Iliac Crest Bone Grafting of the Alveolar Cleft: Clinical and Quantitative Radiographic Assessment

Iliac Crest Bone Grafting of the Alveolar Cleft: Clinical and Quantitative Radiographic Assessment

Thuaksuban, Nuntanaranont Asian J Oral Maxillofac Surg. 2006;18:105-12. CLINICAL OBSERVATIONS Iliac Crest Bone Grafting of the Alveolar Cleft: Clini...

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Thuaksuban, Nuntanaranont

Asian J Oral Maxillofac Surg. 2006;18:105-12. CLINICAL OBSERVATIONS

Iliac Crest Bone Grafting of the Alveolar Cleft: Clinical and Quantitative Radiographic Assessment Nuttawut Thuaksuban, Thongchai Nuntanaranont Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Hatyai, Thailand

Abstract Objective: To evaluate the clinical results and quantitatively assess bone graft volume after secondary alveolar cleft bone grafting. Patients and Methods: Twenty five patients with alveolar clefts (19 unilateral and 6 bilateral) were enrolled in this prospective study. All alveolar cleft defects were grafted with cancellous bone harvested from the anterior iliac crest and closed by advancement flap. Occlusal X-rays were taken preoperatively, early postoperatively, and 1, 3, 6, 12, 18, and 24 months after the operation. A custom-made film holder was used to control film-to-source distance and angulation, thus permitting a reproducible film position at each time interval. An aluminium step wedge was attached to each film for calibrating the quantitative measurement of radiographic bone density. Assessment of the bone graft was done by measurement of bone density, and bone graft height by image processing and analysis software. Results: The average bone graft volume was 3.30 mL (SD, 1.46 mL). The duration of hospital stay was 5.30 days (SD, 1.02 days). The oronasal fistula was closed in all cases. The canines eventually erupted through the grafted area with the assistance of postoperative orthodontic treatment. Bone graft density in the cleft site rapidly decreased 1 month after the operation, becoming stable after 6 months. The bone graft height significantly decreased over 6 months (p < 0.05), then became stable. The average bone density and bone graft height reduction were 20.40% and 35.11%, respectively. Conclusions: Due to the large amount of cancellous bone available and low surgical morbidity, iliac crest bone grafting remains a promising method for the correction of alveolar cleft defects. However, the high resorption rate of the graft should be considered when choosing the grafting material. Key words: Alveolar process, Bone transplantation

Introduction Alveolar cleft grafting is an important procedure for treatment of cleft lip and palate. The objectives are to bridge the alveolar arch, close the oronasal fistula, and support the eruption of teeth. Secondary bone grafting is recommended before canine tooth eruption at the one-half to two-thirds root formation stage. Several sources of bone graft have been proposed, including calvarial bone, mandibular symphyseal bone, rib bone, and iliac bone. Cancellous bone Correspondence: Nuttawut Thuaksuban, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Hatyai, Songkhla, 90112, Thailand. Tel: (66 74) 429 876; Fax: (66 74) 429 876; E-mail: [email protected]

© Asian 2006J Asian Oral Maxillofac Association Surg of Oral Vol 18, andNo Maxillofacial 2, 2006 Surgeons.

harvested from the iliac crest region has been widely used. This technique provides a large volume of osteogenic cells that are beneficial for new bone formation in the cleft defect. The pattern of change in the bone after grafting is a significant factor influencing further dental procedures. Knowledge of this area will permit the clinician to apply orthodontic forces or a prosthesis such as an implant at the appropriate time. Periapical and occlusal X-rays have been used in several studies for evaluation of the quantity of bone graft postoperatively.1-8 However, a major disadvantage of this technique is that the bone graft is visualised in only 2 dimensions, thus bone volume could not be 105

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assessed. 9-11 In addition, standardisation and reproducibility of the position in the radiographic procedure has not been well documented. Thus, the comparative measurement of each film is probably not accurate.1,2,12,13 Several studies have recommended computed tomography (CT) for this purpose because of the clear advantage in reproducibility and the 3-dimensional images. 9-11,13-15 However, the disadvantage of CT is the higher radiation exposure and cost. Rosenstein et al found a significant correlation between the estimated root coverage derived from periapical and occlusal X-rays and that of CT,13 although comparative studies remain desirable. Resorption of the bone graft varies from 24% to 65%.1,10,11,14,15 Kearns et al indicated that alveolar bone was resorbed with time.16 Honma et al used CT to monitor bone volume before the operation and at 3 months and 1 year postoperatively.14 These researchers reported that the volume at 1 year was significantly decreased when compared with that at 3 months — the postoperative bone volume was 99% (SD, 38%) compared with a preoperative bone volume of 115% (SD, 47%). No previous study has focused on the reproducibility of position and radiographic calibration to clearly enable quantitative demonstration of the pattern of graft remodelling at each time interval after bone grafting. The aim of this study was to continuously evaluate the clinical results and radiographic pattern of bone graft remodelling, with attention to improving the comparability of the result between different time intervals.

Patients and Methods The study was conducted from June 2002 to December 2004 at the Dental Hospital, Prince of Songkla University, Hatyai, Thailand. Twenty five patients with a residual alveolar cleft were enrolled in the study. There were 11 boys and 14 girls and the average age was 14.4 years (SD, 6.4 years). Nineteen patients had unilateral alveolar clefts and 6 had bilateral alveolar clefts. Secondary alveolar bone grafting was performed by 2 surgeons using the same surgical technique. All alveolar cleft sites were filled with cancellous bone harvested from the anterior iliac crest by the trapdoor 106

technique (Figure 1). After packing the harvested bone in a syringe, the graft volume was recorded before inserting the bone into the prepared cleft site (Figure 2). The alveolar cleft site was then closed by the gingival advancement flap technique. Analgesics (acetaminophen and meperidine) and antibiotics (intravenous cephalosporin) were prescribed according to the standard protocol. Postoperatively, a temporary palatal acrylic stent was constructed and inserted to stabilise the cleft segment during the graft healing phase. Clinical evaluation included duration of hospital stay, complications of the operation, and presence of an oronasal fistula. Occlusal X-rays were taken by an intraoral radiography machine (Gendex GX 1000; Gendex Corporation, Desplaines, USA) preoperatively, immediately postoperatively, and 1, 3, 6, 12, 18, and 24 months after the operation with individually constant kilovoltage, milliamp, and exposure time. A custom film holder was used to determine the distance and angulation of the radiographic beam, permitting reproducibility of the film for each patient. An aluminium step wedge was attached to each film for calibrating the radiographic bone density (Figure 3).17-19 The films were processed by the radiography machine processing apparatus (DentX 9000; AFD Imaging, Elmsford, USA). Each radiographic image was captured and transferred to a personal computer by the imaging densitometer (Bio-Rad GS-700; GMI Inc, Ramsey, USA) at a resolution of 2672 x 3558 pixels. The digital images were then analysed by image processing and analysis software (Image Pro Plus 5.0, Media Cybernetics Inc, Silver Spring, USA). The preoperative cleft areas were outlined and measured. The outlines were duplicated to each serial postoperative X-ray in the same patient. The areas occupied by the erupted teeth were detected and deleted from the measured outline area. Bone graft quantity in the cleft defect was analysed and assessed by 2 methods. First, the optical density in the outlined cleft site was calculated and measured by the digital image processing and analysis software into the grey measurement (Figure 4). The grey scale measurement produced information about Asian J Oral Maxillofac Surg Vol 18, No 2, 2006

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Figure 1. Technique for alveolar cleft grafting. (a) Preoperative view; (b) cleft prepared for grafting; (c) bone inserted into cleft; and (d) closure using gingival sliding flap.

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Figure 2. Iliac bone harvesting. (a) Iliac crest donor site; and (b) harvested cancellous bone packed into a syringe and the volume measured.

the grey level (brightness) of the entire pixels in the selected image area. The programme measured and calculated the mean grey level according to the following calculation: Mean grey = sum of grey/number of pixels measured. Asian J Oral Maxillofac Surg Vol 18, No 2, 2006

The second assessment consisted of measurement of the remaining bone graft height postoperatively at the previously mentioned time intervals. The method for measuring the bone graft height was modified from Long et al20,21 and Rosenstein et al13 and 107

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Figure 3. (a) The custom film holder with an aluminium step wedge is attached to the occlusal film to provide a reproducible radiographic examination; and (b) the patient’s position is adjusted for the radiographic procedure.

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Figure 4. Resorption of the bone graft was determined by measurement of bone density. The preoperative cleft area was outlined and duplicated on each serial postoperative X-ray for density measurement. (a) Preoperative X-ray; (b) immediately postoperation; (c) 1 month postoperation; (d) 3 months postoperation; and (e) 6 months postoperation.

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demonstrated the percentage of bone coverage of the tooth roots adjacent to the cleft site (Figures 5 and 6).

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Statistical Analysis Descriptive analysis was used for clinical evaluation. Non-parametric statistics (Kruskal-Wallis test and Dunn’s multiple comparison tests) were used for assessment of bone graft quantities at each time interval. A p value <0.05 was considered significant.

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Results All patients tolerated the operation well without postoperative complications. All cleft defects could be closed using a tension-free gingival sliding flap. The average bone graft volume was 3.30 mL (SD, 1.46 mL). The patients were able to walk with weightbearing assistance within a few days. The mean duration of hospital stay was 5.30 days (SD, 1.02 days).

Figure 5. Measurement of bone graft height.

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Figure 6. Bone graft height measured by the image processing and analysis software. (a) Preoperative X-ray; (b) immediately postoperation; (c) 1 month postoperation; (d) 3 months postoperation; and (e) 6 months postoperation. Asian J Oral Maxillofac Surg Vol 18, No 2, 2006

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No postoperative infection or major dehiscence of the flap was detected. The donor site area healed without significant scarring or other problems.

graft height reduction were 20.40% and 35.11%, respectively, when compared with the immediate postoperative stage.

The majority of recipient alveolar cleft defects demonstrated good healing without postoperative infection requiring secondary surgical intervention. Most cleft sites were covered with attached gingival tissue gained by the sliding gingival method. This keratinised tissue was essential for the further eruption of the teeth at the cleft site and prosthesis reconstruction. The teeth in the cleft side erupted well through the grafted area with the assistance of postoperative orthodontic treatment.

Discussion

The bone graft density at the cleft site analysed by the image processing system showed a rapid decrease 1 month after the operation. Then the density gradually reduced until it stabilised at 6 months. No statistically significant difference was noted between the different time intervals. Nevertheless, some increase in bone density at 12 months after grafting was noted (Figure 7). Conversely, the bone graft height showed significant reduction throughout the 6-month interval (p < 0.05) followed by stable measurements without observed increase in crestal height (Figure 8). The average bone density and bone

The clinical results of this study showed a satisfactory outcome for iliac crest bone grafting as secondary alveolar cleft grafting. The gingival sliding flap provided optimal keratinised tissue for further orthodontic and prosthetic reconstruction including implants. The amount of bone graft harvested from the iliac crest and duration of hospital stay were comparable with previous reports.4,10 No serious postoperative complications were detected. The majority of oronasal fistulae could be closed without any soft tissue dehiscence or graft bone exposure. When using plain X-rays to evaluate the bony pattern, a commonly encountered problem is that the outline of the graft is indistinguishable from the surrounding alveolar bone. Thus, to locate the boundary of the bone graft site for any comparative measurement, the outline of the bone graft area from the first postoperative X-ray must be superimposed on subsequent X-rays for each patient in the same position. To solve this problem, first, a constant position in the radiographic technique needs to be

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Figure 8. Bone graft height during the 24-month follow-up period. Asian J Oral Maxillofac Surg Vol 18, No 2, 2006

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achieved. In this study, a simple individual custom film holder was made for each patient to reproduce the spatial position between the radiographic beam and the film. Although some authors mentioned that an error in the reproducible position might occur due to the changing occlusal plane in growing patients,11 this was thought to be minimal in this study and minimal radiographic distortion was noted. Secondly, the aluminium step wedge attached to the films provided precision for the digital image analysis of bone density by the calibration technique. The wedge has been widely used to calibrate the grey level of the radiographic image for subtracted interpretation. This method can reduce the error of different radiation exposures and film processing. To measure bone graft height, the bone coverage of tooth roots was measured as a percentage rather than in mm to prevent radiographic shortening and elongation of the reference points. Bone graft density demonstrated a rapid decrease 1 month postoperatively, gradually reducing until the density became stable at 6 months. This implied a rapid remodelling process immediately after the grafting procedure, with only a gradual change detected thereafter. However, a gradual increase in bone density 12 months after bone grafting was noted. This may be a result of maturation of the cortical structure of the alveolar process in the long term. Koole et al22 measured bone density in sheep by image analysing computer and found that, at 6 weeks, the graft was less radiopaque. At 12 weeks, the alveolar cortex was almost reconstituted, and at 26 weeks, the grafts were almost indistinguishable from the host bone. These researchers suggested that the bone turnover was increased until 6 months after operation. Similarly, Honma, et al14 reported the formation of cortical and cancellous bone that became continuous with the adjacent normal alveolar bone during the observation period of 6 to 12 months after bone grafting.14 Hamamoto et al demonstrated histologically that the graft was undergoing remodelling and replacement with newly formed bone at 6 months, whereas the active remodelling was completed by 12 months.23 Results of studies of the orthodontic force for tooth movement and arch expansion recommended waiting at least 6 months after bone grafting before starting treatment. Asian J Oral Maxillofac Surg Vol 18, No 2, 2006

The bone graft height significantly reduced during the first 6 months, followed by stable measurements without observed increase in crestal height. In this study, the bone graft height reduction was 35.11% and the clinical results were all compatible with an acceptable outcome. However, Tai et al found a possibility of over- or underestimating bone support by 15% to 20% when using routine dental X-rays for evaluation.10 Several factors influence the resorption of the bone graft. Some studies suggested that the existence of the alveolar process depends on the presence of teeth.10,11 Therefore, resorption might occur in the period of absence of the canine, lateral incisor, or both. Honma et al recommended that the graft site should be restored by a functioning tooth to prevent further bone resorption.14 On the other hand, Long et al suggested that the pattern of canine eruption did not affect the success of bone grafting.20 Other factors, including tension of the mucoperiosteal flaps covering the graft, size of the defect, or rapid revascularisation due to an endochondral bone origin, might also be involved in the resorption process.14.21 Keeping these factors in mind, the standard procedure of gingival sliding flap, tension-free closure of the flap, and use of a palatal stent to stabilise the segments during the postoperative phase was used in this study to promote graft bone healing with a satisfactory outcome. Based on the large amount of cancellous bone and low surgical complications, iliac crest bone grafting remains an effective method for correction of alveolar clefts. However, the high bone graft resorption rate and the alveolar crest height reduction despite an appropriate surgical protocol should be considered. Use of a reproducible radiographic technique and step wedge calibration is recommended as a method for precise evaluation of postoperative bone graft quantity.

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scans in determining bone support for cleft-adjacent teeth following early alveolar bone grafts. Cleft Palate Craniofac J. 1997;34:199-205. Honma K, Kobayashi T, Nakajima T, Hayasi T. Computed tomographic evaluation of bone formation after secondary bone grafting of alveolar clefts. J Oral Maxillofac Surg. 1999;57:1209-13. Van der Meij, Baart JA, Prahl-Andersen B, Valk J, Kostense PJ, Tuinzing DB. Bone volume after secondary bone grafting in unilateral and bilateral clefts determined by computer tomography scans. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001;92:136-41. Kearns G, Perrott DH, Sharma A, Kaban LB, Vargervik K. Placement of endosseous implants in grafted alveolar clefts. Cleft Palate Craniofac J. 1997;34:520-25. Cape JB, Samchukov ML. Mineralization dynamic of regenerate bone during mandibular osteodistraction. Int J Oral Maxillofac Surg. 2001;30:234-42. Ortman L, Dunford R, McHenry K, Hausmann E. Subtraction radiography and computer assisted densitometric analyses of standardized radiographs. J Periodont Res. 1985:20:644-51. Ruttimann U, Webber L. Volumetry of localized bone lesions by subtraction radiography. J Periodont Res. 1987; 22:215-6. Long RE, Paterno M, Vinson B. Effect of cuspid positioning in the cleft at the time of secondary alveolar bone grafting on eventual graft success. Cleft Palate Craniofac J. 1996; 33:225-30. Long RE, Spangler BE, Yow M. Cleft width and secondary alveolar bone graft success. Cleft Palate Craniofac J. 1995; 32:420-7. Koole R, deVisscher WJ, Klein WR, Suiker AM. A comparative investigation on autologous mandibular and iliac crest bone grafts: an experimental study in sheep. J Cranio Max Fac Surg. 1991;19:133-43. Hamamoto N, Hamamoto Y, Kobayashi T. Tooth autotransplantation into the bone-grafted alveolar cleft : Report of two cases with histologic finding. J Oral Maxillofac Surg. 1998;56:1451-6.

Asian J Oral Maxillofac Surg Vol 18, No 2, 2006