doi:10.1111/iej.

12784

CASE REPORT

Regenerative endodontic treatment of

perforated internal root resorption: a
case report

M. E. Kaval1 € neri2 & M. K. C

, P. Gu ß alısßkan1
1
Department of Endodontology, School of Dentistry, Ege University, Izmir; and 2Department
of Oral and Maxillofacial Radiology, School of Dentistry, Ege University, Izmir, Turkey

Abstract

€ neri P, C
Kaval ME, Gu ß alısßkan MK. Regenerative endodontic treatment of perforated internal root
resorption: a case report. International Endodontic Journal, 51, 128–137, 2018.

Aim To present the regenerative endodontic treatment procedure of a perforated inter-

nal root resorption case and its clinical and radiographic findings after 2 years.
Summary A 14-year-old female patient was referred complaining of moderate pain
associated with her maxillary left lateral incisor. After radiographic examination, a perfo-
rated internal resorption lesion in the middle third of tooth 22 was detected. Under local
anaesthesia and rubber dam isolation, an access cavity was prepared and the root canal
was shaped using K-files under copious irrigation with 1% NaOCl, 17% EDTA and dis-
tilled water. At the end of the first and second appointments, calcium hydroxide (CH)
paste was placed in the root canal using a lentulo. After 3 months, the CH paste was
removed using 1% NaOCl and 17% EDTA solutions and bleeding in the root canal was
achieved by placing a size 20 K-file into the periapical tissues. Mineral trioxide aggre-
gate was then placed over the blood clot. The access cavity was restored using glass–
ionomer cement and resin composite. After 2 years, the tooth was asymptomatic and
radiographic examination revealed hard tissue formation in the perforated resorption
area and remodelling of the root surface.
Key learning points
• Regenerative endodontic treatment procedures are an alternative approach to treat
perforated internal root resorption lesions.
• Calcium hydroxide was effective as an intracanal medicament in regenerative
endodontic treatment procedures.

Keywords: calcium hydroxide, internal root resorption, regenerative endodontic

treatment.

Received 4 October 2016; accepted 20 April 2017

Correspondence: Mehmet Emin Kaval, Department of Endodontology, School of Dentistry,

Ege University, 35100 Izmir, Turkey (Tel.: +90 232 311 46 08; Fax: +90 232 388 03 25;
e-mail: mehmetkaval@hotmail.com).

128 International Endodontic Journal, 51, 128–137, 2018 © 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd
 CASE REPORT
Introduction

Internal root resorption (IRR) is defined as a resorptive defect of the internal aspect of
the root caused by odontoclastic activity associated mainly with chronic pulp inflamma-
tion and trauma. Continuous microbial irritation, pulpotomy, cracks, transplantation pro-
cedures, orthodontic treatment and even viral infections are considered as other
aetiological factors (Brady & Lewis 1984, Solomon et al. 1986, Walton & Leonard 1986,
Haapasalo & Endal 2006, Patel et al. 2010). Osteoprotegerin, the receptor activator of
nuclear factor kappa-B ligand (RANKL), the receptor activator of nuclear factor kappa-B
(RANK) and the macrophage colony-stimulating factor (MCSF) have been considered
important components for the inflammatory cascade within the pulp tissue that triggers
the differentiation of stem cells to odontoclasts or macrophages to develop dentine
resorption (Rani & MacDougall 2000, Belibasakis et al. 2013). However, the exact
immunohistochemical mechanism of the resorption process is not understood com-
pletely (Nilsson et al. 2013).
Diagnosis of IRR depends on the localisation and severity of the resorptive area. Due
to its asymptomatic nature, IRR initially is mostly detected coincidentally during routine
€rku
radiographic investigations (Calısßkan & Tu €n 1997). However, clinical symptoms (pain,
swelling, sinus tract, discoloration of the related teeth) are noticeable in advanced
stages (Haapasalo & Endal 2006). Additionally, when IRR is located coronally, a typical
pinkish clinical appearance known as a ‘pink spot’ that is related to the vascularized
connective tissue containing the osteoclasts is often observed (Mummery 1920, Silveira
et al. 2009). However, in some cases, the condition might be misdiagnosed as external
root resorption, due to the similar pinkish appearance of such defects (Lyroudia et al.
2002, Heithersay 2007).
Radiographically, the defects are generally uniform, round to oval and the normal root
canal space is disrupted. Even though the margins of IRR are clearly defined in the radi-
olucent area, the outline of the original canal appears distorted. When the resorption
extends to the external root surface and disrupts the root walls, destruction of the adja-
cent periodontal tissues may occur (Gartner et al. 1976, Gulabivala & Searson 1995).
Early diagnosis and accurate management of IRR is essential to maintain the integrity
of the tooth (Patel et al. 2010), and determining the borders of the resorption area is
considered as an important factor in assessing the treatment of choice (Bhuva et al.
2011). Therefore, three-dimensional evaluation of the resorption area with cone beam
computerized tomography (CBCT) provides vital information for early diagnosis and
treatment planning (Patel et al. 2009b, Nilsson et al. 2013). When the defect is limited
to the root canal system and does not extend to the periodontal tissues, root canal
treatment is expected to be successful (Calısßkan & Tu €rku
€n 1997). In such cases, the
main strategy of the treatment process is removal of the remaining destructive and/or
necrotic pulp tissue, stopping the resorptive process and filling of the root canal system
including the resorptive defect (Patel et al. 2010). However, this procedure can be diffi-
cult depending on the location of the resorption area, because the already compromised
tooth can be further weakened during treatment. If the resorption area perforates the
root, then the treatment process could be more challenging and recalcification treat-
ment using calcium hydroxide (CH) and/or surgical approaches has been suggested as
treatments of choice (Calısßkan & Tu €rku
€n 1997, Nilsson et al. 2013). Weakened tooth
structure due to the IRR is susceptible to fracture and sometimes extraction might be
necessary due to the extensive and unrestorable destruction (Jacobovitz & de Lima
2008).
Regenerative endodontic treatment (RET) has been introduced as an alternative treat-
ment protocol for apexification and root canal treatment (Murray et al. 2007). Most of

© 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd International Endodontic Journal, 51, 128–137, 2018 129
 the RET procedures are focused on immature teeth with nonvital pulps (Cotti et al.
CASE REPORT

2008, Bose et al. 2009, Ding et al. 2009, Trope 2010, Iwaya et al. 2011), but there are
limited case reports on its efficacy in other clinical situations (Chaniotis 2014, Santiago
et al. 2015, Priya et al. 2016, Saoud et al. 2016). RET may be successful in IRR cases
(Priya et al. 2016, Saoud et al. 2016) such a treatment approach provides the opportu-
nity for replacement of the missing tooth structures and retention of the related tooth
could be improved significantly. Therefore, the aim of this case report is to present a
RET procedure of a perforated IRR within the middle third of the root and its clinical
and radiographic findings after 2 years.

Case report

A 14-year-old female patient was referred due to moderate pain associated with her
maxillary left lateral incisor (tooth 22). The medical history of the patient was noncon-
tributory. Clinical examination revealed that the tooth was slightly sensitive to percus-
sion and responded negatively to electric pulp testing. Periodontal probing depth and
mobility were within normal limits. On the periapical radiograph, a resorption area in the
middle third of tooth 22 was detected. A preliminary diagnosis of symptomatic apical
periodontitis and internal root resorption was made (Fig. 1a). In order to acquire more
information about the location and borders of the resorption area, a CBCT (Kodak 9000
3D; Practice Works, Inc., Atlanta, GA, USA) image of the tooth was obtained using
standard settings (10.8 s exposure time, 70 kV, and 10 mA). Axial, sagittal and coronal
CBCT cross sections (76 lm thickness) confirmed the severe resorption area which
had perforated the root surface (Fig. 1b,c,d). The buccal and palatal surfaces of the
tooth were resorbed, and the resorptive process had invaded the buccal cortical plate
of bone. The mesial surface of the tooth was also involved, and only the distal side of
the root appeared sound. Using the measurement tool of the software (CS 3D Imaging
Software version 3.1.9; Carestream Dental LLC, Atlanta, GA, USA), the resorption area
was established as 4.6 9 4.5 9 3.8 mm.
The treatment strategy was to perform RET using CH medication with endodontic
surgery being considered as further treatment in the event of the unpredictable progno-
sis of the perforated IRR area. The patient and her parents were fully informed about
the treatment procedure and the follow-up examinations, and a written informed
consent form was obtained before the treatment procedure commenced.
Under local anaesthesia and rubber dam isolation, an access cavity was prepared.
The root canal shaping procedure was conducted in two stages within the same
appointment. At the initial stage, the working length was determined at the level of the
coronal border of the resorption area using an electronic apex locator (Propex II;

(a) (b) (c) (d)

Figure 1 Preoperative periapical radiograph showing maxillary left lateral incisor with severe IRR
(a). Axial (b), sagittal (c) and coronal (d) CBCT images of the related tooth revealing perforations on
the buccal palatal and mesial root surfaces associated with the resorption area.

130 International Endodontic Journal, 51, 128–137, 2018 © 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd
Dentsply Sirona Ballaigues, Switzerland) and a periapical radiograph was taken. The root

CASE REPORT
canal was prepared using K-files (Mani, Inc, Tochigi Ken, Japan) up to size 80. At the
second stage, access to the apical part of the root canal was achieved using a size
15 K-file passing beyond the resorption area, and the working length was set 1 mm.
shorter than the radiographic apex. Root canal preparation was performed at this length
up to a size 45 K-file. During root canal shaping the root canal was gently irrigated using
1% sodium hypochlorite (NaOCl; Merck, Darmstadt, Germany) and distilled water using
a side-vented irrigation needle (KerrHawe Irrigation Probe; KerrHawe SA, Bioggio,
Switzerland). At the end of instrumentation, the root canal was irrigated using 17%
ethylenediaminetetraacetic acid (EDTA; Merck, Darmstadt, Germany). Bleeding originat-
ing from the resorption area did not stop completely, but the coronal part of the resorp-
tion area could be dried using paper points. After that, CH paste (Merck) was placed
into the canal using a lentulo (size 40; Mani Inc., Tochigi-Ken, Japan) and the access
cavity was filled temporarily with glass–ionomer cement (GC Fuji IX Extra; GC Co.,
Tokyo, Japan).
Four weeks later, the CH paste was removed using 1% NaOCl, 17% EDTA and dis-
tilled water. Bleeding in the resorption area was decreased, but has not eliminated
totally; therefore, at the end of the second appointment, CH paste was placed into the
root canal again. The access cavity was filled with glass–ionomer cement.
The patient failed to comply with the schedule because for personal reasons and
was seen 3 months later. The tooth was asymptomatic (Fig. 2a), the temporary filling
was removed and the root canal was irrigated using 1% NaOCl, 17% EDTA and dis-
tilled water. Bleeding into the canal space was achieved by placing a size 20 K-file
(Mani Inc) into the periapical tissues. Mineral trioxide aggregate (MTA) (Dentsply Tulsa
Dental, Tulsa, OK, USA) was placed over the blood clot. The MTA was covered with a
wet cotton pellet to provide moisture, and the access cavity was filled with glass–iono-
mer cement. Two days later, the glass–ionomer cement was removed and the tooth
was restored with composite resin (Clearfil Majesty Esthetic; Kuraray Medical,
Okayama, Japan) (Fig. 2b).
At the 6 months and 2 years, the tooth was asymptomatic and responded negatively
to thermal and electric pulp testing. Periapical radiographs revealed hard tissue forma-
tion in the perforated resorption area and remodelling of the root surface (Fig. 2c,d). At
the 2-year follow-up, CBCT of the tooth was taken and axial, coronal and sagittal CBCT
sections disclosed healing of both the buccal and palatal surfaces of the tooth; the
increase in root canal wall thickness was noticeable on the previous resorption sites,
and significant healing of the periradicular lesion was detected (Fig. 2e–g). Additionally,
comparison of the preoperative and 2-year follow-up sagittal CBCT sections of the tooth
disclosed remineralization within the root canal and 1.1 9 1.5 mm hard tissue formation
was apparent between the coronal and root pulp tissues (Fig. 3).

Discussion

Optimum disinfection of the root canal system using intracanal medicaments is consid-
ered to be an important step of RET (Ding et al. 2009). The most frequently used intra-
canal medicaments in RET procedures are triple (ciprofloxacin, metronidazole and
minocycline) or double (ciprofloxacin, metronidazole) antibiotic combinations (Trope
2010). Although antibiotic combinations are associated with successful results in RET
procedures (Hoshino et al. 1996, Sato et al. 1996), they have disadvantages, including
discoloration, bacterial resistance and allergic reactions (Reynolds et al. 2009). CH paste
is considered as another alternative medicament in RET procedures (Chueh et al. 2009,
Cehreli et al. 2011, European Society of Endodontology Position Statement 2016). The

© 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd International Endodontic Journal, 51, 128–137, 2018 131
CASE REPORT
(a) (b) (c) (d)

(e) (f) (g)

Figure 2 Periapical radiographs at the third visit before placement of MTA (a). The postoperative
periapical radiograph taken after the placement of MTA and composite resin restoration (b). Six
months (c) and two years (d) of follow-up radiographs demonstrating progressive healing of the
resorptive defect. CBCT images (e,f,g) of maxillary left lateral incisor disclosing healing of both the
buccal and palatal surfaces of the tooth, increased root canal wall thickness and significant healing
of the periradicular lesion.

risk of killing the remaining stem or progenitor cells (Thomson & Kahler 2010), partial
obliteration of the root canal (Chueh et al. 2009) and decreasing the fracture resistance
of the root (Andreasen et al. 2002) are amongst the shortcomings of CH treatments.
However, recent reports reported good results of RET procedures using CH pastes
(Chueh & Huang 2006, Cotti et al. 2008, Chueh et al. 2009, Cehreli et al. 2011, Iwaya
et al. 2011). Chueh et al. (2009) suggested using CH in the coronal third of the root
canal as a precaution for minimizing the negative effects of this medicament to stem
cells and reported successful outcomes. In the present case CH paste was preferred
as the intracanal medicament to remove the necrotic residual pulp tissue and eliminate
osteoclastic activity. Additionally, CH paste has positive effects for the control of bleed-
nior et al. 2010).
ing and prevents reinfection of the defect (Brito-Ju
In the present case, root canal shaping and irrigation was performed in two different
stages. Communication of the root canal system with periradicular tissues in the perfo-
ration area and the irregular root canal morphology were the determinant factors during
the shaping procedures. As a precaution, a lower concentration of NaOCl solution was
used, to protect periradicular tissues from its toxic effects (Spangberg et al. 1973,
Baumgartner & Cuenin 1992, Hu €lsmann & Hahn 2000).
The size of the apical foramen might be an important factor on the outcome of the
RET; however, there is no consensus on the minimum diameter of the apical foramen
for providing migration of the stem or progenitor cells into the root canal space. Laureys
et al. (2013) emphasized that enlargement of the apical foramen to at least 1 mm is
not crucial for RET, and they reported that 0.32 mm in diameter did not prevent revas-
cularization. Paryani & Kim (2013) reported that apical enlargement up to size 0.6 mm

132 International Endodontic Journal, 51, 128–137, 2018 © 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd
 CASE REPORT
Figure 3 Subtraction of preoperative and postoperative sagittal CBCT images, demonstrating the
regenerative hard tissue formation on the IRR area following RET procedure.

was sufficient in their two RET cases. In the present case report, apical enlargement
was performed up to 0.45 mm and this apical diameter was successful up to 2 years.
There appears to be two case reports concerning the treatment of IRR cases using
RET (Priya et al. 2016, Saoud et al. 2016), but the presence of a perforation was
reported only in one of the cases (Saoud et al. (2016). They used CH paste (Metapaste;
Meta Biomed, Chungbuk, South Korea) at the first visit and applied triple antibiotic
paste at the second visit. At the third visit, a blood clot was created and covered with
MTA. Progressive healing of the root resorption area and reduction in the periapical
lesion was evident at the 19-month follow-up. Priya et al. (2016) described an uncom-
mon RET protocol in an internal and external root resorption case, which occurred after
a delayed replantation procedure of a mature permanent maxillary central incisor. In that
case, in contrast to the previous RET reports, platelet-rich plasma (PRP) was applied
during the replantation procedure and glass–ionomer cement was placed on the PRP
instead of MTA. Additionally, double antibiotic paste (metronidazole, minocycline) was
injected into the coronal portion of the root canal which contained regenerated vital or
vascular tissues. At the 12-month follow-up, the tooth was asymptomatic, but there
was no demonstrable hard tissue deposition in the area of IRR. In contrast to those
two case reports, definite healing was observed in the IRR area of the present case at
2 years, which was confirmed qualitatively and quantitatively by CBCT evaluation. Com-
parison of subsequent 3D images also revealed regenerative hard tissue formation in
the IRR area following the RET procedure.
Even though periapical radiographs provide useful information, conventional radio-
graphs are not sufficient to define the severity of the condition and the location/borders
of resorptive defect accurately (Patel et al. 2009a, Bhuva et al. 2011). CBCT provides
three-dimensional images of the resorption with high sensitivity and specificity using
axial, coronal and sagittal sections. Thus, it is more suitable to the clinician to correctly

© 2017 International Endodontic Journal. Published by John Wiley & Sons Ltd International Endodontic Journal, 51, 128–137, 2018 133
 diagnose and manage the defect (Bhuva et al. 2011). Additionally, CBCT offers informa-
CASE REPORT

tion on the presence of root perforations, root canal wall thickness, size and the local-
ization of the periradicular lesions, relation to the neighbouring anatomical structures,
and occurrence of metaplastic hard tissue deposition within the canal space that looks
like bone or cementum (Estrela et al. 2009). However, CBCT is associated with higher
radiation to the patient than conventional radiographs, and in order to provide the radia-
tion protection of the patient, and it has been suggested that CBCT imaging should only
be used in essential cases (Scarfe et al. 2009).
The healing mechanism of the present case may be considered as a three-step pro-
cess: disinfection of the root canal, arresting the osteoclastic activity and initiation of
new tissue formation within the resorption area and root canal space. Disinfection of
the root canal system is provided with mechanical preparation, irrigation of the root
canal and application of CH medication. Moreover, CH stops osteoclastic activity and
hard tissue resorption (Tronstad et al. 1981, Mohammadi & Dummer 2011) by necrotiz-
ing and eliminating the granulation tissue, which is the nidus of the osteoclastic pro-
cess. In the final phase, severely weakened tooth structure is treated by the RET
procedure, which allows the migration of progenitor stem cells into the defect and the
root canal space in order to complete the remodelling process.
The nature of the tissue formed within the root canal space following RET proce-
dures has been investigated in previous animal and human studies (Wang et al. 2010,
Yamauchi et al. 2011, Martin et al. 2013, Shimizu et al. 2013). Although the authors
have stated that the newly formed tissue within the root canal either resembled
cementum, bone or periodontal ligament-like fibrous tissue (Wang et al. 2010, Yamau-
chi et al. 2011 Lin et al. 2014), they were not actual parenchymal pulp tissue and the
invasion of endogenous stem cells within the root canal appears to be insufficient to
develop a new dentine–pulp complex.

Conclusion

Regenerative endodontic treatment procedures are an alternative treatment approach in

IRR cases. Calcium hydroxide paste has potential as an intracanal medicament in RET
procedures. However, further clinical investigations are required in order to clarify the
exact healing process of IRR cases using RET and to provide validation of the
suggested protocol in clinical endodontic practice.

Conflict of interest

The authors have stated explicitly that there are no conflicts of interest in connection
with this article.

Disclaimer

Whilst this article has been subjected to Editorial review, the opinions expressed,
unless specifically indicated, are those of the author. The views expressed do not
necessarily represent best practice, or the views of the IEJ Editorial Board, or of its
affiliated Specialist Societies.

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