- Email: [email protected]
Ameloblastoma: a multicentric study
Vol. 113 No. 6 June 2012
Ameloblastoma: a multicentric study Kittipong Dhanuthai, DDS, MSc,a Soranun Chantarangsu, DDS, PhD,a Somsri Rojanawatsirivej, DDS, MS,a Ekarat Phattarataratip, DDS, PhD,a Mark Darling, BChD, MChD,b Linda Jackson-Boeters, MLT,b Nasser Said-Al-Naief, DDS, MS,c Hong-In Shin, DDS, PhD,d Chang-Hyeong An, DDS, PhD,e Nguyen Thi Hong, DDS, PhD,f Phan Huynh An, DDS, PhD,g Watcharaporn Thosaporn, DDS, MS,h Aroonwan Lam-ubol, DDS, PhD,i and Ajiravudh Subarnbhesaj, DDS, MS,j Bangkok, Chiang Mai and Khon Kaen, Thailand; Ontario, Canada; San Francisco, California, USA; Daegu, Korea; and Ho Chi Minh City, Vietnam CHULALONGKORN UNIVERSITY, UNIVERSITY OF WESTERN ONTARIO, UNIVERSITY OF THE PACIFIC, KYUNGPOOK NATIONAL UNIVERSITY, UNIVERSITY OF MEDICINE AND PHARMACY, CHIANGMAI UNIVERSITY, SRINAKHARINWIROT UNIVERSITY, AND KHON KAEN UNIVERSITY
Objective. The objective of this study was to supplement the current ameloblastoma database by reporting the clinicopathologic features of ameloblastoma from Asia and North America. Materials and Methods. Biopsy records of the participating institutes were reviewed for lesions diagnosed as ameloblastoma during the years 1993 to 2009. Slides were reclassified according to the World Health Organization Classification of Odontogenic Tumors in 2005. Clinical information and radiographic features were collected and analyzed. Results. The mean age of the patients ⫾ SD was 38.27 ⫾ 17.78 years; 662 patients (51.36%) were men. Mandible (84.26%) outnumbered maxilla and other locations combined in all countries. The number of multilocular radiolucencies (43.40%) was comparable with that of unilocular radiolucencies (42.04%). Follicular pattern was the most common histopathologic pattern (27.70%), followed by plexiform (21.10%) and unicystic pattern (20.71%), respectively. Conclusions. The clinicopathologic features of ameloblastomas in the present study show some similarities with previous studies; however, minor differences exist. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:782-788)
a
Department of Oral Pathology, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand. b Department of Pathology, Schulich School of Medicine and Dentistry, University of Western Ontario, Ontario, Canada. c Oral & Maxillofacial Pathology Laboratory, Clinical Oral Pathology/Oral Medicine, Department of Pathology & Medicine, University of the Pacific, San Francisco, CA, USA. d Department of Oral Pathology, School of Dentistry, Kyungpook National University, Daegu, Korea. e Department of Oral and Maxillofacial Radiology, School of Dentistry, Kyungpook National University, Daegu, Korea. f Department of Oral Pathology, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam. g Department of Oral Surgery, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam. h Department of Oral Biology and Diagnostic Sciences, Faculty of Dentistry, Chiangmai University, Chiang Mai, Thailand. i Formerly, Department of Oral Pathology, Radiology and Medicine, The University of Iowa; currently, Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, Srinakharinwirot University, Bangkok, Thailand. j Department of Oral Diagnosis, Khon Kaen University, Khon Kaen, Thailand. Received for publication Oct 4, 2011; returned for revision Jan 4, 2012; accepted for publication Jan 13, 2012. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2012.01.011
782
Ameloblastoma is a benign, locally aggressive odontogenic tumor that has a close histopathologic resemblance to the enamel organ. It belongs to the group of tumors arising from odontogenic epithelium with mature fibrous stroma without odontogenic ectomesenchyme according to the World Health Organization (WHO) Classification of Odontogenic Tumors in 2005. Ameloblastoma is divided into 4 types: unicystic, solid/ multicystic, desmoplastic, and peripheral.1 It is believed to originate from remnants of tooth-forming apparatus, such as developing enamel organ, odontogenic rests, reduced enamel epithelium and the epithelial lining of odontogenic cysts, especially dentigerous cysts, or from the basal epithelial cells of the oral mucosa.2,3 There have been several case series of ameloblastomas from several countries with geographic and/or racial variations. Ameloblastoma ranks as the most common odontogenic tumor in Asia and Africa, whereas odontoma is listed as the most common odontogenic tumor in Europe and America.4-12 The fact that odontomas are discovered during routine radiographic examinations and do not produce clinical symptoms may account for odontoma underreporting in the developing countries, as most patients in developing countries do not seek medical attention until their pathologies become symptomatic or grossly apparent.13 The average age of patients afflicted with ameloblastoma in industrialized countries was 39.1 years, whereas developing it was 27.7 years.14
OOOO Volume 113, Number 6
ORIGINAL ARTICLE Dhanuthai et al. 783
Table I. Age distribution of the patients with ameloblastoma Age, y
North America USA Canada Asia Korea Thailand Vietnam Total
Total
0-10
11-20
21-30
31-40
41-50
51-60
61-70
71-80
81-90
91-100
101-110
NS
Mean ⫾ SD
250 153 97 1039 210 751 78 1289
1 0 1 16 1 15 0 17
22 16 6 191 49 128 14 213
34 17 17 221 45 158 18 255
34 23 11 215 44 154 17 249
45 33 12 184 32 136 16 229
40 22 18 123 22 93 8 163
31 15 16 56 13 38 5 87
26 11 15 17 4 13 0 43
13 12 1 4 0 4 0 17
2 2 0 0 0 0 0 2
2 2 0 0 0 0 0 2
0 0 0 12 0 12 0 12
48.54 ⴞ 0.54 48.65 ⫾ 1.43 48.35 ⫾ 9.18 35.75 ⴞ 6.09 34.52 ⫾ 6.37 36.12 ⫾ 6.15 35.62 ⫾ 4.66 38.26 ⫾ 7.78
NS, not specified.
According to Dodge,15 the aging process may be accelerated in developing countries as a result of poor nutrition and health care. Gender and radiographic differences have also been reported among series.16-21 Only the mandibular predilection and 2 most common histopathologic patterns (follicular and plexiform) seem to be agreed on by most reported series. Since the study by Reichart and coworkers in 1995,14 there has been no large-scale case series of ameloblastoma. Most of the reported series of ameloblastoma from Asia are from China and Japan.4,11,16,22-25 There has been a paucity of information from other countries in Asia, such as Thailand and Vietnam, especially in the English-language literature. The objective of this study was to supplement the current ameloblastoma database by reporting the clinicopathologic features of ameloblastoma from Asia (Thailand, Vietnam, and Korea) and North America (Canada and the United States).
MATERIALS AND METHODS The biopsy records of the Department of Oral Pathology, Chulalongkorn University, Kyungpook National University, and University of Medicine and Pharmacy; Department of Oral Biology and Diagnostic Sciences, Chiangmai University; Department of Oral Diagnosis, Khon Kaen University; Department of Oral Pathology, Radiology and Medicine, University of Iowa; Department of Pathology, The University of Alabama at Birmingham and University of Western Ontario were reviewed for ameloblastomas diagnosed from 1993 to 2009. Hematoxylin and eosin–stained glass slides were reviewed and reclassified according to the current WHO criteria.1 Clinical and radiographic information was documented for each case. Maxillary intraosseous lesions were separated into 3 regions: anterior (midline to the distal surface of canine), posterior (mesial surface of the first premolar to the distal surface of the third molar), and tuberosity area. Similarly, mandibular tumors were separated into anterior (midline to the distal surface of canine); posterior (mesial surface of the first premolar to the distal surface of the third
molar); and angle, ramus, condyle, coronoid process. Lesions that occurred exclusively in soft tissue were so designated. Lesions encountered in locations other than the aforementioned ones were designated as “other.” Data collected were analyzed by SPSS version 13.0 (Chicago, IL). The Kruskal-Wallis and Mann-Whitney U tests were used to determine the association between clinical and pathologic parameters. A P value less than .05 was considered to be statistically significant. The ethical committee of the Faculty of Dentistry, Chulalongkorn University approved this research (no. 10/ 2009).
RESULTS Of the 143,712 total accessioned cases, 1289 cases (0.90%) were diagnosed as ameloblastoma. Ameloblastoma constituted from 0.14% (Canada) to 9.96% (Vietnam) of the total accessioned cases. In Asia, 1039 cases (4.64%) were diagnosed as ameloblastoma, whereas 250 cases (0.21%) were diagnosed as ameloblastoma in North America. The age of the patients in the present study ranged from 4 to 107 years with a mean ⫾ SD of 38.26 ⫾ 17.78 years. The mean age of patients afflicted with ameloblastoma in Asia was significantly lower than that in North America (P ⬍ .0001). The peak incidence varied from the second decade in Korea to the sixth decade in Canada. Overall, the peak incidence in Asia fell in the third decade compared with the fifth decade in North America. In all countries, the age of patients with unicystic ameloblastoma was significantly lower than that of solid/multicystic ameloblastoma (data not shown). The age distribution is shown in Table I. Of the 1289 cases of ameloblastoma in the present study, there were 662 males (51.36%) and 627 females (48.64%). The male-to-female ratio was 1.00:0.95, but the difference was not statistically significant (P ⫽ .343). There was an almost equal distribution between genders in Thailand and the United States. North America exhibited male predominance (P ⫽ .043), whereas Asia exhibited a slight male predominance, but the
ORAL AND MAXILLOFACIAL PATHOLOGY 784 Dhanuthai et al.
OOOO June 2012
Table II. Gender distribution of patients with ameloblastoma Total
Male
Female
250 153 97 1039 210 751 78 1289
141 (56.40) 81 (52.94) 60 (61.86) 521 (50.14) 116 (55.24) 371 (49.40) 34 (43.59) 662 (51.36)
109 (43.60) 72 (47.06) 37 (38.14) 518 (49.86) 94 (44.76) 380 (50.60) 44 (56.41) 627 (48.64)
The follicular pattern was the most common histopathologic pattern in most countries except Korea, which had almost equal distribution between follicular and plexiform patterns. The second most common histopathologic pattern for solid/multicystic ameloblastoma in North America was mixed follicular and plexiform pattern, closely followed by the pure plexiform pattern. On the other hand, the plexiform pattern was the second most common pattern in Asia, followed by the acanthomatous pattern. The histopathologic features of ameloblastoma are summarized in Table V.
difference was not statistically significant (P ⫽ .951). The gender distribution of ameloblastoma is shown in Table II. Ameloblastoma demonstrated a strong predilection for the mandible with the mandible-to-maxilla ratio as high as 13.29:1.00 in Korea. Mandible outnumbered maxilla and other locations combined in all countries. Soft tissue lesions were encountered in only 55 cases or 4.27% of the cases. These sites included gingiva, soft tissue of the tuberosity, retromolar pad, and edentulous areas. In the mandible, the posterior region was the predominant site of involvement in all countries, followed by the ramus, angle, and condyle in almost all countries except the United States and Canada in which the anterior region ranked as the second most common site. In the maxilla, the posterior site of region was the predilection in all countries. The anatomical distribution of ameloblastoma is shown in Table III. Radiographic data were not available in 183 cases (14.20%); therefore, the radiographic data were based on the data of the remaining 1106 cases. In general, the number of unilocular radiolucency cases was comparable to that of the multilocular counterpart. Radiographically, 480 cases (43.40%) exhibited multilocular radiolucency, 465 cases (42.04%) showed unilocular radiolucency, and 46 cases (4.16%) demonstrated a mixed radiolucent-radiopaque pattern. Radiolucencies associated with impacted teeth were encountered in 115 cases (10.40%). Another interesting finding was that the number of cases presenting as radiolucency associated with impacted teeth in North America was twice as high as that in Asia. Summary of the radiographic features is shown in Table IV. Histopathologically, most tumors (75.02%) were of solid/multicystic type (Figure 1). Unicystic, desmoplastic, and peripheral ameloblastomas accounted for 20.71%, 4.34%, and 4.27% of the cases, respectively (Figure 2, A and B). Of particular interest, the incidence of unicystic ameloblastoma was remarkably higher in Asia than in North America, whereas the opposite was true for peripheral ameloblastoma.
DISCUSSION In 1995, Reichart et al.14 reviewed the biological profile of 3677 ameloblastomas; the largest series so far. The age of patients in their series ranged from 4 to 92 years. Our data were in accordance with this range. The peak incidence in Asia fell in the third decade of life as compared with the fifth decade of life in North America. This was also in line with previous studies from Thailand,17 Korea,18 India,13 China,11 Kenya,19 and the United States.10 The explanation for this difference may reflect ethnic and possibly socioeconomic differences, as almost of the patients from Asia are of Asian descent, whereas in North America most are Whites. In addition, people in North America frequently have better access to medical care than people in developing countries, such as Thailand and Vietnam. North American patients are more likely to have regular dental visits and routine radiographic check-ups. As a consequence, oral lesion are detected at a younger age. The explanation for the lower average age of patients with ameloblastoma in developing countries compared with that of industrialized countries as being may reflect poor nutrition and reduced access to the health care system in developing countries, as proposed by Dodge’s concept15 may not be entirely applicable. Korea, for example, an industrialized country with a high standard of living and a well-respected health care system, has an average age of patients with ameloblastoma comparable with that of other Asian countries. In all countries, the age of patients with unicystic ameloblastoma was lower than that of patients with solid/multicystic ameloblastoma. This is in accordance with previous studies.14,18,26 The present study revealed an almost equal gender distribution, which is also in accordance with previous studies,14,21,27,28 with the exception of selective studies that demonstrated either male or female predominance.4,13,18,19 The mandible is the site of predilection for odontogenic tumors, including ameloblastoma. In the present study, 1087 cases (84.26%) of intraosseous ameloblastomas were encountered in the mandible. This figure is comparable with the 87.3% reported in a Korean
Gender, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
OOOO Volume 113, Number 6
ORIGINAL ARTICLE Dhanuthai et al. 785
Table III. The anatomical distribution of the patients with ameloblastoma Maxilla, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
Mandible, n (%)
Anterior
Posterior
Tuberosity
Anterior
Posterior
Ramus, angle, condyle
7 (3.85) 3 (2.56) 4 (6.15) 54 (3.42) 5 (1.80) 46 (3.90) 3 (2.44) 61 (3.46)
18 (9.89) 10 (8.55) 8 (12.31) 70 (4.43) 11 (3.96) 52 (4.41) 7 (5.69) 88 (5.00)
4 (2.20) 4 (3.42) 0 (0.00) 10 (0.63) 0 (0.00) 10 (0.85) 0 (0.00) 14 (0.80)
32 (17.58) 21 (17.95) 11 (16.92) 316 (20.01) 53 (19.06) 240 (20.37) 23 (18.70) 348 (19.76)
98 (53.85) 58 (49.57) 40 (61.54) 715 (45.28) 122 (43.88) 543 (46.10) 50 (40.65) 813 (46.17)
23 (12.64) 21 (17.95) 2 (3.08) 414 (26.22) 87 (31.29) 287 (24.36) 40 (32.52) 437 (24.82)
Some lesions spanned more than one anatomical location.
Table IV. The radiological features of the patients with ameloblastoma Radiolucency, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
Total
Unilocular
Multilocular
With impacted tooth
Mixed radiolucent-radiopaque, n (%)
127 71 56 979 199 707 73 1106
58 (45.67) 28 (39.44) 30 (53.57) 407 (41.57) 113 (56.78) 268 (37.91) 26 (35.62) 465 (42.04)
48 (37.80) 29 (40.85) 19 (33.93) 432 (44.13) 86 (43.22) 318 (44.98) 28 (38.36) 480 (43.40)
18 (14.17) 12 (16.90) 6 (10.71) 97 (9.91) 0 (0.00) 78 (11.03) 19 (26.03) 115 (10.40)
3 (2.36) 2 (2.82) 1 (1.79) 43 (4.39) 0 (0.00) 43 (6.08) 0 (0.00) 46 (4.16)
Fig. 1. Photomicrograph of granular cell pattern of ameloblastoma (hematoxylin and eosin stain, original magnification ⫻100).
study,18 87.8% in a Sri Lankan series,29 93.0% in a US data,10 93.5% in a Kenyan study,19 and 93.9% in a Thai study.17 In Asia, the ratio of mandible:maxilla ranged from 8.07:1.00 to 13.29:1.00, compared with 2.95:1.00 to 6.05:1.00 in North America. Sriram and Shetty13 reported the mandible:maxilla ratio as high as 18.1:1.0. They offered an explanation for that high ratio by the possible transfer of the often complex management of the maxillary ameloblastomas to physicians who specialize in the ear, nose, and throat. Most cases (46.17%) were located in the premolar/molar region of the mandible. This finding is consistent with studies by Sirichi-
Fig. 2. Photomicrographs of ameloblastoma: A, unicystic and B, desmoplastic (hematoxylin and eosin stain, original magnification ⫻100).
ORAL AND MAXILLOFACIAL PATHOLOGY 786 Dhanuthai et al.
OOOO June 2012
Table V. The histologic features of the patients with ameloblastoma Follicular
Plexiform
North 66 (26.40%) 31 (12.40%) America USA 36 (23.53%) 18 (11.76%) Canada 30 (30.93%) 13 (13.40%) Asia 291 (28.01%) 241 (23.20%) Korea 53 (25.24%) 54 (25.71%) Thailand 203 (27.03%) 162 (21.57%) Vietnam 35 (44.87%) 25 (32.05%) Total 357 (27.70%) 272 (21.10%)
Acanthomatous
Granular
6 (2.40%)
1 (0.40%)
7 (2.80%)
5 (3.27%) 1 (1.03%) 85 (8.18%) 22 (10.48%) 63 (8.39%) 0 (0.00%) 91 (7.06%)
1 (0.65%) 0 (0.00%) 25 (2.41%) 3 (1.43%) 22 (2.93%) 0 (0.00%) 26 (2.02%)
5 (3.27%) 2 (2.06%) 46 (4.43%) 6 (2.86%) 39 (5.19%) 1 (1.28%) 53 (4.11%)
tra and Dhiravarangkura,17 Kim and Jang,18 and Buchner et al.10 The reason why mandible, particularly the premolar/molar region, is the favored site for ameloblastoma is still unknown. However, Adeline and coworkers19 found that the angle-ramus region was the most common site of ameloblastoma. Of interest is the desmoplastic type, which has a well-documented predilection for the anterior portion of the jaws. In Asia, 33 cases (70.21%) of desmoplastic ameloblastoma occupied the anterior part of the jaws as compared with North America, where only 2 cases (28.57%) were localized there. In the present study, the number of patients presenting with unilocular radiolucencies was comparable with that of patients with multilocular radiolucencies. This is in accordance with the review conducted by Reichart and coworkers,14 but conflicting data still exist from other studies. Some studies revealed that multilocular radiolucencies outnumbered unilocular radiolucencies,17,19-21,28 whereas the contrary was true for others.16,18 In Asia, except Korea, multilocular radiolucency outnumbered unilocular radiolucency, whereas the contrary was true for North America. A previous study by Kim and Jang18 also supports this finding. Desmoplastic ameloblastoma has been reported to account for 0.9% to 13.0% of all ameloblastomas.23,30 In the present study, desmoplastic ameloblastoma accounted for 4.34% of all ameloblastomas. Desmoplastic ameloblastoma has been reported to have a distinctive mixed radiolucent-radiopaque radiographic pattern in 25.00% to 70.83% of the cases.23,31,32 In the present study, 31 cases (55.36%) of desmoplastic ameloblastoma appeared as a mixed radiolucent-radiopaque radiographic pattern. However, Effiom et al.30 reported that only 17.6% of their desmoplastic ameloblastoma cases had the mixed radiolucent-radiopaque radiographic pattern. Philipsen et al.33 proposed that metaplastic bone formation was responsible for the mixed radiolucent-radiopaque radiographic appearance. The etiopathogenesis of metaplastic bone formation is not fully elucidated. Itoh et al.34 suggested that tumor growth factor-beta from the ameloblastoma cells may be responsible for metaplastic bone deposition. On the
Desmoplastic Basal cell
Peripheral
Unicystic
Others
1 (0.40%) 33 (13.20%) 40 (16.00%) 65 (26.00%) 0 (0.00%) 1 (1.03%) 12 (1.15%) 11 (5.24%) 1 (0.13%) 0 (0.00%) 13 (1.01%)
17 (11.11%) 28 (18.30%) 43 (28.10%) 16 (16.49%) 12 (12.37%) 22 (22.68%) 22 (2.12%) 227 (21.85%) 90 (8.67%) 10 (4.76%) 51 (24.29%) 0 (0.00%) 7 (0.93%) 164 (21.84%) 90 (11.98%) 5 (6.41%) 12 (15.38%) 0 (0.00%) 55 (4.27%) 267 (20.71%) 155 (12.02%)
other hand, Li and colleagues23 contended that the radiolucent-radiopaque radiographic appearance of desmoplastic ameloblastoma was attributed to the density of the compressed odontogenic epithelium coupled with desmoplastic stroma and the residual bone, as desmoplastic ameloblastoma did not produce bone. This is especially true considering that ameloblastomas are derived from the enamel organ epithelium before the epithelial-mesenchymal induction takes place.35 Regarding the histopathologic features, the follicular and plexiform patterns were the 2 most common patterns, similar to previous reports.14,17,18,21 The follicular pattern by far is the most common histopathologic pattern encountered in most countries with the exception of Korea, where the plexiform pattern dominated by a small margin. This is also in accordance with a previous report from Korea.18 However, these various histopathologic features do not have significant bearing on behavior or prognosis and, quite often, multiple histopathologic variants are found within the same tumor.1,35 Peripheral ameloblastoma has been reported to account for 0.5% to 9.3% of all ameloblastomas.36-39 In the present study, peripheral ameloblastoma accounted for 4.27% of all ameloblastomas. The prevalence of peripheral ameloblastoma in North America was higher than that in Asia. The plausible explanation for this may be accounted for by that fact that peripheral ameloblastoma does not usually produce gross disfigurement. As a consequence, patients with peripheral ameloblastoma may not seek medical attention or the attending clinicians may misdiagnose peripheral ameloblastoma as other common benign mucosal lesions and discard the surgical specimens without submitting them for histopathologic examination. Another explanation may be an actual lower prevalence of peripheral ameloblastoma in Asia compared with that in North America owing to ethnic influence.
CONCLUSIONS Ameloblastoma is a benign, locally aggressive odontogenic tumor. It mostly affects patients in the third to the fifth decades of life, with no gender predilection. The mandible, especially the posterior part, is the site of predilection. Radiographically, ameloblastomas appear in
OOOO Volume 113, Number 6
equal frequency as multilocular or unilocular radiolucencies. The most common histopathologic pattern is the follicular pattern. In comparison to previous studies, minor differences in age, gender and radiographic features were noted. The clinicopathologic features of ameloblastomas from some countries in Asia differ from those in North America with respect to age, gender, and radiographic features. The differences may be partially accounted for by ethnic influences, accessibility to medical facilities, documentation, and the availability of data.
ORIGINAL ARTICLE Dhanuthai et al. 787
15.
16.
17.
18.
We thank all the staff from the participating institutes for their contributions to this research.
19.
REFERENCES
20.
1. Philipsen HP, Reichart P, Slootweg PJ, Slater LJ. Odontogenic tumours. In: Barnes L, Eveson JW, Reichart P, Sidransky D, editors. World Health Organization classification of tumors, pathology and genetics of head and neck tumors. Lyon: International Agency for Research on Cancer; 2005. p. 283-328. 2. Waldron C. Odontogenic cysts and tumors. In: Neville BW, Damm DD, Allen CM, Bouquot JE, editors. Oral and maxillofacial pathology. St. Louis: W. B. Saunders; 2009. p. 678-740. 3. Ide F, Mishima K, Miyazaki Y, Saito I, Kusama K. Peripheral ameloblastoma in-situ: an evidential fact of surface epithelium origin. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:763-7. 4. 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. 5. Daley TD, Wysocki GP, Pringle GA. Relative incidence of odontogenic tumors and oral and jaw cysts in a Canadian population. Oral Surg Oral Med Oral Pathol 1994;77:276-80. 6. Gupta B, Ponniah I. The pattern of odontogenic tumors in a government teaching hospital in the southern Indian state of Tamil Nadu. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:e32-9. 7. Mothes P, Kreusch T, Harms D, Donath K, Schmelzle R. Frequency of odontogenic tumors in the growth period. Dtsch Zahnarztl Z 1991;46:18-9. 8. Tamme T, Soots M, Kulla A, Karu K, Hanstein SM, Sokk A, et al. Odontogenic tumours, a collaborative retrospective study of 75 cases covering more than 25 years from Estonia. J Craniomaxillofac Surg 2004;32:161-5. 9. Simon EN, Stoelinga PJ, Vuhahula E, Ngassapa D. Odontogenic tumours and tumour-like lesions in Tanzania. East Afr Med J 2002;79:3-7. 10. Buchner A, Merrell PW, Carpenter WM. Relative frequency of central odontogenic tumors: a study of 1,088 cases from Northern California and comparison to studies from other parts of the world. J Oral Maxillofac Surg 2006;64:1343-52. 11. Jing W, Xuan M, Lin Y, Wu L, Liu L, Zheng X, et al. Odontogenic tumours: a retrospective study of 1642 cases in a Chinese population. Int J Oral Maxillofac Surg 2007;36:20-5. 12. Arotiba JT, Ogunbiyi JO, Obiechina AE. Odontogenic tumours: a 15-year review from Ibadan, Nigeria. Br J Oral Maxillofac Surg 1997;35:363-7. 13. Sriram G, Shetty RP. Odontogenic tumors: a study of 250 cases in an Indian teaching hospital. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:e14-21. 14. Reichart PA, Philipsen HP, Sonner S. Ameloblastoma: biological
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32. 33.
34.
profile of 3677 cases. Eur J Cancer B Oral Oncol 1995;31B: 86-99. Dodge OG. Tumors of the jaw, odontogenic tissues and maxillary antrum (excluding Burkitt lymphoma) in Uganda Africans. Cancer 1965;18:205-15. Zhang J, Gu Z, Jiang L, Zhao J, Tian M, Zhou J, Duan Y. Ameloblastoma in children and adolescents. Br J Oral Maxillofac Surg 2010;48:549-54. Sirichitra V, Dhiravarangkura P. Intrabony ameloblastoma of the jaws. An analysis of 147 Thai patients. Int J Oral Surg 1984;13:187-93. Kim SG, Jang HS. Ameloblastoma: a clinical, radiographic, and histopathologic analysis of 71 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;91:649-53. Adeline VL, Dimba EA, Wakoli KA, Njiru AK, Awange DO, Onyango JF, et al. Clinicopathologic features of ameloblastoma in Kenya: a 10-year audit. J Craniofac Surg 2008;19:1589-93. Arotiba GT, Ladeinde AL, Arotiba JT, Ajike SO, Ugboko VI, Ajayi OF. Ameloblastoma in Nigerian children and adolescents: a review of 79 cases. J Oral Maxillofac Surg 2005;63:747-51. Fregnani ER, da Cruz Perez DE, de Almeida OP, Kowalski LP, Soares FA, de Abreu Alves F. Clinicopathological study and treatment outcomes of 121 cases of ameloblastomas. Int J Oral Maxillofac Surg 2010;39:145-9. MacDonald-Jankowski DS, Yeung R, Lee KM, Li TK. Ameloblastoma in the Hong Kong Chinese. Part 2: systematic review and radiological presentation. Dentomaxillofac Radiol 2004;33: 141-51. Li B, Long X, Wang S, Cheng Y, Chen X. Clinical and radiologic features of desmoplastic ameloblastoma. J Oral Maxillofac Surg 2011;69:2173-85. Ueno S, Nakamura S, Mushimoto K, Shirasu R. A clinicopathologic study of ameloblastoma. J Oral Maxillofac Surg 1986;44: 361-5. Takata T, Miyauchi M, Ito H, Ogawa I, Kudo Y, Zhao M, et al. Clinical and histopathological analyses of desmoplastic ameloblastoma. Pathol Res Pract 1999;195:669-75. Ledesma-Montes C, Mosqueda-Taylor A, Carlos-Bregni R, de León ER, Palma-Guzmán JM, Páez-Valencia C, Meneses-García A. Ameloblastomas: a regional Latin-American multicentric study. Oral Dis 2007;13:303-7. Chidzonga MM, Lopez Perez VM, Portilla Alvarez AL. Ameloblastoma: the Zimbabwean experience over 10 years. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:38-41. Dhanuthai KCS, Phattarataratip E, Rojanawatsirivej S. A retrospective study of 486 cases of ameloblastomas. J Dent Assoc Thai 2003;53:349-56. Darshani Gunawardhana KS, Jayasooriya PR, Rambukewela IK, Tilakaratne WM. A clinico-pathological comparison between mandibular and maxillary ameloblastomas in Sri Lanka. J Oral Pathol Med 2010;39:236-41. Effiom OA, Odukoya O. Desmoplastic ameloblastoma: analysis of 17 Nigerian cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;111:e27-31. Black CC, Addante RR, Mohila CA. Intraosseous ameloblastoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:585-92. Sun ZJ, Wu YR, Cheng N, Zwahlen RA, Zhao YF. Desmoplastic ameloblastoma—a review. Oral Oncol 2009;45:752-9. Philipsen HP, Ormiston IW, Reichart PA. The desmo- and osteoplastic ameloblastoma. Histologic variant or clinicopathologic entity? Case reports. Int J Oral Maxillofac Surg 1992;21:352-7. Itoh Y, Nakahara H, Itoh R, Ito A, Satou T. Osteoplastic amelo-
ORAL AND MAXILLOFACIAL PATHOLOGY 788 Dhanuthai et al.
35. 36.
37.
38.
blastoma: A case report and literature review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011 (in press). Said-Al-Naief N. Odontogenic tumors for general pathologists. Adv Exp Med Biol 2005;563:148-64. 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 Radiology Endod 2005;99:191-5. Ochsenius G, Ortega A, Godoy L, Peñafiel C, Escobar E. Odontogenic tumors in Chile: a study of 362 cases. J Oral Pathol Med 2002;31:415-20. Saghravanian N, Jafarzadeh H, Bashardoost N, Pahlavan N, Shirinbak I. Odontogenic tumors in an Iranian population: a 30-year evaluation. J Oral Sci 2010;52:391-6.
OOOO June 2012 39. Buchner A, Merrell PW, Carpenter WM. Relative frequency of peripheral odontogenic tumors: a study of 45 new cases and comparison with studies from the literature. J Oral Pathol Med 2006;35:385-91. Reprint requests: Kittipong Dhanuthai, DDS, MSc Department of Oral Pathology Faculty of Dentistry Chulalongkorn University Pathumwan District Bangkok 10330, Thailand [email protected]
Ameloblastoma: a multicentric study Kittipong Dhanuthai, DDS, MSc,a Soranun Chantarangsu, DDS, PhD,a Somsri Rojanawatsirivej, DDS, MS,a Ekarat Phattarataratip, DDS, PhD,a Mark Darling, BChD, MChD,b Linda Jackson-Boeters, MLT,b Nasser Said-Al-Naief, DDS, MS,c Hong-In Shin, DDS, PhD,d Chang-Hyeong An, DDS, PhD,e Nguyen Thi Hong, DDS, PhD,f Phan Huynh An, DDS, PhD,g Watcharaporn Thosaporn, DDS, MS,h Aroonwan Lam-ubol, DDS, PhD,i and Ajiravudh Subarnbhesaj, DDS, MS,j Bangkok, Chiang Mai and Khon Kaen, Thailand; Ontario, Canada; San Francisco, California, USA; Daegu, Korea; and Ho Chi Minh City, Vietnam CHULALONGKORN UNIVERSITY, UNIVERSITY OF WESTERN ONTARIO, UNIVERSITY OF THE PACIFIC, KYUNGPOOK NATIONAL UNIVERSITY, UNIVERSITY OF MEDICINE AND PHARMACY, CHIANGMAI UNIVERSITY, SRINAKHARINWIROT UNIVERSITY, AND KHON KAEN UNIVERSITY
Objective. The objective of this study was to supplement the current ameloblastoma database by reporting the clinicopathologic features of ameloblastoma from Asia and North America. Materials and Methods. Biopsy records of the participating institutes were reviewed for lesions diagnosed as ameloblastoma during the years 1993 to 2009. Slides were reclassified according to the World Health Organization Classification of Odontogenic Tumors in 2005. Clinical information and radiographic features were collected and analyzed. Results. The mean age of the patients ⫾ SD was 38.27 ⫾ 17.78 years; 662 patients (51.36%) were men. Mandible (84.26%) outnumbered maxilla and other locations combined in all countries. The number of multilocular radiolucencies (43.40%) was comparable with that of unilocular radiolucencies (42.04%). Follicular pattern was the most common histopathologic pattern (27.70%), followed by plexiform (21.10%) and unicystic pattern (20.71%), respectively. Conclusions. The clinicopathologic features of ameloblastomas in the present study show some similarities with previous studies; however, minor differences exist. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:782-788)
a
Department of Oral Pathology, Faculty of Dentistry, Chulalongkorn University, Bangkok, Thailand. b Department of Pathology, Schulich School of Medicine and Dentistry, University of Western Ontario, Ontario, Canada. c Oral & Maxillofacial Pathology Laboratory, Clinical Oral Pathology/Oral Medicine, Department of Pathology & Medicine, University of the Pacific, San Francisco, CA, USA. d Department of Oral Pathology, School of Dentistry, Kyungpook National University, Daegu, Korea. e Department of Oral and Maxillofacial Radiology, School of Dentistry, Kyungpook National University, Daegu, Korea. f Department of Oral Pathology, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam. g Department of Oral Surgery, University of Medicine and Pharmacy, Ho Chi Minh City, Vietnam. h Department of Oral Biology and Diagnostic Sciences, Faculty of Dentistry, Chiangmai University, Chiang Mai, Thailand. i Formerly, Department of Oral Pathology, Radiology and Medicine, The University of Iowa; currently, Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, Srinakharinwirot University, Bangkok, Thailand. j Department of Oral Diagnosis, Khon Kaen University, Khon Kaen, Thailand. Received for publication Oct 4, 2011; returned for revision Jan 4, 2012; accepted for publication Jan 13, 2012. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.oooo.2012.01.011
782
Ameloblastoma is a benign, locally aggressive odontogenic tumor that has a close histopathologic resemblance to the enamel organ. It belongs to the group of tumors arising from odontogenic epithelium with mature fibrous stroma without odontogenic ectomesenchyme according to the World Health Organization (WHO) Classification of Odontogenic Tumors in 2005. Ameloblastoma is divided into 4 types: unicystic, solid/ multicystic, desmoplastic, and peripheral.1 It is believed to originate from remnants of tooth-forming apparatus, such as developing enamel organ, odontogenic rests, reduced enamel epithelium and the epithelial lining of odontogenic cysts, especially dentigerous cysts, or from the basal epithelial cells of the oral mucosa.2,3 There have been several case series of ameloblastomas from several countries with geographic and/or racial variations. Ameloblastoma ranks as the most common odontogenic tumor in Asia and Africa, whereas odontoma is listed as the most common odontogenic tumor in Europe and America.4-12 The fact that odontomas are discovered during routine radiographic examinations and do not produce clinical symptoms may account for odontoma underreporting in the developing countries, as most patients in developing countries do not seek medical attention until their pathologies become symptomatic or grossly apparent.13 The average age of patients afflicted with ameloblastoma in industrialized countries was 39.1 years, whereas developing it was 27.7 years.14
OOOO Volume 113, Number 6
ORIGINAL ARTICLE Dhanuthai et al. 783
Table I. Age distribution of the patients with ameloblastoma Age, y
North America USA Canada Asia Korea Thailand Vietnam Total
Total
0-10
11-20
21-30
31-40
41-50
51-60
61-70
71-80
81-90
91-100
101-110
NS
Mean ⫾ SD
250 153 97 1039 210 751 78 1289
1 0 1 16 1 15 0 17
22 16 6 191 49 128 14 213
34 17 17 221 45 158 18 255
34 23 11 215 44 154 17 249
45 33 12 184 32 136 16 229
40 22 18 123 22 93 8 163
31 15 16 56 13 38 5 87
26 11 15 17 4 13 0 43
13 12 1 4 0 4 0 17
2 2 0 0 0 0 0 2
2 2 0 0 0 0 0 2
0 0 0 12 0 12 0 12
48.54 ⴞ 0.54 48.65 ⫾ 1.43 48.35 ⫾ 9.18 35.75 ⴞ 6.09 34.52 ⫾ 6.37 36.12 ⫾ 6.15 35.62 ⫾ 4.66 38.26 ⫾ 7.78
NS, not specified.
According to Dodge,15 the aging process may be accelerated in developing countries as a result of poor nutrition and health care. Gender and radiographic differences have also been reported among series.16-21 Only the mandibular predilection and 2 most common histopathologic patterns (follicular and plexiform) seem to be agreed on by most reported series. Since the study by Reichart and coworkers in 1995,14 there has been no large-scale case series of ameloblastoma. Most of the reported series of ameloblastoma from Asia are from China and Japan.4,11,16,22-25 There has been a paucity of information from other countries in Asia, such as Thailand and Vietnam, especially in the English-language literature. The objective of this study was to supplement the current ameloblastoma database by reporting the clinicopathologic features of ameloblastoma from Asia (Thailand, Vietnam, and Korea) and North America (Canada and the United States).
MATERIALS AND METHODS The biopsy records of the Department of Oral Pathology, Chulalongkorn University, Kyungpook National University, and University of Medicine and Pharmacy; Department of Oral Biology and Diagnostic Sciences, Chiangmai University; Department of Oral Diagnosis, Khon Kaen University; Department of Oral Pathology, Radiology and Medicine, University of Iowa; Department of Pathology, The University of Alabama at Birmingham and University of Western Ontario were reviewed for ameloblastomas diagnosed from 1993 to 2009. Hematoxylin and eosin–stained glass slides were reviewed and reclassified according to the current WHO criteria.1 Clinical and radiographic information was documented for each case. Maxillary intraosseous lesions were separated into 3 regions: anterior (midline to the distal surface of canine), posterior (mesial surface of the first premolar to the distal surface of the third molar), and tuberosity area. Similarly, mandibular tumors were separated into anterior (midline to the distal surface of canine); posterior (mesial surface of the first premolar to the distal surface of the third
molar); and angle, ramus, condyle, coronoid process. Lesions that occurred exclusively in soft tissue were so designated. Lesions encountered in locations other than the aforementioned ones were designated as “other.” Data collected were analyzed by SPSS version 13.0 (Chicago, IL). The Kruskal-Wallis and Mann-Whitney U tests were used to determine the association between clinical and pathologic parameters. A P value less than .05 was considered to be statistically significant. The ethical committee of the Faculty of Dentistry, Chulalongkorn University approved this research (no. 10/ 2009).
RESULTS Of the 143,712 total accessioned cases, 1289 cases (0.90%) were diagnosed as ameloblastoma. Ameloblastoma constituted from 0.14% (Canada) to 9.96% (Vietnam) of the total accessioned cases. In Asia, 1039 cases (4.64%) were diagnosed as ameloblastoma, whereas 250 cases (0.21%) were diagnosed as ameloblastoma in North America. The age of the patients in the present study ranged from 4 to 107 years with a mean ⫾ SD of 38.26 ⫾ 17.78 years. The mean age of patients afflicted with ameloblastoma in Asia was significantly lower than that in North America (P ⬍ .0001). The peak incidence varied from the second decade in Korea to the sixth decade in Canada. Overall, the peak incidence in Asia fell in the third decade compared with the fifth decade in North America. In all countries, the age of patients with unicystic ameloblastoma was significantly lower than that of solid/multicystic ameloblastoma (data not shown). The age distribution is shown in Table I. Of the 1289 cases of ameloblastoma in the present study, there were 662 males (51.36%) and 627 females (48.64%). The male-to-female ratio was 1.00:0.95, but the difference was not statistically significant (P ⫽ .343). There was an almost equal distribution between genders in Thailand and the United States. North America exhibited male predominance (P ⫽ .043), whereas Asia exhibited a slight male predominance, but the
ORAL AND MAXILLOFACIAL PATHOLOGY 784 Dhanuthai et al.
OOOO June 2012
Table II. Gender distribution of patients with ameloblastoma Total
Male
Female
250 153 97 1039 210 751 78 1289
141 (56.40) 81 (52.94) 60 (61.86) 521 (50.14) 116 (55.24) 371 (49.40) 34 (43.59) 662 (51.36)
109 (43.60) 72 (47.06) 37 (38.14) 518 (49.86) 94 (44.76) 380 (50.60) 44 (56.41) 627 (48.64)
The follicular pattern was the most common histopathologic pattern in most countries except Korea, which had almost equal distribution between follicular and plexiform patterns. The second most common histopathologic pattern for solid/multicystic ameloblastoma in North America was mixed follicular and plexiform pattern, closely followed by the pure plexiform pattern. On the other hand, the plexiform pattern was the second most common pattern in Asia, followed by the acanthomatous pattern. The histopathologic features of ameloblastoma are summarized in Table V.
difference was not statistically significant (P ⫽ .951). The gender distribution of ameloblastoma is shown in Table II. Ameloblastoma demonstrated a strong predilection for the mandible with the mandible-to-maxilla ratio as high as 13.29:1.00 in Korea. Mandible outnumbered maxilla and other locations combined in all countries. Soft tissue lesions were encountered in only 55 cases or 4.27% of the cases. These sites included gingiva, soft tissue of the tuberosity, retromolar pad, and edentulous areas. In the mandible, the posterior region was the predominant site of involvement in all countries, followed by the ramus, angle, and condyle in almost all countries except the United States and Canada in which the anterior region ranked as the second most common site. In the maxilla, the posterior site of region was the predilection in all countries. The anatomical distribution of ameloblastoma is shown in Table III. Radiographic data were not available in 183 cases (14.20%); therefore, the radiographic data were based on the data of the remaining 1106 cases. In general, the number of unilocular radiolucency cases was comparable to that of the multilocular counterpart. Radiographically, 480 cases (43.40%) exhibited multilocular radiolucency, 465 cases (42.04%) showed unilocular radiolucency, and 46 cases (4.16%) demonstrated a mixed radiolucent-radiopaque pattern. Radiolucencies associated with impacted teeth were encountered in 115 cases (10.40%). Another interesting finding was that the number of cases presenting as radiolucency associated with impacted teeth in North America was twice as high as that in Asia. Summary of the radiographic features is shown in Table IV. Histopathologically, most tumors (75.02%) were of solid/multicystic type (Figure 1). Unicystic, desmoplastic, and peripheral ameloblastomas accounted for 20.71%, 4.34%, and 4.27% of the cases, respectively (Figure 2, A and B). Of particular interest, the incidence of unicystic ameloblastoma was remarkably higher in Asia than in North America, whereas the opposite was true for peripheral ameloblastoma.
DISCUSSION In 1995, Reichart et al.14 reviewed the biological profile of 3677 ameloblastomas; the largest series so far. The age of patients in their series ranged from 4 to 92 years. Our data were in accordance with this range. The peak incidence in Asia fell in the third decade of life as compared with the fifth decade of life in North America. This was also in line with previous studies from Thailand,17 Korea,18 India,13 China,11 Kenya,19 and the United States.10 The explanation for this difference may reflect ethnic and possibly socioeconomic differences, as almost of the patients from Asia are of Asian descent, whereas in North America most are Whites. In addition, people in North America frequently have better access to medical care than people in developing countries, such as Thailand and Vietnam. North American patients are more likely to have regular dental visits and routine radiographic check-ups. As a consequence, oral lesion are detected at a younger age. The explanation for the lower average age of patients with ameloblastoma in developing countries compared with that of industrialized countries as being may reflect poor nutrition and reduced access to the health care system in developing countries, as proposed by Dodge’s concept15 may not be entirely applicable. Korea, for example, an industrialized country with a high standard of living and a well-respected health care system, has an average age of patients with ameloblastoma comparable with that of other Asian countries. In all countries, the age of patients with unicystic ameloblastoma was lower than that of patients with solid/multicystic ameloblastoma. This is in accordance with previous studies.14,18,26 The present study revealed an almost equal gender distribution, which is also in accordance with previous studies,14,21,27,28 with the exception of selective studies that demonstrated either male or female predominance.4,13,18,19 The mandible is the site of predilection for odontogenic tumors, including ameloblastoma. In the present study, 1087 cases (84.26%) of intraosseous ameloblastomas were encountered in the mandible. This figure is comparable with the 87.3% reported in a Korean
Gender, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
OOOO Volume 113, Number 6
ORIGINAL ARTICLE Dhanuthai et al. 785
Table III. The anatomical distribution of the patients with ameloblastoma Maxilla, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
Mandible, n (%)
Anterior
Posterior
Tuberosity
Anterior
Posterior
Ramus, angle, condyle
7 (3.85) 3 (2.56) 4 (6.15) 54 (3.42) 5 (1.80) 46 (3.90) 3 (2.44) 61 (3.46)
18 (9.89) 10 (8.55) 8 (12.31) 70 (4.43) 11 (3.96) 52 (4.41) 7 (5.69) 88 (5.00)
4 (2.20) 4 (3.42) 0 (0.00) 10 (0.63) 0 (0.00) 10 (0.85) 0 (0.00) 14 (0.80)
32 (17.58) 21 (17.95) 11 (16.92) 316 (20.01) 53 (19.06) 240 (20.37) 23 (18.70) 348 (19.76)
98 (53.85) 58 (49.57) 40 (61.54) 715 (45.28) 122 (43.88) 543 (46.10) 50 (40.65) 813 (46.17)
23 (12.64) 21 (17.95) 2 (3.08) 414 (26.22) 87 (31.29) 287 (24.36) 40 (32.52) 437 (24.82)
Some lesions spanned more than one anatomical location.
Table IV. The radiological features of the patients with ameloblastoma Radiolucency, n (%)
North America USA Canada Asia Korea Thailand Vietnam Total
Total
Unilocular
Multilocular
With impacted tooth
Mixed radiolucent-radiopaque, n (%)
127 71 56 979 199 707 73 1106
58 (45.67) 28 (39.44) 30 (53.57) 407 (41.57) 113 (56.78) 268 (37.91) 26 (35.62) 465 (42.04)
48 (37.80) 29 (40.85) 19 (33.93) 432 (44.13) 86 (43.22) 318 (44.98) 28 (38.36) 480 (43.40)
18 (14.17) 12 (16.90) 6 (10.71) 97 (9.91) 0 (0.00) 78 (11.03) 19 (26.03) 115 (10.40)
3 (2.36) 2 (2.82) 1 (1.79) 43 (4.39) 0 (0.00) 43 (6.08) 0 (0.00) 46 (4.16)
Fig. 1. Photomicrograph of granular cell pattern of ameloblastoma (hematoxylin and eosin stain, original magnification ⫻100).
study,18 87.8% in a Sri Lankan series,29 93.0% in a US data,10 93.5% in a Kenyan study,19 and 93.9% in a Thai study.17 In Asia, the ratio of mandible:maxilla ranged from 8.07:1.00 to 13.29:1.00, compared with 2.95:1.00 to 6.05:1.00 in North America. Sriram and Shetty13 reported the mandible:maxilla ratio as high as 18.1:1.0. They offered an explanation for that high ratio by the possible transfer of the often complex management of the maxillary ameloblastomas to physicians who specialize in the ear, nose, and throat. Most cases (46.17%) were located in the premolar/molar region of the mandible. This finding is consistent with studies by Sirichi-
Fig. 2. Photomicrographs of ameloblastoma: A, unicystic and B, desmoplastic (hematoxylin and eosin stain, original magnification ⫻100).
ORAL AND MAXILLOFACIAL PATHOLOGY 786 Dhanuthai et al.
OOOO June 2012
Table V. The histologic features of the patients with ameloblastoma Follicular
Plexiform
North 66 (26.40%) 31 (12.40%) America USA 36 (23.53%) 18 (11.76%) Canada 30 (30.93%) 13 (13.40%) Asia 291 (28.01%) 241 (23.20%) Korea 53 (25.24%) 54 (25.71%) Thailand 203 (27.03%) 162 (21.57%) Vietnam 35 (44.87%) 25 (32.05%) Total 357 (27.70%) 272 (21.10%)
Acanthomatous
Granular
6 (2.40%)
1 (0.40%)
7 (2.80%)
5 (3.27%) 1 (1.03%) 85 (8.18%) 22 (10.48%) 63 (8.39%) 0 (0.00%) 91 (7.06%)
1 (0.65%) 0 (0.00%) 25 (2.41%) 3 (1.43%) 22 (2.93%) 0 (0.00%) 26 (2.02%)
5 (3.27%) 2 (2.06%) 46 (4.43%) 6 (2.86%) 39 (5.19%) 1 (1.28%) 53 (4.11%)
tra and Dhiravarangkura,17 Kim and Jang,18 and Buchner et al.10 The reason why mandible, particularly the premolar/molar region, is the favored site for ameloblastoma is still unknown. However, Adeline and coworkers19 found that the angle-ramus region was the most common site of ameloblastoma. Of interest is the desmoplastic type, which has a well-documented predilection for the anterior portion of the jaws. In Asia, 33 cases (70.21%) of desmoplastic ameloblastoma occupied the anterior part of the jaws as compared with North America, where only 2 cases (28.57%) were localized there. In the present study, the number of patients presenting with unilocular radiolucencies was comparable with that of patients with multilocular radiolucencies. This is in accordance with the review conducted by Reichart and coworkers,14 but conflicting data still exist from other studies. Some studies revealed that multilocular radiolucencies outnumbered unilocular radiolucencies,17,19-21,28 whereas the contrary was true for others.16,18 In Asia, except Korea, multilocular radiolucency outnumbered unilocular radiolucency, whereas the contrary was true for North America. A previous study by Kim and Jang18 also supports this finding. Desmoplastic ameloblastoma has been reported to account for 0.9% to 13.0% of all ameloblastomas.23,30 In the present study, desmoplastic ameloblastoma accounted for 4.34% of all ameloblastomas. Desmoplastic ameloblastoma has been reported to have a distinctive mixed radiolucent-radiopaque radiographic pattern in 25.00% to 70.83% of the cases.23,31,32 In the present study, 31 cases (55.36%) of desmoplastic ameloblastoma appeared as a mixed radiolucent-radiopaque radiographic pattern. However, Effiom et al.30 reported that only 17.6% of their desmoplastic ameloblastoma cases had the mixed radiolucent-radiopaque radiographic pattern. Philipsen et al.33 proposed that metaplastic bone formation was responsible for the mixed radiolucent-radiopaque radiographic appearance. The etiopathogenesis of metaplastic bone formation is not fully elucidated. Itoh et al.34 suggested that tumor growth factor-beta from the ameloblastoma cells may be responsible for metaplastic bone deposition. On the
Desmoplastic Basal cell
Peripheral
Unicystic
Others
1 (0.40%) 33 (13.20%) 40 (16.00%) 65 (26.00%) 0 (0.00%) 1 (1.03%) 12 (1.15%) 11 (5.24%) 1 (0.13%) 0 (0.00%) 13 (1.01%)
17 (11.11%) 28 (18.30%) 43 (28.10%) 16 (16.49%) 12 (12.37%) 22 (22.68%) 22 (2.12%) 227 (21.85%) 90 (8.67%) 10 (4.76%) 51 (24.29%) 0 (0.00%) 7 (0.93%) 164 (21.84%) 90 (11.98%) 5 (6.41%) 12 (15.38%) 0 (0.00%) 55 (4.27%) 267 (20.71%) 155 (12.02%)
other hand, Li and colleagues23 contended that the radiolucent-radiopaque radiographic appearance of desmoplastic ameloblastoma was attributed to the density of the compressed odontogenic epithelium coupled with desmoplastic stroma and the residual bone, as desmoplastic ameloblastoma did not produce bone. This is especially true considering that ameloblastomas are derived from the enamel organ epithelium before the epithelial-mesenchymal induction takes place.35 Regarding the histopathologic features, the follicular and plexiform patterns were the 2 most common patterns, similar to previous reports.14,17,18,21 The follicular pattern by far is the most common histopathologic pattern encountered in most countries with the exception of Korea, where the plexiform pattern dominated by a small margin. This is also in accordance with a previous report from Korea.18 However, these various histopathologic features do not have significant bearing on behavior or prognosis and, quite often, multiple histopathologic variants are found within the same tumor.1,35 Peripheral ameloblastoma has been reported to account for 0.5% to 9.3% of all ameloblastomas.36-39 In the present study, peripheral ameloblastoma accounted for 4.27% of all ameloblastomas. The prevalence of peripheral ameloblastoma in North America was higher than that in Asia. The plausible explanation for this may be accounted for by that fact that peripheral ameloblastoma does not usually produce gross disfigurement. As a consequence, patients with peripheral ameloblastoma may not seek medical attention or the attending clinicians may misdiagnose peripheral ameloblastoma as other common benign mucosal lesions and discard the surgical specimens without submitting them for histopathologic examination. Another explanation may be an actual lower prevalence of peripheral ameloblastoma in Asia compared with that in North America owing to ethnic influence.
CONCLUSIONS Ameloblastoma is a benign, locally aggressive odontogenic tumor. It mostly affects patients in the third to the fifth decades of life, with no gender predilection. The mandible, especially the posterior part, is the site of predilection. Radiographically, ameloblastomas appear in
OOOO Volume 113, Number 6
equal frequency as multilocular or unilocular radiolucencies. The most common histopathologic pattern is the follicular pattern. In comparison to previous studies, minor differences in age, gender and radiographic features were noted. The clinicopathologic features of ameloblastomas from some countries in Asia differ from those in North America with respect to age, gender, and radiographic features. The differences may be partially accounted for by ethnic influences, accessibility to medical facilities, documentation, and the availability of data.
ORIGINAL ARTICLE Dhanuthai et al. 787
15.
16.
17.
18.
We thank all the staff from the participating institutes for their contributions to this research.
19.
REFERENCES
20.
1. Philipsen HP, Reichart P, Slootweg PJ, Slater LJ. Odontogenic tumours. In: Barnes L, Eveson JW, Reichart P, Sidransky D, editors. World Health Organization classification of tumors, pathology and genetics of head and neck tumors. Lyon: International Agency for Research on Cancer; 2005. p. 283-328. 2. Waldron C. Odontogenic cysts and tumors. In: Neville BW, Damm DD, Allen CM, Bouquot JE, editors. Oral and maxillofacial pathology. St. Louis: W. B. Saunders; 2009. p. 678-740. 3. Ide F, Mishima K, Miyazaki Y, Saito I, Kusama K. Peripheral ameloblastoma in-situ: an evidential fact of surface epithelium origin. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:763-7. 4. 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. 5. Daley TD, Wysocki GP, Pringle GA. Relative incidence of odontogenic tumors and oral and jaw cysts in a Canadian population. Oral Surg Oral Med Oral Pathol 1994;77:276-80. 6. Gupta B, Ponniah I. The pattern of odontogenic tumors in a government teaching hospital in the southern Indian state of Tamil Nadu. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:e32-9. 7. Mothes P, Kreusch T, Harms D, Donath K, Schmelzle R. Frequency of odontogenic tumors in the growth period. Dtsch Zahnarztl Z 1991;46:18-9. 8. Tamme T, Soots M, Kulla A, Karu K, Hanstein SM, Sokk A, et al. Odontogenic tumours, a collaborative retrospective study of 75 cases covering more than 25 years from Estonia. J Craniomaxillofac Surg 2004;32:161-5. 9. Simon EN, Stoelinga PJ, Vuhahula E, Ngassapa D. Odontogenic tumours and tumour-like lesions in Tanzania. East Afr Med J 2002;79:3-7. 10. Buchner A, Merrell PW, Carpenter WM. Relative frequency of central odontogenic tumors: a study of 1,088 cases from Northern California and comparison to studies from other parts of the world. J Oral Maxillofac Surg 2006;64:1343-52. 11. Jing W, Xuan M, Lin Y, Wu L, Liu L, Zheng X, et al. Odontogenic tumours: a retrospective study of 1642 cases in a Chinese population. Int J Oral Maxillofac Surg 2007;36:20-5. 12. Arotiba JT, Ogunbiyi JO, Obiechina AE. Odontogenic tumours: a 15-year review from Ibadan, Nigeria. Br J Oral Maxillofac Surg 1997;35:363-7. 13. Sriram G, Shetty RP. Odontogenic tumors: a study of 250 cases in an Indian teaching hospital. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:e14-21. 14. Reichart PA, Philipsen HP, Sonner S. Ameloblastoma: biological
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32. 33.
34.
profile of 3677 cases. Eur J Cancer B Oral Oncol 1995;31B: 86-99. Dodge OG. Tumors of the jaw, odontogenic tissues and maxillary antrum (excluding Burkitt lymphoma) in Uganda Africans. Cancer 1965;18:205-15. Zhang J, Gu Z, Jiang L, Zhao J, Tian M, Zhou J, Duan Y. Ameloblastoma in children and adolescents. Br J Oral Maxillofac Surg 2010;48:549-54. Sirichitra V, Dhiravarangkura P. Intrabony ameloblastoma of the jaws. An analysis of 147 Thai patients. Int J Oral Surg 1984;13:187-93. Kim SG, Jang HS. Ameloblastoma: a clinical, radiographic, and histopathologic analysis of 71 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;91:649-53. Adeline VL, Dimba EA, Wakoli KA, Njiru AK, Awange DO, Onyango JF, et al. Clinicopathologic features of ameloblastoma in Kenya: a 10-year audit. J Craniofac Surg 2008;19:1589-93. Arotiba GT, Ladeinde AL, Arotiba JT, Ajike SO, Ugboko VI, Ajayi OF. Ameloblastoma in Nigerian children and adolescents: a review of 79 cases. J Oral Maxillofac Surg 2005;63:747-51. Fregnani ER, da Cruz Perez DE, de Almeida OP, Kowalski LP, Soares FA, de Abreu Alves F. Clinicopathological study and treatment outcomes of 121 cases of ameloblastomas. Int J Oral Maxillofac Surg 2010;39:145-9. MacDonald-Jankowski DS, Yeung R, Lee KM, Li TK. Ameloblastoma in the Hong Kong Chinese. Part 2: systematic review and radiological presentation. Dentomaxillofac Radiol 2004;33: 141-51. Li B, Long X, Wang S, Cheng Y, Chen X. Clinical and radiologic features of desmoplastic ameloblastoma. J Oral Maxillofac Surg 2011;69:2173-85. Ueno S, Nakamura S, Mushimoto K, Shirasu R. A clinicopathologic study of ameloblastoma. J Oral Maxillofac Surg 1986;44: 361-5. Takata T, Miyauchi M, Ito H, Ogawa I, Kudo Y, Zhao M, et al. Clinical and histopathological analyses of desmoplastic ameloblastoma. Pathol Res Pract 1999;195:669-75. Ledesma-Montes C, Mosqueda-Taylor A, Carlos-Bregni R, de León ER, Palma-Guzmán JM, Páez-Valencia C, Meneses-García A. Ameloblastomas: a regional Latin-American multicentric study. Oral Dis 2007;13:303-7. Chidzonga MM, Lopez Perez VM, Portilla Alvarez AL. Ameloblastoma: the Zimbabwean experience over 10 years. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:38-41. Dhanuthai KCS, Phattarataratip E, Rojanawatsirivej S. A retrospective study of 486 cases of ameloblastomas. J Dent Assoc Thai 2003;53:349-56. Darshani Gunawardhana KS, Jayasooriya PR, Rambukewela IK, Tilakaratne WM. A clinico-pathological comparison between mandibular and maxillary ameloblastomas in Sri Lanka. J Oral Pathol Med 2010;39:236-41. Effiom OA, Odukoya O. Desmoplastic ameloblastoma: analysis of 17 Nigerian cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011;111:e27-31. Black CC, Addante RR, Mohila CA. Intraosseous ameloblastoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:585-92. Sun ZJ, Wu YR, Cheng N, Zwahlen RA, Zhao YF. Desmoplastic ameloblastoma—a review. Oral Oncol 2009;45:752-9. Philipsen HP, Ormiston IW, Reichart PA. The desmo- and osteoplastic ameloblastoma. Histologic variant or clinicopathologic entity? Case reports. Int J Oral Maxillofac Surg 1992;21:352-7. Itoh Y, Nakahara H, Itoh R, Ito A, Satou T. Osteoplastic amelo-
ORAL AND MAXILLOFACIAL PATHOLOGY 788 Dhanuthai et al.
35. 36.
37.
38.
blastoma: A case report and literature review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011 (in press). Said-Al-Naief N. Odontogenic tumors for general pathologists. Adv Exp Med Biol 2005;563:148-64. 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 Radiology Endod 2005;99:191-5. Ochsenius G, Ortega A, Godoy L, Peñafiel C, Escobar E. Odontogenic tumors in Chile: a study of 362 cases. J Oral Pathol Med 2002;31:415-20. Saghravanian N, Jafarzadeh H, Bashardoost N, Pahlavan N, Shirinbak I. Odontogenic tumors in an Iranian population: a 30-year evaluation. J Oral Sci 2010;52:391-6.
OOOO June 2012 39. Buchner A, Merrell PW, Carpenter WM. Relative frequency of peripheral odontogenic tumors: a study of 45 new cases and comparison with studies from the literature. J Oral Pathol Med 2006;35:385-91. Reprint requests: Kittipong Dhanuthai, DDS, MSc Department of Oral Pathology Faculty of Dentistry Chulalongkorn University Pathumwan District Bangkok 10330, Thailand [email protected]