Case Report/Clinical Techniques

Periradicular Regenerative Surgery in a Maxillary Central Incisor: 7-year Results Including Cone-beam Computed Tomography Stella Kourkouta, DipDS, MMedSci, FDS RCS, MRD RCS, FDS (Rest Dent) RCS Eng,* and Graham C. Bailey, BDS, MSc (Endo)† Abstract Introduction: A case of a symptomatic maxillary central incisor that underwent periradicular regenerative surgery with a successful long-term clinical and radiographic outcome is presented. Methods: A 52-year old woman was referred to the Endodontology Clinic, UCL Eastman Dental Institute and Hospital, London, UK, in 2004 for swelling and discoloration of the maxillary right central incisor. There was a history of trauma 21 years previously. The tooth was endodontically treated 5 years before the referral. At presentation, there was diffuse facial swelling/erythema and a periodontal probing depth of 11 mm on the midfacial surface with bleeding on probing and purulent exudate. Endodontic retreatment was completed along with subgingival debridement. Reassessment at 6 weeks showed persistent purulent exudate and a probing depth up to 13 mm facially. Periradicular surgery was performed for the purposes of surgical exploration, apical resection and root-end filling with mineral trioxide aggregate, and guided tissue regeneration using a bone xenograft and collagen membrane. Histopathology confirmed the presence of a radicular cyst. Results: Clinical and radiographic evaluation, including conebeam computed tomographic imaging, at 7 years postoperatively showed a probing depth up to 3 mm and hard tissue formation apically, interproximally, and partly facially on the root surface. Conclusions: In this case of a combined endodontic-periodontic lesion in a maxillary central incisor, regenerative periradicular surgery led to the resolution of the defect, significant attachment gain, and a stable clinical and radiographic outcome after 7 years of follow-up. (J Endod 2014;-:1–7)

Key Words Apical pathology, apical periodontitis, apical surgery, apicoectomy, combined endodontic-periodontic lesion, cone-beam computed tomographic imaging, guided tissue regeneration, periradicular surgery, radicular cyst, regenerative surgery

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ndodontic surgery is indicated in cases of failure after endodontic treatment/retreatment or when orthograde treatment is not feasible. The application of tissue engineering principles in the form of guided tissue regeneration (GTR) has shown favorable outcomes mainly in apicomarginal defects (1, 2) but also in large periapical lesions and throughand-through lesions (3–5). Cone-beam computed tomographic (CBCT) imaging is increasingly used in endodontic practice to aid in diagnosis, treatment planning, and follow-up based on highresolution 3-dimensional evaluation. CBCT imaging is considered more accurate than conventional radiography in the assessment of root canal morphology (6) and root fractures (7) and the detection of apical pathosis (8). We present a case of a symptomatic maxillary central incisor with a history of trauma that underwent endodontic retreatment followed by periradicular regenerative surgery with a successful clinical and radiographic outcome after 7 years of follow-up. To our knowledge, no case has been reported in the literature showing long-term results, including CBCT imaging, in this type of surgery.

Methods A 52-year-old woman was referred to the Endodontology Clinic, UCL Eastman Dental Institute and Hospital, London, UK, in 2004 with the chief complaint of swelling and discoloration of the maxillary right central incisor. There was a history of trauma 21 years previously at which time painless swelling developed. (Based on the history the patient gave, the tooth had most likely suffered concussion/subluxation; she was hit by her dog during a visit to the veterinarian.) The tooth was endodontically treated 5 years before the referral, but the swelling persisted. At presentation, there was diffuse facial swelling/erythema associated with the maxillary right central incisor but no tenderness to palpation (Fig. 1A–D). A probing pocket depth (PPD) of 11 mm was present on the midfacial surface with bleeding on probing and purulent exudate. Radiographic examination showed the presence of a dense root filling, which was underextended by approximately 1.5 mm, and suspicion of a root fracture apically. A diagnosis was made of previous endodontic treatment with a chronic apical abscess of the maxillary right central incisor and was classified as a combined endodontic-periodontic lesion. In addition, the patient was nervous about dental treatment. Endodontic retreatment was completed along with subgingival debridement. Local anesthesia was administered by buccal infiltration of 2.2 mL lidocaine hydrochloride 2% and 1:80,000 epinephrine at the start of each visit, and rubber dam isolation was applied throughout the retreatment process. Access was obtained using the operating microscope, and the existing Thermafil (Dentsply Maillefer, Ballaigues, Switzerland) was removed. Chemomechanical preparation followed using K hand files (Dentsply Maillefer)

From the *Restorative Division and †Unit of Endondontology, UCL Eastman Dental Institute and Hospital, London, United Kingdom. Address requests for reprints to Dr Stella Kourkouta, Restorative Division, UCL Eastman Dental Institute and Hospital, 256 Gray’s Inn Road, London WC1X 8LD, UK. E-mail address: [email protected] 0099-2399/$ - see front matter Copyright ª 2014 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2013.10.007

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Figure 1. The maxillary right central incisor at presentation: (A) facial swelling and erythema, (B) exudate, (C) the periodontal probing depth, and (D) the periapical radiograph.

to ISO size 40 apically and a 0.5-mm step-back technique irrigating with 5% NaOCl, 17% EDTA, 10% iodine, and 2% chlorhexidine. Patency was maintained throughout (ISO size 6). Subgingival debridement of the root surface was performed using a piezoelectric ultrasonic unit (EMS Piezon; EMS Electro Medical Systems SA, Nyon, Switzerland). Ca(OH)2 was placed as the intracanal medicament, and obturation was performed during the third visit using a customized cone/cold lateral compaction technique (gutta-percha and zinc oxide/eugenol sealer); the master cone was customized apically by dipping it in chloroform, and accessory points were inserted and compacted laterally. This was followed by energized ultrasonic spreading in which further compaction was achieved with the application of ultrasonic energy (9), vertical compaction coronally with the use of Touch ’n Heat (SynbronEndo Corp, Orange, CA), and placement of intermediate restorative material (IRM; Dentsply DeTrey GmbH, Konstanz, Germany) in the canal orifice and IRM provisional restoration in the access cavity (Fig. 2A and B). Reassessment after 6 weeks showed persistent purulent exudate, slight tenderness on palpation but no tenderness to percussion, mobility grade 1, and PPD up to 13 mm facially (Fig. 2C and D). Radiographic examination showed extensive periradicular bone loss associated with the right maxillary central incisor. The decision was made to proceed with exploratory surgery because there was suspicion of a root fracture. The tooth was splinted preoperatively using twist-flex wire bonded to the palatal surfaces of the maxillary anterior teeth (Fig. 2E). This was done for 2 reasons: 1. To provide stabilization during the healing phase in view of the anticipated extensive bone loss 2

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2. In case the prognosis was determined to be hopeless, the root could be resected and the crown used as an immediate resin-bonded bridge to provide temporization postoperatively The wire was accommodated relatively easily palatally because of the increased overjet and complete overbite in this case. (The incisal edges of the mandibular incisors were in contact with the palatal mucosa behind the maxillary incisors.) Periradicular surgery was performed under local anesthesia as follows (Fig. 2F–L): 1. Surgical exploration 2. Apical resection and root-end filling with mineral trioxide aggregate (MTA) 3. GTR using an anorganic bovine bone mineral and porcine resorbable collagen membrane (Bio-Oss/Bio-Gide; Geistlich Pharma AG, Wolhusen, Switzerland) Local anesthesia was obtained by buccal and palatal infiltration of 8.8 mL lidocaine hydrochloride 2% and 1:80,000 epinephrine throughout the procedure. A full-thickness mucoperiosteal triangular flap was reflected at the base of the papillae, extending from the maxillary right lateral to the left central incisors; the vertical incision was placed on the distal side of the right lateral incisor. There was extensive periradicular bone loss associated with the maxillary right central incisor. No facial, apical, or interproximal bone was present (von Arx and Cochran Class IIb according to the von Arx and Cochran classification (10)), and the defect was extending to the mesial surface of the root of the adjacent lateral incisor. Granulation tissue was curetted and sent

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Figure 2. The case during treatment: (A) purulent exudate from the periodontal pocket at the obturation visit, (B) the final periapical radiograph after endodontic retreatment, (C) purulent exudate at the 6-week reassessment, (D) the probing depth at the 6-week reassessment, (E) preoperative splinting, (F) purulent exudate on the day of operation, (G) facial/apical/interproximal bone loss and methylene blue staining of the root, (H) apicoectomy, (I) the intraoperative radiograph, (J) the placement of xenograft (Bio-Oss), (K) the placement of collagen membrane (Bio-Gide), and (L) healing 4 weeks postoperatively.

to histopathology. Methylene blue staining showed multiple cracks in the apical two thirds of the root surface facially, but no complete fracture was detected. The apical 3 mm were resected using a Lindemann bur (Hu-Friedy Manufacturing Co, Chicago, IL), and the root end was prepared with KiS microsurgical ultrasonic diamond tips (Obtura Spartan, Earth City, MO) and filled with MTA. The prominence of the root surface was reduced facially with an Arkansas stone (Shofu Dental Corp, San Marcos, CA) in an effort to produce a more contained bone defect, and Bio-Oss/Bio-Gide was applied. No additional retentive means were required for stabilization of the membrane. The flap was repositioned after incising the periosteum at the base of the flap to obtain tension-free closure and sutured with multiple interrupted 5/0 monofilament sutures. The patient was advised to avoid rinsing JOE — Volume -, Number -, - 2014

for 24 hours, pain control and oral hygiene instructions were given, and she was reviewed 6 days postoperatively. There had been minimal pain and localized swelling, which resolved by the time of the review. Chlorhexidine debridement was performed, and all sutures were removed. A soft postsurgical toothbrush was provided along with oral hygiene instructions, and the patient was further reviewed at 1, 2, and 6 months postoperatively. Histopathology results confirmed the presence of a radicular cyst. Healing progressed uneventfully. The postoperative follow-up indicated resolution of the inflammation/infection, facial recession of 2 mm, maximum PPD of 3 mm, and no mobility. A radiographic examination 6 months postoperatively showed resolution of the preoperative radiolucency and a radiopaque/granular appearance, presumably caused by

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Figure 3. The case 6 months postoperatively: (A) the periapical radiograph, (B) after internal whitening, (C) a probing depth of 3 mm, and (D) the palatal view.

the presence of Bio-Oss (Fig. 3A). The splint was removed 6 months postoperatively, and internal whitening was performed at that stage. Three visits were required for the whitening; during these visits, sodium perborate was applied weekly internally and carbamide peroxide 35% chairside. The access cavity was subsequently restored with glass ionomer cement within the pulp chamber and composite resin coronally (Fig. 3B–D). The patient was subsequently followed up at regular intervals. Her general dental practitioner identified chronic periodontitis (localized severe) approximately 3 years postoperatively and extracted the mandibular left second and third molars. The maxillary right third molar was subsequently scheduled for extraction.

Results A clinical and radiographic assessment 7 years postoperatively confirmed a stable outcome (Fig. 4A–G). CBCT (i-CAT, voxel dimension 0.2 mm; Imaging Sciences International, Hatfield, PA) showed the presence of radiopaque tissue apically, interproximally, and partly facially. The tissue appeared well integrated although it was slightly more radiopaque and granular compared with the adjacent bone. The density of the newly formed tissue apically was assessed using Hounsfield units (HUs). It was mostly over 1250 HUs and resembled the density of the cortical bone of the hard palate; it was much higher than the density of the adjacent maxillary bone (400–1100 HUs). Repeated linear measurements were taken parallel to the long axis of the root and compared with the anticipated bone level based on the appearance of the left central incisor (3.5 mm apical to the cementoenamel junction) and showed 45% of the anticipated root coverage midfacially. The average measurements were as follows: CEJ to anticipated bone level = 3.5 mm Anticipated bone level to actual bone level = 3 mm Bone level to root end = 2.5 mm 4

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Discussion This is a case of a successful clinical and radiographic outcome 7 years postoperatively in a previously symptomatic maxillary central incisor diagnosed with a combined endodontic-periodontic lesion. Regenerative surgery was performed as a last resort but led to a stable result up to the 7-year recall. Replacement of the tooth with a dental implant or removable partial denture would have been difficult because of the lack of bone and complete overbite. In addition, the patient wished for the tooth to be retained and preferred to avoid extensive treatment because of her dental phobia and costs. She coped well with the treatment. The favorable factors in this case were the following: 1. No mobility or low mobility pre- and perioperatively (maximum grade 1); had the tooth been more mobile, it is likely that the decision would have been made to proceed with extraction 2. No purulent discharge from the root canal; it was only through the periodontal pocket 3. Nonrigid splinting immediately preoperatively and for 6 months during healing 4. Average smile line, which was forgiving for the 2 mm of facial recession (compared with 1 mm on the adjacent central incisor at the 7-year follow-up and up to 4 mm in the other teeth) It is of interest that no antimicrobials were prescribed in this case, either pre-, peri-, or postoperatively, in line with the normal protocols at this dental hospital. The presence of a radicular cyst in this case, which was confirmed by histopathological examination, potentially explains the nonresolution after endodontic retreatment and supports the surgical intervention. Interestingly, it appears debatable whether CBCT imaging can provide a differential diagnosis between cysts and granulomas (11, 12). It has been suggested that CBCT imaging may be more JOE — Volume -, Number -, - 2014

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Figure 4. The 7-year follow-up: (A) smile, (B) the facial view, (C) recession of 2 mm, (D) maximum PPD of 3 mm, (E) the periapical radiograph, (F) CBCT scan of the right maxillary central incisor, and (G) CBCT scan of the left maxillary central incisor showing the anticipated midfacial bone level.

accurate in diagnosing cavitated lesions that would require surgical excision based on a positive or negative grayscale value (12). However, it appears that surgical excision and histopathology remain the standard procedures for differentiating radicular cysts from granulomas because CBCT imaging is not considered a reliable diagnostic method for this purpose at this time (13). Traditionally, total buccal bone loss in apical surgery, as observed in the so-called apicomarginal defects, is associated with considerably lower successful outcomes compared with cases with an intact buccal bone plate (ie, 37% (14) or as low as 27.3% (15)). However, with the wider application of GTR techniques, there have been many case reports of clinically successful outcomes in questionable teeth, confirming new tissue formation at re-entry in the case of nonresorbable membranes and showing radiographic resolution and even histologic evidence of tissue regeneration apically (16, 17). A prospective clinical study comparing the outcomes of endodontic microsurgery in cases of isolated endodontic lesions compared with lesions of endodontic-periodontic origin in which a combination of calcium sulfate and Collatape (Zimmer Dental, Carlsbad, CA) were applied to the periradicular defects showed successful outcome rates of 95.2% and 77.5%, respectively, at the 1- to 5-year postoperative follow-up (18). In the present case, a bone substitute was used mainly as a space filler to support the overlying membrane in such an extensive bone defect and also potentially as a scaffold to provide osteoconductive properties for new bone formation. Resorbable membranes are expected to provide wound stabilization for 6–8 weeks, and considering that the critical phase of healing is 2 months, their function as a barrier seems to be adequate (19). However, we do not know how a nonresorbable membrane might have behaved in this case, both in terms of postoperative complications and tissue gain, or whether adding autogenous bone to the graft and/or using a doublelayer Bio-Gide might have had an added benefit in terms of bone JOE — Volume -, Number -, - 2014

regeneration (20–22). The combination of Bio-Oss/Bio-Gide has been applied extensively in periodontal and implant surgery with positive outcomes. Human histologic studies have shown periodontal regeneration in intrabony defects (23, 24). Britain et al (25) showed that the treatment of combined induced periodontic-endodontic lesions in a canine model using Bio-Gide alone or in combination with Bio-Oss resulted in increased amounts of bone and periodontal ligament and a significant increase in new cementum when compared with open flap debridement alone. The xenograft particles were well incorporated in the host bone in some specimens although in others they appeared to be surrounded by connective tissue. However, it appears that the most critical factor for tissue regeneration in such lesions is the application of the membrane rather than the use of a bone grafting material (25). Interestingly, the application of the GTR principle in apical lesions does not seem to offer any added benefits over control sites (26, 27). Bone formation and cementum regeneration seem rapid in endodontic surgery; in fact, it appears that use of a bone substitute may be associated with less new bone formation and is not generally recommended (28, 29). MTA was used as the root-end filling material because of its superior properties in terms of lack of inflammation, tissue biocompatibility, osteogenesis, periodontal ligament regeneration, and cementogenesis (28, 30, 31). A study by Bernabe et al (32) showed that the use of membranes and bone graft materials isolated or associated in apical surgery did not alter the periapical healing process after root-end filling with MTA. Hard tissue formation apically, interproximally, and partly facially was confirmed by CBCT imaging 7 years postoperatively. To our knowledge, no similar report exists in the literature showing long-term CBCT results. Interestingly, a study comparing conventional radiography and CBCT assessment of the periapical bone defect 1 week and 12 months postoperatively showed that more defects were detected on CBCT scans

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Case Report/Clinical Techniques than on periapical radiographs (33). Approximately 45% of the anticipated bone coverage was observed midfacially; however, in a defect of this type, this is the longest distance for the progenitor cells to travel. In addition, we do not know what level of coverage might have existed in earlier years. Long-term outcomes of apical microsurgery show reduced success rates over time (ie, 75.9% after 5 years compared with 83.8% after 1 year (34)) and a 93.3% maintenance of successful healing after a period of over 6 years in a cohort that also included 31 cases of endodontic-periodontic origin out of a total of 172 cases (35) (overall, a 7%–8% worsening in prognosis after 5–6 years). The hard tissue that formed apically, interproximally, and facially in this case appeared slightly more radiopaque, dense, and granular compared with the adjacent bone, presumably because of the persistence of the xenograft, but there seemed to be good integration with the adjacent bone structure. On the facial and apical root surfaces, there was a minor space between the new tissue and the root, which was wider than normal periodontal ligament space as it appeared on CBCT imaging. It is likely that this space is filled with fibrous tissue. The shallow probing depth (3 mm as opposed to 13 mm preoperatively) in combination with hard tissue formation mainly in the apical part of the root most likely suggest regeneration apically and the presence of connective tissue and junctional epithelial attachment coronally. Without histologic examination, it is impossible to know to what extent this attachment consists of connective tissue fibers (also their orientation) or junctional epithelium, in addition to what extent cementum is covering the previously exposed root surface. However, it has been shown in a dog model that apicomarginal defects in which a membrane had been applied were associated with significantly more connective tissue attachment unrelated to the presence of regenerated alveolar bone (19) and increased cementum formation (25); it was also shown that apical bone regenerated more consistently than coronal alveolar bone (19). The soft tissue attachment has been stable for 7 years so far with a 2-mm recession midfacially compared with 1 mm in the adjacent central incisor. This is despite some posterior sites having been affected by localized periodontal inflammation and even tooth loss when no periodontal disease was present upon the initiation of treatment. This stresses the importance of regular follow-up and appropriate management in order to maintain a successful outcome in a case like this in which the newly formed attachment might be threatened by periodontal inflammation unless appropriately addressed.

Conclusion Periradicular regenerative surgery in this case of a radicular cyst associated with the right maxillary central incisor led to a successful clinical and radiographic outcome 7 years postoperatively including a lack of mobility; a facial recession of 2 mm; a probing depth up to 3 mm; the absence of bone defects; and hard tissue formation apically, interproximally, and partly facially on the root surface as confirmed by conventional radiography and CBCT imaging.

Acknowledgments The authors deny any conflicts of interest related to this study.

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Case Report/Clinical Techniques 28. von Arx T, Britain S, Cochran DL, et al. Healing of periapical lesions with complete loss of the buccal bone plate: a histologic study in the canine mandible. Int J Periodontics Restorative Dent 2003;23:157–67. 29. Bergenholtz G, Wikesjo UM, Sorensen RG, et al. Observations on healing following endodontic surgery in nonhuman primates (Macaca fascicularis): effects of rhBMP-2. Oral Surg Oral Med Oral Path Oral Radiol Endod 2006;101:116–25. 30. Parirokh M, Torabinejad M. Mineral trioxide aggregate: a comprehensive literature review—part III: clinical applications, drawbacks and mechanism of action. J Endod 2010;36:400–13. 31. Baek SH, Plenk H Jr, Kim S. Periapical tissue responses and cementum regeneration with amalgam, SuperEBA, and MTA as root-end filling material. J Endod 2005;31:444–9.

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32. Bernabe PF, Gomes-Filho JE, Cintra LT, et al. Histologic evaluation of the use of membrane, bone graft, and MTA in apical surgery. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:309–14. 33. Christiansen R, Kirkevang LL, Gotfredsen E, et al. Periapical radiography and cone beam computed tomography for assessment of the periapical bone defect 1 week and 12 months after root-end resection. Dentomaxillofac Radiol 2009;38:531–6. 34. von Arx T, Jensen SS, H€anni S, et al. Five-year longitudinal assessment of the prognosis of apical microsurgery. J Endod 2012;38:570–9. 35. Song M, Chung W, Lee SJ, et al. Long-term outcome of the cases classified as successes based on short-term follow-up in endodontic microsurgery. J Endod 2012; 38:1192–6.

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Periradicular regenerative surgery in a maxillary central incisor: 7-year results including cone-beam computed tomography.

A case of a symptomatic maxillary central incisor that underwent periradicular regenerative surgery with a successful long-term clinical and radiograp...
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