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Ameloblastomas of the jaws: Radiological diagnosis and follow-up
British Journal of Oral and Maxillofacial Surgery (1985) 23, 333-340 0 1985 The British Association of Oral and Maxillofacial Surgeons
AMELOBLASTOMAS
OF THE JAWS: RADIOLOGICAL AND FOLLOW-UP
DIAGNOSIS
BENNYO.IKO,M.D.,D.A.B.R.,‘~~ERNESTM.MYERS,M.D.,F.A.C.S.,‘ONYEKEWERE OGAN, M.B., ch.B., F.R.c.s., D.L.o.,~ and CHRISTIANU. CHINWUBA,M.D., D.A.B.R."
'
Department of Radiology,’ Howard University Hospital (HUH), and Divisions of Otorhinolaryngology ‘HUH, Washington D.C. (U.S.A.) & 3University College Hospital, Ihadan (Nigeria) Summary. Eleven of 57 tumours and cysts (19 per cent) seen at two major centres over a 4-year period were ameloblastomas, primary in eight and recurrent in three. Computed Tomography (CT) was the most sensitive imaging technique for detecting ameloblastomas. The radiological features were distinctive maxillary and mandibular pathology in primary cases and soft-tissue, maxillary sinus and asymmetrical deep tissue involvement in both primary and recurrent ameloblastomas. Following surgery and pathological confirmation. serial scans were combined with periodic clinical re-evaluation. We identified clinically occult recurrences in two cases and confirmed a clinically-suspected recurrence in one on the basis of the CT findings. Our protocol appears efficacious and is suggested for the necessary long-term follow-up in all pathologically verified ameloblastomas.
Introduction
The ameloblastoma remains a very controversial tumour of the jaws, perhaps more so than any other neoplasm found in the body (Mehlisch et al., 1972). Vitriolic arguments ramify every aspect of this disease; for instance there are no clear-cut criteria for the preference of either conservative surgery (Crawley & Levin, 1978; Huffmann & Thatcher, 1963; Stout et af., 1963), obligatory radical surgery (Azumi et al., 1981; Sehdev et al., 1974; Shatkin & Hoffmeister, 1965) or other forms of therapy (Fitzgerald et al., 1982; Sehdev et al., 1974; Tsaknis & Nelson, 1980). However, the great propensity of the ameloblastoma for local recurrence is generally recognised (Bahna, 1979; Daramola et al., 1980; Sehdev et al., 1974; Tsaknis & Nelson, 1980) and that this predisposes to both malignant transformation and distant metastases has been emphasised (Azumi et al., 1981; Buff et al., 1980; Ferlito et al., 1982). Histological patterns bear no relationship to the clinical behaviour of the tumour and even the electron microscope has not helped to clarify the histopathology or to predict the biological behaviour (Fitzgerald et al., 1982). The absolute necessity for long-term follow-up of all diagnosed ameloblastomas (Tsaknis & Nelson, 1980) is beyond question, and this has been by means of prolonged clinical surveillance. Unfortunately, clinical evaluation may be hampered by the complex anatomy of the region (Sehdev et al., 1974) and conventional radiology is of limited efficacy in evaluating subtle subcortical or soft-tissue changes that may herald a recurrence. A case of recurrent ameloblastoma demonstrating increased levels of serum calcium (Received
23 March
1984; accepted
17 December
1984)
Present Address: ‘Division of Neuroradiology. Department of Radiology, Bringham & Women’s Hospital, Harvard Medical School. Boston. Mass. U.S.A. of Radiology, College of Health Sciences, Corresponding Author: Dr Benny 0. Iko, ’ Department University of Port Harcourt, P.M.B. 5323, Port Harcourt, Nigeria.
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and urinary cyclic adenosine monophosphate (CAMP) which reverted to normal following surgery has been reported; this patient is being followed with serial measurements of serum calcium and urinary CAMP in the hope that, if the tumour recurs, it can be detected before it is large enough to be clinically evident (McGuirt et al., 1981). However, this case is most unusual, and a wider basis for detecting recurrence appears desirable. Computed tomography (CT) is currently the most sensitive imaging modality for detecting pathology in the head and neck region, but previous reports of the features of ameloblastomas were either anecdotal (Ames et ul., 1980; North & Rice, 1981) or limited to a single case report (Osborn et al., 1982). We therefore wish to review the CT features found in 11 cases. Surgery was performed on all cases, and a clinico-radiological protocol was developed for the follow-up. To our knowledge, the precise role of CT after surgery, has not been documented previously. Patients and Methods
Computed tomography is part of a standard protocol at Howard University Hospital (HUH) for the initial evaluation, staging and follow-up of operated jaw neoplasms. The HUH CT-Laboratory serviced the District of Columbia General Hospital during the study period 1978 to 1982. We saw 11 ameloblastomas (19 per cent) out of a total of 57 jaw tumours and cysts. Eight were primary cases, while three were recurrent, having undergone initial treatment elsewhere. The ages ranged from 28 to 72 years, average 47. There were eight females and three males, consisting of 10 Blacks and one ethnic Chinese. A thorough clinical evaluation preceded plain radiography in all cases (including intra-oral films in four cases), conventional linear tomography in five cases and CT in all cases. As our experience with CT increased, conventional tomography was omitted from the protocol. CT was performed on one of two available scanners, an Ohio Nuclear Whole Body with Fast Scan Modifications (22s) or a GE 8800 CT/T. The initial investigation consisted of plain CT, followed immediately by contrastenhanced scans, using a continuous drip infusion of Reno-M-Dip@ (meglumine diatrizoate). Transverse axial scans were obtained at 0.5 or 1 cm intervals through a plane parallel to the infraorbitomeatal (Reid) line; in selected cases, coronal images, multiplanar reformation and retrospective high-resolution analysis of raw scanning data were performed, as indicated by the tumour extension or artefacts arising from dental amalgams or restorations. Of the 57 tumours and cysts so examined, 42 had subsequent histopathological diagnoses, 11 of which were ameloblastomas. The CT features in the latter group were audited retrospectively. A baseline post-operative scan was performed 12 weeks following surgery and at 6-monthly intervals, usually through planes similar to those on the initial evaluation. A thorough clinical evaluation preceded all follow-up scans. The salient CT features of primary and recurrent ameloblastomas and stable post-maxillectomy status were selected at random. Representative
Case Reports
Case 1 (Primary Maxillary Ameloblastoma). A 32 year-old black female was seen for a painless swelling of the right upper jaw of 6 months’ duration. Physical examination revealed an exophytic and bossellated right gingivobuccal mass. Plain
AMELOBLASTOMAS
OF
Fig. Figure origin, lateral
THE
JAWS
1
l-Primary ameloblastoma in transverse axial projection. A right maxillary mass, medullary in expands and smoothly thins out the medial cortex, exerts a smooth pressure deformity on the sinus wall and shows a relatively homogenous character. The adjacent retromaxillary stripe (arrow) shows a focal infiltration in distinction to antral carcinoma or chrome smusttts
Fig. Fig.
3
2
Figure 2-Transverse axial CT. The recurrent lesion arises from the anterior inferior portion of the maxilla, invades and replaces the maxillary sinus and extends through the ethmoidal region into the nasal cavity. Posteriorly, the parapharyngeal fat stripe (arrow) and laterally and posteriorly the infratemporal boundary (arrow-heads) are obliterated. Compensatory expansion of the left Fossa of Rosenmuller can be contrasted with normal right (curved arrow). Figure 3-Normal post-maxillcctomy scan. Same patient as in Fig. 2, but at a slightly different level and on a different scanner, 4 years later. Residual swelling of the left cheek. The post-operative fibrotic changes are stable and regular. Note the nasomaxillary continuity from the previous surgery.
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radiography and linear tomography demonstrated a focal maxillary osteolysis while CT (Fig. 1) defined the origin, extent and relationship to vital structures and softtissues. A subsequent biopsy of the lesion confirmed an ameloblastoma. Radical surgery (hemimaxillectomy with reconstruction) was performed. The patient has been followed for 4.5 years, is clinically free of disease and has stable postmaxillectomy scans. Case 2 (Recurrent but Subclinical Ameloblastoma). A 61 year-old black female presented for a routine follow-up. She had undergone radical surgery, including a left rhinotomy with excision of the lateral nasal wall following the diagnosis of a maxillary ameloblastoma two years previously. Plain radiography and tomography demonstrated a homogeneous sclerotic lesion expanding the left maxilla while CT (Fig. 2) clearly defined the extent of the lesion. Transoral horizontal maxillectomy
Fig.
4
Figure &Axial CT, This recurrent mass had invaded and replaced the maxillary sinus. destroyed the lateral nasal wall and extended into the floor of the orbit (better seen on higher scans). The left styloid process was eroded, the pterygoid muscles replaced (compare the normal right side. P). the retropharyngeal space invaded and the tumour extended into the base of the skull. The soft tissue mass in the left cheek region (long arrow). was positive upon biopsy. The low density intratumoural lesions (black boxes) measured 20 Hounsfield Units (HU), and the whtte box 49 HU. The former is higher than for normal structures or water (and therefore more compatible with ‘radiation necrosis’ (or granulation tissue than infection) while the latter is 20-30 HU higher than normal structures (and therefore consistent with recurrent tumour). Concurrent right maxillary sinusitis with continuous mucoperosteal thickening (arrow heads) and pockets of residual sinus air.
AMELOBLASTOMAS
OF
THE
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was performed and the lesion excised in toto. This patient has now been followed for over 4 years and remains free of disease clinically, and radiologically (Fig. 3). Case 3 (Recurrent and Complicated Compound Ameloblustoma). A 41-year-old Vietnamese, ethnic Chinese, presented with a recurrent swelling of her left jaw, nasal obstruction and epistaxis. She gave a history of six previous resections of the left mandible for recurrences of ameloblastoma, the last of which was in Vietnam 10 years previously. Reconstruction of the mandible with a rib graft and a ‘fullcourse radiotherapy’ (total dosage unknown) had also been performed. CT (Fig. 4) and a CT-directed percutaneous biopsy of the soft-tissue lesion preceded surgery: a left Caldwell-Luc antrotomy and left hemimandibulectomy with reconstruction. Total excision was technically impossible. This patient has been followed for 1X months and her CT features appear stable. Of some interest is the clinical and radionuclide diagnosis of thyrotoxicosis which coincided with the latest recurrence and for which the patient is being treated. Results We found a high incidence of 11 (19%) ameloblastomas in a series of 57 jaw tumours and cysts. These were primary in eight and recurrent in three. One was compound mandibulo-maxillary, two maxillary and eight mandibular, most of the latter occurring in the retromolar trigone. The left jaw was involved in seven cases (64%). Most patients were females (73%) in the fourth decade, and black. The common presenting symptoms were painless, sometimes disfiguring swelling of the jaw of several months duration. ‘Eggshell crackling’ sensation on gentle pressure was noted in one case. Associated sinuses, pain, loose teeth and intra-oral ulcerations were infrequent and occurred more often in recurrent cases. The predominant histological pattern was follicular, with two cases of the plexiform, two of the mixed and one of the acanthomatous types. Plain radiography was positive in nine cases, equivocal in one and negative in the other. The mandibular lesions were often osteolytic, sometimes with an expansion of the lingual cortex and a multiloculated soap-bubble pattern. The maxillary lesions were well marginated and sclerotic in one case and lytic in the other, both expanding the cortex and were probably better appreciated on conventional linear tomography. Computed
Tomography
A total of 79 CT examinations were performed: 11 initial, 11 post-operative and 57 bi-annual scans; the longest follow-up is 4.5 years and the shortest 12 months. CT scanning in the transverse plane provided the most useful information, although reformation or direct coronal and reformatted sagittal images were in some cases also performed. Other modifications included ‘region of interest’ density analysis, and physiological manoeuvres during scanning to confirm fixation and enable analysis of the symmetry of the deep structures. The CT features were: (a) Bone changes. The case of primary maxillary ameloblastoma (Fig. 1) showed a monocystic cavity, arising from the maxillary tuberosity and adjacent to the molar area and extending towards the lingual aspect. The medullary cavity was widened, but with an apparent respect of the cortex. There was a focal pressure deformity of the adjacent maxillary sinus, and the extension into the sinus was homogenous. Recurrent maxillary ameloblastomas (Figs. 2 & 4) were predominantly osteo-
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sclerotic, but with areas of osteolysis. These findings were distinctive from other pathology occurring in our series, squamous cell carcinomas demonstrating irregular discontinuity of osseous structures, a wide zone of transition and a less uniform density, while chronic sinusitis (Fig. 4) showed a more diffuse but even mucosal thickening with areas of air density and lack of bone discontinuity. In the mandible, primary ameloblastoma presented as one of two patterns, either coarse and multilocular destruction with a rim of uninvolved cortex or more commonly uneven cortical sclerosis at the retromolar trigone. (b) Soft tissue changes. These were more common in recurrent cases (Fig. 4) and consisted of infiltration of the cheek, loss of fascial planes (retromaxillary, pre- or post-pterygoid bands) and of the muscles of mastication. (c) Deep structure changes. Intravenous contrast enhancement was useful in reconstructing landmarks. The extensions of tumour recurrence were identified based on comparison with the baseline scan, performed 14 days following surgery. Recurrent maxillary ameloblastoma may extend posteriorly into the pterygopalatine or infratemporal fossa (Figs. 2 & 4), superiorly into the orbit, medially and anteriorly into the ethmoido-nasal complex (Fig. 2). The mucosa, submucosal structures and ‘blind areas’ such as the lateral pharyngeal recesses (Figs. 2 & 4) were evaluated routinely. (d) Sinus opacification. This was an uncommon feature in primary cases and where it occurred was usually focal, airless and contiguous with a bony abnormality. However, tumour replacement of the maxillary sinus in recurrent cases was always associated with bony destruction (Figs. 2 & 4). Finally, the postoperative baseline scan (Fig. 3) was the most important reference study in detecting recurrent but subclinical disease (Fig. 2), or confirming clinically suspected recurrence (Fig. 4). Discussion
Although a rare tumour of the jaws (about 1% in most series) the ameloblastoma has been very widely reported (Adekeye, 1980; Connole, 1972; Robinson, 1937; Small & Waldron, 1955; Smith, 1968; Swinson, 1976 and many others). Therefore only a brief review of the interesting features in this series which are either unique or at variance with the majority of previous reports is appropriate. We are unable to explain the high incidence of 11 ameloblastomas in a series of 57 tumours (19%) or the 2.6:1 female to male ratio. These may be due to chance, or biased sampling. 91% of our patients were black; this may reflect the high proportion of Blacks in the Washington D.C. area (70 % or more) and the catchment population of the two referral centres. Plain radiography was positive in most cases, but its usefulness in detecting soft tissue involvement was very limited. Conventional linear tomography added little useful information to plain radiography, and we have deleted it from our protocol. The clinical usefulness of CT for both the diagnosis, staging and therapy planning of head and neck tumours has previously been evaluted (Ames et al., 1980; Jeans et af., 1982; North & Rice, 1981). However, the CT features of the ameloblastoma have received little mention in the literature. The analysis emphasises profile recognition. The salient features in our series include the patterns of maxillary or mandibular destruction, superficial soft tissue aberrations, changes in the deep structures reflecting recurrence, extent and direction of growth and the patterns of sinus opacification. While these features may not be pathognomonic, they are certainly distinctive and may aid in the differential diagnosis from antral carcinoma,
AMELOBLASTOMAS
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JAWS
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mucocoeles, odontogenic cysts, fibrous dysplasia, reticuloendothelioses, midline granulomas, lymphomas and osteogenic sarcomas as seen in the remainder of our patients. We were able to suggest the diagnosis of ameloblastoma in six of eight primary cases, based on the pattern recognition. Brant-Zawadzki et al. (1982) concluded that density determination also allowed differentiation of neoplastic soft tissue from inspissated mucus within obstructed sinuses in a study of four patients with acute sinusitis and six with maxillofacial neoplasms. This has been our experience, but we believe that the pattern of sinus involvement is probably more important tha.n densitometry, due to the great variability of the latter. CT defines the origin, position and extension of the mass lesion relative to normal and vital structures and helps the clinician plan the best surgical approach or the radiotherapist, the optimal portals. Following surgery and histopathological confirmation of an ameloblastoma, clinical surveillance can be augmented with CT scanning. The disadvantages of CT include cost, non-availability, a relative lack of specificity in the maxillofacial region and some technical pitfalls. The latter can be identified by the informed CT-radiologist and include ‘partial volume’ artefacts; while sections thinner than 5 mm increase spatial resolution and enable image reformation in various planes, small abnormalities may be missed due to insufficient distraction between tissues or motion artefacts; an artefactually ‘thinned’ bone may result from scanning in an oblique plane. Baseline and subsequent scans should be performed through identical anatomical levels; this was not always possible in the present study, because the patients were examined on one of two available scanners with different collimation capabilities (Figs. 2 & 4). However, a complete visual reconstruction of the anatomy is possible from each study. A pattern recognition approach and perhaps more importantly, a clinicoradiological follow-up protocol have been found most useful. Our experience differs somewhat from that of Proops and Phelps (1982) who suggest that ‘the use of the scanner in follow-up in those treated malignant lesions is somewhat limited, as surgery distorts the anatomy . .‘, perhaps because routinely we performed a baseline study following surgery. Acknowledgements We thank our colleagues of the Head and Neck Division (D.C. General Hospital) and Oral Surgery (HUH) for their co-operation in this project, Dr J. S. Teal, Professor and Chairman, Department of Radiology (HUH) for his constructive criticisms and Benson Esan and Edo Asuen (UNIBEN) for typing the manuscript. References Adekeye, E. 0. (1980). Ameloblastoma of the jaws: A survey of 109 Nigerian patients. Journal of Orul Surgery, 38, 36. Ames, J. R., Johnson, R. P. & Stevens, E. A. (1980). Computerized tomography in oral and maxillofacial surgery. Journal of Oral Surgery. 38, 145. Azumi, T., Nakajima, T., Takeuchi, S.. Fukushima, M. & Ischiki, T. (1981). Malignant ameloblastoma with metastasis to the skull: Report of a case. Journal of Orul Surgery, 39, 690. Archives of Otolaryngology, 105, 54. Bahna, M. S. (1979). Ameloblastoma. Brant-Zawadzki, M. N.. Minagi, H., Federle, M. P. & Rowe, L. D. (1982). High resolution CT with image reformation in maxillofacial pathology. American Journul of Roentgenology, 138, 477. Buff, S. J., Chen, J. T. T., Ravin, C. C. & Moore, J. 0. (1980). Pulmonary metastasis from ameloblastoma of the mandible: Report of a case and review of the literature. Journal of Oral Surgery, 38, 374. Connole, P. W. (1979). Tumors of dental origin: Ameloblastoma. Otologic C’hics of North America, 12, 141.
340
BRI’I’ISH
Crawley,
JOURNAL
W. A. & Levin.
OF
ORAL
L. S. (1978). Treatment
&
MAXILLOFACIAL
of the ameloblastoma:
SURGERY
A controversy.
Cancer. 142,
357.
I
Daramola, J. 0.. Ajagbe, H. A. & Oluwasanmi, .I. 0. (1980). Recurrent ameloblastomaof the jaws-A review of 22 cases. Plastic and Reconstructive Surgery, 65, S77. Ferlito, A., Recher, G.. Calzavara, M. & Bonino, M. (1982). Malignant ameloblastoma of the mandible. American Journal of Otoluryngology, 3, 57. Fitzgerald, G. W., Frcnkiel, S.. Black, K. M. J., Rochon. L. & Baxter, J. D. (1982). Ameloblastoma 01 the jaws: A 12-year review of the McGill experience. Journal of Otolaryngology. 11(l), 23. Huffman, G. G. & Thatcher, J. W. (1963). Ameloblastoma, the conservative approach to the treatment: Report of four cases. Journal of Oral Surgery, 32, 850. Jeans, W. D., Gilani, S. B Bullimore, J. (1982). The effect of CT scanning on staging of tumours of the paranasal sinuses. Clinical Radiology, 33, 173. McGuirt, W. F.. Scruggs, M. S. & Koufman. J. A. (1981). Hypercalcemia secondary to a pseudoparathormone-secreting ameloblastoma. Archives of Otolaryngology, 107, 487. Mehlisch, D. R., Dahlin. D. C. & Masson. J. K. (1972). Ameloblastoma: A clinicopathologic report. Journal of Oral Surgery, 30, 9. North. A. F. & Rice, J. (1981). Computed tomography in oral and maxillofacial surgery. Journal of Oral Surgery, 39, 199. Osborn, A. G., Hanafee, W. H. & Mancuso, A. A. (1982). Normal and pathologic CT anatomy of the American Journal of Roentgenology, 139, 555. mandible. Proops. D. W. & Phelps, P. 0. (1982). Computed tomography in E.N.T. practice. An evaluation of two years’ experience in a British sub-regional centre. The Journal of Laryngology and Otology, 96. 417. Robinson. H. B. G. (1937). Ameloblastoma: A survey of three hundred and seventy-nine cases from the literature. Archives of Pathology, 23, X31. Sehdev. M. K., Huvos, A. G., Strong, E. W., Gerold, F. P. & Willis, G. W. (1974). Ameloblastoma of the maxilla and mandible. Cancer, 33, 324. Shatkin, S. & Hoffmeister, F. S. (1965). Ameloblastoma: A rational approach to therapy. Oral Surgery, Oral Medicine, Oral Pathology, 20, 421. Small. I. A. & Waldron, C. A. (1955). Ameloblastomas of the jaws. Oral Surgery, Oral Medicine. Oral Pathology, 8, 281. Smith, J. T. (1968). The controversial ameloblastoma. Oral Surgery, Oral Medicine, Oral Pathology. 26, 4s. Stout, R. A., Lynch, J. B. & Lewis, S. R. (1963). The conservative surgical approach to amcloblastomas Plastic and Re-constructive Surgery, 31, S.54. of the mandible. Swinson. T. W. (1976). A clinico-pathological comparison of the ameloblastoma with rhe calcifying odontogenic cysts. Briti.yh Jo&nal of-Oral Surgery, 13, 217. Tsaknis. P. J. & Nelson, J. F. (1980). The maxillary ameloblastoma: An analysis of 24 cases. Journal of Oral Surgery. 38, 336.
AMELOBLASTOMAS
OF THE JAWS: RADIOLOGICAL AND FOLLOW-UP
DIAGNOSIS
BENNYO.IKO,M.D.,D.A.B.R.,‘~~ERNESTM.MYERS,M.D.,F.A.C.S.,‘ONYEKEWERE OGAN, M.B., ch.B., F.R.c.s., D.L.o.,~ and CHRISTIANU. CHINWUBA,M.D., D.A.B.R."
'
Department of Radiology,’ Howard University Hospital (HUH), and Divisions of Otorhinolaryngology ‘HUH, Washington D.C. (U.S.A.) & 3University College Hospital, Ihadan (Nigeria) Summary. Eleven of 57 tumours and cysts (19 per cent) seen at two major centres over a 4-year period were ameloblastomas, primary in eight and recurrent in three. Computed Tomography (CT) was the most sensitive imaging technique for detecting ameloblastomas. The radiological features were distinctive maxillary and mandibular pathology in primary cases and soft-tissue, maxillary sinus and asymmetrical deep tissue involvement in both primary and recurrent ameloblastomas. Following surgery and pathological confirmation. serial scans were combined with periodic clinical re-evaluation. We identified clinically occult recurrences in two cases and confirmed a clinically-suspected recurrence in one on the basis of the CT findings. Our protocol appears efficacious and is suggested for the necessary long-term follow-up in all pathologically verified ameloblastomas.
Introduction
The ameloblastoma remains a very controversial tumour of the jaws, perhaps more so than any other neoplasm found in the body (Mehlisch et al., 1972). Vitriolic arguments ramify every aspect of this disease; for instance there are no clear-cut criteria for the preference of either conservative surgery (Crawley & Levin, 1978; Huffmann & Thatcher, 1963; Stout et af., 1963), obligatory radical surgery (Azumi et al., 1981; Sehdev et al., 1974; Shatkin & Hoffmeister, 1965) or other forms of therapy (Fitzgerald et al., 1982; Sehdev et al., 1974; Tsaknis & Nelson, 1980). However, the great propensity of the ameloblastoma for local recurrence is generally recognised (Bahna, 1979; Daramola et al., 1980; Sehdev et al., 1974; Tsaknis & Nelson, 1980) and that this predisposes to both malignant transformation and distant metastases has been emphasised (Azumi et al., 1981; Buff et al., 1980; Ferlito et al., 1982). Histological patterns bear no relationship to the clinical behaviour of the tumour and even the electron microscope has not helped to clarify the histopathology or to predict the biological behaviour (Fitzgerald et al., 1982). The absolute necessity for long-term follow-up of all diagnosed ameloblastomas (Tsaknis & Nelson, 1980) is beyond question, and this has been by means of prolonged clinical surveillance. Unfortunately, clinical evaluation may be hampered by the complex anatomy of the region (Sehdev et al., 1974) and conventional radiology is of limited efficacy in evaluating subtle subcortical or soft-tissue changes that may herald a recurrence. A case of recurrent ameloblastoma demonstrating increased levels of serum calcium (Received
23 March
1984; accepted
17 December
1984)
Present Address: ‘Division of Neuroradiology. Department of Radiology, Bringham & Women’s Hospital, Harvard Medical School. Boston. Mass. U.S.A. of Radiology, College of Health Sciences, Corresponding Author: Dr Benny 0. Iko, ’ Department University of Port Harcourt, P.M.B. 5323, Port Harcourt, Nigeria.
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and urinary cyclic adenosine monophosphate (CAMP) which reverted to normal following surgery has been reported; this patient is being followed with serial measurements of serum calcium and urinary CAMP in the hope that, if the tumour recurs, it can be detected before it is large enough to be clinically evident (McGuirt et al., 1981). However, this case is most unusual, and a wider basis for detecting recurrence appears desirable. Computed tomography (CT) is currently the most sensitive imaging modality for detecting pathology in the head and neck region, but previous reports of the features of ameloblastomas were either anecdotal (Ames et ul., 1980; North & Rice, 1981) or limited to a single case report (Osborn et al., 1982). We therefore wish to review the CT features found in 11 cases. Surgery was performed on all cases, and a clinico-radiological protocol was developed for the follow-up. To our knowledge, the precise role of CT after surgery, has not been documented previously. Patients and Methods
Computed tomography is part of a standard protocol at Howard University Hospital (HUH) for the initial evaluation, staging and follow-up of operated jaw neoplasms. The HUH CT-Laboratory serviced the District of Columbia General Hospital during the study period 1978 to 1982. We saw 11 ameloblastomas (19 per cent) out of a total of 57 jaw tumours and cysts. Eight were primary cases, while three were recurrent, having undergone initial treatment elsewhere. The ages ranged from 28 to 72 years, average 47. There were eight females and three males, consisting of 10 Blacks and one ethnic Chinese. A thorough clinical evaluation preceded plain radiography in all cases (including intra-oral films in four cases), conventional linear tomography in five cases and CT in all cases. As our experience with CT increased, conventional tomography was omitted from the protocol. CT was performed on one of two available scanners, an Ohio Nuclear Whole Body with Fast Scan Modifications (22s) or a GE 8800 CT/T. The initial investigation consisted of plain CT, followed immediately by contrastenhanced scans, using a continuous drip infusion of Reno-M-Dip@ (meglumine diatrizoate). Transverse axial scans were obtained at 0.5 or 1 cm intervals through a plane parallel to the infraorbitomeatal (Reid) line; in selected cases, coronal images, multiplanar reformation and retrospective high-resolution analysis of raw scanning data were performed, as indicated by the tumour extension or artefacts arising from dental amalgams or restorations. Of the 57 tumours and cysts so examined, 42 had subsequent histopathological diagnoses, 11 of which were ameloblastomas. The CT features in the latter group were audited retrospectively. A baseline post-operative scan was performed 12 weeks following surgery and at 6-monthly intervals, usually through planes similar to those on the initial evaluation. A thorough clinical evaluation preceded all follow-up scans. The salient CT features of primary and recurrent ameloblastomas and stable post-maxillectomy status were selected at random. Representative
Case Reports
Case 1 (Primary Maxillary Ameloblastoma). A 32 year-old black female was seen for a painless swelling of the right upper jaw of 6 months’ duration. Physical examination revealed an exophytic and bossellated right gingivobuccal mass. Plain
AMELOBLASTOMAS
OF
Fig. Figure origin, lateral
THE
JAWS
1
l-Primary ameloblastoma in transverse axial projection. A right maxillary mass, medullary in expands and smoothly thins out the medial cortex, exerts a smooth pressure deformity on the sinus wall and shows a relatively homogenous character. The adjacent retromaxillary stripe (arrow) shows a focal infiltration in distinction to antral carcinoma or chrome smusttts
Fig. Fig.
3
2
Figure 2-Transverse axial CT. The recurrent lesion arises from the anterior inferior portion of the maxilla, invades and replaces the maxillary sinus and extends through the ethmoidal region into the nasal cavity. Posteriorly, the parapharyngeal fat stripe (arrow) and laterally and posteriorly the infratemporal boundary (arrow-heads) are obliterated. Compensatory expansion of the left Fossa of Rosenmuller can be contrasted with normal right (curved arrow). Figure 3-Normal post-maxillcctomy scan. Same patient as in Fig. 2, but at a slightly different level and on a different scanner, 4 years later. Residual swelling of the left cheek. The post-operative fibrotic changes are stable and regular. Note the nasomaxillary continuity from the previous surgery.
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radiography and linear tomography demonstrated a focal maxillary osteolysis while CT (Fig. 1) defined the origin, extent and relationship to vital structures and softtissues. A subsequent biopsy of the lesion confirmed an ameloblastoma. Radical surgery (hemimaxillectomy with reconstruction) was performed. The patient has been followed for 4.5 years, is clinically free of disease and has stable postmaxillectomy scans. Case 2 (Recurrent but Subclinical Ameloblastoma). A 61 year-old black female presented for a routine follow-up. She had undergone radical surgery, including a left rhinotomy with excision of the lateral nasal wall following the diagnosis of a maxillary ameloblastoma two years previously. Plain radiography and tomography demonstrated a homogeneous sclerotic lesion expanding the left maxilla while CT (Fig. 2) clearly defined the extent of the lesion. Transoral horizontal maxillectomy
Fig.
4
Figure &Axial CT, This recurrent mass had invaded and replaced the maxillary sinus. destroyed the lateral nasal wall and extended into the floor of the orbit (better seen on higher scans). The left styloid process was eroded, the pterygoid muscles replaced (compare the normal right side. P). the retropharyngeal space invaded and the tumour extended into the base of the skull. The soft tissue mass in the left cheek region (long arrow). was positive upon biopsy. The low density intratumoural lesions (black boxes) measured 20 Hounsfield Units (HU), and the whtte box 49 HU. The former is higher than for normal structures or water (and therefore more compatible with ‘radiation necrosis’ (or granulation tissue than infection) while the latter is 20-30 HU higher than normal structures (and therefore consistent with recurrent tumour). Concurrent right maxillary sinusitis with continuous mucoperosteal thickening (arrow heads) and pockets of residual sinus air.
AMELOBLASTOMAS
OF
THE
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was performed and the lesion excised in toto. This patient has now been followed for over 4 years and remains free of disease clinically, and radiologically (Fig. 3). Case 3 (Recurrent and Complicated Compound Ameloblustoma). A 41-year-old Vietnamese, ethnic Chinese, presented with a recurrent swelling of her left jaw, nasal obstruction and epistaxis. She gave a history of six previous resections of the left mandible for recurrences of ameloblastoma, the last of which was in Vietnam 10 years previously. Reconstruction of the mandible with a rib graft and a ‘fullcourse radiotherapy’ (total dosage unknown) had also been performed. CT (Fig. 4) and a CT-directed percutaneous biopsy of the soft-tissue lesion preceded surgery: a left Caldwell-Luc antrotomy and left hemimandibulectomy with reconstruction. Total excision was technically impossible. This patient has been followed for 1X months and her CT features appear stable. Of some interest is the clinical and radionuclide diagnosis of thyrotoxicosis which coincided with the latest recurrence and for which the patient is being treated. Results We found a high incidence of 11 (19%) ameloblastomas in a series of 57 jaw tumours and cysts. These were primary in eight and recurrent in three. One was compound mandibulo-maxillary, two maxillary and eight mandibular, most of the latter occurring in the retromolar trigone. The left jaw was involved in seven cases (64%). Most patients were females (73%) in the fourth decade, and black. The common presenting symptoms were painless, sometimes disfiguring swelling of the jaw of several months duration. ‘Eggshell crackling’ sensation on gentle pressure was noted in one case. Associated sinuses, pain, loose teeth and intra-oral ulcerations were infrequent and occurred more often in recurrent cases. The predominant histological pattern was follicular, with two cases of the plexiform, two of the mixed and one of the acanthomatous types. Plain radiography was positive in nine cases, equivocal in one and negative in the other. The mandibular lesions were often osteolytic, sometimes with an expansion of the lingual cortex and a multiloculated soap-bubble pattern. The maxillary lesions were well marginated and sclerotic in one case and lytic in the other, both expanding the cortex and were probably better appreciated on conventional linear tomography. Computed
Tomography
A total of 79 CT examinations were performed: 11 initial, 11 post-operative and 57 bi-annual scans; the longest follow-up is 4.5 years and the shortest 12 months. CT scanning in the transverse plane provided the most useful information, although reformation or direct coronal and reformatted sagittal images were in some cases also performed. Other modifications included ‘region of interest’ density analysis, and physiological manoeuvres during scanning to confirm fixation and enable analysis of the symmetry of the deep structures. The CT features were: (a) Bone changes. The case of primary maxillary ameloblastoma (Fig. 1) showed a monocystic cavity, arising from the maxillary tuberosity and adjacent to the molar area and extending towards the lingual aspect. The medullary cavity was widened, but with an apparent respect of the cortex. There was a focal pressure deformity of the adjacent maxillary sinus, and the extension into the sinus was homogenous. Recurrent maxillary ameloblastomas (Figs. 2 & 4) were predominantly osteo-
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sclerotic, but with areas of osteolysis. These findings were distinctive from other pathology occurring in our series, squamous cell carcinomas demonstrating irregular discontinuity of osseous structures, a wide zone of transition and a less uniform density, while chronic sinusitis (Fig. 4) showed a more diffuse but even mucosal thickening with areas of air density and lack of bone discontinuity. In the mandible, primary ameloblastoma presented as one of two patterns, either coarse and multilocular destruction with a rim of uninvolved cortex or more commonly uneven cortical sclerosis at the retromolar trigone. (b) Soft tissue changes. These were more common in recurrent cases (Fig. 4) and consisted of infiltration of the cheek, loss of fascial planes (retromaxillary, pre- or post-pterygoid bands) and of the muscles of mastication. (c) Deep structure changes. Intravenous contrast enhancement was useful in reconstructing landmarks. The extensions of tumour recurrence were identified based on comparison with the baseline scan, performed 14 days following surgery. Recurrent maxillary ameloblastoma may extend posteriorly into the pterygopalatine or infratemporal fossa (Figs. 2 & 4), superiorly into the orbit, medially and anteriorly into the ethmoido-nasal complex (Fig. 2). The mucosa, submucosal structures and ‘blind areas’ such as the lateral pharyngeal recesses (Figs. 2 & 4) were evaluated routinely. (d) Sinus opacification. This was an uncommon feature in primary cases and where it occurred was usually focal, airless and contiguous with a bony abnormality. However, tumour replacement of the maxillary sinus in recurrent cases was always associated with bony destruction (Figs. 2 & 4). Finally, the postoperative baseline scan (Fig. 3) was the most important reference study in detecting recurrent but subclinical disease (Fig. 2), or confirming clinically suspected recurrence (Fig. 4). Discussion
Although a rare tumour of the jaws (about 1% in most series) the ameloblastoma has been very widely reported (Adekeye, 1980; Connole, 1972; Robinson, 1937; Small & Waldron, 1955; Smith, 1968; Swinson, 1976 and many others). Therefore only a brief review of the interesting features in this series which are either unique or at variance with the majority of previous reports is appropriate. We are unable to explain the high incidence of 11 ameloblastomas in a series of 57 tumours (19%) or the 2.6:1 female to male ratio. These may be due to chance, or biased sampling. 91% of our patients were black; this may reflect the high proportion of Blacks in the Washington D.C. area (70 % or more) and the catchment population of the two referral centres. Plain radiography was positive in most cases, but its usefulness in detecting soft tissue involvement was very limited. Conventional linear tomography added little useful information to plain radiography, and we have deleted it from our protocol. The clinical usefulness of CT for both the diagnosis, staging and therapy planning of head and neck tumours has previously been evaluted (Ames et al., 1980; Jeans et af., 1982; North & Rice, 1981). However, the CT features of the ameloblastoma have received little mention in the literature. The analysis emphasises profile recognition. The salient features in our series include the patterns of maxillary or mandibular destruction, superficial soft tissue aberrations, changes in the deep structures reflecting recurrence, extent and direction of growth and the patterns of sinus opacification. While these features may not be pathognomonic, they are certainly distinctive and may aid in the differential diagnosis from antral carcinoma,
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mucocoeles, odontogenic cysts, fibrous dysplasia, reticuloendothelioses, midline granulomas, lymphomas and osteogenic sarcomas as seen in the remainder of our patients. We were able to suggest the diagnosis of ameloblastoma in six of eight primary cases, based on the pattern recognition. Brant-Zawadzki et al. (1982) concluded that density determination also allowed differentiation of neoplastic soft tissue from inspissated mucus within obstructed sinuses in a study of four patients with acute sinusitis and six with maxillofacial neoplasms. This has been our experience, but we believe that the pattern of sinus involvement is probably more important tha.n densitometry, due to the great variability of the latter. CT defines the origin, position and extension of the mass lesion relative to normal and vital structures and helps the clinician plan the best surgical approach or the radiotherapist, the optimal portals. Following surgery and histopathological confirmation of an ameloblastoma, clinical surveillance can be augmented with CT scanning. The disadvantages of CT include cost, non-availability, a relative lack of specificity in the maxillofacial region and some technical pitfalls. The latter can be identified by the informed CT-radiologist and include ‘partial volume’ artefacts; while sections thinner than 5 mm increase spatial resolution and enable image reformation in various planes, small abnormalities may be missed due to insufficient distraction between tissues or motion artefacts; an artefactually ‘thinned’ bone may result from scanning in an oblique plane. Baseline and subsequent scans should be performed through identical anatomical levels; this was not always possible in the present study, because the patients were examined on one of two available scanners with different collimation capabilities (Figs. 2 & 4). However, a complete visual reconstruction of the anatomy is possible from each study. A pattern recognition approach and perhaps more importantly, a clinicoradiological follow-up protocol have been found most useful. Our experience differs somewhat from that of Proops and Phelps (1982) who suggest that ‘the use of the scanner in follow-up in those treated malignant lesions is somewhat limited, as surgery distorts the anatomy . .‘, perhaps because routinely we performed a baseline study following surgery. Acknowledgements We thank our colleagues of the Head and Neck Division (D.C. General Hospital) and Oral Surgery (HUH) for their co-operation in this project, Dr J. S. Teal, Professor and Chairman, Department of Radiology (HUH) for his constructive criticisms and Benson Esan and Edo Asuen (UNIBEN) for typing the manuscript. References Adekeye, E. 0. (1980). Ameloblastoma of the jaws: A survey of 109 Nigerian patients. Journal of Orul Surgery, 38, 36. Ames, J. R., Johnson, R. P. & Stevens, E. A. (1980). Computerized tomography in oral and maxillofacial surgery. Journal of Oral Surgery. 38, 145. Azumi, T., Nakajima, T., Takeuchi, S.. Fukushima, M. & Ischiki, T. (1981). Malignant ameloblastoma with metastasis to the skull: Report of a case. Journal of Orul Surgery, 39, 690. Archives of Otolaryngology, 105, 54. Bahna, M. S. (1979). Ameloblastoma. Brant-Zawadzki, M. N.. Minagi, H., Federle, M. P. & Rowe, L. D. (1982). High resolution CT with image reformation in maxillofacial pathology. American Journul of Roentgenology, 138, 477. Buff, S. J., Chen, J. T. T., Ravin, C. C. & Moore, J. 0. (1980). Pulmonary metastasis from ameloblastoma of the mandible: Report of a case and review of the literature. Journal of Oral Surgery, 38, 374. Connole, P. W. (1979). Tumors of dental origin: Ameloblastoma. Otologic C’hics of North America, 12, 141.
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