Preserving the vitality of adjacent teeth by microsurgical enucleation of a large radicular cyst: A case report with 4-year follow-up

Background: Radicular cysts may enlarge considerably, cause extensive bone destruction, and jeopardize the integrity of the associated vital teeth. The different treatment approaches are aimed mainly at eliminating the cystic epithelial membrane while reducing the risk of injury to vital structures. Contrary to other treatment modalities, preapical surgery offers an unequivocal single occasion resolution for the patient. However, it has been associated with higher risk of collateral damages. Case presentation: When a patient presented with a large radicular cyst originating from a maxillary lateral incisor, the adjacent central and canine teeth initially failed to exhibit responses to sensibility tests but showed signs of vitality. Microsurgical management was aimed at enucleating the cystic membrane while maintaining adjacent teeth vitality by preserving their apical vascular supply. Upon careful and controlled cyst enucleation under the dental operating microscope, the neurovascular bundle of one of the involved teeth was visualized and its integrity was maintained throughout the procedure. Results: The procedure was successful and follow up recalls revealed recovery of normal sensibility of tooth 11 and 13 with complete bone regeneration around their apices. Conclusions: The ndings of this report demonstrate that teeth adjacent to radicular cysts albeit vital, may fail to respond to sensibility tests and that their vitality can be successfully preserved by utilizing the appropriate microsurgical techniques for direct cyst enucleation.


Background
Radicular cyst is the most common cystic pathology of the jaws [1]. It arises as a sequela of in ammatory processes of the pulp and periodontium from the epithelial rests of Malassez and may enlarge to considerable sizes while causing extensive bone destruction [2].
Vitality of non-offending teeth, whose apices protrude into the cystic lumen and are overlapped by the cystic membrane, is a pathognomonic sign of radicular cysts. The slow expansion growth of the cystic membrane resorbs the bone but de ects other structures including major nerves and apical neurovascular bundles of adjacent teeth, compromising their integrity [3], and leading to confounding diagnosis [4,5].
Management of radicular cysts includes non-surgical endodontic treatment of the causative tooth, marsupialization, and surgical enucleation [2]. Direct cyst enucleation by surgery precludes the prognostic uncertainty and patient's discomfort associated with the other treatment modalities, since no pathological tissues remain following treatment and the follow-up recalls monitor the progress of healing rather than the regression of an existing disease process. However, in surgical treatment of an extensive radicular cyst, the operator may be faced with the dilemma of having to pre-emptively devitalize the healthy neighbouring teeth. The rationale for the prophylactic treatment is to prevent of future periodontitis, as devitalization is considered inevitable while enucleating the cystic membrane [5].
However, due to the pivotal rule of the vital pulps in defence and repair and their inherent value as source of stem cells, all effort should be made to avoid unnecessary devitalization whenever possible [6]. Advancement in endodontic armamentarium and magni cation enhanced the clinicians' control over the treatments and improved the long-term outcomes [7]. If the vitality of the surrounding teeth is closely regarded during the surgery by carefully excising the cystic membrane covering their apices without disrupting their neurovascular supply, the advantages of both the surgical and conservative cystic treatments can be combined while their drawbacks minimized.
This case report describes the surgical enucleation of a large maxillary radicular cyst aimed at preserving the vitality of the associated teeth and the results of long-term follow-up.

Case Presentation
A 41-year-old woman was referred to the endodontic department at Mansoura University, Mansoura, Egypt, for evaluation of a periapical lesion related to the roots of maxillary right anterior teeth. The lesion was discovered inadvertently during routine radiographic examination. The patient had been asymptomatic, and her main complaint was related to di culties in mastication due to loss of multiple posterior teeth. Prior medical history was non-contributory. Clinical examination revealed a grossly decayed upper right lateral incisor (FDI tooth no. 12). The labial vestibular mucosa and the palate surrounding the tooth apex were compressible but not tender to palpation, indicating that they were undermined with no underlying cortical bone plates. Panoramic view radiography (Fig. 1) revealed a large well-de ned radiolucent area extending from the distal of tooth 13 to the mesial of tooth 11 and resembling a "through-and-through" bone defect. Teeth 13 and 11 were sound and were not sensitive to percussion or palpation. However, they both failed to exhibit responses to repeated sensibility tests performed with an electric pulp tester (EPT) (Denjoy Dental Co, Ltd, Hunan, China) and Endo-Ice (1,1,1,2 tetra uoroethane; Hygenic Corp, Akron, OH, USA) (contra laterals as control) and were deemed nonvital.
None of the examined teeth had any periodontal symptoms. Clinical and radiographic ndings were consistent with a representation of a radicular cyst originating from tooth 12. After critical appraisal of the clinical and radiographic ndings and discussion with the patient, surgical enucleation was elected to manage the periapical lesion. The patient was scheduled for root canal treatment of the involved teeth in preparation for the surgical intervention.
After informed consent and without anaesthesia, tooth 12 was accessed under rubber dam and emitted pungent odour revealing a necrotic pulp. The root canal was cleaned, and shaped while being irrigated with a frequently refreshed 5.25% sodium hypochlorite. The canal did not discharge cystic uid despite frequent encouragement of patency le through the apex and a nal irrigant activation by manual dynamic agitation. Following dryness, the canal was lled with guttapercha cones and TotalFill biocermaic sealer (FKG Dentaire SA, La Chaux-de-Fonds, Switzerland) (Fig. 1b). When access cavity was initiated for root canal treatment on tooth 11, which was diagnosed with pulpal necrosis, the patient unexpectedly exhibited sudden pain when the bur almost breached the pulpal space. The initial diagnosis of nonvitality for the central incisor and the canine was reconsidered, as both teeth were sound. The cavity was restored, and a decision was taken not to proceed with the planned root canal therapy.
All surgical procedures were performed using a surgical microscope (M320, Leica Microsystems, Heerbrugg, Switzerland), except the incisions, ap elevation, and suturing. 2% lidocaine (with 1:100,000 epinephrine) (Alexandria Co., Alexandria, Egypt) was administered and a full thickness buccal ap was elevated to reveal the cystic lining covering an extensive cortical bone defect. No osteotomy was needed.
After identi cation of tooth 12's root, a 3 mm apical cut was done under copious irrigation with sterile saline. The cystic lining was completely removed by careful dissection starting from the middle craniofacial defect edge and advancing in anteroposterior directions. The cystic membrane was peeled in downward motion along the osseous wall rather than being pulled away from it. Whenever needed, releasing incisions were made in the cystic membrane to facilitate its removal. Following enucleation, the cavity was examined, revealing expansion of the cyst buccally, palatally as well as in the direction of the nasal oor, exposing the nasal mucosa (Fig. 2a). The neurovascular bundle of tooth 11 was observed running from the apical foramen mesially toward the caudomedial defect wall (Fig. 2b). Due to the geometry of the defect in relation to tooth 13 root, similar observation was not possible. Thus, all subsequent procedures were done cautiously to avoid damages. The resected root surface was inspected, prepared, and then lled with pro root MTA (Dentsply/Tulsa Dental, Tulsa, OK, USA) (Fig. 2c). Prior to ap repositioning, the neurovascular bundle of tooth 11 was rechecked again to ensure its integrity (Fig. 2d). Primary mucoperiosteal closure on solid margins was accomplished with no releasing incisions and the ap was sutured with 4 − 0 polypropylene suture (International Sutures, Shrkia, Egypt). Postoperative instructions included a twice daily rinse with 0.12% chlorhexidine gluconate (Peridex, 3M ESPE, St Paul, MN, USA) for 1 week. The patient returned to remove the sutures with uneventful soft tissue healing and no reported complications. The histopathologic examination con rmed the initial diagnosis of an in ammatory radicular cyst.
At the 1-year follow-up, clinical examination revealed that teeth 13 and 11 regained normal responsiveness to EPT and cold sensibility tests. Panoramic radiograph demonstrated reduction in the defect size with partial bone ll around apices of teeth 13, 11 and up to the apicoectomy level of tooth 12's root (Fig. 3a). The 2-dimensional (2D) radiographic healing was judged incomplete by two independent and calibrated reviewers as per Molven's criteria [8]. However, it was in disagreement with the 3-dimensional (3D) healing outcome on the cone-beam computed tomography (CBCT) (Fig. 3b), as it was considered uncertain according to modi ed PENN 3D criteria. [9] As the patient reported absence of any discomfort related to the treated teeth or surgical site since the operation with normal soft tissue (Fig. 3c), a second recall appointment was set at the 4-year mark following the operation. Teeth 13 & 11 remained responsive to sensibility tests with normal signs of vitality four years after surgery. Periapical radiograph and CBCT demonstrated continued and signi cant reduction in the lesion size, indicating a change to an agreement between both the 2D and 3D radiographic healing criteria toward incomplete (limited) healing by scar tissue (Fig. 4). Complete regeneration of bone and periodontium around the apices of teeth 13, 11 was evident.

Discussion
Here, we demonstrated the successful preservation of the vitality of teeth involved with a large radicular cyst in anterior maxilla that was managed by a direct surgical enucleation approach.
Various reports identi ed extra radicular sources of irritations in cases of persistent radicular cysts [10,11]. Thus, both the radicular space and the cyst itself should be considered as individual potential sources of morbidity. Periapical surgery offers an unequivocal single occasion resolution for the patient, in which the two entities are treated simultaneously. Nevertheless, it requires a high level of operator skills and has a higher risk of complications including the possible injury to surrounding vital structures [12].
Magni cation and improved visualization by the dental operating microscope (DOM) in endodontic microsurgery enhance the ability of the operator to critically assess the anatomical features of the surgical eld, leading to accurate judgments and higher success [13]. Development of endodontic microsurgical armamentarium allowed a more precise control of the surgical procedure, reducing the incidence of complications [7]. Traditionally, vigorous removal of the cystic pathological tissue was advocated to rapidly establish haemostasis and reduce the operation time [14]. However, in our case, the magni cation by the DOM permitted carful and controlled excision of the pathological tissue and meticulous execution of the surgical technique while avoiding injury to the surrounding structures.
Furthermore, the detection of tooth 11 neurovascular bundle, immediately after enucleation of the cystic membrane (Fig. 2b) and before ap repositioning (Fig. 2d), allowed us to accurately predict the prognosis of vitality of one of the two vital teeth included in the cystic cavity. Response to sensibility testing in follow-up recalls and absence of periapical radiolucency, resorption, and coronal discoloration are ancillary evidence that support the maintenance of tooth 11 to vitality.
On the other hand, multiple studies discussed the fate of vital pulps when their apical neurovascular bundles were interrupted. Revascularization is possible following injury with various degrees of reparative and neurological events [15]. In our case, tooth 13 demonstrated partial calci c obliteration (PCO) at the follow-up investigations. In absence of other conditions, PCO is a sign of vascular repair following injury to the tooth supporting structure [16]. The deposited dentin is considered reparative, as it's formed by newly differentiated mesenchymal cells following odontoblasts degeneration secondary to the injury [17].
We noticed a near obliteration of coronal pulpal space at the 1-year follow-up radiographs (Fig. 3b). However, over the course of the following three years, the rate of calci cation was signi cantly reduced with only a slight narrowing of the radicular canal (Fig. 4c). The initial pronounced calci cation of the coronal pulp may be attributed to the tendency of in ammation to localize coronally after injury [17]. While reinstatement of the neural regulatory control over the newly differentiated odontoblast following neural regeneration, and reversal of hypoxic conditions in the pulp might have been the reasons of the limitation of calci cation [18,19]. Lundeberg & Cvek study [20] on PCO of traumatized teeth concluded that pre-emptive endodontic treatment is not warranted, based on the histological status of pulps undergoing calci cation. Anderson et al. [16] reported that secondary pulpal necrosis happened only to 1 % of teeth exhibiting PCO during a 1 to 10-year follow-up study, while Robertson et al. [21] calculated a 20-year pulp survival rate to be 84% for permanent teeth with calci ed pulps secondary to dental trauma., As the tooth is vital, the case remains under follow-up.
Guided tissue regeneration techniques utilized in periapical surgeries, are intended to improve the healing outcome in large osseous defects with resorbed cortices [22]. Usually, a membrane is used to cover an osteogenic material packed in a bone cavity. Although placing a membrane barrier might have been bene cial in this case, packing the grafting material in the defect cavity could have jeopardized the integrity of the vital teeth neurovascular bundles. This sighting adds a new factor to consider for the use of regenerative techniques in periapical surgeries.
Teeth 13 and 11 lacked positive responses to initial sensibility tests done by EPT and cold test but regained and maintained normal responsiveness following treatment at 1 and 4-year follow-up recalls.
This could be attributed to compression neuropathy [23]. Positive pressure is considered a key regulator of cystic growth [24]. It has been linked to initiation of bone resorptive mechanisms and to alterations in the physiology of the surrounding structures including the inferior alveolar nerve [4,24]. Previous reports showcased recovery of inferior alveolar nerve's sensory function following decompression of large cystic lesions and illustrated improved responsiveness of the innervated teeth [4,25]. Similarly, in our case, the direct pressure exerted on the periapical neurovascular bundles by the growing cyst might have led to reduced sensation and numbness of the two vital teeth included in the cystic cavity, while eliminating the pressure following cyst enucleation recovered the normal neural function and sensibility.
In neurological studies, reported pressures of 50 mm Hg and 60 mm Hg completely inhibited axonal transport function and interneural blood ow in rabbit vagus and tibial nerves, respectively [26,27]. In addition, a pressure value between 40 mm Hg and 50 mm Hg is considered a critical threshold for the disruption of peripheral nerves conduction and response to cutaneous sensibility tests in healthy patients [23,28]. Those values lie well within the + 47 and + 70 mm Hg means of measured intracystic pressures for radicular cysts [29,30], and a 51 mm Hg minimum continuous pressure necessary to induce bone resorption in the hard palate, based on animal experiment on rats [31].
Additionally, the patient sudden pain reaction while accessing tooth 11 further supports the compression theory. The larger myelinated A-type nerve bres are pressure and hypoxia sensitive compared with Ctype nerve bres [32]. The response to electrical and cold sensibility tests mediated by A-bres might have been suppressed, while the heat build-up and mechanical stimulation by the cutting bur caused a latent C-bre pain response [33]. Ricuccui et al. [5] reported a similar incident when two premolars, whose apices were compressed by large radicular cyst, only gave faint responses to cold sensibility tests, and did not respond to EPT but demonstrated vital pulps when they were endodontically treated. However, due to chronic caries and restorations in the premolars, direct conclusion could not be made. Interestingly, at multiple occasions when similar cases of large cysts and cystic like lesions were presented to our clinic, adjacent vital pulps were accessed without anaesthesia, demonstrating complete lack of sensation, especially in cases of secondary infections.

Conclusions
This report highlights the complexity of diagnosing pulp vitality of teeth whose apices are subjected to the pressure from an expanding periapical pathology. In such instance, neural response-based sensibility tests may give false negative results. Thus, the use of blood perfusion-based vitality testing is indicated. Endodontic microsurgical techniques can be utilized for direct cyst enucleation while preserving the adjacent teeth vitality. Even in case of injury to teeth apical vasculature while handling the cystic epithelium, repair may ensue.