immobilized
Sargassum sp., it is believed that fixed-bed column biosorption was
not affected by the high bed packing, leading to results larger than
those predicted by Langmuir isotherm and these obtained by free
biomass, and indicating a good distribution of immobilized biomass
in the bed.
Some mathematical models utilize the uptake capacity of the
metal species defined by the equilibrium relation between the
phases, which, in this case, is represented by the Langmuir
isotherm obtained in batch system. However, the equilibrium
established in continuous system is different, leading to differences
in biosorption capacity. According to Da Silva et al. (2002), this
difference on values can be justified because at closed system
(batch-mode) the ions released by the biosorbent remain in the
solution, whereas the equilibrium condition in the column is
characterized by the absence of these ions released by the bio-
sorbent, which are carried by the feed solution. Henriques et al.
(2011) and Shahbazi et al. (2013) also observed this behavior.
Although only alginate was processed with calcium ions,
seaweed biomass is also often associated with light metals, such as
Naþ, Kþ, Mg2þ and Ca2þ, present in marine environments (Davis
et al., 2003; Pozdniakova et al., 2016).
In order to simulate the breakthrough curve, Thomas model
(1944) was used. Despite being a simple model, it is still widely
used for breakthrough curve modeling and, in this case, it repre-
sented very well the breakthrough curve for both metal ions, as
shown in Figs. 3 and 4.
Breakthrough curves of free and immobilized biomass experi-
mentally obtained are similar in shape, both for nickel and copper
biosorption. Yet, it should be pointed out that, in order to use the
same bed height, it was necessary a smaller amount of immobilized
biomass, in terms of dry weight, as shown in Table 4.

Fig. 3. Experimental data and Thomas model simulation of breakthrough curves for Fig. 4. Experimental data and Thomas model simulation of breakthrough curves for
the biosorption of Ni2þ ions by free and immobilized Sargassum sp. biomass. the biosorption of Cu2þ ions by free and immobilized Sargassum sp.
 C.E.R. Barquilha et al. / Journal of Cleaner Production 150 (2017) 58e64 63

Table 5
Thomas model parameters and q*Ni values for dynamic biosorption of Ni2þ ions.

Biosorbent ka x 103 (L mmol1 min1) kd x 105 (min1) q*Ni (Exp.) (mmol/g) qmax (Mod.) (mmol/g) Deviationa (%) R2

Free Sargassum sp. 1.503 2.831 1.234 1.124 8.90 0.990

Immobilized Sargassum sp. 1.906 13.608 1.689 1.676 0.76 0.997
 
 
a
Deviation 100 q*exp  q*mod =q*exp .

Table 6
Thomas model parameters and q*Cu values for dynamic biosorption of Cu2þ ions.

Biosorbent ka x 103 (L mmol1 min1) kd x 105 (min1) q*Cu (Exp.) (mmol/g) qmax (Mod.) (mmol/g) Deviationa (%) R2

Free Sargassum sp. 1.460 4.530 1.515 1.516 0.00 0.998

Immobilized Sargassum sp. 1.910 1.790 2.057 2.061 0.16 0.999
 
a  * *  *
Deviation 100 qexp  qmod =qexp .

Though similar, the breakthrough curves for immobilized References

biomass revealed a slightly longer operational time, which can be
attributed to a better distribution of the immobilized biomass in
the column, in this way producing a bed with low porosity that may
have favored the contact between the phases. According to Volesky
(2003) the shape and slope of the breakthrough curve is result of
the equilibrium sorption relationship, the mass transfer to and
throughout the sorbent in the column, and operation parameters.
Tables 5 and 6 show Thomas model parameters, as well as the
biosorption capacities calculated by means of the model
(qmax (Mod.)) and experimental (q* (Exp.)) breakthrough curve of
nickel and copper ions, respectively.
The results of fixed-bed column experiments demonstrated that
the immobilized biosorbent exhibited a greater uptake capacity,
with 49% increase for nickel biosorption and 36% increase for
copper biosorption when compared with the biosorption capacities
of free biomass.
4. Conclusion
The immobilized Sargassum sp. in Ca-alginate beads showed to
be an excellent biosorbent for treatment of nickel and copper in
aqueous solutions. In general, this biosorbent presented better
biosorption performance than the free algae, except for low con-
centrations in batch system due to calcium ions present, confirming
the important role of alginate in the biosorption process involving
brown algae. Biosorption equilibrium data were well represented
by the Langmuir model obtaining favorable type isotherms, and the
results indicate higher affinity and biosorption capacity for copper
ions than for nickel ions. Biosorption in continuous system pre-
sented a different equilibrium condition, since biosorbents
exhibited higher biosorption capacities than those predicted by
Langmuir model in batch. In fixed-bed columns, the free Sargassum
sp. achieved an uptake of 1.23 mmol of Ni2þ g1 and 1.51 mmol of
Cu2þ g1, whereas the immobilized biosorbent reached a removal
of 1.69 mmol of Ni2þ g1 and 2.06 mmol of Cu2þ g1. Although the
bed has had low porosity, the high metal uptake of the immobilized
biosorbent indicated good bed distribution, usually desired using in
nature or particulate biomass. The immobilized biosorbent also
facilitated the bed packing due to its regular spherical shape.
Therefore, the immobilization has proved to be a good alternative
for the biosorption process in fixed-bed column, mainly to scale-up.
Acknowledgements
~o de Aperfeiçoamento de
The authors acknowledge Coordenaça
Pessoal de Nível Superior(CAPES) and Conselho Nacional de
Desenvolvimento Científico e Tecnolo
gico(CNPq) for financial
support.
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