Clinical Research
Regenerative Endodontic Treatment for Necrotic Immature
Permanent Teeth
Ling-Huey Chueh, DDS, MS,* Yi-Ching Ho, DDS,† Tien-Chun Kuo, DDS, MS,‡
Wing-Hong Lai, DDS,§ Yea-Huey Melody Chen, DDS, MS,储 and
Chun-Pin Chiang, DDS, DMSc‡,¶,#
Abstract
This retrospective study included 23 necrotic immature
permanent teeth treated for either short-term (treat-
ment period ⬍3 months) or long-term (treatment pe-
riod ⬎3 months) using conservative endodontic
procedures with 2.5% NaOCl irrigations without instru-
mentation but with Ca(OH)2 paste medication. For
seven teeth treated short-term, the gutta-percha points
were filled onto an artificial barrier of mineral trioxide
aggregate (MTA). For 16 teeth treated long-term, the
gutta-percha points, amalgam, or MTA were filled onto
the Ca(OH)2-induced hard tissue barrier in the root
canal. We found that all apical lesions showed com-
plete regression in 3 to 21 (mean, 8) months after initial
treatment. All necrotic immature permanent teeth
achieved a nearly normal root development 10 to 29
(mean, 16) months after initial treatment. We conclude
that immature permanent teeth with pulp necrosis and
apical pathosis can still achieve continued root devel-
opment after proper short-term or long-term regener-
ative endodontic treatment procedures. (J Endod 2009;
35:160 –164)
Key Words
Apexification, apexogenesis, calcium hydroxide, imma-
ture teeth, mineral trioxide aggregate, NaOCl, regen-
erative endodontics
From the *Elite Dental Clinic, Taipei, Taiwan; †Department
of Dentistry, School of Dentistry, National Yang-Ming Univer-
sity, Taipei, Taiwan; ‡Graduate Institute of Clinical Dentistry,
School of Dentistry, National Taiwan University, Taipei, Tai-
wan; §Dental Department, Tainan Municipal Hospital, Tainan,
Taiwan; 储Department of Endodontics, Chi Mei Medical Center,
Tainan, Taiwan; ¶School of Dentistry, National Taiwan Univer-
sity, Taipei, Taiwan; and #Department of Dentistry, National
Taiwan University Hospital, College of Medicine, National
Taiwan University, Taipei, Taiwan.
Address requests for reprints to Dr Chun-Pin Chiang, De-
partment of Dentistry, National Taiwan University Hospital,
No. 1 Chang-Te Street, Taipei 10048, Taiwan. E-mail address:
cpchiang@ntu.edu.tw.
0099-2399/$0 - see front matter
© 2008 Published by Elsevier Inc. on behalf of the Amer-
ican Association of Endodontists.
doi:10.1016/j.joen.2008.10.019
160 Chueh et al.
T reatment of an immature open-apex permanent tooth with pulp necrosis and apical
pathosis is a big challenge for endodontists. Previous studies and case reports
suggested that both calcium hydroxide– based apexification and apexogenesis proce-
dures are acceptable for treating an immature permanent tooth with pulp necrosis and
apical pathosis (1–11). Teeth treated with the apexification procedure required the
placement of long-term calcium hydroxide in the root canal to induce formation of an
apical hard tissue barrier. Long-term calcium hydroxide therapy might alter the me-
chanical properties of dentin (12). In addition, the apexification-treated tooth only has
a thin and weak root, and these roots are susceptible to fracture. In contrast, teeth
receiving the apexogenesis procedure develop a nearly fully matured root with normal
thickness of root dentin and root length (3–11).
Pulp tissue in an immature open-apex tooth has a rich blood supply and contains
stem cells that possess a great potential to regenerate in response to damage. Therefore,
it is believed that diseased open-apex teeth should be treated as conservatively as
possible to allow successful apexogenesis to occur. Cumulative case reports of regen-
erative endodontic treatment showed convincingly that immature permanent teeth with
pulp necrosis and apical periodontitis or abscess can undergo apexogenesis, revascu-
larization, or regeneration (3–11). However, there is no standardized endodontic
protocol used for treating these necrotic immature permanent teeth.
In this study, we designed a questionnaire and tried to collect immature open-apex
teeth that had been successfully treated with the apexogenesis procedure by endodon-
tists in Taiwan. The collected data were evaluated and analyzed. We tried to evaluate (1)
what specific type of teeth were more frequently involved in this specific type of regen-
erative endodontic therapy, (2) what symptoms and signs were associated with these
necrotic immature teeth, (3) what common endodontic protocol could be used for
treating these necrotic immature teeth, (4) how long was needed to complete this
regenerative endodontic procedure, and (5) what clinical outcomes could be predicted
for necrotic immature teeth treated with regenerative endodontic therapy.
Materials and Methods
The main purpose of this retrospective study was to search for a standardized
protocol to treat immature open-apex permanent teeth with pulp necrosis and apical
pathosis. After approval by the Hospital Review Board, a designed questionnaire was
sent to several endodontists in Taiwan to collect the cases of immature permanent teeth
that fulfilled the following criteria: (1) the tooth showed symptoms and/or signs of
infection; (2) clinically, the tooth had pulp necrosis; (3) radiographically, the root had
an open apex and a radiolucent apical lesion; (4) conservative regenerative endodontic
procedures were performed; (5) symptoms improved and signs of infection disap-
peared after treatment; (6) radiographically, there was evidence of continued root
development and regression of the apical radiolucent lesion after treatment; and (7) the
follow-up period was longer than 6 months after the completion of treatment.
The data collected included the patient’s name, age, sex, tooth number, clinical
symptoms and signs, pulpal and periapical diagnoses, clinical procedures (including
irrigation solution, instrumentation, interappointment medication, and root canal–
filling materials), the number of visits for completion of the regenerative endodontic
treatment, the treatment period, and the follow-up period.
JOE — Volume 35, Number 2, February 2009
 Clinical Research
TABLE 1. Demographic Data of the Patients and Clinical Data of the 23 Necrotic Immature Permanent Teeth
Case Patient Patient Tooth
Pulpal and Periapical Diagnoses Symptoms and Signs
No. Age (y) Sex No.
1 11.9 Male 20 Pulp necrosis, acute apical abscess Pain and swelling
2 12.4 Male 20 Pulp necrosis, acute apical abscess Pain and swelling
3 11.2 Female 20 Pulp necrosis, chronic apical abscess Sinus tract
4 10.4 Male 29 Pulp necrosis, acute apical abscess Pain and swelling
5 13.2 Male 20 Pulp necrosis, asymptomatic apical periodontitis None
6 13.0 Female 29 Pulp necrosis, chronic apical abscess Sinus tract
7 14.2 Male 20 Pulp necrosis, acute apical abscess Pain and swelling
8 10.9 Male 20 Previously initiated therapy, chronic apical abscess Swelling and sinus tract
9 11.0 Male 29 Pulp necrosis, chronic apical abscess Sinus tract
10 13.5 Female 29 Pulp necrosis, asymptomatic apical periodontitis None
11 10.5 Male 20 Pulp necrosis, chronic apical abscess Sinus tract
12 11.8 Female 20 Pulp necrosis, chronic apical abscess Sinus tract
13 10.8 Female 6 Pulp necrosis, chronic apical abscess Swelling and sinus tract
14 9.4 Female 20 Pulp necrosis, chronic apical abscess Sinus tract
15 6.8 Female 30 Previously initiated therapy, chronic apical abscess Sinus tract
16 9.0 Female 29 Previously initiated therapy, acute apical abscess Pain and swelling
17 10.3 Female 13 Pulp necrosis, acute apical abscess Pain and swelling
18 12.0 Male 20 Pulp necrosis, symptomatic apical periodontitis Pain
19 10.7 Female 20 Pulp necrosis, acute apical abscess swelling
20 9.2 Male 29 Pulp necrosis, symptomatic apical periodontitis Pain
21 9.8 Female 20 Previously initiated therapy, asymptomatic apical None
periodontitis
22 10.3 Female 20 Previously initiated therapy, symptomatic apical Pain
periodontitis
23 11.3 Male 20 Pulp necrosis, acute apical abscess Pain and swelling

Results number 23 in Table 2) treatment groups. For teeth in the short-term

A total of 23 immature permanent teeth fulfilling the previously
stated criteria were collected from 21 patients (11 boys and 10 girls).
Two girls each had two second premolars treated. The 23 teeth treated
by 12 endodontists from 1990 to 2008 included three teeth published in
our previous case reports (4). Demographic data of the patients and the
clinical data of the 23 necrotic immature permanent teeth are described
in Table 1. Ages of the patients ranged from 6.8 to 14.2 (mean, 11.0 ⫾
1.7) years. The most common teeth treated were mandibular second
premolars (20 teeth). The other treated teeth were a maxillary canine,
a maxillary second premolar, and a mandibular first molar. For the
pulpal diagnosis, 18 teeth had pulp necrosis, and five had previously
initiated therapy. For the periapical diagnosis, eight teeth had an acute
apical abscess, nine had a chronic apical abscess, three had asymptom-
atic apical periodontitis, and three had symptomatic apical periodonti-
tis. In all 23 teeth, except for the maxillary canine that had trauma
history and the mandibular first molar that had decay, central cusp
fracture was suspected as the main cause of pulp necrosis and apical
pathosis.
Regenerative endodontic treatment and its clinical outcome for the
23 necrotic immature permanent teeth are described in Table 2 and
Figures 1– 4. These teeth had a common protocol involving regenerative
endodontic procedures. During the patient’s first visit, the tooth was
accessed after application of the rubber dam. The pulp chamber was
irrigated with a large amount of 2.5% NaOCl (Clorox, Oakland, CA), and
no instrumentation was performed. The canal was dried with paper
points, and the upper portion of the root canal was loosely packed with
Ca(OH)2 paste (powder mixed with saline; Merck, Frankfurt, Ger-
many), and the access was sealed with Caviton (GC, Aichi, Japan) and/or
IRM (Caulk Dentsply, Milford, DE). No intracanal bleeding was in-
duced, and none of the 23 teeth received “three mix-MP” triple antibi-
otic paste as the interappointment medicament.
These 23 teeth were divided into the short-term (treatment period
ⱕ3 months, n ⫽ 7, case number 1 to number 7 in Table 2) and
long-term (treatment period ⬎3 months, n ⫽ 16, case number 8 to
treatment group, each tooth received the same treatment modality as in
the first visit until clinical symptoms and signs associated with the ne-
crotic pulp subsided. Then, the root canal was packed with mineral
trioxide aggregate (MTA) (or plus gutta-percha points at the upper
portion), and the access was sealed with temporary filling materials or
resin. A total of 3 to 6 (mean, 4 ⫾ 1) visits were required to complete
the entire short-term endodontic treatment. The treatment period
ranged from 1 to 3 (mean, 2 ⫾ 1) months. The follow-up period for this
group ranged from 6 to 30 (mean, 15 ⫾ 11) months.
Each tooth in the long-term treatment group also received the
same treatment modality as in the first visit until symptoms and signs
disappeared, a hard barrier was detected inside the canal clinically, and
the immature tooth showed radiographic evidences of continued root
development and regression of the apical radiolucent lesion. Then, the
coronal portion of the root canal was packed with MTA (five cases),
gutta-percha points (eight cases), or amalgam (three cases), and ac-
cess was sealed with temporary filling materials or resin. In the long-
term treatment group, the diseased teeth were treated once per 1 to 3
weeks in the initial 2 months. They were treated once per 1 to 4 months
thereafter. In average, 6 ⫾ 3 (range, 3–14) visits were required to
complete the entire regenerative endodontic treatment. The treatment
period ranged from 5 to 25 (mean, 12 ⫾ 5) months. A hard tissue
barrier could be detected inside the root canal 7 ⫾ 3 (range, 4 –12)
months after initial treatment. The follow-up period ranged from 7 to
108 (mean, 32 ⫾ 28) months.
For all teeth, radiographic evidence of initial apical bone regener-
ation could be found 3 ⫾ 2 (range, 1–9) months after the initial treat-
ment and that of the complete regression of apical lesion could be
observed 8 ⫾ 5 (range, 3–21) months after the initial treatment. Fur-
thermore, radiographic evidence of continued root development could
be found 5 ⫾ 2 (range, 2–9) months after initial treatment and that of
completion of root development could be observed 16 ⫾ 6 (range,
10 –29) months after initial treatment. Of the 21 treated teeth with
complete root development, 14 had a conical root apex and 7 a blunt

JOE — Volume 35, Number 2, February 2009 Endodontic Treatment for Necrotic Immature Teeth 161
Clinical Research
TABLE 2. Regenerative Endodontic Treatment and Its Clinical Outcomes for the 23 Necrotic Immature Permanent Teeth
Regression of
Root Canal Appearance of Root Development
Case Treatment Treatment Apical Lesion Final root Follow-up
Filling Hard Tissue
No. Visits Period (Month) Initial Complete Initial Complete Apex Shape Period (Month)
Materials Barrier (Month)
(month) (month) (month) (month)
1 3 1 MTA⫹ GP — 1 7 7 13 Conical 19
2 5 1 MTA⫹ GP — 1 13 — 13 Conical 28
3 3 2 MTA — 1 7 7 — * 6
4 3 2 MTA⫹ GP — 1 7 7 — * 6
5 4 2 MTA 9 2 5 5 10 Blunt 8
6 5 3 MTA 6 3 5 5 10 Blunt 7
7 6 3 MTA⫹ GP 10 1 3 3 22 Conical 30
8 5 5 GP 5 5 12 5 12 Blunt 15
9 5 5 GP 5 2 5 2 12 Conical 7
10 8 6 GP 8 3 7 6 13 Conical 59
11 4 7 MTA 7 3 7 7 14 Blunt 22
12 5 9 MTA 10 6 21 6 21 Blunt 17
13 11 9 GP 9 9 21 9 21 Blunt 12
14 3 11 Amalgam 7 3 7 7 20 Conical 108
15 5 11 MTA 11 7 11 7 11 Conical 64
16 3 12 Amalgam 12 4 12 4 12 Conical 24
17 3 12 GP 6 3 6 3 12 Conical 8
18 14 12 MTA 4 4 8 4 26 Conical 12
19 6 14 GP 4 1 4 4 13 Conical 12
20 4 17 GP 4 — 4 4 17 Conical 48
21 8 17 GP 11 2 6 6 29 Conical 21
22 6 19 Amalgam 10 1 10 4 10 Blunt 36
23 12 25 MTA 4 — 4 4 24 Conical 53

MTA ⫽ mineral trioxide aggregate; GP ⫽ gutta-percha points.

*The 6-month follow-up period was not long enough to see the final root apex shape.

one. Two teeth showed complete obliteration of the apical root canal 17
months (case 12) and 59 months (case 10) after the initial treatment,
respectively. The remaining 21 teeth showed more or less partial oblit-
eration of the apical root canal compared with the corresponding por-
tion of the adjacent normal teeth.
Discussion
In this study, 23 necrotic immature permanent teeth were success-
fully treated with either the short-term or long-term regenerative end-
Figure 1. Periapical radiographs of case 1. (A) The initial radiograph showing
a radiolucent lesion at the periapical and mesial regions of tooth #20 with a wide
open apex. (B) A radiograph taken 1 month after initial treatment revealing MTA
and gutta-percha point filling in the root canal and evidence of healing of the
periapical and mesial radiolucent lesion. (C) Seven months after initial treat-
ment exhibiting early root formation and complete healing of the periapical and
mesial radiolucent lesion. (D) Thirteen months after initial treatment showing
complete maturation of the root apex, which is conical in shape. The apical root
canal shadow is visible.
odontic therapy. For all the teeth treated, there were three favorable
clinical outcomes: (1) symptoms and signs associated with the diseased
teeth subsided, (2) apical lesions associated with the diseased teeth
showed regression, and (3) continued root development occurred.
These results indicate that both short-term and long-term regenerative
endodontic treatment modalities are effective in treating of necrotic
immature permanent teeth.
There were several factors that helped the immature teeth achieve
continued root development. First, our patients had a mean age of 11
years, and young children have a greater healing capacity along with
more stem cell regenerative potential. In this study, the apical lesions
showed radiographic signs of initial regression as early as 1 (mean, 3)
month and radiographic signs of complete regression as early as 3
(mean, 8) months after initial treatment. In addition, the immature
teeth exhibited radiographic signs of initial continued root development
as early as 2 (mean, 5) months and radiographic signs of complete root
development as early as 10 (mean, 16) months after initial treatment.
The rapid appearance of apical bone healing and continued root devel-
opment in our patients further proved the high bone healing and tooth
regenerating potential in young children. Because our radiographs
were taken once per 1 to 6 months during the treatment period and
once per 6 to 12 months during the follow-up period, the exact bone
healing time or continued root development time could even be shorter
than the data shown in this study.
Second, immature permanent teeth have a wide root canal and
apical foramen that permits the ingrowth of small blood vessels and
regenerative pulp tissue. A wide root canal and apical opening also
allows the rapid transportation of infectious microorganisms and cyto-
kines or tissue-destruction enzymes secreted by pulpal inflammatory
cells to the periapical tissues. In addition, younger patients have loose
cancellous bones and thin cortical plates that are susceptible to damage.
These two conditions combine and result in the rapid appearance of
pain, swelling, or a sinus tract in the early stage of the disease. There-
fore, although all our patients showed signs of pulp necrosis, we sus-

162 Chueh et al. JOE — Volume 35, Number 2, February 2009


Figure 2. Clinical photographs and periapical radiographs of case 6. (A) A
photograph showing a central cusp at the occlusal surface of tooth #29. (B) A
radiograph revealing normal root development of tooth #29. (C) A photograph
taken 17 months later showing a swelling at the buccal gingiva between teeth
#28 and #29. (D) A radiograph exhibiting a radiolucent lesion at the periapical
area of tooth #29 with a wide open apex and a gutta-percha cone tracing to tooth
#29. (E) Three months after initial treatment showing healing of the buccal
gingival swelling between teeth #28 and #29. (F) A radiograph taken 3 months
after the initial treatment revealing partial regression of the periapical radiolu-
cent lesion. (G) A radiograph taken 5 months after initial treatment showing
complete healing of the periapical bone and initial deposition of hard tissue in
the apical root. (H) Ten months after the initial treatment exhibiting a com-
pletely formed root with a blunt apex and a partially obliterated canal.
pected that there were still some viable pulpal tissues in the wide root
canal. Huang et al. (13) also suggested that the infection may pass
through the survived pulp and apical papilla reaching the periapical
tissue and causing extensive bone resorption. In addition, because the
open apex provides a good communication from the pulp tissue to the
periapical tissue, it may also be possible for periapical disease to occur
while the pulp is only partially necrotic and infected (13).
Third, all root canals of diseased teeth were treated as conserva-
tively as possible. Canal cleaning was performed by irrigation with 2.5%
NaOCl, and no instrumentation or instrument-induced bleeding was
done in the root canals. Minimum instrumentation and disturbance of
the root canal system also preserved more viable pulp tissues. These
residual viable pulp tissues may subsequently contribute to the further
development of the open-apex root, finally resulting in a nearly normal
mature root.
Fourth, Ca(OH)2 paste was loosely packed in the coronal portion
of the root canal. Ca(OH)2 paste helps in the disinfection of microor-
ganisms and induces dentinal bridge formation. The dentinal bridge
JOE — Volume 35, Number 2, February 2009
Clinical Research
may protect the underlying viable pulp tissue and prevent the toxic
materials from diffusion into the residual pulp tissue. We suggest that
the previously mentioned four favorable factors finally lead to successful
clinical outcomes for the necrotic immature teeth after regenerative
endodontic treatment.
In this study, two teeth (9%) showed total obliteration and 21 teeth
(91%) more or less partial obliteration of the apical root canal during
the follow-up period. Furthermore, for the 21 treated teeth that had
complete root development, 14 showed a conical and 7 a blunt root
apex. Complete or partial root canal obliteration and the formation of a
blunt root apex are also found in teeth treated with triple antibiotic
paste– based apexogenesis procedure (9). Therefore, these findings
can be seen as inevitable consequences of conservative regenerative
endodontic treatment. These results also suggest that the treatment-
induced root development may be different from the physiological-
programmed normal root formation. Further studies are required to
explore the exact causes behind these inevitable consequences.
Root development needs two kinds of cells: epithelial cells of
Hertwig’s root sheath and odontoblasts. The former cells are present at
the apical end of immature root and are resistant to destruction, even in
the presence of inflammation (14). The epithelial cells of Hertwig’s root
sheath can induce the differentiation of mesenchymal stem cells into
odontoblasts that subsequently form root dentin. These mesenchymal
stem cells may mainly come from either the residual pulp tissue of
immature permanent teeth or from the apical papilla of immature per-
Figure 3. Clinical photographs and periapical radiographs of case 12. (A) A
photograph showing a parulis at the buccal gingiva of tooth #20. (B) The initial
radiograph showing an immature root of tooth #20 with an open apex and a
radiolucent lesion at the periapical region. (C) Six months after the initial
treatment showing disappearance of the parulis at the buccal gingiva of tooth
#20. (D) A radiograph taken 6 months after the initial treatment revealing
partial regression of the periapical radiolucent lesion. (E) A radiograph taken
10 months after the initial treatment showing MTA filling in the coronal root
canal, nearly complete regression of the periapical radiolucent lesion, and
continued development of the root apex. (F) A radiograph taken 21 months
after the initial treatment showing complete healing of the periradicular bone,
total obliteration of the apical canal, and complete maturation of the root apex,
which is blunt in shape.
Endodontic Treatment for Necrotic Immature Teeth 163
Clinical Research
Figure 4. Periapical radiographs of case 15. (A) A radiograph showing a radi-
olucent lesion at the furcation and periapical area of the tooth #30 with a wide
open distal root apex. (B) Seven months after the initial treatment revealing
narrowing of the root canal space, maturation of the root apex, and regression
of the periapical lesion. (C) A radiograph taken 11 months after the initial
treatment showing MTA filling in the root canals, complete root development,
and complete regression of the lesion. (D) A radiograph taken 64 months after
MTA filling showing normal periradicular bone, total obliteration of the distal
canal, partial obliteration of the mesial canal, and complete maturation of the
root apex, which is conical in shape.
manent teeth (so-called stem cells from the apical papilla [SCAP]) as
reported by Sonoyama et al. (15) and Huang et al. (13). SCAPs residing
in the apical papilla may survive the infection because of their proximity
to the periapical tissues. After endodontic disinfection, under the influ-
ence of the survived epithelial cells of Hertwig’s root sheath, SCAPs
differentiate into primary odontoblasts to complete the root formation
(13). Two other possible mechanisms of root development can be
attributed to stem cells from the periodontal ligament (16, 17) or from
the bone marrow (18, 19).
In the early stage of treating these necrotic immature permanent
teeth, there was no MTA available on the market. Therefore, we treated
the diseased immature permanent teeth with Ca(OH)2 and followed
them up until a hard tissue barrier formed in the root canal and the
apical lesion mostly regressed, which took several months to approxi-
mately a year. When MTA became available, we used it as an artificial
hard barrier to protect the underlying viable pulp tissue. The clinical use
of MTA in conservative endodontic treatment significantly reduced the
treatment period of regenerative endodontic therapy.
After analyzing clinical procedures used in regenerative endodon-
tic treatment, we suggest the following endodontic protocol for the
treatment of necrotic immature permanent teeth. An immature tooth
with pulp necrosis and apical periodontitis or abscess is accessed after
the application of the rubber dam. The pulp chamber is irrigated with a
164 Chueh et al.
large amount of 2.5% NaOCl, and no instrumentation is performed.
After the canal is dried with paper points, the coronal portion of the root
canal is loosely filled with Ca(OH)2 paste and the access is carefully
sealed. The patient receives repeated treatments at 1- to 2-week inter-
vals until clinical symptoms and signs subside. Then, MTA is placed in
the root canal as an artificial barrier, the remaining root canal space is
filled with gutta-percha points, and the access is permanently restored.
After this, the patient is followed up once every 3 to 12 months. Because
long-term calcium hydroxide therapy might alter the mechanical prop-
erties of dentin (12) and because our results show a successful clinical
outcome for teeth treated with the short-term conservative endodontic
protocol, we are in favor of using the short-term treatment modality for
necrotic immature teeth.
In conclusion, necrotic immature permanent teeth can achieve
continued root development after proper short-term or long-term re-
generative endodontic treatment. The clinical use of MTA as an artificial
hard barrier in regenerative endodontic therapy can not only shorten
the treatment period but also results in as favorable a clinical outcome
as is achieved by teeth treated with the long-term regenerative endodon-
tic therapy.
Acknowledgments
The authors thank Drs Yi-Chen Chen, Yueng-Yi Hsu, Yi-Yin Lai,
Hui-Ching Lin, and Kun-Ta Yang for providing either one or two
cases for this study. The authors also thank Sister Mary Ellen Kerri-
gan for editing the manuscript.
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