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The influence of asymmetry of the muscles of mastication upon the bones of the face.

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THE I N F L U E N C E O F ASYMMETRY O F THE
bIUSCLES O F MASTICATION U P O S
THE BONES O F T H E F A C E
WILLIAM M. ROGERS
Department of Anatom!/, College of Physicians and Surgeons,
CoZumb ia University
FOURTEEN
FI GUR E S
Slight asymmetry of thc maridiblc occurs frequently but is
inconspicuous. Over 75% of thc specimens measured by
HrdliEka fell into this category. However, in a relatively
small number of cases differences between the two sides a r e
very noticeable. bIandibular asymnictry may bc due to anomalous development or to traumatic or patliologic tlestruction of bone. Such cases a r e readily distinguishable and
present no problem to the experienced ohserver. I n a n appreciable proportion of tlic skulls in any collection, however, them
may be no apparent reason for noticeable asymmetry. These
caseb usually present as their asymnietric fcaturcs the gonial
angle and the general shape and size of tlic ascending rarnus.
Ales Hrdli6ka ( '40) obsci*ved a considerablc difTcrence ( 4 to
10 degrees) between the gonial angles of the two sides in 13%
of thc. group of 3,000 niaiidihles which he rricasurccl. Although
he was unable to accouiit for tliesc variations, he thought that
a search for possil)lc>causes sliould be made.
I n a n anthropometric survey of a population of about 250
skulls from the ~~urternrriberg-Heicicnheim
locality of Gcrmany in tlic collcctioiis of the American Museum of Natural
History,] the author found scvcn skulls wliich exhibited an
'The author should like t o take this opportunity to express his gratitute f o r
the kindiiess shown to him by Dr. Harry 1,. Shapiro and the Staff of the American
Museum of Natural History, both in the use of the gre:ct collection of skeletal
iuatorial and for the invaluable personal aids mid suggestions. I also wish to tliaiik
Mr. Earl Langguth f o r his valuablc assistance.
617
T I I E A N A T O N I C A L RBCORI) VOL
4UCUST 1958
1'31, S O . 4
618
WILLIAM M. ROGERS
angular asymmetry of five degrees or more. Xeasurcments
significant in evaluating this asyiiimeti*yai'c found in table 1.
None of these skulls sliowcd any structural, developmental o r
patliological reasons for such asymmetry. However, in esaminiiig these specinleiis it hccame apparent that the mandible
-
-_
bKULL NO
4550
4617
_4264
_ _ 4266
_ _ _
_ _4614
_ _ _
Female
Male
Fetiiale
Male
Female
_
46701
Male
Feniale
-~
~~
Goiiial angle
123"
128"
130"
135"
120"
115"
127"
121"
124"
116"
130"
135"
Maximum breadth of ramus
Left
34
Right
34
37
39
37
38
39
37
38
40
40
40
35
36
Miiiimuni brendtti of ranius
Lcf t
25
Right
24
30
30
30
30
30
31
28
29
24
30
25
23
Left
Right
116"
121"
Most posterior point on lateral side of fionto-malar suture t o loivest point still on
lateral side of maxillo-mal,zr suture
Left
45
46
49
42
40
45
41
Right
44
45
45
43
40
46
40
Maxillo-malar siituie: At lowest border of orbit t o lowest point still on lateral side '
Left
31
30
31
28
24
22
30
Riglit
30
31
29
32
25
27
27
Photographed: See plate 1.
Z M e a ~ u r e m e nas
t ~ defined by Woo ('37).
is not the only skeletal component demonstrating asymmetry.
I n plate 1a r e shown photographs of two of the skulls in the
full frontal aspect. The eye is irriniediately caught by the very
obvious differences betiveen the infraorbital regions on the two
sides in each case. B y i.efercnce to the tahle it will bc vei.ificc1
t h a t the side of the reduced infraorbital area in each case is thP
same as the increased gonial angle in the mandible for that
specimen.
MUSCULATURE A N D FACIAL ASYMMETRY
619
Plate 1 shows the lateral aspects of the right arid left sides
of the mandible belonging to specirncn no. 4630. The differences between the ascending rarrii or1 the t\vo sides of the mancliblc a r e readily observed.
The immediate explanation f o r this relationship between
the unilateral differences 011 the mandible arid the zygomatic
area is not hard to postulate. The inferior border of the malar
bone is the area of origin for the masseter. The strongest
attachments of the massetcr on the rnandible a r e on the
external surfaces of the gonion. There would thus seem to be,
at least superficially, some reason for associating an asymmet r y of the masseter muscle with observed asymnietry of the
bony st ruet u re s .
In archaeological material, however, conclusions on this
matter can only be speculative, since after all the muscles
themselves must be liahle to examination before definite
conclusions may be reached.
The author was then indeed fortunate to be able to find and
perform a dissection on a cadaver which demonstrated to a
marked degrcc just the sort of asyrnrneii*y which is under
discussion.
Description of a cndauer showing nsywwaetry of the
muscles of mastication
Tlie only history available on this wliite male cadaver was
his age, 62 years. Superficial inspection revealed a marked
difference between the two sides of the face. The lines of
expression around the eyes and mouth and on the forehead
were symmetrical. Dissection of the superficial muscles of
cspression arid tlie seventh crania1 nerve demonstrated that
they were equally well cleveloped on the two sides.
A s y m m e t r y of tlic wziscles of mcrstication. Bsymmetry of
the muscles innervated hy the fifth cranial nerve was striking
(figs. 1 arid 2). Tlie right rnassetei. was approximately oncfifth tlie size of tlie well developed left masseter. Exposure of
the temporalis revealed an even greater difference. The left
temporalis was of average size, while the right muscle was
alrriost en t i d y absent.
Tlic iiiteriial and estcirrial ptclrygoitls on the riglit side had
a cross-sectional area of abont one-fourth of the cross-sectional area of the same muscles on the opposite side. The
mylohyoid and tlie anterior belly of the cligastric were sonicwliat snialler 011 tlic right sick but no estimate of the differences could 1)e rcaclied. Tlic tensor vcli palatiiii also nppearetl
to 1)c reduced in size.
Fig. 1 A drawing of the iioriiinl ( l e f t ) side of the cadaver skull. Muscle
nttaelniiciits are sliowii in red. Drawing by C. Kellner.
M U S C I.LATLTRE AXI) F A C I B L A S Y M M E T R Y
621
Asymnzetry of t h e skuZZ. The skull was edentulous and liad
been f o r years, as indicated by the resorption of alveolar bone.
I n fact, complete loss of the alveolar ridge on the side with
the well developed musculature (left) was in contrast to a
A drawing of tlie atrophic side (riglit) or tlie cadaver skull. l\luwle
Fig. 2
nttaeliiiients are iii rrd. Dr:twiiig hg C. Kelliier.
rathcr sliaiy alvcolar ridge on the atrophic side. This iiitlicates that most of the chewing was done on thc left side.
The te?nporoi7au~~(Ji0111dlT
joint. The size and shape of the
condyle on the side having reduced musculature differed
622
WILLIAM M. ROGERS
markedly from a typical coidyle, (figs.3, 10, 11, 12, 14). Its
antcroposterior arid rnedioiateral dinieiisions were greatly
reduced (table 2). Tile middle of the superior portion of the
articular surface of the condyle had a small rounded process
(fig. 3 ) . The supcrior p a r t of the gleiioicl fossa had a cor-
A
Fig. 3A A drawing of the c:idaver nxrnclible wit11 p i ticular attention foeiiwtl
the shape of the coiidylcs aiid their respective fossae. Morpl~ologir:~l
:iilnpt:itioii
t o altered fuiietioiial clemni~dsis illastrntecl.
Fig. 3B Scliema sliowiiig pivot mid hinge inoveiiieiits conipatil)le with the
111orp11olog.yof tlie :itropliic side.
011
i*clspo ndii ig tlc pr c s sioii. Thc rriciii sc us wii s srriali l)ut cornplc t 1:
and imperforate. 01ily liiiigc. and pivotal riiovertieiits a r c
compatible with tlic rno~~phology
of this ai+cnlatioii.
0
1
1 the opposite side, (figs. 9 a i d 14) the dorsoventral
dimensions of the condyle were slightly greater than usual.
Tlie aiitcrior supcrior p a l s t of its ai.ticular slll+fiIcewas flat-
MUSCITLATIIKE A N D F A C I A L A S Y M M E T E Y
623
tened and the articular ridge correspondingly flattened, inclieating excessive unbalanced sliding movements. The meniscus
mas complete and imperforate. Articular cartilage covcred
the bone but the flattened surfaces of the condyle and the
articular eminence on the squamous temporal were soniewhat
roughened - - - probably an indication that i.esorption was
occurring and was continuing to transform this joint into onc
better adapted to perform powerful protrusive and latcral
movements. The morphology of the joint somcwhat resenihled
the type present in cud chewers (Ruminantia) such as the
sheep. This condition, plus the unilateral wear on the maxillary and mandibular alveolar ridges, i n d i c a t d that most of the
mastication was accomplislied by the strong left side.
The neck of the condyle shared in the asymmetry. All of its
dimensions on the atrophic side were reduced (table 2). The
area of insertion of tlie external pterygoid on the ventromedial aspect of the neck of tlie condyle was also smaller.
Atrophy of the external pterygoid was so great that it was
unable to perform protrusive and lateral movements. The
joint merely operated as a pivot when the opposing external
pterygoid contracted.
A r e a s of muscle uttachments. The bony areas of origin and
insertion of the atrophic muscles showed approximately the
same reduction in size as did the muscles themselves. Correlated with the nearly total atrophy of the riglit temporalis,
the superior arid inferior temporal lines o n the craniuni were
almost unrecognizable arid the temporal fossa was smooth
(compare figs. 1 and 2 ) . There was a n equally striking reduction in the coroiioid process (figs. 9, 10, 11, 12, 14). The lower
border of the zygomatic arch, from which the masseter arises,
was reduced in its vertical dimensions and in thickness (table
2). This was most noticeable at its ventral end in the region
from which a major portion of the tendinous fibers arise. The
area of insertion of the masseter in the region of the gonion
also showed a marked reduction resulting in a widened angle
and a decrease in the vertical height of the ramus (table 2).
624
WILLIAM M. ROGERS
Ail accurate coniparisoii of tlic areas of iiisertiori of the
internal pterygoids 011 the medial aspect of the gonial region
below the niylohyoid groove could be made. This triangular
area 011 the atrophic side was approximately one-fourth the
size of the same area on the uoimal side (figs. 1, 2, 9, 10,
11, 1 2 ) .
TARLE 2
~
~~
,Vettic d a t a o n the mandible aii,rl zygomatic legion of t h e cadaver
__
~
>I EASURE.Zl):B'P
____-~
Left side
Right sido
120"
133"
. -
Coiiial angle
Oblique height of r:imiis
64 inn1
63 mm
Vertical height of ramus
57 inm
52 nini
M asim uiii bread tli of r aiiiiis
41 mm
39 117111
Miniinnin breadth of ranius
31 mni
21 111111
Masiniuni anteroposterior dinieiisioi~ of condyle
11mni
8 111111
Mnsinium niesiolateral dimeiisioii of condyle
24 111111
19 miii
Jia.siniiiiii depth of maiidibu1;ir iiotcli
Mandibular iiotch to tip of coronoid
Liiiguln to mental f o r a m m
Most anterior point on syiiipliysis t o projwtcd
goiiial point
Mental foramen t o posterior margin of coiidyle
g m i t e s t dimension
6 iiim
10 lnlll
22 111111
66 n1111
20 inm
68 iiim
93 mm
83 iiitii
99 nim
97
-
111111
ZTUOMIATIC R>>.:OIOS
Fronto-malar suture t o mnsillo-nralar suture
49 lillll
42 inin
M:~sillo-inalar suture nicnsurcmcnt
21 llllll
19 mm
~
_
_
~Projected goiiial point: Tlic point defiiied by the intersection of the plaiie
of the horizontal upon which the innndihle rests, t h e plane tnnge1iti:il to the
ascending rariius (iiirnsuring the goiiial angle) and the plnile of the buccal surface of the 1n:indible.
' S e e table 1 f o r drfiliition ant1 origin of mensurcment.
1)iffci.t~iiccsin t h p ptcrygoitl pi*ocesses 011 tlic two sides were
also observed. The lateral plate was reduced slightly in its
do r soven t r a 1 dim ci 1si oil s , wl i i 1e the riled i d pla t c n.a s rria i*kcdI y
atropliic aiid thc pterygoitl fossa was shallow. This was
associated with the atrophy of the pterpgoid muscles.
MUSCULATURE AND FACIAL ASYMMETRY
CiZ
Radioyrapliic f i m h g s
F o u r roentgenographic films reproduced as figures 11, 12,
13 and 14, present cxccllent visual evidence corroborating the
above mentioned measurements (table 2). In addition, the
loss of cortical and trabecular bone in the coronoid process is
demonstrated. The reduction of spongy bone in thc region of
tlie mandibular canal is clearly shown.
the goriial angle MOTV
The cortical bone that forms the rriedial wall of this rcgion is
the area of insertion of the internal pterygoid musclr. ,Is onc
would expect, the trabccular bone is greatly reduced in mass
as it is encroached upon by tlie receding cortex in regressive
structural adaptations to functional changes. However, the
trabecular pattern of tlie spongy bone still presrnt 011 the
atrophic side is similar to that found in the same region on the
normal side. The atrophic nature of the asymmetry is sho\\rn
by the complete disappcarancc of spongy bone in the coronoid
process as it becomes much thinner and its density decreases
more than it cvcr does in a normal riiandible of compai.ahle
surface area. Differences in all dimensions of the contlples are
distinct 1y s110\v 11.
DISCUSSION
F o r years comparativc morphologists have recognized tlie
correlation between the size of the muscles inscrtcd on the
mandible and the form of the mandible itself. Wasliburn, in
a recent article ( '51), divided the mandible into three areas :
A coronoid region related to the temporalis muscle, a gonial
region related to the masscter and internal pterygoicl rnuscles,
and the central area of tlic mandible, which is unrelated to
muscular stresses. Washburn's statement is in accord with
our previous and current conclnsions. I n 1947 Rogers reported seven living human cases in which unilateral muscle
atrophy produced atrophy of the bone at the areas of muscle
attachments on the mandible, the zygoma, and changes in
the form and function of the temporomandibular joint. Rogers
and Katz ('47) documented the dynamics in such asymmetry.
626
WILLIAM M. ROGERS
Rogers and Applebaum ( ’40) considered t h a t atrophy
occurred in non-alveolar bone of tlie mandible in many edentulous patients. They suggested that this change was a sequel
to reduced stvesses associated with decreased intermaxillary
distance. Robinson, Bolling, and Lischer ( ’42) corroborated
these findings.
Keen ( ’45), applying Stein’s ( ’40) mechanical interpretation of the morphology of the mandible, describes changes in
the niaiidibular angle of edentulous patients a s resulting
from the “bending” of the mandible by compression effected
by the masseter and internal pterygoid muscles. He states
that “ a corollary to any increase in the angle of the mandiblr
is an increase in its length. It is difficult for the author to
appreciate how Keen could champion such a concept, since
there is no increase in lcngtli and no change in the trabecular
pattern in such mandibles (plate 2).
The process involved is graphically illustrated by superimposing a projection of the atrophic side upon the same
projection of the normal side in such a way that landmarks
in the muscularly unaffected area on each side coincide. This
has been done, the coincident laiidrnarks being the mental
foramen anteriorly, and lingular and mandibular canal in the
posterior region. It is easily seen that the reduction ill
the mass of bone in the areas of the coronoid process and the
goriion, and of the condyle a r e responsible for the changes
in angle and shape (plate 2). N o increase in tlie length
occurs and none is expected, since the increase in the angle of
tlic rriaiidihle is due to loss of bone aiid not to any sort of
“bcn(1iiig” mechanism. This is supported by the fact that
there is no change in the pattern of the remainder of tlie
trabecular bone (plate 2).
Striking effects of loss of muscular forces on growing
human mandibles were presented by tlie author in 1947 in
cases of residual paralysis of muscles innervated by the fifth
cranial nerve. Experimental proof of similar nature has been
* Clinical and experimental proof of regressive changes i n adult skulls will be
presented in the subsequent paper by the author.
M U S C U L A T U R E AND F A C I A L A S Y M M E T R Y
627
reported by the author in 1955 and by several other investigators.
Toldt ('05) described an interesting case of a wild fox
presenting some asymmetry of the mandible and cranium.
This asymmetry was interpreted to be the result of the
decreased use of the muscles of mastication on one side due to
pain from a carious tooth.
Anthony ( '03)' and Anthony and Pielkiewicz ( '09) reported
several cases of unilateral extirpation of the temporalis in
dogs which produced some asymmetry of the mandible and
cranium.
Pratt ('43) likewise found asymmetric skulls in rats after
unilateral removal of the masseter.
Washburn ('47) presented cases of rats in which the temporalis was removed during the first few days after birth. The
coronoid process failed t o develop.
Horomitz and Shapiro ( '51) repeated Wasliburn's rat
experiments and obtained similar results.
SUMMARY AND COKCLUSIONS
1. The problem of accounting f o r unexplained mandibular
asymmetry often encountered in archaeological and other
skeletal populations is outlined.
2. A dissecting room specimen is reported with marked
asymmetry of the mandible and cranium. Appropriate measurements are reported, together with photographs, radiographs and drawings.
3. It is shown that an extremely atrophic temporalis muscle
was causally related to a small thin coronoid process, and
indistinct temporal lines on the cranium.
4. A very small masscter and internal pterygoid were
related to a reduction in the mass of bone in the region of the
gonion, and therefore to the increase observed in the goiiial
angle on the atrophic side.
5. The small masscter was also related to the atrophy of
the lower border of the zygoma.
628
WILLIAM M. ROGERS
6. The size and shape of the condyle was altered as a
result of the loss of protrusive and lateral iiiorcmcnts and a
decrease in occlusal force.
7. Tlie medial and lateral pterygoid plates and the pterygoid fossa were smaller on the right sick, corresponding to
small pterygoid niiiscles o n the atrophic side.
8. Alteration of the condyle of the mandible and of the
articular eminence of the temporal bone on the “strong” side
indiea ted excessive sliding movements.
9. Asymmetry of the mnsculaturc accounted for the asymrrictry of the mandible and of other bony areas on the skull
from which the affected muscles arose.
10. The change in the gonial angle is therefore attributed
to resorption in the gonial region, and not to the results of any
“beitding” action as has been suggested.
11. This is documented by roentgenographic evidence of
the reduction in the mass of trabccular bone without alteration of the architectural pattern of that which remains.
LTTERATTJRE CITED
ANTHOYY,R. 1903 Iiitrocluction a l’Ktude esperimcntale de la Morphogenie.
Bull. e t Mem. de la Soc. d’Anthrop. Paris. 119-145.
AKTHONY,R., AND W. B. PIETKIEWICZ
1909 Nouvelles experiences sur le role
du muscle rrotaphyte dans la constitution morphologiquc du crane de
la face. Compt. Rendu. Acad. S c . Paris, 1 4 9 : 870.
CLEaVER, I?. H. 1937 A contribution t o the Biometric Study of the human
mandible. Riomctrika, 2 9 : 80-11 2.
HELL31A4N, MILO 1927 Preliminary Study i n Development as it affects human
face. Dent. Cosmos, 6 3 : 250.
HOROWITZ,
S. L., AND H. H. SIIAPIRO1951 Modification of Mandibular Architecture folloiving rrmoval of tcmporalis muscle i n the rat. Jour.
Dent. Research, 30: 276-280.
IIoTTEI,~,,
J. A. 1917 An cxprrimerit:rl study of the effect of stress and strain
on hone d ~ v r l n n m r ~ i tAnnt.
.
Rrr., 13: 233-252.
I~RDLI~~
ALES
K I , 1940 The T,o\rer Jaw: The gonial angle. Am. J. Phys.
Anthrop., 67: 281.
1930 The Lower Jan-: F u r t h r r studies. Am. J. Phys. Anthrop., 27:
388-46 7.
1947 (T. D. Strwxrt r(1.) Pructtcal A n t l r r o p o m e f r y . Wistnr Inst.
Anat. and Biol., Philadelphia.
M U S C U L A T U R E AND FACIAL ASYMMETRY
621)
KEEN,J. A. 1945 A study of the angle of the Mandible. Yearbook of Physical
Antlirop. Wistar Inst. Anat. and Biol., Philadelphia.
MORANT,G. M. 1936 A Bionietric Study of the Human Mandible. Biometrika,
88: 84-122.
MURRAY,P. D. F. 1936 Bonrs: A Stzdy of the Development and Structure of
t h e 'Verttbrate Skeleton. Cambridge Univ. Press. London. p. 92.
PRATT,
L. W. 1943 Experimental inasseterectomy i n the laboratory rat. J.
Mamniol., 6 4 : 204.
AND €5.
LISCHER1942 P~oblems of Aging. 2nd
ROBINSON,H., L. BOLLING
Edition. Williams and Wilkins Co., Baltimore, 366-390.
ROGERS,W. M. 1947 Changes i n the skull associntcd with muscle atrophy resulting from anterior poliomyelitis and other causes. Anat. Rec., 9 7 :
364-365.
1955 Experimental changes similar t o assyinetry observed i n
bulbar polio i n the skull and mandible of monkey following trigeminal
lesions. Anat. Xec., 121 :357-358.
ROGERS,w. M., AND E. APPLEBAIJM 1940 Changes i n the mandible following
closure of the bite with particular reference t o edentulous patients.
J. Am. Dent. Ass., 88: 1573-1586.
ROGERS,w.M., AND S. L. KATZ 1947 Dynaniics of normal and pathological
temporomandibular articulations. Anat. Rec., 97 : 431.
S T E I N , 11. R.
1940 Jlccliauies of tlie Mandible. Dent. Survey, IG: 143-149.
TEBO, H. G., AND I. R. TELFORD 1950 Analysis of variations of position of
Meiitnl Foramen. Anat. Rec., 107: 61-66.
1951 Variation i n position of mental foramen. Dent. Items of
Interest, 93: 7.
TOLDT, K. 1905 Asymmetrische Ausbildung der Schlaefeninuskeln bei einem
Fuclls infolge eiilseitiger Kautaetigkeit . Zool. Anz. Biblio. Zool., 29 :
176-191.
WASIIBGRN,S. 1,. 1947 The Relation of the Temporal Muscle t o the form of
tlic skull. Anat. Rec., 99: 239-247.
3951 The New Physical Anthropology. Trans. New York Acad.
Sci., Srr. 11, 13: 298.
Woo, T. 1,. 1931 Asymmetry of the Human Skull. Biometrika, 88: 324-352.
1937 Biometric study of tlie Human Malar Eone. Biometrika., 69 :
113-123.
PLATE 1
EXPLANATION OF FIGURES
4 and 5 Two of the seven skulls i n the Heidenheim Wiirtelnmberg collection of
the American Museum of h’atural History seen i n the full frontal aspect.
The asymmetry of the infraorbital regions is obvious.
6 and 7 Photographs of the right arid left lateral aspects of the inandible of
no. 4630 (see fig. 5 above). Kotice the difference in goninl angle and minin~um
breadth of the ascending ramus on the two sides.
8 A frontal view of the cadaver skull with mandible removed. Note the
reduced height of the right zygonia - - - which is related to the origin of
the masscter. Wear on the left alveolar ridge is also shown..
9 and 1 0 Photographs of the mandible. Figure 9 presents the medial aspect of
the normal left side and figure 10 is the same view of the atrophic right side.
Surface details, especially the exostoses near the gonial angle which a r e
associated with the insertion of the internal pterygoid muscle, a r e different
on the two sides.
G30
PLATE 1
M U S C U L A T U K E AND FACIAL A S Y M M E T K Y
WILLIAhI hI. R O G E K S
63 1
PLATE 2
ESPL.4NATION OF FIGURES
1,:rtcr:il rocntgeiiogr:iiiis of tlic atrophic riglit :i11(1 iioriiinl left sides
of tlic ninlidible respectively. Tlie opposite sides arc sl~owniii a n oblique
projeetioii in e:icli filni. Tr:tbcculnr bone h a s nliiiost clisnppe:ire(l i n the right
coronoid procrss.
1 1 a~itl 12
13 An anterior-posterior roeiitgciiograiii of the skiill witli the Iiinnclible
position. Asyminrtry of the is~goiiinis sliowii.
14
iii
AII :iiiterior-posterior rociitgciiogrnin of the iiiniidiblc. A (liffcreiicc in the
Incdiolatcral dimensions of the thin riglit and normal left coroiioid processes
is s11o~r.n. Diff ereiiccs in tlic coiid-yles a r e easily visihlc. (The small rounded
cniiiience 011 the upper surfarc of the riglit condglr wns tlnningr(1 Iwfore this
film as made.)
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