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Odontogenic myxoma: review of the literature and report of 30 cases from South Africa
Vol. 104 No. 1 July 2007
ORAL AND MAXILLOFACIAL RADIOLOGY
Editor: Allan G. Farman
Odontogenic myxoma: review of the literature and report of 30 cases from South Africa Claudia E. E. Noffke, BChD, MScOdont,a Erich J. Raubenheimer, MChD, FCPath(SA), PhD, DSc,b Ntombizonke J. Chabikuli, BDS, MDS,c and Michael M. R. Bouckaert, BChD, MDent,d Limpopo, South Africa UNIVERSITY OF LIMPOPO, MEDUNSA CAMPUS
Objective. The purpose of the study was to analyze the clinical and radiographic features of central odontogenic myxomas (OM) of the jaws diagnosed over 23 years in a black South African patient sample. Study design. Records of 30 cases of OMs with radiographs of diagnostic quality were retrieved from 52 cases of histopathologically verified OMs from the archives of the Oral Health Center at the University of Limpopo, South Africa. The age, sex, size, location, and radiographic features were compared with the literature. Results. The study consisted of 21 females and 9 males. The correlation between age and size of the tumor was found to be statistically significant (P ⫽ .004). Septa were shown to be either reorientated cortical bone or sheets of dense fibrous connective tissue. Indistinct borders mimicked malignancy. The most common radiographic feature was the tennis-racket appearance. Conclusions. Variations in radiographic presentation make a radiological differential interpretation of OM challenging because the radiographic features overlap with those of other benign and malignant neoplasms. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:101-9)
Odontogenic myxoma of the jaw was first described by Thoma and Goldman in 1947.1 In the international histological classification of odontogenic tumors, odontogenic myxoma (OM) is defined as a benign odontogenic tumor of mesenchymal origin that is locally invasive and consists of rounded and angular cells that lie in abundant mucoid stroma.2 The origin of OM is believed to be odontogenic ectomesenchyme of a developing tooth or undifferentiated mesenchymal cells in the periodontal ligament.3-5 The odontogenic origin a
Head, Division of Maxillofacial and Oral Radiology, Oral Health Center, University of Limpopo, Medunsa Campus. b Head, Department of Oral Pathology, Oral Health Center, University of Limpopo, Medunsa Campus. c Senior Lecturer, Division of Maxillofacial and Oral Radiology, Oral Health Center, University of Limpopo, Medunsa Campus. d Head, Department of Maxillofacial and Oral Surgery, Oral Health Center, University of Limpopo, Medunsa Campus. Received for publication Nov 27, 2006; returned for revision Jan 21, 2007; accepted for publication Jan 23, 2007. 1079-2104/$ - see front matter © 2007 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2007.01.026
of the neoplasm is supported by its histological similarity to pulpal ectomesenchyme, its exclusive occurrence in close proximity to the tooth-bearing parts of the jaws, occasional association with missing or unerupted teeth, presence of inactive odontogenic epithelium in a minority of cases, and its rare occurrence in other parts of the skeleton.2,5 In Asia, Europe, and America, frequencies for odontogenic myxoma between 0.5% and 17.7% of odontogenic tumors have been reported.6,7 Odontogenic myxomas in Africa perhaps occur slightly more commonly, with relative frequencies reported between 1% and 19%.8-12 In a Nigerian teaching hospital, OM occurs as the second most frequent benign tumor of the jaws after ameloblastoma.13 Odontogenic myxoma frequently displays aggressive infiltration of the adjacent tissue as well as a tendency to recur after surgical removal.14-19 In order to manage these tumors appropriately, it is imperative to determine their extent. The purpose of this study was to record cases of OM diagnosed in a black South African patient sample retrospectively and to compare the data with the literature. 101
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Table I. Demographic data of series larger than 10 cases reported after 1980 Author Mlosek et al. (1982)22 Adekeye et al. (1984)9 Slootweg and Wittkampf (1986)23 Abiose et al. (1987)10 Happonen et al. (1988)24 Günhan et al. (1990)25 De Labrouhe et al. (1993)26 Peltola et al. (1994)18 Odukoya (1995)27 Lo Muzio et al. (1996)28 Arotiba et al. (1997)8 Mosqueda-Taylor et al. (1997)29 Stypulkowska (1998)30 Lu et al. (1998)31 Sassi et al. (2001)32 MacDonald-Jankowski et al. (2002)19 Simon et al. (2004)12 Ladeinde et al. (2005)13 Present study 2006
No. of cases
Populations studied
Mean age
Gender M:F
Site max:mand
11 18 15 10 13 51 27 21 34 10 21 60 12 64 17 10 33 21 30
Poland Nigeria Netherlands Nigeria Finland Turkey France Scandinavia Nigeria Italy Nigeria Mexico Poland China Brazil Hong Kong Tanzania Nigeria South Africa
NA 27.8 26 25 33 32.3 36.1 35.1 24 32.7 33 NA 31.5 19.6 32 36.9 26.1 26.9 31.3
1:0.83 1:2.6 1:4 1:4 1:0.86 1:2.9 1:1.45 1:2 1:1.83 1:2.3 1:1.6 1:2 1:0.7 1:1 1:0.55 1:1.5 1:1.83 1:1 1:2.3
1:1.75 1:1.6 1:2.75 1:1.5 1:2.25 1:0.55 1:3.5 1:4.25 1:3.3 1:1.5 1:0.9 1:0.82 1:3 1:1.06 1:0.4 1:1.5 1:3 1:4.1 1:1.7
Max, maxilla; mand, mandible; NA, not available.
Although some authors report symptoms like pain and paresthesia,3,12,19 OM is generally depicted as slowgrowing tumor with the potential to attain considerable size without noticeable signs and symptoms.20,21 A summary of the demographics of large series recently reported is reflected in Table I.22-32 Children and persons more than 50 years of age are rarely affected.12,33 Several papers report OMs in patients under 10 years of age,34-38 with the youngest recorded case in a baby of 3 months.12 The molar and ramus regions of the mandible are most frequently involved,12,18,20 whereas the premolar–first molar region is the site of predilection in the maxilla.20 Regezi and Sciubba39 (1993) reported an equal distribution in anterior and posterior regions of the maxilla. Odontogenic myxomas in other sites of the jaws have rarely been recorded.12,18,40 In 5000 bone tumors affecting the skeleton studied by McClure and Dahlin41 (1977), only 3 cases of extragnathic myxomas were identified. The borders of multilocular OMs are described as well-defined corticated, well-defined noncorticated, poorly defined, or diffuse.33,40 Odontogenic myxomas can be extensive, involving half of the maxilla or mandible including the ramus and the condyle.18,19,40 The cortex appears thinned due to expansion and may perforate at a later stage of tumor progression. The maxillary sinus is often filled with tumor mass that can lead to exophtalmos.42 Some authors reported cases with unusual peripheral cortical reactions16,18,43,44 mimicking osteogenic malignant lesions. These were described either as radiopaque lines with vertical orientation to the mandible that extended from the periosteum into the
soft tissue, resembling a sunburst effect, or as a destructive lesion exhibiting a peripheral sunray appearance.43 Odontogenic myxoma is depicted in tooth-bearing areas as scalloping between the roots of the teeth.18 The internal structure of OM is described as either a unilocular or an expansile-multilocular radiolucency.18,40 Some authors described multilocular lesions with fine and/or rough trabeculations and applied terms like “tennis racket,” “soap bubble,” or “honeycomb” to depict the internal structure.16,18,19,33 The earliest description of the tennis racket appearance was given when Worth45 compared the locules of the OM with the angular, square, rectangular, or triangular spaces of a tennis racket. This description was accepted by subsequent authors.15,33,46 Farman et al.20 described cases of expansion of OM into the maxillary sinus, resulting in a radiopaque appearance of the sinus. Unusual multilocular lesions with diffuse calcifications in their internal structure have been reported.3,16,40,42,43,47 Although Kaffe et al.40 (1997) found radiological evidence of calcifications in 12.5% of 164 OMs published up to 1997, the microscopic nature of the septa and calcifications within OMs have not been studied in detail. One case was reported that presented like a pericoronal unilocular cystlike radiolucency and resembled a follicular cyst.46 Displacement of teeth is relatively common, though root resorption is less frequently seen.3,18,21 It was reported that involved teeth could be mobile but are usually vital.15,19 The differential diagnosis of OM includes other multilocular lesions like ameloblastoma, central giant cell granuloma, central
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hemangioma, aneurysmal bone cyst, and metastatic lesions to the jaws.18,21,33
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Table II. Distribution by age and gender of 30 odontogenic myxomas Age group (y)
METHODS Records with radiographs of 30 cases of OM were selected from 52 histopathologically verified OMs diagnosed at the Medunsa Oral Health Center of the University of Limpopo, South Africa during the period 1982 to 2005. The Oral Health Center serves mainly a rural and peri-urban African population sample, and consequently all patients were black. Clinical criteria for case acceptance included the presence of a medical and dental history and at least 1 conventional panoramic radiograph of acceptable diagnostic quality for evaluation. Twenty-two cases included extraosseous (peripheral) OM and were excluded from this study. Features of 30 OMs were recorded according to the clinical and radiological criteria suggested by White48 in the ORAD (Oral Radiographic Diagnosis) computeraided diagnostic system. Two previously calibrated investigators with postgraduate training in dental radiology evaluated the radiographs. The images were viewed on a Rinn (Dentsply; Rinn Corp., Elgin, IL) light box. The data were kept anonymous to protect the confidentiality of the patients. The lesions were measured in millimeters on panoramic radiographs—along the longest axis of the tumor—and tabulated. This measurement was selected because it represented the maximal extent of tumor growth. To establish the location of a lesion, the maxilla was divided into 6 anatomical regions, 3 on either side: (1) the anterior region from the midline to the distal surface of the canine, (2) the premolar region from the mesial aspect of the first premolar to the distal side of the second premolar, and (3) the molar region from the mesial aspect of the first molar to the distal surface of the maxillary tuberosity. Each half of the mandible was divided into 4 anatomical regions: (1) the anterior region from the midline to the distal surface of the canine, (2) the premolar region from the mesial aspect of the first premolar to the distal side of the second premolar, (3) the molar region from the mesial surface of the first molar to the beginning of the ascending ramus, and (4) the ramus region from the beginning of the ascending ramus to the sigmoid notch. According to the criteria for the degree of definition of the boundary of a lesion, it was considered to be well defined when its radiodensity changed markedly within a distance of 1 mm when passing from the lesion to the surrounding bone49 and when an imaginary pencil could trace most of the limits of the lesion confidently.50 A lesion was considered corticated when a thin, fairly uniform radiopaque line of reactive bone could be depicted at the periphery of most of the lesion and noncorticated when this line was
10-20 21-30 31-40 41-50 ⬎50 Age range Mean age Total
Male
Female
Total
2 2 3 1 1 11-63 33.1 9 (30%)
5 9 4 1 2 12-70 30.5 21 (70%)
7 (23%) 11 (37%) 7 (23%) 2 (7%) 3 (10%) 11-70 31.3 30 (100%)
Table III. Location of 30 odontogenic myxomas Area Anterior mandible (crossing midline) Premolar and molar area Molar and ramus area Lesions that cross the midline from posterior to posterior area Total
Mandible
Maxilla
Total
1 6 7 5
NA 11 NA —
1 17 7 5
19
11
30
NA, not available.
absent. A lesion was considered poorly defined when it was difficult to outline its periphery and diffuse when the transitional zone between the lesion and the unaffected bone was wide and indistinct. Statistical analysis The internal structure indicated the degree of calcification, locularity, and if present, type of septa. A lesion was considered calcified when radiopaque areas appeared within an otherwise radiolucent lesion.40,50 The presence of locules was indicative of septa. If these divided the radiolucent internal structure into at least 2 compartments, the term multilocular was used. A unilocular lesion represented a single radiolucent lesion that could include internal calcifications but no compartments. The radiographic patterns created by the septa were ascribed to widely used descriptive terms: soap bubble represented large spaces surrounded by round or curved bony septa, tennis racket was represented by crossed straight septa resembling the strings of a tennis racket, honeycomb presented small angular spaces resembling a bee’s honeycomb, and a “ground glass” appearance described the visual effect of many fine, poorly calcified trabeculations being superimposed on each other and arranged in a disorganized fashion.51 The influence of the lesions on the adjacent structures such as the teeth and cortical borders was recorded and tabulated. Microscopic sections were reviewed with the purpose of providing more insight into the nature of the septa. Statistical analysis included the calculation of de-
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Table IV. Relationship between the size of 30 odontogenic myxomas, their location, and locularity Location Size range (mm) 10-20 21-30 31-40 41-50 51-60 61-70 71-80 ⬎80
Unilocular
Multilocular
Maxilla
Mandible
Maxilla
Mandible
Maxilla
Mandible
0 0 0 2 6 2 1 0 11
1 2 1 4 1 3 3 4 19
0 0 0 0 2 0 0 0 2
0 2 1 1 0 0 0 0 4
0 0 0 2 4 2 1 0 9
1 0 0 3 1 3 3 4 15
Total Total size range Mean size Median size
30
6 30-55 42.5 42.5
24 15-130 70.7 66.5
Table V. Radiographic appearance of 30 odontogenic myxomas Mandible Maxilla Borders Well defined and corticated Well defined and noncorticated Poorly defined Poorly defined with invasive pattern Diffuse Perforation of mandibular cortex Expansion of mandible Invasion of the sinus only Invasion of the sinus and the nose cavity Internal structure Unilocular Multilocular Soap bubble appearance Tennis racket appearance Honeycomb appearance Ground glass appearance Calcifications Effect on adjacent teeth Impactions Extrusion and mobile teeth Widened periodontal ligament Tooth displacement Root resorption Scalloping between teeth Cases associated with missing teeth
Total
7 4 7 1
0 0 1 1
7 (23%) 4 (13%) 8 (26%) 2 (7%)
0 7 18
7
9 2
7 (23%) 7 (23%) 18 (95%) 9 (82%) 2 (18%)
4 15 5 7 3 0 6
2 9 2 6 1 2 3
6 (20%) 24 (80%) 7 (23%) 13 (43%) 4 (13%) 2 (7%) 9 (30%)
1 8 2 15 10 2 2
2 1 0 7 3 0 1
3 (10%) 9 (30%) 2 (7%) 22 (73%) 13 (43%) 2 (7%) 3 (10%)
scriptive statistics and comparisons of mean values by the t test and median values by the nonparametric Wilcoxon test. A regression analysis was conducted, with size of the tumor as dependent variable and age, sex, location, internal structure, tooth displacement, root resorption, and borders as independent predictor variables. Correlation coefficients were calculated as appropriate.
Fig. 1. Soap bubble appearance of an odontogenic myxoma (OM) in the mandible. Note the large, smooth, curved septa in the tumor.
RESULTS Five hundred seventy-one odontogenic tumors (excluding keratocystic odontogenic tumors that were recently included in the World Health Organization classification of odontogenic tumors)52 were diagnosed over a 23-year period, of which 52 cases (9.1%) were OM. The distribution according to age and sex of the 30 cases of the sample is given in Table II, and the location of the lesions is noted in Table III. The relationship between the size, location, and locularity of the lesions is reflected in Table IV. The size range for unilocular lesions varied from 30 to 55 mm (mean, 42.5 mm), whereas the size range for multilocular lesions varied from 15 to 130 mm (mean, 70.7 mm). The mean size of unilocular lesions was significantly less than that of multilocular lesions (t test; P ⫽ .026). The median size of unilocular lesions was also significantly less than the
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Fig. 2. Tennis racket appearance of a maxillary OM showing angular intersections of septa.
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Fig. 4. Ground glass appearance of a maxillary OM resembling a fibro-osseous lesion.
Two cases in the maxilla presented with a ground glass appearance (Fig. 4). Comparison between the microscopic slides of archived tissue and the radiographic images showed trabeculations to consist of 2 tissue types: the radiopaque septa, most frequently located at the peripheral aspects of the OMs, were composed of lamellar bone (Fig. 5, A). The delicate septa toward the center of the neoplasms consisted of broad fibrous connective tissue bands (Fig. 5, B). The latter divided the tumor in myxoid lobules. Fig. 3. Honeycomb appearance of a maxillary OM. Note the small adjacent spaces resembling a honeycomb.
median size of multilocular lesions (Wilcoxon test, P ⫽ .008). From a regression analysis conducted on the data with the size of the tumor as a dependent variable, the only predictor variable found to be statistically significant was the age of the patient (P ⫽ .0143). The overall correlation between age and size of the tumor was found to be r ⫽ 0.508 which is statistically significant (P ⫽ .004). In the case of males only, the correlation between age and size of the tumor was found to be r ⫽ 0.133, which is not statistically significant (P ⫽ .732). The correlation between age and size of the tumor for females was found to be r ⫽ 0.665, which is statistically highly significant (P ⫽ .001). A summary of the radiographic features of OM is provided in Table V. The trabeculation of the multilocular lesions showed either soap bubble (Fig. 1), tennis racket (Fig. 2), or honeycomb (Fig. 3) appearances.
DISCUSSION The odontogenic myxoma is generally considered to be a rare neoplasm unique to the jaws, and only a few series with significant numbers of patients have been published (Table I). This series of 52 cases is 9.1% of 571 odontogenic tumors diagnosed over a period of 23 years. The current study supports the finding of Ladeinde et al.13 (2005) and others that OMs do not occur infrequently in African hospital series.8-13 In our archives, they occur more frequently than odontomas (6.5% of our sample). It should be kept in mind, however, that odontomas are usually symptom free and are detected incidentally on radiographs. A speculative number may therefore go unnoticed in all studies of this nature. The study showed a wide age range (11-70 years) and supported previous observations that an OM can occur at any age from childhood to the elderly.15,21,22 It occurred most frequently in the fourth decade in our sample, with a mean age of 31.3 years. These results comply with most reports in the literature as documented in Table I. It is generally accepted that OM is
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Fig. 5. Microscopic appearances of septa in OMs. A, Bony septa (arrow) at the periphery of the case shown in Fig. 1 (hematoxylin-eosin, original magnification ⫻ 80). B, Delicate fibrous connective tissue septa (arrows) of the case shown in Fig. 3 (hematoxylin-eosin, original magnification ⫻50).
rare before 10 years of age and above 50 years of age.12 However, it was stated that the frequency of OM in childhood might be higher than that of other aggressive odontogenic tumors.36 In a study of 80 cases of OM, an incidence of 12.5% in children between the ages of 5 and 16 years (mean age of 11.6 years) was reported.36 In this series, no cases were found in the first decade. This may be due to the tendency of our patients to seek medical care at a late stage. To our knowledge, no correlation between the age of the patient and the size of the tumor has been reported. The present study showed that the correlation between these 2 variables was statistically significant (P ⫽ .001), particularly in the case of females. The male to female ratio in our sample was 1:2.3, and the higher tendency for females was seen in all age groups. This was in agreement with findings of investigators in the rest of the African continent and in other countries (Table I). Equal distri-
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bution among the sexes was noted in China.31 Odontogenic myxoma has been reported by most authors to occur more frequently in the mandible than in the maxilla (Table I), corresponding with the ratio of 1.7:1 in this study. However, Regezi et al.6 (1978) reported an equal distribution in the mandible and the maxilla. In the current study, only 1 lesion was found exclusively in the anterior area of the mandible, whereas 29 lesions were in the posterior areas of both jaws (Table III). This finding correlates with most other reports.19,33,40 Six mandibular lesions crossed the midline. This is probably size related in the mandible and is in contrast with Simon et al.12 (2004), who noted midline crossing to be rare. In the maxilla, the OMs did not cross the median palatal suture, a finding confirmed by the literature. This study presented with 11 well-defined cases in the mandible, 7 of these being corticated and 4 noncorticated. Seven maxillary cases presented with diffuse borders. Eight cases—7 of them located in the mandible and 1 in the maxilla—presented with poorly defined borders, whereas 2 OMs, 1 in each jaw, showed poorly defined borders with invasive patterns. These features together with perforation of the inferior cortical mandibular border in 7 cases resembled malignancy, bringing this into consideration in the differential diagnosis of OM. However, sarcomatous changes in OM are reported to be rare and were described in only 2 cases that resulted in death.22 Nine of the 11 maxillary lesions (82%) showed encroachment on the maxillary sinus only, and 2 lesions affected the maxillary sinus as well as the nasal cavity. This finding is supported in the literature, where it is reported that maxillary lesions encroach upon the maxillary sinus; however, lesions infiltrating the nasal cavity are rare.19 Two mandibular lesions showed scalloping between the teeth, a finding that correlates with the literature.41 Tooth displacement is commonly reported; however, root resorption appears to be rare.18,21,39 In this study, 22 lesions displaced teeth, confirming the frequent occurrence as well as indicating a slow tumor growth rate. Although consensus is that OM grows slowly, there are scattered reports of rapid enlargement.44 The cell-proliferating index of OM was found to be low, and it was therefore suggested that the invasive nature and high tendency of OM to recur was more likely to be the result of tumor spillage in the operating field due to the gelatinous consistency and the poorly defined borders, which present in nearly half of all OMs investigated.33,53 Thirteen cases presented with root resorption, which is relatively high compared with findings in the literature. Kaffe et al.40 (1997) found both features relatively uncommon, with tooth displacement noticed in 26% of cases and root resorption in 9.5% of cases studied. Although no longer generally accepted, it was believed
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that malignancy could not be excluded in the case of neoplasms with indistinct borders and root resorption.3 The more frequent occurrence of root resorption in this study may be due to the larger size and subsequent pressure of OMs when compared with those reported in the literature. All 9 neoplasms manifesting with tooth extrusion showed excessive mobility of associated teeth. Most of these were large lesions that occurred in the mandible. The lack of tooth extrusion in most of the maxillary OMs is probably the result of growth into the maxillary sinus, unlike mandibular OMs that expand into the alveolus.20 Most OMs are reported to be multilocular with coarse or angular trabeculations,20 yet other studies show an equal distribution between unilocularity and multilocularity.18,24 It was reported that the size of the lesions correlated with their locularity.18,40 Multilocular lesions reached sizes larger than 40 mm, thereby exceeding unilocular lesions in the greatest dimension. These findings correspond with the current study. Seven of the 24 multilocular OMs in this study could be described as a soap bubble pattern, referring to multiple round or oval compartments formed by curved bony septa. Thirteen were characterized by square or triangular compartments formed by straight trabeculations and were appropriately described as tennis racket pattern. The honeycomb pattern was exhibited by 4 cases that were characterized by small, round, or angular spaces. Microscopic examination showed that the coarse welldefined peripheral septa were reorientated residual lamellar cortical bone. However, most of the delicate internal septa were found to be dense fibrous partitions that divided the OM in myxomatous lobules. Two cases in the maxilla resembled fibrous dysplasia and were described as having a ground glass appearance. Supporting the opinion of Kaffe et al.,40 it is believed that this pattern is due to the neoplasm projecting into the otherwise radiolucent maxillary sinus, thereby manifesting with increased radiodensity. Some OMs, however, showed a mixed radiopaque-radiolucent appearance,12,33,40 which was ascribed to the presence of foci of calcification.3,40,47 It was suggested that this appearance may be due to residual bone and not to new bone formation, and therefore it was proposed that OM should be considered in the differential diagnosis of mixed radiolucent-radiopaque lesions.40 Although most OMs in this study were entirely radiolucent, 9 patients presented with radiopacities in the lesions. The differential diagnosis of multilocular OMs should include ameloblastoma, intraosseous hemangioma, aneurysmal bone cyst, central giant cell granuloma, cherubism metastatic neoplasms to the jaws,18 glandular odontogenic cyst,55 and the odontogenic keratocyst, especially the multilocular type. Giant cell
Noffke et al. 107
granulomas affect the anterior region of the jaws more frequently than the posterior, giant cell lesions of hyperparathyroidism can be eliminated if the serum chemistry is normal, cherubism is a hereditary condition characterized by bilateral facial swelling during early childhood, aneurysmal bone cysts present with pain and tenderness as opposed to most OM, and intrabony hemangiomas can be ruled out after a nonproductive aspiration.18 In older patients, the possibility of a malignancy should not be ruled out because radiographic features resembling osteosarcoma have been reported.16,18,44 Some cases in our series presented with extruded teeth and widened periodontal ligament spaces, mimicking an osteogenic malignancy. The glandular odontogenic cyst is reported to occur most frequently in the globulomaxillary region, which is not the location of preference for OM. The lack of modern imaging modalities in this study is the result of its retrospective nature. Literature indicates that computed tomography (CT) and magnetic resonance imaging have been found to be superior to plain radiographs when establishing the intraosseous extent of the tumor, cortical perforation and soft tissue involvement, and extent.15,21,33,55,56 Tooth displacement and root resorption, however, can be observed more reliably on conventional radiographs.55 Computed tomographic imaging shows most bony septa to be located at the periphery of an OM.55-57 This characteristic feature was demonstrated in our study by the use of histological examination. It was reported, however, that even with CT examination, several OMs could not be distinguished from other lesions.57 Magnetic resonance imaging is indicated in cases of suspected recurrent OM, because this modality facilitates the differentiation between fibrous connective tissue and tumor tissue due to different signal intensities.21 CONCLUSIONS Variations in radiographic presentation make radiological differential interpretation of OM challenging, as the radiographic features overlap with those of other benign and malignant neoplasms. A biopsy is therefore mandatory in establishing a final diagnosis. Correlation between tumor size and age of patients was significant, and septa seen on radiographs represented either reorientated residual bone or dense fibrous connective tissue partitions. The authors wish to thank Professor H. S. Schoeman for statistical analyses, Professor C. J. Nortje for editorial advice, and C. S. Begemann for typographical assistance. REFERENCES 1. Thoma KH, Goldman HM. Central myxoma of the jaw. Am J Oral Surg Orthod 1947;33:532.
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2. Kramer IRH, Pindborg JJ, Shear M. Histological typing of odontogenic tumours. 2nd ed. Berlin: Springer Verlag; 1992. p. 23. 3. Kangur TT, Dahlin DC, Trulington EG. Myxomatous tumours of the jaws. J Oral Surg 1975;33:523-8. 4. McLoughlin PM. Odontogenic myxoma: an orthodontic presentation. Br Dent J 1991;171-212. 5. Van der Waal I. Diseases of the jaws: diagnosis and treatment. Copenhagen: Munksgaard; 1991. p. 206. 6. Regezi JA, Kerr DA, Courtney RM. Odontogenic tumours: an analysis of 109 cases. J Oral Surg 1978;36:771-8. 7. Daley TD, Wysocki GP, Pringle GA. Relative incidence of odontogenic tumours and oral and jaw cysts in a Canadian population. Oral Surg 1994;77:276-80. 8. Arotiba JT, Ogunbiyi JO, Obiechina AE. Odontogenic tumours: A 15-year review from Ibadan, Nigeria. Br J Oral Maxillofac Surg 1997;35:363-7. 9. Adekeye EO, Avery BS, Edwards MB, Williams HK. Advanced central myxoma of the jaws in Nigeria: clinical features, treatment and pathogenesis. Int J Oral Surg 1984;13:177-86. 10. Abiose BO, Ajagbe HA, Thomas O. Fibromyxomas of the jawbones–a study of 10 cases. Br J Oral Maxillofac Surg 1987;25:415-21. 11. Adebayo ET, Ajike SO, Adekeye EO. Odontogenic tumours in children and adolescents: a study of 78 Nigerian cases. J Craniomaxillofac Surg 2002;30:267-72. 12. Simon ENM, Merkx MAW, Vuhahula E, Ngassapa D, Stoelinga PJW. Odontogenic myxoma: a clinicopathological study of 33 cases. Int J Oral Maxillofac Surg 2004;33:333-7. 13. Ladeinde AL, Ajayi OF, Ogunlewe MO, Adeyemo WL, Arotiba GT, Bamgbose BO, et al. Odontogenic tumors: a review of 319 cases in a Nigerian teaching hospital. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005;99:191-5. 14. Harder F. Myxoma of jaws. Int J Oral Surg 1978;7:148-55. 15. Webb DJ, Colman MF, Rinaldo C. Odontogenic myxoma. Int J Oral Surg 1984;13:448-51. 16. Chuchurru JA, Ricardo L, Cornicelli JC, Dominguez FV. Myxoma of the mandible with unusual radiographic appearance. J Oral Maxillofac Surg 1985;43:987-90. 17. Cuestas-Carnero R, Bachur RO, Gendelman H. Odontogenic myxoma: report of a case. J Oral Maxillofac Surg 1988;46:705-9. 18. Peltola J, Magnusson B, Happonen RP, Borrman H. Odontogenic myxoma–a radiographic study of 21 tumours. Br J Oral Maxillofac Surg 1994;32:298-302. 19. MacDonald-Jankowsky DS, Yeung R, Lee KM, Li TKL. Odontogenic myxoma in the Hong Kong Chinese: clinico radiological presentation and systematic review. Dentomaxillofac Radiol 2002;21:71-83. 20. Farman AG, Nortjie CJ, Grotepass FW, Farman FJ, Van Zyl JA. Myxofibroma of the jaws. Br J Oral Surg 1977;15:3-18. 21. Farman AG, Nortjie CJ, Wood RE. Oral and maxillofacial diagnostic imaging. St. Louis: Mosby; 1993. p. 257– 60. 22. Mlosek K, Kryst L, Piekarczyk J. Odontogenic myxomas [Polish]. Pol Przegl Radiol Med Nukl 1982;46:21-6. 23. Slootweg PJ, Wittkampf ARM. Myxoma of the jaws–an analysis of 15 cases. J Maxillofac Surg 1986;14:46-52. 24. Happonnen RP, Peltola J, Ylipaavalniemi P, Lamberg M. Myxoma of the jaw bones. An analysis of 13 cases. Proc Finn Dent Soc 1988;84:45-52. 25. Gunhan O, Erseven G, Ruacan S, Celasun B, Aydintug Y, Ergun E, et al. Odontogenic tumours: a series of 409 cases. Aust Dent J 1990;35:518-22. 26. De Labrouhe C, Bertrand JC, Guilbert F. Radiologic aspects of myxomas of the jaws. A series of 27 cases. Rev Stomatol Chir Maxillofac 1994;95:80-3.
OOOOE July 2007 27. Odukoya O. Odontogenic tumors: analysis of 289 Nigerian cases. J Oral Pathol Med 1995;24:454-7. 28. Lo Muzio L, Nocinic PF, Favia G, Procaccini M, Mignogna MD. Odontogenic myxoma of the jaws: a clinical, radiologic, immunohistochemical and ultrastructural study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:426-33. 29. Mosqueda-Taylor A, Ledesma-Montes C, Caballero-Sandoval S, Portilla-Robertson J, Rivera LMR, Meneses-García A. Odontogenic tumors in Mexico: a collaborative retrospective study of 349 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84:672-5. 30. Stypulkowska J. Odontogenic tumors and neoplastic-like changes of the jaw bone. Clinical study and evaluation of treatment results. Folia Medica Cracov 1998;39:135-41. 31. Lu Y, Xuan M, Takata T, Wang C, He Z, Zhou Z, et al. Odontogenic tumors: a demographic study of 759 cases in a Chinese population. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:707-14. 32. Sassi LM, Biazolla ER, Freitas SEN, Ramos GHA, Oliveira BV. Myxoma of bones. Review of 17 cases. Oral Oncol 2001;37(Suppl):S77. 33. White SC, Pharoah MJ. Benign tumors of the jaws. In: White SC, Pharoah MJ, editors. Oral radiology principles and interpretation. 5th ed. St. Louis: Mosby; 2004. p. 433-4. 34. Leiberman A, Forte V, Thorner P, Crysdale W. Maxillary myxoma in children. Int J Pediatr Otorhinolaryngol 1990;18:277-84. 35. Wachter BJ, Steinberg MJ, Darro DH, MCGinn JD, Park AH. Odontogenic myxoma of the maxilla: a report of two pediatric cases. Int J Pediatric Otorhinolaryngol 2003;67:389-93. 36. Keszler A, Dominguez FV, Giannunzio G. Myxoma in childhood: an analysis of ten cases. J Oral Maxillofac Surg 1995;53:518-21. 37. Nitzan DW, Gazi D, Azaz B. Childhood odontogenic myxoma: report of two cases. Pediatr Dent 1985;7:140-4. 38. Fenton S, Slootweg PJ, Dunnebier EA, Mourits MP. Odontogenic myxoma in a 17 month old child. J Oral Surg 2003;61: 734-6. 39. Regezi JA, Sciubba J. Odontogenic tumors. In: Oral pathology, clinical-pathologic correlations. 2nd ed. Philadelphia: WB Saunders Co.; 1993. p. 379 – 83. 40. Kaffe I, Naor H, Buchner A. Clinical and radiological features of odontogenic myxoma of the jaws. Dentomaxillofac Radiol 1997; 26:299-303. 41. McClure DK, Dahlin DC. Myxoma of bone. Report of three cases. Mayo Clin Proc 1977;52:249-53. 42. Zimmerman DC, Dahlin DC. Myxomatous tumors of the jaws. Oral Surg 1958;11:1069-80. 43. Large ND, Niebel HH, Fredericks WH. Myxoma of the jaws: report of two cases. Oral Surg 1960;13:1462-8. 44. Schmidseder R, Groddeck A, Scheunemann H. Diagnostic and therapeutic problems of myxomas (myxofibromas) of the jaws. Maxillofac Surg 1978;6:281-6. 45. Worth HM. Principles and practice of oral radiologic interpretation. Chicago: Year Book Medical Publisher; 1963. p. 519-21. 46. Wood NK, Goaz PW. Molecular radiolucencies. In: Differential diagnosis of oral lesions. 5th ed. St. Louis: Mosby; 1997. p. 334. 47. Barros RE, Dominguez FV, Cabrini RL. Myxoma of the jaws. Oral Surg Oral Med Oral Pathol 1969;225-36. 48. White SC. Computer-aided differential diagnosis of oral radiographic lesions. Dentomaxillofac Radiol 1989;18:53-9. 49. Slootweg PJ, Muller H. Differential diagnosis of fibro-osseous jaw lesions: a histological investigation on 30 cases. J Craniomaxillofac Surg 1990;18:210-4. 50. White SC, Pharoah MJ. Principles of radiographic interpretation. In: White SC, Pharoah MJ, editors. Oral radiology principles and interpretation. 5th ed. St. Louis: Mosby; 2004. p. 281-96.
OOOOE Volume 104, Number 1 51. Whaites E. Differential diagnosis of lesions of variable radiopacity in the jaws. In: Whaites E, editor. Essential of dental radiography and radiology. 2nd ed. Edinburgh: Churchill Livingstone; 1989. p. 303-16. 52. Barnes L, Eveson JW, Reichart P, Sidransky D. World Health Organization Classification of Tumours. In: Pathology and genetics of head and neck tumours. Lyon: IARC Press; 2005. p. 283-318. 53. Martins C, Carvalho YR, Do Carmo MAV. Argyrophilic nucleolar organizer regions (AgNORs) in odontogenic myxoma (OM) and ameloblastic fibroma (AF). J Oral Pathol Med 2001;30:489-93. 54. Noffke C, Raubenheimer EJ. The glandular odontogenic cyst: clinical and radiological features; review of the literature and report of nine cases. Dentomaxillofac Radiol 2002;31:333-8. 55. MacDonald-Jankowski DS, Yeung RWK, Li T, Lee KM. Computed tomography of odontogenic myxoma. Clin Radiol 2004;59:281-7.
Noffke et al. 109 56. Hisatomi M, Asaumi J, Konouchi H, Yanagi Y, Matsuzaki H, Kishi K. Comparison of radiographic and MRI features of a root-diverging odontogenic myxoma, with discussion of the differential diagnosis of lesions likely to move roots. Oral Dis 2003;9:152-7. 57. Koseki T, Kobayashi K, Hashimoto K, Ariji Y, Tsuchimochi M, Toyama M, et al. Computed tomography of odontogenic myxoma. Dentomaxillofac Radiol 2003;32:160-5.
Reprint requests: Dr. Claudia E. E. Noffke Head, Maxillofacial and Oral Radiology Box D 16 P.O. MEDUNSA 0204, South Africa [email protected]
ORAL AND MAXILLOFACIAL RADIOLOGY
Editor: Allan G. Farman
Odontogenic myxoma: review of the literature and report of 30 cases from South Africa Claudia E. E. Noffke, BChD, MScOdont,a Erich J. Raubenheimer, MChD, FCPath(SA), PhD, DSc,b Ntombizonke J. Chabikuli, BDS, MDS,c and Michael M. R. Bouckaert, BChD, MDent,d Limpopo, South Africa UNIVERSITY OF LIMPOPO, MEDUNSA CAMPUS
Objective. The purpose of the study was to analyze the clinical and radiographic features of central odontogenic myxomas (OM) of the jaws diagnosed over 23 years in a black South African patient sample. Study design. Records of 30 cases of OMs with radiographs of diagnostic quality were retrieved from 52 cases of histopathologically verified OMs from the archives of the Oral Health Center at the University of Limpopo, South Africa. The age, sex, size, location, and radiographic features were compared with the literature. Results. The study consisted of 21 females and 9 males. The correlation between age and size of the tumor was found to be statistically significant (P ⫽ .004). Septa were shown to be either reorientated cortical bone or sheets of dense fibrous connective tissue. Indistinct borders mimicked malignancy. The most common radiographic feature was the tennis-racket appearance. Conclusions. Variations in radiographic presentation make a radiological differential interpretation of OM challenging because the radiographic features overlap with those of other benign and malignant neoplasms. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:101-9)
Odontogenic myxoma of the jaw was first described by Thoma and Goldman in 1947.1 In the international histological classification of odontogenic tumors, odontogenic myxoma (OM) is defined as a benign odontogenic tumor of mesenchymal origin that is locally invasive and consists of rounded and angular cells that lie in abundant mucoid stroma.2 The origin of OM is believed to be odontogenic ectomesenchyme of a developing tooth or undifferentiated mesenchymal cells in the periodontal ligament.3-5 The odontogenic origin a
Head, Division of Maxillofacial and Oral Radiology, Oral Health Center, University of Limpopo, Medunsa Campus. b Head, Department of Oral Pathology, Oral Health Center, University of Limpopo, Medunsa Campus. c Senior Lecturer, Division of Maxillofacial and Oral Radiology, Oral Health Center, University of Limpopo, Medunsa Campus. d Head, Department of Maxillofacial and Oral Surgery, Oral Health Center, University of Limpopo, Medunsa Campus. Received for publication Nov 27, 2006; returned for revision Jan 21, 2007; accepted for publication Jan 23, 2007. 1079-2104/$ - see front matter © 2007 Mosby, Inc. All rights reserved. doi:10.1016/j.tripleo.2007.01.026
of the neoplasm is supported by its histological similarity to pulpal ectomesenchyme, its exclusive occurrence in close proximity to the tooth-bearing parts of the jaws, occasional association with missing or unerupted teeth, presence of inactive odontogenic epithelium in a minority of cases, and its rare occurrence in other parts of the skeleton.2,5 In Asia, Europe, and America, frequencies for odontogenic myxoma between 0.5% and 17.7% of odontogenic tumors have been reported.6,7 Odontogenic myxomas in Africa perhaps occur slightly more commonly, with relative frequencies reported between 1% and 19%.8-12 In a Nigerian teaching hospital, OM occurs as the second most frequent benign tumor of the jaws after ameloblastoma.13 Odontogenic myxoma frequently displays aggressive infiltration of the adjacent tissue as well as a tendency to recur after surgical removal.14-19 In order to manage these tumors appropriately, it is imperative to determine their extent. The purpose of this study was to record cases of OM diagnosed in a black South African patient sample retrospectively and to compare the data with the literature. 101
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Table I. Demographic data of series larger than 10 cases reported after 1980 Author Mlosek et al. (1982)22 Adekeye et al. (1984)9 Slootweg and Wittkampf (1986)23 Abiose et al. (1987)10 Happonen et al. (1988)24 Günhan et al. (1990)25 De Labrouhe et al. (1993)26 Peltola et al. (1994)18 Odukoya (1995)27 Lo Muzio et al. (1996)28 Arotiba et al. (1997)8 Mosqueda-Taylor et al. (1997)29 Stypulkowska (1998)30 Lu et al. (1998)31 Sassi et al. (2001)32 MacDonald-Jankowski et al. (2002)19 Simon et al. (2004)12 Ladeinde et al. (2005)13 Present study 2006
No. of cases
Populations studied
Mean age
Gender M:F
Site max:mand
11 18 15 10 13 51 27 21 34 10 21 60 12 64 17 10 33 21 30
Poland Nigeria Netherlands Nigeria Finland Turkey France Scandinavia Nigeria Italy Nigeria Mexico Poland China Brazil Hong Kong Tanzania Nigeria South Africa
NA 27.8 26 25 33 32.3 36.1 35.1 24 32.7 33 NA 31.5 19.6 32 36.9 26.1 26.9 31.3
1:0.83 1:2.6 1:4 1:4 1:0.86 1:2.9 1:1.45 1:2 1:1.83 1:2.3 1:1.6 1:2 1:0.7 1:1 1:0.55 1:1.5 1:1.83 1:1 1:2.3
1:1.75 1:1.6 1:2.75 1:1.5 1:2.25 1:0.55 1:3.5 1:4.25 1:3.3 1:1.5 1:0.9 1:0.82 1:3 1:1.06 1:0.4 1:1.5 1:3 1:4.1 1:1.7
Max, maxilla; mand, mandible; NA, not available.
Although some authors report symptoms like pain and paresthesia,3,12,19 OM is generally depicted as slowgrowing tumor with the potential to attain considerable size without noticeable signs and symptoms.20,21 A summary of the demographics of large series recently reported is reflected in Table I.22-32 Children and persons more than 50 years of age are rarely affected.12,33 Several papers report OMs in patients under 10 years of age,34-38 with the youngest recorded case in a baby of 3 months.12 The molar and ramus regions of the mandible are most frequently involved,12,18,20 whereas the premolar–first molar region is the site of predilection in the maxilla.20 Regezi and Sciubba39 (1993) reported an equal distribution in anterior and posterior regions of the maxilla. Odontogenic myxomas in other sites of the jaws have rarely been recorded.12,18,40 In 5000 bone tumors affecting the skeleton studied by McClure and Dahlin41 (1977), only 3 cases of extragnathic myxomas were identified. The borders of multilocular OMs are described as well-defined corticated, well-defined noncorticated, poorly defined, or diffuse.33,40 Odontogenic myxomas can be extensive, involving half of the maxilla or mandible including the ramus and the condyle.18,19,40 The cortex appears thinned due to expansion and may perforate at a later stage of tumor progression. The maxillary sinus is often filled with tumor mass that can lead to exophtalmos.42 Some authors reported cases with unusual peripheral cortical reactions16,18,43,44 mimicking osteogenic malignant lesions. These were described either as radiopaque lines with vertical orientation to the mandible that extended from the periosteum into the
soft tissue, resembling a sunburst effect, or as a destructive lesion exhibiting a peripheral sunray appearance.43 Odontogenic myxoma is depicted in tooth-bearing areas as scalloping between the roots of the teeth.18 The internal structure of OM is described as either a unilocular or an expansile-multilocular radiolucency.18,40 Some authors described multilocular lesions with fine and/or rough trabeculations and applied terms like “tennis racket,” “soap bubble,” or “honeycomb” to depict the internal structure.16,18,19,33 The earliest description of the tennis racket appearance was given when Worth45 compared the locules of the OM with the angular, square, rectangular, or triangular spaces of a tennis racket. This description was accepted by subsequent authors.15,33,46 Farman et al.20 described cases of expansion of OM into the maxillary sinus, resulting in a radiopaque appearance of the sinus. Unusual multilocular lesions with diffuse calcifications in their internal structure have been reported.3,16,40,42,43,47 Although Kaffe et al.40 (1997) found radiological evidence of calcifications in 12.5% of 164 OMs published up to 1997, the microscopic nature of the septa and calcifications within OMs have not been studied in detail. One case was reported that presented like a pericoronal unilocular cystlike radiolucency and resembled a follicular cyst.46 Displacement of teeth is relatively common, though root resorption is less frequently seen.3,18,21 It was reported that involved teeth could be mobile but are usually vital.15,19 The differential diagnosis of OM includes other multilocular lesions like ameloblastoma, central giant cell granuloma, central
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hemangioma, aneurysmal bone cyst, and metastatic lesions to the jaws.18,21,33
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Table II. Distribution by age and gender of 30 odontogenic myxomas Age group (y)
METHODS Records with radiographs of 30 cases of OM were selected from 52 histopathologically verified OMs diagnosed at the Medunsa Oral Health Center of the University of Limpopo, South Africa during the period 1982 to 2005. The Oral Health Center serves mainly a rural and peri-urban African population sample, and consequently all patients were black. Clinical criteria for case acceptance included the presence of a medical and dental history and at least 1 conventional panoramic radiograph of acceptable diagnostic quality for evaluation. Twenty-two cases included extraosseous (peripheral) OM and were excluded from this study. Features of 30 OMs were recorded according to the clinical and radiological criteria suggested by White48 in the ORAD (Oral Radiographic Diagnosis) computeraided diagnostic system. Two previously calibrated investigators with postgraduate training in dental radiology evaluated the radiographs. The images were viewed on a Rinn (Dentsply; Rinn Corp., Elgin, IL) light box. The data were kept anonymous to protect the confidentiality of the patients. The lesions were measured in millimeters on panoramic radiographs—along the longest axis of the tumor—and tabulated. This measurement was selected because it represented the maximal extent of tumor growth. To establish the location of a lesion, the maxilla was divided into 6 anatomical regions, 3 on either side: (1) the anterior region from the midline to the distal surface of the canine, (2) the premolar region from the mesial aspect of the first premolar to the distal side of the second premolar, and (3) the molar region from the mesial aspect of the first molar to the distal surface of the maxillary tuberosity. Each half of the mandible was divided into 4 anatomical regions: (1) the anterior region from the midline to the distal surface of the canine, (2) the premolar region from the mesial aspect of the first premolar to the distal side of the second premolar, (3) the molar region from the mesial surface of the first molar to the beginning of the ascending ramus, and (4) the ramus region from the beginning of the ascending ramus to the sigmoid notch. According to the criteria for the degree of definition of the boundary of a lesion, it was considered to be well defined when its radiodensity changed markedly within a distance of 1 mm when passing from the lesion to the surrounding bone49 and when an imaginary pencil could trace most of the limits of the lesion confidently.50 A lesion was considered corticated when a thin, fairly uniform radiopaque line of reactive bone could be depicted at the periphery of most of the lesion and noncorticated when this line was
10-20 21-30 31-40 41-50 ⬎50 Age range Mean age Total
Male
Female
Total
2 2 3 1 1 11-63 33.1 9 (30%)
5 9 4 1 2 12-70 30.5 21 (70%)
7 (23%) 11 (37%) 7 (23%) 2 (7%) 3 (10%) 11-70 31.3 30 (100%)
Table III. Location of 30 odontogenic myxomas Area Anterior mandible (crossing midline) Premolar and molar area Molar and ramus area Lesions that cross the midline from posterior to posterior area Total
Mandible
Maxilla
Total
1 6 7 5
NA 11 NA —
1 17 7 5
19
11
30
NA, not available.
absent. A lesion was considered poorly defined when it was difficult to outline its periphery and diffuse when the transitional zone between the lesion and the unaffected bone was wide and indistinct. Statistical analysis The internal structure indicated the degree of calcification, locularity, and if present, type of septa. A lesion was considered calcified when radiopaque areas appeared within an otherwise radiolucent lesion.40,50 The presence of locules was indicative of septa. If these divided the radiolucent internal structure into at least 2 compartments, the term multilocular was used. A unilocular lesion represented a single radiolucent lesion that could include internal calcifications but no compartments. The radiographic patterns created by the septa were ascribed to widely used descriptive terms: soap bubble represented large spaces surrounded by round or curved bony septa, tennis racket was represented by crossed straight septa resembling the strings of a tennis racket, honeycomb presented small angular spaces resembling a bee’s honeycomb, and a “ground glass” appearance described the visual effect of many fine, poorly calcified trabeculations being superimposed on each other and arranged in a disorganized fashion.51 The influence of the lesions on the adjacent structures such as the teeth and cortical borders was recorded and tabulated. Microscopic sections were reviewed with the purpose of providing more insight into the nature of the septa. Statistical analysis included the calculation of de-
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Table IV. Relationship between the size of 30 odontogenic myxomas, their location, and locularity Location Size range (mm) 10-20 21-30 31-40 41-50 51-60 61-70 71-80 ⬎80
Unilocular
Multilocular
Maxilla
Mandible
Maxilla
Mandible
Maxilla
Mandible
0 0 0 2 6 2 1 0 11
1 2 1 4 1 3 3 4 19
0 0 0 0 2 0 0 0 2
0 2 1 1 0 0 0 0 4
0 0 0 2 4 2 1 0 9
1 0 0 3 1 3 3 4 15
Total Total size range Mean size Median size
30
6 30-55 42.5 42.5
24 15-130 70.7 66.5
Table V. Radiographic appearance of 30 odontogenic myxomas Mandible Maxilla Borders Well defined and corticated Well defined and noncorticated Poorly defined Poorly defined with invasive pattern Diffuse Perforation of mandibular cortex Expansion of mandible Invasion of the sinus only Invasion of the sinus and the nose cavity Internal structure Unilocular Multilocular Soap bubble appearance Tennis racket appearance Honeycomb appearance Ground glass appearance Calcifications Effect on adjacent teeth Impactions Extrusion and mobile teeth Widened periodontal ligament Tooth displacement Root resorption Scalloping between teeth Cases associated with missing teeth
Total
7 4 7 1
0 0 1 1
7 (23%) 4 (13%) 8 (26%) 2 (7%)
0 7 18
7
9 2
7 (23%) 7 (23%) 18 (95%) 9 (82%) 2 (18%)
4 15 5 7 3 0 6
2 9 2 6 1 2 3
6 (20%) 24 (80%) 7 (23%) 13 (43%) 4 (13%) 2 (7%) 9 (30%)
1 8 2 15 10 2 2
2 1 0 7 3 0 1
3 (10%) 9 (30%) 2 (7%) 22 (73%) 13 (43%) 2 (7%) 3 (10%)
scriptive statistics and comparisons of mean values by the t test and median values by the nonparametric Wilcoxon test. A regression analysis was conducted, with size of the tumor as dependent variable and age, sex, location, internal structure, tooth displacement, root resorption, and borders as independent predictor variables. Correlation coefficients were calculated as appropriate.
Fig. 1. Soap bubble appearance of an odontogenic myxoma (OM) in the mandible. Note the large, smooth, curved septa in the tumor.
RESULTS Five hundred seventy-one odontogenic tumors (excluding keratocystic odontogenic tumors that were recently included in the World Health Organization classification of odontogenic tumors)52 were diagnosed over a 23-year period, of which 52 cases (9.1%) were OM. The distribution according to age and sex of the 30 cases of the sample is given in Table II, and the location of the lesions is noted in Table III. The relationship between the size, location, and locularity of the lesions is reflected in Table IV. The size range for unilocular lesions varied from 30 to 55 mm (mean, 42.5 mm), whereas the size range for multilocular lesions varied from 15 to 130 mm (mean, 70.7 mm). The mean size of unilocular lesions was significantly less than that of multilocular lesions (t test; P ⫽ .026). The median size of unilocular lesions was also significantly less than the
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Fig. 2. Tennis racket appearance of a maxillary OM showing angular intersections of septa.
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Fig. 4. Ground glass appearance of a maxillary OM resembling a fibro-osseous lesion.
Two cases in the maxilla presented with a ground glass appearance (Fig. 4). Comparison between the microscopic slides of archived tissue and the radiographic images showed trabeculations to consist of 2 tissue types: the radiopaque septa, most frequently located at the peripheral aspects of the OMs, were composed of lamellar bone (Fig. 5, A). The delicate septa toward the center of the neoplasms consisted of broad fibrous connective tissue bands (Fig. 5, B). The latter divided the tumor in myxoid lobules. Fig. 3. Honeycomb appearance of a maxillary OM. Note the small adjacent spaces resembling a honeycomb.
median size of multilocular lesions (Wilcoxon test, P ⫽ .008). From a regression analysis conducted on the data with the size of the tumor as a dependent variable, the only predictor variable found to be statistically significant was the age of the patient (P ⫽ .0143). The overall correlation between age and size of the tumor was found to be r ⫽ 0.508 which is statistically significant (P ⫽ .004). In the case of males only, the correlation between age and size of the tumor was found to be r ⫽ 0.133, which is not statistically significant (P ⫽ .732). The correlation between age and size of the tumor for females was found to be r ⫽ 0.665, which is statistically highly significant (P ⫽ .001). A summary of the radiographic features of OM is provided in Table V. The trabeculation of the multilocular lesions showed either soap bubble (Fig. 1), tennis racket (Fig. 2), or honeycomb (Fig. 3) appearances.
DISCUSSION The odontogenic myxoma is generally considered to be a rare neoplasm unique to the jaws, and only a few series with significant numbers of patients have been published (Table I). This series of 52 cases is 9.1% of 571 odontogenic tumors diagnosed over a period of 23 years. The current study supports the finding of Ladeinde et al.13 (2005) and others that OMs do not occur infrequently in African hospital series.8-13 In our archives, they occur more frequently than odontomas (6.5% of our sample). It should be kept in mind, however, that odontomas are usually symptom free and are detected incidentally on radiographs. A speculative number may therefore go unnoticed in all studies of this nature. The study showed a wide age range (11-70 years) and supported previous observations that an OM can occur at any age from childhood to the elderly.15,21,22 It occurred most frequently in the fourth decade in our sample, with a mean age of 31.3 years. These results comply with most reports in the literature as documented in Table I. It is generally accepted that OM is
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Fig. 5. Microscopic appearances of septa in OMs. A, Bony septa (arrow) at the periphery of the case shown in Fig. 1 (hematoxylin-eosin, original magnification ⫻ 80). B, Delicate fibrous connective tissue septa (arrows) of the case shown in Fig. 3 (hematoxylin-eosin, original magnification ⫻50).
rare before 10 years of age and above 50 years of age.12 However, it was stated that the frequency of OM in childhood might be higher than that of other aggressive odontogenic tumors.36 In a study of 80 cases of OM, an incidence of 12.5% in children between the ages of 5 and 16 years (mean age of 11.6 years) was reported.36 In this series, no cases were found in the first decade. This may be due to the tendency of our patients to seek medical care at a late stage. To our knowledge, no correlation between the age of the patient and the size of the tumor has been reported. The present study showed that the correlation between these 2 variables was statistically significant (P ⫽ .001), particularly in the case of females. The male to female ratio in our sample was 1:2.3, and the higher tendency for females was seen in all age groups. This was in agreement with findings of investigators in the rest of the African continent and in other countries (Table I). Equal distri-
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bution among the sexes was noted in China.31 Odontogenic myxoma has been reported by most authors to occur more frequently in the mandible than in the maxilla (Table I), corresponding with the ratio of 1.7:1 in this study. However, Regezi et al.6 (1978) reported an equal distribution in the mandible and the maxilla. In the current study, only 1 lesion was found exclusively in the anterior area of the mandible, whereas 29 lesions were in the posterior areas of both jaws (Table III). This finding correlates with most other reports.19,33,40 Six mandibular lesions crossed the midline. This is probably size related in the mandible and is in contrast with Simon et al.12 (2004), who noted midline crossing to be rare. In the maxilla, the OMs did not cross the median palatal suture, a finding confirmed by the literature. This study presented with 11 well-defined cases in the mandible, 7 of these being corticated and 4 noncorticated. Seven maxillary cases presented with diffuse borders. Eight cases—7 of them located in the mandible and 1 in the maxilla—presented with poorly defined borders, whereas 2 OMs, 1 in each jaw, showed poorly defined borders with invasive patterns. These features together with perforation of the inferior cortical mandibular border in 7 cases resembled malignancy, bringing this into consideration in the differential diagnosis of OM. However, sarcomatous changes in OM are reported to be rare and were described in only 2 cases that resulted in death.22 Nine of the 11 maxillary lesions (82%) showed encroachment on the maxillary sinus only, and 2 lesions affected the maxillary sinus as well as the nasal cavity. This finding is supported in the literature, where it is reported that maxillary lesions encroach upon the maxillary sinus; however, lesions infiltrating the nasal cavity are rare.19 Two mandibular lesions showed scalloping between the teeth, a finding that correlates with the literature.41 Tooth displacement is commonly reported; however, root resorption appears to be rare.18,21,39 In this study, 22 lesions displaced teeth, confirming the frequent occurrence as well as indicating a slow tumor growth rate. Although consensus is that OM grows slowly, there are scattered reports of rapid enlargement.44 The cell-proliferating index of OM was found to be low, and it was therefore suggested that the invasive nature and high tendency of OM to recur was more likely to be the result of tumor spillage in the operating field due to the gelatinous consistency and the poorly defined borders, which present in nearly half of all OMs investigated.33,53 Thirteen cases presented with root resorption, which is relatively high compared with findings in the literature. Kaffe et al.40 (1997) found both features relatively uncommon, with tooth displacement noticed in 26% of cases and root resorption in 9.5% of cases studied. Although no longer generally accepted, it was believed
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that malignancy could not be excluded in the case of neoplasms with indistinct borders and root resorption.3 The more frequent occurrence of root resorption in this study may be due to the larger size and subsequent pressure of OMs when compared with those reported in the literature. All 9 neoplasms manifesting with tooth extrusion showed excessive mobility of associated teeth. Most of these were large lesions that occurred in the mandible. The lack of tooth extrusion in most of the maxillary OMs is probably the result of growth into the maxillary sinus, unlike mandibular OMs that expand into the alveolus.20 Most OMs are reported to be multilocular with coarse or angular trabeculations,20 yet other studies show an equal distribution between unilocularity and multilocularity.18,24 It was reported that the size of the lesions correlated with their locularity.18,40 Multilocular lesions reached sizes larger than 40 mm, thereby exceeding unilocular lesions in the greatest dimension. These findings correspond with the current study. Seven of the 24 multilocular OMs in this study could be described as a soap bubble pattern, referring to multiple round or oval compartments formed by curved bony septa. Thirteen were characterized by square or triangular compartments formed by straight trabeculations and were appropriately described as tennis racket pattern. The honeycomb pattern was exhibited by 4 cases that were characterized by small, round, or angular spaces. Microscopic examination showed that the coarse welldefined peripheral septa were reorientated residual lamellar cortical bone. However, most of the delicate internal septa were found to be dense fibrous partitions that divided the OM in myxomatous lobules. Two cases in the maxilla resembled fibrous dysplasia and were described as having a ground glass appearance. Supporting the opinion of Kaffe et al.,40 it is believed that this pattern is due to the neoplasm projecting into the otherwise radiolucent maxillary sinus, thereby manifesting with increased radiodensity. Some OMs, however, showed a mixed radiopaque-radiolucent appearance,12,33,40 which was ascribed to the presence of foci of calcification.3,40,47 It was suggested that this appearance may be due to residual bone and not to new bone formation, and therefore it was proposed that OM should be considered in the differential diagnosis of mixed radiolucent-radiopaque lesions.40 Although most OMs in this study were entirely radiolucent, 9 patients presented with radiopacities in the lesions. The differential diagnosis of multilocular OMs should include ameloblastoma, intraosseous hemangioma, aneurysmal bone cyst, central giant cell granuloma, cherubism metastatic neoplasms to the jaws,18 glandular odontogenic cyst,55 and the odontogenic keratocyst, especially the multilocular type. Giant cell
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granulomas affect the anterior region of the jaws more frequently than the posterior, giant cell lesions of hyperparathyroidism can be eliminated if the serum chemistry is normal, cherubism is a hereditary condition characterized by bilateral facial swelling during early childhood, aneurysmal bone cysts present with pain and tenderness as opposed to most OM, and intrabony hemangiomas can be ruled out after a nonproductive aspiration.18 In older patients, the possibility of a malignancy should not be ruled out because radiographic features resembling osteosarcoma have been reported.16,18,44 Some cases in our series presented with extruded teeth and widened periodontal ligament spaces, mimicking an osteogenic malignancy. The glandular odontogenic cyst is reported to occur most frequently in the globulomaxillary region, which is not the location of preference for OM. The lack of modern imaging modalities in this study is the result of its retrospective nature. Literature indicates that computed tomography (CT) and magnetic resonance imaging have been found to be superior to plain radiographs when establishing the intraosseous extent of the tumor, cortical perforation and soft tissue involvement, and extent.15,21,33,55,56 Tooth displacement and root resorption, however, can be observed more reliably on conventional radiographs.55 Computed tomographic imaging shows most bony septa to be located at the periphery of an OM.55-57 This characteristic feature was demonstrated in our study by the use of histological examination. It was reported, however, that even with CT examination, several OMs could not be distinguished from other lesions.57 Magnetic resonance imaging is indicated in cases of suspected recurrent OM, because this modality facilitates the differentiation between fibrous connective tissue and tumor tissue due to different signal intensities.21 CONCLUSIONS Variations in radiographic presentation make radiological differential interpretation of OM challenging, as the radiographic features overlap with those of other benign and malignant neoplasms. A biopsy is therefore mandatory in establishing a final diagnosis. Correlation between tumor size and age of patients was significant, and septa seen on radiographs represented either reorientated residual bone or dense fibrous connective tissue partitions. The authors wish to thank Professor H. S. Schoeman for statistical analyses, Professor C. J. Nortje for editorial advice, and C. S. Begemann for typographical assistance. REFERENCES 1. Thoma KH, Goldman HM. Central myxoma of the jaw. Am J Oral Surg Orthod 1947;33:532.
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OOOOE July 2007 27. Odukoya O. Odontogenic tumors: analysis of 289 Nigerian cases. J Oral Pathol Med 1995;24:454-7. 28. Lo Muzio L, Nocinic PF, Favia G, Procaccini M, Mignogna MD. Odontogenic myxoma of the jaws: a clinical, radiologic, immunohistochemical and ultrastructural study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:426-33. 29. Mosqueda-Taylor A, Ledesma-Montes C, Caballero-Sandoval S, Portilla-Robertson J, Rivera LMR, Meneses-García A. Odontogenic tumors in Mexico: a collaborative retrospective study of 349 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84:672-5. 30. Stypulkowska J. Odontogenic tumors and neoplastic-like changes of the jaw bone. Clinical study and evaluation of treatment results. Folia Medica Cracov 1998;39:135-41. 31. Lu Y, Xuan M, Takata T, Wang C, He Z, Zhou Z, et al. Odontogenic tumors: a demographic study of 759 cases in a Chinese population. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:707-14. 32. Sassi LM, Biazolla ER, Freitas SEN, Ramos GHA, Oliveira BV. Myxoma of bones. Review of 17 cases. Oral Oncol 2001;37(Suppl):S77. 33. White SC, Pharoah MJ. Benign tumors of the jaws. In: White SC, Pharoah MJ, editors. Oral radiology principles and interpretation. 5th ed. St. Louis: Mosby; 2004. p. 433-4. 34. Leiberman A, Forte V, Thorner P, Crysdale W. Maxillary myxoma in children. Int J Pediatr Otorhinolaryngol 1990;18:277-84. 35. Wachter BJ, Steinberg MJ, Darro DH, MCGinn JD, Park AH. Odontogenic myxoma of the maxilla: a report of two pediatric cases. Int J Pediatric Otorhinolaryngol 2003;67:389-93. 36. Keszler A, Dominguez FV, Giannunzio G. Myxoma in childhood: an analysis of ten cases. J Oral Maxillofac Surg 1995;53:518-21. 37. Nitzan DW, Gazi D, Azaz B. Childhood odontogenic myxoma: report of two cases. Pediatr Dent 1985;7:140-4. 38. Fenton S, Slootweg PJ, Dunnebier EA, Mourits MP. Odontogenic myxoma in a 17 month old child. J Oral Surg 2003;61: 734-6. 39. Regezi JA, Sciubba J. Odontogenic tumors. In: Oral pathology, clinical-pathologic correlations. 2nd ed. Philadelphia: WB Saunders Co.; 1993. p. 379 – 83. 40. Kaffe I, Naor H, Buchner A. Clinical and radiological features of odontogenic myxoma of the jaws. Dentomaxillofac Radiol 1997; 26:299-303. 41. McClure DK, Dahlin DC. Myxoma of bone. Report of three cases. Mayo Clin Proc 1977;52:249-53. 42. Zimmerman DC, Dahlin DC. Myxomatous tumors of the jaws. Oral Surg 1958;11:1069-80. 43. Large ND, Niebel HH, Fredericks WH. Myxoma of the jaws: report of two cases. Oral Surg 1960;13:1462-8. 44. Schmidseder R, Groddeck A, Scheunemann H. Diagnostic and therapeutic problems of myxomas (myxofibromas) of the jaws. Maxillofac Surg 1978;6:281-6. 45. Worth HM. Principles and practice of oral radiologic interpretation. Chicago: Year Book Medical Publisher; 1963. p. 519-21. 46. Wood NK, Goaz PW. Molecular radiolucencies. In: Differential diagnosis of oral lesions. 5th ed. St. Louis: Mosby; 1997. p. 334. 47. Barros RE, Dominguez FV, Cabrini RL. Myxoma of the jaws. Oral Surg Oral Med Oral Pathol 1969;225-36. 48. White SC. Computer-aided differential diagnosis of oral radiographic lesions. Dentomaxillofac Radiol 1989;18:53-9. 49. Slootweg PJ, Muller H. Differential diagnosis of fibro-osseous jaw lesions: a histological investigation on 30 cases. J Craniomaxillofac Surg 1990;18:210-4. 50. White SC, Pharoah MJ. Principles of radiographic interpretation. In: White SC, Pharoah MJ, editors. Oral radiology principles and interpretation. 5th ed. St. Louis: Mosby; 2004. p. 281-96.
OOOOE Volume 104, Number 1 51. Whaites E. Differential diagnosis of lesions of variable radiopacity in the jaws. In: Whaites E, editor. Essential of dental radiography and radiology. 2nd ed. Edinburgh: Churchill Livingstone; 1989. p. 303-16. 52. Barnes L, Eveson JW, Reichart P, Sidransky D. World Health Organization Classification of Tumours. In: Pathology and genetics of head and neck tumours. Lyon: IARC Press; 2005. p. 283-318. 53. Martins C, Carvalho YR, Do Carmo MAV. Argyrophilic nucleolar organizer regions (AgNORs) in odontogenic myxoma (OM) and ameloblastic fibroma (AF). J Oral Pathol Med 2001;30:489-93. 54. Noffke C, Raubenheimer EJ. The glandular odontogenic cyst: clinical and radiological features; review of the literature and report of nine cases. Dentomaxillofac Radiol 2002;31:333-8. 55. MacDonald-Jankowski DS, Yeung RWK, Li T, Lee KM. Computed tomography of odontogenic myxoma. Clin Radiol 2004;59:281-7.
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