ORIGINAL ARTICLE

Condylar and ramal vertical asymmetry in adolescent patients with cleft lip and palate evaluated with cone-beam computed tomography
Mevlut Celikoglu,a Koray Halicioglu,b Suleyman K. Buyuk,c Ahmet E. Sekerci,d and Faruk I. Ucare Trabzon, Bolu, and Kayseri, Turkey

Introduction: The aims of this study were to evaluate condylar and ramal mandibular vertical asymmetry in a patient group affected by unilateral (UCLP) and bilateral (BCLP) cleft lip and palate, and to compare the ndings with a well-matched control group with normal occlusion. Methods: The study groups included 20 UCLP patients (12 male, 8 female), 21 BCLP patients (12 male, 9 female), and a control group of 21 subjects with normal occlusion (10 male, 11 female). Measurements of condylar, ramal, and condylar plus ramal heights and asymmetry indexes were examined on cone-beam computed tomography images. One-way analysis of variance was used to determine potential statistical differences among the groups for condylar, ramal, and condylar plus ramal asymmetry index measurements. The post-hoc Tukey HSD test was used to determine individual differences. Results: No investigated group showed a statistically signicant sex difference for any asymmetry index (P .0.05). There was a statistically signicant difference between the normal and cleft sides in the ramal height and ramal plus condylar height measurements in the UCLP group (P 5 0.004 and P 5 0.006, respectively). The Tukey HSD test showed a statistically signicant difference between the UCLP and BCLP groups in terms of ramal asymmetry index values (P 5 0.018). Conclusions: The ramal height and ramal plus condylar height measurements were signicantly lower in the cleft side in the UCLP patients, and there was a statistically signicant difference in ramal asymmetry index values between the patients affected by UCLP and BCLP. (Am J Orthod Dentofacial Orthop 2013;144:691-7)

atients affected by cleft lip and palate (CLP) exhibit different growth patterns of the dentomaxillofacial tissues than do their normal peers1 and commonly have anterior and posterior crossbite tendencies caused by scarring.2 The crossbite side, especially unilateral posterior crossbite, is related to
a Associate professor, Department of Orthodontics, Faculty of Dentistry, Karadeniz Technical University, Trabzon, Turkey. b Assistant professor, Department of Orthodontics, Faculty of Dentistry, Abant _ Izzet Baysal University, Bolu, Turkey. c Research assistant, Department of Orthodontics, Faculty of Dentistry, Erciyes University, Kayseri, Turkey. d Assistant professor, Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Erciyes University, Kayseri, Turkey. e Private practice, Kayseri, Turkey. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conicts of Interest, and none were reported. Address correspondence to: Mevlut Celikoglu, Department of Orthodontics, Faculty of Dentistry, Karadeniz Technical University, Trabzon, Turkey; e-mail, mevlutcelikoglu@hotmail.com. Submitted, February 2013; revised and accepted, July 2013. 0889-5406/$36.00 Copyright 2013 by the American Association of Orthodontists. http://dx.doi.org/10.1016/j.ajodo.2013.07.009

asymmetrical muscular function.3 Prolongation of abnormal muscular functions can cause changes in the growth center at the temporomandibular joint4 because the condyle is one of the most sensitive areas to occlusal changes.5 Some studies6,7 have reported mandibular asymmetry in patients affected by CLP, whereas others,8-10 through the use of different radiographs and assessment techniques, have claimed that patients affected by CLP have no asymmetric mandible. For the rst time reported in the literature, Habets et al11,12 applied a method to assess vertical mandibular asymmetry. This new method, which compares the vertical height of the right and left condyles and rami, has been used by some researchers to compare condylar asymmetry in unilateral13,14 and bilateral14,15 posterior crossbite patients, patients with temporomandibular disorders,11 early bilateral rst molar extraction patients,16 and patients with Class II17,18 and Class III18,19 malocclusions. Recently, Kurt et al20 found no statistically signicant differences among unilateral (UCLP) and bilateral
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(BCLP) cleft lip and palate groups and a control group with normal occlusion, using the method of Habets et al.11,12 All of these mentioned studies on vertical mandibular asymmetry were performed with panoramic radiographs, which enable scanning of end-to-end structures of the entire dental system with relatively limited radiation doses and reduced nancial costs to patients and health service providers.21,22 Nevertheless, there are some disadvantages to panoramic radiographs, such as inconstant magnication, image distortion, and vertical measurements that might be affected by the patient's head position.23 However, cone-beam computed tomography (CBCT) technology makes it feasible to achieve true (1:1 size) images without magnication and with a relatively lower radiation dose and lower cost than with computed tomography.24,25 Although studies on vertical condylar asymmetry have increased in recent years, to date, no study has been done with CBCT images to investigate condylar asymmetry in groups of UCLP and BCLP patients and compare them with a normal occlusion sample. Therefore, in this study, we aimed to determine whether there is an increase in condylar asymmetry associated with patients affected by UCLP and BCLP compared with an unaffected control population, using CBCT images according to the method described by Habets et al.11,12
MATERIAL AND METHODS

This study was carried out on the CBCT radiographs selected from the archives of the Departments of Oral and Maxillofacial Radiology and Orthodontics of the Faculty of Dentistry, Erciyes University, Kayseri, Turkey. The CBCT scans of the patients included in this study were part of the diagnostic records collected for patients with impacted teeth or those who required orthodontic treatment; the patients were not exposed to any additional radiation. Therefore, approval from the ethics committee was not required for this retrospective archive study. In addition, as a usual protocol, all patients (or parents) signed an informed consent agreeing to the use of the patients' data for scientic studies. The patients were divided into 3 groups: (1) 20 patients (12 male, 8 female) affected by UCLP, (2) 21 patients (12 male, 9 female) affected by BCLP, and (3) 21 patients (10 male, 11 female) as the control group. Subjects in the control group with normal occlusion met the following criteria, as suggested by Kurt et al20: (1) Class I canine and molar relationships with minor crowding, normal growth, and normal development, including normal skeletal relationship and facial balance; (2) all teeth present

except third molars; (3) no history of trauma, previous orthodontic or prosthodontic treatment, or maxillofacial surgery; and (4) no signicant medical history. All images were obtained with the patient in the supine position using CBCT (NewTom 5G; QR srl, Verona, Italy). Scanning time was 18 seconds, collimation height was 13 cm, exposure time was 3.6 seconds, and voxel size was 0.3 mm3. Digital Imaging and Communications in Medicine (DICOM) les obtained from the CBCT scans were reconstructed using NNT viewer software (QR S.r.l., Verona, Italy). All measurements were made by 1 author (S.K.B.). In addition, the cervical vertebra maturation stages of all patients were determined according to the method of Hassel and Farman.26 On both sides, the most posterior points of the condyle and ramus of the mandible were marked as the X and Y points. A line was drawn through X and Y and called the A-line. Another line, called the B-line, was drawn from the most superior points of the condyle perpendicular to the A-line. The conuence of the A-line and B-line was called point Z. The distance between points X and Z was measured as condylar height. In addition to this measurement, the distance between X and Y and the distance between Z and Y were measured as ramus height and condylar plus ramus height, respectively (Fig). Finally, the vertical mandibular asymmetry indexes of the condyle, ramus, and condyle plus ramus were calculated using the following formula, developed by Habets et al11,12: Asymmetry index (%): [(Right Left)/ (Right 1 Left)] 3 100
Statistical analysis

Two weeks after the rst measurements, 20 randomly selected CBCT images were retraced and remeasured by the same author. The method error coefcient was calculated with Dahlberg's formula.27 Dahlberg's method error values were within acceptable limits (range, 0.409-0.954). In addition, the difference between the 2 tracings was tested for signicance with a paired t test; no signicant difference was found (P .0.05), conrming the intraobserver reliability of the measurements. Data regarding the asymmetry measurements were computed. The normality test of the Shapiro-Wilks and the Levene variance homogeneity test were applied to the data; all data were found to be normally distributed. Thus, the comparisons among the groups and sexes were analyzed using parametric tests. The Student t test was used to compare the sexes, and 1-way analysis of variance (ANOVA) was used to compare the asymmetry indexes among the UCLP, BCLP, and control groups. The

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Fig. Measuring method according to Habets et al.11,12 Table I. Demographic features of the patients in cleft and normal groups
Cervical vertebral maturation (CVM) stage Group UCLP Sex Male Female Total Male Female Total Male Female Total Age (y) 15.49 6 3.84 12.42 6 3.36 14.26 6 3.88 14.38 6 2.48 14.63 6 2.59 14.49 6 2.47 13.85 6 2.22 14.69 6 2.26 14.29 6 2.23 NS Number 12 8 20 12 9 21 10 11 21 NS Sex comparison NS UCB 3 2 5 4 3 7 0 0 0 BCB 2 1 3 6 4 10 0 0 0 1 2 4 6 3 0 3 0 0 0 2 3 0 3 2 1 3 2 1 3 3 2 3 5 2 1 3 1 2 3 4 1 0 1 3 1 4 4 4 8 5 2 0 2 1 2 3 3 2 5 6 2 1 3 1 4 5 0 2 2

BCLP

NS

Normal occlusion

NS

Group comparison

UCLP, Unilateral cleft lip and palate; BCLP, bilateral cleft lip and palate; UCB, unilateral crossbite; BCB, bilateral crossbite; NS, not signicant. CVM stages according to Hassel and Farman26: CVM1, initiation of adolescent growth; CVM2, acceleration of adolescent growth; CVM3, transition of adolescent growth; CVM4, deceleration of adolescent growth; CVM5, maturation of adolescent growth; CVM6, completion of adolescent growth.

Tukey HSD post-hoc test was performed to determine individual differences. In addition, a paired t test was used to determine possible statistical differences between the sides for condylar height, ramal height, and condylar height plus ramal height measurements in all groups. All statistical analyses were performed with SPSS software (version 15.0 for Windows; SPSS, Chicago, Ill); P \0.05 was considered statistically signicant.
RESULTS

Table I shows descriptive data of the patients in the study. Sex distribution and chronologic ages in all

groups were well matched (tested by chi-square and 1way ANOVA, respectively; P .0.05 for both tests). The chronologic ages of the patients affected by UCLP and BCLP and the normal occlusion controls were 14.26 6 3.88, 14.49 6 2.47, and 14.29 6 2.23 years, respectively. The descriptive mandibular asymmetry indexes for both sexes were calculated separately in the normal occlusion and CLP patient groups to investigate the relationship between the sexes. Because no statistically signicant differences were found for these mean values, the data were pooled for further analyses (Table II).

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Table II. Comparison of mandibular asymmetry indexes between the sexes

Male (n 5 34) Group UCLP (n 5 20) (F/M, 8/12) BCLP (n 5 21) (F/M, 9/12) Normal occlusion (n 5 21) (F/M, 11/10) Variable (%) CAI RAI CRAI CAI RAI CRAI CAI RAI CRAI Mean 10.87 4.30 3.83 8.81 1.53 1.47 11.00 2.50 1.98 SD 8.89 5.73 5.50 8.36 1.85 1.57 11.68 1.21 1.75 Female (n 5 28) Mean 11.59 3.72 2.90 6.88 1.49 1.63 13.12 2.48 2.19 SD 7.57 2.29 1.70 7.95 1.89 1.81 7.76 1.16 1.64 P 0.851 0.791 0.649 0.598 0.954 0.827 0.627 0.970 0.788

UCLP, Unilateral cleft lip and palate; BCLP, bilateral cleft lip and palate; CAI, condylar asymmetry index; RAI, ramal asymmetry index; CRAI, condylar plus ramal asymmetry index; F/M, female/male ratio; P, results of Student t test comparing the sexes.

Table III. Comparison of the height measurements for sides in the normal, UCLP, and BCLP groups
UCLP Normal side Variable CH RH CH 1 RH Mean (mm) 3.41 6 0.95 42.70 6 5.63 46.11 6 6.01 Cleft side Mean (mm) 3.56 6 0.84 40.24 6 6.76 43.80 6 7.19 P 0.489 0.004 0.006 Right side Mean (mm) 3.41 6 0.72 39.34 6 3.79 42.75 6 3.99 BCLP Left side Mean (mm) 3.66 6 0.81 39.42 6 3.41 43.08 6 3.98 P 0.148 0.839 0.442 Normal occlusion Right side Mean (mm) 4.41 6 0.89 42.67 6 4.76 47.08 6 5.11 Left side Mean (mm) 4.01 6 0.83 42.07 6 5.26 46.08 6 5.54 P 0.156 0.252 0.054

UCLP, Unilateral cleft lip and palate; BCLP, bilateral cleft lip and palate; CH, condylar height; RH, ramal height; CR 1 RH, condylar plus ramal height; P, results of paired-samples t test.

Means, standard deviations, and statistical results of paired t tests comparing the condylar height, ramal height, and condylar height plus ramal height measurements of the normal and cleft sides in the UCLP group, and the left and right sides in the BCLP and the normal occlusion groups are shown in Table III. There were no statistically signicant differences in the condylar height, ramal height, and condylar height plus ramal height measurements between the right and left sides in the BCLP and control groups; however, there were statistically signicant differences in ramal height and condylar height plus ramal height measurements between the normal and cleft sides in the UCLP groups (P 5 0.004 and P 5 0.006, respectively). The ramal height values were 42.70 6 5.63 mm in the normal side and 40.24 6 6.76 mm in the cleft side; the condylar height plus ramal height values were 46.11 6 6.01 mm in the normal side and 43.80 6 7.19 mm in the cleft side. The results of the ANOVA showed no statistically signicant differences in the condylar asymmetry index or the condylar plus ramal asymmetry index measurements among the groups, whereas the ramal asymmetry index was statistically signicantly different (P 5 0.023). The Tukey HSD test showed a statistically

signicant difference in the ramal asymmetry index between the UCLP and BCLP groups (P 5 0.018). The ramal asymmetry index values were 4.07% 6 4.59% in the UCLP group and 1.52% 6 1.82% in the BCLP group (Table IV).
DISCUSSION

Panoramic lms have often been used by investigators who performed condylar13-20,28 and mandibular29,30 asymmetry studies. However, CBCT is the most accurate and most reliable available technique for determination, without magnication of asymmetries10,24,31 and with a relatively low radiation dose and relatively low cost.11,30 Two-dimensional data obtained from CBCT are more reliable than conventional 2-dimensional radiographs in terms of magnication. Thus, in our study, CBCT images were used for the assessment of mandibular vertical asymmetry. This study is the rst in the literature to use CBCT to investigate vertical condylar and ramal asymmetry with the method of Habets et al11,12 in patients affected by UCLP and BCLP. The reproducibility of vertical measurements on panoramic lms is admissible if the patient's head is correctly positioned in the cephalostat.32 According to Habets et al, a 3% index ratio can result from a 1-cm

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Table IV. Comparisons of mandibular asymmetry index values among the groups
Asymmetry index CAI Group UCLP BCLP Normal occlusion UCLP BCLP Normal occlusion UCLP BCLP Normal occlusion n 20 21 21 20 21 21 20 21 21 Mean (%) 11.16 6 8.18 7.98 6 8.04 12.11 6 9.63 4.07 6 4.59 1.52 6 1.82 2.49 6 1.16 3.46 6 4.33 1.54 6 1.64 2.09 6 1.66 P 0.280 G1-G2 .474 G1-G3 .934 G2-G3 .278

RAI

0.023

0.018

.197

.525

CRAI

0.089

.082

.273

.800

UCLP, Unilateral cleft lip and palate and (G1); BCLP, bilateral cleft lip and palate and (G2); G3, normal occlusion; CAI, condylar asymmetry index; RAI, ramal asymmetry index; CRAI, condylar plus ramal asymmetry index; P, results of 1-way ANOVA comparing the 3 groups.

change in head position while the panoramic lm is being taken; thus, asymmetry index (condylar asymmetry, ramal asymmetry, and condylar plus ramal asymmetry indexes) values greater than 3% should be approved as posterior mandibular vertical asymmetry. In this study, we examined this hypothesis because the patient's head position is not an assessment criterion when using CBCT. The condylar asymmetry index values of all groups were high (control group, 12.11% 6 9.63%; UCLP, 11.16% 6 8.18%; BCLP, 7.98% 6 8.04%) when compared with the 3% threshold value of Habets et al.11,12 Turp et al33 mentioned that mild condyle and ramus asymmetries are part of the biologic variations of humans. Nevertheless, all patients in this study, both with and without CLP, had severely asymmetric mandibles according to the condylar asymmetry index measurements. Furthermore, Uysal et al,14 Halicioglu et al,16 Saglam,18 and Kurt et al20 found condylar asymmetry index values of 7.57% 6 8.39%, 7.04% 6 6.79%, 7.96% 6 6.73%, and 9.95% 6 10.42%, respectively, in their normal occlusion groups. These studies have similarly high condylar asymmetry index values, even though they were performed using panoramic lms. Therefore, investigators who are interested in condylar asymmetry should revise the 3% condylar asymmetry index threshold value of Habets et al.11,12 Kurt et al20 reported that the ramal height and condylar height plus ramal height measurements of their CLP patient groups were approximately 10 mm greater than those of a peer control group with normal occlusion, and they observed that there were statistically signicant condylar height differences in the BCLP patients. We need to take into account condylar asymmetry studies performed on patients with posterior crossbites because patients affected by CLP commonly have unilateral or bilateral posterior crossbites. Most of the patients in our study had unilateral or bilateral posterior crossbites (Table I). Kilic et al15

reported that condylar height, ramal height, and condylar height plus ramal height measurements on the unilateral crossbite side were smaller than those on the noncrossbite side. However, Kiki et al13 and Uysal et al14 found no signicant differences between the right and left sides in the bilateral posterior crossbite group. In our study, condylar height, ramal height, and condylar height plus ramal height measurements were close to each other in both sides of all groups except the UCLP group. Ramal height and condylar height plus ramal height measurements were statistically lower in the cleft side of the UCLP groups when compared with the normal side. In addition, the cleft sides in the UCLP and BCLP groups were approximately 2.5 to 3 mm smaller when compared with the normal sides in the UCLP and control groups. This nding is interesting when compared with the ndings of Kurt et al, who stated that the ramal height and condylar height plus ramal height measurements of their CLP patients were approximately 10 mm greater than those of patients with normal occlusion. We think that this difference between our study and that of Kurt et al is due to the use of panoramic lms in their study and CBCT in our study. In another study performed with CBCT, Veli et al10 reported that ramal heights measured using different anatomic landmarks did not show statistically signicant differences between sides in their UCLP and normal occlusion groups. We attribute the differences between our results and those of earlier studies to the use of different landmarks for ramal-height assessment.10,24 The method we used is different in that it actually undermeasures the full condylar height and overmeasures the actual anatomic ramus. In addition, a recent study of unilateral crossbite patients reported a statistically signicant decrease in the crossbite sides compared with the normal sides.15 This agrees with our ndings because unilateral crossbite is almost always seen in UCLP patients.

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Kurt et al20 found no statistically signicant differences in condylar asymmetry, ramal asymmetry, or condylar plus ramal asymmetry index values among the UCLP, BCLP, and control groups. In our study, no statistically signicant differences in the condylar asymmetry index or condylar plus ramal asymmetry index values were found. However, we found a statistically signicant difference in the ramal asymmetry index between the UCLP and BCLP groups. The differences between our ndings and those of Kurt et al might be due to the different lm techniques used in the studies because CBCT images provide more valuable information than do panoramic lms. It is difcult to compare our ndings with those of previous studies of patients affected by CLP to determine condylar asymmetry because no studies have investigated condylar asymmetry in CLP patients with 2-dimensional data obtained from CBCT and the method of Habets et al.12
CONCLUSIONS

1.

2.

3.

4.

The condylar asymmetry index values of all groups were signicantly higher when compared with the 3% threshold value of Habets et al,11,12 but comparisons among the groups were not statistically signicant. Therefore, the 3% threshold value for the condylar asymmetry index measurement must be examined further. There were statistically signicant differences in the ramal height and condylar height plus ramal height measurements between the normal and cleft sides of the UCLP group (P 5 0.004 and P 5 0.006, respectively). The ramal asymmetry index values of the patients affected by UCLP and BCLP were statistically different (P 5 0.018). Further investigations with larger samples, evaluated in 3 dimensions, and correlating with occlusal asymmetry are needed to conrm the results of this study.

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