Inflamed Odontogenic Cyst with Actinomyces Colonization: Management of an Atypical Case in a 16-Year-Old Patient

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Ahmad Soolari, DMD, MS1 Odontogenic cysts arise from pro- Amin Soolari, BS, CRT2 liferation of remnants of the epi- Christopher Fielding, DDS3 thelial rests of Malassez, stimulated by inflammation that results from pulpal necrosis of an associated tooth that expanded by hydrostatic Inflammatory odontogenic cysts, if not treated, may lead to progression pressure/osmotic gradient, lead- of osteolytic activity, potential paresthesia, and loss of teeth. A 16-year-old ing to fluid transport.1 Interleukin-1, female patient was referred by a pediatric dentist for asymptomatic abnormal interleukin-6, and tumor necrosis radiolucency found interproximally to the mandibular left first and second factor alpha are important proin- premolars. Radiographic, clinical, and pathologic analyses led to a diagnosis of an inflamed odontogenic cyst (type K09.0) with Actinomyces colonization. The flammatory cytokines released by cyst was treated by periodontal regenerative therapy and resulted in successful macrophages,2 and this inflamma- osseous regeneration. This was a rare case because of the patient’s age, the tory response induces proliferation location of the lesion, its association with vital teeth, and its presentation. of fibroblasts that stimulate pros- Int J Periodontics Restorative Dent 2020;40:e35–e41. doi: 10.11607/prd.4452 taglandins, causing the bone resorption seen in a cyst.3 This is the driving force of osmotic gradient differences that lead to increases in internal hydrostatic pressure, driving fluid into the cyst. The World Health Organization 2017 classification of head and neck tumors recognizes two main types of inflammatory odontogenic cysts: Radicular and collateral.4 Radicular cysts, also known as periapical cysts or apical periodontal cysts, are the most common type of inflammatory odontogenic cysts associated with a nonvital tooth, occurring pre- dominantly in the maxilla and at a 1Private practice, Potomac, Maryland, USA. mean age of 37.5 years in males.5 2University of Maryland School of Dentistry, Baltimore, Maryland, USA. 3Department of Dermatology, Johns Hopkins University School of Medicine, Conservative conventional therapy Baltimore, Maryland, USA. of radicular cysts includes root canal treatment followed by apical sur- Correspondence to: Dr Ahmad Soolari, 11616 Toulone Dr, Potomac, MD 20854, USA. 6 Fax: (240) 845-1087. Email: [email protected] gery if the radiolucency persists. The residual cyst remaining after Submitted May 6, 2019; accepted July 16, 2019. ©2020 by Quintessence Publishing Co Inc. extraction of the affected tooth

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Fig 1 (below) (a) Normal mandibular right side. (b) Large bony lesion on the mandibular left side.

Fig 2 (right) The patient presented with a fistula, deep probing, bleeding on probing, purulent exudates, significant bone loss, and occlusal disharmony.

a b

and lateral radicular cysts associ- ed by the referring pediatric dentist. the lingual plate and interruption ated with a lateral root canal also fall The patient had received orthodon- suspected in the buccal plate. The under the radicular cyst category. tic treatment between 2014 and lamina dura adjacent to the lesion Included in the collateral inflamma- 2016. Clinical and conventional and in the interproximal area was tory cyst category are paradental radiographic evaluation disclosed missing along the mesial aspect of cysts, arising from third molars, and deep probing, bleeding on probing, the second premolar and distal as- mandibular buccal bifurcation cysts purulent exudates, significant bone pect of the first premolar, but there on the buccal surface of first and loss, and occlusal disharmony (Fig were no changes to the root apex second molars.5 2). Since the lesion was not typical of and both teeth were alive on vitality Actinomyces are opportunis- periodontal disease, a cone beam testing. tic anaerobic, gram-positive, rod- computed tomography (CBCT) im- Differential diagnosis included shaped bacteria known to cause age was taken, which disclosed a radicular cyst, odontogenic kerato- actinomycosis. Actinomyces species well-defined unilocular low-density cyst, calcifying odontogenic cysts, are highly susceptible to β-lactam lesion extending from the crest to and lateral radicular cyst. To con- antibiotics such as amoxicillin or the root apices, approaching the firm a diagnosis of the findings, the penicillin G.7 Gomes et al reported mental foramen. The intraosseous authors performed an incisional Actinomyces israelii to be the most lesion in the axial cut (mesial-distal biopsy to rule out odontogenic commonly identified microorganism direction) was 8.40 × 10 mm, with tumors. The biopsy confirmed an in radicular cysts.8 10.00-mm buccolingual dimen- inflamed odontogenic cyst with Ac- sions (Figs 3 and 4). The sagittal cut tinomyces colonization. There was showed close proximity of the lesion no evidence of malignant or neo- Case Report to the mental foramen with thinned plastic processes. Although cyst cortical plates. No other pathology fluid samples and culturing were not A 16-year-old Caucasian girl was re- was detected in the oral cavity. performed, 150 mg of the antibiotic ferred for periodontal evaluation of The lesion had a speck of lin- clindamycin was prescribed (three a bony lesion at the interproximal ear high density within it (a possible times a day for 10 days) along with space of the mandibular left first odontogenic remnant). From the the anti-inflammatory methylpred- and second premolars (Fig 1). The buccolingual dimensions, the lesion nisolone, 800 mg of the analgesic patient was asymptomatic, with an was estimated to extend between ibuprofen, and a chlorhexidine rinse atypical large radiolucency detect- the cortical plates, with thinning of (Acclean 0.12% oral rinse USP, twice

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© 2020 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. e37 daily). Periodontal regenerative therapy was offered to rebuild the hard and soft tissue that had been compro- mised by the inflammatory response. The patient and her parents accepted the treatment plan. Panoramic radiographs were taken on December 24, 2011; July 25, 2013; and September 1, 2017 (Fig 5); these radiographs show that the mandibular first premolar erupted in 2011 (Fig 5a) and that the mesial root Fig 3 The CBCT scan disclosed Fig 4 The lesion was in of the second premolar caused a delay in eruption in an 8.40 × 10-mm intraosseous close proximity to the mental 2013 (Fig 5b), but all permanent premolars were pres- lesion in the axial cut (mesial- foramen. distal direction) and 10.00-mm ent and the crowding had been corrected by 2017 (Fig buccolingual dimensions of 5c). The premolar arrangement, however, differed be- bone resorption. tween the mandibular left and right sides: A large space was observed between premolar roots on the left side but not the right side. Both sides presented symmetri- cally up until 2013, before orthodontic treatment.

Treatment

The CBCT images were read by a board-certified oral and maxillofacial radiologist whose report was re- a viewed with the patient and her parents; they agreed to proceed with the treatment plan, which was a biopsy of hard and soft tissues followed by periodontal therapy to regenerate lost tissues. Anesthesia was achieved with one carpule of lidocaine (2%) with epinephrine (1:100,000). The pretreatment photo (Fig 6a) showed the presence of a fistula at the interproximal area of the mandibular left first and second premolars. Two vertical incisions were made (Fig 6b) from the distal aspect b of the second premolar and mesial aspect of the first premolar using a no. 15 blade (carbon steel, Benco Dental), and an intrasulcular incision connected the two vertical incisions. A full-thickness flap was raised and extended beyond the mucogingival junction to en- able full access to the bony defects and to facilitate the ridge-augmentation procedure followed by coronal ad- vancement. The full-thickness flap was used instead of a partial-thickness flap to assist in locating the mental nerve and avoiding injury to the neurovascular bundle c near the surgical area. Reflection of the flap (Fig 6c) dis- Fig 5 Panoramic radiographs showing that (a) the first premolar closed a large bony lesion (8.40 × 10 mm) in the verti- erupted in 2011, and (b) the mesial root of the second premolar cal and horizontal directions at the interproximal area caused a delay in eruption in 2013. (c) By 2017, all permanent premolars were present and the crowding had been corrected. and a paper-thin lingual plate. In addition, the buccal

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Fig 6 (a) Initial clinical impression of the infected area and a draining fistula were noted interproximally to the first and second premolars, along with slight gingival discoloration. (b) Excavated cystic area interproximally to the premolars, showing the length and depth of bone resorption. (c) Packed allograft bone graft. (d) Membrane placement and gingival approximation before closing.

b c d

plate was partially missing on the fitted to the interproximal area (Fig The nonresorbable membrane first premolar. The inferior border 6d). The facial flap was coronally ad- was removed 2 months later due to of the bony lesion approached the vanced to cover the membrane and premature exposure. The area was mental foramen. secured into position with simple in- left to heal for closure and com- The debridement of the bony terrupted 4.0 monofilament sutures plete soft tissue remodeling. The lesion was performed until bare (Cytoplast Non-Absorbable PTFE area was clinically and radiographi- bone was seen with no bleeding Sutures, Osteogenics Biomedical). cally evaluated at 6 and 12 months following removal of all necrotic tis- A surgical soft and hard tissue posttreatment (Fig 8). Conventional sues. The ridge augmentation pro- excisional biopsy specimen (1.3 radiographs showed significant im- cedure consisted of reconstruction × 1.1 × 0.2 cm) was removed and provement but did not provide a of the lost tissue using freeze-dried sent for histopathologic evaluation, comprehensive picture of the exist- bone allograft (Cortical DN025, which showed a reactive and hyper- ing hard and soft tissues; the CBCT Maxxeus Dental; Fig 6c) and a plastic cystic squamous epithelium, taken 17 months after treatment dis- nonresorbable titanium-reinforced with background inflammatory cells, closed a successful ridge augmen- membrane (Cytoplast, Osteogenics that was infected with Actinomyces tation in both the horizontal and Biomedical) that was trimmed and (Fig 7). vertical dimensions (Fig 9). Bone

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Fig 7 Histologic view of biopsy specimens removed during the procedure. (a) Reactive and hyperplastic cystic squamous epithelium (arrows) with background inflammatory cells (h&e staining;× 200 magnification). (b) Cystic epithelium with an associated Actinomyces colony (arrow) (h&e staining; ×400 magnification). (c) Actinomyces colony demonstrating the Splendore-Hoeppli phenomenon (arrows) (h&e staining; ×200 magnification).

b c

a b c Fig 8 Periapical radiographs of the treated area (a) before treatment and (b) 6 and (c) 12 months posttreatment. Gain in bone height was evident after 6 months (b), with denser bone after 12 months (c).

gain was 10 mm in the buccolingual thesia (lesion advancing to the men- Discussion direction and 8 mm in the occluso- tal foramen) and loss of two teeth gingival dimension. (progression of osteolytic activity) In this case, all common inflamma- The interdisciplinary approach and involved delicate management tory odontogenic cysts were ruled in this case avoided potential pares- of a large bony lesion, which is rare. out. Vitality testing ruled out radicu-

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a b

c d Fig 9 Evaluation of the affected area 17 months posttreatment. (a) Radiograph showing significant improvement in vertical dimension. (b) Clinical view of the affected area showing the lack of a fistula. (c) Axial view demonstrating significant improvement in both horizontal and vertical dimension and more condensed bone. (d) Three-dimensional CBCT image showing complete fill in the horizontal dimension of the previous 10-mm bony defect as well as regeneration of the buccal plate above the mental foramen, with thick cortical plates.

lar and lateral radicular cysts. Resid- third molars in the mandible and a genic cyst induced by some coro- ual cysts were ruled out because the history of pericoronitis.9 Mandibular nal remnants of the prior deciduous patient had no history of extractions buccal furcation cysts were ruled tooth infected by Actinomyces that associated with cysts. Paradental out, as they are defined by their as- gained access from the draining fis- cysts could not be completely ruled sociation with first or second molars. tula. A retained root tip (of the same out as they are histologically indis- Because of the clinical and radio- tooth) was also observed by CBCT tinguishable from other inflamma- graphic findings of this case, the just apical to the lesion. tory odontogenic cysts, but they authors hypothesized that this was An inflamed odontogenic cyst are clinically mostly associated with a reactive inflammatory odonto- with Actinomyces colonization was

The International Journal of Periodontics & Restorative Dentistry

© 2020 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER. e41 the final diagnosis; to the best of the diagnosis was important because Acknowledgments authors’ knowledge, the patient’s of the unusual histologic features. age and the location of the lesion, Scholl et al reviewed cysts and The authors declare no conflicts of interest. its association with vital teeth, and cystic lesions of the mandible, and its presentation classify this as a rare noted that many non-odontogenic case. Inflamed odontogenic cysts lesions can mimic odontogenic References with Actinomyces colonization are lesions.12 Marx and Stern recom- three times more prevalent in males mended examination of the origi- . 1 Browne RM. The pathogenesis of odon- (with a peak incidence in the second nal pathologic specimen as well as togenic cysts: A review. J Oral Pathol 1975;4:31–46. to fourth decades of life) and are examining a biopsy specimen if a 2. Colic´ S, Jurisic´ M, Jurisic´ V. Pathophysi- typically associated with nonvital recurrence is observed.13 Cases of ological mechanism of the developing radicular cyst of the jaw [in Serbian]. teeth. inflamed odontogenic cysts should Acta Chir Lugosl 2008;55:87–92. be monitored at least 5 years after 3. Wu Q, Asif M, Qari IH, Qazi JA. Role of surgical removal. interleukin-1 in pathogenesis of radicular cyst. J Ayub Med Coll Abbottabad Clinical, Histopathologic, and Microscopic examination of 2010;22:86 – 87. Radiographic Appearance the biopsy material showed an 4. Soluk-Tekkes¸in M, Wright JM. The World Health Organization Classifica- inflammatory odontogenic cyst tion of Odontogenic Lesions: A Sum- The inflamed odontogenic cyst with characterized by a reactive and non- mary of the Changes of the 2017 (4th) Actinomyces colonization manifest- keratinizing hyperplastic squamous Edition. Turk Patologi Derg 2018;34. 5. Kumar ND, Sherubin JE, Jose M, ed as an asymptomatic lesion, which epithelium set within markedly in- Swaminathan C. Surgical management was detected by a pediatric dentist flamed granulation tissue. The in- of large radicular cyst in mandible. Int J Dent Oral Health 2017;3(3). on a routine dental visit. The lesion flamed granulation tissue contained 6. Hoen MM, LaBounty GL, Strittmatter was central in the mandible and ex- a mixture of inflammatory infiltrate EJ. Conservative treatment of persistent hibited an asymptomatic osteolytic composed of lymphocytes, plasma periradicular lesions using aspiration and irrigation. J Endod 1990;16:182–186. behavior, although it was painless. cells, neutrophils, and scattered 7. Valour F, Sénéchal A, Dupieux C, et al. The Actinomyces colony demon- histiocytes. Abundant filamentous Actinomycosis: Etiology, clinical features, diagnosis, treatment, and management. strated the Splendore-Hoeppli phe- bacterial colonies were present that Infect Drug Resist 2014;7:183–197. nomenon, an in vivo formation of were morphologically consistent 8. Gomes NR, Diniz MG, Pereira TD, et al. eosinophilic material around micro with Actinomyces species. Actinomyces israelii in radicular cysts: A molecular study. Oral Surg Oral organisms leading to prevention of Med Oral Pathol Oral Radiol 2017;123: phagocytosis and chronicity of in- 586–590. 10 9. Ackermann G, Cohen MA, Altini M. The fection. This reaction is thought to Conclusions paradental cyst: A clinicopathologic represent the deposition of antigen- study of 50 cases. Oral Surg Oral Med antibody complexes and debris A 16-year-old female patient with a Oral Pathol 1987;64:308–312. 10. Hussein MR. Mucocutaneous Splendore- 11 from host inflammatory cells. large bony lesion in the premolar re- Hoeppli phenomenon. J Cutan Pathol Histologically, an inflamedgion of the mandible was diagnosed 2008;35:979–988. 11. Gopinath D. Splendore-Hoeppli phe- odontogenic cyst is defined as a with an inflamed odontogenic cyst nomenon. J Oral Maxillofac Pathol 2018; lesion that contains reactive odon- with Actinomyces colonization with- 22:161–162. togenic epithelium. The cyst may out developed complications. This 12. Scholl RJ, Kellett HM, Neumann DP, Lu- rie AG. Cysts and cystic lesions of the have been associated with the man- case of an extremely rare osteo- mandible: Clinical and radiologic-histo- dibular left second premolar. Cystic lytic lesion required special man- pathologic review. Radiographics 1999; 19:1107–1124. lesions in the maxilla are typically agement of diagnosis, treatment 13. Marx RE, Stern D (eds). Oral and Maxil- observed in the anterior region, planning, treatment, evaluation of lofacial Pathology: A Rationale for Treat- while mandibular lesions tend to oc- results, and follow-up. ment, ed 1. Chicago: Quintessence, 2002. cur in the posterior region. Careful

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