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ANTICANCER RESEARCH 32: 2173-2178 (2012)

Radiographic Findings of Odontogenic Myxomas on Conventional Radiographs

REINHARD E. FRIEDRICH1, HANNA A. SCHEUER2, ANDREAS FUHRMANN3 JOZEF ZUSTIN4 and ALEXANDRE T. ASSAF1

1Oral and Maxillofacial , 2Orthodontics, 3Oral Radiology and 4Pathology, Eppendorf University Hospital, University of Hamburg, Germany

Abstract. (OM) is a rare tumour debate (1, 2). The tumour consists of mesenchymal cells that arising in the jaws. The tumour is believed to be of are believed to be of odontogenic origin (3). A striking odontogenic origin due to the close relation to teeth. The argument in favour of odontogenic origin is the preferential radiographic appearance of OM is not specific and the location of OM in the dentoalveolar regions of the jaws (1- diagnosis is frequently unexpected following surgical removal 4). Most authors favour cells of the dental pulp or the of the lesion. The aim of this study was to analyse the periodontium as being the original tumour cell (1-3). radiographic appearance of OM on conventional radiographs. OM is rare. The relative frequency of OM in relation to This type of radiographic diagnosis is typically used by dental other odontogenic tumours varies considerably. OMs practitioners. Materials and Methods: We studied panoramic constitute 5% to more than 20% of odontogenic tumours (4-8). radiographs and plain skull radiographs of 14 patients Radiographic analysis is essential in the diagnosis of investigated over a period of 30 years (male: 3, female: 11; odontogenic tumours (1). Plain radiographs and orthopanto- age at time of diagnosis: 8 to 45 years, ≤16 years: 3). The mograms are the preferred screening modalities to identify was affected in five and the in nine patients. pathologies of hard tissues in the dentoalveolar region (1-8). In each case, all tumour findings were restricted to one jaw. Radiographic findings in cases of OM often exhibit Results: Tumour size varied considerably. The largest tumours multilocular radiolucencies of approximately spherical shape were seen in the distal parts of the mandible and ramus. (1-4). The association of a bulb-like osteolytic lesion coined Displacement of teeth was a frequent finding (8 cases), but the terms ‘honeycomb’ and ‘soap-bubble’ like radiolucency as root resorption was rare (2 cases). Honeycomb appearance on a characteristic and the predominant radiological finding in plain radiographs was associated with the size of the lesion OM (2). However, OM shares this radiographic appearance and restricted to mandibular involvement. Conclusion: The with some other types of jaw tumour and tumour-like lesions, radiographic appearance of OM of the jaws varies preferentially and keratocystic odontogenic considerably. Large lesions may exhibit characteristic tumour (9-13). Furthermore, unilocular lesions are as radiological signs of a slowly growing lesion. However, frequently found as multilocular osteolysis in OM (9), or may discrete displacement of teeth associated with a small be even the predominant feature in children (11). Recently, a osteolytic zone of the alveolar process between two teeth can classification of radiographic findings was presented based on be an OM. Careful interpretation of conventional radiographs conventional radiographs (13). The aim of this study was to is a must in identifying early lesions. add further data to the current literature, with emphasis on findings presented on conventional radiographs. Odontogenic myxoma (OM) is a benign neoplastic lesion of the jaws (1-4). The cellular origin of OM is still a matter of Materials and Methods

We studied conventional radiographs of the jaws and skull of 14 patients with histologically proven diagnosis of OM that were Correspondence to: Professor Dr. R.E. Friedrich, Oral and Cranio- generated in a single institution over a period of 30 years. All Maxillofacial Surgery, Eppendorf University Hospital, University radiographs were derived from the archive of the Department of of Hamburg, Martinistr. 52, D-20246 Hamburg, Germany. Tel: +49 Oral Radiology, University Dental Clinic, Hamburg. We evaluated 40741053259, e-mail: [email protected] conventional radiographs of the following types: panoramic, anterior-posterior and lateral cephalograms, occlusal, Water’s Key Words: Odontogenic myxoma, conventional radiographs, projection, and conventional tomograms. In one case each, a cone orthopantomography, , odontogenic tumours. beam computed tomogram or a cranial computed tomogram were

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Table I. Radiological classification of jaw lesions in odontogenic myxoma depicted on conventional radiographs (13).

1. Definition of the lesion’s border Description of radiological appearance

Well-defined Clear border of the lesion, corticated or sclerotic margin

Poorly defined Border of the lesion identifiable, but corticated margin is absent

Diffuse No margin distinguishable, indistinct transition zone between lesion and unaffected bone

2. Type of lesion Description of radiological appearance

Unilocular (Type I) Single discrete radiolucent cavity

Multilocular (Type II) Two or more compartments with multiple interlaced and interrupted osseous trabeculae

Alveolar bone involvement (Type III) Small lesion affecting the alveolar bone and showing bone resorption

Maxillary sinus involvement (Type IV) Defined by radiologically proven growth into the sinus

Osteolytic destruction (Type V) Large radiolucent area with irregular borders (‘moth-eaten’ margins), cortical erosion and rarely seen interlaced and interrupted osseous trabeculae

Combination of osteolytic Onion-like, agglomerated radiopaque features, ‘sunray’-appearence destruction and osteogenesis (Type VI)

additionally available for analysis of the lesion. The classification Table II. Distribution of odontogenic myxoma according to age and sex of radiological findings in OM proposed by Zhang et al. (13) was (N=14). applied in this study (Table I). Gender Results Age range (years) Male Female Total

The maxilla was affected in five and the mandible in nine 0-9 1 0 1 patients (35.7% vs. 64.3%). In each case, all tumour findings 10-19 0 3 3 20-29 1 2 3 were single and restricted to one jaw (males: 3, females: 11). 30-39 1 4 5 Biographic data related to diagnosis are: age at time of 40-49 0 2 2 diagnosis: 8 to 45 years, mean: 26.5 years, males: 8-36 years >50 0 0 0 (mean: 22.6 years), females: 10-45 years (mean: 27.5 years), patients younger than 10 years: 1 (7.1%), younger than 20 Total 3 11 14 years: 4 (28.5%) (Table II). Tumour size and shape varied considerably. The largest tumours were seen in the distal parts of the mandible and ramus. Displacement of teeth was a frequent finding (8 cases), but root resorption was rare (2 cases). Honeycomb or soap- Discussion bubble appearance was obviously associated with the size of the lesion and restricted to mandibular involvement. The This study confirms the large variability of OM on plain radiological classification of lesions according to Zhang et al. radiographs. A classification of OM is desirable (8-10). (13) resulted in matching the findings to more than one type of However, the radiological findings showed noteworthy lesion in almost every case (Table III). Although the overlaps between distinct radiological categories. Therefore, impressive variety of radiological findings hampered a distinct a typing of radiological features in OM appears to be of allocation of findings to a single type of lesion, the lesions limited value when only plain radiographs of the jaws are shared some findings that are represented in the numerical available for analysis. On the other hand, the numerical code of the classification. The results are summarized in coding of radiological findings may be of value in Tables II and III and illustrated in Figures 1 and 2. epidemiological studies.

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Table III. Radiological findings in odontogenic myxomas. Typing of lesions according to Zhang et al. (13).

Case Gender Age Osseous lesion Teeth (years) Jaw Topography/extension Classified appearance (type) Borders Root Root displacement resorption

1 M 8 Mandible 85 to mid-ramus Multilocular (soap bubble-like), (II, III) Well + – 2 F 45 Mandible Tooth 35 to mid-ramus Multilocular (soap bubble-like) (II, III) Poor – – 3 F 22 Mandible Teeth 33-37 (from alveolar Multilocular (II, III) Well + + limbus to the basal cortex) 4 F 25 Mandible Teeth 32-33 (alveolar process) Unilocular (I, III) Well + – 5 M 24 Maxilla Left tuber Tuber (IV) Poor – – 6 F 34 Maxilla Teeth 23-25 (alveolar process) Unilocular (I, III) Poor – – 7 F 35 Mandible Teeth 32-33 (alveolar process) Unilocular (I) Well + – 8 F 43 Maxilla Teeth 11-13 (periapical lesion) Unilocular (I, III) Well + – 9 F 30 Mandible Teeth 45-46 (alveolar process) Unilocular (I, III) Poor + + 10 F 17 Mandible Tooth 36 – mid ramus Multilocular (soap bubble-like) (II) Well – – 11 M 36 Mandible Toothless region 46-47 (large Unilocular (I) Well – – osteolysis extending to basal cortex) 12 F 36 Maxilla Tooth 28 (Osteolytic Tuber Region) Unilocular, irregular borders (I, III) Poor – – 13 F 10 Maxilla Teeth 21-26, (displaced canine inside Unilocular (with septa on the maxillary sinus) computed tomogram) (I, IV, VI) Poor + – 14 F 16 Mandible Teeth 32-33 (alveolar process) Unilocular (I, III) Well + –

Although rarely diagnosed, knowledge about OM is reported to be diagnosed in the majority of cases (1). In this essential in dental and medical education about lesions of the series, multilocular lesions demonstrating this impressive jaws. OM is the fourth most frequent type of odontogenic radiological feature were rare (n=3, 21.4%). On the other tumour, being surpassed by keratocystic odontogenic tumour, hand, Kaffe et al. (16) noted 55% of OM with multinucleated (), and ameloblastoma only (2). OM lesions. The soap bubble-like lesions often appear to be can develop in any period of life, but is particularly noted in sharply demarcated from the unaffected residual bone. the second to fourth decade. The mean age at the time of However, clinical experience with OM has clearly revealed diagnosis is about 30 years of age, with a slight preference the invasive growth properties of this entity, reflected in the for women (1, 2, 4). 78.5% our patients were female. relative high number of local recurrences of tumour following Occasionally OM is diagnosed in very young children (11, curetting as the treatment strategy, of up to 25% (4). The 14) and in patients in their seventh decade of life (13). In the interrelationship of OM with retained teeth may result in present small series, patients younger than 20 years radiographs that allow no distinction between OM and other accounted for 28.5% of all patients (<16 years: 3; 21.4%). odontogenic lesions (17, 18). This percentage is higher in our study than in the study of A recent review pointed to differences of the radiological Keszler et al. (11), who found 31 cases in their literature patterns of OM in relation to the location of the lesion. review (n=367, 8.4%) and added 10 new cases (12.5% of all Unilocular lesions were predominantly diagnosed in the their 80 myxomas diagnosed). A recent review on published anterior and multilocular lesions in the posterior regions of the case series showed that 66.4% of OM arose in the mandible jaws (9). This approximate distinction can be applied in some (maxilla 33.6%) (1). This distribution of OM was also found cases but cannot be taken as a general rule. It is likely that the in the present study (64.3%). preference for multilocular lesions in the posterior regions of As shown, the radiographic appearance of OM of the jaws the jaws is reducible to the space these regions provide prior to varies considerably (15). Small lesions are not distinguishable clinical attention. This assumption is supported by the analysis from a large variety of jaw lesions, e.g. granuloma, or of Kaffe et al. (16), who demonstrated unilocular lesions other odontogenic lesions (Figure 1B and 2A-C). Large predominantly in lesions smaller than 4 cm. The preference of lesions may exhibit characteristic radiological signs of a soap bubble-like lesions in the distal parts of the mandible on slowly growing lesion, e.g. expansile lesions with linear plain radiographs is possibly a tribute to the preferred imaging radiopaque margins (Figures 1 and 2D). These extensive technique, orthopantomography. Other sectional imaging intraosseous lesions can appear solely or provide the aspect techniques, e.g. cone beam tomography (19) and computed of converging and overlapping roundish osteolytic tumours. tomography (20, 21), provide images of the maxilla that also The honeycomb- or soap bubble-like appearance of OM was show soap bubble-like lesions similar to those typically found

2175 ANTICANCER RESEARCH 32: 2173-2178 (2012)

Figure 1. A: Large odontogenic myxoma (OM) of the right mandibular corpus and ramus associated with a retained and incompletely developed molar in an 8-year-old patient. The tumour shows expansive growth and irregular linear, comma-shaped or soap bubble-like radiopacities projecting inside the lesion. B: Detail of orthopantogram depicting the right anterior maxilla of a 43-year-old patient. The OM of unilocular type in the anterior maxilla appears sharply demarcated only in those parts that are projected on the tooth roots, alveolar process and the nasal aperture, but not towards the distal and cranial regions beyond the apices of tooth 14. Notice root divergences between tooth 13 and 14. Small septa appear to originate from the cranial margin of the lesion and are reaching into the osteolytic zone. C: Detail of panoramic radiograph of the jaws: extensive OM of the maxilla masking as a developmental of the retained right upper canine (10-year-old patient). This radiological appearance on panoramic radiograph is indistinguishable from other tumours or tumour-like lesions of the jaw, with a preference for canine retention, e.g. adenomatoid odontogenic tumour (17).

Figure 2. A: Odontogenic myxoma (OM) of the mandible. The root of the second premolar is incompletely developed. The incomplete apex with the pulp walls running parallel to each other is located at the caudal portion of the osteolytic lesions and appears to be kinked. The periodontal ligaments of the roots of both teeth neighbouring the lesion have been lost. B: OM of the mandible on cone beam computed tomogram. Roots of teeth 32 and 33 are displaced. The cone beam tomogram shows an almost empty lesion. Note the poor quality of visualization concerning radiographic anatomy of teeth, the filling material of tooth 33 and the periodontal space of the artificially deformed lateral incisor. The ovally shaped cavity appears to be covered by a thin osseous layer at the level of the alveolar limbus. C: Detail of conventional panoramic radiograph (orthopantogram) of the same lesion that shows the superimposition of the vertebral column on the right part of the lesion. The lesion appears to be inhomogeneously structured but interpretation of the lesion’s radiolucency is difficult due to superimposition of the vertebral column on the medial part of the cavity. D: Detail of computed tomogram of patient depicted in 1C. Expansive osseous lesion of the maxilla is depicted, with septa originating from the cortical borders of the lesion.

in the mandible (Figure 2D). However, advanced sectional (20). On the other hand, it has to be emphasized that so-called imaging may occasionally show deformed structures in the honey comb-like appearances on any type of radiographic region of interest that do not provide superior imaging of the image may also suggest lesions other than OM, including lesion compared to conventional radiographs (Figure 2 B and ameloblastoma and keratocystic odontogenic tumour (10). C). Computed tomography showed more aspects of OM than This differential diagnosis of large lesions needs to be were distinguishable on conventional radiographs (20, 21). discussed when magnetic resonance imaging is applied in OM Computed tomography was recommended as a diagnostic tool (22). It is noteworthy to refer to the large number of clinics to resolve discrepancies derived from ambiguous that had to contribute to a computed tomography series of OM interpretations of OM-associated lesions of conventional in order to establish a patient collective sufficient for analysis radiographs, in particular to distinguish between uni- and (20) supporting the view that conventional radiographs are still multilocular lesions and the diagnosis of intralesional septa the main diagnostic tool in imaging of the jaws.

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Displacement of teeth associated with a small osteolytic 9 Peltola J, Magnusson B, Happonen RP and Borrman H: zone of the alveolar process between two teeth can be an Odontogenic myxoma – a radiographic study of 21 tumours. Br indicator of a (small) OM (Figure 1B). Displacement of teeth J Oral Maxillofac Surg 32: 298-302, 1994. 10 MacDonald-Jankowski DS, Yeung R, Lee KM and Li TK: was registered in 74% of cases in a large study (16), but root Odontogenic myxomas in the Hong Kong Chinese: clinico- resorption was less frequent (9.5%). In our study, root radiological presentation and systematic review. Dentomaxillofac displacement was seen in more than every second patient Radiol 31: 71-83, 2002. (57%) and root resorption was rare (2 cases, 14%). Careful 11 Keszler A, Dominguez FV and Giannunzio G: Myxoma in interpretation of conventional radiographs is a must in childhood: an analysis of 10 cases. J Oral Maxillofac Surg 53: identifying early lesions. 518-521, 1995. Association of OM with retained teeth may occasionally 12 Chuchurru JA, Luberti R, Cornicelli JC and Dominguez FV: Myxoma of the mandible with unusual radiographic appearance. be found (Figure 1C) but is non-specific (17, 18). On the J Oral Maxillofac Surg 43: 987-990, 1985. other hand, the non-eruption of teeth should be an indication 13 Zhang J, Wang H, He X, Niu Y and Li X: Radiographic to perform a radiographic survey of the dentition in order examination of 41 cases of odontogenic myxomas on the basis diagnose odontogenic or osseous pathologies and to decide of conventional radiographs. Dentomaxillofac Radiol 36: 160- treatment. Orthopantomograms are the preferred radiological 167, 2007. technique to provide this overview. 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GT, Bamgbose BO and Akinwande JA: Odontogenic tumors: a 22 Hisatomi M, Asaumi J, Konouchi H, Yanagi Y, Matsuzaki H and review of 319 cases in a Nigerian teaching hospital. Oral Surg Kishi K: Comparison of radiographic and MRI features of a Oral Med Oral Pathol Oral Radiol Endod 99: 191-195, 2005. root-diverging odontogenic myxoma, with discussion of the 7 Noffke CE, Raubenheimer EJ, Chabikuli NJ and Bouckaert MM: differential diagnosis of lesions likely to move roots. Oral Dis Odontogenic myxoma: review of the literature and report of 30 9: 152-157, 2003. cases from South Africa. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 104: 101-109, 2007. 8 Jing W, Xuan M, Lin Y, Wu L, Liu L, Zheng X, Tang W, Qiao J and Tian W: Odontogenic tumours: a retrospective study of 1642 Received April 9, 2012 cases in a Chinese population. Int J Oral Maxillofac Surg 36: 20- Revised April 27, 2012 25, 2007. Accepted April 27, 2012

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