embryogenesis of the human occipital bone shapiro

8/19/2019 Embryogenesis of the Human Occipital Bone Shapiro

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Am . 7 Roenigenol 1 26 : 1 06 3- 10 6

1 9 7 6

1063

E M B R Y O G E N E S IS O F T H E H U M A N O C C IP IT A L B O N E

A B S T R A C T :

R O B E R T S H A P IR O ’

A N D F R A N K L IN R O B IN S O N 2

F rom a n orig ina l s tu dy of fe ta l spe c im e ns , the e m bry og en es is o f the hu m a n o cc ip -

ita l bo ne is desc ribed . T he o cc ip ita l bon e in m an is de rived fro m cartilage , excep t

fo r the in ten pan ie tal segm en t w h ich has a m em branou s o rig in . N o rm a lly th ere is n o

m id lin e ce reb e llan fissu re o r sy nc ho nd ros is .

A n u nd ers ta nd ing o f th e em bry o lo g ic a l de -

ve lo pm en t o f the o cc ip ita l b on e is e ssen tia l

fo r an apprecia tion o f cnan io ven teb ral

an om alies an d oc cip ita l fra c tu re s . T h e

lite ra tu re co n ta in s in co ns is te nc ie s w ith re -

spe ct to the no m e nc la tu re a n d oss ific a tion

o f the v a riou s c om p one n ts o f th e o c cip ita l

bo ne , w h ic h a dd to th e co n fu sion [i-8 ]. T h e

fo llo w ing re po rt is b ase d up on ou r o w n

stud ie s a n d a tte m p ts to clarify th e inc on -

s is tencies .

M A T E R IA L S A N D M E T H O D S

A to ta l o f

I2 5

sk u lls w ere co llec ted from fe -

tu se s be tw ee n 8 an d

40 w eeks o f gesta tion .

T h ese sk u lls w e re p re pa re d in the d ry s ta te an d

rad io g rap hed in standa rd p ro jec tio ns. In ad d i-

tio n , a g roup 0130 c lea re d , a liz irin -s ta in ed feta l

sku lls o f v ary ing a ge p re pa red a cc o rd ing to the

c la ssical S pa lteho ltz techn iq ue w ere in vesti-

g ated . M ultip le co ro na l an d m id line sag itta l

sec tio ns o frep resen tativ e d eca lc ified fe tal sku lls

w ere em be dd e d in pa ra ffin a nd c ello id in . A g es

w e re

8 , io , I 2 , I 8 , 20 , 30 ,

an d

4 0 w eek s as as -

sessed b y c row n -rum p m e a su rem e n t. T h ese

w ere s tud ie d g ross ly a nd m ic ro sc op ic ally .

E M B R Y O L O G Y

T h e o cc ip i ta l bo ne is fo rm ed from th e

u n io n o f fo u r p rim a ry ca rtila g ino us c en ters

la id d ow n in the c ho nd roc ran ium aro un d

th e fo ra m e n m a gn um an d from a fifth

m e m bra no us e le m e n t (fig .

i).

T h us the

oc cip ita l b on e h as a du al o rig in fro m

c a rtila ge an d m e m b ran e. T h e fou r c an tila g i-

no us c om po ne n ts a re the ba s ioc cip ita l a n -

teno r to th e fo ram en m ag num , th e la tera l

on e xoc c ip ita ls on e ac h s id e o f th e fo ra m en

m agnu m , and th e sup naoccip ital p oste r io r

to th e fo ra m e n m a gn um (i.e ., the in ferio r

sq ua m a b elo w th e m e ndo sal su tu re). T he

m em branou s co m po nen t g ives rise to th e

F IG . i.-D iagram of ossifica tio n o f o ccip ita l bon e .

B as ioc cip ita l (z ), pa ired e xo ccip ita ls 2 a nd 3 ), an d

supraocc ip i ta l (4 de rived from cartilag e ; in terpa ri-

e tal ( d e rived fro m m em bran e. A rrow s p o in t to

m end osa l su tu re s w hich sepa rate in te rpan ieta l from

su prao ccip ital s eg m en t.

I

D e pa r tm e nt o f R a dio lo g y , H o sp ita l o f

S t. R ap hae l, Y ale U n ive rsity S ch ool o f M edicin e, N ew H a ven , C on nec tic u t

0 6 i .

2

D e pa r tm e nt o f N eu r o sur g e ry , H o sp ita l o f

S t. R ap h a el, Y ale U n iver sity S ch oo l of M ed ic in e , N ew H ave n , C o n n ec ticu t

0 6 i .


2/6

F IG . 2 .-P ho tog raph of base of 14 -w eek-o ld fe tal

sku ll p repared by S pa lteho ltz techn ique . B asiocc ip i-

ta l (b ) and pa ired la te ra l ex occip ita l cen ters (e) su r-

ro und fo ram en m agnum (fm ). N ote a lso ossifica tio n

o f g rea te r (G ) an d les ser a rrowhead) spheno ida l

w ings and pos tspheno id cen te rs

a rrow) an terio r to

basioccip i ta l

bone .

1064

SHAPIRO AND ROBINSON

in te rpan ie ta l bon e (i.e ., the supe rio r squam a

ab ov e th e m en do sal su tu re).

At

w eek s o f gestatio n , a sing le m ed ian

os sifica tion cen te r is p re sen t in th e ca rtilag -

ino us basiocc ipu t ven tra l to th e n o tocho rd

a nd in ea ch la tera l o cc ip ita l c art ila ge

arou nd the hyp og lo ssa l can al (f ig . 2).

In al l

the spe c im e ns , th e su p ra oc c ip ita l seg m e n t

also o ss ified fro m a sing le foc us in the

tec tum sy no ticum (i.e ., tha t po rtion o f the

chon droc ran ia l roo f conn ec ting th e aud i-

to ry b u lla e ). C oron al se c tion s a t th is fe ta l

s ta ge d em on stra te oss ific a tion in th e m e m -

bran ous in terpa rieta l segm en t as

w e l l

(f ig s .

3

an d 4).

B y

i 2 w eek s o f gesta tion , the in te rpa ri-

e ta l an d sup rao cc ip ita l se gm en ts ha v e

fu sed in the m id line bu t rem a in sep ara ted

la tera lly b y the m en dosal su tu re s (f ig .

.

O ssif ica tion in th e su prao cc ip ita l segm en t

is m ore adv an ced th an in the in te rpan ie tal.

A t

34 w eeks the re is fu rthe r u n ion o f the

in te rpan ieta l an d su prao cc ip i ta l segm en ts ,

an d th e m en do sa l su tu re s a re re du ce d to

na rrow slits . In som e spe cim e ns , a l ine ar

ve rtic a l s tr ip o f u no ss ified m e m bra ne is

presen t in th e m id line a lon g the sup erio r

m arg in o f th e in te rp an ieta l seg m en t. T h is

m ay oss ify la te r o r pe rs is t a t fu l l te rm .

S im ila r un oss if ied str ip s m ay o ccur e lse -

w he re in th e m e m bra no us in te rpa n ie ta l

seg m e n t. T h e se c a n b e m is ta ke n fo r fra c -

tu re s in the neo na tal p er iod .

In a few spe cim e ns (fou r in o u r se rie s),

th ere m ay be a m id lin e c le ft in the in fe rio r

m arg in o f th e su prao cc ip ita l bo ne (fig . 6 ).

F I G . 3 . - L O W

pow er co ron al sectio n of 1 0-w eek-o ld

hum an fe ta l cran iu m em bedded in para ffin an d

sta ine d w ith H an d E . F oc i o fo ss if ic atio n a rrowhead)

are se en in m em brano us p ort ion of o ccip ita l bone

above leve l o f ten to rium (‘F ) as w ell as in cho ndra l

po rtio n of oc cip i ta l bon e b elow ten to rium a rrow) .

C ro ssha tch ed arrow s o u tline a rea sho w n in h igh

po w er sectio n (f ig .

4).


3/6

-J

F io . -P ho to g rap h o f po ster io r aspect o f fe ta l

sku ll o f

12 w e eks g esta tio n

(Spa lteho ltz p repara -

tion ). ip = in terp arie ta l seg m e nt; so = supraoccip i ta l

se gm en t; e = ex occ ip i ta ls ; fm = fo ram e n m agn um ;

ar row heads

=

m e nd osa l su ture s; arro w s

=

inno m i na te

synchondrosis.

FIG . 4 .-H igh p ow er v iew o f oss ification a rrows)

in m em b ran ous portion of occ ip ita l bon e above ten -

to riu m (see fig . 3) .

E M B R Y O G E N E S IS O F O C C IP IT A L B O N E

io6

S uc h c le fts m ay pe rs is t o r su bseq ue n tly fil l

in w ith bon e . L ess com m on ly (tw o spec i-

m e n s), a sm a ll c en tra l bo ny pro jec tio n is

p re se n t o n the in fe rio r asp ec t o f th e su p ra -

oc c ip ita l seg m e n t (i.e ., K e rck n ing ’s bon e ;

fig s . 7 -9 ). R a re ly , the la tte r m ay be de -

tached an d lie in a ra the r b road m id line

c le ft. O n e or m ore acces so ry ossic le s m ay be

foun d in the in nom ina te syn ch ond ro sis b e-

tw e en the su p ra oc cip ita l a nd e xo cc ip i ta l

se g m e n ts (fig . io ). A c c o rd ing to C a ffey

[v ]

the se oss icle s usu ally fuse w ith the su pra -

occip ital bon e b y the end of the f irs t y ea r

o f life .

O ssif ica tio n o f th e k is ioccip ital segm en t

p roc ee ds la te ra l ly in to the v en tra l po rtion

o f ea ch co nd y le . S im u ltan e ous ly , o ssifica -

tion o f th e la te ra l o cc ip ita ls ad vances in to

the do rsa l po rtio n o f th e o c cip ita l co nd y le s

(f ig . I i). A t b irth , the b a sioc cip ita l a nd

la te ra l occ ip ita l bon es a re sepa rated on

e ac h s id e by a p rom in en t syn ch on dro sis .

F IG . 6 .-P ho to graph o f pos ter io r aspec t o f fe ta l

sku ll o f m on ths ges tation (S pa lteh o ltz p repara -

tion ). A rro w po in ts to c le ft in m idp ortion of in fe rio r

m a rgin ofsupraoc cip ita l seg m e nt. fm - fo ram en m ag -

n u m .


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Fic . 7 .-K erck ring’s b one a rrowhead) pro jec t ing

from infe rio r m arg in o fsu praocc ip ita l segm ent in

35 -

w eek-o ld fe tus. N o te ex occip ita l cen te rs o n e ith e r

side o f fo ram en m agnum (fm ).

F I G .

S .-E x ag gera ted W aters v iew of sku ll o f fu ll-

te rm stillbo rn in fan t d em onstra ting K erck rin g’s bo ne

a rrowheads) a lm os t com ple te ly fu sed to sup raocc i-

p ita l segm ent.

{ 149} K.

.

4 ’ ‘.:

i o66

SHAPIRO AND

R O B I N S O N

O blitera tio n o f the se sy nc ho nd rose s no r-

m a lly o c cu rs a t

2-4 years o f age .

T h e la te ra l

occip itals a re sep ara ted fro m th e sup ra -

oc cip ita l seg m en t b y the p rom in en t in -

nom in ate syn ch on dros is ; bon y fus io n o f

th ese seg m en ts a lso tak es p lac e be tw ee n 2

a nd y ea rs o f a ge . T h ere is an ad d it ion al

syncho nd ros is be tw een th e b asio cc ip u t and

th e ba s isph en o id (sp he no oc cip ita l syn ch on -

dros is). A cco rd in g to M elsen [io ] , o ssifica -

tion be tw een

th e sp he no id a nd oc c ip ita l

bo nes b eg ins at

12-13

yea rs o f age in g ir ls

an d

14-15

y ea rs in b oys . C o m ple te c losu re

of th e syn ch on dro s is do es n o t o cc u r un til

16-20

years o f age . O ccasiona lly the sphe -

noo cc ip itah sy nchon drosis pe rs is ts in to adu lt

l i fe .

A t b irth (fig .

i 2 ),

th e in te rpan ieta l and

sup raocc ip ita l segm en ts are fused , ex cep t

late rally w here th ey a re sepa rated by the

m endo sa l su tu re s. C om ple te o b lite ra tion o f

th e m e ndo sal su tu res u su a lly o cc u rs by the

e nd of th e sec on d ye ar. R are ly , o ne o r bo th

F I G . 9 .-Rad iog raph left) and d iag ram right) of adu lt sku ll in the T o w n e pro jec tion sh ow in g u nun ited

K erckr in g’s bone . (R eprin ted w ith perm iss ion from Shap iro R , Janzen A : The N orm a l Sku ll. N ew Y ork ,

H arpe r & R ow ,

1960)


5/6

,

,1

SI

FIG . I I .-P h o tog raph of base o f

22-week-o ld

fetal

sku ll (S pa lteho ltz p rep aration ) . B asispheno id (bs)

separa ted f rom bas ioccip ita l (bo ) by sph en oocc ip ita l

synchondrosis

a rrowhead) . p = p etro us b ones; e

=

cx -

occ ip i ta l bon es.

*t

‘

ta l bo ne in th e T o w ne p ro jec tion m ay be

rec og n iz e d b y its p ro jec tio n be yo nd the

oc cip ita l bo ne on to the fo ra m e n m a g nu m .

A C K N O W L E D G M E N T S

W e a re d ee p ly g ratefu l to D r. M elv in L .

M o ss , C o lu m b ia U n ive rsi ty , a nd th e la te

‘p

S

EMBRYOGENESIS OF OCCIPITAL BONE

. ,-.

. .

FIG . io .-A n te ro pos te rio r T ow ne A)

and la te ra l

B) v iew s o f new b orn fe tal sk u ll w ith th ree oss icle s

(

arrowheads) in in nom ina te synchond ros is . N o te

presence o f K erck ring ’s p rocess a rrow) . (R epr in ted

w ith p erm ission from C affey J

:

Ped ia tr ic X -Ra y

Diagnos is , 6 th ed . C h icag o , Y ear B o ok M edica l Pu b-

l i shers , 1972) .

10b7

m e nd osal su tu re s m ay re m a in o pe n in

ad u lt life . S ho u ld th is ha p pe n , th e pa te n t

su tu re, p ar ticu la rly if un ilate ral, m ay be

m ista ke n fo r a frac tu re . S in c e the su p ra -

o cc ip ita l segm en t (in fe rio r squam a) ossif ie s

from a s in g le bo ne c en te r, th ere is n o n or-

m al m id lin e su tu re o r sy nc ho nd ros is , de -

sp i te c on trary s ta te m e n ts in th e li tera tu re

[ ii, 12].

T he refo re , a lin e ar m id lin e rad io -

lucency w ith in the su prao cc ip ita l segm en t

o f the o cc ip ita l bon e m ust be c on side red to

be a frac tu re

[2 , 13] (fig . 1 3 ).

A p ers is te nt

m etop ic su tu re su pe rim po se d on th e o c cip i-

FIG . 12 .-T ow ne pro jec tion of sk u ll o f new b orn

fu ll te rm infan t. A rrow p oin ts to m id line un oss ified

m em brano us strip in in te rpa rieta l segm en t (ip ). T he

la tte r is sepa rated by m en dosal su tu re a rrowhead)

from su prao cc ip ita l segm en t (so ) . e =

pa ired exo cc ip i-

ta l segm en ts on e ithe r sid e o f fo ram en m agn um .


6/6

F IG . 3 3 .-M id line vertica l frac tu re arrow invo lv -

ing bo th in te rp arie tal an d sup raocc ip ita l segm en ts .

io68

S H A P IR O A N D R O B IN S O N

D r. B e rtra m S . K n au s, U n iv ers ity o f P itts -

bu rgh , fo r th e ge ne rou s loa n o f hu m an e m -

bryo s p repared

by th e S pa lte ho ltz tec h -

n iq ue ; to D r. E . L eo n K ie r fo r th e lo an o f

sev era l p re pa red fe ta l sk u lls; an d to D r.

J ohn O strom for m ak ing ava ilab le m am -

m ah ian sk u lls from th e P eabo dy M u seu m

co lle c tion . W e a re a lso g ra te fu l to D rs.

K esz le r, L o hm a n , M a nsou n ia n , an d W eis-

fe nu ng fo r v ario us tran s la tion s fro m G e r-

m a n an d F re nc h , to O v id io G a llo fo r the

pho tog raphs, and to M iss A n ge la B rune tti

fo r typ ing the m anu sc rip t.

R E F E R E N C E S

I. A ugie r M : Q uelq ues p rob l { 232} m es re la tifs au d {23 3}-

ve lo ppem en t du c rane . I. V ou te o cc ip ita le chez

l’ho m m e et d ’au tres m am m if { 232} res. A rch Ana t

H isto l Em /iryo l (S t rasb ) 13 :33 -66 , 1931

2 . F rank en

E A Jr: T h e m id line o cc ip ita l f issu re ;

d iagno sis o f frac tu re versu s ana tom ic varian ts.

Rad io lo gy 93 : 1043I046 1969

3

H ad ley L A :

Ana tom ico -R oen tgenog rap h ic S tud ie s

o fthe Sp in e. Spr in gfie ld , I ll., T h om as, 396 4

4 . K ie r E L : F e tal sk u ll, in Rad io log y o fthe Sku ll and

Bra in ,

vo l .

I,

book

I,

ed ited by N ew to n T H ,

P o tts D G , S ain t L o u is , M osby , 19 71 , pp 99-I 1 7

5 . L aco ste A : S ur le d { 2 33}v elop pem ent de l’ {233 }ca illeoc-

c ip ita le { 23 3} tu di { 23 3} eom para tivem en t chez le m ou -

to n e t ch ez l’ho m m e. A rch A na t H is to l Em bryo l

(S t rasb ) 1 2:1 -47 , 3 930

6 .

L eD ouble AF : Tra ite des varia tions des o s du

cran e de l’hom me . P aris , V ig o t F re res ,

I 903

7.

M atth es E : N eue re A rbe iten { 252 }be ra s P rim o r-

dialcra n iu m d er S { 22 8} ug etie re . II . T eil. A rb e iten

{2 52} be rinze lne R eg ionen des C ran iu m . Ergeb

A n at E n tw i ck lu ng sg es c/ i 24 :

I 1 7 -2 4 3 , 1 9 2 3

8. Parker W K , B ettany G I : The

M orph o logy o f th e

Sku l l . L ond on , M cM illan ,

I

87 7

9 . C affey

J

:

O n the accesso ry o ssic les o f the sup ra -

o ccip ita l b on e.

Am 7

Roen tgeno l 70

4 0 I-4 1 2 ,

95 3

30 . M elsen B : T he cran ia l base . Acta O don to l Scan d

32 , supp l. 62 , 3 974

I I . C affey J

:

P ed ia tr ic X -R ay D ia gnos is, 6 th ed .

C h icag o , Y ea r B oo k M edica l P ub lishe rs ,

1972

I 2. K oe h le r A , Z im m er E A :

Bord erlands o f th e No r -

m a l an d E ar ly P a th o log ic in Ske le ta l R oen tgeno l-

ogy ,

I I

th ed . N ew Y o rk , G rune & S tra tton ,

i

96 8

13 . A llen W E III , K ie r E L , R o th m an SL G : P itfalls

in th e eva lua tion o f sk u ll traum a: a rev iew .

Rad io lCl inNor thAm

II : 47 9-5 03 ,

3974

embryogenesis of the human occipital bone shapiro

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