|Year : 2014 | Volume
| Issue : 1 | Page : 47-52
Hybrid desmoplastic ameloblastoma: A case report of rare entity and review of literature
Priya Shirish Joshi1, Someshwar Golgire2, Sachin Majati3
1 Department of Oral Pathology and Microbiology, Vasantdada Patil Dental College and Hospital, Kavalapur, Sangli, Maharashtra, India
2 Department of Oral Pathology and Microbiology, Tatyasaheb Kore Dental College and Research Centre, New Pargaon, Tal-Hatkanangale, Kolhapur, Maharashtra, India
3 Department of Oral and Maxillofacial Surgery, Vasantdada Patil Dental College and Hospital, Kavalapur, Sangli, Maharashtra, India
|Date of Web Publication||6-May-2015|
Dr. Priya Shirish Joshi
B-3, Avani Appt., Off 80 Feet Road, Vishrambaug, Sangli City, Sangli, Maharashtra
Source of Support: None, Conflict of Interest: None
Ameloblastomas are one of the common odontogenic tumors of the oral cavity. They usually present with unilocular or multilocular radiolucency associated with or without impacted tooth. Among the variants of ameloblastomas, desmoplastic ameloblastoma (DA) casts a mixed radiolucent/radiopaque shadow on X-ray and radiograph seldom suggests a diagnosis of ameloblastoma. DA is a rare entity that exhibits important differences in anatomic distribution, histologic appearance, radiographic findings when compared to other variants of ameloblastoma. This fact has been considered by World Health Organization (WHO) and now it has been included as a separate entity in WHO classification (2005) of odontogenic tumors. About 145 cases of DA have been reported worldwide, but cases reported in India are very few. We report a case of a hybrid variety of DA in a female patient in the anterior maxillary region between 12 and 13 as painless hard swelling, showing mixed radiolucent/radiopaque shadow on radiographic examination. Histopathology revealed odontogenic epithelium in the form of follicles, typical of solid/multicystic ameloblastoma, with cystic degeneration and squamous metaplasia at places and elsewhere there were odontogenic islands compressed by dense fibrocellular stroma suggestive of desmoplasia. Also seen was osseous metaplasia. We have also done a detailed review of literature concerning the presentation of DA.
Keywords: Ameloblastoma, desmoplasia, fibro-osseous, mandible, maxilla
|How to cite this article:|
Joshi PS, Golgire S, Majati S. Hybrid desmoplastic ameloblastoma: A case report of rare entity and review of literature. J Dent Allied Sci 2014;3:47-52
|How to cite this URL:|
Joshi PS, Golgire S, Majati S. Hybrid desmoplastic ameloblastoma: A case report of rare entity and review of literature. J Dent Allied Sci [serial online] 2014 [cited 2020 Aug 3];3:47-52. Available from: http://www.jdas.in/text.asp?2014/3/1/47/156532
| Introduction|| |
Ameloblastomas are benign, locally invasive neoplasms arising from odontogenic apparatus prior to tooth formation and primarily arising from the odontogenic epithelium. They are second most common odontogenic tumors of epithelial origin. , They usually begin as the insidious intraosseous lesion and cause expansion of bone rather than perforation. On radiographic examination, they cast either a unilocular or multilocular radiolucency with soap bubble or honeycomb appearance.  Various histopathologic patterns of ameloblastoma are described including follicular, plexiform, acanthomatous, cystic, granular, basal types. ,, These variations have no significant bearing on prognosis.
Among the ameloblastomas, the desmoplastic variation is rare. The desmoplastic ameloblastoma (DA) is characterized by specific clinical, imaging, and histological features. It is more complicated to be treated because of its tendency to penetrate the surrounding bone.
This tumor usually occurs in third to fifth decades of life and has equal sex predilection. DA has a marked prevalence to occur in the anterior region of the maxilla in direct contrast to conventional ameloblastomas, and radiography seldom suggests its diagnosis because of its mixed radiolucent and radiopaque appearance. , It is a rare variant initially described by Eversole et al. in 1984.  It represents 4-5% of all ameloblastomas. 
Because of the growing knowledge regarding the clinicoradiographical presentation and pathology of DAs, World Health Organization (WHO) has categorized it as a distinct variant of ameloblastoma in the classification of odontogenic tumors in 2005. Other variants are solid multicystic ameloblastoma (SMA), unicystic ameloblastoma, and peripheral/extraosseous ameloblastoma. 
Desmoplastic ameloblastoma has distinct histologic features comprised of stroma with intense desmoplasia, few epithelial islands, and cords of various sizes. The mixed radiolucent/radiopaque appearance is due to osseous metaplasia within the dense fibrous septa that characterize the lesion and is not a mineralized product of tumor. When DA coexists with other variants of ameloblastomas, it is referred to as "hybrid DA." ,
Not many cases of DA have been reported in Indian literature and hence this endeavor to report a rare case of hybrid DA with review of literature emphasizing the clinical, radiographic, and histopathogic aspects that are relevant for diagnosis and treatment of this tumor.
| Case Report|| |
A 55-year-old female patient reported to the outpatient department with chief complaint of pain and swelling in the upper right anterior region of the mouth since 4 months and H/O of trauma to the same region 4 years back. There was no other relevant dental or medical history.
Extraoral examination revealed the facial asymmetry due to the swelling. No temporomandibular joint abnormality was detected, and there were was no lymphadenopathy [Figure 1].
|Figure 1: Clinical photograph of patient showing swelling in 12 and 13 region|
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Intraoral examination revealed that the swelling was hard in consistency and localized in between 12 and 13 with the marked migration of 12 and 13.
Intraoral periapical showed a pear shaped, mixed type of radiolucency with irregular radiopacity located between the roots of 12 and 13, evidence of root deviation but no root resorption [Figure 2] laboratory investigation revealed a normal blood report.
|Figure 2: Intraoral periapical showing a pear shaped, mixed type of radiolucency with irregular radiopacity located between the roots of 12 and 13, root deviation but no root resorption|
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A provisional clinical diagnosis of the fibro-osseous lesion including cemento-ossifying fibroma, fibrous dysplasia, and odontogenic tumor was given. Thorough surgical excision was planned along with the extraction of 12 and 13 [Figure 3].
Gross specimen received was in two parts (soft and hard). Both the tissues were processed separately and stained by H and E stain.
Histopathogic examination of the soft tissue revealed few ameloblastic follicles of varying sizes lined by cuboidal to columnar cells with reversely polarized nuclei and stellate reticulum like tissue in the center. Some follicles exhibited cystic degeneration and acanthomatous changes. At places, there were odontogenic islands compressed by dense fibrocellular stroma with hyalinization, suggestive of desmoplasia. Osseous metaplasia with osteocytes within lacunar spaces was evident [Figure 4], [Figure 5] and [Figure 6].
|Figure 4: Photomicrograph showing ameloblastic follicles with areas of cystic degeneration, squamous metaplasia, desmoplasia, and some epithelial islands (×10) (H and E)|
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|Figure 5: Photomicrograph showing squamous metaplasia in follicle surrounded by desmoplasia (×40) (H and E)|
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|Figure 6: Photomicrograph showing bony trabeculae with osteocytes and osteoblasts (×10) (H and E)|
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The hard tissue section showed lamellar bone with Haversian system and osteocytes Masson's Trichrome staining was done to confirm the desmoplasia [Figure 7].
|Figure 7: Photomicrograph showing dense desmoplasia stained by Masson's Trichrome stain (×10)|
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On detailed histopathologic examination coupled with clinical and radiographic findings, a definitive diagnosis of a "hybrid" variety of DA was established.
The follow-up was done, and the healing was uneventful [Figure 8].
| Review of Literature|| |
Eversole et al. were the first to describe three cases of DA in 1984. They referred it to as "ameloblastoma with pronounced desmoplasia."  In 2005, WHO organized ameloblastoma as solid, extraosseous, desmoplastic, and unicystic types in its classification of odontogenic tumors.  Literature review shows DA to be the least frequent odontogenic tumor. About 145 cases of DA have been reported worldwide, but cases reported in India are very few.
Takigawa et al.  and Uji et al.  drew attention to this unusual variant of DA. Among 89 cases of ameloblastomas studied by Takata et al. in 1999,  seven were diagnosed as DA. Philipsen et al. in 2001  have reviewed 100 cases of DA reported from Japanese, Western Chinese, Malaysian, and Black population. Another study by Ledesma-Montes et al.  of 163 cases of ameloblastomas in the Latin American region showed two cases of DA. According to Adebiyi et al.,  among 77 cases of ameloblastomas diagnosed in Nigerian population, four were DA.
In most of the cases of DA reported so far, there has been a strong predilection for the anterior maxilla. According to Kaffe et al.  and Manuel et al.,  more than 70% of DA cases happen to be in the anterior maxillary region, opposite to conventional ameloblastomas which is usually in the posterior mandibular region. In 10 DA cases reported by Kishino et al.,  40% involved anterior maxilla region and 60% were in the posterior mandible.
In contrary to this finding, review done by Desai et al. of 89 cases of ameloblastomas has noted DA to occur commonly in anterior region of mandible (57%) than in maxilla (42.7%). Demographic studies have revealed highest incidence of this tumor in patients of the Japanese race. 
Kawai et al. and Utaka et al. , have reported a case each of DA in the posterior mandibular region. Atalay et al. have reported a rare location for occurrence of DA in symphysis menti region in a female patient.  Yazdi et al. and Rastogi and Jain , have also reported cases of DA in the anterior mandible. Thompson et al.  have reported a case in the anterior maxilla and have for the 1 st time documented computed tomography (CT) scan and magnetic resonance imaging (MRI) features of DA. Mintz and Velez  have also reported two cases of DA in the anterior mandibular region. Smullin et al. have reported a rare case of peripheral DA located on soft tissues of the palate with no osseous involvement. 
Wang et al.  in his study of 15 cases of DA, have reported three distinct radiographic features of DA namely, unilocular radiolucency with varying amount of radiopaque islands or strands of radiopaque material; multilocular radiolucency with irregular or line like radiopaque areas; and Mixed with plexiform radiopaque material with unilocular change. They are of the opinion that DA should be differentiated from osteofibroma and odontogenic myxoma.
| Discussion|| |
The clinical aspects presented in our case are in agreement with the characteristics reported in the literature so far. DA is similar to conventional ameloblastoma in gender and age distribution that is, DA is frequent in third to fifth decades of life with equal male to female ratio.  According to review of literature, predilection of occurrence was frequent in the anterior region of maxilla ,, and our case was also in the same location. Frequently, the tumor is asymptomatic. Painless swelling or maxillary expansion may be the first presenting sign as reported in many cases, and the same features were also seen in our case.
Radiographic findings of our case were typical of DA, presenting as mixed radiopaque/radiolucency of indefinite borders. Such findings are seen in 50% of DA imitating fibro-osseous lesions. ,,,,, The clinical D/D according to radiographic findings includes fibro-osseous lesions, fibrous dysplasias, chronic osteomyelitis, ossifying fibroma. 
Dunfee et al.  are of the opinion that multiple coarse internal calcifications with significant surrounding cortical destruction are distinguishing features of DA. Takata et al. have attributed the mixed radiographic finding, and ill-defined margins of DA to its infiltrative nature and they have suggested that radiographic appearance may indicate more aggressive behavior of this tumor than other variants of ameloblastomas. They also suggest that the tumor infiltrates the bone marrow spaces and in this process, remnants of the original bone either non metaplastic or nonneoplastic remain in the tumor tissue. But this argument does not explain the absence of such bony fragments in solid multilocular ameloblastomas (SMA). 
Philipsen et al. have suggested that tumor islands induce proliferation of mesenchymal cells, resulting in desmoplasia and metaplastic bone formation (osteoplasia). This argument is not credible as such inductive potential is not observed in SMA. 
Root resorption is a common finding in DA but was not noted in our case, instead tooth displacement was observed. Kawai et al.  suggest that the thin cortical plate of maxilla forms a weak barrier for the spread of tumor and so maxillary ameloblastomas may be able to spread earlier and more quickly than mandibular ameloblastomas.
Computed tomography scan can delineate the internal structure of the lesion more accurately and is particularly helpful in determining its margins and extension into adjacent structures. , MRI shows heterogeneous low to intermediate signal intensity on T1-weighted images, heterogeneous high signal intensity on T2-weighted images, and strong enhancement on postgadolinium T1-weighted images. 
Magnetic resonance imaging can clearly differentiate between solid and cystic components. 
The histologic appearance of DA is characteristic and differs from SMA in the nature of collagenous fibrous stroma and the morphology of constituent cell types in odontogenic islands. , Waldron and el-Mofty  described the histologic appearance of DA as small ovoid islands and narrow cords of odontogenic epithelium widely separated by dense moderately cellular, fibrous connective tissue. Peripheral columnar cells with reversely polarized nucleus within the epithelial island are not a dominant feature. The odontogenic islands in DA are irregular and appear to be compressed or squeezed by stromal tissue, giving rise to a stretched out tail like appearance. Microcysts containing either eosinophilic amorphous deposits or appearing empty may occur centrally. Spicules of mature lamellar bony trabeculae have been reported in intimate contact with the tumor and invasion has been demonstrated. Recently, Hirota et al.  reported a case of DA with few areas of characteristic compressed tumor islands along a predominantly basal cell pattern of odontogenic cells similar to the appearance of basal cell ameloblastoma.
In some instances, typical follicular tumor islands as seen in SMA surrounded by less dense collagenous stroma have been observed in DA. This entity is called a "hybrid" lesion.
Our case showed histologic features very characteristically described in the literature so far for DA but belonged to the hybrid variety. This tumor is somewhat histologically different from other odontogenic tumors like ameloblastic fibroma, odontogenic fibroma or squamous odontogenic tumor. In our case, diagnosis was not difficult because the stroma showed extensive desmoplasia and ameloblastic polarization. Some of the tumor nests showed clear follicular pattern with cystic degeneration and squamous metaplasia at places [Figure 4] and [Figure 5]. The simultaneous presence of osteoplasia and desmoplasia as seen in connective tissue stroma of this tumor [Figure 6] has been reported in only four other cases. 
It has been suggested that DA can behave aggressively and has the potential to grow to a large size. The maxillary prevalence explains its early invasion to adjacent structures as maxilla cannot offer an effective barrier. Diffuse radiographic appearance and histologic findings of bone invasion are the reasons behind not finding the exact interface of the lesion with normal bone making it difficult to be treated surgically. , Since DAs tend to infiltrate between bone trabeculae, curettage often leaves islands of the tumor within the bone, which eventually leads to recurrences. Therefore, block excision is the most widely accepted form of treatment. Since its first report by Eversole et al. in 1984 many case of DA have been reported but the peculiar histologic appearance still remains unclear.
Immunohistochemical staining was not necessary in our case as the diagnosis was very straightforward and easy though literature review shows studies demonstrating DA tumor cells to variably express S-100 protein and desmin,  marked immunoexpression of transforming growth factor-beta,  high expression of caspase-3 and fas,  decreased expression of cytokeratin19,  high expression of p63.  Compared to the stroma of SMAs, the desmoplastic stroma of DA has been reported to show strong positive for collagen type VI which rules out scar tissue, immunonegativity for tenascin, strong immunopositivity for fibronectin and type I collagen. 
Kishino et al.  have demonstrated oxytalan fibers in the stromal tissue of one case, and they suggest that the tumor may be derived from epithelial cell rests of malassez present within periodontal ligament of adjacent teeth.
Desmoplasia of stromal connective tissue in DA can be argued to be a maturation change in SMAs as similar dense collagenization is seen during maturation of long standing tumors. This argument can be supported by the "hybrid" tumor as seen in our case where follicles were present in the desmoplastic background. But the lesser frequency of DA in posterior mandible compared to SMAs then remains unanswered. It is probable that the location of the tumor can influence the maturity of the lesion and hence tumors in the anterior jaws may mature sooner than those occurring in the posterior mandible. Of significance in this context is the higher frequency of SMAs in anterior jaws in Blacks, indicating the possible racial influence in the site predilection of ameloblastoma. It is possible that the majority of these ameloblastomas could turn out to be DA if the careful histologic examination is carried out. Second, DA might not actually be a rare entity. Many Hybrid lesions may have been misclassified since the presence of typical ameloblastic islands in some cases could have warranted a diagnosis of SMAs. 
| Conclusion|| |
Desmoplastic ameloblastoma is a rare and unique entity and a hybrid variety of the same is more so. DA is found to be common in anterior jaws particularly maxilla. Anterior lesions mature early explaining the unique site predilection. The mixed radiolucent/radiopaque appearance dictates a differential diagnosis of fibro-osseous lesions. Diagnosis should be based not only on clinical presentation and radiologic features but also on careful histopathologic examination. A definitive final diagnosis prior to surgery is a must for proper and efficient surgical management especially to prevent recurrence. The biologic behavior of DA is still unclear, and future research in the analysis by immunohistochemistry and a long-term follow-up study is needed.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
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