CASE REPORT/CLINICAL TECHNIQUES

Kamolthip Songtrakul, DDS,

Modified Apexification MS,* Talayeh Azarpajouh, DDS,*
Matthew Malek, DDS,*
Procedure for Immature Asgeir Sigurdsson, DDS, MS,*
Bill Kahler, DClinDent, PhD,† and
Permanent Teeth with a Louis M. Lin, BDS, PhD, DMD*

Necrotic Pulp/Apical
Periodontitis: A Case Series

ABSTRACT
SIGNIFICANCE
The current American Association of Endodontists clinical considerations for a regenerative
endodontic procedure state that a regenerative procedure is suitable for immature permanent A modified apexification
teeth with necrotic pulp when the pulp space is not needed for a post/core in the final procedure provides immature
restoration. Therefore, many immature permanent teeth with necrotic pulp that have permanent teeth with necrotic
sustained a substantial loss of coronal tooth structure either from caries or trauma are treated pulp/apical periodontitis
by apexification or mineral trioxide aggregate/Biodentine (Septodent, Lancaster, PA) apical requiring a post/core for a final
barrier techniques in which no further root maturation would occur. This case series presents restoration the potential of
10 immature permanent teeth with necrotic pulp in which a post/core was likely required in the continued apical root
future for adequate coronal restoration because of loss of substantial coronal tooth structure development, which is an
and a modified apexification procedure was used. All 10 cases after the modified apexification advantage over current apical
procedure showed no clinical symptoms/signs and showed radiographic evidence of healed/ barrier techniques.
healing of periapical lesion after a 2-year review. Eight cases showed increased thickness of
the apical root canal walls, increased apical root length, and apical closure. The overall
percentage change in root length was 7.52%, in root width at the apical one third it was
18.89%, and in radiographic root area it was 15.04% at the 24- to 72-month follow-up period.
This modified apexification procedure allows for the tooth to be restored with a post/core if
required for the final restoration in the future as well as continued root development. (J Endod
2019;-:1–8.)

KEY WORDS:
Apexification; apical barrier techniques; modified apexification procedure; post restoration;
regenerative endodontic procedure

Apexification is a method to induce a calcified barrier in a root with an open apex or the continued apical
development of an incompletely formed root in teeth with necrotic pulps1. The purpose of apexification is
to create an apical calcified tissue barrier at the open apex of immature permanent teeth with necrotic
pulp to facilitate root canal filling and also prevent extrusion of root canal filling into the periapical tissues.
The materials used to create an apical calcified tissue barrier can be calcium hydroxide, mineral trioxide From the *Department of Endodontics,
New York University College of Dentistry,
aggregate (MTA), and Biodentine (Septodent, Lancaster, PA)2–4. Calcium hydroxide apexification usually
New York, New York; and †School of
takes an extended period of time such as months for an apical calcified tissue barrier to form. Additionally, Dentistry, The University of Queensland,
calcium hydroxide has a poor sealing ability and poor setting. Compared with calcium hydroxide, MTA Brisbane, Australia
and Biodentine have an excellent sealing ability and take a shorter time to set. Therefore, MTA and Address requests for reprints to Dr Louis
Biodentine can serve as an apical barrier, and clinicians do not have to wait for an apical hard tissue M. Lin, Department of Endodontics, New
barrier to form. Consequently, MTA and Biodentine apical plugs have been used more often than calcium York University College of Dentistry, 345
hydroxide apexification in recent years. East 24th Street, New York, NY 10010.
E-mail address: lml7@nyu.edu
A regenerative endodontic procedure has the potential to promote thickening of the canal walls 0099-2399/$ - see front matter
and/or continued root development of immature permanent teeth with necrotic pulp/apical periodontitis5.
Copyright © 2019 American Association
The “AAE Clinical Considerations for a Regenerative Procedure”6 list under the “case consideration of Endodontists.
section” that a regenerative endodontic procedure is indicated when the “pulp space is not needed for https://doi.org/10.1016/
post/core final restoration.” Therefore, if the coronal tooth structure of the immature permanent teeth with j.joen.2019.10.009

JOE  Volume -, Number -, - 2019 Modified Apexification Procedure Case Series 1

necrotic pulp is lost because of caries or
trauma and an intraradicular post/core may be
required for adequate coronal restoration,
such immature permanent teeth with necrotic
pulp will be better treated with apexification
rather than a regenerative endodontic
procedure6. These immature permanent teeth
with necrotic pulp will be better treated with
apexification rather than a regenerative
endodontic procedure7. In apexification, an
MTA/Biodentine plug is usually placed close to
the open apex, and continued apical root
development of the arrested root of immature
permanent teeth with necrotic pulp/apical
periodontitis usually will not occur. A
polyethylene tube implant study has shown
that tissue surrounding the tubes could grow
into the lumen of polyethylene tubes if the
tubes were short and had a large luminal
diameter8. Replantation and
autotransplantation studies have also shown
that pulpal revascularization occurred more
easily with a shorter root (,8 mm) and larger
apical foramen (.1 mm) of immature
permanent teeth9,10. Based on the experience
of our published11,12 and unpublished cases of
cervical root fracture of immature permanent
teeth with necrotic pulp after a revascularized
procedure, the discussion of proper
restoration of immature permanent teeth after
treatment13–15, and the lack of continued
apical root development after traditional
apexification, the concept of modified
apexification procedure was consequently
developed to potentially promote continued
apical root development of immature
permanent teeth with necrotic pulp/apical
periodontitis for the postgraduate endodontic
program.
The suggested criteria of a modified
apexification procedure are the following:
In the modified apexification procedure,
the involved tooth is isolated with a rubber dam
under local anesthesia. The canal is
chemomechanically debrided to ensure
disruption and disinfection of bacterial biofilm
on the canal walls. A 3-mm thick
biocompatible resorbable collagen matrix is
placed in the apical canal approximately 1–2
mm from the open apex to prevent MTA/
Biodentine from extruding into the periapical
tissues. A 3-mm thick MTA/Biodentine plug is
then placed over the collagen matrix. The rest
of the coronal canal space is backfilled with
warm gutta-percha using the vertical
compaction technique (Fig. 1). The access
cavity is restored with permanent restorative
materials. The collagen matrix in the apical
canal will eventually be resorbed, leaving 4–5
mm of apical canal space unfilled for continued
apical root development. An EDTA canal rinse
and induction of periapical bleeding into the
apical canal were not used in our modified
apexification procedure.
MATERIALS AND METHODS
In the present case series, 10 immature
permanent teeth with necrotic pulp/apical
periodontitis were referred from the
department of pediatric dentistry and treated
with a modified apexification procedure
(Table 1). All immature permanent teeth with
necrotic pulp were considered likely to require
an intraradicular post/core for proper coronal
restoration in the future after the dentoalveolar
structure had completely developed. The
cases for modified apexification procedures
were treated in the postgraduate endodontic
clinic. The department of pediatric dentistry
determined the type of restoration, post or
core, and were responsible for the final
restoration of these immature permanent
teeth.
Treatment Protocol
Modified Apexification Procedure
Under local anesthesia with 2% lidocaine
containing 1:100,000 epinephrine (Dentsply
Sirona, York, PA), the involved tooth was
isolated with a rubber dam. The access cavity
was entered through the lingual surface for
anterior teeth and the occlusal surface for
posterior teeth. The pulp chamber was
irrigated with 3% sodium hypochlorite. The
canal(s) were identified. The working length of
the canals was determined with a hand K-file,
Root ZX II Apex locator (Morita, Irvine, CA), and
a conventional periapical radiograph. The
canal was chemomechanically debrided with
hand K-files and ProTaper Universal Rotary
Files (Dentsply Tulsa Dental Specialties,
Johnson City, TN) to an appropriate size to
disrupt bacterial biofilm on the canal walls and

1. Immature permanent teeth have lost

substantial coronal tooth structure for final
proper restoration. A post/core may
reinforce the strength of these teeth against
masticatory force to prevent cervical root
fracture13–15.
2. Immature permanent teeth at stage 3 and 4
root development16 because these
immature permanent teeth have an
adequate thickness of the root canal walls
and root length for intraradicular post/core if
required; immature permanent teeth at
stage 1 and 2 root development16 are
excluded because they do not have enough
thickness of the root canal walls and root
length for an intraradicular post/core.
3. A modified apexification procedure can be
an alternative treatment to traditional
apexification to encourage continued root
development. FIGURE 1 – A drawing of an immature permanent tooth to show the modified apexification procedure.

2 Songtrakul et al. JOE  Volume -, Number -, - 2019

TABLE 1 - Etiology, Pathology, and Treatment Outcome

Increased
thickness Increased
Types of of the apical apical Years of
Case Periapical Periapical apical plug root canal root Apical final
number Tooth Age Etiology Symptoms lesion healing materials walls length closure review
1 9 9 Trauma Asymptomatic Yes Yes MTA Yes Yes Yes 4
2 8 10 Trauma Asymptomatic Yes Yes MTA Yes Yes Yes 2
3 9 10 Trauma Draining sinus Yes Yes MTA Yes Yes Yes 2
tract
4 31 12 Caries Pain on biting Yes Yes MTA Yes Yes Yes 4
5 18 13 Caries Pain on chewing, Yes Yes Biodentine Yes Yes Yes 2
draining sinus
tract
6 8 10 Trauma Asymptomatic Yes Yes MTA Yes No Yes 2
7 7 28 Dens Pain on biting Yes Yes MTA No No No 3
invaginatus
8 10 18 Trauma Asymptomatic Yes Yes MTA No Yes No 3
9 29 12 Caries Asymptomatic Yes Yes MTA Yes Yes Yes 3
and dens
evaginatus
10 8 7 Trauma Asymptomatic Yes Yes MTA Yes Yes Yes 4

MTA, mineral trioxide aggregate.

irrigated with copious amounts of 3% sodium thickness of ProRoot MTA (Dentsply, Johnson The radiographic outcome was
hypochlorite. The canal was dried and dressed City, TN) or Biodentine was then prepared assessed. The preoperative and postoperative
with calcium hydroxide. The access cavity was according to the manufacturer’s instructions, images were saved in a JPEG format and
closed with a cotton pellet and Intermediate carried into the canal with the MAP system transferred to ImageJ software (version 1.41;
Restorative Material (Dentsply Sirona, (Produitis Dentaies SA, Vevey, Switzerland), National Institutes of Health, Bethesda, MD)
Charlotte, NC) for 2 weeks. and carefully condensed into the canal coronal with the TurboReg plug-in (Lausanne, VD,
At the second visit if the tooth was to the collagen matrix with measured hand Switzerland) for root length, dentin thickness,
asymptomatic, the access cavity was pluggers. Radiography was performed to check and radiographic root area (RRA)
reopened, and the calcium hydroxide was the placement of the MTA/Biodentine plug. The measurement. The images were calibrated,
removed with copious amounts of sodium rest of the coronal canal space was backfilled and the root length, dentin thickness, and RRA
hypochlorite irrigation. The canal was dried with with warm gutta-percha using a vertical from both the preoperative and reevaluation
paper points without EDTA irrigation and also compaction technique. The access cavity was images were measured, which were
no induction of intracanal bleeding from the restored with composite resin (Figs. 2–4). If the performed according to the procedure
periapical tissues. A biocompatible resorbable tooth was symptomatic, another round of described by Bose et al17, Jeeruphan et al18,
collagen matrix (Collagen Matrix, Inc, Oakland, chemomechanical debridement and calcium and Flake et al19.
NJ) of 3-mm thickness was prepared and hydroxide dressing of the canal was performed The “straight-line” tool was used to
placed into the apical canal approximately 1–2 until the tooth became asymptomatic before measure the root length and dentin thickness.
mm short of the apex using appropriate completion of the modified apexification A straight line from the cementoenamel
Buchanan hand plungers (SybronEndo, procedure. The treated teeth were reviewed junction to the radiographic apex of the tooth
Orange, CA) to prevent extrusion of MTA/ at 3, 6, and 12 months; 2 years; and up to 4 was measured as a root length. The dentin
Biodentine into the periapical tissues. A 3-mm years. thickness was obtained as the difference
between the root width and the pulpal space at
the level of the apical one third on preoperative
TABLE 2 - Radiographic Outcome and reevaluated radiographic images (below
the MTA or Biodentine apical plug).
Case Tooth Root length (%) Root width (%) Radiographic Root Area (%) The “polygon” tool was used to outline
the entire radiographic root area starting from
1 9 6.02 35.94 20.55
2 8 3.1 19.55 10.5 the mesial to the distal cementoenamel
3 9 3.38 25.73 16.20 junction and peripherally by the periodontal
4 31 8.96 22.58 11.30 ligament space. The RRA measurement was
5 18 8.08 10.94 8.98 calculated by subtracting the pulp space area
6 8 0.61 17.70 14.62 from the entire root area in each radiograph.
7 7 0.70 0.46 0.74 All radiographic measurements were
8 10 10.41 0.62 9.08 collected. The radiographic root length,
9 29 24.21 20.17 30.73 dentin wall thickness, and root area were
10 8 9.78 35.21 27.69
reported as a percentage change in root
Average 7.53 18.89 15.04
length, a percentage change in dentin

JOE  Volume -, Number -, - 2019 Modified Apexification Procedure Case Series 3

FIGURE 2 – (A ) A preoperative periapical radiograph of teeth #8 and #9. Both teeth had a complicated crown fracture. Tooth #8 has a large pulp cavity, an open apex, and a periapical
lesion. The tooth has an almost closed apex and no periapical lesion. Clinically, tooth #9 was diagnosed with pulp necrosis and symptomatic apical periodontitis and tooth #9 with pulp
necrosis without symptoms. (B ) A postoperative periapical radiograph after the modified apexification procedure of tooth #8. (C ) A periapical radiograph of the 4-year follow-up of tooth
#8. Resolution of the periapical lesion, diffuse intracanal mineralization of the apical root canal, and apical closure are evident. Tooth #9 was treated with root canal therapy because the
apex was closed.

thickness, and a percentage change in root no clinical symptoms/signs and showed 15.04% at the 24- to 72-month follow-up
area, respectively. radiographic evidence of healed periapical period (Table 2).
pathology. Eight cases showed increased
RESULTS thickness of the apical canal walls, increased

Ten cases of immature permanent teeth with

apical root length, and apical closure. Three DISCUSSION
cases showed diffuse intracanal calcification.
necrotic pulp/apical periodontitis treated with Hertwig epithelial sheath (HERS) cells play a
The overall percentage change in root length
modified apexification procedures with a pivotal role in tooth root development20–23.
was 7.52%; in root width at the apical one
minimal follow-up of 2 years are presented in HERS cells provide an inductive signal to stem
third, it was 18.89%; and in RRA, it was
this case series (Table 1). All 10 cases showed cells in the apical papilla to differentiate into

FIGURE 3 – (A ) A preoperative periapical radiograph of tooth #9. The tooth had a complicated crown fracture and has an open apex and a periapical lesion. Clinically, the tooth was
diagnosed with necrotic pulp and asymptomatic apical periodontitis. (B ) A postoperative periapical radiograph after the modified apexification procedure. (C ) A periapical radiograph of
the 2-year follow-up showing resolution of the periapical lesion and apical closure.

4 Songtrakul et al. JOE  Volume -, Number -, - 2019

FIGURE 4 – (A ) A preoperative periapical radiograph of tooth #31. The crown has a large temporary filling. The distal root has an open apex. Clinically, tooth #31 was diagnosed with
irreversible pulpitis with symptomatic apical periodontitis. (B ) A postoperative periapical radiograph. The distal root was treated with the modified apexification procedure, and the
mesial root was treated with root canal therapy because it did not have an open apex. (C ) A periapical radiograph of the 4-year follow-up of tooth #31. Resolution of periapical pathosis,
thickening of the apical canal walls, and apical closure are evident.
odontoblast and produce root dentin24. HERS
cells can also signal stem cells in the dental
follicle to differentiate into cementoblasts and
produce cementum through epithelial-
mesenchymal interaction23. In addition, HERS
cells are capable of undergoing epithelial-
mesenchymal transition into
cementoblasts21,23. Therefore, HERS cells are
responsible for an increase in thickness of the
canal walls, length of the root, and apical
closure. If the HERS is damaged by persistent
apical periodontitis or physical irritation during
the induction of periapical bleeding, continued
root development could be halted.
In immature permanent teeth with
necrotic pulp/apical periodontitis, the
development of the root is usually arrested.
When infection/inflammation involves the
pulpal-periapical tissue complex,
proinflammatory cytokines, such as interleukin
1 and tumor necrosis factor alpha, released
from immunoinflammatory cells are capable of
inhibiting biological functions of the apical
papilla cells and the HERS cells25,26, thus
resulting in the arrest of physiological root
development. Therefore, to rescue arrested
root development of immature permanent
teeth with necrotic pulp/apical periodontitis,
infection/inflammation of the pulp-periapical
tissue complex must be controlled so that the
apical papilla cells and the HERS cells can
resume their biological function. Regenerative
endodontic procedures of immature
permanent teeth with necrotic pulp/apical
periodontitis have shown if infection/
inflammation of the pulpal-periapical tissue
complex is controlled, the arrested root will
have the potential to continue to develop5.
Usually, healing of the arrested root of
immature permanent teeth with necrotic pulp/
apical periodontitis after regenerative
endodontic procedures is by repair and not
regeneration7. A similar biological event should
JOE  Volume -, Number -, - 2019
also occur to the arrested root in the modified
apexification procedure of immature
permanent teeth with pulp necrosis/apical
periodontitis. In the present case series,
continued apical root development (thickening
of the apical canal walls, increased root length,
and apical closure) appeared to occur
frequently with the modified apexification
procedure, probably because the potential of
revascularization/revitalization is related to the
length of the root and the size of the apical
foramen9,10 and the preservation of the HERS
cells.
Wound healing is a continuum and
sequela of inflammation. It is the host’s
programmed response to injury to eliminate
irritants, and the response begins the moment
the tissue is insulted27,28. Wound healing is to
recapitulate the event of embryonic tissue
morphogenesis29,30 and is a very complex
biological process, which requires spatial and
temporal orchestration of cells, matrix, and
bioactive growth factors, cytokines, and
chemokines. During wound healing of the
injured tissue, the wound will be filled with
granulation tissue, regardless of the size of the
wound as a part of programmed wound
healing processes27,28. Eventually, the wound
will heal with tissue similar to or different from
the original tissue (regeneration or repair). In
the modified apexification procedure, the
apical canal space can be easily filled with
granulation tissue from inflamed periapical
tissues even without induction of periapical
bleeding into the apical canal space if the
apical foramen is large enough. The progenitor
cells from apical bone marrow, the periodontal
ligament, and apical papilla can migrate and
proliferate into the apical root canal space;
differentiate into cementoblasts, osteoblasts,
or odontoblasts; and produce cementumlike,
bonelike, or dentinlike tissue, similar to the
tissues formed in the canals after regenerative
Modified Apexification Procedure Case Series
endodontic procedures of immature
permanent teeth with necrotic pulp/apical
periodontitis7.
Vigorous induction of periapical
bleeding into the apical canal space as a
scaffold might physically damage the HERS
and prevent root growth31. In the modified
apexification procedure, only the apical 4–5
mm of the canal space is empty after
chemomechanical debridement. Therefore,
induction of periapical bleeding into the apical
canal as a scaffold might not be necessary.
However, chemomechanical debridement
was used in the modified apexification
procedure to help disrupt and disinfect
intracanal bacterial biofilm. Because all 10
cases had complete periapical healing, our
infection control measurement of the infected
root canals using chemomechanical
debridement and calcium hydroxide
intracanal medication was effective.
In the current apexification procedure
(ie, an MTA/Biodentine apical plug of immature
permanent teeth with necrotic pulp/apical
periodontitis), continued root development
might occur but further maturation usually
does not. In a study using a similar quantitative
analysis, Bose et al17reported minimal
changes in root length and root canal width in
immature teeth treated with an MTA plug
apexification procedure. In the present case
series, 8 of 10 cases treated with the modified
apexification procedure of immature
permanent teeth with necrotic pulp/apical
periodontitis showed continued root
development. Two cases did not show
continued root development, probably
because of severe damage to the HERS cells.
The significance of continued root
development in terms of increasing strength of
the immature permanent tooth with necrotic
pulp in the present case series is not known
and warrants further investigation.
5
Nonetheless, the increased root length might
enhance the strength of the tooth because of
the increased crown/root ratio.
The type of hard tissue formed on the
apical canal walls and in the apical canal space
in the modified apexification procedure in the
present case series is not known without
histologic examination. However, increased
thickness of the apical root canal walls and
diffuse mineralization in the apical root canal
space in the present case series are an
indication that mineralized tissue-forming cells
have migrated into the apical canal space to
form mineralized tissue in the modified
apexification procedure. In an animal study, it
was shown histologically that cementumlike
tissue was deposited on the apical canal walls
and bonelike tissue deposited in the apical
canal space of the 1–3 mm unfilled apical canal
if the apical foramina were enlarged to size 40
to 80 K-files without inducing bleeding into the
apical canal space32. These tissues are similar
to the tissues observed in the canal spaces of
human immature permanent teeth with
necrotic pulp/apical periodontitis after a
regenerative endodontic procedure33–35. The
apical closure in the present case series of
immature permanent teeth with necrotic pulp
treated with the modified apexification
procedure is likely because of the survival of
HERS cells, which can be resistant to
inflammatory processes36.
In immature permanent teeth with
necrotic pulp/apical periodontitis in which the
loss of a substantial coronal tooth structure
may require an intraradicular post/core for
proper coronal restoration, the modified
apexification procedure will be more suitable
than regeneration endodontic procedures to
retain the teeth because regenerative
endodontic procedures do not allow for an
intraradicular post or placing a core of
composite resin into the cervical third of the
root space. Apexification using MTA/
Biodentine as an apical barrier placed close to
the open apex usually does not promote
continued root development, probably
because of the high pH (12.5) of MTA/
Biodentine, which might directly damage
HERS and apical papilla cells. This
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speculation needs further verification because
in vitro studies have shown that calcium
hydroxide, which also has a pH of 12.5, was
conducive with stem cells of apical papilla
survival and proliferation at all concentrations
in culture37 and in human dentin disks38.
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The major drawback of the present case
series of the modified apexification procedure
was that the department of endodontics did
not have control when a post/core had to be
placed on these immature permanent teeth
after treatment. This issue could also happen in
private practice. The endodontists have no
control when a post/core has to be placed for
immature teeth if needed because pediatric
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However, continued apical root (apical 4–5
mm) development was evident after the
modified apexification procedure in the present
case series even though a post/core was not
placed.
CONCLUSION
The modified apexification procedure is easier
than traditional apexification procedures to
perform because an MTA/Biodentine apical
plug does not have to be placed close to the
open apex. In addition, the modified
apexification procedure has the potential to
promote continued apical root development,
thus increasing the crown/root ratio. This is the
advantage of the modified apexification
procedure over calcium hydroxide
apexification and an MTA/Biodentine apical
plug of immature permanent teeth with
necrotic pulp. Therefore, immature permanent
teeth with necrotic pulp at stage 3 or 4 root
development requiring an intracanal post/core
for final restoration because of loss of a
substantial coronal tooth structure can be
treated with the modified apexification
procedure. However, more prospective
controlled clinical trials are needed to verify the
use of the modified apexification procedure for
immature permanent teeth with necrotic pulp/
apical periodontitis to promote apical root
development.
ACKNOWLEDGMENTS
The authors deny any conflicts of interest
related to this study.
JOE  Volume -, Number -, - 2019
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