O r t h o d o n t i c I n s i g h t

Orthodontic traction: Possible consequences for maxillary canines and adjacent teeth

Part 1: Root resorption in lateral and

Alberto Consolaro*

Some professionals are reluctant to indicate Development, structure and functions of orthodontic traction, especially for upper ca- the dental follicle nines. Among the most common reasons for The dental follicle occupies the radiolucent restricting the indication of orthodontic trac- space around the crowns of unerupted teeth tion are: (Figs 1 and 2). It is firmly attached to the sur- 1) Root resorption in lateral incisors and face of the crown by the reduced epithelium premolars. of the (Fig 3). This thin and 2) External cervical resorption of the delicate epithelial component is sustained and canines under traction. nourished by a thick layer of connective tissue 3) Alveolodental ankylosis of the canine(s) with a variable density of collagen, sometimes involved in the process. loosely, sometimes even hyalinized. The outer 4) Calcific metamorphosis of the and portion of dental follicles binds to the surround- aseptic pulp necrosis. ing bone (Figs 2 and 3). In measurements of the These conditions do not result primarily and pericoronal space in periapical radiographs and specifically from orthodontic traction, and can be orthopantomographs, or panoramic radiographs, avoided if certain technical precautions are fol- the thickness of the dental follicle can reach up lowed. For a better understanding of what these to 5.6 mm and still maintain normal structure technical precautions are and how they work and organization2,4 (Fig 3). preventively against the possible consequences of By removing the follicle and detaching it orthodontic traction, we need a biological foun- from the surrounding bone a tissue fragment dation. This is the goal of this series of studies on is obtained which is organized like a thin film orthodontic traction, especially of upper canines, and is therefore also known as pericoronal mem- and its possible consequences. brane. The isolated tissue fragment represented

* Full Professor of Pathology, FOB-USP and FORP-USP Postgraduate courses.

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by the dental follicle has the appearance of a sack containing the dental crown and is thus also called pericoronal pouch. In the middle of the collagen fibers and other components of the extracellular matrix of fol- licular connective tissue there are islands and cords of epithelial cells, remnants of the dental lamina (Fig 3), whose number varies according to patient age.2

FIGURE 1 - Typical image of the pericoronal space and normal follicle: homogeneous radiolucency with no overlapping radiopaque or radiolu- Gubernacular cord development cent points; clear bone limit with solid, uniform line (arrows); uniform The dental lamina gives rise to germs thickness, regular contour with maximum thickness ranging between 1 and 5.6 mm.2,4 in the deepest parts of what will become the

PL

bone tissue

reduced epithelium of the enamel organ RR EI

CT

oral mucosa

FIGURE 2 - Epithelial structures of the dental follicle—such as the reduced epithelium of the enamel organ and the epithelial islands/cords remnants of the dental lamina (EI)—constantly release epidermal (EGF, red arrows) in the connective tissue (CT). This mediator, along with other EGF- activated mediators, induces pericoronal bone resorption, an essential phenomenon in the occurrence of . When the path of an unerupted tooth compresses the vessels of the periodontal ligament (PL) of adjacent teeth—with or without orthodontic traction— die on the spot and the root is resorbed (RR) to give rise to the follicle and its moving crown.

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dentin enamel

RE

dentin CT

enamel

RE CT A B

FIGURE 3 - The pericoronal space and dental follicle of upper canines are more laterally bulging due to the coronary anatomy, as shown in A. The reduced epithelium of the enamel organ (RE) is firmly adhered to the enamel of unerupted teeth, while the epithelial islands remnants of the dental lamina and gubernaculum cord (arrows) are distributed across the connective tissue (CT) of the dental follicle. future or . Soon thereafter, it is cells of the gubernacular cord into its connective fragmented by apoptosis, but some of these cells tissue, while increasing the presence of its epi- persist on a scheduled basis. The remnants of thelial component in this region (Fig 3). dental lamina cells are organized in the form of islands and epithelial cords forming a veritable Development of the alveolar crypts and single row that rises from the reduced epitheli- gubernacular canal um of the enamel organ toward the oral mucosa. The epithelial cells need to be in constant pro- This epithelial cord is called the gubernaculum liferation and synthesis given their constant des- dentis, or gubernacular cord. quamation in skin and mucosal linings and also Once the tooth germs have become estab- because of its intense production of secretions such lished and the dental lamina has undergone frag- as milk, saliva and tears. This constant prolifera- mentation, the neighboring mesenchyme gives tion stimulus is provided by individual epithelial rise to bone tissue. The tooth germs and the cells, which release to their neighbors—via specific cord of epithelial islands remain unscathed as receptors—what is called the Epidermal Growth bone forms around them into the alveolar crypt. Factor (EGF) mediator. Although bone cells have Around the gubernacular cords, a delicate bony EGF receptors, in these cells EGF stimulates bone canal develops, called the gubernacular canal. resorption. Other mediators have their action trig- The function of the gubernacular canal and gered by EGF (Fig 1), such as TGF-beta, which cord lies in directing the tooth—once the crown stimulates the formation of clasts, and CSF-1 and is fully developed—toward the occlusal-most re- IL-1, which recruit their precursors. gion of the . As the tooth erupts The bone tissue is maintained at a distance towards the mucosa, the dental follicle will in- from the epithelial tissues because the released corporate the islands and cords of the epithelial EGF stimulates bone resorption, as occurs in the

Dental Press J Orthod 17 2010 July-Aug;15(4):15-23 Orthodontic traction: possible consequences for maxillary canines and adjacent teeth (Part 1) case of the epithelial rests of Malassez, which fundamental structure of tooth eruption, al- maintain the periodontal space without allowing though for decades the tooth root was believed the bone to reach the surface of the tooth root.3 to be the essential structure in this process. When bone is formed by the mesenchyme, the tooth germs are circumscribed. The alveolar Criteria for evaluating pericoronal space images: crypts and the gubernacular canal are simulta- image, thickness, contour and boundaries neously established, since the tooth germs and The image of the pericoronal space (Figs 1, 3, gubernacular islands and cords are epithelial tis- 4 and 7) should: sues that release EGF, which constantly stimu- (a) Be homogeneously radiolucent, devoid of lates bone resorption in the neighboring tissues. radiopaque points or radiolucent micro The foregoing explanation allows us to as- lodge type areas, as these may denote a sert that: source of odontogenic tumors. 1. The follicle is an epithelial component (b) Have its boundaries with the adjacent comprised of (a) the reduced epithelium bone defined by a uniform and continuous of the enamel organ, firmly adhered to the radiopaque line. If this line is discontinued crown, and (b) the cords and islands of and/or riddled with images that resemble odontogenic cells derived from the dental the gnawing of a mouse, it may represent a lamina (Figs 2 and 3). source of odontogenic cysts and tumors. 2. The connective tissue comprises the largest (c) Have its contour characterized by uni- volume of follicles and, outside the pericoro- form pericoronal space thickness, posi- nal space, it takes on the form of a membrane tioned symmetrically to the dental crown. and/or pouch. When some areas grow thicker than oth- 3. The epithelial component continuously ers, in the form of embroidery and wavy releases EGF and thus preserves the peri- contours, this may characterize a source coronal space by stimulating bone resorp- of odontogenic cysts and tumors. tion and thus keeping the bone away from (d) Have a thickness ranging from 1 mm to less the enamel (Fig 2). than 5.6 mm.2,4 Beyond these limits, one 4. The cascading release of EGF and other me- should suspect the presence of a dentiger- diators is essential for the mechanism of tooth ous cyst or some other follicular disease. eruption. The forces derived from the devel- In assessing the image of the pericoronal opment of teeth and growth vectors stimulate space, one should note that: increased secretion of EGF and promote bone 1) Diseases derived from the dental follicle resorption, directing tooth eruption in the oc- can go unnoticed and may be present even when clusal direction (Fig 2). the pericoronal space displays normal apparent When a tooth root is experimentally re- thickness. moved1 but the crown and dental follicle are 2) Changes derived from the dental follicle preserved, the tooth will erupt normally. Like- take place only occasionally, and are percentage- wise, the tooth will erupt when the crown is wise very rare, considering the frequency of un- removed and the dental follicle and tooth root erupted teeth in patients. are left in its place. When metal or silicone rep- licas replace unerupted teeth but the follicle The concept of pericoronal folliculopathies is preserved, the artificial teeth or replicas will Any disease that originates from or is locat- still erupt. The dental follicle is an essential and ed exclusively in the structures of the dental

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1.5 x MD dist.

A B

FIGURE 4 - Example of unerupted maxillary canine that did not reach the occlusal plane (A). Once the space in the dental arch reached 1.5 times the mesiodistal distance of the crown—to accommodate the bulging dental follicle typical of the maxillary canine—the tooth moved naturally to its place in the dental arch (B). But the existing proximity of the upper canine and its dental follicle caused lateral resorption (circles) in the roots of the lateral and first .

follicle can be termed pericoronal folliculopa- mediators will be increased, thereby stimulating thy, namely: the organization and function of bone modeling • Acute and chronic pericoronaritis. units (BMUs) (Fig 2). • Paradental cyst. From the standpoint of imaging, if an un- • Inflammatory follicular cyst. erupted tooth is located very close to the root • Dentigerous cyst (Fig 7). of another tooth and if the former's trajectory • Eruption cyst. is active due to the eruption and the presence • Hyperplastic dental follicle. of growth vectors, resorption is usually induced However, many other odontogenic cysts and (Figs 2, 4, 5 and 6). This scenario is very often tumors also originate from the dental follicle found in the relationship between the region of but are not exclusive to that structure or loca- the canines and the upper lateral incisors (Figs 4, tion. Odontogenic keratocysts, ameloblastomas, 5 and 6), as well as between third molars and the odontogenic fibroma, odontoma, etc. also origi- distal surface of second molars. nate from the dental follicle. Extraction of the unerupted tooth triggers process regression and re-covering of the resorbed Pericoronal space of unerupted teeth and area by new cementoblasts, with deposition of root resorption of adjacent teeth a new layer of cementoblasts and reattachment The dental follicle is rich in mediators that of periodontal fibers. This behavior often occurs stimulate bone resorption locally, especially with the lower third and second molars. Such oc- EGF (Fig 2). When maxillary growth vectors currence will only take place if the environment and eruptive forces bring the crown of an un- is not contaminated by bacteria. erupted tooth close to the root of an erupted In cases of upper canines, orthodontic and tooth, there occur the compression of periodon- or orthopedic appliances redirect the eruptive tal vessels and the death of cementoblasts that path and/or also the growth vectors involved. cover the surface, protecting it from resorption Root resorption will cease in neighboring (Figs 5 and 6). Thus, the root surface will be teeth, whereas the surface will be repaired by exposed and the amount of local resorption new cementoblasts and renewed

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A B FIGURE 5 - In some cases, detection FIGURE 6 - Regardless of the region related to the proximity of the dental follicle of unerupted teeth, of the resorption caused by unerupted root resorption may occur provided that there is compression of periodontal vessels and death of ce- teeth—including maxillary canines—in mentoblasts. A comparison between right and left sides shows that the apical resorption is linked to the adjacent teeth only occurs when it is al- unerupted canine and not to the orthodontic movement. By moving an unerupted canine through orth- ready too late, as was the case of this up- odontic traction, whenever possible, the dental follicle is also moved away, which is usually sufficient to per lateral incisor. But sometimes, it can stop root resorption and repair the surface. also involve the central incisors.

formation (Fig 4). This situation is often found Size, thickness and shape of follicles in in the relationship of canines with the upper maxillary canines compared with other teeth lateral incisors. The thickness and shape of follicles allow their A conduct that must necessarily be adopt- pericoronal spaces to have a more or less uniform ed to avert the resorption of teeth adjacent to contour of the incisal and occlusal surfaces with the unerupted tooth—when such unerupted their cusps (Fig 1). However, the unique shape of tooth is not being extracted but rather retracted upper canines—with their rather convex lateral orthodontically—lies in increasing dental arch surfaces forming a cusp, as it were, at their incisal space so that the unerupted tooth lodges in edge, which ends in an acute angle—provides a the area along with its crown and especially its very specific pericoronal space shape (Fig 3). follicle. The opening of space eliminates com- The dental follicle of maxillary canines ap- pression of the periodontal ligament of adja- pears to bulge and widen laterally, more so than cent teeth while cementoblasts and cementum the other teeth (Figs 3 and 6). Radiographic im- re-cover the roots of these teeth (Figs 4 and 6). ages and Computed Tomography (CT) scans Thus, the dental follicle of the erupted tooth re- clearly show that the lateral thickness of the mains farther away from the root surface so that pericoronal spaces of upper canines is greater its mediators no longer act as stimulators of re- than in other teeth, especially if compared with sorption. Instead, they only stimulate pericoro- incisors, and even with premolars. nal bone resorption to allow eruption to occur in The dental follicle of the upper canines and the desired path. their resulting pericoronal spaces are so bulging

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because it is the tissue or organ responsible for tooth eruption. Thanks to its large number of me- diators, the dental follicle stimulates pericoronal bone resorption, actively producing tooth move- ment in the occlusal direction (Figs 2, 3 and 4). The follicle is composed of soft tissues and although it can be physically compressed be- tween the canine crown and the roots of the lat- eral incisors and premolars, this maneuver dur- ing traction may impose a biological cost. Re- sorption of these lateral roots cause, to a lesser or greater degree, structural impairment (Fig 4). Compression of the dental follicle of maxillary canines occurs in conjunction with compression of vessels of the periodontal ligament of adja- cent teeth and eventual death of cementoblasts that protect those roots from clasts and other BMU components. In following the clinical guidelines to de- termine how much space must be provided to enable unerupted upper canine traction, profes- FIGURE 7 - The image of the pericoronal space of the maxillary canine reveals that the criteria adopted for classifying a follicle as normal no sionals are encouraged to calculate the mesio- longer apply. From a strictly radiographic point of view, the image is not distal distance of the crown and multiply that homogeneously radiolucent and its contour and thickness are not uni- form, suggesting that it is actually a dentigerous cyst in its early devel- measurement by 1.5. This action will ensure opment phase. This scenario does not preclude the use of orthodontic greater integrity of the lateral roots of adjacent traction, if necessary. teeth (Fig 4). One should be aware, however, that creating this space is not clinically possible in all cases. Using any measurement lower than the one aforementioned may result in highly successful in some cases that added to all the probable im- traction, with no damage to lateral incisors and age distortion, deciding between a diagnosis of premolars, but the risks are greater. The exact- normality or incipient dentigerous cyst poses a ness of mathematics cannot always be systemati- challenge (Figs 3, 6 and 7). cally applied in making biological decisions. The In assessing the need to whether or not open recommended criterion and measurement serve the space between upper lateral incisors and as a starting point for decision making relevant premolars to allow upper canines to naturally to each case. In cases where it can be applied lodge in the upper arch, this lateral bulging of fully, assurance regarding the preservation of their pericoronal space should be considered. neighboring roots will certainly increase. This consideration should be emphasized be- In assessing the damage caused by root re- cause the dental follicle does not represent only sorption in maxillary lateral incisors due to the a soft tissue that covers the crown and could proximity of unerupted canines, it seems ap- be easily compressed under traction, but rather propriate to cite the literature.5,6 The presence

Dental Press J Orthod 21 2010 July-Aug;15(4):15-23 Orthodontic traction: possible consequences for maxillary canines and adjacent teeth (Part 1) of root resorption was found in the periapical represented by the gingival connective tissue, to radiographs of 3,000 patients between 10 and the highly contaminated oral environment. 15 years of age.5 In fact, 12.5% of their lateral incisors were located close to canines that had Final considerations remained unerupted for longer than normal. The Root resorption of upper lateral incisors and same cases were evaluated using tomographic premolars (Figs 4, 5 and 6) is among the pos- sections and reconstructions, and disclosed 25% sible consequences of unerupted upper canine impairment. CT is the best method to accurately traction. In planning treatment of unerupted ca- assess the damage caused by canine traction to nines, one is advised to assess the thickness of the the roots of upper lateral incisors. dental follicle, bearing it in mind when creating space to accommodate it in the dental arch. The Dental follicle development and functions aim here is to seek either normal canine eruption In its early stages, the enamel organ resem- or orthodontic traction of said teeth. The lateral bles a bell and is lined by what are known as the compression of the dental follicle during erup- inner and outer epithelia. Between these epithe- tion—with or without canine traction—against lia there are two other thicker layers of epithe- the roots of the lateral incisors and/or premolars lial cells, which are known as stellate reticulum may cause these teeth to resorb, as a result of the and intermediate stratum. As the enamel organ compression of periodontal vessels and the death forms this mineralized tissue on the inside of of cementoblasts. the bell, it becomes narrower or thinner and the In planning the space to be obtained in the four epithelial layers will flatten to form a single dental arch to ensure that the unerupted tooth epithelium that is firmly adhered to the enamel fits properly, it must be assumed that the dental surface and receives the name of reduced epi- follicle of maxillary canines—given their unique thelium of the enamel organ (Figs 2 and 3). anatomy—tend to bulge and broaden laterally, The reduced epithelium of the enamel organ more than any other teeth. and, as a result, the dental follicle, have the fol- The amount of space in the dental arch that lowing main functions: would offer the least risk of root resorption for a) "Hide" or protect enamel resorption by adjacent teeth during orthodontic traction is clastic cells (Fig 3). equivalent to 1.5 times the mesiodistal distance b) Prevent the bone from developing directly of upper canines, although this measure is not al- on the enamel surface. ways amenable to application in all clinical cases. c) Support tooth eruption by releasing me- In forthcoming studies, we will discuss the diators that are typical of epithelia, such as EGF. other possible consequences of orthodontic The reduced epithelium of the enamel organ traction of unerupted teeth, especially canines, and odontogenic epithelial islands and cords are among which the following are noteworthy: actively involved in pericoronal bone resorption, (1) External cervical resorption in canines un- essential if tooth eruption is to follow a path that der traction, (2) Alveolodental ankylosis of ca- leads to the alveolar mucosal surface, thanks to nines, (3) Calcific metamorphosis of the dental the release of EGF (Fig 2). pulp and aseptic pulp necrosis. d) Constitute the primary junctional epithe- This approach is aimed at preventing the lium by merging with the oral mucosa, and allow possible consequences of orthodontic traction, teeth to erupt in the oral environment without which could be entirely avoided if certain tech- exposing the internal environment of the body, nical precautions are adopted.

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ReferEncEs

1. Cahill DR, Marks SC Jr. Tooth eruption: evidence for the 4. Damante JH. Estudo dos folículos pericoronários de dentes central role of the dental follicle. J Oral Pathol. 1980 não irrompidos e parcialmente irrompidos. Inter-relação Jul;9(4):189-200. clínica, radiográfica e microscópica. [tese]. Bauru (SP): 2. Consolaro A. Caracterização microscópica de folículos Universidade de São Paulo; 1987. pericoronários de dentes não irrompidos e parcialmente 5. Ericson S, Kurol J. Radiographic examination of ectopically irrompidos. Sua relação com a idade. [tese]. Bauru (SP): erupting maxillary canines. Am J Orthod Dentofacial Orthop. Universidade de São Paulo; 1987. 1987 Jun;91(6):483-92. 3. Consolaro A, Consolaro MFMO, Santamaria M Jr. A anquilose 6. Otto RL. Early and unusual incisor resorption due to impacted não é induzida pelo movimento ortodôntico. Os restos maxillary canines. Am J Orthod Dentofacial Orthop. 2003 epiteliais de Malassez na fisiologia periodontal. Rev Clín Oct;124(4):446-9. Ortod Dental Press. 2010 abr-maio;9(2):101-10.

Contact address Alberto Consolaro E-mail: [email protected]

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