Changes in temporomandibular joint after mandibular subcondylar osteotomy: An experimental study in rats

SCIENTIFIC ARTICLES J Oral Maxillofac Surg 51:1221·1234,1993

Changes in Temporomandibular Joint After Mandibular Subcondylar Osteotomy: An Experimental Study in Rats FLORENCIO MONJE, MD,* EMILIO DELGADO, MD,t MARTIN J. NAVARRO, MD,:f: CELIA MIRALLES, MD,§ AND JOSE R. ALONSO DEL HOYO, MD, DMDII The objective of this study was to analyze the changes in the different components of the temporomandibular joint and their relation with age after subcondylar osteotomy. For this purpose 149 Wistar rats were divided into three groups: osteotomy, sham operation, and control. Two experimental ages (30 and 70 days) and radiologic, morphometric, macroscopic, and histologic methods of analysis were used. Different changes were observed in young and adult animals. Subcondylar mandibular osteotomy in growing rats caused anteroinferior displacement of the temporal and mandibular component of the joint. At the end of the experimental period only condylar displacement was maintained. Other changes were flattening of the mandibular condyle, which was transient, and lateral thickening of the articular disc. SUbcondylar mandibular osteotomy in adult rats caused slight anterior displacement of the joint components at the end of the experimental period. At this age, although changes similar to those in growing animals were observed in some cases, in other cases the presence of pathologic findings, such as deformation of the condylar cartilage, thickening of the disc, intra-articular adherences, and osteolysis of the temporal fossa, were observed. Changes in the joint components were more marked in growing rats than in adults. In growing rats they affected the form of the condylar process to a greater extent, but the majority of these changes were transient. In adult rats, alterations in the joints were less pronounced, but they affected a greater number of joint components and were permanent.

fossa. In 66% of patients who present with symptoms/ signs oftemporomandibular dysfunction before surgery on facial deformities, an improvement is observed after surgery. 1 Certain investigatorsi" even prescribe the use of the subcondylar osteotomy as a surgical treatment for patients with TMJ dysfunction. Using condylar path tracing, Harper' showed an improvement in articular function in 28% of patients who had TMJ dysfunction before orthognathic surgery. However, the appearance of the symptoms ofTMJ dysfunction in patients who had undergone corrective surgery for dentofacial deformities, and who did not have symptoms before surgery, should be noted. The rate of such TMJ dysfunction after mandibular osteotomies varies between 3.7%6 and 44%.7 Several investigators.v'? using different radiographic projections, have studied the movements ofthe condyle which occur in patients who have undergone orthognathic surgery. A number of experimental studies describe the changes in position 11.12 or in metabolism 13,14 of the condyle after mandibular osteotomies. However,

Different types of facial deformities exist that may be corrected through maxillary and/or mandibular osteotomies. Mandibular osteotomies are performed close to the temporomandibular joint (TMJ) and may alter the relation between the condyle and the temporal

* StalfSurgeon, Department of Maxillofacial Surgery, La Princesa Hospital, Madrid, Spain; Research Associate, Laboratory of Experimental Microsurgery, La Paz Hospital, Madrid. t Orthopaedic Research; Head, Laboratory of Experimental Microsurgery, La paz Hospital, Madrid. Research Associate, Laboratory of Experimental Microsurgery, La Paz Hospital, Madrid; in private practice in Orthodontics. § Research Associate, Laboratory of Experimental Microsurgery, La Paz Hospital, Madrid . •11 Head, Department of MaxillofacialSurgery, La Princesa Hospital, Madrid. Professor, Department of Surgery, Autonoma University, Madrid. Address correspondence and reprint requests to Dr Monje: Department of Maxillofacial Surgery, Hospital La Princesa, Diego de Leon, 62, 28006 Madrid, Spain.

*

© 1993 American Association of Oral and Maxillofacial Surgeons 0278-2391/93/5111-0010S3.00/0

1221

1222

CHANGES IN TMJ AFTER OSTEOTOMY

no studies exist in which the changes in all TMJ components were examined after mandibular osteotomy, and there has been no homogeneity in regard to experimental age. The objective of this study was to analyze the influence of the mandibular subcondylar osteotomy on the different components of the rat TMJ and to evaluate the relation between the morphologic articular changes, should they occur, and injury age and evolution time.

Materials and Methods One hundred forty-nine male Wistar rats were divided into three groups: osteotomy, sham operation, and control. The animals were anesthetized with a mixture of 50 mg of ketamine, 20 mg of diazepam, and 1 mg ofatropine using I mll 100 g ofbody weight. For the osteotomy, a cutaneous incision was made in front of the external auditory canal. Blunt dissection was performed on the masseter muscle fibers between the lower edge of the zygomatic arch and the upper ramus of the facial nerve as far as the condylar neck, and an osteotomy was performed with a surgical drill. The condylar fragment was placed external to the mandibular ramus. Care was taken not to damage the joint or the blood vessels posterior to the mandibular condyle. To take into account the effects of surgical trauma, a second group was submitted to sham surgery in which the incision and dissection were identical to that ofthe osteotomy group, but the condylar neck was not fractured. A third group served as a control and did not undergo surgery. The animals underwent surgery at 30 days (young or growing animals) or 70 days (adult animals) of age. The animals undergoing surgery at 30 days were killed at 20 or 40 days after surgery (50 or 70 days of age, respectively), and the animals undergoing surgery at 70 days were killed at 30 or 60 days after surgery (100 or 130 days of age, respectively). The animals were killed using an overdose of ether. Animals with facial asymmetry, abnormal occlusion, infection of the surgical wound, or large weight loss were rejected. RADIOLOGIC AND MORPHOLOGIC METHOD

Cranial Measurements On a lateral radiograph of the cranium (focus film distance 40 em , 25 kw voltage, 40 sec exposure) the following parameters were defined (Fig I): Tl, hindmost point of the condyle to the perpendicular projection on the palatal plane; T2, uppermost point of the condyle to the perpendicular projection on the palatal plane; T3, anterior extreme of the temporal fossa to the perpendicular projection on the palatal plane; T4, hindmost point of the condyle to the anteriormost

FIGURE I.

Measurements made on lateral cranial radiographs.

point of the maxilla; T5, uppermost point of the condyle to the anteriormost point of the maxilla; T6, anterior extreme of the temporal fossa to the anteriormost point of the maxilla; T7 , incisor ridge; T8, cranial length; T9, angle between the palatal and occlusal planes; and T 10, angle between the palatal and mandibular planes.

Mandibular Measurements On a lateral radiograph of the mandible (40cm, 25 kw, 40 sec) the following parameters were defined (Fig 2): M I, posterosuperior point of the condyle to the mental foramen; M2, deepest point of the sigmoid notch to the mental foramen; M3, deepest point of the mandibular notch to the mental foramen; M4, end of the coronoid apophysis to the mental foramen; M5, point of the angle process to the mental foramen; M6, posterosuperior point of the condyle to the extreme anterior ofthe alveolar bone; M7, posterosuperior point of the condyle to the point of the incisor crown; M8, posterosuperior point of the condyle to the pre-angle notch; M9, sigmoid notch to the pre-angle notch; MIO, uppermost point of the condyle to the perpendicular projection on the mandibular plane; Mil, length of the incisor crown; M 12, anteroposterior length of the condyle; Angle B-M, between the tangent of the posterior edge of the condyle and the mandibular plane; Angle V-M, between the plane of the inferior dental vasculonervous canal and the mandibular plane; Angle C-M, between the axis of the condyle and the mandibular plane; and Angle CA-M, between the tangent to the hindmost points of the angular and condylar processes and the mandibular plane.

Joint Measurements On the anteroposterior radiograph of a frontal cranial section of 6-0101 thickness that contained both

1223

MONJE ET AL

plane perpendicular to X, which passed through the hindmost point of the condyle, was considered as the Y-axis. The distance from the X-axis to the anterior and posterior edge of the condyle was measured each 3 mm and analyzed statistically to obtain a visual image of the condylar profile for each group. MORPHOLOGIc-MACROSCOPIC METHOD

FIGURE 2. Measurements made on lateral mandibular radiographs.

joints, the following measurements were taken (Fig 3): a I, internal articular space; a2, superior articular space; a3, external articular space; a4, condylar width; a5, width of the condylar neck; a6, distance between the most external and internal point of the temporal fossa; a7, thickness of the zygomatic arch; a8, length of the zygomatic arch; a9, distance between condyles; atO, angle between the axis ofthe mandible ramus (M) and the plane of the cranial base (X); a II, angle between the internal wall of the temporal fossa (T) and the plane of the cranial base; a12, angle between the tangent to the uppermost and outermost points of the temporal component of the joint (Z) and the plane of the cranial base; and a 13, angle between the zygomatic arch plane (Z') and the cranial base plane.

The joints were dissected and the characteristics of joint mobility, joint capsule, articular disc, and the condylar and temporal surfaces were described. HISTOLOGIC METHOD

The entire TMJ region was placed in formalin. After routine fixation, demineralization, dehydration, and paraffin-wax embedding, 5-Jlm-thick sections were cut in the coronal plane and stained with hematoxylineosin. STATISTICAL METHOD

All the quantitative variables were analyzed using the Mann-Whitney U test. In half the animals the morphometric (lateral radiograph of the cranium and mandible), planimetric, and morphologic method was performed and in the other half the morphometric (TMJ anteroposterior radiograph) and histologic method was used.

PLANIMETRIC METHOD

On a lateral radiograph of the mandible, the mandibular base plane was considered as the X-axis and a

Results OSTEOTOMY PERFORMED AT 30 DAYS OF AGEANIMALS KILLED AT 20 DAYS

In the lateral radiograph of the cranium a decrease in the perpendicular distance of the condylar points Table 1. Lateral Cranial Radiographs (Morphometry) 20 Days Postoperatively (Surgical Procedure Performed at 30 Days of Age)

Parameter TI

T2 T3 T4 T5 T6 T7 T8 T9 TIO

FIGURE 3. Measurements made on anteroposterior TMJ radiographs.

Control (n = 6)

Subcondylar Osteotomy (n = 6)

Sham Operation (n = 4)

3.24 ± 0.34 4.37 ± 0.36 4.92 ± 0.97 25.58 ± 0.65 24.Q4 ± 0.68 23.64 ± 0.64 3.26 ± 0.45 39.04 ± 0.57 7.96 ± 0.32 13.75 ± 1.09

2.27 ± 0.39* 3.32 ± 0.52* 3.95 ± 0.49 23.60 ± 1.07t 22.36 ± 0.95t 21.97 ± 0.96t 3.36 ± 0.15 36.86 ± 1.50* 10.53 ± I.77t 14.50 ± 3.78

2.59 ± 0.62 3.70 ± 0.73 4.30 ± 0.72 24.43 ± 0.88 22.98 ± 0.93* 22.73 ± 0.84 2.88 ± 0.23 37.83 ± 1.09 8.63 ± 0.62 13.90 ± I.IO

Data are mean ± SD. Significancetested with Mann-Whitney U. Sec text for description of parameters. * P,,;; .05. tP:s.OI.

1224

CHANGES IN TMJ AFTER OSTEOTOMY

(TI and T2) and the distance from the condyle and temporal fossa to the maxilla point (T4, T5, and T6) were observed (Fig 4). The palatal-occlusal angle (T9) increased while the palatal-mandibular angle (TlO) did not change (Table I). In the mandible, a decrease in the horizontal (M I, M2, M3, M5, M6, and M7) and vertical mandibular measurements of the ramus (M8 , M9, and M 10) was noticeable. A decrease in the length of the incisor (M II) and the anteroposterior length of the condyle (M 12) also were observed. Only the angle formed by the condyle-angIe axis and the mandibular plane was altered (Table 2; Fig 5A and 6A). In the planimetry, the condyle appeared lower and smaller in size, with a hollow anterior edge (Fig 7A). In the joint morphometry, the internal articular space (al) and the intercondylar distance (a9) decreased, and the external articular space (a3), the width of the condyle (a4), the condylar neck (as), and the total articular space (a6) increased (Fig 4C). The thickness of the zygomatic arch (a7) and its length (a8) also decreased (Table 3). In the dissection, a greatly thickened joint capsule, an articular disc adhering closely to the upper aspect of the condyle, and a rounded condyle were observed. In the histology, a condyle flattened on its external aspect could be observed. The condylar cartilage was decreased in thickness (especially in the hypertrophic Table 2. Lateral Mandibular Radiographs (Morphometry) 20 Days Postoperatively . (Surgical Procedure Performed at 30 Days of Age)

Parameter Length MI M2 M3 M4 M5 M6 M7 M8 M9 MIO MIl MI2 Angle 8·M V·M CA·M CoM

Control (n = 12)

Mandibular Osteotomy (n = 12)

Sham Operation (n = 8)

16.73 ± 11.75 ± 13.45 ± 13.55 ± 16.08 ± 21.50 ± 25.28 ± 11.20 ± 8.33 ± 9.69 ± 5.57 ± 2.73 ±

0.35 0.22 0.34 0.37 0.44 0.33 0.40 0.36 0.23 0.37 0.23 0.18

14.86 ± 0.68* 10.77 ± 0.57* 12.35 ± 0.65* 12.65 ± 0.83 14.71 ±0.93* 19.36 ± 0.82* 23.35 ± 0.83* 9.40 ± 0.70* 7.25 ± 0.45* 8.29 ± 0.56* 5.75 ± 1.33 1.97 ± 0.15*

16.84 ± 0.14 11.68 ± 0.17 13.17 ± O.l4t 13.12 ± 0.27 16.06 ± 0.34 21.53 ± 0.14 25.45 ± 0.06t 11.16 ± 0.26 8.09 ±O.llt 9.44 ± 0.24 5.49 ± 0.12 2.46 ± 0.09*

44.79 ± 17.91 ± 89.75 ± 40.02 ±

4.18 1.12 3.4\ 5.33

46.58 ± \8.25 ± 84.83 ± 43.91 ±

44.25 ± \8.50 ± 91.12 ± 38.75 ±

9.58 2.05 7.65t 9.30

1.46 1.16 3.39 1.62

Data are mean ± SD. Significance tested with Mann-Whitney U. See text for description of parameters. * P s: .001. t p s: .05. * Ps: .01.

layer), but the underlying bone tissue was normal. The disc was thickened in the lateral insertions and the synovia was hypertrophied. There was no inflammation present (Fig 8C, D). OSTEOTOMY PERFORMED AT 30 DAYS OF AGEANIMAL KILLED AT 40 DAYS

In the lateral radiograph of the cranium the horizontal distance from the condylar points to the palatal reference point (T4 and TS) were decreased. The palatal-occlusal angle (T9) increased, but the palatalmandibular angle (T I0) did not vary significantly (T I0, Table 4). In the mandibular morphometry, the same measurements as in the previous group were noted, with the exception of the distance between the angular process and mental foramen (M5), which did not appear reduced. In this group a change in the vasculonervous axis was appreciated (Y-M) , and in the condyle axis angle (CA-M) with respect to the mandibular plane Cfable 5; Figs 5B, 6B). In the condylar planimetry the findings were sim ilar to those observed in the previous group (Fig 7'13'>. In the joint morphometry the same parameters as in the previous group could be seen, but with a less appreciable difference than in the control group (Table 6). Upon dissection, a thinner capsule and less adherence of the articular disc to the condyle than in the previous group was observed. In the histologic examination an increase in the height of the cartilage was noted, with a disc thickened in its lateral portion. The condylar neck was broadened and the synovial membrane showed slight hypertrophia (Fig 9C, D). OSTEOTOMY PERFORMED AT 70 DAYS OF AGEANIMALS KILLED AT 30 DAYS

In the lateral radiograph of the cranium there were no significant differences compared with the control group (Table 7). Upon mandibular morphometry a decrease in some horizontal (M I, M6, and M7) and vertical measurements (M8 and M 10) was observed. The anteroposterior length of the condyle (M 12) appeared reduced and the length of the incisor crown (M II) was increased. In the angular parameters, verticalization of the condyle was noted, since the CoM angle was increased. (Table 8; Fig 6C). In condylar planimetry, the anterior and posterior edges appeared more convex (Fig lOA). In the temporomandibular morphometry the internal articular space (a I) was decreased and the external articular space (a3), condylar thickness (a4), condylar neck thickness (a5), and total articular space (a6) were increased. Angular parameters were not affected, nor was the distance between the condyles (a9, Table 9). Upon dissection, the capsule appeared thickened, joint mobility appeared diminished, and the disc was found to be closely adhered to the condyle. In three

MONJE ET AL

1225

FIGURE 4. Radiographs of 50-day-old animals. A. Lateral cranial radiograph (control group). B. Anteroposterior TMJ radiograph (control group). C. Anteroposterior TMJ radiograph (mandibular osteotomy performed at 30 days of age; animal killed after 20 days) showing increased external articular space twhite arrow), thickened condylar neck (cu), and decreased internal articular space (black arrOlI'). D. Lateral cranial radiograph (mandibular osteotomy performed at 30 days of age; animal killed after 20 days) showing anterior displacement of the TMJ components. Key: c, condyle; 1\1, reference point of the maxilla.

cases a hypertrophic callus was observed, and in one the condyle was indented and there was deformation of the condylar process. Histologically, an increase in the height of the fibrous layer was observed (Fig l1A,

B). In some cases adherence between the condyle and the articular disc could be seen (Fig 11 C, D). In three joints disappearance of chondral tissue and a greatly thickened disc were observed.

FIGURE 5. Mandibles. A. 50 days of age. Top. Control group. BOl/OIII. Mandibular osteotomy performed at 30 days of age; animal killed after 20 days. A decreased articular surface of the mandibular condyle (arro\\' tip), angular process atrophied (white arroll'), and osteotomy callus (black arroll's) could be observed. B. 70 days of age. Top. Control group. BOl/OIII. Mandibular osteotomy performed at 30 days of age; animal killed after 40 days. A deepening of the sigmoid and mandibular notchs (white arrOll's) and decreased articular surface of the mandibular condyle (arrOlI' tip) could be observed.

1226 OSTEOTOMY PERFORMED AT 70 DAYS OF AGEANIMALS KILLED AT 60 DAYS

CHANGES IN TMJ AFfER OSTEOTOMY

MM 90

70 60

so 40

90 80

80

In the lateral radiograph ofthe cranium, the condylar (T4 and T5) and temporal (T6) points were much closer

MM

A .........

-_ .............

70

.... -.... ........ _....

, .'.

'.

---- ....

-

60

~._._._._-

50

.'..:.~>:\

,

40

.'.

30

30

20

20

10

B

'0

30d-50d

MM

3Od-70d

MM

FIGURE 7. Condylar planimetry in young animals. A. 50 days of . . . . , manage. B, 70 days of age. Key: - - • ~ " control; dibular osteotomy; - - , sham operation.

to the palatal reference point (Table 10). In mandibular morphometry a decrease in all horizontal (M I, M2, M3, M5, M6, and M7) and vertical (M8, M9, and M 10) measurements was observed. The anteroposterior length of the condyle (MI2) was reduced, and no significant changes in the length of the incisor crown (Mil) were detected (Table II; Fig 6D). In condylar planimetry, the condyle appeared lower, with a reduced articular surface and an irregular anterior edge (Fig lOB). In joint morphometry the same measurements were altered as in the previous group, with the exception of condylar thickness (a4), which appeared normal (Table 12). In dissection the capsule was thickened. Important deformation was observed in three condyles (Fig 6E). Histologically an increase in the thickness of the condylar cartilage was observed. In the temporal fossa there was an increase in the fibrous connective layer. The synovium appeared hypertrophic and the condylar neck showed a significant periosteal reaction. In three cases a large degree ofdeformation was observed in all components, with intense fibrosis and osteolysis (Fig II E, F). SHAM OPERATION PERFORMED AT 30 DAYS OF AGE-ANIMALS KILLED AT 20 DAYS

In the mandibular morphometry, the decrease in M3, M7, M9, and MI2 was significant. However, there were no changes in the other morphometric, macroscopic, morphologic, and histologic features (Tables 1-3).

FIGURE 6.

Lateral mandibular radiographs. A, Osteotomy (white

arroll') performed at 30 days of age; animal killed after 20 days. B,

Osteotomy performed at 30 days of age; animal killed after 40 days. A healing of osteotomy could be appreciated. C. Osteotomy (white arroll') performed at 70 days of age; animal killed after 30 days. Note verticalization of the condyle. D, Osteotomy performed at 70 days of age; animal killed after 60 days. A healing of osteotomy could be appreciated. E. Osteotomy performed at 70 days of age; animal killed after 60 days. Deformation and distortion of the condylar process could be appreciated.

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MONJE ET AL

Table 3. Anteroposterior TMJ Radiographs (Morphometry) 20 Days Postoperatively (Surgical Procedure Performed at 30 Days of Age)

Parameter Length al a2 a3 a4 a5 a6 a7 a8 a9 Angle alO all al2 al3

Control (n = 8)

Mandibular Osteotomy (n = 7)

Sham Operation (n = 5)

0.55 ± 0.11 0.69 ± 0.12 0.83 ± 0.05 1.36 ± 0.06 0.87 ± 0.08 2.71 ± 0.19 1.88 ± 0.27 6.25 ± 0.55 15.34 ± 0.47

0.40 ± 0.12· 0.80 ± 0.14 1.21 ± 0.24t 1.46 ± 0.07· 1.30 ± 0.18t 3.00 ± 0.25t 1.42 ± 0.21t 5.08 ± 0.61t 14.52 ± 0.47t

0.49 ± 0.06 0.62 ± 0.17 0.78 ± 0.65 1.34 ± 0.88 0.90 ± 0.06 2.57 ± 0.22 1.78 ± 0.45 5.52 ± 1.20 15.11 ± 0.16

90.93 ± 3.20 114.93 ± 4.30 33.68 ± 2.35 63.25 ± 4.59

89.57 ± 111.50 ± 30.00 ± 60.42 ±

5.82 1.63 2.67· 7.02

92.05 ± 2.06 113.60 ± 3.41 33.70 ± 2.43 63.90 ± 3.48

Data are mean ± SD. Significance tested with Mann-Whitney U. See text for description of parameters. * p ~ .05. t P ~ .001. tP~ .01.

30 DAYS OF 40 DAYS

SHAM OPERATION PERFORMED AT AGE-ANIMALS KILLED AT

In the lateral radiograph ofthe cranium, the posterior condylar point (T4) appeared closer to the palatal reference point (Table 4). In the morphometry a decrease in M3 and verticalization ofthe condyle were observed due to the increase in the B-M angle and the C-M angle (Table 5). No differences were observed in the remainder of the study. 70 DAYS OF 30 DAYS Some mandibular horizontal (M 1, M2, M6, and M7) or vertical (M 10) measurements decreased. The posterior edge of the mandibular condyle became verticalized (Table 8). No differences were observed in the rest of the study (Tables 7-9). SHAM OPERATION PERFORMED AT AGE-ANIMALS KILLED AT

70 DAYS OF 60 DAYS

SHAM OPERATION PERFORMED AT AGE-ANIMALS KILLED AT

A statistically significant decrease in the height of the ramus (M 10) was observed (Table 11). No differences were observed in the remainder of the study (Tables 10, 12).

Discussion The TMJ is a joint with a complex set of functions. The biomechanical factors that are a result ofthe joint's

functional activity may modify the growth of all of its structures, especially of the condylar cartilage.'? Adaptation and remodeling are biologic mechanisms that serve to maintain the balance between articular form and function. In growing individuals at craniomandibular level it is accepted that adaptive changes, in relation to functional changes, have a secondary cartilage growth response as a basis (eg, condylar cartilage). In adulthood, when the growth function ofthe condylar cartilage is diminished, remodeling, albeit with a reduced quantitative response, is considered to be the most important mechanism that maintains functional balance. However, at this age it is more probable that when functional factors exceed the joint capacity to remodel, the balance beiween form and function is directed toward a stage in which different articular changes start to become apparent." YOUNG ANIMALS

Anteroinferior displacement of the condyle in the intermediary phase of the experiment (at 20 days) was due to several factors: firstly, to the placement of the condylar fragment in a lateral position to the rest of the mandible during surgery; secondly, to intra-articular edema and, thirdly, to lateral pterygoid muscle traction} 1.13 In the final stage of the experiment (at 40 days after surgery) vertical repositioning ofthe condyle was observed, but it continued in a forward position. This may be due to the fact that as the mandible was smaller, the occlusal function attempted to preserve itself. The slight forward movement of the temporal fossa to preserve articular function is also of great interest. Woodside et al'? found similar results when provoking prognathism in young Macaca tnulatta. After osteotomy, the mandible had smaller horizontal and vertical measurements. This was due to the condylotomy itself, and to a transient decrease in masticatory function, which was reflected by an increase in the incisor crown that disappeared in the final phase. However, the decrease in the intrinsic condylar measurement, such as the anteroposterior length of the condyle, could also be related to a decrease in articular function. In addition, we did not find changes in the direction of the condylar process. In this regard, KilIiany and Johnston II proved that anterior and posterior rotation of the condylar fragment had no effect on the direction of condyle or mandible growth. At joint level, the decrease in internal joint space and intercondylar distance was significant. This coincided with other experimentaf and clinical'"!? studies, and was due to the action ofthe lateral pterygoid muscle on the condylar fragment. 13 The increase in the external articular space and the changes in orientation of the zygomatic arch may be due to muscular or vascular factors related to surgical trauma and modified articular loading. The articular morphologic-macroscopic changes

1228

CHANGES IN TMJ AFTER OSTEOTOMY

FIGURE 8. Photomicrographs ofTMJ, 50 days of age. A. Control group (hematoxylin-eosin stain , original magnification X40). B. Detail of Figure 7A (hematoxylin-eosin stain, original magnification X160). C. Mandibular osteotomy performed at 30 days of age; animal killed after 20 days. Histologic section shows flattened external aspect of the mand ibular condyle (arron's) and thickening of the cond ylar neck (hem atoxylineosin stain, original magnification X40). D, Detail of Figure 7C showing a decreased thickness of the condylar cartilage (especially the proliferative and hypertrophic layers (hematoxylin-eosin stain, original magnification X I60). Key: c, condyle; TF, temporal fossa; I, int ernal; E, external; A, articular layer; P, proliferative layer; T, transitional layer; II, hypertrophic layer.

(thickened capsule and adherent articular disc) were modifications occurring in response to the traumatic bone changes, which decreased at the end of the experiment.

An increase in the thickness ofcondylar cartilage as an indication of an increase in cell replication could not be proven. In this regard, Hinton's study'? showed an increase in cartilage DNA synthesis and cell proIif-

1229

MONJE ET AL

Table 6. Anteroposterior TMJ Radiographs (Morphometry) 40 Days Postoperatively (Surgical Procedure Performed at 30 Days of Age)

Table 4. Lateral Cranial Radiographs (Morphometry) 40 Days Postoperatively (Surgical Procedure Performed at 30 Days of Age)

Parameter TI T2 T3 T4 T5 T6 T7 T8 T9 TIO

Control (n = 6) 3.50 ± 4.79 ± 5.28 ± 27.79 ± 26.12 ± 25.42 ± 3.79 ± 41.61 ± 8.16 ± 13.55 ±

0.64 0.65 0.62 0.71 0.58 0.33 0.18 0.67 0.60 1.18

Subcondylar Osteotomy (n = 6) 3.00 ± 4.08 ± 4.61 ± 26.51 ± 24.83 ± 25.01 ± 3.48 ± 40.60 ± 9.61 ± 14.41 ±

0.38 0.50 0.41 0.65* 0.72* 0.34 0.56 0.45t 1.33t 1.55

Sham Operation (n = 4) 3.28 ± 4.52 ± 4.95 ± 26.22 ± 25.10 ± 24.90 ± 3.44 ± 40.53 ± 8.53 ± 13.60 ±

0.44 0.54 0.56 0.65* 0.61 0.51 0.24t 0.78 0.90 1.10

Data are mean ± SO. Significance tested with Mann-Whitney U. See text for description of parameters. *P:S:.OI. t r « .05.

eration posterior to the condylotomy. After day 14, postcondylotomy this decreased (coinciding with the formation of the fracture callus). In our intermediate phase we were only able to note a decrease in condylar

Table 5. Lateral Mandibular Radiographs (Morphometry) 40 Days Postoperatively (Surgical Procedure Performed at 30 Days of Age)

Parameter Length MI M2 M3 M4 M5 M6 M7 M8 M9 MIO Mil MI2 Angle B-M V-M CA-M CoM

Control (n = 12)

Mandibular Osteotomy (n = 12)

Sham Operation (n = 8)

18.61 ± 13.02 ± 14.95 ± 15.00 ± 17.80 ± 23.96 ± 28.22 ± 12.68 ± 9.37 ± 10.49 ± 6.13 ± 2.75 ±

0.49 0.38 0.27 0.19 0.42 0.75 0.46 0.63 0.19 0.46 0.23 0.34

16.67 ± I 1.68 ± 13.34 ± 14.24 ± 16.92 ± 21.97 ± 26.88 ± 10.81 ± 7.97 ± 9.40 ± 6.04 ± 2.42 ±

0.53* 0.38* 0.47* 0.55 0.72 0.50* 0.92* 0.85* 0.45* 0.60* 0.61 0.23*

17.97 ± 12.53 ± 14.08 ± 14.09 ± 17.29 ± 22.88 ± 27.90 ± 12.18 ± 9.01 ± 9.98 ± 6.18 ± 2.35 ±

0.97 0.29 0.32t 0.31 0.41 0.46 0.90 0.29 0.22 0.20 0.17 0.19

39.91 ± 21.12 ± 91.62 ± 30.29 ±

8.41 2.46 4.08 4.70

33.85 ± 18.64 ± 82.67 ± 39.39 ±

9.93 1.82* 6.60* 18.91

47.50 ± 20.10 ± 89.25 ± 39.55 ±

4.40 1.85 1.39 3.41*

Data are mean ± SO. Significance tested with Mann-Whitney U. See text for description of parameters. * P:s: .001. t r « .05. *P:S:.OI.

Parameter Length al a2 a3 a4 as a6 a7 a8 a9 Angle alO all al2 al3

Control (n = 6)

0.56 ± 0.65 ± 0.73 ± 1.31 ± 0.88 ± 2.54 ± 1.52 ± 6.00 ± 15.67 ±

0.07 0.08 0.17 0.10 0.10 0.25 0.25 0.64 0.26

88.~1 ± 110.10 ± 31.46 ± 60.10 ±

3.13 2.30 2.32 5.63

Mandibular Osteotomy (n = 8)

Sham Operation (n = 6)

0.34 ± 0.07* 0.61 ±0.14 0.99 ± 0.16* 1.50 ± 0.14t 1.24 ± 0.12* 2.77 ± 0.20 1.43 ± 0.21 5.16 ± O.4lt 15.27 ± 0.38t

0.48 ± 0.61 ± 0.73 ± 1.30 ± 0.82 ± 2.48 ± 1.58 ± 5.75 ± 15.24 ±

0.09 0.09 0.14 0.14 0.08 0.35 0.24 0.84 0.49

89.91 ± 111.16 ± 29.83 ± 59.41 ±

1.90 6.15 3.15 5.67

91.16 ± 110.50 ± 29.12 ± 59.16 ±

3.09 4.01 3.79 2.98

Data are mean ± SO. Significance tested with Mann-Whitney U. See text for description of parameters. * P:s: .01. t r « .05. *P:s: .001.

cartilage thickness, especially in the proliferating and hypertrophic layer, a fact that seems to suggest an increase in ossification. IS This finding is in accord with the theory of Moss and Salentjin,'? who affirmed that condyle growth is adaptive, since the condylar cartilage grows according to the law of Huete-Volkmann: compressing forces decrease growth and noncompressing forces stimulate adaptive changes. In the final phase, the articular disc thickened, since it seemed to have a cushioning effect on all changes in articular loading. The sham-operated group showed that postcondylotomy joint changes had no relation to the periosteal lesion. However, the latter may provoke a decrease in certain mandibular measurements and may even provoke a slight decrease in condylar growth. 2o ,2 1 ADULT ANIMALS

At the intermediate stage, no displacement of condylar or temporal points was observed compared with the control, since the growth rate at this age is lower. However, in the final phase, anterior displacement of the condyle and temporal fossa were detected. We believe that this also was due to the preservation of occlusal and articular function. The effectof condylotomy on mandibular measurements is less at the intermediated stage than in young animals. In the final phase, the decrease in these parameters was more noticeable

1230

CHANGES IN TMJ AFTER OSTEOTOMY

FIGURE 9. Photomicrographs ofTMJ, 70 days of age. A. Control group (hematoxylin-eosin stain, original magnification X40). B. Detail of Figure 8A (hematoxylin-eosin stain, original magnification X 160). C. Mandibular osteotomy performed at 30 days; animal killed after 40 days. Histologic section shows a thickened articular disc in the lateral aspects (*) (hematoxylin-eosin stain, original magnification XI60). D. Detail of Figure 8C shows increased height of the condylar cartilage (hematoxylin-eosin stain, original magnification XI60). Key: c, condyle; TF, temporal fossa; I, internal; E, external; A, articular layer; P, proliferative layer; T, transitional layer; II, hypertrophic layer.

and we believe that this is due to the same factors analyzed in young animals. As could be appreciated by condylar morphometry and planimetry, no deepening of the regions proximal to the osteotomy (mandibular and sigmoid notch) occurred. This may be explained by the fact that hypertrophic calluses are more frequent at these ages. Deep-

ening ofthe notch was only noticeable in the final stage, from which it was deduced that bone resorption did not take place until that age. With regard to the changes in the direction of mandibular condylar growth, and given the angle measurements, a trend toward vertical growth in the condylar process was noted during the intermediate phase

1231

MONJE ET AL

MM

Table 7. Lateral Cranial Radiographs (Morphometry) 30 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age) Subcondylar

Parameter TI T2 T3 T4 T5 T6 T7 T8 T9 TIO

Control (n = 6) 3.33 ± 4.92 ± 5.36 ± 28.69 ± 27.31 ± 26.91 ± 3.46 ± 43.51 ± 7.83 ± 13.71 ±

0.46 0.69 0.59 0.80 0.83 0.79 0.39 0.39 1.44 2.21

Osteotomy (n = 8) 3.56 ± 4.85 ± 5.44 ± 27.96 ± 26.61 ± 26.17 ± 3.35 ± 42.87 ± 8.81 ± 15.50 ±

0.67 0.51 0.46 1.35 1.27 0.98 0.77 1.14 1.13 1.75

80 70

Sham Operation (n = 3) 3.31 ± 4.70 ± 5.39 ± 28.09 ± 26.30 ± 26.49 ± 3.30 ± 42.91 ± 8.50 ± 14.20 ±

0.22 0.39 0.14 0.80 0.93 0.55 0.28 0.68 1.23 1.93

Data are mean ± SO. Sec text for description of parameters.

of the experiment. This trend was transient and, as it did not appear in growing animals, may indicate slower adaptation to the new occlusal or articular shape formed after condylotomy. I I Morphologically and histologically, the TMJ in adult animals showed more alterations than in growing animals. Macroscopically, it was possible to observe, both

Table 8. Lateral Mandibular Radiographs (Morphometry) 30 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age)

Control Parameter

(n = 12)

Mandibular Osteotomy (n = 16)

60

Sham Operation (n = 6)

50 40

MM

A

90

90

I ~' ,

M3 M4 M5 M6 M7 M8 M9 MIO Mil

MI2

18.94 ± 13.63 ± 15.30 ± 15.83 ± 19.21 ± 24.42 ± 28.91 ± 13.30 ± 10.27 ± 11.41 ± 6.47 ± 2.97 ±

0.16 0.30 0.32 0.36 0.41 0.33 0.26 0.38 0.19 0.19 0.20 0.42

18.08 ± 13.43 ± 15.37 ± 15.71 ± 18.61 ± 23.85 ± 28.58 ± 12.31 ± 10.02 ± 1O.49± 6.84 ± 1.98 ±

0.53* 0.61 0.50 0.68 0.61t 0.67* 0.64* 0.73* 0.74 0.64* 0.35t 0.25*

18.28 ± 13.31 ± 15.11 ± 15.73 ± 18.92 ± 23.85 ± 28.38 ± 12.68 ± 9.98 ± 10.95 ± 6.42 ± 3.02 ±

0.27t 0.24* 0.26 0.40 0.23 0.24* 0.24* 0.38 0.13 0.23* 0.46 0.24

44.91 ± 3.19 21.75± 1.53 81.75 ± 5.04 35.91 ± 4.94

57.00± 21.12 ± 79.43 ± 46.50 ±

1O.21t 1.97 4.18 15.73*

50.66 ± 22.66 ± 81.16 ± 40.66 ±

8.98* 0.51 2.92 5.68

Angle

B-M V-M CA·M C·M

Data are mean ± SO. Significance tested with Mann-Whitney U. See text for description of parameters. * p s .001. tPs.OI. P s .05.

*

70

:

\

'\

60

... . ......... ...

50

<: ", '.

.... ... .,.

40

30

30

20

20

10

10 70 d • tOO d

70 d • 130 d

MM

MM

FIGURE 10. Condylar planimetry in adult animals. A. 100 days of agc. B. 130 days of age. Key: - - - - -, control; . . . , mandibular osteotomy; - - , sham operation .

in the intermediate and final phase of the experiment, a thickening in the articular capsule, disc adherence, and decreased joint movement. Histologically, the variability in the findings was normal. Joints with thickening in the articular disc could be observed, In other cases an additional type oflesion appeared, such as adherence of the articular disc, which was not found in the TMJ in growing animals. Luz et al 22 described adherence of the disc when using an experimental model of indirect trauma to the TMJ, striking the chin of the rat. We did not observe adherence between the temporal fossa and the articular disc in any of our animals, since there was no trauma to the temporal fossa.

Table 9. Anteroposterior TMJ Radiographs (Morphometry) 30 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age)

Length

MI M2

80

B ,,:~

Parameter Length .11 .12 .13 .14 .15 .16 .17 .18 .19 Angle .110 all .112 .113

Control (n = 7)

0.58 ± 0.60 ± 0.91 ± 1.30 ± 0.98 ± 2.73 ± 1.56 ± 6.23 ± 15.67 ±

0.05 0.07 0.14 0.04 0.13 0.15 0.38 0.56 0.55

85.35 ± 110.92 ± 28.21 ± 53.15 ±

3.55 2.92 3.01 8.02

Mandibular Osteotomy (n = 8)

Sham Operation (n = 4)

0.25 ± 0.64 ± 1.31 ± 1.59 ± 1.52 ± 3.12 ± 1.66 ± 6.04 ± 15.23 ±

0.17* 0.23 0.29t 0.18t 0.11* 0.33t 0.49 0.87 0.58

0.50 ± 0.59 ± 0.74 ± 1.34 ± 0.97 ± 2.59 ± 1.52 ± 5.66 ± 15.35 ±

0.12 0.05 0.22 0.03 0.04 0.33 0.36 0.63 0.50

3.64 3.73 5.04 8.45

86.12 ± 112.87 ± 30.62 ± 55.75 ±

1.03 5.07 1.88 2.59

84.93 108.97 24.87 53.10

± ± ± ±

Data are mean ± SO. Significance tested with Mann-Whitney U. Sec text for description of parameters. * P s .001. t P s .01.

1232

CHANGES IN TMJ AFTER OSTEOTOMY

FIGURE II. Photomicrographs ofTMJ, Adult animals. A , 130 days of age. Control group (hemato xylin-eosin stain, original magnification X40). B. Mandibular osteotomy performed at 70 days of age; animal killed after 60 days. Histologic section shows decreased thickness of the articular disc and increased height of the condylar cartilage (hernatoxylin-eosin stain, original magnification XI60). C. Mandibular osteotomy performed at 70 days of age; animal killed after 30 days. Histologic section shows thickened articular disc and adherence between condyle and articular disc (hematoxylin-eosin stain , original magnification X40). D. Detail of Figure JOC (hematoxylin-eosin stain, -original magnification XI60). E, Mandibular osteotomy performed at 70 days of age; animal killed after 60 days . Histologic section showing severe deformation in TMJ components. Note the extensive fibrosis and the osteolysis (hematoxylin-eosin stain, original magnification X40). F, Detail of Figure JOE (hematoxylin-eosin stain, original magnification XI60). Key: c, condyle; rr, temporal fossa; 0, articular disc; I, internal; E, ex-

ternal.

In another group of animals, lesions causing serious articular degeneration existed, with all TM] components being affected (osteolysis, disappearance of chondral tissue, intense articular fibrosis, and degenerative changes in the articular disc), which indicated a lesser ability to adapt to the new articular shape, the presence of fracture callus, or to ischemia. Up to a point, this may explain the frequency with which Heurlirr'! found open bite and posttraumatic facial deformities when performing condylar osteotomies on adult primates. In joints with no pathologic response to the osteotomy in the final phase of the experiment, an increase in cartilage thickness, changes in the articular disc, and

synovial hypertrophy were observed, which seem to attribute a certain adaptive ability to the TM] in these adult animals. The articular or fibrous and hypertrophic layers in these groups arc considered to be a reservoir of cells that aid in the repair of the condylar surface in the case of injury. Degeneration affectsjoints that are not covered with fibrous tissue, such as the sternoclavicular or the metatarsophalangeal joints, to a greater extent.i" In general, the changes that appeared at the intermediate stage were consequences of the applied injury or of functional adaptation. In the final phase, another series of changes, which can be considered adaptive, presented themselves. In adult animals, the functional

1233

MONJE ET AL

Table 12. Anteroposterior TMJ Radiographs (Morphometry) 60 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age)

Table 10. Lateral Cranial Radiographs (Morphometry) 60 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age)

Parameter TI

T2 T3 T4 T5 T6 T7 T8 T9 TIO

Control (n = 6) 3.93 ± 5.32 ± 5.76 ± 29.71 ± 28.15 ± 27.92 ± 3.69 ± 44.70 ± 9.03 ± 14.66 ±

0.64 0.63 0.60 0.72 0.99 0.95 0.33 1.45 2.06 2.99

Subcondylar Osteotomy (n = 8) 3.81 ± 5.11 ± 5.61 ± 28.24 ± 26.84 ± 26.57 ± 3.32 ± 43.08 ± 9.00 ± 16.87 ±

0.42 0.38 0.42 0.86* 0.75t 0.83t 0.22* 1.04* 1.25 2.66

Sham Operation (n = 5) 3.40 ± 4.96 ± 5.57 ± 29.27 ± 27.47 ± 27.95 ± 3.48 ± 44.52 ± 8.91 ± 15.20 ±

0.55 0.35 0.40 0.77 0.91 0.88 0.34 0.59 1.13 2.10

Data are mean ± SD. Significance tested with Mann-Whitney U. See text for description of parameters. * p.,;; .05. tP.,;;.OI.

or structural alteration produced fewer changes in craniofacial, mandibular, or articular structures due to the decrease in growth rate at these ages. At the end of the study, in some cases, pathologic responses were observed in the TMJ. The age or degree of maturity Table 11. Lateral Mandibular Radiographs (Morphometry) 60 Days Postoperatively (Surgical Procedure Performed at 70 Days of Age)

Parameter Length MI M2 M3 M4 M5 M6 M7 M8 M9 MIO MIl MI2 Angle B-M V-M CA-M CoM

Control (n = 12)

Mandibular Osteotomy (n = 16)

Sham Operation (n = 10)

19.43 ± 14.21 ± 15.85 ± 15.90 ± 19.47 ± 24.95 ± 30.11 ± 13.82 ± 10.66 ± 12.03 ± 7.00 ± 2.87 ±

0.43 0.48 0.25 0.71 0.56 0.64 0.57 0.56 0.44 0.50 0.30 0.26

18.04 ± 13.72 ± 14.94 ± 15.84 ± 18.65 ± 23.64 ± 28.31 ± 12.06 ± 9.23 ± 10.37 ± 7.25 ± 2.03 ±

0.82* 0.24t 0.54* 0.36 0.56t 0.93* 1.09* 1.20* 1.14* 0.78* 0.59 0.62t

20.17 ± 14.51 ± 16.18 ± 16.18 ± 20.05 ± 25.67 ± 30.40 ± 14.14 ± 10.91 ± 11.64 ± 7.05 ± 2.82 ±

0.57 0.47 0.37 0.32 0.26 0.58 0.45 0.69 0.88 0.48 0.07 0.16

43.70 ± 23.79 ± 83.20 ± 35.83 ±

5.06 1.07 2.62 2.75

43.18 ± 23.62 ± 79.50 ± 40.81 ±

17.59 1.00 5.02* 12.92

37.80 ± 25.90 ± 84.70 ± 33.50 ±

1.75 3.76 2.62 2.87

Data are mean ± SD. Significance tested with Mann-Whitney U. See text for description of parameters.

* P.,;; .001. t

P.,;; .01.

*P.,;; .05.

Control (n = 8)

Parameter Length al a2 a3 a4 a5 a6 a7 a8 a9 Angle alO all al2 al3

0.48 ± 0.51 ± 0.75 ± 1.30 ± 0.92 ± 2.45 ± 1.65 ± 6.78 ± 15.84 ±

0.04 0.06 0.16 0.19 0.13 0.22 0.34 0.98 0.37

87.]2 ± 108:66 ± 30.i2 ± 55.03 ±

2.17 2.40 2.04 5.30

Mandibular Osteotomy (n = 8)

Sham Operation (n = 4)

0.32 ± 0.16* 0.53 ± 0.11 1.15 ± 0.26t 1.47 ±0.16 1.10 ± 0.18* 2.90 ± O.30t 1.66 ± 0040 6.13 ± 0.72 15.53 ± 0044

0.61 ± 0.12 0.61 ±O.II 0.85 ± 0.25 1.40 ± 0.15 1.08 ± 0.10 2.84 ± 0.55 1.40 ± 0.12 5.64 ± 0.33 16.13 ± 0.12

85.81 ± 108.00 ± 27.62 ± 54.78 ±

2.29 3.21 3.50 4.89

86.75 ± 106.D7 ± 28.87 ± 51.75 ±

1.32 4.56 2.32 1.32

Data are mean ± SD. Significance tested with Mann-Whitney U. See text for description of parameters. * P ~ .05. tP~.OI.

of each individual is a critical factor in determining the potential for articular adaptability. The majority of experimental studies indicate that the TMJ in young or growing animals, especially the mandibular condyle, is a structure with considerable response to changes in the biomechanical environment. Apparently, this ability to adapt to local or regional changes decreases gradually in mature individuals.P:" Therefore, the condylar cartilage in mature animals shows less ability to recover from functional alterations in articular loading and may be more vulnerable to initial degenerative changes." The specific factors that control the relationship between articular adaptation and age is a subject for discussion. Those differences that exist in animals and individuals at different ages or stages of maturity could be attributed to the decrease in the number and/or vitality of the prechondroblasts. This was demonstrated earlier for the periosteum oflong bones. 30•3 1 . References I. Kerstens CJ, Tuinzig DB, van den Kwast WA: Temporomandibular joint symptoms in orthognathic surgery. J CranioMax Fac Surg 17:215, 1989 2. Banks P, Mackenzie I: Condylotomy: A clinical experimental appraisal ofa surgical technique. J Max-Fac Surg 3:170, 1975 3. Nickerson JW, Veaco NS: Condylotomy in surgery of the temporomandibular joint. Dent Clin North Am 1:303, 1989 4. BeltWH, Yamaguchi Y, You Z: Treatment oftemporomandibular joint dysfunction by intraoral vertical ramus osteotomy, ill Belt WHo (ed); Modern Practice in Orthognathic and Reconstructive Surgery. Philadelphia, PA, Saunders, 1992

1234 5. Harper RP: Analysis of temporomandibular joint function after orthognathic surgery using condylar path tracings. Am J Orthod Dentofacial Orthop 97:480 , 1990 6. Karabouta I, Martis C: The TMJ dysfunction syndrome before and after sagittal split osteotomy of the rami. J Max-Fac Surg 13:185, 1985 7. Freihofer HP, Petresevic D: Late results after advancing the mandible by sagittal splitting of the rami. J Max-Fac Surg 3: 250, 1975 8. Sund G, Eckerdal 0, Astrand P: Changes in the temporomandibular joint after oblique sliding osteotomy of the mandibular rami. J Max-Fac Surg 11:87, 1983 9. Rosenquist B, Rune B, Petersson A. et al: Condylar displacement after oblique osteotomy of the mandibular rami. J CranioMax-Fac Surg 16:301, 1988 10. Petersson A, Willmar-Hegeman K: Radiographic changes of the temporomandibular joint after oblique sliding osteotomy of the mandibular rami.lnt J Oral Maxillofac Surg 18:27, 1989 II. Killiany DM, Johnston LE: Experimental condylar rotation and mandibular growth, ill Carlson DS, McNamara JA Jr, Ribbens KA (eds): Developmental Aspects of Temporomandibular Joint Disorders. Craniofacial Growth Series. Center for Human Growth and Development, The University of Michigan, Ann Arbor, MI, 1985 12. Whetten LL, Johnston LE: The control of condylar growth: An experimental evaluation of the role of the lateral pterygoid muscle . Am J Orthod 88:181 ,1985 13. Hinton RJ: Effect of condylotomy on DNA synthesis in cells of the mandibular condylar cartilage in the rat. Arch Oral BioI 32:865, 1987 14. Hinton RJ: Effect of condylotomy on matrix synthesis and mineralization in the rat mandibular cartilage. Arch Oral Bioi 34: 1003,1989 15. Copray JVCM, Jansen JMH, Dutcrloo HS: An in vitro system for studying the effect of variable compressive on the mandibular condylar cartilage of the rat. Arch Oral Bioi 30:305, 1985 . -16. De Bont LGM, Boering G, Liem RS, et al: Osteoarthritis of the temporomandibular joint. J Oral Maxillofac Surg 43:481, 1985 17. Woodside DG, Altuna G, Harvold E, et al: Primate experiments in malocclusion and bone induction. Am J Orthod 83:460, 1986 18. Kotyla JR: An exploratory study of the mandibular condyle in

CHANGES IN TMJ AFTER OSTEOTOMY

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23.

24.

25.

26.

27.

28. 29.

30.

31.

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