Accepted Manuscript

Title: Synthesis and characterization of modified carrageenan

microparticles for the removal of pharmaceuticals from
aqueous solutions

Author: Stavroula G. Nanaki George Z. Kyzas Areti Tzereme

M. Papageorgiou Margaritis Kostoglou Dimitrios N. Bikiaris
Dimitra A. Lambropoulou

PII: S0927-7765(15)00071-5
DOI: http://dx.doi.org/doi:10.1016/j.colsurfb.2015.01.053
Reference: COLSUB 6886

To appear in: Colloids and Surfaces B: Biointerfaces

Received date: 3-10-2014

Revised date: 19-1-2015
Accepted date: 29-1-2015

Please cite this article as: S.G. Nanaki, G.Z. Kyzas, A. Tzereme, M.
Papageorgiou, M. Kostoglou, D.N. Bikiaris, D.A. Lambropoulou, Synthesis and
characterization of modified carrageenan microparticles for the removal of
pharmaceuticals from aqueous solutions, Colloids and Surfaces B: Biointerfaces (2015),
http://dx.doi.org/10.1016/j.colsurfb.2015.01.053

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Highlights

 Synthesis and characterization of modified carrageenan microparticles

 Bisorption and removal of metoprolol from aqueous media
Detailed adsorbent characterization and adsorption studies
Maximum adsorption capacity ~ 109 mg/g

t
ip
cr
us
an
M
d
p te
ce
Ac

Page 1 of 36
 Synthesis and characterization of modified carrageenan
microparticles for the removal of pharmaceuticals from
aqueous solutions

t
ip
cr
Stavroula G. Nanakia, George Z. Kyzasa,b, Areti Tzeremec, M. Papageorgiouc,
Margaritis Kostogloub, Dimitrios N. Bikiarisa, Dimitra A. Lambropoulouc,

us
an
a
Laboratory of Polymer Chemistry and Technology, Department of Chemistry, Aristotle
University of Thessaloniki, GR-541 24 Thessaloniki, Greece
b
Laboratory of General and Inorganic Chemical Technology, Department of Chemistry,
M
Aristotle University of Thessaloniki, GR-541 24 Thessaloniki, Greece
c
Laboratory of Environmental Pollution Control, Department of Chemistry, Aristotle
University of Thessaloniki, GR–541 24 Thessaloniki, Greece
d
p te
ce
Ac

Author to whom correspondence should be addressed; E-Mail: dlambro@chem.auth.gr; Tel.:

+30 2310 997687; Fax: +30 2310 997799.

2
Page 2 of 36
ABSTRACT

In the present study, carrageenan microparticles were synthesized using spray-drying

method and used as biosorbents for the removal of pharmaceutical compounds. The cross-

linking reaction of iota-carrageenan (iCAR) and kappa-carrageenan (kCAR) with

t
glutaraldehyde (GLA) at different concentrations (2.5% or 5% w/w, mass of GLA per mass of

ip
CAR) was studied (iCAR/GLA2.5, iCAR /GLA5, kCAR/GLA2.5, kCAR/GLA5). The

cr
physicochemical properties of the novel cross-linked polymers were investigated by scanning

electron microscopy (SEM), X-ray diffraction (XRD) and Fourier transform infrared

us
spectroscopy (FT-IR). Swelling studies were in accordance with the polymer properties,

an
showing the lowest swelling degree (19%) by using the iCAR/GLA5 microparticles. The

optimal kCAR/GLA5 microparticles were successfully employed for the removal of

M
Metoprolol (MTPL) from aqueous samples. The adsorption capacity of the adsorbents was

investigated using a batch adsorption procedure and the kinetics and thermodynamics of the
d

adsorption process were further investigated. It was found that the adsorption isotherms agree
te

well with the Langmuir-Freundlich model. The maximum adsorption capacity (Qm) was

achieved in pH 6, whereas an increase of Qm was observed increasing the temperature (from

p

109 at 20 °C to 178 mg/g at 40 °C). Kinetic studies showed that the adsorption process on
ce

iCAR/GLA5 microparticles followed pseudo-second-order rate mechanism. Finally, a new

phenomenological model of the adsorption process was proposed in order to extract

Ac

information on the relevant sub-processes.

Keywords: Adsorption; β-blockers; Carrageenan; Kinetic modeling; Metoprolol;

Pharmaceuticals

Page 3 of 36
1. Introduction

The presence of pharmaceuticals and their transformation products in aquatic

environment has received considerable attention due to its environmental and health hazards

[1,2]. Many of these compounds are not completely removed by wastewater treatment plants

t
(WWTPs) and municipal effluents as well as effluents from hospitals and pharmaceutical

ip
manufacturing facilities have been identified as important sources. Consequently, a vast

cr
number of these compounds have been detected in WWTP effluents, surface waters and, less

frequently, in ground and drinking water all over the world [3-6].

us
To reduce the potential risk caused by pharmaceutical compounds in treated

an
wastewater discharged to aquatic environment, their removal in WWTPs is considered a big

technological challenge. Among all the existing treatments, adsorption is one of the most
M
promising techniques for pollutant removal, due to its convenience once applied into current

water treatment processes. The most updated literature screening gives a huge number of
d

papers published for adsorption of various pollutants onto different materials as chitosans,
te

graphenes, clays, activated carbons, zeolites, agricultural-based materials (or wastes) [7-11].

However, a few number of works have been done about the use of carrageenan as adsorbent
p

materials and among them, the majority refers to dyes or metals/ions removal [12-20].
ce

Carrageenans are hydrophilic polymers obtained by extraction of Rhodophyceae red

seaweeds. They are composed of D-galactose residues linked alternately in 3-linked-β-D-

Ac

galactopyranose and 4-linked-α-D-galactopyranose units and they are classified according to

the degree of the substitution that occurs on their free hydroxyl groups. Various degrees of

sulfation (between 15% and 40%) identified by a Greek prefix. Iota-carrageenan (iCAR) is

approximately 32% substituted with ester sulfate groups, is soluble in hot water and forms

solutions with thixotropic characteristics. Kappa-carrageenan (kCAR) has the same properties

Page 4 of 36
(solubility in hot water), but the percentage of substitution with ester sulfate groups is 25%

[21].

Due to non-toxicity, biodegradability, and biocompatibility of carrageenan

biopolymers there are considerable attentions to provide new carrageenan-based materials.

t
Thus, in this report two carrageenans with different degrees of sulfation, iCAR (mono-sulfate)

ip
and kCAR (di-sulfate)) were submitted to cross-linking process in order to prepare materials

cr
with distinct properties for adsorption of pharmaceutical molecules. To the best of our

knowledge, there are no reports available in the literature on carrageenan polymers for

us
pharmaceutical removal.

an
Metoprolol (1-(Isopropylamino)-3-[4-(2-methoxyethyl)phenoxy]propan-2-ol) (MTPL)

(Fig. SI1, Supporting information section), one of the most widely used β-blocker drugs, was
M
chosen as the model absorbate. It is highly resistant to hydrolysis, bioavailable and mobile in

the environment [27] and it has been considered as one of the most frequently detected β-
d

blockers in surface waters (concentrations up to 2200 ng/L) [22-25]. It has been also found in
te

hospital and municipal influents and effluents in concentrations up to μg/L, at various

locations in Europe and USA [26]. Recent investigations [27,28] demonstrated that according
p

to the chemical substance classification of the European Union Directive 93/67EEC, MTPL
ce

can be considered to be harmful (10 < EC50< 100 mg/L) to aquatic organisms (based on

toxicological data from the green alga test (S. vacuolatus). Hence, to avoid its potential
Ac

adverse effects on the environment, research efforts are necessary to develop efficient

techniques for its removal.

In this context, novel cross-linked carrageenan polymers were prepared, characterized

and investigated as biosorbents for MTPL removal. The swelling equilibrium as well as the

swelling kinetics was extensively investigated. The adsorption kinetic was examined using the

pseudo-first order and pseudo-second order equations and the equilibrium data were fitted to

2
Page 5 of 36
three isotherm equations. Finally, a phenomenological model of the adsorption process was

proposed to fit the kinetic data and extract information on the relevant sub-processes.

2. Materials and Methods

t
2.1. Materials

ip
Iota-carrageenan (Gelcarin GP-379NF) and kappa-carrageenan (Gelcarin GP-812NF)

cr
were kindly supplied by FMCBioPolymer (Netherlands). Glutaraldehyde (aqueous solution of

25%wt) was purchased from Aldrich. Metoprolol L-tartrate (purum 99.7%) was supplied by

us
Sigma-Aldrich. Filtration membranes were purchased by Schleicher-Schuell MicroScience.

an
All other materials and solvents used for the analytical methods were of analytical grade.
M
2.2. Preparation of carrageenan/glutaraldehyde microparticles (CAR/GLA)

Carrageenan microparticles (kappa or iota) were prepared after cross-linking with

d

GLA in aqueous medium. In brief, carrageenan was initially dissolved in distilled water at 80
te

°C under mechanical stirring forming solutions of 1% w/v [32]. The adequate quantity of
p

GLA was added in the solution at final concentration of 2.5 and 5.0% wt. The solution was
ce

stirred under magnetic stirrer for 15 min at 60 °C and spray-dried. The microparticles

obtained cured in oven at 110 °C for 45 min. Then, they were collected and sequentially
Ac

washed with deionized water and absolute ethanol several times. Finally, the prepared

materials were dried at room temperature.

2.3. Characterization techniques

X-Ray diffraction (XRD) analysis was performed on carrageenan microparticles,

scanned over the internal range of 5-55° (Rigaku MiniFlex 600 diffractometer with Bragg-

Brentano geometry (θ, 2θ) and a Ni-filtered CuKa radiation.

3
Page 6 of 36
 For Fourier Transform Infrared Spectroscopy (FTIR) measurements, 5 mg of

microparticles were mixed with 180 mg of KBr in agate mortar. The mixture was pressed

under 5 tons for 2 min and pellet was formed. The pellet was then placed into an attachment

in the optical compartment and FT-IR spectra were obtained using a Perkin-Elmer FT-IR

t
spectrometer (model FTIR-2000, Perkin Elmer, Dresden, Germany). Infrared (IR) absorbance

ip
spectra were obtained between 450 and 4000 cm-1 at a resolution of 4 cm-1 using 20 co-added

cr
scans. All spectra presented are baseline corrected, normalized and converted to the

absorbance mode.

us
In general, if any adsorbent material presents high swelling percentage (SP, %)), it is

an
very difficult to be used in columns due to the inevitable fouling. For this reason, swelling

experiments are needed to examine the behavior of biosorbents for future possible application
M
in industrial columns. For swelling studies, 3 g of the prepared materials were allowed to

swell in deionized water for 24 h. The pH (pH = 6) was fixed with micro-additions of acid or
d

alkali (0.01 M HCl or 0.01 M NaOH). After 24 h, the solid swollen particles were collected
te

and weighed. The swelling percentage (SP, %) was calculated (Eq. (1)), where msw (g) is the

mass of the swollen particles after 24 h, and m0 (g) is the initial mass of the particles before
p

swelling.
ce

 m  m0 
SP =  sw  100% (1)
 m0 
Ac

2.4. Spray drying process

For spray drying process a mini spray-dryer was used (model B-290, BUCHI Corporation,

New Castle, USA). Air was used as spray-drying agent. Peristaltic pump and aspirator were

set at 100%, the spray flow rate was set at 40 mm height and the inlet temperature at 180 °C.

The above settings resulted in 100 °C outlet temperature.

4
Page 7 of 36
2.5. HPLC analysis

Quantitative analysis was performed using a Shimadzu HPLC prominence system

(Kyoto, Japan) consisting of a degasser (DGU-20A5), a liquid chromatograph (LC-20 AD),

t
an auto sampler (SIL-20AC), a UV/Vis detector (SPD-20A) and a column oven (CTO-20AC).

ip
A C18 column (120 Å, 250×4.6 mm, 5 μm, CNW Athena) was used and the temperature was

cr
set at 40 °C. Water and methanol were the elution solvents. The samples were eluted

according to the following gradient: 10% methanol as initial condition; 50% methanol for 10

us
min; 80% methanol for 2 min, followed by 3 min 90% in methanol equilibration time, the

an
total run time was 16 min and the flow rate 1 mL/min. Chromatographic data were acquired at

the wavelength of 223 nm.

M
2.6. Adsorption experimental procedure
d

Batch experiments (all experiments were run in triplicate and the respective figures
te

present the experimental points with errors bars calculated after standard deviation (n = 3))

were carried out using 1 g/L of adsorbent (m = 0.01 g of adsorbent’s mass were added to V =
p

10 mL of deionized water in a conical flask). At different time intervals, samples were filtered
ce

by use of membrane filter with a pore size of 0.50 μm. For the pH-effect experiments (C0 = 40

mg/L), the solution pH was initially adjusted with aqueous solutions of acid or base (0.01
Ac

mol/L of HCl and/or 0.01 mol/L NaOH) to reach pH values in the range of 2-12. The agitation

rate was fixed at 160 rpm for all adsorption-desorption tests using shaking incubator (Julabo

SW-21C, Seelbach, Germany) under a controlled temperature. Adsorption isotherms were

obtained by varying initial concentration of target pollutant (C0 = 0-100 mg/L) at three

different temperatures (T = 20, 30, 40 °C) for 24 h (contact time). Kinetic tests were

performed using C0 = 40 mg/L (dissolved MTPL in aqueous solution) at 20 °C (at pH = 6

5
Page 8 of 36
given that it was found to be the optimum value according to pH-effect tests) for different

contact-time intervals during adsorption (t = 0-24 h).

The experimental kinetic data were fitted to pseudo-first [33] (Eq. (2)),-second order [34] (Eq.

(3)) (their selection is based on the fact that they are the two most widely-used kinetic models

t
in adsorption works [34,35]) and intraparticle diffusion model [36,37] :

ip
(2)
C t = C 0  (C 0  C e ) 1  e  k1t 

cr
 1 
Ct = C0  (C 0  Ce ) 1   (3)

us
 1  k2t 

Q t = k D t1/2 (4)

an
where k1, k2 (min-1) are the rate constants for the pseudo-first and -second order kinetic

equations; C0, Ct, Ce (mg/L) are the initial, transient and equilibrium concentrations of MTPL
M
in the aqueous solution, respectively; Qt (mg/g) is the transient adsorption capacity (amount

adsorbed at time t); kD (min-1/2) is the rate constant for the intraparticle diffusion model given
d

by Webber and Morris [37].

te

The equilibrium amount in the solid phase (Qe, mg/g) was calculated according to the
p

following equation where C0 and Ce (mg/L) are the initial and equilibrium concentrations of
ce

MTPL, respectively; V (L) is the volume of aqueous solution; m (g) is the mass of particles

used):
Ac

Qe =
 C0  Ce  V
(5)
m

The experimental equilibrium data were fitted to the Langmuir (Eq. (6)) [38],

Freundlich (Eq. (7)) [39] and Langmuir-Freundlich (L-F) (Eq. (8)) [40] isotherm equations

expressed by the following equations:

Q m K L Ce
Qe = (6)
1+K L Ce

6
Page 9 of 36
Q e = K F C e1/n (7)

Q m K LF  Ce 
1/b

Qe = (8)
1+K LF  Ce 
1/b

where Qm (mg/g) is the maximum amount of adsorption; KL (L/mg) is the Langmuir

t
adsorption equilibrium constant; KF (mg1-1/n L1/n/g) is the Freundlich constant representing the

ip
adsorption capacity; n (dimensionless) is the constant depicting the adsorption intensity; KLF

cr
[(L/mg)1/b] is the L-F constant; b (dimensionless) is the L-F heterogeneity constant.

us
Three main parameters have been calculated (the change of Gibbs free energy (ΔG0,

kJ/mol), enthalpy (ΔH0, kJ/mol) and entropy (ΔS0, kJ/mol K)) based on the isotherms resulted

an
at 20, 30, and 40 °C. The system of equations below can be used for the calculation of the

aforementioned thermodynamic parameters (where Cs (mg/L) is the amount adsorbed on a

M
solid at equilibrium and R (8.314 J/molK) is the universal gas constant) [41]:

Cs
Kc = (9)
Ce
d
te

ΔG 0 =  RTln  K c  (10)

ΔG0 = ΔH0  T ΔS0 (11)

p
ce

 ΔH0  1 ΔS0
ln  Kc  =   
 R  T R (12)
 
Ac

ΔG0 was given from Eq. (10), while ΔH0 and ΔS0 were given from the slop and intercept of

the chart between ln(Kc) versus 1/T (Eq. (12)).

3. Results and Discussion

3.1. Swelling studies of all prepared carrageenan derivatives

7
Page 10 of 36
 To examine which carrageenan product presents the best (hypothetically) adsorption

properties, a detailed swelling study was performed before. The equation of the motion of a

network element during the swelling is the following (Eq. (13)) [42]:

u  K   / 3   u
 D02u    (13)
t f

t
ip
where u is the displacement vector measured from the final equilibrium location after the gel

cr
is fully swollen u = 0 at t = ∞; D0 is the collective diffusion coefficient; t denotes the time; K

is the bulk modulus.

us
Eq. (13) has been used with some success to study the swelling of gels [43]. The above

equation is fundamental in swelling theory, but in the case of particles and not gels (or

an
hydrogels) some hypotheses should be done and the study must be approached from a

different point of view.

M
Investigations of swelling in carrageenan-based adsorbents, to provide a detailed

picture of this process, are still too scarce in the literature. Until recently, research on
d

carrageenans has been limited to swelling studies focused on control release (drug) and there
te

is a lack of data for systematic swelling experiments [44-48]. Furthermore, the majority of
p

research in this field is dedicated to the kCAR and almost nothing is known for iCAR.
ce

The swelling experiments were carried out immersing the carrageenan particles into

deionized water, because this was the medium of performing all adsorption experiments of
Ac

this study. Fig. 1 represents the results of swelling experiments. At first, it is obvious that SP

is different for each carrageenan material.

The samples without cross-linking (iCAR and kCAR) presented the highest swelling

degrees (75% and 88%, respectively). Their SP difference was due to their chemical structure

(Fig. SI2, Supporting information section); kCAR has one more hydroxyl group in its chain,

which increases the whole hydrophilicity of material. On the contrary, iCAR has ester sulfate

group in the position of that hydroxyl group. Furthermore, the same swelling testes were done

8
Page 11 of 36
for samples with 2.5% and 5.0 % wt cross-linking ratio. The SPs were higher for the materials

of 2.5% (iCAR/GLA2.5, 52%; kCAR/GLA2.5, 58%) than those of 5.0% (iCAR/GLA5, 30%;

kCAR/GLA5, 38%). According to all above results, the microparticles with the smallest SP

were those of iota-carrageenan cross-linked with 5.0% wt GLA (iCAR/GLA5). Therefore,

t
this material has the most promising potential in order to apply as adsorbent; so it was

ip
selected to study its properties running a series of adsorption experiments with MTPL.

cr
The swelling kinetic behavior of the micorparticles was also studied. Fig. 1 also

represents the kinetic trend of swelling during immersion. The kinetic curves were found to be

us
similar for the three sets of materials studied (pure carrageenans, cross-linked with 2.5% wt

an
GLA, and cross-linked with 5% wt GLA). This is normal because the material nature is

approximately the same. In the case of non-cross-linked samples (iCAR and kCAR), the water
M
molecules were rapidly immersed in the material’s network in the first 5 mins. iCAR

increased its weight about 15%, while the respective increase for kCAR was 18%. The same
d

intense SP increase was also observed for all materials (iCAR, 65%; iCAR/GLA2.5, 40%;
te

iCAR/GLA5, 19%; kCAR, 82%; kCAR/GLA2.5, 55%; kCAR/GLA5, 25%) until 65 min

(zone 1). After that period, the motion of water molecules became more difficult and the SP
p

continues to increase but in more gradual way. The end of this second time-region is different
ce

for each material and it depends on the chemical structure of each sample. This time-zone was

lasted until 240 mins of immersion (iCAR, 75%; kCAR, 88%), while for the 5% wt cross-
Ac

linked materials until 300 min (zone 2). This difference was due to the cross-linking of GLA

which formed an extra network inside the chain inhibiting the free entrance and motion of

water molecules into it.

3.2. Characterization of iCAR/GLA5

9
Page 12 of 36
 As explained above, the most suitable derivative for carrying out the drug adsorption

experiments was found to be iCAR/GLA5. Therefore, the full characterization of this material

will be presented. In general, iCAR is a linear polymer of about 25,000 galactose derivative

with regular but imprecise structure, depending on the source and extraction conditions. It was

t
previously found that iCAR corresponds to the amorphous state [32]. XRD patterns of spray-

ip
dried iCAR (Fig. 2) showed that the polymer was also amorphous, i.e. spray-dryer didn’t

cr
affect its crystallinity and so did the addition of GLA. MTPL is a white crystalline powder

used as beta-blocker. Its XRD pattern is shown in Fig. 2. As seen, MTPL has its main peaks at

us
19.45° and 23.2° having other smaller peaks at 10.65°, 15.91°, 20.42° and 24.07°. After

an
adsorption, a wide peak was recorded in XRD pattern. This most probably corresponds to

amorphous MTPL. It is known that amorphization is attributed to strong interactions taking

M
place between the drug and the polymer carrier [49].

SEM was used to examine the morphology of the prepared microparticles.

d

Microparticles were found to be smooth on the surface and spherical in scrape. iCAR particles
te

were mainly 20-25 μm in size (Fig. 3a), but having other smaller particles and some

aggregates. The size of iCAR/GLA5 microparticles were smaller (i.e. 15-20 μm) than iCAR
p

and had more aggregates (Fig. 3b). The smaller size may be attributed to cross-linking of
ce

iCAR with GLA. This observation is in accordance with Kahtani et al., who used GLA as

cross-linker to hydroxyethyl cellulose grafted acrylamide [50]. It was found that increasing
Ac

the GLA content, the size of microparticles prepared by emulsion cross-linking method, was

reduced through hydrogen bond formed between the atom of oxygen of GLA and hydroxyl

groups of the polymer. This explanation is also possible in our study, due to the fact that GLA

was also used as cross-linking agent without the use of initiator, i.e. oxygen atom of GLA

probably form hydrogen bonds with hydroxyl groups of iCAR and retain its chains closer to

its other. In order to enhance this hypothesis FTIR spectroscopy was used.

10
Page 13 of 36
3.3. Adsorption interactions and mechanism/ FTIR explanations

To examine the interactions between MTPL and iCAR/GLA5, FTIR spectra were

taken before and after adsorption. At first, FTIR evaluation was conducted for the prepared

t
carrageenan materials (iCAR and iCAR/GLA5). Fig. 4 presents the characteristic peaks of

ip
iCAR; a broad peak at 3600 – 3200 cm-1 owning to O–H interactions, 1645cm-1 (carbonyl

cr
group stretching), 1260 cm-1 (O=S=O asymmetric stretching), 1159 cm-1 (C–O–C asymmetric

stretching), 1072 cm-1 (S–O symmetric stretching), 1028.6 and 1040.7 cm-1 (C–O and C–OH

us
stretching), 933.7 cm-1 (C–O–C stretching in 3,6-anhydrogalactose) [51] and 852 cm-1 (C–O–

an
S) stretching in a (1-3)-D-galactose [52]. By examining the wavenumbers of those peaks it

can be seen that their position was remaining almost the same in microparticles prepared by
M
spray-drying iCAR/GLA5, showing that there are no clear differences in –OH absorption

before and after cross-linking. However, in iCAR/GLA5 sample due to the cross-linking
d

reactions, a new peak is formed (recorded as shoulder) at 1718 cm-1, indicating that ester
te

bonds have been prepared after the reaction of iCAR –OH groups and GLA.

To examine the interactions between iCAR/GLA5 and MTPL, FTIR spectra of MTPL
p

were also measured. According to Fig. 4, MTPL showed a characteristic peak at 3451 cm-1
ce

owning to O–H stretching and another at 1634 cm-1 attributed to N–H vibrations. The peaks at

2552 and 2456 cm-1 ought to H-bonding forming by the complexation of MTPL molecules
Ac

[53] and ring stretching vibration are present at 1600 and 1512.6 cm-1. As observed in the

spectrum of iCAR/GLA5-MTPL, the peaks at 2552 and 2456 cm-1 are absent showing that no

intramolecular bonds of the drug exists. Also, chemical shifts are observed from 3451 cm-1 of

MTPL and 3452 cm-1 of iCAR/GLA5 to 3464 cm-1 indicating that hydrogen bonds between

polymer matrix and MTPL had occurred during adsorption studies (Fig. 5).

11
Page 14 of 36
3.4. Effect of pH on adsorption and isotherms

It is well known that the pH of the initial drug solution plays an important role in the

adsorption process, since it strongly influences the adsorption interactions, the type of bonds

between adsorbent and pollutants, etc. Hence, the effect of pH was carefully studied due to the

t
nature of adsorbent; carrageenan-type materials are mainly in gel-like, so a possible pH

ip
adjustment in extreme pH-zone may cause the dissolution of the material or the change of its

cr
structure.

Fig. 6a presents the effect of pH on MTPL removal. At low pH values (pH 2; strong

us
acidic conditions), the MTPL removal is near zero (2%). Increasing the pH from 2 to 4, the

an
respective removal also increased (to 32%). At pH 6, the removal was further enhanced

reaching 62%, but after this pH value, a decrease was observed (pH 8, 54%; pH 10, 50%; pH
M
12, 21%). This pH-behavior is due to the ionization of different functional groups of the

adsorbent (hydroxyl, sulfate) and pharmaceutical (amino, hydroxyl, carboxyl) over the pH
d

range. The adsorption interaction will be further discussed in the last section of this work.
te

On the other hand, the equilibrium data were fitted to three isotherm models.

However, the best correlation was observed for L-F equation (0.998 < RLF2 < 0.999; 0.929 <
p

RF2 < 0.997; 0.973 < RL2 < 0.982). Comparing the results and mainly the maximum theoretical
ce

adsorption capacities (Qm) of the models (Table SI1, Supporting information section), the

change (~57%) in Qm calculated for Langmuir and L-F models is clear (69 mg/g at 20 °C for
Ac

Langmuir and 109 mg/g for L-F). Fig. 6b illustrates the isotherms curves fitted to the three

aforementioned models. In order to select the best, an evaluation was performed comparing

Qm and Qe. The adsorption capacities in equilibrium (Qe) were measured 61, 66 and 76 mg/g

at 20, 30 and 40 °C, respectively. Although these values are near the Qm calculated with

Langmuir model, the trend of the experimental points seems to be further increasing.

Therefore, the L-F was concluded to be the optimum.

12
Page 15 of 36
 The effect of temperature on adsorption equilibrium was also observed. Increasing the

temperature from 20 to 30 °C, an increase (16%) of Qm (from 109 to 127 mg/g) was found.

The same was revealed increasing more the temperature from 30 to 40 °C, improving by 40%

(from 127 to 178 mg/g) the Qm.

t
A brief thermodynamic analysis was also performed based on the change of Gibbs free

ip
energy (ΔG0, kJ/mol), change of enthalpy (ΔH0, kJ/mol) and entropy change (ΔS0, kJ/mol K).

cr
These parameters (at pH = 6), at selected initial MTPL concentrations (10, 40, 70, 100 mg/L)

and all temperatures (20, 30, 40 °C), were given in Table SI2 (Supporting information

us
section). The negative values of ΔG0 showed the spontaneous adsorption of MTPL onto

iCAR/GLA5. The positive values of ΔH0 indicated the endothermic nature of the process.

an
These values were reduced with the increase of MTPL concentration. The latter could be
M
linked with the fact that in an endothermic process, the adsorbate species (drug in this work)

had to displace more than one water molecule for their adsorption and this resulted in the
d

endothermicity of the adsorption process; therefore ΔH0 would be positive. The magnitude of
te

ΔH0 might also give an idea (but not sure) about the type of adsorption. Moreover, the values

of ΔS0 were found to be positive, which reflected the affinity of the adsorbent towards the
p

adsorbate species. In addition, the positive value of ΔS0 suggested increased randomness at
ce

the solid/solution interface with some structural changes in the adsorbate and adsorbent. The

adsorbed solvent molecules, which were displaced by the adsorbate species, gained more
Ac

translational entropy than was lost by the adsorbate species/molecules, thus allowing for the

prevalence of randomness in the system. The positive ΔS0 value also corresponded to an

increase in the degree of freedom of the adsorbed [54].

3.5. Kinetics (empirical and proposed phenomenological model)

13
Page 16 of 36
 To investigate the mechanism of adsorption and its potential rate-controlling steps that

include mass transport and chemical reaction processes, kinetic models have been employed

to analyze the experimental data. At first, the uptake time data obtained (Fig. 7a) was treated

in the form of two most widely-used kinetic models in adsorption works, pseudo-first and

t
second-order model [31,32] as well as the intraparticle diffusion model (inset in Fig. 7a).

ip
Experimental and theoretical calculated Q values and coefficients related to kinetic models are

cr
given in Table SI3 (Supporting information section).

us
The validity of each model could be checked by the linear regression value

(determination coefficient, R2) and a normalized standard deviation ΔQ (%) calculated by the

an
following equation: M
  Q exp  Qcal  
2

 Q
 
ΔQ =  exp  100%
n 1
d
te

where Qexp and Qcal are the experimental and calculated amount of molecule adsorbed

per unit mass of adsorbent(mg/g) at time t, respectively, and n is the number of data points.
p
ce

So, based on R2 (determination coefficient) as well as comparing the experimental

Qexp measured experimentally with the ones achieved from kinetic models (Table SI3,
Ac

Supporting information section), it was observed that pseudo-second-order kinetic model

provided the best fit for the MTPL, thus indicating that the chemical adsorption process took

place on two different types of adsorption sites. The adsorption capacity increases quickly

during the initial 30 min (removal of MTPL 50%), reached its maximum after 4 h. The kinetic

curve is considered to be a classical example of kinetic adsorption plot, in which the

pollutant’s removal is very fast in the first contact minutes (0-30 min), following a gradual

removal (40-200 min), before reaching the equilibrium (240 min). This kinetic behavior is

14
Page 17 of 36
common in adsorption of different pollutants onto polymeric adsorbents (chitosans, etc) [55-

58].

In intraparticle diffusion model, the lower values of regressions coefficients (R2) and

the higher values of ΔQ (%) observed indicated that intraparticle diffusion was not the sole

t
process governing the kinetic of MTPL adsorption on iCAR polymers. The plots of Qt vs t1/2

ip
presented multi-linearity indicating two or more steps influence the adsorption process. The

cr
first step (sharper portion) is considered as an external surface adsorption or faster adsorption

step, whereas a second step was observed at equilibrium stage due to the extremely low

us
adsorbate concentrations in the solution. Since the plots are not linear over the whole time

an
range and they did not have zero intercept, it can be concluded that the intraparticle diffusion

is not the only rate limiting step. It must be emphasized, however, that the kinetic parameters
M
of this model, as well as those of the first- and second-order kinetic models, depend on the

initial solute concentration. Such dependence is of purely empirical nature and these models
d

do not reveal anything about the physics of the adsorption process. There are simple kinetic
te

models for the extraction of an apparent diffusion coefficient under totally unrealistic

conditions since they are based to small time approximate solution of the diffusion equation
p

[59]. In the majority of cases in literature, these models are unable to represent the
ce

experimental data [60] and therefore other more realistic models are needed to simulate the

adsorption process. An alternative approach is the use of a mechanistic (phenomenological)

Ac

model to describe intraparticle diffusion process. Our research team has been previously

applied some phenomenological models in adsorption experiments studies [54-56,61], but

each adsorbent-adsorbate system is unique and therefore the model applied each time must be

novel and unique.

It is considered, that the solute molecules undergo an adsorption-desorption process at

localized sites in the adsorbent particle and they move from site to site either in the adsorbed

15
Page 18 of 36
state (surface diffusion) or in the desorbed state (pore diffusion) [40]. It is not possible to

separately estimate the extent of both types of diffusion from kinetic curves. Nevertheless

based on the fact that pore diffusion is always present and the corresponding apparent

diffusivity has as upper limit the diffusivity of solute in free water, the following procedure

t
has been suggested [61].

ip
At first pore diffusion is assumed and the corresponding model is used to fit the kinetic

cr
data. If the derived diffusivity is clearly smaller than the one in free water then the process is

pore-diffusion dominated else the process is surface diffusion dominated and the fitting

us
procedure is repeated using the surface diffusion model. The pore diffusion model for

an
spherical particles has the form:

q 1  2 D ap q
= r (14)
t r 2 r ρ p f (C) r
M
with the following boundary conditions :

spherical symmetry
d

 q 
te

  =0 (15)
 r r=0
p

Bulk to particle mass transfer

ce

Dap  q 
K m (Cb - C) =   (16)
f (C)  r  r=R
Ac

where t is the time; r is the radial coordinate in the spherical particle; q is the local adsorbed

ion concentration (mass of solute per mass of dry sorbent); Cb is the mass concentration of the

solute in the solution; Km is the mass transfer coefficient from the bulk solution to the particle;

R is the particle radius of the sorbent and ρρ is the density of the dry particle.

The equilibrium relation between free and adsorbed solute is q = f(C) where C is the

concentration of solute in the liquid phase of the particle. The concentration C in Eqs. (14)

and (16) can be found by inverting the relation q = f(C). As function f the L-F isotherm shown

16
Page 19 of 36
in Eq. (8) is used based on the fact that at steady state local and global equilibrium coincides.

The prime in the above equations denotes the differentiation of a function with respect to its

argument. The apparent pore diffusivity Dap depends in principle on the structure of the

swollen particle. The average concentration of the adsorbed species can be computed by the

t
relation:

ip
R
3
R 3 0
q ave = qr 2dr (17)

cr
The evolution of the solute concentration in the bulk can be found through a global mass

us
balance:

m

an
Cb = C0    q ave (18)
V

The partial differential equation (Eq. (14)) is highly non-linear and it has a time dependent
M
boundary condition (Eq. (16)) so it must be solved numerically. A second order finite

difference spatial discretization is combined to a Runge-Kutta integrator in time domain. The

d

above model is used to fit the experimental kinetic data. An average particle radius of 10 μm
te

is considered.
p

As a first step it was assumed that there are no external mass transfer limitations due to
ce

intense agitation so a very large value is set to Km. The best fitting in this case is shown in

Fig. 7b. The model captures correctly the large time behavior but it considerably over-predicts
Ac

the initial adsorption rate. This is unavoidable due to the well-known initial flux burst

phenomenon of the diffusion equation [62]. To alleviate the problem a finite value of Km is

considered. Using a proper choice of Km and Dap, a very good fitting to the experimental data

is achieved as can be seen in Fig. 7b. The particular value found for Dap is 3.7×10-12 m2/s.

This value is two orders of magnitude smaller than the corresponding diffusivity in free water

confirming the assumption of pore diffusion domination. The small value of diffusivity

suggests that the polymer network is dense and there are no large water cavities to allow

17
Page 20 of 36
unhindered diffusion of the solute. The value found for Km is 4×10-6 m/s. This value is too

small for external mass transfer for particles of 10 μm radius. The explanation for this small

value is that the particles are in form of aggregates in which there are regions of quiescent

liquid. The resistance to solute transfer through these regions appears as an external mass

t
transfer resistance and it is incorporated in Km. The advantage of phenomenological models is

ip
that they give information which are no easily accessible experimentally. The evolution of the

cr
adsorbed solute profiles q(r) inside the particle for the kinetic experiment performed here is

shown in Fig. 8. The profiles are by far non-uniform. A front is initially created and then

us
proceeds into the particle with simultaneous decrease of surface concentration due to bulk

an
solute reduction. Only at very large time (equilibrium) the solute profile approaches

uniformity.
M
3.6. Comparison of iCAR biopolymers to “traditional” adsorbents
d

In general, direct comparison of the modified carrageenan materials with the

te

“traditional” adsorbents is not possible due to the different working conditions and model

adsorbates used. However, the maximum theoretical adsorption capacity calculated for
p

iCAR/GLA5 (109 mg/g) is considered to be high enough compared to other materials used for
ce

the removal of organic pollutants such as mesoporous silica SBA-15, zeolites, activated

carbon etc [29-31]. Concerning the comparison of iCAR/GLA5 performance with other
Ac

carrageenan materials a lower degree of swelling and better adsorption abilities for the former

was observed. For example, in a very recent study of Mahdavinia et al., [63] a swelling degree

of 20.5% and a maximum adsorption capacity of 78.2 mg/g was observed for the cationic dye

crystal violet on magnetic kappa-carrageenan/PVA nanocomposite hydrogels, which are

higher and lower, respectively, from the corresponding values in the present study.

18
Page 21 of 36
4. Conclusions

In this study, iCAR and kCAR carrageenan microparticles were synthesized by using

GLA as cross-linking agent at different concentrations (iCAR/GLA2.5, iCAR/GLA5,

kCAR/GLA2.5, kCAR/GLA5) and tested as biosorbents for the removal of MTPL from

t
aqueous solutions. The modified biopolymers were characterized by using FTIR

ip
spectroscopy, X-ray analysis, SEM and swelling capacity. According to characterization and

cr
swelling capacity data, iCAR/GLA5 polymer exhibited good adsorption abilities toward

MTPL. The adsorption of MTPL was pH dependent due to the variation of surface charges at

us
different solution pH. At optimum pH conditions (pH 6) the calculated high maximum

an
adsorption capacity was 109 mg/g at 20 °C (L-F fitting), while at higher temperatures (30 °C

and 40 °C) an increase of Qm was observed (127 and 178 mg/g at 30 and 40 °C, respectively).
M
The equilibrium adsorption data were analyzed with non-linear Langmuir and Freundlich

models. It was found that the equilibrium process was followed the Langmuir-Freundlich
d

model well. After fitting to empirical kinetic models (pseudo-first and -second order
te

equations), a new phenomenological model was proposed to simulate the kinetic data. The

latter led to a very small value of the apparent pore diffusion coefficients of the solute in the
p

adsorbent particle, suggesting hindered diffusion due to the structure of the water regions. In
ce

addition the small value of the external mass transfer coefficient found seems to be related to

the aggregation of the adsorbent particles.

Ac

Acknowledgements

This research has been co-financed by the European Union (European Social Fund — ESF)

and Greek national funds through the Operational Program “Education and Lifelong

Learning” of the National Strategic Reference Framework (NSRF) — Research Funding

19
Page 22 of 36
Program “Excellence II (Aristeia II)”, Research Grant, No 4199, which is gratefully

appreciated.

t
ip
cr
us
an
M
d
p te
ce
Ac

20
Page 23 of 36
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ce

chitosan to adsorption kinetic data, Langmuir, 26 (2010) 9617-9626.

[62] J. Crank, The Mathematics of Diffusion, Oxford University Press, London, UK, 1975.
[63] Gh. R. Mahdavinia, A. Massoudi, A. Baghban, E. Shokri, Study of adsorption of cationic
dye on magnetic kappa-carrageenan/PVA nanocomposite hydrogels, J. Environ. Chem. Eng., 2
Ac

(2014) 1578-1587.

24

Page 27 of 36
 zone 1 zone 2 zone 3
100
90
80

t
ip
70
60
SP (%)

cr
50
40

us
30
20
kCAR/GLA iCAR

an
10 kCAR/GLA2.5 iCAR/GLA2.5
kCAR/GLA5 iCAR/GLA5
0
0 50 100 150 200 250 300 350 1200 1500
M
Time (min)

Fig. 1. Swelling kinetics of carrageenan derivatives (SD, n = 3).

d
p te
ce
Ac

25

Page 28 of 36
 100000
iCAR/GLA5
90000 MTPL

t
iCAR/GLA5 - MTPL

ip
Intensity (counts)

60000

50000

cr
40000

us
30000

20000

an
10000

0
10 20 30 40 50
M
2theta (degree)

Fig. 2. XRD patterns of iCAR, MTPL, iCAR/GLA5-MTPL.

d
p te
ce
Ac

26

Page 29 of 36
 t
ip
cr
us
(a) (b)

Fig. 3. SEM micrographs of: (a) iCAR; (b) iCAR/GLA5.

an
M
d
p te
ce
Ac

27

Page 30 of 36
 iCAR
MTPL
iCAR/GLA5
iCAR/GLA5 - MTPL

t
ip
Absorbance

cr
us
4000 3500 3000 2500
an
2000 1500
-1
1000 500
M
Wavenumbers (cm )
Fig. 4. FT-IR spectra of the prepared carrageenan derivatives before and after MTPL
adsorption.
d
p te
ce
Ac

28

Page 31 of 36
 HO H H+ O HO H 3C
O N CH3 H
OH
O
HO
H3C CH3
HO H O
O
OSO3 2

O O

t
ip
O
O
O
O HO

cr
O OSO3
O H

HC C3H6 CH +HN

us
CH 3
O O
H3C
OSO3
O

2
O

an
O OH

O
O O OH

HO H

OSO3
M
H
O

HO

HO H H+
N O HO
O CH 3 H
OH
d
HO
H3C CH3
HO H O
O
2
te

Fig. 5. Proposed adsorption interactions.

p
ce
Ac

29

Page 32 of 36
 70
iCAR/GLA5
60

t
50
Removal (%)

ip
40

cr
30

20

us
10

an
0
2 4 6 8 10 12
pH
M
(a)

90
d

Langmuir
80 Freundlich
te

L-F
70

60
p
Qe (mg/g)

50
ce

40

30
Ac

20 o
20 C
o
10 30 C
o
40 C
0
0 5 10 15 20 25 30 35 40 45
Ce (mg/L)

(b)
Fig. 6. Effect of (a) pH and (b) initial MTPL concentration onto iCAR/GLA5 (SD, n = 3).

30

Page 33 of 36
 45
35
40
30
35

t
25

ip
Qt (mg/g)
30 20
Ce (mg/L)

25 15

cr
10
20 Intraparticle diffusion
5 Pseudo-1st order

us
15 Pseudo-2nd order
0
0 30 60 90 120 150 180
10 t (min)

an
5
0 100 200 300 400 500 600 1200
t (min)
M
(a)
d

45 40 40
Pseudo-1st
te

35 35
40 30 30 Pseudo-2nd
25 25
35 20 20
p

15 15
30 10 10
Ce (mg/L)

ce

5 5
25 0 30 60 90 120 150 180 210 240 270 300 0 30 60 90 120 150 180 210 240 270 300

20
zoom-in
Ac

15
External mass transfer
No external mass transfer
10

5
0 100 200 300 400 500 600 1200
t (min)

(b)
Fig. 7. Effect of contact time on adsorption of MTPL using (a) empirical models and (b)
phenomenological model (SD, n = 3).

31

Page 34 of 36
 55
t = 5 min t = 90 min
50 t = 10 min t = 150 min
t = 20 min t = 240 min
45
t = 50 min t = 360 min
40 t = 720 min

t
35

ip
Q (mg/g)

30
25

cr
20
15

us
10
5
0

an
0.0 0.2 0.4 0.6 0.8 1.0
r/R

Fig. 8. Evolution of the adsorbed solute profiles q(r) inside the particle.
M
d
p te
ce
Ac

Page 35 of 36
Graphical Abstract (for review)

i
cr
us
an
M
ed
pt
ce
Ac

Page 36 of 36