The Value of Elective Neck Dissection in Treatment of Cancer of the Tongue

Sefa Kaya, MD, Taner Yilmaz, MD, Bulent Gursel, MD, Sarp Sarac, MD, and Levent Sennaroglu, MD
Purpose: The adequate therapy of tongue cancer has not yet been determined. The authors report their experience with 58 N0 patients to elucidate the role of elective neck dissection in surgical treatment of cancer of the tongue. Materials and Methods: The les of 58 N0 patients with tongue cancer were evaluated retrospectively. In every patient, partial glossectomy continuous with neck dissection was the mainstay of the treatment. TNM staging, intraoperative N staging, pathologically conrmed cervical lymph node metastases and their levels, and clinical outcomes (local and regional recurrences) were recorded. The sensitivity and specicity of intraoperative staging was determined. Results: Fifty-four percent (31/58) of the patients presented as T1, and 26% (15/58) as T2. The overall occult metastasis rate was 29.3% (17/58). The occult metastasis rate for T1 and T2 lesions was 19.4% (6/31) and 26.7% (4/15), respectively. The sensitivity of intraoperative staging was 76.5%, and the specicity was 51.2%. Conclusions: The rate of occult metastasis to the neck is too high in all tongue cancer cases to take the risk of regional recurrence, and the surgeon can not solely depend on neck palpation for determination of neck metastasis. Radiologic investigations and ne-needle aspiration decrease, but never reduce to zero the rate of false-negative examination. There is an obvious indication for neck dissection, even in early cases. (Am J Otolaryngol 2001;22:59-64. Copyright 2001 by W.B. Saunders Company)

Tongue cancer is the second most common oral cavity malignancy after cancer of the lip,1 but its adequate therapy has not yet been determined. The traditional surgical treatment of tongue cancers involves partial glossectomy en bloc with neck dissection. Nevertheless, there are proponents of partial glossectomy alone,2 and some claim that partial glossectomy can be performed discontinuous with neck dissection without compromising local recurrence and cure rates.3 The current study was conducted to elucidate the role of elective neck dissection in surgical treatment of cancer of the tongue. MATERIALS AND METHODS
The les of 58 N0 patients out of 88 cases with squamous cell carcinoma of the tongue who were

From the Department of Otolaryngology-Head & Neck Surgery, Hacettepe University Faculty of Medicine, Ankara, Turkey. Address reprint requests to Taner Yilmaz, MD, 12. Sokak No: 8-7, 06490 Bahcelievler, Ankara, Turkey. Copyright 2001 by W.B. Saunders Company 0196-0709/01/2201-0001$35.00/0 doi:10.1053/AJOT.2001.20681

treated surgically at Hacettepe University Faculty of Medicine Department of Otolaryngology-Head and Neck Surgery between the years of 1967 and 1997 were reviewed retrospectively. Cancers of the base of the tongue and lesions with histopathology other than squamous cell carcinoma were excluded from the study. Further histologic data, such as depth and peripheral invasion, were not evaluated. Routine radiologic examination of the neck was not done in N0 cases. Out of 58 patients, 37 were men and 21 were women; the mean age was 53 years (range 21-78 years). All T stages were included, but occult metastasis rates were given separately for T stages, especially T1 and T2. In every patient, partial glossectomy continuous with neck dissection was the mainstay of the treatment. N0 lesions were treated by either supraomohyoid or modied radical neck dissection, sparing the sternocleidomastoid muscle, internal jugular vein, and spinal accessory nerve. If lymph nodes that are suspected to contain metastasis were discovered intraoperatively, the modied radical neck dissection or supraomohyoid dissection was converted to radical neck dissection. For lesions at the tip or approaching the midline, contralateral suprahyoid, or supraomohyoid neck dissection was performed.

RESULTS The false negative rate of neck palpation is 29.3% (17/58). Table 1 shows intraoperative
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TABLE 1. The Relation Between Intraoperative N-staging and Pathologic N-staging Pathologic N0 Intraoperative N0 Intraoperative N Total 21 20 41 Pathologic N 4 13 17 Total 25 33 58

TABLE 2. The Relation Between T-stages and Pathologic N-stages Pathologic N0 T1-2 T3-4 Total 36 5 41 Pathologic N 10 7 17 Total 46 12 58

staging of suspicious lymph nodes in relation to pathologic N-staging. False positive rate is 48.8% (20/41). The false negative rate is 23.5% (4/17). Sensitivity of intraoperative Nstaging is 76.5%, and specicity is 51.2%. Fifty-four percent (31/58) of the cases are T1, 26% (15/58) of cases are T2, 10% (6/58) are T3 and 10% (6/58) of the cases are T4. In addition, 70.7% (41/58) of cases are pathologically N0, and 29.3% (17/58) are N (Table 2). Of clinically N0 cases that were proven to be pathologically N , 6 are clinically T1; 4 are T2; 2 are T3; and 5 are T4. Of 6 T1 cases, 3 came out to be pathologically N1 and 3 N2. Two T2 cases are pathologically N1, and the other 2 are N2. The T3 cases are N2. Four T4 cases are pathologically N2, and the other T4 case is N1. Table 2 shows the distribution of pathologically N0 and N cases among T1-2 and T3-4 stages. A total of 78.3% (36/46) of T1-2 are pathologically N0, and 21.7% (10/46) are N . A total of 41.7% (5/12) of T3-4 are N0, and 58.3% (7/12) are N . The occult metastasis rate for T1 and T2 lesions was 19.4% (6/31) and 26.7% (4/15), respectively. For 58 N0 tongue cancer patients, 32 radical neck dissections, 11 modied radical neck dissections, 13 supraomohyoid dissections, and 2 selective anterolateral (level I-IV) dissections were performed for the ipsilateral neck. Three modied radical, 2 supraomohyoid, and 11 suprahyoid dissections were done for the contralateral neck. Among the 16 supraomohyoid dissections, only 2 patients had metastatic lymph nodes at middle cervical area and were treated with postoperative radiation therapy. Two selective anterolateral neck dissections (level I-IV) did not have any metastasis. No metastatic lymph nodes were detected in any of the suprahyoid dissections. Thirty-six patients were treated with surgery only, 14 patients received postoperative radiotherapy, 6 received postoperative chemotherapy, and 2 patients were given both

postoperative radiotherapy and chemotherapy. Seventeen pathologically N cases showed 35 metastatic lymph nodes. The distribution of these metastases is shown in Table 3. There was only one N0 patient who had metastatic lower jugular node. Surgical margins were positive in 4 patients (6.9%). Fourteen patients experienced recurrences 9 of them were local, and 5 were regional recurrences. Three of the regional recurrences were in the contralateral undissected neck, 2 of these patients did not have ipsilateral metastasis. The contralateral regional recurrences were observed in cases having lesions without midline crossing. One of the ipsilateral regional recurrences appeared after supraomohyoid neck dissection, and did not contain pathologic lymph node metastasis. The other ipsilateral regional recurrence was observed after radical neck dissection, which was reported to contain 3 metastatic submandibular lymph nodes. Three of the local recurrences appeared in T4 cases, one of which had positive surgical margins. Four of the local recurrences were observed in T2 cases, one of which had positive surgical margins. Two of the local recurrences appeared in T1 and T3 cases. All recurrent cases were treated with surgery, radiotherapy, and chemotherapy, but all of them died from their disease in a short time. The overall 3-year disease-free survival

TABLE 3. Distribution of Lymph Node Metastasis According to Cervical Levels in N0 Tongue Cancer Lymph Node Levels Submandibular Upper cervical Middle cervical Lower cervical Posterior cervical Number of Lymph Nodes 12 12 10 1 % of Lymph Nodes 34.3% 34.3% 28.6% 2.8%

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rate was 78.3% for T1 and T2 lesions, and 66.7% for T3 and T4 lesions. Out of 4 patients with positive surgical margins, 2 developed local recurrences. The other 2 are still on follow-up; they completed 17 years and 3 years disease-free. All of these patients received postoperative radiation therapy. DISCUSSION Although tongue cancer is such a common disease of head and neck, its treatment seems to be unsettled. Patients with cancer of oral tongue present to head and neck surgeons at early stages because of early complaints and easy diagnosis. In spite of early presentation, cancer of oral tongue behaves aggressively. Among the oral cavity sites, the tongue carries the highest incidence of delayed development of nodal disease if they are not present at the time of admission.4 Furthermore, regional recurrence is the most common cause of failure after surgical treatment of early tongue cancer.5 The reliability of clinical examination of the neck is between 50% and 80%.6-8 It is obvious that one can not solely depend on neck palpation for determination of neck metastasis. Different gures are given for occult neck metastasis in the literature. The incidence of occult neck metastasis varies from 16% to 38% for T1, 21% to 57% for T2, and up to 77% for T3 oral cavity tumors.2,4,9-15 Our results of 21.7% for T1-2, 58.3% for T3-4, and 29.3% overall false-negative neck examination are compatible with these gures and are too high to take the risk of neck recurrence with hemiglossectomy alone. Palpation is the most practical means of staging the neck; however, its false-negative rate approaches to 30%. The risk of undetected metastases can be improved from approximately 30% to 7.5% by using computerized tomography, magnetic resonance imaging, and ultrasound-guided ne-needle aspiration cytology in patients who are previously staged as N0 by clinical palpation alone.16,17 However, Byers et al18 found that the use of computerized tomography and ultrasonography was not better than the clinical examination in determining the presence or absence of nodal metastases of tongue cancer.

Elective lymph node dissection is dependent on the philosophy and experience of the surgeon, but it is generally suggested that elective neck dissection is to be performed in the presence of advanced stage tumor, delay in therapy, inadequate follow-up potential, recurrence, poor differentiation, perineural invasion, and aggressive and inltrating tumor.19 Fakih et al2 and Jesse et al20 do not support the idea of elective neck dissection in early tongue cancer cases, whereas Spiro and Strong,3 Cunningham et al,21 Kligerman et al,22 Yii et al,23 and Beenken et al24 favor elective dissection. However, clear-cut indications for and against elective dissection are absent, and the issue of performing and not performing dissection in early cases is still controversial. Fakih et al2 failed to show a signicant survival difference between patients who underwent elective radical neck dissection and those who did not. They determined tumor thickness as the major determinant of neck metastasis, and proposed that a policy of interval elective radical neck dissection only in those with a tumor depth of greater than 4 mm might optimize cure rates and avoid neck dissection in those who are unlikely to develop neck recurrence. Furthermore, they indicated that highly successful local control could be achieved by peroral excision of T1 or T2 cancer of oral tongue. Jesse et al20 indicated that the percentage of patients who would benet from elective neck dissection was too small. Maddox11 determined 3 risk factors for occult metastases clinical size of the primary tumor, perineural invasion, and sex. He believed that patients with primary tumors of 1 cm or less in diameter should not have elective treatment to the at-risk neck, whereas those having tumors greater than 3 cm in diameter and those having tumors with perineural invasion should have elective treatment. He observed 25% recurrence in the neck after observation. Franceschi et al25 observed a signicant improvement in 5-year survival when compared with the preceding 10-year period, which they believed was related to a more aggressive and effective treatment of the neck. They found 41% positive nodes in elective dissection of T1-2 lesions. However, they could not show

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any difference in 5-year survival between patients with elective dissection and N0 patients who subsequently developed a neck recurrence and underwent a therapeutic node dissection in stage I and II tongue cancer cases. Hicks et al26 recommended elective neck dissection for lesions that are T2 and above. They did not propose elective dissection for T1 lesions, even though 5 of 7 regional recurrences that they observed were on T1 lesions. Byers et al18 supported elective dissection for all T2-4 cases and T1 cases with poor differentiation, with a double DNA-aneuploid tumor, and with a depth of muscle invasion greater than 4 mm, but not for the other T1 patients. This study and many others do not support these hypotheses. High incidence of neck recurrence were documented in those patients with T1 and T2 tumors that were treated by primary tumor excision alone.21,24 Cervical node metastases developed subsequently in 38% 43% of patients treated by glossectomy alone.3,23,24 In the series of Beenken et al24 there were no regional recurrences after elective dissection in T1-2 tongue cancer cases. Furthermore, Kligerman et al22 determined fewer neck recurrences and better survival rates for patients who were treated by resection with supraomohyoid neck dissection than those who had undergone resection alone. Yii et al23 determined signicantly lower regional recurrence rate in early tongue cancer patients with elective dissection than observation alone, whereas 5-year survival was not signicantly different (75% vs. 65%, respectively). However, Yuen et al5 found out that elective dissection signicantly reduced mortality caused by regional recurrence and also increased the overall survival. In predicting the clinical course of oral cavity cancer, the status of regional nodes is the single most important factor.4 Histopathologic examination of cervical lymphatics is necessary for accurate staging, because TNM staging has been of limited help in identifying patients who might possibly benet from an elective neck dissection.2,12,27 Minute cervical carcinoma cell populations may be missed in the histopathologic sampling process, removal of which may account for the high survival rate of patients with both

clinically and histologically negative neck.21 Therefore, the gures for occult node metastasis should be higher, and elective neck dissection not only performs staging but it also cures more patients of cancer than expected. Spiro and Strong28 found a prolonged survival in patients with cancer of oral tongue and N0 neck who were detected to have occult cervical node metastasis after neck dissection when compared with patients with N neck at admission. Elective treatment of the neck has increased, prompted by the high incidence of neck failure when lymphadenectomy is deferred until metastases appear.28,29 Inasmuch as viable tumor cells may be present in the lymphatics between the primary and involved regional nodes, the neck operation is performed in continuity with excision of the primary tumor. Spiro and Strong3 claim that partial glossectomy, and radical neck dissection can be performed in discontinuity without apparent adverse effect on either local recurrence or cure rate. The salvage rate for patients with recurrent disease is 0% regardless of the initial size of the lesion, the status of the cervical nodes, or the treatment of recurrence.30 Once local or regional recurrence appears, the prognosis is absolutely poor without long-term survivors. Therefore, the head and neck surgeon should try to prevent recurrence with the best possible resection and necessary adjunctive therapy.31 In the management of early carcinoma of tongue, there is a survival advantage if metastases are treated while still occult, rather than delaying therapy until they become palpable.12 Having undergone neck dissection, patients with metastases that are limited to cervical lymph nodes have survival similar to patients with no cervical metastasis.27 Supraomohyoid neck dissection with frozen-section analysis in the management of clinically negative neck provides an adequate sample of lymph nodes in cases of oral cancer, restricts the number of radical and modied radical neck dissection preventing unnecessary morbidity, and allows more selective use of postoperative radiation.5,7,25,32,33 Regional recurrence rate after supraomohyoid neck dissection has been only 5%.33 It has been recommended that, for oral tongue lesions, level IV must also be treated because of the frequent

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skip metastases to level III and IV.34,35 Furthermore, Yuen et al36 have recently indicated that elective supraomohyoid neck dissection is an effective but not adequate therapeutic procedure, and that postoperative adjuvant radiotherapy and chemotherapy have to be considered for all pathologically positive necks. In our study, the gures indicate that 70.3% of patients will undergo questionably unnecessary neck dissection, whereas 29.3% of patients will be cured of occult neck metastasis, thereby preventing early neck recurrence. Rassekh et al37 indicated that intraoperative staging of clinically N0 necks did not signicantly improve the false-negative rate of clinical staging, and that intraoperative staging had 73% false-positive rate in upstaging the neck. They recommended the use of frozensection biopsy before converting the selective dissection to a radical or modied radical neck dissection. Our study also showed that intraoperative staging of suspicious lymph nodes has moderate sensitivity but low specicity; that is, it determines the metastatic nodes with moderate accuracy, but the nonmetastatic nodes are generally evaluated incorrectly. Elective neck dissection makes the stages of patients accurate and determines the need for adjunctive therapy. Submandibular and upper cervical regions were most commonly involved by cervical metastasis of tongue cancer. Only one N0 patient had metastatic lower cervical node. Posterior cervical nodes were never involved by N0 tongue cancer. The increased incidence of contralateral neck recurrence after elective neck dissection in conjunction with primary tumor resection has been noted, and this has been suggested to be attributable to aberrant migration of in transit cancer cells to the opposite side of the neck.25 We also observed more contralateral neck recurrence than ipsilateral after elective neck dissection. As a conclusion, the rate of occult metastasis to the neck is too high in all tongue cancer cases to take the risk of regional recurrence. Radiologic investigations and ne-needle aspiration decrease, but never reduce to zero the rate of false-negative examination. There is an obvious indication for neck dissection, even in early cases.

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of the tongue in persons younger than 30 years of age. Arch Otolaryngol 109:302-304, 1983 31. Saroglu T, Ylmaz T, Sungur A, et al: The effect of lymphocytic inltration on clinical survival in cancer of the tongue. Eur Arch Otorhinolaryngol 251:366-369, 1994 32. van den Hoogen FJA, Manni JJ: Value of the supraomohyoid neck dissection with frozen section analysis as a staging procedure in the clinically negative neck in squamous cell carcinoma of the oral cavity. Eur Arch Otorhinolaryngol 249:144-148, 1992 33. Spiro JD, Spiro RH, Shah JP, et al: Critical assessment of supraomohyoid neck dissection. Am J Surg 156: 286-289, 1988 34. Byers RM, Weber RS, Andrews T, et al: Frequency and therapeutic implications of skip metastasis in the neck from squamous carcinoma of the oral tongue. Head Neck 19:14-19, 1997 35. Clayman GL, Frank DK: Selective neck dissection of anatomically appropriate levels is as efcacious as modied radical neck dissection for elective treatment of the clinically negative neck in patients with squamous cell carcinoma of the upper respiratory and digestive tracts. Arch Otolaryngol Head Neck Surg 124:348-352, 1998 36. Yuen AP, Lam KY, Chan AC, et al: Clinicopathological analysis of elective neck dissection for N0 neck of early oral tongue carcinoma. Am J Surg 177:90-92, 1999 37. Rassekh CH, Johnson JT, Myers EN: Accuracy of intraoperative staging of the N0 neck in squamous cell carcinoma. Laryngoscope 105:1334-1336, 1995