BASIC AND PATIENT-ORIENTED RESEARCH J Oral Maxillofac Surg 64:1010-1014, 2006
Ameloblastoma: A Surgeon’s Dilemma Dinaz Ghandhi, BDS, FDSRCS,* Ashraf F. Ayoub, PhD, FDSRCS, FDSRCPS, MDS, BDS,† M. Anthony Pogrel, MD, DDS,‡ Gordon MacDonald, BDS, PhD, FDSRCPS,§ Laetitia M. Brocklebank, BDS, MScFRACDS, FDSRCPS,¶ and Khursheed F. Moos, MBBS, BDS, FRCSE, FDSRCS, FDSRCPS储 Purpose: To investigate whether there were any significant differences in the mode of presentation,
treatment, and outcome of patients presenting with a primary diagnosis of ameloblastoma in Glasgow, Scotland and San Francisco, CA. Materials and Methods: All cases of ameloblastoma seen in both institutions between January 1, 1980 and December 31, 1999 were included in this study. Mode of presentation, radiographic appearance, histologic appearance, treatment, and follow-up were recorded. Results: There were no significant differences in the clinical features on presentation (swelling, followed by pain, and altered sensation), the radiographic appearance (unilocular approximately 30% and multilocular 70%), or management with either local treatment (enucleation and/or curettage in just over 50% of cases) or radical treatment (a form of resection in under 50%) in the 50 cases included in this study. Primary care by conservative treatment led to a recurrence in approximately 80% of cases and this included cases of unicystic ameloblastoma. Conclusion: The mode of presentation, diagnosis, and management of the ameloblastoma was remarkably similar in Glasgow and San Francisco. The recurrence rate following local enucleation and curettage was unacceptably high, and this included the cases of unicystic ameloblastoma, which should be treated more aggressively than has been recommended in the past. © 2006 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 64:1010-1014, 2006
*Assistant Professor Oral and Maxillofacial Surgery, Jinnah Medical and Dental College, Karachi, Pakistan. †Professor/Honorary Consultant in Oral and Maxillofacial Surgery, University of Glasgow, and Head of Biotechnology and Craniofacial Research Section, Glasgow Dental Hospital and School, Glasgow, United Kingdom. ‡Professor of Oral and Maxillofacial Surgery, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of California, San Francisco, CA. §Late Professor of Oral Pathology, University of Glasgow, Glasgow Dental Hospital and School, Glasgow, United Kingdom. ¶Senior Lecturer in Oral Radiology, University of Glasgow, Glasgow Dental Hospital and School, Glasgow, United Kingdom. 储Honorary Senior Research Fellow, Department of Oral and Maxillofacial Surgery, University of Glasgow, Glasgow Dental Hospital and School, Glasgow, United Kingdom. Address correspondence and reprint requests to Dr Ayoub: Glasgow Dental Hospital and School, 378 Sauchiehall St, Glasgow G2 3JZ, UK; e-mail:
[email protected] © 2006 American Association of Oral and Maxillofacial Surgeons
0278-2391/06/6407-0004$32.00/0 doi:10.1016/j.joms.2006.03.022
Ameloblastoma is the most common odontogenic neoplasm affecting the jaws, yet it accounts for only 1% of all tumors of the maxilla and mandible1-3 and 11% of all odontogenic tumors. It is an aggressive benign tumor of epithelial origin that may arise from the enamel organ, remnants of dental lamina, the lining of an odontogenic (dentigerous) cyst, or possibly from the basal epithelial cells of the oral mucosa. It often presents as a slow-growing, painless, swelling4 causing expansion of the cortical bone, perforation of the lingual and/or buccal plates, and infiltration of soft tissue. There is often delay in the diagnosis because of its slow-growing nature. The classification of ameloblastoma in the past was poorly defined.5,6 The current concept is to classify ameloblastomas as solid (or multicystic) classical intraosseous ameloblastoma or unicystic with peripheral subtypes. This classification has a direct bearing on the pathologic behavior of these variants. Ameloblastomas are notorious for their invasive growth and their tendency to recur. Treatment is primarily surgical.6 There has been some debate regarding the most appropriate method for surgical removal of the
1010
1011
GHANDHI ET AL
Table 1. DEMOGRAPHIC DATA FOR AMELOBLASTOMAS FROM THE WEST OF SCOTLAND AND SAN FRANCISCO
No. of patients Age range M:F Mandible:Maxilla Unilocular:Multilocular Unicystic ameloblastoma (postoperative histology)
West of Scotland
San Francisco
22 13–74 (mean, 41) 8:14 18:4 8:14 5
28 14–83 (mean, 32) 15:13 26:2 7:21 4
Ghandhi et al. Ameloblastoma: A Surgeon’s Dilemma. J Oral Maxillofac Surg 2006.
tumor.7 These range from conservative8-10 to radical11-13 modes of treatment. The conservative approach includes enucleation, curettage, and cryosurgery. The more radical treatment involves marginal resection, segmental resection, or composite resection.14 There is a lack of consensus over the most appropriate treatment modality. Solid or multicystic variants of ameloblastoma are locally aggressive and recur if inadequately excised. On the other hand, the unicystic ameloblastoma first described by Robinson and Martinez15 in 1977 has been regarded as a separate variant. In early reports it was considered less aggressive and a conservative approach was recommended by many authors.2,15,16 There are differences in behavior between lesions that are basically unicystic that show intramural proliferation, and those that, in addition, contain tumor nodules in the fibrous capsule, because they may have a greater tendency to recur.5,17 This 2-center retrospective study compares the management of ameloblastomas in the West of Scotland with that at the University of California, San Francisco (UCSF). The purpose of this study was to evaluate the treatment of the ameloblastoma in relation to the biologic behavior of the variants over a 20-year period.
Patients and Methods All cases of ameloblastoma (n ⫽ 22) from the West of Scotland between January 1, 1980 and December 31, 1999 were reviewed. The histopathology reports were obtained from the Department of Oral Pathology, Glasgow Dental Hospital and School (Glasgow, UK). Similarly, 28 cases of ameloblastoma treated at UCSF were reviewed using copies of patients’ records, radiographs, and histopathology reports. All histology slides from both centers were subsequently reviewed by a single pathologist to confirm the original diagnosis. The demographic features obtained from these 2 centers were analyzed and the clinical findings, radiographic details, histologic variations, and surgical treatment were compared. Patients were reviewed 1 month after treatment to eval-
uate healing and local control, then every 6 months for 2 years, and every year afterwards. Each recurrence was histologically confirmed.
Results The basic data from each center is shown in Table 1. In the West of Scotland, of the 18 mandibular tumors, 2 were in the anterior region and 16 were in the body and ramus region. The principal finding in all patients was swelling. Thirteen patients complained of pain and 2 had symptoms of lip/facial numbness. Of the 5 unicystic lesions, 4 were treated by enucleation and 1 was radically excised. The recurrence rate for the unicystic lesions was 80%. In 1 case (Fig 1), the enucleation of unicystic ameloblastoma showed a recurrence at the socket of the extracted lower second molar, despite the radiographic appearance of bony infill at the site of the enucleated lesion (Fig 2). This case was successfully treated with subsequent mandibular resection. All the unicystic ameloblastomas which were treated conservatively recurred, except 1. In the solid/multicystic group, 7 patients were treated radically and 10 conservatively. There were no recurrences in the radically treated group. Among the conservative group, 8 of the 10 cases recurred. Recurrences occurred up to 14 years postoperatively. The length of follow-up ranged from 3 to 15 years. All the recurrent cases were treated with radical surgery. One case had a second recurrence and required further treatment, and this showed spread to the base of the skull. In the UCSF group of mandibular tumors, 8 were in the anterior mandible and 18 in the body and ramus region. Swelling was the principal finding in all patients. Six patients complained of pain and 3 had symptoms of lip/facial numbness. All 4 unicystic ameloblastomas were treated conservatively. Two recurred (50%), requiring radical treatment. Of the 24 solid or multicystic ameloblastomas, 13 were treated radically and 11 by enucleation. No radically treated cases recurred. Of those treated conservatively, 8 recurred (72%), 1 of them as late as 19 years from the date of primary surgery. The length of follow-up ranged from 1 to 21 years. Twenty of the 28 patients
1012
AMELOBLASTOMA: A SURGEON’S DILEMMA
sis for ameloblastoma is more dependent on the method of surgical treatment rather than the histologic type of the tumor. A high rate of recurrence was found in solid ameloblastomas treated conservatively; 80% in the West of Scotland and 78% in the UCSF. The reported recurrence rate for the solid ameloblastoma treated by enucleation or curettage ranged from 55% to 90%.6,18,19 The architectural pattern of the ameloblastoma is such that the border of the tumor within cancellous bone lies beyond the apparent macroscopic surface and the radiographic boundaries of the
FIGURE 1. Panoramic (A) and PA (B) views showing a unilocular cystic lesion (confirmed by aspiration biopsy) associated with an impacted third molar. Ghandhi et al. Ameloblastoma: A Surgeon’s Dilemma. J Oral Maxillofac Surg 2006.
received follow-up for more than 4 years. All the recurrent cases were treated radically. One case had a second recurrence and required further treatment, which was successful.
Discussion Treatment modalities for ameloblastomas are many and varied; they may be divided into conservative and radical therapies. This study suggests that the progno-
FIGURE 2. Panoramic (A) and PA (B) views showing bony infill at the site of the enucleated unicystic ameloblastoma, but also recurrence at the site of the extracted lower second molar. Ghandhi et al. Ameloblastoma: A Surgeon’s Dilemma. J Oral Maxillofac Surg 2006.
1013
GHANDHI ET AL
lesion. Therefore, complete removal can seldom be achieved by curettage alone. Both groups produced recurrence rates of 0% when radical surgery was the primary surgical treatment. With secondary radical surgery there is a well-recognized recurrence rate, but in our series only 1 case was clearly identified at each center. Segmental or composite resection produces good results, especially when carried out as a primary treatment.20 Once the tumor infiltrates the surrounding soft tissues, the rate of recurrence increases. This is mainly because of the difficulty in identifying the tumor boundary. Even extensive surgery cannot guarantee complete excision. Shatkin and Hoffmeister18 showed that continued under-treatment of ameloblastomas can lead to unresectable recurrences. In an early series of 13 cases, they reported a mortality of 30% from recurrent ameloblastomas. The unicystic ameloblastoma deserves special consideration on the basis of its clinical and radiologic appearance, its histopathology, and its response to treatment.15 This variant of ameloblastoma was reported to have shown less aggressive behavior than the conventional ameloblastoma.15 These tumors often occur as a painless swelling involving the posterior region of the mandible. Radiographically, they present primarily as a unilocular radiolucency and diagnosis is often made following histologic study of the enucleated specimen. A review of the English-language literature taken from case reports and reviews from 1977 to present disclosed a total of 123 cases of unicystic ameloblastoma, of which 18 had recurred (14.6%).15,16,21-30 The series of cases from the West of Scotland and UCSF that were identified as unicystic ameloblastoma had a recurrence rate, following conservative treatment, of 80% and 50%, respectively. This recurrence rate of unicystic ameloblastoma is not dissimilar to that of the multicystic type when treated conservatively, although the evidence in the literature suggests otherwise.31 Three histologic variants of unicystic ameloblastoma are described in the literature.5,17 In the first type, luminal ameloblastoma, the tumor is confined to the luminal surface of the cyst. In the second type, intraluminal ameloblastoma, tumor nodules project from the cystic lining into the lumen of the cyst. In the third type, mural ameloblastoma, the fibrous wall of the cyst is infiltrated with tumor nodules. The third type is considered the most aggressive of the 3 variants, with a recurrence rate as high as 35.7% reported in the literature for mural unicystic ameloblastomas.32 Different proliferating potentials exist between different areas of the unicystic ameloblastoma, in the form of a higher PCNA and Ki-67 labeling index, especially in the tumor nodules within the cystic wall.33 This
discovery provided a biological basis to recommend a more radical surgical excision as the treatment of choice for this subgroup of lesion. There would appear to be some difficulty in deciding which radiographically unicystic lesions should be biopsied before their removal. Based on our experience on the management of ameloblastomas, unicystic lesions would appear to require a more radical form of excision than enucleation on the basis of the size and site of the lesion. However, most surgeons would not agree that every cystic lesion should be biopsied. Analysis of aspirated fluid from a cystic lesion alone would not rule out a unicystic ameloblastoma. Therefore, it is reasonable to suggest a biopsy be carried out for a cystic lesion over 3 cm, particularly if radiographically it appeared to perforate the surrounding bone. Any cystic excision specimen should be subjected to multiple sections to exclude the presence of a mural ameloblastoma in the cyst lining. Their presence would indicate the appropriateness of a more aggressive surgical approach, possibly involving a second operation to remove surrounding bone and/or close long-term follow-up. The treatment of choice should be radical, ie, a marginal or segmental resection depending on the size of the lesion,34 to minimize the risk of any recurrence. The follow-up for all patients should be at least 10 years or as long as practically possible because recurrence has been reported even after 21 years.35 This study, although not providing a statistically significant number of cases for the evaluation of different treatment modalities, does indicate the aggressive nature of the so-called cystic ameloblastoma. In the past, this has perhaps been treated too conservatively, leading to recurrences. Despite the heterogeneity of the sample (Scottish vs Western American cases), treatment modalities and results of surgery were very similar from both centers. Acknowledgment The authors would like to dedicate this article to the memory of Prof G. MacDonald, the pathologist involved in this study, who sadly died after completing the article.
References 1. Gorlin RJ, Chaudhry AP, Pindborg JJ: Odontogenic tumors: Classification, histopathology clinical behaviour in man and domesticated animals. Cancer 14:73, 1961 2. Adekeye EO: Ameloblastoma of jaws: A survey of 109 Nigerian patients. J Oral Surg 38:36, 1980 3. Adekeye EO, Lavery KM: Recurrent ameloblastoma of the maxillofacial region. Clinical features and treatment. J Maxillofac Surg 14:153, 1986 4. Miyamoto CT, Brady LW, Markoe A, et al: Ameloblastoma of the jaw: Treatment with radiation therapy and a case report. Am J Clin Oncol 14:225, 1991 5. Gardner DG: A pathologist’s approach to the treatment of ameloblastoma. J Oral Maxillofac Surg 42:161, 1984
1014 6. Sehdev MK, Huvos AG, Strong EW, et al: Ameloblastoma of maxilla and mandible. Cancer 33:324, 1974 7. Muller H, Slootweg PJ: The ameloblastoma, the controversial approach to therapy. J Maxillofac Surg 13:79, 1985 8. Takahashi K, Miyauchi K, Sato K: Treatment of ameloblastoma in children. Br J Oral Maxillofac Surg 36:453, 1998 9. Nakamura N, Higuchi Y, Tashiro H, et al: Marsupialization of cystic ameloblastoma: A clinical and histopathologic study of the growth characteristics before and after marsupialization. J Maxillofac Surg 53:748, 1995 10. Shigeru U, Mushimoto K, Shirasu R: Prognostic evaluation of ameloblastoma based on histologic and radiographic typing. J Maxillofac Surg 47:11, 1989 11. Olaitan AA, Adeola DS, Adekeye EO: Ameloblastoma: Clinical features and management of 315 cases from Kaduna, Nigeria. J Craniomaxillofac Surg 21:351, 1993 12. Gardner DG, Pecak AMJ: The treatment of ameloblastoma based on pathologic and anatomic principles. Cancer 46:2514, 1980 13. Molla MR, Shaheed I, Shrestha P: Ameloblastoma a clinical study of 13 cases. Bangladesh Med Res Counc Bull 17:29, 1991 14. Bataineh AB: Effect of preservation of the inferior and posterior borders on recurrence of ameloblastomas of the mandible. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 90:155, 2000 15. Robinson L, Martinez MG: Unicystic ameloblastoma: A prognostically distinct entity. Cancer 40:2278, 1977 16. Shteyer A, Lustman J, Lewis-Epstein J: The mural ameloblastoma: A review of literature. J Oral Surg 36:866, 1978 17. Ackermann GL, Altini M, Shear M: The unicystic ameloblastoma: A clinicopathological study of 57 cases. J Oral Pathol 17:541, 1988 18. Shatkin S, Hoffmeister FS: Ameloblastoma: A rational approach to therapy. Oral Surg 20:421, 1965 19. Waldron CA: Ameloblastoma in perspective. J Oral Surg 24: 331, 1966 20. Sampson DE, Pogrel MA: Management of mandibular ameloblastoma: The clinical basis for a treatment algorithm. J Oral Maxillofac Surg 57:1074, 1999
AMELOBLASTOMA: A SURGEON’S DILEMMA 21. Josell SD, Reisken AB, Gross BD: Dentigerous cyst with mural ameloblastoma. J Am Dent Assoc 99:634, 1979 22. Rittersma J, Hadders HN, Feenstra K: Early unicystic ameloblastoma: Report of cases. J Oral Surg 37:747, 1979 23. Rapidis AD, Angelopoulos AP, Skouteris CA: Papanicolaou S. mural (intracystic) ameloblastoma. Int J Oral Surg 11:166, 1982 24. Marks R, Block M, Sanusi ID, et al: Unicystic ameloblastoma. Int J Oral Surg 12:186, 1983 25. Iscasson G, Andersson L, Forsslund H, et al: Diagnosis and treatment of unicystic ameloblastoma. Int J Oral Maxillofac Surg 15:759, 1986 26. Stoelinga PJ, Bronkhorst FB: The incidence, multiple presentation and recurrence of aggressive cyst of jaws. J Craniomaxillofac Surg 16:184, 1988 27. El-Abdin H, Ruprecht A: Unicystic ameloblastoma in Sudan. Int J Oral Maxillofac Surg 18:64, 1989 28. Punnia-Moorthy A: An unusual late recurrence of unicystic ameloblastoma. Br J Oral Maxillofac Surg 27:254, 1989 29. Cabrita L, Boleo-Tome J, Cunha AS: Intramural unilocular ameloblastoma. Stoma (Lisb) 2:23, 1990 30. Olaitan AA, Adekeye EO: Unicystic ameloblastoma of the mandible: A long-term follow-up. J Oral Maxillofac Surg 55:345, 1997 31. Li TJ, Kitano M, Arimura K, et al: Recurrence of unicystic ameloblastoma: A case report and review of the literature. Arch Pathol Lab Med 122:371, 1998 32. Li TJ, Wu YT, Yu SF, et al: Unicystic ameloblastoma: A clinicopathologic study of 33 Chinese patients. Am J Surg Pathol 24:1385, 2000 33. Li TJ, Browne RM, Matthews JB: Expression of proliferating cell nuclear antigen (PCNA) and Ki-67 in unicystic ameloblastoma. Histopathology 26:219, 1995 34. Pinsolle J, Michelet V, Coustal B, et al: Treatment of ameloblastoma of the jaws. Arch Otolaryngol Head Neck Surg 121:994, 1995 35. Thompson IO, Ferreira R, van Wyk CW: Recurrent unicystic ameloblastoma of the maxilla. Br J Oral Maxillofac Surg 31:180, 1993
