Australian Dental Journal

The official journal of the Australian Dental Association

Australian Dental Journal 2016; 61:(1 Suppl): 95–106

doi: 10.1111/adj.12401

Management of incompletely developed teeth requiring

root canal treatment
SC Harlamb*
*Specialist Endodontist, Private Practice, Burwood, New South Wales, Australia.

ABSTRACT
Endodontic management of the permanent immature tooth continues to be a challenge for both clinicians and research-
ers. Clinical concerns are primarily related to achieving adequate levels of disinfection as ‘aggressive’ instrumentation is
contraindicated and hence there exists a much greater reliance on endodontic irrigants and medicaments. The open apex
has also presented obturation difficulties, notably in controlling length. Long-term apexification procedures with calcium
hydroxide have proven to be successful in retaining many of these immature infected teeth but due to their thin dentinal
walls and perceived problems associated with long-term placement of calcium hydroxide, they have been found to be
prone to cervical fracture and subsequent tooth loss. In recent years there has developed an increasing interest in the
possibility of ‘regenerating’ pulp tissue in an infected immature tooth. It is apparent that although the philosophy and
hope of ‘regeneration’ is commendable, recent histologic studies appear to suggest that the calcified material deposited
on the canal wall is bone/cementum rather than dentine, hence the absence of pulp tissue with or without an odontoblast
layer.
Keywords: Apexification, immature teeth, regenerative endodontic procedure, root canal, trauma.
Abbreviations and acronyms: CEJ = cemento-enamel junction; CMCP = camphorated para-chlorphenol; HERS = Hertwig’s Epithelial
Root Sheath; IADT = International Association of Dental Traumatology; MTA = mineral trioxide aggregate; PDL = periodontal liga-
ment; PLP = plasma-rich plasma; REP = regenerative endodontic procedures; SCAP = stem cells from the apical papilla; TAP = triple
antibiotic paste.

niques, follow-up and outcomes. Rafter’s review in

INTRODUCTION
The incompletely developed permanent tooth, follow-
ing a traumatic injury, provides the clinician with
diagnostic and clinical challenges. Endodontic treat-
ment, if indicated, poses instrumentation and obtura-
tion issues due to the wide canal and thin dentinal
walls, and as such the decision to commit the tooth to
endodontic treatment should be based on definitive
findings and sound biological principles. Studies have
shown that the endodontically treated immature tooth
is more prone to fracture1 than its fully developed
root filled counterpart, and as such there is presently
an abundance of researchers exploring the notion of
continued root development of the immature tooth
with a necrotic and infected pulp.
Until recently, when asked to present a review on
the endodontic management of the immature tooth,
the author would discuss and describe techniques such
as conservative pulp therapy (apexogenesis) or apexifi-
cation. There would be an outline of indications, tech-
2005 was an excellent example and even included the
then exciting, relatively new material known as mineral
trioxide aggregate (MTA).2 In 2015, however, prepar-
ing such a paper is not so straightforward. Despite
Nygaard-Østby’s3 work in the 1960s, which showed
the possibility of the growth of connective tissue into
the pulp space following formation of a blood clot, the
concept of ‘pulp regeneration’ remained relatively quiet
(and ignored) until the turn of the century. Since then,
there have been an abundance of case series and reports
with at least 35 papers4 dealing with pulp ‘regeneration’
published between 2007 and 2013, reflecting a mounting
interest in the possibility of continued root development
in the infected immature tooth.
This review will explore the impact of trauma on
the immature tooth, as well as endodontic treatment
options such as pulpotomy and apexification and the
roles of calcium hydroxide and MTA. ‘Regenerative’
procedures will also be discussed and the current
treatment protocol outlined.

© 2016 Australian Dental Association 95

SC Harlamb
Although an immature tooth may require endodon-
tic intervention due to caries or congenital anomalies
such as dens invaginatus, it is important to note this
review will deal with the endodontic management of
the trauma-afflicted immature permanent tooth.
Trauma and the incompletely developed tooth
Studies have revealed that 30% of children are
affected by a traumatic dental injury, with the major-
ity occurring before complete formation of the root.5
Prior to commencement of endodontic treatment,
careful assessment, both clinical and radiographic, is
essential. The clinician should be mindful that, if pos-
sible, every attempt should be made to preserve pulp
integrity in the incompletely developed mature tooth.
As such, the type of trauma the permanent imma-
ture tooth has been subjected to plays an essential role
in formulating a treatment plan. Avulsion injuries,
fractures and luxation injuries all have vastly differing
impacts on both the pulp and periodontal ligament
(PDL), and subsequently need to be individually
considered.
Avulsion injuries and the immature tooth
The majority of avulsion injuries occur between the
ages of 8 to 12 years.6 Following an avulsion injury,
severe damage is inflicted upon both the pulp and
periodontal attachment. As a result of the tooth being
separated from its socket, viable PDL cells are present
on both the root surface as well as the socket wall.
Therefore, the timing of replantation of the avulsed
tooth is critical. The avulsed immature permanent
tooth has the added complications of its shortened
root and thin walls, and the impact these will have on
its long-term prognosis. The time that an avulsed
tooth is out of its socket7 is critical and therefore
should be considered as follows:
Extraoral dry time MORE than 60 minutes
Following an avulsion injury, a tooth with a dry time
in excess of 1 hour will have virtually no viable PDL
cells on its root surface.8 It has been concluded that
the ‘60-minute mark’ of dry time is the critical point
at which PDL cell damage occurred. At 2 hours, there
were no viable cells present on the root surfaces.8
As a result, the management of the avulsed immature
tooth with a dry time in excess of 1 hour is complex –
to replant or not? Some argue that the prognosis for
such teeth is so poor that replantation will lead to
probable replacement resorption and ankylosis with all
the well-known complications (difficulties with extrac-
tion, impact on marginal bone, etc.)6 ensuing.
Conversely, others argue that replantation will
allow for maintenance of both the alveolar height and
96
width, hence ensuring easier implant placement once
the child has fully developed.9 Malmgren and co-
workers10 in 1984 introduced decoronation as a
treatment alternative to extraction of the ankylosed
tooth – they argued that removal of the ankylosed
tooth would lead to severe bone loss, thereby com-
promising implant placement. The technique
involved removal of the crown at the cemento-
enamel junction (CEJ), encouraging bone deposition
over the resorbing root. The authors argued that
such a technique ‘supports the indication for replan-
tation of avulsed teeth in children even when the
extra-alveolar conditions indicate that healing might
be compromised by ankylosis’.6,11
The recently revised International Association of
Dental Traumatology Dental Trauma Guidelines11
confirm the prognosis for such teeth is poor with
resorption and ankylosis to be expected. However,
replantation is recommended (delayed replantation)
‘for aesthetic, functional and psychological reasons
and to maintain alveolar contour’.11
Extraoral dry time LESS than 60 minutes
If stored ideally (physiological storage media such as
milk, saline, saliva or HBSS) or extraoral dry time of
less than 60 minutes, it is generally accepted that pulp
revascularization and continued root development is
possible. Andreasen et al., in their seminal 1995 series
of papers12 examined the pulp and periodontal
responses of 400 replanted incisors – which included
28 teeth with incompletely developed roots. In 34%
of the immature teeth, following replantation, sponta-
neous revascularization occurred, a finding consistent
with a study13 10 years earlier. The authors hypothe-
sized that Hertwig’s Epithelial Root Sheath (HERS)
‘can tolerate the trauma of avulsion and replantation
plus damage due to extra-alveolar storage’.12,14
Therefore, as opposed to the replanted fully
matured tooth, endodontic treatment for the imma-
ture replanted tooth should be initially avoided – any
opportunity for continued root growth in these cases
will be lost if endodontic treatment is initiated.14
Follow-up and review is critical – it is recommended
that the patient be reviewed at 4 weeks, 3 months, 6
months, 1 year and yearly15 thereafter for pulp sensi-
bility testing and clinical and radiographic examina-
tion. Carbon dioxide (CO2) has been found to be
extremely reliable in assessing pulp status, even in
immature teeth.16 The clinician should be aware of
any radiographic changes such as apical ‘breakdown’
or root resorption, as well as clinical findings such as
tenderness to percussion and palpation. However, the
decision to commence endodontic treatment must be
based on a ‘holistic’ approach, ensuring all the clinical
and radiographic findings have been considered and
accurately interpreted.
© 2016 Australian Dental Association

Luxation injuries and the immature tooth
Luxation injuries are the most prevalent of all trau-
matic dental injuries, comprising 15–61%.17 Five
types of luxation injuries have been identified: concus-
sion, subluxation, extrusive luxation, lateral luxation
and intrusive luxation. In teeth with closed apices,
studies have consistently confirmed that the more sev-
ere the luxation injury, the greater the prevalence of
pulp necrosis. For example, 3% of teeth with a con-
cussion type injury exhibited pulp necrosis while 85%
of intrusively luxated teeth had necrotic pulps.18
Immature teeth are less likely to develop pulp
necrosis following a luxation injury – according to
Andreasen and Vestergaard Pedersen,18 only 8% of
immature luxated teeth exhibited pulp necrosis over a
10-year period, as opposed to 38% of luxated teeth
with closed apices while root development was the
only significant factor in predicting healing following
a luxation injury.18 It was also found that the wider
the diameter of the apical foramen, the higher the
probability of pulp survival.19 Researchers have sur-
mised that the greater the width of the apical fora-
men, the easier it is for revascularization to occur.19
Additionally, the type of luxation injury an immature
tooth is subjected to does not have the same impact
on pulp necrosis developing when compared to the
closed apex tooth.
Therefore, it is imperative to carry out all appropri-
ate testing prior to commencement of endodontic
treatment for the luxated immature tooth. The clini-
cian should be mindful that colour change, a negative
response to pulp sensibility testing and indeed a radio-
graphic apical radiolucency can all be followed by
pulp repair, especially given the immature tooth’s
propensity for pulp revascularization. Andreasen20 has
concluded that tenderness to percussion is the only
clinical sign which can be consistently relied upon as
an indicator of pulp necrosis and infection.
Management of the intrusively luxated immature tooth
Intrusive luxation, the displacement of a tooth (along
its long axis) into the alveolar socket, is considered
the most severe of all the luxation injuries.21 An asso-
ciated fracture of the alveolar socket is also commonly
seen. Studies have shown that the survival of intru-
sively luxated teeth (whether fully developed or not)
range from 69% to 95%.21 Irrespective of root devel-
opment, 30% of all intruded teeth are lost after 15
years.22
Following intrusive luxation, the stage of root
development plays a major role in determining the
potential outcome of pulp necrosis, root resorption
and loss of marginal bone. Complications have been
found to be significantly less in the immature tooth
following intrusive luxation – researchers have
© 2016 Australian Dental Association
Management of incompletely developed teeth
hypothesized a reason for the more favourable out-
come is the ‘softer’ bone, thereby ensuring the impact
of the intrusion on the PDL to be significantly less in
the growing patient.22
The challenge associated with intrusive luxation has
for many years been its clinical management. Three
options are available to the clinician in the manage-
ment of the intruded tooth: (1) await spontaneous
re-eruption; (2) immediate surgical reduction and
fixation; or (3) orthodontic repositioning.23
Until recently,24 the management of intrusive luxa-
tion injuries received very little attention in the litera-
ture,23 primarily due to it being a rare dental injury
(0.5% to 1%).25 However, Andreasen et al. in 200626
have provided specific guidelines as to management of
the intrusively luxated tooth – the stage of root for-
mation and the age of the patient greatly assist the
clinician in the decision-making process. The authors
concluded that allowing the permanent immature
tooth to spontaneously re-erupt is the treatment of
choice, so long as the tooth is not completely embed-
ded. If no crown is visible, then the incisal edge
should be surgically exposed and the crown loosened
slightly with forceps to facilitate re-eruption, which
can take up to 6 months (the authors reported a range
of 2 to 14 months).24
Figures 1 to 3 illustrate an example of spontaneous
re-eruption of an intrusively luxated open apex tooth
21 in a 10-year-old patient. The patient was monitored
for 7 months with continued evidence of re-eruption.
Endodontic treatment was eventually deemed necessary
for the intrusively luxated tooth 21 because the root
canal system had become infected, and this was com-
menced following complete eruption of the tooth.23
If the clinician decides to allow for re-eruption, a
follow-up and review plan must be formulated with
the patient and parent/carer. The author recommends
review at 2, 4, 8 and 12 weeks initially. At each
appointment, mobility and percussion testing should
be carried out as well as pulp sensibility tests, prefer-
ably with CO2.23 Guidelines currently advise radio-
graphs to be taken at 2–3 weeks, 6–8 weeks, 1 year
and 5, 10 and 15 years.11
During the observation period it is imperative to
note any signs of pulp necrosis and infection, and
inflammatory root resorption – endodontic treatment
will then need to be commenced as soon as practical
but as per other luxation injuries and the immature
tooth, endodontic treatment should only be initiated
if absolutely indicated.
A common concern for the clinician is if the
intruded tooth is not showing any signs of re-eruption
or the possibility of ankylosis. It is recommended that
if there is no indication of re-eruption after one
month then the crown should be loosened with for-
ceps and the tooth orthodontically repositioned.21
97
SC Harlamb
Fig. 1 Intrusive luxation of immature tooth 21 of approximately
2–3 mm with crown clinically visible. (Reproduced from Harlamb SC,
Messer HH. Endodontic management of a rare combination (intrusion
and avulsion) of dental trauma. Dent Traumatol 1997;1:42-46, courtesy
John Wiley and Sons.)
Fig. 2 Seven months post-trauma with clinically acceptable re-eruption
of tooth 21. Note the apical radiolucency and tooth was non-responsive
to CO2 testing. (Reproduced from Harlamb SC, Messer HH. Endodontic
management of a rare combination (intrusion and avulsion) of dental
trauma. Dent Traumatol 1997;1:42-46, courtesy John Wiley and Sons.)
In conclusion, current guidelines stipulate that if a
tooth with incomplete root formation is intrusively
luxated then the clinician should expect a favourable
response with spontaneous re-eruption. Although the
98
Fig. 3 Fourteen months post-trauma with associated periapical healing
of tooth 21. (Reproduced from Harlamb SC, Messer HH. Endodontic
management of a rare combination (intrusion and avulsion) of dental
trauma. Dent Traumatol 1997;1:42-46, courtesy John Wiley and Sons.)
widened canal and open apex should allow for pulp
healing, the clinician should be mindful that endodon-
tic treatment is commonly indicated for the intrusively
luxated tooth.
The crown fractured immature tooth
The management of a pulp exposure of an immature
tooth following crown fracture (complicated crown
fracture) has long been recommended to be conserva-
tive in nature. Cvek27 has stated that ‘the exposed
vital pulp should be maintained in young teeth with
incomplete root formation’ and that premature
removal of the pulp deprives the tooth of adequate
root development.
In a clinical study where patients aged 7 to 16 were
examined over 12 hours following a complicated
crown fracture, the primary pulp response observed
was hyperplastic in nature28 whereas following a
mechanically induced pulp exposure, researchers
found no evidence of necrosis, other than a superficial
inflammatory response of no more than 2 mm.29
These findings served as the basis for the development
of the Cvek partial pulpotomy, a technique designed
to maintain the integrity of the pulp by surgically
removing the coronal portion of the pulp, thereby
ensuring continued root development in the immature
tooth.
Calcium hydroxide was the material of choice pro-
posed by Cvek – he recommended cutting a cavity
© 2016 Australian Dental Association

approximately 2 mm below the site of the pulp expo-
sure, establishing haemostasis and then covering the
wound with calcium hydroxide to promote hard tissue
formation. MTA has recently been proposed as an
alternative material to calcium hydroxide in partial
pulpotomy cases, the main advantages being that
complete haemostasis need not be achieved as MTA
requires fluid to be present to set and that once set,
MTA acts as a barrier against bacteria penetration.30
Both calcium hydroxide and MTA will be discussed
in detail below.
Apexification
The American Association of Endodontists defines
apexification as ‘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 pulps’.31 Endodontic management of an
immature tooth is justifiably described as challenging
for three fundamental reasons:7
(1) The open apex creates a difficult environment for
controlling the root canal filling material to be
used.
(2) Due to the width of the canal and the thin root
dentine walls, it can be extremely difficult to ade-
quately ‘clean’ the canal, as an aggressive instru-
mentation approach is contraindicated.
(3) The remaining canal walls are inevitably quite
thin and therefore there exists a high degree of
possibility of root fracture.
Two types of apexification procedures have been
described: calcium hydroxide (multiple visit) apexifica-
tion and MTA apical barrier (single visit)
apexification.
Calcium hydroxide (multiple visit) apexification
Calcium hydroxide has played an integral role in den-
tistry since first described by Hermann32 in 1930 as a
pulp capping agent. Since then numerous studies have
been carried out confirming its bactericidal efficacy
and in turn its ability to promote healing and the for-
mation of a hard tissue barrier. These effects are
directly related to calcium hydroxide’s alkaline pH of
12.5, which enables it to cause localized tissue necro-
sis, allowing inflammatory cells to migrate to the area,
thereby pre-empting wound healing. It has also been
found that 99.9% of common bacterial flora within
an infected root canal system are killed when they
come into contact with calcium hydroxide.33 Calcium
hydroxide also has the ability to dissolve necrotic pulp
tissue,34 which therefore allows the clinician to mini-
mize filing (see below).
Calcium hydroxide’s ability to promote a hard tis-
sue barrier (i.e. whether it has osteogenic properties)
© 2016 Australian Dental Association
Management of incompletely developed teeth
remains uncertain. However, it is generally accepted
that the apical placement of calcium hydroxide within
the root canal of a tooth with an open apex elicits a
response similar to when it comes into contact with
coronal pulp tissue. Rather than dentine being formed
however, ‘reparative or cementum-like’ hard tissue
has been identified.35
Frank first described the calcium hydroxide apexifi-
cation technique36 in 1966 following Kaiser’s37 pre-
sentation 2 years earlier which combined calcium
hydroxide with camphorated para-chlorphenol
(CMCP). Frank advocated the placement of calcium
hydroxide with CMCP, with the calcium hydroxide to
be replaced every 3 months until an apical barrier
was formed which could take up to 24 months.
The calcium hydroxide apexification technique is
simple. Once working length is established radio-
graphically, light filing is advocated with copious irri-
gation using 0.5% sodium hypochlorite (NaOCl)33 to
facilitate the removal of necrotic pulp tissue. Sterile
paper points must be used to dry the canal followed
by placement of calcium hydroxide, which can be
mixed with saline, sterile or distilled water.2 Pulp-
dentâ – calcium hydroxide mixed with methylcellu-
lose – has been proposed by Heithersay38 and
Feiglin.39 An adequate interappointment temporary
restoration is a critical, yet often overlooked, step in
the apexification procedure, as it is essential the
medicament remains within the canal without any
possibility of bacterial ingress.41
Abbott41 has recommended replacement of the cal-
cium hydroxide every 2 to 3 months, usually over 5
to 6 appointments. A single application of calcium
hydroxide may lead to the medicament ‘washing out’,
hence the possibility of delayed healing (Fig. 4).41 The
apical barrier, Abbott also argues, can only be accu-
rately assessed clinically – ‘tapping’ a sterile paper
point apically provides the clinician with an idea of
the integrity of the barrier. If blood or exudate are
detected, then the calcium hydroxide needs to be
replenished and further assessment indicated. Radio-
graphs alone are not an accurate indicator of barrier
formation.41
Chawla42 has suggested that calcium hydroxide
needs to be placed only once as the author states there
is no benefit in multiple applications of the medica-
ment. However, this approach generally leads to
much longer treatment times and it is not possible to
ascertain when the root filling can be done.
Once the clinician is satisfied with apical barrier
integrity, calcium hydroxide should be placed one
final time and left in situ for a further 3 months – the
canal can then be obturated, usually with a heat soft-
ened gutta-percha technique.
As apexification with calcium hydroxide is the most
established of all the techniques, its long-term success
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SC Harlamb
Fig. 4 Calcium hydroxide ‘washed out’ in the apical half of the canal of
tooth 11 after 3 months – it has therefore been recommended calcium
hydroxide be replaced at 3 monthly intervals in apexification cases.
(Reproduced from Abbott PV. Apexification with calcium hydroxide –
when should the dressing be changed? Aust Endod J 1998;24:27-32,
courtesy John Wiley and Sons.)
rates are well documented. Ballesio et al.43 reported
success rates of up to 90% with a follow-up of 7 to
13 years, while Heithersay38 and Cvek44 reported suc-
cess rates above 95%. Cvek observed no difference in
periapical healing between calcium hydroxide treated
mature and immature teeth after 4 years.1
Equally, disadvantages have been identified with the
calcium hydroxide apexification method. Multiple
appointments for replenishment of calcium hydroxide
do pose problems for the clinician. Managing a child
over numerous appointments can be challenging while
the literature is replete with evidence that children
may be traumatized in an ever-increasing manner
when subjected to multiple appointments.45
Apexification does not promote continued root
development while calcium hydroxide has been shown
to cause dentine brittleness via its proteolytic and
hygroscopic properties.46 Andreasen et al.47 reported
that long-term calcium hydroxide dressings could
increase the risk of root fracture, hypothesizing that
the high pH produced by the hydroxyl ions have a
detrimental effect on the organic support (denatura-
tion and dissolution of protein) of dentine. Cvek
reported a high incidence of fracture (specifically at
the cervical portion of the root) in the immature tooth
following long-term calcium hydroxide applications.
In teeth with very early root development, a fracture
rate of 77% in 26 teeth was observed which fell to
2% in 362 mature teeth.1
100
Therefore, although some disadvantages do exist
with the multiple visit calcium hydroxide apexification
technique, the clinician should bear in mind it is, to
date, a technique which has been scrutinized and
assessed for many years. It is a reliable and simple
technique to carry out and therefore should not be
readily dismissed as newer materials or techniques are
proposed – the clinician should continue to consider
and offer it as a treatment option.
MTA apical barrier (single visit) apexification
MTA was initially proposed as an ‘apical plug’ in
apexification cases in 1999.48 The authors at the time
suggested that following 1 week with calcium hydrox-
ide dressing, 3–4 mm of MTA be placed apically with
pluggers and paper points. Over the ensuing years the
technique has evolved into a single visit treatment. As
will be shown, subsequent studies have shown very
little difference in success rates between the single visit
and multiple visit techniques.
MTA is composed of calcium silicate, bismuth
oxide, calcium carbonate, calcium aluminate and cal-
cium sulfate, and when mixed with water or saline is
made up of 33% calcium, 49% phosphate, 2% car-
bon, 3% chloride and 6% silica.49 MTA takes up to
3 hours to set, has excellent sealing properties, is bio-
compatible and has the ability to set in a moist envi-
ronment.50 Additionally, when set MTA comes into
contact with fluid, calcium hydroxide is released.
Friedland and Rosado51 deduced that this was the
reason that MTA formed a hard tissue barrier similar
to calcium hydroxide. As a result, MTA has been pro-
posed as an excellent material in apexification cases.
The MTA apexification technique is more challeng-
ing than the calcium hydroxide technique previously
described. Following light filing and copious irrigation
with 0.5% sodium hypochlorite and 17% EDTA, the
canal is dried with sterile paper points.
The MTA, once mixed to the correct consistency,
can be dispensed on an MTA ‘block’ (Fig. 4) and the
material placed into the middle to apical third of the
canal with a Half Hollenbach instrument (Fig. 5). The
MTA can then be compacted to the correct working
length with large paper points or loose fitting pluggers
(pre-measured). It is advisable to place a moist cotton
pellet against the MTA which should be left in situ
for at least 6 hours.7 Advocates of the MTA single
visit technique place a bonded composite resin mate-
rial directly over the MTA, filling both the canal and
access opening.50 However, such an extensive restora-
tion would likely render the tooth impossible to
retreat.
There is no doubt that MTA offers many advan-
tages when utilized in apexification procedures. How-
ever, it does have poor handling characteristics, being
© 2016 Australian Dental Association

Fig. 5 MTA is placed into the ‘slots’ of the MTA block.
Fig. 6 MTA is placed on a Half Hollenbach to allow for ease of place-
ment into the canal.
heavily reliant on correct mixing techniques and its
long setting time is a concern in the single visit tech-
nique as the clinician is unable to observe whether the
material has set. Control of placement of MTA is dif-
ficult while both grey and white MTA have been
found to discolour teeth. Another limitation with
MTA is the difficulty the clinician is faced with if it
needs to be removed.
Witherspoon et al.,50 in a retrospective study, anal-
ysed the success rates of 144 immature teeth which
were treated with an MTA apical plug over one
(92/144) or two visits (52/144). The group in the two-
visit category had calcium hydroxide placed for 3
weeks prior to the MTA plug being placed. Both
groups achieved high success rates of over 90% fol-
lowing recall of at least 12 months However, with
only 39.7% of the two-visit group being recalled as
opposed to 60.3% of the single visit group, it is diffi-
cult to conclude much more than both techniques
worked well in the short-term period.
As can be seen, apexification procedures over the
years have been successful in retaining the trauma-
tized immature tooth. However, regardless of the
technique or material employed the remaining tooth
© 2016 Australian Dental Association
Management of incompletely developed teeth
structure and thin dentinal walls continue to be a clin-
ical concern. Ongoing research appears to indicate
that resin-bonded restorations within the canal and
beyond the CEJ do act to reinforce these fracture
prone teeth.52
Regenerative endodontic procedures and the
incompletely developed tooth – where are we?
The disadvantages associated with apexification dis-
cussed above have led, over the past 10 to 15 years,
to increasing interest in the possibility of regenerating
pulp tissue in the immature tooth with an infected
necrotic pulp, thereby allowing for continued root
development. This ‘new frontier’ of regenerative
endodontics has been met with either extreme enthusi-
asm4,53 or scepticism.54,55 There also appears to be a
distinct lack of consensus regarding a ‘title’. At last
count, the author has identified at least 7 descriptors:
pulp regeneration;53 pulp revascularization;56 maturo-
genesis;57 pulp revitalization;58 pulp replacement;59
pulp repair;60 or most recently regenerative endodontic
procedures (REPs).4 A factor in this lack of consensus is
that there is little agreement as to what is actually being
regenerated and the impact that this ‘tissue’ has (and
will have) on the remaining tooth structure.54
Nygaard-Østby3 in 1961 found that following the
creation of a blood clot in an infected root canal, tis-
sue ingrowth was established. It was, however, not
pulp in origin, rather it was consistent with fibrous
connective tissue and cementum. As previously stated,
the concept of ‘pulp regeneration’ remained relatively
quiet until recently, followed by ongoing hysteria
amongst researchers – multiple papers (152 case
reports and case series)4 dealing with pulp ‘regenera-
tion’ have been published, with claims that with pulp
regeneration, a paradigm shift in the management of
the infected immature tooth has been created.53
REPs are defined as ‘biologically based procedures
designed to replace damaged structures, including
dentine and root structures, as well as cells of the
pulp-dentine complex’.4 Mesenchymal stem cells were
identified within the apical papilla of immature
teeth61 and have subsequently been coined ‘stem cells
from the apical papilla’ (SCAP), which in turn have
been found to differentiate into odontoblast-like cells
(in vitro).61 Therefore, the hypothesis of the REP is
that undifferentiated cells within the apical papilla of
an immature tooth can be stimulated to assist in the
further development of the root and that for the pro-
cedure to succeed, all bacteria must have been elimi-
nated, a scaffold is established apically to allow for
ingrowth of new tissue and that a barrier and restora-
tion ensures no bacterial recontamination.62
Being an immature tooth, it was recommended that
virtually no mechanical instrumentation be carried
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SC Harlamb
out and as such research was conducted to identify a
new ‘disinfection medicament’ which could effectively
disinfect the canal and have no deleterious effect on
the root dentine or any undifferentiated cells in the
apical region. Hoshino et al.63 found the combination
of ciprofloxacin 200 mg, metronidazole 500 mg and
minocycline 100 mg to be effective in eliminating bac-
teria from infected dentine – the combination has
become known as ‘triple antibiotic paste’ (TAP).
For cells and vasculature to proliferate in any regen-
erative procedure, a ‘scaffold’ is required – in the
immature tooth researchers have found that the cre-
ation of a blood clot serves as a scaffold which then
allows for stimulation of cell growth as well as possi-
ble odontoblast-like cells forming.64 As it is impera-
tive that the clot/scaffold remain free of bacterial
contamination, a barrier needs to be placed and MTA
has been found to be the most reliable material for
this.
As previously mentioned, interest was renewed with
REPs following two case reports published in 200165
and 2004,66 the former providing the basis for the
recommended protocol of REPs. Below is a summary
of the most recently revised clinical recommendations
for REP proposed by the American Association of
Endodontists:67
First appointment
(1) Local anaesthesia, dental dam isolation and
access.
(2) Copious, gentle irrigation with 20 ml 1.5%
NaOCl using an irrigation system that minimizes
the possibility of extrusion of irrigants into the
periapical space.
(3) Dry canals with paper points.
(4) Place calcium hydroxide or low concentration of
triple antibiotic paste. If the triple antibiotic
paste is used: (a) consider placing a dentine
bonding agent in the pulp chamber [to minimize
risk of staining]; and (b) mix 1:1:1 ciprofloxacin:
metronidazole:minocycline to a final concentra-
tion of 0.1 mg/ml.
(5) If triple antibiotic paste is used, ensure that it
remains below the CEJ.
(6) Place 3–4 mm of a temporary restorative mate-
rial such as Cavit, IRM, GIC or another tempo-
rary material. Dismiss patient for 1–4 weeks
Second appointment (1–4 weeks after first visit)
(1) Assess response to initial treatment. If there are
signs/symptoms of persistent infection, consider
additional treatment time with the antimicrobial,
or an alternative antimicrobial, intracanal
dressing.
102
(2) Anaesthesia with 3% mepivacaine without vaso-
constrictor.
(3) Rubber dam isolation.
(4) Copious, gentle irrigation with 20 ml of 17%
EDTA.
(5) Dry with paper points.
(6) Create bleeding into the root canal system by
over-instrumenting (induce by rotating a pre-
curved K-file at 2 mm past the apical foramen
with the goal of having the entire canal filled
with blood to the level of the CEJ).
(7) Stop bleeding at a level that allows for 3–4 mm
of restorative material.
(8) Place white MTA as the capping material. MTA
has been associated with discolouration. Alterna-
tives to MTA (such as resin-modified glass iono-
mer or bioceramics) should be considered in
teeth where there is an aesthetic concern.
(9) A 3–4 mm layer of GIC is flowed gently over the
capping material.
Follow-up
(1) Clinical and radiographic exam:
o No pain, soft tissue swelling or sinus tract
(healing is often observed between the first
and second appointments).
o Resolution of the periapical radiolucency
(often observed 6–12 months after treatment).
o Increased width of the root walls and length
of the root.
o Positive pulp sensibility test response (not
always present).
As can be seen, the REP technique is not a simple
one and a clear understanding of each of the clinical
steps is imperative. The intention of this review is nei-
ther to dismiss nor advocate a particular procedure
and this has been the rationale for providing the cur-
rent67 REP treatment protocol. However, the clinician
should be aware of the pitfalls and disadvantages of a
relatively new technique that lacks high levels of evi-
dence and is largely based on case reports.
Identified problems with REPs
It is important to note that the outcomes of REPs are
to date based on case studies alone. These case studies
‘lack the use of a standardised treatment protocol and
include a broad range of differences in the aetiology
of treated disease, chemo-mechanical debridement reg-
imen, number of visits and intra-canal medicament’.4
Indeed, many of these case studies involve no more
than one or two teeth and the lack of consistency as
to the aetiology (trauma, caries, dens evaginatus, etc.)
makes it extremely difficult to draw any conclusions
about the outcomes, as the impact on HERS in partic-
© 2016 Australian Dental Association

ular varies greatly from one case to another. Case
studies are unreliable in determining success and fail-
ure outcomes68 with the Centre for Evidence Based
Medicine at Oxford University ranking case studies as
the lowest form of evidence-based studies (Level 5).68
Minocycline (a component in the TAP) and MTA
have been identified as possible causes of discoloura-
tion of a tooth following an REP and patients should
be warned of the possibility of this occurring. In a
recent article,69 10 of 16 teeth treated without the
minocycline component in the TAP (substituted with
amoxicillin) were found to have discoloured and the
authors concluded that the use of grey and white
MTA was the cause. Internal bleaching may be
required but this may not be feasible if MTA has been
placed within the pulp chamber due to the difficulties
associated with its removal. It is interesting to note
that as a result of this complication, a technique with-
out the use of the TAP has been suggested.70
In an editorial, Nair55 argued that proponents of
regenerative endodontics have not yet seen the ‘ele-
phant in the room’, namely, that to date there has
been no evidence of an acceptable pulp-odontoblast-
dentine complex in these infected cases, and it is
indeed the presence of infection which is precluding
that outcome, primarily caused by continued chal-
lenges in dealing with residual biofilms in all aspects
of endodontics. He states that research should be
focused on ‘generative’ dentistry and likens it to
demolishing an old decrepit house and rebuilding it
according to its original design, rather than retaining
it by carrying out a ‘soft’ renovation.55
The creation of the blood clot has also been
reported during the second stage to have been met
with difficulty. Kahler et al.,69 despite using an
anaesthetic without a vasoconstrictor, could not ini-
tiate bleeding in some of their cases. They also
reported that even if bleeding was initiated, the
amount of blood required for clot formation was
insubstantial. Another report, where a vasoconstric-
tor was used, failed to cause bleeding in 4 of 12
teeth.71 As a result of this possible complication, the
use of a plasma-rich plasma (PRP) scaffold has been
suggested,72 where blood is drawn from the patient,
red blood cells are removed and thrombin and cal-
cium are added to prepare the PRP. The use of PRP
is designed to replicate the functions of a naturally
occurring blood clot/scaffold as it contains the fol-
lowing properties: (1) stimulates collagen produc-
tion; (2) contains growth factors; (3) promotion of
vascular ingrowth; and (4) induces cell differentia-
tion.72
However, the practicalities of the creation and sub-
sequent placement of a PRP scaffold in a clinical den-
tal setting will likely preclude it from being used in
most practices.
© 2016 Australian Dental Association
Management of incompletely developed teeth
Subsequent to this study, in a pilot study using fer-
rets, histologic examination has been carried out on
the type of tissue formed following blood clot creation
and the use of PRP as a scaffold.59 The authors
found, histologically, in both groups an ‘ingrowth of
bonelike tissue from the apical region extending to
the coronal third of the root’.59 Connective tissue was
also identified in the pulp space in association with
fibroblasts and blood vessels. Interestingly, the authors
concluded that the thickening of the root was essen-
tially due to the presence of bone and cementum
rather than dentine. Therefore, if this is the case, the
claimed advantage of increased resistance to fracture
following a REP comes into question. As previously
mentioned, a long-held cited disadvantage associated
with apexification has been increased susceptibility to
fracture due to cessation of dentine deposition in the
cervical one third of the root. As histological studies
are continuing to show no evidence of dentine deposi-
tion following a REP (especially in the coronal third
of the root), one needs to question if there is any dif-
ference in the long term with respect to fracture resis-
tance in either treatment scenario. Long-term
prospective clinical studies are indicated prior to these
claims continuing to be made.
Authors of a recent histological study73 reported
that following bone ingrowth into the pulp space (a
now known phenomenon following REPs), replace-
ment resorption, as a result of fusion between the
bone and the canal wall, was identified due to the
absence of the protective qualities of the PDL against
resorption. Replacement resorption could therefore be
a long-term outcome of REPs.
Recent case reports74 continue to claim evidence of
an increase in root length and thickness following a
REP. However, the lack of radiographic standardiza-
tion renders the findings impossible to draw any
definitive conclusions other than subjective interpreta-
tion (which is consistently reported positively4).
Indeed, the case cited74 presents three radiographic
images (preoperative, 6 months and 1 year) with three
different angulations. Research is also lacking as to
the true long-term impact of these ‘marginal’ improve-
ments in length and thickness with respect to fracture
resistance and tooth survival.
There is little doubt REPs have captured the imag-
ination of endodontic researchers and continued
investigations into the procedure are to be com-
mended and encouraged. However, the reliance on
case studies alone to determine treatment protocols
is troublesome and has medico-legal and ethical
implications. Additionally, the uncertainty of what is
actually being produced in the pulp space following
these procedures will hopefully be clarified and that
well-designed prospective outcome studies are to be
produced.
103
SC Harlamb
Equally of concern is that as REPs are reliant on
the presence of a scaffold and subsequent cell differen-
tiation in the apical papilla region, the differing
impact of disease process in that region needs further
clarification. For example, one would expect that fol-
lowing an intrusive luxation injury, cells in the apical
region of an immature tooth behave and respond dif-
ferently to those same cells in a tooth affected by a
long-term caries lesion progression or an exposed pulp
due to a genetic malformation such as a dens evagina-
tus where the apical PDL has not been damaged or
affected.
The authors of a recent review75 recommended a
REP only be considered if the other alternatives (apex-
ification and partial pulpotomy) were not possible, i.e.
the procedure should be treated as the ‘option of last
resort’. Given the lack of long-term outcome studies
and as yet incomplete understanding of the biologic
responses following initiation of an REP, there is little
reason to not support their proposition.
SUMMARY
An immature permanent tooth which has been sub-
jected to a traumatic episode requires careful clinical
and radiographic examination prior to committing it
to endodontic treatment. As has been shown, the
immature tooth, in a number of trauma scenarios, has
a good chance of revascularizing without any clinical
intervention. If a necrotic and infected pulp within
such teeth has been definitively diagnosed, then
endodontic treatment can pose clinical challenges.
Although treatment protocols such as apexification
techniques have been in existence for many years, the
reality of dealing with a structurally weakened tooth
persists, with cervical fractures in particular being an
ongoing concern. Caution needs to be exercised when
so-called ‘regenerative procedures’ are to be consid-
ered. Claims that pulp is being ‘regenerated’ are sim-
ply not supported by many recent histologic findings
and, as such, proven therapies such as apexification
should still be considered the first treatment of choice.
DISCLOSURE
The author has no conflicts of interest to declare.
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