Engineering, 2010, 2, 344-352
doi:10.4236/eng.2010.25045 Published Online May 2010 (
Copyright © 2010 SciRes. ENG
Engineering of Carbonate Apatite Bone Substitute
Based on Composition-Transformation of
Gypsum and Calcium Hydroxide
Ika Dewi Ana1, Shigeki Matsuya2, Kunio Ishikawa3
1Department of Dental Biomedical Sciences, Faculty of Dentistry,
Gadjah Mada University, Yogyakarta, Indonesia
2Section of Bioengineering, Department of Dental Engineering, Fukuoka Dental College, Fukuoka, Japan
3Department of Biomaterials, Faculty of Dental Science, Kyushu University, Fukuoka, Japan
Received November 29, 2009; revised February 7, 2010; accepted February 12, 2010
Even though a lot of research has been carried out concerning the preparation of carbonate apatite (CHA),
they were related to CHA in the form of powder. In the present study, macroporous CHA bone substitutes
were prepared through composition-transformation of gypsum and Ca-hydroxide. Here, we investigated the
effect of added Ca-hydroxide to gypsum, carbonation periods, and hydrothermal temperatures for phos-
phatization to understand the basic principle of composition-transformation of gypsum added Ca-hydroxide
to fabricate CHA bone substitutes. The specimens were characterized in terms of chemical and physical
properties, such as extent of transformation of macroporous gypsum added Ca-hydroxide into CHA body,
type and content of carbonate, and crystal morphology. It was observed that the transformation was faster
with higher hydrothermal temperature. However, higher hydrothermal temperature caused de-carbonation
phenomena which resulted in the lack of carbonate ions of the product. Moreover, the higher the percentage
of Ca-hydroxide added to gypsum, caused the complete transformation of gypsum into CHA to be slower.
These findings have been applied to the standard fabrication procedure of carbonate apatite, which in turn
will allow scaling up process, and will be provided for biomedical purposes for the Indonesian community.
Keywords: Carbonate Apatite (CHA), Bone Substitute, Composition-Transformation, Gypsum, Calcium Hydroxide
1. Introduction
Bone tissue is one of the most frequently used tissues for
transplantation. Annually more than a million patients
are treated worldwide for skeletal problems in the field
of orthopedic surgery, plastic surgery, maxillofacial sur-
gery, and neurosurgery. The use of autologous bone
grafts is still considered to be the golden standard, but
there are several major disadvantages in this technique,
for example: 1) low availability of transplantable tissue,
2) postoperative morbidity, and 3) lack of functional
shape of the transplant. Meanwhile, despite four decades
of the researches to provide synthetic bone substituting
materials, the engineered bone-substituting materials are
still largely inferior to auto- or allografts as the golden
standard. The clinical success of the current generation
of bone-substituting materials is disappointingly limited
since they lack the high functionality of bone tissue in
terms of biological and mechanical properties [1]. This
lack of biofunctionality is related mainly to an engineer-
ing attitude towards design of novel biomaterials that
lacks a biological mindset [2,3]. Therefore, the develop-
ment of alternatives to autologous bone is a very relevant
engineering issue in bone reconstructive surgery.
To provide the answer to the issue, the basic knowl-
edge on the composition of human bone mineral must be
understood. In view of this, it is known from the current
studies that the mineral phase of human hard tissue con-
sists of hydroxyapatite (HA: Ca10(PO4)6(OH)2) contain-
ing a variety of impurity ions such as carbonate, sodium,
and magnesium, etc. [4-8]. Carbonate is one of the most
abundant impurity ions and its content is about wt 4-8%
[9-11]. In this sense, hard tissue is regarded as carbon-
ate-substituted HA (CHA).
I. D. ANA ET AL.345
It has been reported that synthetic CHA revealed the
biological activity better than synthetic HA because the
incorporation of carbonate into HA caused an increase in
solubility, a decrease in crystallinity, a change in crystal
morphology, and an enhancement of chemical reactivity
owing to the weak bonding [5,12,13]. In this context,
CHA is actually more soluble in vivo than HA and in-
creases the local concentration of calcium and phosphate
ions that are necessary for new bone formation [14-16].
For these reasons, recent studies have focused on CHA
in comparison with HA.
Even though a lot of research has been carried out
concerning the preparation of CHA, they were related to
CHA in the form of powder [10,12,17-19]. In the present
study, macroporous CHA bone substitutes were prepared
through composition-transformation of gypsum and Ca-
hydroxide, the abundant minerals in Indonesia. The suc-
cessful composition-transformation process will allow the
modification of the macroporous CHA body to provide
bone-substitutes with proper mechanical and biological
properties, based on the needs of reconstructive surgeon.
The specimens were characterized in terms of chemical
and physical properties, such as extent of transformation
of CaCO3 body into CHA body, type and content of car-
bonate, and crystal morphology.
This research was also basically directed to find a low
cost technology and environmental friendly method to
prepare CHA bone substitutes. Its aim is to provide
lower cost bone substitutes for the Indonesian market to
help the people improve their quality of life. Many re-
lated cases showed low access to bone-substitution
treatment due to the high cost of medical treatment in
which it needs engineering approach to solve the prob-
2. Materials and Method
2.1. Composite Preparation
Calcium sulphate hemihydrate (CaSO4.1/2H2O) of Wako
Pure Chemical (Japan) was added by 20, 40, 50, and 100
weight% of Calcium hydroxide (Ca(OH)2) of Nacalai
Tesque, Kyoto (Japan). The weight% of added Ca- hy-
droxide applied in this study was based on the prelimi-
nary studies done ranging from 0 to 100% Ca-hydroxide
additions. The gypsum added Ca-hydroxide powders
were used to prepare a monolith by mixing the powder
with water in 1:2 W/P. The mixture was put in a stainless
steel mold (6 mm in inner diameter by 3 mm thickness)
and pressed uniaxially at 10 MPa to prepare CaSO4/
Ca(OH)2 composite. The composite was then put into
37oC incubator with 80% humidity for 24 hour to allow
it to set completely.
2.2. Composite Carbonation
The composite was placed in carbon dioxide reaction
vessel for 72 hours at room temperature. The reaction
vessel (approximately 5L) was saturated with water va-
por and carbon dioxide gas was supplied at a rate of 0.15
to 0.20L/min.
2.3. Hydrothermal Treatment
The composite monolith was then treated hydrothermally
in 1M phosphate solutions at 60oC for various times,
ranging from 3 to 14 days. The phosphate used was
tri-sodium phosphate (Na3PO4.12H2O; Wako Chemicals,
Japan). Each monolith after the hydrothermal treatment
was washed with distilled water for 6h to eliminate solu-
ble ions.
2.4. X-Ray Diffraction Analysis
The purity and crystallite size of the CHA formed were
determined by XRD (RINT 2500V, Rigaku, Japan)
analysis. The XRD pattern was obtained in the range of
2h from 2 o of 10 to 60 in a continuous mode at a scan-
ning rate of 2o/min.
2.5. Fourier Transformed Infrared (FT-IR)
Infrared spectra between 400 and 4,000 cm–1 were re-
corded on the FT-IR spectrometer (Spectrum 2000,
Perkin-Elmer, USA) to examine structural changes by
the hydrothermal treatment, in particular, CO3
2– ions
substituting for PO4
3– and/or OH ions.
2.6. Scanning Electron Microscope (SEM)
The morphology of fracture surface and crystal shape
were observed by SEM (JSM 5400LV, JEOL, Japan) at
an acceleration voltage of 15kV after gold sputtering.
2.7. Chemical Analysis
Chemical analysis was also done to determine carbon
and nitrogen contents using CHN elemental analyzer
(CHN coder MT-6, Yanaco, Japan). Calcium and phos-
phorus content were determined by Ion-meter (TOA-
DKK Model IM-55G, TOA, Japan) and a spectrometer
(UV-Spectrometer, JASCO, Japan) respectively.
2.8. Mechanical Analysis
Diametral tensile strength of the composite monolith was
evaluated at a constant crosshead speed of 1mm/min on a
Copyright © 2010 SciRes. ENG
universal testing machine (SV-301, IMADA, Japan). For
each experimental condition ten specimens were tested.
3. Results and Discussion
3.1. X-Ray Diffraction Patterns
Figure 1 shows XRD patterns of gypsum added Ca- hy-
droxide composite after 72 hours carbonation. It was
detected that CaCO3 (calcite) peaks were developed by
carbonation regardless the percentage of Ca-hydroxide
addition, shown by the peak development at around 2 of
28.5o. However, the complete transformation into CaCO3
was faster in the monolith containing 100% Ca-hydroxide.
Other compositions (20, 40, and 50% addition) trans-
formed into biphasic DCPD/CaCO3 which was shown by
peaks (121) at around 2 of 21o, (141), (112) and (121) at
around 2 of 29 to 31o, and at around 2 of 34o for (022)
and (150).
It was also shown in the Figure 1 that the CaCO3 re-
sulted in the carbonation reaction has broader peaks than
the commercially available one, indicating that the crys-
tallite size of CaCO3 resulted by carbonation was much
smaller. Ca-hydroxide was completely transformed into
CaCO3 after 72 hours carbonation, in a single phase or in
the form of biphasic DCPD/CaCO3. Up to this reaction
stage, it is expected that the carbonation products will
show good tissue response to be applied for biomedical
purposes. This is due to the composition transformation
into low crystalline CaCO3 that has similar biological
properties with aragonite, which is the constituent of
marine coral [20]. In case of biphasic DCPD/CaCO3, it
was also reported that DCPD is considered to be HA
precursor [21].
Figure 2 shows XRD patterns of gypsum added Ca-
hydroxide after phosphatization by 1M Na3PO412H2O
for 7 days (a) and 14 days (b). Hydroxyapatite (HA)
phase was detected as a main reaction product regardless
of the percentage of Ca-hydroxide added into gypsum.
The composition transformations into HA phase were
marked by peaks development at around 2 of 25.5o and
32.5o. Meanwhile peaks at around 2 of 28.5o decreased
in their intensity. Transformation of CaCO3 or DCPD/
CaCO3 into HA is seemed to proceed faster by lower
concentration of added Ca(OH)2. In higher Ca-hydroxide
concentrations (50 and 100%), the CaCO3 peaks at
around 2 of 28.5o still remained high even after 14 days
hydrothermal treatment in phosphate solution. In the
lower concentrations of Ca-hydroxide (20 and 40%), the
CaCO3 peaks also remained although the intensity was
lower than those of with higher Ca-hydroxide concentra-
tions. This is probably due to high pH in Na3PO412H2O
solution, which resulted in the stabilization of CaCO3
compared with carbonate apatite [22,23]. Moreover in
the composition where CaCO3 remained, the peaks
around 2 of 32o were merged, showing different feature
with the composition without remaining CaCO3 (gypsum
without added Ca-hydroxide) where it was found clear
separation between (211) and (112) diffraction peaks.
Regarding the peak separation, LeGeros [24] observed
that the lattice parameter of a-axis in a hexagonal apatite
crystal decreased with the increasing CO3 content. In this
study, it was theoretically predicted that the more the
percentage of Ca-hydroxide added into gypsum, the
faster the composition transformation of the composite
into CaCO3 monolith after carbonation.
Figure 1. X-Ray diffraction patterns of gypsum added Ca-
hydroxide after 72 hours carbonation. Peak development at
around 2 of 28.5o was observed regardless the amount of
Ca-hydroxide additions. Another pattern shows diffraction
of DCPD and DCPA for comparison.
Copyright © 2010 SciRes. ENG
I. D. ANA ET AL.347
Figure 2. X-Ray diffraction patterns of gypsum added
Ca-hydroxide after 7 days (a) and 14 days (b) phosphatiza-
tion in 1M Na3PO412H2O.
Table 1 summarizes the qualitative analysis of XRD
showing the composition transformation after carbona-
tion and phosphatization.
3.2. FT-IR Spectra
Figure 3 shows the FT-IR spectra of the specimens after
carbonation and 7 days phosphatization. Although typi-
cal CO3
2- bands were detected between 1000 and 900 cm-1
and 1600 to 1400 cm-1 but the bands between 1600- 1400
cm-1 were broad indicating that the transformation into
CHA was not completed yet by 7 days process, irrespec-
tive of the percentage of Ca-hydroxide added into gyp-
sum. After carbonation and 7 days phoshatization, bands
around 1100 cm-1 were developed in all specimens, re-
gardless the amount of Ca-hydroxide added into gypsum.
These bands were correlated with PO4
3- of the typical
B-type CHA [15,25,26] but also A-type CHA indicated
by CO3
2- bands development at around 810-800 cm-1.
The higher the amount of Ca(OH)2 added, the more the
absorbance indicating CO3
2- bands at around 980-960
cm-1 was observed. The complete composition transfor-
mation into B-type CHA was detected by prolonging
phosphatization to 14 days as shown in the typical com-
position transformation process (Figure 4).
Figures 4 and 5 show the FT-IR spectra of the process
after carbonation, continued by 7 days phosphatization,
and 14 days phosphatization. After 14 days phosphatiza-
tion, the typical CO3
2- bands were developed at 1455-
1410 cm-1 and 880-860 cm-1 in which the absorbance
was higher by longer phosphatization period. On the
same figure, the typical PO4
3- bands were observed at
600-560, and 1100-960 cm-1 indicating the development
of B-type CHA. The PO4
3- band at around 600-560 was
well separated. The existence of carbonate ion bands in
the spectra shows the formation of CO3
2- substituted HA
(CHA). Elliot [23] in his explanation of the structure and
chemistry of apatites mentioned that B-type CHA shows
2- band at 1410 and 1455 cm-1 while A-type at about
1545 and 1455 cm-1. In the final reaction products, the
2- band appeared at around 1410 and 1455 cm-1.
Table 1. Qualitative analysis of XRD showing the composi-
tion transformation of gypsum added Ca-hydroxide after
carbonation and phosphatization in continuous treatment.
Content of
After 72 hours
After 7 days
After 14 days
(0% Ca(OH)2)
DCPD, Gyp-
sum Gypsum, CHA CHA
50% Ca(OH)2 DCPD, CaCO3CaCO3 CHA, CaCO3
100% Ca(OH)2CaCO3 CaCO3 CHA, CaCO3
Copyright © 2010 SciRes. ENG
This observation showed that the composition transfor-
mation reaction by carbonation and phosphatization re-
sulted in B-type CHA. Figure 5 show extended bands
found in the study. Landi et al. [18] reported that the
increasing of CO3
2- band at about 1545 and 1455 cm-1
caused by the migration of CO3
2- band at 1410 and 1455
cm-1 to OH- lattice site with heat treatment caused a de-
crease in crystallinity. The decrease in crystallinity at-
tributed to the ability of hydroxyl site to accept more
vacancies and the increasing degree of freedom of CO3
ion. Based on that phenomenon, in this study, lower
hydrothermal treatment (60oC) was applied after experi-
menting different temperatures ranging from 100 to 60oC
to allow formation of low crystalline B-type CHA. It was
observed that the longer the phosphatization period, the
lower the crystallinity obtained by composition trans-
formation of gypsum added Ca-hydroxide ended with
B-type CHA.
Table 2 summarizes the composition of CHA pre-
pared by composition transformation of gypsum added
Ca-hydroxide. The Ca/P molar ratio ranged between 1.53
to 2.01 molar ratio. Without Ca-hydroxide addition into
Figure 3. FT-IR spectra of the monoliths after 72 hours
carbonation and 7 days phosphatization, showing CHA
peaks development which was not completed.
Figure 4. FT-IR spectra of gypsum added 40 weight% Ca-
hydroxide after carbonation, continued by 7 days phos-
phatization, and prolonged up to 14 days phosphatization.
Table 2. Chemical composition of CHA prepared by com-
position transformation of gypsum added Ca-hydroxide.
Content of
(0% Ca(OH)2) 1.53±0.04 0.58 0.55
20% Ca(OH)2 1.71±0.02 3.36 0.47
40% Ca(OH)2 1.83±0.02 6.12 0.52
50% Ca(OH)2
100% Ca(OH)2
Table 3. Qualitative analysis on setting reaction on the
gypsum added Ca-hydroxide.
Content of Ca-hydroxide
(0% Ca(OH)2) Good
20% Ca(OH)2 Good
40% Ca(OH)2 Good
50% Ca(OH)2
100% Ca(OH)2
(Difficult to handle)
Very Poor
(Very difficult to handle)
Copyright © 2010 SciRes. ENG
Copyright © 2010 SciRes. ENG
Figure 5. Extended CO3
2- and PO4
3- bands of FT-IR spectra found by composition transformation reaction.
gypsum, the Ca/P ratio was slightly lower than that of
stoichiometric HA, that is 1.67, indicating that calcium
deficient apatite was formed. By addition of Ca-hydroxide
into gypsum followed by carbonation and phosphatization
treatment using Na3PO4.12H2O, the Ca/P ratio are 1.71,
1.83, 1.88, and 2.01 molar ratio for 20, 40, 50, and 100%
additions respectively. These results showed that by Ca-
hydroxide additions, PO4
3- was replaced by CO3
2- which
led to the formation of B-type CHA.
The CO3
2- content of the specimens ranging from 0.58
(for gypsum without Ca-hydroxide addition), 3.10, 3.27,
and 3.36 for 50, 100, and 20 weight% Ca-hydroxide ad-
ditions respectively, to 6.12 weight% (for the specimen
with 40 weight% Ca-hydroxide addition). Only by addi-
tion of 40 weight% Ca-hydroxide the carbonate content
resulted by composition transformation is on the range of
bone mineral, that is 4-8 weight% [9,10].
Figure 6 shows SEM photographs of CHA obtained in
various addition of Ca-hydroxide. Without addition of
Ca-hydroxide into gypsum, the CHA crystal showed a
needle like apatite morphology after carbonation and
phosphatization reaction (Figure 6(b)). By 20 weight%
addition of Ca-hydroxide into gypsum, the CHA resulted
both a needle like morphology and fine globular crystal
(Figure 6(d)). Increasing the amount of Ca-hydroxide
(to 40 and 50 weight%) added into gypsum resulted in
fine globule-like CHA crystals (Figure 6(f) and 6(h)).
Inter connective porosity is observed on the microstruc-
ture of the monoliths.
Figure 7 shows the changes in DTS (diametral tensile
strength) of the specimens. The mechanical strength in-
creased after carbonation and phosphatization reactions,
and the increased strength after carbonation and phos-
phatization was found 50% in pure set Ca-hydroxide,
25% in gypsum added by 20 or 40 weight% of Ca- hy-
droxide, 20% in gypsum added by 50 weight% of Ca-
hydroxide, and remained the same in the gypsum without
Ca-hydroxide addition. The difference in DTS is proba-
bly due to the crystallite size and shape of the specimens.
In this study, we investigated the effect of added Ca-
hydroxide to gypsum, carbonation and phosphatization
temperatures and periods to understand the basic princi-
ple of composition-transformation of gypsum added Ca-
hydroxide to fabricate carbonate apatite bone substitutes.
It was observed that faster transformation was achieved
with higher hydrothermal temperature. However, higher
hydrothermal temperature caused de-carbonation phe-
nomena which resulted in the lack of carbonate ions in
the product. Decreasing phosphatization temperatures
required longer reaction periods. Moreover, the higher
the percentage of Ca-hydroxide added to gypsum re-
sulted in slower complete transformation of gypsum into
CHA, indicated by remaining CaCO3 phase inside the
composition. These findings have been applied to the
standard fabrication procedure of carbonate apatite that is
provided for biomedical purposes in Indonesia. Cell
studies and in vivo animal studies are being carried out
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 6. Scanning electron microscopic observation of set gypsum, gypsum added Ca-hydroxide by 20, 40, and 50 weight%
before treatment (a, c, e, g) and after carbonation and phosphatization (b, d, f, h).
Copyright © 2010 SciRes. ENG
I. D. ANA ET AL.351
Figure 7. Changes in DTS (MPa) before and after carbona-
tion and phosphatization reactions.
in our laboratory. For the continuation of these studies, it
is suggested to start preliminary clinical trials, so as to
have an overview study to scale up fabrication, and to
precede valorization and actual bone substitute produc-
tion for the Indonesian market.
4. Acknowledgements
This study was a part of series of research collaboration
supported by first batch bilateral joint program JSPS-
DGHE (Japan Society for the Promotion of Science-
Directorate General of Higher Education of the Republic
of Indonesia).
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