CASE REPORT/CLINICAL TECHNIQUES

Abayomi O. Baruwa, BDS, PhD*

Management of Apico-marginal Jorge N. R. Martins, DDS, MSc,
PhD*†‡ Mariana D. Pires, DDS,
Defects With Endodontic MSc* Beatriz Pereira, DDS,
MSc* Pedro May Cruz, DDS,
Microsurgery and Guided MSc* and Anto
nio Ginjeira, MD,
DMD, PhD*†
Tissue Regeneration: A Report
of Thirteen Cases

ABSTRACT
SIGNIFICANCE
The loss of periodontal tissue support and vertical buccal bone loss in apico-marginal defects
can often be mistaken for features indicative of vertical root fractures and this study reports Apico-marginal defects could
thirteen cases with persistent symptomatic apical periodontitis, apico-marginal defects, and be mistaken for vertical root
large periapical lesions that were managed with endodontic microsurgery in conjunction with fracture due to the similarity in
bone grafts and barrier placements with a follow-up period of up to 9 years. At the recall clinical presentation of alveolar
sessions, all cases were asymptomatic with radiographical success with only 2 cases bone loss. Hence the
exhibiting residual apical radiolucency, but with evident reduction in the lesion size, indicative diagnosis and type of
of healing. This study highlights the potential of utilizing endodontic microsurgery combined periodontal.
with guided tissue regeneration that proved effective in stimulating the regeneration of
periodontal tissue in cases of apico-marginal defects that can lead to favourable long-term
outcomes. (J Endod 2023;49:1207–1215.)

KEY WORDS
Apico-marginal defect; endodontic microsurgery; guided tissue regeneration; periodontal
bone loss

Endodontic microsurgery (EMS) procedure aims at surgically eradicating persistent peri-radicular From the *Faculdade de Medicina
infection in teeth where nonsurgical endodontic retreatment had failed, or a retreatment is not viable due Denta
ria, Universidade de Lisboa; †Grupo
de Investigaça~o em Bioquimica e Biologia
to anatomic complexities or in cases of heavily restored teeth with cast posts and/or crown1. This
Oral, Unidade de Investigaça ~o em
procedure is performed by using a retrograde approach whose success depends on controlling
Ci^encias Orais e Biome
dicas (UICOB),
microorganism leakage and their byproducts from the root canal system to the periodontium1,2. In the Faculdade de Medicina Denta
ria,
past 4 decades, the introduction of the clinical microscope, new micro-instruments, and retrograde Universidade de Lisboa; and ‡Centro de
apical sealing material, such as mineral trioxide aggregate (MTA), together with a better understanding of Estudo de Medicina Dent
aria Baseada na
Evid^encia (CEMDBE) - Cochrane
the healing process, has made EMS significantly evolved in comparison to the conventional surgical
Portugal, Faculdade de Medicina
endodontics, becoming in many situations a viable alternative to the extraction of teeth with the eventual Denta
ria, Universidade de Lisboa, Lisboa,
replacement with endo-osseous implants. EMS is no longer considered a solution of last resort1,3. The Portugal
differences between the conventional and the current microsurgical techniques are very relevant and Address requests for reprints to Dr
have been well described and documented in literature1,3,4. Hence, the success rates have gone from an Abayomi O. Baruwa, Faculdade de
average of 62%5 to averages higher than 90%6,7. This difference is even more marked at the level of Medicina Dent
aria da Universidade de
posterior teeth where rates of around 44%8 have increased to above 90%9. With increasing overall
ria, Lisboa
Lisboa, Cidade Universita
1649-003, Portugal.
success rates, EMS has gained popularity. However, clinicians may encounter prognostically challenging
E-mail address: baruwaabayomi@gmail.
apico-marginal defects, characterized by localized bone loss along the root’s entire length, often on the com
buccal side. This characteristic can be mistaken for a vertical root fracture10. Retrospective studies 0099-2399
indicate that conventional surgical techniques yield success rates as low as 27%11,12, while EMS shows Copyright © 2023 The Authors. Published
78% success, lower than the reported 95% in the absence of these defects13. by Elsevier Inc. on behalf of American
The guided tissue regeneration (GTR) technique has shown promising results in improving the Association of Endodontists. This is an
prognosis of cases with apico-marginal defects14. However, the prognosis may depend on the open access article under the CC BY
license (http://creativecommons.org/
characteristics and extent of the bone defect. Establishing a differential diagnosis can be challenging due licenses/by/4.0/).
to the potential endodontic, periodontal, or combined etiology of these defects. Therefore, a classification https://doi.org/10.1016/
system is essential to guide treatment planning and determine the prognosis for each clinical case10, also j.joen.2023.07.009

JOE  Volume 49, Number 9, September 2023 Apico-marginal Defects With Endodontic Microsurgery and GTR 1207
considering the morphology, etiology, and
pathogenesis of these defects is crucial for
accurate classification6,10. Kim’s classification,
which incorporates clinical and radiographic
findings, has gained consensus15. It consists
of 6 stages (A–F), with Classes A, B, and C
having a favorable prognosis and Classes D, E,
and F presenting larger bone defects, requiring
technically demanding resolutions that may
involve GTR techniques. The principles of GTR
have been applied in implantology to
regenerate bone defects and enhance alveolar
ridge augmentation with local application of
growth factors and modulating agents have
been used to maximize tissue response16,
such as rhBMP-2 proteins17, enamel matrix
derivatives18, and growth factor-rich plasma19.
Membrane usage in GTR and guided bone
regeneration (GBR) has become standard in
periodontology and implantology, making it a
potentially effective technique for treating
endodontic-periodontal lesions6. Similarly,
surgical endodontic treatments aim to
regenerate peri-radicular tissues, including
cementum, periodontal ligament, and alveolar
bone, aligning with the goals of GTR6,20. Bone
grafts play a significant role in GTR
procedures, especially when space
preservation for regeneration is critical.
However, their application can be controversial
in some situations. Grafts derived from
different sources, with ideal properties of
osteoinduction, osteoconduction, and
osteogenesis, can be utilized and among these
options, autogenous grafts, which possess all
3 desired properties, are still widely regarded
as the gold standard in this context16.
Clinical cases with apico-marginal bone
defects, specifically those classified as Kim’s
class F, have been recognized as challenging
with a reserved prognosis. Therefore, the
objective of this study is to present a
successful management approach utilizing
both endodontic microsurgery and guided
tissue regeneration in 13 cases with a follow-
up period of up to 9 years.
CASE REPORT
This present report documents 13 clinical
cases from 12 Portuguese patients, aged 30–
75 years involving different tooth types:
7 molars, 2 premolars, and 4 central and lateral
incisors, that complained of persistent pain
following endodontic treatment or retreatment,
except for case 5 where a previous apical
surgical treatment had been performed. The
patients had noncontributory medical histories
as at the first appointment. At examination,
inspection of soft tissues for the presence of
fistulas and/or fractures was performed. All
cases had restorations (fillings and crowns),
1208 Baruwa et al.
with positive response to palpation of the
buccal and lingual apical regions, percussion,
and continuous periodontal probing of the
affected tooth. Further intra-oral examination
was performed to evaluate the status of
adjacent teeth with obligatory pulp sensitivity
tests (using cold test with ethyl chloride and
possibly electrical test) and radiographic
examinations of all teeth (Fig. 1A–C).
From the clinical history and
examinations, a pulpal and apical diagnosis
was made for each case which is documented
in (Table 1) and the findings were discussed
with each patient, including the various
therapeutic options. Patients were therefore
involved in the therapeutic decision and signed
an informed consent. Oral and written
instructions for preoperative care were given.
Additionally, the patients were asked to start
rinsing with chlorhexidine elixir 0.2% (3 times a
day for at least 30 seconds) 2 days before the
surgery, and to start antibiotic coverage with
Amoxicillin (Clamoxyl 1 g) every 8 hours. They
were also asked to start oral nonsteroidal anti-
inflammatory therapy (Ibuprofen/Brufen or
Nimesulide/Nimed) the day before. Sedation
was not necessary in any of the cases and all
patients were warned not to fast.
All 12 endodontic microsurgeries for
apico-marginal lesions correction of primary
endodontic etiology had the same procedures
and were performed by the same single
clinician (PMC) between 2011 and 2015 with a
technique of guided tissue regeneration with
Bio-Gide (Geistlich Biomaterials, Wolhusen,
Switzerland) resorbable membrane and with or
without placement of bone graft (xenograft or
autogenous) on the buccal wall of the root
stripped of alveolar bone. The procedures
were performed under local anesthesia with
infiltrative technique in the buccal and palatal
sides. Four or 5 anesthetic cartridges of 2%
lidocaine with epinephrine 1:100,000
(Xilonibsa, Inibsa, Spain) were used per
patient. After completion of the anesthetic
technique, a full thickness triangular flap was
made (Fig. 1D) with a 15C blade, aided by an
endodontic microscope (OPMI Pro Ergo, Carl
Zeiss, Oberkochen, Germany), with the vertical
incision being made one to two teeth per
mesial of the involved teeth, when the surgery
was in the posterior sextants, or one to two
teeth per distal in the second sextant. Table 1
highlights the differences in bone defects, flap
design, and augmentation technique used for
all cases.
The flap, after detachment with a 2/4
Molt detacher (Henry Schein, New York, USA),
was held in place with a Carr retractor (Sybron
Endo, Orange CA, USA). At this point the Kim’s
class F type of defect was observed. Then the
granulation tissue was removed (Fig. 1E) with
Lucas’s type curettes and mini-Jaquette and/
or Gracey 3/4 curettes. The root was
inspected for possible vertical fractures,
eventually using a methylene blue dye. In the
most cervical region of the exposed root, a
very light passage was made with the lateral
part of the Kiss ultrasound tips (Dentsply,
Ballaigues, Switzerland) without having as an
objective to try to perform a root smoothing. As
in none of these cases vertical fractures were
observed, the procedure continued after the
patients had been warned that in these Kim’s
class F defects, the prognosis is not so
favorable.
The ostectomy (in these cases required
very slight removals to improve access to the
apical area) and 3-mm apicectomy, without
beveling, were performed using a laminated
tungsten truncated cone drill and an Impact air
45 turbine with distilled water. Thinner bone
was removed only with curettes. After the
apicectomy (Fig. 1F), the removal of the
granulation tissue was completed with small
curettes and a mini-Jaquette curette around
the periodontal ligament space. The "new"
apex was then inspected with micro mirrors
(Hufriedy, Chicago, USA) to locate the canals
and look for micro fractures. The retrograde
cavities were performed with nondiamond
ultrasound tips (Sybron Endo, Orange CA,
USA) and Kiss tips (Dentsply, Ballaigues,
Switzerland) coupled in a piezoelectric
ultrasound unit (Satelec Acteon, Cedex,
France) (Fig. 1G). The cavities, after being dried
with micro tips (Ultradent, Utah, USA) attached
to a Stropko adapter (Vista Dental, CA, USA),
were inspected (Fig. 1H) for possible fracture
lines, presence of internal debris and to
confirm the retro prepped cavity shape. White
MTA (Dentsply, Ballaigues, Switzerland) was
placed in the cavity, as the root-end filling
material (Fig. 1I), with a wall-carver, and
compacted and burnished with a micro
presser and a micro burnisher, respectively
(Sybron Endo, Orange CA, USA), while the
excesses were removed in the end. The
materials used for obtaining hemostasis were
ActCel (Coreva Health Sciences, CA, USA),
Collacote (Zimmer Biomet, Indiana USA) or
Spongostan (Johnson & Johnson, New
Jersey, USA) and for protecting the bone loca
a Telfa compress (Covidien, Dublin, Ireland)
was used, which was removed after the
procedure. In the end, the loca was curetted
again to obtain a good blood clot.
In some of the cases, the bone-deprived
buccal portion of the root was then covered
either with a bovine bone graft (Bio-Oss,
Geistlich Biomaterials, Wolhusen, Switzerland)
or with the patient’s own bone collected from
the cortical bone of the surgical site using bone
scrapers (Micro-Oss/ACE, Henry Schein, New
JOE  Volume 49, Number 9, September 2023
York, USA) or with both options. Then the graft
zone, or just the root, as well as the entrance of
the bone loca were covered with a resorbable
collagen membrane (Bio-Gide, Geistlich
Biomaterials, Wolhusen, Switzerland), always
taking care to cover the margins with at least
two millimeters. The tissues were re-
approximated and sutured with Tevdek 4/
0 (Tevdek II, Henry Schein, New York, USA). A
sling-suture was made with a slight
modification and the remaining sites with
interrupted stitches. At the end, a light
compression of the tissues with a wet gauze
was made for a better adaptation of the graft
area.
Postoperative instructions were given
verbally and in writing, including intense but
discontinuous application of cold to the face in
the following hours, soft food in the following
days, no brushing in the surgical area, at least
until the sutures were removed, and continued
rinsing with chlorhexidine elixir at 0.2% until
approximately one month with the additional
care of very gentle rinsing in the following days.
The sutures were removed 3–7 days later.
Afterwards, the patients were asked to
carefully apply a chlorhexidine gel daily (at
night) on the most cervical part of the clinical
crown of the tooth near the free gingiva,
around the defect for about 2 months. Soft
tissue clinical checks were carried out after 1
month and radiographic controls every 6
months until radiographic healing of the lesion
whenever possible (Fig. 1J–L). A new
periodontal probe was carried out not earlier
than 6 months after surgery. The treatments
documentation is summarized in Figures 1–3
and in Table 1.
In all the cases presented, none of the
patients reported pain, either spontaneous or
upon palpation and/or percussion, and there
were no instances of fistulas, periodontal
pockets, or mobility associated with the
surgically treated teeth. Radiographic
evaluations showed complete or partial
resolution in cases 6 and 7 of periapical
radiolucency, indicating symptom remission
and apparent healing of chronic apical
periodontitis during the follow-up period. The
corresponding follow-up duration for each
case is provided in Table 1.
DISCUSSION
The presented cases highlight the
prognostically reserved Kim’s class F defect
characterized by endo-periodontal lesions
primarily caused by endodontic factors with
secondary periodontal involvement and
associated marginal bone defects in various
teeth. These cases were successfully
managed using microsurgery combined with
guided tissue regeneration utilizing bone
grafts. Although studies have documented
healing rates of endodontic microsurgery, with
follow-up periods of at least one year, ranging

FIGURE 1 – Detailed and representative clinical image series for Case 1 (tooth 16): (A ) preoperative radiograph of the upper right first molar; (B ) initial clinical photograph; (C )
periodontal probing depth on the buccal surface of the tooth; (D ) granulation tissue and bone defect following the surgical flap; (E ) loca of the defect after granulation tissue removal;
(F ) root end resection; (G ) root end preparation with ultrasonic tip; (H ) inspection of retro-preparation with micro-mirror; (I ) retrograde filling with MTA; (J ) follow-up radiograph at one
year; (K ) clinical photograph at 8 years follow-up; (L ) follow-up radiograph after 8 years.

JOE  Volume 49, Number 9, September 2023 Apico-marginal Defects With Endodontic Microsurgery and GTR 1209
 1210
Baruwa et al.

TABLE 1 - Demographic Data of Reported Cases With the Respective Clinical Finding, Diagnosis, Flap Design, Materials Used in the Endodontic Microsurgery Procedure and Years of Follow-Up

Periodontal Bi-cortical bone

probing defect Kim’s Root end filling Follow up
Case Age Gender Tooth (Yes/No) Diagnosis (Yes/No) classification Flap design Bone augmentation material (y)
1 49 Male 16 Yes PTT/SAP No F Intrasucular Biooss MTA 8
2 75 Female 26 Yes PTT/SAP No F Intrasucular/Papila base incision BioOss 1 autologous bone MTA 5
3 67 Female 26 Yes PTT/SAP No F Intrasucular BioOss 1 autologous bone MTA 7
4 57 Male 26 Yes PTT/SAP No F Intrasucular BioOss MTA 8
5 60 Female 21, 22 Yes PTT/SAP No F Intrasucular/Papila base incision BioOss MTA 9
6 36 Male 11 Yes PTT/SAP Yes F Intrasucular/Papila base incision BioOss MTA 3
7 44 Male 46 Yes PTT/SAP No F Intrasucular BioOss 1 autologous bone MTA 2
8 30 Male 16 Yes PTT/SAP No F Intrasucular BioOss MTA 8
9 67 Female 16 Yes PTT/SAP No F Intrasucular BioOss MTA 8
10 59 Male 25 Yes PTT/SAP No F Intrasucular BioOss 1 autologous bone MTA 5
11 63 Female 35 Yes PTT/SAP No F Intrasucular Biooss MTA 8
12 61 Male 21 Yes PTT/SAP No F Intrasucular/Papila base incision Biooss MTA 3

PPT, previous treated tooth; SAP, symptomatic apical periodontitis.

JOE  Volume 49, Number 9, September 2023
FIGURE 2 – Summarized clinical image series for cases 2–7 showing as follows: (A ) preoperative radiograph; (B ) granulation tissue and bone defect following the surgical flap; (C )
loca of the defect after granulation tissue removal; (D ) root end resection; (E ) follow-up periapical radiograph.

JOE  Volume 49, Number 9, September 2023 Apico-marginal Defects With Endodontic Microsurgery and GTR 1211

FIGURE 3 – Summarized clinical image series for cases 8 to 12 showing: (A ) preoperative radiograph; (B ) periodontal
probing depth/exposure of apico-marginal defect; (C ) radiograph at follow-up.
from 77% to 96%2,3,20,21. It has been
observed that the survival rates decline,
particularly after 5 years, especially in cases
with larger lesions or defects2,22. In a
prospective study conducted in South Korea,
Kim demonstrated a success rate of 78% for
cases classified as Kim’s classes D, E, and F,
1212 Baruwa et al.
compared to 95% for cases classified as
classes A, B, and C, emphasizing the
significance of the marginal bone factor23.
Follow-up evaluations revealed complete
resolution of clinical symptoms in all cases, and
most cases demonstrated periapical
normalization on radiographs. However, 2
cases (cases 6 and 7) with the least follow-up
period of up to 3 years showed a progressive
reduction in the size of the radiolucent area,
indicating the healing of periapical tissues and
bone regeneration. Notably, these 2 cases
presented with a larger lesion, with case 6
demonstrating an extensive bone defect
impacting both cortical plates. The healing and
remodeling trajectory of these cases may vary
depending on the aforementioned factors.
While an overall conclusive success cannot be
attributed to all cases at this point, the
outcomes thus far can generally be classified
as favorable and indicative of a good response
following the employed techniques and
approach used. In comparison to previous
reports without the utilization of GTR
technique, it is noteworthy that lower success
rates were observed in 2 retrospective studies
conducted by Hirsch in 197911 and Skoglund
in 198512. These studies achieved only a 27%
and 37% cure rate, respectively, in similar
cases; however, it is important to acknowledge
that an operating microscope enhancement
was not employed. Conversely, in 2003,
Dietrich reported a success rate of 83% by
incorporating Bio-Oss as graft and Bio-Gide
membrane as a barrier24. The relatively lower
success rates observed in cases with apico-
marginal defects, ranging from 27% to
44%11,12,24, can be attributed to the absence
of magnification and the omission of guided
tissue regeneration (GTR) technique. Some
studies utilized nonresorbable membranes
made of expanded polytetrafluoroethylene
(ePTFE) or resorbable membranes like
collagen, while others employed a combination
of membrane types with a bone graft, typically
of bovine origin16. However, limited research
has been published in this area, and the
literature search revealed divergent protocols
with apparently positive outcomes, as well as
seemingly similar protocols with contradictory
results. For example, Pecora25 concluded that
placing an ePTFE membrane (without bone
graft) at the entrance of a lesion larger than
10 mm in diameter, as measured on
radiographs and lacking apico-marginal
communication, leads to accelerated bone
regeneration. Indeed, the size of the lesion has
been identified as a significant factor, and the
association between healing and defect size
was elucidated by Hirsch11 in their study. They
found that the success rate for lesions larger
than 15 mm in diameter was only 40%,
compared to 62% for lesions around 5 mm in
diameter. Similar findings were reported by
Rubinstein26, who observed that small (up to
5 mm) and medium-sized (6–10 mm) defects
regenerated in approximately 7.25 months,
while larger defects required more time for
regeneration. Additionally, von Arx27
JOE  Volume 49, Number 9, September 2023
established a correlation between lesion
volume, defect width, and the type of healing.
One year after surgery, lesions with a volume of
approximately 395 mm3 showed better healing
compared to those with a volume of
approximately 554 mm3, and defects with a
bone window wider than 8 mm exhibited
poorer bone regeneration. Another
prospective study investigated the healing of
lesions larger than 10 mm and found no
advantage in using Bio-Oss to fill the site and
protecting it with Bio-Gide compared to the
conventional technique28.
Pompa29 reported 3 successful clinical
cases using only nonresorbable membranes
(GoreTex) without the use of any bone graft.
However, after 6 months, these membranes
needed to be removed, requiring a second
surgical intervention30. To avoid the need for
another surgical approach, resorbable
membranes have been utilized, which have
shown similar clinical and histological behavior
to nonresorbable membranes31,32. In the
presence of apico-marginal defects, these
resorbable membranes, in combination with a
xenograft (Bio-Oss) and collagen membrane
(Bio-Gide), achieved a success rate of 83%
after one year24,31,32. Collagen has been found
to promote platelet aggregation and fibroblast
migration, thereby assisting in clot stability and
surgical wound healing16. Additionally,
Britain32 demonstrated significant advantages
of using these membranes (Bio-Gide), with or
without the placement of a xenograft (Bio-
Oss), compared to not employing guided
tissue regeneration (GTR) in cases of apico-
marginal defects of primary endodontic origin.
Therefore, the placement of a barrier
membrane in surgical endodontics aims to
create an optimal environment for tissue
regeneration, similar to its application in
periodontology and implantology. This involves
the establishment of a stable and protected
blood clot, exclusion of fast proliferating
undesirable cells from the healing process in
the bone defect6, and facilitation of migration of
periodontal ligament, cementum, and bone
cells to promote true new insertion33,34.
However, it should be noted that barrier
membranes used in GTR can degrade over
time or become exposed, potentially
compromising the success of the procedure.
Secondary infections or other complications
may arise, leading to incorrect regeneration35.
A limitation of the current reported cases is that
preoperative assessment and follow-up were
based solely on periapical radiographs, as
cone-beam computed tomography was not
accessible for all cases during the procedure
due to logistical constraints. Furthermore, it is
important to note that these case reports
represent management of carefully selected
cases, and the outcomes achieved may not be
fully replicable in all patients when utilizing
similar techniques. However, it can be inferred
that factors such as the accuracy of diagnosis
and the quality and type of periodontal therapy
implemented in the presence of an apico-
marginal defect of endodontic origin may
significantly influence the obtained results.
These factors may partially explain the relatively
low clinical success rates reported in the
literature for such situations.
It is worth highlighting that apico-
marginal defects often present with clinical
features that resemble those of vertical root
fractures. Therefore, achieving a definitive
diagnosis for these cases through exploratory
surgery is of paramount importance to prevent
unnecessary extraction of potentially
salvageable teeth. Considering that controlling
the infiltration of microorganisms and their by-
products from the root canal system into the
periodontium is a fundamental prerequisite for
both surgical and nonsurgical endodontic
success23, it is crucial to utilize all available
resources. Failure to do so would likely hinder
the achievement of favorable outcomes,
particularly in the context of multi-rooted
teeth4.
CONCLUSION
Endodontic microsurgery with guided tissue
regeneration is a viable treatment option in
managing teeth with large periapical lesions
and apico-marginal defects and the outcome
achieved in these cases relied on the diagnosis
and appropriate selection of periodontal
treatment.
ACKNOWLEDGMENT
The authors deny any conflicts of interest
related to this study.

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