Journal of Medical and Bioengineering Vol. 6, No.

1, June 2017

Synthesis of a Bone Like Composite Material

Dderived from Natural Pearl Oyster Shells for
Potential Tissue Bioengineering Applications
Ravi Krishna Brundavanam, Derek Fawcett, and Gérrard Eddy Jai Poinern
Murdoch Applied Nanotechnology Research Group, Department of Physics, Energy Studies and Nanotechnolog,
School of Engineering and Energy, Murdoch University, Murdoch, Western Australia 6150, Australia
Email: [email protected], {d.fawcett, g.poinern}@murdoch.edu.au

Abstract—Hydroxyapatite is generally considered a viable been improved by combining it with other materials. For
substitute for bone in a number of medical and dental example, materials such as high density polyethylene and
procedures such as bone repair, bone augmentation and polypropylene have been successfully combined with
coating metal implants. Unfortunately, hydroxyapatites HAP to improve its load bearing capabilities [5], [6].
poor mechanical properties make it unsuitable for many Alternatively, other researchers have gone back to
load bearing applications. In this work various grades of
nature to look for a more effective ways of producing
finely crushed Pinctada maxima (pearl oyster shell) were
combined with a nanometre scale hydroxyapatite powder to biosynthetic materials and composites for potential tissue
form novel composite materials. A comparative study was engineering applications. Seashells are naturally
made between the various powder based composites occurring ceramic composites that are dense, hard, and
synthesized. The crystalline structure and morphology of remarkably robust. The shell structure has a number of
the various powder based composites were investigated highly desirable mechanical properties that enable it to
using X-ray diffraction and field emission scanning electron protect the soft body of the animal against environmental
microscopy. Also examined was a number of techniques for damage and predators. Shells are brittle or quasi-brittle
depositing hydroxyapatite directly onto oyster shell materials composed of mineral components (~95%) and
substrates. 
proteins (~5%). It is this compositional blend that gives a
shell its high degree of stiffness and hardness. However,
Index Terms—nano-hydroxyapatite, biocompatible,
ultrasonic irradiation, oyster shells
it is shell toughness and its ability to resist crack
propagation that has attracted considerable interest [7],
[8]. This interest stems from the observation that shell
I. INTRODUCTION fracture toughness can be two to three orders of
magnitude greater than the toughness of individual shell
The human skeletal system is essential for support and components [9], [10]. Another interesting feature is the
movement of the body. An important structural material much larger mechanical strain shells have at failure
forming the skeletal system is an organic-inorganic compared to manmade ceramics [8].
composite called bone. This natural composite is Nacre is the inner iridescent layer found in Pinctada
composed of proteins in the form of collagen fibrils and maxima (pearl oyster shell) and similar shells such as
macromolecules like proteoglycans that are all embedded abalone. Nacre is composed of a crystalline CaCO3
in a well arrayed inorganic crystalline hydroxyapatite mineral phase (aragonite) suspended in an organic matrix.
(HAP) matrix [1, 2]. It is this remarkable combination The aragonite is in the form of polygon shaped tablets
and distribution of constituent materials that gives bone ranging in size from 5 to15 µm in diameter and 0.5 to 1
its unique mechanical properties and its ability to µm in thickness that are stacked into a three dimensional
withstand various mechanical and structural loads brick wall-like structure. The wall-like structures can
encountered during daily physical activity. HAP is a consist of columns or sheets depending on the species and
mineral composed of calcium and phosphate ions and has typically forms 95% of the composite. Pearl oyster shells
the general formula of [Ca10 (OH)2 (PO4)6]. The close have a sheet-like structure. Recent atomic force
chemical similarity between synthetic HAP and HAP microscopy studies have shown the individual tablets are
naturally found in bone has led to an extensive research suspended in an organic matrix of proteins and
effort focused on using synthetic HAP as a viable bone polysaccharides. The organic matrix makes up the
replacement material in a number of clinical procedures remaining 5% of the composite [11], [12]. Besides the
[3], [4]. Unfortunately, due to HAPs low mechanical highly advantageous mechanical properties, the nacre is
strength its use has been restricted to low load bearing biologically compatible with bone tissues [13], [14].
applications. In a number of cases, its deficiencies have Because of the promising mechanical and
biocompatibility properties, nacre is a prime candidate for
Manuscript received August 26, 2016; revised March 15, 2017. potential tissue engineering applications. For example,

©2017 Journal of Medical and Bioengineering 29

doi: 10.18178/jomb.6.1.29-34
 Journal of Medical and Bioengineering Vol. 6, No. 1, June 2017

recent animal in vivo studies by Berland et al. have shown

good cellular interaction between nacre implants and
bone forming cells [15]. From another perspective,
Vecchio et al. have been able to converted Strombus
gigas (conch) and Tridacna gigas (Giant clam) shells to
HAP while preserving their original dense columnar
structure [16].
This article reports on the use of HAP and CaCO 3
derived from oyster shells to form novel HAP/CaCO 3
composites and HAP surface coatings on nacre. The first
part of the article reports on the crystalline structure and
morphology of synthesized nanometre scale HAP
powders. The second part examines the use of shell
derived CaCO3 that still retains properties of the shell to
manufacture HAP/CaCO3 composites. And thirdly, we
report on the use of HAP surface coating on nacre
substrates to improve biocompatibility and overcome
poor mechanical properties inherent with pure HAP
constructs.

II. MATERIALS AND METHODS

Figure 1. Schematic of synthesis process for producing HAP and
HAP/CaCO3 composites.
A. Materials
All chemicals used in this work were supplied by
Chem-Supply (Australia) and all aqueous solutions were C. Preparation of HAP Based Calcium Carbonate
made using Milli-Q® water (18.3 M cm-1) produced by Composite Powders
an ultrapure water system (Barnstead Ultrapure Water CaCO3 was derived from Pinctada Maxima (pearl
System D11931; Thermo Scientific, Dubuque, IA). oyster) shells. The shells were first washed and scrubbed
Pinctada Maxima (pearl oyster) shells were supplied raw to removal all traces of organic matter. This was followed
and were prepared as specified in section 2.3. by giving the shells a final wash down using Milli-Q®
water and then allowing them to air dry before being
B. Preparation of Nanometre Scale HAP Powders stored for the next stage of process. Shell material was
A detailed description of the HAP synthesis process used in two forms. In the first form shells underwent
developed by the authors can be found in the literature milling to produce CaCO3 powders of varying grades. A
[17, 18]. For completeness, a brief procedural description metallurgical ring crusher was used to crush and grind the
is outlined as follows. The procedure begins by first shells into a powder. After grinding, a Roto-Tap was used
adding a 40 mL solution of 0.32 M calcium nitrate tetra- for 30 minute to sieve the powder. Sieving produce a
hydrate into a small glass beaker and then adjusting the variety of powder grades ranging from 38 to 850
solution pH to 9.0 using approximately 2.5 mL of micrometers as seen in Fig. 2. In the second form shells
ammonium hydroxide. The solution is then sonicated were cut into 1 cm2 test substrates.
using a Hielscher Ultrasound Processor UP50H set at 50 Preparation of the HAP/CaCO3 composites started by
W and maximum amplitude for 1 h. During a second hour selecting the appropriate CaCO3 grade and then weighing
of sonication 60 mL of 0.19 M potassium di-hydrogen out the required mass. In this case the mass percentages
phosphate solution was slowly added while the solution of CaCO3 selected were 5% and 10%, with the remaining
pH was maintained at 9.0 and the Calcium/Phosphate mass balance made up of HAP powder. However, before
[Ca/P] ratio was maintained at 1.67. At the end of the being incorporated into the HAP synthesis process the
second sonication period, the solution was centrifuged CaCO3 powders were bleached for 30 minutes. The
(15,000 g) for 20 minutes at room temperature to produce
bleached CaCO3 was then added to the HAP processing
a precipitate. The precipitate was collected, washed and
procedure to produce the required blend as seen in Fig. 1.
centrifuged for a further 10 minutes before being placed
Visual inspection during processing and after heat
into a ceramic boat ready for heat treatment. The heat
treatment consisted of placing a sample loaded ceramic treatment revealed a noticeable difference between pure
boat into an electric tube furnace. The reaction HAP powders, pure CaCO3 powders and the respective
temperatures used were either 300oC or 400oC and the HAP/CaCO3 powder blends. However, differences
reaction time period was 2 hours for temperatures. After between the 5% and 10% CaCO3 blends were much
thermal treatment, the agglomerated samples were milled harder to distinguish and could only be differentiated
to form an ultrafine HAP powder. A schematic of the under electron microscopy. Fig. 3 presents a
synthesis process is presented in Fig. 1. representative image of a 10% CaCO3 blend.

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 Journal of Medical and Bioengineering Vol. 6, No. 1, June 2017

TABLE I. SUBSTRATE SURFACE PRE-TREATMENTS USED PRIOR TO

COATING APPLICATION.
Substrate Surface Description
Type Treatment
1 None Sample is cleaned using Milli-Q®
(Control) water and then air dried.
2 Chemical Sample is placed into a 500 ml
Hydrochloric beaker containing 200 ml of
Acid (HCl) Milli-Q® water and 10 ml of 35%
HCL. Solution pH was measured
and found to be 1. The sample
remains in the solution for 3
minutes. It is then removed and
washed with Milli-Q® water and
air dried.
3 Chemical Sample is place into a 500 ml
Figure 2. (a) Pinctada Maxima (pearl oyster) shells and (b) Various Sodium beaker containing 200 ml of
grades produced after sieving CaCO3 powder (38 to 850 micrometers). Hypochlorate household bleach. (45g/l of
(SH) sodium hypochlorate). The
sample remains in the solution
D. Preparation of Shell Substrates
for 30 minutes. It is then
The second part of the study used the shell as a removed and washed with Milli-
substrate for the deposition of a HAP coating. The Q® water and then air dried.
substrates were prepared by first pre-washing and 4 Boiling (B) Sample is place into a 500 ml
cleaning the raw shells. After cleaning the shells were beaker containing 200 ml of
placed in a clean bench vice and cut into 1 cm2 test Milli-Q® water and boiled for 10
substrates using a standard hacksaw (32 teeth per 25 mm). minutes. It was then removed and
Substrates were then washed in running water in the lab washed with Milli-Q® water and
then air dried.
sink to remove all cutting debris. In the next stage of
5 Mechanical Sample is roughened using
cleaning samples were placed into a 250 ml beaker of
Abrasion (A) silicon carbide sand paper
Milli-Q® water then exposed to ultrasonic irradiation for (180p). 15 lateral movements
10 minutes to remove any loose particles that may have followed by 15 vertical
been embedded in the samples during the cutting stage. movements. The sample was then
After the first irradiation, the Milli-Q® water was changed placed into a 500 ml beaker
and the process repeated. In total, the samples were containing 200 ml of Milli-Q®
treated three times before being air dried and stored ready water and exposed to 5 minutes
for surface treatment. of ultrasonic irradiation to
remove any loose particles and
contamination from the sand
paper. The sample was then air
dried.
6 Mechanical Sample is placed into a bench
(S) vice. The sample is scored by 20
lateral movements (both
directions) by a surgical scalpel.
The sample was then placed into
a 500 ml beaker containing 200
ml of Milli-Q® water and
exposed to 5 minutes of
ultrasonic irradiation to remove
any loose particles. The sample
was then air dried.
Figure 3. Figure 3 Representative electron microscopy image of
HAP/CaCO3 powder blend. The surface coating procedure consisted of using a
spatula to evenly spread a layer of HAP powder over the
surface of sample types 2 to 6, sample 1 being the
E. Subrate Surface Treatments and Coatings unloaded control sample. After coating, all samples were
A specific surface pre-treatment was applied to each placed into ceramic furnace boats and then individually
respective substrate prior to coating. This was done to placed into a pre-heated furnace set to 400oC. Samples
gauge the effectiveness of each surface pre-treatment in remained in the furnace for 2 hours to calcify the coating
promoting coating attachment. Five pre-treatment in the presence of atmospheric air. After 2 hours of
procedures and an untreated substrate (control) were thermal treatment, the ceramic boats were removed from
investigated and details of each pre-treatment are the furnace and allowed to cool down to room
presented in Table I. temperature in air.

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 Journal of Medical and Bioengineering Vol. 6, No. 1, June 2017

F. Advanced Characterisation where, λ is the wavelength of the monochromatic X-

Powder X-ray diffraction (XRD) spectroscopy was ray beam, B is the Full Width at Half Maximum (FWHM)
used to identify the crystalline size and phases present in of the peak at the maximum intensity, θ(hkl) is the peak
synthesized HAP powders. Spectroscopy data was diffraction angle that satisfies Bragg’s law for the (h k l)
plane and t(hkl) is the crystallite size. The crystallite size of
recorded at room temperature, using a Siemens D500
each sample was calculated from the (002) reflection
series diffractometer [Cu Kα = 1.5406 Å radiation source]
peak. HAP samples thermally treated at 400 ºC gave a
operating at 40 kV and 30 mA. The diffraction patterns
mean particle size of 30 nm.
were collected over a 2θ range of 20° to 60° with an
incremental step size of 0.04°using flat plane geometry B. FESEM Analysis of Pure and Blended Powders
with a 2 second acquisition time for each scan. The FESEM was used to study particle size and
crystalline size of the particles was calculated using the morphology of the pure powders and blended powders.
Debye-Scherrer equation [Equation 1] from the Representative micrographs of the synthesized powders
respective spectroscopy patterns. Field emission scanning are presented in Fig. 5 (a) to (d). Fig. 5 (b) reveals a
electron microscopy (FESEM) was also used to study spherical/granular particle morphology that is highly
size, shape and morphological features of the various agglomerated and is typical of the synthesised HAP
powders. All micrographs were taken using a high powder samples. Also present in Fig. 5 (b) are three 50
resolution FESEM [Zeiss 1555 VP-FESEM] at 3 kV with nm diameter circles placed randomly to highlight the
a 30 µm aperture operating under a pressure of 1.33310- spherical/granular morphology. This morphology is
10
mbar. Samples were mounted on individual substrate similar to particle morphologies previously reported in
holders using carbon adhesive tape before being sputter the literature [21-22].
coated with a 2 nm layer of gold to prevent charge build
up using a Cressington 208HR High Resolution Sputter
coater.

III. RESULTS AND DISCUSSIONS

A. XRD Spectroscopy Analysis of Synthesised HAP

Powders
XRD spectroscopy was used to identify the crystalline
size of the synthesised nanometre scale HAP powders. A
representative XRD pattern of a thermally treated HAP
powder (400 ºC for 2 h) is presented in Fig. 4. The
pattern shows the main (h k l) indices found in the sample,
namely (002), (211), (112), (300), (202), (310), (222), Figure 5. (a) Milled CaCO3 powder sifted through a 38 micron sieve;
(213) and (004). These indices match the known phases (b) Pure ultrafine HAP powder; (c) HAP/CaCO3 composite (5% CaCO3
present in pure HAP and are consistent with the phases and particle sizes less than 38 micron) and (d) HAP/CaCO3 composite
(10 % CaCO3 particle graded between 38 and 75 microns).
listed in the ICDD database.
The raw CaCO3 powder was sifted through a 38
micron sieve to produce a relatively homogeneous
powder consisting of thin plates and finer granular shaped
particles ranging in size from 20 to 100 nm as seen in Fig.
5 (a). A representative micrograph of a HAP/CaCO 3
composite (5%) is presented in Fig. 5 (c) and reveals the
presence of granular shaped particles with pronounced
edges that appear to be moderately packed and range in
size from 50 to 100 nm. This is in stark contrast to the
smooth and spherical HAP particle morphologies seen in
Fig. 5 (b). Fig. 5 (d) presents a representative micrograph
Figure 4. Representative XRD pattern of a HAP powder after thermal
treatment. of a HAP/CaCO3 (10%) and also reveals the presence of
tightly packed granular particles. The particles range in
The crystalline size, t (hkl), of each sample was size from 50 to 100 nm and have similar morphology to
calculated from the respective XRD patterns using the particles seen in the HAP/CaCO3 (5%) composite.
Debye-Scherrer equation [19], [20]. Analysis of FESEM micrographs taken of composite
samples has confirmed the influence of CaCO3 on particle
0.9
t ( hkl)  (1) morphology during the synthesis of the HAP composites.
B cos θ ( hkl)

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 Journal of Medical and Bioengineering Vol. 6, No. 1, June 2017

C. Surface Pre-Treatments and Coating Attachment coverage with large areas of underlining substrate clearly
The results of HAP deposition revealed some visible. However, further investigation is needed to fully
interesting surface features on the various substrates after investigate the effects of surface texturing, and in
thermal treatment. Initial inspection revealed lamellae particular the effects of surface texturing before
from the inner white layers of the substrate had bubbled chemically treating the substrates with bleach. Bleaching
and broken away during calcification in the furnace. substrates using the Type 3 (SH) method has proven to
Substrate Type 1 (control) showed signs of surface produce a superior HAP surface coating compared to
bubbling and still retained its pearlescent lustre. The other methods tested in this study. Future studies are
remaining 5 substrate types all exhibited a dull white planned to investigate the wear properties and load
coating that indicated HAP had adhered to the respective bearing capacity of the Type 3 (SH) substrates. In
surfaces. Substrate Type 2 (HCl) showed signs of minor addition, in vitro studies are also planned to investigate
delaminating and on the whole HAP had adhered to the the biocompatibility of the substrates towards a number
surface. Type 3 (SH) that had involved a bleaching of bone cell lines.
process showed the most significant change. The surface
had a distinctive white appearance with a significantly
thicker and denser HAP coating compared to the other
substrate types. Type 4 (B) that had involved a boiling
treatment showed significant lamellae delaminating and
also produced very brittle substrates. Overall, Type 4
produced poor quality substrates that were unsuitable for
any tissue engineering applications. Both Type 5 (A) and
Type 6 (S) revealed significant amounts of HAP had been
trapped within the rough surface features created by the
respective surface treatments. Surface scoring used in
Type 6 trapped the largest amounts of HAP within the
surface features and significantly contributed to coating
integrity. Generally, both surface texturing techniques
were found to be beneficial in promoting surface fixation
of the coatings. Figure 6. FESEM analysis of various substrate surfaces: (a) Substrate
Type 1 (Control) showing the deposition of HAP particles during the
Subsequent FESEM surface studies of the various calcination process; (b) Type 2 (HCl) showing minor delaminating of
substrate types revealed some interesting surface features. the thin HAP coating; (c) Type 2 (HCl) enlarged view of coating with
In the case of Type 1 (control) there was tracing of HAP underlying lamellae exposed, and (d) Type 3 (SH) substrate showing an
evenly distributed thick coating over the entire substrate surface with far
found, even though there was no HAP coating applied to fewer exposed lamellae regions.
the surface. The presence of distinct HAP particles over
the entire face of the control substrate was found to be the
result of ongoing calcification processes occurring within IV. CONCLUSION
the furnace environment as seen in Fig. 6 (a). Both water
and NH4 evaporating from surrounding substrates tended HAP is a calcium phosphate that is considered to be a
to be deposit on everything within the furnace. Only Type viable replacement for bone material in a number of low-
1 substrate showed this type of surface feature. Type 2 load bearing tissue engineering applications. While the
(HCl) substrate had a thick surface covering, nacre layer found inside the Pinctada maxima (pearl
unfortunately the coating was not uniformly distributed oyster) shell is hard, stiff, and extremely tough. The
over the entire surface. There were numerous regions present study has shown that a nanometre scale HAP
were the underlying lamellae structure could be seen as powder (mean particle size of 30 nm) can be combined
shown in Fig. 6 (b). Type 3 (SH) substrates were covered with sieved powders derived from Pinctada maxima
with a thick and dense white surface coating that was (CaCO3) to produce a composite powder. During
evenly distributed over the entire surface. Unlike Type 2, synthesis, the addition of sieved powders were found to
Type 3 substrates had a superior surface coverage with influence particle size and morphology of composite
far fewer exposed underlining lamellae regions. Overall, powders. The tough nacre was used as a substrate and a
FESEM analysis found HAP coating preferred to deposit number of surface pre-treatments were investigated
and attach to the bleached surfaces of Type 3 substrates before the substrates were coated with HAP. The results
than those of the acid treated surfaces of Type 2 as seen of the investigation revealed a substrate pre-treated with
in Fig. 6 (c) and 6 (d). In both cases, the mean HAP sodium hypochlorate (Type 3) before HAP deposition
particle size for both substrate types determined from produced the superior coating. The surface coating was
FESEM analysis was found to be 500 nm. The surface thick, dense and evenly distributed. However, further
coverage on substrate types 5 and 6 were not thick or studies are needed to investigate wear properties and load
uniformly distributed. Instead they tended to accumulate bearing capacities of the Type 3 substrate. Future in vitro
HAP within and around the roughened surface features. studies are planned to determine the biocompatibility of
On the whole, both substrate types had surfaces with poor the substrates towards a number of bone cell lines.

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 Journal of Medical and Bioengineering Vol. 6, No. 1, June 2017

[16] K. S. Vecchio, X. Zhang, J. B. Massie, M. Wang, and C. W. Kim,

“Conversion of bulk seashells to biocompatible hydroxyapatite for
ACKNOWLEDGEMENTS bone implants,” Acta Biomaterialia, vol. 3, pp. 910-918, 2007.
The authors would like to thank Dr Xuan Le for her [17] G. E. J. Poinern, R. Brundavanam, X. Le, S. Djordjevic, M. Prokic,
and D. Fawcett, “Thermal and ultrasonic influence in the
assistance with FESEM analysis. formation of nanometer scale hydroxyapatite bio-ceramic,”
International Journal of Nanomedicine, vol. 6, pp. 2083-2095,
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