Clinical Oral Investigations (2020) 24:1065–1072

https://doi.org/10.1007/s00784-019-03003-x

ORIGINAL ARTICLE

Assessment of bone healing after mineral trioxide aggregate

and platelet-rich fibrin application in periapical lesions using
cone-beam computed tomographic imaging
Nazife Begüm Karan 1 & Banu Aricioğlu 2

Received: 23 February 2019 / Accepted: 28 June 2019 / Published online: 18 July 2019
# Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract
Objectives The aim of this study was to compare the effects of mineral trioxide aggregate (MTA) and platelet-rich fibrin (PRF)
use on periapical healing in surgically treated periapical lesions using three-dimensional (3D) cone-beam computed tomographic
(CBCT) imaging.
Materials and methods A total of 40 periapical lesions undergoing apical surgery were selected between December 2016 and
November 2017. The participants were randomly divided into four study groups: control, MTA, PRF, and MTA+PRF. No
interventions were made in the control group except root-end resection. Routine radiographs were taken in the 3rd, 6th, and
12th months. The volume and density of periapical lesions at the 1-year follow-up were compared with the pre-op values using
the MIMICS software program. Primary healing of the periapical tissues was evaluated, and the outcomes were noted.
Results Post-op volume values were significantly decreased, and density values were significantly increased according to the pre-
op measurements. In the post-op volume evaluation between the groups, significant differences were observed in the MTA and
MTA+PRF groups compared with the control group (p < 0.005). However, no substantial significance was noted between the
control and PRF groups. There were no significant differences in post-op density calculations between all groups.
Conclusion and clinical relevance High success rates were achieved using MTA in periapical lesions in endodontic microsurgery.
The application of PRF to the surgical cavity may not necessarily improve outcomes. Further studies are needed with long-term
follow-up.
Trial registration number: NCT03743987 (The Effect of MTA and PRF Application in Periapical Lesions).

Keywords Periapical lesions . Apical surgery . Root resection . Retrograde filling . MTA . PRF

Introduction [1]. Nevertheless, in the presence of unreached root canals in

the orthograde route, apical resection (root-end resection)
Through the root canal, bacteria and their toxins may reach to should be considered the treatment of choice in failed re-treat-
periapical tissues and create pathologic changes. Success rates ments, as well as for persistent infections and cystic forma-
of over 90% for periapical healing have been reported with the tions [2]. Infected necrotic tissues can be removed in
provision of adequate cleaning through endodontic treatment periapical surgery, and consequently, the potential loss of a
tooth is prevented [3].
Periapical surgical procedures comprise elimination of
* Nazife Begüm Karan necrotic and infected tissues, resection of the apical part of
karanbegum@gmail.com the tooth (apicoectomy), and preparation of the apical cav-
ity for the insertion of a retrograde filling material. In ad-
Banu Aricioğlu dition, proper condensation of the retrograde filling mate-
banu.arc@gmail.com
rial (gutta-percha or others) is crucial for the long-term
1
Faculty of Dentistry, Department of Oral &Maxillofacial Surgery,
success of apical resections [4].
Recep Tayyip Erdoğan University, Rize, Turkey Some studies have shown that, when the filling of the root
2
Faculty of Dentistry, Department of Endodontics, Recep Tayyip
canal is strong and condensation is excellent, decent healing
Erdoğan University, Rize, Turkey of periapical tissues can be achieved regardless of the use of
1066
retrograde filling materials [5, 6]. However, in many ex vivo
studies, it has been reported that the growth of bacteria in root
canals and their transmission to periapical tissues can only be
prevented by retrograde fillers and thus, it has been accepted
as a routine treatment protocol [7, 8].
During the last decade, many new materials and techniques
have been developed. Mineral trioxide aggregate (MTA), a
biomaterial that has been successfully used in root canals since
1993, is a hydrophilic material consisting of tricalcium sili-
cate, tricalcium oxide, tricalcium aluminate, and silicate oxide.
Its setting time is nearly 150 min, and its pH is over 12 [9].
With its biologic and physical superiority, it has become an
excellent retrofilling material. In vivo and in vitro studies have
shown that the material has good sealing properties, as well as
harmony with the periapical tissues, triggering cellular renew-
al and supporting cementation and bone formation [10, 11]. It
is the most popular material used by endodontists all over the
world, and continues to be the gold standard for comparing
new materials [12].
Platelet-based treatments were developed in the early
1990s after the identification of various growth factors re-
leased from the α-granules of platelets [13]. The slow poly-
merization mode confers a particularly favorable physiologic
architecture to the platelet-rich fibrin (PRF) membrane to sup-
port the healing process [14]. It mimics the needs of physio-
logic wound healing and restorative tissue processes by locat-
ing and sustaining growth factors and proteins, and is used to
stimulate and accelerate soft tissue and bone healing with
osteogenic potential [15, 16].
For successful periapical healing, a decrease in the size of the
radiolucent area and bone tissue healing should be observed. It
is known that periapical radiography cannot reflect the real size
of the periapical lesion [16]. For the best diagnosis, the use of
cone-beam computed tomography (CBCT) has increased and
some researchers demonstrated an almost complete agreement
between CBCT and histopathologic diagnosis [17, 18].
The aim of this study was to evaluate the effects of different
successful biocompatible and biologic materials (MTA and
PRF) on periapical healing using volume measurements with
CBCT. MTA and PRF were used both separately and in com-
bination after apical resection and compared with a control
group. The study was conducted to analyze the long-term
post-operative changes of volume and bone density to com-
pare the healing of the groups. The null hypothesis established
was that there would be no significant differences in healing
rates between the application of PRF and/or MTA and apical
resection without any intervention on periapical healing.
Materials and methods
This study was approved by the Ethics Committee of RTE
University/Rize-Turkey (No: 2016/88). Power analysis was
Clin Oral Invest (2020) 24:1065–1072
performed using the G-Power software package (99.97%
power, two-sided 5% significance level) to predict the number
of cases, and a previous study was used to calculate the sample
size [19]. It was found that at least 10 periapical lesions (40 in
total) were required in each group.
Periapical lesions of failed root-canal treatments, at least 1-
year previous retreatment cases, lesions two times greater in
width than the periodontal membrane with no active site in-
fections, and systemically healthy patients aged between 18
and 50 years were selected for the study. Unhealthy patients,
pregnant women, and those with teeth that had deep pockets
with periodontal pathologies, fractured roots, and resorption
cases were excluded. Only single-rooted teeth with a single
root canal were included in the study. Molar teeth and teeth
with double canals were excluded.
Patients were randomly selected into the groups from
December 2016 through November 2017. The possible risks
and benefits of the assigned applications were explained, and
written informed consent was obtained from all individual
participants prior to performing the interventions. Thirty-
seven patients were initially enrolled in the study. Due to
dropouts and patients being reluctant to attend long-term fol-
low-up, a total of 40 periapical lesions from 33 patients were
included in the analysis at the end of the study.
The groups were designed to include 10 teeth in each, and
the participants were randomly divided into four study groups:
control, MTA, PRF, and MTA+PRF. All surgical procedures
were performed by the same surgeon using a dental loupe
(Kerr Dental, Orange, Calif) at × 2.5 magnification. A
mucoperiosteal flap was raised, and osteotomy was performed
as a 5-mm diameter circle under saline irrigation. After enter-
ing the necrotic cystic cavity, periapical curettage and enucle-
ation was performed. Using surgical micromotors and a car-
bide bur with copious irrigation, 3 mm of root tip was sec-
tioned. Three-millimeter-deep retrograde root-end prepara-
tions were performed using a piezoelectric device (Acteon
Inc., Mt. Laurel, NJ) with ultrasonic retrotips (Satelec, Paris,
France).
Group 1: control (GP)
The sectioned root end was washed and dried. Previously
(orthogradely) placed GP was smoothed with a heated steel
plugger in the apical cavity. Condensation of the resected root
was secured, and no other application was performed.
Group 2: MTA
The surgically prepared 3-mm-deep root-end cavity was
washed and dried. The MTA (Angelus Soluções
Odontológicas, Londrina, Brazil) was prepared (liquid:powder
at a ratio of 3:1) on a paper slab with the aid of plastic spatulas.
A special MTA carrier (Dentsply Maillefer, Ballaigues,
Clin Oral Invest (2020) 24:1065–1072
Switzerland) was used to place MTA into the cavity. A small
plugger was used for condensation. The surface of the root was
cleaned with a wet piece of gauze to set the MTA.
Group 3: PRF
As described in the control group, a root-end preparation was
performed. Ten milliliters of venous blood was drawn from
the patients’ antecubital fossa and centrifuged at 3000 rpm for
10 min. The fibrin clot containing the platelets was inserted
into the surgical site until the entire cavity was completely
filled.
Group 4: MTA+PRF
The root-end cavity preparation and placement of MTA was
performed as mentioned in the MTA group. After the place-
ment of MTA into the retrograde cavity, PRF was acquired
and then applied to the surgical cavity with the same protocol
as the PRF group.
Wound closure was performed with 3-0 Vicryl sutures in all
groups. Antibiotics, analgesics, and mouthwashes were pre-
scribed postoperatively. Amoxicillin (1 g) was given twice
daily for 7 days.
Routine radiographs were taken at months 3, 6, and 12. In
the 12th month, CBCT scans were compared with the pre-
operative CBCT measurements in each case. The primary
healing of the periapical tissues was assessed, volume and
Fig. 1 Calculation of bone defect volume
1067
density changes were measured, and the long-term outcomes
of the procedures were compared.
Evaluation of bone measurements
CBCT (Planmeca 3D Classic, Helsinki, Finland) scans of the
related regions were taken. Each scan was obtained in 9–37 s
at a setting of 60–90 kVp and 1–14 mA, with a voxel size of
0.2 mm. All CBCT data scans were processed using medical
image processing software (MIMICS, Belgium).
Segmentations and calculations were performed in the highest
resolution (slice thickness and intervals = 0.2 mm). The sag-
ittal, axial, and coronal views of the periapical lesions were
selected and cropped. The combined lesions were considered
individual lesions, and calculations for these were performed
as a single entity.
Grayscale value (GSV) ranges were individually selected
to populate the lesion until the defect was completely filled. In
order to achieve more realistic outcomes, manual corrections
such as additions or subtractions were made on some small
voxels. The defect area was corrected in each view and then
converted into three-dimensional (3D) volumes. (Fig. 1) The
bone destruction caused by the periapical lesions before and
after the treatments were calculated and the results were com-
pared statistically.
In addition to the evaluation of volume changes, density
measurements were calculated in each lesion. To use a stan-
dard protocol and to compare the post-op measurements, a
1068
point was selected approximately 1 mm away from the verti-
cal axis of the root apex in the sagittal section. The vertical
distance from the cement-enamel junction to the selected point
was measured with GSVs (Fig. 2). In the post-operative anal-
yses, the previous distance from the cement-enamel junction
was calculated in the vertical axis of the tooth in the sagittal
view, and the density of the selected area was measured on the
axial plane.
Statistical analysis
All data were analyzed using the IBM SPSS V23 (SPSS/IBM,
Armonk, NY) statistical software. The Kruskal-Wallis method
was used to compare the volume and density measurements
between the groups. In-group comparisons were made using
the nonparametric Wilcoxon signed-rank test to compare pre-
operative and post-operative volume and density values.
Statistical significance was taken as p < 0.05.
Results
Between 2016 and 2017, 37 patients with 44 periapical lesions
were recruited into the study. Four patients were lost to follow-
up. Forty periapical lesions of 33 patients in total were includ-
ed in the final analysis. In two cases (in the control group),
secondary apical surgery was needed due to symptoms such as
swelling and pain while chewing. Secondary closure of the
Fig. 2 Measurement of bone density
Clin Oral Invest (2020) 24:1065–1072
mucoperiosteal flap opening was performed in two cases (in
the MTA group). Mucosal healing was achieved without any
symptoms.
Preoperatively, the largest volume was 426.15 mm3 (in the
PRF group) and the smallest was 44.68 mm3 (in MTA+PRF
group). Postoperatively, the largest volume was 319.15 mm3
(in the control group) and the smallest was 0 mm3 (in the
MTA, MTA+PRF, PRF groups) (Figs. 3 and 4).
Preoperatively, the lowest density was 64.0 ± 22.77 GSVs
(in the MTA+PRF group) and the highest density was 396.78
± 36.89 GSVs (in the MTA group). Postoperatively, the lowest
density was 139.62 ± 56.71 GSVs (in the control group) and
the highest density was 1485.27 ± 313.56 GSVs (in the MTA+
PRF group).
For the volume evaluation in-between groups, no signifi-
cance was present in the pre-op measurements, whereas there
were significant differences between the post-op values in all
groups (p < 0.005). Although there were significant differ-
ences between the control and MTA, and control and MTA+
PRF groups, no significant difference was found between the
control and PRF groups. The lowest volume value was ob-
tained in the MTA and MTA+PRF groups, but the difference
between them was not significant (Table 1).
According to the density evaluation between the groups, a
significant difference was observed in pre-op values in all
groups; however, no significant difference was found in
post-op calculations. The highest pre-op values of density
were obtained from the MTA and the PRF groups. The
Clin Oral Invest (2020) 24:1065–1072
Fig. 3 Pre-op volume values
MTA+PRF group was significantly different from the MTA
and PRF groups (Table 2).
In-group comparisons revealed that post-op volumes were
significantly decreased and density values were significantly
increased according to the pre-op measurements in all groups.
Discussion
The success of endodontic therapy depends on complete
periapical repair and regeneration. Teeth with apical
Fig. 4 Post-op volume
1069
lesions typically heal satisfactorily after non-surgical end-
odontic treatments; however, periradicular surgery is an
indispensable treatment option in endodontics for the
management of unhealed and symptomatic periapical pa-
thologies. In general, the prognosis of periapical surgery
varies between 25 and 90% [20]. Although the application
of a retrograde filling material is still controversial, many
ex vivo studies have demonstrated the passage of bacteria
to periapical tissues without the presence of a retrograde
filler at the root ends and therefore this approach has been
accepted as a routine treatment protocol [8, 9].
1070
Table 1 Comparison of volume changes according to groups
Pre-op volume Post-op volume
MTA 156.81 (53.71–319.15) 1.41 (0–70.28)a
PRF 120.62 (73.77–642.25) 5.55 (0–115.44)ab
MTA+PRF 165.82 (44.68–409.48) 3.33 (0–12.3)a
Control 153.59 (46.07–347.08) 26.79 (1.78–319.15)b
a,b
There is no difference between the groups with the same letters
MTA is a biocompatible material and has superior properties
in terms of sealing ability and periapical tissue regeneration
compared with conventional retrograde fillers such as GP [10,
21]. In a meta-analysis, it was reported that MTA inhibited
bacterial penetration better than Super EBA, amalgam, and
IRM [22]. In previous randomized clinical trials, the success
rates of MTA were reported as over 80% after 12 months’
follow-up and over 90% at the 24th month follow-up [23,
24]. These findings are in correlation with the current results.
According to the outcomes of the present study, the lowest
healing rate was found in groups in which a retrograde filling
material was not used (control and PRF groups). Despite the
positive features, the length of setting time and difficulty in
application present some of the drawbacks of MTA. In addition,
it can be easily washed away if good care is not taken. The
amount of nanoparticles and their size, liquid and powder ratio,
environmental factors (pH and room temperature), and the air
trapped during preparation may affect setting time, as well as
the physical properties of the placed MTA [25, 26].
PRF is known to be a biomaterial with tissue healing prop-
erties, and studies suggested that PRF increases the osteogenic
potential owing to the growth hormones it contains, which con-
tinue to be released into the tissue for up to 1 week. PRF is an
autologous material derived from the patient’s own blood and
thus prevents an immunologic reaction [14, 27]. In a case series,
PRF was applied after periapical surgery and all patients showed
complete bone healing with no signs of infection at the end of
the 6 months [28]. In this study, periapical radiography was used
and to the best of our knowledge, digital periapical radiography
cannot show the real dimension of lesions, besides, a significant
difference was observed between 2D and 3D scan calculations
while comparing the size of the periapical lesions. 3D imaging
Table 2 Comparison of density changes according to groups
Pre-op density Post-op density
MTA 286.47 (199–396.78)b 687.73 (103.56–1289.7) 0.013
PRF 305.3 (71.22–377)b 670.81 (186.22–904.86) 0.005
MTA+ 85.72 (44.33–200)a 728.07 (495.27–1485.27) 0.005
PRF
Control 231.85 (48.73–287.81)ab 374.11 (139.62–1233.22) 0.013
a,b
There is no difference between the groups with the same letters
Clin Oral Invest (2020) 24:1065–1072
allows a more precise evaluation and is recommended as a valu-
p able tool for endodontic microsurgery. In a study, periapical
surgery was performed on lesions with apico-marginal defects.
0.007 PRF was applied to the wound area considering its healing
0.005 properties, but the results showed no significance of bone
0.005 healing [29]. These findings showed that the results of previous
0.005 studies are in correlation with those of the present study.
According to the post-operative volume comparisons, the
null hypothesis was rejected. No significant difference in bone
healing was found between the PRF and control groups. MTA
and MTA+PRF results were significantly lower than in the
control group, which was indicative of better healing. In addi-
tion, although there was no statistically significant difference,
the success rates of the MTA group were higher than the MTA+
PRF group. In view of these findings, it can be suggested that
PRF has no positive effect on periapical healing and placing a
retrograde filling material after root end resection is crucial.
A possible explanation for the inefficient effect of PRF may
well be due to its tiny structure, which can be rapidly resorbed
in oral tissues [14, 30]. Besides, according to some studies, it
was emphasized that biomolecules that are known to be re-
leased from PRF could not provide a proper environment for
osteogenesis, and the stimulating effect of platelet concentra-
tions was found more effective in soft tissue healing rather
than in osteogenic tissue [31]. Furthermore, processes such
as centrifugation can lead to microbial and chemical contam-
ination, which affects the homogeneity and stability of the
PRF membrane [32, 33]. On the other hand, placement of
PRF to the surgical area immediately after the MTA applica-
tion possibly caused dissolution of MTA, which leads to dis-
ruption of hermetic obturation. The elongation of healing time
in the MTA+PRF group compared with the MTA group can
be considered a consequence of this situation.
Success for endodontic interventions remains ambiguous.
With consideration to the literature, there is no consensus in
terms of the factors affecting the prognosis of apical resection.
In general, endodontic success is assessed based on clinical,
radiographic, and histopathologic features. Clinically, pa-
tients’ asymptomatic history (absence of pain, sensitivity, per-
cussion), absence of abnormal physical symptoms (absence of
sinus tract and swelling), and lack of negative radiographic
findings define the mechanism of the decision process [34,
35]. In this study, lesions with asymptomatic clinical findings
and significant new ossification areas detected on CBCT scans
were evaluated as healed. All lesions in the current study were
p healed as expected because the applications used were all
proven successful in the literature; nevertheless, the purpose
of this study was to evaluate the speed of recovery.
CBCT is an accurate 3D imaging technique and one of
the best diagnostic tools for assessing regenerated tissue
[36–39]. A high correlation has been demonstrated be-
tween CBCT-based predictions and histologic evidence,
suggesting that the CBCT is an effective non-invasive
Clin Oral Invest (2020) 24:1065–1072
diagnostic tool for periapical lesions [17, 18, 40]. This
study was conducted to analyze periapical healing using
bone volume measurements in teeth with periapical lesions
with CBCT. In addition to bone volume, density values
were also measured by a blinded researcher. In the current
study, we aimed to analyze the composition and structure
of the related tissue by choosing a stable standard point to
compare the pre-op and post-op density changes.
All post-operative density values were increased compared
with pre-operative values. The groups were also evaluated
within themselves. The least density change was seen in the
control group and was correlated with the volume changes.
However, in the PRF and MTA groups, there were no signif-
icant differences observed and the maximum density increase
was found in the MTA+PRF group. These findings are not in
total harmony with volume evaluations. Such a discrepancy
should not be a surprise in as much as the density measure-
ments are not accurate for CBCT. Increased scatter radiation
and artifacts caused by the beam can corrupt the density as-
sessment. In addition, GSVs of CBCT images can be spatially
inhomogeneous and do not correspond 1:1 to Hounsfield units
(HUs); hence, it may well be unreliable [41]. On the other
hand, the total density measurements of the lesions were not
performed, which can be considered a drawback of the study.
The current study was a prospective, randomized con-
trolled trial with an optimal sample size. Nevertheless, the
study has some limitations. Patients were followed over a 1-
year period to evaluate the periapical healing results; however,
pursuing an extended follow-up may better accentuate the
uncertain category (PRF and control group) of healing [42].
The lack of histologic evidence is another limitation of the
study. CBCT evaluation in combination with histologic evi-
dence may be a better diagnostic way to determine the true
nature of the healing process in tissues. However, it is uneth-
ical to procure post-operative healed tissue from patients to
compare histologic findings with CBCT scans [17].
Conclusion
It can be concluded that the placement of a hermetic retro-
grade filling material such as MTA is crucial for successful
endodontic microsurgery. The application of PRF to the sur-
gical cavity may not necessarily improve outcomes. Further
studies are needed with long-term follow-up.
Funding information This study was supported by Scientific Research
Fund of RTE University in Rize/Turkey. (No:TSA-2017-706, Id:706).
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
1071
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the institu-
tional and/or national research committee and with the 1964 Helsinki
declaration and its later amendments or comparable ethical standards.
This study was approved by the Ethics Committee of RTE University/
Rize-Turkey. (No: 2016/88).
Informed consent Informed consent was obtained from all individual
participants included in the study.
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