Root Resorption During Orthodontic Therapy

Edward F. Harris
External apical root resorption (EARR) is the most common iatrogenic consequence of orthodontics, and orthodontics is the most common cause of EARR. Localized root resorption is a normal and constant remodeling process, a response to oral microtraumas throughout life. Roots do not shorten naturally with age unless forces (eg, bruxism, tongue thrusting) overcompress the periodontal ligament. Appositional repair normally corrects resorptive defects. Irreversible root shortening occurs with excessive forces or decreased resistance to normal forces. Orthodontically induced root resorption starts adjacent to hyalinized zones and occurs during and after elimination 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 distance the apex is moved is often correlated with the degree of root shortening. 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 periodically. 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

o o t r e s o r p t i o n occurs w h e n pressure o n the c e m e n t u m exceeds its reparative capacity a n d d e n t i n is exposed, allowing multinucleated odontoclasts to degrade the r o o t substance. 1,2 O r t h o n d o n t i c a l l y i n d u c e d r o o t r e s o r p t i o n begins adjacent to hyalinized zones a n d occurs d u r i n g a n d after elimination o f hyaline tissues? Removal o f hyalinized tissue (ie, a z o n e o f sterile necrosis) leads to removal o f c e m e n t o i d a n d m a t u r e collagen, leaving a raw c e m e n t a l surface that is readily attacked by dentinoclasts. 4 T h e r e is a positive association between removal o f hya-

From the Department of Orthodontics, Collegeof Dentistu, University 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 n e c r o t i c tissue a n d r o o t resorption. 5-7 Because c e m e n t u m n o r m a l l y is m o r e resistant t h a n b o n e , forces applied to a t o o t h usually cause b o n e r e s o r p t i o n r a t h e r t h a n loss o f c e m e n t u m . However, forces are c o n c e n t r a t e d at the r o o t a p e x because o r t h o d o n t i c t o o t h m o v e m e n t is never entirely translatory, which places the narrow periapical r e g i o n in h a r m ' s way. R u d o l p h 8 n o t e d that r e s o r p t i o n typically attacks the r o o t tip a n d travels coronally, m a k i n g what has b e e n t e r m e d a "shed r o o f ' effect to the root. T h e p o r t i o n o f the r o o t nearest the p u l p a p p e a r s to be the last to give way. This process is exactly opposite to that o f t o o t h f o r m a t i o n . Albert K e t c h a m '-~,~0was the first to b r i n g the message that apical r e s o r p t i o n is a c o m m o n a n d occasionally severe iatrogenic c o n s e q u e n c e o f o r t h o d o n t i c treatment. A d v e n t o f the c o m m o n place use o f dental x-ray e q u i p m e n t m a d e it possible for K e t c h a m to evaluate a large series o f treated cases. K e t c h a m also m a d e a less well183

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Edward K Harris

known discovery, namely that the appliance used to move teeth influences the risk of root resorption. 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 c e m e n t u m b r o a d e n and permit dentinoclasia. Surface resorption can occur anywhere on a root but is most c o m m o n periapically. 2 Surface resorption stops when the instigating agent (usually pressure) is removed and there is repair of the cementum. 2-~95 Inflammatory 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 b o n e 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 researchers agree that odontoclasts are of hematopoietic origin from the bone marrow and dissemination of their precursors is through the vascular system, 2s so but a local tissue contribution has not been ruled O U t . 18,~-31 Andreasen et al conducted a series of illuminating experiments to determine which tissue protects 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 irreversible external apical root resorption (EARR)? Andreasen reasoned that the following cell types and structures could provide a protective mechanism from irreversible EARR: cementoblasts, fibroblasts, osteoblasts, vascular endothelial cells, perivascular cells, Malassez epithelial cells, cementum, cementoid, osteoid, alveolar b o n e or Sharpey's fibers, or a combination of these tissues, is To narrow the possibilities, Andreasen 35,36 first removed the c e m e n t u m side and then the alveolar bone side of the periodontal membrane. In both instances, little resorption occurred, and he inferred that the protective structure was in a central region of the

periodontal membrane. Sharpey's fibers (located in the innermost and outermost regions of the periodontal ligament [PDL], which are acellular) 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 endothelial cell, and the perivascular cell as protective agents against resorption. Andreasen concluded that the innermost cellular structures-cementoblasts, fibroblasts, endothelial cells, and perivascular cells (ie, those nearest the root surface within the cellular region of the PDL) are the likely candidates for a root resorption protective mechanism. To confirm this, he destroyed the thin innermost cellular zone within the PDL. The result was significant root resorption, implying that the protective mechanism was lost with removal of the constituents of this cellular zone. is

Prevalence
The intentional m o v e m e n t 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 farthest tend to show the most frequent and most severe EARR. x4,4-42 However, it is pointless to compare the frequencies of root resorption a m o n g studies because of the diverse and generally undefined criteria used to define resorption. For example, Hemley 4~ f o u n d that 3% of the teeth examined of 195 orthodontic patients showed apical root resorption. Rudolph, s on the other hand, f o u n d 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 established 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 different from other teeth that place them at risk, but there is no evidence of such a difference. A n o t h e r 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 middle third is intermediate. Cellular c e m e n t u m

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forms m o r e rapidly a n d is m o r e active than acellular c e m e n t u m , but this cellular periapical cem e n t u m d e p e n d s o n a p a t e n t vasculature; accordingly, periapical c e m e n t u m is m o r e friable a n d easily i n j u r e d in the face o f heavy forces a n d c o n c o m i t a n 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 m o d u l a t e s the resorptive process. Resorption l a c u n a e o c c u r r e d all a l o n g the r o o t surface o f teeth with h y p e r c e m e n t o s i s ; a few lac u n a e were r e p a i r e d with s e c o n d a r y c e m e n t u m a n d bone, b u t there was n o loss o f r o o t length. I n contrast, teeth with thin layers o f c e m e n t o i d a n d p r e d e n t i n s h o w e d m a r k e d EARR.

Teeth Affected
Single-rooted teeth are at g r e a t e r risk o f experie n c i n g EARR t h a n m u l t i r o o t e d teeth, p r o b a b l y because o f the g r e a t e r r o o t surface area o f m o lars for the dissipation o f forces. 4~52 O n the o t h e r h a n d , teeth in the a n t e r i o r s e g m e n t are m o v e d g r e a t e r distances o n average d u r i n g treatm e n t t h a n o t h e r teeth in the dental arches, so the g r e a t e r f r e q u e n c y a n d g r e a t e r m o d a l loss o f r o o t l e n g t h in the incisor may be a c o m b i n a t i o n o f b o t h factors. T h e consensus f r o m several studies is that the average patient receiving c o m p r e hensive t r e a t m e n t will loose a b o u t 2 m m f r o m the apex of the m a x i l l a u central incisor, with loss o n the lateral incisor being a bit more, perhaps because o f the m o r e spindly apical region. Kalkwarf et aD s m o d e l e d the shape o f a maxillary lateral incisor to quantify the relationship b e t w e e n loss o f r o o t l e n g t h a n d loss o f surface area for a t t a c h m e n t (Fig 1). A l t h o u g h the relationship is essentially linear, it can also be seen

that the d r o p in surface area is n o t as steep over the first few millimeters as w h e n m o r e r o o t is resorbed. T h e r e is an inflection p o i n t at a b o u t 3 m m w h e r e loss o f a t t a c h m e n t slows a n d b e c o m e s linear. O f note, a b o u t the first 3 m m o f an incisor r o o t are m o r e spindly and, perhaps, m o r e p r o n e to r e s o r p t i o n because o f its h i g h e r ratio o f l e n g t h to area than the rest o f the root. Almost all reports o f EARR have f o u n d average r e s o r p t i o n d u e to o r t h o d o n t i c t r e a t m e n t to be less t h a n 3 m m . Kalkwarffs data also address loss o f crestal b o n e support. T h e highest ratio o f surface area for a t t a c h m e n t occurs n e a r the cem 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 h e i g h t is m o s t influential in this region. Loss o f b o n y s u p p o r t o p e n s the d o o r to d i m i n i s h e d stability a n d to t o o t h mobility. 54-~6 R e d u c e d b o n y supp o r t can increase '~iggling" t o o t h m o v e m e n t s leading to periapical r o o t resorption. ~6,5r,58 Researchers w h o have m e a s u r e d b o n e s u p p o r t in relation to o r t h o d o n t i c t o o t h m o v e m e n t r e p o r t a decrease relative to the adjacent c e m e n t o e n a m e l j u n c t i o n (CEJ); this is true o f incisors 56,5'-~ as well as p o s t e r i o r teeth. 41,54,58,6-62 T e e t h used as a b u t m e n t teeth a n d those with considerable loss o f crestal b o n e h e i g h t (measured, for instance, by p e r i o d o n t a l p r o b i n g d e p t h ) characteristically show g r e a t e r periapical resorption, p r e s u m a b l y because o f jiggling forces. 41,6S-65 Considerably m o r e relationships between b o n e a n d d e n t i n o c c u r t h a n can be covered in this b r i e f review. O n e m i g h t suppose that the typical f r e q u e n c y o f EARR c o u l d be abstracted f r o m a review o f the literature. This is n o t the case because o f a n u m b e r o f i m p o r t a n t differences, notably the teeth observed, the m e c h a n i c s used, the kinds o f

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

A
100 T ~ | i~ 80 ~ | E 60~ 40"~ ~ 200 0

100 ..
8O 60 40

20 0

6 8 1'0 12 14 Millimeters of Root Resorption

2 4 6 8 10 12 14 Millimeters of Root Resorption

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Edward F. Harris

radiographic data (particularly periapical v panoramic v cephalometric x-rays), and the sophistication of the m e a s u r e m e n t technique. For example, older studies used ordinal scales and only scored EARR when it was overt, 9,1 whereas Massler and Perreault 66 apparently used any suggestion o f apical blunting as evidence of resorption. There also is an important set of studies of extracted teeth in which light microscopy91,67 or, even, scanning electron microscopy was used to evaluate the n u m b e r and severity of resorption lacunae in the cementum. 2,68,6

Measurement Methods
EARR can be defined operationally as the degree 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. A n o t h e r approach using light or electron microscopy seld o m has yielded quantitative results 2,48,7,71 although histomorphometric methods are beginning to be used. 72-74 Morphological scales, such as in Figure 2, are easy to use because they d e p e n d on shape criteria rather than size, so measurements are unnecessary and there is less c o n c e r n about standardization of orientation o f the tooth r o o t s . 56,75,76 The negative aspect is that the data are ordi-

nal scale, which can limit some statistical approaches and there is the opportunity for differences within and a m o n g examiners because of inaccuracies in defining, and discriminating between grades of resorption. Various approaches have been used to measure root length. Dental radiographs can be measured directly with calipers, although enlarging 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 c o m p u t e r screen with any of several software packages.

Radiography
The key to measuring tooth dimensions and, thus, loss of root length is standardization o f the radiographs to, hopefully, eliminate foreshortening and differences in the aspect of the x-ray source to the tooth. Panoramic radiographs are not well-suited for this because the focal trough 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 s o u r c e - o b j e c t differences for each tooth a m o n g individuals. Periapical x-rays, particularly with a long-cone technique, offer greater flexibility in standardizing orientation to each tooth. However, there commonly 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 commercially available guide that substantially improves repeatability in conjunction with the longcone paralleling technique is the Rinn xcp instrument for extension cone paralleling technique (Rinn Corporation, Elgin, IL). SjMien and Zachrisson 6,61 described a method of correcting for tooth and crestal bone height due to divergence 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 / R o o t A

f'\

ml
0 1 2 3 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).

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in which "crown" is the distance from the incisive edge to the c e m e n t o e n a m e l j u n c f i o n , "root" is the distance from the CEJ to the root apex, and A and B are two examinations, such as pretreatment and posttreatment. The adjustment is a decimal equivalent of how m u c h root length at time B differs from that at time A having corrected 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 Costopoulos and Nanda. 77

Occlusal Forces
Heavy mastication, occlusal trauma, and chronic bruxism each increases the risk of root resorption. 57,67,s3-86Heavy mastication can p r o d u c e 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 Orban 88 and Dellinger s9 previously had p r o d u c e d this effect in laboratory animals. I m p r o p e r occlusion or inadequate dental restorations and prosthetic appliances can also cause occlusal trauma and 'jiggling" forces that p r o m o t e root resorption. 9,1 Glickman 9z f o u n d a high frequency of EARR in roots of long-term abutment teeth. He speculated that this occurs because relatively normal teeth are carrying abnormally greater occlusal loads when used as bridge abutments. 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 c o m m o n cause seems to be the orthopedic forces produced by repetitive clenching, thumb or digit sucking, and tongue thrusting associated with chronic mouth breathing.

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 f o u n d no age-dependent trend 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 a m o u n t of shortening would be detectable. The only longitudinal study seems to be that of Bishara et a196 who c o m p a r e d measurements taken from periapical radiographs o f orthodontically 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 t h r o u g h o u t the age range studied. The authors n o t e d that this is a pertinent clinical finding because the orthodontist 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 b r o u g h t on by the supplantation of a highly refined diet, requiring very small axial forces on the teeth and p r o d u c i n g trivial apical resorption. In prior eras and in unacculturated societies when most food processing was d o n e in the m o u t h 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 orthodontically, even when age, sex, nature of the malocclusion, 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 susceptibility 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 p r o n e to resorption. 12,47,56,1-1z O f the few studies that have reported a sex difference, most f o u n d that females were more susceptible to root resorption. 66,1~-15 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

Normal Events of Aging

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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, although not in the population at large. It is well d o c u m e n t e d that males have significantly longer roots on all tooth types, 95A6 so in theory, females should lose a greater p r o p o r t i o n of root length than males. This is not the case, however, because the association between root length and the a m o u n t of resorption during treatment is essentially zero. The risk of EARR also seems to be independent of age once the teeth have completed root formation. There are several reasons to anticipate that adults would be more susceptible. Rates of alveolar turnover are slower in older adolescents and adults than in children and y o u n g adolescents. 17-~ Young persons possess more loose fibrous tissue in their alveolar bone. 2 Young teeth have more cellular c e m e n t u m in the apical region, which depends more on a patent vascular supply than mature acellular cementum, which is thicker in adults. Initiation of tooth m o v e m e n t is slower in adults, 17,m perhaps because of their dense lamellar bone in their alveolar structures. T o o t h m o v e m e n t generally is greater in adults because they are not growing, n2 Taken together, adults are speculated to be at greater risk for root resorption. One study that explicitly c o m p a r e d the extent of resorption in adolescents and adults treated by a single orthodontist f o u n d 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, presumably from wear and tear on the roots between when the adults were adolescents and when they began treatment. Mirabella and ~rtun n4 p e r f o r m e d an extensive study of EARR in adult orthodontic patients, but without an adolescent 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 s o r p t i o n . 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 researchers 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 aberrant root forms. EARR that is evident before treatment is indicative of an increased susceptibility to moderate-to-severe root resorption during full-banded treatment, n,76 Levander and Malmgren 76 conducted one of the more t h o r o u g h assessments of root form and its susceptibility to EARR. They scored incisor roots as normal, short, blunt, apically bent (often 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 morphology: short roots (X2 = 18.0; P < 0.001); blunt roots (X2 = 34.3; P < 0.001), apically bent roots (X2 = 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 f o u n d to increase the risk and severity of EARR. The first orthodontists to describe the association between treatment and resorption, Ottolengui, 117 O p p e n h e i m , 118 and Ketcham 9 noted that of the several possible modes of movement, intrusion and heavy tipping forces are the most likely to cause noticeable apical resorption. Intrusion damages the root apex because root shape concentrates pressure at the conical root tip. 7 Several studies have measured the vertical, horizontal, and angular changes in the maxillary incisor viewed in

Short

Blunt

Apical Bend

Pipette Shape

Figure 3, Variant root shapes, such as the four shown here, are significantly more likely to show EARR during the course of orthodontic treatment than normal-shape roots. (Reprinted with permission from Levander E, Malmgren 0. 8)

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n o r m a lateralis. 4,m,n3,n9 There is a positive correlation between the a m o u n t of resorption and the a m o u n t of intrusion. Parker and Harris 14 also f o u n d 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 cautioned that few of their patients experienced as much as 1 m m 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 nonextraction cases. Similarly, cases with anterior openbites (apertognathia) lose more root length than cases requiring less incisor movement, u,5-~,94Linge 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 c o m m o n 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 p r o n e to resorption when they are pushed out of the alveolar through and toward the less resilient cortical bone. 42A2,191 Attention has focused 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 cortical 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 o p e n e d (as in cases with deepbites). Anchorage bends mesial o f 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. Conversely, in o p e n 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) c o m p a r e d with extrusion, which appears to be protective of the root. Reitan a,a25 came to the same conclusion from histologic analysis of human premolars. Dougherty 13 and Sj~lien and Zachrisson 6,61 also remarked on this association, showing that where maximum anchorage was prepared, the greatest resorption occurred on the distal (intruded) root of mandibular molars.

Familial Factors
A scattering of studies over the past several decades has suggested a familial predisposition for root resorption. 9,66,15,n6,12(~ It is clear that susceptibility does not d e p e n d on segregation of a simple Mendelian gene, either d o m i n a n t or recessive. Instead, inheritance is multifactorial (polygenic), although no one has yet tested for a major gene effect.

A
Figure 4. Different consequences to the mesial and distal roots of the maxillary first molar depending on the mechanics used (A and B). Comparison shows the resorption-promoting effects of intrusion and the protective effects of extrusion. (Drawn from Beck BW, Harris EF.12).

13
Incisor Intrusion

Intrusion and ~ IExtrusion Resor

~ Extrusion
eR ! I

Intrusion and Resorption

R~action
\J

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Edward F. Harris

Figure 5. Posttreatment closeups of cephalograms of 2 brothers showing the similarity in the extreme degree of root resorption, which is suggestive of an inherited susceptibility to loss of root length in the face of orthodontic stressors.

I n a study o f 320 treated o r t h o d o n t i c patients, only 2 cases s h o w e d e x t r e m e incisor r o o t resorption (Fig 5). O n inspection, the 2 cases were brothers, which initiated a formal search for a heritable c o m p o n e n t f o r EARR a m o n g siblings, lu7 M e a s u r e m e n t s o n 3 roots in a large series o f siblings, all o f w h o m h a d received comprehensive o r t h o d o n t i c treatment, p r o d u c e d heritability estimates on the o r d e r o f 70% (Fig 6). This m e a n s that a b o u t two-thirds o f the total variance in r o o t r e s o r p t i o n was a c c o u n t e d for by the siblings in each family sharing half o f their genes in c o m m o n by descent. It is, then, primarily biochemically based risk factors that m o d u late a given patient's r e s o r p t i o n potential d u r i n g treatment. This finding also absolves the ortho d o n t i s t o f the bulk o f responsibility for the e x t e n t o f resorption. O n the o t h e r h a n d , the clinician still bears responsibility for m o n i t o r i n g the teeth d u r i n g the course o f treatment. 12s T h e clinical relevance is that the association b e t w e e n siblings is h i g h e n o u g h that the best 1.0

available p r e d i c t o r o f o n e p e r s o n ' s susceptibility to EARR is a p r i o r sibling e x p e r i e n c e in treatm e n t . O f m o r e l o n g - t e r m i m p o r t a n c e is recognition that a search for b i o c h e m i c a l markers (eg, in crevicular fluid) would be fruitful. T h e goal would be to have a s c r e e n i n g m e t h o d to identify those few patients w h o are at particular risk o f EARR d u r i n g treatment. Preliminary results addressing this issue have already be published. 129q33

Periodic E v a l u a t i o n
It is n o t the average o r t h o d o n t i c patient who presents a p r o b l e m in terms o f r o o t resorption, as 1 to 2 m m o f apical r o o t loss seems inconsequential, particularly in light o f the functional a n d esthetic benefits o f o r t h o d o n t i c treatment; instead, it is the u n c o m m o n individual w h o loses considerable r o o t l e n g t h a l t h o u g h the n a t u r e o f the malocclusion a n d the t r e a t m e n t seem unremarkable. T M T h e s e individuals c a n n o t be iden-

/
1

Figure 6. Heritability estimates plus 95% confidence limits for EARR on three roots. In each case, the estimate is significantly different from zero; the mean h 2 of all 3 roots is 70%. (Data from Harris EF, Kineret SE, Tolley EA.127)

~>'0"81 ~ 0-61 ~ 0.4J

0.2J 00

MX Central Incisor M;~

MD Molar, Mesial

MD Molar, Distal

Root Resotption During Orthodontic Therapy

191

tiffed given the present state of knowledge, but there are some precautions that can be taken.

flag patients at particular risk of EARR. Such research is ongoing.

Periodic periapical radiographs of the maxillary incisors (the most susceptible teeth) at approximately 6-month intervals will flag those uncomm o n 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 movem e n t can be slowed along using lighter forces, so that the reparative process of the c e m e n t u m can keep abreast of the erosive processes of overcompressing 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 m o v e m e n t is resumed. It has been shown in animal models 123,a3s and h u m a n s t,7,s that a force-free "rest period" allows the c e m e n t u m 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.

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.

References
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Overview
External apical root resorption is the most common iatrogenic consequence of orthodontic treatment, but it is seldom severe enough to compromise treatment or a tooth's longevity. The most c o m m o n 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 predictors of EARR because of the large interindividual variation in response to treatment. An individual's genetic background is the single strongest predictor of resorption, as shown by familial analysis. This suggests that research will lead to a biochemical assay, perhaps of crevicular fluid, that would

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