The Dental Follicle in Normally and Ectopically Erupting Maxillary Canines: A Computed Tomography Study

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1 Original Article The Dental Follicle in Normally and Ectopically Erupting Maxillary Canines: A Computed Tomography Study Sune Ericson, DDS, PhD a ; Krister Bjerklin, DDS, PhD b Abstract: The subjects in the study were children who were X-rayed because of increased risk for resorption following ectopically erupting maxillary canines. One hundred and seven children 9 to 15 years of age with 156 maxillary canines that were erupting ectopically and 58 normally were investigated by computed tomography (CT) to describe the features of the dental follicles of the erupting maxillary canines. Contiguous, transverse CT scans were exposed through the maxilla in the canine region and the width and shape of the dental follicles were registered scan by scan throughout the extension of the follicle. The width and the shape of the dental follicle of the erupting maxillary canine varied greatly. The range of the maximum width, measured from the crown to the periphery of the follicle, was mm, with a mean of 2.9 mm and a 95% confidence interval of mm for the entire sample. No relationship was found between the width or shape of the follicles and sex, age, stage of eruption, inclination of the canine, or width of the dental arch. However, the location of the maxillary canine vis-à-vis the adjacent incisor was significantly associated with the width of the follicle, which indicated that local anatomic conditions might influence the width and shape of the follicle. The dental follicles of the ectopically erupting canines were, on average, wider than those of the normally erupting canines. The 95% confidence interval for the normally erupting canines was mm; for the buccally erupting canines mm; for the lingually erupting canines mm; and for the apically erupting canines in relation to the lateral incisors mm. Canine follicles that were wide but within normal limits did not cause deviations in adjacent teeth. Cystically degenerated dental follicles were found but were indistinguishable on the CT scans from those that had been widened physiologically. The contributions of the studied variables to the variation in the width of the dental follicle of the maxillary canine were analyzed with regression models. (Angle Orthod 2001;71: ) Key Words: Eruption; Child; Tooth follicle; Dental follicle; Dentigerous cyst; Ectopic tooth; Canine; Cuspid; Computed tomography INTRODUCTION The dental follicle is a loose connective tissue layer that surrounds the erupting tooth. The follicle is necessary for tooth eruption. Specific cellular changes occur in and around the follicle when a tooth erupts. 1,2 An eruption pathway is formed when the bone and roots of deciduous teeth are resorbed events initiated by the dental follicle during eruption. 2 5 Because tooth eruption depends on the dental a Associate Professor, Chairman, Department of Oral and Maxillofacial Radiology, Institute for Postgraduate Dental Education, Jönköping, Sweden. b Associate Professor, Chairman, Department of Orthodontics, Institute for Postgraduate Dental Education, Jönköping, Sweden. Corresponding author: Dr Sune Ericson, Department of Oral and Maxillofacial Radiology, The Institute for Postgraduate Dental Education, Box 1030, SE Jönköping, Sweden. ( sune.ericson@telia.com). Accepted: January Submitted: December by The EH Angle Education and Research Foundation, Inc. follicle and activities around it, studies of the follicle may shed some light on eruption disturbances. Tooth eruption is a long-lasting multifactorial process composed of several overlapping phases which seem to involve the size of the dental follicle. 2,5 9 In some cases this process of normal tooth eruption does not occur and the maxillary canine is retained in the alveolar process. The prevalence of impaction of maxillary canines has been reported to be percent with a palatal displacement in 85 percent but the distribution varies widely in different ethnic populations. 14 The gender ratio between males and females concerning maxillary canine impaction is contradictory. Most studies report a higher prevalence in females In a randomized Israeli population, however, the incidence in males was approximately equal to that in females. 18 Cellular changes in and around the follicle, activated by hormones and other growth-related factors, probably cause variations in the follicle dimensions. 2,5,19,20 Canine eruption 333

2 334 ERICSON, BJERKLIN TABLE 1. Distribution of the Maxillary Canines According to Sex and Eruption in a Sample of 107 Children Between 9 and 15 Years of Age with Ectopically Erupting Canines Uni- or Bilaterally Individuals Sex Boys Girls All N Ectopically Positioned Canines Erupted N indicates number of patients. Normally Positioned Canines Erupted Unerupted Unerupted Total Number of Canines (36%) 136 (64%) 214 (100%) is discontinuous with periods of active growth, 5,20,21 therefore, the size of the dental follicle may fluctuate during eruption and reflect the stage of eruption. Variations in width and form of the dental follicle have not been investigated in humans of different ages and in different eruptive situations. Such an analysis can be performed with high accuracy using CT, which unlike conventional radiographic methods, is not complicated by distortions and overlappings The purpose of this study was to analyze the width and shape of the dental follicle of the permanent canine during normal and ectopic eruption to see if these anatomical qualities correlate with eruption. SUBJECTS AND METHODS The subjects consisted of 107 children: 39 boys (36%) and 68 girls (64%). The subjects had 156 maxillary canines erupting ectopically and 58 erupting normally (Table 1). The subjects had been referred to the orthodontic clinic for consultation because of the risk of resorption of the incisors associated with the eruption of the maxillary canines. The assessment of the dental follicle was evaluated secondary to resorption as a part of that investigation. The ages of the children varied from 9 to 15 years with a mean age of 12.5 years for both sexes. The maxillary canines that were ectopically positioned were evenly distributed between the right and left sides. The distribution of these canines according to sex was consistent with the sex distribution of the whole sample. Among the boys, 58 canines (74%) and among the girls, 98 canines (72%) were ectopically positioned. Seven lateral incisors were missing because of aplasia, 2 bilaterally and 3 unilaterally. The children were examined according to our usual clinical routines, 10 which includes a clinical examination supplemented with panoramic or intraoral periapical films or both in special situations. Children with maxillary canines that are erupting ectopically and are difficult to assess on panoramic or intraoral film usually undergo a CT examination to evaluate the risks of root resorption on adjacent teeth. 26 The data in this study is derived from these boys and girls. Clinical investigation Between the ages of 9 and 12 years all schoolchildren in Jönköping County are screened by general practitioners for the position of the maxillary canines. When the canines are not buccally palpable in a normal position, when there is contralateral asymmetry in palpation or eruption, or when the lateral incisor tips distally or buccally, a radiographic examination is performed. Based on these indications, it has been reported that the position of the maxillary canine is examined radiographically in 8% of 10-year-old children. 27 Radiographic examination About 90% of the children with ectopically erupting canines during the time of the study participated in the investigation. A basic panoramic and intraoral investigation was performed at the time of the initial consultation. 10 A Siemens Somatome Plus CT scanner (Siemens AG, Germany) was used to make the tomographic images. 28 A bone algorithm for ultrahigh resolution was applied and the window setting was approximately 2800 Hounsfield Units (HU) with a center value of Filtration was performed according to the standard of the algorithm. The images of the objects on screen and on film were reconstructed from raw data sets. Contiguous transverse CT scans with a slice thickness of 2 mm were exposed through the alveolar bone of the maxilla perpendicular to the long axis of the lateral maxillary incisors (Figures 1 10). Usually, 6 scans were made. The scans were documented on films using a Siemens laser camera (Siemens AG, Germany). The enlargement (zooming factor) on film was 1.5 and the image resolution was about 0.3 mm. The values presented in the tables are corrected for the magnification on the films. For a more detailed description of the performance and the accuracy of the CT method when imaging maxillary canines, see Ericson and Kurol. 25,26 Variables studied The eruptions of the maxillary canines and the images of the dental follicles of the canines were analyzed on screen and on film images. The following variables were registered for the permanent canines. Stage of eruption Canine located within the bone, follicle present and surrounded by a lining of unbroken compact bone (Figures 1 and 3 through 7) Canine approaching eruption; follicle not completely covered by bone, gingiva intact (Figures 2, 8 and 9) Canine eruption through the gingiva; no follicle or not assessable

3 RADIOGRAPHIC ASSESSMENT OF THE DENTAL FOLLICLE 335 FIGURE 1. The patient is an 11-year-old girl. (A) Periapical films. No. 13 is erupting ectopically and lingual to No. 12. The dental follicle of No. 13 is enlarged near the eruption site through the alveolar crest. No visible resorption. (B through D) Axial (transversal) CT scans through the alveolar process at the level of the crowns of the maxillary canines. No. 13 is erupting ectopically and No. 23 is in a normal position. The dental follicle of No.13 is symmetrically extended and has exposed the roots of Nos. 12 and 11 lingually, distally and in between the 2 roots. The root of No. 12 is slightly resorbed lingually close to the crown of No. 13, and is buccally displaced. The root of No. 11 has no contact with No. 13 and is intact and positioned normally. The mesial migration of No. 13 is marked in scan C with. Lingual to the roots of Nos. 21 and 22 in scans B and C (arrows), the spongeous bone is loose and lacks trabeculae. Biopsies of the dental follicle of No. 13 show normal, loose connective tissue with elements of reduced enamel epitheliums and no cystic degeneration. FIGURE 2. The patient is a 10-year-old girl. CT scan. No. 13 is rotated in a distobuccal position to No. 12. The crypt of the dental follicle has caused the buccal bone of the alveolar process to bulge and the cortical lining of the crypt is missing locally (arrows). The follicle of No. 13 is spherically enlarged and the root of No. 12 is exposed. No. 23 is positioned mesiobuccally to No. 22. The dental follicle is enlarged asymmetrically and the buccal lining of the bone crypt of the follicle is missing (arrows), the follicle has partly exposed the roots of Nos. 21 and 22, and the crown of No. 23 has displaced 22. The width of the dental arch is marked with. Vertical eruption of the canine; the least distance (mm) from the canine to the occlusal line 29 Open or closed apex of the canine. Position Position of the crown of the canine to adjacent incisors (26) FIGURE 3. The patient is an 11-year-old boy. CT scan shows bilateral aplasia of the lateral incisors. The maxillary canines are erupting within the dental arch. The dental follicles are symmetrically enlarged, and the follicle crypts are surrounded by an intact cortical lining. The roots of Nos. 11 and 21 are partly exposed. Mesial migration of the canine; the distance (mm) from the most mesial part of the crown of the canine to the midline as registered on the CT scan (Figure 1C) Inclination of the canine to the midline 29 Form of the dental follicle Symmetric: rounded or spherical form with the crown of the canine in the center (Figures 1, 3, and 4) Asymmetric: irregular form buccal, mesial, distal, or lin-

4 336 ERICSON, BJERKLIN FIGURE 4. The patient is a 12-year-old girl. CT scan shows No. 23 erupting buccal to No. 22 and resorption can be seen on the root of No. 22 (arrow-head). The dental follicle of No. 23 is spherically extended, less mesially because of No. 21 and more distally where there is space and spongeous bone. The buccal and lingual extension is restrained by the cortical bone of the alveolar process. The root of No. 21 is partly exposed by the follicle. No. 13 is erupting normally. The biopsy of the follicle of No. 23 showed a loose, matrix of connective tissue with elements of microcyst formation. FIGURE 7. The patient is a 12-and-a-half-year-old girl. CT scan shows No. 23 erupting lingual to No. 22. The follicle is asymmetrically widened and extends distally into the spongeous bone. The follicle has partly exposed the roots of Nos. 22 and 21. Biopsy of the dental follicle of No. 23 showed normal follicular tissues. FIGURE 5. The patient is a 12-year-old girl. CT scan shows No. 13 erupting ectopically and No. 23 normally. Number 13 is erupting distolingual to No. 12. The follicle of No. 13 is widened at the crypt and surrounded by a cortical lining. The follicle extends buccally and has partly exposed the roots of Nos. 12 and 14. A biopsy of the dental follicle of No. 13 showed a dentigerous cyst. FIGURE 8. The patient is a 14-year-old boy. Nos. 13 and 23 erupt lingually and close to the adjacent permanent incisors. No resorptions on the incisors. The dental follicles are asymmetrically widened and have exposed the roots of Nos. 12, 11, 21, and 22. The palatal plate is bulging and the cortical lining of the follicular crypt No.13 is partly missing (arrow-head). The roots of the temporary canines have been partly resorbed. FIGURE 6. The patient is a 12-year-old girl. CT scan shows Nos. 13 and 23 erupting buccally to Nos.12 and 22, respectively. The follicles have caused the buccal plate of the alveolar bone to bulge (arrow-head) and extend asymmetrically into the spongeous bone (arrow). There are contacts between the ectopic canines and the adjacent roots of the incisors with no root resorption. The roots of the lateral incisors have been displaced by the canines. Biopsies of the dental follicles of Nos. 13 and 23 showed normal follicular tissues. FIGURE 9. The patient is a 14-year-old boy. CT scan shows impacted No. 13 positioned lingual and close to Nos. 11 and 12. No resorption of the roots of the incisors. The dental follicle is thin, which suggests that No. 13 is in an inactive phase of eruption. The palatal plate is bulging and partly resorbed close to the crown of No. 13 (arrow).

5 RADIOGRAPHIC ASSESSMENT OF THE DENTAL FOLLICLE 337 TABLE 2. Variables Used in the Different Statistic Models Variable Type of Answer and Quantification Sex Male (1), female (2) Age Years and month Position of the canine crown to adjacent lateral or central incisor Buccal (1), not buccal (2) Distobuccal (1), not distobuccal (2) Lingual (1), not lingual (2) Distolingual (1), not distolingual (2) Apical (1), not apical (2) Distal (1), not distal (2) Degrees to the midline Inclination of the canine Apex of the canine Open (1), closed (2) Stage of canine 1. Approaching eruption, the dental follicle partly lacks bone covering (1), follicle completely covered by bone (2) 2. Degree of vertical eruption, distance (mm) to the occlusal line 3. Mesial migration of the (ectopically positioned) canine, mm to the midline Form of dental follicle Symmetric (1), asymmetric (2) Expansion of the dental follicle around the canine crown Width of the alveolar process Space of eruption Centered (1), not centered (2) Buccal (1), not buccal (2) Mesial (1), not mesial (2) Lingual (1), not lingual (2) Distal (1), not distal (2) Transversal distance (mm) between the maxillary first premolars No lack of space (1), lack of space in the dental arch (2) Biopsy FIGURE 10. The patient is a 13-and-a-half-year-old boy. (A) Periapical films show No. 23 in an impacted position lingual to Nos. 21 and 22. The dental follicle of No. 23 is asymmetric and slightly widened (arrow). (B and C) CT scans show the crown of the ectopic positioned No. 23 located close to the roots of Nos. 21 and 22. The roots of the incisors are exposed, but there is no resorption of the roots. The dental follicle is thin but wider in the coronal parts of the crown, especially distally, where the dental crypt bulges palatally (arrow). The width of the dental follicle indicates low eruptive activity and retention of No. 23. The biopsy of the dental follicle of No. 23 showed normal follicular tissue. gual to the crown or in combination (Figures 2 and 5 through 8) Width of the dental follicle The largest distance from the crown of the maxillary canine to the periphery of the follicle. The distance was measured on axial CT scan to the nearest half millimeter. Width of the alveolar process The transversal distance between the center of the pulps of teeth 14 and 24 at the level of the alveolar crest (Figure 2). Seventeen dental follicles from ectopically erupting maxillary canines were histologically processed. After fixation in 10% formalin, the tissue was embedded in paraffin, sectioned, and stained with hematoxylin-eosin according the methods of van Giesen and Malloroy. Sections were made at different levels through the extirpated follicle. Statistical analyses The SPSS computer program was used for the statistical analyses. 30 Relationships of data were studied using the chisquared test with Fishers exact test, differences between groups using the Mann-Whitney U-test, and differences in means between 2 groups using the Student s t-test. The associations between the maximum widths of the dental follicles (mm) of the maxillary canines (dependent variable) and some explanatory variables (regressors) were analyzed using univariate and multivariate regression models. The studied variables are shown in Table 2, as well as the numeric quantification of the variables. The criterion of entry or removal of variables in the multivariate analyses was P The correlation coefficient for the equation is R and the explanatory value corresponds to R 2.

6 338 ERICSON, BJERKLIN TABLE 3. The Maximum Width of the Dental Follicle (mm) in a Sample of 107 Children with 176 Unerupted Maxillary Canines as Measured on CT Scans Individuals Number Mean SD Range Boys Girls Total Level of Significance CT indicates computed tomography; SD, standard deviation; and NS, not significant. TABLE 4. The Maximum Width of the Dental Follicle (mm) in a Sample of 107 Children with 176 Unerupted Maxillary Canines as Measured on CT Scans Canine Position Number Mean SD Range Ectopic Normal NS Level of Significance P.01 CT indicates computed tomography; SD, standard deviation; and P, p-value. RESULTS The distribution of the maxillary canines according to sex and eruption is shown in Table 1. Of the 107 children, 39 boys (36%) and 68 girls (64%) had maxillary canines that were ectopically positioned unilaterally or bilaterally. In all, 156 (73%) canines were misplaced. Four of the ectopically positioned canines and 34 of the 58 normally erupting canines had penetrated the gingiva; these were excluded in the following analyses of the dental follicles. No statistically significant differences between boys and girls were found concerning the degree of the eruption of the maxillary canines, unilateral or bilateral occurrence of the ectopic canines, or the migration and location of the ectopically positioned canines in the jaw vis-à-vis the adjacent incisors, or the closure of the root apex. Width of the dental follicle The widths of the dental follicles of the unerupted maxillary canines in boys and girls are shown in Table 3. There was a large variation in width (Figures 1 through 10) but no statistically significant differences between boys and girls were found, neither for the normally or the ectopically erupting canines, nor between the age groups, which ranged from 9 to 15 years of age. In the following analyses, the values of the dental follicles in boys and girls are pooled. In Table 4 the maximum width of the dental follicle of the ectopically and normally positioned maxillary canines is shown. There was a small but significant difference in width between the 2 groups (P.01). The follicles of the ectopic canines were, on average, larger than those of the canines that were erupting normally. The 95% confidence interval (CI) for the maximal width of the dental follicles TABLE 5. The Width of the Dental Follicle (mm) of the Maxillary Canine Positioned Distally, Buccally, Lingually, or Apically to the Adjacent Incisor in a Sample of 176 Unerupted Maxillary Canines Canine Position Number Mean SD Distally* Buccally Lingually Apically Level of Significance in Comparison with the Distally Positioned P.01 NS P.01 SD indicates standard deviation; P, p-value; and NS, not significant. * Distally, distobucally and distolingually. TABLE 6. The Maximal Width of the Dental Follicle (mm) in a Sample of 107 School Children with 176 Unerupted Maxillary Canines as Measured on CT Scans. Stages of Canine Eruption Stage of Canine Eruption Approaching eruption Completely bone-covered Ectopic Position Mean SD Number Number 16 8 Normal Position Mean SD CT indicates computed tomography; and SD, standard deviation. was mm for the whole sample, and mm for the normally erupting canines. The CIs for the dental follicles were also calculated for different crown positions. When the crown of the maxillary canine appeared buccal to the lateral incisor, the 95% CI was mm; lingual, mm, and apical, mm. To determine whether the position of the canine within the jaw distal (normal), buccal, lingual, or apical to the adjacent incisor was related to the width of the dental follicle of the canine, the widths of the follicles in these 4 positions were measured. The widths of the follicles of the canines that were erupting ectopically were compared with the widths of the follicles of the canines that were erupting normally (ie, distal to the lateral incisor) (Table 5). Compared to the dental follicles of the canines that were erupting normally, those of buccally and apically positioned canines, relative to the adjacent maxillary incisors, were wider (P.01) and those of the lingually positioned canines did not differ significantly. To see if the widths of the dental follicles varied with the stage of eruption, the widths of the follicles were measured in 2 situations: (1) when the canines were about to penetrate the alveolar bone and (2) when the follicles were situated in a crypt in the bone and covered by intact cortical bone. There were no significant differences in width between the 2 situations (Table 6). Normally and ectopically erupting canines agreed in that respect. Deviations in adjacent permanent roots because of an expanded dental fol-

7 RADIOGRAPHIC ASSESSMENT OF THE DENTAL FOLLICLE TABLE 7. The Appearance and Maximal Width (mm) of the Dental Follicle in a Sample of 107 Children with 176 Unerupted Maxillary Canines as Assessed on CT Scans Follicle form Symmetric Asymmetric Number Canine Position Ectopic Normal 19 5 CT indicates computed tomography; and P, p-value. Level of Significance P.001 TABLE 8. The Maximal Width of the Dental Follicle (mm) in a Sample of 107 School Children with 152 Unerupted, Ectopically Positioned Maxillary Canines as Measured on CT Scans Follicle Appearance Number Mean SD Symmetric Asymmetric Level of Significance P.01 CT indicates computed tomography; SD, standard deviation; and P, p-value. licle were not seen. When root displacement did occur, it was because of pressure from an ectopically positioned canine (Figures 1, 2, 4, and 6). The cortical lining of the alveolar bone bulged often close to the dental follicle. The bulgings varied in extent and occurred more often buccally, but they were also seen lingually, depending on the location of the maxillary canine (Figures 1 and 2; 6 through 10). However, most follicle expansion occurred within the spongeous alveolar bone, where the resistance to expansion was lower. As a rule, the follicles resorbed the periodontal contours facing the roots of the adjacent permanent teeth and sometimes extended in between and almost around the roots, forcing the follicle to take on an asymmetric form (Figures 2; 5 through 8). Shape of the dental follicle The extension of the follicle varied not only in width but also in shape (Figures 1 through 10). It was found that asymmetric forms were more common for canines that 339 erupted ectopically than for those that erupted normally (Table 7, P.001). The irregularly shaped follicles were also wider (Table 8, P.01). Histological investigation Of the 17 dental follicles that were analyzed histologically, the widths of all but 4 were above average. The follicles consisted of a loose connective matrix (ground substance) containing small portions of myxomatous cell, fragments of reduced enamel epithelium, and sometimes PMN cells. Microcyst formations or complete cystic degenerations were found in 4 follicles (Figures 4 and 5). Regression analyses Regression analyses were performed to study the relationships between the widths of the dental follicles of the unerupted maxillary canines (regressand) and the listed variables (regressors) (Table 2) and to evaluate the influence those variables might have on the variation in the width of the dental follicle of the maxillary canine. Twenty-two variables were included in the univariate analyses, of which 7 were significantly correlated to the width of the dental follicle (P.05), but with low coefficients. The contribution of the 7 variables to the variance in the width of the follicle was subsequently small (R ). The results of the univariate analyses are presented in Table 9. When the same variables presented in Table 9 were regressed multivariately, only one follicle centered around the crown remained significant (P.001, R ). A possible contribution to the power of that variable were the follicles of the canines positioned apically to the lateral incisors, which were wider, on average, than the others (Table 5). The low R-value of the multivariate analysis indicates that the variation in the width of the dental follicle is mainly explained by factors other than those included in these analyses. A combination of factors such as stage of eruption, location of the canine in the jaw, and space available for follicle expansion are likely of more importance TABLE 9. Univariate Regression Analyses with the Width of the Dental Follicle of the Maxillary Canines as Dependent Variable in a Sample of 107 Boys and Girls with 176 Unerupted Canines Canine Canine Canine Variable (regressor) Crown positioned buccally Crown positioned lingually Crown positioned distally Form of the dental follicle Dental follicle centered Dental follicle extended lingually Dental follicle extended distally All Canines N a NS a b b c NS Regression Coefficient Se a P.05, b P.001, c P Se indicates standard error; N, number of patients; NS, not significant; and, too few values to test. Ectopically Erupting Canines N 152 Normally Erupting Canines N a a NS b b c c NS b

8 340 ERICSON, BJERKLIN for the variance in follicle width than any of the factors that were analyzed separately. DISCUSSION The subjects in this study were not randomly selected. They were children referred by general dental practitioners to the orthodontic clinic for consultation because of risk of resorption associated with the ectopic eruption of the maxillary canine. In this respect, our results are representative but may diverge from those of an average school population of the same age and sex. However, the effect of the selection on our results is most likely small and clinically insignificant. Assessment of the dental follicle in children is usually performed adequately in a clinical examination or in combination with intraoral films. In situations where conventional radiography poorly depicts the actual relationships between an ectopically erupting tooth and the root(s) of adjacent permanent teeth, CT substantially increases the diagnostic possibilities. This is especially valuable in situations where the risks of resorption are enhanced. 23,24,26 The children in this study were investigated on that indication. 26 Computed tomography does, however, mean additional radiation and costs. The probability of stochastic effects, expressed as an equivalent whole body radiation dose (effective dose), in our CT approach increases about 2 to 8 times compared with panoramic, conventional full mouth, and film tomography examinations The effective dose used is still acceptable because of the low total risk for stochastic effects. The benefits of accurate diagnosis when the maxillary canine erupts ectopically balance the drawbacks of using CT by providing a better foundation and prognosis for orthodontic treatment. By using CT to study the dental follicle scan by scan, we were able to assess the follicle in 3 dimensions. The dental follicle of the erupting maxillary canine varied in shape and width from 0.5 mm to 7 mm with a mean value of 2.9 mm, and a confidence interval of mm, measured as the largest distance from the crown of the canine to the periphery of the follicle. This means that in some individuals, the width of the follicle exceeded the mean values substantially and exceeded the normal width by about 2 to 3 times, indicating that some follicles had undergone cystic transformation Histological evaluations of the follicles were only available in a few cases. Literature and clinical experience show that cystic or other degenerative changes may appear in dental follicles during eruption Some of the wide follicles were also found to have undergone cystic degeneration. However, signs or symptoms of cystic follicles (eg, deviation in adjacent teeth because of the expanding follicle) were not seen. The risk of cystic transformation of the entire dental follicle is probably small in these age groups, 40,42,43 but may occur in the first 2 decades of life. When appearing in the second decade, dentigerous cysts most frequently involve the maxillary canine. 38,40,44 If a cystic degeneration of the dental follicle begins to develop shortly before or after crown formation is completed, it is not possible to distinguish from intraoral films whether there is a cyst or whether the change is physiological because of eruption. Nor is it possible to reliably discriminate between physiologically and cystically enlarged follicles by CT scanning. Clinically, this diagnostic difficulty is usually of minor importance in normally erupting canines as the true dental follicle, as well as the degenerated follicle, will be destroyed, when the crown reaches the gingival surface. 2,40,44 The ectopically positioned canines may behave differently and should be controlled during the period of growth, if embedded. Mourshed 42 and Toller 45 estimated that one in 150 unerupted teeth might develop a dentigerous cyst; the risk seems to be greater in individuals over 20 years of age, especially for impacted third molars. The width and shape of the dental follicle varied by the location of the canine in the jaw. Follicles of buccally and apically displaced canines were significantly wider than follicles of distally (normally) positioned canines, while the lingually displaced canines had follicles of about the same width as those positioned normally. This points to a relationship between the width of the follicles and the available space. Hard tissues such as roots of adjacent incisors or a thick layer of cortical bone (eg, lingual to the alveolar process) may restrict the symmetric expansion of the follicle while a thin cortical layer and spongeous bone will allow the follicle to expand (Figures 2; 4 through 8). In jaws where the bone tissue is loosely spongeous and the bone spacious, the follicles adapt a spherical form; when the follicle has little space for expansion, its form will be more irregular. The impact of local anatomical factors on the shape and width of the dental follicle is easily observed on CT scans but has not been previously reported. In cases where the follicles of the maxillary canines have been enlarged, a common procedure has been to extract the deciduous canines. Enlarged follicles are sometimes thought to be a risk factor for deviations in adjacent permanent roots and to induce root resorption of adjacent incisors. 6,40,41 From this study, we cannot confirm that widened dental follicles of the maxillary canines during eruption increase the risk of displacement of adjacent incisor roots. Whether or not a widened dental follicle causes root resorption of adjacent permanent roots has not been thoroughly investigated. 46 The follicles often expanded into the loose spongeous bone close to, and sometimes around, the root(s) of the adjacent permanent teeth by causing the alveolar cortex to bulge; however, the follicles did not interfere with or cause deviations in adjacent teeth. Root deviations close to a dental follicle only appeared near an ectopically positioned canine and were probably caused by the eruptive force of the canine and not by the follicle.

9 RADIOGRAPHIC ASSESSMENT OF THE DENTAL FOLLICLE No relationships were found between the form or width of the canine and sex, age, or stage of eruption of the canine. Nor were differences in width or form seen between follicles located within an intact bone crypt and the follicles of canines approaching eruption into the oral cavity. In this respect, the results differ from those of earlier observations based on routine radiographic procedures. 47 The radiological observations were supported by the results of the regression analyses. However, the data of the analyses (R 2 values) suggest that one or more factors, as yet not identified but possibly innate, may have an influence on follicle width and contribute substantially to the individual variation in the width of the dental follicle. Cellular changes in and around the dental follicle, activated by hormones or other growth-related factors, most likely induce variations in the follicle dimensions. 2,3,5,10,11 As the eruption of the canine is discontinuous and undergoes periods of growth, the size of the dental follicle may fluctuate with eruption and reflect the stage of the eruption process. CONCLUSION The 95% confidence interval of the width of the dental follicle of an erupting maxillary canine was mm for canines that erupted normally and mm for canines that erupted ectopically. The dental follicles of maxillary canines that erupted ectopically were, on average, wider than the dental follicles of those that erupted normally. The dental follicle of the erupting maxillary canine varied in shape and width between subjects. Asymmetric forms of the dental follicle were more common in canines that erupted ectopically than in those that erupted normally. The width of dental follicles with an asymmetric form was wider, on average, than that of those with a symmetric form. Dental follicles of the maxillary canine that were normally enlarged did not cause deviations in adjacent teeth during eruption. Dental follicles that had undergone cystic degeneration were indistinguishable from physiologically widened follicles on radiographs. The anatomical structures close to the follicle had an impact on the width and form of the dental follicle. ACKNOWLEDGMENT We thank statistician Birgit Ljungqvist, PhD, for statistical advice. REFERENCES 1. Marks SC Jr, Cahill DR. Regional control by the dental follicle of alterations in alveolar bone metabolism during tooth eruption. J Oral Pathol. 1987;16: Marks SC Jr, Schroeder HE, Andreasen JO. Theories and mechanisms of tooth eruption. In: Andreasen JO, Kölsen-Pedersen J, Laskin DM, eds. Textbook and Color Atlas of Tooth Impactions. 1st ed. Copenhagen: Munksgaard; 1997: Shroff B, Siegel SM. Molecular basis for tooth eruption and its 341 clinical implications in orthodontic tooth movement. Semin Orthod. 2000;6: Marks SC Jr, Gorski JP, Wise GE. The mechanisms and mediators of tooth eruption models for developmental biologists. Int J Dev Biol. 1995;39: Marks SC Jr, Schroeder HE. Tooth eruption: theories and facts. Anat Rec. 1996;245: Magnusson B. Tissue Changes During Molar Tooth Eruption [master s thesis]. Stockholm and Umeå: Transactions of the Royal School of Dentistry; 1968;13: Steedle JR, Proffit WR. The pattern and control of eruptive tooth movements. Am J Orthod. 1985;87: Wise GE, Marks SC Jr, Cahill DR. Ultrastructural features of the dental follicle associated with formation of the tooth eruption pathway in the dog. J Oral Pathol. 1985;14: Berkovitz BK. How teeth erupt. Dent Update. 1990;17: Ericson S, Kurol J. Radiographic assessment of maxillary canine eruption in children with clinical signs of eruption disturbance. Eur J Orthod. 1986;8: Thilander B, Jakobsson SO. Local factors in impaction of maxillary canines. Acta Odontol Scand. 1968;26: Kramer RM, Williams AC. The incidence of impacted teeth. A survey of Harlem Hospital. Oral Surg. 1970;29: Jacoby H. The etiology of maxillary canine impactions. Am J Orthod. 1983;84: Becker A. The Orthodontic Treatment of Impacted Teeth. London: Martin Dunitz Ltd; 1998; Dachi SF, Howell FU. A survey of 3874 routine full-month radiographs. II. A study of impacted teeth. Oral Surg Oral Med Oral Path. 1961;14: Becker A, Smith P, Behar R. The incidence of anomalous lateral incisors in relation to palatally displaced cuspids. Angle Orthod. 1981;51: Oliver RG, Mannion JE, Robinson JM. Morphology of the maxillary lateral incisor in cases of unilateral impaction of the maxillary canine. Br J Orthod. 1989;16: Brin J, Becker A, Shalhav M. Position of the maxillary permanent canine in relation to anomalous or missing lateral incisors: a population study. Eur J Orthod. 1986;8: Thesleff I. Does Epidermal growth factor control tooth eruption? ASDC J Dent Child. 1987;54: Kardos TB. The mechanism of tooth eruption. Br Dent J. 1996; 10: Olow-Nordenram M, Anneroth G. Eruption of maxillary canines. Scand J Dent Res. 1982;90: Ericson S, Kurol J. CT diagnosis of ectopically erupting maxillary canines a case report. Eur J Orthod. 1988;10: Schmuth GPF, Freisfeld M, Köster O, Schüller H. The application of computerized tomography (CT) in cases of impacted maxillary canines. Eur J Orthod. 1992;14: Elefteriadis J, Athanasiou AE. Evaluation of impacted canines by means of computerized tomography. Int J Adult Orthod Orthognath Surg. 1996;11: Ericson S, Kurol J. Incisor root resorptions due to ectopic maxillary canines imaged by computerized tomography. A comparative study in extracted teeth. Angle Orthod. 2000;70: Ericson S, Kurol J. Resorption of incisors after ectopic eruption of maxillary canines: a CT-study. Angle Orthod. 2000;70: Ericson S, Kurol J. Longitudinal study and analysis of clinical supervision of maxillary canine eruption. Community Dent Oral Epidemiol. 1986;14: Operating Manual: SOMATOM; PLUS/PLUS-S. Image quality guide. Erlangen, Germany: Siemens AG; 1995: Ericson S, Kurol J. Resorption of maxillary lateral incisors caused by ectopic eruption of the canines. A clinical and radiographic

10 342 ERICSON, BJERKLIN analysis of predisposing factors. Am J Orthod Dentofacial Orthop. 1988;94: Nie N, Hull CH, Jenkins JG, Steinbrenner K, Bent DH. Statistical Package for the Social Sciences. 2nd ed. New York, NY: MacGraw-Hill; Ericson S, Eckerdal O, Kurol J, Carlsson C, Helmrot E. Riktlinjer för klinisk och röntgenologisk övervakning av överkäkshörntändernas eruption hos och och ungdomar mellan 8 och 15 år. [In Swedish]. ISSN SSI P182 81;1984: Stenström B. Dose contributions to Swedish population from oral radiography [master s thesis]. Swed Dent J. 1986;Suppl Gibbs SJ, Pujol A Jr, Chen TS, James A Jr. Patient risk from intraoral dental radiography. Dentomaxillofac Radiol. 1988;17: Frederiksen NL, Benson BW, Sokolowski TW. Effective dose and risk assessment from film tomography used for dental implant diagnostics. Dentomaxillofac Radiol. 1994;23: Frederiksen NL, Benson BW, Sokolowski TW. Effective dose and risk assessment from computed tomography of the maxillofacial complex. Dentomaxillofac Radiol. 1995;24: Leitz W, Axelsson B, Szeudrö G. Computed tomography dose assessment a practical approach. Radiat Prot Dosim. 1995;57: Dula K, Mini R, van der Stelt PF, Lambrecht JT, Schneeberger P, Buser D. Hypothetical mortality risk associated with spiral computed tomography of the maxilla and mandible. Eur J Oral Sci. 1996;104: Stafne EC. Oral Radiographic Diagnosis. 5th ed. In: Gibilisco JA, ed. Cysts of the Jaws. Philadelphia: WB Saunders; 1985: Chap Beyer D, Herzog F, Zamilla FF. Kieferzysten. Chap 6. In: Röntgendiagnostik von Zahn und Kieferkrankungen [in German]. Berlin: Springer-Verlag; 1987: Shear M. Cysts of the Oral Regions. 3rd ed. London: Bulterworth- Heinemann Ltd; 1992: Kurol J, Ericson S, Andreasen JO. The impacted maxillary canine. In: Andreasen JO, Kölsen-Pedersen J, Laskin DM, eds. Textbook and Color Atlas of Tooth Impactions. 1st ed. Copenhagen: Munksgaard; 1997: Mourshed F. A roentgenographic study of dentigerous cysts. I. Incidence in a population sample. Oral Surg Oral Med Oral Path. 1964;18: Mourshed F. A roentgenographic study of dentigerous cysts. III. Analyses of 180 cases. Oral Surg Oral Med Oral Path. 1964;18: Shear M. Developmental odontogenic cysts. An update. J Oral Pathol Med. 1994;23: Toller PA. Origin and growth of cysts of the jaws. Ann R Coll Surg Engl. 1967;40: Ericson, S, Bjerklin, K. Does the canine dental follicle resorb permanent incisor roots? A computed tomography study of erupting maxillary canines. Angle Orthod. (In Press). 47. Becker A. The Orthodontic Treatment of Impacted Teeth. London: Martin Dunitz Ltd; 1998:13 14.

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