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The histology and rate of tooth eruption with and without temporary impaction in the dog.

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The Histology and R a t e of Tooth Eruption with
and without Temporary Impaction in the Dog'
DONALD R. CAHILL*
Department of A n a t o m y , T e m p l e University,
Philadelphia, Pennsylvania
ABSTRACT
Eruption was studied b j experimentally impacting and releasing permanent premolars in puppies. Eruption rates of both normal and experimentally delayed teeth were calculated from weekly radiographs. The rate of normal eruption is
triphasic and similar to a normal growth curve. It has an initial slow exponential
rate which changes to a more rapid exponential rate followed in turn by a terminal
plateau. AU of the teeth released from impaction erupted and their rates exceeded or
equaled the normal rate.
The morphology of the bony trabeculae beneath the erupting teeth and the relative
amount of soft tissue between the bone and teeth are expressions of the eruptive rate.
The trabeculae around rapidly erupting teeth are thinner, more delicate and more
widely separated from one another than those of slowly erupting teeth. Trabecular
orientation aligns with the direction of eruption, showing not only its vertical component, but also whether the tooth moved mesially or distally during eruption.
When erupting teeth were experimentally immobilized within the mandible, thus
eliminating direct and continual pressure
on the overlying bone by the tooth, eruption pathways formed in the same marcner as in normal eruption (Cahill, '69;.
That investigation demonstrated that the
mechanism of pathway formation is nct
dependent upon direct and continual pre5;sure from the erupting tooth.
The present investigation utilizes the
same early immobilization technique except that the teeth were released from
impaction by removing the restraining
wires. This was done to determine whether
the teeth would erupt through pathways
which formed during the immobilizatioii
period. Furthermore, the normal eruption
rate was established to provide a baseline
for evaluating the experimental findings.
their eruptive movement (Cahill, '69),
then after the desired delay, the teeth were
allowed to continue eruption by removing
the restraining wires. The length of the
delays ranged from 4-7 weeks at varying
times during the normal eruptive period.
Onset, duration and time of release for
the impactions is shown in figure 1A and
B. Here, the flat portion of the curves illustrates the absence of eruptive movement and the sharp change in slope - the
time of wire removal. In all cases, the left
side of the animal was the control side;
the right, the experimental side.
Measurements for the eruption rates
were made to the nearest millimeter from
a line drawn along the base of the mandible perpendicularly upward to the apex of
the crown on a series of dental radiographs
taken at weekly intervals. Error in measuring tooth position by this method is
negligible because this distance did not
MATERIALS AND METHODS
change during impaction periods. This inEruption of normal and experimentally dicates that there is no appreciable growth
delayed permanent third premolars in the at the lower border of the mandible and
mandible of medium-sized mongrel pup- that it is a stable reference for measurepies was studied from the thirteenth ment during the period studied.
The tissues were prepared for microthrough the twenty-seventh postnata 1
weeks. The normal eruption rate was cal- scopic examination by decalcification and
culated and compared with the eruption
Received Aug. 4, '69. Accepted Sept. 24, '69.
rates of the experimentally delayed teeth.
1 Supported by USPHS grant 1 SO 1 FR 5417-04-5.
2 Present
address: Department of Biostructure,
Teeth were impacted by lacing wire
Medical and Dental School, Northwestern University,
through the mandible (fig. 10A) to sto:3 Chicago, Illinois 60611.
ANAT.REC.. 166: 225-238.
225
226
DONALD R. CAHILL
paraffin processing, cited in greater detail
by Cahill, '69. Serial sections were cut at
12
and stained with hematoxylin and
eosin.
OBSERVATIONS
Tooth eruption rates: Normal
and after release from
impaction
To calculate the eruption rate of third
permanent mandibular premolars in the
puppy, tooth position versus animal age
(distance vs time) was plotted on semilog
paper (figs. 2A,B) from the measurements
taken from the weekly radiographs. The
time range studied (thirteenth through
the twenty-seventh postnatal weeks) includes the normal eruption period of this
tooth.
Since the individual graphs (figs. 2A,B)
were remarkably similar in shape, the
average rate was plotted by superimposing
them (fig. 2C, solid line). The twentieth
week was selected for superimposition
because all curves, whether complete or
incomplete, crossed this midpoint of the
time range studied. Tooth position at 1 3
weeks was arbitrarily designated 1.0 and
thus positions on the average rate curve
are relative to one another and not actual
distances from the base of the mandible
to any particular crown.
On semilog paper, the average eruption
rate (fig. 2C) is triphasic and its first two
parts are exponential. The first part, from
13 to 18 weeks, depicts a slow exponential
rate with root formation commencing on
the fifteenth week. Shortly after the eighteenth week the teeth begin the second
phase which is characterized by a much
more rapid exponential rate. At 21.3
weeks, about halfway through the rapid
phase, the crowns begin emerging from
the bone and at 22.4 weeks pierce the
gingiva. The third part of the curve shows
that the rate decreases late in the twentythird week when the teeth gain functional
occlusion.
Release from impaction was studied in
seven of the eight animals; their rate
curves are shown in figures 1A-D. The
mandible, as shown radiographically in
cross section (fig. 6B), developed atypically in one case in which the eruption path-
way failed to form in the usual manner.
This caused the tooth to erupt noticeably
slower than others after release and as
an exception, it was not included in the
graphs.
As in figure 2, the data for eruption
after delay are presented as tooth position
(from the crown to the base of the mandible) versus animal age. Figures IC and
D are composites formed by normalizing
all curves to a common origin where
distance at release equals 1.0 and time at
release equals zero. The data are presented
in this manner to emphasize characteristics of movement after release from impaction.
All of the released teeth showed eruptive movement and, during the first week,
six of the seven erupted at the maximal
rate (fig. l D , Oj) after the restraining
wires were removed. The eruption rate
diminished after the first week but in two
specimens it was only slightly slower than
the maximal rate (fig. lD, Or). The remaining three, although even slower (fig.
l C , C; fig. l D , Oc), were comparable to
the rapid rate of normal eruption.
Histologic and radiologic findings
of teeth released from
impaction
These observations are grouped and
presented in the sequence: ( 1 ) the group
sacrificed one week after release, i.e.,
showing the maximal rate (figs. 3,4); (2)
the group continuing a rapid but slightly
slower rate after the first week (figs. 8 , l O ) ;
and ( 3 ) the lowest group, a rate which,
however, matched the normal eruptive
rate after the first week (fig. 1 1 ) .
The most striking finding after a week
of movement is the new, relatively radiolucent tissue that separates the tooth in
its new position from the rim of old bone
that marked its previous location (figs. 3,
4,5). This tissue contains thin, interconnected trabeculae radiating upward from
the outline of old bone to the tooth (figs.
3,4). It also contains the prospective
periodontal ligament and clusters of osteoblasts (fig. 7) forming the rapidly developing trabeculae. After the first week of
maximal movement, distance between the
tooth and the old bone can be measured
EXPERIMENTAL STUDY OF TOOTH ERUPTION
radiographically (fig. 5), however, as remodeling takes place, the sharp outline
of old bone is gradually lost and from
that time accurate measurement can no
longer be made.
Group 11, demonstrating continued rapid movement at a slightly reduced rate,
is characterized by the specimen shown
in figure 8. Prior to release, this tooth was
experimentally immobilized for seven
weeks. After release, it erupted for three
weeks and then process was terminated
for histologic examination. The stringy,
radiate pattern of delicate trabeculae beneath the roots, and in the interradicular
area is similar to that described for the
first group. These features are characteristic of rapid movement. Trabecular orientation aligns with the direction of eruption, showing not only its vertical coniponent, but also whether the tooth moved
mesially or distally during eruption.
Comparison of the rapidly erupting released teeth (fig. 8) with controls (fig. 9 )
shows that the trabeculae beneath the
normally erupting teeth are thicker than
the trabeculae beneath the released teeth.
Furthermore, there is considerably more
soft tissue (mainly osteoblasts and osteoid
material) between the bone and the tooth
on the more rapidly erupting side than on
the normal side; thus the size of the
trabeculae and the amount of soft tissue
between the old bone and the tooth i n dicate the rate of movement.
A radiographic series in figure 10 shows
the rapid eruption of the tooth just dcscribed. The radiolucent area above thse
impacted tooth (fig. 10A) is the eruption
pathway. This pathway formed during thipreceding period of immobilization. Figurls
10B shows the tooth one week after release i.e., after the maximal rate period,
and figure 1OC shows its position threlc
weeks after release. In the three weeks
following release, the tooth erupted almost
as much as a normal tooth (fig. 10D) in
six weeks of rapid eruption.
The third group ( 3 specimens) showed
an eruptive rate nearly identical with the
rate at the middle of the normal eruptive
curve. This slower eruption rate is characterized histologicaIIy by the bony trabeculae which are similar to those of the
controls. Assumed reasons for the slower
227
eruptive rate are not conclusive; however,
two of the three impacted teeth in this
group became misdirected into adjacent
bone (fig. 11) rather than into the preformed emption pathway. This probably
retarded a potentially greater rate. Reasons for the slower rate in the third case
were not apparent.
DISCUSSION
Releasing teeth from experimental impactions, maintained for varying periods
during prefunctional eruption, is a useful
method for studying tooth eruption. It is
particularly valuable as it reveals that
released teeth erupt rapidly through channels which formed during the impaction.
Characteristics and significance of delayed
eruption were compared both histologically
and radiologically with normal eruption,
wherein establishment of the normal
eruption rate was an essential factor.
Normal eruption
The normal prefunctional eruption rate
is triphasic showing successive slow and
fast periods of exponential movement and
a terminal plateau. Root formation begins on the fifteenth week, that is during
the slower period of exponential movement, about three weeks before the rapid
exponential phase. This finding supports
Weinmann's ('41) study of human embryos. More recently descriptions of prefunctional emption, partially stemming
from Weinmann ('41), have drifted away
from this observation as they now key
the onset of rapid eruption to root formation (Orban, '66) and (Provenza, '64).
In the dog, the prefunctional phase terminates late in the twenty-third week (fig.
2C) when the teeth reach the occlusal
plane.
The exponential character of the eruption rate is a previously unreported finding, and the general shape of its curve
resembles the normal growth curve. It is
significant that the rapid exponential
phase commences about three weeks before the crown begins to emerge from the
mandible. The exponential eruption rate
is possibly a reflection of a corresponding
exponential increase in tissue mass by
cells responsible for eruptive movement.
228
DONALD R. CAHILL
However, such a volumetric increase in
tissue through cellular activity would entail more than cell division; it would also
involve the formation or deposition of a
considerable amount of extracellular material, i.e. collagen and mineral matter.
Correlating eruption rate with tissue mass
increase is further complicated because at
present, it is not possible to attribute
eruption rate specifically to any of the
various cell types (osteoblasts, fibroblasts,
cementoblasts) or to their relative participation, Along this line, however, Kenny
and Ramfjord ('69) show that the radioactive index (percentage of labelled cells)
of osteoblasts near the root apex during
eruption is considerably higher than cementoblasts. That both cell types become
differentially labelled during normal eruption indicates their approximate contribution to increase in tissue mass through
mitosis, but not through such functions
as collagen formation. At present, relating
exponential increase in tissue mass to the
known exponential eruption rate remains
an interesting possibility; however, the
requisite details about cellular activity
during eruption which would be necessary
to test this hypothesis are not currently
available.
Delayed eruption
Rapid eruptive movement began as
soon as the restraining wires were removed; some teeth continuing to move
more rapidly than others after the initial
fast period. In every instance, however,
eruption rates of released teeth exceeded
or equaled the normal rate. Their eruption pathways were formed by osteoclastic
activity during the period of restraint
(Cahill, '69). Although no attempt was
made to determine whether more prolonged impaction would prevent subsequently released teeth from erupting, observations show that the capacity for
eruptive movement remains active during
4-7 weeks delay.
The rate (Oj, fig. 1D) during the first
week after release was the maximal rate
of eruption, a full expression of the potential rate. It was achieved because the
pathway for eruption was already formed,
because the teeth had room to reorient
regardless of slight misdignment and be-
cause the development or maturation of
the eruption system had proceeded during
the delay thereby eliminating the slow
exponential phase seen in normal eruption. The continued maximal eruption
rate of two of the seven released specimens is further evidence of this finding.
The weekly radiographs showed that the
eruptive pathways of these two had
formed sufficiently and that they were
not misoriented in the pathway.
The morphology of the bony trabeculae
beneath the erupting teeth and the relative
amount of soft tissue between the bone
and teeth are expressions of the eruptive
rate. The trabeculae around rapidly erupting teeth are thinner, more delicate and
more widely separated from one another
than those of more slowly erupting teeth.
They also, in radiating upward, accurately
reflect the directional movement of the
teeth. This finding agrees with those of
Meyer ('35) and Massler and Schour
('41); but apparently the orientation of
the trabecular pattern varies in different
species since Weinmann ('41) reports
trabeculae in man are at right angles to
the long axis of the teeth.
Prefunctional tooth eruption is a normal growth process wherein physical
factors involving mass, acceleration and
inertia probably play no effective role. In
the present investigation teeth were studied
as they emerged from the bony crypt and
moved through the eruption pathway to
pierce the gingiva and finally reach the
occlusal plane. The eruption process can
be considered as a balance between osteoclastic activity above the tooth (with directional reference to the mandible) and
principally osteoblastic activity below the
tooth. Both of these factors implicate incompletely understood functions of the
dental follicle. The eruption pathway forms
by osteoclastic activity along the sides of
the follicle above the tooth (in the part
that connects to the oral mucosa) and by
osteoblastic activity at the base of the
follicle. The follicle appears to act as a
reservoir to provide the necessary osteoblasts and osteoclasts for the bony changes
that occur in eruption. Because of this
profound bone remodeling, it appears that
origin and differentiation of osteoclasts
EXPERIMENTAL STUDY OF TOOTH ERUPTION
can be studied by experimentally controlling eruption.
If the follicle plays a primary role in
eruption (OBrien et al., '58; Cahill, '69)
it would be important to know factors
regulating its performance i.e., temporal
scheduling of its activity. Questions of
this nature may be answered by experimentation. Transplantation of the follicle,
of its contents or both into various sites
at different developmental stages is presently being carried out in the puppy.
ACKNOWLEXMENTS
Again it is a pleasure to express rny
appreciation to Dr. Carson D. Schneck for
his guidance throughout the study. I would
also like to acknowledge Dr. Alan D.
Conger for the valuable discussions concerning the eruption rates and the work
of Mr. Dewey Blackstone for the radiologic assistance is greatly appreciated.
229
LITERATURE CITED
Cahill, D. R. 1969 Eruption pathway formation
in the presence of experimental tooth impaction in puppies. Anat. Rec., 164: 67-78.
Kenney, E. B., and S. P. Ramfjord 1969 Cellular dynamics in root formation of teeth in
rhesus monkeys. J. Dent. Res., 48: 114-119.
Massler, M., and I. Schour 1941 Studies in
tooth development: Theories of eruption. Amer.
J. Orthodont., Oral Surg., 27: 552-576.
Meyer, W. 1935 Meyer's Normal Histology and
Histogenesis of the Human Teeth and Associated Parts. Translated and edited by H. R.
Churchill, J. B. Lippincott Co., Philadelphia,
London and Montreal. Chap. 14, pp. 237-248.
O'Brien, C., S. N. Bhaskar and A. G. Brodie 1958
Eruptive mechanism and movement in the first
molar of the rat. J. Dent. Res., 37: 467-484.
Orban, B. J. 1966 Orban's Oral Histology and
Embryology. H., Sicher, ed. C. V. Mosby Co.,
St. Louis, 6th ed.
Provenza, D. V. 1964 Oral Histology, Inheritance and Development. J. B. Lippincott Co.,
Philadelphia and Montreal.
Weinmann, J. P. 1941 Bone changes related
to eruption of the teeth. Angle Orthodont., 11:
83-99.
PLATE 1
EXPLANATION OF FIGURE
1
Four graphs of the impaction-release eruption rates o n semilog paper.
A and B, show the individual curves i n mm (from the base of the
mandible to the top of the crown) against weekly age. The impaction
durations are identifiable as the flat parts of the curves. C, shows
the curves normalized, where time of release equals zero and impaction height equals 1.0, ( C , is equivalent to rapid exponential portion
of the normal rate). D, shows the findings in simplified form where
ej is the maximal rate, Or is a rapid but slightly diminished rate and
8 c is a rate nearly identical to the rapid part of the normal rate.
EXPERIMENTAL STUDY OF TOOTH ERUPTION
Donald R. Cahill
PLATE 1
2(
10
€
E_ 1(
5:e 11
U
i
L
1:
E
n
, ' " "
a
16
ia
PI G E , weeks
k
-
C.
-
!.O
1.5
1.0
D.
-
1.0
-2
-'I
0
*l + 2
+3
*4
+5
Time from release, weeks
ERUPTION RATES AFTER RELEASE FROM IMPACTION
231
PLATE 2
EXPLANATION OF FIGURE
2
232
Three graphs showing the normal eruptive rate of the third permanent
mandibular premolar on semilog paper. A and B, show individual
curves plotted as height in mm (measured from the base of the
mandible to the top of the crown) against weekly age. C , shows the
average eruption rate curve (solid line) and the range (dotted lines).
The average is triphasic with a n initial period of slow exponential
growth, a middle rapid rate and a terminal plateau. This curve was
computed by superimposing the individual curves of A and B at 20
weeks and by designating 1.0 for height at 13 weeks.
EXPERIMENTAL STUDY OF TOOTH ERUPTION
Donald R. Cahill
PLATE 2
233
PLATE 3
EXPLANATION O F FIGURES
3
Anteroposterior section showing the third permanent premolar (3p)
one week after release from three-week impaction. ( a ) apex of old
bone before release;" shown at higher magnification in figure 7. x
5.0.
4
Anteroposterior section through the third permanent premolar one
week after release from a five-week impaction. Notice the trabecular
pattern ( T ) radiating toward the tooth from the old bone. Its radiograph is seen in figure 5. x 5.0.
5
Dental radiograph: The space between the arrows demonstrates the
distance moved ( a t the maximal eruption rate) in one week after releasing the impaction. Same specimen as in figure 4. x 2.3.
6
Radiographs from the frontal aspect of dissected mandibles showing
the control side ( A ) and its atypical experimental side (B). The
eruption pathway (arrow) failed to enlarge i n the usual manner and
also, cross-sectional shape of the mandible became distorted. x 2.0.
7 The area marked ( * ) in figure 3, ( e d ) epithelial diaphragm. Ossification centers are seen within clusters of osteoblasts ( T ) .
234
x
26.
EXPERIMENTAL STUDY OF TOOTH ERUPTION
Donald R. Cahill
PLATE 3
235
PLATE 4
EXPLANATION OF FIGURES
8
Anteroposterior section of a rapidly erupting tooth three weeks after
release; its radiograph is seen in figure 1OC. Notice the stringy, thin
bony trabeculae that rzdiate toward the tooth. They are characteristic
of rapid eruption and are comparatively more delicate than the trabeculae of the more slowly erupting control (fig. 9). X 5.0.
9
Anteroposterior section through the fully erupted control side of
figure 8. x 5.0.
10 Dental radiographs: A, shows the impacted tooth surrounded by its
restraining wires. This film, made six weeks after wire placement,
shows the eruption pathway (arrow) as a radiolucent area. B, same
specimen one week after wire removal where comparison of crown
position with the preceding film shows the amount of eruptive movement during the first week after release. C, shows the same tooth
three weeks after release (histologic section of this tooth is shown
i n figure 8). D, control side taken at the same time as B. Actual size.
11
236
Anteroposterior section of a slowly erupting release specimen of group
111. As a result of the impaction, the tooth became misdirected into
overlying bone (arrows) rather than directly into its eruption pathway.
x 5.0.
EXPERIMENTAL STUDY OF TOOTH ERUPTION
Donald R. Cahill
PLATE 4
237
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