Late Ioco-regional recurrences after radical resection for mandibular ameloblastoma

0ncology Luc J. -M. J. D e m e u l e m e e s t e r , Maur ice Y. Mommaer ts , 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 ameloblas toma are described with multiple recur- rences 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 tumor 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 non- invaded bone. I f the tumor has eroded through the cortical bone and invaded into the soft tissues, wider margins are necessary to eliminate possible tumor extensions that are left behind. Adequate follow-up on a regular basis should enable the clinician to detect early recurrence so as to avoid major surgery.

Key words: Ameloblastoma; recurrences; radical resection.

Accepted for publication 9 June 1988

The tendency of intraosseous amelo- blastoma to recur and to invade soft tissues is well documented. Radical re- section is generally accepted as im- perative and it h a s been proven to help in decreasing the number o f re- currences significantly 34. Radical resec- tion is designed to remove the tumor together with at least 1 cm of sur- rounding healthy tissue. Since the tu- mor is generally not well-defined, de- spite clinical and radiological examin- ation 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 recur- rences several years after resection 20. Few such recurrences are seen in a single surgeon's lifetime. Well-docu- mented long-term studies on the surgi- cal t reatment o f ameloblas toma are also rare. Therefore, conservative treatment, to reduce muti la t ion and morbidity, is sometimes recom- mended 4, 6, 18, 25, 36

5 cases will be presented to illustrate extremely late recurrences after radical resection. Finally, we will discuss a ra- tional approach to the t reatment 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 amelobla- stoma. Her history revealed that a wide re- section of an ameloblastoma was carried out in 1960. The left ascending ramus and the distal part of the left mandibular body

were resected and reconstructed with a free iliac crest graft 3 months later.

16 years later, she presented with a recur- rence 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.

cluding the deep lobe of the parotid gland, the bonegraft and the pterygoid process, up to the base of the skull. Frozen sections of the resection margins were negative, as were those of 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. Neuro- logical and radiological examinations reveal- ed no detectable tumor. Alcoholization of 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). Bone- scintigraphy showed increased isotope-de- posit in the distal part of the remaining man- dibular body and in the 4th lumbal vertebra. CT-scanning with contrast-perfusion showed signs of possible intracranial invasion. NMR- imaging of the cranial base showed a cystic process along the left carotid artery with de- struction of surrounding bone including the sella turcica and extending posteriorly along the lateral side of the pedunculus cerebri (Fig. 2). The 3rd division of the left trigeminal nerve below the foramen ovale had an irregu- lar aspect, and this probably reflects the path- way of the intracerebral invasion. No neuro- logical symptoms were present. The treat- ment 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 con- firmed histologically. 6 months postopera- tively, the patient is doing well. If necessary, palliative radiotherapy will be given.

Case no, 2

A 49-year-old female was referred for treat- ment of a recurrent ameloblastoma. She com- plained 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 amelobla- stoma 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 im- plant was removed and 2 months later, re- placed by a free bone graft from the iliac crest.

In 1986, the patient returned with a slowly growing swelling of the right cheek. The CT- scanning, with contrast-perfusion, demon- strated 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

Recurrent ameloblastoma 311

Fig. 2. Case no. 1. Intracranial invasion of the ameloblastoma.

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 maxil- lary tuberosity and the pterygoid-plates in- cluding 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 tu- mor-mass in the infratemporal fossa (Fig. 3). This was promptly removed through a tem- poral approach, with resection of the zygo-

matic arch. The temporal muscle was dis- sected free and rotated into the defect, ped- icled 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 of difficulty in access. The histopa- thological diagnosis was multicystic amelo- blastoma. The patient was immediately re- ferred to our department for further evalu-

312 Demeulemeester et al.

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, in- cluding 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 recur- rent lesion in the bone graft (Fig. 4). A biopsy revealed a recurrent ameloblast0ma. CT- examination showed invasion into the pterygomaxillary fossa. Surgical access was gained by a hemicoronal incision with pre- auricular 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 in- vasion 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 ameloblasto- ma. 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 mastiea- tory 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 myocutane- ous latissimus dorsi flap. The sections near the cranial base were free of tumor. The facial paralysis was symptomatically corrected 1 month later by an eyebrow-lift, a partial tar- soraphy plasty and by lifting the corner of the mouth.

An orthopantomogram by the end of 1983 showed an area suspicious of tumor. The CT- scan 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. X- rays and CT-scan revealed several recur- fences, 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 resec- tion of 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 pa- tient 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 micro- vascular 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 swell- ing. A follicular cyst of the left lower 3rd molar had been removed in 1957. She under- went 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 amelo- blastoma. 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

Fig. 6. Case no. 4. CT-scan showing the extent of the first recurrence.

Fig. 7. Case no. 4. The recurrence in the contralateral side is not in continuity with the 4th recurrence at the primary site.

years after the first operation). Through a temporal approach, the arch was resected and the tumor could be removed from the cranial base. The left mandible was recon- structed with a free costochondral graft. The soft tissue defect was filled with a free sub- mammary, dermofat-graft. 1 year after the latest surgery, the patient is free of tumor. The free fat graft and the rib graft underwent slow aseptic necrosis. Definitive reconstruc- tive surgery is planned.

Discussion and conclusions

Ameloblastoma is a benign odontogenic tumor which in rare instances may show

malignant behaviour. It is a slowly growing, locally invasive tumor with a reported high recurrence rate if not re- moved adequately ~°, 24, 39. Since malig- nant transtbrmation 3, 5, ~9, 33 and metasta- ses~2, ~3, 22 are rare, it has been suggested that one approach these tumors rather conservatively 35.

The problem of recurrence can be attributed to an inadequate resection of the involved bone (particularly bone marrow), to the spreading of residual bone fragments that contain tumor tis- sue and most of all to the inadequate excision of the overlying soft tissues ~.

As shown by Mtiller & Slootweg 26 ame- loblastoma, produces extensions into the bone marrow space well past the bone cavities demonstrable on radio- graphs. Particularly when the tumor has eroded through the cortical bone, find- ing its way into the soft tissues, diag- nosis of the extent of the lesion becomes very difficult. In these cases, the surgeon has to rely on CT-scanning and NMR- imaging to perform an adequate resec- tion 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 pro- cess them well. This does not imply, however, that every case of solid amelo- blastoma must be treated initially by a radical resection 4. Treatment can cer- tainly not be based upon histological patterns2~, 23, 2s, 3~. According to GARD- NER • PE(~AK 1°, one must consider the clinical type (introasseous solid or mul- ticystic, unicystic, peripheral amelobla- toma) 2, the location 7,16, 30 and the size of the tumor within the jaw bones 7.

The solid or multicystic ameloblasto- ma is known to invade the intertrabecu- lar spaces of cancellous bone without accompanying resorption of the trabec- ulae. It does not invade compact bone, although it may erode it Iv. If the treat- ment constits of enucleation, tumor cells may be left in the surrounding cancel- lous bone and the tumor may subse- quently 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 appar- ently uninvolved bone. Solid or multicy- stic ameloblastomas of greater size, es- pecially when they tend to erode through the cortical plate of the man- dible, need a more aggressive approach: segmental resection (without main- taining the continuity of bone) includ- ing the overlying periosteum and also the overlying soft tissues 26. The same approach is indicated in the case of maxillary ameloblastoma because of anatomical considerations. A recur- rence in this region is often inoperable and must be avoided by all means.

In contrast to the solid or multicystic type, the unicystic ameloblastoma can initially be treated conservatively by simple enucleation 15, 29.37 or marsupializ- ation and marginal resection 4°. Micro- scopic examination should determine whether there is involvement of the per- iphery of the connective tissue wall of the cyst. If there is, a secondary mar-

314 Demeulemeester et al.

Fig. 8. Case no. 5. Recurrent tumor on the left temporal fossa.

ginal resection is indicated, especially when it concerns an ame lob l a s toma of the pos ter ior maxil la 9.

The 3rd i m p o r t a n t clinical type o f ame lob la s toma is the rare per iphera l ameloblas toma. It occurs mos t com- monly in the m a n d i b u l a r gingiva and has a very low potent ia l for bony in- vas ion 8, H, 14, 32, 39 It is t reated by simple

excision wi th a small marg in o f n o r m a l tissue down to bu t no t necessarily in- cluding the periosteurn.

In conclusion, the au thors wan t to stress the impor t ance of a careful clin- ico-radiological eva lua t ion of each case of ame lob la s toma to decide upon the best t rea tment . The experience of these 5 extremely late recurrences, somet imes at quite a dis tance f rom the p r imary tumor, i l lustrates t ha t some ben ign tu- mors can be so aggressive so as to necessitate wide and radical surgery. A careful follow-up is indicated in all ame- lob las tomas to detect early recurrences, thus mak ing secondary surgery wor th while and prevent ing invas ion of such vital areas as the orb i t and the crania l base.

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Address: M. Mommaerts Department Stomatology, Maxillofacial and

Head and Neck Surgery UZ St. Rqfa~'_l Kapucijnenvoer 7 B-3000 Leuven Belgium