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Predisposing factors for severe incisor root resorption associated with impacted maxillary canines
ORIGINAL ARTICLE
Predisposing factors for severe incisor root resorption associated with impacted maxillary canines Stella Chaushu,a Karolina Kaczor-Urbanowicz,b Małgorzata Zadurska,c and Adrian Beckerd Jerusalem, Israel, and Warsaw, Poland
Introduction: Severe incisor root resorption (SIRR) associated with impacted maxillary canines is rare but has important implications. Early diagnosis and treatment are imperative. In this investigation, we aimed to identify predisposing factors for impacted canine-linked SIRR. Methods: Clinical and radiographic data of 55 consecutive patients (77 canines) with SIRR of 96 incisors were compared with data from 57 consecutive control subjects (72 canines). The studied variables were age, sex, position of the impacted canine, size of the dental follicle, and incidence of anomalous lateral incisors. Results: Lateral incisors were more often affected than central incisors, and bilateral SIRR was common. When each variable was examined separately, SIRR was significantly associated with female sex, severely mesiodistally displaced and vertically positioned canines in the middle third of the adjacent incisor root, dental follicles wider than 2 mm, and normal lateral incisors. The multivariate statistical analysis showed that the risk for SIRR was significantly higher in female subjects (4.2 times) with enlarged dental follicles (8.3 times) and normal lateral incisors (5.8 times). Conclusions: SIRR should be carefully screened in female patients with enlarged dental follicles and normal lateral incisors. A greater degree of canine displacement might also be associated with SIRR. (Am J Orthod Dentofacial Orthop 2015;147:52-60)
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arly studies with plain film radiography indicated that canine-related incisor root resorption occurs in approximately 12% of patients.1 Yet the authors were at pains to point out that with plain film radiography, it was impossible to properly assess the buccolingual aspects of the incisor roots. With the advent of more advanced imaging techniques such as computerized tomography scanning, detectable root resorption was diagnosed in 38% of resorbed lateral incisors and 9% of central incisors.2 Moreover, from the study of Walker et al3 using cone-beam computed
a Associate professor and chair, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. b Postgraduate student, International Postgraduate Orthodontic Program, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. c Associate professor and head, Department of Orthodontics, Medical University of Warsaw, Warsaw, Poland. d Clinical associate professor emeritus, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Address correspondence to: Stella Chaushu, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, PO Box 12272, Jerusalem 91120, Israel; e-mail, [email protected]. Submitted, February 2014; revised and accepted, September 2014. 0889-5406/$36.00 Copyright Ó 2015 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.09.012
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tomography (CBCT), detection capability increased to 67% of cases of which 11% were central incisors and 4% were premolars.3,4 Congenitally missing, small, and peg-shaped maxillary lateral incisors are highly correlated with maxillary canine palatal impaction.5 Whereas resorption of maxillary incisor roots is a well-recognized phenomenon that can occur in patients with impacted canines,6-11 these anomalous lateral incisors with reduced size or abnormal shape have been reported to be less at risk to develop severe root resorption, compared with patients with normally shaped and sized lateral incisors.11 Fortunately, severe incisor root resorption (SIRR) associated with impacted maxillary canines is rare, but when is appears, it threatens the long-term survival of the affected teeth. Early diagnosis and treatment are imperative to save the affected tooth.12,13 At present, evidence-based information regarding potential predisposing factors for SIRR is lacking. The aim of this study was to identify predisposing risk factors for SIRR associated with impacted maxillary canines. MATERIAL AND METHODS
The study group included 55 consecutive patients with impacted maxillary canines and SIRR, and the
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Fig 1. A 14-year-old boy with severely resorbed maxillary right lateral incisor associated with canine impaction: A, panoramic view; B, periapical view; C, transaxial and 3-dimensional CBCT views.
control group included 57 consecutive patients with impacted maxillary canines without SIRR from the Department of Orthodontics of the Hebrew University in Jerusalem, Israel, and the Medical University of Warsaw in Poland and from the private practices of 2 authors (S.C. and A.B.). The inclusion criterion for the study group was SIRR of at least 1 maxillary incisor associated with an adjacent impacted canine in untreated healthy patients. Diagnosis of SIRR was made from the available panoramic and periapical radiographs that had been taken earlier with the intention of commencing orthodontic treatment (Fig 1, A and B). For most of the patients (75%) in the study group, CBCT images were also available for examination (Fig 1, C). CBCT was considered superfluous for patients in whom SIRR could be diagnosed on plain films alone. When CBCT was unavailable for a patient, the buccolingual position of the ectopic canine was determined using the routine tube-shift method and confirmed by the treating orthodontist or surgeon during surgical exposure. In the control group, CBCT had been available for all subjects to exclude any signs of root resorption. The radiographs were examined by 2 authors (S.C. and A.B.) using an x-ray viewer with standard light intensity. The CBCT examinations were performed with an iCAT scanner (12-bit; Imaging Sciences International, Hatfield, Pa) with the following parameters: 26.9 seconds scan time, 120 kV, 5 mA, field of view size of 13 (height) 3 16 (diameter) cm, and 0.2-mm voxel. The
resultant slice image data were converted to 3-dimensional images in DICOM format, reconstructed by XoranCat software (version 3.1.62; Xoran Technologies, Inc, Ann Arbor, Mich) and imported to be evaluated in i-CATVision (2008 version 1.8.1.10; Imaging Sciences International). The reconstructed image had a 2-mm slice thickness. Traditionally, root resorption has been described elsewhere as horizontal shortening of the root.14 The pattern is different for SIRR associated with impacted maxillary canines, where the resorption is mostly oblique rather than horizontal (Fig 2). Root resorption was measured on the radiographs, and it was considered severe when it affected more than a third of the length of the root, but not specifically its apical part (Fig 3). The exclusion criteria for the sample were root resorption of maxillary incisors less than one third of their expected root length, root resorption secondary to trauma or pulp pathology, or the presence of cysts and other pathologies. The numbers of involved central vs lateral incisors, and unilateral vs bilateral cases, were recorded. The associations between SIRR and the following variables were evaluated: (1) age; (2) sex; (3) buccolingual location: palatally, buccally, or in the line of the arch; (4) mesiodistal location: sector7 (Fig 4, A); (5) angulation to the midline14,15 (Fig 4, B); (6) overlap of the adjacent incisor14,15 (Fig 4, C); (7) vertical crown height relative to the adjacent incisor root: apical, middle, or coronal16 (Fig 4, D); (8) maximum width of the
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logistic regression analyses with SAS software (version 9.4; SAS Institute, Cary, NC) to calculate odds ratios and 95% confidence intervals. A multivariate regression model including 9 categorical variables was performed to identify the significant factors associated with SIRR. Only 1 side was included in the bilateral cases on the advice of the statistician. The inclusion of each side as a separate case was discounted because the 2 sides are not independent variables. The side was chosen at random by the statistician, so that both affected sides had an equal probability to be included in the analysis. All statistical tests were 2 sided at a 5 0.05. RESULTS
Fig 2. CBCT views showing various configuration patterns of SIRR associated with maxillary canine impaction: A, oblique; B, horizontal. Red arrows indicate the resorption area.
Fig 3. Severely resorbed maxillary left lateral incisor associated with canine impaction.
canine dental follicle graded in 1-mm intervals (0-1 mm, grade 1; 1-2 mm, grade 2; 2-3 mm, grade 3; $3 mm, grade 4); and (9) anomalies of the lateral incisors adjacent to the impacted canines (congenitally missing, small, or peg-shaped).5 Statistical analysis
The statistical methods for the associations between each variable and SIRR included chi-square tests and
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In the total study group of 55 patients, there were 96 severely resorbed maxillary incisors—69 lateral and 27 central (ratio 2.5:1)—a difference that was highly statistically significant (P 5 0.001; Table I). The most frequently resorbed tooth associated with maxillary canine impaction was the maxillary right lateral incisor (41.6%). The study group included 22 patients (20 girls, 2 boys) with bilateral impacted canines, and the control group included 15 bilateral subjects (12 female, 3 male). In the study group among the bilateral impacted canine patients, 3 (13.6%) had unilateral SIRR. The control group was older than the study group (14.2 6 4.7 vs 12.0 6 1.4 years) because of the presence of 3 adults (.20 years old). A markedly elevated prevalence of SIRR was associated with maxillary canine impaction in female subjects (83.6% in the study group vs 54.4% in the control group) compared with male subjects (16.4% in the study group vs 45.6% in the control group; P \0.001; Fig 5). When studied in isolation, the risk of female patients having SIRR was 4.2 times higher than in males. In both groups, the prevalence of palatally impacted canines was higher than that of buccally impacted canines by a ratio just under 2:1 (Fig 6). No statistically significant differences were seen between the study and control groups. In the study group, most canines (64.9%) were located close to the midline, mainly in sector 5 (35%) and sector 4 (29.9%) (Fig 7). In the control group, only a small percentage of the canines were seen in sector 5 (13.9%), with larger percentages in sectors 3 (33.3%) and 2 (20.8%). The differences between the distributions of canines were almost statistically significant (P 5 0.06). When studied separately, the risk of SIRR in association with canines positioned in sector 5 was 5.5 and 3.5 times higher than for canines positioned in sectors 2 and 3, respectively.
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Fig 4. Schematic illustration of the projection of the canine in the panoramic image: A, canine position in sectors 1 through 5 (the most mesial contour of the crown is taken)7; B, canine angulation to the midline14,15 (grade 1, 0 -15 ; grade 2, 16 -30 ; grade 3, $31 ); C, canine overlap of the adjacent incisor root14,15 (grade 1, no horizontal overlap; grade 2, less than half of the root width; grade 3, more than half, but less than the whole root width; grade 4, complete overlap of root width or more); D, vertical canine crown height16 (apical, middle, coronal).
Table I. Distribution of SIRR according to the maxil-
lary incisors (N 5 55 patients) Resorbed maxillary incisor Right Right Left Left lateral central central lateral Total No. of teeth (%) 40 (41.6) 18 (18.8) 9 (9.4) 29 (30.2) 96 (100)
In the study group, 68.8% of the impacted canines were angulated $31 (grade 3), 20.8% of the canines were between 16 and 30 (grade 2), and 10.4% of the canines were between 0 and 15 (grade 1) (Fig 8). In contrast, in the control group, only 40.3% of the canines were grade 3, 36.1% were grade 2, and 23.6% were grade 1. The increased prevalence of severely angulated maxillary canines (grade 3) in association with SIRR was statistically significant in comparison with the controls (P 5 0.02). When this factor was studied in isolation, the risk of SIRR associated with a canine in sector 3 was about 3 times more than the risk for SIRR in canines in sectors 1 and 2.
The overlap of the adjacent incisor root was more toward the more extreme end of the grading in the SIRR group, with 64.9% of impacted maxillary canines exhibiting complete overlap of the adjacent root or beyond (grade 4) compared with 26.4% in the control group (Fig 9). Only 14.3% of the canines showed no or less than half root horizontal overlap (grade 1) in the study group, compared with 45.8% in the control group, and the differences were highly statistically significant (P 5 0.001). When studied separately, the risks of SIRR in canines graded 4 were 17.8, 5.8, and 3 times more than in canines graded 1, 2, and 3, respectively. In the vertical plane, more than half (62.3%) of the impacted maxillary canines in the SIRR-affected group were located in the middle third of the adjacent incisor root (Fig 10).16 Apically positioned crowns of involved maxillary canines comprised 15.6%, and coronally positioned crowns, 22.1% of the total. The differences in the vertical location were highly statistically significant (P 5 0.001). The pattern was different in the control group, with a much higher incidence of coronally positioned crowns (43.1%) and smaller incidences of middle
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Fig 5. Distribution of the SIRR and control groups according to sex.
Fig 6. The buccolingual location of the impacted canines (palatal, buccal, or in line of the arch) in the SIRR and control groups. Fig 8. Canine angulation to the midline according to the study of Stivaros and Mandall.14
Fig 7. Distribution of the impacted canines in sectors, according to the study of Ericson and Kurol.7
(45.8%) and apical canines (11.1%) compared with the SIRR group (P 5 0.05). When this factor was studied in isolation, the risk of SIRR was 2.7 times higher for a canine in the middle third than for a canine positioned coronally. The dental follicle was graded 4 ($3 mm) in 19.5% of the canines in the SIRR group (Fig 11). Grade 4 dental follicles were not observed in any control subject. The differences were statistically significant (P 5 0.03). Grades 3 and 4 dental follicles ($2 mm) were found in 41.6% of the patients in the study group compared with 8.3% of the subjects in the control group.
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Fig 9. Canine overlap of the adjacent incisor root according to the study of Stivaros and Mandall.14
The patients with congenital absence of the lateral incisor, but whose central incisor was the affected tooth, were combined with subjects with anomalous lateral incisors (Fig 12). In the study group, 20.0% of the lateral incisors were anomalous (congenitally missing and peg-shaped), compared with 42.1% in the control group. Significantly, 31.6% of the lateral incisors in the control group were small, whereas no small lateral incisors with SIRR were found. Because of the total absence of small lateral incisors, all
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Fig 12. Maxillary lateral incisor anomalies in the SIRR and control groups. Fig 10. Distribution of impacted canines in the vertical plane according to the study of Chaushu et al.16
Table II. Multivariate analysis of effects Effect Wald chi-square Probability .chi-square Age 1.5581 0.2119 Sex 5.0492 0.0246* Vertical position 0.5261 0.7687 Sector 2.1351 0.7109 Horizontal overlap 2.5120 0.2848 Buccolingual position 1.2401 0.2654 Angulation 2.3445 0.3097 Dental follicle size 10.0736 0.0065* Anomalous lateral 5.5319 0.0187* incisors *Significant association with SIRR.
DISCUSSION Fig 11. Dental follicle size in the SIRR and control groups.
anomalous lateral incisors were grouped together for the statistical analysis. The risk of SIRR for a normal lateral incisor was 5.8 times greater than for an anomalous lateral incisor. The multivariate analysis considered all 9 parameters together (Table II). The “buccolingual position” variable took into account only buccal and palatal canines because of the small number of “in line of the arch” canines. Similarly, the anomalous lateral incisors were grouped together compared with the normal lateral incisors because of the lack of small incisors in the SIRR group. The analysis showed that only 3 factors significantly discriminated between the groups: sex, dental follicle size, and anomalous lateral incisors. More specifically, female subjects had a 4.2 times higher risk for SIRR than did males; dental follicles wider than 2 mm increased the risk by 8.3 compared with normal dental follicles; and lateral incisors of normal shape and size increased the risk for SIRR by 5.8 compared with anomalous lateral incisors.
The etiologic factors underlying root resorption caused by the neighboring erupting tooth are still unknown. Some authors suggested that the erupting tooth exerts physical pressure.17-20 Others postulated that the pressure is caused by the dental follicle and not by the tooth per se.17 The fact that maxillary lateral incisors are more affected by SIRR than central incisors, reported in this study and also in previous studies, partially supports these theories, which are based on the closer intimacy of the canine to the lateral incisor than to the central incisor.2,20-22 But why the roots resorb in one patient and are intact in another patient, in whom the canine is identically situated, remains an enigma. Our study points toward a multifactorial etiology including both general systemic factors (sex) and local factors (aberrant position of the canine, follicle size, anomalous incisors). Incisor root resorption associated with impacted maxillary canines has been reported to occur more in female patients, but the number of affected persons in that study was inadequate to draw valid conclusions.1 Lai et al20 noted that female subjects seem to be more affected than males, but their results did not reach statistical significance. Other authors found no differences
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with regard to sex.18,21,22 However, none of these investigations restricted their samples to severe cases, which comprised only 11,21 20,20 24,22 and 4118 teeth within larger samples. Thus, severe resorption was largely unrepresented, in contrast to our study (96 teeth). Furthermore, their definition of “severe” or “resorption through the pulp” included subjects whose resorption was limited to the root apex. If the inclusion criteria of our study had been applied, their samples would have been further reduced. It is imperative to note that canine-related resorption of incisor roots does not generally shorten the roots in a horizontal manner but, rather, causes oblique resorption, which is usually found on the palatal or the labial aspect, depending on the location of the impacted canine. To the best of our knowledge, this study includes the largest sample of patients with severe root resorption linked to impacted canines in the literature. The results show a definite predilection for SIRR in female subjects (5:1 ratio, female to male) compared with the control group (almost a 1:1 ratio). These results regarding the distribution of the sexes in the control group support previous findings from a random population of the same ethnicity living in the same general area.23 However, in other previous studies, impacted canines were more frequently found in female subjects than in males; therefore, it may be claimed that the apparent predilection of root resorption in females merely reflects this imbalance. In studies of orthodontic patient samples, the ratios of impacted canines in females to males were 2.3:1 in an American sample,24 2.5:1 in an Israeli sample,5 and 3:1 in each of Welsh,25 American,26 and Italian orthodontic samples.27 Thus, the finding reported here of a 5:1 female-tomale ratio of SIRR indicates an obvious affinity for the condition among female patients, over and above their apparent naturally occurring predilection for canine impaction. Although the reasons for this are unknown, it must be assumed that genetic or hormonal etiologic factors, as well as girls' earlier skeletal growth spurt, earlier eruption of canines, and in general earlier dental development; jaw discrepancies; and root and crown sexual dimorphism might play significant roles. Patients with bilateral maxillary canine impaction were seen here in considerable numbers (40% in the study group, 26% in the control group); this has been reported elsewhere.28 However, the fact that 19 of 22 (86.4%) patients exhibited bilateral canine-related SIRR was surprising. This bilateral pattern further supports a more general, systemic etiology, in addition to local factors for SIRR. The control group of consecutive patients was older than the SIRR group. SIRR will typically be diagnosed
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and treatment initiated at an earlier age than for a patient with routine canine impaction. Furthermore, a significant proportion of the affected teeth may not survive into adulthood without treatment. Local factors can be divided into those related to the canine (position and size of the dental follicle) and those related to the size and shape of the affected lateral incisor. In this study, a majority of the examined SIRRaffected incisors were associated with palatal impaction; this was almost double the number with buccal impaction (Fig 6). However, this is similar to the palatal-tobuccal impaction ratio, as can be seen in the control group and as reported in the literature.27,29-31 Lai et al20 also found no difference in the prevalence of root resorption between labial and palatal canines. In contrast, SIRR was associated with severely horizontally displaced impacted canines that were closer to the midline and severely mesially angulated canines, overlapping the lateral incisors. This confirms results published previously.1,7,32 In the vertical plane, the most riskprone canines were those superimposed on the middle third of the adjacent maxillary incisor root. The fact that the middle third of the maxillary incisor root is most commonly resorbed in association with maxillary canine impaction has already been reported.2,20,32-34 In their earlier study, using plain film radiography, Ericson and Kurol33 found that 82% of the lateral incisors were resorbed in the middle third and only 13% apically, with the remainder cervically resorbed. More recent studies with computerized tomography have confirmed that maxillary incisor resorption occurs most commonly in the middle third of the roots.2,20 Our results support the view that pressure from an enlarged dental follicle may increase the risk for root resorption. This finding is in contrast to other studies, which claimed that the existing contact relationship of the impacted maxillary canine with the lateral incisor root is critical.19,22 However, our study included only the most severe cases of root resorption, and this could be the reason for the apparent conflict. In this sample, SIRR was not seen in any of the small lateral incisors. This study is consistent with previous studies,5,11 in which anomalous lateral incisors have been reported to be less likely to develop severe root resorption, compared with normally shaped and sized lateral incisors.11,35 One may be permitted to speculate that in patients with impacted canines, the normally sized and early developing lateral incisor root obstructs the deviated eruption path of the canine and consequently stands a greater chance of being damaged by resorption.11 Conversely, shorter36 or late developing5 roots of anomalous incisors are
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more easily bypassed and not endangered by the impacted canines. This finding confirms the results of a recent study, in which small lateral incisors were found to be less likely to develop orthodontically related root resorption.36 When all of these factors were examined together in the multivariate analysis model, only 1 general factor (sex) and 2 local factors (enlarged dental follicle and normally sized and shaped lateral incisor) were found to significantly increase the risk of SIRR. However, this might be related to sample size and the number of variables. Future research on larger canine-related SIRR samples might show that the other factors, which were significantly associated when each was studied in isolation, also reach significance in a multivariate model that combines them all. CONCLUSIONS
1
2
3 4
The etiology of impacted canine-associated SIRR is multifactorial, including both systemic and local factors. The risk for SIRR is increased in female patients with enlarged dental follicles and anomalous lateral incisors. Lateral incisors are affected more than central incisors, and the chance of bilateral occurrence is high. SIRR is found in both palatally and buccally impacted maxillary canines but is associated with the more severely displaced canines, situated in the middle third of the adjacent incisor roots.
Screening for SIRR is recommended for all patients with impacted canines, but especially for female patients with impacted maxillary canines surrounded by enlarged follicles and with normally sized and shaped lateral incisors. When one incisor is diagnosed with SIRR in a bilateral impaction, the contralateral incisor should also be carefully screened. Severely mesially angulated canines positioned over the middle third of the adjacent incisor root should also be treated with suspicion. This information is of major importance for early diagnosis by the orthodontist, but also for pediatric or general dentists who are frequently the first practitioners to meet the patients, and for surgeons so that they can plan the most appropriate interdisciplinary treatment. REFERENCES 1. Ericson S, Kurol J. Radiographic examination of ectopically erupting maxillary canines. Am J Orthod Dentofacial Orthop 1987;91: 483-92. 2. Ericson S, Kurol J. Resorption of incisors after ectopic eruption of maxillary canines: a CT study. Angle Orthod 2000;70:415-23.
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3. Walker L, Enciso R, Mah J. Three-dimensional localization of maxillary canines with cone-beam computed tomography. Am J Orthod Dentofacial Orthop 2005;128:418-23. 4. Bjerklin K, Guitirokh CH. Maxillary incisor root resorption induced by ectopic canines. A follow-up study, 13-28 years posttreatment. Angle Orthod 2011;81:800-6. 5. Becker A, Smith P, Behar R. The incidence of anomalous lateral incisors in relation to palatally displaced cuspids. Angle Orthod 1981;51:24-9. 6. Ericson S, Kurol J. Radiographic assessment of maxillary canine eruption in children with clinical signs of eruption disturbance. Eur J Orthod 1986;8:133-40. 7. Ericson S, Kurol J. Resorption of maxillary lateral incisors caused by ectopic eruption of canines. Am J Orthod Dentofacial Orthop 1988;94:503-13. 8. Brown ID, Matthews RW. Apical resorption of a maxillary lateral incisor from a misplaced canine in a 17 year old. A case report. Br J Orthod 1981;8:3-5. 9. Sasakura H, Yoshida T, Murayama S, Hanada K, Nakajima T. Root resorption of upper permanent incisor caused by impacted canine. Int J Oral Surg 1984;13:299-306. 10. Regan D, Craig GT. External resorption of a maxillary lateral incisor by a labially placed canine: pathology and management. Br J Orthod 1988;15:161-7. 11. Brin I, Becker A, Zilberman Y. Resorbed lateral incisors adjacent to impacted canines have normal crown size. Am J Orthod Dentofacial Orthop 1993;104:60-6. 12. Becker A, Chaushu S. Long-term follow-up of severely resorbed maxillary incisors after resolution of an etiologically associated impacted canine. Am J Orthod Dentofacial Orthop 2005;127:650-4. 13. Levander E, Malmgren O. Long-term follow-up of maxillary incisors with severe apical root resorption. Eur J Orthod 2000;22:85-92. 14. Stivaros N, Mandall NA. Radiographic factors affecting the management of impacted upper permanent canines. J Orthod 2000; 27:169-73. 15. Power M, Short BE. An investigation into the response of palatally displaced canines to the removal of deciduous canines and an assessment of factors contributing to favourable eruption. Br J Orthod 1993;20:215-23. 16. Chaushu S, Chaushu G, Becker A. The use of panoramic radiographs to localize displaced maxillary canines. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;88:511-6. 17. Marks SC, Schroeder HE, Andreasen JO. Theories and mechanism of tooth eruption. In: Andreasen JO, K€ olsen-Pedersen J, Laskin DM, editors. Textbook and color atlas of tooth impactions. St Louis: Mosby; 1997. p. 20-65. 18. Ericson S, Kurol J. Incisor resorptions due to ectopic maxillary canines imaged by computerized tomography: a comparative study in extracted teeth. Angle Orthod 2000;70:276-83. 19. Ericson S, Bjerklin K, Falahat B. Does the canine dental follicle cause resorption of permanent incisor roots? A computed tomographic study of erupting maxillary canines. Angle Orthod 2002;72:95-104. 20. Lai CS, Bornstein MM, Mock L, Heuberger BM, Dietrich T, Katsaros C. Impacted maxillary canines and root resorptions of neighbouring teeth: a radiographic analysis using cone-beam computed tomography. Eur J Orthod 2013;35:529-38. 21. Falahat B, Ericson S, Mak D'Amico R, Bjerklin K. Incisor root resorption due to ectopic maxillary canines: a long-term radiographic follow-up. Angle Orthod 2008;78:778-85. 22. Strbac GD, Foltin A, Gahleitner A, Bantleon HP, Watzek G, Bernhart T. The prevalence of root resorption of maxillary incisors caused by impacted maxillary canines. Clin Oral Investig 2013;17: 553-64.
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23. Brin I, 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;8:12-6. 24. Dachi SF, Howell FV. A survey of 3874 routine full-mouth radiographs. II. A study of impacted teeth. Oral Surg Oral Med Oral Pathol 1961;14:1165-9. 25. 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;16:9-16. 26. Johnston WD. Treatment of palatally impacted canine teeth. Am J Orthod 1969;56:589-96. 27. Sacerdoti R, Baccetti T. Dentoskeletal features associated with unilateral or bilateral palatal displacement of maxillary canines. Angle Orthod 2004;74:725-32. 28. Becker A, Peck S, Peck L, Kataja M. Palatal canine displacement: guidance theory or anomaly of genetic origin? Angle Orthod 1995;65:95-102. 29. Mucedero M, Ricchiuti MR, Cozza P, Baccetti T. Prevalence rate and dentoskeletal features associated with buccally displaced maxillary canines. Eur J Orthod 2013;35:305-9.
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30. Nordenram A, Stromberg C. Positional variations of the impacted upper canine: a clinical and radiologic study. Oral Surg Oral Med Oral Pathol 1966;22:711-4. 31. Becker A. Orthodontic treatment of impacted teeth. 3rd ed. Oxford, UK: Wiley-Blackwell; 2012. 32. Alqerban A, Jacobs R, Lambrechts P, Loozen G, Willems G. Root resorption of the maxillary lateral incisor caused by impacted canine: a literature review. Clin Oral Investig 2009; 13:247-59. 33. Ericson S, Kurol J. Incisor resorption caused by maxillary cuspids: a radiographic study. Angle Orthod 1987;57:332-46. 34. Rimes RJ, Mitchell CN, Willmot DR. Maxillary incisor resorption in relation to the ectopic canine: a review of 26 patients. Eur J Orthod 1977;19:79-84. 35. Becker A, Zilberman Y, Tzur B. Root length of lateral incisors adjacent to palatally-displaced maxillary cuspids. Angle Orthod 1984; 54:218-25. 36. Kook YA, Park S, Sameshima GT. Peg-shaped and small lateral incisors not at higher risk for root resorption. Am J Orthod Dentofacial Orthop 2003;123:253-8.
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Predisposing factors for severe incisor root resorption associated with impacted maxillary canines Stella Chaushu,a Karolina Kaczor-Urbanowicz,b Małgorzata Zadurska,c and Adrian Beckerd Jerusalem, Israel, and Warsaw, Poland
Introduction: Severe incisor root resorption (SIRR) associated with impacted maxillary canines is rare but has important implications. Early diagnosis and treatment are imperative. In this investigation, we aimed to identify predisposing factors for impacted canine-linked SIRR. Methods: Clinical and radiographic data of 55 consecutive patients (77 canines) with SIRR of 96 incisors were compared with data from 57 consecutive control subjects (72 canines). The studied variables were age, sex, position of the impacted canine, size of the dental follicle, and incidence of anomalous lateral incisors. Results: Lateral incisors were more often affected than central incisors, and bilateral SIRR was common. When each variable was examined separately, SIRR was significantly associated with female sex, severely mesiodistally displaced and vertically positioned canines in the middle third of the adjacent incisor root, dental follicles wider than 2 mm, and normal lateral incisors. The multivariate statistical analysis showed that the risk for SIRR was significantly higher in female subjects (4.2 times) with enlarged dental follicles (8.3 times) and normal lateral incisors (5.8 times). Conclusions: SIRR should be carefully screened in female patients with enlarged dental follicles and normal lateral incisors. A greater degree of canine displacement might also be associated with SIRR. (Am J Orthod Dentofacial Orthop 2015;147:52-60)
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arly studies with plain film radiography indicated that canine-related incisor root resorption occurs in approximately 12% of patients.1 Yet the authors were at pains to point out that with plain film radiography, it was impossible to properly assess the buccolingual aspects of the incisor roots. With the advent of more advanced imaging techniques such as computerized tomography scanning, detectable root resorption was diagnosed in 38% of resorbed lateral incisors and 9% of central incisors.2 Moreover, from the study of Walker et al3 using cone-beam computed
a Associate professor and chair, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. b Postgraduate student, International Postgraduate Orthodontic Program, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. c Associate professor and head, Department of Orthodontics, Medical University of Warsaw, Warsaw, Poland. d Clinical associate professor emeritus, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, Jerusalem, Israel. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Address correspondence to: Stella Chaushu, Department of Orthodontics, Hebrew University-Hadassah School of Dental Medicine, PO Box 12272, Jerusalem 91120, Israel; e-mail, [email protected]. Submitted, February 2014; revised and accepted, September 2014. 0889-5406/$36.00 Copyright Ó 2015 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2014.09.012
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tomography (CBCT), detection capability increased to 67% of cases of which 11% were central incisors and 4% were premolars.3,4 Congenitally missing, small, and peg-shaped maxillary lateral incisors are highly correlated with maxillary canine palatal impaction.5 Whereas resorption of maxillary incisor roots is a well-recognized phenomenon that can occur in patients with impacted canines,6-11 these anomalous lateral incisors with reduced size or abnormal shape have been reported to be less at risk to develop severe root resorption, compared with patients with normally shaped and sized lateral incisors.11 Fortunately, severe incisor root resorption (SIRR) associated with impacted maxillary canines is rare, but when is appears, it threatens the long-term survival of the affected teeth. Early diagnosis and treatment are imperative to save the affected tooth.12,13 At present, evidence-based information regarding potential predisposing factors for SIRR is lacking. The aim of this study was to identify predisposing risk factors for SIRR associated with impacted maxillary canines. MATERIAL AND METHODS
The study group included 55 consecutive patients with impacted maxillary canines and SIRR, and the
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Fig 1. A 14-year-old boy with severely resorbed maxillary right lateral incisor associated with canine impaction: A, panoramic view; B, periapical view; C, transaxial and 3-dimensional CBCT views.
control group included 57 consecutive patients with impacted maxillary canines without SIRR from the Department of Orthodontics of the Hebrew University in Jerusalem, Israel, and the Medical University of Warsaw in Poland and from the private practices of 2 authors (S.C. and A.B.). The inclusion criterion for the study group was SIRR of at least 1 maxillary incisor associated with an adjacent impacted canine in untreated healthy patients. Diagnosis of SIRR was made from the available panoramic and periapical radiographs that had been taken earlier with the intention of commencing orthodontic treatment (Fig 1, A and B). For most of the patients (75%) in the study group, CBCT images were also available for examination (Fig 1, C). CBCT was considered superfluous for patients in whom SIRR could be diagnosed on plain films alone. When CBCT was unavailable for a patient, the buccolingual position of the ectopic canine was determined using the routine tube-shift method and confirmed by the treating orthodontist or surgeon during surgical exposure. In the control group, CBCT had been available for all subjects to exclude any signs of root resorption. The radiographs were examined by 2 authors (S.C. and A.B.) using an x-ray viewer with standard light intensity. The CBCT examinations were performed with an iCAT scanner (12-bit; Imaging Sciences International, Hatfield, Pa) with the following parameters: 26.9 seconds scan time, 120 kV, 5 mA, field of view size of 13 (height) 3 16 (diameter) cm, and 0.2-mm voxel. The
resultant slice image data were converted to 3-dimensional images in DICOM format, reconstructed by XoranCat software (version 3.1.62; Xoran Technologies, Inc, Ann Arbor, Mich) and imported to be evaluated in i-CATVision (2008 version 1.8.1.10; Imaging Sciences International). The reconstructed image had a 2-mm slice thickness. Traditionally, root resorption has been described elsewhere as horizontal shortening of the root.14 The pattern is different for SIRR associated with impacted maxillary canines, where the resorption is mostly oblique rather than horizontal (Fig 2). Root resorption was measured on the radiographs, and it was considered severe when it affected more than a third of the length of the root, but not specifically its apical part (Fig 3). The exclusion criteria for the sample were root resorption of maxillary incisors less than one third of their expected root length, root resorption secondary to trauma or pulp pathology, or the presence of cysts and other pathologies. The numbers of involved central vs lateral incisors, and unilateral vs bilateral cases, were recorded. The associations between SIRR and the following variables were evaluated: (1) age; (2) sex; (3) buccolingual location: palatally, buccally, or in the line of the arch; (4) mesiodistal location: sector7 (Fig 4, A); (5) angulation to the midline14,15 (Fig 4, B); (6) overlap of the adjacent incisor14,15 (Fig 4, C); (7) vertical crown height relative to the adjacent incisor root: apical, middle, or coronal16 (Fig 4, D); (8) maximum width of the
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logistic regression analyses with SAS software (version 9.4; SAS Institute, Cary, NC) to calculate odds ratios and 95% confidence intervals. A multivariate regression model including 9 categorical variables was performed to identify the significant factors associated with SIRR. Only 1 side was included in the bilateral cases on the advice of the statistician. The inclusion of each side as a separate case was discounted because the 2 sides are not independent variables. The side was chosen at random by the statistician, so that both affected sides had an equal probability to be included in the analysis. All statistical tests were 2 sided at a 5 0.05. RESULTS
Fig 2. CBCT views showing various configuration patterns of SIRR associated with maxillary canine impaction: A, oblique; B, horizontal. Red arrows indicate the resorption area.
Fig 3. Severely resorbed maxillary left lateral incisor associated with canine impaction.
canine dental follicle graded in 1-mm intervals (0-1 mm, grade 1; 1-2 mm, grade 2; 2-3 mm, grade 3; $3 mm, grade 4); and (9) anomalies of the lateral incisors adjacent to the impacted canines (congenitally missing, small, or peg-shaped).5 Statistical analysis
The statistical methods for the associations between each variable and SIRR included chi-square tests and
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In the total study group of 55 patients, there were 96 severely resorbed maxillary incisors—69 lateral and 27 central (ratio 2.5:1)—a difference that was highly statistically significant (P 5 0.001; Table I). The most frequently resorbed tooth associated with maxillary canine impaction was the maxillary right lateral incisor (41.6%). The study group included 22 patients (20 girls, 2 boys) with bilateral impacted canines, and the control group included 15 bilateral subjects (12 female, 3 male). In the study group among the bilateral impacted canine patients, 3 (13.6%) had unilateral SIRR. The control group was older than the study group (14.2 6 4.7 vs 12.0 6 1.4 years) because of the presence of 3 adults (.20 years old). A markedly elevated prevalence of SIRR was associated with maxillary canine impaction in female subjects (83.6% in the study group vs 54.4% in the control group) compared with male subjects (16.4% in the study group vs 45.6% in the control group; P \0.001; Fig 5). When studied in isolation, the risk of female patients having SIRR was 4.2 times higher than in males. In both groups, the prevalence of palatally impacted canines was higher than that of buccally impacted canines by a ratio just under 2:1 (Fig 6). No statistically significant differences were seen between the study and control groups. In the study group, most canines (64.9%) were located close to the midline, mainly in sector 5 (35%) and sector 4 (29.9%) (Fig 7). In the control group, only a small percentage of the canines were seen in sector 5 (13.9%), with larger percentages in sectors 3 (33.3%) and 2 (20.8%). The differences between the distributions of canines were almost statistically significant (P 5 0.06). When studied separately, the risk of SIRR in association with canines positioned in sector 5 was 5.5 and 3.5 times higher than for canines positioned in sectors 2 and 3, respectively.
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Fig 4. Schematic illustration of the projection of the canine in the panoramic image: A, canine position in sectors 1 through 5 (the most mesial contour of the crown is taken)7; B, canine angulation to the midline14,15 (grade 1, 0 -15 ; grade 2, 16 -30 ; grade 3, $31 ); C, canine overlap of the adjacent incisor root14,15 (grade 1, no horizontal overlap; grade 2, less than half of the root width; grade 3, more than half, but less than the whole root width; grade 4, complete overlap of root width or more); D, vertical canine crown height16 (apical, middle, coronal).
Table I. Distribution of SIRR according to the maxil-
lary incisors (N 5 55 patients) Resorbed maxillary incisor Right Right Left Left lateral central central lateral Total No. of teeth (%) 40 (41.6) 18 (18.8) 9 (9.4) 29 (30.2) 96 (100)
In the study group, 68.8% of the impacted canines were angulated $31 (grade 3), 20.8% of the canines were between 16 and 30 (grade 2), and 10.4% of the canines were between 0 and 15 (grade 1) (Fig 8). In contrast, in the control group, only 40.3% of the canines were grade 3, 36.1% were grade 2, and 23.6% were grade 1. The increased prevalence of severely angulated maxillary canines (grade 3) in association with SIRR was statistically significant in comparison with the controls (P 5 0.02). When this factor was studied in isolation, the risk of SIRR associated with a canine in sector 3 was about 3 times more than the risk for SIRR in canines in sectors 1 and 2.
The overlap of the adjacent incisor root was more toward the more extreme end of the grading in the SIRR group, with 64.9% of impacted maxillary canines exhibiting complete overlap of the adjacent root or beyond (grade 4) compared with 26.4% in the control group (Fig 9). Only 14.3% of the canines showed no or less than half root horizontal overlap (grade 1) in the study group, compared with 45.8% in the control group, and the differences were highly statistically significant (P 5 0.001). When studied separately, the risks of SIRR in canines graded 4 were 17.8, 5.8, and 3 times more than in canines graded 1, 2, and 3, respectively. In the vertical plane, more than half (62.3%) of the impacted maxillary canines in the SIRR-affected group were located in the middle third of the adjacent incisor root (Fig 10).16 Apically positioned crowns of involved maxillary canines comprised 15.6%, and coronally positioned crowns, 22.1% of the total. The differences in the vertical location were highly statistically significant (P 5 0.001). The pattern was different in the control group, with a much higher incidence of coronally positioned crowns (43.1%) and smaller incidences of middle
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Fig 5. Distribution of the SIRR and control groups according to sex.
Fig 6. The buccolingual location of the impacted canines (palatal, buccal, or in line of the arch) in the SIRR and control groups. Fig 8. Canine angulation to the midline according to the study of Stivaros and Mandall.14
Fig 7. Distribution of the impacted canines in sectors, according to the study of Ericson and Kurol.7
(45.8%) and apical canines (11.1%) compared with the SIRR group (P 5 0.05). When this factor was studied in isolation, the risk of SIRR was 2.7 times higher for a canine in the middle third than for a canine positioned coronally. The dental follicle was graded 4 ($3 mm) in 19.5% of the canines in the SIRR group (Fig 11). Grade 4 dental follicles were not observed in any control subject. The differences were statistically significant (P 5 0.03). Grades 3 and 4 dental follicles ($2 mm) were found in 41.6% of the patients in the study group compared with 8.3% of the subjects in the control group.
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Fig 9. Canine overlap of the adjacent incisor root according to the study of Stivaros and Mandall.14
The patients with congenital absence of the lateral incisor, but whose central incisor was the affected tooth, were combined with subjects with anomalous lateral incisors (Fig 12). In the study group, 20.0% of the lateral incisors were anomalous (congenitally missing and peg-shaped), compared with 42.1% in the control group. Significantly, 31.6% of the lateral incisors in the control group were small, whereas no small lateral incisors with SIRR were found. Because of the total absence of small lateral incisors, all
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Fig 12. Maxillary lateral incisor anomalies in the SIRR and control groups. Fig 10. Distribution of impacted canines in the vertical plane according to the study of Chaushu et al.16
Table II. Multivariate analysis of effects Effect Wald chi-square Probability .chi-square Age 1.5581 0.2119 Sex 5.0492 0.0246* Vertical position 0.5261 0.7687 Sector 2.1351 0.7109 Horizontal overlap 2.5120 0.2848 Buccolingual position 1.2401 0.2654 Angulation 2.3445 0.3097 Dental follicle size 10.0736 0.0065* Anomalous lateral 5.5319 0.0187* incisors *Significant association with SIRR.
DISCUSSION Fig 11. Dental follicle size in the SIRR and control groups.
anomalous lateral incisors were grouped together for the statistical analysis. The risk of SIRR for a normal lateral incisor was 5.8 times greater than for an anomalous lateral incisor. The multivariate analysis considered all 9 parameters together (Table II). The “buccolingual position” variable took into account only buccal and palatal canines because of the small number of “in line of the arch” canines. Similarly, the anomalous lateral incisors were grouped together compared with the normal lateral incisors because of the lack of small incisors in the SIRR group. The analysis showed that only 3 factors significantly discriminated between the groups: sex, dental follicle size, and anomalous lateral incisors. More specifically, female subjects had a 4.2 times higher risk for SIRR than did males; dental follicles wider than 2 mm increased the risk by 8.3 compared with normal dental follicles; and lateral incisors of normal shape and size increased the risk for SIRR by 5.8 compared with anomalous lateral incisors.
The etiologic factors underlying root resorption caused by the neighboring erupting tooth are still unknown. Some authors suggested that the erupting tooth exerts physical pressure.17-20 Others postulated that the pressure is caused by the dental follicle and not by the tooth per se.17 The fact that maxillary lateral incisors are more affected by SIRR than central incisors, reported in this study and also in previous studies, partially supports these theories, which are based on the closer intimacy of the canine to the lateral incisor than to the central incisor.2,20-22 But why the roots resorb in one patient and are intact in another patient, in whom the canine is identically situated, remains an enigma. Our study points toward a multifactorial etiology including both general systemic factors (sex) and local factors (aberrant position of the canine, follicle size, anomalous incisors). Incisor root resorption associated with impacted maxillary canines has been reported to occur more in female patients, but the number of affected persons in that study was inadequate to draw valid conclusions.1 Lai et al20 noted that female subjects seem to be more affected than males, but their results did not reach statistical significance. Other authors found no differences
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with regard to sex.18,21,22 However, none of these investigations restricted their samples to severe cases, which comprised only 11,21 20,20 24,22 and 4118 teeth within larger samples. Thus, severe resorption was largely unrepresented, in contrast to our study (96 teeth). Furthermore, their definition of “severe” or “resorption through the pulp” included subjects whose resorption was limited to the root apex. If the inclusion criteria of our study had been applied, their samples would have been further reduced. It is imperative to note that canine-related resorption of incisor roots does not generally shorten the roots in a horizontal manner but, rather, causes oblique resorption, which is usually found on the palatal or the labial aspect, depending on the location of the impacted canine. To the best of our knowledge, this study includes the largest sample of patients with severe root resorption linked to impacted canines in the literature. The results show a definite predilection for SIRR in female subjects (5:1 ratio, female to male) compared with the control group (almost a 1:1 ratio). These results regarding the distribution of the sexes in the control group support previous findings from a random population of the same ethnicity living in the same general area.23 However, in other previous studies, impacted canines were more frequently found in female subjects than in males; therefore, it may be claimed that the apparent predilection of root resorption in females merely reflects this imbalance. In studies of orthodontic patient samples, the ratios of impacted canines in females to males were 2.3:1 in an American sample,24 2.5:1 in an Israeli sample,5 and 3:1 in each of Welsh,25 American,26 and Italian orthodontic samples.27 Thus, the finding reported here of a 5:1 female-tomale ratio of SIRR indicates an obvious affinity for the condition among female patients, over and above their apparent naturally occurring predilection for canine impaction. Although the reasons for this are unknown, it must be assumed that genetic or hormonal etiologic factors, as well as girls' earlier skeletal growth spurt, earlier eruption of canines, and in general earlier dental development; jaw discrepancies; and root and crown sexual dimorphism might play significant roles. Patients with bilateral maxillary canine impaction were seen here in considerable numbers (40% in the study group, 26% in the control group); this has been reported elsewhere.28 However, the fact that 19 of 22 (86.4%) patients exhibited bilateral canine-related SIRR was surprising. This bilateral pattern further supports a more general, systemic etiology, in addition to local factors for SIRR. The control group of consecutive patients was older than the SIRR group. SIRR will typically be diagnosed
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and treatment initiated at an earlier age than for a patient with routine canine impaction. Furthermore, a significant proportion of the affected teeth may not survive into adulthood without treatment. Local factors can be divided into those related to the canine (position and size of the dental follicle) and those related to the size and shape of the affected lateral incisor. In this study, a majority of the examined SIRRaffected incisors were associated with palatal impaction; this was almost double the number with buccal impaction (Fig 6). However, this is similar to the palatal-tobuccal impaction ratio, as can be seen in the control group and as reported in the literature.27,29-31 Lai et al20 also found no difference in the prevalence of root resorption between labial and palatal canines. In contrast, SIRR was associated with severely horizontally displaced impacted canines that were closer to the midline and severely mesially angulated canines, overlapping the lateral incisors. This confirms results published previously.1,7,32 In the vertical plane, the most riskprone canines were those superimposed on the middle third of the adjacent maxillary incisor root. The fact that the middle third of the maxillary incisor root is most commonly resorbed in association with maxillary canine impaction has already been reported.2,20,32-34 In their earlier study, using plain film radiography, Ericson and Kurol33 found that 82% of the lateral incisors were resorbed in the middle third and only 13% apically, with the remainder cervically resorbed. More recent studies with computerized tomography have confirmed that maxillary incisor resorption occurs most commonly in the middle third of the roots.2,20 Our results support the view that pressure from an enlarged dental follicle may increase the risk for root resorption. This finding is in contrast to other studies, which claimed that the existing contact relationship of the impacted maxillary canine with the lateral incisor root is critical.19,22 However, our study included only the most severe cases of root resorption, and this could be the reason for the apparent conflict. In this sample, SIRR was not seen in any of the small lateral incisors. This study is consistent with previous studies,5,11 in which anomalous lateral incisors have been reported to be less likely to develop severe root resorption, compared with normally shaped and sized lateral incisors.11,35 One may be permitted to speculate that in patients with impacted canines, the normally sized and early developing lateral incisor root obstructs the deviated eruption path of the canine and consequently stands a greater chance of being damaged by resorption.11 Conversely, shorter36 or late developing5 roots of anomalous incisors are
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more easily bypassed and not endangered by the impacted canines. This finding confirms the results of a recent study, in which small lateral incisors were found to be less likely to develop orthodontically related root resorption.36 When all of these factors were examined together in the multivariate analysis model, only 1 general factor (sex) and 2 local factors (enlarged dental follicle and normally sized and shaped lateral incisor) were found to significantly increase the risk of SIRR. However, this might be related to sample size and the number of variables. Future research on larger canine-related SIRR samples might show that the other factors, which were significantly associated when each was studied in isolation, also reach significance in a multivariate model that combines them all. CONCLUSIONS
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The etiology of impacted canine-associated SIRR is multifactorial, including both systemic and local factors. The risk for SIRR is increased in female patients with enlarged dental follicles and anomalous lateral incisors. Lateral incisors are affected more than central incisors, and the chance of bilateral occurrence is high. SIRR is found in both palatally and buccally impacted maxillary canines but is associated with the more severely displaced canines, situated in the middle third of the adjacent incisor roots.
Screening for SIRR is recommended for all patients with impacted canines, but especially for female patients with impacted maxillary canines surrounded by enlarged follicles and with normally sized and shaped lateral incisors. When one incisor is diagnosed with SIRR in a bilateral impaction, the contralateral incisor should also be carefully screened. Severely mesially angulated canines positioned over the middle third of the adjacent incisor root should also be treated with suspicion. This information is of major importance for early diagnosis by the orthodontist, but also for pediatric or general dentists who are frequently the first practitioners to meet the patients, and for surgeons so that they can plan the most appropriate interdisciplinary treatment. REFERENCES 1. Ericson S, Kurol J. Radiographic examination of ectopically erupting maxillary canines. Am J Orthod Dentofacial Orthop 1987;91: 483-92. 2. Ericson S, Kurol J. Resorption of incisors after ectopic eruption of maxillary canines: a CT study. Angle Orthod 2000;70:415-23.
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3. Walker L, Enciso R, Mah J. Three-dimensional localization of maxillary canines with cone-beam computed tomography. Am J Orthod Dentofacial Orthop 2005;128:418-23. 4. Bjerklin K, Guitirokh CH. Maxillary incisor root resorption induced by ectopic canines. A follow-up study, 13-28 years posttreatment. Angle Orthod 2011;81:800-6. 5. Becker A, Smith P, Behar R. The incidence of anomalous lateral incisors in relation to palatally displaced cuspids. Angle Orthod 1981;51:24-9. 6. Ericson S, Kurol J. Radiographic assessment of maxillary canine eruption in children with clinical signs of eruption disturbance. Eur J Orthod 1986;8:133-40. 7. Ericson S, Kurol J. Resorption of maxillary lateral incisors caused by ectopic eruption of canines. Am J Orthod Dentofacial Orthop 1988;94:503-13. 8. Brown ID, Matthews RW. Apical resorption of a maxillary lateral incisor from a misplaced canine in a 17 year old. A case report. Br J Orthod 1981;8:3-5. 9. Sasakura H, Yoshida T, Murayama S, Hanada K, Nakajima T. Root resorption of upper permanent incisor caused by impacted canine. Int J Oral Surg 1984;13:299-306. 10. Regan D, Craig GT. External resorption of a maxillary lateral incisor by a labially placed canine: pathology and management. Br J Orthod 1988;15:161-7. 11. Brin I, Becker A, Zilberman Y. Resorbed lateral incisors adjacent to impacted canines have normal crown size. Am J Orthod Dentofacial Orthop 1993;104:60-6. 12. Becker A, Chaushu S. Long-term follow-up of severely resorbed maxillary incisors after resolution of an etiologically associated impacted canine. Am J Orthod Dentofacial Orthop 2005;127:650-4. 13. Levander E, Malmgren O. Long-term follow-up of maxillary incisors with severe apical root resorption. Eur J Orthod 2000;22:85-92. 14. Stivaros N, Mandall NA. Radiographic factors affecting the management of impacted upper permanent canines. J Orthod 2000; 27:169-73. 15. Power M, Short BE. An investigation into the response of palatally displaced canines to the removal of deciduous canines and an assessment of factors contributing to favourable eruption. Br J Orthod 1993;20:215-23. 16. Chaushu S, Chaushu G, Becker A. The use of panoramic radiographs to localize displaced maxillary canines. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;88:511-6. 17. Marks SC, Schroeder HE, Andreasen JO. Theories and mechanism of tooth eruption. In: Andreasen JO, K€ olsen-Pedersen J, Laskin DM, editors. Textbook and color atlas of tooth impactions. St Louis: Mosby; 1997. p. 20-65. 18. Ericson S, Kurol J. Incisor resorptions due to ectopic maxillary canines imaged by computerized tomography: a comparative study in extracted teeth. Angle Orthod 2000;70:276-83. 19. Ericson S, Bjerklin K, Falahat B. Does the canine dental follicle cause resorption of permanent incisor roots? A computed tomographic study of erupting maxillary canines. Angle Orthod 2002;72:95-104. 20. Lai CS, Bornstein MM, Mock L, Heuberger BM, Dietrich T, Katsaros C. Impacted maxillary canines and root resorptions of neighbouring teeth: a radiographic analysis using cone-beam computed tomography. Eur J Orthod 2013;35:529-38. 21. Falahat B, Ericson S, Mak D'Amico R, Bjerklin K. Incisor root resorption due to ectopic maxillary canines: a long-term radiographic follow-up. Angle Orthod 2008;78:778-85. 22. Strbac GD, Foltin A, Gahleitner A, Bantleon HP, Watzek G, Bernhart T. The prevalence of root resorption of maxillary incisors caused by impacted maxillary canines. Clin Oral Investig 2013;17: 553-64.
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23. Brin I, 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;8:12-6. 24. Dachi SF, Howell FV. A survey of 3874 routine full-mouth radiographs. II. A study of impacted teeth. Oral Surg Oral Med Oral Pathol 1961;14:1165-9. 25. 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;16:9-16. 26. Johnston WD. Treatment of palatally impacted canine teeth. Am J Orthod 1969;56:589-96. 27. Sacerdoti R, Baccetti T. Dentoskeletal features associated with unilateral or bilateral palatal displacement of maxillary canines. Angle Orthod 2004;74:725-32. 28. Becker A, Peck S, Peck L, Kataja M. Palatal canine displacement: guidance theory or anomaly of genetic origin? Angle Orthod 1995;65:95-102. 29. Mucedero M, Ricchiuti MR, Cozza P, Baccetti T. Prevalence rate and dentoskeletal features associated with buccally displaced maxillary canines. Eur J Orthod 2013;35:305-9.
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30. Nordenram A, Stromberg C. Positional variations of the impacted upper canine: a clinical and radiologic study. Oral Surg Oral Med Oral Pathol 1966;22:711-4. 31. Becker A. Orthodontic treatment of impacted teeth. 3rd ed. Oxford, UK: Wiley-Blackwell; 2012. 32. Alqerban A, Jacobs R, Lambrechts P, Loozen G, Willems G. Root resorption of the maxillary lateral incisor caused by impacted canine: a literature review. Clin Oral Investig 2009; 13:247-59. 33. Ericson S, Kurol J. Incisor resorption caused by maxillary cuspids: a radiographic study. Angle Orthod 1987;57:332-46. 34. Rimes RJ, Mitchell CN, Willmot DR. Maxillary incisor resorption in relation to the ectopic canine: a review of 26 patients. Eur J Orthod 1977;19:79-84. 35. Becker A, Zilberman Y, Tzur B. Root length of lateral incisors adjacent to palatally-displaced maxillary cuspids. Angle Orthod 1984; 54:218-25. 36. Kook YA, Park S, Sameshima GT. Peg-shaped and small lateral incisors not at higher risk for root resorption. Am J Orthod Dentofacial Orthop 2003;123:253-8.
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