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Vascular supply to the developing teeth of rats.

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Vascular Supply to the Developing Teeth of R a t s
SOL BERNICK
Department of Anatomy, School of Medicine, University of Southern
California, Los AngeEes 7, California
The distribution of blood vessels to the
mature functional tooth and its supporting
structures has been demonstrated by many
investigators, (Bolings, '42, Russel and
Kramer, '56, Saunders, '57). These studies
have shown the general vascular patterns
to the pulp, periodontal membrane and
gingivae. On the other hand there is a
marked lack of information concerning the
distribution of blood vessels supplying the
developing tooth and periodontium. Thus
it was felt that a detailed systematic study
of the vascular patterns of the developing
tooth from the bell stage through functional occlusion was in order.
The rat was chosen for this study for
the following reasons : ( a ) primarily
through the necessity of having available
material exhibiting consecutive developmental, eruptive and functional age stages,
a situation which is difficult if not impossible to attain with human material, ( b ) ,
its size is such that one can section the intact head and trace fairly completely the
vascular patterns from the main arterial
trunk in the alveolar bone through the
teeth and periodontium to the final venous
drainage, and ( c ) , the molar teeth of the
rat are of limited growth and are similar in
both development and eruption to the human primary teeth.
MATERIAL AND METHODS
The teeth and jaws used in this study
were from rats ranging in age from 5 to 30
days. The animals were first anesthesized
with ether, and the blood vascular circulation was perfused through the heart with
physiological saline in order to wash out
the blood. The saline perfusion was then
replaced with an India ink gelatin solution.
Following the perfusion period the heads
were removed and fixed in a formol acetic
acid, alcohol solution, (90 cm3 95% alcohol; 10 cm3 formalin; 5 cm3 acetic acid).
The specimens were decalcified in a 10%
nitric acid in 10% formalin solution. After
adequate washing the specimens were dehydrated and infiltrated in the routine
manner for nitrocellulose embedding. The
embedded blocks of tissue were sectioned
from 100-250 microns in thickness. The
thick sections were cleared by the Spalteholz method and mounted unstained.
OBSERVATIONS
Early development
Bell stage. The earliest stage of tooth development studied in the present investigation is the bell stage. It is during this stage
of tooth development that the inner enamel
epithelium becomes transformed into columnar cells and also the time of the first
appearance of odontoblasts in the dental
papilla (fig. 1). To supply the enamel organ vascular plexuses arising from the
main alveolar vessels encircle the dental
sac giving off capillaries at the region of
the outer enamel epithelium. At this stage
no blood capillaries are seen entering the
enamel organ. At the basal region of the
developing tooth small caliber vessels originating from the main vascular trunk enter
the dental papilla. They soon divide and
become distributed mainly in the core of
the connective tissue. The peripheral limits of this vascular network are at the
future pulpal odontoblastic border (fig. 1).
Appositional stage. By the 5th day the
first and second molar teeth are in the
appositional stage. Both enamel and dentin have been deposited in the crown of the
tooth (fig. 2). Blood vessels originating in
the oral mucosa pass towards and penetrate the enamel organ to form a rich plexu s in the stellate reticulum. In the dental
papilla vessels are visible coursing mainly
towards the cuspal region. Figure 5 is a
high magnification view of the mesial surface of the first molar from a 5-day-old rat.
141
142
SOL BERNICK
Vascular branches from the main alveolar vessels pass occlusally in the dental sac
to anastomose with the perforating vessels
originating from the alveolar bone. In
their course occlusally capillaries are given
off which enter the enamel organ to form
a plexus in direct apposition to the ameloblasts. At the basal region of the forming
crown small caliber vessels are seen entering the dental papilla and pass towards
the lateral surface of the papilla. At first
these terminal branches are found located
at the basal surface of the odontoblasts.
However, at a more occlusal level the vasular network is located in the odontoblastic
layer, and at the cuspal region the capillaries are now located next to the developing
dentin. A high magnification view of the
occlusal surface of the same tooth is seen
in figure 6. A rich vascular plexus is observed in the stellate reticulum of the enamel organ. Capillary loops arising from
these vessels pass towards the ameloblastic
layer where they form a rich continuous
network in direct relationship to the amelooblasts. The cuspal vessels of the dental
papilla branch freely to send capillaries
through the odontoblastic layer to form an
anastomosing plexus next to the developing
dentin.
Prefunctio2al and functional
phases of eruption
A. General distribution. At the 15th day
the bifurcation of the roots of the :Erst
molar has already begun. Figure 3 i s a
mesiodistal view of the first molar of a
15-day-oldrat. The basic vascular patterns
supplying the occlusal surface of the tooth
has not changed since the earlier described
stage. At the base of the mesial root of the
developing first molar vessels from both
the mesial and distal surfaces of the apical
area enter the pulp. One vessel passes coronally to supply the lateral surface .while a
second vessel courses directly to the cuspal
horn. In this region these vessels break
up into a rich plexus. A third vessel takes
a distal course to anastomose with branches originating from the distal root.
By the 30th day, the upper Grst and
second molars are in functional occlusion.
There is now an apparent increase not only
in the caliber of the pulpal vessels but also
in the degree of arborization of these
branches (fig. 4).
B. Pulp. Figure 7 is a section of the interproximal region of the first and second
molars of a 15-day-old rat. Vessels are observed entering the pulp at the base of the
developing root. Arterial branches pass
towards the odontoblastic layer, but their
final arborization is limited to the basal
surface of the odontoblasts. However, at
the region of the cementoenamel junction
the capillary plexus has partially penetrated the odontoblastic layer whereas in
the coronal region of the pulp the capillary
network is not only found in the odontoblastic layer but is situated in direct relation to the developing predentin.
This basic relationship of blood vessels
to the odontoblasts and dentin persists in
the molar teeth of animals of age 21 to
30 days. Figure 8 is a view of the mesial
surface of the upper first molar from a 21day-old rat. At this age the first molar bas
erupted into the oral cavity. The position
of the terminal capillary network in the
apical root region may be seen at the base
of the odontoblasts. In contrast, at the
coronal region of the pulp the capillaries
are in direct apposition to the dentin. Even
at the time of functional occlusion, which
in the rat is at 30 days, this basic vascular
pattern is present in the pulp (fig. 9 ) .
C . Peridontal membrane. By the 15th
day the bifurcation of the root has taken
place (figs. 3 , 7). The vascular supply to
the developing periodontal membrane is
from two sources. Blood vessels enter the
periapical area and pass occlusally to anastomose with the perforating vessels arising
from the interseptal bone. As these vessels
pass gingivally, their course is limited to
the bony half of the periodontal membrane, and terminal twigs could not be
demonstrated in the cementa1 half of the
membrane. At the cementoenamel junction the vascular plexus continues into the
coronal region where branches are found
that are in direct association with the persisting ameloblasts (fig. 3 ) . By the 21st
day the gingiva is formed, and the reduced
enamel epithelium has become transformed into the epithelial attachment (fig.
8 ) . The vascular pattern of the periodontal membrane has not fundamentally
changed from what has been described
BLOOD SUPPLY TO DEVELOPING TEETH
above. The vessels are still limited in their
passage to the bony half of the membrane.
In the gingival area the blood vessels arising from the periodontal membrane are
found located directly underneath the basal surface of the epithleial attachment.
With further eruption into functional
occlusion the interalveolar bone becomes
dense in appearance. Figure 9 is a section
from the interproximal region of the first
and second molars from a 30-day-old animal. The blood vessels from the periapical
region plus the perforating branches proceed gingivally in the same manner as described above. At the transseptal region
a rich anastomosing plexus is formed from
( a ) branches originating from the periodontal membrane vessels of the distal surface of the first molar, (b) the mesial surface of the second molar, ( c ) and crestal
branches of the interseptal vessels. From
this anastomosis twigs arise that proceed
into the tunica propia of the gingiva to
terminate in direct apposition to the basal
surface of the epithelium.
D. Incisor. The blood vessels supplying
the upper incisor arise from the maxillary
alveolar vessels. In the region of the lingual periodontal bone branches arise and
penetrate the bone to enter the lingual periodontal membrane in the midregion. The
pulpal blood vessels of the incisors are
continuations of the posterior trunk of the
lingual periodontal vessels. At the base of
the incisor a multitude of branches enter
the pulp and immediately give off twigs
that pass towards the labial dentin (fig.
10). The position of the terminal capillary
network in relation to the dentin depends
upon the area of the tooth studied. Figure
11 is a high magnification of the odontogenic zone. At the base of this zone the
capillary plexus is limited to the base of
the odontoblasts, whereas at the anterior
portion of this figure the capillaries are
entering the odontoblastic zone. At the
midportion of the tooth the capillary plexuses are found in direct relation to the dentin (fig. 12).
The blood vessels supplying the labial
alveolar periosteum are derived from two
sources. Blood vessels originating from the
odontogenic zone proceed into the labial
alveolar periosteum. These vessels soon
anastomose with vessels entering the peri-
143
osteum from overlying bone. From this
network capillaries pass through the enamel organ to lie adjacent to the ameloblasts
(figs. 10, 11).
DISCUSSION
The problem of the vascular supply to
the developing teeth and periodontium has
been neglected by the earlier workers.
This apparent lack of study is partially due
to the difficulty in obtaining adequate human material to enable one to trace the
distribution of blood vessels in the progressive stages of tooth development and finally to functional occlusion. If one may
assume the fundamenutal findings observed in the rat are biologically similar
to the human, then the rat lends itself
readily to a study of vascular patterns to
the teeth and periodontium for several reasons. One can easily obtain an adequate
number of specimens varying in age from
birth to 30 days. In addition the size of
the animal is such that one can section the
intact head and follow fairly completely
the vascular pathways from the main
trunks in the alveolar bone to their terminal capillary loops in the developing teeth
and supporting structures.
As to the nature and extent of the vascular supply to the developing organ and
particularly to the ameloblasts there has
been considerable lack of knowledge regarding the relationship between blood
vessels to the various layers of the enamel
organ. In general the enamel organ is
described as being an avascular structure.
A typical description in textbooks reads as
follows : “The vascularized connective tissue surrounding the enamel organ on its
convexity is in close contact with the outer
enamel epithelium. The capillaries are
prolific in this area and protrude towards
the enamel organ. Immediately before
enamel formation commences capillaries
may invade the stellate reticulum” (Orban, ’57).
In the present study the limitation of the
blood vessels to the dental sac was observed
in the bell stage before the beginning of
amelogenesis. However, when amelogenesis has begun, blood vessels from both the
dental sac and oral mucosa invade the outter enamel epithelium to form a rich vascular plexus in the stellate reticulum. From
144
SOL BERNICK
this plexus capillaries pass towards and
finally form terminal loops directly adjacent to the basal surfaces of the ameloblasts.
This intimate relationship between blood
vessels and ameloblasts insures a rich inAux of nutrients from the blood to these
highly metabolic cells during their active
secretory phase. If, on the other hand, the
blood vessels were limited to even the stellate reticulum, only a limited flow of nutrients from the vascular structures to the
ameloblasts would take place. This intimacy between blood vessels and ameloblasts persists to the eruptive stage where
the reduced enamel epithelium becomes
transformed into the epithelial attachment.
How can one explain the difference between the findings of the present study
and the results of the previous investigations? The difficulty of obtaining sufficient
and adequate human material is probably
one of the major contributing factors. All
workers interested in tooth development
realize the difficulty in obtaining sufficient
numbers of late prenatal and early postnatal developmental stages. In addition if
one is fortunate to obtain such material,
the perfusion of the circulation would be
hampered greatly by the clotted blood and
thus prevent an adequate preparation for
study. A second reason to be discussed is
the comparative value between thick and
thin sections. If thin sections (less than
30 w ) either singly or serially are studied,
only fragments of the blood vessels may
be observed in the dental sac and even in
the stellate reticulum. On the other hand,
by studying sections of 100-200 microns
thickness not only may one gain a complete visualization of the vascular tree, but
an intimate relation of terminal vessels to
cells may be observed.
Dentogenesis
The terminal relation of the blood vessels in the pulp of both intact and extracted
teeth has been described by many workers.
They have all agreed that the capillaries
form terminal plexuses close to the odontoblasts at the pulpo-odontoblastic border.
On the other hand in the developing teeth
of the young rat the terminal position of
the pulpal capillaries depends upon the
surface area studied. If the basal cervical
area of the pulp is studied, the capillary
plexus is limited to the basal surface of
the odontoblasts. At a more occlusal area
where the dentin is more mature, the capillaries are seen passing into the odontoblastic zone, and in the region of the cuspal horn the capillaries have reached the
predentin to form a rich vascular network.
The main reason for the difference between the findings of the present investigation and those of the earlier workers is
probably due to the age difference of the
material studied. The previous investigations that are described in the literature
were completed on the teeth and jaws of
older animals or extracted teeth of man.
Limited studies by the author on the molar
teeth of one year old rats showed the same
terminal capillary relationship as described
by the earlier investigators, that is, the
terminal capillary networks were limited
to the basal surface of the odontoblasts.
However, i t is of further interest to note
that in these old animals the approximate
relation of the capillaries to the predentin
of the incisor remained similar to that described in young immature animals. This
is not surprising for the incisor is a continuously growing and erupting tooth, and
as such, undergoes a greater active dentin
formation than the molar teeth of limited
growth .
This intimate relationship of blood vessels to the forming dentin of young animals should not be so unexpected. I n the
process of dentinogenesis two steps occur.
The first is the manufacturing of the organic intercellular matrix, and second, its
calcification which is dependent on an
adequate supply of minerals which are
brought to the matrix by the blood vessels.
It is undoubtedly more efficient to have
these essential minerals brought in directIy to the uncalcified predentin instead
of diffusing through an odontoblastic layer.
Periodontal membrane
The blood supply to the periodontal
membrane of teeth from mature individuals has been described as being derived
from two sources, “ ( a ) from the periapical
area blood vessels enter the periodontal
membrane and pass gingivally in the
membrane, ( b ) in its course gingivally,
anastomosing branches are derived from
BLOOD SUPPLY T O DEVELOPING TEETH
the perforating blood vessels entering from
the openings in the alveolar bone. The
capillaries form a rich network in the periodontal membrane intertwining between
the fibers” (Orban, ’57).
In the development of the periodontal
membrane, alveolar bone, and the root
the above described vascular patterns may
be easily traced. The one factor that needs
elucidation is the position of the vessels
in their course through the membrane. In
the periodontal membrane of the young
immature animals the blood vessels pass
gingivally adjacent to the alveolar bone
leaving the cemental half of the membrane
free of blood vessels. Again, why the difference between the present study and
previous investigations? When the tooth
first erupts, the alveolar bone is much
larger than the root resulting in a wide
periodontal membrane. With the process
of aging the width of the periodontal membrane is reduced by the deposition of lamellar bone (Coolidge, ’37). Thus with the
narrowing of the periodontal membrane
with age, the blood vessels shift nearer to
the cementum allowing twigs to reach the
cemental region of the periodontal membrane.
SUMMARY
1. Young rats, 5-30 days old, were used
to study the vascular supply to the developing teeth and periodontium. The blood vessels were demonstrated by the saline-India
ink-gelatin perfusion method. The jaws
and teeth were fixed in a formol-acetic
acid-alcohol solution, decalcified, dehydrated, and embedded in nitro-cellulose in
145
the usual manner. The embedded specimens were sectioned at 150-200 microns
and cleared by the Spalteholz method,
mounted unstained.
2. At the bell stage of tooth development
the blood vessels are located at the periphery of the outer enamel epithelium and
at the pulpal odontoblastic border of the
dental papilla.
3 . At the beginning of the appositional
stage of tooth development blood vessels
penetrate the enamel organ to lie directly
adjacent to the ameloblasts, and this intimate relationship persists to the transformation to the epithelial attachment.
4. At the same time pulpal capillaries
reach the odontoblastic zone, penetrate
these cells, and form a network at the predentin border.
5. As the root forms the vessels pass
gingivally paralleling the bony surf ace of
the periodontal membrane with the cemental side being devoid of vessels. Above the
crest there is formed a rich transseptal
network which continues into the gingiva.
LITERATURE CITED
1942 Blood vessels of the dental
Boline.
-, L. R.
pulp. Anat. Rec., 82: 25-38.
Coolidge, E. D. 1937 The thicknesses of the
human periodontal membrane. J.A.D.A., 24:
1260-1269.
Orban, B. 1957 Oral Histology and Embryology, The C. V. Mosby Co., St. Louis, chap. 11,
chap. VII, pp. 37, 184.
Russel, L. H., and I. R. Kramer 1956 Observations on the vascular architecture of the dental
pulp. J. Dent. Res., 37: 957.
Saunders, R. L. de C. H. 1957 Microradiographic studies of human adult and fetal dental
pulp vessels X-Ray Microscopy and Microradiography, I: 561-571.
The bell stage of a third molar. Note that the blood vessels are limited to the outer
enamel epithelium of the enamel organ and the pulpo-odontoblastic border of the dental
papilla. x 35.
First upper molar from a 5-day-old rat. Note that the blood vessels from the oral mucosa
have penetrated the enamel organ to form a rich plexus i n the stellate reticulum. Also
observe the vessels entering the dental papilla to pass mainly towards the cuspal horn.
X 25.
Upper first molar from a 15-day-old rat. Note that the basic vascular patterns to the
enamel organ and root has not changed since the above described stage (fig. 2 ) . X 25.
Upper first molar from a 30-day-old rat. Note the apparent increase in the size of the
vessels in the pulp and their arborizations. Also observe the rich gingival vascular
network. X 25.
2
3
4
E X P L A N A T I O N OF FIGURES
PLATE 1
G., gingiva
L.P., labial alveolar periosteum
Li. P., lingual periodontal membrane
O., odontoblastic layer
O.O.E., outer enamel epithelium
P.M., periodontal membrane
Pu., pulp
S.R., stellate reticulum
Abbreviations to plates
1
A., ameloblasts
E., bone
C . , cementum
D., dentin
D.P., dental papilla
E., enamel
E.A., epithelial attachment
E.O., enamel organ
BLOOD SUPPLY TO DEVELOPING TEETH
Sol Bernick
PLATE 1
PLATE 2
EXPLANATION O F FIGURES
148
5
Medial surface of the upper first molar from a 5-day-old rat. Blood vessels originating
from the main alveolar trunk are seen passing occlusally in the dental sac and giving
off terminal loops that are in direct association with the ameloblasts. Note the various
locations of the terminal capillary networks along the lateral surface of the dental
papilla. x 250.
6
Occlusal surface of the upper first molar from a 5-day-old rat (same tooth as figure 5 ) .
Note: ( a ) vascular plexus in the stellate reticulum, ( b ) the terminal relation of the
capillary loops to the ameloblasts, and ( c ) the relation of the capillary loops to the
predentin. X 250.
7
Interproximal region between the upper first and second molars from a 15-day-old rat.
Note the terminal locations of the capillary loops a t the apical portion of the root, at
the cementoenamel junction, and a t the coronal portion of the pulp. Also follow the
course of the blood vessels i n the periodontal membrane and in the gingiva. X 250.
8
Mesial surface of the upper first molar from a 21-day-old rat. Note: ( a ) the relation
of the blood vessels to odontoblasts and predentin, ( b ) the absence of blood vessels in
the cementa1 half of the periodontal membrane, and ( c ) the close proximity of the
blood vessels to the epithelial attachment. X 250.
BLOOD SUPPLY TO DEVELOPING TEETH
PLATE 2
Sol Bernick
149
Interproximal region between the upper first and second molars from a 30-day-old rat.
Note: ( a ) increase i n the size and number of arborizations of the blood vessels i n the
pulp, ( b ) the vascular supply to the periodontal membrane, ( c ) the rich vascular
anastomosis a t the transseptal region, and ( d ) the relation of the capillaries to the basal
surface of the epithelium. x 250.
Odontogenic zone of the incisor of figure 10. Note that a t the basal region of the pulp,
the blood vessels are external to the odontoblasts while at the anterior region of the
figure the blood vessels are entering the odontoblastic zone. x 250.
Mid-portion of the incisor of figure 10. Note that the blood vessels have penetrated the
odontoblastic zone to lay in direct apposition to the predentin. x 250.
11
12
10 Upper incisor from a 21-day-old rat. Note the rich blood supply in the pulp arising from
continuations of the lingual periodontal vessels. x 35.
9
EXPLANATION OF FIGURES
PLATE 3
BLOOD SUPPLY TO DEVELOPING TEETH
Sol Bernick
PLATE 3
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