Introduction
For patients with complete unilateral cleft lip and palate (CUCLP), secondary alveolar bone grafting (SABG) can be performed before or after the emergence of the cleft side permanent canine (pre-CE and post-CE, respectively). The controversy regarding dental outcomes related to the timing of SABG remains unsettled. The objective of this study was to evaluate dental survival and specific dental outcomes of cleft-adjacent teeth in children with CUCLP who received either pre-CE or post-CE SABG.
Methods
The permanent maxillary canines and the central and lateral incisors of 21 pre-CE and 23 post-CE SABG subjects with nonsyndromic CUCLP and all cleft-related surgeries performed by the same surgeon were analyzed retrospectively. Intraoral radiographs and clinical chart notes were collected at age 7 years, at the time of the SABG, and approximately 4 years after the grafting. Dental survival, spontaneous canine eruption, planned prosthetic replacement, root development, and root resorption were analyzed.
Results
Dental outcomes on the noncleft side were better than those on the cleft side. On the cleft side, dental survival of the cleft-adjacent teeth was not significantly different between the pre-CE and post-CE SABG groups ( P >0.05). Most teeth completed root development after grafting, and the cleft side canine root development in the pre-CE SABG group appeared to accelerate after SABG. Trends showed that the pre-CE SABG group suffered less root resorption (16.28%; post-CE: 22.73%; P >0.05) and received fewer planned prosthetic replacements (14.29%; post-CE: 26.01%; P >0.05) but required a greater number of canine exposures (33.33%; post-CE: 4.55%; P = 0.02).
Conclusions
Pre-CE SABG showed better dental outcomes in patients with CUCLP, with fewer adverse dental outcomes than post-CE SABG.
Highlights
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Pre-CE SABG showed fewer adverse dental outcomes than post-CE SABG.
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Permanent maxillary canine root development accelerated after pre-CE SABG.
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Pre-CE SABG was associated with greater need for surgical canine exposures.
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As differences were small, if pre-CE timing is narrowly missed, post-CE SABG is still recommended.
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Dental outcomes are improved on the noncleft side compared with the cleft side.
Almost 75% of patients with cleft lip and palate (CLP) have cleft involvement of the maxillary alveolar ridge. Deficient alveolar bone at the cleft site impedes normal dental development and eruption and in consequence, adversely influences the long-term survival of the cleft-adjacent permanent maxillary dentition. , Surgical rehabilitation of the alveolar cleft is a common procedure. Currently, a commonly conducted surgical intervention for the repair of alveolar clefts is secondary alveolar bone grafting (SABG), but its optimal timing is controversial.
SABG is typically performed in mixed dentition before the eruption of the cleft side permanent maxillary canine, when its root is one-third to two-thirds developed. , This timing creates a continuous maxillary alveolar ridge that facilitates eruption and survival of the cleft side permanent maxillary canine. , , , SABG can also be performed after canine eruption, but some investigators contend that delaying SABG decreases the survival of cleft-adjacent teeth because of insufficient bone support. , Grafting after canine eruption has also been linked to decreased alveolar bone height, less bone graft uptake, , , and increased risk of external root resorption. A recent systematic review of 3-dimensional radiographic measurement of SABG success reported lower success rates when SABG was performed after canine eruption, but high-quality evidence was reportedly lacking.
Delayed tooth development is common in patients with CLP, both relative to age-matched controls and when comparing the cleft side teeth with the noncleft side teeth. , Very few studies have measured the influence of SABG on tooth development of cleft-adjacent teeth. , , Overall, the results of these studies indicate no adverse effects of SABG on tooth development. , , Only 1 study compared the effects of SABG performed before vs after maxillary canine eruption on the root development of the cleft side permanent maxillary canine. Although the study showed no adverse effects on root development for both SABG groups, it was limited by its small sample size and did not assess the root development of the cleft side central incisor or evaluate the noncleft side. More studies are required to understand the influence of the timing of SABG on the root development of the cleft side and noncleft side permanent maxillary canines and central incisors.
Many studies compared the success of SABG performed before and after canine eruption using various outcomes, , , , , , most commonly, alveolar bone height. Most of these studies included patients treated by multiple surgeons and a wide variety of cleft categories. Because a clinical indication of SABG success includes the eruption and survival of cleft-adjacent teeth, the measurement of dental outcomes is important in the determination of the ideal timing to perform SABG. , , The purpose of this study was to evaluate the dental survival and specific dental outcomes of cleft-adjacent teeth when SABG is performed before and after the initiation of the cleft side permanent maxillary canine emergence from the alveolus (pre-CE and post-CE, respectively) in subjects with complete unilateral cleft lip and palate (CUCLP).
Material and methods
The study design was a retrospective longitudinal assessment conducted at The Hospital for Sick Children in Toronto, Canada. Ethics approval was obtained before initiation. To minimize surgical variation, and for sample homogeneity, subjects were only included if they were born with CUCLP and had all cleft-related surgeries and SABG performed by the same experienced surgeon (D.M.F.). To reduce variation resulting from cleft type and severity, only patients with a diagnosis of CUCLP were included, with all other cleft types, including cleft lip and alveolus, being excluded.
All subjects had been treated with infant orthopedics, initiated soon after birth until primary cheiloplasty, which was completed using Fisher Anatomical Subunit technique at age 3-6 months. This was followed by primary palatoplasty using the hybrid palatoplasty technique at approximately 12 months of age. During the primary surgeries (cheiloplasty and palatoplasty), gingivoperiosteoplasty was not performed. After primary surgery, a residual unrepaired alveolar cleft was present, intended to be addressed by subsequent SABG during the mixed dentition phase of childhood. At The Hospital for Sick Children, the preferred timing for SABG is before the eruption of the cleft side permanent maxillary canine. However, if this timing is missed, SABG may still be performed after canine eruption in many cases. In the included sample, the SABG procedure was performed at either the preferred time or soon after the emergence of the cleft side permanent maxillary canine through the alveolar bone or mucosa. The SABG procedure included division and closure of the nasoalveolar communication and placement of an iliac crest cancellous bone graft by the same surgeon who had performed the primary surgeries. Pre-SABG expansion was performed for patients who presented with asymmetrical arch form, maxillary constriction, posterior crossbites, and/or those who required better access for graft placement.
The subjects had received no other surgical interventions during the period for which study data were collected. Subjects were excluded if they had a craniofacial syndrome, any soft tissue bridging or Simonart’s band, or were missing any records. The collected records included panoramic, maxillary occlusal, and/or periapical radiographs, clinical chart notes, and intraoperative findings at 3 time points: T1, pre-SABG (age, 7 years); T2, at the time of SABG (immediately before or up to 3 months before SABG); and T3, post-SABG (at least 2 years after SABG). Patient classification into SABG groups was performed by an experienced craniofacial orthodontist (S.S.) using T2 radiographs and intraoperative surgical findings recorded at the time of surgery. The stage of eruption of the canine at the time of SABG was classified into 1 of 3 eruption stages ( Fig 1 ): (1) stage 1, bone covering the canine crown; (2) stage 2, canine crown erupted through alveolar bone as seen radiographically, but not visible intraorally (not erupted through the mucosa yet); and (3) stage 3, canine crown erupted through alveolar bone and emerged through the mucosa, visible intraorally.
Stage 1, which represents the stage before canine eruption, was classified as pre-CE SABG. Stages 2 and 3, which represent the stages after the canine has already initiated its eruption through the alveolus, were classified as post-CE SABG. Twenty patients were randomly selected for reclassification after 1 month for intrarater reliability assessment.
Five dental outcomes were measured by 1 investigator (Y.R.V.) who was blinded to the SABG grouping: (1) The dental survival (presence and intraoral retention at T3) of the cleft and noncleft side permanent maxillary central incisors, lateral incisors, and canines was assessed using radiographs and clinical chart notes. Cleft side permanent lateral incisors are very sensitive to developmental disruptions in CUCLP and are commonly congenitally missing or extracted before SABG because of malformations or poor bone support. , , Therefore, the presence of a cleft side lateral incisor or supernumerary tooth in the lateral incisor position was also assessed at T2 (immediately before SABG), to describe the longitudinal lateral incisor survival accurately; (2) planned prosthetic replacement at the cleft and noncleft side permanent lateral incisor site was assessed from T3 radiographs supplemented by the treatment plan noted in the patient chart; (3) spontaneous eruption of the cleft and noncleft side permanent maxillary canines or need for exposure was assessed from clinical chart notes and intraoral radiographs; (4) root development of the cleft and noncleft side permanent maxillary canines and central incisors was assessed using panoramic or periapical radiographs at T1, T2, and T3. Crown and root lengths were measured and a root development score of 0-6 was assigned using the root development rating system described by El Deeb et al ( Table I ), which compares relative crown and root lengths; and (5) the presence of root resorptive defects on the cleft and noncleft side permanent maxillary canines, central incisors, or lateral incisors was determined using T3 radiographs. If root resorption was found, earlier radiographs were also assessed to determine if these defects were present before SABG or if they presented after SABG.
| Score | Description |
|---|---|
| 0 | Complete crown formation, no root formation |
| 1 | Initial root formation |
| 2 | One-fourth root formation (root < crown) |
| 3 | One-half root formation (root = crown) |
| 4 | Three-fourth root formation (root > crown) |
| 5 | Complete root formation, open apex |
| 6 | Complete root formation, closed apex |
Root development and root resorption ratings could be considered to be potentially affected by interpretation; therefore, they were assessed for intrarater reliability. Thirteen radiographs from each time point for root development and 13 T3 radiographs for root resorption were randomly selected and analyzed 1 month after the initial assessment. All other dental outcomes (eg, canine exposure, noted in the chart notes) were dichotomous and not subject to interpretation; therefore, they were not assessed for intrarater reliability.
Statistical analysis
SPSS (version 24; IBM, Chicago, IL) for Windows was used for statistical analysis. Fisher exact test was used for categorical data including sample characteristics (male/female, right/left CUCLP) and dental outcomes (dental survival, prosthetic replacement, canine exposures, and root resorption). An unpaired t test was used for mean age at T1 and T2, and a Mann-Whitney U test was used for mean years post-SABG at T3 and mean age at T3. Odds ratios or mean differences with 95% confidence intervals were calculated for categorical or continuous variables, respectively. Longitudinal root development was assessed using generalized linear mixed modeling, in which correlation was captured with a regression model that accounted for within-individual and between-individual variations. Intrarater reliability was assessed using an unweighted kappa statistic. Statistical significance was set at P <0.05.
Results
Between the years of 2000 and 2017, a total of 350 patients with CLP had SABG procedures performed by the same surgeon (D.M.F.) at The Hospital for Sick Children, Toronto. To allow a minimum follow-up of 2 years after SABG, the final year of inclusion for SABG surgery was 2016. Between January 2009 and August 2016, 64 patients with CUCLP had all cleft-related surgeries (cheiloplasties and palatoplasties) in addition to SABG surgeries performed by the same surgeon (D.M.F.), which were important inclusion criteria for this study to facilitate homogeneity. After applying inclusion and exclusion criteria, 20 patients were excluded (4 patients had been diagnosed with craniofacial syndromes; 16 patients did not have the complete radiographic records required for this study because of orthodontic treatment outside of the hospital). Therefore, a total of 44 subjects with nonsyndromic CUCLP were included in this study. After applying the classification criteria, 21 patients were classified as the pre-CE SABG group and 23 as the post-CE SABG group. The intrarater reliability for patient classification was excellent (k = 0.89; P <0.001). Table II shows the sample characteristics, which were not significantly different between the groups ( P >0.05). Because of both the heterogeneity of the available literature on SABG timing and dental outcomes and the different dental outcomes measured in the current study, our sample size calculation was based on relevant studies reported in the literature. The number of patients in the current study was similar to that of other published studies that looked at dental outcomes in the comparison of SABG performed before and after canine eruption in CUCLP, which indicated that the sample sizes (21 and 23) were sufficient to show a difference at P <0.05.
| Characteristics | Pre-CE (n = 21) | Post-CE (n = 23) | Group difference (pre-CE vs post-CE) |
|---|---|---|---|
| OR (95% CI), P value | |||
| Sex, male/female | 16/5 | 11/12 | 3.49 (0.96, 12.75), P >0.05 |
| CUCLP side, right/left | 7/14 | 9/14 | 0.78 (0.23, 2.67), P >0.05 |
| Mean Difference (95% CI), P value | |||
|---|---|---|---|
| Age at T1, years | 7.7 ± 1.0 (5.0-9.1) | 7.5 ± 0.8 (6.2-9.1) | 0.19 (−0.37, 0.75), P >0.05 |
| Age at T2, ∗ years | 10.0 ± 0.7 (8.5-11.5) | 10.2 ± 0.7 (8.4-11.8) | −0.19 (−0.67, 0.29), P >0.05 |
| Age at T3, years | 13.4 ± 1.3 (11.8-16.3) | 14.3 ± 1.8 (11.3-17.3) | −0.93 (−1.90, 0.04), P >0.05 |
| Post-SABG at T3, years | 4.0 ± 1.5 (2.0-6.9) | 4.1 ± 1.5 (2.0-6.8) | −0.07 (−0.98, 0.84), P >0.05 |
∗ Immediately before or up to a maximum of 3 months before SABG.
In general, dental outcomes were improved on the noncleft side relative to the cleft side for both SABG groups, with some outcomes reaching statistical significance ( Tables III-VII ). In addition, fewer adverse dental outcomes were observed on the cleft side in the pre-CE SABG group compared with the post-CE SABG group. The dental survival of the permanent maxillary central incisor was excellent in both SABG groups (100% survival; P >0.05). Canine survival was also excellent and not significantly different between groups ( P > 0.05; Table III ). Conversely, the dental survival of the cleft side lateral incisor was poor in both SABG groups, with only 1 lateral incisor surviving in the pre-CE SABG group on the cleft side ( Table IV ). This lateral incisor completed root development (stage 6) but presented with cervical external root resorption after SABG. The noncleft side in both groups had a greater number of lateral incisors at T3 ( P <0.001) than the cleft side. In both groups, the cleft side lateral incisor survival was also poor at the time of SABG (pre-CE SABG: congenitally missing = 47.62%, extracted before SABG = 47.62%, present = 4.76%; vs post-CE SABG: congenitally missing = 69.57%, extracted before SABG = 30.43%, present = 0%).
| Groups | Present intraorally | Not present (unerupted at T3/extracted) |
Group comparisons (contrasts) OR (95% CI), P value |
|---|---|---|---|
| CS pre-CE SABG (n = 21) | 19 (90.48%) | 2 (9.52%) | CS pre-CE vs CS post-CE: 0.91 (0.12, 7.07), P >0.05 |
| CS post-CE SABG (n = 23) | 21 (91.30%) | 2 (8.70%) | NCS pre-CE vs NCS post-CE: (−), P >0.05 |
| NCS pre-CE SABG (n = 21) | 21 (100.00%) | 0 | CS pre-CE vs NCS pre-CE: 0.91 (0.79, 1.04), P >0.05 |
| NCS post-CE SABG (n = 22) ∗ | 22 (100.00%) | 0 | CS post-CE vs NCS post-CE: 0.91 (0.81, 1.04), P >0.05 |
∗ Sample size (n = 22) because 1 canine was extracted before T3 as a result of caries (unrelated to SABG).
| Groups | Present intraorally | Extracted/congenitally missing | Group comparisons (contrasts) OR (95% CI), P value |
|---|---|---|---|
| CS pre-CE SABG (n = 21) | 1 (4.76%) | 20 (95.24%) | CS pre-CE vs CS post-CE: 0.95 (0.87,1.05), P >0.05 |
| CS post-CE SABG (n = 23) | 0 | 23 (100.00%) | NCS pre-CE vs NCS post-CE: 0.31 (0.05,1.78), P >0.05 |
| NCS pre-CE SABG (n = 21) | 16 (76.19%) | 5 (23.81%) | CS pre-CE vs NCS pre-CE: 0.02 (0.002, 0.15), P <0.001 ∗ |
| NCS post-CE SABG (n = 23) | 21 (91.30%) | 2 (8.70%) | CS post-CE vs NCS post-CE: 1.00 (0.13, 7.78), P <0.001 ∗ |
| Groups | Planned prosthetic replacement | No planned prosthetic replacement | Group comparisons (contrasts) OR (95% CI), P value |
|---|---|---|---|
| CS pre-CE SABG (n = 21) | 3 (14.29%) | 18 (85.71%) | CS pre-CE vs CS post-CE: 0.47 (0.10, 2.20), P >0.05 |
| CS post-CE SABG (n = 23) | 6 (26.09%) | 17 (73.91%) | NCS pre-CE vs NCS post-CE: (−), P >0.05 |
| NCS pre-CE SABG (n = 21) | 0 | 21 (100.00%) | CS pre-CE vs NCS pre-CE: 0.86 (0.72, 1.02), P >0.05 |
| NCS post-CE SABG (n = 23) | 0 | 23 (100.00%) | CS post-CE vs NCS post-CE: 0.74 (0.58, 0.94), P <0.05 ∗ |
