Accepted Manuscript Imaging characteristics of ameloblastomas and diagnostic value of CT and MRI in a series of 26 patients Satu Apajalahti, DDS, PhD, Jetta Kelppe, DDS, Risto Kontio, MD, DDS, PhD, Jaana Hagström, DDS, PhD PII:
S2212-4403(15)00897-4
DOI:
10.1016/j.oooo.2015.05.002
Reference:
OOOO 1191
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 4 February 2015 Revised Date:
25 April 2015
Accepted Date: 6 May 2015
Please cite this article as: Apajalahti S, Kelppe J, Kontio R, Hagström J, Imaging characteristics of ameloblastomas and diagnostic value of CT and MRI in a series of 26 patients, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2015), doi: 10.1016/j.oooo.2015.05.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Imaging characteristics of ameloblastomas and diagnostic value of CT and MRI in a series of 26 patients Satu Apajalahti, DDS, PhD, a Jetta Kelppe, DDS, b Risto Kontio, MD, DDS, PhD, c and Jaana Hagström, DDS, PhD d HUS Medical Imaging Center, Department of Radiology, Helsinki University Central Hospital
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a
([email protected])
c
Department of Oral Pathology, University of Helsinki ([email protected])
Department of Oral and Maxillofacial Diseases, Helsinki University Central Hospital
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b
d
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([email protected])
Department of Pathology/Haartman Institute and HUSLab, Helsinki University Central Hospital
([email protected])
Satu Apajalahti, DDS, PhD
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Corresponding author:
HUS Medical Imaging Center
PO Box 263
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Department of Radiology, Helsinki University Central Hospital
FI-00029 HUS, Helsinki
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Finland
e-mail: [email protected] mobile: +358 40 5868994
Conflict of interest: none
Word count: abstract 154; manuscript 2884; number of references 22; number of figures 9; number of tables 4
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Objectives. To evaluate the imaging characteristics of ameloblastomas and to analyse the diagnostic value of CT and MRI compared with conventional dentoalveolar imaging. Study Design. In this observational retrospective study the panoramic radiographs (n=25), CT
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(n=26) and MRI (n=5) images of histopathologically verified ameloblastomas in 26 patients were reviewed.
Results. Characteristic findings were multilocularity, marked expansion of the cortical plate,
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perforation at an earlier stage and extensive root resorption. On contrast-enhanced CT or MRI,
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majority (14/17) of the non-unicystic ameloblastomas contained a mixed cystic and solid pattern. Unicystic ameloblastomas (n=6) and ameloblastomas derived from the cyst epithelium (n=2) showed thick rim-enhancement or mural solid component in an otherwise cystic lesion. Conclusions. Contrast-enhanced CT and MRI greatly aid in differential diagnosis between
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ameloblastomas and other cyst-like lesions because they allow visualisation of a mixed cystic and solid content characteristic for non-unicystic ameloblastomas. The differential diagnostic value of
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CT and MRI is significant regarding unicystic ameloblastomas.
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ACCEPTED MANUSCRIPT Introduction
Ameloblastomas are a group of benign, locally aggressive tumours in the maxillomandibular region originating from odontogenic epithelium. Ameloblastoma is the second most common odontogenic tumour after keratocystic odontogenic tumour (KCOT).1 Ameloblastomas are often asymptomatic
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and are frequently detected during routine panoramic radiography. A painless swelling of the jaw is the usual clinical presentation. According to the WHO histological classification, ameloblastomas are divided into solid/multicystic, extraosseous/peripheral, desmoplastic and unicystic types.2
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Unicystic ameloblastomas are further classified into luminal (ameloblastomatous cyst epithelium), mural (tumour growth invading the fibrous wall of the cyst) and intraluminal (protruding into the
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cyst cavity) types. All growth patterns may be seen in the same tumour.3 Rarely does an ameloblastoma exhibit malignant behaviour. In the present department two cases of ameloblastic carcinomas have been diagnosed between 2005 and 2014.4
The treatment of ameloblastomas is surgical and more radical than in the case of KCOTs and other
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cystic lesions. Solid/multicystic ameloblastomas require segmental or en bloc resection and reconstruction with free cancellous bone and fixation plate. In the case of a large block resection a free vascularized bone flap should be considered. KCOTs and other cystic lesions are often treated
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by enucleation. In conventional two-dimensional imaging (panoramic radiograph) differential diagnosis between ameloblastomas and cystic lesions is not straightforward. Cone beam computed
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tomography (CBCT) produces three-dimensional images of the bony structures and cortical bone but does not allow visualisation of the contents of the lesion due its poor soft tissue contrast. In the present observational retrospective study we reviewed the panoramic radiographs, helical CT and MRI examinations of 26 patients with histopathologically diagnosed ameloblastoma in order to evaluate the imaging characteristics of the tumour and to assess the value of CT and MRI compared with conventional dentoalveolar imaging (panoramic radiograph). In addition, we wanted to find
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ACCEPTED MANUSCRIPT out whether CT and MRI features reflected the histopathological pattern of different types of ameloblastoma in the present series.
Materials and methods
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Patients
The patients were primarily selected from the Q-pati database, Department of Pathology, HusLab, Helsinki University Central Hospital, having been diagnosed with ameloblastoma between 2000
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and 2013 (n=34). Of these, 26 patients (age range 18-82 years; mean 48 years) who had undergone MSCT and/or MRI examination at HUS Medical Imaging Center before surgical treatment, were
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selected for this study.
Based on their histology, 15/26 (58%) the majority (61%) of the ameloblastomas were solid/multicystic types, six were unicystic and two were diagnosed as peripheral ameloblastomas. Nine Over half (57%) of the solid/multicystic ameloblastomas showed a mainly follicular growth
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pattern. Two of the ameloblastomas cases were histopathologically suggestive as being primarily dentigerous cysts with ameloblastomatous growth. In one case three cases the histological subtype was unclear. Microscope examination showed four of the unicystic type ameloblastomas to have a
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mural or intraluminal component, one was luminal, whereas in one unicystic type no information
Imaging
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concerning the subtype was obtained. Malignant ameloblastomas were excluded.
Panoramic radiography (Scanora, Soredex, Finland or OP 200 Instrumentarium Imaging, Finland) was performed in 25 patients prior to additional imaging. All patients underwent MSCT examination. High-resolution helical CT scanning (slice thickness 1.25 mm, slice interval 0.63 mm) was performed using either a 4- or 16-slice scanner (Light Speed Plus or Bright Speed; GE Medical Systems, Milwaukee, US) with bone and soft tissue algorithms.
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ACCEPTED MANUSCRIPT The data were reformatted into 2.0 mm or 2.5 mm-thick axial, coronal and sagittal images. In 17 cases, contrast medium (Ultravist, 300 mgI/mL; Schering, Germany, or Omnipaque, 350 mgI/mL; GEHealthcare) was used. Of these, in six patients scanning was first performed without contrast medium and then with contrast enhancement. The remaining nine cases were non-contrast
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examinations.
In addition to non-contrast CT examination, five patients also underwent MRI. MRI examination (n=5) was performed using a 1.5 T unit (Magnetom Vision; Siemens, Erlangen, Germany). One
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MRI examination was performed elsewhere. The imaging protocol consisted of axial and coronal T2-weighted fast spin echo (FSE) images with fat-suppression (fs) and axial T1W FSE images
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(slice thickness 3 mm) with and without fs. After intravenous administration of gadolinium (Magnevist, 0.5 mmol/mL; Schering, Germany), axial and coronal T1W fs images (slice thickness 3 mm) were acquired.
In addition, in three patients CBCT examination was performed elsewhere, and was available for
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reading.
Image analysis
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The radiological findings were compared with histopathological diagnosis.
The MRI and CT images were retrospectively viewed on a Dome E2 greyscale display (size 19.6
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in.; Planar Systems, Beaverton, USA) with a display resolution of 1,200 x 1,600 pixels by an experienced oral radiologist.
On panoramic radiographs, the following were assessed: location, locularity (unilocular or multilocular), expansion in two dimension, as well as tooth association, tooth displacement or root resorption. On CT with the bone algorithm, the features assessed, in addition to those examined on panoramic radiograph included size of the tumour, internal bony architecture, three dimensional expansion and
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cortical perforation. Perforation was considered if not even a thinned cortical plate was visible in an expanded cortex. With CT, the contents of the tumours were divided into either solid or cystic components based on CT density values and contrast enhancement. On CT without contrast enhancement, density values averaging that of the cerebrospinal fluid (hypodense to muscle) and
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musculature (isodense to muscle) were designated as cystic and non-cystic components,
respectively. Additionally, the enhancement pattern of solid structures as well as any rim
enhancement of the cystic contents were evaluated in the 17 CT examinations where contrast
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medium was used. With MRI, for the criterion of the signal intensity, the musculature was defined as an intermediate signal on T1WI, and the cerebrospinal fluid as a bright high signal on T2WI.
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MRI and CT features were compared with the imaging features of KCOTs and odontogenic cysts reported earlier.4-9
The radiological findings were compared with histopathological diagnosis and surgery reports.
Results
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The present study was approved by the Ethics Committee of HUCH.
The distribution of the location, largest dimensions and histopathological diagnoses of the
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ameloblastomas are shown in Table 1. The dimensions of the ameloblastomas varied from 10 mm to 110 mm, the largest extending from the mandible to the zygoma. 16/26 (62%) of the tumours
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involved the posterior body, angle and/or ramus of the mandible, whereas five occurred in the maxilla. All maxillary ameloblastomas involved the maxillary sinus and three of them extended into the nasal fossa or ethmoid (Figures 1 and 2). The CT (n=20) and MRI (n=5) features of non-unicystic ameloblastomas (n=20) are given in Table 2 and Table 3, respectively. Vast majority (12/15) of the non-unicystic type ameloblastomas in the mandible were multilocular, whereas five ameloblastomas in the maxillary sinus did not show multilocularity. Multilocularity was apparent already in a panoramic radiograph, but CT revealed
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ACCEPTED MANUSCRIPT more clearly the internal architecture. Multiple curved septa providing a “soap bubble” or a honeycombed appearance was present in 6/15 of these cases (Table 2, Figures 3 and 4). Of all non-unicystic ameloblastomas (n=20), 14 had a mixed cystic and solid pattern based on contrast-enhanced CT or MRI (Figures 4 and 5). In three more, the content of the lesion appeared
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mixed isodense and hypodense to muscle based on non-contrast CT. Two small solid/multicystic ameloblastomas had a solid content. One non-unicystic ameloblastoma histopathologically
suggestive as being the result of neoplastic transformation of dentigerous cyst epithelium showed
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thick rim enhancement in otherwise cystic lesion in contrast-enhanced CT (Figure 6).
On MRI (n=5), all non-unicystic ameloblastomas showed homogeneous intermediate signal on
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T1WI. The cystic areas showed homogeneous bright high signal on T2WI and thick rim enhancement, whereas solid compartments showed heterogeneous or homogeneous high signal on T2WI and heterogeneous or homogeneous enhancement (Figure 7, Table 3). Three of the sinonasal solid/multicystic ameloblastomas (n=5) showed similar heterogeneous
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enhancement pattern and differed from mandibular ameloblastomas that showed separate solid and cystic compartements (Figures 1 and 2).
The CT findings of unicystic ameloblastomas (n=6) are given in Table 4. Three of the unicystic
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ameloblastomas had a multilocular appearance, whereas three appeared as a circumscribed radiolucency that surrounded the crown of an unerupted mandibular third molar, thus resembling a
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dentigerous cyst on the panoramic radiograph (Figure 8). Contrast-enhanced CT showed a cystic lesion with irregularly thick rim-enhancement or contrast-enhancing solid component in two of these cases, whereas one showed cystic content in non-contrast CT. The other three unicystic ameloblastomas did not resemble dentigerous cysts, because of their multilocular pattern and their atypical location in the mandibular body. In contrast-enhanced CT, they showed a cystic lesion with intraseptal enhancement or a mixed cystic and solid pattern (Figure 9, Table 4).
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ACCEPTED MANUSCRIPT On CT, all ameloblastomas showed expansion and thinning of mandibular cortical plates or maxillary sinus wall. Panoramic radiographs failed to reveal expansion of buccal and lingual cortical plates. Extreme expansion was presented by large tumours, especially in the mandibular ramus (Figure 5). Perforation was present in 20/26 (77%) cases. Perforation was evident already at
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an early state, i.e. , in small ameloblastomas. Extensive root resorption of adjacent teeth was evident in 72% (8/11) of the cases that involved tooth-bearing areas (Figure 9). Dislocation of a tooth was
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noted in four cases.
Discussion
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Characteristic radiological features of ameloblastomas were multilocularity and a tendency to cause cortical expansion and perforation that was frequently present already at the early stage. Although multilocular appearance was already visible in a panoramic radiograph, panoramic radiography failed to reveal buccal and lingual cortical perforation characteristic for ameloblastoma. The
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apparent tendency of an ameloblastoma to cause marked expansion and perforation is an important differential diagnostic aspect. KCOTs have a similar site predilection and often have a multilocular appearance, and therefore may resemble ameloblastoma in panoramic radiography. Contrary to
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ameloblastoma, KCOT has a tendency to grow along the longitudinal axis of the mandible body.7, 8 In this aspect, CT greatly aids in differential diagnosis, because it allows three-dimensional
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visualisation of cortical bone and reveals the internal bony architecture, i.e., a honeycombed or a “soap-bubble” appearance characteristic for some ameloblastomas. The use of a bone algorithm in MSCT is recommended in order to clearly evaluate fine bony structures. For solving dentoalveolar problems, CBCT is the recommended imaging modality because the radiation dose to the patient is lower than with MSCT.10 However, CBCT does not allow visualisation of the contents of the lesion due its poor soft tissue contrast. Therefore, its diagnostic value in tumour diagnosis is weak,
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ACCEPTED MANUSCRIPT although it allows visualisation of bony structures and cortical bone and in this regard helps the radiologist. In the present series, fourteen (70%) of all non-unicystic ameloblastomas showed varying combinations of solid and cystic contents on contrast-enhanced CT or MRI. Our analysis suggests
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that contrast-enhanced CT and MRI enable differentiating non-unicystic ameloblastomas and odontogenic cysts because the latter do not show solid content and tend to show thin rim-
enhancement in an otherwise cystic lesion.6 This is in agreement with many earlier reports
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demonstrating the characteristic pattern of mixed cystic and solid contents of ameloblastomas and the differential diagnostic value of MRI 6, 9, 11 In the present series, seven cases with non-unicystic
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ameloblastoma were non-contrast CT examinations. Four of these patients also underwent MRI thus allowing reliable analysis of the content of the lesion in four of these cases. Non-contrast CT with soft tissue algorithm allows evaluation of the content of the lesion based on density value and when comparing attenuation with surrounding muscle. In the three non-contrast cases the contents of the
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lesions were evaluated as hypodense, isodense and mixed hypo- and isodense to muscle, respectively (Table 2). CT density values significantly lower than muscle correspond cystic content, whereas contents with higher attenuation values cannot be reliable analysed based on non-contrast
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CT only. This is because the cyst lumen of KCOTs frequently displays high attenuation areas on native CT because of intraluminal desquamated keratin. 4, 5, 8 The use of diffusion-weighted MRI
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and dynamic contrast-enhanced MRI as a means of differentiating KCOTs from the cystic contents of ameloblastomas has been studied based on apparent diffusion coefficient (ADC) values and signal intensities.11-16,
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Srinivasan et al.14 reported significant differences in ADC values between
KCOTs and cystic ameloblastomas due, at least partly, to the keratin content of KCOTs. In our series, the cystic components of two non-unicystic ameloblastomas showed homogeneous bright high signal intensities on T2WI corresponding non-proteinous cystic content.
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ACCEPTED MANUSCRIPT Six out of the 26 ameloblastomas (23%) were histologically classified as unicystic. This is somewhat higher than in previous studies, in which unicystic ameloblastomas represent 5-15% of
all intraosseous ameloblastomas. 17, 18 The selection criterion in the present study, i.e., preoperative CT or MRI imaging, may explain the high occurrence of unicystic ameloblastomas in the present
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series. In our study, the age distribution of patients with unicystic ameloblastoma was 14-31 years (except for one patient aged 83 years), whereas the mean age for solid/multicystic ameloblastomas was 51 years. This is in agreement with earlier reports demonstrating the peak incidence in a
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younger age group for unicystic ameloblastomas.18
Three of the unicystic ameloblastomas were unilocular resembling dentigerous cysts in the
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panoramic radiograph. In our study, however, contrast-enhanced CT revealed irregularly thick rimenhancement or intraluminal solid component, providing a clue to the correct diagnosis of unicystic ameloblastoma (Figure 8). None of the patients with unicystic ameloblastoma underwent MRI. MRI provides better soft tissue contrast resolution than CT, and presumably small solid intraluminal or
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mural components characteristic for unicystic ameloblastomas would be detected even more easily with MRI, as has been reported earlier. 13-15, 17 Nevertheless, based on our analysis, CT allowed visualization of these intraluminal solid nodules, although the diagnosis was dependent on careful
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evaluation and use of high-resolution CT.
Radiological diagnosis of unicystic ameloblastomas is valuable in planning surgical treatment, since
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surgical findings of unicystic ameloblastomas may also suggest that the lesion in question is a cyst, and the final diagnosis of ameloblastoma is made only after a microscope examination of the specimen. In the Department of Oral and Maxillofacial Diseases, surgical treatment of unicystic ameloblastoma differs from that of dentigerous cyst. Unicystic ameloblastomas require a resection with slight margins, whereas dentigerous cysts can be enucleated, often leaving the surrounding bone almost intact. However, in the literature a conservative approach has also been advocated.19 Other types of ameloblastoma are often treated by block resection in order to achieve free margins.
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Three of the histopathologically diagnosed unicystic ameloblastomas did not resemble dentigerous cysts since their multilocular pattern and their atypical location in the mandibular body. A clear predominance of unilocular appearance for unicystic ameloblastoma has been reported and it has been questioned whether a unicystic ameloblastoma can have a truly multilocular radiographic 21
Based on our data, multilocular unicystic ameloblastomas do exist, as previously
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presentation.20, reported.17
It has been debated whether unicystic ameloblastoma originates either de novo or as the result of
certainty which mechanism occurs in an individual case.
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neoplastic transformation of odontogenic cyst epithelium, and it may be impossible to decide with
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In the present series, two ameloblastomas were suggestive of a neoplastic transformation into dentigerous cyst epithelium with ameloblastomatous growth in part of the epithelium. Another showed a large cyst involving the mandibular angle and ramus. The contrast-enhanced CT showed the cyst cavity to have thicker rim enhancement than usually seen in odontogenic cysts (Figure 6).
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The thickness of the rim suggested an infected cyst, and the tumour was enucleated as a dentigerous cyst prior to final diagnosis. So far, after three years’ follow-up, there has been no recurrence. The other involved an impacted third molar and thus simulated dentigerous cyst in panoramic
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radiography. MRI examination showed a sizable cystic portion of the tumour to have a intermediate signal in T1W images, homogeneously bright high signal intensity in T2W images and thick rim-
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enhancement after contrast administration. However, an enhancing pericoronal soft-tissue nodule was visible on MRI, thus excluding the radiological diagnosis of a conventional dentigerous cyst (Figure 7).
Three sinonasal ameloblastomas showed similar heterogeneous enhancement pattern and differed from mandibular ameloblastomas that showed separate solid and cystic compartements (Figures 1 and 2). All these sinonasal ameloblastomas had mixed solid/multicystic appearance and histopathologically follicular, plexiform or granular growth pattern. However, the radiological
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ACCEPTED MANUSCRIPT enhancement pattern was similar despite the histological appearance. Sinonasal ameloblastomas usually originate in the maxilla and extend to sinonasal region secondarily. However, primary sinonasal ameloblastomas, without extension from the gnathic region, and with similar
enhancement pattern than in our case, has also been reported. 22 It has been speculated that during
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embryological development odontogenic epithelium might get trapped to sinonasal area. This might explain the different enhancement pattern for sinonasal ameloblastomas in the present series.
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Conclusions
Characteristic radiological features of ameloblastomas are multilocularity, a tendency to cause
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marked expansion and perforation of cortical plates at an early stage, marked root resorption and a mixed cystic and solid content. A tendency for an ameloblastoma to cause marked expansion and perforation is an important differential diagnostic aspect, which cannot be visualize by means of conventional 2-dimensional imaging alone. Both contrast-enhanced CT and MRI allow reliable
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differential diagnosis between non-unicystic ameloblastomas and other odontogenic cystic lesions based on different contents of these lesions, whereas non-contrast CT is of limited value. In the diagnosis of ameloblastomas derived from cyst epithelium or unicystic ameloblastomas that
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resemble a dentigerous cyst visualisation of the content by means of contrast-enhanced CT or MRI is essential. In the present series, three ameloblastomas involved the maxillary sinus and extended
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into the nasal fossa or ethmoid area. Ameloblastoma should be included in the differential diagnosis of benign tumours in the sinonasal area.
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ACCEPTED MANUSCRIPT References 1. Verbin R, Barnes L. Cysts and cyst-like lesions of the oral cavity, jaws and neck. In: Barnes L, editor. Surgical Pathology of the Head and Neck. New York: Marcel Dekker; 2000, p.1437-1555. 2. Barnes L, Eveson JW, Reichart P, Sidransky D. World Health Organization classification of
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tumours. Pathology and genetics of head and neck tumours. Lyon: IARC Press; 2005.
3. Ackermann GL, Altini M, Shear M. The unicystic ameloblastoma: a clinicopathological study of 57 cases. J Oral Pathol 1988;17:541-546.
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4. Yoshiura K, Higuchi Y, Ariji Y, Shinohara M, Yasa K, Nakayama E, et al. Increased attenuation in odontogenic keratocysts with CT:a new finding. Dentomaxillofac Radiol 1994;23:138-142.
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5. Yonetsu K, Bianchi JG, Troulis MJ, Curtin HD. Unusual CT appearance in an odontogenic keratocyst of the mandible:case report. Am J Neuroradiol 2001;22:1887-1889. 6. Hisatomi M, Asaumi J, Konouchi H, Shigehara H, Yanagi Y, Kishi K. MR imaging of epithelial cysts of the oral and maxillofacial region. Eur J Radiol 2003;48:178-182.
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7. MacDonald-Jankowski DS, Li TK. Keratocystic odontogenic tumour in a Hong Kong community: The clinical and radiological features. Dentomaxillofacial Radiol 2010;39:167-175. 8. Apajalahti S, Hagström J, Lindqvist C and Suomalainen A. CT findings and recurrence of
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keratocystic odontogenic tumor of the mandible and maxillofacial region in a series of 46 patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;111:e39-e37.
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9. Minami M, Kaneda T, Ozawa K, yamamoto H, Itai Y, Ozawa M, Yoshikawa K and Sasaki Y. Cystic lesions of the maxillomandibular region: MR imaging distinction of odontogenic keratocysts and ameloblastomas from other cysts. AJR Am J Roentgenol 1996;166(4):943-949. 10. Hashimoto K, Arai Y, Iwai K, Araki M, Kawashima S, Terakado M. A comparison of a new limited cone beam computed tomography machine for dental use with multidetector row helical CT machine. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;95:371-377.
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Nagatsuka H and Asaumi J-I. Diagnostic value of MRI for odontogenic tumours. Dentomaxillofac Radiol 2013;42:20120265. 12. Asaumi J-i, Hisatomi M, Yanagi Y, Matsuzaki H, Choi Y K, Kawai N, Konouchi H and Kishi
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K. Assessment of ameloblastomas using MRI and dynamic contrast-enhanced MRI. Eur J radiol 2005;56:25-30.
13. Hisatomi M, Yanagi Y, Konouchi H, Matsuzaki H, Takenobu T, Unetsobu T and Asaumi J.
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Diagnostic value of dynamic contrast-enhanced MRI for unilocular cystic-type ameloblastomas with homogeneously bright signal intensity on T2-weighted or STIR MR images. Oral Oncology
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2011;47:147-152.
14. Srinivasan K, Seith Balla A, Sharma A, Roychoudhury A and Bhutia O. Diffusion-weighted imaging in the evaluation of odontogenic cysts and tumours. Brit J Radiol 2012; 85:e864-e870. 15. Konouchi H, Asaumi J-i, Yanagi Y, Hisatomi M, Kawai N, Matsuzaki H and Kishi K.
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Usefulness of contrast enhanced-MRI in the diagnosis of unicystic ameloblastoma. Oral Oncology 2006;42:481-486.
16. Sumi M, Ichikawa Y, Katayama I, Tashiro S, Nakaruma T. Diffusion-Weighted MR Imaging of
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Ameloblastomas and Keratocystic Odontogenic Tumours: Differentiation by Apparent Diffusion Coefficients of Cystic Lesions. AJNR. Am J Neuroradiol 2008;29:1897-1901.
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17. Singh A, Shaikh S, Samadi FM and Shrivastava S. Maxillary unicystic ameloblastoma: A review of the literature. Natl J Maxillofac Surg 2011;2(2):163-168. 18. Seintou A, Martinelli-Kläy CP and Lombardi T. Unicystic ameloblastoma in children: systematic review of clinicopathological features and treatment outcomes. Int J Oral and Maxillofac Surg 2014;41:405-412.
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ACCEPTED MANUSCRIPT 19. Ahmad I, Choudhary R. Wide surgical excision with split rib graft reconstruction of mandible for ameloblastoma; our 10 year experience. Indian J Otolaryngol Head Neck Surg 2013;65(1):4043.
Cancer B:oral Oncol 1995;31B:86-99.
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20. Reichart PA, Philipsen HP, Sonner S. Ameloblastoma: biological profile of 3677 cases. Eur J
21. Gardner DG. Critique of the 1995 review by Reichart et al. of the biologic profile of 3677 ameloblastomas. Oral Oncol 1999;35:443-449.
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22. Guilemany JM, Ballesteros F, Alós L, Alobid I, Prades E, Menéndez LM and Cardesa A. Plexiform ameloblastoma presenting as a sinonasal tumor. Eur Arch Otorhinolaryngol
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2004;261:304-306.
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ACCEPTED MANUSCRIPT Figure 1. Contrast-enhanced CT shows a solid/multicystic (follicular pattern) ameloblastoma presenting as a sinonasal tumour. The tumour occupies the right maxillary sinus, nasal fossa and ethmoid air cells and reaches the cribriform plate. Heterogeneity of enhancement is evident,
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corresponding to the solid and multicystic contents of the tumour.
Figure 2. A solid/multicystic (plexiform pattern) ameloblastoma occupying the left maxillary sinus and extending into the nasal fossa. A. A cloudy sinus with remodelled and fragmented sinus wall is
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evident even in a panoramic radiograph (arrows). B and C. Contrast-enhanced CT shows a
heterogeneous enhancement pattern. The tumour appears to arise from the antral floor and alveolus,
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where there is bone destruction. D. Bony fragments are present (arrows) originating from the sinus wall.
Figure 3. A cropped panoramic radiograph (A) and axial bone window CT scan from superior to
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inferior (B-D) of the same patient showing a solid/multicystic (follicular pattern) ameloblastoma in the mandibular premolar area with a “soap bubble” appearance.
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Figure 4. A solid/multicystic ameloblastoma (follicular pattern) involving the mandibular incisor area. Native (A, B) and contrast-enhanced (C, D) CT scans demonstrating a mixed solid and cystic
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pattern of the tumour. C. Contrast-enhanced CT shows an enhancing mass in the midline representing the solid component of the tumour (arrow in C), whereas a slightly inferior contrastenhanced CT scan shows a cystic non-enhancing content (arrow in D). Bone window CT scans (E and F) show a “soap bubble” appearance.
Figure 5. A. Preoperative panoramic radiograph showing a large ameloblastoma in the right mandible causing expansion of the mandibular body, ramus and coronoid process.
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ACCEPTED MANUSCRIPT C. Contrast-enhanced CT shows an enhancing nodule in the caudal part of the tumour corresponding to the solid content (arrow in C) while the main portion of the tumour is cystic. D. On CT with bone algorithm the loculated margin is evident (arrow in D). B. Postoperative
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panoramic radiograph after mandibular resection and reconstruction with a customised prosthesis.
Figure 6. A. Native and B. contrast-enhanced axial CT scan of an ameloblastoma suggestive as being the result of neoplastic transformation of dentigerous cyst epithelium showing thick rim
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enhancement (arrow in B).
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Figure 7. (A) Panoramic radiograph of an ameloblastoma in a pericoronal relationship with an impacted and slightly displaced 3rd molar mimicking an odontogenic cyst. (B) Axial T2-weighted, (C) T1-weighted, fat suppressed and (D) T1-weighted, fat suppressed, contrast-enhanced MR images show a cystic lesion with relatively thick rim enhancement (arrow in D). (E, F and G)
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Corresponding MR images slightly caudal to levels B, C and D show an enhancing pericoronal softtissue mass (arrow in G). This was an ameloblastoma histopathologically suggestive as the result of
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neoplastic transformation of a dentigerous cyst.
Figure 8. A. Panoramic radiograph of a unicystic ameloblastoma in a pericoronal relationship with
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an impacted and slightly displaced 3rd molar mimicking a dentigerous cyst. B. Panoramic radiograph of another patient with a unilocular ameloblastoma resembling a dentigerous cyst. C. Contrast-enhanced CT of the same patient as in B. The internal low density is suggestive of a cystic lesion; however, an enhancing tiny mural nodule provides a clue to unicystic ameloblastoma.
Figure 9. A. Panoramic radiograph of a unicystic ameloblastoma involving the mandibular body. Distinct resorption of roots of associated teeth is evident (arrows in A). C. Native and D. contrast-
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enhanced CT. The content of the tumour is cystic; however, some enhancement of the septations is evident (arrow in D). Histological analysis of the surgical specimen showed a unicystic ameloblastoma without intraluminal or mural component. B. Bone window CT showing septa in the
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Table 1 Clinical features and histopathological diagnosis of ameloblastomas (n=26). __________________________________________________________________________________________
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Age
Sex
Location
Maximum diameter (mm)
Histopathological diagnosis __________________________________________________________________________________________ F
mandibular incisor
12
solid/multicystic
2. 55
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mandibular symphysispremolar
43
solid/multicystic
3. 44
F
mandibular premolar
20
solid/multicystic
4. 62
F
mandibular premolar
10
solid/multicystic
5. 34
F
mandibular body
25
solid/multicystic
6. 20
F
mandibular body
20
7. 29
F
mandibular body
27
8. 30
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mandibular body
25
9. 73
M
mandibular body-ramus, zygoma
110
10. 67
F
mandibular angle-ramus
80
11. 58
M
maxillary sinus
33
12. 64
M
maxillary sinus, extending into the nasal fossa and ethmoid
63
13. 84
M
maxillary sinus, extending into the nasal fossa and ethmoid
55
solid/multicystic
14. 60
M
maxillary sinus
25
solid/multicystic
15. 80
M
maxillary sinus, nasal fossa
55
solid/multicystic
16. 58
M
mandibular premolar
13
peripheric (follicular)
17. 57
F
mandibular body
35
peripheric
18. 56
M
mandibular angleramus
60
neoplastic transformation of dentigerous cyst epithelium
19. 26
F
mandibular angle-ramus, third molar involved
58
neoplastic transformation of dentigerous cyst epithelium
20. 52
M
mandibular angle
25
unspecified
21. 35
F
mandibular body
65
unicystic (luminal)
22. 21
F
mandibular agle-ramus, impacted third molar involved
33
unicystic (mural)
F
mandibular body-angle-ramus
50
unicystic (intraluminal and mural)
M
mandibular angle-ramus
65
unicystic
F
mandibular body-ramus, impacted third molar involved
75
unicystic
M
mandibular angle, third molar involved
40
unicystic (mural)
24. 83 25. 23 26. 14
solid/multicystic solid/multicystic
solid/multicystic
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23. 31
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1. 41
solid/multicystic solid/multicystic
solid/multicystic
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1. solid/multicystic
*
2. solid/multicystic (Fig.4)
Locularity
_______________________________________________________ non-contrast contrastboth non-contrast (attenuation) enhanced and contrast
multilocular with honeycombed pattern
content isodense to muscle
multilocular with soap-bubble appearance *
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Histopathological diagnosis (Figure number)
mixed cystic and solid
isodense
4. solid/multicystic
multilocular with honeycombed pattern
isodense
5. solid/multicystic
multilocular with honeycombed pattern
6. solid/multicystic (Fig.3)
multilocular with soap-bubble appearance
7. solid/multicystic
multilocular
8. solid/multicystic
multilocular
9. solid/multicystic
multilocular
10. solid/multicystic (Fig.5)
multilocular
11. solid/multicystic
maxillary sinus
mixed solid and cystic
12. solid/multicystic (Fig.1)
sinonasal
heterogeneous enhancement
13. solid/multicystic
sinonasal
14. solid/multicystic
maxillary sinus
mixed cystic and solid
sinonasal
heterogeneous enhancement
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mixed cystic and solid
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*
mixed cystic and solid
mixed cystic and solid
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15. solid/multicystic (Fig.2)
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multilocular with honeycombed pattern
3. solid/multicystic
mixed cystic and solid
mainly isodense minor hypodense areas involved mixed cystic and solid (mainly cystic)
heterogeneous enhancement
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*
intraosseal component unilocular
18. neoplastic transformation of dentigerous cyst epithelium (Fig.6) *
mixed cystic and solid
hypodense (intraosseal cystic component) isodense (peripheric component)
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17. peripheric
multilocular
unilocular
thick rim-enhancement
multilocular
hypodense
20. unspecified
unilocular
hypodense
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19. neoplastic transformation of dentigerous cyst epithelium
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16. peripheric
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patients that also underwent MRI, see Table 3
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*
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T2
solid/multicystic
homogeneous intermediate
homogeneous high
3.
solid/multicystic
homogeneous intermediate
homogeneous high heterogeneous high
15.
solid/multicystic
homogeneous intermediate
17.
peripheric
homogeneous intremediate
homogeneous intermediate
homogeneous enhancement
heterogeneous enhancement
homogeneous bright high (intraosseal cystic part) + heterogeneous (peripheric, solid component)
thick rim-enhancement (intraosseal cystic part) + heterogeneous enhancement (solid part)
homogeneous brigt high (cystic component) + homogeneous high (pericoronal solid component)
thick rim-enhancement (cystic component) + homogeneous enhancement (pericoronal solid component)
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19. neoplastic transformation of dentigerous cyst epithelium (Fig.7)
homogeneous enhancement
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1.
T1 + Gd
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T1
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Patient number and histopathological diagnosis
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Table 4. CT findings of unicystic ameloblastomas (n=6). __________________________________________________________________________________________________________________________ Locularity
TT
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Patient number and histopathological diagnosis
non-contrast attenuation value
contrast-enhanced
both non-contrast and contrast-enhanced
multilocular
22. unicystic (mural) (Fig.8a)
unilocular third molar involved
23. unicystic (intraluminal and mural)
multilocular
cystic + intraseptal enhancement
cystic + irregularly thick rim-enhancement mixed cystic and solid (mainly cystic)
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21. unicystic (luminal) (Fig.9)
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_______________________________________________________________________________________________________________________________________
multilocular
cystic (hypodense to muscle)+ thick isodense rim
25. unicystic (Fig.8b,c)
unilocular third molar involved
26. unicystic (mural)
unilocular developing third molar involved
cystic with small contrast-enhanced solid component
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24. unicystic (mural)
cystic (hypodense to muscle)
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Ameloblastomas and other cyst-like pathologies in the maxillomandibular regions display common radiologic features in conventional dentoalveolar imaging (panoramic radiograph). We have retrospectively viewed the MRI and MSCT images of 26 patients having been diagnosed with ameloblastoma in order to evaluate the differential diagnostic features of this benign but locally
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aggressive odontogenic tumour. The effective preoperative differential diagnosis may help surgeons plan treatment because ameloblastomas often require more radical treatment than odontogenic
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cysts.
S2212-4403(15)00897-4
DOI:
10.1016/j.oooo.2015.05.002
Reference:
OOOO 1191
To appear in:
Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology
Received Date: 4 February 2015 Revised Date:
25 April 2015
Accepted Date: 6 May 2015
Please cite this article as: Apajalahti S, Kelppe J, Kontio R, Hagström J, Imaging characteristics of ameloblastomas and diagnostic value of CT and MRI in a series of 26 patients, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2015), doi: 10.1016/j.oooo.2015.05.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Imaging characteristics of ameloblastomas and diagnostic value of CT and MRI in a series of 26 patients Satu Apajalahti, DDS, PhD, a Jetta Kelppe, DDS, b Risto Kontio, MD, DDS, PhD, c and Jaana Hagström, DDS, PhD d HUS Medical Imaging Center, Department of Radiology, Helsinki University Central Hospital
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a
([email protected])
c
Department of Oral Pathology, University of Helsinki ([email protected])
Department of Oral and Maxillofacial Diseases, Helsinki University Central Hospital
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b
d
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([email protected])
Department of Pathology/Haartman Institute and HUSLab, Helsinki University Central Hospital
([email protected])
Satu Apajalahti, DDS, PhD
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Corresponding author:
HUS Medical Imaging Center
PO Box 263
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Department of Radiology, Helsinki University Central Hospital
FI-00029 HUS, Helsinki
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Finland
e-mail: [email protected] mobile: +358 40 5868994
Conflict of interest: none
Word count: abstract 154; manuscript 2884; number of references 22; number of figures 9; number of tables 4
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Objectives. To evaluate the imaging characteristics of ameloblastomas and to analyse the diagnostic value of CT and MRI compared with conventional dentoalveolar imaging. Study Design. In this observational retrospective study the panoramic radiographs (n=25), CT
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(n=26) and MRI (n=5) images of histopathologically verified ameloblastomas in 26 patients were reviewed.
Results. Characteristic findings were multilocularity, marked expansion of the cortical plate,
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perforation at an earlier stage and extensive root resorption. On contrast-enhanced CT or MRI,
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majority (14/17) of the non-unicystic ameloblastomas contained a mixed cystic and solid pattern. Unicystic ameloblastomas (n=6) and ameloblastomas derived from the cyst epithelium (n=2) showed thick rim-enhancement or mural solid component in an otherwise cystic lesion. Conclusions. Contrast-enhanced CT and MRI greatly aid in differential diagnosis between
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ameloblastomas and other cyst-like lesions because they allow visualisation of a mixed cystic and solid content characteristic for non-unicystic ameloblastomas. The differential diagnostic value of
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CT and MRI is significant regarding unicystic ameloblastomas.
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ACCEPTED MANUSCRIPT Introduction
Ameloblastomas are a group of benign, locally aggressive tumours in the maxillomandibular region originating from odontogenic epithelium. Ameloblastoma is the second most common odontogenic tumour after keratocystic odontogenic tumour (KCOT).1 Ameloblastomas are often asymptomatic
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and are frequently detected during routine panoramic radiography. A painless swelling of the jaw is the usual clinical presentation. According to the WHO histological classification, ameloblastomas are divided into solid/multicystic, extraosseous/peripheral, desmoplastic and unicystic types.2
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Unicystic ameloblastomas are further classified into luminal (ameloblastomatous cyst epithelium), mural (tumour growth invading the fibrous wall of the cyst) and intraluminal (protruding into the
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cyst cavity) types. All growth patterns may be seen in the same tumour.3 Rarely does an ameloblastoma exhibit malignant behaviour. In the present department two cases of ameloblastic carcinomas have been diagnosed between 2005 and 2014.4
The treatment of ameloblastomas is surgical and more radical than in the case of KCOTs and other
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cystic lesions. Solid/multicystic ameloblastomas require segmental or en bloc resection and reconstruction with free cancellous bone and fixation plate. In the case of a large block resection a free vascularized bone flap should be considered. KCOTs and other cystic lesions are often treated
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by enucleation. In conventional two-dimensional imaging (panoramic radiograph) differential diagnosis between ameloblastomas and cystic lesions is not straightforward. Cone beam computed
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tomography (CBCT) produces three-dimensional images of the bony structures and cortical bone but does not allow visualisation of the contents of the lesion due its poor soft tissue contrast. In the present observational retrospective study we reviewed the panoramic radiographs, helical CT and MRI examinations of 26 patients with histopathologically diagnosed ameloblastoma in order to evaluate the imaging characteristics of the tumour and to assess the value of CT and MRI compared with conventional dentoalveolar imaging (panoramic radiograph). In addition, we wanted to find
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ACCEPTED MANUSCRIPT out whether CT and MRI features reflected the histopathological pattern of different types of ameloblastoma in the present series.
Materials and methods
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Patients
The patients were primarily selected from the Q-pati database, Department of Pathology, HusLab, Helsinki University Central Hospital, having been diagnosed with ameloblastoma between 2000
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and 2013 (n=34). Of these, 26 patients (age range 18-82 years; mean 48 years) who had undergone MSCT and/or MRI examination at HUS Medical Imaging Center before surgical treatment, were
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selected for this study.
Based on their histology, 15/26 (58%) the majority (61%) of the ameloblastomas were solid/multicystic types, six were unicystic and two were diagnosed as peripheral ameloblastomas. Nine Over half (57%) of the solid/multicystic ameloblastomas showed a mainly follicular growth
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pattern. Two of the ameloblastomas cases were histopathologically suggestive as being primarily dentigerous cysts with ameloblastomatous growth. In one case three cases the histological subtype was unclear. Microscope examination showed four of the unicystic type ameloblastomas to have a
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mural or intraluminal component, one was luminal, whereas in one unicystic type no information
Imaging
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concerning the subtype was obtained. Malignant ameloblastomas were excluded.
Panoramic radiography (Scanora, Soredex, Finland or OP 200 Instrumentarium Imaging, Finland) was performed in 25 patients prior to additional imaging. All patients underwent MSCT examination. High-resolution helical CT scanning (slice thickness 1.25 mm, slice interval 0.63 mm) was performed using either a 4- or 16-slice scanner (Light Speed Plus or Bright Speed; GE Medical Systems, Milwaukee, US) with bone and soft tissue algorithms.
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ACCEPTED MANUSCRIPT The data were reformatted into 2.0 mm or 2.5 mm-thick axial, coronal and sagittal images. In 17 cases, contrast medium (Ultravist, 300 mgI/mL; Schering, Germany, or Omnipaque, 350 mgI/mL; GEHealthcare) was used. Of these, in six patients scanning was first performed without contrast medium and then with contrast enhancement. The remaining nine cases were non-contrast
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examinations.
In addition to non-contrast CT examination, five patients also underwent MRI. MRI examination (n=5) was performed using a 1.5 T unit (Magnetom Vision; Siemens, Erlangen, Germany). One
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MRI examination was performed elsewhere. The imaging protocol consisted of axial and coronal T2-weighted fast spin echo (FSE) images with fat-suppression (fs) and axial T1W FSE images
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(slice thickness 3 mm) with and without fs. After intravenous administration of gadolinium (Magnevist, 0.5 mmol/mL; Schering, Germany), axial and coronal T1W fs images (slice thickness 3 mm) were acquired.
In addition, in three patients CBCT examination was performed elsewhere, and was available for
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Image analysis
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The radiological findings were compared with histopathological diagnosis.
The MRI and CT images were retrospectively viewed on a Dome E2 greyscale display (size 19.6
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in.; Planar Systems, Beaverton, USA) with a display resolution of 1,200 x 1,600 pixels by an experienced oral radiologist.
On panoramic radiographs, the following were assessed: location, locularity (unilocular or multilocular), expansion in two dimension, as well as tooth association, tooth displacement or root resorption. On CT with the bone algorithm, the features assessed, in addition to those examined on panoramic radiograph included size of the tumour, internal bony architecture, three dimensional expansion and
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cortical perforation. Perforation was considered if not even a thinned cortical plate was visible in an expanded cortex. With CT, the contents of the tumours were divided into either solid or cystic components based on CT density values and contrast enhancement. On CT without contrast enhancement, density values averaging that of the cerebrospinal fluid (hypodense to muscle) and
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musculature (isodense to muscle) were designated as cystic and non-cystic components,
respectively. Additionally, the enhancement pattern of solid structures as well as any rim
enhancement of the cystic contents were evaluated in the 17 CT examinations where contrast
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medium was used. With MRI, for the criterion of the signal intensity, the musculature was defined as an intermediate signal on T1WI, and the cerebrospinal fluid as a bright high signal on T2WI.
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MRI and CT features were compared with the imaging features of KCOTs and odontogenic cysts reported earlier.4-9
The radiological findings were compared with histopathological diagnosis and surgery reports.
Results
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The present study was approved by the Ethics Committee of HUCH.
The distribution of the location, largest dimensions and histopathological diagnoses of the
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ameloblastomas are shown in Table 1. The dimensions of the ameloblastomas varied from 10 mm to 110 mm, the largest extending from the mandible to the zygoma. 16/26 (62%) of the tumours
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involved the posterior body, angle and/or ramus of the mandible, whereas five occurred in the maxilla. All maxillary ameloblastomas involved the maxillary sinus and three of them extended into the nasal fossa or ethmoid (Figures 1 and 2). The CT (n=20) and MRI (n=5) features of non-unicystic ameloblastomas (n=20) are given in Table 2 and Table 3, respectively. Vast majority (12/15) of the non-unicystic type ameloblastomas in the mandible were multilocular, whereas five ameloblastomas in the maxillary sinus did not show multilocularity. Multilocularity was apparent already in a panoramic radiograph, but CT revealed
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ACCEPTED MANUSCRIPT more clearly the internal architecture. Multiple curved septa providing a “soap bubble” or a honeycombed appearance was present in 6/15 of these cases (Table 2, Figures 3 and 4). Of all non-unicystic ameloblastomas (n=20), 14 had a mixed cystic and solid pattern based on contrast-enhanced CT or MRI (Figures 4 and 5). In three more, the content of the lesion appeared
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mixed isodense and hypodense to muscle based on non-contrast CT. Two small solid/multicystic ameloblastomas had a solid content. One non-unicystic ameloblastoma histopathologically
suggestive as being the result of neoplastic transformation of dentigerous cyst epithelium showed
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thick rim enhancement in otherwise cystic lesion in contrast-enhanced CT (Figure 6).
On MRI (n=5), all non-unicystic ameloblastomas showed homogeneous intermediate signal on
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T1WI. The cystic areas showed homogeneous bright high signal on T2WI and thick rim enhancement, whereas solid compartments showed heterogeneous or homogeneous high signal on T2WI and heterogeneous or homogeneous enhancement (Figure 7, Table 3). Three of the sinonasal solid/multicystic ameloblastomas (n=5) showed similar heterogeneous
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enhancement pattern and differed from mandibular ameloblastomas that showed separate solid and cystic compartements (Figures 1 and 2).
The CT findings of unicystic ameloblastomas (n=6) are given in Table 4. Three of the unicystic
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ameloblastomas had a multilocular appearance, whereas three appeared as a circumscribed radiolucency that surrounded the crown of an unerupted mandibular third molar, thus resembling a
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dentigerous cyst on the panoramic radiograph (Figure 8). Contrast-enhanced CT showed a cystic lesion with irregularly thick rim-enhancement or contrast-enhancing solid component in two of these cases, whereas one showed cystic content in non-contrast CT. The other three unicystic ameloblastomas did not resemble dentigerous cysts, because of their multilocular pattern and their atypical location in the mandibular body. In contrast-enhanced CT, they showed a cystic lesion with intraseptal enhancement or a mixed cystic and solid pattern (Figure 9, Table 4).
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ACCEPTED MANUSCRIPT On CT, all ameloblastomas showed expansion and thinning of mandibular cortical plates or maxillary sinus wall. Panoramic radiographs failed to reveal expansion of buccal and lingual cortical plates. Extreme expansion was presented by large tumours, especially in the mandibular ramus (Figure 5). Perforation was present in 20/26 (77%) cases. Perforation was evident already at
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an early state, i.e. , in small ameloblastomas. Extensive root resorption of adjacent teeth was evident in 72% (8/11) of the cases that involved tooth-bearing areas (Figure 9). Dislocation of a tooth was
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noted in four cases.
Discussion
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Characteristic radiological features of ameloblastomas were multilocularity and a tendency to cause cortical expansion and perforation that was frequently present already at the early stage. Although multilocular appearance was already visible in a panoramic radiograph, panoramic radiography failed to reveal buccal and lingual cortical perforation characteristic for ameloblastoma. The
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apparent tendency of an ameloblastoma to cause marked expansion and perforation is an important differential diagnostic aspect. KCOTs have a similar site predilection and often have a multilocular appearance, and therefore may resemble ameloblastoma in panoramic radiography. Contrary to
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ameloblastoma, KCOT has a tendency to grow along the longitudinal axis of the mandible body.7, 8 In this aspect, CT greatly aids in differential diagnosis, because it allows three-dimensional
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visualisation of cortical bone and reveals the internal bony architecture, i.e., a honeycombed or a “soap-bubble” appearance characteristic for some ameloblastomas. The use of a bone algorithm in MSCT is recommended in order to clearly evaluate fine bony structures. For solving dentoalveolar problems, CBCT is the recommended imaging modality because the radiation dose to the patient is lower than with MSCT.10 However, CBCT does not allow visualisation of the contents of the lesion due its poor soft tissue contrast. Therefore, its diagnostic value in tumour diagnosis is weak,
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ACCEPTED MANUSCRIPT although it allows visualisation of bony structures and cortical bone and in this regard helps the radiologist. In the present series, fourteen (70%) of all non-unicystic ameloblastomas showed varying combinations of solid and cystic contents on contrast-enhanced CT or MRI. Our analysis suggests
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that contrast-enhanced CT and MRI enable differentiating non-unicystic ameloblastomas and odontogenic cysts because the latter do not show solid content and tend to show thin rim-
enhancement in an otherwise cystic lesion.6 This is in agreement with many earlier reports
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demonstrating the characteristic pattern of mixed cystic and solid contents of ameloblastomas and the differential diagnostic value of MRI 6, 9, 11 In the present series, seven cases with non-unicystic
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ameloblastoma were non-contrast CT examinations. Four of these patients also underwent MRI thus allowing reliable analysis of the content of the lesion in four of these cases. Non-contrast CT with soft tissue algorithm allows evaluation of the content of the lesion based on density value and when comparing attenuation with surrounding muscle. In the three non-contrast cases the contents of the
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lesions were evaluated as hypodense, isodense and mixed hypo- and isodense to muscle, respectively (Table 2). CT density values significantly lower than muscle correspond cystic content, whereas contents with higher attenuation values cannot be reliable analysed based on non-contrast
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CT only. This is because the cyst lumen of KCOTs frequently displays high attenuation areas on native CT because of intraluminal desquamated keratin. 4, 5, 8 The use of diffusion-weighted MRI
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and dynamic contrast-enhanced MRI as a means of differentiating KCOTs from the cystic contents of ameloblastomas has been studied based on apparent diffusion coefficient (ADC) values and signal intensities.11-16,
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Srinivasan et al.14 reported significant differences in ADC values between
KCOTs and cystic ameloblastomas due, at least partly, to the keratin content of KCOTs. In our series, the cystic components of two non-unicystic ameloblastomas showed homogeneous bright high signal intensities on T2WI corresponding non-proteinous cystic content.
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all intraosseous ameloblastomas. 17, 18 The selection criterion in the present study, i.e., preoperative CT or MRI imaging, may explain the high occurrence of unicystic ameloblastomas in the present
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series. In our study, the age distribution of patients with unicystic ameloblastoma was 14-31 years (except for one patient aged 83 years), whereas the mean age for solid/multicystic ameloblastomas was 51 years. This is in agreement with earlier reports demonstrating the peak incidence in a
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younger age group for unicystic ameloblastomas.18
Three of the unicystic ameloblastomas were unilocular resembling dentigerous cysts in the
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panoramic radiograph. In our study, however, contrast-enhanced CT revealed irregularly thick rimenhancement or intraluminal solid component, providing a clue to the correct diagnosis of unicystic ameloblastoma (Figure 8). None of the patients with unicystic ameloblastoma underwent MRI. MRI provides better soft tissue contrast resolution than CT, and presumably small solid intraluminal or
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mural components characteristic for unicystic ameloblastomas would be detected even more easily with MRI, as has been reported earlier. 13-15, 17 Nevertheless, based on our analysis, CT allowed visualization of these intraluminal solid nodules, although the diagnosis was dependent on careful
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evaluation and use of high-resolution CT.
Radiological diagnosis of unicystic ameloblastomas is valuable in planning surgical treatment, since
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surgical findings of unicystic ameloblastomas may also suggest that the lesion in question is a cyst, and the final diagnosis of ameloblastoma is made only after a microscope examination of the specimen. In the Department of Oral and Maxillofacial Diseases, surgical treatment of unicystic ameloblastoma differs from that of dentigerous cyst. Unicystic ameloblastomas require a resection with slight margins, whereas dentigerous cysts can be enucleated, often leaving the surrounding bone almost intact. However, in the literature a conservative approach has also been advocated.19 Other types of ameloblastoma are often treated by block resection in order to achieve free margins.
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Three of the histopathologically diagnosed unicystic ameloblastomas did not resemble dentigerous cysts since their multilocular pattern and their atypical location in the mandibular body. A clear predominance of unilocular appearance for unicystic ameloblastoma has been reported and it has been questioned whether a unicystic ameloblastoma can have a truly multilocular radiographic 21
Based on our data, multilocular unicystic ameloblastomas do exist, as previously
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presentation.20, reported.17
It has been debated whether unicystic ameloblastoma originates either de novo or as the result of
certainty which mechanism occurs in an individual case.
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neoplastic transformation of odontogenic cyst epithelium, and it may be impossible to decide with
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In the present series, two ameloblastomas were suggestive of a neoplastic transformation into dentigerous cyst epithelium with ameloblastomatous growth in part of the epithelium. Another showed a large cyst involving the mandibular angle and ramus. The contrast-enhanced CT showed the cyst cavity to have thicker rim enhancement than usually seen in odontogenic cysts (Figure 6).
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The thickness of the rim suggested an infected cyst, and the tumour was enucleated as a dentigerous cyst prior to final diagnosis. So far, after three years’ follow-up, there has been no recurrence. The other involved an impacted third molar and thus simulated dentigerous cyst in panoramic
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radiography. MRI examination showed a sizable cystic portion of the tumour to have a intermediate signal in T1W images, homogeneously bright high signal intensity in T2W images and thick rim-
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enhancement after contrast administration. However, an enhancing pericoronal soft-tissue nodule was visible on MRI, thus excluding the radiological diagnosis of a conventional dentigerous cyst (Figure 7).
Three sinonasal ameloblastomas showed similar heterogeneous enhancement pattern and differed from mandibular ameloblastomas that showed separate solid and cystic compartements (Figures 1 and 2). All these sinonasal ameloblastomas had mixed solid/multicystic appearance and histopathologically follicular, plexiform or granular growth pattern. However, the radiological
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ACCEPTED MANUSCRIPT enhancement pattern was similar despite the histological appearance. Sinonasal ameloblastomas usually originate in the maxilla and extend to sinonasal region secondarily. However, primary sinonasal ameloblastomas, without extension from the gnathic region, and with similar
enhancement pattern than in our case, has also been reported. 22 It has been speculated that during
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embryological development odontogenic epithelium might get trapped to sinonasal area. This might explain the different enhancement pattern for sinonasal ameloblastomas in the present series.
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Conclusions
Characteristic radiological features of ameloblastomas are multilocularity, a tendency to cause
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marked expansion and perforation of cortical plates at an early stage, marked root resorption and a mixed cystic and solid content. A tendency for an ameloblastoma to cause marked expansion and perforation is an important differential diagnostic aspect, which cannot be visualize by means of conventional 2-dimensional imaging alone. Both contrast-enhanced CT and MRI allow reliable
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differential diagnosis between non-unicystic ameloblastomas and other odontogenic cystic lesions based on different contents of these lesions, whereas non-contrast CT is of limited value. In the diagnosis of ameloblastomas derived from cyst epithelium or unicystic ameloblastomas that
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resemble a dentigerous cyst visualisation of the content by means of contrast-enhanced CT or MRI is essential. In the present series, three ameloblastomas involved the maxillary sinus and extended
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into the nasal fossa or ethmoid area. Ameloblastoma should be included in the differential diagnosis of benign tumours in the sinonasal area.
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ACCEPTED MANUSCRIPT References 1. Verbin R, Barnes L. Cysts and cyst-like lesions of the oral cavity, jaws and neck. In: Barnes L, editor. Surgical Pathology of the Head and Neck. New York: Marcel Dekker; 2000, p.1437-1555. 2. Barnes L, Eveson JW, Reichart P, Sidransky D. World Health Organization classification of
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tumours. Pathology and genetics of head and neck tumours. Lyon: IARC Press; 2005.
3. Ackermann GL, Altini M, Shear M. The unicystic ameloblastoma: a clinicopathological study of 57 cases. J Oral Pathol 1988;17:541-546.
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4. Yoshiura K, Higuchi Y, Ariji Y, Shinohara M, Yasa K, Nakayama E, et al. Increased attenuation in odontogenic keratocysts with CT:a new finding. Dentomaxillofac Radiol 1994;23:138-142.
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5. Yonetsu K, Bianchi JG, Troulis MJ, Curtin HD. Unusual CT appearance in an odontogenic keratocyst of the mandible:case report. Am J Neuroradiol 2001;22:1887-1889. 6. Hisatomi M, Asaumi J, Konouchi H, Shigehara H, Yanagi Y, Kishi K. MR imaging of epithelial cysts of the oral and maxillofacial region. Eur J Radiol 2003;48:178-182.
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7. MacDonald-Jankowski DS, Li TK. Keratocystic odontogenic tumour in a Hong Kong community: The clinical and radiological features. Dentomaxillofacial Radiol 2010;39:167-175. 8. Apajalahti S, Hagström J, Lindqvist C and Suomalainen A. CT findings and recurrence of
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keratocystic odontogenic tumor of the mandible and maxillofacial region in a series of 46 patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;111:e39-e37.
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9. Minami M, Kaneda T, Ozawa K, yamamoto H, Itai Y, Ozawa M, Yoshikawa K and Sasaki Y. Cystic lesions of the maxillomandibular region: MR imaging distinction of odontogenic keratocysts and ameloblastomas from other cysts. AJR Am J Roentgenol 1996;166(4):943-949. 10. Hashimoto K, Arai Y, Iwai K, Araki M, Kawashima S, Terakado M. A comparison of a new limited cone beam computed tomography machine for dental use with multidetector row helical CT machine. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;95:371-377.
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ACCEPTED MANUSCRIPT 11. Fujita M, Matsuzaki H, Yanagi Y, Hara M, Katase N, Hisatomi M, Unetsubo T, Konouchi H,
Nagatsuka H and Asaumi J-I. Diagnostic value of MRI for odontogenic tumours. Dentomaxillofac Radiol 2013;42:20120265. 12. Asaumi J-i, Hisatomi M, Yanagi Y, Matsuzaki H, Choi Y K, Kawai N, Konouchi H and Kishi
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K. Assessment of ameloblastomas using MRI and dynamic contrast-enhanced MRI. Eur J radiol 2005;56:25-30.
13. Hisatomi M, Yanagi Y, Konouchi H, Matsuzaki H, Takenobu T, Unetsobu T and Asaumi J.
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Diagnostic value of dynamic contrast-enhanced MRI for unilocular cystic-type ameloblastomas with homogeneously bright signal intensity on T2-weighted or STIR MR images. Oral Oncology
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2011;47:147-152.
14. Srinivasan K, Seith Balla A, Sharma A, Roychoudhury A and Bhutia O. Diffusion-weighted imaging in the evaluation of odontogenic cysts and tumours. Brit J Radiol 2012; 85:e864-e870. 15. Konouchi H, Asaumi J-i, Yanagi Y, Hisatomi M, Kawai N, Matsuzaki H and Kishi K.
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Usefulness of contrast enhanced-MRI in the diagnosis of unicystic ameloblastoma. Oral Oncology 2006;42:481-486.
16. Sumi M, Ichikawa Y, Katayama I, Tashiro S, Nakaruma T. Diffusion-Weighted MR Imaging of
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Ameloblastomas and Keratocystic Odontogenic Tumours: Differentiation by Apparent Diffusion Coefficients of Cystic Lesions. AJNR. Am J Neuroradiol 2008;29:1897-1901.
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17. Singh A, Shaikh S, Samadi FM and Shrivastava S. Maxillary unicystic ameloblastoma: A review of the literature. Natl J Maxillofac Surg 2011;2(2):163-168. 18. Seintou A, Martinelli-Kläy CP and Lombardi T. Unicystic ameloblastoma in children: systematic review of clinicopathological features and treatment outcomes. Int J Oral and Maxillofac Surg 2014;41:405-412.
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ACCEPTED MANUSCRIPT 19. Ahmad I, Choudhary R. Wide surgical excision with split rib graft reconstruction of mandible for ameloblastoma; our 10 year experience. Indian J Otolaryngol Head Neck Surg 2013;65(1):4043.
Cancer B:oral Oncol 1995;31B:86-99.
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20. Reichart PA, Philipsen HP, Sonner S. Ameloblastoma: biological profile of 3677 cases. Eur J
21. Gardner DG. Critique of the 1995 review by Reichart et al. of the biologic profile of 3677 ameloblastomas. Oral Oncol 1999;35:443-449.
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22. Guilemany JM, Ballesteros F, Alós L, Alobid I, Prades E, Menéndez LM and Cardesa A. Plexiform ameloblastoma presenting as a sinonasal tumor. Eur Arch Otorhinolaryngol
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ACCEPTED MANUSCRIPT Figure 1. Contrast-enhanced CT shows a solid/multicystic (follicular pattern) ameloblastoma presenting as a sinonasal tumour. The tumour occupies the right maxillary sinus, nasal fossa and ethmoid air cells and reaches the cribriform plate. Heterogeneity of enhancement is evident,
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corresponding to the solid and multicystic contents of the tumour.
Figure 2. A solid/multicystic (plexiform pattern) ameloblastoma occupying the left maxillary sinus and extending into the nasal fossa. A. A cloudy sinus with remodelled and fragmented sinus wall is
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evident even in a panoramic radiograph (arrows). B and C. Contrast-enhanced CT shows a
heterogeneous enhancement pattern. The tumour appears to arise from the antral floor and alveolus,
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where there is bone destruction. D. Bony fragments are present (arrows) originating from the sinus wall.
Figure 3. A cropped panoramic radiograph (A) and axial bone window CT scan from superior to
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inferior (B-D) of the same patient showing a solid/multicystic (follicular pattern) ameloblastoma in the mandibular premolar area with a “soap bubble” appearance.
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Figure 4. A solid/multicystic ameloblastoma (follicular pattern) involving the mandibular incisor area. Native (A, B) and contrast-enhanced (C, D) CT scans demonstrating a mixed solid and cystic
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pattern of the tumour. C. Contrast-enhanced CT shows an enhancing mass in the midline representing the solid component of the tumour (arrow in C), whereas a slightly inferior contrastenhanced CT scan shows a cystic non-enhancing content (arrow in D). Bone window CT scans (E and F) show a “soap bubble” appearance.
Figure 5. A. Preoperative panoramic radiograph showing a large ameloblastoma in the right mandible causing expansion of the mandibular body, ramus and coronoid process.
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ACCEPTED MANUSCRIPT C. Contrast-enhanced CT shows an enhancing nodule in the caudal part of the tumour corresponding to the solid content (arrow in C) while the main portion of the tumour is cystic. D. On CT with bone algorithm the loculated margin is evident (arrow in D). B. Postoperative
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panoramic radiograph after mandibular resection and reconstruction with a customised prosthesis.
Figure 6. A. Native and B. contrast-enhanced axial CT scan of an ameloblastoma suggestive as being the result of neoplastic transformation of dentigerous cyst epithelium showing thick rim
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enhancement (arrow in B).
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Figure 7. (A) Panoramic radiograph of an ameloblastoma in a pericoronal relationship with an impacted and slightly displaced 3rd molar mimicking an odontogenic cyst. (B) Axial T2-weighted, (C) T1-weighted, fat suppressed and (D) T1-weighted, fat suppressed, contrast-enhanced MR images show a cystic lesion with relatively thick rim enhancement (arrow in D). (E, F and G)
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Corresponding MR images slightly caudal to levels B, C and D show an enhancing pericoronal softtissue mass (arrow in G). This was an ameloblastoma histopathologically suggestive as the result of
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neoplastic transformation of a dentigerous cyst.
Figure 8. A. Panoramic radiograph of a unicystic ameloblastoma in a pericoronal relationship with
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an impacted and slightly displaced 3rd molar mimicking a dentigerous cyst. B. Panoramic radiograph of another patient with a unilocular ameloblastoma resembling a dentigerous cyst. C. Contrast-enhanced CT of the same patient as in B. The internal low density is suggestive of a cystic lesion; however, an enhancing tiny mural nodule provides a clue to unicystic ameloblastoma.
Figure 9. A. Panoramic radiograph of a unicystic ameloblastoma involving the mandibular body. Distinct resorption of roots of associated teeth is evident (arrows in A). C. Native and D. contrast-
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enhanced CT. The content of the tumour is cystic; however, some enhancement of the septations is evident (arrow in D). Histological analysis of the surgical specimen showed a unicystic ameloblastoma without intraluminal or mural component. B. Bone window CT showing septa in the
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caudal part of the tumour.
Table 1 Clinical features and histopathological diagnosis of ameloblastomas (n=26). __________________________________________________________________________________________
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Age
Sex
Location
Maximum diameter (mm)
Histopathological diagnosis __________________________________________________________________________________________ F
mandibular incisor
12
solid/multicystic
2. 55
M
mandibular symphysispremolar
43
solid/multicystic
3. 44
F
mandibular premolar
20
solid/multicystic
4. 62
F
mandibular premolar
10
solid/multicystic
5. 34
F
mandibular body
25
solid/multicystic
6. 20
F
mandibular body
20
7. 29
F
mandibular body
27
8. 30
M
mandibular body
25
9. 73
M
mandibular body-ramus, zygoma
110
10. 67
F
mandibular angle-ramus
80
11. 58
M
maxillary sinus
33
12. 64
M
maxillary sinus, extending into the nasal fossa and ethmoid
63
13. 84
M
maxillary sinus, extending into the nasal fossa and ethmoid
55
solid/multicystic
14. 60
M
maxillary sinus
25
solid/multicystic
15. 80
M
maxillary sinus, nasal fossa
55
solid/multicystic
16. 58
M
mandibular premolar
13
peripheric (follicular)
17. 57
F
mandibular body
35
peripheric
18. 56
M
mandibular angleramus
60
neoplastic transformation of dentigerous cyst epithelium
19. 26
F
mandibular angle-ramus, third molar involved
58
neoplastic transformation of dentigerous cyst epithelium
20. 52
M
mandibular angle
25
unspecified
21. 35
F
mandibular body
65
unicystic (luminal)
22. 21
F
mandibular agle-ramus, impacted third molar involved
33
unicystic (mural)
F
mandibular body-angle-ramus
50
unicystic (intraluminal and mural)
M
mandibular angle-ramus
65
unicystic
F
mandibular body-ramus, impacted third molar involved
75
unicystic
M
mandibular angle, third molar involved
40
unicystic (mural)
24. 83 25. 23 26. 14
solid/multicystic solid/multicystic
solid/multicystic
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23. 31
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solid/multicystic solid/multicystic
solid/multicystic
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1. solid/multicystic
*
2. solid/multicystic (Fig.4)
Locularity
_______________________________________________________ non-contrast contrastboth non-contrast (attenuation) enhanced and contrast
multilocular with honeycombed pattern
content isodense to muscle
multilocular with soap-bubble appearance *
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Histopathological diagnosis (Figure number)
mixed cystic and solid
isodense
4. solid/multicystic
multilocular with honeycombed pattern
isodense
5. solid/multicystic
multilocular with honeycombed pattern
6. solid/multicystic (Fig.3)
multilocular with soap-bubble appearance
7. solid/multicystic
multilocular
8. solid/multicystic
multilocular
9. solid/multicystic
multilocular
10. solid/multicystic (Fig.5)
multilocular
11. solid/multicystic
maxillary sinus
mixed solid and cystic
12. solid/multicystic (Fig.1)
sinonasal
heterogeneous enhancement
13. solid/multicystic
sinonasal
14. solid/multicystic
maxillary sinus
mixed cystic and solid
sinonasal
heterogeneous enhancement
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mixed cystic and solid
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mixed cystic and solid
mixed cystic and solid
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15. solid/multicystic (Fig.2)
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multilocular with honeycombed pattern
3. solid/multicystic
mixed cystic and solid
mainly isodense minor hypodense areas involved mixed cystic and solid (mainly cystic)
heterogeneous enhancement
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*
intraosseal component unilocular
18. neoplastic transformation of dentigerous cyst epithelium (Fig.6) *
mixed cystic and solid
hypodense (intraosseal cystic component) isodense (peripheric component)
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17. peripheric
multilocular
unilocular
thick rim-enhancement
multilocular
hypodense
20. unspecified
unilocular
hypodense
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16. peripheric
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patients that also underwent MRI, see Table 3
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T2
solid/multicystic
homogeneous intermediate
homogeneous high
3.
solid/multicystic
homogeneous intermediate
homogeneous high heterogeneous high
15.
solid/multicystic
homogeneous intermediate
17.
peripheric
homogeneous intremediate
homogeneous intermediate
homogeneous enhancement
heterogeneous enhancement
homogeneous bright high (intraosseal cystic part) + heterogeneous (peripheric, solid component)
thick rim-enhancement (intraosseal cystic part) + heterogeneous enhancement (solid part)
homogeneous brigt high (cystic component) + homogeneous high (pericoronal solid component)
thick rim-enhancement (cystic component) + homogeneous enhancement (pericoronal solid component)
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19. neoplastic transformation of dentigerous cyst epithelium (Fig.7)
homogeneous enhancement
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1.
T1 + Gd
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T1
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Patient number and histopathological diagnosis
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Table 4. CT findings of unicystic ameloblastomas (n=6). __________________________________________________________________________________________________________________________ Locularity
TT
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Patient number and histopathological diagnosis
non-contrast attenuation value
contrast-enhanced
both non-contrast and contrast-enhanced
multilocular
22. unicystic (mural) (Fig.8a)
unilocular third molar involved
23. unicystic (intraluminal and mural)
multilocular
cystic + intraseptal enhancement
cystic + irregularly thick rim-enhancement mixed cystic and solid (mainly cystic)
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21. unicystic (luminal) (Fig.9)
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_______________________________________________________________________________________________________________________________________
multilocular
cystic (hypodense to muscle)+ thick isodense rim
25. unicystic (Fig.8b,c)
unilocular third molar involved
26. unicystic (mural)
unilocular developing third molar involved
cystic with small contrast-enhanced solid component
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24. unicystic (mural)
cystic (hypodense to muscle)
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Ameloblastomas and other cyst-like pathologies in the maxillomandibular regions display common radiologic features in conventional dentoalveolar imaging (panoramic radiograph). We have retrospectively viewed the MRI and MSCT images of 26 patients having been diagnosed with ameloblastoma in order to evaluate the differential diagnostic features of this benign but locally
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aggressive odontogenic tumour. The effective preoperative differential diagnosis may help surgeons plan treatment because ameloblastomas often require more radical treatment than odontogenic
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cysts.
