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Craniofacial biology Animal surgical experimentation and clinical practice.

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Craniof acial Biology : Animal Surgical Experimentation
and Clinical Practice
't2
B E R N A R D G . SARNAT
Department o f Plastic Surgery, Division o f Surgery, Cedars-Sinai Medical
Center und Research Institute; and Division o f Oral Biology,
School o f Dentistry, University o f California;
Los Angeles, California 90007
ABSTRACT
Studies are presented on the growth of the mandibIe in the pig,
growth of the frontonasal suture and snout in the rabbit, and the development
of the face and jaws in a human patient with anodontia. Growth of the snout
after extirpation of the frontonasal suture is contrasted with its growth following resection of the cartilaginous nasal septum. The results of the studies have
clinical applications in surgery and dentistry.
The basic blue print of a bone is inherent (Sarnat, '71). In addition, prenatal
and postnatal environmental factors influence growth, thereby affecting the external
form and internal architecture of part of
a bone to a complex of bones. Although
bone is hard, semirigid, and supporting, it
is also a dynamic, sensitive everchanging
tissue. An important physiologic concept is
that growth is active only during early life
whereas remodeling, with changes in size
and shape, and repair remain active
throughout life. The differential responses
and interrelationships of these processes
are important to recognition of both normal and pathologic conditions.
John Hunter (1778) proposed that resorption was as characteristic of bone
growth as apposition. Since bone remains
in a continuous state of apposition and resorption along periosteal and endosteal surfaces, the mass and shape of bones are
always subject to change. When the skeletal mass increases, as in children, total
apposition is greater than resorption and
both endochondral and sutural growth are
active. When the skeletal mass is constant,
as in the adult, apposition and resorption
are in equilibrium whereas both endochondral and sutural growth have ceased.
When the skeletal mass decreases in old
age, resorption is more active than apposition.
Any disturbance that affects the growth
activity of bones will produce some type
of deformity in any or all three planes:
AM. J. PnYs. ANTHROP.,38: 315-324.
height, width, and depth. The results of
injury are determined by the severity, duration, and type of noxious agent, and also
significantly by the time of occurrence. The
effect in infancy will be greater when there
is more growth activity than it will be later
in life when there is less activity and the
bones have assumed nearly adult size and
shape. The end result at any given time
records the effects of all the vicissitudes.
This report will consider by use of several examples the biology of facial bones
in terms of growth and remodeling, correlate this with the development of facial
deformities, and consider in the light of
this information some principles which
could be an aid in the prevention and
treatment of facial deformities and malocclusion.
The lower face
An understanding of normal growth of
the mandible forms the basis for early
recognition and proper surgical treatment
of some deformities. Mandibular growth
occurs in two ways. One is appositional
and resorptive with differential bone remodeling at various periosteal and endosteal surfaces. In the ramus, the posterior
border is a particularly active site of bone
apposition, whereas the anterior border is
a particularly active site of bone resorption.
1 This report was supported in part by research
grants HD 00179 from the National Institute of Child
Health and Human Development and RR05468. U. S.
Public Health Service.
2 Presented at the Fourth International Congress of
Primatology, Portland, Oregon, August 16, 1972.
315
316
BERNARD G. SARNAT
The second type of mandibular bone
growth is endochondral at the condyle.
Growth of the condyle and ramus is in a
superior and posterior direction. Because
the condyle articulates with the mandibular fossa of the temporal bone, the final
result is a downward and forward movement of the mandible. Normal development of the mandible is dependent upon
the synchronous co-ordination of the
growth activities of the various sites. By
means of both clinical and experimental
studies much information has been
obtained.
Robinson and Sarnat ('55) studied the
normal growth pattern of the pig mandible
with serial cephalometric radiographs in
combination with metallic implants (fig.
1). The condylar region contributed about
80% to total ramus height of the mandible.
The posterior border contributed as much
as 80% to total length of the mandible.
Since the amount of apposition at the posterior border was about twice the amount of
resorption at the anterior border, ramus
width increased (fig. 2). Resorption of the
anterior border of the ramus played a n important role in lengthening the body of the
Fig. 1A-B Lateral cephalometric radiographs of pig 12. Outline of ramus and body
drawn in. Note relation in figure 1A of four implants (3 in ramus and 1 in anterior part
of body) to various borders at this period. Note changed relation in figure 1B of four implants to various borders. Posterior border has grown away from implants in ramus. Anterior border of ramus has been progressively resorbed and is now closer to ramus implants.
Permanent first molar has erupted into occlusion; second molar is undergoing development in ramus. Crypts of permanent premolars are now visible as radiolucent areas at
apices of deciduous premolars (Robinson and Sarnat, '55).
CRANIOFACIAL BIOLOGY
317
h
GROWTH W T T E R N OF PIG MANDIBLE
8 Weeks
1
6 Weeks 020 Weeks
Fig. 2 Serial tracings of lateral cephalometric radiographs of pig 12 superposed on outlines of four implants. Note direction and amount of growth that has occurred between
various periods along all borders except anterior border of ramus which has been resorbed
(Robinson and Sarnat, ’55 ).
mandible in the molar region. Thus it may
be stated that in the growing mandible
“the ramus of today will be the body of
tomorrow.”
As the anterior border of the ramus continued to be resorbed it exposed not only
more and more of the body but also the
crowns of erupting permanent molars
which formed in what was initially the
center of the mandibular ramus. With
subsequent growth of the mandible and
the molar it finally erupted from what was
then the most posterior part of the body
of the mandible (fig. 3 ) . Before root formation was completed the erupting crown
was being freed by resorption of surrounding bone at the anterior border of the
ramus so as to allow it to erupt into occlusion with its maxillary opponent. Thus
mandibular body space was being created
a t the expense of the anterior border of the
ramus. There was a harmonious relation
between dental development and growth
of the mandible. This growth was not dependent upon the developing teeth. Normal
eruption of the permanent molars however, was entirely dependent upon the
normal growth of the mandibular ramus
which in turn may be directed by the activity of the condyle.
I n growth of the mandible the only
part subservient to erupting teeth was
alveolar bone. The contribution of alveolar
bone growth to the increase in mandibular
body height was about 60%. The roles
played by the alveolar processes and mandibular bone proper were quite different.
The important feature of alveolar bone was
its ability to serve the needs of the ever
changing requirements of the teeth. In
contrast however, the formed mandibular
bone remained constant, although there
were changes in proportion by surface
apposition.
Comment. Several clinical applications
can be made from the findings i n this
study. Growth in length of the mandible
occurred primarily at the ramus and not
in the body. Thus resection of the body of
the mandible in a child, because of a
tumor, should not alter growth in length.
The anterior and posterior segments however, should be maintained in position.
Diminished resorption of the anterior
border of the ramus will lead to unerupted
molars in the ramus. Conversely increased
resorption of the anterior border of the
ramus leads to a longer mandibular body
with ample opportunity for the molars to
erupt. In the growing mandible the body
is stable, except for changes a t its borders,
whereas the position of the alveolar bone
and teeth are subject to continual change.
318
BERNARD G . SARNAT
T h e upper face
The upper face and nose are subject to
a number of deformities, some of which
are the result of trauma. The cartilaginous
nasal septum and the frontonasal suture
are two sites of growth o f the nose and
adjacent regions. The present purpose is
to contrast the gross differential effect of
surgical trauma to the nasal bones and to
the cartilaginous nasal septum upon postnatal growth of the rabbit snout.
A. Growth at the frontonasal suture.
The method of metallic implantation was
utilized on either side of the frontonasal
suture to determine its contribution to the
growth of the snout in growing female
New Zealand albino rabbits (Selman and
Sarnat, '55). Dental amalgam was packed
into two undercut cavities prepared i n the
cortical plate of each nasal and frontal
bone (fig. 4A). For each pair of implants
on either side of the frontonasal suture the
distance was recorded. After the animals
were killed, the distances between the same
groups of implants were again measured
as a t the beginning of the experiment. The
increased distance was found after an 84day period to range from 10.6 to 11.9 mm
(fig. 5). Thus it was concluded that the
frontonasal suture was a site of growth.
B. Growth o f the snout after extirpation o f the frontonasal suture region. In
this group of rabbits amalgam was implanted in the frontal and nasal bones and
in addition the frontonasal suture was extirpated either unilaterally or bilaterally
(fig. 4B) (Selman and Sarnat, '57). The postoperative survival was as long as 84 days.
The distances between the same group
of implants, as in the previous experiment,
were determined at the beginning and at
the end of the experiment. The gross size
and shape of the snout, in the animals in
which the frontonasal suture had been unilaterally or bilaterally extirpated, was similar to that of the control animals. No
lateral deviation of the snout was observed
in the animals with a unilateral extirpation. Total longitudinal growth was essentially the same whether the suture had
been extirpated bilaterally, unilaterally, or
not at all. From these findings, it was concluded that the frontonasal suture, al-
though a site of growth, was a secondary
rather than a primary one.
C. Growth o f the snout after resection
o f cartilaginous nasal septum. The purpose was to determine the effects of resection of varying amounts of cartilaginous
nasal septum upon the snout i n growing
New Zealand albino rabbits (Sarnat and
Wexler, '66). The postoperative survival
ranged from 105 to 145 days. Antemortem
observations revealed a marked deficiency
of the upper face (fig. 6 ) . This was noted
in less than two months after resection of
a major portion of the nasal septum. Instead o f the long, smoothly curved tapered
face seen in the operated on and unoperated on controls, these animals exhibited
a short, rounded, stubby face with a pronounced indentation above the tip of the
nose. The appearance was suggestive of
a bull dog. The changes noted in the dissected skulls varied with the amount of
septum resected and the time of the experiment, Whereas the snout in the normal
animal was the prominent part of the anterior face and much larger than the anterior mandible, this was no longer true
in the experimental rabbit. There was a
deflection of the snout which was in contrast to the smoothly curved dorsum of the
control animals. The snout from above
was shorter. From below, the palate and
the incisive foramen were shorter. From
in front, the nasal aperture was much
Fig. 3 Serial tracings of lateral radiographs of
pig 12, illustrating calcification and eruption of
the permanent teeth correlated with growth of
the mandible. The tracings have been projected
in a vertical series on two lines, passing respectively through one implant, I, in the ramus and
another, I, in the body of the mandible. Since the
implants maintained a stable relationship to each
other, the vertical lines remained parallel. Thus,
the length of the body of the mandible between
the implants remained unchanged. This consistency does not apply to the teeth and alveolar
bone (fig. 2). Note the progressive resorption of
the anterior border of the ramus, exposing the
permanent molar crown and allowing it to erupt
into occlusion. The mandible increased in length,
owing to apposition of bone at both the posterior
and anterior (not ramus) borders. The teeth
moved superiorly followed by progressive addition
of alveolar bone. MI, M P , M3, permanent first,
second and third molars; MC, mandibular canal;
PE, Ps,P4, permanent second, third and fourth
premolars; PIT,PIII,and PI", deciduous second,
third and fourth premolars (Robinson and
Sarnat, '55).
319
CRANIOFACIAL BIOLOGY
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Figure 3
Fig. 4 Dorsahview of rabbit skulls, showing sites of implantation of silver amalgam in the
nasal and frontal bones. A, normal animal with frontonasal suture intact. A, A1, implants in frontal
and nasal bones; S, point on frontonasal suture where straight line crosses between AAI, etc. B,
animal i n which the frontonasal suture was extirpated, a, al, points on either side of extirpation
site where a straight line crosses between AAI, etc. (Selman and Sarnat, '57).
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CRANIOFACIAL BIOLOGY
32 1
Fig. 5 Serial ventrodorsal cephalometric radiographs of animal 21 taken A, at six weeks
of age B, ten weeks of age C, 16 weeks of age. Note changed skull form and increased
longitudinal separation of implants on either side of frontonasal suture. Distances between
implants in nasal bones and anterior margin of bones also increased with age. Distances
between implants within nasal or frontal bones remained constant. Tips of earposts are in
external auditory canals. Incisal pin is in position (Selman and Sarnat, '55).
smaller. The nasal bones were markedly
shorter, less wide and less high particularly toward the incisal end than those of
the control animals. The nasal bones converged toward the premaxilla with nasal
height and volume markedly reduced. The
premaxilla and its frontal process were also
markedly shorter.
Examination of the parasagitally sectioned crania revealed the extent of the
nasal septum and its relation to the snout
in the control animals and the relation of
the extent of the septal defect to the deformity of the snout in the experimental
animals. The site of the beginning of the
downward deflection of the nasal bones
was correlated with the posterior border of
the septal defect.
D. Comment. The amount of increase
in separation of the implants on either side
of the frontonasal suture indicated that
this was a site of growth. Since growth at
this region was not affected after resection
of the frontonasal suture, it was concluded
to be a secondary growth site. Resection of
cartilaginous nasal septum produced a
severe growth arrest of the snout and upper
face. From the above evidence it seems
likely that the growing cartilaginous nasal
septum is a primary and important growth
site of the snout and upper face. What are
the effects of resection of cartilaginous
nasal septum upon growth at the frontonasal suture?
Precise analogies cannot be made between rabbits and human beings. I n view
of the above findings however, it would be
advisable that young children, who have
sustained injuries to the cartilaginous
septum and nose, be treated and observed
not only for the immediate but also for
the late septal and nasal deformities. In
addition they should be followed for related deformities of the teeth, jaws, and
face. In children with complete bilateral
cleft palates, the upper jaw may be unable
to obtain a full expression of growth because of lack of contact with the septovomeral region. Furthermore, trauma to
the septal region, in cleft palate or septal
surgery, might have a n untoward effect
upon growth of the nose, upper jaw and
face.
The total face
The importance of the deciduous and
permanent teeth in the development of the
face and jaws has been a much debated
question for a long time. The ant eater,
who is born without teeth, has long jaws.
322
BERNARD G. SARNAT
A 21-month-old patient with complete
anodontia and ectodermal dysplasia presented a n unusual opportunity to study
this problem (Sarnat, Brodie and Kubacki,
'53 ). Serial cephalometric radiographs
were taken beyond 16 years of age (fig. 7 ) .
Study of the superposed tracings of the
radiographs indicated that growth was
within normal limits and that complete
absence of teeth did not significantly
impair development of the face and jaws,
with the exception of alveolar bone. Thus,
in surgery of the jaws, disturbance of the
teeth or tooth buds may lead to loss, malformation and/or malposition of teeth,
with changes in alveolar bone. The general size and shape of the face and jaws,
however, will not be affected.
LITERATURE CITED
Hunter, J. 1778 The Natural History of the
Human Teeth. Second ed. Johnson, London.
Robinson, I. B., and B. G. Sarnat 1955 Growth
pattern of the pig mandible. A serial roentgenographic study using metallic implants. Am.
J. Anat., 96: 37-64.
Sarnat, B. G. 1971 Surgical experimentation
and gross postnatal growth of the face and
jaws. J. Dent. Res., 50: 1462-1476.
Sarnat, B. G., A. G. Brodie and W. H. Kubacki
1953 A fourteen year report of facial growth
in case of complete anodontia with ectodermal
dysplasia. Amer. J. Dis. Child, 86: 162-169.
Sarnat, B. G., and M. R. Wexler 1966 Growth
of the face and jaws after resection of the
septa1 cartilage in the rabbit. Am. J. Anat., 118:
755-767.
Selman, A. J., and B. G. Sarnat 1955 Sutural
bone growth of the rabbit snout: A gross and
serial roentgenographic study by means of
metallic implants. Am. J. Anat., 97: 395-408
Selman, A. J., and B. G. Sarnat 1957 Growth
of the rabbit snout after extirpation of the
frontonasal suture: A gross and serial roentgenographic study by means of metallic implants. Am. J. Anat., 101: 273-293.
Fig. 6 Antemortem lateral, frontal, and dorsal
(retouched) views of rabbit 4 with minor amount
of nasal septum removed and rabbit 18 with
major amount of nasal septum removed at 21
days of age. Note contrast in facial appearance
and short, stubby, rounded face in animal 18,
with indentation above nostrils and overerupted
lower incisor (Sarnat and Wexler, '66).
Fig. 7 Lateral cephalometric radiographs of patient with complete anodontia. A, at three
years of age. B, at 16 years of age. Note complete absence of teeth or tooth buds. Compare A,
normal lack of development of the face and B, normal development of the face. Also note
in B the development of the frontal and maxillary sinuses and the ossification of the vertebrae
(Sarnat, Brodie and Kubacki, '53).
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