Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
Contents lists available at ScienceDirect
Journal of Cranio-Maxillo-Facial Surgery journal homepage: www.jcmfs.com
A single cervical lymph node metastasis of malignant ameloblastoma Yoori Kim a, Sung-Weon Choi b, Jong-Ho Lee c, Kang-Min Ahn a, * a
Department of Oral and Maxillofacial Surgery, College of Medicine, University of Ulsan, Asan Medical Center, Seoul, South Korea Oral Oncology Clinic, National Cancer Center, Gyeonggi-do, South Korea c Department of Oral and Maxillofacial Surgery, School of Dentistry, Seoul National University, Seoul, South Korea b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 4 June 2014 Accepted 25 September 2014 Available online 5 October 2014
Introduction: Cervical node metastasis of malignant ameloblastoma is extremely rare. Because of its rarity, there is no standard treatment modality in a single lymph node metastasis in malignant ameloblastoma. Materials and methods: Eleven patients of malignant ameloblastoma involving a single cervical lymph node metastasis and one new case were reviewed. Neck treatment was classified into neck dissection and simple excision. Local nodal recurrence, distant metastasis and follow-up periods were investigated. Results: Eight patients were treated with neck dissection (group A) and four patients underwent a simple node excision (group B). Two patients in group A experienced multiple organ metastases such as liver and lung seven months and 13 years after neck dissection respectively. The other patients showed no recurrence and metastasis. In group B, there was no report of a regional neck recurrence and distant metastasis during follow-up of 1e7 years. Conclusion: Multiple nodes metastasis requires a radical neck dissection; however, simple excision with close follow-up may be used in a single node metastasis in malignant ameloblastoma. © 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Malignant ameloblastoma Neck node Metastasis Neck dissection Node excision
1. Introduction Ameloblastoma is a slowly growing, benign, but locally invasive odontogenic neoplasm with a high recurrence rate if the initial lesion is treated by simple enucleation or curettage (Shin et al., 2011). Despite the fact of its benign histologic characteristics, ameloblastoma has the ability to develop metastasizing lesions in organs such as the lungs (Chou et al., 2013), cervical lymph nodes (Park et al., 2003; Jayaraj et al., 2013), spine (Nguyen, 2005), myocardium (Zwahlen et al., 2003), skull (Hayashi et al., 1997), kidney (Hayakawa et al., 2004) and skin (White and Patterson, 1986). The two malignant counterparts of ameloblastoma are malignant ameloblastoma and ameloblastic carcinoma, and they compose less than 1% of all ameloblastomas. Malignant ameloblastoma is defined by the World Health Organization as an ameloblastoma which has metastasized, and the metastatic lesion must maintain the same benign histopathologic feature as the primary tumor. On the other hand, ameloblastic carcinoma is an ameloblastic tumor characterized by distinct cytologic atypia, which can
* Corresponding author. Department of Oral and Maxillofacial Surgery, College of Medicine, University of Ulsan, Asan Medical Center, 88 Olympic-ro, 43-gil, Songpa-gu, Seoul, 137-736, South Korea. Tel.: þ82 2 3010 5901; fax: þ82 2 3010 6967. E-mail address: [email protected] (K.-M. Ahn).
show microscopic evidence of malignancy, regardless of whether it has metastasized. Ameloblastic carcinoma also presents aggressive clinical characteristics which include rapid growth, perforation of the cortex, and painful swelling (Bruce and Jackson, 1991; Ryu et al., 2002). Treatment of the metastatic lymph node in malignant ameloblastoma is controversial because of the rarity of cases. There have only been 23 articles reported since 1928 about ameloblastoma with lymph node metastasis (Simmons, 1928; Masson et al., 1959; Eda et al., 1972; Ikemura et al., 1972; Brandenburg et al., 1976; Lanham, 1987; Ueda et al., 1989; Houston et al., 1993; Duffey et al., 1995; Takeda, 1996; Witterick et al., 1996; Narozny et al., 1999; Sugiyama et al., 1999; Verneuil et al., 2002; Goldenberg et al., 2004; Gilijamse et al., 2007; Cardoso et al., 2009; Dao et al., 2009; Reid-Nicholson et al., 2009; Dissanayake et al., 2011; Bansal et al., 2012; Golubovic et al., 2012; Jayaraj et al., 2013). Goldenberg et al. (2004) and Dissanayake et al. (2011) suggested a radical neck dissection for cervical lymph node metastasis; however, Houston et al. (1993) and Dao et al. (2009) performed simple lymph node excision and reported no recurrence during their follow-up period. The purpose of this review is to suggest a treatment modality of a single cervical lymph node metastasis in malignant ameloblastoma and to report our experience of simple lymph node excision with ten years follow-up.
http://dx.doi.org/10.1016/j.jcms.2014.09.010 1010-5182/© 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
2036
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2. Materials and methods 2.1. Review of the literature 2.1.1. Search strategy and study selection A computerized literature search on the subject of malignant ameloblastoma was conducted focusing on the database of Medical Literature Analysis and Retrieval System online (MEDLINE) from 1920 to 2013. The searching term was “malignant ameloblastoma” or “metastatic ameloblastoma” or “metastasizing ameloblastoma” or “malignant odontogenic tumor” or “adamantinoma”. Inclusion and exclusion criteria were as followed. 2.1.2. Inclusion criteria Ameloblastoma with metastasis to a single cervical lymph node was included in this analysis. The additional inclusion criteria for the analysis were; Publications in the English literature Studies with follow-up periods and survival Studies with clearly defined surgical methods such as neck dissection or neck node excision Studies with live patients
2.1.3. Exclusion criteria The reasons for exclusion were as followed: Non-English literature Ameloblastic carcinoma Other organ metastasis such as lung, liver, kidney, skin and spleen Multiple cervical lymph node metastasis No treatment due to patient's general condition Autopsy case Chemotherapy as a main treatment modality No follow-up periods and no report about survival 2.2. New case In June 2004, a 20-year-old female was referred from a local clinic to the department of Oral and Maxillofacial Surgery with a complaint of painless swelling of the right mandible. The patient has been de-identified and approval from the Institutional Review Board (IRB) of Seoul Asan Medical Center was obtained. The patient
denied any significant medical history existed beforehand. A computed tomographic scan (CT) depicted multilocular, radiolucent lesions with buccolingual expansion (Fig. 1A, B), involving the right premolar to molar area which was diagnosed as an ameloblastoma by incisional biopsy. Different treatment options along with the advantages versus disadvantages of each option were presented to the patient. To decrease the possibility of recurrence, segmental mandibular resection surgery is recommended initially, but the patient chose to receive a more conservative treatment considering the young age of the patient. Thus, the patient underwent extraction of right lower canine to third molar, right marginal mandibulectomy with preservation of the inferior border and a free iliac bone reconstruction surgery under general anesthesia (Fig. 2). Biopsy confirmed the diagnosis of ameloblastoma (Fig. 3). During the 2.5 years of follow up, no evidence of recurrence was found in the primary site. In January 2007, the patient presented for a regular annual check-up regarding neck swelling on the right side with discomfort. Clinical examination revealed one soft lump in the right submandibular region. CT of the neck region showed a welldemarcated submandibular node swelling which was suspected as a reactive lymph node or a metastatic lymph node (Fig. 4). Ultrasono-guided fine needle aspiration biopsy was performed to confirm that there were no malignant cells in the aspirated fluid and tissues. Single node excision surgery or modified radical neck dissection surgery are considered as possible treatment options. Because the lesion was a well-demarcated single node and the patient strongly wanted to keep functionality of her neck as much as possible along with minimizing post-op impairment, a single node excision surgery was performed under general anesthesia in January 2007. The submandibular lymph node was removed without disruption of the capsule and it consisted of one soft tissue nodule measuring 4.0 2.5 2.5 cm (Fig. 5A, B). The lymph node revealed the identical histopathologic morphology as the primary lesion, which confirmed the diagnosis of a malignant ameloblastoma (Fig. 6). The patient has been regularly monitored each year for follow-up visits, presently has been free of symptoms for 10 years after mandibular surgery and seven years after neck node excision, and will be under close evaluation to detect any recurrences or metastasis. 3. Results Of the 587 articles were examined and 11 studies were selected for this study. In the English literature, there are 23 cases of cervical
Fig. 1. Computed tomography showing multilocular radiolucency with destruction of buccal cortical bone of right mandible in June 2004 (A: axial section, B: coronal section).
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2037
Fig. 2. Intraoperative photograph showing buccal bone resection and preservation of inferior alveolar nerve. Peripheral ostectomy was performed after ameloblastoma resection.
metastasis of malignant ameloblastoma in which the treatment methods are explained in the research (Simmons, 1928; Masson et al., 1959; Eda et al., 1972; Ikemura et al., 1972; Brandenburg et al., 1976; Lanham, 1987; Ueda et al., 1989; Houston et al., 1993; Duffey et al., 1995; Takeda, 1996; Witterick et al., 1996; Narozny et al., 1999; Sugiyama et al., 1999; Verneuil et al., 2002; Goldenberg et al., 2004; Gilijamse et al., 2007; Cardoso et al., 2009; Dao et al., 2009; Reid-Nicholson et al., 2009; Dissanayake et al., 2011; Bansal et al., 2012; Golubovic et al., 2012; Jayaraj et al., 2013). Among 23 cases, 12 patients showed a single cervical lymph node metastasis. One of the reports which did not describe a final prognosis and follow-up was excluded (Masson et al., 1959). And one study in which patient was not treated due to general health condition was also excluded (Golubovic et al., 2012). Thus, the 11 single node metastasis cases along with our case have been reviewed and the characteristics of the selected studies are summarized in Table 1. The first study was reported in 1928 and the last study was reported in 2013. All the included studies are a case report. The
Fig. 3. Photomicrograph of mandibular ameloblastoma showing follicular pattern. Multiple islands of odontogenic epithelium having central cystic degeneration (H & E staining, original magnification 100).
Fig. 4. Coronal view of computed tomography showing a lymph node swelling (arrow) in the right submandibular area (January 2007).
average age was 48.3 ± 19.4 (22e81 years old) and male to female ratio was 5:7. Seven patients were treated with neck dissection (group A) and four patients underwent a simple node excision (group B). Two patients in group A experienced multiple organ metastases such as liver and lung seven months and 13 years after neck dissection respectively. The other five patients in group A showed no recurrence and metastasis (follow-up 16 months-8 years). In group B, there was no report of a regional neck recurrence and distant metastasis (follow-up 1e7 years). 4. Discussion There are several reports analyzing the incidence of the metastasis site of malignant ameloblastoma, and typically the most common site is the lungs (70e88%) (Berger et al., 2012). The cervical lymph nodes are the second most common site (15e37.8%), and other minor sites include the pleura, spine, skull, diaphragm, liver, parotid, spleen, kidney and skin. Dissanayake et al. (2011) also found that the mean disease-free period, the time from initial diagnosis of ameloblastoma to metastasis, for cervical lymph node metastasis is 12.96 years. This is shorter than the mean disease-free interval for pulmonary metastasis (14.37 years), which may indicate that cervical metastasis precedes lung metastasis. In the case of pulmonary metastasis, as a standardized treatment protocol, wedge resection or lobectomy is considered. However, for cervical metastasis of ameloblastoma, the protocol for treatment is not fully established because of a lack of experience with this tumor, which is known to be a quite rare case. Some authors suggest wide neck dissection (Goldenberg et al., 2004; Dissanayake et al., 2011); however, there is no evidencebased suggestion for wide neck dissection. Therefore, emphasis should be placed on the collection and analysis of additional cases of cervical metastasis of malignant ameloblastoma in order to promote a standardized protocol that may be utilized for treatment. Due to the locally invasive characteristic of conventional ameloblastoma and the high risk for recurrence, it is recommended to resect the primary lesion with a 1 cm safety margin to decrease the potential of recurrence. From that similar prophylactic viewpoint,
2038
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
Fig. 5. (A) Submandibular incision to expose metastatic lymph node. (B) Excised lymph node with intact capsule.
some researchers maintain that cervical lymph node metastasis should be treated by neck dissection (Bansal et al., 2012). However, there is not a noticeable difference in the success rates according to the types of surgery performed; treatment was successful in our patient and three other cases where a single cervical node metastasis of malignant ameloblastoma was removed by simple excision. All of them comprised of a solitary cystic mass which was well circumscribed and easily separated from the surrounding tissues. And during the excision surgery, there was no evidence of damage to the capsular tissue. Therefore, they were removed successfully without a recurrence in any patient having been reported during the 1e5 year postoperative period. One thing which should never be ignored is the correct treatment selection depending on the histologic and clinical characteristics. Witterick et al. (1996) and Ikemura et al. (1972) presented cases in which the patients had undergone multiple recurrences in multiple organs in a relatively short period of time. Hence, despite the benign histologic entity, if the metastatic ameloblastoma resembles a malignant tumor, a more aggressive and prophylactic approach should be performed.
Fig. 6. Photomicrograph of the excised lymph node showing follicular pattern. Multiple islands of odontogenic epithelium showing peripheral columnar differentiation with reverse polarization. The central zone has cystic degeneration (H & E staining, original magnification 200).
The effectiveness of adjunctive radiation therapy or chemotherapy in the case of malignant ameloblastoma is not well-known, thus it has been controversial. Ikemura et al. (1972) considered radiation therapy as one of the reasons for the metastasis of the case presented in his research, and he argued that radiotherapy should be abandoned in ameloblastoma patients since ameloblastoma is radio-insensitive. Laughlin (1989) reported a disseminated type of ameloblastoma does not respond to chemotherapy. There are some reports that claim the response for radiotherapy is slow but progressive, and it would be beneficial if used conjunctively with a surgical procedure (Gardner, 1988). There are also other cases which showed a partial response or improved clinical symptoms for chemotherapy (Amzerin et al., 2011; Grunwald et al., 2001). The objective of neck dissection surgery is to remove lymph nodes from the side of the neck in which cancer cells may have migrated. Although the modified radical neck dissection and selective neck dissection methods have been introduced to preserve the functionality of the neck more than the radical neck dissection, many complications can still occur after surgery. It has also been reported in the study regarding the treatment of the N0 neck in patients with squamous cell carcinoma that the Neck Dissection Impairment Index was considerably better in the case of neck biopsy than the case of neck dissection when comparing 33 patients after neck node biopsy and 29 patients after neck dissection surgery (Murer et al., 2011). Evidently, the treatment of choice for a metastatic lesion in the neck node of other types of oral cancers has been a matter of debate. Especially since malignant ameloblastoma is a rare type, there is a lack of precedent cases in which to refer to, thus the treatment method largely depends on the decision of the surgeon. However, there is a definitive difference between a cancer cell and a metastatic ameloblastoma, in which the latter consists of a benign cell. According to the authors' experience, if the following prerequisites are well-managed, the method of neck node excision can be chosen as a successful treatment option for cervical metastasis of malignant ameloblastoma. Prerequisites for neck node excision in a single node metastasis of malignant ameloblastoma: I. There should not be any characteristics of malignancy in the histologic findings or the clinical pattern. II. Thorough investigation of every level of the neck region should be performed before and during the surgery.
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2039
Table 1 Malignant ameloblastoma with single neck node metastasis. No
Authors
A/S
Metastasis
Neck treatment
Primary site
Recurrence
1 2 3
Simmons (1928) Houston et al. (1993) Duffey et al. (1995)
37/F 36/M 50/F
Left bifurcation of the carotid Left cervical lymph node Left deep upper cervical node
Radical neck dissection Simple excision (Right-SOHND, left-MRND)
mandible mandible mandible
4 5 6 7 8 9 10 11
Sugiyama et al. (1999) Verneuil et al. (2002) Goldenberg et al. (2004) Gilijamse et al. (2007) Dao et al. (2009) Bansal et al. (2012) Jayaraj et al. (2013) Present case
67/F 70/M 81/M 26/F 57/M 40/F 22/M 22/F
Right cervical lymph node Right submental lymph node Cervical lymph node Submandibular lymph node Submandibular lymph node Right cervical lymph node Left cervical lymph node Right submandibular lymph node
SOHND mRND Neck dissection MRND Simple excision E-RND Simple excision Simple excision
mandible mandible maxilla mandible mandible mandible mandible mandible
N (8Y) N (5Y) Y (4M, multiple recurrences in liver and both lungs expired in 13Y) N (3Y) Y (7M, level V neck, lung metastasis) N (15Y) N (16M) N (3Y) N (2Y) N (1Y) N (7Y)
(A: age (years), S: sex, Y: yes, N: no, RND: radical neck dissection, Y: years, M: months, SOHND: supraomohyoid neck dissection, MRND: modified radical neck dissection, E-RND: extended radical neck dissection).
III. Cervical metastasis should not be a diffuse type, must be solitary. IV. The neck node should be well-demarcated and adequately separated from the adjacent tissue. V. Patient must be able to maintain a close semi-annual or yearly follow-up for any recurrences at the primary site or any metastasis. Since cervical metastasis of malignant ameloblastoma is an extremely rare type of tumor and the current classification system is still relatively new, not enough cases are available to develop the right therapeutic guideline. The information in this study cannot be conclusive since the post-operative data is limited and the postoperative periods are all different. Two of the successfully treated excisional biopsy cases (Dao et al., 2009; Jayaraj et al., 2013), in which the treatment protocol and excised lesion were explained in detail, were found to be similar to our case. The similarity highlights that the affected lymph nodes were distinct single lesions, which were well separated from the adjacent tissue and not connected to any other structure. Although a significant difference in results between the types of surgeries was not found, the number of reported cases is inadequate to establish the right baseline for cervical metastasis of ameloblastoma, thus, continuous research is necessary in order to develop a standard treatment protocol. Future studies regarding the follow-up of existing cases and the report of new cervical metastasis cases with their treatment will be important. A timely and appropriate surgical intervention of a primary tumor lesion should never be underestimated since inadequate surgical resection of an original ameloblastoma and a long duration of the tumor significantly correlates with a metastatic lesion. 5. Conclusion A cautious and sensible approach should be utilized with radical neck dissection when treating a single cervical lymph node metastasis in malignant ameloblastoma. A patient presenting with multiple metastatic lymph nodes may require a radical neck dissection; however, excisional biopsy without disruption of the capsule may be used in the case of a single node metastasis to minimize a patient's morbidity. Fund Korea Healthcare technology R& D Project, Ministry of Health, Welfare & Family Affairs, Republic of Korea (A101578). Conflict of interests None.
Acknowledgment Yoori Kim and Sung-Weon Choi contributed equally as a first author to this study. References Amzerin M, Fadoukhair Z, Belbaraka R, Iraqui M, Boutayeb S, M'Rabti H, et al: Metastatic ameloblastoma responding to combination chemotherapy: case report and review of the literature. J Med Case Rep 5: 491, 2011 Bansal A, Bhatnagar A, Saxena S: Metastasizing granular cell ameloblastoma. J Oral Maxillofac Pathol 16: 122e124, 2012 Berger AJ, Son J, Desai NK: Malignant ameloblastoma: concurrent presentation of primary and distant disease and review of the literature. J Oral Maxillofac Surg 70: 2316e2326, 2012 Brandenburg JH, Finch WW, Kirkham WR: Malignant ameloblastoma of the maxilla. Trans Sect Otolaryngol Am Acad Ophthalmol Otolaryngol 82: 576e578, 1976 Bruce RA, Jackson IT: Ameloblastic carcinoma. Report of an aggressive case and review of the literature. J Craniomaxillofac Surg 19: 267e271, 1991 Cardoso A, Lazow SK, Solomon MP, Berger JR, Rock A: Metastatic ameloblastoma to the cervical lymph nodes: a case report and review of literature. J Oral Maxillofac Surg 67: 1163e1166, 2009 Chou YH, Jhuang JY, Chang MH, Huang WC, Hsieh MS: Metastasizing ameloblastoma with localized interstitial spread in the lung: report of two cases. Int J Surg Pathol 22: 343e346, 2013 Dao TV, Bastidas JA, Kelsch R, Kraut RA: Malignant ameloblastoma: a case report of a recent onset of neck swelling in a patient with a previously treated ameloblastoma. J Oral Maxillofac Surg 67: 2685e2689, 2009 Dissanayake RK, Jayasooriya PR, Siriwardena DJ, Tilakaratne WM: Review of metastasizing (malignant) ameloblastoma (METAM): pattern of metastasis and treatment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 111: 734e741, 2011 Duffey DC, Bailet JW, Newman A: Ameloblastoma of the mandible with cervical lymph node metastasis. Am J Otolaryngol 16: 66e73, 1995 Eda S, Koike H, Tachikawa T, Yamane H, Shimono M: An autopsy case of the malignant ameloblastoma with metastases to the submaxillary lymph nodes, lungs and thoracic vertebrae. Bull Tokyo Dent Coll 13: 91e101, 1972 Gardner DG: Radiotherapy in the treatment of ameloblastoma. Int J Oral Maxillofac Surg 17: 201e205, 1988 Gilijamse M, Leemans CR, Winters HA, Schulten EA, van der Waal I: Metastasizing ameloblastoma. Int J Oral Maxillofac Surg 36: 462e464, 2007 Goldenberg D, Sciubba J, Koch W, Tufano RP: Malignant odontogenic tumors: a 22year experience. Laryngoscope 114: 1770e1774, 2004 Golubovic M, Petrovic M, Jelovac DB, Nenezic DU, Antunovic M: Malignant ameloblastoma metastasis to the neckeradiological and pathohistological dilemma. Vojnosanit Pregl 69: 444e448, 2012 Grunwald V, Le Blanc S, Karstens JH, Weihkopf T, Kuske M, Ganser A, et al: Metastatic malignant ameloblastoma responding to chemotherapy with paclitaxel and carboplatin. Ann Oncol 12: 1489e1491, 2001 Hayakawa K, Hayashi E, Aoyagi T, Hata M, Kuramoto C, Tonogi M, et al: Metastatic malignant ameloblastoma of the kidneys. Int J Urol 11: 424e426, 2004 Hayashi N, Iwata J, Masaoka N, Ueno H, Ohtsuki Y, Moriki T: Ameloblastoma of the mandible metastasizing to the orbit with malignant transformation. A histopathological and immunohistochemical study. Virchows Arch 430: 501e507, 1997 Houston G, Davenport W, Keaton W, Harris S: Malignant (metastatic) ameloblastoma: report of a case. J Oral Maxillofac Surg 51: 1152e1155, 1993 discussion 1156e1157 Ikemura K, Tashiro H, Fujino H, Ohbu D, Nakajima K: Ameloblastoma of the mandible with metastasis to the lungs and lymph nodes. Cancer 29: 930e940, 1972
2040
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
Jayaraj G, Sherlin HJ, Ramani P, Premkumar P, Natesan A, Ramasubramanian A, et al: Metastasizing ameloblastoma e A perennial pathological enigma? Report of a case and review of literature. J Craniomaxillofac Surg 42: 772e779, 2014 Lanham RJ: Chemotherapy of metastatic ameloblastoma. A case report and review of the literature. Oncology 44: 133e134, 1987 Laughlin EH: Metastasizing ameloblastoma. Cancer 64: 776e780, 1989 Masson JK, Mc DJ, Figi FA: Adamantinoma of the jaws; a clinicopathologic study of 100 histologically proved cases. Plast Reconstr Surg Transplant Bull 23: 510e525, 1959 Murer K, Huber GF, Haile SR, Stoeckli SJ: Comparison of morbidity between sentinel node biopsy and elective neck dissection for treatment of the n0 neck in patients with oral squamous cell carcinoma. Head Neck 33: 1260e1264, 2011 Narozny W, Stankiewicz C, Skorek A, Kaminski M: Malignant ameloblastoma of the maxilla as an interdisciplinary problem. Otolaryngol Pol 53: 667e670, 1999 Nguyen BD: Malignant ameloblastoma with thoracic vertebral metastasis: PET/CT and MR imaging. Clin Nucl Med 30: 450e452, 2005 Park JH, Jeong JH, Yun PY, Hong JR, Myung H, Hwang SJ, et al: Malignant ameloblastoma of mandible with lymph node metastasis. J Korean Assoc Oral Maxillofac Surg 29: 298e300, 2003 Reid-Nicholson M, Teague D, White B, Ramalingam P, Abdelsayed R: Fine needle aspiration findings in malignant ameloblastoma: a case report and differential diagnosis. Diagn Cytopathol 37: 586e591, 2009
Ryu DM, Jeon YI, Lee SC, Kim YG, Lee BS: A case report of ameloblastic carcinoma on the mandible. J Korean Assoc Oral Maxillofac Surg 28: 226e230, 2002 Shin YM, Park JH, Kim JW, Kwon TG, Lee SH, Kim CS: The clinico-statistical analysis of the treatments of the 139 ameloblastomas. J Korean Assoc Oral Maxillofac Surg 37: 287e294, 2011 Simmons CC: Adamantinoma. Ann Surg 88: 693e704, 1928 Sugiyama M, Ogawa I, Katayama K, Ishikawa T: Simultaneous metastatic ameloblastoma and thyroid carcinoma in the cervical region: report of a case. J Oral Maxillofac Surg 57: 1255e1258, 1999 Takeda Y: Melanocytes in malignant ameloblastoma. Pathol Int 46: 777e781, 1996 Ueda M, Kaneda T, Imaizumi M, Abe T: Mandibular ameloblastoma with metastasis to the lungs and lymph nodes: a case report and review of the literature. J Oral Maxillofac Surg 47: 623e628, 1989 Verneuil A, Sapp P, Huang C, Abemayor E: Malignant ameloblastoma: classification, diagnostic, and therapeutic challenges. Am J Otolaryngol 23: 44e48, 2002 White RM, Patterson JW: Distant skin metastases in a long-term survivor of malignant ameloblastoma. J Cutan Pathol 13: 383e389, 1986 Witterick IJ, Parikh S, Mancer K, Gullane PJ: Malignant ameloblastoma. Am J Otolaryngol 17: 122e126, 1996 Zwahlen RA, Vogt P, Fischer FS, Gratz KW: Case report: myocardial metastasis of a maxillary malignant ameloblastoma. J Oral Maxillofac Surg 61: 731e734, 2003
Contents lists available at ScienceDirect
Journal of Cranio-Maxillo-Facial Surgery journal homepage: www.jcmfs.com
A single cervical lymph node metastasis of malignant ameloblastoma Yoori Kim a, Sung-Weon Choi b, Jong-Ho Lee c, Kang-Min Ahn a, * a
Department of Oral and Maxillofacial Surgery, College of Medicine, University of Ulsan, Asan Medical Center, Seoul, South Korea Oral Oncology Clinic, National Cancer Center, Gyeonggi-do, South Korea c Department of Oral and Maxillofacial Surgery, School of Dentistry, Seoul National University, Seoul, South Korea b
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 4 June 2014 Accepted 25 September 2014 Available online 5 October 2014
Introduction: Cervical node metastasis of malignant ameloblastoma is extremely rare. Because of its rarity, there is no standard treatment modality in a single lymph node metastasis in malignant ameloblastoma. Materials and methods: Eleven patients of malignant ameloblastoma involving a single cervical lymph node metastasis and one new case were reviewed. Neck treatment was classified into neck dissection and simple excision. Local nodal recurrence, distant metastasis and follow-up periods were investigated. Results: Eight patients were treated with neck dissection (group A) and four patients underwent a simple node excision (group B). Two patients in group A experienced multiple organ metastases such as liver and lung seven months and 13 years after neck dissection respectively. The other patients showed no recurrence and metastasis. In group B, there was no report of a regional neck recurrence and distant metastasis during follow-up of 1e7 years. Conclusion: Multiple nodes metastasis requires a radical neck dissection; however, simple excision with close follow-up may be used in a single node metastasis in malignant ameloblastoma. © 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
Keywords: Malignant ameloblastoma Neck node Metastasis Neck dissection Node excision
1. Introduction Ameloblastoma is a slowly growing, benign, but locally invasive odontogenic neoplasm with a high recurrence rate if the initial lesion is treated by simple enucleation or curettage (Shin et al., 2011). Despite the fact of its benign histologic characteristics, ameloblastoma has the ability to develop metastasizing lesions in organs such as the lungs (Chou et al., 2013), cervical lymph nodes (Park et al., 2003; Jayaraj et al., 2013), spine (Nguyen, 2005), myocardium (Zwahlen et al., 2003), skull (Hayashi et al., 1997), kidney (Hayakawa et al., 2004) and skin (White and Patterson, 1986). The two malignant counterparts of ameloblastoma are malignant ameloblastoma and ameloblastic carcinoma, and they compose less than 1% of all ameloblastomas. Malignant ameloblastoma is defined by the World Health Organization as an ameloblastoma which has metastasized, and the metastatic lesion must maintain the same benign histopathologic feature as the primary tumor. On the other hand, ameloblastic carcinoma is an ameloblastic tumor characterized by distinct cytologic atypia, which can
* Corresponding author. Department of Oral and Maxillofacial Surgery, College of Medicine, University of Ulsan, Asan Medical Center, 88 Olympic-ro, 43-gil, Songpa-gu, Seoul, 137-736, South Korea. Tel.: þ82 2 3010 5901; fax: þ82 2 3010 6967. E-mail address: [email protected] (K.-M. Ahn).
show microscopic evidence of malignancy, regardless of whether it has metastasized. Ameloblastic carcinoma also presents aggressive clinical characteristics which include rapid growth, perforation of the cortex, and painful swelling (Bruce and Jackson, 1991; Ryu et al., 2002). Treatment of the metastatic lymph node in malignant ameloblastoma is controversial because of the rarity of cases. There have only been 23 articles reported since 1928 about ameloblastoma with lymph node metastasis (Simmons, 1928; Masson et al., 1959; Eda et al., 1972; Ikemura et al., 1972; Brandenburg et al., 1976; Lanham, 1987; Ueda et al., 1989; Houston et al., 1993; Duffey et al., 1995; Takeda, 1996; Witterick et al., 1996; Narozny et al., 1999; Sugiyama et al., 1999; Verneuil et al., 2002; Goldenberg et al., 2004; Gilijamse et al., 2007; Cardoso et al., 2009; Dao et al., 2009; Reid-Nicholson et al., 2009; Dissanayake et al., 2011; Bansal et al., 2012; Golubovic et al., 2012; Jayaraj et al., 2013). Goldenberg et al. (2004) and Dissanayake et al. (2011) suggested a radical neck dissection for cervical lymph node metastasis; however, Houston et al. (1993) and Dao et al. (2009) performed simple lymph node excision and reported no recurrence during their follow-up period. The purpose of this review is to suggest a treatment modality of a single cervical lymph node metastasis in malignant ameloblastoma and to report our experience of simple lymph node excision with ten years follow-up.
http://dx.doi.org/10.1016/j.jcms.2014.09.010 1010-5182/© 2014 European Association for Cranio-Maxillo-Facial Surgery. Published by Elsevier Ltd. All rights reserved.
2036
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2. Materials and methods 2.1. Review of the literature 2.1.1. Search strategy and study selection A computerized literature search on the subject of malignant ameloblastoma was conducted focusing on the database of Medical Literature Analysis and Retrieval System online (MEDLINE) from 1920 to 2013. The searching term was “malignant ameloblastoma” or “metastatic ameloblastoma” or “metastasizing ameloblastoma” or “malignant odontogenic tumor” or “adamantinoma”. Inclusion and exclusion criteria were as followed. 2.1.2. Inclusion criteria Ameloblastoma with metastasis to a single cervical lymph node was included in this analysis. The additional inclusion criteria for the analysis were; Publications in the English literature Studies with follow-up periods and survival Studies with clearly defined surgical methods such as neck dissection or neck node excision Studies with live patients
2.1.3. Exclusion criteria The reasons for exclusion were as followed: Non-English literature Ameloblastic carcinoma Other organ metastasis such as lung, liver, kidney, skin and spleen Multiple cervical lymph node metastasis No treatment due to patient's general condition Autopsy case Chemotherapy as a main treatment modality No follow-up periods and no report about survival 2.2. New case In June 2004, a 20-year-old female was referred from a local clinic to the department of Oral and Maxillofacial Surgery with a complaint of painless swelling of the right mandible. The patient has been de-identified and approval from the Institutional Review Board (IRB) of Seoul Asan Medical Center was obtained. The patient
denied any significant medical history existed beforehand. A computed tomographic scan (CT) depicted multilocular, radiolucent lesions with buccolingual expansion (Fig. 1A, B), involving the right premolar to molar area which was diagnosed as an ameloblastoma by incisional biopsy. Different treatment options along with the advantages versus disadvantages of each option were presented to the patient. To decrease the possibility of recurrence, segmental mandibular resection surgery is recommended initially, but the patient chose to receive a more conservative treatment considering the young age of the patient. Thus, the patient underwent extraction of right lower canine to third molar, right marginal mandibulectomy with preservation of the inferior border and a free iliac bone reconstruction surgery under general anesthesia (Fig. 2). Biopsy confirmed the diagnosis of ameloblastoma (Fig. 3). During the 2.5 years of follow up, no evidence of recurrence was found in the primary site. In January 2007, the patient presented for a regular annual check-up regarding neck swelling on the right side with discomfort. Clinical examination revealed one soft lump in the right submandibular region. CT of the neck region showed a welldemarcated submandibular node swelling which was suspected as a reactive lymph node or a metastatic lymph node (Fig. 4). Ultrasono-guided fine needle aspiration biopsy was performed to confirm that there were no malignant cells in the aspirated fluid and tissues. Single node excision surgery or modified radical neck dissection surgery are considered as possible treatment options. Because the lesion was a well-demarcated single node and the patient strongly wanted to keep functionality of her neck as much as possible along with minimizing post-op impairment, a single node excision surgery was performed under general anesthesia in January 2007. The submandibular lymph node was removed without disruption of the capsule and it consisted of one soft tissue nodule measuring 4.0 2.5 2.5 cm (Fig. 5A, B). The lymph node revealed the identical histopathologic morphology as the primary lesion, which confirmed the diagnosis of a malignant ameloblastoma (Fig. 6). The patient has been regularly monitored each year for follow-up visits, presently has been free of symptoms for 10 years after mandibular surgery and seven years after neck node excision, and will be under close evaluation to detect any recurrences or metastasis. 3. Results Of the 587 articles were examined and 11 studies were selected for this study. In the English literature, there are 23 cases of cervical
Fig. 1. Computed tomography showing multilocular radiolucency with destruction of buccal cortical bone of right mandible in June 2004 (A: axial section, B: coronal section).
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2037
Fig. 2. Intraoperative photograph showing buccal bone resection and preservation of inferior alveolar nerve. Peripheral ostectomy was performed after ameloblastoma resection.
metastasis of malignant ameloblastoma in which the treatment methods are explained in the research (Simmons, 1928; Masson et al., 1959; Eda et al., 1972; Ikemura et al., 1972; Brandenburg et al., 1976; Lanham, 1987; Ueda et al., 1989; Houston et al., 1993; Duffey et al., 1995; Takeda, 1996; Witterick et al., 1996; Narozny et al., 1999; Sugiyama et al., 1999; Verneuil et al., 2002; Goldenberg et al., 2004; Gilijamse et al., 2007; Cardoso et al., 2009; Dao et al., 2009; Reid-Nicholson et al., 2009; Dissanayake et al., 2011; Bansal et al., 2012; Golubovic et al., 2012; Jayaraj et al., 2013). Among 23 cases, 12 patients showed a single cervical lymph node metastasis. One of the reports which did not describe a final prognosis and follow-up was excluded (Masson et al., 1959). And one study in which patient was not treated due to general health condition was also excluded (Golubovic et al., 2012). Thus, the 11 single node metastasis cases along with our case have been reviewed and the characteristics of the selected studies are summarized in Table 1. The first study was reported in 1928 and the last study was reported in 2013. All the included studies are a case report. The
Fig. 3. Photomicrograph of mandibular ameloblastoma showing follicular pattern. Multiple islands of odontogenic epithelium having central cystic degeneration (H & E staining, original magnification 100).
Fig. 4. Coronal view of computed tomography showing a lymph node swelling (arrow) in the right submandibular area (January 2007).
average age was 48.3 ± 19.4 (22e81 years old) and male to female ratio was 5:7. Seven patients were treated with neck dissection (group A) and four patients underwent a simple node excision (group B). Two patients in group A experienced multiple organ metastases such as liver and lung seven months and 13 years after neck dissection respectively. The other five patients in group A showed no recurrence and metastasis (follow-up 16 months-8 years). In group B, there was no report of a regional neck recurrence and distant metastasis (follow-up 1e7 years). 4. Discussion There are several reports analyzing the incidence of the metastasis site of malignant ameloblastoma, and typically the most common site is the lungs (70e88%) (Berger et al., 2012). The cervical lymph nodes are the second most common site (15e37.8%), and other minor sites include the pleura, spine, skull, diaphragm, liver, parotid, spleen, kidney and skin. Dissanayake et al. (2011) also found that the mean disease-free period, the time from initial diagnosis of ameloblastoma to metastasis, for cervical lymph node metastasis is 12.96 years. This is shorter than the mean disease-free interval for pulmonary metastasis (14.37 years), which may indicate that cervical metastasis precedes lung metastasis. In the case of pulmonary metastasis, as a standardized treatment protocol, wedge resection or lobectomy is considered. However, for cervical metastasis of ameloblastoma, the protocol for treatment is not fully established because of a lack of experience with this tumor, which is known to be a quite rare case. Some authors suggest wide neck dissection (Goldenberg et al., 2004; Dissanayake et al., 2011); however, there is no evidencebased suggestion for wide neck dissection. Therefore, emphasis should be placed on the collection and analysis of additional cases of cervical metastasis of malignant ameloblastoma in order to promote a standardized protocol that may be utilized for treatment. Due to the locally invasive characteristic of conventional ameloblastoma and the high risk for recurrence, it is recommended to resect the primary lesion with a 1 cm safety margin to decrease the potential of recurrence. From that similar prophylactic viewpoint,
2038
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
Fig. 5. (A) Submandibular incision to expose metastatic lymph node. (B) Excised lymph node with intact capsule.
some researchers maintain that cervical lymph node metastasis should be treated by neck dissection (Bansal et al., 2012). However, there is not a noticeable difference in the success rates according to the types of surgery performed; treatment was successful in our patient and three other cases where a single cervical node metastasis of malignant ameloblastoma was removed by simple excision. All of them comprised of a solitary cystic mass which was well circumscribed and easily separated from the surrounding tissues. And during the excision surgery, there was no evidence of damage to the capsular tissue. Therefore, they were removed successfully without a recurrence in any patient having been reported during the 1e5 year postoperative period. One thing which should never be ignored is the correct treatment selection depending on the histologic and clinical characteristics. Witterick et al. (1996) and Ikemura et al. (1972) presented cases in which the patients had undergone multiple recurrences in multiple organs in a relatively short period of time. Hence, despite the benign histologic entity, if the metastatic ameloblastoma resembles a malignant tumor, a more aggressive and prophylactic approach should be performed.
Fig. 6. Photomicrograph of the excised lymph node showing follicular pattern. Multiple islands of odontogenic epithelium showing peripheral columnar differentiation with reverse polarization. The central zone has cystic degeneration (H & E staining, original magnification 200).
The effectiveness of adjunctive radiation therapy or chemotherapy in the case of malignant ameloblastoma is not well-known, thus it has been controversial. Ikemura et al. (1972) considered radiation therapy as one of the reasons for the metastasis of the case presented in his research, and he argued that radiotherapy should be abandoned in ameloblastoma patients since ameloblastoma is radio-insensitive. Laughlin (1989) reported a disseminated type of ameloblastoma does not respond to chemotherapy. There are some reports that claim the response for radiotherapy is slow but progressive, and it would be beneficial if used conjunctively with a surgical procedure (Gardner, 1988). There are also other cases which showed a partial response or improved clinical symptoms for chemotherapy (Amzerin et al., 2011; Grunwald et al., 2001). The objective of neck dissection surgery is to remove lymph nodes from the side of the neck in which cancer cells may have migrated. Although the modified radical neck dissection and selective neck dissection methods have been introduced to preserve the functionality of the neck more than the radical neck dissection, many complications can still occur after surgery. It has also been reported in the study regarding the treatment of the N0 neck in patients with squamous cell carcinoma that the Neck Dissection Impairment Index was considerably better in the case of neck biopsy than the case of neck dissection when comparing 33 patients after neck node biopsy and 29 patients after neck dissection surgery (Murer et al., 2011). Evidently, the treatment of choice for a metastatic lesion in the neck node of other types of oral cancers has been a matter of debate. Especially since malignant ameloblastoma is a rare type, there is a lack of precedent cases in which to refer to, thus the treatment method largely depends on the decision of the surgeon. However, there is a definitive difference between a cancer cell and a metastatic ameloblastoma, in which the latter consists of a benign cell. According to the authors' experience, if the following prerequisites are well-managed, the method of neck node excision can be chosen as a successful treatment option for cervical metastasis of malignant ameloblastoma. Prerequisites for neck node excision in a single node metastasis of malignant ameloblastoma: I. There should not be any characteristics of malignancy in the histologic findings or the clinical pattern. II. Thorough investigation of every level of the neck region should be performed before and during the surgery.
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
2039
Table 1 Malignant ameloblastoma with single neck node metastasis. No
Authors
A/S
Metastasis
Neck treatment
Primary site
Recurrence
1 2 3
Simmons (1928) Houston et al. (1993) Duffey et al. (1995)
37/F 36/M 50/F
Left bifurcation of the carotid Left cervical lymph node Left deep upper cervical node
Radical neck dissection Simple excision (Right-SOHND, left-MRND)
mandible mandible mandible
4 5 6 7 8 9 10 11
Sugiyama et al. (1999) Verneuil et al. (2002) Goldenberg et al. (2004) Gilijamse et al. (2007) Dao et al. (2009) Bansal et al. (2012) Jayaraj et al. (2013) Present case
67/F 70/M 81/M 26/F 57/M 40/F 22/M 22/F
Right cervical lymph node Right submental lymph node Cervical lymph node Submandibular lymph node Submandibular lymph node Right cervical lymph node Left cervical lymph node Right submandibular lymph node
SOHND mRND Neck dissection MRND Simple excision E-RND Simple excision Simple excision
mandible mandible maxilla mandible mandible mandible mandible mandible
N (8Y) N (5Y) Y (4M, multiple recurrences in liver and both lungs expired in 13Y) N (3Y) Y (7M, level V neck, lung metastasis) N (15Y) N (16M) N (3Y) N (2Y) N (1Y) N (7Y)
(A: age (years), S: sex, Y: yes, N: no, RND: radical neck dissection, Y: years, M: months, SOHND: supraomohyoid neck dissection, MRND: modified radical neck dissection, E-RND: extended radical neck dissection).
III. Cervical metastasis should not be a diffuse type, must be solitary. IV. The neck node should be well-demarcated and adequately separated from the adjacent tissue. V. Patient must be able to maintain a close semi-annual or yearly follow-up for any recurrences at the primary site or any metastasis. Since cervical metastasis of malignant ameloblastoma is an extremely rare type of tumor and the current classification system is still relatively new, not enough cases are available to develop the right therapeutic guideline. The information in this study cannot be conclusive since the post-operative data is limited and the postoperative periods are all different. Two of the successfully treated excisional biopsy cases (Dao et al., 2009; Jayaraj et al., 2013), in which the treatment protocol and excised lesion were explained in detail, were found to be similar to our case. The similarity highlights that the affected lymph nodes were distinct single lesions, which were well separated from the adjacent tissue and not connected to any other structure. Although a significant difference in results between the types of surgeries was not found, the number of reported cases is inadequate to establish the right baseline for cervical metastasis of ameloblastoma, thus, continuous research is necessary in order to develop a standard treatment protocol. Future studies regarding the follow-up of existing cases and the report of new cervical metastasis cases with their treatment will be important. A timely and appropriate surgical intervention of a primary tumor lesion should never be underestimated since inadequate surgical resection of an original ameloblastoma and a long duration of the tumor significantly correlates with a metastatic lesion. 5. Conclusion A cautious and sensible approach should be utilized with radical neck dissection when treating a single cervical lymph node metastasis in malignant ameloblastoma. A patient presenting with multiple metastatic lymph nodes may require a radical neck dissection; however, excisional biopsy without disruption of the capsule may be used in the case of a single node metastasis to minimize a patient's morbidity. Fund Korea Healthcare technology R& D Project, Ministry of Health, Welfare & Family Affairs, Republic of Korea (A101578). Conflict of interests None.
Acknowledgment Yoori Kim and Sung-Weon Choi contributed equally as a first author to this study. References Amzerin M, Fadoukhair Z, Belbaraka R, Iraqui M, Boutayeb S, M'Rabti H, et al: Metastatic ameloblastoma responding to combination chemotherapy: case report and review of the literature. J Med Case Rep 5: 491, 2011 Bansal A, Bhatnagar A, Saxena S: Metastasizing granular cell ameloblastoma. J Oral Maxillofac Pathol 16: 122e124, 2012 Berger AJ, Son J, Desai NK: Malignant ameloblastoma: concurrent presentation of primary and distant disease and review of the literature. J Oral Maxillofac Surg 70: 2316e2326, 2012 Brandenburg JH, Finch WW, Kirkham WR: Malignant ameloblastoma of the maxilla. Trans Sect Otolaryngol Am Acad Ophthalmol Otolaryngol 82: 576e578, 1976 Bruce RA, Jackson IT: Ameloblastic carcinoma. Report of an aggressive case and review of the literature. J Craniomaxillofac Surg 19: 267e271, 1991 Cardoso A, Lazow SK, Solomon MP, Berger JR, Rock A: Metastatic ameloblastoma to the cervical lymph nodes: a case report and review of literature. J Oral Maxillofac Surg 67: 1163e1166, 2009 Chou YH, Jhuang JY, Chang MH, Huang WC, Hsieh MS: Metastasizing ameloblastoma with localized interstitial spread in the lung: report of two cases. Int J Surg Pathol 22: 343e346, 2013 Dao TV, Bastidas JA, Kelsch R, Kraut RA: Malignant ameloblastoma: a case report of a recent onset of neck swelling in a patient with a previously treated ameloblastoma. J Oral Maxillofac Surg 67: 2685e2689, 2009 Dissanayake RK, Jayasooriya PR, Siriwardena DJ, Tilakaratne WM: Review of metastasizing (malignant) ameloblastoma (METAM): pattern of metastasis and treatment. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 111: 734e741, 2011 Duffey DC, Bailet JW, Newman A: Ameloblastoma of the mandible with cervical lymph node metastasis. Am J Otolaryngol 16: 66e73, 1995 Eda S, Koike H, Tachikawa T, Yamane H, Shimono M: An autopsy case of the malignant ameloblastoma with metastases to the submaxillary lymph nodes, lungs and thoracic vertebrae. Bull Tokyo Dent Coll 13: 91e101, 1972 Gardner DG: Radiotherapy in the treatment of ameloblastoma. Int J Oral Maxillofac Surg 17: 201e205, 1988 Gilijamse M, Leemans CR, Winters HA, Schulten EA, van der Waal I: Metastasizing ameloblastoma. Int J Oral Maxillofac Surg 36: 462e464, 2007 Goldenberg D, Sciubba J, Koch W, Tufano RP: Malignant odontogenic tumors: a 22year experience. Laryngoscope 114: 1770e1774, 2004 Golubovic M, Petrovic M, Jelovac DB, Nenezic DU, Antunovic M: Malignant ameloblastoma metastasis to the neckeradiological and pathohistological dilemma. Vojnosanit Pregl 69: 444e448, 2012 Grunwald V, Le Blanc S, Karstens JH, Weihkopf T, Kuske M, Ganser A, et al: Metastatic malignant ameloblastoma responding to chemotherapy with paclitaxel and carboplatin. Ann Oncol 12: 1489e1491, 2001 Hayakawa K, Hayashi E, Aoyagi T, Hata M, Kuramoto C, Tonogi M, et al: Metastatic malignant ameloblastoma of the kidneys. Int J Urol 11: 424e426, 2004 Hayashi N, Iwata J, Masaoka N, Ueno H, Ohtsuki Y, Moriki T: Ameloblastoma of the mandible metastasizing to the orbit with malignant transformation. A histopathological and immunohistochemical study. Virchows Arch 430: 501e507, 1997 Houston G, Davenport W, Keaton W, Harris S: Malignant (metastatic) ameloblastoma: report of a case. J Oral Maxillofac Surg 51: 1152e1155, 1993 discussion 1156e1157 Ikemura K, Tashiro H, Fujino H, Ohbu D, Nakajima K: Ameloblastoma of the mandible with metastasis to the lungs and lymph nodes. Cancer 29: 930e940, 1972
2040
Y. Kim et al. / Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040
Jayaraj G, Sherlin HJ, Ramani P, Premkumar P, Natesan A, Ramasubramanian A, et al: Metastasizing ameloblastoma e A perennial pathological enigma? Report of a case and review of literature. J Craniomaxillofac Surg 42: 772e779, 2014 Lanham RJ: Chemotherapy of metastatic ameloblastoma. A case report and review of the literature. Oncology 44: 133e134, 1987 Laughlin EH: Metastasizing ameloblastoma. Cancer 64: 776e780, 1989 Masson JK, Mc DJ, Figi FA: Adamantinoma of the jaws; a clinicopathologic study of 100 histologically proved cases. Plast Reconstr Surg Transplant Bull 23: 510e525, 1959 Murer K, Huber GF, Haile SR, Stoeckli SJ: Comparison of morbidity between sentinel node biopsy and elective neck dissection for treatment of the n0 neck in patients with oral squamous cell carcinoma. Head Neck 33: 1260e1264, 2011 Narozny W, Stankiewicz C, Skorek A, Kaminski M: Malignant ameloblastoma of the maxilla as an interdisciplinary problem. Otolaryngol Pol 53: 667e670, 1999 Nguyen BD: Malignant ameloblastoma with thoracic vertebral metastasis: PET/CT and MR imaging. Clin Nucl Med 30: 450e452, 2005 Park JH, Jeong JH, Yun PY, Hong JR, Myung H, Hwang SJ, et al: Malignant ameloblastoma of mandible with lymph node metastasis. J Korean Assoc Oral Maxillofac Surg 29: 298e300, 2003 Reid-Nicholson M, Teague D, White B, Ramalingam P, Abdelsayed R: Fine needle aspiration findings in malignant ameloblastoma: a case report and differential diagnosis. Diagn Cytopathol 37: 586e591, 2009
Ryu DM, Jeon YI, Lee SC, Kim YG, Lee BS: A case report of ameloblastic carcinoma on the mandible. J Korean Assoc Oral Maxillofac Surg 28: 226e230, 2002 Shin YM, Park JH, Kim JW, Kwon TG, Lee SH, Kim CS: The clinico-statistical analysis of the treatments of the 139 ameloblastomas. J Korean Assoc Oral Maxillofac Surg 37: 287e294, 2011 Simmons CC: Adamantinoma. Ann Surg 88: 693e704, 1928 Sugiyama M, Ogawa I, Katayama K, Ishikawa T: Simultaneous metastatic ameloblastoma and thyroid carcinoma in the cervical region: report of a case. J Oral Maxillofac Surg 57: 1255e1258, 1999 Takeda Y: Melanocytes in malignant ameloblastoma. Pathol Int 46: 777e781, 1996 Ueda M, Kaneda T, Imaizumi M, Abe T: Mandibular ameloblastoma with metastasis to the lungs and lymph nodes: a case report and review of the literature. J Oral Maxillofac Surg 47: 623e628, 1989 Verneuil A, Sapp P, Huang C, Abemayor E: Malignant ameloblastoma: classification, diagnostic, and therapeutic challenges. Am J Otolaryngol 23: 44e48, 2002 White RM, Patterson JW: Distant skin metastases in a long-term survivor of malignant ameloblastoma. J Cutan Pathol 13: 383e389, 1986 Witterick IJ, Parikh S, Mancer K, Gullane PJ: Malignant ameloblastoma. Am J Otolaryngol 17: 122e126, 1996 Zwahlen RA, Vogt P, Fischer FS, Gratz KW: Case report: myocardial metastasis of a maxillary malignant ameloblastoma. J Oral Maxillofac Surg 61: 731e734, 2003
