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The Saudi Dental Journal 36 (2024) 461–465

Contents lists available at ScienceDirect

The Saudi Dental Journal


journal homepage: www.ksu.edu.sa
www.sciencedirect.com

Original Article

The use of guided tissue regeneration in endodontic Microsurgery: Setting


a threshold
Fatemah A. Alkandari a, *, Mazen K. Alotaibi b, Sami Al-Qahtani c, Samhan Alajmi d
a
Periodontics unit, Al-Jahra Specialties Center, Ministry of Health, Kuwait
b
Dental department, Periodontics Unit, Prince Sultan Military Medical City, Riyadh, Saudi Arabia
c
Dental department, Periodontics Unit, King Saud University, Riyadh, Saudi Arabia
d
Kuwait Board of Endodontics, Kuwait Institute for Medical Specialties, Kuwait

A R T I C L E I N F O A B S T R A C T

Keywords: Aim: We aimed to compare the radiographic outcomes of conventional and regenerative approaches in end­
Apical surgery odontic microsurgery (EMS) and set a critical defect size for healing in conventional and regenerative therapies.
Endodontic microsurgery Methodology: The study evaluated 53 root canal-treated teeth (33 patients) with periapical lesions. Among them,
Guided bone regeneration
19 teeth (35.8 %) were treated with regenerative treatment, whereas 34 teeth (64.1 %) were managed with the
Guided tissue regeneration
Healing criteria
conventional approach. Conventional and regenerative approaches were performed by endodontic and peri­
odontic residents under consultants’ supervision. Healing was evaluated after a minimum period of 6 months by
comparing pre- and post-operative cone-beam computed tomography (CBCT) findings. The radiographic inter­
pretation was conducted by a single examiner who was not participating in the surgeries and was blind on the
type of treatment prior to CBCT evaluation. New healing criteria were proposed owing to the limitations on the
present criteria in evaluating endodontic surgery after regenerative treatment. Critical measurements were
calculated for each approach based on periapical lesion dimensions.
Results: The regenerative approach presented significantly better healing than conventional treatment (mean,
1.21 and 1.59, respectively; p = 0.047). Based on the critical-point calculations, the conventional approach was
effective in lesions of up to 3 mm depth and height, whereas the regenerative approach resulted in better healing
rates in lesions with 3–9 mm depth and 3–6 mm height.
Conclusions: Performing the regenerative approach in EMS resulted in better healing rates than those of the
conventional approach. The conventional approach is recommended for small periapical lesions, whereas the
first had better results in larger lesions.

1. Introduction of a lost or injured tissue by completely restoring its structure and


function (Karring, 2000). This is performed by using a barrier over the
Endodontic microsurgery (EMS) is a newer version of the traditional osseous defect to prevent or retard the fast proliferation of the oral
root-end surgical intervention for managing a tooth that uderwent failed epithelium and gingival connective tissue and allow the repopulation of
endodontic treatment and cannot be managed with the orthograde cells with osteogenic potential (Gottlow and Nyman, 1996).
endodontic approach. Although the osteotomy site is considerably small, Several human and animal studies have compared the healing rates
the bone loss around the root can be significant, and the healing of the after EMS with or without performing the regenerative approaches
periapical lesion may be challenging (Kim and Kratchman, 2006). The (Apaydin and Torabinejad, 2004; Garrett et al., 2002; Pantchev et al.,
main objective of EMS is to optimise the healing environment for the 2009; Yoshikawa et al., 2002). The outcomes after using calcium sulfate
peri-radicular tissue by effectively eliminating persistent pathogens and were compared with those obtained after conducting the conventional
directly accessing the root apices and periapical area (European Society treatment in beagle dogs. The results indicated that adding calcium
of Endodontology, 2006). sulfate had no benefits in some studies but significantly better healing
Tissue regeneration is defined as the reproduction or reconstruction rates in others (Apaydin and Torabinejad, 2004; Murashima et al.,

* Corresponding author at: Al-Jahra specialties Center, Al-Jahra, Kuwait.


E-mail address: jomant-aljoman@hotmail.com (F.A. Alkandari).

https://doi.org/10.1016/j.sdentj.2023.12.005
Received 26 June 2023; Received in revised form 10 December 2023; Accepted 11 December 2023
Available online 12 December 2023
1013-9052/© 2023 THE AUTHORS. Published by Elsevier B.V. on behalf of King Saud University. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
F.A. Alkandari et al. The Saudi Dental Journal 36 (2024) 461–465

2002). When evaluating human clinical trials, radiographic evaluation 2.1. Radiographic measurements
showed complete healing in 100 % of the cases received resorbable
hydroxyapatite filler with an expanded polytertafluoroethylene (e- The CBCT measurements included the height, width, depth, and
PTFE) membrane compared to 77.8 % and 88.9 % in the second group volume of the lesion; presence or absence of buccal or palatal perfora­
(e-PTFE membrane only) and the third group, respectively (conven­ tion; and buccal plate length. These measurements were taken as follows
tional therapy) (Garrett et al., 2002). (Fig. 1):
The outcomes of applying guided tissue regeneration (GTR) during
EMS were investigated. However, several limitations were found. Most 1) Height: from the sagittal section, the deepest point considered in a
of the studies did not consider the three-dimensional size of the defect. parallel line with the tooth long axis
Assessing the lesions based on two-dimensional periapical radiographs 2) Width: from coronal section, the deepest point of the lesion consid­
may not reflect the actual healing (Garrett et al., 2002; Pantchev et al., ered in a line perpendicular to the tooth long axis
2009; Pecora et al., 1995; Stassen et al., 1994; Taschieri et al., 2007; 3) Depth: from the sagittal section, the deepest point considered in a
Tobón et al., 2002). Evaluating the outcomes of apical surgery using line perpendicular to the long axis of the tooth
periapical radiographs significantly overestimated the success rate 4) Volume: calculated by multiplying the height x width x depth of the
compared to that after using CBCT (Schloss et al., 2017). Conversely, defect
when comparing the measurements taken intraoperatively with CBCT 5) Buccal or palatal perforation: marked as present or absent
measurements, a strong correlation was found, indicating the accuracy 6) Buccal plate length: from the sagittal section, the distance from
of CBCT measurements (Grimard et al., 2009). Although some studies alveolar crest level till the buccal or palatal perforation
have used CBCT in pre-operative evaluation (Kim et al., 2016; Kurt et al.,
2014), no study has compared the outcomes of the EMS in CBCT pre- and 2.2. Records data retrievement
post-operatively after regenerative treatment. Additionally, many
studies have evaluated surgically created periapical defects, which may Once the CBCT measurements were taken, patients’ data were
have a different healing mechanism than that of bacterially infected retrieved. Patient age, sex, tooth type (single-rooted, multi-rooted),
defects in humans (Maguire et al., 1998; Murashima et al., 2002; tooth position (maxilla, mandible), type of treatment (conventional,
Yoshikawa et al., 2002). Another limitation is the use of alloplast or GTR), type of retrograde filling (bioceram, mineral trioxide aggregate,
xenograft materials in most of the studies (Pantchev et al., 2009; or zinc oxide eugenol cement), and the skills of the operator (resident,
Taschieri et al., 2007; Yoshikawa et al., 2002). Although new bone specialist/ consultant) were recorded.
formation may occur using these materials, they are primarily used as
fillers, and the remaining particles will not resorb within an extended 2.3. Healing criteria
period. The mean percentage of new bone formation when using allo­
graft is 65 % compared to 45 % and 49 % when using xenograft and Although the healing criteria have been found in the literature using
alloplast, respectively (Nappe et al., 2016). CBCT (Estrela et al., 2008; Kang et al., 2020; von Arx et al., 2016), these
Therefore, in this study, we aimed to compare the radiographic are based mainly on conventional treatment and will not be applicable
outcomes after using the conventional and regenerative approaches in for evaluating GTR treatment outcomes. Therefore, new criteria have
patients who underwent EMS and set a critical defect size for healing in been proposed to evaluate the study outcomes. Table 1 shows the pro­
conventional and regenerative therapies. posed healing criteria.

2. Materials and methods 2.4. Data analysis

This retrospective study was conducted at Riyadh Elm University, The sample size calculation was executed. The considered test power
from January 2021 to January 2022. It was approved by the Institutional was 0.80, and the marginal error was 0.2. This yielded a sample size of
Review Board of Riyadh Elm University (number FPGRP/2019/449/ 42 patients. The tooth was considered the unit of evaluation in this
138/273), and was conducted in accordance with the tenets of the study. Additionally, intra-examiner calibration was calculated. The
Helsinki Declaration. statistical analysis was performed using the Statistical Package For The
The patients’ records were retrieved retrospectively for those who Social Sciences (SPSS) program. Descriptive statistics, simple linear
underwent EMS. Patients’ data and the surgery details were obtained regression for comparing two variables, and multiple linear regression
from the patients’ records as well as from pre- and post-operative CBCT for more than two variables were conducted. Additionally, cross-
findings. As the university clinic is an educational centre, consent forms tabulation was used to specify the critical points in this study. A p-
were usually signed before any provided treatment for using the pa­ value of < 0.05 was considered significant.
tients’ data for educational and research purposes; therefore, no new
consent forms were needed. Surgical interventions were conducted by 3. Results
endodontic and periodontic residents with supervision of specialists or
consultants or by endodontic specialists and consultants alone. The use In total, 53 teeth of 33 patients had complete examination data after
of the microscope and endodontic microsurgery is considered the stan­ EMS.
dard of care in the centre. Patients with complete data were not recalled, To check the reliability of the measurements, CBCT examinations
whereas those with only pre-operative CBCT findings and detailed sur­ were conducted twice with 2-week time gap in the group of patients who
gical records were recalled to undergo post-operative CBCT examina­ were not included in the study. The intraclass correlation coefficient was
tion. The post-operative CBCT examination was conducted voluntarily. 0.98 showing excellent reliability.
The exclusion criteria were as follows: missing detailed surgical infor­ Table 2 shows the descriptive analysis of treated teeth in this study. A
mation in the record that prevent proper statistical analysis; absence of smoking habit cannot be assessed owing to incomplete data in most
pre-operative CBCT; Refusal to undergo post-operative CBCT examina­ records. The mean age of the treated patients was 37.1 (range, 16–69).
tion; presence of through-and-through lesion; and healing period < 6 The mean follow-up period was 1.47 years, whereas the longest follow-
months. up period was 3.29 years. Among the group treated with GTR, all cases
CBCT measurements were conducted before checking the records for had been treated with a collagen membrane. Allograft placement was
the type of treatment performed. performed in 78.9 % of the cases, whereas the rest did not receive any
bone grafting.

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F.A. Alkandari et al. The Saudi Dental Journal 36 (2024) 461–465

Fig 1. A sagittal and coronal section of CBCT showed the measurements taken Orange = tooth long axis, Blue = height of the lesion, Red = depth of the lesion, Green
= buccal plate length, Purple = width of the lesion. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of
this article.)

Table 1 Table 2
Proposed healing criteria. Descriptive analysis of the treated teeth.
Periapical defect Around the The buccal window N %
resected root Type of treatment

Complete Complete absence of Presence or Filled with bone Conventional treatment 34 64.1
healing periapical defect with absence of with or without GTR treatment 12 22.6
bone fill of similar periodontal cortical bone plate Gender
density or more ligament around or overbuild with Male 23 43.4
radiopaque than the sectioned lateral ridge Female 30 56.6
surrounding natural tooth apex augmentation Tooth type
bone Single rooted 41 77
Partial Reduction in the size Presence or Decreased on size Multi-rooted 12 22.6
healing of the defect in pre absence of but not necessary Arch
and post-operative periodontal closed with bone Maxilla 41 77
CBCT measurements ligament around Mandible 12 22.6
without complete the sectioned Type of retrograde filling
bone fillPresence of tooth apex MTA 11 34
radiopaque bone fill Bioceram 20 54.7
with radiolucent rim IRM 1 1.9
around the defect Buccal or palatal plate perforation
separating natural Yes 19 36.5
bone from the lesion No 33 63.4
Failed no change or increase Absence of no change or Skills
in the size of periodontal increase in the size Resident 24 45.3
periapical defect ligament around of buccal window Consultant/ specialist 29 54.7
resected tooth

partial healing when the site depth ranged between 1 and 9 mm. This
The simple linear regression analysis (Table 3) showed a statistically indicated that the critical depth of the lesion for GTR treatment is 9 mm.
significant difference in healing between cases treated with GTR Failure was found when the defect was deeper than 9 mm.
compared to conventional treatment. There was no statistically signifi­ Similarly, the height of the periapical lesion had a statistically sig­
cant effect of the width and volume of the periapical lesion on healing nificant effect on the healing among patients treated with conventional
among those treated with GTR and conventional treatment. and GTR approaches (Table 4). On sites with 1–3 mm height, both
The multiple linear regression analysis indicated that the depth of treatments showed a high percentage of complete healing. This per­
the defect had a statistically significant effect on healing among the two centage decreased to 16.7 % and 37.5 %, respectively, for conventional
treated groups (Table 4). The deeper the defect, the less likely the site to and GTR approaches with defects ranging between 3 and 6 mm. Based
show complete healing. Based on cross-tabulation, 75 % of the sites with on that, the critical height for periapical defect healing is 3 mm for the
a depth of 1–3 mm had healed completely or presented with partial conventional treatment and 6 mm for the GTR approach.
healing in conventional treatment. The healing dropped to 30.6 % when Prognostic factors, such as the tooth type (single or multi-rooted),
the depth increased to 3–6 mm. Based on that, the critical depth for arch position (maxilla or mandible), type of retrograde filling, pres­
using conventional treatment is 3 mm. ence of buccal or palatal bone perforation, and crestal bone level, which
In comparison, all patients treated with GTR presented complete or indicated apicomarginal communication, as well as the skills of the

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F.A. Alkandari et al. The Saudi Dental Journal 36 (2024) 461–465

Table 3
The effect of the type of treatment on healing.
N Mean (±SD) Sum of squares Df Mean of squares F p-Value

Conventional Treatment 34 1.59 (±0.7) Between groups 1.739 1 1.739 4.145 0.047*
GTR treatment 19 1.21 (±0.53) Within groups 21.393 51 0.419
Total 23.132 52

Complete healing = 1, partial healing = 2, failed = 3.


*
p-value is statistically significant < 0.05.

the conventional approach is effective in lesions with a depth up to 3


Table 4
mm. Using the GTR approach may improve the healing in lesions ≥ 3
The multiple linear regression showing statistically significant measurements
mm. The likelihood of complete or partial healing will decrease among
that affect the healing among patients treated with conventional approach and
GTR.
patients treated with GTR in > 9 mm depth lesions. Similarly, there was
a significant difference in healing between lesion height and treatment
Variable B Std. Error p-value
approaches. Conventional treatment is effective in lesions up to 3 mm in
Healing (Constant) 1.607 0.284 0 height. The probability of complete healing decreased with conventional
Depth of the defect 0.069 0.025 0.009*
treatment in lesions > 3 mm. Sites with 3–6 mm height may have higher
Type of treatment − 0.372 0.175 0.038*
(conventional VS GTR)
complete healing rates when applying the GTR approach. Areas that
Healing (Constant) 1.809 0.289 0 showed > 6 mm height had a low healing probability even with GTR
Height of the defect − 0.382 0.184 0.043* treatment. To the best of our knowledge, no study to date has examined
Type of treatment 0.032 0.032 0.177 the critical points for healing among the two treatment approaches.
(conventional VS GTR)
In this study, the prognostic factors, such as tooth type (single or
*
p-value is statistically significant < 0.05. multi-rooted), arch position (maxilla or mandible), type of retrograde
filling, presence of buccal or palatal bone perforation, and crestal bone
operator (resident or specialist/consultant) did not show a statistically level, which indicated apicomarginal communication, as well as the
significant effect on the healing rates in the studied sample. skills of the operator (resident or specialist/consultant), had no signifi­
cant effect on healing regardless of the treatment type, in consistency
4. Discussion with the findings of previous studies (Li et al., 2014; Shinbori et al.,
2015).
The introduction of GTR therapy and bone augmentation in EMS However, our study had some limitations. First, it had a limited
aimed to increase the ability of the area to heal with regeneration sample size and there was a possibility of attrition bias. Especially,
instead of fibrous connective tissue and epithelial migration (Maguire although the sample size calculation indicated that 42 individuals were
et al., 1998). This study was conducted to specify the critical defect needed, only 33 participants were enrolled owing to the unavailability
measures beyond which the healing might be affected in conventional of the cases. As this study was based on voluntary participation, many
and GTR approaches. patients refused to undergo the post-operative CBCT examination, spe­
Several studies have compared the effects of conventional treatment cifically those with no signs and symptoms, even after explaining the
and with those of GTR. Based on the defect type, a review article found benefice of such investigation. The additional radiation dose and the
that GTR had better performance in through-and-through lesion (von extra cost were other factors that prevented the patients from undergo
Arx and Alsaeed, 2011). However, no conclusion can be drawn for the post-operative CBCT examination; this can cause an underestimation of
apicomarginal defect, and limitations were found in isolated defects; this the effectiveness of the treatment provided. In addition, as this was a
explained why these two types of defects were included in our study. retrospective study, controlling all relevant variables was not possible
Some studies have reported better results using GTR (Pantchev et al., and post-operative signs and symptoms were not evaluated.
2009; Yoshikawa et al., 2002), in agreement with our results. In Finally, this study was based solely on radiographic interpretation. In
contrast, others have reported the absence of significant differences after an attempt to mask the type of treatment, radiographic measures were
using the two approaches (Garrett et al., 2002; Taschieri et al., 2007). taken prior to retrieving the data from the patients’ files; however, the
With the introduction of CBCT in the dental field, studies have re­ type of treatment provided can be identified based on CBCT appearance
ported that CBCT is superior in assessing post-operative healing most of the time owing to the experience of the author in that field.
compared to periapical radiographs (Kruse et al., 2018; Schloss et al.,
2017). To the best of our knowledge, no study has compared the CBCT 5. Conclusions
findings before and after EMS among patients treated with the GTR
approach. The GTR approach in isolated and apicomarginal periapical lesions
In contrast, the effect of defect size was assessed by CBCT evaluation seemed to result in significantly better healing rates than that of the
among patients treated with conventional treatment in previous studies. conventional treatment. Further studies are needed to generalise our
This study showed that the lesion’s depth significantly affected the findings and overcome the shortage of this article. Clinical guidelines
healing for patients treated with conventional and GTR approaches. Von can be recommended based on the findings that conventional treatment
Arx et al. (von Arx et al., 2007) showed that healed lesions had a smaller is effective in periapical lesions with a depth and height of ≤ 3 mm and
depth (mean: 7.15 mm) than non-healed lesions (mean: 8.1 mm) among using the GTR approach has a higher probability of complete healing in
those treated with the conventional approach, whereas Kim et al. (Kim lesions with a depth of 3–9 mm and height of 3–6 mm. Lesions with a
et al., 2016) indicated that the depth of the defect had no effect on periapical lesion deeper than 9 mm and a height of > 6 mm had a lower
healing. likelihood of healing.
Evaluating the height of the defect had a significant effect on healing
among the studied population. This was in contrary to the findings of
Declaration of competing interest
Kim et al. and Von Arx et al. (Kim et al., 2016; von Arx et al., 2007).
When comparing the defect size critical measurements that influence
The authors declare that they have no known competing financial
the healing in conventional treatment and GTR, our data indicated that
interests or personal relationships that could have appeared to influence

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F.A. Alkandari et al. The Saudi Dental Journal 36 (2024) 461–465

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