Review Article
Internal Root Resorption: A ReviewShanon Patel, BDS, MSc,
MClinDent,* Domenico Ricucci, MD, DDS, Conor Durak, BDSc, MFDS RCS
(Eng),* and Franklin Tay, BDSc (Hons), PhDAbstractIntroduction:
Internal root resorption is the progressive destruction of
intraradicular dentin and dentinal tubules along the middle and
apical thirds of the canal walls as a result of clastic activities.
Methods: The prevalence, etiology, pathogenesis, histologic
manifestations, differential diagnosis with cone beam computed
tomography, and treatment perspectives involved in internal root
resorption are reviewed. Results: The majority of the documentation
that exists in the literature is in the form of case reports, and
there are only a limited number of studies that attempted to
examine the histologic manifestations and biologic aspects of the
disease. This might be due, in part, to the relatively rare
occurrence of this type of resorption and the lack of an in vivo
model, apart from the previous attempt on the use of diathermy, to
predictably reproduce the condition for study. From a histologic
perspective, internal root resorption is manifested in one form
that is purely destructive, internal (root canal) inammatory
resorption, and another that is accompanied by repair, internal
(root canal) replacement resorption that is featured by the
deposition of metaplastic bone/cementum-like tissues adjacent to
the sites of resorption. Conclusions: From a differential diagnosis
perspective, the advent of cone beam computed tomography has
considerably enhanced the clinicians capability of diagnosing
internal root resorption. Nevertheless, root canal treatment
remains the treatment of choice for this pathologic condition to
date. (J Endod 2010;36:11071121)
R
oot resorption is the loss of dental hard tissues as a result of
clastic activities (1). It might occur as a physiologic or
pathologic phenomenon. Root resorption in the primary dentition is
a normal physiologic process except when the resorption occurs
prematurely (2, 3). The initiating factors involved in physiologic
root resorption in the primary dentition are not completely
understood, although the process appears to be regulated by
cytokines and transcription factors that are similar to those
involved in bone remodeling (4, 5). Unlike bone that undergoes
continuous physiologic remodeling throughout life, root resorption
of permanent teeth does not occur naturally and is invariably
inammatory in nature. Thus, root resorption in the permanent
dentition is a pathologic event; if untreated, this might result in
the premature loss of the affected teeth. Root resorption might be
broadly classied into external or internal resorption by the
location of the resorption in relation to the root surface (6, 7).
Internal root resorption has been reported as early as 1830 (8).
Compared with external root resorption, internal root resorption is
a relatively rare occurrence, and its etiology and pathogenesis
have not been completely elucidated (9). Nevertheless, internal
root resorption poses diagnostic concerns to the clinician because
it is often confused with external cervical resorption (ECR)
(1012). Incorrect diagnosis might result in inappropriate treatment
in certain cases (13). The aim of this work is to review the
etiology and pathogenesis of internal root resorption as well as
the problems encountered in the diagnosis and treatment planning of
this condition. In addition, the epidemiology, classication, and
histologic features of internal root resorption will be
discussed.
PrevalenceInternal root resorption has been described as
intraradicular or apical according to the location in which the
condition is observed (9). Intraradicular internal resorption is an
inammatory condition that results in progressive destruction of
intraradicular dentin and dentinal tubules along the middle and
apical thirds of the canal walls. The resorptive spaces might be
lled by granulation tissue only or in combination with bone-like or
cementum-like mineralized tissues (14). The condition is more
frequently observed in male than female subjects (15, 16). Although
intraradicular internal root resorption is a relatively rare
clinical entity even after traumatic injury (17, 18), a higher
prevalence of the condition has been associated with teeth that had
undergone specic treatment procedures such as autotransplantation
(19). Cabrini et al (20) amputated the coronal pulps of 28 teeth
and dressed the radicular pulp stumps with calcium hydroxide mixed
with distilled water. Eight of the 28 teeth extracted between 49
and 320 days after the procedure demonstrated histologic evidence
of internal resorption. Calis and Turkun (16) examined the
prognosis of endodontic treatment on 25 teeth xkan with
nonperforating and perforating internal resorption. The authors
reported that the most commonly affected teeth were maxillary
incisors. The small sample sizes in these studies precluded
denitive conclusions to be drawn on the prevalence of internal root
resorption. Moreover, diagnosis of internal resorption in most of
the earlier studies was based solely on 2-dimensional radiographic
evidence, without complementary 3dimensional radiographic and/or
histologic support. Further epidemiologic studies are required to
identify whether there are racial predilections in the
manifestation of intraradicular internal resorption. Compared with
intraradicular internal resorption, apical internal resorption is a
fairly common occurrence in teeth with periapical lesions (21). The
authors examined the extent of internal resorption in 75 roots (69
roots with radiolucent periapical
Key WordsBone metaplasia, cone beam computed tomography,
internal root resorption, pulp histology, pulp inammation
From the *Endodontic Postgraduate Unit, Kings College, London
Dental Institute, London, United Kingdom; Private practice, Rome,
Italy; and Department of Endodontics, School of Dentistry, Medical
College of Georgia, Augusta, Georgia. Address requests for reprints
to Dr Domenico Ricucci, Piazza Calvario, 7, 7022 Cetraro (CS),
Italy. E-mail address: [email protected]. 0099-2399/$0 - see front
matter Copyright 2010 American Association of Endodontists.
doi:10.1016/j.joen.2010.03.014
JOE Volume 36, Number 7, July 2010
Internal Root Resorption
1107
Review Articlelesions and 6 vital control roots) and graded the
severity of resorption on a 4-point scale. They concluded that 75%
of teeth associated with periapical lesions had internal apical
resorption and that vital teeth had statistically less apical
internal resorption than teeth with periapical lesions. Severe
internal resorption could be identied in 48% of those cases with
periapical lesions. Conversely, only 1 root in the control group
displayed mild internal resorption, which was speculated to be
transient in nature as a result of trauma. Because apical internal
resorption is invariably associated with apical inammatory external
resorption of the cementum from partially resorbed root apices (22,
23), only the intraradicular forms of internal root resorption will
be discussed in the rest of this article and will be simply
referred to as internal root resorption. results in inhibition of
the regulation of clastic cell differentiation. Thus, it is
possible that the OPG/RANKL/RANK system might be actively involved
in the differentiation of odontoclasts during internal root
resorption. It is known that osteoclasts do not adhere to
nonmineralized collagen matrices (40). It has been suggested that
the presence of a noncollagenous, organic component within dentin
(odontoblast layer and predentin) prevents resorption of the root
canal wall (41, 42). Similar to osteoclasts, odontoclasts might
bind to extracellular proteins containing the RGD
(arginine-glycine-aspartic acid) sequence of amino acids via
integrins (43). The latter are specic surface adhesion glycoprotein
membrane receptors containing different a and b subunits. In
particular, avb3 integrin plays a key role in the adhesion of
clastic cells (44). Extracellular matrix proteins containing the
RGD peptide sequence present on the surface of mineralized tissues,
in particular osteopontin, serve as binding sites of clastic cells
(45). The osteopontin molecule contains different domains, with one
domain binding to apatites in the denuded dentin and another domain
binding to integrin receptors in the plasma membranes of clastic
cells. Thus, osteopontin serves as a linker molecule that optimizes
the attachment of a clastic cell to mineralized tissues, mediating
the rearrangement of its actin cytoskeleton (46). It has been
speculated that the lack of RGD peptides in predentin reduces the
binding of odontoclasts, thereby conferring resistance of the canal
walls to internal root resorption. For internal root resorption to
occur, the outermost protective odontoblast layer and the predentin
(Fig. 1) of the canal wall must be damaged, resulting in exposure
of the underlying mineralized dentin to odontoclasts (40, 47). The
precise injurious events necessary to bring about such damages have
not been completely elucidated. Various etiologic factors have been
proposed for the loss of predentin, including trauma, caries and
periodontal infections, excessive heat generated during restorative
procedures on vital teeth, calcium hydroxide procedures, vital root
resections, anachoresis, orthodontic treatment, cracked teeth, or
simply idiopathic dystrophic changes within normal pulps (18, 20,
4855). In a study of 25 teeth with internal resorption, trauma was
found to be the most common predisposing factor that was
responsible for 45% of the cases examined (16). The suggested
etiologies in the other cases were inammation as a result of
carious lesions (25%) and carious/periodontal lesions (14%). The
cause of the internal resorption in the remaining teeth was
unknown. Other reports in the literature also support the view that
trauma (18, 42, 56) and pulpal inammation/infection (11, 56) are
the major contributory factors in the initiation of internal
resorption. Wedenberg and Lindskog (47) reported that internal root
resorption could be a transient or a progressive event. In an in
vivo primate study, the root canals were accessed in 32 incisors
with the predentin intentionally damaged. The access cavities in
half of the teeth were sealed; the other half were left open to the
oral cavity. The teeth were extracted at intervals of 1, 2, 6, and
10 weeks. The authors noted only a transient colonization of the
damaged dentin by multinucleated clastic cells in the teeth that
had been sealed (ie, transient internal root resorption). Those
teeth were free from bacterial contamination, and no signs of
active hard tissue resorption occurred. In the teeth that were left
unsealed during the experimental period, there were signs of
extensive bacterial contamination of pulpal tissue and dentinal
tubules. Those teeth demonstrated extensive and prolonged
colonization of the damaged dentin surface by clastic cells and
signs of mineralized tissue resorption (progressive internal root
resorption). Damage to the odontoblast layer and predentin of the
canal wall is a prerequisite for the initiation of internal root
resorption (42). However, the advancement of internal root
resorption depends on bacterial stimulation of the clastic cells
involved in hard tissue resorption (Fig. 2). Without this
stimulation, the resorption will be self-limiting (42).JOE Volume
36, Number 7, July 2010
Etiology and PathogenesisOsteoclasts are motile, multinucleated
giant cells that are responsible for bone resorption. They are
formed by the fusion of mononuclear precursor cells of the
monocyte-macrophage lineage derived from the spleen or bone marrow,
as opposed to osteoblasts and osteocytes that are derived from
skeletal precursor cells (2426). They are recruited to the site of
injury or irritation by the release of many proinammatory
cytokines. To perform their function, osteoclasts must attach
themselves to the bone surface. Recent studies indicated that the
polarity of osteoclasts is regulated by their actin cytoskeleton
(27, 28). On contact with mineralized extracellular matrices, the
actin cytoskeleton of an actively resorbing osteoclast is
reorganized to produce an organelle-free zone of sealing cytoplasm
(clear zone) associated with the osteoclasts cell membrane to
enable it to achieve intimate contact with the hard tissue surface
(29). The clear zone surrounds a series of nger-like projections
(podosomes) of cell membrane known as the rufed border. It is
underneath this rufed border that bone resorption occurs. The
resorptive area within the clear zone, therefore, is isolated from
the extracellular environment, creating an acidic microenvironment
for the resorption of hard tissues (30). Odontoclasts are the cells
that resorb dental hard tissues (Fig. 1) and are morphologically
similar to osteoclasts (31). Odontoclasts differ from osteoclasts
by being smaller in size and having fewer nuclei and smaller
sealing zones possibly as result of differences in their respective
resorption substrata (32). Osteoclasts and odontoclasts resorb
their target tissues in a similar manner (29). Both cells possess
similar enzymatic properties (33), and both create resorption
depressions termed Howships lacunae on the surface of the
mineralized tissues (Fig. 1) (29). Although mononuclear dendritic
cells share a common hematopoietic lineage with the multinucleated
osteoclasts, they have previously been regarded solely as
immunologic defense cells. Recent studies indicated that immature
dendritic cells function also as osteoclast precursors that have
the potential to transdifferentiate into osteoclasts (34, 35).
Because dendritic cells are present in the dental pulp, it is
possible they might function also as precursors of odontoclasts.
From a molecular signaling perspective, the OPG/RANKL/RANK
transcription factor system (36) that controls clastic functions
during bone remodeling has also been identied in root resorption
(37). The system is responsible for the differentiation of clastic
cells from their precursors via complex cell-cell interactions with
osteoblastic stromal cells. Similar to periodontal ligament cells
that are responsible for external root resorption (38), the human
dental pulp has recently been shown to express osteoprotegerin
(OPG) and receptor activator of nuclear factor kappa B ligand
(RANKL) mRNAs (39). Osteoprotegerin, a member of the tumor necrosis
factor superfamily, has the ability to inhibit clast functions by
acting as decoy receptors that bind to RANKL and reduce the afnity
of the latter to RANK receptors on the surface of clastic
precursors. This 1108Patel et al.
Review Article
Figure 1. Light microscopy images of a case with early internal
(root canal) inammatory resorption. (a) Maxillary canine with
caries penetrating the pulp. The tooth was tender to percussion.
There was no response to sensitivity tests. (b) Sections were taken
along the buccolingual plane. Overview image shows carious
perforation and necrotic tissue in the root canal (Taylors modied
Brown & Brenn [TBB]; original magnication, 2). (c) Coronal
third of the root canal shown in (b). Dense bacterial biolm was
present on the canal walls. Necrotic tissue can be identied in the
canal lumen (TBB; original magnication, 16). (d) High magnication
of the area indicated by the arrow in (c). Dense aggregation of
bacteria can be seen along the canal wall (TBB; original
magnication, 400. Inset; original magnication, 1000). (e) Apical
third of the root. Contrary to the histologic condition present in
the coronal two thirds, the tissue was vital (hematoxylineosin
[H&E]; original magnication, 25). (f) Magnication of the left
root canal wall. The odontoblast layer was absent, with only some
remaining predentin. Resorption lacunae can be observed along the
canal wall (H&E; original magnication, 100). (g) Higher
magnication of the upper lacuna in (f). Large multinucleated
resorbing cell (odontoclast) and granulation tissue consisting of
broblasts and chronic inammatory cells can be seen (H&E;
original magnication, 400). (h) High magnication view of the
odontoclast showing multiple nuclei. The empty space is a shrinkage
artifact (H&E; original magnication, 1000).
JOE Volume 36, Number 7, July 2010
Internal Root Resorption
1109
Review ArticleFor internal resorption to occur, the pulp tissue
apical to the resorptive lesion must have a viable blood supply to
provide clastic cells and their nutrients, whereas the infected
necrotic coronal pulp tissue provides stimulation for those clastic
cells (7) (Fig. 2). Bacteria might enter the pulp canal through
dentinal tubules, carious cavities, cracks, fractures, and lateral
canals. In the absence of a bacterial stimulus, the resorption will
be transient and might not advance to the stage that can be
diagnosed clinically and radiographically. Therefore, the pulp
apical to the site of resorption must be vital for the resorptive
lesion to progress (Fig. 1). If left untreated, internal resorption
might continue until the inamed connective tissue lling the
resorptive defect degenerates, advancing the lesion in an apical
direction. Ultimately, if left untreated, the pulp tissue apical to
the resorptive lesion will undergo necrosis, and the bacteria will
infect the entire root canal system, resulting in apical
periodontitis (57) (Fig. 2). Zetterqvist (56). In that study,
internal root resorption lesions in both primary and permanent
teeth were examined with light microscopy, scanning electron
microscopy, and enzyme histochemistry. The study examined 6 primary
and 7 permanent teeth that were extracted as a result of
progressive internal resorption. The histologic appearance and
histochemical proles of the primary and permanent teeth were
identical, but the resorption process generally occurred at a
faster rate in the primary teeth. Pulpal tissues in all the teeth
were inamed to varying degrees, with the inammatory inltrate
consisting predominantly of lymphocytes and macrophages, with some
neutrophils. The inammation was associated with dilated blood
vessels, and in 11 of the cases, bacteria were evident either in
the necrotic coronal pulp tissue or within the dentinal tubules
adjacent to the lesion. The granulation tissue in the pulp cavities
contained fewer blood vessels than in normal pulp tissue and
resembled periodontal connective tissues, with comparatively more
cells and bers. Indeed, the periodontal membrane was continuous
with the tissue in the pulp cavities in all but 2 teeth through
either the apical foramen or perforations of the external root
surfaces as a result of the resorption process. A distinguishing
feature of all the lesions
Histologic ManifestationsOur knowledge of the histologic
manifestations of internal root resorption in humans is based
largely on the work of Wedenberg and
Figure 2. Light microscopy images of a case with early internal
(root canal) inammatory resorption followed by necrosis and
infection. (a) Periapical radiograph shows a mandibular second
premolar with gross caries and enlargement of the periodontal
ligament. There was no response to sensitivity tests, and the tooth
was extremely sensitive to percussion. The buccal gingival tissues
were swollen and uctuant. The diagnosis was pulpal necrosis with
acute apical abscess. After discussing the various treatment
options, the patient opted for extraction. (b) Sections were taken
along the mesiodistal plane. Overview image shows that the distal
caries had penetrated the pulp space. Pulp tissue was necrotic
(TBB; original magnication, 2). (c) Apical third. Main canal and
ramications were lled with a bacterial biolm (TBB; original
magnication, 16). (d) Higher magnication of the main canal in (c).
Numerous resorptive defects were present on the right root canal
walls and lled with bacteria (TBB; original magnication, 100). (e)
High magnication of the upper lacuna in (d). Predentin was absent,
and the cavity was occupied by a bacterial biolm. Some
polymorphonuclear leukocytes can be observed (TBB; original
magnication, 400). (f) Resorption lacuna apical to that shown in
(e) (TBB; original magnication, 400). (g) High magnication taken
from the left canal wall of the apical canal. Despite the presence
of necrotic pulp tissue along the root canal wall, predentin was
intact at this level, and no resorption can be seen (H&E;
original magnication, 400).
1110
Patel et al.
JOE Volume 36, Number 7, July 2010
Review Articleexamined was the presence of numerous, large,
multinucleated odontoclasts occupying resorption lacunae on the
canal walls. The odontoclasts displayed evidence of active
resorption and were accompanied by mononuclear inammatory cells in
the adjacent connective tissue. Both types of cell displayed
tartrate-resistant acid phosphatase activity. There were no
predentin or odontoblasts on the dentinal walls. Of interest was
the presence of a metaplastic mineralized tissue that resembled
bone or cementum. The metaplastic mineralized tissues incompletely
lined the pulp cavity in all cases, and islands of calcied tissues
were identied from the pulp in 3 teeth. Similar metaplastic
mineralized tissues were reported by Cvek (58) and Cvek et al (59),
with ankylosis of the canal walls similar to what was observed
along the external root surfaces. On the basis of those results, 2
types of internal root resorption were described by Ne et al (60)
and Heithersay (61), internal (root canal) inammatory resorption
and internal (root canal) replacement resorption. The prexes
internal and root canal were used to delineate these entities from
similar observations in external root resorption.
Internal (Root Canal) Inammatory Resorption This type of
resorption might occur in any area of the root canal system. It is
characterized by the radiographic appearance of an ovalshaped
enlargement within the pulp chamber (Fig. 3). The condition might
go unnoticed until the lesion has advanced signicantly, resulting
in a perforation (62) or symptoms of acute or chronic apical
periodontitis after the entire pulp has undergone necrosis and the
pulp space has become infected. If resorption occurs in the coronal
portion of the tooth, the latter might exhibit a pinkish hue that
is classically described as the pink tooth of Mummery after the
19th century anatomist James Howard Mummery (63), who rst reported
the phenomenon. Internal root canal inammatory resorption involves
a progressive loss of intraradicular dentin without adjunctive
deposition of hard tissues adjacent to the resorptive sites (Figs.
13). It is frequently associated with chronic pulpal inammation,
and bacteria might be identied from the granulation tissues when
the lesion is progressive to the extent that it is identiable with
routine radiographs (47) (Fig. 3). Although chronic inammation is
commonly present in pulpal
Figure 3. Light microscopy images of a case with internal (root
canal) inammatory resorption. (a) Radiograph of a nonrestorable
grossly carious mandibular molar. A radiolucent area can be seen in
the distal root at the transition between the middle and the apical
thirds of the root canal. (b) Longitudinal section of the distal
root, taken from a mesiodistal plane. The defect appears empty,
except for some debris present in its apical extension (H&E;
original magnication, 16). (c) High magnication of the area from
the right wall indicated by the arrow in (b). Resorption lacunae
appear empty; no multinucleated cells are visible (H&E;
original magnication, 400). (d) Section taken approximately 60
sections after that shown in (b). Necrotic tissues can be seen at
the transition between the resorption area and the apical canal
followed by a concentration of cells (TBB; original magnication,
50). (e) High magnication of the area demarcated by the rectangle
in (d), showing the transition between necrotic tissue with
bacterial colonies and an area of acute inammation (TBB; original
magnication, 400). (f) High magnication of the area indicated by
the arrow at the center of the cellular accumulation in (d). Dense
aggregation of polymorphonuclear leukocytes can be identied (TBB;
original magnication, 400). (Reprinted with permission from Ricucci
D. Patologia e Clinica Endodontica. Edizioni Martina, Bologna,
Italy, 2009).JOE Volume 36, Number 7, July 2010 Internal Root
Resorption
1111
Review Articleinfections, it alone does not provide the
conditions necessary for mediating root canal inammatory
resorption. Other conditions must be present simultaneously to
initiate the event; for example, conditions must prevail for the
recruitment and activation of odontoclast precursors within the
dental pulp, and the adjacent odontoblast layer and predentin must
be disrupted (64) for those activated clastic cells to adhere to
the intraradicular mineralized dentin (Fig. 1). This probably
explains why root canal inammatory resorption is less frequently
observed than external inammatory root resorption (EIRR). The
coronal part of the pulp is usually necrotic, whereas the apical
part of the pulp must remain vital for the resorptive lesion to
progress and enlarge (Fig. 1). One hypothesis suggests that the
necrotic coronal part of the infected pulp provides a stimulus for
inammation in the apical part of the pulp. An alternative
hypothesis is based on the recent understanding that osteocytes
participate in bone homeostasis by inhibiting osteoclastogenesis
(65). In the presence of living osteocytes, osteoclasts fail to
produce actin rings, which are the hallmark of active resorbing
cells. Conversely, apoptosis of osteocytes induces the secretion of
osteoclastogenic cytokines that trigger bone resorption (66, 67).
Similar to osteocytes, dental pulp cells and odontoblasts undergo
apoptosis during tooth development as well as in response to
certain types of injury (68 71). Thus, it is possible that
odontoblasts or pulpal broblasts undergoing apoptosis as a result
of trauma or caries produce cytokines that initiate an internal
resorptive response in the apical part of the pulp. Internal
resorption only occurs when the predentin adjacent to the site of
chronic inammation is lost as a result of trauma (56) or other
unknown etiologic factors. might subsequently arrest and might be
followed by complete obliteration of the canal space by cancellous
bone. Different hypotheses have been proposed regarding the origin
of the metaplastic hard tissues that are formed within the canal
space. The rst hypothesis suggests that the metaplastic tissues are
produced by postnatal dental pulp stem cells (75, 76) present in
the apical, vital part of the root canal as a reparative response
to the resorptive insult. This is analogous to the formation of
tertiary reparative dentin by odontoblast-like cells after the
death of the primary odontoblasts (77). Unlike reactionary
dentinogenesis, dentin repair studies have shown that the matrix
deposited during reparative dentinogenesis demonstrates a high
degree of heterogeneity. Following the depletion of
epithelial-mesenchymal interactions that occur in primary
dentinogenesis, the matrix deposited in reparative dentinogenesis
often resembles osteoid instead of tubular dentin (7880).
Odontoblasts are postmitotic cells that are incapable of cell
division following their terminal differentiation. Despite the
advances in our understanding of the molecular signaling that
determines cell fate during tooth morphogenesis and regeneration
(81, 82), the precise cross-talk mechanisms that determine the
commitment of mesenchymal progenitor cells to a denitive
odontoblast lineage (as opposed to the osteoblast lineage) remain
ambiguous at large (83, 84). In the absence of highly specic
epigenetically derived signals required for lineage diversication
and differentiation of true odontoblasts in an adult tooth,
multipotent stem cells engaged in the process of reparative dentin
formation retain the osteoblastic phenotype and secrete a matrix
that more resembles bone than dentin. These histologic observations
appear to be supported by the results of a recent article that
involved the use of gene therapy to introduce a growth factor into
dental pulp stem cells (85). In that study, the newly formed hard
tissue resembled bone rather than dentin, with concentric lamellae
of mineralized matrix entrapping osteocyte-like cells. In addition,
a bone marrowlike hematopoietic tissue could be identied within the
newly formed hard tissues. Thus, it is possible that a similar
phenomenon occurs during the formation of metaplastic tissues in
root canal replacement resorption. The second hypothesis proposes
that both the granulation tissues and metaplastic hard tissues are
of nonpulpal origin. Those tissues might be derived from cells that
transmigrated from the vascular compartments or originated from the
periodontium (86). This hypothesis suggests that in internal
resorption, the pulpal tissues are replaced by periodontiumlike
connective tissues. Such a scenario is analogous to what occurs
during ingrowth of connective tissues into the pulp space when a
blood clot became available (8789) or, more recently, after pulpal
revascularization procedures (90, 91). Indeed, the histologic
features of heavy inammatory inltrates and bone/cementum-like
metaplastic tissues formation in root canal replacement resorption
are highly reminiscent of similar unresolved lymphocyte inltration
and intracanal cementum-like hard tissue deposition in experimental
revascularization procedures conducted in immature dog teeth with
apical periodontitis (92). Similar to the challenge posed by the
authors of that article (92), it is not clear whether internally
resorbed roots lled with bone/ cementum-like tissues are as strong
as teeth with canal walls supported by intact intraradicular
tubular dentin. Although root fracture associated with internal
resorption had been reported (93), the absence of histologic backup
and the paucity of such reports preclude evidence-based conclusions
to be drawn regarding the correlation between teeth with histories
of root canal replacement resorption and their fracture
resistance.
Internal (Root Canal) Replacement Resorption Internal root canal
replacement resorption is characterized by an irregular
radiographic enlargement of the pulp chamber, with discontinuity of
the normal canal space (72). Because the resorption process is
initiated within the root canal, the defect includes part of the
canal space, and hence the outline of the original canal appears
distorted. The enlarged canal space appeared radiographically to be
obliterated by a fuzzy-appearing material of mild to moderate
radiodensity (Fig. 4). This form of resorption is typically
asymptomatic, and the affected teeth might respond normally to
thermal and/or electric pulp testing unless the resorptive process
results in crown or root perforation (60). Root canal replacement
resorption appears to be caused by a low-grade inammation of the
pulpal tissues such as chronic irreversible pulpitis or partial
necrosis. Similar to root canal inammatory resorption, the chronic
inammatory process must occur along a region of the canal wall in
which the odontoblast layer and the predentin are disrupted or
damaged before the resorption component of the condition commences
(56), because odontoblasts have to bind to extracellular proteins
containing the RGD amino acid sequence. Histologically, resorption
of the intraradicular dentin is accompanied by subsequent
deposition of a metaplastic hard tissue that resembles bone or
cementum instead of dentin (Fig. 4). Metaplasia refers to a
reversible change in which one adult cell type (epithelial or
mesenchymal) is replaced by another cell type (73). In the present
context, the metaplastic tissue appears lamella-like, with
entrapped osteocyte-like cells that resemble osteons of compact
bone (Fig. 4). A variant of internal root canal replacement
resorption has previously been reported as internal tunnelling
resorption (74). This entity is usually found in the coronal
portion of root fractures but might also be seen after luxation
injuries. The resorption process tunnels into the dentin adjacent
to the root canal, with concomitant deposition of bonelike tissues
in some regions. These bone-like tissues have the appearance of
cancellous bone instead of compact bone (Fig. 5). The
process1112Patel et al.
Differential DiagnosisThe manner in which internal root
resorption presents clinically depends, to a degree, on the nature
and position of the lesion withinJOE Volume 36, Number 7, July
2010
Review Article
Figure 4. Light microscopy images of a case with internal (root
canal) replacement resorption. The tooth was derived from a
44-year-old male patient who was referred to the rst author for
management of a perforated root. The tooth was asymptomatic on
examination, but there was a history of previous trauma. (a)
Radiograph of a maxillary central incisor with a radiolucent lesion
in the mid-third of the root canal. The radiolucent lesion appears
to be mottled, which is suggestive of internal root resorption with
metaplasia. (b) Radiograph of the tooth after extraction taken at
90-degree angle to the clinical radiograph showing the continuity
of the resorptive lesion with the canal space. (c) Cross section
taken approximately at the level of line 1 in (b). Low magnication
overview shows that the dentin around the root canal had been
replaced by an ingrowth of bone tissue, and the root appears to
have been perforated on the distopalatal aspect (H&E; original
magnication, 8). (d) Higher magnication of (c) (H&E; original
magnication, 16). (e) High magnication of the area demarcated by
the rectangle in (d). The intraradicular dentin has been resorbed
(H&E; original magnication, 100). (f) High magnication taken
from the right part of (c) showing that the resorbed dentin has
been substituted by lamellar bone. Osteocytes are present in
lacunae between the lamellae. A characteristic cross section of an
osteon can be seen on the right (open arrows), with concentric
lamellae surrounding a vascular structure (H&E; original
magnication, 100). (g) High magnication of the area indicated by
the left open arrow in (e). A multinucleated resorbing cell
(odontoclast) can be seen in a dentinal lacuna, indicating active
resorption of the dentinal wall (H&E; original magnication,
1000). (h) High magnication view of the bone surface indicated by
the right arrow in (e). The large cells are osteoblast-like cells.
Once they produced mineralized tissue, they were embedded in the
bone lacunae, assuming the characteristics of osteocytes (H&E;
original magnication, 1000). (i) Cross section taken approximately
at the level of line 2 in (b). The root canal was still large at
this level and surrounded by a relatively thin layer of newly
formed bone (H&E; original magnication, 16). (j) Cross section
taken approximately at the level of line 3 in (b). At this level
the root canal appears consistently narrowed by a dense layer of
newly formed bone (H&E; original magnication, 16).
JOE Volume 36, Number 7, July 2010
Internal Root Resorption
1113
Review Article
Figure 4. (continued).
the tooth. If the pulp is still partially vital, the patient
might experience symptoms of pulpitis. However, if the resorption
is no longer active and the entire pulp has become necrotic, the
patient might eventually develop symptoms of apical periodontitis.
Sinus tracts might be detected clinically, which might be
indicative of root perforation or chronic apical abscess. A pink
discoloration might be visible through the crown of the tooth as a
result of internal root resorption in the coronal third of the root
canal. The pink spot is caused by granulation tissue undermining
the necrotic area of coronal pulp. Traditionally, the pink spot of
Mummery has been thought to be pathognomonic of internal root
resorption. However, these pink spots are more commonly associated
with ECR (12). Thus, differential diagnosis of internal root
resorption cannot be based solely on the observation of pink spots.
In many instances, there are no clinical signs, and the teeth that
exhibit internal root resorption are asymptomatic. Given the varied
manner in which internal root resorption might present clinically,
the diagnosis of the condition is primarily based on radiographic
examination, with supplementary information gained from history and
clinical ndings (10). The difculty in distinguishing internal
resorption from ECR has been highlighted in the literature (7, 10,
94). The problem in diagnosis occurs when the ECR lesion is not
accessible by probing and is projected radiologically over the root
canal. Both lesions might have a similar radiographic appearance
(Fig. 6). Gartner et al (95) described guidelines that enable
clinicians to differentiate the 2 processes radiographically. The
authors reported internal root resorption lesions to be smooth and
generally symmetrically distributed over the root. They described
the radiolucency of the internal root resorption as having a
uniform density. The pulp chamber or root canal outline could not
be followed through the lesion, because the canal walls
essen1114
tially balloon out. Internal root resorption lesions might also
be oval, circumscribed radiolucencies in continuity with the canal
walls (60). Lesions caused by ECR, by contrast, have borders that
are ill-dened and asymmetrical, with radiodensity variations in the
body of the lesion. The canal wall should be traceable through the
ECR lesion because the latter is superimposed over the root canal
(9598). The use of parallax radiographic techniques is advocated
for differentiating internal from external resorption defects (10,
94, 95). A second radiograph taken at a different angle often
conrms the nature of the resorptive lesion. ECR lesions will move
in the same direction as the x-ray tube shift if they are
lingually/palatally positioned. They will move in the opposite
direction to the tube shift if they are buccally positioned.
Conversely, internal root resorption lesions should remain in the
same position relative to the canal in both radiographs (Fig. 7).
Radiologically, internal (root canal) replacement resorption
presents as a cloudy, mottled, radiopaque lesion with irregular
margins (Fig. 8) as a result of the presence of metaplastic hard
tissue deposits within the canal space. Differentiating internal
(root canal) replacement resorption from ECR might be clinically
challenging, especially if the metaplasia has occupied the entire
resorptive cavity. Diagnostic accuracy based on conventional and
digital radiographic examination is limited by the fact that the
images produced by these techniques only provide a 2-dimensional
representation of 3-dimensional objects (94, 99, 100). In addition,
the anatomic structures being imaged might be distorted (101). This
might lead to misdiagnosis and incorrect treatment in the
management of internal root resorption and ECR. The advent of cone
beam computed tomography (CBCT) has enhanced radiographic diagnosis
(102, 103). The use of CBCT
Patel et al.
JOE Volume 36, Number 7, July 2010
Review Article
Figure 5. Light microscopy images of a variant of internal (root
canal) replacement resorption with tunneling resorption. Lower
right lateral incisor was derived from a 39-year-old former boxer
who suffered from jaw fracture during a boxing match in his early
twenties and was placed in intermaxillary xation. The patient
developed symptoms 20 years later and complained of pain associated
with his lower incisors. (a) Radiograph of the mandibular right
incisors. Lower right central incisor had asymptomatic apical
periodontitis associated with a necrotic and infected pulp. Lower
right lateral incisor showed a large area of internal root
resorption. The tooth did not respond to sensitivity tests. (b)
Sagittal CBCT slice shows some calcied tissue in the resorptive
defect. (c) Cross section taken at the level of line 1 in (a, b).
Overview shows that the canal was apparently empty at this level
(H&E; original magnication, 6). (d) High magnication of the
area indicated by the arrow in (c). Lamellar bone lls an area of
previous resorption. Note the osteon structure (arrow) (H&E;
original magnication, 100). (e) Cross section taken at the level of
line 2 in (a, b). Overview shows that the canal lumen was partly
occupied by necrotic remnants, partly by bone-like tissue (H&E;
original magnication, 8). (f) High magnication of the lower part in
(e) (H&E; original magnication, 50). (g) Higher magnication of
(f). Bone trabeculae surrounded by necrotic debris (H&E;
original magnication, 100). (h) Cross section taken from the same
area as that in (e) (TBB; original magnication, 16). (i) High
magnication of the area indicated by the arrow in (h). Fragment of
bone-like tissue can be seen surrounded by bacteria-colonized
necrotic tissues (TBB; original magnication, 100. Inset; original
magnication, 1000). (j) Longitudinal section passing approximately
through the center of the root apex. Dentin walls had been resorbed
and substituted by a bone-like tissue (H&E; original
magnication, 16).
JOE Volume 36, Number 7, July 2010
Internal Root Resorption
1115
Review Articledecisions/the number of actually negative cases,
respectively, constitute the basic measures of performance of
diagnostic tests. The receiver operating characteristic (ROC)
curve, which is dened as a plot of test sensitivity versus its
specicity, is a well-accepted method of evaluating the quality or
performance of diagnostic tests. The area under an ROC curve that
has been t by the conventional binormal model (Az) is widely used
as an index of diagnostic performance (107). Recently, Patel et al
(98) compared the accuracy of intraoral periapical radiography with
CBCT for the detection and management of root resorption lesions.
ROC Az values for correctly diagnosing internal root resorption
with intraoral radiography were satisfactory (0.78). However, CBCT
resulted in a perfect diagnosis (Az 1.00). The authors concluded
that the superior accuracy of CBCT warrants reassessment of the use
of conventional radiographic techniques for assessing root
resorption lesions. The use of CBCT can be invaluable in the
decision-making process. The scanned data provide the clinician
with a 3-dimensional appreciation of the tooth, the resorption
lesion, and the adjacent anatomy. The true nature of the lesion
might be assessed, including root perforations and whether the
lesion is amendable to treatment (Figs. 7 and 8). In the same study
(98), the authors concluded that there was a signicantly higher
prevalence in the choice of the correct treatment option when CBCT
was used compared with the use of intraoral radiographs for
diagnosing resorptive lesions.
Treatment PerspectivesOnce internal root resorption has been
diagnosed, the clinician must make a decision on the prognosis of
the tooth. If the tooth is deemed restorable and has a reasonable
prognosis, root canal treatment is the treatment of choice. The aim
of root canal treatment is to remove any remaining vital, apical
tissue and the necrotic coronal portion of the pulp that might be
sustaining and stimulating the resorbing cells via their blood
supply, and to disinfect and obturate the root canal system (108).
Internal root resorption lesions present the endodontist with
unique difculties in the preparation and obturation of the affected
tooth. Access cavity preparation should be conservative, preserving
as much tooth structure as possible, and should avoid further
weakening of the already compromised tooth. In teeth with actively
resorbing lesions, bleeding from the inamed pulpal and granulation
tissues might be profuse and might impair visibility during the
initial stages of chemomechanical debridement. The shape of the
resorption defect usually renders it inaccessible to direct
mechanical instrumentation.
Figure 6. (a) Clinical examination reveals that the mandibular
left central incisor tooth was discolored and nonresponsive to
sensitivity testing. (b) Two periapical radiographs taken at
different horizontal angles conrm the resorptive lesion is labially
positioned by using the parallax principle; the root canal outline
is still visible through the lesion, indicating that the lesion is
ECR. (c, d) Sagittal and axial CBCT slices show that the lesion is
actually internal root resorption, which is located at the
periphery of the root canal. True nature of the resorptive lesion
could only be assessed with CBCT. (Reprinted with permission from
Patel S. New dimensions in endodontic imaging: part 2cone beam
computed tomography. Int Endod J 2009;42:46375).
provides greater 3-dimensional geometric accuracy when compared
with conventional radiography (104). Several case reports and case
series have conrmed the usefulness of CBCT in diagnosing and
managing resorptive lesions (105, 106). Sensitivity and specicity,
which are dened as the number of true positive decisions/the number
of actually positive cases and the number of true negative
1116Patel et al.
Chemomechanical Debridement of the Root Canal The principal
cause of persistent apical periodontitis might be attributed to
microorganisms remaining within the canal after root canal
treatment (109112). Root canals have complex morphology that
harbors bacteria. Despite advances in endodontic techniques,
instruments and irrigants fail to predictably access the restricted
areas of the canal space (113116). The use of ultrasonic
instruments to agitate the irrigant has been shown to improve the
removal of necrotic debris and biolms from inaccessible areas of
the root canal (117). Ultrasonic activation of irrigants after
mechanical preparation of root canals has been shown to reduce the
number of bacteria. Given the inaccessibility of internal root
resorption lesions to chemomechanical debridement, ultrasonic
activation of irrigants should be viewed as an essential step in
the disinfection of the internal resorption defect. However, even
with the use of ultrasonic instruments, bacteria might still remain
in conned areas (117). Chemomechanical debridement of the root
canal space fails to consistently render the root canal system
bacteria-free (118122). Thus, an intracanal, antibacterial
medicament should be used to improve disinfection of the
inaccessible rootJOE Volume 36, Number 7, July 2010
Review Article
Figure 7. (a, b) Parallax views of the maxillary left lateral
incisor showing internal (root canal) resorption. A gutta-percha
point has been used to track the sinus. The reconstructed sagittal
(c) and axial (d) slices from CBCT reveal that the lesion has
extensively resorbed the palatal aspect of the root (arrows) and
has nearly perforated the root wall. (e) The tooth has been
obturated with gutta-percha by using a thermoplasticized
technique.
resorption defects (114). Calcium hydroxide is antibacterial and
has been shown to effectively eradicate bacteria that persist after
chemomechanical instrumentation (123, 124). Calcium hydroxide has
also been shown to have a synergistic effect when used in
conjunction with sodium hypochlorite to remove organic debris from
the root canal (125, 126). Nevertheless, some case reports
demonstrated the inability of calcium hydroxide to eliminate
bacteria in ramications because of its low solubility and
inactivation by dentin, tissue uids, and organic matter (127, 128).
Despite these limitations, the use of multiple calcium hydroxide
dressings has been advocated to enhance chemomechanical debridement
of the internal root resorption defect.
Obturation of the Root Canal The primary objective of root canal
treatment is to disinfect the root canal system. This is followed
by obturation of the disinfected canal with an appropriate
root-lling material to prevent it from reinfection. By their very
nature, internal root resorption defects can be difcult to
obturateJOE Volume 36, Number 7, July 2010
adequately. To completely seal the resorptive defect, the
obturation material should be owable. Gutta-percha is the most
commonly used lling material in endodontics. Gencoglu et al (129)
examined the quality of root llings in teeth with articially
created internal resorptive cavities. They found that the Microseal
(Sybron Endo, Orange, CA) and Obtura II (Spartan, Fenton, MO)
thermoplastic gutta-percha techniques were signicantly better in
lling articial resorptive cavities than Thermal (Dentsply, York,
PA), Soft-Core core systems (CMS Dental, Copenhagen, Denmark), and
cold lateral condensation (CLC). The CLC technique produced
slightly fewer voids than Obtura II, but a larger proportion of the
canal space was lled with sealer with this technique. Goldman et al
(130) also concluded that the Obtura II system performed
statistically better in obturating resorptive defects than CLC,
Thermal, and a hybrid technique. Stamos and Stamos (131) reported 2
cases of internal root resorption in which the Obtura II system was
used to successfully obturate the canals. Similar conclusions were
reached by others (132). In situations when the root wall has been
perforated, mineral trioxide aggregate (MTA) should be considered
the material of choice 1117
Internal Root Resorption
Review Article
Figure 8. (a, b) Radiographs reveal internal (root canal)
replacement resorption of maxillary left central incisor; note the
lesion remains centered with second parallax view. (c)
CBCT-reconstructed coronal (left) and axial (right) views of the
tooth indicate that calcied tissue was present in the coronal part
of the defect. (d) The tooth was obturated with gutta-percha by
using a thermoplasticized technique; note the irregular borders and
varying radiodensity of the root lling associated within the
internal root resorption lesion. (e) 2-year review radiograph.
to seal the perforation. MTA is biocompatible (133) and has been
shown to be effective in repairing furcation perforations (134) and
lateral root perforations (135). The material is well-tolerated by
periradicular tissues and has been shown to support almost complete
regeneration of the periodontium (134). In addition, MTA has
superior sealing properties when compared with other materials
(136). A hybrid technique might also be used to obturate canals;
the canal apical to the resorption defect is obturated with
gutta-percha, and then the resorption defect and associated
perforation are sealed with MTA (137, 138). When internal
resorption has rendered the tooth untreatable or unrestorable,
extraction is the only treatment option.
Concluding Remarks and Future DirectionsTo date, root canal
treatment remains the only treatment of choice with teeth diagnosed
with internal root resorption. Because the resorptive defect is the
result of an inamed pulp and the clastic precursor cells are
predominantly recruited through the blood vessels, controlling the
process of internal root resorption is conceptually easy, via
severing the blood supply to the resorbing tissues with
conventional root canal therapy. With that said, early detection
and a correct differential diagnosis are essential for successful
management of the outcome of internal resorption to prevent
overweakening of the remaining root structures and root
perforations. The advent of CBCT no doubt has improved the
clinicians diagnostic capability for internal root resorption.
Neverthe1118Patel et al.
less, internal root resorption is often asymptomatic, and
painful symptoms do not appear until an advanced stage of the
lesion. Thus, the clinicians ability to detect this pathologic
entity must rely heavily on the use of radiographs in routine oral
examinations. Although the advent of CBCT provides an important
adjunctive diagnostic tool for differentiating between internal
root resorption and ECR, it does not break new ground from a
treatment perspective. Irrespective of whether the lesion is
manifested histologically as the inammatory or the replacement form
of the disease, the ultimate treatment of choice for those
prognostically favorable teeth is still nonsurgical root canal
therapy. Although this pathologic condition has been reported for
more than a century, our knowledge on the pathogenesis of this
disease is, unfortunately, surprisingly thin. The majority of the
documentation that existed in the literature is in the form of case
reports, and there are only a limited number of studies that
examined the histologic manifestations and biologic aspects of the
disease. In particular, the pathogenesis aspects of this disease
still contain a high degree of uncertainty, with much of the
information adapted from our understanding of external root
resorption. This might be due, in part, to the relatively rare
occurrence of this type of resorption and the lack of an in vivo
model, apart from the previous attempt on the use of diathermy, to
predictably reproduce the condition for study. From a histologic
perspective, it appears that the disease might be manifested as one
form that is purely destructive, caused by inammation and
elaborative clastic functions, and another form that isJOE Volume
36, Number 7, July 2010
Review Articleaccompanied by repair, albeit a frustrated repair,
as a result of the deposition of metaplastic bone/cementum-like
tissues instead of true dentin. In the general scheme of things,
the reparative form of the disease exhibits histologic
manifestations that are not so much different to the manifestation
of similar frustrated repairs in reparative dentinogenesis (eg,
direct pulp capping; Ricucci et al, unpublished results, 2009) and
revascularization of nonvital dental pulps (92). There remains a
wide gap of knowledge in our understanding of the conditions that
precipitate the 2 different forms of internal root resorption. For
example, it is not known whether one can alter the inammatory and
microbial status of the involved pulp to shift the manifestation of
the disease from a purely destructive form to one that is
accompanied by at least some form of repair. Such a notion might
sound philosophical to the practicing clinician. However, it might
have an outreaching appeal to the molecular biologists and stem
cell scientists within our profession in their quest for
controlling the commitment of progenitor cell types capable of
recapitulating the embryonic events in primary odontogenesis as a
future endodontic treatment strategy. As the concept of pulpal
regeneration becomes a foreseeable reality, it is prudent to
elaborate on whether such a treatment strategy might be adaptable
for the management of teeth with internal root resorption. There
are similarities and differences between the currently achievable
status of pulpal revascularization and the replacement form of
internal root resorption. The similarities are evident in the
manifestations of frustrated repair by metaplastic hard tissues
after the senescence of primary odontoblasts. The dental pulp is
equipped with the potential of regenerating odontoblast-like cells
from dental pulpal stem cells through limited molecular signaling
mechanisms after succumbing of ectomesenchymal crosstalks that
occur during primary dentinogenesis. Scientists are beginning to
grasp the fundamentals of these intricate signaling mechanisms;
however, control is still lacking in the ability to precisely
delineate the odontoblastic lineage from the osteoblastic lineage.
Nevertheless, the advances achieved so far have been phenomenal.
After all, the creativity of evolution in which nature explores all
options and produces the best solution has taken millions of years
to bring to perfection. On the contrary, gene and stem cell
therapies have only been proactive for more than 2 decades. Unlike
pulpal revascularization procedures, however, the onset of internal
root resorption is hallmarked by the recruitment of clastic
precursors, their activation, and subsequent attachment to
osteopontin-rich mineralized matrices. Thus, even if precise
controls of signaling mechanisms for the differentiation of
odontoblasts from their progenitor cells are available, additional
strategies must be targeted at pacifying the activities of clastic
cells at 1 of the 3 aforementioned stages (ie, recruitment,
activation, and attachment). Although these tasks might appear
formidable, it is at the molecular signaling level that one
anticipates the greatest expansion of horizons. Advances in
different scientic disciplines will enrich the pool of ideas for
future therapeutic strategies, apart from conventional root canal
therapy, in the treatment of internal root resorption. The scope of
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AcknowledgmentsThe authors wish to thank Cavendish Imaging,
London, UK, and the Department of Dental & Maxillofacial
Imaging, The Dental Institute, Kings College London, London.
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