Abstract

Background: This article reports on a case of extraosseous inflammatory lesion of endodontic origin (EILEO) that was recalcitrant to nonsurgical root canal treatment and was caused by a complex intraradicular and extraradicular bacterial infection.

Case description: The histopathological and histobacteriological aspects of the biopsy specimen were evaluated. The affected tooth was a mandibular premolar that exhibited an abraded crown with exposed dentin and enamel cracks, but no caries. The patient reported previous abscess episodes and presented with symptoms and a sinus tract. Nonsurgical root canal treatment was not effective in controlling infection, even after using ultrasonic agitation of irrigants and intracanal medication. Surgery was indicated and the biopsy specimen including the extraosseous extension was processed for histopathological and histobacteriological analyses. Bacterial infection in the form of biofilms and planktonic cells was observed not only in the main apical root canal, but also in ramifications and extending to the extraradicular environment. The intraosseous part of the lesion showed severe inflammation in the areas surrounding the root apex and the extraradicular biofilms. The extraosseous tissue showed an abundance of collagen fibers externally, and inflammatory tissue layering the sinus tract internally.

Conclusion: EILEO can be regarded as a different manifestation of apical periodontitis and its prevalence and clinical implications remain to be clarified.

Introduction

Apical periodontitis is an inflammatory disease caused by bacterial infection of the root canal system (Ørstavik 2020). The disease may have different clinical manifestations, but radiographically it is usually associated with a radiolucent area in the bone tissue apically or laterally to the root. This is caused by bone resorption that affects the cancellous and, in many cases, can evolve to perforate the cortical plate (Jalali et al. 2019). In these cases, this often represents the most peripheral part of the lesion, but the possibility exists that the lesion can expand through the submucous tissue. In addition, given the anatomic position of the root apex and/or the presence of fenestration, the possibility exists that the inflammatory lesion can develop directly in the submucous tissue and spread to the extraosseous soft tissue. Therefore, an extraosseous inflammatory lesion of endodontic origin (EILEO) can extend from an intraosseous apical periodontitis lesion or form exclusively outside the bone. These lesions are sometimes not visible radiographically and have been associated with persistent pain and/or infection following nonsurgical endodontic treatment (Shneider, 2021).

While these concepts have been demonstrated with multiple cases in lecture and webinar format (Shneider, 2021), this article represents the first written report on a case of EILEO that was recalcitrant to nonsurgical root canal treatment and was caused by a complex intraradicular and extraradicular bacterial infection. The histopathological and histobacteriological aspects of the biopsy specimen were evaluated.

Case report

A 77-year-old woman was referred by her general dentist to an endodontist for an abscess occurring in her mandibular left region. The patient reported that there had been repeated abscess episodes in the last year, with swelling on the buccal gingiva, moderate pain, and occasional discharge of purulent material. She declared that these episodes were treated with antibiotics.

Upon examination, the lower teeth showed generalized occlusal wear, and the patient confirmed a parafunctional habit of grinding her teeth. At inspection, a tumefaction was present on the gingiva, buccally to mandibular left premolars, with a sinus tract discharging pus at the base of gingival papilla between the first molar and second premolar (Fig. 1 A). The occlusal surface of the first premolar appeared severely abraded, with exposure of dentin, and crack lines in the surrounding enamel (Fig. 1 B). Tooth #21 was tender to lateral and vertical percussion and did not respond to thermal and electric pulp tests, while teeth #19, #20, and #22 responded normally to pulp tests and were negative to percussion. Periodontal probing did not exceed 2-3 mm for all mandibular left teeth. Palpation revealed a thickened mucosa buccally to premolars, with soft consistency. It also caused a moderate painful response and pus discharge through the sinus tract.

A periapical radiograph revealed a round periradicular radiolucency, measuring 6 x 5 mm, around the apex of the mandibular first premolar (Fig. 1 C). The diagnosis of necrotic pulp and chronic apical abscess was made for tooth #21. Root canal treatment was scheduled. All procedures were carried out under an operating microscope (CJ-Optik, Flexion Advanced, Asslar, Germany). After rubber dam isolation and field disinfection with 30% H₂O₂, an access cavity was prepared, and working length was established using an electronic apex locator (Apex ID, SybronEndo, Glendora, CA, USA). A slight apical curvature was noted in a distal direction. The single root canal was prepared with rotary nickel-titanium instruments Protaper Next (Dentsply Tulsa Dental Specialties, Tulsa, OK, USA) to a master apical file X3. Irrigation was performed with copious amounts of 5.25% sodium hypochlorite (NaOCl) (Chloraxid 5,25%, PPH Cerkamed, Stalowa Wola, Poland) delivered by a 30G diameter needle (NaviTip, Ultradent, South Jordan, UT, USA). The canal was finally irrigated with 17% EDTA (CERKAMED, Stalowa Wola, Poland) to remove the smear layer, followed by a final rinse with NaOCl. These last two solutions were activated with ultrasonics for about 1 min each. The canal was dried with sterile paper points, and medicated with calcium hydroxide (UltraCal, Ultradent, South Jordan, UT, USA). The access cavity was temporized with a reinforced zinc oxide-eugenol cement (IRM, Dentsply International, Milford, DE, USA).

At the second appointment, one week later, the sinus tract was still open and active. Pus drained from the sinus tract upon palpation. The canal was reopened, and the intracanal medication removed with irrigation and hand files. The canal was reinstrumented, increasing the apical size up to Protaper Next X4. The irrigation protocol was repeated with NaOCl and EDTA, both solutions being activated ultrasonically. At the end of the appointment, the canal was dried. It was packed once again with UltraCal (Ultradent, South Jordan, UT, USA), and the access sealed as above.

After two more weeks, the situation was unchanged, with pus still draining from the sinus tract, and the patient reported a feeling of discomfort. At this point, because the condition was refractory to nonsurgical root canal procedures for infection control, apical microsurgery was deemed as necessary. The patient agreed, after being fully informed about the procedure and the possible risks.

After rubber dam isolation, the intracanal medication was removed, and the canal was filled with hydraulic compaction of a bioceramic sealer (Endosequence BC Sealer, Brasseler, Savannah, GA, USA) and a single gutta-percha point. The access cavity was filled with SDR^® flow+ (Dentsply Sirona, Charlotte, NC, USA) and a nanoceramic composite (Ceram.X, Dentsply Sirona). A postoperative radiograph revealed the separated tip of a #10 K-file apical to the canal filling (Fig. 1 D).

Apical surgery was scheduled four months after completion of the RTC treatment, for patient convenience. The day of surgery, the patient declared that in the period after root canal obturation, the tooth had caused only mild discomfort, and that she constantly felt the taste of pus draining from the sinus tract. At examination, the sinus tract was present, proximal to the mesial aspect of the first molar, with pus discharging at palpation. A gutta-percha cone was inserted into the sinus tract (Fig. 1 E) and a radiograph taken. This showed that the cone pointed mesially, ending to the radiolucency located around the apex of the first premolar (Fig. 1 F).

Before surgery, amoxicillin (1g) and ibuprofen (600 mg) were administered. Local anesthesia was obtained by infiltration with two cartridges of Articaine with epinephrine (1:100.000). A modified Kirkland intrasulcular incision with an angled relieving incision mesial to the canine was made. During flap elevation, a strand of granulation (inflammatory) tissue was identified, approximately 15 mm in length, extending from the tract exit to the apical region of the first premolar (Fig. 1 G). This tissue originated from an opening in the cortical plate, adjacent to the apex of the first premolar (Fig. 1 G). This could be easily separated from the overlying periosteum by means of blunt dissection. When detached from the bone, a shallow superficial depression on the cortical plate was observed (Fig. 1 H).

Osteotomy was performed with piezo driven inserts (Piezo surgery, Mectron S.p.A., Loreto, Italy) protecting the soft tissue bundle arising from the mental foramen, and the apex located. The strand of inflammatory tissue grown on the cortical plate was found to be continuous with the periapical pathologic tissue (Fig. 1 I). Apicoectomy was carried out and this revealed that the mass of inflammatory tissue was composed of an intraosseous portion continuous with an extraosseous portion, located between the cortical plate and the periosteum (Fig. 1 I). The resected apex could be removed with the entire mass of pathologic tissue attached (Fig. 2 A).

A retrograde cavity was prepared using an ultrasonic tip, and sealed with a bioceramic material (MTA Angelus, Angelus, Londrina, Brazil). After the bone cavity was filled with blood, the flap was sutured. No bone grafts or membranes were used. A radiograph was taken and postoperative instructions were given to the patient as per routine.

The patient gave consent for histologic analysis of the excised tissue. The biopsy consisting of the long strand of soft pathologic tissue attached to the root tip was immediately immersed in fixative for histologic processing.

Healing of the sinus tract wound was evident when sutures were removed seven days later, but the patient experienced numbness in the left side of the lower lip and corner of the mouth. The patient did not experience pain after surgery and took all prescribed antibiotics. Numbness disappeared spontaneously within the successive three months.

A follow-up radiograph after 1 year showed that the lesion had healed completely, with new bone filling the cavity. Numbness had subsided, and the tooth was asymptomatic.

Histological processing

Immediately after retrieval, the soft pathologic tissue was immersed in 10% neutral buffered formalin solution for 48 hours. Photographs of the biopsy were taken after fixation (Fig. 2 A). Using a sharp razor blade, the longest part of the lesion was separated, approximately at the transition from the intraosseous to the extraosseous portion. This tissue was not subjected to demineralization and was dehydrated in ascending grades of ethanol (50-100%), and then cleared in xylene. Serial sections parallel to the long axis of the pathologic mass were cut. The remaining portion consisting of the apex with the surrounding periapical tissue was demineralized in a solution consisting of 22.5% (vol/vol) formic acid and 10% (wt/vol) sodium citrate for 4 weeks. The end-point was determined radiographically. At the end of the demineralization process, the specimen was washed in running water for 24 hours and dehydrated in ascending grades of ethanol. Clearing in xylene followed.

The specimen was first embedded in paraffin so that cross sections of the apex could be cut starting from the resected surface in an apical direction.

Approximately 200 (5-μm thick) sections were cut. The specimen was then removed from the paraffin block and re-embedded, so that longitudinal sections encompassing the apical canal and foramen, in conjunction with the periapical tissue, could be obtained. Serial sections were cut until the specimen was exhausted. Sections were stained with hematoxylin and eosin, and the Taylor’s modified Brown and Brenn technique for staining bacteria (Taylor 1966).

The stained sections were examined using a light microscope (Leica DMLB; Leica Microsystems, Wetzlar, Germany), and photomicrographs were taken (Leica DFC420; Leica Microsystems).

Histopathological and histobacteriological results

Cross sections of the apical segment cut approximately 3 mm from the root tip showed that the whole circumference of the canal at this level had been adequately prepared with clean dentin walls. Residual masses of filling material were present in the canal. No bacteria could be observed in the canal lumen or within dentinal tubules (Fig. 2 B). Longitudinal serial sections of the apical segment revealed the presence of several apical ramifications (Figs. 2-3). During sectioning, it became evident that the separated file was blocked in one of these ramifications (Fig. 2 C). This fragment was removed from the paraffin block with the help of an operating microscope, so that serial sectioning could be performed with no loss of any part of the specimen. Sections encompassing the exit of one of these ramifications at the geometrical top of the root, revealed heavy infection both in the lumen and in the extraradicular compartment immediately adjacent to the foraminal region (Fig. 2 D-F). Bacterial biofilms were observed attached to the walls of the ramification or floating in its lumen (Fig. 2 E). Biofilms were also seen adhered to the resorbed external apical profile (Fig. 2 E), enmeshed with necrotic debris slightly beyond the foramen, and apparently free in the periapical pathologic tissue (Fig. 2 F). Other ramifications appeared clogged with thick bacterial biofilms (Fig. 3 A-D). Serial sections revealed that apical ramifications formed an intricate system, with intracanal infection fostering the extraradicular infection.

The periodontal tissue adjacent to the foraminal openings and surrounding the biofilms covering the apical surfaces was heavily inflamed, with severe concentrations of polymorphonuclear leukocytes (PMNs). More peripherally, chronic inflammatory cells predominated, fading into a pseudocapsule of fibrous tissue (Fig. 3 E-F).

Sections cut through the superficial part of the elongated pathologic tissue mass showed a predominance of the collagenous component, with dense collagen bundles and few scattered chronic inflammatory cells (Fig. 4 A-B). Sections cut at the center of the mass revealed a tortuous channel, which divided into several branches ending at the distal pole of the pathologic tissue strand (Fig. 4 C). Its lumen was partly filled with disintegrating red blood cells, necrotic debris, and inflammatory cells with different degrees of regressive changes (Fig. 4 D-F). The walls of this channel were lined by inflammatory tissue, with absence of epithelium (Fig. 4 D-F).

Discussion

In this article, we report on a case of EILEO that perforated the buccal cortical plate and spread to the soft submucous tissues. The lesion was recalcitrant to nonsurgical root canal treatment and was caused and maintained by a complex bacterial infection established in the apical root canal system, including ramifications, with an extraradicular component. The case was resolved by apical microsurgery.

The involved tooth had no caries and presented with a severely abraded occlusal surface probably caused by a parafunctional habit. Dentin was exposed and crack lines in the surrounding enamel were clearly evident. Dentinal tubules exposed by both abrasion and cracks are the most likely pathways for bacteria from biofilms colonizing these surfaces to reach the pulp and cause inflammation and further necrosis/infection (Love 1996, Ricucci et al. 2015a).

Persistent apical periodontitis is caused by residual infection in the root canal system, usually located in areas that are difficult or even impossible to reach with instruments and irrigants. In this particular case, the disinfection protocol included NaOCl irrigation, a supplementary approach with ultrasonic agitation of NaOCl and EDTA, and an interappointment medication with calcium hydroxide. These procedures have been largely recommended to improve root canal disinfection (Nakamura et al. 2018, Aveiro et al. 2020, Pereira et al. 2021, Loyola-Fonseca et al. 2023, Rôças et al. 2023). However, this protocol was still ineffective in controlling the complex bacterial infection established in the intricate apical root anatomy and extending to the extraradicular space. Infections reaching anatomic complexities in the apical root canal system and extraradicular areas are difficult to eliminate or control and have been reported to be the main cause of post-treatment disease even in apparently well-treated teeth (Ricucci & Siqueira 2008, Arnold et al. 2013, Ricucci et al. 2015b).

Lesions affecting the cortical plate have been commonly reported in cone-beam computed tomographic exams (Jalali et al. 2019, Saini et al. 2023), but little attention has been given in describing these conditions and its implications. In the present case, the lesion not only perforated the cortical bone but also extended to the adjacent soft tissue. The development outside the bone may be due to local factors, such as a locus of minoris resistentia and proximity of the root apex to the cortical bone. When a bone fenestration is present at the level of the root apex, the possibility exists that the inflammatory lesion can even develop in its entirety outside the bone, in the submucous tissues. In the case reported here, the patient had repeated previous episodes of abscess formation and presented with a sinus tract; whether or not these events preceded bone perforation and spread of the lesion to the soft tissues cannot be ascertained. Histopathologically, the tissue growing out of the bone was composed by an outer portion characterized by abundance of collagen fibers with only few aggregations of inflammatory cells, and an inner core of inflammatory tissue surrounding the tortuous channel of the sinus tract. It is noteworthy that no epithelium was observed lining the tract, similarly to what was described in a previous study (Baumgartner et al. 1984).

In conclusion, in some circumstances EILEOs can form exclusively outside the bone in the submucous soft tissues or as an extension of an intraosseous apical periodontitis lesion, as reported here. In the present case, the extraosseous component showed lower accumulation of inflammatory cells than the intraosseous component, but this may be a result of the tissue being more distant from the cause, i.e., the intraradicular/extraradicular infection. In cases of apical fenestration in which the lesion can form directly in the soft tissue, the histopathological results may be different. EILEO can be regarded as a different manifestation of apical periodontitis and further studies evaluating its prevalence and clinical implications should be encouraged.