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Tem porom andibular Jo int daptat ions

s soc ia ted W ith H erbst pp l iance T reatm ent

i n Juven i l e R hes us M onkeys

M acaca

mulatta)

John E. Peterson Jr an d James A. M cNam ara Jr

Th is s tudy eva lua ted h is to log ica l ly the tempo roma nd ibu la r j o in t and pos te -

r ior ramal reg ions in juven i le Rhesus monkeys whose mandib les had been

pos i t ioned forw ard w i th a Herbst app liance. Acry l ic sp l in t Herbst app liances

were bonded to the max i l l a ry and mand ibu la r den ta l a rches o f 20 ma le

juveni le an imals . The a n imals w ere k i l led a t 3- , 6- , 12-, and 24-wee k in terva ls

af ter app l iance p lacement . Seven male juven i le Rhesus monk eys served as

con t ro ls . The TMJ reg ions , i nc lud ing the pos te r io r bo rder o f the rami , then

were prepared for qua l i ta t ive and quant i ta t ive h is to log ica l ana lys is . L inear

measurements were ob ta ined by way o f B ioquan t m ic roscop ic equ ipment

Bioquant Image Analys is Corp, Nashv i l le , TN) . St ruc tura l adaptat ions were

no ted in the mand ibu la r condy le , i n f ra tempora l fossa , and the pos te r io r

ramal border o f the exper imenta l an imals in compar ison to cont ro ls . Spe-

c i f ica l ly , increased pro l i fe ra t ion o f the condy lar car t i lage was noted. These

adap ta t ions occur red p r imar i l y i n the pos te r io r and pos te rosupe r io r condy -

la r reg ions . Bone depos i t i on was no ted a long the an te r io r bo rder o f the

postg leno id sp ine; bone resorpt ion occur red a long i ts poster ior border .

S ign i f ican t b ony appo s i t ion a lso was ev iden t a long the pos te r io r bo rder o f

the mandibu lar ramus dur ing ear ly exper imenta l per iods. No gross or mi -

c roscop ic pa tho log ica l changes were no ted in the tem porom and ibu la r j o in t

i n any o f the an ima ls . The resu l ts o f th i s s tudy ind ica te tha t the response o f

the temporomand ibu la r j o in t reg ion in the juven i le an ima ls undergo ing

fo rced mand ibu la r p ro t rus ion w i th the Herbs t b i te - jump ing mechan ism i s

s imi lar to prev ious s tud ies invest igat ing the response to funct iona l pro t ru-

s ion wi th cast occ lusa l sp l in ts . Th is s tudy a lso may prov ide some ins ight

in to the genera l changes occur ring m ic roscop ica ll y i n the temp orom and ib -

u lar jo in t reg ions o f growing pat ients undergo ing Herbst app l iance therapy.

Semin Orthod 2003;9:12-25.)

Cop yr ight 2003, E lsev ier Sc ience USA ). A l l

r igh ts reserved.

From the Department o f Pediatric Dentistry, Loma Lin da University , Loma L inda, CA; an d the Department of Orthodontics and Pediatric

Dentistry, School of Dentistry, Un iversity of Michigan, A nn Arbor, M1.

Supported in par t by United States Public Hea lth Service Ca antDE -03610 a nd b~, un ds made available thw ugh the Thomas M. a nd Doris

Ca abet Endow ed Professorship at the University o f Michigan.

Address carrespondence o James A. McN ama ra Jr, DD S, Phi) , Department o f Orthodontics and Pediatric Dentis try, School of Dentis try,

Universi ty of Michigan, An n Arbor, M I 48109-1078.

Copyright 2003, Elsevier ,Science (USA). Al l rights reserved.

1 0 7 3 8 7 4 6 / 0 3 / 0 9 0 1 - 0 0 0 1 5 3 5 .0 0 / 0

doi: 10.1053/sodo. 2003 .340 21

2

S e m i n a r s i n O r t h o d o n t i c s , V o l 9 , N o 1 ( M a r c h ) , 2 0 0 3 : p p 1 2 - 2 5

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Temporomandibular oint daptations 1 3

e r h a p s m o r e t h a n a n y o t h e r t y pe o f f u n c -

t i o n a l a p p l i a n c e , w h e t h e r f i x e d o r r e m o v -

a b le , t h e t r e a t m e n t e f fe c ts p r o d u c e d b y t h e

b a n d e d H e r b s t a p p li a n c e in h u m a n s h a v e b e e n

w e l l d o c u m e n t e d i n c l in i c al s t u d ie s , e s p e c i a ll y b y

P a n c h e r z a n d c o w o r k e r s . ~q~ O t h e r i n v e s ti g a t o rs

h a v e e v a l u a t e d a l t e r n a t i v e d e s i g ns , i n c l u d i n g t h e

c a s t H e r b s t a p p l i a n c e b y W i e s l a n d e r , 1<~7 t h e

a c ry li c s p l in t H e r b s t a p p l i a n c e b y M c N a m a r a

a n d c o w o r k e r s , lS.~-~ a n d t h e s t a i n l e s s s t e e l c r o w n

a p p l i a n c e b y B u r k h a r d t a n d c o w o r k e r s, e°

M o s t c l in i c al s t u d ie s o f H e r b s t a p p l i a n c e

t r e a t m e n t , r e g a r d l e s s o f t h e d e s i g n o f t h e a p p l i-

a n c e , h a v e i n d i c a t e d t h a t in g e n e r a l t h e e f f e c t s

o f t r e a t m e n t a r e d i v i d e d m o r e o r l es s e q u a l ly

i n t o d e n t o a l v e o l a r a n d s k e l e t a l e f f e c t s . T h e 2

m a i n d e n t o a l v e o l a r e f f e c t s i n c l u d e t h e d i s ta li z a-

t i o n o f th e m a x i l l a r y m o l a r s a n d t h e f o l~ v a rd

m o v e m e n t o f t h e m a n d i b u l a r d e n t i t i o n . M a x il -

l a r y m o l a r d i s t a l i z a t i o n i s s i m i l a r i n m a n y r e -

s p e c t s t o t h a t w h i c h m i g h t o c c u r a f t e r t h e u s e o f

e x t r a o r a l t r a c t i o n , i n t h a t t h e f i r st m o l a r u s u a l ly

i s i n a p o s i t i o n 2 . 0 t o 2 . 5 m m p o s t e r i o r t o t h a t

o b s e r v e d i n u n t r e a t e d C l a ss II in d i v i d u al s f o l-

l o w e d f o r a s i m i la r p e r i o d o f ti m e . T h e s k e l e ta l

t r e a t m e n t e f fe c ts c o n s is t p r i m a r i ly o f m a n d i b u -

l a r a d a p t a t i o n s , w i t h r e l a t iv e l y m i n o r a d a p t a -

t i o n s o b s m w e d i n t h e m a x i l l a ry c o m p l e x . T y p i -

c a ll y, t h e l e n g t h o f t h e m a n d i b l e i n c r e a s e s a b o u t

2 .5 m m m o r e t h a n i n m a t c h e d u n t r e a t e d c o n -

t ro ls d u r i n g t h e t i m e o f H e r b s t a p p l i a n c e

w e a r . i 5 9 i 8

P r e v i o u s x p e r i m e n t a l S t u d i e s

A l t h o u g h m u c h is k n o w n a b o u t t h e e f f ec t s o f t h e

H e r b s t a p p l i a n c e a s o b s e r v e d c l in i ca l ly , r e la t iv e l y

f e w e x p e r i m e n t a l s t u d i e s s p e c i fi c a ll y h a v e c o n -

s i d e r e d t h e s t r u c t u r a l a d a p t a t i o n s p r o d u c e d b y

t h e H e r b s t a p p l i a n c e , a n a p p l i a n c e t h a t f o r c e s a

f o r w a r d m a n d i b u l a r p o s i t io n b y w a y o f th e

H e r b s t b i t e - j u m p i n g m e c h a n i s m . ~ R a t h e r , t h e

m o r e g e n e r a l e x p e r i m e n t a l m o d e l o f fu n c t i o n a l

p r o t r u s i o n h a s b e e n s t u d i e d e x t e n s i v e l y , a m o d e l

i n w h i c h c a s t o v e r la y s ty p i c a ll y h a v e b e e n u s e d t o

c r e a t e a C l a s s I I I o c c l u s a l r e l a t i o n s h i p .

S t u d i e s o f F u n c t i o n a l P r o t r u s io n

B r e i t n e r 29-24 w a s t h e f i r st t o c o n d u c t s u c h e x p e r -

i m e n t s , f o l l o w e d b y t h o s e o f H f i u p l a n d P s a n -

s k y, ~:' H o f f e r a n d C o l i c o , 26 D e r i c h s w e i l e r a n d

B a u m e , 27,~s H i n i k e r a n d Ra m t . }o r d , ~ . ' J o h o , :~° a n d

S t 6 c k l i a n d W i l l e r t. :~l T h e s e s t u d i e s , c o n d u c t e d

p r i m a r i ly in n o n h u m a n p r i m a t e s , w e r e c h ar a c -

t e r i z e d b y o c c l u sa l a l t e r a ti o n s f r o m a n o r m a l t o

a C l as s I I I r e l a t i o n s h i p , s i m i l a r in c o n c e p t b u t

d i f f e r e n t i n s p e c i fi c s f r o m t h e c o r r e c t i o n o f a

C l a ss I I o c c l u s a l r e l a t i o n s h i p t o a n o r m a l o c c l u -

s i o n .

A n u m b e r o f t h e s e e a r l y i n v e s t i g a t o r s -''~2< ~,~u

s h o w e d t h a t t h e c o n d y l a r c a r t i l a g e i s c a p a b l e o f

e x h i b i t i n g c o m p e n s a t o W ti ss u e r e s p o n s e s a f t e r

e x p e r i m e n t a l a l t e r a ti o n o f t h e m a n d i b u l a r f u n c-

t i o n a l p o s i t i o n . B r e i t n e r 2'~e~ a l s o n o t e d s i g n if i -

c a n t a d a p t i v e c h a n g e s i n t h e t e m p o r a l b o n e a f -

t e r f i m c t i o n a l p r o t r u s i o n , c o n c l u d i n g t h a t a

m e s i a l m i g r a t i o n o f t h e g l e n o i d f bs s a h a d o c -

c u r r e d . S i m i l a r f i n d i n g s w e r e r e p o r t e d b y H / i u p l

an d Psa nsky , e :' bu t o t he r inv es t ig a to rs 2<~s,:~e d id

n o t o b s e r v e e v i d e n c e o f s i g n i fi c a n t f o r w a r d m i -

g r a t i o n o f t h e g l e n o i d f o ss a .

O n e o f th e m o s t c o m p r e h e n s i v e s e ri es o f i n-

v e s t i g a t i o n s d e a l i n g w i t h t h e i s su e o f a l t e r i n g

m a n d i b u l a r g r o w th h a s b e e n c o n d u c t e d b y

P e t r o v i c , S t u t z x n a n n , a n d c o l l e a g u e s a t t h e U n i -

vers i ty o f S t r as bo urg . T he i r i n i t i a l s tud ies :~:~-:~

s h o w e d t h a t a n t e r i o r d i s p l a c e m e n t o f t h e m a n -

d i b u l a r c o n d y l e i n r a t s r e s u l t e d i n i n c r e a s e d

g r o w t h o f t h e c o n d y l a r c a r ti la g e . C h a r l i e r a n d

P e t r o v i c :~:~ r e p o r t e d t h a i t h e c o n d y l a r c a r t i l a g e

d i d n o t a p p e a r t o h a v e a n i n d e p e n d e n t g r o w t h

p o t e n t i a l w h e n i s o la t e d f r o m it s e n v i r o n m e n t a l

s t r u c tu r e s . A f t e r t h e m a n d i b l e w a s d is p l a c e d a n -

t e r i o r l y , h o w e v e r , i n c r e a s e d c o n d y l a r g r o w t h o c -

c u r r e d t h r o u g h s t im u l a t i o n o f t h e p r e c h o n d r o -

b l a s t ic a n d c h o n d r o b l a s t i c ( p r o l i f e r a t i v e ) l ay e r s

o f c el ls . :~:~,>* A la te r s tu dy by Pe tro vi c :~; in di ca te d

t h a t m a n d i b u l a r g r o w t h a u g m e n t a t i o n c a n b e

a c h i e v e d i n r a ts w h e n a p p l i a n c e s s i m u l a t i n g

t h o s e u s e d i n c l in i ca l t r e a t m e n t o f h u m a n s ( e g,

b i o n a t o r , F r f i n k e l a p p l i a n c e ) a r e u s e d .

O u r g r o u p a t t h e U n i v e r s i ty o f M i c h i g a n a l so

h a s c o n d u c t e d a se r ie s o f in v e s t ig a t i o n s t h a t h a v e

c o n s i d e r e d c r a n i o f a c i a l a d a p t a t i o n s t o p r o t r u -

s iv e f i m c t i o n , a n d t h e y a re s u m m a r i z e d b r i e f l y

h e r e . T o s t u d y f u n c t i o n a l a d a p t a t i o n s t o c h a n g e s

i n m a n d i b u l a r p o s t u r a l p o s i t i o n i n t h e R h e s u s

m o n k e y , w e h a ve u s e d m a n y e x p e r i m e n t a l d e -

s ig n s, m o s t f r e q u e n t l y t h e m o d e l o f f i m c t i o n a l

p r o t r u s i o n ? 7 *~ A u n i q u e a s p e c t o f t h e s e i n v es t i-

g a t i o n s h a s b e e n t h a t b o t h s t r u c t u r a l a n d f u n c -

t i o n a l a d a p t a t i o n s w e r e c o n s i d e r e d s i m u l t a -

n e o u s ly . F o r e x a m p l e , a n i n c r e a s e i n l a t er a l

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1 4 Peterson and McNamara

p t e r y g o i d a c ti v it y w a s a s so c i a t e d w i t h t h e f o r w a r d

p o s i t i o n i n g o f th e l o w e r j a w . T h i s n e w f u n c t i o n a l

p a t t e r n w a s n o t e d f i r st w i t h s u c h p h a s i c a c t iv i t ie s

a s s w a l l o w i n g a n d s u b s e q u e n t l y w i t h s u c h t o n i c

f u n c ti o n s a s m a i n t e n a n c e o f th e m a n d i b u l a r

p o s t u r a l p o s i ti o n . A s t h e e x p e r i m e n t a l p e r i o d

l e n g t h e n e d h o w e v e r t h e r e w a s a g r a d u a l r e t u r n

t o w a r d t h e p r e a p p l i a n c e l e ve ls o f m u s c l e a c ti vi ty

a n d t h is c h a n g e w a s c o r r e l a t e d i n t im e w i t h th e

s k e l e t a l a n d d e n t o a l v e o l a r a d a p t a t i o n s o b s e r v e d

i n t h e s a m e a n i m a l s .

I n a n o t h e r s tu d y o f f u n c t i o n a l p r o t r u s i o n :~

t h e s e q u e n c e o f a d a p t a t i o n w i th i n t h e c o n d y l a r

c a r t i la g e w a s e x a m i n e d o n a c r o s s- s e c ti o n a l b as is .

P r o l i f e r a t i o n o f th e c o n d y l a r c a r t i la g e w a s o b -

s e r v e d a s e a r l y as 2 w e e k s a f t e r a p p l i a n c e p l a c e -

m e n t . M a x i m u m c a r ti la g e p r o l i f e r a ti o n w a s o b -

s e r v e d a t 6 w e e k s a f t e r w h i c h t i m e t h e r e w a s a

g r a d u a l r e t u r n t o c o n d y l a r m o r p h o l o g y s im i l a r

t o t h a t o b s e r v e d in th e t e m p o r o m a n d i b u l a r r e -

g i o n s o f c o n t r o l a n i m a l s. A l a t e r c e p h a l o m e t r i c

i n v e s t ig a t i o n b y M c N a m a r a a n d B r y a n 4~ i n d i-

c a t e d t h a t t h e c o n d y l a r c a r t i l a g e p r o l i f e r a t i o n

i n d e e d w a s f o l lo w e d b y in c r e a s e d b o n e d e p o s i-

t i o n l e a d i n g t o a l e n g t h e n e d m a n d i b l e . I n f a c t

a t th e e n d o f t h e a c t iv e g r o w t h p e r i o d t h a t e x -

t e n d e d f r o m t h e m i x e d d e n t i t i o n t o a f t e r t h e

e r u p t i o n o f t h e t h ir d m o l a r s t h e a v e r a g e l e n g t h

o f t h e m a n d i b l e i n t h e e x p e r i m e n t a l g r o u p w a s

5 to 6 m m l o n g e r t h a n t h a t o f t h e c o n t r o l a n i -

m a l s .

Studies of orced Protrusion

I n c o n t r a s t t o t h e n u m e r o u s c l i n i c a l s t u d i e s o f

H e r b s t t r e a t m e n t r e l at i ve l y f e w s t u d ie s o f t h e

H e r b s t b i t e - j u m p i n g m e c h a n i s m h a v e b e e n c a r-

r i e d o u t i n e x p e r i m e n t a l a n i m a l s . W o o d s i d e

a n d c o w o r k e r s 42 r e p o r t e d t h a t a f t e r p l a c e m e n t

o f a H e r b s t a p p l i a n c e i n a j u v e n i l e C y n o m o l g u s

m o n k e y

M acac a fascicularis)

f o r a 1 3 - w e e k e x -

p e r i m e n t a l p e r i o d d u r i n g w h i c h a C l as s I I I m a l -

o c c l u s io n w a s c r e a t e d a s m a ll a m o u n t o f r e m o d -

e l i n g w a s n o t e d i n th e s u p e r i o r a s p e c t o f t h e

c o n d y l e . G r o u n d s e c t i o n s w i t h t e tr a c y c l i n e vi ta l

s t a i n i n g a n d d e c a l c i f i e d s e c t i o n s s t a i n e d w i t h

h e m a t o x y l i n a n d e o s i n s h o w e d b o n e f o r m a t i o n

o n t h e s u r t a c e o f a n d w i th i n t h e m a n d i b u l a r

c o n d y l e . T h e g l e n o i d f o s s a a l s o s h o w e d e x t e n -

s iv e b o n e f o r m a t i o n i n th e p o s t e r i o r r e g i o n a f t e r

1 3 w e e k s . W o o d s i d e a n d c o w o r k e r s 42 o n t h e

b a s is o f t h e r e s u lt s f r o m t h is a n d o t h e r e x p e r i -

m e n t s a l so c i t e d w i t h i n t h e a r t ic l e c o n c l u d e d

t h a t c h r o n i c o r c o n t i n u o u s a l t e ra t i o n i n m a n d i b -

u l a r p o s it i on w i t hi n t h e n e u r o m u s c u l a r e n v i r o n -

m e n t p r o d u c e s e x t e n si v e c o n d y l a r r e m o d e l i n g

a n d c h a n g e s i n m a n d i b u l a r s i z e .

I n a l a t e r s t u d y b y W o o d s i d e a n d c o w o r k e r s 4:~

7 C y n o m o l g u s m o n k e y s w e r e u s e d i n a s tu d y o f

H e r b s t a p p l i a n c e t h e r a p y . F i ve o f t h e a n i m a l s

w o r e H e r b s t a p p l i a n c e s f o r 6 t o 1 3 w e e k s ; 2

a d d i t i o n a l a n i m a l s w o r e in a c t i v a t e d a p p l i a n c e s

a s s h a m c o n t ro l s. T h e a p p l i a n c e s w e r e b o n d e d

t o t h e t e e t h a n d a c t i v a t e d 2 m m i n i t i a l l y . T h e y

t h e n w e r e r e a c t i v a t e d e v e r y 2 w e e k s f o r a n a d d i -

t i o n a l 1 t o 2 m m w i t h a t o ta l a c t i v a t i o n o f 7 t o 1 0

m m . O n e o f t h e p r i m a r y f in d i ng s n o t e d b y

W o o d s i d e a n d c o w o r k e r s 4:~ w a s a p r o g r e s s i v e a n -

t e r io r r e m o d e l i n g o f t h e g l e n o id f o s sa p r o d u c e d

b y c o n t i n u o u s a n d p r o g r e ss i v e m a n d i b u l a r p r o -

t r u s i o n t h u s l e a d i n g t o a n a n t e r i o r r e p o s i t i o n -

i ng o f t h e m a n d i b l e .

I t is i m p o r t a n t t o n o t e t h a t n o t a ll o f t h e

a n i m a l s i n t h e W o o d s i d e s tu d y w e r e o f t h e s a m e

a g e . T h e i n v e s t i g a t o r s c l a s s i f i e d 1 a n i m a l a s a

j u v e n i l e 1 a n i m a l a s a n a d u l t a n d 3 a n i m a l s

a s a d o l e s c e n t s . T h e 2 s h a m c o n t r o l a n i m a l s

w e r e a l s o c l a s s i f i e d a s a d o l e s c e n t s . P r o l i f e r a t i o n

o f c o n d y l a r t is su e a n d i n c r e a s e d m a n d i b u l a r

l e n g t h w e r e s e e n o n l y in t h e j u v e n i l e p r i m a t e .

A d o l e s c e n t p r i m a t e s i n t h e p e r m a n e n t d e n t i t i o n

b e f o r e t h e e r u p t i o n o f th e t h i r d m o l a r s d i d n o t

s h o w a n y c o n d y l a r r e s p o n s e . N o c o n d y l a r r e-

s p o n s e w a s o b s e r v e d i n t h e a d u l t a n i m a l a s w e ll .

O n e a d d i t i o n a l f i n d i n g o f si g n i f ic a n c e w a s t h e

a d a p t a t i o n s o c c u r r i n g i n t h e p o s t e r i o r p a r t o f

t h e f i b r o u s a r t i c u l a r d i s c. T h i c k e n i n g o f t h e t is -

s u e in t h is r e g i o n c a u s e d a n e c c e n t r i c r e p o s i t i o n -

i n g o f th e c o n d y l a r h e a d w i t h i n t h e g l e n o i d

f b s sa . T h i s t i s s u e c o n t a i n e d e n l a r g e d a c t i v e f i-

b r o b l a s ts m o s t o f w h i c h a p p e a r e d i n a r e a s i n

w h i c h t h e a n t e r i o r d i s p l a c e m e n t o f t h e c o n d y l e

h a d i n c r e a s e d t h e t e n s i o n b e i n g e x e r t e d o n t h e

f ib e r s. T h e s e f i n d i n g s s u g g e s t t h a t p a r t o f th e

a n t e r i o r d i s p l a c e m e n t o f t h e m a n d i b l e m a y b e

b e c a u s e o f s o ft - ti s su e p r o l i f e r a t i o n r a t h e r t h a n

s k e l e t a l a d a p t a t i o n s . A s u b s e q u e n t r e m o d e l i n g

o f t hi s s of t ti ss u e a f t e r t h e r e m o v a l o f t h e H e r b s t

a p p l i a n c e c o u l d e x p l a i n i n p a r t s o m e o f t h e

r e l a p s e o c c a s i o n a l l y o b s e r v e d d u r i n g t h e f i rs t

f ew m o n t h s a f t e r th e r e m o v a l o f th e H e r b s t a p -

p l i a n c e i n h u m a n s .

N o t s u r p r is i n g ly a n u m b e r o f q u e s t i o n s r e -

m a i n r e g a r d i n g a d a p t a ti o n s i n th e t e m p o r o m a n -

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TemporomandibularJoi,~g Adaptations 15

d i b u l a r j o i n t t h a t o c c u r d u r i n g t r e a t m e n t w i t h

th e H erb s t ap p l i an ce . Th u s , i t i s r ea so n ab l e t o

t e st t h e a s s u m p t i o n t h a t i n a j u v e n i l e n o n h u m a n

p r ima te , t h e re sp o n ses a t t h e t i s su e l ev e l o b -

s e rv e d w i th i n t he t e m p o r o m a n d i b u l a r j o i n t w it h

th e H erb s t ap p l i an ce w i l l b e s imi l a r i n n a tu re ,

s e q u e n c e , a n d t i m i n g t o t h o s e o b s e r v e d i n a

f u n c t i o n a l p r o t r u s i o n m o d e l b y a d a p t i n g t h e

H erb s t ap p l i an ce sp ec i f i ca l l y fo r u se i n a n o n h u -

m a n p r i m a t e . T h e r e f o r e , t h e p u r p o s e o f t hi s

s tudy was to invest iga te h is to logica l ly the t i ssue

r e s p o n se s p r o d u c e d b y t h e H e r b s t a p p l i a n c e o n

t h e c o n d y le , p o s t e r i o r b o r d e r o f t h e m a n d i b l e

an d p o r t i o n s o f th e i n f i ' a t em p o ra l fo ssa .

Materials and Methods

T h e e x p e r i m e n t a l g r o u p c o n si s te d o f 2 0 j u ve n i l e

m a l e R h e s u s m o n k e y s

Macaca mulatta).

T h e i r

a v e r a g e a g e a t t h e c o n c l u s i o n o f th e s t u d y p e r i o d

w a s 2 8 m o n t h s . E a c h e x p e r i m e n t a l a n i m a l

w o re an ac iT l ic sp l i n t H e rb s t ap p l i an ce 4~ ,~ t h a t

w a s b o n d e d t o t h e m a x i ll a ~ , a n d m a n d i b u l a r

d e n t i t i o n s ( F ig 1 ). T h e H e r b s t b i t e - j u m p i n g

mech an i sm, h o w ev e r , w as rev e rsed so t h a t i n t -

p i n g e m e n t o f t h e i n a n d i b u l a r r a m u s b y t h e p r o-

t r u d i n g e n d o f th e p h m g e r w a s a v o i d ed . A ll

a n i m a l s w e r e m a i n t a i n e d u n e v e n t f u l ly u n t il t h e y

w ere t e r mi n a t ed a t r eg u l a r i n te rv a ls . Fo u r j u v e -

n i l e an ima l s w ere sac r i f i ced a f t e r 3 w eek s , 6 a f t e r

6 w eek s , 6 a f t e r 1 2 w eek s , an d t h e rema in in g 4

mo n k e y s a f t e r 2 4 w eeks . In ad d i t i o n , 7 j u v en i l e

m a l e m o n k e y s s e w e d a s c o n t r o l s .

T h e H e r b s t b i t e - j u m p i n g m e c h a n i s m w as co n -

n ec t ed t h r o u g h ac iT l ic spl i n ts o f a d es ig n s im i l a r

Figure 1. lntvaoral photo grap h of the bonded acwlic

splint Herbs t appliance adapted for use in the Rhesus

monkey. The Herbst bi te: jumping mechanism is re-

versed to avoid ramal impingement posteriorly.

to tha t us ed in hu ina n pat ien ts . 1~' Th e only vari-

a t ion in the design was the add i t ion of fu l l cov-

e rag e o f th e p a l a t e a n d max il la~y an t e r i o r t e e th .

Th e sp l i n t w as b o n d ed i n p lace u s in g Ex ce l T

a d h e s i v e ( R e l i a n c e O r t h o d o n t i c P r o d u c t s ,

I t as c a, IL ) . T h e a c tu a l a m o u n t o f a d v a n c e m e n t

( 2. 8 n n n ) w as d e t e r m i n e d c e p h a l o m e t r i c a l l y ,

w i th t h e a m o u n t o f a d v a n c e m e n t v a D 4 n g s li gh tl y

a m o n g a n i m a l s . N o s u b s e q u e n t r e a c t i v a t i o n s o f

t h e a p p l i a n c e s w e r e p e r f o r m e d .

Histological nalysis

Befo re sacr i f ice , h ep a r in (3 00 -5 00 U /k g ) w as

in j ec t ed i n t rav en o u s ly i n to each an ima l t o fac i l -

i t a t e t i s su e p rep a ra t i o n fo r h i s t o lo g i ca l sec t i o n -

in g an d s t a in in g . Th e an ima l w as an es th e t i zed

i n t r a m u s c u l a r l y w i t h X y l a z i n e ( H a v e r - L o c k h a r t

Mi l c s Lab o ra to tT , Sh aw n ee , K S) (1 -2 mg /k g )

a n d i n t r a v en o u s l y w i th p e n t o b a r b i t a l s o d i n m

(8 -1 0 m g / k g ) , s ac r i f i ced b y ca th e t e r i za t i o n o f

th e l e f t v en t r i c l e o r t h e ca ro t i d a r t ew , an d p ro -

f l l sed wi th an AFA fixa t ive (ace t ic ac id , fomal in ,

95% ethyl a lcoh ol ) . ,M' ter dea th , th e he ad was

r e m o v e d s u r g i ca l ly f r o m t h e t o r s o a n d p l a c e d

in to a so lu t i o n o f 1 0 % n eu t ra l b u f fe red fo rma l in

b e f o r e t he r e m o v a l o f t h e t e m p o r o m a n d i b u l a r

. jo inl reg ions b i la tera l ly . The le f t an d r igh t ten t -

p o r o m a n d i b n l a v j o i n t r e g i o n s w e r e r e m o v e d e n

h lo c , immersed i n Bo u in ' s f i x a t i v e fo r 7 2 h o u rs ,

and then decalc i f ied in Warshawsky s e thv l-

en ed i amin e t e t race t i c ac id . D eca l c i f i ca t i o n u su -

a l l) ' was co m ple te in 3 to 6 weeks an d veri f ied

rad io g rap h i ca l l y .

T i s s u e p r e p a r a t i o n f o l l o w e d o n r r o u t i n e l a b -

o r a t o W d e h y d r a t i o n a n d i n f il t r at i o n p r o t o c o l .

Th e t i s su e b lo ck s w ere imb ed d ed i n p a ra f f i n ,

sec t ioned a t 18 to 22 /xm, and s ta ined wi th a

h ema to x y l in an d eo s in s t a in . Th e t i s su e sec t i o n s

th en w ere ev a lu a t ed b o th q u a l i ta t i v e ly an d q u an -

t i t a t i v e ly u s in g l i g h t mic ro sco p y . Th e p o r t i o n s o f

t h e s t u d y l e q u i r i n g l i n e a r m e a s u r e m e n t s w e r e

q u a n t i f i e d w i t h B i o q u a n t m i c r o s c o p i c e q u i p -

men t (B io q u an t imag e A n a ly s i s Co rp , N ash v i l l e

TN ) . V a r io u s an a to mica l s t ru c tu re s i n t h e t en >

p o r o m a n d i b u l a r j o i n t a r e a w e r e i d en t if i ed a n d

s tu d i ed b ased o n t h e l o ca t i o n s w i thin t h e j o in /

f l o m w h ich t h e sec t i o n s w ere cu t . S t rn c tn re s

s tu d i ed f ro n t cen t ra l sec t i o n s i n c lu d ed t h e man -

d i b u l a r c o n d y l e a n d t h e p o s t e r i o r b o r d e r o f t h e

m a n d i b l e . T h e p o s t g l e n o i d s p i n e w a s s t u d i e d

u s in g mo re med ia l sec t i o n s . Th ree cen t ra l sec -

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6 Peterson and McNamara

t i on s a n d 2 m e d i a l s e c t io n s f r o m e a c h j o i n t w e r e

ev a lu a t ed .

Statistical nalysis

A t t e s t w as u sed t o ev a lu a t e t h e co n d y la r a r t i c -

u l a r t i s su es an d ca r t i l ag e fo r d i f fe ren ce b e tw een

c o n t r o l a n d e x p e r i m e n t e d a n i m a l s . T h e l e a s t

sq u a re s reg re ss io n an a ly s i s w as u sed t o d e t ec t

s i g n i f i can t v a r i a t i o n s w i th in ex p e r imen ta l g ro u p s

for a r t icu lar t i ssue and condylar car t i lage wid th .

T h e p o s t g l e n o i d s p i n e , p r e s e n c e o f o s s if i ed

c a r t i l a g e i n t h e c o n d y l e , a n d t h e p o s t e r i o r b o r -

d e r o f th e m a n d i b l e w e r e e v a l u a t e d b y a s s i g ni n g

t h e m a d e g r e e o f e x p r e s s i o n r a t i n g o f 0 t o 3 ( 0,

n o n e ; 1 , min ima l ; 2 , mo d e ra t e ; 3 , ex t en s iv e ) . A

b o n y c a p u n d e r l y i n g t h e c o n d y l a r c a r t i l a g e w a s

j u d g e d s i m p l y t o b e p r e s e n t o r n o t . A c h i - s qu a r e

an a lys i s w as u sed t o ev a lu a t e t h e p o s t g l en o id

s p i n e , o s si f ie d c ar t il a g e , a n d p o s t e r i o r b o r d e r o f

t h e m a n d i b l e . T w o h i s t o lo g i c a l s e c ti o n s p e r j o i n t

w e r e u s e d t o e v a l u a te t h e p o s t g l e n o i d s p i n e , a n d

3 sec t i o n s p e r j o i n t w e re u sed fo r t h e o ss i f ied

c a r t il a g e a n d p o s t e r i o r b o r d e r o f t h e m a n d i b l e .

T o u s e t h e c h i - s q u a r e a n a l y s i s , t h e c o m b i n e d

r e a d i n g s o f e a c h j o i n t a n d r a m u s w e r e c o l l a p s e d

in to e i ther a 0-1 or 2-3 ca tegory . Occasional ly ,

t h e c o m b i n e d r a t i n g f o r a j o i n t o r r a m u s w as

b e tw een t h e 0 -1 o r 2 -3 ca t eg o ry . In t h e se i n -

s t an ces , t h e p a r t i cu l a r j o i n t o r ran ms w as e l imi -

n a t ed f ro m th e ch i - sq u a re an a ly s i s .

T o e v a l u a t e d i f f e r e n c e s a m o n g t h e e x p e r i -

me n ta l g ro u p s , a 2 × 4 ch i - sq u a re t e s t w as u sed .

Ev en w i th sma l l samp le s i ze , t h e se t e s t s ad e -

q u a t e l y p r o t e c t a g a i n s t i n c o r r e c t l y r e j e c t i n g t h e

n u l l h y p o th es i s ( i e, co m mi t t i n g a t y p e I e r ro r ). 4 6

T o c o m p a r e t h e r e sp e c ti v e e x p e r i m e n t a l g r o u p s

w i th t h e co n t ro l g ro u p , a 2 × 2 ch i - sq u a re t e s t

w as u sed . Becau se ad e q u ac y o f p o w er i s a t is-

sue , 7 w e d id n o t c o r re c t t h e t ex t s ta t is t ic s o r u se

Fi sh e r s ex ac t p ro b ab i l i t y t es t. 4s

T h e e r r o r o f th e m e a s u r e m e n t f o r th e q u a n -

t it at iv e d a t a w as d e t e r m i n e d b y r e p e a t i n g t h e

m e a s u r i n g o f 10 c o n t r o l a n d 1 0 e x p e r i m e n t a l

sec t i on s . Th e e r r o r w as w i th in acc ep t ab l e l imi ts .

R e s u l t s

A l t h o u g h t h e g e n e r a l a n a t o m i c c o n f i g u r a t i on o f

t h e t e m p o r o m a n d i b u l a r j o i n t o f th e m o n k e y is

s i m i l ar t o t h a t o f m a n , t h e r e a r e s o m e s t r u c t u r a l

d i ff e r en c e s. T h e t e m p o r o m a n d i b u l a r j o i n t r e -

g i o n s o f b o t h s p e c ie s a r e c h a r a c t e r i z e d b y th e

p r e s e n c e o f a m a n d i b u l a r c o n d y le , a r t i c ul a r

d i sk , g l en o id fo ssa , an d a r t i cu l a r emin en ce (F ig

2 A ). T h e m o s t s tr i k i ng d i f f e r e n c e b e t w e e n t h e 2

sp ec i e s i s t h e p o s tg l en o id sp in e , a v e r t i ca l s t ru c -

t u r e t h a t is l o c a t e d j u s t a n t e r i o r t o t h e e x t e r n a l

a u d i t o r y m e a t u s .

Th e re su l t s f ro m th i s s t u d y w il l b e co n s id e red

a c c o r d i n g t o e a c h a n a t o m i c a r e a ( i e , a r t i c u l a r

an d ca r t i l ag in o u s t i ssu es o f t h e co n d y le , p o s tg l e -

n o id sp in e , co n d y la r t i s su es b en ea th t h e ca r t i -

l a ge , a n d t h e p o s t e r i o r b o r d e r o f t h e m a n d i b u -

l a r r a m u s ) .

Figure 2. The tem por om and ibu larj oin t of a juvenile control animal. Lower power view shows the man dibular

condyle, the articular disk and retrodiscal region, the articular eminence, and the postglenoid spine. The external

auditory meatus (not shown) is located posterior to the postglenoid spine (A). Highe r power view showing the

art icular carti lage covering the m andib ular condyle and the prechondrob last ic-chondroblast ic layer of condylar

cartilage overlying the bony trabeculae of the condyle. The retrodiscal region also can be observed (B).

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TemporomandibularJoint AdaptatioT~s 7

Condylar Cartilage

Two dist inct soft- t issue layers were identif ied in

th e e x t e rn a l su r f a ce s o f t h e m a n d ib u la r c o n d y le

(F ig 2B) , the condy la r ca r t i lage layer covered by

the dense a r t icu la r t i s sue layer . The condyla r

car t i lage resem bled ac t ive ly g rowing seco ndary

car t i lage and was d iv ided a rb i t ra r i ly in to p re -

c h o n d ro b la s t i c a n d c h o n d ro b la s t i c z o n e s . T h e

th ickes t por t ion of the ca r t i lage was ib un d in the

pos te ros upe r io r a rea (312 /~m) of the condyle

fo l lowed by the pos te r io r (272 ~m) and su per io r

(248/~m ) reg ions (F ig 3 ) .

T h e h y p e rp l a s i a a n d h y p e r t ro p h y o f t h e p r e -

chon drobl as t ic a nd ch ondro blas t ic layers o f ca r-

t i lage was ev iden t in bo th the p os te r io r and pos-

te rosuper io r a reas by th ree weeks (F ig 4 ) . The

increase in ca r t i lage th ickness was s ign i f ican t

par t icu la r ly in the pos te r io r reg ion , in which the

mean wid th increased f rom 279 /~m to 511 /~m

(Fig 3) . In con tras t to these 2 areas, however, the

min ima l wid th increase in the th ickness o f the

supe r io r ca r t i lage was no t s ta ti s t ica l ly s ign i f ican t

(Table 1).

T h e a d a p t iv e h y p e rp l a s i a a n d h y p e r t ro p h y o f

the condyla r ca r t i lage var ied f rom 6 (F ig 5 ) , 12

(Fig 6) , and 24 (Fig 7) weeks after appliance

p la c e m e n t . O n th e su p e r io r p o r t i o n o f t h e co n -

dy le , the ca r t i lage decreas ed in wid th (P < . 05)

br ie f ly a t 6 weeks bu t then resu med a wid th tha t

was no t s ign i f ican t ly d i f fe ren t f i om the con t ro ls

in the 6-week ( P < .001), 12-week ( P < .01) and

24-week (p < .01) in tervals (Fig 3, Tab les 1 an d

2) . The car t i lage of the pos te r io r reg ion re -

sp o n d e d in a m a n n e r s im i l a r t o t h e p o s t e ro su -

per io r aspec t , excep t a t the 12 th-week per iod

w h e n th e w id th d i f f e r e n c e f ro m th e c o n t ro l w a s

signif ic ant a t only P < .05 (Fig 3, Tables 1 an d

2). Thus, i t can be seen that the adaptive re-

sp o n se o f t h e p o s t e r io r a n d p o s t e ro su p e r io r c o n -

dy la r ca r t i lage was s ign if ican t ly g rea te r in exper -

imenta l an imals than in the con t ro ls .

rticular Tissue

The a r t icu la r t i s sue (F ig 2B) cons is ted of dense

i r regu la r connec t ive t i s sue wi th f ibers genera l ly

ar ranged para l le l to the ca r t i lag inous sur face o f

the condyle . The wid th o f th is t i s sue var ied , w i th

the pos te r io r a rea be ing th ickes t (116 .4 /xm) ,

d im in i sh in g in t h e p o s t e r io r su p e r io r r e g io n ,

and be ing th in nes t in the super io r zone (F ig 3 ) .

T h e a n im a l s t e rm in a t e d a f t e r w e a r in g th e

Herbs t app l iance fo r 3 weeks (F ig 4 ) showed

signif icant , a l though variable , increases in art ic-

u la r t i s sue wid th (F ig 3 ) . The pos te r io r snper io r

and super io r a reas th icken ed mo re (P < . 001)

than d id the p os te r io r a r t icu la r t i s sues (P < . 05) .

Af te r the in i t ia l w iden ing of the a r t icu la r t i s sue

observed a t 3 weeks , however , these connec t ive

500 F, rn PostedorARicular 500 F/am Posterosuperior Adieular 500

400 400 [ - 400

300 300 ~ 300

200 200 200

100 ~ - ~ / ~ ] l ~ T ~ 100 ~00

~

0

Control 3 Wk 6 Wk 12V@ 24'¢~ Control 3 Wk 6 Wk 12W k 24Wk

,urn Superior Arlicular

i i l i l l i l i .

Control 3 Wk 6 Wk 12Wk 24Wk

500 500

400

300

200

100

0

PosterosuperiorCondylar

400 ~ 400

300 300

200 200

tO0 100

0 0

Control 3 Wk 6 Wk 12 Wk 24'~& Control 3 Wk 6 Wk 12Wk 24Wk Conlrol 3 Wk 6 Wk 12Wk 24Wk

500

Figure 3. Graphic representation of the relative thicknesses of the articular and condylar cartilages of the

ma ndib ular condyle, as deter mi ned by the B ioquant mea suring system. For each condy le, the thicknesses were

determined at 3 regions: superior, posterosuperior, and posterior.

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8 P e t e r s o n a n d M c N a m a r a

Figure 4. The tem por oma ndi bul arj oin t region of two 3-week experimental animals. Lower power views of the

overall condylar morphology. Note the t hick enin g of the condylar cartilage in both views A and C). Increased

bone deposition can be observed along tile anterior borde r of the postglenoid spine. Increased bone deposition

alon g the posteri or bord er of the gl enoid fossa also can be observed A and C). H igher power views of the

man dib ula r condyles of the same 2 animals B and D).

t issues maintained a thickness that was not s ta-

t ist ical ly signif icantly differ ent from the controls .

The cons is tency in a r t icu lar width con t in ued

through the 6 th and 12th exper i menta l week

and for the posteri or ar t icular area even to the

24th week Fig 3) . I t shoul d be noted that even

though the art icular t issue widths of the poste-

r ior superio r areas were different from the con-

Table 1

Juveni le Control Versus Juven ile Experimen tal t test)

3 wk n - 8 ) 6 wk n = 12) 12 wk n - 12) 24 wk n = 8)

Posterior

articular cartilage * NS NS NS

Posterosuperior

articular cartilage + NS NS ,~

Superior

articular cartilage + NS NS ++

Posterior

condylar cartilage ~ .+ * ~-

Posterosuperior

condylar cartilage + +* ~- ~-

Superior

condylar cartilage NS * NS NS

Abbreviations: NS, not significant; n, number of temporal mandibular oints includes right and left joints).

*P < .05.

tP < .01.

~P < .001.

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TemporomandibularJoint Adaptatio ns

19

F i g u r e 5 . T h e t e mp o r o m a n d i b u l a r j o i n t r e g i o n o f a 6 -w e ek e x p e r i me n t a l a n ima l . L o w e r p o w e r A ) . H i g h e r

p o w e r o f t h e ma n d i b u l a r c o n d y l e. N o t e t h e e n d o c h o n d r a l b o n e f o r m a t i o n o c c u r r i n g u n d e r t h e p r o l i f e r a ti o n o f

the cond y lar car t i l age . I s l ands o f ca lc i f i ed car t i l age mat r ix can be observed wi th in the t rabecu lae B) .

F i g u r e 6 . T i l e t e m p o r o ma n d i b u l a r j o i n t r e g i o n o f a 1 2- we ek e x p e r i me n t a l a n i ma l . L o w e r p o w e r v ie w th a t

t ea tu res an increase p ro l i fe ra t ion o f the condy lar car t i l age , par t i cu lar ly in the pos te r io r reg ion o f the condv le

A ) . H i g h e r p o w e r v ie w o f t h e ma n d i b u l a r c o n d y l e f r o m t h e s a me j o i n t B) . H i g h e r p o w e r v ie w o f t h e p o s t e r i o r

r a ma l a r e a f r om t h e s a me j o i n t C) . Bo th i n t r a m e mb r a n o u s a n d e n d o c h o n d r a l b o n e d e p o s i t i o n is e ~. id en t.

H i g h e r p o w e r vi ew o f ma n d i b u l a r c o n d y l e f ro m a c o n t r o l a n i ma l D ) .

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9 Peterson and McNamara

Figure 7. T he tem poro ma ndib ular joi nt reg ion of a 24-week experimen tal animal. Lower power view of the

temp orom andib ular join t region. The postglenoid spine is not present in th is medial section A). Higher power

view of the man dibular condyle. Note the increased thickness of the condylar cartilage B).

t ro i s P < .001) , t he i r mea n va lues were l ess than

the con t ro l s Tab le 1 ) .

Postglenoid Spine

Typica l ly , t he pos te r io r su r f ace o f the pos tg le -

n o i d s p i n e i n t h e c o n t r o l a n i m a l s w a s q u i e s c e n t ,

i n t h a t n o d e p o s i t i o n o r r e s o r p t i o n o f b o n e w as

e v i d e n t in a n y o f t h e s e c t i o ns a n a l y z e d T a b l e 3 ).

I n c o n t r a s t , t h e p o s t e r i o r s u r f a c e o f t h e p o s t gl e -

n o i d s p i n e s h o w e d a s i g n i f i c a n t i n c r e a s e i n r e -

so rp t ion fo r the 3 -, 6 -, an d 12-week ex per im en t a l

g r o u p s ; t h e 2 4 - w ee k e x p e r i m e n t a l g r o u p w a s n o t

s i g n if i ca n t ly d i f f e r e n t f r o m c o n t r o l s . I n c o n t r a s t ,

t h e p o s t e r i o r s u r f a c e s h o w e d n o s i g n i f i c a n t d i f -

f e r e n c e s b e t w e e n a n y o f t h e g r o u p s w h e n e x a m -

i n e d f o r b o n y a p p o s i t i o n a l a ct iv it y.

I n t h e c o n t r o l a n i m a l s , b o n e d e p o s i t i o n w a s

n o t e v i d e n t a lo n g t h e a n t e r i o r s u r fa c e o f t h e

p o s t g l e n o i d s p i n e ; h o w e v e r , a r ea s o f b o n e r e-

s o r p t i o n w e r e p r e s e n t a l o n g t h i s s u r f a c e . A

s i g n i f i c a n t i n c r e a s e i n b o n e d e p o s i t i o n a c t i v i t y

b e g a n t o t a k e p l a c e i m m e d i a t e l y i n t h e e x p e r i -

m e n t a l g r o u p s F ig 8 ) a n d c o n t i n u e d t o b e sig -

n i f ic a n t ly g r e a t e r t h a n c o n t r o l s t h r o u g h t h e 1 2 t h

e x p e r i m e n t a l w e e k T a b l e s 3 a n d 4 ) . I t is i n t e r-

es t ing to no te tha t t he l eve l o f s ign i f icance de-

c l i n e d d u r i n g t h e 1 2 t h e x p e r i m e n t a l w e e k a n d

d i s a p p e a r e d a l t o g e t h e r a t t h e 2 4 t h w e e k . I n c o n -

t ra s t, t h e p o s t e r i o r s u r f a c e o f t h e p o s t g l e n o i d

sp ine show ed n o s ign i f i can t r eso rp t ive ac t iv i ty in

c o n t r o l o r e x p e r i m e n t a l a n i m a l s u n t i l t h e 2 4 t h

w e e k o f a p p l i a n c e u s e w as r e a c h e d . A t t h is p o i n t ,

h a l f o f th e s p e c i m e n s e x a m i n e d s h o w e d p o s te -

r i o r s u r f a c e r e s o r p t i o n .

ony Cap

T h e p r e s e n c e o r a b s e n c e o f a c o a l e s ce d b o n y

c a p a r e a b e l o w t h e c o n d y l a r c ar t il a g e m a y b e a n

i n d i c a t o r o f t h e d e g r e e o f b o n e f o r m a t i o n a c ti v-

it y. T h e r e w as n o t s i g n i fi c a n t e v i d e n c e o f a b o n y

c a p f o r e i t h e r t h e c o n t r o l o r e x p e r i m e n t a l

g r o u p s T a b l e s 3 a n d 4 ) .

Ossified

Car t i l age

Car t i l age , which is ac tive ly p ro l i f e r a t ing a nd

f i m c t i o n i n g a s a p r o g e n i t o r o f ne w b o n e , u n d e r -

goes severa l morpho log ic s t ages . The l as t s t age ,

w h i c h o c c u r s j u s t b e f o r e o s s if i ca t io n a n d t r a b ec -

u l a e f o r m a t i o n , h a s b e e n d e f i n e d a s os s i fi e d ca r-

Table

2. Least Squares Regres sion Analysis 3 Weeks, 6 Weeks, 12 Weeks, and 24 Weeks)

Posterior Post Sup. Superior Posterior Post Sup. Superior

Articular Articular Articular Condylar Condylar Condylar

Cartilage Cartilage Cartilage Cartilage Cartilage Cartilage

Juv en i le Exp . NS + ~ ~- -~

P < .05.

+p < .-1.

++P < .00 1,

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TemporomandibularJoint daptations 21

d i b u l a r p o s t u r e i n g r o w i n g n o n h u m a n p r i -

mates.:~8,4°,41,49

Figure 8. Postglenoid spine of a control juvenile Rhe-

sus monkey. Neithe r the anterior right) n or poste-

rior left) surfaces of the spine show evidence of bone

deposit ion or resorption A). Postglenoid spine of a

3-week experim ental animal B). Deposit ion D) of

new bone is occurring a long the anterior a spect of the

postglenoid spine; resorption R) of bone occurs

along i ts posterior border.

t i lag e , w ith t h e p re s en c e o f ca lc i f i ed ca r t i l ag e

ma t r i x ev id en t . Th i s s t ag e ap p ea rs t o b e an i n -

d i c a t o r o f a c ti v e b o n e f o r m a t i o n . B o t h c o n t r o l

a n d e x p e r i m e n t a l g r o u p s s h o w e d s i g n i f i c a n t

a m o u n t o f o s s if i ed c a rt i la g e , i n c l u d i n g t r a p p e d

i s l an ds o f cal c i f ied ca r t i l ag e ma t r i x . T h e re w ere

n o s i g n i f i c a n t d i f f e r e n c e s b e t w e e n t h e g r o u p s ,

h o w e v e r Tab l e s 3 an d 4 , F ig 9 ) .

P os te r ior Bor de r o f the Mandibu lar Ramus

T h e p o s t e r i o r b o r d e r o f t h e m a n d i b u l a r r a m u s

w a s e x a m i n e d f o r r e s o r p t i v e a n d a p p o s i t i o n a l

ac ti vi ty . Th e ram u s sh o w ed e ssen t ia l l y n o re so rp -

t i o n i n an y g ro u p , w i th n o s i g n i f i can t d i f fe ren c e

b e t w e e n c o n t r o l a n d e x p e r i m e n t a l g r o u p s .

Th e re w as , h o w ev e r , a s i g n i f i can t i n c rease i n t h e

am o u n t o f ap p o s i t i o n a l ac ti v it y i n t h e 3 - an d

6 -w ee k e x p e r i m e n t a l g r o u p s w h e n c o m p a r e d

w i th co n t ro l s . By t h e t im e t h e 1 2 th an d 2 4 th

e x p e r i m e n t a l w e e k s w e r e r e a c h e d , t h e r e o n c e

a g a i n w e r e n o s i g n i f i c a n t d i f f e r e n c e s f r o m c o n -

t ro ls Tables 3 an d 4 , Fig 10) .

i s cuss ion

Th e re su l t s o f t h is s t u d y a re s imi l a r t o o u r p re -

v i ou s e x p e r i m e n t a l s t u di e s o f a d a p t a t i o n o c c u r -

r i n g w i th in t h e t e m p o r o m a n d i b u l a r j o i n t a n d

in f ra t emp o ra l t o s sa a f t e r a l t e ra t i o n s i n man

Condylar Adaptat ions

T h e a d a p t i v e r e s p o n s e s o b s e r v e d i n t h e p r e -

c h o n d r o h l a s t i c a n d c h o n d r o b l a s t i c l ay e rs o f t h e

c o n d y l a r c a r t i l a g e r e a c h e d a m a x i n m m a t 3

w eek s an d g en e ra l l y d imin i sh ed i n i n t en s i t y a f t e r

t h a t t ime . Th e ex cep t i o n t o t h i s o b se rv a t i o n w as

in t h e su p e r io r ca r t i l ag in o u s a rea , i n w h ich t h e

o n ly s t a t i s t i c a l l y s i g n i f i can t d i f fe ren ce b e tw een

c o n t r o l s a n d e x p e r i m e n t a l a n i m a l s o c c u r r e d a t 6

w eek s w h e n t h e w id th o f t h e ca r t i l ag e d ec rea sed .

Prev io u s s t u d i e s b y Mc N a ma ra an d Bry an 4~ i n d i-

c a t e th a t t h e l e n g t h o f th e m a n d i b l e c a n b e

in c reased s i g n i fi can t ly i e, 5 -6 m m) o v e r co n t ro l

v a lu e s a t t h e e n d o f th e g r o w t h p e r i o d w h e n

a f lmc t io n a l l y p ro t ru s iv e ap p l i an ce i s u sed i n

g r o w i n g m o n k e y s .

Th e a r t i cu l a r t i s su es o v e r ly in g t h e co n d y la r

c a r t i l a g e a l s o r e s p o n d e d s o m e w h a t t o t h e

c h a n g e i n m a n d i b u l a r p o s t u r e . T h e r e w as a s ig -

n i f i can t i n c rease i n t h e w id th o f t h e a r t i cu l a r

t i s su e a t 3 w eek s , b u t su b seq u en t ly i t d imin i sh ed

to a wid th s imi lar to tha t o f cont ro ls . I t i s in ter-

e s t i n g , h o w ev e r , t h a t t h e 2 4 -w eek ex p e r imen ta l

v a lu e s f o r th e p o s t e r o s u p e r i o r a n d s u p e r i o r a >

t icn lar zones were s ign i f ican t ly less than the con-

trol widths.

Th e o b smw at io n s t h a t g en e ra l l y sh o w th e ca r -

t i lage and ar t icu lar t i ssues to increase in wid th

th e m o s t d u r in g t h e f i rs t f ew w eek s o f ap p l i a n ce

w e a r p e r h a p s c a n b e e x p l a i n e d a s t b l l o w s : b o n y

d e v e l o p m e n t i n t h e c o n d y l e is p r e c e d e d b y t h e

p r o l i f e r a t i o n a n d m a t u r a t i o n o f s e c o n d a W c o n -

d y l a r ca r t i l ag e . O u r d a t a sh o w th e p ro l i fe ra t i v e

e f f e c t t h a t a f o rw a r d p o s i t i o n i n g o f t he m a n d i b l e

in i ti a te s . Th e re may b e , h o w ev e r , a l ag p e r io d

b e tw e en t h e t im e w h e n ca r t i l ag e p ro l i fe ra t i o n is

e s t a b l i s h e d a n d w h e n t h e s u b s e q u e n t b o n e f o r -

ma t io n b eg in s . Th u s , i t i s p o ss ib l e t h a t b o n e

fo rma t io n p l ay s ca t ch -u p fo r sev e ra l w eek s , an d

th e ca r t i l ag e l ay e rs w ill ap p e a r t o b e re tu rn in g t o

a w id th s imi l a r t o co n t ro l s . Th i s o b se rv a t i o n

sh o u ld n o t b e i n t e rp re t ed n ecessa r i l y a s a s l o w -

i n g d o w n o f c a r ti l ag e p r o l i f e r a t i o n b u t r a t h e r a n

i n d i c a t o r t h a t b o n y t r a b e c u l a r f o r m a t i o n h a s

c a u g h t u p a n d i s n o w k e e p i n g p a c e w i t h t h e

i n c r e a s e d r a t e o f c a r ti l a ge f o r m a t i o n .

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P e t e r s o n a n d M c N a m a r a

T a b l e 3 . J u v e n i l e C o n t r o l a n d E x p e r i m e n t a l D a t a I n d i c a t i n g t h e P r e s e n c e o r A b s e n c e o f C e r t a i n H i s t o lo g i c a l

C h a r a c t e r i s t i c s f o r t h e A n a t o m i c A r e a s L i s t e d

3 - w k 6 - w k 1 2 - w k 2 4 - w k

Control Experiment Experiment E xperiment Experiment

Ana tomic Areas n n n n n

P o s t g l e n o id s p i n e - p o s t e r i o r

s u r f a c e r e s o r p t i o n

0 1 17 100 5 62 3 43 4 57 6 86

2-3 0 0 3 38 4 57 3 43 1 14

P o s t g l e n o i d s p i n e - p o s t e r i o r

s u r f a c e a p p o s i t i o n

0-1 19 100 8 100 8 100 8 89 7 88

2-3 0 0 0 0 0 0 1 11 1 12

P o s t g le n o i d s p i n e - a n t e r i o r


0-1 15 88 8 100 8 100 8 89 4 50

2-3 2 12 0 0 0 0 1 11 4 50


s u r f a c e a p p o s i t i o n

0-1 19 100 0 0 0 0 7 78 7 100

2-3 0 0 8 100 4 100 2 22 0 0

P r e s e n c e o f b o n y c a p - c o n d y l e

Yes 1 5 0 0 0 0 0 0 0 0

N o 1 8 9 5 8 1 0 0 1 2 1 0 0 1 2 1 0 0 8 1 0 0

O s s i f ie d c a r t i l a g e - c o n d y l e

0 1 1 6 0 0 0 0 0 0 0 0

2-3 17 94 8 100 12 100 12 100 8 100

P o s t er i o r b o r d e r o f r a m u s -

r e s o r p t i o n

0-1 18 95 8 100 12 100 11 92 8 100

2-3 1 5 0 0 0 0 1 8 0 0

P o s t er i o r b o r d e r o f r a m u s -

a p p o s i t i o n

0-1 11 73 0 0 2 18 8 73 4 57

2-3 4 27 8 100 9 82 3 27 3 43

A b b r e v i a t i o n s : n , n u m b e r o f t e m p o r a l m a n d i b u l a r j o i n t s f o r e a c h c a t e g o r y i n c l u d e s r i g h t a n d l e ft ); 0 -1 , n o n e - m i n i m a l ; 2 -3 ,

m o d e r a t e - e x t e n s i v e .

N o t e . T w o o r 3 s l i d e s w e r e e v a l u a t e d f o r e a c h j o i n t a r e a a n d j u d g e d c o l l e c ti v e l y to b e e i t h e r i n t h e 0 -1 o r 2 - 3 c a te g o ry , . I f t h e y

w e r e j u d g e d t o b e b e t w e e n t h e 2 c a te g o r i e s , th e y w e r e o m i t t e d f r o m t h e a b o v e d a t a c o m p i l a t i o n a n d c h i - s q u a r e a n a l ys is .

T a b l e 4 . C h i - S q u a r e T e s t f o r S t a t i s ti c a l S i g n i f i c a n c e f o r I n d i v i d u a l A n a t o m i c A r e a s

Anatomical Areas

Chi-Square (Control Group Compared With Each Experimental 2× 4 Chi-Square al l 4

Czroup lndividuaUy) Experimental (~o ups

3 - w k 6 - w k 1 2 - w k 2 4 - w k G r ou p C o m pa re d

Experiment Experiment Experiment Experiment Am ong Themselves




s u r f a c e a p p o s i t i o n N S


s u r f a c e r e s o r p t i o n N S


s u r f a c e a p p o s i t i o n ++

P r e se n c e o f b o n y c a p ~ o n d y l e N S

O s s i f ie d c a r t i l a g e - c o n d y l e N S

P o st . b o r d e r o f r a m u s - r e s o r p t i o n N S

P o s t. b o r d e r o f r a m u s - a p p o s i t i o n ++

t S S

N S N S N S N S

N S N S * *

N A * N S {

N S N S N S N S

N S N S N S N S

N S N S N S N S

t N S N S t

A b b r e v i a t i o n s : n , n u m b e r o f t e m p o r a l m a n d i b u l a r j o i n t s f o r e a c h c a t e g o r y i n c l u d e s r i g h t a n d l e ft ); N S , n o t s i g n i fi c a n t ; N A =

c h i - s q u a r e n o t a p p r o p r i a t e t o c a lc u l a t e b e c a u s e o f e x ce s s iv e z e r o s in t h e 2 x 2 c o n f i g u r a t i o n .

* P < . 0 5 .

t P < . 0 1 .

+ P < . 0 0 1 .

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TemporomandibularJoint Ad tations

23

Figure 9. Mandibular condyle of 6-week experimen-

tal animal showing many areas of calcified cartilage

matrix within the bony trabecnlae.

Temporal daptations

A p r o m i n e n t a n a t o m i c f e a t u r e o f th e R h e s us

mo n k ey i s t h e p o s tg l en o id sp in e , w h ich i s l o -

ca t ed p o s t e r i o r l y an d l a t e ra l l y t o t h e g l en o id

fo ssa (F ig s 2 an d 8 ) . D ep o s i t i o n o f n ew b o n e

a l o n g t h e a n t e r i o r s u r f a c e o f t h e p o s t g l e n o i d

s p i n e c a n b e c o n s i d e r e d e v i d e n c e t h a t a n a n t e -

r i o r r e p o s i t i o n i n g o f t h e g l e n o i d f o ss a o c c u r r e d ,

as or ig ina l ly des cr i bed by Bre i tne r ~2~24 in the

1930s.

In t h e cu r ren t s t u d y , t h e p o s t e r i o r su r face o f

t h e p o s tg l en o id sp in e b eg an t o u n d e r g o s i g n i f -

i c a n t s u r f a c e r e s o r p t i o n a t t h r e e w e e k s a n d c o n -

t i n n e d t o d o s o t h r o u g h t h e 1 2 th e x p e r i m e n t a l

w e e k. T h e p o s t e r i o r s u r f a c e o f t h e p o s t g l e n o i d

sp in e , h o w ev e r , d id n o t sh o w an y s i g n i f i can t ap -

p o s i t i o n a l ac t i v i t y . In co n t ra s t , t h e an t e r i o r su r -

f a c e o f th e p o s t g l e n o i d s p i n e s h o w e d s i g n if i c a nt

b o n y a p p o s i t i o n d u r i n g t h e s a m e p e r i o d b u t d i d

n o t s h o w a n y d e g r e e o f r e s o r p t i o n u n t i l t h e 2 4 t h

w e e k . It w o u l d a p p e a r f r o m t h e s e o b s e r v a t i on s

t h a t t h e p o s t g l e n o i d s p i n e a n d t h e r e f o r e t h e

g l e n o i d f o s s a r e s p o n d e d t o t he f o r w a r d p o s i t i o n -

i n g o f t h e m a n d i b l e b y m i g r a t i n g m o r e a n t e r i -

o r l y . Th i s o b se rv a t i o n i s co n s i s t en t w i th o u r ea r -

l i e r f i n d in g s o n b o n y a l t e ra t i o n s seco n d a ry t o

pro t rus ive fun ct io n , :~ z~.~ - as well as with tho se of

W o o d s i d e a n d c o w o r k e r s . ~

Mandibular Ramus

T h e p o s t e r i o r b o r d e r o f t h e r a m u s a l so s ho w e d

s i gn s o f r e s p o n d i n g t o t h e f o r w a r d p o s i t i o n i n g

o f t h e man d ib l e . Th i s w as ev id en ced b y a s i g n i f -

i c a n t in c r e a s e i n t h e a m o u n t o f b o n y a p p o s i t i o n

th a t o ccu r re d t h ro u g h t h e f i r st 6 w eek s o f t h e

s tu d y. T h i s b o n y a p p o s i t i o n o f t h e r a m u s c o n t i n -

u e d t h r o u g h o u t t h e e x p e r i m e n t a l p e r i o d , b u t b y

th e 1 2 th an d 2 4 th w eek p e r io d s , i t h ad re tu r n ed

to a d eg ree o f act i vi t y s imi l a r t o t h e co n t ro l s .

T h e s e f i n d i n g s c o n c e r n i n g f o r c e d p r o t r u s i o n

a l so a re c o n s i s t en t w i th o u r ea r l i e r s t u d i e s i n v o lv-

ing th e f im ct ion al p r o t r us ion mo del . ~9,41,m

Summary and onclusion s

Th e p u r p o s e o f th i s s tu d y was t o ev a lu a t e h i s to -

l o gi c al ly t h e t e m p o r o m a n d i b u l a r j o i n t , g l e n o i d

f os s a, a n d t h e p o s t e r i o r b o r d e r o f t h e m a n d i b l e

i n j n v e n i l e R h e s u s m o n k e y s w h o s e m a n d i b l e s

h a d b e e n p o s i t i o n e d f o r w a r d w i th a H e r b s t a p -

p l i an ce . A c ry l i c sp l i n t H e rb s t ap p l i an ces w ere

b o n d e d t o t h e u p p e r a n d l o w e r d e n t a l a r c h e s o f

2 0 ma le j u v en i l e an im a l s . Th e an ima l s w ere t e r -

m in at ed at 3-, 6-, 12- an d 24-we ek intelw als af ter

a p p l i a n c e p l a c e m e n t . S e v en m a l e j u v e n i l e R h e -

s u s m o n k e y s s e r v e d a s c o n t r o l s . T h e t e m p o r o -

m a n d i b u l a r j o i n t , i n f r a t e m p o r a l f o s s a a r e a , a n d

t h e p o s t e r i o r b o r d e r o f th e r a m u s t h e n w e r e

p rep a red f i ) r an d an a ly zed h i s t o lo g i ca l l y .

Th e re su l ts o f th i s s t u d y in d i ca t e t h a t b o th

c o n d y l a r t e m p o r a l b o n e a n d m a n d i b u l a r r a m u s

a d a p t a t i o n s o c c u r a f t e r p l a c e m e n t o f t h e H e r b s t

appl iance . The fb l lo~4ng adapta t ions were ob-

served:

Figure 10. Deposit ion of new bone along the poste-

rior border of the mandibular ramus in a 3-week

experimental animal (A). Deposit ion of new bone

along the poster ior border of the m andibular ramus

in a 12-week animal. The bony architecture is more

organized than that ira the 3-week animal (B).

7/17/2019 1-s2.0-S107387460200004X-main


4 P e te rs o n a n d c N a m a r a

1 . I ncr ea s ed p ro l i f era t i o n o f the co nd y l a r car t i

l a g e w a s n o t e d . T h e s e a d a p t a t i o n s o c c u r r e d

p r im a r i l y i n t h e p o s t e r i o r a n d p o s t e r o s u p e

r i o r r e g i o n s o f t h e c o n d y l e .

2 . S i g n i f i c a n t d e p o s i t i o n o f n e w b o n e o n t h e

a n t e r i o r s u r f a c e o f t h e p o s t g l e n o i d s p i n e o c -

c u r r e d , i n d i c a t i n g a n a n t e r i o r r e p o s i t i o n i n g

o f t h e g l e n o i d f o ss a .

3 . S ig n i f i c a n t b o n e r e s o r p t i o n o n t h e p o s t e r i o r

s u r f a c e o f t h e p o s t g l e n o i d s p i n e w a s n o t e d .

4 . S i g n i f i c a n t b o n y a p p o s i t i o n o n t h e p o s t e r i o r

b o r d e r o f t h e m a n d i b u l a r r a m u s w a s e v i d e n t

d u r i n g e a r l y e x p e r i m e n t a l p e r i o d s .

5 . N o g r o s s o r m i c r o s c o p i c p a t h o l o g i c a l c h a n g e s

w e r e n o t e d i n t h e t e m p o r o m a n d i b u l a r j o i n t

o f t h e j u v e n i l e R h e s u s m o n k e y .

T h e r e s u l t o f a n y s t u d y in a n i m a l s , e v e n i n

n o n h u m a n p r i m a t e s , c a n n o t b e a p p l i e d d i r e c t l y

t o h u m a n o r t h o p e d i c t r e a t m e n t . B e c a u s e t h e

t is s u e ty p e s a n d t h e m o r p h o l o g y o f t h e t e m p o r o -

m a n d i b u l a r j o i n t a r e s i m i l a r b e t w e e n m o n k e y

a n d m a n , h o w e v e r , t h e f i n d i n g s o f t h e p r e s e n t

s t u d y c a n b e u s e d t o s h e d l i g h t o n t h e c h a n g e s

o c c u r r i n g i n t h e t e m p o r o m a n d i b u l a r j o i n t r e -

g i o n f o l l o w i n g H e r b s t a p p l i a n c e t h e r a p y i n

g r o w i n g p a t i e n t s .

A c k n o w l e d g m e n t s

T h e a u th o r s w i s h to th a n k D r B a rb a ra N e s b i t t E m e r ic k fo r

h e r in v a lu a b le t e c h n ic a l s u p p o r t d u r in g th e e x p e r im e n ta l

phase o f th is p ro jec t .

R e f e r e n c e s

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m e t r i c i n v e s t ig a t io n . A m J O r th o d 1 9 79 ;7 6 :4 2 3-44 2 .

2 . P a n c h e r z H . T h e e f f e ct o f c o n t i n u o u s b i t e j u m p i n g o i l

t h e d e n to fa c ia l c o m p le x : a fo l lo w -u p stu d y a f t e r H e rb s t

a p p l i a n c e t r e a tm e n t o f C la s s I I m a lo c c lu s io n s . E u r

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3 . P a n c h e rz H . T h e m e c h a n i s m o f C las s I I c o r re c t io n in

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