Three-Dimensional Assessment of the Eruption Path of the Canine in Individuals With Bone-Grafted Alveolar Clefts Using Cone Beam

Computed Tomography
Snehlata Oberoi, D.D.S., Pawandeep Gill, Radhika Chigurupati, D.D.S., M.D., William Y. Hoffman, M.D., David C. Hatcher, D.D.S., M.S.C., M.R.C.D., Karin Vargervik, D.D.S.
Objective: To evaluate the eruption path of the permanent maxillary canine during a 1-year period after secondary alveolar bone grafting and to (1) compare the canine eruption path on the cleft and noncleft side, (2) examine the number of congenially missing lateral incisors and the rate of canine impaction, and (3) examine the relationship between the eruption status of the canine and timing of alveolar bone grafting relative to age and canine root development using cone beam computed tomography (CBCT). Methods: Cone beam computed tomography scans for 17 nonsyndromic unilateral cleft lip and palate (UCLP), and four bilateral cleft lip and palate (BCLP) consecutive cases of alveolar bone grafting surgery were obtained after orthodontic expansion and before alveolar bone grafting and at least 1 year postsurgery on the Hitachi MercuRay CBCT machine. The DICOM files were imported into Dolphin 3D Imaging 10.5 and reoriented for consistency. The X, Y, and Z coordinates were determined for the canine cusp tip and root tip on both the cleft and noncleft sides. The direction of movement of the canine in 1 year was determined. Results: Most canines on both the cleft and noncleft sides moved incisally, facially, and mesially. Twelve percent of the canines on the cleft side appeared to require surgical exposure. Eighty percent of the canines had less than half root development at the time of bone grafting. The amount of root development did not affect the outcome in terms of eruption amount or direction. Conclusions: Most canines on both the cleft and noncleft side moved incisally, facially, and mesially. KEY WORDS: canine eruption, cleft lip and palate, cone beam computed tomography

Orofacial clefts affect 1 in every 500 to 1000 births worldwide (Murray, 2002). In the United States approximately 6800 babies are born with CL/P each year, making it
Dr. Oberoi is Associate Clinical Professor, Center for Craniofacial Anomalies, Department of Orofacial Sciences, School of Dentistry, University of California at San Francisco, San Francisco, California. Ms. Gill is a dental student, University of California at San Francisco, San Francisco, California. Dr. Hoffman is Professor and Chief, Division of Plastic Surgery, Department of Surgery, School of Medicine, University of California San Francisco, San Francisco, California. Dr. Hatcher is in private practice, Roseville, California. Dr. Vargervik is Professor and Director, Center for Craniofacial Anomalies, Department of Orofacial Sciences, School of Dentistry, University of California at San Francisco, San Francisco, California. Supported by the AAO Foundation Faculty Development Award (2007), UC Orthodontic Alumni Foundation and Departmental support from Orofacial Sciences. Presented at the American Association of Orthodontists 108th Annual Session, Denver, 2008 (Rising star presentation). Submitted October 2008; Accepted January 2010. Address correspondence to: Dr. Snehlata Oberoi, S 747, 513 Parnassus Ave, Center for Craniofacial Anomalies, University of California, San Francisco, CA 94143. E-mail sneha.oberoi@ucsf.edu. DOI: 10.1597/08-171 507

the most common birth defect in the United States (CDC, 2006). Secondary alveolar bone grafting has become the gold standard for the treatment of the alveolar defect in individuals with cleft lip, alveolus, and palate (Feichtinger et al., 2007). The utility and success of secondary alveolar bone grafting has been established in the literature (Boyne and Sands, 1972; Bergland et al., 1986a). The timing is defined as early if done just prior to eruption of the central incisor or late when the canine root development is between one fourth to two thirds of its final root length between 9 and 11 years of age (Boyne and Sands, 1972; Lilja et al., 2000; Rosenstein et al., 2003). A successful alveolar bone graft bridges the cleft defect with bone, provides alar base support, facilitates eruption of the permanent tooth adjacent to the cleft, preserves the periodontal health of the adjacent teeth, allows closure of the communication between the oral and nasal cavities, and may provide adequate bone for replacement of a missing lateral incisor with an endosseous implant (Bergland et al., 1986b). Among the several aims of secondary alveolar bone grafting is the formation of a continuous and stable dental

508 Cleft PalateCraniofacial Journal, September 2010, Vol. 47 No. 5

arch that facilitates eruption of the permanent canine into a desired position (Hynes and Earley, 2003). Therefore, one parameter to evaluate success of the bone graft is the eruption status of the permanent canine. Presently, most centers use two-dimensional (2D) plain periapical, occlusal, or panoramic radiographs for assessing alveolar cleft defects before surgery and grafted sites after surgery (Semb et al., 1986; Long et al., 1995; Kindelan et al., 1997). Plain radiographs have several confounding factors, such as image enlargement and distortion, structure overlap, limited identifiable landmarks, and positioning problems, that can adversely affect image quality (Waitzman et al., 1992). More recent advances in diagnostic imaging using cone beam computed tomography (CBCT) allow better imaging of the cleft and three-dimensional (3D) volume analysis (Hamada et al., 2005). Plain radiographs show the approximate postgraft condition of the alveolus and adjacent teeth as compared to dental 3D CT images which clearly show precise 3D morphology of the new alveolar bone and its relationship to the roots of adjacent teeth, as shown by Hamada et al. (2005). Studies on 3D localization of impacted maxillary canines with CBCT has been done in noncleft individuals with findings of 40% to 92% of the impactions being palatal, 8% to 45% being buccal, and lateral incisor resorption occurring in 27% to 66% of cases (Walker et al., 2005; Liu et al., 2008). These studies used linear and angular measurements of the inclination and location of the impacted cuspids at one time point only. Few studies have been done to evaluate the eruption status of the canine in cleft lip and palate individuals at a given time point. To our knowledge no 3D study has been reported on the eruption path of the canine over time. Although studies have found that most canines erupt through the bone grafted site (Turvey et al., 1984; da Silva Filho et al., 2000), the eruption path has not been reported previously (Collins et al., 1998; da Silva Filho et al., 2000). The aim of our study was to evaluate the eruption path of the permanent maxillary canine during a 1-year period after secondary alveolar bone grafting and (1) to compare the canine eruption path on the cleft and noncleft side, (2) to examine the number of congenially missing lateral incisors and the rate of canine impaction, and (3) to examine the relationship between the eruption status of the canine and timing of alveolar bone grafting relative to age and canine root development using CBCT. MATERIALS AND METHODS Subjects The sample for this study consisted of all consecutive nonsyndromic cleft lip and palate subjects from the UCSF Center for Craniofacial Anomalies over a period of 2 years, who underwent secondary alveolar bone grafting as part of

their treatment protocol (IRB/CHR approval # H4460127916-02). The bone graft material was autogenous corticocancellous bone harvested from the anterior iliac crest. The lateral sliding labial flap as described by Boyne and Sands (1972) was the surgical approach for soft tissue closure in both unilateral and bilateral clefts. The subjects consisted of 17 unilateral and four bilateral cleft lip and palate individuals (12 boys, nine girls). Individuals who had been diagnosed with a syndrome associated with the clefting condition or had previous bone grafting were excluded from the study. The average age at alveolar bone graft surgery was 10 years 6 months. The average age at the time of the first scan was 10 years 6 months (SD 5 2 years 8 months). The average age at the time of the second scan was 11 years 9 months (SD 5 2 years 7 months). The average time interval between scans was 13.6 months (SD 5 5.9 months). Methods CBCT scans with 0.4-mm slices were obtained at two time points (at least 1 year apart) on the Hitachi MercuRay CBCT machine (Hitachi Medical Corporation, Tokyo, Japan). The first scans were taken after orthodontic expansion, before alveolar bone grafting and the second scans at least 1 year after alveolar bone grafting. The first step was reorienting the DICOM files using Dolphin 3D Imaging 10.5 (Glendora, CA). The volumetric data were loaded and oriented such that the X, Y, and Z planes were set at internal landmarks and cranial base structures. The sagittal cross-section was used to set the X plane at the SellaNasion (S-N) as a line from the geometric center of sella (S) to the frontonasal suture (N). The coronal view was used to set the Y plane at midsagittal as a line bisecting the clivus in the base of the skull. The axial cross-section was used to set the Z plane as a line bisecting the optic foramina (Fig. 1). After reorienting, the canine cusp tip and a point along the long axis of the developing root were selected on both the cleft and noncleft sides in the volumetric view using the digitizing landmarks tool (Fig. 1). These points were verified in the sagittal, coronal, and axial views (Fig. 1). The X, Y, and Z coordinates of each digitized point were determined by the software and pasted onto an Excel spreadsheet. The direction and amount of movement of the canine were calculated by subtracting the individual X, Y, and Z coordinates in the post scans from the values determined in the pre scans. The vertical growth changes in the skull are very minimal since we used cranial base landmarks. Therefore, there will no significant influence on the eruption measurements of the canine. Statistical Methods SAS Proc MIXED and SAS Proc NLMIXED (SAS Ver 9.1, SAS Institute, Cary, NC) were used to perform the

Oberoi et al., CBCT AND CANINE ERUPTION IN GRAFTED ALVEOLAR CLEFTS 509

FIGURE 1 Reorientation along the coronal, sagittal, and axial planes and landmark identification on CBCT scans.

statistical analyses. Mixed model analyses were used to accommodate the correlations in measurements due to the contribution of two measurements from each of the bilateral patients. Two operators each repeated the method 10 times on the same scans. The average pairwise difference in measurements between raters was found to be 0.51 (SD 5 .26), 0.30 (SD 5 .29), and 1.03 (SD 5 .31) for the X, Y, and Z coordinates, respectively. RESULTS In general, the canines on both the cleft and noncleft sides moved incisally, facially, and mesially as shown on the histograms (Fig. 2A through 2C). Only one canine on the cleft side appeared to move apically 0.9 mm. This is a relative movement due to change to a more mesial inclination. Vertical Movement The canines moved incisally in 24 of the 25 cleft sites. The mean and median incisal movements were 6.8 (SD 5 4.9)

and 5.7 mm with a minimum of 0.4 mm and maximum of 16 mm. The mean and median incisal movements of the noncleft side canines (n 5 17) were 5.9 mm (SD 5 4.7) and 5.0 mm (Tables 1 and 2). Facial-Palatal Movement Facial movement was seen in 20 of the cleft side canines. The mean and median facial movements were 2.5 mm (SD 5 2.13) and 1.8 mm with a minimum of 0.1 mm and maximum of 7.5 mm. Facial movement was recorded in 10 of the noncleft side canines. The mean and median facial movements were 2.5 (SD 5 1.74) and 1.75 mm (Tables 1 and 2). Palatal movement occurred in five of the cleft side canines. The mean and median palatal movements were 2.4 mm (SD 5 1.4) and 3.1 mm with a minimum of 0.4 mm and maximum of 3.9 mm. Palatal movement was recorded in seven of the noncleft side canines. The mean and median palatal movements were 1.2 (SD 5 1.6) and 0.5 mm (Tables 1 and 2).

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TABLE 1

Movement on the Cleft Side

Median (mm) Mean (mm) SD (mm) MinMax (mm)

Direction of Number Movement of Canines

Incisal Apical Mesial Distal Facial Palatal

24 1 22 3 20 5

5.75 0.9 2.8 0.7 1.8 3.1

6.8 0.9 3.25 2.03 2.5 2.42

4.92 0 2.5 2.84 2.14 1.5

0.416 0.69.8 0.15.3 0.17.5 0.43.9

Lateral Movement Mesial movement occurred in 22 of the cleft side canines. The mean and median mesial movements were 3.2 mm (SD 5 2.5) and 2.8 mm with a minimum of 0.6 mm and maximum of 9.8 mm. Mesial movement was recorded in 10 of the noncleft side canines The mean and median mesial movements were 1.6 (SD 5 1.2) and 1.5 mm (Tables 1 and 2). Cleft Versus Noncleft Side Movement in the Unilateral Clefts Most of the distal movement was on the noncleft side. The mean and median distal movements of the cleft side canines (n 5 3) were 2 mm (SD 5 2.8) and 0.7 mm with a minimum of 0.1 mm and maximum of 5.3 mm. The mean and median distal movements of the noncleft side canines (n 5 7) were 3 mm (SD 5 1.6) and 2.6 mm with a minimum of 1.5 mm and maximum of 6.3 mm (Tables 1 and 2). Canine Impaction The estimated percentage of the canines that needed surgical exposure due to impaction was 12% with a bootstrapped 95% confidence interval of 4% to 33%. Congenitally Missing Lateral Incisor Lateral incisors were missing in 88% of the unilateral and 75% of the bilateral clefts. In addition, the unilateral cases were missing 24% of the contralateral lateral incisors. The presence or absence of lateral incisors did not affect vertical eruption. Younger Versus Older Group The younger group (,9 years) consisted of five individuals (23.8%), and the older group (.9 years) had 16 individuals (76.2%). We analyzed canine movements in the mesial or distal directions and canine movements in the facial or
B FIGURE 2 a: Movement amount (mm) of maxillary canine on cleft and noncleft sides in the incisal and apical directions. b: Movement amount (mm) of maxillary canine on cleft and noncleft sides in the facial and lingual directions. c: Movement amount (mm) of maxillary canine on cleft and noncleft side in the mesial and distal directions.

Oberoi et al., CBCT AND CANINE ERUPTION IN GRAFTED ALVEOLAR CLEFTS 511

TABLE 2
Direction of Movement

Movement on the Noncleft Side

Number of Canines Median (mm) Mean (mm) SD (mm) MinMax. (mm)

Incisal Mesial Distal Facial Palatal

17 10 7 10 7

5 1.55 2.6 1.75 0.5

5.95 1.6 3 2.51 1.24

4.73 1.19 1.62 1.74 1.66

0.118.2 0.13.7 1.56.3 0.44.9 0.24.9

palatal directions separately. There was no statistical difference between the older and younger groups in the amount of movement of the canine in the mesial-distal group ( p 5 .39) or in the facial-palatal group ( p 5 .20). Canine Root Development Versus Eruption Eighty percent of canines had root development less than 50%, and 20% had root development greater than 50%. Individuals with root development less than 50% had incisal movement amounts 5.13 mm less than individuals with root development greater than 50% (bootstrapped 95% CI 5 28.32 to 21.9; p 5 .002) DISCUSSION Our study may be the first 3D assessment of the eruption path of the canine during a 1-year period after secondary alveolar bone grafting using CBCT. Most prior studies on canine eruption have been based on 2D assessments using periapical and panoramic radiographs. A few studies have looked at canine position using conventional CT but have not quantified the movement of the canine over time. The optimal timing of bone grafting has been debated for many years, but there now appears to be a consensus that the most successful outcome is seen when secondary alveolar bone grafting is undertaken between the ages of 9 and 11 years and the canine root development is between one half to one third developed (Boyne and Sands, 1972; Turvey et al., 1984; Bergland et al., 1986a). Long et al. (1996) noted several studies suggesting bone graft success to decrease if the procedure is performed after eruption of the permanent canine into the cleft site. Similarly, Tai et al. (2000) cite many previous studies that concluded overall surgical success is improved if bone grafting is performed before canine eruption or when only two thirds to three fourths of the canine root is formed. We found no difference in canine eruption path between the younger (,9 years) and older (.9 years) children and between those who had canine root development above or below 50% in our sample. It is important to note that in none of our patients had the crown of the canine broken through the cortical bone of the alveolar defect. Thus the canine crown was not exposed during the procedure. Spontaneous canine eruption through the bone-grafted site has been reported to vary from 27% to 97% (Turvey et al., 1984; Enemark et al., 1985; Bergland et al., 1986a;

Paulin et al., 1988; da Silva Filho et al., 2000; Hogan et al., 2003). Arch expansion before bone grafting allows for arch development and more room for spontaneous eruption of the canine. In our study, the risk for canine impaction was found in three clefts, 12% as compared to the general population prevalence of 1% to 2%. This is lower than recent studies by Enemark et al. (2001) and Matsui et al. (2005) who reported rates for canine impaction in clefts at 35% and 18.9%, respectively. A recent study by Russell and McLeod (2008) showed a 20-fold impaction anticipated over normal increased risk for canine impaction. They also found that the canine became more vertical with eruption through the bone graft in contrast to Gereltzul et al. (2005) who reported no change in angulation with eruption. In addition they reported a higher impaction rate on the noncleft side as compared with the general population. Presence or absence and size and shape of the adjacent lateral incisor have been known to influence canine eruption (Bishara, 1992; Peck et al., 1994). Individuals with clefts have an increased number of lateral incisor anomalies that may potentially place them at a higher risk for canine impactions. In some studies, the risk for canine impaction was 1.5 to 2 times higher when the lateral incisor was missing or malformed or a supernumerary tooth was present. The study by Gereltzul et al. (2005) showed that the status of the lateral incisor had no effect. In our study, most canines on the cleft side erupted mesially, and most of the lateral incisors were missing. Canine substitution was preferred as the treatment plan whenever possible. In noncleft individuals, the eruption path of the canine has been found to displace toward the occlusal plane, straighten gradually, and then deviate toward a more vertical position (Tai et al., 2000; Gereltzul et al., 2005). In our study, we found that most of the noncleft canines also moved incisally, facially, and mesially. Most of the distal movement was seen on the noncleft side in unilateral clefts. This could be attributed to presence of a lateral incisor on the noncleft side, thereby allowing for a more vertical eruption path. CONCLUSIONS This is the first 3D study using CBCT to assess the eruption of the canine over a 1-year period after secondary alveolar bone grafting. Most canines on both the cleft and noncleft side moved incisally, facially, and mesially. Twelve percent of the canines on the cleft side needed surgical exposure, while the rest erupted spontaneously. The presence or absence of the lateral incisor did not affect the vertical eruption of the canine. The amount of root development did not affect the outcome in terms of canine eruption. Three-dimensional imaging using Dolphin 10.5 provided precise information on the eruption path of the canine through the grafted alveolar cleft. Alveolar bone

512 Cleft PalateCraniofacial Journal, September 2010, Vol. 47 No. 5

grafting after orthodontic expansion and before eruption of the permanent canine crown into the defect allowed a normal path of eruption of the canine, predominantly without impaction, thereby enhancing alveolar bone development and facilitating orthodontic management. REFERENCES
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