Japanese Journal of Clinical Oncology Advance Access originally published online on February 12, 2009
Japanese Journal of Clinical Oncology 2009 39(4):231-236; doi:10.1093/jjco/hyp001
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© The Author (2009). Published by Oxford University Press. All rights reserved
Metastatic Neck Disease Beyond the Limits of a Neck Dissection: Attention to the ‘Para-hyoid’ Area in T1/2 Oral Tongue Cancer
1 Head and Neck Surgery Division, National Cancer Center Hospital, Tokyo
2 Department of Otorhinolaryngology, School of Medicine, University of Tokyo, Tokyo
3 Division of Head and Neck Surgery, National Cancer Center Hospital East, Chiba, Japan
For reprints and all correspondence: Mizuo Ando, Department of Otorhinolaryngology, School of Medicine, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-8655, Japan. E-mail: andom-tky{at}umin.ac.jp
Received September 7, 2008; accepted December 31, 2008
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Abstract |
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 TOP Abstract INTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONConflict of interest statementReferences |
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Objective: We evaluated patients with small oral tongue cancer suffering from recurrence, which develops in the intervening area between the primary site and the neck. Lesions in the area around the cornu of the hyoid bone (‘para-hyoid’ area) often involve the hypoglossal nerve and the root of the lingual artery, resulting in treatment failure and death.
Methods: A 10-year retrospective chart review was conducted of 248 oral tongue cancer patients with small primary tumors (T1/2). No patients who underwent postoperative radiotherapy (PORT) were included.
Results: After excluding those who had local failure or developed new primary lesions, 6.3% of the patients were noted to have a para-hyoid lesion. A similar incidence was observed between the patients with and without previous neck dissection, 6.9% and 5.7%, respectively. All but one patient died due to uncontrolled neck disease.
Conclusions: Recurrent para-hyoid lesions could occur, irrespective of a previous neck dissection. In other words, the para-hyoid area is beyond the limits of a neck dissection. Once a para-hyoid lesion becomes clinically evident, it seems difficult to salvage. Therefore, a careful inspection of the area should be included intraoperatively in any type of neck dissection (i.e. elective or therapeutic) for patients with oral tongue cancer. This may be the key to improving the regional control rate of patients with small oral tongue cancer. We believe that some patients will benefit from more aggressive treatment of the neck, although PORT seems unnecessary for the majority of the patients with limited neck disease.
Key Words: head and neck • squamous cell carcinoma • tongue • neck dissection
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INTRODUCTION |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONConflict of interest statementReferences |
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A neck dissection has been the most reliable treatment for metastatic neck disease in patients with head and neck cancer, since the first description of radical neck dissection by Crile in 1906 (1). To date, detailed knowledge of lymphatic drainage patterns has led to a modification in early indications for radical neck dissection (2–5). Most small oral tongue tumors with limited neck disease can be sufficiently treated by a transoral glossectomy and discontinuous neck dissection, using either a modified radical or selective procedure. Postoperative radiotherapy (PORT) may be beneficial for node-positive patients, especially those with multiple nodal involvement, but further studies are needed (6–10). Postoperative chemoradiotherapy may be selectively administered to those who show an inadequate surgical margin and/or lymph node metastasis with extracapsular spread (11).
Recurrence occasionally develops in the area between the primary site and the neck. This makes it difficult to choose between the treatment radicality and postoperative function, as the sacrifice of the intervening floor-of-mouth tissues will increase the morbidity in terms of function and the need for reconstruction using a microvascular free-tissue flap. In order to surgically improve the regional control rate while preserving the floor-of-mouth tissues, the area around the cornu of the hyoid bone is of particular concern. This will be referred to as the ‘para-hyoid’ area in this article. It is located near the boundary of levels I and II in the two-dimensional drawing, but is actually much deeper. Metastatic disease in this area involves the hypoglossal nerve, the root of the lingual artery and the cornu of the hyoid bone (Figs 1 and 2), often resulting in treatment failure and death. A large series of patients with oral tongue squamous cell carcinoma were retrospectively reviewed to clarify the characteristics of para-hyoid lesions. This study focused on the patients who underwent a glossectomy without reconstruction using a microvascular free-tissue flap. In other words, patients with small primary tumors whose floor-of-mouth tissues should be largely preserved were the subjects of this study.
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PATIENTS AND METHODS |
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This study identified 290 previously untreated patients with T1/2 squamous cell carcinoma of the oral tongue who underwent surgery at National Cancer Center Hospital during the years 1993 through 2002 and were followed either for at least 2 years or until death. Patients who underwent extensive resection requiring microvascular free-tissue flap for reconstruction were excluded, because the consequent anatomical changes made the assessment of the area difficult. Patients who underwent PORT were also excluded, and the remaining 248 patients were the subjects of this study. There were 140 males and 108 females who ranged in age from 24 to 93 years (median, 59 years). The population distribution is shown in Table 1. The median follow-up time was 66 months.
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All patients underwent at least a glossectomy as a part of their initial surgery. On initial assessment, 211 patients were considered clinically node negative. A glossectomy only was performed for 188 patients, whereas a glossectomy with elective neck dissection was performed for other 23 patients either because of the surgeons' preference or the need for a transcervical (pull-through) resection of the primary tumor. At our institution, most of the T2 tumors that extend to the base of tongue or the floor of mouth could be successfully resected by a transcervical approach without microvascular free-tissue flap transfer. Instead, we often used the digastric muscle to close the defect on the floor of mouth. Every elective neck dissection included at least levels I to III. The remaining 37 patients had clinically evident neck disease on their initial assessment; therefore, a glossectomy with neck dissection was performed, including 4 patients who underwent a synchronous bilateral neck dissection. The policy regarding adjuvant treatment at that period was to add PORT for patients who were found to have an inadequate surgical margin and/or lymph node metastases with extracapsular spread on pathological examination. In this study, however, patients who underwent PORT were excluded in order to eliminate the possible therapeutic effect to the para-hyoid area. The follow-up time was calculated from the patients' initial surgery for the primary tumor until the date of last contact or death. The survival curves were plotted using the Kaplan–Meier method and compared using the log-rank test. Relationships between various clinicopathological parameters and a para-hyoid involvement were tested by the
2 test or the Fisher exact test when appropriate. All statistical calculations were performed using the SPSS software program (release 11.0; SPSS Inc., Chicago, IL, USA). |
RESULTS |
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The charts of 248 patients were reviewed and then 25 patients who had local failure or developed new primary tumors that might reseed the neck were excluded from the analysis. During the follow-up period, 77 patients suffered from regional recurrence and 14 (6.3% of the 223) of these patients had para-hyoid involvement (Fig. 3). No statistically significant difference was observed between the cases of recurrence-free and the cases with para-hyoid involvement, except for tumor differentiation (P = 0.032, Table 2). The tumor thickness reached almost significant level (P = 0.083). None was noted to have such para-hyoid lesions on their initial assessment. All of the lesions were observed as recurrence in the neck in 7 of the 122 patients without a previous neck dissection, and 7 of the 101 patients with either an elective or therapeutic, synchronous or metachronous neck dissection (Tables 3 and 4). The duration of time after the initial surgery until the para-hyoid lesion was noted ranged from 2.0 to 29.9 months (median, 6.5 months). In eight patients, the para-hyoid lesion was the only manifestation of recurrent neck disease, whereas the other six patients were found to have multiple nodal involvement. Despite all efforts at salvage treatment, all but one of these 14 patients died due to uncontrolled neck disease. There was a statistically significant difference in the disease-specific survival rate between the 77 patients (regional failure) with and without the para-hyoid involvement (P < 0.001, Fig. 4).
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DISCUSSION |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONConflict of interest statementReferences |
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A transoral glossectomy with discontinuous neck dissection seems to be the current surgical practice for the patients who have small oral tongue tumor with limited neck disease, although the effectiveness of PORT for all node-positive patients remains to be discussed (6–10). There have been arguments whether to remove the intervening tissues between the primary site and the neck (12,13). It is apparent that the lymphatic drainage from the oral tongue travels through the floor of mouth before entering the upper neck, and some recurrences develop in this area. This study focused on the intervening area between the primary site and the neck, particularly the para-hyoid area that is located near the boundary of levels I and II in a two-dimensional drawing, but actually deeper within it. We presume that this area is located deep behind the hypoglossal nerve and includes the area where the lingual artery passes deep to the post-lateral border of the hyoglossus muscle. In other words, it is almost synonymous with ‘the lower tip of the parapharyngeal space’. Although para-hyoid lesions were sometimes noted as simple metastatic disease in the upper neck, they frequently involved the hypoglossal nerve, the root of the lingual artery and the cornu of the hyoid bone.
A 10-year chart review of 248 patients revealed that the incidence of a para-hyoid lesion in the patients with small oral tongue cancer was estimated to be 6.3%, not counting the patients who had local failure. The result of salvage treatment was extremely poor. It was interesting to note that a similar incidence was observed between the patients with and without previous neck dissection, namely 6.9% (7 of 101) and 5.7% (7 of 122), respectively. A simple comparison between the patients with and without previous neck dissection is unreasonable because their backgrounds, including the timing of the neck dissection, tended to be different. The current data certainly indicated, however, that a previous neck dissection was insufficient for preventing recurrent disease in the para-hyoid area. Indeed, the para-hyoid area is beyond the limits of a traditional neck dissection.
It should also be noted that all of the para-hyoid lesions occurred as recurrent disease. Preoperative assessment as well as the efficacy of neck treatment should be reconsidered, if surgical practices do not address the tissues at risk for metastases in this area. For comparison, the para-hyoid involvement in patients with T3/4 tumor who underwent extensive composite resection remains to be addressed. The observation of serial sections of the intervening tissues may provide useful information.
The etiology of para-hyoid lesions remains unclear. Metastatic nodal structure was confirmed in three cases, whereas tumor cells invaded unspecified soft tissue in six cases. The para-hyoid area is located on the draining course of the lateral lingual nodes described by several authors in the literature (15–17). Metastatic disease in this area might occur due to occult metastatic lingual nodes themselves or to ‘in transit’ tumor cells in the draining lymphatics to the deep jugular chain. It is interesting to note that our past personal experience suggested that the lingual nodes are very prone to show extracapsular spread, probably because of their small size and the thin capsule. Another possibility is that mechanical obstruction of the lymphatic channels after previous surgery might alter the drainage of the tumor cells. Whatever the etiology, occult tumor cells left behind in the intervening tissues between the primary site and the neck appear to be responsible for the para-hyoid lesions. It seems reasonable to deliver some treatment to these possible tumor cells, although not all of them are capable of progressing to viable tumors.
There are several possibilities for dealing with the occult tumor cells in the intervening tissues. Some advocate a neck dissection in continuity with the primary tumor (13,14). The problem is to what extent a surgeon should remove the intervening tissues through an in-continuity neck dissection. In addition, it is not always acceptable because of the greater morbidity in comparison to a discontinuous neck dissection. An extensive composite resection including the para-hyoid area causes quite a large defect, which will always adds the need for reconstruction using a microvascular free-tissue flap. This is not necessary in the majority of the patients with small primary tumors.
Another possibility is to deliver extended surgery selectively, based on the prediction of the para-hyoid involvement. Such surgery would be ideal, although no such clinicopathological factor was observed in the current study. Tumor differentiation and thickness have been shown to be predictive factors of neck metastases, but such factors are insufficient to distinguish between cases of regional failure with and without para-hyoid lesions as indicated in Table 2. As long as no predicting factor for the para-hyoid involvement is identified, at least a careful inspection of the area should be included intraoperatively during neck dissection for patients with oral tongue cancer. An elective neck dissection should also include an inspection of this area. This requires only 10 min at maximum and causes essentially no increased morbidity. In order to routinely dissect the para-hyoid area, surgical procedures with low morbidity while extending the limit of neck dissection would be justified, considering the low incidence of the lesion. A combination of surgery with PORT is possible. This may be similar to the treatment of the retropharyngeal nodes in patients with hypopharyngeal carcinoma.
It should also be noted that the recurrent para-hyoid lesion developed in four patients with pathological N0 or N1 status after neck dissection (Table 4, No. 11–14). This means that systematic PORT only for patients with multiple nodal involvements may miss some patients at risk for the recurrent para-hyoid involvement.
In conclusion, the incidence of the para-hyoid lesion in patients with T1/2 oral tongue cancer was estimated to be 6.3%, and that the involvement of this area was significantly related to a poor outcome. Recurrent para-hyoid lesions could occur, irrespective of a previous neck dissection. An extension of the limits of a neck dissection, whether elective or therapeutic, may therefore be warranted. Additional treatment to the patients who are found to have such para-hyoid involvement remains to be discussed. We also plan to carry out another chart review that focuses on the patients who underwent an extensive resection with free-tissue flap transfer in order to compare the control rate of the para-hyoid area.
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Conflict of interest statement |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONConflict of interest statementReferences |
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None declared.
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References |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONConflict of interest statementReferences |
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