The growth in situ of isolated

mandibular segments
Raymond L. Bernabei* and Lysle E. Johnston**
Mentor, Ohio, and St. Louis, MO.

M uch of the presentcontroversysurroundingthe study of mandibulargrowth

concernsthe role of condylar cartilage. It was once widely assumedthat condylar growth
is directly responsiblefor mandibular translation.. 35-37The condylar hypothesis was
basedto a considerableextent on the facile assumptionthat condylar cartilageservesas an
epiphyseal plate. In many respectsthis analogy is questionable.Unlike an epiphyseal
plate, the layer of condylar cartilage is a secondaryaddition to a pre-existing membrane
bone,32,4ohaswhat might be called a perichondrium,2~ 3*accomplishesmuch of its growth
by apposition, and has a distinctly different antigenic profiie.5 Despite these obvious
differences, pathosessuch as acromegaly,vogelgesicht, and Class III malocclusions,to
namea few, make it easyto believethat somekind of discretegrowth centeris responsible
for mandibulartranslation.
Of late, the condylar hypothesishasbeenchallengedby Moss and his co-workers.21-2s
They argue that the translatory growth of the various bonesof the craniofacial complex
occurs as a result of the volumetric expansion of a variety of so-called capsular
matrices-brain, orbital contents,functioning spaces,and the like. A basic featureof
this provocativeformulation is the claim that condylar cartilagecan grow only in response
to changes in mandibular position brought about by the enlargement of the
oropharyngeal functioning space.
Although the current version of Moss functional matrix hypothesishas achieveda
considerablemeasureof popular support,craniofacial biologists have beenable to provide
little in the way of evidencefor its more extremeelements.Functioning spacesare easyto
talk about but hard to study. As a result, workers of all persuasionsstill tend to study
mandibulargrowth from the vantagepoint of the condyle. As a generalrule, two experi-
mental questionsare most often asked:(1) Can condylar cartilagegrow in a functionally
neutral environment?(2) Can mandiblesgrow in the absenceof condyles?
Although it has been demonstratedrepeatedlythat epiphyseal, synchondrosal,and
septal cartilages will grow in the absenceof functional stimulation,s**-** 30*31S41
transplantationstudiesinvolving condylar cartilage have producedequivocal results. Ini-
tially, condylar transplantationproducedresultsthat were technically suspectand, perhaps
Based on a thesis submitted in partial fulfilhnent of the requirements for the Master of Science
Degree, Case Western Reserve University, Department of Orthodontics.
Presented before the American Association of Orthodontists in New York, 1976.
*Recipient of Harry Sicher Award, 1976.
**Chairman of the Department of Orthodontics, Saint Louis University.

24
volume 13
Number 1
Growth in situ of isolated mandibular segments 25

as a result, largely but not entirely negative.Interestinglyenough,many choseto ignore

the growth seen in some specimensand drew the conclusion that condyles have no
intrinsic growth potential and, as a result, could not be primarily responsiblefor
mandibulartranslation.13-16, 34M ore recently, however, a numberof investigatorshave
shownthat condylartransplantsdo havethe capacityto grow, albeit for a limited periodof
time.4, 8*2oUnfortunately,the significanceof this growth potentialto the intact mandible
remainsto be determined.However, if workers erred in ignoring the occasionalpositive
results seen in transplantationstudies, the conventionalinterpretationof experimental
condylectomyis, if anything, even more questionable.
For a numberof years it has beenassumedthat condylectomyprovidesa reasonably
exact test of the contribution of condylar cartilageto the growth of the mandible. As a
result, this approachhas beenfavoredby many investigators,all of whosestudies,by and
large, have generatedsimilar data: mandiblesgrow in the absenceof condyles-but to a
lesserextentthan do intact controls. Interestinglyenough,this common finding hasled to
markedly different conclusions.Some have arguedthat condylescannotbe important if
mandibleswill grow without them and, as a result, haveinferredthat condylargrowth is a
secondaryphenomenonthat merely serves to maintain the anatomic integrity of the
temporomandibular joint.12,33(It shouldbe notedthat this conclusion,if correct, doesnot
really support the functional matrix hypothesis. Although it denies an active role for
condyles,it saysnothingaboutthe oropharyngealcapsularmatrix or the significanceof its
growth.) Other workers have chosen insteadto emphasizethe significant reduction in
mandibular size and have concluded that condyles are important centers of primary
growth., 3s Given the similarity of the experiments,it is probably fair to assumethat
althoughthesedisparateconclusionsserveto delineateschoolsof thought, they fall short
of clarifying mechanismsof mandibulargrowth. More to the point, it can be arguedthat
condylar extirpation is a nonexperiment;a free-floatingmandiblecould hardly fail to be
moved downward and forward by the growth of the midface and by the tendencyof
occlusalreflexesto advancethe mandiblein orderto maintainthe usualocclusalposition.
Thus, it may be arguedthat the results seenin condylectomyexperimentswould obtain
regardlessof the mechanismnormally responsiblefor mandibulartranslation.
Recently,FullerlOdescribeda techniquethat may provide a new approachto the study
of condylar growth. All hypotheseshold that the mandible undergoesa presumably
forceful downwardand forward translation(for an estimateof the magnitudeof the force,
see Belhobek,3);however, they differ with respectto the mandibularregion primarily
affectedby the various hypotheticalgrowth centers.In the functional matrix hypothesis,
for example,the forces derivedfrom the expansionof the oral spaceate depictedas being
appliedto the inner surfaceof the mandibularbody.22By way of contrast,the condylar
hypothesisholds that a major growth force is exertedin the condylarregion. Fuller argued
that if the mandiblewere to be surgically divided in the region of the condylar neck, the
resultingfragmentswould be free to reactindependentlyto whatevergrowth forces might
actually exist. Thus, if the bodylramus segmentgrew and the condylar segmentdid not,
one would be temptedto disregardthe caveatof the previousparagraphand concludethat
this set of results conforms closely to expectationsgeneratedby the functional matrix
hypothesis.On the other hand, if the condyle were to grow (in the absenceof any pull
from the rest of the mandible)and the body/ramussegmentwere to remain stationaryor
26 Bernabei and Johnston

Growth

GROUP I GROUP II

Growth

GROUP III GROUP IV

Flg. 1. Experimental design.

perhapscollapse, this set of results would be consistentwith some kind of condylar

hypothesisand would be difficult to explain accordingto the tenets of the functional
matrix hypothesis.
With thesealternativesin mind, Fuller performedunilateralcondylotomiesin a series
of young, growing guineapigs. On the experimentalside, the lateral pterygoid muscle
was strippedfrom its insertion,the marginsof the condylotomywerecoatedwith acrylic,
and metallic implants were placed in both the condylar and bodylramussegments.The
contralateralside also was markedwith implants and servedas a sham-operated control.
As judged from a comparisonof cephalometricradiographstaken at the time of surgical
interventionand 30 dayslater, isolatedcondylescontinuedto grow norm&y; however,in
contrastto the downwardandforward vector of the control side(not to mentionthe claims
of the proponentsof the functional matrix hypothesis-for example, Moss and Ran-
kow2), the bodylramus segmentshowed only a modest forward displacementand a
marked vertical collapse. Whatever, the action of expandingspaces,the effect proved
minimal in the absenceof continuity with a growing condyle.
Although Fullers experimentswould seemto achievemany of the goals of transplan-
tation without the concomitanttechnical problems of revascularizationand rejections,
severalpotential limitations may be mentioned.The use of unilateralpreparationsraises
the questionsof interactionbetweenexperimentalandintact sides,a problemthat could be
amelioratedby the useof bilateralcondylotomies.Moreover,the limitations of condylec-
tomy experimentsneedbe kept in mind when inferencesare drawn from the behaviorof
isolatedbody/ramussegments.Specifically, it might be expectedthat someof the body/
ramustranslationwas causedby the growth of the midface.The confoundingof midfacial
 Growth in situ of isolated mandibular segments 27

Flg. 2. Cephalometric landmarks. Implants: F, Mldsagittal implant in the frontal bone; Cl, superior ramal
implant; C,, inferior ramal implant; MI, posterior mandibular body implant; Ms, anterior mandibular body
implant. Anatomic points: N, The tip of the nasal bone; S, the hiihest point of the spheno-occipital
synchondrosis; I, the highest point of the intersphenoidal synchondrosls; I, the intersectiin of the lingual
periodontal ligament of the maxillary incisors and the bony palate; 0, most posterior, superior aspect of
the occipital bone; o, most posterior, inferior aspect of the occipital bone.

growth with mandibulargrowth could be lessenedby the useof an experimentalsystemin

which the mandibleis the only bone capableof an appreciableamount of translatory
growth. Inasmuchas numerousworkers have shown that the administrationof growth
hormoneto matureanimalswill producerelativelydiscretemandibularovergrowth,l*4 the
use of matureanimalstreatedwith growth hormonewould seemappropriateto the study
of isolatedmandibularsegments.
It will be the purposeof the presentstudyto determinewhich portionsof the mandible
are acted upon by the forces responsiblefor mandibulartranslation.The mandiblesof
growth-hormone-treated maturerats will be divided into threesegments:two condylesand
a single fragmentcomposedof the body and the two rami. It is assumedthat only those
parts associatedwith an active growth center will undergotranslator-ygrowth and that
the outcomewill have somebearingon the statusof the contemporaryhypotheses.
Materials and methods
Forty mature, female, Sprague-Dawleyrats were employedin the presentinvestiga-
tion. When receivedfrom the supplier,eachanimal was approximately200 days old and
weighedabout 300 grams.All were observedfor 10 days, and only thosethat gainedno
more than 10 gramswere used.
The samplewas divided randomlyinto four groupsof ten, eachof which was assigned
a specificcombinationof treatments:Group I, condylotomyand growth hormone;Group
II, condylotomyand saline;Group III, shamsurgeryand growth hormone;andGroupIV,
shamsurgeryand saline (Fig. 1).
Surgical procedures. Two types of surgical treatment were employed; each was
appliedto twenty animals.
CONDYLOTOMY. In twenty animals(GroupsI and II), both condyleswere separated
surgicallyfrom the rest of the mandible.The condyleswereexposedbilaterally, and pairs
28 Bernabei and Johnston

425 *-* SHAM S GROWW HORMONE

..*-
.*
400 t
375

350

325

300

275

250

225

200

25 T

I,, *
-10 I 10 30 30
SURGERY

TIME days
Fig. 3. Weight gainof sample.
of metallic implants were placedin eachcondyle and ramus(Fig. 2). In order to permit
radiographicimagesof the right and left implantsto be differentiated,the implanEson one
side were made of amalgam;those on the other side were composedof a m ixture of
amalgampowder and quick-cureacrylic. An additionalimplant was placedsag&ally in
the frontal bone. The condylar necks were then sectionedwith a No. 6 round bur, the
lateralpterygoidmuscleswere strippedfrom their insertions,and, to retardreunionof the
mandibularsegments,the cut marginof the condylarsegmentwas coatedwith cranioplas-
tic acrylic.
S H A M SURGERY. In the remainingtwenty animals(GroupsIII and IV), shamoperations
were performed. The soft tissueswere incised and a full complementof implants was
placed, but the mandiblewas left intact.
Injections. All animals received one of two levels of a secondtreatment:growth
hormoneor normal saline solution.
GROWTH HORMONE. Bovine growth hormone(somatotropin,0.8 to 1.O U.S.P. units
per m illigram) was administeredto half of the condylotomizedrats (Group I) and half of
the shams(GroupIII). Injections(1 mg./lOOgm. body we&&) were begunat the time of
surgery and were repeatedon each of the next 30 days. s in body weight were
monitored(Fig. 3) to assaythe effect of the hormoneand to determinethe appropriate
individual daily dosage.
SALINE SOLUTION. The other half of the animals(GroupsII and IV) were given thirEy
daily injections of normal salinesolution.
Cephdometric methods. With a cepbalostatdevisedby Gangein 1973and modified
by FullerlOin 1974,lateral cephalogrumswere obtainedimme&atelya&r surgeryaud at
the endof tbe 30-dayexperimentalperiod. Separateexposuresweremadewith the left and
right sidesnext to the film .
Volume 73
Number 1
Growth in situ of isolated mandibular segments 29

Flg. 4. Linear measures; anatomic points.

Flg. 5. Linear measures; implants.

The cephalometricanalysisemployeda systemof Cartesiancoordinates.The palatd

plane served as the abscissaand a perpendicularerectedthrough the frontal implant
constitutedthe ordinate.The X-Y coordinatesof eachimplant, as well as the anteropos-
terior position of a numberof craniometricpoints constitutedthe data (Pigs. 4 and 5).
Data reduction. The experimentwas cast in the form of a 2 x 2 analysisof variance
with twenty replications(the right and left sidesof the ten animalsin eachgroup). Main
effects (surgery or injections) were tested wheneverinteraction proved nonsignificant
(P > 0.05). In the presenceof interaction,single-degree-of-freedom tests of simple ef-
fects were performed.
Results
Descriptivestatisticsfor the changein the X-Y coordinatesof the five implantsandthe
six anatomiclandmarks,alongwith the weight gain in eachof the four groups,is summa-
rized in Table I. Changesin the position of condylar and ramal implant changesare
depictedin Figs. 6 and 7.
30 Bernabei and Johnston

Table 1. Means (d) and standard deviations (S.D.) for the change in the X-Y coordinates of
the five implants and six anatomic points, along with weight change in each of the four
groups and five assay animals

Group I Bilateral Group II Bi- Group II! Sham + Group IV

+ growth hormone lateral i saline growth hormone Sham + saline

Measure d S.D.,j d S.D.d d S.D.,l d S.D.,,

Implants: Condylar
(3 +0.61 0.58 +0.30 0.19 +0.04 0.42 -0.20 0.47
CIY -0.46 0.46 i-O.26 0.32 -0. IO 0.51 +0.02 0.39
GX +0.44 0.54 +0.21 0.67 +0.05 0.45 -0.23 0.57
GY -0.42 0.57 +0.26 0.46 -0.02 0.42 +0.05 0.46
Implants: Mandibular Body
MIX -0.47 0.64 -0.60 0.83 +o. 18 0.63 -0.26 0.50
MIY +0.22 0.69 +0.59 0.45 -0.06 0.45 -0.15 0.32
MJ -0.53 0.62 -0.58 0.79 +0.07 0.48 -0.30 0.49
MzY +0.08 0.60 +0.44 0.43 -0.01 0.44 +0.02 0.32
Cranial and midfacial
0 -0.31 0.27 -0.16 0.12 -0.41 0.28 -0.27 0.39
0' -0.35 0.27 -0.23 0.21 -0.63 0.30 -0.38 0.44
I -0.14 0.23 -0.17 0.19 -0.19 0.23 -0. I I 0.25
S -0.36 0.25 -0.23 0.24 -0.49 0.30 -0.37 0.36
i +0.61 0.31 +0.09 0.21 +0.50 0.34 +0.36 0.44
N +0.65 0.25 +o. 15 0.28 +0.74 0.36 +0.50 0.58
F +0.03 0.11 +0.07 0.24 +0.22 0.21 +o. 17 0.30
Weight
Weight 83.55 17.86 7.40 29.58 98.35 25.71 14.70 13.59

The resultsof the variousanalysesof variancearepresentedin Table II. Supplemental

F ratios for those measureshaving significant interactionare summarizedin Table III.
Discussion
Although it is generallyassumedthat condylar growth and mandibulartranslationare
somehowcorrelated,the direction of dependence,if any, is currently quite controversial.
There is an obvious physical basis for much of the confusion:condylesare linked to the
rest of the mandible. Thus, no matter where a translatoryforce is applied, the mandible
will respondas a unit. In order to minimize the confoundingof action and reaction, rat
mandibleswere divided into severalindependentsegments,each of which is intimately
associatedwith a potential growth center-oropharyngeal spaceor condylar cartilage.
It was assumedthat the subsequent behaviorof the isolatedsegmentscould thenbe usedto
determinewhich of the two contemporaryhypothesesis the more tenable.For the purpose
of discussion, horizontal (X) and vertical (Y) implant changeswill be examinedsepa-
rately.
Anteroposteriorly,there was no significant among-treatmentinteraction, and, as a
result, only main effects needbe considered.The major differenceswere associatedwith
surgery (GroupsI and II versusGroupsIII and IV): Isolatedcondylesshoweda marked
forward translation, while the ramus/body segmentswere displaceddistally. Although
these changesseem to argue against the functional matrix hypothesis, the condylar
changesappearedin both the presenceand the absenceof growth hormoneand, therefore,
Volum4?13
Number 1
Growth in situ of isolated mandibular segments 31

Group I Group II Group Ill Group IV

rh q -6.9 d =-x6 6 = mm 6 = 0.c

Fig. 6. Translation and rotation of condylar implants (initial to 30 days).

may reflect the influenceof extraneousphenomena,such as reattachmentof the lateral

pterygoid musclesor forward rotation from scar contracture.Differencesbetweenthe
effectsof growthhormoneand salinesolutionwere significantfor condylesbut not for the
rest of the mandible.Although the differenceswere small, the most obviousconclusion
seemsto be that, in terms of anteroposteriorgrowth, condylesare a target organ for
growth hormoneand the oropharyngealspaceis not.
An analysis of the vertical changesrevealsthat there was considerabletreatment
interaction.Specifically, only isolated,hormone-treated condylesshowedan appreciable
downward displacement (see Table III hormone/saline within condylotomy and
condylotomylshamwithin hormone).This result is difficult to explain on the basisof
muscle pull, scar contracture,expandingspaces,or structural collapse. Again, it
would appearthat the condyleservesas a targetfor growth hormoneand can &w in the
absenceof any downwardpull from the mandibleas a whole. Indeed,for the rest of the
mandible,the only major effect was that of condylotomy;the body and rarhuscollapsed
upwardand backward.The only significanteffect of hormonewas to lessenthe extentof
the upwarddisplacement(seeTable III, hormone/salinewithin condylotomy).
It hasbeensuggestedthat hormone-induced mandibularovergrowthmay be causedby
an enlargementof the tongue.Although soft-tissuegrowth providesat least,a plausible
explanationfor the lessenedmandibularcollapsein hormone-treated rats, thisargum&nt,
even if valid, may be of limited significance;soft-tissuehypertrophymight have a pro-
found effect on a free-floatingbodylramussegmentand still be of little significanceto the
growth of an intact mandible. Moreover, although the presenthormone do$agewas
sufficient to produceweight gain (TablesI and II) and growth of isolated condyles,it
apparentlywas not enoughto producefrank acromegaly(Fig. 7, Group III).
The presentresults are remarkablysimilar to those of an earlier inv&tigation by
FullerlOin which condylar growth and body/ra.muscollapsewere seenfollowitig con-
dylotomy in young, growing guineapigs. Indeed,the condylarvectorsfor Group.1o# the
presentstudy are almostidentical to thosereportedby Fuller (Fig. 3, p. 35).l Fuller &JO
reporteda modestforward translationof the body/ramusfragmentsand suggested that this
32 Bernabei and Johnston Am. .I Onhod.
Jununrv 1978

Group I ~~-1.8"

(-9.84, -4.79)
m2
___ ..____ ---.-.A Tc,

(-9.31,-4.86)
ml
C13.75,-4.99)

(-1,. 40, -4.08p-p A=-3.10

Tl ( -8.63,-4.32 )

------22

\. \*

ml m2(-6.05, -4.76)
(-10.80. -4.67 )

(-6.76, -5.12)

t-9.43
-&h)
( -9.25,
1 -5.50)

G-p iv A= 4.8'

(-7.20,-6.02) (-5.19, -6.05)

ml
p

ml (-5.49,~6.04)
(-7.46,~6.17 1

Fig. 7. Translatiin and rot&ion of mandibular implants (initiai to 30 day@.

mesial displacementmight be merely a reflection of the concomitantgrowth of the mid-

face. In the present study, it was assumedthat the use of hormone-treatedmature rats
would producemandibulargrowth in the relative absenceof midfacial translatorygrowth.
Although the extent to which this goal was achievedcannot be estimated,there was, on
the average,no forward growth of bodylramus segmentsin our experiments.
Recently, it has becomefashionableto discount suqical riments on the basis of
engineeringstatics. Indeed, the obvious explanation for the upward and backward dis-
placementof the body/ramus segmentin condylotomized animals is a loss of support.
However, it should be noted that if it is assumedthat expandingspacescan overcome
ambientstresssuch as musclepull in order to translatea mandibledownwardand forward
during periods of active growth, the samespaceshould be able to maintain this advance-
ment in the absenceof any element whose growth is truly cumpensatory.
Taken as a whole, this study and that of Fuller would seemto suggestthat condyles
Volume13
Growth in situ of isolated mandibular segments 33
Number1

Table II. Analysis of variance

Variance ratios (F)

Measure Interaction Surgery Hormone

Implants: Condylar
c,x 0.074 17.124** 4.342*
G=f 8.846** See Table III
w 0.041 10.801** 3.944*
GY 7.792** See Table III
Implants: Mandibular Body
1.122 11.209** 3.572
4.537* See Table III
1.440 10.637** 2.253
2.899 6.192* 3.611
Cranium and midfacial
0 2.106 0.300 0.595
0 0.859 9.121** 7.293*"
I 2.897 0.010 0.093
S 2.118 0.493 0.389
i 6.446* See Table III
N 2.152 6.411* 17.887**
F 0.940 8.560** 0.000
Weight
Weight 0.276 2.395 125.206**

*Significant at .95 level (F,ax1,76j= 3.99).

**Significant at .99 level (F.99(,,r6j= 7.08).

Table Ill. Simple effects, supplemental contrasts required by the presence of interaction
Measure

CIY C*Y MJ i

Treatment comparisons MSQ F MSQ F MSQ F MSQ F

Hormone/salinewithin 4.761 26.159** 4.489 19.43** 1.406 5.717* 2.704 24.143**

Condylotomy
Hormone/salinewith- 0.150 0.825 0.049 0.212 0.095 0.386 0.196 1.750
in sham
Condylotomylsham 1.122 6.166* 1.541 6.669* 0.743 3.019 0.121 1.080
within hormone
Condylotomylsham 0.541 2.970 0.431 1.864 5.550 22.562** 0.729 6.509*
within saline
*Significant at 0.95 level (F.,,,,,,, = 3.99).
**Significant at 0.99 level (F.ar,,,,rsj=7.08).
df= 1.

can grow without mandiblesbut that mandiblescannotgrow normally without condyles.

Obviously, thesefindings do not prove that condylesactually serveas growth centersfor
intact mandibles but, rather, that condyles have an independentgrowth potential and
might, therefore,contributeto mandibulartranslatorygrowth. In this context, it shouldbe
noted that condyles in situ might serve not so much as a prime mover but, rather, as a
 .Am. J. Orrhod.
34 Bernabei and Johnston Januan~ 1978

tissue whose growth is rate limiting under normal circumstances. Given this interpreta-
tion, translation could be caused by a wide variety of factors, whose combined effect
would be permitted (rather than caused or compensated for) by condylar growth.

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Volume73
Number I
Growth in situ of isolated mandibular segments 3!i

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