Success, Survival Rate, and Soft Tissue Esthetic of Tooth Autotransplantation

Journal Pre-proof Success, Survival Rate and Soft Tissues Esthetic of Tooth Autotransplantation Natalia Barcellos, Fernanda Carneiro Nunes, João Batista Gagno Intra, Armelindo Roldi, Adriana de Jesus Soares, Marcos Roberto dos Santos Frozoni, Marcelo Santos Coelho PII:

S0099-2399(20)30919-5

DOI:

https://doi.org/10.1016/j.joen.2020.11.013

Reference:

JOEN 4734

To appear in:

Journal of Endodontics

Received Date: 16 April 2020 Revised Date:

23 September 2020

Accepted Date: 11 November 2020

Please cite this article as: Barcellos N, Nunes FC, Gagno Intra JB, Roldi A, de Jesus Soares A, Roberto dos Santos Frozoni M, Coelho MS, Success, Survival Rate and Soft Tissues Esthetic of Tooth Autotransplantation, Journal of Endodontics (2020), doi: https://doi.org/10.1016/j.joen.2020.11.013. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. 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. Copyright © 2020 Published by Elsevier Inc. on behalf of American Association of Endodontists.

Success, Survival Rate and Soft Tissues Esthetic of Tooth Autotransplantation Natalia Barcellos ¹, Fernanda Carneiro Nunes ¹, João Batista Gagno Intra ², Armelindo Roldi ², Adriana de Jesus Soares ³, Marcos Roberto dos Santos Frozoni ¹ , Marcelo Santos Coelho ¹ ¹ São Leopoldo Mandic School of Dentistry – Campinas, Brazil

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³ State University of Campinas – Piracicaba, Brazil

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² Brazilian Association of Dentistry – Vitória, Brazil

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Corresponding author

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Campinas, SP, Brazil

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Rua Emilio Ribas 776/13

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Marcelo Santos Coelho

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CEP 13025-141

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Introduction: The aim of this retrospective study was to assess the success, survival rate, and soft tissue esthetic of autotransplanted teeth. Methods: This study included patients with at least 1 tooth autotransplanted to the maxilla during childhood or adolescence. The autotransplantation technique included the removal of an immature tooth from a donor site and its placement in the maxilla as a replacement for a missing or extremely compromised tooth. The cases were properly

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restored to assure function and esthetic. To be considered successful, the tooth should

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be asymptomatic at the time of assessment, no pain to palpation and percussion, have no signs of apical periodontitis or sinus tract, have a periodontal probe ≤ 3, and have an

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absence of root resorption and development of at least 70% of the normal root. The

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esthetic evaluation of the soft tissue was based on the Pink Esthetic Score (PES) and

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graded as very unsatisfactory, unsatisfactory, poor, fair, good, or excellent. Data were

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statistically analyzed at a significance level of 5%.

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Results: Thirty-five patients (23 male and 12 female) had 43 anterior teeth replaced,

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including 42 central incisors and one lateral incisor. The follow-up period ranged from 1 year to 25 years. In regard to success and survival rate, 43 teeth were assessed; 34 cases (79.07%) were considered successful and 9 (20.93%) unsuccessful. Only 1 tooth was lost, and 42 teeth remained functional (survival rate 97.67%). In regard to the esthetic, 40 teeth could be assessed and were considered as excellent (30%), good (35%), fair (27.5%), and poor (7.5%); there were no reports of unsatisfactory or very unsatisfactory cases. Conclusions: Tooth autotransplantation can be considered a valid procedure to replace lost teeth in the maxilla, presenting high survival and success rates. The overall esthetic of the patients was considered as satisfactory.

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Keywords: autotransplantation, root development, anterior maxilla, survival, success Introduction Modern dentistry offers several options for rehabilitation when there is tooth loss. However, when a child or adolescent presents a missing tooth, the clinical options narrow. Due to incomplete bone growth at a young age, fixed bridges are contraindicated as they can prevent complete development of bone in the area. Likewise,

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implants are not suitable because, with the later development of the maxilla, the

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esthetics of the area might be jeopardized (1). Meanwhile, removable prosthesis lacks

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proper esthetic and comfort for the patient. Thus, a different approach should be

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considered in order to reestablish function and esthetic for young patients in such

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conditions.

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Autotransplantation has been proposed as an option to replace a missing tooth (2-4). This procedure consists of repositioning a tooth from a donor area to a site in which its

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function and esthetic would be more relevant. Often, third molars are used to replace

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posterior teeth that present an injury that cannot be addressed by endodontic or restorative procedures (5). However, when the anterior maxilla is affected, premolars or canines are usually used as donor teeth (6-8). The initial step to reach success includes the proper choice of the donor tooth, in which the maturation of its root should be carefully evaluated (9). The parameters of success include clinical and radiographic assessment of the autotransplanted tooth. Determination of success in autotransplantation cases encompasses several aspects, such as bone formation, root development, pulp regeneration, function, and esthetic (10). A recent study showed an autotransplantation success rate of up to 87.6% and survival rate of 94.4% (11).

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Rehabilitation of teeth in the anterior maxilla should not disregard the esthetic aspects. Shargill et al. evaluated the satisfaction of patients who underwent autotransplantation of teeth to the anterior maxilla (12). However, few studies have assessed the overall esthetic aspect of autotransplanted teeth using professional assessment (2, 13, 14). Recent reviews point to the general lack of information on this topic, mainly when the anterior maxilla is the recipient site (15, 16). Therefore, the aim of the present study is

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to provide further information on this topic, presenting a long-term follow-up of 44

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cases of autotransplantation of teeth in which the anterior maxilla was the main

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recipient site.

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Materials and Methods

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This retrospective study was reviewed and approved by the Ethical Committee of our

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Institution (#2.974.180). A search in the records of patients who underwent autotransplantation of teeth from 1994 to 2018 was performed. The patients’ records

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registered the causes of tooth loss, along with gender, date of birth, date of procedure,

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donor tooth, and replaced tooth. The patients who had autotransplantation of teeth to the maxilla were contacted for clinical and radiographic evaluation. The clinical examination at the time of consultation evaluated symptoms to percussion or palpation and pulp sensitivity test. Also, the signs of sinus tract or swelling, and periodontal probing were assessed. The radiographic images were assessed for periapical radiolucency, external or internal root resorption, ankylosis, and the stage of root development. After the clinical and radiograph examination, the patients were photographed using a Canon EOS XTI camera (Canon Corporation, Tokyo, Japan), lens 105 mm (Sigma Corporation, Tokyo Japan), circular flash KF-150 (K&F Concept, Beijing, China). The

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distance from the lens to the patient was 500 mm, in frontal position, with the patient using a mouth opening and contrast devices. Success and survival rate To be considered successful, the autotransplanted tooth had to be asymptomatic, with no pain to palpation or percussion, and an absence of sinus tract or swelling. Moreover, the successful tooth should present physiologic mobility and periodontal probe ≤ 3 mm.

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The radiographic aspect of a successful case should present healthy periapical bone,

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absence of external and internal root resorption, or ankylosis. Failure in one or more of

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these parameters classified the case as unsuccessful.

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The survival rate was based on the number of teeth present in the arch, but not

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presenting indication for extraction. Both success and survival rate were assessed and

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Root Development

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compared at short-term periods (up to 10 years) and long-term follow-ups (more than 10

The tooth should present signs of root development of at least 70% of the length of a normal root. Root development was classified as: complete, incomplete,or under development. This classification took into consideration the stage of the root at the moment of transplantation and the stage of the root at the follow-up. Two experienced operators assessed the roots and classified them in one of the categories. In cases of disagreement, a third operator discussed the case until a consensus was reached. Bone Formation The assessment of bone formation was based on a formula adopted in a previous study (17). The radiographic images were compared using the Image J software by the same

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two evaluators; a third evaluator was again used in cases of disagreement. Using this program, a line was drawn from the mesial cementoenamel junction (CEJ) of the distal adjacent tooth to the distal CEJ of the mesial adjacent tooth. Then, a perpendicular line was used to measure the distance from this line to the crestal bone in both mesial and distal aspects of the tooth. The mean distance of both sides was calculated in both preand postoperative images; the bone formation, calculated in millimeters (mm), was the difference between the final and initial mean.

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Esthetic Assessment

The images obtained were assessed by six dentists, including two endodontists, two

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periodontists, and two orthodontists. Each case was individually assessed comparing the

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gingival aspect of the assessed tooth with the adjacent teeth. The score used was based

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on the previously proposed Pink Esthetic Score (PES) (18). The evaluators were

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calibrated by assessing six cases of autotransplantation to the anterior maxilla not

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related to this study. At this stage, discrepancies were discussed in order to reach the

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best calibration possible. Then, a new set of cases was assessed until the discrepancies were considered low. Moreover, a guideline was sent to the evaluators with instructions to be followed (Figure 1). The evaluators were asked to assess the following aspects: 1) presence or absence of the mesial papilla; 2) presence or absence of the distal papilla; 3) level of the soft tissue in comparison with the adjacent teeth; 4) gingival contour compared with the adjacent teeth; and 5) color and texture of the gingiva. Each aspect was graded as “0” when unsatisfactory or “1” when satisfactory. For items 1 and 2, the evaluator was to grade as “0” when the papilla was not filling all the interdental space and “1” when all the interproximal space was filled with the papilla. For item 3, the grade “1” was to be applied only when the soft tissue was at the same level as the adjacent teeth. Any

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discrepancy either to coronal or apical level resulted in grade “0”. In item 4, the regular contour of the gingiva was graded as satisfactory and any irregularity resulted as unsatisfactory. In item 5, any difference in color or texture of the gingiva was considered as unsatisfactory; meanwhile, the regularity in color and texture resulted in a satisfactory grade. The overall evaluation resulted in the maximum value of 5 for each assessed tooth. Afterward, the median value of each tooth was classified as: very

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unsatisfactory (0), unsatisfactory (1), poor (2), fair (3), good (4), or excellent (5).

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Descriptive analysis was performed for success and survival rate and reasons for failure. The chi-square test was used for assessment of differences between the short and long-

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term follow ups. The Z-test was used for assessment of differences between the initial

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and the final bone height. Data were statistically analyzed at a significance level of 5%

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Results

Overall, 35 patients, including 23 males (65.71%) and 12 females (34.29%), had 43

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teeth replaced, including 42 central incisors and 1 lateral incisor.

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The age of the patients at the time of the procedure ranged from 8 to 16 years old (11.47 ± 2.07); the age of the patients at the time of the follow-up ranged from 10 to 33 years old (21.02 ± 7.49). The time lapse of autotransplantation varied from 1 year to 25 years (9.68 ± 7.89). The main reason for tooth loss was 42 cases of trauma, with 1 case due to agenesis. The replaced teeth were 42 central incisors (97.67%) and 1 lateral incisor (2.33%). Considering the donor teeth, 10 were maxillary premolars (3 first and 7 second), 32 mandibular premolars (17 first and 15 second), and 1 maxillary canine. The success rate was 79.07% as 34 out of 43 the teeth fulfilled all the parameters to be considered successful and 20.93% of the cases were unsuccessful, with 9 teeth presenting at least one parameter of lack of success. The longitudinal follow-up of the

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cases showed no statistically significant differences in the success rate under 10 years, 20 of 23 cases (86.96%), or above it 14 of 20 cases (70%) (P > .05). Thirteen of the 43 teeth required root canal treatment. The main factors for lack of success were apical periodontitis (6 cases) and external root resorption (4 cases). The survival rate was 97.67%, as 42 out of the 43 teeth were still present while only 1 tooth (2.33%) was extracted. The assessment of all of the clinical and radiographic parameters

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are depicted in Table 1.

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Forty-two cases were assessed for root development; 37 (88.10%) presented complete

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development of the root, 3 (7.14%) presented incomplete root development and 2

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(4.76%) presented roots still in development. One tooth underwent apical microsurgery;

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thus, the root development was not considered.

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Twenty-three teeth were assessed for bone formation; the mean height in bone formation was 0.862 mm. The overall difference between the initial measurement and

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the final measurement was statistically significant (P < .05). The results of bone

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formation are shown in Table 2.

For the esthetic parameter, 240 grades were obtained (40 patients x 6 evaluators); 67 received five points, 68 received four points, 54 received three points, 42 received two points, 8 received one point, and 1 received zero points. The median values showed 12 of 40 (30%) of the cases receiving five points, 14 of 40 (35%) receiving four points, 11 of 40 (27.5%) receiving three points, and 3 of 40 (7.5%) receiving two points. The mean value was 3.58 ± 0.809 points, and the median value was 4 points. The overall results for the PES are shown in Table 3. Figure 2 depicts samples of cases graded as these values. Discussion

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The overall success rate of 34 of 43 teeth (79.07%) and the survival rate 42 of 43 teeth (97.67%) of the present study are in agreement with previous studies of autotransplantation (6, 11, 19, 20). Stange et al. showed a 100% survival rate in 15 autotransplanted teeth after 12.3 years of follow-up and Kafourou et al. showed a 94.4% survival rate in 89 autotransplanted teeth after an average 13.2 years of follow-up (11, 19). In the present study, the overall survival rate was similar, with more than or less than 10 years of follow-up, which is similar to the findings of a previous study at 6 and

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12 years of follow-up (6). In the present study, the single case that was lost during the

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follow-up period presented a failure in the autotransplantation protocol. This tooth was

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re-anatomized and orthodontically treated at an early stage of healing, therefore

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resulting in failure. It can be hypothesized that proper management of this case could

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have resulted in a 100% survival rate as found in previous studies (19, 21).

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While the survival rate seemed to be influenced by a particular reason, the unsuccessful

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cases could have been affected by confound factors. One tooth presented a periodontal

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probe higher than 3 mm and was suffering from periodontal disease instead of adverse effects of the autotransplantation per se. Six out of the 43 teeth presented apical periodontitis, meaning that, despite being classified as unsuccessful, there was still the option of an apical microsurgery to predictably maintain the functionality of these teeth (7, 22). The five cases that presented external root resorption seemed to be stable and surrounded by healthy bone, presenting low risk of poor outcome in the next years. The maintenance of healthy bone in the area of a failure case can be paramount to the success of a future implant (13). Two recent studies presented a survival rate of autotransplantation to the anterior maxilla with similar findings to the present study. Stange et al. presented 100% of survival rate after 12-22 years of follow-up (19). In that study, five out of the twenty

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patients could not return for clinical assessment; however, they informed the researchers verbally that the tooth was functional. Mendoza-Mendoza presented a success rate of 80% after 14 years of follow-up, which is similar to the present study; however, the survival rate was 83.33%, with 2 teeth lost due to external resorption after 6 to 10 years of autotransplantation. Despite the challenges involving the follow-up of the patients, in the present study, the survival rate was calculated only among those patients who could be clinically and radiographically evaluated. Moreover, in order to achieve a reliable

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assessment of the cases, not all parameters could be assessed in each case. Root resorption is one of the main causes of failure in autotransplantation. Substitutive

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resorption or ankylosis was not present in any of the cases of the present study. This

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might be explained by the short extra-oral time allowed in the procedures. A previous

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study showed that a higher extraoral time was correlated with increasing occurrence of

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ankylosis (23). Other studies found ankylosis in autotransplantation cases, such as 8.3%

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in Mendoza-Mendoza et al. and 10.7% in Kim et al. (6, 24). In Mendoza-Mendoza, the

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ankylosis occurred in only 1 case, in which the donor had complete formation of the root. Kim et al. also presented a higher rate of ankylosis at 10.7%. In the latter study, mature molar teeth were predominant among the donor teeth, also contributing to this discrepancy (24). In the present study, there was no case of a donor tooth with complete root formation; only teeth with no more than stage 8 of Nolla were autotransplanted. The findings of the present study showed an average bone formation of 0.86 mm, which is lower than 1.2 mm as presented by Michl et al. (21). However, the present study used periapical radiographs for the assessment of bone formation, while that study had the results based on orthopantomography images. While CBCT scans could have provided more reliable measurements in both studies, it can be hypothesized that periapical

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radiographs seem more accurate than orthopantomography radiographs for this measurement. The findings of the present study showed complete root development in 37 (88.10%) of the roots, and 5 teeth (11.90%) teeth had incomplete or paralyzed root development. Similar to a case reported by Tsukiboshi et al. (10), lack of root development is not necessarily related to tooth loss. In the aforementioned study, a third molar placed in the

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mandible had no root development after 18 months; however, the tooth survived and

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was asymptomatic.

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In the present study, 10 maxillary premolars (3 first and 7 second) and 32 mandibular

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premolars (17 first and 15 second) were used as donor teeth, and only 1 canine was used

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as a donor tooth. The higher incidence of premolars as donor teeth in the present study (97.67%) is in agreement with a previous study that used premolars in 92.0% of the

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cases (11). However, while that study used maxillary second premolars in

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approximately half of the cases, in the present study, mandibular premolars were the

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major source of donor teeth (74.42%), and maxillary second premolars contributed to only 16.28% of the cases. Despite the difference in the donor teeth, that study resulted in a similar success rate (87.6%) and survival rate (94.4%), suggesting that both maxillary and mandibular premolars are suitable as donor teeth. Assessment of aesthetic aspects can be influenced by the experience or calibration of the evaluators. In the present study, the calibration process informed the evaluators to grade any discrepancy in an optimal result as unsatisfactory. A different approach was used in 2 studies by Czochrowska et al., which had 3 or 5 different grades for gingival papilla (13, 14). Whichever these approaches might be more accurate, the grading process herein adopted can be considered stricter and could have resulted in lower levels of success. The present study relied on 6 calibrated evaluators; meanwhile, only 2

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evaluators were used by Czochrowska et al. (13). Fürhauser et al. used 20 evaluators, including prosthetists, orthodontists, and oral surgeons, as well as undergraduate dental students, in the original PES assessment. Since aesthetic is a subjective factor, the present study used a score with objective parameters (PES) based on a previous study of single-unit implants (18). While the procedures are not equal, both studies aimed to assess the esthetic aspect of

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rehabilitation in the anterior maxilla. The values ranged from 0 to 5, with 5 being the

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best achievement possible. The mean value obtained was 3.58 ± 0.809 and the median value was 4, suggesting that the results obtained were satisfactory. Moreover, in 65% of

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the scores, the results could be considered as good or excellent, and only in 7.5% as

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poor. Among the assessed individuals, there was no occurrence of mean values

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considered unsatisfactory or very unsatisfactory. The results obtained in the present

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study suggest that a great level of esthetic success was achieved.

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While the results of the present study suggest that the esthetic aspects of

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autotransplantation of the teeth of the anterior maxilla are satisfactory some points should be further assessed in future studies. The overall satisfaction of the patients should be compared with the assessment done by the professionals as presented in previous findings. The present study, in contrast to a previous one, focused on the professional evaluation of aesthetics, rather than on patient´s impression (12). Stange et al. showed that professionals are more critical than laypeople regarding the assessment of the aesthetic aspects of autotransplanted teeth (19). General dentists and endodontists should be familiar with the autotransplantation technique, thus considering this approach as an option to use original teeth to replace missed anterior teeth in the maxilla. Based on the findings of the present study, it can be

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concluded that autotransplantation of teeth to the maxilla resulted in high rates of success and survival rate and satisfactory esthetic achievement. ACKNOWLEDGMENTS

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The authors deny any conflict of interest related to this study

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Table 1. Absolute numbers for each clinical and radiographic parameter assessed

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symptomatology pain to palpation pain to percussion periodontal probe > 3 mm mobility class ≥ 1 periapical radioluscency sinus tract root fracture internal root resorption external root resorption ankylosis

present absent 0 42 0 42 1 41 1 41 0 42 6 36 0 42 0 42 1 41 4 38 0 42

Table 2. Values (mm) of bone formation at the mesial aspect, distal aspect the mean and standard deviation of both aspects T-test 1.862 3.460 3.162

P value 0.076* 0.002 0.005

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value in mm postoperative follow-up mesial -2.254 ± 1.557 -2.902 ± 1.917 distal -1.328 ± 0.977 -2.405 ± 1.350 mean -1.791 ± 1.153 -2.653 ± 1.471 * not statistically different at P > .05

Table 3. Pink Esthetic Score, absolute and percentage of the values obtained from the 240 assessments; percentage of median value in each score absolute value (n=240) percentage (%) 1 0.42 8 3.33 42 17.5 54 22.5 68 28.33 67 27.92

median (%) 0.0 0.0 7.5 27.5 35 30

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PES Score 0 1 2 3 4 5

Figure 1. Summary of the images sent as instructions for the evaluators: absence (A) or presence of dental papilla (B); level of the soft tissue: above (C), below (D) and ideal

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(E); and contour of the gingiva irregular (F) or regular (G).

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Figure 2. Samples of cases that were graded as poor (A), fair (B), good (C) and excellent (D). The autotransplanted teeth were left maxillary incisors (A and B) and

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right maxillary incisors (C and D)

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Natalia Barcellos: Clinical procedures, study design, review of manuscript Fernanda Carneiro Nunes: Clinical procedures, study design, review of manuscript João Batista Gagno Intra Clinical procedures, study design, review of manuscript Armelindo Roldi: Clinical procedures, follow-up management Adriana de Jesus Soares : study design, review of manuscript

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Marcos Roberto dos Santos Frozoni: Clinical procedures, study design, review of

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manuscript

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Marcelo Santos Coelho: Writing of manuscript, study design, review of manuscript