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Effect of magnetite nanoparticles on the biological and mechanical properties

of hydroxyapatite porous scaffolds coated with ibuprofen drug

Article  in  Materials Science and Engineering C · March 2020

DOI: 10.1016/j.msec.2020.110835

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Materials Science & Engineering C

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Effect of magnetite nanoparticles on the biological and mechanical properties of
hydroxyapatite porous scaffolds coated with ibuprofen drug
Saeid Sahmani a , Amirsalar Khandan b ,⁎ , Saeed Saber-Samandari b , Mohammad Mohammadi Aghdam c

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a
School of Science and Technology, The University of Georgia, Tbilisi 0171, Georgia
b
New Technologies Research Center, Amirkabir University of Technology, Tehran 15875-4413, Iran
c
Mechanical Engineering Department, Amirkabir University of Technology, Tehran 15875-4413, Iran

ARTICLE INFO ABSTRACT

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Keywords Gelatin (GN) is a polymer, which is similar to the protein derived from collagen, an organic element in the bone.
Nanocomposite scaffold GN can incorporate into the mineral part of the bone, hydroxyapatite (HA). The HA bioceramic has properties
Drug release very close to the natural bone characteristics. Therefore, in this research, bio-nanocomposite scaffolds made of the
Space holder technique HA composed with magnetite nanoparticles (MNPs) are fabricated. For this purpose, the space holder technique
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Gelatin polymer is put to use using NaCl particles as the spacers. The HA-X%MNP (X = 0 wt%, 5 wt%, 10 wt%, and 15 wt%)
scaffolds are coated via gelatin-ibuprofen (GN-IBO) in order to determine the capabilities of the scaffolds for com-
patibility and fibroblastic cells of the related tissue. The coated bio-nanocomposite scaffolds are characterized us-
ing scanning electron microscopy (SEM) and energy dispersive spectroscopy (EDS) tools. Then, the porosity and
bioactivity of the prepared samples are tested in the simulated body fluid (SBF), and the associated compressive
strength, fracture toughness, porosity and hardness are investigated. Also, the magnetic behavior of the scaffolds
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during the release of IBO in the phosphate buffer saline (PBS) is monitored after 21 days incubation. Finally, an
analytical sandwich plate model is developed to analyze the vibrational response of an axially loaded plate-type
HA-MNP bio-nanocomposite implants. The obtained X-ray diffraction (XRD) confirms the presence of IBO peaks
after removing the samples from the PBS which proves the lower release speed of the sample containing 10 wt%
MNPs. It is found that the interaction between IBO and HA affects the mechanical performance of the scaffolds.
IBO release profiles present a burst release that depends on the HA content. The given results indicate that the
manufactured scaffolds have good potentials for biological as well as hyperthermia applications in bone tissue
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engineering.

1. Introduction growth factor, and genes in the scaffolds may produce suitable mecha-
nisms to change the physiological conditions (pH, osmolality/tempera-
The magnetic targeting and the drug radiotherapy combination have ture response) [11,12].
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been developed during the recent decade in order to treat the bone
cancer cells remains after surgery. Subsequently, the Fe3O4 nanoparti-
cles release heat after inserting in a magnetic field to destroy the in-
fected cells [1–4]. Metal cations in lactate dehydrogenase (LDH) in-
clude Mg2+, Zn2+, Ni2+, Cu2+, Al3+ and Fe3+ are bioavailable and
have high ion exchange, high growth, and pH-dependent solubility.
Loading drug on magnetite nanoparticles (MNPs) during hyperther-
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One of the most important limitations in using MNPs is the size,
chemistry, crystalline structure and shape of the nanoparticles. For in-
stance, the high surface-to-volume ratio (ultrasound vibrations with a
given amount of power) of nanoparticles and their high surface activ-
ity cause to increase the efficiency of nanoparticles in drug stability
and loading. Moreover, in recent years, addition of MNPs to the hy-
droxyapatite (HA) in order to build a suitable scaffold has been investi-

mia treatment (an increase of temperature for MNP after insert in the
AC magnetic field) may lead to release drugs easier [5–10]. Releas-
ing the painkiller like Ibuprofen (IBO) (relatively constant concentra-
tion and non-steroidal anti-inflammatory drug (NSAID)), antibiotics car-
rier (gentamicin sulfate, tetracycline), anti-inflammatory agents (sali-
cylic acid), analgesic, anti-cancer drugs (cisplatin and mercaptopropyl),
gated based upon various techniques like: space holder technique [4–6],
freeze drying [10,11], three-dimensional printing [12], pressureless sin-
tering in air [13], and wet chemistry technique [13,14].
The pharmacokinetics of MNPs depend on their ability to carry the
drug as a biological barrier and increase the duration of their circula-
tion in the blood. After several decades, the development of nanotech-
nology leads to change the traditional method of using bioceramics

⁎
Corresponding author.
E-mail address: amir_salar_khandan@yahoo.com (A. Khandan)

https://doi.org/10.1016/j.msec.2020.110835
Received 13 August 2018; Received in revised form 8 March 2020; Accepted 9 March 2020
Available online xxx
0928-4931/© 2018.
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

like bredigite, baghdadite, diopside, akermanite, and HA in drug deliv-
ery system (DDS) [15–17]. In addition, the drugs have been dominated
by the biodegradable polymers which carry supports in DDS domain.
The size, microstructural pores, highly active surfaces, proper biochem-
ical and physical properties of bioceramics can lead to control and pro-
long of the drug release parameters (such as delivery location, the abil-
the starting blended material to inhibit from two important events like
agglomeration and cold welding in the milling action according to the
previous work [6–10]. The prepared material in the previous step is
then heated at 1200 °C for 3 h with heating and cooling rate of 10 °C/
min. The co-precipitation method is used as the simplest and most ef-
fective chemical method for synthesis of metal oxides and ferrites mag-

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ity to deliver the drug to a specific tissue, and deliver multiple drug netic nanoparticles. The main advantage of coexistence is its ability to
substances) compared to polymer types [18–20]. Unlike polymers, ce- synthesize a large number of nanoparticles. However, the control of the
ramic nanoparticles do not swell in the water or change in porosity and particle size distribution is limited in this method as the kinetic factors

remain very stable during variation of pH or temperature for develop-
ing pharmacokinetic model and stochastic treatment in the health treat-
ment program [20–22]. The development of new mesoporous structures
which are suitable for drug transfer, new perspectives for treating vari-
ous types of cancers are provided. Consequently, magnetite mesoporous
nanoparticles can propagate and distribute drugs in specific cancerous
cells [23–26]. When the pores are closed with molecular nano-elec-
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affect the growth of particles.
The basic material made of n-HA is composed with 0 wt%, 5 wt%,
10 wt%, and 15 wt% of MNPs for 2 h in a planetary high energy ball
mill (HEBM) machine. The ball to powder ratio (BPR) in the HEBM
process is set equal to 10:1 using stainless steel vial and cup. Then, the
milled powders are placed at the temperature of 800 °C for 24 h to dry
up the moisture.

trolytes, stimulant responsive systems can be obtained, resulted in con-
trolling the release of drugs via an external stimuli, such as magnetic
fields, ultrasound, or optical light. In the current study, the HA-MNPs
bio-nanocomposite scaffolds with GN-IBO surface coating are manufac-
tured using space holder technique. Based upon the required experi-
ments, the mechanical properties of the scaffolds are extracted. Also,
with aid of scanning electron microscopy (SEM) and energy dispersive
spectroscopy (EDS) tools, the biological characteristics of the fabricated
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2.2. Preparation of n-HA-MNPs bio-nanocomposite scaffolds
To prepare the bio-nanocomposite scaffolds, the space holder tech-
nique is employed to fabricate the porous microstructure using sodium
chloride (NaCl) with 70% of the total sample weight as the spacer with
5–10 μm particle size similar with previous work [27–33]. In order
to compress the homogeneous mixture together with edible liquid oil

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bio-nanocomposite scaffolds before and after soaking in the simulated (2 wt% of homogenized powder), a cubic mold with 14 × 15 × 6 mm3
body fluid (SBF) are studied. In addition, on the basis of the extracted is pressurized at 140–160 MPa for 50 s using stainless steel mold and
mechanical properties, a sandwich plate model is developed to ana- die. Then, the bio-nanocomposite bulk samples are removed from the
lyze the vibration response of an axially loaded plate-type bone implant mold and kept in the furnace at 1000–1100 °C for 50 min. After that,
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made of the fabricated HA-MNP bio-nanocomposites. the samples are inserted into the deionized water for 24 h to remove re-
mained NaCl particles.
2. Materials and methods
2.3. Coating of bio-nanocomposite scaffolds
2.1. Preparation of hydroxyapatite powder
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In order to achieve the capability of drug delivery together with

For the current research, the nanocrystalline hydroxyapatite (n-HA)
is purchased from CAM Implants Company, Netherland with particle
size less than 100 nm and 98% purity. The morphological investigation
of n-HA shows a spherical shape of the powders. The chemical analysis
of the n-HA powder is shown in Table 1.
Magnetite nanoparticles (MNPs: Fe3O4) are made with the co-pre-
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an improvement in the mechanical and biological properties with simi-
lar chemical composition with the bone, the designed bio-nanocompos-
ite scaffolds are coated with a gelatin (GN) biopolymer that loaded via
IBO drug. IBO is a non-steroidal anti-inflammatory drug (NSAID) that is
utilized to treat arthritis symptoms such as arthritis, arrhythmia, gout,
fever, menstrual pain, headache, back pain, toothache, muscle cramps,

cipitation technique by combining a base to an aqueous compound of
Fe3+ chloride ions at molar ratio of 1:2. Moreover, citric acid is ap-
plied for the process as a control agent (PCA) duty which is inserted to
Table 1
The XRF of the nanocrystalline HA used in this work.
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pain due to ligament elongation, joint bolting and minor injuries. In
the current study, 10 g of GN polymer is dissolved in 100 ml hot wa-
ter for 2 h on a hot plate stirrer at 60 °C with 1000 rpm speed. There-
after, the GN-IBO coating solution is obtained for after 10 h stirrer, and
then the samples are immersed in the obtained GN-IBO solution. The
coated bio-nanocomposite scaffolds are then removed from the solution

and kept in the incubator for a day.

Compound/element Concentration (%w/w)
2.4. Materials characterization
CaO 55.5
P2O5 38.5
Na2O 1.5 In order to investigate the microstructural and nanocrystalline struc-
SO3 1.3 ture of the fabricated scaffolds including the measurement of the aver-
MgO 1.2 age distance between layers and atomic series, determination the posi-
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SiO2 1.1 tion of single crystals or grains is carried out via the X-ray diffraction
Cl 0.95
H2O 0.85
(XRD, Philips X pert) using CuKα radiation between 0 and 90°. The scan
Al2O3 0.65 rate is selected equivalent to 1°/min, the applied voltage is 40 kW and
SrO 0.60 the electric current is 30 mA. The electromagnetic spectrum within the
K2O 0.55 range between gamma and ultraviolet rays occurs for all of the samples.
Fe2O3 0.45
CuO 0.40
To achieve the nanoparticle morphology and porosity of the designed
ZnO 0.42 scaffolds (shape, size and relevance), the SEM (Amirkabir University of
TiO2 0.05 Technology) with 30–40 kV voltage is put to use. The quantum irradia-
LOI 0.03 tion regarding the presence of apatite layer is performed using elemental
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analysis with X-ray energy dispersive spectroscopy (EDS) after 21 days
soaking in the SBF with refreshing the SBF every 7

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S. Sahmani et al.
days. The total mass density and porosity of the n-HA-MNP scaffolds
coated with GN-IBO are measured according to the Archimedes prin-
ciple. The experiments related to the compressive strength and frac-
ture toughness are performed on the cubic specimens using CS SAN-
TAM-STM50 machine (CRLAB.IR, New Technologies Research Center).
The elastic modulus is also calculated from the slope of the obtained
stress-strain curve. The value of Poisson's ratio and Young's modulus are
determined with a Hounsfield tensile test machine.
The in vitro drug release behavior of the n-HA-MNPs scaffolds with
GN-IBO surface coating is evaluated by dipping them in PBS solution
(pH = 7.4) at 37 °C and the release content is studied by UV–Vis spec-
troscopy. Consequently, the released NSAID drug is calculated based on
the calibration curve. Due to the tightness of the ceramic scaffold struc-
ture, the head speed is considered to be 2 mm/min. The immersion test
in the SBF and PBS was previously conducted by Kokubo [14] to evalu-
ate the scaffold bioactivity and degradability according to the procedure
described. The fabricated bio-nanocomposite scaffolds soaked in the SBF
induce apatite nucleation on their free surface.
To evaluate the apatite formation, the samples are weighted before
and after soaking in the SBF solution. Then, the samples are marked in
the SEM images with high, medium and low formation of the apatite
layer on their free surface. Accordingly, the tiny agglomerated particles
precipitated in the porous scaffolds can be detected in the optical im-
ages. The cauliflower area is marked and then calculated using J-im-
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ages software for every sample with specific amount of MNPs. Then, us-
ing EDS analysis and cauliflower rate, it is found that calcium chloride
is very effective in depositing apatite, it is usually used in its granular
form, and it takes a long time to dissolve the seeds, which must be com-
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pletely dissolved before the next material is dissolved.
The magnetic behavior and hyperthermia term of the manufactured
scaffolds are also investigated at differential temperature changes for
15 s. The proliferation of cells is evaluated by MTT Assay Kit (Cell Pro-
liferation) (comprehensive in vitro toxicology) associated with 10, 20,
30, and 48 h. A 100 μL aliquot of MTT solution (5 mg mL−1 in PBS) is
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added and incubated for 4 h at 37 °C with 95% air and 5% CO2. Then
the medium is discarded and 1 mL dimethyl sulfoxide is added to dis-
solve the purple crystals. The optical density (OD) of the solution is then
tested with a microplate reader at 550–580 nm.
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3. Result and discussion
The n-HA-MNPs bio-nanocomposite scaffolds in this study are dip
coated by GN-IBO thin layer. In bone tissue engineering, the poros-
ity and compressive strength of the scaffolds must be balanced with
each other. Fig. 1 shows a schematic representation for the prepara
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Fig. 1. Schematic representation of the fabrication procedure for HA-MNP bio-nanocomposite scaffolds coated by GN-IBO thin layer.
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Materials Science & Engineering C xxx (xxxx) xxx-xxx
tion process of n-HA-MNPs bio-nanocomposite scaffolds produced via
the space holder technique using NaCl particles as the pore-forming
agents.
Fig. 2 depicts the XRD pattern for the pure HA, pure Fe3O4, and
HA-Fe3O4 bio-nanocomposite materials with (X = 0 wt%, 5 wt%,
10 wt%, and 15 wt%) MNPs. It is obvious that there are several Fe3O4
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peaks flap with several n-HA peaks, so it is not possible to recognize
them. The obtained results from the XRD results and modified Scherrer
equation (Fig. 3) indicate that by increasing the amount of MNPs from
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5 wt% to 15 wt%, the n-HA peaks shift to the maximum angles due to
the performance of n-HA and Fe3O4 ionic radius. It is also observed that
higher MNPs weight fraction leads to reduce the peaks related to the
n-HA, especially at 2θ, about 30–32°. Therefore, it is confirmed that the
substitution of calcium ions (0.099 nm) by Fe3+ ions (0.068 nm) can oc-
cur during composition of n-HA powder with the Fe3O4 nanoparticles
[4,5]. Also, the crystallite size of the samples increases corresponding to
higher amount of Fe3O4 nanoparticles (Fig. 3). Fig. 3 shows the modi-
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fied Scherrer evaluation of the sample with 15 wt% MNPs including the
general standard peak of n-HA powder.
A microscopic image is also taken to compare the microstructure of
the bioceramic scaffolds with different percentages of Fe3O4 amount.
The results indicate that an increment in MNPs content leads to change
significantly the microstructural shape of the composite powder before
using for scaffold preparation as well as their porosity percentage as
shown in Fig. 4. The SEM images are associated with 0 wt%, 5 wt% of
Fe3O4, 10 wt% of Fe3O4, and 15 wt% of Fe3O4 powder, based on which
the crystalline size increases as shown in Fig. 4. It is observed that the
pore size is within micron size which helps the cells to penetrate into the
pore microstructure during the primary incubation and cultivation.
The SEM micrographs determined that there are two different do-
mains of size distribution which are represented by the cluster-like
shape with micron size which is the locality of “small” n-HA crystalline,
and widespread or scattered-like shape that is locality of “large” n-HA
crystalline. Consequently, in the cluster-like size domain, the n-HA dis-
plays a medium size varying from 200 nm to about 400 nm in diam-
eter, while the scattered-like size domain displays at least two times
larger, being between 400 and 600 nm in diameter. Furthermore, the
SEM analysis shows that by increasing the weight fraction of MNPs, the
cluster shape becomes more considerable due to the cold welding of the
Fe3O4 nanoparticles to the Ca10(PO4)6OH2 groups.
Fig. 5 represents the SEM images of the samples with various
amounts of MNPs including consistent arrangement of holes and pores
with the size of 10–30 μm at low amount of Fe3O4. It is demonstrated
that the magnetite nanoparticles may be recognized at the blade of
the microclusters. The SEM micrographs reveal that the prepared bio-
S. Sahmani et al.
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Fig. 2. XRD patterns of the pure HA (standard peak), pure MNPs, and HA-MNP bio-nanocomposite scaffolds containing 5 wt%, 10 wt%, 15 wt% MNPs.
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Fig. 3. Modified Scherrer evaluation result for the HA-MNP bio-nanocomposite scaffold with 15 wt% MNPs including the general standard peaks of n-HA powder.
nanocomposite scaffolds consist of several clusters. Fig. 6 shows that
a decomposition happens in the sample with 10 wt% Fe3O4 and it oc-
curs more than the sample with 15 wt% Fe3O4. This change is due to
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high apatite formation rate of sample with 10 wt% MNPs compare with
other samples, and it leads to higher degradation after the supersat-
uration of saline with calcium ions and decomposition of the sample.
The associated EDS analyses are conducted to characterize the white ap-
atite layer on the free surface of the sample with 15 wt% Fe3O4. As-
suming the number of distinct components is not recognized/monitored,
the variation of the dependent atomic amount like Calcium and Phos-
phor can be exhibited as shown in Fig. 6(c). It is seen that as the mass
of Fe3O4 reaches to 15 wt% (Fig. 6c), calcium (Ca2+) and phosphate
(PO42−) peaks represent a growing trend which assures an increase
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Materials Science & Engineering C xxx (xxxx) xxx-xxx
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in the inclination of apatite disposition on the free surface of sample in-
cluding tiny agglomerated particles. As the scaffold is immersed in the
SBF, the ion transfer between its free surface with high roughness and
porosity and the SBF liquid happens [17–28].
Also, the cell cultural examination for bone magnetic bio-nanocom-
posite is performed within the cell environment using an MTT assay. As
it is illustrated in Fig. 6d, in the first 24 h, the cell growth is higher
on the samples with higher amount of MNPs, but as the soaking period
increases, the cell remains healthy after 7 and 8 days. The MTT assay
indicates that even in higher concentrations of extracts, the biocompat-
ibility is less than 100%, but after 48 h, it experiences remarkable im-
provement, especially on the sample with 5 wt% MNPs, and for almost
all concentrations. The results reveal that the produced porous scaf
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

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Fig. 4. SEM images of the fabricated HA-MNP bio-nanocomposite scaffolds: (a) 0 wt% MNPs, (b) 5 wt% MNPs, (c) 10 wt% MNPs, and (d) 15 wt% MNPs.
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Fig. 5. The SEM images of the fabricated HA-MNP bio-nanocomposite scaffolds with GN-IBO surface coating: (a) 0 wt% MNPs, (b) 5 wt% MNPs, (c) 10 wt% MNPs, (d) 15 wt% MNPs.
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folds are not only highly biocompatible, but also have biocompatibil-
ity bias of between 48 h and 72 h which has a positive effect on the
cell growth. In the first 24 h, the cell viability is somewhat better than
the neat sample, which is due to the presence of more MNPs that pro-
vides better conditions for biocompatibility that improve the compatibil-
ity with the body's internal tissue. The analysis indicated that the archi-
tecture of synthetic nanocomposite is similar to the human's bone femur
and can be a potential choice as bone implantation. Also, the analysis
proved that the porosity and compression strength of the bone femur are
similar to a spongy bone.
In accordance with Fig. 7, the analysis of porosity and apatite for-
mation shows that increasing the MNPs amount causes to reduce the
interconnected porosities while the biodegradation rate on the free sur-
face of scaffold enhances. Although the reduction in porosity may pre-
sent a low penetrable architecture which prevents the cells from en-
tering to the holes. As a result, it causes a reduction in cell seed-
ing and makes tissue ingrowth and vascularization. However, it leads
to increase the compressive strength of the specimens as presented in
Fig. 7(b). The obtained conclusion reveals that the microhardness and
elastic modulus of the fabricated scaffolds can be increased by rising

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S. Sahmani et al.
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Fig. 6. (a) SEM image of the scaffold with GN-IBO surface coating and 10 wt% MNP after soaking in SBF, (b) SEM image of the scaffold with GN-IBO surface coating and 15 wt% MNP
after soaking in SBF, (c) the EDS images of the precipitated apatite layer containing calcium and phosphate group on sample with 15 wt% MNPs, (d) cell cultural examination for bone
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magnetic bio-nanocomposite in the cell environment using a MTT assay for the first 24 h.
the amount of MNPs, and it leads to higher strain rate. Fig. 7(c) shows
the porosity value of the samples, in which the addition of MNPs causes
to decrease the porosity percentages, it also affects the IBO release to the
minimum amount in the PBS solution. Moreover, the porosity changes
do not limit the hardness and modulus of elasticity of the samples as
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shown in Fig. 7(d). The compressive strength of the fabricated ceramic
scaffolds with different MNPs weight fractions is obtained within the
range of 2.1 to 3.1 MPa.
Fig. 8a shows the amount of IBO release after 40 h (fast release)
which proves this point that increasing the amount of Fe3O4 nanopar-
ticles protects the manufactured scaffolds from high degradation rate
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and release in the PBS solution. It can be seen that the most of drug
is released from the sample with the lowest amount of MNPs (with-
out MNPs). Therefore, one can say that the sample without MNPs has
weaker interactions with polyhedral oligomeric silsesquioxanes (POSS)
in comparison with a sample contains higher amount of Fe3O4 nanopar-
ticles [29–40]. In addition, the UV spectrum results show a weaker peak
associated with the IBO peak in comparison with those detected in the
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samples with 5 wt% and 10 wt% Fe3O4 nanoparticles as it can be seen
in Fig. 8(b). Also, Fig. 8(c) depicts that the sample with higher amount
of Fe3O4 nanoparticles release the maximum heat after 15 s compared
to the other samples. This matter means that it is possible to increase
the IBO drug release around the tissue with 10–14 °C of changes in the
temperature. Fig. 8(d) represents a comparison of the total porosity, ap-
atite formation and degradation rate of the bio-nanocomposite scaffolds
which proves this point that in general, the sample with 10 wt% and
15 wt% Fe3O4 nanoparticles have better biological properties compared
with the pure and the sample with 5 wt% Fe3O4 nanoparticles.
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Materials Science & Engineering C xxx (xxxx) xxx-xxx
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4. Sandwich plate model for n-HA-MNP bone implants coated with
GN-IBO thin layer
It has been reported previously that vibrations of biological implants
may lead to increase their capability of cell regeneration [41–44]. So,
in the current study, the linear and nonlinear vibrations on an axially
loaded plate-type bone implant made of the n-HA-MNP bio-nanocom-
posites coated with GN-IBO thin layer are studied. For this purpose,
as illustrated in Fig. 9, a sandwich plate model with length L1, width
L2, total thickness h including the bulk thickness hb and the coating
layer thickness hf is considered for a plate-type implant made of the
n-HA-MNP bio-nanocomposites coated by GN-IBO thin layer. This point
should be noted that the manufactured scaffolds are porous, and GN-IBO
can be coated on the surface of any connected pores when the specimens
are immersed in GN-IBO solutions, even deep inside the bulk scaffolds.
Therefore, the present analytical model is a reasonable simplification of
the geometric model. Accordingly, it is supposed that the coating layers
are smooth and uniformly distributed on the free surface of the bulk ma-
terial. Also, the bulk material is considered homogenous and isotropic,
the mechanical properties of which are similar to those obtained experi-
mentally for the manufactured scaffolds.
Within the framework of the refined exponential shear deformation
plate theory, the components of displacement field along different coor-
dinate directions can be written as
(1a)
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

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Fig. 7. (a) Variation of the weight loss and bioactivity behavior, (b) compressive strength and fracture toughness, (c) porosity value, (d) elastic modulus and hardness with MNP weight
fractions for the manufactured scaffolds coated with GN-IBO thin layer.
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(1b)

(1c) (3)

where u, v and w in order represent the displacement components along

where
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x-, y- and z-axis. Moreover, ψx and ψy in order denote the rotations of

the cross section at neutral plane normal about y- and x-axis.
Based upon the von Karman nonlinear strain-displacement relation-
ships, it yields
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(2)
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(4)

where Eb and Ef represent, respectively, the Young's modulus of the

where εij0, κij(1), κij(2) (i, j = x, y) stand for the mid-plane strain compo- bulk and coating film, νb and νf in order are the Poisson's ratio asso-
nents, the first- and higher-order curvature components, respectively. ciated with the bulk and coating film of the sandwich plate-type im-
Consequently, the constitutive relationship for a sandwich plate-type plant. The values of these parameters are extracted experimentally for
implant takes following form

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S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

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Fig. 8. (a) The analysis for drug release of the fabricated bio-nanocomposite scaffolds soaked in the PBS after 40 h, (b) the UV spectrum of IBO after detection in the PBS, (c) the hyperther-
mia evaluation of the fabricated bio-nanocomposite scaffolds for 15 s, (d) the comparison between apatite formation, total porosity and degradation rate of the fabricated bio-nanocom-
posite scaffolds.
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Fig. 9. Schematic representation of the sandwich plate model for a n-HA-MNP bio-nanocomposite implant dip coated by GN-IBO thin film.
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the fabricated n-HA-MNP bio-nanocomposite scaffolds with GN-IBO sur-

face coating as given in Table 2.
On the basis of the continuum elasticity, the total strain energy of
the sandwich plate-type implant can be written as

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S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

Table 2 in which
The mechanical and physical properties of the gelatin, ibuprofen, gelatin/IBO, and
HA-MNPs scaffolds fabricated via space holder technique with NaCl particles as spacer
size.

Young's
Modulus Energy at Poisson Density Strength
Materials (MPa) break (J) ratio (g/cm 3) (MPa)

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Gelatin 2.7–3.0 0.98 ± 0.1 0.28 1.40 0.11 ± 0.01
IBO 2.9–3.3 1.10 ± 0.2 0.29 1.03 1.1 ± 0.2

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Gelatin/IBO 1.5–2.0 1.78 ± 0.1 0.33 1.65 0.8 ± 0.1
S1 220 – 0.28 3.76 2.1
S2 280 – 0.29 3.89 2.8
S3 300 – 0.29 4.36 2.95
S4 360 – 0.30 4.69 3.1

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(5)

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in which the related stress resultants can be defined as
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EC

(7)
RR

(6)
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9
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

F
OO
in which ρf1, ρf2, ρb denote, respectively, the mass density of the upper
surface coating layer, lower surface coating layer, and bulk of the sand-
wich plate-type implant.
Moreover, the work ΠP done by the external distributed load can be
expressed as

(10)

PR
Thereafter, with the aid of the Hamilton's principle, the nonlinear
governing differential equations of motion in terms of the stress resul-
tants can constructed as

(11a)

In addition, the kinetic energy of the sandwich plate-type implant (11b)

D
made of the fabricated n-HA-MNP bio-nanocomposites with GN-IBO sur-
face coating based upon the exponential shear deformable plate model
can be written as (11c)
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(11d)

(11e)

(8)
EC

Additionally, the Airy stress function f(x, y) can be introduced as fol-

lows

(12)
where
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A perfect geometric is considered for the plate-type implant, the

compatibility equation relevant to the mid-plane strain components can
be given as

(13)

Based upon eqs. (6) and (13), the nonlinear governing differential
(9)
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equations of motion can be rewritten in terms of the displacement com-

ponents as below
UN

10
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

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(14a)
(14c)

PR
D
TE
EC

(14b)
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11
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

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(16)

(14d)

PR
D
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(17)
EC

On the other hand, the equilibrium condition related to the applied

loads in the direction of x-axis can be given as

(15)

Moreover, the shortenings per length of the sandwich plate-type im-

RR

plant along x-axis and y-axis, respectively, can be introduced as below

Thereafter, through making the nonlinear governing differential

equations of motion in dimensionless form, and then employing an
CO

improved perturbation method together with the Galerkin technique

[45–64], analytical explicit expressions for the nonlinear stability curve
and nonlinear vibration response of the sandwich plate-type implant
made of the axially loaded n-HA-MNP bio-nanocomposites dip coated by
GN-IBO thin film can be extracted as

(18)
UN

(19)

(20)

(21)

where represents the dimensionless maximum deflection of

12
S. Sahmani et al. Materials Science & Engineering C xxx (xxxx) xxx-xxx

the sandwich plate-type implant. The proceeding numerical results are
presented for samples with dimensions of L1 = L2 = 1 cm, hb = 2 mm,
and hf = 10 μm. However, in order to give the results in a general form,
they are presented in dimensionless pattern.
In Fig. 10, the variation of the nonlinear frequency to linear fre-
quency ratio (ωNL/ωL) with the maximum deflection is demon
strated associated with free vibrations of a plate-type bone implant made
of the fabricated n-HA-MNP bio-nanocomposites with GN-IBO surface
coating and corresponding to different MNP weight fractions. It is ob-
served that by increasing the MNP weight fraction, the slope of this
variation decreases, so for a specific value of the maximum deflection,
the ωNL/ωL ratio of the implant with higher value of MNP weight frac

F
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PR
D
TE
EC

Fig. 10. Variation of the nonlinear frequency with maximum deflection of a plate-type bone implant made of the fabricated HA-MNP bio-nanocomposites coated with GN-IBO layer corre-
sponding to various MNP weight fractions.
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CO
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Fig. 11. Dimensionless load-frequency of an axially loaded plate-type bone implants made of the fabricated HA-MNP bio-nanocomposites coated with GN-IBO layer corresponding to
various MNP weight fractions.

13
S. Sahmani et al.
D
Fig. 12. dimensionless nonlinear frequency-deflection response an axially loaded plate-type bone implants made of the fabricated HA-MNP bio-nanocomposites coated with GN-IBO layer
corresponding to various MNP weight fractions.
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tion is lower. However, for higher weight fraction, the significance of
this pattern reduces. This anticipation is the same for the both simply
supported (SSSS) and clamped (CCCC) edge supports.
Fig. 11 illustrates the dimensionless load-frequency response of
an axially loaded plate-type bone implant made of the fabricated
n-HA-MNP bio-nanocomposites with GN-IBO surface coating corre-
EC
sponding to various values of MNP weight fraction. It is found that
within the prebuckling regime, for a specific value of the axial compres-
sion, the natural frequency of the implant enhances by increasing the
value of the MNP weight fraction. However, there is an opposite pattern
within the postbuckling domain. Moreover, it is obvious that the implant
containing higher amount of MNP buckles at higher value of applied ax-
RR
ial compressive load.
In Fig. 12, the dimensionless nonlinear frequency-deflection re-
sponse of an axially loaded plate-type bone implant made of the fabri-
cated n-HA-MNP bio-nanocomposites with GN-IBO surface coating is de-
picted corresponding to various values of MNP weight fraction. It is seen
that within the both prebuckling and postbuckling regimes, the nonlin-
CO
ear frequency associated with a specific value of the implant deflection
increases through an increment in the amount of MNP. This pattern is
similar for SSSS and CCCC boundary conditions.
5. Conclusion
The development of new mesoporous structures which are suitable
UN
for drug transfer, new perspectives for treating various types of cancers
were provided in this work. For this purpose, magnetite mesoporous
nanoparticles can propagate and distribute drugs in specific cancerous
cells. The magnetic behavior of the manufactured scaffolds during the
release of IBO in the PBS was monitored after 21 days incubation. The
obtained XRD confirmed the presence of IBO peaks after removing the
samples from the PBS which proved the lower release speed of the sam-
ple containing 10 wt% MNPs. Furthermore, it was found that the in-
teraction between IBO and n-HA affects the mechanical performance of
the fabricated scaffolds. It was observed that IBO release profiles pre-
sent a burst release that depends on the HA content. The given results
indicated that the manufactured scaffolds have good potentials for bio
14
Materials Science & Engineering C xxx (xxxx) xxx-xxx
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PR
logical as well as hyperthermia applications in bone tissue engineer-
ing. The analysis of porosity revealed that increasing the MNPs amount
causes to reduce the interconnected porosities while the biodegradation
rate on the free surface of scaffold enhances.
Additionally, on the basis of the extracted mechanical properties, a
sandwich plate model was constructed to analyze the vibrational char-
acteristics of an axially loaded plate-type bone implant made of the fab-
ricated HA-MNP bio-nanocomposites. It was found that within the both
prebuckling and postbuckling regimes, the nonlinear frequency associ-
ated with a specific value of the bio-nanocomposite implant deflection
increases through an increment in the amount of MNPs.
Declaration of competing interest
The authors declare that they have no known competing financial in-
terests or personal relationships that could have appeared to influence
the work reported in this paper.
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