Introduction
The aims of this study were to investigate the eruption pattern of maxillary permanent canines in the alveolar cleft area after secondary alveolar bone grafting and to assess the risk indicators for canine impaction.
Methods
The sample consisted of 75 patients with unilateral cleft lip and palate who underwent secondary alveolar bone grafting with rhBMP-2 with a mean age of 9.8 years of age at 1 center. A split-mouth study design was used, with the noncleft hemiarch comprising the control group. Panoramic radiographs taken before, immediately after, and 1 year after secondary alveolar bone grafting were used to assess the following parameters in both cleft side (CS) and noncleft side: canine mesiodistal angulation, canine height relative to the occlusal plane, canine mesial displacement, and superimposition with the neighboring maxillary incisors. The frequency of associated dental anomalies was compared between patients with and without CS canine impaction. Data were evaluated using analysis of variance, t tests, Fisher tests, and multiple logistic regression analysis ( P <0.05).
Results
On the CS, maxillary canines were usually more mesially angulated and more distant from the occlusal plane compared with the noncleft side. The prevalences of canine impaction on the CS and noncleft side were 24% and 1.3%, respectively. Maxillary impacted canines on the CS demonstrated increased mesiodistal angulation and height at all time points. No association between CS canine impaction and mesial displacement (sectors) was found. An increased prevalence of lateral incisor agenesis on the CS was observed in the subgroup with canine impaction.
Conclusions
Increased mesial angulation and lateral incisor agenesis on the CS are early risk indicators for maxillary canine impaction in patients with unilateral cleft lip and palate.
Highlights
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Increased mesidiostal inclination increases the risk of canine impaction in patients with unilateral cleft lip and palate (UCLP).
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Maxillary lateral incisor agenesis on the cleft side influences canine impaction.
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Mesial displacement/superimposition could not predict canine impaction in UCLP.
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Canine impaction etiology in the cleft region seems to be mostly environmental.
The prevalence of maxillary canine impaction in noncleft populations varies from 1.7% to 3%. In contrast, patients with cleft lip and palate (CLP) have a frequency of 12% to 35% for maxillary canine impaction after the bone graft on the cleft side (CS).
In patients without oral clefts, the ectopic eruption of the maxillary canines can be diagnosed early during the late mixed dentition using clinical examinations supplemented by panoramic radiographs. Ericson and Kurol suggested that (1) asymmetry on canine bud palpation between 2 sides, (2) inability to palpate the canine, and (3) late eruption of the maxillary lateral incisor or pronounced buccal or labial displacement are clinical signs of maxillary canine eruption disturbance. In the panoramic radiograph, the superimposition of the cusp tip of maxillary canine buds with the roots of the lateral or central incisors is a sensible method to predict canine impaction. This method can identify almost 80% of the canines likely to become impacted.
Canine impaction in noncleft patients is related to a genetic background and is associated with other dental anomalies including tooth agenesis and small teeth. However, factors that can contribute to a higher prevalence of impacted canines in patients with unilateral CLP (UCLP) are still unknown. Some authors have associated impacted canines and the lack of bone in alveolar defects, which can reduce the available space in the jaw and result in canine displacement. Bone graft surgery and timing to repair the cleft could interfere with permanent canine eruption. Currently, studies demonstrated that an increased mesiodistal inclination of the permanent canine after autogenous bone grafting seems to be associated with canine impaction in patients with CLP. Additionally, a positive relationship between tooth agenesis, clefting, and genetic disturbances has been suggested. May impacted canines in patients with UCLP share the same genetic etiology as dental anomalies? Or do canines remain impacted as a consequence of the cleft environment? These questions still have no evidence-based answers, and we still need a reliable method for early detection of canine impaction in patients with CLP.
Considering the benefits of prevention to reduce the burden of care in patients with CLP, we had 2 objectives in this study: (1) to longitudinally assess permanent canine eruption path in the rhBMP-2 grafted alveolar cleft compared with the antimere tooth on the noncleft side, and (2) to evaluate early risk indicators of maxillary canine impaction on the CS including associated dental anomalies.
Material and methods
This retrospective observational study was approved by the institutional ethical committee (protocol 17860713.5.0000.5441) of the University of São Paulo in the Hospital for Rehabilitation of Craniofacial Anomalies. The sample size calculation was based on preliminary studies. For a standard deviation of 14.1° and a minimal intergroup difference of 5° for the canine angle to be detected, a sample of 65 patients was required to provide statistical power of 80% with an alpha of 0.05.
The sample consisted of 75 patients with unilateral complete CLP (51 boys, 24 girls) who underwent secondary alveolar bone grafting with rhBMP-2 at 1 center in Bauru, SP, Brazil. At T1, the subjects were considered in the late mixed dentition when the cleft side canine root development was between one fourth and two thirds of its final length before the secondary alveolar bone graft. The inclusion criteria were (1) consecutive patients whose secondary alveolar bone grafting was performed between 2009 and 2014 with rhBMP2 (INFUSE; Memphis, Tenn); and (2) a complete set of panoramic radiographs before (T1), from 3 to 12 months after secondary alveolar bone grafting (T2), and more than 13 months after secondary alveolar bone grafting (T3). Exclusion criteria were 1 or 2 maxillary canines erupted at T1, associated craniofacial syndromes, and radiographs with poor image quality. The subjects had an initial mean age of 9.8 years (SD, 0.7), and the mean observation time was an average of 33 months. Ninety percent of the sample underwent rapid maxillary expansion before secondary alveolar bone grafting. At T2, no patient had orthodontic treatment. At T3, 28% of the patients received a partial fixed appliance to correct the rotation of the central incisor adjacent to the cleft while waiting for canine eruption on the CS. The CS group comprised maxillary permanent canines on the CS. The noncleft side (NCS) group comprised the contralateral maxillary permanent canines on the NCS.
Digital panoramic radiographs taken at T1, T2, and T3 were used. Software (version10.5; Dolphin Imaging, Chatsworth, Calif) was used to measure the following parameters on all radiographs: mesiodistal angulation and height of the maxillary canine buds, horizontal displacement of the maxillary canine bud relative to the neighboring incisors, tooth agenesis, transpositions, and premolar distoangulation. The mesiodistal angulation of the canine bud was measured using the angle between the long axis of the maxillary canine and the bicondylar line ( Fig 1 ). The canine bud height was measured from the cusp tip to the occlusal plane, perpendicularly ( Fig 1 ).
The modified method of Ericson and Kurol and Lindauer et al was used for evaluating the mesiodistal canine germ displacement relative to the roots of central and lateral incisors on the CS and NCS, respectively ( Fig 2 ).
Tooth agenesis (excluding third molars), tooth transpositions, and distoangulation of second premolars were assessed by direct observation of each panoramic radiograph. Distoangulation of the mandibular second premolar was measured according to the method of Shalish et al.
Canines were considered impacted at T3 based on the clinical notes of surgical access for traction in the files.
Statistical analyses
Two examiners performed the measurements twice with an interval of 30 days. Intraexaminer and interexaminer reliabilities were calculated using the intraclass correlation coefficient (ICC) and weighted kappa statistic. The average and standard deviation of the assessed quantitative parameters were calculated. Interphase differences for maxillary canine position were evaluated using analysis of variance and Tukey tests. Prevalences of impaction and dental anomalies were calculated in percentages. Comparisons of canine positional parameters between the CS and NCS, and between impaction and nonimpaction patients, were performed using paired and independent t tests, respectively. Comparisons for the frequency of associated dental anomalies between the CS impaction and nonimpaction subgroups were performed using the Fisher exact test. Comparisons of the mesiodistal displacement of canines (sectors) between the CS and NCS and between the CS impacted and nonimpacted subgroups were performed using the Fisher exact test. Multiple logistic regression analysis was used to assess the risk indicators at T1 for CS canine impaction. Specificity and sensitivity of a critical mesiodistal angulation of CS canine buds were calculated using receiver operating characteristic curves. The significance level was set at 0.05. Statistical analysis was conducted using software for Windows (version 16.0; SPSS, Chicago, Ill).
Results
The intraexaminer and interexaminer reliabilities for angulation and height in the CS and NCS ranged from ICC 0.93 to 0.97. Intraexaminer and interexaminer reliabilities for sector scores varied from ICC 0.64 to 0.83.
From T1 to T3, the height and mesiodistal angulation of the maxillary canines decreased on both the CS and NCS ( Table I ). At the 3 times, the CS had maxillary canines that were more angulated and more distant from the occlusal plane ( Table II ).
| T1 | T2 | T3 | P | ||||
|---|---|---|---|---|---|---|---|
| Mean | SD | Mean | SD | Mean | SD | ||
| Cleft side | |||||||
| Angulation (α)° | 67.85 a | 14.23 | 65.62 a | 15.47 | 74.42 b | 16.09 | <0.001 |
| Height (mm) | −11.58 a | 5.30 | −7.05 b | 6.55 | −1.67 c | 7.51 | <0.001 |
| Noncleft side | |||||||
| Angulation (α)° | 79.48 a | 12.15 | 82.63 b | 11.59 | 86.62 c | 8.33 | <0.001 |
| Height (mm) | −7.74 a | 6.37 | −2.63 b | 6.84 | 1.92 c | 5.89 | <0.001 |
| Cleft side | Noncleft side | Difference | P | |||
|---|---|---|---|---|---|---|
| Mean | SD | Mean | SD | |||
| Angulation (α)° T1 | 67.85 | 14.23 | 79.48 | 12.15 | −11.63 | <0.001 |
| Height T1 (mm) | −11.58 | 5.30 | −7.74 | 6.37 | −3.84 | <0.001 |
| Angulation (α)° T2 | 65.62 | 15.47 | 82.63 | 11.59 | −17.01 | <0.001 |
| Height T2 (mm) | −7.05 | 6.55 | −2.64 | 6.84 | −4.42 | <0.001 |
| Angulation (α)° T3 | 74.42 | 16.09 | 86.62 | 8.33 | −12.20 | <0.001 |
| Height T3 (mm) | −1.67 | 7.51 | 1.92 | 5.89 | −3.59 | <0.001 |
In the CS, 18 (24%) patients had impacted canines, and 57 had fully erupted canines (76%) at T3. On the NCS, only 1 canine (1.3%) was impacted, and 74 (98.7%) were erupted at T3.
Table III shows that patients whose maxillary impacted canines became impacted on the CS had increased mesiodistal angulation and height before the bone graft stage (T1). CS canine impaction was more likely to occur when alpha was less than 68° at T1, with specificity of 59.65 and sensitivity of 88.9.
| Impacted canines | Nonimpacted canines | P | |||
|---|---|---|---|---|---|
| Mean | SD | Mean | SD | ||
| Angulation (α)° T1 | 56.98 | 14.33 | 71.28 | 12.45 | <0.001 |
| Height T1 (mm) | −14.46 | 4.90 | −10.66 | 5.12 | <0.01 |
| Angulation (α)° T2 | 53.22 | 14.60 | 69.53 | 13.66 | <0.001 |
| Height T2 (mm) | −11.46 | 6.20 | −5.65 | 6.06 | <0.01 |
| Angulation (α)° T3 | 62.24 | 18.46 | 78.26 | 13.26 | <0.001 |
| Height T3 (mm) | −7.10 | 9.11 | 0.04 | 6.06 | <0.001 |
The mesiodistal position of the canine bud on the CS (sectors) was not a discriminant factor between canines that would or would not be eventually impacted ( Table IV ).
