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Clinical Research|Articles in Press

Pulp revascularization after autotransplantation of the mandibular canines with partially resected roots. Report of five cases with follow-ups between 26 and 80 months

Open AccessPublished:March 17, 2023DOI:https://doi.org/10.1016/j.joen.2023.03.006

      ABSTRACT

      Introduction

      Transmigrated (migrated through the midline) mandibular canines constitute a treatment challenge. Advanced transmigration can be successfully treated by autotransplantation. In developing canines, pulp revascularisation is typical after transplantation. On the contrary, the pulp of teeth with completed apex formation does not undergo revascularization. In this case, root canal treatment becomes compulsory and decreases the success of autotransplantation. The aim of this observational retrospective study was to evaluate whether partial resection of the root (performed during the autotransplantation of mature canines) would enable revascularization of the pulp after the surgery.

      Methods

      Five transmigrated mandibular canines with complete apex formation before the surgery were evaluated. During the autotransplantation surgery, the resection of 2-4 mm of the root apex was performed to open the path for revascularisation of the pulp after surgery. The transplanted teeth were observed during healing after the surgery for the presence of pulp obliteration. Clinical and radiographic examinations were performed.

      Results

      All treated canines survived the minimum observation period of two years (ranging from 26 to 80 months, mean: 55 months) without pulp healing complications. The survival was 100 percent, and the success was 80 percent. In one canine, the external cervical root resorption was diagnosed and treated one year after the surgery. At the final examination, transplanted canines presented radiographic features of pulp obliteration, normal mobility, and healthy periodontal tissues.

      Conclusions

      The surgical protocol proved to be successful in promoting revascularization to maintain pulp vitality, in all cases. The outcomes confirm that autotransplantation, combined with the resection of the root, constitutes as a valid treatment for mature ectopic canines.

      Keywords

      INTRODUCTION

      Autotransplantation of teeth has attracted special attention in the last decades. Successful outcomes for specific protocols have been well documented and, as a result, more patients can benefit from this type of treatment.
      It has been proven that autotransplantation of developing teeth had better outcomes regarding survival and success, when compared to teeth autotransplanted with complete root development (
      • 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.
      ,
      • Almpani K
      • Papageorgiou SN
      • Papadopoulos MA
      Autotransplantation of teeth in humans: a systematic review and meta-analysis.
      ). In developing teeth with widely open apices, the revascularisation of the pulp is expected within the first weeks after the surgery. In teeth with complete root development, pulp does not undergo revascularization and root canal treatment (RCT) becomes compulsory. Therefore, the success of autotransplantation of mature teeth is additionally dependent on the outcome of the RCT of the transplants. The study by Murtadha and Kwok (
      • Murtadha L
      • Kwok J
      Do autotransplanted teeth require elective root canal therapy? A long-term follow-up case series.
      ), showed that even though post-surgical RCT was not performed, some mature autotransplanted teeth presented pulp obliteration. However, the authors concluded that routine RCT should be considered after transplantation of mature donors. In 2015, revascularization of a maxillary incisor transplanted from an ectopic position was described despite detachment of its root apex during the surgery (
      • Plakwicz P
      • Kapuścińska A
      • Kukuła K
      • Czochrowska EM
      Pulp Revascularization after repositioning of impacted incisor with a dilacerated root and a detached apex.
      ). In 2018, Jakse (
      • Jakse N
      • Ruckenstuhl M
      • Rugani P
      • Kirnbauer B
      • Sokolowski A
      • Ebeleseder KJ
      Influence of extraoral apicoectomy on revascularization of an autotransplanted tooth: A case report.
      ) demonstrated the technique of resection of the apical part of premolar’s root to promote revascularization of pulp. This phenomenon was previously described in an animal study (
      • Skoglund A
      Pulpal changes in replanted and autotransplanted apicoectomized mature teeth of dogs.
      ). Furthermore, in 2019, the “fragile fracture technique” was applied to assist autotransplantation of a mature premolar. The dentine was abraded to produce an external groove in the root surface, without invading the root canal. Later, the fragile fracture root-end resection was performed using a dental elevator, maintaining the apical pulp tissue intact. Successful pulp revascularization was later observed (
      • Gaviño Orduña JF
      • García García M
      • Dominguez P
      • Caviedes Bucheli J
      • Martin Biedma B
      • Abella Sans F
      • et al.
      Successful pulp revascularization of an autotransplantated mature premolar with fragile fracture apicoectomy and plasma rich in growth factors: a 3‐year follow‐up.
      ). Until now, only one study reported several patients who have undergone partial root resection performed during autotransplantation of a mature tooth (
      • Raabe C
      • Bornstein MM
      • Ducommun J
      • Sendi P
      • von Arx T
      • Janner SFM
      A retrospective analysis of autotransplanted teeth including an evaluation of a novel surgical technique.
      ). Pulp revascularization and obliteration after the surgery was found in 4 out of 9 resected teeth.
      After a standard surgical procedure (without resection of the root end) the healing outcomes for different groups of donor teeth have different predictability for normal post-surgical healing. Autotransplanted premolars have the highest survival, followed by molars and canines with 75%, 50% and 25% survival respectively (
      • Schwartz O
      • Bergmann P
      • Klausen B
      Autotransplantation of human teeth. A life-table analysis of prognostic factors.
      ,
      • Akhlef Y
      • Schwartz O
      • Andreasen JO
      • Jensen SS
      Autotransplantation of teeth to the anterior maxilla: A systematic review of survival and success, aesthetic presentation and patient-reported outcome.
      ).
      The incidence of impaction of permanent canines in the mandible ranges from 0.3% to 1.35% and is lower than in the maxilla (
      • Aydin U
      • Yilmaz HH
      • Yildirim D
      Incidence of canine impaction and transmigration in a patient population.
      ,
      • Aras MH
      • Halicioğlu K
      • Yavuz MS
      • Çağlaroğlu M
      Evaluation of surgical-orthodontic treatments on impacted mandibular canines.
      ). Once diagnosed, ectopic or migrated mandibular canine constitutes a major challenge and usually requires a multidisciplinary treatment approach. Autotransplantation may also be considered as one of the treatment options (
      • Plakwicz P
      • Czochrowska EM
      The prospective study of autotransplanted impacted developing premolars: periodontal status and the long-term outcome.
      . The choice of the treatment of migration depends on age, orthodontic indications and severity of migration. It includes surgical exposure of the affected tooth followed by orthodontic extrusion, autotransplantation, and extraction or conditional observation (
      • Sajnani AK
      • King NM
      Success rates of different management techniques for impacted mandibular canines and associated complications in children and adolescents.
      ). Transmigrated mandibular canines (canines which have migrated across mandibular midline) are particularly difficult regarding orthodontic treatment planning. In contrast to slightly migrated canines (which can be aligned in the dental arch after forced orthodontic eruption) advanced transmigration can be successfully treated by autotransplantation or the canine must be extracted. Furthermore, severely migrated, or transmigrated canines are usually diagnosed after complete maturation of their roots. In these cases, root canal treatment (RCT) is necessary to avoid pulp necrosis after transplantation because revascularization of pulp cannot be expected. RCT is associated with additional costs, increased treatment time, and frequent appointments with a specialist. Additionally, some patients relate RCT to pain, discomfort, and complications, that can occur as well. As a result, most patients’ families and dentists abandon the option of transplantation of a mature tooth and the removal of a canine remains the only solution.
      In agreement with the findings above, the aim of this observational retrospective study was to evaluate whether partial resection of the root (performed during the autotransplantation of mature canines) would enable revascularization of the pulp after the surgery. Donor teeth were treated with partial resection of the root, which was performed during autotransplantation of the canine from its ectopic to the normal position in the dental arch. Resection of the root end was performed to remove the apical constriction to widen the apical diameter and allow revascularization of the pulp.

      MATERIALS AND METHODS

      The Ethical Committee of the Medical University <blinded> approved the study (AKBE/86/14). A total of one hundred and twenty-seven patients with ectopic position of the mandibular canine were diagnosed from 2007 to 2018 in the oral surgery practice, which specializes in tooth impactions and autotransplantation. In 50 patients, the impacted canines had developing roots and in 77 patients, the root development was complete (stage 7 according to Moorrees classification) (
      • Moorrees CFA
      • Fanning EA
      • Edward E
      • Hunt J
      Age variation of formation stages for ten permanent teeth.
      ). Orthodontic and surgical consultations were performed for all patients and different treatment options were presented to the patients and their legal guardians. Figure 1 presents the diagram of enrolment, the selection criteria, the number of surgeries performed, dropouts, and the final number of the autotransplanted mature canines included in the study. The inclusion criteria were as follows: patients with transmigration of the mandibular canine with complete apex formation who underwent autotransplantation with partial resection of the root apex and minimum observation time of two years after the surgery. Exclusion criteria were incomplete data after the surgery or absence on the follow-up visits. Nine patients underwent trans-alveolar autotransplantation of the canine with the partial resection of a root during the transplantation surgery. These canines had complete root development and, therefore, the surgical protocol was modified in relation to the developing canines (when root resection was not performed). In one patient, the decision of canine extraction was made at the time of the surgery due to iatrogenic traumatization during removal from its ectopic position. Finally, after applying inclusion and exclusion criteria, five autotransplanted canines with complete root development and partial root resection (at the time of autotransplantation) were evaluated.
      Figure thumbnail gr1
      Figure 1Diagram of enrolment, selection, dropouts, and follow-up of patients in the study.
      In the study group, panoramic radiographs confirmed unilateral transmigration of the mandibular canine and pattern 1 of transmigration according to classification proposed by Mupparapu (

      Mupparapu M. Patterns of intra-osseous transmigration and ectopic eruption of mandibular canines: review of literature and report of nine additional cases. Dentomaxillofac Radiol 202;31:355-360.

      ). Migration of canines was advanced to the stage in which the tips of canines’ crowns were at the site of the lateral incisors’ roots on the opposite side of the arch. All transmigrated canines were located labially to the roots of mandibular incisors which was confirmed on the CBCT examination. Four patients had previous orthodontic treatment of opening the space between a lateral incisor and a first premolar on the affected side. Space opening was performed to facilitate a spontaneous eruption of the migrated canine; however, it was unsuccessful and there was no improvement in canine eruption before the surgery. One patient had no orthodontic treatment before the surgery. In four patients there were no primary canines at the migration site. In one patient, the primary canine was present until the autotransplantation surgery. The demographic data of study patients are given in Table 1.
      Table 1Demographic data of study patients at the time of the surgery.
      PATIENT 1PATIENT 2PATIENT 3PATIENT 4PATIENT 5
      Genderfemalefemalefemalefemalefemale
      Age at the surgery12y/4m12y12y/1m13y/7m14y
      Tooth number2227222222
      Stage of root development*77777
      Pattern of transmigration**11111
      Previous orthodontic treatmentyesyesyesyesno
      Legend to Table 1. *Root development was assessed according to the Moorrees (Moorrees et al. 1963). **Pattern of transmigration established based on description given by Mupparapu (Mupparapu 2002).
      According to the regular protocol for transplantation of mature teeth, all mature canines would be scheduled for root canal treatment a few weeks after the surgery. This would be required to avoid pulp complications because revascularization after transplantation was not expected in teeth with mature apices. All patients’ families disliked the necessity of root canal treatment and preferred to remove the canine to avoid having a non-vital tooth after treatment. Consultations with paediatric dentists and orthodontists were provided to discuss all potential treatment options with patients’ families. To save the vitality of the migrated canines and to minimize the risk of mandibular fracture, the decision was made to perform a resection of the apex of canines during autotransplantation to widen the apical foramen and to enhance the revascularization of the pulp after surgery. Informed consent was obtained for the surgical procedure, follow-up appointments and orthodontic treatment in the future.

      Surgical procedure

      The surgeries were performed under local anaesthesia (articaine with epinephrine; 1:200.000) deposited in the area between the first mandibular premolars. In all cases, the surgical procedure was the same. The full-thickness flap was raised with at least one vertical incision at the sites of the first premolars on the vestibular side of the alveolus. The transmigrated canine was carefully exposed from the buccal bone which covered their crowns. Afterwards, the canine was gently removed from its initial location in the way to avoid trauma to the periodontal ligament of the root. The intra-surgical assessment of complexity of the canine removal and the status of PDL (periodontal ligament) was individually performed. This inspection of the root allowed for the assessment of any damage to the root surface and that the tooth had a favourable chance of successful periodontal healing after transplantation." In every case, an individual decision was made to continue the procedure of transplantation with resection of an apex and not to extract the canine. During apex resection, the canine’s crown was kept in the surgeon’s fingers to avoid trauma of the PDL from sharp instruments. When the 2–4-millimetre apical part of the canine’s root (containing apical constriction) was resected with a diamond bur in a contra-angle handpiece at 3000 rpm, the root of the canine was continually hydrated with saline administered by syringe. Then, the canine was stored in saline to avoid drying of the PDL until the artificial root socket was prepared at the recipient site between the lateral incisor and the first premolar. The surgical socket at the recipient site was prepared after removal of the migrated canine from its crypt. This was due to the presence of the canine’s root below the recipient site which could be traumatised if recipient socked was prepared first. The preparation of the socket, according to the measurements taken from the initial CBCT examination, was complete when an adequate width and height of the socket was achieved to accommodate the resected canine and to avoid the damage to the adjacent teeth. The preparation was performed with surgical carbide round burs at the 1000 rpm under copious saline rinsing. To keep a safe distance from the roots of the lateral incisor and the first premolar, the new socket was prepared more labially than the normal position of the canine’s root. The preparation of the socket created a bone dehiscence at the labial side of the alveolar bone. The dehiscence was left to heal spontaneously by labial bone apposition on the transplanted canine’s root after surgery, as previously described in a case report (
      • Plakwicz P
      • Wojtaszek J
      • Zadurska M
      New bone formation at the site of autotransplanted developing mandibular canines: a case report.
      ). The cumulative extra-oral time of root resection and preparation of surgical socket didn’t exceed 7 minutes. The canine was loosely placed in the prepared socket with 1-millimeter free space around the root surface and apically to the resected root. There were no repeated attempts to accommodate canine in the sockets to avoid damage of the PDL. The space filled spontaneously with blood after positioning of the transplant and before suturing. The stabilisation of canines in the socket was obtained only by suturing the soft tissues. The canine’s crown didn’t reach the opposite teeth to avoid occlusal contacts which could disturb early healing. The intra-oral radiograph was taken before suturing to confirm adequate position of the transplanted canine. The mucoperiosteal flap was repositioned and stabilized with 5-0 resorbable sutures. (Fig. 2). All patients were prescribed amoxicillin (500 mg every 8 hours for 5 days) to reduce the risk of postoperative infection and development of root resorption (
      • Hammarström L
      • Blomlöf L
      • Feiglin B
      • Andersson L
      • Lindskog S
      Replantation of teeth and antibiotic treatment.
      ,
      • Andreasen JO
      • Paulsen HU
      • Yu Z
      • Bayer T
      A long-term study of 370 autotransplanted premolars. Part II. Tooth survival and pulp healing subsequent to transplantation.
      ,
      • Chung WC
      • Tu YK
      • Lin YH
      • Lu HK
      Outcomes of autotransplanted teeth with complete root formation: a systematic review and meta-analysis.
      ).
      Figure thumbnail gr2
      Figure 2(Adjustment of brightness were performed). Clinical photographs from the representative surgery performed in the study patient (Patient 1). Preparation of a full-thickness flap (a) exposure of labial bone for gentle removal of the ectopic canine (b), measurements of the apical part of the apex before resection (c, d), resection on apical part with the use of diamond bur (e), measurements after resection (f, g), placement of canine in the surgical socket (h), final stabilization of the transplanted canine and sutures (i).

      Follow-up

      The healing was uncomplicated in all cases, with no signs of oedema or inflammation and sutures were removed 10-14 days after surgeries. All treated patients were monitored from 26 to 80 months after surgery (mean follow-up was 55 months). The intra-oral radiographs were taken at each follow-up appointment i.e., 1, 2, 3, 5, 7, 9, 12, 18, 24 months after surgery and then annually.
      The criteria of success included:
      • Normal periodontal healing (i.e., an absence of pathology within PDL, and normal canine eruption and mobility).
      • Pulp healing (i.e., pulp revascularization observed as presence of progressing obliteration combined with an absence of any type of inflammatory root resorption associated with pulp necrosis).
      • Presence of a healthy bone around the left part of the root. Root development was not expected since the apical part of the root (which contained Hertwig’s epithelial root sheath) was intentionally resected during autotransplantation surgery.

      RESULTS

      All transplanted canines were present in the oral cavity after an observation period. The survival was 100%.
      Spontaneous eruption of the autotransplanted canines towards occlusal contact was observed in all cases and before including the transplanted canines to the orthodontic appliance.
      Orthodontic alignment of transplanted canines was performed between two and ten months after the surgery and was completed before the final examination. The periodontal tissues were healthy and pocket probing depths were between 2 and 4 mm with no bleeding on probing. A normal clinical attachment level and a wide keratinized gingiva were present around the teeth. (Fig. 3). Canines presented normal mobility and responded to vitality tests within normal limits.
      Figure thumbnail gr3
      Figure. 3Adjustment of brightness were performed). The clinical presentation of the mandible of five patients (P1-P5) at the final examination are presented in the left column. A normal contour of the alveolus with no gingival recession and an adequate width of the keratinized gingiva is present at the sites of the autotransplanted canines (black arrows). The long clinical crown of the transplant in the fifth patient is present but the root is not exposed. Sagittal scans from CBCT examinations performed after the surgery in patients are presented in the right column. The normal appearance of the alveolar bone and the labial plate is visible. White arrow in panel/row 4 (P4) indicates the presence of external cervical resorption of the root at the lingual side of the transplanted canine.
      Extra-oral periapical radiographs confirmed clinical observation of an eruption and re-establishment of lamina dura of the alveolar socket. No pathology of alveolar bone or the root of the transplant was found within the first year. One transplant presented an external cervical resorption (ECR) of the root at the follow-up one year post surgery.
      Progressive pulp obliteration was detected on radiographs in all autotransplanted canines. Initial pulp obliteration was detected between five and seven months after the surgery. It consisted of a partial narrowing of the pulp space, which was uniform along the length of the remaining root. Obliteration progressed gradually and at the final radiographic examination, three out of five canines presented complete pulp obliteration. Two teeth had only partial obliteration even after two years of observation. (Fig. 4)
      Figure thumbnail gr4
      Figure 4Radiographic examination of the patients: pre-surgical cropped panoramic radiographs (5 patients: P1-P5); resection at the surgery (P1s-P5s); one year follow-up (P1y-P5y); and final status of root healing (P1f-P5f) on periapical radiographs. Additional information: in one patient, Geristore (Den-Mat Holdings, Lompoc CA, USA) restoration was placed after cleaning the ECR lacuna and is visible at the cervical level (P4f – white arrow).
      The resected roots of the canines were not associated with any pathology on radiographs. At the intra-oral radiographs, taken immediately after the resection, the roots had sharp edges (Fig. 4. P1surg-P5surg) which gradually tapered with time (P1-1year-P5-1year). At the final radiographs (Fig. 4. From 26 to 80 months), their resected ends were smoothed and surrounded by a normal PDL space.
      Four out of five transplanted canines successfully healed according to the established criteria. One transplanted canine (in patient 4) developed ECR which was detected and successfully treated one year after surgery. The small reflection of marginal gingiva was performed under local anaesthesia. The granulation tissue was removed with excavators and the resorption lacuna was filled with Geristore (Den-Mat Holdings, Lompoc CA, USA). The gingiva was sutured with resorbable material. No recurrence was observed afterwards. Success was confirmed in four out of five autotransplanted canines. All treated patients were satisfied with the treatment and had no complaints regarding the outcomes.
      Cone beam computed tomography (CBCT) was performed after the surgery. It was limited to the operated area and served to evaluate the position of the canines’ roots during or after the orthodontic treatment. At each site of the autotransplanted canine, the labial plate of the alveolar bone was present at the CBCT examination and covered most of the root (Fig. 3-right column), even though the labial dehiscence was created at the time of the surgery (Fig. 2h).
      Due to the small number of canines in the study, the statistical analyses were considered inappropriate. Instead, Table 2 presents intra-surgery data, information about orthodontic treatment and healing, and survival/success of the transplanted canines.
      Table 2Intra-surgery data, follow-up observations and survival/success of study canines.
      PATIENT 1PATIENT 2PATIENT 3PATIENT 4PATIENT 5
      Extra-oral time during surgery (in 0.9% saline /in minutes)55657
      Observation period after surgery (in months)2680656443
      CBCT after surgery (in months)2531251236
      Start of the orthodontic mobilization of the transplant after surgery (in months)/ length of the post-surgical orthodontics (in months).5 / 19 completed10 / 18 completed3 / 35 completed2 / 24 completed4 / 32 completed
      First signs of pulp obliteration after the surgery (in months)56576
      Type of final obliteration of the pulp (“full” or “partial”)partialfullfullpartialfull
      Periapical pathology / resorption of the apical part of the root-----
      Pocket probing (in mm)/ bleeding (“yes” or “no”)2-4/no2-3/no2-3/no2-4/no2-3/no
      Complications (time of detection in months)---ECR (12)-
      Survival+++++
      Success (established criteria)+++-+

      DISCUSSION

      The presence of a permanent mandibular canine is important for the shape of a lower arch and the occlusal conditions, especially regarding the canine guidance also known as the canine protected occlusion (
      • D'Amico A
      Functional occlusion of the natural teeth of man.
      ).
      In case of migration or impaction of a mandibular canine, different treatment options are available. Most of them are associated with duration and high cost of the treatment and possibility of various complications. Surgical removal of impacted mandibular canine is the most frequently performed treatment (
      • Plakwicz P
      • Abramczyk J
      • Wojtaszek-Lis J
      • Sajkowska J
      • Warych B
      • Gawron K
      • et al.
      The retrospective study of 93 patients with transmigration of mandibular canine and a comparative analysis with the control group.
      ). For this reason, autotransplantation is an option to save migrated mandibular canines. It decreases the time of the treatment and avoids complications related to the adjacent teeth.
      The migrated canines in the study had complete root development. The patients were selected from the 127 cases diagnosed with mandibular canine migration. In the presented cases, the impaction couldn’t be treated with orthodontic exposure and bonding of an orthodontic bracket followed by gradual orthodontic traction. Orthodontic traction was not possible because it could pose a threat to the roots of the adjacent teeth. Autotransplantation was the only alternative treatment option to save the affected canine. For the nine patients who participated in the surgery, one patient had the canine removed instead of being autotransplanted, because the canine’s root was seriously traumatized during removal from the bone. this demonstrates that, in some cases, removal of an intact canine may not be possible despite a labial position of impacted canine. Another two canines didn’t fulfil the inclusion criterion of the two-year observation period, which was considered the minimum time to reliably assess the pulpal healing and treatment outcomes.
      Autotransplantation of the tooth requires a gentle technique of removing the transplanted tooth from its initial location, careful handling and placing the transplant in the recipient site. Avoiding trauma to the periodontal ligament and cementum of the root is crucial to prevent complication of healing after surgery. For this reason, manipulation of the transplant is usually limited to the direct contact with the coronal part of the donor (this includes elevation from the donor site, handling during transfer and accommodation within the recipient site) while all efforts are made to avoid any contact with the root surface. In these cases, the contact with the canines’ root could not be avoided because the root apices were resected during the extra-oral handling of the canines. The resection of the apices was performed under copious irrigation with saline and the canines were stored in saline during preparation of the surgical sockets, which prevented from drying of the periodontal ligament and cementum.
      Antibiotic prophylaxis was administered after surgery to all operated patients to reduce the risk of infection. Antibiotic use can potentially improve the outcome of autotransplantation, as the failure rate has been reported to be 2.5 times higher in studies which report not using systemic antibiotics when compared with those when antibiotics were administered (
      • Hammarström L
      • Blomlöf L
      • Feiglin B
      • Andersson L
      • Lindskog S
      Replantation of teeth and antibiotic treatment.
      ,
      • Andreasen JO
      • Paulsen HU
      • Yu Z
      • Bayer T
      A long-term study of 370 autotransplanted premolars. Part II. Tooth survival and pulp healing subsequent to transplantation.
      ,
      • Chung WC
      • Tu YK
      • Lin YH
      • Lu HK
      Outcomes of autotransplanted teeth with complete root formation: a systematic review and meta-analysis.
      ).
      Final clinical and radiographic examinations of the canines were performed between 26 and 80 months after the surgery, which is enough time to conclude healing outcomes.
      Revascularization of the pulp of autotransplanted teeth is desired to maintain vitality of transplants after the surgery. This phenomenon can prevent potential complications faced by the presence of non-vital teeth including discoloration, fracture, or secondary inflammation in the future. Pulp revascularization is normally observed in autotransplanted developing teeth which have open apices at the time of surgery (
      • D'Amico A
      Functional occlusion of the natural teeth of man.
      ,
      • Kafourou V
      • Tong HJ
      • Day P
      • Houghton N
      • James Spencer R
      • Duggal M
      Outcomes and prognostic factors that influence the success of tooth autotransplantation in children and adolescents.
      ). Progressive obliteration of the pulp is a radiographic feature which confirms the revascularization of the pulp. The first signs of obliteration are usually detected several weeks after autotransplantation of immature teeth with gradual partial or complete obliteration of the canal, and the coronal part of the pulp. (
      • Skoglund A
      • Tronstad L
      Pulpal changes in replanted and autotransplanted immature teeth of dogs.
      ). The revascularization does not occur in mature teeth, in which apical constriction prevents ingrowth of vessels in most mature transplants.
      Only a few studies suggested incidence of revascularization and presence of pulp obliteration in mature teeth (
      • Murtadha L
      • Kwok J
      Do autotransplanted teeth require elective root canal therapy? A long-term follow-up case series.
      ). It is extremely rare in mature teeth and, consequently, the root canal treatment is routinely performed (before or few weeks after transplantation of mature teeth) to avoid inflammatory complications (
      • Schwartz O
      • Bergmann P
      • Klausen B
      Autotransplantation of human teeth. A life-table analysis of prognostic factors.
      ,
      • Chung WC
      • Tu YK
      • Lin YH
      • Lu HK
      Outcomes of autotransplanted teeth with complete root formation: a systematic review and meta-analysis.
      ,
      • Lin PY
      • Chiang YC
      • Hsu LY
      • Chang HJ
      • Chi LY
      Endodontic considerations of survival rate for autotransplanted third molars: a nationwide population-based study.
      ). In the experimental study on dogs, Skoglund (
      • Skoglund A
      Pulpal changes in replanted and autotransplanted apicoectomized mature teeth of dogs.
      ) documented that revascularization is possible after resection of an apex of the root during surgery. According to the study finding, the vessels from the trabecular bone, adjacent to the end of the resected root, entered the root canal and the replacement of the necrotic pulp by a well-vascularized connective tissue was documented three months after the surgery. The results were recently confirmed in an experimental study in mice (
      • Nakakura‐Ohshima K
      • Quispe‐Salcedo A
      • Sano H
      • Hayasaki H
      • Ohshima H
      The effects of reducing the root length by apicoectomy on dental pulp revascularization following tooth replantation in mice.
      ). The treatment described in the present study was aimed at investigating whether autotransplantation of the mature impacted canines with root resected during the surgery, would bring benefit in terms of pulp revascularization.
      The resection of the apical part of the root was performed to make revascularization more likely. Pulp obliteration was documented in all cases and demonstrated complete revascularization of the pulp after the surgery, contrarily to the results published by Raabe (
      • Raabe C
      • Bornstein MM
      • Ducommun J
      • Sendi P
      • von Arx T
      • Janner SFM
      A retrospective analysis of autotransplanted teeth including an evaluation of a novel surgical technique.
      ), where only four out of nine teeth presented the signs of obliteration. No pathology related to the remaining root end was clinically or radiologically diagnosed. Root growth after transplantation was not expected as a natural consequence of the removal of the tip of the root which contained Hertwig’s epithelial root sheath.
      The clinical examination of the canines after the surgery showed typical features of successful autotransplantation: spontaneous eruption after the surgery, normal mobility, submission to the orthodontic forces (features which proved the absence of an ankylosis) and pocket probing depths within normal ranges. These features enhanced normal alveolar bone development and for that reason were crucial in young patients, in which alveolar bone development was still expected. A normal bone level was detected in all operated patients, both at the proximal sites of transplants and at the labial and lingual surfaces of their roots. These findings were in agreement with the study published in 1998 and more recently in 2021, which documented maintenance of the alveolar bone at the sites of autotransplanted teeth (
      • Paulsen HU
      • Andreasen JO
      Eruption of premolars subsequent to autotransplantation. A longitudinal radiographic study.
      ,
      • Plakwicz P
      • Andreasen JO
      • Górska R
      • Burzykowski T
      • Czochrowska E
      Status of the alveolar bone after autotransplantation of developing premolars to the anterior maxilla assessed by CBCT measurements.
      ).
      Four out of five transplanted teeth presented periodontal healing without any complications during the observation period. External cervical resorption (ECR) was observed in one canine. The development of ECR is usually associated with damage to the periodontal ligament on the root surface during the surgery and not due to the status of the pulp (
      • Patel S
      • Mavridou AM
      • Lambrechts P
      • Saberi N
      External cervical resorption‐part 1: histopathology, distribution and presentation.
      ). The lesion was detected at the cervical part of one canine, which was considered a typical place of occurrence of ECR. The lesion did not correlate to the apex resection procedure performed during transplantation, but rather to iatrogenic trauma to the cervical region during autotransplantation surgery. ECR can also be triggered with orthodontic treatment. The orthodontic treatment in a traumatized tooth is usually not recommended for at least six months after different types of traumatic injuries (
      • Kindelan SA
      • Day PF
      • Kindelan JD
      • Spencer JR
      • Duggal MS
      Dental trauma: an overview of its influence on the management of orthodontic treatment. Part 1.
      ). Autotransplantation of a tooth may be considered as a controlled trauma to the donor. Both periodontal and pulpal healing are monitored afterwards with the possibility of developing some complications. From this point of view, the orthodontic movement of a transplanted canine could only be considered at a minimum of six months after the surgery. In a single patient diagnosed with ECR, the orthodontic movement of the canine was initiated two months after the autotransplantation. In retrospect, it may have been carried out too early. ECR is occasionally found in the transplanted teeth but can be treated if it is detected early. Successful treatment of resorption lacunae was previously described in cases of ECR in the autotransplanted teeth (
      • Szemraj-Folmer A
      • Kuc-Michalska M
      • Plakwicz P
      Patient with asymmetric multiple hypodontia treated with autotransplantation of 2 premolars.
      ). Similarly, the treatment of the lesion was performed in the affected canine and a stable satisfactory outcome was observed after one year.
      Radiographic examination of the canines was based on the periapical radiography technique and allowed to periodically monitor the healing of the pulp and periodontal ligament without unnecessary exposure to larger doses of radiation, which are associated with other techniques such as panoramic radiographs or Cone Beam Computed Tomography. The use of periapical radiography technique proved its effectiveness in early detection of ECR in one of the transplanted canines.
      The small sample size is the main limitation of this study. Limited number of cases occurred, firstly, due to relatively small number of patients with indication for this type of treatment, and secondly, because autotransplantation with root resection was quite a novel approach. In fact, the description of this technique was first published by Jakse (
      • Jakse N
      • Ruckenstuhl M
      • Rugani P
      • Kirnbauer B
      • Sokolowski A
      • Ebeleseder KJ
      Influence of extraoral apicoectomy on revascularization of an autotransplanted tooth: A case report.
      ) three years after the first patient was treated in the presented study.
      Until now, the typical protocol for the autotransplantation of mature teeth included a root canal treatment performed before or shortly after the surgery, because revascularization of the pulp in transplanted mature teeth was deemed impossible or at least not expected.
      For this reason, a technique allowing revascularization in mature transplanted teeth would potentially play an important role in increasing the likelihood of survival of vital transplants without pulpal complications. The limitations related to autotransplantation of teeth with complete root development could be overcome by modification of the standard surgical protocol. Future studies should focus on determining if other types of mature teeth can undergo revascularization after autotransplantation with partial root resection.

      CONCLUSIONS

      The mature autotransplanted canines, with partially resected roots, presented radiological features of pulp obliteration, which indicated revascularization of the pulp after the surgery. No bone or root pathology associated with inflammatory root resorption or pulp necrosis was detected. The surgical protocol proved to be successful in protecting the periodontal ligament in four cases. One complication related to the root surface was detected. The outcomes of the study demonstrate that root resection at the time of autotransplantation may maintain the vitality of mature ectopic canines and possibly other types of mature teeth.

      Acknowledgements:

      The authors gratefully acknowledge Ms.<blinded>, BSc, for her help in language editing of the manuscript. The authors have no conflict of interest regarding the study and have nothing to disclose.

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