Orthodontically induced inflammatory root resorption

Orthodontically InducedOrthodontically Induced
Inflammatory RootInflammatory Root
Resorption.Resorption.
Part I: The Basic SciencePart I: The Basic Science
AspectsAspects
www.indiandentalacademy.comwww.indiandentalacademy.com

*Naphtali Brezniak, MD, DMD, MSD*Naphtali Brezniak, MD, DMD, MSD
**Atalia Wasserstein, DMD**Atalia Wasserstein, DMD
*Head of the orthodontic residency, Israel*Head of the orthodontic residency, Israel
Defense Forces, Tel-Hashomer,Israel.Defense Forces, Tel-Hashomer,Israel.
**Lecturer, Israel Defense Forces, Tel-**Lecturer, Israel Defense Forces, Tel-
Hashomer, Israel.Hashomer, Israel.
Angle Orthodontist, Vol 72, No 2, 2002Angle Orthodontist, Vol 72, No 2, 2002

INTRODUCTIONINTRODUCTION
Orthodontically induced inflammatory rootOrthodontically induced inflammatory root
resorption (OIIRR) or, as it is betterresorption (OIIRR) or, as it is better
known, root resorption, is an unavoidableknown, root resorption, is an unavoidable
pathologic consequence of orthodonticpathologic consequence of orthodontic
tooth movement.tooth movement.

 Discuss the basic sciences aspects ofDiscuss the basic sciences aspects of
OIIRROIIRR
 In part II, present the clinical aspectsIn part II, present the clinical aspects

THE ROOT RESORPTIONTHE ROOT RESORPTION
PROCESSPROCESS
 Wehrbein et alWehrbein et al discussed differentdiscussed different
grades of root resorption mainly in termsgrades of root resorption mainly in terms
of the close proximity of the root to theof the close proximity of the root to the
cortical nonmetaplastic bones, as well ascortical nonmetaplastic bones, as well as
other pathologic phenomena such asother pathologic phenomena such as
dehiscence and fenestrations.dehiscence and fenestrations.
 Highlighted the risk and perhaps theHighlighted the risk and perhaps the
iatrogenic effect of orthodontic treatment.iatrogenic effect of orthodontic treatment.

 However, it is important to note that theHowever, it is important to note that the
aforementioned studies were based solelyaforementioned studies were based solely
on one human non experimental study.on one human non experimental study.
 Orthodontic force applications induce aOrthodontic force applications induce a
local process that includes all of thelocal process that includes all of the
characteristics of inflammation.characteristics of inflammation.
 Rubor(redness), calor (heat), tumorRubor(redness), calor (heat), tumor
(swelling), dolor (pain), and, to a small(swelling), dolor (pain), and, to a small
extent, functio laesa (inhibited function).extent, functio laesa (inhibited function).

 This inflammation, which is essential toThis inflammation, which is essential to
tooth movement, is actually thetooth movement, is actually the
fundamental component behind the rootfundamental component behind the root
resorption process.resorption process.
 Therefore, in light of the full extent of theTherefore, in light of the full extent of the
histologic process, orthodontic forcehistologic process, orthodontic force
induced root resorption should be moreinduced root resorption should be more
accurately termedaccurately termed orthodontically inducedorthodontically induced
inflammatory root resorptioninflammatory root resorption (OIIRR).(OIIRR).

There are three degrees of severity ofThere are three degrees of severity of
OIIRR:OIIRR:
 1.1. Cemental or surface resorption withCemental or surface resorption with
remodeling.remodeling. In this process, only the outerIn this process, only the outer
cemental layers are resorbed, and theycemental layers are resorbed, and they
are later fully regenerated or remodeled.are later fully regenerated or remodeled.
This process resembles trabecular boneThis process resembles trabecular bone
remodeling.remodeling.

 2.2. Dentinal resorption with repairDentinal resorption with repair (deep(deep
resorption). In this process, the cementumresorption). In this process, the cementum
and the outer layers of the dentin areand the outer layers of the dentin are
resorbed and usually repaired withresorbed and usually repaired with
cementum material.cementum material.
 The final shape of the root after thisThe final shape of the root after this
resorption and formation process may orresorption and formation process may or
may not be identical to the original form.may not be identical to the original form.

 3.3. Circumferential apical root resorptionCircumferential apical root resorption. In. In
this process, full resorption of the hardthis process, full resorption of the hard
tissue components of the root apextissue components of the root apex
occurs, and root shortening is evident.occurs, and root shortening is evident.

 Different degrees of apical root shorteningDifferent degrees of apical root shortening
are, of course, possible. When the rootare, of course, possible. When the root
loses apical material beneath theloses apical material beneath the
cementum, no regeneration is possible.cementum, no regeneration is possible.
 External surface repair usually occurs inExternal surface repair usually occurs in
the cemental layer. Over time, sharpthe cemental layer. Over time, sharp
edges may be gradually leveled. Ankylosisedges may be gradually leveled. Ankylosis
is not a common sequel of OIIRR.is not a common sequel of OIIRR.

The cellular processThe cellular process
 Brudvik and RyghBrudvik and Rygh
OIIRR is a part of the hyaline zoneOIIRR is a part of the hyaline zone
elimination process. The first cells to beelimination process. The first cells to be
involved in this necrotic tissue removal areinvolved in this necrotic tissue removal are
cells that are negative for tartratecells that are negative for tartrate
resistance acid phosphatase (TRAP) andresistance acid phosphatase (TRAP) and
that have no ruffled borders.that have no ruffled borders.

 These are Macrophage-like cells, whichThese are Macrophage-like cells, which
are most probably activated by signalsare most probably activated by signals
coming from the sterile necrotic tissue, thecoming from the sterile necrotic tissue, the
result of the orthodontic force application.result of the orthodontic force application.
 Macrophages are scavenger cells fromMacrophages are scavenger cells from
the hematopoietic lineage, and their role isthe hematopoietic lineage, and their role is
to eliminate necrotic tissues.to eliminate necrotic tissues.

 The initial elimination process takes placeThe initial elimination process takes place
at the periphery of the hyaline zone, whereat the periphery of the hyaline zone, where
blood supply to the periodontal ligamentblood supply to the periodontal ligament
exists or is even increased.exists or is even increased.

 During removal of the hyaline zone, theDuring removal of the hyaline zone, the
nearby outer surface of the root, whichnearby outer surface of the root, which
consists of the cementoblast layerconsists of the cementoblast layer
covering the cementoid, can be damaged,covering the cementoid, can be damaged,
thus exposing the underlying highly densethus exposing the underlying highly dense
mineralized cementum.mineralized cementum.

 It is possible that the orthodontic pressureIt is possible that the orthodontic pressure
itself directly damages the outer rootitself directly damages the outer root
surface layers in such a way that there is asurface layers in such a way that there is a
need for their removal as well. The rootneed for their removal as well. The root
surface under the main hyaline zone issurface under the main hyaline zone is
resorbed only several days later when theresorbed only several days later when the
repair process in the periphery is alreadyrepair process in the periphery is already
taking place.taking place.

 Confirmed by studies of human premolarsConfirmed by studies of human premolars
that were moved buccally before theirthat were moved buccally before their
extraction.extraction.

 The resorption process continues until noThe resorption process continues until no
hyaline tissue is present and/or the forcehyaline tissue is present and/or the force
level decreases. Resorption lacunaelevel decreases. Resorption lacunae
expand the root surfaces involved andexpand the root surfaces involved and
thereby indirectly decrease the pressurethereby indirectly decrease the pressure
exerted through force application.exerted through force application.
 Thus, decompression allows the processThus, decompression allows the process
to reverse and the cementum to beto reverse and the cementum to be
repaired.repaired.

 The role and the kinetics of theThe role and the kinetics of the
osteoclasts in tooth movement and rootosteoclasts in tooth movement and root
resorption during different reactivationresorption during different reactivation
schedules have been studied in rats.schedules have been studied in rats.
 In all but one of the activation andIn all but one of the activation and
reactivation schedules, the amount of rootreactivation schedules, the amount of root
surface involved in the resorption reachedsurface involved in the resorption reached
a plateau of 50% of the root surface on thea plateau of 50% of the root surface on the
compression side.compression side.

 The extent of root resorption wasThe extent of root resorption was
increased only when force reactivationincreased only when force reactivation
was performed at the peak presence ofwas performed at the peak presence of
osteoclast count in the involved regionosteoclast count in the involved region
(day 4).(day 4).
 In all other re-activation schedules, toothIn all other re-activation schedules, tooth
movement was improved with no risk tomovement was improved with no risk to
root surfaces.root surfaces.

 Osteoclast recruitment after activation andOsteoclast recruitment after activation and
reactivation do not exhibit the samereactivation do not exhibit the same
pattern.pattern.
 There are unexplained different refractoryThere are unexplained different refractory
periods of 10, 7,4,& 1days afterperiods of 10, 7,4,& 1days after
reactivation and after1,4,7& 10 days,reactivation and after1,4,7& 10 days,
respectively.respectively.

 Since the refractory period is 10 daysSince the refractory period is 10 days
following the first activation, it is only afollowing the first activation, it is only a
matter of simple mathematics that ifmatter of simple mathematics that if
reactivation is after one day, the refractoryreactivation is after one day, the refractory
period is 10 days, and if reactivation isperiod is 10 days, and if reactivation is
after four days, the refractory period is 7after four days, the refractory period is 7
days, etc.days, etc.

 The immediate increase in osteoclastsThe immediate increase in osteoclasts
count after one day indicates that in rats,count after one day indicates that in rats,
when force is applied to the teeth,when force is applied to the teeth,
progenitor cells in the osteoclast lineageprogenitor cells in the osteoclast lineage
are ready in the periodontal ligament or itsare ready in the periodontal ligament or its
immediate vicinity, waiting to be fullyimmediate vicinity, waiting to be fully
expressed.expressed.

 In addition to the mono-nucleatedIn addition to the mono-nucleated
macrophage-like cells, multinucleatedmacrophage-like cells, multinucleated
TRAP-positive giant cells without ruffledTRAP-positive giant cells without ruffled
borders are involved in the hyaline tissueborders are involved in the hyaline tissue
removal. These cells may be osteoclastsremoval. These cells may be osteoclasts
or odontoclasts that did not come to fullor odontoclasts that did not come to full
expression earlier (ie, preosteoclasts) andexpression earlier (ie, preosteoclasts) and
that become involved in the necrotic tissuethat become involved in the necrotic tissue
elimination.elimination.

 On introduction of a new mechanicalOn introduction of a new mechanical
stimulus, they differentiate into fullystimulus, they differentiate into fully
developed osteoclasts or odontoclasts in adeveloped osteoclasts or odontoclasts in a
matter of hours. (TRAP-positive cells withmatter of hours. (TRAP-positive cells with
ruffled borders and a clear zone areruffled borders and a clear zone are
pathognomonic to the clast lineage.)pathognomonic to the clast lineage.)

 Most studies agree that osteoclasts andMost studies agree that osteoclasts and
odontoclasts are comparable cells.odontoclasts are comparable cells.
 Lasfargues and SaffarLasfargues and Saffar believe that thebelieve that the
odontoclast, unlike the osteoclast, isodontoclast, unlike the osteoclast, is
prostaglandin independent becauseprostaglandin independent because
indomethacin administration to rats duringindomethacin administration to rats during
physiologic tooth movement decreasesphysiologic tooth movement decreases
bone resorption but enhances rootbone resorption but enhances root
resorption.resorption.

Root resistance to resorptionRoot resistance to resorption
 All new reports in the literature recognizeAll new reports in the literature recognize
the overall protective function of the root’sthe overall protective function of the root’s
outer layers, the cementoblasts, and theouter layers, the cementoblasts, and the
outer uncalcified cementum (theouter uncalcified cementum (the
precementum or cementoid). These layersprecementum or cementoid). These layers
might contain non collagenic materials,might contain non collagenic materials,
eg, the cells themselves, that possesseg, the cells themselves, that possess
potent anticollagenase properties. This ispotent anticollagenase properties. This is
in agreement with the findings of previousin agreement with the findings of previous
reports.reports.

 A clinical study revealed that exposure ofA clinical study revealed that exposure of
the roots to two sequential orthodonticthe roots to two sequential orthodontic
treatment procedures, one administeredtreatment procedures, one administered
during adolescence and the otherduring adolescence and the other
administered later during adulthood,administered later during adulthood,
actually decreased the extent of OIIRR.actually decreased the extent of OIIRR.

Accordingly, two questions might be raised:Accordingly, two questions might be raised:
1. what sort of protective effect was1. what sort of protective effect was
provided to the roots by the firstprovided to the roots by the first
treatment?treatment?
2. Could the remodeled cementum2. Could the remodeled cementum
contribute some additional protectivecontribute some additional protective
effect in the outer layers?effect in the outer layers?
 These questions have yet to be answered.These questions have yet to be answered.

The repair processThe repair process
 Morphologically, the repair process of theMorphologically, the repair process of the
resorbed lacunae is described asresorbed lacunae is described as
beginning from the periphery, bottom, orbeginning from the periphery, bottom, or
all directions.all directions.
 It begins about two weeks after forceIt begins about two weeks after force
removal, with the placement of acellularremoval, with the placement of acellular
cementum succeeded by cellularcementum succeeded by cellular
cementum.cementum.

 This process is evident in 38% and 82% ofThis process is evident in 38% and 82% of
human premolar lacunae after two andhuman premolar lacunae after two and
five weeks, respectively.five weeks, respectively.
 In bone, osteoclasts undergoing apoptosisIn bone, osteoclasts undergoing apoptosis
leave at the bottom of the lacuna a proteinleave at the bottom of the lacuna a protein
layer that is composed partially oflayer that is composed partially of
osteoponin and bone sialoprotein.osteoponin and bone sialoprotein.

 This layer is recognized later as theThis layer is recognized later as the
cemental line with which the osteoblastscemental line with which the osteoblasts
meet on bone formation.meet on bone formation.
 According toAccording to Bosshardt and Schroeder,Bosshardt and Schroeder,
the odontoclasts leave the root lacunarthe odontoclasts leave the root lacunar
surfaces exposed with no sediment at thesurfaces exposed with no sediment at the
base of the crater.base of the crater.

 Recently, however, it has been reportedRecently, however, it has been reported
that a specific cementum attachmentthat a specific cementum attachment
protein (CAP) has been identified inprotein (CAP) has been identified in
human cementum.human cementum.
 This protein has the ability to bind toThis protein has the ability to bind to
mineralized root surfaces with high affinity.mineralized root surfaces with high affinity.

 Its role in cementogenesis andIts role in cementogenesis and
cementoblast recruitment is still undercementoblast recruitment is still under
investigation.investigation.
 Individual variations characterize theIndividual variations characterize the
repair process as evident in OIIRR.repair process as evident in OIIRR.

Effects of pharmacologic agents onEffects of pharmacologic agents on
OIIRROIIRR
 The effects of L-thyroxine on rootThe effects of L-thyroxine on root
resorption are still controversial.resorption are still controversial.
 Administration of very low doses of thisAdministration of very low doses of this
hormone to rats during 10 days of toothhormone to rats during 10 days of tooth
movement decreased the amount of rootmovement decreased the amount of root
resorption by about 50% relative to that inresorption by about 50% relative to that in
a control group.a control group.

 Although the conclusions of this studyAlthough the conclusions of this study
were far from definitive, the investigatorswere far from definitive, the investigators
prescribed 0.5 g of thyroid to three so-prescribed 0.5 g of thyroid to three so-
called OIIRR high risk patients.called OIIRR high risk patients.
 They reported that treatment with theThey reported that treatment with the
hormone produced no new roothormone produced no new root
resorption, no worsening of the existingresorption, no worsening of the existing
resorption, and no adverse effects.resorption, and no adverse effects.

 The definition ofThe definition of high-risk patients thathigh-risk patients that
was used in the study was partlywas used in the study was partly
challenged bychallenged by Owman-Moll and Kurol.Owman-Moll and Kurol.

 Christiansen’sChristiansen’s comment on this study didcomment on this study did
not clarify the mechanism by which thenot clarify the mechanism by which the
hormone acts. It is assumed that thehormone acts. It is assumed that the
hormone either increases the resistancehormone either increases the resistance
of the cementum and dentin to clasticof the cementum and dentin to clastic
activity or increases the rate of alveolaractivity or increases the rate of alveolar
bone resorption (high levels of alkalinebone resorption (high levels of alkaline
phosphatase were found). Thus, thephosphatase were found). Thus, the
hormone enhances tooth movement as ithormone enhances tooth movement as it
indirectly reduces OIIRR.indirectly reduces OIIRR.

 Furthermore, no substantial differencesFurthermore, no substantial differences
were found in the response of monocyteswere found in the response of monocytes
to L-thyroxine and thyrocalcitonin in ato L-thyroxine and thyrocalcitonin in a
study that measured the amount ofstudy that measured the amount of
interleukin-b and tumor necrosis factor ininterleukin-b and tumor necrosis factor in
two groups that had completedtwo groups that had completed
orthodontic treatment, one with severeorthodontic treatment, one with severe
root resorption and the other with no rootroot resorption and the other with no root
resorption.resorption.

 ShiraziShirazi et al demonstrated that in rats,et al demonstrated that in rats,
increasing doses of L-thyroxine decreasedincreasing doses of L-thyroxine decreased
the extent of root resorption whilethe extent of root resorption while
increasing the amount of tooth movement.increasing the amount of tooth movement.

 Few studies have been published in theFew studies have been published in the
last decade about the role oflast decade about the role of
prostaglandins in OIIRR. Two studiesprostaglandins in OIIRR. Two studies
confirmed the known role of this majorconfirmed the known role of this major
cytokine.cytokine.

 Bisphosphonates, potent inhibitors ofBisphosphonates, potent inhibitors of
bone resorption, causes a significant dosebone resorption, causes a significant dose
dependent inhibition of root resorption independent inhibition of root resorption in
rats after force application.rats after force application.
 On the other hand, others have reportedOn the other hand, others have reported
increased resorption with bis-phosphonateincreased resorption with bis-phosphonate
treatment.treatment.

 According toAccording to AlatliAlatli et al, injections of 1-et al, injections of 1-
hydroxyethylidene-1-bisphosphonatehydroxyethylidene-1-bisphosphonate
(HEBP) in rats induces a cementum(HEBP) in rats induces a cementum
surface alteration, inhibits formation ofsurface alteration, inhibits formation of
acellular extrinsic fiber cementum (AEFC),acellular extrinsic fiber cementum (AEFC),
and delays formation of cellular mixedand delays formation of cellular mixed
fiber cementum.fiber cementum.

 Hence, HEBP increases the vulnerabilityHence, HEBP increases the vulnerability
of the root surface to resorption duringof the root surface to resorption during
orthodontic tooth movement.orthodontic tooth movement.
 Reports in the literature do not agree onReports in the literature do not agree on
the origin of AEFC. Is it a part of thethe origin of AEFC. Is it a part of the
cementum itself, laid down bycementum itself, laid down by
cementoblasts, or a part of the Sharpeycementoblasts, or a part of the Sharpey
fibers that is subsequently incorporatedfibers that is subsequently incorporated
into the acellular cementum layer?into the acellular cementum layer?

 Administration of corticosteroids in dosesAdministration of corticosteroids in doses
of 15 mg/kg to rats during orthodonticof 15 mg/kg to rats during orthodontic
treatment increases root resorption,treatment increases root resorption,
whereas low doses of one mg/kgwhereas low doses of one mg/kg
decrease root resorption.decrease root resorption.
 Alcohol consumption in adults duringAlcohol consumption in adults during
orthodontic treatment tends to increaseorthodontic treatment tends to increase
root resorption through vitamin Droot resorption through vitamin D
hydroxylation in the liver.hydroxylation in the liver.

General considerationsGeneral considerations
 The causal relationship between forceThe causal relationship between force
application and root resorption has neverapplication and root resorption has never
been fully answered.been fully answered.
 Is it a local mechanism that actuallyIs it a local mechanism that actually
expands the root surface area, therebyexpands the root surface area, thereby
decreasing the level of actual pressure?decreasing the level of actual pressure?

 Is it an essential mechanism thatIs it an essential mechanism that
maintains the width or subsistence area ofmaintains the width or subsistence area of
the periodontal membrane and its differentthe periodontal membrane and its different
components?components?
 Or is it a side effect of the inflammatoryOr is it a side effect of the inflammatory
process?process?

 Is it a reaction to loss of integrity of theIs it a reaction to loss of integrity of the
cementum layer (including cracks)?cementum layer (including cracks)?
 Or is it a part of the normal sequence ofOr is it a part of the normal sequence of
root adaptation over years?root adaptation over years?
 The last question has been addressed inThe last question has been addressed in
several publications.several publications.

 Bishara et al,Bishara et al, Performed an extensivePerformed an extensive
radiographic survey and found noradiographic survey and found no
systematic root shortening between earlysystematic root shortening between early
and mid adulthood.and mid adulthood.
 Harris et al,Harris et al, however, reported thathowever, reported that
resorption was present in about 10% ofresorption was present in about 10% of
teeth that had not been orthodonticallyteeth that had not been orthodontically
treated, and 1%–2% demonstrated severetreated, and 1%–2% demonstrated severe
resorption, mostly in the upper incisors.resorption, mostly in the upper incisors.

 Recent publications include an anecdotalRecent publications include an anecdotal
description of idiopathic root resorptiondescription of idiopathic root resorption
and two cases of long-term stability withand two cases of long-term stability with
severely resorbed roots after orthodonticseverely resorbed roots after orthodontic
treatment.treatment.

Looking aheadLooking ahead
 The previous view that the immuneThe previous view that the immune
system is linked to OIIRR has beensystem is linked to OIIRR has been
abandoned in the last 10 years.abandoned in the last 10 years.

 What about genetic causation? Thus far, itWhat about genetic causation? Thus far, it
is found that only one group has usedis found that only one group has used
polymerase chain reaction analysis topolymerase chain reaction analysis to
analyze two mRNA-encodedanalyze two mRNA-encoded
collagenolytic enzymes, matrixcollagenolytic enzymes, matrix
metalloproteinase-1 (MMP-1) andmetalloproteinase-1 (MMP-1) and
cathepsin K, in root resorbing tissue. Thiscathepsin K, in root resorbing tissue. This
research offers a new direction towardsresearch offers a new direction towards
root resorption research, which might beroot resorption research, which might be
cultivated extensively in the years aheadcultivated extensively in the years ahead

SUMMARYSUMMARY
 The cellular process of root resorption andThe cellular process of root resorption and
the effects of pharmacologic agents onthe effects of pharmacologic agents on
this process.this process.
 The ultimate predictive factors that mightThe ultimate predictive factors that might
prevent OIIRR remain unknown.prevent OIIRR remain unknown.
 Still, several clinical measures may beStill, several clinical measures may be
considered.considered.

Thank youThank you

Orthodontically induced inflammatory root resorption

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