The influence of functional appliance therapy on glenoid fossa remodeling

American Journal of ORTHODONTICS and DENTOFACIAL ORTHOPEDICS Founded in 1915

Volume 92 Number 3 Copyright

September 1987

0 1987 by The C. V. Mosby Company

ORIGINAL

ARTICLES

The influence of functional appliance therapy on glenoid fossa remodeling D. G. Woodslde,* A. Metaxas,** and G. Altuna*** Toronto, Ontario,

Canada

This study investigates the remodeling changes in the condyle and glenoid fossa following a period of progressively activated and continuously maintained mandibular advancement using the Herbst appliance. Progressive mandibular advancement was achieved by adding stops to the telescopic arms of the appliance, with the total activation reaching 7.0 to 10.0 mm, dependent upon the length of the treatment phase. This mandibular advancement produced extensive remodeling and anterior relocation of the glenoid fossa, which contributed to anterior mandibular positioning and altered jaw relationships. (AM J ORTHOD DENTOFAC ORTHOP 1987;92:181-98.)

R

emovable functional orthodontic appliances have been used for nearly 85 years in an attempt to induce mandibular growth by changing muscle function and condylar-glenoid fossa relationships. This type of therapy has provided opportunities, both clinical and experimental, to test bone and muscle relationships’” in a setting of intermittently altered condylar position. In contrast to removable functional appliances, fixed functional appliances (eg, Herbst) maintain a continuous alteration in condylar relationships. At the University of Toronto, clinical studies of Class II treatment using this appliance all showed abnormalities in condylar position4-6 and two studies (Fig. 1) showed no increase in mandibular length after treatment.5,6 Our studies suggested that the final result reflected the op-

eration of multiple factors described below; however, these factors did not explain fully the results achieved. We postulated that forward remodeling of the glenoid fossa may also have contributed to the correction. Thus, it was suggested that a nonhuman model using the Herbst appliance might provide information about the cellular and remodeling responses in the temporomandibular joint to continuously altered, condyle-glenoid fossa relationships. REVIEW OF LITERATURE

In spite of considerable research and debate, the precise mode of action of functional appliances remains obscure. Of the many theories offered to explain this action, the most common include one, or a combination, of the following. 1. Dentoalveolar

This article is based on research that received the Award of Special Merit in the 1987 Mile Hellman Research competition of the American Association of Orthodontists. It was based on a thesis by Angeles Metaxas conducted in the Department of Orthodontics, Faculty of Dentistry, University of Toronto, in partial fulfillment of the requirements for the degree of master of science. Presented to the American Association of Orthodontists in Kansas City, May 1984, and the European Orthodontic Society in Madrid, June 1986. *Professor and Chairman, Department of Orthodontics, University of Toronto. **Assistant Professor, Department Orthodontics, University of Toronto. ***Associate Professor, Department of Orthodontics, University of Toronto.

changes

Harvold7-9 and others’@‘* have stressed the importance of a vertical manipulation of the functional occlusal plane in achieving Class II corrections with removable functional appliances. This occurs by preventing the eruption of the maxillary buccal segments, which is normally in a downward and mesial direction. Removable functional appliances do not appear to move 181

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Fig. 1. This figure shows the occlusion and facial appearance of a growing 1Cyear old boy before treatment (A and D) and following a 6-month treatment with a Herbst appliance (B and E), and the relapse that occurred 6 months posttreatment (C and F).

the upper buccal teeth distally unless a headgear is attached13; however, there may be undesirable tooth movement in the mandibular dentition. 14-16Many have reported both distal movement of maxillary teeth and mandibular anchorage loss with the Herbst appliance.5~‘7~‘s 2. Midface restriction

It has been shown that an important factor in achieving Class II correction in both removable and fixed functional appliances is restriction of forward maxillary growth.W.‘W 3. Mandibular growth induction

A. Intermittent change in condylar position. Of the two distinct schools of thought regarding therapeutic

induction of condylar growth, one group believes that we cannot increase mandibular length to a clinically useful degree by current methods of orthodontic treatment. The other group maintains that the condyle responds to such treatment and the mandibular length can be increased by changing the functional environment of the craniofacial complex. The conflicting results in this area may possibly depend on whether the treatment is intermittent as with removable appliances, or truly continuous, as in fixed functional appliances. Activators are worn primarily during the evening and at night, and thus produce intermittent changes in condylar-glenoid fossa relationships. The best controlled clinical studies of such treatment have been unable to show clinically useful increases in mandibular length.‘6~‘9-22

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Fig. 1 (Cont’d). G and H show the abnormal condylar position 1 week posttreatment; the tracing in I shows the relapse in mandibular position. A subsequent study has shown lesser degrees of condylar position abnormalities when the treatment time was extended to 9 to 11 months.6 In this study there was no discernible difference in condylar position between subjects who had large initial protrusive bite registrations (7.0 to 8.0 mm) and those who had small initial bite registrations (3.0 to 4.0 mm) followed by small amounts of progressive protrusion.

Histologic examination following intermittent forward mandibular functioning in animals usually shows proliferation of condylar cartilage after treatment23W33; however, very few of these studies actually measured mandibular length. Of those that did, some showed no increased length, 32-34while others showed small increases.*7-31,33 The results achieved in some animal studies may be due to the extent of mandibular reposturing, which varies considerably and in some instances is in the extreme range of what could be tolerated physiologically and may be unlike any analogous human situation. B. Continuous change in condylar position. Truly continuous functional therapy requires that the appiiantes be worn constantly and not removed for eating or social purposes; this is essential if a constant alteration in condylar-glenoid fossa relationships is to be achieved. Because few appliances have been designed for truly continuous wear, the literature contains a minimal number of studies on this aspect of functional jaw orthopedics. Two Herbst appliance studies4’35reported an increase in mandibular length when this was mea-

Fig. 2. Experimental animal with appliance inserted and bonded in the mouth. ,One tube used to advance the bite can be seen in right telescope plunger (arrow).

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Flg. 3. A, The temporomandibular joint of a nonexperimental animal showing postglenoid spine (PGS), superior portion of the glenoid fossa fF/, articular eminence (Af), mandibular condyle (C), and articular disk (‘0). (Safranine 0 stain. Original magnification x 8, sagittal section.) B, Enlargement of the superior area of the condyle of the same animal showing zones of condylar cartilage. A, Articular zone. B, Prechondroblastic zone (proliferative zone). C, Chondroblastic zone (hypertrophic zone). 0, Zone of endochondral bone formation (zone of calcification). (Safranine 0 stain. Original magnification x 100, sagittal section.)

Fig. 4. A, Experimental animal before insertion of the Herbst appliance. Note the Class I buccal segment relationship, the mesiodistal relationship of the occlusal amalgam fillings in the first permanent molars, and the location of the metallic implants. B, Same animal at the end of the 12-week experimental period. A severe Class Ill malocclusion is evident (note position of amalgam fillings). In addition, the condyle appears to be forward, relative to the glenoid fossa, when one compares the distance between the condylar head and the basi-sphenoid implants or the vertebral column in A and B.

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A

Fig. 5. A, A modified standard coordinate system28,3awas used to assess the changes in the jaws with respect to the cranial bone. Thus, a line was drawn from sella to nasal tip (NT) on the tracing of the initial cephalogram; a perpendicular to this line from the sella point provided a coordinate system. Successive tracings were superimposed on the cranial base implants in the sphenoid bone and on the best fit of cranial base and endocranial contours. Implants in the occipital area of the cranial base were lnot used because growth was taking place at the sphenocccipital synchondrosis. Then overall horizontal changes in jaw position were measured parallel to the SNT plane, while the overall vertical changes were measured parallel to the SNT perpendicular. increments of change between stages were calculated by subtraction (12-week experimental animal). B and C, The same type of templates were used to assess the bony and dental changes in the maxilla and mandible. Reference planes were drawn on the occlusal surfaces of the maxillary and mandibular dentitions and perpendiculars were dropped from this line. Then the successive tracings of the maxilla and mandible were superimposed on their respective implants. Horizontal and vertical changes within the bones were measured parallel to these planes and the increments of change calculated by subtraction (12-week experimental animal). sured by means of midplane lateral cephalograms, while two studies in which mandibular length was measured on right and left 45” oblique cephalograms showed no increase in length. 5.6 Animal studies using continuous Class II elastics23,3a,37 have shown no increased cartilage proliferation in juvenile and adult monkeys. However, our continuing studies of posterior occlusal bite-blocks3X-4”have shown that varying degrees of continuous mandibular opening with no forced protrusion induced extensive proliferation of condylar cartilage and large increases in mandibular length in both juvenile and adolescent monkeys. 3 4. Redirection of condylar growth Several studies5.4’33 suggest that functional appliance treatment of Class II malocclusions may induce

favorable change in condylar growth direction. It is likely that such changes represent remodeling of various areas of the mandible to produce changes in form.@ 5. Deflection of ramal form Animal

experiments in mandibular repositionand human functional appliance studies5.43.47 have reported changes in the gonial angle that appear to be the result of remodeling in response to altered activity and tone in the masseter-internal pterygoid muscle sling.

ing3.32.3X.45.46.4X.49

6. Horizontal expression of mandibular growth Our continuing serial studies of mandibular growth direction have shown that removal of adverse environmental influences, such as severe airway obstruction, may be followed by a more horizontal mandibular

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Figs.

6 and 7. For legends,

see opposite

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growth direction. 5o-54In addition, we have used posterior occlusal bite-blocks and functional appliances to inhibit buccal segment eruption in both arches, and thus produced horizontal mandibular growth directions in children with excess lower anterior facial height.‘8-40.53 This horizontal expression of mandibular growth either through actual mandibular autorotation, as in orthognathic surgery, or relative mandibular rotation through buccal segment intrusion in growing children is one of the more powerful tools available for the correction of Class II malocclusions associated with excess lower anterior facial height. While others have also achieved similar results with different appliances,55-57unfortunately, the functional appliance literature has largely ignored this highly effective method for improving mandibular position. 7. Changes in neuromuscular and function

anatomy

Abundant evidence suggests that functional appliances modify the neuromuscular environment of the dentition and associated bones. However, the interaction between bone and muscle cannot be explained solely on a pressure-tension basis.J8-a Even though the mechanism of neuromuscular adaptation to functional appliance therapy is complex and difficult to explain, extensive research in this area suggests several adaptive processes-for example, elongation of muscle fibers6’,62 or tendons,63 migration of muscle attachments along bony surfaces,6’.64-66and changes in mus-

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cle dimensions due to bone displacements and rotations.3840,6’ Petrovic and co-workers33.67-69concluded that increased lateral pterygoid activity stimulates increased proliferation of condylar tissue; others have been unable to demonstrate this response.” Experiments at the University of Toronto using chronically implanted electrodes have shown that lateral pterygoid muscle activity, induced by the placement of functional appliances, is depressed for up to 18 weeks.7’-74In addition, we have shown that, with the use of posterior occlusal biteblocks, certain muscles of mastication can adapt by changing the proportion of specific muscle fiber types and fiber diameters.” Obviously, studies of neuromuscular activity are important to the clinician who designs functional appliances. For example, the observation that induced neuromuscular change is depressed for some weeks after appliance placement suggests that we should design appliances to utilize inherent tissue tension and lip activity. 8. Adaptive changes in glendoid fossa location

The adaptive capacity of the glenoid fossa has been demonstrated in human studies of condylar fractures,75 permanent tooth 10ss,‘~and occlusal equilibration” not related to orthodontic therapy. Animal experiments with tooth extraction,78 condylectomy,79-8’ and surgical repositioning of the glenoid fossas show adaptive changes in the glenoid fossa similar to those

Fig. 6. A, Section of the temporomandibular joint of a g-week experimental adolescent animal. Note extensive bone formation along the anterior border of the glenoid fossa and postglenoid spine (arrows), despite the short experimental period. The response of condylar cartilage seems to be within normal limits. (Hematoxylin and eosin stain. Original magnification x8.) B, Under higher magnification, the periosteum of the anterior border of the spine appeared to be thicker than normal. A highly cellular inner layer contained numerous osteogenic cells differentiating into osteoblasts, which, in turn, appeared to be forming osteoid and bone at a rapid rate. This osteoid and new bone (arrows) were not as bright and dense as the adjacent adequately calcified mature bone when examined under normal or polarizing light. In addition, the new bone lacked the typical morphology of mature haversian-type compact bone and showed irregularly organized fibrous elements with large osteocytes and thick, coarse, and irregular collagen fibers; it resembled woven bone in the process of being rapidly remodeled to form mature, lamellar bone. R shows areas of bone resorption along the posterior border of the spine. (Hematoxylin and eosin stain, section photographed with polarized light. Original magnification x42.) Fig. 7. A, Section of the temporomandibular joint of the 12-week experimental adolescent animal. Note extensive bone formation along the anterior border of the postglenoid spine (circle, arrow) and increased thickness of posterior part of the disk. The condyle is clearly in an anterior position in relation to the glenoid fossa and does not show evidence of significant proliferation of cartilage. (Hematoxylin and eosin stain. Original magnification x8.) B, High-power view of the postglenoid spine of the same animal. Arrows demonstrate location of newly formed bone along the anterior border of the spine. Note increased cellular activity in the inner (osteogenic) layer of periosteum (pe) and rows of osteoblasts (ob) along the lower border of the spine. (Hematoxylin and eosin stain. Original magnification x 42.)

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Fig. 8. Enlargement of the superior and anterior area of the condyle in the 12-week experimental adolescent animal. Note reduced thickness of chondroblastic zone with cell-free areas (arrows) and no evidence of excessive remodeling in zone of endochondral bone formation. (Safranine 0 stain. Original magnification x 160.) Fig. 9. A, Decalcified section of the temporomandibular joint of the experimental adult animal. Note absence of condylar cartilage, bone apposition along the anterior border of glenoid fossa and postglenoid spine (arrows), increased thickness of posterior part of articular disk, and anterior repositioning of the mandibular condyle in relation to the fossa. (Hematoxylin and eosin stain. Original magnification x 8.) B, High-power view of superior area of the glenoid fossa showing extensive new bone formation and increased cellular activity of inner (osteogenic) layer of periosteum foe). (Hematoxylin and eosin stain. Original magnification x 100.)

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Fig. 10. Condyle and glenoid fossa of the juvenile pilot study animal. Note extensive bone formation (s) along the anterior border of the postglenoid spine and the posterior border of the condyle. Also note increased proliferation of condylar cartilage (arrow). M, Lateral pterygoid muscle attachment. (Hematoxylin and eosin stain. Original magnification x 10.)

Fig. 11. The figure shows the pretreatment occlusion (A through C) and the occlusion following 6 months’ treatment (D through F) with a Herbst appliance in a 12-year old growing girl.

seen in humans. Few human studies have demonstrated changes in the glenoid fossa following activator treatment43.“3 or explored the possibility that glenoid fossa relocation contributes to the correction of skeletal dysplasia.16 Animal studies showing glenoid fossa remodeling and relocation fall into two groups: those that

show temporal bone adaptation to protrusive mandibular function23~26~30-32*37~W~86~87 and those that show changes after retrusive mandibular forces.23,“7,45.46.84.85,8x Thus, one can make a strong argument that altered function induces temporal bone adaptive remodeling. The contribution of this response to the correction

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Table I. Measured changes in the condyle obtained from mandibular metallic implant superimpositions during

control, sham control, and experimental periods Sample

Control Condyle

Serial

No.

Sex

913 915 979 926 951 Sham 914 Sham 978

*Positive **Positive

Cyno Cyno Cyno Cyno Cyno Cyno Cyno

Duration (weeks)

Age P P P 6 0 0 P

Adolescent Adolescent Adolescent Adult Adolescent Adolescent Juvenile (Pilot)

extension

period

(mm) .

Horizontal

61 50 61 46 46 61 45

3 5.75 2.9 0 2.1 4.2 4.0

indicates forward movement; negative indicates backward movement = horizontal indicates downward movement; negative indicates upward movement = vertical

Vertical 4.95 4.2 5.9 0 1.4 3.8 2.0

co.

to co. (mm) 5.15 7.5 6.5 0 2.4 5.3 4.4

Co. to AMI fmm) 4.5 7.3 6.1 0 2.3 5.0 4.2

measurement. measurement.

Table II. Measured changes in tooth position obtained from maxillary and mandibular metallic implant

superimpositions during the experimental period

Serial

No.

973 915 979 926 957 Sham 974 Sham 978

*Positive **Positive

Sex Cyno Cyno Cyno Cyno Cyno Cyno Cyno

Duration

Age P P P 6 0 P P

Adolescent Adolescent Adolescent Adult Adolescent Adolescent Juvenile (Pilot)

indicates forward movement; negative indicates backward movement indicates downward movement; negative indicates upward movement

of skeletal dysplasia following orthodontic treatment needs further investigation. STATEMENT OF PROBLEM

This study was designed to assess the remodeling that took place in the condyle and particularly the glenoid fossa of adolescent and adult primates in response to a progressively reactivated and continuously maintained mandibular advancement. The present study enlarges an earlier pilot study in which the Herbst appliance was used to achieve progressive and continuous mandibular protrusion.3 It was designed to test whether temporomandibular joint changes following continuous functional appliance therapy make an important contribution to the correction of disproportionate jaw relationships. In addition, this study might show whether the changes observed represent healthy or degenerative adaptations.

6 6 12 12 12 12 13

= horizontal = vertical

weeks weeks weeks weeks weeks weeks weeks

Activation I mm 7mm 10 mm 8 mm 10 mm

measurement. measurement.

MATERIALS AND METHODS

The sample consisted of 6 female and one male cynomolgus (Macaca fascicularis) monkeys; one was juvenile (24 to 36 months), five were adolescent (36 to 48 months), and one was adult (male 70 to 80 months).89,W Activated Herbst appliances (Fig. 2) were placed in five experimental animals; two adolescents wore inactivated appliances (sham controls). Tables I, II, and III show the duration of the control, sham control, and experimental periods. The joints of four additional animals were examined histologically to provide a basis for study of normal joint histology (Fig. 3, A and B). Metallic implants and occlusal amalgams were inserted by standard methods28,9’in the left side of the jaws, the skull, the cranial base, and the first permanent molar to facilitate the measurement and superimposition of the cephalograms (Fig. 4, A). Fiberglass masks were prepared to allow

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Experimental Con&le Duration (weeks)

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on glenoid

I 7 10 8 10

molar

Horizontal*

Vertical**

0.5 1.2 0 0 1.65 0.8 -0.4

0 I 0 0 0.9 I .22 1.9

to co. (mm)

Co.

0.5 1.33 0 II 1.3 1.23 2.0

to AMI (mm) 0.5 1.25 0 0 I .45 0.84 IO

Mandible Incisor

(mm)

191

remodeling

(mm)

Maxilla First

fossa

period

co.

Activation (mm)

6 6 12 12 12 12 13

extension

appliance

(mm)

First

Horizontal*

Vertical**

Horizontal

Vertical

Horizontal

0 - 1.3 - 1.4 - 1.14 0.5 0.32 -2.1

0 -0.5 -0.65 -0.2 -0.5 0.1 - 1.9

0.2 - 0.63 0.8 0.7 0.75 -0.42 -0.5

0 2.1 I -0.4 I 0.6 0

0.7.5 0.52 I 1.12 0.2 0.38 1.5

the animals free movement while protecting the appliances.” Herbst appliances were bonded to the teeth of all experimental animals and activated to give an initial 2.0-mm mandibular advancement. Progressive mandibular advancement was achieved by adding tube stops, 1.O to 2.0 mm thick, to the telescopic arms of the Herbst appliance approximately every 2 weeks (Fig. 2). The total activation was 7.0 to 10.0 mm, dependent upon the length of the experimental period (Table I). Obviously, there was no activation for the sham controls. A custom head positioner prepared for each monkey secured a reproducible head position during serial cephalometry. Fine-grained no-screen film (Kodak XAR-2), used at 80 kvp and 15 mA with exposure time of 10 seconds, produced the finest radiographic resolution possible (Fig. 4, A and@. Radiographs and study models were made of all animals at the start of the control period, the start and end of the experimental

molar

(mm)

Incisor

Vertical 0 -0.65 - 1.1

0.35 0 -0.29 -0.5

Horizontal 1.3 1.5 2 1.2 1.25 0.3 1.5

(mm) Vertical 0.3 0.61 1.5 0.7 0.7 0 3.0

period, and at the end of the posttreatment period after removal of the appliances. Radiographs were made in centric occlusion and with the teeth separated at a standard distance of 25.0 mm so that the cond,yles could be seen clearly. CEPHALOMETRIC

ANALYSIS

A standard coordinate system’8.38was used to measure changes in the position of the jaws relative to the cranial bones and changes within the maxilla and mandible. This is described in the legend of Fig. 5, A through C. Many measurements of bony and dental changes were made,” but this study reports only the following obtained at the beginning and end of the experiment: Horizontal condylar extension: the distance between the perpendiculars drawn from the horizontal axis to the most posterior points of the condylar outlines from the mandibular superimpositions (Fig. 5, C) Vertical condylar extension: the distance between the

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Table III. Mandibular displacement during the experimental period obtained from overall superimpositions on cranial base structures Serial No. 973 975 979 926 957 Sham 974 Sham 978

Sex Cyno Cyno Cyno Cyno Cyno Cyno Cyno

Age P 0 P 6 P 0 0

Adolescent Adolescent Adolescent Adult Adolescent Adolescent Juvenile (Pilot)

horizontal lines drawn from the vertical axis to the uppermost portion of the condylar outlines Condylion to condyfion: the distance between the most posterior and superior points of the condyles Condylion to the anterior metallic implant (AMI): the distance between the most posterior and superior points of the condyle and the most anterior point of the anterior metallic implant Ramus to ramus: the distance between the perpendiculars drawn from the horizontal axis to the most posterior point of the condyles from the overall superimpositions on cranial base structures ( Fig. 5, A). This distance was used to identify possible anterior mandibular displacement. Table IV shows that an acceptable level of accuracy was achieved in superimposing successive tracings and in the subsequent measurements of horizontal and vertical changes between and within individuals.

Duration 6 6 12 12 12 12 13

weeks weeks weeks weeks weeks weeks weeks

Activation

Ramus co ramus (mm)

I mm 7mm 10 mm 8 mm 10 mm

0.9 0 4 1 0 0.7 1.5

RESULTS 1. Occlusal changes

All of the experimental animals had normal occlusion at the beginning of the experiment. Progressive appliance activation produced mandibular prognathism with a Class III malocclusion in the buccal segments and an anterior open bite. These changes were more pronounced in the 12-week experimental animal (Fig. 4, B) than in the 6-week animals. After the appliances were removed, there was a minor abatement of the Class III malocclusion. However, 5 to 7 days after the end of treatment, the Class III malocclusion was stabilized and the mandible could not be manipulated posteriorly under general anesthesia. The sham controls wearing unactivated Herbst appliances maintained a Class I buccal relationship and normal incisal relationship during the 12-week sham control period.

HISTOLOGIC ASSESSMENT

2. Cephalometric evaluation and coordinate analysis

Decalcified sections from the mandibular condyles and the glenoid fossa were examined histologically. The right temporomandibular joints of all the animals were stored in 10% neutral buffered formalin and then decalcified in a 1: 1 solution of 45” formic acid and 20% sodium citrate, changed every second day for 21 days. The tissue was sectioned at 6 pm, stained with hematoxylin and eosin (to show osteoblasts, osteoid, woven bone, resorption, resting line, inflammation), safranine 0 (to show cartilage, stained red; bone, stained green), toluidine blue (to show cartilage, stained dark blue; bone, stained light blue), and Masson trichrome (to show nuclei, stained black; collagen, stained blue). The sections were examined under a Leitz Orthomat microscope and photographed on Kodachrome 25 daylight film with correction filters. Polarizing light was added to some of the slides to emphasize areas of new bone formation and bring out the difference in density and organization between mature and young bone.

The overall superimposition of tracings showed a downward and forward translation of the mandible (Fig. 5, A). The ramus-to-ramus measurement and the forward displacement of the mandibular metallic implants showed that there had been a forward displacement of the mandible relative to the cranial base in all experimental animals except one 6-week animal (Table III). The maxilla was displaced down and back in the incisor area and up and back in the molar area. This brought the molars into a more distal position relative to the cranial base (Fig. 5, A). The sham controls showed a normal forward translation of the maxillary and mandibular complex with horizontal displacement of the implants greater than vertical displacement. The maxillary superimpositions showed that three of four experimental animals had distal movement of the maxillary first molars (Fig. 5, B), while the lingual and inferior displacement of the incisors was minimal (Table II). Thus, the combination of maxillary trans-

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Table IV. Replications of condylar extension measurements obtained by superimposition of mandibles on metallic implants

I

Operator I (A.M.), Replication I Condyle

Serial No.

973 975 979 926 951 Sham 974 Sham

Operator I (A.M.), Replication 2

I

extension

Condyle

Operator

extension

Condyle

II (D.G.W.) extemon

Horizontal

Vertical

Horizontal

Vertical

Horizontal

Vertical

0.5 1.2 0 0 1.65 0.8

0 1 0 0 0.9 1.22

0.6 1.1 0 0 1.60 0.75

0.2 I 0 0 0.85 1.2

0.8 I.25 0 0 I .4 0.6

0.1 1.0 0 0 I.2 I.0

lation plus tooth movement produced a large occlusal change relative to the cranial base. The sham controls showed minimal dental changes. Despite normal mandibular growth in the experimental juvenile and adolescent animals during the control period, none of the measurements used to evaluate condylar extension showed any significant additional mandibular growth at the end of the experiment (Table I). Both of the sham control adolescents showed some horizontal and vertical growth of the condyles (Table I). Dentoalveolar changes in the mandible of the experimental animals consisted of a labial and inferior movement of the incisors and a forward and slightly superior movement of the first molars (Fig. 5, C, Table II). The overall tooth movement was greater in the 12-week adolescent animal than in the two 6-week adolescent monkeys. The dentoalveolar changes in the experimental adult were similar to those in the adolescents, while the sham controls showed minimal changes. 3. Histologic study of the temporomandibular

joint

On this examination the condylar cartilage in the experimental adolescents showed a minimal remodeling response and the prechondroblastic and chondroblastic zones were thin in both the B-week and the 12-week animals. Furthermore, no evidence was found of matrix calcification or remodeling of the osseous trabeculae (Figs. 6, A, and 7, A). The condylar cartilage of the 12-week adolescent showed cell-free areas in the superior and anterior regions of the chondroblastic zone (Fig. S), but no similar areas were seen in the 6-week animals. The condylar head appeared to be flatter in the experimental animals (Fig. 7, A) in contrast to the normal round shape. The experimental adult condyles had no cartilage and only a few scattered chondrocytcs

in the superior and posterior regions, and mature cancellous bone adjacent to a thin articular zone (Fig. 9, A). Histologic examination of the juvenile animal showed a completely different condylar response to the stimulus. There was extensive cartilage proliferation at the end of 13 weeks (Fig. 10). This correlated with the cephalometric examination, which showed a small vertical condylar extension. The experimental adolescents showed subperiosteal bone resorption along the anterior border of the condyle under the insertion of the lateral pterygoid muscle. This resorption appeared to be more extensive in the 6-week animals than in the 12-week animal. 4. Glenoid fossa-postglenoid

spine

The most dramatic changes were seen in 1he glenoid fossa, especially in the area of the postglenoid spine. Study of the animals used to assess normal joint histology showed bone deposition along the pos,terior border of the spine and bone resorption along the anterior part of this area, in agreement with McNamara’s finding? (Fig. 3, A). This contrasted sharply with the histologic findings in all experimental animals. The experimental adolescents showed a dramatic remodeling response of the glenoid fossa and especially the postglenoid spine. There was a reversal of the normal pattern-namely, extensive bone formation along the anterior border followed by bone resorption along the posterior border; this was greater in the 12-week animal than in the 6-week animals (Figs. 6, A and B, and 7, A and B). The experimental adult showed a similar response despite the total absence of any condylar remodeling (Fig. 9, A and B). A juvenile pilot study animal also showed extensive bone formation in the same areas (Fig. 10). Another important finding concerned the posterior part of the articular disk; in all experimental animals,

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Fig. 11 (Co&t). Facial appearance at the beginning of treatment (G), after six months’ treatment (H), and 7 months posttreatment (I). The tomographs show the very abnormal condylar position 1 week following appliance removal (J and K) and the partial correction that occurred 7 months posttreatment (L and M). This case required 2 additional years of orthodontic treatment to correct the dual bite that was created by the appliance. A subsequent study has shown lesser degrees of condylar position abnormalities ihen the treatment time was extended to 9 to 11 months.” In this study there was no discernible difference in condylar position between subjects who had large initial protrusive bite registrations (7.0 to 8.0 mm) and those who had small initial bite registrations (3.0 to 4.0 mm) followed by small amounts of progressive activation. It is assumed that these abnormalities would be further minimized if treatment was extended even longer in growing children.

this appeared to proliferate posteriorly to fill the space created by the condylar displacement. In this area the fibrous tissue contained numerous, enlarged active fibroblasts; most of these appeared in areas where the anterior displacement of the condyle had increased the tension being exerted on the fibers (Figs. 6, A, 7, A, and 9, A).

DISCUSSION

A number of factors contributed to the rapid creation of the Class III malocclusion-eg, maxillary and mandibular tooth movement, changes in maxillary position, anterior glenoid fossa relocation, condylar displacement in the glenoid fossa, and proliferation of the posterior part of the fibrous disk. Mandibular growth was

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a contributing factor in the juvenile animal only. Human studieP also have shown anchorage loss changes and condylar displacement, which in many cases are considered undesirable. Condylar response

After continuous mandibular advancements, cephalometric and histologic examinations of the adolescent and adult animals did not demonstrate any useful increase in mandibular length or increased proliferation of the cellular elements in the cartilaginous zones of the mandibular condyle. Although a number of factors may be operating, this finding may be age- and sexrelated because the juvenile female animal responded with increased mandibular length and proliferation of condylar tissues.3 Further, it may be related to the fact that the degree of mandibular protrusion used in some experimental animals was extreme compared to the protrusion achieved in clinical work. Experiments with a sample of juvenile animals are in progress to clarify this point. Further, experiments by Degroote95 have shown that the presence or absence of posterior occlusal contact during mandibular protrusion is related to proliferation of condylar tissues. The cell-free zones noted in the superior and anterior regions of the chondroblastic zone may represent either damage or a temporary aberration; further investigation is necessary to clarify this point. However, the condylar flattening observed (Figs. 7, A, and 10) obviously represents an adaptation to continuously altered condylar position and may be undesirable. Glenoid fossalpostglenoid

spine

The most important findings in this study are the changes in the glenoid fossa observed after continuous anterior repositioning of the condyle. In all the experimental animals, including, most importantly, the mature adult, a large volume of new bone had formed in the glenoid fossa, especially along the anterior border of the postglenoid spine. With this bone formation and the resorption along the posterior border of the postglenoid spine, the glenoid fossa appeared to be remodeling anteriorly. Expert histopathologists have agreed that the newly forming bone had a normal appearance . The new bone formation appeared to be localized in the primary attachment area of the posterior fibrous tissue of the articular disk. The desposition of the fingerlike woven bone seemed to correspond to the direction of tension exerted by the stretched fibers of the posterior part of the disk. These findings were completely opposite to those observed in our nonexperimental growing animals in whom bone resorption occurred along the anterior part and bone deposition along the posterior part of the spine. This study, which sup-

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ports the work of Hinton and McNamara3’ and others 23,26*30*37,84~86**7 demonstrates that fixed functional appliance therapy may exercise a strong influence on glenoid fossa remodeling. The new bone was deposited rapidly on the anterior border of the postglenoid spine in direct response to the altered mandibular position. This deposition was greater in the 1Zweek adolescent than the 6-week monkeys, indicating that the glenoid fossa was adapting continuously to the continuous stimulus-specifically, the progressive activation of the Herbst appliance. The amount of newly formed bone was large considering the size of the animals’ glenoid fossa. Morphometric analysis to estimate the thickness and volume of new bone is in progress. The posterior part of the articular disk, between the postglenoid spine and the posterior part of the condyle, increased in thickness and showed active cellular and connective tissue response associated with numerous enlarged fibroblasts in active stage. The increased fibrous tissue of the disk posterior to the condyle, associated with the bone apposstion in the glenoid fossa, appeared to stabilize the anterior condylar displacement, which was demonstrated cephalometrically, functionally, and histologically. This fibrous tissue overgrowth may explain why the mandible could not be manipulated posteriorly under anesthesia or after sacrifice and removal of the adjacent musculature. However, it is still possible that such fibrous tissue may resorb after the stimulus is removed and the mandible may partially return toward its original position. In a study of human material at the University of Toronto, the mandible could not be manipulated posteriorly after 6 months’ treatment with the Herbst appliance. However, tomographs of the temporomandibular joints showed that the condyle was displaced anteriorly in relation to the glenoid fossa in some patients and that at 8 months posttreatment the jaw position had undergone a partial relapse (Fig. 11). Similar observations also have been noted during the early stages of removable functional appliance therapy. A recent study,16 using a longer treatment period, also showed condylar displacement but not to the same degree. It is possible that proliferation of fibrous connective tissue similar to that observed in the animals might have contributed to the above clinical findings in human subjects. These observations may aho indicate that the condyle needs time to grow back into the glenoid fossa, or the fossa needs time to remodel anteriorly, or both. In summary, all the glenoid fossa findings in adult, adolescent, and juvenile animals support the view that temporomandibular joint changes following continuous functional appliance therapy may assist in the correction

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of disproportionate jaw relationships. Remodeling such as that seen in this study may create the appearance of an increased mandibular length with or without a true increase. Studies using larger samples of juvenile animals and studies of the posttreatment stability of the altered jaw relationships are in progress in our laboratory. CONCLUSIONS

1. In adult, adolescent, and juvenile primates, continuous and progressive mandibular protrusion produces extensive anterior remodeling of the glenoid fossa. 2. This glenoid fossa remodeling contributes to anterior mandibular positioning and altered jaw relationships. 3. Proliferation of condylar tissues and increased mandibular length following continuous and progressive mandibular protrusion may be age- and sex-related, and was seen only in the juvenile primate. Adolescent primates in the permanent dentition prior to third molar eruption did not show any condylar response. 4. After continuous protrusion, proliferation of the posterior part of the fibrous articular disk splinted the condylar head eccentrically in the glenoid fossa. 5. Skeletal jaw relationship may be altered by both glenoid fossa remodeling and condylar extension in young primates, thereafter by glenoid fossa relocation. This result may be related to age, sex, and the amount of mandibular protrusion. The authors wish to express their sincere thanks to Dr. G. Lie for his critical reading of the manuscript. REFERENCES 1. Wolff J. Virchow’s arch. Path01 Anat Physiol 1899;155:256. 2. Harvold EP. Altering craniofacial growth: force application and neuromuscular-bone interaction. In: McNamara JA, Ribbens KA, Howe RP, eds. Clinical alteration of the growing face. Monograph 14, Craniofacial Growth Series. Ann Arbor: 1983. Center for Human Growth and Development, University of Michigan. 3. Woodside DC?,Altuna G, Harvold E, Herbert M, Metaxas A. Primate experiments in malocclusion and bone induction. AM J ORTHOD1983;83:460-8. 4. Mercer W. Dento-facial adaptation to protrusive function in adolescent children with a modified Herbst appliance [Thesis]. Department of Orthodontics, University of Toronto, 1981. 5. Hutchison LG. Herbst appliance therapy in adolescent children: stability of skeletal and dental adaptation [Thesis]. Department of Orthodontics, University of Toronto, 1982. 6. Strelzow AG. Herbst appliance therapy: its effects on the structure and function of the temporomandibular joint in adolescent children [Thesis]. Department of Orthodontics, University of Toronto, 1986. 7. Harvold EP. Some biologic aspects of orthodontic treatment in the transitional dentition. AM J ORTHOD1963;49:1-14.

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8. Harvold EP, Vargervik K. Morphogenetic response to activator treatment. AM J OR~HOD1971;60:478-90. 9. Harvold EP. Bone remodeling and orthodontics. Eur J Orthod 1985;7:217-30. 10. Thurow RC. Edgewise orthodontics. St. Louis: The CV Mosby Company, 1966. 11. Woodside DG. The activator. In: Graber TM, Neumann B, eds. Removable orthodontic appliances. Philadelphia: WB Saunders Company, 1977:269-336. 12. Wambera IC. A study of the incisal apices line inclination in various malocclusions [Thesis]. Department of Orthodontics, University of Toronto, 1972. 13. Teuscher U. Direction of force application for Class II, Division 1 treatment with the activator-headgear combination. Studieweek 1980:193-203. The Netherlands: Krips Repro Meppel, 1980. 14. Bjijrk A. The principle of the Andtesen method of orthodontic treatment. A discussion based on cepbalometric x-ray analysis of treated cases. AM J ORTHOD1951;37:437-58. 15. Trayfoot J, Richardson A. Angle Class II, Division 1 malocclusions treated by the Andresen method. An analysis of 17 cases. Br Dent J 1968;124:516-9. 16. Vargervik K, Harvold EP. Response to activator treatment in Class II malocclusions. AM J ORTHOD1985;88:242-51. 17. Pancherz H. The mechanism of Class II correction in Herbst appliance treatment. A cephalometric investigation. AM J ORTHOD1982;82:104-13. 18. Sarniis KV, Pancherz H, Rune B, Selvik G. Hemifacial microsomia treated with the Herbst appliance. Report of a case analyzed by means of roentgen stereometry and metallic implants. Atvr J ORTHOD1982;82:68-74. 19. Woodside DG, Reed RT, Doucet JD, Thompson GW. Some effects of activator treatment on the growth rate of the mandible and position of the midface. In: Cook JT, ed. Transactions of Third International Orthodontic Congress. St. Louis: The CV Mosby Company, 1973. 20. Jakobsson SO. Cephalometric evaluation of treatment effect on Class II, Division 1 malocclusions. AM J ORTHOD 1967;53: 446-57.

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50. Lundstrom A, Woodside DG. A comparison of various facial and occlusal characteristics in mature individuals with vertical and horizontal growth direction expressed at the chin. Eur J Orthod 1981;3:227-35. 51. Lundstrom A, Woodside DG. Longitudinal changer, in facial type in cases with vertical and horizontal mandibular growth directions. Eur 3 Orthod 1983;5:259-68. 52. Woodside DC, Linder-Aronson S. The channelization of upper and lower anterior face heights compared to population standard in males between ages 6 and 20 years. Eur J Orthod 1979;l: 25-40. 53. Woodside DG, Linder-Aronson S. Progressive increase in lower anterior face height and the use of posterior occlusal bite block in its management. In: Graber LW, ed. Orthodontics-State of the art, essence of the science. St. Louis: The CV Mosby Company, 1986:200-2 1. 54. Linder-Aronson S, Woodside DG, Lundstrom A. Mandibular growth direction following adenoidectomy. Ah/i J ORTHOD 1986;89:273-84. 55. Pearson LE. Vertical control through use of mandibular posterior intrusive forces. Angle Orthod 1973;43:194-200. 56. Pearson LE. Vertical control in treatment of patients having backward rational growth tendencies. Angle Orthod 197 5;48: 132-40. 57. FrInkel R, Frlnkel C. A functional approach to treatment of skeletal open bite. AM J ORTHOD 1983;84:54-68. 58. Hoyte DA, Enlow DH. Wolff’s law and problem of muscle attachment on resorptive surfaces of bone. Am J Phys Anthropol 1966;24:205-13. 59. Enlow DH. Handbook of facial growth. Philadelphia: WB Saunders Company, 1975. 60. Chierici G. Personal communication with DG Woodside. 1982, Centre for the Management of Congenital Malformations, University of California, San Francisco. 61. McNamara JA. Neuromuscular and skeletal adaptations to altered function in theorofacial region. AM J ORTHOD 1973;64:578606. 62. Goldspink G. The adaptation of muscle to a new functional length. In: Anderson DG, Matthews B, eds. Mastication. Bristol, England: John Wright & Sons, 1976. 63. Muhl ZF, Grimm AF. Adaptability of rabbit digastric muscle to an abrupt change in length: a radiographic study. Ar:h Oral Biol 1974;19:829-34. 64. Symons NB. The attachment of the muscles of mastication. Br Dent J 1954;96:76-8 1. 65. Van der Klaauw CJ. Projections, deepening and undulations of the surface of the skull in relation to the attachment of muscles. Verh Kon Ned Akad Wetensch Afd Naturk 1963;2(55): l-247. 66. Rayne J, Crawford GNC. Increase in fibre numbers of the rat pterygoid muscles during postnatal growth. J Anat 1975;119: 347-57. 67. Petrovic A, Stutzman JJ. Further investigations inio the functioning of the peripheral “comparator” of the servc’system (respective positions of the upper and lower dental arches) in the control of the condylar cartilage growth rate and of the lengthening of the jaw. In: McNamara JA, ed. The biology of occlusal development. Monograph 7, Craniofacial Growth Series. Ann Arbor: 1977:255-91. Center for Human Growth and Development, University of Michigan. 68. Oudet C, Petrovic AG. Variations in the number of sarcomeres in series in the lateral pterygoid muscle as a function of the longitudinal deviation of the mandibular position produced by the postural hyperpropulsor. In: Carlson DS, McNamara JA. eds. Muscle adaptation in the craniofacial region. Monograph 8, Cra-

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Woodside, Metaxas, and Altuna niofacial Growth Series. Ann Arbor: 1978:233-46. Center for Human Growth and Development, University of Michigan. Petrovic A, Stutzman J, Oudet C. Orthopaedic appliances modulate the bone formation in the mandible as a whole. Swed Dent J [Suppl] 1982;15:197-201. Whetten LL, Johnston LE. The control of condylar growth: an experimental evaluation of the role of the lateral pterygoid muscle. AM 1 ORTHOD 1985;88:181-90. Woodside DG. Studies of functional appliance therapy. In: Graber TM, ed. Physiologic principles of functional appliances. St. Louis: The CV Mosby Company, 198556-62. Gurza SC. The lateral pterygoid muscle: a review of structure and function and a new electromyographic methodology for its study [Thesis]. Department of Orthodontics, University of Toronto, 1981. Sessle BJ, Gurza SC. Jaw movement-related activity and reflexly induced changes in the lateral pterygoid muscle of the monkey Macaca fascicularis. Arch Oral Biol 1982;27: 167-73. Powell GR. A study of refex and associated activities of the monkey lateral pterygoid muscle: electromyographic changes associated with placement of a functional appliance [Thesis]. Department of Orthodontics, University of Toronto, 1984. Lindahl L, Hollender L. Condylar fractures of the mandible. II. A radiographic study of remodeling processes in the temporomandibular joint. Int J Oral Surg 1977;6: 153-65. Carlsson G, Oberg T. Remodeling of the temporomandibular joint. In: Zarb G, Carlsson G, eds. Temporomandibular joint function and dysfunction. St. Louis: The CV Mosby Company, 1979:155-74. Mongini F. Condylar remodeling after occlusal therapy. J Prosthet Dent 1980;43:568-77. Breitner C. Further investigation of bone changes resulting from experimental orthodontic treatment. AM J ORTHOD ORAL SURG 1941;27:605-32.

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87. Hiniker JJ, Ramfjord SP. Anterior displacement of the mandible in adult rhesus monkeys. J Prosthet Dent 1966;16:503-12. 88. Ramfjord SP, Hiniker JJ. Distal displacement of the mandible in adult rhesus monkeys. J Prosthet Dent 1966;16:491-502. 89. Hurme VO, van Wagenen G. Basic data on the emergence of permanent teeth in the rhesus monkey (Macaca mulafta). Proc Am Philo Sot 1961;105:105-40. 90. Schultz AH. Growth and development. In: Hartman CG, Straus WL Jr, eds. The anatomy of the rhesus monkey. New York: Hafner Publishing Company, 1965:10-27. 91. Van Ness AL. Implantation of cranial base metallic markers in nonhuman primates. Am J Phys Anthropol 1978;49:85-90. 92. Metaxas A. Primate experiments in bone remodeling in the temporomandibular joint and facial complex using the Herbst appliance [Thesis]. Department of Orthodontics, University of Toronto, 1983. 93. Altuna G, Herbert M, Woodside DG. The effect of bite blocks on the fibre composition of the muscles of mastication [Abstract]. J Dent Res 1983;62:185. 94. Woodside DG, Voudouris J, Altuna G, Metaxas A. Use of a facemask to protect the intra-oral area in cynomolgus monkeys. Lab Anim Sci 1983;33:600-2. 95. Degroote CW. Alterability of mandibular condylar growth in the young rat and its implications [Thesis]. Leuven, Belgium: Katholieke Universiteit Leuven, 1984. Reprint

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Dr. Donald G. Woodside Faculty of Dentistry University of Toronto 124 Edward St. Toronto, Ontario, Canada M5G lG6