Journal of Cranio-Maxillo-Facial Surgery 42 (2014) 2035e2040

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Journal of Cranio-Maxillo-Facial Surgery

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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
b
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

a r t i c l e i n f o a b s t r a c t

Article history: Introduction: Cervical node metastasis of malignant ameloblastoma is extremely rare. Because of its
Paper received 4 June 2014 rarity, there is no standard treatment modality in a single lymph node metastasis in malignant
Accepted 25 September 2014 ameloblastoma.
Available online 5 October 2014
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
Keywords:
and simple excision. Local nodal recurrence, distant metastasis and follow-up periods were investigated.
Malignant ameloblastoma
Results: Eight patients were treated with neck dissection (group A) and four patients underwent a simple
Neck node
Metastasis
node excision (group B). Two patients in group A experienced multiple organ metastases such as liver
Neck dissection and lung seven months and 13 years after neck dissection respectively. The other patients showed no
Node excision 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.

1. Introduction show microscopic evidence of malignancy, regardless of whether it

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 ma-
lignant ameloblastoma and ameloblastic carcinoma, and they
compose less than 1% of all ameloblastomas. Malignant amelo-
blastoma is defined by the World Health Organization as an ame-
loblastoma 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 amelo-
blastic 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: ahnkangmin@hanmail.net (K.-M. Ahn).
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 amelo-
blastoma 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 amelo-
blastoma 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 denied any significant medical history existed beforehand. A
computed tomographic scan (CT) depicted multilocular, radiolu-
2.1. Review of the literature cent lesions with buccolingual expansion (Fig. 1A, B), involving the
right premolar to molar area which was diagnosed as an amelo-
2.1.1. Search strategy and study selection blastoma by incisional biopsy.
A computerized literature search on the subject of malignant Different treatment options along with the advantages versus
ameloblastoma was conducted focusing on the database of Medical disadvantages of each option were presented to the patient. To
Literature Analysis and Retrieval System online (MEDLINE) from decrease the possibility of recurrence, segmental mandibular
1920 to 2013. The searching term was “malignant ameloblastoma” resection surgery is recommended initially, but the patient chose to
or “metastatic ameloblastoma” or “metastasizing ameloblastoma” receive a more conservative treatment considering the young age of
or “malignant odontogenic tumor” or “adamantinoma”. Inclusion the patient. Thus, the patient underwent extraction of right lower
and exclusion criteria were as followed. canine to third molar, right marginal mandibulectomy with pres-
ervation of the inferior border and a free iliac bone reconstruction
2.1.2. Inclusion criteria surgery under general anesthesia (Fig. 2). Biopsy confirmed the
Ameloblastoma with metastasis to a single cervical lymph node diagnosis of ameloblastoma (Fig. 3).
was included in this analysis. The additional inclusion criteria for During the 2.5 years of follow up, no evidence of recurrence was
the analysis were; found in the primary site. In January 2007, the patient presented for
a regular annual check-up regarding neck swelling on the right side
 Publications in the English literature with discomfort. Clinical examination revealed one soft lump in the
 Studies with follow-up periods and survival right submandibular region. CT of the neck region showed a well-
 Studies with clearly defined surgical methods such as neck demarcated submandibular node swelling which was suspected
dissection or neck node excision as a reactive lymph node or a metastatic lymph node (Fig. 4).
 Studies with live patients 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
2.1.3. Exclusion criteria dissection surgery are considered as possible treatment options.
The reasons for exclusion were as followed: Because the lesion was a well-demarcated single node and the
patient strongly wanted to keep functionality of her neck as much
 Non-English literature as possible along with minimizing post-op impairment, a single
 Ameloblastic carcinoma node excision surgery was performed under general anesthesia in
 Other organ metastasis such as lung, liver, kidney, skin and January 2007. The submandibular lymph node was removed
spleen without disruption of the capsule and it consisted of one soft tissue
 Multiple cervical lymph node metastasis nodule measuring 4.0  2.5  2.5 cm (Fig. 5A, B). The lymph node
 No treatment due to patient's general condition revealed the identical histopathologic morphology as the primary
 Autopsy case lesion, which confirmed the diagnosis of a malignant amelo-
 Chemotherapy as a main treatment modality blastoma (Fig. 6). The patient has been regularly monitored each
 No follow-up periods and no report about survival year for follow-up visits, presently has been free of symptoms for 10
years after mandibular surgery and seven years after neck node
2.2. New case excision, and will be under close evaluation to detect any re-
currences or metastasis.
In June 2004, a 20-year-old female was referred from a local
clinic to the department of Oral and Maxillofacial Surgery with a 3. Results
complaint of painless swelling of the right mandible. The patient
has been de-identified and approval from the Institutional Review Of the 587 articles were examined and 11 studies were selected
Board (IRB) of Seoul Asan Medical Center was obtained. The patient 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
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 sum-
marized 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).
2037
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 recur-
rence 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 cer-
vical 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 indi-
cate 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 evidence-
based 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 ame-
loblastoma 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 metas-
tasis 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 treat-
ment selection depending on the histologic and clinical character-
istics. 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 re-
sembles a malignant tumor, a more aggressive and prophylactic
approach should be performed.
Fig. 6. Photomicrograph of the excised lymph node showing follicular pattern. Mul-
tiple 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 chemo-
therapy 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 amelo-
blastoma is radio-insensitive. Laughlin (1989) reported a dissemi-
nated 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 conjunc-
tively 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 se-
lective 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 bi-
opsy than the case of neck dissection when comparing 33 patients
after neck node biopsy and 29 patients after neck dissection sur-
gery (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 pre-
requisites 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 Simmons (1928) 37/F Left bifurcation of the carotid Radical neck dissection mandible N (8Y)
2 Houston et al. (1993) 36/M Left cervical lymph node Simple excision mandible N (5Y)
3 Duffey et al. (1995) 50/F Left deep upper cervical node (Right-SOHND, left-MRND) mandible Y (4M, multiple recurrences in liver
and both lungs expired in 13Y)
4 Sugiyama et al. (1999) 67/F Right cervical lymph node SOHND mandible N (3Y)
5 Verneuil et al. (2002) 70/M Right submental lymph node mRND mandible Y (7M, level V neck, lung metastasis)
6 Goldenberg et al. (2004) 81/M Cervical lymph node Neck dissection maxilla N (15Y)
7 Gilijamse et al. (2007) 26/F Submandibular lymph node MRND mandible N (16M)
8 Dao et al. (2009) 57/M Submandibular lymph node Simple excision mandible N (3Y)
9 Bansal et al. (2012) 40/F Right cervical lymph node E-RND mandible N (2Y)
10 Jayaraj et al. (2013) 22/M Left cervical lymph node Simple excision mandible N (1Y)
11 Present case 22/F Right submandibular lymph node Simple excision mandible 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 Acknowledgment

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 post-
operative 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 high-
lights that the affected lymph nodes were distinct single lesions,
which were well separated from the adjacent tissue and not con-
nected 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 inad-
equate 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.
Yoori Kim and Sung-Weon Choi contributed equally as a first
author to this study.
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