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Premolar autotransplantation in juvenile dentition: quantitative assessment of vertical bone and soft tissue growth
Accepted Manuscript Premolar autotransplantation in juvenile dentition: Quantitative assessment of vertical bone and soft tissue growth Inessa Michl, DMD, Dirk Nolte, MD, DMD, PhD, Claudia Tschammler, DMD, Martin Kunkel, MD, DMD, PhD, Robert Linsenmann, MD, DMD, Johannes Angermair, DMD PII:
S2212-4403(17)30061-5
DOI:
10.1016/j.oooo.2017.02.002
Reference:
OOOO 1705
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 14 September 2016 Revised Date:
16 January 2017
Accepted Date: 13 February 2017
Please cite this article as: Michl I, Nolte D, Tschammler C, Kunkel M, Linsenmann R, Angermair J, Premolar autotransplantation in juvenile dentition: Quantitative assessment of vertical bone and soft tissue growth, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2017), doi: 10.1016/ j.oooo.2017.02.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Premolar autotransplantation in juvenile dentition: Quantitative assessment of vertical bone and soft tissue growth Inessa Michl, DMD
1, 2
, Dirk Nolte, MD, DMD, PhD
1, 2
, Claudia Tschammler, DMD
2
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1, 3
, Martin 1
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Kunkel, MD, DMD, PhD , Robert Linsenmann, MD, DMD , Johannes Angermair, DMD
Running title: Premolar transplantation in juvenile dentition
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1. Private Practice for Oral and Maxillofacial Surgery, Sauerbruchstraße 48, 81377 Munich, Germany
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2. Ruhr-University of Bochum, Department of Oral & Maxillofacial Surgery, In der Schornau 23-25, 44892 Bochum, Germany
3. University of Goettingen, Department of Preventive Dentistry,
Periodontology and Cariology, Robert-Koch-Str. 40, 37075 Goettingen, Germany
Dirk Nolte, MD, DMD, PhD [email protected] Tel. +49-89/74 80 99 99
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Fax +49-89/74 00 91 35
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Correspondence:
Conflict of Interests: The authors have no financial interest to disclose.
Keywords:
Autogenous tooth transplantation; premolar transplantation; traumatic dental injury (TDI); tooth aplasia; pediatric dentistry; orthodontics
Word count abstract: 188, manuscript: 6520, number of references: 50, number of tables/figures: 15
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Abstract: Objective: Premolar autotransplantation represents an effective therapeutic option for the treatment of juvenile dentition with either aquired or congenital hypodontia. The objective of this prospective clinical study was to quantitatively assess bone
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and soft tissue levels after autogenous premolar transplantation by clinical and radiographic parameters.
Study Design: In the study 26 premolars were transplanted in 20 patients after
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traumatic tooth loss (n=16) or congenital aplasia (n=10) in the anterior maxilla. Based on standardized photographic documentation, the relative soft tissue level
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was measured in comparison to the healthy adjacent teeth. Radiographic findings included the evaluation of root resorption, pulp canal obliterations and the relative bone height.
Results: Average survival rate of transplanted premolars (n = 26) was 100% over
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a follow-up period of 29 months (range 10-60 months). The relative soft tissue level significantly increased by +1.1 mm (p<0.05). Radiographs showed the tendency to vertical bone growth. Continuous root development and signs of pulpal
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healing were observed postoperatively on 18 transplants (69.2%). Conclusions: Autogenous premolar transplantation represents a safe method to
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ensure functional and aesthetic rehabilitation in the anterior maxilla irrespective of the nature of tooth loss. ClinicalTrials.gov: NCT02740907
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Introduction Traumatic dental injury (TDI) to the upper anterior teeth represents a frequent injury in children and adolescents with a prevalence of up to 30%
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(1). According to previous studies, 7% to 8% of all accidents are associated with concomitant tooth loss (2). The practitioner faces a difficult task in the
clinical management of the resulting tooth gap in children aged 8-12 years
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since an implant as tooth replacement is not a treatment option during active jaw growth (3, 4).
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A similar situation is encountered in case of tooth aplasia of the maxillary incisors. According to Kavadia et al. the maxillary lateral incisor is the third most common aplastic tooth after the lower wisdom tooth and the mandibular second premolar (5).
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Orthodontic gap closure is the treatment of choice under favourable conditions. However, a symmetrical and aesthetically satisfying result cannot always be achieved with this method, especially in case of traumatic
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avulsion of the central incisors. In addition, the indication for an orthodontic gap closure is limited by the orthognathic situation of the dental arch in many
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cases (6). While treatment with composite-adhesive attached bridges represents a viable alternative, the underlying alveolar bone resorption may impede later dental implant placement. A tooth loss without adequate replacement in general leads to a psychological impairment of the children which can not be underestimated (7, 8). Premolar autotransplantation (auto-TX) represents a treatment option with an excellent long-term prognosis and reliable aesthetic results starting at the
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ACCEPTED MANUSCRIPT age of 10 (9). It is the only available technique that favorably affects the growth of the adolescent dentition due to its known potential to support soft tissue and bone development (3, 10, 11). In contrast to all other alternative therapies, vertical defects can be compensated during the adolescent growth
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period. This is the crucial advantage of premolar transplantation in cases of
trauma where vertical defects of the anterior upper jaw arise frequently. The
technique has already been described in 1960 by Slagsvold and Bjercke (12,
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13). In the literature, excellent average survival rates of > 90% in follow-up
observations up to 41 years have been published (14-19). In addition, long-
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term studies report no clinically or radiographically detectable difference of transplants compared to the adjacent teeth (20). The aesthetic result from the patients` and dentists` point of view is very satisfying and can be achieved by composite or ceramic restorations of the transplant after the
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healing period (21). Premolars are especially suited as transplants in the anterior maxillary region because they often have to be extracted for orthodontic reasons and, due to their root morphology, an atraumatic
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extraction is technically feasible (22).
The ideal root development for transplantation is proposed in the literature at
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the age of about 10 years with an open apex and with a root length of ¾ (growth stage 11 according to Moorrees et al.) (23). The reason therefore is that the regeneration of the periodontal ligament and the revascularisation of the transplant is the greatest during this growth period (24-26). The indication for premolar transplantation must always be made in close consultation with the orthodontist. In cases of malocclusion, in which a compensation extraction is planned, a win-win situation can arise (27, 28). 4
ACCEPTED MANUSCRIPT To the best of our knowledge, there has been no scientific study which has quantitatively assessed the inductive potency of premolar transplantation on both soft tissue and bone growth. The objective of this prospective clinical case study was therefore to quantitatively assess the vertical changes of the
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adolescents following premolar transplantation.
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peri-transplant tissues in the maxillary anterior region in children and
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Materials and Methods Subjects In 20 patients 26 premolar transplantations were performed from 2006 to 2014 to replace the maxillary incisors (mean age 13.6, females: 10, males:
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10). Thirteen patients suffered from traumatic dental injury (TDI) with
subsequent tooth loss (n=16 transplants). In 7 patients, aplasia of teeth in
the maxillary anterior region from right canine to left canine was present
regard to donor and recipient regions.
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(n=10 transplants). Table 1 shows the distribution of the transplants with
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The choice of transplant selection was planned in close cooperation with the orthodontist.
The guidelines of this study have followed the Declaration of Helsinki. The study was approved by the ethics committee of the Bavarian Medical
Surgical procedure
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Association of Munich, No. 13116/2013.
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All patients were preoperatively informed about therapeutic alternatives to
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the planned intervention as well as risks and chances of success. The following procedures were undertaken with the understanding and written consent of each patient. All procedures were performed under short general anaesthesia. The teeth to be transplanted were gently extracted with anatomical forceps and stored in a nutrient solution for preservation of the periodontal ligament based on the concept of anti-resorptive therapy (29). The tooth storing solution consisted of 100 mg doxycycline, 4 mg dexamethasone and 10 ml of physiological saline. Teeth transplanted 6
ACCEPTED MANUSCRIPT without intermediate storage in the nutrient solution, had a storage or ischemic time of zero minutes (see Table 2). The transplant bed was prepared with a surgical bur (Surgery TC-Cutter, Acurata medica, Thurmansbang, Germany) as atraumatically as possible, preferably using a
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tunneling preparation technique. The transplants were inserted in orthograde
position with anatomical tweezers without injuring the root surface. All teeth were conditioned using an enamel etching technique and flexibly fixed for 3
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weeks with a titanium trauma splint (TTS, Medartis, Basel, Switzerland) and
composite (Syntac Classic, Tetric Evo Flow, Ivoclar Vivadent, Schaan,
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Lichtenstein). If an orthodontic arch wire was present, then the teeth were fixed in a flexible manner to the available wire. Wound closure was performed using modified backstitch sutures. Patients greater than 12 years of age were prescribed systemic antibiotics using doxycycline 100 mg per
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day (100 mg/d, Doxycyclin AL, Aliud Pharma®, Laichingen, Germany) for 7 days as an antiresorptive therapy (29) intra- and postoperatively as well as soft diet for 3-4 days under continuation of daily oral hygiene. The first
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wound control took place on the first post-operative day. Sutures were removed on day seven. The splinting was removed after three weeks and
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the tooth surfaces were polished and fluoridated. This was followed by an appointment at the orthodontist for the integration of the transplant into the multibracket appliance. Recall visits included clinical and radiographic controls after 3, 6, 9, and 12 months. The patients were then seen at yearly intervals for follow-up care.
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ACCEPTED MANUSCRIPT Clinical follow-up The clinical follow-up included the evaluation of the periodontal status, percussion sensitivity and sensibility of the transplants. The approach applied is similar to that from previous studies of our group
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(30, 31). Oral hygiene and periodontal status of the transplants were
determined using the Peridontal Screening Index (PSI) and a pocket depth measurement. The percussion sensitivity was clinically identified to help
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determine a physiological percussion and to identify ankylosis. In addition, a quantitative measurement of the tooth mobility was carried out clinically and
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with the periotest device (Periotest Classic; Medizintechnik Gulden, Modautal, Germany).
The vitality of the teeth was tested by sensitivity control using a cold spray and by electric pulse technique (Vitality Scanner; SybronEndo, Orange, CA,
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USA). Radiographic analysis was performed in regard to partial and total pulp canal obliteration. Pulp canal obliteration was considered as physiological response of the transplant to trauma and thus as vital sign of
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pulpal healing (32, 33).
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ACCEPTED MANUSCRIPT Soft tissue level The soft tissue level measurement was carried out on the basis of a standardized photographic documentation. The procedure was performed analogously to a previously published study in which the technique of vertical
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soft tissue measurements in the growing dentition was described (31): a
central photograph of the anterior maxillary region was chosen as reference. As shown in Figure 1, a vertical line was drawn through the middle of the
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transplant parallel to the tooth axis. In addition, an orthogonal was created
tangentially to the gingival margin. This line yields the relative level of soft
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tissue compared to the healthy neighbouring tooth. The scaling in mm was calculated using the rule of three from the crown lengths measured in vivo (Figure 1).
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Radiographic follow-up
The relevant parameters were determined using orthopantomography. This radiographic technique was used as standard diagnostics to allow
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reproducibility of the measured bone and root lengths. Dental films were used for a more accurate diagnostics of the root surfaces. Pulp canal
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obliterations, the change in the length of the transplants` roots, factors of bone healing and root resorptions were determined. Root resorptions were classified and documented according to Andreasen et al. (34). The mineralisation stages of the root development were determined according to Moorrees et al. (23) in order to correlate the stage of root development versus occurrence of root resorptions (Table 3).
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ACCEPTED MANUSCRIPT Bone level The bone height in the growing dentition was determined in relation to the adjacent teeth as previously described (31). For this, a connecting line was drawn on the x-ray between the mesial cementoenamel junction of the distal
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adjacent tooth and the distal cementoenamel junction of the mesial adjacent tooth (Figure 2). Starting from this line, a perpendicular was drawn to the
most distant point of the alveolar ridge both mesially and distally and the
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length of this line was measured. All measured values lying coronally to line
A were marked with a positive sign, all those lying apically with a negative
distances was calculated (Fig. 2).
Determination of root length
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sign. For final data generation, the average between the mesial and distal
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The root length of the transplants was determined by the distance between two lines. The first line was constructed by connecting the two most apical points of the root tip, while the second line was a connection of the mesial
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and distal cementoenamel junction of the tooth (31, 35). To enable the comparability of measured lengths on the different radiographic images, a
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magnification factor was calculated from the quotient of postoperative crown length and crown length at the follow-up time (36). The measured root length of the follow-up image was multiplied by the magnification factor and then subtracted from the postoperatively measured initial length. Measurement errors were levelled by repeated measurement according to a time interval. Houston’s reliability coefficient and Dahlberg’s Formula were used to
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ACCEPTED MANUSCRIPT evaluate the error of measurement (37, 38). The overall values were ≥0.95, therefore an acceptable accuray was reached.
Transplant Survival and Success
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Transplant survival and success were assessed in the follow-up intervals.
The success criteria were based on a previous study of our group (30): Clinical success criteria were PSI under 3, tooth mobility less than II and no
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the transplant and the absence of root resorptions.
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percussion sensitivity. Radiographic criteria were bony regeneration arround
Statistical analysis
The statistical analysis was performed using Excel 2010 (Microsoft Corp., Redmond, WA, United States) and Prism (GraphPad Software, La Jolla, CA,
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USA). For parametrically distributed data, a dependent t-test was conducted and for non-parametrically distributed data, a Wilcoxon test was applied. The
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significance level was set at p<0.05.
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Results Transplant survival and success 26 premolar transplants were performed in the anterior maxillary for tooth replacement after tooth aplasia (n=10) or previous TDI (n=16) in 20 patients
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(N=20; n=26). There were 14 males and 12 females and their ages ranged
from 11 to 19 years of age. The survival rate of the transplants was 100% over an average follow-up observation period of 29 months (min.: 10 months;
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max.: 60 months). Since all transplants were clinically free from irritation, no
limitation of success was given with regard to tooth mobility and periodontal
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conditions. In 8 of the 26 transplants, a resorption was present. Since one resorption occurred after a renewed trauma, the transplant was excluded from the non-successful group yielding a success rate of 73%. All other
Surgical parameters
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conditions of success have been met.
The average ischemia time during transplantation was 3 min (min: 0; max.:
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17) (Table 2). 15 transplants were temporarily stored in the above described
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nutrient solution, whereas 6 transplants were directly positioned in the recipient region. In 5 cases, there were no data regarding the ischemia time. After transplantation, 20 transplants were splinted by wire-composite fixation. One premolar was solely stabilized by a backstitch suture, five other premolars were attached to the orthodontic labial bar with composite adhesive. A difference in the healing process in relation to the type of fixation could not be determined clinically or radiographically.
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ACCEPTED MANUSCRIPT Clinical parameters The clinical parameters are summarized in Table 2 for each transplant. The periodontal examination of the transplants revealed an average PSI of 1.2 in the follow-up observation period (min.: 0; max.: 3). A 6-point measurement of
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the pocket depths revealed an average pocket depth of 1.9 mm (min.: 1; max.: 3) and was thus in the physiological range for all transplants.
The clinical degree of mobility of the transplants showed a degree of mobility
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of I in five transplants and a degree of mobility of 0 in 21 transplants.
In the course of the follow-up observations, there was a tendency towards a
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decrease of the percussion sensitivity. In the clinical follow-up controls after 3 months, a percussion sensitivity could be determined in 19 teeth (73%). Only 4 of the transplants (15.4%) showed a sensitivity after 9 months. After 12 months, no percussion sensitivity could be determined in any of the
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transplants (0%). All teeth showed positive periotest values (min.: 2; max.: 19; mean: 8) and no metallic percussion sound, assuming a physiological
Pulpal healing
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healing of the periodontal ligament and no ankylosis of the transplants.
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Pulpal healing was evaluated by the clinical sensitivity measurement and recording of pulp canal obliteration (Table 2). A positive reaction sensitivity was found at the last follow-up observation time point in 18 of the 26 transplants (69.2%). A pulp canal obliteration was found in 12 teeth. Whereas the six transplants with partial pulp canal obliteration showed positive reaction to sensitivity measurement, there was no clinical sensitivity found at the six transplants with total obliteration. It is therefore assumed that 13
ACCEPTED MANUSCRIPT pulp healing occurred in 69.2% of cases. Eight teeth showed pulp necrosis with root resorptions leading to endodontic treatment in the further course. All these teeth belonged to the group of transplants with root development
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stage ≥ 12 according to Moorrees et al. (23) (Fig. 7).
Soft tissue level
Compared to the adjacent teeth, the relative soft tissue level revealed a
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statistically significant increase of 1.1 mm ± 0.3 (min.: 0.5 mm; max.: 4 mm) over the follow-up observation period (Fig. 3). The average value of the
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mesial and distal measurements of the soft tissue heights showed a tendency to increase 6 months postoperatively. 24 months postoperatively, a significant increase of soft tissue levels compared to the adjacent teeth (p≤0.01) was noted. Although transplants after orthodontic therapy showed a
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slightly higher mean value no significant difference could be evaluated for soft tissue levels of transplants with orthodontic therapy and teeth without
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orthodontic therapy after transplantation (Fig. 5).
Radiographic parameters
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Bone level
The mesial bone level increased by 1.5 ± 0.6 mm on average (min.: 0.2 mm; max.: 9.5 mm) during the follow-up period (Fig. 4A); accordingly, the distal bone level increased by 1.0 ± 0.5 mm on average (min.: 0.2 mm; max.: 7.6 mm) (Fig. 4B). On average, a vertical bone gain of 1.2 ± 0.4 mm was observed. Figures 4A and 4B indicate the adequate co-development of bone height compared to the healthy adjacent teeth. In comparison between 14
ACCEPTED MANUSCRIPT transplants with or without orthodontic therapy no significant difference of relative bone levels could be identified (Fig. 5).
Root length and development
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The changes in the root lengths over the follow-up observation period are shown in Figure 6. The changes in root length are specified as relative length
changes of the original length in %. A tendency towards an increase in root
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length from the 12th to the 36th month was found so that a further progress in
root development can be assumed. The average root length of transplants
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was 16.8 mm (min: 12.5 mm; max: 21.5 mm). On 18 teeth, an increase in root length was observed postoperatively (69.2%), which was 1.5 ± 0.2 mm on average.
All transplants showed a root development stage in the postoperative
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radiographs where more than half of the root was mineralised. Eight transplants (31%) showed a half closed apical foramen and ten teeth (38%) showed a closed apical foramen, which was partly due to the late
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presentation of patients. In summary, it can be concluded that only one transplantation was performed within the ideal time window, whereas 96% of
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transplantations (n=25) were performed with completed rooth lengths (stage ≥12 according to Moorrees). Figure 7 depicts the occurence of root resorptions within the follow-up.
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ACCEPTED MANUSCRIPT Complications Discolouration of the transplants was not observed in any of the cases. One transplant evolved a carious lesion, which was treated with a composite filling.
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According to the classification of Andreasen et al. (34) eight transplants
showed a root resorption in the follow-up examinations. None of the
transplants showed replacement resorption with ankylosis. Eight infection-
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related root resorptions were identified. In a causal relation teeth that had
been transplanted with a closed apex showed significantly more resorptions
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(p=0.03) than teeth with a lower root development. Seven of the eight resorptions occurred in transplants with already closed apical foramina (Figure 7). One resorption occurred after the transplant suffered from a renewed dental trauma. This tooth was excluded from the non-successful
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group. Radiographic findings also revealed two cases of healing-related surface resorptions without a need for endodontic intervention. An endodontic therapy with calcium hydroxide was performed as clinical
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treatment as soon as an infection-related root resorption was identified. All transplants with an apical osteolysis, showed regeneration of the
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surrounding bone in the further follow-up. The root canal treated teeth showed no difference to the non-root canal-treated transplants in regards to soft and hard tissue development.
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Discussion Premolar transplantation has been suggested as a proven therapeutic alternative of tooth replacement if orthodontic gap closure in the juvenile dentition is not possible. The technique has been shown to co-develop the
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alveolar process after tooth trauma or aplasia until its completion of jaw growth (39). The reliability of this method is reflected by the excellent survival
rates published in the literature. In this study the survival rate of premolar
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transplants was 100% over an average follow-up period of 29 months, thus correlating well with the earlier success and survival rates reported by others
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(14, 28, 40).
Radiographic evaluation of bone healing after transplantation of third molars was described by Waikakul et al. (11). The authors observed a statistically significant bone formation in the first three months postoperatively, as well as
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the formation of a lamina dura. In the literature bone development after premolar transplantation has so far only been assumed in several case reports (41-43). A quantitative measurement and demonstration of vertical
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bone formation in the anterior maxilla after TDI or tooth aplasia has so far not
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been performed in the literature so far. This study provides first quantitative data on the co-development of peritransplant tissues in comparison to the adjacent healthy teeth after premolar transplantation. The horizontal curves of relative bone level compared to the adjacent teeth (Fig. 4) indicate the adequate stimulation of bone growth in the trauma or aplasia affected jaw section. Thus, premolar transplantation is likely to stimulate jaw growth in the affected regions, as a
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ACCEPTED MANUSCRIPT mean plus of relative bone height of +1.2 mm was observed compared to the adjacent dentition. The stimulation of bone growth may be attributed to the osteoinductive effect of the transplants in combination with the orthodontic extrusion therapy.
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Through the formation of a physiological periodontal gap, the orthodontic tension via the periodontal fibres induces a three-dimensional augmentation of the affected local alveolar bone. This has already been clinically applied in
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teeth worthy of being extracted by extrusion therapy prior to implantation (44, 45). The extrusive force activates angiogenetic factors, which lead to the
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reconstruction of the periodontal fibres. Subsequently, the induced increase in osteoblast function results in the formation of new bone (46, 47). To differentiate the effects of orthodontic extrusion and proliferative effect of the transplantation, a correlation between the transplants with and without
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orthodontic extrusion was made. Figure 5 shows an equivalent mesial and distal bone level in both groups implying an osteoinductive effect of the transplants. Also for soft tissue levels no significant differences could be
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detected between the groups.
In a recent study, we have examined the relative bone height after primary
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canine transplantion in children's and juvenile dentition without orthodontic treatment. Also here, a reliable development of vertical bone could be detected (31), suggesting the osteoinductive potential of the transplants to be responsible for the osteoinductive effects. The osteoinductive potential of the transplants overcame even extreme cases of vertical bony growth deficits of more than -4 mm as demonstrated in the clinical case reported (Figure 9). 18
ACCEPTED MANUSCRIPT Vertical bone gain is narrowly associated with soft tissue augmentation, leading to a broadening of the keratinised gingiva (48). This study showed a statistically significant soft tissue increase compared to the adjacent teeth (Fig. 3). Over the entire observation period, the transplants showed a relative
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soft tissue gain of +1.1 mm, which correlates well with the gain in bone
height. Tschammler et al. (31) showed an increase of +3.4 mm in the soft tissue level during the follow-up period after primary canine transplantation in
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the anterior maxilla. In addition, a tendency to hyperplastic gingiva growth
after premolar transplantation has been described in the literature (21). The
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results of this study support this observation with quantitative data.
Increases of root length after transplantation (average 1.5 mm) could be observed on 18 teeth (69.2%) in this study (Figure 6). This correlates well with the results of other studies. Paulsen et al. showed an arrested root
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development after premolar transplantation at 19% of the teeth, a complete root development at 26%, and in 55% of the transplants a progressive, but limited growth (32). Andreasen et al. published similar results and showed
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that the arrest of root development is significantly correlated with a too early root development stage for transplantation (49). This has been attributed to
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the separation or trauma of the Hertwig's epithelial root sheath (50). Signs of pulpal healing were found in 18 (69.2%) transplants. Andreasen et al. reported a rate of pulpal healing for transplants with partial root development of 96% and 15% for teeth transplanted with complete root formation (17). In the literature, a root development stage of 11 is specified as favourable according to Moorrees et al. (23) (Table 3), since an atraumatic extraction is possible and an open apical foramen is still present 19
ACCEPTED MANUSCRIPT facilitating the revascularisation of the transplant (17). The premolars transplanted in this study showed root development stages between 11 and 14 according to Moorrees et al., which is likely to be responsible for the lower rate of pulpal healing and also for the higher incidence of infection-related
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root resorptions. The correlation between root development stage and incidence of root resorptions (p=0.03) confirms this causal relationship
(Figure 7). This underlies the importance of root development and the ideal
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timing for autotransplantations to reduce complications in the form of root resorptions.
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In conclusion, autogenous premolar transplantation represents a reliable and biologically effective method of tooth replacement in the later mixed dentition. This study provides first quantitative evidence of the osteoinductive and soft tissue inductive effects of this technique. Especially in tooth aplasia or TDI,
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where tissue deficits are common, the development of the surrounding bone and soft tissue by this surgical technique can reliably be expected. The technique should be preferred as alternative therapy to other tooth
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replacement measures such as the Maryland bridge or a later planned implantation in those cases in which orthodontic gap closure is technically not
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possible.
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Acknowledgements
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We would like to thank Dr. Christian Kuffer for his statistical support.
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References
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1. Andreasen JO, Andreasen FM, Andersson L, Andreasen JO. Textbook and color atlas of traumatic injuries to the teeth. 4th ed. Oxford, UK ; Ames, Iowa: Blackwell Munksgaard; 2007. xiv, 897 p. p. 2. Borum MK, Andreasen JO. Therapeutic and economic implications of traumatic dental injuries in Denmark: an estimate based on 7549 patients treated at a major trauma centre. International journal of paediatric dentistry / the British Paedodontic Society [and] the International Association of Dentistry for Children. 2001;11(4):249-58. 3. Nimcenko T, Omerca G, Varinauskas V, Bramanti E, Signorino F, Cicciu M. Tooth autotransplantation as an alternative treatment option: A literature review. Dental research journal. 2013;10(1):1-6. 4. Sugerman PB, Barber MT. Patient selection for endosseous dental implants: oral and systemic considerations. The International journal of oral & maxillofacial implants. 2002;17(2):191-201. 5. Kavadia S, Papadiochou S, Papadiochos I, Zafiriadis L. Agenesis of maxillary lateral incisors: a global overview of the clinical problem. Orthodontics : the art and practice of dentofacial enhancement. 2011;12(4):296-317. 6. Stenvik A, Zachrisson BU. Orthodontic closure and transplantation in the treatment of missing anterior teeth. An overview. Endodontics & dental traumatology. 1993;9(2):45-52. 7. Rodd HD, Barker C, Baker SR, Marshman Z, Robinson PG. Social judgements made by children in relation to visible incisor trauma. Dental traumatology : official publication of International Association for Dental Traumatology. 2010;26(1):2-8. 8. Oka AE, N'Cho KJ, Bakayoko-Ly R. [Replacement of deciduous incisors in children: psychological aspects]. Odonto-stomatologie tropicale = Tropical dental journal. 2003;26(102):30-6. 9. Andreasen JO, Schwartz O, Kofoed T, Daugaard-Jensen J. Transplantation of premolars as an approach for replacing avulsed teeth. Pediatric dentistry. 2009;31(2):129-32. 10. Tsukiboshi M. Autotransplantation of teeth: requirements for predictable success. Dental traumatology : official publication of International Association for Dental Traumatology. 2002;18(4):157-80. 11. Waikakul A, Punwutikorn J, Kasetsuwan J, Korsuwannawong S. Alveolar bone changes in autogenous tooth transplantation. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2011;111(3):e1-7. 12. Slagsvold O, Bjercke B. Autotransplantation of premolars with partly formed roots. A radiographic study of root growth. American journal of orthodontics. 1974;66(4):355-66. 13. Slagsvold O, Bjercke B. Applicability of autotransplantation in cases of missing upper anterior teeth. American journal of orthodontics. 1978;74(4):410-21. 14. Kugelberg R, Tegsjo U, Malmgren O. Autotransplantation of 45 teeth to the upper incisor region in adolescents. Swedish dental journal. 1994;18(5):165-72. 15. Kristerson L, Lagerstrom L. Autotransplantation of teeth in cases with agenesis or traumatic loss of maxillary incisors. European journal of orthodontics. 1991;13(6):486-92. 16. Lundberg T, Isaksson S. A clinical follow-up study of 278 autotransplanted teeth. The British journal of oral & maxillofacial surgery. 1996;34(2):181-5. 17. Andreasen JO, Paulsen HU, Yu Z, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars. Part II. Tooth survival and pulp healing subsequent to transplantation. European journal of orthodontics. 1990;12(1):14-24. 18. Czochrowska EM, Stenvik A, Bjercke B, Zachrisson BU. Outcome of tooth transplantation: survival and success rates 17-41 years posttreatment. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2002;121(2):110-9; quiz 93.
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19. Gilijamse M, Baart JA, Wolff J, Sandor GK, Forouzanfar T. Tooth autotransplantation in the anterior maxilla and mandible: retrospective results in young patients. Oral Surg Oral Med Oral Pathol Oral Radiol. 2016; 122(6): e187-e192. 20. Czochrowska EM, Stenvik A, Album B, Zachrisson BU. Autotransplantation of premolars to replace maxillary incisors: a comparison with natural incisors. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2000;118(6):592-600. 21. Czochrowska EM, Stenvik A, Zachrisson BU. The esthetic outcome of autotransplanted premolars replacing maxillary incisors. Dental traumatology : official publication of International Association for Dental Traumatology. 2002;18(5):237-45. 22. Andreasen JO, Paulsen HU, Yu Z, Ahlquist R, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars. Part I. Surgical procedures and standardized techniques for monitoring healing. European journal of orthodontics. 1990;12(1):3-13. 23. Moorrees CF, Fanning EA, Hunt EE, Jr. Age Variation of Formation Stages for Ten Permanent Teeth. Journal of dental research. 1963;42:1490-502. 24. Kristerson L. Autotransplantation of human premolars. A clinical and radiographic study of 100 teeth. International journal of oral surgery. 1985;14(2):200-13. 25. Jonsson T, Sigurdsson TJ. Autotransplantation of premolars to premolar sites. A long-term follow-up study of 40 consecutive patients. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2004;125(6):668-75. 26. Watanabe Y, Mohri T, Takeyama M, Yamaki M, Okiji T, Saito C, et al. Long-term observation of autotransplanted teeth with complete root formation in orthodontic patients. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2010;138(6):720-6. 27. Zachrisson BU, Stenvik A, Haanaes HR. Management of missing maxillary anterior teeth with emphasis on autotransplantation. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2004;126(3):284-8. 28. Plakwicz P, Wojtowicz A, Czochrowska EM. Survival and success rates of autotransplanted premolars: a prospective study of the protocol for developing teeth. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2013;144(2):229-37. 29. Pohl Y, Filippi A, Kirschner H. Results after replantation of avulsed permanent teeth. II. Periodontal healing and the role of physiologic storage and antiresorptive-regenerative therapy. Dental traumatology : official publication of International Association for Dental Traumatology. 2005;21(2):93-101. 30. Huth KC, Nazet M, Paschos E, Linsenmann R, Hickel R, Nolte D. Autotransplantation and surgical uprighting of impacted or retained teeth: A retrospective clinical study and evaluation of patient satisfaction. Acta odontologica Scandinavica. 2013;71(6):1538-46. 31. Tschammler C, Angermair J, Heiligensetzer M, Linsenmann R, Huth KC, Nolte D. Primary canine auto-transplantation: a new surgical technique. Oral surgery, oral medicine, oral pathology and oral radiology. 2015;119(2):158-69. 32. Paulsen HU, Andreasen JO, Schwartz O. Pulp and periodontal healing, root development and root resorption subsequent to transplantation and orthodontic rotation: a long-term study of autotransplanted premolars. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 1995;108(6):630-40. 33. Andreasen FM, Andreasen JO. Diagnosis of luxation injuries: the importance of standardized clinical, radiographic and photographic techniques in clinical investigations. Endodontics & dental traumatology. 1985;1(5):160-9. 23
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34. Andreasen JO, Hjorting-Hansen E. Replantation of teeth. I. Radiographic and clinical study of 110 human teeth replanted after accidental loss. Acta odontologica Scandinavica. 1966;24(3):263-86. 35. Paschos E, Huth KC, Fassler H, Rudzki-Janson I. Investigation of maxillary tooth sizes in patients with palatal canine displacement. Journal of orofacial orthopedics = Fortschritte der Kieferorthopadie : Organ/official journal Deutsche Gesellschaft fur Kieferorthopadie. 2005;66(4):28898. 36. Linge L, Linge BO. Patient characteristics and treatment variables associated with apical root resorption during orthodontic treatment. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 1991;99(1):35-43. 37. Houston WJ. The analysis of errors in orthodontic measurements. American journal of orthodontics. 1983;83(5):382-90. 38. Dahlberg G. Statistical methods for medical and biological students. London,: G. Allen & Unwin ltd.; 1940. 3 p. l., 9 -232 p. p. 39. Schwartz-Arad D, Levin L, Ashkenazi M. Treatment options of untreatable traumatized anterior maxillary teeth for future use of dental implantation. Implant dentistry. 2004;13(2):120-8. 40. Plakwicz P, Czochrowska EM. The prospective study of autotransplanted severely impacted developing premolars: periodontal status and the long-term outcome. Journal of clinical periodontology. 2014;41(5):489-96. 41. Plakwicz P, Czochrowska EM, Milczarek A, Zadurska M. Vertical bone growth following autotransplantation of the developing maxillary third molar to replace a retained mandibular permanent molar: a case report. The International journal of periodontics & restorative dentistry. 2014;34(5):667-71. 42. Kim S, Lee SJ, Shin Y, Kim E. Vertical Bone Growth after Autotransplantation of Mature Third Molars: 2 Case Reports with Long-term Follow-up. Journal of endodontics. 2015;41(8):1371-4. 43. Hjortdal O, Bragelien J. [Induction of jaw bone formation by tooth autotransplantation]. Den Norske tannlaegeforenings tidende. 1978;88(7):319-22. 44. Brindis MA, Block MS. Orthodontic tooth extrusion to enhance soft tissue implant esthetics. Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons. 2009;67(11 Suppl):49-59. 45. Zuccati G, Bocchieri A. Implant site development by orthodontic extrusion of teeth with poor prognosis. Journal of clinical orthodontics : JCO. 2003;37(6):307-11; quiz 13. 46. Shiu YT, Weiss JA, Hoying JB, Iwamoto MN, Joung IS, Quam CT. The role of mechanical stresses in angiogenesis. Critical reviews in biomedical engineering. 2005;33(5):431-510. 47. de Molon RS, de Avila ED, de Souza JA, Nogueira AV, Cirelli CC, Margonar R, et al. Forced orthodontic eruption for augmentation of soft and hard tissue prior to implant placement. Contemporary clinical dentistry. 2013;4(2):243-7. 48. Salama H, Salama M. The role of orthodontic extrusive remodeling in the enhancement of soft and hard tissue profiles prior to implant placement: a systematic approach to the management of extraction site defects. The International journal of periodontics & restorative dentistry. 1993;13(4):312-33. 49. Andreasen JO, Paulsen HU, Yu Z, Bayer T. A long-term study of 370 autotransplanted premolars. Part IV. Root development subsequent to transplantation. European journal of orthodontics. 1990;12(1):38-50. 50. Andreasen JO, Kristerson L, Andreasen FM. Damage of the Hertwig's epithelial root sheath: effect upon root growth after autotransplantation of teeth in monkeys. Endodontics & dental traumatology. 1988;4(4):145-51.
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Legends of Tables and Figures Table 1: Distribution of transplants sorted by donor and recipient sites. The largest part of premolars was transplanted to the right central and left central incisor sites (n=17, 65%), four transplants replaced lateral incisors, and five
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transplants replaced canines.
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Table 2: Summary of the clinical and radiographic examination results.
Table 3: Stages of tooth development after Moorrees et al. (23).
according to Andreasen et al. (50).
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The black box indicates the ideal time window for premolar autotransplantation
Figure 1: Method for determination of the soft tissue level around transplants in the juvenile dentition as described in a previous study (31).
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The present case shows a 12-year-old patient after premolar transplantation of a mandibular second premolar to the position of the left central incisor with a soft tissue
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method section.
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level increase of +3 mm compared to the healthy adjacent tooth. For detail see
Figure 2: Schematic drawing for the measurement of relative bone height in the juvenile dentition according to Tschammler et al. (31). The example shows a vertical bone deficit of -2 mm as compared to the healthy adjacent tooth. For detail see method section.
25
ACCEPTED MANUSCRIPT Figure 3: Soft tissue levels around the transplants after premolar transplantation. The grey area represents one standard deviation (SD). The curve shows a significant increase in soft tissue levels compared to the adjacent healthy teeth (p<0.01) 24 months after transplantation.
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Statistics: One-way ANOVA with Bonferroni’s Multiple Comparison test.
Figure 4: Relative mesial (A) and distal (B) bone levels compared to the adjacent
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teeth.
The curves in both figures show constant profiles, implying a co-development of bone
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around the transplants compared to the healthy adjacent teeth.
Figure 5: Comparison between relative soft tissue and bone level values between patients with or without orthodontic treatment.
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Mean values revealed no significant differences between teeth with or without orthodontic treatment after transplantation.
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Figure 6: Relative root lengths of transplants in relation to postoperative root lengths. There is a tendency to an increase of the relative root lengths from 6 months
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postoperatively, indicating a sustained root growth after transplantation (N=20; n=26).
Figure 7: Occurrence of root resorption within the follow-up period. A) Kaplan-Meier curve indicates that most root resorptions were identified within the first year. B) Bar graph depicts root resorption in percent dependent of the root development stage according to Moorees et al. (23). All root resorptions occurred in teeth with root development stage ≥13. Statistics: Chi-Square test. 26
ACCEPTED MANUSCRIPT Figure 8: Clinical case of premolar auto-TX in a 12-year-old girl after replantation of the avulsed central right incisor with posttraumatic ankylosis. (A): Due to progressive resorption with vertical growth inhibition compared to the adjacent tooth, the traumatized incisor had to be removed and replaced by transplantation of the upper
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right second premolar (B). The elimination of the vertical deficit through the induced growth of the hard and soft tissues in the follow-up period of 3.5 years can clearly be
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seen (C). The dental composite structure yielded a very good aesthetic result (D, E).
Figure 8 A: Radiographic and clinical view after replantation of the traumatized
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central right incisor with ensuing signs of ankylosis, rooth resorption and discoloration.
Figure 8 B: Intraoperative situation revealing progressive apical root resorption and a
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vertical bony deficit.
Figure 8 C: Radiographic and clinical postoperative findings after premolar
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transplantation. The transplant had to be inserted in about 5 mm infraposition due to
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the lack of adequate soft tissue coverage.
Figure 8 D: Radiographic and clinical findings one year after transplantation. The tooth crown has been constructed in composite adhesive technique. Orthodontic extrusion of the transplant led to a co-development of both bone and surrounding soft tissues. The former gingival deficit of about 5 mm has completely been compensated.
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ACCEPTED MANUSCRIPT Figure 8 E: Radiographic and clinical findings 3.5 years after transplantation. After orthodontic treatment the transplant shows an excellent aesthetic view with a soft-tissue plus of approximately +1 mm. Root obliteration of the transplant is visible
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Recipient region Right upper quadrant Left upper quadrant Canine Incisors Incisors Canine
Donor region
Mandible
n = 20 First premolar
Second premolar
Sum %
-
Lateral -
Central -
Central -
Lateral -
-
Sum 0
% 0.0
Left upper quadrant
-
-
-
-
-
-
0
0.0
Right upper quadrant
-
-
4
-
-
-
4
15.4
Left upper quadrant
-
-
1
1
-
-
2
7.7
Right lower quadrant
-
2
-
-
-
1
3
11.5
Left lower quadrant
2
-
Right lower quadrant
1
-
Left lower quadrant
-
-
3
2
11.5
7.7
1
1
2
-
6
23.0
4
1
-
1
7
26.9
-
4
-
-
4
15.9
10
7
2
2
38.5
26.9
7.7
7.7
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Table 1: Distribution of transplants sorted by donor and recipient sites.
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Second premolar
Right upper quadrant
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First premolar
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n=6
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Maxilla
ACCEPTED MANUSCRIPT Table 2: Transplants 1
2
X
X
3
4
5
6
7
8
9
10
11
12
13
14
15
16
X
X
X
X
17
18
19
20
X
X
21
22
23
24
25
26
Sum
%
10
38.5
16
61.5
12
46.2
14
53.8
Mean
Reason for surgery X X
Traumatic loss
X
X
X
X
X
X
X
X
X
Gender Female
X
X
Male
Age of transplant (years)
X X
X
X
X
X
X
X
X
X
X X
X
X
X
X
X
X
17
12
12
11
11
11
13
19
19
14
14
12
11
12
14
17
17
12
12
11
11
13.3
0
0
0
7
n.d.
n.d.
7.4
6.4
1.3
1.3
4
0
0
0
0.2
1
0.5
2
2
14
n.d.
n.d.
0.3
n.d.
3
5
3
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
3
3
1
2
1
1
1
1
1
2
2
1
1
1
1
1
1
-
-
-
+
+ + +
+ + +
+
+
X
+
+
+
X
X
1
1
1
1
1
1
1
+ + +
+ + +
+ + +
+ + +
high Mobility of transplant X
X
X
X
X
X
X
X
X
X
Grade I 6
6
5
8
7
17
3
5
X
X
2
7
Endodontic treatment
X
X
Orthodontic treatment
X
X
X
X
X
X
X
Transplant modeling X
Crown/Veneer Composite core
X
X
X
X
X
X
X
X
1
1
1
1
1
1
1
1
1
+
+
+ + +
+ + +
+
X
+
X
X
X
X
X
Table 2: Summary of results of the clinical and radiographic examination.
3
4
X
19
X X
X
1
3
0
1
1
1
2
1
+
+
+
+
X
+
+
X
+
X
5
4
6
7
16
8
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X X
X
X X
19.2
14
53.8
1
1
1.2
1
1
1
1
1
1
1.1
+
+
+
+ + +
-
-
+
+
+
X 6
X X
X
19
13
9
+
X
+
X
8
6
X
X
X X
X X
5
1
X
X
X
X
X
69.2
10
38.5
26
100
26
100
0
0
21
80.8
5
19.2 8
23.1
6
23.1
X
8
30.7
X
22
84.6
3
11.5
7
26.9
16
61.5
X X
18
6
X X
3.9
1
X X
1
0
X X
76.9
X
X 9
20
X
X
AC C
X
partial
X
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X
X
X X
X
X
Pulp obliteration total
X
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Electrometry
+
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X
X
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Preparation of Neoalveolus
No change
X
17
X
Periotest
X
X
14
X
Grade 0
X
X
12
Bracket
normal
X
X
11
Suture splinting
Percussion test
X
X
11
Wire-composite splinting
Periodontal Screening Index Oral hygiene (1:good, 2:moderate) Cold sensibility
X
X
Surgical procedure Extraoral storage time (min)
X
X
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Aplasia
X
ACCEPTED MANUSCRIPT Explanation Initial calcification
2
Confluence of the cusps
3
Contour of the cusps complete
4
Crown formed to ½
5
Crown formed to ¾
6
Crown formed completely
7
Initial root formation
8
Initial formation of the bifurcation
9
Root length ¼
10
Root length ½
11
Root length ¾
12
Root length complete
13
Apex closed to ½
14
Apex closed completely
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1
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Stage
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Table 3: Stages of tooth development after Moorrees et al. (22).
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Soft Tissue Level
Relative Soft Tissue [mm]
5
n= 17
17
19
4
9
5
**
**
3
** = p < 0.01
2 1
Range of 1 SD 3 months after sugery
0 -1 -2 Baseline (n=21)
6
12
24
months post sugery
36
A
mesial
10
n= 20
19
22
22
8
8 6 4 2 0 -2 -4
10
n= 20
19
22
22
8
12
24
36
8 6 4 2 0 -2 -4 -6
-6 Baseline (n=26)
distal
B
Relative Bone Level [mm]
Relative Bone Level [mm]
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6
12
24
months post surgery
36
Baseline (n=26)
6
months post surgery
Mesial Bone Level 10
Bone Level [mm]
4 2 0 -2 -4
Bone Level [mm]
10 5 0 -5
Orthodontic treatment
5 0 -5
w ith
-10 w ith ou t
w ith
-10 w ith ou t
Soft tissue level [mm]
6
Distal Bone Level
Orthodontic treatment
w ith
Soft Tissue Level
w ith ou t
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Orthodontic treatment
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Relative Root Length [% of baseline value]
Relative Root Length n= 20 19 30
20
18
8
12
24
36
20 10 0 -10 -20 Baseline (n=26)
6
months post surgery
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Root Resorption
A
21
18
15
14
B 7
80
60
40
20
0 Baseline (n= 26)
n= 1
6
6 13
100 Percent of transplants
Percent root resorbtion
n= 25 100
80
no resorption resorption
60 40 20 0
6
12
24
months post surgery
36
11 12 13 14 Root Development Stage
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S2212-4403(17)30061-5
DOI:
10.1016/j.oooo.2017.02.002
Reference:
OOOO 1705
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 14 September 2016 Revised Date:
16 January 2017
Accepted Date: 13 February 2017
Please cite this article as: Michl I, Nolte D, Tschammler C, Kunkel M, Linsenmann R, Angermair J, Premolar autotransplantation in juvenile dentition: Quantitative assessment of vertical bone and soft tissue growth, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2017), doi: 10.1016/ j.oooo.2017.02.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Premolar autotransplantation in juvenile dentition: Quantitative assessment of vertical bone and soft tissue growth Inessa Michl, DMD
1, 2
, Dirk Nolte, MD, DMD, PhD
1, 2
, Claudia Tschammler, DMD
2
1
1, 3
, Martin 1
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Kunkel, MD, DMD, PhD , Robert Linsenmann, MD, DMD , Johannes Angermair, DMD
Running title: Premolar transplantation in juvenile dentition
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1. Private Practice for Oral and Maxillofacial Surgery, Sauerbruchstraße 48, 81377 Munich, Germany
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2. Ruhr-University of Bochum, Department of Oral & Maxillofacial Surgery, In der Schornau 23-25, 44892 Bochum, Germany
3. University of Goettingen, Department of Preventive Dentistry,
Periodontology and Cariology, Robert-Koch-Str. 40, 37075 Goettingen, Germany
Dirk Nolte, MD, DMD, PhD [email protected] Tel. +49-89/74 80 99 99
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Fax +49-89/74 00 91 35
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Correspondence:
Conflict of Interests: The authors have no financial interest to disclose.
Keywords:
Autogenous tooth transplantation; premolar transplantation; traumatic dental injury (TDI); tooth aplasia; pediatric dentistry; orthodontics
Word count abstract: 188, manuscript: 6520, number of references: 50, number of tables/figures: 15
1
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Abstract: Objective: Premolar autotransplantation represents an effective therapeutic option for the treatment of juvenile dentition with either aquired or congenital hypodontia. The objective of this prospective clinical study was to quantitatively assess bone
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and soft tissue levels after autogenous premolar transplantation by clinical and radiographic parameters.
Study Design: In the study 26 premolars were transplanted in 20 patients after
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traumatic tooth loss (n=16) or congenital aplasia (n=10) in the anterior maxilla. Based on standardized photographic documentation, the relative soft tissue level
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was measured in comparison to the healthy adjacent teeth. Radiographic findings included the evaluation of root resorption, pulp canal obliterations and the relative bone height.
Results: Average survival rate of transplanted premolars (n = 26) was 100% over
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a follow-up period of 29 months (range 10-60 months). The relative soft tissue level significantly increased by +1.1 mm (p<0.05). Radiographs showed the tendency to vertical bone growth. Continuous root development and signs of pulpal
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healing were observed postoperatively on 18 transplants (69.2%). Conclusions: Autogenous premolar transplantation represents a safe method to
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ensure functional and aesthetic rehabilitation in the anterior maxilla irrespective of the nature of tooth loss. ClinicalTrials.gov: NCT02740907
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Introduction Traumatic dental injury (TDI) to the upper anterior teeth represents a frequent injury in children and adolescents with a prevalence of up to 30%
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(1). According to previous studies, 7% to 8% of all accidents are associated with concomitant tooth loss (2). The practitioner faces a difficult task in the
clinical management of the resulting tooth gap in children aged 8-12 years
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since an implant as tooth replacement is not a treatment option during active jaw growth (3, 4).
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A similar situation is encountered in case of tooth aplasia of the maxillary incisors. According to Kavadia et al. the maxillary lateral incisor is the third most common aplastic tooth after the lower wisdom tooth and the mandibular second premolar (5).
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Orthodontic gap closure is the treatment of choice under favourable conditions. However, a symmetrical and aesthetically satisfying result cannot always be achieved with this method, especially in case of traumatic
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avulsion of the central incisors. In addition, the indication for an orthodontic gap closure is limited by the orthognathic situation of the dental arch in many
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cases (6). While treatment with composite-adhesive attached bridges represents a viable alternative, the underlying alveolar bone resorption may impede later dental implant placement. A tooth loss without adequate replacement in general leads to a psychological impairment of the children which can not be underestimated (7, 8). Premolar autotransplantation (auto-TX) represents a treatment option with an excellent long-term prognosis and reliable aesthetic results starting at the
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ACCEPTED MANUSCRIPT age of 10 (9). It is the only available technique that favorably affects the growth of the adolescent dentition due to its known potential to support soft tissue and bone development (3, 10, 11). In contrast to all other alternative therapies, vertical defects can be compensated during the adolescent growth
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period. This is the crucial advantage of premolar transplantation in cases of
trauma where vertical defects of the anterior upper jaw arise frequently. The
technique has already been described in 1960 by Slagsvold and Bjercke (12,
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13). In the literature, excellent average survival rates of > 90% in follow-up
observations up to 41 years have been published (14-19). In addition, long-
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term studies report no clinically or radiographically detectable difference of transplants compared to the adjacent teeth (20). The aesthetic result from the patients` and dentists` point of view is very satisfying and can be achieved by composite or ceramic restorations of the transplant after the
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healing period (21). Premolars are especially suited as transplants in the anterior maxillary region because they often have to be extracted for orthodontic reasons and, due to their root morphology, an atraumatic
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extraction is technically feasible (22).
The ideal root development for transplantation is proposed in the literature at
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the age of about 10 years with an open apex and with a root length of ¾ (growth stage 11 according to Moorrees et al.) (23). The reason therefore is that the regeneration of the periodontal ligament and the revascularisation of the transplant is the greatest during this growth period (24-26). The indication for premolar transplantation must always be made in close consultation with the orthodontist. In cases of malocclusion, in which a compensation extraction is planned, a win-win situation can arise (27, 28). 4
ACCEPTED MANUSCRIPT To the best of our knowledge, there has been no scientific study which has quantitatively assessed the inductive potency of premolar transplantation on both soft tissue and bone growth. The objective of this prospective clinical case study was therefore to quantitatively assess the vertical changes of the
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adolescents following premolar transplantation.
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peri-transplant tissues in the maxillary anterior region in children and
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Materials and Methods Subjects In 20 patients 26 premolar transplantations were performed from 2006 to 2014 to replace the maxillary incisors (mean age 13.6, females: 10, males:
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10). Thirteen patients suffered from traumatic dental injury (TDI) with
subsequent tooth loss (n=16 transplants). In 7 patients, aplasia of teeth in
the maxillary anterior region from right canine to left canine was present
regard to donor and recipient regions.
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(n=10 transplants). Table 1 shows the distribution of the transplants with
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The choice of transplant selection was planned in close cooperation with the orthodontist.
The guidelines of this study have followed the Declaration of Helsinki. The study was approved by the ethics committee of the Bavarian Medical
Surgical procedure
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Association of Munich, No. 13116/2013.
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All patients were preoperatively informed about therapeutic alternatives to
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the planned intervention as well as risks and chances of success. The following procedures were undertaken with the understanding and written consent of each patient. All procedures were performed under short general anaesthesia. The teeth to be transplanted were gently extracted with anatomical forceps and stored in a nutrient solution for preservation of the periodontal ligament based on the concept of anti-resorptive therapy (29). The tooth storing solution consisted of 100 mg doxycycline, 4 mg dexamethasone and 10 ml of physiological saline. Teeth transplanted 6
ACCEPTED MANUSCRIPT without intermediate storage in the nutrient solution, had a storage or ischemic time of zero minutes (see Table 2). The transplant bed was prepared with a surgical bur (Surgery TC-Cutter, Acurata medica, Thurmansbang, Germany) as atraumatically as possible, preferably using a
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tunneling preparation technique. The transplants were inserted in orthograde
position with anatomical tweezers without injuring the root surface. All teeth were conditioned using an enamel etching technique and flexibly fixed for 3
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weeks with a titanium trauma splint (TTS, Medartis, Basel, Switzerland) and
composite (Syntac Classic, Tetric Evo Flow, Ivoclar Vivadent, Schaan,
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Lichtenstein). If an orthodontic arch wire was present, then the teeth were fixed in a flexible manner to the available wire. Wound closure was performed using modified backstitch sutures. Patients greater than 12 years of age were prescribed systemic antibiotics using doxycycline 100 mg per
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day (100 mg/d, Doxycyclin AL, Aliud Pharma®, Laichingen, Germany) for 7 days as an antiresorptive therapy (29) intra- and postoperatively as well as soft diet for 3-4 days under continuation of daily oral hygiene. The first
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wound control took place on the first post-operative day. Sutures were removed on day seven. The splinting was removed after three weeks and
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the tooth surfaces were polished and fluoridated. This was followed by an appointment at the orthodontist for the integration of the transplant into the multibracket appliance. Recall visits included clinical and radiographic controls after 3, 6, 9, and 12 months. The patients were then seen at yearly intervals for follow-up care.
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ACCEPTED MANUSCRIPT Clinical follow-up The clinical follow-up included the evaluation of the periodontal status, percussion sensitivity and sensibility of the transplants. The approach applied is similar to that from previous studies of our group
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(30, 31). Oral hygiene and periodontal status of the transplants were
determined using the Peridontal Screening Index (PSI) and a pocket depth measurement. The percussion sensitivity was clinically identified to help
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determine a physiological percussion and to identify ankylosis. In addition, a quantitative measurement of the tooth mobility was carried out clinically and
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with the periotest device (Periotest Classic; Medizintechnik Gulden, Modautal, Germany).
The vitality of the teeth was tested by sensitivity control using a cold spray and by electric pulse technique (Vitality Scanner; SybronEndo, Orange, CA,
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USA). Radiographic analysis was performed in regard to partial and total pulp canal obliteration. Pulp canal obliteration was considered as physiological response of the transplant to trauma and thus as vital sign of
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pulpal healing (32, 33).
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ACCEPTED MANUSCRIPT Soft tissue level The soft tissue level measurement was carried out on the basis of a standardized photographic documentation. The procedure was performed analogously to a previously published study in which the technique of vertical
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soft tissue measurements in the growing dentition was described (31): a
central photograph of the anterior maxillary region was chosen as reference. As shown in Figure 1, a vertical line was drawn through the middle of the
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transplant parallel to the tooth axis. In addition, an orthogonal was created
tangentially to the gingival margin. This line yields the relative level of soft
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tissue compared to the healthy neighbouring tooth. The scaling in mm was calculated using the rule of three from the crown lengths measured in vivo (Figure 1).
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Radiographic follow-up
The relevant parameters were determined using orthopantomography. This radiographic technique was used as standard diagnostics to allow
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reproducibility of the measured bone and root lengths. Dental films were used for a more accurate diagnostics of the root surfaces. Pulp canal
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obliterations, the change in the length of the transplants` roots, factors of bone healing and root resorptions were determined. Root resorptions were classified and documented according to Andreasen et al. (34). The mineralisation stages of the root development were determined according to Moorrees et al. (23) in order to correlate the stage of root development versus occurrence of root resorptions (Table 3).
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ACCEPTED MANUSCRIPT Bone level The bone height in the growing dentition was determined in relation to the adjacent teeth as previously described (31). For this, a connecting line was drawn on the x-ray between the mesial cementoenamel junction of the distal
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adjacent tooth and the distal cementoenamel junction of the mesial adjacent tooth (Figure 2). Starting from this line, a perpendicular was drawn to the
most distant point of the alveolar ridge both mesially and distally and the
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length of this line was measured. All measured values lying coronally to line
A were marked with a positive sign, all those lying apically with a negative
distances was calculated (Fig. 2).
Determination of root length
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sign. For final data generation, the average between the mesial and distal
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The root length of the transplants was determined by the distance between two lines. The first line was constructed by connecting the two most apical points of the root tip, while the second line was a connection of the mesial
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and distal cementoenamel junction of the tooth (31, 35). To enable the comparability of measured lengths on the different radiographic images, a
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magnification factor was calculated from the quotient of postoperative crown length and crown length at the follow-up time (36). The measured root length of the follow-up image was multiplied by the magnification factor and then subtracted from the postoperatively measured initial length. Measurement errors were levelled by repeated measurement according to a time interval. Houston’s reliability coefficient and Dahlberg’s Formula were used to
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ACCEPTED MANUSCRIPT evaluate the error of measurement (37, 38). The overall values were ≥0.95, therefore an acceptable accuray was reached.
Transplant Survival and Success
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Transplant survival and success were assessed in the follow-up intervals.
The success criteria were based on a previous study of our group (30): Clinical success criteria were PSI under 3, tooth mobility less than II and no
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the transplant and the absence of root resorptions.
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percussion sensitivity. Radiographic criteria were bony regeneration arround
Statistical analysis
The statistical analysis was performed using Excel 2010 (Microsoft Corp., Redmond, WA, United States) and Prism (GraphPad Software, La Jolla, CA,
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USA). For parametrically distributed data, a dependent t-test was conducted and for non-parametrically distributed data, a Wilcoxon test was applied. The
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significance level was set at p<0.05.
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Results Transplant survival and success 26 premolar transplants were performed in the anterior maxillary for tooth replacement after tooth aplasia (n=10) or previous TDI (n=16) in 20 patients
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(N=20; n=26). There were 14 males and 12 females and their ages ranged
from 11 to 19 years of age. The survival rate of the transplants was 100% over an average follow-up observation period of 29 months (min.: 10 months;
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max.: 60 months). Since all transplants were clinically free from irritation, no
limitation of success was given with regard to tooth mobility and periodontal
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conditions. In 8 of the 26 transplants, a resorption was present. Since one resorption occurred after a renewed trauma, the transplant was excluded from the non-successful group yielding a success rate of 73%. All other
Surgical parameters
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conditions of success have been met.
The average ischemia time during transplantation was 3 min (min: 0; max.:
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17) (Table 2). 15 transplants were temporarily stored in the above described
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nutrient solution, whereas 6 transplants were directly positioned in the recipient region. In 5 cases, there were no data regarding the ischemia time. After transplantation, 20 transplants were splinted by wire-composite fixation. One premolar was solely stabilized by a backstitch suture, five other premolars were attached to the orthodontic labial bar with composite adhesive. A difference in the healing process in relation to the type of fixation could not be determined clinically or radiographically.
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ACCEPTED MANUSCRIPT Clinical parameters The clinical parameters are summarized in Table 2 for each transplant. The periodontal examination of the transplants revealed an average PSI of 1.2 in the follow-up observation period (min.: 0; max.: 3). A 6-point measurement of
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the pocket depths revealed an average pocket depth of 1.9 mm (min.: 1; max.: 3) and was thus in the physiological range for all transplants.
The clinical degree of mobility of the transplants showed a degree of mobility
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of I in five transplants and a degree of mobility of 0 in 21 transplants.
In the course of the follow-up observations, there was a tendency towards a
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decrease of the percussion sensitivity. In the clinical follow-up controls after 3 months, a percussion sensitivity could be determined in 19 teeth (73%). Only 4 of the transplants (15.4%) showed a sensitivity after 9 months. After 12 months, no percussion sensitivity could be determined in any of the
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transplants (0%). All teeth showed positive periotest values (min.: 2; max.: 19; mean: 8) and no metallic percussion sound, assuming a physiological
Pulpal healing
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healing of the periodontal ligament and no ankylosis of the transplants.
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Pulpal healing was evaluated by the clinical sensitivity measurement and recording of pulp canal obliteration (Table 2). A positive reaction sensitivity was found at the last follow-up observation time point in 18 of the 26 transplants (69.2%). A pulp canal obliteration was found in 12 teeth. Whereas the six transplants with partial pulp canal obliteration showed positive reaction to sensitivity measurement, there was no clinical sensitivity found at the six transplants with total obliteration. It is therefore assumed that 13
ACCEPTED MANUSCRIPT pulp healing occurred in 69.2% of cases. Eight teeth showed pulp necrosis with root resorptions leading to endodontic treatment in the further course. All these teeth belonged to the group of transplants with root development
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stage ≥ 12 according to Moorrees et al. (23) (Fig. 7).
Soft tissue level
Compared to the adjacent teeth, the relative soft tissue level revealed a
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statistically significant increase of 1.1 mm ± 0.3 (min.: 0.5 mm; max.: 4 mm) over the follow-up observation period (Fig. 3). The average value of the
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mesial and distal measurements of the soft tissue heights showed a tendency to increase 6 months postoperatively. 24 months postoperatively, a significant increase of soft tissue levels compared to the adjacent teeth (p≤0.01) was noted. Although transplants after orthodontic therapy showed a
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slightly higher mean value no significant difference could be evaluated for soft tissue levels of transplants with orthodontic therapy and teeth without
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orthodontic therapy after transplantation (Fig. 5).
Radiographic parameters
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Bone level
The mesial bone level increased by 1.5 ± 0.6 mm on average (min.: 0.2 mm; max.: 9.5 mm) during the follow-up period (Fig. 4A); accordingly, the distal bone level increased by 1.0 ± 0.5 mm on average (min.: 0.2 mm; max.: 7.6 mm) (Fig. 4B). On average, a vertical bone gain of 1.2 ± 0.4 mm was observed. Figures 4A and 4B indicate the adequate co-development of bone height compared to the healthy adjacent teeth. In comparison between 14
ACCEPTED MANUSCRIPT transplants with or without orthodontic therapy no significant difference of relative bone levels could be identified (Fig. 5).
Root length and development
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The changes in the root lengths over the follow-up observation period are shown in Figure 6. The changes in root length are specified as relative length
changes of the original length in %. A tendency towards an increase in root
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length from the 12th to the 36th month was found so that a further progress in
root development can be assumed. The average root length of transplants
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was 16.8 mm (min: 12.5 mm; max: 21.5 mm). On 18 teeth, an increase in root length was observed postoperatively (69.2%), which was 1.5 ± 0.2 mm on average.
All transplants showed a root development stage in the postoperative
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radiographs where more than half of the root was mineralised. Eight transplants (31%) showed a half closed apical foramen and ten teeth (38%) showed a closed apical foramen, which was partly due to the late
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presentation of patients. In summary, it can be concluded that only one transplantation was performed within the ideal time window, whereas 96% of
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transplantations (n=25) were performed with completed rooth lengths (stage ≥12 according to Moorrees). Figure 7 depicts the occurence of root resorptions within the follow-up.
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ACCEPTED MANUSCRIPT Complications Discolouration of the transplants was not observed in any of the cases. One transplant evolved a carious lesion, which was treated with a composite filling.
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According to the classification of Andreasen et al. (34) eight transplants
showed a root resorption in the follow-up examinations. None of the
transplants showed replacement resorption with ankylosis. Eight infection-
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related root resorptions were identified. In a causal relation teeth that had
been transplanted with a closed apex showed significantly more resorptions
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(p=0.03) than teeth with a lower root development. Seven of the eight resorptions occurred in transplants with already closed apical foramina (Figure 7). One resorption occurred after the transplant suffered from a renewed dental trauma. This tooth was excluded from the non-successful
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group. Radiographic findings also revealed two cases of healing-related surface resorptions without a need for endodontic intervention. An endodontic therapy with calcium hydroxide was performed as clinical
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treatment as soon as an infection-related root resorption was identified. All transplants with an apical osteolysis, showed regeneration of the
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surrounding bone in the further follow-up. The root canal treated teeth showed no difference to the non-root canal-treated transplants in regards to soft and hard tissue development.
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Discussion Premolar transplantation has been suggested as a proven therapeutic alternative of tooth replacement if orthodontic gap closure in the juvenile dentition is not possible. The technique has been shown to co-develop the
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alveolar process after tooth trauma or aplasia until its completion of jaw growth (39). The reliability of this method is reflected by the excellent survival
rates published in the literature. In this study the survival rate of premolar
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transplants was 100% over an average follow-up period of 29 months, thus correlating well with the earlier success and survival rates reported by others
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(14, 28, 40).
Radiographic evaluation of bone healing after transplantation of third molars was described by Waikakul et al. (11). The authors observed a statistically significant bone formation in the first three months postoperatively, as well as
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the formation of a lamina dura. In the literature bone development after premolar transplantation has so far only been assumed in several case reports (41-43). A quantitative measurement and demonstration of vertical
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bone formation in the anterior maxilla after TDI or tooth aplasia has so far not
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been performed in the literature so far. This study provides first quantitative data on the co-development of peritransplant tissues in comparison to the adjacent healthy teeth after premolar transplantation. The horizontal curves of relative bone level compared to the adjacent teeth (Fig. 4) indicate the adequate stimulation of bone growth in the trauma or aplasia affected jaw section. Thus, premolar transplantation is likely to stimulate jaw growth in the affected regions, as a
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ACCEPTED MANUSCRIPT mean plus of relative bone height of +1.2 mm was observed compared to the adjacent dentition. The stimulation of bone growth may be attributed to the osteoinductive effect of the transplants in combination with the orthodontic extrusion therapy.
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Through the formation of a physiological periodontal gap, the orthodontic tension via the periodontal fibres induces a three-dimensional augmentation of the affected local alveolar bone. This has already been clinically applied in
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teeth worthy of being extracted by extrusion therapy prior to implantation (44, 45). The extrusive force activates angiogenetic factors, which lead to the
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reconstruction of the periodontal fibres. Subsequently, the induced increase in osteoblast function results in the formation of new bone (46, 47). To differentiate the effects of orthodontic extrusion and proliferative effect of the transplantation, a correlation between the transplants with and without
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orthodontic extrusion was made. Figure 5 shows an equivalent mesial and distal bone level in both groups implying an osteoinductive effect of the transplants. Also for soft tissue levels no significant differences could be
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detected between the groups.
In a recent study, we have examined the relative bone height after primary
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canine transplantion in children's and juvenile dentition without orthodontic treatment. Also here, a reliable development of vertical bone could be detected (31), suggesting the osteoinductive potential of the transplants to be responsible for the osteoinductive effects. The osteoinductive potential of the transplants overcame even extreme cases of vertical bony growth deficits of more than -4 mm as demonstrated in the clinical case reported (Figure 9). 18
ACCEPTED MANUSCRIPT Vertical bone gain is narrowly associated with soft tissue augmentation, leading to a broadening of the keratinised gingiva (48). This study showed a statistically significant soft tissue increase compared to the adjacent teeth (Fig. 3). Over the entire observation period, the transplants showed a relative
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soft tissue gain of +1.1 mm, which correlates well with the gain in bone
height. Tschammler et al. (31) showed an increase of +3.4 mm in the soft tissue level during the follow-up period after primary canine transplantation in
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the anterior maxilla. In addition, a tendency to hyperplastic gingiva growth
after premolar transplantation has been described in the literature (21). The
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results of this study support this observation with quantitative data.
Increases of root length after transplantation (average 1.5 mm) could be observed on 18 teeth (69.2%) in this study (Figure 6). This correlates well with the results of other studies. Paulsen et al. showed an arrested root
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development after premolar transplantation at 19% of the teeth, a complete root development at 26%, and in 55% of the transplants a progressive, but limited growth (32). Andreasen et al. published similar results and showed
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that the arrest of root development is significantly correlated with a too early root development stage for transplantation (49). This has been attributed to
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the separation or trauma of the Hertwig's epithelial root sheath (50). Signs of pulpal healing were found in 18 (69.2%) transplants. Andreasen et al. reported a rate of pulpal healing for transplants with partial root development of 96% and 15% for teeth transplanted with complete root formation (17). In the literature, a root development stage of 11 is specified as favourable according to Moorrees et al. (23) (Table 3), since an atraumatic extraction is possible and an open apical foramen is still present 19
ACCEPTED MANUSCRIPT facilitating the revascularisation of the transplant (17). The premolars transplanted in this study showed root development stages between 11 and 14 according to Moorrees et al., which is likely to be responsible for the lower rate of pulpal healing and also for the higher incidence of infection-related
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root resorptions. The correlation between root development stage and incidence of root resorptions (p=0.03) confirms this causal relationship
(Figure 7). This underlies the importance of root development and the ideal
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timing for autotransplantations to reduce complications in the form of root resorptions.
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In conclusion, autogenous premolar transplantation represents a reliable and biologically effective method of tooth replacement in the later mixed dentition. This study provides first quantitative evidence of the osteoinductive and soft tissue inductive effects of this technique. Especially in tooth aplasia or TDI,
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where tissue deficits are common, the development of the surrounding bone and soft tissue by this surgical technique can reliably be expected. The technique should be preferred as alternative therapy to other tooth
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replacement measures such as the Maryland bridge or a later planned implantation in those cases in which orthodontic gap closure is technically not
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possible.
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Acknowledgements
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We would like to thank Dr. Christian Kuffer for his statistical support.
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References
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1. Andreasen JO, Andreasen FM, Andersson L, Andreasen JO. Textbook and color atlas of traumatic injuries to the teeth. 4th ed. Oxford, UK ; Ames, Iowa: Blackwell Munksgaard; 2007. xiv, 897 p. p. 2. Borum MK, Andreasen JO. Therapeutic and economic implications of traumatic dental injuries in Denmark: an estimate based on 7549 patients treated at a major trauma centre. International journal of paediatric dentistry / the British Paedodontic Society [and] the International Association of Dentistry for Children. 2001;11(4):249-58. 3. Nimcenko T, Omerca G, Varinauskas V, Bramanti E, Signorino F, Cicciu M. Tooth autotransplantation as an alternative treatment option: A literature review. Dental research journal. 2013;10(1):1-6. 4. Sugerman PB, Barber MT. Patient selection for endosseous dental implants: oral and systemic considerations. The International journal of oral & maxillofacial implants. 2002;17(2):191-201. 5. Kavadia S, Papadiochou S, Papadiochos I, Zafiriadis L. Agenesis of maxillary lateral incisors: a global overview of the clinical problem. Orthodontics : the art and practice of dentofacial enhancement. 2011;12(4):296-317. 6. Stenvik A, Zachrisson BU. Orthodontic closure and transplantation in the treatment of missing anterior teeth. An overview. Endodontics & dental traumatology. 1993;9(2):45-52. 7. Rodd HD, Barker C, Baker SR, Marshman Z, Robinson PG. Social judgements made by children in relation to visible incisor trauma. Dental traumatology : official publication of International Association for Dental Traumatology. 2010;26(1):2-8. 8. Oka AE, N'Cho KJ, Bakayoko-Ly R. [Replacement of deciduous incisors in children: psychological aspects]. Odonto-stomatologie tropicale = Tropical dental journal. 2003;26(102):30-6. 9. Andreasen JO, Schwartz O, Kofoed T, Daugaard-Jensen J. Transplantation of premolars as an approach for replacing avulsed teeth. Pediatric dentistry. 2009;31(2):129-32. 10. Tsukiboshi M. Autotransplantation of teeth: requirements for predictable success. Dental traumatology : official publication of International Association for Dental Traumatology. 2002;18(4):157-80. 11. Waikakul A, Punwutikorn J, Kasetsuwan J, Korsuwannawong S. Alveolar bone changes in autogenous tooth transplantation. Oral surgery, oral medicine, oral pathology, oral radiology, and endodontics. 2011;111(3):e1-7. 12. Slagsvold O, Bjercke B. Autotransplantation of premolars with partly formed roots. A radiographic study of root growth. American journal of orthodontics. 1974;66(4):355-66. 13. Slagsvold O, Bjercke B. Applicability of autotransplantation in cases of missing upper anterior teeth. American journal of orthodontics. 1978;74(4):410-21. 14. Kugelberg R, Tegsjo U, Malmgren O. Autotransplantation of 45 teeth to the upper incisor region in adolescents. Swedish dental journal. 1994;18(5):165-72. 15. Kristerson L, Lagerstrom L. Autotransplantation of teeth in cases with agenesis or traumatic loss of maxillary incisors. European journal of orthodontics. 1991;13(6):486-92. 16. Lundberg T, Isaksson S. A clinical follow-up study of 278 autotransplanted teeth. The British journal of oral & maxillofacial surgery. 1996;34(2):181-5. 17. Andreasen JO, Paulsen HU, Yu Z, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars. Part II. Tooth survival and pulp healing subsequent to transplantation. European journal of orthodontics. 1990;12(1):14-24. 18. Czochrowska EM, Stenvik A, Bjercke B, Zachrisson BU. Outcome of tooth transplantation: survival and success rates 17-41 years posttreatment. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2002;121(2):110-9; quiz 93.
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19. Gilijamse M, Baart JA, Wolff J, Sandor GK, Forouzanfar T. Tooth autotransplantation in the anterior maxilla and mandible: retrospective results in young patients. Oral Surg Oral Med Oral Pathol Oral Radiol. 2016; 122(6): e187-e192. 20. Czochrowska EM, Stenvik A, Album B, Zachrisson BU. Autotransplantation of premolars to replace maxillary incisors: a comparison with natural incisors. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2000;118(6):592-600. 21. Czochrowska EM, Stenvik A, Zachrisson BU. The esthetic outcome of autotransplanted premolars replacing maxillary incisors. Dental traumatology : official publication of International Association for Dental Traumatology. 2002;18(5):237-45. 22. Andreasen JO, Paulsen HU, Yu Z, Ahlquist R, Bayer T, Schwartz O. A long-term study of 370 autotransplanted premolars. Part I. Surgical procedures and standardized techniques for monitoring healing. European journal of orthodontics. 1990;12(1):3-13. 23. Moorrees CF, Fanning EA, Hunt EE, Jr. Age Variation of Formation Stages for Ten Permanent Teeth. Journal of dental research. 1963;42:1490-502. 24. Kristerson L. Autotransplantation of human premolars. A clinical and radiographic study of 100 teeth. International journal of oral surgery. 1985;14(2):200-13. 25. Jonsson T, Sigurdsson TJ. Autotransplantation of premolars to premolar sites. A long-term follow-up study of 40 consecutive patients. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2004;125(6):668-75. 26. Watanabe Y, Mohri T, Takeyama M, Yamaki M, Okiji T, Saito C, et al. Long-term observation of autotransplanted teeth with complete root formation in orthodontic patients. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2010;138(6):720-6. 27. Zachrisson BU, Stenvik A, Haanaes HR. Management of missing maxillary anterior teeth with emphasis on autotransplantation. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2004;126(3):284-8. 28. Plakwicz P, Wojtowicz A, Czochrowska EM. Survival and success rates of autotransplanted premolars: a prospective study of the protocol for developing teeth. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 2013;144(2):229-37. 29. Pohl Y, Filippi A, Kirschner H. Results after replantation of avulsed permanent teeth. II. Periodontal healing and the role of physiologic storage and antiresorptive-regenerative therapy. Dental traumatology : official publication of International Association for Dental Traumatology. 2005;21(2):93-101. 30. Huth KC, Nazet M, Paschos E, Linsenmann R, Hickel R, Nolte D. Autotransplantation and surgical uprighting of impacted or retained teeth: A retrospective clinical study and evaluation of patient satisfaction. Acta odontologica Scandinavica. 2013;71(6):1538-46. 31. Tschammler C, Angermair J, Heiligensetzer M, Linsenmann R, Huth KC, Nolte D. Primary canine auto-transplantation: a new surgical technique. Oral surgery, oral medicine, oral pathology and oral radiology. 2015;119(2):158-69. 32. Paulsen HU, Andreasen JO, Schwartz O. Pulp and periodontal healing, root development and root resorption subsequent to transplantation and orthodontic rotation: a long-term study of autotransplanted premolars. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 1995;108(6):630-40. 33. Andreasen FM, Andreasen JO. Diagnosis of luxation injuries: the importance of standardized clinical, radiographic and photographic techniques in clinical investigations. Endodontics & dental traumatology. 1985;1(5):160-9. 23
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34. Andreasen JO, Hjorting-Hansen E. Replantation of teeth. I. Radiographic and clinical study of 110 human teeth replanted after accidental loss. Acta odontologica Scandinavica. 1966;24(3):263-86. 35. Paschos E, Huth KC, Fassler H, Rudzki-Janson I. Investigation of maxillary tooth sizes in patients with palatal canine displacement. Journal of orofacial orthopedics = Fortschritte der Kieferorthopadie : Organ/official journal Deutsche Gesellschaft fur Kieferorthopadie. 2005;66(4):28898. 36. Linge L, Linge BO. Patient characteristics and treatment variables associated with apical root resorption during orthodontic treatment. American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics. 1991;99(1):35-43. 37. Houston WJ. The analysis of errors in orthodontic measurements. American journal of orthodontics. 1983;83(5):382-90. 38. Dahlberg G. Statistical methods for medical and biological students. London,: G. Allen & Unwin ltd.; 1940. 3 p. l., 9 -232 p. p. 39. Schwartz-Arad D, Levin L, Ashkenazi M. Treatment options of untreatable traumatized anterior maxillary teeth for future use of dental implantation. Implant dentistry. 2004;13(2):120-8. 40. Plakwicz P, Czochrowska EM. The prospective study of autotransplanted severely impacted developing premolars: periodontal status and the long-term outcome. Journal of clinical periodontology. 2014;41(5):489-96. 41. Plakwicz P, Czochrowska EM, Milczarek A, Zadurska M. Vertical bone growth following autotransplantation of the developing maxillary third molar to replace a retained mandibular permanent molar: a case report. The International journal of periodontics & restorative dentistry. 2014;34(5):667-71. 42. Kim S, Lee SJ, Shin Y, Kim E. Vertical Bone Growth after Autotransplantation of Mature Third Molars: 2 Case Reports with Long-term Follow-up. Journal of endodontics. 2015;41(8):1371-4. 43. Hjortdal O, Bragelien J. [Induction of jaw bone formation by tooth autotransplantation]. Den Norske tannlaegeforenings tidende. 1978;88(7):319-22. 44. Brindis MA, Block MS. Orthodontic tooth extrusion to enhance soft tissue implant esthetics. Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons. 2009;67(11 Suppl):49-59. 45. Zuccati G, Bocchieri A. Implant site development by orthodontic extrusion of teeth with poor prognosis. Journal of clinical orthodontics : JCO. 2003;37(6):307-11; quiz 13. 46. Shiu YT, Weiss JA, Hoying JB, Iwamoto MN, Joung IS, Quam CT. The role of mechanical stresses in angiogenesis. Critical reviews in biomedical engineering. 2005;33(5):431-510. 47. de Molon RS, de Avila ED, de Souza JA, Nogueira AV, Cirelli CC, Margonar R, et al. Forced orthodontic eruption for augmentation of soft and hard tissue prior to implant placement. Contemporary clinical dentistry. 2013;4(2):243-7. 48. Salama H, Salama M. The role of orthodontic extrusive remodeling in the enhancement of soft and hard tissue profiles prior to implant placement: a systematic approach to the management of extraction site defects. The International journal of periodontics & restorative dentistry. 1993;13(4):312-33. 49. Andreasen JO, Paulsen HU, Yu Z, Bayer T. A long-term study of 370 autotransplanted premolars. Part IV. Root development subsequent to transplantation. European journal of orthodontics. 1990;12(1):38-50. 50. Andreasen JO, Kristerson L, Andreasen FM. Damage of the Hertwig's epithelial root sheath: effect upon root growth after autotransplantation of teeth in monkeys. Endodontics & dental traumatology. 1988;4(4):145-51.
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Legends of Tables and Figures Table 1: Distribution of transplants sorted by donor and recipient sites. The largest part of premolars was transplanted to the right central and left central incisor sites (n=17, 65%), four transplants replaced lateral incisors, and five
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transplants replaced canines.
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Table 2: Summary of the clinical and radiographic examination results.
Table 3: Stages of tooth development after Moorrees et al. (23).
according to Andreasen et al. (50).
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The black box indicates the ideal time window for premolar autotransplantation
Figure 1: Method for determination of the soft tissue level around transplants in the juvenile dentition as described in a previous study (31).
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The present case shows a 12-year-old patient after premolar transplantation of a mandibular second premolar to the position of the left central incisor with a soft tissue
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method section.
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level increase of +3 mm compared to the healthy adjacent tooth. For detail see
Figure 2: Schematic drawing for the measurement of relative bone height in the juvenile dentition according to Tschammler et al. (31). The example shows a vertical bone deficit of -2 mm as compared to the healthy adjacent tooth. For detail see method section.
25
ACCEPTED MANUSCRIPT Figure 3: Soft tissue levels around the transplants after premolar transplantation. The grey area represents one standard deviation (SD). The curve shows a significant increase in soft tissue levels compared to the adjacent healthy teeth (p<0.01) 24 months after transplantation.
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Statistics: One-way ANOVA with Bonferroni’s Multiple Comparison test.
Figure 4: Relative mesial (A) and distal (B) bone levels compared to the adjacent
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teeth.
The curves in both figures show constant profiles, implying a co-development of bone
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around the transplants compared to the healthy adjacent teeth.
Figure 5: Comparison between relative soft tissue and bone level values between patients with or without orthodontic treatment.
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Mean values revealed no significant differences between teeth with or without orthodontic treatment after transplantation.
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Figure 6: Relative root lengths of transplants in relation to postoperative root lengths. There is a tendency to an increase of the relative root lengths from 6 months
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postoperatively, indicating a sustained root growth after transplantation (N=20; n=26).
Figure 7: Occurrence of root resorption within the follow-up period. A) Kaplan-Meier curve indicates that most root resorptions were identified within the first year. B) Bar graph depicts root resorption in percent dependent of the root development stage according to Moorees et al. (23). All root resorptions occurred in teeth with root development stage ≥13. Statistics: Chi-Square test. 26
ACCEPTED MANUSCRIPT Figure 8: Clinical case of premolar auto-TX in a 12-year-old girl after replantation of the avulsed central right incisor with posttraumatic ankylosis. (A): Due to progressive resorption with vertical growth inhibition compared to the adjacent tooth, the traumatized incisor had to be removed and replaced by transplantation of the upper
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right second premolar (B). The elimination of the vertical deficit through the induced growth of the hard and soft tissues in the follow-up period of 3.5 years can clearly be
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seen (C). The dental composite structure yielded a very good aesthetic result (D, E).
Figure 8 A: Radiographic and clinical view after replantation of the traumatized
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central right incisor with ensuing signs of ankylosis, rooth resorption and discoloration.
Figure 8 B: Intraoperative situation revealing progressive apical root resorption and a
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vertical bony deficit.
Figure 8 C: Radiographic and clinical postoperative findings after premolar
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transplantation. The transplant had to be inserted in about 5 mm infraposition due to
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the lack of adequate soft tissue coverage.
Figure 8 D: Radiographic and clinical findings one year after transplantation. The tooth crown has been constructed in composite adhesive technique. Orthodontic extrusion of the transplant led to a co-development of both bone and surrounding soft tissues. The former gingival deficit of about 5 mm has completely been compensated.
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ACCEPTED MANUSCRIPT Figure 8 E: Radiographic and clinical findings 3.5 years after transplantation. After orthodontic treatment the transplant shows an excellent aesthetic view with a soft-tissue plus of approximately +1 mm. Root obliteration of the transplant is visible
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Recipient region Right upper quadrant Left upper quadrant Canine Incisors Incisors Canine
Donor region
Mandible
n = 20 First premolar
Second premolar
Sum %
-
Lateral -
Central -
Central -
Lateral -
-
Sum 0
% 0.0
Left upper quadrant
-
-
-
-
-
-
0
0.0
Right upper quadrant
-
-
4
-
-
-
4
15.4
Left upper quadrant
-
-
1
1
-
-
2
7.7
Right lower quadrant
-
2
-
-
-
1
3
11.5
Left lower quadrant
2
-
Right lower quadrant
1
-
Left lower quadrant
-
-
3
2
11.5
7.7
1
1
2
-
6
23.0
4
1
-
1
7
26.9
-
4
-
-
4
15.9
10
7
2
2
38.5
26.9
7.7
7.7
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Table 1: Distribution of transplants sorted by donor and recipient sites.
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Second premolar
Right upper quadrant
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First premolar
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n=6
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Maxilla
ACCEPTED MANUSCRIPT Table 2: Transplants 1
2
X
X
3
4
5
6
7
8
9
10
11
12
13
14
15
16
X
X
X
X
17
18
19
20
X
X
21
22
23
24
25
26
Sum
%
10
38.5
16
61.5
12
46.2
14
53.8
Mean
Reason for surgery X X
Traumatic loss
X
X
X
X
X
X
X
X
X
Gender Female
X
X
Male
Age of transplant (years)
X X
X
X
X
X
X
X
X
X
X X
X
X
X
X
X
X
17
12
12
11
11
11
13
19
19
14
14
12
11
12
14
17
17
12
12
11
11
13.3
0
0
0
7
n.d.
n.d.
7.4
6.4
1.3
1.3
4
0
0
0
0.2
1
0.5
2
2
14
n.d.
n.d.
0.3
n.d.
3
5
3
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
3
3
1
2
1
1
1
1
1
2
2
1
1
1
1
1
1
-
-
-
+
+ + +
+ + +
+
+
X
+
+
+
X
X
1
1
1
1
1
1
1
+ + +
+ + +
+ + +
+ + +
high Mobility of transplant X
X
X
X
X
X
X
X
X
X
Grade I 6
6
5
8
7
17
3
5
X
X
2
7
Endodontic treatment
X
X
Orthodontic treatment
X
X
X
X
X
X
X
Transplant modeling X
Crown/Veneer Composite core
X
X
X
X
X
X
X
X
1
1
1
1
1
1
1
1
1
+
+
+ + +
+ + +
+
X
+
X
X
X
X
X
Table 2: Summary of results of the clinical and radiographic examination.
3
4
X
19
X X
X
1
3
0
1
1
1
2
1
+
+
+
+
X
+
+
X
+
X
5
4
6
7
16
8
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X X
X
X X
19.2
14
53.8
1
1
1.2
1
1
1
1
1
1
1.1
+
+
+
+ + +
-
-
+
+
+
X 6
X X
X
19
13
9
+
X
+
X
8
6
X
X
X X
X X
5
1
X
X
X
X
X
69.2
10
38.5
26
100
26
100
0
0
21
80.8
5
19.2 8
23.1
6
23.1
X
8
30.7
X
22
84.6
3
11.5
7
26.9
16
61.5
X X
18
6
X X
3.9
1
X X
1
0
X X
76.9
X
X 9
20
X
X
AC C
X
partial
X
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X
X
X X
X
X
Pulp obliteration total
X
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+
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X
X
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Preparation of Neoalveolus
No change
X
17
X
Periotest
X
X
14
X
Grade 0
X
X
12
Bracket
normal
X
X
11
Suture splinting
Percussion test
X
X
11
Wire-composite splinting
Periodontal Screening Index Oral hygiene (1:good, 2:moderate) Cold sensibility
X
X
Surgical procedure Extraoral storage time (min)
X
X
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Aplasia
X
ACCEPTED MANUSCRIPT Explanation Initial calcification
2
Confluence of the cusps
3
Contour of the cusps complete
4
Crown formed to ½
5
Crown formed to ¾
6
Crown formed completely
7
Initial root formation
8
Initial formation of the bifurcation
9
Root length ¼
10
Root length ½
11
Root length ¾
12
Root length complete
13
Apex closed to ½
14
Apex closed completely
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1
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Stage
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Table 3: Stages of tooth development after Moorrees et al. (22).
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Soft Tissue Level
Relative Soft Tissue [mm]
5
n= 17
17
19
4
9
5
**
**
3
** = p < 0.01
2 1
Range of 1 SD 3 months after sugery
0 -1 -2 Baseline (n=21)
6
12
24
months post sugery
36
A
mesial
10
n= 20
19
22
22
8
8 6 4 2 0 -2 -4
10
n= 20
19
22
22
8
12
24
36
8 6 4 2 0 -2 -4 -6
-6 Baseline (n=26)
distal
B
Relative Bone Level [mm]
Relative Bone Level [mm]
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6
12
24
months post surgery
36
Baseline (n=26)
6
months post surgery
Mesial Bone Level 10
Bone Level [mm]
4 2 0 -2 -4
Bone Level [mm]
10 5 0 -5
Orthodontic treatment
5 0 -5
w ith
-10 w ith ou t
w ith
-10 w ith ou t
Soft tissue level [mm]
6
Distal Bone Level
Orthodontic treatment
w ith
Soft Tissue Level
w ith ou t
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Orthodontic treatment
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Relative Root Length [% of baseline value]
Relative Root Length n= 20 19 30
20
18
8
12
24
36
20 10 0 -10 -20 Baseline (n=26)
6
months post surgery
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Root Resorption
A
21
18
15
14
B 7
80
60
40
20
0 Baseline (n= 26)
n= 1
6
6 13
100 Percent of transplants
Percent root resorbtion
n= 25 100
80
no resorption resorption
60 40 20 0
6
12
24
months post surgery
36
11 12 13 14 Root Development Stage
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