ORIGINAL ARTICLE Selective vs Modified Radical Neck Dissection and Postoperative Radiotherapy vs Observation in the Treatment of Squamous Cell Carcinoma of the Oral Tongue

Bradley A. Schiff, MD; Dianna B. Roberts, PhD; Adel El-Naggar, MD, PhD; Adam S. Garden, MD; Jeffrey N. Myers, MD, PhD

Objectives: To assess the role of selective neck dissec- Results: For clinically Nϩ patients, 5 of 45 treated with tion in patients with squamous cell carcinoma (SCC) of selective neck dissection and 1 of 19 treated with radi- the oral tongue with advanced nodal disease, and to as- cal or modified radical neck dissection had recurrences sess the role of postoperative radiotherapy in patients with in the ipsilateral neck. If only patients with significant SCC of the oral tongue with pathologically N1 necks. tumor burden on final pathological examination (clini- cally Nϩ/pathologically N2) are considered, 4 (25.0%) Design: Retrospective study of the medical records of of 16 patients undergoing selective neck dissection had all patients who underwent neck dissection for SCC of recurrences in the neck, while none of the 14 patients the oral tongue from January 1, 1980, to December 31, treated with radical or modified radical neck dissection 1995. Median follow-up was 5.7 years. had recurrences in the ipsilateral neck (P=.07). Of the 50 patients who had pathologically N1 disease, 25 re- Setting: The University of Texas M. D. Anderson Can- ceived postoperative radiotherapy and 25 did not. Of the cer Center, Houston, a tertiary care cancer hospital. latter, 2 had recurrences in the neck, while none of the 25 patients who received radiotherapy had recurrences Patients: A total of 220 patients with SCC of the oral in the neck (P=.24). tongue who received surgical treatment of both the pri- mary tumor and the neck and who had an identifiable Conclusions: Selective neck dissection may be suffi- type of neck dissection, no synchronous or metachro- cient for many Nϩ patients with SCC of the oral tongue, nous lesions, and no evidence of local recurrence. but some patients with extensive nodal disease may ben- efit from more aggressive treatment of the neck. Radio- Interventions: All patients underwent resection of the therapy may be beneficial for all of the node-positive pa- primary tumor and neck dissection. The extent of neck tients, but further studies are needed. Prospective, dissection was determined by surgeon preference. Some randomized clinical trials will be useful in further defin- patients received radiotherapy to the neck as well. ing the role of selective neck dissection in the clinically N2 neck and radiotherapy in the N1 neck for patients Main Outcome Measures: Clinical and pathological with SCC of the oral tongue. nodalstatus,typeofneckdissection,anduseofradiotherapy. The end points evaluated included the regional control rates. Arch Otolaryngol Head Neck Surg. 2005;131:874-878

HE TREATMENT OF THE NECK sternocleidomastoid muscle, and spinal ac- in oral cavity cancer has un- cessory nerve, based on an understand- dergone numerous changes ing of the fascial planes and lymphatic during the past 50 years. Author Affiliations: Radical neck dissection was CME course available at Departments of Head and Neck first described by Crile in 19061 and popu- T 2 Surgery (Drs Schiff, Roberts, larized by Martin et al, and it was the main www.archoto.com El-Naggar, and Myers), surgical treatment of cervical lymphade- Radiation Oncology nopathy secondary to squamous cell car- anatomy of the neck. Bocca and Pigna- (Dr Garden), and Pathology cinoma (SCC) until the last third of the taro4 subsequently presented this proce- (Dr El-Naggar), The University 20th century. The cosmetic and func- dure in the English-language literature, and of Texas M. D. Anderson Ballantyne5 pioneered its use in the United Cancer Center, Houston; and tional defects associated with radical neck Department of Otolaryngology, dissection prompted the search for less States. Modified radical neck dissection, Albert Einstein College of morbid alternatives. According to Ferlito which is often oncologically equivalent to Medicine, Montefiore Medical and Rinaldo,3 Suárez suggested a modi- radical neck dissection but with a signifi- Center, Bronx, NY (Dr Schiff). fied dissection preserving the jugular vein, cant improvement in postoperative mor-

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 bidity, gradually replaced radical neck dissection in the treatment of the neck for many patients with SCC of the Table 1. Total and Ipsilateral Regional Recurrence oral tongue. Detailed examination of lymphatic drain- in All Neck Dissections age patterns by Rouvierre and others6-9 showed levels I and II to be the main sites of drainage for SCC of the oral No. tongue, with levels IV and V playing a lesser role. Work Pathological No by Lindberg,7 Byers,10 andShahetal11 further eluci- Neck Stage Radiotherapy Radiotherapy Total dated the patterns of lymphatic drainage most common Total Regional Recurrences for SCC of the oral tongue, establishing the rationale for pN0 6/102 1/17 7/119 selective neck dissections of specific lymph node levels pN1 4/25 0/25 4/50 initially developed by Suárez.3,5 One particular selective pN2b 0/3 10/42 10/45 pN2c 0 1/6 1/6 neck dissection, that of levels I to III—also known as the Total, No. (%) 10/130 (7.7) 12/90 (13.3) 22/220 (10.0) supraomohyoid neck dissection12—has been com- monly used in the management of the clinically node- Ipsilateral Regional Recurrences pN0 4/102 1/17 5/119 negative neck in patients with SCC of the oral tongue. pN1 2/25 0/25 2/50 13 Many studies, including one performed prospectively, pN2b 0/3 5/42 5/45 have shown that the supraomohyoid neck dissection pro- pN2c 0 1/6 1/6 vides control rates similar to that of modified radical neck Total, No. (%) 6/130 (4.6) 7/90 (7.8) 13/220 (5.9) dissection for patients with N0 oral cavity SCC. The role of selective neck dissection in patients with clinically evident nodal disease (cNϩ) is more contro- versial. Medina and Byers12 suggested supraomohyoid neck dissection for patients with N0 disease and select METHODS patients with N1 disease, while Shah and Andersen14 rec- ommended supraomohyoid neck dissection for patients We reviewed the medical records of all patients treated at The with N0 disease, but modified radical neck dissection with University of Texas M. D. Anderson Cancer Center, Houston, sacrifice of the sternocleidomastoid muscle and the in- for SCC of the oral tongue from January 1, 1980, through ternal jugular vein for patients with nodal disease. More December 31, 1995. We identified 266 patients who underwent 15-17 surgery that included a neck dissection. Patients who had an un- recent articles have suggested that selective neck dis- specified type of neck dissection, had synchronous or metachro- section is adequate surgical treatment for certain pa- nous lesions, or experienced local recurrence were eliminated tients with N2 disease. However, no prospective clinical from the study. Of the 266 patients with SCC of the tongue, 220 studies exist to prove the efficacy of supraomohyoid neck met the foregoing criteria. dissection compared with modified radical neck dissec- The major variables examined were the clinical and pathologi- tion in patients with SCC of the oral tongue with node- cal nodal status, type of neck dissection received, and use of positive necks. radiotherapy. The end points evaluated included the regional con- The role of postoperative radiotherapy in treatment trol rates. Follow-up time was calculated from the patient’s of the neck in patients with SCC of the oral tongue also initial visit at M. D. Anderson Cancer Center for treatment of the continues to evolve. Studies by Meoz et al18 and Leborgne primary tumor until the date of last contact or death. The use of 19 preoperativeimagingwasdependentonsurgeonpreference.Ninety- et al show that radiotherapy is a viable modality for six (36.1%) of 266 patients underwent preoperative imaging. Ap- elective treatment of the neck. There is evidence that proximately 90% (86/96) of these patients were treated after 1990. postoperative radiotherapy to the neck improves locore- Differences in the proportions of patients who developed disease gional control,20 and adjuvant radiation is often used af- recurrences were tested by the Pearson ␹2 test. If there were 10 ter neck dissections for patients with significant nodal or fewer patients in a group, the 2-tailed Fisher exact test was used. disease. The criteria for neck radiation are not well es- The ␹2 tests were performed with the assistance of the Statistica tablished, and radiation can be given postoperatively on statistical software application (StatSoft, Tulsa, Okla). the basis of either characteristics of the primary tumor or pathological features of the neck dissection speci- RESULTS men. Radiotherapy is often given to patients with ad- vanced-stage disease, close or inadequate surgical mar- REGIONAL CONTROL RATES FOR PATIENTS gins, unfavorable histologic findings including TREATED WITH SELECTIVE NECK DISSECTION lymphovascular invasion or perineural spread, multiple AND MODIFIED RADICAL OR RADICAL or large lymph node metastasis, or the presence of ex- NECK DISSECTION tracapsular spread.14 The role of radiotherapy for the N1 neck without extracapsular spread, however, is not well We reviewed the records of the 220 patients with oral tongue established. cancer treated with resection of the primary tumor and neck Given the lack of information on the role of selective dissection with or without adjuvant treatment and found neck dissection in patients with SCC of the oral tongue with that 22 patients (10.0%) had recurrences in the neck alone advanced nodal disease, and the potential benefit of post- (Table 1). Of these patients, 13 (5.9% of the 220) had re- operative radiotherapy in patients with SCC of the oral currences in the ipsilateral neck. tongue with pathologically N1 (pN1) necks, we reviewed To determine the impact of the type of neck dissection our experience with these interventions for patients with on regional failure in patients treated for oral tongue can- tongue cancer treated at our institution from 1980 to 1995. cer, we noted that 195 underwent selective neck dissections

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Table 2. Ipsilateral Regional Recurrence in Selective Neck Table 4. Ipsilateral Regional Recurrence in Radical/ Dissection and Radical/Modified Radical Neck Dissection Modified Radical Neck Dissection for Clinically N؉ Necks

No. No.

Pathological No Pathological No Neck Stage Radiotherapy Radiotherapy Total Neck Stage Radiotherapy Radiotherapy Total Selective Neck Dissection pN0 0 0/2 0/2 pN0 4/99 1/15 5/114 pN1 0/1 0/1 0/2 pN1 2/24 0/23 2/47 pN2b 0 0/14 0/14 pN2b 0/3 5/27 5/30 pN2c 0 1/1 1/1 pN2c 0 0/4 0/4 Total, No. (%) 0/1 1/18 (5.6) 1/19 (5.3) Total, No. (%) 6/126 (4.8) 6/69 (8.7) 12/195 (6.2) Radical/Modified Radical Neck Dissection pN0 0/3 0/2 0/5 pN1 0/1 0/2 0/3 pN2b 0 0/15 0/15 or modified radical neck dissection more commonly pN2c 0 1/2 1/2 were staged pN2. For patients with cNϩ disease with Total, No. (%) 0/4 1/21 (4.8) 1/25 (4.0) advanced pathological staging (pN2), differences in regional control were seen according to neck dissection type. Of the 16 patients with clinically positive disease staged pN2b who were treated with a selective neck dis- Table 3. Ipsilateral Regional Recurrence in Selective Neck section, 4 (25.0%) had recurrences in the ipsilateral Dissection for Clinically N0 and N؉ Necks neck. All but 1 of the 16 patients received postoperative radiotherapy, and 10 of the 16 had extracapsular No. spread. Of the 14 patients with clinically positive dis- ease and 2 or more disease-positive lymph nodes found Pathological No on pathological examination that were treated with Neck Stage Radiotherapy Radiotherapy Total radical or modified radical neck dissection, none had Clinically N0 Necks recurrences in the ipsilateral neck (P =.07). All 14 pN0 3/88 1/13 4/101 patients received postoperative radiotherapy, and 10 of pN1 2/20 0/13 2/33 pN2b 0/2 1/12 1/14 the 14 had extracapsular spread. pN2c 0 0/2 0/2 Total, No. (%) 5/110 (4.5) 2/40 (5.0) 7/150 (4.7) IMPACT OF POSTOPERATIVE RADIOTHERAPY Clinically N؉ Necks ON REGIONAL RECURRENCE pN0 1/11 0/2 1/13 pN1 0/4 0/10 0/14 Postoperative radiotherapy was administered to 69 (35.4%) pN2b 0/1 4/15 4/16 of 195 patients who underwent selective neck dissections pN2c 0 0/2 0/2 and 21 (84.0%) of 25 patients who underwent radical or Total, No. (%) 1/16 (6.3) 4/29 (13.8) 5/45 (11.1) modified radical neck dissections (Table 2), for a total of 90 (40.9%) of 220 patients. Radiotherapy was delivered to 17 (14.3%) of 119 patients with pN0 disease, 25 (50.0%) of 50 patients with pN1 disease, 42 (93.3%) of 45 patients and 12 (6.2%) of these had disease recur in the ipsilateral with pN2b disease, and 6 of 6 patients with pN2c disease neck, while 1 (4.0%) of 25 patients who underwent radi- (Table 1). No patients had N2a or N3 disease. Of the pa- cal neck dissection had disease recur in the ipsilateral neck tients who received postoperative radiotherapy, 7 (7.8%) (Table 2). These data suggest that excellent regional con- of 90 had recurrences in the treated neck: 1 (5.9%) of 17 trol could be obtained with either type of neck dissection. patients who had pN0 disease, 0 of 25 patients who had pN1 Further examination of these results and their depen- disease, 5 (11.9%) of 42 patients who had pN2b disease, dence on clinical nodal status showed differences in con- and 1 (16.7%) of 6 patients who had pN2c disease (Table 1). trol dependent on the type of neck dissection selected. Of the 50 patients found to have pN1 disease after neck In the case of 150 patients without clinically evident nodal dissection, 47 had been treated with a selective neck dis- disease (cN0) who were treated with selective lymph node section and 3 had undergone a radical or modified radi- dissection of levels I to III or I to IV, 7 (4.7%) developed cal neck dissection. Among these 50 patients, 40 did not ipsilateral regional recurrence, indicating acceptable re- have extracapsular spread and 10 did. Half of the 50 pa- gional control with selective neck dissection for pa- tients did not receive postoperative radiotherapy and half tients with cN0 disease (Table 3). did. We examined the impact of adjuvant radiotherapy If data from only patients with clinically positive in this group of patients; 2 (8.0%) of 25 patients who did nodes are examined, then 5 (11.1%) of 45 patients not receive postoperative radiotherapy had ipsilateral re- (Table 3) treated with selective neck dissection and 1 gional recurrence, whereas 0 of 25 patients who re- (5.3%) of 19 patients (Table 4) treated with radical or ceived postoperative radiotherapy had recurrences in the modified radical neck dissection had recurrences in the neck (P=.24). Of the 40 patients without extracapsular ipsilateral neck. However, patients treated with radical spread, 2 (8.7%) of 23 who did not receive radiotherapy

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 experienced ipsilateral regional recurrence, whereas 0 of 17 patients who received radiotherapy experienced re- Table 5. Ipsilateral Regional Recurrence in All Neck gional recurrence. Although there was a lower inci- Dissections for Pathologically N1 Disease With or Without Radiotherapy dence of regional recurrence for patients with pN1 dis- ease without extracapsular spread who received No. (%) postoperative radiotherapy vs those who did not receive postoperative radiotherapy, the difference was not sta- No tistically significant (P=.32) (Table 5). pN1 Disease Radiotherapy Radiotherapy Total No extracapsular spread 2/23 (8.7) 0/17 2/40 (5.0) Extracapsular spread 0/2 0/8 0/10 COMMENT Total 2/25 (8.0) 0/25 2/50 (4.0)

The treatment of the neck for SCC of the oral tongue has undergoneconsiderablerefinementduringthepast50years. In the case of the N0 neck, selective neck dissection of lymph neck dissection needed for patients with significant nodal node levels I to III or I to IV has gained wide acceptance as disease, because of the difference in tumor burden on fi- management of the neck for patients with SCC of the oral nal pathological evaluation between patients treated with tongue. The current study documents our observed regional radical or modified radical neck dissection and selective recurrence rate of 7.3% (4.7% if only ipsilateral recurrence neck dissection, and because of the fact that preoperative isconsidered)in150patientswithcN0SCCoftheoraltongue imaging was rarely performed (decreasing the sensitivity treated with selective neck dissection, which is in excellent of clinical staging), we decided to compare patients with agreement with regional recurrence rates reported by other cNϩnecks who also had 2 or more positive nodes on patho- investigators.12,13,21-24 logical examination. We believe that, in this study, this The extent of neck dissection needed for patients with group of patients most accurately represents patients with SCC of the oral tongue with positive cervical lymphade- significant tumor burden. On pathological review of the nopathy is more controversial than the management of the surgical specimens, none of the 220 patients included in N0 neck. Kowalski and Carvalho17 suggested that selec- the study had pN2a disease. Every patient with a lymph tive neck dissection may be feasible in patients with N1 or node larger than 3 cm that was positive on pathological N2a disease. However, their conclusion was based not on examination had additional positive lymph nodes. a comparison of selective and modified radical neck dis- We found 30 patients who had clinically positive lymph section but on the fact that no patient who underwent radi- nodes that were pathologically staged N2 or greater. Of these cal neck dissections had metastasis to level IV or V. Traynor patients, 16 underwent selective neck dissection, and 14 un- et al16 examined 29 patients with upper aerodigestive tract derwent radical or modified radical neck dissection. The use SCC who presented with N1 or N2 disease and under- of selective vs radical neck dissection in this group was based went a selective neck dissection. Only 1 of the 29 patients on surgeon preference. This selection bias and the retrospec- experienced recurrence in the neck, again suggesting that tive nature of this work are the major flaws of the current selective neck dissection may be effective in patients with study. The incidence of extracapsular spread and the use of N1 or N2 disease. Andersen et al15 looked at 106 patients postoperative radiotherapy were very similar between the with N1 or greater disease treated with selective neck dis- 2 groups. Four of the 16 patients who underwent selective section and found a control rate of 94.3%. However, only neck dissection experienced ipsilateral regional recurrence, 31% of these patients had N2a or N2b disease. whereas none of the 14 patients who underwent radical or We initially studied all patients with cNϩ disease, con- modified radical neck dissection had ipsilateral regional re- centrating on the differences in regional control among currence. The difference in incidence of regional recurrences patients who underwent radical or modified radical neck betweenthe2groupswasnotstatisticallysignificant(P=.07). dissection or selective neck dissection. For the patients While the data are not statistically significant, they do sug- in this study, there was no significant difference in regional gestthatmoreaggressivetreatmentoftheneck,perhapseither recurrence between patients with cNϩ disease receiving more aggressive surgery or more aggressive postoperative selective and radical or modified radical neck dissection. therapy (chemotherapy or radiotherapy), may be needed in However, the patients undergoing radical or modified radi- patients with significant tumor burden. cal neck dissection had a substantially higher disease bur- For patients with intermediate nodal stage (N1) with den on final histologic examination. Of the 19 patients with or without extracapsular spread, the type of neck dissec- cNϩ disease treated with radical or modified radical neck tion performed is probably less critical for regional con- dissection,15(78.9%)werestagedatN2borhigher,whereas trol, and the role of postoperative radiotherapy appears less only 18 (40.0%) of the 45 patients with cNϩdisease treated clear. Although numerous studies have supported the withselectiveneckdissectionwerestagedatpN2borhigher. efficacy of postoperative radiotherapy in cancer of the head In addition, only 36.1% of patients involved in this study and neck,20,26 few have concentrated on the role of radia- underwent preoperative imaging. Because computed to- tion specifically for patients with cancer of the oral tongue. mography is a more sensitive method of determining nodal However, the use of radiotherapy for the adjuvant treat- status than physical examination in patients with SCC of ment of SCC of the oral tongue has increased in many the oral tongue,25 clinical staging does not accurately rep- institutions.27 Indications are not standardized, but post- resent discernible tumor burden for the patients in this operative radiotherapy is often used for patients with study. Because our goal was to investigate the extent of advance-stage disease, close or inadequate surgical mar-

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 gins, or unfavorable pathological findings, including lym- Submitted for Publication: September 10, 2004; final re- phovascular invasion or perineural spread, multiple or large vision received May 10, 2005; accepted May 10, 2005. lymph node metastasis, and the presence of extracapsular Correspondence: Jeffrey N. Myers, MD, PhD, Department spread.27 Most current practitioners would not recom- of Head and Neck Surgery, The University of Texas M. D. mend radiotherapy for patients with a single positive lymph Anderson Cancer Center, 1515 Holcombe Blvd, Unit 441, node smaller than 3 cm, provided that the characteristics Houston, TX 77030-4009 ([email protected]). of the primary tumor did not indicate postoperative radio- Financial Disclosure: None. therapy, especially if no extracapsular spread was present. We explored the role of postoperative radiotherapy for the N1 neck by looking at the 50 patients with pN1 disease. Of those 50 patients, 25 received postoperative radiotherapy REFERENCES and 25 did not. Forty of the 50 patients did not have ex- tracapsular spread. Two of the 25 patients who underwent 1. Crile G. Excision of cancer of the head and neck. JAMA. 1906;47:1780-1786. 2. Martin H, Del Valle B, Ehrlich H, Cahan WG. Neck dissection. Cancer. 1951;4:441-499. selective neck dissection and did not receive radiotherapy 3. Ferlito A, Rinaldo A. Osvaldo Suárez: often-forgotten father of functional neck had recurrences in the ipsilateral neck, whereas none of the dissection (in the non–Spanish-speaking literature). Laryngoscope. 2004;114: patients who received radiotherapy had recurrences. This 1177-1178. difference was not statistically significant (P=.24). 4. Bocca E, Pignataro O. A conservation technique in radical neck dissection. 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