CASE REPORT/CLINICAL TECHNIQUES

Jing Lu, DDS, MDS,* He Liu,

Regenerative Endodontic DDS, MDS,† Zhaojie Lu, DDS,
MDS,* Bill Kahler, DClinDent,
Procedures for Traumatized PhD,‡ and Louis M. Lin, BDS,
DMD, PhDx
Immature Permanent Teeth
with Severe External Root
Resorption and Root
Perforation

ABSTRACT
SIGNIFICANCE
External root resorption (ERR) is often a complication of traumatic injury to the teeth.
Traditionally, external inflammatory root resorption is treated with calcium hydroxide. The This case report shows REPS
outcome of ERR, especially replacement resorption, is unpredictable. The purpose of the may be used to manage
present case report was to describe regenerative endodontic procedures (REPs) for 1 traumatized immature
replanted avulsed tooth with severe external root resorption and root perforation (tooth #9) permanent teeth with necrotic
and 1 extruded tooth (tooth #8). A 9-year-old girl was referred for the treatment of teeth #8 and pulp and apical periodontitis
#9 4 months after the initial trauma. Clinical examination showed that tooth #9 had a sinus associated with severe
tract present near the periapical area, was tender to percussion and palpation, and did not external root resorption with
respond to pulp sensibility tests. Tooth #8 responded to pulp sensibility tests. Periapical root perforation. The resorptive
radiographic and cone-beam computed tomographic examination showed that tooth #9 had area was arrested and
a periapical radiolucent lesion and severe ERRs with a root perforation. Tooth #9 was subsequently repaired with
diagnosed with a necrotic pulp and symptomatic apical periodontitis. Regenerative hard tissue.
endodontic procedures (REPs) were initiated. Tooth #8 became nonresponsive to pulp
sensibility tests and developed a periapical lesion 12 months after REPs of tooth #9 and was
also treated with REPs. The clinical symptoms and apical lesions resolved for both teeth after
REPs. The severe ERRs were arrested, and root perforation was repaired for tooth #9. Teeth
#8 and #9 underwent canal obliteration by hard tissue formation after REPs and were in
function at 18 months and 30 months, respectively. REPs may be used to manage
traumatized immature permanent teeth with a necrotic pulp and apical periodontitis
associated with severe ERR and root perforation. (J Endod 2020;-:1–6.)
From the *Key Laboratory of Oral Disease,
KEY WORDS School and Hospital of Stomatology,
Fujian Medical University, Fuzhou, China;
Avulsion; calcium hydroxide; external root resorption; regenerative endodontic procedures †
Department of Stomatology, Affiliated
Hospital of Jining Medical University,
Jining, China; ‡School of Dentistry,
University of Queensland, Brisbane,
Trauma, such as intrusion and avulsion, has been recognized as an important etiology of pulp necrosis Australia; and xDepartment of
of immature and mature teeth. In 1 study, approximately one half of luxated teeth resulted in pulpal Endodontics, College of Dentistry, New
necrosis1. Pulp necrosis can be a sequela of trauma and is related to the severity of the luxation York University, New York, New York
suffered, with a landmark study finding the incidence for concussion (3%), subluxation (6%), extrusion Address requests for reprints to Dr Louis
(26%), lateral luxation (58%), and extrusion (85%)2. External root resorption (ERR) is a pathologic M. Lin, Department of Endodontics,
process and frequently a complication of traumatic injury to the teeth3. ERR can be classified as College of Dentistry, New York University,
345 East 24th Street, New York, NY
inflammatory root resorption and replacement root resorption (RRR) based on the etiology4. It has
10010.
been reported that the rate of infiammatory resorption differed between the various types of luxation E-mail address: lml7@nyu.edu
injuries (extrusive luxation 5 5.6%, lateral luxation 5 11.6%, and intrusive luxation 5 33.3%). Following 0099-2399/$ - see front matter
avulsion and replantation, the incidence of active infiammatory resorptions (26.5%) and ankylosis/ Copyright © 2020 American Association
replacement resorptions (42.9%) were diagnosed5. A recent meta-analysis of avulsed teeth found an of Endodontists.
incidence of EIRR of 26.2% and RRR of 51%6. https://doi.org/10.1016/
j.joen.2020.07.022

JOE  Volume -, Number -, - 2020 RET with Severe ERR and Root Perforation 1
 EIRR is caused by surface root
resorption of cementum caused by traumatic
injury resulting in the exposure of root dentinal
tubules with a concurrent infected necrotic
pulp in the canal of the traumatized tooth7. The
bacterial toxins from the canal penetrate
through canal dentinal tubules to the root
surface denuded of cementum to initiate an
inflammatory response. The control of root
canal infection, such as root canal therapy, can
arrest EIRR4. However, if the EIRR perforates
into the canal, the perforation may not be able
to be repaired. The mechanism of RRR is not
clear. It appears to be caused by severe
damage to the root periodontal ligament (more
than 20%) of a traumatized tooth4. RRR is
characterized by replacing the root structure
by bone without the presence of a periodontal
ligament space. Root canal therapy cannot
arrest RRR because it is not of infective origin4.
Even if apexification and root canal filling were
performed for traumatized teeth with RRR,
progressive root resorption can still occur.
Biologically, RRR is also initiated by an
inflammatory process, such as root resorption
caused by orthodontic tooth movement8.
The mechanism of root resorption is
considered to be similar to bone resorption8.
However, the tooth root is more resistant than
bone to osteoclast/odontoclast bone
resorption, probably because of the low
metabolic activity because bone is constantly
undergoing modeling and remodeling. The
cellular and molecular mechanism of bone
resorption is well-known and requires
interaction between osteocytes, osteoblasts,
and osteoclast and bioactive signaling
molecules9. However, the mechanism of ERR
is not well-known8. The purpose of this case
report was to describe the clinical and
biological outcomes of traumatized immature
permanent teeth with severe ERR after REPs.
CASE REPORT
A 9-year-old girl accompanied by her mother
was referred for consultation and treatment of
traumatized maxillary central incisors (teeth #8
and #9) at the Department of Special Service,
School and Hospital of Stomatology, Fujian
Medical University, Fuzhou, China. The patient
had a traumatic injury to her maxillary anterior
teeth 4 months ago according to the patient’s
mother. Tooth #9 was avulsed for 5 hours (dry
storage) before replantation, and tooth #8 was
extruded and immediately repositioned in the
emergency dental department at a local
hospital. The patient’s medical history was
noncontributory. The patient’s dental history
was not significant, except for the dental
trauma, which had occurred 4 months
previously. On clinical examination, teeth #7,
2 Lu et al.
#8, #9, and #10 were splinted. Tooth #9 was
discolored, had a sinus tract present near the
periapical area on the buccal aspect, and was
tender to percussion and palpation.
Periodontal probing depths were less than 4
mm circumferentially. Tooth #9 did not
respond to pulp sensibility tests with the
electric pulp tester, cold, and heat, but teeth
#7, #8, and #10 responded to pulp sensibility
tests with short sharp responses with no
lingering pain when the stimulus was removed.
The teeth were asymptomatic. Teeth #8 and
#9 presented with grade II mobility. Tooth #9
had a periapical radiolucent lesion and severe
external root resorptions on the mesial and
distal root surfaces (Fig. 1A). In addition, there
was a mesial root perforation (Fig. 1A, arrow).
The root of tooth #9 appeared to be
surrounded by an irregular periodontal
ligament space. Tooth #8 did not have
evidence of ERR. Both teeth #9 and #8 had a
slightly open apex and a large pulp cavity
(Fig. 1A). Cone-beam computed tomographic
imaging revealed a large periapical osteolytic
lesion, severe ERRs, and thin buccal and
palatal root canal walls of tooth #9 (Fig. 2A–C).
Mesial root perforation of tooth #9 was
confirmed by cone-beam computed
tomographic imaging (arrow). Tooth #9 was
diagnosed as having a necrotic pulp with
symptomatic apical periodontitis and severe
ERR. Tooth #8 was diagnosed with a normal
pulp and periapical tissues. Treatment options
presented to the patient for tooth #9 included
apexification, REPs, and no treatment. The
patient decided to have treatment by REPs.
Consent was obtained from the patient’s
mother. REPs were adapted from the
American Association of Endodontists’
recommendations for clinical consideration for
a regenerative procedure10.
First Treatment Visit
A 2% topical lidocaine jelly (Akorn, Amityville,
NY) was applied around the gingiva of tooth #9
before rubber dam application. The access
opening was initiated from the lingual aspect of
the tooth crown. The canal was identified. No
vital tissue was noted. The pulp chamber and
canal were irrigated with copious amounts of
1.5% sodium hypochlorite. The working length
was determined by an electronic apex locator
and a K-file 1 mm short of the apex and
confirmed by periapical radiography.
Mechanical debridement of the canal was not
performed. Ultrasonic activation of sodium
hypochlorite was performed for 60 seconds
with an ultrasonic activator (Vista, Racine, WI).
The canal was then irrigated with saline
solution, dried with paper points, and
medicated with a paste of calcium hydroxide to
the apical third of the canal. The tooth was
temporized with glass ionomer cement.
Second Treatment Visit
The patient was scheduled 2 weeks later for a
second treatment visit. Tooth #9 was
asymptomatic, and the sinus tract resolved.
After local anesthesia with 3% Carbocaine
(Septodont, Taicang, Jiangsu, China) without
vasoconstrictor and rubber dam isolation, the
temporary restoration was removed. Calcium
hydroxide was removed with copious amounts
of sodium hypochlorite irrigation followed by
saline solution irrigation. The canal was dried
and rinsed with 17% EDTA and dried again.
Under a surgical microscope, bleeding was
induced into the canal up to the
cementoenamel junction by passing a
prebended #25 sterile K-file 2 mm beyond the
apex, which physically irritated the periapical
tissues. After a blood clot was formed,
CollaCote (Integra Life Sciences, Shanghai,
China) was placed over the blood clot in the
canal. A 3-mm thickness of mineral trioxide
aggregate paste was then placed against the
CollaCote. The tooth was restored with glass
ionomer cement and composite resin. A final
radiograph was taken (Fig. 1B). The patient
was examined after 1, 6, 12, 24, and 30
months, respectively.
Follow-up Examinations
At the 6-month follow-up (Fig. 1C), tooth #9
was asymptomatic, and radiographic
examinations showed resolution of the
periapical lesion and the arrest of ERRs with
the presence of a periodontal ligament space.
The size of the canal space was slightly
decreased because of deposition of hard
tissue on the canal walls. Tooth #8 continued
to respond to pulp sensibility tests. At the 12-
month follow-up (Fig. 1D), tooth #9 was
asymptomatic. Radiographic findings were
similar to that of the 6-month follow-up.
However, the mesial external root perforation
of tooth #9 appeared to be repaired with hard
tissue (Fig. 1D). Tooth #8 demonstrated the
presence of a periapical radiolucent lesion with
no response to pulp sensibility tests and was
diagnosed with pulp necrosis and apical
periodontitis. The splint was removed. The
patient’s mother was informed. After consent
was obtained from the patient, REPs were
performed (Fig. 1D). Both teeth were
asymptomatic at the 24-month follow-up of
tooth #9 and the 12-month follow-up of tooth
#8 (Fig. 1E and Fig. 3A–C). The canal spaces of
both teeth #9 and #8 were filled with hard
tissue. In tooth #8, the periapical lesion had
resolved. The canals of both teeth #9 and #8
were completely filled with hard tissue at the
JOE  Volume -, Number -, - 2020
FIGURE 1 – Periapical radiographs. (A ) The preoperative radiograph. Teeth #6, #7, #8, and #9 were splinted. Tooth #9 had a periapical lesion and severe ERRs with distal root
perforation (arrow ). Tooth #8 did not have evidence of ERR. Both teeth #8 and #9 had a slightly open apex and a large pulp cavity. (B ) The postoperative radiograph after REPs. (C ) Six
months after REPs, tooth #9 showed resolution of the periapical lesion and arrest of ERR. (D ) Twelve months after REPs, the radiographic findings of tooth #9 were similar to that of the
6-month follow-up. The mesial root perforation of tooth #9 appeared to be repaired with hard tissue. Tooth #8 showed the presence of a periapical lesion. REPs were performed on
tooth #8. (E ) The 24-month follow-up of tooth #9 and the 12-month follow-up of tooth #8. The canal spaces of both teeth #9 and #8 were filled with hard tissue. The periapical lesion of
tooth #8 had resolved. (F ) The 30-month follow-up of tooth #9 and the 18-month follow-up of tooth #8; the canals of both #8 and #9 were completely filled with hard tissue. The root of
tooth #9 was surrounded by a thin periodontal ligament space.

30-month follow-up of tooth #9 and 18-month
follow-up of tooth #8 (Fig. 1F). The root of tooth
#9 was surrounded by a thin periodontal
ligament space (arrows). Both teeth were
asymptomatic and in function.
DISCUSSION
Traditionally, traumatized immature permanent
teeth with a necrotic pulp/apical periodontitis
were treated with apexification to create an
apical hard tissue barrier formation by calcium
hydroxide or MTA apical plug. However,
apexification does not have the potential to
encourage thickening of the canal walls and/or
continued root development. Therefore, REPs
have become an alternate treatment for
traditional apexification because there is the
potential to promote thickening of the root
canal wall and continued root development.
ERR and root perforation of traumatized teeth
are usually treated with long-term intracanal
calcium hydroxide. Calcium hydroxide could
change the acidic environment of the resorbed
root surface to prevent osteoclast/odontoclast
activity4,11. Calcium hydroxide might be able to
induce hard tissue formation to repair root
perforation, similar to calcium hydroxide
apexification to form a hard tissue barrier to
close an open apex. Recently, REPs have

FIGURE 2 – Preoperative cone-beam computed tomographic imaging. (A ) The coronal view. The radiolucent area at the apex of tooth #9 and perforation in the distal area (arrow ). A
large periapical radiolucency is evident with erosion of the buccal cortical plate. (B ) The sagittal view. Tooth #9 had thin buccal and palatal bone plates. (C ) The axial view. Perforation of
the mesial root of tooth #9 (arrow ).

JOE  Volume -, Number -, - 2020 RET with Severe ERR and Root Perforation 3
FIGURE 3 – Cone-beam computed tomographic imaging. Twenty-four-month follow-up of tooth #9 and 12-month follow-up of tooth #8. (A ) The coronal view. Resolution of the
periapical lesion of tooth #8. Thickening of the canal walls of teeth #9 and #8. Mesial root perforation of tooth #9 filled with hard tissue. (B ) Thickening of the buccal and palatal bone
plates. (C ) Mesial root perforation of tooth #9 was filled with hard tissue.

been used to manage ERR of traumatized
teeth12–16. Furthermore, inflammatory root
perforation treated with REPs was also
reported12. In the present case report, tooth
#9 showed a decrease in the size of the canal
space because of deposition of hard tissue on
the canal walls and canal space, healing of root
perforation, and the arrest of EIRR to
strengthen the tooth after REPs.
EIRR of traumatized teeth is caused by
infection4,7. During infection/inflammation,
proinflammatory cytokines released by
immunoinflammatory cells can activate
osteoclasts/odontoclasts to induce ERR8. If
root canal infection is treated by apexification or
REPs, the proinflammatory cytokines released
by immunoinflammatory cells will be reduced,
and the ERR will be arrested because of the
inactivation of osteoclasts. Monocyte/
macrophage-colony stimulating factor and the
RANKL/RANK/OPG system are necessary for
osteoclast/odontoclast differentiation from
hematopoietic stem cells in bone marrow17,18.
In bone resorption, the osteoclasts cannot
attach to the unmineralized bone (woven bone).
The woven bone has to be primed probably by
osteoblasts, which secrete collagenase to
remove the unmineralized bone so that the
surface integrin of osteoclasts can bind to the
bone matrix, such as the osteopontin-
expressing RGD sequence9. Similarly, in dentin
and cementum, the predentin and
precementum have to be removed, most likely
by phagocytes in order for dentin and
cementum to be resorbed by odontoclasts.
After osteoclast/odontoclast resorption of the
root, similar to bone wound healing,
osteoclasts/odontoclasts will signal
cementoblasts and not osteoblasts to produce
cementum to repair the resorbed root. Wound
healing of external inflammatory root resorption
involving the cementum and dentin can only be
repaired by cementum19,20. This is because the
stem cells in the periodontal ligament can
differentiate into cementoblasts21 if given the
right signaling molecules, such as bioactive
growth factors embedded in the extracellular
matrix of cementum22 but not odontoblasts.
During root development, the cementum is
formed on the root dentin23. In immature
permanent teeth with necrotic pulp after REPs,
cementum is also formed on the root canal
dentin in many cases24. Therefore, besides
bioactive molecules released from the
cementum matrix22, the dentin matrix might
also be capable of releasing bioactive
molecules to signal stem cells in the periodontal
ligament to differentiate into cementoblasts
under specific environmental conditions25.
Although RRR did not occur in the
present case report, it is frequently a
complication of avulsed teeth after delayed
replantation. RRR of traumatized teeth is
caused by severe damage to the periodontal
ligament and not infection4. Compared with
inflammatory root resorption, the mechanism
of RRR is not clear. The tooth root must be
damaged to activate osteoclasts/odontoclasts
to remove the damaged root. It is probably
because the periodontal ligament is severely
damaged in traumatized teeth; therefore,
before the stem cells in the viable periodontal
ligament differentiate into cementoblasts and
migrate to the resorbed root surface, the
mesenchymal stem cells in the bone marrow of
nearby alveolar bone have differentiated into
osteoblasts and migrated to the resorbed root
surface and produce bone. Because the
mechanism of RRR is not clear, RRR cannot
be successfully treated. The pulp of most
avulsed teeth replanted after 30 minutes
usually do not survive26. Progressive RRR may
be prevented if the traumatized teeth contain
vital tissue in the canal, such as after REPs,
because vital tissue is endowed with an
immune defense mechanism. However, this
speculation warrants further investigation.
To our knowledge, the present case
report of tooth #9 is only the second one to
show that inflammatory root perforation of a
traumatized tooth could be treated with
REPs12. Intracanal calcification is 1 of the
outcomes of immature permanent teeth with
necrotic pulp after REPs27. The prevalence of
intracanal calcification accounts for 62.1% of
all immature permanent teeth with necrotic
pulp after revascularization28. After REPs of
tooth #9, increased thickness of the canal
walls and hard tissue formation in the canal
space were observed, which sealed the root
perforation. This is caused by stem cells from
the periodontal ligament and bone marrow
introduced into the canal by the induction of
periapical bleeding during REPs29,30. Case
reports and case series cannot be used as a
definitive treatment for a disease. However, if
more case reports and case series have a
similar observation, a hypothesis can be
formulated to conduct a controlled clinical trial
to test the validity of the treatment.
CONCLUSION
This report adds to the literature that REPs can
be a viable option to manage traumatized teeth
with severe ERR and root perforation because
the signs and symptoms of ERR were
successfully arrested at a 30-month follow-up.
ACKNOWLEDGMENTS
The authors deny any conflicts of interest
related to this study.

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