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Late loco-regional recurrences after radical resection for mandibular ameloblastoma
0ncology
Late Ioco-regional recurrences after radical resection for mandibular ameloblastoma
Luc J . - M . J. D e m e u l e m e e s t e r , M a u r i c e Y. M o m m a e r t s , Eric Fossion and Michel Bossuyt Department of Oral and Head and Neck Surgery and Department of Stomatology and Maxillofacial Surgery, University Hospitals K,U.L.., Leuven, Belgium
L. J.-M. J. Demeulemeester, M. Y.. Mommaerts, E. Fossion and M. Bossuyt: Late loco-regional recurrences after radical resection Jor mandibular ameloblastoma. Int. J. Oral Maxillofac. Surg. 1988; 17: 310-315. Abstract. 5 cases o f mandibular ameloblastoma are described with multiple recurrences after a long period of time. 4 o f them were primarily treated by radical resection. 1 was initially treated by enucleation and extensive resection was performed only after its recurrence. The invasive growth of the recurrent t u m o r into the soft tissues and the cranial base, necessitating extensive ablative and reconstructive surgery, reflects the potential aggressiveness o f this tumor. It is therefore recommended, to plan an adequate resection in cases of multicystic ameloblastoma, which includes a margin of at least 1 cm, o f apparently noninvaded bone. If the tumor has eroded through the cortical bone and invaded into the soft tissues, wider margins are necessary to eliminate possible t u m o r extensions that are left behind. A d e q u a t e follow-up on a regular basis should enable the clinician to detect early recurrence so as to avoid m a j o r surgery.
The tendency of intraosseous ameloblastoma to recur and to invade soft tissues is well documented. Radical resection is generally accepted as imperative and it h a s been proven to help in decreasing the n u m b e r o f recurrences significantly 34. Radical resection is designed to remove the t u m o r together with at least 1 cm of surrounding healthy tissue. Since the tumor is generally not well-defined, despite clinical and radiological examination perhaps suggesting the contrary, the extension into the adjacent bone, but particularly into the surrounding soft tissues is often underestimated. Tumor cells left behind may give rise to uncontrollable loco-regional recurrences several years after resection 20. Few such recurrences are seen in a single surgeon's lifetime. Well-documented long-term studies on the surgical treatment o f ameloblastoma are also rare. Therefore, conservative treatment, to reduce mutilation and morbidity, is sometimes recommended 4, 6, 18, 25, 36 5 cases will be presented to illustrate extremely late recurrences after radical resection. Finally, we will discuss a rational approach to the treatment of ameloblastomas based on pathological and anatomical considerations.
Case reports Case no. 1
A 51-year-old female presented in 1976 for treatment of a recurrence of an ameloblastoma. Her history revealed that a wide resection of an ameloblastoma was carried out in 1960. The left ascending ramus and the distal part of the left mandibular body
Key words: Ameloblastoma; recurrences; radical resection. Accepted for publication 9 June 1988
were resected and reconstructed with a free iliac crest graft 3 months later. 16 years later, she presented with a recurrence of 6 cm in diameter, involving the left postero-lateral part of the soft palate, the left maxillary tuberosity, the retromolar zone and the tonsilar fossa. The biopsy confirmed the diagnosis of ameloblastoma. The tumor was resected in one piece, in-
Fig. 1. Case no. 1. CT-scan showing the chin area with the intraosseous tumor recurrence.
Recurrent ameloblastoma cluding the deep lobe of the parotid gland, the bonegraft and the pterygoid process, up to the base o f the skull. Frozen sections of the resection margins were negative, as were those o f the parotid lymphnodes. The intraoral defect was reconstructed with an island, pedicled, forehead-flap. 4 years later, the patient was re-admitted for atypical left trigeminal neuralgia. Neurological and radiological examinations revealed no detectable tumor. Alcoholization o f the trigeminal nerve at the level of the left foramen ovale was performed and the pain gradually decreased. In 1987 (27 years after the 1st treatment), pain and swelling in the chin area urged the patient to seek treatment again. A biopsy again revealed a recurrence (Fig. 1). Bonescintigraphy showed increased isotope-deposit in the distal part of the remaining mandibular body and in the 4th lumbal vertebra. CT-scanning with contrast-perfusion showed signs of possible intracranial invasion. N M R imaging of the cranial base showed a cystic process along the left carotid artery with destruction of surrounding bone including the sella turcica and extending posteriorly along the lateral side o f the pedunculus cerebri (Fig. 2). The 3rd division of the left trigeminal nerve below the foramen ovale had an irregular aspect, and this probably reflects the pathway of the intracerebral invasion. No neurological symptoms were present. The treatment consisted of resection of the symphysis with primary reconstruction by a free iliac crest graft to support the tongue and the chin. The intracerebral invasion has not been treated since it was symptomless. The same applies to the possible metastasis in the 4th lumbal vertebra, which has not yet been confirmed histologically. 6 months postoperatively, the patient is doing well. If necessary, palliative radiotherapy will be given.
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Fig. 2. Case no. 1. Intracranial invasion o f the ameloblastoma.
Case no, 2
A 49-year-old female was referred for treatment of a recurrent ameloblastoma. She complained of a painless swelling in the right cheek, which had slowly increased in volume during the last 3 years. She had first been treated for an ameloblastoma in the right mandible in 1957, at age 20 years. The tumor had been enucleated. A first recurrence was noted at age 29 years, at which time a hemimandibutectomy was carried out, saving the coronoid process. The reconstruction was performed by using an acrylic implant, l year later, the infected implant was removed and 2 months later, replaced by a free bone graft from the iliac crest. In 1986, the patient returned with a slowly growing swelling of the right cheek. The CTscanning, with contrast-perfusion, demonstrated a mass of 6 cm in diameter above the proximal part of the reconstructed mandible, with subcutaneous extension laterally and pushing the muscles of the floor of mouth caudally. Erosion of the maxillary sinus wall
Fig. 3. Case no. 2. Tumor recurrence in the right infratemporal fossa.
and slight infratemporal invasion were also noted. A Ferguson-Weber approach enabled the removal of the tumor, which was fixed to the remaining coronoid process. The whole block was resected together with the maxillary tuberosity and the pterygoid-plates including the contents of the pterygomaxillary fossa up to the base of the skull. The defect was packed to heal on secondary intention. Histopathological examination Showed no invasion of the tumor into the maxilla, but extension towards the cranial base. CT-scanning 4 months later revealed a tumor-mass in the infratemporal fossa (Fig. 3). This was promptly removed through a temporal approach, with resection of the zygo-
matic arch. The temporal muscle was dissected free and rotated into the defect, pedicled on its superficial vascular system. At present, one 18 months later, there is no sign of recurrence. Case no. 3
In 1976, a 46-year-old man had been treated for what at that time was interpreted as an infected follicular cyst of the left mandibular 3rd molar. Part of the cyst was left behind because o f difficulty in access. The histopathological diagnosis was multicystic ameloblastoma. The patient was immediately referred to our department for further evalu-
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Fig. 4. Case no. 3. Recurrent ameloblastoma in the iliac crest bonegraft.
Fig. 5. Case no. 4. Orthopantomogram showing the primary multicystic ameloblastoma in the left mandible.
ation and treatment. A left hemimandibulectomy was performed, including the condyle. The tumor had to be resected from the pterygoid-plates and the cranial base. 1 month later, the mandible was reconstructed using a free iliac bone graft. 10 years later, radiographs showed a recurrent lesion in the bone graft (Fig. 4). A biopsy revealed a recurrent ameloblast0ma. CTexamination showed invasion into the pterygomaxillary fossa. Surgical access was gained by a hemicoronal incision with preauricular extension along with an intraoral incision in the buccal sulcus. The proximal part of the bone graft was resected together with the left pterygoid plates, including a wide margin of surrounding soft tissues. No attempt was made to reconstruct the lost part of the graft. Healing was uneventful.
Histopathological examination showed invasion of the tumor into the soft tissues to the lateral aspect o f the bonegraft. Case no. 4
In 1973, a 67-year-old male was referred for diagnosis and treatment of a large multicystic tumor in the left mandibular angle. (Fig. 5). A biopsy lead to the diagnosis ameloblastoma. An intraoral hemimandibulectomy was carried out including the condyle, and the reconstruction was performed immediately with a free rib graft. It was noted at that time that the tumor was adherent to the mastieatory muscles. The rib graft had to be removed 2 months later because of infection and was replaced by a free iliac crest graft. The first recurrence became apparent 8
years later. It was located in the tendon of the temporal muscle, the infratemporal fossa, the parotid gland and in the distal portion of ~ the iliac crest graft (Fig. 6). A massive block resection was carried out including the above-mentioned structures. Reconstruction was achieved by a microvascular myocutaneous latissimus dorsi flap. The sections near the cranial base were free o f tumor. The facial paralysis was symptomatically corrected 1 month later by an eyebrow-lift, a partial tarsoraphy plasty and by lifting the corner of the mouth. An orthopantomogram by the end of 1983 showed an area suspicious of tumor. The CTscan localized the tumor in the left cheek, invading the buccal mucosa, and the cranial base. A radical resection was attempted, but left incomplete at the cranial base because of the poor prognosis in this 77-year-old man. A 3rd recurrence in the chin area was treated by a partial resection in September 1984. The patient recovered and did not need reconstructive surgery since he functioned well with what was left of the mandible. In May 1987, a swelling appeared in the anterior region of the floor of the mouth. Xrays and CT-scan revealed several recurfences, one of which extended from the chin to the hyoid bone and one at the left base of skull down to the soft palate. The right horizontal part of the remaining mandible also appeared to be invaded (Fig. 7). A 3rd operation was performed, including a resection o f the tumor at the left cranial base and the right mandible and chin. Because of the extensive soft tissue loss, a 2nd free latissimus dorsi flap with microsurgical anastomosis had to be brought in. To support the soft tissues and the tongue, a free rib graft was fixed to the right ascending ramus with a long plate. On the left side, no additional soft tissues were needed. Postoperatively, the patient was unable to swallow. A tracheostomy was necessary and nasogastric tube feeding was maintained for several months. The ribgraft underwent aseptic necrosis and was replaced by a free iliac crest flap with microvascular anastomosis. At present, swallowing is still difficult, but the soft tissues are again supported. Case no. 5
In November 1986, a 50-year-old patient was seen for a temporal and pre-auricular swelling. A follicular cyst of the left lower 3rd molar had been removed in 1957. She underwent surgery for a recurrent lesion at the same site in 1962. Further information on this procedure was not available, except that the histopathological diagnosis was ameloblastoma. A left hemimandibulectomy was carried out for a new recurrence in 1966, involving the coronoid and condylar process, and invading the soft tissues at the lingual side. No reconstruction was attempted at that time. A 3rd recurrence was detected medially of the left zygomatic arch (Fig. 8) in 1986 (29
Recurrent ameloblastoma
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As shown by Mtiller & Slootweg26ameloblastoma, produces extensions into the bone marrow space well past the bone cavities demonstrable on radiographs. Particularly when the tumor has eroded through the cortical bone, finding its way into the soft tissues, diagnosis of the extent of the lesion becomes very difficult. In these cases, the surgeon has to rely on CT-scanning and NMRimaging to perform an adequate resection with reasonable margins of normal tissue. Frozen sections can be difficult to rely on because the presence of bone fragments, often makes it hard to process them well. This does not imply, however, that every case of solid ameloblastoma must be treated initially by a radical resection4. Treatment can certainly not be based upon histological patterns2~, 23, 2s, 3~. According to GARDNER • PE(~AK1°, one must consider the Fig. 6. Case no. 4. CT-scan showing the extent of the first recurrence. clinical type (introasseous solid or multicystic, unicystic, peripheral ameloblatoma) 2, the location7,16,30and the size of the tumor within the jaw bones 7. The solid or multicystic ameloblastoma is known to invade the intertrabecular spaces of cancellous bone without accompanying resorption of the trabeculae. It does not invade compact bone, although it may erode it Iv. If the treatment constits of enucleation, tumor cells may be left in the surrounding cancellous bone and the tumor may subsequently recur. This suggests that the most appropriate treatment for a small solid or multicystic ameloblastoma of the mandible is a conservative marginal resection with a 10 mm border of apparently uninvolved bone. Solid or multicystic ameloblastomas of greater size, especially when they tend to erode through the cortical plate of the mandible, need a more aggressive approach: segmental resection (without mainFig. 7. Case no. 4. The recurrence in the contralateral side is not in continuity with the 4th taining the continuity of bone) includrecurrence at the primary site. ing the overlying periosteum and also the overlying soft tissues26. The same years after the first operation). Through a malignant behaviour. It is a slowly approach is indicated in the case of temporal approach, the arch was resected growing, locally invasive tumor with a maxillary ameloblastoma because of and the tumor could be removed from the reported high recurrence rate if not reanatomical considerations. A recurcranial base. The left mandible was recon- moved adequately ~°, 24, 39. Since maligstructed with a free costochondral graft. The nant transtbrmation3,5,~9,33and metastarence in this region is often inoperable soft tissue defect was filled with a free suband must be avoided by all means. ses~2, ~3,22 are rare, it has been suggested mammary, dermofat-graft. 1 year after the In contrast to the solid or multicystic latest surgery, the patient is free of tumor. that one approach these tumors rather type, the unicystic ameloblastoma can conservatively 35. The free fat graft and the rib graft underwent initially be treated conservatively by The problem of recurrence can be slow aseptic necrosis. Definitive reconstrucsimple enucleation15,29.37or marsupializattributed to an inadequate resection of tive surgery is planned. ation and marginal resection4°. Microthe involved bone (particularly bone scopic examination should determine marrow), to the spreading of residual Discussion and conclusions whether there is involvement of the perbone fragments that contain tumor tisAmeloblastoma is a benign odontogenic sue and most of all to the inadequate iphery of the connective tissue wall of excision of the overlying soft tissues ~. the cyst. If there is, a secondary martumor which in rare instances may show
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Fig. 8. Case no. 5. Recurrent tumor on the left temporal fossa.
ginal resection is indicated, especially w h e n it concerns a n a m e l o b l a s t o m a o f the p o s t e r i o r maxilla 9. The 3rd i m p o r t a n t clinical type o f a m e l o b l a s t o m a is the rare p e r i p h e r a l a m e l o b l a s t o m a . It occurs m o s t comm o n l y in the m a n d i b u l a r gingiva a n d has a very low p o t e n t i a l for b o n y invasion 8, H, 14,32,39 It is treated by simple excision with a small m a r g i n o f n o r m a l tissue d o w n to b u t n o t necessarily including the periosteurn. In conclusion, the a u t h o r s w a n t to stress the i m p o r t a n c e of a careful clinico-radiological e v a l u a t i o n o f each case o f a m e l o b l a s t o m a to decide u p o n the best treatment. T h e experience o f these 5 extremely late recurrences, s o m e t i m e s at quite a distance f r o m the p r i m a r y tumor, illustrates t h a t some b e n i g n tumors can be so aggressive so as to necessitate wide a n d radical surgery. A careful follow-up is indicated in all amel o b l a s t o m a s to detect early recurrences, thus m a k i n g secondary surgery w o r t h while a n d preventing i n v a s i o n o f such vital areas as the o r b i t a n d the cranial base.
References 1. Baden, E.: Contribution ~ l'ktude de lameloblastome du maxillaire inf~rieur. Th~se, Facult6 de Medecine, Universit6 de Genrve, Berichthaus, Zfirich, 1964 2. Cannon, C.R. & Burnett, W.M.: Mandibular ameloblastoma. South Med. J. 1986: 79: 1446-1448. 3. Cart, R.F. & Halperin, V.: Malignant
ameloblastomas from 1953 to 1966. Oral Surg. 1968: 26: 514-522. 4. Crawley, W.A. & Levin, L.S.: Treatment of the ameloblastoma. A controversy. Cancer 1978: 42: 357-363. 5. Dararnola, J.O., Abioye, A.A., Ajagbe, H.A. & Aghadiuno, P.U.: Maxillary malignant anaeloblastoma with intraorbital extension: report of a case. J. Oral Surg. 1980: 38: 203-206. 6. Emmings, F.G., Gage, A.A. & Koepf, S.W.: Combined curettage and cryotherapy for recurrent ameloblastoma of the mandible: ~eport of a case. J. Oral Surg. 1971: 29: 41-44. 7. Eversole, L.R.: Clinical outline of oral pathology: diagnosis and treatment, 2nd edition, Lea & Febiger, Philadelphia, 1984: pp. 201-210. 8. Ficarra, G: & Hansen, L.S.: Peripheral ameloblastoma. A case report. J. Cranio.Max.-Fac. Surg. 1987: 15: 110-112. 9. Gardner, D.G., Morton, T.H. Jr. & Worsham, J.C.: Plexiform unicystic ameloblastoma of the maxilla. Oral Surg. 1987: 63: 221-223. 10. Gardner, D.G. & Pe~ak, A.M.J.: The treatment of ameloblastoma based on pathology and anatomic principles. Cancer 1980: 46: 2514-2519. 11. Guralnick, W., Chuong, R. & Goodman, M.: Peripheral ameloblastoma of the gingiva. J. Oral Maxillofac. Surg. 1983: 41: 536-539. 12. Harrer, W.V. & Patchevsky, A.S.: Mandibular ameloblastoma with intracerebral and pulmonary metastasis. Oral Surg. 1970: 29: 893-898. 13. Herceg, S.J. & Harding, R.L.: Malignant ameloblastoma with pulmonary metastases. Report of a case and review of the literature. Plast. Reconstr. Surg. 1972: 49. 456-460.
14. Horowitz, I., Hirshberg, A. & Dayan, D.: Peripheral ameloblastoma - a clinical dilemma in gingival lesions. J. Clin. Periodont. 1987: 14: 366-369. 15. Isacsson, G. Andersson, L. Forsslund, M. Bodin, I. & Thomsson, M.: Diagnosis and treatment of the unicystic ameloblastoma. Int J. Oral Maxillofac. Surg. 1986: 15" 759-764. 16. Kameyama, Y, Takehana, S., Mizohata, M., Nonobe, K.,Hara, M., Kuwai, T. & Fukaya, M.: A clinicopathological study of ameloblastoma. Int. J. Oral Maxillofac. Surg. 1987: 16: 706-712. 17. Kramer, I.R.H.: Ameloblastoma: a clinicopathological appraisal. Br. J. Oral Surg. 1963: 1: 13-28. 18. Krfiger, G.O.: Textbook of oral and maxillofacial surgery, 6th edition, The C.V. Mosby Company, St Loius, Toronto, 1984. 19. Larsson, A. & Almeren, H.: Ameloblastoma of the jaws. An analysis of a consecutive series of all cases reported by the Swedish Cancer Society during 1958-1971. Acta Pathol. Microbiol. Scand. 1978: 86: 337-349. 20. Lello, G.E. & Smith, I.: Ameloblastoma with multiple delayed recurrences: a case report. Head Neck Surg. 1987: 9: 295-298. 21. Lucas, R.B.: Pathology o f tumours o f the oral tissues. 4th edition, Churchill Livingstone, Edinburgh, 1984, pp. 30-59. 22. Madiedo, G., Choi, H., Kleinman, J.G.: Ameloblastoma of the maxilla with distant metastases and hypercalcemia. Am. J. Clin. Pathol. 1981: 75: 585-591. 23. Masson, J.K., McDonald, J.R. & Figi, F.A.: Adamantinoma of the jaws. A clinicopathologic study of 101 histologically proved cases. Plast. Reconstr. Surg. 1959: 23: 510-528. 24. Mehlisch, D.R., Dahtin, D.C. & Masson, J.K.: Ameloblastoma: a clinicopathologic report. J. Oral. Surg. 1972: 3 0 : 9 22. 25. Monks, F.T.: Treatment of adamantinoma by conservative surgery: a review. J. Oral. Surg. Anesth. Hosp. D. Serv. 1964: 22: 171-177. 26. Miiller, H. & Stootweg, P.J.: The growth characteristic of multilocular ameloblastomas. J. Max.-Fae. Surg. 1985: 13: 224-230. 27. Oka, K., Fukui, M., Yamashita, M., Takeshita, I., Fujii, K., Kitamura, K., Nakamura, S., Tashiro, H. & Masuda, S.: Mandibular ameloblastoma with intracranial extension and distant metastasis. Clin. Neurol. Neurosurg. 1986: 88: 303-309. 28. Prein, J., Remagen, W., Spiessl, B. & Uehlinger, E.: Atlas of tumors o f the facial skeleton, 1st edition, Springer Verlag, Berlin 1986, pp. 7-15. 29. Robinson, L., & Martinez, M.G.: Unicystic ameloblastoma. A prognostically distinct entity. Cancer 1977: 40: 22782285.
Recurrent ameloblastoma 30. Sehdev, M.K., Huvos, A.G., Strong, E.W., Gerold, ER, Willis, G.W.: Ameloblastoma of maxilla and mandible. Cancer 1974: 33: 324-333. 31. Shafer, W.G., Hine, M.K. & Levy, B.M.: A textbook of oral pathology, 4th edition, W.B. Saunders Company, Philadelphia, 1983: pp. 276-285. 32. Shiba, R., Sakoda, S. & Yamada, N.: Peripheral ameloblastoma. J. Oral Maxillofac. Surg. 1983: 41: 460M63. 33. Slootweg, RJ. & Miiller, H.: Malignant ameloblastoma or ameloblastic carcinoma. Oral. Surg. 1984: 57: 168-176. 34. Small. I.A. & Waldron, C.A.: Ameloblastoma of the jaw. Oral Surg. 1985: 8: 281-297. 35. Stout, R.A., Lynch, J.B. & Lewis, S.R.:
The conservative surgical approach to ameloblastoma of the mandible. Plast. Reconstr. Surg. 1963: 31: 554-562. 36. Tingchun, W., Zhe, C., Fengchen, T. Quanziang, T. & Citing, Y.: Ameloblastoma of the mandible treated by resection, preservation of the inferior alveolar nerve, and bone grafting. J. Oral Maxillofac. Surg. 1984: 42: 93-96. 37. Van de Vijver, H., Neyt, L., De Clercq, C., Bergmans, G. & MichMssen, R: Het ameloblastoom: naonderzoek bij zeven pati~nten. Rev. Belge. Med. Dent. 1987: 42: 43M9. 38. Van Geel, A.N., Van Slooten, E.A., Snow, G.B. & Van der Waal, I.: Het ameIoblastoom. Ned. Tijdschr. Geneeskd. 1977: 11: 442M46.
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39. Woo, S.B., Smith-Williams, J.E., Scimbla, J.J. & Sipper, S.: Peripheral ameloblastoma of the buccal mucosa: a case report and review of the English literature. Oral. Surg. 1987: 63: 78-84. 40. Yokobayashi, Y., Yokobayashi, T., Nakajima, T., Oyama, T., Fukushima, M. & Ishiki, T.: Marsupialization as a possible diagnostic aid in cystic ameloblastoma. J. Max.-Fac. Surg. 1983: 11: 137-141. Address: M. Mommaerts Department Stomatology, Maxillofacial and Head and Neck Surgery U Z St. Rqfa~'_l Kapucijnenvoer 7 B-3000 Leuven Belgium
Late Ioco-regional recurrences after radical resection for mandibular ameloblastoma
Luc J . - M . J. D e m e u l e m e e s t e r , M a u r i c e Y. M o m m a e r t s , Eric Fossion and Michel Bossuyt Department of Oral and Head and Neck Surgery and Department of Stomatology and Maxillofacial Surgery, University Hospitals K,U.L.., Leuven, Belgium
L. J.-M. J. Demeulemeester, M. Y.. Mommaerts, E. Fossion and M. Bossuyt: Late loco-regional recurrences after radical resection Jor mandibular ameloblastoma. Int. J. Oral Maxillofac. Surg. 1988; 17: 310-315. Abstract. 5 cases o f mandibular ameloblastoma are described with multiple recurrences after a long period of time. 4 o f them were primarily treated by radical resection. 1 was initially treated by enucleation and extensive resection was performed only after its recurrence. The invasive growth of the recurrent t u m o r into the soft tissues and the cranial base, necessitating extensive ablative and reconstructive surgery, reflects the potential aggressiveness o f this tumor. It is therefore recommended, to plan an adequate resection in cases of multicystic ameloblastoma, which includes a margin of at least 1 cm, o f apparently noninvaded bone. If the tumor has eroded through the cortical bone and invaded into the soft tissues, wider margins are necessary to eliminate possible t u m o r extensions that are left behind. A d e q u a t e follow-up on a regular basis should enable the clinician to detect early recurrence so as to avoid m a j o r surgery.
The tendency of intraosseous ameloblastoma to recur and to invade soft tissues is well documented. Radical resection is generally accepted as imperative and it h a s been proven to help in decreasing the n u m b e r o f recurrences significantly 34. Radical resection is designed to remove the t u m o r together with at least 1 cm of surrounding healthy tissue. Since the tumor is generally not well-defined, despite clinical and radiological examination perhaps suggesting the contrary, the extension into the adjacent bone, but particularly into the surrounding soft tissues is often underestimated. Tumor cells left behind may give rise to uncontrollable loco-regional recurrences several years after resection 20. Few such recurrences are seen in a single surgeon's lifetime. Well-documented long-term studies on the surgical treatment o f ameloblastoma are also rare. Therefore, conservative treatment, to reduce mutilation and morbidity, is sometimes recommended 4, 6, 18, 25, 36 5 cases will be presented to illustrate extremely late recurrences after radical resection. Finally, we will discuss a rational approach to the treatment of ameloblastomas based on pathological and anatomical considerations.
Case reports Case no. 1
A 51-year-old female presented in 1976 for treatment of a recurrence of an ameloblastoma. Her history revealed that a wide resection of an ameloblastoma was carried out in 1960. The left ascending ramus and the distal part of the left mandibular body
Key words: Ameloblastoma; recurrences; radical resection. Accepted for publication 9 June 1988
were resected and reconstructed with a free iliac crest graft 3 months later. 16 years later, she presented with a recurrence of 6 cm in diameter, involving the left postero-lateral part of the soft palate, the left maxillary tuberosity, the retromolar zone and the tonsilar fossa. The biopsy confirmed the diagnosis of ameloblastoma. The tumor was resected in one piece, in-
Fig. 1. Case no. 1. CT-scan showing the chin area with the intraosseous tumor recurrence.
Recurrent ameloblastoma cluding the deep lobe of the parotid gland, the bonegraft and the pterygoid process, up to the base o f the skull. Frozen sections of the resection margins were negative, as were those o f the parotid lymphnodes. The intraoral defect was reconstructed with an island, pedicled, forehead-flap. 4 years later, the patient was re-admitted for atypical left trigeminal neuralgia. Neurological and radiological examinations revealed no detectable tumor. Alcoholization o f the trigeminal nerve at the level of the left foramen ovale was performed and the pain gradually decreased. In 1987 (27 years after the 1st treatment), pain and swelling in the chin area urged the patient to seek treatment again. A biopsy again revealed a recurrence (Fig. 1). Bonescintigraphy showed increased isotope-deposit in the distal part of the remaining mandibular body and in the 4th lumbal vertebra. CT-scanning with contrast-perfusion showed signs of possible intracranial invasion. N M R imaging of the cranial base showed a cystic process along the left carotid artery with destruction of surrounding bone including the sella turcica and extending posteriorly along the lateral side o f the pedunculus cerebri (Fig. 2). The 3rd division of the left trigeminal nerve below the foramen ovale had an irregular aspect, and this probably reflects the pathway of the intracerebral invasion. No neurological symptoms were present. The treatment consisted of resection of the symphysis with primary reconstruction by a free iliac crest graft to support the tongue and the chin. The intracerebral invasion has not been treated since it was symptomless. The same applies to the possible metastasis in the 4th lumbal vertebra, which has not yet been confirmed histologically. 6 months postoperatively, the patient is doing well. If necessary, palliative radiotherapy will be given.
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Fig. 2. Case no. 1. Intracranial invasion o f the ameloblastoma.
Case no, 2
A 49-year-old female was referred for treatment of a recurrent ameloblastoma. She complained of a painless swelling in the right cheek, which had slowly increased in volume during the last 3 years. She had first been treated for an ameloblastoma in the right mandible in 1957, at age 20 years. The tumor had been enucleated. A first recurrence was noted at age 29 years, at which time a hemimandibutectomy was carried out, saving the coronoid process. The reconstruction was performed by using an acrylic implant, l year later, the infected implant was removed and 2 months later, replaced by a free bone graft from the iliac crest. In 1986, the patient returned with a slowly growing swelling of the right cheek. The CTscanning, with contrast-perfusion, demonstrated a mass of 6 cm in diameter above the proximal part of the reconstructed mandible, with subcutaneous extension laterally and pushing the muscles of the floor of mouth caudally. Erosion of the maxillary sinus wall
Fig. 3. Case no. 2. Tumor recurrence in the right infratemporal fossa.
and slight infratemporal invasion were also noted. A Ferguson-Weber approach enabled the removal of the tumor, which was fixed to the remaining coronoid process. The whole block was resected together with the maxillary tuberosity and the pterygoid-plates including the contents of the pterygomaxillary fossa up to the base of the skull. The defect was packed to heal on secondary intention. Histopathological examination Showed no invasion of the tumor into the maxilla, but extension towards the cranial base. CT-scanning 4 months later revealed a tumor-mass in the infratemporal fossa (Fig. 3). This was promptly removed through a temporal approach, with resection of the zygo-
matic arch. The temporal muscle was dissected free and rotated into the defect, pedicled on its superficial vascular system. At present, one 18 months later, there is no sign of recurrence. Case no. 3
In 1976, a 46-year-old man had been treated for what at that time was interpreted as an infected follicular cyst of the left mandibular 3rd molar. Part of the cyst was left behind because o f difficulty in access. The histopathological diagnosis was multicystic ameloblastoma. The patient was immediately referred to our department for further evalu-
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Fig. 4. Case no. 3. Recurrent ameloblastoma in the iliac crest bonegraft.
Fig. 5. Case no. 4. Orthopantomogram showing the primary multicystic ameloblastoma in the left mandible.
ation and treatment. A left hemimandibulectomy was performed, including the condyle. The tumor had to be resected from the pterygoid-plates and the cranial base. 1 month later, the mandible was reconstructed using a free iliac bone graft. 10 years later, radiographs showed a recurrent lesion in the bone graft (Fig. 4). A biopsy revealed a recurrent ameloblast0ma. CTexamination showed invasion into the pterygomaxillary fossa. Surgical access was gained by a hemicoronal incision with preauricular extension along with an intraoral incision in the buccal sulcus. The proximal part of the bone graft was resected together with the left pterygoid plates, including a wide margin of surrounding soft tissues. No attempt was made to reconstruct the lost part of the graft. Healing was uneventful.
Histopathological examination showed invasion of the tumor into the soft tissues to the lateral aspect o f the bonegraft. Case no. 4
In 1973, a 67-year-old male was referred for diagnosis and treatment of a large multicystic tumor in the left mandibular angle. (Fig. 5). A biopsy lead to the diagnosis ameloblastoma. An intraoral hemimandibulectomy was carried out including the condyle, and the reconstruction was performed immediately with a free rib graft. It was noted at that time that the tumor was adherent to the mastieatory muscles. The rib graft had to be removed 2 months later because of infection and was replaced by a free iliac crest graft. The first recurrence became apparent 8
years later. It was located in the tendon of the temporal muscle, the infratemporal fossa, the parotid gland and in the distal portion of ~ the iliac crest graft (Fig. 6). A massive block resection was carried out including the above-mentioned structures. Reconstruction was achieved by a microvascular myocutaneous latissimus dorsi flap. The sections near the cranial base were free o f tumor. The facial paralysis was symptomatically corrected 1 month later by an eyebrow-lift, a partial tarsoraphy plasty and by lifting the corner of the mouth. An orthopantomogram by the end of 1983 showed an area suspicious of tumor. The CTscan localized the tumor in the left cheek, invading the buccal mucosa, and the cranial base. A radical resection was attempted, but left incomplete at the cranial base because of the poor prognosis in this 77-year-old man. A 3rd recurrence in the chin area was treated by a partial resection in September 1984. The patient recovered and did not need reconstructive surgery since he functioned well with what was left of the mandible. In May 1987, a swelling appeared in the anterior region of the floor of the mouth. Xrays and CT-scan revealed several recurfences, one of which extended from the chin to the hyoid bone and one at the left base of skull down to the soft palate. The right horizontal part of the remaining mandible also appeared to be invaded (Fig. 7). A 3rd operation was performed, including a resection o f the tumor at the left cranial base and the right mandible and chin. Because of the extensive soft tissue loss, a 2nd free latissimus dorsi flap with microsurgical anastomosis had to be brought in. To support the soft tissues and the tongue, a free rib graft was fixed to the right ascending ramus with a long plate. On the left side, no additional soft tissues were needed. Postoperatively, the patient was unable to swallow. A tracheostomy was necessary and nasogastric tube feeding was maintained for several months. The ribgraft underwent aseptic necrosis and was replaced by a free iliac crest flap with microvascular anastomosis. At present, swallowing is still difficult, but the soft tissues are again supported. Case no. 5
In November 1986, a 50-year-old patient was seen for a temporal and pre-auricular swelling. A follicular cyst of the left lower 3rd molar had been removed in 1957. She underwent surgery for a recurrent lesion at the same site in 1962. Further information on this procedure was not available, except that the histopathological diagnosis was ameloblastoma. A left hemimandibulectomy was carried out for a new recurrence in 1966, involving the coronoid and condylar process, and invading the soft tissues at the lingual side. No reconstruction was attempted at that time. A 3rd recurrence was detected medially of the left zygomatic arch (Fig. 8) in 1986 (29
Recurrent ameloblastoma
313
As shown by Mtiller & Slootweg26ameloblastoma, produces extensions into the bone marrow space well past the bone cavities demonstrable on radiographs. Particularly when the tumor has eroded through the cortical bone, finding its way into the soft tissues, diagnosis of the extent of the lesion becomes very difficult. In these cases, the surgeon has to rely on CT-scanning and NMRimaging to perform an adequate resection with reasonable margins of normal tissue. Frozen sections can be difficult to rely on because the presence of bone fragments, often makes it hard to process them well. This does not imply, however, that every case of solid ameloblastoma must be treated initially by a radical resection4. Treatment can certainly not be based upon histological patterns2~, 23, 2s, 3~. According to GARDNER • PE(~AK1°, one must consider the Fig. 6. Case no. 4. CT-scan showing the extent of the first recurrence. clinical type (introasseous solid or multicystic, unicystic, peripheral ameloblatoma) 2, the location7,16,30and the size of the tumor within the jaw bones 7. The solid or multicystic ameloblastoma is known to invade the intertrabecular spaces of cancellous bone without accompanying resorption of the trabeculae. It does not invade compact bone, although it may erode it Iv. If the treatment constits of enucleation, tumor cells may be left in the surrounding cancellous bone and the tumor may subsequently recur. This suggests that the most appropriate treatment for a small solid or multicystic ameloblastoma of the mandible is a conservative marginal resection with a 10 mm border of apparently uninvolved bone. Solid or multicystic ameloblastomas of greater size, especially when they tend to erode through the cortical plate of the mandible, need a more aggressive approach: segmental resection (without mainFig. 7. Case no. 4. The recurrence in the contralateral side is not in continuity with the 4th taining the continuity of bone) includrecurrence at the primary site. ing the overlying periosteum and also the overlying soft tissues26. The same years after the first operation). Through a malignant behaviour. It is a slowly approach is indicated in the case of temporal approach, the arch was resected growing, locally invasive tumor with a maxillary ameloblastoma because of and the tumor could be removed from the reported high recurrence rate if not reanatomical considerations. A recurcranial base. The left mandible was recon- moved adequately ~°, 24, 39. Since maligstructed with a free costochondral graft. The nant transtbrmation3,5,~9,33and metastarence in this region is often inoperable soft tissue defect was filled with a free suband must be avoided by all means. ses~2, ~3,22 are rare, it has been suggested mammary, dermofat-graft. 1 year after the In contrast to the solid or multicystic latest surgery, the patient is free of tumor. that one approach these tumors rather type, the unicystic ameloblastoma can conservatively 35. The free fat graft and the rib graft underwent initially be treated conservatively by The problem of recurrence can be slow aseptic necrosis. Definitive reconstrucsimple enucleation15,29.37or marsupializattributed to an inadequate resection of tive surgery is planned. ation and marginal resection4°. Microthe involved bone (particularly bone scopic examination should determine marrow), to the spreading of residual Discussion and conclusions whether there is involvement of the perbone fragments that contain tumor tisAmeloblastoma is a benign odontogenic sue and most of all to the inadequate iphery of the connective tissue wall of excision of the overlying soft tissues ~. the cyst. If there is, a secondary martumor which in rare instances may show
314
Demeulemeester et al.
Fig. 8. Case no. 5. Recurrent tumor on the left temporal fossa.
ginal resection is indicated, especially w h e n it concerns a n a m e l o b l a s t o m a o f the p o s t e r i o r maxilla 9. The 3rd i m p o r t a n t clinical type o f a m e l o b l a s t o m a is the rare p e r i p h e r a l a m e l o b l a s t o m a . It occurs m o s t comm o n l y in the m a n d i b u l a r gingiva a n d has a very low p o t e n t i a l for b o n y invasion 8, H, 14,32,39 It is treated by simple excision with a small m a r g i n o f n o r m a l tissue d o w n to b u t n o t necessarily including the periosteurn. In conclusion, the a u t h o r s w a n t to stress the i m p o r t a n c e of a careful clinico-radiological e v a l u a t i o n o f each case o f a m e l o b l a s t o m a to decide u p o n the best treatment. T h e experience o f these 5 extremely late recurrences, s o m e t i m e s at quite a distance f r o m the p r i m a r y tumor, illustrates t h a t some b e n i g n tumors can be so aggressive so as to necessitate wide a n d radical surgery. A careful follow-up is indicated in all amel o b l a s t o m a s to detect early recurrences, thus m a k i n g secondary surgery w o r t h while a n d preventing i n v a s i o n o f such vital areas as the o r b i t a n d the cranial base.
References 1. Baden, E.: Contribution ~ l'ktude de lameloblastome du maxillaire inf~rieur. Th~se, Facult6 de Medecine, Universit6 de Genrve, Berichthaus, Zfirich, 1964 2. Cannon, C.R. & Burnett, W.M.: Mandibular ameloblastoma. South Med. J. 1986: 79: 1446-1448. 3. Cart, R.F. & Halperin, V.: Malignant
ameloblastomas from 1953 to 1966. Oral Surg. 1968: 26: 514-522. 4. Crawley, W.A. & Levin, L.S.: Treatment of the ameloblastoma. A controversy. Cancer 1978: 42: 357-363. 5. Dararnola, J.O., Abioye, A.A., Ajagbe, H.A. & Aghadiuno, P.U.: Maxillary malignant anaeloblastoma with intraorbital extension: report of a case. J. Oral Surg. 1980: 38: 203-206. 6. Emmings, F.G., Gage, A.A. & Koepf, S.W.: Combined curettage and cryotherapy for recurrent ameloblastoma of the mandible: ~eport of a case. J. Oral Surg. 1971: 29: 41-44. 7. Eversole, L.R.: Clinical outline of oral pathology: diagnosis and treatment, 2nd edition, Lea & Febiger, Philadelphia, 1984: pp. 201-210. 8. Ficarra, G: & Hansen, L.S.: Peripheral ameloblastoma. A case report. J. Cranio.Max.-Fac. Surg. 1987: 15: 110-112. 9. Gardner, D.G., Morton, T.H. Jr. & Worsham, J.C.: Plexiform unicystic ameloblastoma of the maxilla. Oral Surg. 1987: 63: 221-223. 10. Gardner, D.G. & Pe~ak, A.M.J.: The treatment of ameloblastoma based on pathology and anatomic principles. Cancer 1980: 46: 2514-2519. 11. Guralnick, W., Chuong, R. & Goodman, M.: Peripheral ameloblastoma of the gingiva. J. Oral Maxillofac. Surg. 1983: 41: 536-539. 12. Harrer, W.V. & Patchevsky, A.S.: Mandibular ameloblastoma with intracerebral and pulmonary metastasis. Oral Surg. 1970: 29: 893-898. 13. Herceg, S.J. & Harding, R.L.: Malignant ameloblastoma with pulmonary metastases. Report of a case and review of the literature. Plast. Reconstr. Surg. 1972: 49. 456-460.
14. Horowitz, I., Hirshberg, A. & Dayan, D.: Peripheral ameloblastoma - a clinical dilemma in gingival lesions. J. Clin. Periodont. 1987: 14: 366-369. 15. Isacsson, G. Andersson, L. Forsslund, M. Bodin, I. & Thomsson, M.: Diagnosis and treatment of the unicystic ameloblastoma. Int J. Oral Maxillofac. Surg. 1986: 15" 759-764. 16. Kameyama, Y, Takehana, S., Mizohata, M., Nonobe, K.,Hara, M., Kuwai, T. & Fukaya, M.: A clinicopathological study of ameloblastoma. Int. J. Oral Maxillofac. Surg. 1987: 16: 706-712. 17. Kramer, I.R.H.: Ameloblastoma: a clinicopathological appraisal. Br. J. Oral Surg. 1963: 1: 13-28. 18. Krfiger, G.O.: Textbook of oral and maxillofacial surgery, 6th edition, The C.V. Mosby Company, St Loius, Toronto, 1984. 19. Larsson, A. & Almeren, H.: Ameloblastoma of the jaws. An analysis of a consecutive series of all cases reported by the Swedish Cancer Society during 1958-1971. Acta Pathol. Microbiol. Scand. 1978: 86: 337-349. 20. Lello, G.E. & Smith, I.: Ameloblastoma with multiple delayed recurrences: a case report. Head Neck Surg. 1987: 9: 295-298. 21. Lucas, R.B.: Pathology o f tumours o f the oral tissues. 4th edition, Churchill Livingstone, Edinburgh, 1984, pp. 30-59. 22. Madiedo, G., Choi, H., Kleinman, J.G.: Ameloblastoma of the maxilla with distant metastases and hypercalcemia. Am. J. Clin. Pathol. 1981: 75: 585-591. 23. Masson, J.K., McDonald, J.R. & Figi, F.A.: Adamantinoma of the jaws. A clinicopathologic study of 101 histologically proved cases. Plast. Reconstr. Surg. 1959: 23: 510-528. 24. Mehlisch, D.R., Dahtin, D.C. & Masson, J.K.: Ameloblastoma: a clinicopathologic report. J. Oral. Surg. 1972: 3 0 : 9 22. 25. Monks, F.T.: Treatment of adamantinoma by conservative surgery: a review. J. Oral. Surg. Anesth. Hosp. D. Serv. 1964: 22: 171-177. 26. Miiller, H. & Stootweg, P.J.: The growth characteristic of multilocular ameloblastomas. J. Max.-Fae. Surg. 1985: 13: 224-230. 27. Oka, K., Fukui, M., Yamashita, M., Takeshita, I., Fujii, K., Kitamura, K., Nakamura, S., Tashiro, H. & Masuda, S.: Mandibular ameloblastoma with intracranial extension and distant metastasis. Clin. Neurol. Neurosurg. 1986: 88: 303-309. 28. Prein, J., Remagen, W., Spiessl, B. & Uehlinger, E.: Atlas of tumors o f the facial skeleton, 1st edition, Springer Verlag, Berlin 1986, pp. 7-15. 29. Robinson, L., & Martinez, M.G.: Unicystic ameloblastoma. A prognostically distinct entity. Cancer 1977: 40: 22782285.
Recurrent ameloblastoma 30. Sehdev, M.K., Huvos, A.G., Strong, E.W., Gerold, ER, Willis, G.W.: Ameloblastoma of maxilla and mandible. Cancer 1974: 33: 324-333. 31. Shafer, W.G., Hine, M.K. & Levy, B.M.: A textbook of oral pathology, 4th edition, W.B. Saunders Company, Philadelphia, 1983: pp. 276-285. 32. Shiba, R., Sakoda, S. & Yamada, N.: Peripheral ameloblastoma. J. Oral Maxillofac. Surg. 1983: 41: 460M63. 33. Slootweg, RJ. & Miiller, H.: Malignant ameloblastoma or ameloblastic carcinoma. Oral. Surg. 1984: 57: 168-176. 34. Small. I.A. & Waldron, C.A.: Ameloblastoma of the jaw. Oral Surg. 1985: 8: 281-297. 35. Stout, R.A., Lynch, J.B. & Lewis, S.R.:
The conservative surgical approach to ameloblastoma of the mandible. Plast. Reconstr. Surg. 1963: 31: 554-562. 36. Tingchun, W., Zhe, C., Fengchen, T. Quanziang, T. & Citing, Y.: Ameloblastoma of the mandible treated by resection, preservation of the inferior alveolar nerve, and bone grafting. J. Oral Maxillofac. Surg. 1984: 42: 93-96. 37. Van de Vijver, H., Neyt, L., De Clercq, C., Bergmans, G. & MichMssen, R: Het ameloblastoom: naonderzoek bij zeven pati~nten. Rev. Belge. Med. Dent. 1987: 42: 43M9. 38. Van Geel, A.N., Van Slooten, E.A., Snow, G.B. & Van der Waal, I.: Het ameIoblastoom. Ned. Tijdschr. Geneeskd. 1977: 11: 442M46.
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39. Woo, S.B., Smith-Williams, J.E., Scimbla, J.J. & Sipper, S.: Peripheral ameloblastoma of the buccal mucosa: a case report and review of the English literature. Oral. Surg. 1987: 63: 78-84. 40. Yokobayashi, Y., Yokobayashi, T., Nakajima, T., Oyama, T., Fukushima, M. & Ishiki, T.: Marsupialization as a possible diagnostic aid in cystic ameloblastoma. J. Max.-Fac. Surg. 1983: 11: 137-141. Address: M. Mommaerts Department Stomatology, Maxillofacial and Head and Neck Surgery U Z St. Rqfa~'_l Kapucijnenvoer 7 B-3000 Leuven Belgium