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Interfacial characteristics of Biodentine and MTA with dentin in simulated

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Article  in  Journal of Dentistry · December 2014

DOI: 10.1016/j.jdent.2014.11.004 · Source: PubMed

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 journal of dentistry 43 (2015) 241–247

Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.intl.elsevierhealth.com/journals/jden

Interfacial characteristics of Biodentine and MTA

with dentine in simulated body fluid

Jong Ryul Kim a, Ali Nosrat b, Ashraf F. Fouad b,*

a
Department of Endodontology, Temple University Maurice H. Kornberg School of Dentistry, Philadelphia, PA, USA
b
Department of Endodontics, Prosthodontics and Operative Dentistry, University of Maryland School of Dentistry,
Baltimore, MD, USA

article info abstract

Article history: Objectives: Newer tricalcium silicate cements (TSC) may offer biocompatibility with im-
Received 12 August 2014 proved working properties. This study aimed to evaluate: (1) the occurrence of mineral
Received in revised form deposition at the interface between dentine and two TSC (ProRoot1 MTA and Biodentine1)
28 October 2014 in simulated body fluid, and (2) to investigate the nature of interfacial layer.
Accepted 8 November 2014 Methods: Six root dentine segments of 1.5 mm thickness were obtained from extracted
human teeth and were instrumented with Gates-Glidden drills. The specimens were then
randomly filled with either MTA or Biodentine. The specimens were placed in the simulated
Keywords: body fluid containing the same phosphate concentration as blood plasma. After 4 weeks, the
Biodentine specimens were examined with Scanning Electron Microscope (SEM) and Energy Disperse X-
Mineral trioxide aggregate ray Spectroscopy (EDX) to measure the thickness of the interfacial layer and Ca/P ratio.
Bioactivity Transmission Electron Microscope (TEM) and Selective Area Electron Diffraction (SAED)
Interfacial layer were conducted to examine the interface ultramicroscopically and to determine the nature
Ca/P ratio of the crystalline structure within interfacial layer.
TEM Results: The thickness of interfacial layer was significantly higher in the MTA group (14.5 mm
Amorphous calcium phosphate vs 4.8 mm) ( p < 0.001). However, there was no significant difference between MTA and
Biodentine in Ca/P ratio of interfacial layer (4.1 vs 2.7) ( p > 0.05). From TEM examination,
amorphous calcium phosphate (ACP) was observed in the interface along with the surface of
dentine.
Conclusions: As an alternative to MTA, Biodentine displayed bioactivity by producing an
interfacial layer on the root canal dentine even though its thickness was significantly lower
than MTA. ACP was observed in the interfacial layer of both biomaterials.
Clinical significance: Biodentine could be considered as an alternative to MTA due to compa-
rable bioactivity which creates interfacial layer between root canal dentin and Biodentine.
# 2014 Elsevier Ltd. All rights reserved.

mineralized tissues has been attributed to materials that

1. Introduction have the ability to form carbonated apatite on their surface
when exposed to simulated body fluids in vitro.1 An ideal
Bioactivity of materials is an important feature for tissue biomaterial should stimulate and modulate the healing
regeneration and healing. Bioactivity in the context of process to properly seal a communication that may promote

* Corresponding author at: Department of Endodontics, Prosthodontics and Operative Dentistry, University of Maryland School of
Dentistry, 650W Baltimore Street, Baltimore, MD, USA. Tel.: +1 410 7067047; fax: +1 410 7061565.
E-mail address: afouad@umaryland.edu (A.F. Fouad).
http://dx.doi.org/10.1016/j.jdent.2014.11.004
0300-5712/# 2014 Elsevier Ltd. All rights reserved.
242 journal of dentistry 43 (2015) 241–247
inflammation and degeneration of tissue.2 Sealing the
communication of pulp tissue with the oral cavity in different
types of vital pulp therapies including direct pulp capping,
partial pulpotomies and full pulpotomies, sealing the com-
munication of the root canal space with periradicular tissues
in perforation repair procedures, and sealing the root-end
cavities in endodontic surgeries are examples of situations
where the bioactivity of a biomaterial plays a key role to
promote healing around teeth.
Mineral trioxide aggregate (MTA) is a bioactive material
which was first introduced as a root-end filling material.3 MTA
powder is mainly a mixture of tricalcium silicate, tricalcium
aluminate, tricalcium oxide and silicate oxide. Bismuth oxide
has been added as radiopacifier.4 Because of its biocompati-
bility and bioactivity,5 MTA has become the material of choice
in several applications such as perforation repair6 and vital
pulp therapies.7 Bioactivity of MTA has been proved in several
studies.1,8–10 Sarkar et al.9 showed formation of hydroxyapa-
tite crystals in a phosphate buffered saline (PBS) on MTA
surface and MTA–dentine interface by using Scanning
Electron Microscope (SEM) and X-ray diffraction (XRD) analy-
sis. Studies have shown that MTA produces different superfi-
cial precipitates following immersion in different fluids. Han
et al.8 identified precipitates on the surface of MTA as calcium
carbonate and calcium hydroxide in contact with distilled
water. However, it produces amorphous calcium phosphate
(ACP) when in contact with PBS which would eventually
transform to crystalline apatite. Additionally, other studies
have shown formation of different shapes of ACP precipitate
and apatite on the surface of MTA, formation of new
interfacial layer on the cement–dentine interface, and forma-
tion of tag-like structures within dentinal tubules.11,12 Bioac-
tivity of MTA has been correlated to its biocompatibility and
osteoconductivity.13
To improve MTA drawbacks such as long setting time,
difficult handling property and discoloration, Biodentine
(Septodont, Saint-Maur-des-fossés Cedex, France) was
introduced. Biodentine is a newly developed tricalcium
silicate cement. The powder is composed of a tricalcium
silicate cement, as the main component, which makes it
similar to the MTA. Small proportions of dicalcium silicate,
calcium carbonate and zirconium oxide as radiopacifier are
added.14 The liquid for mixing with the cement powder
consists of calcium chloride (as an accelerator to reduce
setting time) and a hydrosoluble polymer.14 Compared to
MTA’s setting time of 3–4 h,4 Biodentine provides a signifi-
cantly shorter setting time of 12 min according to the
manufacturer as well as better handling characteristics;
thus, it may serve as an attractive alternative to MTA.
Biodentine is currently being used as a dentine substitute
under composite resins and shows favourable clinical
outcomes.15 Biological and animal studies on Biodentine
showed that this new restorative material induces TGF-b1
secretion from human dental pulp cells,16 and may
potentially become an acceptable material for direct pulp
capping.17 Although in vitro studies by Atmeh et al.18 and
Han and Okiji10 showed bioactivity of Biodentine in distilled
water and PBS, there is still no study to evaluate the
bioactivity of Biodentine in a simulated body fluid (SBF)
which has ion concentrations similar to the body’s
environment. In addition, a search of the literature revealed
that there is no study available on elemental analysis of the
MTA–dentine or Biodentine–dentine interface formed in
SBF.
The purpose of this study was to perform morphological
and chemical analyses of the interfacial layers that form
between MTA or Biodentine and dentine in simulated body
fluid.
2. Materials and methods
The materials tested in this study included: white ProRoot1
MTA (Maillefer, Dentsply, Switzerland) and Biodentine1
(Septodont, Saint-Maur-des-fossés Cedex, France). Both mate-
rials were mixed according to the manufacturer’s instructions.
2.1. Preparation of specimens
Six root dentine segments of 1.5 mm thickness were
obtained from the middle third of extracted single-rooted
human teeth by using a water-cooled low-speed ISOMET
diamond saw (Buehler, Lake Bluff, NY). The teeth were
sterilized overnight using ethylene oxide gas prior to usage.
The root canals were enlarged with #4 Gates-Glidden drills
(Dentsply Maillefer, Ballaigues, Switzerland) to obtain 1.1-
mm-diameter cavities. Smear later was removed by irriga-
tion with 2.5% sodium hypochlorite (Clorox, the Clorox
Company, Oakland, CA, USA) followed by 17% ethylene
diamine tetra-acetic acid (EDTA) (Sigma–Aldrich, St. Louis,
MO, USA), and drying with paper points (Diadent, Chonjiu,
South Korea). The dentine specimens were then randomly
divided into 2 groups (N = 3). The root canals of each root
segment in group 1 were then filled with ProRoot MTA and in
group 2 they were filled with Biodentine, which simulated
the use of materials as root-end filling and perforation
repair.
The specimens were immediately placed in the Kokubo’s
corrected simulated body fluid (SBF) containing the same
phosphate concentration as blood plasma (1 mM).19 SBF was
changed every 3 days. After 4 weeks, the specimens were
examined with Scanning Electron Microscope (SEM) and
Energy Disperse X-ray Spectroscopy (EDX) to measure the
thickness of the interfacial layer and the Ca/P ratio.
2.2. Scanning Electron Microscopy (SEM) of interfacial
region
To analyze the interface of materials with the dentine,
specimens were dehydrated with ascending concentrations
of ethanol (70%, 80%, 90%, 100%). The dried specimens were
set in chemically-cured epoxy resin using vacuum impregna-
tion and ground under copious propylene glycol irrigation
using progressively finer grits of abrasive paper (600, 1000,
2400 SiC paper), diamond paste (5 mm) and 0.5 mm alumina to
produce a flat surface. The specimens were placed in a 100%
ethanol baths that were ultrasonically vibrated for 5 min. They
were then thoroughly dried, demineralized in 37% phosphoric
acid for 5 s, and deproteinized in 1% NaOCl for 5 min. After
drying at room temperature, the specimens were mounted on
 journal of dentistry 43 (2015) 241–247
aluminium stubs (Ted Pella Inc.) with adhesive carbon disks
(Ted Pella Inc.) The specimens were then sputter-coated with
gold–palladium, by means of an EMS-350 sputter-coater
(Electron Microscopy Sciences, Hatfield, PA, USA) at 20 mA
for 90 s. The specimens were observed under FEI Quanta 200
SEM (FEI, Hillsboro, Oregon, USA) at an accelerating voltage of
10 kV, and a working distance of 5–10 mm.
2.3. Determination of interfacial layer thickness and Ca/P
ratio
Three images from each specimen of both groups were
selected randomly and analyzed. For each image, three
measurements of the interfacial layer thickness (total of 9
images per group) were performed with Image J software (NIH,
Bethesda, MD). Energy Disperse X-ray Spectroscopy (EDX) was
used to measure the Ca/P ratio, resulting in 9 measurements
per group (Three measurements for each specimen). Data
were analyzed separately using Student t-tests with a = 0.05.
2.4. Transmission Electron Microscopy (TEM) and
Selective Area Electron Diffraction (SAED)
After SEM analysis, ultra-thin sections of about 90 nm were cut
by means of a diamond knife (Diatome, Bienne, Switzerland)
in an ultramicrotome (Leica Microsystems, Buffalo Grove, IL,
USA) across the interface. Unstained sections were examined
using a TEM (Tecnai T12, FEI, Hillsboro, Oregon, USA) at 110 kV.
SAED20 was performed to determine the nature of the
crystalline structure within the interfacial layer as reported
previously.9,11
Fig. 1 – Scanning electron micrographs of cement–dentine interfacial layer after four weeks of immersion in simulated body
fluid. (A and B) ProRoot MTA–Dentine; (C and D) Biodentine–dentine. d: dentine, IL: interfacial layer.
243
3. Results
3.1. Microscopy of interfacial region of MTA/Biodentine
and root dentine
The scanning electron microscopic images of the interfacial
region are shown in Fig. 1. MTA group showed the presence of
a distinguishable interfacial layer between cement and
dentine (Fig. 1A and B) and also demonstrated tag-like
structures extended to the dentinal tubules (Fig. 1B). In
Biodentine group, separated interfacial layer attached to the
dentine was seen (Fig. 1C). It also frequently showed the gap
without interfacial layer between cement and dentine
(Fig. 1D).
3.2. Interfacial layer thickness and Ca/P ratio
The graphs of interfacial layer thickness and Ca/P ratio are
shown in Fig. 2. The thicknesses of the interfacial layer for
MTA and Biodentine were 14.5 mm and 4.8 mm, respectively
(P < 0.001). Ca/P ratios calculated from EDX data were 4.1 for
MTA and 2.7 for Biodentine, which were not significantly
different (P > 0.05).
3.3. TEM and SAED
Transmission electron microscopy of specimens revealed
partially demineralized layers along the dentine (likely caused
by use of EDTA) that were approximately 0.5 mm thick for both
groups (Fig. 3A and D). At higher magnification, TEM showed
244 journal of dentistry 43 (2015) 241–247

Fig. 2 – (A) Thickness of interfacial layer; (B) and Ca/P ratio. Asterisk indicated the statistical significant difference (P < 0.05).

Fig. 3 – Transmission electron micrographs of cement–dentine interface and Electron Diffraction patterns after four weeks of
immersion in simulated body fluid. (A and B) ProRoot MTA–dentine; (D and E) Biodentine–dentine. (C and F) Electron
diffraction patterns were acquired from the area indicated with arrows in (B) and (E), respectively.

the presence of non-crystalline spherical aggregates (about
10–20 nm in diameter) on top of demineralized layers (Fig. 3B)
and even inside the dentinal tubules in the Biodentine group
(Fig. 3E). The arrows in Fig. 3B and E indicate the centres of the
electron diffraction. In the electron diffraction, dim and broad
ring patterns were observed in both groups (Fig. 3C and F),
which indicate that ACP were formed after soaking in SBF for 4
weeks.
4. Discussion
The bioactivity of MTA has been attributed to its superior
sealing ability and biocompatibility over other filling materials
such as amalgam, IRM1, Super EBA1. An important finding in
this study was the average Ca/P ratio of 4.1 at the interface of
MTA and dentine. This finding is comparable to findings by
Sarkar et al.9 (Ca/P ratio of 5.8) and Reyes-Carmona et al.11 (Ca/
P ratio of 5.1) in the MTA–dentine interface. The interfacial
precipitates have been described as hydroxyapatite9 or
calcium-deficient carbonated apatite.11 The mechanisms
involved in the formation of the interfacial layer include
release of Ca2+ ions into the phosphate containing environ-
ment, during and after setting, and the formation of ACP
precipitate which subsequently transforms into apatite
crystals.11 Formation of apatite crystals at the interface of
MTA and dentine has been correlated to its sealing ability
and biocompatibility.9,21 However, detailed evaluation of
data presented in these studies shows that the Ca/P ratios
at the MTA–dentine interface are much higher than the Ca/P
ratio in ideal stoichiometric crystalline hydroxyapatite
Ca10(PO4)6(OH)2 (1.67)22 and those in human body (1.5–1.7).23
 journal of dentistry 43 (2015) 241–247
This means that the precipitates in the MTA–dentine interface
might not be hydroxyapatite as previously believed. On the
other hand, XRD analysis of precipitates formed on the surface
of MTA in a PBS solution revealed that the precipitates are
hydroxyapatite crystals.21 Therefore, there might be a differ-
ence between the precipitates formed on the surface of MTA
and precipitates formed at the interface of MTA and dentine.
An explanation for this phenomenon is that phosphate from
the soaking solution cannot reach the material–dentine
interface as much as it would contact the material’s surface.
In addition, the ion composition of the environment affects
the composition of precipitates.8 Studies on tricalcium silicate
cements have used several different phosphate-containing
solutions such as PBS,1,11 Hanks Balanced Salt Solution
(HBSS)24 and Synthetic Tissue Fluid (STF)9 as the environment
in which the bioactivity of the cements was evaluated. The
concentrations of phosphate in PBS and STF were approxi-
mately 9–10 mM11,13 and 9.56 mM9 (calculated from data
presented in the article) respectively, which is significantly
higher than blood plasma (1 mM).19 Apatite crystals formed in
solutions with different ion concentrations than blood plasma
differed from bone apatites.25 Studies have shown that an
apatite with a composition and structure equal to, or close to,
those of bone apatites would be produced if the test solution
has ion concentrations equal to, or close to, those of blood
plasma.25,26 Therefore, when the experimental solutions were
not similar to the physiological environment,9,11,21 the
outcome of studies on the bioactivities of calcium silicate
cements should be carefully interpreted. Indeed, Gandolfi
et al.24 showed that bioactivity of tricalcium silicate cement in
HBSS (0.776 mM of phosphate), was represented by the
formation of superficial Ca-rich layer (calcium carbonate or
calcite layer) on the surface of materials, was less prominent
than in Dulbecco’s PBS (9.56 mM of phosphate). Use of SBF,
introduced by Kokubo and Takadama,19 is an advantage in this
study which guarantees the similarity of findings to what
happens in the body environment. On the other hand, even
though we used SBF, analysis showed that precipitates at the
MTA–dentine interface were not hydroxyapatites according to
EDX and TEM/electron diffraction data. Although the Ca/P
ratio in the Biodentine–dentine interface was numerically
lower than MTA group on average, it was still higher than the
ideal ratio of stoichiometric hydroxyapatite (1.67) or normal
range of hydroxyapatite in human body (1.5–1.7).
So far, studies on the interface between tricalcium silicate-
based cements and dentine were mainly done with SEM/
EDX.9,11,12 Only one study with TEM was reported by
Leiendecker et al.27 in which the bioactivity of calcium silicate
materials was not the main focus of the study. The high
resolution microscopic technique with TEM generates excel-
lent information on crystalline shape and structure, and along
with electron diffraction analysis, it gives information about
the crystal structure. In this study, the typical needle-shape
apatite crystal was not observed from TEM examination of
either material; rather, it showed non-crystalline spherical
aggregates in the interface. This result is in contrast to other
studies using SEM/EDX analysis9,11 that claimed hydroxyapa-
tite was formed in the interface. To analyze the crystal
structure, the electron diffraction was performed on spherical
aggregates on the surface of partially demineralized dentine
245
and dentinal tubules from both groups. Results of the present
study showed a dim, broad ring pattern, which is typical of
ACP. Similarly, a study by Tay et al.1 showed the initial
formation of ACP with TEM/electron diffraction when port-
land cement blocks were immersed in phosphate buffered
saline for 10 days. The ACP was later transformed to calcium-
deficient, poorly crystalline, B-type carbonated apatite crystal-
lites. On the contrary, our results did not show the
transformation to apatite from ACP even after 4 weeks of
observation. This could be caused by using different soaking
solutions (PBS vs SBF) and different examination sites
(precipitates vs interface). These differences could be affected
by the availability and accessibility of phosphorous ions to
form apatite crystals.
The clinical significance of the aforementioned finding is
that there would be concerns about the stability of the
interface of biomaterial and dentine over time. Studies have
shown that biodegradation of calcium phosphate biomaterials
is directly influenced by the type of material crystallization
and it caused a decrease in material volume as well as particle
formation causing phagocytosis by numerous macrophages
and osteoclasts.28 For instance, tricalcium phosphate was
more biodegradable than hydroxyapatite when cylinders of
each material were implanted in the tibiae of rabbits over nine
months.29 Fibroblasts and multinucleated cells (macrophages
and monocytes) can solubilize the calcium-phosphate crystals
and absorb bioactive materials.30 Long-term (5-year) follow-up
of patients who received periapical surgery with MTA root-end
fillings showed a decrease in the success rate of the
treatment31 compared to the short-term (1-year) outcome of
the same patient population.32 According to the findings of the
present study, biodegradation of the MTA–dentine interface
and breakage of the root-end seal leading to the communica-
tion between possible residual bacteria and periapical tissue
might be an explanation for the reduction in the success rate
of the treatment over time.
A limited number of studies are available on bioactivity of
Biodentine. Formation of a Biodentine–dentine interfacial
layer was demonstrated by Han and Okiji.10 They evaluated
the bioactivity of Biodentine versus MTA by measuring the
amount of ions incorporated from material into the adjacent
dentine in the presence of PBS. The elemental uptake of Ca, Si
was significantly higher for Biodentine. They also showed
formation of tag-like structures extending from the material
into dentinal tubules. Atmeh et al.18 showed the formation of
an interfacial layer and a tag-like structure in Biodentine–
dentine interface of specimens soaked in distilled water for 4
days. In order to simulate in vivo conditions, Camilleri et al.33
soaked Biodentine specimens in HBSS and verified formation
of superficial hydroxyapatite crystals. Outcomes of the
present study confirm, for the first time, the bioactivity of
Biodentine in SBF and formation of a Biodentine–dentine
interfacial layer.
In an animal model, Tran et al.17 showed the formation of
homogenous continuous dentinal bridges with well-distin-
guishable dentinal tubules underneath Biodentine following
direct pulp capping. Biodentine caused proliferation and
differentiation of immortalized murine pulp cells to odonto-
blast-like cells and increased expression of collagen-I gene.34
These data could indirectly document the bioactivity of
246 journal of dentistry 43 (2015) 241–247
Biodentine. Recently, a histological study on healthy human
pulps capped with either Biodentine or MTA showed no
significant difference in biological outcomes.35 The outcome of
the present study confirms the bioactivity of Biodentine in an
environment similar to the human body and supports the
aforementioned findings.
Our findings show that the thickness of the interfacial layer
in the Biodentine group is significantly lower than the MTA
group. This finding might be attributed to the reduced setting
time of Biodentine due to the addition of calcium chloride to its
liquid, which could result in reduced time of interaction
between calcium from Biodentine and phosphate from SBF.
Reduced setting time is a clinical advantage for Biodentine
when being used as a dentine replacement under composite
restorations.15 However, reduction in setting time might affect
other biological properties of the material. Our findings show a
significant reduction in the thickness of the interfacial layer in
Biodentine specimens compared to MTA. This is not in
accordance with previous reports on accelerated tricalcium
silicate cement11 which showed increased bioactivity follow-
ing addition of calcium chloride. The chemical differences
between Biodentine and materials tested in those studies and,
more importantly, the soaking media used in those experi-
ments (PBS vs SBF), might be the reasons for the different
findings. Additionally, none of the studies evaluated changes
in the thickness of the cement–dentine interfacial layer after
addition of calcium chloride. Moreover, unlike the MTA group,
SEM examination of specimens in this study showed frequent
gaps in the Biodentine–dentine interface (Fig. 1D). Manufac-
turer’s instructions indicate that Biodentine should be pre-
vented from exposure to water and fluid during the initial
setting. However, in this study, specimens from both groups
were immersed in SBF immediately to simulate the clinical
situation. This excessive moisture for Biodentine might
hamper the setting reaction resulting in separation from the
dentine. This was not the case in MTA group.
Within the limitations of this in vitro study, Biodentine
demonstrated the potential for bioactivity by producing an
interfacial layer on the root canal dentine in the simulated
body fluid. Ca/P ratio of the interfacial layer was not
statistically different between MTA and Biodentine, but the
thickness in Biodentine group was significantly lower. The
clinical implications of a different thickness of interfacial layer
have not been reported yet. TEM analysis of interfacial layer of
both materials showed formation of amorphous calcium
phosphate but not hydroxyapatite. The faster setting time and
better handling property of Biodentine could benefit the
clinician in some way but any improvements of physical
properties should be accomplished without concomitant
sacrifice in biocompatibility and bioactivity. Further studies
in this area are recommended.
Acknowledgements
This study was partly supported by Sherill-Ann Siegel Endodon-
tic Research Award from University of Maryland School of
Dentistry. The authors would like to thank Drs. Ru-Ching Hsia
and Wen Chiou for their assistance in SEM and TEM analyses.
The authors deny any conflict of interest related to this study.
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