Acta Odontologica Scandinavica

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Basic mechanisms in craniofacial growth

Birgit Thilander

To cite this article: Birgit Thilander (1995) Basic mechanisms in craniofacial growth, Acta
Odontologica Scandinavica, 53:3, 144-151, DOI: 10.3109/00016359509005964

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 Basic mechanisms in craniofacial growth
Birgir Thilander
Department of Orthodontics, Goteborg University, Goteborg, Sweden

Thilander B. Basic mechanisms in craniofacial growth. Acta Odontol Scand 1995;53:144-151. Oslo. ISSN
000 1-63 5 7.
Bone growth is controlled by growth areas, not active growth centers as stated earlier. Conversion of
cartilage, sutural deposition, and periosteal remodeling are the basic phenomena involved in growth
mechanisms. The principles of bone growth will result in changes in the size and shape of the mandible
and the nasomaxillary complex in the three dimensions. The growth rate varies at different times during
the development of the child. The processes of facial growth and changes in the dental arches continue to
a much later age than had previously been realized. Although our knowledge of craniofacial growth has
increased during recent times, it is still incomplete with regard to the explanation for the regulation of
craniofacial growth. 0 Growth mechanism; growth pattern; mandibular growth; nasomaxilla9 growth
Birgit Thilander, Department of Orthodontics, Goteborg University, Medicinaregatan 12, S-413 90 Goteborg, Sweden
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The fully developed cranium represents the sum of its The development, growth, and maturation of the
separate parts, in which growth is highly differentiated skull comprise phenomena falling within the scope of
and occurs at different rates and in different directions, several disciplines and occurring at several levels,
and is thus a complex concept. By birth the craniofacial including the molecular, cellular tissue, and organ
skeleton has undergone between 30% and 60% of its levels. No specific method can therefore be assigned to
total growth. Although this reflects the early develop- the study of these events. The commonly used methods
ment of the skull, the remaining increase in size is not are embryologic research, use of tissue and organ cul-
equal rn all parts of the cranium. Whereas the size of tures, experiments on laboratory animals, twin studies,
the nruro-cranium will increase by about 50% after pathologic conditions (malformations or acquired
birth, the facial skeleton will grow to more than twice defects). Biometric and cephalometric data on cranio-
the size, the increase in height being the greatest facial growth usually serve to describe dimensional
(approximately 200%), that in depth somewhat smaller, changes between different bones and growth mech-
and that in the width the smallest (approximately 75%). anisms. All these different methods are the basis for
The growth of the soft tissues is also of importance. modern basic knowledge on craniofacial growth (4).
Changes in the soft-tissue profile with age follow the From experiences of all those studies we can state
growth in the underlying hard tissues but are not today that craniofacial growth may be divided into
directly correlated with those in bones. The convexity four components: growth mechanism (how new bone is
of the face increases with age, as nasal growth mainly formed), growth pattern (change in size and shape of
occurs in the anteroinferior direction. The lip profile the bone), growth rate (speed at which the bone is
also changes during childhood, due partly to growth formed), and the regulation mechanism, which initiates
and partly to changes in the dentition. and directs those three factors.
The old theory on facial growth, introduced by Brodie
( l ) , that the skull increases in size by direct symmetric
expansion of all surfaces and contours is an antiquated Growth mechanisms
statement. By the use of cephalometric radiography the
Bolton standards (2) will give the impression of a Growth and ossification of the cranium occurs in two
smooth downward and forward pattern of facial growth. ways: by growth and ossification of a cartilage model,
This is. however, also misleading. We have learned from endochondral ossification, and by a transformation of
years of research that the fully grown skull is not simply mesenchymal connective tissue and deposition of bone
a largcr version of the infant form and that the adult on existing bone surfaces, intramembranous ossi-
skull differs not only in size but also in shape from that fication. Whereas the bone of the skull base is mainly
of the child, depending on a process of differential of endochondral origin, the vault of the cranium and
growth in various parts of the cranium. This can be facial skeleton are mainly developed by intramem-
illustrated by superimposed tracings from boys and girls branous ossification.
with normal (‘ideal’) occlusion, followed from 7 years Although several ossified areas fuse into large mor-
up to 30 years of age (3) (Fig. 1). As can be seen, there phologic units, remnants of the chondrocranium persist
are obvious changes also in the period between 16 and as cartilaginous joints, synchondroses, between bones
30 years of age. in the cranial base. When intramembranously formed
 ACTA ODONTOL WAND 53 (1995) Mechnism in craniofacial growth 145

middle face consists entirely of a cartilage plate (nasal

septum), which is a part of the nasal capsule of the
chondrocranium (Fig. 3). In connection with ossifica-
tion of the cranial base, parts of this cartilage septum
are also ossified to form the ethmoid and vomer bones.
Thus only a small, anterior part of the original cartilage
persists postnatally. The nasal septum is thought to
play an important part in the prenatal and very early
postnatal growth of the middle face. Opinions differ,
however, as to its role in postnatal growth (8).
According to Scott (9), the septal cartilage occupies a
unique location for pushing the whole maxilla fonvard-
downward, and his famous nasal septal theory was born.
The opposing view, commonly termed the functional
matrix by Moss (lo), suggests that the nasal septal
cartilage is a locus of secondary, compensatory, and
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Fig. 1 . Templates from boys 7, 10, 13, 16, and 30 years of age (3), mechanical growth.
illustrating skeletal and soft-tissue changes.
Many experimental studies have been performed to
find evidence favoring the septal hypothesis or the func-
tional matrix hypothesis ( 1 1). The growth potential of
bones meet, sutures develop. Bone growth and adaption the nasal septum has been investigated by transplanting
can thus proceed as a result of continued separation of the whole septum, or parts of it, in ‘neutral’ environ-
bones in the synchondroses and suture areas. Premature ments (subcutaneously, intracerebrally) or in organ cul-
fusion or hindrance of separation for any other reason tures. Autoradiographic methods (tritiated thymidine
will result in an abnormal growth pattern for the bones or 35S-sulfate) have shown labeling throughout the
in question, with a risk of cranial deformity. whole septum. However, changes in site of growth
Bone growth is controlled by growth areas, not active activity were observed, as were age-specific differences
growth centers as stated earlier. The following basic in this activity. Experiments involving partial or total
phenomena are involved in the growth mechanisms: removal of the septum have given different results.
conversion of cartilage (synchondroses, nasal septal car- Sarnat (12) found a significant decrease in growth of
tilage, condylar cartilage), sutural deposition, and peri- the nasal complex when such a procedure was carried
osteal remodeling. out in the young rabbit. Stenstrom & Thilander (13),
however, found no or only little change in the dimension
Synchondroses of the snout of growing guinea pigs after such surgical
extirpations, results in agreement with those of Moss et
Displacement growth in the cranial base is made al. (14) in growing rats.
possible mainly by the synchondroses. Only a few per- A review of the pertinent literature on the role of the
sist postnatally in the region of the cranial midbase, the nasal septal cartilage in postnatal midfacial growth will
spheno-occipital synchondrosis being the most impor- conclude that its growth is secondary to and com-
tant one (5, 6 ) . pensatory for a prior passive displacement of the mid-
The young human synchondrosis consists of a bipolar facial bones but plays a significant biomechanical role
‘epiphyseal’ plate with endochondral ossification (Fig. in maintaining normal midfacial form (1 1, 14).
2), and its structural organization changes with age.
The hyaline cartilage is partly replaced by fibrocartilage
in the superior part, which becomes narrower through Condylar cartilage
ossification from both sides, and is completely covered This is a secondary type of cartilage and thus differs
with bone by the age of 12-13 years in girls and some morphologically from epiphyseal and synchondrosal
years later in boys. The synchondroses of the cranial cartilage. It participates in growth early in human life
base may be regarded as special joints enabling growth and absorbs pressure forces later in life. Its histo-
to take place at younger ages. The postnatal importance morphologic picture varies from birth to adulthood (15)
of the spheno-occipital synchondrosis, sometimes con- (Fig. 4).
sidered the driving force for skull base growth, has been The role of the condylar cartilage in mandibular
questioned. It is more likely that this cartilage plays a growth is a subject of controversy (7). It has previously
relatively greater role in the adjustment changes in been claimed that it was expansive, similar to the
cranial base flexure than in its linear growth (7). epiphyseal cartilage, thereby pushing the mandible for-
ward. The information at hand indicates that the con-
Nasal septal cartilage dyle and its cartilage participate only in regional
During the fetal period the midsagittal part of the adaptive growth and are thus not a major growth center
 146 B . Thilandcr ACTA ODONTOL SCAND 53 (1995)
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Fig. 2. Photomicrographs from the human speno-occipital syn-

chondrosis at 7 months and 15 years ofage (closure in progress).

for thc whole mandible. The condyle has a great capa- lar growth’ is therefore misleading. ‘Ramus and condy-
city $0 adapt to mandibular displacement during lar growth’ is more correct (1 6).
growth. As the condyle is also a part of the ramus, the
fibrous layers of condylar cartilage are continuous with
the periosteum of the ramus, and remodeling processes Sutures
are seen in all components of thejoint. The term ‘condy- Displacement growth is made possible by the cranio-
facial sutures, which have a dual function of permitting
growth movement and uniting the bones of the cranium
(Fig. 5). The fibrous component of the suture increases
with age, and bundles of fibers can be seen running
transversally across the suture and further increasing
the mechanical strength of the joint (17 ) . When cranial
growth ceases, most sutures ossify. Animal studies indi-
cate that the bone movements resulting from growth
also regulate the development of the sutures.

Periosteum
A periosteal cell layer, the inner cambium layer, is
established with the initiation of the intramembranous
ossification of bone, and the surrounding mesenchymal
Fig. 3. I‘he human nasal cartilage from a 5-month-old fetus. A small cells acquire the character of osteoblasts (Fig. 6).
part of the original cartilage, anterior to the dotted line, persists Bone growth presupposes a continuous replacement
postnatally. of matrix-producing cells via cell division in the cam-
 ACTA ODONTOL SCAND 53 (1995) Mechanism in naniofacial growth 147

erative capacity is extremely high in the young child.

The influence of the periosteum is of greatest sig-
nificance for the change in size and shape of the bones
(the growth pattern).

Growth pattern
Bone grows by two fundamental physiologic processes,
modeling and remodeling. Modeling is a surface-specific
activity (apposition and resorption) that produces a
change in the size and shape of the bone. Remodeling,
however, occurs in the bone tissues as reconstruction of
bone by turnover of previously existing osseous tissue
(Haversian system) and rebuilding at the molecular
level (biochemical remodeling). The process we are
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dealing with in facial morphogenesis is growth

remodeling-that is, both modeling and remodeling are
included in this term. In the present paper the term
‘remodeling’ in its wide concept will be used.
Most articles and textbooks dealing with growth prin-
ciples refer to Enlow’s theories (16). According to him,
the change in size and shape of the bone takes place on
the basis of several basic principles: remodeling, cortical
drift, relocation, displacement, and ‘V-principle’. His
original studies were based on 25 human mandibles,
obtained from cadaver material or from commercial
supply houses (18). Information on race and sex was
uncertain in most cases. The two halves of the mandibles
were sawed into transversal sections and studied micro-
scopically. In adult specimens extensive structural
changes had taken place in the compact bone tissue.
Therefore, only mandibles having primary and mixed
dentitions were studied; the number is not given.
The continuous remodeling serves to maintain the
shape and proportions of the bone throughout the
growth period. As bone deposition occurs during a
coincident breakdown of opposing bone surfaces, the
bone will migrate in relation to a fixed structure. This
migration through remodeling is known as drift. As a
general rule, the surface towards which growth occurs
is appositional, whereas the surface facing away from
the direction of growth is resorptive. The two processes
need not occur with the same intensity, but, rather,
Fig. 4. Photomicrographs from the human condylar cartilage at appositional activity normally exceeds resorption dur-
different ages (newborn, 6 years, and 20 years). ing the growth period.
Due to new bone deposition on one surface, all other
parts of the structure will undergo shifts in relative
position, a movement that is termed relocation. As a
bium layer. Owing to their location, both matrix-pro- result of this process, further adaptive bone remodeling
ducing and proliferating cells are subject to mechanical has to take place, to adjust shape and size of the bone
influence. If the pressure exceeds a certain threshold to its new position. An example of such passive drift in
level, so that the blood supply to these cells is reduced, the facial region is the hard palate, which subsides in
osteogenesis ceases and osteoclasts appear until a bio- relation to the overlying structures, due to resorption of
chemical equilibrium is restored. If, on the other hand, the nasal floor and concomitant deposition on the roof
the periosteum is exposed to tension, it responds with of the palate. Relocation and structural remodeling thus
bone deposition. The periosteum continues to function are closely related to each other.
as an osteogenic zone throughout life, but its regen- At the same time as the nasal floor subsides owing to
 148 H. Thilandcr ACTA ODONTOL SCAND 53 (1995)
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Fig. 5. Photomicrographsfrom the human intermaxillary suture at different ages (14 to 25 years), showing
various stages of fusion.

remodeling, the whole maxilla also subsides in relation ment, and it always takes place in the direction opposite
to the hase of the cranium. This more active movement to the vector of bone growth. The secondary dis-
of a whole bone is called translation or displacement, placement is not associated with growth of the bone
which i s both primary and secondary. The primary itself but initiated by enlargement of adjacent bones
displacement is associated with a bone’s own enlarge- and soft structures and transferred to adjacent bones.
 ACTA ODONTOL WAND 53 (1995) Mechanisnu in craniofacial growth 149

therefore the result of two separate growth processes:

drift, owing to remodeling growth, and displacement,
owing to movement of the maxilla as a whole. Any
attempt to study the separate roles of these processes
would require access to fixed points in the bone tissue
(for example, metal indicators), or else the use of his-
tologic methods such as bone labeling. A knowledge of
these separate processes in bone tissue movement is
essential for a proper understanding of growth events
and the effects of various forms of treatment. An ortho-
pedic force or pathologic fusion of sutures, for example,
may prevent normal growth through displacement but
need not necessarily prevent drift from continuing or
even increasing, to compensate for this absence of dis-
placement growth.
Fig. 6. Intramembranous bone covered with periosteum. It is important to note that the vertical growth of the
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alveolar process is rapid during tooth eruption and

exceeds the lowering of the roof of the palate threefold.
The transversal growth occurs by separation of the
The significance of the interplay between deposition two maxillary bodies in the median suture, i.e. lateral
and resorption for the shape of the various bones may displacement, and bone resorption on the lateral walls
be difficult to perceive in the case of complex structures. of the nasal cavity. During tooth eruption the alveolar
Enlow (16) has shown, however, that many of these process increases in transversal dimension due to the
structures are V-shaped and that the same basic rules buccal eruption path of the premolars and molars.
can be applied to all of them. Deposition on the inside
of the V in the direction of growth and resorption on
the outside enables the bone to retain its characteristic
shape during growth, the V-principle. Growth of the mandible
These principles of bone growth will result in the Like the nasomaxillary complex, the mandible grows
following changes in size and shape of the nasomaxillary forward and downward mainly as a result of dis-
complex and mandible. placement (both primary and secondary) of the whole
bone. This creates the conditions for a simultaneous
growth in the size of the bone in the opposite direction,
Growth o f the nasornaxillary complex including a lengthening of the basal arch at the condyle.
The anterior growth is mainly the result of dis- Deposition thus occurs on the posterior margin of the
placement of the two maxillary bodies. The dimensional ramus, with simultaneous bone resorption along its
increase occurs mainly in the opposite direction, by bone anterior contours.
deposition on the tuberosity. This upward-backward Because of its early fusion, the mandibular symphysis
relocation will result in a primary forward-downward plays little part in the postnatal growth in the width.
displacement of the maxillary bones, together with a As the two rami have a diverging V-shape, the growth
secondary displacement of the adjacent bones (nasal, in width will occur, due to the V-principle. A complex
orbital). These tensile forces initiate adaptive sutural sequence of remodeling changes takes place during the
growth. The alveolar base is thereby elongated, creating growth of the mandibular body (18). A buccal drift of
space for posterior and late-erupting teeth. The anterior the mandibular body is seen as bone is added on the
surface, on the other hand, is fairly stable from a growth buccal side, with corresponding resorption and endos-
point of view. teal bone formation on the lingual side. Our own studies,
The vertical growth is the combined result of lowering placing fixtures in jaws of growing pigs, are clearly in
of the maxilla as a whole and a remodeling at the bone agreement with these principles (20).
surfaces, as shown by Bjork & Skieller (19) in a sample Displacement of the mandible is associated with a
of boys 4 to 20 years old. The displacement of the rotation, depending on the direction of the condylar
maxilla, classified as sutural lowering of the bone, cre- growth. Anterior (forward) rotation will take place in

t
ates space for a expansion of the nasal cavity and orbits
of the eyes. Lo ering of the orbital floor is limited by a
certain bone deposition towards the orbits, but the floor
subjects with an upward and forward direction ofcondy-
lar growth, whereas in subjects with predominantly
backward direction of the condylar growth the mandible
of the nasal cavity continues to be lowered owing to will rotate in a posterior (backward) direction (21).
resorption nasally, with simultaneous deposition of bone Coincident remodeling along the inferior margin of the
orally on the palate. The movement of the nasal floor mandible reduces the apparent effect of this rotation on
in relation to overlying structures during growth is the facial morphology. This is especially true in subjects
 ACTA ODONTOL SCAND 53 (1995)

with an anterior rotation pattern, in whom about half sidered suture growth to be a response to growth in
of the mandibular rotation is masked in this manner. adjacent structures, which carried the genetic infor-
T h r mechanism underlying the rotation of the jaws mation (epigenetic regulation). The displacement of the
is obscure. It was previously believed that growth of bones of the cerebral cranium was now considered to
the rondylar cartilage was the cause of mandibular be secondary to the morphogenetic requirements of the
displacement, on the basis of the assumption that the brain mass, whereas the growth of the middle face was
condyles govern the growth of the entire mandile (‘push’ mainly the result of growth of the chondrocranium-
theory). However, they are not a type of ‘control center’ above all the nasal septum-which pushed the bones
with direct control over the growth fields but function away from the structures in the cranial base. Similarly,
only locally. According to these growth theories, man- the growth of the mandible was considered to be the
dibular displacement is the primary process and results result of the autonomic expansive growth of the condylar
from mlargement of the soft tissues (22). The type of cartilage.
rotation (upward or downward) is determined by those On the basis of new information concerning the physi-
structures that start the displacement of the mandible, ology of bone, Moss (10) launched a completely new
and the direction of condylar growth thus is a secondary theory on the control of craniofacial growth. The osteo-
phenomenon to adapt for the space in the temporo- genic tissue was deprived of all innate genetic control
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mandibular joint region (‘pull’ theory). (‘bone has no genes’), and the theory of the functional
matrix was formulated instead. The craniofacial com-
plex is regarded as a structure with certain functions,
Growth rate classified as functional cranial components. These con-
sist of a functional matrix, comprising the tissues and
The basic pattern of growth is further complicated in cavities that carry out the function as such, and a
that the rate at which adult size is achieved is not skeletal unit, consisting of bone, cartilage, and tendons,
constant. The speed varies at different times during the which protects and supports this matrix. Parts of the
development of the child. Recent studies suggest that functional matrix can be shown to have direct influence
the process of facial growth and changes in the dental on the bone through the periosteum-for example,
arches continue to a much later age than had previously muscle function in muscle insertions and the teeth in
been iealized (23). The changes observed are small, the alveolar process-and are therefore referred to as
affecting both the size and the shape of the face and the the periosteal matrix. This control of osteogenesis is a
dentition. local process comprising remodeling and drift and is
limited to changes in the size and shape of small skeletal
units. A broader effect is achieved by the tissues and
Regulation mechanisms functional cavities surrounded by capsules, summarized
by the term capsular matrix-for example, the brain
Postnatal growth processes occur within their individual
mass and respiratory function-which produce the
structures to various extents at different intervals and
movement of the whole bone classified as displacement.
in various directions. The control of such a komplex
Other hypotheses assume that postnatal facial growth
morphogenesis requires a precise biologic regulator
is controlled by a multifactorial system that is influenced
mechanism for initiating and directing the growth mech-
anisms, growth pattern, and growth rate. by intrinsic, genetic, and local factors. According to van
‘The regularity with which the child’s face grows, with Limborgh (25), craniofacial morphogenesis is controlled
maintrnance of the general morphology and resem- by five different factors: intrinsic genetic factors, local
blance to relatives, suggests that genetic factors have a and general epigenetic factors, and local and general
strong influence on craniofacial growth. Craniofacial environmental factors. According to this theory, both
morphology is now considered to be multifactorial; that local and general factors can cause anomalies.
is, facial development is influenced by several genes The intrinsic genetic factors exert their influence
together with various environmental factors. within the cells in which they are contained and deter-
Even in the 1940s, Sicher (24), among others, was mine the characteristics of cells and tissues (cranial
still claiming that craniofacial growth as a whole was differentiation). Epigenetic factors are those that are
the result of innate genetic formation in the skeletal determined genetically but are effective outside the cells
tissues. The importance of environmental factors, such and tissues in which they are produced. According to
as pressure from adjacent organs, was reduced to a van Limborgh, these factors can have an effect on the
certain influence on the shape of the bone during devel- adjacent structures such as local epigenetic factors (for
opment. example, embryonic induction influences) or have a
As this view was incompatible with several clinical distant influence such as general epigenetic factors (for
observations, Scott (9) limited the heredity and expan- example, sex and growth hormones). The local en\won- ‘

sive growth of the osteogenic tissues to the periosteum mental factors (such as muscular force) are of much
and chondral structures. I n contrast to Sicher, he con- greater relevance to the postnatal craniofacial growth
 ACTA O W N T O L SCAND 53 (1995) Mechanisms in craniofacial growth 151

control than the general factors (for example, food, 5. Melsen B. The cranial base. Acta Odontol Scand 1974;32 Suppl
62.
oxygen supply). 6. Thilander B, Ingervall B. The human sphenooccipital syn-
On the basis of studies on growth in the rat, Petrovic chondrosis. 11. A histological and microradiographic study of its
et al. (26) have developed a cybernetic model (direction growth. Acta Odontol Scand 1976;31:323-36.
and control of a course of events), illustrating the com- 7. Koski K. Mechanisms of craniofacial skeletal growth. In: Barrer
plexities of multifactorial relationships involved in the HC, editor. Orthodontics. The state of the art. Philadelphia:
University of Pennsylvania Press, 1981.
growth process. In sum, the physiologic effect of factors 8. Melsen B. Histological analysis of the postnatal development of
controlling the facial growth is not limited to simple the nasal septum. Angle Orthodont 1977;47:83-96.
commands but includes relays, implying interactions 9. Scott JH. The growth of the craniofacial skeleton. In J Med Sci
and feedback loops as follows: 1) all of them form a 1962;438:276-86.
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structured system, a servosystem, in which the position editors. Vistas in orthodontics. Philadelphia: Lea & Febiger, 1962.
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‘comparator’; 2) the sagittal position of the upper dental strain of hypopituitary dwarf mouse. Eur J Orthod 1994;16:13%
arch is the ‘constant changing reference input’, con- 48.
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of the midface. Craniofacial Growth Series, Vol 6. Ann Arbor
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It can be stated that, although our knowledge of cra- 1977;4:5%64.
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14:99-109.
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