Biological and mechanical properties of pmma based bioactive bone cements bioactive bone cements

1. Short Communication
Mechanical properties and apatite-forming ability of PMMA bone cements
D. Rentería-Zamarrón *, D.A. Cortés-Hernández, L. Bretado-Aragón, W. Ortega-Lara
CINVESTAV IPN-Unidad Saltillo, Carr. Saltillo-Mty, Km 13, Apdo. Postal #663, C.P. 25000 Saltillo, Coahuila, Mexico
a r t i c l e i n f o
Article history:
Received 18 April 2008
Accepted 29 November 2008
Available online 10 December 2008
a b s t r a c t
The in vitro bioactivity of wollastonite-containing polymethyl-methacrylate (PMMA) cements was eval-
uated. Cements were prepared by varying the wollastonite content. Working times of the mixtures, as
well as the maximum temperature reached during setting, were evaluated. The bioactivity was assessed
by soaking samples in a simulated body fluid (SBF) with an ionic concentration nearly equal to that of
human blood plasma. The compressive strength of the cements was also evaluated. Potentially bioactive
PMMA cements were obtained by adding more than 20 wt% of wollastonite ceramics. The compressive
strength of the cements decreased as the wollastonite content was increased.
Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction
Polymethyl-methacrylate (PMMA) cements are widely used for
the mechanical fixation of metallic hip replacement prostheses to
bone. Methyl-methacrylate monomers (MMA) are the basic com-
ponent of these systems. For clinical applications, the liquid
MMA is mixed with solid beads of PMMA and inserted in the hard
tissue where the polymerization process is completed [1]. Poly-
merizing accelerators and/or activators are also currently added
to the liquid/solid mixture. The PMMA cements were developed
in the early 1960s and they have been classified as bioinert mate-
rials due to the presence of fibroblastic cells at the cement–bone
interface. The PMMA allows an immediate structure support how-
ever, the cement is considered to be the weak link between bone
and the metallic implant, providing a barrier to direct fracture
healing. In extreme cases this may lead to loosening of the joint
and the necessity of a second surgical intervention. To overcome
these problems, research has been performed in the aim to induce
bioactivity and to improve the mechanical properties of organic ce-
ments by adding an inorganic bioactive system [2–4]. Apart from
promoting bioactivity, the mechanical properties of PMMA ce-
ments may also be improved by adding small amounts of bioactive
systems, such as hydroxyapatite (HA) [5]. Other type of cement,
which formulation contains both a polymer and a ceramic has
shown to be highly bioactive [6]. This cement consists of triethyl-
ene-glycol-dimethacrylate (TEGDMA) and apatite- and wollaston-
ite-containing glass–ceramic (A/W) which shows also appropriate
mechanical properties. Its excellent bioactivity has been attributed
to the monomers content, those corresponding to TEGDMA, which
lead to a high reactivity of the A/W glass–ceramic when the ce-
ment is soaked in a simulated body fluid (SBF) [6].
A PMMA/silica nanocomposite showing both high fracture
toughness and appropriate bioactivity was also developed [7]. Its
high fracture toughness was achieved by reducing the covalently
bonded siloxane linkages.
On the other hand, the high bioactivity of wollastonite ceramics
has been demonstrated [8,9]. The reaction between wollastonite
and SBF starts with an ionic exchange of Ca2+
for 2H+
. This reaction
transforms the wollastonite crystals into an amorphous silica
phase and increases the calcium concentration and the pH of the
surrounding SBF, giving the condition for apatite nucleation and
simultaneous dissolution of the amorphous silica. Furthermore,
when a ceramic or polymeric material is immersed in SBF on a
bed of A/W glass–ceramic [10] or wollastonite ceramics [11,12] a
bone-like apatite layer is formed on the substrates. Both wollaston-
ite ceramics and A/W glass–ceramic act as a supplier of calcium
ions increasing the supersaturation degree of the fluid with respect
to apatite [13].
This work aims to promote bioactivity on PMMA cements by
adding wollastonite ceramics. The effect of the wollastonite con-
tent on the in vitro bioactivity of the cements and on the compres-
sive strength has been evaluated. Additionally, during
polymerization, setting and doughing times of the mixtures and
the maximum temperature reached were determined.
2. Materials and methods
2.1. Preparation of the wollastonite-containing PMMA cements (W/
PMMA)
A solid and a liquid component were mixed for the preparation
of cements. The solid component consisted of a powder mixture of
wollastonite (W, Gosa S.A.), PMMA beads with an average molecu-
lar weight (Mw) of 350,000 (Alfa Aesar) and benzoyl peroxide
(BPO, Sigma–Aldrich) as a polymerization initiator. The powders
0261-3069/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.matdes.2008.11.024
* Corresponding author. Tel.: +52 844 4389600x9680; fax: +52 844 4389610.
E-mail address: dora.cortes@cinvestav.edu.mx (D. Rentería-Zamarrón).
Materials and Design 30 (2009) 3318–3324
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2. were mixed for 1 min. The liquid component was prepared by mix-
ing MMA monomer (Alfa Aesar) and N,N-dimethyl-p-toluidine
(DMPT, Alfa Aesar) for 30 s. DMPT was added to the MMA mono-
mer as a polymerization accelerator. Five different mixtures were
prepared by varying the wollastonite content with respect to
PMMA (Table 1). The quantity of MMA, BPO and DMPT was kept
constant [2]. Each paste was prepared by mixing the solid compo-
nent with the liquid for 3 min at a powder-to-liquid (P/L) mass ra-
tio of 1:1 at room temperature.
2.2. Measurement of temperature and setting and doughing times
during polymerization
After mixing the liquid and the solid for 3 min, each paste was
poured into a cylindrical mold (19 mm in diameter, 50 mm in
height) and the setting behavior was evaluated using a Vicat nee-
dle (ASTM C 191). Setting temperature was recorded every 20 s
using a digital thermometer (Taylor, model 9841). To determine
the doughing time (which defines the moment when the cement
should be applied), the paste was probed by finger wearing a latex
glove every 20 s until the mixture separated cleanly from the glove
(ASTM F451-99a).
2.3. Compressive strength
For the compressive strength evaluation, after mixing the solid
with the liquid for 3 min (Section 2.1), each paste was poured into
a previously designed mold with internal dimensions of 6 mm in
diameter and 12 mm in height. After setting, the cements were
kept in a desiccator before testing. The compressive load was ap-
plied at a cross-head speed of 0.5 mm/min according to the speci-
fied in the ASTM F-451-95 standard. Five specimens were tested
for each composition (Table 1) and the average and standard devi-
ation were calculated.
2.4. In vitro bioactivity assessment
After mixing the solid and the liquid for 3 min (see procedure
described in Section 2.1) each paste was poured into a mold to ob-
tain cylindrical specimens with 19 mm in diameter and 5 mm in
height. After setting, the specimens were ground on SiC papers
ranging from 600 to 2400 grit and finally polished with 1 and
3 lm diamond paste. To assess bioactivity polished and unpolished
samples were immersed in a simulated body fluid (SBF) with ion
concentration nearly equal to that of human blood plasma (Table
2) [14]. For the preparation of SBF appropriate amounts of reagent
grade chemicals of NaCl, NaHCO3, KCl, K2HPO4 Á 3H2O, MgCl2 Á
6H2O, CaCl2 Á 2H2O, Na2SO4 and tris-hydroxymethyl aminometh-
ane (CH2OH)3CNH2 were dissolved into deionized water and buf-
fered to pH 7.25 at 36.5 °C with hydrochloric acid [14]. Each of
the five sets of samples was immersed in 150 ml of SBF for 21 days
at physiological conditions of pH and temperature.
The surface of the cements before and after immersion in SBF
was analyzed by Scanning Electron Microscopy (SEM, XL-30, Phil-
Table 1
Compositions of wollastonite-containing PMMA cements.
Identification Powder (wt%) Liquid (wt%)
PMMA BPO W MMA DMPT
W-97 – 2.9 97.1 99.2 0.8
W-68 29.1 2.9 68 99.2 0.8
W-49 48.6 2.9 48.6 99.2 0.8
W-39 58.3 2.9 38.8 99.2 0.8
W-19 77.7 2.9 19.4 99.2 0.8
Table 2
Ionic concentration of SBF and human blood plasma.
Na+
K+
Ca2+
Mg2+
ClÀ
HCOÀ
3 HPO2À
4 SO2À
4
SBF 142.0 5.0 2.5 1.5 147.8 4.2 1.0 0.5
Human blood
plasma
142.0 5.0 2.5 1.5 103.0 27.0 1.0 0.5
Table 3
Working times and maximum temperature reached during setting.
Identification Doughing time
(min)
Setting time
(min)
Maximum
temperature (°C)
W-97 – – 36.5
W-68 9.36 15.33 46.8
W-49 3.45 6.66 71
W-39 3.17 6.60 80.5
W-19 4.31 8.33 90.5
W-0 (no wollastonite
added)
7 10.33 98
Fig. 1. Effect of the wollastonite content on the mechanical properties.
Fig. 2. XRD patterns of the cement mixtures before immersion in SBF.
D. Rentería-Zamarrón et al. / Materials and Design 30 (2009) 3318–3324 3319

3. lips), Energy Dispersive Spectroscopy (EDS), X-ray Diffraction
(XRD, Xpert-P3040, Philips) and Fourier-Transformed-Infrared
Spectroscopy (FT-IR). In the aim to determine Ca and P ion concen-
tration, the remaining SBF solutions were analyzed by Inductively
Coupled Plasma Atomic Emission Spectroscopy (ICP-AES, FMO-
02M, Spectroflame).
Fig. 3. SEM and EDS analysis of the cements before immersion in SBF.
3320 D. Rentería-Zamarrón et al. / Materials and Design 30 (2009) 3318–3324

4. 3. Results and discussion
Table 3 shows the setting and doughing times of the W/PMMA
cements and the maximum temperature reached during polymer-
ization. When the highest content of wollastonite was added (sam-
ple W-97), the doughing and setting times were over 20 min, while
those corresponding to the wollastonite-free sample (W-O) were
10.33 and 7 min, respectively. Generally, these working times de-
creased as the ceramic content was increased up to 49 wt%. Thus,
the handling properties of samples W-19, W-39 and W-49 are sim-
ilar. As expected, the samples with more than 50 wt% of wollaston-
ite took longer time for setting due to the low content of PMMA
beads in the formulation.
The maximum temperature reached during setting decreased
considerably as the ceramic content was increased. According to
the literature [15], the ceramic present in the organic cements ab-
sorbs part of the heat produced by the exothermic polymerization
reaction. This decrease in the polymerization temperature will
potentially reduce the tissue damage when implanted.
Fig. 1 shows the compressive strength of the PMMA cements as
a function of the ceramic content. As observed, the strength de-
creased as the wollastonite content was increased up to 68 wt%,
where a value of about 40 MPa was obtained. The sample W-97,
which has the highest content of wollastonite, shows an appropri-
ate strength however, its setting time is extremely long (more than
20 min). According to the ASTM F-451, a minimum value of 70 MPa
is required for bone cements, thus only W-19 and W-39 (19 and
39 wt% of wollastonite) meet this mechanical requirement.
Fig. 2 shows the XRD patterns of the cements before immersion
in SBF. In all the cases, wollastonite and an amorphous phase were
detected. The amorphous phase may correspond to PMMA, since
the sample identified as W-19, which has the highest content of
this polymer, shows an amorphous halo of higher intensity. The
sample with no PMMA added (W-97) shows a small amorphous
halo due to the liquid content (mainly MMA).
Fig. 3 shows SEM images and the corresponding EDS spectra of
the samples before immersion in SBF. As corroborated by the EDS
spectrum, which shows the presence of Ca and Si, the sample W-97
consists mainly of wollastonite particles. The rest of the samples
consist of polymer beads surrounded by wollastonite particles.
The presence of C is due to the monomer added in this formulation.
Fig. 4 shows the FT-IR spectra of the W/PMMA samples before
immersion in SBF. The functional groups described in Table 4 are
present in all the samples, these groups correspond to both wollas-
tonite and PMMA.
Fig. 5 shows the XRD patterns of the samples identified as W-39
and W-49 after 21 days of immersion in SBF. As observed, apatite
was formed on the surface of these samples. This indicates the fea-
sibility to obtain potential bioactive materials by adding wollas-
tonite to PMMA before mixing this polymer with the liquid
phase (MMA + DMPT). No apatite was detected by XRD on the rest
of the samples (W-97, W-68 and W-19) after 21 days of immersion
in SBF. A high bioactivity of W-97 and W-68 was expected due to
the high content of wollastonite ceramics (97 and 68 wt%, respec-
tively). It seems that a higher content of PMMA is required to pro-
mote polymerization and to avoid the encapsulation of the ceramic
particles in MMA, which inhibits bioactivity.
Fig. 6 shows the SEM images and corresponding EDS spectra of
the W/PMMA specimens after 21 days of immersion in SBF. A thick
and homogenous ceramic layer, constituted by small Ca, P-rich
agglomerates was formed on the samples W-49 and W-39. Similar
results were observed on the unpolished samples. The Ca, P-rich
layer was the one identified as apatite by XRD (Fig. 5). After
21 days of immersion the elements corresponding to the sub-
strates (W-49 and W-39) were no longer detected by EDS. The
Fig. 4. FT-IR spectra of the W/PMMA cements.
Table 4
Functional groups present in the spectra shown in Fig. 4.
Wavenumber (cmÀ1
) Functional group
(1) 3000–3500 @CH–NH2
(2) 2300–3000 Methacrylamide
(3) 1742 Carbonyl C@O
(4) 1491 a-Methyl (CH3)
(5) 1281 a-Methyl (CH3)
(6) 1205 CH chain
(7) 998 RHC@CH2
(8) 700–1200 Si–O
(9) 576 CH3 + CH
(10) 550 C–O
Fig. 5. XRD patterns of the samples after 21 days of immersion in SBF.
D. Rentería-Zamarrón et al. / Materials and Design 30 (2009) 3318–3324 3321

5. Ca/P atomic ratio of the layers formed on these samples was calcu-
lated from the EDS results and this value was 1.65 for the layer
formed on W-49 and 1.56 for that one formed on W-49. These val-
ues are close to the Ca/P ratio of hydroxyapatite (1.67). On the W-
97 and W-68 samples a Ca, P-rich layer was also detected by SEM
and EDS however, this layer was not completely covering the sub-
Fig. 6. SEM images and EDS spectra of the samples after 21 days of immersion in SBF.
3322 D. Rentería-Zamarrón et al. / Materials and Design 30 (2009) 3318–3324

6. strate, which explains the reason for not detecting this layer by
XRD. Larger agglomerates were formed on the W-97 and W-68
samples in comparison to those formed on W-49 and W-39. The
quantity of wollastonite added to the sample W-19 (19 wt%) was
not enough to promote the formation of the Ca, P-rich agglomer-
ates on this sample.
Fig. 7 shows the FT-IR spectra of the samples W-39 and W-49
after 21 days of immersion in SBF. These spectra are similar to
those of the samples before immersion (Fig. 4 and Table 4), func-
tional groups corresponding to PMMA and wollastonite were de-
tected. Furthermore, in the spectra of W-39 and W-49, a new
band appeared at 940–1080 cmÀ1
, corresponding to P–O vibration
mode. The results obtained by FT-IR are in good agreement with
those of XRD, SEM and EDS analysis. No a significant change was
observed on the rest of the samples by using FT-IR.
Fig. 8 shows the change in concentrations in Ca and P in the SBF
with the immersion time. The Ca concentration increases slightly
during the first 7 days of immersion. According to the literature,
the apatite formation is mainly due to the Ca2+
ions released into
the SBF from the wollastonite leading to the increase of the super-
saturation degree of the fluid with respect to apatite by increasing
pH [16]. After 7 days of immersion, the Ca concentration in SBF de-
creases due to the formation of apatite on the samples and this de-
crease is greater for the W-49 sample, which has a higher
wollastonite content (49 wt%) than W-39 (39 wt%). This may indi-
cate that the in vitro bioactivity of W-49 is higher than that of W-
39. The P concentration decreases considerably in the SBF solutions
corresponding to both of the samples due to the incorporation of
this element in the apatitic structure.
According to the results obtained, the sample W-19 (19.4 wt% of
wollastonite + 77.7 wt% of PMMA) is not bioactive. The behavior
observed during the characterization of the sample W-19 may be
due to the low content of wollastonite and the high content of
PMMA, being the polymer an inhibitor of bioactivity. By adding
more than 20 wt% of wollastonite, highly bioactive cements are ob-
tained. However, by increasing the wollastonite content in the
monomeric samples (W-97, 97 wt% of wollastonite + MMA, with-
out adding PMMA beads) a slightly bioactive behavior was ob-
served. This may be explained taking into account the long
setting time measured in this sample (longer than 20 min). Poly-
merization of this sample may not be complete, leading to mono-
mer-free wollastonite particles that promote a slight bioactivity.
4. Conclusions
Potential bioactive PMMA cements can be obtained by adding
more than 20 wt% of wollastonite ceramics. A higher bioactivity
was observed on cements formulated with 39 and 49 wt% of cera-
mic (W-39 and W-49, respectively). After 21 days of immersion in
SBF a homogeneous and thick apatite layer was observed on the
samples W-39 and W-49, while the Ca, P-rich agglomerates ob-
served by SEM and EDS on the samples containing 68 and
97 wt% of wollastonite (W-68 and W-97, respectively) were not
detected by XRD.
The handling behavior of the highly bioactive cements (W-39
and W-49) is similar: the doughing time was between 3 and
4 min and the setting time was about 7 min. In comparison with
the wollastonite-free cement, the doughing and setting time de-
creased as the wollastonite content was increased up to 49 wt%.
At higher ceramic content (68 and 97 wt%), these times increase
considerably.
The temperature reached by the cement mixtures during poly-
merization and the compressive strength of the hard cements de-
creased substantially as the wollastonite content was increased.
Among the formulations prepared in this work, the cement with
39 wt% of wollastonite showed both bioactivity and appropriate
compressive strength. A further research needs to be performed
by varying the powder-to-liquid ratio, however the results ob-
tained in this work indicate that wollastonite can be used for
obtaining bioactive PMMA bone cements.
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