REVIEW ARTICLE

Bioactive and Biomimetic Restorative Materials:

A Comprehensive Review. Part II
STEVEN JEFFERIES, MS, DDS, PhD

ABSTRACT
This second part (Part II) of a two-part comprehensive review of bioactive and biomimetic restorative materials
reviews the calcium aluminate-based restorative dental materials. Part II explores the development, composition,
properties, and application of the bioactive calcium aluminate-based materials that have been developed for several
indications in restorative dentistry.

CLINICAL SIGNIFICANCE
Bioactive materials have evolved over the past three decades from relatively specialized, highly biocompatible, but
low-strength dental materials to now emerge in product compositions for expanded clinical uses in restorative
dentistry. Further developments to meet additional restorative clinical needs are anticipated in the newly emerging
category of dental materials.
(J Esthet Restor Dent 26:2739, 2014)

CALCIUM ALUMINATE CEMENTS

Similar to the calcium silicate cements (CSCs), the
calcium aluminate cements (CAC) are also derived
from the class of cements called hydraulic
or natural cements. Their hydrating solution is water
with 30 to 90 ppm lithium to accelerate the hardening
process. A typical CAC contains prereacted
constituents as follows: Al2O3 = 43%; CaO = 19%;
H2O = 15%; ZrO2 = 19% (silicon, iron, magnesium,
titanium, and alkali oxides less than 10%). The calcium
aluminate undergoes very rapid hydration with a setting
reaction at a pH of 11.4 to 12.5 and the formation of
the reaction products Katoite and Gibbsite. The
chemical reaction forming the CAC is depicted as
follows:1

3CaO Al 2 O3
12H 2 O
+
Calcium Aluminate Water
Ca [ Al (OH )4 ]2 (OH )4 4 Al (OH )3
+

Gibbsite
Katoite
Mechanistically, water dissolves the calcium aluminate
powder with the subsequent formation of calcium ions
calcium ions (Ca2+), aluminum hydroxyl ions (Al(OH)4-,
and hydroxyl ions (OH-). This activity is then followed
almost immediately by precipitation of new solid phases
(Katoite and Gibbsite) as the solution reaches
saturation. These precipitates grow until they meet, and
a connected cluster of hydroxide particles is formed
continually. Crystallization of the phases proceeds and
the hydrates grow in size from nanometers (nm) to
microns (m).1

Professor, Kornberg School of Dentistry, Temple University, Restorative Dentistry, Philadelphia, PA, USA
This segment is the second part (Part II) of a two-part comprehensive review of bioactive and biomimetic restorative materials. Part I considered the
calciumsilicate-based dental materials. Part II will now review the calcium aluminate-based restorative dental materials.

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There have been two specic restorative dental

products that have appeared to date based on calcium
aluminate chemistry: one as a direct restorative material
(Doxadent [DD], Doxa Dental AB, Uppsala, Sweden),2
and one as a luting cement (Ceramir [CM] Crown &
Bridge, Doxa Dental AB).3 The luting cement is actually
a hybrid composition combining both calcium
aluminate and glass ionomer chemistry.3,4 The glass
ionomer component contains both polyacrylic acid and
a reactive glass, which in the presence of the water
available in the liquid component, permits a classical
glass ionomer reaction. The manufacturer claims that
the glass ionomer component contributes to a low
initial, short-duration pH, improved ow and setting
characteristics, early adhesive properties to tooth
structure, and early strength properties. In contrast, the
calcium aluminate component in the cement is
reported to contribute to: increased strength and
retention over time; biocompatibility; sealing of tooth
material interface; bioactivity-apatite formation; stable,
sustained long-term properties and lack of
solubility/degradation; and ultimate development of a
stable basic cement pH. Nevertheless, this review will
rst consider another calcium aluminate material for
dentistry that preceded the introduction the calcium
aluminateglass ionomer luting material, CM.

USE OF CALCIUM ALUMINATE AS A

DIRECT DENTAL RESTORATIVE MATERIAL
Clinical use of predominantly CACs appear
approximately 8 to 10 years after the rst
documentation of mineral trioxide aggregate
(MTA)/calcium silicate/Portland-type cements use in
dentistry. DD was a powder-liquid two-component
CAC composed of a powder component containing
calcium aluminate powder and other components
described later, and a liquid component containing
water and an accelerator comprising a lithium salt. The
material is inorganic and nonmetallic, and the main
components are CaO, Al2O3, SiO2, and water. DD was
described in its 510-K approval to market document
from the Federal Food and Drug Administration as a
dental ceramic composed of CAC and oxides that is
intended to restore carious lesions or structural defects

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in teeth.4 More specically, this restorative cement was

described as composed of CAC and oxides, i.e., silica
and zirconium oxide (as well as iron oxide as a
colorant), as a ller material, and a blend of ne,
irregularly shaped particles ranging from 0.5 to 5.0 m
in diameter, and microne particles having a diameter
from 0.02 to 0.2 m. DD was intended for use as a
restorative dental material for the permanent
restoration of Class I, II, and V cavity preparations. The
product was presented in a two-component form
comprising a tablet that was saturated in a plastic well
with a specic amount of the liquid component. The
wet tablet was then condensed into the cavity
preparation.
Physical properties of this material have been described
by several researchers. The rst published research
report dealt with some important mechanical properties
(hardness, dimensional stability, compressive and
exural strength) of an experimental version of a
translucent calcium aluminate dental restorative
material.5 All samples investigated have been made
from prepressed tablets, with a compaction degree of
approximately 60%, hydrated using a 0.15 wt% Li salt
solution as an accelerator. The samples were stored in
water at 37C between the measurements. As reference
materials, one composite, Tetric Ceram, and one glass
ionomer, Fuji II, were used with specimens prepared
according to the manufacturers recommendations. For
the reference materials, some of the properties were
published data. Vickers hardness for this novel material
ranged from 87.1 HV for a coarse ller to 102 HV for a
ne ller, and compared with Tetric Ceram (a
composite resin) at 71 and 59 HV for Fuji II (a glass
ionomer). Compressive strength (CS) using specimen
rods 7.5 mm in length and 4 mm in diameter yielded a
mean value of 182 12.5 MPa as compared with
300 MPa for Tetric Ceram and 160 MPa for Fuji II
(based on technical documentation cited by the
authors). Flexural strength was reportedly measured
according to ASTM F394 standard for ceramic
materials using a circular plate of the material
supported on three balls and loaded in the center of the
plate by a fourth ball on the opposing side until fracture
occurs. Specimens were stored in distilled water at 37C
for 14 days prior to testing. Using this method, mean

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exural strength for the calcium aluminate material was

106 28.8 MPa as compared with 142 and 41 MPa for
Tetric Ceram and Fuji II, respectively. Expansion values
for the material ranged from 0% to 0.1%, to 0.1% to
0.2% for the ne and coarse ller grain materials,
respectively. The authors concluded that the results
showed that the calcium aluminate material has
sucient mechanical properties to be used as a
permanent dental restorative taking as a reference the
International Standard Organization (ISO) 9917 and the
ISO 4049 as well as the reference materials. In addition
the results indicate that the mechanical properties are
controlled by the microstructure, which is mainly
determined by the grain size of the ller. In another
research paper describing the physical properties of the
calcium aluminate restorative material (now termed a
CBC), Lf et al. report on the diametral tensile
strength (DTS). exural strength, and CS of this
calcium aluminate material (believed to a DD)
compared directly with dental amalgam (Disperalloy,
DeTrey Dentsply, York, PA, USA) and a glass ionomer
restorative (Chemex, DeTrey Dentsply).6 In contrast
with the method for CS cited in the study described
previously in this review, the CS method in this report
was conducted according to ISO 9917; 1991 (cylinder
specimen dimensions of 6-mm length by 4-mm
diameter). Strength values for were obtained at a variety
of time points ranging from 1 hour to 4 weeks.
Diametral tensile and exural strength values, in this
study, were in a similar range for both the CBC
material (calcium aluminate-based) and the glass
ionomer material (Chemex) but lacked a
corresponding comparison with Disperalloy, having
only data at 1-hour time frame. CS values for the
CBC-calcium aluminate were reported as
139.7 20 MPa at 24 hours but increased signicantly
to 197.1 17 MPa at 1 week and 258 12 MPa at 4
weeks.
Sunnegrdh-Grnberg et al. also evaluated the physical
properties of DD in a series of publications.79 The aim
of the rst study was to compare a new ceramic
restorative cement for posterior restorations, DD, with
other types of tooth-colored materials for direct use as
regards to hardness and in vitro wear.7 Four hybrid
resin composites (RCs)one polyacid-modied RC,

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one resin-modied glass ionomer (RMGI) cement, one

conventional glass ionomer cement (GIC), and one zinc
phosphate cement, an experimental version as well as
the marketed version of the ceramic restorative
cementwere investigated. Hardness of the materials
was tested with the Wallace indentation tester, and
wear was tested with the Academic Centre for
Dentistry Amsterdam wear machine. All tests were
carried out on 2-week-old specimens. DD was as hard
as the zinc phosphate cement and the hardest RC. The
ceramic restorative cement wore signicantly more
than the RCs, the same as the zinc phosphate cement,
and less than the GICs. No correlation between
hardness and wear was found. It was concluded by the
authors that the ceramic restorative cement (DD) is a
rather hard material but with a relatively low wear
resistance.
Another study was concluded to determine the surface
roughness of a novel CAC (DD) intended for posterior
restorations after treatment with dierent polishing
devices in vitro.8 Forty-eight CAC specimens were
polished with diamond burs at 15,550 or 27,000 rpm,
Sof-Lex discs, Jiy points, Shofu silicone points, and
Aaba universal polishers. Amalgam specimens were
polished with Shofu silicone points and used as
reference. Roughness was measured using a
prolometer. The smoothest CAC surface was observed
after use of the ne Sof-Lex disc (roughness average
[Ra] 0.26 m). Diamond burs at higher speed,
points, and polisher gave rather similar results (Ra
0.580.72 m). An increase in surface roughness was
seen from using diamond burs at lower speed (Ra
2.3 m). Polished amalgam showed the smoothest
surface in the study (Ra 0.17). It was concluded that the
smoothest CAC surfaces were obtained with the ne
Sof-Lex discs. Dierent polishing points and diamond
burs at higher speed, which are suitable polishing
devices for posterior restorations, also gave relatively
smooth surfaces.
An additional study by this group was conducted to
compare this new restorative cement intended for
posterior restorations, DD, with other types of
tooth-colored materials with regards to exural
strength and exural modulus.9 Four hybrid RCsone

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polyacid-modied RC, one RMGI cement, one

conventional GIC, one zinc phosphate cement, and an
experimental version as well as the marketed version of
DDwere investigated. Flexural strength and exural
modulus were tested according to ISO standard 4049
and determined after 1 day, 1 week, and 2 weeks.
Together with the zinc phosphate cement, DD had the
lowest exural strengths (1322 MPa). The strongest
materials were the RCs and the polyacid-modied RC
(83136 MPa). The highest exural modulus was found
for DD (1719 GPa). The exural strength of DD
decreased signicantly from 1 to 2 weeks, whereas
exural modulus remained unchanged. The other
materials reacted in dierent ways to prolonged water
storage. It can be concluded that the restorative cement
DD had signicantly lower exural strength and
signicantly higher exural modulus than todays
materials used for direct posterior restorations.
Another group also investigated the physical properties
of the CAC, DD.10 This study compared in vitro the
mechanical properties of a directly placed ceramic
restorative material (DD) to glass ionomer (Fuji IX),
hybrid composite control (Z250), and amalgam control
(Tytin). DTS, CS, and Vickers hardness number (VHN)
were measured for 10 specimens per group (N = 480
total) with time (1 hour, 24 hours, 1 week, 4 weeks).
CS and DTS specimens were loaded to failure (Instron,
Rate of Strain = 0.5 mm/minute). VHN discs were
indented. Data were analyzed using analysis of variance
(ANOVA) and Tukeys test (p < 0.05) for pairwise
comparisons of group means at each time. The CS of
DD, in this in-vitro study, ranged from 44 6 MPa at 1
hour to 63 10 MPa at 24 hours, yet increased
signicantly at 1 week to 118 9, and appeared to level
at 4 weeks at a CS of 120 11 MPa. DTS for DD ranged
from 7 1 at both 1 and 24 hours, and also increased
signicantly at 1 and 4 weeks to 14 3 MPa and
15 3 MPa, respectively. Vickers hardness values
increased progressively from 52 4 at 1 hour to 95 2
at 4 weeks. The investigators concluded from their
ndings that for CS and DTS, DD was weakest
(p < 0.05) for all testing times except Fuji IX DTS at 1and 4-week intervals. For VHN, DD was harder than
glass ionomer, better than composite except at 1hour
and less than amalgam. Except for VHN for Z250, all

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values improved from 1 to 24 hours. Based on current

in vitro results, this novel restorative material does not
yet equal composite or amalgam CS or DTS.
The cytotoxic eects of DD were compared with
several currently used direct restorative materials.11
Specimens of three composites (QuiXl, Tetric Ceram,
Filtek Supreme)one zinc phosphate cement (Harvard
Cement), one GIC (Ketac Molar), and the CAC
(DD)were used fresh or after 7-days of pre-incubation
in cell culture medium at 37C, pH 7.2. polyvinyl
chloride strips for ISO 10993-5 cytotoxicity test were
used as positive control and glass specimens as negative
control. L-929 broblasts (5-mL aliquots, containing
3 104 cells/mL), cultivated in Dulbeccos Modied
Eagle Medium with 10% fetal calf serum, 1% glutamine,
and 1% penicillin/streptomycin at 37C/5% CO2 and
trypsinized were exposed to the specimens for 72 hours.
The cells were harvested, centrifuged, and resuspended
in 500 L of DMEM and then counted in 500 L of
DMEM for 30 seconds with a ow cytometer at
488 nm. The ANOVA comparing the six materials
showed dierent inuences on L-929 broblast
cytotoxicity (p < 0.0001). The cytotoxicity of all
specimens diminished with increasing pre-incubation
time (p < 0.0001). Fresh DD exhibited the lowest
cytotoxicity, followed by QuiXl. Ketac Molar showed
the highest cytotoxicity. After 7 days of pre-incubation,
Harvard Cement and Filtek Supreme demonstrated
more cytotoxicity than the other materials (p < 0.005).
The clinical performance of DD as a posterior
restorative material was also evaluated up to a 3-year
recall point.12,13 The aim of this study was to evaluate
intra-individually the experimental CAC (DD) and an
RC in Class II restorations. Each of 57 participants
received at least one pair of restorations of the same
size, one CAC and one RC (Tetric Ceram). Sixty-one
pairs were performed. The restorations were evaluated
clinically, according to slightly modied United States
Public Health Service criteria, at baseline, after 6
months, and 1, 2, and 3 years. One hundred and twenty
restorations were evaluated at 2 years.12 Postoperative
sensitivity was reported for ve restorations (2 RC, 3
CAC). Signicantly better clinical durability was shown
for RC. Five nonacceptable CAC restorations (8.2%)

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were observed at 6 months, 10 CAC (16.7%) and 2 RC

(3.3%) at 12 months and 11 CAC (18.3%) at 24 months.
This resulted in a cumulative failure frequency, at 24
months, of 43.3% for the CAC material and 3.3% for the
RC material. Main reasons for failure for the CAC were
partial material fracture (seven restorations), cusp
fracture (ve restorations), and proximal chip fracture
(six restorations). The CAC showed a nonacceptable
clinical failure rate for Class II restorations probably
caused by its dicult handling and low mechanical
properties. This trend continued at the 3-year recall, At
3 years, 62 out of 63 originally placed restorations were
evaluated.13 At 6 months, 9.5% nonacceptable DD
restorations were observed, 17.5% at 12 months, 24.2%
at 2 years, and 21% at 3 years, which resulted in a
cumulative failure frequency of 72.6% at the end of the
3 years for the new restorative material. Main reasons
for failure were material or tooth fracture. The authors
of this study concluded that DD showed a
nonacceptable clinical failure rate as a posterior
restorative, especially in Class II cavities. Clearly, based
on this study, this calcium aluminate-based material
appeared unacceptable as an amalgam replacement for
posterior restorations. That said and in view of the
observation that the in-vitro physical property
performance of the DD material was closer to that of
glass ionomer as opposed to composite resin or
amalgam, it is interesting to speculate whether this
CAC compares more closely in clinical performance
with a high-strength glass ionomer restorative in
posterior restorations. A 2-year clinical investigation of
a high-strength glass ionomer in Class I and II posterior
restorations was reported in 2009.14 In this controlled,
prospective, clinical study, the highly viscous GIC Ketac
Molar was clinically assessed in Class I and Class II
cavities. Forty-nine subjects (mean age 32.3 years)
received 108 restorations placed by six operators in
conventional Black Class I and II type cavities with
undercuts after excavating primary lesions or after
removing defective restorations. At baseline and after 6,
12, and 24 months, restorations were assessed by two
independent investigators according to modied
USPHS codes and criteria. Recall rates were 83% after 6
months, 50% after 12 months, and 24% after 24 months.
Failure rates after 24 months were 8% for Class I and
40% for Class II llings mainly because of bulk fracture

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at occlusally loaded areas. This failure rate for this

highly viscous glass ionomer is proportionally similar to
failure rates for DD at 2 years recall reported by van
Dijken and Sunnegrdh-Grnberg,12 namely 10% for
Class I restorations and 43% for Class II restorations.
One nal point: This case study of the in-vitro and
in-vivo performance of DD illustrates another critical
object-lesson in the development of new dental devices,
and more specically new compositions or chemistries
in dental restorative materials. Clinical evaluations of
sucient duration are still absolutely necessary prior to
the introduction of new dental restorative materials
with new chemistries or signicant changes in
formulation prior to their introduction and marketing.

CALCIUM ALUMINATEGLASS IONOMER

LUTING CEMENT
The most recent modication in bioactive chemically
bonded cements with a predominant use in restorative
dentistry has been the introduction of a calcium
aluminateglass ionomer luting cement (CM Crown &
Bridge, originally named XeraCem). CM is a luting
agent intended for permanent cementation of crowns
and xed partial dentures, gold inlays and onlays,
prefabricated metal and cast dowel and cores, and
high-strength all-zirconia or all-alumina crowns.15,16
The cement is a water-based composition comprising
calcium aluminate and glass ionomer components, and
has been demonstrated to be bioactive.15,17 The term
bioactivity again refers to a property of this new
cement to form hydroxyapatite (HA) when immersed
in vitro in a physiological phosphate-buered saline
(PBS) solution.17 The introduction of any new cement
chemistry necessitates assessment of its laboratory and
clinical performance, and it should be noted that both
laboratory and clinical investigations were initiated and
ndings were collected prior to commercial
introduction of this material. The laboratory
performance of this new cement has been assessed with
respect to a number of performance criteria.
Assessment of CS, lm thickness, and setting time all
conformed favorability to the ISO standard for
water-based luting cements.18 Comparative in-vitro
microleakage performance of this new bioactive cement

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has also been assessed by two methodologies. Dye

leakage analysis in cemented crowns concluded that
CM demonstrated signicantly less leakage than a
conventional GIC, Ketac-Cem (KC).19 An in-vitro
bacterial leakage model comparison of CM with a
conventional glass ionomer luting cement, again KC,
and an RMGI cement (Rely X Luting Plus, RX)
demonstrated that the groups cemented with CM and
RX showed no signicant dierence in microleakage
patterns (p > 0.05), whereas both recorded signicantly
lower microleakage scores (p < 0.05) than the group
cemented with KC.19,20
Biocompatibility ranks as one of the most important
properties of a nal luting cement, and as such, a
number of in-vitro and in-vivo tests (as recommended
by American National Standards Institute/American
Dental Association (ANSI/ADA) Spec. 41 and ISO
10993) were conducted prior to the clinical
investigation to evaluate the biocompatibility of CM
Crown & Bridge cement.21 Results for the Ames test for
mutagenicity indicated that this new cement
formulation did not induce gene mutations. In-vitro
cytotoxicity testing indicated cell responses ranging
from none to mildly cytotoxic, an acceptable response.
The skin sensitization test (in guinea pigs) indicated
that this cement is not a skin sensitizer, whereas testing
for mucous membrane irritation (hamster pouch test)
indicated that it produced no local irritation.21 Pulpal
testing in Rhesus macaques, according to ANSI/ADA
Spec. 41, indicated a virtual absence of pulpal
inammation at both 30- and 85-day evaluation periods
after CM was used to cement composite resin inlays in
a Class V preparation.21
Retention is perhaps the most critical factor in the
performance of a nal luting cement. A comparative,
in-vitro crown retention study was conducted (also
prior to the clinical evaluation) to assess the retentive
properties of this new cement with noble metal (gold)
crown-copings.22 Results of this test indicated that it
demonstrated retentive values equivalent (no
statistically signicant dierence) to a self-adhesive
resin cement, Rely X Unicem, but were signicantly
higher than a conventional glass ionomer, KC, and zinc
phosphate cement.

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A clinical investigation was initiated approximately 2

years prior to the introduction of CM.2326 The aim of
this pilot clinical study (a prospective, consecutive case
series clinical study) was to assess the clinical
performance of a new bioactive cement as a luting
cement for cast high-gold alloy and noble metal
porcelain-fused-to-metal restorations. This clinical
study was conducted to determine the multiyear clinical
performance of this new bioactive dental cement (CM
Crown & Bridge) for permanent cementation. A total of
38 crowns and bridges were cemented in 17 patients.
Thirty-one of the abutment teeth were vital and seven
nonvital. Six (6) restorations were bridges with a total
of 14 abutment teeth (12 vital/2 nonvital). One xed
splint comprising two abutment teeth was also
included. Preparation parameters were recorded, as well
as cement characteristics such as working-time,
setting-time, seating characteristics, and ease of cement
removal. Baseline data were recorded for the handling
of the cement, gingival inammation, and
precementation sensitivity. Postcementation parameters
included postcementation sensitivity, gingival tissue
reaction, marginal integrity, and discoloration. All
patients were seen for recall examinations at 30 days
and 6 months.23 Fifteen of 17 subjects and 13 of 17
patients were also available for subsequent
comprehensive 1-24 and 2-year recall examination,25 and
13 patients were available for a 3-year recall
examination.26 Two-year recall data yielded no loss of
retention, no secondary caries, no marginal
discolorations, and no subjective sensitivity. All
restorations rated alpha for marginal integrity at the
2-year recall.25 Restorations available for the 3-year
recall examination included 14 single-unit full-coverage
crown restorations, four three-unit bridges comprising
eight abutments, and one two-unit splint. Three-year
recall data yielded no loss of retention, no secondary
caries, no marginal discolorations, and no subjective
sensitivity. All restorations rated excellent for marginal
integrity. Average visual analog scale scores for tooth
sensitivity decreased from 7.63 mm at baseline to
0.44 mm at 6-month recall, 0.20 mm at 1-year recall,
0.00 mm at 2- and 3-year recall. Average gingival index
scores for gingival inammation decreased from 0.56 at
baseline to 0.11 at 6-month recall, 0.16 at 1-year recall,
0.21 at 2-year recall, and 0.07 at 3-year recall. After

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periodic recalls up to 3 years, CM Crown & Bridge thus

far has performed quite favorably as a luting agent for
permanent cementation of permanent restorations.26
At the time of reporting the 3-year recall data,
additional in-vitro crown-coping retention data were
presented using CM and crown-copings utilizing
various all-ceramic crown and bridge materials. Mean
laboratory retentive forces measured for CM Crown &
Bridge were comparable with other currently available
luting agents for both metal and additionally all-ceramic
indirect restorative materials, specially all-zirconia and
lithium disillicate.26 Figure 1 depicts a lithium disillicate
e.Max crown (Ivoclar Vivadent, AG, Bendererstrasse 2,
9494 Schaan, Principality of Liechtenstein) cemented on
a mandibular left second premolar with a calcium
aluminate/glass ionomer luting cement (CM Crown &
Bridge) at 6 months postcementation. An excellent
gingival soft-tissue gingival response can be noted in
this digital photograph.

BIOACTIVITY AND INTERACTIONS WITH

DENTIN AND THE PULP
The preceding review has provided a broad overview of
the major calcium silicate- and calcium
aluminate-based dental materials that originated within

FIGURE 1. Lithium Disillicate e.Max Crown (Ivoclar

Vivadent) cemented on a mandibular left second premolar
with a calcium aluminate/glass ionomer luting cement
(Ceramir Crown & Bridge, Doxa Dental AB) at 6 months
postcementation.

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the eld of endodontics and have increasingly expanded

into the area of other, non-stress-bearing indications in
restorative dentistry. This review will now conclude
with some more recent research ndings concerning
the property of bioactivity, and the interaction of these
bioactive materials with dentin and pulpal tissue, which
have particular clinical signicance in the areas of
adhesive and restorative dentistry.
In order to better clarify the form of bioactivity
specically associated with these calcium-based dental
materials, this author suggests the use of the term
bioactive CBCs (BCBCs) to dierentiate this type of
material, specically one displaying apatite-forming
bioactivity, from phenomena associated with other
device or drug actions. That said, an important
question concerning the bioactivity of BCBCs is how
this phenomenon impacts the interaction of these
materials with both enamel and dentin. MTA and
Portland cement, in the presence of PBS, promote a
biomineralization process that leads to the formation of
an interfacial layer with tag-like structures at the
cement-dentin interface.27 BCBCs, such as MTA or
Portland cement, also appear to enhance their adhesion
to dentin through their bioactivity. This increased
adhesion to dentin was demonstrated by increased
push-out strength of these cements when inserted into
sectioned root segments and after contact with PBS for
72 hours, particularly the MTA groups.28
More in-depth analytical assessment of these BCBCs
with dentin has also been reported. The interfacial
properties of the tricalcium silicate-based restorative
material (Biodentine, Septodont, St Maure des Fosses,
France) and a GIC with dentin were studied by a
combination of advanced analytical techniques such as
confocal laser scanning microscopy (CLSM), scanning
electron microscopy (SEM), micro-Raman
spectroscopy, and two-photon autouorescence and
second-harmonic generation imaging.29 Results of this
study indicated the formation of tag-like structures
alongside an interfacial layer called the mineral
inltration zone, where the alkaline caustic eect of the
CSCs hydration products degrades the collagenous
component of the interfacial dentin. This degradation
leads to the formation of a porous structure that

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facilitates the permeation of high concentrations of

Ca(2+), OH(), and CO(3) (2) ions, leading to
increased mineralization in this region. Comparison of
the dentin-restorative interfaces shows that there is a
dentin-mineral inltration with the Biodentine, whereas
polyacrylic and tartaric acids, and their salts
characterize the penetration of the GIC.
A new type of interfacial interaction, the mineral
inltration zone, was suggested by these investigators
for these calcium-silicate-based cements.

the bonding agents containing the bioactive microllers

tested in this study showed stable bond strengths at 6
months of storage, an evident reduction of nanoleakage,
and mineral deposition after SBS storage. A second
study employed additional modications to these
bioactive microllers also yield similar favorable
results.32 Resin bonding systems containing specically
tailored Portland cement microllers may promote a
therapeutic mineral deposition within the hybrid layer
and increase the durability of the resin-dentin bond.

As was noted earlier in this review, degradation of

denuded collagen within adhesive resin-inltrated
dentin is a pertinent problem in dentin bonding.
Utilizing a remineralization medium consists of a
Portland cement/simulated body uid (SBF) that
includes polyacrylic acid and polyvinylphosphonic acid
biomimetic analogs for amorphous calcium phosphate
dimension regulation and collagen targeting; this
research report describes the remineralization of
incompletely inltrated resin-dentin interfaces created
by etch-and-rinse adhesives.30 The objective of this
study was to remineralize resin-free, acid-etched dentin,
with evidence of intrabrillar and interbrillar
remineralization. Using this concept that the authors
termed biomimetic remineralization, both interbrillar
and intrabrillar apatites became readily discernible
within the hybrid layers after 2 to 4 months. In
addition, intraresin apatite clusters were deposited
within the porosities of the adhesive resin matrices.
Thus, the use of BCBCs or their derivatives, as part of a
biomimetic remineralization scheme, may provide an
alternative strategy to extend the longevity of
resin-dentin bonding.

The eect of smear layer removal on the push-out bond

strength between radicular dentin and three CSCs in
comparison with gutta percha and sealer has recently
been examined.33 Two major groups: (1) smear layer
preserved, and (2) smear layer removed using irrigation
with 17% ethylenediaminetetraacetic acid were
examined. Roots within each major group were further
divided into four subgroups according to the obturation
material used: (1) ProRoot MTA, (2) Biodentine, (3)
Harvard MTA, and (4) gutta percha and AH-plus sealer
(Dentsply DeTrey, Konstanza, Germany). Obturated
roots were stored in synthetic tissue uid for 7 days to
allow maximum setting of the root lling materials.
Three 2-mm-thick slices were obtained from each root
at dierent section levels (coronal, middle, apical). The
canal diameters and slice thickness were measured, and
the adhesion surface area for each slice was calculated.
Push-out bond strength test was carried out using a
universal testing machine. The bond failure mode was
assessed under an optical microscope at 40. The mean
push-out bond strength in groups 1A, 2A, and 3A were
7.54 (1.11), 7.64 (1.08), and 8.79 (1.55) MPa,
respectively, whereas those for groups 1B, 2B, and 3B
were 6.58 (1.13), 6.47 (1.08), 7.71 (1.81) MPa,
respectively. In the gutta percha and sealer groups, the
push-out bond strength means were 1.98 (0.48) and
2.09 (0.51) MPa in the preserved and removed smear
layer groups, respectively. The push-out strength values
were signicantly reduced when the smear layer was
removed in the CSC groups (p < 0.05), whereas no
signicant dierence was detected in the gutta percha
and sealer groups. Based on the conditions of this
ex-vivo study, it was concluded that smear layer
removal is detrimental to the bond strength between
CSCs and dentin.

This concept of hybrid-zone dentin remineralization

using BCBCs (or their components) has been extended
most recently to novel experimental formulations for
dentin bonding agents.31,32 One study aimed at
evaluating the therapeutic bioactive eects on the bond
strength of three experimental bonding agents
containing modied Portland cement-based microllers
applied to acid-etched dentin and submitted to aging in
SBF solution (SBS). The analysis of the material-dentin
interface was utilized CLSM and SEM morphological
analysis.31 All the resin-dentin interfaces created using

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Several investigators have attempted to capture the

in-vivo tooth/material ultramorphology of BCBC
materials. The aim of one in-vivo study was to evaluate
the interfacial marginal adaptation of a CAC, DD, and
to compare it intraindividually with an RC, tetric
ceram/syntac single-component (TC/SS), in Class II
cavities.34 Sixteen Class II box-shaped, enamel-bordered
cavities were prepared in eight premolars scheduled to
be extracted after 1 month of service for orthodontic
reasons. The interfacial marginal adaptation (internal
surfaces) of the restorations was evaluated by a
quantitative SEM analysis using a replica method. DD
showed a statistically signicant, lower degree of
gap-free adaptation to enamel compared with TC/SS:
84% versus 93%. To dentin, DD showed a signicantly
better adaptation than TC/SS: 72% versus 49%. A high
frequency of enamel fractures perpendicular to the
margins was observed for the DD restorations, which
may be explained by an expansion of the
calcium-aluminate cement. It can be concluded that
DD showed a better adaptation to dentin, whereas
TC/SS showed a better adaptation to enamel. Another
research paper investigated the interface formed in vivo
between the calcium aluminate-based dental lling
material (DD) and teeth.35 Class 1 occlusal llings were
made in wisdom teeth (3rd molars) and extracted after
up to 4 weeks. Polished cross-sections of the teeth were
studied with SEM, focused ion beam microscopy, and
transmission electron microscopy. In order to analyze
the distribution of elements at the interface elemental
mapping was performed using scanning transmission
electron microscopy and energy-dispersive X-ray
spectroscopy. The results showed that a tight bond
forms between the lling material and tooth, and no
gap could be found even at high magnication. A 100
to 200 nm wide zone with an increase in oxygen was
detected in the enamel next to the lling. The zone was
denser than the rest of the enamel. Elemental mapping
indicated an increase of silicon and a decrease of Ca at
the interface. Dark eld imaging and EDX mapping also
showed that the calcium aluminate system formed
apatite in situ during hardening through precipitation.
Both of these investigations demonstrate the ability of a
bioactive calcium aluminate lling material to form an
intimate interface between both enamel and dentin
tooth structure in vivo.

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While the vast majority of in-vitro studies utilize an

SBF, such as PBS, however, only a limited amount of
research has been devoted to formation of HA in
contact with actual biological uids which contain
inorganic phosphate sources. A recent research
publication has documented the uptake of inorganic
phosphate and the formation of apatite-like calcium
phosphate on the surface of the calcium aluminate/glass
ionomer luting agent (CM) in the presence of human
saliva.36 The objective of this investigation was to study
the surface reactions occurring in human salvia on a
novel dental cement. CM Crown & Bridge, a
bioceramic luting agent that has been discussed earlier
in this review, was evaluated by immersing discs
made from the cement in human saliva and PBS for
7 days, after which they were dried and analyzed. The
analytical methods used in order to verify HA
formation on the surface were grazing incidence X-ray
diraction, SEM, and X-ray photoelectron
spectroscopy. All results showed that HA was formed
on the surfaces of samples stored in saliva as well as on
samples stored in PBS. The authors speculate
about the possibility of a dental luting cement able
to promote natural formation of HA at the tooth
interface in order to increases the stability and
durability of the system and could help prevent
secondary caries.
The adhesive shear bond strength of the calcium
aluminate/glass ionomer luting agent, CM, to enamel,
dentin, and various restorative materials, has been
documented both by the manufacturer,37 Doxa Dental
AB, and also an independent testing laboratory (The
Dental Advisor).38 The manufacturers bond strength
data (without pretreatment) was 11 MPa to dentin,
8.4 MPa to enamel, 10.2 MPa to gold, 7.5 MPa to
aluminum oxide ceramic, and 8.2 MPa to zirconium
oxide.37 The independent testing laboratories bond
strength data (without pretreatment) was 8.6 MPa to
supercial dentin, 16 MPa to gold alloy, 10.4 MPa to
Ivoclar Porcelain System e.max ZirCAD ceramic, and
12.0 MPa to BruxZir zirconium oxide.38 Again, the
evidence of adhesive strength to tooth structure and
dental material substrates suggests the adhesive
potential of both the calcium silicate- and calcium
aluminate-based BCBC materials.

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Pulpal biocompatibility is a critical necessity for liners,

bases, direct lling materials, and most importantly
luting cements. Although evidence-based literature
concerning the pulpal response to each of the bioactive
materials and chemistries has been previously discussed
in this review, some recent research reports have now
provided even stronger guidance regarding the use of
these bioactive materials in vital pulp therapies such as
direct and indirect pulp capping. The recent availability
of human clinical and pulp histology has provided a
clearer picture on this topic.
With regard to a comparison of the direct pulp capping
performance of MTA versus calcium hydroxide
Ca[OH]2, one research study was conducted on 90
intact rst and second premolars of human maxillary
and mandibular teeth.39 The teeth were randomly
assigned into three groups of 30 each. Under local
anesthesia, teeth were exposed and capped either with
gray mineral trioxide aggregate, white mineral trioxide,
or Dycal. After 30, 60, and 90 days, 10 teeth of each
group were extracted and prepared for histological
observation. The calcied bridge in teeth that were
capped with GMTA was signicantly thicker than that
measured in the Dycal pulp capped teeth at 30 and 60
days (p = 0.015 and p = 0.002, respectively), whereas
WMTA showed signicantly thicker calcied bridge
than Dycal at 90 days (p = 0.02). In addition, GMTA
specimens showed signicantly less inammation
compared with Dycal samples at 90-day interval
(p = 0.019). No signicant dierence was found between
GMTA and WMTA in terms of calcied bridge
thickness and pulp inammatory response to the
capping materials (p > 0.05). Based on the result of this
study, the authors state that both types of MTA can be
suggested as the materials of choice for direct pulp
capping procedure instead of Dycal calcium hydroxide
cement.
To assess the eectiveness of MTA used as an indirect
pulp-capping material in human molar and premolar
teeth, another human clinical study was conducted.40
Sixty teeth underwent an indirect pulp-capping
procedure with either MTA or calcium hydroxide
cement (Dycal). Calcium hydroxide was compared with
MTA, and the thickness of the newly formed dentine

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was measured at regular time intervals. The follow up

was at 3 and 6 months, and dentin formation was
monitored by radiological measurements on digitized
images using Mesurim Pro software. At 3 months, the
clinical success rates of MTA and calcium hydroxide
were 93% and 73%, respectively (p = 0.02). At 6 months,
the success rate was 89.6% with MTA and remained
steady at 73% with calcium hydroxide (p = 0.63). The
mean initial residual dentine thickness was 0.23 mm
and increased by 0.121 mm with MTA and by
0.136 mm with calcium hydroxide at 3 months. At 6
months, there was an increase of 0.235 mm with MTA
and of 0.221 mm with calcium hydroxide. A higher
success rate was observed in the MTA group relative to
the Dycal group after 3 months, which was statistically
signicant. After 6 months, no statistically signicant
dierence was found in the dentine thickness between
the two groups. The authors concluded that additional
histological investigations are needed to corroborate
these ndings, but that these nding suggest a superior
performance of MTA in indirect pulp capping.
A recently published, large, randomized, controlled,
clinical trial has provided pivotal information in the
debate regarding use of a calcium silicate-based MTA
material versus the traditional use of calcium hydroxide
(CaOH) in direct pulp capping.41 This practice-based,
randomized, clinical trial evaluated and compared the
success of direct pulp capping in permanent teeth with
MTA or CaOH. Thirty-ve practices in Northwest
Practice-Based Research Collaborative in
Evidence-Based Dentistry were randomized to perform
direct pulp caps with either CaOH (16 practices) or
MTA (19 practices). Three hundred seventy-six
individuals received a direct pulp cap with CaOH
(N = 181) or MTA (N = 195). These individuals were
followed for up to 2 years at regular recall
appointments or as dictated by tooth symptoms. The
primary outcomes were the need for extraction or root
canal therapy. Teeth were also evaluated for pulp
vitality, and radiographs were taken at the dentists
discretion. The probability of failure at 24 months was
31.5% for CaOH versus 19.7% for MTA (permutation
log-rank test, p = 0.046). This large randomized clinical
trial appears to have provided conrmatory evidence
for a superior performance with MTA as a direct

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BIOACTIVE AND BIOMIMETIC RESTORATIVE MATERIALS Jefferies

pulp-capping agent as compared with CaOH when

evaluated in a practice-based research network for up
to 2 years.
A concluding footnote on this topic of BCBCs and
direct pulp capping comes with a recent human clinical
study involving Biodentine and MTA.42 The purpose of
the present study was to compare the response of the
pulp-dentin complex in human teeth after direct
capping with this new tricalcium silicate-based cement
with that of MTA. Pulps in 28 caries-free maxillary and
mandibular permanent intact human molars scheduled
for extraction for orthodontic reasons were
mechanically exposed and assigned to one of two
experimental groups, Biodentine or MTA, and one
control group. Assay of periapical response and clinical
examination were performed. After 6 weeks, the teeth
were extracted, stained with hematoxylin-eosin, and
categorized using a histological scoring system. The
majority of specimens showed complete dentinal bridge
formation and an absence of inammatory pulp
response. Layers of well-arranged odontoblast and
odontoblast-like cells were found to form tubular
dentin under the osteodentin. Statistical analysis
showed no signicant dierences between the
Biodentine and MTA experimental groups during the
observation period. Within the limitations of this study,
Biodentine had a similar ecacy in the clinical setting
and may be considered an interesting alternative to
MTA in pulp-capping treatment during vital pulp
therapy.

4. Recent animal and human pulpal histology suggest

that a tricalcium silicate bioactive material,
Biodentine, is equivalent to MTA in direct pulp
capping.
5. Clinical indications for use of bioactive cements
have expanded further into uses such as lining and
bases (Biodentine) and luting cements for crown
and bridge applications with the introduction and
laboratory/clinical validation of a calcium
aluminate/glass ionomer luting cement (CM Crown
& Bridge).
6. Strength and physical properties of BCBCs have
increased gradually and are now approaching
the CS range of conventional, water-based
GICs.

DISCLOSURE AND ACKNOWLEDGEMENTS

The authors institution has received research funding
from Doxa Dental AB, Uppsala, Sweden, the company
that markets CM Crown & Bridge Cement. The author
also holds common stock in the company Dentsply
International, the company that markets ProRoot
MTA.

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CONCLUSIONS
1. MTA (gray MTA and white MTA) have
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variety of clinical indications, including pulp cap,
pulpotomy, root ending lling, repair of root
resorption, repair of root perforations, and
apexication.
2. Additional materials with compositions similar to
MTA have been introduced, including MTA
Angelus, Bioaggregate, iRoot BP, and BP Plus.
3. In the area of vital pulp therapy, MTA appears to
be clearly equivalent and possibly superior to
classical CaOH in terms of direct pulp capping.

2013 Wiley Periodicals, Inc.

DOI 10.1111/jerd.12066

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Reprint requests: Steven Jefferies, MS, DDS, PhD, Kornberg School of

Dentistry, Temple University, Restorative Dentistry, 3223 N. Broad Street,
Philadelphia, PA 19140, USA; Tel.: 215-707-3751; Fax: 215-707-2840;
email: SJefferies@dental.temple.edu

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