Received: 18 October 2022

| Accepted: 14 May 2023

DOI: 10.1111/iej.13936

REVIEW ARTICLE

Effect of guided tissue regeneration on the success

of surgical endodontic treatment of teeth with
endodontic-­periodontal lesions: A systematic review

Eyal Rosen1,2 | Igor Tsesis1 | Eitan Kavalerchik1 | Rahaf Salem1 |

Adrian Kahn3 | Massimo Del Fabbro4,5 | Silvio Taschieri4,6,7 | Stefano Corbella4,6,7
1
Department of Endodontology, Abstract
Maurice and Gabriela Goldschleger
Background: Endodontic-­ periodontal lesions may need surgical approach and
School of Dental Medicine, Tel Aviv
University, Tel Aviv, Israel the application of guided tissue regeneration (GTR) to be treated by a combined
2
Tel Aviv University Center for approach.
Nanoscience and Nanotechnology, Tel Objectives: The aim of the present study was to evaluate the effects of GTR on the
Aviv, Israel
3
success (clinical and radiological healing) of teeth with endodontic-­periodontal le-
Department of Oral and Maxillofacial
Surgery, Goldschleger School of Dental sions treated by modern surgical endodontic treatment, by means of a systematic
Medicine, Tel-­Aviv University, Tel Aviv, review of the literature.
Israel
4
Methods: An exhaustive electronic (Medline, Embase and Scopus searched from
Department of Biomedical, Surgical,
and Dental Sciences, Università degli
inception to August 2020) and manual literature search combined with strict in-
Studi di Milano, Milan, Italy clusion and exclusion criteria was undertaken to identify any clinical (prospective
5
Fondazione IRCCS Ca’ Granda case series or comparative trials) studies that assessed the added benefit of GTR in
Ospedale Maggiore Policlinico, Milan,
modern surgical endodontic treatment of teeth with endodontic-­periodontal lesions.
Italy
6 The success of the treatment was assessed based on radiographic healing and clini-
IRCCS Ospedale Spedale Galeazzi
Sant'Ambrogio, Milan, Italy cal evaluations. The risk of bias of the identified studies was evaluated using the
7
Department of Oral Surgery, Institute Cochrane's collaboration RoB 2.0 tool and the Joanna Briggs Institute (JBI) critical
of Dentistry, I. M. Sechenov First appraisal tools.
Moscow State Medical University,
Moscow, Russia Results: A systematic literature search for eligible reports retrieved three rand-
omized controlled trials (RCTs) and one prospective single arm study with a total of
Correspondence
125 teeth in 125 subjects. One of the RCTs has a low risk of bias, while the other two
Eitan Kavalerchik, Department of
Endodontology, Maurice and Gabriela raised some concerns, using the RoB 2.0 tool. Due to the heterogeneity of the results,
Goldschleger School of Dental it was not possible to perform a comparative meta-­analysis and the results are pre-
Medicine, Tel Aviv University, Tel Aviv
sented in a narrative manner and by calculating pooled outcomes. Pooling together
69978, Israel.
Email: [email protected] the data from all the included studies, the reported outcome was of complete healing
in 58.4% of all cases, of scar tissue formation/incomplete healing in 24% of cases, of
uncertain healing in 12.8% of cases, and of failure in 4.8% of all analysed teeth, with
a follow-­up ranging from 12 to 60 months.

Eyal Rosen and Igor Tsesis are contributed equally to this work.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2023 The Authors. International Endodontic Journal published by John Wiley & Sons Ltd on behalf of British Endodontic Society.

910 | wileyonlinelibrary.com/journal/iej
 Int Endod J. 2023;56:910–921.
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ROSEN et al.    911

Discussion: The scientific evidence about the use of GTR in modern surgical endo-
dontic treatment of endodontic-­periodontal lesion is sparse, and the available results
are derived from very heterogeneous studies, thus not permitting to clarify which is
the most effective treatment option in these cases.
Conclusions: There is an absence of studies comparing GTR versus no GTR.
Registration: The protocol for this review was registered in the PROSPERO data-
base with the registration ID number CRD42022300470.

KEYWORDS
endodontic surgery, endodontic-­periodontal lesions, GTR, outcome

I N T RO DU CT ION lesions, leaving the prognosis of such cases unknown, and

not systematically explored in literature.
Endodontic-­periodontal lesions manifest when an infec- Additional reports have suggested that regenera-
tion involves both the pulpal space and the periodontium. tive periodontal procedures that include GTR may im-
The end result of such infections is a necrotic and infected prove tooth survival and provide long term stability
pulp (or root canal filling) and deep periodontal pockets while reducing periodontitis progression and the need
(Rosen et al., 2019). for re-­intervention (Cortellini et al., 2017; Nemcovsky
Modern surgical endodontic treatment uses en- & Nart, 2019). Furthermore, a combined approach of
hanced magnification, minimal root resection bevel, surgical endodontic treatment and periodontal surgical
ultrasonic root-­end preparation to a depth of 3–­4 mm, treatments was recently proposed as an alternative for
and biocompatible root-­ end filling materials (Kim & teeth with endodontic-­ periodontal lesions (Alquthami
Kratchman, 2006; Tsesis et al. 2011). This type of inter- et al., 2018; Dietrich et al., 2003; Kim et al., 2008; Mali
vention is indicated for teeth with periapical pathology & Lele, 2011; Oh et al., 2009, 2019; Rohilla et al., 2017;
when non-­surgical retreatment is impractical or unlikely Sharma et al., 2014; Tewari et al., 2018). Notably, these
to improve previous results (Gutmann & Harrison, 1985; publications possess significant variability in study design,
Tsesis et al., 2009, 2011), and has been reported to have a treatment protocols, follow-­up periods, and inclusion and
success rate of over 90% (Kim & Kratchman, 2006; Tsesis exclusion criteria, thus generating inconsistent and con-
et al., 2006, 2009, 2011). However, it is important to note fusing results (Alquthami et al., 2018; Dietrich et al., 2003;
that these success rates predominantly relate to teeth Kim et al., 2008; Mali & Lele, 2011; Oh et al., 2009, 2019;
without any periodontal involvement (Kim et al., 2008; Rohilla et al., 2017; Sharma et al., 2014; Tewari et al., 2018).
Tsesis et al., 2011). Evidence-­based dentistry is an approach to oral health-
Complete periapical wound healing after surgical end- care that integrates the best available clinical evidence to
odontic treatment requires regeneration of alveolar bone, combine a practitioner's clinical expertise with an individ-
periodontal ligament, and cementum (Lin et al., 2010). ual patient's treatment needs and preferences (Gutmann
The use of guided tissue regeneration (GTR) techniques & Solomon, 2009; Mileman & van den Hout, 2009;
has been proposed as an adjunct to endodontic surgery Rosenberg & Donald, 1995). Systematic reviews con-
in order to promote bone healing (Baek & Kim, 2001; stitute the basis for practicing evidence-­based dentistry
Maguire et al., 1998; Taschieri et al., 2008; Tobon (Gutmann & Solomon, 2009; Rosenberg & Donald, 1995;
et al., 2002). A previous systematic review of the literature Sutherland & Matthews, 2004).
(Tsesis et al., 2011) reported that GTR techniques could Thus, the aim of the present study was to evaluate the
improve bone regeneration following surgical endodontic effects of GTR on the success (clinical and radiological
treatment particularly in cases with large and through-­ healing) of teeth with endodontic-­ periodontal lesions
and-­through periapical lesions (Tsesis et al., 2011). Other, treated by modern surgical endodontic treatment, by
more recent, both narrative and systematic reviews of means of a systematic review of the literature.
the literature confirmed that GTR procedure could pro-
mote bone healing after surgical endodontic treatment,
confirming that their efficacy is higher in presence of MATERIALS AND METHODS
large periapical lesions (Corbella et al., 2016; Zubizarreta-­
Macho et al., 2022). However, those reviews did not per- The protocol for this review was registered in the
formed a specific analysis on endodontic-­ periodontal PROSPERO database with the registration ID number
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912    EFFECT OF GTR ON ENDO SURGERY WITH ENDO-­PERIO SR

CRD42022300470. The systematic review was reported Information sources and search strategy
according to the PRISMA (preferred reporting items for
systematic reviews and meta-­analyses) statement (Page The search covered all English language articles pub-
et al., 2021). lished in dental journals from inception to August
2020. The following electronic databases were searched:
MEDLINE using the PubMed search engine (http://www.
Eligibility criteria ncbi.nlm.nih.gov/sites/​pubmed) with the key words:
(((((("periodontal") OR ("endodontic periodontal")) OR
This systematic review comprises comparative and non-­ ("apico-­marginal")) OR ("periodontal endodontic")) OR
comparative clinical studies that reported the use of GTR ("endo-­perio")) OR ("perio-­endo")) AND ((((((("apicoec-
in surgical endodontic treatment in teeth with endodontic-­ tomy") OR ("periradicular surgery")) OR ("endodontic sur-
periodontal lesions. The detailed PICOS principles were gery")) OR ("apical surgery")) OR ("periapical surgery"))
stated as follows: (1) Participant: patients who presented OR ("root-­end surgery")) OR ("root-­end resection")).
with periapical pathology and periodontal involvement and An electronic search through the Embase database
required endodontic-­periodontal surgery. (2) Intervention: (http://www.embase.com) used the same key words, with
GTR techniques were applied in the surgery. (3) Blank the Embase limits set to ‘Embase ONLY’.
control: GTR techniques were not used in the surgery. (4) A search using the Scopus database (http://www.sco-
Outcome: Healing of the periapical pathology as assessed pus.com) used the same keywords, with the scopus limits
by clinical symptoms and radiographic results. (5) Study set to: NOT INDEX (medline).
design: Randomized clinical trials (RCTs), controlled clini- An adjunctive search was performed on the reference
cal trials (CCT), or prospective case series (PCS). lists of the included articles and reviews retrieved. It was
also performed a manual search of the issues from the last
Inclusion criteria: 20 years of the following journals: Journal of Endodontics,
International Endodontic Journal, Journal of Clinical
1. Randomized clinical trials (RCT), controlled clinical Periodontology, Journal of Dentistry and Clinical Oral
trials (CCT), or prospective case series (PCS). Investigations, and Australian Endodontic Journal.
2. Studies that evaluated modern surgical endodontic In addition, the grey literature was screened on the
treatment (defined by the use of enhanced magnifica- following databases: Networked Digital Library of Theses
tion, minimal root resection bevel, ultrasonic root-­end and Dissertations, Open Access Theses and Dissertations,
preparation to a depth of 3–­4 mm, and placement of DART-­Europe E-­theses Portal—­DEEP, Opening access to
a root-­end filling material; Kim & Kratchman, 2006; UK theses—­EthOS.
Tsesis et al., 2011) in teeth with endodontic-­periodontal
lesions (defined as teeth with infected root canal sys-
tems and deep periodontal pockets; Rosen et al., 2019). Selection process
GTR techniques that included the use of one or more
of the following: a barrier membrane, a bone substitute, The articles were initially evaluated for relevance based
platelet-­rich plasma (PRP), or platelet-­rich fibrin (PRF), on their titles and abstracts by two independent observ-
were required to be part of the surgical protocol (for the ers. Possibly relevant studies were subjected to a full text
treatment group; Goyal et al., 2011; Tsesis et al., 2011). evaluation, where the full text of selected studies was ob-
3. At least 1-­year follow-­up. tained and reviewed for suitability based on the inclusion
4. Outcome based on a clinical examination and a radio- and exclusion criteria of the proposed systematic review.
graphic evaluation (Tsesis et al., 2013). Any disagreements or doubts were resolved by discussions
5. Radiographic evaluation based on periapical radio- with a third reviewer. Articles identified as suitable arti-
graphs (Rud et al. and/or Molven at al criteria; Molven cles were subjected to data extraction, assessment of the
et al., 1987; Rud et al., 1972a, 1972b), or on cone beam methodological quality, and data synthesis and analysis.
computed tomography (CBCT; Schloss et al., 2017).

Exclusion criteria: Data collection process and data items

1. Previous endodontic surgery (re-­surgery cases). Data were extracted by two independent observers,
2. Root fractures or root perforations. with any disagreements or doubts resolved by discus-
3. Retrospective study design. sions with a third reviewer. The parameters recorded
4. Case reports, reviews, and expert opinions. for each study included the authors' names and the date
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ROSEN et al.    913

of publication, as well as the following methodologi- up to five items scored ‘yes’ (Polmann et al., 2019; Valesan
cal variables: study purpose; sample size; demographic et al., 2021).
details of the subjects, inclusion criteria; study design; The presence of a funding bias was also evaluated in all
randomization method, evaluators' blinding, and homo- the studies, as well as the declaration of the presence of
geneity of the subjects. any conflict of interest.
Additional details recorded for each study were: le- In cases in which there was a discrepancy between the
sion size (small if diameter < 10 mm, or large if diam- two reviewers, an agreement was reached by discussion,
eter ≥ 10 mm); the GTR protocol: the use of a barrier otherwise, a third reviewer was consulted until a consen-
membrane (yes\no) and the type of membrane (resorb- sus was achieved.
able or non-­resorbable), grafting at the site (yes\no) and
the type of bone substitute, the use of platelet-­rich plasma
(PRP) or platelet-­rich fibrin (PRF) (yes\no) (4, 28); and the Data synthesis and analysis
timing of adjunct periodontal surgery (during or follow-
ing the endodontic surgery). A comparative meta-­analysis of the results was not feasi-
In order to assess the success of the treatment, the pri- ble due to the heterogeneity of the study protocols. For this
mary outcome was the healing of the periapical lesion that reason, a quantitative analysis was performed by pooling
was graded according to the following four-­item outcome the results from the single studies about the success rate
classification: complete healing, incomplete healing (scar), of the procedure.
uncertain healing, and unsatisfactory healing. The success
of the treatment was assessed by radiographic healing cri-
teria (Molven et al., 1987; Rud et al., 1972a, 1972b) and RESULTS
a clinical evaluation. Regardless of the radiographic eval-
uation, a case was considered a failure if a clinical sign The systematic search performed using the electronic da-
or symptom, such as pain, swelling, tenderness to percus- tabases retrieved only four papers suitable for the review.
sion or palpation, or sinus tract was present. In addition No additional articles were found using the adjunctive
to the four-­item outcome analysis, the outcome data were search of the references or the manual search of journals
adjusted to a dichotomized success/failure classification. and grey literature. A summary of the article selection
For this purpose, the categories complete and incomplete process is presented in Figure 1. Three studies (Dhiman
healing were combined and considered ‘success’; while et al., 2015; Goyal et al., 2011; Marin-­Botero et al., 2006)
the categories uncertain and unsatisfactory healing were are randomized controlled clinical trials (RCTs), while the
similarly combined as ‘failure’. fourth (Kim et al., 2008) is a prospective cohort study. The
characteristics of the studies are presented in Table 1.
ROB 2.0 tool (Sterne et al., 2019) assessment revealed
Methodological quality assessment that one of the three RCTs had a ‘low risk of bias’ (Marin-­
Botero et al., 2006), while two other studies were judged
The methodological quality of each of the selected stud- as having ‘some concerns’ (Dhiman et al., 2015; Goyal
ies was evaluated by two independent reviewers as part et al., 2011), The JBI critical appraisal tool judged the
of the data extraction process. Randomized controlled study by Kim and co-­workers, published in 2008, as hav-
trials were evaluated using the Cochrane's collaboration ing some concerns (Kim et al., 2008). A summary of the
risk of bias tool 2.0 (RoB 2.0) (Sterne et al., 2019), while risk of bias evaluation for RCTs is presented in Figure S1
non-­comparative studies were evaluated using the ap- (using the ROB 2.0 tool). None of the studies reported the
propriate JBI critical appraisal tool (Munn et al., 2020; presence of a funding bias, since just one of them clearly
Tufanaru et al., 2020). When using RoB 2.0, the studies stated the source of funding (Marin-­Botero et al., 2006).
were judged as having a ‘low risk of bias’, ‘some concerns Due to the heterogeneity in study design, and of the
of bias’, or a ‘high’ risk of bias for each of the following characteristics of the population and of the interventions
domains: bias arising from the randomization process, it was not possible to perform a meta-­analysis of the re-
bias due to deviations from intended interventions, bias sults, comparing two treatments. Thus, just a qualitative
due to missing outcome data, bias in measurement of the and descriptive analysis of the results of these four studies
outcome, bias in selection of the reported results. When is presented.
evaluating case series using the JBI critical appraisal tool, The studies describe the treatment of a total of 174
studies were judged as having a ‘low risk of bias’ if at least teeth with endodontic-­ periodontal lesions of which
8 items on the checklist scored ‘yes’; ‘some concerns of 153 (87.9%) were analysed. All subjects were treated by
bias’ if 5–­7 items scored ‘yes’; and a ‘high risk of bias’ if the ‘modern’ surgical endodontics technique (Dhiman
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914    EFFECT OF GTR ON ENDO SURGERY WITH ENDO-­PERIO SR

Identification of studies via databases and registers F I G U R E 1 The results of the

literature search. GTR, guided tissue
regeneration.
Identification

Records identified from:

Databases (n = 321): Records removed before screening:
MEDLINE (n = 258) Duplicate records removed (n = 21)
Embase (n = 25)
Scopus (n = 38)

Records screened
Records excluded (n = 271)
(n = 300)

Reports sought for retrieval Reports not retrieved

Screening

(n = 29) (n = 0)

Reports assessed for eligibility Reports excluded:

(n = 29) No modern technique (n = 9)
Cases without endodontic
periodontal lesions (n = 10)
No use of GTR technique (n = 3)
Other study types (including
retrospective) (n = 7)
Included

Studies included in review

(n = 4)

TABLE 1 Summary of study characteristics.

Authors Year Study type Country Demographics Diagnosis

Marin-­Botero 2006 Randomized controlled Colombia 30 patients; age 19–­70 years; Suppurative chronic
et al. clinical trial 78 females in the apical periodontitis
graft group; mean age and apicomarginal
43.7 years in the graft communication
group
Kim et al. 2008 Prospective cohort study South Korea For the entire sample: Class D–­F from Kim
age 14–­70 years; 33.5% & Kratchman
male; 59 teeth with classification
apicomarginal lesions
Goyal et al. 2011 Randomized controlled India 30 patients/30 teeth; age 17–­ Suppurative chronic
clinical trial 45 years; 17 males apical periodontitis
and apicomarginal
communication
Dhiman et al. 2015 Randomized controlled India 30 patients/30 teeth: age 17–­ Suppurative chronic
clinical trial 47 years; 19 males; mean apical periodontitis
age 17.9 years in the test and apicomarginal
group communication

et al., 2015; Goyal et al., 2011; Kim et al., 2008; Marin-­ Goyal et al., 2011; Marin-­Botero et al., 2006), ranged from
Botero et al., 2006). Only one study reported data about 56.3 to 115.5 mm.
tooth location, and in this case about half the treated teeth Intermediate restorative material (IRM) was used ex-
were in the posterior area (premolars and molars; Marin-­ clusively as a root-­end filling material in one study (Marin-­
Botero et al., 2006). However, all four studies provided de- Botero et al., 2006), while two studies used MTA as the
tails about the magnification device used (oral microscope exclusive root-­end filling material (Dhiman et al., 2015;
in three studies; Dhiman et al., 2015; Goyal et al., 2011; Goyal et al., 2011), the fourth study used either IRM, super
Kim et al., 2008), and magnification loupes in the last EBA or MTA randomly (Kim et al., 2008). With regard
study (Marin-­Botero et al., 2006). The average size of the to the GTR procedure, bone substitute was used in one
lesions (reported in three papers; Dhiman et al., 2015; study (Kim et al., 2008), a membrane composed of platelet
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ROSEN et al.    915

derivatives was used as an enhancer for bone healing in an- considered essential for periodontal healing, particularly
other two reports (Dhiman et al., 2015; Goyal et al., 2011) in non-­contained defects (Nibali et al., 2020). Thus, the
and a periosteal graft or an absorbable membrane was use of GTR protocols, could find an indication in cases of
used in the fourth study (Marin-­Botero et al., 2006). non-­contained periodontal defects since the use of GTR
The follow-­up period was 12 months in three of the protocols allows the defect to be isolated, thereby promot-
included studies (Dhiman et al., 2015; Goyal et al., 2011; ing repopulation of the lesion by periodontal ligament
Marin-­Botero et al., 2006), and up to 60 months for the (PDL) and bone cells, while preventing more rapidly pro-
fourth (Kim et al., 2008). Pooling together the data from liferating cells (such as connective tissue and epithelial
all the included studies, the reported outcome was of com- cells originating in the gingiva) from colonizing the area.
plete healing in 58.4% of all cases, of scar tissue formation/ This prevents apical migration of the junctional epithe-
incomplete healing in 24% of cases, namely 82.4% of fa- lium, which could otherwise occur. Another advantage
vourable outcome, of uncertain healing in 12.8% of cases, of the mechanical isolation is the prevention of contam-
and of failure in 4.8% of all analysed teeth, namely 17.6% ination by bacteria from the oral cavity (Nemcovsky &
of unfavourable healing; overall 125 teeth in 125 subjects, Nart, 2019).
with a follow-­up ranging from 12 to 60 months. A sum- There are numerous studies on the outcomes of end-
mary of the results of the included studies is presented in odontic surgery using GTR techniques as an adjunct to
Table 2. One study reported that healing was uneventful the surgery in the literature (Baek & Kim, 2001; Maguire
in all cases (Marin-­Botero et al., 2006), while the other pa- et al., 1998; Taschieri et al., 2007, 2008; Tobon et al., 2002).
pers provided no information on the subject. None of the These propose the use of a variety of biomaterials as an os-
included studies presented patient reported outcomes. teoconductive scaffold for periapical surgery (Apaydin &
The study by Dhiman et al. (2015) published in 2015 Torabinejad, 2004; Barkhordar & Meyer, 1986; Beck-­Coon
that compared the use of Platelet-­rich fibrin membrane to et al., 1991; Dietrich et al., 2003; Murashima et al., 2002;
a negative control group, concluded that PRF membranes Salman & Kinney, 1992; Stassen et al., 1994; Tobon
did not significantly improve the outcomes when used in et al., 2002; von Arx et al., 2003; Yoshikawa et al., 2002).
the treatment of apicomarginal defects as compared to Some of these studies (Taschieri et al., 2007, 2008; Tobon
controls. et al., 2002) applied GTR techniques to teeth with a
healthy periodontium in order to promote periapical bone
regeneration following surgical endodontics. However,
DI S C US S I O N in other cases (Murashima et al., 2002; Oh et al., 2009,
2019; Rohilla et al., 2017; Tewari et al., 2018), GTR tech-
The root canal system and the periodontium share many niques were applied to improve the healing of marginal
potential routes of communication (Rosen et al., 2019) periodontal disease in teeth with endodontic-­periodontic
provided by the apical foramen (Rotstein & Simon 2004; lesions. The heterogeneity in inclusion criteria, study de-
Simring & Goldberg, 1964), exposed dentinal tubules sign, treatment protocols, and follow-­up periods may be
(Adriaens et al., 1988), the lateral and accessory ca- responsible for the inconsistent results, and for the obser-
nals (Gutmann, 1978), certain anatomical variations vation that none of these techniques or biomaterials has
(Arambawatta et al., 2009; Naik et al., 2014), or pathologi- yet achieved a consensus for use.
cal conditions such as root perforations and fractures. The present study was designed to resolve this issue
The important difference between endodontic and peri- by evaluating the effects of GTR on the outcome of sur-
odontal therapy is that the periodontium is usually healthy gical endodontic treatment of teeth with endodontic-­
in endodontic treatment situations, and flap elevation is periodontal lesions, by means of a systematic review of
performed only for access, whereas periodontal treatment the literature and meta-­analysis.
is usually initiated in diseased tissues. Furthermore, the The study designs considered for inclusion in the pres-
periodontal defect is usually an open wound, in commu- ent review were randomized clinical trials (RCT), con-
nication with oral cavity, whereas the endodontic lesion trolled clinical trials (CCT), and prospective case series
is primarily a closed wound (Bashutski & Wang, 2009; (PCS). These study types were chosen to cover the topic,
Lin et al., 2010). Complete periapical tissue regeneration without excluding non-­comparative studies, due to the
after surgical endodontic treatment has previously been relative lack of research in this field.
demonstrated even when a GTR protocol was not adopted Only four published studies fulfilled our selection cri-
(Kim & Kratchman, 2006; Tsesis et al., 2006, 2007, 2009; teria, and even these display a significant heterogeneity in
Zuolo et al., 2000), while the application of a regenerative study design, characteristics of the population, and in the
protocol (with or without a barrier membrane) is usually interventions performed. Since performing a quantitative
 | 916
  

TABLE 2 Summary of the results from the included studies.

Subjects/teeth treated/ Follow-­up

Study Treatment GTR/bone substitute analysed (months) Outcomes
Marin-­Botero Modern surgical endodontics Resorbable membrane 30 subjects/30 teeth 12 15 complete healing; 11 scar tissue; 2 uncertain
et al. (2006) technique; surgical loupes; healing; 2 failures
root-­end filling: IRM
Kim et al. (2008) Modern surgical endodontics Calcium 54 subjects/54 teeth included; 60; range 23 complete healing; eight scar tissue; five
technique; operating sulphate + CollaTape 40 subjects/40 teeth 12–­60 uncertain healing; four failures
microscope; root-­end filling: membrane analysed
IRM, SuperEBA, MTA
Goyal et al. (2011) Modern surgical endodontics TEST GROUP: Collagen 10 subjects/10 teeth 12 Seven complete healing; one incomplete
technique; operating membrane healing; two uncertain healing
microscope; root-­end filling: CONTROL GROUP: PRP or PRP: 6 subjects/6 teeth; 12 PRP: five complete healing; one uncertain
MTA PRP + collagen sponge PRP + collagen sponge: 9 healing PRP + collagen sponge: seven
subjects/9 teeth complete healing; one incomplete healing;
one uncertain healing
Dhiman Modern surgical endodontics TEST GROUP: PRF 15 subjects/15 teeth 12 Eight complete healing; five scar tissue; two
et al. (2015) technique; operating uncertain healing
microscope for most phases; CONTROL GROUP; None 15 subjects/15 teeth 12 Eight complete healing; four scar tissue; three
root-­end filling: MTA uncertain healing
EFFECT OF GTR ON ENDO SURGERY WITH ENDO-­PERIO SR

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ROSEN et al.    917

synthesis (comparative meta-­analysis) is only appropriate and no GTR in endodontic-­ periodontal lesions. Cases
when the included studies are sufficiently similar to pro- judged as ‘complete healing’ represented 50%–­83.3% of all
vide a meaningful summery (Deeks & Altman, 2022), it cases, with 10%–­36.7% of cases ranked ‘scar tissue/incom-
was, therefore, inappropriate, and only a qualitative, nar- plete healing’, ‘uncertain healing’ in 6.7%–­20% of cases,
rative analysis of the results was performed. and failure in 0%–­10% of all treated teeth. Two studies
Bias may be defined as ‘a systematic error, or devia- (Goyal et al., 2011; Marin-­Botero et al., 2006) reported no
tion from the truth, in results or inferences’ that may lead cases of unsatisfactory healing although it is unrealistic to
to a false estimation of the intervention effect (Higgins expect a 100% success rate for any treatment modality. The
et al., n.d.). A systematic review of data obtained from absence of failures in these studies may be attributed to
studies of variable validities may result in wrong conclu- strict case-­selection, and the type of defects (i.e. minimal
sions, and differences in risks of bias among the identi- or no bone loss in the proximal area). Notably, proximal
fied studies may explain the variation in the results of the defects, which have a less favourable prognosis than de-
studies included in a systematic review. Thus, it is crucial fects confined to the buccal surface were excluded from
to assess the risk of bias in the studies in a systematic re- these studies (Goyal et al., 2011; Marin-­Botero et al., 2006).
view (Higgins et al., n.d.). In the present systematic re- Regarding the factors evaluated in our survey, it was
view the methodological quality of the included studies not possible to identify a significant influence of any spe-
was appraised, and was described as the risk of bias in cific patient/tooth based/operative factor on the outcome
included studies (Higgins et al., n.d.). RCTs were evalu- in the included studies.
ated using the Cochrane collaboration risk of bias tool The average size of the lesions (reported in three pa-
2.0 (Sterne et al., 2019), while case series were evaluated pers; Dhiman et al., 2015; Goyal et al., 2011; Marin-­Botero
using the appropriate JBI critical appraisal tool (Munn et al., 2006) ranged from 56.3 to 115.5 mm. Although res-
et al., 2020; Tufanaru et al., 2020), since some of the bias ident osteoblasts, PDL cells, and cementoblasts might be
domains (mainly randomization and blinding) by which capable of restoring damaged periapical tissues in small
randomized clinical trials are assessed are not applicable periapical lesions, wound healing of larger defects re-
when assessing a case series study design. By the JBI tool, quires the recruitment and differentiation of progenitor
one study (Kim et al., 2008) was judged as having some cells/stem cells (Grzesik & Narayanan, 2002). According
concerns of bias. However, by the Cochrane collaboration to Andreasen and Rud (1972), osseous regeneration can-
ROB 2.0 tool (Sterne et al., 2019), one of the three RCTs not repair a large wound and the defect will then be filled
(Marin-­Botero et al., 2006) was judged as having a ‘low by fibrous connective tissue (Andreasen & Rud, 1972).
risk of bias’, with the other two (Dhiman et al., 2015; Goyal In the included studies, there were no information on
et al., 2011) raising ‘some concerns’. Overall, the identified the primary aetiology of the lesions that were treated. The
studies presented a moderate risk of bias. authors can assume that, due to the different aetiopatho-
Only studies in which the cases were followed up for genesis, endodontic-­periodontal lesions of primary end-
at least one year after the surgery were included. This odontic origin and lesions of primary periodontal origin
was the follow-­up time for three of the studies (Dhiman could need different treatment approaches and may have
et al., 2015; Goyal et al., 2011; Marin-­Botero et al., 2006) a different prognosis (Rosen et al., 2019). Unfortunately,
with only one study (Kim et al., 2008) that included a the studies included in the present review did not provide
group of 40 teeth that were followed up for 12–­60 months enough data to speculate on such aspect.
following the surgery. Evidence for a stable long term out- Moreover, just one study evaluated the combined
come comes from a study by Rud et al. (1972a, 1972b), use of a collagen membrane and bone substitute (Kim
which reported a solid correlation between the outcome et al., 2008), while the others used other types of
diagnosed 1 and 4 years following surgical endodontic biomaterials.
treatments. Similarly Rubinstein and Kim (1999, 2002) re- A recently published systematic review and network
ported that 91.5% of the cases diagnosed as healed 1 year meta-­ analysis examined the influence of GTR tech-
following endodontic surgical treatments remained healed niques on the outcome of surgical endodontic treatment
for an additional 5–­7 years. However, since these studies (Zubizarreta-­Macho et al., 2022). The inclusion criteria
involved teeth with purely endodontic lesions and without included randomized controlled trials with a minimum
GTR, they should not be considered fully comparable to of 6 months follow-­up. Lesion type was not limited and
the cases analysed in the present systematic review. included cases with apical and apicomarginal lesions.
The benefit of GTR for the treatment of endodontic-­ Eleven RCTs were included in the final data synthesis
periodontal lesions in the include studies is difficult to de- and analysis. The network meta-­analysis compared sev-
termine because of the absence of studies comparing GTR eral techniques indirectly via control group. The authors
 |

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918    EFFECT OF GTR ON ENDO SURGERY WITH ENDO-­PERIO SR

concluded that GTR techniques increased the success involved in conceptualization, methodology, supervision,
rate of surgical endodontic treatments. Consequently, the review and editing. Eitan Kavalerchik involved in investi-
authors state that they recommend the use of bone grafts gation, project administration, review and editing. Rahaf
combined with barrier membranes in surgical endodontic Salem involved in data curation, investigation, project ad-
procedures. Our study differs in the fact that it's limited ministration, resources, original draft preparation. Adrian
to endodontic-­periodontal lesions, with a minimum fol- Kahn involved in conceptualization and visualization.
low-­up period of at least 1 year. Moreover, in addition to Massimo Del Fabbro involved in formal analysis, method-
RCTs, prospective case series were also included in the in- ology and visualization. Silvio Taschieri involved in formal
clusion criteria as well. analysis, methodology and visualization. Stefano Corbella
This is the first systematic review to evaluate the effect involved in conceptualization, formal analysis, methodol-
of GTR techniques on the outcome of surgical endodon- ogy, original draft preparation, review and editing.
tic treatment in teeth with endodontic-­ periodontal le-
sions, since these were excluded in a previous publication ACKNO​WLE​DGE​MENTS
(Tsesis et al., 2011). The study was self-­funded.
However, the results of the current systematic review
should be interpreted with caution due to the scarcity of FUNDING INFORMATION
high-­quality studies with a large sample size currently None.
available in the literature and to the absence of compara-
tive studies evaluating GTR versus no GTR. Moreover, the CONFLICT OF INTEREST STATEMENT
heterogeneity in study design, treatment protocol, and fol- The authors deny any conflict of interest.
low-­up periods of the included studies limits the ability to
draw strong conclusions. Furthermore, when evaluating DATA AVAILABILITY STATEMENT
the outcomes reported in the studies included in the re- Data sharing is not applicable to this article as no new data
view, we should consider that they were reported based on were created or analyzed in this study.
bidimensional periapical radiographs that did not allow to
evaluate the reconstruction of the bony buccal plate, thus ETHICS STATEMENT
impeding to evaluate if a hard tissue dehiscence remained This systematic review did not need the Ethics Committee
referred to the tooth root. Approval due to the absence of research with patients.
Nevertheless, the current systematic review is the best
available evidence on this topic, and our investigations ORCID
may offer some insight into the continuing search for al- Igor Tsesis https://orcid.org/0000-0002-5824-0379
ternative treatment modalities for compromised teeth that Eitan Kavalerchik https://orcid.
are often destined for extraction. org/0000-0001-8319-1786
More research, with well-­ defined inclusion criteria Massimo Del Fabbro https://orcid.
for cases, comparing different approaches for the surgical org/0000-0001-7144-0984
treatment of endodontic-­periodontal lesions and the use Stefano Corbella https://orcid.
of 3D imaging is needed to increase the scientific burden org/0000-0001-8428-8811
of the evidence about this topic.
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SUPPORTING INFORMATION
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Additional supporting information can be found online
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