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DOI: 10.1055/s-0041-1723070
Effectiveness of Secondary Alveolar Bone Graft on Canine Eruption: Systematic Review
- Abstract
- Introduction
- Materials and Methods
- Results
- Discussion
- Conclusions
- References
Abstract
There are controversies related to the effects of bone grafts on tooth eruption and impaction in patients with cleft lip and palate. The aim of this systematic review was to evaluate the effectiveness of bone grafting on eruption of canines in patients with unilateral cleft lip and palate (UCLP). An electronic search was conducted in six electronic databases and gray literature, without limitations on year of publication or language. The primary outcome was the increase in rate of canine eruption; the secondary outcomes were success of the bone graft, canine impaction due to agenesis of the lateral incisor, and effect of orthodontic treatment before and after bone grafting. The risk of bias was analyzed by means of the tool Cochrane risk of bias in nonrandomized controlled trials (NRCTs) of interventions (ROBINS-I). The certainty of the evidence was assessed for outcomes reported through a narrative synthesis using grading of recommendations, assessment, development and evaluation (GRADE) approach. Four NRCTs were included, with a total of 360 patients, 283 UCLP and 77 bilateral cleft lip and palate (BCLP). The studies reported association between the increase in the rate of tooth eruption and bone graft with very low certainty of evidence, and greater experience of surgical success, with low certainty of evidence. The majority of the studies found an association between increase in the rate of canine impaction and agenesis of the lateral incisor, with very low certainty of evidence. There was very low certainty of the efficacy of secondary alveolar bone grafting for increasing the rates of eruption and reducing impaction of the maxillary canine.
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Introduction
Cleft lip with or without cleft palate and cleft palate are common craniofacial deformities in human beings.[1] Patients with clefts involving the palate generally need bone grafts at different stages of life, in order to re-establish the growth and development of the face and allow the evolution of normal occlusion, [2] especially the canines commonly involved in the morphogenesis of cleft palate.[3]
Among these grafts, the primary type is used before patients complete 1 year of age; the early secondary type is performed before eruption of the permanent canine, and the late secondary, after eruption of the permanent canine.[3] [4] Successful bone grafting has been related to the patient’s age at the time of surgery, gender, stage of eruption of permanent canine adjacent to the cleft, size of cleft, development of postoperative infection, and orthodontic treatment.[2] [5] [6]
Pre and postsurgery orthodontic treatment may play an important role in allowing space in the dental arch for the requirements of the graft and for suiting the teeth in the rehabilitation of patients with clefts.[2] [7] [8] Some studies [9] [10] have reported that secondary bone grafting may increase the intraosseous retention of the maxillary canines, while others [11] [12] have demonstrated that the bone graft works as a guide for the eruption of these teeth.[3] [7] [13] [14]
In conjunction, the literature has shown controversies in relation to the real effects of bone grafting, and its influence on eruption of the canine in adolescent patients with clefts.[3] [7] [11] [14] In view of the absence of systematic reviews about the topic up to now, the aim of the authors of this review was to evaluate the body of scientific evidence of the efficacy of secondary alveolar bone grafting on eruption of the permanent canine in patients with clefts.
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Materials and Methods
Focus Question
This systematic review was conducted in order to answer the following clinical question: Is there any scientific evidence of the efficacy of secondary alveolar bone graft surgery has in patients with unilateral clefts for increasing the rate of eruption of the maxillary canine in the cleft area when compared with the control or to patients who were not submitted to surgery? The population, intervention, control, and outcomes (PICO) question and eligibility criteria are detailed in [Table 1].
This systematic review was conducted in accordance with the items of reference for the evaluation of articles in systematic reviews and meta-analysis (preferred reporting items for systematic review and meta-analysis [PRISMA]).[15]
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Search Strategy
An electronic search was conducted in the following databases up until November 2020, without limitation on year of publication or language: PubMed (Medline), Scopus, Web of Science, Medline Complete (EBSCO), Cochrane (Database for Systematic Review, CENTRAL, and Protocols), and gray literature through Trials Central and Clinical Trials. A manual search was conducted in specific periodicals of the area (The Cleft Palate-Craniofacial Journal, Plastic and Reconstructive Surgery) and in the list of references of the articles selected.[15] [16] The search strategies are described in [Table 2].
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Eligibility Criteria of the Articles
Two researchers (R.G.B. and R.L.S.) independently selected the abstracts, titles and complete texts, according to the eligibility criteria ([Table 1]). Discrepancies were decided by discussion and consensus.[17] In the event of divergences between the two evaluators, who could not reach consensus, a third evaluator (S.S.N.) was consulted.
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Quality and Risk of Bias Assessment
Two independent reviewers evaluated the risk of bias of the studies included by using the Cochrane risk of bias in nonrandomized controlled trials (NRCTs) of interventions (ROBINS-I) guidelines.[18]
The domains evaluated by ROBINS-I were: (1) bias due to a confusion; (2) bias in selection of the study participants; (3) bias in classification of the interventions; (4) bias due to deviations from the intended intervention; (5) bias due to lack of data; (6) bias in measurement of the results; (7) bias in selection of the result reported. The general risk of bias of the individual studies was classified as being low (if all the domains were considered to have low risk of bias), moderate (if one or more domains showed moderate risk of bias), serious (if one or more domains showed serious risk of bias), or critical (if one or more domains showed critical risk of bias).
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Data Extraction and Data Analysis
Two independent reviewers extracted data. Disagreements were solved by discussion until a consensus was reached. The primary outcome was increase in the rate of canine eruption. The secondary outcomes were success of bone graft, canine impaction due to agenesis of the lateral incisor, and effect of orthodontic treatment before and after bone grafting.
The was a high level of heterogeneity in data reported by studies, thus it was not possible to pool data for a meta-analysis. A narrative synthesis was planned instead. For reporting the outcomes, a summary of findings (SoF) table was built for each outcome according to grading of recommendations, assessment, development and evaluation (GRADE) pro. We followed the GRADE approach when using ROBINS-I to assess the certainty of the evidence for narrative synthesis.[19] [20] Using ROBINS-I, the certainty of the evidence began with high, and it could be further rated up by magnitude of the effect, dose response, and effect of residual confounders.[20]
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Results
Selection of Studies
After triage of the titles and abstracts of 750 articles, 66 potentially eligible articles were selected for full text analysis; of these, 04 NRCTs.[3] [7] [13] [14] were included ([Fig. 1]). RCTs were not found for the addressed criteria. The characteristics of studies are described in [Table 3] and the outcomes in [Table 4].
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Characteristics of Studies
The studies evaluated a total of 360 patients, of whom 283 patients had unilateral cleft lip and palate (UCLP) and 77 had bilateral cleft lip and palate (BCLP), with mean age ranging between 7 and 13.7 years. The studies were conducted between 2007 and 2018 in Canada,[3] Brazil,[7] Italy,[13] and Sweden.[14]
All the studies[3] [7] [13] [14] evaluated the position of the vertical angulation of the canine, one[13] study evaluated the long axis of the canine in relation to the occlusal plane, two[3] [14] evaluated it in relation to the median sagittal plane, and the other,[7] in relation to the bicondylar line. The lateral position of the canine in relation to the lateral incisor was evaluated by only one[3] study, and its height, in relation to the occlusal plane by the other study.[7]
As control, two[3] [13] studies made paired evaluations of patients with BCLP, one[13] study used the analysis of Bergland for the graft, and both[3] [13] used predefined angulation for the canine, and the split mouth system for the patients with UCLP.[3] [13]Two other studies[7] [14] used the split mouth system for all the patients with UCLP.
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Risk of Bias
All[3] [7] [13] [14] the studies showed serious risk of bias due to confounding factors, and two [13] [14] studies had serious risk of bias due to missing data and bias in selection of the result reported. All [3] [7] [13] [14] the studies had critical risk of bias due to measurement of outcomes. The overall bias of studies3,7,13,14 was of critical risk ([Fig. 2]).
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Results of Studies Included
Increased Rate of Canine Eruption
The SoF in [Table 5] describes the outcomes and the certainty of the evidence using GRADE approach for narrative synthesis. All the studies[3] [7] [13] [14] reported improvement in angulation of the canine after bone grafting, which favored canine eruption ([Tables 3]-[4]), with very low certainty of evidence ([Table 5]). In a prior manner, the angulation of canine eruption before bone graft surgery was considered a risk for impaction by all[3] [7] [13] [14] the studies, and only one[7] study clearly described the stage of root formation in 1/4 to 2/3 of the root of the canine on the cleft side before the bone graft.
One[13] study reported that the rate of canine eruption was strongly correlated with its previous inclination (Fisher, p < 0.00); the angulation of the canine on the noncleft side ranged from 15.90 (p < 0.001)[14] to 86.60 (p < 0.001),[7] values with significant difference in relation to the cleft side. Canine impaction on the noncleft side ranged from 1.3% (86.60) (p < 0.001)[7] and 2.9% (300) (p < 0.05)[14] to 25% (> 45).[3] One[13] study did not clearly report about the frequency of canine impaction on the noncleft side. Only one[14] study clearly reported that canine impaction increased by 50% after reoperation of the bone graft.
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Success of Bone Graft
In general, all[3] [7] [13] [14] the studies reported success of the bone graft ([Table 4]) with low certainty of evidence ([Table 5]). After follow-up, the condition of the graft was considered a success in all the individuals in two[3] [7] studies, and successful in 93.7% of patients in one[13] study. Only two [13] [14] studies reported rates of bone graft failures; however, the rates were low, 11.8%[14] and 6.3%,[13] indicating that bone grafting procedures were successful in the large majority of cases.
All[3] [7] [13] [14] the studies performed 2D radiographic follow-up examinations, with initial and final panoramic r-X examinations; however, with wide sample [13] [14] and temporal variation in[3] [7] [13] [14] the examinations performed. No study used 3D examinations. The initial and final r-X examinations, respectively, were performed on an average at 4.9 y and 12.5 y (partial sample = 76),[13] 7 y (partial sample = 59) and 10 y (partial sample = 41)[14], 6.2 y and 8.10 y (early graft) and 12.8 y and 14.4 y (late graft),[3] and 9.8 y (T1)–T2 (3–12 m after T1) and T3 > 13 m after T1 (mean time of follow-up 33m).[7]
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Canine Impacted due to Agenesis of the Lateral Incisor
Three studies clearly reported canine impaction due to agenesis of the lateral incisor, with conflicting results.[3] [7] [13] Two[3] [7] studies reported association between the rate of canine impaction and agenesis of the lateral incisor, while another[13] study did not find this association ([Tables 3]-[4]), with very low certainty of the evidence ([Table 5]). Agenesis of the lateral incisor generated distinct canine impaction in the patients with UCLP, ranging from 72.2%,[7] 68% of the vertical position and/or abnormal lateral position[3], of up to 20%.[13] Non impaction was 33.3% (p = 0.006) in one[7] study, and 80% in the other.[13] One[3] study reported that the noncleft side also demonstrated some type of abnormal position of the canine, 54%, vertical and/or lateral.
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Effect of Orthodontic Treatment before and after Bone Graft Surgery
Two studies reported the effect of orthodontic treatment before and after the bone graft. [7] [13] In general, one [7] study reported association between rapid maxillary expansion (RME) and gain of space in the maxilla and improved response of tooth eruption before the bone graft, while the other[13] study did not obtain this association ([Tables 3]-[4]), with very low certainty of the evidence ([Table 5]). In the pregraft period, only one[7] study clearly reported the type of orthodontic treatment performed, which was RME in 90% of the patients. In the postgraft period, one study[13], with a subgroup of 45 patients at the stage of permanent dentition were treated with orthodontic movement and 70% of the patients were submitted to RME. In another study[7], 28% of the patients were submitted to orthodontic treatment with partial fixed appliances for rotational correction of the lateral incisor. In both studies, the treatments were performed after the period of canine eruption.[7] [13]
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Certainty of the Evidence
The certainty of the evidence was very low or low due to problems of risk of bias, inconsistency, indirectness, imprecision, and publication bias ([Table 5]). The evidence was rated up due to large effect.
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Discussion
There was very low evidence of patients with cleft lip and palate being able to benefit from bone graft surgery for eruption of the canine teeth.
With regard to the outcome, involving successful bone graft, different types of grafts were reported, which contributed to the heterogeneity of the estimates. The rhBMP-2 (morphogenetic bone proteins) were used in one[7] study and may have influenced bone healing[7] [21] and favored tooth eruption. Complications such as reoperation procedures performed due to failure of the bone grafts reported[13] [14] elevated the risk of canine impaction, due to the additional surgery that deteriorated a site that was already overloaded with inherited and environmental limitations[14]. Although the studies [3] [7] [13] [14] reported successful bone grafting and tooth eruption with panoramic radiography, [22] there was wide methodological variability of the studies and potential influence of the evaluator on the results. In this sense, 3D analyses must be encouraged as a method for evaluating the results of canine eruption, and recently-formed bone [23] 6 months post-surgery with cortical bone maturation.[24] The 3D examination may increase the interexaminer reliability, improve reproducibility of the method[25], enable digitization of small regions for precise diagnosis, and have low dose irradiated in reduced images[26] of the cleft.
Cleft lip and palate arise from the absence of fusion between the primary palate, secondary uni- or bilateral maxillary and palatine processes, affect the upper lip and extend up to the sulcus between the canine and lateral incisor (LI), commonly generating agenesis and tooth impactions, even attaining the maxilla and nose in the eighth week of gestation.[3] [27] As from this gestational phase, absence of the LI over the course of time appears to be a factor that reduces the potential of verticalization of the canines and spontaneous eruption,[3] [14] with 68% more risk of impaction versus 6% on the noncleft side[3], and predictive of impaction in 81% of the individuals.[7] For other[13] [27] studies, the presence of LI did not appear to be so relevant in the orientation of canine eruption.
In the outcome, rate of canine eruption, mesiodistal inclination appeared to be predictive of canine retention.[13] Some studies have suggested that mesiodistal inclination of the canine > 30 in 7 to 10 years may increase the probability of impaction,[3] [14] [27] [28] when compared with the medium angle of 22°[29] of impacted canines in patients without clefts. Although other authors[30] have not found this association, in the studies evaluated, the cleft side showed canines that were more angulated[3] [7] [13] [14] and more distant from the occlusal plane[7]. In the postgraft period, the position of the canine became more vertical in the majority of the individuals[3] [7] [13] [14] and the neoformed bone frequently allowed spontaneous migration and eruption of the canine on the cleft side.[7] [31] [33] The studies[3] [7] [13] [14] were not sufficiently clear about whether the follow-up of the canine corresponded to the period of rhizogenesis and active eruption, commonly occurring from 9 to 12 years; and only two studies reported follow-up for periods longer than 36 months.[13] [14]
The outcome, orthodontic treatment success, combined orthodontics with the surgical approaches as a common procedure in UCLP and BCLP. Along this line, expansion of the maxillary arch before bone grafting has been recommended in many clinical discussions, but not supported in the literature as being necessary to increase the space in the area of the cleft and promote canine eruption.[3] Only one[7] study was clear about the orthodontic treatment performed prior to bone grafting, RME in 90% of the individuals. As an alternative approach, post bone-grafting expansion would minimize the size of the cleft defect. Two[3] [13] studies considered postbone grafting the adequate time for performing the two treatments, using maxillary expansion and fixed orthodontic appliances. To sum up, it was not sufficiently clear whether there would be a significant difference in canine eruption if expansion of the arch were performed pre- or postbone grafting.[31] [32] Although this study addressed as comparison (C) in PICO question the side not submitted to surgery for patients with UCLP, the descriptive results demonstrated for BCLP suggest a behavior similar to the cleft side of patients with UCLP, with analogous outcomes.
The certainty of the evidence was low to very low. In general, all studies had critical risk of bias, due to confunding, bias on account of missing data, bias in measurement of the outcome and selection of the result reported. There was imprecision for some outcomes due to limited number of studies and this consequently limited the sample size and number of events. We also found inconsistency in results with conflicting data and limited applicability of the types of orthodontic treatments that could improve the rates of canine eruption. Although we thoroughly searched several electronic databases, gray literature and performed a manual search, we suspected a selection reporting bias in trials that did not publishing negative outcomes. We rated up the certainty of the evidence, since some studies reported effect estimates of large effect.
Strengths and Limitations
This study had limitations. There were a limited number of studies included, which led to the effect of imprecision of the data input on the results. Meta-analysis was not possible due to the great heterogeneity of data reported among studies. However, as a strong point, we used the GRADE approach to report the certainty of the evidence for narrative synthesis when ROBINS-I was used for risk of bias.[19] The GRADE approach for narrative synthesis can avoid misleading conclusions and be more conservative for interpretation of the results.[19] [34] This systematic view was conducted with strict methodological rigor.
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Implications for Research
Controlled clinical trials (RCTs) with clinical and radiographic methodologies such as standardization of the severity of the cleft, blinding of the professionals (the outcome evaluator should not be the surgeon, and should not have knowledge of the patient's previous history), performing sample calculation, evaluating the level of rhizogenesis of the canine, and time of follow-up longer than 3 years, in order to evaluate the influence of bone grafting and agenesis of the lateral incisor on the eruption of the canine, are necessary and would offer more information in the long term. However, due to the particularities of patients with cleft lip and palate, factors such as age, patient expectations, surgical options, and orthodontic planning may make it difficult to conduct RCTs. Therefore, future high-quality, nonrandomized observational studies may allow significant outcomes to be obtained.
Possible sources of bias must be controlled, such as the insertion of sufficiently clear protocols for surgical and orthodontic treatment, 3D measurement instruments of recently-formed bone and tooth eruption, and longer periods of follow-up. Further studies must also investigate the esthetic satisfaction and quality of life of patients submitted to the different treatment modalities.
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Conclusions
There is low to very low certainty of evidence:
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Of the efficacy of the secondary bone graft for patients with cleft lip and palate.
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Secondary alveolar bone grafting favored the increase in rates of eruption and diminished impaction of maxillary canines.
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On the effect of grafting on the rate of canine impaction and agenesis of the lateral incisor.
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On the efficacy of orthodontic treatment before bone grafting to promote greater gain of space in the maxilla and improve the response of tooth eruption.
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Conflict of Interest
None declared.
Acknowledgment
Acknowledgment for the Scientific Initiation Scholarships of the PIBIC and VIC Programs (CNPq/UFJF).
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References
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- 2 Liao YF, Huang CS. Presurgical and postsurgical orthodontics are associated with superior secondary alveolar bone grafting outcomes. J Craniomaxillofac Surg 2015; 43 (05) 717-723
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- 4 Souza J, Raskin S. Clinical and epidemiological study of orofacial clefts. J Pediatr (Rio J) 2013; 89 (02) 137-144
- 5 Collins M, James DR, Mars M. Alveolar bone grafting: a review of 115 patients. Eur J Orthod 1998; 20 (02) 115-120
- 6 Jia YL, Fu MK, Ma L. Long-term outcome of secondary alveolar bone grafting in patients with various types of cleft. Br J Oral Maxillofac Surg 2006; 44 (04) 308-312
- 7 Simões Holz I, Martinelli Carvalho R, Lauris JR, Lindauer SJ, Gamba Garib D. Permanent canine eruption into the alveolar cleft region after secondary alveolar bone grafting: Are there prediction factors for impaction?. Am J Orthod Dentofacial Orthop 2018; 154 (05) 657-663
- 8 Schultze-Mosgau S, Nkenke E, Schlegel AK, Hirschfelder U, Wiltfang J. Analysis of bone resorption after secondary alveolar cleft bone grafts before and after canine eruption in connection with orthodontic gap closure or prosthodontic treatment. J Oral Maxillofac Surg 2003; 61 (11) 1245-1248
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Address for correspondence
Publication History
Article published online:
23 February 2021
© 2021. European Journal of Dentistry. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).
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References
- 1 Park HM, Han DH, Baek SH. Comparison of tooth development stage of the maxillary anterior teeth before and after secondary alveolar bone graft: Unilateral cleft lip and alveolus vs unilateral cleft lip and palate. Angle Orthod 2014; 84 (06) 989-994
- 2 Liao YF, Huang CS. Presurgical and postsurgical orthodontics are associated with superior secondary alveolar bone grafting outcomes. J Craniomaxillofac Surg 2015; 43 (05) 717-723
- 3 Russell KA, McLeod CE. Canine eruption in patients with complete cleft lip and palate. Cleft Palate Craniofac J 2008; 45 (01) 73-80
- 4 Souza J, Raskin S. Clinical and epidemiological study of orofacial clefts. J Pediatr (Rio J) 2013; 89 (02) 137-144
- 5 Collins M, James DR, Mars M. Alveolar bone grafting: a review of 115 patients. Eur J Orthod 1998; 20 (02) 115-120
- 6 Jia YL, Fu MK, Ma L. Long-term outcome of secondary alveolar bone grafting in patients with various types of cleft. Br J Oral Maxillofac Surg 2006; 44 (04) 308-312
- 7 Simões Holz I, Martinelli Carvalho R, Lauris JR, Lindauer SJ, Gamba Garib D. Permanent canine eruption into the alveolar cleft region after secondary alveolar bone grafting: Are there prediction factors for impaction?. Am J Orthod Dentofacial Orthop 2018; 154 (05) 657-663
- 8 Schultze-Mosgau S, Nkenke E, Schlegel AK, Hirschfelder U, Wiltfang J. Analysis of bone resorption after secondary alveolar cleft bone grafts before and after canine eruption in connection with orthodontic gap closure or prosthodontic treatment. J Oral Maxillofac Surg 2003; 61 (11) 1245-1248
- 9 Enemark H, Sindet-Pedersen S, Bundgaard M. Long-term results after secondary bone grafting of alveolar clefts. J Oral Maxillofac Surg 1987; 45 (11) 913-919
- 10 Hardesty RA, Marsh JL. Craniofacial onlay bone grafting: a prospective evaluation of graft morphology, orientation, and embryonic origin. Plast Reconstr Surg 1990; 85 (01) 5-14
- 11 Enemark H, Jensen J, Bosch C. Mandibular bone graft material for reconstruction of alveolar cleft defects: long-term results. Cleft Palate Craniofac J 2001; 38 (02) 155-163
- 12 Kortebein MJ, Nelson CL, Sadove AM. Retrospective analysis of 135 secondary alveolar cleft grafts using iliac or calvarial bone. J Oral Maxillofac Surg 1991; 49 (05) 493-498
- 13 Meazzini MC, Tortora C, Morabito A, Garattini G, Brusati R. Alveolar bone formation in patients with unilateral and bilateral cleft lip and palate after early secondary gingivoalveoloplasty: Long-term results. Plast Reconstr Surg 2007; 119 (05) 1527-1537
- 14 Westerlund A, Sjöström M, Björnström L, Ransjö M. What factors are associated with impacted canines in cleft patients?. J Oral Maxillofac Surg 2014; 72 (11) 2109-2114
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