Bevel: Case Report

Calcifying Cystic Odontogenic Tumor Presenting as a Dentigerous Cyst: A Case Report with Literature Review

Ali Hanttash Abu Hanttash, Aysegul Tuzuner Oncul, Umit Akal Aktaş

Abstract

The calcifying cystic odontogenic tumor is comparatively rare in occurrence, constituting about 1.6% - 4.3% of all odontogenic tumors. Various terminologies have been used to describe this rare odontogenic tumor, sometimes referred to as the keratinizing and calcifying odontogenic cyst, Gorlin cyst, calcifying odontogenic cyst, calcifying ghost cell odontogenic tumor, dentinogenic ghost cell tumor, and epithelial odontogenic ghost cell tumor. It is characterized by the presence of ghost cells with proliferative odontogenic epithelium and has a propensity for calcification. The aim of this paper is to report a case of calcifying cystic odontogenic tumor misdiagnosed as a dentigerous cyst in the posterior region of the mandible associated with unerupted tooth, along with a brief review of literature based on the term calcifying cystic odontogenic tumor. The lesion was surgically enucleated. After enucleation no recurrence has been observed during the follow up period of four years.

 

Keywords: Calcifying Cystic Odontogenic Tumour; Dentigerous Cyst; Ghost Cells; Hybrid Odontogenic Tumor; Odontogenic Tumors.

 

Ali Hanttash Abu Hanttash, Aysegul Tuzuner Oncul, Umit Akal Aktaş. Calcifying Cystic Odontogenic Tumor Presenting as a Dentigerous Cyst: A Case Report with Literature Review. International Journal of Oral & Maxillofacial Pathology; 2015:6(1):11-18. International Journal of Oral and Maxillofacial Pathology. Published by Publishing Division, Celesta Software Private Limited. All Rights Reserved.

 

Introduction


Calcifying cystic odontogenic tumor (CCOT) is defined as a cystic lesion, which contains masses of ghost cells within ameloblastic epithelium. It represents about 1.6%-4.3% of all odontogenic tumors. It constitutes 2% of all odontogenic pathological changes in the jaw. The lesion usually has extraosseous variant called extraosseous calcifying cystic odontogenic tumor and intraosseous variant called intraosseous calcifying cystic odontogenic tumor.1,2 Clinically the tumor characterized by its painless, slow-growing tumor which affects the maxilla and mandible equally, It is commonly observed in the anterior region of jaws followed by the premolar and molar area. CCOT does not demonstrate any gender predilection. It has a peak incidence during the second and third decades on life, with a mean age of 30, ranging 3-33 years. The youngest reported patient was a two-year-old baby and the oldest was 82 years old.3,4

 

The literature was reviewed through a search of PubMed, Google scholarship and Science Direct database about CCOT using the keywords calcifying cystic odontogenic tumors, Ghost Cells and Hybrid odontogenic tumor. All the reported cases of CCOT in the English literature especially which termed by a CCOT were reviewed and summarized for academic purpose. The results revealed two review studies and 54 case reports in association with our case. The 54 CCOT cases included 12 cases reported as CCOT associated with other tumors and three cases reported as pigmented CCOT. The present systematic review attempts to fill the gaps and establish guidelines for specific statistical results about age, gender, location and recurrence of CCOT tumor.

 

Case Report

A local dentist, to Department of Oral and Maxillofacial Surgery, Ankara University for routine asymptomatic impacted tooth removal, directed a 54-year-old female patient. The patient was free from any medical conditions. Intraoral examination did not reveal any symptoms such as swelling or pain on palpation. The mucosa over the lesion was intact; the patient gave no past history of swelling or parasthesia. Panoramic Radiography examination (Figure 1a) revealed a well defined, 4-5mm unilocular radiolucency, with a significant radiopaque outline border with discrete radiopaque foci associated with unerupted first molar at the site of lower right premolar and molar region with root resorption noticed in the second premolar. An initial diagnosis of dentigerous cyst was considered. Due to jaw fracture possibility tooth extraction and cyst enucleation was performed under general anesthesia. Follicle-like tissue was sent to the Department of Oral Pathology for histopathological examination. The findings were a cystic lesion with a fibrous capsule lined by odontogenic epithelium; with a prominent feature of large ballooning epithelial cells without nucleus (ghost cells), which presented a slightly eosinophilic, round enlarged morphology (Figure 1b). Based on these features, the lesion was diagnosed as CCOT. No recurrence was detected in a clinical and radiographic follow-up of 4 years (Figure 1c).


 

Figure1: The Panoramic radiograph demonstrating a well-circumscribed radiolucency with root resorption of the second premolar and radiolucent lesion containing radiopaque foci enclosing unerupted permanent first molar (a). The photomicrograph showing cystic cavity lined by ameloblastomatous epithelium with ghost cell keratinization (arrow) and calcification (arrowhead) (Hematoxylin & Eosin; x400)(b). The follow-up panoramic radiograph demonstrating complete healing after 4 years(c).

 


Review of Literature

A literature review was performed in order to establish guidelines for specific statistical results concerning age, gender, location, and recurrence of CCOT tumor. The results revealed 54 case reports in association with our case. As presented in table1, the reported cases demonstrate an apparent male predilection of 1,3:1. The age distribution ranged widely from 2 to 86 years, with a mean age of 30.5 years. Regarding the anatomical location of CCOT, (55.5%) were in the maxilla, (44.4%) were in the mandible. The available radiological information among 54 cases, 51 cases presented with available information about radiolucency or mixed radiolucency- radiopaque view. As presented in table 1, 74.5% presented as mixed radiolucent-radiopaque lesions. Around 25.5% were totally radiolucent, While 75.6% had unilocular appearance, and 24.4% had multilocular appearance. Resorption of tooth roots was reported in 40.7% of the 54 cases, cortical perforation was reported in 24% of the 54 cases and tooth or root displacement was reported in 46.2% of the 54 cases. From 54 cases, just 40 cases with available treatment approaches were found, most of the lesions (34 of 40 cases 85%) were treated by enucleation and curettage, five cases were treated by segmental resection and one case by marsuplization. (Table 1)1-3, 6-19, 24-27, 29-33

 

Discussion

Currently the origin of CCOT is not known but regarding to histogenesis it is thought to originate from the remnants of odontogenic epithelium or reduced enamel epithelium and islands of odontogenic epithelium entrapped in jaws bone giving rise to intraosseous CCOT or gingival tissue giving rise to extraosseous CCOT lesion respectively.5,6

 

Mean age (range) in years

 0-10                                   6

 11-20                                 20

 21-30                                 8

 31-40                                 6

 41-50                                 3

 51-60                                 5

 61-70                                 3

 71-80                                 3

Sex

 Male                                  30

 Female                              24

Chief complaint

 Swelling                            40

 Pain                                  3

Parasthesia                       3

Asymptomatic                   2

 NA                                    6

Location

Maxilla                              30

 Anterior-premolar            14

 Anterior-molar                 9

 Premolar-molar               7

 Cross Medline                 4

Mandible                          24

 Anterior-premolar            8

 Anterior-molar                 6

 Premolar-molar              10

 Cross Medline                5

Radiographic features

Internal structure of tumor

 Mixed pattern with both radiolucent and radiopaque                             38

 Radiolucent                                  13

 NA                                                3

Unilocular                                      31

 Multilocular                                  10

 NA                                               13

Root resorption approved in         22

 Tooth displacement approved in 25

 Cortical perforation                      13

Treatment approaches

Segmental resection                     5

Marsuplization                              1

Enucleation                                  34

NA                                                14

Recurrent cases                           3

Table 1: Systematic review of the clinical behavior, radiological properties and treatment approaches of CCOT (NA: not available) 1-3, 6-19, 24-27, 29-33

 

Studies report that the molecular changes underlying its development include mutations and overexpression of β-catenin gene which regulates Wnt signaling whereas aberrations of the Wnt signaling pathway may play a crucial role in the differentiation of the odontogenic epithelium in CCOT via the deregulation of cell proliferation.7 Because of the histological complexity, morphological differences, clinical biological behavioral diversity and aggressive proliferation nature of CCOT, a lack of agreement is present until now about the terminology with specific classification to CCOT. İn this systemic review we noticed that several classifications have been suggested in the literature in order to separate its variants.

 

Firstly about the history of the tumor (Table 2) from where it had been considered as a member of ghost cell odontogenic tumors family until 2005, whereas WHO defined the clinico-pathological features of the ghost cell odontogenic tumours and separate it to three tumors, terming the third one as CCOT and defined it as a benign cystic neoplasm of odontogenic origin, characterized by an ameloblastoma-like epithelium with ghost cells that may calcify and present as an intraosseous or extraosseous process.

 

Tumor classification had been continued from other specific researches as in 2006 a new classification of odontogenic ghost cell lesions was presented by Praetorius in Shear books Cysts of the oral and maxillofacial regions as presented in (Table 2). Finally in 2008, an international collaborative study distinguished four variants of CCOT, they used a classification that would include all the so-called CCOT subtypes (cystic and solid) under the 2005 WHO guidelines as follows: CCOT type 1 (simple cystic), CCOT type 2 (odontoma associated), CCOT type 3 (ameloblastomatous proliferation), and CCOT type 4 (associated with benign odontogenic tumors other than odontomatumors.3

 

İn the present systemic review we can observed that several classifications have been suggested in the literature and surgeons reported cases to the same lesion using different terms so there is a lack of agreement is present until now about the terminology of this tumor. We believe that there will be a new classification or terms to ghost cell tumors as soon as possible from WHO association or another large studies in the future.

Concerning incidence rates of CCOT, the extraosseous variants ranges from 0.2% to 0.6% of all odontogenic lesions and they represent 8% of peripheral odontogenic tumors.2 The intraosseous CCOT form is more common with a prevalence rate of (70%) by a 3:1 ratio with extraosseous CCOT. They are usually diagnosed in the second decade of life, while the extraosseous lesions are usually noted after 50 years.8


In 1932 Rywkind, reported CCOT by a lesion of the jaw which resembled cholesteatoma of the ear and called it as cholesteatoma of the jaw.13

In 1946 Thoma and Goldman described a lesion az a strange variant of ameloblastoma.14,15

İn 1962 Gorlin et al., classified the lesion as a calcifying odontogenic cyst related to the odontogenic apparatus.16

In1975 Freedman et al., suggested the name Calcifying cystic odontogenic tumor13,5

In 1981 Pretorius et al., proposed that calcifying odontogenic cyst comprises of two entities: a cyst and a neoplasm.1

In 1992 Kramer et al., classified it as a benign odontogenic tumour.17

in 2005 World Health Organization in Classification of Head and Neck Tumor renamed the lesion by Pretorius and Ledesma-Montes as a calcifying cystic odontogenic tumor including all its variant.19,20

In 2006 Pretorius was presented in Shear books Cysts of the oral and maxillofacial regions this classification include four groups according to lesion histopathological analysis, the first group called simple cyst where is the lesion just contain ghost cells without benign tumor or dentinoid formation nor malignancy differentiation and termed calcifying odontogenic cyst COC. The second group where the lesion has ghost cells and accompanied with one of these benign tumors (odontome, adenomatoid odontogenic tumor, ameloblastoma, ameloblastic fibroma, ameloblastic fibro-odontoma, odonto-ameloblastoma, odontogenic myxofibroma) and it is called calcifying cystic odontogenic tumor CCOT. The third group where the lesion of first or second group accompanied with dentinoid formation and termed by dentinogenic ghost cell tumor (DGCT). In the last group the term ghost cell odontogenic carcinoma (GCOC) where the lesion have ghost cells, dentinoid formation and malignant differentiations.7,9

In 2008 an international collaborative study distinguished four variants of CCOT, they employed an objective, comprehensive and useful classification that would include all the so-called COC subtypes (cystic and solid) under the 2005 WHO guidelines as follows: CCOT type 1 (simple cystic), CCOT type 2 (odontomas-associated), CCOT type 3 (ameloblastomatous proliferation), and CCOT type 4 (associated with benign odontogenic tumors other than odontoma).5

 

Tabel 2: Through history, different classification terms of CCOT.

 


The CCOT affects the maxilla and mandible equally, commonly anterior region of jaws are affected, followed by the premolar and molar area without any gender predilection.3 Although some studies report that it is slightly more common in women.8 Buchner et al., noted that extraosseous CCOT tend to occur more often in mandibular incisor, canine and premolar areas and also occurred more often in females (66.6%) than in males (33.3%).9 Resende et al., in their review of 44 well-defined cases of peripheral CCOT, also reported a slight predilection for females and the anterior region. However, they found a similar distribution throughout the maxillary (40.9%) and mandible (47.7%) regions. In their study, the mean age at the time of diagnosis was 49.4 years.10 In the present systemic review, we noticed almost all case reports occurred equally in the maxilla and the mandible in all regions equally, lesion occurred especially in the second decade of life (37%) with a mean age of 30.5 years and a slight prediction for male gender 1.3:3.

 

The extraosseous variant of CCOT, due to the common clinical aspect of the lesion appears clinically as a well-circumscribed fibrous mass, differences in dimension observed between 1.5 - 4 cm in greatest diameter, mimicking a nonspecific gingival enlargement or pedunculated gingival mass with no distinctive features and radiographically show no or only superficial bone involvement with surface erosion.11 Differential diagnosis of extraosseous cases depends on its localization and should include peripheral giant cell lesions, gingival cysts of the adult, fibroma, mucocele, fibrous hyperplasia, peripheral ameloblastoma and other benign mesenchymal tumors.12 Taghavi et al., reported a unique case of large recurrent extraosseous CCOT with rapidly enlargement in two month that also caused face enlargement in left mandibular area.11 Only one case of recurrent extraosseous CCOT was seen in reported cases.

 

The CCOT appear clinically as slowly growing swelling with a duration ranging from 6 months to 25 years. The size of the lesion usually ranges from 1 to 7 cm. According to Joseph et al., mandibular lesions may cross the midline which is a rare feature in the 12 different results, the impacted tooth may be adjacent to the lesions in or surrounded by the radiolucent lesions, which were attached to the cemento-enamel junctions.14 Displacements of adjacent teeth were found in 44% and root resorption was found in 33% of CCOTs. These frequencies were low compared with a report of root resorption rate of (77.1%) and a report of root resorption rate of (80%) and another report with tooth displacement rate of (100%) from other studies.15

 

The CCOT may mimic numerous odontogenic and non odontogenic lesions therefore the clinical diagnosis is difficult and a specific knowledge in oral pathology is required to differentiate odontogenic lesions.16 There have been case reports where persistent periapical periodontitis with unsuccessful attempts at root canal treatment became clear to be CCOT on histopathological examination of the surgically enucleated periapical tissue. The authors opinioned that CCOT can mimic apical periodontitis and therefore, should be considered in the differential diagnosis of large lesions associated with the apex of the root of the tooth.17 A CCOT in the peri-coronal location can resemble a dentigerous cyst or ameloblastoma in its earlier stages.18 In later phases when radiopaque foci are evident, it resembles adenomatoid odontogenic tumours, partially mineralized odontoma, calcifying epithelial odontogenic tumour, ameloblastic fibroodontoma. Unilocular lesions in periapical location may mimic radicular or residual cysts, while multilocular lesions may resemble ameloblastoma or odontogenic keratocysts.6 Manveen et al., present a rare case of calcifying odontogenic cyst mimicking as a residual cyst in the maxillary anterior region.6 Santos et al., reported a case of CCOT involving the maxillary sinus radiographically mimicking a sinus mucocele.16 In the present case report the presence of unerupted tooth with follicular space large than 5 mm evoked the diagnosis of dentigerous cyst and it is to our knowledge the first case report that CCOT misdiagnosed with dentigerous cyst.

 

The CCOT may be aggressive some times. The presence of root resorption supports the suggested aggressive nature of CCOTs. Moen et al., reported a slow-growing aggressive behavior giant CCOT which protruded and elevated the nasal cavity with orbital floor.19 Devilliers et al., reported a nearly six cm diameter, sharply marginated unilocular expansible radiolucent CCOT which expanded into the left maxillary sinus and left nasal cavity and elevated the left orbital floor.19 The reasons of such like aggressiveness discussed in literature, positive staining for MMP-9 protein has been detected in stromal cells of CCOT and it may be linked with invasive ability of this tumor.20 Podoplanin, a trans-membrane sialo-mucin like glycoprotein, is a specific marker of lymphatic vessels, and its expression is also considered to be associated with tumor invasion and tooth development, Kikuchi et al., examined the expression of podoplanin in CCOT. Whereas the podoplanin expression in CCOTs was evident in the periphery of ameloblastoma-like epithelium (6%) and the epithelial cells adjacent to ghost cells (60%). These findings suggest that the expression of podoplanin in CCOTs may reflect rapid turnover of cytoskeletal filaments and local invasiveness.21

 

Matrix metalloproteinase (MMPs) comprise a family of calcium- and zinc-dependent endopeptidases participating in physiologic events and pathologic processes and facilitating tumor growth, invasion, and metastasis.22 Study by Ribeiro et al., aimed to evaluate and compare the Immunohistochemical expression of MMPs 1, 2, 7, 9, and 26 in calcifying cystic odontogenic tumors to define contribution of this MMP in process of tumor growth and expansion, they found that MMPs 1, 2, 7, 9, and 26 are expressed in parenchymal and stromal cells of CCOTs, with the exception of MMP-2, suggesting their contribution to tumor growth and expansion.23,24

 

The recurrence of CCOT was discussed in literature. Habibi et al., reported 60 CCOTs where two cases recurrences occurred with malignant transformation in one case was reported.2 Ghost cell odontogenic carcinoma (GCOC) is the malignant counterpart of this tumor and it frequently arises from malignant transformation of CCOT after multiple recurrences.25 Some studies reveled that recurrent CCOT was more common in maxilla and in male patients due to obtaining an adequate surgical margin is difficult in maxilla.26 Moreover, CCOTs with cribriform nests, high Ki-67 and p53 expression, increased atypia, and mitotic rate are aggressive neoplasms and have a greater probability of malignant transformation in future. Therefore, the pathologists should point out these histopathological features in pathology reports as its clinical importance to the surgeons.24

 

The occurrence of CCOT with other lesions at different locations in the same patient is rare. Only 4 such patients have been documented in CCOTs reports. In these patients tumors occurred with either keratocystic odontogenic tumor or dentigerous cyst.27,28 Chindasombatjaroen et al., describe case of a patient with CCOT associated with an odontoma, a supernumerary tooth, and dentigerous cyst simultaneously occurring at different locations in the maxilla.29

 

At the same time CCOT can be found in association with other odontogenic tumours at same location or it can have been said like the components that often observed in CCOT, like odontome, ameloblastoma, ameloblastic fibroodontoma, odontoameloblastic tumor, calcifying epithelial odontogenic tumor, odontogenic myxofibroma and adenomatoid odontogenic tumours.29 It is a finding that is a rare event in other types of odontogenic cysts or tumors. İn the present systematic review we found 12 cases in which CCOT associated with other tumors specially odontoma and ameloblastoma.

 

The biological mechanism causing such a unique mixture has not been well described. But, it is considered that the development of CCOT which possesses the features of other odontogenic tumours results in the development of these tumours secondarily, rather than that these tumours are themselves secondary phenomena of preexisting odontogenic tumours.4 Pretorius et al., believed that what appeared to be an associated odontogenic tumor was simply an integral part of the entire lesion developing from the wall of CCOT. Other studies reveled that CCOT represents the pathologic counterpart of normal odontogenesis and the epithelial components have the ability to induce the formation of dental tissues in the adjacent connective tissue wall.29 Therefore, several odontogenic tumors may seem to arise from CCOTs.

 

The exact etiology of CCOT pigmentation is unknown, leaving room for speculations. As described in previous reports, most of these cases occurred in Blacks and Asians, there by implicating racial pigmentation to be an important factor. Jahanshahi et al. reported a case of pigmented calcifying cystic odontogenic tumor associated with odontoma and concluded that due to the same neural crest origin for melanocytes and dental lamina, the presence of melanocytes and melanin in this lesion is accountable. However, up to date, no biologic behavioral and prognostic role has been considered.30

 

Finally, according to the World Health Organization (WHO) typical histological and microscopic features of extraosseous CCOT are similar to the Intraosseous CCOT characteristics, and include a cystic cavity with a fibrous capsule lined by an odontogenic epithelium formed by a distinct columnar and occasionally cuboidal basal layer, with cells that contain darkly staining nuclei, polarized away from the basement membrane and palisading, similar to the ameloblast. Within the epithelial lining, there is an irregular collection of cells, including sheets of stellate reticulum and ghost cells. The presence of irregular or dysplastic dentin and osteoid can also be found adjacent to the lesion tissue.4,15

 

As had been seen during the review process, the diagnostic workup and treatment in cases of CCOT usually includes panoramic radiography, computed tomography, and biopsy for histopathological analysis, followed by surgical removal using an enucleation with curettage procedure (85%). However, a few reports about giant or aggressive CCOT presented another forms of treatment. Sakai et al., treat a young patient by marsupialization approach, they concluded marsupialization should be considered when planning CCOT treatment, primarily in young patients with large lesions, to avoid differences in the growth and tooth buds loss.31 Moen et al., presented a hemi-maxillectomy resection using a Weber- Ferguson approach for aggressive behavior CCOT.19 Devilliers et al., reported a medial maxillectomy for a patient had a nearly 6 cm radiolucent CCOT expanded into the left maxillary sinus and left nasal cavity with elevated left orbital floor. Schuster et al., presents removal CCOT via a trans nasal endoscopic approach.32 About the recurrences and malignant transformation of a preexisting CCOT studies recommended have long-term follow-up at least 10 years.33

 

Conclusion

The possibility of mimicking numerous odontogenic and non-odontogenic lesions makes the clinical diagnosis of (CCOT) difficult, so the definitive diagnosis is made histologically. Morphological differences, clinical and biological behavior diversity of CCOT results in a lack of agreement until now about the terminology with specific classification. A universally accepted classification must be established in the future. Due to malignant transformation possibility long term follow-up period of at least 10 years is recommended after enucleation CCOT.

 

Acknowledgement

We would like to thank Dt. Poyzan bozkurt from the Department of Oral and Maxillofacial surgery for grammar correction in the manuscript.

 

Author Affiliations

1.Dr.Ali Hanttash Abu Hanttash, 2.Dr.Aysegul Tuzuner Oncul., 3.Dr.Umit Akal Aktaş, Professor, Ankara University, Faculty of Dentistry, Department of Oral & Maxillofacial Surgery, Beşevler 06500, Ankara, Turkey.

 

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Corresponding Author

Dr. Ali Hanttash Abu Hanttash,

Ankara University,

Faculty of Dentistry,

Department of Oral & Maxillofacial Surgery,

Beşevler 06500, Ankara, Turkey.

Email: ali.hanttash@gmail.com

Ph: +90 542 288 82 10


 

 

 

Source of Support: Nil, Conflict of Interest: None Declared.

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