Objective

To assess differences in root development between the cleft side (CS) and noncleft side (NCS) for permanent maxillary central incisor and canine longitudinally in patients with nonsyndromic complete unilateral cleft lip and palate (cUCLP) who received secondary alveolar bone grafting (SABG) and to evaluate the effects of SABG on the acceleration of root development of these teeth.

Materials and Methods

Permanent maxillary central incisors and canines of 44 subjects with nonsyndromic cUCLP who had all their cleft-related surgeries performed by the same surgeon were analyzed retrospectively from chart notes and radiographs. Panoramic and periapical radiographs at time point 1 (T1) (age, 7.55 years), at SABG (time point 2 [T2], 10.13 years), and a minimum of 2 years after SABG were studied. Root development rating scores on the NCS and CS were compared using paired t-tests and analyses of proportions.

Results

Mean root development score differences (NCS − CS) for canines and central incisors were greatest at T2 but diminished at time point 3 (T3). A larger proportion of teeth on the CS trailed the teeth on the NCS by at least 1 point at T2 than at T1 or T3, with the smallest proportion being observed at T3. The change in root development scores from T1 to T2 and from T2 to T3 showed relative CS acceleration from T2 to T3, indicating a catch-up of root development of cleft-adjacent teeth after SABG.

Conclusions

Root development of cleft-adjacent central incisors and canines is slow in comparison with their noncleft analogs. Root development of these teeth accelerates following SABG.

An increased frequency of dental developmental anomalies has been reported in patients with cleft lip and palate (CLP), with these differences being more pronounced in the immediate cleft vicinity.1  One specific dental alteration that has been reported in patients with CLP is a delay in root development, both relative to age-matched controls2–5  and when comparing the cleft side (CS) to the contralateral noncleft side (NCS).2,3,6–12  Patients with CLP are three to four times more likely to have a difference of at least one stage of root and/or crown development between the CS and the NCS in comparison to contralateral sides in control populations.9,13,14 

The presence of a cleft of the maxillary alveolar ridge itself has also been found to inhibit normal dental development.15,16  In patients with complete unilateral cleft lip and palate (cUCLP), a missing lingual cortical plate in the cleft site has been hypothesized to delay root development due to the lack of space for the root to develop.10,17  Secondary alveolar bone grafting (SABG) in the mixed dentition is a commonly performed surgical procedure to repair clefts of the maxillary alveolus and is usually undertaken prior to the eruption of the CS permanent maxillary canine. While the continuity of the alveolar ridge provided by SABG may have a positive effect on root development, surgical treatment may impede root development due to a decreased blood supply and scar tissue formation.11 

A few studies have investigated the influence of SABG on root development (Table 1).6,10,18–22  An acceleration of root development of the permanent maxillary canine following SABG performed before canine eruption has been previously reported without any adverse effects on root development.10,20  Other studies have also reported minimal adverse effects of SABG on tooth development, but these studies were limited by subjects not always being separated based on cleft severity,6,21,22  surgical treatment being provided by more than one surgeon,21  or a lack of clarity as to whether the included patients were treated by more than one surgeon.6,10,18,19,22  As the experience of the surgeon can affect the outcomes of SABG,23  and root development can be influenced by cleft severity,13  these factors ideally should be controlled for. Additionally, while all studies measured root development at more than one time point, a longitudinal assessment of root development from a time prior to SABG, to the time of SABG, to a time after SABG has not been reported by most. Most studies also measured only the permanent maxillary canine6,18,19,21,22  and not the maxillary central incisor (Table 1).

Table 1.

Published Literature on the Influence of SABG on the Root Development of Permanent Maxillary Teeth in Patients with UCLPa

Published Literature on the Influence of SABG on the Root Development of Permanent Maxillary Teeth in Patients with UCLPa
Published Literature on the Influence of SABG on the Root Development of Permanent Maxillary Teeth in Patients with UCLPa

To better understand the longitudinal effects of SABG on the root development of cleft-adjacent teeth, the objectives of this study were (1) to determine the root development differences between cleft-adjacent teeth on the CS and their analogs on the NCS over time in patients with nonsyndromic cUCLP who received SABG by the same surgeon and (2) to explore the potential acceleration of root development following SABG.

A retrospective longitudinal assessment of root development in patients with nonsyndromic cUCLP was performed at The Hospital for Sick Children in Toronto, Canada. The study design was reviewed and approved by the research ethics board of The Hospital for Sick Children and the University of Toronto prior to study initiation. The management of patients with cUCLP from birth up to and including SABG surgery followed the same standardized protocol. All subjects had been treated with infant orthopedics, initiated soon after birth until primary cheiloplasty, which was undertaken at the age of 3–6 months. This was followed by primary palatoplasty at approximately 12 months of age. Gingivoperiosteoplasty was not performed. After primary surgery, a residual unrepaired alveolar cleft was present, which was to be reconstructed by subsequent SABG in the mixed dentition. Pre-SABG expansion was performed for patients who presented with maxillary constriction, posterior crossbite, or asymmetrical arch form and/or for those who required better access for graft placement. SABG was performed either prior to or soon after the emergence of the CS permanent maxillary canine through the alveolar bone or mucosa, with the former being the preferred timing when possible.

To ensure sample homogeneity and to reduce surgical variation, patient inclusion criteria included only patients with cUCLP who had all cleft-related surgeries and SABG performed by the same experienced surgeon (Dr Fisher), had received no other surgical procedures during the observation period, and had suitable radiographic records to visualize root development of the maxillary central incisors and canines on the CS and NCS. Patients with craniofacial syndromes, missing radiographic records, or poor visualization of the teeth on radiographs to allow determination of their root development status and those with Simonart’s band or soft tissue bridging were excluded.

Panoramic or periapical radiographs were collected and analyzed at three time points: time point 1 (T1), pre-SABG (mean age, 7.55 years); T2, at the time of SABG (immediately before or up to 3 months before SABG; mean age, 10.13 years); and T3, post-SABG (at least 2 years after SABG; mean age, 14.19 years). The longitudinal root development of the CS and NCS permanent maxillary canines and central incisors was analyzed from the radiographs using the rating system of El Deeb et al.6  (Table 2; Figure 1), which compares relative root lengths and crown heights. All root development scoring was performed by the same investigator (Dr Vandersluis-Solomon). As root development can be affected by interpretation, intrarater reliability was assessed through the random selection and analysis of 13 radiographs at each time point 1 month after the initial assessment.

Figure 1.

Crown height and root length measurements for root development rating scores. The long axis of the tooth (white dashed vertical line) and incisal, cervical, and apical lines (white solid horizontal lines) are drawn. Relative to tooth width, midpoints of the incisal, cervical, and apical lines are marked (white circles). Crown height (CH) is the vertical distance from the midpoint of the incisal line to the midpoint of the cervical line. Root length (RL) is the vertical distance from the midpoint of the apical line to the midpoint of the cervical line. CH and RL are compared to determine the root development rating score.

Figure 1.

Crown height and root length measurements for root development rating scores. The long axis of the tooth (white dashed vertical line) and incisal, cervical, and apical lines (white solid horizontal lines) are drawn. Relative to tooth width, midpoints of the incisal, cervical, and apical lines are marked (white circles). Crown height (CH) is the vertical distance from the midpoint of the incisal line to the midpoint of the cervical line. Root length (RL) is the vertical distance from the midpoint of the apical line to the midpoint of the cervical line. CH and RL are compared to determine the root development rating score.

Close modal
Table 2.

Root Development Rating System Based on Relative Crown and Root Lengths (from El Deeb et al.6 )

Root Development Rating System Based on Relative Crown and Root Lengths (from El Deeb et al.6)
Root Development Rating System Based on Relative Crown and Root Lengths (from El Deeb et al.6)

Statistical analysis included descriptive statistics, paired t-tests, and analyses of proportions. The Wilcoxon signed-rank test was used to determine if the differences in the root development scores were significant at the respective time points. Regression modeling of the CS and NCS permanent maxillary central incisor and canine root development scores as a function of age was also undertaken.

After applying all inclusion and exclusion criteria, a total of 44 subjects with cUCLP who had all cleft-related and SABG surgeries performed by the same surgeon were selected. This sample size was similar to those of other published studies that looked at the effects of SABG on root development in cUCLP (Table 1). Sample characteristics are shown in Table 3. The intrarater reliability for root development scoring was excellent (k = 0.85; P < .001). Root development of the CS and NCS permanent maxillary central incisors and canines was not adversely affected by SABG as all teeth reached at least stage 4 of root development, and most reached stage 5 or 6, at T3.

Table 3.

Characteristics of the Included Sample of Patientsa

Characteristics of the Included Sample of Patientsa
Characteristics of the Included Sample of Patientsa

For both the maxillary central incisor and the canine, the root development of the CS tooth was delayed relative to the NCS tooth, with the greatest difference being seen at T2 (Tables 4 and 5; Figures 2 and 3). A larger proportion of teeth on the CS trailed those on the NCS by at least 1 point at T2 than at T1 or T3, with the smallest proportion being seen at T3 (Figures 4 and 5). Regression modeling of the CS and NCS permanent maxillary central incisor and canine root development scores as a function of age20  revealed that the average root development score differences for the canine and the central incisor were the greatest at T2 but diminished at T3 (Figures 6 and 7). An examination of the slopes of the graphs revealed that the greatest acceleration of root development for the maxillary central incisors generally occurred between T1 and T2. Examination of the slopes of the graphs of the maxillary central incisors and canines on the CS and NCS from T1 to T2 and from T2 to T3 revealed a relative CS acceleration from T2 to T3, indicating a catch-up of root development of cleft-adjacent teeth after SABG (Figures 6 and 7).

Figure 2.

Root development scores of the maxillary central incisor observed at different time points. NCS indicates noncleft side; CS, cleft side; T1, time point 1; T2, time point 2; and T3, time point 3.

Figure 2.

Root development scores of the maxillary central incisor observed at different time points. NCS indicates noncleft side; CS, cleft side; T1, time point 1; T2, time point 2; and T3, time point 3.

Close modal
Figure 3.

Root development scores of the maxillary canine observed at different time points. NCS indicates noncleft side; CS, cleft side; T1, time point 1; T2, time point 2; and T3, time point 3.

Figure 3.

Root development scores of the maxillary canine observed at different time points. NCS indicates noncleft side; CS, cleft side; T1, time point 1; T2, time point 2; and T3, time point 3.

Close modal
Figure 4.

Proportion of maxillary central incisors at each time point with a difference in the root development score of at least 1 between the CS and NCS or no difference. The root development score difference was calculated as NCS − CS for all time points, where >/= d = 1 indicates that the NCS score is higher by at least 1, </= d = −1 indicates that the CS score is higher by at least 1, and d = 0 indicates no difference between the NCS and CS scores. T1 indicates time point 1; T2, time point 2; and T3, time point 3.

Figure 4.

Proportion of maxillary central incisors at each time point with a difference in the root development score of at least 1 between the CS and NCS or no difference. The root development score difference was calculated as NCS − CS for all time points, where >/= d = 1 indicates that the NCS score is higher by at least 1, </= d = −1 indicates that the CS score is higher by at least 1, and d = 0 indicates no difference between the NCS and CS scores. T1 indicates time point 1; T2, time point 2; and T3, time point 3.

Close modal
Figure 5.

Proportion of maxillary canines at each time point with a difference in the root development score of at least 1 between the CS and NCS or no difference. The root development score difference was calculated as NCS − CS for all time points, where >/= d = 1 indicates that the NCS score is higher by at least 1, </= d = −1 indicates that the CS score is higher by at least 1, and d = 0 indicates no difference between the NCS and CS scores. T1 indicates time point 1; T2, time point 2; and T3, time point 3.

Figure 5.

Proportion of maxillary canines at each time point with a difference in the root development score of at least 1 between the CS and NCS or no difference. The root development score difference was calculated as NCS − CS for all time points, where >/= d = 1 indicates that the NCS score is higher by at least 1, </= d = −1 indicates that the CS score is higher by at least 1, and d = 0 indicates no difference between the NCS and CS scores. T1 indicates time point 1; T2, time point 2; and T3, time point 3.

Close modal
Figure 6.

Regression modeling of the cleft and noncleft permanent maxillary central incisor root development scores as a function of age. A local regression line was fitted for each group to depict the average root development over time (shown for ages 6 years to 16 years). Solid line, CS; Dashed line, NCS.

Figure 6.

Regression modeling of the cleft and noncleft permanent maxillary central incisor root development scores as a function of age. A local regression line was fitted for each group to depict the average root development over time (shown for ages 6 years to 16 years). Solid line, CS; Dashed line, NCS.

Close modal
Figure 7.

Regression modeling of the cleft and noncleft permanent maxillary canine root development scores as a function of age. A local regression line was fitted for each group to depict the average root development over time (shown for ages 6 years to 16 years). Solid line, CS; Dashed line, NCS.

Figure 7.

Regression modeling of the cleft and noncleft permanent maxillary canine root development scores as a function of age. A local regression line was fitted for each group to depict the average root development over time (shown for ages 6 years to 16 years). Solid line, CS; Dashed line, NCS.

Close modal
Table 4.

Comparison of Mean CS and NCS Root Development Scores of the Maxillary Central Incisors and Canines at the Three Time Pointsa

Comparison of Mean CS and NCS Root Development Scores of the Maxillary Central Incisors and Canines at the Three Time Pointsa
Comparison of Mean CS and NCS Root Development Scores of the Maxillary Central Incisors and Canines at the Three Time Pointsa
Table 5.

Distribution of Root Development Scores of NCS and CS Maxillary Central Incisors and Canines Observed at Each Time Pointa

Distribution of Root Development Scores of NCS and CS Maxillary Central Incisors and Canines Observed at Each Time Pointa
Distribution of Root Development Scores of NCS and CS Maxillary Central Incisors and Canines Observed at Each Time Pointa

Cleft-adjacent teeth have more frequent agenesis, tooth shape and size variations, eruption delays,1,3,7,8,24–27  poor periodontal support,28–31  and caries risk.31,32  With a high frequency of agenesis of maxillary lateral incisors on the CS, the maxillary central incisors and canines are frequently cleft-adjacent teeth, and clinicians need to observe differences in their shape, size, and development compared with their contralateral analogs, especially when planning and executing the reconstruction of the alveolar cleft by SABG, orthodontic correction of the dentition in this area, and/or restorative treatment for esthetics and long-term health and function.

The literature regarding the root development of cleft-adjacent teeth following SABG in UCLP is equivocal. Some studies reported a delay in maxillary canine root development on the CS that showed an acceleration after SABG,10,18,20–22  consistent with the findings of this investigation. Others found no significant differences.6,19  Regarding the maxillary central incisors, some reports described a delay in root development at the time of SABG,20  while others did not.10  In this investigation, delayed root development was seen more frequently on the CS for both the maxillary central incisors and maxillary canines. Results of t-tests and Wilcoxon signed-rank tests showed significantly lower root development scores (P < .05) at T2 for the CS central incisors and at all three time points for the CS canines (Table 3; Figures 2 through 5). However, a catch-up or acceleration was evident, especially in the CS canines, roughly around and after the age of 10 years, corresponding to T2 to T3 (Figures 6 and 7), indicating that there was likely a favorable effect of SABG on the root development of the CS maxillary canine with the provision of mesenchymal matrix and bone volume at the cleft site.

While this was a retrospective longitudinal study using radiographs that had been acquired to support clinical decision-making and follow-up, all cleft surgeries and SABG were conducted by the same experienced plastic surgeon using the same standardized technique. This improved sample homogeneity regarding the surgical aspects of treatment that all patients in the sample received. The findings of this study clarified that the development of the cleft-adjacent teeth was not adversely affected by SABG. The provision of the alveolar bone graft soon after T2 allowed cleft-adjacent teeth that were slower in root development to catch up with their contralateral analogs. This supports the recommendation of providing SABG to patients with cUCLP from the standpoint of promoting the root development of the cleft-adjacent teeth. Ethical constraints precluded the possibility of having a control group that would not have had SABG, and there was no equivalent sample that had longitudinal radiographs at similar ages as the included study patients but had not been provided with bone grafts. This limits the possibility of concluding that the catch-up in root development seen in the CS teeth after SABG would not have happened or would have happened at a different rate without SABG.

Three-dimensional (3D) and cone-beam computed tomography (CBCT) images at various time points were not available due to radiation exposure and costs. Future studies could incorporate 3D imaging when available to better understand any aspects of the grafting process that may enhance or affect root development. While statistically significant and frequent, the mean magnitude of the differences in the root development scores was modest. This implies that clinicians should observe each patient’s root development on the CS and NCS carefully for alveolar bone grafting.

  • Root development of cleft-adjacent central incisors and canines is slow in comparison to their noncleft analogs.

  • Root development of these teeth accelerates following SABG.

The authors thank the Department of Dentistry, The Hospital for Sick Children, Toronto, for assistance in data collection.

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Author notes

a

 Staff Orthodontist, Holland Bloorview Kids Rehabilitation Hospital; and Instructor, Orthodontics, Faculty of Dentistry, University of Toronto, Toronto, Canada.

b

 Professor and Director, Graduate Orthodontics, Faculty of Dentistry, University of Toronto; and Staff Orthodontist, Department of Dentistry, The Hospital for Sick Children, Toronto, Canada.

c

 Medical Director, Cleft Lip and Palate Program, The Hospital for Sick Children, Toronto; and Professor, Department of Surgery, University of Toronto, Toronto, Canada.

d

 Director of Orthodontics, Department of Dentistry, The Hospital for Sick Children, Toronto, Canada.

e

 Associate Professor Emeritus, Faculty of Dentistry, University of Toronto, Toronto, Canada.

f

 Professor and Head, Division of Biostatistics, Dalla Lana School of Public Health, University of Toronto, Toronto, Canada.

The first two authors contributed equally to this work.

Parts of this research were presented at the 123rd Annual Session of the American Association of Orthodontists, Chicago, IL, April 2023.