Journal of Cranio-Maxillofacial Surgery (2009) 37, 363e369 2009 European Association for Cranio-Maxillofacial Surgery doi:10.1016/j.jcms.2009.05.

.001, available online at http://www.sciencedirect.com

A treatment algorythmn for adult ameloblastomas according to the -Salpe trie ` re Hospital experience Pitie
Catherine ESCANDE, MD1, Andre CHAINE, MD1, Philippe MENARD, MD, PhD1, Didier ERNENWEIN, MD1, 2,3 Sonia GHOUL, DDS, PhD , Ayman BOUATTOUR, DDS2, Ariane BERDAL, DDS, PhD2, Jacques-Charles BERTRAND, MD, PhD1, Blandine RUHIN-PONCET, MD, PhD1,2 Stomatology and Maxillofacial Surgery Department (Pr Bertrand), Pitie -Salpe trie ` re University Hospital, Assistance Publique des Ho pitaux de Paris, Pierre et Marie Curie-Paris6 University, Paris F-75013, France; 2 INSERM UMR S 872, Orofacial Biology and Pathology Department (Pr Berdal), Equipe 5, Les Cordeliers; Rene Descartes-Paris5 University, UMR S 872, Paris F-75006, France; 3 Histology and Embryology Department, Dental Faculty of Monastir, Tunisia
1

SUMMARY. During a 13-year period (from 1994 to 2007), in the Oral and Maxillofacial Surgery Department of

-Salpe trie ` re Hospital, 116 new cases of adult ameloblastomas, were analyzed for treatment composed the Pitie against radiographic presentation, size, histological type. Follow-up and recurrence were also analyzed. Treatment was surgical consisting of enucleations (82%), segmental mandibulectomy (8.3%) resections (24.7%) 85% of them underwent reconstruction. The follow-up was documented for 97%. More than two recurrences occurred in 21% of the patients after the rst enucleation: 66% with a follicular histological diagnosis. Lenthly, a therapeutic algorythmn is suggested for adult ameloblastomas that underlines the importance of the conservative enucleation treatment as far as possible. 2009 European Association for Cranio-Maxillofacial Surgery Keywords: ameloblastoma, jaws, treatment, enucleation, mandibulectomy, algorythmn

INTRODUCTION Odontogenic tumours (OTs) are derived from epithelial, ectomesenchymal and/or mesenchymal elements of the tooth-forming apparatus. Their identication is based on the World Health Organization (WHO) classication (Pindborg et al., 1971) and the latest updated edition of OT histological typing (Barnes et al., 2005). These rare heterogeneous tumours yield signicant diagnostic and therapeutic challenges. Among them, ameloblastoma is a benign, but locally aggressive and inltrative OT. They can be intra-osseous (central) or extra-osseous (peripheral). Different histological types of ameloblastomas are described: follicular, cystic, unicystic, plexiform and mixed follicular-cystic, follicular-plexiform and follicular-cystic-plexiform types (Pindborg et al., 1971). They rarely metastasize but have a high tendency to recur because of the presence of satellite tumour cells. Ameloblastoma treatment is controversial and management is different according to surgical centres. On one hand, there is a school advocating major segmental or bloc resection for ameloblastoma with a requirement of 1e 1.5 cm of clinically and radiographically normal bone and uninvolved margins (Williams, 1993). On the other hand, there is a school advocating a more conservative surgical management by enucleation with adjacent bone curettage (with or without periostal resection) (Himmelfarb and Goodstein, 1972; Huffman and Thatcher,
363

1974; Muller and Slootweg, 1985; Haidar and Al-Gailani, 1987; Lello and Smith, 1987; Bataineh, 2000; Nakamura et al., 2002). There is also an intermediary behaviour proposed by Sachs (2006) consisting of surgical excision with peripheral ostectomy. Examination of a large retrospective series should then allow conclusions and establishment of a therapeutic algorythmn. Therefore, all cases of ameloblastomas diagnosed and followed in the Oral and Maxillofacial Surgery Clinic of the Pitie -Salpe trie ` re Hospital have been retrospectively reviewed from 1994 to 2007. This is also the rst large European and French follow-up report. MATERIAL AND METHODS Case les and biopsy reports of adult patients who presented with an ameloblastoma, during the period from 1994 to 2007, were retrieved from the records of both the Stomatology, Maxillofacial and the Pathology Departments of the Pitie -Salpe trie ` re Hospital. In order to focus treatment management of ameloblastoma, we studied more accurately three parameters. Radiological aspects of the lesions were rst analyzed (mandibular or maxillary, unilocular or multilocular): two cases of peripheral ameloblastomas were then excluded of the study. Lesion sizes were also placed into

364 Journal of Cranio-Maxillofacial Surgery Table 1 e Treatment of unilocular ameloblastomas considering their location and their size Treatment of unilocular ameloblastomas (44 cases) Location/size Symphysis and para-symphysis, n 8 Horizontal ramus, n 13 Angle and vertical ramus, n 16 Corono d process and cranial base, n 4 Maxilla, n 3 \5 cm 4 Enucleations, 1 enucleation unicystic 5 Enucleations, 2 enucleations (unicystic) 7 Enucleations, 1 enucleation unicystic 2 Enucleations 2 Enucleations From 5 to 13 cm 1 Enucleation, 1 IM, 1 IM after enucleation 4 enucleations, 1 IM, 1 unicystic: enucleation 8 Enucleations 2 IM after enucleation 1 Enucleation .13 cm 0 0 0 0 0

Table 2 e Treatment of multilocular ameloblastoma considering their location and their size Treatment of multilocular ameloblastomas (65 cases) Location/size Symphysis and para-symphysis, n 14 Horizontal ramus, n 28 Angle and vertical ramus, n 7 Corono d process and cranial base, n 12 Maxilla, n 4 \5 cm 3 Enucleations, 2 NIM after enucleation 7 Enucleations, 1 NIM, 1 IM after enucleation 1 Enucleation, 1 NIM after enucleation 1 NIM after enucleation 1 Enucleation From 5 to 13 cm 3 Enucleations, 3 IM after enucleation 8 Enucleations, 3 NIM (2 as primary procedures), 3 IM (2 at primary surgery) 5 Enucleations 1 Enucleation, 4 IM, 4 IM after enucleation 3 Enucleations .13 cm 1 Enucleation, 1 NIM, 1 IM 5 IM (3 in rst intention)

1 IM, 1 enucleation

three groups: less than 5 cm, between 5 and 13 cm and more than 13 cm (corresponding to the group of the giant ameloblastomas). Then, jaw locations were studied. Regarding site, the maxilla was divided into three regions: anterior, premolar and molar areas. The mandible was divided into ve areas: symphysealeparasymphyseal, horizontal ramus, angle, vertical ramus, coronoid process and cranial base. For each parameter, therapeutic modalities were then noted: enucleationecurettage, segmental bloc resection, radical resection and radical resection with reconstruction. Enucleation (with or without curettage) consists of a single tumour removal by a slow, smooth surgical approach avoiding as far as possible any tumour spillage (it can be associated with curettage accompanied by abrasion of the adjacent osseous wall of the cavity using a mechanical or chemical method). A segmental bloc resection consists of a limited box bone resection of the tumour, the adjacent bone and sometimes the adjacent periosteum suspected as being invaded by the tumour; it doesnt attempt the jaw osseous continuity. Radical resection involves a discontinuity defect of the jaw. Reconstructive surgery can then be undertaken with a bone graft, an osseous free ap (for example a bula free ap or an iliac free ap). Then, histological analysis should produce a denitive diagnosis. Follow-up and recurrence rate have been noted for each case. Data were analyzed using the statistical software SigmaPlot version 2. RESULTS A total of 114 patients corresponding to 202 central (intra-osseous) ameloblastomas were examined; 109 were operated upon and followed-up during that 13-year

period (from 1994 to 2007). Two were lost, one after nearly 13 years and one after 2 years. Cases of recurrent ameloblastomas accounted for the discrepancy observed between the number of patients and pathology cases. In order to rene the therapeutic management of ameloblastomas, we have correlated the treatment of the three chief features (radiological aspect, size and location). Concerning the radiographic presentation, 65 patients (59.6%) had a multilocular radiolucent lesion and 44 (40.4%) had unilocular lesion. Forty-two patients (38.6%) presented initially with a lesion of less than 5 cm For 57 patients (52.3%), the size was between 5 and 13 cm, and the last group had lesions longer than 13 cm (10 patients, 9.1%). This last group was classied as giant ameloblastoma. As for the initial location, we found that seven cases (6.5 %) of ameloblastomas were located in the maxilla and 102 cases (93.5%) in the mandible. In the mandible, 22 cases (21.5%) of ameloblastomas were in the symphysis/para-symphysis area, 44 cases (43.2%) in the horizontal ramus and 36 cases (35.3%) in the angle. We have then studied the way of extension involving the symphysis area, the mandibular arch, the angle, the ramus and the cranial base. We counted 36 cases (33%) of follicular type, 28 cases (24.6%) cystic, 3 cases (2.75%) plexiform, 29 cases (27%) of folliculo-cystic type, three cases (2.75%) of folliculo-plexiform type and three follicular, plexiform and cystic cases (2.75%). One (0.9%) was basaloid and one (0.9%) acanthotic. Only ve cases (4.6%) were unicystic lesions. A total of 197 surgical interventions were performed during 13 years. Five patients had no denitive treatment because they did not attend to honour their appointments. One hundred and sixty-one enucleations were performed (corresponding to 82% of the surgical treatments) on 91 patients (83%). Seventy-three patients

Treatment algorythmn for adult ameloblastomas 365

Radiographical features Unilocular or Multilocular ameloblastoma

5 cm

Size

Size < 5 to 13 cm >

Giant size 13 cm

One large or several medium soap bubbles

Cystic aspect and little peripherical bubbles

Cortical and/or basilar lysis +/- soft tissue involvement Maxillectomy or interruptive mandibulectomy with resection of the periosteum +/- the attached muscles

Ramus sigmoid process and coronoid process +/- cranial base involvement

Temporal fossa involvement

Enucleation curettage

Osseous and tumoral box resection with 1 cm safe margins (maxillectomy or non interruptive mandibulectomy) +/- periostectomy

Interruptive mandibulectomy with desarticulation and resection of the attempted periosteum and muscles

Zygomatic arch section and tumorectomy

Bone reconstruction by iliac bone graft, fibula or iliac free flap

Follow-up Rcurrence
Fig. 1 e Treatment algorythmn. A therapeutic distinction is made between enucleation, osseous bone resection, limited radical resection with reconstruction, large radical resection with reconstruction and coronoid process involvement leading to a radical resection with disarticulation.

Fig. 2 e Case of a limited ameloblastoma enucleation. a: Radiograph before treatment: unilocular ameloblastoma involving right mandibular horizontal ramus with premolar and molar root resorption (arrows). b: Radiograph after ameloblastoma enucleation: the mandibular bone continuity is preserved (arrow). c: Radiograph 1 year later, showing spontaneous bone regrowth in the enucleation cavity (arrow).

Fig. 3 e Case of a large ameloblastoma enucleation. a: Radiograph before treatment: multicystic ameloblastoma with mandibular left angle and horizontal branch involvement (arrows). The coronoid process is not invaded. b: Radiograph after a large enucleation showing the cavity and the preserved osseous margins (arrow). Radiographs after 1 year (c) and 3 years (d) showing a spontaneous osteogenesis (arrows). No recurrence was evident.

(67%) had only enucleations. Forty-three patients (39.4%) have undergone unique enucleation. Sixteen patients (14.7%) have undergone two enucleations and nine patients (8.3%) required three enucleations and ve patients (4.6%) had had four enucleations to arrest disease without any other treatment. Nine patients (8.3%) have undergone a segmental mandibulectomy (non-interruptive mandibulectomy (NIM)). In this subgroup, ve patients (4.6%) have rst had an enucleation before mandibulectomy while four patients (3.7%) have undergone a primary local bone resection: one patient had only one enucleation, two patients had two enucleations, one patient had three enucleations and one patient had four enucleations before segmental mandibulectomy. Among the 27 patients (24.7%) with a mandibular resection (interruptive mandibulectomy: IM), 13 patients (11.9%) had an enucleation rst: seven patients had one enucleation, three patients had two enucleations, two patients had three enucleations and one had eight enucleations before mandibulectomy. Fourteen patients

366 Journal of Cranio-Maxillofacial Surgery

Fig. 4 e Case of an osseous bloc resection. a: Multilocular ameloblastoma with soap bubbles located in the incisor area of the mandibular symphysis (arrows). b: osseous bloc resection leaving in place the mandibular arch (arrows).

previously had a mandibulectomy. Twenty-three patients (21%) had a mandible reconstruction (six iliac grafts, two iliac free aps, and 20 bula free aps) after initial surgery. The different treatments decided for unilocular and multilocular ameloblastomas, considering the location and size of the lesion are detailed in Tables 1 and 2. Of all the patients having undergone surgery, 109 patients (96%) were followed-up after their last treatment. Follow-up records of all the treated cases were available for between 6 months and 13 years (with a median period of 5 years). Sixty-one patients (56%) had no recurrence during that period; 24 patients (21%) had one recurrence, 14 patients (13%) had two recurrences, eight had three recurrences (7.2%), one patient (0.9%) had four recurrences and one patient (0.9%) had eight recurrences. Among them, 16 cases were follicularecystic (33%), 16 cases were follicular (33%) and 10 cases were cystic (21%). Concerning the unicystic ameloblastomas (ve cases in our study), two patients had no recurrence and three patients had one recurrence. DISCUSSION Treatment of adult ameloblastomas is different according to surgical teams and remains a controversial issue (Sehdev et al., 1974; Gardner and Pecak, 1980; Muller and Slootweg, 1985; Gold et al., 1991; MacIntosh, 1991; Williams, 1993). Choosing between radical or conservative treatment could be a real dilemma although they are both supposed to have the same aim, removing the tumour. A radical approach may be justied in the case of a late presentation, involvement of cranial base or temporal fossa, poor patient compliance or in countries where it would be difcult to follow-up patients (Crezoit et al., 2003), as described in Maghreb (Jeblaoui et al., 2007). The approach to management in African series is then quite radical: resection is the predominant form of surgical treatment with 72.2% of patients in a Nigerian children series (Arotiba et al., 2005). This radical approach is similar to our philosophy to deal with large adult ameloblastomas coming from foreign countries. But, these large ameloblastomas provide several management challenges, including a long and complicated

Fig. 5 e Ameloblastoma involving left angle and horizontal ramus requiring a limited radical resection with a bula free ap reconstruction using a double barrel technique.

surgical procedure which involves mandibular disarticulation at the temporomandibular joint. Reconstruction of the mandible and post-operative rehabilitation produces difculties relating to eating and speaking (Ghandhi et al., 2006), and often such patients can lead miserable lives because of pain and loss of facial symmetry. In order to reduce morbidity, a Taiwan team proposed an immediate reconstruction using a bula free ap with endosteal implants for large mandible ameloblastomas (Chana et al., 2004). We agree with that reconstructive approach which has become possible since the introduction of free aps. Although, the management of giant ameloblastomas (greater than 13 cm) is widely accepted as requiring a radical (but as little as possible) mandibulectomy, it remains controversial for small and medium ones. These are more often managed conservatively (Muller and Slootweg, 1985; Nakamura et al., 2002; Sachs, 2006). This varies between teams: marsupialization (Nakamura et al., 1995), or enucleation dened by Gardner and Pecak (1980), as the removal of a lesion by shelling it out intact. Sampson and Pogrels (1999) team (prefers to call it curettage recommending that the term enucleation should be abandoned. Teams favour a more radical approach as described by Carlson and Marx (2006) underlining that ameloblastomas may inltrate tissues

Treatment algorythmn for adult ameloblastomas 367

Fig. 6 e Case of a large resection. a: Patient presenting with a giant mandibular ameloblastoma with tooth displacements. b: Panoramic radiograph showing giant ameloblastoma leading to the severe mandibular resorption from right angle to left angle (arrows). c: Panoramic radiograph after a radical resection and a mandible reconstruction by a bula free ap with endosteal implants.

2e8 mm further than it is radiologically evident and advocating major segmental or bloc resection based on a requirement of 1e1.5 cm of clinical and radiographically normal bone to ensure clear margins (Mehlisch et al., 1972; Gardner and Pecak, 1980; Sammartino et al., 2007). In 2007, Sammartino et al. use the term of box resection when bone around cyst is also removed and Nakamura et al. (2002) speak of radical surgery with a safety margin of at least 1 cm of normal bone. We chose the term enucleation for cyst removal when it is located in bone and does not involve soft tissues. This treatment is always followed by bone curettage consisting of removing of the surrounding bone, when the lesion is unilocular or multilocular with soap bubbles. We use the term resection when it is necessary to take margins, resections of bone or soft tissues, usually when enucleations may leave tumour cells.

Gardner (1984, 1996) recommends separation of ameloblastomas into solid or multicystic, unicystic and peripheral types. Indeed, the prognosis for the unicystic and peripheral ameloblastomas is so much better after a limited surgical procedure such as enucleation, enucleationecurettage and simple excision than it is for a solid or multicystic ameloblastomas. As for Ueno et al. (1989), in conservative surgery, the recurrence rate of multicystic ameloblastomas was signicantly higher in multilocular or soap bubble type (60.7%) than in the unilocular type (35%). A major factor is cancellous bone inltration by ameloblastomas, but is largely conned by compact bone of the mandible inferior border and ascending ramus. That explains the recurrence rate obtained after enucleation of multicystic ameloblastomas without cautery or removal of surrounding bone. We have noted that radical segmental resection was performed in cases of multilocular ameloblastomas not approachable by enucleation (Gardner, 1984, 1996) but also in the case of large ameloblastomas (because of bone invasion and the impossibility of preserve the jaw without a high risk of recurrence). We underline the importance of bone and soft tissue margins in these cases: recurrences can occur in grafts or free aps if the resection is inadequate, especially if periostal margins are not respected. Tumour location is the second major factor affecting the behaviour and the more adapted treatment of ameloblastomas. The nearer the ameloblastoma is to vital structures, the higher is the risk of inltration. In the case where extension occurs to the mandibular vertical ramus and coronoid process, a large radical resection will avoid invasion into the temporal fossa, the pterygomaxillary fossa and cranial base. By the same means, a posterior maxilla location has to be treated by resection to avoid a possible extension into the orbital cavity, the pterygomaxillary fossa and the cranial base. As for examples, Feinberg and Steinberg (1996) recommend resection (avoiding enucleation or curettage) for large lesions located from bicuspid to condyle; Chapelle et al. (2004) adopt this attitude for unicystic and multicystic lesions. The CT-scan can be useful to identify relationships between the lesion and bone whereas MR is better for soft tissue denitions (Sampson and Pogrel, 1999). Recurrence rates are not always reported. Kim and Jang (2001) and Ogunsalu (2003) respectively reported 17.1% and 21.1% of recurrences. The reported recurrence rates after resection vary from 0% to 25% (Muller and Slootweg, 1985). In our series, upon 13 years, the recurrence rate was 45% (21% with only one recurrence and 21% with two recurrences or more). That appears poor but in the management of this benign OT, our philosophy is to be as minimally aggressive as possible, choosing at rst enucleation when it is possible, in order to conserve osseous volume and to decrease the morbidity which follows radical segmental resection. This philosophy is also possible in our centre where the follow-up is stringent and respected by patients. We also agree with Adebayo et al. (2002) that prolonged follow-up is necessary for these patients. While radiological appearance, size and location are important in treatment decisions (Olaitan and Adekeye,

368 Journal of Cranio-Maxillofacial Surgery

Fig. 7 e a: Case of a patient addressed for ameloblastoma recurrence and right temporal fossa involvement (arrows). b: Axial CT-scan view of the right coronoid process involvement (arrows). c: Frontal CT-scan view showing ramus, coronoid, cranial base and temporal fossa involvement (arrows). d: Fibula free ap reconstruction after a large resection by a trans-zygomatic approach and a mandibular disarticulation.

1996), there is also a signicant relationship between recurrence and histological type (Wu et al., 1984; Ueno et al., 1989). In our study, most recurrences appear in follicular or follicular and cystic types: 42% of follicular types had recurrences and 51.6% of follicular and cystic type. Ueno et al. (1989), using conservative surgery, showed a recurrence rate signicantly higher in the follicular type (56.8%) than in the plexiform type (32.4%). According to Hong et al. (2007), there is a signicant correlation between recurrence, treatment method and histopathological type. The difference between the resection with bone margin and radical segmental resection groups was not signicant. A resection with safety margin is the best method to treat most proven ameloblastomas, and conservative treatment is reasonable for patients in their rst decades or with unicystic or plexiform ameloblastomas. Although they possess a much better prognosis after enucleation or curettage (Reichart et al., 1995), unicystic ameloblastomas (ve cases in our series) are liable to recur (15% according to Gardner, 1996): two cases had no recurrence and three cases had one recurrence in this series. In this study, the treatment of ameloblastomas was conservative. As far as possible, enucleation was used rst to conserve bone continuity and to reduce morbidity. Resection involves complete tumour removal with a clearance of at least 1 cm of apparently normal bone on all sides of the lesion (MacIntosh, 1991; Olaitan

et al., 1993; Olaitan and Adekeye, 1996). Mandibulectomy was used for giant ameloblastomas, when tumour involvement extended to the cranial base and when recurrence was of the follicular type (14/16). According to these results and considering the three main parameters (radiographic presentation, size and location), we propose a therapeutic algorythmn for ameloblastomas (Fig. 1). A therapeutic distinction is drawn between enucleation (Figs. 2 and 3), osseous bone resection (Fig. 4), limited radical resection with reconstruction (Fig. 5), large radical resection with reconstruction (Fig. 6) and coronoid process involvement leading to a radical resection with disarticulation (Fig. 7). CONCLUSION Treatment of a patient with an ameloblastoma should be based on accurate clinical details, radiographs, special imaging and a representative biopsy, followed and reviewed by an oral pathologist and a maxillofacial surgeon. This study provides information about the therapeutic management of 114 adult cases of ameloblastomas, seen in our department over a 13-year period (1994e2007). This large series allowed us to propose a treatment algorythmn for adult ameloblastomas based on radiographic appearance, size and location. Each case is unique and has to be considered in the clinical

Treatment algorythmn for adult ameloblastomas 369

context and the relationship of the lesion to surrounding tissues, histological type and recurrence rate. It remains each clinicians responsibility to formulate an individual surgical plan for each patient: a therapeutic algorythmn is just a guide.
ACKNOWLEDGEMENTS

To Professor Francis Guilbert (y): his clinical and surgical experience allowed this work and analysis. To the past and present practicians of the Stomatology and MaxilloFacial Surgery Department. References
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Blandine RUHIN-PONCET, MD, PhD and Catherine ESCANDE, MD Stomatology and Maxillofacial Surgery Department Pitie -Salpe trie ` re University Hospital Pierre et Marie Curie-Paris6 University 47-83 boulevard de lHo pital 75651 Paris Cedex 13 France Tel.: +33 1 42 16 13 05 Fax: +33 1 42 16 13 69 E-mail addresses: catherine.escande@psl.aphp.fr (C.E.) blandine.ruhin@psl.aphp.fr (B.R-P.) Paper received 15 September 2008 Accepted 22 May 2009