Accepted 11 April 2008 Published online 16 September 2008 in Wiley InterScience ( DOI: /hed.

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1 ORIGINAL ARTICLE NODAL METASTASES AT LEVEL IIb DURING NECK DISSECTION FOR HEAD AND NECK CANCER: CLINICAL AND PATHOLOGIC EVALUATION Roberto Santoro, MD, 1 Alessandro Franchi, MD, 2 Oreste Gallo, MD, 1 Giulia Burali, MD, 1 Enrico de Campora, MD 1 1 Department of Oto-Neuro-Ophtalmological Surgical Sciences, University of Florence, Florence, Italy. r.santoro@med.unifi.it or santororoberto@interfree.it 2 Department of Human Pathology and Oncology, University of Florence, Florence, Italy Accepted 11 April 2008 Published online 16 September 2008 in Wiley InterScience ( DOI: /hed Abstract: Background. Selective neck dissection as a part of an elective or therapeutic treatment of the neck is a common practice during the surgical treatment of patients with head and neck cancer. Recently, the need for routine dissection of level IIb has been discussed. The aim of this study was to verify the incidence of metastases at level IIb in patients with clinically negative necks (N0) and clinically positive necks (N1) and discuss the need for its excision. Methods. A total of 114 patients with head and neck cancer undergoing neck dissection were prospectively analyzed. The total number of neck dissections analyzed was 148. The surgical specimens from each node level of the neck were pathologically diagnosed, with special attention to level IIb. Univariate associations between N classification and IIb positive cases were assessed using logistic regression and between IIa and IIb positive cases using Fisher exact test. Results. Of 148 neck dissections performed, level IIb resulted positive in 5 cases (3.3%): 1 patient with laryngeal cancer, 1 patient with oral cavity cancer, and 2 patients with oropharyngeal cancer, of which 1 underwent bilateral neck dissection. According to clinical N classification, for N0 and N1 the incidence of positive level IIb was 2% and 5%, respectively. All the cases with metastases at level IIb also showed metastases at level IIa. A statistically significant association between the presence of nodal metastases at level IIb and those at level IIa (p Correspondence to: R. Santoro VC 2008 Wiley Periodicals, Inc. <.001) was found. The statistical association between N classification and IIb positive nodes only showed a trend toward significance (p 5.06). Conclusions. The incidence of metastases at level IIb is low, also in the N1 necks, therefore dissection of this level could be unnecessary in N0 necks. Furthermore, an interesting statistical association between the presence of metastases at level IIb and at level IIa was recorded. VC 2008 Wiley Periodicals, Inc. Head Neck 30: , 2008 Keywords: neck dissection; level IIb; head and neck cancer; pathological findings; T classification It is well known that clinical evidence of neck metastases is 1 of the most important prognostic factors in head and neck cancer. 1 Therefore, neck dissection must always be considered in the therapeutic flowchart of patients with head and neck cancer. Keeping in mind that the incidence of occult metastases is about 20% to 30%, 2 elective neck dissection for clinical negative neck (N0) has to be evaluated too. Nevertheless, the trend in recent years is to reduce the morbidity of neck dissection while maintaining the same oncological results; therefore, in our department, modified radical neck dissections and selective dissections Nodal Metastases at Level IIb HEAD & NECK DOI /hed November

2 are currently performed in positive clinical neck (N1) cases and in N0 cases, respectively. In N0 cases, node levels at higher risk for metastases in relation to the site of primary tumor are identified and only those are excised during selective dissections. 3 In this way, avoiding the excision of node levels at lower risk, the morbidity of neck surgery is reduced. In this study, we considered the nodes of level IIb (submuscular recess), whose excision, often laborious, has been frequently associated with functional shoulder complications and increased operative time. Recognition of level IIb as a distinct anatomical subsite is relatively recent, and its contents are a part of the dissection of level II; however, the incidence of metastases at this subsite is still not well characterized. The aim of this study was to verify the incidence of metastases at this level in N0 and N1 necks in patients with head and neck cancer and, consequently, to discuss the necessity to perform its excision. Table 1. Primary tumor site in patients undergoing neck dissection. Site of primary tumor T subsite Oral cavity 47 Floor of the mouth (n 5 7) Tongue (n 5 19) Retromolar trigon (n 5 8) Buccal mucosa (n 5 6) Alveolus (n 5 7) Oropharynx 17 Tonsil (n 5 7) Base of tongue (n 5 8) Soft palate (n 5 2) Hypopharynx 6 Pyriform fossa (n 5 3) Posterior wall (n 5 3) Larynx 41 Supraglottic (n 5 19) Glottic (n 5 19) Glottic-subglottic (n 5 3) Nose 2 Skin of the nose (n 5 2) Cervical esophagus 1 (n 5 1) (n 5 114) PATIENTS AND METHODS Patients treated for head and neck cancer, without any other previous treatment, who underwent neck dissection at Otorhinolaryngology Clinic of University of Florence from October 2004 to January 2007, were analyzed. Only neck dissections that included level II and had the subgroup IIb dissected, labelled, and processed separately from the main neck dissection specimen, were included in the study. The subdivision in IIa and IIb subgroups was carried out by the surgeon who performed the neck dissection. The whole content of level IIb was embedded in paraffin and from every embedding 10 sections, each being 6 lm thick, were obtained, with special attention to equatorial region of the nodes; after that, these sections were stained with hematoxylin-eosin stain and examined with an optic microscope. Also, size and number of nodes of IIb level were examined. All neck dissection specimens were submitted for definitive histopathologic analysis. In cases of bilateral neck dissections, specimens from each side were considered separately. The AJCC/UICC (American Joint Committee on Cancer/Union Internationale Contre le Cancer) TNM System (2002) was used to classify primary tumor and regional and distant metastases. Patients considered at high risk (advanced primary tumor, positive resection margin, extracapsular spread, and/or involvement of 2 or more nodes) underwent postoperative radiation therapy. Univariate associations between N classification and IIb positive cases were assessed using logistic regression test. Univariate associations between IIa and IIb positive cases were calculated using Fisher exact test. RESULTS One hundred fourteen patients were examined, 80 of which were men and 34 women; mean age was 62 years (range, years). All patients had a histopathologic diagnosis of squamous cell carcinoma of the head and neck. Thirty-four patients underwent bilateral neck dissection. The distribution of primary tumor site included: 47 oral cavity (41.2%), with 9 T1, 27 T2, 5 T3 and 6 T4; 41 larynx (35.9%), with 4 T1, 13 T2, 19 T3, 5 T4; 17 oropharynx (14.9%), with 6 T1, 8 T2, 2 T3, 1 T4; 6 hypopharynx (5.2%), with 3 T2, 2 T3 and 1 T4; 2 nose (1.7%), with 1 T2 and 1 T3; 1 cervical esophagus (0.8%), classified as T2 (Table 1). On the whole, T classification included 19 T1 (16.6%), 53 T2 (46.4%), 29 T3 (25.4%), and 13 T4 (11.4%). N classification included 66 N0 (57.8%), 23 N1 (20.1%), and 20 N2 (17.5%), with 4 N2a, 8 N2b, 8 N2c, 5 (4.3%) N3. Considering the contralateral neck dissections, 26 were clinically N0 and 8 were N1; the total number of N0 necks was 92 and the total number of N1 was 56. Sixty-eight patients (59.6%) underwent postoperative radiotherapy: 32 (28%) for T and 36 (31.5%) for N Nodal Metastases at Level IIb HEAD & NECK DOI /hed November 2008

3 Table 2. N staging and types of neck dissection performed. No. of patients N status RND SND (I, II, III) SND (II, III, IV) MRND I MRND II MRND III N N Abbreviations: RND, radical neck dissection; SND, selective neck dissection; MRND, modified radical neck dissection. Of the 148 neck dissections performed, 128 were selective neck dissections (SND), of which 66 were anterolateral and 62 supraomohyoid; 12 radical neck dissections (RND); and 8 modified radical neck dissections (MRND), 1 of type I, 2 of type II, and 5 of type III. The association between N classification and the type of neck dissection performed is summarized in Table 2. Ninety-two (62%) of 148 necks studied were clinically classified as N0, of which 2 (2%) were found to have occult nodal metastases at level IIb and other levels too, and 13 only at the other levels. Therefore, the overall number of N01 necks were 15 (16%) (Table 3). In 5 cases, extracapsular spread was documented (33% of N01): 3 at level IIa, 1 at level III, and 1 at level IV. Of the 56 necks clinically classified as N1 (38% of necks studied), only 3 (5%) revealed metastases at level IIb and at the other levels, whereas 36 were positive only at the other levels. In 10 cases (8 of the oral cavity and 2 of the larynx), therefore, clinically N1 necks were false positive (N2) (18%) (Table 4). In another 2 cases, both laryngeal cancer, the pathologic N classification was different from clinical N classification, changing in N2c and N2b from N1 and N2a, respectively. Extracapsular spread was found in 34 necks (61% of N1), corresponding to 25 patients, and in 3 cases level IIb was involved, together with the constant extracapsular spread of at least 1 node at the level IIa. The great majority of nodes with extracapsular spread were found at levels IIa and III. The mean number of the nodes found at level IIb was 5.7 (range, 1 13); in the 5 cases with positive level IIb, the number of nodes were 2 in 1 case, 4 and 6 in 2 cases, and 10 in the remaining 2 cases. Overall, the incidence of metastases at level IIb was of 3.3% (5 on 148 cases), with a level IIa positivity documented in each of these. In N0 necks, the incidence of positive level IIb when compared with all positive level IIa is 17%. According to site of primary tumor, 1 of the positive level IIb neck was from 1 patient with laryngeal cancer, 1 with oral cavity cancer, and 2 with oropharyngeal cancer, of which 1 underwent bilateral neck dissection. A statistically significant association between the presence of nodal metastases at level IIb and the presence of metastases at level IIa (p <.001) was found. On the other hand, the statistical association between N class and IIb positive nodes is not significant, but shows only a trend to a significant correlation (p 5.06). Table 5 shows positive level IIb cases. DISCUSSION Selective neck dissection is the worldwide treatment of choice for clinically N0 necks in patients with head and neck cancer, considering that we can now identify node levels at higher risk of metastases in relation to the primary site of the tumor. 3 6 This type of neck dissection is useful not only as a staging procedure, but also for the treatment of occult node metastases. Functional results are not so good, mainly because of a postoperative shoulder dysfunction in most of cases Shoulder dysfunction is due to traction injury Table 3. Tumor site, clinically N0 necks and pathologic N01 and neck levels. Tumor site N0 necks N0 1 Level I 1 Level IIa 1 Level IIb 1 Level III 1 Level IV 1 Level V 1 Oral cavity Oropharynx Hypopharynx Larynx Esophagus Nodal Metastases at Level IIb HEAD & NECK DOI /hed November

4 Table 4. Tumor site and clinically N 1 necks. Tumor site N1 N 1 other levels False positive Level I 1 Level IIa 1 Level IIb 1 Level III 1 Level IV 1 Level V 1 Oral cavity Oropharynx Hypopharynx Larynx Nose and interruption of blood supply to the spinal nerve during dissection of level IIb. Avoiding the dissection of this level, therefore, should help to minimize this complication, but its oncological effectiveness is still controversial. Koybasioglu et al 14 analyzed the incidence of metastases at level IIb in patients with laryngeal cancer and did not report any case of metastases at this subsite. In a similar study, 15 others reported only 4 metastases at level IIb out of 102 neck dissections. Chone et al 12 have found metastases at this level with an incidence of 2.3% for N0 necks and 16.7% for N1 necks. Other authors 11,16 observed metastases at level IIb in patients affected by cancer of the oral cavity with a range of incidence from 2% to 3%. Silverman 17 reported an incidence of metastases at level IIb of 1.6% for N0 necks, 1.1% for N1 cases, and a total incidence of 4.4% of cases. In our study, the incidence of micrometastases at level IIb was 2% for clinically N0 necks, similar to those reported in literature. Therefore, the low incidence suggests the possibility to avoid dissection of level IIb during selective neck dissection. The total incidence of N01 was 16%, in a range that justifies the treatment with a selective neck dissection. 18 Furthermore, no micrometastases at level IV were observed among N0 patients with laryngeal cancer, and only 1 metastases was found among N1 patients (on the contrary, level III showed a low incidence of occult metastases, but there is a Table 5. Neck dissection in 5 level llb1 cases. Case no. Tumor site ctnm ptnm IIb1/total IIb N 1 Larynx T3N0M0 T3N1M0 2 on 10 lt N 2 Oropharynx* T3N3M0 T3N3M0 1 on 2 rt N 3 Oropharynx* T3N3M0 T3N3M0 2 on 10 lt N 4 Oropharynx T1N0M0 T1N1M0 3 on 6 lt N 5 Oral cavity T2N2bM0 T2N2bM0 2 on 4 lt *Bilateral neck dissection in the same patient. high incidence of metastases in N1 necks). Results from our study suggest further considerations, in agreement with recent reports in literature, 19 about the opportunity of performing a dissection of level IV in clinically N0 necks of patients with laryngeal cancer. In clinically N1 necks, the incidence of metastases at level IIb was of 5% of cases, slightly higher than the incidence in N0 necks, but lower than the incidences reported in other studies. 11,12,16,17 This incidence underlines the low prevalence of the metastases at level IIb. Moreover, it is interesting to observe the high incidence (18%) of false-positive cases in clinically N1 necks, highlighting the limits of clinical examination and of imaging. Fine-needle aspiration cytology of suspected nodes could increase the accuracy of clinical staging, helping in planning a proper neck dissection. 20 The total incidence of metastases at level IIb was of 3.3% of cases, and there was a constant association with involvement of the level IIa nodes, in agreement with other studies. 17 The mean number of nodes of the level IIb was in a range similar to those reported in other articles. 21 In conclusion, the results of the present study suggest that the dissection of level IIb in clinically N0 necks need not be necessary, keeping in mind that, in our study, we found a significant statistical association between the presence of metastases at level IIb and the presence of metastases at level IIa. For this reason, some authors 17 suggest use of frozen section analysis at level IIa during neck dissection, but, in our opinion, this procedure is not so accurate in detecting occult node metastases. In some reports, 17,12 the authors found a statistically significant association between the metastases at level IIb and advanced N class, in particular with positive level IIa, as well as the presence of extracapsular spread. On the contrary, in our study we only found a statistically significant trend between N classification and positive level Ilb (p ). Further studies with a 1486 Nodal Metastases at Level IIb HEAD & NECK DOI /hed November 2008

5 larger number of cases with positive level IIb will be necessary to recognize the potential risk factors of metastases at this subsite. REFERENCES 1. Kramer S, Marcial VA, Pajak TF, Maclean CJ, Davis LW. Prognostic factors for locoregional control and metastasis and the impact on survival. Int J Radiat Oncol Biol Phis 1986;12: 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 patient with squamous cell carcinoma of the upper respiratory and digestive tracts. Arch Otolaryngol Head Neck Surg 1998;124: Shah JP. The patterns of cervical lymph node metastases from squamous carcinoma of the upper aerodigestive tract. Am J Sur 1990;160: Robbins KT, Clayman G, Levine PA, et al. Neck dissection classification update. Arch Otolaryngol Head Neck Surg 2002;128: Jones AS, Roland NJ, Field JK. The level of cervical lymph node metastases: their prognostic relevance and relationship with head and neck squamous carcinoma primary sites. Clin Otolaryngol 1994;19: Ferlito A, Buckley JG, Shaha AR. Rationale for selective neck dissection in tumors of upper aerodigestive tract. Acta Otolaryngol 2001;121: Talmi YP, Horowitz Z, Pfeffer MR, et al. Pain in the neck after neck dissection. Otolaryngol Head Neck Surg 2000;123: Leipzig B, Suen JY, English JL, Barnes J, Hooper M. Functional evaluation of the spinal accessori nerve after neck dissection. Am J Surg 1983;146: Cheng PT, Hao SP, Lin YH, Yeh AR. Objective comparison of shoulder dysfunction after three neck dissection techniques. Ann Otol Rhinol Laryngol 2000;109(Part 1): Sobol S, Jensen C, Sawyer W II, Costiloe P, Thong N. Objective Comparison of physical dysfunction after neck dissection. Am J Surg 1985;150: Kraus DH, Rosenberg DB, Davidson BJ, et al. Supraspinal accessory Lymph node metastases in supraomohyoid neck dissection. Am J Surg 1996;172: Chone CT, Crespo AN, Rezende AS, Carvalho DS, Altemani A. Neck lymph node metastases to the posterior triangle: evaluation of clinical and histopatological risk factors. Head Neck 2000;22: Koybasioglu A, Tokcaer AB, Uslu S. Accessory nerve function after modified radical and lateral neck dissections. Laryngoscope 2000;110: Koybasioglu A, Uslu S, Yilmaz M. Linfatic metastases to the supraretrospinal recess in laryngeal squamous cell carcinoma. Ann Otol Rhinol Laryngol 2002;111: Talmi YP, Hoffman H, Hrowitz Z. Patterns of metastases to the upper jugular lymph nodes (the submuscular recess). Head Neck 1998;20: Lim YC, Song MH, Kim SC, Kim KM, Choi EC. Preserving level IIb lymph nodes in elective supraomohyoid neck dissection for oral cavity squamous cell carcinoma. Arch Otolaryngol Head Neck Surg 2004;130: Silverman DA, El-Hajj M, Strome S. Prevalence of nodal metastases in the submuscolar recess(level IIb) during selective neck dissection. Arch Otolaryngol Head Neck Surg 2003;129: Weiss MH, Harrison LB, Isaacs RS. Use of decision analysis in planning a management strategy for the stage N0 neck. Arch Otolaryngol Hed Neck Surg 1994;120: Khafif A, Fliss DM, Gil Z, Medina JE. Routine inclusion of level IV in neck dissection for squamous cell carcinoma of the larynx: is it justified? Head Neck 2004;26: Van del Brekel MWM, Stel HV, Castelijns JA. Lymph node staging in patient with clinical negative neck examination by ultrasound and ultrasound-guided aspiration cytology. Am J Surg 1991;162: 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: Nodal Metastases at Level IIb HEAD & NECK DOI /hed November