Murray C. Meikle, FLIPS., M.S.

cambridge, England

e perennial interest that has been shown in the condyle and its
importance in mandibular growth has unquestionably been due to the presence
in the condyle of cartilage bearing a superficial resemblance to the epiphyseal
cartilage of a long bone.
Following the conclusion of Charles I2 that “mandible growth is solely con-
trolled by the growth that takes place at the top of the condyle,” the majority
of workers in the fieldln, w 58,w 61 have expressed the same sentiments to varying
degrees. The traditional concept of mandibular growth views the condyle as
a primary growth center which, under the control of intrinsic factors, not only
governs the over-all growth of the mandible but also displaces the mandible
downward and forward, thereby regulating the anteroposterior relationship of
the mandible to the maxilla.
An opposite view has been expressed by Moss~~-~~who, in a series of
publications, has revitalized and popularized a functional concept of cranial
growth originally conceived by Van der Klaauw. 63 According to this hypothesis,
the origin, growth, and maintenance of the skeleton depend almost exclusively
upon the functional matrix, that is to say, those tissues, organs, and functioning
spaces related to any given skeletal element, Applying the hypothesis to the
mandible, Moss fails to credit the condyle with any inherent growth and main-
tains that mandibular growth occurs as a secondary or adaptive response to
the functional beha.vior of the oral ca,vity and related orofacial musculature.
In other words, extrinsic factors regulate the growth of the condyle which, he
believes, contributes little to the over-all growth of the mandible.
Two questions need to be answered before any attempt can be made to resolve
this controversy. First, does the growth that takes place at the condyle make any
contribution to the over-all mass of the mandible”1 Second, what is the relative

From the Department of Anatomy, University of Cambridge.

This experimental research was supported by Grant MA-4020 from the Medical
Research Council of Canada.

50
 Bole 0f condyie in postnatal growth of manddible

Fig. 1. Outlines of the mandibles representing the condylectomy [stippled) and contra;
groups, superimposed on the molar teeth. [Original magnification, x2.5.)

importance of intrinsic and extrinsic factors in regulating condylar growth? The

purpose of this article, therefore, is to attempt to clarify some of the miseoncep-
tions concerning the nature of the mechanisms regulating the growth of condylar
cartilage and the role played by the eondyle in the postnatal growth of the
mandible.

ostnatal condylectomy

Although a number of investigators 29, w 32 have studied the effect of ex-

perimental condylectomy on the mandible of the rat, Gianelly and Moorrees23
and Das, Meyer and Sicherls performed bilateral condylectomy on 3- to 5-week-
old rats in order to determine whether or not the condyle is a primary growth
center. Despite comparable findings, however, the conclusions derived from these
two studies were quite contradictory. Gianelly and Moorrees suggested that, in
view of the small difference in length between the experimental and control
groups, condylar growth is of an adaptive nature. Das and associates, however,
considered the continued enlargement of the mandible in the experimental
group to be due to adjust&e growth, in contrast to normal developmental
growth, and did not believe that it could be taken as evidence against the leading
role of the condyle in mandibular growth.
The first criticism that can be made concerning the two studies is that the
animals upon which the experiments were performed were too old. At birth,
the mandible of the rat has acquired approximately 50 per cent of its mature
length, and by the a,ge of 3 weeks this has increased to 66 per cent. In order to
remedy this deficiency in the experimental design, Pimenidis and Gianelly’”
performed bilateral condylectomies on l-day-old rats. They also found only
relatively minor changes in length and spatial positioning of the mandibles and
concluded that the results supported the functional matrix hypothesis that
condylar growth is adaptive.
A second and far more serious criticism of eondylectomy studies such as
these is that they have been used to resolve a problem in mandibular growth for
which they cannot possibly provide an answer. Removal of the condyle and
observation of the effect on the subsequent growth of the mandible does not
prove one way or another what makes the condyle itself grow and raises the
question of what can be learned from condylectomy experiments.
Fig. 1 represents the outlines at 10 weeks of two mandibles, each representing
 Am. J. Orthod.
52 Meikle July 1973

a gro-up of twenty rats; one group had been subjected to bilateral condylectonty
at 1 week, and the other served as a control group. Since Jeffreys31 had noted
that rats reared in extremes of litter size showed a significant difference in
skull and mandibular dimensions, the size of each litter used in the experiment
was limited to eight animals. At death the mandibles were dissected free and
a standardized lateral radiograph of each was taken with a conventional
cephalostat on occlusal x-ray film. Measurements were made directly from the
radiographs with a Helios gauge to 0.10 mm., and the data were processed with
an electronic desk computer. The mandibular outlines were constructed from
the mean values of these measurements and superimposed on the outlines of the
molar teeth. The selection of the molar teeth for superimposition was based on
the fact that it was the region least a,ffected by the experimentation.
Brash8 termed such experiments mutilation procedures and further cautioned
that ‘(,, . . on account of the introduction of special factors by the injury or
mutilation which is their basis . . . they can be held to prove only that under the
particular circumstances of the experiment the growth of the jaws may be
influenced in a particular wa.y.” Nevertheless, although the influence of the
surgical procedure cannot be disregarded completely, particularly the effect on
the ant’eroposterior relationship of the mandible to the maxilla, if one wishes to
evaluate the contribution of th.e condyle to mandibular growth, the amount of
information that can be gained from morphologic st,udies alone is limited. HOW-
ever, the only conclusion that can be made concerning the relevance of con-
dylectolmy experiments to an understanding of mandibular growth is that, within
the limitations imposed by the age of the animal at operation, such experiments
can give, at most, a very rough indication of the quantitative contribution of
the condyle to the postnatal growth of the mandible. It would appear from Fig.
1 that, although the condyle does not govern the growth of the entire mandible,
it is nevertheless essential for normal mandibular growth, in particular for the
enlargernent of the ramus.

Condylar transplantation

Much information regarding the relative importance of intrinsic and extrinsic

factors in determining the form of the skeleton has been provided by the in vitro
cultivation of skeletal rudiments. Murray’s”O, 52 classic experiments on chorioal-
lantoic grafts of fragments of chick limb buds demonstrated that the primordia
of long bones, which isolated in vitro, acquire a fairly normal shape. Prolonged
cultivation of skeletal rudiments, however, leads to the eventual loss of the nor-
mal anatomic features that were previously evident. Such experimental evidence
is interpreted as indicating that, while the general shape of the c,artilaginous
skeleton develops as a result of intrinsic factors, extrinsic factors-in particular,
functional activity--are responsible for the preservation of skeletal form.20
In order to study skeletal morphogenesis at a more advanced stage of develop-
ment, because of the limitations of the in vitro technique as regards nutrition
and volume of tissue, transplantation in vivo to a vascular site in a host animal
is necessary. It has been demonstrated ~1 =, 3gp64 that embryonic and postem-
bryonic long bones transplanted in vivo into a nonfunctional environment will
 Eole of condyle in postnatal growth of mandible

Fig. 2. Photomicrograph of a third metacarpal, 4 weeks after transpiantation into the

brain of a littermate rat at 1 week of age. The boxed area corresponds to the auto-
radiograph shown in Fig. 3. (Hematoxylin and eosin stain, Original magnification, x120.)

achieve growth levels comparable to that of the bone in situ. It is generally

accepted that the longitudinal growth exhibited by such transplants is due to
the continued proliferation of cartilage cells within the epiphyseal cartilage, the
fundamental control mechanism being intrinsic to the cartilage itself. Fig. 3
shows an autoradiograph from a third metacarpal bone of a rat 4 weeks after
transplantation into the brain of a littermate. The presence of many labeled cells
within the epiphyseal cartilage indicates that cell division was very active at
the time of death.
The ma.ndibular condyle has also been transplanted in vivo, in order to
determine the role of intrinsic and extrinsic factors in the regulation of the,
growth of condylar cartilage. Koski and associates3S-37transplanted components
of the mandibular ramus into 3- to 5-day-old littermate rats. The transplants
were recovered after 30 to 90 days and, although some growth did occur, the
amount did not approach that of the condyle in situ. They concluded that
condylar cartilage lacks an independent growth potential similar to that of
epiphyseal cartilage and suggested that the results supported the functional
matrix concept of eondylar growth.
However, since it is the cells of the proliferative zone alone that are respon-
 Am. J. Orthod.
54 Meifde J&1/ 1973

Fig. 3. Autoradiograph of a section through the epiphyseal cartilage of a third meta-

carpal, 4 weeks after transplantation into the brain of a littermate rat at 1 week of age.
H3-thymidine was administered to the host 1 and 2 hours prior to sacrifice. The presence
of many labeled cells in the proliferative zone indicates that cell division within the
cartilage was relatively unaffected by transplantation, as indeed was differentiation.
(Hematoxylin stain. Original magnification, x800.)
Fig. 4. Photomicrograph of a coronal section through the condyle 7 days after intra-
cerebral transplantation of the mandibular joint into a littermate at 1 week of age. The
section illustrates the spread of osteogenesis from the direction of the proliferative zone
(PZ). The arrows indicate chondroclasts (Cl) eroding the cartilage. CC, Condylar cartilage;
AZ, articular zone. (Hematoxylin and eosin stain. Original magnification, x200.)

sible for the growth of condylar cartilage,6j ‘* it is necessary to establish

whether the cells of the proliferative zone in a transplanted condyle still retain
the capacity to differentiate into chondroblasts and lay down new cartilage
matrix. A satisfactory method of achieving this is to use .tritiated thymidine
as a cellular label and to follow the distribution of the labeled cells during the
transplantation period. In the young rat the proliferative zone, being composed
of a rapidly dividing cell population, readily takes up the label.
 Role of condyle in postnatal growth of w~andible

Duterloo17 transplanted the mandibular eondyle autologously into the intra-

cerebral site in 4-day-old rats and utilized I-13-thymidine as a cellular label in
five of the experimental animals. They were injected with HS-thymidine 4, 5,
and 6 days postoperatively and killed 2 and 24 hours later. He interpreted the
presence of labeled cells in both the proliferative zone and the cartilage as
esta.blishing without doubt that proliferation and differentiation into chondro-
blasts was occurring in the transplants and concluded that intrinsic factors were
responsible for the increase in length which occurred in the transplants. How-
ever, it is doubtful that differentiation into chondroblasts was occurring and at
a more rapid rate than in the controls, as was claimed. It is more likely that the
labeled cells located in the cartilage were, in fact, osteoprogenitor cells and
osteoblasts occupying lacunae of degenerated chondrocytes.
H3-thymidine has also been used to determine the behavior of the prolifera-
tive zone of the condyle in a nonfunctional environment.@ The complete man-
dibular joint was transplanted as an isograft between 7-day-old littermate rats
and recovered over periods of from 1 to 21 days. The transplants were of two
types, depending upon whether they were labeled with H3-thymidine before or
after transplantation. Within 24 hours the cells of the proliferative zone ceased
to divide and differentiate into chondroblasts. After 3 to 4 days the transplants
became vascularized, and proliferative activity was restored. However, the
autoradiographic evidence favored the view that, following the restoration of
cell division, the cells of the proliferative zone differentiated into osteoblasts and
not chondroblasts as in situ (Figs. 4 and 5). Evidence that cellular proliferation
is relatively independent of the functional environment was provided by the
presence of many labeled cells in the proliferative zone of 3-week transplants
following the administration of H3-thymidine to host animals containing un-
labeled transplants (Fig. 6).

Discussion

It is clear that the role of the condyle was highly exaggerated in the classic
concept of mandibular growth and, in retrospect, it is surprising that anybody
believed it. However, early ideas of mandibular growth were largely based upon
decalcified histologic material. Indeed, CharleP derived his conclusions from a
study of the mandible of the human fetus, a.t which stage the wedge of condylar
cartilage is at its most dominant. Such material gives little indication of the
intensity of the growth and remodeling changes that occur in the other parts
of the mandible and are highlighted by vital staining techniques.40, 62 It is
perhaps interesting to note that, as long ago as 1934, Brash9 considered the
condyle to be relatively unimportant, following a study of the growth of the
pig mandible in which madder was used as a vital stain.
If the evidence against the leading role of the condyle in mandibular growth
would seem to be overwhelming, the evidence supporting the dominant role of
extrinsic factors in determining condylar growth is less convincing. The fact
that, following condylectomy, there is relatively little impairment in the
relationship of the mandible to the maxilla can in no way be accepted as proof
that condylar growth occurs as an adaptive response to the functional behavior
 Am. J. Orthod.
56 Meikle July 1973

Fig. 5. Autoradiograph from the 7-day mandibular joint transplant shown in Fig. 4. The
transplant was labeled with HB-thymidine prior to transplantation. The section illustrates
one labeled cell (PZC) within the proliferative zone and two labeled osteoblasts (OB) and
an osteocyte (OC) in the adjacent region of osteogenesis. Prior to transplantation, the
labeled cells are confined to the proliferative zone. (Hematoxylin stain. Original magnifica-
tion, x500.)
Fig. 6. Autoradiograph from a mandibular joint transplant 3 weeks after introcerebral
transplantation into a littermate rat at 1 week of age. The host received two intra-
peritoneal injections of H3-thymidine prior to sacrifice. The presence of labeled cells within
the proliferative zone (PZ) and adjacent region of osteogenesis (0), indicated by arrows,
shows that cell division within the mandibular condyle is relatively independent of the
functional environment. (Hematoxylin stain. Original magnification, x500.)

of the oral cavity and orofacial musculature, as frequently claimed.23s 34*4g,54

Nor does the case report by KazanjianZ3 of a woman in whom congenital absence
of the rami had little effect on the growth of the rest of the mandible support the
same general thesis. Such information does add further support for the rela-
tively minor part played by the condyle, but, having established that the condyle
does not control over-all mandibular growth, it does not necessarily follow that
it is beneficial to be without it, as the protagonists of the functional matrix
 BZole of condyle in postnatal growth of mandible

seem eager to prove. Looking at the preoperative photographs of the young lady
in question, one could not help feeling that she was considerably disadvantaged,
functionally and esthetically, by the absence of both mandibular rami, a senti-
ment that she apparently shared.
In the past considerable time and energy have been devoted to comparing
the eondylar and epiphyseal cartilages, a situation which has in some ways
tended to make an understanding of condylar cartilage and its role in mandibular
growth more confused. The question as to whether eondylar cartilage is a growth
center or a growth site is a case in point. In 1961 Baume” proposed the use of
the term growth cen,ter to describe “places of endochondral ossification with a
tissue separating force” and growth site for “regions of periosteal or sutural bone
formation and modeling resorption adaptive to environmental influences.”
Moski34 has argued at some length tha,t most of the so-called growth centers in
the craniofacial complex, including condylar cartilage, would not, by definition,
qualify as growth centers but should be regarded as growth sites. But does
such a label serve any meaningful purpose? These terms have been considered
almost exclusively in relation to areas of chondrogenesis and thereby tend to
create the impression that the role of the periosteum in bone growth is a
subordinate one, a point to bear in mind when considering the growth of the
mandible as a whole. The condyle or, more specifically, the eondylar cartilage is
no more or no less a growth site than any other part of the mandible, the only
difference being that in part of the periosteum covering the head of the condyle
ohondrogenesis takes place.
Similarly, DurkinlG in an article designed “. . . to point out the true nature
and character . . .” of condylar cartilage, has suggested that a more appropriate
term for this cartilage would be embryonic cartilage. Durkin16 and Silvermann
and FrommeP maintain that condylar cartilage has the morphologic and
metabolic characteristics of a.n embryonic type of tissue when it is compared to
the more highly differentiated and organized structure of epiphyseal cartilage
and, therefore, eondylar cartilage should be regarded as an embryonic tissue.
There is no question that these two cartilages are different in almost every
respect. But what are the metabolic characteristics typical of an embryonic
cartilage? By what criteria do we establish that one tissue is more embryonic
than another? Does a relatively simple structural organization necessarily imply
that a tissue is embryonic ? One might even argue, in view of the fact that
epiphyseal cartilage is a remnant of the primary cartilaginous skeleton and thus
predates the appearance of condylar cartilage, that of the two it is the more
embryonic. Furthermore, can this be interpreted as proof that embryonic
cartilages are remodeling centers the growth response of which is adaptive in
character as Durkin concluded ? That condylar cartilage can be remodeled has
been demonstrated by many investigatorsl, 13,41 However, it is important to
understand that a detailed histologic description of condylar cartilage, no matter
how exhaustive, is not synonymous with an explanation of the growth processes
of the cartilage. As Kremenak3* pointed out at the International Craniofacial
Conference at Nijemgen, it is easy to fall into the trap that equates naming with
explanation.
Although the mandible is a membrane bone, its development is complicated
 Am. J. Orthod.
58 Meikle JUZZJ 1973

by the formation of three secondary cartilages, of which the condylar cartilage is

one. In the rat, the condylar blastema appears at 17 days postconception in the
mandibular blastema,5 and Duterloo and Jansen18 observed that at 18 days post-
conception, the perichondrium. covering the condylar blastema was continuous
with the periosteum covering the bony sheath of the mandible. Since the
chondroblasts of eondylar cartilage do not divide,6 the only potential source of
cells a.ble to maintain growth of the mandible in this area is the cellular layer
of the covering perichondrium. Furthermore, transplantation experiments sug-
gest that the cells of the proliferative zone of the condyle are multipotential
and can form either bone or cartilage, depending upon the environmental
circumstances.42
There is, therefore, strong evidence that the articular and proliferative zones
of the condyle are derived from periosteum. The change from the normal
osteogenic function to one of chondrogenesis is the result of the development of
an articular condylar process in the mammalian mandible and, as a consequence,
the altered functional requirements of the periosteum covering the articular
joint surface.
There are many examples of connective tissues adapting to changing mechan-
ical and other environmental circumstances. The formation of secondary
cartilages7 or adventitious cartilage51 in membrane bones has been described at
the cranial and facial sutures of mammals45’ 55 and on avian membrane bones.26y51
It has been shown that the cellular periosteum of long bones of the chick cultured
in vitrOls, 25 and of the rat transplanted in vivoZ1 can produce cartilage, and
HamZ8 described periosteal chondrogenesis in his experiments on fracture repair.
However, of all the above studies, perhaps the one most relevant to the man-
dibular condyle is that of Murray,“’ who described the development of adven-
titious cartilage in a number of articulations in the skull of the embryonic chick.
The cartilage always developed. in membrane bones and only at articulations that
were mobile or where the anatomy of the musculature at relevant developmental
stages could be expected to set up conditions of strain. Furthermore, in grafted
and paralyzed embryoP the cartilage did not form and germinal cells which
normally would have formed cartilage produced bone instead.
Ha11,27 in a review of cellular differentiation in skeletal tissues, points out
that the common initiating factors in evoking either osteogenesis or chondro-
genesis are the degree of vascularity of the tissues and the presence or absence
of mechanical stress. It has been shown in vitro that hypoxia enhances osteo-
genesis and anoxia enhances chondrogenesis,2, 3, 24 and Hall suggests that
mechanical stresses may act by producing ischemia, thereby inducing osteogenic
cells to chondrogenesis. This could explain chondrogenesis at the mandibular
condyle in situ and also explain how the absence of mechanical stresses, in
combination with the rich vascularity of mandibular condyle transplants, would
favor osteogenesis.
One of the problems in evaluating the conclusions of previous investigators
in the field of condylar transplantation is the failure to make it absolutely clear
whether they are talking about the condyle in general or condylar cartilage in
particular. This is particularly important when one is analyzing the role of
 Role of cor&~le in postnatal growth of mn~~Zbie

intrinsic and extrinsic factors in condylar growth. Although there is evidence

to indicate that the activity of the proliferative zone can be altered by external
mechanical stresses,‘, 22a4-1it is clear that cell division within the proliferative
zone can operate independently of such extrinsic factors.42, 43 Despite the
probability, therefore, that cell division within the proliferative zone is linked
to some intrinsic program, one may nevertheless regard the continued main-
tenance of condylar cartilage, at least postnatally, as being due to the extrinsic
mechanical factors resulting from the functional activity of the mandibular
joint. In other words, eondylar growth itself is not dependent upon extrinsic
factors, but the existence of condylar cartilage is.
For convenience, the terms intrinsic and extrinsic have been used throughout
this article in the broadest possible sense as being synonymous with genotype
and environment. Although this is beneficial from a conceptual point of view,
when it comes to considering cellular behavior, it oversimplifies a highly com-
plicated and incompletely understood biologic process. Cellular activity results
from the continued interplay between the cell and its environment, of which
functional or mec.hanical factors comprise only one part. Trying to attribute
the growth of the condyle or condylar cartilage to either intrinsic or extrinsic
factors as if they were mutually exclusive, which has been the objective of many
investigators in the field of craniofacial growth, is rather naive. Even if it is
accepted that extrinsic factors are necessary for the differentiation of proliferative
zone cells into chondroblasts, the eventual phenotypic expression of such a stim-
ulus is ultimately controlled by the cellular genome, that is, by intrinsic factors.

Summary

1. Transplantation experiments indicate that cell division within the condyle,

including the proliferative zone, can occur independently of the functional
environment, suggesting that it is linked to some intrinsic program of a genetic
nature.
2. The cells of the proliferative zone are multipotential and can form either
cartilage or bone, depending upon the environmental circumstances.
3. Extrinsic mechanical factors resulting from the functional activity of
the mandibular joint provide t.he stimulus for the differentiation of proliferative
zone cells into chondroblasts.
4. Growth of the condyle is not dependent upon extrinsic mechanical or
functional fa,ctors, unlike the existence and maintenance of condylar cartilage.
5. There is strong evidence for regarding the articular and proliferative zones
of the condyle as being of periosteal origin, and condylar cartilage the product
of periosteal chondrogenesis.
6. The change from the normal osteogenic function of periosteum to one of
chondrogenesis can be explained on the basis of thi? development of an articular
condylar process in the mammalian mandible, and, consequently, the altered
functional requirements of the periosteum covering the articular joint surface.
7. The condyle does not control the gromth of the entire mandible. Never-
theless, it is essential for normal mandibular growth, particularly the enlarge-
ment of the ramus.
 60 Me&e Am. J. Orthod.
July 1973

The author wishes to express his gratitude to Mrs. Barbara Tait, Department of Ortho-
dontics, University (of British Columbia, who prepared the histologic material, and to Drs.
B. C. Moffett and C. W. M. Pratt for their comments on the manuscript.

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