Endodontics

Tooth résorptionRita F. Ne, DDSVDavid E. Witherspooti, BDSc, BEcon MSVJames L. Gutmafin, DDS*

Tooth résorption is a common sequela toitowing injuries to cr irritation ot the pericdontai ligament and/ortooth pulp The course ol tocth résorption involves an elaborate interaction among infiammatory celts, re-sorbing coils, and hard tissue structures. The i<ey ceils involved in résorption are of the dastic type, whichinclude osteobtasts and cdontoclasts. Types of tooth résorption include internal résorption and external ré-sorption. There are two types of internai résorption: root canal (internai) replacement résorption and in-ternai Intiammatory résorption. Externai résorption can be dassitied into four categories by its clinical andhistoiogic manitestations: external surface résorption, external inflammatory root résorption, replacementrésorption, and ankyiosis. External inflammatory root résorption can be further categorized into cervicalrésorption with or without a vital pulp (invasive cervical root résorption) and externai apical root résorption.Other variations ot résorption inciude combined internai and external résorption and transient apicalbreakdown (Quintessence Int 1999;30:9-25|

Key words: externai résorption, inflammatory résorption, internal résorption, odonfoclast, osteoclast,periodontal ligament, pulp, replacement résorption

"TJesorption is a condition associated with either aXVphysiologic or a pathologic process resulting in a

loss of dentin, cementum or bone."' Invariably, toothrésorption results from injuries to or irritation of theperiodontal ligament and/or tooth pulp. It may ariseas a sequela of traumatic luxation injuries, orthodontictooth movement, or chronic infections of the pulp orperiodontal structures.

The process of tooth résorption involves an elabo-rate interaction among inflammatory cells, resorbingcells, and hard tissue structures. Frequently, this patho-logic condition is difficult to predict, diagnose, andtreat.^ However, the process of tooth résorption is be-lieved to be very simiiar to that of bone résorption.'Injuries to and irritation of bone, dentin, or cementumleads to chemical changes within these tissues; the re-suit is the formation of multinucleated giant cells, re-ferred to as ctasts.^-^ The clastic ceil is the key cell typeresponsible for all hard tissue resorptive processes. It isjoined by cells such as macrophages and monocytes inresorptive activities. Collectively, these cells orcbes-trate a compiex interplay of molecular biologic events,involving cytokines, enzymes, and hormones, thai in-fluences the progression of résorption.^

'Department ot Restorative Sciences, Graduate Endodontics, Texas A S MUniversity Systern, Baylor Coliege of Dentisfry, Dallas, Texas.

Reprint requests: Dr David E. Witherspoon, tJepartment of ResforafiueSciences, Texas A S f University System, Baylor Coiiege of Denlistry, 33DSGasfon Avenue, Oaiiss, Te<as 752t4. E-mail: Dewspoon@tambcd.eclu

This articie is an introduction to the foilowing 3-part series on invasive cer-vical résorption by Dr Geottrey S. Heithersay

KEY CELLS AND FACTORS INVOLVED IN THEMECHANISMS OF RESORPTION

Monocytes and macrophages

Monocytes and macrophages, along with osteoclasts,play an important role in hone and tooth résorption.'^They are found in tissue sections adjacent to hone-resorbing surfaces of rheumatoid arthritis, periodontaldisease, periradicular granulomas and cysts, and inmetastatic bone tumors."" These ceils play a criticalrole in tbe deveiopment and healing of ail wounds,"-''

Initiaily, monocytes are recruited to the site of in-jury or irritation by tbe release of many pro-inflamma-tory cytokines. Subsequently, tbey differentiate intomacrophages, whose major role is wound debride-ment. Tbe migration and recruitment of macrophagesinto bone are regulated by macrophage chemotacticfactors that are derived from bone and tissue break-down products and are controlled by increased intra-cellular levels of adenosine 3,5-cyciic phosphate(cAMP) and calcium.'^" Aitbough macrophages havea structure similar to tbat of osteoclasts and, hke os-teoclasts, can also become muitinucieated giant cells,macropbages lack a ruffled border tbat is attached tohard tissue substrates during résorption and do notcreate lacunae on the dentinal surface.'^'^

Osteociasts

Osteoclasts arc hone-resorbing cells derived from he-mopoietic cells of tbe monocyte-macrophage lineage;

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Fig 1 Osteociast in IHowship laojnae(arrow). Bone (B] stained witii hematoxylinand eosin (originai magnification xiOO¡.

osteoclasts have a life span of approximately 2 weeks.The osteociast is a very active eell: it has the ability tomove between resorbing sites and is highly vacuolatedwith numerous mitochondria, indicating a high meta-bolic rate. It is a multinucleated giant ceil (20 to 30nuclei), formed from the fusion of mononuclear pre-cursor ceils that arrive at the site of résorption via thebloodstream. These precursor celis proliferate and dif-ferentiate into osteoclasts through a complex cell-ceilinteraction with osteoblastic stromal cells.

These eells arc characterized by speeialized mem-brane structures, clear zones, and ruffled borders. Thesize of the clear zone is indicative of the cell's resorb-ing activity and, in combination with the ruffled bor-der, is responsible for the process of résorption.'Osteoclasts are found in tiny depressions, pits, or ir-regular grooves, termed llowship lacunae, in cemen-tum, dentin, and bone^'^ (Fig 1).

Resorption mechanism. The unique structurai ar-rangement of the osteoeiasts to hard tissues ailows thecell to establish a microenvironment between the ruf-fled border and the bone in which résorption taiíesplace.^ The resorptive process itself ean be describedas being bimodal, involving the degradation of the in-organic crystal structure of hydroxyapatite and the or-ganie structure of collagen, principally type I.'' The ac-tivated osteoclasts produce an acidic pH (3.0 to 4,5) intheir mieroenvironment- At pH 5,0 or lower, the solu-bility of hydroxyapatite increases dramaticaily, and ré-sorption of hard tissue can occur. This acidic environ-ment is primarily achieved through the action of a

highly active polarized proton pump contained withinthe ruffled border.

The enzyme carbonic anhydrase 11 (CA II), which isspecific to osteoclasts, also plays a critical role in estab-lishing a subosteociastic acidic pH. The CA II catalyzesthe intracellular conversion of CO^ to H^CO , whichprovides a readily available source of H" ions to bepumped into the subosteociastic region. The critical na-ture of this enzyme to the resorptive process is high-lighted by osteoporosis, a disease characterized by a fail-ure to resorb bone and a congenital deficiency in CA II.

The degradation of the organic matrix is accom-piished by three groups of proteinase enzymes: coUa-genases and matrix metalloproteinases (iVlMP), whichact at neutral or just below neutral pH (7.4),'" and thecysteine proteinase family, which act at an acidic pH,'*The eysteine proteinases appear to work closer to theruffled border, where the pH is more acidic, while thecoUagenases appear to be active at the resorbing bonesurface, where the pH is closer to neutral because ofthe buffering capacity of the dissolving bone salts.Cysteine proteinases are secreted directly by the osteo-ciast into the clear zone via the ruffled border. Whilethe source ot the eollagcnascs remains in question, twopotentiai origins exist-the osteociast itself or the sur-rounding osteoblasts.' ' " Recent evidence suggests thatit may be a combination of both, with the osteociastresponsible for the secretion of MMP 9 in particular.''

Systemic regulatory factors. The major systemicregulatory factors of osteoclastic function includeparathyroid hormone (PTFÍ), 1,25-dihydroxyvitamin D,(l,25(OH)p,), and calcitonin (CT).'" Increases in thecirculating concentration of PTH promote bone résorp-tion by increasing both the number of cells present andthe rate of activity among individual eiastie cells. Theeffect of PTH appears to be muitifactorial: (1) stimula-tion of osteoblasts using a receptor-mediated, cAMP-dependent pathway to increase the produetion of neu-tral proteases and to decrease the amount of proteaseinhibitor and matrix deposition; f2J direct action on theosteociast to increase CA II activity by cAMP-mediatedphosphorylation of the enzyme; and (3) promotion ofthe fusion of marrow cells, leading to the formation ofmuitinucleated giant cell of osteoclastie phenotj/pe.

The major effect of l,25-dihydroxyvitamin D^ is toincrease the resorbing activity of osteoclasts alreadypresent, without increasing osteoelastic numbers. Theexact mechanism of action, however, remains unclear.

Calcitonin inhihits résorption by inhibiting cyto-plasmic motility and producing cell retraction. This ef-fect occurs at minimal concentration of CT and ishighly sensitive, prolonged, and modulated through aspecific receptor unique to the osteociast. ' ^ The in-hibitory action of ealcitonin has also been demon-strated on cells actively resorbing tooth

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Local regulatory factors. Osteoclasts are subject toextensive regulatory mechanisms that are facilitated toa large degree by osteoblasts mediating the effects ofosteotropic hormones and local mediators on thesecells. The presence of leukocyte antigens on the osteo-clast cell membrane favors the derivation of osteo-clasts and their precursors from the multipotentlalstem cells that produce peripheral blood leukocytes. ' *

Several local factors are key to osteoclastic forma-tion, regulation, and activation, including macrophagecolony-stimulating factor (M-CSF), interleukin 1 (IL-1), interleukin 6 (lL-6), interleukin 11 (IL-11), andtumor necrosis factor-alpha (TNF-a). Generally, thesecytokines stimulate development of osteoclasts whentested individually. However, in most cases, they re-quire cell-cell recognition among osteoblast cells, os-teoclast progenitors, and osteoclasts for formation andactivation. They are secreted from inflammatory cells(macrophages and polymorphonuclear neutrophilleukocytes) and osteoblasts as a result of stimulationby bacteria, tissue breakdown products, and the cy-tokines themselves.

Macrophage colony-stimulating factor is prohablythe most important soluble factor. It appears to benecessary not only for proliferation of osteoclast pro-genitor but also for the subsequent differentiation intomature osteoclasts and survival.

Interleukin 6 acts on osteoblastic stromal cells toinduce osteoclast differentiation factor, which recog-nizes osteoclastic progenitors and prepares them todifferentiate into mature osteoclasts. It has been foundthat IL-6 induces osteoclast-like cell formation inhuman marrow cultures^' and stimulates osteoclasticbone résorption in vivo. Serum levels of IL-6 are in-creased in several metabolic bone diseases.''

Interleukin 1 was one of the first bone-resorbing cy-tokines to be identified. It is active at all stages in os-teoclast formation, differentiation, and activation indi-rectly through the osteoblast. It increases résorptionlocally by stimulating the production and release ofprostaglandin E (PGE,) and acting directly on the os-teoclast. However, its action appears to be enhancedin the presence of IL-6.

The major effect of TNF-a on hard tissues is tostimulate osteoclastic activity. Like IL-1, PGE, andIL-6 mediate the effect of TNF-a.

Arachidonic acid metabolites, particularly prosta-glandin, are associated with diseases in which markedbone résorption is found, such as periodontal and peri-radicular disease, hypercalcemia of malignancy, andrheumatoid arthritis. Release of PGE, locally bychronic inflammatory cells simulates the formation ofosteoclasfs by enhancing fusion of osteoclastic precur-sors and increasing the resorbing activity of existingcells adjacent to mineralized tissue.'^

Bacteria play an important role in many destructivebone diseases. Likewise, bacteria are integral to theprocess of tooth résorption. Two possibilities exist forthe mechanism of bacteria-induced résorption: (1)bacteria produce acids and proteases that destroy thebone matrix cornponents, and (2) bacteria stimulatethe production of osteolytic factor, which promotesosteoclastic activity. In the case of tooth résorption,the overriding mechanism is likely to be induction ofosteolytic factors because of the effect of endotoxin(lipopolysaccharides). These substances represent theouter surface of the gram-negative bacteria. Lipopoly-saccharides stimulate a number of molecular biologicevents, including lysosomal enzyme release, collage-nase release from macrophages, and osteoblastic se-cretion of osteolytic factors IL-1, IL-6, M-CSE, andPGE,. ^ Together, these evetits result in the prolifera-tion of osteoclasts and enhanced bone résorption.However, with large amounts of endotoxin, osteoclas-tic responses decrease, sttggesting a toxic reaction.^"

Odontoclasts

It is unknown whether osteoclasts and tooth-resorbingcells (dentinoclasts, odontoclasts, and cementoclasts)are the same cell, but a number of similarities do exist.Odontoclasts are smaller, have a ruffled border, con-tain fewer nuclei than osteoclasts, and have smaller orno clear zone.'''^ Both cells have similar enzymaticproperties and intense tartrate-resistant acid phos-phatase activity. Their résorption patterns also appearto be the same mononuclear odontoclasts (4''/o ofodontoclasts) that participate in tooth résorption.However, the majority of odontoclasts (94%) thatform lacunae on the dentin are multinucleated, having10 or fewer nuclei. Oligonuclear odontoclasts (cellswith fewer than five nuclei) resorh more dentin pernucleus than do cells with a higher number of nuclei.'^

TYPES OF TOOTH RESORPTION

Tooth résorption is classified based on the site, nature,and pattern of the process, ' It is generally differenti-ated into internal and external résorption. Oc-casionally, combinations of both internal and externalrésorption can be found on the same tooth.

Internal résorption

Internal résorption is rare in permanent teeth. ' ' ' Inluxation injuries, it has been recorded as a sequela inapproximately 2''/o of recalled patients. However, it hasalso been reported in nontraumatized teeth. Typicallyasymptomatic, it is usually discovered during a routine

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Fig 2 internai intiammatory résorption and Figs 3a and 3b internai root replacement résorption (metapiastic résorption) with externalinternai replacement résorption: (1) intiammatory résorption at the apex. fLeflJ Radiographie appearance fR/g/if; Diagrammaticnecrotic puip; (2) vilai puip: (3) vitai pulp; description.¡4) internai inflammatory résorption; (5) in-ternai repiacement résorption.

radiographie evaluation and is often misdiagnosed asexternal résorption.^- There are two types of internalrésorption: root canal replacement résorption and in-ternal inflammatory résorption^ [Fig 2).

Root canal replacemetit résorption (metapiasticrésorption). Etiology. This disease process appears toresuit from a iow-grade irritation of pulpal tissue, suchas chronic irreversible pulpitis or partial necrosis, thatis usually localized to a stTiall area of tbe root canalsystem. ' Root eanal replaeement résorption involvesrésorption of tbe dentin and a subsequent depositionof hard tissue that resembles bone or cementum, butnot dentin. Tbis type of résorption takes place wben achronic inflammatory process occurs juxtaposed to aregion in wbieb tbe odontoblastie layer and predentinare absent or damaged, wbich can occur as a result oftrauma or application of extreme heat to the tootb.'-

Clinicai evaluation. This phenomenon is typicallyasymptomatic, and the affected teeth may respondwithin normal limits to thermal or electric pulp test-ing. ' The condition can become painful if tbe processperforates the root or crown of the tooth.

Radiographie evaluation. Internal replacement ré-sorption generally appears as enlargement of canalspace, including diseontinuity of the normal eanalspace. This space is then engorged with a less radio-dense material, giving the appearance of partial canalobliteration (Figs 3 and 4).

Histologie evaluation. There is a gradual enlarge-ment of the pulp space because of continuous forma-tion of bone or osteodentin at tbe expense of dentin.The normal pulpal tissue is replaced by a cancelloustype of hard tissue.

Variations. Internal tunneling résorption is usuallycaused by luxation injuries. Evidence of résorptionmay be found on a coronal fragment of root fracturein whieb a tunneling résorption process occurs next totbe root canal. Resorptive processes may be arrested,or complete pulp canal obliteration may take place.

Treatment. Once internal résorption is diagnosed,treatment witb nonsurgical root canal therapy is nec-essary. It is critical that the pulp and granulation tis-sue with odontoclasts be removed to arrest theprocess.^'

Internal inflammatory résorption. Etiology. Thistype of résorption involves a progressive loss of rootsubstance without deposition of hard tissue in the ré-sorption cavity.- It frequently results from chronic in-flammation of the pulp." The progression of inflam-matory résorption is dependent on the interactionbetween vital pulp tissue and necrotic tissue.^ Chronicirritation of pulpal tissues occurs wben bacteria andtbeir eomponents enter root canals via dentinaltubules that are exposed by tneebanical damage.'^Bacteria can also enter tbe canals at areas of dilacera-tion or cracks in tbe cervical area of the root.

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Figs 4a and 4b nvr' iai root repiacement résorption (metapiastic résorption). (Lett)Radiograpnic appea-arcs (Right) Diagrammatic description

Most commonly, internal résorption is found in thecervical region; however, it can occur in all areas ofthe root canal system. Areas of internal roof résorp-tion usually seem shallow.'^ Infrequently, in root-filledteeth, bacteria present in the root canal may commu-nicate with the periodontium via an accessory canal,from which soft fissue may proliferate into the rootcanal and resorh contaminated dentin.^

Clinicai evaluation. As in root canal replacementrésorption, internal inflammatory résorption is gener-ally asymptomatic and is usually identified on routineradiographs. The process of résorption is active only ifpart of the pulp remains vital; therefore, pulp testingcan he positive. However, usually the coronal pulp isnecrotic while the apical pulp is vital, resulting in anonresponsive test." Pain may he present if perfora-fion of the crown or root occurs." If résorption takesplace in the coronal portion of the tooth, the toothmay exhibit a pinkish or reddish hue because of thepresence of numerous capillaries in the pulpal granu-lation tissue undermining the coronal enamel.'^

Internal inflammatory résorption can be transientor progressive. The transient type of résorption occursfrequently in traumatized teeth or in teeth that haveundergone orthodontic or periodontal treatment. Incase of progressive internal inflammatory résorption,the dentinai tubules have a special and fortuitouscourse. These tubules must open to an area of the root

canal where the tissue is necrotic and infected, so thatmicroorganisms may enter the tubules and lead to anarea of canal with vital pulpal tissue. The resorptivearea and the root canal apical to this area contain vitaltissue that is necessary for the résorption to continue. ''

Radiographie evaluation. Internal inflammatory ré-sorption appears as a circumscribed, ova! enlargernent(radiolucency) continuous with the root canal wall,usually in the coronal cr radicular portion of thetooth.- ' ' Labially or lingually located external rootsurface résorption may have a similar appearance;therefore, additional radiographs, taken from mesialand distal angles, are recommended to locate the areain question^' (Figs 5 and 6).

Histologie evaluation. Normal pulpal tissue ispresent. This transforms into granulomatous tissuewith giant cells that resorb the predentin of the rootcanal. A necrotic zone containing bacteria is usuallyfound coronal to resorbing tissue.^'"'*

Treatment. Nonsurgical root canal therapy is rec-ommended, unless the résorption cavity is In the vicin-ity of the apical foramen and suspected of being re-lated to pulpal revascularization.-'^' Failure to treatinternal inflammatory résorption can lead to its even-tual extension to the periodontal ligatnent, via a crownor root perforation.'^ In these cases, a periodontal pro-cedure, such as crown lengthening or root extrusion,may be implemented to gain access for repair.

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Figs 5a and 5b internai .niiammatoiy résorption. ¡Lett) Radiogiaptiic appearance. (Right)Diagrammatic descnption.

Externai résorption of teeth

Externai résorption can be classified into four cate-gories by the ciinicai and histoiogic manifestations: ex-ternal surface résorption, external inflammatory rootrésorption, ankylosis, and replacement résorption(Figs 7 and 8). In addition to these four categories, ex-ternal résorptions are often described according totheir iocation on tbe tootb; cervix, body, or apex ofthe tooth. As a general ruie, external résorption can bedifferentiated from internal résorption by its radio-graphic presentation. Tbe resorptive radioiucenciesare superimposed over the root canai system.

External surface résorption. Externai surface ré-sorption is a transient phenomenon in which the rootsurface undergoes spontaneous destruction and repair.It is found in all teeth, in varying degrees, and is likelyto be a normal physiologic response.'' It is the least de-structive form of external root résorption and Is a self-limiting process; hence, it requires no treatment.-"

Etiology. External surface résorption occurs as a re-sponse to indirect physical injury, caused by physio-logic function, to localized areas of periodontal liga-ment or cementum on root surface. In cases oftrauma, it occurs because of direct mechanical contactof tbe root surface and alveoiar bone proper. It can beconsidered as part of the repair process of physicallydamaged calcified tissue by recruitment of cells fromadjacent normal tissue. *

Clinical evaluation. No significant signs of externalsurface résorption are detectable on the supragingivalportion of the tooth.

Radiographie evaluation. External surfaee résorp-tion is usually not visible on radiographs because of itssmall size. However, when visibie, it appears as smallexcavations on the root surface with nortnal laminadura and periodontal space. These excavations ean befound on the lateral surface of tbe root or at tbe apex,resulting in the appearance of shorter roots.

Histoiogic evaluation. External surface résorptionoccurs as small, superficial lacunae in the cementumand the outermost layer of dentin, which is simultane-ously being repaired with new cementum. While thereis generally no significant inflammatory reaction in theadjacent periodontal ligament, it can occur in areas oflocalized necrosis of the periodontal ligament andwhere cementoblasts are damaged.'^

Treatment. No treatment is indicated."External intiammatory root résorption (EIRR).

This represents tbe most common type of externairoot résorption. It is best described as a bowl-shapedresorptive defect that penetrates dentin.'*

Etiology. Several etiologic factors have been found tocause external inflamtnatory root résorption. In general,injury to or irritation of the periodontium from trauma,periodontal infection, or orthodontic treatmenf initiatesan inflammatory response within the periodontal liga-ment and leads to résorption.'^ External inflammatory

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Figs 6a and 6b Internai inflammatory résorption (Left) Radiograpiiic appearanceDiagrammatic description

Fig 7 External inflammatory root résorptionat the cervical and apicai areas of the tootiiwhen the pulp is vital: (1] vitai pulp; (2) ex-ternai inflammatciy root lesorptioh al thecervicai area: (3) externai inliammatory rootrésorption al the apicai area.

Fig 8 Externai infiammatory root résorptionat tlie cervicai areas ot tine toolh with exter-nal replacement résorption and ankyiosiswhen the puip is necrotic: (1) necrotic puip;(2) external inliammatoiy root rescrption atthe cervicai area: (3¡ externai repiacementrésorption; (4] ankyiosis.

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Figs 9a and 9b Externai intiammalory root résorption (Left) Radiograptiic appearance.(flight) Diagrammatic description.

root résorption can occur on any part of the root; how-ever, it is frequently subcategorized according to thatpart of the tooth to which it has occurred.

The most common cause of external inflammatoryroot résorption is trauma, particularly in cases wherethe injury results in pulpal necrosis and damage to theroot surface, leaving dentinal tubules exposed. Thiscreates a communication between the internal and ex-ternal surfaces of the root. Bacteria, bacterial by-prod-ucts, and tissue breakdown products from within theroot canal system stimulate inflammation in the adja-cent periodontal tissue and lead to aggressive progres-sive inflammatory résorption of the root.

Pressure has also been hypothesized as a possibleetiologic agent of external inflatnmatory root résorp-tion, as evidenced by résorption that transpires inorthodontic tooth movement, tooth eruption, bone le-sions, tumors, cysts. Impacted teeth, and occlusaltrauma. In these cases, résorption tends to cease whenthe source of pressure is removed from the root sur-face'i (Eigs 9a and 9b).

1. Cervical. External inflammatory root résorption{invasive cervical résorption) can occur foflowing in-jury to the epithelial cervical attachment apparatusand to the area of the root surface just below the at-tachment apparatus. Clastic cells then colonize thedamaged area and begin resorbing the tooth. If left un-treated, résorption will eventually penetrate the rootcanal." The injuries can be differentiated into physicaland chemical injuries. Physical injury, which occurs tononendodontically and endodontically treated teeth,

typically includes all forms of tooth trauma, surgicalprocedures, orthodontic treatment, hruxism, and peri-odontal root planing and scaling. Chemical Injury canoccur from agents used within the root canal system,such as internal bleaching solutions. When 30''/o hy-drogen peroxide is used for internal bleaching, gingivalor periodontal tissues can become irritated as the hy-drogen peroxide leaches through cervical dentinaltubules^' (Eigs 10a and 10b).

2. Apical. There are three variants of external in-flammatory root résorption. They are related to (1)traumatic injury, particularly intrusive luxation (Eigs10a and 10b); (2) periradicular periodontitis (Eigs 2,11, and 12); and (3) orthodontic treatment in whichthe pulp reinains vital (external apical root résorp-tion) (Eigs 13 and 14). Regularly, all teeth with peri-radicular periodontitis will exhibit some degree of ex-ternal inflammatory root résorption at the apex.*Intense and progressive inflammation conflned to theapex causes sufficient pressure to overcome the "re-sistance" of the cémentai layer to résorption.^^ Intraumatic injuries, especially intrusive luxation, mi-crobial stimuli from the infected root canal cause in-flammatory root résorption at the apical foramina.The speciflc causes of external root résorption duringorthodontic treatment are not well understood, butexcessive forces, notably intrusive or tipping in na-ture, are commonly implicated.'* It is hypothesizedthat the excessive forces initiate inflammation eitheras a result of stimulation of a phagocytic process bytissue breakdown products or through some form ofneurogenic inflammation.*"

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Figs lOa atid 10b Externai inliammatory root résorption at thecervicai anä apicai parts ot the root, related to trauma. (Left)Radiographie appearance. (Above) Diagrammatic description

Figs 11a and 11b Externai intiammatory root résorption at the apex, related to periradicuiarperiodcnlitis. Note the widened periodontal iigament and ioss of adjacenl lamina dura andtooth structure. (Left) Radiographie appearance. (Right) Diagrammatic description

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Figs 12a to 12c Externai intiammatoiy root'esorplion at tiie apex, related tc penradicuiar periodonti-tis. Note the widened periodontai ligament and ioss ci adjacent iamina dura and tootti structure.

Fig 12a Radiographie appearance. Fig 12b Diagrammatic description.

F;g 12c Ptiotograpnic appearance ot extracted tootn.

Clinical evaluation. External inflammatory root ré-sorption is considered a major resorptive conditionwithout symptoms." This type of résorption is foundfo progress more rapidly and frequently in immatureteeth because of wide tubules and thin dentinai walls.The most cornmon location for external inflammatoryrésorption is the cervical aspect of the footh, wherethe progression of résorption is inward and lateral butleaves the canal intact. The résorption can begin 2 to12 weeks after injury. It progresses rapidly, especiallyafter tooth replantation in patients between the agesof 6 and 10 years.

The process of EIRR can be transient or progres-sive. The transient type occurs frequently in trauma-tized teeth and in feeth that have undergone orth-odontic and periodontai treattnent. For résorption tocontinue, resorbing cells require continuous stimula-tion. However, stimulation by resorptive cells on de-nuded dentin or cementum surface appears to be sus-

tained for no more than 2 to 3 weeks; therefore, thetransient type of résorption tnay arrest spontaneously.

The progressive type of external inflammatory ré-sorption occurs when the source of inflammation isnot removed, causing an ongoing resorptive process.Extensive résorption can ultimately lead to an increasein mobility of the tooth. Coronally, as résorption ad-vances further inward at the cervical level, the crownof the tooth becomes undermined. Granulomatous tis-sue grows into the resorptive defect, resulting in pinkdiscoloration of the crown.

Radiographie evaluation. With EIRR, the peri-odontal ligament space becomes widened and there isa loss of adjacent lamina dura and tooth structure(Figs 10, 11, and 13), resulting in ragged, poorly de-fined mesial and distal borders. There may also be agradual increase in radiopacily toward the root canalspace. External résorption in the cervical aspect of thetooth is visible clinically and radiographically as a sin-

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Figs 13a and 13b Externai intiammaiory root résorption at tiie apex related to orth-odontic treatment. (Left) Radiographic appearanoe. (Right) Diagrammatic description.

Figs 14a and 14b Externai intiammatory root résorption at fhe apex, reiated to orthodontictreafment. (Left) Radiographio appearance. (Right) Diagrammatic description.

gle résorption lacuna in the cervical area.'*" It is lo-cated at the supra-alveolar portion and does not in-volve tbe subcrestai part of the root.'" In case of exter-nal inflammatory root résorption in tbe root apex, apersistent and progressive radioiucency is typicallyfound adjacent fo the region of root résorption^' (Figs10 to 13),

Histoiogic evaluation. Histologically, EIRR is rep-resented by a bowl-shaped résorption area into ce-mentum and dentin with inflammation of adjacentperiodontal tissue and presence of infected or necroticpulp in the root canal.^ In the periodontium, granulo-

matous tissue is present with lympbocytes, plasmacells, and poiymorphonuciear leukocytes. The adja-cent resorbing surface of tbe root has many Howshiplacunae, wbicb occasionaliy contain osteoclasts.'*

Variations. In undermining EIRR, a small openingon the external surface of the root and a resorptivecavity within the body of the root are present. Tbecavity contains granulomatous tissue, with activeodontoclastic ceils, and inflammatory cells (Figs 15aand 15b). Late external inflammatory root résorptionoccurs years after injury and is usually located at thecementoename! junction.

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FIgs 15a and ISb External inNammatory root résorption (undermining) (Left) Radiographieappearance. ÍH/g/iíJ Diagrammatic description.

Treatment. Treatment of external inflammatory rootrésorption is dependent on the etiology:

1. Resorption as a result of orthodontic treatment:In cases where orthodontic treattnent is the soleetiologic agent for the resorptive process, re-moval of the pressure of orthodontic movementwill arrest the résorption,

2. Cervieally loeated résorption in which the pulp isvital and treatment of the cervical résorption isunlikely to cause pulpal injury; If pulpal injury isuniikely during the repair of EIRR, baseline ther-mai and electrical pulp tests should be recordedand the defect restored.

3. Ccrvically iocated résorption in which the pulp isvitai and treatment of the cervical résorption islikely to cause pulpal injury: Nonsurgieal rooteanal therapy is performed, and the external re-sorbed defect is restored.

4. Cervieally located résorption in which the pulp isnonvital: Nonsurgical root canal therapy is per-formed, and the external resorbed defect is re-stored.

5. Resorption as a result of puipai necrosis andperiodontal injury: tNonsurgicai root canal ther-apy is performed, and the external resorbed de-fect is restored, when indicated.

In the event that the pulp is necrotic or likely to un-dergo irreversible injury during the treatment of exter-nal cervical résorption, nonsurgical root canai therapy

with the use of calcium hydroxide as an interimmedicament is recommended.^ In some instances, en-dodontic and periodontal therapy may be necessary toehminate resorption-eausing bacteria and inflamma-tion.^' Furthermore, ail teeth with external inflamma-tory root résorption should be evaluated radiographi-cally on a regular basis.

Posttreatment complications. The major concernafter treatment of externai inflammatory root résorp-tion is the high rate of recurrence. This may be causedby cells in the adjacent periodontal ligament under-going a metaplastic process and again beeoming re-sorptive. Other posttreatment complications ineludecervicai root fracture with severe cervical résorptionand periodontal defects resulting from flap reflectionduring excavation and restorations of résorption de-fects.^' Alternatively, as infiammatory résorption be-comes arrested, ankyiosis can occur.

Ankyiosis. Etiology. Ankyiosis is primariiy associ-ated with a history of luxation injuries, especially avul-sion. It occurs after extensive necrosis of the peri-odontal ligament with formation of bone on thedenuded area of the root surface. Ankyiosis is a unionof tooth and bone, with no intervening connective tis-sue, foliowing external inflammatory résorption.Studies of mechanical removal of ail or part of theperiodontal ligament prior to tooth replantation havedemonstrated that this procedure eonsistently leads todentoaiveolar anltylosis. *'"*

Ankyiosis can be progressive or transient.^ The like-lihood of progressive ankyiosis increases dramatically

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when greater than 20% of the root surface isdamaged.^-*« In replanted teeth, physical and bio-chemical alterations to the periodontal ligatnent mayinfluence the phenotypie expression of the progenitorcells and account for the development of ankylosisand replacement résorption.""^

Ankylosis is not a disease process. It occurs as a"mistake" because cells involved in the remodeling ofbone are not able to distinguish among root cemen-tum, dentin, and bone.'-* The tooth root is thus incor-porated into the normal remodeling process of thealveolus and its gradual replacetnent by bone. The rateof progression of ankyiosis is directly related to theinitial damage to the root surface and the age of thepatient. The progression of ankylosis is very rapid inyoung individuals.-

Clinical evaluation. The tooth will be immobileonce it is ankylosed; therefore, percussion of the teethis an important diagnostic tool. When a tooth is anky-losed, there Is a high pitch or metallic tone that will bevery different from that elicited from adjacent unin-jured teeth. In some cases, a change in tone on percus-sion may be evident before radiographie changes be-come apparent.

However, in some cases, ankylosis is transitory andmay disappear within a year of injury as the tooth re-turns to normal percussion tone. Studies show thatloss of mobility occurs when more than 10°'b of theroot surface is ankylosed.-' -'-' Ankylosis can usually bediagnosed 4 to 6 weeks after replantation. High-pitched percussion tone occurs when 20% of the rootsurface is anliylosed."'" Other clinical signs that may bepresent include infraocclusion, incomplete alveolarprocess development in a young patient, and lack of anormal mesial drift.

Radiographie evaluation. It is difflcult to identifyankylosis on radiographs because of overlapping struc-tures and bone marrow spaces.'^ However, a completedisappearance of the periodontal space and an unevenroot surtace contour is common^ (Eigs 16 and 17).

Histoiogic evaluation. There is a continuous re-placement of root substance with bone, resulting in aunion between bone and root substance without inter-vening connective tissue.^ Ankylosis occurs when theexternal surface of the replanted tooth becomes popu-lated by osteoblasts and osteoclasts that are continu-ous with the endosteal spaces of the adjacent bonemarrow. The endosteal spaces of alveolar bone con-fain a reservoir of progenitor cells that are capable ofmigrating into the periodontal ligament to become os-teoblasts or cementoblasts.-'s-'

Treatment. There is no treatment for ankylosis atpresent. Ultimately the crown of the tooth will fractureoff at the gingival crest as ankylosis progresses, result-ing in a complete replacement of the root by bone,'''

Potential complications. Ankylosis in young pa-tients can complicate normal bone growth and devel-opment, resulting in problems such as malocclusionor supereruption of opposing teeth. Careful considera-tion is necessary if extraction is the treatment ofchoice for ankylosed incisors because this may signifi-cantly reduce alveolar bone height that will be diffi-cult to restore.^

External replacement résorption. Etiology. Theprimary cause of replacement résorption is luxationinjuries. This is a continuous process whereby thetooth is gradually resorbed and subsequently replacedby bone.'"' It differs from ankyjosis because of thepresence of intervening inflamed connective tissue.''" ""During tooth avulsion, large areas of the periodontalligament are lost or damaged. Healing then occursfrom the alveolar side of the socket and leads to aunion between the tooth and alveolar bone."'"

Clinical evaluation. The clinical flndings for re-placement résorption are similar to those for ankylosisin that replacement résorption typically follows anasymptomatic course. The most signiflcant clinical fea-ture is a high-pitched response to percussion com-pared to Ihat of the adjacent teeth.

Radiographie evaluation. Disappearance of theperiodontal ligament space will be obsei ved, with as-sociated progressive root résorption, followed by bonereplacement.- The defect margins have an irregular ap-pearance'' (Eigs 16 and 17).

Histoiogic evaluation. The root substance is beingreplaced by bone, although a connective tissue inter-face is present, and there is no actual union betweenroot and bone.= The connective tissue interface fre-quently contains inflaminatory cells and osteoclasticcells, which can be seen resorbing the tooth andbone. Bone then grows into the region that has beenresorbed.

Treatment. Despite attempts at treatment, such asplacement of calcium hydroxide in the canal, this typeof résorption usually progresses until there is litfle orno root left, and tooth extraction is necessary.''

Transient apical breakdown (TAB)

Transient apical breakdown is a temporary phenome-non in which the apex of the tooth displays the radio-graphic appearance of résorption that is linked to therepair processes of a traumatically injured pulp and/orperiodontium of luxated mature teeth. This process isinvariahly followed by surface résorption and/or oblit-eration of the pulp canal. The injured periradicular tis-sue generally returns to normal following repair,which usually takes place 1 year after trauma.-**«

Etiology. This breakdown process is related to thetype of injury and stage of root development.

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Figs 16a and 16b External repiacement resorptioh or anhyiosiswith externai inflammatory root résorption at the cer^'ioai part otthe root. (Left) Radiographie appearance (Below) Diagrammaticdescription.

Figs 17a and 17b Externai repiacemeni résorption or ani<yiosiswith externai intiammatory root résorption at the cervical part ofihe rcot. (Left) Radiographie appearance (Below) Diagrammaticdescription

Typically, it is caused by moderate injuries to the pulp,such as subluxation, extrusion, and lateral luxation, ora moderate eombined injury to the periodontai liga-ment and the pulp in mature teeth. It is rare after aslight injury and absent after a severe injury. Otherpossible causes of TAB are infections, orthodontictreatment, and ocelusal insult to the periodontium.''^

Clinical evaluation. The tooth wiil often respondwithin normal limits to pulp tests. Clinicaliy, in someinstances, the tooth may undergo a color changeand/or have varying results from electrical pulp testing.However, following repair, clinical and radiographiefindings will return to normal'' (Figs 18 and 19}.

Radiographie evaluation. Transient apical break-down can only be found in teeth with fully formedroots and closed or half-closed apices. A transient lo-calized change in the size of the apical periodontal lig-ament space, ranging from 2-times normal width to asemicircular radiolucency, cotnbined with a bluntingof the apex from surface résorption, can be observed.Also, pulp canal obliteration may be seen during TABor foiiowing TAB«- « (Figs 18a and 18b),

Histologie evaluation. No butnan or animal studieshave examined the histologie healing events of tran-sient apical breakdown,''* •'

Treatment. No treatment is recommended.

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Figs 18a and leb Transient apicai breakdown at tne initial visit Resuits of the sensitivity testwere witiiin normai iimits. (Left) Radiographic appearance (Right) Diagrammatic description.

Figs 19a and 19b Transient apicai breakdown at ttie 1-year foliow-up. Resuits ot the sensitiv-ity test were witnin noimai limits. (Left) Radiographie appearance, (flight) Diagrammatic de-scription.

Combined internal and external résorption

Internal and external résorptions can occur simultane-ously on the same tooth. This can be detected at vari-ous stages of progression and may appear as separate

or joined defects. As the résorptions advance inwardfrom the external surface and otttward from the inter-nal surface, fhe defects will eventually communicate(Figs 16, 17, 20, and 21).

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Figs 20a and 20b Combined internai and external résorption. (Left) Radiographic appear-ance. (Right) Diagrammatic description.

Figs 21a and 21b Combined internal and externai résorption fi-eftj Radiographio appearance. (Right)Diagrammatic desciiplion

REFERENCES

1. American Association of Endodontists. Glossary:Contemporary Terminology for Endodontics. Chicago:American Association of Endodontists, 1994.

2. Andreasen JO. Andreasen FM. Textbook and Color Atlas ofTraumatic Injuries to the Teeth. St Louis: Moshy, 1994.

3. Pierce AM, Lindskog S, Hammarström L. Osteoclasts:Structure and function. Electron Microsc Rev 1991;4:l-45.

4. Anan H, Akamine A, Maeda K. An enzyme hist o chemicalstudy of the behavior oi rat bone cells during experitnentalapical periodontitis. J Endod 1993;19:83-86.

5. Boyde A, Ali NN, Iones SJ. Resorption of dentine by iso-lated osteoclasts in vitro. Br Dent J 1984; 156:216-220.

6. Andreasen JO, Andreasen FM. Root résorption followingtraumatic dental injuries. Proc Finn Dent Soc 1992;88:(suppl 1):95-114,

7 Akamine A, Hashiguchi 1, Toriya Y, Maeda K. Immuno-histochemical exatnination on the localization of macro-phages and plasma cells in induced rat periapical lesions.Endod Dent Traumatol 1994;10:121-128.

8. Alîamine A, Anau H, Hamachi T, Maeda K. A hi s to chemicalstudy of the behavior of macrophages during experimentalapical periodontitis in rats. J Endod 1994;20:474-478.

9. Shafer WG, Hine Mti, Levy BM. A Textbook of OralPathology. Philadelphia: Saunders, 1993.

24 Volume 30, Number 1, 1999

Ne et al

10. Cluhisy DR, Ogilvie CM, Carpanter RI, Ramnarainc ML.Localized, tumor-associated osteolysis involves the recruit-ment and aetivation of osteoclasts. I Orthop Res 1996;14:2-6.

11. Aaboe M. Pinholt EM, Hjorting-Hansen E. Healing of ex-peritnentally created defects: A review. Br J Oral MaxillofacSurg 1995:33:312-318.

12. Ashcroft GS, Horati MA, Ferguson MW. The effects ofaging on cutaneous wound healing in mammals. I Anat1995;187:K26.

13. Seltzer S. Endodontology: Biologic Considerations in Endo-dontic Procedures, ed 2. Philadelphia: Lea & Febiger, 1988.

14. Wilson M. Biological activities of lipopolysaccliarides frotnoral bacteria and their relevance to the pathogenesis ofchronic periodontitis. Sei Prog 1995;78;19-34.

15. Rifkin BR, Baker RL, Somerman MJ, Pointon SE, ColemanSJ, Au WG. Osteoid resorptign by mononuclear cells invitro. Cell Tissue Res 1980;210:493-500.

16. Domon T, Osanai M, Yasuda M, Seki E, Takahashi S,Yamamot T, Wakita M. Mononuclear odontoclast participa-tion in tooth résorption. The distribution of nuclei inhuman odontoclasts. Anat Rec 1997;249;449-457.

17. Gilles JA, Carnes DL, Windeier AS. Development of an invitro culture System for the study of osteociast activity andfunction. J Endod 1 9 9 4 ; 2 0 : J 2 7 - 3 3 1 .

18. Bord S, Horner A, Hembry RM, Reynolds JJ, Compstoii JE.Production of collagenase by human osteoblasts and osteo-clasts in vivo. Bone 1996;19:35-40.

19. Debari K, Sasaki T, Udagawa N, Rifliin BR. An ultrastruc-tural evaluation of the effects of cysteine-proteinase in-hibitors on osteoclastie resorptive functions. Calcif TissueInt 1995:56:566-570.

20. Rifkin BR, Gay CV. Biology and Physiology of theOsteoelast. Boca Raton, FL: CRC Press, 1992.

21. Okada Y, Naka K, Kawamura K, Matsunioto T, Seiki M.Localization of matrix metalloproteinase 9 ¡92-kilodaltongelatinase/type IV collagenase-gelatinase B) in osteoelasts:Implications for bone résorption. Lab Invest 1995;72:3U-322.

22. Datta HK, Manning P, Rathod H, McNeil CJ. Effect of cal-eitonin, elevated calcium and extracellular matrices on su-peroxide anion production by rat osteoclasts. Exp Physiol1995:80:713-719.

23. Egerton M, Needham M, Evans S, Millest A. Cerillo G,McPheat J, et al. Identifieation of multiple human calcitoninreceptor isoforms: Heterologous expression and pharmaco-logical characterization. J Mol Biol 1995; 14:179-189.

24. Pierce A, Berg JO, Lindskog S. Calcitonin as an alternativetherapy in the treatment of root résorption. J Endod 1988;14:459-464,

25 Pierce AM, Lindskog S, Early responses by osteoclasts invivo and dentinoclasts in vitro to cortieosteroids JSuhmicrosc Cytol Pathol 1989;21:501-508.

26. Pierce A. Experimental basis for the management of dentalrésorption. Endod Dent Traumatol 1989;5;255-265.

27 Suda T, Udagawa N, Nakamura I, Miyaura C, Takahashi N.Modulation of osteociast differentiation by local faetors.Bone 1995:17(suppl):87S-91S.

28. Yamasaki K, Miura F, Suda T. Prostaglandin as a mediatorof bone résorption induced by experimental tooth move-ment in rats. J Dent Res 1980;59:1635-1642.

29 Suda T, Nakamura 1, Jimi E, Takahashi N, Regulation of os-teociast function. J Bone Miner Res 1997; 12:869-879.

30. Nair SP, Meghjl S, Wilson M, Reddi K, White P, HendersonB. Bacterially induced bone destruction: Mechanisms andmisconceptions. Infect Immun 1996:64:2371-2380.

31. Beneiiati F. Root résorption: Types and treatment. GenDent 1997:45:42-45.

32. Trope M, Chivian N, Sigurdsson A. Traumatic injuries. In:Cohen S, Burns RC (eds). Pathways of the Pulp. St Louis:Mosby, 1998.552-599.

33. Trope M. Root résorption of dental and traumatic origin:Classification based on etiology. Pract Periodont AesthetDent 1998:10:515-522.

34. Tronstad L. Root resorption-Etiology, terminology and clin-ical manifestations. Endod Dent Traumatol 1988;4:241-252,

35. Wedenberg C, Lindskog S. Experimental internal résorp-tion in monkey teeth. Endod Dent Traumatol 1985,1:221-227.

36. Wedenberg C, Zetterqvist L, Intemal résorption in humanteeth-A histological, scanning electron microscopic, andenzyme histoehemical study. J Endod 1987;13:255-259.

37. Malueg LA, Wilcox LR, Johnson W. Examination of exter-nal apical root résorption with scanning electron mi-croscopy. Oral Surg Oral Med Oral Pathol Oral RadiolEndod 1996:82:89-93.

38. Barrett E, Kenny DJ. Avulsed permanent teeth: A review ofthe literature and treatment guidelines. Endod DentTraumatol 1997:13:153-163.

39. Kaley |, Phillips C. Factors related to root résorption inedgewise practice. Angle Orthod 1991:61:125-132.

40. Bender IB, Byers MR, Mori K. Periapical replacement ré-sorption of permanent, vital, endodontically treated incisorsafter orthodontic movement: Report of two cases. J Endod1997:23:768-772

41. Berglundh T, Thilander B, Sagne S. Tissue characteristics ofroot résorption areas in transplanted maxillary canines.Acta Odontol Scand 1997:55:206-211.

42. Lindskog S, Pierce AM, Blomlof L, Hammarström L. Tberoie of necrotic periodontal membrane in cementum ré-sorption and ankyiosis. Endod Dent Traumatoi 1985;1:96-101,

43. Andersson L, Blomlof L, Lindskog S, Feiglin R. Hammar-ström L. Tooth ankyiosis. Clinical, radiographie and histo-logical assessments. Int i Oral Surg 1984:13:423-43 L

44 Hammarström L, Blomlof L, Lindskog S. Dynamics of den-toaiveolar ankyiosis and associated root résorption. EndodDent Traumatol I989;5:163-175.

45. McCuUoch CA, Nemeth E, Lowenberg B, Melcher AH.Paravascular cells in endosteal spaces of alveolar bone con-tribute to periodontal ligament eells populations. Anat Rec1987:219 233-242.

46. McCulloch CA. Progenitor cell populations in tbe periodon-tal ligament of mice. Anat Rec 1985;211:258-262,

47 Hammarström L, Lindskog S. Factors regulating and inodi-lying dental root résorption. Proc Finn Dent Soc 1992;88(suppl 1¡:115-123.

48. Boyd KS. Transient apical breakdown following subluxationinjury: A case report. Endod Dent Traumatol 1995;11:37-40.

49. Andreasen F. Transient apical breakdown and its relation tocolor and sensibility changes after luxation injuries to teeth,Endod Dent Traumatol 1986;2:9-19.

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