Relevance of level I and IIB neck dissection in laryngeal cancer
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1 The Journal of Laryngology & Otology (2012), 126, JLO (1984) Limited, 2012 doi: /s MAIN ARTICLE Relevance of level I and IIB neck dissection in laryngeal cancer S WIEGAND 1, J ESTERS 1, H-H MÜLLER 2, T JÄCKER 3, M ROESSLER 4, J A FASUNLA 1, J A WERNER 1, A M SESTERHENN 1 Departments of 1 Otolaryngology, Head and Neck Surgery, and 3 Anaesthesia and Critical Care, and Institutes of 2 Medical Biometry and Epidemiology, and 4 Pathology, Giessen and Marburg University Hospital, Marburg, Germany Abstract Objectives: Dissection of neck levels I and IIB is time-consuming and can cause comorbidity. This study aimed to determine whether level I and IIB neck dissection was necessary in patients with laryngeal cancer and clinically detectable or nondetectable neck nodes. Patients and methods: This was a retrospective review of 73 patients with laryngeal cancer. Essential clinical data were obtained and analysed to determine the incidence of neck node metastasis in levels I and IIB. Results: Of the 48 patients with no clinically apparent neck nodes, none had level I metastases and only one had level IIB metastases. Of the patients with clinically detectable neck nodes, three of 21 patients had level I metastases and three of 25 patients had level IIB metastases; these six patients also had additional metastases in level IIA. Conclusion: Dissection of neck levels I and IIB is justifiable in laryngeal cancer patients with clinically detectable neck nodes and suspicious lymph nodes in the respective level or level IIA. However, in patients without clinically detectable neck nodes, preservation of levels I and IIB is oncologically safe, economical and reduces the risk of comorbidity. Key words: Larynx; Carcinoma, Squamous Cell; Neck Dissection Introduction The presence of cervical lymph node metastases is one of the most important prognostic factors in patients with laryngeal carcinoma. 1,2 Although the morbidity associated with laryngeal cancer has significantly reduced in recent times, the oncological outcome still remains unimpressive. 2 A few researchers advocate a policy of watchful waiting in the treatment of laryngeal cancer patients with no clinically apparent neck nodes (i.e. N 0 ). 3 Studies have shown that per cent of laryngeal cancer patients with a clinical N 0 neck harbour occult cervical metastasis. 3 5 The available radiological investigative tools (e.g. ultrasonography, computed tomography (CT) and magnetic resonance imaging (MRI)) are helpful in identifying lymph node metastasis but have a low sensitivity. 4 Although neck dissection is often included in the treatment protocol of these patients, the value of elective treatment of the clinically N 0 neck with selective neck dissection or modified radical neck dissection requires investigation. In patients with clinically apparent neck nodes (i.e. N + ), a modified radical neck dissection is often favoured, which includes dissection of levels I to V. 3 The appropriate extent of neck dissection for different indications has been widely discussed in the literature. 2 6 When healthcare resources become scarce, especially with regards to staff, materials and time, operative procedures need to be economised. In such circumstances, the efficiency of time-consuming surgical interventions must be re-evaluated. The dissection of certain neck levels is considered to be time-consuming and associated with particular complications. Neck level I contains important structures such as lymphatics, the submandibular gland, the marginal branch of the facial nerve, the lingual and facial arteries, the lingual and hypoglossal nerves, and the facial vein. All of these important structures are vulnerable to injury during neck dissection, with very significant consequences. Neck level IIB contains the accessory nerve as its cardinal structure, as well as multiple vascular structures in the area of the submuscular Accepted for publication 24 October 2011 First published online 15 June 2012
2 796 recess. Special care must be taken during the dissection of this level, prolonging the operation time. Level I is not included as part of the main lymphatic drainage of tumours of the larynx. 6 However, in laryngeal tumour patients surgical dissection of the neck frequently reveals metastatic lymph nodes in level IIA, while levels I and IIB are considered to be at low metastatic risk. Therefore, this study aimed to verify whether inclusion of levels I and IIB during neck dissection is justified in laryngeal cancer patients who are clinically N 0 or N +. Materials and methods This was a retrospective review of patients who had undergone surgical treatment for laryngeal tumour, including neck dissection, at the Department of Otorhinolaryngology, Head and Neck Surgery of Philipps University Marburg, Germany, over a 10- year period (April 1998 to August 2008). Patients who had received primary chemoradiotherapy or who had undergone previous neck treatment were excluded from the study. The following clinical data were obtained from patients medical records: sex, site of primary lesion, tumour-node-metastasis (TNM) staging status, 7 operative procedure (especially type of neck dissection), and number and level of cervical lymph node metastases. Patients necks were examined with ultrasonography and thereafter appropriately staged. Lymph nodes larger than 10 mm were considered suspicious for metastasis. In addition, and depending on the location of the primary tumour, CT or (in selected cases) MRI were also performed. After neck dissection, the neck node specimens were separated into different containers according to their neck level and sent to the Institute of Pathology for processing and examination. Pathological examination included assessment of the number of metastatic nodes in levels I, IIA, IIB, III and IV. The T and N stages were determined from the pathologist s report, while the M stage was determined by radiological investigation. Data were collated and analysed using the Statistical Package for the Social Sciences version software S WIEGAND, J ESTERS, H-H MÜLLER et al. program. Ninety-five per cent confidence intervals were calculated according to the method of Clopper and Pearson. 8 Results A total of 73 patients with squamous cell carcinoma of the larynx were included in the study. There were 67 (91.8 per cent) men and six (8.2 per cent) women, giving a sex ratio (male:female) of 11:1. Patients ages ranged from 41.7 to 79.2 years, with a mean age of 60.1 years. Forty-one (56.2 per cent) patients suffered from supraglottic carcinoma, 17 (23.3 per cent) from glottic carcinoma, three (4.1 per cent) from subglottic carcinoma and 12 (16.4 per cent) from transglottic laryngeal carcinoma. In 27 (37.0 per cent) patients, the tumour had crossed the midline to the contralateral side. The types of neck dissection performed in these patients are shown in Table I. Ipsilateral neck dissection was performed in all the patients, but 49 (67.1 per cent) patients also had associated contralateral neck dissection. In the ipsilateral neck, clinical nodal staging was N 0 in 48 patients and N + in 25 patients. In those who also underwent contralateral neck dissection, clinical nodal staging was N 0 in 43 patients and N + in six patients. The indications for contralateral neck dissection included transglottic laryngeal carcinoma, tumours crossing the midline to the contralateral side, and suspicious contralateral lymph nodes. There were no patients with distant metastases. The distribution of pathological staging is shown in Table II. Neck dissection involving level I was performed in 46 (63.1 per cent) patients, of whom 19 (41.3 per cent) had a bilateral neck dissection. The decision to undertake a contralateral neck dissection was based on the localisation and extent of the primary tumour. However, histological analysis of neck node specimens identified metastasis in only two (4.3 per cent) patients undergoing ipsilateral level I neck dissection. These patients also had metastases in their ipsilateral level IIA nodes. One (5.3 per cent) patient undergoing a bilateral neck dissection had bilateral nodal metastases in levels I and IIA, as well as ipsilateral metastases in level IIB; the ipsilateral side had been clinically N + and the contralateral side clinically N 0. Of these three TABLE I TYPES OF NECK DISSECTION Ipsilateral side (level) Contralateral side (level) (pts; n (%)) Total (pts; n (%)) No ND SND (I III) SND (I IV) SND (II III) SND (II IV) MRND SND (I III) 0 1 (1.4) (1.4) SND (I IV) 3 (4.1) 0 5 (6.8) 0 1 (1.4) 0 9 (12.3) SND (II III) (16.4) 0 12 (16.4) SND (II IV) 12 (16.4) (16.4) SND (II V) 1 (1.4) (1.4) 1 (1.4) 0 3 (4.1) MRND 8 (11) 2 (2.7) 3 (4.1) 1 (1.4) 14 (19.2) 8 (11) 36 (49.3) Total 24 (32.9) 3 (4.1) 8 (11) 2 (2.8) 28 (38.4) 8 (11) 73 (100) Pts = patients; ND = neck dissection; SND = selective neck dissection; MRND = modified radical neck dissection
3 LEVEL I AND IIB NECK DISSECTION IN LARYNGEAL CANCER 797 TABLE II PATHOLOGICAL STAGING N 0 N 1 N 2a N 2b N 2c N 3 Total T T T T Total Data represent patient numbers. N = node stage; T = tumour stage patients with histopathological neck node metastasis, two had supraglottic carcinoma and one had subglottic carcinoma. These tumours were staged as T 1 N 2b,T 1 N 2c and T 2 N 2b, based on histopathological analysis. All the patients had level II included in their neck dissection; 49 (67.1 per cent) patients had bilateral neck dissection while 24 (33 per cent) had ipsilateral neck dissection. The neck node specimens of 22 (30 per cent) patients were pathologically N + in level IIA. These nodal metastases were ipsilateral in 16 (73 per cent) patients, bilateral in five (23 per cent) and contralateral in one (4 per cent). The clinical nodal staging was N 0 in one patient and N + in 21 patients. Only four patients were pathologically N + in ipsilateral level IIB; their clinical staging was N 0 in one patient and N + in the remaining three patients. Only one of these patients had associated, synchronous, bilateral neck node metastases in level I. These four primary tumours were staged pathologically as T 1 N 2c,T 2 N 2b,T 2 N 2c and T 4 N 1. Patients with more than one metastasis underwent post-operative adjuvant chemoradiotherapy. The distribution of cervical lymph node metastases in levels I, IIA and IIB is shown in Tables III and IV. TABLE III DISTRIBUTION OF LYMPH NODE METASTASES IN IPSILATERAL LEVELS I, II, IIA AND IIB Patient parameter Level I Level II Level IIA Level IIB Total ND Total ND pts (n) pn + pts (n) pn + pts (% of total 73 ND pts) (95% CI) 4.1 ( ) 30.1 ( ) 28.8 ( ) 5.5 ( ) pn + pts (% of total ND pts for each ND level) (95% CI) 6.5 ( ) 30.1 ( ) 28.8 ( ) 5.5 ( ) ND in cn 0 pts Total cn 0 pts (n) pn + cn 0 pts (n) pn + cn 0 pts (% of 48 cn 0 pts) (95% CI) 0 (0 7.4) 4.2 ( ) 2.0 ( ) 2.0 ( ) pn + cn 0 pts (% of cn 0 pts for each ND level) (95% CI) 0 (0 13.7) 4.2 ( ) 2.0 ( ) 2.0 ( ) ND in cn + pts Total cn + pts (n) pn + cn + pts (n) pn + cn + pts (% of 25 cn + pts) (95% CI) 12.0 ( ) 80.0 ( ) 80.0 ( ) 12.0 ( ) pn + cn + pts (% of cn + pts for each ND level) (95% CI) 14.3 ( ) 80.0 ( ) 80.0 ( ) 12.0 ( ) ND = neck dissection; pts = patients; pn + = pathologically node-positive; CI = confidence interval; cn 0 = clinally node-negative; cn + = clinically node-positive TABLE IV DISTRIBUTION OF LYMPH NODE METASTASES IN CONTRALATERAL LEVELS I, II, IIA AND IIB Patient parameter Level I Level II Level IIA Level IIB Total ND Total ND pts (n) pn + pts (n) pn + pts (% of total 73 ND pts) (95% CI) 1.4 ( ) 8.2 ( ) 8.2 ( ) 0 (0 49.3) pn + pts (% of total ND pts for each ND level) (95% CI) 5.3 (0.1 26) 12.2 ( ) 12.2 ( ) 0 (0 7.3) ND in cn 0 pts Total cn 0 pts (n) pn + cn 0 pts (n) pn + cn 0 pts (% of 67 cn 0 pts ) (95% CI) 1.5 ( ) 3.0 ( ) 3.0 ( ) 0 (0 53.6) pn + cn 0 pts (% of cn 0 pts for each ND level) (95% CI) 6.7 ( ) 4.7 ( ) 4.7 ( ) 0 (0 8.2) ND in cn + pts Total cn + pts (n) pn + cn + pts (n) pn + cn + pts (% of 6 cn + pts) (95% CI) 0 (0 45.9) 66.7 ( ) 66.7 ( ) 0 (0 45.9) pn + cn + pts (% of cn + pts for each ND level) (95% CI) 0 (0 60.2) 66.7 ( ) 66.7 ( ) 0 (0 45.9) 43 patients + 24 patients who did not undergo contralateral surgery. ND = neck dissection; pts = patients; pn + = pathologically nodepositive; CI = confidence interval; cn 0 = clinally node-negative; cn + = clinically node-positive
4 798 Discussion The dissection of neck levels I and IIB is time-consuming because of their anatomical location. There is an associated risk of injury to adjacent structures, including blood vessels 9 and the accessory nerve (leading to shoulder dysfunction). 10,11 The present study findings agree with previous reports that not all clinically node-negative necks harbour occult metastasis, and that performing neck dissection thus increases operation time and morbidity risk unnecessarily in truly node-negative patients. Thus, the issue is the identification of cases in which neck dissection is justified, as opposed to those in which it can be omitted without impairing the oncological outcome. Numerous studies have demonstrated that lymph node metastases from laryngeal squamous cell carcinoma to level I are infrequent In patients with a clinically N 0 neck, only a few cases of occult metastasis to this region have been described. Some studies have found that neck dissection specimens from patients with a clinically N 0 neck contain no metastases. 14,16,17 The present study findings agree with the above-mentioned studies. In the present study, ipsilateral metastasis to level I was found in only 4.1 per cent of patients, and contralateral metastasis to level I in only 1.4 per cent. Based on the fact that patients with a clinically N 0 neck frequently have no level I metastases, several authors have recommended surgical therapy that preserves this region. 9,12 14,16,17 The findings from the present study support this recommendation. Some authors have stated that routine performance of neck dissection including level I in laryngeal cancer patients with a clinically N + neck is unjustified. 13,15,17,18 In the present study, all patients with pathologically proven nodal metastases in level I also had metastases in level IIA. Therefore, dissection of level I is recommended in cases in which ultrasound or CT reveal suspicious lymph nodes in levels I or IIA. Lymph node metastases greatly affect laryngeal carcinoma prognosis Level I and IIB dissection is time-consuming and increases costs Preservation of these levels in clinically nodenegative necks is cost-effective and lowers comorbidity, without oncological risk Patients with clinically apparent nodes in levels I, IIA and IIB should have these levels dissected The physiological lymphatic drainage of the supraglottic and glottic larynx is mainly to the lymph nodes in levels II and III. 19 The introduction of radiological investigative tools such as ultrasound and CT has helped to improve identification of neck node metastasis. According to the current understanding of the S WIEGAND, J ESTERS, H-H MÜLLER et al. lymphatic drainage pathway, laryngeal carcinomas metastasise firstly to levels II and III before reaching other lymph node regions. However, numerous evaluations of patients with laryngeal carcinoma have shown that metastases are rarely found in level IIB Metastases in this region are often associated with metastases in sublevel IIA. 28 In the present study, ipsilateral level II nodes were dissected in all 73 patients, and associated contralateral level I nodes in 49 patients. Level IIB metastases were found in 5.5 per cent of ipsilateral dissections and 0 per cent of contralateral dissections, a rather low incidence. In only one patient (2 per cent), with an advanced tumour stage (pathologically T 4 ) but a clinically N 0 neck, was a single metastasis found in level IIB. These results support the recommendation to preserve level IIB in patients with a clinically N 0 neck ,28 This approach seems to be oncologically safe and may prevent patients from developing the frequent complication of shoulder dysfunction, thus reducing post-operative morbidity. In our patients with a clinically N + neck, all those with metastases in level IIB had additional metastases in level IIA. Therefore, it is debatable whether it is necessary to dissect level IIB in all patients with a clinically N + neck, or whether it would be preferable to preserve level IIB in those patients with a clinically N + neck in whom pre-operative staging investigations show no suspicious lymph nodes in levels IIA or IIB. However, we recognise that not all patients in our study underwent bilateral neck surgery, and a broad spectrum of different types of neck dissection were performed. This may have biased our study findings. As not all patients underwent contralateral neck dissection, and level I dissection was not performed in all patients, the prevalence of metastasis may have been underestimated. Moreover, the 95 per cent confidence intervals calculated for all metastatic rates were often rather wide, because of the low number of cases. Conclusion In this study, laryngeal cancer patients with a clinically N + neck had a higher prevalence of lymph node metastases in level IIA compared with levels I and IIB. Therefore dissection of levels I, IIA and IIB is recommended in patients with clinically apparent lymph nodes in these levels. However, patients with a clinically N 0 neck rarely had metastases in levels I and IIB. These findings support previous recommendations for preservation of levels I and IIB in patients with a clinically N 0 neck. This approach has the advantages of better post-operative quality of life and greater cost-effectiveness (due to reduced surgical time), without any impairment of oncological outcomes. References 1 Kramer S, Marcial VA, Pajak TF, MacLean CJ, Davis LW. Prognostic factors for loco/regional control and metastasis and the impact on survival. Int J Radiat Oncol Biol Phys 1986;12: 573 8
5 LEVEL I AND IIB NECK DISSECTION IN LARYNGEAL CANCER Ferlito A, Rinaldo A, Silver CE, Robbins KT, Medina JE, Rodrigo JP et al. Neck dissection for laryngeal cancer. J Am Coll Surg 2008;207: Clayman GL, Frank DK. Selective neck dissection of anatomically appropriate levels is as efficacious as modified 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 1998;124: Ferlito A, Rinaldo A, Devaney KO, Nakashiro K, Hamakawa H. Detection of lymph node micrometastases in patients with squamous cell carcinomas of the head and neck. Eur Arch Otorhinolaryngol 2008;265: Waldfahrer F, Hauptmann B, Iro H. Lymph node metastasis of glottic laryngeal carcinoma [in German]. Laryngorhinootologie 2005;84: Ferlito A, Silver CE, Suarez C, Rinaldo A. Preliminary multiinstitutional prospective pathologic and molecular studies support preservation of sublevel IIB and level IV for laryngeal squamous cell carcinoma with clinically negative neck. Eur Arch Otorhinolaryngol 2007;264: Wittekind C, Meyer H-J, Bootz F, eds. International Union Against Cancer. TNM Classification of Malignant Tumours [in German], 6th edn. Berlin: Springer, Clopper C, Pearson S. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 1934;26: Wenig BL, Applebaum EL. The submandibular triangle in squamous cell carcinoma of the larynx and hypopharynx. Laryngoscope 1991;101: Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann Otol Rhinol Laryngol 2000;109: Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessory nerve after neck dissection. Am J Surg 1983;146: Candela FC, Shah J, Jaques DP, Shah JP. Patterns of cervical node metastases from squamous carcinoma of the larynx. Arch Otolaryngol Head Neck Surg 1990;116: Li XM, Wei WI, Guo XF, Yuen PW, Lam LK. Cervical lymph node metastatic patterns of squamous carcinomas in the upper aerodigestive tract. J Laryngol Otol 1996;110: Buckley JG, MacLennan K. Cervical node metastases in laryngeal and hypopharyngeal cancer: a prospective analysis of prevalence and distribution. Head Neck 2000;22: dos Santos CR, Goncalves Filho J, Magrin J, Johnson LF, Ferlito A, Kowalski L. Involvement of level I neck lymph nodes in advanced squamous carcinoma of the larynx. Ann Otol Rhinol Laryngol 2001;110: Byers RM, Wolf PF, Ballantyne AJ. Rationale for elective modified neck dissection. Head Neck Surg 1998;10: Mercante G, Bacciu A, Oretti G, Ferri T. Involvement of level I neck lymph nodes and submandibular gland in laryngeal and/or hypopharyngeal squamous cell carcinoma. J Otolaryngol 2006; 35: Ferlito A, Rinaldo A. Level I dissection for laryngeal and hypopharyngeal cancer: is it indicated? J Laryngol Otol 1998;112: Werner JA, Dünne AA, Myers JN. Functional anatomy of the lymphatic drainage system of the upper aerodigestive tract and its role in metastasis of squamous cell carcinoma. Head Neck 2003;25: Chone CT, Crespo AN, Rezende AS, Carvalho DS, Altemani A. Neck lymph node metastases to the posterior triangle apex: evaluation of clinical and histopathological risk factors. Head Neck 2000;22: Koybasioglu A, Uslu S, Yilmaz M, Inal E, Ileri F, Asal K. Lymphatic metastasis to the supraretrospinal recess in laryngeal squamous cell carcinoma. Ann Otol Rhinol Laryngol 2002;111: Coskun HH, Erisen L, Basut O. Selective neck dissection for clinically N0 neck in laryngeal cancer: is dissection of level IIb necessary? Otolaryngol Head Neck Surg 2004;131: Corlette TH, Cole IE, Albsoul N, Ayyash M. Neck dissection of level IIb: is it really necessary? Laryngoscope 2005;115: Silverman DA, El-Hajj M, Strome S, Esclamado RM. Prevalence of nodal metastases in the submuscular recess (level IIb) during selective neck dissection. Arch Otolaryngol Head Neck Surg 2003;129: Elsheikh MN, Mahfouz ME, Salim EI, Elsheikh EA. Molecular assessment of neck dissections supports preserving level IIB lymph nodes in selective neck dissection for laryngeal squamous cell carcinoma with a clinically negative neck. ORL J Otorhinolaryngol Relat Spec 2006;68: Lim YC, Lee JS, Koo BS, Choi EC. Level IIb lymph node metastasis in laryngeal squamous cell carcinoma. Laryngoscope 2006; 116: Villaret AB, Piazza C, Peretti G, Calabrese L, Ansarin M, Chiesa F et al. Multicentric prospective study on the prevalence of sublevel IIb metastases in head and neck cancer. Arch Otolaryngol Head Neck Surg 2007;133: Santoro R, Franchi A, Gallo O, Burali G, de Campora E. Nodal metastases at level IIb during neck dissection for head and neck cancer: clinical and pathologic evaluation. Head Neck 2008;30: Address for correspondence: Prof Dr Andreas M Sesterhenn, Department of Otolaryngology, Head and Neck Surgery, UKGM, Marburg Campus, Baldingerstrasse, Marburg, Germany Fax: sesterhe@med.uni-marburg.de Dr A Sesterhenn takes responsibility for the integrity of the content of the paper Competing interests: None declared
Accepted 11 April 2008 Published online 16 September 2008 in Wiley InterScience (www.interscience.wiley.com). DOI: /hed.
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