Bone volume after secondary bone grafting in unilateral and bilateral clefts determined by computed tomography scans

Bone volume after secondary bone grafting in unilateral and bilateral clefts determined by computed tomography scans A. J. W. Van der Meij, DMD,a J. A. Baart, DMD,a B. Prahl-Andersen, DMD, PhD,b J. Valk, MD, PhD,c P. J. Kostense, PhD,d and D. B. Tuinzing, DMD, PhD,a Amsterdam, The Netherlands TEACHING HOSPITAL OF THE FREE UNIVERSITY IN AMSTERDAM/ACADEMIC CENTRE DENTISTRY AMSTERDAM (ACTA)

Objective. The purpose of this study was to evaluate the outcome of bone grafts in cleft palate patients, thus assessing the amount of bone necessary to facilitate eruption—especially in the buccopalatal direction—of the permanent canine into the bone graft. Study design. Computed tomography scans taken immediately postoperatively and 1 year postoperatively of 42 unilateral and of 8 bilateral cleft lip and palate patients who underwent surgery at the age of 9 years (early secondary bone graft) or 12 years (late secondary bone graft) were compared. Three slices from the computed tomography scans taken immediately after the surgery were selected from the center of the bone graft and were then compared with corresponding slices from the 1-year postoperative computed tomography scans. Statistical analysis was performed by using the Wilcoxon 2-sample rank sum test. Results. In the unilateral cleft group, 70% of the transplanted bone remained in the cleft area after 1 year, whereas in the bilateral cleft group, only 45% of the initial bone graft remained after 1 year. Conclusion. No statistically significant difference was found between early secondary bone grafting and late secondary bone grafting. In most cases, a sufficient amount of bone was present in the target area to facilitate eruption of the permanent canine.

(Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:136-41)

Using intraoral radiographs, Enemark et al1 evaluated the results after bone grafting with respect to the marginal bone level of teeth adjacent to the cleft. They reported a significantly higher marginal bone level, both in unilateral and bilateral cases, after early secondary bone grafting than was reported in those groups bone grafted after eruption of the permanent canine. However, the question remains whether the bone level, indicated on nonstandardized intraoral radiographs, gives an accurate indication of the bone volume in the area. Enemark et al1 also compared short-term follow-up results and long-term follow-up results (ie, more than 4 years) of a similar patient group and indicated that in the majority of patients no signs of differences in bone levels over time could be seen. Prahl-Andersen and Lijten2 measured the bone height score of the distal surface of the central incisor on standardized dental radiographs, taken from 28 cleft lip and palate patients (range, 8.7-17.7 years) after secondary aDepartment

of Oral and Maxillofacial Surgery. of Orthodontics. cDepartment of Radiology. dDepartment of Epidemiology and Biostatistics. Received for publication Apr 11, 2000; returned for revision Aug 3, 2000; accepted for publication Jan 4, 2001. Copyright © 2001 by Mosby, Inc. 1079-2104/2001/$35.00 + 0 7/12/115274 doi:10.1067/moe.2001.115274 bDepartment

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bone grafting, by using a measuring grid (a method described by Sjölien and Zachrisson3). Prahl-Andersen and Lijten2 reported a mean bone support of 18.5 score units for their patient group, results that compare favorably with those reported by Sjölien and Zachrisson3— 21.9 score units in a group of orthodontically treated patients without cleft lip and palate. The purpose of this study was to evaluate the outcome of the bone graft, thus assessing whether a sufficient amount of bone in the in buccopalatal direction was present to facilitate eruption of the permanent canine into the bone graft. Evaluation of the fate of the bone graft 1 year postoperatively was carried out through use of computed tomography (CT) scanning techniques.4 All parents and patients were informed of CT scanning protocol and gave their consent. The CT scan is the only technique that shows the bone graft in 3 dimensions, thus providing a method to precisely evaluate bone volumes. At the Free University in Amsterdam, the cleft lip and palate team follows a protocol for the treatment of all patients that entails closing the hard palate and the alveolar cleft and grafting the bone—preferably before the eruption of the permanent canine. This so-called early secondary bone grafting has the advantage of providing a bony eruption path for the canine and sometimes the lateral incisor adjacent to the cleft.5 However, for several reasons, such as the severe

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Van der Meij et al 137

Fig 1. Tracings from immediately after surgery (A1) and 1 year postoperatively (A2) with same magnification factor. Superimposition (A1-A2) of tracings.

malposition of teeth in the cleft area and subsequent realignment by orthodontic presurgical treatment or cases of larger clefts and planned anterior placement of the lesser segment, late secondary bone grafting had to be carried out when the patient was 12 years old or older. Management-related factors such as shifting of the cleft lip and palate team could also be a reason for later bone grafting. In the present investigation, we considered only patients in the 12- to 14-year-old age range from this late secondary group.

STUDY DESIGN The patients were referred by the cleft palate team of the Free University Hospital in Amsterdam from 1983 to 1991; 42 patients had unilateral cleft lip and palate and 8 had bilateral cleft lip and palate. The group represents an average Caucasian cleft lip and palate population.6 Early secondary bone grafting was performed in 30 patients (group 1); late secondary bone grafting was performed in the remaining 20 patients (group 2). Iliac crest bone was used for bone grafting in all patients, and all clefts were closed in one stage by the same surgeon using the same surgical technique. Three days postoperatively and 1 year postoperatively, axial computer tomographs (CT scans) were made, with a slice thickness of 1.5 mm. The distance between consecutive slices, which ran parallel to the occlusal plane and from the occlusal plane to the nasal cavity, was 1.5 mm. Three slices from the center of the bone graft from the CT scans taken immediately after surgery were

selected, and corresponding slices from the 1 year postoperative CT scans were selected (Fig 1). In this way, 3 pairs of CT scans were formed and evaluation of the bone graft could be completed at 3 representative—but different—axial levels (slice levels A, B, and C). Selection and matching of slices was carried out by using the best-fit method and was facilitated by comparing anatomical landmarks, such as the shape of the maxilla and the dorsal part of the cranial base. The CT scans taken immediately after surgery were used as a template to localize the bone graft area on the 1-year postoperative CT scans.4 After the selection and matching of the CT scans, each CT scan was magnified 3 times with an overhead projector. Then the magnified CT scans were traced, digitized, and superimposed. The surface of the initial and the residual bone graft was calculated by using the “surface-measuring” AutoCAD program (Autodesk LTD, Cross Lanes, Guildford, Surrey, United Kingdom).4 The percentage of bone remaining after 1 year was determined in each patient on 3 different axial levels. To evaluate the accuracy and reproducibility of the measurement technique, one randomly chosen CT scan was enlarged, traced, superimposed, and digitized 10 times at 1-week intervals. The SD was 1.95%.

RESULTS The median percentages of residual bone per group are shown in Table I. To explain how these medians were calculated for each group, the statistical method for the unilateral left-sided group will be described in detail.

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Fig 2. Ranking numbers are given in the first row; distribution is in quartiles. These calculations were carried out for each group.

Table I. Median percentage of residual bone per group and significance of differences between groups Group Group 1 UL Group 1 UR Group 2 UL Group 2 UR Group 1 B Group 2 B

Clefts

Median (%)

P value

18 8 10 6 7 6

71.5 68.9 65.0 78.4 53.9 34.0

P > .1 — P > .1 — Not tested —

Group 1, Early; group 2, late secondary bone grafting. UL, Unilateral left-sided; UR, unilateral right-sided; B, bilateral.

The results of the unilateral left-sided cases of group 1 are shown in Table II. The percentage of residual bone per slice and the mean per patient are given. Because the variation of the results among patient groups is larger than within a single patient group, the use of mean values for each patient is justified. These mean values are not normally distributed, which means that outliers will strongly influence the SD. We therefore decided to use the median, quartiles, and the interquartile range (Fig 2). Statistical analysis was performed by using the Wilcoxon 2-sample rank sum test to demonstrate differences within each group as well as between group 1 and group 2. The Wilcoxon test shows that with an 18 (unilateral left-sided group 1) over 8 (unilateral right-sided group 1) series and a level of significance (P) at .1, the nonsignificant range lies between 212 and 274. The rank sum for group 1 is 237, which indicates that there is no significant difference between the left-sided and right-sided results of this group. The results of groups 1 and 2 are shown in Table I; no significant difference was found between the unilateral cases of groups 1 and 2. Both bilateral groups consist of 4 patients; this number is considered too small to perform formal significance testing.

DISCUSSION AND CONCLUSIONS The nomenclature of early secondary bone grafting and late secondary bone grafting is problematic because the optimal age of early bone grafting can be dictated by the dental age of the patient rather than by the biological age. In light of this confusion, it might even be proposed that the secondary bone graft should be performed on much younger patients to allow not only the cuspid to erupt but also the second upper incisor adjacent to the cleft. However, trying to strike a balance between the desire to leave the hard palate open as long as possible to allow the transverse growth of the maxilla and, on the other hand, the desire to close the palate and graft the cleft, allowing the teeth to erupt, can be difficult; nevertheless, we deemed the age of approximately 9 years a rational compromise in this study. On the basis of a group of patients undergoing surgery relatively “late” (ie, at 12 years old and older), the younger group was qualified as “early.” The use of CT scans brings up ethical questions because of the amount of radiation the patient receives. Although in the research on cleft patients, conventional radiographs were shown to have a number of limiting factors, such as distortion and limited numbers of reliable landmarks and superimposing structures, the advantages of CT scans are obvious. Information on the amount of bone in the buccopalatal direction is of clinical importance because the eruption path of the permanent canine is not always favorable in cleft patients because of the lack of deciduous teeth to guide the eruption path. Some discussion exists about the clinical use of evaluating the residual amount of bone 1 year after bone grafting, as the new alveolar ridge responds to the erupting canine after early secondary bone grafting. Information on the behavior and the volume of bone in the target area of the cuspid eruption is critical to treatment planning because, in most cases, the eruption of the canine will occur 2 years after a bone transplantation if the patient is 9 years old.

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Table II. Residual quantity of bone grafts 1-year postoperatively per slice and mean quantity per patient Unilateral left-sided cleft lip and palate patients in group 1 % residual bone Sex

Age

Patient

M

8 y, 6 mo

1

M

9 y, 2 mo

2

M

9 y, 2 mo

3

M

9 y, 4 mo

4

F

9 y, 4 mo

5

F

9 y, 4 mo

6

M

9 y, 5 mo

7

M

9 y, 6 mo

8

F

9 y, 6 mo

9

F

9 y, 6 mo

10

M

9 y, 7 mo

11

M

9 y, 8 mo

12

F

9 y, 8 mo

13

M

9 y, 10 mo

14

M

9 y, 10 mo

15

M

9 y, 11 mo

16

F

9 y, 11 mo

17

M

10 y, 2 mo

18

Level

A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C A B C

Per slice

Mean

79.5 99.3 61.7 68.0 71.4 73.7 55.9 79.9 0.0 99.0 96.3 97.8 61.8 79.2 83.4 31.9 13.1 4.6 100.0 94.5 93.3 76.6 79.5 59.7 21.4 48.8 63.2 0.6 3.6 44.3 39.2 67.0 61.9 54.4 91.6 95.6 86.8 85.2 71.6 96.6 71.9 63.5 1.6 26.5 68.6 0.0 5.9 3.4 55.9 64.5 66.0 82.9 92.1 63.1

80.2

14

Rank

71.0

9

45.3

6

97.7

18

74.8

11

16.5

3

95.9

17

71.9

10

44.5

5

16.2

2

56.0

7

80.5

15

81.2

16

77.3

12

32.2

4

3.1

1

62.1

8

79.4

13

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ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY August 2001

In the present study, no significant differences between early and late secondary bone grafting results were found in unilateral cases. This may be because in the early secondary group the teeth, in most cases, did not jet erupt through the graft, which is actually the main difference between the early group and the late group. Careful interpretation of the results with respect to the number of patients indicates that in both bilateral groups the amount of bone remaining in the alveolar cleft after 1 year is less than the amount remaining in the unilateral groups. The number of patients in the bilateral groups is too small to perform formal significance testing; therefore, no conclusion with respect to significant differences in the amount of bone remaining in the alveolar cleft after early secondary bone grafting and after late secondary bone grafting can be drawn. Bergland et al5 reported 4 failures (out of a group of 41 bilateral cases) of late secondary bone grafting after eruption of the permanent canine, indicating that the difference in success between early and late secondary bone grafting can best be explained by the additional bone formation that takes place when the canine erupts into the grafted area in the early secondary bonegrafted children. Differentiation between horizontal and vertical bone resorption is described by Witsenburg and Freihofer7 by using intraoral radiographs. Witsenburg8 also states that results are not easily compared because one author considers bone grafting successful if oronasal fistulas do not reoccur,9 although the bone graft has disappeared almost completely, whereas another author regards such a result a failure. This disparity indicates the need for objective and reliable evaluation methods. If a cleft palate team wants to change their protocol with respect to the many factors involved, they should begin by evaluating their long-term follow-up results in large patient groups. Thereafter, clinical trials should be set up. The most important factor in evaluating treatment results is a reliable representative evaluation method. The present CT scanning technique gives researchers the ability to determine bone quantities at different axial levels. However, objections can be made to the use of CT scans because of the relatively high dose of radiation involved. We chose to use CT scans to evaluate the results of bone grafting in this investigation on the basis of the following considerations: • CT scans visualize the bone graft in 3 directions and also provide information on the amount of bone in the buccopalatal direction. • A high level of standardization can be achieved. • The size of the defect and the position of teeth in

the area can be assessed with more accuracy. This can be considered as an additional advantage for both surgeon and orthodontist. • Comparison of treatment results from different cleft palate teams can only be done properly if researchers can reach agreement on the methodology. It must be emphasized that although CT scans are useful for research purposes, this technique should not be used on a regular basis. It was shown that in unilateral cases, approximately 70% of the bone transplanted from the iliac crest to the alveolar cleft was still present after 1 year. This indicates that a sufficient amount of bone was present in the target area. No difference was found between early and late secondary bone grafting. In the bilateral cases, an average of 45% of the transplanted bone from the iliac crest to the alveolar cleft was found after 1 year. The resorption of transplanted bone might occur because of tension in mucoperiosteal flaps resulting in inadequate covering of the graft.1,5,10-12 The absence of functional stress on the bone due to agenesis of teeth in the area and the size of the defect have an additional negative effect. Although the presence of an adequate amount of bone to unite the greater and the lesser alveolar segment is of importance, this only represents a part of the overall management of cleft lip and palate patients. Other factors such as morbidity, hospitalization time, normal maxillary development, and spontaneous eruption of the permanent canine without complications are important as well.

REFERENCES 1. Enemark H, Sindet-Pedersen S, Bundgaard M. Long-term results after secondary bone grafting of alveolar clefts. J Oral Maxillofac Surg 1987;45:913-9. 2. Prahl-Andersen B, Lijten WJ. Secondary bone transplantation in cleft lip and palate cases. NVOS. 3. Sjölien T, Zachrisson BU. A method for radiographic assessment of periodontal bone support following orthodontic treatment. Scand J Dent Res 1973;81:210-7. 4. Van der Meij AJW, Baart JA, Prahl-Andersen B, Valk J, Kostense PJ, Tuinzing DB. The use of CT-scan in the evaluation of early secondary bone grafting. Int J Oral Maxillofac Surg 1994;23:132-6. 5. Bergland O, Semb G, Abyholm F, Borchgrevink H, Eskeland G. Secondary bone grafting and orthodontic treatment in patients with bilateral complete clefts of the lip and palate. Ann Plast Surg 1986;17:460-74. 6. Felix-Schollaart B. Solitary, non-syndromic cleft lip and/or palate; a comparison between Cleft lip, Cleft lip and palate and Cleft palate on epidemiologic characteristics and growth [thesis]. Free University Hospital Amsterdam; 1989. 7. Witsenburg B, Freihofer HPM. Autogenous rib graft for reconstruction of alveolar bone defects in cleft patients: long-term follow-up results. J Craniomaxillofac Surg 1990;18:55-62. 8. Witsenburg B. The reconstruction of anterior residual bone

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defects in patients with cleft lip, alveolus and palate: a review. J Maxillofac Surg 1985;13:197-208. Schultz RC. Cleft palate fistula repair. Improved results by the addition of bone. J Craniomaxillofac Surg 1989;17(Suppl 1):34-6. Bergland O, Semb G, Abyholm F. Elimination of residual alveolar cleft by secondary bone grafting and subsequent orthodontic treatment. Cleft Palate J 1986;23:175-205. Enemark H, Krantz-Simonsen E, Schramm JE. Secondary bone grafting in unilateral cleft lip palate patients: indications and treatment procedure. Int J Oral Surg 1985;14:2-10. Lilja J, Moller M, Friede H, Lauritzen C, Petterson LE,

Johanson B. Bone grafting at the stage of mixed dentition in cleft lip and palate patients. Scand J Plast Reconstr Surg Hand Surg 1987;21:73-9.

9. 10. 11. 12.

Reprint requests: J. A. Baart, DMD Academisch Ziekenhuis Vrije Universiteit Afdeling mondziekten en kaakchirurgie Postbus 7057 1007 MB Amsterdam The Netherlands

Abstract Long-term follow-up on keratocysts treated according to a defined protocol P. J. W. Stoelinga International Journal of Oral and Maxillofacial Surgery 2001;30:14-25. A prospective evaluation of 82 patients with odontogenic keratocysts (OKCs) was conducted over a 25-year period. For the 60% of patients whose diagnosis was made before definitive surgery and who had mandibular lesions, a defined protocol was used to manage the cyst. The protocol involved nucleation of the cyst and overlying mucosa, followed by the application of Carnoy’s solution (a chemical cauterizing agent). The cystic defect was then packed with gauze soaked with Whitehead’s varnish, and the packing was changed weekly until the defect was fully epithelialized and no longer retained any packing. The article describes the demographics of and the patterns of cyst distribution in the total patient group. Patients in whom the diagnosis of OKC was made only after nucleation did not have overlying mucosa removed or Carnoy’s solution applied. Carnoy’s was only used for maxillary OKCs if the cystic defect was not adjacent to the maxillary sinus. In the 44 cases in which overlying mucosa was excised during nucleation, 23 were found to contain epithelial islands and 11 contained microcysts. Six patients in whom the specific protocol was not used had recurrent OKCs, whereas there were only 3 recurrences in patients receiving protocol-driven care. Recurrences often developed 6 or more years after nucleation and were found as long as 16 years later. The author concludes that by following the defined protocol used in this study the recurrence rate of OKCs is significantly reduced and if further surgery is ever needed, the extent of that surgery is more limited. James R. Hupp DMD, MD, JD, MBA