J Oral Maxillofac Surg 61:731-734, 2003
Case Report: Myocardial Metastasis of a Maxillary Malignant Ameloblastoma Roger A. Zwahlen, MD, DMD,* Peter Vogt, MD,† Frank S. Fischer, MD, DMD,‡ and Klaus W. Gra ¨ tz, MD, DMD§ In 1879, Falkson first described this odontogenic tumor arising from residues of the dental lamina,1,2 whereas the name ameloblastoma was introduced by Churchill in 1933.2,3 Ameloblastomas constitute approximately 1% of all cysts and tumors of the jaws.4 The occurrence in the mandible is 4 times higher than that in the maxilla.5,6 The average age of occurrence is in the third or fourth decade7; women and men are afflicted equally.5,8,9 In 1955, Small and Waldron4 showed that 47% of maxillary ameloblastomas occur in the molar region, 33% occur in the antrum and floor of the nose, 9% occur in both the premolar and the canine regions, and 2% occur in the palate. This slowly growing tumor with a benign histologic appearance shows a local invasiveness and a high incidence (50% to 72%) of local recurrence after therapy.3 Malignant features and metastasis are rare, exhibiting varying kinds of histology and clinical behavior.10-17 There remains much controversy regarding how to designate the rare malignant features of ameloblastomas.18-20 Formerly, any aggressive and metastazising ameloblastoma was included within the category of malignant ameloblastoma.2 Many authors,16,17,21 according to Slootweg and Mu ¨ ller,19 distinguish between the term ameloblastic carcinoma, describing any ameloblastoma with evident histopathologic features of malignancy in the primary, recurrent, or metastatic tumor regardless of metastasis, and the term malignant ameloblastoma, indicating those ameloblastomas
metastazising despite a benign cytology of both the primary and the metastatic lesion. We describe the case of a patient with an initially slowly growing, painless follicular ameloblastoma of the right maxilla. After an en bloc resection with tumor-free margins was achieved in 1987, it recurred in 1993 and grew to a large size within the midface up to the orbit and the skull base, showing histologically metaplastic squamous cell changes. Further surgical management was not successful. The patient died 13 years after the tumor’s onset. A myocardial metastasis revealed by the post mortem examination has not previously been reported in cases of maxillary ameloblastoma.
Report of a Case In 1987, a 44-year-old man with a 6-year history of an ulcer in the region of the right maxillary tuberosity was referred to the Department of Cranio-Maxillofacial Surgery of the University Hospital of Zurich with a histologically proved “follicular ameloblastoma.” The extraoral clinical and neurologic examinations did not show any abnormalities. Intraorally, the patient was edentulous. The right maxillary tuberosity presented with an ulcer of 30-mm maximum diameter. The patient underwent a tumor resection en bloc from the premolar region to the maxillary tuberosity including the right pterygoid process and curettage of the maxillary sinus. The histologic specimen showed a “follicular ameloblastoma”; the margins were free of tumor. After an incomplete follow-up, the patient presented in 1993 with hypesthesia of the right infraorbital nerve and proptosis of the right globe. The right nasal and auditory passages were partially occluded. No movement of the tympanic membrane could be detected. All other clinical and neurologic examinations were normal. Intraorally, ulcers were found on the palate. In March 1993, the patient underwent a right hemimaxillectomy, with resection of the mucous membrane of the right maxillary sinus, the right orbital floor, the retromaxillary tissue up to the skull base, the parapharyngeal tissue of the right side, the anterior portion of the soft palate, the prevertebral fascia, the anterior wall of the sphenoidal sinus, the ethmoidal complex, the lateral nasal wall, and nasal mucosa on the right side including the right inferior turbinate. All biopsy specimens taken intraoperatively were free of tumor. In March 1995, deafness occurred on the right side and was caused by fluid in the tympanum; in addition, the patient had memory disturbances. A biopsy specimen
Received from University Hospital Zurich, Zurich, Switzerland. *Consultant, Department of Cranio-Maxillofacial Surgery. †Consultant, Department of Pathology. ‡Consultant, Department of Cranio-Maxillofacial Surgery. §Head, Department of Cranio-Maxillofacial Surgery. Address correspondence and reprint requests to Dr Zwahlen: Department of Cranio-Maxillofacial Surgery, University Hospital of Zurich, Ra¨mistrasse 100, CH-8091 Zu ¨ rich, Switzerland; e-mail: [email protected]
© 2003 American Association of Oral and Maxillofacial Surgeons
MAXILLARY MALIGNANT AMELOBLASTOMA myocardial metastasis in the right ventricle of 25 mm maximum diameter (Fig 2). Two foci within the brain could not be precisely identified as metastases or adverse effects of radiotherapy.
FIGURE 1. Histopathologic specimen from March 1995 showing a follicular ameloblastoma with peripheral palisading and central stellate reticulum areas (broad arrow) and focal squamous cell metaplasia (narrow arrow) (hematoxylin and eosin stain, original magnification ⫻70).
from a swelling near the palatal mid-line showed a “follicular ameloblastoma with focal squamous cell metaplasia” (Fig 1). Computed tomography (CT) scans showed that the neoplasm in the left maxillary sinus was infiltrating the left maxilla. This was managed with a total maxillectomy. The sphenoidal sinus, the anterior portion of the left ethmoidal complex, and parapharyngeal soft tissue were resected via a combined intraoral and temporal approach. In 1996, CT scans and magnetic resonance imaging revealed infiltration of the skull base. Palliative radiotherapy, initially refused by the patient, was performed from February 19 through March 21, 1997, with a total dose of 41.4 Gy. Clinically, paresis of the right buccal branch of the facial nerve, a bilateral hypesthesia of the infraorbital nerves, and anesthesia of right mandibular nerve V3 were detected. In September 1998, a palliative tumor reduction in the right infraorbital region was performed via an intraoral approach. CT scans in October 1998 showed infiltration of the right mandible, of the right submandibular space, and of the right parotid region. Another palliative tumor reduction in the submandibular space was performed in December 1998. The specimens from the palliative tumor reductions in both September 1998 and December 1998 showed the histologic features of an ameloblastoma without any cytologic features of malignancy. In 1999, further infiltration of the skull base, including the petrous bone, was detected on CT scans. The patient complained of vertigo. CT scans taken in March 2000 after an ophthalmologic examination revealed infiltration of the optic chiasm. The radiation oncologist advised against a second course of radiotherapy. Another palliative tumor reduction with the same cytologic features was completed in August 2000. In December 2000 the patient was hospitalized on an emergency basis. He lost orientation, was confused, and behaved aggressively. Chest radiograph showed reduced transparency of the right apical pulmonary field, suspicious of metastasis. On December 21, 2000, the patient died. The post mortem examination revealed infiltration of the anterior and middle skull base, 2 metastases in the right upper pulmonary lobe of 15 and 2 mm maximum diameter, and 1
Ameloblastomas are rare odontogenic neoplasms.22 They have complicated histopathologic appearances with rather pleomorphic microscopic pictures, varying from one portion of the tumor to another.23 The lesion in the case presented arose in the posterior portion of the maxilla. As described by Biorklund et al in 197923 and Shatkin and Hoffmeister in 1965,24 the chief complaint of the patient was a painless vestibular ulcer. Because of the lack of early painful symptoms, the patient was seen by his dentist for 6 years after the lesion’s onset. The medullary bone structure of the maxilla is different from the compact bone structure of the mandible. Although medullary bone is invaded by neoplasm,4 compact bone is eroded rather than invaded.25 The absence of compact bone in the maxilla and the intimacy with the nasal cavity, paranasal sinuses, orbits, parapharyngeal tissues, and vital structures at the skull base mandate a clinical aspect of maxillary ameloblastomas totally different than that of mandible ameloblastomas. Joseph and Savage7 mentioned that the more abundant blood supply of the maxilla may also aid in hematogenous spread of the neoplasm. The initial lesion was totally removed via an en bloc resection with margins free of tumor. This technique, according to Shatkin and Hoffmeister,24 was proposed as the method of choice from the point of view of cure as well as of appearance and function, if available with a 10- to 15-mm margin of normal
FIGURE 2. Ameloblastic tubular and follicular structures within the myocardium (star). Heart muscle tissue of myocardium is shown (arrows) (hematoxylin and eosin stain, original magnification ⫻90).
ZWAHLEN ET AL
bone.21 Nevertheless the tumor recurred without cytologic features of malignancy and the diagnosis of a malignant ameloblastoma. Causes for the focal squamous cell metaplasia (Fig 1) are unknown. With the diagnosis based on histologic atypia and spread,22,26 approximately 2% of ameloblastomas are considered to be malignant. Before the development of spread, ameloblastomas show local recurrence.27 Infiltration of the orbit and skull base was reported.14 Madiedo et al28 showed that the maxilla is an unusual site of origin for ameloblastomas, especially in patients with metastasis, in whom the average time from onset to metastasis is 9.7 years (range, 1.5 to 40 years). The same authors28 considered the most common sites of metastasis to be the lung (75.9%), followed by regional lymph nodes (41.4%), pleura and vertebrae (17.2%), skull (10.3%), and liver, parotid gland, diaphragm, and soft tissue (6.9%); metastases to other bones, spleen, peritoneum, small intestines, and kidney are rare. Estrada et al29 attributed spread to the following conditions: 1) the tumor has existed for a long period of time, 2) the case is advanced, and 3) the patient has undergone surgery or radiotherapy more than once. Our patient had a metastazising malignant maxillary ameloblastoma. After an en bloc resection, local recurrence occurred 6 years and infiltration of the skull base occurred 9 years after onset of the tumor. The conditions given by Estrada et al29 favoring spread are fulfilled in this case. Metastases were found in the lungs, whereas the regional lymph nodes were free of tumor. The fact that no lymph node metastasis was found suggests hematogenous spread. Usually, curative treatment is adequately achieved with surgery. It is no longer indicated that ameloblastoma should be considered an innocent or nonaggressive entity and therefore narrow resection of the tumor is to be performed.30 The partial maxillectomy approached with a Le Fort I osteotomy with downfracture or with a en bloc resection with a 10- to 15-mm margin of bone including the entire affected alveolar ridge and hard palate, as well as the membrane of the entire maxillary sinus and lateral wall of the nose,6,21-23,31-35 is the current treatment of choice. The temporal approach to tumors related to or invading the retromaxillary space described by Obwegeser36 is the preferred one at the Department of Cranio-Maxillofacial Surgery of the University Hospital of Zurich. In this manner, tumors like that reported here can be radically removed. Together with an additional oral vestibular incision to resect the maxilla and a transconjunctival incision to access the orbital floor, the removal of the zygoma, of the maxilla including the orbital floor, and of retromaxillary tissues is possible. This approach, unlike most others, provides ample access to radical resection, without leav-
ing visible facial scars. Palliative radiotherapy, as occurred in the reported case, with or without cryotherapy is broadly accepted1,6,10,16,26 to achieve some decrease in tumor size and pain, whereas chemotherapy is neither effective to reduce tumor size nor palliative.26 To our knowledge this is the first reported case with histologically proved myocardial metastasis of a maxillary malignant ameloblastoma. We believe hematogenous spread of a maxillary tumor with rich blood supply caused this phenomenon.
References 1. Bredenkamp JK, Zimmerman MC, Mickel RA: Maxillary ameloblastoma. A potentially lethal neoplasm. Arch Otolaryngol Head Neck Surg 115:99, 1989 2. Shaw HJ, Katsikas DK: Ameloblastoma of the maxilla. A clinical study with four cases. J Laryngol Otol 87:873, 1973 3. Iordanidis S, Makos C, Dimitrakopoulos J, et al: Ameloblastoma of the maxilla. Case report. Aust Dent J 44:51, 1999 4. Small IA, Waldron CA: Ameloblastoma of the jaws. Oral Surg Oral Med Oral Pathol 8:281, 1955 5. Reichart PA, Philipsen HP: Odontogene Tumoren; Ameloblastome, in Rateitschak KH, Wolf HF (eds): Oralpathologie 10. Stuttgart, Germany, Thieme, 1999, pp 223-228 6. Chaudhuri P: Ameloblastoma of the upper jaw. J Laryngol Otol 89:457, 1975 7. Joseph BK, Savage NW: Maxillary ameloblastoma. Case report and review of the literature. Aust Dent J 37:98, 1992 8. Burkhardt A: Einfu ¨ hrung in die spezielle Pathologie, in Laissue J-A, Gebbers J-O (eds): Einfu ¨ hrung in die Spezielle Pathologie. Stuttgart, Germany, Gustav Fischer, 1991, p 199 9. Robinson HBG: Ameloblastoma: A survey of 379 cases from the litterature. Arch Pathol 23:831, 1937 10. Infante-Cossio P, Hernandez-Guisado JM, Fernandez-Machin P, et al: Ameloblastic carcinoma of the maxilla: A report of 3 cases. J Craniomaxillofac Surg 26:159, 1998 11. Andersen E, Bang G: Ameloblastic carcinoma of the maxilla. A case report. J Maxillofac Surg 14:338, 1986 12. Feun LG, Albores-Saavedra J, Savaraj N: Osteogenic sarcoma arising adjacent to a long-standing ameloblastoma. A case report. Oral Surg Oral Med Oral Pathol 71:77, 1991 13. Inoue N, Shimojyo M, Iwai H, et al: Malignant ameloblastoma with pulmonary metastasis and hypercalcemia. Report of an autopsy case and review of the literature. Am J Clin Pathol 90:474, 1988 14. Komisar A: Plexiform ameloblastoma of the maxilla with extension to the skull base. Head Neck Surg 7:172, 1984 15. Lee L, Maxymiw WG, Wood RE: Ameloblastic carcinoma of the maxilla metastatic to the mandible. Case report. J Craniomaxillofac Surg 18:247, 1990 16. Ueda M, Kosaki K, Kaneda T, et al: Doubling time of ameloblastoma metastasizing to the lung: Report of two cases. J Craniomaxillofac Surg 20:320, 1992 17. Corio RL, Goldblatt LI, Edwards PA, et al: Ameloblastic carcinoma: A clinicopathologic study and assessment of eight cases. Oral Surg Oral Med Oral Pathol 64:570, 1987 18. Pindborg JJ, Kramer IR, Torloni H: Odontogenic carcinomas, in Pindborg JJ, Kramer IR, Torloni H (eds): Histological Typing of Odontogenic Tumours, Jaw Cysts and Allied Lesions. Geneva, Switzerland, World Health Organization, 1971, pp 35-36 19. Slootweg PJ, Mu ¨ ller H: Malignant ameloblastoma or ameloblastic carcinoma. Oral Surg Oral Med Oral Pathol 57:168, 1984 20. Kramer IR, Pindborg JJ, Shear M: Histological Typing of Odontogenic Tumors (ed 2). International Histological Classification of Tumours, no 5. Berlin, Germany, Springer, 1992
734 21. Gardner DG, Pecak AM: The treatment of ameloblastoma based on pathologic and anatomic principles. Cancer 46: 2514, 1980 22. Daramola JO, Ajagbe HA, Oluwasanmi JO: Recurrent ameloblastoma of the jaws—A review of 22 cases. Plast Reconstr Surg 65:577, 1980 23. Biorklund A, Elner A, Snorradottir M: Ameloblastoma of the maxilla. Report of three cases. J Laryngol Otol 93:1105, 1979 24. Shatkin S, Hoffmeister FS: Ameloblastoma: A rational approach to therapy. Oral Surg Oral Med Oral Pathol 20:421, 1965 25. Kramer IRH: Ameloblastoma: A clinico-pathological appraisal. Br J Oral Surg 1:13, 1963 26. Sato K, Sudo S, Fukuya Y, et al: Maxillary ameloblastoma with intracranial invasion—Case report. Neurol Med Chir (Tokyo) 34:704, 1994 27. Brandenburg JH, Finch WW, Kirkham WR: Malignant ameloblastoma of the maxilla. Trans Am Acad Ophthalmol Otolaryngol 82:576, 1976 28. Madiedo G, Choi H, Kleinman JG: Ameloblastoma of the maxilla with distant metastases and hypercalcemia. Am J Clin Pathol 75:585, 1981
29. Estrada R, Zurawin R, Awe R: Mandibular ameloblastoma with long-standing pulmonary metastasis. South Med J 75:1414, 1982 30. Eichhorn T, Glanz H, Kleinsasser O: Ameloblastome des Oberkiefers. Bericht u ¨ ber 6 Fa¨lle und Literaturzusammenstellung. HNO 30:1, 1982 31. Sailer HF, Haers PE, Gra¨tz KW: The Le Fort I osteotomy as a surgical approach for removal of tumours of the midface. J Craniomaxillofac Surg 27:1, 1999 32. Symington OG, Caminiti MF: Le Fort 1 downfracture approach for the treatment of a posterior maxillary ameloblastoma. J Can Dent Assoc 61:1048, 1995 33. Crawley WA, Levin LS: Treatment of the ameloblastoma: A controversy. Cancer 42:357, 1978 34. Feinberg SE, Steinberg B: Surgical management of ameloblastoma. Current status of the literature. Oral Surg Oral Med Oral Pathol 81:383, 1996 35. Weissman BW, Wetli C: Ameloblastoma of the maxilla. South Med J 70:251, 1977 36. Obwegeser HL: Temporal approach to the TMJ, the orbit and the retromaxillary-infracranial region. Head Neck Surg 7:185, 1985