internal root resorption- a review

Internal Root Resorption: A ReviewShanon Patel, BDS, MSc, MClinDent,* Domenico Ricucci, MD, DDS,† Conor Durak, BDSc, MFDSRCS (Eng),* and Franklin Tay, BDSc (Hons), PhD‡

AbstractIntroduction: Internal root resorption is the progressivedestruction of intraradicular dentin and dentinal tubulesalong the middle and apical thirds of the canal walls asa result of clastic activities. Methods: The prevalence,etiology, pathogenesis, histologic manifestations, differ-ential diagnosis with cone beam computed tomography,and treatment perspectives involved in internal rootresorption are reviewed. Results: The majority of thedocumentation that exists in the literature is in theform of case reports, and there are only a limited numberof studies that attempted to examine the histologicmanifestations and biologic aspects of the disease.This might be due, in part, to the relatively rare occur-rence of this type of resorption and the lack of an invivo model, apart from the previous attempt on theuse of diathermy, to predictably reproduce the conditionfor study. From a histologic perspective, internal rootresorption is manifested in one form that is purelydestructive, internal (root canal) inflammatory resorp-tion, and another that is accompanied by repair, internal(root canal) replacement resorption that is featured bythe deposition of metaplastic bone/cementum-liketissues adjacent to the sites of resorption. Conclusions:From a differential diagnosis perspective, the advent ofcone beam computed tomography has considerablyenhanced the clinician’s capability of diagnosinginternal root resorption. Nevertheless, root canal treat-ment remains the treatment of choice for this pathologiccondition to date. (J Endod 2010;36:1107–1121)

Key WordsBone metaplasia, cone beam computed tomography,internal root resorption, pulp histology, pulp inflamma-tion

Root resorption is the loss of dental hard tissues as a result of clastic activities (1). Itmight occur as a physiologic or pathologic phenomenon. Root resorption in the

primary dentition is a normal physiologic process except when the resorption occursprematurely (2, 3). The initiating factors involved in physiologic root resorption in theprimary dentition are not completely understood, although the process appears to beregulated by cytokines and transcription factors that are similar to those involved inbone remodeling (4, 5). Unlike bone that undergoes continuous physiologicremodeling throughout life, root resorption of permanent teeth does not occurnaturally and is invariably inflammatory in nature. Thus, root resorption in thepermanent dentition is a pathologic event; if untreated, this might result in thepremature loss of the affected teeth.

Root resorption might be broadly classified into external or internal resorption bythe location of the resorption in relation to the root surface (6, 7). Internal rootresorption has been reported as early as 1830 (8). Compared with external rootresorption, internal root resorption is a relatively rare occurrence, and its etiologyand pathogenesis have not been completely elucidated (9). Nevertheless, internalroot resorption poses diagnostic concerns to the clinician because it is often confusedwith external cervical resorption (ECR) (10–12). Incorrect diagnosis might result ininappropriate treatment in certain cases (13).

The aim of this work is to review the etiology and pathogenesis of internal rootresorption as well as the problems encountered in the diagnosis and treatment planningof this condition. In addition, the epidemiology, classification, and histologic features ofinternal 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 resorp-tion is an inflammatory condition that results in progressive destruction of intraradic-ular dentin and dentinal tubules along the middle and apical thirds of the canal walls.The resorptive spaces might be filled by granulation tissue only or in combination withbone-like or cementum-like mineralized tissues (14). The condition is more frequentlyobserved in male than female subjects (15, 16). Although intraradicular internal rootresorption is a relatively rare clinical entity even after traumatic injury (17, 18), a higherprevalence of the condition has been associated with teeth that had undergone specifictreatment procedures such as autotransplantation (19). Cabrini et al (20) amputatedthe coronal pulps of 28 teeth and dressed the radicular pulp stumps with calciumhydroxide mixed with distilled water. Eight of the 28 teeth extracted between 49 and320 days after the procedure demonstrated histologic evidence of internal resorption.Calisxkan and Turkun (16) examined the prognosis of endodontic treatment on 25 teethwith nonperforating and perforating internal resorption. The authors reported that themost commonly affected teeth were maxillary incisors. The small sample sizes in thesestudies precluded definitive conclusions to be drawn on the prevalence of internal rootresorption. Moreover, diagnosis of internal resorption in most of the earlier studies wasbased solely on 2-dimensional radiographic evidence, without complementary 3-dimensional radiographic and/or histologic support. Further epidemiologic studiesare required to identify whether there are racial predilections in the manifestation ofintraradicular internal resorption.

Compared with intraradicular internal resorption, apical internal resorption isa fairly common occurrence in teeth with periapical lesions (21). The authors exam-ined the extent of internal resorption in 75 roots (69 roots with radiolucent periapical

From the *Endodontic Postgraduate Unit, King’s College,London Dental Institute, London, United Kingdom; †Privatepractice, Rome, Italy; and ‡Department of Endodontics, Schoolof 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]/$0 - see front matter

Copyright ª 2010 American Association of Endodontists.doi:10.1016/j.joen.2010.03.014

JOE — Volume 36, Number 7, July 2010 Internal Root Resorption 1107

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lesions and 6 vital control roots) and graded the severity of resorptionon a 4-point scale. They concluded that 75% of teeth associated withperiapical lesions had internal apical resorption and that vital teethhad statistically less apical internal resorption than teeth with periapicallesions. Severe internal resorption could be identified in 48% of thosecases with periapical lesions. Conversely, only 1 root in the controlgroup displayed mild internal resorption, which was speculated to betransient in nature as a result of trauma. Because apical internal resorp-tion is invariably associated with apical inflammatory external resorp-tion of the cementum from partially resorbed root apices (22, 23),only the intraradicular forms of internal root resorption will bediscussed in the rest of this article and will be simply referred to asinternal root resorption.

Etiology and PathogenesisOsteoclasts are motile, multinucleated giant cells that are respon-

sible for bone resorption. They are formed by the fusion of mononu-clear precursor cells of the monocyte-macrophage lineage derivedfrom the spleen or bone marrow, as opposed to osteoblasts and oste-ocytes that are derived from skeletal precursor cells (24–26). They arerecruited to the site of injury or irritation by the release of manyproinflammatory cytokines. To perform their function, osteoclastsmust attach themselves to the bone surface. Recent studies indicatedthat the polarity of osteoclasts is regulated by their actin cytoskeleton(27, 28). On contact with mineralized extracellular matrices, theactin cytoskeleton of an actively resorbing osteoclast is reorganizedto produce an organelle-free zone of sealing cytoplasm (clear zone)associated with the osteoclast’s cell membrane to enable it to achieveintimate contact with the hard tissue surface (29). The clear zonesurrounds a series of finger-like projections (podosomes) of cellmembrane known as the ruffled border. It is underneath this ruffledborder that bone resorption occurs. The resorptive area within the clearzone, therefore, is isolated from the extracellular environment, creatingan 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 differfrom osteoclasts by being smaller in size and having fewer nuclei andsmaller sealing zones possibly as result of differences in their respectiveresorption substrata (32). Osteoclasts and odontoclasts resorb theirtarget tissues in a similar manner (29). Both cells possess similar enzy-matic properties (33), and both create resorption depressions termedHowship’s lacunae on the surface of the mineralized tissues (Fig. 1)(29). Although mononuclear dendritic cells share a common hemato-poietic lineage with the multinucleated osteoclasts, they have previouslybeen regarded solely as immunologic defense cells. Recent studies indi-cated that immature dendritic cells function also as osteoclast precur-sors that have the potential to transdifferentiate into osteoclasts (34,35). Because dendritic cells are present in the dental pulp, it ispossible they might function also as precursors of odontoclasts.

From a molecular signaling perspective, the OPG/RANKL/RANK tran-scription factor system (36) that controls clastic functions during boneremodeling has also been identified in root resorption (37). The systemis responsible for the differentiation of clastic cells from their precursorsvia complex cell-cell interactions with osteoblastic stromal cells. Similar toperiodontal ligament cells that are responsible for external root resorp-tion (38), the human dental pulp has recently been shown to express os-teoprotegerin (OPG) and receptor activator of nuclear factor kappa Bligand (RANKL) mRNAs (39). Osteoprotegerin, a member of the tumornecrosis factor superfamily, has the ability to inhibit clast functions byacting as decoy receptors that bind to RANKL and reduce the affinity ofthe latter to RANK receptors on the surface of clastic precursors. This

results in inhibition of the regulation of clastic cell differentiation. Thus,it is possible that the OPG/RANKL/RANK system might be actively involvedin the differentiation of odontoclasts during internal root resorption.

It is known that osteoclasts do not adhere to nonmineralizedcollagenmatrices (40). It has been suggested that the presence of a non-collagenous, organic component within dentin (odontoblast layer andpredentin) prevents resorption of the root canal wall (41, 42). Similarto osteoclasts, odontoclasts might bind to extracellular proteinscontaining the RGD (arginine-glycine-aspartic acid) sequence ofamino acids via integrins (43). The latter are specific surface adhesionglycoprotein membrane receptors containing different a andb subunits. In particular, avb3 integrin plays a key role in the adhesionof clastic cells (44). Extracellular matrix proteins containing the RGDpeptide sequence present on the surface of mineralized tissues, inparticular osteopontin, serve as binding sites of clastic cells (45).The osteopontin molecule contains different domains, with one domainbinding to apatites in the denuded dentin and another domain bindingto integrin receptors in the plasma membranes of clastic cells. Thus,osteopontin serves as a linker molecule that optimizes the attachmentof a clastic cell to mineralized tissues, mediating the rearrangementof its actin cytoskeleton (46). It has been speculated that the lack ofRGD peptides in predentin reduces the binding of odontoclasts, therebyconferring resistance of the canal walls to internal root resorption.

For internal root resorption to occur, the outermost protectiveodontoblast layer and the predentin (Fig. 1) of the canal wall must bedamaged, resulting in exposure of the underlying mineralized dentin toodontoclasts (40, 47). The precise injurious events necessary to bringabout such damages have not been completely elucidated. Variousetiologic factors have been proposed for the loss of predentin,including trauma, caries and periodontal infections, excessive heatgenerated during restorative procedures on vital teeth, calciumhydroxide procedures, vital root resections, anachoresis, orthodontictreatment, cracked teeth, or simply idiopathic dystrophic changeswithin normal pulps (18, 20, 48–55). In a study of 25 teeth withinternal resorption, trauma was found to be the most commonpredisposing factor that was responsible for 45% of the casesexamined (16). The suggested etiologies in the other cases were inflam-mation as a result of carious lesions (25%) and carious/periodontallesions (14%). The cause of the internal resorption in the remaining teethwas unknown. Other reports in the literature also support the view thattrauma (18, 42, 56) and pulpal inflammation/infection (11, 56) are themajor contributory factors in the initiation of internal resorption.

Wedenberg and Lindskog (47) reported that internal root resorp-tion could be a transient or a progressive event. In an in vivo primatestudy, the root canals were accessed in 32 incisors with the predentinintentionally damaged. The access cavities in half of the teeth weresealed; the other half were left open to the oral cavity. The teeth wereextracted at intervals of 1, 2, 6, and 10 weeks. The authors notedonly a transient colonization of the damaged dentin by multinucleatedclastic cells in the teeth that had been sealed (ie, transient internalroot resorption). Those teeth were free from bacterial contamination,and no signs of active hard tissue resorption occurred. In the teeththat were left unsealed during the experimental period, there were signsof extensive bacterial contamination of pulpal tissue and dentinaltubules. Those teeth demonstrated extensive and prolonged coloniza-tion of the damaged dentin surface by clastic cells and signs of miner-alized tissue resorption (progressive internal root resorption). Damageto the odontoblast layer and predentin of the canal wall is a prerequisitefor the initiation of internal root resorption (42). However, the advance-ment of internal root resorption depends on bacterial stimulation of theclastic cells involved in hard tissue resorption (Fig. 2). Without thisstimulation, the resorption will be self-limiting (42).

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Figure 1. Light microscopy images of a case with early internal (root canal) inflammatory resorption. (a) Maxillary canine with caries penetrating the pulp. Thetooth was tender to percussion. There was no response to sensitivity tests. (b) Sections were taken along the buccolingual plane. Overview image shows cariousperforation and necrotic tissue in the root canal (Taylor’s modified Brown & Brenn [TBB]; original magnification,!2). (c) Coronal third of the root canal shownin (b). Dense bacterial biofilm was present on the canal walls. Necrotic tissue can be identified in the canal lumen (TBB; original magnification, !16). (d) Highmagnification of the area indicated by the arrow in (c). Dense aggregation of bacteria can be seen along the canal wall (TBB; original magnification, !400. Inset;original magnification,!1000). (e) Apical third of the root. Contrary to the histologic condition present in the coronal two thirds, the tissue was vital (hematoxylin-eosin [H&E]; original magnification, !25). (f) Magnification 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 magnification, !100). (g) Higher magnification of the upper lacuna in (f). Large multi-nucleated resorbing cell (odontoclast) and granulation tissue consisting of fibroblasts and chronic inflammatory cells can be seen (H&E; original magnification,!400). (h) High magnification view of the odontoclast showing multiple nuclei. The empty space is a shrinkage artifact (H&E; original magnification, !1000).

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For internal resorption to occur, the pulp tissue apical to theresorptive lesion must have a viable blood supply to provide clastic cellsand their nutrients, whereas the infected necrotic coronal pulp tissueprovides stimulation for those clastic cells (7) (Fig. 2). Bacteria mightenter the pulp canal through dentinal tubules, carious cavities, cracks,fractures, and lateral canals. In the absence of a bacterial stimulus, theresorption will be transient and might not advance to the stage that canbe diagnosed clinically and radiographically. Therefore, the pulp apicalto the site of resorption must be vital for the resorptive lesion to prog-ress (Fig. 1). If left untreated, internal resorption might continue untilthe inflamed connective tissue filling 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, andthe bacteria will infect the entire root canal system, resulting in apicalperiodontitis (57) (Fig. 2).

Histologic ManifestationsOur knowledge of the histologic manifestations of internal root

resorption in humans is based largely on the work of Wedenberg and

Zetterqvist (56). In that study, internal root resorption lesions inboth primary and permanent teeth were examined with light micros-copy, scanning electron microscopy, and enzyme histochemistry. Thestudy examined 6 primary and 7 permanent teeth that were extractedas a result of progressive internal resorption. The histologic appear-ance and histochemical profiles of the primary and permanent teethwere identical, but the resorption process generally occurred ata faster rate in the primary teeth. Pulpal tissues in all the teethwere inflamed to varying degrees, with the inflammatory infiltrateconsisting predominantly of lymphocytes and macrophages, withsome neutrophils. The inflammation was associated with dilatedblood vessels, and in 11 of the cases, bacteria were evident eitherin the necrotic coronal pulp tissue or within the dentinal tubulesadjacent to the lesion. The granulation tissue in the pulp cavities con-tained fewer blood vessels than in normal pulp tissue and resembledperiodontal connective tissues, with comparatively more cells andfibers. Indeed, the periodontal membrane was continuous with thetissue in the pulp cavities in all but 2 teeth through either the apicalforamen or perforations of the external root surfaces as a result ofthe resorption process. A distinguishing feature of all the lesions

Figure 2. Light microscopy images of a case with early internal (root canal) inflammatory resorption followed by necrosis and infection. (a) Periapical radiographshows a mandibular second premolar with gross caries and enlargement of the periodontal ligament. There was no response to sensitivity tests, and the tooth wasextremely sensitive to percussion. The buccal gingival tissues were swollen and fluctuant. The diagnosis was pulpal necrosis with acute apical abscess. After dis-cussing the various treatment options, the patient opted for extraction. (b) Sections were taken along the mesiodistal plane. Overview image shows that the distalcaries had penetrated the pulp space. Pulp tissue was necrotic (TBB; original magnification, !2). (c) Apical third. Main canal and ramifications were filled witha bacterial biofilm (TBB; original magnification, !16). (d) Higher magnification of the main canal in (c). Numerous resorptive defects were present on the rightroot canal walls and filled with bacteria (TBB; original magnification, !100). (e) High magnification of the upper lacuna in (d). Predentin was absent, and thecavity was occupied by a bacterial biofilm. Some polymorphonuclear leukocytes can be observed (TBB; original magnification,!400). (f) Resorption lacuna apicalto that shown in (e) (TBB; original magnification,!400). (g) High magnification taken from the left canal wall of the apical canal. Despite the presence of necroticpulp tissue along the root canal wall, predentin was intact at this level, and no resorption can be seen (H&E; original magnification, !400).

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examined was the presence of numerous, large, multinucleatedodontoclasts occupying resorption lacunae on the canal walls. Theodontoclasts displayed evidence of active resorption and wereaccompanied by mononuclear inflammatory cells in the adjacentconnective tissue. Both types of cell displayed tartrate-resistant acidphosphatase activity. There were no predentin or odontoblasts onthe dentinal walls.

Of interest was the presence of a metaplastic mineralized tissuethat resembled bone or cementum. The metaplastic mineralized tissuesincompletely lined the pulp cavity in all cases, and islands of calcifiedtissues were identified from the pulp in 3 teeth. Similar metaplasticmineralized tissues were reported by Cvek (58) and Cvek et al (59),with ‘‘ankylosis of the canal walls’’ similar to what was observed alongthe external root surfaces. On the basis of those results, 2 types ofinternal root resorption were described by Ne et al (60) and Heithersay(61), internal (root canal) inflammatory resorption and internal (rootcanal) replacement resorption. The prefixes ‘‘internal’’ and ‘‘rootcanal’’ were used to delineate these entities from similar observationsin external root resorption.

Internal (Root Canal) Inflammatory ResorptionThis type of resorption might occur in any area of the root canal

system. It is characterized by the radiographic appearance of an oval-shaped enlargement within the pulp chamber (Fig. 3). The conditionmight go unnoticed until the lesion has advanced significantly, result-ing in a perforation (62) or symptoms of acute or chronic apical pe-riodontitis after the entire pulp has undergone necrosis and the pulpspace has become infected. If resorption occurs in the coronalportion of the tooth, the latter might exhibit a pinkish hue that is clas-sically described as the pink tooth of Mummery after the 19th centuryanatomist James Howard Mummery (63), who first reported thephenomenon.

Internal root canal inflammatory resorption involves a progressiveloss of intraradicular dentin without adjunctive deposition of hardtissues adjacent to the resorptive sites (Figs. 1–3). It is frequentlyassociated with chronic pulpal inflammation, and bacteria might beidentified from the granulation tissues when the lesion is progressiveto the extent that it is identifiable with routine radiographs (47)(Fig. 3). Although chronic inflammation is commonly present in pulpal

Figure 3. Light microscopy images of a case with internal (root canal) inflammatory resorption. (a) Radiograph of a nonrestorable grossly carious mandibularmolar. 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 thedistal root, taken from a mesiodistal plane. The defect appears empty, except for some debris present in its apical extension (H&E; original magnification,!16). (c)High magnification of the area from the right wall indicated by the arrow in (b). Resorption lacunae appear empty; no multinucleated cells are visible (H&E; originalmagnification, !400). (d) Section taken approximately 60 sections after that shown in (b). Necrotic tissues can be seen at the transition between the resorptionarea and the apical canal followed by a concentration of cells (TBB; original magnification,!50). (e) High magnification of the area demarcated by the rectangle in(d), showing the transition between necrotic tissue with bacterial colonies and an area of acute inflammation (TBB; original magnification,!400). (f) High magni-fication of the area indicated by the arrow at the center of the cellular accumulation in (d). Dense aggregation of polymorphonuclear leukocytes can be identified(TBB; original magnification, !400). (Reprinted with permission from Ricucci D. Patologia e Clinica Endodontica. Edizioni Martina, Bologna, Italy, 2009).

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infections, it alone does not provide the conditions necessary for medi-ating root canal inflammatory resorption. Other conditions must bepresent simultaneously to initiate the event; for example, conditionsmust prevail for the recruitment and activation of odontoclast precur-sors within the dental pulp, and the adjacent odontoblast layer and pre-dentin must be disrupted (64) for those activated clastic cells to adhereto the intraradicular mineralized dentin (Fig. 1). This probably explainswhy root canal inflammatory resorption is less frequently observed thanexternal inflammatory root resorption (EIRR). The coronal part of thepulp is usually necrotic, whereas the apical part of the pulp must remainvital for the resorptive lesion to progress and enlarge (Fig. 1). Onehypothesis suggests that the necrotic coronal part of the infected pulpprovides a stimulus for inflammation in the apical part of the pulp.An alternative hypothesis is based on the recent understanding that oste-ocytes participate in bone homeostasis by inhibiting osteoclastogenesis(65). In the presence of living osteocytes, osteoclasts fail to produceactin rings, which are the hallmark of active resorbing cells. Conversely,apoptosis of osteocytes induces the secretion of osteoclastogenic cyto-kines that trigger bone resorption (66, 67). Similar to osteocytes, dentalpulp cells and odontoblasts undergo apoptosis during toothdevelopment as well as in response to certain types of injury (68–71). Thus, it is possible that odontoblasts or pulpal fibroblastsundergoing apoptosis as a result of trauma or caries producecytokines that initiate an internal resorptive response in the apicalpart of the pulp. Internal resorption only occurs when the predentinadjacent to the site of chronic inflammation is lost as a result oftrauma (56) or other unknown etiologic factors.

Internal (Root Canal) Replacement ResorptionInternal root canal replacement resorption is characterized by an

irregular radiographic enlargement of the pulp chamber, with discon-tinuity of the normal canal space (72). Because the resorption processis initiated within the root canal, the defect includes part of the canalspace, and hence the outline of the original canal appears distorted.The enlarged canal space appeared radiographically to be obliteratedby a fuzzy-appearing material of mild to moderate radiodensity(Fig. 4). This form of resorption is typically asymptomatic, and theaffected teeth might respond normally to thermal and/or electric pulptesting unless the resorptive process results in crown or root perfora-tion (60). Root canal replacement resorption appears to be caused bya low-grade inflammation of the pulpal tissues such as chronic irrevers-ible pulpitis or partial necrosis. Similar to root canal inflammatoryresorption, the chronic inflammatory processmust occur along a regionof the canal wall in which the odontoblast layer and the predentin aredisrupted or damaged before the resorption component of the condi-tion commences (56), because odontoblasts have to bind to extracel-lular proteins containing the RGD amino acid sequence.Histologically, resorption of the intraradicular dentin is accompaniedby subsequent deposition of a metaplastic hard tissue that resemblesbone or cementum instead of dentin (Fig. 4). Metaplasia refers toa reversible change in which one adult cell type (epithelial ormesenchymal) is replaced by another cell type (73). In the presentcontext, the metaplastic tissue appears lamella-like, with entrappedosteocyte-like cells that resemble osteons of compact bone (Fig. 4).

A variant of internal root canal replacement resorption has previ-ously been reported as ‘‘internal tunnelling resorption’’ (74). This entityis usually found in the coronal portion of root fractures but might alsobe seen after luxation injuries. The resorption process tunnels into thedentin adjacent to the root canal, with concomitant deposition of bone-like tissues in some regions. These bone-like tissues have the appear-ance of cancellous bone instead of compact bone (Fig. 5). The process

might subsequently arrest and might be followed by complete oblitera-tion of the canal space by cancellous bone.

Different hypotheses have been proposed regarding the origin ofthe metaplastic hard tissues that are formed within the canal space.The first hypothesis suggests that the metaplastic tissues are producedby postnatal dental pulp stem cells (75, 76) present in the apical,vital part of the root canal as a reparative response to the resorptiveinsult. This is analogous to the formation of tertiary reparative dentinby odontoblast-like cells after the death of the primary odontoblasts(77). Unlike reactionary dentinogenesis, dentin repair studies haveshown that the matrix deposited during reparative dentinogenesisdemonstrates a high degree of heterogeneity. Following the depletionof epithelial-mesenchymal interactions that occur in primary dentino-genesis, the matrix deposited in reparative dentinogenesis often resem-bles osteoid instead of tubular dentin (78–80). Odontoblasts arepostmitotic cells that are incapable of cell division following theirterminal differentiation. Despite the advances in our understanding ofthe molecular signaling that determines cell fate during toothmorphogenesis and regeneration (81, 82), the precise cross-talk mech-anisms that determine the commitment of mesenchymal progenitor cellsto a definitive odontoblast lineage (as opposed to the osteoblast lineage)remain ambiguous at large (83, 84). In the absence of highly specificepigenetically derived signals required for lineage diversification anddifferentiation of ’’true’’ odontoblasts in an adult tooth, multipotentstem cells engaged in the process of reparative dentin formationretain the osteoblastic phenotype and secrete a matrix that moreresembles bone than dentin. These histologic observations appear tobe supported by the results of a recent article that involved the use ofgene therapy to introduce a growth factor into dental pulp stem cells(85). In that study, the newly formed hard tissue resembled bone ratherthan dentin, with concentric lamellae of mineralized matrix entrappingosteocyte-like cells. In addition, a bone marrow–like hematopoietictissue could be identified within the newly formed hard tissues. Thus,it is possible that a similar phenomenon occurs during the formationof metaplastic tissues in root canal replacement resorption.

The second hypothesis proposes that both the granulation tissuesand metaplastic hard tissues are of nonpulpal origin. Those tissues mightbe derived from cells that transmigrated from the vascular compartmentsor originated from the periodontium (86). This hypothesis suggests thatin internal resorption, the pulpal tissues are replaced by periodontium-like connective tissues. Such a scenario is analogous to what occursduring ingrowth of connective tissues into the pulp space when a bloodclot became available (87–89) or, more recently, after pulpalrevascularization procedures (90, 91). Indeed, the histologic featuresof heavy inflammatory infiltrates and bone/cementum-like metaplastictissues formation in root canal replacement resorption are highly reminis-cent of similar unresolved lymphocyte infiltration and intracanalcementum-like hard tissue deposition in experimental revascularizationprocedures 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 filled with bone/cementum-like tissues are as strong as teeth with canal walls supportedby intact intraradicular tubular dentin. Although root fracture associatedwith internal resorption had been reported (93), the absence of histologicbackup and the paucity of such reports preclude evidence-based conclu-sions to be drawn regarding the correlation between teeth with histories ofroot canal replacement resorption and their fracture resistance.

Differential DiagnosisThe manner in which internal root resorption presents clinically

depends, to a degree, on the nature and position of the lesion within

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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 wasreferred to the first 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 sugges-tive of internal root resorption with metaplasia. (b) Radiograph of the tooth after extraction taken at 90-degree angle to the clinical radiograph showing the conti-nuity of the resorptive lesion with the canal space. (c) Cross section taken approximately at the level of line 1 in (b). Low magnification overview shows that thedentin 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 magnification,!8). (d) Higher magnification of (c) (H&E; original magnification,!16). (e) High magnification of the area demarcated by the rectanglein (d). The intraradicular dentin has been resorbed (H&E; original magnification,!100). (f) High magnification taken from the right part of (c) showing that theresorbed dentin has been substituted by lamellar bone. Osteocytes are present in lacunae between the lamellae. A characteristic cross section of an osteon can beseen on the right (open arrows), with concentric lamellae surrounding a vascular structure (H&E; original magnification, !100). (g) High magnification of thearea indicated by the left open arrow in (e). A multinucleated resorbing cell (odontoclast) can be seen in a dentinal lacuna, indicating active resorption of thedentinal wall (H&E; original magnification, !1000). (h) High magnification view of the bone surface indicated by the right arrow in (e). The large cells areosteoblast-like cells. Once they produced mineralized tissue, they were embedded in the bone lacunae, assuming the characteristics of osteocytes (H&E; originalmagnification,!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 relativelythin layer of newly formed bone (H&E; original magnification, !16). (j) Cross section taken approximately at the level of line 3 in (b). At this level the root canalappears consistently narrowed by a dense layer of newly formed bone (H&E; original magnification, !16).

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the tooth. If the pulp is still partially vital, the patient might experiencesymptoms of pulpitis. However, if the resorption is no longer active andthe entire pulp has become necrotic, the patient might eventuallydevelop symptoms of apical periodontitis. Sinus tracts might be detectedclinically, which might be indicative of root perforation or chronicapical abscess. A pink discoloration might be visible through the crownof the tooth as a result of internal root resorption in the coronal third ofthe root canal. The pink spot is caused by granulation tissue undermin-ing the necrotic area of coronal pulp. Traditionally, the pink spot ofMummery has been thought to be pathognomonic of internal rootresorption. However, these pink spots are more commonly associatedwith ECR (12). Thus, differential diagnosis of internal root resorptioncannot be based solely on the observation of pink spots. In manyinstances, there are no clinical signs, and the teeth that exhibit internalroot resorption are asymptomatic. Given the varied manner in whichinternal root resorption might present clinically, the diagnosis of thecondition is primarily based on radiographic examination, with supple-mentary information gained from history and clinical findings (10).

The difficulty in distinguishing internal resorption from ECR hasbeen highlighted in the literature (7, 10, 94). The problem indiagnosis occurs when the ECR lesion is not accessible by probingand is projected radiologically over the root canal. Both lesionsmight have a similar radiographic appearance (Fig. 6). Gartner et al(95) described guidelines that enable clinicians to differentiate the 2processes radiographically. The authors reported internal root resorp-tion lesions to be smooth and generally symmetrically distributed overthe root. They described the radiolucency of the internal root resorptionas having a uniform density. The pulp chamber or root canal outlinecould not be followed through the lesion, because the canal walls essen-

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-definedand asymmetrical, with radiodensity variations in the body of the lesion.The canal wall should be traceable through the ECR lesion because thelatter is superimposed over the root canal (95–98).

The use of parallax radiographic techniques is advocated for differ-entiating internal from external resorption defects (10, 94, 95). Asecond radiograph taken at a different angle often confirms the natureof the resorptive lesion. ECR lesions will move in the same directionas the x-ray tube shift if they are lingually/palatally positioned. Theywill move in the opposite direction to the tube shift if they arebuccally positioned. Conversely, internal root resorption lesionsshould remain in the same position relative to the canal in bothradiographs (Fig. 7). Radiologically, internal (root canal) replacementresorption presents as a cloudy, mottled, radiopaque lesion with irreg-ular margins (Fig. 8) as a result of the presence of metaplastic hardtissue deposits within the canal space. Differentiating internal (rootcanal) replacement resorption from ECRmight be clinically challenging,especially if the metaplasia has occupied the entire resorptive cavity.

Diagnostic accuracy based on conventional and digital radio-graphic examination is limited by the fact that the images producedby these techniques only provide a 2-dimensional representation of3-dimensional objects (94, 99, 100). In addition, the anatomicstructures being imaged might be distorted (101). This might lead tomisdiagnosis and incorrect treatment in the management of internalroot resorption and ECR.

The advent of cone beam computed tomography (CBCT) hasenhanced radiographic diagnosis (102, 103). The use of CBCT

Figure 4. (continued).

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Figure 5. Light microscopy images of a variant of internal (root canal) replacement resorption with tunneling resorption. Lower right lateral incisor was derivedfrom a 39-year-old former boxer who suffered from jaw fracture during a boxing match in his early twenties and was placed in intermaxillary fixation. The patientdeveloped symptoms 20 years later and complained of pain associated with his lower incisors. (a) Radiograph of the mandibular right incisors. Lower right centralincisor had asymptomatic apical periodontitis associated with a necrotic and infected pulp. Lower right lateral incisor showed a large area of internal root resorp-tion. The tooth did not respond to sensitivity tests. (b) Sagittal CBCT slice shows some calcified tissue in the resorptive defect. (c) Cross section taken at the level ofline 1 in (a, b). Overview shows that the canal was apparently empty at this level (H&E; original magnification,!6). (d) High magnification of the area indicated bythe arrow in (c). Lamellar bone fills an area of previous resorption. Note the osteon structure (arrow) (H&E; original magnification, !100). (e) Cross sectiontaken 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; originalmagnification, !8). (f) High magnification of the lower part in (e) (H&E; original magnification, !50). (g) Higher magnification of (f). Bone trabeculae sur-rounded by necrotic debris (H&E; original magnification,!100). (h) Cross section taken from the same area as that in (e) (TBB; original magnification,!16). (i)High magnification 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 magnification, !100. Inset; original magnification, !1000). (j) Longitudinal section passing approximately through the center of the root apex. Dentinwalls had been resorbed and substituted by a bone-like tissue (H&E; original magnification, !16).

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provides greater 3-dimensional geometric accuracy when comparedwith conventional radiography (104). Several case reports and caseseries have confirmed the usefulness of CBCT in diagnosing andmanaging resorptive lesions (105, 106). Sensitivity and specificity,which are defined as the number of true positive decisions/thenumber of actually positive cases and the number of true negative

decisions/the number of actually negative cases, respectively, constitutethe basic measures of performance of diagnostic tests. The receiveroperating characteristic (ROC) curve, which is defined as a plot of testsensitivity versus its specificity, is a well-accepted method of evaluatingthe quality or performance of diagnostic tests. The area under an ROCcurve that has been fit by the conventional binormal model (Az) is widelyused as an index of diagnostic performance (107). Recently, Patel et al(98) compared the accuracy of intraoral periapical radiography withCBCT for the detection and management of root resorption lesions.ROC Az values for correctly diagnosing internal root resorption with in-traoral radiography were satisfactory (0.78). However, CBCT resulted ina perfect diagnosis (Az 1.00). The authors concluded that the superioraccuracy of CBCT warrants reassessment of the use of conventionalradiographic 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 apprecia-tion of the tooth, the resorption lesion, and the adjacent anatomy. Thetrue nature of the lesion might be assessed, including root perforationsand whether the lesion is amendable to treatment (Figs. 7 and 8). In thesame study (98), the authors concluded that there was a significantlyhigher prevalence in the choice of the correct treatment option whenCBCT was used compared with the use of intraoral radiographs for diag-nosing 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 isdeemed restorable and has a reasonable prognosis, root canal treatmentis the treatment of choice. The aim of root canal treatment is to removeany remaining vital, apical tissue and the necrotic coronal portion of thepulp that might be sustaining and stimulating the resorbing cells via theirblood supply, and to disinfect and obturate the root canal system (108).

Internal root resorption lesions present the endodontist withunique difficulties in the preparation and obturation of the affectedtooth. Access cavity preparation should be conservative, preserving asmuch tooth structure as possible, and should avoid further weakeningof the already compromised tooth. In teeth with actively resorbinglesions, bleeding from the inflamed pulpal and granulation tissuesmight be profuse and might impair visibility during the initial stagesof chemomechanical debridement. The shape of the resorption defectusually renders it inaccessible to direct mechanical instrumentation.

Chemomechanical Debridement of the Root CanalThe principal cause of persistent apical periodontitis might be

attributed to microorganisms remaining within the canal after root canaltreatment (109–112). Root canals have complex morphology thatharbors bacteria. Despite advances in endodontic techniques,instruments and irrigants fail to predictably access the restricted areasof the canal space (113–116). The use of ultrasonic instruments toagitate the irrigant has been shown to improve the removal of necroticdebris and biofilms from inaccessible areas of the root canal (117).Ultrasonic activation of irrigants after mechanical preparation of rootcanals has been shown to reduce the number of bacteria. Given the inac-cessibility of internal root resorption lesions to chemomechanicaldebridement, ultrasonic activation of irrigants should be viewed as anessential step in the disinfection of the internal resorption defect.However, even with the use of ultrasonic instruments, bacteria might stillremain in confined areas (117). Chemomechanical debridement ofthe root canal space fails to consistently render the root canal systembacteria-free (118–122). Thus, an intracanal, antibacterial medica-ment should be used to improve disinfection of the inaccessible root

Figure 6. (a) Clinical examination reveals that the mandibular left centralincisor tooth was discolored and nonresponsive to sensitivity testing. (b)Two periapical radiographs taken at different horizontal angles confirm theresorptive lesion is labially positioned by using the parallax principle; theroot canal outline is still visible through the lesion, indicating that the lesionis ECR. (c, d) Sagittal and axial CBCT slices show that the lesion is actuallyinternal root resorption, which is located at the periphery of the root canal.True nature of the resorptive lesion could only be assessed with CBCT. (Re-printed with permission from Patel S. New dimensions in endodontic imaging:part 2—cone beam computed tomography. Int Endod J 2009;42:463–75).

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resorption defects (114). Calcium hydroxide is antibacterial and hasbeen shown to effectively eradicate bacteria that persist after chemome-chanical instrumentation (123, 124). Calcium hydroxide has also beenshown to have a synergistic effect when used in conjunction withsodium hypochlorite to remove organic debris from the root canal(125, 126). Nevertheless, some case reports demonstrated the inabilityof calcium hydroxide to eliminate bacteria in ramifications because ofits low solubility and inactivation by dentin, tissue fluids, and organicmatter (127, 128). Despite these limitations, the use of multiplecalcium hydroxide dressings has been advocated to enhancechemomechanical debridement of the internal root resorption defect.

Obturation of the Root CanalThe primary objective of root canal treatment is to disinfect the root

canal system. This is followed by obturation of the disinfected canal withan appropriate root-filling material to prevent it from reinfection. By theirvery nature, internal root resorption defects can be difficult to obturate

adequately. To completely seal the resorptive defect, the obturation mate-rial should be flowable. Gutta-percha is the most commonly used fillingmaterial in endodontics. Gencoglu et al (129) examined the quality ofroot fillings in teeth with artificially created internal resorptive cavities.They found that the Microseal (Sybron Endo, Orange, CA) and ObturaII (Spartan, Fenton, MO) thermoplastic gutta-percha techniques weresignificantly better in filling artificial resorptive cavities than Thermafil(Dentsply, York, PA), Soft-Core core systems (CMS Dental, Copenhagen,Denmark), and cold lateral condensation (CLC). The CLC techniqueproduced slightly fewer voids than Obtura II, but a larger proportionof the canal space was filled with sealer with this technique. Goldmanet al (130) also concluded that the Obtura II system performed statisti-cally better in obturating resorptive defects than CLC, Thermafil, anda hybrid technique. Stamos and Stamos (131) reported 2 cases of internalroot resorption in which the Obtura II system was used to successfullyobturate the canals. Similar conclusions were reached by others (132).

In situations when the root wall has been perforated, mineraltrioxide aggregate (MTA) should be considered the material of choice

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 nearlyperforated the root wall. (e) The tooth has been obturated with gutta-percha by using a thermoplasticized technique.

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to seal the perforation. MTA is biocompatible (133) and has beenshown to be effective in repairing furcation perforations (134) andlateral root perforations (135). The material is well-tolerated by peri-radicular tissues and has been shown to support almost completeregeneration of the periodontium (134). In addition, MTA has superiorsealing properties when compared with other materials (136). A hybridtechnique might also be used to obturate canals; the canal apical to theresorption defect is obturated with gutta-percha, and then the resorp-tion defect and associated perforation are sealed with MTA (137,138). When internal resorption has rendered the tooth untreatableor 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 resorp-tive defect is the result of an inflamed pulp and the clastic precursor cellsare predominantly recruited through the blood vessels, controlling theprocess of internal root resorption is conceptually easy, via severingthe blood supply to the resorbing tissues with conventional root canaltherapy. With that said, early detection and a correct differential diag-nosis are essential for successful management of the outcome of internalresorption to prevent overweakening of the remaining root structuresand root perforations. The advent of CBCT no doubt has improved theclinician’s diagnostic capability for internal root resorption. Neverthe-

less, internal root resorption is often asymptomatic, and painful symp-toms do not appear until an advanced stage of the lesion. Thus, theclinician’s ability to detect this pathologic entity must rely heavily onthe use of radiographs in routine oral examinations. Although the adventof CBCT provides an important adjunctive diagnostic tool for differenti-ating between internal root resorption and ECR, it does not break newground from a treatment perspective. Irrespective of whether the lesionis manifested histologically as the inflammatory or the replacement formof the disease, the ultimate treatment of choice for those prognosticallyfavorable teeth is still nonsurgical root canal therapy.

Although this pathologic condition has been reported for morethan a century, our knowledge on the pathogenesis of this disease is,unfortunately, surprisingly thin. The majority of the documentationthat existed in the literature is in the form of case reports, and thereare only a limited number of studies that examined the histologic mani-festations and biologic aspects of the disease. In particular, the patho-genesis aspects of this disease still contain a high degree of uncertainty,with much of the information adapted from our understanding ofexternal root resorption. This might be due, in part, to the relativelyrare occurrence of this type of resorption and the lack of an in vivomodel, apart from the previous attempt on the use of diathermy, topredictably reproduce the condition for study.

From a histologic perspective, it appears that the disease might bemanifested as one form that is purely destructive, caused by inflamma-tion and elaborative clastic functions, and another form that is

Figure 8. (a, b) Radiographs reveal internal (root canal) replacement resorption of maxillary left central incisor; note the lesion remains centered with secondparallax view. (c) CBCT-reconstructed coronal (left) and axial (right) views of the tooth indicate that calcified 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 filling asso-ciated within the internal root resorption lesion. (e) 2-year review radiograph.

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accompanied by repair, albeit a ‘‘frustrated repair,’’ as a result of thedeposition of metaplastic bone/cementum-like tissues instead of truedentin. In the general scheme of things, the reparative form of thedisease exhibits histologic manifestations that are not so much differentto the manifestation of similar frustrated repairs in reparative dentino-genesis (eg, direct pulp capping; Ricucci et al, unpublished results,2009) and revascularization of nonvital dental pulps (92). Thereremains a wide gap of knowledge in our understanding of the condi-tions that precipitate the 2 different forms of internal root resorption.For example, it is not known whether one can alter the inflammatoryand microbial status of the involved pulp to shift the manifestation ofthe disease from a purely destructive form to one that is accompaniedby at least some form of repair. Such a notion might sound philosoph-ical to the practicing clinician. However, it might have an outreachingappeal to the molecular biologists and stem cell scientists within ourprofession in their quest for controlling the commitment of progenitorcell types capable of recapitulating the embryonic events in primaryodontogenesis as a future endodontic treatment strategy.

As the concept of pulpal regeneration becomes a foreseeablereality, it is prudent to elaborate on whether such a treatment strategymight be adaptable for the management of teeth with internal rootresorption. There are similarities and differences between the currentlyachievable status of pulpal revascularization and the replacement formof internal root resorption. The similarities are evident in the manifes-tations of frustrated repair by metaplastic hard tissues after the senes-cence of primary odontoblasts. The dental pulp is equipped with thepotential of regenerating odontoblast-like cells from dental pulpalstem cells through limited molecular signaling mechanisms after suc-cumbing of ectomesenchymal crosstalks that occur during primarydentinogenesis. Scientists are beginning to grasp the fundamentals ofthese intricate signaling mechanisms; however, control is still lackingin the ability to precisely delineate the odontoblastic lineage from theosteoblastic lineage. Nevertheless, the advances achieved so far havebeen phenomenal. After all, the creativity of evolution in which natureexplores all options and produces the best solution has taken millionsof years to bring to perfection. On the contrary, gene and stem cell ther-apies have only been proactive for more than 2 decades. Unlike pulpalrevascularization procedures, however, the onset of internal rootresorption is hallmarked by the recruitment of clastic precursors, theiractivation, and subsequent attachment to osteopontin-rich mineralizedmatrices. Thus, even if precise controls of signaling mechanisms for thedifferentiation of odontoblasts from their progenitor cells are available,additional strategies must be targeted at pacifying the activities of clasticcells at 1 of the 3 aforementioned stages (ie, recruitment, activation, andattachment). Although these tasks might appear formidable, it is at themolecular signaling level that one anticipates the greatest expansion ofhorizons. Advances in different scientific disciplines will enrich the poolof ideas for future therapeutic strategies, apart from conventional rootcanal therapy, in the treatment of internal root resorption. The scope ofdeepening this pool is tremendous.

AcknowledgmentsThe authors wish to thank Cavendish Imaging, London, UK,

and the Department of Dental & Maxillofacial Imaging, The DentalInstitute, Kings’ College London, London.

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internal root resorption- a review

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