Australian Dental Journal, August, 1 9 7 1 227

Pulpal changes following the reimplantation of teeth

in dogs: A histological study*
F. N. T. Monrour, M.D.&.

Introduction studies have been p e r f o r m e d on man

Although the literature available on the re-
implantation of vital teeth is not voluminous,
the procedure has attracted extensive interest
in recent years. There are several recent
reports of experimental investigations of the
healing processes in cases of reimplantation
after t he complete luxation of teeth. These
Financial support for this project was recelved
from the Australian Universtties Commission Post-
graduate Training Grant.
Recelved for publication August, 1970.
(I) Emmertsen, E.-Replantation of extracted
molars. Oral Surg..
- . 9: 1. 115-122 (Jan.),
1956.
(2) Henning F R.-Reimplantation of luxated teeth.
Austril. D. J., 10: 4, 306-312 (Aug.). 1966.
(9 Plndbora. J. J.. and Hansen, J.-A case of re-
plantation of .an upper lateral lnclsor : a histo-
logical study. Oral Surg., 4: 5, 661-667 (May),
1981
(Emmertsen,") Henning,-) Pindborg and
Hamen,(*) Love1 and Hopper,(') Andreasen and
H j ~ r t i n g - H a n s e n , ~ ~Ohman,'")
) and on various
animals such a s m o n k e y s (Loe and
Waerhaug:" Shulman, Kalis and Goldhaber,(@)),
dogs (Knight,(1o) Loe and Waerhaug,(*' Roths-
child and Goodman,'") Mink and Van Schaik,")
Anderson, Sharav and Massler(l*'), and ham-
sters (Myers and Flanagan,(l') Sorg("). How-
ever, the literature on tooth reimplantation
is dominated by clinical reports of treated
cases.
It is in those cases where the pulpal,
cemental, and periodontal tissues remain
viable, that the procedure is referred to as
vital reimplantation. However, the main
interest in the past was shown in the mechan-
ism by which the tooth is anchored to the jaw,
while the pulp of the reimplanted tooth
received little attention.
The vital reimplantation of teeth is per-
formed mainly for two reasons:
1. The treatment of traumatic accidental
dislocation of teeth.
2. The surgical repositioning of developing
or unerupted teeth.
The importance of the retention of vital
characteristics in the preservation of tooth
integrity and appearance as well as continued
growth and hence the long-term prognosis, is
well established. This study was designed to
investigate the essential biological phenomena
associated with the reimplantation of vital
anterior teeth in dogs.

Materials and methods

M7kE.J. R.. and Van Schaik, M. V.-Intentional The experiments were performed on eight
avulsion and replantatlon of dog teeth with
varied root surface treatment. Int. Ass. Dent.dogs from the same litter. The dog was chosen
Res., Abstr. 43 1968. because the dental apparatus and supporting
(18) Anderson, A. W.,Sharav,
' Y.,and Massler, M.-
Periodontal reattachment after tooth re- tissues have a similar pattern of growth and
p!antation. Periodontics 6 : 161-167 (Aug.),
1868. repair to human tissues, and the teeth were
0
') Myers, H. I., and Flanagan, V.-Long-range of a desirable size and shape to facilitate their
post-operative evaluation of transplanted ham-
ster second molars. J. oral Surg., 17: 4, 22-29 extraction, reimplantation and splinting.
(July). 1959.
(m Sorg, W. R.-Nerve regeneration in replanted The teeth selected for reimplantation were
hamster teeth. J. Dent. Res., 39: 6, 1222-1231
(Nov.), 1960. the single rooted maxillary incisors, since these
220
Fig. 1.-Maxillary anterior teeth of a n experi-
mental animal immediately prior to reim-
plantation, showing t h e tooth form and t h e
selected s t a g e of development.
Fig. 3.-Recovery of t h e pulp 14 d a y s
a f t e r immediate reimplantation. Note
the intact line of odontoblasts and a
narrow hand of tubular dentine (D)
formed beyond t h e calcio-traumatic
line (CTL). H and E ( x 100).
teeth presented less difficulty with t h e pro-
cedure under trial conditions. The degree of
primary tissue damage on removal of a tooth
for reimplantation i s of the utmost importance
in influencing t h e success of this procedure.
The time selected for reimplantation was
when the maxillary incisor roots had reached
approximately two-thirds their completed for-
mation (Fig. 1).
This ensured that: ( i ) t h e teeth possessed
open apices but with adequate root length for
Australian Dental Journal, August, I97 I
Fig. 2.-Wrought stainless steel s lint
ligated in position on the m a x i z a r y
anterior teeth.
Fig. 4.-The growth of granulation
tissue into the pulp chamber a n d pro-
gressive replacement of t h e dead pulp
7 d a y s a f t e r reimplantation. Note t h e
proliferative zone ( P ) , t h e exudative
zone (E) a n d the dead pulp ( D P ) .
H a n d E ( x 40).
support, and ( i i ) the active development of the
teeth retained t h e presence of immature tissues
capable of more rapid differentiation and
repair.
Following the successful removal of the
selected experimental teeth, the reimplantation
procedure took one of two forms: ( i ) imme-
diate reimplantation, and ( i i ) delayed reim-
plantation.
I n the delayed reimplantation t h e extracted
teeth were placed in sterile normal isotonic
Australian Dental Journal, August, I97 I
Fig. B.-Almost complete elimination
of the dead pulp by the replacement
tissues 28 days after reimplantation.
H and E ( x 1 0 ) .
saline and left for three minutes. This period
was in excess of the bleeding time for the
animal (bleeding time: 1-1& minutes in dogs).
After this period a clot had formed within the
extraction socket necessitating some prepara-
tion by mild curettage of the site before
reimplantation.
The teeth were flrmly replaced into their
sockets and a wrought wire splint was adapted
into position and wired to the arch (Fig. 2 ) .
The splints were retained in a stable position
for 14 days a t which time they were removed.
This time interval was selected a s being ade-
quate to the requirements of partial immobiliz-
ation of the reimplanted teeth, and the creation
of effective reparative reattachment. (The dog
has a rate of repair equal to two and a half
times that of human tissues.)
A radiographic examination was carried out
every 7 days and the material was recovered
for histological examination a t 7, 14, 28, 60, 84,
120, 154 and 190 days post-operative.
Result8
I n two of the immediately reimplanted teeth
recovery of the pulp was seen following the
early degenerative change. These teeth showed
continued formation of tubular dentine with
healthy odontoblasts, and retained the normal
histological character of the pulp (Fig. 3).
Although there were two cases of identified
recovery of the pulp following reimplantation,
generally the pulpal behaviour followed a pat-
tern of slow degeneration and replacement by
the ingrowth of tissues through the wide apical
229
Bic. &--The differentiation ol osteoblast-like
~~ ~~ ~
Ceik ( 0 )-from--theCrepiacement pulp tissues
~ ~
with the formation of osteo-dentine ( O D ) on
the tubular dentine ( D ) after 28 day'E. H and
E ( x 100).
canal (Fig. 4 ) . Where no disturbance such as
deep cervical resorption and fracture inter-
rupted their progress, the replacement tissues
advanced to eliminate all the dead tissues and
completely fill the pulp chamber (Fig. 5).
With the continued advance of the replace-
ment tissues, the more distal areas showed
maturation of the stroma and the differentia-
tion of more specialized cells. Cells resembling
osteoblasts were situated peripherally in the
pulp, and were responsible for the deposition of
a n osteo-dentine on the walls of the pulp
chamber (Fig. 6 ) . This led to the progressive
obliteration of the pulp chamber which in
some cases was observed to be complete. Where
the process was not complete there remained
relatively inactive mature fibrous pulpal
tissues. I n some instances where intra-pulpal
ossification was evident or with the ingrowth
of supporting bone through the apex, there was
seen an intrapulpal ligamental attachment with
the osteo-dentine (Fig. 7 ) .
The osteo-dentine strongly resembled bone in
its formation and morphology. There was a
distinct lamellar pattern and haversion canal
system (Fig. 8 ) . The extensive formation of
osteo-dentine was also partially responsible for
the extension of growth of the root following
the disintegration of the disrupted Hertwig's
root sheath. This w a s associated with the
extensive formation of cellular cementum
about the apical canal.
The regenera.tion of elements of nerve tissue
was seen in the later observation periods, how-
ever, its presence was restricted to the apical
third of the pulp.
230
Fig. 7.-A reimplanted tooth after 1 5 4 days.
Ingrowth of bone ( B ) with an intrapulpal liga-
mental attachment ( I L ) to the deposit of osteo-
dentine (OD) on the tubular dentine wall (D).
Mallory's stain ( x 4 0 ) .
While the pulpal changes took place there
were observed varying changes in t h e clinical
appearance of t h e crown of the reimplanted
tooth. During the extended observation period
t w o of the reimplanted teeth showed no dis-
cernible colour change, while the remaining
reimplanted teeth exhibited changes varying
from minimal to very marked darkening of
the crown. These features could not he related
to observed recovery of the pulp.
Discussion
The course of healing of the pulpal tissues
was clearly influenced by the extent and
character of the primary pulpal damage. I t is
impossible to determine from this investiga-
tion which factors, apart from t h e degree of
root development and difficulties with extrac-
tion, were responsible for variations in the
extent of primary pulpal damage. I t seems
likely t h a t in reimplanted teeth with minimal
primary pulpal injury, t h e circulation had
recommenced within a short time following
trauma with subsequent recovery. Some tissues
have a n inherent capability to survive for a
time independent of their nutritional supply
and Nordenram,(la) explains that during the
first critical period when revascularization h a s
not occurred, usually three to five days after
reimplantation, nourishment is probably sup-
plied to the implant by diffusion of tissue fluids
from t h e surrounding tissues. I t i s important,
therefore, t h a t there exist no barriers t o t h i s
diffusion otherwise degeneration of the pulp
will result.
I n the delayed reimplantations the extended
exposure of the teeth, together with the neces-
Australian Dental Journal, August, 19 7 1
Fig. %--The lamellar pattern of the
osteo-dentine ( O D ) on the tubular
dentine wall ( D ) 1 5 4 days post-opera-
tive. Mallory's stain ( X 100).
sary curettage of organizing elements from t h e
sockets, may have contributed to the extent
of pulpa.1 damage and influenced t h e type of
repair. I t i s also realized that satisfactory
knowledge will be acquired only when more
extensive variation i n the procedure is utilized.
However, it i s signiflcant t h a t identified
recovery of the original pulpal tissues occurred
only in teeth which were immediately reim-
planted, whereas i n t h e delayed and remaining
immediaie reimplantations t h e pattern of
repair was vital replacement with subsequent
partial or complete ossification. It seems essen-
tial that the degeneration of t h e original pulp
must be slow to allow replacement to occur
rather than severe reaction and abscess for-
mation.
There has been much speculation on t h e cells
responsible for the deposition of osteo-dentine.
The formation of osteo-dentine was described
by Ohman,") Sorg,c'J) Tomlin,(") and Lenstrup
and Skieller,(18) all of whom have shown t h a t
t h e pulp chamber becomes progressively fllled
by mineralized tissue identified t o be osseous
i n nature. No conclusive evidence is reported
as to whether this mineralized tissue i s a pro-
duct of redifferentiated odontoblasts o r other
cells of the pulp. Fleming,(1e' and Agnew and
Fang,'") indicated that, where present, t h e
osteo-dentine appeared to be deposited upon a
layer of reparative dentine, indicating activity
by t h e odontoblasts. Ohman,(?) SOig'lK' and
Fang(=) suggested t h a t the formation of normal
tubular dentine a t t h e dentinal-pulpal junction
Australian Dental Journal, August, I97 I
does not continue after the formation of osteo-
dentine until there i s regeneration of the
odontoblastic layer, thus favouring the theory
of redifferentiation of the odontoblasts.
I n this investigation i t was clearly seen that,
following traumatic interruption of the odonto-
blastic activity by extraction and reimplanta-
tion, these cells, prior to degeneration, continue
to form a deposit of tubular or reparative den-
tine. There was then oessation of deposition of
any mineralized tissues upon death of the
original pulp. I t was not until the coronal
advance of the replacement tissues from the
apex, with progressive maturation and the dif-
ferentiation of osteoblast-like cells, that any
further deposit waa observed. These productive
cells were differentiated from the flbrous
replacement tissues and probably from the
primative fibroblasts in this tissue, and were
responsible for the deposition of osteo-dentine.
In the cases where a n odontoblast-like layer
of cells was identified a t 14 and 84 days after
reimplantation, this was situated on a wall of
tubular dentine with no osteo-dentine present,
suggesting recovery rather than redifferentia
tion of these cells.
The atypical extension of the growth of the
root by the extensive deposition of cellular
cementum about the apex, was observed soon
after t h e disintegration of the disrupted
Hertwig's root sheath. There must exist some
initiating forces requiring the continued
growth of the root irrespective of the presence
of an intact Hertwig's root sheath. These forces
may be associa,ted with continued eruption of
the teeth, or possibly the inbuilt potential of
the developing tisues of the periodontium. A
combination of these factors probably operated
and was influenced by the functional require-
ments of the reimplanted teeth.
Although regeneration of neural elements
was observed in the pulpal replacement tissues
late in the observation period, no significant
evidence waa found as t o their influence on
the pattern of recovery or repair. It is most
elm Nordenram. A.-Auto transplantation of teeth. pulpal tissues was a possibility and where it
A clinical and experimental investigation. Acta.
Odont. Scand., 21, 13-76, suppl., 33, 1-138 1963. did not occur the pulpal tissues underweiit
(17) Tnmlin. A. J.-ReimDlantation of four imuacted
.. -->port of a case. Oral-Surg., degeneration, and were replaced by tissues
March) 1966.
Skielle;, V.-Follow-up study which underwent differentiation and osteoid
of teeth redanted after accidental loss. Acta
Odont.--Scaid.. 17 : 503-509 (Dec.), 1959.
Fleming H. S.-The osteogenic tendency of
dentin; after formation in tooth germ trans-
plants. Oral Surg., 6 : 1315-1324 (Nov.). 1953.
Amew. R. G.. and Fonz. C. C.-Histoloeic
s'tuhies in experimental-' transplantation -of
teeth. Oral Surg., 9 : 1, 18-39 (Jan-), 1956.
(a)Fona C.-Histoloaic studies of aUtOtranSDlanted
teeih. Int. Ass. Dent. Res. Abstr. 41: 112, 1963.
23 1
likely that the proliferating neural elements
from the periapical area followed the course of
the arterioles seen in the apical region of the
Pulp.
I n a morphological study of this kind definite
limitations were experienced. It was possible
to observe the biological behaviour in terms
of: type of reaction, time of onset, duration,
and the final result. I t was, however, impos-
sible to determine why this occurred and what
initiating forces were present. This study has
highlighted the desirability to parallel such
an investigation with the use of specific pro-
cedures, such as histochemical analysis, in
describing the biological processes involved in
the vital reimpla.ntation of teeth.
Concluslon
I t is readily recognized in this preliminary
investigation that successful vital reimplanta-
tion is a possibility. Also, there is no doubt
that in most successful cases of reimplantation
of extracted teeth, complete mineralization of
the pulp chamber will eventually occur. It is
possible, however, that while the tooth will
lose its pulp, i t retains much of the vital
character and acceptance which must be lost in
root-filled reimplanted teeth.
No rationale for the successful clinical
management of teeth for reimplantation can
be suggested due to the many variants involved
such as the stage of development, the extra-oral
period, primary trauma, and contamination.
However, the results of this study would
indicate that, owing to the considerable
recovery potential of the pulp in cases of mini-
mal trauma, there is the distinct possibility of
successful surgical reimplantation and re-
positioning of teeth.
Summary
The reimplantation of teeth with the reten-
tion of vital characteristics was performed in
the incisor teeth in dogs.
The procedure was varied only in respect of
the time teeth were out of the socket.
It was observed that revitalization of the
material was deposited on the walls of the pulp
chamber leading to its complete or partial
obliteration.
Dental College,
University of Queensland.
Brisbane, 4000.