UNIVERSIDADE ESTADUAL PAULISTA
“JÚLIO DE MESQUITA FILHO”
Instituto de Ciência e Tecnologia
Campus de São José dos Campos
ORIGINAL ARTICLE DOI: https://doi.org/10.4322/bds.2023.e3791
1
Braz Dent Sci 2023 July/Sept;26 (3): e3791
Suckermouth catfish bone extract as bone graft raw material for
bone-healing promotes bone growth in bone loss
Extrato de osso de bagre como material de reparo promove o crescimento ósseo em perda óssea
Nursyamsi DJAMALUDDIN1 , Nurlindah HAMRUN2 , Nurhayaty NATSIR3 , Nursinah AMIR4 ,
Andi Apriliiqa Megumi Adhila LARASATI5 , Rahma Sania SYAHRIR5 , Shaffati SHAFFA6 , Syamsiah SYAM7
1 - Hasanuddin University, Department of Dental Public Health, Faculty of Dentistry, Makassar, Indonesia.
2 - Hasanuddin University, Department of Oral Biology, Faculty of Dentistry, Makassar, Indonesia.
3 - Hasanuddin University, Department of Conservative Dentistry, Faculty of Dentistry, Makassar, Indonesia.
4 - Hasanuddin University, Department of Fishries, Faculty of Marine Science and Fishries, Makassar, Indonesia
5 - Hasanuddin University, Faculty of Dentistry, Makassar, Indonesia.
6 - Hasanuddin University, Department of Veterinary Medicine, Faculty of Medicine, Makassar, Indonesia.
7 - Universitas Muslim Indonesia, Department of Conservative Dentistry, Faculty of Dentistry, Makassar, Indonesia.
How to cite: Djamaluddin N, Hamrun N, Natsir N, Amir N, Larasati AAMA, Syahrir RS, et al. Suckermouth catsh bone extract as bone graft
raw material for bone-healing promotes bone growth in bone loss. Braz Dent Sci. 2023;26(3):e3791. https://doi.org/10.4322/bds.2023.e3791
ABSTRACT
Objective: This study aimed to evaluate the properties of suckermouth catsh bone extract, which allows
it to be adopted as a raw material for bone graft following its graft in an articial defect of a rat model.
Material and Methods: Hydroxyapatite (HA) from suckermouth catsh bone extract was characterized using
Fourier-transform infrared spectroscopy (FTIR), and its toxicity was evaluated by Brine Shrimp Lethality Test
(BSLT). This material was grafted on articial defects in rats’ femoral bones, which were observed immunologically
by Enzyme-linked immunosorbent assay (ELISA) after one week and four weeks, and radiographically in the
second week, and histologically in the second and fourth weeks. Results: FTIR shows that this material consists of
phosphate, hydroxyl, and carbonate groups, while the BSLT results show that this material is not toxic. Observations
by ELISA showed an increase in the expression of Tumor necrosis factor alpha (TNF-α) in defects with HA in the
fourth week. Radiographically the defect did not show closure in the second week. In contrast, histological analysis
showed a better bone healing process in the defect, which was applied with the HA of the suckermouth catsh bone.
Conclusion: The HA extracted from the suckermouth catsh bone has benecial properties as an alternative to bone
graft raw material and, more investigated needed to support this biomaterial to be used in the treatment of bone loss.
KEYWORDS
Hydroxyapatite; Bone graft; Bone defect; Bone healing; Fourier Transform Infrared Spectroscopy.
RESUMO
Objetivo: Avaliar as propriedades do extrato de osso de bagre, que permitem sua adoção como material bruto
para enxerto ósseo, em um defeito ósseo articial em ratos. Material e Métodos: A hidroxiapatita (HA) do extrato
de osso de bagre foi caracterizada usando espectroscopia infravermelha por transformada de Fourier (FTIR), e
sua toxicidade foi avaliada pelo Teste de Letalidade do Camarão de Sal (BSLT). Esse material foi enxertado em
defeitos articiais nos ossos femorais de ratos. Análise imunológica por meio do ensaio imunoenzimático (ELISA)
foi realizada uma e quatro semanas após a colocação dos enxertos. Análises radiográcas foram feitas na segunda
semana e histológica na segunda e quarta semanas. Resultados: A FTIR mostrou que esse material é composto por
grupos de fosfato, hidroxila e carbonato, enquanto os resultados do BSLT mostraram que esse material não é tóxico.
As observações pelo ELISA mostraram um aumento na expressão do fator de necrose tumoral alfa (TNF-α) nos
defeitos com HA na quarta semana. Radiogracamente, o defeito não apresentou fechamento na segunda semana.
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Braz Dent Sci 2023 July/Sept;26 (3): e3791
Djamaluddin et al.
Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
INTRODUCTION
Alveolar bone is a structure that supports
teeth, protects nerves, blood vessels, and glands,
and supports masticatory and facial muscles [1,2].
Alveolar bone loss can occur due to periodontal
disease, cysts, tumors, post-extraction trauma, or
other trauma [3-5]. The patient’s quality of life
can be signicantly impacted by alveolar bone loss
because it can lead to mobility issues and tooth loss
if it progresses without treatment [3,6,7].
Efforts to overcome challenges in recovering
lost alveolar bone currently can be done with
several types of treatment, one of which is the use
of bone grafts which aim to replace damaged bone
tissue using specic materials that can come from
the patient’s body, synthetic/chemical materials,
or other materials [4,5,8]. This treatment
shows a high success rate in rebuilding alveolar
bone morphology [9-11]. Bone grafts must be
biocompatible, osteoconductive, osteoinductive,
and osteointegration to provide structural support
and stimulate bone healing [4,5,12]. The primary
raw material for bone grafts is hydroxyapatite
(HA) with the formula Ca10(PO4)6(OH)2, which
is an inorganic biomaterial compound that is a
component of human bones, teeth, and dentine
and can come from various natural sources, such
as bovine bone, a mixture of pork bones with
horse bones, sh scales, limestone, egg shells,
cow teeth, and sh bones [13-17].
The need for HA for bone grafts has
signicantly increased in response to the rise in
occurrences of alveolar bone loss [18-20]. This
problem necessitates creating and investigating
substitute HA materials for bone graft raw
materials made from natural materials. Indonesia,
a maritime nation rich in different marine biota
that contains HA, can be exploited as a source of
raw materials for bone transplants, such as sh
bones [21,22]. In many lakes, the suckermouth
catsh (
Pterygoplichtys pardalis
) is a species of
fish whose bones can be utilized as a natural
source of raw materials to synthesize HA, which
is anticipated to help lessen environmental issues
as sh populations rise. However, in Lake Tempe,
South Sulawesi, Indonesia, suckermouth catsh are
an invasive species that threaten the ecosystem’s
equilibrium and compete with native sh species,
upsetting the food chain and resulting in the
extinction of several endemic sh species [23].
Based on the problem of tooth loss due to
alveolar bone loss and the potential content of
HA from suckermouth catsh bones, this study
innovates to seek HA alternatives by evaluating
the properties of suckermouth catsh bones in
their utilization as bone graft raw material for
bone healing.
MATERIALS AND METHODS
Material preparation
The hydrothermal technique which refers to
the procedure proposed by Alqap and Sopyan [24]
which is modied by the procedure carried out by
Chadijah [25], was adopted in this investigation
to manufacture 100 suckermouth catsh bones
as the HA raw material. The suckermouth catsh
is obtained from Lake Tempe, which is located
in the province of South Sulawesi, Indonesia.
First, the esh and bones of the suckermouth
catsh are separated once it has been skinned.
Next, the sh bones are cleaned, washed under
running water, and dried in the air for 24 hours.
Next, the fish bones were soaked in acetone
solution (C3H6O) for 3×24 hours and exchanged
daily to decontaminate protein in the sh bones.
After that, the fish bones were placed in the
oven for 30 minutes at 115oC. Next, sh bones
were smashed in a mortar and sieved through
a 200 mesh screen before being subjected to
the calcination process. The following step is
calcination, which takes place for five hours
at a temperature of 700 to 800oC. The initial
stage of HA synthesis was weighing 5.117 g
of sh bone powder and then dissolving it in
100 mL of distilled water in a 250 mL Erlenmeyer.
Em contraste, a análise histológica mostrou um melhor processo de cicatrização óssea no defeito que foi aplicado
com a HA do osso de bagre. Conclusão: A HA extraída do osso de bagre possui propriedades benécas como
alternativa ao material bruto para enxerto ósseo, sendo necessárias mais investigações para apoiar esse biomaterial
a ser usado no tratamento da perda óssea.
PALAVRAS-CHAVE
Hidroxiapatita; Enxerto ósseo; Defeito ósseo; Cicatrização óssea; Espectroscopia no infravermelho por transformada
de Fourier.
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Djamaluddin et al.
Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
Next, the solution was homogenized using a
stirrer speed of 300 rpm at 90oC for 1 hour after
the dissolved bone sh was combined with 100 mL
of a 0.547 M solution of ammonium dihydrogen
phosphate (NH4H2PO4). Furthermore, the
solution was processed hydrothermally using an
autoclave for 1 hour at a temperature of 121oC
and a pressure of 1 atm. Then, the sterilized
solution was filtered using Whatman filter
paper no. 42. The precipitate obtained was
then washed three times using distilled water to
remove the remains of ammonium dihydrogen
phosphate, heated at 105oC for 30 minutes,
and continued with the blasting stage, namely
at 700oC for 5 hours and then at 900oC for
10 minutes. Finally, the obtained material was
tested for toxicity and FTIR.
FTIR analysis
The fishbone powder was placed on an
Attenuated Total Reflectance (ATR) plate at
a controlled ambient temperature (25oC) and
scanned using an FTIR spectrophotometer
(ABB MB3000, Clairet Scientic, Northampton, UK)
at a wavenumber of 4000 – 650 cm-1 equipped with
a deuterated triglycine sulfate (DTGS) detector
and potassium bromide (KBr) as the beam splitter,
recorded for 32 scans at 8 cm-1 resolution. These
spectra were recorded as absorbance values at each
data point in triplicate.
Toxicity test
In the present study, the toxicity test was
carried out using the BSLA method. The toxicity of
the sh bones was tested at concentrations of 62.5,
125, 250, 500, and 1000 ppm in 10 ml seawater
solution and 0 ppm without the test substance as a
control, which was added with 1% DMSO solvent
(v/v). Then 30 Artemia salina Leach (nauplii)
shrimp larvae aged 48 hours were used at each
concentration tested. The toxic effect was obtained
from observations by calculating the percentage
of death of nauplii at each concentration within
24 hours, which was obtained by multiplying the
ratio by 100%, namely the number of dead larvae
divided by the number of initial larvae multiplied
by 100% for each replication (three replications
were used for each concentration). Then it was
compared with the control, and the results were
analyzed using probit analysis so that the LC50
value was obtained using the Software Package
used for Statistical Analysis (Version 25.0; SPSS
Inc., Chicago, IL, USA).
Grafting procedure
Twenty-four Rattus norvegicus rats aged
8-10 weeks with an average body weight of
188.365 g were used in this study. The animal
study protocols were reviewed and approved by
the Ethics Committee of the Dentistry Faculty
of Hasanuddin University under approval
no. 0065/PL09/KEPK FKG-RSGM UNHAS/2021
and conducted at Veterinary Captive Laboratory,
Hasanuddin University (Makassar, Indonesia).
Rattus norvegicus rats were divided into four
groups based on the grafting material consisting
of P0 (without grafting), P1 (100% HA shbone),
P2 (100% HA bovine), and P3 (50% HA shbones
and 50% HA bovine). The HA bovine that we
used in this study were commercial HA (BATAN
RESEARCH TISSUE BANK, FDBX Xenogrfat)
produced by BATAN Jakarta, Indonesia.
The grafting procedure was performed under
general anesthesia using isourane inhalation.
Approximately 0.1 g of HA powder P1 (n = 3),
P2 (n = 3), and P3 (n = 3) was mixed with
the blood of the test animals and then grafted
onto the femoral bone of the rat after creating
an articial defect by drilling which resulted in
a defect with a diameter of 2 mm and 2 mm
depth. At the same time, control group P0 was
left without graft material.
ELISA observation
In the rst and fourth weeks after grafting,
blood serum was taken from each group to
test the effectiveness of the raw material
using the Mouse Tumor Necrosis Factor Alpha
ELISA kit (GenWay BioTech, San Diego, USA),
which followed the manual instructions.
Data from the test results were then analyzed
using the dependent sample T-test with the
Software Package used for Statistical Analysis
(Version 25.0; SPSS Inc., Chicago, IL, USA)
application.
Radiography analysis
The effectiveness of raw materials was
also tested by radiographic examination, which
was carried out randomly on experimental
animals, one tail per group. In addition,
radiographic examinations using x-rays (Toshiba
MRAD-A32S, Toshiba Medical Manufacturing
Co., Ltd, Tochigi, Japan) were carried out in
the second weeks to determine the progress of
bone growth.
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Braz Dent Sci 2023 July/Sept;26 (3): e3791
Djamaluddin et al.
Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
Histopathological analysis
Testing the effectiveness of raw materials is
also carried out by histopathological examination
to determine the progress of osteoblast cell growth.
Rattus norvegicus rats were euthanized in the
second and fourth weeks after grafting, and the
femur from each treatment group was taken.
Samples were rinsed with distilled water, xed
with 10% formalin, and decalcified with 10%
EDTA. Then the samples were washed in distilled
water, dehydrated, embedded, trimmed, stained
with Hematoxylin and Eosin (H & E), and examined
via a digital image capture pathology scanner
(Aperio CS model, Leica Biosystems, Buffalo
Grove, IL, USA) under 400 × magnifications.
Histopathological examination was only carried
out in groups P1, P2 and P3.
RESULTS
FTIR analysis
Figure 1 shows the spectra of phosphate,
carbonate, and hydroxyl groups in shbone and
bovine. The stretching vibrations of phosphate
HA from sh bones and HA bovine are in the
same wave number range, 1031-1093 cm-1.
The sharp uptake of phosphate HA phosphate
from sh bones was detected at wave numbers
1047-1093 cm-1 and HA bovine phosphate
groups at wave numbers 1031.92 cm-1. The
wave numbers 569 cm-1 and 601 cm-1 indicate
a symmetrical stretching vibration of the HA
phosphate of sh bone compared to the bovine
HA phosphate group at waves 603.72 cm-1 and
561.29 cm-1, both of which are at the same wave
number range, namely, 561.29-603.72 cm-1. The
stretching vibration of the HA hydroxyl group in
the shbone was detected at a wave number of
3570.24 cm-1. The wave numbers of 1413.82 cm-1
and 837.11 cm-1 indicated carbonate groups’
presence in the shbone’s HA. While, carbonate
group in the HA bovine detected at waves
1411.89 cm-1, 867.97 cm-1, and 732.95 cm-1.
Toxicity test
Nauplii that were exposed to the extract
of the sh bones at the highest concentration,
namely 1000 ppm, showed the highest mortality
of 20%. However, probit analysis of the HA of the
sh bones as shown in Figure 2 depicted that the
LC50 value was 49137.4644 ppm (> 1000 ppm)
which showed that the HA of the sh bones was
not toxic.
ELISA observation
Table I shows the average expression of
TNF-α from experimental animals after four
weeks of treatment. All treatment groups except
P0 experienced an increase in TNF-α expression
in the fourth week, and the test results of the four
types of treatment in the rst and fourth weeks
showed a signicant difference (p=0.037).
Radiography analysis
In Figure 3 it can be seen that until the
second week for each defect made on the femur
and given HA according to the type of treatment
P0, P1, P2, and P3 showed no signicant healing
process which was marked by all defects still
Figure 2 - Correlation between mortality percentage (probit value) of nauplii and HA concentration of fish bones.
Figure 1 - Spectra of phosphate, carbonate, and hydroxyl groups in
HA of fish bones and bovine.
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Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
visible radiolucent (red circle) which indicates
that complete closure has not occurred.
Histologic evaluation
Figure 4 shows the results of H&E staining
of the sample defects treated with HA at weeks
2 and 4. At week 2, groups P1 and P2 showed a
more pronounced formation of granulation tissue in
the defect area treated with HA compared to group
P3. Furthermore, in the fourth week, all treatment
groups showed granulation tissue formation.
However, the P1 group showed denser granulation
tissue formation than the P2 and P3 groups, which
indicated better bone renewal in the P1 groups.
Table I. The average TNF-α expression value of the test animals in the first and fourth weeks
Treatment Groups 1st Week 4th Week
p
-value
P0 192.804a120.082b
0.037*
P1 73.691a154.842b
P2 203.846a253.560b
P3 150.570a280.274b
*Dependent sample T test;
p
< 0.05: significant. The value with different superscript letters in a column are significantly different.
Figure 3 - Radiographic picture showing a radiolucency in the defect of the femur in the second week of the test animal.
Figure 4 - H&E staining result of the P1, P2, and P3 treatment groups at 2 and 4 weeks after grafting with various HA. (Black arrow: defect with HA).
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Djamaluddin et al.
Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
DISCUSSION
The use of hydroxyapatite as a bone substitute
has been widely developed because the structure
of hydroxyapatite is component of human bone. In
addition, the bioactive bio-ceramic hydroxyapatite
is also biocompatible, biodegradable, non-toxic,
osteoconductive, and osteoinductive, making it an
auspicious material for use as a replacement and
bone regeneration in cases of bone damage and
defects [26-29]. In this study, FTIR spectroscopy
was used to characterize HA. It detected the
presence of phosphate, hydroxyl, and carbonate
groups in both the HA of sh bones and HA bovine.
In the present study, the FTIR spectroscopy analysis
showed there is no signicant different between HA
of sh bones and HA bovine. Compared to normal
bone, bone and dentin have the most carbonates,
which contain up to 8% of the weight [30]. While
in some synthetic HA, carbonate groups are
absent [31]. Thermal stability during the synthesis
process can affect the loss of carbonate groups, so
this must be controlled to ensure the biomaterial
exhibits sufcient biological behaviour [32]. In this
study, HA preparation was carried out using the
hydrothermal method, which has the advantage
of minimizing material loss [33].
The biocompatibility of a biomaterial is very
important so that failure does not occur when
using it. When in contact with tissues, biomaterials
in the form of graft materials will induce foreign
body reactions, which trigger the aggregation of
large numbers of immune cells and inammatory
cytokines, inducing acute and chronic inammatory
responses and brous reactions [34]. So that if
the biomaterial has a high enough toxicity, it will
result in tissue damage and even affect some of
the functions of the body’s organs [34,35]. In this
research, the toxicity test showed that the HA of the
sh bones is not toxic. Several studies have shown
that nano-hydroxyapatite has a toxic potential that
can cause cell death due to exposure of macrophages
to high levels of nano-hydroxyapatite due to the
release of high levels of intracellular calcium,
which disrupts the homeostasis of intracellular
calcium [36]. However, nano-hydroxyapatite
has physical properties that resemble natural
bone minerals and is easily absorbed to stimulate
bone-tissue regeneration [36-38]. This study
produced HA from a 200-mesh sieve equivalent to
74 microns. Even on a micro scale, hydroxyapatite
can still encourage bone-tissue regeneration
through extracellular pathways and does not
interfere with calcium homeostasis [39].
The bone healing procedure consists of three
phases: inammation, bone repair/production, and
bone remodeling [40,41]. Inammatory cytokines
such as TNF-α are essential factors in the process
of bone healing, and this study showed that HA
application would increase TNF-α secretion in the
fourth week. This indicates that defects receiving
HA treatment can stimulate the release of cytokines
resulting in increased expression of TNF-α from
endothelial cells through an inammatory reaction,
the initial phase of the bone healing process.
Therefore, in the radiographic appearance, there
was no wound closure in all treatments in the
second week. In the biological process of bone
repair, the final phase, namely the remodeling
phase, begins with the formation of granulation
tissue [42]. Histological analysis in this study
showed that the bone healing process had been
seen in the second week. However, the defects
that received treatment with HA suckermouth
catsh bones expressed more granulation tissue in
the fourth week than the other treatment groups,
indicating better bone repair. As discussed above,
suckermouth catsh bone can be used as a raw
material for making bone grafts because of its
hydroxyapatite content which can promote better
bone healing. However, the limitations of this
study were the limited characterization evaluation
of the material, the use of a small sample size, the
histological examination, which did not involve
samples with defects without administration of HA
material, and the brief evaluation period. Therefore,
further studies with a complete evaluation of
material characteristics, histological examination
for all treatment groups, larger sample sizes, and
long-term evaluation periods are needed to support
the current study’s ndings.
CONCLUSION
FTIR analysis showed the presence of
carbonate, phosphate, and hydroxyl groups,
which are components of HA and also a
component of bone formation. A toxicity test
using the BSLT method showed that the HA of
the sh bones is not toxic. TNF-α quantication
from the results of the ELISA showed an increase
in TNF-α expression in the fourth week in
defects receiving HA treatment. Radiographs
showed that the defect had not completely
closed after the HA application in the second
week. At the same time, the histological ndings
showed that the defects applied with the HA
of the shbone had a better bone healing process.
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Braz Dent Sci 2023 July/Sept;26 (3): e3791
Djamaluddin et al.
Suckermouth catfish bone extract as bone graft raw material for bone-healing promotes bone growth in bone loss
Djamaluddin et al. Suckermouth catfish bone extract as bone graft raw material
for bone-healing promotes bone growth in bone loss
Therefore, the HA extracted from the bone of the
suckermouth catsh has benecial properties as an
alternative to bone graft raw material and, more
investigated needed to support this biomaterial to
be used in the treatment of bone loss.
Acknowledgements
The authors would like to thank Muhammad
Ruslin for technical support.
Author’s Contributions
ND: Conceptualization, Validation, Supervision.
NH: Conceptualization, Validation, Writing (Review
and Editing). NN: Methodology, Data Curation.
NA: Methodology, Data Curation. AAMAL:
Investigation. RSS: Investigation. Shaffati Shaffa:
Investigation. SS:
Data Curation, Writing Original
Draft Preparation
Conicts of Interest
The authors declare no conict of interest.
Funding
This research has received funding from
Director General of Learning and Student Affairs,
Ministry of Research, Technology and Higher
Education, Indonesia (1949/E2/KM.05.01/2021).
Regulatory Statement
This study protocols were reviewed and
approved by the Ethics Committee of the Dentistry
Faculty of Hasanuddin University under approval
no. 0065/PL09/KEPK FKG-RSGM UNHAS/2021.
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Nurlindah Hamrun
(Corresponding address)
Hasanuddin University, Department of Oral Biology, Faculty of Dentistry,
Makassar, Indonesia.
Email: lindahamrun@unhas.ac.id
Date submitted: 2023 Jan 26
Accepted submission: 2023 Jun 22
