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Total mandibular reconstruction after resection of rare “honeycomb-like” ameloblastic carcinoma – A case report
Journal of Cranio-Maxillo-Facial Surgery (2010) 38, 465e468 Ó 2009 European Association for Cranio-Maxillo-Facial Surgery doi:10.1016/j.jcms.2009.10.020, available online at http://www.sciencedirect.com
Total mandibular reconstruction after resection of rare ‘‘honeycomb-like’’ ameloblastic carcinoma e A case report Jelena V. JEREMIC, MD1, Zivorad S. NIKOLIC, MD, DDS, PhD2, Ivan V. BORICIC, MD, PhD3, Zoran D. TACEVIC, MD, PhD1, Nada R. TOMANOVIC, MD3, Lazar J. DRCIC, DDS2, Milijanka D. NOVKOVIC, MD1 1
Clinic for Burns, Plastic and Reconstructive Surgery (Chief: Prof. Miodrag Colic), Clinical Centre of Serbia, Zvecanska 9, Belgrade, Serbia; 2 Clinic for Maxillofacial Surgery (Chief: Prof. Miodrag Gavric), Faculty of Stomatology, Dr Subotica 4, Belgrade, Serbia; 3 Institute for Pathology (Chief: Prof. Gordana Basta), Faculty of Medicine, Dr Subotica 1, Belgrade, Serbia
Purpose: This case report describes a rare and aggressive ameloblastic carcinoma that infiltrated the mandible in a ‘‘honeycomb’’ pattern. Methods: A total mandibulectomy with bilateral modified neck dissection was followed by primary reconstruction with a single free vascularised fibula flap. Results: The postoperative course was uneventful. The one year follow-up revealed no signs of recurrent tumour or metastases. Nine months later distant metastases occurred in the lung. Conclusion: Ameloblastic carcinoma is a highly malignant lesion, which requires aggressive therapy. Prognosis is poor. Further reporting of ameloblastic carcinoma is encouraged. Ó 2009 European Association for Cranio-Maxillo-Facial Surgery
SUMMARY.
Keywords: ameloblastic carcinoma, mandible, reconstruction, free fibula
excision of extremely rare and malignant ameloblastic carcinoma that involved the entire mandible.
INTRODUCTION Ameloblastic carcinoma is an extremely rare, aggressive odontogenic malignant neoplasm of the jaws, predominantly the mandible. Odontogenic tumours were classified by the World Health Organisation in 1971, and a modified classification was published by Slootweg and Muller (1984), which is still widely accepted. Most ameloblastic carcinomas are presumed to arise de novo, with less than 1% of ameloblastomas that undergo malignant transformation. As a highly aggressive lesion with ill-defined margins and cortical destruction, ameloblastic carcinoma has a poor prognosis due to local recurrence, and regional and distant metastasis, frequently to the lungs, and to a lesser extent to the vertebrae and viscera. The prognosis still appears to be poor, but the paucity of documented cases with long term follow up does not permit accurate assumptions to be made (Slater, 2004). Loss of mandible continuity results in alteration in speech, swallowing and mastication, and in the appearance of the patient. The restoration of a defect that involves the entire mandible is a rare and challenging problem for surgeons after ablation of malignant and aggressive tumours. Vascularised fibula transfer has become the preferred method of mandible reconstruction after oncologic surgical ablation. The fibula flap was firstly described by Taylor et al. (1975) and was used for the first time in mandibular reconstruction by Hidalgo (1989). We report a vascularised fibula free flap in the reconstruction of a total mandibular defect after radical
CASE REPORT A 58-year-old male patient with previously histopathologically diagnosed ameloblastic carcinoma of the mandible was admitted to the Department of Maxillofacial Surgery, Belgrade. The patient had suffered from bilateral lower lip numbness and diffuse swelling affecting the whole mandible without any mucosal or skin ulceration. Panoramic and computed tomography (CT) examination revealed small honeycomb-like osteolytic changes extending up to the condylar neck region bilaterally. (Fig. 1a, b, c, d) The total mandibulectomy with bilateral modified neck dissection was followed by primary reconstruction with 28 cm long free vascularised fibula flap. In order to achieve the desired mandible form, the graft was shaped by four subperiosteal osteotomies and fixed using mini plates (Fig. 2). The neomandible was also fixed to the existing healthy condylar processes on both sides. The flap pedicle was anastomised to the right facial artery and internal jugular vein. The specimen was subjected to a full histopathological examination with immunohistochemical analysis. The tumour was composed of nests and islands of basaloid cells within a collagenous, mature stroma. In focal areas, tumour cell nests demonstrated peripheral palisading of columnar cells enclosing a stellate reticulum type zone. 465
466 Journal of Cranio-Maxillo-Facial Surgery
Fig. 1 e Clinical (a) extraoral and intraoral (b) appearance with no mucosal or skin ulcerations. Panoramic (c) and CT (d) findings revealing ‘‘honeycomb-like’’ osteolytic changes of entire mandible (from one to another condylar neck) with multiple cortical perforations.
Fig. 2 e A 28 cm long harvested free fibular graft after remodeling.
More than fifty metastatic nodules of ameloblastic carcinoma were found in soft tissue of the neck region (Fig. 3a). Malignant tissue of ameloblastic carcinoma was present only in one lymph node from 25 lymph nodes present in vast surgical material. This node was infiltrated by ameloblastic carcinoma through lymph node capsule, without actual lymphatic spread (Fig. 3b). At the cytological level, the epithelial component exhibited overt cytological malignancy including pleomorphism, hyperchromatic nuclei, and high mitotic rate. In addition, perineural invasion was noted (Fig. 3c). The one year follow-up revealed no signs of recurrent tumour or metastasis. The postoperative CT findings were regarded as normal. The whole body examination showed no atypical findings (Figs. 4 and 5). Nine months later, distant metastases occurred in the lung, and further chemo and radiotherapy was administered. The adjuvant radiation therapy was not successful, and the patient subsequently died. DISCUSSION Ameloblastic carcinoma is a rare malignant epithelial neoplasm that is associated with an ameloblastoma
(then termed e carcinoma ex ameloblastoma), or histologically resembles an ameloblastoma e de novo ameloblastic carcinoma. Cytological atypia and mitotic activity rate are higher in ameloblastic carcinoma than ameloblastoma (Slater, 2004). Nagai et al. (1991) reported 46 ameloblastic carcinoma in English and Japanese literature. According to Lolachi et al. (1995), a total of 34 cases of ameloblastic carcinoma were reported in the English literature. Since then, a few additional case reports have been published (Corio et al., 1987; Simko et al., 1998; Cizmecy et al., 2004). The common clinical signs and symptoms of the disease include swelling, pain, trismus and dysphonia (Corio et al., 1987). Lower lip numbness and diffuse swelling were the only signs that were found in our patient. The age range of patients with a diagnosis of ameloblastic carcinoma shows large variation, with a reported mean age of 30 years, and no sex predilection that has been reported (Corio et al., 1987). Ameloblastic carcinoma is an aggressive neoplasm that is locally invasive and can spread to regional lymph nodes or distant sites, such as lungs and bones Kuriakose et al. (2003). Local invasion often extends out of bone to involve infratemporal fossa, parapharyngeal space, the masticator space or cervical soft tissue (Slater, 2004). This unique case demonstrated an unusual spreading pattern of the ameloblastic carcinoma which infiltrated the entire mandible in a ‘‘honeycomb’’ pattern. The tumour showed perineural invasion and also invasion of soft tissue of the neck region with lymph node infiltration. After mandibular reconstruction there was no local recurrence of the tumour, although in the later course of the disease there were distant metastases to the lung, despite apparently adequate control of the primary mandibular neoplasm. As there are very few documented cases in the literature, it is difficult to make a definitive recommendation regarding treatment. Because of its aggressive behaviour with extensive local destruction, the treatment of ameloblastic carcinoma should include wide local excision that could extend even to total mandibulectomy. Parotidectomy and regional lymph node dissection should also be considered. Radiation to both the tumour and neck bed, and chemotherapy seem to be of limited value
Total mandibular reconstruction after resection of rare ‘‘honeycomb-like’’ ameloblastic carcinoma 467
Fig. 3 e a. Ameloblastic carcinomaemetastasis in the soft tissue of the neck, haematoxylin & eosin 25. b. Ameloblastic carcinoma infiltrating lymph node capsule (thin arrow). On this slide there is also one smaller lymph node without malignant tissue (thick arrow), and soft tissue metastasis of ameloblastic carcinoma (arrowhead). c. Signs of perineural invasion.
Fig. 4 e Postoperative panoramic view of reconstructed mandible.
(Nagai et al., 1991; Lolachi et al., 1995; Infante-Cossio et al., 1998; Simko et al., 1998). We performed a radical tumour resection that included total mandibulectomy with bilateral modified neck dissection. The matter of restoring a total mandiblular defect is a rare and challenging problem for surgeons after ablation of malignant and aggressive tumours. Microvascular techniques to transfer vascularised bone to the head and neck region have been successfully applied to solve the problem of various segmental mandible defects (Urken et al., 1998; Cordeiro et al., 1999; Pohlenz et al., 2007). In our case, the entire mandible was successfully reconstructed with a single vascularised fibula flap. CONCLUSION Ameloblastic carcinoma is a rare odontogenic carcinoma which is highly malignant. It is an aggressive tumour
Fig. 5 e Patient appearance one year postoperatively.
468 Journal of Cranio-Maxillo-Facial Surgery
presenting a very unusual spreading pattern. Rarity of well documented cases and unpredictable clinical behaviour of ameloblastic carcinoma preclude definitive recommendation regarding treatment. Close follow-up of the patient is needed. Prognosis is usually poor. CONFLICT OF INTEREST None. References Cizmecy O, Aslan A, Onel D, Demiryont M: Ameloblastic carcinoma ex ameloblastoma of the mandible: a case report. Otolaryngol Head Neck Surg 130: 633e634, 2004 Cordeiro PG, Disa JJ, Hidalgo DA, Hu QY: Reconstruction of the mandible with osseous free flaps: a 10-year experience with 150 consecutive patients. Plast Reconstr Surg 104(5): 1314e1320, 1999 Corio RL, Goldblatt LI, Edwards PA, Hartman KS: Ameloblastic carcinoma: a clinicopathologic study and assessment of eight cases. Oral Surg Oral Med Oral Pathol 64(5): 570e576, 1987 Hidalgo DA: Fibulae free flap: a new method of mandible reconstruction. Plast Reconstr Surg 84: 71e79, 1989 Infante-Cossio P, Hernandez-Guisado JM, Fernandez-Machin P, Garcia-Perla A, Rollon-Mayordomo A, Jose L, Gutierrez-Perez JL: Ameloblastic carcinoma of the maxilla: a report of 3 cases. J Craniomaxillofac Surg 26(3): 159e162, 1998 Kuriakose MA, Rigual NR, Hicks Jr WL: Ameloblastic carcinoma: report of an aggressive case with multiple bony metastases. Am J Otolaryngol 24: 66e69, 2003 Lolachi CM, Maden SK, Jacobs JR: Ameloblastic carcinoma of the maxilla. J Laryngol Otol 109(10): 1019e1022, 1995
Nagai N, Takeshita H, Nagatsuka M, Inoue M, Nishijima K, Nojima T, Yamasaki M, Hoh C: Ameloblastic carcinoma: a case report and review. J Oral Pathol Med 20: 460e463, 1991 Pohlenz P, Blessmann M, Heiland M, Blake F, Schmelzle R, Li L: Postoperative complications in 202 cases of microvascular head and neck reconstruction. J Craniomaxillofac Surg 35: 311e315, 2007 Simko EJ, Brannon RB, Eibling DE: Ameloblastic carcinoma of the mandible. Head Neck 20: 654e659, 1998 Slater LJ: Odontogenic malignancies. Oral Maxillofac Surg Clin North Am 16: 409e424, 2004 Slootweg PJ, Muller H: Malignant ameloblastoma or ameloblastic carcinoma. Oral Surg Oral Med Oral Pathol 54: 168e179, 1984 Taylor GI, Miller GD, Ham F: The free vascularised bone graft: a clinical extension of microvascular techniques. Plast Reconstr Surg 55: 533, 1975 Urken ML, Buchbinder D, Costantino PD, Sinha U, Okay D, Lawson W, Biller HF: Oromandibular reconstruction using microvascular composite flaps: report of 210 cases. Arch Otolaryngol Head Neck Surg 124(1): 46e55, 1998
Nikolic S. ZIVORAD, MD, DDS, PhD Clinic for Maxillofacial Surgery Faculty of Stomatology Dr. Subotica 4 11000 Belgrade Serbia E-mail: [email protected] Paper received 9 May 2009 Accepted 21 October 2009
Total mandibular reconstruction after resection of rare ‘‘honeycomb-like’’ ameloblastic carcinoma e A case report Jelena V. JEREMIC, MD1, Zivorad S. NIKOLIC, MD, DDS, PhD2, Ivan V. BORICIC, MD, PhD3, Zoran D. TACEVIC, MD, PhD1, Nada R. TOMANOVIC, MD3, Lazar J. DRCIC, DDS2, Milijanka D. NOVKOVIC, MD1 1
Clinic for Burns, Plastic and Reconstructive Surgery (Chief: Prof. Miodrag Colic), Clinical Centre of Serbia, Zvecanska 9, Belgrade, Serbia; 2 Clinic for Maxillofacial Surgery (Chief: Prof. Miodrag Gavric), Faculty of Stomatology, Dr Subotica 4, Belgrade, Serbia; 3 Institute for Pathology (Chief: Prof. Gordana Basta), Faculty of Medicine, Dr Subotica 1, Belgrade, Serbia
Purpose: This case report describes a rare and aggressive ameloblastic carcinoma that infiltrated the mandible in a ‘‘honeycomb’’ pattern. Methods: A total mandibulectomy with bilateral modified neck dissection was followed by primary reconstruction with a single free vascularised fibula flap. Results: The postoperative course was uneventful. The one year follow-up revealed no signs of recurrent tumour or metastases. Nine months later distant metastases occurred in the lung. Conclusion: Ameloblastic carcinoma is a highly malignant lesion, which requires aggressive therapy. Prognosis is poor. Further reporting of ameloblastic carcinoma is encouraged. Ó 2009 European Association for Cranio-Maxillo-Facial Surgery
SUMMARY.
Keywords: ameloblastic carcinoma, mandible, reconstruction, free fibula
excision of extremely rare and malignant ameloblastic carcinoma that involved the entire mandible.
INTRODUCTION Ameloblastic carcinoma is an extremely rare, aggressive odontogenic malignant neoplasm of the jaws, predominantly the mandible. Odontogenic tumours were classified by the World Health Organisation in 1971, and a modified classification was published by Slootweg and Muller (1984), which is still widely accepted. Most ameloblastic carcinomas are presumed to arise de novo, with less than 1% of ameloblastomas that undergo malignant transformation. As a highly aggressive lesion with ill-defined margins and cortical destruction, ameloblastic carcinoma has a poor prognosis due to local recurrence, and regional and distant metastasis, frequently to the lungs, and to a lesser extent to the vertebrae and viscera. The prognosis still appears to be poor, but the paucity of documented cases with long term follow up does not permit accurate assumptions to be made (Slater, 2004). Loss of mandible continuity results in alteration in speech, swallowing and mastication, and in the appearance of the patient. The restoration of a defect that involves the entire mandible is a rare and challenging problem for surgeons after ablation of malignant and aggressive tumours. Vascularised fibula transfer has become the preferred method of mandible reconstruction after oncologic surgical ablation. The fibula flap was firstly described by Taylor et al. (1975) and was used for the first time in mandibular reconstruction by Hidalgo (1989). We report a vascularised fibula free flap in the reconstruction of a total mandibular defect after radical
CASE REPORT A 58-year-old male patient with previously histopathologically diagnosed ameloblastic carcinoma of the mandible was admitted to the Department of Maxillofacial Surgery, Belgrade. The patient had suffered from bilateral lower lip numbness and diffuse swelling affecting the whole mandible without any mucosal or skin ulceration. Panoramic and computed tomography (CT) examination revealed small honeycomb-like osteolytic changes extending up to the condylar neck region bilaterally. (Fig. 1a, b, c, d) The total mandibulectomy with bilateral modified neck dissection was followed by primary reconstruction with 28 cm long free vascularised fibula flap. In order to achieve the desired mandible form, the graft was shaped by four subperiosteal osteotomies and fixed using mini plates (Fig. 2). The neomandible was also fixed to the existing healthy condylar processes on both sides. The flap pedicle was anastomised to the right facial artery and internal jugular vein. The specimen was subjected to a full histopathological examination with immunohistochemical analysis. The tumour was composed of nests and islands of basaloid cells within a collagenous, mature stroma. In focal areas, tumour cell nests demonstrated peripheral palisading of columnar cells enclosing a stellate reticulum type zone. 465
466 Journal of Cranio-Maxillo-Facial Surgery
Fig. 1 e Clinical (a) extraoral and intraoral (b) appearance with no mucosal or skin ulcerations. Panoramic (c) and CT (d) findings revealing ‘‘honeycomb-like’’ osteolytic changes of entire mandible (from one to another condylar neck) with multiple cortical perforations.
Fig. 2 e A 28 cm long harvested free fibular graft after remodeling.
More than fifty metastatic nodules of ameloblastic carcinoma were found in soft tissue of the neck region (Fig. 3a). Malignant tissue of ameloblastic carcinoma was present only in one lymph node from 25 lymph nodes present in vast surgical material. This node was infiltrated by ameloblastic carcinoma through lymph node capsule, without actual lymphatic spread (Fig. 3b). At the cytological level, the epithelial component exhibited overt cytological malignancy including pleomorphism, hyperchromatic nuclei, and high mitotic rate. In addition, perineural invasion was noted (Fig. 3c). The one year follow-up revealed no signs of recurrent tumour or metastasis. The postoperative CT findings were regarded as normal. The whole body examination showed no atypical findings (Figs. 4 and 5). Nine months later, distant metastases occurred in the lung, and further chemo and radiotherapy was administered. The adjuvant radiation therapy was not successful, and the patient subsequently died. DISCUSSION Ameloblastic carcinoma is a rare malignant epithelial neoplasm that is associated with an ameloblastoma
(then termed e carcinoma ex ameloblastoma), or histologically resembles an ameloblastoma e de novo ameloblastic carcinoma. Cytological atypia and mitotic activity rate are higher in ameloblastic carcinoma than ameloblastoma (Slater, 2004). Nagai et al. (1991) reported 46 ameloblastic carcinoma in English and Japanese literature. According to Lolachi et al. (1995), a total of 34 cases of ameloblastic carcinoma were reported in the English literature. Since then, a few additional case reports have been published (Corio et al., 1987; Simko et al., 1998; Cizmecy et al., 2004). The common clinical signs and symptoms of the disease include swelling, pain, trismus and dysphonia (Corio et al., 1987). Lower lip numbness and diffuse swelling were the only signs that were found in our patient. The age range of patients with a diagnosis of ameloblastic carcinoma shows large variation, with a reported mean age of 30 years, and no sex predilection that has been reported (Corio et al., 1987). Ameloblastic carcinoma is an aggressive neoplasm that is locally invasive and can spread to regional lymph nodes or distant sites, such as lungs and bones Kuriakose et al. (2003). Local invasion often extends out of bone to involve infratemporal fossa, parapharyngeal space, the masticator space or cervical soft tissue (Slater, 2004). This unique case demonstrated an unusual spreading pattern of the ameloblastic carcinoma which infiltrated the entire mandible in a ‘‘honeycomb’’ pattern. The tumour showed perineural invasion and also invasion of soft tissue of the neck region with lymph node infiltration. After mandibular reconstruction there was no local recurrence of the tumour, although in the later course of the disease there were distant metastases to the lung, despite apparently adequate control of the primary mandibular neoplasm. As there are very few documented cases in the literature, it is difficult to make a definitive recommendation regarding treatment. Because of its aggressive behaviour with extensive local destruction, the treatment of ameloblastic carcinoma should include wide local excision that could extend even to total mandibulectomy. Parotidectomy and regional lymph node dissection should also be considered. Radiation to both the tumour and neck bed, and chemotherapy seem to be of limited value
Total mandibular reconstruction after resection of rare ‘‘honeycomb-like’’ ameloblastic carcinoma 467
Fig. 3 e a. Ameloblastic carcinomaemetastasis in the soft tissue of the neck, haematoxylin & eosin 25. b. Ameloblastic carcinoma infiltrating lymph node capsule (thin arrow). On this slide there is also one smaller lymph node without malignant tissue (thick arrow), and soft tissue metastasis of ameloblastic carcinoma (arrowhead). c. Signs of perineural invasion.
Fig. 4 e Postoperative panoramic view of reconstructed mandible.
(Nagai et al., 1991; Lolachi et al., 1995; Infante-Cossio et al., 1998; Simko et al., 1998). We performed a radical tumour resection that included total mandibulectomy with bilateral modified neck dissection. The matter of restoring a total mandiblular defect is a rare and challenging problem for surgeons after ablation of malignant and aggressive tumours. Microvascular techniques to transfer vascularised bone to the head and neck region have been successfully applied to solve the problem of various segmental mandible defects (Urken et al., 1998; Cordeiro et al., 1999; Pohlenz et al., 2007). In our case, the entire mandible was successfully reconstructed with a single vascularised fibula flap. CONCLUSION Ameloblastic carcinoma is a rare odontogenic carcinoma which is highly malignant. It is an aggressive tumour
Fig. 5 e Patient appearance one year postoperatively.
468 Journal of Cranio-Maxillo-Facial Surgery
presenting a very unusual spreading pattern. Rarity of well documented cases and unpredictable clinical behaviour of ameloblastic carcinoma preclude definitive recommendation regarding treatment. Close follow-up of the patient is needed. Prognosis is usually poor. CONFLICT OF INTEREST None. References Cizmecy O, Aslan A, Onel D, Demiryont M: Ameloblastic carcinoma ex ameloblastoma of the mandible: a case report. Otolaryngol Head Neck Surg 130: 633e634, 2004 Cordeiro PG, Disa JJ, Hidalgo DA, Hu QY: Reconstruction of the mandible with osseous free flaps: a 10-year experience with 150 consecutive patients. Plast Reconstr Surg 104(5): 1314e1320, 1999 Corio RL, Goldblatt LI, Edwards PA, Hartman KS: Ameloblastic carcinoma: a clinicopathologic study and assessment of eight cases. Oral Surg Oral Med Oral Pathol 64(5): 570e576, 1987 Hidalgo DA: Fibulae free flap: a new method of mandible reconstruction. Plast Reconstr Surg 84: 71e79, 1989 Infante-Cossio P, Hernandez-Guisado JM, Fernandez-Machin P, Garcia-Perla A, Rollon-Mayordomo A, Jose L, Gutierrez-Perez JL: Ameloblastic carcinoma of the maxilla: a report of 3 cases. J Craniomaxillofac Surg 26(3): 159e162, 1998 Kuriakose MA, Rigual NR, Hicks Jr WL: Ameloblastic carcinoma: report of an aggressive case with multiple bony metastases. Am J Otolaryngol 24: 66e69, 2003 Lolachi CM, Maden SK, Jacobs JR: Ameloblastic carcinoma of the maxilla. J Laryngol Otol 109(10): 1019e1022, 1995
Nagai N, Takeshita H, Nagatsuka M, Inoue M, Nishijima K, Nojima T, Yamasaki M, Hoh C: Ameloblastic carcinoma: a case report and review. J Oral Pathol Med 20: 460e463, 1991 Pohlenz P, Blessmann M, Heiland M, Blake F, Schmelzle R, Li L: Postoperative complications in 202 cases of microvascular head and neck reconstruction. J Craniomaxillofac Surg 35: 311e315, 2007 Simko EJ, Brannon RB, Eibling DE: Ameloblastic carcinoma of the mandible. Head Neck 20: 654e659, 1998 Slater LJ: Odontogenic malignancies. Oral Maxillofac Surg Clin North Am 16: 409e424, 2004 Slootweg PJ, Muller H: Malignant ameloblastoma or ameloblastic carcinoma. Oral Surg Oral Med Oral Pathol 54: 168e179, 1984 Taylor GI, Miller GD, Ham F: The free vascularised bone graft: a clinical extension of microvascular techniques. Plast Reconstr Surg 55: 533, 1975 Urken ML, Buchbinder D, Costantino PD, Sinha U, Okay D, Lawson W, Biller HF: Oromandibular reconstruction using microvascular composite flaps: report of 210 cases. Arch Otolaryngol Head Neck Surg 124(1): 46e55, 1998
Nikolic S. ZIVORAD, MD, DDS, PhD Clinic for Maxillofacial Surgery Faculty of Stomatology Dr. Subotica 4 11000 Belgrade Serbia E-mail: [email protected] Paper received 9 May 2009 Accepted 21 October 2009