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Root Resorption During Orthodontic Therapy Edward F. Harris External apical root resorption (EARR) is the most common iatrogenic con- sequence of orthodontics, and orthodontics is the most common cause of EARR. Localized root resorption is a normal and constant remodeling pro- cess, a response to oral microtraumas throughout life. Roots do not shorten naturally with age unless forces (eg, bruxism, tongue thrusting) overcom- press the periodontal ligament. Appositional repair normally corrects re- sorptive defects. Irreversible root shortening occurs with excessive forces or decreased resistance to normal forces. Orthodontically induced root resorp- tion starts adjacent to hyalinized zones and occurs during and after elimi- nation of hyalinized tissue. Incisors are most susceptible to EARR, probably because of their roots" spindly apex and because incisors typically are moved farther than other teeth during correction. Intrusion is probably the most detrimental direction of tooth movement, although simply the dis- tance the apex is moved is often correlated with the degree of root short- ening. The strongest single association with EARR seems to be a person's genotype. Familial studies show that a person's genotype accounts for about two-thirds of the variation in the extent of periapical resorption. In most instances, this absolves the orthodontist from blame that treatment markedly influenced the extent of resorption, and it also means that a test can be developed that will flag individuals at particular risk of developing EARR. In any event, all patients" root status should be monitored periodi- cally. Rapid resorption can be diminished with slow, intermittent forces with pauses of 2 to 3 months to allow repair of the eroded cementum. (Semin Orthod 2000;6:183-194.) Copyright © 2000 by W.B. Saunders Company R oot resorption occurs when pressure on the cementum exceeds its reparative capac- ity and dentin is exposed, allowing multinucle- ated odontoclasts to degrade the root substance. 1,2 Orthondontically induced root resorption be- gins adjacent to hyalinized zones and occurs during and after elimination of hyaline tissues? Removal of hyalinized tissue (ie, a zone of sterile necrosis) leads to removal of cementoid and mature collagen, leaving a raw cemental surface that is readily attacked by dentinoclasts. 4 There is a positive association between removal of hya- From the Department of Orthodontics, Collegeof Dentistu, Uni- versity of Tennessee, Memphis, TN. Address correspondence to Edward F. Harris, PhD, Department oJ Orthodontics, Collegeof Dentistry, University of Tennessee, 875 Union Ave, Memphis, TN 38163. Copyright 0 2000 by W.B. Saunders Company 1073-8746/00/0603-0006510.00/0 doi: 10.1053/sodo.2000. 8084 linized necrotic tissue and root resorption. 5-7 Be- cause cementum normally is more resistant than bone, forces applied to a tooth usually cause bone resorption rather than loss of cementum. However, forces are concentrated at the root apex because orthodontic tooth movement is never entirely translatory, which places the nar- row periapical region in harm's way. Rudolph 8 noted that resorption typically attacks the root tip and travels coronally, making what has been termed a "shed roof' effect to the root. The portion of the root nearest the pulp appears to be the last to give way. This process is exactly opposite to that of tooth formation. Albert Ketcham '-~,~0was the first to bring the message that apical resorption is a common and occasionally severe iatrogenic consequence of orthodontic treatment. Advent of the common- place use of dental x-ray equipment made it possible for Ketcham to evaluate a large series of treated cases. Ketcham also made a less well- Seminars in Orthodontics, Vol 6, No 3 (September), 2000: pp 183-194 183
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Root Resorption During Orthodontic Therapy Edward F. Harris

External apical root resorption (EARR) is the most common iatrogenic con- sequence of orthodontics, and orthodontics is the most common cause of EARR. Localized root resorption is a normal and constant remodeling pro- cess, a response to oral microtraumas throughout life. Roots do not shorten naturally with age unless forces (eg, bruxism, tongue thrusting) overcom- press the periodontal ligament. Appositional repair normally corrects re- sorptive defects. Irreversible root shortening occurs with excessive forces or decreased resistance to normal forces. Orthodontically induced root resorp- tion starts adjacent to hyalinized zones and occurs during and after elimi- nation of hyalinized tissue. Incisors are most susceptible to EARR, probably because of their roots" spindly apex and because incisors typically are moved farther than other teeth during correction. Intrusion is probably the most detrimental direction of tooth movement, although simply the dis- tance the apex is moved is often correlated with the degree of root short- ening. The strongest single association with EARR seems to be a person's genotype. Familial studies show that a person's genotype accounts for about two-thirds of the variation in the extent of periapical resorption. In most instances, this absolves the orthodontist from blame that treatment markedly influenced the extent of resorption, and it also means that a test can be developed that will flag individuals at particular risk of developing EARR. In any event, all patients" root status should be monitored periodi- cally. Rapid resorption can be diminished with slow, intermittent forces with pauses of 2 to 3 months to allow repair of the eroded cementum. (Semin Orthod 2000;6:183-194.) Copyright © 2000 by W.B. Saunders Company

R oo t resorp t ion occurs when pressure on the c e m e n t u m exceeds its reparative capac-

ity and den t in is exposed, allowing mult inucle- ated odontoclasts to degrade the roo t substance. 1,2 Or thondont ica l ly i nduc e d roo t resorp t ion be- gins adjacent to hyalinized zones a nd occurs du r ing and after e l iminat ion o f hyaline tissues? Removal o f hyalinized tissue (ie, a zone o f sterile necrosis) leads to removal o f c e m e n t o i d and ma tu re collagen, leaving a raw cementa l surface that is readily at tacked by dentinoclasts. 4 The re is a positive association between removal o f hya-

From the Department of Orthodontics, College of Dentistu, Uni- versity of Tennessee, Memphis, TN.

Address correspondence to Edward F. Harris, PhD, Department oJ Orthodontics, College of Dentistry, University of Tennessee, 875 Union Ave, Memphis, TN 38163.

Copyright 0 2000 by W.B. Saunders Company 1073-8746/00/0603-0006510.00/0 doi: 10.1053/sodo.2000. 8084

l inized necro t ic tissue and roo t resorpt ion. 5-7 Be- cause c e m e n t u m normal ly is m o r e resistant than bone , forces appl ied to a too th usually cause b o n e resorp t ion ra ther than loss o f c e m e n t u m . However, forces are concen t r a t ed at the roo t apex because o r t h o d o n t i c too th m o v e m e n t is never entirely translatory, which places the nar- row periapical reg ion in ha rm ' s way. R u d o l p h 8 n o t e d that resorp t ion typically attacks the roo t tip and travels coronally, mak ing what has b e e n t e rmed a "shed r o o f ' effect to the root. Th e por t ion o f the roo t neares t the pu lp appears to be the last to give way. This process is exactly opposi te to tha t o f too th fo rmat ion .

Alber t Ke tcham '-~,~0 was the first to b r ing the message that apical resorp t ion is a c o m m o n and occasionally severe ia t rogenic consequence o f o r t hodon t i c t reatment . Adven t o f the c o m m o n - place use o f denta l x-ray e q u i p m e n t made it possible for Ke tcham to evaluate a large series o f t reated cases. Ke tcham also made a less well-

Seminars in Orthodontics, Vol 6, No 3 (September), 2000: pp 183-194 183

184 Edward K Harris

known discovery, namely that the appliance used to move teeth influences the risk of root resorp- tion. Only in recent years has this difference in risks between appliances been reevaluated. 11-14

Root Resorption

Root resorption can be classified into at least 3 categories: 15-~9 surface resorption, inflammatory resorption, and replacement resorption. Surface resorption occurs constantly as microdefects on all roots; 2,7,2°-22 these normally repair themselves without notice. It is only consequential when lacunae in the cementum broaden and permit dentinoclasia. Surface resorption can occur any- where on a root but is most common periapi- cally. 2 Surface resorption stops when the insti- gating agent (usually pressure) is removed and there is repair of the cementum. 2-~ 95 Inflamma- tory resorption occurs when root resorption progresses into the dentinal tubules to pulpal tissue that is infected or necrotic or into an infected leukocyte zone. Thirdly, replacement resorption produces ankylosis of a tooth because bone replaces the resorbed tooth substance.

The odontoclast is the root-resorbing cellY 6 It is a large pleomorphic, usually multinucleated, cell formed by monocyte precursors. 27 Most re- searchers agree that odontoclasts are of hemato- poietic origin from the bone marrow and dis- semination of their precursors is through the vascular system, 2s so but a local tissue contribu- tion has not been ruled OUt. 18,~°-31

Andreasen et al conducted a series of illuminat- ing experiments to determine which tissue pro- tects a root against resorption during normal oral functions. 32-:~9 If root resorption is a normal and constant process associated with microtraumatic injuries and forces of occlusion, what protects the root surface in permanent teeth against irrevers- ible external apical root resorption (EARR)?

Andreasen reasoned that the following cell types and structures could provide a protective mechanism from irreversible EARR: cemento- blasts, fibroblasts, osteoblasts, vascular endothe- lial cells, perivascular cells, Malassez epithelial cells, cementum, cementoid, osteoid, alveolar bone or Sharpey's fibers, or a combination of these tissues, is To narrow the possibilities, An- dreasen 35,36 first removed the cementum side and then the alveolar bone side of the periodon- tal membrane. In both instances, little resorp- tion occurred, and he inferred that the protec- tive structure was in a central region of the

periodontal membrane. Sharpey's fibers (lo- cated in the innermost and outermost regions of the periodontal ligament [PDL], which are acel- lular) also were eliminated as a protective agent because no resorption occurred when they were absent. 32 Experiments also serially eliminated cementum, cementoid, the Malassez epithelial cell, the cementoblast, the fibroblast, the endo- thelial cell, and the perivascular cell as protec- tive agents against resorption.

Andreasen concluded that the innermost cel- lular structures-cementoblasts, fibroblasts, en- dothelial cells, and perivascular cells (ie, those nearest the root surface within the cellular re- gion of the PDL) are the likely candidates for a root resorption protective mechanism. To con- firm this, he destroyed the thin innermost cellu- lar zone within the PDL. The result was signifi- cant root resorption, implying that the protective mechanism was lost with removal of the constitu- ents of this cellular zone. is

Prevalence

The intentional movement of teeth that is the backbone of orthodontic treatment typically produces some blunting of the root apices, and, in general, tooth types that are moved the far- thest tend to show the most frequent and most severe EARR. x4,4°-42 However, it is pointless to compare the frequencies of root resorption among studies because of the diverse and gen- erally undefined criteria used to define resorp- tion. For example, Hemley 4~ found that 3% of the teeth examined of 195 orthodontic patients showed apical root resorption. Rudolph, s on the other hand, found EARR in nearly 100% of the 439 patients he treated. This extreme range is primarily due to vastly different, but generally unpublished, criteria for identification. 44

It is clear that incisors are most likely to show root EARR as well as the most advanced modal degree of resorption. 4-w47 It has not been estab- lished whether this is because these are the teeth moved the farthest or because of the single-root, spindly cone-shape of the root. Additionally, it may be that incisors possess biochemical pathways dif- ferent from other teeth that place them at risk, but there is no evidence of such a difference.

Another consideration is that resorption most often occurs at the apex. The coronal third of a root is covered with acellular cementum, whereas the apical third is cellular and the mid- dle third is intermediate. Cellular cementum

Root Resorption During O*vthodontic Therapy 185

forms m o r e rapidly and is m o r e active than acel- lular c e m e n t u m , but this cellular periapical ce- m e n t u m depends on a pa ten t vasculature; ac- cordingly, periapical c e m e n t u m is m o r e friable and easily in jured in the face o f heavy forces and concomi t an t vascular stasis. 48 no

Reitan 5~ r e p o r t e d that thickness o f c e m e n t u m s o m e h o w modula tes the resorptive process. Re- sorpt ion lacunae o c c u r r e d all a long the roo t surface o f teeth with hypercementos is ; a few la- cunae were repa i red with secondary c e m e n t u m and bone, bu t there was no loss o f roo t length. In contrast , tee th with thin layers o f c e m e n t o i d and p reden t in showed m a r k e d EARR.

Teeth Affected

Single-rooted teeth are at grea ter risk o f experi- enc ing EARR than mul t i roo ted teeth, p robab ly because o f the grea ter roo t surface area o f mo- lars for the dissipation o f forces. 4~52 O n the o the r hand, tee th in the an te r ior s egmen t are moved grea ter distances on average du r ing treat- m e n t than o the r teeth in the denta l arches, so the grea ter f r equency and grea ter moda l loss o f roo t length in the incisor may be a comb ina t i on o f bo th factors. The consensus f rom several stud- ies is that the average pat ient receiving compre- hensive t r ea tmen t will loose abou t 2 m m f rom the apex of the maxi l lau central incisor, with loss on the lateral incisor being a bit more, perhaps because o f the more spindly apical region.

Kalkwarf et aD s m o d e l e d the shape o f a max- illary lateral incisor to quantify the relat ionship be tween loss o f roo t length and loss o f surface area for a t t a chmen t (Fig 1). A l t h o u g h the rela- t ionship is essentially linear, it can also be seen

that the d r o p in surface area is no t as steep over the first few mill imeters as when m o r e roo t is resorbed. T h e r e is an inf lect ion po in t at abou t 3 m m where loss o f a t t a chmen t slows and becomes linear. O f note , abou t the first 3 m m of an incisor roo t are m o r e spindly and, perhaps, m o r e p r o n e to resorp t ion because o f its h igher ratio o f length to area than the rest o f the root. Almost all repor ts o f EARR have f o u n d average resorp t ion due to o r t h o d o n t i c t r ea tmen t to be less than 3 mm. Kalkwarffs data also address loss o f crestal b o n e support . The highes t ratio o f surface area for a t t a chmen t occurs nea r the ce- m e n t o e n a m a l j u n c t i o n , so loss o f b o n e he ight is mos t inf luential in this region. Loss o f bony suppor t opens the d o o r to d imin ished stability and to too th mobility. 54-~6 Reduc e d bony sup- po r t can increase '~iggling" too th movemen t s leading to periapical roo t resorption. ~6,5r,58 Re- searchers who have measu red b o n e suppor t in re lat ion to o r t h o d o n t i c too th m o v e m e n t r epor t a decrease relative to the adjacent cemen toe - n a m e l j u n c t i o n (CEJ); this is t rue o f incisors 56,5'-~ as well as pos te r ior teeth. 41,54,58,6°-62 Tee th used as a b u t m e n t teeth and those with considerable loss o f crestal b o n e he igh t (measured, for in- stance, by pe r iodon ta l p rob ing depth) charac- teristically show grea ter periapical resorpt ion, p resumably because o f j iggl ing forces. 41,6S-65 Considerably m o r e relat ionships between b o n e a nd den t in occur than can be covered in this br ie f review.

O n e migh t suppose that the typical f r equency o f EARR could be abstracted f rom a review of the literature. This is no t the case because o f a n u m b e r o f impor t an t differences, notably the teeth observed, the mechan ics used, the kinds o f

A Figure 1. The association between loss of root length by EARR and the percent of 100 T remaining area for attach- ~ | ment. The specific tooth is a i~ 80 maxillary lateral incisor, one of the teeth most likely to ~ | show apical resorption (A). E 60- The graph is for millimeter increments. Although the graph is essentially linear, it ~ 40- is evident that about 3 mm at "~ the apical end, because of its ~ 20- spindly shape, has the largest length to area ratio and a flatter slope (B). (Data from 0 Kalkwarf KL, Krejci RF, Pao 0 YC. 5~)

I 6 8 1'0 12

Millimeters of Root Resorption

B 100 .. 8O

60

40

20

0 14 0 2 4 6 8 10 12 14

Millimeters of Root Resorption

1 86 Edward F. Harris

radiographic data (particularly periapical v pan- oramic v cephalometric x-rays), and the sophis- tication of the measurement technique. For ex- ample, older studies used ordinal scales and only scored EARR when it was overt, 9,1° whereas Massler and Perreault 66 apparently used any sug- gestion of apical blunting as evidence of resorp- tion. There also is an important set of studies of extracted teeth in which light microscopy 91,67 or, even, scanning electron microscopy was used to evaluate the number and severity of resorption lacunae in the cementum. 2°,68,6°

Measurement Methods

EARR can be defined operationally as the de- gree a root has shortened from its original (or expected) length by elastic activity. Broadly, two methods have been used to quantify resorption: visually-assessed grades of resorption (ordinal scale data) or measurements with calipers or some computer-aided device (ratio scale data), almost always on radiographs. Another ap- proach using light or electron microscopy sel- dom has yielded quantitative results 2°,48,7°,71 although histomorphometr ic methods are be- ginning to be used. 72-74

Morphological scales, such as in Figure 2, are easy to use because they depend on shape crite- ria rather than size, so measurements are unnec- essary and there is less concern about standard- ization of orientation of the tooth r o o t s . 56,75,76

The negative aspect is that the data are ordi-

0 1 2 3

f ' \

ml 4

Figure 2. The ordinal scale used to score the extent of external apical root resorption. Grade 0 depicts normal, intact root morphology, in which the apical outline is smooth and continuous. Also, the distance between the root and the lamina dura is uniform. Grade 1 shows evidence of erosion periapically, but root length probably is not yet affected. Grade 2 shows scalloping and blunting of the apex. Grade 3 occurs when at least one-fourth of the root has been resorbed. Grade 4 involves the loss of at least one-half the original root length. (Reprinted with permission from Levander E, Malmgren O.S°).

nal scale, which can limit some statistical ap- proaches and there is the opportunity for differ- ences within and among examiners because of inaccuracies in defining, and discriminating be- tween grades of resorption.

Various approaches have been used to mea- sure root length. Dental radiographs can be measured directly with calipers, al though enlarg- ing the image will decrease error in landmark identification. It now is generally practical to capture the radiographic image with a scanner or import the image from a digital x-ray machine and make the measurements on a computer screen with any of several software packages.

Radiography

The key to measuring tooth dimensions and, thus, loss of root length is standardization of the radiographs to, hopefully, eliminate foreshort- ening and differences in the aspect of the x-ray source to the tooth. Panoramic radiographs are not well-suited for this because the focal t rough is not identical to the shape of the individual's dental arch, so there is variable enlargement of each tooth and variable orientation to each tooth. 77 Different sizes and shapes of arches will also be variably magnified and again there are variable source-object differences for each tooth among individuals.

Periapical x-rays, particularly with a long-cone technique, offer greater flexibility in standardizing orientation to each tooth. However, there com- monly are problems with ectopic and rotated teeth in patients before orthodontic treatment. Some researchers have gone to the effort of fabricating a jig for each tooth 62,78,79 but Melsen 62 concluded that, "the benefit of this method was considered limited in relation to the resources used." A com- mercially available guide that substantially im- proves repeatability in conjunction with the long- cone paralleling technique is the Rinn xcp instrument for extension cone paralleling tech- nique (Rinn Corporation, Elgin, IL). SjMien and Zachrisson 6°,61 described a method of correcting for tooth and crestal bone height due to diver- gence of the x-rays emanating from the source.

Dermaut and De Munck 82 published formulae that correct for angulation of a tooth relative to the x-ray film, at least as compared to a prior film:

(Crown A × Root B ) / ( R o o t A × CrownB)

= Root B /Root A

Root Resorption During Orthodontic Therapy 187

in which "crown" is the distance from the inci- sive edge to the cementoenamel juncf ion, "root" is the distance from the CEJ to the root apex, and A and B are two examinations, such as pre- treatment and posttreatment. The adjustment is a decimal equivalent of how much root length at time B differs from that at time A having cor- rected for differences in parasagittal angulafion. With EAR.R, the ratio (right side of equation) will be less than 1. Similar ratios have been published by Linge and Linge H as well as Costo- poulos and Nanda. 77

Occlusal Forces

Heavy mastication, occlusal trauma, and chronic bruxism each increases the risk of root resorp- tion. 57,67,s3-86 Heavy mastication can produce loss of periapical root substance. Baden 8v inferred that stunting of the developing root occurs when excessive intrusive forces are introduced to the tooth during development. Gottlieb and Or- ban 88 and Dellinger s9 previously had produced this effect in laboratory animals. Improper oc- clusion or inadequate dental restorations and prosthetic appliances can also cause occlusal trauma and 'jiggling" forces that promote root resorption. 9°,°1 Glickman 9z found a high fre- quency of EARR in roots of long-term abutment teeth. He speculated that this occurs because rel- atively normal teeth are carrying abnormally greater occlusal loads when used as bridge abut- ments.

Adolescents with anterior open bites present to the orthodontist with significantly shorter roots, a greater frequency of EARR, and significantly less facial bony support compared with comparable patients with a positive overbite. 59 Linge and Linge 11 found a positive association between EARR and lip and tongue dysfunction as well as an association between resorption and a history of finger-sucking habits persisting beyond age 7. In the same vein, children who are chronic nail biters exhibit more EARR than controls. 9a,94 Teeth used as abutments tend to experience resorption. 58 The common cause seems to be the orthopedic forces produced by repetitive clenching, thumb or digit sucking, and tongue thrusting associated with chronic mouth breathing.

Normal Events of Aging

With increases in the median age of the US population and more adults seeking orthodon-

tic care, it is of interest whether loss of root length is a natural function of aging. The answer is "No." Woods et a195 tested for an effect using cross-sectional data on adults. They found no age-dependent t rend between root length and age in people not treated orthodontically, but it was also obvious that interindividual variation in root length was so great that only a substantial amount of shortening would be detectable. The only longitudinal study seems to be that of Bishara et a196 who compared measurements taken from periapical radiographs of or thodon- tically untreated adults at 25 and again at 45 years of age. From comparisons of all tooth types except third molars, they concluded that root length remained constant throughout the age range studied. The authors noted that this is a pert inent clinical finding because the or thodon- tist can be assured that no systematic loss of root length will occur posttreatment.

The caveat, however, is that the apparent lack of root shortening seen in the United States and other westernized countries is probably a fairly recent p h e n o m e n o n brought on by the supplan- tation of a highly refined diet, requiring very small axial forces on the teeth and producing trivial apical resorption. In prior eras and in unacculturated societies when most food pro- cessing was done in the mouth by the dentition (rather than by machines before ingestion), tooth roots were shorter and blunter. 83,97-99

Predictors of EARR

There is considerable variation in the amount of root resorption among patients treated orthodon- tically, even when age, sex, nature of the malocclu- sion, and type of treatment are held constant. The differences in patient response would seem to be due to differences intrinsic to the individual. The search for key biological factors governing suscep- tibility has been ongoing for over half a century, but without a great deal of success.

Sex of the patient is a variable easily obtained and tested, but the consensus is that neither sex is more prone to resorption. 12,47,56,1°°-1°z Of the few studies that have reported a sex difference, most found that females were more susceptible to root resorption. 66,1°~-1°5 Even if there is a sex difference, it is trivial because in the best of cases, sex accounts for little of the total variation, and no study design to date has accounted for the powerful difference in compliance between adolescent boys and girls. In addition, it does

188 Edward F. Ha,~is

not appear that any study has accounted for severity of the malocclusion, which tends to be greater in male orthodontic patients, al though not in the population at large.

It is well documented that males have signif- icantly longer roots on all tooth types, 95A°6 so in theory, females should lose a greater proport ion of root length than males. This is not the case, however, because the association between root length and the amount of resorption during treatment is essentially zero.

The risk of EARR also seems to be indepen- dent of age once the teeth have completed root formation. There are several reasons to antici- pate that adults would be more susceptible. Rates of alveolar turnover are slower in older adolescents and adults than in children and young adolescents. 1°7-~° Young persons possess more loose fibrous tissue in their alveolar bone. 2 Young teeth have more cellular cementum in the apical region, which depends more on a patent vascular supply than mature acellular ce- mentum, which is thicker in adults. Initiation of tooth movement is slower in adults, 1°7,m per- haps because of their dense lamellar bone in their alveolar structures. Tooth movement gen- erally is greater in adults because they are not growing, n2 Taken together, adults are specu- lated to be at greater risk for root resorption.

One study that explicitly compared the extent of resorption in adolescents and adults treated by a single orthodontist found that the 2 age groups lost equivalent amounts of root length. 56 On the other hand, adults bad substantially more resorption at the onset of treatment, pre- sumably from wear and tear on the roots be- tween when the adults were adolescents and when they began treatment. Mirabella and ~r- tun n4 performed an extensive study of EARR in adult or thodontic patients, but without an ado- lescent comparison.

The effect of age is quite different when dealing with children in the mixed dentition. Children treated before their roots are completely formed encounter less r o o t r e so rp t ion . 27,7°,114,115 After treatment, although the roots are not as apt to show blunting, they are shorter. The suggestion is that orthodontic treatment slowed root grouch of the forming teeth, but subsequent root growth obliterated effects of dentinoclasia, leaving the roots with reduced final lengths. 55,1u~ Some re- searchers have used this difference to promote treatment of patients at earlier ages. 8,45,~16 Case control studies have disclosed 2 other risk factors,

namely evidence of prior root resorption and ab- errant root forms. EARR that is evident before treatment is indicative of an increased susceptibil- ity to moderate-to-severe root resorption during full-banded treatment, n,76

Levander and Malmgren 76 conducted one of the more thorough assessments of root form and its susceptibility to EARR. They scored incisor roots as normal, short, blunt, apically bent (of- ten mistakenly termed dilaceration), and pipette shape (Fig 3). Similar depictions are published by Mirabella and flkrtun. 113 Reassessment of Levander and Malmgren's published data using contingency tables (a = 0.05) shows quite clearly that irregular root form is a risk factor and obviously, it is identifiable before treatment. All 4 varieties of root form increase the risk and severity of EARR over roots with normal mor- phology: short roots (X 2 = 18.0; P < 0.001); blunt roots (X 2 = 34.3; P < 0.001), apically bent roots (X 2 = 18.0; P < 0.001), and pipette shape roots (1 ̀2 = 45.0; P < 0.001).

Cortical Plate

Certain directions of tooth movement, notably intrusion, have been found to increase the risk and severity of EARR. The first orthodontists to describe the association between treatment and resorption, Ottolengui, 117 Oppenheim, 118 and Ketcham 9 noted that of the several possible modes of movement, intrusion and heavy tip- ping forces are the most likely to cause notice- able apical resorption. Intrusion damages the root apex because root shape concentrates pres- sure at the conical root tip. 7° Several studies have measured the vertical, horizontal, and an- gular changes in the maxillary incisor viewed in

Short Blunt Apical Pipette Bend Shape

Figure 3, Variant root shapes, such as the four shown here, are significantly more likely to show EARR dur- ing the course of orthodontic treatment than nor- mal-shape roots. (Reprinted with permission from Levander E, Malmgren 0. 8°)

Root Resorption During Orthodontic Therapy 189

norma lateralis. 4°,m,n3,n9 There is a positive cor- relation between the amount of resorption and the amount of intrusion. Parker and Harris 14 also found consistent correlations between EARR and incisor proclination. Mirabella and fi~rtun stated, "Movement of the roots in either an anterior or posterior direction is associated with root resorption." Although they found no significant association between vertical movement of the incisor apex and root resorption, they cau- tioned that few of their patients experienced as much as 1 mm of extrusion or intrusion.

EARR also is a function of the amount of apical movement. Sharpe et a141 reported that incisors experienced more EARR in premolar extraction cases in which retraction is greater than in nonex- traction cases. Similarly, cases with anterior open- bites (apertognathia) lose more root length than cases requiring less incisor movement, u,5-~,94 Linge and Linge u as well as Beck and Harris 12 found highly significant, positive associations between periapical resorption and both overjet and the AOBO discrepancy. The common theme here is that the amount of movement is itseff predictive of the degree of resorption to occur.

An important related issue is that tooth roots are prone to resorption when they are pushed out of the alveolar through and toward the less resilient cortical bone. 42A2°,191 Attention has fo- cused on the incisor root being pushed against the lingual cortical plate, but the risk probably is as great for the labial plate and, in instances of marked intrusion, for the nasal floor, s2 Likewise, Vardimon et a1122q23 have shown that roots of buccal teeth are resorbed with rapid maxillary expansion. It would be of interest to quantify the consequences of buccal tooth root lengths with the bioprogressive technique 124 in which the buccal molar roots are moved toward the corti- cal plates for anchorage.

Effects of intrusion also are evident on teeth besides the incisors. The extent of EARR on the roots of the maxillary molars used as anchorage has been studied, and the location and degree of resorption depends on the malocclusion? 2 More resorption occurs on the distal molar root when the bite is opened (as in cases with deep- bites). Anchorage bends mesial of the maxillary first molar intrude the anterior teeth, but they also compress the distal root of the molar into the socket (Fig 4A). The deeper the bite, the greater the tip back placed in the wire, and the greater the compression of the distal root before correction of the deep bite is achieved. Con- versely, in open bite cases and in cases with overjet that needs to be reduced (Fig 4B), the mesial molar root is intruded and experiences more EARR than the distal root. Consequently, the first molar provides an informative model of the effects of intrusion (producing resorption) compared with extrusion, which appears to be protective of the root. Reitan a,a25 came to the same conclusion from histologic analysis of hu- man premolars. Dougherty 1°3 and Sj~lien and Zachrisson 6°,61 also remarked on this association, showing that where maximum anchorage was pre- pared, the greatest resorption occurred on the distal (intruded) root of mandibular molars.

Familial Factors

A scattering of studies over the past several de- cades has suggested a familial predisposition for root resorption. 9,66,1°5,n6,12(~ It is clear that sus- ceptibility does not depend on segregation of a simple Mendelian gene, either dominant or re- cessive. Instead, inheritance is multifactorial (polygenic), al though no one has yet tested for a major gene effect.

Figure 4. Different conse- quences to the mesial and distal roots of the maxillary first molar depending on the mechanics used (A and B). Comparison shows the re- sorption-promoting effects of intrusion and the pro- tective effects of extrusion. (Drawn from Beck BW, Har- ris EF.12).

A 13 ~ Intrusion Intrusion ~ IExtrusion Extrusion and and Resorption Resor \

eR ! I Incisor R~action Intrusion

\ J

190 Edward F. Harris

Figure 5. Posttreatment close- ups of cephalograms of 2 broth- ers showing the similarity in the extreme degree of root resorp- tion, which is suggestive of an inherited susceptibility to loss of root length in the face of orthodontic stressors.

In a study of 320 t rea ted o r t hodon t i c patients, only 2 cases showed ex t reme incisor roo t resorp- t ion (Fig 5). O n inspect ion, the 2 cases were brothers , which init iated a formal search for a heri table c o m p o n e n t fo r EARR a m o n g sib- lings, lu7 Measurements on 3 roots in a large series o f siblings, all o f w h o m had received com- prehensive o r t h o d o n t i c t rea tment , p r o d u c e d heritability estimates on the o rde r o f 70% (Fig 6). This means that abou t two-thirds o f the total variance in roo t resorp t ion was a c c o u n t e d for by the siblings in each family shar ing hal f o f their genes in c o m m o n by descent . It is, then, pr imar- ily b iochemical ly based risk factors that m o d u - late a given pat ient ' s resorp t ion potent ia l du r ing t rea tment . This f inding also absolves the orth- odont i s t o f the bulk o f responsibili ty for the ex tent o f resorpt ion. O n the o the r hand , the clinician still bears responsibil i ty for m o n i t o r i n g the teeth du r ing the course o f t reatment . 12s

The clinical re levance is tha t the association be tween siblings is h igh e n o u g h that the best

available p red ic to r o f one pe r son ' s susceptibility to EARR is a p r io r sibling exper ience in treat- ment . O f m o r e long- te rm impor t ance is recog- ni t ion that a search for b iochemica l markers (eg, in crevicular fluid) would be fruitful. Th e goal would be to have a sc reening m e t h o d to identify those few patients who are at par t icular risk o f EARR dur ing t reatment . Prel iminary re- sults address ing this issue have already be pub- lished. 129q33

Periodic Evaluat ion

It is no t the average o r t hodon t i c pat ient who presents a p rob lem in terms o f roo t resorpt ion, as 1 to 2 m m of apical roo t loss seems inconse- quential , part icularly in l ight o f the funct ional and esthetic benefi ts o f o r t hodon t i c t reatment ; instead, it is the u n c o m m o n individual who loses considerable roo t length a l though the na ture o f the malocclus ion and the t r ea tmen t seem unre- markable . T M These individuals c anno t be iden-

1.0 / Figure 6. Heritability esti- ~>'0"81 mates plus 95% confidence ~ 0-61 limits for EARR on three 1 roots. In each case, the esti- ~ 0.4J mate is significantly different / from zero; the mean h 2 of all 0.2J 3 roots is 70%. (Data from | Harris EF, Kineret SE, Tolley 0 0 EA.127) M;~ MX Central Incisor MD Molar, Mesial MD Molar, Distal

Root Resotption During Orthodontic Therapy 191

t i f fed g i v e n t h e p r e s e n t s t a t e o f k n o w l e d g e , b u t

t h e r e a r e s o m e p r e c a u t i o n s t h a t c a n b e t a k e n .

Periodic periapical radiographs of the maxillary incisors (the most susceptible teeth) at approx- imately 6-month intervals will flag those uncom- mon cases, 76,a35 and the operator has at least 4 options. The least satisfactory choice is to ignore the evidence and proceed as usual. 12s In fact, this is identical to treatment without interim radiographs. Second, the rate of tooth move- ment can be slowed along using lighter forces, so that the reparative process of the cementum can keep abreast of the erosive processes of over- compressing the PDL and forcing the root against the alveolus. 136,137 Third, "rest periods" can be built into treatment, 8° that is, the tooth is moved, then forces are minimized with passive arch wires for 2 to 3 months to allow root repair, then movement is resumed. It has been shown in animal models 123,a3s and humans t,7,s° that a force-free "rest period" allows the cementum to recover the exposed dentin, thus improving root length at the end of treatment. A pause also permits repair of the necrotic hyalinization zone, including central tissue zones in the PDL that appear to be protective of the root. 7,18 A fourth option in the face of severe resorption, is to compromise treatment, to stop short of the treatment goals for the sake of the supporting root structure.

Overview

External apical root resorption is the most com- mon iatrogenic consequence of orthodontic treat- ment, but it is seldom severe enough to compro- mise treatment or a tooth's longevity. The most common kind of root resorption occurs on the external periapical surfaces of single-rooted teeth, especially if the tooth has a variant root form, such as being narrow or apically bent. The tissue that normally protects cementum from being eroded seems to reside in the root side of the cellular region of the PDL, but the tissue and its apocrine signals have not been isolated. Description and analysis of EARR extends throughout this century, but few variables are clinically valuable as predic- tors of EARR because of the large interindividual variation in response to treatment. An individual's genetic background is the single strongest predic- tor of resorption, as shown by familial analysis. This suggests that research will lead to a biochem- ical assay, perhaps of crevicular fluid, that would

flag patients at particular risk of EARR. Such re- search is ongoing.

Acknowledgment The author thanks former students who conducted research on root resorption: Dr Barry Beck, Dr Stephen Kineret, Dr Dale Wheeler, Dr Brandon Boggan, and Dr Robert Parker.

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