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Europcai Jcmmd cf Onhodcnlta 12 (1990) 25-37 © 1990 European Orthodontic Society

A long-term study of 370 autotransplanted premolars.


Part III. Periodontal healing subsequent to
transplantation
J. 0. Andreasen,1 H. U. Paulsen,2 Z. Yu 3 and 0. Schwartz5
'Department of Oral Surgery and Oral Medicine, University Hospital (Rigshospitalet), Copenhagen,
Denmark department of Orthodontics, Municipal Dental Health Service, Copenhagen, Denmark 'Faculty
of Stomatology, Beijing, China 'Statistical Research Unit, University of Copenhagen, Denmark
department of Oral and Maxillofacial Surgery, Dental College, Copenhagen, Denmark

SUMMARY The purpose of the present investigation was to determine the long-term prognosis of
autotransplanted premolars with respect to periodontal healing. The subjects consisted of 195
patients aged 7 to 35 years, with a total of 370 autotransplanted all operated and followed with a
standard technique. The observation period ranged from 1 to 13 years. Periodontal healing as
demonstrated radiographically was complete in most cases after 8 weeks. Root resorption
occurring after transplantation was divided into surface-, inflammatory- and replacement
resorption (ankylosis). Root resorption occurred in 52 of the transplanted teeth and was usually
diagnosed within 6 months. Root resorption was found to be significantly related to increasing
stage of root development and the stage of eruption at the time of transplantation. Subsequent
orthodontic movement of teeth with completed root formation at the time of transplantation
resulted in a slight increase in the frequency of both surface and inflammatory resorption. The
present study indicates that trauma to the PDL of the transplant is the explanatory factor for the
development of root resorption.

Introduction related to extra-alveolar storage of replanted and


autotransplanted teeth before replantation
Autotransplantation of premolars has recently (Andreasen, 1981c; Schwartz et al., 1985a, b) and
become a popular method of treating various the maturation stage of experimentally replanted
types of malocclusions. A precondition for the and autotransplanted teeth (Kristerson and
use of this method is a thorough knowledge of
the expected long-term success rate. In this Andreasen, 1983, 1984a, b; Schwartz and
regard both pulpal healing, periodontal healing Andreasen, 1988, 1989).
without root resorption and continued root Based on the knowledge gained from these
formation are of importance. So far, the only experiments it would be useful to examine clini-
established relationship between periodontal cal material of autotransplanted premolars with
healing and transplantation of premolars has respect to their resorption potential. The purpose
been that increased root development of the graft of the present study was, therefore, to analyse the
leads to a greater risk of root resorption (Krister- following healing events in autotransplanted
son, 1985; Schwartz el al, 1985a, b). In experi- premolars:
mental replantation and autotransplantation 1. How soon after autotransplantation of pre-
experiments a strong correlation has been found molars can periodontal ligament healing be
between damage to the innermost zone of the observed radiographically?
periodontal ligament and subsequent root 2. How soon after autotransplantation can root
resorption (Andreasen, 1981a, b, c; Andreasen resorption be diagnosed?
and Kristerson, 1981). Furthermore, root 3. Is root resorption related to pre-, per- or post-
resorption has been found to be significantly operative variables?
26 J. O. ANDREASEN ET AL.

O.d. 2 months 6 months 2 years


Figure 1 Surface resorption (arrow) after transplantation of a maxillary second premolar. The cause of resorption is possibly
orthodontic treatment of the transplanted tooth.

O.d. 4 weeks 6 months


Figure 2 Surface resorption (arrow) subsequent to transplantation of a maxillary second premolar. The cause of resorption is
possibly collision between the graft and the mesial cervical socket wall.

Subjects and methods on the root surface adjacent to a normal or


slightly extended periodontal ligament space
The material consisted of 370 premolar trans- (Figs. 1 and 2).
plants reviewed over a period of 1 to 13 years.
The description of criteria for patients entering Inflammatory resorption: small or large
the study, the surgical procedure and the follow- resorption cavities on the root surface associated
up regimen has been dealt with in previous with similar resorption activity of the adjacent
reports (Andreasen et al., 1990a, b). Periodontal alveolar bone (Figs. 3 and 4).
ligament healing was registered radiographically Replacement resorption: disappearance of the
and classified as partial when a periodontal periodontal space and root resorption without
ligament space could be partly followed around radiolucency in relation to the resorption area
the root and complete when the root periphery (Fig. 5) (Andreasen 1980a).
was entirely surrounded by a newly formed The methodology in the statistical analysis has
periodontal ligament space. been reported in an earlier study (Andreasen el
al., 1990b).
External root resorption (i.e. originating from
the periodontium) was also registered according
to the system described by Andreasen and
Hjeorting-Hansen (1966a, b). Results
Surface resorption: small resorption cavities Partial periodontal ligament healing was found
AUTOTRANSPLANTED PREMOLARS. PART III 27

O.d. 4 weeks 8 weeks


Figure 3 Inflammatory resorption after transplantation of a maxillary second premolar. Note the undermining nature of the
resorption cavity and the associated breakdown of the lamina dura.

1 week 4 months 6 months


Figure 4 Inflammatory resorption affecting the cervical area of a transplanted maxillary second premolar. Note that the
buccally or lingually positioned resorption cavities show up as stamped out radiolucencies. After extirpation of necrotic and
infected pulp tissue and the use of calcium hydroxide as a dressing, the resorption process is arrested.

O.d. 2 months year 5 years


Figure 5 Replacement resorption affecting the cervical area of a transplanted second maxillary premolar. Note the rapid
progression of the resorption process and the infraposition of the transplant.
28 J. O. ANDREASEN ET AL.

O.d. O.d. 1 month 2 months 1 year


Figure 6 Radiographic progression of periodontal healing after transplantation of a maxillary second premolar to site of
aplasia in the mandible.

LIFE TABLE ANALYSIS OF PERIODONTAL LIGAMENT HEALING


Table 1 the time interval before diagnosing the
% survival
individual resorption types is shown. It appears
that the diagnosis of replacement resorption was
100
IncompUU root formation made considerably later than surface- or inflam-
90 matory resorption.

i
1
I
80 A univariate analysis showed that the follow-
ing factors were significantly related to root
70
resorption activity: Sex of patient, type of pre-
60 molar graft, stage of root development, stage of
SO
Complete root formation eruption, age of patient, number of roots, extent
of damage to the periodontal ligament, inflam-
40 mation in the recipient region, traumatic occlu-
30 sion of the graft after surgery (Table 2).
A multivariate analysis showed that stage of
20.
root development divided into two stages
10 Years (namely, incomplete and complete) was the best
12 5 10 predictor for root resorption (Tables 3 and 4).
However, the variable stage of eruption had
Imo. Stno. Smo. lyr. 2yr. 5yr. tOyr.
almost the same explanatory value. The indi-
vidual types of resorption could not be studied
by a multivariate analysis because of their rela-
Comply root *» * k 53 49 40 12 17 5
fomutlon R«»orplloo 0 9 4 3 0 0 tively rare occurrence.
Figure 7 Life table analysis of periodontal healing of 370 As a control for the multivariate analysis, the
autotransplanted premolars. material was re-analysed for influence of the
different variables; but now divided into teeth
with incomplete and complete root formation.
after 4 weeks, the majority of transplants showed This analysis resulted in only one significant
complete periodontal healing 8 weeks after trans- relation, namely, a relation to the previously
plantation (Fig. 6). identified factor stage of eruption. It appears that
abnormal position in contrast to normal position
External root resorption before eruption significantly increased the risk of
Altogether, 52 teeth showed external root resorption.
resorption. The time span before the diagnosis of To further characterize possible relationships
root resorption according to complete or incom- between the three different resorption types and
plete root development is shown in Fig. 7 and in the registered clinical variables, each resorption
AUTOTRANSPLANTED PREMOLARS. PART III 29

Table 1 Relation between observation period and diagnosis of root


resorption.

Observation period

No. 4 wk 8wk 6 mo lyr 2yr Syr

Surface resorption 4 1 6 5 1
Inflammatory resorption 5 11 2
Ankylosis 3 7 8 I 2

type was analysed according to stage of root significantly related to the stage of root develop-
development (divided into incomplete and com- ment.
plete). The statistical analysis revealed a significant
Surface resorption was found in only 17 cases increase in the frequency of inflammatory
(4.6%). This resorption type was usually located resorption when there was more than 25 per cent
in the cervical part of the root and usually of the periodontal ligament damaged at the time
diagnosed within the first year after transplan- of transplantation (Table 8).
tation (Table 1). Active resorption took place Another significant relationship was found
over a period of several weeks or months, between a narrow alveolus with apparently
whereafter a new periodontal ligament space was physical contact between the graft and alveolar
established, usually leaving an indentation in the bone for teeth with completed root formation
root surface (Fig. 3). Typically, the resorption (Table 9).
cavity was shallow and not undermined as in Finally, orthodontic treatment of teeth with
inflammatory root resorption (see later). completed root formation was related to a
In the statistical analysis surface resorption significant decrease in inflammatory root resorp-
was related to complete and incomplete root tion (Table 7).
formation being more prominent in the latter As inflammatory resorption is known to be
group. If all stages were used in rating root strongly related to pulpal status, root resorption
development (Table 3), it appears that surface activity was correlated with pulpal status (Table
resorption was especially prominent in stages 3, 5 10). It appears that inflammatory resorption
and 6. (except for one case with a cervical resorption
The other factor (also significantly related to process) was associated with pulp necrosis.
the combined resorption group) was stage of
eruption. In this analysis, surface resorption Treatment of inflammatory root resorption
appeared to be significantly increased under one This resorption type was in 18 cases treated by
particular circumstance; namely, eruption of a pulp extirpation and a calcium hydroxide dress-
tooth with incomplete root formation before ing prior to definitive root filling with gutta
occlusion. percha and a sealer. In all cases, periapical
Extra-alveolar storage, divided into imme- healing as well as arrest of the inflammatory
diate transplantation and a storage period before resorption occurred (Fig. 8). However, due to the
transplantation, showed significantly more sur- large diameter of the root canal one premolar
face resorption after storage, but only for teeth later fractured at the cervical margin during
with incomplete root formation (Table 6). normal function. In two cases inflammatory
Orthodontic movement of the transplanted resorption was arrested but ankylosis developed
tooth was found to be followed by a significantly at the previous resorption sites (Fig. 9).
increased risk of surface resorption for teeth with Replacement resorption (ankylosis) occurred
complete root development (Table 7). in 21 (4.8%), and this complication could usually
Inflammatory resorption was seen in 18 cases be diagnosed within the first year after transplan-
(4.8%), usually diagnosed one to two months tation (Table 1) (Fig. 10). In 15 instances,
after transplantation amd also found to be ankylosis was diagnosed by the combined radio-
30 J. O. ANDREASEN ET AL.

Table 2 Relation between various clinical variables and root resorption.

*No. and
% with Probability
Variable No. root resorp- value
tion

Sex Male 160 30 19%


Female 210 22 10% 0.034
Graft type Pi sup 28 6 21%
P 2 sup 274 39 14%
Pi inf 6 3 50%
P 2 inf 62 4 6% 0.014
Position of graft Occlusion 81 26 32%
Infraocclusion 63 10 16%
Not erupted, abnormal position 43 6 14%
Not erupted, normal position 183 10 5%
Age of patient (years) 9-11 71 5 7%
12-13 218 30 14%
14-31 81 17 21% 0.047
Stage of root development 0 2 0 0%
1 4 1 25%
2 73 3 4%
3 210 24 11%
4 28 3 11%
5 20 6 30%
6 33 15 45% 0.001
Apical pulp width, preoperatively (mm) 0-0.9 30 13 43%
1.0-1.9 62 12 19%
2.0-2.9 109 9 8%
3.0-3.9 63 3 5%
4.0-4.9 12 I 8%
5.0-5.9 7 I 14% 0.00001
Apical pulp width, postoperatively (mm) 0-0.9 21 6 29%
1.0-1.9 39 6 19%
2.0-2.9 62 6 10%
3.0-3.9 97 10 10%
4.0^.9 77 8 10%
5.0-7.0 32 3 9% 0.227
Pulp length, preoperatively (mm) 6-8 21 1 5%
9-11 119 13 11%
12-14 153 16 10%
15-20 70 20 29% 0.00001
Pulp length, postoperatively (mm) 6-8 12 0 0%
9-11 100 II 11%
12-14 118 15 13%
15-20 64 19 30% 0.0002
Inflammation in recipient region no 362 49 15%
yes 3 2 66% 0.104
Alveolar process atrophy no 352 50 14%
yes 17 2 12% 0.999
Osteotomy at graft removal no 145 33 23%
yes 220 18 8% 0.001
Type of bur cooling internal 175 28 16%
external 184 22 18% 0.909
Apicoectomy no 363 50 14%
yes 7 2 29% 0.256
AUTOTRANSPLANTED PREMOLARS. PART III 31

TaWe 2 Continued

•No. and
% with Probability
Variable No. root resorp- value
tion

Damage to PDL 0-25% 307 33 11%


26-50% 23 6 23%
51-75% 16 5 31%
76-100% 11 6 54% 0.000
Storage of graft (min.) 0 102 18 18%
1-5 161 22 14%
6-10 63 8 13%
11-30 34 3 9% 0.581
Bone graft used no 329 45 14%
yes 37 5 14% 1.000
Recipient region max. anterior 33 4 12%
max. premolar 50 5 10%
mand. premolar 267 39 15%
other 20 4 20% 0.697
Antibiotics postoperatively 201 24 12%
pre and postoperatively 166 27 16% 0.295
Fixation type no splinting 8 1 13%
suture 298 42 14%
flexible 16 1 6%
rigid 46 8 17% 0.743
Orthodontic movement of graft no 199 27 14%
yes 170 25 15% 0.869

*The numbers of teeth in the various groups do not always add up to 370 due to missing values.

Table 3 Relation between stage of root development and subsequent periodontal healing.

Root development stages

0 I 2 3 4 5 6

PDL healing 2(100%) 3 (75%) 70 (96%) 186(89%) 25 (89%) 14 (70%) 18(55%)


Root resorption 0 1 3 24 3 6 15
Surface resorption 0 0 1 10 1 3 2
Inflammatory resorption 0 0 2 4. 2 3 7
Ankylosis 0 1 0 11 0 0 9

graphic changes and a high metallic percussion losis site, using local anaesthesia and luxation
sound. In 5 instances, clinical findings were the forces by forceps (small rotation movements). In
only indication of ankylosis. 7 of these cases immediate orthodontic extrusion
The statistical analysis revealed that ankylosis of the infrapositioned tooth was initiated. In 3 of
was significantly related to administration of these cases, restoration of normal periodontal
penicillin both preoperatively and postoperati- conditions was established, i.e. a normal perio-
vely in teeth with completed root formation dontal ligament as demonstrated by radio-
(Table 5). graphic and clinical examination (Fig. 10). In 11
Treatment of replacement resorption: In 10 untreated cases, two showed restoration of a
cases luxation was attempted to break the anky- normal PDL. In one of these cases after place-
32 J. O. ANDREASEN ET AL.

Table 4 Relation between graft position before transplantation and subsequent periodontal
healing.

Not erupted
Not erupted Abnormal
Normal position position Infra occlusion Occlusion

PDL healing 173 (95%) 37 (88%) 53 (84%) 55 (68%)


Root rcsorption 10 6 10 26
Surface resorption 4 1 6 6
Inflammatory resorption 4 1 0 1
Ankylosis 10 5 8 17

Table 5 Relation between method of administering antibiotics and external root resorption.

Preoperative Pre and postoperative Unknown *p value

Incomplete root formation


Periodontal healing 153(92%) 131 (89%) 2 N.S.
Root resorption 14 16 1 N.S.
Surface resorption 4 7 1 N.S.
Inflammatory resorption 3 5 0 N.S.
Ankylosis 7 5 0 N.S.
Complete root formation
Periodontal healing 24(71%) 8 (42%) 0 N.S.
Root resorption 10 11 0 N.S.
Surface resorption 3 2 0 N.S.
Inflammatory resorption 6 4 0 N.S.
Ankylosis 2 7 7 0.01

* Significance level according to a Fisher's exact test.

Table 6 Relation between length of extraalveolar storage and subsequent periodontal healing.

Extra-alveolar period in min.

0 1-5 6-10 11-30 Unknown pvalue

Incomplete root formation


Periodontal healing 81 (86%) 121 (90%) 47 (94%) 29 (97%) 8
Root resorption 13 13 3 1 1 N.S.
Surface resorption 8 3 0 0 1 0.01
Inflammatory resorption 2 5 0 1 0 N.S.
Ankylosis 4 5 3 0 0 N.S.
Complete root formation
Periodontal healing 16(55%) 13 (72%) 1 (33%) 2 (66%) 0 N.S.
Root resorption 13 5 2 1 0 N.S.
Surface resorption 0 4 1 0 0 N.S.
Inflammatory resorption 9 1 0 0 0 N.S.
Ankylosis 6 1 I 1 0 N.S.

* Significance level according to a Fisher's exact test when no storage was compared to a storage period.
AUTOTRANSPLANTED PREMOLARS. PART III 33

Table 7 Relation between orthodontic treatment and external root resorption.

No orthodontic Orthodontic
treatment treatment Unknown •p value

Incomplete root formation


Periodontal healing 156(92%) 129 (88%) 0 N.S.
Root resorption 14 17 1 N.S.
Surface resorption 3 9 0 N.S.
Inflammatory resorption 6 2 0 N.S.
Ankylosis 5 7 0 N.S.
Complete root formation
Periodontal healing 16(56%) 16(66%) 0 N.S.
Root resorption 13 8 0 N.S.
Surface resorption 0 5 0 0.02
Inflammatory resorption 9 1 0 0.02
Ankylosis 6 3 0 N.S.

* Significance level according to a Fisher's exact test.

Table 8 Relation between extent of PDL damage and external root resorption.

PDL damage
0-24% 25-100% Unknown *p value

Incomplete root formation


Periodontal healing 250 (92) 34 (77%) 0 0.06
Root resorption 21 10 1 N.S.
Surface rcsorption 10 2 0 N.S.
Inflammatory resorption 4 4 0 0.03
Ankylosis 8 4 0 N.S.
Complete root formation
Periodontal healing 24 (66%) 8 (47%) 0 N.S.
Root resorption 12 9 0 N.S.
Surface resorption 3 2 0 N.S.
Inflammatory resorption 4 2 0 N.S.
Ankylosis 4 5 0 N.S.

'Significance level according to a Fisher's exact test.

Table 9 Relation between size of alveolus and external root resorption.

Size of alveolus Narrow Normal Wide Unknown *p value

Incomplete root formation


Periodontal healing 68 (86%) 147(91%) 67 (92%) 4 N.S.
Root resorption 11 14 6 0 N.S.
Surface resorption 6 4 2 0 N.S.
Inflammatory resorption 4 2 2 0 N.S.
Ankylosis 1 9 2 4 N.S.
Complete root formation
Periodontal healing 9 (53%) 17(71%) 6 (50%) 0 N.S.
Root resorption 8 7 6 0 N.S.
Surface resorption 0 4 1 0 N.S.
Inflammatory resorption 8 1 1 0 0.002
Ankylosis 3 2 4 0 N.S.

'Significance level according to a Chi-square test.


34 J. O. ANDREASEN ET AL.

Table 10 Relation between pulp and periodontal ment of a restoration which brought the tooth
ligament healing. into occlusion and in one tooth after orthodontic
treatment.
Number of cases with
Loss of marginal attachment
Pulp Pulp
Resorption type healing necrosis This complication was seen in only 3 instances
(0.8%). It appeared to be due to a too superficial
Periodontal healing 289 32 placement of the transplant in its new socket.
Surface resorption 13 3
Replacement resorption 8 6
(Fig. 11).
Inflammatory resorption 1 14
Surface resorption +
Replacement resorption 1 Discussion
Replacement resorption+
Inflammatory resorption 0
An important fact to consider in a study like this
is the reliability of radiographs in diagnosing

1 week h months 1 year 5 years

Figure 8 Arrest of inflammatory resorption by combined initial use ofcalciumhydroxide followed later by a gutta percha root
filling.

1 week 'i -yest


Figure 9 Arrest of inflammatory resorption by endodontic therapy with calcium hydroxide leading to ankylosis of the previous
resorption cavities.
AUTOTRANSPLANTED PREMOLARS. PART I I I 35

1 week 4 weeks 4 months 1 year


Figure 10 Replacement resorption of a transplanted second maxillary premolar successfully treated by luxation (after 6
months) and immediate orthodontic extrusion of the infrapositioned tooth.

O.d. 1 week 2 years


Figure 11 Loss of marginal attachment probably due to a too superficial position of the transplant.

root resorption. A recent autopsy study, where majority of surface resorption cavities have been
artificial 'resorption' cavities were introduced in overlooked in this clinical study.
premolars, showed that there is a critical lower The significant relationship found in this study
dimension of cavity depth of approximately 0.6 between root resorption and root development
mm where radiographic demonstration becomes and/or stage of eruption calls for an explanation.
unreliable (Andreasen et al., 1987). As both Is this relationship an expression of a greater
replacement resorption and inflammatory repair or regenerative capacity due to a more
resorption at least if left untreated usually pro- embryonic character of the pulp and periodon-
gress until they reach the limits of the root canal, tium in immature teeth, or does it reflect ranges
the follow-up schedule used in the present study of damage to the PDL and/or the pulp elicited by
has possibly identified the majority of these two the different surgical approaches necessary to
resorption entities. More questionable is diagno- remove the tooth or tooth germ, or a combina-
sis of surface resorption cavities due to their very tion of both?
limited depth. Thus, previous histological studies In previous replantation and transplantation
have shown that their depth is usually around 0.1 experiments in monkeys it was found that root
mm. (Henry and Weinmann, 1951; Andreasen, resorption was significantly related to damage to
198Id). This would indicate that possibly the the innermost layer of the PDL (Andreasen
36 J. O. ANDREASEN ET AL.

1980b, 1981a, b, 1985; Andreasen and Krister- but may represent a type 2 error in the statistical
son, 1981). Damage to the periodontal ligament analysis.
during a transplantation procedure could be In a previous study by Lagerstrom and Kris-
related to either accidental severance of the terson (1985), it was shown that orthodontic
periodontal ligament close to or at the root treatment of autotransplanted teeth resulted in
surface, or a compression injury to the PDL slightly increased apical shortening (average 0.4
during graft removal. In immature stages of root mm). The present study supports this finding.
development, it appears from clinical experience However, in both studies the slight resorption
that the tooth is usually covered by a thick follicle appears to have limited clinical relevance.
or periodontal ligament. Furthermore, the forces The relationships found between extra-alveo-
necessary for removing the graft from its socket lar storage, damage to the periodontal ligament
are very small, possibly indicating that a mini- and method of antibiotic administration were on
mum of damage has been inflicted upon the the borderline of significance. Considering the
PDL. In contrast, when the tooth is fully erupted, number of associations tested they should prob-
it implies a firm attachment of the periodontal ably be considered as type 2 errors.
ligament fibres to both the cementum and alveo-
lar socket. The severance of these during luxation
can occur at all levels of the PDL. This usually Conclusions
implies that some areas on the root surface are 1. Root resorption can usually be diagnosed
left with no or very few vital cells (Reinholdt el radiographically and/or clinically 4 to 8 weeks
al., 1977). Moreover, the luxation procedure after transplantation.
appears to result in considerable cell death at the 2. The risk of root resorption is closely related to
'corners' of the root, afindingwhich seems to be stage of root development and increases with
accompanied by a significant disposition to root increasing root development.
resorption at these corners (Andreasen, 1981a, 3. Subsequent orthodontic treatment of teeth
b).' with complete root development resulted in a
In light of the above-mentioned findings, it slight increase in the frequency of both surface
seems reasonable to assume that the strong and inflammatory root resorption.
relationship between root development and/or
stage of eruption and subsequent root resorption
of the graft is dependent upon the combination Acknowledgments
of differences in anatomy and forces necessary to This study has been supported by Danmarks
remove the graft at different stages of develop- Sundhedsfond.
ment. As root resorption was still found to occur
(although with a low frequency) when transplan-
tation is performed at initial stages of root References
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developing teeth in order to improve techniques tation of mature permanent incisors in monkeys. Swedish
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pulpal healing of mature permanent incisors in monkeys.
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odontic treatment and surface resorption is to be and autotransplantation of incisors in monkeys. Inter-
expected when the known relationship between national Journal of Oral Surgery 10: 54-61
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(Rygh, 1977; Linge and Linge, 1985). Most the periodontal ligament after replantation and sub-
likely the orthodontic forces used have created sequent development of root resorption. Acta Odontolo-
gica Scandinavica 39: 15-25
local injury zones (hyaline areas) which have
Andreasen J O 1981c Effect of extra-alveolar period and
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AUTOTRANSPLANTED PREMOLARS. PART I I I 37

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