Materials Science and Engineering C 57 (2015) 288293

Contents lists available at ScienceDirect

Materials Science and Engineering C

journal homepage: www.elsevier.com/locate/msec

On the mechanical properties of PLCbioactive glass scaffolds fabricated

via BioExtrusion
T. Fiedler a,, A.C. Videira b,c, P. Brtolo c, M. Strauch a, G.E. Murch a, J.M.F. Ferreira b
a
b
c

Discipline of Mechanical Engineering, The University of Newcastle, Callaghan, NSW 2308, Australia
Department of Materials and Ceramic Engineering, University of Aveiro, CICECO, 3810-193 Aveiro, Portugal
Centre for Rapid and Sustainable Product Development, Polytechnic Institute of Leiria (IPL), Leiria, Portugal

a r t i c l e

i n f o

Article history:
Received 11 February 2015
Received in revised form 15 April 2015
Accepted 30 July 2015
Available online 1 August 2015
Keywords:
Polycaprolactone (PCL)
FastOsBG
Scaffolds
Robocasting
Mechanical properties

a b s t r a c t
This paper addresses the mechanical characterization of polycaprolactone (PCL)bioglass (FastOsBG) composites and scaffolds intended for use in tissue engineering. Tissue engineering scaffolds support the self-healing
mechanism of the human body and promote the regrowth of damaged tissue. These implants can dissolve
after successful tissue regeneration minimising the immune reaction and the need for revision surgery. However,
their mechanical properties should match surrounding tissue in order to avoid strain concentration and possible
separation at the interface. Therefore, an extensive experimental testing programme of this advanced material
using uni-axial compressive testing was conducted. Tests were performed at low strain rates corresponding to
quasi-static loading conditions. The initial elastic gradient, plateau stress and densication strain were obtained.
Tested specimens varied according to their average density and material composition. In total, four groups of
solid and robocast porous PCL samples containing 0, 20, 30, and 35% bioglass, respectively were tested. The addition of bioglass was found to slightly decrease the initial elastic gradient and the plateau stress of the biomaterial
scaffolds.
2015 Elsevier B.V. All rights reserved.

1. Introduction
A signicant change in life span was observed in the last century,
especially in the most developed countries, because of various improvements in the quality of life [1]. But this enhancement in life expectancy has also resulted in the increased incidence of degenerative
musculoskeletal diseases including back pain, osteoarthritis and osteoporosis that might be exacerbated by excessively sedentary lifestyles [2]. Other limitations to mobility derive from serious injuries
caused by traumatic accidents. All these changes have created a
new need for bone repair and regeneration and have been the main
driving forces towards developing improved bone grafts and constructing scaffold materials for bone tissue engineering [3].
The tissue engineering concept was dened by Langer and
Vacanti [4] as an interdisciplinary eld that applies the principles of
engineering and the life sciences toward the development of biological
substitutes that restore, maintain or improve tissue function. The
main idea is combining living cells, biologically active molecules and a
structural scaffold to support cell colonization, migration, growth and
differentiation, thereby guiding the development of the required tissue.
However, from a materials science and engineering viewpoint, the design and fabrication of scaffolds with suitable composition, structure
Corresponding author.
E-mail address: Thomas.Fiedler@newcastle.edu.au (T. Fiedler).

http://dx.doi.org/10.1016/j.msec.2015.07.063
0928-4931/ 2015 Elsevier B.V. All rights reserved.

and properties (mechanical, bioactive, degradation rate, etc.) are highly

challenging problems. Besides providing the three-dimensional growth
of cells in an organized way, an ideal scaffold should be characterized by
biocompatibility, biodegradability, appropriate mechanical properties,
interconnectivity of pores with appropriate size to retain cells, and
allow exchanges of nutrients and waste products. Therefore, a wise selection of the starting materials and of the fabrication techniques is of
paramount importance. Numerous natural and synthetic materials can
be used for the fabrication of scaffolds including polymers, ceramics,
bioactive glass, and calcium phosphates, and have been reviewed in detail elsewhere, see for example [3].
Poly (-caprolactone) or PCL is one of the most extensively investigated polymers due to its interesting and attractive set of properties [5,
6]. PCL is a noncytotoxic polymer, has a low melting point (~60 C) and
glass transition temperature (~60 C) [5], and possesses suitable mechanical properties for bone tissue regeneration [610]. The main limitation of PCL is its relatively slow bioresorption rate in vivo [11,12].
Strategies to enhance the degradation rate of PCL scaffolds have included the addition of inorganic bioresorbable materials such as calcium
phosphates and bioglasses into the PCL matrix [1317]. However,
most of the PCLbioglass composites developed so far [1417] have
dealt with the addition of 45S5 Bioglass, a relatively water soluble material that tends to originate high pH values due to its high sodium content. Aiming at mitigating these drawbacks, a series of alkali-free
bioactive glasses (FastOsBG) have been developed and patented

T. Fiedler et al. / Materials Science and Engineering C 57 (2015) 288293

289

recently [18]. It has been revealed that FastOsBG possesses a fast biomineralization rate in vitro by developing a carbonated hydroxyapatite
surface layer after 1 h of immersion in simulated body uid (SBF) [19].
Considering the biomineralization mechanism and steps proposed by
Larry Hench [20], it was suggested that FastOsBG enables jumping immediately from step 1 to step 5 of the mechanism, skipping the intermediate 24 steps [21]. The formation of a silica-rich gel layer, considered
to be essential in the biomineralization of 45S5 Bioglass and other
compositions derived from it seems not to be required. Therefore,
FastOsBG was selected as a bioactive ller for the PCL matrix aiming
at developing scaffolds for bone regeneration and tissue engineering
with a better balanced set of properties.
But information available in the literature reporting on the effects
of bioactive glass powders on the mechanical properties of glassreinforced polycaprolactone composites is still scarce and not detailed
enough [1316,22,23]. Moreover, no study has been undertaken so far
using FastOsBG particles as reinforcement for the PCL matrix. Therefore, the specic objective of the present work is on evaluating the
effects of incorporating different weight proportions of FastOsBG (0,
20, 30, and 35%) on the mechanical properties of PCLFastOsBG composite scaffolds produced via BioExtrusion [9,24]. Cylindrical samples of
the separated components (PCL, FastOsBG) were equally submitted to
the same uni-axial compressive testing in an attempt to get a deeper insight about the specic contributions to the mechanical properties of
these composites.

(Rigaku Geigerex D/Max, Tokyo, Japan; C Series; CuKa radiation; 2

angle range 1080; step 0.02 s1) (data not shown).
Cylindrical testing samples of bioactive glass with lengths varying in
the range from 6.53 mm to 16.74 mm and a xed diameter of ~11 mm,
were also prepared by cutting a cylindrical rod cast into a metallic
mould and annealed for 1 h at around the transformation temperature,
Tg 750 C. The bulk density of the resulting FastOsTCP20 samples
was 2.77 g/cm3. This density had been obtained by measuring the
mass of the nal samples and dividing the value by the calculated cylindrical sample volume.
A semi-crystalline (56%) aliphatic thermoplastic polyester powder of
polycaprolactone (PCL) with a molecular weight of ~50,000 g mol1, a
low melting point of 5860 C and a glass transition temperature (Tg)
of approximately 60 C was used.
Feedstock mixtures of PCL + FastOsTCP20 with several bioglass
contents (0, 20, 30, and 35 wt.%) were prepared by mixing the components at a temperature of ~80 C under slow mechanical hand stirring.
No additives were used and accordingly the corresponding PCL contents
are 100, 80, 70, and 65 wt.%. The obtained feedstocks were then used to
prepare solid cylindrical testing specimens (diameter = 1.32 mm,
height 9 mm) and porous scaffolds (see Fig. 1) by using a BioExtruder
device reported elsewhere [8,9]. Scaffolds were manufactured by deposition of cylindrical laments of 300 m diameter in a layer by
layer fashion according to a 0/90 geometry, and distances of
280 m and 650 m between consecutive layers, or consecutive laments, respectively.

2. Experimental procedure

2.2. Compressive testing

All compression tests were executed with Shimadzu AG series compression machines. A 50 kN load cell was used for the solid samples and
a 5 kN load cell was used for the porous scaffolds for improved accuracy
at lower forces. The experiment was controlled by the TrapeziumX software. A sampling rate of 10 measurements per second was selected at a
maximum compression rate of 1.0 mm/min (quasi-static compression).
During the uni-axial compression tests, the software captured force F
and corresponding displacement values u. These were converted into
engineering stress and strain by division with the initial sample
cross section A0 and height h0, i.e. = F A0, = u h0. The obtained
stressstrain data was further processed to determine the plateau stress
P, plateau modulus P, elastic modulus E, and 1% offset yield strength
1.0. To this end, the approximate plateau stress p was calculated as
the average stress between = 0.2 and = 0.3 macroscopic strain.
The elastic modulus E is equal to the slope between the two points
P1 and P2 (see Fig. 2) that correspond to 25% and 30% of the approximate plateau stress p. The line connecting both points was extrapolated and its interception with the x-axis was selected as the new
origin. As a result, settling effects of samples between the pressure
stamps were ltered from the stressstrain data. Using these

2.1. Materials and reagents

An alkali-free bioactive glass composition was designed in the system diopside (CaMgSi2O6 hereafter referred to as Di)uorapatite
([Ca5(PO4)3F] hereafter referred to as FA)tricalcium phosphate
(3CaOP2O5 hereafter referred to as TCP) with a general formula
Di70FA10TCP20 (wt.%). Belonging to the set of FastOsBG compositions, this was specically designated as FastOsTCP20 [19].
High-purity powders of SiO2 (purity N 99.5%), CaCO3 (N 99.5%),
MgCO3 (BDH Chemicals Ltd, UK, purity N 99.0%), NH4H2PO4 (SigmaAldrich, Germany, N 99.0%) and CaF2 (Sigma Aldrich, Germany,
325 mesh, N 99.9%) were used. Homogeneous mixtures of batches
(~ 100 g), obtained by ball milling, were preheated at 900 C for 1 h
for decarbonization and then melted in Pt crucibles at 1570 C for
1 h in air. The glass was obtained in frit form by quenching the melt in
cold water. The frits were dried and then milled in a high speed agate
mill, resulting in ne glass powders with mean particle sizes of
~1020 m (determined by light scattering technique; Coulter LS 230,
Beckman Coulter, Fullerton, CA; Fraunhofer optical model). The amorphous nature of glasses was conrmed by X-ray diffraction analysis

Fig. 1. Robocast scaffold: a) three dimensional view and b) magnication of the meso-structure.

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T. Fiedler et al. / Materials Science and Engineering C 57 (2015) 288293

Fig. 2. Correction and evaluation of stressstrain data.

corrected data, the real plateau stress P and the plateau modulus P
(i.e. the gradient of the stressstrain curve between = 0.2, 0.3)
were determined. The offset yield stress was obtained by drawing a
parallel to the elastic gradient with a strain offset of 1.0%. The intersection with the stressstrain curve marks the offset yield strength.
The plateau end strain is the strain at the intersection point between
the stressstrain data and = 1.3 P.
3. Results and discussion
In the following the results of the experimental study are presented.
In the rst part the compressive testing results of solid bioglassPCL
samples are presented. The second part focuses on the effective mechanical properties of bioglassPCL scaffolds.
3.1. Solid composites
First, uni-axial compressive tests were performed on solid composite
samples with varying bioglass content. All solid samples were of cylindrical shape with an outer diameter between 11.64 mm and 13.23 mm and

Table 1
Solid composite sample data.
ID

Bioglass content

Diameter
[mm]

Volume
[cm3]

Mass
[g]

Density
[g/cm3]

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20

0%
0%
0%
0%
20%
20%
20%
20%
30%
30%
30%
30%
35%
35%
35%
35%
100%
100%
100%
100%

13.19
13.20
13.18
13.20
13.14
13.22
13.21
13.23
13.18
13.20
13.20
13.17
13.23
13.14
13.22
13.02
11.64
11.67
11.75
11.73

0.95
1.04
1.02
1.29
0.71
0.69
0.95
1.08
0.73
0.77
0.93
1.05
0.84
0.89
0.96
1.07
0.83
0.70
0.82
0.67

1.07
1.17
1.15
1.45
0.88
0.85
1.19
1.34
0.95
1.01
1.21
1.39
1.12
1.18
1.27
1.40
2.30
1.94
2.30
1.86

1.12
1.12
1.12
1.13
1.24
1.24
1.25
1.24
1.30
1.31
1.30
1.32
1.33
1.32
1.33
1.31
2.77
2.76
2.79
2.77

a variable height ranging from 5.00 mm to 9.45 mm. The sample data
is summarized in Table 1. It becomes clear from the table that the
bioglass content determines the average density since the density
of the bioglass (BG = 2.77 g/cm 3) is distinctly higher than PCL
(PCL = 1.12 g/cm3 ). The densities shown in Table 1 are derived
from experimental measurements (i.e. calculated as the ratio of measured mass divided by the sample volume). Alternatively, the mixing
rule 1 [BG BG + (1 BG) PCL] can be applied to estimate the
composite density, where BG is the weight percentage of the
bioglass. The resulting values slightly overpredict the measured densities which can be related to experimental error and possibly the occurrence of small pores within the samples.
Fig. 3 shows the compressive stressstrain response for bioglass contents ranging from 0%35%. It can be observed that all samples exhibit a
similar compressive behaviour. An initial elastic range (slope is the
quasi-elastic modulus E) is followed by a region of moderate stress increase (plateau modulus P) before the stress rises rapidly due to increasing sample cross sections.
Fig. 4a shows the elastic gradient of solid biomaterial composite
samples plotted versus their average density. The elastic gradient
of the composites is found to increase with the addition of bioglass.
Moderate scatter of the data points can be attributed to limited measurement accuracy at small strains due to settling effects and data

Fig. 3. Compressive stressstrain response of solid biomaterial composites.

T. Fiedler et al. / Materials Science and Engineering C 57 (2015) 288293

291

Fig. 4. Effective material properties of solid biomaterial composites vs density: a) elastic gradient and b) plateau stress.

correction (see Fig. 2). Fig. 4b shows the plateau stress of the solid
biomaterial composites plotted versus their average density. The
plateau stress does not seem to be systematically affected by the
bioglass content of the composite and values scatter around the average value of 28.5 MPa. Only a minor increase of the plateau stress
due to the addition bioglass is found.
In addition to the tests on bioglassPLC composites, compressive
tests have been performed on pure bioglass samples (i.e. 100% bioglass
content). The corresponding stressstrain data are shown in Fig. 5. In
contrast to the composite samples (see Fig. 3) brittle material behaviour
is observed. After reaching a maximum stress, the samples fracture and
are unable to support further load. Transient spikes in the stressstrain
curve are caused by the spalling of small fragments from the cylindrical
samples. The stressstrain data indicate a strong variation in mechanical properties of the pure bioglass samples. A likely explanation is the
insufcient annealing of the glass samples. As a result, the thermomechanical stresses due to rapid cooling upon casting might not have
been completely relieved. Maximum stresses and failure strains of the
four considered samples exhibit signicantly different values. This inconsistency of bioglass properties is likely to contribute to the scatter
of mechanical properties in the solid composite samples (see Fig. 4).
Hence annealing of the bioglass is likely to decrease the scattering of
the mechanical properties of these composites.
3.2. Scaffold composites
The second experimental testing series focused on uni-axial compressive tests of BioExtruded scaffolds. The samples were of prismatic shape (see Fig. 1) with side length varying between 7.75 mm and
9.47 mm. The sample data are summarized in Table 2. The porosity

p is calculated according to p = 1 Sc Sl where Sc is the scaffold

density and Sl is the average solid density for the corresponding
bioglass content (see Table 1). The porosity values of the tested scaffolds range between 43.1 and 53.9% and tend to increase with
bioglass content.
The stressstrain curves of the composite scaffolds are shown in
Fig. 6. Different line types represent variations in the bioglass content
of the scaffold material. The stressstrain curves exhibit a similar characteristic as the solid biomaterial composites: initial elastic deformation
is followed by a plateau with a moderate stress increase and a nal stage
with a rapid stress increase at high strains. The onset of this nal stage is
shifted towards higher strains in comparison to the solid samples due to
the scaffold porosity. Furthermore, distinctly lower stress levels are
found in comparison to Fig. 3.
In the next step, the stressstrain data were used to extract effective scaffold properties. The results are visualised in the following
Figs. 7 and 8 where effective material properties are plotted versus
density. Data points with high specic stiffness or strength are located in the top left of these plots whereas low specic values are found
in the bottom right. The initial slope of the curve is the initial elastic
gradient E. It should be mentioned here that analogous to the solid
samples the measurement of the elastic gradient was affected by
the settling of the samples. Since the two scaffold planes in contact
with the compression plates were not perfectly parallel, a small precompression was required to establish full contact. This effect is ltered in the stressstrain data but has a negative impact on the measurement accuracy of the elastic gradient and the 1.0% offset yield
stress. In Fig. 7a, the elastic gradient is plotted versus the density.
The effective scaffold property shows a strong dependence on the
density. Among the considered samples, the PCL-only scaffolds
Table 2
Scaffold sample data.

Fig. 5. Compressive stressstrain response of solid bioglass.

ID

Bioglass content

Volume
[cm3]

Mass
[g]

Density
[g/cm3]

Porosity
[%]

Sc1
Sc2
Sc3
Sc4
Sc5
Sc6
Sc7
Sc8
Sc9
Sc10
Sc11
Sc12
Sc13
Sc14
Sc15
Sc16
Sc17

0%
0%
0%
0%
20%
20%
20%
20%
20%
30%
30%
30%
30%
30%
35%
35%
35%

0.687
0.701
0.710
0.715
0.678
0.691
0.667
0.680
0.685
0.659
0.682
0.666
0.676
0.679
0.680
0.708
0.670

0.36
0.42
0.40
0.45
0.48
0.45
0.45
0.45
0.45
0.43
0.44
0.41
0.43
0.41
0.43
0.47
0.42

0.530
0.604
0.569
0.623
0.707
0.654
0.678
0.656
0.651
0.653
0.648
0.619
0.637
0.603
0.636
0.667
0.629

52.8
46.2
49.3
44.5
43.1
47.4
45.4
47.2
47.6
50.1
50.4
52.7
51.3
53.9
51.9
49.6
52.4

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T. Fiedler et al. / Materials Science and Engineering C 57 (2015) 288293

Fig. 6. Compressive stressstrain response of scaffolds.

exhibit the highest value for a given density and show an approximately linear dependence. The addition of bioglass decreases the
elastic gradient. However, no clear dependence between bioglass
content and scaffold stiffness could be established. Fig. 7b shows

the 1.0% offset yield stress. Again, an approximately linear dependence on density is observed and the yield stress exhibits maximum
values for PCL scaffolds (0% bioglass content). The addition of
bioglass seems to gradually decrease the stress values. The scatter
of data points is attributed to both measurement inaccuracy due to
settling effects and inconsistent mechanical properties of the
bioglass phase (see Fig. 5).
Fig. 8a shows the plateau stress (i.e. the arithmetic mean of the macroscopic engineering stress between the strain = 0.2 0.3) plotted
versus the average scaffold density. Owing to measurement at higher
strains 0.2, settling effects do not affect these measurements. PCLonly scaffolds exhibit the highest plateau stresses among the considered
samples. The addition of bioglass continuously decreases the plateau
stress for a given scaffold density. This can be best seen in Fig. 8b
where the plateau stress has been normalised by the scaffold density
(P/Sc). The plot shows a linear decrease of this normalised plateau
stress with increasing bioglass content.
The numerical values of the effective scaffold properties are given in
Table 3. In addition to the properties shown in Figs. 7 and 8, the plateau
modulus, the deformation energy and the plateau end strain are listed.
The plateau modulus is found to vary between 9.919.5 MPa with no
clear correlation to the bioglass content. The plateau modulus tends to
increase for higher scaffold densities. The deformation energy (i.e. the

Fig. 7. Effective material properties of scaffolds vs density: a) elastic gradient and b) 1.0% offset yield stress.

Fig. 8. Plateau stress of composite scaffolds: a) vs density and b) normalised vs bioglass content.

T. Fiedler et al. / Materials Science and Engineering C 57 (2015) 288293

Table 3
Effective scaffold properties.
ID

Bioglass
content
[%]

Elastic
gradient
[MPa]

1% offset
yield stress
[MPa]

Plateau
stress
[MPa]

Plateau
modulus
[MPa]

Energy
[MJ/m3]

Plateau
end strain
[]

Sc1
Sc2
Sc3
Sc4
Sc5
Sc6
Sc7
Sc8
Sc9
Sc10
Sc11
Sc12
Sc13
Sc14
Sc15
Sc16
Sc17

0%
0%
0%
0%
20%
20%
20%
20%
20%
30%
30%
30%
30%
30%
35%
35%
35%

25.9
81.7
76.1
91.0
89.6
84.7
71.3
81.5
42.4
80.9
77.5
48.4
63.5
65.2
67.4
90.0
64.7

3.12
4.23
3.56
4.43
4.70
3.81
4.08
3.80
5.72
3.04
3.41
2.85
4.29
4.11
2.92
3.41
2.38

5.08
7.19
6.69
8.26
7.98
6.52
6.89
6.80
7.49
5.79
5.97
5.06
6.75
6.04
5.27
6.21
4.60

13.4
15.7
13.6
19.3
19.0
12.9
14.0
13.7
19.5
11.3
13.0
9.9
17.9
15.6
14.3
15.6
11.4

1.45
2.13
1.92
2.28
2.25
1.97
2.08
2.04
1.99
1.75
1.73
1.53
1.85
1.68
1.39
1.71
1.26

0.37
0.36
0.35
0.34
0.35
0.36
0.36
0.36
0.34
0.36
0.35
0.37
0.34
0.34
0.33
0.34
0.34

293

on the scaffold density. All material properties except the plateau end
strain were found to increase with the scaffold density. The addition of
bioglass was found to decrease the elastic gradient and yield stress if
two scaffolds of the same density are compared.
Acknowledgements
The authors T. Fiedler and G.E. Murch wish to acknowledge the nancial support by the Australian Research Council (ARC) in the
framework of the Discovery Project DP130101377.
This work was also supported by the European Regional Development Fund (FEDER) under the PT2020 Partnership Agreement through
the COMPETE, by the Portuguese Government through the Portuguese
Foundation for Science and Technology (FCT), in the scope of the projects UID/CTM/50011/2013 (Aveiro Institute of Materials, CICECO,
www.ciceco.ua.pt) and the fellowship grant Reference PTDC/CTM/
99489/2008.
References

area under the stressstrain curve up to 30% macroscopic strain) lies between 1.26 and 2.28 MJ/m3 and correlates with the plateau stress. Finally, a relatively consistent plateau end strain e = 0.33 0.37 is found.
The results of this study can be used as a design aid to select the
optimum bioglass/PCL composition for a tissue engineering scaffold.
Young's modulus of spongy bone has been found to be about
300 MPa [25] which distinctly exceeds the elastic gradient of all
scaffolds. Fig. 7a indicates that the scaffold stiffness is primarily
governed by density and thus higher density scaffolds seem benecial for improved elastic compatibility with the surrounding bone
tissue. However, a higher density is equivalent with lower scaffold
porosity and thus less available volume for the formation of new
bone tissue. The strength of spongy bone is approximately 2.2
4.5 MPa [26]. The 1% offset yield stress of all tested scaffolds falls
into this range irrespective of their density and bioglass content
and are therefore considered sufciently strong for mechanical support. Hence the highest bioglass content (35%) seems benecial as it
(i) does not signicantly deteriorate the scaffold mechanical properties and (ii) promotes bioactivity.
4. Conclusions
The present paper addresses the mechanical characterization of
PCLbioglass composites. Both solid and porous composites (scaffolds)
have been considered for the bioglass contents 0%, 20%, 30% and 35%.
Uni-axial compressive testing was conducted for quasi-static loading
to determine the stressstrain response and effective mechanical properties. The addition of bioglass was found to increase the density of the
composites due to the higher density of bioglass (2.77 g/cm3) in comparison to PCL (1.12 g/cm3). In solid samples, the addition of bioglass
was found to slightly increase the elastic gradient whereas the plateau
stress remains approximately constant. Testing of pure solid bioglass
samples showed strong scatter of mechanical properties. This was attributed to residual stresses arising from incomplete annealing of the
bioglass. Testing of composite scaffolds showed a strong dependence

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