British Journal of Oral Surgery (1982) 20, 217-224 0007- t 17X/82/00310217502.

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9 1982. The Association of Oral Surgeons

DEVELOPMENT OF THE HUMAN TEMPOROMANDIBULAR JOINT

DAVIDA. KEITH, B.D.S., F.D.S., R.C.S.

Departments of Oral and Maxillo-facial Surgery, Harvard School of Dental Medicine,
Massachusetts General Hospital: Department of Orthopaedic Surgery, Children's
Hospital Medical Center, Boston, Massachusetts U.S.A.

Summary. Tile TMJ develops later than most other human joints. Unlike other joints which develop from
a single blastema, the TMJ forms from two blastemata which grow toward one another. Most joints are
covered by hyaline cartilage while the articulating surfaces of the TMJ are covered by fibrous tissue
consisting of both elastic and collagen fibres. Finally, the process of bone formation in the condyle is
different from that seen in growth plates.

Introduction
The temporomandibular joint (TMJ) occupies an unusual place in human evolution,
development and function. In evolutionary terms it is a new joint which has replaced
the joint between the malleus and incus (Symons, 1952). It is one of the last joints in
the body to develop (Moffett, 1966; O'Rahilly & Gardner, 1978), and unlike most
other synovial joints, which develop within a single blastema,it develops from w i l l y
separated intra-membranous elements which grow towards one another (Baume,
1962; Baume & Holz, 1970). The articulating surfaces of the TMJ are composed of
fibrous tissue in contrast to the hyaline cartilage which covers most other joint
surfaces (Miles & Dawson, 1962). Furthermore, in function the joints act as one unit,
depending on the precise co-ordination between the fixed cranial articulation at
either end of the mandible and the occlusion of the teeth. Dysfunctions (Helkimo,
1979) and diseases (Guralnick et al., 1978) of the TMJ are relatively common clinical
disorders, few of which are thoroughly understood. The purpose of this paper is to
bring together information about the development of the human TMJ as a basis for
understanding some of these disorders.

Mammalian Joint Development

The features of embryonic development of most human joints (for example,
shoulder, elbow, hip and knee) are similar (O'Rahi!ly & Gardner, 1978). By about
the fifth week of intrauterine life, the skeletal elements are outlined by a condensa-
tion of mesenchymal cells which differentiate into chondroblasts and form the
cartilaginous precursor. The future joint cavity is visible by the seventh week of
intrauterine life as a homogenous interzone of cells. Ossification starts in the central
region of each bone and spreads towards the periphery, The cartilage remaining at
the ends of the bones becomes the articular cartilage. During the eighth week the
cells in the interzonedegenerate and the definitive joint cavity is created. It should be
noted that the main events in joint formation occur within a short period, are
complete by the end of the embryonic period, and depend on the formation of one
single blastema.
(Received 15 January 198t; accepted 1 July 1981)
Reprint requests to: D. A. Keith, Dept. of Oral and Maxillofacial Surgery., Massachusetts General
Hospital, Fruit Street, Boston, MA,, 02114.
217
 218 BRITISH JOURNAL OF O R A L S U R G E R Y

Temporomandibular Joint Development

Development of tile TMJ differs markedly from this pattern in that its formation is
spread over a longer period of time, it is completed relatively late in foetal llfe, and it
depends on the formation and subsequent growth of two separate blastemata
(Symons, 1952; Moffett. 1966; Baume, 1962; Baume & Holz, 1970; Moffett, 1957;
Youdelis, 1966; Furstman, 1963). Meckel's carlilage is the skeletal element of the
first branchial arch that provides the template but not the substar, ce for mandibular
development. It is present throughout the period of TMJ development until mid-
foetal life at which time itsdorsal end has become incorporated into the middle ear as
the malleus. The first indication of mandibular ossification occurs at about the sixth
week of intrautcrine life on the lateral aspect of Meckel's cartilage in the region of the
division of the inferior alveolar ncrve into its mental and incisive branches. Ossifica-
tion spreads dorsally and ventrally to form the body and ascending ramus of the
mandible up to the lingula area.
During the eighth week the first indication ef TMJ developtncnt occurs as a
condensation of mesenchymal cells, derived from the neural crest, on the dorsal end
of the mandible (Fig. 1). During the next two weeks these cells proliferate and
differentiate into the condylar cartilage (Fig. 2). This is a ,,,,,edge shaped structure
attached to the mandible, and is separated from the temporal component of the joint.

FtG. 1. (left). Developing condyle (36 tam'crown rump- approximately 8 weeks i.u.). Posterior-superior
end of mandible surrounded by a condensation of cells which will differentiate and form condylar
cartilage. Cochineal and orange c x 375.
Fro. 2 (right). Developing condyle (45 mm c.r.- approximately 11 weeks i.u.). The condylar cartilage
(CC) develops independently of the temporal component of the joint. Superior to it is seen the initial
condensation of cells which will form the disc (D). Cochineal and orange cx375.
 DEVELOPMENT OF T H E H U M A N TEMPOROMANDIBULAR JOINT 219
During the tenth to twelfth weeks the condylar cartilage undergoes tremendous
growth in size and in a posterior and lateral direction to keep pace with the widening
cranial base.
The temporal component of the joint forms in the eighth week as a separate'
condensation of cells posterior and lateral to the developing condyle. Between these
two blastemata a third condensation of cells occurs which is associated with the
lateral pter./goid muscle and which subsequently becomes the disc (Fig. 2). There is
controversy as to the precise origin of these cells. Some authorities feel that they arise
from the tendon of the lateral pterygoid while others feel that they arise partly from
the co~dylar and partly from the temporal blastema, or indeed as a separate mesen-
chymal condensation.
Growth of ithe condylar blastema causes these two structures to meet about the
twelfth week (Fig. 3). Cavitation then occurs by a process of cell death and break-
down to form upper and lower joint spaces so that the basic morphology of the joint ~s
established by t 4 weeks. In vitro experiments have shown that the joint cavity will
foril~ in the absence of nerves, bones and muscle movement but that subsequent
development is erratic, suggesting that movement is not necessary for joint forma-
tion, but that it is necessary for the maintenance of joint function (Fell & Canti,
1934).

9 ", 9 9 .... ~': "" 9 ' ' 'IP'.aN~. ,. . ' .

FIt~. 3 (left). Developing temporomandibular joint (78 mm c.r.- approximately 14 weeks i.u.). The
condylar cartilage (CC) and temporal component(T) are separated by a condensation of cells which will
form the disc (D)' Cavitation has not yet occurred. Aluminiurn haematoxylin • 150.
FIG, 4 (right), Neonatal ternporomandibutar joint (bovine specimen). The condyle is capped by surface
layer which covers a thick well vascularised cartilaginous zone. The hypertrophic zone (HZ) is prominent
H and E x60.
 220 LaEITISH J O U R N A L OF ORAL S U R G E R Y

Other struc',ures develop cor, comitantly with the joint. The capsule, for example,
forms laterally and medially to the joint and is recognisable by the eleventh week.
The muscles of mastication are derivatives of the first arch and differentiate as
separate entities. As the ramus and condyle regions change in shape and size, the
muscles are continually reattaching. Reflex muscle movement develops first in the
perioral region as the trigeminal nerve is the first cranial nerve to become active.
Earliest movements have been elicited by cutaneous stimulation of the lips at nine
and a half weeks and mouth opening at ten and a half weeks; all before the definitive
TMJ forms. Swullowin__ghh.asbeen recorded possibly as early as six weeks but certainly
by 14.~ weeks which is about the time that cavitation of the joint occurs (Sperber,
1976). Apparently the synovial apparatus is the last structure to form (Toiler, 196 !).

Prenatal growth
Once the joint has formed, significant growth and morphological changes occur.
The condyle consists of a carrot-shaped cartilaginous cap on top of the mandible
which comprises four distinct layers, all of which are well vascularised:
(1) An articular layer of fiat undifferentiated cells;
(2) An intermediate zone of proliferating cells;
(3) A hypertropic zone in which the cartilage cells enlarge and are haphazardly
arranged with little matrix between them. A zone of pericellular mineralisation is
present in the deeper layers;
(4) An erosive zone in which the mineralised cartilage is removed by chondro-
clasts and below which bone formation occurs by a type of intramembranous process
without the existence of a primary spongiosa.
During the latter part of foetal life this bone front moves in a superior direction
gradually reducing the size of the carrot-shaped cartilage. The process of bone
formation in the condyle is distinctly different from the classical endochondral
sequence seen in a growth plate cartilage in which the i~ypertrophic cartilage cells line
up in parallel rows and mineralisation occurs within the ~.ube of matrix surrounding
the cells. Erosion occurs by vascular activity and a primary bony spongiosa is evident.
In contrast, the process of bone formation in the condyle is similar to that seen in
embryonic bone. The characteristics of this hypertrophic or immature cartilage have
been described in detail in the rat by Durkin et al. (1974) and similar features are
seen in the human.
Information on this stage of human embryonic development is meagre but it is
clear thatthere is a tremendous amount of growth of the condylar cartilage in a
superior, lateral and posterior direction keeping pace with the growth of the
neurocranium.

Postnatal growth
At texm the TMJis characterised by vascularisation of all component s and active
bone formation in the condyle and glenoid fossa regions (Fig. 4). Growth and
maturation changes occur postnatally in all parts of the joint, and arenot finally
completed until the end of the second decade of life (Ingeratl et al., 1976; Wright &
Moffett, 1974).
Tile condyle is covered by a thick layer of cartilage - the remains of the carrot-
shaped condylar cartilage- in which the hypertrophic zone is very prominent. Loose
mesenchymal columns or 'crampons' consisting of vascular connective tissue are
seen extending into tfle bony condyle (Fig. 4) During tile first six months of life there
 D E V E L O P M E N T OF T H E H U M A N T E M P O R O M A N D I B U L A R J O I N T 221
is a reduction of cartilage thickness mainly at the expense of the hypertrophic zone.
Associated with this is a reduction in the vascularity of the area.
By seven years of age (that is, at the start of the mixed dentition) the cartilage is a
thin layer. Growth continues into the permanent dentition as shown by a diminished
hypertrophic zone with fewer cells, more matrix and reduced mineratised cartilage
(Fig. 5). In late teenage the sub-articular plate of bone forms, separating the cartilage
from the cancellous spaces (Fig. 6). Thus, in its mature state the condyle is covered by
a surface articular layer consisting of collagen fibres mainly running in an anterior-
posterior direction and interspersed with some elastic fibres. The intermediate layer
of cells remains into adult life together with a diminutive layer of cartilage with few
cells some of which may look chondroblastic. This layer is a constant feature of adult
specimens and retains the capacity to respond to physical stress. Under appropriate
circumstances the ceils in this area will either produce a cartilaginous matrix which
advances the surface layer (progressive remodelling) or alternatively osteoclasts will
resorb the subarticular bone thus moving the surface layer away from the stimulus
(regressive remodelling) (Johnson, ]962).
Postnatal changes also occur in the temporal region. At birth the temporal fossa is
flat (Fig. 7) and there is little evidence of an articular eminence, but during the first
three years the eminence develops to resemble the mature S-gbape which is finally
obtained at about six to seven years of age, in other words, at the sta~'t of the mixed
dentition (Fig. 8).
It is interesting to note that bone formation in the articular eminence occurs by an
unusual process. Chondroid bone is formed in which a predominantly collagenous

FXG.5 (left). Section of articular surface of TMJ from teenager Irhe hypertrophic zone (HZ) is thinner and
less cellular. H and E •
FiG. 6 (right). Section of articular surface of adult TM]I The subarticular, plate of bone has formed and the
articularlayer consists mainly of a. fibrous layer: Verhoeff's stain, x.l.50.
222 BRITISH J O U R N A L OF ORAL S U R G E R Y

FIG. 7. Fetal skull. The temporomandibul-~r joint is flat with a poorly defined articular eminence.

Fie;. 8:iSkull at:at~out:3 years of age. The articular eminence has developed.
 D E V E L O P M E N T OF T H E H U M A N T E M P O R O M A N D I B U L A R JOINT 223
extracellular matrix is laid down which has the basophilic characteristic of bone but
which contains nests of cells in lacunae resembling chondrocytes (Wright & Moffett,
1974). This type of change of cellular activity is true metaplasia and is seen in certain
other situations (Hall, 1978).
The articular surface of the fossa and eminence become more fibrous and less
vascular with age. Similar cellular layers are seen as in the condyle, and the prolifera-
tive zone is present until late teenage. Collagen and elastic fibres form the surface
layer which is thickest on the posterior-inferior aspect of the eminence.
During postnatal life the disc changes in shape concomitant with growth of the
articular eminence. It also becomes more compact with a decrease in the number of
cells and an increase in the amount of collagen. The mature disc is avascular and
aneural in its central part and consists of a basket weave of collagen fibres inter-
twined with some elastic fibres. It is worth noting that a band of connective tissue
attaches the posterior rim of the disc to the squamo-tympanic suture region and that
this is composed of vessels, nerves and a thick band of elastic fibres. This is the
mechanism by which the disc is retracted on closing the mouth as there are no
muscles which specifically move the disc backwards.
The developmental processes which have been outlined are a complex series of
events which are spatially and temporally integrated. From the migration of neural
crest cells into the area to the development of mature structures the process depends
o:.~ the precise behaviour of cells in terms of their interaction, proliferation and
synthetic functions. Given the complexity of the process and its span over a relatively
long period ot time, it is remarkable how few anomalies of TMJ developmenf are
seen in clinical practice. Ross (1979) has recently provided a classification of
developmental TMJ anomalies which includes the following conditions:
Developmental Hypoplasia is a group of anomalies in which the condyle and
mandible are small but relatively normal in form and function. It is thought that there
is a deficiency of undifferentiated mesenchyme at an early stage of development.
This deficiency riaay arise because of lack of migration of neural crest cells into the
area, beca use of a lack of proliferation of these cells or possibly their destruction. The
deficiency is bilateral and usually symmetrical. One example is the Treacher-Collins
syndrome.
Developmental Hyperplasia may be generalised or localised. In facial hemi-
hypertrophy, all structures including the teeth are enlarged due to an excess of
mesenchyme. More common is unilateral condylar hyperplasia in which the growth
site persists beyond adolescence.
In Developmental Dysplasia there is a malformation or agenesis of parts of the
TM.I which may or may not be accompanied by micrognathia. This condition is seen
in the lateral facial defects which include certain types of hemifacial microsomia and
the first and second Branchial Arch syndromes.
The dysplasia is localised without regard for embryonic differentiation suggesting
that the injury occurred late in development.~Several mechanisms have been sug-
gested including, localised cell destruction, interference with cell movement or
differentiation, displacement of cel!s or biochemical failure. Poswillo (t973) has
suggested that haematoma due to failure of the transient stapedial artery system is
the aetiology of firstand second Arch syndrome inhis animal model.
In Developmental Dysmorphias, anomalies of adjacent structures (forexampte,
the temporal bone) affect the development of the TMJI:~In discussing development of
the TMJ, it was noted that the jointstructures grow laterally concomitant with
growth of the neurocranium. In cases of mandibular hypoplasia the intercondylar
width is usually normal suggesting that the temporal element is critical in establishing
 224 BRITISH JOURNAL OF O R A L S U R G E R Y

this dimension. Where the condyle is absent there is no well defined fossa or
eminence (Ross, 1979).
In recent years there has been more attention paid to internal derangements of the
TMJ, sucl~ as displacement of the disc, which usually occurs in an antero-lateral
direction. It must remain a matter of speculation but it is possible that a develop-
mental anomaly could cause or at least predispose to the displacement of the disc
possibly as a result of a tear of the posterior attachment.

Acknowledgements
I atu i~debted to David Gunning, Curator of the Warren Museum, Harvard Medical School, for access
to the Minor collection ,.ff human embryologic specimens and to my colleagues, Dr W. C. Guralnick,
Dr I.. B. Kaban, Dr R. B. Donoff, Dr A. Weber and Mr J. Healy for their helpful comments.

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