Mandibular Symphyseal Bone Graft for Reconstruction of Alveolar Cleft Defects: Volumetric Assessment with Cone Beam Computed Tomography 1-Year Postsurgery

Abstract

Objective

The aims of this retrospective study were to evaluate the volumetric outcome of mandibular symphyseal bone graft in patients with unilateral cleft lip and palate by estimating the bone fill 1-year postoperatively on cone beam computed tomography. The outcome was assessed in relation to the (1) root development stage of the cleft side canine, (2) presence/absence of a cleft side lateral incisor, and (3) volume size of the preoperative cleft defect.

Methods

The alveolar bone defect volume of 32 consecutive unilateral cleft lip and palate patients aged 8 years 1 month to 11 years 11 months was evaluated using a recently defined and standardized protocol. The outcome was calculated as the percentage of bone fill using the formula (VOLpre - VOLpost) / VOLpre) x 100.

Results

The preoperative mean alveolar cleft volume was 934 mm³, and the average percentage bone fill was 87%. There was no significant difference between bone fill and root developmental stage of the cleft-side canine (P = .882) nor presence/absence of the cleft side lateral incisor (P = .803). The size of the cleft defect did not correlate with the bone fill (r = .03, P = .84).

Conclusions

Secondary alveolar bone grafting with mandibular symphyseal bone graft in patients with unilateral cleft lip and palate is an attractive procedure assessed from the volumetric outcome using cone beam computed tomography. The 1-year average bone fill of 87% was not significantly influenced by root development stage of the cleft-side canine, presence or the absence of a cleft side lateral incisor, or size of the alveolar defect.

Keywords

alveolar bone grafting CBCT cone beam computed tomography mandibular bone volume

Secondary bone grafting in alveolar clefts was first reported by Boyne and Sands (1972, 1976) in the 1970s, and it is today an integral part of the management of patients with cleft lip and palate (CLP) (Shaw et al., 2000; Murthy and Lehman, 2005). A successful alveolar bone graft procedure ensures continuity of the maxillary arch, facilitates eruption of the permanent teeth, provides adequate bone support, preserves the periodontal health of the teeth adjacent to the cleft, permits orthodontic tooth alignment, allows placement of osseointegrated implants, and improves alar base symmetry (Bergland et al. 1986; Amanat and Langdon, 1991; Cohen et al., 1993; Dempf et al., 2002).

Various bone sources, including anterior iliac crest, tibia, rib, calvarium, and mandible, have been studied and compared. The question of which donor site to use has been debated for decades (Rawashdeh and Telfah, 2008; Semb, 2012). The choice is often guided by the surgeon's experience and preference, the bone volume needed, and even by donor site morbidity, although it is difficult to compare morbidity at different bone graft donor sites (Rawashdeh and Telfah, 2008; Semb, 2012).

The clinical use of mandibular symphyseal bone graft (MSBG) for reconstructive procedures in the maxillofacial region was first described by Bosker and van Dijk (1980), who reported good results for reconstruction of alveolar cleft defects. Since then, numerous reports have documented that MSBG is a very attractive donor material and the mandibular symphysis an ideal site because a MSBG is usually assumed to have a satisfactory risk-benefit ratio (Sindet-Pedersen and Enemark, 1988; Koole et al., 1989; Sindet-Pedersen and Enemark, 1990; Koole et al. 1991; Hoppenreijs et al., 1992; Freihofer et al., 1993; Enemark et al., 2001; Booij et al., 2005; Mikoya et al., 2010; Andersen et al., 2013). Yet, a study from the millennium reported that only 4% of European CLP teams use MSBG; whereas, the most frequent donor site is the anterior iliac crest, which is favored by 87% (Shaw et al., 2000). This trend apparently has not changed much, but it is worth noticing that autogenous bone substitute is continuously being developed and could soon be a competitive alternative to natural bone (Semb, 2012).

The mandibular symphyseal area is easily accessed, and the advantages of using bone from this site are the involvement of a single site of intraoral operation, a shorter stay in the hospital, an “invisible” scar in the lower alveolar sulcus, and minimal postoperative pain or discomfort (Enemark et al., 2001; Andersen et al., 2013). Andersen et al. (2013) concluded in their recent study that all patients were discharged from the hospital the day after surgery, and medical records revealed few postoperative complications: 5.6% described persistent sensory disturbances in the donor area. Postoperative pain was 3.6 ± 2.1 (scale, 0 to 10). The overall satisfaction with the surgical result averaged 8.7 ± 1.7 (scale, 0 to 10) (Andersen et al., 2013).

Conversely, the volume of bone in the mandibular symphyseal area available for the graft is limited by the eruption of the permanent dentition, and other disadvantages include risk of damage to and disturbance of the adjacent teeth, the mental nerve, and soft tissue (Sindet-Pedersen and Enemark, 1988; Sindet-Pedersen and Enemark, 1990; Hoppenreijs et al., 1992; Koole, 1994; Enemark et al., 2001; Booij et al., 2005). Furthermore, it has been argued that because MSBG contains a high amount of cortical bone compared with iliac bone, for instance, (Chen et al., 1994; Pinholt et al., 1994), MSGB will increase the risk of cleft side canine impaction; however, this notion has been contradicted (Enemark et al., 2001).

Cone beam computed tomography (CBCT) has become a widely acknowledged tool for oral and maxillofacial diagnosis and treatment planning during the past decade (Cattaneo and Melsen, 2008; Grauer et al., 2009). It is a promising method for planning and evaluation of alveolar bone grafts, even if its use for three-dimensional (3D) volumetric analysis of the alveolar bone defect involves a higher radiation dose than two-dimensional (2D) radiographs (Hamada et al., 2005; Oberoi et al., 2009; Shirota et al., 2010; Choi et al., 2012; Quereshy et al., 2012; Zhang et al., 2012; Amirlak et al., 2013).

Diagnostic imaging before alveolar bone grafting is fundamental to the surgical team's planning of the operation and to the effort to minimize any unnecessary excess or insufficient harvesting of bone graft. This, in turn, decreases the total operative time, surgery costs, and morbidity risks while improving treatment outcome. Postoperative CBCT is indicated for evaluation of the grafted area in relation to volumetric estimation of the bone graft and for evaluation of dental development, particularly the eruption pattern of the cleft side canine. Furthermore, if the alveolar graft procedure involves a mandibular donor site, this can be assessed as well. Accordingly, CBCT may provide surgeons and orthodontists with clinical information that has critical importance for their treatment protocol.

However, caution is advised when comparing the results between CBCT studies that use different, unstandardized measurement protocols because outcomes may vary as a matter of fact (Spin-Neto et al., 2011; Linderup et al., 2015). Especially problematic is the absence of standardization of the following parameters : (1) the image acquisition parameters (e.g. CBCT equipment, settings [kV and mA], exposure time, and voxel size); and (2) the image reconstructing parameters (e.g., how to export the image [quality]), field of view, plane definition (anatomical boundaries) for area of interest, thresholding (gray scale) for bone and cleft defects, and segmentation method (e.g., outlining of cleft defect, slice thickness, and number of measured slices) (Spin-Neto et al., 2011).

Furthermore, until today, secondary alveolar bone grafting with anterior iliac crest bone has been the primary object of 3D volumetric analysis, and to our knowledge no volumetric assessment with MSBG has so far been performed.

The aim of the present study was therefore to evaluate the volumetric outcome of MSBG in patients with unilateral CLP (UCLP) by estimating the bone fill 1-year postoperatively. The outcome of alveolar bone grafting was assessed in relation to (1) the root development stage of the maxillary canine on the cleft side, (2) the presence or absence of a lateral incisor, and (3) the volume size of the preoperative cleft defect.

Material and Method

Subjects

The sample for this retrospective study consisted of 34 consecutive patients with nonsyndromic UCLP treated with MSBG in the period from January 2011 to December 2012. Included were only patients for whom CBCT scans obtained before surgery and approximately 1 year after surgery were available. Two patients did not have a postsurgical CBCT due to apparatus failure and no-show, and therefore they were excluded from the study.

In total, presurgical and postsurgical CBCT scans from 32 patients (22 boys and 10 girls) were available, and the patients' average age at the time of alveolar bone grafting was 9 years ± months (range, 8 years 1 month to 11 years 11 months).

All patients included in this study followed a well-established Standard of Care for treatment of Danish CLP patients. Informed consent was obtained from all patients enrolled in the Standard of Care and principles outlined in the Declaration of Helsinki were followed (World Medical Association, 2013).

Preoperative Treatment Planning

All patients underwent secondary alveolar bone grafting at the Aarhus Cleft Palate Center and the Department of Oral and Maxillofacial Surgery, Aarhus University Hospital, Denmark. Following the established Standard of Care, a team including an experienced orthodontist and an experienced maxillofacial surgeon evaluated the indication and proper timing for reconstruction of the alveolar defect, the indication for preoperative extraction of deciduous and supernumerary teeth as well as the type of bone graft, and the indication for a postoperative splint. In all cases, surgery was initiated after orthodontic expansion of the upper dental arch had been completed and the permanent upper incisors had erupted. Deciduous teeth, supernumerary teeth, and malformed permanent incisors in the cleft area were extracted before reconstruction of the alveolar defect to allow proper healing of the mucosa before reconstruction.

Surgical Technique

The bone graft procedure was done by the same surgeon, one who has extensive experience and who uses a firmly established surgical technique (Andersen et al., 2013). A monocortical spongious bone block comprising the outer cortical bone and cancellous part was harvested with a piezoelectric device (Piezosurgery, Mectron, Carasco, Italy). The defect area was visualized and the block of graft bone adjusted and fitted tightly in the defect area without the use of osteosynthesis. The residual bone graft was particulated using a bone mill (Roswitha Quétin Dental Products, Leimen, Germany) to obtain bone graft particles that filled in the residual defects.

CBCT Scans and Volumetric Assessment

According to the established procedure, all patients had a 15 × 12 cm (Diameter X Height) CBCT scan taken about 1 month before secondary alveolar bone grafting (T0) to plan the operation. They had a second scan approximately 1 year after the secondary alveolar bone grafting (T1) to evaluate the cleft area and the donor site (NewTom VGi, QR s.r.1., Verona, Italy). The average time between T0 and T1 was 1 year 2 months (range, 11 months to 1 year 6 months).

The image acquisition parameters included a total exposure time of 3.6 seconds, with settings of 110 kV and 3-7 mA (pulsed mode). Each CBCT scan was reconstructed with a 0.30-mm isotropic voxel dimension and converted into a free matrix Digital Imaging and Communications in Medicine format (NNT software v. 4.6, Verona, Italy). The next step was to import the data into specific 3D analysis software in a lossless data compression (Mimics 15.0; Materialise Interactive Medical Image Control System, Leuven, Belgium).

The qualitative assessment was done according to a reproducible and practical method recently described by the authors (Linderup et al., unpublished data). The protocol is based on standardized image acquisition and reconstruction parameters, which include a semiautomatic segmentation appropriate to the most optimal pseudo Hounsfield units (gray values) (Fig. 1). The volume of the alveolar bone defect (VOLpre) was measured on the preoperative scans, and the volume of any residual defect (VOLpost) was measured on the postoperative scans. In our study, we anticipated that the entire defect would be packed with bone graft material. The radiographic outcome of the alveolar bone graft was calculated as a percentage of bone fill (residual bone volume) using the formula (VOLpre – VOLpost) / VOLpre) X 100.

Figure 1

Screenshots from segmentation. A: Axial plane illustration of the segmentation of the alveolar bone defect on a single slice. B: Axial plane after total segmentation; the total volume of the defect is calculated by the software. C: A 3D model illustrating the segmented defect.

A panoramic radiograph was constructed from the preoperative CBCT scan of each patient to verify the root development stage of the cleft side maxillary canine (less or more than half of the canine root developed) and the presence of a cleft side lateral incisor (yes or no).

Statistical Analysis

The statistical analysis was performed using MedCalc, version 12.7.0.0 (MedCalc, Chicago, IL). The bone fill was conducted with descriptive statistics and illustrated graphically using plots. All variables in relation to bone fill were assessed for normal distribution using the D'Agostino-Pearson test (Sheskin, 2011). Thereafter, the status of canine root development and lateral incisor presence in relation to bone fill was assessed with an independent Student's t test with a P value set to .05 or less. The cleft size in relation to bone fill was tested with the Pearson correlation coefficient.

Results

It was possible to perform volumetric alveolar bone defect analysis on both the preoperative and the postoperative CBCT scans in all 32 patients. Table 1 summarizes the descriptive data. A panoramic radiograph was successfully constructed from each preoperative CBCT scan, which allowed verification of the status of the cleft side canine root development and the occurrence of the cleft-side lateral incisor.

Table 1

Descriptive Data for Alveolar Cleft Volume Preoperatively (VOLpre) and Postoperatively (VOLpost) and Bone Fill

	VOLpre	VOLpost	Bone Fill
Sample size	32	32	32
Arithmetic mean	934mm³	111 mm³	87%
95% CI for the mean*	827	to 1041 mm³	67 to 155 mm³	83% to 93%
Range	451-1601 mm³	0-453 mm³	46%-100%
Standard deviation	296	mm³	122 mm³	14%

CI = confidence interval.

Bone Fill

The mean alveolar cleft volume was 934 mm³ (range, 451 to 1601 mm³) before surgery. The equivalent amount of residual alveolar cleft volume was 111 mm³ (range, 0 to 453 mm³) 1 year after surgery (Table 1; Fig. 2). The average bone fill ratio was 87% (range, 46% to 100%) 1 year after surgery (Table 1).

Root Developmental of Cleft-Side Canine

In the group of individuals in whom less than half of the canine root development was completed, the percentage bone fill was 87%; in the group of individuals in whom more than half of the canine root had developed, it was 88%. This difference was not statistically significant (P = .882), and the stage of root development of the cleft-side canine, therefore, did not affect the percentage bone fill in the present study.

Occurrence of Cleft Side Lateral Incisor

Lateral incisors were absent in 44% of the individuals. The percentage of bone fill in the presence of a lateral incisor was 87% against 88% in the individuals where the lateral incisor was missing (P = .803; no significant difference).

Size of Preoperative Alveolar Cleft Defect

A Pearson correlation coefficient was calculated with the percentage of bone fill as the dependent variable and the preoperative volumetric cleft size as the independent variable. A nonsignificant correlation (r = .03, P = .84) was found between cleft size and the bone fill after 1 year (Table 2; Fig. 3).

Table 2

Correlation Coefficient for Percentage of Bone Fill and Preoperative Volumetric Cleft Size, Variable X; Bone Fill, Variable Y; Preoperative Cleft Volume (VOLpre)

Sample size	32
Correlation coefficient r	.04
Significance level	.84
95% confidence interval for r	−.32 to .38

Figure 2

Dots and lines plot illustrating the change of cleft defect volume preoperatively and postoperatively (VOLpre and VOLpost).

Figure 3

Scatterplot illustrating the correlation between the variables bone fill and preoperative cleft volume (VOLpre).

Discussion

Recent years have seen a shift toward the use of CBCT for assessment of alveolar cleft patients' preoperative and postoperative status, including the volume of the defect (Hamada et al. 2005; Oberoi et al., 2009; Shirota et al., 2010; Choi et al., 2012; Quereshy et al., 2012; Zhang et al., 2012; Amirlak et al., 2013; Linderup et al., unpublished data). Secondary alveolar bone grafting is part of the standard care for patients with alveolar clefts. The amount of alveolar cleft bone fill achieved weighs heavily in the assessment of the outcome of orthodontic treatment, especially if the canine or lateral incisor is missing and, for example, placement of osseointegrated implants is needed (Bergland et al., 1986; Amanat and Langdon, 1991; Cohen et al., 1993; Dempf et al., 2002).

Bone Fill

To our knowledge, only two previous studies have evaluated the quantitative volumetric outcome of alveolar bone grafting on CBCT before and after surgery in CLP patients (Oberoi et al., 2009; Zhang et al., 2012). Oberoi et al. (2009) found 84% bone fill in a group of both UCLP and bilateral CLP 1 year after surgery (mean age = 10.6 years); whereas, Zhang et al. (2012) found 71% bone fill in a group of UCLP patients 6 months after surgery (mean age = 15.8 years). In both studies, all patients were treated with autologous bone from the anterior iliac crest.

In an in vitro study, Albuquerque and coauthors compared the use of CT and CBCT for volumetric assessment of alveolar cleft patients. The authors demonstrated that CT and CBCT both achieved high efficiency and were effective tools for volumetric assessment of bone defects. Both modalities also demonstrated excellent and equally high reliability in a study of the volume of bone defects (Albuquerque et al., 2011). With this in mind, the results of CT studies that evaluate the volumetric outcome of alveolar bone grafting may be comparable with those that use CBCT (Table 3). Nevertheless, due to the various measurement protocols used, caution is required when bone fill rates are compared between studies. Furthermore, there is no obvious criterion standard against which the validity of the results in vivo can be compared.

Table 3

Schematic Literature Overview of Bone Fill (%) Approximately 1 Year After Alveolar Bone Grafting*

Authors	Scans	Patients	Donor Site	Bone Fill (%)
Tai et al., 2000	CT	14 BCLP/UCLP	AICBG	57
van der Meij et al., 2003	CT	53 UCLP	AICBG	64
Dieleman et al., 2004	CT	5 UCLP	AICBG	75
Feichtinger el al., 2007	CT	24 UCLP	AICBG	50
Oberoi et al., 2009	CBCT	21 UCLP	AICBG	84
Zhang et al., 2012†	CBCT	19 UCLP	AICBG	71
Linderup et al. (present study)	CBCT	30 UCLP	MSBG	87

Caution should be used when comparing the bone fill rates between these studies because different measurement techniques can give rise to different outcomes. AICBG = anterior iliac crest bone graft; MSBG = mandibular symphyseal bone graft.

†

6 months postoperative.

Among the studies based on CT, Tai et al. (2000) found that the overall bone fill was 57% in a 1-year prospective study of secondary alveolar bone grafting. van der Meij et al. (2003) found a mean bone fill of 64% in a unilateral group after 1 year. Dieleman et al. (2004) found a 75% bone fill 1 year after secondary bone grafting in a small sample of five patients with UCLP. Feichtinger et al. (2007) reported a mean bone fill of 50% over a period of 1 year and that the transplants remained almost constant for the following 2 years.

It is intriguing to notice the large variation in bone fill among these studies (range, 50% to 87%). We ascribe this variation to the use of different protocols, in particular the variation between these studies in terms of slice thickness, method of segmentation, and definition of area of interest (e.g., superior and inferior margins of the cleft defect). However, the present study may indicate that the bone fill percentage after MSBG is not significantly different from that which is achieved in studies using anterior iliac crest bone grafts.

Physiological Stress

One of the most apparent reasons for resorption of a graft observed after alveolar bone grafting is the absence of physiological stress. Hence, several authors conclude that the bone volume will increase if the grafted area is exposed to dental eruption, orthodontic tooth movement, and/or placement of a dental implant (Kearns et al., 1997; Honma et al., 1999; Dempf et al., 2002; Schultze-Mosgau, et al. 2003; Feichtinger et al., 2007; Ozawa et al., 2007; Zhang et al., 2012). It has been suggested, therefore, that the optimal time for secondary alveolar bone grafting is between 9 and 11 years, that is, before the eruption of the canine, with the canine root half to two-thirds developed (Boyne and Sands, 1976; Bergland et al., 1986). However, in the present study the volumetric outcome was affected neither by the stage of root development of the cleft side canine nor by the presence or absence of a cleft-side lateral incisor. The present results corroborate those reported by Oberoi et al. (2009). Inversely, Zhang et al. (2012) found a significant increase in bone fill depending on the spontaneous eruption of the permanent teeth.

Using 3D, Ozawa et al. (2007) illustrated the importance of migration and eruption of the germs of teeth at the bone grafting area involving initiation and accumulation of bone. The mesial and downward eruption of the canine into the grafted alveolus area was found to be particularly important to achieving a high bone fill ratio (Oberoi et al., 2009; Oberoi et al., 2010).

In the study by Oberoi et al. (2009), 12% of the cleft side canines needed surgical exposure due to impaction. The observation period of the present study (T0 to T1) was too short to judge canine impaction, and a future investigation with a longer observation period should therefore be conducted to reveal the impaction frequency for these patients.

Size of Preoperative Cleft Defect

A 2D study by Long et al. (1995) and a 3D study by van der Meij et al. (2003) showed that the alveolar cleft width is one of the factors that influences the success of bone graft, which indicates that wider clefts are more prone to resorption. Honma et al. (1999) concluded that the wider the cleft between the teeth, the more bone loss occurs after alveolar bone grafting. As in the present study, Oberoi et al. (2009) indicated that the volumetric size of the preoperative defect did not appear to affect the outcome in terms of bone fill. This confirmed previous CT studies (Feichtinger et al., 2006; Kim et al., 2008). Whether presurgical expansion of the maxilla has any direct influence on the resorption in relation to cleft width remains unknown. Only a few studies within this specialty mention whether presurgical expansion was performed (Long et al., 1995; Kim et al., 2008; Oberoi et al., 2009).

The resorption of transplanted bone may also be attributed to other, previously described factors such as dental hygiene, periodontal infections (Keese and Schmelzle, 1995), and tension in the mucoperiostal flap resulting in inadequate bone cover (Bergland et al., 1986; Enemark et al., 1987), which highlights the importance of the skills of the surgeon who performs the procedure (Semb, 2012).

In the present study, oral hygiene and periodontal status were generally well maintained, and presurgical orthodontic expansion allowed approximation of wide cleft defects with a well-vascularized, tension-free gingival flap. Moreover, the same surgeon, who had much experience, performed all the bone graft procedure.

Clinical Implications for the Use of CBCT

Arctander et al. (2005) estimated the clinical condition and amount of remaining grafted bone 20 years after secondary alveolar bone grafting in patients with UCLP. Using CT and clinical examination, they found that there was significantly less bone mass on the grafted cleft side than on the noncleft side, but the functional results were satisfactory. This indicates that the quantitative bone fill may not be the only important factor. It therefore seems misleading to equate the terms bone fill and success rate when the outcome is evaluated in quantitative volume terms only. Qualitative factors like sufficient bone continuity (bridging) between the alveolar segments, the status of the adjacent teeth, and a radiographic architecture showing labial and palatal cortices with interjacent cancellous bone pack is essential to attain survival and orthodontic alignment of the teeth and/or positioning of a dental implant (Rosenstein et al., 1997; Tai et al., 2000). In the present study, 32 patients were evaluated 1 year after surgery and overall bone fill reached 87%. This result revealed that the use of MSBG for alveolar bone grafting in patients with UCLP is an attractive procedure based on the volumetric outcome using CBCT and the few previously reported donor site morbidities (Enemark et al., 2001; Andersen et al., 2013).

In the future, we will therefore use postoperative CBCT imaging only in those cases where information additional to that which may be obtained by conventional radiographic imaging is vital for further treatment planning. This is in agreement with the “as low as reasonably achievable” principle that should be honored at all times. So although contemporary CBCT technology seems to decrease the radiation exposure, the clinician should weight the potential benefits of a CBCT scan against the risk of the additional radiation hazard in each individual patient (Ludlow et al., 2008; Ludlow, 2012).

However, the preoperative CBCT scan remains a fundamental tool in treatment planning because it allows the interdisciplinary team to better plan the operation and hence to minimize any unnecessary excess or insufficient harvesting of bone graft, which, in turn, decreases the total operative time, costs, and morbidity risks while improving treatment outcome.

Conclusion

In conclusion, MSBG is an attractive procedure for reconstruction of alveolar defects in patients with UCLP based on the volumetric outcome using CBCT. The 1-year average bone fill of 87% was not significantly influenced by the root development stage of the cleft side canine, the presence or the absence of a cleft side lateral incisor or the size of the alveolar defect.

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