Tooth avulsion and replantation - A review

Hammarstrom L, Pierce A, Blomlof L, Feiglin B, Lindskog S.

Tooth avulsion and replantation - A review. Endod Dent Traumatol 1986; 2: 1-8.
Abstract - The major causes of post-replantation tooth loss are
inflammatory root resorption and root resorption associated
with ankylosis. Recent studies have concentrated on delineating
the cellular interactions in the pulp and periodontium in order to
more fully understand the various factors affecting the prognoses
of such teeth. The aim of this report is to discuss the nature of the
pathology responsible for tooth loss following avulsion and to
review recent replantation and attachment studies.
LIBRARY
b^H-.JL

Or

U.JIIAL

Lars Hammarstrom, Angela Pierce, Leif

Blomiof, Barry Faigiin^ and Sven Lindskog
Department of Oral Pathology, School of Dentistry,
Karolinska Insfitutet, 'Department of Periodontoiogy, Skanstull Public Dental Health, Stockholm, Sweden, 'Department of Restorative Dentistry, Faculty
of Dental Science, The University of Melbourne,
Melbourne, Australia

Key words: ankylosis, replantation, review, root

resorption, tooth avulsion.
Professor L. Hammarstrom, Dept. ot Oral Pathology, School ot Dentistry, Karolinska Institutet, Box
4064, S-141 04 Huddlnge, Sweden.
Accepted for publication 11 July 1985.

A variety of treatment procedures have been advocated in the past for the management of avulsed or
exarticulated teeth (1). The majority of these were
directed at the prevention of root resorption associated witli inflammation or ankylosis, the major
causes of tooth loss following replantation. However,
many treatment methods have been unsuccessful,
and tooth loss following replantation is a disconcerting but not uncommon clinical observation. It is
apparent that a basic understanding of the cellular
interactions occurring at the root surface and within
the periodontal membrane is essential to the successful management of the avulsed tooth. The following
discussion aims to examine these interactions in the
context of recent replantation and attachment
studies.
The normal periodontium

The dental root is separated from the alveolar bone

by a thin layer of connective tissue, the periodontal
membrane. Not only does this tissue form an attachment between the root and bone, but it also serves
to maintain the integrity of the root. Furthermore,
it is unique in nature, containing a web of epithelial
cells (the epithelial rests of Malassez) which are
surrounded by connective tissue. Absence of this
periodontal membrane zone results in ankylosis, a
union between tooth and bone (2,3).
Collagen fibers form a major part of the cementum and are responsible for its attachment to the
periodontal membrane. Recently, attention has

been focused upon the complex nature of the outermost layers of the root: the granular layer of Tomes,
the intermediate cementum and, closest to the periodontal membrane, the dental cementum. It has
been suggested that the intermediate cementum,
forming an effective barrier between the dentin and
the periodontal membrane, is critical to the progress
of root resorption (4,5). Furthermore, it can not be
regenerated once it has been damaged. An appreciation of the development and function of these layers is essential to the understanding of periodontal
repair.
Root resorption associated with inflammation or ankylosis:
The major causes of tooth loss following replantation

Under normal circumstances, invasion of the periodontal membrane by bone, and dentoalveolar
ankylosis (union between tooth and bone) are not
observed. However, these tissues are not static. The
bone socket surface is continuously remodelled in
response to functional demands, and cementum,
although not normally resorbed, grows slowly but
continuously throughout life.
In contrast, pathological resorption of the dental
root is often found on the external surface of replanted teetli in association with trauma and infection or with dentoalveolar ankylosis. In the past,
root resorption has been subdivided into static and
separate entities which, labelled accordingly, inferred a difference in the basic resorptive mechanisms. This has become somewhat misleading and
1

Hammarstrom et al.
the following discussion attempts to focus on resorption as a dynamic and unified process.
Root resorption, although an e.ssentially pathological process, apparently differs little from its osseous homcostatic counterpart. There are, however,
some notable differences between the cells responsible for resorption of the different tissues (6). Although both are of hematogenous origin, dentinresorbing cells (Fig. 1) are usually smaller and contain fewer nuclei than osteoclasts (7). Furthermore,
the well-developed clear zones evident in activelyresorbing osteoclasts contrast with those observed in
dentin-resorbing cells, which are either very small
or non-existent (6,8). It has been suggested that
the appearance of resorbing eells is affected by the
nature of the tissue being resorbed and that the cells
should be designated accordingly, as in the terms
dentinoclast and osteoclast (6).
During the actual avulsion and replantation procedures, small areas of mechanical damage to the
cementum surface are sustained, and these result
in the shallow resorption lacunae observed after
replantation and termed surlace resorption
(9,10). Under ideal conditions (that is, where the
vitality ol the periodontal membrane has not been
compromised, and the pulp or dentin is not contaminated by bacteria), rapid periodontal healing
and root surface repair occur. Apposition of reparative cementum within these resorption lacunae is
usually completed within 14 days (11).
The status of the dental pulp is critical to the
root resorption process. The pul|3 invariably loses its
vascular supply following avulsion and, except in
the case of an immature tooth with an open apex,
revascularization rarely occurs (12,13). Necrosis
generally proceeds and the pulp is often infected as
a result of contact with saliva or extra-oral debris
(1,12). Nevertheless, as long as the eementum covering the root surface remains intaet, the bacteria and
products of pulp tissue degradation remain reasonably confined to the root canal. Once the cementum
and intermediate cementum are penetrated by the
surface resorption referred to earlier, the dentinal
tubules provide a pathway for the passage of bacteria and their toxic products from the pulp
chamber to the root surface. An inflammatory response is subsequently evoked within the periodontal membrane, and root substance and bone are
destroyed. This proce.ss is accelerated in the younger
patient in whom the dentinal tubules, often sealed
with the progress of years, are still patent (1,14).
This sequence of events has been termed inflammatory root resorption (15,16) and, if not resolved,
can cause rapid destruction of the dental root. If,
however, the inflammation subsides, ankylosis often
results from the fusion of ingrowing bone to dentin
exposed by the resorption process.

Replantatioti ofa tooth with a necrotic periodontal

membrane, in the absence of infection, results in an
ankylotic fusion between bone and the cementum
surface or shallow resorption lacunae (17). This may
differ from, or at least be a delayed form of the replacement resorption described by Andreasen
(4,18,19), in which ankylosis is subsequent to inflammatory resorption. The status of the periodontal
membrane is thus critical to the initiation of ankylosis
(1,2,18,20,21,22) and this raises the question of how
the progression of ankylosis is influenced by such factors as a necrotic periodontal membrane, or the state
of the dental cementum. No such long-term experimental studies have been reported. However, our
preliminary data indicate that the root resorption
which follows an ankylotic fusion between the dental
root and the alveolar bone progresses more slowly if
the cementum layer is intact. It may thus prove more
favorable to chemically remove a necrotic and often
infected periodontal membrane prior to replantation
(e.g. when an avulsed tooth has been stored for too
long in an unsuitable medium) (21).
Recently, experimental studies on formation of
reattachment and new att;ichment iti jjeriodontallycompromiscd teeth have demonstrated the potential
of periodontal membrane cells to proliferate apically
into a denuded area of the root, provided the alveolar bone and pocket epithelium are prevented
from simultaneous invasion (23,24,25). This concept of a competition between the various tissue
elements was also investigated by Andreasen (26)
who found that periodontal cells proliferated apically from the crevicular gingival tissues when the
root surface had been denuded of vital periodontal
ligament prior to replantation. It was proposed that
a competitive situation existed between the downgrowth of new periodontal membrane from the cervical region, and the ingrowth of the alveolar bone
across the periodontal spaCe. Andreasen postulated
that if alveolar bone growth across the periodontal
space, and thereby ankylosis, could be prevented, a
new periodontal ligament could form as a result of
continued downgrowth from the crevicular site.
In conclusion, ankylosis "esults after replantation
of all teeth with necrotic periodontal membranes.
Furthermore, if the periodontal membrane is vital
at the time of replantation, but pulpally-derived
inflammatory resorption ensues, ankylosis will result
after endodontic treatment when the inflammation
subsides. Hence the importance of the status of both
the periodontium and the pulp is emphasized.
Experimental studies: Factors intiuencing the prognosis of
the replanted tooth
The use of a histomorphometric evaluation technique, pioneered by Andreasen (9,10), has facili-

Tooth replantation

Fig. 1. A dcnliiioclasl ( O ) in a shallow resorption l a c u n a from a m o n k e y tooth in a s i a i i n i n y electron niurosKiijii p i e p a r a l i o n . T h e

d e n t i n o e l a s i ha.s a rulTled b o r d c i ' ( a r r o w ) loward.s llic d e n l i n a l suiface. T l i e r e is very litlie e v i d e n c e fbi llie existence o('elear /.ones
o r a n y struc tures sealing ofl' the rallied b o r d e r .

tated experimental studies of tooth replantation and

its sequelae. The basic principles of this technique
are illustrated in Figs. 2 and 3. Examination of
periodontal membrane repair and reattachment is
common to all of these studies, each one of which
emphasizes a different variable capable of altering
the prognosis of the re]3lanted tooth (Fig. 4).
Mechanical damage during exarticulation and replantation

In the processes of avulsion and rcjjlantation, tissues

are torn and cells are damaged. These areas of
damage api^ear as surface resorption defects which.

if uncomplicated by other factors, heal relatively

quickly. It has been demonstrated that damage to
the root surface is maximal on those surfaces where
physical contact occurs with the bone socket during
rotatory movement, i.e. the convex buccal and lingual surfaces of the root. 1 he proximal concave
surfaces are least damaged during the exarticulation
- replantation sequence (10). 'fhus, it is not surprising that resorption sites, after experimental extraction and replantation, arc most commonly observed
on the convex surfaces of the root and, less commonly, on the proximal surfaces which are ustially
concave and thereby protected from damage.

Hammarstrom et al.

Fig. 2. The histomorphometric evaluation technique. A predetermined number of radii were superimposed over each section
taken from a step-serial sectioned tooth. At the intersections of
the radii and the root surlaee (at 8 points shown in this Figure)
the appearance of the periodontium was elassified according
to defmed criteria (normal periodontium, surface resorption,
inflammatory resorption, ete). The percentage area of root surface showing a defined criterion was caleulated by dividing the
product of the number of observation points showing the defmed
criterion X 100, by the total number of observation points.

Storage of the tooth prior to replantation

Although it is most desirable to replant the exarticulated tooth as quickly as possible, this may not
always be feasible. In these situations, it is essential
to ensure maximal viability of the periodontal metnbrane attached to the root surface. Accordingly, the
tooth must be prevented from drying, and it is
important that its storage medium is of the correct
osmolality and pH (27,28). It has been shown that
after 60 min of dry storage very few periodontal
cells retain their vitality (22,29). Such a situation
guarantees the onset of extensive pulpally-derived
inflammatory resorption or of ankylosis and subsequent replacement root resorption of endodontically treated teeth (1,19,22). Storage in tap water
is equally as damaging as dry storage, the hypotonic
eonditions resulting in rapid cell lysis (27). Experimentally available media, such as physiological culture media, preserve cell viability well, but these are
rarely available at the site of accident (27,28,30).
Saliva allows storage of teeth for about 2 h (31).
However, its hypotonicity augers poorly for cell survival and, furthermore, the compromised cells demonstrate a lowered resistance lo the bacteria normally found in saliva (22,27,28,32). Recent studies
have established that milk is an excellent storage
medium, and teeth stored for up to 6 h demonstrate
the same low index of resorption as teeth replanted
immediately following avulsion (30,31), The pH

and osmolality of milk, being 6.5-6.8 and 230-270

mOsm/kg respectively, are compatible with longterm cell survival (28,30,33). Furthermore, pasteurized milk contains few virulent baeteria (22,27).
Milk products such as sour milk and yoghurt provide poor conditions for cell survival because of their
low pH (27).
Cell survival can also be encouraged by preventing osmotic damage caused by evaporation. Recent
experiments have demonstrated that teeth wrapped
in plastic foil for 1 h have a similary low rate of
resorption as those replanted immediately following
avulsion (34).
The temperature of the storage medium appears
to have little influence on"periodontal healing and
vitality of the cells of the periodontal metnbrane, as
long as it is kept below 37C (27). Accordingly, milk
taken directly from the refrigerator may be used as
a storage medium.
The use of chemical agents to prevent root-resorption

While it is apparetit from the foregoing that cell

survival is essential for prevention of the resorptioti
process, what can be done if cell damage has already
intervened? Many different chemical agents have
been used in order to produce a root surface that is
resistant to resorptioti (1). Treatment with acids,
formaliti atid calcium hydroxide has been utisuccessful, but the use ofa fluoride solutioti has been reported to slow down the resorption process (35-38).
Recent studies have investigated the possibility of
rendering the root surface unreactive by decalcification followed by enzymatic deletion of glycoproteins, and cross-linkage of cementum collagen
using glutaraldehyde. Initial results hold some
promise for the prevention of resorption (39).
Treatment of the socket

In the past, there was a tetideticy to attribute an

influence of the socket to the onset and progress of
replacement resorption. However, results of later
experiments, in which newly avulsed teeth were
replanted into previously prepared sockets, indicated that the main factor determining the onset of
replacement resorption was the state of the periodontal membrane. Curettage of the socket wall
and presence or removal of a blood elot had little
itifluence on the healing pattem of the replanted
tooth (1).
Splinting of the replanted tooth

The role of rigid and semi-rigid fixation in the treatment of the replanted tooth has been investigated
and it was concluded that minimal splinting permits

Tooth replantation

T^z'fj. J?. Schematic drawing and photomicrc^graphs illustrating the most common periodontal re])air patterns observed during re|)lantation studies.

Hammarstrom et al.
I M M I D I A l I Kl PI \ N 1 ,\1 K ) \ '

Ih

42%

86%

MILK (ih

SAtlVA

21%

79%

Fig. 4. Periodontal healing patterns after variotis extraoral treatments of an avulsed tooth. The drawings summarize results (Voni a
number of studies (17,21,27,30,31,34,41). I'-ndo indicates that the teeth were treated endodontically with gutta percha root fillings
extraorally. The periodontal ccjnditions were evaluated after a healing period of 8 weeks. The figures indicate the relative area (in
%) of the root stnlace showing the tiiost common periodontal re])air patterns indicated in Fig. 3.

Tooth replantation

physiological jiggling movements of the tootli

which result in a low incidence of ankylosis (1,9,40).
Rigid fixation produced a high degree of bony outgrowth across the periodontal space, ankylosis to
the root, and replacetnent resorption (1,9).
Effect of mastication on periodontal repair

Masticatory stimulation has been shown to have a

positive eflect in reducitig the extent of ankylosis
(41). Monkey teeth were extracted, air dried for 1
h, endodontically treated atid replanted, and the
anitnals were subsequently placed on either a hard
or a soft diet. The hard diet resulted in significandy
less ankylosis and a higher incidence of normal periodontal ligametit compared with the soft diet.
Endodontic treatment

It has been established that bacteria and breakdown

products from infected pulp tissue can readily penetrate the dentinal tubules. In the absence o( the
intermediate cementum layer, these products produce inflammatory changes within the periodontal
membrane leading to inflatnmatory root resorptton
(4,5). Rapid and efficient management of the necrotic pulp is necessary to prevent the onset of inflammatory root resorption, and debridetnent of the
root-canal within a period of 14 d following replantation has been recomtnended (1).
As the primary goal of therapy is to tninimize
periodontal damage, endodontic treatment should
not be carried out on the tooth prior to replantation,
as the excessive handlitig risks additional damage to
the membrane (1,4). Similarly, it has been suggested
that agents such as calciutn hydroxide or root canal
sealers should not be placed within the root canal
initially as these have a cytotoxic eflbct which tnay
add to the datnage already sustained by the periodontal tnetnbrane (4,42).

Conclusions

Successful managemetit of the avulsed tooth should

aim at the prevetition of both ankylosis and inflammatory resorption. Cotisequently, the vitality ol the
periodontal membrane must be maintained and
bacterial invasion of the pulp prevented. CutTendy,
we are aware of the factors responsible for the itiitiation of the various healing patterns in the periodotital tnembrane, but further sttidies are required
to examine the progression of these patterns utider
various conditions.
Acknowtedgements Gratits from the Swedish Medical
Research Council (nos. 06001 & 6651), Stockholms
Iatis latidsting, Folksatn forskningsfond and Sveriges
Mejeriers Riksforbund have supported the studies
by the authors of this review.
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