Dentofacial changes produced during and after use of a modified Milwaukee brace on Macaca mulatta

Dentof acial changes produced during and after use of a modified Milwaukee brace on Macaca rnulatta Barry S. Cutler, D.M.D., M.S.D.,* David 1. Turpin, D.D.S., M.S.D. Seattle, Wash.

Fred H. Hassig,

D.D.S., M.S.D.,*

and

S

ince the Milwaukee brace was introduced by Blount and Schmidt in 1946, its application and acceptance have gained worldwide attention. That it is an effective support and corrective appliance for the treatment of dysplastic spinal curvatures cannot be disputed. However, untoward changes in the dentoskeletal complex have been demonstrated clinically and cephalometrically as a result of prolonged Milwaukee brace therapy. 2p22p3o Current research has documented disruption of the occlusion and secondary changes in normal growth of the facial skeleton. Existing malocclusions are aggravated, while others are initiated from the continuing pressure of the mandible resting on the brace. The standard system of cephalometric superimposition using fixed reference landmarks and implants has been utilized to interpret the amount and relative direction of bony changes under the influence of the brace. No histologic evidence is available, however, to confirm or refute suppositions made by previous researchers regarding the nature of the altered growth phenomenon produced by the Milwaukee brace. It is very unlikely that this type of data will be available from human autopsy material. The purpose of this investigation is to evaluate cephalometrically and histoFrom the Department of University of Washington. This investigation RR-00166.

was supported

The authors gratefully Washington Orthodontic based on this research. *This

article

Orthodontics by Public

and

Regional

Health

Primate

Center,

Service Grants HD-02280.02

acknowledge financial assistance from Alumni Memorial Fund in preparing

is based on the author’s

Research

and

the University of scientific exhibits

M.S.D. thesis as listed in the bibliography.

115

116

Cutler, Hassig, and Turpin

Am. J. O&hod. February 1972

logically the effects of a modified M ilwaukee brace on the dental, facial, and cranial complex of the growing Macaca mulatta monkey, both during and after brace therapy. It is hoped that the information obtained m ight be useful in understanding and defining the influence of the M ilwaukee brace on the dentofacial complex in man. Review

of the literature

Scoliosis and the Milwaukee brace. Scoliosis is a lateral curvature of the spine. It is a diseaseof the growing child which usually becomesprogressively more severe until growth ceases.It may be of a m ild nature, going unnoticed throughout life, or it may be grossly disfiguring, debilitating, and life-threatening, with the curvature becomingso severethat respiratory and cardiac functions are encroachedupon. Although scoliosis may often be attributed to some specific disease entity, such as poliomyelitis or muscular dystrophy, the majority of casesfall into the category of idiopathic scoliosis-etiology unknown. Current research indicates that idiopathic scoliosis may be due to an abnormality in connective tissue metabolism and possible aberration of the elastic tissue of the spine. This allows the vertebrae to start to deviate to one side and rotate. Once started, the disease then tends to become self-perpetuating and progressive. As the growth of the vertebrae continues, the pressure of weight bearing comes to rest increasingly on the affected or concaveside of the curve. As growth on the contralateral side proceeds normally, the curve progressively worsens. The treatment of scoliosis has always been considered formidable and unsatisfactory. At the end of World War II, two orthopedists, Blount and Schmidt,G introduced a brace which was much less bulky than the plaster jackets and more effective than jackets of lighter material then in use. It was not until 1958, when supportive orthopedic literature becameavailable, that the appliance gained in popularity and becameused more extensively. The M ilwaukee brace consists of a reinforced molded leather pelvic girdle that rides on the superior rim of the iliac crest of the pelvic bone and fits snugly around the waist. Two adjustable vertical bars of steel posteriorly and one anteriorly, extend upward to the neck region where they support an occipital and a mandibular pad, respectively. A torso pressure pad (major pad) of reinforced leather exerts a thrust against the rib hump at and below the apex of the convex side of the curve As the patient grows and spinal curvature is reduced, the bars are extended and the pressure pad is adjusted to accommodatethe increase in stature. Correction of the spinal deformity is accomplished by the alternation of forces described by Blount as being both “active” and “passive” in nature. Passive distraction is provided by the lift of a comfortable flat chin rest and the occipital pad, opposed by the pelvic girdle. Sufficient clearance is provided to allow the patient to raise his chin and occiput from the pads when the brace is forced down against the hips. Active distraction requires the patient to push against the trunk pads which give adequate support while he raises his head. Passive derotation is caused by the major pad pressing against the convex

Volume 61 Number 2

Modified Milwaukee brace 117

curvature of the torso. In this pressure there is a component of mesially directed force that reduces the lateral curve. Active derot,ation is accomplished by the patient when he rests his chin on the mandibular support and moves his torso away from the pressure pad. Thus, while no forcible pressure on the mandible is intended, it is intermittently applied as the patient repeatedly attempts to correct the deformity by his efforts to move his body away from the torso pad. The brace is worn by the patient at least 23 hours per day and is removed only for bathing and to permit attention to personal hygiene. The patient is seen periodically by the orthopedic surgeon, at which time requisite adjustments are made. The brace is worn until such time as the curvature reaches its maximum correction and shows no tendency to regression when support is removed briefly. According to Blount, “this means that an adolescent must be kept in it constantly until the skeleton is mature by all available criteria; that a young child wears it until he has grown straight,” Eflects of orthopedic pressures on the dentofacial complex. More than 40 years ago, HowardI published his observations on two patients wearing scoliosis casts. Although no patients’ ages or roentgenograms were presented, Howard did report a clinically perceptible decreasein lower face height with depression of molar and premolar teeth. He described a concomitant flaring of the anterior teeth with labial tipping. He stated that a constant upward pressure was being exerted upon the lower border of the mandible by the weight of the head, intensified by muscle pull. He also raised the question of perhaps using the scoliosis casts for the treatment of dental open-bites. In 1929 the same investigatorZOreported that the two patients previously described evidenced little tendency to relapse to their former normal state 12 months after the casts were removed. There remained a persistent decreasein lower face height and depression of the mandibular molars and premolars. StillwellZD theorized that unnatural postural positions and pressure situations may affect the internal bones of the face to the same extent as has been shown for the body and back of the head. He emphasized his thesis by presenting pictorial evidence of the influence of externa,l pressures in a horizontal plane upon the alveolar processes.He also reported shortening of the bite caused by resting the mandible upon the hand, thereby producing excessive vertical pressure on the molars and premolars. As the use of the Milwaukee brace increased in popularity, other investigators gl 16123*3odescribed dentofacial changes found during growth of the treated perions. Recently there have been two sophisticated longitudinal studies on the effect of this brace on the dentofacial complex. The first of these was initiated at the University of Texas by Alexander” in 1963. His initial findings were releasedin 1964, and subsequent reports on this continuing study were presented by Fairleigh,13Watson3” Barkley,” and Gee.I4 These authors utilized photographs, study models, and cephalograms to present their findings. The records were taken initially and at 3- to 6-month intervals thereafter. The second study was begun at the University of Washington in 1966. The first report by Lindskogz2 was extended into a continuing analysis by Eastham.ll

118

Cutler, Has&g, and Turpi’l~

Am. J. Orthod. February 1972

This study employed similar research tools with the addition of laminagrams of the temporomandibular joints. Also, metallic implants were placed in the mandible and maxilla, making for morr accurate cephalometric superimpositioning. Hence, a more critical evaluation of the changes taking place in and aronntl these structures was possible In both of these studies a sufficient number of patients were included to ma,kc statistical analysis possible. The profound effects of the Milwaukee brace on the developing fact and tlcl~tition can best be described by combining a.nd summarizing the findings of these two longitudinal studies. These represent the cha.nges seen typically hut, of course, are subject to variation in any given person. The dental changes generally produced are as follows : 1. Depression of maxillary and mandibular molars and premolars. 2. Resorption of the alveolar processes corresponding to the depression. 3. Displacement of the mandibular and maxillary molars and premolars generally in a mesial and buccal direction. 4. Increased procumbency of the anterior t,eeth, often with concomit,ant spacing. 5. Increased anterior overbite. 6. Closure of open-bites. The typical alterations found in the mandible include : 1. Resorption of the lower border where contact is made with the pad. 2. Antegonial notching. 3. Decrease in the gonial angle. 4. Increased apposition of bone at the gonial angle. 5. Decrease in the mandibular plane angle. 6. Counterclockwise mandibular rotation. 7. Possible redirection and/or inhibition of mandibular growth. The upper and over-all facial changes noted are as follows : 1. Reduction in vertical facial height at the expense of facial esthetics. 2. Counterclockwise rotation of the maxilla. 3. Possible redirection of the normal downward and forward sutural growth of the face. 4. Elevation of the palatal plane. From the longitudinal studies of Barkley” and GeeI at the University of Texas have come the first well-documented findings regarding the permanence of these dentofacml changes. Significant among their findings were the following: 1. There was a tendency for recovery of lost vertical dimension. The mean total anterior face height lost was 6.91 mm., with a mean of 2.05 mm. regained in the posttherapy period. 2. There was a tendency for lower incisors to upright themselves. The mean amount of protrusion during therapy was 8 degrees, with a mean recovery of 4 degrees. 3. There was a tendency for the upper incisors to upright themselves. The mean amount of protrusion during treatment was 9.68 degrees, with a mean recovery of 5.27 degrees. 4. The morphologic changes noted in the mandible did not show a

Volume 61 Number 2

Modified

Milwaukee

brace

119

tendency to recover. These would include the increased acuteness of the gonial angle and the increased body length. Methods

and

materials

Five Macaca muZatta monkeys were used as experimental animals in this study. They were chosen because of their similarity to man in growth patterns and anatomy. The age of the animals at the beginning of the study was between 30 and 40 months, as determined from their stage of dental development.26 All animals were provided and maintained for this study by the Regional Primate Research Center at the University of Washington. Although each of the five monkeys wore a modified Milwaukee brace for varying intervals of time, only two of them were used to determine what craniofacial changes occur after the brace is removed. Control data for cepkalometric and histologic comparison were obtained from previously published theses at the University of Washington by Erickson,12 Pih1,27 Turpin31 and Henderson.ls Implants. In order to interpret more accurately the cephalometric results, tantalum implants were placed in various skeletal structures at the beginning of the experimental period. Each was inserted with a modified implant punch, according to the technique described by B jiirk.4 The implants were placed in the maxilla, the mandible, and across the facial sutures. For this procedure Pentothal sodium was used to obtain the required level of surgical anesthesia. The maxillary and mandibular implants were placed by direct penetration of the thin overlying mucosa, connective tissue, and periosteum. The sutural implants were placed after a. flap exposure to the suture and adjacent bone was made. The distance between these implants was measured at the time of placement and at the termination of the study. Cephalometric roentgenograms and ihminagrams. Serial roentgenographic head films of the monkeys were taken at monthly intervals throughout the period of study. The technique employed was similar to that described by Erickson12; an orthodontic roentgenographic cephalometer was modified in order to take these head films. Laminagrams of two monkeys were taken monthly with a Ricketts sectograph cephalometer. To analyze the over-all cranial and facial changes, the serial lateral tracings were superimposed by orientation along the anterior and middle cranial base landmarks of the posterosuperior outlines of 6he orbits, the cribriform plate, and the anterior wall of the middle cranial fossa, with registration on sella turcica. Analysis of maxillary and mandibular changes was made by superimpositioning on their respective implants. In vivo bone markers. Oxytetracycline and Procion Red H-8BS were utilized as in vivo bone markers in the experiment (Table I). The oxytetracycline was given intravenously in a dose of 50 mg. per kilogram of body weight. The Procion RH-8BS was given intraperitoneally at a dose of 100 mg. per kilogram of body weight. These bone markers, given periodically for the duration of the study, served as reference points for subsequent histologic observations. Modified Milwaukee brace. The braces used in the study were constructed by

120

Cutler, Ha&g,

Table I. Experimental Experimental Monkey Male

ad protocol

animal 1

-1 0 81 108 171 172 178

T T P T T T T P

-1 0 174 175 198-200 201

5

Procedure Marker given Brace applied Marker given Marker given Sacrifice Marker given Brace applied Marker given Marker given Marker given Marker given Sacrifice Marker given Brace applied Marker given Brace applied Marker given (brace removed) Marker given Marker given Marker givrn Sacrifice

-1 0 196-198 264 265 330 331

4

T = Tetracycline

Bone marker

-1 0

Monkey 3 Male

Monkey Male

Day _~1 0 245 246 252

Monkey 2 Female

Monkey Male

Turpis

T T P T T

Marker given Brace applied Marker given (brace removed) Marker given Marker given Sacrifice

50 mg./kg.

P = Procion red H-8BS 100 mg./kg.

the Cullen Brace Company, a firm which constructs Milwaukee braces and other orthopedic prostheses in the Seattle, Washington, area. Certain modifications in the brace were required because of the different anatomy of the pelvic region in the Macaca mulatta monkey as compared to man. Because of the prominence of the iliac crests and their relatively sharp form, it was considered inadvisable to have the brace rest on these structures. The appliance was so modified that, in lieu of sitting on the iliac crests, the primary support was obtained by resting the brace on the shoulders of the monkey. The modified Milwaukee brace design consists of a heat-molded plastic’ breast and back plate, each carrying a single vertical steel bar on which is fixed an occipital or mandibular support pad (Fig. 1). Both plates are sponge relieved and leather lined in order to reduce irritation a.t areas of contact with the monkey. Two shoulder straps originate from the anterior support bar, extend over the shoulders, and buckle posteriorly. Considerable sponge relief on the *Thermoplast.

Volume 61 Number 2

Modified Milwaukee brace 12 1

Fig. 1. Side view of modified Milwaukee brace. It is constructed of a heat-molded plastic breast and back plate, with each carrying a single vertical steel bar on which is fixed an occipital or mandibular support pad.

under surface of the strap was added later to minimize pressure irritation. A lower horizontal strap, also buckling at the rear, assures close adaptation of the chest and back plates to the body of the monkey and lends increased stability to the appliance. Particular attention was focused on the precise design and positioning of the mandibular and occipital supports. It was found that a contoured chin support which generally followed the morphologic form of the inferior border of the mandible provided an even distribution of pressure and did not permit the monkey to escape from its influence by turning its head laterally. The occipital and mandibular supports were joined by a circumferential horizontal frame which is a standard feature of the conventional brace. The degree of distraction was controlled in two ways: (1) by raising the occipital and mandibular support pads which are attached to the vertical structural bars on the brace and (2) by tightening or loosening the supporting shoulder straps. Histologic preparation. At the end of the experimental period, final cephalometric films were taken and the monkeys were killed with an overdose of Sernylan. Each animal was perfused first with normal saline solution and then with 10 per cent buffered formalin. The head was removed, tagged for identification, and stored in 10 per cent buffered formalin to await dissection and microscopic examination, The mandibles were freed by cutting through the condylar necks with a

122

Cutler, Ha&g,

artd Turpin

Am. J. Orthod. Febnmy 1972

dental handpiece a,nd bur. An attempt was made not to disturb the anatomic relationship of the condyle within the fossa. After removal of soft tissues, the. mandibles were cut frontally into slabs about I cm. thick, and alternate sections were used for unclecalcified and decalcified preparations. The entire maxilla was removed by sawing in a coronal plane through the cranium at the level of the pterygoid plates. Further saw cuts isolated the left half of the maxilla, including t,he midline sutures. The maxillae were cut frontally up to but not including the pterpgomaxillary suture which was sectioned horizontally. The zygomaticofrontal and zygomaticomaxillary sutures were isolated and sectioned frontally, the zpgomaticotemporal and frontomaxillary ones, sagitally. The temporomandibular joints were removed from the cranium intact wit,h a dental handpiece and a diamond disk and sectioned in the sagittal plane. Alternate blocks of tissue from each mandible, the right temporomandibular joint of each monkey and the right half of the maxilla, including its sutures, were decalcified, embedded in paraffin, and sectioned on a microtome at 10 microns. The se&ions were stained with hematoxylin and eosin prior to mount,ing. I)ecalcified sections were viewed under polarized and bright light. The remaining blocks of tissue from a given animal were embedded in Bioplastic in the manner described by LnftZ4 for preparation of undecalcified ground sections. Sections 120 to 160 microns in thickness were cut from the Bioplastic blocks on a Gillings-Hamco thin sectioning machine and mounted on glass slides with Canada balsam. At least one representative section from each block of tissue was hand ground to a thickness of 80 microns and mounted. The ground bone sections were examined under ultraviolet and polarized light. Histologic measurements were made by means of a microscope calibrated with a stage micrometer. Observations

Throughout the experimental period the monkeys were housed in separate cages at the Regional Primate Research Center. They appeared to adapt remarkably well to the appliances, and on no occasion did the animals damage or escape from the braces. No restraint to their normal activity was found necessary, and their eating habits appeared unaffected as evidenced by normal incremental weight gains during the experimental period. Cephalometric findings. In order to ana,lyze changes in all experimental animals, the cephalometric evaluation must be divided into two periods. The first represents the period of brace therapy and includes all five monkeys. The second is the period after brace removal and includes only monkeys 4 and 5. PERIOD OF BRACE THERAPY. The most significant result of brace therapy was the reversal of normal downward and forward growth of the maxilla and mandible. The entire dentofacial complex was displaced in a superior direction. Superimposed cephalometric tracings for all five monkeys demonstrated this common pattern of change in implant orientation relative to the cranial base registrations (Figs. 2 and 3). Maxillary and mandibular implants had moved in both an upward and forward direction, the mandibular change being ap-

Volume Number

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Modified Milwaukee

brace

123

Fig. 2. Lateral tracings of the skull of a control monkey superimposed on cranial base registration. The direction of growth in the dentofacial complex is downward and forward. Fig. 3. Lateral tracings of the skull of monkey 1 after 245 days of brace therapy. The normal direction of growth has been altered with displacement of the entire dentofacial complex in a superior direction relative to the cranial base registration.

proximately twice as great as that in the maxilla. There was also a concomitant loss in anterior and posterior facial height as determined by direct measurements from the maxillary and mandibular implants. The implants in the anterior part of the face moved slightly more upward and forward than the posterior ones, suggesting a rotational component in the facial changes. The entire dentofacial complex appeared to be moving in a counterclockwise direction around an undetermined axis when viewed from the right side. The most obvious effect of brace therapy on the mandible was a lack of increase in vertical height of the ramus as compared to controls (Figs. 4 and 5). There was no radiographic evidence of flattening or resorption of the condylar head. Considerable resorption was noted along the posterior half of the inferior border of the mandible. The remaining changes appeared similar to those in normal growth: appositional growth on the posterior border of the ramus and the posterosuperior aspect of the coronoid process along with resorption on the anterior borders of the processes. In all monkeys the occlusal and palatal planes were elevated during brace therapy relative to the cranial base registration. When tracings were superimposed on maxillary implants, the palatal plane in the experimental animals seemed to descend without rotation, just as in the control monkeys, This would indicate that appositional growth took place on the oral surface with concomitant resorption on the nasal surface of the palate. The mandibular first permanent molars were intruded from 1 to 1.5 mm. in all the experimental animals; the greatest amount of intrusion occurred in the monkeys that wore the brace for the longest period of time. The maxillary molars showed the same amount of intrusion as the lower teeth. The incisors showed labial tipping to a marked degree in the mandible but less in the maxilla. The control animals described by Ericksonl? and Pihlz7 showed continued eruption of the first molars with simultaneous development of the buccal alveolar

124

Cutler,

Has&g,

and

Am. J. Orthod. February 1972

Turpi~t

July 1957 Jan. 1958 Dee

July Dee

..

1957 1958

__

1958 .-.-.,: ..” . ..............’.’ a .P’ ‘. .:’ ..” .,., ::y ,L, “’ “‘. . . . . . .. . . ::. ., ‘... ._,, : ,c ::“- .,. .. . ,., ., ..’ i.l ..d : :.: ‘.,. ,:

Fig.

4.

trol

animal

Lateral

tracings

exhibited

of the normal

mandible growth

and

and

maxilla

remodeling

superimposed

April June Dec. Fig.

5. Lateral

therapy. appear

The

tracings increase

intruded,

and

of the

mandible

in vertical the

maxillary

and

ramus and

maxilla

height

implants.

This

con-

1967 1967 ,................ 1967 ________

of monkey

is diminished,

mandibular

on

changes.

incisors

1 after the are

days

of brace

first

245

permanent

molars

tipped

labially.

processes. At the same time, the maxillary and mandibular incisors maintained a constant inclination to their respective bony bases. The frontal bones in both the control and experimental animals showed surface apposition. The orbital processes of the frontal bones moved upward and forward as the height of the roof of the orbital cavity was increased relative to the cranial registration. In the control animals, the anterior movement of both the orbital roof and floor was equal. In the experimental animals, the orbital floor moved farther forward than did the roof. This movement further illustrates the rotational movement of the facial complex in the experimental animals. While the pattern of growth in the ant,erior half of the calvaria in the experimental monkeys did not differ from that observed in the control animals, definite morphologic differences were seen in the posterior part of the cranium. The part of the occipital bone subjected to the distracting force from the head pad of the brace appeared to be moving endocranially as if an anterior relocation of the bone in that part of the posterior cranial fossa was occurring. This was observed consistently in the experimental animals. A sharp contrast to this pattern was seen in the control monkeys, where cranial dimensions continued to expand in this region. BRACE REMOVAL. The most significant finding in this period was general reversal of the changes noted during bract therapy. In animals 4 and 5 relatively

Volume 61 Number 2

Modified Milwaukee brace 125

normal growth patterns were again re-established in the dentofacial complex. The maxillary and mandibular implants moved downward and forward, with the mandibular implants exhibiting the greatest amount of movement. The squamous portion of the occipital bone, which demonstrated upward and forward displacement or resorption, returned slightly toward its original position in both monkeys. In the mandible, vertical height of the ramus increased at a faster rate following brace removal. Monkey 4 showed approximately 4 mm. of upward and backward growth. Continued appositional growth was evident on the posterior border and coronoid process. The mandibular first permanent molars in both monkeys erupted to or slightly above their original level prior to brace therapy. The permanent central incisors recovered 10 degrees from the 20 degreesof labial tipping which occurred during therapy. Histologic results. Wherever mineralized tissue is being formed at the time tetracycline is injected, a bright yellow-gold fluorescencewill be produced when the undecalcified section is viewed under ultraviolet light. If the quantity and frequency of injections are standardized, the width of the mark will reflect the rate of bone formation. The intensity of the mark is determined by technical variables, such as the thickness of the section, dosage,storage in formalin, etc. Procion Red H-8BS can be seen under fluorescent light microscopy but with considerably less brilliance or definition than the tetracycline bone marker. Under ultraviolet light, the Procion dye appears a brownish red color and is not confined to tissues undergoing mineralization. Evidence of the dye will remain in nonmineralized connective tissue unless a period of at least 30 days has been allowed between injection and death. Histologic differences were seen in the experimental maxillary sutures as compared with the description given by Hendersonls in control animals. During brace therapy there was almost a complete lack of tetracycline uptake along the sutural margins. The frontomaxillary suture under compression from the brace showed predominantly resorptive activity (Fig. 6). After removal of the brace, this suture showed a definite reversal line followed by a clearly evident zone of bone deposition (Fig. 7). Bone deposition was quit,e evident along most sutural margins following brace removal. The histologic sections of the maxillary tuberosity in the experimental monkeys showed no differences from the description of control animals by Henderson.18Coarse woven bone was seen on the tuberosity, and lamellar deposition was seen on the adjacent anterior surfaces of the pterygoid plates. A loosely cellular connective tissue separatedthe two bonesin the area. The following summary of normal histology for the t,emporomandibu?arjoint is based on three control mankeys. The surface of the condyle is covered by a layer of connective tissue approximately 120 microns thick. The collagen bundles are parallel to the articular surface, mostly in an anteroposterior direction. A dense cellular layer of chondrogenic cells 60 microns thick lies inferior to the fibrous covering and merges gradually into the hyaline growth cartilage. The hyaline cartilage in the condyle averages about 264 microns thick and shows its greatest width at the anterosuperior aspect (Fig. 8). The superficial

126

Cutler, Has&g, UMZ Tuqk

Fig. 6. Micrograph loped

edges

dividing a

lack

force.

and

cells of

of

in the

bone

(Sagittal

deposition

Hematoxylin

the and

lamellae

time eosin

zone

of the

during

the

Hematoxylin

of

The deposition

(R) indicate

frontomaxillary

central

section.

Fig. 7. Micrograph moval.

the

interrupted

the

brace stain.

bone

removal.

and

period

brace

stain.

suture ++

the

monkey

absence

ligament of

eosin

is seen

Magnification,

of

bone

sutural

frontomaxillary

of new of

and

“brace-treated”

suture of

of

(5) indicate therapy.

of

monkey

along

all

sutural

=

Direction

of

bone

*

=

Magnification,

1. The

osteoblasts resorption

Direction

scai-

and

of and

of

brace

X7.5.) 5,

27

margins brace

days

after

brace

(I]. The reversal force.

(Sagittal

relines

section.

X75.)

sixth of t.his cartilage consists of immature chondrocytes which proliferate matrix as the cells extend deeper into the cartilage. The deeper five-sixths of the condylar cartiIage shows the hypertrophic changes assoc,iated with cntlochondral ossification. On its deep surface the remaining matrix is calcified and undergoes resorption by osteoclasts or chondroclasts. Osteoblasts then deposit bone on the remnants of the calcified cartilage and foml the pCmary spongiosa of the condyle. The articular disc is composed of dense connective tissue, with the coarse bundles of collagenous fibers interlacing to FOJ~IJI a tllrcc-c~jnlensiollal network.

lllodified

Milwaukee

brace

127

Blood vessels and nerves are seen only in the periphery of the disc. The bilaminar region is characterized by many blood vessels in a loose connective tissue matrix. The articular tissue on the temporal side of the joint ranges in thickness from 204 microns on the articular tubercle to 24 microns on the roof of the fossa. The articular tissue on the inferior aspect of the articular eminence is composed of dense fibrous connective tissue and contains hypertrophying chondrocytes in its deeper layers. Small areas of boric resorption usually were seen on the upper posterior slope of the articular tuberele and on the lower anterior surface of the postglenoid process. Occasionally, however, bone deposition was seen on these surfaces (Fig. 10). Periosteal apposition was noted along the posterior surface of the postglenoid process. Tetracycline marks were found in the bone forming the roof of the fossn and the crest of the articular tubercle, as well as in the calcifying cartilage and the bone formed at this site. The temporomandibular joints of some of the experimental animals showed changes from the histologic picture of the condylar growth center and articulation just described (Figs. 8 and 9). The fibrous covering of the condyles was the same thickness (120 microns) as in the control animals and showed no destructive changes, such as fraying, fissuring, or noticeable loss of tissue at the articular surface. The transitional zone was 156 microns thick on the anterosuperior surface of the condyle, more than double the thickness of the same area in the control. This zone also seemed to extend farther down the posterior surface of the condyle than normal. The cartilaginous zone was the same thickness as observed in the control animal (264 microns) but appeared to cover less of the total area of the head of the condyle and showed a broader zone of immature and proliferating chondrocyt,es. This zone comprised almost one third of the cartilage zone in the experimental monkey as compased to a 1:16 ratio in the normal animal. The amount of intercellular matrix separating the chondrocytes also appeared greater, and the zone of hypertrophying chondrocytes was correspondingly shorter than in the control and appeared less regular in arrangement. The net effect is that the hypertrophic cartilage covering the condyle in experimental animals 1, 2, and 3 appeared thinner than normal. Endochondral bone formation was seen deep to t.he cartilage zone. The extent and distribution of the tetracycline bone marker in the condyles of the first three experimental monkeys were less than in the control animals (Figs. 10 and 11). This was particularly noticeable in animal 2, where very little of the bone marker was seen. The mark was almost completely absent along its posterior contour, and the primary and secondary spongiosa also contained only a sparse distribution. The tetracycline mark was more noticeable in monkey 1, but it took on a peculiar distribution. In the areas of calcifying cartilage it appeared spotty and irregular in arrangement and did not extend for any distance into the primary spongiosa. The heads of condyles in experimental animals 4 and 5, in which brace therapy had been discontinued, appeared very similar to the age-matched “normal” control animals. The uptake of tetracycline was similar to that in the

128 Cutler, Has&g, md l’uqk

of the anterosuperior aspect of the condyle from an age-matched conFig. 8. Micrograph trol monkey showing the various zones of the condylar growth cartilage and their relf ative th ic:knesses. F, Fibrous zone; T, transitional zone; I, zone of immature and prolifen sting chc lndrocytes; M, zone of hypertrophying and dying chondrocytes; B, zone of endochor ldral (Sagittaf section. Hematoxylin and eosin stain. Magnification, X225.) bol le formation. Fig . 9. Micrograph of the anterosuperior aspect of the condyle from experimental mo nkey with the control animal reveals a relatively thick transitional zone (T) and 1. Comparison felt ;Itively thin zone of hypertrophying and chondrocytes (M). (Sagittal section. Hematoxylin eo: ;in stain. Magnification, X225.)

Volume

61

Number 2

Modijied

Milwaukee

brace

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Fig. 10. Micrograph of the temporomandibular joint of an age-matched control monkey. Tetracycline uptake is seen in the calcified zone (C) just beneath the growth cartilage. (Sagittal, ground section. Ultraviolet light. Magnification, Xl 2.) Fig. 11. Micrograph of the temporomandibular joint of “brace-treated” monkey 2. Tetracycline uptake by the calcified zone (C) is markedly reduced. (Sagittal, ground section. Ultraviolet light. Magnification, Xl 2.)

control monkeys, with a continuous uniform deposition along most of the periphery of the condylar head. The decalcified sections were similar, revealing a growt.h cartilage that appeared normal. Adjacent to the unmarked posterior portion of the condyle in Fig, 11, the resorption on the anterior surface of the postglenoid tubercle and the deposition on its posterior surface are more pronounced than in control joints. The observed resorption of the inferior border of0the experimental mandibles sharply contrasted the activity of this region in the control animals from Turpin’C study (Figs. 12 and 13). The circumferential periosteal apposition normally occurring along the inferior border of the body was interrupted by an irregular scalloping resulting from the presence of Howship’s lacunae. This was par-

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Fig. 12. Micrograph of the inferior border of the mandible from an age-matched control monkey. Rather uniform periosteal bone deposition is seen along the inferior border as indicated by the presence of three tetracycline bone marks which were given at 82-day intervals. (Coronal, ground section. Ultraviolet light. Magnification, X12.)

Fig. 13. Micrograph

of the inferior border of the mandible in experimental monkey 1. The irregular scalloping of the inferior border results from the Howship’s lacunae (arrows) usually seen on a resorptive bone surface. (Coronal section. Hematoxylin and eosin stain. Magnification, X54.1

titularly true for monkey 1, which had worn the brace for the longest experimental period. This resorption was followed by appositional growth after removal of the brace in monkeys 4 and 5 (Fig. 14). Examination of the first molars, which were fully erupted during the experimental period, showed active resorption of bone at the apices of several teeth (Fig. 15). This was in contrast to the control animals, which showed cementurn formation and the presence of osteoblasts at the bony surfaces in the apical areas. These differences were confirmed by the tetracycline preparat,ions, which

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Fig. 14, Micrograph of the inferior border of the mandible from monkey 4, 133 days after removal of the Milwaukee brace. The initial mark (1) is interrupted inferiorly, in contrast to the normal pattern of uniform appositional growth (Fig. 12). The second mark (2) was given at the time of brace removal. The third (3) and fourth (4) marks indicate that bone deposition had occurred following brace removal. (Coronal, ground section. Ultraviolet light. Magnification, X30.) Fig. 15. Micrograph of the apical region of the mandibular first permanent molar in monkey 1 following “brace therapy.” The bone opposite the root apex (R) shows resorptive activity along the entire periodontal surface (arrows) with numerous osteoclasts still present. (Coronal section. Hematoxylin and eosin stain. Magnification, Xl 38.)

also showed that the molars in the experimental monkeys were being tipped buccally around an axis near the apical third of the root. A similar labial tipping was observedin the central incisors of both arches. Discussion

The observations just described indicate that definite dentofacial changes can be produced in a nonhuman primate by means of a modified Milwaukee

brace. Three important aspects of t,liese findings squire rlisc~Issioll: ( I ) J IOW ,I(! thcsc experimentally induced changes resemble those seen in saoliotic child WI I during Milwaukee brace t,hcrapy’? (2) To what degree arc t,hcse changes rclcrsihle when USCof the Milwaukee brace is discontinued? (3) What, informatiolr tlot~s this experiment provide on the mechanisms of facial growth and remodeling. CliGcnI a~pplicntim The changes in dentition and facial skeleton prod~~til in this st’udy differ only in degree from the clinical phenomena which led to this experiment. Serial cephalograms of children show t,hat within 6 to 7 months of t,he initiation of Milwaukee brace therapy there is marked intrusion of the posterior teeth in both arches,13, 2L splaying of the incisors and canines, decrease in lower facial height, and extensive remodeling of t,he lower border of the mandible, that is, resorption just anterior to the gonial angle and appositional bony growt,h greater than normal on the gonial angle, on the posterior border of the ramus, under the anterior half of the lower border, and inferior to the symphysis. A decrease in posterior height of the ramus was reported by one investigator,” while what appearetl to be inhibition of condylar growth was described hs Alexander2 and Lindskog.?’ The same dental and skeletal changes were found in the present experimental monkeys. While the condyles in the control animals grew 3 to 4 mm., the increase in height of the condyle and posterior border of the ramus in the experimental monkeys was diminished during brace therapy. Although cellular activity itI the condylar growth cartilage appeared to be reduced histologically and radiographically by the presence of the Milwaukee brace, there were no signs oi degenerative changes in the temporomandibular joint. A similar reduced response in condyla~ growt,h was reported by Janzen and BluheP when a continuous rctracbing force (If 150 grams was applied to the mandibles of experimental monkeys via brad cap and elastics. The results of this study are in a,greement wit,h their conclusion that condylar growth did not reach its full potential during the period of bract wear. While the magnitude of the force applied by thr braces was not determined, it appeared that tlistractiou was present constantly over the experimental period. It is entirely possible that. at times durin, 0’the stud? only a, minimum of pressure was applied to the lower border of the mandible of experimental monkeys due to growth of t,he animal or adaptation of the brace. For this reason, the brace was adjusted at each cephalometric procedure in ortler to maintain visible estension of the head. The mandibular support pads on the experimental braces were contour designed to fit the anatomy of the monkey mandibles. Ry contrast, the conventional Milwaukee brace chin support pat1 consists of a straight pad which contacts the posterior half of the lower border of the mandible in front of the gonial notch. Blounb and Schmidt’, a claimed that this design did not cause an increase in overbite. Clinical reports by Alexander,2 Fairleigh,‘” and Lindskogz2 and the results of the present investigation indicate that the effects of the external pressure upon the head and face were similar regardless of the design of the chin pad. The only difference nottd in the experimental monkeys was more extensive resorption on the inferior border of the mandible which corresponded to the broader area of coverage of the support pad in the experimental braces. Thus, the observed changes differed only in degree and not in response.

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That the clinical changes were not duplicated exactly in this study could result from three major differences in circumstances: the design of the brace had to be modified, the facial skeleton of the Macacn mulntta differs from that of man, and the experimental animals were not scoliotic. Reversal of changes induced by the brace. Following removal of the modified Milwaukee brace, resumption of condylar growth was quite evident. The investigators believe that growth during the first month after removal of the brace was more active than normal. In the serial cephalometric tracings of monkey 5, considerable condylar growth occurred during this time. Monkey 4 also demonstrated an apparent accelerated growth response during the initial 30 days of this relapse period. This would be in agreement with the clinical impression of Blount and Clarke,5 who reported that an initial growth spurt followed the removal of staples placed across the epiphyseal plate in growing children being treated for leg-length discrepancies. It must be emphasized, however, that this impression of an initial spurt of condylar growth immediately following brace removal was not documented cephalometrically because of the difficulty of obtaining precise condylar tracings from the head films. A method of measuring condylar growth by means of metallic implants must be devised for future studies. Upon removal of the brace, appositional growth was again apparent on those surfaces of the mandible which had previously undergone resorption. This would indicate that the inhibition of periosteal appositional growth by surface pressure was of a temporary nature, produced probably by an altered distribution of stress in these regions and possibly by an alteration in periosteal blood supply. The dental findings following removal of the brace were in general agreement with those of Gee.14Uprighting of the lower incisors and eruption of the posterior teeth were observed. Probably the most significant histologic finding in the facial sutures was the inEtia1 growth response of the frontomaxillary, frontozygomatic, and zygomaticomaxillary sutures to the removal of the brace. This was seen in monkey 5 and was characterized by rapid deposition of bone along the sutural margins perpendicular to the brace force. The osteoblastic activity along these margins was considerably greater than that seen in the control animals. This response would lead to rapid downward maxillary growth, which was also seen cephalometrically. In contrast, monkey 4, with a much longer relapse period, demonstrated sutural activity similar to that of the control animals, indicating that this initial “growth spurt” was followed by a more normal pattern of sutural growth. The effects of brace therapy on the occipital bone and adjacent lambdoidal suture demonstrated that the force applied by the occipital support pad evoked a response almost identical to that by the mandibular support pad. This response included resorption of the outer cortical plate under the support pad and reduced bone deposition in the adjoining lambdoidal suture. Removal of the force resulted in reversal of this response, namely, the resumption of the normal pattern of appositional growth on the surface of the occipital bone and along the margins of the lambdoidal suture. These findings, along with those noted in the dentofacial complex, illustrate that application of a force to an individual bone of the cranium or to the mandible may result in both a localized resorptive response and a more distant

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sutural and/or periodontal response as the force is transmit~tetl t,o am1 dissipated by the surrounding structures. I-n general, following removal of the brace, there was a reversal of the changes noted during brace therapy. Caution must be exercised in the clinical application of the findings of this period, since the experimental animals were removed from the braces while they were still actively growing. This is not the normal procedure in children under treatment for seoliosis with the Milwaukee brace. Growth and remodeling implications. The correlation between roentgenograms and histologic findings corroborated the clinical impression that vertical ramus height did not increase normally during brace therapy. It is thought by the investigators that this diminished growth is due partly to resorption of the lower border of the mandible near the gonial angle. Vertical growth of the condyle may have been inhibited, but with the methods used it was impossible to make an accurate determination of condylar growth. The cephalometric tracings of this area were not sufficiently accurate to be conclusive. Vital bone markers are of limited value in determining the degree of condylar growth retardation. More accurate measurements would be possible if the temporomandibular joint had been implanted. The inhibition of condylar growth resulting from pressure or microtrauma to the temporomandibular joint has been suggested by Weinmann and Sichcr”” and Ricketts.zs Although the exact mechanism of such an occurrence has never been elucidated, these investigators intimated that repeated or prolonged strain on the joint could possibly limit proliferative activity of the chondrogenic zone in the condyle, thereby preventing its contribution to growth of the condylnr cartilage. The present study shows a thickened transitional or chondrogenic zone in the condylar growth center in the experiment,al animals with a normal covering of fibrous connective tissue on the articular surface. The zone of hypertrophying ehondrocvtes is narrowed, and resorption of the intercellular matrix in this area appears diminished. This is the zone in which the cells and intercellular matrix undergo the changes progressing to endochondral ossification. These findings suggest that differentiation of fibroblasts to chondrogenic cells is not impeded under the stress of the abnormal pressure produced by the brace. However, the normal hypertrophic changes of these cells appeared retarded under this same influence. This interpretation is in close agreement with that of Oelbke,15 who placed a loop of wire across the growing epiphyseal plate of the femur in a dog, thereby inhibiting longitudinal bone growth. He found that as long as this pressure was maintained the normal proliferation of the cartilage cells was prevented, with a consequent inhibition of epiphyseal growth. He made it clear that the direction of epiphyseal growth was not altered by this pressure: instead, growth had ceased. He further observed that when the epiphyseal growth plate was released from pressure, there was no spurt of compensatory growth. The femur began to grow again at approximately the normal rate, but it always remained shorter than its control. Another conclusion to be drawn from this study is that the fibrous articular tissue of the temporomandibular joint may be more resistant and better adapted to withstand compressive stresses than had formerly been anticipated. In the

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present study no significant changesin connective tissue covering the head of the condyle and the articular eminence could be observed becauseof the increased external pressure from the brace. Findings with respect to the depth of the fossa also showed that this area did not undergo any remodeling phenomena distinguishable from that of the controls. The experimental monkeys exhibited more than normal resorption on the postglenoid tubercle, and a pattern of tetracycline marking on the adjacent portion of the condyle similar to that seen in recent experimental studies by Adam+ and Meikle.25 These investigators applied posteriorly directed forces to the mandible by means of Class III intermaxilla.ry elastics and created remodeling changes indicative of posterior displacement of the mandible. The brace in the present study also appears to produce condylar displacement posteriorly in greater degreethan would occur normally. Interpretation of microscopic findings of the areas surrounding the roots of the maxillary and mandibular permanent first molar teeth supports the view expressed by many clinical investigators that these teeth are being depressed under the pressure of the brace. It is also noteworthy that this intrusion is accompaniedby an element of buccal tipping, as had been suggestedby Loganz3 and Barkley.3 The teeth of either arch appeared to be similarly affected in this respect. Summary

and

conclusions

The purpose of this investigation is to study the dentofacial changes which occur in the Macaca mulatta monkey during and following treatment with a modified Milwaukee brace. Five young growing monkeys were subjected to brace therapy until changes were produced similar to those seen clinically in children under treatment for scoliosis with the Milwaukee brace. Three of the animals were killed after periods of brace therapy ranging from 54 to 252 days. The remaining two monkeys were studied for additional periods of 29 days and 135 days after brace removal. Tantalum implants were placed in the maxillas and mandibles of the animals, thereby providing stable landmarks for the superpositioning of serial cephalometric tracings. Procion and tetracycline vital stains were administered at appropriate intervals, so as to make later histologic interpretation more meaningful. On the basis of the cephalometric and histologic results, the following conclusions were made: 1. The modified Milwaukee brace produces a directional change in growth of the dentofacial complex in the Macaca mulatta similar to that seen in clinically treated scoliosis patients. Following brace removal the normal direction of growth is again established. 2. Although evidence of articular remodeling is present on the posterior surface of the condyle, no degenerative changes are produced in the temporomandibular joint. by pressure from the modified Milwaukee brace. 3. Histologic and radiographic findings suggest that condylar growth

is retarded by pressure from the brace. The transitional or chondrogenic zone appears thicker and the zone of hypertrophying chondrocytes is narrowed in comparison with the control condyles. 4. Displacement of the maxilla and zygoma is accomplished by means of sutural resorptive remodeling and adjustment, particularly at the frontomaxillarp, frontozygomatic, and zygomaticomaxillary sutures. After removal of the brace, normal growth of these sutures is reestablished. 5. Normal periosteal deposition at the lower border of the mandible is converted to bone resorption by sustained contact with the mandibular pad of the brace. Removal of the brace is followed by resumption of periosteal deposition at the former contact area,. 6. Reduction of over-all facial height is attributed to an eyual amount of intrusion and buccal tipping of both the maxillary and mandibular molars. Labial tipping of the incisor teeth is common to both arches but is more pronounced in the lower. ,2 definite tendency for recovery is seen following removal of the brace, with the teeth returning toward their original positions and axial inclinations. 7. While anterior cranial base growth is unaffected by the modified Milwaukee brace, the pressure of the occipital support pad against the posterior aspect of the calvarium results in an anterior relocation of t,he bone in this area. Endocranial bone deposition plus a moderate degree of sutural readjustment at the articulations of the occipital and parietal bones is considered responsible for this change. 8. Procion Red II-8BS provides an additional in viva bone marker, having an advantage ovc~~ tetracycline in that it is visible in both decalcified and undecalcified tissue sections. In order to ensure its removal from nonrnineralizctl connective tissue, the I’rocion d.ve should not be administcrcd later than 30 days prior to sacrifice. REFERENCES

1. Adams, C. I).: The effects of continuous posterior mandibular forces (Class III) on the temporomandibular joint and t,he dentofacial skeleton of the Mucaca muluttn, M.S.D. thesis, University of Washington, 1969. 2. Alexander, R.: The effects on tooth position and maxillofacial vertical growth during scoliosis t,reatment with the Milwaukee brace; an initial study, A&f. J. ORTHOD. 52: 161-189, 1966. 3. Barkley, J. B.: A study of the changes in the vertical position of the maxillary and mandibular first permanent molars resulting from treatment of scoliosis with a Milwaukee brace, M.S.D. thesis, University of Texas, 1967. 4. Bjork, A.: Facial growth in man; studied with the aid of metallic implants, Acta Odontol. Stand. 13: 9-34, 1955. 5. Blount, W. P., and Clarke, G. R.: Control of bone growth by epiphyseal stapling, .J. Hone Joint Surg. 31A: 464-478, 1949. 6. Blount, W. P., and Schmidt, A. C.: Paper read before the American Academy of Orthopedic Surgeons, 1946. 7. Blount, W. P., and Schmidt, A. C.: Making the Milwaukee brace, J. Bone Joint Surg. 40A: 526-528, 1968. S. Blount, W. P., and Schmidt, A. C.: The Milwaukee brace in the operative treatment of scoliosis, J. Bone Joint Surg. 40A: 511-525, 1958. 9. Bunch, B. W.: Orthodontic positioner treatment during orthopedic treatment of scoliosis, AM. J. ORTHOD. 47: 174-202, 1961.

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10. Cutler, B. S,: Dentofacial changes produced by a modified Milwaukee brace in &~WXUX mzllatta: A roentgenographic and histologic study, M.S.D. thesis, University of Washington, 1968. 11. Eastham, R. M.: Milwaukee brace treated scoliosis patients: A longitudinal study of dentofacial changes and orthodontic stabilizing appliances utilizing cephalometry, laminagraphy and implants, M.S.D. thesis, University of Washington, 1968. 12. Erickson, L. C.: Facial growth in the Macaque monkey: A longitudinal cephalometric roentgenographic study using metallic implant,s, M.S.D. thesis, University of Washington, 1958. 13. Fairleigh, J. F.: A continuation of the study of tooth position and maxillofacial vertical growth during scoliosis treatment with the Milwaukee brace, M.S.D. thesis, University of Texas, 1965. 14. Gee, D. R.: A study of dental and facial changes during and after Milwaukee brace therapy, M.S.D. thesis, University of Texas, 1968. 15. Gelbke, H.: The influence of pressure and tension on growing bone in experiments with animals, J. Bone Joint Surg. 33-A: 947-953, 1951. 16. Glass, D. F.: Bone deformation caused by external pressure, Trans. European Orthod. SOL, pp. 302-311, 1961. 17. Hassig, F. H.: A cephalometric and histologic study in Uacacn mulatta of the changes in the craniofacial complex during and following modified Milwaukee brace therapy, M.S.D. thesis, University of Washington, 1969. 18. Henderson, P. D.: A histologic study of bone growth and remodeling in the maxilla of the Nacaca mulatta monkey, M.S.D. thesis, University of Washington, 1967. 19. Howard, C. C.: A preliminary report of infraocclusion of the molars and premolar5 produced by orthopedic treatment of scoliosis, INT. J. ORTHOD. 12: 434-437, 1926. 20. Howard, C. C.: A second report of infraocclusion of the molars and premolars produced by orthopedic treatment of scoliosis, INF. J. ORTHOD. 15: 329-333, 1929. 21. Janzen, E. K., and Bluher, J. A.: The cephalometrie, anatomic, and histologic changes in Mncaca mulatta after application of a continuous-acting retraction force on the mandible, A X J. ORTHOD. 51: 823-555, 1965. 22. Lindskog, J. A.: Cephalometrie roentgenographic analysis of “Milwaukee brace treated” scoliosis patients with and without orthodontic appliances, M.S.D. thesis, University of Washington, 1967. 23. Logan, R. W.: The effect of the Milwaukee brace on the developing dentition, Dent. Pi-act. 12: 447-454, 1962. 24. Luft, J. H.: Improvements in epoxy resin embedding methods, J. Biophys. Biochem. Cytol. 9: 409-414, 1961. 25. Meikle, M. C.: The effect of a Class II intermaxillary force upon the dentofacial complex in the adult Macaca m@Zatta monkey, M.S.D. thesis, University of Washington, 1969. 26. Merrill, 0. M.: The calcification pattern of the developing permanent dentition of the Macoca nemestrina monkey as related to chronological age, M.S.D. thesis, nniversity of Washington, 1968. 27. Pihl, E. B.: A serial study of the growth of various cranial and facial bones in the Macaque monkey, M.S.D. thesis, University of Washington, 1959. 28. Ricketts, R. H.: Clinical implications of the temporomandibular joint, AY. J. ORTHOD. 52: 416-439, 1966. 29. Stillwell, F. S.: The correlation of malocclusion and seoliosis to posture and its effect upon the teeth and spine, Dent. Cosmos 69: 154-163, 1927. 30. Thors, 0.: Compression of facial sutures by external pressure demonstrated by the implant method, Trans. European Orthod. Sot., pp. 221-232, 1964. 31. Turpin, D. L.: Growth and remodeling of the mandible in the Macaca mdatta monkey, M.S.D. thesis, University of Washington, 1966. 32. Watson, J. G.: Changes in the normal mandibular growth pattern during scoliosis treatment with the Milwaukee brace, M.S.D. thesis, University of Texas, 1966. 33. Weinmann, J. P., and Sicher, H.: Bone and Bones, St. Louis, 1955, The C. V. Mosby Company.