Australian Dental Journal

The official journal of the Australian Dental Association

Australian Dental Journal 2010; 55: 446–452
CASE REPORT
doi: 10.1111/j.1834-7819.2010.01268.x

Regenerative endodontics – biologically-based treatment for

immature permanent teeth: a case report and review of the
literature
A Thomson,* B Kahler*
*School of Dentistry, The University of Queensland, Brisbane.

ABSTRACT
Background: A paradigm shift in the treatment of immature, necrotic teeth has occurred with biologically-based principles
and regenerative endodontic protocols replacing traditional ‘apexification’ procedures. Preliminary research suggests that
stem and progenitor cells from the pulp and ⁄ or periodontium contribute to continued root development when regenerative
procedures are followed.
Methods: A mandibular premolar tooth with a chronic periapical abscess was irrigated with sodium hypochlorite with
minimal instrumentation and then dressed with tri-antibiotic paste consisting of ciprofloxacin, metronidazole and
amoxicillin. At a subsequent visit a blood clot was evoked in the canal by irritating periapical tissues and the canal sealed
with mineral trioxide aggregate, glass ionomer cement and composite resin.
Results: Resolution of apical periodontitis and the draining sinus, continued root maturation and apical closure occurred
over an 18-month period. The tooth became responsive to pulp sensibility testing.
Conclusions: It is important that dentists recognize the potential of regenerative endodontics in the treatment of necrotic,
immature teeth. Initial management should involve irrigation with sodium hypochlorite only. Intra-canal medicaments, such
as calcium hydroxide, are contraindicated as they inhibit further root growth. This report uses a variation of the tri-
antibiotic paste currently recommended for regenerative procedures that avoided the discolouration of the crown associated
with current protocols. Regenerative endodontics with continued root growth may reduce the risk of fracture and premature
tooth loss associated with traditional ‘apexification’ procedures where the root remains thin and weak.
Keywords: Regenerative endodontics, revascularization, tri-antibiotic paste.
Abbreviation: MTA = mineral trioxide aggregate.
(Accepted for publication 25 January 2010.)

procedures and revasularization of the root canal in

INTRODUCTION
Revascularization of a necrotic pulp following a
traumatic incident such as avulsion in an immature
tooth with an open apex is well established and a
desirable outcome as it allows further development of
the root.1 In this clinical scenario, the pulp is necrotic
but not infected and can act as a matrix to allow
revascularization of the tooth. Optimal replantation
techniques, prompt replantation to minimize the risk of
infection, and an open apex greater than 1.1 mm
increases the chances of revasularization.2 Recently, a
number of case series and case reports have described
continued root development and even responses to pulp
sensibility testing in treated necrotic immature teeth
with infected root canal systems, including those with
draining sinus tracts.3–9 These regenerative endodontic
446
teeth with infected root canal systems have been termed
‘a paradigm shift’ in the treatment protocol for
endodontic management.7,10
Traditionally, the clinical protocol for immature
teeth with infected root canal systems was termed
‘apexification’ and involved placing calcium hydroxide
as an intra-canal medicament to firstly eliminate the
intra-radicular infection and then induce an apical
barrier over time.11 There was a requirement for
multiple visits and a lengthy time period (average
12 months) before a root filling could be completed.12
More recently, an alternative ‘apexification’ protocol
involved placement of mineral trioxide aggregate
(MTA) which acts as an artificial barrier on which a
hard tissue barrier forms.13 An advantage of this
technique is it is generally completed in one or two
ª 2010 Australian Dental Association
 Pulp regeneration

appointments.14 However, ‘apexification’ techniques

with either placement of calcium hydroxide or MTA
have in general not allowed continued root maturation.
Hence, there is a greater risk of fracture as a conse-
quence of thin dentinal walls and premature loss of the
tooth.15
Regenerative procedures generally advocate the
placement of a tri-antibiotic paste to eliminate the
intra-radicular infection which is regarded as a man-
datory requirement for success.3–9 The tri-antibiotic
paste in these studies consists of a combination of
ciprofoxacilin, metronidazole and minocycline which
has been shown to reliably eliminate bacteria in
infected root dentine whereas the respective drugs used
alone have only substantially reduced but did not
eliminate the bacteria.16 This combination of drugs has
also been shown to be effective at eliminating bacteria
in the deep layers of root canal dentine.17 However, a
disadvantage of this technique is discolouration of the
crown of the tooth presumably due to the minocycline.9
Ledermix (Lederle Pharmaceutical, GMBH Wolfrats-
hausen, Germany), an intra-canal medicament contain-
ing tetracycline, has been shown to cause greater
discolouration in immature teeth than mature teeth.18
Sato et al. studied the antibacterial efficacy of a variety Fig 1. Clinical photograph of teeth in the posterior segment of the left
of antibiotic combinations and found that amoxycillin, mandible. Gingival swelling and pointed abscess is evident adjacent
used as the third antibiotic, was also as effective as the lower second premolar.
minocycline when used in combination with ciproflox-
acin and metronidazole in eliminating bacteria.17 electric pulp sensibility testing, whilst the remaining
However, there are no known reports of regenerative teeth in the lower left arch were all responsive.
protocols using a tri-antibiotic paste which includes Periodontal probing confirmed normal attachment
in its formulation amoxycillin, and whether this levels with no probing depths greater then 3 mm.
combination also results in crown discolouration. The Mobility of the tooth was in the physiologic range. No
inherent risk of sensitization and allergy to penicillin crown discolouration was noted (Fig 1).
would be a contraindication in some patients.19 This Radiographically, the mandibular left second pre-
case report describes an endodontic regenerative pro- molar had an increase in the periodontal ligament
cedure using a combination of ciprofloxacin, metroni- space, incomplete root formation and a diffuse peri-
dazole and amoxycillin for a mandibular left second apical radiolucency 5 mm x 3 mm in size (Fig 2). No
premolar diagnosed with pulpal necrosis, an infected carious lesion was evident. A gutta-percha point was
root canal system and chronic periapical abscess. placed in the sinus tract and illustrated the relationship
between the lesion and the periapical lucency (Fig 3).
A diagnosis of pulpal necrosis, an infected root canal
CASE REPORT
system and chronic periapical abscess was made on the
A 12-year-old Caucasian female patient presented to basis of the clinical and radiographic examination. It
the Kingston School Dental Clinic for evaluation of was considered that the aetiology of the infection was
her mandibular left second premolar. The medical an occlusal tubercle that had fractured, allowing
history was non-contributory. There was no history of bacterial contamination of the pulp. Pulpal regenera-
pain or discomfort with the tooth and her only tion was regarded as the optimal treatment choice
complaint was that of intermittent bad breath, whilst considering the stage of root development, the thin
her mother was concerned about some swelling of the dentinal wall maturation and the wide open apex. A
gingiva adjacent to the mandibular left second pre- comprehensive discussion of the risks, complications
molar. An intra-oral examination revealed the tooth to and alternative treatment options was undertaken and
be intact with no signs of caries without any history of parental consent obtained.
trauma. A large draining sinus was present in the buccal Local anaesthesia was administered and the mandib-
gingiva (Fig 1). Sensibility testing of the mandibular left ular left second premolar isolated with rubber dam.
second premolar was non-responsive to both cold and Access preparation was made utilizing an operating
ª 2010 Australian Dental Association 447
A Thomson and B Kahler
Fig 2. Periapical radiograph illustrating a periapical radiolucency
associated with the lower left mandibular second premolar. Thin
dentinal wall at the apex of the root which exhibits a wide open apex is
noted. There is no evidence of caries.
Fig 3. A radiographic image of a gutta-percha point placed in the
draining sinus tract that traces to the periapical radiolucency.
microscope and a single, wide canal was visualized and
drainage of haemorrhagic, purulent exudate was
obtained. Working length was estimated with an apex
locater (Sybron Endo, Orange, CA, USA) and a
periapical radiograh taken with a size 15 K-file (Sybron
448
Endo, Orange, CA, USA) for length confirmation. The
file was placed carefully so as to limit any damage to the
canal walls. The canal was then irrigated with 30 mL
of 1% sodium hypochlorite 2 mm from the working
length prior to drying the canal with paper points. The
tri-antibiotic paste consisted of a powder of 20 mg each
of metronidazole, ciprofloxacin and amoxicillin mixed
with 1 mL of sterile water. The paste was carefully
introduced into the canal with a lentulo spiral root
canal filler attempting to minimize placement in the
coronal portion of the tooth and filled to the level of
just below the cemento-enamel junction. The access
cavity was sealed with 4 mm of Cavit (ESPE, Seefeld,
Germany) and 2 mm of Fuji IX (GC, IL, USA).
The tooth was reviewed three weeks later. The
patient reported some pain three days postoperatively
which required oral analgesics (Ibuprofen), but had
been asymptomatic since that time. Intraorally, the
draining sinus had resolved. However, due to the
episode of pain it was decided to redress the tooth.
Under rubber dam isolation, the canal was irrigated
with 20 mL of sodium hypochlorite, which was ultra-
sonically agitated with a size 10 K-file for one minute
after each 5 ml was administered. The canal was then
dried and redressed with the tri-antibiotic paste com-
bination mentioned earlier utilizing the same placement
technique.
The patient was recalled after a further three weeks
reporting that the tooth had been asymptomatic for
that entire time. A periapical radiograph was taken and
revealed some Cavit had been dislodged apically in
the root canal. Under rubber dam isolation, the canal
was irrigated with 10 mL of sodium hypochlorite
with ultrasonic agitation for one minute every 5 mL
of solution. With the infection and foreign material
controlled, the regenerative process was commenced.
After the canal was dried with paper points, a D11T
NiTi hand spreader (Dentsply Tulsa Dental, TN, USA)
was used to irritate the apical tissue until bleeding
occurred apically in the root canal space so as to create
a biological scaffold for the regenerative process
(Fig 4). Over a 15-minute time period, the blood was
allowed to clot to a level 3 mm below the cemento-
enamel junction. Then 3 mm of ProRoot white MTA
(Dentsply Tulsa Dental, TN, USA) was placed with the
aid of a Lee block (San Francisco, USA) and Buchannan
Pluggers (Sybron Endo, Orange, CA, USA). The access
cavity was sealed with 3 mm of Fuji IX and 2 mm of
acid etched composite resin (Fig 5).
The tooth remained asymptomatic over an 18-month
follow-up period. Clinically, the tooth was responsive
to electric pulp sensibility testing while earlier testing
throughout the follow-up period had been inconclusive.
No tenderness to percussion or palpation could be
discerned. Radiographically, osseous healing of the
periapical lesion was evident as well as root maturation
ª 2010 Australian Dental Association

Fig 4. Clinical picture of the tooth where bleeding has been evoked by
irritating the periapical tissues with a D11T instrument.
Fig 5. Radiographic image following placement of MTA to a level
3 mm below the cemento-enamel junction. The access cavity is filled
with glass ionomer cement and composite resin. The radio-opaque
material at the apical border is Cavit.
(Figs 2, 6, 7 and 8). The appearance of the mandibular
left second premolar showed no obvious change in
shade or colour (Fig 9).
DISCUSSION
The promise and potential of regenerative endodontic
therapies in necrotic teeth was first explored by
ª 2010 Australian Dental Association
Pulp regeneration
Fig 6. Radiographic image taken at the six-month follow-up
appointment. Resolution of the periapical radiolucency and some
closure of the apex are evident.
Nygaard-Østby in 1961 with limited success.20 Histo-
logical analysis demonstrated that a functional pulp-
dentine complex was not routinely induced. Current
and future research into regenerative endodontics is
focused on tissue engineering principles including root
canal revascularization, postnatal stem cell therapy,
pulp implantation, scaffold implantation, injectable
scaffold delivery, three-dimensional cell printing and
gene delivery.21 The challenge for the clinician is to
recognize the potential of these new therapies and
where appropriate incorporate them into everyday
practice.
The current report and others demonstrate that
regenerative endodontics is a viable treatment option
which has been described as a ‘paradigm shift’ that
allows for continued root development, a return of
vitality and health in formerly necrotic immature
teeth.10 Hargreaves et al. outline a number of common
factors that are consistent findings and important
observations in these reports.22 Firstly, the presence of
a wide, open apex is most likely a physical requirement
for tissue ingrowth. Secondly, because of the young age
of the patients there may be a high stem cell regener-
ative potential. Thirdly, care is required not to instru-
ment the canal walls and sodium hypochlorite has
proved to be an effective irrigant. Fourthly, calcium
hydroxide is not recommended as an intra-canal
medicament.22 There is a concern that calcium hydroxide
449
A Thomson and B Kahler
Fig 7. Radiographic image taken at the 18-month follow-up
appointment. Continued root maturation and resolution of the
periapical radioluceny is evident.
Fig 8. Periapical film taken at the 18-month follow-up appointment.
may kill viable pulp cells, including stem and progen-
itor cells in the apical papilla, considered crucial for
further root maturation.4 In a study where calcium
hydroxide was used, thickening of the dental wall only
occurred apically to the level of where the medicament
was placed.7 Fifthly, the use of a tri-antibiotic paste
consisting of ciprofloxacin, metronidazole and mino-
cycline is effective for eliminating bacteria from the
infected root canal system. Finally, initiation of a blood
450
Fig 9. Clinical photograph of teeth in the posterior segment of the left
mandible taken at the 18-month follow-up appointment. When
compared to Fig 1 there is no obvious change in shade or colour.
clot may act as a protein scaffold that allows tissue
regeneration.22 Not listed by Hargreaves et al., but
another consistent observation of these reports, is the
use of MTA to complete the coronal seal which has
known biological conductive properties to ensure an
adequate coronal seal.23
While these case reports have been labelled as either
pulpal revascularization and ⁄ or regenerative endo-
dontics with continued root development and apical
closure, it is unknown what tissue has indeed been
regenerated. Some authors have suggested that there
may be remaining viable pulpal tissue in necrotic teeth
that initiates the regenerative process.4,24 Indeed, the
resilience of pulpal tissue survival in necrotic and ⁄ or
pulpless teeth has long been known.25,26 However, a
recent study on dog teeth has shown that the ingrowth
of tissue is more likely to originate from the periodontal
ligament consisting of cementum, bone, and dentine-
like material rather than pulp tissue.27,28 These authors
suggest that there is approximately a 30% chance of
pulp tissue re-entering the pulp space.28 Further histo-
logical research on dogs by this group has reported that
the canal dentinal walls were thickened by the appo-
sition of cementum-like tissue they termed ‘intra-canal
cementum’.29
Despite these limitations of knowledge, these case
reports show evidence of the success of regenerative
endodontic procedures but the literature to date has
only been low levels of evidence; case series and case
reports. There have been only a few published reports
that address success and failure of the regenerative
procedure.5,7,8,30 Jung et al. examined the outcomes of
ª 2010 Australian Dental Association

nine teeth, five of which had some residual vital tissue
so treatment consisted of irrigation with sodium
hypochlorite and tri-antibiotic paste was placed as a
medicament but no irritation to induce bleeding of the
periapical tissues was performed.5 In the remaining
four teeth, as no vital tissue could be discerned the
protocol was the same except a blood clot was evoked.
In all nine teeth, patients were asymptomatic with
resolution of apical periodontis and draining sinuses
when present over a 1–5 year follow-up period. How-
ever, in one of the teeth with no vital pulp remnants,
there was no observable narrowing of the root canal
space despite resolution of the apical periodontitis.
Ding et al. examined 12 teeth that commenced
regenerative endodontics that included irrigation with
5.25% sodium hypochlorite and medication with tri-
antibiotic paste.8 Six patients dropped out of the study
as a consequence of pain or failure to induce bleeding
after canal disinfection and were treated with an
apexification procedure with a MTA barrier technique.
A further three patients failed to attend recall appoint-
ments. The remaining three patients exhibited complete
root development with the teeth responsive to pulp
sensibility testing. Cheuh et al. irrigated four teeth with
2.5% sodium hypochlorite but used calcium hydroxide
placed over an induced blood clot without medication
with tri-antibiotic paste.7 Whilst all four teeth demon-
strated further root maturation and apical closure,
these authors noted that this phenomenon only
occurred apically to the calcium hydroxide and
concluded that the use of calcium hydroxide was
contraindicated as potential progenitor cells may be
eliminated. Shah et al. attempted regenerative end-
odontics with a different protocol.27 Fourteen teeth
were irrigated with 2.5% sodium hypochlorite and 3%
hydrogen peroxide and formocresol was used as an
inter-appointment medicament rather than tri-antibi-
otic paste. Over a follow-up period of 0.5 to 3.5 years,
radiographic resolution was considered good to excel-
lent in 93% (13 ⁄ 14) of teeth. Thickening of the dentinal
walls was evident in 57% (8 ⁄ 14) of cases and increased
root length was observed in 71% (10 ⁄ 14) of cases.
There is an obvious need for randomized clinical trials
and further studies to evaluate clinical outcomes and
suggest a standardized approach. The American Asso-
ciation of Endodontists has commenced a database so
that clinicians can supply details of their regenerative
endodontic cases, evaluate the different approaches and
determine guidelines that have optimal outcomes.31
Interestingly, ultrasonic irrigation is not generally
reported in the listed case reports3–9 as ultrasonic
agitation of the irrigant has been shown to enhance the
cleaning and disinfection of the canal.32 In this report,
ultrasonication was used during the second treatment
session as the patient had experienced some discomfort
which may have been related to the lack of mechanical
ª 2010 Australian Dental Association
Pulp regeneration
preparation of the canal as outlined in the protocol. It is
important to use ultrasonics with minimal endosonic
filing to avoid damage to the canal walls. Ding et al.
reported two cases where pain was experienced
following placement of the antibiotic paste and the
regenerative endodontic procedure abandoned in
favour of traditional apexification techniques.8 In that
report, endosonic irrigation was not performed but
these authors suggested that this practice be recom-
mended in future clinical trials. This report suggests this
recommendation has merit as treatment successfully
included ultrasonic activation of the irrigant.
This case reported on a successful regenerative
endodontic procedure utilizing a slight variation of
the tri-antibiotic pasted developed by Hoshino and
colleagues16 as amoxicillin was used instead of mino-
cycline. In this case, there was no observable colour
change that is often associated with minocycline.
However, amoxicillin use would not be indicated in
patients with known allergy to penicillin. An alternative
approach to discolouration was taken by Reynolds
et al.9 where the dentinal tubules of the crown were first
etched with 35% phosphoric acid (Ultra-Etch, Ultra-
dent, South Jordan, UT, USA) and then sealed with
SingleBond (3M, Minneapolis, MN, USA) and flowable
composite (PermaFlo DC, Ultradent, South Jordan, UT,
USA) before placement of the tri-antibiotic paste. These
authors also recommended backfilling of the tri-antibi-
otic paste with a 20G needle to reduce the risk of
coronal placement and potential discolouration.9
SUMMARY
The immature teeth featured in the majority of the
quoted case reports were either maxillary incisors
where necrosis had developed following trauma or
premolar teeth where the evaginatus had fractured,
allowing bacterial invasion of the root canal system.3–9
This case report and others suggest that indeed there is
a paradigm shift in the endodontic management of
these teeth. Regenerative endodontic procedures allow
for resolution of apical peridontitis and associated
draining sinus tracts and continued root maturation.
Furthermore, this may reduce the risk of root fracture
associated with the thin roots in teeth treated by
traditional apexification procedures. Therefore, it is
important that dentists recognize the new protocols and
the importance of not instrumenting the canal walls
or applying medicaments such as calcium hydroxide
which have been shown to be detrimental to the
outcome. In some cases, the inability to generate
bleeding or pain may necessitate the use of traditional
apexification procedures, such as filling the apical third
of the canal with MTA. This alternative therapy should
be outlined to the patient and their guardians before
embarking on regenerative endodontic procedures as
451
A Thomson and B Kahler
part of informed consent and advice on the inherent
risks of the procedure. This case report described a
successful regenerative endodontic procedure where
amoxicillin was used instead of minocycline to reduce
the risk of discolouration of the tooth. Further guide-
lines on optimal outcomes should be released by the
American Association of Endodontists in the future as
this and other case reports are evaluated.
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Address for correspondence:
Dr Bill Kahler
School of Dentistry
The University of Queensland
200 Turbot Street
Brisbane QLD 4000
Email: w.kahler@uq.edu.au
ª 2010 Australian Dental Association
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